p66Shc as a switch in bringing about contrasting responses in cell growth: Implications on cell proliferation and apoptosis

Molecular Cancer

Volumn 14, Issue 1, 2015, Pages

  Bhat, Sahar S ^a   Anand, Deepak ^b   Khanday, Firdous A ^b  

^a UNIVERSITY OF KASHMIR   (India)

^b KING FAHD UNIVERSITY OF PETROLEUM AND MINERALS   (Saudi Arabia)

Author keywords

Apoptosis; Cancer; Cell proliferation; p53; p66Shc; ROS

Indexed keywords

ADAPTOR PROTEIN; PROTEIN P66SHC; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; SHC SIGNALING ADAPTOR PROTEIN;

ANOIKIS; APOPTOSIS; ARTICLE; BREAST CANCER; CARCINOGENESIS; CELL AGING; CELL GROWTH; CELL PROLIFERATION; ESOPHAGUS CANCER; HUMAN; INTRACELLULAR SIGNALING; LONGEVITY; LUNG CANCER; OVARY CANCER; OXIDATIVE STRESS; PROSTATE CANCER; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; THYROID CANCER; METABOLISM; NEOPLASM; PATHOLOGY; SIGNAL TRANSDUCTION;

APOPTOSIS; CELL PROLIFERATION; HUMANS; NEOPLASMS; REACTIVE OXYGEN SPECIES; SHC SIGNALING ADAPTOR PROTEINS; SIGNAL TRANSDUCTION;

EID: 84928790568     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/s12943-015-0354-9     Document Type: Article

References (114)

