PTEN functions by recruitment to cytoplasmic vesicles

Molecular Cell

Volumn 58, Issue 2, 2015, Pages 255-268

  Naguib, Adam ^a   Bencze, Gyula ^a   Cho, Hyejin ^a   Zheng, Wu ^a   Tocilj, Ante ^a,b   Elkayam, Elad ^a,b,c   Faehnle, Christopher R ^a,b   Jaber, Nadia ^d   Pratt, Christopher P ^a   Chen, Muhan ^a   Zong, Wei Xing ^d   Marks, Michael S ^e,f   Joshua Tor, Leemor ^a,b,c   Pappin, Darryl J ^a   Trotman, Lloyd C ^a  

^a Simons Center for Quantitative Biology   (United States)

^b W M Keck Structural Biology Laboratory   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d STONY BROOK UNIVERSITY   (United States)

^e CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^f UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBONYL REDUCTASE; NOCODAZOLE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 PHOSPHATE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; SMALL INTERFERING RNA; POLYPHOSPHOINOSITIDE; PTEN PROTEIN, MOUSE;

ANIMAL CELL; ANTIBODY DETECTION; ARTICLE; BINDING SITE; CELL MEMBRANE; CONTROLLED STUDY; CRYSTAL STRUCTURE; EMBRYO; ENDOSOME; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; FEMALE; FLUORESCENCE ACTIVATED CELL SORTING; HELA CELL LINE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; INSECT CELL; LOSS OF FUNCTION MUTATION; MEMBRANE VESICLE; MICROTUBULE; MOUSE; NONHUMAN; PROTEIN DEPHOSPHORYLATION; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; SURFACE PROPERTY; 3T3 CELL LINE; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; ENZYMOLOGY; METABOLISM; PROTEIN SECONDARY STRUCTURE; TRANSPORT VESICLE;

ANIMALS; BINDING SITES; MICE; MICROTUBULES; MODELS, MOLECULAR; NIH 3T3 CELLS; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHATIDYLINOSITOL PHOSPHATES; PROTEIN STRUCTURE, SECONDARY; PTEN PHOSPHOHYDROLASE; SIGNAL TRANSDUCTION; TRANSPORT VESICLES;

EID: 84928212368     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2015.03.011     Document Type: Article

References (68)

