Induction of PERV antigen in porcine peripheral blood mononuclear cells by human herpesvirus 1
Background Xenotransplantation represents one of alternative candidates for allotransplantation due to the chronic shortage of suitable human tissues; however, many obstacles remain. Expression and release of endogenous retroviral antigens by porcine cells after transplantation may evoke adverse imm...
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| Published in | Xenotransplantation (Københaven) Vol. 22; no. 2; pp. 144 - 150 |
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| Main Authors | , , |
| Format | Journal Article |
| Language | English |
| Published |
Denmark
Blackwell Publishing Ltd
01.03.2015
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| Subjects | |
| Online Access | Get full text |
| ISSN | 0908-665X 1399-3089 1399-3089 |
| DOI | 10.1111/xen.12160 |
Cover
| Abstract | Background
Xenotransplantation represents one of alternative candidates for allotransplantation due to the chronic shortage of suitable human tissues; however, many obstacles remain. Expression and release of endogenous retroviral antigens by porcine cells after transplantation may evoke adverse immune responses in human subjects. Here, we examined whether human herpesvirus 1 (HHV‐1) could induce the production of porcine endogenous retrovirus (PERV) antigens in porcine peripheral blood mononuclear cells (PBMCs).
Methods
Porcine PBMCs were infected with HHV‐1 and examined for the production of PERV Gag protein and HHV‐1 using antigen‐capture ELISA and quantitative real‐time polymerase chain reaction (PCR), respectively.
Results
HHV‐1 infection resulted in a 1.7‐ to 33.2‐fold induction of PERV Gag relative to mock infection controls, compared to a 2.9‐ to 12.9‐fold induction following treatment with PMA. Expression of PERV Gag was detected in porcine PBMCs and PK‐15 cells after HHV‐1 infection by double immunofluorescence staining of PERV Gag and HHV‐1 antigen. The viability of HHV‐1‐infected porcine PBMCs was significantly lower than that of mock‐infected cells. The HHV‐1 level in the culture supernatant increased 5.2‐fold relative to controls 24‐h post‐infection, indicative of active replication within these cells; decreased levels of HHV‐1 were detected 72‐h post‐infection.
Conclusions
These results suggest that HHV‐1 may be capable of infecting transplanted porcine cells, resulting in strong direct induction of PERV antigen. |
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| AbstractList | Xenotransplantation represents one of alternative candidates for allotransplantation due to the chronic shortage of suitable human tissues; however, many obstacles remain. Expression and release of endogenous retroviral antigens by porcine cells after transplantation may evoke adverse immune responses in human subjects. Here, we examined whether human herpesvirus 1 (HHV-1) could induce the production of porcine endogenous retrovirus (PERV) antigens in porcine peripheral blood mononuclear cells (PBMCs). Porcine PBMCs were infected with HHV-1 and examined for the production of PERV Gag protein and HHV-1 using antigen-capture ELISA and quantitative real-time polymerase chain reaction (PCR), respectively. HHV-1 infection resulted in a 1.7- to 33.2-fold induction of PERV Gag relative to mock infection controls, compared to a 2.9- to 12.9-fold induction following treatment with PMA. Expression of PERV Gag was detected in porcine PBMCs and PK-15 cells after HHV-1 infection by double immunofluorescence staining of PERV Gag and HHV-1 antigen. The viability of HHV-1-infected porcine PBMCs was significantly lower than that of mock-infected cells. The HHV-1 level in the culture supernatant increased 5.2-fold relative to controls 24-h post-infection, indicative of active replication within these cells; decreased levels of HHV-1 were detected 72-h post-infection. These results suggest that HHV-1 may be capable of infecting transplanted porcine cells, resulting in strong direct induction of PERV antigen. Xenotransplantation represents one of alternative