Publications

# Equal contribution  * Co-corresponding authors

 

Preprints


Visualizing chaperone-mediated multistep assembly of the human 20S proteasome
Adolf F#*, Du J#, Goodall EA, Walsh jr RM, Rawson S, von Gronau S, Harper JW, Hanna J*, Schulman BA*
bioRxiv 2024.01.27.577538. https://doi.org/10.1101/2024.01.27.577538

 

2024


Skraban-Deardorff intellectual disability syndrome-associated mutations in WDR26 impair CTLH E3 complex assembly
Gross A, Müller J, Chrustowicz J, Strasser A, Gottemukkala KV, Sherpa D, Schulman BA, Murray PJ*, Alpi AF*
FEBS Letters.  https://doi.org/10.1002/1873-3468.14866

Combinatorial selective ER-phagy remodels the ER during neurogenesis
Hoyer MJ, Capitanio C#, Smith IR#, Paoli JC, Bieber A, Jiang Y, Paulo JA, Gonzalez-Lozano MA, Baumeister W, Wilfling F, Schulman BA, Harper JW
Nat Cell Biol. https://doi.org/10.1038/s41556-024-01356-4 (cover)
> News & Views: Molinari M. 2024 ER remodelling by ER-phagy in neurogenesis Nat Cell Biol. https://doi.org/10.1038/s41556-024-01362-6

Cullin-RING ligases employ geometrically optimized catalytic partners for substrate targeting
Li J#, Purser N#, Liwocha J#, Scott DC#, Byers HA, Steigenberger B, Hill S, Tripathi-Giesgen I, Hinkle T, Hansen FM, Prabu RJ, Radhakrishnan SK, Kirkpatrick DS, Reichermeier KM, Schulman BA* & Kleiger G*
Mol Cell. 2024. https://doi.org/10.1016/j.molcel.2024.01.022

Mechanism of millisecond Lys48-linked poly-ubiquitin chain formation by cullin-RING ligases
Liwocha J#, Li J#, Purser N#, Rattanasopa C, Maiwald S, Krist DT, Scott DC, Steigenberger B, Prabu RJ, Schulman BA* & Kleiger G*
Nat Struct Mol Biol. 2024. https://doi.org/10.1038/s41594-023-01206-1

Multisite phosphorylation dictates selective E2-E3 pairing as revealed by Ubc8/UBE2H-GID/CTLH assemblies
Chrustowicz J#, Sherpa D#, Li J, Langlois CR, Papadopoulou EC, Vu DT, Hehl LA, Karayel Ö, Beier V, von Gronau S, Müller J, Prabu JR, Mann M, Kleiger G, Alpi AF, Schulman BA
Mol Cell. 2024 Jan 18;84(2):293-308. https://doi.org/10.1016/j.molcel.2023.11.027

DOA10/MARCH6 architecture interconnects E3 ligase activity with lipid-binding transmembrane channel to regulate SQLE
Botsch JJ, Junker R, Sorgenfrei M, Ogger PP, Stier L, von Gronau S, Murray P, Seeger MA, Schulman BA*, Bräuning B*
Nat Commun. 2024 Jan 9;15(1):410. https://doi.org/10.1038/s41467-023-44670-5

Recovering from stress during pandemic
Lewis SC, Jourdain AA, R Schulman BA, Vousden KH,  Fabius JM, Liu H
Mol Cell. 2024 Jan 4;84(1):8-11. https://doi.org/10.1016/j.molcel.2023.11.013 (invited commentary)

 

2023


K6-linked ubiquitylation marks formaldehyde-induced RNA-protein crosslinks for resolution
Suryo Rahmanto AS, Blum CJ, Scalera C, Heidelberger JB, Mesitov M, Horn-Ghetko D, Gräf JF, Mikicic I, Hobrecht R, Orekhova A, Ostermaier M, Ebersberger S, Möckel MM; Krapoth N, Da Silva Fernandes N, Mizi A, Zhu Y, Chen JX, Choudhary C, Papantonis A, Ulrich HD, Schulman BA, König J, Beli P
Mol Cell. 2023 Dec 7;83(23), 4272-4289 e4210. https://doi.org/10.1016/j.molcel.2023.10.011

Insights into the ISG15 transfer cascade by the UBE1L activating enzyme
Wallace I, Baek K, Prabu JR, Vollrath R, von Gronau S, Schulman BA*, Swatek KN*
Nat Commun. 2023 Dec 2;14(1); 7970. https://doi.org/10.1038/s41467-023-43711-3
> News & Views: Serrano I (2024) Structural insights into the specific recognition and transfer of ISG15. Nat Struct Mol Biol 31, 214. https://doi.org/10.1038/s41594-024-01226-5

Catalysis of non-canonical protein ubiquitylation by the ARIH1 ubiquitin ligase
Purser N, Tripathi-Giesgen I, Li J, Scott DC, Horn-Ghetko D, Baek K, Schulman BA, Alpi A, Kleiger G
Biochem J. 2023 Nov 29;480(22): 1817-1831. https://doi.org/10.1042/BCJ20230373

 Activity-based profiling cullin-RING ligase networks by conformation-specific probes
Henneberg LT#, Singh J#, Duda DM#, Baek K, Yanishevski D, Murray PJ, Mann M, Sidhu SS*, Schulman BA*
Nat Chem Biol. 2023 Aug 31;19(12): 1513-1523. https://doi.org/10.1038/s41589-023-01392-5
> News & Views: Parui AL, Walden H (2023) Hunting down the shapeshifters. Nat Chem Biol. 19(12):1438-1439. https://doi.org/10.1038/s41589-023-01407-1

Structural snapshots along K48-linked ubiquitin chain formation by the HECT E3 UBR5
Hehl LA, Horn-Ghetko D, Prabu JR, Vollrath R, Tung Vu D, Perrez Berrocal DA, Mulder MPC, van der Heden van Noort GJ, Schulman BA
Nat Chem Biol. 2023 Aug 24;20, 190–200. https://doi.org/10.1038/s41589-023-01414-2
> Forum - Special Issue: Targeted protein degradation: Taherbhoy AM, Daniels DL (2023) Harnessing UBR5 for targeted protein degradation of key transcriptional regulators. Trends in Pharmacological Sciences 44 (11), 758-761. https://doi.org/10.1016/j.tips.2023.09.001

A Pro-fluorescent Ubiquitin based probe to monitor cysteine-based E3 ligase activity
Perez Berrocal DA, Vishwanatha TM, Horn-Ghetko D, Botsch JJ, Hehl LA, KostrhonS, Misra M, Dikic I, Geurink PP, van Dam H, Schulman BA, Mulder MPC 
Angew Chem Int Ed Eng 2023 Aug 7;63(32): e202303319. https://doi.org/10.1002/anie.202303319

To be (in a transcriptional complex) or  not to be (promoting UBR5 ubiquitylation): That is an answer to how degradation controls gene expression
Hehl LA, Schulman BA
Mol Cell. 2023 Aug 3;83(15):2616-2618. https://doi.org/10.1016/j.molcel.2023.07.010

PARK15/FBXO7 is dispensable for PINKI/Parkin mitophagy in iNeurons and HeLa cell systems
Kraus F, Goodall EA, Smith ER, Jiang Y, Paoli JC, Adolf F, Paulo JA, Schulman BA, Harper JW
EMBO Rep. 2023 Aug 3;24(8): e56399. https://doi.org/10.15252/embr.202256399

Ubiquitination regulates ER-phagy and remodelling of endoplasmatic reticulum
Gonzalez A, Covarrubias-Pinto A, Bhaskara RM, Glogger M, Kuncha SK, Xavier A, Seemann E, Misra M, Hoffmann ME, Bräuning B, Balakrishnan A, Qualmann B, Dötsch V, Schulman BA, Kessels MM, Hübner CA, Heilemann M, Hummer G, Dikic I
Nature 2023 Jun;618(7964):394-401. https://doi.org/10.1038/s41586-023-06089-2

Systemwide disassembly and assembly of SCF ubiquitin ligase complexes
Baek K, Scott DC, Henneberg LT, King MT, Mann M, Schulman BA
Cell 2023 Apr 27; 186( 9):1895-1911. https://doi.org/10.1016/j.cell.2023.02.035
> Preview: Xie Y, Minglei Z (2023) CAND1 orchestrates CRLs through rock and roll. Cell. 186(9):1817-1818. https://doi.org/10.1016/j.cell.2023.04.001
> Research Highlight: Garcia SF, Pagano M (2023) How “rock-and-roll” solved the cullin supply chain problem. Cell Res. 33:741-742. https://doi.org/10.1038/s41422-023-00825-z

An expanded lexicon for the ubiquitin code
Dikic I* and Schulman BA*
Nat Rev Mol Cell Biol 2023 Apr;24(4) ;273-287. https://doi.org/10.1038/s41580-022-00543-1 (invited review)

In situ snapshots along a mammalian selective autophagy pathway
Li M, Tripathi-Giesgen I, Schulman BA, Baumeister W, Wilfling F
Proc Natl Acad Sci USA. 2023 Mar21;120(12):e2221712120. https://doi.org/10.1073/pnas.2221712120

E3 ligase autoinhibition by C-degron mimicry maintains C-degron substrate fidelity
Scott DC, King MT, Baek K, Gee CT, Kalathur R, Li J, Purset N, Nourse A, Chai SC, Vaithiyalingam S, Chen T, Lee RE, Elledge SJ, Kleiger G, Schulman BA
Mol Cell. 2023 Feb 16;83(5), 770-786 e779. https://doi.org/10.1016/j.molcel.2023.01.019
> Research Highlight: Heinke L (2023) C-degron mimicry confers E3 ligase selectivity. Nat Rev Mol Cell Biol. 24, 241. https://doi.org/10.1038/s41580-023-00597-9

