P14ARF inhibits human glioblastoma-induced angiogenesis by upregulating the expression of TIMP3

Journal of Clinical Investigation

Volumn 122, Issue 4, 2012, Pages 1283-1295

  Zerrouqi, Abdessamad ^a   Pyrzynska, Beata ^a,b   Febbraio, Maria ^c   Brat, Daniel J ^a,d   Van Meir, Erwin G ^a,d  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INTERNATIONAL INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Poland)

^c LERNER RESEARCH INSTITUTE   (United States)

^d EMORY UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 2A; PREGNANCY SPECIFIC BETA1 GLYCOPROTEIN; PROTEIN MDM2; PROTEIN P53; TISSUE INHIBITOR OF METALLOPROTEINASE 3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ARTICLE; CANCER CELL; CELL MIGRATION; CONTROLLED STUDY; ENDOTHELIUM CELL; GENE FUNCTION; GENE INTERACTION; GENETIC TRANSCRIPTION; GLIOBLASTOMA; HUMAN; HUMAN CELL; MOUSE; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR SUPPRESSOR GENE; UPREGULATION; VASCULAR DISEASE;

ANIMALS; BRAIN NEOPLASMS; CELL LINE, TRANSFORMED; CHEMOTAXIS; CORNEAL NEOVASCULARIZATION; CULTURE MEDIA, CONDITIONED; ENDOTHELIAL CELLS; FIBROBLASTS; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, P53; GLIOBLASTOMA; HUMANS; MICE; NEOPLASM PROTEINS; NEOVASCULARIZATION, PATHOLOGIC; PROTO-ONCOGENE PROTEINS C-MDM2; RECOMBINANT FUSION PROTEINS; RNA INTERFERENCE; RNA, SMALL INTERFERING; SP1 TRANSCRIPTION FACTOR; TISSUE INHIBITOR OF METALLOPROTEINASE-3; TRANSCRIPTION, GENETIC; TUMOR CELLS, CULTURED; TUMOR SUPPRESSOR PROTEIN P14ARF; UP-REGULATION;

EID: 84859733234     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI38596     Document Type: Article

References (67)

