Immune determinants of COVID-19 disease presentation and severity (original) (raw)

• van Doremalen, N. et al. Aerosol and surface stability of SARS-CoV-2 as compared with SARS-CoV-1. N. Engl. J. Med. 382, 1564–1567 (2020).
  Article PubMed Google Scholar
• Huang, C. et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet 395, 497–506 (2020).
  Article CAS PubMed PubMed Central Google Scholar
• Wölfel, R. et al. Virological assessment of hospitalized patients with COVID-2019. Nature 581, 465–469 (2020).
  Article PubMed CAS Google Scholar
• Moghadas, S. M. et al. The implications of silent transmission for the control of COVID-19 outbreaks. Proc. Natl Acad. Sci. USA 117, 17513–17515 (2020).
  Article CAS PubMed PubMed Central Google Scholar
• Brodin, P. Why is COVID‐19 so mild in children? Acta Paediatr. 109, 1082–1083 (2020).
  Article CAS PubMed Google Scholar
• Takahashi, T. et al. Sex differences in immune responses that underlie COVID-19 disease outcomes. Nature 588, 315–320 (2020).
  Article CAS PubMed PubMed Central Google Scholar
• Liu, Y. et al. Viral dynamics in mild and severe cases of COVID-19. Lancet Infect. Dis. 20, 656–657 (2020).
  Article CAS PubMed PubMed Central Google Scholar
• Smith, J. C. et al. Cigarette smoke exposure and inflammatory signaling increase the expression of the SARS-CoV-2 receptor ACE2 in the respiratory tract. Dev. Cell 53, 514–529(2020).
  Article CAS PubMed PubMed Central Google Scholar
• Mehta, P. et al. COVID-19: consider cytokine storm syndromes and immunosuppression. Lancet 395, 1033–1034 (2020).
  Article CAS PubMed PubMed Central Google Scholar
• Cao, X. COVID-19: immunopathology and its implications for therapy. Nat. Rev. Immunol. 20, 269–270 (2020).
  Article CAS PubMed PubMed Central Google Scholar
• Mathew, D. et al. Deep immune profiling of COVID-19 patients reveals distinct immunotypes with implications for therapeutic interventions. Science 369, eabc8511 (2020).
  Article CAS PubMed PubMed Central Google Scholar
• Lucas, C. et al. Longitudinal immunological analyses reveal inflammatory misfiring in severe COVID-19 patients. Nature 584, 463–469 (2020).
  Article CAS PubMed PubMed Central Google Scholar
• Rodriguez, L. et al. Systems-level immunomonitoring from acute to recovery phase of severe COVID-19. Cell Rep. Med. 1, 100078 (2020).
  Article PubMed PubMed Central Google Scholar
• Carfì, A. et al. Persistent symptoms in patients after acute COVID-19. JAMA 324, 603–605 (2020).
  Article PubMed PubMed Central CAS Google Scholar
• Dennis, A. et al. Multi-organ impairment in low-risk individuals with long COVID. Preprint at medRxiv https://doi.org/10.1101/2020.10.14.20212555 (2020).
• Ludvigsson, J. F. Case report and systematic review suggest that children may experience similar long‐term effects to adults after clinical COVID‐19. Acta Paediatr. https://doi.org/10.1111/apa.15673 (2020).
• Davido, B., Seang, S., Tubiana, R. & de Truchis, P. Post-COVID-19 chronic symptoms: a post-infectious entity? Clin. Microbiol. Infec. 26, 1448–1449 (2020).
  Article CAS Google Scholar
• Guillot, X., Ribera, A. & Gasque, P. Chikungunya-induced arthritis in Reunion Island: a long-term observational follow-up study showing frequently persistent joint symptoms, some cases of persistent chikungunya immunoglobulin M positivity, and no anticyclic citrullinated peptide seroconversion after 13 years. J. Infect. Dis. 222, 1740–1744 (2020).
  Article PubMed Google Scholar
• Clark, D. V. et al. Long-term sequelae after Ebola virus disease in Bundibugyo, Uganda: a retrospective cohort study. Lancet Infect. Dis. 15, 905–912 (2015).
