Contribution of the murine and primate models to the study of arenaviral diseases and hemorrhagic fevers

Authors

  • Juan David Rodas G.
  • Roger Hewson
  • María S. Salvato

DOI:

https://doi.org/10.17533/udea.rccp.324453

Keywords:

animal models, arenavirus,, immunology, LCMV

Abstract

Summary

This manuscript is an inedited part of my PhD dissertation, based on historical and recent findings on animal models, that was presented as part of the requirements to fulfill the conditions to become a philosophical doctor on Veterinary Sciences at the University of Wisconsin on October of 2003.The current mini-review written on a free-version style, underlines some of the cornerstones of immunology as a science, understood thanks to the use of the Lymphocytic Choriomeningitis virus (LCMV) experimentally and naturally infected mouse model. It should suffice to say that there have been two Nobel prices of Medicine for discoveries made through the employment of this animal model, in order to recognize the right importance to it. In addition, several laboratories, Dr. Salvato´s among them, have also employed the LCMV-infected Rhesus monkey model as a tool to unravel the mysteries of arenaviral hemorrhagic fever, and particularly the physiopathology of Lassa disease in humans. Here I show some of the knowledge generated through the study of both animal infections.

 

|Abstract
= 57 veces | PDF
= 12 veces|

Downloads

Download data is not yet available.

References

Adler H, Jungi TW, Pfi ster H, Strasser M, Sileghem M et al. Cytokine regulation by virus infection: bovine viral diarrhea virus, a fl avivirus, downregulates production of tumor necrosis factor alpha in macrophages in vitro. J Virol 1996; 70:2650-3.

Ahmed R, Salmi A, Butler LD, Chiller JM, and Oldstone MB. Selection of genetic variants of lymphocytic choriomeningitis virus in spleens of persistently infected mice. Role in suppression of cytotoxic T lymphocyte response and viral persistence. J Exp Med 1984; 160:521-40.

Alcami A, and Smith GL. Vaccinia, cowpox, and camelpox viruses encode soluble gamma interferon receptors with novel broad species specifi city. J Virol 1995; 69:4633-9.

Alche LE, and Coto CE. Differentiation of Junin virus and antigenic variants isolated in vivo by kinetic neutralization assays. J Gen Virol 1988; 69 ( Pt 8):2123-7.

AlthageA, Odermatt B, Moskophidis D, Kundig T, Hoffman-Rohrer U et al. Immunosuppression by lymphocytic choriomeningitis virus infection: competent effector T and B cells but impaired antigen presentation. Eur J Immunol 1992; 22:1803-12.

Ando K, Moriyama T, Guidotti LG, Wirth S, Schreiber RD et al. Mechanisms of class I restricted immunopathology. A transgenic mouse model of fulminant hepatitis. J Exp Med 1993; 178:1541-54.

Bach JF. Insulin-dependent diabetes mellitus as an autoimmune disease. Endocr Rev 1994; 15:516-42.

Bachmann MF, Kundig TM, Hengartner H and Zinkernagel RM. Protection against immunopathological consequences of a viral infection by activated but not resting cytotoxic T cells: T cell memory without „memory T cells“? Proc Natl Acad Sci U S A 1997; 94:640-5.

Battegay M, Kyburz D, Hengartner H and Zinkernagel RM. Enhancement of disease by neutralizing antiviral antibodies in the absence of primed antiviral cytotoxic T cells. Eur J Immunol 1993; 23:3236-41.

Bonilla WV, Pinschewer DD, Klenerman P, Rousson V, Gaboli M et al. Effects of promyelocytic leukemia protein on virus-host balance. J Virol 2002; 76:3810-8.

Borrow P, Evans CF and Oldstone MB. Virus-induced immunosuppression: immune system-mediated destruction of virus-infected dendritic cells results in generalized immune suppression. J Virol 1995; 69:1059-70.

