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Of Mice and Men: The Coronavirus MHV and Mouse Models as a Translational Approach to Understand SARS-CoV-2

Robert Körner, Mohamed Majjouti, Miguel Alcazar and 1 more

Viruses · 2020 · Review · CC BY

doi:10.3390/v12080880

Abstract

The fatal acute respiratory coronavirus disease 2019 (COVID-19) is caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). Since COVID-19 was declared a pandemic by the World Health Organization in March 2020, infection and mortality rates have been rising steadily worldwide. The lack of a vaccine, as well as preventive and therapeutic strategies, emphasize the need to develop new strategies to mitigate SARS-CoV-2 transmission and pathogenesis. Since mouse hepatitis virus (MHV), severe acute respiratory syndrome coronavirus (SARS-CoV), and SARS-CoV-2 share a common genus, lessons learnt from MHV and SARS-CoV could offer mechanistic insights into SARS-CoV-2. This review provides a comprehensive review of MHV in mice and SARS-CoV-2 in humans, thereby highlighting further translational avenues in the development of innovative strategies in controlling the detrimental course of SARS-CoV-2. Specifically, we have focused on various aspects, including host species, organotropism, transmission, clinical disease, pathogenesis, control and therapy, MHV as a model for SARS-CoV and SARS-CoV-2 as well as mouse models for infection with SARS-CoV and SARS-CoV-2. While MHV in mice and SARS-CoV-2 in humans share various similarities, there are also differences that need to be addressed when studying murine models. Translational approaches, such as humanized mouse models are pivotal in studying the clinical course and pathology observed in COVID-19 patients. Lessons from prior murine studies on coronavirus, coupled with novel murine models could offer new promising avenues for treatment of COVID-19.

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    Chen Y., Chen L., Deng Q., Zhang G., Wu K., Ni L., Yang Y., Liu B., Wang W., Wei C., et al. The presence of SARS-CoV-2 RNA in the feces of COVID-19 patients. J. Med. Virol. 2020;92:833-840.

    Not in our library10.1002/jmv.25825

  97. 97.

    Pan L., Mu M., Yang P., Sun Y., Wang R., Yan J., Li P., Hu B., Wang J., Hu C., et al. Clinical Characteristics of COVID-19 Patients With Digestive Symptoms in Hubei, China: A Descriptive, Cross-Sectional, Multicenter Study. Am. J. Gastroenterol. 2020;115:766-773.

    Not in our library10.14309/ajg.0000000000000620

  98. 98.

    Rothe C., Schunk M., Sothmann P., Bretzel G., Froeschl G., Wallrauch C., Zimmer T., Thiel V., Janke C., Guggemos W., et al. Transmission of 2019-nCoV Infection from an Asymptomatic Contact in Germany. N. Engl. J. Med. 2020;382:970-971.

    Not in our library10.1056/nejmc2001468

  99. 99.

    Bai Y., Yao L., Wei T., Tian F., Jin D.Y., Chen L., Wang M. Presumed Asymptomatic Carrier Transmission of COVID-19. JAMA. 2020.

    Not in our library10.1001/jama.2020.2565

  100. 100.
    Transplacental transmission of SARS-CoV-2 infection · 2020
    No notice
  101. 101.
    Does the human placenta express the canonical cell entry mediators for SARS-CoV-2? · 2020
    No notice
  102. 102.
    Complexity of the Basic Reproduction Number (R 0 ) · 2019
    No notice
  103. 103.

    Rodriguez-Morales A.J., Cardona-Ospina J.A., Gutierrez-Ocampo E., Villamizar-Pena R., Holguin-Rivera Y., Escalera-Antezana J.P., Alvarado-Arnez L.E., Bonilla-Aldana D.K., Franco-Paredes C., Henao-Martinez A.F., et al. Clinical, laboratory and imaging features of COVID-19: A systematic review and meta-analysis. Travel Med. Infect. Dis. 2020;34:101623.

    Not in our library10.1016/j.tmaid.2020.101623

  104. 104.
    Estimating the asymptomatic proportion of coronavirus disease 2019 (COVID-19) cases on board the Diamond Princess cruise ship, Yokohama, Japan, 2020 · 2020
    Corrected
  105. 105.

