Role of hypoxia-inducible factor 1α in gastric cancer cell growth, angiogenesis, and vessel maturation

Journal of the National Cancer Institute

Volumn 96, Issue 12, 2004, Pages 946-956

  Stoeltzing, Oliver ^a   McCarty, Marya F ^a   Wey, Jane S ^a   Fan, Fan ^a   Liu, Wenbiao ^a   Belcheva, Anna ^a   Bucana, Corazon D ^a   Semenza, Gregg L ^b   Ellis, Lee M ^a  

^a UNIVERSITY OF TEXAS   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

DESMIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 1BETA; PROTEIN SUBUNIT; UNCLASSIFIED DRUG; VASCULOTROPIN; ARNT PROTEIN, HUMAN; ARNT PROTEIN, MOUSE; AROMATIC HYDROCARBON RECEPTOR; DNA BINDING PROTEIN; HIF1A PROTEIN, HUMAN; TRANSCRIPTION FACTOR; VASCULOTROPIN A;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL CULTURE; CANCER GROWTH; CELL CULTURE; CELL HYPOXIA; CELL PROLIFERATION; CELL SECRETION; COMPLEX FORMATION; CONTROLLED STUDY; DIMERIZATION; DOMINANT GENE; ENDOTHELIUM CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; EXPRESSION VECTOR; GENE ACTIVITY; GENE REPRESSION; GENETIC CODE; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MALE; MOLECULAR CLONING; MOUSE; NONHUMAN; ORTHOTOPIC TRANSPLANTATION; PERICYTE; PLASMID; PRIORITY JOURNAL; PROTEIN SECRETION; STOMACH CANCER; SUBCUTANEOUS TISSUE TUMOR; TRANSCRIPTION INITIATION; TUMOR MODEL; TUMOR VOLUME; VASCULARIZATION; WEIGHT; ANIMAL; APOPTOSIS; CELL DIVISION; DRUG ANTAGONISM; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MUTATION; NEOVASCULARIZATION (PATHOLOGY); NUDE MOUSE; RANDOMIZATION; STOMACH TUMOR; TUMOR CELL LINE; UPREGULATION; WESTERN BLOTTING; XENOGRAFT;

ANIMALS; APOPTOSIS; ARYL HYDROCARBON RECEPTOR NUCLEAR TRANSLOCATOR; BLOTTING, WESTERN; CELL DIVISION; CELL LINE, TUMOR; DNA-BINDING PROTEINS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MICE; MICE, NUDE; MUTATION; NEOVASCULARIZATION, PATHOLOGIC; RANDOM ALLOCATION; RECEPTORS, ARYL HYDROCARBON; STOMACH NEOPLASMS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSFECTION; TRANSPLANTATION, HETEROLOGOUS; UP-REGULATION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 2942685341     PISSN: 00278874     EISSN: None     Source Type: Journal    
DOI: 10.1093/jnci/djh168     Document Type: Article

References (63)