1. Alimonti A., Carracedo A., Clohessy J.G., Trotman L.C., Nardella C., Egia A., Salmena L., Sampieri K., Haveman W.J., Brogi E., et al. Subtle variations in Pten dose determine cancer susceptibility. Nat. Genet. 2010, 42:454-458.
2. Backer J.M. The regulation and function of Class III PI3Ks: novel roles for Vps34. Biochem. J. 2008, 410:1-17.
3. Berger A.H., Knudson A.G., Pandolfi P.P. A continuum model for tumour suppression. Nature 2011, 476:163-169.
4. Bravo J., Karathanassis D., Pacold C.M., Pacold M.E., Ellson C.D., Anderson K.E., Butler P.J., Lavenir I., Perisic O., Hawkins P.T., et al. The crystal structure of the PX domain from p40(phox) bound to phosphatidylinositol 3-phosphate. Mol. Cell 2001, 8:829-839.
5. Butler M.G., Dasouki M.J., Zhou X.P., Talebizadeh Z., Brown M., Takahashi T.N., Miles J.H., Wang C.H., Stratton R., Pilarski R., Eng C. Subset of individuals with autism spectrum disorders and extreme macrocephaly associated with germline PTEN tumour suppressor gene mutations. J.Med. Genet. 2005, 42:318-321.
6. Campbell R.B., Liu F., Ross A.H. Allosteric activation of PTEN phosphatase by phosphatidylinositol 4,5-bisphosphate. J.Biol. Chem. 2003, 278:33617-33620.
7. Cerami E., Gao J., Dogrusoz U., Gross B.E., Sumer S.O., Aksoy B.A., Jacobsen A., Byrne C.J., Heuer M.L., Larsson E., et al. The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov. 2012, 2:401-404.
8. Chen Z., Trotman L.C., Shaffer D., Lin H.K., Dotan Z.A., Niki M., Koutcher J.A., Scher H.I., Ludwig T., Gerald W., et al. Crucial role of p53-dependent cellular senescence in suppression of Pten-deficient tumorigenesis. Nature 2005, 436:725-730.
9. Chen M., Pratt C.P., Zeeman M.E., Schultz N., Taylor B.S., O'Neill A., Castillo-Martin M., Nowak D.G., Naguib A., Grace D.M., et al. Identification of PHLPP1 as a tumor suppressor reveals the role of feedback activation in PTEN-mutant prostate cancer progression. Cancer Cell 2011, 20:173-186.
10. Chen M., Nowak D.G., Trotman L.C. Molecular pathways: PI3K pathway phosphatases as biomarkers for cancer prognosis and therapy. Clin. Cancer Res. 2014, 20:3057-3063.
11. Di Cristofano A., De Acetis M., Koff A., Cordon-Cardo C., Pandolfi P.P. Pten and p27KIP1 cooperate in prostate cancer tumor suppression in the mouse. Nat. Genet. 2001, 27:222-224.
12. Di Paolo G., De Camilli P. Phosphoinositides in cell regulation and membrane dynamics. Nature 2006, 443:651-657.
13. Dippold H.C., Ng M.M., Farber-Katz S.E., Lee S.K., Kerr M.L., Peterman M.C., Sim R., Wiharto P.A., Galbraith K.A., Madhavarapu S., et al. GOLPH3 bridges phosphatidylinositol-4- phosphate and actomyosin to stretch and shape the Golgi to promote budding. Cell 2009, 139:337-351.
14. Dowler S., Kular G., Alessi D.R. Protein lipid overlay assay. Sci. STKE 2002, 2002:pl6.
15. Engelman J.A., Luo J., Cantley L.C. The evolution of phosphatidylinositol 3-kinases as regulators of growth and metabolism. Nat. Rev. Genet. 2006, 7:606-619.
16. Farkas T., Daugaard M., Jäättelä M. Identification of small molecule inhibitors of phosphatidylinositol 3-kinase and autophagy. J.Biol. Chem. 2011, 286:38904-38912.
17. Fayard E., Xue G., Parcellier A., Bozulic L., Hemmings B.A. Protein kinase B (PKB/Akt), a key mediator of the PI3K signaling pathway. Curr. Top. Microbiol. Immunol. 2010, 346:31-56.