    Guan W.J., Ni Z.Y., Hu Y., Liang W.H., Ou C.Q., He J.X., Liu L., Shan H., Lei C.L., Hui D.S.C., et al. Clinical Characteristics of Coronavirus Disease 2019 in China. N. Engl. J. Med. 2020;382:1708-1720.

    Not in our library10.1056/nejmoa2002032

  106. 106.

    Lechien J.R., Chiesa-Estomba C.M., De Siati D.R., Horoi M., Le Bon S.D., Rodriguez A., Dequanter D., Blecic S., El Afia F., Distinguin L., et al. Olfactory and gustatory dysfunctions as a clinical presentation of mild-to-moderate forms of the coronavirus disease (COVID-19): A multicenter European study. Eur. Arch. Otorhinolaryngol. 2020;277:2251-2261.

    Not in our library10.1007/s00405-020-05965-1

  107. 107.

    Zimmermann P., Curtis N. Coronavirus Infections in Children Including COVID-19: An Overview of the Epidemiology, Clinical Features, Diagnosis, Treatment and Prevention Options in Children. Pediatr. Infect. Dis. J. 2020;39:355-368.

    Not in our library10.1097/inf.0000000000002660

  108. 108.

    Jeng M.J. Coronavirus disease 2019 in children: Current status. J. Chin. Med. Assoc. 2020;83:527-533.

    Not in our library10.1097/jcma.0000000000000323

  109. 109.

    Wang W., Tang J., Wei F. Updated understanding of the outbreak of 2019 novel coronavirus (2019-nCoV) in Wuhan, China. J. Med. Virol. 2020;92:441-447.

    Not in our library10.1002/jmv.25689

  110. 110.

    WHO. China Joint Mission on Coronavirus Disease 2019 (COVID-19). 2020.

    Not in our library

  111. 111.

    Robert Koch Institute. Taeglicher Lagebericht des RKI zur Coronavirus-Krankheit-2019 (COVID-19). 2020.

    Not in our library

  112. 112.

    Center for Disease Control and Prevention. Estimated Influenza Illnesses, Medical Visits, Hospitalizations, and Deaths in the United States—2018–2019 Influenza Season. 2020.

    Not in our library

  113. 113.

    Hoffmann M., Kleine-Weber H., Schroeder S., Kruger N., Herrler T., Erichsen S., Schiergens T.S., Herrler G., Wu N.H., Nitsche A., et al. SARS-CoV-2 Cell Entry Depends on ACE2 and TMPRSS2 and Is Blocked by a Clinically Proven Protease Inhibitor. Cell. 2020;181:271-280.e8.

    Not in our library10.1016/j.cell.2020.02.052

  114. 114.

    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. Biophys. Res. Commun. 2020;526:135-140.

    Not in our library10.1016/j.bbrc.2020.03.044

  115. 115.

    Barkauskas C.E., Cronce M.J., Rackley C.R., Bowie E.J., Keene D.R., Stripp B.R., Randell S.H., Noble P.W., Hogan B.L. Type 2 alveolar cells are stem cells in adult lung. J. Clin. Investig. 2013;123:3025-3036.

    Not in our library10.1172/jci68782

  116. 116.

    Rivellese F., Prediletto E. ACE2 at the centre of COVID-19 from paucisymptomatic infections to severe pneumonia. Autoimmun. Rev. 2020;19:102536.

    Not in our library10.1016/j.autrev.2020.102536

  117. 117.

    Huang C., Wang Y., Li X., Ren L., Zhao J., Hu Y., Zhang L., Fan G., Xu J., Gu X., et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet. 2020;395:497-506.

    Not in our library10.1016/s0140-6736(20)30183-5

  118. 118.
    Comparative pathogenesis of COVID-19, MERS, and SARS in a nonhuman primate model · 2020
    No notice
  119. 119.

    Tian S., Hu W., Niu L., Liu H., Xu H., Xiao S.Y. Pulmonary Pathology of Early-Phase 2019 Novel Coronavirus (COVID-19) Pneumonia in Two Patients With Lung Cancer. J. Thorac. Oncol. 2020;15:700-704.

    Not in our library10.1016/j.jtho.2020.02.010

  120. 120.

    Xu Z., Shi L., Wang Y., Zhang J., Huang L., Zhang C., Liu S., Zhao P., Liu H., Zhu L., et al. Pathological findings of COVID-19 associated with acute respiratory distress syndrome. Lancet Respir. Med. 2020;8:420-422.

