This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Seagroves, T. N.
Right arrow Articles by Johnson, R. S.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Seagroves, T. N.
Right arrow Articles by Johnson, R. S.

 Previous Article  |  Next Article 

Molecular and Cellular Biology, May 2001, p. 3436-3444, Vol. 21, No. 10
0270-7306/01/$04.00+0   DOI: 10.1128/MCB.21.10.3436-3444.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

Transcription Factor HIF-1 Is a Necessary Mediator of the Pasteur Effect in Mammalian Cells

Tiffany N. Seagroves,1 Heather E. Ryan,1 Han Lu,1 Bradly G. Wouters,2 Merrill Knapp,3 Pierre Thibault,4 Keith Laderoute,3 and Randall S. Johnson1,*

Molecular Biology Section, Division of Biology, University of California San Diego, La Jolla, California 920931; University of Ottawa and the Ottawa Regional Cancer Centre, Ottawa, Ontario K1H 8L6,2 and Institute for Biological Sciences, National Research Council of Canada, Ottawa, Ontario K1A 0R6,4 Canada; and SRI International, Menlo Park, California 940253

Received 15 November 2000/Returned for modification 20 December 2000/Accepted 13 February 2001

The ability to respond to differential levels of oxygen is important to all respiring cells. The response to oxygen deficiency, or hypoxia, takes many forms and ranges from systemic adaptations to those that are cell autonomous. Perhaps the most ancient of the cell-autonomous adaptations to hypoxia is a metabolic one: the Pasteur effect, which includes decreased oxidative phosphorylation and an increase in anaerobic fermentation. Because anaerobic fermentation produces far less ATP than oxidative phosphorylation per molecule of glucose, increased activity of the glycolytic pathway is necessary to maintain free ATP levels in the hypoxic cell. Here, we present genetic and biochemical evidence that, in mammalian cells, this metabolic switch is regulated by the transcription factor HIF-1. As a result, cells lacking HIF-1alpha exhibit decreased growth rates during hypoxia, as well as decreased levels of lactic acid production and decreased acidosis. We show that this decrease in glycolytic capacity results in dramatically lowered free ATP levels in HIF-1alpha -deficient hypoxic cells. Thus, HIF-1 activation is an essential control element of the metabolic state during hypoxia; this requirement has important implications for the regulation of cell growth during development, angiogenesis, and vascular injury.

* Corresponding author. Mailing address: Division of Biology, University of California, San Diego, 1212 Pacific Hall, Mail code 0366, 9500 Gilman Dr., La Jolla, CA 92093. Phone: (858) 822-0509. Fax: (858) 534-5831. E-mail: rjohnson{at}biomail.ucsd.edu.

Molecular and Cellular Biology, May 2001, p. 3436-3444, Vol. 21, No. 10
0270-7306/01/$04.00+0   DOI: 10.1128/MCB.21.10.3436-3444.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.


This article has been cited by other articles:

