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Regular Articles |
and HIF-2 in Normal Human Tissues, Cancers, and Tumor-Associated Macrophages
From the Nuffield Department of Clinical Laboratory
Sciences,*
University of Oxford, Oxford; the Wellcome Trust
Centre for Human Genetics,
Headington, Oxford;
and the Imperial Cancer Research Fund Molecular Oncology
Laboratory and Angiogenesis Group,
Institute
of Molecular Medicine, John Radcliffe Hospital, Oxford, United Kingdom
The cellular response to hypoxia includes the hypoxia-inducible
factor-1 (HIF-1)-induced transcription of genes involved in diverse
processes such as glycolysis and angiogenesis. Induction of the
HIF-regulated genes, as a consequence of the microenvironment
or genetic changes, is known to have an important role in the
growth of experimental tumors. Hypoxia-inducible factors 1
and 2
(HIF-1 and HIF-2) are known to dimerize with the aryl hydrocarbon
receptor nuclear translocator in mediating this response. Because
regulation of the chain protein level is a primary determinant of
HIF activity, our aim was to investigate the distribution of
HIF-1 and HIF-2 by immunohistochemistry in normal and
pathological tissues using monoclonal antibodies (mAb). We raised a new
mAb to detect HIF-1, designated 122, and used our
previously validated mAb 190b to HIF-2. In the majority of solid
tumors examined, including bladder, brain,
breast, colon, ovarian, pancreatic,
prostate, and renal carcinomas, nuclear expression of
HIF-1 and -2 was observed in varying subsets of the tumor cells.
HIF-2 was also strongly expressed by subsets of tumor-associated
macrophages, sometimes in the absence of any tumor cell
expression. Less frequently staining was observed in other stromal
cells within the tumors and in normal tissue adjacent to tumor margins.
In contrast, in normal tissue neither molecule was detectable
except within subsets of bone marrow macrophages, where
HIF-2 was strongly expressed.
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C. Lewis and C. Murdoch Macrophage Responses to Hypoxia: Implications for Tumor Progression and Anti-Cancer Therapies Am. J. Pathol., September 1, 2005; 167(3): 627 - 635. [Abstract] [Full Text] [PDF]
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P J van Diest, M M Vleugel, E van der Wall, M J Currie, V Hanrahan, S P Gunningham, H R Morrin, C Frampton, C Han, B A Robinson, et al. Expression of HIF-1{alpha} in human tumours J. Clin. Pathol., March 1, 2005; 58(3): 335 - 336. [Full Text] [PDF]
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S. McMahon, F. Grondin, P. P. McDonald, D. E. Richard, and C. M. Dubois Hypoxia-enhanced Expression of the Proprotein Convertase Furin Is Mediated by Hypoxia-inducible Factor-1: IMPACT ON THE BIOACTIVATION OF PROPROTEINS J. Biol. Chem., February 25, 2005; 280(8): 6561 - 6569. [Abstract] [Full Text] [PDF]
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S. R. Walmsley, C. Print, N. Farahi, C. Peyssonnaux, R. S. Johnson, T. Cramer, A. Sobolewski, A. M. Condliffe, A. S. Cowburn, N. Johnson, et al. Hypoxia-induced neutrophil survival is mediated by HIF-1{alpha}-dependent NF-{kappa}B activity J. Exp. Med., January 3, 2005; 201(1): 105 - 115. [Abstract] [Full Text] [PDF]
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 L. K. Kairaitis, Y. Wang, M. Gassmann, Y.-C. Tay, and D. C. H. Harris HIF-1{alpha} expression follows microvascular loss in advanced murine adriamycin nephrosis Am J Physiol Renal Physiol, January 1, 2005; 288(1): F198 - F206. [Abstract] [Full Text] [PDF]
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G. J. Hutchison, H. R. Valentine, J. A. Loncaster, S. E. Davidson, R. D. Hunter, S. A. Roberts, A. L. Harris, I. J. Stratford, P. M. Price, and C. M. L. West Hypoxia-Inducible Factor 1{alpha} Expression as an Intrinsic Marker of Hypoxia: Correlation with Tumor Oxygen, Pimonidazole Measurements, and Outcome in Locally Advanced Carcinoma of the Cervix Clin. Cancer Res., December 15, 2004; 10(24): 8405 - 8412. [Abstract] [Full Text] [PDF]