    Not in our library10.1016/s2213-2600(20)30076-x

  121. 121.

    Ye Q., Wang B., Mao J. The pathogenesis and treatment of the ‘Cytokine Storm’ in COVID-19. J. Infect. 2020;80:607-613.

    Not in our library10.1016/j.jinf.2020.03.037

  122. 122.

    Chung H.Y., Sung B., Jung K.J., Zou Y., Yu B.P. The molecular inflammatory process in aging. Antioxid. Redox Signal. 2006;8:572-581.

    Not in our library10.1089/ars.2006.8.572

  123. 123.
    Exacerbated Innate Host Response to SARS-CoV in Aged Non-Human Primates · 2010
    No notice
  124. 124.

    Grifoni A., Weiskopf D., Ramirez S.I., Mateus J., Dan J.M., Moderbacher C.R., Rawlings S.A., Sutherland A., Premkumar L., Jadi R.S., et al. Targets of T Cell Responses to SARS-CoV-2 Coronavirus in Humans with COVID-19 Disease and Unexposed Individuals. Cell. 2020;181:1489-1501.e15.

    Not in our library10.1016/j.cell.2020.05.015

  125. 125.

    Takada A., Kawaoka Y. Antibody-dependent enhancement of viral infection: Molecular mechanisms and in vivo implications. Rev. Med. Virol. 2003;13:387-398.

    Not in our library10.1002/rmv.405

  126. 126.

    Meyer N.J., Christie J.D. Genetic heterogeneity and risk of acute respiratory distress syndrome. Semin. Respir. Crit. Care Med. 2013;34:459-474.

    Not in our library10.1055/s-0033-1351121

  127. 127.
    Virology, Epidemiology, Pathogenesis, and Control of COVID-19 · 2020
    No notice
  128. 128.

    Zhao J., Yuan Q., Wang H., Liu W., Liao X., Su Y., Wang X., Yuan J., Li T., Li J., et al. Antibody responses to SARS-CoV-2 in patients of novel coronavirus disease 2019. Clin. Infect. Dis. 2020.

    Not in our library10.1093/cid/ciaa344

  129. 129.

    Wolfel R., Corman V.M., Guggemos W., Seilmaier M., Zange S., Muller M.A., Niemeyer D., Jones T.C., Vollmar P., Rothe C., et al. Virological assessment of hospitalized patients with COVID-2019. Nature. 2020;581:465-469.

    Not in our library10.1038/s41586-020-2196-x

  130. 130.

    Verdecchia P., Cavallini C., Spanevello A., Angeli F. The pivotal link between ACE2 deficiency and SARS-CoV-2 infection. Eur. J. Intern. Med. 2020;76:14-20.

    Not in our library10.1016/j.ejim.2020.04.037

  131. 131.

    Imai Y., Kuba K., Rao S., Huan Y., Guo F., Guan B., Yang P., Sarao R., Wada T., Leong-Poi H., et al. Angiotensin-converting enzyme 2 protects from severe acute lung failure. Nature. 2005;436:112-116.

    Not in our library10.1038/nature03712

  132. 132.

    Alifano M., Alifano P., Forgez P., Iannelli A. Renin-angiotensin system at the heart of COVID-19 pandemic. Biochimie. 2020;174:30-33.

    Not in our library10.1016/j.biochi.2020.04.008

  133. 133.

    Bernstein K.E., Khan Z., Giani J.F., Cao D.Y., Bernstein E.A., Shen X.Z. Angiotensin-converting enzyme in innate and adaptive immunity. Nat. Rev. Nephrol. 2018;14:325-336.

    Not in our library10.1038/nrneph.2018.15

  134. 134.

    Fu Y., Cheng Y., Wu Y. Understanding SARS-CoV-2-Mediated Inflammatory Responses: From Mechanisms to Potential Therapeutic Tools. Virol. Sin. 2020;35:266-271.

    Not in our library10.1007/s12250-020-00207-4

  135. 135.

    D’Amico F., Baumgart D.C., Danese S., Peyrin-Biroulet L. Diarrhea During COVID-19 Infection: Pathogenesis, Epidemiology, Prevention, and Management. Clin. Gastroenterol. Hepatol. 2020;18:1663-1672.

    Not in our library10.1016/j.cgh.2020.04.001

  136. 136.