A central role for regulated protein stability in the control of TFE3 and MITF by nutrients
Nardone C, Palanski BA, Scott DC, Timms RT,  Barber KW, Gu X, Mao A, Leng Y, Watson EV, Schulman BA, Cole PA, Elledge SJ
Mol Cell. 2023 Jan 5;83(1):57-73 e59. https://doi.org/10.1016/j.molcel.2022.12.013

 

2022


  Modular UBE2H-CTLH E2-E3 complexes regulate erythroid maturation
Sherpa D, Müller J, Karayel O, Chrustowicz J, Xu P, Gottemukkala KV, Baumann C, Gross A, Czarneki O, Zhang W, Gu J, Nilvebrant J, Weiss MJ, Sidhu SS, Murray PJ, Mann M, Schulman BA, Alpi A
elife. 2022 Dec 2;11:e77937. https://doi.org/10.7554/eLife.77937

In situ structural analysis reveals membrane shape transitions during autophagosome formation
Bieber A#, Capitanio C#, Erdmann PS*, Fiedler F, Beck F, Lee CW, Li D, Hummer G, Schulman BA*, Baumeister W*, Wilfling F*
Proc Natl Acad Sci USA 2022 Sep 27;119(39):2209823119. https://doi.org/10.1073/pnas.2209823119

Structure of CRL7FBXW8 reveals coupling with CUL1-RBX1/ROC1 for multi-cullin-RING E3 catalyzed ubiquitin ligation
Hopf L, Baek K, Klügel M, von Gronau S, Xiong Y, Schulman BA
Nat Struct Mol Biol 2022 Aug 18. https://doi.org/10.1038/s41594-022-00815-6

Cryo-EM structures of Gid12-bound GID E3 reveal steric blockade as  a mechanism inhibiting substarte ubiquitylation
Qiao S, Lee CW, Sherpa D, Chrustowicz J, Cheng J, Duennebacke M, Steigenberger B,, Karayel O, Vu DT, von Gronau S, Mann M, Wilfling F, Schulman BA
Nat Commun. 2022 Jun 1;13(1):3041. https://doi.org/10.1038/s41467-022-30803-9

The structural context of PTMs at a proteome wide scale
Bludau I, Willems S, Zeng WF, Strauss MT, Hansen FM Tanzer MC, Karayel O,  Schulman BA, Mann M
PLOS Biol. 2022 May 16;20(5):e3001636. https://doi.org/10.1371/journal.pbio.3001636

GID E3 ligase assembly ubiquitinates an Rsp5 E3 adaptor and regulates plasma membrane transporters
Langlois CR*, Beier V, Karayel O, Chrustowicz J, Sherpa D, Mann M, Schulman BA*
EMBO Rep 2022 Apr 19;23: e53835. https://doi.org/10.15252/embr.202153835

How the ends signal the end: Regulation by E3 ubiquitin ligases recognizing protein termini
Sherpa D, Chrustowicz J, Schulman BA
Mol Cell. 2022 Apr 21;82(8), 1424-1438. https://doi.org/10.1016/j.molcel.2022.02.004 (invited review)

New classes of E3 ligases illuminated by chemical probes
Horn-Ghetko D, Schulman BA
Curr Opin Struct Biol. 2022 Feb 24;73:102341. https://doi.org/10.1016/j.sbi.2022.102341 (invited review)

Targeted protein degradation: from small molecules to complex organelles - a Keystone Symposia report
Cable J, Weber-Ban E, Clausen T, Walters KJ, Sharon M, Finley DJ, Gu Y, Hanna J, Feng Y, Martens S, Hansen M, Zhang H, Goodwin JM, Reggio A, Chang C, Ge L, , Schulman BA, Deshaies RJ, Dikic I, Harper JW, Wertz IE, Thomä NH, Stabicki M, Frydman J, Jakob U, David DC, Bennet EJ, Bertozzi CR, Sardana R, Eapen VV, Carra S
Ann N Y Acad  Sci 2022. Jan 8;1510(1), 79-99. https://doi.org/10.1111/nyas.14745

Multifaceted N-degron recognition and ubiquitylation by GID/CTLH E3 Ligases
Chrustowicz J, Sherpa D, Teyra J, Loke MS, Popowicz GM, Basquin J, Sattler M, Prabu JR, Sidhu SS, Schulman BA
J Mol Biol. 2022 Jan 30;434 (2):167347. https://doi.org/10.1016/j.jmb.2021.167347

APC7 mediates ubiquitin signaling in constitutive heterochromatin in the developing mammalian brain
Ferguson CJ, Urso O, Bodrug T, Gassaway BM, Watson ER, Prabu JR, Lara-Gonzalez P, Martinez-Jacin RC, Wu DY, Brigatti KW, Puffenberger EG, Taylor CM, Haas-Givler B, Jinks RN, Strauss KA, Desai A, Gabel HW, Gygi SP, Schulman BA, Brown NG, Bonni A.
Mol Cell.2022 Jan 6;82(1):90-105.e113. https://doi.org/10.1016/j.molcel.2021.11.031

 

2021


CUL5-ARIH2 E3-E3 ubiquitin ligase structure reveals cullin-specific NEDD8 activation
Kostrhon S, Prabu JR, Baek K, Horn-Ghetko D, von Gronau S, Klügel M, Basquin J, Alpi AF, Schulman BA
Nat Chem Biol. 2021 Oct;17(10): 1075-1083.  https://doi.org/10.1038/s41589-021-00858-8

Host ubiquitin protein tags lipid to fight bacteria
Schulman BA, Harper JW
Nature. 2021 Jun;594(7861):28-29.  https://doi.org/10.1038/d41586-021-01267-6 (invited commentary)

NEDD8 and ubiquitin ligation by cullin-RING E3 ligases
Baek K, Scott CD, Schulman BA
Curr Opin Struct Biol. 2021 Apr;(67):101-109.  https://doi.org/10.1016/j.sbi.2020.10.007 (invited review)

Improvement of oral bioavailability of Pyrazolo Pyridone inhibitors of the interaction of DCN1/2 and UBE2M
Kim HS, Hammil JT, Scott CD, Chen Y, Rice AL, Pistel W, Singh B, Schulman BA, Guy RK
J Med Chem. 2021 May 13;64(9):5850-5862. https://doi.org/10.1021/acs.jmedchem.1c00035

 GID E3 ligase supramolecular chelate aasembly configures multipronged ubiquitin targeting of an oligomeric metabolic enzyme
Sherpa D#, Chrustowicz J#, Qiao S, Langlois CR, Hehl LA, Gottemukkala KV, Hansen FM, Karayel O, von Gronau S, Prabu JR, Mann M, Alpi AF, Schulman BA
Mol Cell. 2021 Jun 3;81(11):2445-2459. https://doi.org/10.1016/j.molcel.2021.03.025
> Preview: Fechter L, Pfirrmann T (2021) The GID ubiquitin ligase complex just reached the next level of complexity. Mol Cell 81(11):2270-2. https://doi.org/10.1016/j.molcel.2021.05.003

Decoding the messaging of the ubiquitin system using chemical and protein probes
Henneberg L, Schulman BA
Cell Chem Biol. 2021 Jul 15;28(7):889-902.  https://doi.org/10.1016/j.chembiol.2021.03.009 (invited review)

Cullin RING ubiquitin ligase regulatory circuits: a quartercentury beyond the F-box hypthesis
Harper W, Schulman BA
Annu Rev Biochem. 2021 Jun 20;90:403-429. https://doi.org/10.1146/annurev-biochem-090120-013613 (invited review)

Linkage-specific ubiquitin chain formation depends on a Lysine hydrocarbon ruler
Liwocha J#, Krist DT#, van der Heden van Nort GJ#, Hansen FM, Truong VH, Karayel O, Purser N, Houston D, Burton N  Bostock MJ, Sattler M, Mann M, Harrison JS, Kleiger G*, Ovaa H*, Schulman BA*
Nat Chem Biol. 2021 Mar 17;3:272-279.  https://doi.org/10.1038/s41589-020-00696-0

The UBA domain of conjugating enzyme Ubc1/Ube2K facilitates assembly of K48/K63-branched ubiquitin chains
Pluska L, Jarosch E, Zauber H, Kniss A, Waltho A, Bagola K, von Delbrück M, Löhr F, Schulman BA, Selbach M, Dötsch V, Sommer T
EMBO J. 2021 Mar 15;40(6):e106094.  https://doi.org/10.15252/embj.2020106094

The IMiD target CRBN determines HSP90 activity toward transmembrane proteins essential in multiple myeloma
Heider M, Eichner R, Stroh J, Morath V, Kuisl A, Zecha J, Lawatscheck J, Baek K, Garz AK, Rudelius M, Deuschle FC, Keller U, Lemeer S, Verbeek M, Götze KS, Skerra A, Weber WA, Buchner J,  Schulman BA, Kuster B, Fernandez-Saiz V, Bassermann F
Mol Cell. 2021 Mar 18; 81(6):1170-1186.  https://doi.org/10.1016/j.molcel.2020.12.046 (cover)

Ubiquitin ligation to F-box protein targets by SCF-RBRE3-E3 super-assembly
Horn-Ghetko D, Krist DT, Prabu RJ, Baek K, Mulder MPC, Klügel M, Scott DC, Ovaa H, Kleiger G, Schulman BA
Nature. 2021 Feb;590(7847):671-676.  https://doi.org/10.1038/s41586-021-03197-9

