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Structural studies of Phosphoinositide signaling

Roger Williams group

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Publications

Gulluni F, Prever L, Li H, Krafcikova P, Corrado I, Lo WT, Margaria JP, Chen A, De Santis MC, Cnudde SJ, Fogerty J, Yuan A, Massarotti A, Sarijalo NT, Vadas O, Williams RL, Thelen M, Powell DR, Schueler M, Wiesener MS, Balla T, Baris HN, Tiosano D, McDermott BM Jr, Perkins BD, Ghigo A, Martini M, Haucke V, Boura E, Merlo GR, Buchner DA, Hirsch E. (2021) PI(3,4)P2-mediated cytokinetic abscission prevents early senescence and cataract formation. Science. 374(6573):eabk0410. doi: 10.1126/science.abk0410. Epub 2021 Dec 10. PMID: 34882480.

Mercer TJ, Ohashi Y, Boeing S, Jefferies HBJ, De Tito S, Flynn H, Tremel S, Zhang W, Wirth M, Frith D, Snijders AP, Williams RL, Tooze SA. Phosphoproteomic identification of ULK substrates reveals VPS15-dependent ULK/VPS34 interplay in the regulation of autophagy.(2021) EMBO J. 40(14):e105985. doi: 10.15252/embj.2020105985. Epub 2021 Jun 14. PMID: 34121209

Tremel S, Ohashi Y, Morado DR, Bertram J, Perisic O, Brandt LTL, von Wrisberg MK, Chen ZA, Maslen SL, Kovtun O, Skehel M, Rappsilber J, Lang K, Munro S, Briggs JAG, Williams RL. Structural basis for VPS34 kinase activation by Rab1 and Rab5 on membranes. Nat Commun. 2021:1564. PMID: 33692360.

Ohashi Y, Tremel S, Williams RL. (2021) Unsaturation, curvature and charge: effects of membrane parameters on PIK3C3/VPS34-containing complexes. Autophagy. Epub ahead of print. PMID: 33446010.

Buckles TC, Ohashi Y, Tremel S, McLaughlin SH, Pardon E, Steyaert J, Gordon MT, Williams RL, Falke JJ. (2020) The G-Protein Rab5A Activates VPS34 Complex II, a Class III PI3K, by a Dual Regulatory Mechanism. Biophys J. Dec 1;119(11):2205-2218. PMID: 33137306.

Ohashi Y, Tremel S, Masson GR, McGinney L, Boulanger J, Rostislavleva K, Johnson, CM, Niewczas I, Clark J, Williams RL (2020). Membrane characteristics tune activities of endosomal and autophagic human VPS34 complexes. Elife. 2020;9:e58281. PMID: 32602837.

Baretic D, Maia de Oliveira T, Niess M, Wan P, Pollard H, Johnson CM, Truman C, McCall E, Fisher D, Williams R, Phillips C. (2019) Structural insights into the critical DNA damage sensors DNA-PKcs, ATM and ATR. Prog Biophys Mol Biol. 147:4-16. PMID: 31255703

Anandapadamanaban M, Masson GR, Perisic O, Berndt A, Kaufman J, Johnson CM, Santhanam B, Rogala KB, Sabatini DM, Williams RL. (2019) Architecture of human Rag GTPase heterodimers and their complex with mTORC1. Science 366:203-210. doi: 10.1126/science.aax3939. PMID: 31601764; PMCID: PMC6795536.

Anandapadamanaban, M. and Williams, RL (2019) Prime Time for Dimeric Cytohesins: Surveying the Membrane with One Foot at a Time. Structure 27, 1739. doi.org/10.1016/j.str.2019.11.009.

Harding HP, Ordonez A, Allen F, Parts L, Inglis AJ,Williams RL, Ron D. (2019) The ribosomal P-stalk couples amino acid starvation to GCN2 activation in mammalian cells. Elife. 8:e50149. doi: 10.7554/eLife.50149. PMID:31749445

Takeda AJ, Maher TJ, Zhang Y, Lanahan SM, Bucklin ML, Compton SR, Tyler PM, Comrie WA, Matsuda M, Olivier KN, Pittaluga S, McElwee JJ, Long Priel DA, Kuhns DB, Williams RL, Mustillo PJ, Wymann MP, Koneti Rao V, Lucas CL. (2019) Human PI3Kγ deficiency and its microbiota-dependent mouse model reveal immunodeficiency and tissue immunopathology. Nat Commun. 10(1):4364. doi: 10.1038/s41467-019-12311-5. PMID: 31554793

Masson GR, Williams RL. (2019) Structural Mechanisms of PTEN Regulation. Cold Spring Harb Perspect Med. pii: a036152. doi: 10.1101/cshperspect.a036152. PMID: 31636093

Inglis AJ, Masson GR, Shao S, Perisic O, McLaughlin SH, Hegde RS, Williams RL. (2019) Activation of GCN2 by the ribosomal P-stalk. Proc Natl Acad Sci U S A. 116(11):4946-4954. PMID: 30804176.