    Li L.Y., Wu W., Chen S., Gu J.W., Li X.L., Song H.J., Du F., Wang G., Zhong C.Q., Wang X.Y., et al. Digestive system involvement of novel coronavirus infection: Prevention and control infection from a gastroenterology perspective. J. Dig. Dis. 2020;21:199-204.

    Not in our library10.1111/1751-2980.12862

  137. 137.

    Ruan Q., Yang K., Wang W., Jiang L., Song J. Clinical predictors of mortality due to COVID-19 based on an analysis of data of 150 patients from Wuhan, China. Intensive Care Med. 2020;46:846-848.

    Not in our library10.1007/s00134-020-05991-x

  138. 138.

    Guzik T.J., Mohiddin S.A., Dimarco A., Patel V., Savvatis K., Marelli-Berg F.M., Madhur M.S., Tomaszewski M., Maffia P., D’Acquisto F., et al. COVID-19 and the cardiovascular system: Implications for risk assessment, diagnosis, and treatment options. Cardiovasc. Res. 2020;116:1666-1687.

    Not in our library10.1093/cvr/cvaa106

  139. 139.

    National Institute of Allergy and Infectious Diseases. NIH Clinical Trial Shows Remdesivir Accelerates Recovery from Advanced COVID-19. 2020.

    Not in our library

  140. 140.

    Takeda. Takeda Initiates Development of a Plasma-Derived Therapy for COVID-19. 2020.

    Not in our library

  141. 141.

    Geleris J., Sun Y., Platt J., Zucker J., Baldwin M., Hripcsak G., Labella A., Manson D.K., Kubin C., Barr R.G., et al. Observational Study of Hydroxychloroquine in Hospitalized Patients with Covid-19. N. Engl. J. Med. 2020;382:2411-2418.

    Not in our library10.1056/nejmoa2012410

  142. 142.
    Effective treatment of severe COVID-19 patients with tocilizumab · 2020
    No notice
  143. 143.

    Du L., He Y., Zhou Y., Liu S., Zheng B.J., Jiang S. The spike protein of SARS-CoV—A target for vaccine and therapeutic development. Nat. Rev. Microbiol. 2009;7:226-236.

    Not in our library10.1038/nrmicro2090

  144. 144.

    Wang X., Tan L., Wang X., Liu W., Lu Y., Cheng L., Sun Z. Comparison of nasopharyngeal and oropharyngeal swabs for SARS-CoV-2 detection in 353 patients received tests with both specimens simultaneously. Int. J. Infect. Dis. 2020;94:107-109.

    Not in our library10.1016/j.ijid.2020.04.023

  145. 145.

    De Albuquerque N., Baig E., Ma X., Zhang J., He W., Rowe A., Habal M., Liu M., Shalev I., Downey G.P., et al. Murine hepatitis virus strain 1 produces a clinically relevant model of severe acute respiratory syndrome in A/J mice. J. Virol. 2006;80:10382-10394.

    Not in our library10.1128/jvi.00747-06

  146. 146.

    Will J.P., Hirani D., Thielen F., Klein F., Vohlen C., Dinger K., Dotsch J., Alejandre Alcazar M.A. Strain-dependent effects on lung structure, matrix remodeling, and Stat3/Smad2 signaling in C57BL/6N and C57BL/6J mice after neonatal hyperoxia. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2019;317:R169-R181.

    Not in our library10.1152/ajpregu.00286.2018

  147. 147.

    Khanolkar A., Hartwig S.M., Haag B.A., Meyerholz D.K., Harty J.T., Varga S.M. Toll-like receptor 4 deficiency increases disease and mortality after mouse hepatitis virus type 1 infection of susceptible C3H mice. J. Virol. 2009;83:8946-8956.

    Not in our library10.1128/jvi.01857-08

  148. 148.

    Poltorak A., He X., Smirnova I., Liu M.Y., Van Huffel C., Du X., Birdwell D., Alejos E., Silva M., Galanos C., et al. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: Mutations in Tlr4 gene. Science. 1998;282:2085-2088.

    Not in our library10.1126/science.282.5396.2085

  149. 149.

    Ma X.Z., Bartczak A., Zhang J., Khattar R., Chen L., Liu M.F., Edwards A., Levy G., McGilvray I.D. Proteasome inhibition in vivo promotes survival in a lethal murine model of severe acute respiratory syndrome. J. Virol. 2010;84:12419-12428.

    Not in our library10.1128/jvi.01219-10

  150. 150.

