Cited by 1,256SARS-CoV-2 and COVID-19 ResearchAnimal Virus Infections StudiesViral Infections and Outbreaks Research

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Coronavirus Pathogenesis and the Emerging Pathogen Severe Acute Respiratory Syndrome Coronavirus

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Weiss, Susan R., Navas-Martin, Sonia·2005·Microbiology and Molecular Biology Reviews

DOI 10.1128/mmbr.69.4.635-664.2005PMC PMC1306801

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Abstract

SUMMARY: Coronaviruses are a family of enveloped, single-stranded, positive-strand RNA viruses classified within the Nidovirales order. This coronavirus family consists of pathogens of many animal species and of humans, including the recently isolated severe acute respiratory syndrome coronavirus (SARS-CoV). This review is divided into two main parts; the first concerns the animal coronaviruses and their pathogenesis, with an emphasis on the functions of individual viral genes, and the second discusses the newly described human emerging pathogen, SARS-CoV. The coronavirus part covers (i) a description of a group of coronaviruses and the diseases they cause, including the prototype coronavirus, murine hepatitis virus, which is one of the recognized animal models for multiple sclerosis, as well as viruses of veterinary importance that infect the pig, chicken, and cat and a summary of the human viruses; (ii) a short summary of the replication cycle of coronaviruses in cell culture; (iii) the development and application of reverse genetics systems; and (iv) the roles of individual coronavirus proteins in replication and pathogenesis. The SARS-CoV part covers the pathogenesis of SARS, the developing animal models for infection, and the progress in vaccine development and antiviral therapies. The data gathered on the animal coronaviruses continue to be helpful in understanding SARS-CoV.

