Reduced ING1 levels in breast cancer promotes metastasis

Oncotarget

Volumn 5, Issue 12, 2014, Pages 4244-4256

  Thakur, Satbir ^a   Singla, Arvind K ^a   Chen, Jie ^a   Tran, Uyen ^a   Yang, Yang ^a   Salazar, Carolina ^a   Magliocco, Anthony ^c   Klimowicz, Alexander ^d,e   Jirik, Frank ^a   Riabowol, Karl ^a,b  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

^c H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

^d TOM BAKER CANCER CENTRE   (Canada)

^e BOEHRINGER INGELHEIM PHARMACEUTICALS INC   (United States)

Author keywords

Breast cancer; Epigenetics; ING1; Metastasis; Survival

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 2; ESTROGEN RECEPTOR; INHIBITOR OF GROWTH 1 PROTEIN; ONCOPROTEIN; TRANSCRIPTOME; UNCLASSIFIED DRUG; ING1 PROTEIN, HUMAN; NUCLEAR PROTEIN; SIGNAL PEPTIDE; TUMOR SUPPRESSOR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOMATED QUANTITATIVE FLUORESCENCE IMMUNOHISTOCHEMISTRY; BIOASSAY; BREAST CANCER; CANCER PROGNOSIS; CANCER RECURRENCE; CELL ASSAY; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE SPECIFIC SURVIVAL; DISTANT METASTASIS FREE SURVIVAL; DOWN REGULATION; FEMALE; FLUORESCENCE HISTOCHEMISTRY; GENE CONTROL; HUMAN; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MAJOR CLINICAL STUDY; METASTASIS; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PREDICTION; PROTEIN EXPRESSION; PROTEIN FUNCTION; TUMOR VOLUME; UPREGULATION; ANIMAL; BREAST TUMOR; COHORT ANALYSIS; DISEASE COURSE; GENETIC TRANSFECTION; GENETICS; METABOLISM; MORTALITY; PATHOLOGY; PROGNOSIS; TUMOR SUPPRESSOR GENE;

ANIMALS; BREAST NEOPLASMS; COHORT STUDIES; DISEASE PROGRESSION; FEMALE; GENES, TUMOR SUPPRESSOR; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; NEOPLASM METASTASIS; NUCLEAR PROTEINS; PROGNOSIS; TRANSFECTION; TUMOR SUPPRESSOR PROTEINS;

EID: 84905113829     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.1988     Document Type: Article

References (44)