    Han B., Ma X., Zhang J., Zhang Y., Bai X., Hwang D.M., Keshavjee S., Levy G.A., McGilvray I., Liu M. Protective effects of long pentraxin PTX3 on lung injury in a severe acute respiratory syndrome model in mice. Lab. Investig. 2012;92:1285-1296.

    Not in our library10.1038/labinvest.2012.92

  151. 151.

    Yang Z., Du J., Chen G., Zhao J., Yang X., Su L., Cheng G., Tang H. Coronavirus MHV-A59 infects the lung and causes severe pneumonia in C57BL/6 mice. Virol. Sin. 2014;29:393-402.

    Not in our library10.1007/s12250-014-3530-y

  152. 152.

    Palao M., Fernandez-Diaz E., Gracia-Gil J., Romero-Sanchez C.M., Diaz-Maroto I., Segura T. Multiple sclerosis following SARS-CoV-2 infection. Mult. Scler. Relat. Disord. 2020;45:102377.

    Not in our library10.1016/j.msard.2020.102377

  153. 153.

    Matias-Guiu J., Gomez-Pinedo U., Montero-Escribano P., Gomez-Iglesias P., Porta-Etessam J., Matias-Guiu J.A. Should we expect neurological symptoms in the SARS-CoV-2 epidemic? Neurologia. 2020;35:170-175.

    Not in our library10.1016/j.nrleng.2020.03.002

  154. 154.

    Leibowitz J.L., Srinivasa R., Williamson S.T., Chua M.M., Liu M., Wu S., Kang H., Ma X.Z., Zhang J., Shalev I., et al. Genetic determinants of mouse hepatitis virus strain 1 pneumovirulence. J. Virol. 2010;84:9278-9291.

    Not in our library10.1128/jvi.00330-10

  155. 155.

    Das Sarma J. A Mechanism of Virus-Induced Demyelination. Interdiscip. Perspect. Infect. Dis. 2010;2010.

    Not in our library10.1155/2010/109239

  156. 156.

    Indwiani Astuti Y. Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2): An overview of viral structure and host response. Diabetes Metab. Syndr. 2020;14:407-412.

    Not in our library10.1016/j.dsx.2020.04.020

  157. 157.

    Rempel J.D., Murray S.J., Meisner J., Buchmeier M.J. Mouse hepatitis virus neurovirulence: Evidence of a linkage between S glycoprotein expression and immunopathology. Virology. 2004;318:45-54.

    Not in our library10.1016/j.virol.2003.08.041

  158. 158.

    Zhang R., Li Y., Cowley T.J., Steinbrenner A.D., Phillips J.M., Yount B.L., Baric R.S., Weiss S.R. The nsp1, nsp13, and M proteins contribute to the hepatotropism of murine coronavirus JHM.WU. J. Virol. 2015;89:3598-3609.

    Not in our library10.1128/jvi.03535-14

  159. 159.

    Khanolkar A., Hartwig S.M., Haag B.A., Meyerholz D.K., Epping L.L., Haring J.S., Varga S.M., Harty J.T. Protective and pathologic roles of the immune response to mouse hepatitis virus type 1: Implications for severe acute respiratory syndrome. J. Virol. 2009;83:9258-9272.

    Not in our library10.1128/jvi.00355-09

  160. 160.

    Preston S., Wright G.J., Starr K., Barclay A.N., Brown M.H. The leukocyte/neuron cell surface antigen OX2 binds to a ligand on macrophages. Eur. J. Immunol. 1997;27:1911-1918.

    Not in our library10.1002/eji.1830270814

  161. 161.

    Wright G.J., Cherwinski H., Foster-Cuevas M., Brooke G., Puklavec M.J., Bigler M., Song Y., Jenmalm M., Gorman D., McClanahan T., et al. Characterization of the CD200 receptor family in mice and humans and their interactions with CD200. J. Immunol. 2003;171:3034-3046.

    Not in our library10.4049/jimmunol.171.6.3034

  162. 162.

    Rijkers E.S., de Ruiter T., Baridi A., Veninga H., Hoek R.M., Meyaard L. The inhibitory CD200R is differentially expressed on human and mouse T and B lymphocytes. Mol. Immunol. 2008;45:1126-1135.

    Not in our library10.1016/j.molimm.2007.07.013

  163. 163.
    CD200 receptor controls sex-specific TLR7 responses to viral infection. · 2012
    Not checked
  164. 164.