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“CoVs are known to cause upper and lower respiratory diseases, gastroenteritis, and central nervous system infections in a number of avian and mammalian hosts, including humans (Weiss and Navas-Martin, 2005).”
Background
Next-generation computational tools and resources for coronavirus research: From detection to vaccine discovery
Kangabam, R. D., Sahoo, S., Ghosh, A., Roy, R., Silla, Y., Misra, N., & Suar, M. (2020) · Computers in Biology and Medicine · doi:10.1016/j.compbiomed.2020.104158 · Cited by 23
Biomaterials-Based Opportunities to Engineer the Pulmonary Host Immune Response in COVID-19
Jarai, B. M., Stillman, Z. S., Bomb, K., Kloxin, A. M., & Fromen, C. A. (2020) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.0c01287 · Cited by 22
Dimethyl sulfoxide reduces the stability but enhances catalytic activity of the main SARS‐CoV‐2 protease 3CLpro
Ferreira, J. C., Fadl, S., Ilter, M., Pekel, H., Rezgui, R., Şensoy, Ö., & Rabeh, W. M. (2021) · The FASEB Journal · doi:10.1096/fj.202100994 · Cited by 22
IgG antibody titers against SARS-CoV-2 nucleocapsid protein correlate with the severity of COVID-19 patients
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“The E proteins play multiple roles in the viral replication cycle [7], virion release [8] and viral pathogenesis [9].”
Background
Unconventional Use of LC3 by Coronaviruses through the Alleged Subversion of the ERAD Tuning Pathway
Reggiori, F., de Haan, C. A. M., & Molinari, M. (2011) · Viruses · doi:10.3390/v3091610 · Cited by 23
Expected immune recognition of COVID-19 virus by memory from earlier infections with common coronaviruses in a large part of the world population
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An overview of viruses discovered over the last decades and drug development for the current pandemic
Mirza, A. Z., Shamshad, H., Osra, F. A., Habeebullah, T. M., & Morad, M. H. (2020) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2020.173746 · Cited by 23
“Group I coronaviruses include not only animal pathogens but also human coronaviruses HCoV-229E and HKU1 (Weiss and Navas-Martin, 2005).”
Background
Recent updates on COVID-19: A holistic review
Jakhmola, S., Indari, O., Kashyap, D., Varshney, N., Rani, A., Sonkar, C., Baral, B., Chatterjee, S., Das, A., Kumar, R., et al. (2020) · Heliyon · doi:10.1016/j.heliyon.2020.e05706 · Cited by 20
“The virus originated in the Wuhan province of China, and the disease, coronavirus disease-2019 (COVID-19), has become an emerging global health emergency since 11 th March 2020 [25].”
Influential
An Overview of the Perspective of Cellular Autophagy
Alharbi, Y. M., Bima, A. I. H., & Elsamanoudy, A. Z. (2021) · Journal of Microscopy and Ultrastructure · doi:10.4103/jmau.jmau_33_20 · Cited by 24
“Coronaviruses (CoVs) are single-stranded RNA enveloped viruses (26–32 kilobases in size).[65] They belong to the Coronaviridae family of viruses in the order Nidovirales.”
Background
Murine-β-coronavirus-induced neuropathogenesis sheds light on CNS pathobiology of SARS-CoV2
Chakravarty, D., & Sarma, J. D. (2021) · Journal of NeuroVirology · doi:10.1007/s13365-021-00945-5 · Cited by 20
The stalk domain of SARS-CoV-2 NSP13 is essential for its helicase activity
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The effects of SARS-CoV-2 infection on modulating innate immunity and strategies of combating inflammatory response for COVID-19 therapy
Wang, Y., Wu, M., Li, Y., Yuen, H. H., & He, M. (2022) · Journal of Biomedical Science · doi:10.1186/s12929-022-00811-4 · Cited by 22
“The structure of SARS‐CoV‐2 Coronaviruses are enveloped viruses with a positivesense single-stranded RNA (+ ssRNA) [10].”
Background
Repurposing of FDA Approved Drugs Against SARS-CoV-2 Papain-Like Protease: Computational, Biochemical, and in vitro Studies
Kulandaisamy, R., Kushwaha, T., Dalal, A., Kumar, V., Singh, D., Baswal, K., Sharma, P., Praneeth, K., Jorwal, P., Kayampeta, S. R., et al. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.877813 · Cited by 21
“Moreover, the available literature distinctly demonstrates the similarities in various pathways between the two viruses including the unfolded protein response, the MAPK pathway and the proinflammatory response pathways (Tyrrell, 1965;Weiss, 2005).”
Background
DDX5: an expectable treater for viral infection- a literature review
Hu, M., Zheng, H., Wu, J., Sun, Y., Wang, T., & Chen, S. (2022) · Annals of Translational Medicine · doi:10.21037/atm-22-2375 · Cited by 21
“( 95-97).”
Research progress in methods for detecting neutralizing antibodies against SARS-CoV-2
Chen, C., Liang, J., Hu, H., Li, X., Wang, L., & Wang, Z. (2023) · Analytical Biochemistry · doi:10.1016/j.ab.2023.115199 · Cited by 22
A phage-displayed peptide recognizing porcine aminopeptidase N is a potent small molecule inhibitor of PEDV entry
Meng, F., Suo, S., Zarlenga, D. S., Cong, Y., Ma, X., Zhao, Q., & Ren, X. (2014) · Virology · doi:10.1016/j.virol.2014.01.010 · Cited by 21
“Coronaviruses belong to the family of Coronaviridae and commonly cause respiratory or gastroenteric diseases (Weiss and Navas-Martin, 2005; Lai et al., 2007).”
