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Preliminary PCR-Based Screening Indicates a Higher Incidence of Porcine Endogenous Retrovirus Subtype C (PERV-C) in Feral Versus Domestic Swine

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Preliminary PCR-Based Screening Indicates a Higher Incidence of Porcine Endogenous Retrovirus Subtype C (PERV-C) in Feral Versus Domestic Swine Fort Hays State University FHSU Scholars Repository Biology Faculty Publications Biology 2019 Preliminary PCR-based screening indicates a higher incidence of Porcine Endogenous Retrovirus subtype C (PERV-C) in feral versus domestic swine Rashmi Acharya Zoey K. Wallis Robert Keener Eric T. Gillock Follow this and additional works at: https://scholars.fhsu.edu/biology_facpubs Part of the Biology Commons TRANSACTIONS OF THE KANSAS Vol. 122, no. 3-4 ACADEMY OF SCIENCE p. 257-263 (2019) Preliminary PCR-based screening indicates a higher incidence of Porcine Endogenous Retrovirus subtype C (PERV-C) in feral versus domestic swine RASHMI ACHARYA1, ZOEY K. WALLIS1, ROBERT J. KEENER2 AND ERIC T. GILLOCK1 1. Department of Biological Sciences, Fort Hays State University, Hays, Kansas [email protected] 2. Department of Agriculture, Fort Hays State University, Hays, Kansas Xenotransplantation is considered a potential alternative to allotransplantation to relieve the current shortage of human organs. Due to their similar size and physiology, the organs of pigs are of particular interest for this purpose. Endogenous retroviruses are a result of integration of retroviral genomes into the genome of infected germ cells as DNA proviruses, which are then carried in all cells of the offspring of the organism. Porcine endogenous retroviruses (PERVs) are of special concern because they are found in pig organs and tissues that might otherwise be used for xenotransplantation. PERV proviruses can be induced to replicate and recombine in pigs, and have been shown to infect human cells in vitro. There are three subtypes of PERVs based on differences in the receptor binding domain of the env protein; PERV-A, PERV-B, and PERV-C. PERVs A and B can infect human cells in vitro and can recombine with PERV-C, resulting in a recombinant virus with a higher rate of replication in pig and human cell lines. In this study, we used a PCR-based analysis of 50 domestic and 35 feral pigs to study the distribution of PERVs A, B, and C in swine raised under domestic conditions, versus feral swine from rural areas. PERV-A and PERV-B were universal in both domestic and feral swine. Feral swine had a higher incidence of PERV-C (85.7%) compared to domestic swine (42.0%). Further studies in other feral swine herds are ongoing to verify this observation. Keywords: Porcine endogenous retroviruses, domestic swine, feral swine, PCR analysis INTRODUCTION implantation, or infusion into a human recipient of either 1) live cells, tissues, or Xenotransplantation, the transplantation organs from a nonhuman animal source, of living cells, tissues, and organs between or 2) human body fluids, cells, tissues, or species, is a widely suggested alternative organs that have had ex vivo contact with to allotransplantation due to the shortage of live nonhuman animal cells, tissues or viable donated organs (Denner and Tönjes organs (Gola and Mazurek 2014). Although 2012; Takeuchi et al. 1998). As of August promising, xenotransplantation carries its own 2018, there were over 114,000 candidates on challenges and risks that include physiological transplantation waiting list in the United States, incompatibilities, immunological rejection, and and only approximately 10,100 donors (Organ transmission of infectious agents. Introducing Procurement and Transplantation Network animal tissue and its microbiological flora into [https://optn.transplant.hrsa.gov]). the human system and lowering the natural host defense mechanisms for the integration of According to the United States Public Health the organ provides opportunity for transmission Service, xenotransplantation includes any of xenogenic infections crossing the species procedure that involves the transplantation, barrier (Brown et al. 1998). Suppressing the 258 Acharya, Wallis, Keener and Gillock recipient’s immune system is a mandatory integrated provirus passed to the offspring step in transplantation of organs, to avoid and inherited in Mendelian fashion: this is organ rejection. This, however, also makes known as an endogenous retrovirus (ERV) the recipient more susceptible to infection that (Jern and Coffin 2008). It has been postulated might otherwise be easily controlled. in some cases that ERVs may provide some evolutionary advantage to the offspring, The virulence and clinical outcome of perhaps allowing the survival of an epidemic of infectious agents are highly unpredictable the exogenous form of the virus (Brown et al. when they enter a new species and cause 1998). Once integrated into the host genome, infections. Brown et al. (1998) demonstrated these