Borrow P and Oldstone MBA. Lymphocytic Chroriomeningitis Virus, p. 593-627. In N. N. e. al. (ed.), Viral pathogenesis, First ed. Lippincott-Raven, Philadelphia. 1997.Chisari FV. Hepatitis B virus transgenic mice: models of viral immunobiology and pathogenesis. Curr Top Microbiol Immunol 1996; 206:149-73.

Ciurea A, Hunziker L, Martinic MM, Oxenius A, Hengartner H et al. CD4+ T-cell-epitope escape mutant virus selected in vivo. Nat Med 2001; 7:795-800.

Ciurea A, Klenerman P, Hunziker L, Horvath E, Senn BM et al. Viral persistence in vivo through selection of neutralizing antibody-escape variants. Proc Natl Acad Sci U S A 2000; 97:2749-54.

Cole GA, Gilden DH, Monjan AA and Nathanson N. Lymphocytic choriomeningitis virus: pathogenesis of acute central nervous system disease. Fed Proc 1971; 30:1831-41.

Cole GA and Nathanson N. Lymphocytic choriomeningitis. Pathogenesis. Prog Med Virol 1974; 18:94-110.Cole GA, Nathanson N and Prendergast RA. Requirement for theta-bearing cells in lymphocytic choriomeningitis virus-induced central nervous system disease. Nature 1972; 238:335-7.

Coto C, Vidal MC, D’Aiutolo AC and Damonte E. Selection of spontaneous ts mutants of Junin and Tacaribe viruses in persistent infections, p. 59-64. In B. D.H.L. and C. R.W. (ed.). The replication of negative strand viruses. Elsevier-North Holland, New York. 1981.

Djavani M, Yin C, Lukashevich IS, Rodas J, Rai SK et al. Mucosal immunization with Salmonella typhimurium expressing Lassa virus nucleocapsid protein cross-protects mice from lethal challenge with lymphocytic choriomeningitis virus. J Hum Virol 2001; 4:103-8.

Djavani M, Yin C, Xia L, Lukashevich IS, Pauza CD et al. Murine immune responses to mucosally delivered Salmonella expressing Lassa fever virus nucleoprotein. Vaccine 2000; 18:1543-54.Doherty PC, Dunlop MB, Parish CR and Zinkernagel RM. Infl ammatory process in murine lymphocytic choriomeningitis is maximal in H-2K or H-2D compatible interactions. J Immunol 1976; 117:187-90.

Dong B, and Silverman RH. Alternative function of a protein kinase homology domain in 2’, 5’-oligoadenylate dependent RNase L. Nucleic Acids Res 1999; 27:439-45.

Eddy GA, Scott SK, Wagner FS and Brand OM. Pathogenesis of Machupo virus infection in primates. Bull World Health Organ 1975; 52:517-21.

Foster GR, Ackrill AM, Goldin RD, Kerr IM, Thomas HC et al. Stark. Expression of the terminal protein region of hepatitis B virus inhibits cellular responses to interferons alpha and gamma and double-stranded RNA. Proc Natl Acad Sci U S A 1991; 88:2888-92.

Genovesi EV and Peters CJ. Immunosuppression-induced susceptibility of inbred hamsters (Mesocricetus auratus) to lethal-disease by lymphocytic choriomeningitis virus infection. Arch Virol 1987; 97:61-76.

Gresser, I. Can interferon induce disease? Interferon 1982; 4:95-127.Guidotti LG, Ando K, Hobbs MV, Ishikawa T, Runkel L et al. Cytotoxic T lymphocytes inhibit hepatitis B virus gene expression by a noncytolytic mechanism in transgenic mice. Proc Natl Acad Sci U S A 1994; 91:3764-8.

Guidotti LG, Borrow P, Hobbs MV, Matzke B, Gresser I et al. Viral cross talk: intracellular inactivation of the hepatitis B virus during an unrelated viral infection of the liver. Proc Natl Acad Sci U S A 1996; 93:4589-94.

Guidotti LG and Chisari FV. Cytokine-induced viral purging--role in viral pathogenesis. Curr Opin Microbiol 1999; 2:388-91.Guidotti LG and Chisari FV. Cytokine-mediated control of viral infections. Virology 2000; 273:221-7.