1. Reinmuth N, Parikh AA, Ahmad SA, Liu W, Stoeltzing O, Fan F, et al. Biology of angiogenesis in tumors of the gastrointestinal tract. Microsc Res Tech 2003;60:199-207.
2. Folkman J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med 1995;1:27-31.
3. Fidler IJ, Ellis LM. The implications of angiogenesis for the biology and therapy of cancer metastasis. Cell 1994;79:185-8.
4. Leung DW, Cachianes G, Kuang WJ, Goeddel DV, Ferrara N. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 1989; 246:1306-9.
5. Kondo Y, Arii S, Mori A, Furutani M, Chiba T, Imamura M. Enhancement of angiogenesis, tumor growth, and metastasis by transfection of vascular endothelial growth factor into LoVo human colon cancer cell line. Clin Cancer Res 2000;6:622-30.
6. Maeda K, Chung YS, Ogawa Y, Takatsuka S, Kang SM, Ogawa M, et al. Prognostic value of vascular endothelial growth factor expression in gastric carcinoma. Cancer 1996;77:858-63.
7. Takahashi Y, Cleary KR, Mai M, Kitadai Y, Bucana CD, Ellis LM. Significance of vessel count and vascular endothelial growth factor and its receptor (KDR) in intestinal-type gastric cancer. Clin Cancer Res 1996;2: 1679-84.
8. Yamamoto S, Yasui W, Kitadai Y, Yokozaki H, Haruma K, Kajiyama G, et al. Expression of vascular endothelial growth factor in human gastric carcinomas. Pathol Int 1998;48:499-506.
9. Saito H, Tsujitani S, Kondo A, Ikeguchi M, Maeta M, Kaibara N. Expression of vascular endothelial growth factor correlates with hematogenous recurrence in gastric carcinoma. Surgery 1999;125:195-201.
10. Kido S, Kitadai Y, Hattori N, Haruma K, Kido T, Ohta M, et al. Interleukin 8 and vascular endothelial growth factor-prognostic factors in human gastric carcinomas? Eur J Cancer 2001;37:1482-7.
11. Cascinu S, Staccioli MP, Gasparini G, Giordani P, Catalano V, Ghiselli R, et al. Expression of vascular endothelial growth factor can predict event-free survival in stage II colon cancer. Clin Cancer Res 2000;6:2803-7.
12. Niedergethmann M, Hildenbrand R, Wostbrock B, Hartel M, Sturm JW, Richter A, et al. High expression of vascular endothelial growth factor predicts early recurrence and poor prognosis after curative resection for ductal adenocarcinoma of the pancreas. Pancreas 2002;25:122-9.
13. Ellis LM, Takahashi Y, Liu W, Shaheen RM. Vascular endothelial growth factor in human colon cancer: biology and therapeutic implications. Oncologist 2000;5 Suppl 1:11-5.
14. Semenza GL. HIF-1: mediator of physiological and pathophysiological responses to hypoxia. J Appl Physiol 2000;88:1474-80.
15. Forsythe JA, Jiang BH, 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.
16. Fang J, Yan L, Shing Y, Moses MA. HIF-1 alpha-mediated up-regulation of vascular endothelial growth factor, independent of basic fibroblast growth factor, is important in the switch to the angiogenic phenotype during early tumorigenesis. Cancer Res 2001;61:5731-5.
17. Semenza GL. Targeting HIF-1 for cancer therapy. Nat Rev Cancer 2003; 3:721-32.
18. Birner P, Gatterbauer B, Oberhuber G, Schindl M, Rossler K, Prodinger A, et al. Expression of hypoxia-inducible factor-1 alpha in oligodendrogliomas: its impact on prognosis and on neoangiogenesis. Cancer 2001;92: 165-71.
19. Birner P, Schindl M, Obermair A, Breitenecker G, Oberhuber G. Expression of hypoxia-inducible factor 1alpha in epithelial ovarian tumors: its impact on prognosis and on response to chemotherapy. Clin Cancer Res 2001;7:1661-8.
20. Bos R, Zhong H, Hanrahan CF, Mommers EC, Semenza GL, Pinedo HM, et al. Levels of hypoxia-inducible factor-1 alpha during breast carcinogenesis. J Natl Cancer Inst 2001;93:309-14.
21. Zagzag D, Zhong H, Scalzitti JM, Laughner E, Simons JW, Semenza GL. Expression of hypoxia-inducible factor 1alpha in brain tumors: association with angiogenesis, invasion, and progression. Cancer 2000;88:2606-18.
22. Zhong H, De Marzo AM, Laughner E, Lim M, Hilton DA, Zagzag D, et al. Overexpression of hypoxia-inducible factor 1alpha in common human cancers and their metastases. Cancer Res 1999;59:5830-5.