  Article PubMed Google Scholar
• Hickie, I. et al. Post-infective and chronic fatigue syndromes precipitated by viral and non-viral pathogens: prospective cohort study. BMJ 333, 575 (2006).
  Article PubMed PubMed Central Google Scholar
• Rodriguez, L. S. T. et al. Achieving symptom relief in patients with Myalgic encephalomyelitis by targeting the neuro-immune interface and inducing disease tolerance. Preprint at bioRxiv https://doi.org/10.1101/2020.02.20.958249 (2020).
• Whittaker, E. et al. Clinical characteristics of 58 children with a pediatric inflammatory multisystem syndrome temporally associated with SARS-CoV-2. JAMA 324, 259–269 (2020).
  Article CAS PubMed PubMed Central Google Scholar
• Belot, A. et al. SARS-CoV-2-related paediatric inflammatory multisystem syndrome, an epidemiological study, France, 1 March to 17 May 2020. Euro. Surveill. 25, 2001010 (2020).
  Article PubMed Central Google Scholar
• Toubiana, J. et al. Kawasaki-like multisystem inflammatory syndrome in children during the COVID-19 pandemic in Paris, France: prospective observational study. BMJ 369, m2094 (2020).
  Article PubMed PubMed Central Google Scholar
• Morris, S. B. et al. Case series of multisystem inflammatory syndrome in adults associated with SARS-CoV-2 infection—United Kingdom and United States, March–August 2020. Morbidity Mortal. Wkly Rep. 69, 1450–1456 (2020).
  Article CAS Google Scholar
• Marrani, E., Burns, J. C. & Cimaz, R. How should we classify Kawasaki disease? Front Immunol. 9, 2974 (2018).
  Article CAS PubMed PubMed Central Google Scholar
• Corwin, D. J. et al. Distinguishing multisystem inflammatory syndrome in children from Kawasaki disease and benign inflammatory illnesses in the SARS-CoV-2 pandemic. Pediatr. Emerg. Care 36, 554–558 (2020).
  Article PubMed PubMed Central Google Scholar
• Diorio, C. et al. Multisystem inflammatory syndrome in children and COVID-19 are distinct presentations of SARS-CoV-2. J. Clin. Invest. 130, 5967–5975 (2020).
  Article CAS PubMed PubMed Central Google Scholar
• Consiglio, C. R. et al. The immunology of multisystem inflammatory syndrome in children with COVID-19. Cell 183, 968–981 (2020).
  Article CAS PubMed PubMed Central Google Scholar
• Consiglio, C. R. & Brodin, P. Stressful beginnings with long-term consequences. Cell 180, 820–821 (2020).
  Article CAS PubMed Google Scholar
• Gruber, C. et al. Mapping systemic inflammation and antibody responses in multisystem inflammatory syndrome in children (MIS-C). Cell 183, 982–995 (2020).
  Article CAS PubMed PubMed Central Google Scholar
• Hoffmann, M. et al. SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor. Cell 181, 271–280 (2020).
  Article CAS PubMed PubMed Central Google Scholar
• Xu, H. et al. High expression of ACE2 receptor of 2019-nCoV on the epithelial cells of oral mucosa. Int. J. Oral. Sci. 12, 8 (2020).
  Article CAS PubMed PubMed Central Google Scholar
• Qi, F., Qian, S., Zhang, S. & Zhang, Z. Single cell RNA sequencing of 13 human tissues identify cell types and receptors of human coronaviruses. Biochem. Bioph. Res. Co. 526, 135–140 (2020).
  Article CAS Google Scholar
• Hamming, I. et al. Tissue distribution of ACE2 protein, the functional receptor for SARS coronavirus. A first step in understanding SARS pathogenesis. J. Pathol. 203, 631–637 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Hikmet, F. et al. The protein expression profile of ACE2 in human tissues. Mol. Syst. Biol. 16, e9610 (2020).