    Khanolkar A., Fulton R.B., Epping L.L., Pham N.L., Tifrea D., Varga S.M., Harty J.T. T cell epitope specificity and pathogenesis of mouse hepatitis virus-1-induced disease in susceptible and resistant hosts. J. Immunol. 2010;185:1132-1141.

    Not in our library10.4049/jimmunol.0902749

  165. 165.

    Hartwig S.M., Holman K.M., Varga S.M. Depletion of alveolar macrophages ameliorates virus-induced disease following a pulmonary coronavirus infection. PLoS ONE. 2014;9:e90720.

    Not in our library10.1371/journal.pone.0090720

  166. 166.

    Lutz C., Maher L., Lee C., Kang W. COVID-19 preclinical models: Human angiotensin-converting enzyme 2 transgenic mice. Hum. Genom. 2020;14:20.

    Not in our library10.1186/s40246-020-00272-6

  167. 167.

    Kim Y.I., Kim S.G., Kim S.M., Kim E.H., Park S.J., Yu K.M., Chang J.H., Kim E.J., Lee S., Casel M.A.B., et al. Infection and Rapid Transmission of SARS-CoV-2 in Ferrets. Cell Host Microbe. 2020;27:704-709.e2.

    Not in our library10.1016/j.chom.2020.03.023

  168. 168.
    Susceptibility of ferrets, cats, dogs, and other domesticated animals to SARS–coronavirus 2 · 2020
    No notice
  169. 169.

    Chan J.F., Zhang A.J., Yuan S., Poon V.K., Chan C.C., Lee A.C., Chan W.M., Fan Z., Tsoi H.W., Wen L., et al. Simulation of the clinical and pathological manifestations of Coronavirus Disease 2019 (COVID-19) in golden Syrian hamster model: Implications for disease pathogenesis and transmissibility. Clin. Infect. Dis. 2020.

    Not in our library10.1093/cid/ciaa325

  170. 170.

    Woolsey C., Borisevich V., Prasad A.N., Agans K.N., Deer D.J., Dobias N.S., Heymann J.C., Foster S.L., Levine C.B., Medina L., et al. Establishment of an African green monkey model for COVID-19. bioRxiv. 2020.

    Not in our library10.1101/2020.05.17.100289

  171. 171.

    Yu P., Qi F., Xu Y., Li F., Liu P., Liu J., Bao L., Deng W., Gao H., Xiang Z., et al. Age-related rhesus macaque models of COVID-19. Anim. Model. Exp. Med. 2020;3:93-97.

    Not in our library10.1002/ame2.12108

  172. 172.

    Subbarao K., McAuliffe J., Vogel L., Fahle G., Fischer S., Tatti K., Packard M., Shieh W.J., Zaki S., Murphy B. Prior infection and passive transfer of neutralizing antibody prevent replication of severe acute respiratory syndrome coronavirus in the respiratory tract of mice. J. Virol. 2004;78:3572-3577.

    Not in our library10.1128/jvi.78.7.3572-3577.2004

  173. 173.

    Glass W.G., Subbarao K., Murphy B., Murphy P.M. Mechanisms of host defense following severe acute respiratory syndrome-coronavirus (SARS-CoV) pulmonary infection of mice. J. Immunol. 2004;173:4030-4039.

    Not in our library10.4049/jimmunol.173.6.4030

  174. 174.

    Hogan R.J., Gao G., Rowe T., Bell P., Flieder D., Paragas J., Kobinger G.P., Wivel N.A., Crystal R.G., Boyer J., et al. Resolution of primary severe acute respiratory syndrome-associated coronavirus infection requires Stat1. J. Virol. 2004;78:11416-11421.

    Not in our library10.1128/jvi.78.20.11416-11421.2004

  175. 175.

    Herriges M., Morrisey E.E. Lung development: Orchestrating the generation and regeneration of a complex organ. Development. 2014;141:502-513.

    Not in our library10.1242/dev.098186

  176. 176.

    Morrisey E.E., Cardoso W.V., Lane R.H., Rabinovitch M., Abman S.H., Ai X., Albertine K.H., Bland R.D., Chapman H.A., Checkley W., et al. Molecular determinants of lung development. Ann. Am. Thorac. Soc. 2013;10:S12-S16.

