ING4 regulates a secretory phenotype in primary fibroblasts with dual effects on cell proliferation and tumor growth

Oncogene

Volumn 33, Issue 15, 2014, Pages 1945-1953

  Moreno, A ^a   Soleto, I ^a   Garcia Sanz P ^a,b   Moreno Bueno, G ^a,b   Palmero, I ^a  

^a INSTITUTO DE INVESTIGACIONES BIOMÉDICAS ALBERTO SOLS   (Spain)

^b HOSPITAL UNIVERSITARIO LA PAZ IDIPAZ   (Spain)

Author keywords

ING4; p53; secretory phenotype; tumor suppression

Indexed keywords

ANIMALS; BLOTTING, WESTERN; CELL CYCLE PROTEINS; CELL LINE; CELL PROLIFERATION; CHROMATIN IMMUNOPRECIPITATION; CYTOKINES; DISEASE PROGRESSION; ENZYME-LINKED IMMUNOSORBENT ASSAY; FIBROBLASTS; HETEROGRAFTS; HOMEODOMAIN PROTEINS; HUMANS; IMMUNOHISTOCHEMISTRY; MICE; MICE, NUDE; NEOPLASMS, EXPERIMENTAL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHENOTYPE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TUMOR SUPPRESSOR PROTEINS;

EID: 84899431917     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2013.145     Document Type: Article

References (43)

