4,068
Views
3
CrossRef citations to date
0
Altmetric
Review Article

Study on hypoxia-inducible factor and its roles in immune system

, , , , &
Pages 223-236 | Received 30 Dec 2020, Accepted 25 Mar 2021, Published online: 25 Apr 2021

References

  • Cheng SC, Quintin J, Cramer RA, et al. mTOR-and HIF-1α–mediated aerobic glycolysis as metabolic basis for trained immunity. Science. 2014;345(6204):1250684.
  • Rius J, Guma M, Schachtrup C, et al. NF-κB links innate immunity to the hypoxic response through transcriptional regulation of HIF-1α. Nature. 2008;453(7196):807–811.
  • Peyssonnaux C, Boutin AT, Zinkernagel AS, et al. Critical role of HIF-1α in keratinocyte defense against bacterial infection. J Invest Dermatol. 2008;128(8):1964–1968.
  • Cramer T, Johnson RS. A novel role for the hypoxia inducible transcription factor HIF-1alpha: critical regulation of inflammatory cell function. Cell Cycle. 2003;2(3):191–192.
  • Moorlag SJ, Röring RJ, Joosten LA, et al. The role of the interleukin‐1 family in trained immunity. Immunol Rev. 2018;281(1):28–39.
  • Tannahill GM, Curtis AM, Adamik J, et al. Succinate is an inflammatory signal that induces IL-1β through HIF-1α. Nature. 2013;496(7444):238–242.
  • Shi LZ, Wang R, Huang G, et al. dependent glycolytic pathway orchestrates a metabolic checkpoint for the differentiation of TH17 and Treg cells. J Exp Med. 2011;208(7):1367–1376.
  • Cramer T, Yamanishi Y, Clausen BE, et al. HIF-1α is essential for myeloid cell-mediated inflammation. Cell. 2003;112(5):645–657.
  • Acosta-Iborra B, Elorza A, Olazabal IM, et al. Macrophage oxygen sensing modulates antigen presentation and phagocytic functions involving IFN-γ production through the HIF-1α transcription factor. J Immunol. 2009;182(5):3155–3164.
  • Walmsley SR, Farahi N, Peyssonnaux C, et al. Hypoxia-induced neutrophil survival is mediated by HIF-1α–dependent NF-κB activity. J Exp Med. 2005;201(1):105–115.
  • Walmsley SR, Chilvers ER, Thompson AA, et al. Prolyl hydroxylase 3 (PHD3) is essential for hypoxic regulation of neutrophilic inflammation in humans and mice. J Clin Invest. 2011;121(3):1053–1063.
  • Schatz V, Strüssmann Y, Mahnke A, et al. Myeloid cell–derived HIF-1α promotes control of Leishmania major. J Immunol. 2016;197(10):4034–4041.
  • van Dijk A, Hedegaard CJ, Haagsman HP, et al. The potential for immunoglobulins and host defense peptides (HDPs) to reduce the use of antibiotics in animal production. Vet Res. 2018;49(1):1–6.
  • Kitamura K, Kangawa K, Kawamoto M, et al. Adrenomedullin: a novel hypotensive peptide isolated from human pheochromocytoma. Biochem Biophys Res Commun. 1993;192(2):553–560.
  • Imtiyaz HZ, Williams EP, Hickey MM, et al. Hypoxia-inducible factor 2α regulates macrophage function in mouse models of acute and tumor inflammation. J Clin Invest. 2010;120(8):2699–2714.
  • Thompson AR, Elks PM, Marriott HM, et al. Hypoxia-inducible factor 2α regulates key neutrophil functions in humans, mice, and zebrafish. Blood. 2014;123(3):366–376.
  • Elks PM, van Eeden FJ, Dixon G, et al. Activation of hypoxia-inducible factor-1α (Hif-1α) delays inflammation resolution by reducing neutrophil apoptosis and reverse migration in a zebrafish inflammation model. Blood. 2011;118(3):712–722.
  • Kojima H, Gu H, Nomura S, et al. Abnormal B lymphocyte development and autoimmunity in hypoxia-inducible factor 1α-deficient chimeric mice. Proc Natl Acad Sci USA. 2002;99(4):2170–2174.
