Shank-interacting protein-like 1 promotes tumorigenesis via PTEN inhibition in human tumor cells

Journal of Clinical Investigation

Volumn 120, Issue 6, 2010, Pages 2094-2108

  He, Lizhi ^a,b   Ingram, Alistair ^a,b   Rybak, Adrian P ^a,b   Tang, Damu ^a,b  

^a MCMASTER UNIVERSITY   (Canada)

^b ST JOSEPH S HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; REGULATOR PROTEIN; SHANK INTERACTING PROTEIN LIKE 1; SMALL INTERFERING RNA; UBIQUITIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; CARCINOGENESIS; CONTROLLED STUDY; ENZYME ACTIVITY; EPIGENETICS; FEMALE; GLIOMA CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PRIMARY TUMOR; PRIORITY JOURNAL; PROSTATE CARCINOMA; PROTEIN DOMAIN; UTERINE CERVIX CANCER;

CELL LINE, TUMOR; CELLS; CELLULAR STRUCTURES; GENES; HELA CELLS; HUMANS; MALE; NEOPLASMS; PHOSPHATIDYLINOSITOL PHOSPHATES; PHOSPHATIDYLINOSITOLS; PHOSPHORIC MONOESTER HYDROLASES; PROSTATIC NEOPLASMS; PROTEINS; PTEN PHOSPHOHYDROLASE;

EID: 77953213657     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI40778     Document Type: Article

References (68)

