Inhibition of tumor angiogenesis by p53: a new role for the guardian of the genome (original) (raw)

References

1. Donehower LA, Harvey M, Slagle BL, McArthur MJ, Montgomery CA Jr, Butel JS, Bradley A (1992) Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 356:215–221
   Article PubMed CAS Google Scholar
2. Hollstein M, Sidransky D, Vogelstein B, Harris CC (1991) p53 mutations in human cancers. Science 253:49–53
   Article PubMed CAS Google Scholar
3. Greenblatt MS, Bennett WP, Hollstein M, Harris CC (1994) Mutations in the p53 tumor suppressor gene: clues to cancer etiology and molecular pathogenesis. Cancer Res 54:4855–4878
   PubMed CAS Google Scholar
4. Vousden KH, Lu X (2002) Live or let die: the cell’s response to p53. Nat Rev Cancer 2:594–604
   Article PubMed CAS Google Scholar
5. Ho J, Benchimol S (2003) Transcriptional repression mediated by the p53 tumour suppressor. Cell Death Differ 10:404–408
   Article PubMed CAS Google Scholar
6. Bergers G, Benjamin LE (2003) Tumorigenesis and the angiogenic switch. Nat Rev Cancer 3:401–410
   Article PubMed CAS Google Scholar
7. Folkman J, Long DM Jr, Becker FF (1963) Growth and metastasis of tumor in organ culture. Cancer 16:453–467
   Article PubMed CAS Google Scholar
8. Yu EY, Yu E, Meyer GE, Brawer MK (1997) The relation of p53 protein nuclear accumulation and angiogenesis in human prostatic carcinoma. Prostate Cancer Prostatic Dis 1:39–44
   Article PubMed Google Scholar
9. Takahashi Y, Bucana CD, Cleary KR, Ellis LM (1998) p53, vessel count, and vascular endothelial growth factor expression in human colon cancer. Int J Cancer 79:34–38
   Article PubMed CAS Google Scholar
10. Faviana P, Boldrini L, Spisni R, Berti P, Galleri D, Biondi R, Camacci T, Materazzi G, Pingitore R, Miccoli P, Fontanini G (2002) Neoangiogenesis in colon cancer: correlation between vascular density, vascular endothelial growth factor (VEGF) and p53 protein expression. Oncol Rep 9:617–620
    PubMed CAS Google Scholar
11. Kang SM, Maeda K, Onoda N, Chung YS, Nakata B, Nishiguchi Y, Sowa M (1997) Combined analysis of p53 and vascular endothelial growth factor expression in colorectal carcinoma for determination of tumor vascularity and liver metastasis. Int J Cancer 74:502–507
    Article PubMed CAS Google Scholar
12. Gasparini G, Weidner N, Maluta S, Pozza F, Boracchi P, Mezzetti M, Testolin A, Bevilacqua P (1993) Intratumoral microvessel density and p53 protein: correlation with metastasis in head-and-neck squamous-cell carcinoma. Int J Cancer 55:739–744
    Article PubMed CAS Google Scholar
13. Gasparini G, Weidner N, Bevilacqua P, Maluta S, Dalla Palma P, Caffo O, Barbareschi M, Boracchi P, Marubini E, Pozza F (1994) Tumor microvessel density, p53 expression, tumor size, and peritumoral lymphatic vessel invasion are relevant prognostic markers in node-negative breast carcinoma. J Clin Oncol 12:454–466
    PubMed CAS Google Scholar
14. Pugh CW, Ratcliffe PJ (2003) Regulation of angiogenesis by hypoxia: role of the HIF system. Nat Med 9:677–684
    Article PubMed CAS Google Scholar
15. Forsythe JA, Jiang BH, Iyer NV, Agani F, Leung SW, Koos RD, Semenza GL (1996) Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol 16:4604–4613
    PubMed CAS Google Scholar