    Not in our library10.1513/annalsats.201207-036ot

  177. 177.
    Development of the lung · 2017
    No notice
  178. 178.

    Copland I., Post M. Lung development and fetal lung growth. Paediatr. Respir. Rev. 2004;5:S259-S264.

    Not in our library10.1016/s1526-0542(04)90049-8

  179. 179.

    Alejandre-Alcazar M.A., Kwapiszewska G., Reiss I., Amarie O.V., Marsh L.M., Sevilla-Perez J., Wygrecka M., Eul B., Kobrich S., Hesse M., et al. Hyperoxia modulates TGF-beta/BMP signaling in a mouse model of bronchopulmonary dysplasia. Am. J. Physiol. Lung Cell. Mol. Physiol. 2007;292:L537-L549.

    Not in our library10.1152/ajplung.00050.2006

  180. 180.

    Alejandre Alcazar M.A., Kaschwich M., Ertsey R., Preuss S., Milla C., Mujahid S., Masumi J., Khan S., Mokres L.M., Tian L., et al. Elafin Treatment Rescues EGFR-Klf4 Signaling and Lung Cell Survival in Ventilated Newborn Mice. Am. J. Respir. Cell. Mol. Biol. 2018;59:623-634.

    Not in our library10.1165/rcmb.2017-0332oc

  181. 181.

    Domm W., Misra R.S., O’Reilly M.A. Affect of Early Life Oxygen Exposure on Proper Lung Development and Response to Respiratory Viral Infections. Front. Med. (Lausanne). 2015;2:55.

    Not in our library10.3389/fmed.2015.00055

  182. 182.

    Wahl A., De C., Abad Fernandez M., Lenarcic E.M., Xu Y., Cockrell A.S., Cleary R.A., Johnson C.E., Schramm N.J., Rank L.M., et al. Precision mouse models with expanded tropism for human pathogens. Nat. Biotechnol. 2019;37:1163-1173.

    Not in our library10.1038/s41587-019-0225-9

  183. 183.

    Franceschi C., Garagnani P., Vitale G., Capri M., Salvioli S. Inflammaging and ‘Garb-aging’. Trends Endocrinol. Metab. 2017;28:199-212.

    Not in our library10.1016/j.tem.2016.09.005

  184. 184.

    Merad M., Martin J.C. Pathological inflammation in patients with COVID-19: A key role for monocytes and macrophages. Nat. Rev. Immunol. 2020;20:355-362.

    Not in our library10.1038/s41577-020-0331-4

  185. 185.
    An atlas of the aging lung mapped by single cell transcriptomics and deep tissue proteomics · 2019
    No notice
  186. 186.

    Roberts A., Paddock C., Vogel L., Butler E., Zaki S., Subbarao K. Aged BALB/c mice as a model for increased severity of severe acute respiratory syndrome in elderly humans. J. Virol. 2005;79:5833-5838.

    Not in our library10.1128/jvi.79.9.5833-5838.2005

  187. 187.

    Chen J., Lau Y.F., Lamirande E.W., Paddock C.D., Bartlett J.H., Zaki S.R., Subbarao K. Cellular immune responses to severe acute respiratory syndrome coronavirus (SARS-CoV) infection in senescent BALB/c mice: CD4+ T cells are important in control of SARS-CoV infection. J. Virol. 2010;84:1289-1301.

    Not in our library10.1128/jvi.01281-09

  188. 188.

    McCray P.B., Pewe L., Wohlford-Lenane C., Hickey M., Manzel L., Shi L., Netland J., Jia H.P., Halabi C., Sigmund C.D., et al. Lethal infection of K18-hACE2 mice infected with severe acute respiratory syndrome coronavirus. J. Virol. 2007;81:813-821.

    Not in our library10.1128/jvi.02012-06

  189. 189.

    Yang X.H., Deng W., Tong Z., Liu Y.X., Zhang L.F., Zhu H., Gao H., Huang L., Liu Y.L., Ma C.M., et al. Mice transgenic for human angiotensin-converting enzyme 2 provide a model for SARS coronavirus infection. Comp. Med. 2007;57:450-459.

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    Yoshikawa N., Yoshikawa T., Hill T., Huang C., Watts D.M., Makino S., Milligan G., Chan T., Peters C.J., Tseng C.T. Differential virological and immunological outcome of severe acute respiratory syndrome coronavirus infection in susceptible and resistant transgenic mice expressing human angiotensin-converting enzyme 2. J. Virol. 2009;83:5451-5465.