  • Goda N, Ryan HE, Khadivi B, et al. Hypoxia-inducible factor 1α is essential for cell cycle arrest during hypoxia. Mol Cell Biol. 2003;23(1):359–369.
  • Palazon A, Goldrath AW, Nizet V, et al. HIF transcription factors, inflammation, and immunity. Immunity. 2014;41(4):518–528.
  • Wang H, Flach H, Onizawa M, et al. Negative regulation of Hif1a expression and TH 17 differentiation by the hypoxia-regulated microRNA miR-210. Nat Immunol. 2014;15(4):393–401.
  • Clambey ET, McNamee EN, Westrich JA, et al. Hypoxia-inducible factor-1 alpha–dependent induction of FoxP3 drives regulatory T-cell abundance and function during inflammatory hypoxia of the mucosa. Proc Natl Acad Sci USA. 2012;109(41):E2784–E2793.
  • Angelin A, Gil-de-Gómez L, Dahiya S, et al. Foxp3 reprograms T cell metabolism to function in low-glucose, high-lactate environments. Cell Metab. 2017;25(66):1282–1293.
  • Yoshimura Y. Avian β-defensins expression for the innate immune system in hen reproductive organs. Poult Sci. 2015;94(4):804–809.
  • Kumar V, Gabrilovich DI. Hypoxia‐inducible factors in regulation of immune responses in tumour microenvironment. Immunology. 2014;143(4):512–519.
  • Poitz DM, Augstein A, Hesse K, et al. Regulation of the HIF-system in human macrophages–Differential regulation of HIF-α subunits under sustained hypoxia. Mol Immunol. 2014;57(2):226–235.
  • Singh SP, Sharma J, Ahmad T, et al. Oxygen stress: impact on innate immune system, antioxidant defence system and expression of HIF-1α and ATPase 6 genes in Catla catla. Fish Physiol Biochem. 2016;42(2):673–688.
  • Harris AJ, Thompson AR, Whyte MK, et al. HIF-mediated innate immune responses: cell signaling and therapeutic implications. Hypoxia (Auckl). 2014;2:47–58.
  • Thompson AR, Binham J, Plant T, et al. Hypoxia, the HIF pathway and neutrophilic inflammatory responses. Biol Chem. 2013;394(4):471–477.
  • Palsson‐McDermott EM, O'neill LA. The Warburg effect then and now: from cancer to inflammatory diseases. Bioessays. 2013;35(11):965–973.
  • Hu X, Li YQ, Li QG, et al. Osteoglycin-induced VEGF inhibition enhances T lymphocytes infiltrating in colorectal cancer. EBioMedicine. 2018;34:35–45.
  • Sefikogullari M, Kaya A, Aydin H, et al. Increased levels of VEGF-A and HIF-1α in Turkish children with Crimean-Congo hemorrhagic fever. J Arthropod Borne Dis. 2017;11(1):19–26.
  • Liu J, Zeng Y, Ma W, et al. Preliminary investigation of the clinical value of vascular endothelial growth factor and hypoxia-inducible factor-1α in pericardial fluid in diagnosing malignant and tuberculous pericardial effusion. Cardiology. 2010;116(1):37–41.
  • Wan J, Wu W. Hyperthermia induced HIF-1a expression of lung cancer through AKT and ERK signaling pathways. J Exp Clin Cancer Res. 2016;35(1):119.
  • Gupta N, Wish JB. Hypoxia-inducible factor prolyl hydroxylase inhibitors: a potential new treatment for anemia in patients with CKD. Am J Kidney Dis. 2017;69(6):815–826.
  • Martinez VG, Ontoria-Oviedo I, Ricardo CP, et al. Overexpression of hypoxia-inducible factor 1 alpha improves immunomodulation by dental mesenchymal stem cells. Stem Cell Res Ther. 2017;8(1):208.
  • Burrows N, Maxwell PH. Hypoxia and B cells. Exp Cell Res. 2017;356(2):197–203.
  • Berger EA, McClellan SA, Vistisen KS, et al. HIF-1α is essential for effective PMN bacterial killing, antimicrobial peptide production and apoptosis in Pseudomonas aeruginosa keratitis. PLoS Pathog. 2013;9(7):e1003457.
