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JNCI Journal of the National Cancer Institute 2001 93(4):266-276; doi:10.1093/jnci/93.4.266
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Journal of the National Cancer Institute, Vol. 93, No. 4, 266-276, February 21, 2001
© 2001 Oxford University Press

REVIEW

Tumor Hypoxia: Definitions and Current Clinical, Biologic, and Molecular Aspects

Michael Höckel, Peter Vaupel

Affiliations of authors: M. Höckel, Department of Obstetrics and Gynecology, University of Leipzig, Germany; P. Vaupel, Institute of Physiology and Pathophysiology, University of Mainz, Germany.

Correspondence to: Professor Dr. Peter Vaupel, Institute of Physiology and Pathophysiology, University of Mainz, Duesbergweg 6, 55099 Mainz, Germany (e-mail: VAUPEL{at}mail.uni-mainz.de).

Tissue hypoxia results from an inadequate supply of oxygen (O2) that compromises biologic functions. Evidence from experimental and clinical studies increasingly points to a fundamental role for hypoxia in solid tumors. Hypoxia in tumors is primarily a pathophysiologic consequence of structurally and functionally disturbed microcirculation and the deterioration of diffusion conditions. Tumor hypoxia appears to be strongly associated with tumor propagation, malignant progression, and resistance to therapy, and it has thus become a central issue in tumor physiology and cancer treatment. Biochemists and clinicians (as well as physiologists) define hypoxia differently; biochemists define it as O2-limited electron transport, and physiologists and clinicians define it as a state of reduced O2 availability or decreased O2 partial pressure that restricts or even abolishes functions of organs, tissues, or cells. Because malignant tumors no longer execute functions necessary for homeostasis (such as the production of adequate amounts of adenosine triphosphate), the physiology-based definitions of the term "hypoxia" are not necessarily valid for malignant tumors. Instead, alternative definitions based on clinical, biologic, and molecular effects that are observed at O2 partial pressures below a critical level have to be applied.


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Arrest-defective-1 Protein, an Acetyltransferase, Does Not Alter Stability of Hypoxia-inducible Factor (HIF)-1{alpha} and Is Not Induced by Hypoxia or HIF
J. Biol. Chem., September 2, 2005; 280(35): 31132 - 31140.
[Abstract] [Full Text] [PDF]

Home page
 Mol. Cell. Biol.Home page
J. An and M. B. Rettig
Mechanism of von Hippel-Lindau Protein-Mediated Suppression of Nuclear Factor kappa B Activity
Mol. Cell. Biol., September 1, 2005; 25(17): 7546 - 7556.
[Abstract] [Full Text] [PDF]

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 Molecular Cancer TherapeuticsHome page
B. Solomon, D. Binns, P. Roselt, L. I. Weibe, G. A. McArthur, C. Cullinane, and R. J. Hicks
Modulation of intratumoral hypoxia by the epidermal growth factor receptor inhibitor gefitinib detected using small animal PET imaging
Mol. Cancer Ther., September 1, 2005; 4(9): 1417 - 1422.
[Abstract] [Full Text] [PDF]

Home page
 Mol. Cell. Biol.Home page
R. R. Raval, K. W. Lau, M. G. B. Tran, H. M. Sowter, S. J. Mandriota, J.-L. Li, C. W. Pugh, P. H. Maxwell, A. L. Harris, and P. J. Ratcliffe
Contrasting Properties of Hypoxia-Inducible Factor 1 (HIF-1) and HIF-2 in von Hippel-Lindau-Associated Renal Cell Carcinoma
Mol. Cell. Biol., July 1, 2005; 25(13): 5675 - 5686.
[Abstract] [Full Text] [PDF]

Home page
 Am. J. Respir. Crit. Care Med.Home page
M. P. L. Bard, A. Amelink, V. N. Hegt, W. J. Graveland, H. J. C. M. Sterenborg, H. C. Hoogsteden, and J. G. J. V. Aerts
Measurement of Hypoxia-related Parameters in Bronchial Mucosa by Use of Optical Spectroscopy
Am. J. Respir. Crit. Care Med., May 15, 2005; 171(10): 1178 - 1184.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
S.-O. Yoon, S. Shin, and A. M. Mercurio
Hypoxia Stimulates Carcinoma Invasion by Stabilizing Microtubules and Promoting the Rab11 Trafficking of the {alpha}6{beta}4 Integrin
Cancer Res., April 1, 2005; 65(7): 2761 - 2769.
[Abstract] [Full Text] [PDF]

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 J. Physiol.Home page
J. R Robbins, S. M. Lee, A. H Filipovich, P. Szigligeti, L. Neumeier, M. Petrovic, and L. Conforti
Hypoxia modulates early events in T cell receptor-mediated activation in human T lymphocytes via Kv1.3 channels
J. Physiol., April 1, 2005; 564(1): 131 - 143.
[Abstract] [Full Text] [PDF]