Ravenhill BJ, Boyle KB, von Muhlinen N, Ellison CJ, Masson GR, Otten EG, Foeglein A, Williams R, Randow F. (2019) The Cargo Receptor NDP52 Initiates Selective Autophagy by Recruiting the ULK Complex to Cytosol-Invading Bacteria. Mol Cell. pii: S1097-2765(19)30061-9. doi: 10.1016/j.molcel.2019.01.041. PMID: 30853402

Ohashi Y, Tremel S, Williams RL. (2019) VPS34 complexes from a structural perspective. J Lipid Res. 60(2):229-241. PMID: 30397185

Gangadhara G, Dahl G, Bohnacker T, Rae R, Gunnarsson J, Blaho S, Öster L, Lindmark H, Karabelas K, Pemberton N, Tyrchan C, Mogemark M, Wymann MP, Williams RL, Perry MWD, Papavoine T, Petersen J. (2019) A class of highly selective inhibitors bind to an active state of PI3Kγ. Nat Chem Biol. 15:348-357. PMID: 30718815.

Bunney TD, Inglis AJ, Sanfelice D, Farrell B, Kerr CJ, Thompson GS, Masson GR, Thiyagarajan N, Svergun DI, Williams RL, Breeze AL, Katan M. (2018) Disease Variants of FGFR3 Reveal Molecular Basis for the Recognition and Additional Roles for Cdc37 in Hsp90 Chaperone System. Structure. 26(3):446-458. PMID: 29478821

Tsolakos N, Durrant TN, Chessa T, Suire SM, Oxley D, Kulkarni S, Downward J, Perisic O, Williams RL, Stephens L, Hawkins PT. (2018) Quantitation of class IA PI3Ks in mice reveals p110-free-p85s and isoform-selective subunit associations and recruitment to receptors. Proc Natl Acad Sci U S A. 115(48):12176-12181 PMID: 30442661

Williams RL, Anandapadamanaban M (2017) Ragtime Regulation: Mechanism of TORC1 Activation in Nutrient Sensing. Biochemistry 56(49):6411-6412. PMID: 29185712.

Ohashi Y, Tremel S, Williams RL. (2019) VPS34 complexes from a structural perspective. J Lipid Res. 60(2):229-241. PMID: 30397185

Inglis AJ, Masson GR, Shao S, Perisic O, McLaughlin SH, Hegde RS, Williams RL. (2019) Activation of GCN2 by the ribosomal P-stalk. Proc Natl Acad Sci U S A. 116(11):4946-4954. PMID: 30804176.

Gangadhara G, Dahl G, Bohnacker T, Rae R, Gunnarsson J, Blaho S, Öster L, Lindmark H, Karabelas K, Pemberton N, Tyrchan C, Mogemark M, Wymann MP, Williams  RL, Perry MWD, Papavoine T, Petersen J. (2019) A class of highly selective inhibitors bind to an active state of PI3Kγ. Nat Chem Biol. 15:348-357. PMID: 30718815.

Bunney TD, Inglis AJ, Sanfelice D, Farrell B, Kerr CJ, Thompson GS, Masson GR, Thiyagarajan N, Svergun DI, Williams RL, Breeze AL, Katan M. (2018) Disease Variants of  FGFR3 Reveal Molecular Basis for the Recognition and Additional Roles for Cdc37 in Hsp90 Chaperone System. Structure. 26(3):446-458. PMID: 29478821

Tsolakos N, Durrant TN, Chessa T, Suire SM, Oxley D, Kulkarni S, Downward J, Perisic O, Williams RL, Stephens L, Hawkins PT. (2018) Quantitation of class IA PI3Ks in mice reveals p110-free-p85s and isoform-selective subunit associations and recruitment to receptors. Proc Natl Acad Sci U S A. 115(48):12176-12181 PMID: 30442661

Williams RL, Anandapadamanaban M (2017) Ragtime Regulation: Mechanism of TORC1 Activation in Nutrient Sensing. Biochemistry 56(49):6411-6412. PMID: 29185712.

Buckles TC, Ziemba BP, Masson GR, Williams RL, Falke JJ (2017) Single-Molecule study reveals how receptor and Ras synergistically activate PI3Ka and PIP3 Signaling. Biophys J. 113:2396-2405. PMID: 29211993.

Bohnacker T, Prota AE, Beaufils F, Burke JE, Melone A, Inglis AJ, Rageot D, Sele AM, Cmiljanovic V, Cmiljanovic N, Bargsten K, Aher A, Akhmanova A, Díaz JF, Fabbro D, Zvelebil M, Williams RL, Steinmetz MO, Wymann MP. Deconvolution of Buparlisib’s mechanism of action defines specific PI3 and tubulin inhibitors for therapeutic intervention.  (2017)  Nat Commun. 8:14683. pubmed entry

Masson GR, Maslen SL, Williams RL Analysis of phosphoinositide 3-kinase inhibitors by bottom-up electron-transfer dissociation hydrogen/deuterium exchange mass spectrometry.  (2017)  Biochem J. 474(11):1867-1877. pubmed entry