  • Palsson-McDermott EM, Curtis AM, Goel G, et al. Pyruvate kinase M2 regulates Hif-1α activity and IL-1β induction and is a critical determinant of the warburg effect in LPS-activated macrophages. Cell Metab. 2015;1(1):65–80.
  • Lohninger L, Tomasova L, Praschberger M, et al. Hydrogen sulphide induces HIF-1α and Nrf2 in THP-1 macrophages. Biochimie. 2015;112:187–195.
  • Shalova IN, Lim JY, Chittezhath M, et al. Human monocytes undergo functional re-programming during sepsis mediated by hypoxia-inducible factor-1α. Immunity. 2015;42(3):484–498.
  • Bhandari T, Olson J, Johnson RS, et al. HIF-1α influences myeloid cell antigen presentation and response to subcutaneous OVA vaccination. J Mol Med (Berl). 2013;91(10):1199–1205.
  • Nizet V, Johnson RS. Interdependence of hypoxic and innate immune responses. Nat Rev Immunol. 2009;9(9):609–617.
  • Zarember KA, Malech HL. HIF-1α: a master regulator of innate host defenses? J Clin Invest. 2005;115(7):1702–1704.
  • Morinet F, Casetti L, François JH, et al. Oxygen tension level and human viral infections. Virology. 2013;444(1-2):31–36.
  • Gupta-Saraf P, Miller CL. HIF-1α downregulation and apoptosis in hypoxic prostate tumor cells infected with oncolytic mammalian orthoreovirus. Oncotarget. 2014;5(2):561–574.
  • Fraga CA, Oliveira MV, Alves LR, et al. Immunohistochemical profile of HIF-1α, VEGF-A, VEGFR2 and MMP9 proteins in tegumentary leishmaniasis. An Bras Dermatol. 2012;87(5):709–713.
  • Hammami A, Charpentier T, Smans M, et al. IRF-5-mediated inflammation limits CD8+ T cell expansion by inducing HIF-1α and impairing dendritic cell functions during Leishmania infection. PLoS Pathog. 2015;11(6):e1004938.
  • Song T, Li H, Yang L, et al. Expression of hypoxia-inducible factor-1α in the infiltrative belt surrounding hepatic alveolar echinococcosis in rats. J Parasitol. 2015;101(3):369–373.
  • Hirota K. Involvement of hypoxia-inducible factors in the dysregulation of oxygen homeostasis in sepsis. Cardiovasc Hematol Disord Drug Targets. 2015;15(1):29–40.
  • Schäfer ST, Frede S, Winning S, et al. Hypoxia-inducible factor and target gene expression are decreased in patients with sepsis: prospective observational clinical and cellular studies. Anesthesiology. 2013;118(6):1426–1436.
  • Zhang L, Ye SB, Li ZL, et al. Increased HIF-1alpha expression in tumor cells and lymphocytes of tumor microenvironments predicts unfavorable survival in esophageal squamous cell carcinoma patients. Int J Clin Exp Path. 2014;7(7):3887.
  • Palazón A, Martínez-Forero I, Teijeira A, et al. The HIF-1α hypoxia response in tumor-infiltrating T lymphocytes induces functional CD137 (4-1BB) for immunotherapy. Cancer Discov. 2012;2(7):608–623.
  • Noman MZ, Desantis G, Janji B, et al. PD-L1 is a novel direct target of HIF-1α, and its blockade under hypoxia enhanced MDSC-mediated T cell activation. J Exp Med. 2014;211(55):781–790.
  • Bollinger T, Bollinger A, Gies S, et al. Transcription regulates HIF‐1α expression in CD4+ T cells. Immun Cell Biol. 94(1):109–113.
  • Warfel NA, El-Deiry WS. HIF-1 signaling in drug resistance to chemotherapy. Curr Med Chem. 2014;21(26):3021–3028.
  • Kobayashi H, Ohyama T, Kitamura-Miyazaki M, et al. Studies on novel HIF activators, A-503451sII: biological activities of A-503451A. J Antibiot. 2016;69(10):754–758.
  • Lee SH, Jee JG, Bae JS, et al. A group of novel HIF-1α inhibitors, glyceollins, blocks HIF-1α synthesis and decreases its stability via inhibition of the PI3K/AKT/mTOR pathway and Hsp90 binding. J Cell Physiol. 2015;230(4):853–862.