  Article CAS PubMed PubMed Central Google Scholar
• Xu, Y. et al. Characteristics of pediatric SARS-CoV-2 infection and potential evidence for persistent fecal viral shedding. Nat. Med. 26, 502–505 (2020).
  Article CAS PubMed Google Scholar
• Uhlen, M. et al. A genome-wide transcriptomic analysis of protein-coding genes in human blood cells. Science 366, eaax9198 (2019).
  Article CAS PubMed Google Scholar
• Lim, Y., Ng, Y., Tam, J. & Liu, D. Human coronaviruses: a review of virus–host interactions. Diseases 4, 26 (2016).
  Article PubMed Central CAS Google Scholar
• Fitzgerald, K. A. & Kagan, J. C. Toll-like receptors and the control of immunity. Cell 180, 1044–1066 (2020).
  Article CAS PubMed Google Scholar
• Nieto-Torres, J. L. et al. Severe acute respiratory syndrome coronavirus E protein transports calcium ions and activates the NLRP3 inflammasome. Virology 485, 330–339 (2015).
  Article CAS PubMed Google Scholar
• Rodrigues, T.S. et al. Inflammasomes are activated in response to SARS-CoV-2 infection and are associated with COVID-19 severity in patients. J. Exp. Med. 218, e20201707 (2021).
  Article CAS PubMed Google Scholar
• Han, Y. et al. Lactate dehydrogenase, a risk factor of severe COVID-19 patients. Aging 12, 11245–11258 (2020).
  Article CAS PubMed PubMed Central Google Scholar
• Wu, C. et al. Inflammasome activation triggers blood clotting and host death through pyroptosis. Immunity 50, 1401–1411 (2019).
  Article CAS PubMed PubMed Central Google Scholar
• Middeldorp, S. et al. Incidence of venous thromboembolism in hospitalized patients with COVID-19. J. Thromb. Haemost. 18, 1995–2002 (2020).
  Article CAS PubMed PubMed Central Google Scholar
• Greenhalgh, T., Knight, M., A’Court, C., Buxton, M. & Husain, L. Management of post-acute COVID-19 in primary care. BMJ 370, m3026 (2020).
  Article PubMed Google Scholar
• Züst, R. et al. Ribose 2′-O-methylation provides a molecular signature for the distinction of self and non-self mRNA dependent on the RNA sensor Mda5. Nat. Immunol. 12, 137–143 (2011).
  Article PubMed PubMed Central CAS Google Scholar
• Spiegel, M. et al. Inhibition of beta interferon induction by severe acute respiratory syndrome coronavirus suggests a two-step model for activation of interferon regulatory factor 3. J. Virol. 79, 2079–2086 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Miorin, L. et al. SARS-CoV-2 Orf6 hijacks Nup98 to block STAT nuclear import and antagonize interferon signaling. Proc. Natl. Acad Sci. USA 117, 28344–28354 (2020).
  Article CAS PubMed PubMed Central Google Scholar
• Arunachalam, P. S. et al. Systems biological assessment of immunity to mild versus severe COVID-19 infection in humans. Science 369, 1210–1220 (2020).
  Article CAS PubMed PubMed Central Google Scholar
• Blanco-Melo, D. et al. Imbalanced host response to SARS-CoV-2 drives development of COVID-19. Cell 181, 1036–1045 (2020).
  Article CAS PubMed PubMed Central Google Scholar
• Lucas, C. et al. Longitudinal analyses reveal immunological misfiring in severe COVID-19. Nature 584, 463–469 (2020).
  Article CAS PubMed PubMed Central Google Scholar
• Vabret, N. et al. Immunology of COVID-19: current state of the science. Immunity 52, 910–941 (2020).
  Article CAS PubMed PubMed Central Google Scholar
• Casanova, J.-L., Su, H. C. & COVID Human Genetic Effort. A global effort to define the human genetics of protective immunity to SARS-CoV-2 infection. Cell 181, 1194–199 (2020).
• Zhang, Q. et al. Inborn errors of type I IFN immunity in patients with life-threatening COVID-19. Science 370, eabd4570 (2020).