1. Rozakis-Adcock M, McGlade J, Mbamalu G, Pelicci G, Daly R, Li W, et al. Association of the Shc and Grb2/Sem5 SH2-containing proteins is implicated in activation of the Ras pathway by tyrosine kinases. Nature. 1992;360:689-92.
2. Nakamura T, Muraoka S, Sanokawa R, Mori N. N-Shc and Sck, two neuronally expressed Shc adapter homologs. Their differential regional expression in the brain and roles in neurotrophin and Src signaling. J Biol Chem. 1998;273:6960-7.
3. Bonfini L, Migliaccio E, Pelicci G, Lanfrancone L, Pelicci PG. Not all Shc's roads lead to Ras. Trends Biochem Sci. 1996;21:257-61.
4. Ravichandran KS. Signaling via Shc family adapter proteins. Oncogene. 2001;20:6322-30.
5. Pelicci G, Lanfrancone L, Grignani F, McGlade J, Cavallo F, Forni G, et al. A novel transforming protein (SHC) with an SH2 domain is implicated in mitogenic signal transduction. Cell. 1992;70:93-104.
6. Migliaccio E, Giorgio M, Mele S, Pelicci G, Reboldi P, Pandolfi PP, et al. The p66shc adaptor protein controls oxidative stress response and life span in mammals. Nature. 1999;402:309-13.
7. Ventura A, Luzi L, Pacini S, Baldari CT, Pelicci PG. The p66Shc longevity gene is silenced through epigenetic modifications of an alternative promoter. J Biol Chem. 2002;277:22370-6.
8. Luzi L, Confalonieri S, Di Fiore PP, Pelicci PG. Evolution of Shc functions from nematode to human. Curr Opin Genet Dev. 2000;10:668-74.
9. Rozakis-Adcock M, Fernley R, Wade J, Pawson T, Bowtell D. The SH2 and SH3 domains of mammalian Grb2 couple the EGF receptor to the Ras activator mSos1. Nature. 1993;363:83-5.
10. Pelicci G, Dente L, De Giuseppe A, Verducci-Galletti B, Giuli S, Mele S, et al. A family of Shc related proteins with conserved PTB, CH1 and SH2 regions. Oncogene. 1996;13:633-41.
11. Migliaccio E, Mele S, Salcini AE, Pelicci G, Lai KM, Superti-Furga G, et al. Opposite effects of the p52shc/p46shc and p66shc splicing isoforms on the EGF receptor-MAP kinase-fos signalling pathway. EMBO J. 1997;16:706-16.
12. Pacini S, Pellegrini M, Migliaccio E, Patrussi L, Ulivieri C, Ventura A, et al. p66SHC promotes apoptosis and antagonizes mitogenic signaling in T cells. Mol Cell Biol. 2004;24:1747-57.
13. Okada S, Kao AW, Ceresa BP, Blaikie P, Margolis B, Pessin JE. The 66-kDa Shc isoform is a negative regulator of the epidermal growth factor-stimulated mitogen-activated protein kinase pathway. J Biol Chem. 1997;272:28042-9.
14. Nemoto S, Combs CA, French S, Ahn BH, Fergusson MM, Balaban RS, et al. The mammalian longevity-associated gene product p66shc regulates mitochondrial metabolism. J Biol Chem. 2006;281:10555-60.
15. Innocenti M, Tenca P, Frittoli E, Faretta M, Tocchetti A, Di Fiore PP, et al. Mechanisms through which Sos-1 coordinates the activation of Ras and Rac. J Cell Biol. 2002;156:125-36.
16. Khanday FA, Yamamori T, Mattagajasingh I, Zhang Z, Bugayenko A, Naqvi A, et al. Rac1 leads to phosphorylation-dependent increase in stability of the p66shc adaptor protein: role in Rac1-induced oxidative stress. Mol Biol Cell. 2006;17:122-9.
17. Arany I, Faisal A, Nagamine Y, Safirstein RL. p66shc inhibits pro-survival epidermal growth factor receptor/ERK signaling during severe oxidative stress in mouse renal proximal tubule cells. J Biol Chem. 2008;283:6110-7.
18. Lithgow GJ, Kirkwood TB. Mechanisms and evolution of aging. Science. 1996;273:80.
19. Orr WC, Sohal RS. Extension of life-span by overexpression of superoxide dismutase and catalase in Drosophila melanogaster. Science. 1994;263:1128-30.
20. Stracke ML, Engel JD, Wilson LW, Rechler MM, Liotta LA, Schiffmann E. The type I insulin-like growth factor receptor is a motility receptor in human melanoma cells. J Biol Chem. 1989;264:21544-9.
21. Berniakovich I, Trinei M, Stendardo M, Migliaccio E, Minucci S, Bernardi P, et al. p66Shc-generated oxidative signal promotes fat accumulation. J Biol Chem. 2008;283:34283-93.
22. Soliman MA, Abdel Rahman AM, Lamming DW, Birsoy K, Pawling J, Frigolet ME, et al. The adaptor protein p66Shc inhibits mTOR-dependent anabolic metabolism. Sci Signal. 2014;7:ra17.