16. Carmeliet P, Dor Y, Herbert JM, Fukumura D, Brusselmans K, Dewerchin M, Neeman M, Bono F, Abramovitch R, Maxwell P, Koch CJ, Ratcliffe P, Moons L, Jain RK, Collen D, Keshert E (1998) Role of HIF-1alpha in hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis. Nature 394:485–490
    Article PubMed CAS Google Scholar
17. Iyer NV, Kotch LE, Agani F, Leung SW, Laughner E, Wenger RH, Gassmann M, Gearhart JD, Lawler AM, Yu AY, Semenza GL (1998) Cellular and developmental control of O2 homeostasis by hypoxia-inducible factor 1 alpha. Genes Dev 12:149–162
    PubMed CAS Google Scholar
18. Ryan HE, Lo J, Johnson RS (1998) HIF-1 alpha is required for solid tumor formation and embryonic vascularization. EMBO J 17:3005–3015
    Article PubMed CAS Google Scholar
19. Jaakkola P, Mole DR, Tian YM, Wilson MI, Gielbert J, Gaskell SJ, Kriegsheim A, Hebestreit HF, Mukherji M, Schofield CJ, Maxwell PH, Pugh CW, Ratcliffe PJ (2001) Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 292:468–472
    PubMed CAS Google Scholar
20. Ivan M, Kondo K, Yang H, Kim W, Valiando J, Ohh M, Salic A, Asara JM, Lane WS, Kaelin WG Jr (2001) HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science 292:464–468
    PubMed CAS Google Scholar
21. Ravi R, Mookerjee B, Bhujwalla ZM, Sutter CH, Artemov D, Zeng Q, Dillehay LE, Madan A, Semenza GL, Bedi A (2000) Regulation of tumor angiogenesis by p53-induced degradation of hypoxia-inducible factor 1alpha. Genes Dev 14:34–44
    PubMed CAS Google Scholar
22. Rempe DA, Lelli KM, Vangeison G, Johnson RS, Federoff HJ (2007) In cultured astrocytes, p53 and MDM2 do not alter hypoxic HIF-1alpha function regardless of presence of DNA damage. J Biol Chem 282:16187–16201
    Article PubMed CAS Google Scholar
23. Kaluzova M, Kaluz S, Lerman MI, Stanbridge EJ (2004) DNA damage is a prerequisite for p53-mediated proteasomal degradation of HIF-1alpha in hypoxic cells and downregulation of the hypoxia marker carbonic anhydrase IX. Mol Cell Biol 24:5757–5766
    Article PubMed CAS Google Scholar
24. Pan Y, Oprysko PR, Asham AM, Koch CJ, Simon MC (2004) p53 cannot be induced by hypoxia alone but responds to the hypoxic microenvironment. Oncogene 23:4975–4983
    Article PubMed CAS Google Scholar
25. Pal S, Datta K, Mukhopadhyay D (2001) Central role of p53 on regulation of vascular permeability factor/vascular endothelial growth factor (VPF/VEGF) expression in mammary carcinoma. Cancer Res 61:6952–6957
    PubMed CAS Google Scholar
26. Ueba T, Nosaka T, Takahashi JA, Shibata F, Florkiewicz RZ, Vogelstein B, Oda Y, Kikuchi H, Hatanaka M (1994) Transcriptional regulation of basic fibroblast growth factor gene by p53 in human glioblastoma and hepatocellular carcinoma cells. Proc Natl Acad Sci USA 91:9009–9013
    Article PubMed CAS Google Scholar
27. Sherif ZA, Nakai S, Pirollo KF, Rait A, Chang EH (2001) Downmodulation of bFGF-binding protein expression following restoration of p53 function. Cancer Gene Ther 8:771–782
    Article PubMed CAS Google Scholar
28. Subbaramaiah K, Altorki N, Chung WJ, Mestre JR, Sampat A, Dannenberg AJ (1999) Inhibition of cyclooxygenase-2 gene expression by p53. J Biol Chem 274:10911–10915
    Article PubMed CAS Google Scholar
29. Tsujii M, Kawano S, Tsuji S, Sawaoka H, Hori M, DuBois RN (1998) Cyclooxygenase regulates angiogenesis induced by colon cancer cells. Cell 93:705–716