Data-independent acquisition method for ubiquitinome analysis reveals regulation of circadian biology
Hansen FM, Tanzer MC, Brüning F, Bludau I, Schulman BA, Robles MS, Karayel O, Mann M
Nat Commun. 2021 Jan 11;12(1):254. https://doi.org/10.1038/s41467-020-20509-1

FBX011-mediatedproteolysis of BAHD1 relieves PRC2 dependent transcriptional repression in erythropoesis
Xu P, Scott DC, Xu B, Yao Y, Feng R, Cheng L, Mayberry K, Bi W, Palmer LE, King MT, Wang H, Li Y, Fan Y, Alpi AF, Li C, Peng J, Papizan J, Pruett-Miller SM, Spallek R, Bassermann F, Cheng Y, Schulman BA, Weiss MJ
Blood. 2021 Jan 14;137(2):155-167. https://doi.org/10.1182/blood.2020007809

 

2020


DIA-based systems biology approach unveils novel E3-dependent responses to a metabolic shift
Karayel O, Michaelis AC, Mann M*, Schulman BA*, Langlois CR*
Proc Natl Acad Sci USA. 2020 Dec 22;117(51):32806-32815. https://doi.org/10.1073/pnas.2020197117

A selective autophagy pathway for phase separated endocytic protein deposits
Wilfling F, Lee C-W, Erdmaann P, Zheng Y, Sherpa D, Jentsch S, Pfander B, Schulman BA, Baumeister W
Mol Cell. 2020 Dec3 80(5):764-778. https://doi.org/10.1016/j.molcel.2020.10.030
> Preview: Makar AN, Gammoh N (2020) Autophagy Brings an END to Aberrant Endocytosis. Mol Cell. 80(5):758-759. https://doi.org/10.1016/j.molcel.2020.11.020

Integrative proteomics reveals principles of dynamic phospho-signaling networks in human erythropoiesis
Karayel O, Xu P, Bludau I, Bhoopalan SV, Yao Y, Colaco ARF, Delgado AS, Schulman BA*, Alpi AF*, Weiss MJ*, Mann M*
Mol Syst Biol. 2020 Dec;16(12)e9813. https://doi.org/10.15252/msb.20209813

Structural and mechanistic basis of the EMC-dependent biogenesis of distinct transmembrane clients
Miller-Vedam LE#, Bräuning B#, Popova KD#, Schirle Oakdale NT, Bonnar JL, Prabu JR, Boydston EA, Sevillano N, Shurtleff MJ, Craik JS, Schulman BA*, Frost A*, Weissman JS*
Elife 2020 Nov 25;9:e62611. https://doi.org/10.7554/elife.62611

Papain-like protease regulates SARS-CoV-2 viral spread and innate immunity
Shin D, Mukherjee R, Grewe D, Bojkova D, Baek K, Bhattacharya A, Schulz L, Widera M, Mehdipour AR, Tascher G, Geurink PP, Wilhelm A, van der Heden  van Noort GJ, Ovaa H, Müller S, Knobeloch KP, Rajalingam K, Schulman BA, Cinatl J, Hummer G, Ciesek S, Dikic I
Nature. 2020 Nov 587(7835):657-662. https://doi.org/10.1038/s41586-020-2601-5

E3-mediated Ubiquitin and Ubiquitin-like Protein Ligation: Mechanisms and Chemical Probes
Krist DT* and Schulman BA*
In Protein Degradation with New Chemical Modalities, H. Weinmann, and C. Crews, eds. (The Royal Society of Chemistry), pp. 0. 10.1039/9781839160691-00184. https://doi.org/10.1039/9781839160691-00184 (invited book chapter)

 Gene expression and cell identity controlled by anaphase-promoting complex
Oh E, Mark KG, Mocciaro A, Watson ER, Prabu JR, Cha DD, Kampmann M, Gamarra N, Rape M
Nature. 2020 579(7797):136-140. https://doi.org/10.1038/s41586-020-2034-1

Quantifying the heterogeneity of macromolecular machines by mass photometry
Sonn-Segev A, Belacic K, Bodrug T, Young G, VanderLinden RT, Schulman BA, SchimpfJ, Friedrich T, Dip PV Schwartz TU, Bauer B, Peters JM, Struw WB, Benesch JLP, Brown NG, Haselbach D, Kukura P
Nat Commun 2020 Apr 14;11(1):1772. https://doi.org/10.1038/s41467-020-15642-w

Paradoxical mitotic exit induced by a small molecule inhibitor of APC/CCdc20  
Richeson KV, Bodrug T, Sackton KL, Yamaguchi M, Paulo JA, Gygi SP, Schulman BA, Brown NG, King RW
Nat Chem Biol. 2020 May;16(5):546-555. https://doi.org/10.1038/s41589-020-0495-z

NEDD8 nucleates a multivalent cullin-RING-UBE2D ubiquitin ligation assembly
Baek K, Krist DT, Prabu JR, Hill S, Klügel M, Neumaier L-M, von Gronau S, Kleiger G, Schulman BA
Nature.  2020 Feb;578(7795):461-466. https://doi.org/10.1038/s41586-020-2000-y
> News & Views: Deshaies RJ, Pierce NW (2020) Transfer of ubiquitin protein caught in act. Nature. 578, 372-373. https://doi.org/10.1038/d41586-020-00325-9

Molecular glue concept solidifies
Baek K, Schulman BA
Nat Chem Biol.  2020 Jan;16(1): 2-3. https://doi.org/10.1038/s41589-019-0414-3

Allosteric regulation through a switch element in the autophagy E2, Atg3
Qiu Y, Zheng Y, Grace CRR, Liu X, Klionsky DJ, Schulman BA
Autophagy.  2020 Jan;16(1):183-184. https://doi.org/10.1080/15548627.2019.1688550

Interconversion between Anticipatory and Active GID E3 Ubiquitin Ligase Conformations via Metabolically Driven Substrate Receptor Assembly
Qiao S, Langlois CR#, Chrustowicz J#, Sherpa D#, Karayel O, Hansen FM, Beier V, von Gronau S, Bollschweiler D, Schäfer T, Alpi AF, Mann M, Prabu JR, Schulman BA
Mol Cell. 2020 Jan 2;77(1):150-163.e9.  https://doi.org/10.1016/j.molcel.2019.10.009

 

2019


Robust cullin-RING ligase function is established by a multiplicity of poly-ubiquitylation pathways
Hill S, Reichermeier K, Scott DC, Samentar L, Coulombe-Huntington J, Izzi L, Tang X, Ibarra R, Bertomeu T, Moradian A, Sweredoski MJ, Caberoy N, Schulman BA, Sicheri F, Tyers M, Kleiger G
Elife. 2019 Dec 23;8:e51163. https://doi.org/10.7554/elife.51163

Discovery of Novel Pyrazolo-pyridone DCN1 Inhibitors Controlling Cullin Neddylation
Kim HS, Hammill JT, Scott DC, Chen Y, Min J, Rector J, Singh B, Schulman BA, Guy RK. 
J Med Chem. 2019 Sep 26;62(18):8429-8442. https://doi.org/10.1021/acs.jmedchem.9b00410

Protein engineering of a ubiquitin-variant inhibitor of APC/C identifies a cryptic K48 ubiquitin chain binding site
Watson ER, Grace CRR, Zhang W, Miller DJ, Davidson IF, Prabu JR, Yu S, Bolhuis DL, Kulko ET, Vollrath R, Haselbach D, Stark H, Peters JM, Brown NG, Sidhu SS, Schulman BA
Proc Natl Acad Sci USA. 2019 Aug 27;116(35):17280-17289. https://doi.org/10.1073/pnas.1902889116
> Commentary: Walters KJ (2019) Ubiquitin in disguise unveils a cryptic binding site in 1.2-MDa anaphase-promoting complex/cyclosome. Proc Natl Acad Sci USA. 116(35) 17142-17144. https://doi.org/10.1073/pnas.1911388116

A switch element in the autophagy E2 Atg3 mediates allosteric regulation across the lipidation cascade
Zheng Y#, Qiu Y#, Grace CRR, Liu X, Klionsky DJ, Schulman BA
Nat Commun. 2019 Aug 9;10(1):3600. https://doi.org/10.1038/s41467-019-11435-y

ARIH2 is a Vif-dependent regulator of CUL5-mediated APOBEC3G degradation in HIV infection
Hüttenhain R, Xu J, Burton LA, Gordon D, Hultquist JF, Johnson JR, Satkamp L, Hiatt J, Rhee DY, Baek K, Crosby DC, Frankel AD, Marson A, Harper WJ, Alpi AF, Schulman BA, Gross JD, Krogan NJ
Cell Host and Microbe. 2019 Jul 10;26(1):86-99. https://doi.org/10.1016/j.chom.2019.05.008

Posing the APC/C E3 Ubiquitin Ligase to Orchestrate Cell Division
Watson ER, Brown NG, Peters JM, Stark H, Schulman BA
Trends Cell Biol. 2019 Feb 29;(2):117-134. https://doi.org/10.1016/j.tcb.2018.09.007

Dual-color pulse-chase ubiquitination assays to simultaneously monitor substrate priming and extension
Scott DC, Schulman BA
Methods Enzymol. 2019 Feb 11;618:29-48. https://doi.org/10.1016/bs.mie.2019.01.004

 

