Suppression of cellular proliferation and invasion by the concerted lipid and protein phosphatase activities of PTEN

Oncogene

Volumn 29, Issue 5, 2010, Pages 687-697

  Davidson, L ^a   MacCario, H ^a   Perera, N M ^a   Yang, X ^a,b   Spinelli, L ^a   Tibarewal, P ^a   Glancy, B ^a   Gray, A ^a   Weijer, C J ^a   Downes, C P ^a   Leslie, N R ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b MEDICAL COLLEGE OF JINAN UNIVERSITY   (China)

Author keywords

Akt; Cancer; Phosphoinositide; PI3 kinase; PTEN; TPIP

Indexed keywords

LIPID; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN;

ARTICLE; CANCER CELL CULTURE; CELL INVASION; CELL PROLIFERATION; CELL STRAIN HEK293; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME MECHANISM; GLIOBLASTOMA; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION;

CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; HUMANS; LIPID METABOLISM; PROTEINS; PTEN PHOSPHOHYDROLASE; SIGNAL TRANSDUCTION;

EID: 76349098001     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2009.384     Document Type: Article

References (49)

1. Campbell RB, Liu F, Ross AH. (2003). Allosteric activation of PTEN phosphatase by phosphatidylinositol 4,5-bisphosphate. J Biol Chem 278: 33617-33620.
2. Cheney IW, Johnson DE, Vaillancourt MT, Avanzini J, Morimoto A, Demers GW, et al. (1998). Suppression of tumorigenicity of glioblastoma cells by adenovirus-mediated MMAC1/PTEN gene transfer. Cancer Res 58: 2331-2334.
3. Chow LM, Baker SJ. (2006). PTEN function in normal and neoplastic growth. Cancer Lett 241: 184-196.
4. Das S, Dixon JE, Cho W. (2003). Membrane-binding and activation mechanism of PTEN. Proc Natl Acad Sci USA 100: 7491-7496.
5. Davies MA, Lu Y, Sano T, Fang X, Tang P, LaPushin R, et al. (1998). Adenoviral transgene expression of MMAC/PTEN in human glioma cells inhibits Akt activation and induces anoikis. Cancer Res 58: 5285-5290.
6. de Bouard S, Christov C, Guillamo JS, Kassar-Duchossoy L, Palfi S, Leguerinel C, et al. (2002). Invasion of human glioma biopsy specimens in cultures of rodent brain slices: a quantitative analysis. J Neurosurg 97: 169-176.
7. Deleu S, Choi K, Pesesse X, Cho J, Sulis ML, Parsons R, et al. (2006). Physiological levels of PTEN control the size of the cellular Ins(1,3,4,5,6)P(5) pool. Cell Signal 18: 488-498.
8. Dey N, Crosswell HE, De P, Parsons R, Peng Q, Su JD, et al. (2008). The protein phosphatase activity of PTEN regulates SRC family kinases and controls glioma migration. Cancer Res 68: 1862-1871.
9. Freeman DJ, Li AG, Wei G, Li HH, Kertesz N, Lesche R, et al. (2003). PTEN tumor suppressor regulates p53 protein levels and activity through phosphatase-dependent and-independent mechanisms. Cancer Cell 3: 117-130.
10. Furnari FB, Huang HJ, Cavenee WK. (1998). The phosphoinositol phosphatase activity of PTEN mediates a serum-sensitive G1 growth arrest in glioma cells. Cancer Res 58: 5002-5008.
11. Furnari FB, Lin H, Huang HS, Cavenee WK. (1997). Growth suppression of glioma cells by PTEN requires a functional phosphatase catalytic domain. Proc Natl Acad Sci USA 94: 12479-12484.
12. Gil A, Andres-Pons A, Pulido R. (2007). Nuclear PTEN: a tale of many tails. Cell Death Differ 14: 395-399.
13. Gildea JJ, Herlevsen M, Harding MA, Gulding KM, Moskaluk CA, Frierson HF, et al. (2004). PTEN can inhibit in vitro organotypic and in vivo orthotopic invasion of human bladder cancer cells even in the absence of its lipid phosphatase activity. Oncogene 23: 6788-6797.