1. Myers MP, et al. P-TEN, the tumor suppressor from human chromosome 10q23, is a dual-specificity phosphatase. Proc Natl Acad Sci U S A. 1997;94(17):9052-9057. (Pubitemid 27357780)
2. Myers MP, et al. The lipid phosphatase activity of PTEN is critical for its tumor supressor function. Proc Natl Acad Sci U S A. 1998;95(23):13513-13518.
3. Maehama T, Dixon JE. The tumor suppressor, PTEN/MMAC1, dephosphorylates the lipid second messenger, phosphatidylinositol 3,4,5-trisphosphate. J Biol Chem. 1998;273(22):13375-13378. (Pubitemid 28268370)
4. Cantley LC, Neel BG. New insights into tumor suppression: PTEN suppresses tumor formation by restraining the phosphoinositide 3-kinase/AKT pathway. Proc Natl Acad Sci U S A. 1999;96(8):4240-4245.
5. Yuan TL, Cantley LC. PI3K pathway alterations in cancer; variations on a theme. Oncogene. 2008;27(41):5497-5510.
6. Li J, et al. PTEN, a putative protein tyrosine phosphatase gene mutated in human brain, breast, and prostate cancer. Science. 1997;275(5308):1943-1947. (Pubitemid 27148818)
7. Steck PA, 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(4):356-362.
8. Li DM, Sun H. PTEN/MMAC1/TEP1 suppresses the tumorigenicity and induces G1 cell cycle arrest in human glioblastoma cells. Proc Natl Acad Sci U S A. 1998;95(26):15406-15411. (Pubitemid 29018711)
9. Bastola DR, Pahwa GS, Lin MF, Cheng PW. Down-regulation of PTEN/MMAC/TEP1 expression in human prostate cancer cell line DU145 by growth stimuli. Mol Cell Biochem. 2002;236(1-2):75-81. (Pubitemid 34846136)
10. Di Cristofano A, Pandolfi PP. The multiple roles of PTEN in tumor suppression. Cell. 2000;100(4):387-390.
11. Lee JO, et al. Crystal structure of the PTEN tumor suppressor: implications for its phosphoinositide phosphatase activity and membrane association. Cell. 1999;99(3):323-334.
12. Liaw D, et al. Germline mutations of the PTEN gene in Cowden disease, an inherited breast and thyroid cancer syndrome. Nat Genet. 1997;16(1):64-67. (Pubitemid 27198157)
13. Mallory SB. Cowden syndrome (multiple hamartoma syndrome). Dermatol Clin. 1995;13(1):27-31.
14. Goel A, et al. Frequent inactivation of PTEN by promoter hypermethylation in microsatellite instability-high sporadic colorectal cancers. Cancer Res. 2004;64(9):3014-3021. (Pubitemid 38581399)
15. Whang YE, 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. 1998;95(9):5246-5250.
16. Cheung TH, et al. Epigenetic and genetic alternation of PTEN in cervical neoplasm. Gynecol Oncol. 2004;93(3):621-627.
17. Su TH, et al. Mutation analysis of the putative tumor suppressor gene PTEN/MMAC1 in cervical cancer. Gynecol Oncol. 2000;76(2):193-199. (Pubitemid 30067194)
18. Yaginuma Y, et al. Abnormal structure and expression of PTEN/MMAC1 gene in human uterine cancers. Mol Carcinog. 2000;27(2):110-116. (Pubitemid 30090592)
19. 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. 2001;18(3):493-497.
20. Kurose K, Zhou XP, Araki T, Eng C. Biallelic inactivating mutations and an occult germline mutation of PTEN in primary cervical carcinomas. Genes Chromosomes Cancer. 2000;29(2):166-172.
21. El-Mansi MT, Williams AR. Evaluation of PTEN expression in cervical adenocarcinoma by tissue microarray. Int J Gynecol Cancer. 2006;16(3):1254-1260.
22. Lee JS, et al. Expression of PTEN in the progression of cervical neoplasia and its relation to tumor behavior and angiogenesis in invasive squamous cell carcinoma. J Surg Oncol. 2006;93(3):233-240.
23. Beaudenon S, Huibregtse JM. HPV E6, E6AP and cervical cancer. BMC Biochem. 2008;9(suppl 1):S4.
24. Yugawa T, Kiyono T. Molecular mechanisms of cervical carcinogenesis by high-risk human papillomaviruses: novel functions of E6 and E7 oncoproteins. Rev Med Virol. 2009;19(2):97-113.
25. Contreras-Paredes A, De la Cruz-Hernández E, Martínez- Ramírez I, Dueñas- González A, Lizano M. E6 variants of human papillomavirus 18 differentially modulate the protein kinase B/phosphatidylinositol 3-kinase (akt/PI3K) signaling pathway. Virology. 2009;383(1):78-85.
