Tumor suppressor XAF1 induces apoptosis, inhibits angiogenesis and inhibits tumor growth in hepatocellular carcinoma

Oncotarget

Volumn 5, Issue 14, 2014, Pages 5403-5415

  Zhu, Li Ming ^a,b   Shi, Dong Mei ^c   Dai, Qiang ^a   Cheng, Xiao Jiao ^b   Yao, Wei Yan ^b   Sun, Ping Hu ^b   Ding, Yanfei ^b   Qiao, Min Min ^b   Wu, Yun Lin ^b   Jiang, Shi Hu ^b   Tu, Shui Ping ^b  

^a School of Medicine   (China)

^b SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^c FUDAN UNIVERSITY   (China)

Author keywords

Angiogenesis; Apoptosis; Hepatocellular cancer; VEGF; XAF1

Indexed keywords

ADENOVIRUS VECTOR; ANTINEOPLASTIC AGENT; CASPASE 3; CASPASE 8; CASPASE 9; FLUOROURACIL; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN X LINKED INHIBITOR OF APOPTOSIS ASSOCIATED FACTOR 1; UNCLASSIFIED DRUG; VASCULOTROPIN; X LINKED INHIBITOR OF APOPTOSIS; X LINKED INHIBITOR OF APOPTOSIS ASSOCIATED FACTOR 1; SIGNAL PEPTIDE; TUMOR PROTEIN; XAF1 PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CANCER GENE THERAPY; CANCER INHIBITION; CANCER SURVIVAL; CLINICAL ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; DRUG MECHANISM; DRUG SAFETY; EMBRYO; FEMALE; GENE EXPRESSION; HEPATOCELLULAR CARCINOMA CELL LINE; HUMAN; HUMAN CELL; HUMAN TISSUE; LIVER CELL CARCINOMA; MOUSE; NONHUMAN; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN SYNTHESIS INHIBITION; SURVIVAL TIME; TUMOR SUPPRESSOR GENE; TUMOR VOLUME; TUMOR XENOGRAFT; VIRAL GENE DELIVERY SYSTEM; XAF1 GENE; ANIMAL; CARCINOMA, HEPATOCELLULAR; CELL PROLIFERATION; GENE THERAPY; GENETIC TRANSFECTION; GENETICS; HEK293 CELL LINE; LIVER NEOPLASMS; METABOLISM; NEOVASCULARIZATION, PATHOLOGIC; PATHOLOGY; TUMOR CELL LINE; VASCULARIZATION;

ANIMALS; APOPTOSIS; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; CELL PROLIFERATION; DOWN-REGULATION; GENETIC THERAPY; HEK293 CELLS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIVER NEOPLASMS; MICE; NEOPLASM PROTEINS; NEOVASCULARIZATION, PATHOLOGIC; TRANSFECTION;

EID: 84906236889     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2114     Document Type: Article

References (57)

