Aiolos promotes anchorage independence by silencing p66Shc transcription in cancer cells

Cancer Cell

Volumn 25, Issue 5, 2014, Pages 575-589

  Li, Xichuan ^a   Xu, Zhao ^a,b   Du, Wei ^a   Zhang, Zhenfa ^a   Wei, Yiliang ^a   Wang, Hao ^a   Zhu, Zhiyan ^a   Qin, Litao ^a   Wang, Lin ^a   Niu, Qing ^a   Zhao, Xiulan ^a   Girard, Luc ^c   Gong, Yimei ^d   Ma, Zhenyi ^a   Sun, Baocun ^a   Yao, Zhi ^a   Minna, John D ^c   Terada, Lance S ^d   Liu, Zhe ^a  

^a TIANJIN MEDICAL UNIVERSITY   (China)

^b SECOND HOSPITAL OF TIANJIN MEDICAL UNIVERSITY   (China)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN P66; PROTEIN SHC; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR AIOLOS; UNCLASSIFIED DRUG;

ANCHORAGE INDEPENDENT GROWTH; ANOIKIS; ARTICLE; CANCER CELL; CANCER TISSUE; CELL ADHESION; CELL INTERACTION; CELL LINEAGE; CELL SURVIVAL; CHROMATIN STRUCTURE; CONTROLLED STUDY; GENE DISRUPTION; GENE EXPRESSION; GENE SILENCING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; LUNG CANCER; LYMPHOCYTE; METASTASIS; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; TUMOR GENE;

ANOIKIS; CARCINOMA, NON-SMALL-CELL LUNG; CELL ADHESION; CELL COMMUNICATION; CELL LINE, TUMOR; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; CHROMATIN; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; HUMANS; IKAROS TRANSCRIPTION FACTOR; LUNG; LUNG NEOPLASMS; LYMPHOPOIESIS; PROMOTER REGIONS, GENETIC; SHC SIGNALING ADAPTOR PROTEINS; TRANSCRIPTION, GENETIC;

EID: 84900312417     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccr.2014.03.020     Document Type: Article

References (49)