23. Kumar S, Vikram A, Kim YR, SJ J, Irani K. P66Shc mediates increased platelet activation and aggregation in hypercholesterolemia. Biochem Biophys Res Commun. 2014;449:496-501.
24. Cesselli D, Jakoniuk I, Barlucchi L, Beltrami AP, Hintze TH, Nadal-Ginard B, et al. Oxidative stress-mediated cardiac cell death is a major determinant of ventricular dysfunction and failure in dog dilated cardiomyopathy. Circ Res. 2001;89:279-86.
25. De Marchi E, Baldassari F, Bononi A, Wieckowski MR, Pinton P. Oxidative stress in cardiovascular diseases and obesity: role of p66Shc and protein kinase C. Oxid Med Cell Longev. 2013;2013:564961.
26. Savino C, Pelicci P, Giorgio M. The P66Shc/mitochondrial permeability transition pore pathway determines neurodegeneration. Oxid Med Cell Longev. 2013;2013:719407.
27. Bashir M, Parray AA, Baba RA, Bhat HF, Bhat SS, Mushtaq U, et al. beta-Amyloid-evoked apoptotic cell death is mediated through MKK6-p66shc pathway. Neuromolecular Med. 2014;16:137-49.
28. Canevari L, Abramov AY, Duchen MR. Toxicity of amyloid beta peptide: tales of calcium, mitochondria, and oxidative stress. Neurochem Res. 2004;29:637-50.
29. Giorgio M, Migliaccio E, Orsini F, Paolucci D, Moroni M, Contursi C, et al. Electron transfer between cytochrome c and p66Shc generates reactive oxygen species that trigger mitochondrial apoptosis. Cell. 2005;122:221-33.
30. Pellegrini M, Pacini S, Baldari CT. p66SHC: the apoptotic side of Shc proteins. Apoptosis. 2005;10:13-8.
31. 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;6:1135-9.
32. Stevenson LE, Frackelton Jr AR. Constitutively tyrosine phosphorylated p52 Shc in breast cancer cells: correlation with ErbB2 and p66 Shc expression. Breast Cancer Res Treat. 1998;49:119-28.
33. Veeramani S, Igawa T, Yuan TC, Lin FF, Lee MS, Lin JS, et al. Expression of p66(Shc) protein correlates with proliferation of human prostate cancer cells. Oncogene. 2005;24:7203-12.
34. 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;221:140-5.
35. Miyazawa M, Tsuji Y. Evidence for a novel antioxidant function and isoform-specific regulation of the human p66Shc gene. Mol Biol Cell. 2014;25:2116-27.
36. Galimov ER, Chernyak BV, Sidorenko AS, Tereshkova AV, Chumakov PM. Prooxidant properties of p66shc are mediated by mitochondria in human cells. PLoS One. 2014;9:e86521.
37. Foschi M, Franchi F, Han J, La Villa G, Sorokin A. Endothelin-1 induces serine phosphorylation of the adaptor protein p66Shc and its association with 14-3-3 protein in glomerular mesangial cells. J Biol Chem. 2001;276:26640-7.
38. Faisal A, el-Shemerly M, Hess D, Nagamine Y. Serine/threonine phosphorylation of ShcA. Regulation of protein-tyrosine phosphatase-pest binding and involvement in insulin signaling. J Biol Chem. 2002;277:30144-52.
39. Park YJ, Kim TY, Lee SH, Kim H, Kim SW, Shong M, et al. p66Shc expression in proliferating thyroid cells is regulated by thyrotropin receptor signaling. Endocrinology. 2005;146:2473-80.
40. Le S, Connors TJ, Maroney AC. c-Jun N-terminal kinase specifically phosphorylates p66ShcA at serine 36 in response to ultraviolet irradiation. J Biol Chem. 2001;276:48332-6.
41. Yang CP, Horwitz SB. Distinct mechanisms of taxol-induced serine phosphorylation of the 66-kDa Shc isoform in A549 and RAW 264.7 cells. Biochim Biophys Acta. 2002;1590:76-83.
42. Olson MF, Ashworth A, Hall A. An essential role for Rho, Rac, and Cdc42 GTPases in cell cycle progression through G1. Science. 1995;269:1270-2.
43. 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;19:2664-77.
44. Stevenson MA, Pollock SS, Coleman CN, Calderwood SK. X-irradiation, phorbol esters, and H2O2 stimulate mitogen-activated protein kinase activity in NIH-3T3 cells through the formation of reactive oxygen intermediates. Cancer Res. 1994;54:12-5.
45. Orsini F, Migliaccio E, Moroni M, Contursi C, Raker VA, Piccini D, et al. The life span determinant p66Shc localizes to mitochondria where it associates with mitochondrial heat shock protein 70 and regulates trans-membrane potential. J Biol Chem. 2004;279:25689-95.