Guidotti LG and Chisari FV. Noncytolytic control of viral infections by the innate and adaptive immune response. Annu Rev Immunol 2001; 19:65-91.Guidotti LG and Chisari FV. To kill or to cure: options in host defense against viral infection. Curr Opin Immunol 1996; 8:478-83.

Guidotti LG, McClary H, Loudis JM and Chisari FV. Nitric oxide inhibits hepatitis B virus replication in the livers of transgenic mice. J Exp Med 2000; 191:1247-52.

Guidotti LG, Morris A, Mendez H, Koch R, Silverman RH et al. Interferon-regulated pathways that control hepatitis B virus replication in transgenic mice. J Virol 2002; 76:2617-21.

Guidotti LG, Rochford R, Chung J, Shapiro M, Purcell R et al. Viral clearance without destruction of infected cells during acute HBV infection. Science 1999; 284:825-9.

Guilhot S, Guidotti LG and Chisari FV. Interleukin-2 downregulates hepatitis B virus gene expression in transgenic mice by a posttranscriptional mechanism. J Virol 1993, 67:7444-9.

Haller O, Frese M and Kochs G. Mx proteins: mediators of innate resistance to RNA viruses. Rev Sci Tech 1998; 17:220-30.

Hotchin J. The biology of lymphocytic choriomeningitis infection: virus induced immune disease. Cold Spring Harb Symp Quant Biol:479-499. 1962.

Jacobson S and Pfau CJ. Viral pathogenesis and resistance to defective interfering particles. Nature 1980; 283:311-3.

Kagi D, Ledermann B, Burki K, Seiler P, Odermatt B et al. Cytotoxicity mediated by T cells and natural killer cells is greatly impaired in perforin-defi cient mice. Nature 1994; 369:31-7.

Kagi D, Vignaux F, Ledermann B, Burki K, Depraetere V et al. Fas and perforin pathways as major mechanisms of T cell-mediated cytotoxicity. Science 1994; 265:528-30.

Kalvakolanu DV, Bandyopadhyay SK, Harter ML and Sen GC. Inhibition of interferon-inducible gene expression by adenovirus E1A proteins: block in transcriptional complex formation. Proc Natl Acad Sci U S A 1991; 88:7459-63.

Kalvakolanu DV and Borden EC. An overview of the interferon system: signal transduction and mechanisms of action. Cancer Invest 1996; 14:25-53.

Kenyon RH, Green DE and Peters CJ. Effect of immunosuppression on experimental Argentine hemorrhagic fever in guinea pigs. J Virol 1985; 53:75-80.

Kenyon RH and Peters CJ. Cytolysis of Junin infected target cells by immune guinea pig spleen cells. Microb Pathog 1986; 1:453-64.

Klenerman P and Zinkernagel RM. Original antigenic sin impairs cytotoxic T lymphocyte responses to viruses bearing variant epitopes. Nature 1998; 394:482-5.

Kundig TM., Bachmann MF, Oehen S, Hoffmann UW, Simard JJ et al. On the role of antigen in maintaining cytotoxic T-cell memory. Proc Natl Acad Sci U S A 1996; 93:9716-23.

Lau LL, Jamieson BD, Somasundaram T and Ahmed R. Cytotoxic T-cell memory without antigen. Nature 1994; 369:648-52.

Leist TP, Ruedi E and Zinkernagel RM. Virus-triggered immune suppression in mice caused by virus-specifi c cytotoxic T cells. J Exp Med 1988; 167:1749-54.

Lukashevich IS. Generation of reassortants between African arenaviruses. Virology 1992; 188:600-5.

Lukashevich IS, Maryankova R, Vladyko AS, Nashkevich N, Koleda S et al.

Lassa and Mopeia virus replication in human monocytes/macrophages and in endothelial cells: different effects on IL-8 and TNF-alpha gene expression. J Med Virol 1999; 59:552-60.