18. Fedele C.G., Ooms L.M., Ho M., Vieusseux J., O'Toole S.A., Millar E.K., Lopez-Knowles E., Sriratana A., Gurung R., Baglietto L., et al. Inositol polyphosphate 4-phosphatase II regulates PI3K/Akt signaling and is lost in human basal-like breast cancers. Proc. Natl. Acad. Sci. USA 2010, 107:22231-22236.
19. Flint A.J., Tiganis T., Barford D., Tonks N.K. Development of "substrate-trapping" mutants to identify physiological substrates of protein tyrosine phosphatases. Proc. Natl. Acad. Sci. USA 1997, 94:1680-1685.
20. Fotin A., Cheng Y., Grigorieff N., Walz T., Harrison S.C., Kirchhausen T. Structure of an auxilin-bound clathrin coat and its implications for the mechanism of uncoating. Nature 2004, 432:649-653.
21. Funderburk S.F., Wang Q.J., Yue Z. The Beclin 1-VPS34 complex-at the crossroads of autophagy and beyond. Trends Cell Biol. 2010, 20:355-362.
22. Gaullier J.M., Simonsen A., D'Arrigo A., Bremnes B., Stenmark H., Aasland R. FYVE fingers bind PtdIns(3)P. Nature 1998, 394:432-433.
23. Georgescu M.M., Kirsch K.H., Kaloudis P., Yang H., Pavletich N.P., Hanafusa H. Stabilization and productive positioning roles of the C2 domain of PTEN tumor suppressor. Cancer Res. 2000, 60:7033-7038.
24. Gewinner C., Wang Z.C., Richardson A., Teruya-Feldstein J., Etemadmoghadam D., Bowtell D., Barretina J., Lin W.M., Rameh L., Salmena L., et al. Evidence that inositol polyphosphate 4-phosphatase type II is a tumor suppressor that inhibits PI3K signaling. Cancer Cell 2009, 16:115-125.
25. Guan R., Dai H., Harrison S.C., Kirchhausen T. Structure of the PTEN-like region of auxilin, a detector of clathrin-coated vesicle budding. Structure 2010, 18:1191-1198.
26. Hickson I., Zhao Y., Richardson C.J., Green S.J., Martin N.M., Orr A.I., Reaper P.M., Jackson S.P., Curtin N.J., Smith G.C. Identification and characterization of a novel and specific inhibitor of the ataxia-telangiectasia mutated kinase ATM. Cancer Res. 2004, 64:9152-9159.
27. Hodgkin M.N., Masson M.R., Powner D., Saqib K.M., Ponting C.P., Wakelam M.J. Phospholipase D regulation and localisation is dependent upon a phosphatidylinositol 4,5-biphosphate-specific PH domain. Curr. Biol. 2000, 10:43-46.
28. Hollander M.C., Blumenthal G.M., Dennis P.A. PTEN loss in the continuum of common cancers, rare syndromes and mouse models. Nat. Rev. Cancer 2011, 11:289-301.
29. Howitt J., Lackovic J., Low L.H., Naguib A., Macintyre A., Goh C.P., Callaway J.K., Hammond V., Thomas T., Dixon M., et al. Ndfip1 regulates nuclear Pten import invivo to promote neuronal survival following cerebral ischemia. J.Cell Biol. 2012, 196:29-36.
30. Jaber N., Dou Z., Chen J.S., Catanzaro J., Jiang Y.P., Ballou L.M., Selinger E., Ouyang X., Lin R.Z., Zhang J., Zong W.X. Class III PI3K Vps34 plays an essential role in autophagy and in heart and liver function. Proc. Natl. Acad. Sci. USA 2012, 109:2003-2008.
31. Johnson E.E., Overmeyer J.H., Gunning W.T., Maltese W.A. Gene silencing reveals a specific function of hVps34 phosphatidylinositol 3-kinase in late versus early endosomes. J.Cell Sci. 2006, 119:1219-1232.
32. Kim J.S., Lee C., Bonifant C.L., Ressom H., Waldman T. Activation of p53-dependent growth suppression in human cells by mutations in PTEN or PIK3CA. Mol. Cell. Biol. 2006, 7:662-677.
33. Kwabi-Addo B., Giri D., Schmidt K., Podsypanina K., Parsons R., Greenberg N., Ittmann M. Haploinsufficiency of the Pten tumor suppressor gene promotes prostate cancer progression. Proc. Natl. Acad. Sci. USA 2001, 98:11563-11568.
