ER Stress, UPR Activation and the Inflammatory Response to Viral Infection
Abstract
:1. Viruses, PPRs, and Inflammation
2. Viruses, ER Stress, UPR Activation and Inflammation
3. UPR and PRR Cross-Talk
4. Possible Consequences of Excessive Inflammation in Response to Viral Infection
5. Targeting UPR or PRR Signaling to Mitigate Excessive Inflammation in the Course of Viral Infections
Virus | UPR/UPR Arm | Inflammatory Molecules | References |
---|---|---|---|
Hepatitis B virus (HBV) | eIF2α/ATF4 | Cox-2 | [40] |
Dengue virus (DENV) | PERK/Nrf2 | TNF-α | [41] |
Kaposi’s sarcoma-associated herpesvirus (KSHV) | IRE1a | TNF-α, IL-6, IL-10, IL-8, VEGF | [33] |
PERK | CCL-2 | [33] | |
SARS-CoV-2 | ER stress/UPR | IL-6, IL-1b | [36] |
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Lester, S.N.; Li, K. Toll-like receptors in antiviral innate immunity. J. Mol. Biol. 2014, 426, 1246–1264. [Google Scholar] [CrossRef] [PubMed]
- Sabbah, A.; Chang, T.H.; Harnack, R.; Frohlich, V.; Tominaga, K.; Dube, P.H.; Xiang, Y.; Bose, S. Activation of innate immune antiviral responses by Nod2. Nat. Immunol. 2009, 10, 1073–1080. [Google Scholar] [CrossRef]
- Almanza, A.; Carlesso, A.; Chintha, C.; Creedican, S.; Doultsinos, D.; Leuzzi, B.; Luis, A.; McCarthy, N.; Montibeller, L.; More, S.; et al. Endoplasmic reticulum stress signalling—from basic mechanisms to clinical applications. FEBS J. 2019, 286, 241–278. [Google Scholar] [CrossRef] [PubMed]
- Takeuchi, O.; Akira, S. Pattern recognition receptors and inflammation. Cell 2010, 140, 805–820. [Google Scholar] [CrossRef] [Green Version]
- Larsen, S.B.; Cowley, C.J.; Fuchs, E. Epithelial cells: Liaisons of immunity. Curr. Opin. Immunol. 2020, 62, 45–53. [Google Scholar] [CrossRef] [PubMed]
- Reverendo, M.; Mendes, A.; Arguello, R.J.; Gatti, E.; Pierre, P. At the crossway of ER-stress and proinflammatory responses. FEBS J. 2019, 286, 297–310. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Corazzari, M.; Gagliardi, M.; Fimia, G.M.; Piacentini, M. Endoplasmic Reticulum Stress, Unfolded Protein Response, and Cancer Cell Fate. Front. Oncol. 2017, 7, 78. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chan, S.W. The unfolded protein response in virus infections. Front. Microbiol. 2014, 5, 518. [Google Scholar] [CrossRef]
- Choi, J.A.; Song, C.H. Insights Into the Role of Endoplasmic Reticulum Stress in Infectious Diseases. Front. Immunol. 2019, 10, 3147. [Google Scholar] [CrossRef] [Green Version]
- Hetz, C.; Zhang, K.; Kaufman, R.J. Mechanisms, regulation and functions of the unfolded protein response. Nat. Rev. Mol. Cell Biol. 2020, 21, 421–438. [Google Scholar] [CrossRef]
- Cirone, M. Perturbation of bulk and selective macroautophagy, abnormal UPR activation and their interplay pave the way to immune dysfunction, cancerogenesis and neurodegeneration in ageing. Ageing Res. Rev. 2020, 58, 101026. [Google Scholar] [CrossRef]
- Cirone, M. EBV and KSHV Infection Dysregulates Autophagy to Optimize Viral Replication, Prevent Immune Recognition and Promote Tumorigenesis. Viruses 2018, 10, 599. [Google Scholar] [CrossRef] [Green Version]
- Santarelli, R.; Granato, M.; Pentassuglia, G.; Lacconi, V.; Gilardini Montani, M.S.; Gonnella, R.; Tafani, M.; Torrisi, M.R.; Faggioni, A.; Cirone, M. KSHV reduces autophagy in THP-1 cells and in differentiating monocytes by decreasing CAST/calpastatin and ATG5 expression. Autophagy 2016, 12, 2311–2325. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gilardini Montani, M.S.; Santarelli, R.; Granato, M.; Gonnella, R.; Torrisi, M.R.; Faggioni, A.; Cirone, M. EBV reduces autophagy, intracellular ROS and mitochondria to impair monocyte survival and differentiation. Autophagy 2019, 15, 652–667. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Romeo, M.A.; Gilardini Montani, M.S.; Benedetti, R.; Giambelli, L.; D’Aprile, R.; Gaeta, A.; Faggioni, A.; Cirone, M. The cross-talk between STAT1/STAT3 and ROS up-regulates PD-L1 and promotes the release of pro-inflammatory/immune suppressive cytokines in primary monocytes infected by HHV-6B. Virus Res. 2021, 292, 198231. [Google Scholar] [CrossRef] [PubMed]