Lukashevich IS, Tikhonov I, Rodas JD, Zapata JC, Yang Y et al. Arenavirus-mediated liver pathology: acute lymphocytic choriomeningitis virus infection of rhesus macaques is characterized by high-level interleukin-6 expression and hepatocyte proliferation. J Virol 2003; 77:1727-37.

Lukashevich IS, Vasiuchkov AD, Stel’makh TA, Scheslenok EP and Shabanov AG. [The isolation and characteristics of reassortants between the Lassa and Mopeia arenaviruses]. Vopr Virusol 1991; 36:146-50.

Martz E and Howell DM. CTL: virus control cells fi rst and cytolytic cells second? DNA fragmentation, apoptosis and the prelytic halt hypothesis. Immunol Today 1989; 10:79-86.

McFadden G, Graham K, Ellison K, Barry M, Macen J et al. Interruption of cytokine networks by poxviruses: lessons from myxoma virus. J Leukoc Biol 1995; 57:731-8.

Michalopoulos GK and DeFrances MC. Liver regeneration. Science 1997; 276:60-6.

Mims CA and Blanden RV. Antiviral action of immune lymphocytes in mice infected with lymphocytic choriomeningitis virus. Infect Immun 1972; 6:695-8.

Mims CA and Wainwright S. The immunodepressive action of lymphocytic choriomeningitis virus in mice. J Immunol 1968; 101:717-24.

Moskophidis D, Lechner F, Pircher H and Zinkernagel RM. Virus persistence in acutely infected immunocompetent mice by exhaustion of antiviral cytotoxic effector T cells. Nature 1993; 362:758-61.

Murphy FA, Buchmeier MJ and Rawls WE. The reticuloendothelium as the target in a virus infection. Pichinde virus pathogenesis in two strains of hamsters. Lab Invest 1977; 37:502-15.

Ochsenbein AF, Fehr T, Lutz C, Suter M, Brombacher F et al. Control of early viral and bacterial distribution and disease by natural antibodies. Science 1999; 286:2156-9.

Ochsenbein AF, Karrer U, Klenerman P, Althage A, Ciurea A et al. A comparison of T cell memory against the same antigen induced by virus versus intracellular bacteria. Proc Natl Acad Sci U S A 1999; 96:9293-8.

Odermatt B, Eppler M, Leist TP, Hengartner H and Zinkernagel RM. Virus-triggered acquired immunodefi ciency by cytotoxic T-cell-dependent destruction of antigen-presenting cells and lymph follicle structure. Proc Natl Acad Sci U S A 1991; 88:8252-6.

Ohashi PS, Oehen S, Buerki K, Pircher H, Ohashi CT et al. Ablation of “tolerance” and induction of diabetes by virus infection in viral antigen transgenic mice. Cell 1991; 65:305-17.

Oldstone MB, Blount P, Southern PJ and Lampert PW. Cytoimmunotherapy for persistent virus infection reveals a unique clearance pattern from the central nervous system. Nature 1986; 321:239-43.

Oldstone MB and Buchmeier MJ. Restricted expression of viral glycoprotein in cells of persistently infected mice. Nature 1982; 300:360-2.

Oldstone MB, Nerenberg M, Southern P, Price J and Lewicki H. Virus infection triggers insulin-dependent diabetes mellitus in a transgenic model: role of anti-self (virus) immune response. Cell 1991; 65:319-31.

Oldstone MB, Tishon A and Buchmeier MJ. Virus-induced immune complex disease: genetic control of C1q binding complexes in the circulation of mice persistently infected with lymphocytic choriomeningitis virus. J Immunol 1983; 130:912-8.

Peters CJ, Jahrling PB, Liu CT, Kenyon RH, McKee KT et al. Experimental studies of arenaviral hemorrhagic fevers. Curr Top Microbiol Immunol 1987; 134:5-68.

Pircher H, Moskophidis D, Rohrer U, Burki K, Hengartner H et al. Viral escape by selection of cytotoxic T cell-resistant virus variants in vivo. Nature 1990; 346:629-33.