  • Rankin, E. B., Rha, J., Selak, M. A., Unger, T. L., Keith, B., Liu, Q., Haase, V. H. (2009). Hypoxia-Inducible Factor 2 Regulates Hepatic Lipid Metabolism. Mol. Cell. Biol. 29: 4527-4538 [Abstract] [Full Text]  
  • Semenza, G. L. (2009). Regulation of Oxygen Homeostasis by Hypoxia-Inducible Factor 1. Physiology 24: 97-106 [Abstract] [Full Text]  
  • Xie, H., Valera, V. A., Merino, M. J., Amato, A. M., Signoretti, S., Linehan, W. M., Sukhatme, V. P., Seth, P. (2009). LDH-A inhibition, a therapeutic strategy for treatment of hereditary leiomyomatosis and renal cell cancer. Molecular Cancer Therapeutics 8: 626-635 [Abstract] [Full Text]  
  • Knaup, K. X., Jozefowski, K., Schmidt, R., Bernhardt, W. M., Weidemann, A., Juergensen, J. S., Warnecke, C., Eckardt, K.-U., Wiesener, M. S. (2009). Mutual Regulation of Hypoxia-Inducible Factor and Mammalian Target of Rapamycin as a Function of Oxygen Availability. Mol Cancer Res 7: 88-98 [Abstract] [Full Text]  
  • Beyer, S., Kristensen, M. M., Jensen, K. S., Johansen, J. V., Staller, P. (2008). The Histone Demethylases JMJD1A and JMJD2B Are Transcriptional Targets of Hypoxia-inducible Factor HIF. J. Biol. Chem. 283: 36542-36552 [Abstract] [Full Text]  
  • Wirthner, R., Wrann, S., Balamurugan, K., Wenger, R. H., Stiehl, D. P. (2008). Impaired DNA double-strand break repair contributes to chemoresistance in HIF-1{alpha}-deficient mouse embryonic fibroblasts. Carcinogenesis 29: 2306-2316 [Abstract] [Full Text]  
  • Choi, S. M., Cho, H.-J., Cho, H., Kim, K. H., Kim, J. B., Park, H. (2008). Stra13/DEC1 and DEC2 inhibit sterol regulatory element binding protein-1c in a hypoxia-inducible factor-dependent mechanism. Nucleic Acids Res 36: 6372-6385 [Abstract] [Full Text]  
  • Zhai, P., Sadoshima, J. (2008). Overcoming an Energy Crisis?: An Adaptive Role of Glycogen Synthase Kinase-3 Inhibition in Ischemia/Reperfusion. Circ. Res. 103: 910-913 [Full Text]  
  • Lu, C.-W., Lin, S.-C., Chen, K.-F., Lai, Y.-Y., Tsai, S.-J. (2008). Induction of Pyruvate Dehydrogenase Kinase-3 by Hypoxia-inducible Factor-1 Promotes Metabolic Switch and Drug Resistance. J. Biol. Chem. 283: 28106-28114 [Abstract] [Full Text]  
  • Wang, L., Gao, J., Dai, W., Lu, L. (2008). Activation of Polo-like Kinase 3 by Hypoxic Stresses. J. Biol. Chem. 283: 25928-25935 [Abstract] [Full Text]  
  • Schipani, E., Clemens, T. L. (2008). Hypoxia and the Hypoxia-Inducible Factors in the Skeleton. IBMS BoneKEy 5: 275-284 [Abstract] [Full Text]  
  • Walczak-Drzewiecka, A., Ratajewski, M., Wagner, W., Dastych, J. (2008). HIF-1{alpha} Is Up-Regulated in Activated Mast Cells by a Process That Involves Calcineurin and NFAT. J. Immunol. 181: 1665-1672 [Abstract] [Full Text]  
  • Gillies, R. J., Robey, I., Gatenby, R. A. (2008). Causes and Consequences of Increased Glucose Metabolism of Cancers. JNM 49: 24S-42S [Abstract] [Full Text]  
  • Zhang, H., Bosch-Marce, M., Shimoda, L. A., Tan, Y. S., Baek, J. H., Wesley, J. B., Gonzalez, F. J., Semenza, G. L. (2008). Mitochondrial Autophagy Is an HIF-1-dependent Adaptive Metabolic Response to Hypoxia. J. Biol. Chem. 283: 10892-10903 [Abstract] [Full Text]  
  • Jantsch, J., Chakravortty, D., Turza, N., Prechtel, A. T., Buchholz, B., Gerlach, R. G., Volke, M., Glasner, J., Warnecke, C., Wiesener, M. S., Eckardt, K.-U., Steinkasserer, A., Hensel, M., Willam, C. (2008). Hypoxia and Hypoxia-Inducible Factor-1{alpha} Modulate Lipopolysaccharide-Induced Dendritic Cell Activation and Function. J. Immunol. 180: 4697-4705 [Abstract] [Full Text]  