14. Goldbrunner RH, Bernstein JJ, Tonn JC. (1998). ECM-mediated glioma cell invasion. Microsc Res Tech 43: 250-257.
15. Gray A, Olsson H, Batty IH, Priganica L, Peter Downes C. (2003). Nonradioactive methods for the assay of phosphoinositide 3-kinases and phosphoinositide phosphatases and selective detection of signaling lipids in cell and tissue extracts. Anal Biochem 313: 234-245.
16. Gu J, Tamura M, Pankov R, Danen EH, Takino T, Matsumoto K, et al. (1999). Shc and FAK differentially regulate cell motility and directionality modulated by PTEN. J Cell Biol 146: 389-404.
17. Hjelmeland AB, Hjelmeland MD, Shi Q, Hart JL, Bigner DD, Wang XF, et al. (2005). Loss of phosphatase and tensin homologue increases transforming growth factor beta-mediated invasion with enhanced SMAD3 transcriptional activity. Cancer Res 65: 11276-11281.
18. Iijima M, Huang YE, Luo HR, Vazquez F, Devreotes PN. (2004). Novel mechanism of PTEN regulation by its phosphatidylinositol 4,5-bisphosphate binding motif is critical for chemotaxis. J Biol Chem 279: 16606-16613.
19. Ikeda Y, Takeuchi Y, Martin F, Cosset FL, Mitrophanous K, Collins M. (2003). Continuous high-titer HIV-1 vector production. Nat Biotechnol 21: 569-572.
20. Ji SP, Zhang Y, Van Cleemput J, Jiang W, Liao M, Li L, et al. (2006). Disruption of PTEN coupling with 5-HT2C receptors suppresses behavioral responses induced by drugs of abuse. Nat Med 12: 324-329.
21. Keniry M, Parsons R. (2008). The role of PTEN signaling perturbations in cancer and in targeted therapy. Oncogene 27: 5477-5485.
22. Lackey J, Barnett J, Davidson L, Batty IH, Leslie NR, Downes CP. (2007). Loss of PTEN selectively desensitizes upstream IGF1 and insulin signaling. Oncogene 26: 7132-7142.
23. Lee JO, Yang H, Georgescu MM, Di Cristofano A, Maehama T, Shi Y, et al. (1999). Crystal structure of the PTEN tumor suppressor: implications for its phosphoinositide phosphatase activity and membrane association. Cell 99: 323-334.
24. Leslie NR, Batty IH, Maccario H, Davidson L, Downes CP. (2008). Understanding PTEN regulation: PIP2, polarity and protein stability. Oncogene 27: 5464-5476.
25. Leslie NR, Yang X, Downes CP, Weijer CJ. (2007). PtdIns(3,4,5)P(3)- dependent and-independent roles for PTEN in the control of cell migration. Curr Biol 17: 115-125.
26. Liaw D, Marsh DJ, Li J, Dahia PL, Wang SI, Zheng Z, et al. (1997). Germline mutations of the PTEN gene in Cowden disease, an inherited breast and thyroid cancer syndrome. Nat Genet 16: 64-67. (Pubitemid 27198157)
27. Maccario H, Perera NM, Davidson L, Downes CP, Leslie NR. (2007). PTEN is destabilized by phosphorylation on Thr366. Biochem J 405: 439-444.
28. Mahimainathan L, Choudhury GG. (2004). Inactivation of platelet-derived growth factor receptor by the tumor suppressor PTEN provides a novel mechanism of action of the phosphatase. J Biol Chem 279: 15258-15268.
29. McConnachie G, Pass I, Walker SM, Downes CP. (2003). Interfacial kinetic analysis of the tumour suppressor phosphatase, PTEN: evidence for activation by anionic phospholipids. Biochem J 371: 947-955.
30. Myers MP, Pass I, Batty IH, Van der Kaay J, Stolarov JP, Hemmings BA, et al. (1998). The lipid phosphatase activity of PTEN is critical for its tumor supressor function. Proc Natl Acad Sci USA 95: 13513-13518.