  Article CAS PubMed PubMed Central Google Scholar
• Bastard, P. et al. Auto-antibodies against type I IFNs in patients with life-threatening COVID-19. Science 370, eabd4585 (2020).
  Article CAS PubMed PubMed Central Google Scholar
• Gudbjartsson, D. F. et al. Humoral immune response to SARS-CoV-2 in Iceland. N. Engl. J. Med. 383, 1724–1734 (2020).
  Article CAS PubMed Google Scholar
• Wajnberg, A. et al. Robust neutralizing antibodies to SARS-CoV-2 infection persist for months. Science 370, eabd7728 (2020).
  Article CAS Google Scholar
• Lumley, S. F. et al. Antibodies to SARS-CoV-2 are associated with protection against reinfection. Preprint at medRxiv https://doi.org/10.1101/2020.11.18.20234369 (2020).
• Grifoni, A. et al. Targets of T cell responses to SARS-CoV-2 coronavirus in humans with COVID-19 disease and unexposed individuals. Cell 181, 1489–1501 (2020).
  Article CAS PubMed PubMed Central Google Scholar
• Su, L. F., Kidd, B. A., Han, A., Kotzin, J. J. & Davis, M. M. Virus-specific CD4+ memory-phenotype T cells are abundant in unexposed adults. Immunity 38, 373–83 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Bert, N. L. et al. SARS-CoV-2-specific T cell immunity in cases of COVID-19 and SARS, and uninfected controls. Nature 584, 457–462 (2020).
  Article PubMed CAS Google Scholar
• Tetro, J. A. Is COVID-19 receiving ADE from other coronaviruses? Microbes Infect. 22, 72–73 (2020).
  Article CAS PubMed PubMed Central Google Scholar
• Wan, Y. et al. Molecular mechanism for antibody-dependent enhancement of coronavirus entry. J. Virol. 94, e02015–e02019 (2019).
  Google Scholar
• Iwasaki, A. What reinfections mean for COVID-19. Lancet Infect. Dis. https://doi.org/10.1016/S1473-3099(20)30783-0 (2020).
• Lipsitch, M., Grad, Y. H., Sette, A. & Crotty, S. Cross-reactive memory T cells and herd immunity to SARS-CoV-2. Nat. Rev. Immunol. 20, 709–713 (2020).
  Article CAS PubMed Google Scholar
• Mateus, J. et al. Selective and cross-reactive SARS-CoV-2 T cell epitopes in unexposed humans. Science 370, 89–94 (2020).
  Article CAS PubMed PubMed Central Google Scholar
• Ng, K. W. et al. Preexisting and de novo humoral immunity to SARS-CoV-2 in humans. Science 370, eabe1107 (2020).
  Article CAS Google Scholar
• Anderson, E. M. et al. Seasonal human coronavirus antibodies are boosted upon SARS-CoV-2 infection but not associated with protection. Preprint at medRxiv https://doi.org/10.1101/2020.11.06.20227215 (2020).
• Tso, F. Y. et al. High prevalence of pre-existing serological cross-reactivity against SARS-CoV-2 in sub-Sahara Africa. Int. J. Infect. Dis. 102, 577–583 (2020).
  Article PubMed PubMed Central CAS Google Scholar
• Rostad, C. A. et al. Quantitative SARS-CoV-2 serology in children with multisystem inflammatory syndrome (MIS-C). Pediatrics 146, e2020018242 (2020).
  Article PubMed Google Scholar
• Weisberg, S. P. et al. Distinct antibody responses to SARS-CoV-2 in children and adults across the COVID-19 clinical spectrum. Nat. Immunol. https://doi.org/10.1038/s41590-020-00826-9 (2020).
• Pierce, C. A. et al. Immune responses to SARS-CoV-2 infection in hospitalized pediatric and adult patients. Sci. Transl. Med. 564, eabd5487 (2020).
  Article CAS Google Scholar
• Berghöfer, B. et al. TLR7 ligands induce higher IFN-α production in females. J. Immunol. 177, 2088–2096 (2006).