- Romeo, M.A.; Gilardini Montani, M.S.; Falcinelli, L.; Gaeta, A.; Nazzari, C.; Faggioni, A.; Cirone, M. HHV-6B reduces autophagy and induces ER stress in primary monocytes impairing their survival and differentiation into dendritic cells. Virus Res. 2019, 273, 197757. [Google Scholar] [CrossRef] [PubMed]
- Kaneko, M.; Niinuma, Y.; Nomura, Y. Activation signal of nuclear factor-kappa B in response to endoplasmic reticulum stress is transduced via IRE1 and tumor necrosis factor receptor-associated factor 2. Biol. Pharm. Bull. 2003, 26, 931–935. [Google Scholar] [CrossRef] [Green Version]
- Chen, L.; Deng, H.; Cui, H.; Fang, J.; Zuo, Z.; Deng, J.; Li, Y.; Wang, X.; Zhao, L. Inflammatory responses and inflammation-associated diseases in organs. Oncotarget 2018, 9, 7204–7218. [Google Scholar] [CrossRef] [Green Version]
- Kmonickova, E.; Canova, N.K.; Farghali, H.; Holy, A.; Zidek, Z. Modulator of intracellular Ca(2+), thapsigargin, interferes with in vitro secretion of cytokines and nitric oxide. Biomed. Pap. Med. Fac. Univ. Palacky Olomouc Czech. Repub. 2005, 149, 321–324. [Google Scholar] [CrossRef] [Green Version]
- Mahameed, M.; Wilhelm, T.; Darawshi, O.; Obiedat, A.; Tommy, W.S.; Chintha, C.; Schubert, T.; Samali, A.; Chevet, E.; Eriksson, L.A.; et al. The unfolded protein response modulators GSK2606414 and KIRA6 are potent KIT inhibitors. Cell Death Dis. 2019, 10, 300. [Google Scholar] [CrossRef]
- Smith, J.A. Regulation of Cytokine Production by the Unfolded Protein Response; Implications for Infection and Autoimmunity. Front. Immunol. 2018, 9, 422. [Google Scholar] [CrossRef] [PubMed]
- Janssens, S.; Pulendran, B.; Lambrecht, B.N. Emerging functions of the unfolded protein response in immunity. Nat. Immunol. 2014, 15, 910–919. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kim, S.; Joe, Y.; Surh, Y.J.; Chung, H.T. Differential Regulation of Toll-Like Receptor-Mediated Cytokine Production by Unfolded Protein Response. Oxid. Med. Cell. Longev. 2018, 2018, 9827312. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Martinon, F.; Chen, X.; Lee, A.H.; Glimcher, L.H. TLR activation of the transcription factor XBP1 regulates innate immune responses in macrophages. Nat. Immunol. 2010, 11, 411–418. [Google Scholar] [CrossRef]
- Cullinan, S.B.; Diehl, J.A. Coordination of ER and oxidative stress signaling: The PERK/Nrf2 signaling pathway. Int. J. Biochem. Cell Biol. 2006, 38, 317–332. [Google Scholar] [CrossRef]
- Meares, G.P.; Liu, Y.; Rajbhandari, R.; Qin, H.; Nozell, S.E.; Mobley, J.A.; Corbett, J.A.; Benveniste, E.N. PERK-dependent activation of JAK1 and STAT3 contributes to endoplasmic reticulum stress-induced inflammation. Mol. Cell. Biol. 2014, 34, 3911–3925. [Google Scholar] [CrossRef] [Green Version]
- Lin, X.; Wang, R.; Zou, W.; Sun, X.; Liu, X.; Zhao, L.; Wang, S.; Jin, M. The Influenza Virus H5N1 Infection Can Induce ROS Production for Viral Replication and Host Cell Death in A549 Cells Modulated by Human Cu/Zn Superoxide Dismutase (SOD1) Overexpression. Viruses 2016, 8, 13. [Google Scholar] [CrossRef] [Green Version]
- Yoshikawa, T.; Hill, T.; Li, K.; Peters, C.J.; Tseng, C.T. Severe acute respiratory syndrome (SARS) coronavirus-induced lung epithelial cytokines exacerbate SARS pathogenesis by modulating intrinsic functions of monocyte-derived macrophages and dendritic cells. J. Virol. 2009, 83, 3039–3048. [Google Scholar] [CrossRef] [Green Version]
- Bonizzoli, M.; Arvia, R.; di Valvasone, S.; Liotta, F.; Zakrzewska, K.; Azzi, A.; Peris, A. Human herpesviruses respiratory infections in patients with acute respiratory distress (ARDS). Med. Microbiol. Immunol. 2016, 205, 371–379. [Google Scholar] [CrossRef]