candidates for allotransplantation due to the chronic shortage of suitable human tissues; however, many obstacles remain. Expression and release of endogenous retroviral antigens by porcine cells after transplantation may evoke adverse immune responses in human subjects. Here, we examined whether human herpesvirus 1 (HHV-1) could induce the production of porcine endogenous retrovirus (PERV) antigens in porcine peripheral blood mononuclear cells (PBMCs). Porcine PBMCs were infected with HHV-1 and examined for the production of PERV Gag protein and HHV-1 using antigen-capture ELISA and quantitative real-time polymerase chain reaction (PCR), respectively. HHV-1 infection resulted in a 1.7- to 33.2-fold induction of PERV Gag relative to mock infection controls, compared to a 2.9- to 12.9-fold induction following treatment with PMA. Expression of PERV Gag was detected in porcine PBMCs and PK-15 cells after HHV-1 infection by double immunofluorescence staining of PERV Gag and HHV-1 antigen. The viability of HHV-1-infected porcine PBMCs was significantly lower than that of mock-infected cells. The HHV-1 level in the culture supernatant increased 5.2-fold relative to controls 24-h post-infection, indicative of active replication within these cells; decreased levels of HHV-1 were detected 72-h post-infection. These results suggest that HHV-1 may be capable of infecting transplanted porcine cells, resulting in strong direct induction of PERV antigen. Xenotransplantation represents one of alternative candidates for allotransplantation due to the chronic shortage of suitable human tissues; however, many obstacles remain. Expression and release of endogenous retroviral antigens by porcine cells after transplantation may evoke adverse immune responses in human subjects. Here, we examined whether human herpesvirus 1 (HHV-1) could induce the production of porcine endogenous retrovirus (PERV) antigens in porcine peripheral blood mononuclear cells (PBMCs).BACKGROUNDXenotransplantation represents one of alternative candidates for allotransplantation due to the chronic shortage of suitable human tissues; however, many obstacles remain. Expression and release of endogenous retroviral antigens by porcine cells after transplantation may evoke adverse immune responses in human subjects. Here, we examined whether human herpesvirus 1 (HHV-1) could induce the production of porcine endogenous retrovirus (PERV) antigens in porcine peripheral blood mononuclear cells (PBMCs).Porcine PBMCs were infected with HHV-1 and examined for the production of PERV Gag protein and HHV-1 using antigen-capture ELISA and quantitative real-time polymerase chain reaction (PCR), respectively.METHODSPorcine PBMCs were infected with HHV-1 and examined for the production of PERV Gag protein and HHV-1 using antigen-capture ELISA and quantitative real-time polymerase chain reaction (PCR), respectively.HHV-1 infection resulted in a 1.7- to 33.2-fold induction of PERV Gag relative to mock infection controls, compared to a 2.9- to 12.9-fold induction following treatment with PMA. Expression of PERV Gag was detected in porcine PBMCs and PK-15 cells after HHV-1 infection by double immunofluorescence staining of PERV Gag and HHV-1 antigen. The viability of HHV-1-infected porcine PBMCs was significantly lower than that of mock-infected cells. The HHV-1 level in the culture supernatant increased 5.2-fold relative to controls 24-h post-infection, indicative of active replication within these cells; decreased levels of HHV-1 were detected 72-h post-infection.RESULTSHHV-1 infection resulted in a 1.7- to 33.2-fold induction of PERV Gag relative to mock infection controls, compared to a 2.9- to 12.9-fold induction following treatment with PMA. Expression of PERV Gag was detected in porcine PBMCs and PK-15 cells after HHV-1 infection by double immunofluorescence staining of PERV Gag and HHV-1 antigen. The viability of HHV-1-infected porcine PBMCs was significantly lower than that of mock-infected cells. The HHV-1 level in the culture supernatant increased 5.2-fold relative to controls 24-h