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Overexpression of Hypoxia-inducible Factor 1 in Common Human Cancers and Their Metastases¹

The Johns Hopkins Oncology Center, Brady Urological Institute [H. Z., M. L., W. B. I., J. W. S.], Department of Pathology [A. M. D.], Departments of Pediatrics and Medicine, and Institute of Genetic Medicine [E. L., G. L. S.], The Johns Hopkins University School of Medicine, Baltimore, Maryland 21287; Department of Histopathology, Derriford Hospital, Plymouth PL6 8DH, United Kingdom [D. A. H.]; Department of Pathology, Division of Neuropathology, New York University Medical Center, New York, New York 10016 [D. Z.]; and Division of General Surgery, University of California-Los Angeles School of Medicine, Los Angeles, California 90095-6904 [P. B.]

Neovascularization and increased glycolysis, two universal characteristics of solid tumors, represent adaptations to a hypoxic microenvironment that are correlated with tumor invasion, metastasis, and lethality. Hypoxia-inducible factor 1 (HIF-1) activates transcription of genes encoding glucose transporters, glycolytic enzymes, and vascular endothelial growth factor. HIF-1 transcriptional activity is determined by regulated expression of the HIF-1 subunit. In this study, HIF-1 expression was analyzed by immunohistochemistry in 179 tumor specimens. HIF-1 was overexpressed in 13 of 19 tumor types compared with the respective normal tissues, including colon, breast, gastric, lung, skin, ovarian, pancreatic, prostate, and renal carcinomas. HIF-1 expression was correlated with aberrant p53 accumulation and cell proliferation. Preneoplastic lesions in breast, colon, and prostate overexpressed HIF-1, whereas benign tumors in breast and uterus did not. HIF-1 overexpression was detected in only 29% of primary breast cancers but in 69% of breast cancer metastases. In brain tumors, HIF-1 immunohistochemistry demarcated areas of angiogenesis. These results provide the first clinical data indicating that HIF-1 may play an important role in human cancer progression.

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				M. Lopez-Lazaro Hypoxia-Inducible Factor 1 as a Possible Target for Cancer Chemoprevention Cancer Epidemiol. Biomarkers Prev., December 1, 2006; 15(12): 2332 - 2335. [Abstract] [Full Text] [PDF]

				C. Leo, L.-C. Horn, C. Rauscher, B. Hentschel, A. Liebmann, G. Hildebrandt, and M. Hockel Expression of Erythropoietin and Erythropoietin Receptor in Cervical Cancer and Relationship to Survival, Hypoxia, and Apoptosis Clin. Cancer Res., December 1, 2006; 12(23): 6894 - 6900. [Abstract] [Full Text] [PDF]

				J.-H. Lim, J.-W. Park, M.-S. Kim, S.-K. Park, R. S. Johnson, and Y.-S. Chun Bafilomycin Induces the p21-Mediated Growth Inhibition of Cancer Cells under Hypoxic Conditions by Expressing Hypoxia-Inducible Factor-1{alpha} Mol. Pharmacol., December 1, 2006; 70(6): 1856 - 1865. [Abstract] [Full Text] [PDF]

				Y.-J. Peng, G. Yuan, D. Ramakrishnan, S. D. Sharma, M. Bosch-Marce, G. K. Kumar, G. L. Semenza, and N. R. Prabhakar Heterozygous HIF-1{alpha} deficiency impairs carotid body-mediated systemic responses and reactive oxygen species generation in mice exposed to intermittent hypoxia J. Physiol., December 1, 2006; 577(2): 705 - 716. [Abstract] [Full Text] [PDF]

				S. Patiar and A. L Harris Role of hypoxia-inducible factor-1{alpha} as a cancer therapy target Endocr. Relat. Cancer, December 1, 2006; 13(Supplement_1): S61 - S75. [Abstract] [Full Text] [PDF]

				H. Choi, Y.-S. Chun, S.-W. Kim, M.-S. Kim, and J.-W. Park Curcumin Inhibits Hypoxia-Inducible Factor-1 by Degrading Aryl Hydrocarbon Receptor Nuclear Translocator: A Mechanism of Tumor Growth Inhibition Mol. Pharmacol., November 1, 2006; 70(5): 1664 - 1671. [Abstract] [Full Text] [PDF]

				Q. Ke and M. Costa Hypoxia-Inducible Factor-1 (HIF-1) Mol. Pharmacol., November 1, 2006; 70(5): 1469 - 1480. [Abstract] [Full Text] [PDF]

				K S Kimbro and J W Simons Hypoxia-inducible factor-1 in human breast and prostate cancer. Endocr. Relat. Cancer, September 1, 2006; 13(3): 739 - 749. [Abstract] [Full Text] [PDF]

				R. P Singh and R. Agarwal Mechanisms of action of novel agents for prostate cancer chemoprevention. Endocr. Relat. Cancer, September 1, 2006; 13(3): 751 - 778. [Abstract] [Full Text] [PDF]

				D. T. Jones and A. L. Harris Identification of novel small-molecule inhibitors of hypoxia-inducible factor-1 transactivation and DNA binding. Mol. Cancer Ther., September 1, 2006; 5(9): 2193 - 2202. [Abstract] [Full Text] [PDF]

