PTEN enters the nucleus by diffusion

Journal of Cellular Biochemistry

Volumn 96, Issue 2, 2005, Pages 221-234

  Liu, Fenghua ^a,b   Wagner, Stefan ^a   Campbell, Robert B ^a,c   Nickerson, Jeffrey A ^a   Schiffer, Celia A ^a   Ross, Alonzo H ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c Charles River Discovery and Development Services   (United States)

Author keywords

FRAP; Nucleus; Phosphatase; Phosphatidylinositol; Signal transduction

Indexed keywords

COMPLEMENTARY DNA; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; PHOSPHATASE; PHOSPHATIDYLINOSITOL; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE;

ANIMAL CELL; ARTICLE; CANCER CELL CULTURE; CELL NUCLEUS; CELLULAR DISTRIBUTION; DNA SEQUENCE; ENZYME ACTIVITY; ENZYME ASSAY; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; HELA CELL; HUMAN; HUMAN CELL; KIDNEY CELL; MOLECULAR WEIGHT; NONHUMAN; PLASMID; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

CELL LINE, TUMOR; CELL NUCLEUS; DIFFUSION; HUMANS; MICROSCOPY, FLUORESCENCE; MOLECULAR WEIGHT; MUTATION; PHOSPHORIC MONOESTER HYDROLASES; PROTEIN TRANSPORT; RECOMBINANT PROTEINS;

EID: 26444498071     PISSN: 07302312     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcb.20525     Document Type: Article

References (76)