    Article PubMed CAS Google Scholar
30. Williams CS, Tsujii M, Reese J, Dey SK, DuBois RN (2000) Host cyclooxygenase-2 modulates carcinoma growth. J Clin Invest 105:1589–1594
    Article PubMed CAS Google Scholar
31. Masferrer JL, Leahy KM, Koki AT, Zweifel BS, Settle SL, Woerner BM, Edwards DA, Flickinger AG, Moore RJ, Seibert K (2000) Antiangiogenic and antitumor activities of cyclooxygenase-2 inhibitors. Cancer Res 60:1306–1311
    PubMed CAS Google Scholar
32. Iniguez MA, Rodriguez A, Volpert OV, Fresno M, Redondo JM (2003) Cyclooxygenase-2: a therapeutic target in angiogenesis. Trends Mol Med 9:73–78
    Article PubMed CAS Google Scholar
33. Koumenis C, Alarcon R, Hammond E, Sutphin P, Hoffman W, Murphy M, Derr J, Taya Y, Lowe SW, Kastan M, Giaccia A (2001) Regulation of p53 by hypoxia: dissociation of transcriptional repression and apoptosis from p53-dependent transactivation. Mol Cell Biol 21:1297–1310
    Article PubMed CAS Google Scholar
34. Dameron KM, Volpert OV, Tainsky MA, Bouck N (1994) Control of angiogenesis in fibroblasts by p53 regulation of thrombospondin-1. Science 265:1582–1584
    Article PubMed CAS Google Scholar
35. Good DJ, Polverini PJ, Rastinejad F, Le Beau MM, Lemons RS, Frazier WA, Bouck NP (1990) A tumor suppressor-dependent inhibitor of angiogenesis is immunologically and functionally indistinguishable from a fragment of thrombospondin. Proc Natl Acad Sci USA 87:6624–6628
    Article PubMed CAS Google Scholar
36. Tolsma SS, Volpert OV, Good DJ, Frazier WA, Polverini PJ, Bouck N (1993) Peptides derived from two separate domains of the matrix protein thrombospondin-1 have anti-angiogenic activity. J Cell Biol 122:497–511
    Article PubMed CAS Google Scholar
37. Weinstat-Saslow DL, Zabrenetzky VS, VanHoutte K, Frazier WA, Roberts DD, Steeg PS (1994) Transfection of thrombospondin 1 complementary DNA into a human breast carcinoma cell line reduces primary tumor growth, metastatic potential, and angiogenesis. Cancer Res 54:6504–6511
    PubMed CAS Google Scholar
38. Slack JL, Bornstein P (1994) Transformation by v-src causes transient induction followed by repression of mouse thrombospondin-1. Cell Growth Differ 5:1373–1380
    PubMed CAS Google Scholar
39. Tikhonenko AT, Black DJ, Linial ML (1996) Viral Myc oncoproteins in infected fibroblasts down-modulate thrombospondin-1, a possible tumor suppressor gene. J Biol Chem 271:30741–30747
    Article PubMed CAS Google Scholar
40. Janz A, Sevignani C, Kenyon K, Ngo CV, Thomas-Tikhonenko A (2000) Activation of the myc oncoprotein leads to increased turnover of thrombospondin-1 mRNA. Nucleic Acids Res 28:2268–2275
    Article PubMed CAS Google Scholar
41. Watnick RS, Cheng YN, Rangarajan A, Ince TA, Weinberg RA (2003) Ras modulates Myc activity to repress thrombospondin-1 expression and increase tumor angiogenesis. Cancer Cell 3:219–231
    Article PubMed CAS Google Scholar
42. Rak J, Mitsuhashi Y, Sheehan C, Tamir A, Viloria-Petit A, Filmus J, Mansour SJ, Ahn NG, Kerbel RS (2000) Oncogenes and tumor angiogenesis: differential modes of vascular endothelial growth factor up-regulation in ras-transformed epithelial cells and fibroblasts. Cancer Res 60:490–498
    PubMed CAS Google Scholar
