Human cancer, PTEN and the PI-3 kinase pathway

Seminars in Cell and Developmental Biology

Volumn 15, Issue 2, 2004, Pages 171-176

  Parsons, Ramon ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

Human cancer; PI 3 kinase; PTEN

Indexed keywords

PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; RAPAMYCIN;

CANCER; CANCER CHEMOTHERAPY; CANCER INHIBITION; CARCINOGENESIS; CHROMOSOME 10; CLINICAL TRIAL; ENZYME ACTIVATION; EPIGENETICS; HUMAN; MUTATION; NONHUMAN; PROTEIN DOMAIN; REGULATORY MECHANISM; REVIEW; RNA TRANSLATION;

EID: 1342342989     PISSN: 10849521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.semcdb.2003.12.021     Document Type: Article

References (75)

1. Whitman M., Kaplan D.R., Schaffhausen B., Cantley L., Roberts T.M. Association of phosphatidylinositol kinase activity with polyoma middle-T competent for transformation. Nature. 315:1985;239-242.
2. Ling L.E., Druker B.J., Cantley L.C., Roberts T.M. Transformation- defective mutants of polyomavirus middle T antigen associate with phosphatidylinositol 3-kinase (PI 3-kinase) but are unable to maintain wild-type levels of PI 3-kinase products in intact cells. J. Virol. 66:1992;1702-1708.
3. Webster M.A., Hutchinson J.N., Rauh M.J., Muthuswamy S.K., Anton M., Tortorice C.G.et al. Requirement for both Shc and phosphatidylinositol 3′ kinase signaling pathways in polyomavirus middle T-mediated mammary tumorigenesis. Mol. Cell Biol. 18:1998;2344-2359.
4. Moscatello D.K., Holgado-Madruga M., Emlet D.R., Montgomery R.B., Wong A.J. Constitutive activation of phosphatidylinositol 3-kinase by a naturally occurring mutant epidermal growth factor receptor. J. Biol. Chem. 273:1998;200-206.
5. Carraway K.L. III, Soltoff S.P., Diamonti A.J., Cantley L.C. Heregulin stimulates mitogenesis and phosphatidylinositol 3-kinase in mouse fibroblasts transfected with erbB2/neu and erbB3. J. Biol. Chem. 270:1995;7111-7116.
6. Rodriguez-Viciana P., Warne P.H., Dhand R., Vanhaesebroeck B., Gout I., Fry M.J.et al. Phosphatidylinositol-3-OH kinase as a direct target of Ras. Nature. 370:1994;527-532.
7. Varticovski L., Daley G.Q., Jackson P., Baltimore D., Cantley L.C. Activation of phosphatidylinositol 3-kinase in cells expressing abl oncogene variants. Mol. Cell Biol. 11:1991;1107-1113.
8. Chang H.W., Aoki M., Fruman D., Auger K.R., Bellacosa A., Tsichlis P.N. et al. Transformation of chicken cells by the gene encoding the catalytic subunit of PI 3-kinase. Science. 276:1997;1848-1850.
9. Staal S.P., Hartley J.W. Thymic lymphoma induction by the AKT8 murine retrovirus. J. Exp. Med. 167:1988;1259-1264.
10. Shayesteh L., Lu Y., Kuo W.L., Baldocchi R., Godfrey T., Collins C.et al. PIK3CA is implicated as an oncogene in ovarian cancer [see comments]. Nat. Genet. 21:1999;99-102.
11. Woenckhaus J., Steger K., Werner E., Fenic I., Gamerdinger U., Dreyer T.et al. Genomic gain of PIK3CA and increased expression of p110alpha are associated with progression of dysplasia into invasive squamous cell carcinoma. J. Pathol. 198:2002;335-342.