viruses tend to accumulate random this phenomenon in the case of cercopithecine mutations with time, eventually leading to an herpes-virus 1 (B virus). In its natural host, inactive ERV remnant. the macaque monkey, it causes persistent latent infection with intermittent, recurrent ERVs are present in all vertebrate species mucocutaneous disease. However in humans, studied thus far, with a majority of ERVs it causes fatal meningoencephalitis (Brown being inactive. However, of those that are et al. 1998). Because cases of xenographic active and replication competent, some have transmission of infectious diseases in humans been associated with spontaneous tumors as in have not yet been identified, evidence from endogenous murine leukemia viruses (MLV) human retroviral infections and natural and mouse mammary tumor viruses (MMTV) occurring zoonoses like AIDS have been used (Frankel et al. 1990; Stoye 2001). Vertebrates to assess transplant-related risks of retroviral have, over time, developed a variety of infections and epidemics in humans (Brown silencing mechanisms to limit the activity of et al. 1998). Human retroviral infections newly-acquired, replication-competent ERVs. commonly manifest as neurological disorders, These silencing mechanisms are generally less immunodeficiencies, and long-latency effective in cases of viruses that have switched malignancies for which there are limited hosts (Hayward and Katzourakis 2015) treatments available (Gallo 1995; Brown et and thus exposure to ERVs from different al. 1998). As such, due to the high risk of vertebrate species poses a risk of infections. retroviral infections, the concerns associated with xenotransplantation are legitimate from a Pigs are one of the preferred choices for public health perspective. xenotransplantation because of anatomical and physiological similarities to humans, relatively Retroviruses have an unconventional life cycle short generation time, and ease of production compared to other viruses. Their life cycle starts of transgenic pigs (Cozzi et al. 2009; Gola and with reverse transcription of the viral RNA Mazurek 2014). The phylogenetic distance genome to DNA, followed by integration of the between pigs and humans reduces the risk of newly formed DNA into the host genome as transmission of viral infections, with screening a provirus. The provirus is then transcribed to and qualified breeding further lowering the risk produce the RNA genome and messenger RNA of other zoonotic infections (Gola and Mazurek (mRNA). The mRNA directs translation of 2014). However, the presence of porcine viral proteins and processing of viral particles, endogenous retroviruses (PERVs) and their resulting in budding and release of new virions capability to produce viral particles, hinders the from host cell (Jern and Coffin 2008). use of porcine tissue xenografts. Although retroviruses usually infect somatic According to the International Committee on cells, occasionally infection of a germline the Taxonomy of Viruses (ICTV), PERVs are cell by a retrovirus may occur, leading to an classified as family: Retroviridae, subfamily: Transactions of the Kansas Academy of Science 122(3-4), 2019 259 Orthoretrovirinae, genus: Gammaretrovirus, (Niu et al. 2017). Currently, the use of these Porcine type-C oncovirus species (Virus PERV-inactivated pigs is limited to research, Taxonomy: The 9th Report of the ICTV and are not approved for human trials. 2011). Retroviruses have been infecting mammalian species for more than 100 million Currently, there is limited information about years according to genomic fossil records and the evolutionary history, distribution patterns, gammaretroviruses as a group have jumped roles and potential infectious capability of between species frequently (Hayward and PERVs. A better understanding of PERVs is Katzourakis 2015). There are three replication essential to prevent the possible emergence competent subtypes of PERVs: PERV-A, of novel xenozoonoses from pig to human PERV-B, and PERV-C, which are identified transplantations. The purpose of this research based on differences in the receptor binding was to study and compare the distribution of domain of the env protein. PERVs A and B are the three types of PERVs in feral and domestic present in the genomes of all pigs and are able varieties of pigs. Although with proper to infect human cells in vitro, as well as cells containment of domestic herds, the likelihood of other species (Wilson et al. 1998; Denner of PERV transmission from a feral pig into a and Tönjes 2012). PERV-C is integrated into domestic herd is low, it is nonetheless possible. the genomes of many, but not all, pigs and is restricted to infecting pig cells (Takeuchi et al. MATERIALS AND METHODS 1998; Denner 2016). Sample collection: The total sample size The origin of PERVs was most likely a murine for this study was 85 samples. Tails from retrovirus (Denner and Tönjes 2012). Due 50 domestic piglets
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