  • Selvaraju V, Parinandi NL, Adluri RS, et al. Molecular mechanisms of action and therapeutic uses of pharmacological inhibitors of HIF-prolyl 4-hydroxylases for treatment of ischemic diseases. Antioxid Redox Signal. 2014;20(1616):2631–2665.
  • Lai FF, Niu F, Yang HZ, et al. Development of a novel screening assay for inhibitors targeting HIF-1alpha and P300 interaction. Yao Xue Xue Bao. 2014;49(6):849–853.
  • Eltzschig HK, Bratton DL, Colgan SP. Targeting hypoxia signalling for the treatment of ischaemic and inflammatory diseases. Nat Rev Drug Discov. 2014;13(11):852–869.
  • Ramakrishnan SK, Shah YM. Role of intestinal HIF-2α in health and disease. Annu Rev Physiol. 2016;78:301–325.
  • Scholz CC, Taylor CT. Targeting the HIF pathway in inflammation and immunity. Curr Opin Pharmacol. 2013;1;13(4):646–653.
  • Zinkernagel AS, Johnson RS, Nizet V. Hypoxia inducible factor (HIF) function in innate immunity and infection. J Mol Med (Berl). 2007;85(12):1339–1346.
  • Feldhoff LM, Rueda CM, Moreno-Fernandez ME, et al. IL-1β induced HIF-1α inhibits the differentiation of human FOXP3+ T cells. Sci Rep. 2017;7(1):1.
  • Jang Y, Jeong SH, Park YH, et al. UVB induces HIF-1α-dependent TSLP expression via the JNK and ERK pathways. J Invest Dermatol. 2013;133(11):2601–2608.
  • Zhao G, Liu Y, Fang J, et al. Dimethyl fumarate inhibits the expression and function of hypoxia-inducible factor-1α (HIF-1α). Biochem Biophys Res Commun. 2014;6448(3):303–307.
  • Wilczynski J, Duechler M, Czyz M. Targeting NF-κB and HIF-1 pathways for the treatment of cancer: part I. Arch Immunol Ther Exp. 2011;59(4):289–299.
  • Bobek G, Surmon L, Mirabito KM, et al. Placental regulation of inflammation and hypoxia after TNF-α Infusion in Mice. Am J Reprod Immunol. 2015;74(5):407–418.
  • Näthke I, Rocha S. Antagonistic crosstalk between APC and HIF-1α. Cell Cycle. 2011;10(10):1545–1547.
  • Robador PA, San Jose G, Rodríguez C, et al. HIF-1-mediated up-regulation of cardiotrophin-1 is involved in the survival response of cardiomyocytes to hypoxia. Cardiovasc Res. 2011;92(2):247–255.
  • Agani F, Jiang BH. Oxygen-independent regulation of HIF-1: novel involvement of PI3K/AKT/mTOR pathway in cancer. Curr Cancer Drug Targets. 2013;1;13(3):245–251.
  • Choe SS, Shin KC, Ka S, Lee YK, Chun JS, et al. Macrophage HIF-2α ameliorates adipose tissue inflammation and insulin resistance in obesity. Diabetes. 2014;63(10):3359–3371.
  • Lee YS, Kim JW, Osborne O, et al. Increased adipocyte O2 consumption triggers HIF-1α, causing inflammation and insulin resistance in obesity. Cell. 2014;157(6):1339–1352.
  • Liu Z, Xi R, Zhang Z, et al. 4-Hydroxyphenylacetic acid attenuated inflammation and edema via suppressing HIF-1α in seawater aspiration-induced lung injury in rats. Int J Mol Sci. 2014;15(7):12861–12884.
  • Suzuki A, Osanai T, Tanaka M, et al. Coupling factor 6 attenuates CXCR4 expression through the HIF-1α and c-Src pathways and promotes endothelial apoptosis and inflammation. Hypertens Res. 2014;37(8):708–715.
  • Scholz CC, Cavadas MA, Tambuwala MM, Hams E, et al. Regulation of IL-1β–induced NF-κB by hydroxylases links key hypoxic and inflammatory signaling pathways. Proc Natl Acad Sci USA. 2013;110(46):18490–18495.