1. Garkavtsev I, Kazarov A, Gudkov A and Riabowol K. Suppression of the novel growth inhibitor p33ING1 promotes neoplastic transformation. Nature genetics. 1996; 14(4): 415-420.
2. Nouman GS, Anderson JJ, Crosier S, Shrimankar J, Lunec J and Angus B. Downregulation of nuclear expression of the p33(ING1b) inhibitor of growth protein in invasive carcinoma of the breast. J Clin Pathol. 2003; 56(7): 507-511.
3. Toyama T, Iwase H, Watson P, Muzik H, Saettler E, Magliocco A, DiFrancesco L, Forsyth P, Garkavtsev I, Kobayashi S and Riabowol K. Suppression of ING1 expression in sporadic breast cancer. Oncogene. 1999; 18(37): 5187-5193.
4. Doyon Y, Cayrou C, Ullah M, Landry AJ, Cote V, Selleck W, Lane WS, Tan S, Yang XJ and Cote J. ING tumor suppressor proteins are critical regulators of chromatin acetylation required for genome expression and perpetuation. Mol Cell. 2006; 21(1): 51-64.
5. Hung T, Binda O, Champagne KS, Kuo AJ, Johnson K, Chang HY, Simon MD, Kutateladze TG and Gozani O. ING4 mediates crosstalk between histone H3 K4 trimethylation and H3 acetylation to attenuate cellular transformation. Mol Cell. 2009; 33(2): 248-256.
6. Loewith R, Meijer M, Lees-Miller SP, Riabowol K and Young D. Three yeast proteins related to the human candidate tumor suppressor p33(ING1) are associated with histone acetyltransferase activities. Molecular and cellular biology. 2000; 20(11): 3807-3816.
7. Feng X, Bonni S and Riabowol K. HSP70 induction by ING proteins sensitizes cells to tumor necrosis factor alpha receptor-mediated apoptosis. Molecular and cellular biology. 2006; 26(24): 9244-9255.
8. Pena PV, Davrazou F, Shi X, Walter KL, Verkhusha VV, Gozani O, Zhao R and Kutateladze TG. Molecular mechanism of histone H3K4me3 recognition by plant homeodomain of ING2. Nature. 2006; 442(7098): 100-103.
9. Shi X, Hong T, Walter KL, Ewalt M, Michishita E, Hung T, Carney D, Pena P, Lan F, Kaadige MR, Lacoste N, Cayrou C, Davrazou F, Saha A, Cairns BR, Ayer DE, et al. ING2 PHD domain links histone H3 lysine 4 methylation to active gene repression. Nature. 2006; 442(7098): 96-99.
10. Vieyra D, Toyama T, Hara Y, Boland D, Johnston R and Riabowol K. ING1 isoforms differentially affect apoptosis in a cell age-dependent manner. Cancer research. 2002; 62(15): 4445-4452.
11. Schafer A, Karaulanov E, Stapf U, Doderlein G and Niehrs C. Ing1 functions in DNA demethylation by directing Gadd45a to H3K4me3. Genes & development. 2013; 27(3): 261-273.
12. GraffJR, Gabrielson E, Fujii H, Baylin SB and Herman JG. Methylation patterns of the E-cadherin 5' CpG island are unstable and reflect the dynamic, heterogeneous loss of E-cadherin expression during metastatic progression. The Journal of biological chemistry. 2000; 275(4): 2727-2732.
13. Peinado H, Ballestar E, Esteller M and Cano A. Snail mediates E-cadherin repression by the recruitment of the Sin3A/histone deacetylase 1 (HDAC1)/HDAC2 complex. Molecular and cellular biology. 2004; 24(1): 306-319.
14. Vanharanta S, Shu W, Brenet F, Hakimi AA, Heguy A, Viale A, Reuter VE, Hsieh JJ, Scandura JM and Massague J. Epigenetic expansion of VHL-HIF signal output drives multiorgan metastasis in renal cancer. Nature medicine. 2013; 19(1): 50-56.
15. Fang F, Turcan S, Rimner A, Kaufman A, Giri D, Morris LG, Shen R, Seshan V, Mo Q, Heguy A, Baylin SB, Ahuja N, Viale A, Massague J, Norton L, Vahdat LT, et al. Breast cancer methylomes establish an epigenomic foundation for metastasis. Science translational medicine. 2011; 3(75): 75ra25.
