Molecular pathways: hypoxia response in immune cells fighting or promoting cancer

Targeting of HIF-α to the von Hippel-Lindau Ubiquitylation Complex by O ₂ -Regulated Prolyl Hydroxylation

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Molecular mechanisms and clinical applications of angiogenesis

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Macrophage Diversity Enhances Tumor Progression and Metastasis

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Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis

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Macrophage activation and polarization

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A nuclear factor induced by hypoxia via de novo protein synthesis binds to the human erythropoietin gene enhancer at a site required for transcriptional activation

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Hypoxia-inducible factors and the response to hypoxic stress

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Durable Complete Responses in Heavily Pretreated Patients with Metastatic Melanoma Using T-Cell Transfer Immunotherapy

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Immunosuppressive networks in the tumour environment and their therapeutic relevance

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Control of TH17/Treg Balance by Hypoxia-Inducible Factor 1

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HIF‐1α is required for solid tumor formation and embryonic vascularization

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FIH-1 is an asparaginyl hydroxylase enzyme that regulates the transcriptional activity of hypoxia-inducible factor

Lando, D., Peet, D. J., Gorman, J. J., Whelan, D. A., Whitelaw, M. L., & Bruick, R. K. (2002) · Genes & Development · doi:10.1101/gad.991402 · Cited by 1,550 · see citing works

Tumour hypoxia promotes tolerance and angiogenesis via CCL28 and Treg cells

Facciabene, A., Peng, X., Hagemann, I. S., Balint, K., Barchetti, A., Wang, L.-P., Gimotty, P. A., Gilks, C. B., Lal, P., Zhang, L., et al. (2011) · Nature · doi:10.1038/nature10169 · Cited by 1,376 · see citing works

Endothelial PAS domain protein 1 (EPAS1), a transcription factor selectively expressed in endothelial cells.

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The Expression and Distribution of the Hypoxia-Inducible Factors HIF-1α and HIF-2α in Normal Human Tissues, Cancers, and Tumor-Associated Macrophages

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Macrophage polarization in tumour progression

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Different Tumor Microenvironments Contain Functionally Distinct Subsets of Macrophages Derived from Ly6C(high) Monocytes

Movahedi, K., Laoui, D., Gysemans, C. A., Baeten, M., Stangé, G. M., den Bossche, J. V., Mack, M., PIPELEERS, D. G., Veld, P. I. '., BAETSELIER, P. D., et al. (2010) · Cancer Research · doi:10.1158/0008-5472.can-09-4672 · Cited by 1,229 · see citing works

HIF-1α regulates function and differentiation of myeloid-derived suppressor cells in the tumor microenvironment

Corzo, C. A., Condamine, T., Lu, L., Cotter, M. J., Youn, J.-I., Cheng, P., Cho, H.-I., Celis, E., Quiceno, D. G., Padhya, T., et al. (2010) · Journal of Experimental Medicine · doi:10.1084/jem.20100587 · Cited by 1,173 · see citing works

HIF1α Induces the Recruitment of Bone Marrow-Derived Vascular Modulatory Cells to Regulate Tumor Angiogenesis and Invasion

Du, R., Lu, K. V., Petritsch, C. K., Liu, P., Ganß, R., Passegue, E. A., Song, H., VandenBerg, S. R., Johnson, R. S., Werb, Z., et al. (2008) · Cancer Cell · doi:10.1016/j.ccr.2008.01.034 · Cited by 1,131 · see citing works

A2A adenosine receptor protects tumors from antitumor T cells

Ohta, A., Gorelik, E., Prasad, S. J., Ronchese, F., Lukashev, D. E., Wong, M. K. K., Huang, X., Caldwell, S. A., Liu, K., Smith, P. T., et al. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0605251103 · Cited by 1,066 · see citing works

Integration of Oxygen Signaling at the Consensus HRE

Wenger, R. H., Stiehl, D. P., & Camenisch, G. (2005) · Science's STKE · doi:10.1126/stke.3062005re12 · Cited by 1,032 · see citing works