46. Trinei M, Giorgio M, Cicalese A, Barozzi S, Ventura A, Migliaccio E, et al. A p53-p66Shc signalling pathway controls intracellular redox status, levels of oxidation-damaged DNA and oxidative stress-induced apoptosis. Oncogene. 2002;21:3872-8.
47. Khanday FA, Santhanam L, Kasuno K, Yamamori T, Naqvi A, Dericco J, et al. Sos-mediated activation of rac1 by p66shc. J Cell Biol. 2006;172:817-22.
48. Xie ZZ, Shi MM, Xie L, Wu ZY, Li G, Hua F, et al. Sulfhydration of p66Shc at Cysteine59 Mediates the Antioxidant Effect of Hydrogen Sulfide. Antioxid Redox Signal. 2014;18:2531-42.
49. Vikram A, Kim YR, Kumar S, Naqvi A, Hoffman TA, Kumar A, et al. Canonical Wnt signaling induces vascular endothelial dysfunction via p66Shc-regulated reactive oxygen species. Arterioscler Thromb Vasc Biol. 2014;34:2301-9.
50. Alam SM, Rajendran M, Ouyang S, Veeramani S, Zhang L, Lin MF. A novel role of Shc adaptor proteins in steroid hormone-regulated cancers. Endocr Relat Cancer. 2009;16:1-16.
51. Pages G, Lenormand P, L'Allemain G, Chambard JC, Meloche S, Pouyssegur J. Mitogen-activated protein kinases p42mapk and p44mapk are required for fibroblast proliferation. Proc Natl Acad Sci U S A. 1993;90:8319-23.
52. Nemoto S, Finkel T. Redox regulation of forkhead proteins through a p66shc-dependent signaling pathway. Science. 2002;295:2450-2.
53. Ames BN, Shigenaga MK, Hagen TM. Oxidants, antioxidants, and the degenerative diseases of aging. Proc Natl Acad Sci U S A. 1993;90:7915-22.
54. Favetta LA, Robert C, King WA, Betts DH. Expression profiles of p53 and p66shc during oxidative stress-induced senescence in fetal bovine fibroblasts. Exp Cell Res. 2004;299:36-48.
55. Jiang X, Edstrom E, Altun M, Ulfhake B. Differential regulation of Shc adaptor proteins in skeletal muscle, spinal cord and forebrain of aged rats with sensorimotor impairment. Aging Cell. 2003;2:47-57.
56. Klein LE, Freeze BS, Smith 3rd AB, Horwitz SB. The microtubule stabilizing agent discodermolide is a potent inducer of accelerated cell senescence. Cell Cycle. 2005;4:501-7.
57. Turrens JF. Mitochondrial formation of reactive oxygen species. J Physiol. 2003;552:335-44.
58. Migliaccio E, Giorgio M, Pelicci PG. Apoptosis and aging: role of p66Shc redox protein. Antioxid Redox Signal. 2006;8:600-8.
59. Helbock HJ, Beckman KB, Ames BN. 8-Hydroxydeoxyguanosine and 8-hydroxyguanine as biomarkers of oxidative DNA damage. Methods Enzymol. 1999;300:156-66.
60. Northey JJ, Chmielecki J, Ngan E, Russo C, Annis MG, Muller WJ, et al. Signaling through ShcA is required for transforming growth factor beta- and Neu/ErbB-2-induced breast cancer cell motility and invasion. Mol Cell Biol. 2008;28:3162-76.
61. Ratner S, Patrick P, Bora G. Lymphocyte development of adherence and motility in extracellular matrix during IL-2 stimulation. J Immunol. 1992;149:681-8.
62. Giorgio M, Berry A, Berniakovich I, Poletaeva I, Trinei M, Stendardo M, et al. The p66Shc knocked out mice are short lived under natural condition. Aging Cell. 2012;11:162-8.
63. Frisch SM, Francis H. Disruption of epithelial cell-matrix interactions induces apoptosis. J Cell Biol. 1994;124:619-26.
64. Paoli P, Giannoni E, Chiarugi P. Anoikis molecular pathways and its role in cancer progression. Biochim Biophys Acta. 1833;2013:3481-98.
65. Ma Z, Myers DP, Wu RF, Nwariaku FE, Terada LS. p66Shc mediates anoikis through RhoA. J Cell Biol. 2007;179:23-31.
66. Ma Z, Liu Z, Wu RF, Terada LS. p66(Shc) restrains Ras hyperactivation and suppresses metastatic behavior. Oncogene. 2010;29:5559-67.
67. Pinton P, Rizzuto R. p66Shc, oxidative stress and aging: importing a lifespan determinant into mitochondria. Cell Cycle. 2008;7:304-8.
68. Anand-Apte B, Zetter BR, Viswanathan A, Qiu RG, Chen J, Ruggieri R, et al. Platelet-derived growth factor and fibronectin-stimulated migration are differentially regulated by the Rac and extracellular signal-regulated kinase pathways. J Biol Chem. 1997;272:30688-92.
69. Klemke RL, Cai S, Giannini AL, Gallagher PJ, de Lanerolle P, Cheresh DA. Regulation of cell motility by mitogen-activated protein kinase. J Cell Biol. 1997;137:481-92.