16. Shimada H, Liu TL, Ochiai T, Shimizu T, Haupt Y, Hamada H, Abe T, Oka M, Takiguchi M and Hiwasa T. Facilitation of adenoviral wild-type p53-induced apoptotic cell death by overexpression of p33(ING1) in T. Tn human esophageal carcinoma cells. Oncogene. 2002; 21(8): 1208-1216.
17. Shinoura N, Muramatsu Y, Nishimura M, Yoshida Y, Saito A, Yokoyama T, Furukawa T, Horii A, Hashimoto M, Asai A, Kirino T and Hamada H. Adenovirus-mediated transfer of p33ING1 with p53 drastically augments apoptosis in gliomas. Cancer research. 1999; 59(21): 5521-5528.
18. Xie Y, Zhang H, Sheng W, Xiang J, Ye Z and Yang J. Adenovirus-mediated ING4 expression suppresses lung carcinoma cell growth via induction of cell cycle alteration and apoptosis and inhibition of tumor invasion and angiogenesis. Cancer letters. 2008; 271(1): 105-116.
19. Zhang X, Xu LS, Wang ZQ, Wang KS, Li N, Cheng ZH, Huang SZ, Wei DZ and Han ZG. ING4 induces G2/M cell cycle arrest and enhances the chemosensitivity to DNA-damage agents in HepG2 cells. FEBS Lett. 2004; 570(1-3):7-12.
20. Thakur S, Feng X, Qiao Shi Z, Ganapathy A, Kumar Mishra M, Atadja P, Morris D and Riabowol K. ING1 and 5-azacytidine act synergistically to block breast cancer cell growth. PloS one. 2012; 7(8): e43671.
21. Thalappilly S, Feng X, Pastyryeva S, Suzuki K, Muruve D, Larocque D, Richard S, Truss M, von Deimling A, Riabowol K and Tallen G. The p53 tumor suppressor is stabilized by inhibitor of growth 1 (ING1) by blocking polyubiquitination. PloS one. 2011; 6(6): e21065.
22. Li F, Li J, Sheng H, Dai L, Cheng K and Lin S. [Mutation of ING1 gene in laryngeal squamous cell carcinoma and its association with p33ING1b protein expression]. Lin chuang er bi yan hou tou jing wai ke za zhi = Journal of clinical otorhinolaryngology, head, and neck surgery. 2011; 25(21): 986-989.
23. Li J, Martinka M and Li G. Role of ING4 in human melanoma cell migration, invasion and patient survival. Carcinogenesis. 2008; 29(7): 1373-1379.
24. Lu M, Chen F, Wang Q, Wang K, Pan Q and Zhang X. Downregulation of inhibitor of growth 3 is correlated with tumorigenesis and progression of hepatocellular carcinoma. Oncol Lett. 2012; 4(1): 47-52.
25. Wang QS, Li M, Zhang LY, Jin Y, Tong DD, Yu Y, Bai J, Huang Q, Liu FL, Liu A, Lee KY and Fu SB. Down-regulation of ING4 is associated with initiation and progression of lung cancer. Histopathology. 2010; 57(2): 271-281.
26. Garkavtsev I, Kozin SV, Chernova O, Xu L, Winkler F, Brown E, Barnett GH and Jain RK. The candidate tumour suppressor protein ING4 regulates brain tumour growth and angiogenesis. Nature. 2004; 428(6980): 328-332.
27. Tallen G, Farhangi S, Tamannai M, Holtkamp N, Mangoldt D, Shah S, Suzuki K, Truss M, Henze G, Riabowol K and von Deimling A. The inhibitor of growth 1 (ING1) proteins suppress angiogenesis and differentially regulate angiopoietin expression in glioblastoma cells. Oncology research. 2009; 18(2-3):95-105.
28. Liu Y, Yu L, Wang Y, Zhang Y and Zhang G. Expression of tumor suppressor gene ING4 in ovarian carcinoma is correlated with microvessel density. J Cancer Res Clin Oncol. 2012; 138(4): 647-655.
29. Guo XB, Jing CQ, Li LP, Zhang L, Shi YL, Wang JS, Liu JL and Li CS. Down-regulation of miR-622 in gastric cancer promotes cellular invasion and tumor metastasis by targeting ING1 gene. World journal of gastroenterology: WJG. 2011; 17(14): 1895-1902.
30. Umbricht CB, Evron E, Gabrielson E, Ferguson A, Marks J and Sukumar S. Hypermethylation of 14-3-3 sigma (stratifin) is an early event in breast cancer. Oncogene. 2001; 20(26): 3348-3353.