Substrate Fate in Activated Macrophages: A Comparison between Innate, Classic, and Alternative Activation

Rodríguez-Prados, J.-C., Través, P. G., Cuenca, J., Rico, D., Aragonés, J., Martín-Sanz, P., Cascante, M., & Boscá, L. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.0901698 · Cited by 1,022 · see citing works

A novel bHLH-PAS factor with close sequence similarity to hypoxia-inducible factor 1α regulates the <i>VEGF</i> expression and is potentially involved in lung and vascular development

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Histopathologic-Based Prognostic Factors of Colorectal Cancers Are Associated With the State of the Local Immune Reaction

Mlecnik, B., Tosolini, M., Kirilovsky, A., Berger, A., Bindea, G., Meatchi, T., Bruneval, P., Trajanoski, Z., Fridman, W.-H., Pagès, F., et al. (2011) · Journal of Clinical Oncology · doi:10.1200/jco.2010.30.5425 · Cited by 1,009 · see citing works

Oxygen Sensing, Homeostasis, and Disease

Semenza, G. L. (2011) · New England Journal of Medicine · doi:10.1056/nejmra1011165 · Cited by 989 · see citing works

Tumor microenvironmental physiology and its implications for radiation oncology

Vaupel, P. W. (2004) · Seminars in Radiation Oncology · doi:10.1016/j.semradonc.2004.04.008 · Cited by 948 · see citing works

An essential role for p300/CBP in the cellular response to hypoxia

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HIF-1α expression regulates the bactericidal capacity of phagocytes

Peyssonnaux, C., Datta, V., Cramer, T., Doedens, A. L., Theodorakis, E. A., Gallo, R. L., Hurtado‐Ziola, N., Nizet, V., & Johnson, R. S. (2005) · Journal of Clinical Investigation · doi:10.1172/jci23865 · Cited by 702 · see citing works

hsa-miR-210 Is Induced by Hypoxia and Is an Independent Prognostic Factor in Breast Cancer

Camps, C., Buffa, F. M., Colella, S., Moore, J., Sotiriou, C. P., Sheldon, H., Harris, A. L., Gleadle, J., & Ragoussis, J. (2008) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-07-1755 · Cited by 658 · see citing works

Macrophage Expression of Hypoxia-Inducible Factor-1α Suppresses T-Cell Function and Promotes Tumor Progression

Doedens, A. L., Stockmann, C., Rubinstein, M. P., Liao, D., Zhang, N., DeNardo, D. G., Coussens, L. M., Karin, M., Goldrath, A. W., & Johnson, R. S. (2010) · Cancer Research · doi:10.1158/0008-5472.can-10-1439 · Cited by 652 · see citing works

Immunostimulatory monoclonal antibodies for cancer therapy

Melero, I., Hervás‐Stubbs, S., Glennie, M. J., Pardoll, D. M., & Chen, L. (2007) · Nature reviews. Cancer · doi:10.1038/nrc2051 · Cited by 626 · see citing works

Differential activation and antagonistic function of HIF-α isoforms in macrophages are essential for NO homeostasisPreprint

Takeda, N., O'Dea, E. L., Doedens, A. L., Kim, J., Weidemann, A., Stockmann, C., Asagiri, M., Simon, M. C., Hoffmann, A., & Johnson, R. S. (2010) · Genes & Development · doi:10.1101/gad.1881410 · Cited by 621 · see citing works

Hypoxia-inducible factor-2 (HIF-2) regulates hepatic erythropoietin in vivo

Rankin, E. B., Biju, M. P., Liu, Q., Unger, T. L., Rha, J., Johnson, R. S., Simon, M. C., Keith, B., & Haase, V. H. (2007) · Journal of Clinical Investigation · doi:10.1172/jci30117 · Cited by 596 · see citing works