26. Qi M, Anderson AE, Chen DZ, Sun S, Auborn KJ. Indole-3-carbinol prevents PTEN loss in cervical cancer in vivo. Mol Med. 2005;11(1-12):59-63.
27. Bertelsen BI, Steine SJ, Sandvei R, Molven A, Laerum OD. Molecular analysis of the PI3K-AKT pathway in uterine cervical neoplasia: frequent PIK3CA amplification and AKT phosphorylation. Int J Cancer. 2006;118(8):1877-1883.
28. Cully M, You H, Levine AJ, Mak TW. Beyond PTEN mutations: the PI3K pathway as an integrator of multiple inputs during tumorigenesis. Nat Rev Cancer. 2006;6(3):184-192. (Pubitemid 43292562)
29. Robertson GP, et al. In vitro loss of heterozygosity targets the PTEN/MMAC1 gene in melanoma. Proc Natl Acad Sci USA. 1998;95(16):9418-9423.
30. Furnari FB, Huang HJ, Cavenee WK. The phosphoinositol phosphatase activity of PTEN mediates a serum-sensitive G1 growth arrest in glioma cells. Cancer Res. 1998;58(22):5002-5008.
31. Franke TF, Kaplan DR, Cantley LC. PI3K: downstream AKTion blocks apoptosis. Cell. 1997;88(4):435-437.
32. Lim S, et al. Sharpin, a novel postsynaptic density protein that directly interacts with the shank family of proteins. Mol Cell Neurosci. 2001;17(2):385-397. (Pubitemid 32176494)
33. Daigo Y, Takayama I, Ward SM, Sanders KM, Fujino MA. Novel human and mouse genes encoding a shank-interacting protein and its upregulation in gastric fundus of W/WV mouse. J Gastroenterol Hepatol. 2003;18(6):712-718. (Pubitemid 36791711)
34. Junttila MR, et al. CIP2A inhibits PP2A in human malignancies. Cell. 2007;130(1):51-62.
35. Torres J, Pulido R. The tumor suppressor PTEN is phosphorylated by the protein kinase CK2 at its C terminus. Implications for PTEN stability to proteasome-mediated degradation. J Biol Chem. 2001;276(2):993-998. (Pubitemid 32096519)
36. Silva A, et al. PTEN posttranslational inactivation and hyperactivation of the PI3K/Akt pathway sustain primary T cell leukemia viability. J Clin Invest. 2008;118(11):3762-3774
37. Wang X, et al. NEDD4-1 is a proto-oncogenic ubiquitin ligase for PTEN. Cell. 2007;128(1):129-139.
38. Kim RH, et al. DJ-1, a novel regulator of the tumor suppressor PTEN. Cancer Cell. 2005;7(3):263-273.
39. Seymour RE, et al. Spontaneous mutations in the mouse Sharpin gene result in multiorgan inflammation, immune system dysregulation and dermatitis. Genes Immun. 2007;8(5):416-421
40. Di Cristofano A, Pesce B, Cordon-Cardo C, Pandolfi PP. Pten is essential for embryonic development and tumour suppression. Nat Genet. 1998;19(4):348-355.
41. Suzuki A, et al. High cancer susceptibility and embryonic lethality associated with mutation of the PTEN tumor suppressor gene in mice. Curr Biol. 1998;8(21):1169-1178.
42. Stambolic V, et al. Negative regulation of PKB/Akt-dependent cell survival by the tumor suppressor PTEN. Cell. 1998;95(1):29-39. (Pubitemid 28458022)
43. Haas-Kogan D, Shalev N, Wong M, Mills G, Yount G, Stokoe D. Protein kinase B (PKB/Akt) activity is elevated in glioblastoma cells due to mutation of the tumor suppressor PTEN/MMAC. Curr Biol. 1998;8(21):1195-1198. (Pubitemid 28494720)
44. He L, et al. Co-existence of high levels of the PTEN protein with enhanced Akt activation in renal cell carcinoma. Biochim Biophys Acta. 2007;1772(10):1134-1142.
45. Naylor TL, et al. High resolution genomic analysis of sporadic breast cancer using array-based comparative genomic hybridization. Breast Cancer Res. 2005;7(6):R1186-R1198.
46. Choi YW, et al. Gene expression profiles in squamous cell cervical carcinoma using array-based comparative genomic hybridization analysis. Int J Gynecol Cancer. 2007;17(3):687-696. (Pubitemid 46743999)
47. Jeon YK, Cheon JE, Kim SK, Wang KC, Cho BK, Park SH. Clinicopathological features and global genomic copy number alterations of pilomyxoid astrocytoma in the hypothalamus/optic pathway: comparative analysis with pilocytic astrocytoma using array-based comparative genomic hybridization. Mod Pathol. 2008;21(11):1345-1356