post-infection, indicative of active replication within these cells; decreased levels of HHV-1 were detected 72-h post-infection.These results suggest that HHV-1 may be capable of infecting transplanted porcine cells, resulting in strong direct induction of PERV antigen.CONCLUSIONSThese results suggest that HHV-1 may be capable of infecting transplanted porcine cells, resulting in strong direct induction of PERV antigen. Background Xenotransplantation represents one of alternative candidates for allotransplantation due to the chronic shortage of suitable human tissues; however, many obstacles remain. Expression and release of endogenous retroviral antigens by porcine cells after transplantation may evoke adverse immune responses in human subjects. Here, we examined whether human herpesvirus 1 (HHV‐1) could induce the production of porcine endogenous retrovirus (PERV) antigens in porcine peripheral blood mononuclear cells (PBMCs). Methods Porcine PBMCs were infected with HHV‐1 and examined for the production of PERV Gag protein and HHV‐1 using antigen‐capture ELISA and quantitative real‐time polymerase chain reaction (PCR), respectively. Results HHV‐1 infection resulted in a 1.7‐ to 33.2‐fold induction of PERV Gag relative to mock infection controls, compared to a 2.9‐ to 12.9‐fold induction following treatment with PMA. Expression of PERV Gag was detected in porcine PBMCs and PK‐15 cells after HHV‐1 infection by double immunofluorescence staining of PERV Gag and HHV‐1 antigen. The viability of HHV‐1‐infected porcine PBMCs was significantly lower than that of mock‐infected cells. The HHV‐1 level in the culture supernatant increased 5.2‐fold relative to controls 24‐h post‐infection, indicative of active replication within these cells; decreased levels of HHV‐1 were detected 72‐h post‐infection. Conclusions These results suggest that HHV‐1 may be capable of infecting transplanted porcine cells, resulting in strong direct induction of PERV antigen. |
| Author | Kim, Jiyeon Kim, Jung Heon Hwang, Eung Soo |
| Author_xml | – sequence: 1 givenname: Jiyeon surname: Kim fullname: Kim, Jiyeon organization: Department of Microbiology and Immunology, Seoul National University College of Medicine, Seoul, Korea – sequence: 2 givenname: Jung Heon surname: Kim fullname: Kim, Jung Heon organization: Department of Microbiology and Immunology, Seoul National University College of Medicine, Seoul, Korea – sequence: 3 givenname: Eung Soo surname: Hwang fullname: Hwang, Eung Soo email: hesss@snu.ac.kr organization: Department of Microbiology and Immunology, Seoul National University College of Medicine, Seoul, Korea |
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| Keywords | xenotransplantation human herpesvirus porcine endogenous retrovirus Gag porcine cells |
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| References | Nyberg SL, Hibbs JR, Hardin JA et al. Influence of human fulminant hepatic failure sera on endogenous retroviral expression in pig hepatocytes. Liver Transpl 2000; 6: 76-84. Heneine W, Tibell A, Switzer WM et al. No evidence of infection with porcine endogenous retrovirus in recipients of porcine islet-cell xenografts. Lancet 1998; 352: 695-699. Nicuolo GD, D'Alessandro A, Andria B et al. Long-term absence of porcine endogenous retrovirus infection in chronically immunosuppressed patients after treatment with the porcine cell-based Academic Medical Center bioartificial liver. Xenotransplantation 2010; 17: 431-439. Millard AL, Häberli L, Sinzger C et al. Efficiency of porcine endothelial cell infection with human cytomegalovirus depends on both virus tropism and endothelial cell vascular origin. Xenotransplantation 2010; 17: 274-287. Vincenti F, Kirk AD. What's next in the pipeline. Am J Transplant 2008; 8: 1972-1981. Ghielmetti M, Millard AL, Haeberli L et al. Human CMV infection of porcine endothelial cells increases adhesion receptor expression and human leukocyte recruitment. Transplantation 2009; 87: 1792-1800. Löwer J, Davidson EA, Teich NM et al. Heterophil human antibodies recognize oncovirus envelope antigens: epidemiological