2018


Cancer Mutations of the Tumor Suppressor SPOP Disrupt the Formation of Active, Phase-Separated Compartments
Bouchard JJ, Otero JH, Scott DC, Szulc E, Martin EW, Sabri N, Granata D, Marzahn MR, Lindorff-Larsen K, Salvatella X, Schulman BA, Mittag T
Mol Cell. 2018 Oct 4;72(1):19-36. https://doi.org/10.1016/j.molcel.2018.08.027

Piperidinyl Ureas Chemically Control Defective in Cullin Neddylation 1 (DCN1)-Mediated Cullin Neddylation
Hammill JT, Scott DC, Min J, Connelly MC, Holbrook G, Zhu F, Matheny A, Yang L, Singh B, Schulman BA, Guy RK. J
Med Chem. 2018 Apr 12;61(7):2680-2693. https://doi.org/10.1021/acs.jmedchem.7b01277

Discovery of an Orally Bioavailable Inhibitor of Defective in Cullin Neddylation 1 (DCN1)-Mediated Cullin Neddylation
Hammill JT, Bhasin D, Scott DC, Min J, Chen Y, Lu Y, Yang L, Kim HS, Connelly MC, Hammill C, Holbrook G, Jeffries C, Singh B, Schulman BA, Guy RK
J Med Chem. 2018 Apr 12;61(7):2694-2706. https://doi.org/10.1021/acs.jmedchem.7b01282

SCF E3 Ligase Substrates Switch from CAN-D to Can-ubiquitylate
Scott DC, Schulman BA
Mol Cell. 2018 Mar 1;69(5):721-723. https://doi.org/10.1016/j.molcel.2018.02.019 (invited commentary)

 

2017


Blocking an N-terminal acetylation-dependent protein interaction inhibits an E3 ligase
Scott DC#, Hammill JT#, Min J, Rhee DY, Connelly M, Sviderskiy VO, Bhasin D, Chen Y, Ong SS, Chai SC, Goktug AN, Huang G, Monda JK, Low J, Kim HS, Paulo JA, Cannon JR, Shelat AA, Chen T, Kelsall IR, Alpi AF, Pagala V, Wang X, Peng J, Singh B, Harper JW, Schulman BA*, Guy RK*
Nat Chem Biol. 2017 Aug 13;8:850-857. https://doi.org/10.1038/nchembio.2386

Structural Studies of HHARI/UbcH7Ub Reveal Unique E2Ub Conformational Restriction by RBR RING1
Dove KK, Olszewski JL, Martino L, Duda DM, Wu XS, Miller DJ, Reiter KH, Rittinger K, Schulman BA*, Klevit RE*
Structure. 2017 Jun 6;25(6):890-900.e5. https://doi.org/10.1016/j.str.2017.04.013
> Preview: Dunkerley KM, Shaw GS. RBR Ubiquitin Transfer: Not Simply an "Open" and "Closed" Case? Structure. 2017 Jun 6;25(6):817-819. https://doi.org/10.1016/j.str.2017.05.013

Insights into links between autophagy and the ubiquitin system from the structure of LC3B bound to the LIR motif from the E3 ligase NEDD4
Qiu Y, Zheng Y, Wu KP, Schulman BA
Protein Sci. 2017 Aug 26(8):1674-1680. https://doi.org/10.1002/pro.3186

Production of Human ATG Proteins for Lipidation Assays
Zheng Y#, Qiu Y#, Gunderson JE, Schulman BA
Methods Enzymol. 2017;587:97-113. https://doi.org/10.1016/bs.mie.2016.09.055

Crystallographic Characterization of ATG Proteins and Their Interacting Partners
Qiu Y, Zheng Y, Taherbhoy AM, Kaiser SE, Schulman BA
Methods Enzymol. 2017;587:227-246. https://doi.org/10.1016/bs.mie.2016.09.058

 

2016


Two Distinct Types of E3 Ligases Work in Unison to Regulate Substrate Ubiquitylation
Scott DC#, Rhee DY#, Duda DM#, Kelsall IR, Olszewski JL, Paulo JA, de Jong A, Ovaa H, Alpi AF, Harper JW*, Schulman BA*
Cell. 2016 Aug 25;166(5):1198-1214.e24. https://doi.org/10.1016/j.cell.2016.07.027
> Preview: Kleiger G, Deshaies R. Tag Team Ubiquitin Ligases. Cell. 2016 Aug 25;166(5):1080-1081. https://doi.org/10.1016/j.cell.2016.08.014

Cryo-EM of Mitotic Checkpoint Complex-Bound APC/C Reveals Reciprocal and Conformational Regulation of Ubiquitin Ligation
Yamaguchi M, VanderLinden R, Weissmann F, Qiao R, Dube P, Brown NG, Haselbach D, Zhang W, Sidhu SS, Peters JM*, Stark H*, Schulman BA*
Mol Cell. 2016 Aug 18;63(4):593-607. https://doi.org/10.1016/j.molcel.2016.07.003
> News & Views: Morgan DO (2016) Cell division: Mitotic regulation comes into focus. Nature. 536:407-408. https://doi.org/10.1038/nature19423

Dual RING E3 Architectures Regulate Multiubiquitination and Ubiquitin Chain Elongation by APC/C
Brown NG, VanderLinden R, Watson ER, Weissmann F, Ordureau A, Wu KP, Zhang W, Yu S, Mercredi PY, Harrison JS, Davidson IF, Qiao R, Lu Y, Dube P, Brunner MR, Grace CRR, Miller DJ, Haselbach D, Jarvis MA, Yamaguchi M, Yanishevski D, Petzold G, Sidhu SS, Kuhlman B, Kirschner MW, Harper JW, Peters JM*, Stark H*, Schulman BA*
Cell. 2016 Jun 2;165(6):1440-1453. https://doi.org/10.1016/j.cell.2016.05.037

A cascading activity-based probe sequentially targets E1-E2-E3 ubiquitin enzymes
Mulder MP, Witting K, Berlin I, Pruneda JN, Wu KP, Chang JG, Merkx R, Bialas J, Groettrup M, Vertegaal AC, Schulman BA, Komander D, Neefjes J, El Oualid F, Ovaa H
Nat Chem Biol. 2016 Jul;12(7):523-30. https://doi.org/10.1038/nchembio.2084

A role of autophagy in spinocerebellar ataxia-Rare exception or general principle?
Burmeister M, Lee JH, Schulman BA, Yapici Z, Tolun A, Juhasz G, Li JZ, Klionsky DJ
Autophagy. 2016 Jul 2;12(7):1208-9. https://doi.org/10.1080/15548627.2016.1170266 (invited commentary)

Mechanism of APC/CCDC20 activation by mitotic phosphorylation
Qiao R, Weissmann F, Yamaguchi M, Brown NG, VanderLinden R, Imre R, Jarvis MA, Brunner MR, Davidson IF, Litos G, Haselbach D, Mechtler K, Stark H*, Schulman BA*, Peters JM*
Proc Natl Acad Sci U S A. 2016 Apr 25;113(19):E2570-8. https://doi.org/10.1073/pnas.1604929113

biGBac enables rapid gene assembly for the expression of large multisubunit protein complexes
Weissmann F, Petzold G, VanderLinden R, Huis In 't Veld PJ, Brown NG, Lampert F, Westermann S, Stark H, Schulman BA*, Peters JM*
Proc Natl Acad Sci U S A. 2016 Apr 25;113(19):E2564-9. https://doi.org/10.1073/pnas.1604935113

System-Wide Modulation of HECT E3 Ligases with Selective Ubiquitin Variant Probes
Zhang W, Wu KP, Sartori MA, Kamadurai HB, Ordureau A, Jiang C, Mercredi PY, Murchie R, Hu J, Persaud A, Mukherjee M, Li N, Doye A, Walker JR, Sheng Y, Hao Z, Li Y, Brown KR, Lemichez E, Chen J, Tong Y, Harper JW, Moffat J, Rotin D, Schulman BA*, Sidhu SS*
Mol Cell. 2016 Apr 7;62(1):121-36. https://doi.org/10.1016/j.molcel.2016.02.005
> Preview: Canadeo LA, Huibregtse JM. A Billion Ubiquitin Variants to Probe and Modulate the UPS. Mol Cell. 2016 Apr 7;62(1):2-4. https://doi.org/10.1016/j.molcel.2016.03.023

Multiple Weak Linear Motifs Enhance Recruitment and Processivity in SPOP-Mediated Substrate Ubiquitination
Pierce WK, Grace CR, Lee J, Nourse A, Marzahn MR, Watson ER, High AA, Peng J, Schulman BA, Mittag T
J Mol Biol. 2016 Mar 27;428(6):1256-71. https://doi.org/10.1016/j.jmb.2015.10.002

Mutation in ATG5 reduces autophagy and leads to ataxia with developmental delay
Kim M, Sandford E, Gatica D, Qiu Y, Liu X, Zheng Y, Schulman BA, Xu J, Semple I, Ro SH, Kim B, Mavioglu RN, Tolun A, Jipa A, Takats S, Karpati M, Li JZ, Yapici Z, Juhasz G, Lee JH, Klionsky DJ, Burmeister M
Elife. 2016 Jan 26;5:e12245. https://doi.org/10.7554/elife.12245

Measuring APC/C-Dependent Ubiquitylation In Vitro
Jarvis MA, Brown NG, Watson ER, VanderLinden R, Schulman BA*, Peters JM*
Methods Mol Biol. 2016;1342:287-303. https://doi.org/10.1007/978-1-4939-2957-3_18

 