23. Talks KL, Turley H, Gatter KC, Maxwell PH, Pugh CW, Ratcliffe PJ, et al. The expression and distribution of the hypoxia-inducible factors HIF-1alpha and HIF-2alpha in normal human tissues, cancers, and tumor-associated macrophages. Am J Pathol 2000;157:411-21.
24. Iyer NV, Kotch LE, Agani F, Leung SW, Laughter E, Wenger RH, et al. Cellular and developmental control of O2 homeostasis by hypoxia-inducible factor 1 alpha. Genes Dev 1998;12:149-62.
25. Semenza GL. Surviving ischemia: adaptive responses mediated by hypoxia-inducible factor 1. J Clin Invest 2000;106:809-12.
26. Jiang BH, Semenza GL, Bauer C, Marti HH. Hypoxia-inducible factor 1 levels vary exponentially over a physiologically relevant range of O2 tension. Am J Physiol 1996;271:C1172-80.
27. Helmlinger G, Yuan F, Dellian M, Jain RK. Interstitial pH and pO2 gradients in solid tumors in vivo: high-resolution measurements reveal a lack of correlation. Nat Med 1997;3:177-82.
28. Wang GL, Jiang BH, Rue EA, Semenza GL. Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc Natl Acad Sci U S A 1995;92:5510-4.
29. Feldser D, Agani F, Iyer NV, Pak B, Ferreira G, Semenza GL. Reciprocal positive regulation of hypoxia-inducible factor 1alpha and insulin-like growth factor 2. Cancer Res 1999;59:3915-8.
30. Semenza GL. Regulation of mammalian O2 homeostasis by hypoxia-inducible factor 1. Annu Rev Cell Dev Biol 1999;15:551-78.
31. Elson DA, Ryan HE, Snow JW, Johnson R, Arbeit JM. Coordinate up-regulation of hypoxia inducible factor (HIF)-1alpha and HIF-1 target genes during multi-stage epidermal carcinogenesis and wound healing. Cancer Res 2000;60:6189-95.
32. Chen C, Pore N, Behrooz A, Ismail-Beigi F, Maity A. Regulation of glut1 mRNA by hypoxia-inducible factor-1. Interaction between H-ras and hypoxia. J Biol Chem 2001;276:9519-25.
33. Jiang BH, 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.
34. Laughner E, Taghavi P, Chiles K, Mahon PC, Semenza GL. HER2 (neu) signaling increases the rate of hypoxia-inducible factor 1alpha (HIF-1alpha) synthesis: novel mechanism for HIF-1-mediated vascular endothelial growth factor expression. Mol Cell Biol 2001;21:3995-4004.
35. Mazure NM, Chen EY, Laderoute KR, Giaccia AJ. Induction of vascular endothelial growth factor by hypoxia is modulated by a phosphatidylinositol 3-kinase/Akt signaling pathway in Ha-ras-transformed cells through a hypoxia inducible factor-1 transcriptional element. Blood 1997;90:3322-31.
36. Fukuda R, Hirota K, Fan F, Jung YD, Ellis LM, Semenza GL. Insulin-like growth factor 1 induces hypoxia-inducible factor 1-mediated vascular endothelial growth factor expression, which is dependent on MAP kinase and phosphatidylinositol 3-kinase signaling in colon cancer cells. J Biol Chem 2002;277:38205-11.
37. Krishnamachary B, Berg-Dixon S, Kelly B, Agani F, Feldser D, Ferreira G, et al. Regulation of colon carcinoma cell invasion by hypoxia-inducible factor 1. Cancer Res 2003;63:1138-43.
38. Carmeliet P, Dor Y, Herbert JM, Fukumura D, Brusselmans K, Dewerchin M, et al. Role of HIF-1alpha in hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis. Nature 1998;394:485-90.
39. Tsuzuki Y, Fukumura D, Oosthuyse B, Koike C, Carmeliet P, Jain RK. Vascular endothelial growth factor (VEGF) modulation by targeting hypoxia-inducible factor-1alpha→ hypoxia response element→ VEGF cascade differentially regulates vascular response and growth rate in tumors. Cancer Res 2000;60:6248-52.
40. Ryan HE, Poloni M, McNulty W, Elson D, Gassmann M, Arbeit JM, et al. Hypoxia-inducible factor-1alpha is a positive factor in solid tumor growth. Cancer Res 2000;60:4010-5.
41. Kung AL, Wang S, Klco JM, Kaelin WG, Livingston DM. Suppression of tumor growth through disruption of hypoxia-inducible transcription. Nat Med 2000;6:1335-40.
42. Chen J, Zhao S, Nakada K, Kuge Y, Tamaki N, Okada F, et al. Dominant-negative hypoxia-inducible factor-1alpha reduces tumorigenicity of pancreatic cancer cells through the suppression of glucose metabolism. Am J Pathol 2003;162:1283-91.