70. Sastre J, Pallardo FV, Vina J. The role of mitochondrial oxidative stress in aging. Free Radic Biol Med. 2003;35:1-8.
71. Lauffenburger DA, Horwitz AF. Cell migration: a physically integrated molecular process. Cell. 1996;84:359-69.
72. Klemke RL, Yebra M, Bayna EM, Cheresh DA. Receptor tyrosine kinase signaling required for integrin alpha v beta 5-directed cell motility but not adhesion on vitronectin. J Cell Biol. 1994;127:859-66.
73. Huttenlocher A, Sandborg RR, Horwitz AF. Adhesion in cell migration. Curr Opin Cell Biol. 1995;7:697-706.
74. Guo M, Hay BA. Cell proliferation and apoptosis. Curr Opin Cell Biol. 1999;11:745-52.
75. Bashir M, Kirmani D, Bhat HF, Baba RA, Hamza R, Naqash S, et al. P66shc and its downstream Eps8 and Rac1 proteins are upregulated in esophageal cancers. Cell Commun Signal. 2010;8:13.
76. Evan GI, Vousden KH. Proliferation, cell cycle and apoptosis in cancer. Nature. 2001;411:342-8.
77. Ginaldi L, De Martinis M, D'Ostilio A, Marini L, Loreto MF, Corsi MP, et al. Cell proliferation and apoptosis in the immune system in the elderly. Immunol Res. 2000;21:31-8.
78. Mignatti P, Morimoto T, Rifkin DB. Basic fibroblast growth factor released by single, isolated cells stimulates their migration in an autocrine manner. Proc Natl Acad Sci U S A. 1991;88:11007-11.
79. Lee MS, Igawa T, Chen SJ, Van Bemmel D, Lin JS, Lin FF, et al. p66Shc protein is upregulated by steroid hormones in hormone-sensitive cancer cells and in primary prostate carcinomas. Int J Cancer. 2004;108:672-8.
80. Sachs M, Weidner KM, Brinkmann V, Walther I, Obermeier A, Ullrich A, et al. Motogenic and morphogenic activity of epithelial receptor tyrosine kinases. J Cell Biol. 1996;133:1095-107.
81. Chobanyan NS. Re: Henderson,B.E. and Feigelson,H.S. (2000) hormonal carcinogenesis. Carcinogenesis, 21, 427-433. Carcinogenesis. 2001;22:529.
82. Dabrosin C, Ollinger K, Ungerstedt U, Hammar M. Variability of glutathione levels in normal breast tissue and subcutaneous fat during the menstrual cycle: an in vivo study with microdialysis technique. J Clin Endocrinol Metab. 1997;82:1382-4.
83. Devanesan P, Santen RJ, Bocchinfuso WP, Korach KS, Rogan EG, Cavalieri E. Catechol estrogen metabolites and conjugates in mammary tumors and hyperplastic tissue from estrogen receptor-alpha knock-out (ERKO)/Wnt-1 mice: implications for initiation of mammary tumors. Carcinogenesis. 2001;22:1573-6.
84. Dickson RB, Lippman ME. Estrogenic regulation of growth and polypeptide growth factor secretion in human breast carcinoma. Endocr Rev. 1987;8:29-43.
85. Witsch E, Sela M, Yarden Y. Roles for growth factors in cancer progression. Physiology (Bethesda). 2010;25:85-101.
86. Grossmann ME, Huang H, Tindall DJ. Androgen receptor signaling in androgen-refractory prostate cancer. J Natl Cancer Inst. 2001;93:1687-97.
87. Weigel NL, Moore NL. Kinases and protein phosphorylation as regulators of steroid hormone action. Nucl Recept Signal. 2007;5:e005.
88. Guo Z, Dai B, Jiang T, Xu K, Xie Y, Kim O, et al. Regulation of androgen receptor activity by tyrosine phosphorylation. Cancer Cell. 2006;10:309-19.
89. Kraus S, Gioeli D, Vomastek T, Gordon V, Weber MJ. Receptor for activated C kinase 1 (RACK1) and Src regulate the tyrosine phosphorylation and function of the androgen receptor. Cancer Res. 2006;66:11047-54.
90. Hamada J, Nagayasu H, Takayama M, Kawano T, Hosokawa M, Takeichi N. Enhanced effect of epidermal growth factor on pulmonary metastasis and in vitro invasion of rat mammary carcinoma cells. Cancer Lett. 1995;89:161-7.
91. Engebraaten O, Bjerkvig R, Pedersen PH, Laerum OD. Effects of EGF, bFGF, NGF and PDGF(bb) on cell proliferative, migratory and invasive capacities of human brain-tumour biopsies in vitro. Int J Cancer. 1993;53:209-14.
92. Natalicchio A, Laviola L, De Tullio C, Renna LA, Montrone C, Perrini S, et al. Role of the p66Shc isoform in insulin-like growth factor I receptor signaling through MEK/Erk and regulation of actin cytoskeleton in rat myoblasts. J Biol Chem. 2004;279:43900-9.
93. Choudhury GG, Karamitsos C, Hernandez J, Gentilini A, Bardgette J, Abboud HE. PI-3-kinase and MAPK regulate mesangial cell proliferation and migration in response to PDGF. Am J Physiol. 1997;273:F931-8.
