p66Shc longevity protein regulates the proliferation of human ovarian cancer cells

Molecular Carcinogenesis

Volumn 54, Issue 8, 2015, Pages 618-631

  Muniyan, Sakthivel ^a   Chou, Yu Wei ^a   Tsai, Te Jung ^a   Thomes, Paul ^a   Veeramani, Suresh ^a   Benigno, Benedict B ^b   Walker, L Deette ^c   Mcdonald, John F ^c   Khan, Shafiq A ^d   Lin, Fen Fen ^a   Lele, Subodh M ^a   Lin, Ming Fong ^a,e,f  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b Ovarian Cancer Institute   (United States)

^c GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^d CLARK ATLANTA UNIVERSITY   (United States)

^e UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^f KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

Author keywords

ErbB 2 signaling; Estrogen; P66Shc; ROS; Tyrosine phosphatase

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; ACID PHOSPHATASE; BETA ACTIN; CYCLIN D1; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ESTROGEN; MITOGEN ACTIVATED PROTEIN KINASE; P66SHC PROTEIN; PROTEIN SHC; UNCLASSIFIED DRUG; 2-(2-AMINO-3-METHOXYPHENYL)-4H-1-BENZOPYRAN-4-ONE; ERBB2 PROTEIN, HUMAN; FLAVONOID; PROTEIN KINASE INHIBITOR; SHC1 PROTEIN, HUMAN;

ARTICLE; CARCINOGENESIS; CELL COUNT; CELL GROWTH; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; FEMALE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MALE; OVARIAN CANCER CELL LINE; OVARY CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; DRUG EFFECTS; GENETICS; METABOLISM; OVARY TUMOR; PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE; UPREGULATION;

MURINAE; OXALIS TUBEROSA;

CELL LINE, TUMOR; CELL PROLIFERATION; ESTROGENS; FEMALE; FLAVONOIDS; HUMANS; OVARIAN NEOPLASMS; PROTEIN KINASE INHIBITORS; RECEPTOR, ERBB-2; SHC SIGNALING ADAPTOR PROTEINS; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 84937024079     PISSN: 08991987     EISSN: 10982744     Source Type: Journal    
DOI: 10.1002/mc.22129     Document Type: Article

References (50)