- Foley, J.H.; Conway, E.M. Cross Talk Pathways Between Coagulation and Inflammation. Circ. Res. 2016, 118, 1392–1408. [Google Scholar] [CrossRef]
- Evans, C.E.; Zhao, Y.Y. Impact of thrombosis on pulmonary endothelial injury and repair following sepsis. Am. J. Physiol. Lung Cell. Mol. Physiol. 2017, 312, L441–L451. [Google Scholar] [CrossRef]
- Song, P.; Li, W.; Xie, J.; Hou, Y.; You, C. Cytokine storm induced by SARS-CoV-2. Clin. Chim. Acta 2020, 509, 280–287. [Google Scholar] [CrossRef]
- Gilardini Montani, M.S.; Falcinelli, L.; Santarelli, R.; Granato, M.; Romeo, M.A.; Cecere, N.; Gonnella, R.; D’Orazi, G.; Faggioni, A.; Cirone, M. KSHV infection skews macrophage polarisation towards M2-like/TAM and activates Ire1 alpha-XBP1 axis up-regulating pro-tumorigenic cytokine release and PD-L1 expression. Br. J. Cancer 2020, 123, 298–306. [Google Scholar] [CrossRef]
- Rojas-Rivera, D.; Delvaeye, T.; Roelandt, R.; Nerinckx, W.; Augustyns, K.; Vandenabeele, P.; Bertrand, M.J.M. When PERK inhibitors turn out to be new potent RIPK1 inhibitors: Critical issues on the specificity and use of GSK2606414 and GSK2656157. Cell Death Differ. 2017, 24, 1100–1110. [Google Scholar] [CrossRef]
- Yu, M.; Wang, H.; Ding, A.; Golenbock, D.T.; Latz, E.; Czura, C.J.; Fenton, M.J.; Tracey, K.J.; Yang, H. HMGB1 signals through toll-like receptor (TLR) 4 and TLR2. Shock 2006, 26, 174–179. [Google Scholar] [CrossRef]
- Hsu, A.C.Y.; Wang, G.; Reid, A.T.; Veerati, P.C.; Pathinayake, P.S.; Daly, K.; Mayall, J.R.; Hansbro, P.M.; Horvat, J.C.; Wang, F.; et al. SARS-CoV-2 Spike protein promotes hyper-inflammatory response that can be ameliorated by Spike-antagonistic peptide and FDA-approved ER stress and MAP kinase inhibitors in vitro. Biorxiv 2020. [Google Scholar] [CrossRef]
- Boukhvalova, M.S.; Mortensen, E.; Mbaye, A.; Lopez, D.; Kastrukoff, L.; Blanco, J.C.G. Herpes Simplex Virus 1 Induces Brain Inflammation and Multifocal Demyelination in the Cotton Rat Sigmodon hispidus. J. Virol. 2019, 94. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Khan, G. Epstein-Barr virus and the germinal center B cells. Exp. Hematol. 2006, 34, 695–696. [Google Scholar] [CrossRef] [PubMed]
- Wu, Z.X.; Chen, F.S.; Zhou, X.L.; Huang, Q.; Zhang, S.A.; Wu, H.C.; Cai, L.R.; Zeng, Z.Y.; Li, Y.H.; Li, D.L. Tenofovir and telbivudine combination therapy rapidly decreases viral loads in immune-tolerant chronic hepatitis B patients awaiting assisted reproduction: An open-label, randomized, controlled study. Eur. J. Gastroenterol. Hepatol. 2019, 31, 832–835. [Google Scholar] [CrossRef] [PubMed]
- Cho, H.K.; Kim, S.Y.; Kyaw, Y.Y.; Win, A.A.; Koo, S.H.; Kim, H.H.; Cheong, J. HBx induces the proliferation of hepatocellular carcinoma cells via AP1 over-expressed as a result of ER stress. Biochem. J. 2015, 466, 115–121. [Google Scholar] [CrossRef]
- Cheng, Y.L.; Lin, Y.S.; Chen, C.L.; Tsai, T.T.; Tsai, C.C.; Wu, Y.W.; Ou, Y.D.; Chu, Y.Y.; Wang, J.M.; Yu, C.Y.; et al. Activation of Nrf2 by the dengue virus causes an increase in CLEC5A, which enhances TNF-alpha production by mononuclear phagocytes. Sci. Rep. 2016, 6, 32000. [Google Scholar] [CrossRef] [PubMed] [Green Version]
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Cirone, M. ER Stress, UPR Activation and the Inflammatory Response to Viral Infection. Viruses 2021, 13, 798. https://doi.org/10.3390/v13050798
Cirone M. ER Stress, UPR Activation and the Inflammatory Response to Viral Infection. Viruses. 2021; 13(5):798. https://doi.org/10.3390/v13050798
Chicago/Turabian StyleCirone, Mara. 2021. "ER Stress, UPR Activation and the Inflammatory Response to Viral Infection" Viruses 13, no. 5: 798. https://doi.org/10.3390/v13050798
APA StyleCirone, M. (2021). ER Stress, UPR Activation and the Inflammatory Response to Viral Infection. Viruses, 13(5), 798. https://doi.org/10.3390/v13050798