  • Koh, M. Y., Spivak-Kroizman, T., Venturini, S., Welsh, S., Williams, R. R., Kirkpatrick, D. L., Powis, G. (2008). Molecular mechanisms for the activity of PX-478, an antitumor inhibitor of the hypoxia-inducible factor-1{alpha}. Molecular Cancer Therapeutics 7: 90-100 [Abstract] [Full Text]  
  • Mason, S. D., Rundqvist, H., Papandreou, I., Duh, R., McNulty, W. J., Howlett, R. A., Olfert, I. M., Sundberg, C. J., Denko, N. C., Poellinger, L., Johnson, R. S. (2007). HIF-1{alpha} in endurance training: suppression of oxidative metabolism. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293: R2059-R2069 [Abstract] [Full Text]  
  • Cai, Q., Murakami, M., Si, H., Robertson, E. S. (2007). A Potential {alpha}-Helix Motif in the Amino Terminus of LANA Encoded by Kaposi's Sarcoma-Associated Herpesvirus Is Critical for Nuclear Accumulation of HIF-1{alpha} in Normoxia. J. Virol. 81: 10413-10423 [Abstract] [Full Text]  
  • Hoogewijs, D., Terwilliger, N. B., Webster, K. A., Powell-Coffman, J. A., Tokishita, S., Yamagata, H., Hankeln, T., Burmester, T., Rytkonen, K. T., Nikinmaa, M., Abele, D., Heise, K., Lucassen, M., Fandrey, J., Maxwell, P. H., Pahlman, S., Gorr, T. A. (2007). From critters to cancers: bridging comparative and clinical research on oxygen sensing, HIF signaling, and adaptations towards hypoxia. Integr. Comp. Biol. 47: 552-577 [Abstract] [Full Text]  
  • Mizukami, Y., Kohgo, Y., Chung, D. C. (2007). Hypoxia Inducible Factor-1 Independent Pathways in Tumor Angiogenesis. Clin. Cancer Res. 13: 5670-5674 [Abstract] [Full Text]  
  • Dehne, N., Kerkweg, U., Otto, T., Fandrey, J. (2007). The HIF-1 response to simulated ischemia in mouse skeletal muscle cells neither enhances glycolysis nor prevents myotube cell death. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293: R1693-R1701 [Abstract] [Full Text]  
  • Agrawal, A., Guttapalli, A., Narayan, S., Albert, T. J., Shapiro, I. M., Risbud, M. V. (2007). Normoxic stabilization of HIF-1{alpha} drives glycolytic metabolism and regulates aggrecan gene expression in nucleus pulposus cells of the rat intervertebral disk. Am. J. Physiol. Cell Physiol. 293: C621-C631 [Abstract] [Full Text]  
  • Cairns, R. A., Papandreou, I., Sutphin, P. D., Denko, N. C. (2007). Metabolic targeting of hypoxia and HIF1 in solid tumors can enhance cytotoxic chemotherapy. Proc. Natl. Acad. Sci. USA 104: 9445-9450 [Abstract] [Full Text]  
  • Lum, J. J., Bui, T., Gruber, M., Gordan, J. D., DeBerardinis, R. J., Covello, K. L., Simon, M. C., Thompson, C. B. (2007). The transcription factor HIF-1{alpha} plays a critical role in the growth factor-dependent regulation of both aerobic and anaerobic glycolysis. Genes Dev. 21: 1037-1049 [Abstract] [Full Text]  
  • Gruber, M., Hu, C.-J., Johnson, R. S., Brown, E. J., Keith, B., Simon, M. C. (2007). Acute postnatal ablation of Hif-2{alpha} results in anemia. Proc. Natl. Acad. Sci. USA 104: 2301-2306 [Abstract] [Full Text]  
  • Maher, J. C., Wangpaichitr, M., Savaraj, N., Kurtoglu, M., Lampidis, T. J. (2007). Hypoxia-inducible factor-1 confers resistance to the glycolytic inhibitor 2-deoxy-D-glucose. Molecular Cancer Therapeutics 6: 732-741 [Abstract] [Full Text]  
  • Liao, D., Corle, C., Seagroves, T. N., Johnson, R. S. (2007). Hypoxia-Inducible Factor-1{alpha} Is a Key Regulator of Metastasis in a Transgenic Model of Cancer Initiation and Progression. Cancer Res. 67: 563-572 [Abstract] [Full Text]  