1. Siegel R, Naishadham D, Jemal A. Cancer statistics. CA Cancer J Clin 2012; 62:10-29.
2. Cho KR, Shih IeM. Ovarian cancer. Annu Rev Pathol 2009; 4:287-313.
3. Bast RC Jr, Hennessy B, Mills GB. The biology of ovarian cancer: New opportunities for translation. Nat Rev Cancer 2009; 9:415-428.
4. Barakat RR, Bundy BN, Spirtos NM, Bell J, Mannel RS. Randomized double-blind trial of estrogen replacement therapy versus placebo in stage I or II endometrial cancer: A Gynecologic Oncology Group Study. J Clin Oncol 2006; 24:587-592.
5. Rubin SC, Randall TC, Armstrong KA, Chi DS, Hoskins WJ. Ten-year followup of ovarian cancer patients after second-look laparotomy with negative findings. Obstet Gynecol 1999; 93:21-24.
6. Pelicci G, Lanfrancone L, Grignani J, et al. A novel transforming protein (SHC) with an SH2 domain is implicated in mitogenic signal transduction. Cell 1992; 70:93-104.
7. Ray PD, Huang BW, Tsuji Y. Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell Signal 2012; 24:981-990.
8. Ravichandran KS. Signaling via Shc family adapter proteins. Oncogene 2001; 20:6322-6330.
9. Gotoh N, Toyoda M, Shibuya M. Tyrosine phosphorylation sites at amino acids 239 and 240 of Shc are involved in epidermal growth factor-induced mitogenic signaling that is distinct from Ras/mitogen-activated protein kinase activation. Mol Cell Biol 1997; 17:1824-1831.
10. Veeramani S, Igawa T, Yuan TC, et al. Expression of p66(Shc) protein correlates with proliferation of human prostate cancer cells. Oncogene 2005; 24:7203-7212.
11. Gotoh N, Tojo A, Shibuya M. A novel pathway from phosphorylation of tyrosine residues 239/240 of Shc, contributing to suppress apoptosis by IL-3. EMBO J 1996; 15:6197-6204.
12. Pellegrini M, Pacini S, Baldari CT. p66SHC: The apoptotic side of Shc proteins. Apoptosis 2005; 10:13-18.
13. Rajendran M, Thomes P, Zhang L, Veeramani S, Lin MF. p66Shc-a longevity redox protein in human prostate cancer progression and metastasis: p66Shc in cancer progression and metastasis. Cancer Metastasis Rev 2010; 29:207-222.
14. Alam SM, Rajendran M, Ouyang S, et al. A novel role of Shc adaptor proteins in steroid hormone regulated cancers. Endocr Relat Cancer 2009; 16:1-16.
15. Migliaccio E, Giorgio M, Mele S, et al. The p66shc adaptor protein controls oxidative stress response and life span in mammals. Nature 1999; 402:309-313.
16. Giorgio M, Migliaccio E, Orsini F, et al. Electron transfer between cytochrome c and p66Shc generates reactive oxygen species that trigger mitochondrial apoptosis. Cell 2005; 122:221-233.
17. Veeramani S, Yuan TC, Lin FF, Lin MF. Mitochondrial redox signaling by p66Shc is involved in regulating androgenic growth stimulation of human prostate cancer cells. Oncogene 2008; 27:5057-5068.
18. Khanday FA, Santhanam L, Kasuno K, et al. Sos-mediated activation of rac1 by p66shc. J Cell Biol 2006; 172:817-822.
19. Stevenson LE, Ravichandran KS. Frackelton AR Jr. Shc dominant negative disrupts cell cycle progression in both G0-G1 and G2-M of ErbB2-positive breast cancer cells. Cell Growth Differ 1999; 10:61-71.
20. Lee MS, Igawa T, Chen SJ, et al. p66Shc protein is upregulated by steroid hormones in hormone-sensitive cancer cells and in primary prostate carcinomas. Int J Cancer 2004; 108:672-678.
21. Jackson JG, Yoneda T, Clark GM, Yee D. Elevated levels of p66 Shc are found in breast cancer cell lines and primary tumors with high metastatic potential. Clin Cancer Res 2000; 6:1135-1139.
22. Davol PA, Bagdasaryan R, Elfenbein GJ, Maizel AL, Frackelton AR Jr. Shc proteins are strong, independent prognostic markers for both node-negative and node-positive primary breast cancer. Cancer Res 2003; 63:6772-6783.
23. Grossman SR, Lyle S, Resnick MB. p66 Shc tumor levels show a strong prognostic correlation with disease outcome in stage IIA colon cancer. Clin Cancer Res 2007; 13:5798-5804.
24. Park YJ, Kim TY, Lee SH, et al. p66Shc expression in proliferating thyroid cells is regulated by thyrotropin receptor signaling. Endocrinology 2005; 146:2473-2480.
25. Xie Y, Hung MC. p66Shc isoform down-regulated and not required for HER-2/neu signaling pathway in human breast cancer cell lines with HER-2/neu overexpression. Biochem Biophys Res Commun 1996; 221:140-145.
26. Lacey JV Jr, Mink PJ, Lubin JH, et al. Menopausal hormone replacement therapy and risk of ovarian cancer. JAMA 2002; 288:334-341.
