Expression of hypoxia-inducible factor 1α in brain tumors: Association with angiogenesis, invasion, and progression

Cancer

Volumn 88, Issue 11, 2000, Pages 2606-2618

  Zagzag, David ^a   Zhong, Hua ^b   Scalzitti, Joanne M ^c   Laughner, Erik ^d   Simons, Jonathan W ^b   Semenza, Gregg L ^d  

^a NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

^b JOHNS HOPKINS HOSPITAL   (United States)

^c UNIVERSITY OF NEBRASKA AT KEARNEY   (United States)

^d JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Angiogenesis; Glioblastoma multiforme; Glioma; Hemangioblastoma; HIF 1 ; HIF 1 ; Hypoxia

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA;

ANGIOGENESIS; ANIMAL CELL; ARTICLE; BRAIN TUMOR; CANCER GROWTH; CARCINOGENESIS; GLIOBLASTOMA; GLIOMA CELL; HEMANGIOBLASTOMA; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TISSUE OXYGENATION;

ANIMALS; BRAIN NEOPLASMS; DNA-BINDING PROTEINS; GLIOMA; HEMANGIOBLASTOMA; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MICE; NEOPLASM PROTEINS; NEOVASCULARIZATION, PATHOLOGIC; NUCLEAR PROTEINS; TRANSCRIPTION FACTORS; TUMOR CELLS, CULTURED;

EID: 0034213146     PISSN: 0008543X     EISSN: None     Source Type: Journal    
DOI: 10.1002/1097-0142(20000601)88:11<2606::AID-CNCR25>3.0.CO;2-W     Document Type: Article

References (65)