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 JCOHome page
A. G. Taghian, R. Abi-Raad, S. I. Assaad, A. Casty, M. Ancukiewicz, E. Yeh, P. Molokhia, K. Attia, T. Sullivan, I. Kuter, et al.
Paclitaxel Decreases the Interstitial Fluid Pressure and Improves Oxygenation in Breast Cancers in Patients Treated With Neoadjuvant Chemotherapy: Clinical Implications
J. Clin. Oncol., March 20, 2005; 23(9): 1951 - 1961.
[Abstract] [Full Text] [PDF]

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 J. Clin. Pathol.Home page
M M Vleugel, A E Greijer, A Shvarts, P van der Groep, M van Berkel, Y Aarbodem, H van Tinteren, A L Harris, P J van Diest, and E van der Wall
Differential prognostic impact of hypoxia induced and diffuse HIF-1{alpha} expression in invasive breast cancer
J. Clin. Pathol., February 1, 2005; 58(2): 172 - 177.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
A. M. Samuni, U. Kasid, E. Y. Chuang, S. Suy, W. DeGraff, M. C. Krishna, A. Russo, and J. B. Mitchell
Effects of Hypoxia on Radiation-Responsive Stress-Activated Protein Kinase, p53, and Caspase 3 Signals in TK6 Human Lymphoblastoid Cells
Cancer Res., January 15, 2005; 65(2): 579 - 586.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
M. O. Arcasoy, K. Amin, S.-C. Chou, Z. A. Haroon, M. Varia, and J. A. Raleigh
Erythropoietin and Erythropoietin Receptor Expression in Head and Neck Cancer: Relationship to Tumor Hypoxia
Clin. Cancer Res., January 1, 2005; 11(1): 20 - 27.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
I. J. Hoogsteen, H. A.M. Marres, K. I.E.M. Wijffels, P. F.J.W. Rijken, J. P.W. Peters, F. J.A. van den Hoogen, E. Oosterwijk, A. J. van der Kogel, and J. H.A.M. Kaanders
Colocalization of Carbonic Anhydrase 9 Expression and Cell Proliferation in Human Head and Neck Squamous Cell Carcinoma
Clin. Cancer Res., January 1, 2005; 11(1): 97 - 106.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
Y.-G. Yoo, M. G. Yeo, D. K. Kim, H. Park, and M.-O. Lee
Novel Function of Orphan Nuclear Receptor Nur77 in Stabilizing Hypoxia-inducible Factor-1{alpha}
J. Biol. Chem., December 17, 2004; 279(51): 53365 - 53373.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
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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 CarcinogenesisHome page
J.-T. Hwang, M. Lee, S.-N. Jung, H.-J. Lee, I. Kang, S.-S. Kim, and J. Ha
AMP-activated protein kinase activity is required for vanadate-induced hypoxia-inducible factor 1{alpha} expression in DU145 cells
Carcinogenesis, December 1, 2004; 25(12): 2497 - 2507.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
A. Bhattacharya, K. Toth, R. Mazurchuk, J. A. Spernyak, H. K. Slocum, L. Pendyala, R. Azrak, S. Cao, F. A. Durrani, and Y. M. Rustum
Lack of Microvessels in Well-Differentiated Regions of Human Head and Neck Squamous Cell Carcinoma A253 Associated with Functional Magnetic Resonance Imaging Detectable Hypoxia, Limited Drug Delivery, and Resistance to Irinotecan Therapy
Clin. Cancer Res., December 1, 2004; 10(23): 8005 - 8017.
[Abstract] [Full Text] [PDF]

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 Mol Cancer ResHome page
W. H. Dragowska, C. Warburton, D. T.T. Yapp, A. I. Minchinton, Y. Hu, D. N. Waterhouse, K. Gelmon, K. Skov, J. Woo, D. Masin, et al.
HER-2/neu Overexpression Increases the Viable Hypoxic Cell Population within Solid Tumors without Causing Changes in Tumor Vascularization
Mol. Cancer Res., November 1, 2004; 2(11): 606 - 619.
[Abstract] [Full Text] [PDF]

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 The OncologistHome page
P. Vaupel and L. Harrison
Tumor Hypoxia: Causative Factors, Compensatory Mechanisms, and Cellular Response
Oncologist, November 1, 2004; 9(suppl_5): 4 - 9.
[Abstract] [Full Text] [PDF]

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 The OncologistHome page
P. Vaupel
The Role of Hypoxia-Induced Factors in Tumor Progression
Oncologist, November 1, 2004; 9(suppl_5): 10 - 17.
[Abstract] [Full Text] [PDF]

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 The OncologistHome page
L. Harrison and K. Blackwell
Hypoxia and Anemia: Factors in Decreased Sensitivity to Radiation Therapy and Chemotherapy?
Oncologist, November 1, 2004; 9(suppl_5): 31 - 40.
[Abstract] [Full Text] [PDF]