				G. Melillo Inhibiting Hypoxia-Inducible Factor 1 for Cancer Therapy Mol. Cancer Res., September 1, 2006; 4(9): 601 - 605. [Abstract] [Full Text] [PDF]

				Y. Sumiyoshi, Y. Kakeji, A. Egashira, K. Mizokami, H. Orita, and Y. Maehara Overexpression of Hypoxia-Inducible Factor 1{alpha} and p53 Is a Marker for an Unfavorable Prognosis in Gastric Cancer Clin. Cancer Res., September 1, 2006; 12(17): 5112 - 5117. [Abstract] [Full Text] [PDF]

				G. L. Semenza Regulation of physiological responses to continuous and intermittent hypoxia by hypoxia-inducible factor 1 Exp Physiol, September 1, 2006; 91(5): 803 - 806. [Abstract] [Full Text] [PDF]

				S. McMahon, M. Charbonneau, S. Grandmont, D. E. Richard, and C. M. Dubois Transforming Growth Factor beta1 Induces Hypoxia-inducible Factor-1 Stabilization through Selective Inhibition of PHD2 Expression J. Biol. Chem., August 25, 2006; 281(34): 24171 - 24181. [Abstract] [Full Text] [PDF]

				S.-B. Catrina, I. R. Botusan, A. Rantanen, A. I. Catrina, P. Pyakurel, O. Savu, M. Axelson, P. Biberfeld, L. Poellinger, and K. Brismar Hypoxia-Inducible Factor-1{alpha} and Hypoxia-Inducible Factor-2{alpha} Are Expressed in Kaposi Sarcoma and Modulated by Insulin-like Growth Factor-I Clin. Cancer Res., August 1, 2006; 12(15): 4506 - 4514. [Abstract] [Full Text] [PDF]

				D. Generali, A. Berruti, M. P. Brizzi, L. Campo, S. Bonardi, S. Wigfield, A. Bersiga, G. Allevi, M. Milani, S. Aguggini, et al. Hypoxia-Inducible Factor-1{alpha} Expression Predicts a Poor Response to Primary Chemoendocrine Therapy and Disease-Free Survival in Primary Human Breast Cancer Clin. Cancer Res., August 1, 2006; 12(15): 4562 - 4568. [Abstract] [Full Text] [PDF]

				L. Li, X. Lin, A. R. Shoemaker, D. H. Albert, S. W. Fesik, and Y. Shen Hypoxia-Inducible Factor-1 Inhibition in Combination with Temozolomide Treatment Exhibits Robust Antitumor Efficacy In vivo Clin. Cancer Res., August 1, 2006; 12(15): 4747 - 4754. [Abstract] [Full Text] [PDF]

				D. Nie, S. Krishnamoorthy, R. Jin, K. Tang, Y. Chen, Y. Qiao, A. Zacharek, Y. Guo, J. Milanini, G. Pages, et al. Mechanisms Regulating Tumor Angiogenesis by 12-Lipoxygenase in Prostate Cancer Cells J. Biol. Chem., July 7, 2006; 281(27): 18601 - 18609. [Abstract] [Full Text] [PDF]

				A. Kaidi, D. Qualtrough, A. C. Williams, and C. Paraskeva Direct Transcriptional Up-regulation of Cyclooxygenase-2 by Hypoxia-Inducible Factor (HIF)-1 Promotes Colorectal Tumor Cell Survival and Enhances HIF-1 Transcriptional Activity during Hypoxia. Cancer Res., July 1, 2006; 66(13): 6683 - 6691. [Abstract] [Full Text] [PDF]

				C. Koumenis and B. G. Wouters "Translating" Tumor Hypoxia: Unfolded Protein Response (UPR)-Dependent and UPR-Independent Pathways Mol. Cancer Res., July 1, 2006; 4(7): 423 - 436. [Abstract] [Full Text] [PDF]

				E.-J. Yeo, J.-H. Ryu, Y.-S. Chun, Y.-S. Cho, I.-J. Jang, H. Cho, J. Kim, M.-S. Kim, and J.-W. Park YC-1 Induces S Cell Cycle Arrest and Apoptosis by Activating Checkpoint Kinases. Cancer Res., June 15, 2006; 66(12): 6345 - 6352. [Abstract] [Full Text] [PDF]

				Q. Zhang, S.-Y. Wang, A. C. Nottke, J. V. Rocheleau, D. W. Piston, and R. H. Goodman Redox sensor CtBP mediates hypoxia-induced tumor cell migration PNAS, June 13, 2006; 103(24): 9029 - 9033. [Abstract] [Full Text] [PDF]

				H. Okuyama, B. Krishnamachary, Y. F. Zhou, H. Nagasawa, M. Bosch-Marce, and G. L. Semenza Expression of Vascular Endothelial Growth Factor Receptor 1 in Bone Marrow-derived Mesenchymal Cells Is Dependent on Hypoxia-inducible Factor 1 J. Biol. Chem., June 2, 2006; 281(22): 15554 - 15563. [Abstract] [Full Text] [PDF]