1. Aguissa-Toure AH, Wong RP, Li G. The ING family tumor suppressors: From structure to function. Cell Mol Life Sci 2010; 68: 45-54
2. Coles AH, Jones SN. The ING gene family in the regulation of cell growth and tumorigenesis. J Cell Physiol 2009; 218: 45-57
3. Jafarnejad SM, Li G. Regulation of p53 by ING family members in suppression of tumor initiation and progression. Cancer Metastasis Rev 2012; 31: 55-73
4. Ythier D, Larrieu D, Brambilla C, Brambilla E, Pedeux R. The new tumor suppressor genes ING: Genomic structure and status in cancer. Int J Cancer 2008; 123: 1483-1490
5. Doyon Y, Cayrou C, Ullah M, Landry AJ, Cote V, Selleck W, et al. ING tumor suppressor proteins are critical regulators of chromatin acetylation required for genome expression and perpetuation. Mol Cell 2006; 21: 51-64
6. Pena PV, Davrazou F, Shi X, Walter KL, Verkhusha VV, Gozani O, et al. Molecular mechanism of histone H3K4me3 recognition by plant homeodomain of ING2. Nature 2006; 442: 100-103
7. Shiseki M, Nagashima M, Pedeux RM, Kitahama-Shiseki M, Miura K, Okamura S, et al. p29ING4 and p28ING5 bind to p53 and p300, and enhance p53 activity. Cancer Res 2003; 63: 2373-2378
8. Kim S, Chin K, Gray JW, Bishop JM. A screen for genes that suppress loss of contact inhibition: Identification of ING4 as a candidate tumor suppressor gene in human cancer. Proc Natl Acad Sci USA 2004; 101: 16251-16256
9. Hung T, Binda O, Champagne KS, Kuo AJ, Johnson K, Chang HY, et al. ING4 mediates crosstalk between histone H3 K4 trimethylation and H3 acetylation to attenuate cellular transformation. Mol Cell 2009; 33: 248-256
10. Garkavtsev I, Kozin SV, Chernova O, Xu L, Winkler F, Brown E, et al. The candidate tumour suppressor protein ING4 regulates brain tumour growth and angiogenesis. Nature 2004; 428: 328-332
11. Shen JC, Unoki M, Ythier D, Duperray A, Varticovski L, Kumamoto K, et al. Inhibitor of growth 4 suppresses cell spreading and cell migration by interacting with a novel binding partner, liprin alpha1. Cancer Res 2007; 67: 2552-2558
12. Li J, Martinka M, Li G. Role of ING4 in human melanoma cell migration, invasion and patient survival. Carcinogenesis 2008; 29: 1373-1379
13. Moreno A, Palacios A, Orgaz JL, Jimenez B, Blanco FJ, Palmero I. Functional impact of cancer-Associated mutations in the tumor suppressor protein ING4. Carcinogenesis 2010; 31: 1932-1938
14. Tapia C, Zlobec I, Schneider S, Kilic E, Guth U, Bubendorf L, et al. Deletion of the inhibitor of growth 4 (ING4) tumor suppressor gene is prevalent in human epidermal growth factor 2 (HER2)-positive breast cancer. Hum Pathol 2011; 42: 983-990
15. Coles AH, Gannon H, Cerny A, Kurt-Jones E, Jones SN. Inhibitor of growth-4 promotes IkappaB promoter activation to suppress NF-kappaB signaling and innate immunity. Proc Natl Acad Sci USA 2010; 107: 11423-11428
16. Kuilman T, Michaloglou C, Mooi WJ, Peeper DS. The essence of senescence. Genes Dev 2010; 24: 2463-2479
17. Collado M, Blasco MA, Serrano M. Cellular senescence in cancer and aging. Cell 2007; 130: 223-233
18. Goeman F, Thormeyer D, Abad M, Serrano M, Schmidt O, Palmero I, et al. Growth inhibition by the tumor suppressor p33ING1 in immortalized and primary cells: Involvement of two silencing domains and effect of Ras. Mol Cell Biol 2005; 25: 422-431
19. Abad M, Moreno A, Palacios A, Narita M, Blanco F, Moreno-Bueno G, et al. The tumor suppressor ING1 contributes to epigenetic control of cellular senescence. Aging Cell 2011; 10: 158-171
20. Pedeux R, Sengupta S, Shen JC, Demidov ON, Saito S, Onogi H, et al. ING2 regulates the onset of replicative senescence by induction of p300-dependent p53 acetylation. Mol Cell Biol 2005; 25: 6639-6648
21. Menendez C, Abad M, Gomez-Cabello D, Moreno A, Palmero I. ING proteins in cellular senescence. Curr Drug Targets 2009; 10: 406-417
22. Serrano M, Lin AW, McCurrach ME, Beach D, Lowe SW. Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell 1997; 88: 593-602
23. Wong RP, Lin H, Khosravi S, Piche B, Jafarnejad SM, Chen DW, et al. Tumour suppressor ING1b maintains genomic stability upon replication stress. Nucleic Acids Res 2011; 39: 3632-3642
24. Larrieu D, Ythier D, Binet R, Brambilla C, Brambilla E, Sengupta S, et al. ING2 controls the progression of DNA replication forks to maintain genome stability. EMBO Rep 2009; 10: 1168-1174
25. Campisi J, d'Adda di Fagagna F. Cellular senescence: When bad things happen to good cells. Nat Rev Mol Cell Biol 2007; 8: 729-740
26. Chicas A, Wang X, Zhang C, McCurrach M, Zhao Z, Mert O, et al. Dissecting the unique role of the retinoblastoma tumor suppressor during cellular senescence. Cancer Cell 2010; 17: 376-387
27. Nozell S, Laver T, Moseley D, Nowoslawski L, De Vos M, Atkinson GP, et al. The ING4 tumor suppressor attenuates NF-kappaB activity at the promoters of target genes. Mol Cell Biol 2008; 28: 6632-6645
28. Erez N, Truitt M, Olson P, Arron ST, Hanahan D. Cancer-Associated fibroblasts are activated in incipient neoplasia to orchestrate tumor-promoting inflammation in an NF-kappaB-dependent manner. Cancer Cell 2010; 17: 135-147
29. Lazennec G, Richmond A. Chemokines and chemokine receptors: New insights into cancer-related inflammation. Trends Mol Med 2010; 16: 133-144
30. Acosta JC, O'Loghlen A, Banito A, Guijarro MV, Augert A, Raguz S, et al. Chemokine signaling via the CXCR2 receptor reinforces senescence. Cell 2008; 133: 1006-1018
31. Chien Y, Scuoppo C, Wang X, Fang X, Balgley B, Bolden JE, et al. Control of the senescence-Associated secretory phenotype by NF-kappaB promotes senescence and enhances chemosensitivity. Genes Dev 2011; 25: 2125-2136
32. Coppe JP, Patil CK, Rodier F, Sun Y, Munoz DP, Goldstein J, et al. Senescenceassociated secretory phenotypes reveal cell-nonautonomous functions of oncogenic RAS and the p53 tumor suppressor. PLoS Biol 2008; 6: 2853-2868
33. Kuilman T, Michaloglou C, Vredeveld LC, Douma S, van Doorn R, Desmet CJ, et al. Oncogene-induced senescence relayed by an interleukin-dependent inflammatory network. Cell 2008; 133: 1019-1031
34. Kuilman T, Peeper DS. Senescence-messaging secretome: SMS-ing cellular stress. Nat Rev Cancer 2009; 9: 81-94
35. Coppe JP, Desprez PY, Krtolica A, Campisi J. The senescence-Associated secretory phenotype: The dark side of tumor suppression. Annu Rev Pathol 2010; 5: 99-118
36. Krtolica A, Parrinello S, Lockett S, Desprez PY, Campisi J. Senescent fibroblasts promote epithelial cell growth and tumorigenesis: A link between cancer and aging. Proc Natl Acad Sci USA 2001; 98: 12072-12077
37. Colla S, Tagliaferri S, Morandi F, Lunghi P, Donofrio G, Martorana D, et al. The new tumor-suppressor gene inhibitor of growth family member 4 (ING4) regulates the production of proangiogenic molecules by myeloma cells and suppresses hypoxia-inducible factor-1 alpha (HIF-1alpha) activity: Involvement in myeloma-induced angiogenesis. Blood 2007; 110: 4464-4475
38. Perkins ND. The diverse and complex roles of NF-kappaB subunits in cancer. Nat Rev Cancer 2012; 12: 121-132
39. Acosta JC, O'Loghlen A, Banito A, Raguz S, Gil J. Control of senescence by CXCR2 and its ligands. Cell Cycle 2008; 7: 2956-2959
40. Liu F, Wu S, Ren H, Gu J. Klotho suppresses RIG-I-mediated senescence-Associated inflammation. Nat Cell Biol 2011; 13: 254-262
41. Minn AJ, Gupta GP, Siegel PM, Bos PD, Shu W, Giri DD, et al. Genes that mediate breast cancer metastasis to lung. Nature 2005; 436: 518-524
42. Palmero I, Murga M, Zubiaga A, Serrano M. Activation of ARF by oncogenic stress in mouse fibroblasts is independent of E2F1 and E2F2. Oncogene 2002; 21: 2939-2947
43. Gomez-Cabello D, Callejas S, Benguria A, Moreno A, Alonso J, Palmero I. Regulation of the microRNA processor DGCR8 by the tumor suppressor ING1. Cancer Res 2010; 70: 1866-1874