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 The OncologistHome page
K. Blackwell, P. Gascon, G. Sigounas, and L. Jolliffe
rHuEPO and Improved Treatment Outcomes: Potential Modes of Action
Oncologist, November 1, 2004; 9(suppl_5): 41 - 47.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
K. L. Bennewith and R. E. Durand
Quantifying Transient Hypoxia in Human Tumor Xenografts by Flow Cytometry
Cancer Res., September 1, 2004; 64(17): 6183 - 6189.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
J. Okami, D. M. Simeone, and C. D. Logsdon
Silencing of the Hypoxia-Inducible Cell Death Protein BNIP3 in Pancreatic Cancer
Cancer Res., August 1, 2004; 64(15): 5338 - 5346.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
Z. F. Yang, R. T. Poon, J. To, D. W. Ho, and S. T. Fan
The Potential Role of Hypoxia Inducible Factor 1{alpha} in Tumor Progression after Hypoxia and Chemotherapy in Hepatocellular Carcinoma
Cancer Res., August 1, 2004; 64(15): 5496 - 5503.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
B. Kaufman, O. Scharf, J. Arbeit, M. Ashcroft, J. M. Brown, R. K. Bruick, J. D. Chapman, S. M. Evans, A. J. Giaccia, A. L. Harris, et al.
Proceedings of the Oxygen Homeostasis/Hypoxia Meeting
Cancer Res., May 1, 2004; 64(9): 3350 - 3356.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. Biol.Home page
A. Suzuki, J. Lu, G.-i. Kusakai, A. Kishimoto, T. Ogura, and H. Esumi
ARK5 Is a Tumor Invasion-Associated Factor Downstream of Akt Signaling
Mol. Cell. Biol., April 15, 2004; 24(8): 3526 - 3535.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
Z. Dong and J. Wang
Hypoxia Selection of Death-resistant Cells: A ROLE FOR Bcl-XL
J. Biol. Chem., March 5, 2004; 279(10): 9215 - 9221.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
Y. Mizukami, J. Li, X. Zhang, M. A. Zimmer, O. Iliopoulos, and D. C. Chung
Hypoxia-Inducible Factor-1-Independent Regulation of Vascular Endothelial Growth Factor by Hypoxia in Colon Cancer
Cancer Res., March 1, 2004; 64(5): 1765 - 1772.
[Abstract] [Full Text] [PDF]

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 BloodHome page
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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 Cancer Res.Home page
E. K. Rofstad, B. Mathiesen, and K. Galappathi
Increased Metastatic Dissemination in Human Melanoma Xenografts after Subcurative Radiation Treatment: Radiation-induced Increase in Fraction of Hypoxic Cells and Hypoxia-induced Up-Regulation of Urokinase-Type Plasminogen Activator Receptor
Cancer Res., January 1, 2004; 64(1): 13 - 18.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
G. H. Mahabeleshwar and G. C. Kundu
Tyrosine Kinase p56lck Regulates Cell Motility and Nuclear Factor {kappa}B-mediated Secretion of Urokinase Type Plasminogen Activator through Tyrosine Phosphorylation of I{kappa}B{alpha} following Hypoxia/Reoxygenation
J. Biol. Chem., December 26, 2003; 278(52): 52598 - 52612.
[Abstract] [Full Text] [PDF]

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 Br. J. Radiol.Home page
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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 Cancer Res.Home page
P. Vaupel, A. Mayer, S. Briest, and M. Hockel
Oxygenation Gain Factor: A Novel Parameter Characterizing the Association between Hemoglobin Level and the Oxygenation Status of Breast Cancers
Cancer Res., November 15, 2003; 63(22): 7634 - 7637.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
A. J. Pantuck, G. Zeng, A. S. Belldegrun, and R. A. Figlin
Pathobiology, Prognosis, and Targeted Therapy for Renal Cell Carcinoma: Exploiting the Hypoxia-Induced Pathway
Clin. Cancer Res., October 15, 2003; 9(13): 4641 - 4652.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
R. L. Aft, J. S. Lewis, F. Zhang, J. Kim, and M. J. Welch
Enhancing Targeted Radiotherapy by Copper(II)diacetyl- bis(N4-methylthiosemicarbazone) Using 2-Deoxy-D-Glucose
Cancer Res., September 1, 2003; 63(17): 5496 - 5504.
[Abstract] [Full Text] [PDF]

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 Molecular Cancer TherapeuticsHome page
G. R. Macpherson, S. S.W. Ng, S. L. Forbes, G. Melillo, T. Karpova, J. McNally, T. P. Conrads, T. D. Veenstra, A. Martinez, F. Cuttitta, et al.
Anti-angiogenic activity of human endostatin is HIF-1-independent in vitro and sensitive to timing of treatment in a human saphenous vein assay
Mol. Cancer Ther., September 1, 2003; 2(9): 845 - 854.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
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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 RadiologyHome page
C. N. Coleman
Linking Radiation Oncology and Imaging through Molecular Biology (or Now That Therapy and Diagnosis Have Separated, It's Time to Get Together Again!)
Radiology, July 1, 2003; 228(1): 29 - 35.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
B. Bachtiary, M. Schindl, R. Potter, B. Dreier, T. H. Knocke, J. A. Hainfellner, R. Horvat, and P. Birner
Overexpression of Hypoxia-inducible Factor 1{alpha} Indicates Diminished Response to Radiotherapy and Unfavorable Prognosis in Patients Receiving Radical Radiotherapy for Cervical Cancer
Clin. Cancer Res., June 1, 2003; 9(6): 2234 - 2240.
[Abstract] [Full Text] [PDF]


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