43. Ren B, Yee KO, Lawler J, Khosravi-Far R (2006) Regulation of tumor angiogenesis by thrombospondin-1. Biochim Biophys Acta 1765:178–188
    PubMed CAS Google Scholar
44. Nor JE, Mitra RS, Sutorik MM, Mooney DJ, Castle VP, Polverini PJ (2000) Thrombospondin-1 induces endothelial cell apoptosis and inhibits angiogenesis by activating the caspase death pathway. J Vasc Res 37:209–218
    Article PubMed CAS Google Scholar
45. Jimenez B, Volpert OV, Crawford SE, Febbraio M, Silverstein RL, Bouck N (2000) Signals leading to apoptosis-dependent inhibition of neovascularization by thrombospondin-1. Nat Med 6:41–48
    Article PubMed CAS Google Scholar
46. Hsu SC, Volpert OV, Steck PA, Mikkelsen T, Polverini PJ, Rao S, Chou P, Bouck NP (1996) Inhibition of angiogenesis in human glioblastomas by chromosome 10 induction of thrombospondin-1. Cancer Res 56:5684–5691
    PubMed CAS Google Scholar
47. Dawson DW, Pearce SF, Zhong R, Silverstein RL, Frazier WA, Bouck NP (1997) CD36 mediates the In vitro inhibitory effects of thrombospondin-1 on endothelial cells. J Cell Biol 138:707–717
    Article PubMed CAS Google Scholar
48. Crawford SE, Stellmach V, Murphy-Ullrich JE, Ribeiro SM, Lawler J, Hynes RO, Boivin GP, Bouck N (1998) Thrombospondin-1 is a major activator of TGF-beta1 in vivo. Cell 93:1159–1170
    Article PubMed CAS Google Scholar
49. Derynck R, Akhurst RJ, Balmain A (2001) TGF-beta signaling in tumor suppression and cancer progression. Nat Genet 29:117–129
    Article PubMed CAS Google Scholar
50. Nishimori H, Shiratsuchi T, Urano T, Kimura Y, Kiyono K, Tatsumi K, Yoshida S, Ono M, Kuwano M, Nakamura Y, Tokino T (1997) A novel brain-specific p53-target gene, BAI1, containing thrombospondin type 1 repeats inhibits experimental angiogenesis. Oncogene 15:2145–2150
    Article PubMed CAS Google Scholar
51. Miao WM, Seng WL, Duquette M, Lawler P, Laus C, Lawler J (2001) Thrombospondin-1 type 1 repeat recombinant proteins inhibit tumor growth through transforming growth factor-beta-dependent and -independent mechanisms. Cancer Res 61:7830–7839
    PubMed CAS Google Scholar
52. Kaur B, Brat DJ, Devi NS, Van Meir EG (2005) Vasculostatin, a proteolytic fragment of brain angiogenesis inhibitor 1, is an antiangiogenic and antitumorigenic factor. Oncogene 24:3632–3642
    Article PubMed CAS Google Scholar
53. Van Meir EG, Polverini PJ, Chazin VR, Su Huang HJ, de Tribolet N, Cavenee WK (1994) Release of an inhibitor of angiogenesis upon induction of wild type p53 expression in glioblastoma cells. Nat Genet 8:171–176
    Article PubMed Google Scholar
54. Brantley DM, Cheng N, Thompson EJ, Lin Q, Brekken RA, Thorpe PE, Muraoka RS, Cerretti DP, Pozzi A, Jackson D, Lin C, Chen J (2002) Soluble Eph A receptors inhibit tumor angiogenesis and progression in vivo. Oncogene 21:7011–7026
    Article PubMed CAS Google Scholar
55. Dohn M, Jiang J, Chen X (2001) Receptor tyrosine kinase EphA2 is regulated by p53-family proteins and induces apoptosis. Oncogene 20:6503–6515
    Article PubMed CAS Google Scholar
56. Pasquale EB (2005) Eph receptor signalling casts a wide net on cell behaviour. Nat Rev Mol Cell Biol 6:462–475
    Article PubMed CAS Google Scholar
57. Dodelet VC, Pasquale EB (2000) Eph receptors and ephrin ligands: embryogenesis to tumorigenesis. Oncogene 19:5614–5619
    Article PubMed CAS Google Scholar