2015


Itch WW Domains Inhibit Its E3 Ubiquitin Ligase Activity by Blocking E2-E3 Ligase Trans-thiolation
Riling C, Kamadurai H, Kumar S, O'Leary CE, Wu KP, Manion EE, Ying M, Schulman BA, Oliver PM
J Biol Chem. 2015 Sep 25;290(39):23875-87. https://doi.org/10.1074/jbc.m115.649269

ProteoPlex: stability optimization of macromolecular complexes by sparse-matrix screening of chemical space
Chari A, Haselbach D, Kirves JM, Ohmer J, Paknia E, Fischer N, Ganichkin O, Möller V, Frye JJ, Petzold G, Jarvis M, Tietzel M, Grimm C, Peters JM, Schulman BA, Tittmann K, Markl J, Fischer U, Stark H
Nat Methods. 2015 Sep;12(9):859-65. https://doi.org/10.1038/nmeth.3493

PAX5 is a tumor suppressor in mouse mutagenesis models of acute lymphoblastic leukemia
Dang J, Wei L, de Ridder J, Su X, Rust AG, Roberts KG, Payne-Turner D, Cheng J, Ma J, Qu C, Wu G, Song G, Huether RG, Schulman B, Janke L, Zhang J, Downing JR, van der Weyden L, Adams DJ, Mullighan CG
Blood. 2015 Jun 4;125(23):3609-17. https://doi.org/10.1182/blood-2015-02-626127

Defining roles of PARKIN and ubiquitin phosphorylation by PINK1 in mitochondrial quality control using a ubiquitin replacement strategy
Ordureau A, Heo JM, Duda DM, Paulo JA, Olszewski JL, Yanishevski D, Rinehart J, Schulman BA*, Harper JW*
Proc Natl Acad Sci U S A. 2015 May 26;112(21):6637-42. https://doi.org/10.1073/pnas.1506593112

RING E3 mechanism for ubiquitin ligation to a disordered substrate visualized for human anaphase-promoting complex
Brown NG, VanderLinden R, Watson ER, Qiao R, Grace CR, Yamaguchi M, Weissmann F, Frye JJ, Dube P, Ei Cho S, Actis ML, Rodrigues P, Fujii N, Peters JM*, Stark H*, Schulman BA*
Proc Natl Acad Sci U S A. 2015 Apr 28;112(17):5272-9. https://doi.org/10.1073/pnas.1504161112

Structure of an APC3-APC16 complex: insights into assembly of the anaphase-promoting complex/cyclosome
Yamaguchi M, Yu S, Qiao R, Weissmann F, Miller DJ, VanderLinden R, Brown NG, Frye JJ, Peters JM, Schulman BA
J Mol Biol. 2015 Apr 24;427(8):1748-64. https://doi.org/10.1016/j.jmb.2014.11.020

Protein neddylation: beyond cullin-RING ligases
Enchev RI, Schulman BA, Peter M
Nat Rev Mol Cell Biol. 2015 Jan;16(1):30-44. https://doi.org/10.1038/nrm3919 (invited review)

 

2014


Mechanism of polyubiquitination by human anaphase-promoting complex: RING repurposing for ubiquitin chain assembly
Brown NG, Watson ER, Weissmann F, Jarvis MA, VanderLinden R, Grace CR, Frye JJ, Qiao R, Dube P, Petzold G, Cho SE, Alsharif O, Bao J, Davidson IF, Zheng JJ, Nourse A, Kurinov I, Peters JM*, Stark H*, Schulman BA*
Mol Cell. 2014 Oct 23;56(2):246-60. https://doi.org/10.1016/j.molcel.2014.09.009
> Preview: Iwai K, Tanaka K. Ubiquitin chain elongation: an intriguing strategy. Mol Cell. 2014 Oct 23;56(2):189-191. https://doi.org/10.1016/j.molcel.2014.10.009

Quantitative proteomics reveal a feedforward mechanism for mitochondrial PARKIN translocation and ubiquitin chain synthesis
Ordureau A, Sarraf SA, Duda DM, Heo JM, Jedrychowski MP, Sviderskiy VO, Olszewski JL, Koerber JT, Xie T, Beausoleil SA, Wells JA, Gygi SP, Schulman BA, Harper JW
Mol Cell. 2014 Nov 6;56(3):360-75. https://doi.org/10.1016/j.molcel.2014.09.007
> Preview: Stolz A, Dikic I. PINK1-PARKIN interplay: down to ubiquitin phosphorylation. Mol Cell. 2014 Nov 6;56(3):341-342. https://doi.org/10.1016/j.molcel.2014.10.022

Structure of a RING E3 trapped in action reveals ligation mechanism for the ubiquitin-like protein NEDD8
Scott DC, Sviderskiy VO, Monda JK, Lydeard JR, Cho SE, Harper JW, Schulman BA
Cell. 2014 Jun 19;157(7):1671-84. https://doi.org/10.1016/j.cell.2014.04.037

The instability of the BTB-KELCH protein Gigaxonin causes Giant Axonal Neuropathy and constitutes a new penetrant and specific diagnostic test
Boizot A, Talmat-Amar Y, Morrogh D, Kuntz NL, Halbert C, Chabrol B, Houlden H, Stojkovic T, Schulman BA, Rautenstrauss B, Bomont P
Acta Neuropathol Commun. 2014 Apr 24;2:47. https://doi.org/10.1186/2051-5960-2-47

Atomistic autophagy: the structures of cellular self-digestion
Hurley JH, Schulman BA
Cell. 2014 Apr 10;157(2):300-311. https://doi.org/10.1016/j.cell.2014.01.070 (invited review)

Dynamic regulation of macroautophagy by distinctive ubiquitin-like proteins
Klionsky DJ, Schulman BA
Nat Struct Mol Biol. 2014 Apr;21(4):336-45. https://doi.org/10.1038/nsmb.2787 (invited review)

SPOP promotes tumorigenesis by acting as a key regulatory hub in kidney cancer
Li G, Ci W, Karmakar S, Chen K, Dhar R, Fan Z, Guo Z, Zhang J, Ke Y, Wang L, Zhuang M, Hu S, Li X, Zhou L, Li X, Calabrese MF, Watson ER, Prasad SM, Rinker-Schaeffer C, Eggener SE, Stricker T, Tian Y, Schulman BA, Liu J, White KP
Cancer Cell. 2014 Apr 14;25(4):455-68. https://doi.org/10.1016/j.ccr.2014.02.007

2013

Building and remodelling Cullin-RING E3 ubiquitin ligases
Lydeard JR, Schulman BA, Harper JW
EMBO Rep. 2013 Dec;14(12):1050-61. https://doi.org/10.1038/embor.2013.173 (invited review)

Binding to E1 and E3 is mutually exclusive for the human autophagy E2 Atg3
Qiu Y, Hofmann K, Coats JE, Schulman BA*, Kaiser SE*
Protein Sci. 2013 Dec;22(12):1691-7. https://doi.org/10.1002/pro.2381

TRIAD1 and HHARI bind to and are activated by distinct neddylated Cullin-RING ligase complexes
Kelsall IR, Duda DM, Olszewski JL, Hofmann K, Knebel A, Langevin F, Wood N, Wightman M, Schulman BA, Alpi AF
EMBO J. 2013 Oct 30;32(21):2848-60. https://doi.org/10.1038/emboj.2013.209

Mechanism of ubiquitin ligation and lysine prioritization by a HECT E3
Kamadurai HB, Qiu Y, Deng A, Harrison JS, Macdonald C, Actis M, Rodrigues P, Miller DJ, Souphron J, Lewis SM, Kurinov I, Fujii N, Hammel M, Piper R, Kuhlman B, Schulman BA
Elife. 2013 Aug 8;2:e00828. https://doi.org/10.7554/elife.00828
> Insight: Meyer HJ, Rape M. Caught in the act. Elife. 2013 Aug 8;2:e01127. https://doi.org/10.7554/elife.01127

Electron microscopy structure of human APC/C(CDH1)-EMI1 reveals multimodal mechanism of E3 ligase shutdown
Frye JJ, Brown NG, Petzold G, Watson ER, Grace CR, Nourse A, Jarvis MA, Kriwacki RW, Peters JM*, Stark H*, Schulman BA*
Nat Struct Mol Biol. 2013 Jul;20(7):827-35. https://doi.org/10.1038/nsmb.2593
> News & Views: Yamano H. EMI1, a three-in-one ubiquitylation inhibitor. Nat Struct Mol Biol. 2013 Jul;20(7):773-4. https://doi.org/10.1038/nsmb.2626
> Select: Intrinsically Disordered Proteins. Cell. 2013;154(3): 473-475. ISSN 0092-8674. https://doi.org/10.1016/j.cell.2013.07.026

Structure of HHARI, a RING-IBR-RING ubiquitin ligase: autoinhibition of an Ariadne-family E3 and insights into ligation mechanism
Duda DM, Olszewski JL, Schuermann JP, Kurinov I, Miller DJ, Nourse A, Alpi AF, Schulman BA
Structure. 2013 Jun 4;21(6):1030-41. https://doi.org/10.1016/j.str.2013.04.019
> Preview: Davies CW, Das C. HHARI is one HECT of a RING. Structure. 2013 Jun 4;21(6):872-4. https://doi.org/10.1016/j.str.2013.05.003
> Have you seen?: Byrd RA, Weissman AM. Compact Parkin only: insights into the structure of an autoinhibited ubiquitin ligase. EMBO J. 2013 Jul 31;32(15):2087-9. https://doi.org/10.1038/emboj.2013.158