  • Filippi I, Carraro F, Naldini A. Interleukin-1β Affects MDAMB231 Breast Cancer Cell Migration under Hypoxia: Role of HIF-1α and NFκB Transcription Factors. Mediators Inflamm. 2015;2015(789414):1–10.
  • Bollinger T, Gies S, Naujoks J, et al. HIF‐1α‐and hypoxia‐dependent immune responses in human CD4+ CD25high T cells and T helper 17 cells. J Leukoc Biol. 2014;96(2):305–312.
  • D'Ignazio L, Bandarra D, Rocha S. NF-κB and HIF crosstalk in immune responses. Febs J. 2016;283(3):413–424.
  • Zhu G, Tang Y, Geng N, et al. HIF-α/MIF and NF-κB/IL-6 axes contribute to the recruitment of CD11b + Gr-1+ myeloid cells in hypoxic microenvironment of HNSCC. Neoplasia. 2014;16(2):168–179.
  • Vasilopoulos Y, Sourli F, Zafiriou E, et al. High serum levels of HIF-1α in psoriatic patients correlate with an over-expression of IL-6. Cytokine. 2013;62(1):38–39.
  • Xing J, Lu J. HIF-1α activation attenuates IL-6 and TNF-α pathways in hippocampus of rats following transient global ischemia. Cell Physiol Biochem. 2016;39(2):511–520.
  • Choi SH, Kwon OJ, Park JY, et al. Inhibition of tumour angiogenesis and growth by small hairpin HIF‐1α and IL‐8 in hepatocellular carcinoma. Liver Int. 2014;34(4):632–642.
  • Bortolanza S, Bunuales M, Otano I, et al. Treatment of pancreatic cancer with an oncolytic adenovirus expressing interleukin-12 in Syrian hamsters. Mol Ther. 2009;17(4):614–622.
  • Velásquez SY, Killian D, Schulte J, et al. Short term hypoxia synergizes with interleukin 15 priming in driving glycolytic gene transcription and supports human natural killer cell activities. J Biol Chem. 2016;291(25):12960–12977.
  • Remels AH, Gosker HR, Verhees KJ, et al. TNF-α-induced NF-κB activation stimulates skeletal muscle glycolytic metabolism through activation of HIF-1α. Endocrinology. 2015 May;156(5):1770–1781.
  • Lv L, Yuan J, Huang T, et al. Stabilization of Snail by HIF-1α and TNF-α is required for hypoxia-induced invasion in prostate cancer PC3 cells. Mol Biol Rep. 2014;41(7):4573–4582.
  • Tang M, Tian Y, Li D, et al. TNF-α mediated increase of HIF-1α inhibits VASP expression, which reduces alveolar-capillary barrier function during acute lung injury (ALI). PLoS One. 2014;9(7):e102967.
  • Ghosh S, Gupta P, Sen E. TNFα driven HIF-1α-hexokinase II axis regulates MHC-I cluster stability through actin cytoskeleton. Exp Cell Res. 2016;340(1):116–124.
  • Huang CY, Hsieh YL, Ju DT, et al. Attenuation of magnesium sulfate on CoCl2-induced cell death by activating ERK1/2/MAPK and inhibiting HIF-1α via mitochondrial apoptotic signaling suppression in a neuronal cell line. Chin J Physiol. 2015;58(4):244–253.
  • Nys K, Van Laethem A, Michiels C, et al. A p38-HIF-1 pathway initiated by UVB irradiation is required to induce Noxa and apoptosis of human keratinocytes. Leuven (Belgium): InOncoforum; 2010.
  • Teng M, Jiang XP, Zhang Q, et al. Microtubular stability affects pVHL-mediated regulation of HIF-1alpha via the p38/MAPK pathway in hypoxic cardiomyocytes. PLoS One. 2012;7(4):e35017.
  • Lombaert N, Castrucci E, Decordier I, et al. Hard-metal (WC–Co) particles trigger a signaling cascade involving p38 MAPK, HIF-1α, HMOX1, and p53 activation in human PBMC. Arch Toxicol. 2013;87(2):259–268.
  • Zhang QL, Cui BR, Li HY, et al. MAPK and PI3K pathways regulate hypoxia-induced atrial natriuretic peptide secretion by controlling HIF-1 alpha expression in beating rabbit atria. Biochem Biophys Res Commun. 2013;438(3):507–512.