1. Jain S, Singhal S, Lee P and Xu R. Molecular genetics of hepatocellular neoplasia. American journal of translational research. 2010; 2(1):105.
2. Henry LR, Lee HO, Lee JS, Klein-Szanto A, Watts P, Ross EA, Chen WT and Cheng JD. Clinical implications of fibroblast activation protein in patients with colon cancer. Clin Cancer Res. 2007; 13(6):1736-1741.
3. Yi Li Y and LI XM. The IAP family: endogenous caspase inhibitors with multiple biological activities. Cell research. 2000; 10(3):169-177.
4. Ngan CY, Yamamoto H, Seshimo I, Tsujino T, Man-i M, Ikeda JI, Konishi K, Takemasa I, Ikeda M, Sekimoto M, Matsuura N and Monden M. Quantitative evaluation of vimentin expression in tumour stroma of colorectal cancer. Br J Cancer. 2007; 96(6):986-992.
5. Salvesen GS and Duckett CS. IAP proteins: blocking the road to death's door. Nature Reviews Molecular Cell Biology. 2002; 3(6):401-410.
6. Zhu L, Cheng X, Ding Y, Shi J, Jin H, Wang H, Wu Y, Ye J, Lu Y, Wang TC, Yang CS and Tu SP. Bone marrow-derived myofibroblasts promote colon tumorigenesis through the IL-6/JAK2/STAT3 pathway. Cancer Lett. 2014; 343(1):80-89.
7. LeBleu VS, Taduri G, O'Connell J, Teng Y, Cooke VG, Woda C, Sugimoto H and Kalluri R. Origin and function of myofibroblasts in kidney fibrosis. Nat Med. 2013; 19(8):1047-1053.
8. Tu SP, Chi AL, Ai W, Takaishi S, Dubeykovskaya Z, Quante M, Fox JG and Wang TC. p53 inhibition of AP1-dependent TFF2 expression induces apoptosis and inhibits cell migration in gastric cancer cells. Am J Physiol Gastrointest Liver Physiol. 2009; 297(2):G385-396.
9. Pan Q, Liu B, Liu J, Cai R, Liu X and Qian C. Synergistic antitumor activity of XIAP-shRNA and TRAIL expressed by oncolytic adenoviruses in experimental HCC. Acta Oncol. 2008; 47(1):135-144.
10. Yamaguchi Y, Shiraki K, Fuke H, Inoue T, Miyashita K, Yamanaka Y, Saitou Y, Sugimoto K and Nakano T. Targeting of X-linked inhibitor of apoptosis protein or survivin by short interfering RNAs sensitize hepatoma cells to TNF-related apoptosis-inducing ligand-and chemotherapeutic agent-induced cell death. Oncol Rep. 2005; 14(5):1311-1316.
11. Zhu AX, Duda DG, Sahani DV and Jain RK. HCC and angiogenesis: possible targets and future directions. Nat Rev Clin Oncol. 8(5):292-301.
12. Hicklin DJ and Ellis LM. Role of the vascular endothelial growth factor pathway in tumor growth and angiogenesis. J Clin Oncol. 2005; 23(5):1011-1027.
13. Moon WS, Rhyu KH, Kang MJ, Lee DG, Yu HC, Yeum JH, Koh GY and Tarnawski AS. Overexpression of VEGF and angiopoietin 2: a key to high vascularity of hepatocellular carcinoma? Mod Pathol. 2003; 16(6):552-557.
14. Tseng PL, Tai MH, Huang CC, Wang CC, Lin JW, Hung CH, Chen CH, Wang JH, Lu SN, Lee CM, Changchien CS and Hu TH. Overexpression of VEGF is associated with positive p53 immunostaining in hepatocellular carcinoma (HCC) and adverse outcome of HCC patients. J Surg Oncol. 2008; 98(5):349-357.
15. Finn RS and Zhu AX. Targeting angiogenesis in hepatocellular carcinoma: focus on VEGF and bevacizumab. Expert Rev Anticancer Ther. 2009; 9(4):503-509.
16. Liston P, Fong WG, Kelly NL, Toji S, Miyazaki T, Conte D, Tamai K, Craig CG, McBurney MW and Korneluk RG. Identification of XAF1 as an antagonist of XIAP anti-Caspase activity. Nat Cell Biol. 2001; 3(2):128-133.
17. Fong WG, Liston P, Rajcan-Separovic E, St Jean M, Craig C and Korneluk RG. Expression and genetic analysis of XIAP-associated factor 1 (XAF1) in cancer cell lines. Genomics. 2000; 70(1):113-122.
18. Byun DS, Cho K, Ryu BK, Lee MG, Kang MJ, Kim HR and Chi SG. Hypermethylation of XIAP-associated factor 1, a putative tumor suppressor gene from the 17p13.2 locus, in human gastric adenocarcinomas. Cancer Res. 2003; 63(21):7068-7075.
19. Ma TL, Ni PH, Zhong J, Tan JH, Qiao MM and Jiang SH. Low expression of XIAP-associated factor 1 in human colorectal cancers. Chin J Dig Dis. 2005; 6(1):10-14.
20. Huang J, Yao WY, Zhu Q, Tu SP, Yuan F, Wang HF, Zhang YP and Yuan YZ. XAF1 as a prognostic biomarker and therapeutic target in pancreatic cancer. Cancer Sci. 101(2):559-567.
21. Wang Y, Mao H, Hao Q, Yang Y, Shen L, Huang S and Liu P. Association of expression of XIAP-associated factor 1 (XAF1) with clinicopathologic factors, overall survival, microvessel density and cisplatin-resistance in ovarian cancer. Regul Pept. 178(1-3):36-42.
