Nuclear translocation of HIF-1α induced by influenza A (H1N1) infection is critical to the production of proinflammatory cytokines

References

• Novel Swine-Origin Influenza AVIT, Dawood FS, Jain Set al.Emergence of a novel swine-origin influenza A (H1N1) virus in humans. N Engl J Med 2009;360: 2605–2615.
   Google Scholar
• Komissarov A, Fadeev A, Sergeeva Met al.Rapid spread of influenza A(H1N1)pdm09 viruses with a new set of specific mutations in the internal genes in the beginning of 2015/2016 epidemic season in Moscow and Saint Petersburg (Russian Federation). Influenza Other Respir Viruses 2016;10: 247–253.
   PubMed Web of Science ®Google Scholar
• Zhu W, Zhang H, Xiang Xet al.Reassortant Eurasian avian-like influenza A(H1N1) Virus from a severely ill child, Hunan Province, China, 2015. Emerg Infect Dis 2016;22: 1930–1936.
   PubMed Web of Science ®Google Scholar
• Berhane Y, Ojkic D, Pople Net al.Reoccurrence of suspected human-to-Turkey transmission of H1N1 Pandemic 2009 Virus in Turkey breeder flocks in Ontario and Manitoba, 2016. Transbound Emerg Dis 2016;63: 590–594.
   PubMed Web of Science ®Google Scholar
• Writing Committee of the WHO Consultation on Clinical Aspects of Pandemic (H1N1) 2009 Influenza, Bautista E, Chotpitayasunondh T. N Engl J Med 2010;362: 1708–1719.
   PubMed Web of Science ®Google Scholar
• Hendrickson CM, Matthay MA.Viral pathogens and acute lung injury: investigations inspired by the SARS epidemic and the 2009 H1N1 influenza pandemic. Semin Respir Crit Care Med 2013;34: 475–486.
   PubMed Web of Science ®Google Scholar
• Poulakou G, Perez M, Rello J.Severe acute respiratory infections in the postpandemic era of H1N1. Curr Opin Crit Care 2012;18: 441–450.
   PubMed Web of Science ®Google Scholar
• Tscherne DM, Garcia-Sastre A.Virulence determinants of pandemic influenza viruses. J Clin Invest 2011;121: 6–13.
   PubMed Web of Science ®Google Scholar
• Woo PC, Tung ET, Chan KHet al.Cytokine profiles induced by the novel swine-origin influenza A/H1N1 virus: implications for treatment strategies. J Infect Dis 2010;201: 346–353.
   PubMed Web of Science ®Google Scholar
• Hui KP, Lee SM, Cheung CYet al.Induction of proinflammatory cytokines in primary human macrophages by influenza A virus (H5N1) is selectively regulated by IFN regulatory factor 3 and p38 MAPK. J Immunol 2009;182: 1088–1098.
   PubMed Web of Science ®Google Scholar
• Chi Y, Zhu Y, Wen Tet al.Cytokine and chemokine levels in patients infected with the novel avian influenza A (H7N9) virus in China. J Infect Dis 2013;208: 1962–1967.
   PubMed Web of Science ®Google Scholar
• Bian JR, Nie W, Zang YSet al.Clinical aspects and cytokine response in adults with seasonal influenza infection. Int J Clin Exp Med 2014;7: 5593–5602.
   PubMed Web of Science ®Google Scholar
• Hagau N, Slavcovici A, Gonganau DNet al.Clinical aspects and cytokine response in severe H1N1 influenza A virus infection. Crit Care 2010;14: R203.
   PubMed Web of Science ®Google Scholar
• Salihefendic N, Zildzic M, Ahmetagic S.Acute respiratory distress syndrome (ARDS) from endemic influenza A/H1N1: prehospital management. Med Arch 2015;69: 62–63.
   PubMedGoogle Scholar
• Wang GL, Jiang BH, Rue EAet al.Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc Natl Acad Sci USA 1995;92: 5510–5514.
   PubMed Web of Science ®Google Scholar
• Jaakkola P, Mole DR, Tian YMet al.Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 2001;292: 468–472.
   PubMed Web of Science ®Google Scholar
• Hong SS, Lee H, Kim KW.HIF-1alpha: a valid therapeutic target for tumor therapy. Cancer Res Treat 2004;36: 343–353.
   PubMedGoogle Scholar
• Konisti S, Kiriakidis S, Paleolog EM.Hypoxia—a key regulator of angiogenesis and inflammation in rheumatoid arthritis. Nat Rev Rheumatol 2012;8: 153–162.
   PubMed Web of Science ®Google Scholar
• Rohwer N, Zasada C, Kempa Set al.The growing complexity of HIF-1alpha's role in tumorigenesis: DNA repair and beyond. Oncogene 2013;32: 3569–3576.
   PubMed Web of Science ®Google Scholar
• Chen S, Okahara F, Osaki Net al.Increased GIP signaling induces adipose inflammation via a HIF-1alpha-dependent pathway and impairs insulin sensitivity in mice. Am J Physiol Endocrinol Metab 2015;308: E414–E425.