Vascular normalization in Rgs5-deficient tumours promotes immune destruction

Hamzah, J., Jugold, M., Kiessling, F. M., Rigby, P. J., Manzur, M., Marti, H. H., Rabie, T., Kaden, S., Gröne, H., Hämmerling, G. J., et al. (2008) · Nature · doi:10.1038/nature06868 · Cited by 565 · see citing works

Regulation of immune cells by local-tissue oxygen tension: HIF1α and adenosine receptors

Sitkovsky, M., & Lukashev, D. (2005) · Nature Reviews Immunology · doi:10.1038/nri1685 · Cited by 518 · see citing works

Hypoxia-inducible factor 2α regulates macrophage function in mouse models of acute and tumor inflammation

Imtiyaz, H. Z., Williams, E. P., Hickey, M. M., Patel, S. A., Durham, A. C., Yuan, L.-J., Hammond, R., Gimotty, P. A., Keith, B., & Simon, M. C. (2010) · Journal of Clinical Investigation · doi:10.1172/jci39506 · Cited by 461 · see citing works

Hypoxic gene activation by lipopolysaccharide in macrophages: implication of hypoxia-inducible factor 1α

Blouin, C. C., Pagé, E. L., Soucy, G. M., & Richard, D. E. (2003) · Blood · doi:10.1182/blood-2003-07-2427 · Cited by 459 · see citing works

Hypoxia-inducible factor 1 is a master regulator of breast cancer metastatic niche formation

Wong, C. C.-L., Gilkes, D. M., Zhang, H., Chen, J., Wei, H., Chaturvedi, P., Fraley, S. I., Wong, C.-M., Khoo, U.-S., Ng, I. O.-L., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1113483108 · Cited by 437 · see citing works

Differential Effects of Physiologically Relevant Hypoxic Conditions on T Lymphocyte Development and Effector Functions

Caldwell, C. C., Kojima, H., Lukashev, D., Armstrong, J., Farber, M., Apasov, S. G., & Sitkovsky, M. V. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.167.11.6140 · Cited by 420 · see citing works

Hydrogen peroxide secreted by tumor‐derived macrophages down‐modulates signal‐transducing zeta molecules and inhibits tumor‐specific T cell‐and natural killer cell‐mediated cytotoxicity

Kono, K., Salazar‐Onfray, F., Petersson, M., Hansson, J., Masucci, G. V., Wasserman, K., Nakazawa, T., Anderson, P., & Kiessling, R. W. (1996) · European Journal of Immunology · doi:10.1002/eji.1830260620 · Cited by 360 · see citing works

Hypoxia-inducible factors 1 and 2 are important transcriptional effectors in primary macrophages experiencing hypoxia

Fang, H.-Y., Hughes, R., Murdoch, C., Coffelt, S. B., Biswas, S. K., Harris, A. L., Johnson, R. S., Imityaz, H. Z., Simon, M. C., Fredlund, E., et al. (2009) · Blood · doi:10.1182/blood-2008-12-195941 · Cited by 319 · see citing works

Oxygen Sensors at the Crossroad of Metabolism

Aragonés, J., Fraisl, P., Baes, M. I., & Carmeliet, P. (2009) · Cell Metabolism · doi:10.1016/j.cmet.2008.10.001 · Cited by 290 · see citing works

Macrophage skewing by Phd2 haplodeficiency prevents ischaemia by inducing arteriogenesis

Takeda, Y., Costa, S., Delamarre, E., Roncal, C., de Oliveira, R. L., Squadrito, M. L., Finisguerra, V., Deschoemaeker, S., Bruyére, F., Wenes, M., et al. (2011) · Nature · doi:10.1038/nature10507 · Cited by 287 · see citing works

Tumor Promotion via Injury- and Death-Induced Inflammation

Kuraishy, A. I., Karin, M., & Grivennikov, S. I. (2011) · Immunity · doi:10.1016/j.immuni.2011.09.006 · Cited by 265 · see citing works