1. Sharpless NE. INK4a/ARF: a multifunctional tumor suppressor locus. Mutat Res. 2005;576(1-2):22-38. (Pubitemid 40982680)
2. Quelle DE, Zindy F, Ashmun RA, Sherr CJ. Alternative reading frames of the INK4a tumor suppressor gene encode two unrelated proteins capable of inducing cell cycle arrest. Cell. 1995;83(6):993-1000. (Pubitemid 26006540)
3. Pomerantz J, et al. The Ink4a tumor suppressor gene product, p19Arf, interacts with MDM2 and neutralizes MDM2's inhibition of p53. Cell. 1998;92(6):713-723. (Pubitemid 28155311)
4. Randerson-Moor JA, et al. A germline deletion of p14(ARF) but not CDKN2A in a melanoma-neural system tumour syndrome family. Hum Mol Genet. 2001;10(1):55-62. (Pubitemid 32051568)
5. Kamijo T, et al. Tumor suppression at the mouse INK4a locus mediated by the alternative reading frame product p19ARF. Cell. 1997;91(5):649-659. (Pubitemid 27513656)
6. Weber HO, Samuel T, Rauch P, Funk JO. Human p14(ARF)-mediated cell cycle arrest strictly depends on intact p53 signaling pathways. Oncogene. 2002;21(20):3207-3212. (Pubitemid 34548091)
7. Kelly-Spratt KS, Gurley KE, Yasui Y, Kemp CJ. p19Arf suppresses growth, progression, and metastasis of Hras-driven carcinomas through p53-dependent and -independent pathways. PLoS Biol. 2004;2(8):E242.
8. Kamijo T, et al. Loss of the ARF tumor suppressor reverses premature replicative arrest but not radiation hypersensitivity arising from disabled atm function. Cancer Res. 1999;59(10):2464-2469. (Pubitemid 29242298)
9. Kamijo T, Bodner S, van de Kamp E, Randle DH, Sherr CJ. Tumor spectrum in ARF-deficient mice. Cancer Res. 1999;59(9):2217-2222. (Pubitemid 29217688)
10. Radfar A, Unnikrishnan I, Lee HW, DePinho RA, Rosenberg N. p19(Arf) induces p53-dependent apoptosis during abelson virus-mediated pre-B cell transformation. Proc Natl Acad Sci U S A. 1998;95(22):13194-13199.
11. Ichimura K, Bolin MB, Goike HM, Schmidt EE, Moshref A, Collins VP. Deregulation of the p14ARF/MDM2/p53 pathway is a prerequisite for human astrocytic gliomas with G1-S transition control gene abnormalities. Cancer Res. 2000;60(2):417-424. (Pubitemid 30070771)
12. Weber JD, et al. p53-independent functions of the p19(ARF) tumor suppressor. Genes Dev. 2000;14(18):2358-2365.
13. Watanabe T, Katayama Y, Yoshino A, Komine C, Yokoyama T. Deregulation of the TP53/p14ARF tumor suppressor pathway in low-grade diffuse astrocytomas and its influence on clinical course. Clin Cancer Res. 2003;9(13):4884-4890. (Pubitemid 37323294)
14. Van Meir EG, Hadjipanayis CG, Norden AD, Shu HK, Wen PY, Olson JJ. Exciting new advances in neuro-oncology: the avenue to a cure for malignant glioma. CA Cancer J Clin. 2010;60(3):166-193.
15. Fulci G, et al. p53 gene mutation and ink4a-arf deletion appear to be two mutually exclusive events in human glioblastoma. Oncogene. 2000;19(33):3816- 3822. (Pubitemid 30621189)
16. Verhaak RG, et al. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell. 2010;17(1):98-110.
17. Brat DJ, Van Meir EG. Vaso-occlusive and prothrombotic mechanisms associated with tumor hypoxia, necrosis, and accelerated growth in glioblastoma. Lab Invest. 2004;84(4):397-405. (Pubitemid 41656467)
18. Kaur B, Brat DJ, Devi NS, Van Meir EG. Vasculostatin, a proteolytic fragment of brain angiogenesis inhibitor 1, is an antiangiogenic and antitumorigenic factor. Oncogene. 2005;24(22):3632-3642. (Pubitemid 40756232)
19. Kaur B, et al. Vasculostatin inhibits intracranial glioma growth and negatively regulates in vivo angiogenesis through a CD36-dependent mechanism. Cancer Res. 2009;69(3):1212-1220.
20. Groth A, Weber JD, Willumsen BM, Sherr CJ, Roussel MF. Oncogenic Ras induces p19ARF and growth arrest in mouse embryo fibroblasts lacking p21Cip1 and p27Kip1 without activating cyclin D-dependent kinases. J Biol Chem. 2000;275(35):27473-27480.
21. Birkedal-Hansen H, et al. Matrix metalloproteinases: a review. Crit Rev Oral Biol Med. 1993;4(2):197-250. (Pubitemid 23103292)
22. Van Meir EG, Polverini PJ, Chazin VR, Su Huang HJ, de Tribolet N, Cavenee WK. Release of an inhibitor of angiogenesis upon induction of wild type p53 expression in glioblastoma cells. Nat Genet. 1994;8(2):171-176. (Pubitemid 24308365)