58. Zelinski DP, Zantek ND, Stewart JC, Irizarry AR, Kinch MS (2001) EphA2 overexpression causes tumorigenesis of mammary epithelial cells. Cancer Res 61:2301–2306
    PubMed CAS Google Scholar
59. Coffman KT, Hu M, Carles-Kinch K, Tice D, Donacki N, Munyon K, Kifle G, Woods R, Langermann S, Kiener PA, Kinch MS (2003) Differential EphA2 epitope display on normal versus malignant cells. Cancer Res 63:7907–7912
    PubMed CAS Google Scholar
60. Kinch MS, Carles-Kinch K (2003) Overexpression and functional alterations of the EphA2 tyrosine kinase in cancer. Clin Exp Metastasis 20:59–68
    Article PubMed CAS Google Scholar
61. Noblitt LW, Bangari DS, Shukla S, Knapp DW, Mohammed S, Kinch MS, Mittal SK (2004) Decreased tumorigenic potential of EphA2-overexpressing breast cancer cells following treatment with adenoviral vectors that express EphrinA1. Cancer Gene Ther 11:757–766
    Article PubMed CAS Google Scholar
62. Teodoro JG, Parker AE, Zhu X, Green MR (2006) p53-mediated inhibition of angiogenesis through up-regulation of a collagen prolyl hydroxylase. Science 313:968–971
    Article PubMed CAS Google Scholar
63. Prockop DJ, Kivirikko KI (1995) Collagens: molecular biology, diseases, and potentials for therapy. Annu Rev Biochem 64:403–434
    Article PubMed CAS Google Scholar
64. Nissi R, Autio-Harmainen H, Marttila P, Sormunen R, Kivirikko KI (2001) Prolyl 4-hydroxylase isoenzymes I and II have different expression patterns in several human tissues. J Histochem Cytochem 49:1143–1153
    PubMed CAS Google Scholar
65. Nissi R, Bohling T, Autio-Harmainen H (2004) Immunofluorescence localization of prolyl 4-hydroxylase isoenzymes and type I and II collagens in bone tumours: type I enzyme predominates in osteosarcomas and chondrosarcomas, whereas type II enzyme predominates in their benign counterparts. Acta Histochem 106:111–121
    Article PubMed CAS Google Scholar
66. Miled C, Pontoglio M, Garbay S, Yaniv M, Weitzman JB (2005) A genomic map of p53 binding sites identifies novel p53 targets involved in an apoptotic network. Cancer Res 65:5096–5104
    Article PubMed CAS Google Scholar
67. Wei CL, Wu Q, Vega VB, Chiu KP, Ng P, Zhang T, Shahab A, Yong HC, Fu Y, Weng Z, Liu J, Zhao XD, Chew JL, Lee YL, Kuznetsov VA, Sung WK, Miller LD, Lim B, Liu ET, Yu Q, Ng HH, Ruan Y (2006) A global map of p53 transcription-factor binding sites in the human genome. Cell 124:207–219
    Article PubMed CAS Google Scholar
68. Bian J, Sun Y (1997) Transcriptional activation by p53 of the human type IV collagenase (gelatinase A or matrix metalloproteinase 2) promoter. Mol Cell Biol 17:6330–6338
    PubMed CAS Google Scholar
69. Kalluri R (2003) Basement membranes: structure, assembly and role in tumour angiogenesis. Nat Rev Cancer 3:422–433
    Article PubMed CAS Google Scholar
70. Folkman J, Kalluri R (2004) Cancer without disease. Nature 427:787
    Article PubMed CAS Google Scholar
71. Sund M, Hamano Y, Sugimoto H, Sudhakar A, Soubasakos M, Yerramalla U, Benjamin LE, Lawler J, Kieran M, Shah A, Kalluri R (2005) Function of endogenous inhibitors of angiogenesis as endothelium-specific tumor suppressors. Proc Natl Acad Sci USA 102:2934–2939
    Article PubMed CAS Google Scholar