Structures of Atg7-Atg3 and Atg7-Atg10 reveal noncanonical mechanisms of E2 recruitment by the autophagy E1
Kaiser SE, Qiu Y, Coats JE, Mao K, Klionsky DJ, Schulman BA
Autophagy. 2013 May;9(5):778-80. https://doi.org/10.4161/auto.23644 (invited commentary)

SCFFbxw5 mediates transient degradation of actin remodeller Eps8 to allow proper mitotic progression
Werner A, Disanza A, Reifenberger N, Habeck G, Becker J, Calabrese M, Urlaub H, Lorenz H, Schulman B, Scita G, Melchior F
Nat Cell Biol. 2013 Feb;15(2):179-88. https://doi.org/10.1038/ncb2661

Structural conservation of distinctive N-terminal acetylation-dependent interactions across a family of mammalian NEDD8 ligation enzymes
Monda JK, Scott DC, Miller DJ, Lydeard J, King D, Harper JW, Bennett EJ, Schulman BA
Structure. 2013 Jan 8;21(1):42-53. https://doi.org/10.1016/j.str.2012.10.013

2012

­Noncanonical E2 recruitment by the autophagy E1 revealed by Atg7-Atg3 and Atg7-Atg10 structures
Kaiser SE, Mao K, Taherbhoy AM, Yu S, Olszewski JL, Duda DM, Kurinov I, Deng A, Fenn TD, Klionsky DJ, Schulman BA
Nat Struct Mol Biol. 2012 Dec;19(12):1242-9. https://doi.org/10.1038/nsmb.2415
> Research Highlights: Donner, A. E2 loader. Nat Chem Biol 9, 8 (2013). https://doi.org/10.1038/nchembio.1145

APC15 mediates CDC20 autoubiquitylation by APC/C(MCC) and disassembly of the mitotic checkpoint complex
Uzunova K, Dye BT, Schutz H, Ladurner R, Petzold G, Toyoda Y, Jarvis MA, Brown NG, Poser I, Novatchkova M, Mechtler K, Hyman AA, Stark H, Schulman BA*, Peters JM*
Nat Struct Mol Biol. 2012 Nov;19(11):1116-23. https://doi.org/10.1038/nsmb.2412
> News & Views: Musacchio A, Ciliberto A. The spindle-assembly checkpoint and the beauty of self-destruction. Nat Struct Mol Biol. 2012 Nov;19(11):1059-61. https://doi.org/10.1038/nsmb.2429

Structural basis for a reciprocal regulation between SCF and CSN
Enchev RI, Scott DC, da Fonseca PC, Schreiber A, Monda JK, Schulman BA*, Peter M*, Morris EP*
Cell Rep. 2012 Sep 27;2(3):616-27. https://doi.org/10.1016/j.celrep.2012.08.019

Structural biology: A protein engagement RING
Lima CD, Schulman BA
Nature. 2012 Sep 6;489(7414):43-4. https://doi.org/10.1038/489043a (invited commentary)

Structure of a glomulin-RBX1-CUL1 complex: inhibition of a RING E3 ligase through masking of its E2-binding surface
Duda DM, Olszewski JL, Tron AE, Hammel M, Lambert LJ, Waddell MB, Mittag T, DeCaprio JA, Schulman BA
Mol Cell. 2012 Aug 10;47(3):371-82. https://doi.org/10.1016/j.molcel.2012.05.044
> Preview: Hristova VA, Stringer DK, Weissman AM. Cullin RING ligases: glommed by glomulin. Mol Cell. 2012 Aug 10;47(3):331-2. https://doi.org/10.1016/j.molcel.2012.07.025

Ubiquitin-like modifiers
Taherbhoy AM, Schulman BA, Kaiser SE
Essays Biochem. 2012;52:51-63. https://doi.org/10.1042/bse0520051 (invited book chapter)

The glomuvenous malformation protein Glomulin binds Rbx1 and regulates cullin RING ligase-mediated turnover of Fbw7
Tron AE, Arai T, Duda DM, Kuwabara H, Olszewski JL, Fujiwara Y, Bahamon BN, Signoretti S, Schulman BA, DeCaprio JA
Mol Cell. 2012 Apr 13;46(1):67-78. https://doi.org/10.1016/j.molcel.2012.02.005

Viral E3 ubiquitin ligase-mediated degradation of a cellular E3: viral mimicry of a cellular phosphorylation mark targets the RNF8 FHA domain
Chaurushiya MS, Lilley CE, Aslanian A, Meisenhelder J, Scott DC, Landry S, Ticau S, Boutell C, Yates JR 3rd, Schulman BA, Hunter T, Weitzman MD
Mol Cell. 2012 Apr 13;46(1):79-90. https://doi.org/10.1016/j.molcel.2012.02.004

Trans mechanism for ubiquitin-like protein transfer in autophagy
Taherbhoy AM, Kaiser SE, Schulman BA
Cell Cycle. 2012 Feb 15;11(4):635-6. https://doi.org/10.4161/cc.11.4.19277 (invited commentary)

2011

­Atg8 transfer from Atg7 to Atg3: a distinctive E1-E2 architecture and mechanism in the autophagy pathway
Taherbhoy AM, Tait SW, Kaiser SE, Williams AH, Deng A, Nourse A, Hammel M, Kurinov I, Rock CO, Green DR, Schulman BA
Mol Cell. 2011 Nov 4;44(3):451-61. https://doi.org/10.1016/j.molcel.2011.08.034 (cover)

Twists and turns in ubiquitin-like protein conjugation cascades
Schulman BA
Protein Sci. 2011 Dec;20(12):1941-54. https://doi.org/10.1002/pro.750 (invited review)

N-terminal acetylation acts as an avidity enhancer within an interconnected multiprotein complex
Scott DC, Monda JK, Bennett EJ, Harper JW, Schulman BA
Science. 2011 Nov 4;334(6056):674-8. https://doi.org/10.1126/science.1209307
> Research Highlights: Mason, S. Acetylating for avidity. Nat Struct Mol Biol 18, 1183 (2011). https://doi.org/10.1038/nsmb.2181

A RING E3-substrate complex poised for ubiquitin-like protein transfer: structural insights into cullin-RING ligases
Calabrese MF, Scott DC, Duda DM, Grace CR, Kurinov I, Kriwacki RW, Schulman BA
Nat Struct Mol Biol. 2011 Jul 17;18(8):947-9. https://doi.org/10.1038/nsmb.2086
> News & Views: Rahighi S, Dikic I. Conformational flexibility and rotation of the RING domain in activation of cullin-RING ligases. Nat Struct Mol Biol. 2011 Aug 3;18(8):863-5.https://doi.org/10.1038/nsmb.2117

Structural regulation of cullin-RING ubiquitin ligase complexes
Duda DM, Scott DC, Calabrese MF, Zimmerman ES, Zheng N, Schulman BA
Curr Opin Struct Biol. 2011 Apr;21(2):257-64. https://doi.org/10.1016/j.sbi.2011.01.003 (invited review)

IDH1 and IDH2 mutations in pediatric acute leukemia
Andersson AK, Miller DW, Lynch JA, Lemoff AS, Cai Z, Pounds SB, Radtke I, Yan B, Schuetz JD, Rubnitz JE, Ribeiro RC, Raimondi SC, Zhang J, Mullighan CG, Shurtleff SA, Schulman BA, DowningJR
Leukemia. 2011 Oct;25(10):1570-7. https://doi.org/10.1038/leu.2011.133

2010 - 2006

Crystal structure of UBA2(ufd)-Ubc9: insights into E1-E2 interactions in Sumo pathways
Wang J, Taherbhoy AM, Hunt HW, Seyedin SN, Miller DW, Miller DJ, Huang DT, Schulman BA
PLoS One. 2010 Dec 30;5(12):e15805. https://doi.org/10.1371/journal.pone.0015805

Pathogenic bacteria target NEDD8-conjugated cullins to hijack host-cell signaling pathways
Jubelin G, Taieb F, Duda DM, Hsu Y, Samba-Louaka A, Nobe R, Penary M, Watrin C, Nougayrède JP, Schulman BA, Stebbins CE, Oswald E
PLoS Pathog. 2010 Sep 30;6(9):e1001128. https://doi.org/10.1371/journal.ppat.1001128

Structural assembly of cullin-RING ubiquitin ligase complexes
Zimmerman ES, Schulman BA, Zheng N
Curr Opin Struct Biol. 2010 Dec;20(6):714-21. https://doi.org/10.1016/j.sbi.2010.08.010 (invited review)

A dual E3 mechanism for Rub1 ligation to Cdc53
Scott DC, Monda JK, Grace CR, Duda DM, Kriwacki RW, Kurz T, Schulman BA
Mol Cell. 2010 Sep 10;39(5):784-96. https://doi.org/10.1016/j.molcel.2010.08.030

Structural biology: Transformative encounters
Schulman BA, Haas AL
Nature. 2010 Feb 18;463(7283):889-90. https://doi.org/10.1038/463889a (invited commentary)

Identification and characterization of the first small molecule inhibitor of MDMX
Reed D, Shen Y, Shelat AA, Arnold LA, Ferreira AM, Zhu F, Mills N, Smithson DC, Regni CA, Bashford D, Cicero SA, Schulman BA, Jochemsen AG, Guy RK, Dyer MA
J Biol Chem. 2010 Apr 2;285(14):10786-96. https://doi.org/10.1074/jbc.m109.056747