Baretic D, Pollard HK, Fisher DI, Johnson CM, Santhanam B, Truman CM, Kouba T, Fersht AR, Phillips C, Williams RL Structures of closed and open conformations of dimeric human ATM.  (2017)  Sci Adv. 10;3(5):e1700933. pubmed entry

Ziemba BP, Swisher GH, Masson G, Burke JE, Williams RL, Falke JJ Regulation of a Coupled MARCKS-PI3K Lipid Kinase Circuit by Calmodulin: Single-Molecule Analysis of a Membrane-Bound Signaling Module.  (2016)  Biochemistry . 55:6395-6405. pubmed entry

Ohashi Y, Soler N, García Ortegón M, Zhang L, Kirsten ML, Perisic O, Masson GR, Burke JE, Jakobi AJ, Apostolakis AA, Johnson CM, Ohashi M, Ktistakis NT, Sachse C, Williams RL Characterization of Atg38 and NRBF2, a fifth subunit of the autophagic Vps34/PIK3C3 complex.  (2016)  Autophagy . 2129-2144. pubmed entry

Masson GR, Perisic O, Burke JE, Williams RL The intrinsically disordered tails of PTEN and PTEN-L have distinct roles in regulating substrate specificity and membrane activity.  (2016)  Biochem J. . 473:135-144. pubmed entry

Fowler ML, McPhail JA, Jenkins ML, Masson GR, Rutaganira FU, Shokat KM, Williams RL, Burke JE Using hydrogen deuterium exchange mass spectrometry to engineer optimized constructs for crystallization of protein complexes: Case study of PI4KIIIbeta with Rab11.  (2016)  Protein Sci. . 25:826-839. pubmed entry

Masson GR, Burke JE, Williams RL Methods in the Study of PTEN Structure: X-Ray Crystallography and Hydrogen Deuterium Exchange Mass Spectrometry.  (2016)  Methods Mol Biol. . 1388:215-230. pubmed entry

Galindo A, Soler N, McLaughlin SH, Yu M, Williams RL, Munro S Structural Insights into Arl1-Mediated Targeting of the Arf-GEF BIG1 to the trans-Golgi  (2016)  Cell Rep. . 16:839-850. pubmed entry

Ziemba BP, Burke JE, Masson G, Williams RL, Falke JJ Regulation of PI3K by PKC and MARCKS: Single-Molecule Analysis of a Reconstituted Signaling Pathway.  (2016)  Biophys J. . 110(8):1811-25. pubmed entry

Baretic D, Berndt A, Ohashi Y, Johnson CM, Williams RL Tor forms a dimer through an N-terminal helical solenoid with a complex topology.  (2016)  Nat. Commun. . 7:11016. pubmed entry

Rostislavleva, K., Soler, N., Ohashi, Y., Zhang, L., Pardon, E., Burke, JE, Masson, GR, Johnson, C., Jan Steyaert, J., Ktistakis, NT, Williams, RL. Structure and flexibility of the endosomal Vps34 complex r\ eveals the basis of its function on membranes.  (2015)  Science . 350:aac7365. pubmed entry

Shnitsar, I, Bashkurov, M, Masson, GR, Ogunjimi, A, Mosessian, S, Cabeza, EA, Hirsch, CL, Trcka, D, Gish, G, Jiao, J, Wu, H, Winklbauer, R, Williams, RL, Pelletier, L, Wrana, JL, and Barrios-Rodiles, M PTEN Regulates Cilia Through Dishevelled. p (2015)  Nat. Comm. . 6:8388. pubmed entry

Shymanets A, Prajwal, Vadas O, Czupalla C, LoPiccolo J, Brenowitz M, Ghigo A, Hirsch E, Krause E, Wetzker R, Williams RL, Harteneck C, Nürnberg B. Different inhibition of Gbeta/gamma-stimulated class IB phosphoinosi\ tide 3-kinase (PI3K) variants by a monoclonal antibody. Specific function of p101 as a Gbeta/gamma-dependent regulator of PI3Kgamma enzymatic activity.  (2015)  Biochem J . 469:59-69 pubmed entry

Burke JE, Williams RL. Synergy in activating class I PI3Ks.  (2015)  Trends Biochem Sci. . 40:88-100 pubmed entry

Clarke JH, Giudici ML, Burke JE, Williams RL, Maloney DJ, Marugan J, Irvine RF. The function of phosphatidylinositol 5-phosphate 4-kinase gamma (PI5P4Kgamma) explored using a specific inhibitor that targets the PI5P\ -binding site.  (2015)  Biochem J. . 466:359-367 pubmed entry

Burke, JE, Inglis, AJ, Perisic, O,Masson, GR, McLaughlin, SH, Rutaganira, F, Shokat, KM and Williams RL. Structures of PI4KIIIbeta complexes show simultaneous recruitment of Rab11 and its effectors.  2014)  Science . 344: 1035-1038 pubmed entry

Baretic D, Williams RL. PIKKs–the solenoid nest where partners and kinases meet.  (2014)   Curr Opin Struct Biol. .29:134-142. pubmed entry

Baretic D, Williams RL. The structural basis for mTOR function.  (2014)  Cell Dev Biol. . 36:91-101. pubmed entry