48. van Duin M, et al. High-resolution array comparative genomic hybridization of chromosome 8q: evaluation of putative progression markers for gastroesophageal junction adenocarcinomas. Cytogenet Genome Res. 2007;118(2-4):130-137.
49. Kim JH, et al. Integrative analysis of genomic aberrations associated with prostate cancer progression. Cancer Res. 2007;67(17):8229-8239. (Pubitemid 47395160)
50. Kim SW, et al. Analysis of chromosomal changes in serous ovarian carcinoma using high- resolution array comparative genomic hybridization: Potential predictive markers of chemoresistant disease. Genes Chromosomes Cancer. 2007;46(1):1-9.
51. Hermsen M, et al. Chromosomal changes in relation to clinical outcome in larynx and pharynx squamous cell carcinoma. Cell Oncol. 2005;27(3):191-198. (Pubitemid 41032904)
52. Okamoto H, Yasui K, Zhao C, Arii S, Inazawa J. PTK2 and EIF3S3 genes may be amplification targets at 8q23-q24 and are associated with large hepatocellular carcinomas. Hepatology. 2003;38(5):1242-1249. (Pubitemid 37314833)
53. Chochi Y, et al. A copy number gain of the 6p arm is linked with advanced hepatocellular carcinoma: an array-based comparative genomic hybridization study. J Pathol. 2009;217(5):677-684.
54. Douglas EJ, et al. Array comparative genomic hybridization analysis of colorectal cancer cell lines and primary carcinomas. Cancer Res. 2004;64(14):4817-4825. (Pubitemid 38924525)
55. Buffart TE, et al. DNA copy number changes at 8q11-24 in metastasized colorectal cancer. Cell Oncol. 2005;27(1):57-65.
56. Suzuki A, Nakano T, Mak TW, Sasaki T. Portrait of PTEN: messages from mutant mice. Cancer Sci. 2008;99(2):209-213. (Pubitemid 351232668)
57. Davies MA, et al. Regulation of Akt/PKB activity, cellular growth, and apoptosis in prostate carcinoma cells by MMAC/PTEN. Cancer Res. 1999;59(11):2551-2556.
58. Tang D, et al. Akt is activated in response to an apoptotic signal. J Biol Chem. 2001;276(32):30461-30466. (Pubitemid 37385133)
59. Tang X, Powelka AM, Soriano NA, Czech MP, Guilherme A. PTEN, but not SHIP2, suppresses insulin signaling through the phosphatidylinositol 3- kinase/Akt pathway in 3T3-L1 adipocytes. J Biol Chem. 2005;280(23):22523-22529. (Pubitemid 40827910)
60. Tang D, Chun AC, Zhang M, Wang JH. Cyclin-dependent kinase 5 (Cdk5) activation domain of neuronal Cdk5 activator. Evidence of the existence of cyclin fold in neuronal Cdk5a activator. J Biol Chem. 1997;272(19):12318-12327. (Pubitemid 27203317)
61. Tang D, Gururajan R, Kidd VJ. Phosphorylation of PITSLRE p110 isoforms accompanies their processing by caspases during Fas-mediated cell death. J Biol Chem. 1998;273(26):16601-16607. (Pubitemid 28311449)
62. Ochiya T, et al. New delivery system for plasmid DNA in vivo using atelocollagen as a carrier material: the Minipellet. Nat Med. 1999;5(6):707-710. (Pubitemid 29289437)
63. Yu D, Sekine E, Fujimori A, Ochiya T, Okayasu R. Down regulation of BRCA2 causes radio-sensitization of human tumor cells in vitro and in vivo. Cancer Sci. 2008;99(4):810-815. (Pubitemid 351453830)
64. Iwaki K, et al. A small interfering RNA targeting proteinase-activated receptor-2 is effective in suppression of tumor growth in a Panc1 xenograft model. Int J Cancer. 2008;122(3):658-663. (Pubitemid 350308962)
65. Georgescu MM, Kirsch KH, Akagi T, Shishido T, Hanafusa H. The tumor-suppressor activity of PTEN is regulated by its carboxyl-terminal region. Proc Natl Acad Sci U S A. 1999;96(18):10182-10187. (Pubitemid 29422533)
66. Randall LM, et al. Markers of angiogenesis in high-risk, early-stage cervical cancer: A Gynecologic Oncology Group study. Gynecol Oncol. 2009;112(3):583-589.
67. Mehta R, et al. Independent association of angiogenesis index with outcome in prostate cancer. Clin Cancer Res. 2001;7(1):81-88. (Pubitemid 32110208)
68. Maw MK, Fujimoto J, Tamaya T. Expression of the inhibitor of DNA- binding (ID)-1 protein as an angiogenic mediator in tumour advancement of uterine cervical cancers. Br J Cancer. 2008;99(10):1557-1563.