31. Myers MP, Stolarov JP, Eng C, Li J, Wang SI, Wigler MH, et al. (1997). P-TEN, the tumor suppressor from human chromosome 10q23, is a dual-specificity phosphatase. Proc Natl Acad Sci USA 94: 9052-9057.
32. Ning K, Miller LC, Laidlaw HA, Burgess LA, Perera NM, Downes CP, et al. (2006). A novel leptin signalling pathway via PTEN inhibition in hypothalamic cell lines and pancreatic beta-cells. EMBO J 25: 2377-2387.
33. Okumura K, Zhao M, Depinho RA, Furnari FB, Cavenee WK. (2005). Cellular transformation by the MSP58 oncogene is inhibited by its physical interaction with the PTEN tumor suppressor. Proc Natl Acad Sci USA 102: 2703-2706.
34. Orchiston EA, Bennett D, Leslie NR, Clarke RG, Winward L, Downes CP, et al. (2004). 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 279: 1116-1122.
35. Park MJ, Kim MS, Park IC, Kang HS, Yoo H, Park SH, et al. (2002). PTEN suppresses hyaluronic acid-induced matrix metalloprotei-nase-9 expression in U87MG glioblastoma cells through focal adhesion kinase dephosphorylation. Cancer Res 62: 6318-6322.
36. Raftopoulou M, Etienne-Manneville S, Self A, Nicholls S, Hall A. (2004). Regulation of cell migration by the C2 domain of the tumor suppressor PTEN. Science 303: 1179-1181.
37. Redfern RE, Redfern D, Furgason ML, Munson M, Ross AH, Gericke A. (2008). PTEN phosphatase selectively binds phosphoi-nositides and undergoes structural changes. Biochemistry 47: 2162-2171.
38. Salmena L, Carracedo A, Pandolfi PP. (2008). Tenets of PTEN tumor suppression. Cell 133: 403-414.
39. Sansal I, Sellers WR. (2004). The biology and clinical relevance of the PTEN tumor suppressor pathway. J Clin Oncol 22: 2954-2963.
40. Shen WH, Balajee AS, Wang J, Wu H, Eng C, Pandolfi PP, et al. (2007). Essential role for nuclear PTEN in maintaining chromosomal integrity. Cell 128: 157-170.
41. Suzuki A, Nakano T, Mak TW, Sasaki T. (2008). Portrait of PTEN: messages from mutant mice. Cancer Sci 99: 209-213.
42. Tamura M, Gu J, Matsumoto K, Aota S, Parsons R, Yamada KM. (1998). Inhibition of cell migration, spreading, and focal adhesions by tumor suppressor PTEN. Science 280: 1614-1617.
43. Tapparel C, Reymond A, Girardet C, Guillou L, Lyle R, Lamon C, et al. (2003). The TPTE gene family: cellular expression, subcellular localization and alternative splicing. Gene 323: 189-199.
44. Trotman LC, Wang X, Alimonti A, Chen Z, Teruya-Feldstein J, Yang H, et al. (2007). Ubiquitination regulates PTEN nuclear import and tumor suppression. Cell 128: 141-156.
45. Vazquez F, Grossman SR, Takahashi Y, Rokas MV, Nakamura N, Sellers WR. (2001). Phosphorylation of the PTEN tail acts as an inhibitory switch by preventing its recruitment into a protein complex. J Biol Chem 276: 48627-48630.
46. Vogelmann R, Nguyen-Tat MD, Giehl K, Adler G, Wedlich D, Menke A. (2005). TGFbeta-induced downregulation of E-cadherin-based cell-cell adhesion depends on PI3-kinase and PTEN. J Cell Sci 118: 4901-4912.
47. Walker SM, Downes CP, Leslie NR. (2001). TPIP: a novel phosphoinositide 3-phosphatase. Biochem J 360: 277-283.
48. Walker SM, Leslie NR, Perera NM, Batty IH, Downes CP. (2004). The tumour-suppressor function of PTEN requires an N-terminal lipid-binding motif. Biochem J 379: 301-307.
49. Yang X, Dormann D, Munsterberg AE, Weijer CJ. (2002). Cell movement patterns during gastrulation in the chick are controlled by positive and negative chemotaxis mediated by FGF4 and FGF8. Dev Cell 3: 425-437.