  • Lopez-Lazaro, M. (2006). Hypoxia-Inducible Factor 1 as a Possible Target for Cancer Chemoprevention. Cancer Epidemiol. Biomarkers Prev. 15: 2332-2335 [Abstract] [Full Text]  
  • Choi, S. M., Choi, K.-O., Park, Y.-K., Cho, H., Yang, E. G., Park, H. (2006). Clioquinol, a Cu(II)/Zn(II) Chelator, Inhibits Both Ubiquitination and Asparagine Hydroxylation of Hypoxia-inducible Factor-1{alpha}, Leading to Expression of Vascular Endothelial Growth Factor and Erythropoietin in Normoxic Cells. J. Biol. Chem. 281: 34056-34063 [Abstract] [Full Text]  
  • Ke, Q., Costa, M. (2006). Hypoxia-Inducible Factor-1 (HIF-1). Mol. Pharmacol. 70: 1469-1480 [Abstract] [Full Text]  
  • Oda, T., Hirota, K., Nishi, K., Takabuchi, S., Oda, S., Yamada, H., Arai, T., Fukuda, K., Kita, T., Adachi, T., Semenza, G. L., Nohara, R. (2006). Activation of hypoxia-inducible factor 1 during macrophage differentiation. Am. J. Physiol. Cell Physiol. 291: C104-C113 [Abstract] [Full Text]  
  • Lopez-Lazaro, M. (2006). HIF-1: hypoxia-inducible factor or dysoxia-inducible factor?. FASEB J. 20: 828-832 [Abstract] [Full Text]  
  • Rissanen, E., Tranberg, H. K., Sollid, J., Nilsson, G. E., Nikinmaa, M. (2006). Temperature regulates hypoxia-inducible factor-1 (HIF-1) in a poikilothermic vertebrate, crucian carp (Carassius carassius). J. Exp. Biol. 209: 994-1003 [Abstract] [Full Text]  
  • Ibrahim, N. O., Hahn, T., Franke, C., Stiehl, D. P., Wirthner, R., Wenger, R. H., Katschinski, D. M. (2005). Induction of the Hypoxia-Inducible Factor System by Low Levels of Heat Shock Protein 90 Inhibitors. Cancer Res. 65: 11094-11100 [Abstract] [Full Text]  
  • Choi, K.-O., Lee, T., Lee, N., Kim, J.-H., Yang, E. G., Yoon, J. M., Kim, J. H., Lee, T. G., Park, H. (2005). Inhibition of the Catalytic Activity of Hypoxia-Inducible Factor-1{alpha}-Prolyl-Hydroxylase 2 by a MYND-Type Zinc Finger. Mol. Pharmacol. 68: 1803-1809 [Abstract] [Full Text]  
  • Biju, M. P., Akai, Y., Shrimanker, N., Haase, V. H. (2005). Protection of HIF-1-deficient primary renal tubular epithelial cells from hypoxia-induced cell death is glucose dependent. Am. J. Physiol. Renal Physiol. 289: F1217-F1226 [Abstract] [Full Text]  
  • Raval, R. R., Lau, K. W., Tran, M. G. B., Sowter, H. M., Mandriota, S. J., Li, J.-L., Pugh, C. W., Maxwell, P. H., Harris, A. L., Ratcliffe, P. J. (2005). Contrasting Properties of Hypoxia-Inducible Factor 1 (HIF-1) and HIF-2 in von Hippel-Lindau-Associated Renal Cell Carcinoma. Mol. Cell. Biol. 25: 5675-5686 [Abstract] [Full Text]  
  • Nakamura, H., Makino, Y., Okamoto, K., Poellinger, L., Ohnuma, K., Morimoto, C., Tanaka, H. (2005). TCR Engagement Increases Hypoxia-Inducible Factor-1{alpha} Protein Synthesis via Rapamycin-Sensitive Pathway under Hypoxic Conditions in Human Peripheral T Cells. J. Immunol. 174: 7592-7599 [Abstract] [Full Text]  
  • Grimberg, A., Coleman, C. M., Burns, T. F., Himelstein, B. P., Koch, C. J., Cohen, P., El-Deiry, W. S. (2005). p53-Dependent and p53-Independent Induction of Insulin-Like Growth Factor Binding Protein-3 by Deoxyribonucleic Acid Damage and Hypoxia. J. Clin. Endocrinol. Metab. 90: 3568-3574 [Abstract] [Full Text]  
  • Covello, K. L., Simon, M. C., Keith, B. (2005). Targeted Replacement of Hypoxia-Inducible Factor-1{alpha} by a Hypoxia-Inducible Factor-2{alpha} Knock-in Allele Promotes Tumor Growth. Cancer Res. 65: 2277-2286 [Abstract] [Full Text]  