12. Cheng J.Q., Godwin A.K., Bellacosa A., Taguchi T., Franke T.F., Hamilton T.C.et al. AKT2, a putative oncogene encoding a member of a subfamily of protein-serine/threonine kinases, is amplified in human ovarian carcinomas. Proc. Natl. Acad. Sci. U.S.A. 89:1992;9267-9271.
13. Cheng J.Q., Ruggeri B., Klein W.M., Sonoda G., Altomare D.A., Watson D.K.et al. Amplification of AKT2 in human pancreatic cells and inhibition of AKT2 expression and tumorigenicity by antisense RNA. Proc. Natl. Acad. Sci. U.S.A. 93:1996;3636-3641.
14. Philp A.J., Campbell I.G., Leet C., Vincan E., Rockman S.P., Whitehead R.H.et al. The phosphatidylinositol 3′-kinase p85alpha gene is an oncogene in human ovarian and colon tumors. Cancer Res. 61:2001;7426-7429.
15. Sulis M.L., Parsons R. PTEN: from pathology to biology. Trends Cell Biol. 13:2003;478-483.
16. Wishart M.J., Dixon J.E. PTEN and myotubularin phosphatases: from 3-phosphoinositide dephosphorylation to disease. Phosphatase and tensin homolog deleted on chromosome ten. Trends Cell Biol. 12:2002;579-585.
17. Luo J., Manning B.D., Cantley L.C. Targeting the PI3K-Akt pathway in human cancer: rationale and promise. Cancer Cell. 4:2003;257-262.
18. Vivanco I., Sawyers C.L. The phosphatidylinositol 3-Kinase AKT pathway in human cancer. Nat. Rev. Cancer. 2:2002;489-501.
19. Bigner S.H., Mark J., Burger P.C., Mahaley M.S., Bullard D.E., Muhlbaier L.H.et al. Specific chromosomal abnormalities in malignant human gliomas. Cancer Res. 48:1988;405-411.
20. James C.D., Carlbom E., Dumanski J.P., Hansen M., Nordenskjold M., Collins V.P.et al. Clonal genomic alterations in glioma malignancy stages. Cancer Res. 48:1988;5546-5551.
21. Herbst R.A., Weiss J., Ehnis A., Cavenee W.K., Arden K.C. Loss of heterozygosity for 10q22-10qter in malignant melanoma progression. Cancer Res. 54:1994;3111-3114.
22. Peiffer S.L., Herzog T.J., Tribune D.J., Mutch D.G., Gersell D.J., Goodfellow P.J. Allelic loss of sequences from the long arm of chromosome 10 and replication errors in endometrial cancers. Cancer Res. 55:1995;1922-1926.
23. Ittmann M. Allelic loss on chromosome 10 in prostate adenocarcinoma. Cancer Res. 56:1996;2143-2147.
24. Petersen S., Wolf G., Bockmuhl U., Gellert K., Dietel M., Petersen I. Allelic loss on chromosome 10q in human lung cancer: association with tumour progression and metastatic phenotype. Br. J. Cancer. 77:1998;270-276.
25. Bose S., Wang S.I., Terry M.B., Hibshoosh H., Parsons R. Allelic loss of chromosome 10q23 is associated with tumor progression in breast carcinomas. Oncogene. 17:1998;123-127.
26. Hsu S.C., Volpert O.V., Steck P.A., Mikkelsen T., Polverini P.J., Rao S.et al. Inhibition of angiogenesis in human glioblastomas by chromosome 10 induction of thrombospondin-1. Cancer Res. 56:1996;5684-5691.
27. Ichikawa T., Nihei N., Kuramochi H., Kawana Y., Killary A.M., Rinker Schaeffer C.W.et al. Metastasis suppressor genes for prostate cancer. Prostate Suppl. 6:1996;31-35.
28. Nelen M.R., Padberg G.W., Peeters E.A., Lin A.Y., van den Helm B., Frants R.R.et al. Localization of the gene for Cowden disease to chromosome 10q22-23. Nat. Genet. 13:1996;114-116.
29. Li J., Yen C., Liaw D., Podsypanina K., Bose S., Wang S.I.et al. PTEN, a putative protein tyrosine phosphatase gene mutated in human brain, breast, and prostate cancer [see comments]. Science. 275:1997;1943-1947.