94. Taub J, Lau JF, Ma C, Hahn JH, Hoque R, Rothblatt J, et al. A cytosolic catalase is needed to extend adult lifespan in C. elegans daf-C and clk-1 mutants. Nature. 1999;399:162-6.
95. Taylor WR, Greenberg AH, Turley EA, Wright JA. Cell motility, invasion, and malignancy induced by overexpression of K-FGF or bFGF. Exp Cell Res. 1993;204:295-301.
96. Grossman SR, Lyle S, Resnick MB, Sabo E, Lis RT, Rosinha E, et al. p66 Shc tumor levels show a strong prognostic correlation with disease outcome in stage IIA colon cancer. Clin Cancer Res. 2007;13:5798-804.
97. Davol PA, Bagdasaryan R, Elfenbein GJ, Maizel AL, Frackelton Jr AR. Shc proteins are strong, independent prognostic markers for both node-negative and node-positive primary breast cancer. Cancer Res. 2003;63:6772-83.
98. De S, Razorenova O, McCabe NP, O'Toole T, Qin J, Byzova TV. VEGF-integrin interplay controls tumor growth and vascularization. Proc Natl Acad Sci U S A. 2005;102:7589-94.
99. Haines E, Saucier C, Claing A. The adaptor proteins p66Shc and Grb2 regulate the activation of the GTPases ARF1 and ARF6 in invasive breast cancer cells. J Biol Chem. 2014;289:5687-703.
100. Bhat HF, Baba RA, Adams ME, Khanday FA. Role of SNTA1 in Rac1 activation, modulation of ROS generation, and migratory potential of human breast cancer cells. Br J Cancer. 2014;110:706-14.
101. 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;27:5057-68.
102. Veeramani S, Chou YW, Lin FC, Muniyan S, Lin FF, Kumar S, et al. Reactive oxygen species induced by p66Shc longevity protein mediate nongenomic androgen action via tyrosine phosphorylation signaling to enhance tumorigenicity of prostate cancer cells. Free Radic Biol Med. 2012;53:95-108.
103. Chen X, Yang CS. Esophageal adenocarcinoma: a review and perspectives on the mechanism of carcinogenesis and chemoprevention. Carcinogenesis. 2001;22:1119-29.
104. Pelicci G, Giordano S, Zhen Z, Salcini AE, Lanfrancone L, Bardelli A, et al. The motogenic and mitogenic responses to HGF are amplified by the Shc adaptor protein. Oncogene. 1995;10:1631-8.
105. Fritz G, Just I, Kaina B. Rho GTPases are over-expressed in human tumors. Int J Cancer. 1999;81:682-7.
106. Li X, Xu Z, Du W, Zhang Z, Wei Y, Wang H, et al. Aiolos promotes anchorage independence by silencing p66Shc transcription in cancer cells. Cancer Cell. 2014;25:575-89.
107. Zheng Z, Yang J, Zhao D, Gao D, Yan X, Yao Z, et al. Downregulated adaptor protein p66(Shc) mitigates autophagy process by low nutrient and enhances apoptotic resistance in human lung adenocarcinoma A549 cells. FEBS J. 2013;280:4522-30.
108. Du W, Jiang Y, Zheng Z, Zhang Z, Chen N, Ma Z, et al. Feedback loop between p66(Shc) and Nrf2 promotes lung cancer progression. Cancer Lett. 2013;337:58-65.
109. Muniyan S, Chou YW, Tsai TJ, Thomes P, Veeramani S, Benigno BB, et al. p66Shc longevity protein regulates the proliferation of human ovarian cancer cells. Mol Carcinog. 2014. [Epub ahead of print]
110. Kumar S, Kumar S, Rajendran M, Alam SM, Lin FF, Cheng PW, et al. Steroids up-regulate p66Shc longevity protein in growth regulation by inhibiting its ubiquitination. PLoS One. 2011;6:e15942.
111. Benbrook DM, Nammalwar B, Long A, Matsumoto H, Singh A, Bunce RA, et al. SHetA2 interference with mortalin binding to p66shc and p53 identified using drug-conjugated magnetic microspheres. Invest New Drugs. 2014;32:412-23.
112. Liu G, Xie B, Gong L, Zhou J, Shu G. The expression of p66Shc protein in benign, premalignant, and malignant gastrointestinal lesions. Pathol Oncol Res. 2014;20:733-9.
113. Galimov ER, Sidorenko AS, Tereshkova AV, Pletiushkina O, Cherniak BV, Chumakov PM. P66shc action on resistance of colon carcinoma RKO cells to oxidative stress. Mol Biol (Mosk). 2012;46:139-46.
114. Frijhoff J, Dagnell M, Augsten M, Beltrami E, Giorgio M, Ostman A. The mitochondrial reactive oxygen species regulator p66Shc controls PDGF-induced signaling and migration through protein tyrosine phosphatase oxidation. Free Radic Biol Med. 2014;68:268-77.