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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.
Coronaviruses infect many species of animals, including humans. Coronaviruses have been described for more than 50 years; the isolation of the prototype murine coronavirus strain JHM, for example, was reported in 7 , The molecular mechanisms of replication as well as the pathogenesis of several coronaviruses have been actively studied since the s. Some of the animal viruses, such as porcine transmissible gastroenteritis virus TGEV , bovine coronavirus BCoV , and avian infectious bronchitis viruses IBV , are of veterinary importance.
The murine coronavirus mouse hepatitis virus MHV is studied as a model for human disease. This family of viruses remained relatively obscure, probably because there were no severe human diseases that could definitely be attributed to coronaviruses; human coronaviruses caused only the common cold.
However, in the spring of , when it became clear that a new human coronavirus was responsible for severe acute respiratory syndrome SARS , coronaviruses became much more recognized. Since the SARS epidemic, two new human respiratory coronaviruses have been described.
In this review we discuss the pathogenesis of the previously known coronaviruses. It has become evident that the body of information gathered over the last 30 years regarding coronavirus replication and pathogenesis has helped to begin understanding of the origin and the biology of SARS-CoV. In , the Coronaviridae family was established by the International Committee on the Taxonomy of Viruses. The Coronaviridae family, along with the Arteviridae and Roniviridae families, form the Nidovirales order.
The Arteviridae family includes swine and equine pathogens, and the Roniviridae family is composed of invertebrate viruses 64 , Group II also includes pathogens of veterinary relevance, such as BCoV, porcine hemagglutinating encephalomyelitis virus, and equine coronavirus, as well as human coronaviruses viruses OC43 and NL63, which, like HCoVE, also cause respiratory infections.
Group II also includes viruses that infect both mice and rats. MHV is often studied as a prototype coronavirus; MHV is a group of highly related strains causing a variety of diseases, such as enteric disease, hepatitis, and respiratory disease, as well as encephalitis and chronic demyelination.
Rat sialodacryoadenitis coronavirus also belongs to group II. Recently, using reverse transcription-PCR RT-PCR , coronavirus sequences were detected in the graylag goose Anser anser , feral pigeon Columbia livia , and mallard Anas platyrhynchos ; phylogenetic analyses of the replicase and nucleocapsid N sequences suggest that these viruses are members of group III, but as yet they have not been isolated or characterized.
Coronaviruses cause acute and chronic respiratory, enteric, and central nervous system CNS diseases in many species of animals, including humans The pathogenesis of a few of these will be reviewed below. There had long been speculation about the association of human coronaviruses with more serious human diseases such as multiple sclerosis 33 , hepatitis , or enteric disease in newborns However, none of these early associations had been substantiated.
The recently identified SARS-CoV, which was shown to cause a severe acute respiratory syndrome was the first example of serious illness in humans caused by a coronavirus and will be discussed in detail in below. Since the identification of SARS-CoV, there have been reports of two new human coronaviruses associated with respiratory disease. This virus has been difficult to propagate in cell culture, and there is little information available about the biology of this virus.
HCoV-NL63 is a group I coronavirus isolated from a 7-month-old child in The Netherlands who was suffering from bronchiolitis and conjunctivitis , It has subsequently been reported in other parts of the world, including Canada 12 , Japan 86 , Hong Kong 52 , Australia 5 , and Belgium HCoV-NL63 is associated with serious respiratory symptoms, including upper respiratory infection, bronchiolitis, and pneumonia The strong correlation of the presence of NL63 with croup in children with lower respiratory infections has suggested a causal relationship between the virus and croup While primarily associated with infections of children, NL63 has been also been detected in immunocompromised adults with respiratory tract infections.
That group has suggested that this virus is associated with Kawasaki's disease in children 92 ; however, this has been disputed by two other reports 14 , While little is known about the pathogenesis of any of the human coronaviruses E, OC43, HKU1, NL63, and SARS-CoV , there have been detailed studies of the pathogenesis of some of the animal coronaviruses, which may contribute to the understanding of the human viruses.
We summarize some of these data below. There are many strains of murine coronavirus, or MHV, exhibiting different tropisms and levels of virulence. The commonly used laboratory strains infect primarily the liver and the brain and thus provide animal models for encephalitis and hepatitis as well as the immune-mediated demyelinating disease that develops late after infection, peaking at about 1 month postinfection MHV infection of the mouse is regarded as one of the best animal models for the study of demyelinating diseases such as multiple sclerosis.
Other strains cause enteric disease, are spread easily by an oral-fecal route in animal colonies, and are a particular danger to immunocompromised animals The extensive studies of the pathogenesis of MHV and the resulting host immune response have been reviewed , , It is clear that the level of virulence as well as the tropism of MHV strains results from the interplay of viral gene products and the host immune response. The contributions of individual viral genes to tropism and pathogenic phenotype are discussed later in this review.
The role of the immune response to MHV infection in viral clearance and pathogenesis in the CNS has been well characterized Both antibody- and cell-mediated immune responses are required to protect against coronavirus infections. These and other data suggest that the development of demyelination depends on adequate spread of virus during the acute stage. MHV T-cell epitopes have been mapped to several structural proteins; there may be additional epitopes, however, in the two-thirds of the genome that encodes the replicase proteins, a portion of the genome that has not yet been examined for epitopes.