31. (1997). AJCC Cancer Staging Manual. (Philadelphia Lippincott-Raven).
32. Camp RL, Chung GG and Rimm DL. Automated subcellular localization and quantification of protein expression in tissue microarrays. Nature medicine. 2002; 8(11): 1323-1327.
33. Suzuki K, Boland D, Gong W and Riabowol K. Domain recognition of the ING1 tumor suppressor by a panel of monoclonal antibodies. Hybridoma (Larchmt). 2011; 30(3): 239-245.
34. Jechlinger M, Sommer A, Moriggl R, Seither P, Kraut N, Capodiecci P, Donovan M, Cordon-Cardo C, Beug H and Grunert S. Autocrine PDGFR signaling promotes mammary cancer metastasis. J Clin Invest. 2006; 116(6): 1561-1570.
35. Schito L, Rey S, Tafani M, Zhang H, Wong CC, Russo A, Russo MA and Semenza GL. Hypoxia-inducible factor 1-dependent expression of platelet-derived growth factor B promotes lymphatic metastasis of hypoxic breast cancer cells. Proceedings of the National Academy of Sciences of the United States of America. 2012; 109(40): E2707-2716.
36. Bondareva A, Downey CM, Ayres F, Liu W, Boyd SK, Hallgrimsson B and Jirik FR. The lysyl oxidase inhibitor, beta-aminopropionitrile, diminishes the metastatic colonization potential of circulating breast cancer cells. PloS one. 2009; 4(5): e5620.
37. Taube JH, Herschkowitz JI, Komurov K, Zhou AY, Gupta S, Yang J, Hartwell K, Onder TT, Gupta PB, Evans KW, Hollier BG, Ram PT, Lander ES, Rosen JM, Weinberg RA and Mani SA. Core epithelial-to-mesenchymal transition interactome gene-expression signature is associated with claudin-low and metaplastic breast cancer subtypes. Proceedings of the National Academy of Sciences of the United States of America. 2010; 107(35): 15449-15454.
38. Carvalho I, Milanezi F, Martins A, Reis RM and Schmitt F. Overexpression of platelet-derived growth factor receptor alpha in breast cancer is associated with tumour progression. Breast cancer research: BCR. 2005; 7(5): R788-795.
39. Kuzmichev A, Zhang Y, Erdjument-Bromage H, Tempst P and Reinberg D. Role of the Sin3-histone deacetylase complex in growth regulation by the candidate tumor suppressor p33(ING1). Molecular and cellular biology. 2002; 22(3): 835-848.
40. Smith KT, Martin-Brown SA, Florens L, Washburn MP and Workman JL. Deacetylase inhibitors dissociate the histone-targeting ING2 subunit from the Sin3 complex. Chem Biol. 2010; 17(1): 65-74.
41. Luu TH, Morgan RJ, Leong L, Lim D, McNamara M, Portnow J, Frankel P, Smith DD, Doroshow JH, Wong C, Aparicio A, Gandara DR and Somlo G. A phase II trial of vorinostat (suberoylanilide hydroxamic acid) in metastatic breast cancer: a California Cancer Consortium study. Clinical cancer research: an official journal of the American Association for Cancer Research. 2008; 14(21): 7138-7142.
42. Munster PN, Thurn KT, Thomas S, Raha P, Lacevic M, Miller A, Melisko M, Ismail-Khan R, Rugo H, Moasser M and Minton SE. A phase II study of the histone deacetylase inhibitor vorinostat combined with tamoxifen for the treatment of patients with hormone therapy-resistant breast cancer. British journal of cancer. 2011; 104(12): 1828-1835.
43. He GH, Helbing CC, Wagner MJ, Sensen CW and Riabowol K. Phylogenetic analysis of the ING family of PHD finger proteins. Molecular biology and evolution. 2005; 22(1): 104-116.
44. Hostetter CL, Licata LA and Keen JC. Timing is everything: order of administration of 5-aza 2' deoxycytidine, trichostatin A and tamoxifen changes estrogen receptor mRNA expression and cell sensitivity. Cancer letters. 2009; 275(2): 178-184.