1. Antica M., Cicin-Sain L., Kapitanovic S., Matulic M., Dzebro S., Dominis M. Aberrant Ikaros, Aiolos, and Helios expression in Hodgkin and non-Hodgkin lymphoma. Blood 2008, 111:3296-3297.
2. Billot K., Parizot C., Arrouss I., Mazier D., Debre P., Rogner U.C., Rebollo A. Differential aiolos expression in human hematopoietic subpopulations. Leuk. Res. 2010, 34:289-293.
3. Billot K., Soeur J., Chereau F., Arrouss I., Merle-Béral H., Huang M.E., Mazier D., Baud V., Rebollo A. Deregulation of Aiolos expression in chronic lymphocytic leukemia is associated with epigenetic modifications. Blood 2011, 117:1917-1927.
4. Byers L.A., Diao L., Wang J., Saintigny P., Girard L., Peyton M., Shen L., Fan Y., Giri U., Tumula P.K., et al. An epithelial-mesenchymal transition gene signature predicts resistance to EGFR and PI3K inhibitors and identifies Axl as a therapeutic target for overcoming EGFR inhibitor resistance. Clin. Cancer Res. 2013, 19:279-290.
5. Caballero R., Setien F., Lopez-Serra L., Boix-Chornet M., Fraga M.F., Ropero S., Megias D., Alaminos M., Sanchez-Tapia E.M., Montoya M.C., et al. Combinatorial effects of splice variants modulate function of Aiolos. J.Cell Sci. 2007, 120:2619-2630.
6. Debnath J., Mills K.R., Collins N.L., Reginato M.J., Muthuswamy S.K., Brugge J.S. The role of apoptosis in creating and maintaining luminal space within normal and oncogene-expressing mammary acini. Cell 2002, 111:29-40.
7. Derksen P.W., Liu X., Saridin F., van der Gulden H., Zevenhoven J., Evers B., van Beijnum J.R., Griffioen A.W., Vink J., Krimpenfort P., et al. Somatic inactivation of E-cadherin and p53 in mice leads to metastatic lobular mammary carcinoma through induction of anoikis resistance and angiogenesis. Cancer Cell 2006, 10:437-449.
8. Duhamel M., Arrouss I., Merle-Béral H., Rebollo A. The Aiolos transcription factor is up-regulated in chronic lymphocytic leukemia. Blood 2008, 111:3225-3228.
9. Edgren H., Murumagi A., Kangaspeska S., Nicorici D., Hongisto V., Kleivi K., Rye I.H., Nyberg S., Wolf M., Borresen-Dale A.L., Kallioniemi O. Identification of fusion genes in breast cancer by paired-end RNA-sequencing. Genome Biol. 2011, 12:R6.
10. Fischer B., Arcaro A. Current status of clinical trials for small cell lung cancer. Rev. Recent Clin. Trials 2008, 3:40-61.
11. Frisch S.M., Francis H. Disruption of epithelial cell-matrix interactions induces apoptosis. J.Cell Biol. 1994, 124:619-626.
12. Frisch S.M., Schaller M., Cieply B. Mechanisms that link the oncogenic epithelial-mesenchymal transition to suppression of anoikis. J.Cell Sci. 2013, 126:21-29.
13. Giorgio M., Migliaccio E., Orsini F., Paolucci D., Moroni M., Contursi C., Pelliccia G., Luzi L., Minucci S., Marcaccio M., et al. Electron transfer between cytochrome c and p66Shc generates reactive oxygen species that trigger mitochondrial apoptosis. Cell 2005, 122:221-233.
14. Glodek A.M., Honczarenko M., Le Y., Campbell J.J., Silberstein L.E. Sustained activation of cell adhesion is a differentially regulated process in B lymphopoiesis. J.Exp. Med. 2003, 197:461-473.
15. Han H.J., Russo J., Kohwi Y., Kohwi-Shigematsu T. SATB1 reprogrammes gene expression to promote breast tumour growth and metastasis. Nature 2008, 452:187-193.
16. Heintzman N.D., Stuart R.K., Hon G., Fu Y., Ching C.W., Hawkins R.D., Barrera L.O., Van Calcar S., Qu C., Ching K.A., et al. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat. Genet. 2007, 39:311-318.
17. Hermann P.C., Huber S.L., Herrler T., Aicher A., Ellwart J.W., Guba M., Bruns C.J., Heeschen C. Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell 2007, 1:313-323.
18. Holmfeldt L., Wei L., Diaz-Flores E., Walsh M., Zhang J., Ding L., Payne-Turner D., Churchman M., Andersson A., Chen S.C., et al. The genomic landscape of hypodiploid acute lymphoblastic leukemia. Nat. Genet. 2013, 45:242-252.
19. Hystad M.E., Myklebust J.H., Bø T.H., Sivertsen E.A., Rian E., Forfang L., Munthe E., Rosenwald A., Chiorazzi M., Jonassen I., et al. Characterization of early stages of human B cell development by gene expression profiling. J.Immunol. 2007, 179:3662-3671.
20. Jackman D.M., Johnson B.E. Small-cell lung cancer. Lancet 2005, 366:1385-1396.
21. Jung M.J., Rho J.K., Kim Y.M., Jung J.E., Jin Y.B., Ko Y.G., Lee J.S., Lee S.J., Lee J.C., Park M.J. Upregulation of CXCR4 is functionally crucial for maintenance of stemness in drug-resistant non-small cell lung cancer cells. Oncogene 2013, 32:209-221.
22. Kilpinen S., Autio R., Ojala K., Iljin K., Bucher E., Sara H., Pisto T., Saarela M., Skotheim R.I., Björkman M., et al. Systematic bioinformatic analysis of expression levels of 17,330 human genes across 9,783 samples from 175 types of healthy and pathological tissues. Genome Biol. 2008, 9:R139.
23. Kim J., Sif S., Jones B., Jackson A., Koipally J., Heller E., Winandy S., Viel A., Sawyer A., Ikeda T., et al. Ikaros DNA-binding proteins direct formation of chromatin remodeling complexes in lymphocytes. Immunity 1999, 10:345-355.
24. Koipally J., Renold A., Kim J., Georgopoulos K. Repression by Ikaros and Aiolos is mediated through histone deacetylase complexes. EMBO J. 1999, 18:3090-3100.