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H. Yoshimura, D. K. Dhar, H. Kohno, H. Kubota, T. Fujii, S. Ueda, S. Kinugasa, M. Tachibana, and N. Nagasue Prognostic Impact of Hypoxia-Inducible Factors 1{alpha} and 2{alpha} in Colorectal Cancer Patients: Correlation with Tumor Angiogenesis and Cyclooxygenase-2 Expression Clin. Cancer Res., December 15, 2004; 10(24): 8554 - 8560. [Abstract] [Full Text] [PDF]
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S. B. Fox, J. Braganca, H. Turley, L. Campo, C. Han, K. C. Gatter, S. Bhattacharya, and A. L. Harris CITED4 Inhibits Hypoxia-Activated Transcription in Cancer Cells, and Its Cytoplasmic Location in Breast Cancer Is Associated with Elevated Expression of Tumor Cell Hypoxia-Inducible Factor 1{alpha} Cancer Res., September 1, 2004; 64(17): 6075 - 6081. [Abstract] [Full Text] [PDF]
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M J Currie, V Hanrahan, S P Gunningham, H R Morrin, C Frampton, C Han, B A Robinson, and S B Fox Expression of vascular endothelial growth factor D is associated with hypoxia inducible factor (HIF-1{alpha}) and the HIF-1{alpha} target gene DEC1, but not lymph node metastasis in primary human breast carcinomas J. Clin. Pathol., August 1, 2004; 57(8): 829 - 834. [Abstract] [Full Text] [PDF]
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 O. Stoeltzing, M. F. McCarty, J. S. Wey, F. Fan, W. Liu, A. Belcheva, C. D. Bucana, G. L. Semenza, and L. M. Ellis Role of Hypoxia-Inducible Factor 1{alpha} in Gastric Cancer Cell Growth, Angiogenesis, and Vessel Maturation J Natl Cancer Inst, June 16, 2004; 96(12): 946 - 956. [Abstract] [Full Text] [PDF]
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T. Koike, N. Kimura, K. Miyazaki, T. Yabuta, K. Kumamoto, S. Takenoshita, J. Chen, M. Kobayashi, M. Hosokawa, A. Taniguchi, et al. Hypoxia induces adhesion molecules on cancer cells: A missing link between Warburg effect and induction of selectin-ligand carbohydrates PNAS, May 25, 2004; 101(21): 8132 - 8137. [Abstract] [Full Text] [PDF]
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A M Jubb, T Q Pham, A M Hanby, G D Frantz, F V Peale, T D Wu, H W Koeppen, and K J Hillan Expression of vascular endothelial growth factor, hypoxia inducible factor 1{alpha}, and carbonic anhydrase IX in human tumours J. Clin. Pathol., May 1, 2004; 57(5): 504 - 512. [Abstract] [Full Text] [PDF]
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G. Powis and L. Kirkpatrick Hypoxia inducible factor-1{alpha} as a cancer drug target Mol. Cancer Ther., May 1, 2004; 3(5): 647 - 654. [Abstract] [Full Text] [PDF]
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 G. Hopfl, O. Ogunshola, and M. Gassmann HIFs and tumors--causes and consequences Am J Physiol Regulatory Integrative Comp Physiol, April 1, 2004; 286(4): R608 - R623. [Abstract] [Full Text] [PDF]
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S. Welsh, R. Williams, L. Kirkpatrick, G. Paine-Murrieta, and G. Powis Antitumor activity and pharmacodynamic properties of PX-478, an inhibitor of hypoxia-inducible factor-1{alpha} Mol. Cancer Ther., March 1, 2004; 3(3): 233 - 244. [Abstract] [Full Text]
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K. Ameri, C. E. Lewis, M. Raida, H. Sowter, T. Hai, and A. L. Harris Anoxic induction of ATF-4 through HIF-1-independent pathways of protein stabilization in human cancer cells Blood, March 1, 2004; 103(5): 1876 - 1882. [Abstract] [Full Text] [PDF]
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M. Zimmer, D. Doucette, N. Siddiqui, and O. Iliopoulos Inhibition of Hypoxia-Inducible Factor Is Sufficient for Growth Suppression of VHL-/- Tumors Mol. Cancer Res., February 1, 2004; 2(2): 89 - 95. [Abstract] [Full Text] [PDF]
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M. C. Bosco, M. Puppo, S. Pastorino, Z. Mi, G. Melillo, S. Massazza, A. Rapisarda, and L. Varesio Hypoxia Selectively Inhibits Monocyte Chemoattractant Protein-1 Production by Macrophages J. Immunol., February 1, 2004; 172(3): 1681 - 1690. [Abstract] [Full Text] [PDF]
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J. Li, G. Davidson, Y. Huang, B.-H. Jiang, X. Shi, M. Costa, and C. Huang Nickel Compounds Act through Phosphatidylinositol-3-kinase/Akt-Dependent, p70S6k-Independent Pathway to Induce Hypoxia Inducible Factor Transactivation and Cap43 Expression in Mouse Epidermal Cl41 Cells Cancer Res., January 1, 2004; 64(1): 94 - 101. [Abstract] [Full Text] [PDF]