Background
Hydroxychloroquine for treatment of nonsevere COVID‐19 patients: Systematic review and meta‐analysis of controlled clinical trials
Elsawah, H. K., Elsokary, M. A., Elrazzaz, M., & Elshafie, A. H. (2020) · Journal of Medical Virology · doi:10.1002/jmv.26442 · Cited by 20
Cancer Care Management During the COVID-19 Pandemic
Jafari, A., Rezaei–Tavirani, M., Karami, S., Yazdani, M., Zali, H., & Jafari, Z. (2020) · Risk Management and Healthcare Policy · doi:10.2147/rmhp.s261357 · Cited by 21
Identification of Amino Acids within Nonstructural Proteins 10 and 14 of the Avian Coronavirus Infectious Bronchitis Virus That Result in Attenuation In Vivo and In Ovo
Keep, S., Stevenson-Leggett, P., Dowgier, G., Everest, H., Freimanis, G. L., Oade, M. S., Hammond, J., Armesto, M., Vila, R., Bru, T., et al. (2022) · Journal of Virology · doi:10.1128/jvi.02059-21 · Cited by 22
“drome coronavirus (SARS-CoV), which caused over 800 deaths from 2003 to 2004 (2, 3);”
Background
Correlations between Kidney and Heart Function Bioindicators and the Expressions of Toll-Like, ACE2, and NRP-1 Receptors in COVID-19
Sultan, R. H., Abdallah, M., Ali, T. M., Assal, H. H., Ahmed, A. E., Elesawy, B. H., & Ahmed, O. M. (2022) · Vaccines · doi:10.3390/vaccines10071106 · Cited by 21
Sterilizing Immunity against COVID-19: Developing Helper T cells I and II activating vaccines is imperative
Kyei-Barffour, I., Akwetey, S. A., Aninagyei, E., Ghartey‐Kwansah, G., & Acheampong, D. O. (2021) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2021.112282 · Cited by 21
Negatively charged residues in the endodomain are critical for specific assembly of spike protein into murine coronavirus
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Transgene expression in the genome of Middle East respiratory syndrome coronavirus based on a novel reverse genetics system utilizing Red-mediated recombination cloning
Muth, D., Meyer, B., Niemeyer, D., Schroeder, S., Osterrieder, N., Müller, M. A., & Drosten, C. (2017) · Journal of General Virology · doi:10.1099/jgv.0.000919 · Cited by 20
Coronavirus as silent killer: recent advancement to pathogenesis, therapeutic strategy and future perspectives
Aran, K. R., Rohit, Ghosh, A., & Singh, S. (2020) · VirusDisease · doi:10.1007/s13337-020-00580-4 · Cited by 20
Predicting COVID-19 Spread in Pakistan using the SIR Model
Shah, S. T. A., Mansoor, M., Mirza, A. F., Dilshad, M., Khan, M. I., Farwa, R., Khan, M. A., Bilal, M., & Iqbal, H. M. N. (2020) · Journal of Pure and Applied Microbiology · doi:10.22207/jpam.14.2.40 · Cited by 20
Features of the development of the COVID-19 pandemic
Болехан, В. Н., Улюкин, И. М., & Peleshok, S. A. (2020) · Medico-Biological and Socio-Psychological Problems of Safety in Emergency Situations · doi:10.25016/2541-7487-2020-0-4-16-26 · Cited by 20
Engineered Aptamers for Enhanced COVID-19 Theranostics
Acquah, C., Jeevanandam, J., Tan, K. X., & Danquah, M. K. (2021) · Cellular and Molecular Bioengineering · doi:10.1007/s12195-020-00664-7 · Cited by 20
SARS coronavirus outbreaks past and present—a comparative analysis of SARS-CoV-2 and its predecessors
Low, Z. Y., Yip, A. J. W., Sharma, A., & Lal, S. K. (2021) · Virus Genes · doi:10.1007/s11262-021-01846-9 · Cited by 23
Coronavirus genotype diversity and prevalence of infection in wild carnivores in the Serengeti National Park, Tanzania
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“They are enveloped, single-stranded RNA viruses with the largest genomes of all RNA viruses [13, 21].”
Background
Medicinal herb extracts ameliorate impaired growth performance and intestinal lesion of newborn piglets challenged with the virulent porcine epidemic diarrhea virus
Kim, H. B., Lee, C. Y., Kim, S., Han, J., & Choi, K. H. (2015) · Journal of Animal Science and Technology · doi:10.1186/s40781-015-0065-1 · Cited by 20
“The porcine epidemic diarrhea virus (PEDV) or genus Alphacoronavirus causes an acute or sub-acute gastrointestinal disorder in pigs of all ages resulting in serious economic losses across Europe and Asia [1] [2] [3] .”
Background
Porcine amino peptidase N domain VII has critical role in binding and entry of porcine epidemic diarrhea virus
Kamau, N. A., Park, J.-E., Park, E., Yu, J.-E., Rho, J., & Shin, H. (2016) · Virus Research · doi:10.1016/j.virusres.2016.10.004 · Cited by 20
“Thus, two mutants; (David and Kathryn, 2007) expressing domains I–VI of pAPNwt and (Susan and Navas-Martin, 2005) expressing domain VII of pAPNwt were constructed and designated pAPND1-VI and pAPNDVII, respectively.”
Method
Temporal evolution, most influential studies and sleeping beauties of the coronavirus literature
Haghani, M., & Varamini, P. (2021) · Scientometrics · doi:10.1007/s11192-021-04036-4 · Cited by 20
Severe Acute Respiratory Syndrome Coronavirus (SARS-CoV-1) and Middle East Respiratory Syndrome Coronavirus (MERS-CoV) infections in pregnancy – An overview
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“The immune response in normal pregnancy is strikingly similar to what happens with SARS-CoV-2 infection, comprising an increase in Angiotensin converting enzyme 2 (ACE2) receptors, a decrease in natural killer cells, a rise in numbers of NKG2A receptors, a fall in lymphocyte count and an increase in activity of proinf…”