  • Xie, L., Johnson, R. S., Freeman, R. S. (2005). Inhibition of NGF deprivation-induced death by low oxygen involves suppression of BIMEL and activation of HIF-1. JCB 168: 911-920 [Abstract] [Full Text]  
  • Piret, J.-P., Minet, E., Cosse, J.-P., Ninane, N., Debacq, C., Raes, M., Michiels, C. (2005). Hypoxia-inducible Factor-1-dependent Overexpression of Myeloid Cell Factor-1 Protects Hypoxic Cells against tert-Butyl Hydroperoxide-induced Apoptosis. J. Biol. Chem. 280: 9336-9344 [Abstract] [Full Text]  
  • Blum, R., Jacob-Hirsch, J., Amariglio, N., Rechavi, G., Kloog, Y. (2005). Ras Inhibition in Glioblastoma Down-regulates Hypoxia-Inducible Factor-1{alpha}, Causing Glycolysis Shutdown and Cell Death. Cancer Res. 65: 999-1006 [Abstract] [Full Text]  
  • Obach, M., Navarro-Sabate, A., Caro, J., Kong, X., Duran, J., Gomez, M., Perales, J. C., Ventura, F., Rosa, J. L., Bartrons, R. (2004). 6-Phosphofructo-2-kinase (pfkfb3) Gene Promoter Contains Hypoxia-inducible Factor-1 Binding Sites Necessary for Transactivation in Response to Hypoxia. J. Biol. Chem. 279: 53562-53570 [Abstract] [Full Text]  
  • Bindra, R. S., Schaffer, P. J., Meng, A., Woo, J., Maseide, K., Roth, M. E., Lizardi, P., Hedley, D. W., Bristow, R. G., Glazer, P. M. (2004). Down-Regulation of Rad51 and Decreased Homologous Recombination in Hypoxic Cancer Cells. Mol. Cell. Biol. 24: 8504-8518 [Abstract] [Full Text]  
  • Semenza, G. L. (2004). Hydroxylation of HIF-1: Oxygen Sensing at the Molecular Level. Physiology 19: 176-182 [Abstract] [Full Text]  
  • Michiels, C. (2004). Physiological and Pathological Responses to Hypoxia. Am. J. Pathol. 164: 1875-1882 [Abstract] [Full Text]  
  • Laderoute, K. R., Calaoagan, J. M., Knapp, M., Johnson, R. S. (2004). Glucose Utilization Is Essential for Hypoxia-Inducible Factor 1{alpha}-Dependent Phosphorylation of c-Jun. Mol. Cell. Biol. 24: 4128-4137 [Abstract] [Full Text]  
  • Pfander, D., Kobayashi, T., Knight, M. C., Zelzer, E., Chan, D. A., Olsen, B. R., Giaccia, A. J., Johnson, R. S., Haase, V. H., Schipani, E. (2004). Deletion of Vhlh in chondrocytes reduces cell proliferation and increases matrix deposition during growth plate development. Development 131: 2497-2508 [Abstract] [Full Text]  
  • Hu, C.-J., Wang, L.-Y., Chodosh, L. A., Keith, B., Simon, M. C. (2003). Differential Roles of Hypoxia-Inducible Factor 1{alpha} (HIF-1{alpha}) and HIF-2{alpha} in Hypoxic Gene Regulation. Mol. Cell. Biol. 23: 9361-9374 [Abstract] [Full Text]  
  • Yim, S., Choi, S. M., Choi, Y., Lee, N., Chung, J., Park, H. (2003). Insulin and Hypoxia Share Common Target Genes but Not the Hypoxia-inducible Factor-1{alpha}. J. Biol. Chem. 278: 38260-38268 [Abstract] [Full Text]  
  • Huang, L. E., Bunn, H. F. (2003). Hypoxia-inducible Factor and Its Biomedical Relevance. J. Biol. Chem. 278: 19575-19578 [Full Text]  
  • Pfander, D., Cramer, T., Schipani, E., Johnson, R. S. (2003). HIF-1{alpha} controls extracellular matrix synthesis by epiphyseal chondrocytes. J. Cell Sci. 116: 1819-1826 [Abstract] [Full Text]  
  • Chen, J., Zhao, S., Nakada, K., Kuge, Y., Tamaki, N., Okada, F., Wang, J., Shindo, M., Higashino, F., Takeda, K., Asaka, M., Katoh, H., Sugiyama, T., Hosokawa, M., Kobayashi, M. (2003). Dominant-Negative Hypoxia-Inducible Factor-1{alpha} Reduces Tumorigenicity of Pancreatic Cancer Cells through the Suppression of Glucose Metabolism. Am. J. Pathol. 162: 1283-1291 [Abstract] [Full Text]  