30. Steck P.A., Pershouse M.A., Jasser S.A., Yung W.K., Lin H., Ligon A.H.et al. Identification of a candidate tumour suppressor gene, MMAC1, at chromosome 10q23.3 that is mutated in multiple advanced cancers. Nat. Genet. 15:1997;356-362.
31. Liaw D., Marsh D.J., Li J., Dahia P.L., Wang S.I., Zheng Z.et al. Germline mutations of the PTEN gene in Cowden disease, an inherited breast and thyroid cancer syndrome. Nat. Genet. 16:1997;64-67.
32. Levine R.L., Cargile C.B., Blazes M.S., van Rees B., Kurman R.J., Ellenson L.H. PTEN mutations and microsatellite instability in complex atypical hyperplasia, a precursor lesion to uterine endometrioid carcinoma. Cancer Res. 58:1998;3254-3258.
33. Rasheed B.K., Stenzel T.T., McLendon R.E., Parsons R., Friedman A.H., Friedman H.S.et al. PTEN gene mutations are seen in high-grade but not in low-grade gliomas. Cancer Res. 57:1997;4187-4190.
34. Cairns P., Okami K., Halachmi S., Halachmi N., Esteller M., Herman J.G. et al. Frequent inactivation of PTEN/MMAC1 in primary prostate cancer. Cancer Res. 57:1997;4997-5000.
35. Dicuonzo G., Angeletti S., Garcia-Foncillas J., Brugarolas A., Okrouzhnov Y., Santini D.et al. Colorectal carcinomas and PTEN/MMAC1 gene mutations. Clin. Cancer Res. 7:2001;4049-4053.
36. Harima Y., Sawada S., Nagata K., Sougawa M., Ostapenko V., Ohnishi T. Mutation of the PTEN gene in advanced cervical cancer correlated with tumor progression and poor outcome after radiotherapy. Int. J. Oncol. 18:2001;493-497.
37. Hahn M., Wieland I., Koufaki O.N., Gorgens H., Sobottka S.B., Schackert G.et al. Genetic alterations of the tumor suppressor gene PTEN/MMAC1 in human brain metastases. Clin. Cancer Res. 5:1999;2431-2437.
38. Suzuki H., Freije D., Nusskern D.R., Okami K., Cairns P., Sidransky D., Isaacs W.B., Bova G.S. Interfocal heterogeneity of PTEN/MMAC1 gene alterations in multiple metastatic prostate cancer tissues. Cancer Res. 58:1998;204-209.
39. Sakai A., Thieblemont C., Wellmann A., Jaffe E.S., Raffeld M. PTEN gene alterations in lymphoid neoplasms. Blood. 92:1998;3410-3415.
40. Butler M.P., Wang S.I., Chaganti R.S., Parsons R., Dalla-Favera R. Analysis of PTEN mutations and deletions in B-cell non-Hodgkin's lymphomas. Genes Chromosomes Cancer. 24:1999;322-327.
41. Soria J.C., Lee H.Y., Lee J.I., Wang L., Issa J.P., Kemp B.L.et al. Lack of PTEN expression in non-small cell lung cancer could be related to promoter methylation. Clin. Cancer Res. 8:2002;1178-1184.
42. Mutter G.L., Lin M.C., Fitzgerald J.T., Kum J.B., Baak J.P., Lees J.A.et al. Altered PTEN expression as a diagnostic marker for the earliest endometrial precancers. J. Natl. Cancer Inst. 92:2000;924-930.
43. Perren A., Weng L.P., Boag A.H., Ziebold U., Thakore K., Dahia P.L.et al. Immunohistochemical evidence of loss of PTEN expression in primary ductal adenocarcinomas of the breast. Am. J. Pathol. 155:1999;1253-1260.
44. Bose S., Crane A., Hibshoosh H., Mansukhani M., Sandweis L., Parsons R. Reduced expression of PTEN correlates with breast cancer progression. Hum. Pathol. 33:2002;405-409.