23. Wick M, et al. Structure of the human TIMP-3 gene and its cell cycle-regulated promoter. Biochem J. 1995;311(pt 2):549-554.
24. Blume SW, Snyder RC, Ray R, Thomas S, Koller CA, Miller DM. Mithramycin inhibits SP1 binding and selectively inhibits transcriptional activity of the dihydrofolate reductase gene in vitro and in vivo. J Clin Invest. 1991;88(5):1613-1621.
25. Gualberto A, Baldwin AS Jr. p53 and Sp1 interact and cooperate in the tumor necrosis factor-induced transcriptional activation of the HIV-1 long terminal repeat. J Biol Chem. 1995;270(34):19680-19683.
26. Daujat S, Neel H, Piette J. MDM2: life without p53. Trends Genet. 2001;17(8):459-464. (Pubitemid 32727238)
27. Matheu A, et al. Increased gene dosage of Ink4a/Arf results in cancer resistance and normal aging. Genes Dev. 2004;18(22):2736-2746. (Pubitemid 39507767)
28. Serrano M. The INK4a/ARF locus in murine tumorigenesis. Carcinogenesis. 2000;21(5):865-869. (Pubitemid 30265127)
29. Folkman J. The role of angiogenesis in tumor growth. Semin Cancer Biol. 1992;3(2):65-71.
30. Yassini PR, Stickler DL, Bloomfield SM, Wiggins RC, Konat GW. Glioma-stimulated chemoattraction of endothelial cells and fibroblasts in vitro: a model for the study of glioma-induced angiogenesis. Metab Brain Dis. 1994;9(4):391-399.
31. Cornelius LA, Nehring LC, Roby JD, Parks WC, Welgus HG. Human dermal microvascular endothelial cells produce matrix metalloproteinases in response to angiogenic factors and migration. J Invest Dermatol. 1995;105(2):170-176.
32. van Hinsbergh VW, Koolwijk P. Endothelial sprouting and angiogenesis: matrix metalloproteinases in the lead. Cardiovasc Res. 2008;78(2):203-212. (Pubitemid 351556093)
33. Spurbeck WW, Ng CY, Strom TS, Vanin EF, Davidoff AM. Enforced expression of tissue inhibitor of matrix metalloproteinase-3 affects functional capillary morphogenesis and inhibits tumor growth in a murine tumor model. Blood. 2002;100(9):3361-3368. (Pubitemid 35217088)
34. Qi JH, et al. A novel function for tissue inhibitor of metalloproteinases-3 (TIMP3): inhibition of angiogenesis by blockage of VEGF binding to VEGF receptor-2. Nat Med. 2003;9(4):407-415. (Pubitemid 36460074)
35. Nakamura M, et al. Frequent LOH on 22q12.3 and TIMP-3 inactivation occur in the progression to secondary glioblastomas. Lab Invest. 2005;85(2):165-175. (Pubitemid 40208920)
36. Bachman KE, et al. Methylation-associated silencing of the tissue inhibitor of metalloproteinase-3 gene suggest a suppressor role in kidney, brain, and other human cancers. Cancer Res. 1999;59(4):798-802. (Pubitemid 29086729)
37. Mahller YY, et al. Tissue inhibitor of metalloproteinase-3 via oncolytic herpesvirus inhibits tumor growth and vascular progenitors. Cancer Res. 2008;68(4):1170-1179. (Pubitemid 351272236)
38. Eymin B, et al. Human ARF binds E2F1 and inhibits its transcriptional activity. Oncogene. 2001;20(9):1033-1041. (Pubitemid 32238852)
39. Eymin B, Leduc C, Coll JL, Brambilla E, Gazzeri S. p14ARF induces G2 arrest and apoptosis independently of p53 leading to regression of tumours established in nude mice. Oncogene. 2003;22(12):1822-1835. (Pubitemid 36513141)
40. Hemmati PG, et al. Adenovirus-mediated overexpression of p14(ARF) induces p53 and Bax-independent apoptosis. Oncogene. 2002;21(20):3149-3161. (Pubitemid 34548086)
41. Silva RL, et al. Arf-dependent regulation of Pdgf signaling in perivascular cells in the developing mouse eye. Embo J. 2005;24(15):2803-2814. (Pubitemid 41170029)
42. Gibson SL, et al. Inhibition of colon tumor progression and angiogenesis by the Ink4a/Arf locus. Cancer Res. 2003;63(4):742-746. (Pubitemid 36231968)
43. Kawagishi H, et al. ARF suppresses tumor angiogenesis through translational control of VEGFA mRNA. Cancer Res. 2010;70(11):4749-4758.
44. Rizos H, Woodruff S, Kefford RF. p14ARF interacts with the SUMO-conjugating enzyme Ubc9 and promotes the sumoylation of its binding partners. Cell Cycle. 2005;4(4):597-603. (Pubitemid 41359789)
45. Fatyol K, Szalay AA. The p14ARF tumor suppressor protein facilitates nucleolar sequestration of hypoxia-inducible factor-1alpha (HIF-1alpha) and inhibits HIF-1-mediated transcription. J Biol Chem. 2001;276(30):28421-28429.
46. Lee M, Song SU, Ryu JK, Suh JK. Sp1-dependent regulation of the tissue inhibitor of metalloproteinases-1 promoter. J Cell Biochem. 2004;91(6):1260- 1268.