1. Ahn JY, Rong R, Liu X, Ye K. 2004. PIKE/nuclear PI 3-kinase signaling mediates the antiapoptotic actions of NGF in the nucleus. Embo J 23:3995-4006.
2. Anderson MT, Tjioe IM, Lorincz MC, Parks DR, Herzenberg LA, Nolan GP. 1996. Simultaneous fluorescence-activated cell sorter analysis of two distinct transcriptional elements within a single cell using engineered green fluorescent proteins. Proc Natl Acad Sci USA 93:8508-8511.
3. Andjelkovic M, Alessi DR, Meier R, Fernandez A, Lamb NJC, Frech M, Cron P, Cohen P, Lucocq JM, Hemmings BA. 1997. Role of translocation in the activation and function of protein kinase B. J Biol Chem 272:31515-31524.
4. Baake M, Bauerle M, Doenecke D, Albig W. 2001. Core histones and linker histones are imported into the nucleus by different pathways. Eur J Cell Biol 80:669-677.
5. Backman S, Stambolic V, Mak T. 2002. PTEN function in mammalian cell size regulation. Curr Opin Neurobiol 12:516-522.
6. Balla T, Bondeva T, Varnai P. 2000. How accurately can we image inositol lipids in living cells? Trends Pharmacol Sci 21:238-241.
7. Bjornsti MA, Houghton PJ. 2004. The tor pathway: A target for cancer therapy. Nat Rev Cancer 4:335-348.
8. Boronenkov IV, Loijens JC, Umeda M, Anderson RA. 1998. Phosphoinositide signaling pathways in nuclei are associated with nuclear speckles containing pre-mRNA processing factors. Mol Biol Cell 9:3547-3560.
9. Boulikas T. 1993. Nuclear localization signals (NLS). Crit Rev Eukaryotic Gene Expression 3:193-227.
10. Brunet A, Roux D, Lenormand P, Dowd S, Keyse S, Pouyssegur J. 1999. Nuclear translocation of p42/p44 mitogen-activated protein kinase is required for growth factor-induced gene expression and cell cycle entry. Embo J 18:664-674.
11. Campbell RB, Liu F, Ross AH. 2003. Allosteric activation of PTEN phosphatase by phosphatidylinositol 4,5-bisphosphate. J Biol Chem 278:33617-33620.
12. Caramelli E, Matteucci A, Zini N, Carini C, Guidotti L, Ricci D, Maraldi NM, Capitani S. 1996. Nuclear phosphoinositide-specific phopholipase C, phosphatidylinositol 4,5-bisphosphate and protein kinase C during rat spermatogenesis. Eur J Cell Biol 71:154-164.
13. Chen R, Kang VH, Chen J, Shope JC, Torabinejad J, DeWald DB, Prestwich GD. 2002. A monoclonal antibody to visualize PtdIns(3,4,5)P3 in cells. J Histochem Cytochem 50:697-708.
14. Czech MP. 2000. PIP2 and PIP3: Complex roles at the cell surface. Cell 100:603-606.
15. Davies MA, Koul D, Dhesi H, Berman R, McDonnell TJ, McConkey D, Yung WK, Steck PA. 1999. Regulation of Akt/PKB activity, cellular growth, and apoptosis in prostate carcinoma cells by MMAC/PTEN. Cancer Res 59:2551-2556.
16. Freeman DJ, Li AG, Wei G, Li HH, Kertesz N, Lesche R, Whale AD, Martinez-Diaz H, Rozengurt N, Cardiff RD, Liu X, Wu H. 2003. PTEN tumor suppressor regulates p53 protein levels and activity through phosphatase-dependent and-independent mechanisms. Cancer Cell 3:117-130.
17. Fukuda M, Gotoh Y, Nishida E. 1997. Interaction of MAP kinase with MAP kinase kinase: Its possible role in the control of nucleocytoplasmic transport of MAP kinase. Embo J 16:1901-1908.
18. Furnari FB, Lin H, Huang H-JS, Cavenee WK. 1997. Growth suppression of glioma cells by PTEN requires a functional phosphatase catalytic domain. Proc Natl Acad Sci USA 94:12479-12484.
19. Furnari FB, Huang H-JS, Cavenee WK. 1998. The phosphoinositol phosphatase activity of PTEN mediates a serum-sensitive G1 growth arrest in glioma cells. Cancer Res 58:5002-5008.
20. Gimm O, Perren A, Weng LP, Marsh DJ, Yeh JJ, Ziebold U, Gil E, Hinze R, Delbridge L, Lees JA, Mutter GL, Robinson BG, Komminoth P, Dralle H, Eng C. 2000. Differential nuclear and cytoplasmic expression of PTEN in normal thyroid tissue, and benign and malignant epithelial thyroid tumors. Am J Pathol 156:1693-1700.