22. Chung SK, Lee MG, Ryu BK, Lee JH, Han J, Byun DS, Chae KS, Lee KY, Jang JY, Kim HJ and Chi SG. Frequent alteration of XAF1 in human colorectal cancers: implication for tumor cell resistance to apoptotic stresses. Gastroenterology. 2007; 132(7):2459-2477.
23. Zou B, Chim CS, Zeng H, Leung SY, Yang Y, Tu SP, Lin MC, Wang J, He H, Jiang SH, Sun YW, Yu LF, Yuen ST, Kung HF and Wong BC. Correlation between the single-site CpG methylation and expression silencing of the XAF1 gene in human gastric and colon cancers. Gastroenterology. 2006; 131(6):1835-1843.
24. Ng KC, Campos EI, Martinka M and Li G. XAF1 expression is significantly reduced in human melanoma. J Invest Dermatol. 2004; 123(6):1127-1134.
25. Fang X, Liu Z, Fan Y, Zheng C, Nilson S, Egevad L, Ekman P and Xu D. Switch to full-length of XAF1 mRNA expression in prostate cancer cells by the DNA methylation inhibitor. Int J Cancer. 2006; 118(10):2485-2489.
26. Kempkensteffen C, Hinz S, Schrader M, Christoph F, Magheli A, Krause H, Schostak M, Miller K and Weikert S. Gene expression and promoter methylation of the XIAP-associated Factor 1 in renal cell carcinomas: correlations with pathology and outcome. Cancer Lett. 2007; 254(2):227-235.
27. Lee MG, Huh JS, Chung SK, Lee JH, Byun DS, Ryu BK, Kang MJ, Chae KS, Lee SJ, Lee CH, Kim JI, Chang SG and Chi SG. Promoter CpG hypermethylation and downregulation of XAF1 expression in human urogenital malignancies: implication for attenuated p53 response to apoptotic stresses. Oncogene. 2006; 25(42):5807-5822.
28. Sakemi R, Yano H, Ogasawara S, Akiba J, Nakashima O, Fukahori S, Sata M and Kojiro M. X-linked inhibitor of apoptosis (XIAP) and XIAP-associated factor-1 expressions and their relationship to apoptosis in human hepatocellular carcinoma and non-cancerous liver tissues. Oncol Rep. 2007; 18(1):65-70.
29. Tu SP, Liston P, Cui JT, Lin MC, Jiang XH, Yang Y, Gu Q, Jiang SH, Lum CT, Kung HF, Korneluk RG and Wong BC. Restoration of XAF1 expression induces apoptosis and inhibits tumor growth in gastric cancer. Int J Cancer. 2009; 125(3):688-697.
30. Tu SP, Sun YW, Cui JT, Zou B, Lin MC, Gu Q, Jiang SH, Kung HF, Korneluk RG and Wong BC. Tumor suppressor XIAP-Associated factor 1 (XAF1) cooperates with tumor necrosis factor-related apoptosis-inducing ligand to suppress colon cancer growth and trigger tumor regression. Cancer. 116(5):1252-1263.
31. Sun PH, Zhu LM, Qiao MM, Zhang YP, Jiang SH, Wu YL and Tu SP. The XAF1 tumor suppressor induces autophagic cell death via upregulation of Beclin-1 and inhibition of Akt pathway. Cancer Lett. 310(2):170-180.
32. Zhang W, Guo Z, Jiang B, Niu L, Xia G, Wang X, Cheng T, Zhang Y and Wang J. Identification of a functional p53 responsive element within the promoter of XAF1 gene in gastrointestinal cancer cells. Int J Oncol. 36(4):1031-1037.
33. Qiao L, Gu Q, Dai Y, Shen Z, Liu X, Qi R, Ma J, Zou B, Li Z, Lan HY and Wong BC. XIAP-associated factor 1 (XAF1) suppresses angiogenesis in mouse endothelial cells. Tumour Biol. 2008; 29(2):122-129.
34. Arora V, Cheung HH, Plenchette S, Micali OC, Liston P and Korneluk RG. Degradation of survivin by the X-linked inhibitor of apoptosis (XIAP)-XAF1 complex. J Biol Chem. 2007; 282(36):26202-26209.
35. O'Connor DS, Schechner JS, Adida C, Mesri M, Rothermel AL, Li F, Nath AK, Pober JS and Altieri DC. Control of apoptosis during angiogenesis by survivin expression in endothelial cells. Am J Pathol. 2000; 156(2):393-398.
36. Kawasaki H, Toyoda M, Shinohara H, Okuda J, Watanabe I, Yamamoto T, Tanaka K, Tenjo T and Tanigawa N. Expression of survivin correlates with apoptosis, proliferation, and angiogenesis during human colorectal tumorigenesis. Cancer. 2001; 91(11):2026-2032.
37. Tu SP, Jiang XH, Lin MC, Cui JT, Yang Y, Lum CT, Zou B, Zhu YB, Jiang SH, Wong WM, Chan AO, Yuen MF, Lam SK, Kung HF and Wong BC. Suppression of survivin expression inhibits in vivo tumorigenicity and angiogenesis in gastric cancer. Cancer Res. 2003; 63(22):7724-7732.