Insights into ubiquitin transfer cascades from a structure of a UbcH5B~ubiquitin-HECT(NEDD4L) complex
Kamadurai HB, Souphron J, Scott DC, Duda DM, Miller DJ, Stringer D, Piper RC, Schulman BA
Mol Cell. 2009 Dec 25;36(6):1095-102. https://doi.org/10.1016/j.molcel.2009.11.010

Cullin neddylation and substrate-adaptors counteract SCF inhibition by the CAND1-like protein Lag2 in Saccharomyces cerevisiae
Siergiejuk E, Scott DC, Schulman BA, Hofmann K, Kurz T, Peter M
EMBO J. 2009 Dec 16;28(24):3845-56. https://doi.org/10.1038/emboj.2009.354

Structures of SPOP-substrate complexes: insights into molecular architectures of BTB-Cul3 ubiquitin ligases
Zhuang M, Calabrese MF, Liu J, Waddell MB, Nourse A, Hammel M, Miller DJ, Walden H, Duda DM, Seyedin SN, Hoggard T, Harper JW, White KP, Schulman BA
Mol Cell. 2009 Oct 9;36(1):39-50. https://doi.org/10.1016/j.molcel.2009.09.022

Insights into anaphase promoting complex TPR subdomain assembly from a CDC26-APC6 structure
Wang J, Dye BT, Rajashankar KR, Kurinov I, Schulman BA
Nat Struct Mol Biol. 2009 Sep;16(9):987-9. https://doi.org/10.1038/nsmb.1645

(G2)BRinging an E2 to E3
Wang J, Schulman BA
Structure. 2009 Jul 15;17(7):916-7. https://doi.org/10.1016/j.str.2009.06.005 (invited commentary)

How the MccB bacterial ancestor of ubiquitin E1 initiates biosynthesis of the microcin C7 antibiotic
Regni CA, Roush RF, Miller DJ, Nourse A, Walsh CT, Schulman BA
EMBO J. 2009 Jul 8;28(13):1953-64. https://doi.org/10.1038/emboj.2009.146

JAK mutations in high-risk childhood acute lymphoblastic leukemia
Mullighan CG, Zhang J, Harvey RC, Collins-Underwood JR, Schulman BA, Phillips LA, Tasian SK, Loh ML, Su X, Liu W, Devidas M, Atlas SR, Chen IM, Clifford RJ, Gerhard DS, Carroll WL, Reaman GH, Smith M, Downing JR, Hunger SP, Willman CL
Proc Natl Acad Sci U S A. 2009 Jun 9;106(23):9414-8. https://doi.org/10.1073/pnas.0811761106

Ubiquitin-like protein activation by E1 enzymes: the apex for downstream signalling pathways
Schulman BA, Harper JW
Nat Rev Mol Cell Biol. 2009 May;10(5):319-31. https://doi.org/10.1038/nrm2673 (invited review)

E2-RING expansion of the NEDD8 cascade confers specificity to cullin modification
Huang DT, Ayrault O, Hunt HW, Taherbhoy AM, Duda DM, Scott DC, Borg LA, Neale G, Murray PJ, Roussel MF*, Schulman BA*
Mol Cell. 2009 Feb 27;33(4):483-95. https://doi.org/10.1016/j.molcel.2009.01.011 (cover)
> Preview: Pichler A. A second E2 for nedd8ylation expands substrate selection. Structure. 2009 Mar 11;17(3):321-2.https://doi.org/10.1016/j.str.2009.02.003

Deletion of IKZF1 and prognosis in acute lymphoblastic leukemia
Mullighan CG, Su X, Zhang J, Radtke I, Phillips LA, Miller CB, Ma J, Liu W, Cheng C, Schulman BA, Harvey RC, Chen IM, Clifford RJ, Carroll WL, Reaman G, Bowman WP, Devidas M, Gerhard DS, Yang W, Relling MV, Shurtleff SA, Campana D, Borowitz MJ, Pui CH, Smith M, Hunger SP, Willman CL, Downing JR; Children's Oncology Group
N Engl J Med. 2009 Jan 29;360(5):470-80. https://doi.org/10.1056/nejmoa0808253

Structural insights into NEDD8 activation of cullin-RING ligases: conformational control of conjugation
Duda DM, Borg LA, Scott DC, Hunt HW, Hammel M, Schulman BA
Cell. 2008 Sep 19;134(6):995-1006. https://doi.org/10.1016/j.cell.2008.07.022
> Preview: Saifee NH, Zheng N. A ubiquitin-like protein unleashes ubiquitin ligases. Cell. 2008 Oct 17;135(2):209-11. https://doi.org/10.1016/j.cell.2008.09.049

Structural dissection of a gating mechanism preventing misactivation of ubiquitin by NEDD8's E1
Souphron J, Waddell MB, Paydar A, Tokgöz-Gromley Z, Roussel MF, Schulman BA
Biochemistry. 2008 Aug 26;47(34):8961-9. https://doi.org/10.1021/bi800604c
> Spotlighted in Rich RL, Myszka DG (2009) Grading the commercial optical biosensor literature—Class of 2008: ‘The Mighty Binders’. J. Mol Rec. 23(1): 1-64. https://doi.org/10.1002/jmr.1004

Identification of conjugation specificity determinants unmasks vestigial preference for ubiquitin within the NEDD8 E2
Huang DT, Zhuang M, Ayrault O, Schulman BA
Nat Struct Mol Biol. 2008 Mar;15(3):280-7. https://doi.org/10.1038/nsmb.1387

­Structural mechanisms underlying posttranslational modification by ubiquitin-like proteins
Dye BT, Schulman BA
Annu Rev Biophys Biomol Struct. 2007;36:131-50. https://doi.org/10.1146/annurev.biophys.36.040306.132820 (invited review)

Structure of a SUMO-binding-motif mimic bound to Smt3p-Ubc9p: conservation of a non-covalent ubiquitin-like protein-E2 complex as a platform for selective interactions within a SUMO pathway
Duda DM, van Waardenburg RC, Borg LA, McGarity S, Nourse A, Waddell MB, Bjornsti MA, Schulman BA
J Mol Biol. 2007 Jun 8;369(3):619-30. https://doi.org/10.1016/j.jmb.2007.04.007

Basis for a ubiquitin-like protein thioester switch toggling E1-E2 affinity
Huang DT, Hunt HW, Zhuang M, Ohi MD, Holton JM, Schulman BA
Nature. 2007 Jan 25;445(7126):394-8. https://doi.org/10.1038/nature05490
> News & Views: Trempe JF, Endicott JA. Structural biology: pass the protein. Nature. 2007 Jan 25;445(7126):375-6. https://doi.org/10.1038/nature05564
> Research Highlight: Pickett JA (2007) A Smotth handover. Nat Rev Mol Cell Biol. 8(3);178. Nat Rev Mol Cell Biol
> Preview: Haas AL. Structural insights into early events in the conjugation of ubiquitin and ubiquitin-like proteins. Mol Cell. 2007 Jul 20;27(2):174-175. https://doi.org/10.1016/j.molcel.2007.07.003

Breaking up with a kinky SUMO
Huang DT, Schulman BA
Nat Struct Mol Biol. 2006 Dec;13(12):1045-7. https://doi.org/10.1038/nsmb1206-1045 (invited commentary)

Distinct functional domains of Ubc9 dictate cell survival and resistance to genotoxic stress
van Waardenburg RC, Duda DM, Lancaster CS, Schulman BA, Bjornsti MA
Mol Cell Biol. 2006 Jul;26(13):4958-69. https://doi.org/10.1128/mcb.00160-06

Structural complexity in ubiquitin recognition
Harper JW, Schulman BA
Cell. 2006 Mar 24;124(6):1133-6. https://doi.org/10.1016/j.cell.2006.03.009 (invited review)

A calcium-regulated MEF2 sumoylation switch controls postsynaptic differentiation
Shalizi A, Gaudillière B, Yuan Z, Stegmüller J, Shirogane T, Ge Q, Tan Y, Schulman B, Harper JW, Bonni A
Science. 2006 Feb 17;311(5763):1012-7. https://doi.org/10.1126/science.1122513

2005 - 2001

Protein ubiquitination: CHIPping away the symmetry
Schulman BA, Chen ZJ
Mol Cell. 2005 Dec 9;20(5):653-5. https://doi.org/10.1016/j.molcel.2005.11.019 (invited commentary)

High-level expression and purification of recombinant SCF ubiquitin ligases
Li T, Pavletich NP*, Schulman BA*, Zheng N*
Methods Enzymol. 2005;398:125-42. https://doi.org/10.1016/s0076-6879(05)98012-9

Expression, purification, and characterization of the E1 for human NEDD8, the heterodimeric APPBP1-UBA3 complex
Huang DT, Schulman BA
Methods Enzymol. 2005;398:9-20. https://doi.org/10.1016/s0076-6879(05)98002-6

Structural basis of the Cks1-dependent recognition of p27(Kip1) by the SCF(Skp2) ubiquitin ligase
Hao B, Zheng N, Schulman BA, Wu G, Miller JJ, Pagano M, Pavletich NP
Mol Cell. 2005 Oct 7;20(1):9-19. https://doi.org/10.1016/j.molcel.2005.09.003

E2 conjugating enzymes must disengage from their E1 enzymes before E3-dependent ubiquitin and ubiquitin-like transfer
Eletr ZM, Huang DT, Duda DM, Schulman BA, Kuhlman B
Nat Struct Mol Biol. 2005 Oct;12(10):933-4. https://doi.org/10.1038/nsmb984