72. Zorick TS, Mustacchi Z, Bando SY, Zatz M, Moreira-Filho CA, Olsen B, Passos-Bueno MR (2001) High serum endostatin levels in Down syndrome: implications for improved treatment and prevention of solid tumours. Eur J Hum Genet 9:811–814
    PubMed CAS Google Scholar
73. Bond GL, Hu W, Bond EE, Robins H, Lutzker SG, Arva NC, Bargonetti J, Bartel F, Taubert H, Wuerl P, Onel K, Yip L, Hwang SJ, Strong LC, Lozano G, Levine AJ (2004) A single nucleotide polymorphism in the MDM2 promoter attenuates the p53 tumor suppressor pathway and accelerates tumor formation in humans. Cell 119:591–602
    Article PubMed CAS Google Scholar
74. Kaminski JM, Shinohara E, Summers JB, Niermann KJ, Morimoto A, Brousal J (2005) The controversial abscopal effect. Cancer Treat Rev 31:159–172
    Article PubMed CAS Google Scholar
75. Camphausen K, Moses MA, Menard C, Sproull M, Beecken WD, Folkman J, O’Reilly MS (2003) Radiation abscopal antitumor effect is mediated through p53. Cancer Res 63:1990–1993
    PubMed CAS Google Scholar
76. O’Reilly MS, Holmgren L, Shing Y, Chen C, Rosenthal RA, Moses M, Lane WS, Cao Y, Sage EH, Folkman J (1994) Angiostatin: a novel angiogenesis inhibitor that mediates the suppression of metastases by a Lewis lung carcinoma. Cell 79:315–328
    Article PubMed CAS Google Scholar
77. Sckell A, Safabakhsh N, Dellian M, Jain RK (1998) Primary tumor size-dependent inhibition of angiogenesis at a secondary site: an intravital microscopic study in mice. Cancer Res 58:5866–5869
    PubMed CAS Google Scholar
78. Prehn RT (1991) The inhibition of tumor growth by tumor mass. Cancer Res 51:2–4
    PubMed CAS Google Scholar
79. Hartford AC, Gohongi T, Fukumura D, Jain RK (2000) Irradiation of a primary tumor, unlike surgical removal, enhances angiogenesis suppression at a distal site: potential role of host–tumor interaction. Cancer Res 60:2128–2131
    PubMed CAS Google Scholar
80. Baker SJ, Preisinger AC, Jessup JM, Paraskeva C, Markowitz S, Willson JK, Hamilton S, Vogelstein B (1990) p53 gene mutations occur in combination with 17p allelic deletions as late events in colorectal tumorigenesis. Cancer Res 50:7717–7722
    PubMed CAS Google Scholar
81. Giuriato S, Ryeom S, Fan AC, Bachireddy P, Lynch RC, Rioth MJ, van Riggelen J, Kopelman AM, Passegue E, Tang F, Folkman J, Felsher DW (2006) Sustained regression of tumors upon MYC inactivation requires p53 or thrombospondin-1 to reverse the angiogenic switch. Proc Natl Acad Sci USA 103:16266–16271
    Article PubMed CAS Google Scholar
82. Holmgren L, Jackson G, Arbiser J (1998) p53 induces angiogenesis-restricted dormancy in a mouse fibrosarcoma. Oncogene 17:819–824
    Article PubMed CAS Google Scholar
83. Gautam A, Densmore CL, Melton S, Golunski E, Waldrep JC (2002) Aerosol delivery of PEI-p53 complexes inhibits B16-F10 lung metastases through regulation of angiogenesis. Cancer Gene Ther 9:28–36
    Article PubMed CAS Google Scholar
84. Black WC, Welch HG (1993) Advances in diagnostic imaging and overestimations of disease prevalence and the benefits of therapy. N Engl J Med 328:1237–1243
    Article PubMed CAS Google Scholar
85. Harach HR, Franssila KO, Wasenius VM (1985) Occult papillary carcinoma of the thyroid. A “normal” finding in Finland. A systematic autopsy study. Cancer 56:531–538
    Article PubMed CAS Google Scholar