45. Kurose K., Zhou X.P., Araki T., Cannistra S.A., Maher E.R., Eng C. Frequent loss of PTEN expression is linked to elevated phosphorylated Akt levels, but not associated with p27 and cyclin D1 expression, in primary epithelial ovarian carcinomas. Am. J. Pathol. 158:2001;2097-2106.
46. McMenamin M.E., Soung P., Perera S., Kaplan I., Loda M., Sellers W.R. Loss of PTEN expression in paraffin-embedded primary prostate cancer correlates with high Gleason score and advanced stage. Cancer Res. 59:1999;4291-4296.
47. Zhou X.P., Loukola A., Salovaara R., Nystrom-Lahti M., Peltomaki P., de la Chapelle A.et al. PTEN mutational spectra, expression levels, and subcellular localization in microsatellite stable and unstable colorectal cancers. Am. J. Pathol. 161:2002;439-447.
48. Zhou X.P., Gimm O., Hampel H., Niemann T., Walker M.J., Eng C. Epigenetic PTEN silencing in malignant melanomas without PTEN mutation. Am. J. Pathol. 157:2000;1123-1128.
49. Whiteman D.C., Zhou X.P., Cummings M.C., Pavey S., Hayward N.K., Eng C. Nuclear PTEN expression and clinicopathologic features in a population-based series of primary cutaneous melanoma. Int. J. Cancer. 99:2002;63-67.
50. Depowski P.L., Rosenthal S.I., Ross J.S. Loss of expression of the PTEN gene protein product is associated with poor outcome in breast cancer. Mod. Pathol. 14:2001;672-676.
51. Sano T., Lin H., Chen X., Langford L.A., Koul D., Bondy M.L.et al. Differential expression of MMAC/PTEN in glioblastoma multiforme: relationship to localization and prognosis. Cancer Res. 59:1999;1820-1824.
52. Lee J.I., Soria J.C., Hassan K.A., El-Naggar A.K., Tang X., Liu D.D.et al. Loss of PTEN expression as a prognostic marker for tongue cancer. Arch. Otolaryngol. Head Neck Surg. 127:2001;1441-1445.
53. Lee H.S., Lee H.K., Kim H.S., Yang H.K., Kim W.H. Tumour suppressor gene expression correlates with gastric cancer prognosis. J. Pathol. 200:2003;39-46.
54. Tachibana M., Shibakita M., Ohno S., Kinugasa S., Yoshimura H., Ueda S. et al. Expression and prognostic significance of PTEN product protein in patients with esophageal squamous cell carcinoma. Cancer. 94:2002;1955-1960.
55. Terakawa N., Kanamori Y., Yoshida S. Loss of PTEN expression followed by Akt phosphorylation is a poor prognostic factor for patients with endometrial cancer. Endocr. Relat. Cancer. 10:2003;203-208.
56. Leupin N., Cenni B., Novak U., Hugli B., Graber H.U., Tobler A.et al. Disparate expression of the PTEN gene: a novel finding in B-cell chronic lymphocytic leukaemia (B-CLL). Br. J. Haematol. 121:2003;97-100.
57. Cheong J.W., Eom J.I., Maeng H.Y., Lee S.T., Hahn J.S., Ko Y.W.et al. Phosphatase and tensin homologue phosphorylation in the C-terminal regulatory domain is frequently observed in acute myeloid leukaemia and associated with poor clinical outcome. Br. J. Haematol. 122:2003;454-456.
58. Whang Y.E., Wu X., Suzuki H., Reiter R.E., Tran C., Vessella R.L.et al. Inactivation of the tumor suppressor PTEN/MMAC1 in advanced human prostate cancer through loss of expression. Proc. Natl. Acad. Sci. U.S.A. 95:1998;5246-5250.