1. Folkman J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med 1995;1:27-31.
2. Yancopoulos GD, Klagsbrun M, Folkman J. Vasculogenesis, angiogenesis, and growth factors: ephrins enter the fray at the border. Cell 1998;93:661-4.
3. Shweiki D, Itin A, Soffer D, Keshet E. Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature 1992;359:843-5.
4. Wizigmann-Voos S, Breier G, Risau W, Plate KH. Up-regulation of vascular endothelial growth factor and its receptors in von Hippel-Lindau disease-associated and sporadic hemangioblastomas. Cancer Res 1995;55:1358-64.
5. Berkman RA, Merrill JM, Reinhold WC, Monacci WT, Saxena A, Clark WG, et al. Expression of the vascular permeability factor/vascular endothelial growth factor gene in central nervous system neoplasms. J Clin Invest 1993;91:153-9.
6. Senger DR, Galli SJ, Dvorak AM, Perruzzi CA, Harvey VS, Dvorak HF. Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science 1983;219:983-5.
7. 2 tension. Proc Natl Acad Sci USA 1995;92:5510-4.
8. Wang GL, Semenza GL. Purification and characterization of hypoxia-inducible factor 1. J Biol Chem 1995;270:1230-7.
9. 2 homeostasis by hypoxia-inducible factor 1α.. Genes Dev 1998; 12:149-62.
10. Hoffman BC, Reyes H, Chu FF, Sander F, Conley LH, Brooks BA, et al. Cloning of a factor required for activity of the Ah (dioxin) receptor. Science 1991;52:954-8.
11. Semenza GL, Jiang BH, Leung SW, Passantino R, Concordet J-P, Maire P, et al. Hypoxia response elements in the aldolase A, enolase 1, and lactate dehydrogenase A gene promoters contain essential binding sites for hypoxia-inducible factor1. J Biol Chem 1996;271:32529-37.
12. 2 tension. Am J Physiol 1996;271:C1172-80.
13. 2 homeostasis. Curr Opin Genet Dev 1998;8:588-94.
14. Tazuke SI, Mazure NM, Sugawara J, Carland G, Faessen GH, Suen LF, et al. Hypoxia stimulates insulin-like growth factor binding protein 1 (IGFBP-1) gene expression in HepG2 cells: a possible model for IGFBP-1 expression in fetal hypoxia. Proc Natl Acad Sci USA 1998;95:10188-93.
15. Feldser D, Agani F, Iyer NV, Pak B, Ferreira G, Semenza GL. Reciprocal positive regulation of hypoxia-inducible factor la and insulin-like growth factor 2. Cancer Res 1999;59: 3915-8.
16. Flamme I, Froehlich T, von Reutern M, Kappel A, Damert A, Risau W, et al. HRF, a putative basic helix-loop-helix-PAS-domain transcription factor is closely related to hypoxia-inducible factor-1α and developmentally expressed in blood vessels. Mech Dev 1997;63:51-60.
17. Ema M, Taya S, Yokotani N, Sogawa K, Matsuda Y, Fujii-Kuriyama Y, et al. A novel bHLH-PAS factor with close sequence similarity to hypoxia-inducible factor 1α regulates the VEGF expression, and is potentially involved in lung and vascular development. Proc Natl Acad Sci USA 1997;94:4273-8.
18. Tian H, McKnight SL, Russel DW. Endothelial PAS domain protein 1 (EPAS1), a transcription factor selectively expressed in endothelial cells. Genes Dev 1997;11:72-82.
19. Wenger RH, Gassmann M. Oxygen(es) and the hypoxia-inducible factor-1. Biol Chem 1997;378:609-16.
20. Damert A, Machein M, Breier G, Fujita MQ, Hanahan D, Risau W, et al. Up-regulation of vascular endothelial growth factor expression in a rat glioma is conferred by two distinct hypoxia-driven mechanisms. Cancer Res 1997;57:3860-4.
21. Flamme I, Krieg M, Plate KH. Up-regulation of vascular endothelial growth factor in stromal cells of hemangioblastomas is correlated with up-regulation of the transcription factor HRF/HIF-2α. Am J Pathol 1998;153:25-9.
22. Stratmann C, Krieg R, Haas M, Plate KH. Putative control of angiogenesis in hemangioblastomas by the von Hippel-Lindau tumor suppressor gene. J Neuropath Exp Neurol 1997;56:1242-52.
23. Krieg M, Marti HH, Plate KH. Coexpression of erythropoietin and vascular endothelial growth factor in nervous system tumors associated with von Hippel-Lindau tumor suppressor gene loss of function. Blood 1998;92:3388-93.