  • Krishnamachary, B., Berg-Dixon, S., Kelly, B., Agani, F., Feldser, D., Ferreira, G., Iyer, N., LaRusch, J., Pak, B., Taghavi, P., Semenza, G. L. (2003). Regulation of Colon Carcinoma Cell Invasion by Hypoxia-Inducible Factor 1. Cancer Res. 63: 1138-1143 [Abstract] [Full Text]  
  • Goda, N., Ryan, H. E., Khadivi, B., McNulty, W., Rickert, R. C., Johnson, R. S. (2003). Hypoxia-Inducible Factor 1{alpha} Is Essential for Cell Cycle Arrest during Hypoxia. Mol. Cell. Biol. 23: 359-369 [Abstract] [Full Text]  
  • Koumenis, C., Naczki, C., Koritzinsky, M., Rastani, S., Diehl, A., Sonenberg, N., Koromilas, A., Wouters, B. G. (2002). Regulation of Protein Synthesis by Hypoxia via Activation of the Endoplasmic Reticulum Kinase PERK and Phosphorylation of the Translation Initiation Factor eIF2{alpha}. Mol. Cell. Biol. 22: 7405-7416 [Abstract] [Full Text]  
  • Karni, R., Dor, Y., Keshet, E., Meyuhas, O., Levitzki, A. (2002). Activated pp60c-Src Leads to Elevated Hypoxia-inducible Factor (HIF)-1alpha Expression under Normoxia. J. Biol. Chem. 277: 42919-42925 [Abstract] [Full Text]  
  • Isaacs, J. S., Jung, Y.-J., Mimnaugh, E. G., Martinez, A., Cuttitta, F., Neckers, L. M. (2002). Hsp90 Regulates a von Hippel Lindau-independent Hypoxia-inducible Factor-1alpha -degradative Pathway. J. Biol. Chem. 277: 29936-29944 [Abstract] [Full Text]  
  • Palmada, M., Kanwal, S., Rutkoski, N.J., Gustafson-Brown, C., Johnson, R.S., Wisdom, R., Carter, B.D. (2002). c-jun is essential for sympathetic neuronal death induced by NGF withdrawal but not by p75 activation. JCB 158: 453-461 [Abstract] [Full Text]  
  • WENGER, R. H. (2002). Cellular adaptation to hypoxia: O2-sensing protein hydroxylases, hypoxia-inducible transcription factors, and O2-regulated gene expression. FASEB J. 16: 1151-1162 [Abstract] [Full Text]  
  • Hopfl, G., Wenger, R. H., Ziegler, U., Stallmach, T., Gardelle, O., Achermann, R., Wergin, M., Kaser-Hotz, B., Saunders, H. M., Williams, K. J., Stratford, I. J., Gassmann, M., Desbaillets, I. (2002). Rescue of Hypoxia-inducible Factor-1{alpha}-deficient Tumor Growth by Wild-Type Cells Is Independent of Vascular Endothelial Growth Factor. Cancer Res. 62: 2962-2970 [Abstract] [Full Text]  
  • Minchenko, A., Leshchinsky, I., Opentanova, I., Sang, N., Srinivas, V., Armstead, V., Caro, J. (2002). Hypoxia-inducible Factor-1-mediated Expression of the 6-Phosphofructo-2-kinase/fructose-2,6-bisphosphatase-3 (PFKFB3) Gene. ITS POSSIBLE ROLE IN THE WARBURG EFFECT. J. Biol. Chem. 277: 6183-6187 [Abstract] [Full Text]  
  • Marti, H. H., Katschinski, D. M., Wagner, K. F., Schaffer, L., Stier, B., Wenger, R. H. (2002). Isoform-Specific Expression of Hypoxia-Inducible Factor-1{alpha} During the Late Stages of Mouse Spermiogenesis. Mol. Endocrinol. 16: 234-243 [Abstract] [Full Text]  
  • Griffiths, J. R., McSheehy, P. M. J., Robinson, S. P., Troy, H., Chung, Y.-L., Leek, R. D., Williams, K. J., Stratford, I. J., Harris, A. L., Stubbs, M. (2002). Metabolic Changes Detected by in Vivo Magnetic Resonance Studies of HEPA-1 Wild-Type Tumors and Tumors Deficient in Hypoxia-inducible Factor-1{beta} (HIF-1{beta}): Evidence of an Anabolic Role for the HIF-1 Pathway. Cancer Res. 62: 688-695 [Abstract] [Full Text]  
  • Schipani, E., Ryan, H. E., Didrickson, S., Kobayashi, T., Knight, M., Johnson, R. S. (2001). Hypoxia in cartilage: HIF-1alpha is essential for chondrocyte growth arrest and survival. Genes Dev. 15: 2865-2876 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»