27. Cunat S, Hoffmann P, Pujol P. Estrogens and epithelial ovarian cancer. Gynecol Oncol 2004; 94:25-32.
28. Meng TC, Lin MF. Tyrosine phosphorylation of c-ErbB-2 is regulated by the cellular form of prostatic acid phosphatase in human prostate cancer cells. J Biol Chem 1998; 273:22096-22104.
29. Lin MF, Meng TC, Rao PS, et al. Expression of human prostatic acid phosphatase correlates with androgen-stimulated cell proliferation in prostate cancer cell lines. J Biol Chem 1998; 273:5939-5947.
30. Veeramani S, Chou YW, Lin FC, et al. Reactive oxygen species induced by p66Shc longevity protein mediate non-genomic androgen action via tyrosine phosphorylation signaling to enhance tumorigenicity of prostate cancer cells. Free Radic Biol Med 2012; 53:95-108.
31. Chen SJ, Karan D, Johansson SL, et al. Prostate-derived factor as a paracrine and autocrine factor for the proliferation of androgen receptor-positive human prostate cancer cells. Prostate 2007; 67:557-571.
32. Lin MF, Lee MS, Zhou XW, et al. Decreased expression of cellular prostatic acid phosphatase increases tumorigenicity of human prostate cancer cells. J Urol 2001; 166:1943-1950.
33. Meng TC, Fukada T, Tonks NK. Reversible oxidation and inactivation of protein tyrosine phosphatases in vivo. Mol Cell 2002; 9:387-399.
34. Meng TC, Buckley DA, Galic S, Tiganis T, Tonks NK. Regulation of insulin signaling through reversible oxidation of the protein-tyrosine phosphatases TC45 and PTP1B. J Biol Chem 2004; 279:37716-37725.
35. Meng TC, Lee MS, Lin MF. Interaction between protein tyrosine phosphatase and protein tyrosine kinase is involved in androgen-promoted growth of human prostate cancer cells. Oncogene 2000; 19:2664-2677.
36. Sauer H, Wartenberg M, Hescheler J. Reactive oxygen species as induring cell growth and differentiation. Cell Physiol Biochem 2001; 11:173-186.
37. Murrell GA, Francis MJ, Bromley L. Modulation of fibroblast proliferation by oxygen free radicals. Biochem J 1990; 265:659-665.
38. Nicotera TM, Privalle C, Wang TC, Oshimura M, Barrett JC. Differential proliferative responses of syrian hamster embryo fibroblasts to paraquat-generated superoxide radicals depending on tumor suppressor gene function. Cancer Res 1994; 54:3884-3888.
39. Langdon SP, Hawkes MM, Lawrie SS. Oestrogen receptor expression and the effects of oestrogen and tamoxifen on the growth of human ovarian carcinoma cell lines. Br J Cancer 1990; 62:213-216.
40. Bai W, Oliveros-Saunders B, Wang Q, Acevedo-Duncan ME, Nicosia SV. Estrogen stimulation of ovarian surface epithelial cell proliferation. In Vitro Cell Dev Biol Anim 2000; 36:657-666.
41. Lindgren P, Backstrom T, Mahlck CG, Ridderheim M, Cajander S. Steroid receptors and hormones in relation to cell proliferation and apoptosis in poorly differentiated epithelial ovarian tumors. Int J Oncol 2001; 19:31-38.
42. Wang Y, Yang J, Gao Y, et al. Regulatory effect of E2, IL-6 and IL-8 on the growth of epithelial ovarian cancer cells. Cell Mol Immunol 2005; 2:365-372.
43. Hu Y, Rosen DG, Zhou Y, et al. Mitochondrial manganese-superoxide dismutase expression in ovarian cancer: Role in cell proliferation and response to oxidative stress. J Biol Chem 2005; 280:39485-39492.
44. Foulkes JG. Phosphotyrosyl-protein phosphatase. Curr Top Microbiol Immunol 1983; 107:163-180.
45. Li HC, Chernoff J, Chen LB, Kirschonbaum A. A phosphotyrosyl-protein phosphatase activity associated with acid phosphatase from human prostate gland. Eur J Biochem 1984; 138:45-51.
46. Lin MF, Clinton GM. Prostatic acid phosphatase has phosphotryosyl protein phosphatase activity. Biochem J 1986; 235:351-357.
47. Veeramani S, Lee MS, Lin MF. Revisiting histidine-dependent acid phosphatases: A distinct group of tyrosine phosphatases. Trends Biochem Sci 2009; 34:273-278.
48. Chuang TD, Chen SJ, Lin FF, et al. Human prostatic acid phosphatase, an authentic tyrosine phosphatase, dephosphorylates ErbB-2 and regulates prostate cancer cell growth. J Biol Chem 2010; 285:23598-23606.
49. Lin MF, DaVolio J, Garcia-Arenas R. Expression of human prostatic acid phosphatase activity and growth of prostate carcinoma cells. Cancer Res 1992; 52:4600-4607.
50. Honig A, Rieger L, Kapp M, et al. Increased tartrate-resistant acid phosphatase (TRAP) expression in malignant breast, ovarian and melanoma tissue: An investigational study. BMC Cancer 2006; 6:199.