parameters and immunological specificity of the reaction. Virology 1981; 109: 409-417. Denner J. Immunosuppression by retroviruses: implications for xenotransplantation. Ann NY Acad Sci 1998; 862: 75-86. Bate SL, Dollard SC, Cannon MJ. Cytomegalovirus seroprevalence in the United States: the national health and nutrition examination surveys, 1988-2004. Clin Infect Dis 2010; 50: 1439-1447. Scobie L, Taylor S, Logan NA et al. Characterization of germline porcine endogenous retroviruses from Large White pig. J Gen Virol 2004; 85: 2421-2428. Paradis K, Langford G, Long Z et al. Search for cross-species transmission of porcine endogenous retrovirus in patients treated with living pig tissue. Science 1999; 285: 1236-1241. Bittmann I, Mihica D, Plesker R et al. Expression of porcine endogenous retroviruses (PERV) in different organs of a pig. Virology 2012; 433: 329-336. Tacke S, Bodusch K, Berg A et al. Sensitive and specific detection methods for porcine endogenous retroviruses applicable to experimental and clinical xenotransplantation. Xenotransplantation 2001; 8: 125-135. Kim JH, Jung ES, Kwon Y et al. Infection of porcine cells with human herpesviruses. Transplant Proc 2010; 42: 2134-2137. Gaines H, von Sydow M, Sönnerborg A et al. Antibody response in primary human immunodeficiency virus infection. Lancet 1987; 329: 1249-1253. Garkavenko O, Croxson MC, Irgang M et al. Monitoring for presence of potentially xenotic viruses in recipients of pig islet xenotransplantation. J Clin Microbiol 2004; 42: 5353-5356. Cha CY, Hwang ES, Kook YH. Production and characterization of monoclonal antibodies specific to herpes simplex viruses. J Korean Soc Microbiol 1988; 23: 505-515. Nahmias AJ, Lee FK, Beckman-Nahmias S. Sero-epidemiological and -sociological patterns of herpes simplex virus infection in the world. Scand J Infect Dis Suppl 1990; 69: 19-36. Grant RF, Windsor SK, Malinak CJ et al. Characterization of infectious type D retrovirus from baboons. Virology 1995; 207: 292-296. 2004; 85 2010; 42 2004; 42 2009; 87 1990; 69 2000; 6 2010; 17 1987; 329 1995; 207 2001; 8 1999; 285 1981; 109 1988; 23 2008; 8 1998; 862 2012; 433 1998; 352 2010; 50 e_1_2_7_6_1 e_1_2_7_5_1 e_1_2_7_4_1 e_1_2_7_3_1 e_1_2_7_7_1 e_1_2_7_19_1 e_1_2_7_18_1 e_1_2_7_17_1 e_1_2_7_16_1 e_1_2_7_2_1 e_1_2_7_15_1 e_1_2_7_14_1 e_1_2_7_13_1 e_1_2_7_12_1 Nahmias AJ (e_1_2_7_9_1) 1990; 69 e_1_2_7_11_1 e_1_2_7_10_1 e_1_2_7_20_1 Cha CY (e_1_2_7_8_1) 1988; 23 |
| References_xml | – reference: Scobie L, Taylor S, Logan NA et al. Characterization of germline porcine endogenous retroviruses from Large White pig. J Gen Virol 2004; 85: 2421-2428. – reference: Nicuolo GD, D'Alessandro A, Andria B et al. Long-term absence of porcine endogenous retrovirus infection in chronically immunosuppressed patients after treatment with the porcine cell-based Academic Medical Center bioartificial liver. Xenotransplantation 2010; 17: 431-439. – reference: Löwer J, Davidson EA, Teich NM et al. Heterophil human antibodies recognize oncovirus envelope antigens: epidemiological parameters and immunological specificity of the reaction. Virology 1981; 109: 409-417. – reference: Bate SL, Dollard SC, Cannon MJ. Cytomegalovirus seroprevalence in the United States: the national health and nutrition examination surveys, 1988-2004. Clin Infect Dis 2010; 50: 1439-1447. – reference: Garkavenko O, Croxson MC, Irgang M et al. Monitoring for presence of potentially xenotic viruses in recipients of pig islet xenotransplantation. J Clin Microbiol 2004; 42: 5353-5356. – reference: Tacke S, Bodusch K, Berg A et al. Sensitive and specific detection methods for porcine endogenous retroviruses applicable to experimental and clinical xenotransplantation. Xenotransplantation 2001; 8: 125-135. – reference: Gaines H, von Sydow M, Sönnerborg A et al. Antibody response in primary human immunodeficiency virus infection. Lancet 1987; 329: 1249-1253. – reference: Paradis K, Langford G, Long Z et al. Search for cross-species transmission of porcine endogenous retrovirus in patients treated with living pig tissue. Science 1999; 285: 