SARS-CoV-2 spike protein: Site-specific breakpoints for the development of COVID-19 vaccines
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“For complete contact with ACE-2, the RBM (receptor binding motif) consisting of 424– 494 amino acids of the RBD is essential, and hence is also known as receptor-binding loop (Weiss and Navas-Martin, 2005).”
Non-invasive imaging of mouse hepatitis coronavirus infection reveals determinants of viral replication and spreadin vivo
Raaben, M., Prins, H., Martens, A. C., Rottier, P. J. M., & de Haan, C. A. M. (2009) · Cellular Microbiology · doi:10.1111/j.1462-5822.2009.01298.x · Cited by 20
“Also interferon (IFN)-and perforin-mediated mechanisms are involved in the clearance of MHV from different cell types (Weiss and Navas-Martin, 2005) .”
Background
The Relationship of Severe Acute Respiratory Syndrome Coronavirus with Avian and Other Coronaviruses
Jackwood, M. W. (2006) · Avian Diseases · doi:10.1637/7612-042006r.1 · Cited by 20
Identification of the avian infectious bronchitis coronaviruses with mutations in gene 3
Liu, S., Zhang, Q., Chen, J., Han, Z., Shao, Y., Kong, X., & Tong, G. (2008) · Gene · doi:10.1016/j.gene.2008.01.004 · Cited by 20
An mRNA vaccine against SARS-CoV-2: Lyophilized, liposome-based vaccine candidate EG-COVID induces high levels of virus neutralizing antibodiesPreprint
Hong, H., Kim, K. S., Park, S. A., Chun, M. J., Hong, E. Y., Chung, S. W., Kim, H. J., Shin, B. G., Braka, A., Thanappan, J., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.03.22.436375 · Cited by 20
New Pyrimidinone Bearing Aminomethylenes and Schiff Bases as Potent Antioxidant, Antibacterial, SARS-CoV-2, and COVID-19 Main Protease M Pro Inhibitors: Design, Synthesis, Bioactivities, and Computational Studies
Sarfraz, M., Ayyaz, M., Rauf, A., Yaqoob, A., Tooba, Ali, M. A., Siddique, S. A., Qureshi, A. M., Sarfraz, M. H., Aljowaie, R. M., et al. (2024) · ACS Omega · doi:10.1021/acsomega.3c09393 · Cited by 19
Genetic diversity of MERS-CoV spike protein gene in Saudi Arabia
Sohrab, S. S., & Azhar, E. I. (2019) · Journal of Infection and Public Health · doi:10.1016/j.jiph.2019.11.007 · Cited by 19
“They ave single stranded positive-sense RNA genome with ∼26–32 kb n size [1,2].”
Background
COVID-19 and Hematology—What Do We Know So Far?
Khandait, H. V., Gandotra, G., Sachdeva, S., Kramer, C., Nye, D. M. R., Golamari, R. R., & Jain, R. (2020) · SN Comprehensive Clinical Medicine · doi:10.1007/s42399-020-00607-3 · Cited by 19
Phylogeography and evolutionary dynamics analysis of porcine delta‐coronavirus with host expansion to humans
Li, G., Zhai, S., Zhou, X., Chen, T., Niu, J., Xie, Y., Si, G., Cong, F., Chen, R., & He, D. (2022) · Transboundary and Emerging Diseases · doi:10.1111/tbed.14503 · Cited by 19
Porcine Respiratory Coronavirus (PRCV): Isolation and Characterization of a Variant PRCV from USA Pigs
Rawal, G., Yim‐Im, W., Aljets, E. K., Halbur, P. G., Zhang, J., & Opriessnig, T. (2023) · Pathogens · doi:10.3390/pathogens12091097 · Cited by 19
Optimization of a DNA Vaccine Against SARS
Zakhartchouk, A. N., Viswanathan, S., Moshynskyy, I., Petric, M., & Babiuk, L. A. (2007) · DNA and Cell Biology · doi:10.1089/dna.2007.0616 · Cited by 19
“…(1) those with a clear homology to other coronaviruses and for which functions are proposed (such ORFs include the replicase and the structural genes) and (2) those with no clear homology to any known genes and often referred to as accessory or group-speciﬁc genes (Weiss and Navas-Martin, 2005).”
Prevention of Cytotoxic T Cell Escape Using a Heteroclitic Subdominant Viral T Cell Determinant
Butler, N. S., Theodossis, A., Webb, A. I., Nastovska, R., Ramarathinam, S. H., Dunstone, M. A., Rossjohn, J., Purcell, A. W., & Perlman, S. M. (2008) · PLoS Pathogens · doi:10.1371/journal.ppat.1000186 · Cited by 19
“One possible explanation for this result is that S598 is not as plastic as S510, even though both determinants are derived from a region of the spike gene that is hypervariable and even deleted in some strains of MHV [32].”
BackgroundInfluential
Structural and Biological Basis of CTL Escape in Coronavirus-Infected Mice
Butler, N. S., Theodossis, A., Webb, A. I., Dunstone, M. A., Nastovska, R., Ramarathinam, S. H., Rossjohn, J., Purcell, A. W., & Perlman, S. M. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.180.6.3926 · Cited by 19
The New Coronavirus (SARS-CoV-2): A Comprehensive Review on Immunity and the Application of Bioinformatics and Molecular Modeling to the Discovery of Potential Anti-SARS-CoV-2 Agents
Boas, G. R. V., Rescia, V. C., Paes, M. M., Lavorato, S. N., de Magalhães-Filho, M. F., Cunha, M. S., Simões, R. D. C., de Lacerda, R. B., de Freitas-Júnior, R. S., Ramos, B. H. D. S., et al. (2020) · Molecules · doi:10.3390/molecules25184086 · Cited by 19
Identification of SARS-CoV-2 CTL epitopes for development of a multivalent subunit vaccine for COVID-19
Rencilin, C. F., Rosy, J. C., Mohan, M., Coico, R., & Sundar, K. (2021) · Infection Genetics and Evolution · doi:10.1016/j.meegid.2021.104712 · Cited by 19