24. Kleihues P, Burger PC, Scheithauer BW. The new WHO classification of brain tumours. Brain Pathol 1993;3:255-68.
25. Zagzag D, Amirnovin R, Greco MA, Yee H, Holash J, Wiegand SJ, et al. Vascular apoptosis and involution in gliomas precede neovascularization: a novel concept for glioma growth and angiogenesis. Lab Invest 2000.
26. Akbasak A, Olderfield EH, Saris SC. Expression and modulation of major histocompatibility antigens on murine primary brain tumor in vitro. J Neurosurg 1991;75:922-9.
27. Zhong H, De Marzo AM, Laughner E, Lim M, Hilton DA, Zagzag D, et al. Overexpression of HIF-1 in common human cancers and their metastases. Cancer Res 1999;59:5830-5.
28. Zagzag D, Hooper A, Friedlander DR, Chan W, Holash J, Wiegand JJ, et al. In situ expression of angiopoietins in astrocytomas identifies angiopoietin-2 as an early marker of tumor angiogenesis. Exp Neurol 1999;159:391-400.
29. Brem S, Cotran R, Folkman J. Tumor angiogenesis: a quantitative method for histologic grading. J Natl Cancer Inst 1972;48:347-56.
30. Siegal S. Nonparametric statistics for the behavioral sciences. New York: Academic Press, 1997.
31. Zhong H, Agani F, Baccala AA, Laughner E, Rioseco-Camacho N, Isaacs WB, et al. Increased expression of hypoxia inducible factor-1α in rat and human prostate cancer. Cancer Res 1998;58:5280-4.
32. O'Shaughnessy J, Deseau V, Amini S, Rosen N, Bolen JB. Analysis of the c-src gene product structure, abundance, and protein kinase activity in human neuroblastoma and glioblastoma cells. Oncogene Res 1987;2:1-18.
33. Theurillat JP, Hainfellner J, Maddalena A, Weissenberger J, Aguzzi A. Early induction of angiogenetic signals in gliomas of GFAP-v-src transgenic mice. Am J Path 1999;154:581-90.
34. Jiang B-H, Agani F, Passaniti A, Semenza GL. V-SRC induces expression of hypoxia-inducible factor 1 (HIF-1) and transcription of genes encoding vascular endothelial growth factor and enolase 1: Involvement of HIF-1 in tumor progression. Cancer Res 1997;57:5328-35.
35. Agani F, Semenza GL. Mersalyl is a novel inducer of vascular endothelial growth factor gene expression and hypoxia-inducible factor 1 activity. Mol Pharmacol 1998;54:749-54.
36. Resnicoff M, Tjuvajev J, Rotman HL, Abraham D, Curtis M, Aiken R, et al. Regression of C6 rat brain tumors by cells expressing an antisense insulin-like growth factor 1 receptor RNA. J Exp Ther Oncol 1996;1:385-9.
37. Sandberg-Nordqvist AC, Stahlbom PA, Reinecke M, Collins VP, von Holst H, Sara V. Characterization of insulin-like growth factor 1 in human primary brain tumors. Cancer Res 1993;53:2475-8.
38. Huang LE, Arany Z, Livingston DM, Bunn HF. Activation of hypoxia-inducible transcription factor depends primarily upon redox-sensitive stabilization of its α subunit. J Biol Chem 1996;271:32253-9.
39. 2 gradients in solid tumors in vivo: high-resolution measurements reveal a lack of correlation. Nat Med 1997;3:177-82.
40. Kanno H, Kondo K, Ito S, Yamamoto I, Fujii S, Torigoes S, et al. Somatic mutations of the von Hippel-Lindau tumor suppressor gene in sporadic central nervous system hemangioblastomas. Cancer Res 1994;54:4845-7.
41. Tse JYM, Wong JHC, Lo K-W, Poon W-S, Huang DP, Ng HK. Molecular genetic analysis of the von Hippel-Lindau disease tumor suppressor gene in familial and sporadic cerebellar hemangioblastoma. Am J Clin Pathol 1997;107:459-66.
42. Vortmeyer AO, Gnarra JR, Emmert-Buck MR, Katz D, Linehan WM, Oldfield EH, et al. von Hippel-Lindau gene deletion detected in the stromal cell component of a cerebellar hemangioblastoma associated with von Hippel-Lindau disease. Hum Pathol 1997;28:540-3.
43. Lee JY, Dong SM, Park WS, Yoo NJ, Kin CS, Jang JJ, et al. Loss of heterozygosity and somatic mutations of the VHL tumor suppressor gene in sporadic cerebellar HBs. Cancer Res 1998;59:504-8.