21. Ginn-Pease ME, Eng C. 2003. Increased nuclear phosphatase and tensin homologue deleted on chromosome 10 is associated with G0-G1 in mcf-7 cells. Cancer Res 63:282-286.
22. Gozani O, Karuman P, Jones DR, Ivanov D, Cha J, Lugovskoy AA, Baird CL, Zhu H, Field SJ, Lessnick SL, Villasenor J, Mehrotra B, Chen J, Rao VR, Brugge JS, Ferguson CG, Payrastre B, Myszka DG, Cantley LC, Wagner G, Divecha N, Prestwich GD, Yuan J. 2003. The PHD finger of the chromatin-associated protein ING2 functions as a nuclear phosphoinositide receptor. Cell 114:99-111.
23. Gu J, Tamura M, Yamada KM. 1998. Tumor suppressor PTEN inhibits integrin- and growth factor-mediated mitogen-activated protein (MAP) kinase signaling pathways. J Cell Biol 143:1375-1383.
24. Holway AH, Rieger-Christ KM, Miner WR, Cain JW, Dugan JM, Pezza JA, Silverman ML, Shapter A, McLellan R, Summerhayes IC. 2000. Somatic mutation of PTEN in vulvar cancer. Clin Cancer Res 6:3228-3235.
25. Iijima M, Devreotes P. 2002. Tumor suppressor PTEN mediates sensing of chemoattractant gradients. Cell 109:599-610.
26. 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.
27. Ishii N, Maier D, Merlo A, Tada M, Sawamura Y, Diserens AC, Van Meir EG. 1999. Frequent co-alterations of TP53, p16/CDKN2A, p14ARF, PTEN tumor suppressor genes in human glioma cell lines. Brain Pathol 9:469-479.
28. Jäkel S, Albig W, Kutay U, Bischoff FR, Schwamborn K, Doenecke D, Görlich D. 1999. The importin b/importin 7 heterodimer is a functional nuclear import receptor for histone H1. Embo J 18:2411-2423.
29. Kurz M, Doenecke D, Albig W. 1997. Nuclear transport of H1 histones meets the criteria of a nuclear localization signal-mediated process. J Cell Biochem 64:573-578.
30. Lachyankar MB, Sultana N, Schonhoff CM, Mitra P, Poluha W, Lambert S, Quesenberry PJ, Litofsky NS, Recht LD, Nabi R, Miller SJ, Ohta S, Neel BG, Ross AH. 2000. A role for nuclear PTEN in neuronal differentiation. J Neurosci 20:1404-1413.
31. Lee J-O, Yang H, Georgescu M-M, Di Cristofano A, Maehama T, Shi Y, Dixon JE, Pandolfi P, Pavletich NP. 1999. Crystal structure of the PTEN tumor suppressor: Implications for its phosphoinositide phosphatase activity and membrane association. Cell 99:323-334.
32. Li D-M, Sun H. 1997. TEP1, encoded by a candidate tumor suppressor locus, is a novel protein tyrosine phosphatase regulated by transforming growth factor β. Cancer Res 57:2124-2129.
33. Li J, Yen C, Liaw D, Podsypanina K, Bose S, Wang SI, Puc J, Miliaresis C, Rodgers L, McCombie R, Bigner SH, Giovanella BC, Ittmann M, Tycko B, Hibshoosh H, Wigler MH, Parsons R. 1997. PTEN, a putative protein tyrosine phosphatase gene mutated in human brain, breast, and prostate cancer. Science 275:1943-1947.
34. Li L, Liu F, Salmonsen RA, Turner TK, Litofsky NS, Di Cristofano A, Pandolfi PP, Jones SN, Recht LD, Ross AH. 2002. PTEN in neural precursor cells: Regulation of migration, apoptosis, and proliferation. Mol Cell Neurosci 20:21-29.
35. Liliental J, Moon SY, Lesche R, Mamillapalli R, Li D, Zheng Y, Sun H, Wu H. 2000. Genetic deletion of the Pten tumor suppressor gene promotes cell motility by activation of Rac1 and Cdc42 GTPases. Curr Biol 10:401-404.
36. Lu P-J, Hsu A-L, Wang D-S, Yan HY, Yin HL, Chen C-S. 1998. Phosphoinositide 3-kinase in rat liver nuclei. Biochemistry 37:5738-5745.
37. Maehama T, Dixon JE. 1998. The tumor suppressor, PTEN/MMAC1, dephosphorylates the lipid second messenger, phosphatidylinositol 3,4,5-triphosphate. J Biol Chem 273:13375-13378.