Tag-team SUMO wrestling
Duda DM, Schulman BA
Mol Cell. 2005 Jun 10;18(6):612-4. https://doi.org/10.1016/j.molcel.2005.05.017 (invited commentary)

Structural analysis of Escherichia coli ThiF
Duda DM, Walden H, Sfondouris J, Schulman BA
J Mol Biol. 2005 Jun 17;349(4):774-86. https://doi.org/10.1016/j.jmb.2005.04.011

Structural basis for recruitment of Ubc12 by an E2 binding domain in NEDD8's E1
Huang DT, Paydar A, Zhuang M, Waddell MB, Holton JM, Schulman BA
Mol Cell. 2005 Feb 4;17(3):341-50. https://doi.org/10.1016/j.molcel.2004.12.020
> Preview: VanDemark AP, Hill CP. E1 on the move. Mol Cell. 2005 Feb 18;17(4):474-5. https://doi.org/10.1016/j.molcel.2005.02.004

A unique E1-E2 interaction required for optimal conjugation of the ubiquitin-like protein NEDD8
Huang DT, Miller DW, Mathew R, Cassell R, Holton JM, Roussel MF, Schulman BA
Nat Struct Mol Biol. 2004 Oct;11(10):927-35. https://doi.org/10.1038/nsmb826
> News & Views: VanDemark AP, Hill CP. Grabbing E2 by the tail. Nat Struct Mol Biol. 2004 Oct;11(10):908-9. https://doi.org/10.1038/nsmb1004-908
> News: Structural Insights for Therapeutic Targeting of an E2 Function and NEDDylation in Proliferation Control. Cancer Biology & Therapy, 3:10, 923-930. https://doi.org/10.4161/cbt.3.10.1261

Structural and dynamic independence of isopeptide-linked RanGAP1 and SUMO-1
Macauley MS, Errington WJ, Okon M, Schärpf M, Mackereth CD, Schulman BA, McIntosh LP
J Biol Chem. 2004 Nov 19;279(47):49131-7. https://doi.org/10.1074/jbc.m408705200

The UbcH8 ubiquitin E2 enzyme is also the E2 enzyme for ISG15, an IFN-alpha/beta-induced ubiquitin-like protein
Zhao C, Beaudenon SL, Kelley ML, Waddell MB, Yuan W, Schulman BA, Huibregtse JM, Krug RM
Proc Natl Acad Sci U S A. 2004 May 18;101(20):7578-82. https://doi.org/10.1073/pnas.0402528101

Local and global cooperativity in the human alpha-lactalbumin molten globule
Quezada CM*, Schulman BA*, Froggatt JJ, Dobson CM, Redfield C
J Mol Biol. 2004 Apr 16;338(1):149-58. https://doi.org/10.1016/j.jmb.2004.02.045

Ubiquitin-like protein activation
Huang DT, Walden H, Duda D, Schulman BA
Oncogene. 2004 Mar 15;23(11):1958-71. https://doi.org/10.1038/sj.onc.1207393 (invited review)

The structure of the APPBP1-UBA3-NEDD8-ATP complex reveals the basis for selective ubiquitin-like protein activation by an E1
Walden H, Podgorski MS, Huang DT, Miller DW, Howard RJ, Minor DL Jr, Holton JM, Schulman BA
Mol Cell. 2003 Dec;12(6):1427-37. https://doi.org/10.1016/s1097-2765(03)00452-0

Structure of a beta-TrCP1-Skp1-beta-catenin complex: destruction motif binding and lysine specificity of the SCF(beta-TrCP1) ubiquitin ligase
Wu G, Xu G, Schulman BA, Jeffrey PD, Harper JW, Pavletich NP
Mol Cell. 2003 Jun;11(6):1445-56. https://doi.org/10.1016/s1097-2765(03)00234-x

Insights into the ubiquitin transfer cascade from the structure of the activating enzyme for NEDD8
Walden H, Podgorski MS, Schulman BA
Nature. 2003 Mar 20;422(6929):330-4. https://doi.org/10.1038/nature01456
> News & Views: VanDemark AP, Hill CP. Two-stepping with E1. Nat Struct Biol. 2003 Apr;10(4):244-6. https://doi.org/10.1038/nsb0403-244

Parkin is a component of an SCF-like ubiquitin ligase complex and protects postmitotic neurons from kainate excitotoxicity
Staropoli JF, McDermott C, Martinat C, Schulman B, Demireva E, Abeliovich A
Neuron. 2003 Mar 6;37(5):735-49. https://doi.org/10.1016/s0896-6273(03)00084-9

Identification of a multifunctional binding site on Ubc9p required for Smt3p conjugation
Bencsath KP, Podgorski MS, Pagala VR, Slaughter CA, Schulman BA
J Biol Chem. 2002 Dec 6;277(49):47938-45. https://doi.org/10.1074/jbc.M207442200

The SOCS box: a tale of destruction and degradation
Kile BT, Schulman BA, Alexander WS, Nicola NA, Martin HM, Hilton DJ
Trends Biochem Sci. 2002 May;27(5):235-41. https://doi.org/10.1016/s0968-0004(02)02085-6 (invited review)

Structure of the Cul1-Rbx1-Skp1-F boxSkp2 SCF ubiquitin ligase complex
Zheng N, Schulman BA, Song L, Miller JJ, Jeffrey PD, Wang P, Chu C, Koepp DM, Elledge SJ, Pagano M, Conaway RC, Conaway JW, Harper JW, Pavletich NP
Nature. 2002 Apr 18;416(6882):703-9. https://doi.org/10.1038/416703a

Probing subtle differences in the hydrogen exchange behavior of variants of the human alpha-lactalbumin molten globule using mass spectrometry
Last AM, Schulman BA, Robinson CV, Redfield C
J Mol Biol. 2001 Aug 24;311(4):909-19. https://doi.org/10.1006/jmbi.2001.4911

A splice variant of Skp2 is retained in the cytoplasm and fails to direct cyclin D1 ubiquitination in the uterine cancer cell line SK-UT
Ganiatsas S, Dow R, Thompson A, Schulman B, Germain D
Oncogene. 2001 Jun 21;20(28):3641-50. https://doi.org/10.1038/sj.onc.1204501

Role of the F-box protein Skp2 in lymphomagenesis
Latres E, Chiarle R, Schulman BA, Pavletich NP, Pellicer A, Inghirami G, Pagano M
Proc Natl Acad Sci U S A. 2001 Feb 27;98(5):2515-20. https://doi.org/10.1073/pnas.041475098

2000 and earlier

Insights into SCF ubiquitin ligases from the structure of the Skp1-Skp2 complex
Schulman BA, Carrano AC, Jeffrey PD, Bowen Z, Kinnucan ER, Finnin MS, Elledge SJ, Harper JW, Pagano M, Pavletich NP
Nature. 2000 Nov 16;408(6810):381-6. https://doi.org/10.1038/35042620

Alpha-lactalbumin forms a compact molten globule in the absence of disulfide bonds
Redfield C, Schulman BA, Milhollen MA, Kim PS, Dobson CM
Nat Struct Biol. 1999 Oct;6(10):948-52. https://doi.org/10.1038/13318

Substrate recruitment to cyclin-dependent kinase 2 by a multipurpose docking site on cyclin A
Schulman BA, Lindstrom DL, Harlow E
Proc Natl Acad Sci U S A. 1998 Sep 1;95(18):10453-8. https://doi.org/10.1073/pnas.95.18.10453

A residue-specific NMR view of the non-cooperative unfolding of a molten globule
Schulman BA, Kim PS, Dobson CM, Redfield C
Nat Struct Biol. 1997 Aug;4(8):630-4. https://doi.org/10.1038/nsb0897-630

Proline scanning mutagenesis of a molten globule reveals non-cooperative formation of a protein's overall topology
Schulman BA, Kim PS
Nat Struct Biol. 1996 Aug;3(8):682-7. https://doi.org/10.1038/nsb0896-682

Disulfide determinants of calcium-induced packing in alpha-lactalbumin
Wu LC, Schulman BA, Peng ZY, Kim PS
Biochemistry. 1996 Jan 23;35(3):859-63. https://doi.org/10.1021/bi951408p

Different subdomains are most protected from hydrogen exchange in the molten globule and native states of human alpha-lactalbumin
Schulman BA, Redfield C, Peng ZY, Dobson CM, Kim PS
J Mol Biol. 1995 Nov 10;253(5):651-7. https://doi.org/10.1006/jmbi.1995.0579

Does the molten globule have a native-like tertiary fold?
Peng ZY, Wu LC, Schulman BA, Kim PS
Philos Trans R Soc Lond B Biol Sci. 1995 Apr 29;348(1323):43-7. https://doi.org/10.1098/rstb.1995.0044 (invited review)

Hydrogen exchange in BPTI variants that do not share a common disulfide bond
Schulman BA, Kim PS
Protein Sci. 1994 Dec;3(12):2226-32. https://doi.org/10.1002/pro.5560031208

Hydrogen-oxidizing electron transport components in the hyperthermophilic archaebacterium Pyrodictium brockii
Pihl TD, Black LK, Schulman BA, Maier RJ
J Bacteriol. 1992 Jan;174(1):137-43. https://doi.org/10.1128/jb.174.1.137-143.1992

Hydrogen-sulfur autotrophy in the hyperthermophilic archaebacterium, Pyrodictium brockii
Pihl TD, Schicho RN, Black LK, Schulman BA, Maier RJ, Kelly RM
Biotechnol Genet Eng Rev. 1990;8:345-77. https://doi.org/10.1080/02648725.1990.10647874 (invited review)

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