Hypoxia-Inducible Factor-1 (HIF-1) Up-Regulates Adrenomedullin Expression in Human Tumor Cell Lines during Oxygen Deprivation: A Possible Promotion Mechanism of Carcinogenesis

Garayoa, M., Martı́nez, A., Lee, S., Pı́o, R., An, W. G., Neckers, L., Trepel, J. B., Montuenga, L. M., Ryan, H. E., Johnson, R. S., et al. (2000) · Molecular Endocrinology · doi:10.1210/mend.14.6.0473 · Cited by 262 · see citing works

Blocking Hypoxia-Induced Autophagy in Tumors Restores Cytotoxic T-Cell Activity and Promotes Regression

Noman, M. Z., Janji, B., Kaminska, B., Van Moer, K., Pierson, S., Przanowski, P., Buart, S., Berchem, G., Romero, P., Mami-Chouaib, F., et al. (2011) · Cancer Research · doi:10.1158/0008-5472.can-11-1094 · Cited by 256 · see citing works

Turn me on: regulating HIF transcriptional activity

Lisy, K., & Peet, D. J. (2008) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4402315 · Cited by 235 · see citing works

CD73: A Novel Target for Cancer Immunotherapy

Zhang, B. (2010) · Cancer Research · doi:10.1158/0008-5472.can-10-1544 · Cited by 234 · see citing works

Oxygen sensors in context

Ward, J. P. T. (2007) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2007.10.010 · Cited by 219 · see citing works

Arginine availability, arginase, and the immune response

Bansal, V., & Ochoa, J. B. (2003) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/00075197-200303000-00012 · Cited by 213 · see citing works

Cutting Edge: Hypoxia-Inducible Factor 1α and Its Activation-Inducible Short Isoform I.1 Negatively Regulate Functions of CD4+ and CD8+ T Lymphocytes

Lukashev, D., Klebanov, B., Kojima, H., Grinberg, A., Ohta, A., Berenfeld, L., Wenger, R. H., Ohta, A., & Sitkovsky, M. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.177.8.4962 · Cited by 208 · see citing works

Prediction of survival in diffuse large B-cell lymphoma based on the expression of 2 genes reflecting tumor and microenvironment

Alizadeh, A. A., Gentles, A. J., Alencar, A. J., Liu, C. L., Kohrt, H. E. K., Houot, R., Goldstein, M. J., Zhao, S., Natkunam, Y., Advani, R. H., et al. (2011) · Blood · doi:10.1182/blood-2011-03-345272 · Cited by 200 · see citing works

Targeted Deletion of HIF-1α Gene in T Cells Prevents their Inhibition in Hypoxic Inflamed Tissues and Improves Septic Mice Survival

Thiel, M., Caldwell, C. C., Kreth, S., Kuboki, S., Chen, P., Smith, P., Ohta, A., Lentsch, A. B., Lukashev, D., & Sitkovsky, M. V. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000853 · Cited by 175 · see citing works

Knockout of HIF-1 in tumor-associated macrophages enhances M2 polarization and attenuates their pro-angiogenic responses

Werno, C., Menrad, H., Weigert, A., Dehne, N., Goerdt, S., Schledzewski, K., Kzhyshkowska, J. G., & Brune, B. (2010) · Carcinogenesis · doi:10.1093/carcin/bgq088 · Cited by 168 · see citing works

Importance of culturing primary lymphocytes at physiological oxygen levels

Atkuri, K. R., Herzenberg, L. A., Niemi, A.-K., Cowan, T., & Herzenberg, L. A. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0611732104 · Cited by 163 · see citing works

Agonist Anti-CD137 mAb Act on Tumor Endothelial Cells to Enhance Recruitment of Activated T Lymphocytes