Angulo I, Vadas O, Garçon F, Banham-Hall E, Plagnol V, Leahy TR, Baxendale H, Coulter T, Curtis J, Wu C, Blake-Palmer K, Perisic O, Smyth D, Maes M, Fiddler C, Juss J, Cilliers D, Markelj G, Chandra A, Farmer G, K\ ielkowska A, Clark J, Kracker S, Debré M, Picard C, Pellier I, Jabado N, Morris JA, Barcenas-Morales G, Fischer A, Stephens L, Hawkins P, Barrett JC, Abinun M, Clatworthy M, Durandy A, Doffinger R, Chilvers ER, Cant AJ,\ Kumararatne D, Okkenhaug K, Williams RL, Condliffe A, Nejentsev S. Phosphoinositide 3-kinase delta gene mutation predisposes to respiratory infection and airway damage,  (2013)  Science . 342(6160):866-871 pubmed entry

D’Angelo G, Uemura T, Chuang CC, Polishchuk E, Santoro M, Ohvo-Rekilä H, Sato T, Di Tullio G, Varriale A, D’Auria S, Daniele T, Capuani F, Johannes L, Mattjus P, Monti M, Pucci P, Williams RL, Burke JE, Platt FM, Harada A, De Matteis MA. Vesicular and non-vesicular transport feed distinct glycosylation pathways in the Golgi.  (2013)  Nature . 501:116-120 pubmed entry

Walser R, Burke JE, Gogvadze E, Bohnacker T, Zhang X, Hess D, Küenzi P, Leitges M, Hirsch E, Williams RL, Laffargue M, Wymann MP. PKCbeta phosphorylates PI3Kgamma to activate it and release it from GPCR control.  (2013)   PL\ oS Biol. . 11:e1001587 pubmed entry

Vadas O, Dbouk HA, Shymanets A, Perisic O, Burke JE, Abi Saab WF, Khalil BD, Harteneck C, Bresnick AR, Nürnberg B, Backer JM, Williams RL. Molecular determinants of PI3Kbeta-mediated activation downstream of G-protein-coupled receptors (GPCRs). (2012)   Proc Natl Acad Sci U S A . 110: 18862-18867 pubmed entry

Dbouk HA, Vadas O, Williams RL, Backer JM. PI3Kbeta downstream of GPCRs – crucial partners in oncogenesis.  (2012)   Ontarget. 3:1485-1486 pubmed entry

Burke JE, Perisic O, Williams RL. Allosteric activation of PI3Kalpha by oncogenic mutations.  (2013)   Oncotarget. . 4:180-181. pubmed entry

Burke JE, Williams RL. Connecting with an old partner in a new way.  (2013)  Cancer Cell . 23:559-561. pubmed entry

Ganesh K, van Maldegem F, Telerman SB, Simpson P, Johnson CM, Williams RL, Neuberger MS, Rada C. Structural and mutational analysis reveals that CTNNBL1 binds NLSs in a manner distinct from that of its closest armadillo-relative, karyopherin alpha  (2014)  FEBS Lett . 588:21-27 pubmed entry

Burke JE, Williams RL.  Dynamic steps in receptor tyrosine kinase mediated activation of class IA phosphoinositide 3-kinases (PI3K) captured by H/D exchange (HDX-MS).  (2012)  Adv Biol Regul . pii: S2212-4926(12)00089-9.  [Epub ahead of print].  pubmed entry, download/view pdf reprint (23194976)

Dbouk, HA*, Vadas, O*, Shymanets, A, Burke, JE, Salamon, RS, Khalil, BD, Barrett, MO, Waldo, GL, Surve, C, Hsueh, C, Perisic, O, Harteneck, C, Shepherd, PR, Harden, TK, Smrcka, AV, Taussig, R, Bresnick, AR, Nürnberg, B, Williams, RL, Backer, JM (2012) Gbetagamma Is Required for Cellular Transformation and Invasiveness. Sience Signaling 5, ra89.   pubmed entry, download/view pdf reprint

Dbouk, HA*, Vadas, O*, Shymanets, A, Burke, JE, Salamon, RS, Khalil, BD, Barrett, MO, Waldo, GL, Surve, C, Hsueh, C, Perisic, O, Harteneck, C, Shepherd, PR, Harden, TK, Smrcka, AV, Taussig, R, Bresnick, AR, Nürnberg, B, Williams, RL, Backer, JM (2012) Gbetagamma Is Required for Cellular Transformation and Invasiveness. Sience Signaling 5, ra89.   pubmed entry, download/view pdf reprint (vadas_science_signaling)

Hadders,MA, Agromayor M, Obita, T, Perisic, O, Caballe, A,  Kloc, M, Lamers, MH., Williams, RL, and Martin-Serrano, J. (2012) ESCRT-III binding protein MITD1 is involved in cytokinesis and has an unanticipated PLD fold that binds membranes. Proc Nat Acad Sciences. 109: 17424–17429.  pubmed entry, download/view pdf reprint (23045692)