86. Nielsen M, Thomsen JL, Primdahl S, Dyreborg U, Andersen JA (1987) Breast cancer and atypia among young and middle-aged women: a study of 110 medicolegal autopsies. Br J Cancer 56:814–819
    PubMed CAS Google Scholar
87. Paris F, Fuks Z, Kang A, Capodieci P, Juan G, Ehleiter D, Haimovitz-Friedman A, Cordon-Cardo C, Kolesnick R (2001) Endothelial apoptosis as the primary lesion initiating intestinal radiation damage in mice. Science 293:293–297
    Article PubMed CAS Google Scholar
88. Yu JL, Rak JW, Coomber BL, Hicklin DJ, Kerbel RS (2002) Effect of p53 status on tumor response to antiangiogenic therapy. Science 295:1526–1528
    Article PubMed CAS Google Scholar
89. Graeber TG, Peterson JF, Tsai M, Monica K, Fornace AJ Jr, Giaccia AJ (1994) Hypoxia induces accumulation of p53 protein, but activation of a G1-phase checkpoint by low-oxygen conditions is independent of p53 status. Mol Cell Biol 14:6264–6277
    PubMed CAS Google Scholar
90. Graeber TG, Osmanian C, Jacks T, Housman DE, Koch CJ, Lowe SW, Giaccia AJ (1996) Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumours. Nature 379:88–91
    Article PubMed CAS Google Scholar
91. Dameron KM, Volpert OV, Tainsky MA, Bouck N (1994) The p53 tumor suppressor gene inhibits angiogenesis by stimulating the production of thrombospondin. Cold Spring Harb Symp Quant Biol 59:483–489
    PubMed CAS Google Scholar
92. O’Reilly MS, Boehm T, Shing Y, Fukai N, Vasios G, Lane WS, Flynn E, Birkhead JR, Olsen BR, Folkman J (1997) Endostatin: an endogenous inhibitor of angiogenesis and tumor growth. Cell 88:277–285
    Article PubMed CAS Google Scholar
93. Ramchandran R, Dhanabal M, Volk R, Waterman MJ, Segal M, Lu H, Knebelmann B, Sukhatme VP (1999) Antiangiogenic activity of restin, NC10 domain of human collagen XV: comparison to endostatin. Biochem Biophys Res Commun 255:735–739
    Article PubMed CAS Google Scholar
94. Colorado PC, Torre A, Kamphaus G, Maeshima Y, Hopfer H, Takahashi K, Volk R, Zamborsky ED, Herman S, Sarkar PK, Ericksen MB, Dhanabal M, Simons M, Post M, Kufe DW, Weichselbaum RR, Sukhatme VP, Kalluri R (2000) Anti-angiogenic cues from vascular basement membrane collagen. Cancer Res 60:2520–2526
    PubMed CAS Google Scholar
95. Kamphaus GD, Colorado PC, Panka DJ, Hopfer H, Ramchandran R, Torre A, Maeshima Y, Mier JW, Sukhatme VP, Kalluri R (2000) Canstatin, a novel matrix-derived inhibitor of angiogenesis and tumor growth. J Biol Chem 275:1209–1215
    Article PubMed CAS Google Scholar
96. Maeshima Y, Colorado PC, Torre A, Holthaus KA, Grunkemeyer JA, Ericksen MB, Hopfer H, Xiao Y, Stillman IE, Kalluri R (2000) Distinct antitumor properties of a type IV collagen domain derived from basement membrane. J Biol Chem 275:21340–21348
    Article PubMed CAS Google Scholar
97. Petitclerc E, Boutaud A, Prestayko A, Xu J, Sado Y, Ninomiya Y, Sarras MP Jr., Hudson BG, Brooks PC (2000) New functions for non-collagenous domains of human collagen type IV. Novel integrin ligands inhibiting angiogenesis and tumor growth in vivo. J Biol Chem 275:8051–8061
    Article PubMed CAS Google Scholar
98. Xu R, Yao ZY, Xin L, Zhang Q, Li TP, Gan RB (2001) NC1 domain of human type VIII collagen (alpha 1) inhibits bovine aortic endothelial cell proliferation and causes cell apoptosis. Biochem Biophys Res Commun 289:264–268
    Article PubMed CAS Google Scholar

Download references