Neutralizing B-cell epitopes have been mapped primarily to the spike proteins, but nonneutralizing epitopes have been identified in the other viral structural proteins 68 , 69 , , While MHV is cleared primarily by the cell-mediated immune response, in the absence of B cells, antibodies are essential to prevent reemergence of the virus in the CNS after initial T-cell mediated clearance. Interestingly, the requirement does not pertain to virus replication and clearance in the liver , The increase in chemokines is associated with high levels of macrophages and neutrophils during acute infection and also in later demyelination stages Recombinant virus studies suggest that the macrophage infiltration may be influenced by the S protein ; K.
Iacono and S. Weiss, unpublished data. The most neurovirulent isolate of JHM fails to induce a significant T-cell response; the resulting inability of the host to clear virus is likely responsible for the high mortality even at low doses of virus These data suggest that MHV-2 may have a specific mechanism for evading the immune response. There are several porcine coronaviruses that have been studied reviewed in references 89 , , and Transmissible gastroenteritis virus was recognized in It is a major cause of viral enteritis and fetal diarrhea in swine; it is most severe in neonates, with mortality resulting in significant economic loss In neonates, TGEV infects epithelial cells of the small intestines, leading to potentially fatal gastroenteritis.
Infection also occurs in the upper respiratory tract and, less often, in the lungs In adults, TGEV causes mild disease. PRCoV infects lung epithelial cells, and antigen is found in type I and type II pneumocytes as well as alveolar macrophages; infection is followed by interstitial pneumonia. Thus, emergence of PRCoV from TGEV resulted from deletions within the spike gene and is an example of evolution of a coronavirus with altered tissue tropism as well as reduced virulence Various types of vaccines have been evaluated for protection against TGEV , Immunization of pregnant swine with attenuated TGEV is not sufficient to protect suckling pigs from infection.
Inoculation of young pigs directly with attenuated virus is also unable to stimulate enough immunoglobulin A IgA -secreting cells in the intestines to protect against TGEV. However, sows recovering from virulent TGEV infection do produce enough milk IgA to protect suckling pigs from infection and diarrhea. Subunit vaccines using spike and nucleocapsid proteins have also been tested.
The spike protein of TGEV has four major antigenic sites, two of which are neutralizing. While these vaccines are unable to induce either passive or active protection against TGEV, they are able to boost responses in animals vaccinated with attenuated TGEV. This virus appeared in Europe in the late s into the s and spread to Asia, but it has not been reported in the United States Another porcine coronavirus, hemagglutinating enteric coronavirus, is a group II virus, antigenically unrelated to the other porcine viruses.
IBV causes a highly contagious disease in chickens; it is spread by aerosol and thus is of considerable economic importance to the poultry industry. IBV, which has also reported in pheasants and turkeys, replicates in upper respiratory tissues, with infection of bronchi and severe disease in young animals. Some strains of IBV cause more systemic infections, replicating in other tissues, including the kidney causing nephritis , the oviduct causing decreased egg production , and the gut , While chickens of all ages are susceptible, very young chicks exhibit more severe respiratory signs and much higher mortality than older birds While the mechanisms of protection against IBV-induced disease are not completely clear, high levels of antibodies are believed to prevent spread of virus from the respiratory tract to other organs.
Maternal antibodies have also been shown to protect against IBV infection during the first 2 weeks of life. Both live attenuated and inactivated vaccines have been developed and used to protect against IBV.
Protection from live vaccines may be short lived, and serotype-specific and inactivated vaccines are unable to protect alone. However, inactivated vaccines may be used to boost birds that have been primed with live attenuated vaccine. Further difficulties in inducing protection by vaccination are due to the multiple serotypes of IBV, which are often not cross protective. The feline coronaviruses are composed of two biotypes.
Feline enteric coronavirus FeCoV , commonly found in multicat environments in an asymptomatic carrier state, causes seroconversion. FIPV, a less common variant of FeCoV, has the ability to replicate in macrophages, causing a severe and lethal disease.
FIPV replicates initially in pharyngeal respiratory or intestinal epithelial cells. Infection of macrophages then leads to viremia and systemic spread of the virus, including inflammation of the abdominal and thoracic cavities and causing occasional ocular and neurological disorders 1 , A complication of FIPV infection involves immune-mediated pathology This has presented a great challenge to vaccine development for FIPV.
It has been shown that after vaccination against spike protein, cats challenged with FIPV develop an early-death syndrome caused by antibody-dependent enhancement of virus infection. A DNA vaccine approach, directed against the N and M proteins followed by the same to protein-expressed vial vaccinia virus, also has not been successful. Thus, the development of a vaccine against FIPV remains a challenge BCoV is a ubiquitous virus worldwide as measured by serology.
BCoV causes both respiratory and enteric disease, including calf diarrhea, winter dysentery in adults, and respiratory infections in cattle of all ages, including those with shipping fever.
Viruses isolated from cattle with either respiratory or enteric disease are antigenically similar. Epidemiological studies suggest that serum antibody correlates with immunity. There are currently no vaccines available to prevent BCoV-associated disease ,
Coronavirus Pathogenesis and the Emerging Pathogen Severe Acute Respiratory Syndrome Coronavirus
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