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C.-J. Hu, L.-Y. Wang, L. A. Chodosh, B. Keith, and M. C. Simon Differential Roles of Hypoxia-Inducible Factor 1{alpha} (HIF-1{alpha}) and HIF-2{alpha} in Hypoxic Gene Regulation Mol. Cell. Biol., December 15, 2003; 23(24): 9361 - 9374. [Abstract] [Full Text] [PDF]
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Y. Makino, H. Nakamura, E. Ikeda, K. Ohnuma, K. Yamauchi, Y. Yabe, L. Poellinger, Y. Okada, C. Morimoto, and H. Tanaka Hypoxia-Inducible Factor Regulates Survival of Antigen Receptor-Driven T Cells J. Immunol., December 15, 2003; 171(12): 6534 - 6540. [Abstract] [Full Text] [PDF]
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N Raghunand, R A Gatenby, and R J Gillies Microenvironmental and cellular consequences of altered blood flow in tumours Br. J. Radiol., December 1, 2003; 76(suppl_1): S11 - S22. [Abstract] [Full Text] [PDF]
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F. Coulet, S. Nadaud, M. Agrapart, and F. Soubrier Identification of Hypoxia-response Element in the Human Endothelial Nitric-oxide Synthase Gene Promoter J. Biol. Chem., November 21, 2003; 278(47): 46230 - 46240. [Abstract] [Full Text] [PDF]
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M. E. Daly, A. Makris, M. Reed, and C. E. Lewis Hemostatic Regulators of Tumor Angiogenesis: A Source of Antiangiogenic Agents for Cancer Treatment? J Natl Cancer Inst, November 19, 2003; 95(22): 1660 - 1673. [Abstract] [Full Text] [PDF]
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 P. Maxwell HIF-1: An Oxygen Response System with Special Relevance to the Kidney J. Am. Soc. Nephrol., November 1, 2003; 14(11): 2712 - 2722. [Full Text] [PDF]
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Y. Cuevas, R. Hernandez-Alcoceba, J. Aragones, S. Naranjo-Suarez, M. C. Castellanos, M. A. Esteban, S. Martin-Puig, M. O. Landazuri, and L. del Peso Specific Oncolytic Effect of a New Hypoxia-Inducible Factor-Dependent Replicative Adenovirus on von Hippel-Lindau-Defective Renal Cell Carcinomas Cancer Res., October 15, 2003; 63(20): 6877 - 6884. [Abstract] [Full Text] [PDF]
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B. Burke, A. Giannoudis, K. P. Corke, D. Gill, M. Wells, L. Ziegler-Heitbrock, and C. E. Lewis Hypoxia-Induced Gene Expression in Human Macrophages: Implications for Ischemic Tissues and Hypoxia-Regulated Gene Therapy Am. J. Pathol., October 1, 2003; 163(4): 1233 - 1243. [Abstract] [Full Text] [PDF]
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S. T. Palayoor, P. J. Tofilon, and C. N. Coleman Ibuprofen-mediated Reduction of Hypoxia-inducible Factors HIF-1{alpha} and HIF-2{alpha} in Prostate Cancer Cells Clin. Cancer Res., August 1, 2003; 9(8): 3150 - 3157. [Abstract] [Full Text] [PDF]
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N. J. Mabjeesh, M. T. Willard, C. E. Frederickson, H. Zhong, and J. W. Simons Androgens Stimulate Hypoxia-inducible Factor 1 Activation via Autocrine Loop of Tyrosine Kinase Receptor/Phosphatidylinositol 3'-Kinase/Protein Kinase B in Prostate Cancer Cells Clin. Cancer Res., July 1, 2003; 9(7): 2416 - 2425. [Abstract] [Full Text] [PDF]
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R. Giavazzi, B. Sennino, D. Coltrini, A. Garofalo, R. Dossi, R. Ronca, M. P. M. Tosatti, and M. Presta Distinct Role of Fibroblast Growth Factor-2 and Vascular Endothelial Growth Factor on Tumor Growth and Angiogenesis Am. J. Pathol., June 1, 2003; 162(6): 1913 - 1926. [Abstract] [Full Text] [PDF]
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M. Y. Liu, L. Poellinger, and C. L. Walker Up-Regulation of Hypoxia-inducible Factor 2{alpha} in Renal Cell Carcinoma Associated with Loss of Tsc-2 Tumor Suppressor Gene Cancer Res., May 15, 2003; 63(10): 2675 - 2680. [Abstract] [Full Text] [PDF]
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R. Fukuda, B. Kelly, and G. L. Semenza Vascular Endothelial Growth Factor Gene Expression in Colon Cancer Cells Exposed to Prostaglandin E2 Is Mediated by Hypoxia-inducible Factor 1 Cancer Res., May 1, 2003; 63(9): 2330 - 2334. [Abstract] [Full Text] [PDF]
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