   PubMed Web of Science ®Google Scholar
• Sinha S, Koul N, Dixit Det al.IGF-1 induced HIF-1alpha-TLR9 cross talk regulates inflammatory responses in glioma. Cell Signal 2011;23: 1869–1875.
   PubMed Web of Science ®Google Scholar
• Zampell JC, Yan A, Avraham Tet al.HIF-1alpha coordinates lymphangiogenesis during wound healing and in response to inflammation. FASEB J 2012;26: 1027–1039.
   PubMed Web of Science ®Google Scholar
• Yoo YG, Oh SH, Park ESet al.Hepatitis B virus X protein enhances transcriptional activity of hypoxia-inducible factor-1alpha through activation of mitogen-activated protein kinase pathway. J Biol Chem 2003;278: 39076–39084.
   PubMed Web of Science ®Google Scholar
• Yoo YG, Cho S, Park Set al.The carboxy-terminus of the hepatitis B virus X protein is necessary and sufficient for the activation of hypoxia-inducible factor-1alpha. FEBS Lett 2004;577: 121–126.
   PubMed Web of Science ®Google Scholar
• Moin SM, Chandra V, Arya Ret al.The hepatitis E virus ORF3 protein stabilizes HIF-1alpha and enhances HIF-1-mediated transcriptional activity through p300/CBP. Cell Microbiol 2009;11: 1409–1421.
   PubMed Web of Science ®Google Scholar
• Cai QL, Knight JS, Verma SCet al.EC5S ubiquitin complex is recruited by KSHV latent antigen LANA for degradation of the VHL and p53 tumor suppressors. PLoS Pathog 2006;2: e116.
   PubMed Web of Science ®Google Scholar
• Mabjeesh NJ, Escuin D, LaVallee TMet al.2ME2 inhibits tumor growth and angiogenesis by disrupting microtubules and dysregulating HIF. Cancer Cell 2003;3: 363–375.
   PubMed Web of Science ®Google Scholar
• Deshmane SL, Mukerjee R, Fan Set al.Activation of the oxidative stress pathway by HIV-1 Vpr leads to induction of hypoxia-inducible factor 1alpha expression. J Biol Chem 2009;284: 11364–11373.
   PubMed Web of Science ®Google Scholar
• Tolnay AE, Baskin CR, Tumpey TMet al.Extrapulmonary tissue responses in cynomolgus macaques (Macaca fascicularis) infected with highly pathogenic avian influenza A (H5N1) virus. Arch Virol 2010;155: 905–914.
   PubMed Web of Science ®Google Scholar
• Topfer L, Menk M, Weber-Carstens Set al.Influenza A (H1N1) vs non-H1N1 ARDS: analysis of clinical course. J Crit Care 2014;29: 340–346.
   PubMed Web of Science ®Google Scholar
• Traylor ZP, Aeffner F, Davis IC.Influenza A H1N1 induces declines in alveolar gas exchange in mice consistent with rapid post-infection progression from acute lung injury to ARDS. Influenza Other Respir Viruses 2013;7: 472–479.
   PubMed Web of Science ®Google Scholar
• Wanderer AA.Hypoxia and inflammation. N Engl J Med 2011;364: 1976, author reply 1977.
   PubMed Web of Science ®Google Scholar
• Huang LE, Gu J, Schau Met al.Regulation of hypoxia-inducible factor 1alpha is mediated by an O2-dependent degradation domain via the ubiquitin-proteasome pathway. Proc Natl Acad Sci USA 1998;95: 7987–7992.
   PubMed Web of Science ®Google Scholar
• Chandel NS, McClintock DS, Feliciano CEet al.Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1alpha during hypoxia: a mechanism of O2 sensing. J Biol Chem 2000;275: 25130–25138.
   PubMed Web of Science ®Google Scholar
• Cramer T, Yamanishi Y, Clausen BEet al.HIF-1alpha is essential for myeloid cell-mediated inflammation. Cell 2003;112: 645–657.
   PubMed Web of Science ®Google Scholar
• Peyssonaux C, Johnson RS.An unexpected role for hypoxic response: oxygenation and inflammation. Cell Cycle 2004;3: 168–171.
   PubMed Web of Science ®Google Scholar
• Lall H, Coughlan K, Sumbayev VV.HIF-1alpha protein is an essential factor for protection of myeloid cells against LPS-induced depletion of ATP and apoptosis that supports Toll-like receptor 4-mediated production of IL-6. Mol Immunol 2008;45: 3045–3049.
   PubMed Web of Science ®Google Scholar
• Zhou H, Chen X, Zhang WMet al.HIF-1alpha inhibition reduces nasal inflammation in a murine allergic rhinitis model. PLoS One 2012;7: e48618.
   PubMed Web of Science ®Google Scholar
• Xing J, Lu J.HIF-1alpha activation attenuates IL-6 and TNF-alpha Pathways in hippocampus of rats following transient global ischemia. Cell Physiol Biochem 2016;39: 511–520.
   PubMedGoogle Scholar
• Gao X, Li Y, Wang Het al.Inhibition of HIF-1alpha decreases expression of pro- inflammatory IL-6 and TNF-alpha in diabetic retinopathy. Acta Ophthalmol 2016 10.1111/aos.13096.