  • Yan L, Cao X, Zeng S, et al. Associations of proteins relevant to MAPK signaling pathway (p38MAPK-1, HIF-1 and HO-1) with coronary lesion characteristics and prognosis of peri-menopausal women. Lipids Health Dis. 2016;15(1):1–1.
  • Guo C, Hao LJ, Yang ZH, Chai R, et al. Deferoxamine-mediated up-regulation of HIF-1α prevents dopaminergic neuronal death via the activation of MAPK family proteins in MPTP-treated mice. Exp Neurol. 2016;280:13–23.
  • Befani CD, Vlachostergios PJ, Hatzidaki E, et al. Bortezomib represses HIF-1α protein expression and nuclear accumulation by inhibiting both PI3K/Akt/TOR and MAPK pathways in prostate cancer cells. J Mol Med (Berl). 2012;90(1):45–54.
  • Wang Y, Huang Y, Guan F, et al. Hypoxia-inducible factor-1alpha and MAPK co-regulate activation of hepatic stellate cells upon hypoxia stimulation. PLoS One. 2013;8(9):e74051.
  • Cheng YL, Choi Y, Seow WL, et al. Evidence that neuronal Notch-1 promotes JNK/c-Jun activation and cell death following ischemic stress. Brain Res. 2014;1586:193–202.
  • Song K, Li M, Xu XJ, et al. HIF-1α and GLUT1 gene expression is associated with chemoresistance of acute myeloid leukemia. Asian Pac J Cancer Prev. 2014;15(4):1823–1829.
  • Bosco MC, Varesio L. Dendritic cell reprogramming by the hypoxic environment. Immunobiology. 2012;217(12):1241–1249.
  • Filippi I, Morena E, Aldinucci C, et al. Short-term hypoxia enhances the migratory capability of dendritic cell through HIF-1α and PI3K/Akt pathway. J Cell Physiol. 2014;229(12):2067–2076.
  • Chieosilapatham P, Ikeda S, Ogawa H, et al. Tissue-specific regulation of innate immune responses by human cathelicidin LL-37. Curr Pharm Des. 2018;24(10):1079–1091.
  • Poitz DM, Augstein A, Gradehand C, et al. Regulation of the Hif-system by micro-RNA 17 and 20a – role during monocyte-to-macrophage differentiation. Mol Immunol. 2013;56(4):442–451.
  • Labiano S, Palazon A, Melero I. Immune response regulation in the tumor microenvironment by hypoxia. Semin Oncol. 2015;42(3):378–386.
  • Wan J, Wu W, Che Y, et al. Low dose photodynamic-therapy induce immune escape of tumor cells in a HIF-1α dependent manner through PI3K/Akt pathway. Int Immunopharmacol. 2015;28(1):44–51.
  • Coleman JW. Nitric oxide in immunity and inflammation. Int Immunopharmacol. 2001;1(8):1397–1406.
  • Bogdan C. Nitric oxide and the immune response. Nat Immunol. 2001;2(10):907–916.
  • Zhao T, Ren H, Jia L, et al. Inhibition of HIF-1α by PX-478 enhances the anti-tumor effect of gemcitabine by inducing immunogenic cell death in pancreatic ductal adenocarcinoma. Oncotarget. 2015;6(4):2250–2262.
  • Zudaire E, Portal‐Núñez S, Cuttitta F. The central role of adrenomedullin in host defense. J Leukoc Biol. 2006;80(2):237–244.
  • Patel P, Mishra A, Sheikh AA, et al. Adrenomedullin: a novel peptide hormone. A review. J Pharmacogn Phytochem. 2017;6:2068–2073.
  • Koh HS, Chang CY, Jeon SB, et al. The HIF-1/glial TIM-3 axis controls inflammation-associated brain damage under hypoxia. Nat Commun. 2015;6(1):1–5.
  • Tao JH, Barbi J, Pan F. Hypoxia-inducible factors in T lymphocyte differentiation and function. A review in the theme: cellular responses to hypoxia. Am J Physiol Cell Physiol. 2015;309(9):C580–C589.
  • Doedens AL, Phan AT, Stradner MH, et al. Hypoxia-inducible factors enhance the effector responses of CD8+ T cells to persistent antigen. Nat Immunol. 2013;14(11):1173–1182.