Burke, JE, Perisic O, Masson GR, Vadas O, and Williams RL. (2012) Proc. Natl. Acad. Sci. USA 109(38):15259-64. Oncogenic mutations mimic and enhance dynamic events in the natural activation of phosphoinositide 3-kinase p110α (PIK3CA). pubmed entry, download/view pdf reprint

Agromayor, M*, Soler, N* Caballe, A, Kueck, K, Freund, SM, Allen, MD. Bycroft, M. Perisic, O, Ye, Y, McDonald, B, Scheel, H, Hofmann, K, Neil, SJ, Martin-Serrano, J, Williams, RL. (2012) The UBAP1 subunit of ESCRT-I interacts with ubiquitin via a novel SOUBA domain. Structure 20, 414-428. pubmed entry

 

Hon, W-C, Berndt, A. and Williams, R.L. (2012) Regulation of lipid binding underlies the activation mechanism of class IA PI3-kinases. Oncogene  31:3655-66. pubmed entry, download/view pdf reprint (22120714)

Vadas O, Burke JE, Zhang X, Berndt A and Williams R. (2011) Structural basis for activation and inhibition of class I phosphoinositide 3-kinases.Science Signaling, 4(195), re2.  pubmed entry , download/view pdf reprint)

Burke, JE, Vadas, O, Berndt, A, Finegan, T, Perisic, O, Williams, RL (2011) Dynamics of the Phosphoinositide 3-Kinase p110δ Interaction with p85α and Membranes Reveals Aspects of Regulation Distinct from p110α. Structure 19, 1127-1137. pubmed entry , download/view pdf reprint (21827948))

Zhang, X.,  Vadas, O, Perisic, O, Anderson, KE, Clark, J, Hawkins, PT, Stephens, LR, Williams, RL.  (2011) Structure of lipid kinase p110β/p85 elucidates a novel SH2-domain mediated inhibitorymechanism.  Mol. Cell 41:567-578.  pubmed entry, )

Hadders, M, Williams R (2010) Kinases charging to the membrane. Cell 143: 865-7. pubmed entry, download/view pdf reprint (21145452))

Miller S, Oleksy A, Perisic O, Williams RL (2010) Finding a fitting shoe for Cinderella: Searching for an autophagy inhibitor. Autophagy 6: 805-807.  (pubmed entry, download/view pdf reprint (20574157))

Miller S, Tavshanjian B, Oleksy A, Perisic O, Houseman BT, Shokat KM, Williams RL (2010) Shaping development of autophagy inhibitors with the structure of the lipid kinase Vps34. Science 327:1638-1642. (pubmed entry, download/view pdf reprint (20339072) )

Berndt, A, Miller, S, Williams, O, Le, DD, Houseman, BT, Pacold, JI, Gorrec, F, Hon, WC, Ren, P., Liu, Y, Rommel, C, Gaillard, P, Ruckle, T, Schwarz, MK, Shokat, KM, Shaw, JP, Williams, RL (2010) The p110 delta structure: mechanisms for selectivity and potency of new PI(3)K inhibitors. Nat Chem Biol 6: 117-124. (pubmed entry, download/view pdf reprint (20081827) )

Williams R, Berndt A, Miller S, Hon WC, Zhang X (2009) Form and flexibility in phosphoinositide 3-kinases. Biochem Soc Trans. 37:615-26. (pubmed entry, download/view pdf reprint (19614567) )

Ghazi-Tabatabai S, Obita T, Pobbati AV, Perisic O, Samson RY, Bell SD, Williams RL (2009) Evolution and assembly of ESCRTs.  Biochem Soc Trans. 37:151-155. (pubmed entry, download/view pdf reprint (18786397) )

Samson, R. Y., Obita, T., Freund, S. M., Williams, R. L., Bell, S. D. (2008) A Role for the ESCRT system in cell division in archaea. Science 322:1710-1713 (pubmed entry, download/view pdf reprint (19008417)

Ghazi-Tabatabai S, Saksena S, Short JM, Pobbati AV, Veprintsev DB, Crowther RA, Emr SD, Egelman EH, Williams RL. (2008) Structure and disassembly of filaments formed by the ESCRT-III subunit Vps24. Structure 16:1345-1356 (pubmed entry, download/view pdf reprint (18786397)

Apsel B, Blair JA, Gonzalez B, Nazif TM, Feldman ME, Aizenstein B, Hoffman R, Williams RL, Shokat KM, Knight ZA. (2008) Targeted polypharmacology: discovery of dual inhibitors of tyrosine and phosphoinositide kinases.  Nat Chem Biol. 4:691-699. (pubmed entry,download/view pdf reprint (18849971)

Obita T, Saksena S, Ghazi-Tabatabai S, Gill DJ, Perisic O, Emr SD, Williams RL. (2007) Structural basis for selective recognition of ESCRT-III by the AAA ATPase Vps4.  Nature. 449:735-739. (pubmed entry,download/view pdf reprint (17928861))

Miled N, Yan Y, Hon WC, Perisic O, Zvelebil M, Inbar Y, Schneidman-Duhovny D, Wolfson HJ, Backer JM, Williams RL. (2007) Mechanism of two classes of cancer mutations in the phosphoinositide 3-kinase catalytic subunit. Science  317:239-42. (pubmed entry, download/view pdf reprint (17626883))