34. Kwon C.H., Luikart B.W., Powell C.M., Zhou J., Matheny S.A., Zhang W., Li Y., Baker S.J., Parada L.F. Pten regulates neuronal arborization and social interaction in mice. Neuron 2006, 50:377-388.
35. Lee J.O., Yang H., Georgescu M.M., Di Cristofano A., Maehama T., Shi Y., Dixon J.E., Pandolfi P., Pavletich N.P. Crystal structure of the PTEN tumor suppressor: implications for its phosphoinositide phosphatase activity and membrane association. Cell 1999, 99:323-334.
36. Lee D.W., Wu X., Eisenberg E., Greene L.E. Recruitment dynamics of GAK and auxilin to clathrin-coated pits during endocytosis. J.Cell Sci. 2006, 119:3502-3512.
37. Lemmon M.A. Membrane recognition by phospholipid-binding domains. Nat. Rev. Mol. Cell Biol. 2008, 9:99-111.
38. Leslie N.R., Foti M. Non-genomic loss of PTEN function in cancer: not in my genes. Trends Pharmacol. Sci. 2011, 32:131-140.
39. Li J., Yen C., Liaw D., Podsypanina K., Bose S., Wang S.I., Puc J., Miliaresis C., Rodgers L., McCombie R., et al. PTEN, a putative protein tyrosine phosphatase gene mutated in human brain, breast, and prostate cancer. Science 1997, 275:1943-1947.
40. Liaw D., Marsh D.J., Li J., Dahia P.L., Wang S.I., Zheng Z., Bose S., Call K.M., Tsou H.C., Peacocke M., et al. Germline mutations of the PTEN gene in Cowden disease, an inherited breast and thyroid cancer syndrome. Nat. Genet. 1997, 16:64-67.
41. Liu Y., Bankaitis V.A. Phosphoinositide phosphatases in cell biology and disease. Prog. Lipid Res. 2010, 49:201-217.
42. Maehama T., Dixon J.E. The tumor suppressor, PTEN/MMAC1, dephosphorylates the lipid second messenger, phosphatidylinositol 3,4,5-trisphosphate. J.Biol. Chem. 1998, 273:13375-13378.
43. Massol R.H., Boll W., Griffin A.M., Kirchhausen T. A burst of auxilin recruitment determines the onset of clathrin-coated vesicle uncoating. Proc. Natl. Acad. Sci. USA 2006, 103:10265-10270.
44. McConnachie G., Pass I., Walker S.M., Downes C.P. Interfacial kinetic analysis of the tumour suppressor phosphatase, PTEN: evidence for activation by anionic phospholipids. Biochem. J. 2003, 371:947-955.
45. Mester J., Eng C. When overgrowth bumps into cancer: the PTEN-opathies. Am. J. Med. Genet. C. Semin. Med. Genet. 2013, 163C:114-121.
46. Miaczynska M., Christoforidis S., Giner A., Shevchenko A., Uttenweiler-Joseph S., Habermann B., Wilm M., Parton R.G., Zerial M. APPL proteins link Rab5 to nuclear signal transduction via an endosomal compartment. Cell 2004, 116:445-456.
47. Naguib A., Trotman L.C. PTEN plasticity: how the taming of a lethal gene can go too far. Trends Cell Biol. 2013, 23:374-379.
48. Orchiston E.A., Bennett D., Leslie N.R., Clarke R.G., Winward L., Downes C.P., Safrany S.T. PTEN M-CBR3, a versatile and selective regulator of inositol 1,3,4,5,6-pentakisphosphate (Ins(1,3,4,5,6)P5). Evidence for Ins(1,3,4,5,6)P5 as a proliferative signal. J.Biol. Chem. 2004, 279:1116-1122.
49. Patki V., Lawe D.C., Corvera S., Virbasius J.V., Chawla A. Afunctional PtdIns(3)P-binding motif. Nature 1998, 394:433-434.
50. Petiot A., Faure J., Stenmark H., Gruenberg J. PI3P signaling regulates receptor sorting but not transport in the endosomal pathway. J.Cell Biol. 2003, 162:971-979.
51. Platta H.W., Stenmark H. Endocytosis and signaling. Curr. Opin. Cell Biol. 2011, 23:393-403.
52. Razidlo G.L., Katafiasz D., Taylor G.S. Myotubularin regulates Akt-dependent survival signaling via phosphatidylinositol 3-phosphate. J.Biol. Chem. 2011, 286:20005-20019.