59. Zysman M.A., Chapman W.B., Bapat B. Considerations when analyzing the methylation status of PTEN tumor suppressor gene. Am. J. Pathol. 160:2002;795-800.
60. Baeza N., Weller M., Yonekawa Y., Kleihues P., Ohgaki H. PTEN methylation and expression in glioblastomas. Acta Neuropathol. (Berl.). 106:2003;479-485.
61. Podsypanina K., Ellenson L.H., Nemes A., Gu J., Tamura M., Yamada K.M.et al. Mutation of Pten/Mmac1 in mice causes neoplasia in multiple organ systems. Proc. Natl. Acad. Sci. U.S.A. 96:1999;1563-1568.
62. Byun D.S., Cho K., Ryu B.K., Lee M.G., Park J.I., Chae K.S., Kim H.J., Chi S.G. Frequent monoallelic deletion of PTEN and its reciprocal association with PIK3CA amplification in gastric carcinoma. Int. J. Cancer. 104:2003;318-327.
63. Tamura M., Gu J., Matsumoto K., Aota S., Parsons R., Yamada K.M. Inhibition of cell migration spreading and focal adhesions by tumor suppressor PTEN. Science. 280:1998;1614-1617.
64. Freeman D.J., Li A.G., Wei G., Li H.H., Kertesz N., Lesche R.et al. PTEN tumor suppressor regulates p53 protein levels and activity through phosphatase-dependent and -independent mechanisms. Cancer Cell. 3:2003;117-130.
65. Caffrey J.J., Darden T., Wenk M.R., Shears S.B. Expanding coincident signaling by PTEN through its inositol 1,3,4,5,6-pentakisphosphate 3-phosphatase activity. FEBS Lett. 499:2001;6-10.
66. Lee J.O., Yang H., Georgescu M.M., Di Cristofano A., Maehama T., Shi Y. et al. Crystal structure of the PTEN tumor suppressor: implications for its phosphoinositide phosphatase activity and membrane association. Cell. 99:1999;323-334.
67. Das S., Dixon J.E., Cho W. Membrane-binding and activation mechanism of PTEN. Proc. Natl. Acad. Sci. U.S.A. 100:2003;7491-7496.
68. Campbell R.B., Liu F., Ross A.H. Allosteric activation of PTEN phosphatase by phosphatidylinositol 4,5-bisphosphate. J. Biol. Chem. 278:2003;33617-33620.
69. Vazquez F., Ramaswamy S., Nakamura N., Sellers W.R. Phosphorylation of the PTEN tail regulates protein stability and function. Mol. Cell Biol. 20:2000;5010-5018.
70. Miller S.J., Lou D.Y., Seldin D.C., Lane W.S., Neel B.G. Direct identification of PTEN phosphorylation sites. FEBS Lett. 528:2002;145-153.
71. Tolkacheva T., Boddapati M., Sanfiz A., Tsuchida K., Kimmelman A.C., Chan A.M. Regulation of PTEN binding to MAGI-2 by two putative phosphorylation sites at threonine 382 and 383. Cancer Res. 61:2001;4985-4989.
72. Lu Y., Yu Q., Liu J.H., Zhang J., Wang H., Koul D.et al. Src family protein-tyrosine kinases alter the function of PTEN to regulate phosphatidylinositol 3-kinase/AKT cascades. J. Biol. Chem. 278:2003;40057-40066.
73. Hu L., Zaloudek C., Mills G.B., Gray J., Jaffe R.B. In vivo and in vitro ovarian carcinoma growth inhibition by a phosphatidylinositol 3-kinase inhibitor (LY294002). Clin. Cancer Res. 6:2000;880-886.
74. Neshat M.S., Mellinghoff I.K., Tran C., Stiles B., Thomas G., Petersen R.et al. Enhanced sensitivity of PTEN-deficient tumors to inhibition of FRAP/mTOR. Proc. Natl. Acad. Sci. U.S.A. 98:2001;10314-10319.
75. Podsypanina K, Lee, RT, Politis C, Crane A, Puc J, Neshat M, et al. Inhibition of the mTOR/RAFT/FRAP pathway and the reduction of neoplasia in Pten+/- mice. 2001, submitted for publication.