1236-1241. – reference: Nyberg SL, Hibbs JR, Hardin JA et al. Influence of human fulminant hepatic failure sera on endogenous retroviral expression in pig hepatocytes. Liver Transpl 2000; 6: 76-84. – reference: Ghielmetti M, Millard AL, Haeberli L et al. Human CMV infection of porcine endothelial cells increases adhesion receptor expression and human leukocyte recruitment. Transplantation 2009; 87: 1792-1800. – reference: Vincenti F, Kirk AD. What's next in the pipeline. Am J Transplant 2008; 8: 1972-1981. – reference: Grant RF, Windsor SK, Malinak CJ et al. Characterization of infectious type D retrovirus from baboons. Virology 1995; 207: 292-296. – reference: Bittmann I, Mihica D, Plesker R et al. Expression of porcine endogenous retroviruses (PERV) in different organs of a pig. Virology 2012; 433: 329-336. – reference: Nahmias AJ, Lee FK, Beckman-Nahmias S. Sero-epidemiological and -sociological patterns of herpes simplex virus infection in the world. Scand J Infect Dis Suppl 1990; 69: 19-36. – reference: Cha CY, Hwang ES, Kook YH. Production and characterization of monoclonal antibodies specific to herpes simplex viruses. J Korean Soc Microbiol 1988; 23: 505-515. – reference: Denner J. Immunosuppression by retroviruses: implications for xenotransplantation. Ann NY Acad Sci 1998; 862: 75-86. – reference: Heneine W, Tibell A, Switzer WM et al. No evidence of infection with porcine endogenous retrovirus in recipients of porcine islet-cell xenografts. Lancet 1998; 352: 695-699. – reference: Kim JH, Jung ES, Kwon Y et al. Infection of porcine cells with human herpesviruses. Transplant Proc 2010; 42: 2134-2137. – reference: Millard AL, Häberli L, Sinzger C et al. Efficiency of porcine endothelial cell infection with human cytomegalovirus depends on both virus tropism and endothelial cell vascular origin. 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2010 end-page: 287 article-title: Efficiency of porcine endothelial cell infection with human cytomegalovirus depends on both virus tropism and endothelial cell vascular origin publication-title: Xenotransplantation – volume: 329 start-page: 1249 year: 1987 end-page: 1253 article-title: Antibody response in primary human immunodeficiency virus infection publication-title: Lancet – volume: 6 start-page: 76 year: 2000 end-page: 84 article-title: Influence of human fulminant hepatic failure sera on endogenous retroviral expression in pig hepatocytes publication-title: Liver Transpl – volume: 17 start-page: 431 year: 2010 end-page: 439 article-title: Long‐term absence of porcine endogenous retrovirus infection in chronically immunosuppressed patients after treatment with the porcine cell–based Academic Medical Center bioartificial liver publication-title: Xenotransplantation – volume: 8 start-page: 1972 year: 2008 end-page: 1981 article-title: What's next in the pipeline publication-title: 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Xenotransplantation represents one of alternative candidates for allotransplantation due to the chronic shortage of suitable human tissues; however,... Xenotransplantation represents one of alternative candidates for allotransplantation due to the chronic shortage of suitable human tissues; however, many... |
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| SubjectTerms | Animals Antigens, Viral - biosynthesis Cell Line Coinfection - immunology Coinfection - virology Endogenous Retroviruses - immunology Endogenous Retroviruses - pathogenicity Enzyme-Linked Immunosorbent Assay - methods Gag Gene Products, gag - biosynthesis Gene Products, gag - immunology HEK293 Cells Herpesvirus 1, Human - pathogenicity Heterografts - virology human herpesvirus Human herpesvirus 1 Humans Leukocytes, Mononuclear - immunology Leukocytes, Mononuclear - virology porcine cells Porcine endogenous retrovirus Swine - virology Swine, Miniature Transplantation, Heterologous - adverse effects xenotransplantation |
| Title | Induction of PERV antigen in porcine peripheral blood mononuclear cells by human herpesvirus 1 |
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