    Not in our library10.1128/jvi.02272-08

  191. 191.

    Tseng C.T., Huang C., Newman P., Wang N., Narayanan K., Watts D.M., Makino S., Packard M.M., Zaki S.R., Chan T.S., et al. Severe acute respiratory syndrome coronavirus infection of mice transgenic for the human Angiotensin-converting enzyme 2 virus receptor. J. Virol. 2007;81:1162-1173.

    Not in our library10.1128/jvi.01702-06

  192. 192.

    Bao L., Deng W., Huang B., Gao H., Liu J., Ren L., Wei Q., Yu P., Xu Y., Qi F., et al. The pathogenicity of SARS-CoV-2 in hACE2 transgenic mice. Nature. 2020;583:830-833.

    Not in our library10.1038/s41586-020-2312-y

  193. 193.

    Sun S.H., Chen Q., Gu H.J., Yang G., Wang Y.X., Huang X.Y., Liu S.S., Zhang N.N., Li X.F., Xiong R., et al. A Mouse Model of SARS-CoV-2 Infection and Pathogenesis. Cell Host Microbe. 2020;28:124-133.e4.

    Not in our library10.1016/j.chom.2020.05.020

  194. 194.

    Hassan A.O., Case J.B., Winkler E.S., Thackray L.B., Kafai N.M., Bailey A.L., McCune B.T., Fox J.M., Chen R.E., Alsoussi W.B., et al. A SARS-CoV-2 Infection Model in Mice Demonstrates Protection by Neutralizing Antibodies. Cell. 2020;182:744-753.e4.

    Not in our library10.1016/j.cell.2020.06.011

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    Sun J., Zhuang Z., Zheng J., Li K., Wong R.L., Liu D., Huang J., He J., Zhu A., Zhao J., et al. Generation of a Broadly Useful Model for COVID-19 Pathogenesis, Vaccination, and Treatment. Cell. 2020;182:734-743.e5.

    Not in our library10.1016/j.cell.2020.06.010

  196. 196.

    Roberts A., Deming D., Paddock C.D., Cheng A., Yount B., Vogel L., Herman B.D., Sheahan T., Heise M., Genrich G.L., et al. A mouse-adapted SARS-coronavirus causes disease and mortality in BALB/c mice. PLoS Pathog. 2007;3:e5.

    Not in our library10.1371/journal.ppat.0030005

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    Nagata N., Iwata N., Hasegawa H., Fukushi S., Harashima A., Sato Y., Saijo M., Taguchi F., Morikawa S., Sata T. Mouse-passaged severe acute respiratory syndrome-associated coronavirus leads to lethal pulmonary edema and diffuse alveolar damage in adult but not young mice. Am. J. Pathol. 2008;172:1625-1637.

    Not in our library10.2353/ajpath.2008.071060

  198. 198.

    Day C.W., Baric R., Cai S.X., Frieman M., Kumaki Y., Morrey J.D., Smee D.F., Barnard D.L. A new mouse-adapted strain of SARS-CoV as a lethal model for evaluating antiviral agents in vitro and in vivo. Virology. 2009;395:210-222.

    Not in our library10.1016/j.virol.2009.09.023

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    Frieman M., Yount B., Agnihothram S., Page C., Donaldson E., Roberts A., Vogel L., Woodruff B., Scorpio D., Subbarao K., et al. Molecular determinants of severe acute respiratory syndrome coronavirus pathogenesis and virulence in young and aged mouse models of human disease. J. Virol. 2012;86:884-897.

    Not in our library10.1128/jvi.05957-11

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    Dinnon K.H., Leist S.R., Schafer A., Edwards C.E., Martinez D.R., Montgomery S.A., West A., Yount B.L., Hou Y.J., Adams L.E., et al. A mouse-adapted SARS-CoV-2 model for the evaluation of COVID-19 medical countermeasures. bioRxiv. 2020.

    Not in our library10.1101/2020.05.06.081497

  201. 201.

    Masters P.S., Koetzner C.A., Kerr C.A., Heo Y. Optimization of targeted RNA recombination and mapping of a novel nucleocapsid gene mutation in the coronavirus mouse hepatitis virus. J. Virol. 1994;68:328-337.

    Not in our library10.1128/jvi.68.1.328-337.1994

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