Blatner,  N.R., Wilson, M.I., Lei, C., Hong, W., Murray, D., Williams, R.L., Cho, W. (2007) The structural basis of novel endosome anchoring activity of KIF16B kinesin.  EMBO J. 26:3709-3719. (pubmed entry, download/view pdf reprint)

Stahelin RV, Karathanassis D, Murray, D, Williams RL, Cho W. (2007) Structural and Membrane Binding Analysis of the PX Domain of Bem1p:

Basis of Phosphatidylinositol-4-Phosphate Specificity. J.Biol. Chem. 282:25737-25747 (pubmed entry, Download pdf reprint

Williams, R.L. and Urbe, S. (2007)  The emerging shape of the ESCRT machinery. Nat Rev Mol Cell Biol 8:355-368. (pubmed entry,download/view pdf reprint (17450176))

Tanaka T, Williams RL, Rabbitts TH (2007)   Tumour prevention by a single antibody domain targeting the interaction of signal transduction proteins with RAS.  EMBO J.  26:3250-3259. (pubmed entry,download/view pdf reprint (17568777))

Gill DJ, Teo H, Sun J, Perisic O, Veprintsev DB, Emr SD, Williams RL (2007) Structural insight into the ESCRT-I/-II link and its role in MVB trafficking. EMBO J 26: 600-612. (pubmed entry, download/view pdf reprint (17215868))

Gill DJ, Teo H, Sun J, Perisic O, Veprintsev DB, Vallis Y, Emr SD, Williams RL.  (2007) Structural studies of phosphoinositide 3-kinase-dependent traffic to multivesicular bodies. Biochem Soc Symp. 74:47-57. (pubmed entry, download/view pdf reprint (17233579_proof))

Stahelin RV, Karathanassis D, Bruzik KS, Waterfield MD, Bravo J, Williams RL, Cho W. (2006) Structural and membrane binding analysis of the PX domain of phosphoinositide 3-kinase-C2α. J. Biol. Chem. 281:39396-39406. (pubmed entry, download/view pdf reprint (17038310))

Li S, Sandercock A.M., Conduit P., Robinson C.V., Williams R.L., Kilmartin J.V.  (2006) Structural role of Sfi1p-centrin filaments in budding yeast spindle pole body duplication.  J. Cell Biol. 173:867-877. ( pubmed entry, download/view pdf reprint (16785321))

Knight, Z.A.,Gonzalez, B., Feldman, M.E., Zunder, E.R., Goldenberg,D.D.,  Williams, O.,  Loewith, R., Stokoe, D., Balla, A., Toth, B., Balla, T., Weiss,W.A., Williams, R.L., Shokat, K.M.  (2006) A pharmacological map of the PI3-K family defines a role for p110α in insulin signaling. Cell 125:733-747.(pubmed entry, download/view pdf reprint (16647110))

Teo H, Gill DJ, Sun J, Perisic O, Veprintsev DB, Vallis Y, Emr SD, Williams R.  (2006)  ESCRT-I Core and ESCRT-II GLUE Domain Structures Reveal Role for GLUE in Linking to ESCRT-I and Membranes. Cell 125:99-111.( pubmed entry, download/view pdf reprint (16615893))

Stephens L, Williams R, Hawkins P.  (2005) Phosphoinositide 3-kinases as drug targets in cancer. Curr Opin Pharmacol  5:357-365. (pubmed entry, download/view pdf reprint (15963759))

Teo, H., Perisic, O., Gonzlez, B. & Williams, R.L. (2004) ESCRT-II, an endosome-associated complex required for protein sorting: crystal structure and interactions with ESCRT-III and membranes. Dev. Cell 7: 559-569. (pubmed entry, download/view pdf reprint)

Gonzalez, B., Schell M.J., Letcher, A.J., Veprintsev, D.B., Irvine, R.F., & Williams, R.L. (2004) Structure of a human inositol 1,4,5-trisphosphate 3-kinase: Substrate binding reveals why it is not a phosphoinositide 3-kinase. Mol. Cell 15: 689-701. (pubmed entry, download/view pdf reprint)

Krugmann S., Williams R., Stephens L, & Hawkins P.T. (2004) ARAP3 is a PI3K and rap-regulated GAP for RhoA. Curr Biol.14:1380-1384. (pubmed entry, download/view pdf reprint)

Teo, H., Veprintsev, D.B. & Williams, R.L. (2004) Structural insights into ESCRT-I recognition of ubiquitinated proteins. J. Biol. Chem. 279:28689-28696. (pubmed entry, download/view pdf reprint)

Panic, B., Perisic, O., Veprintsev, D.B., Williams, R.L., Munro, S.  (2003) Structural Basis for Arl1-Dependent Targeting of Homodimeric GRIP Domains to the Golgi Apparatus.  Mol.  Cell 12: 863-874.(pubmed entry, download/view pdf reprint)