53. Schink K.O., Raiborg C., Stenmark H. Phosphatidylinositol 3-phosphate, a lipid that regulates membrane dynamics, protein sorting and cell signalling. Bioessays 2013, 35:900-912.
54. Schu P.V., Takegawa K., Fry M.J., Stack J.H., Waterfield M.D., Emr S.D. Phosphatidylinositol 3-kinase encoded by yeast VPS34 gene essential for protein sorting. Science 1993, 260:88-91.
55. Song M.S., Salmena L., Pandolfi P.P. The functions and regulation of the PTEN tumour suppressor. Nat. Rev. Mol. Cell Biol. 2012, 13:283-296.
56. Steck P.A., Pershouse M.A., Jasser S.A., Yung W.K., Lin H., Ligon A.H., Langford L.A., Baumgard M.L., Hattier T., Davis T., et al. Identification of a candidate tumour suppressor gene, MMAC1, at chromosome 10q23.3 that is mutated in multiple advanced cancers. Nat. Genet. 1997, 15:356-362.
57. Taylor G.S., Maehama T., Dixon J.E. Myotubularin, a protein tyrosine phosphatase mutated in myotubular myopathy, dephosphorylates the lipid second messenger, phosphatidylinositol 3-phosphate. Proc. Natl. Acad. Sci. USA 2000, 97:8910-8915.
58. Taylor B.S., Schultz N., Hieronymus H., Gopalan A., Xiao Y., Carver B.S., Arora V.K., Kaushik P., Cerami E., Reva B., et al. Integrative genomic profiling of human prostate cancer. Cancer Cell 2010, 18:11-22.
59. Trotman L.C., Niki M., Dotan Z.A., Koutcher J.A., Di Cristofano A., Xiao A., Khoo A.S., Roy-Burman P., Greenberg N.M., Van Dyke T., et al. Pten dose dictates cancer progression in the prostate. PLoS Biol. 2003, 1:E59.
60. Trotman L.C., Alimonti A., Scaglioni P.P., Koutcher J.A., Cordon-Cardo C., Pandolfi P.P. Identification of a tumour suppressor network opposing nuclear Akt function. Nature 2006, 441:523-527.
61. Trotman L.C., Wang X., Alimonti A., Chen Z., Teruya-Feldstein J., Yang H., Pavletich N.P., Carver B.S., Cordon-Cardo C., Erdjument-Bromage H., et al. Ubiquitination regulates PTEN nuclear import and tumor suppression. Cell 2007, 128:141-156.
62. Vanhaesebroeck B., Stephens L., Hawkins P. PI3K signalling: the path to discovery and understanding. Nat. Rev. Mol. Cell Biol. 2012, 13:195-203.
63. Varga E.A., Pastore M., Prior T., Herman G.E., McBride K.L. The prevalence of PTEN mutations in a clinical pediatric cohort with autism spectrum disorders, developmental delay, and macrocephaly. Genet. Med. 2009, 11:111-117.
64. Walker S.M., Leslie N.R., Perera N.M., Batty I.H., Downes C.P. The tumour-suppressor function of PTEN requires an N-terminal lipid-binding motif. Biochem. J. 2004, 379:301-307.
65. Wang X., Trotman L.C., Koppie T., Alimonti A., Chen Z., Gao Z., Wang J., Erdjument-Bromage H., Tempst P., Cordon-Cardo C., et al. NEDD4-1 is a proto-oncogenic ubiquitin ligase for PTEN. Cell 2007, 128:129-139.
66. Xiong Q., Oviedo H.V., Trotman L.C., Zador A.M. PTEN regulation of local and long-range connections in mouse auditory cortex. J.Neurosci. 2012, 32:1643-1652.
67. Yang X., Ongusaha P.P., Miles P.D., Havstad J.C., Zhang F., So W.V., Kudlow J.E., Michell R.H., Olefsky J.M., Field S.J., Evans R.M. Phosphoinositide signalling links O-GlcNAc transferase to insulin resistance. Nature 2008, 451:964-969.
68. Zoncu R., Perera R.M., Balkin D.M., Pirruccello M., Toomre D., De Camilli P. A phosphoinositide switch controls the maturation and signaling properties of APPL endosomes. Cell 2009, 136:1110-1121.