43. Blouw B, Song H, Tihan T, Bosze J, Ferrara N, Gerber HP, et al. The hypoxic response of tumors is dependent on their microenvironment. Cancer Cell 2003;4:133-46.
44. Jiang BH, Rue E, Wang GL, Roe R, Semenza GL. Dimerization, DNA binding, and transactivation properties of hypoxia-inducible factor 1. J Biol Chem 1996;271:17771-8.
45. Jung YD, Fan F, McConkey DJ, Jean ME, Liu W, Reinmuth N, et al. Role of P38 MAPK, AP-1, and NF-kappaB in interleukin-1beta-induced IL-8 expression in human vascular smooth muscle cells. Cytokine 2002;18:206-13.
46. Reinmuth N, Fan F, Liu W, Parikh AA. Stoeltzing O, Jung YD, et al. Impact of insulin-like growth factor receptor-I function on angiogenesis, growth, and metastasis of colon cancer. Lab Invest 2002;82:1377-89.
47. Stoeltzing O, Ahmad SA, Liu W, McCarty MF, Parikh AA, Fan F, et al. Angiopoietin-1 inhibits tumour growth and ascites formation in a murine model of peritoneal carcinomatosis. Br J Cancer 2002;87:1182-7.
48. Morikawa S, Baluk P, Kaidoh T, Haskell A, Jain RK, McDonald DM. Abnormalities in pericytes on blood vessels and endothelial sprouts in tumors. Am J Pathol 2002;160:985-1000.
49. Stoeltzing O, Ahmad SA, Liu W, McCarty MF, Wey JS, Parikh AA, et al. Angiopoietin-1 inhibits vascular permeability, angiogenesis, and growth of hepatic colon cancer tumors. Cancer Res 2003;63:3370-7.
50. Benjamin LE, Hemo I, Keshet E. A plasticity window for blood vessel remodelling is defined by pericyte coverage of the preformed endothelial network and is regulated by PDGF-B and VEGF. Development 1998;125: 1591-8.
51. Abramsson A, Berlin O, Papayan H, Paulin D, Shani M, Betsholtz C. Analysis of mural cell recruitment to tumor vessels. Circulation 2002;105: 112-7.
52. Gerhardt H, Betsholtz C. Endothelial-pericyte interactions in angiogenesis. Cell Tissue Res 2003;314:15-23.
53. Hellstrom N, Kalen M, Lindahl P, Abramsson A, Betsholtz C. Role of PDGF-B and PDGFR-beta in recruitment of vascular smooth muscle cells and pericytes during embryonic blood vessel formation in the mouse. Development 1999;126:3047-55.
54. 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 U S A 1997;94:8104-9.
55. Oh H, Takagi H, Suzuma K, Otani A, Matsumura M, Honda Y. Hypoxia and vascular endothelial growth factor selectively up-regulate angiopoietin-2 in bovine microvascular endothelial cells. J Biol Chem 1999;274:15732-9.
56. Maisonpierre PC, Suri C, Jones PF, Bartunkova S, Wiegand SJ, Radziejewski C, et al. Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis. Science 1997;277:55-60.
57. Zhang L, Yang N, Park JW, Katsaros D, Fracchioli S, Cao G, et al. Tumor-derived vascular endothelial growth factor up-regulates angiopoietin-2 in host endothelium and destabilizes host vasculature, supporting angiogenesis in ovarian cancer. Cancer Res 2003;63:3403-12.
58. Guo P, Hu B, Gu W, Xu L, Wang D, Huang HJ, et al. Platelet-derived growth factor-B enhances glioma angiogenesis by stimulating vascular endothelial growth factor expression in tumor endothelia and by promoting pericyte recruitment. Am J Pathol 2003;162:1083-93.
59. Reinmuth N, Liu W, Jung YD, Ahmad SA, Shaheen RM, Fan F, et al. Induction of VEGF in perivascular cells defines a potential paracrine mechanism for endothelial cell survival. FASEB J 2001;15:1239-41.
60. Semenza GL. Involvement of hypoxia-inducible factor 1 in human cancer. Intern Med 2002;41:79-83.
61. Ryan HE, Lo J, Johnson RS. HIF-1 alpha is required for solid tumor formation and embryonic vascularization. EMBO J 1998;17:3005-15.
62. Mabjeesh NJ, Escuin D, LaVallee TM, Pribluda VS, Swartz GM, Johnson MS, et al. 2ME2 inhibits tumor growth and angiogenesis by disrupting microtubules and dysregulating HIF. Cancer Cell 2003;3:363-75.
63. Yeo EJ, Chun YS, Cho YS, Kim J, Lee JC, Kim MS, et al. YC-1: a potential anticancer drug targeting hypoxia-inducible factor 1. J Natl Cancer Inst 2003;95:516-25.