Authors: Weiss, S. R., & Navas-Martin, S.
Affiliations: University of Pennsylvania (US)
Department of Microbiology and Immunology, Center for Molecular Medicine and Infectious Disease, Drexel College of Medicine, Philadelphia, Pennsylvania
Corresponding author: Weiss, Susan R.
ORCID: Weiss, Susan R.
Venue: Microbiology and Molecular Biology Reviews
Publisher: American Society for Microbiology
Published: 2005-12
Volume: 69
Issue: 4
Pages: 635-664
ISSN: 1092-2172 (ISSN-L)
1098-5557
DOI: 10.1128/mmbr.69.4.635-664.2005
PMC: PMC1306801
OpenAlex: W2131988685
Cited by: 1,256
References: 391
Citations by year: 2026: 14 · 2025: 39 · 2024: 69 · 2023: 80 · 2022: 149 · 2021: 253 · 2020: 352 · 2019: 18 · 2018: 12 · 2017: 19 · 2016: 24 · 2015: 14 · 2014: 33 · 2013: 23 · 2012: 18
FWCI: 3.70
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: journals.asm.org/non-commercial-tdm-license (tdm)
Locations: Microbiology and Molecular Biology Reviews (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Multiple Sclerosis Society
Drexel University
Multiple Sclerosis Society
National Institutes of Health
National Institute of Allergy and Infectious Diseases (AI 17418, AI-47800, N01 AI060021, R01AI047800, R01AI060021, R01AI017418, AI60021)
National Institute of Neurological Disorders and Stroke (R01NS021954, NS-21954, NS-30606, P01NS030606)
Topics: Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Animal Virus Infections Studies
Health Sciences › Medicine › Infectious Diseases › Viral Infections and Outbreaks Research
Keywords: coronavirus pathogenesis, severe acute respiratory syndrome coronavirus, SARS-CoV, animal coronaviruses, mouse hepatitis virus, reverse genetics, coronavirus proteins, SARS, animal models of infection, vaccine development, antiviral therapy, emerging pathogens
MeSH terms: Animals, Cats, Cattle, Disease Models, Animal, Humans, Viral Proteins, Viral Vaccines, Virion, Coronavirus, Coronavirus Infections, Severe Acute Respiratory Syndrome, Severe acute respiratory syndrome-related coronavirus, Mice

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Coronavirus Pathogenesis and the Emerging Pathogen Severe Acute Respiratory Syndrome Coronavirus

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