38. Maehama T, Taylor GS, Slama JT, Dixon JE. 2000. A sensitive assay for phosphoinositide phosphatases. Anal Biochem 279:248-250.
39. Manzoli L, Billi AM, Rubbini S, Bavelloni A, Faenza I, Gilmour RS, Rhee S-G, Cocco L. 1997. Essential role for nuclear phospholipase C β1 in insulin-like growth factor I-induced mitogenesis. Cancer Res 57:2137-2139.
40. Marshall JG, Booth JW, Stambolic V, Mak T, Balla T, Schreiber AD, Meyer T, Grinstein S. 2001. Restricted accumulation of phosphatidylinositol 3-kinase products in a plasmalemmal subdomain during Fcg receptor-mediated phagocytosis. J Cell Biol 153:1369-1380.
41. Mazzotti G, Zini N, Rizzi E, Rizzoli R, Galanzi A, Ognibene A, Santi S, Matteucci A, Martelli AM, Maraldi NM. 1995. Immunocytochemical detection of phosphatidylinositol 4,5-bisphosphate localization sites within the nucleus. J Histochem Cytochem 43:181-191.
42. 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.
43. McLaughlin S, Wang J, Gambhir A, Murray D. 2002. PIP2 and proteins: Interactions, organization, and information flow. Annu Rev Biophys Biomol Struct 31:151-175.
44. Meier R, Alessi DR, Cron P, Andjelkovic M, Hemmings BA. 1997. Mitogenic activation, phosphorylation, and nuclear translocation of protein kinase BB. J Biol Chem 272:30491-30497.
45. Mohamed AJ, Vargas L, Nore BF, Backesjo CM, Christensson B, Smith CI. 2000. Nucleocytoplasmic shuttling of Bruton's tyrosine kinase. J Biol Chem 275:40614-40619.
46. Myers MP, Pass I, Batty IH, Van der Kaay J, Stolarov JP, Hemmings BA, Wigler MH, Downes CP, Tonks NK. 1998. The lipid phosphatase activity of PTEN is critical for its tumor suppressor function. Proc Natl Acad Sci USA 95:13513-13518.
47. Neri LM, Borgatti P, Capitani S, Martelli AM. 1998. Nuclear diacylglycerol produced by phosphoinositide-specific phospholipase C is responsible for nuclear translocation of protein kinase C-a. J Biol Chem 273:29738-29744.
48. Perren A, Komminoth P, Saremaslani P, Matter C, Feurer S, Lees JA, Heitz PU, Eng C. 2000. Mutation and expression analyses reveal differential subcellular compartmentalization of PTEN in endocrine pancreatic tumors compared to normal islet cells. Am J Pathol 157:1097-1103.
49. Peters R. 1986. Fluorescence microphotolysis to measure nucleocytoplasmic transport and intracellular mobility. Biochim Biophys Acta 864:305-359.
50. Phair RD, Misteli T. 2000. High mobility of proteins in the mammalian cell nucleus. Nature 404:604-609.
51. 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.
52. Sano T, Lin H, Chen X, Langford LA, Koul D, Bondy ML, Hess KR, Myers JN, Hong YK, Yung WK, Steck PA. 1999. Differential expression of MMAC/PTEN in glioblastoma multiforme: Relationship to localization and prognosis. Cancer Res 59:1820-1824.
53. Sato M, Ueda Y, Takagi T, Umezawa Y. 2003. Production of PtdInsP(3) at endomembranes is triggered by receptor endocytosis. Nat Cell Biol 5:1016-1022.
54. Shibasaki F, Price ER, Milan D, McKeon F. 1996. Role of kinases and the phosphatase calcineurin in the nuclear shuttling of transcription factor NF-AT4. Nature 382:370-373.
55. Shibayama S, Shibata-Seita R, Miura K, Kirino Y, Takishima K. 2002. Identification of a C-terminal region that is required for the nuclear translocation of ERK2 by passive diffusion. J Biol Chem 277:37777-37782.
56. Shoman N, Klassen S, McFadden A, Bickis MG, Torlakovic E, Chibbar R. 2005. Reduced PTEN expression predicts relapse in patients with breast carcinoma treated by tamoxifen. Mod Pathol 18:250-259.
57. Simpson L, Parsons R. 2001. PTEN: Life as a tumor suppressor. Exp Cell Res 264:29-41.
58. Siomi H, Dreyfuss G. 1995. A nuclear localization domain in the hnRNP A1 protein. J Cell Biol 129:551-560.