47. Zhong ZD, Hammani K, Bae WS, DeClerck YA. NF-Y and Sp1 cooperate for the transcriptional activation and cAMP response of human tissue inhibitor of metalloproteinases-2. J Biol Chem. 2000;275(24):18602-18610.
48. Young DA, et al. Identification of an initiator-like element essential for the expression of the tissue inhibitor of metalloproteinases-4 (Timp-4) gene. Biochem J. 2002;364(pt 1):89-99. (Pubitemid 34538950)
49. Ahonen M, Baker AH, Kahari VM. Adenovirus-mediated gene delivery of tissue inhibitor of metalloproteinases-3 inhibits invasion and induces apoptosis in melanoma cells. Cancer Res. 1998;58(11):2310-2315. (Pubitemid 28252684)
50. Black AR, Black JD, Azizkhan-Clifford J. Sp1 and kruppel-like factor family of transcription factors in cell growth regulation and cancer. J Cell Physiol. 2001;188(2):143-160. (Pubitemid 32622905)
51. Borellini F, Glazer RI. Induction of Sp1-p53 DNA-binding heterocomplexes during granulocyte/macrophage colony-stimulating factor-dependent proliferation in human erythroleukemia cell line TF-1. J Biol Chem. 1993;268(11):7923-7928. (Pubitemid 23120371)
52. Stros M, Ozaki T, Bacikova A, Kageyama H, Nakagawara A. HMGB1 and HMGB2 cell-specifically down-regulate the p53- and p73-dependent sequence-specific transactivation from the human Bax gene promoter. J Biol Chem. 2002;277(9):7157-7164. (Pubitemid 34953105)
53. Mukhopadhyay D, Knebelmann B, Cohen HT, Ananth S, Sukhatme VP. The von Hippel-Lindau tumor suppressor gene product interacts with Sp1 to repress vascular endothelial growth factor promoter activity. Mol Cell Biol. 1997;17(9):5629-5639. (Pubitemid 27357659)
54. Johnson-Pais T, Degnin C, Thayer MJ. pRB induces Sp1 activity by relieving inhibition mediated by MDM2. Proc Natl Acad Sci U S A. 2001;98(5):2211-2216. (Pubitemid 32209461)
55. Udvadia AJ, et al. Sp-1 binds promoter elements regulated by the RB protein and Sp-1-mediated transcription is stimulated by RB coexpression. Proc Natl Acad Sci U S A. 1993;90(8):3265-3269. (Pubitemid 23111346)
56. Clark SJ, Harrison J, Molloy PL. Sp1 binding is inhibited by (m)Cp(m)CpG methylation. Gene. 1997;195(1):67-71. (Pubitemid 27336963)
57. Guo CS, Degnin C, Fiddler TA, Stauffer D, Thayer MJ. Regulation of MyoD activity and muscle cell differentiation by MDM2, pRb, and Sp1. J Biol Chem. 2003;278(25):22615-22622. (Pubitemid 36830319)
58. Bothner B, Lewis WS, DiGiammarino EL, Weber JD, Bothner SJ, Kriwacki RW. Defining the molecular basis of Arf and Hdm2 interactions. J Mol Biol. 2001;314(2):263-277. (Pubitemid 33105092)
59. Zhang Y, Xiong Y, Yarbrough WG. ARF promotes MDM2 degradation and stabilizes p53: ARF-INK4a locus deletion impairs both the Rb and p53 tumor suppression pathways. Cell. 1998;92(6):725-734. (Pubitemid 28155312)
60. Tao W, Levine AJ. P19(ARF) stabilizes p53 by blocking nucleo-cytoplasmic shuttling of Mdm2. Proc Natl Acad Sci U S A. 1999;96(12):6937-6941. (Pubitemid 29274988)
61. Kondo S, et al. The transforming activities of MDM2 in cultured neonatal rat astrocytes. Oncogene. 1996;13(8):1773-1779. (Pubitemid 26377510)
62. Ishii N, et al. Frequent co-alterations of TP53, p16/CDKN2A, p14ARF, PTEN tumor suppressor genes in human glioma cell lines. Brain Pathol. 1999;9(3):469-479. (Pubitemid 29316287)
63. Albertoni M, et al. Anoxia induces macrophage inhibitory cytokine-1 (MIC-1) in glioblastoma cells independently of p53 and HIF-1. Oncogene. 2002;21(27):4212-4219. (Pubitemid 34753827)
64. Tan C, et al. Identification of a novel small-molecule inhibitor of the hypoxia-inducible factor 1 pathway. Cancer Res. 2005;65(2):605-612.
65. Kenyon BM, Voest EE, Chen CC, Flynn E, Folkman J, D'Amato RJ. A model of angiogenesis in the mouse cornea. Invest Ophthalmol Vis Sci. 1996;37(8):1625-1632. (Pubitemid 26271414)
66. Zeng Y, Rosborough RC, Li Y, Gupta AR, Bennett J. Temporal and spatial regulation of gene expression mediated by the promoter for the human tissue inhibitor of metalloproteinases-3 (TIMP-3)-encoding gene. Dev Dyn. 1998;211(3):228-237. (Pubitemid 28150606)
67. Kadonaga JT, Courey AJ, Ladika J, Tjian R. Distinct regions of Sp1 modulate DNA binding and transcriptional activation. Science. 1988;242(4885):1566-1570.