Palazón, A., Teijeira, Á., Martínez‐Forero, I., Hervás‐Stubbs, S., Roncal, C., Peñuelas, I., Dubrot, J., Morales‐Kastresana, A., Perez‐Gracia, J. L., Ochoa, M. C., et al. (2011) · Cancer Research · doi:10.1158/0008-5472.can-10-1733 · Cited by 143 · see citing works

Tumor and stromal pathways mediating refractoriness/resistance to anti-angiogenic therapies

Crawford, Y., & Ferrara, N. (2009) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2009.09.004 · Cited by 140 · see citing works

Hypoxia modulates the gene expression profile of immunoregulatory receptors in human mature dendritic cells: identification of TREM-1 as a novel hypoxic marker in vitro and in vivo

Bosco, M. C., Pierobon, D., Blengio, F., Raggi, F., Vanni, C., Gattorno, M., Eva, A., Novelli, F., Cappello, P., Giovarelli, M., et al. (2010) · Blood · doi:10.1182/blood-2010-06-292136 · Cited by 125 · see citing works

Hypoxia inducible factor 1α regulates T cell receptor signal transduction

Neumann, A. K., Yang, J., Biju, M. P., Joseph, S. K., Johnson, R. S., Haase, V. H., Freedman, B. D., & Turka, L. A. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506070102 · Cited by 120 · see citing works

Culturing at atmospheric oxygen levels impacts lymphocyte function

Atkuri, K. R., Herzenberg, L. A., & Herzenberg, L. A. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0409910102 · Cited by 114 · see citing works

Multi-layered action mechanisms of CD137 (4-1BB)-targeted immunotherapies

Melero, I., Murillo, O., Dubrot, J., Hervás‐Stubbs, S., & Perez‐Gracia, J. L. (2008) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2008.05.005 · Cited by 107 · see citing works

Hypoxia-Dependent Inhibition of Tumor Cell Susceptibility to CTL-Mediated Lysis Involves NANOG Induction in Target Cells

Hasmim, M., Noman, M. Z., Lauriol, J., Benlalam, H., Mallavialle, A., Rosselli, F., Mami‐Chouaib, F., Alcaïde‐Loridan, C., & Chouaı̈b, S. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1101011 · Cited by 65 · see citing works

The interaction between HIF-1 and AP-1 transcription factors in response to low oxygen

Laderoute, K. R. (2005) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2005.03.005 · Cited by 63 · see citing works

Carcinoma-Derived Interleukin-8 Disorients Dendritic Cell Migration Without Impairing T-Cell Stimulation

Alfaro, C., Suárez, N., Martínez‐Forero, I., Palazón, A., Rouzaut, A., Solano, S., Feijoó, E., Gúrpide, A., Bolaños, E., Erro, L., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0017922 · Cited by 43 · see citing works

Hypoxia-inducible factor-1α suppresses the expression of macrophage scavenger receptor 1

Shirato, K., Kizaki, T., Sakurai, T., Ogasawara, J.-E., Ishibashi, Y., Iijima, T., Okada, C., Noguchi, I., Imaizumi, K., Taniguchi, N., et al. (2009) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-009-0702-y · Cited by 37 · see citing works

Oxygen Is a Master Regulator of the Immunogenicity of Primary Human Glioma Cells

Olin, M. R., Andersen, B. M., Litterman, A. J., Grogan, P. T., Sarver, A. L., Robertson, P. T., Liang, X., Chen, W., Parney, I. F., Hunt, M. A., et al. (2011) · Cancer Research · doi:10.1158/0008-5472.can-11-1166 · Cited by 18 · see citing works

Antiangiogenesis Strategies Revisited: From Starving Tumors to Alleviating Hypoxia

Jain, R. K. (2014) · Cancer Cell · doi:10.1016/j.ccell.2014.10.006 · Cited by 1,589 · see citing works

Therapeutic targeting of hypoxia and hypoxia-inducible factors in cancer

Wigerup, C., Påhlman, S., & Bexell, D. (2016) · Pharmacology &amp; Therapeutics · doi:10.1016/j.pharmthera.2016.04.009 · Cited by 687 · see citing works