44. Olschwang S, Richard S, Boisson C, Giraud S, Laurent-Puig P, Resche F, et al. Germline mutation profile of the VHL gene in von Hippel-Lindau disease and in sporadic hemangioblastoma. Hum Mutat 1998;12:424-30.
45. Maher ER, Kaelin WG Jr. Reviews in molecular medicine von Hippel-Lindau disease. Medicine 1997;76:381-91.
46. Ohh M, Kaelin WG Jr. The von Hippel-Lindau tumor suppressor protein: new perspectives. Mol Med Today 1999;5: 257-63.
47. Gnarra JR, Zhou S, Merrill MJ, Wagner JR, Krumm A, Paprassiliiou E, et al. Post-transcriptional regulation of vascular endothelial growth factor mRNA by the product of the VHL tumor suppressor gene. Proc Natl Acad Sci USA 1996; 93:10589-94.
48. Illiopoulos O, Levy AP, Jiang C, Kaelin WG Jr, Goldberg MA. Negative regulation of hypoxia-inducible genes by the von Hippel-Lindau protein. Proc Natl Acad Sci USA 1996;93: 10595-9.
49. Maxwell PH, Wiesener MS, Chang G-W, Clifford SC, Vaux EC, Cockman ME, et al. The tumor suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 1999;399:271-5.
50. Leung SY, Chan YSA, Wong PM, Yuen TS, Chung PL. Expression of vascular endothelial growth factor and its receptors in pilocytic astrocytoma. Am J Surg Pathol 1997;21:941-50.
51. Forsythe JA, Jiang B-H, Iyer NV, Agani F, Leung SW, Koos RD, et al. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol 1996;16:4604-13.
52. Maxwell PH, Dachs GU, Gleadle JM, Nicholls LG, Harris AL, Stratford IJ, et al. Hypoxia-inducible factor-1 modulates gene expression in solid tumors and influences both angiogenesis and tumor growth. Proc Natl Acad Sci USA 1997;94: 8104-9.
53. Ravi R, Mookerjee B, Bhujwalla ZM, Sutter CH, Artemov D, Zeng Q, et al. Regulation of tumor angiogenesis by p53-induced degradation of hypoxia-inducible factor 1α. Genes Dev 2000;14:34-44.
54. Levy AP, Levy NS, Goldberg MA. Post-transcriptional regulation of vascular endothelial growth factor by hypoxia. J Biol Chem 1996;271:2746-53.
55. Kalra VJ, Shen Y, Sultana C, Rattan V. Hypoxia induces PECAM-1 phosphorylation and transendothelial migration of monocytes. Am J Physiol 1996;271:2025-34.
56. Meininger CJ, Schelling ME, Granger HJ. Adenosine and hypoxia stimulate proliferation and migration of endothelial cells. Am J Physiol 1988;255:554-62.
57. Bar-Eli M. Role of interleukin-8 in tumor growth and metastasis of human melanoma. Pathobiology 1999;67:12-8.
58. Cuvier C, Jang A, Hill RP. Exposure to hypoxia, glucose starvation and acidosis: effect on invasive capacity of murine tumor cells and correlation with cathepsin(L + B) secretion. Clin Exp Metastasis 1997;15:19-25.
59. Fitzpatrick TE, Graham CH. Stimulation of plasminogen activator inhibitor-1 expression in immortalized human trophoblast cells cultured under low levels of oxygen. Exp Cell Res 1998;245:155-62.
60. Graham CH, Fitzpatrick TE, McCrae KR. Hypoxia stimulates urokinase receptor expression through a heme protein-dependent pathway. Blood 1998;91:3300-7.
61. Graham CH, Forsdike J, Fitzgerald CJ, Macdonald-Goodfellow S. Hypoxia-mediated stimulation of carcinoma cell invasiveness via upregulation of urokinase receptor expression. Int J Cancer 1999;80:617-23.
62. Mohan PM, Chintala SK, Mohanam S, Gladson CL, Kim ES, Gokaslan ZL, et al. Adenovirus-mediated delivery of antisense gene to urokinase-type plasminogen activator receptor suppresses glioma invasion and tumor growth. Cancer Res 1999;59:3369-73.
63. Arai Y, Kubota T, Nakagawa T, Kabuto M, Sato K, Kobayashi H. Production of urokinase-type plasminogen activator (u-PA) and plasminogen activator inhibitor-1 (PAI-1) in human brain tumours. Acta Neurochir 1998;140:377-86.
64. Kietzmann T, Roth U, Jungermann K. Induction of the plasminogen activator inhibitor-1 gene expression by mild hypoxia via a hypoxia response element binding the hypoxia-inducible factor-1 in rat hepatocytes. Blood 1999;94:4177-85.
65. Semenza GL. HIF-1: mediator of physiological and pathophysiological responses to hypoxia. J Appl Physiol 2000;88: 1474-80.