  Article PubMed Google Scholar
• Klein, S. L., Marriott, I. & Fish, E. N. Sex-based differences in immune function and responses to vaccination. Trans. R. Soc. Trop. Med. H. 109, 9–15 (2015).
  Article CAS Google Scholar
• Klein, S. L., Jedlicka, A. & Pekosz, A. The Xs and Y of immune responses to viral vaccines. Lancet Infect. Dis. 10, 338–349 (2010).
  Article PubMed PubMed Central CAS Google Scholar
• Webb, K. et al. Sex and pubertal differences in the type 1 interferon pathway associate with both X chromosome number and serum sex hormone concentration. Front Immunol. 9, 3167 (2019).
  Article PubMed PubMed Central CAS Google Scholar
• Kollmann, T. R., Levy, O., Montgomery, R. R. & Goriely, S. Innate immune function by Toll-like receptors: distinct responses in newborns and the elderly. Immunity 37, 771–783 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Mertz, D. et al. Pregnancy as a risk factor for severe outcomes from influenza virus infection: a systematic review and meta-analysis of observational studies. Vaccine 35, 521–528 (2017).
  Article PubMed PubMed Central Google Scholar
• Pido-Lopez, J., Imami, N. & Aspinall, R. Both age and gender affect thymic output: more recent thymic migrants in females than males as they age. Clin. Exp. Immunol. 125, 409–413 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Saso, A. & Kampmann, B. Vaccine responses in newborns. Semin. Immunopathol. 39, 627–642 (2017).
  Article CAS PubMed PubMed Central Google Scholar
• Lagunas-Rangel, F. A. Neutrophil-to-lymphocyte ratio and lymphocyte-to-C-reactive protein ratio in patients with severe coronavirus disease 2019 (COVID-19): a meta-analysis. J. Med. Virol. 92, 1733–1734 (2020).
  Article CAS PubMed Google Scholar
• Li, J. et al. Neutrophil-to-lymphocyte ratio positively correlates to age in healthy population. J. Clin. Lab Anal. 29, 437–43 (2014).
  Article PubMed PubMed Central CAS Google Scholar
• Yilmaz, H. et al. Usefulness of the neutrophil-to-lymphocyte ratio to prediction of type 2 diabetes mellitus in morbid obesity. Diabetes Metab. Syndr. Clin. Res. Rev. 9, 299–304 (2015).
  Article CAS Google Scholar
• Molony, R. D. et al. Aging impairs both primary and secondary RIG-I signaling for interferon induction in human monocytes. Sci. Signal. 10, eaan2392 (2017).
  Article PubMed PubMed Central CAS Google Scholar
• McGonagle, D., Sharif, K., O’Regan, A. & Bridgewood, C. The role of cytokines including interleukin-6 in COVID-19 induced pneumonia and macrophage activation syndrome-like disease. Autoimmun. Rev. 19, 102537 (2020).
  Article CAS PubMed PubMed Central Google Scholar
• Kang, R. et al. HMGB1 in health and disease. Mol. Asp. Med. 40, 1–116 (2014).
  Article CAS Google Scholar
• Gao, Y., Chen, Y., Liu, M., Shi, S. & Tian, J. Impacts of immunosuppression and immunodeficiency on COVID-19: a systematic review and meta-analysis. J. Infection. 81, 93–95 (2020).
  Article CAS Google Scholar
• Fung, M. & Babik, J. M. COVID-19 in immunocompromised hosts: what we know so far. Clin. Infect. Dis. ciaa863 (2020).
• Robilotti, E. V. et al. Determinants of COVID-19 disease severity in patients with cancer. Nat. Med. 26, 1218–1223 (2020).
  Article CAS PubMed PubMed Central Google Scholar
• Quinti, I. et al. A possible role for B cells in COVID-19?: lesson from patients with Agammaglobulinemia. J. Allergy Clin. Immunol. 146, 211–213 (2020).
  Article CAS PubMed PubMed Central Google Scholar