25. Kumar S., Park S.H., Cieply B., Schupp J., Killiam E., Zhang F., Rimm D.L., Frisch S.M. A pathway for the control of anoikis sensitivity by E-cadherin and epithelial-to-mesenchymal transition. Mol. Cell. Biol. 2011, 31:4036-4051.
26. Ma Z., Myers D.P., Wu R.F., Nwariaku F.E., Terada L.S. p66Shc mediates anoikis through RhoA. J.Cell Biol. 2007, 179:23-31.
27. Ma S., Pathak S., Trinh L., Lu R. Interferon regulatory factors 4 and 8 induce the expression of Ikaros and Aiolos to down-regulate pre-B-cell receptor and promote cell-cycle withdrawal in pre-B-cell development. Blood 2008, 111:1396-1403.
28. Ma Z., Liu Z., Wu R.F., Terada L.S. p66(Shc) restrains Ras hyperactivation and suppresses metastatic behavior. Oncogene 2010, 29:5559-5567.
29. Mainiero F., Murgia C., Wary K.K., Curatola A.M., Pepe A., Blumemberg M., Westwick J.K., Der C.J., Giancotti F.G. The coupling of alpha6beta4 integrin to Ras-MAP kinase pathways mediated by Shc controls keratinocyte proliferation. EMBO J. 1997, 16:2365-2375.
30. Mandal M., Powers S.E., Ochiai K., Georgopoulos K., Kee B.L., Singh H., Clark M.R. Ras orchestrates exit from the cell cycle and light-chain recombination during early B cell development. Nat. Immunol. 2009, 10:1110-1117.
31. Mehlen P., Puisieux A. Metastasis: a question of life or death. Nat. Rev. Cancer 2006, 6:449-458.
32. Morgan B., Sun L., Avitahl N., Andrikopoulos K., Ikeda T., Gonzales E., Wu P., Neben S., Georgopoulos K. Aiolos, a lymphoid restricted transcription factor that interacts with Ikaros to regulate lymphocyte differentiation. EMBO J. 1997, 16:2004-2013.
33. Müller A., Homey B., Soto H., Ge N., Catron D., Buchanan M.E., McClanahan T., Murphy E., Yuan W., Wagner S.N., et al. Involvement of chemokine receptors in breast cancer metastasis. Nature 2001, 410:50-56.
34. Niebuhr B., Kriebitzsch N., Fischer M., Behrens K., Günther T., Alawi M., Bergholz U., Müller U., Roscher S., Ziegler M., et al. Runx1 is essential at two stages of early murine B-cell development. Blood 2013, 122:413-423.
35. Onder T.T., Gupta P.B., Mani S.A., Yang J., Lander E.S., Weinberg R.A. Loss of E-cadherin promotes metastasis via multiple downstream transcriptional pathways. Cancer Res. 2008, 68:3645-3654.
36. Osborne J.K., Larsen J.E., Shields M.D., Gonzales J.X., Shames D.S., Sato M., Kulkarni A., Wistuba I.I., Girard L., Minna J.D., Cobb M.H. NeuroD1 regulates survival and migration of neuroendocrine lung carcinomas via signaling molecules TrkB and NCAM. Proc. Natl. Acad. Sci. USA. 2013, 110:6524-6529.
37. Pelicci G., Lanfrancone L., Grignani F., McGlade J., Cavallo F., Forni G., Nicoletti I., Grignani F., Pawson T., Pelicci P.G. A novel transforming protein (SHC) with an SH2 domain is implicated in mitogenic signal transduction. Cell 1992, 70:93-104.
38. Quintana F.J., Jin H., Burns E.J., Nadeau M., Yeste A., Kumar D., Rangachari M., Zhu C., Xiao S., Seavitt J., et al. Aiolos promotes TH17 differentiation by directly silencing Il2 expression. Nat. Immunol. 2012, 13:770-777.
39. Rada-Iglesias A., Bajpai R., Swigut T., Brugmann S.A., Flynn R.A., Wysocka J. A unique chromatin signature uncovers early developmental enhancers in humans. Nature 2011, 470:279-283.
40. Reynaud D., Demarco I.A., Reddy K.L., Schjerven H., Bertolino E., Chen Z., Smale S.T., Winandy S., Singh H. Regulation of B cell fate commitment and immunoglobulin heavy-chain gene rearrangements by Ikaros. Nat. Immunol. 2008, 9:927-936.
41. Romero F., Martínez-A C., Camonis J., Rebollo A. Aiolos transcription factor controls cell death in Tcells by regulating Bcl-2 expression and its cellular localization. EMBO J. 1999, 18:3419-3430.
42. Sung Y.M., Xu X., Sun J., Mueller D., Sentissi K., Johnson P., Urbach E., Seillier-Moiseiwitsch F., Johnson M.D., Mueller S.C. Tumor suppressor function of Syk in human MCF10A invitro and normal mouse mammary epithelium invivo. PLoS ONE 2009, 4:e7445.
43. Thompson E.C., Cobb B.S., Sabbattini P., Meixlsperger S., Parelho V., Liberg D., Taylor B., Dillon N., Georgopoulos K., Jumaa H., et al. Ikaros DNA-binding proteins as integral components of B cell developmental-stage-specific regulatory circuits. Immunity 2007, 26:335-344.
44. Timp W., Feinberg A.P. Cancer as a dysregulated epigenome allowing cellular growth advantage at the expense of the host. Nat. Rev. Cancer 2013, 13:497-510.
45. Valastyan S., Weinberg R.A. Tumor metastasis: molecular insights and evolving paradigms. Cell 2011, 147:275-292.
46. Ventura A., Luzi L., Pacini S., Baldari C.T., Pelicci P.G. The p66Shc longevity gene is silenced through epigenetic modifications of an alternative promoter. J.Biol. Chem. 2002, 277:22370-22376.
47. Wang J.H., Avitahl N., Cariappa A., Friedrich C., Ikeda T., Renold A., Andrikopoulos K., Liang L., Pillai S., Morgan B.A., Georgopoulos K. Aiolos regulates B cell activation and maturation to effector state. Immunity 1998, 9:543-553.
48. Wary K.K., Mainiero F., Isakoff S.J., Marcantonio E.E., Giancotti F.G. The adaptor protein Shc couples a class of integrins to the control of cell cycle progression. Cell 1996, 87:733-743.
49. Xi G., Shen X., Clemmons D.R. p66shc inhibits insulin-like growth factor-I signaling via direct binding to Src through its polyproline and Src homology 2 domains, resulting in impairment of Src kinase activation. J.Biol. Chem. 2010, 285:6937-6951.