Wilson MI, Gill DJ, Perisic O, Quinn MT, Williams RL. (2003) PB1 domain-mediated heterodimerization in NADPH oxidase and signaling complexes of atypical protein kinase C with Par6 and p62. Mol Cell. 2003 12:39-50. (pubmed entry, download/view pdf reprint)

Karathanassis D, Stahelin RV, Bravo J, Perisic O, Pacold CM, Cho W, Williams RL. (2002) Binding of the PX domain of p47(phox) to phosphatidylinositol 3,4-bisphosphate and phosphatidic acid is masked by an intramolecular interaction. EMBO J.  21: 5057-5068 (pubmed entry, download/view pdf reprint)

Rodriguez R, Matsuda M, Perisic O, Bravo J, Paul A, Jones NP, Light Y, Swann K, Williams RL, Katan M. (2001) Tyrosine residues in phospholipase Cgamma 2 essential for the enzyme function in B-cell signaling. J Biol. Chem. 276: 47982-947982. (pubmed entry,download/view pdf reprint (11606584))

Bravo J, Karathanassis D, Pacold CM, Pacold ME, Ellson CD, Anders KE, Butler, PJ, Lavenir I, Perisic O, Hawkins PT, Stephens L, Williams RL.  (2001) The crystal structure of the PX domain from p40(phox) bound to phosphatidylinositol 3-Phosphate.  Mol. Cell. 8, 829-839.(pubmed entry, download/view pdf reprint)

Pacold, M.E., Suire, S., Perisic, O., Lara-Gonzalez, S., Davis, C.T., Walker, E.H., Hawkins, P.T., Stephens, L., Eccleston, J.F.,  & Williams, R.L.  (2000) Crystal structure and functional analysis of Ras binding to its effector phosphoinositide 3-kinase gamma. Cell 103: 931-943. (pubmed entry, download/view pdf reprint (11136978))

Walker, E.H., Pacold, M.E., Perisic, O., Stephens, L., Hawkins, P.T., Wymann, M.P., & Williams, R.L. (2000) Structural determnants of phosphoinositide 3-kinase inhibition by wortmannin, LY294002, quercetin, myricetin and staurosporine.  Mol. Cell 6: 909-919. (pubmed entry, download/view pdf reprint)

Warren AJ, Bravo J, Williams RL, & Rabbitts TH (2000) Structural basis for the heterodimeric interaction between the acute leukaemia-associated transcription factors AML1 and CBFbeta.  EMBO J  19: 3004-3015. (pubmed entry, download/view pdf reprint (10856244))

Walker, E.H., Perisic, O., Ried, C. Stephens, L. & Williams, R.L.  (1999) Structural insights into phosphoinositide 3-kinase catalysis and signalling.  Nature 402: 313-320. (pubmed entry, download/view pdf reprint (10580505))

Williams, R.L.  Mammalian phosphoinositide-specific phospholipase C. (1999) Biochim. Biophys. Acta  1441: 255-267. (pubmed entry,download/view pdf reprint (10570253))

Poget, S.F., Legge, G.B., Proctor, M.R., Butler, P.J.G., Bycroft, M. & Williams, R.L. (1999) The structure of a tunicate C-type lectin from Polyandrocarpa misakiensis complexed with D-galactose. J. Mol. Biol. 290: 867-879. (pubmed entry, download/view pdf reprint (10398588))

Holliger, P., Riechmann, L. & Williams, R.L. (1999) Crystal structure of the two N-terminal domains of g3p from filamentous phage fd at 1.9 Ã… : evidence  for conformational lability. J. Mol. Biol. 288: 649-657. (pubmed entry, download/view pdf reprint (10329170))

Perisic, O., Paterson, H.F., Mosedale, G., Lara-Gonzalez, S. & Williams, R.L. (1999) Mapping the phospholipid binding surface and translocation determinants of the C2 domain from cytosolic phospholipase A2.  J. Biol. Chem. 274: 14979-14987. (pubmed entry, download/view pdf reprint (10329700))

Roberts, M.F., Wu, Y., Perisic, O., Williams, R.L. & Katan, M. (1999) Sequential mechanism and allosteric activation of phosphoinositide-specific phospholipase C-delta1.  In  Phosphoinisitides: Chemistry, Biochemistry and Biomedical Applications, K. Bruzik, Ed. ACS Symp. Ser. 718: 137-155.

Essen, L.-O., Brownlie, P.D. , Perisic, O. , Katan, M. & Williams, R.L. (1999) Structural analysis of the catalysis and membrane association of PLC-delta In Phosphoinisitides: Chemistry, Biochemistry and Biomedical Applications, K. Bruzik, Ed. ACS Symp. Ser. 718: 121-136.Â

Davletov, B., Perisic, O., Williams, R.L.  (1998) Calcium-dependent membrane penetration is a hallmark of the C2 domain of cytosolic phospholipase A2 whereas the C2A domain of synaptotagmin binds membranes electrostatically.  J. Biol. Chem. 273 19093-19096. (pubmed entry, download/view pdf reprint (9668093))