38. Blanc-Brude OP, Mesri M, Wall NR, Plescia J, Dohi T and Altieri DC. Therapeutic targeting of the survivin pathway in cancer: initiation of mitochondrial apoptosis and suppression of tumor-associated angiogenesis. Clin Cancer Res. 2003; 9(7):2683-2692.
39. Koukourakis MI, Giatromanolaki A, Thorpe PE, Brekken RA, Sivridis E, Kakolyris S, Georgoulias V, Gatter KC and Harris AL. Vascular endothelial growth factor/KDR activated microvessel density versus CD31 standard microvessel density in non-small cell lung cancer. Cancer Res. 2000; 60(11):3088-3095.
40. Qi R, Gu J, Zhang Z, Yang K, Li B, Fan J, Wang C, He Z, Qiao L, Lin Z and Liu XY. Potent antitumor efficacy of XAF1 delivered by conditionally replicative adenovirus vector via caspase-independent apoptosis. Cancer Gene Ther. 2007; 14(1):82-90.
41. Lunardi A, Ala U, Epping MT, Salmena L, Clohessy JG, Webster KA, Wang G, Mazzucchelli R, Bianconi M, Stack EC, Lis R, Patnaik A, Cantley LC, Bubley G, Cordon-Cardo C, Gerald WL, et al. A co-clinical approach identifies mechanisms and potential therapies for androgen deprivation resistance in prostate cancer. Nat Genet. 45(7):747-755.
42. Zhang F, Wu LM, Zhou L, Chen QX, Xie HY, Feng XW and Zheng SS. Predictive value of expression and promoter hypermethylation of XAF1 in hepatitis B virus-associated hepatocellular carcinoma treated with transplantation. Ann Surg Oncol. 2008; 15(12):3494-3502.
43. Shibata T, Mahotka C, Wethkamp N, Heikaus S, Gabbert HE and Ramp U. Disturbed expression of the apoptosis regulators XIAP, XAF1, and Smac/DIABLO in gastric adenocarcinomas. Diagn Mol Pathol. 2007; 16(1):1-8.
44. Yeh CN, Lee WC, Jeng LB, Chen MF and Yu MC. Spontaneous tumour rupture and prognosis in patients with hepatocellular carcinoma. Br J Surg. 2002; 89(9):1125-1129.
45. Leung DW, Cachianes G, Kuang WJ, Goeddel DV and Ferrara N. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science. 1989; 246(4935):1306-1309.
46. Ferrara N and Davis-Smyth T. The biology of vascular endothelial growth factor. Endocr Rev. 1997; 18(1):4-25.
47. Moeini A, Cornella H and Villanueva A. Emerging Signaling Pathways in Hepatocellular Carcinoma. Liver Cancer. 1(2):83-93.
48. Fisher WE and Berger DH. Angiogenesis and antiangiogenic strategies in pancreatic cancer. Int J Gastrointest Cancer. 2003; 33(1):79-88.
49. Folkman J. Antiangiogenic gene therapy. Proc Natl Acad Sci U S A. 1998; 95(16):9064-9066.
50. Rea D, Havenga MJ, van den Assem M, Sutmuller RP, Lemckert A, Hoeben RC, Bout A, Melief CJ and Offringa R. Highly efficient transduction of human monocyte-derived dendritic cells with subgroup B fiber-modified adenovirus vectors enhances transgene-encoded antigen presentation to cytotoxic T cells. The Journal of Immunology. 2001; 166(8):5236-5244.
51. Zhou H, Ou SY, Yan RA and Wu JZ. 1,2-Bis(4-nitro-benz-yl)diselane. Acta Crystallogr Sect E Struct Rep Online. 67(Pt 8):o1938.
52. Wang G, Li G, Liu H, Yang C, Yang X, Jin J, Liu X, Qian Q and Qian W. E1B 55 kDa deleted, Ad5/F35 fiber chimeric adenovirus, a potential oncolytic agent for B lymphocytic malignancies. The journal of gene medicine. 2009; 11(6):477-485.
53. Xiang D, Chen Z, Wang D, Li M, Xie J, Zhang Y, Qing Y, Li Z and Xie J. Chimeric adenoviral vector Ad5/F35-mediated APE1 siRNA enhances sensitivity of human colorectal cancer cells to radiotherapy in vitro and in vivo. Cancer gene therapy. 2008; 15(10):625-635.
54. Blagosklonny MV and El Deiry WS. Acute overexpression of wt p53 facilitates anticancer drug induced death of cancer and normal cells. International journal of cancer. 1998; 75(6):933-940.
55. Saturno G, Valenti M, Brandon ADH, Thomas GV, Eccles S, Clarke PA and Workman P. Combining TRAIL with PI3 kinase or HSP90 inhibitors enhances apoptosis in colorectal cancer cells via suppression of survival signaling. Oncotarget. 2013; 4(8):1185.
56. Gao G, Chen L, Li J, Zhang D, Fang Y, Huang H, Chen X and Huang C. Isorhapontigenin (ISO) inhibited cell transformation by inducing G0/G1 phase arrest via increasing MKP-1 mRNA Stability. Oncotarget. 2014.
57. Walsby E, Pratt G, Shao H, Abbas AY, Fischer PM, Bradshaw TD, Brennan P, Fegan C, Wang S and Pepper C. A novel Cdk9 inhibitor preferentially targets tumor cells and synergizes with fludarabine. Oncotarget. 2013; 4(9).