Vascular Normalization as an Emerging Strategy to Enhance Cancer Immunotherapy

Huang, Y., Goel, S., Duda, D. G., Fukumura, D., & Jain, R. K. (2013) · Cancer Research · doi:10.1158/0008-5472.can-12-4354 · Cited by 669 · see citing works

Improving immunotherapy outcomes with anti-angiogenic treatments and vice versa

Khan, K. A., & Kerbel, R. S. (2018) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2018.9 · Cited by 661 · see citing works

Deciphering and Reversing Tumor Immune Suppression

Motz, G. T., & Coukos, G. (2013) · Immunity · doi:10.1016/j.immuni.2013.07.005 · Cited by 600 · see citing works

Hypoxia-targeted drug delivery

Sharma, A. K., Arambula, J. F., Koo, S., Kumar, R., Singh, H., Sessler, J. L., & Kim, J. S. (2018) · Chemical Society Reviews · doi:10.1039/c8cs00304a · Cited by 547 · see citing works

Targeting the tumor vasculature to enhance T cell activity

Lanitis, E., Irving, M. B., & Coukos, G. (2015) · Current Opinion in Immunology · doi:10.1016/j.coi.2015.01.011 · Cited by 338 · see citing works

Targeting the renin-angiotensin system to improve cancer treatment: Implications for immunotherapy

Pinter, M., & Jain, R. K. (2017) · Science Translational Medicine · doi:10.1126/scitranslmed.aan5616 · Cited by 335 · see citing works

Hypoxia‐inducible factors in regulation of immune responses in tumour microenvironment

Kumar, V., & Gabrilovich, D. I. (2014) · Immunology · doi:10.1111/imm.12380 · Cited by 329 · see citing works

Combining microenvironment normalization strategies to improve cancer immunotherapy

Mpekris, F., Voutouri, C., Baish, J. W., Duda, D. G., Munn, L. L., Stylianopoulos, T., & Jain, R. K. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1919764117 · Cited by 292 · see citing works

Hypoxia downregulates the expression of activating receptors involved in NK ‐cell‐mediated target cell killing without affecting ADCC

Balsamo, M., Manzini, C., Pietra, G., Raggi, F., Blengio, F., Mingari, M. C., Varesio, L., Moretta, L., Bosco, M. C., & Vitale, M. (2013) · European Journal of Immunology · doi:10.1002/eji.201343448 · Cited by 284 · see citing works

Reprogramming the tumor microenvironment: tumor-induced immunosuppressive factors paralyze T cells

Wu, A. A., Drake, V. E., Huang, H.-S., Chiu, S., & Zheng, L. (2015) · OncoImmunology · doi:10.1080/2162402x.2015.1016700 · Cited by 274 · see citing works

Regulation of the anti-tumour immune response by cancer-associated fibroblasts

Harper, J. A., & Sainson, R. C. A. (2014) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2013.12.005 · Cited by 269 · see citing works

Randomized Phase II and Biomarker Study of Pembrolizumab plus Bevacizumab versus Pembrolizumab Alone for Patients with Recurrent Glioblastoma

Nayak, L., Molinaro, A. M., Peters, K. B., Clarke, J. L., Jordan, J. T., de Groot, J., Nghiemphu, L., Kaley, T. J., Colman, H., McCluskey, C. S., et al. (2020) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-20-2500 · Cited by 267 · see citing works

Anti-VEGF therapy induces ECM remodeling and mechanical barriers to therapy in colorectal cancer liver metastases

Rahbari, N. N., Kedrin, D., Incio, J., Liu, H., Ho, W. W., Nia, H. T., Edrich, C. M., Jung, K., Daubriac, J., Chen, I., et al. (2016) · Science Translational Medicine · doi:10.1126/scitranslmed.aaf5219 · Cited by 258 · see citing works

Increased vessel perfusion predicts the efficacy of immune checkpoint blockade

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