Perisic O, Fong S, Lynch DE, Bycroft M, Williams RL (1998) Crystal structure of a calcium-phospholipid binding domain from cytosolic phospholipase A2.  J. Biol. Chem. 273:1596-604. (pubmed entry,download/view pdf reprint (9430701))

Ellis, M.V., James, S.R., Perisic, O., Downes, C.P., Williams, R.L. Katan, M. (1998) Catalytic domain of phosphoinositide-specific phospholipase C. J. Mol. Biol. 275: 635-650. (pubmed entry, download/view pdf reprint (9565585))

Heinz, D.W., Essen, L.-O., Williams, R.L. Structural and mechanistic comparison of prokaryotic and eukaryotic phosphoinositide-specific phospholipases C. J. Mol. Biol. (1998) J. Mol. Biol. 275: 635-650. (pubmed entry, download/view pdf reprint (9466937))

Wu, Y., Perisic, O.,Katan, Williams, R.L., Roberts, M.F. (1997) Phosphoinositide-specific phospholipase Cd1 activity towards micellar substrates, inositol 1,2-cyclic phosphate and other water soluble substrates: a sequential mechanism and allosteric activation. Biochemistry 36: 11223-11233. (pubmed entry, download/view pdf reprint (9287165))

Pei, X.Y., Holliger, P., Murzin, A.G., Williams, R.L. (1997) The 2 A resolution crystal structure of a trimeric antibody fragment with non-cognate VH/VL domain pairs shows a rearrangement of VH CDR3. Proc. Natl. Acad. Sci. USA 94: 9637-9642. (pubmed entry, download/view pdf reprint (9275175))

Katan, M., Williams, R.L. (1997) Phosphoinositide-specific phospholipase C: Structural basis for catalysis and regulatory interactions. Seminars in Cell & Develop. Biol. 8, 287-296. (pubmed entry, download/view pdf reprint (10024492))

Essen, L.-O., Perisic, O., Lynch, D.E., Katan, M., Williams, R.L. (1997) A ternary metal binding site in the C2 domain of phosphoinositide-specific phospholipase C-delta1. Biochemistry 36, 2753-2762. (pubmed entry,download/view pdf reprint (9062102))

Essen, L.-O., Perisic, O., Katan, M., Wu, Y., Roberts, M.F., Williams, R.L. (1997) Structural mapping of the catalytic mechanism for a mammalian phosphoinositide-specific phospholipase C. (1997) Biochemistry 36: 1704-1718. (pubmed entry, download/view pdf reprint (9048554))

Williams, R.L., Katan, M. (1996) Structural views of phosphoinositide-specific phospholipase C: signalling the way ahead. Structure 4: 1387-1394. (pubmed entry)

Essen, L.-O., Perisic, O., Cheung, R., Katan, M., Williams, R.L. (1996) Crystal structure of a mammalian phosphoinositide-specific phospholipase Cdelta. Nature 380: 595-602. (pubmed entry)Â

Holliger, P., Brissinck, J.,Williams, R.L., Thielemans, K., Winter, G. (1996) Specific killing of lymphoma cells by cytotoxic T-cells mediated by a bispecific diabody. Prot. Eng. 9: 299-305. (pubmed entry)

Paterson, H.F., Savopoulos, J.W., Perisic, O., Cheung, R., Ellis, M.V., Williams, R.L, Katan, M. (1995) Phospholipase Cdelta1 requires a PH domain for interaction with the plasma membrane. Biochem. J. 312: 661-666. (pubmed entry). 

Webb, P.A., Perisic, O., Mendola, C.E., Backer, J.M.,Williams, R.L (1995) The crystal structure of a human nucleoside diphosphate kinase, NM23-H2. J. Mol. Biol. 251: 574-587. (pubmed entry)

Strelkov, S.V., Perisic, O., Webb, P.A., Williams, R.L (1995) The 1.9 Ã… crystal structure of a nucleoside diphosphate kinase complex with 3′,5′-cyclic monophosphate: Evidence for competitive inhibition. J. Mol. Biol. 249: 665-674. (pubmed entry)

De La Rosa, A., Williams, R.L, Steeg, P.S. (1995) Nm23/nucleoside diphosphate kinase: Toward a structural and biochemical understanding of its biological functions. BioEssays, 17: 53-62. (pubmed entry)

Perisic, O., Webb, P.A., Holliger, P., Winter, G.,Williams, R.L. (1994) Crystal structure of a diabody, a bivalent antibody fragment. Structure 2: 1217-1226. (pubmed entry)

Williams, R.L, Oren, D.A., Muñoz-Dorado, J., Inouye, S., Inouye, M. & Arnold, E. (1993) Crystal structure of Myxococcus xanthus nucleoside diphosphate kinase and its interaction with a nucleotide substrate at 2.0 Å resolution. J. Mol. Biol., 234: 1230-1247. (pubmed entry)

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Roger L. Williams,  FMedSci, FRS
Group Leader
MRC Laboratory of Molecular Biology
Francis Crick Avenue
Cambridge CB2 0QH, UK
Phone: +44-1223 267094
FAX: +44-1223 268305

e-mail rlw@mrc-lmb.cam.ac.uk

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