59. Stacey DW, Allfrey VG. 1984. Microinjection studies of protein transit across the nuclear envelope of human cells. Exp Cell Res 154:283-292.
60. Steck PA, Pershouse MA, Jasser SA, Yung WKA, Lin H, Ligon AH, Langford LA, Baumgard ML, Hattier T, Davis T, Frye C, Hu R, Swedlund B, Teng DHF, Tavtigian SV. 1997. Identification of a candidate tumour suppressor gene, MMAC1, at chromosome 10q23.3 that is mutated in multiple advanced cancers. Nature Genetics 15:356-362.
61. Su JD, Mayo LD, Donner DB, Durden DL. 2003. PTEN and phosphatidylinositol 3′-kinase inhibitors up-regulate p53 and block tumor-induced angiogenesis: Evidence for an effect on the tumor and endothelial compartment. Cancer Res 63:3585-3592.
62. Sun B, Murray NR, Fields AP. 1997. A role for nuclear phosphatidylinositol-specific phospholipase C in the G2/M phase transition. J Biol Chem 272:26313-26317.
63. Tachibana T, Imamoto N, Seino H, Nishimoto T, Yoneda Y. 1994. Loss of RCC1 leads to suppression of nuclear protein import in living cells. J Biol Chem 269:24542-24545.
64. Tachibana M, Shibakita M, Ohno S, Kinugasa S, Yoshimura H, Ueda S, Fujii T, Rahman MA, Dhar DK, Nagasue N. 2002. Expression and prognostic significance of PTEN product protein in patients with esophageal squamous cell carcinoma. Cancer 94:1955-1960.
65. Tanaka K, Horiguchi K, Yoshida T, Takeda M, Fujisawa H, Takeuchi K, Umeda M, Kato S, Ihara S, Nagata S, Fukui Y. 1999. Evidence that a phosphatidylinositol 3,4,5-triphosphate-binding protein can function in nucleus. J Biol Chem 274:3919-3922.
66. Tsao H, Mihm MC, Jr., Sheehan C. 2003. PTEN expression in normal skin, acquired melanocytic nevi, and cutaneous melanoma. J Am Acad Dermatol 49:865-872.
67. 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.
68. Wei X, Henke VG, Strubing C, Brown EB, Clapham DE. 2003. Real-time imaging of nuclear permeation by EGFP in single intact cells. Biophys J 84:1317-1327.
69. Wheelock MJ, Johnson KR. 2003. Cadherin-mediated cellular signaling. Curr Opin Cell Biol 15:509-514.
70. Whiteman DC, Zhou XP, Cummings MC, Pavey S, Hayward NK, Eng C. 2002. Nuclear PTEN expression and clinicopathologic features in a population- based series of primary cutaneous melanoma. Int J Cancer 99:63-67.
71. Wishart MJ, Dixon JE. 2002. PTEN and myotubularin phosphatases: From 3-phosphoinositide dephosphorylation to disease. Trends Cell Biol 12:579-585.
72. Zhang P, Steinberg BM. 2000. Overexpression of PTEN/MMAC1 and decreased activation of Akt in human papillomavirus-infected laryngeal papillomas. Cancer Res 60:1457-1462.
73. Zhao K, Wang W, Rando OJ, Xue Y, Swiderek K, Kuo A, Crabtree GR. 1998. Rapid and phosphoinositol-dependent binding of the SWI/SNF-like BAF complex to chromatin after T lymphocyte receptor signaling. Cell 95:625-636.
74. Zhou XP, Loukola A, Salovaara R, Nystrom-Lahti M, Peltomaki P, de la Chapelle A, Aaltonen LA, Eng C. 2002. PTEN mutational spectra, expression levels, and subcellular localization in microsatellite stable and unstable colorectal cancers. Am J Pathol 161:439-447.
75. Zini N, Ognibene A, Bavelloni A, Santi S, Sabatelli P, Baldini N, Scotlandi K, Serra M, Maraldi NM. 1996. Cytoplasmic and nuclear localization sites of phosphatidylinositol 3-kinase in human osteosarcoma sensitive and multidrug-resistant Saos-2 cells. Histochem Cell Biol 106:457-464.
76. Zuniga A, Torres J, Ubeda J, Pulido R. 1999. Interaction of mitogen-activated protein kinases with the kinase interaction motif of the tyrosine phosphatase PTP-SL provides substrate specificity and retains ERK2 in the cytoplasm. J Biol Chem 274:21900-21907.