   Web of Science ®Google Scholar
• Palazon A, Goldrath AW, Nizet Vet al.HIF transcription factors, inflammation, and immunity. Immunity 2014;41: 518–528.
   PubMed Web of Science ®Google Scholar
• Blouin CC, Page EL, Soucy GMet al.Hypoxic gene activation by lipopolysaccharide in macrophages: implication of hypoxia-inducible factor 1alpha. Blood 2004;103: 1124–1130.
   PubMed Web of Science ®Google Scholar
• Ding Q, Zhao L, Guo Het al.The nucleocytoplasmic transport of viral proteins. Virol Sin 2010;25: 79–85.
   PubMedGoogle Scholar
• Christie M, Chang CW, Rona Get al.Structural biology and regulation of protein import into the nucleus. J Mol Biol 2016;428 (10 Pt A): 2060–2090.
   PubMed Web of Science ®Google Scholar
• Chachami G, Paraskeva E, Mingot JMet al.Transport of hypoxia-inducible factor HIF-1alpha into the nucleus involves importins 4 and 7. Biochem Biophys Res Commun 2009;390: 235–240.
   PubMed Web of Science ®Google Scholar
• Hudjetz B, Gabriel G.Human-like PB2 627 K influenza virus polymerase activity is regulated by importin-alpha1 and -alpha7. PLoS Pathog 2012;8: e1002488.
   PubMed Web of Science ®Google Scholar
• Signorelli S, Jennings P, Leonard MOet al.Differential effects of hypoxic stress in alveolar epithelial cells and microvascular endothelial cells. Cell Physiol Biochem 2010;25: 135–144.
   PubMedGoogle Scholar
• Lam SY, Liu Y, Ng KMet al.Chronic intermittent hypoxia induces local inflammation of the rat carotid body via functional upregulation of proinflammatory cytokine pathways. Histochem Cell Biol 2012;137: 303–317.
   PubMed Web of Science ®Google Scholar
• Angelo MF, Aguirre A, Aviles Reyes RXet al.The proinflammatory RAGE/NF-kappaB pathway is involved in neuronal damage and reactive gliosis in a model of sleep apnea by intermittent hypoxia. PLoS One 2014;9: e107901.
   PubMed Web of Science ®Google Scholar
• Pierobon D, Bosco MC, Blengio Fet al.Chronic hypoxia reprograms human immature dendritic cells by inducing a proinflammatory phenotype and TREM-1 expression. Eur J Immunol 2013;43: 949–966.
   PubMed Web of Science ®Google Scholar
• Whyte MK, Walmsley SR.The regulation of pulmonary inflammation by the hypoxia-inducible factor-hydroxylase oxygen-sensing pathway. Ann Am Thorac Soc 2014;11 (Suppl 5): S271–S276.
   PubMedGoogle Scholar
• Frohlich S, Boylan J, McLoughlin P.Hypoxia-induced inflammation in the lung: a potential therapeutic target in acute lung injury? Am J Respir Cell Mol Biol 2013;48: 271–279.
   PubMed Web of Science ®Google Scholar
• Liu Z, Xi R, Zhang Zet al.4-hydroxyphenylacetic acid attenuated inflammation and edema via suppressing HIF-1alpha in seawater aspiration-induced lung injury in rats. Int J Mol Sci 2014;15: 12861–12884.
   PubMed Web of Science ®Google Scholar
• Huang X, He Z, Jiang Xet al.Folic acid represses hypoxia-induced inflammation in THP-1 cells through inhibition of the PI3K/Akt/HIF-1alpha pathway. PLoS One 2016;11: e0151553.
   PubMed Web of Science ®Google Scholar
• Kim HJ, Jeong JS, Kim SRet al.Inhibition of endoplasmic reticulum stress alleviates lipopolysaccharide-induced lung inflammation through modulation of NF-kappaB/HIF-1alpha signaling pathway. Sci Rep 2013;3: 1142.
   PubMed Web of Science ®Google Scholar
• Kamali A, Holodniy M.Influenza treatment and prophylaxis with neuraminidase inhibitors: a review. Infect Drug Resist 2013;6: 187–198.
   PubMedGoogle Scholar
• Viasus D, Pano-Pardo JR, Cordero Eet al.Effect of immunomodulatory therapies in patients with pandemic influenza A (H1N1) 2009 complicated by pneumonia. J Infect 2011;62: 193–199.
   PubMed Web of Science ®Google Scholar
• Oldstone MB, Rosen H.Cytokine storm plays a direct role in the morbidity and mortality from influenza virus infection and is chemically treatable with a single sphingosine-1-phosphate agonist molecule. Curr Top Microbiol Immunol 2014;378: 129–147.
   PubMed Web of Science ®Google Scholar
• Uematsu T, Fujita T, Nakaoka HJet al.Mint3/Apba3 depletion ameliorates severe murine influenza pneumonia and macrophage cytokine production in response to the influenza virus. Sci Rep 2016;6: 37815.
   PubMed Web of Science ®Google Scholar