Planz O, Ehl S, Furrer E, Horvath E, Brundler MA et al. A critical role for neutralizing-antibody-producing B cells, CD4(+) T cells, and interferons in persistent and acute infections of mice with lymphocytic choriomeningitis virus: implications for adoptive immunotherapy of virus carriers. Proc Natl Acad Sci U S A 1997; 94:6874-9.

Planz O, Seiler P, Hengartner H and Zinkernagel RM. Specifi c cytotoxic T cells eliminate B cells producing virus-neutralizing antibodies [corrected]. Nature 1996; 382:726-9.

Rakasz E, MacDougall AV, Zayas MT, Helgelund JL, Ruckward TJ et al. Gammadelta T cell receptor repertoire in blood and colonic mucosa of rhesus macaques. J Med Primatol 2000; 29:387-96.

Riviere Y, Ahmed R, Southern PJ, Buchmeier MJ and Oldstone MB. Genetic mapping of lymphocytic choriomeningitis virus pathogenicity: virulence in guinea pigs is associated with the L RNA segment. J Virol 1985; 55:704-9.

Riviere Y, Gresser I, Guillon JC, Bandu MT, Ronco P et al. Severity of lymphocytic choriomeningitis virus disease in different strains of suckling mice correlates with increasing amounts of endogenous interferon. J Exp Med 1980; 152:633-40.

Riviere Y, Gresser I, Guillon JC and Tovey MG. Inhibition by anti-interferon serum of lymphocytic choriomeningitis virus disease in suckling mice. Proc Natl Acad Sci U S A 1977; 74:2135-9.

Rowe WP. Studies on pahtogenesis and immunity in lymphocytic choriomeningitis infection of the mouse. Navy Research Report: 167-220. 1954.

Sandberg K, Kemper P, Stalder A, Zhang J, Hobbs MV et al. Altered tissue distribution of viral replication and T cell spreading is pivotal in the protection against fatal lymphocytic choriomeningitis in mice after neutralization of IFN-alpha/beta. J Immunol 1994; 153:220-31.

Saura M., Zaragoza C, McMillan A, Quick RA, Hohenadl C et al. An antiviral mechanism of nitric oxide: inhibition of a viral protease. Immunity 1999; 10:21-8.

Schmitz JE, Kuroda MJ, Santra S, Sasseville VG, Simon MA et al. Control of viremia in simian immunodeficiency virus infection by CD8+ lymphocytes. Science 1999; 283:857-60.

Schmitz JE, Kuroda MJ, Santra S, Simon MA, Lifton MA et al. Effect of humoral immune responses on controlling viremia during primary infection of rhesus monkeys with simian immunodefi ciency virus. J Virol 2003; 77:2165-73.

Schmitz JE, Lifton MA, Reimann KA, Montefi ori DC, Shen L et al. Effect of complement consumption by cobra venom factor on the the course of primary infection with simian immunodefi ciency virus in rhesus monkeys. AIDS Res Hum Retroviruses 1999; 15:195-202.

Schreiber M and McFadden G. The myxoma virus TNF-receptor homologue (T2) inhibits tumor necrosis factor-alpha in a species-specifi c fashion. Virology 1994; 204:692-705.

Silberman SL, Jacobs RP and Cole GA. Mechanisms of hemopoietic and immunological dysfunction induced by lymphocytic choriomeningitis virus. Infect Immun 1978; 19:533-9.

Symons JA, Alcami A and Smith GL. Vaccinia virus encodes a soluble type I interferon receptor of novel structure and broad species specifi city. Cell 1995; 81:551-60.

Terenzi F, deVeer MJ, Ying H, Restifo NP, Williams BR et al. The antiviral enzymes PKR and RNase L suppress gene expression from viral and non-viral based vectors. Nucleic Acids Res 1999; 27:4369-75.

Thimme R, Wieland S, Steiger C, Ghrayeb J, Reimann KA et al. CD8(+) T cells mediate viral clearance and disease pathogenesis during acute hepatitis B virus infection. J Virol 2003; 77:68-76.

Upton C, Mossman K and McFadden G. Encoding of a homolog of the IFN-gamma receptor by myxoma virus. Science 1992; 258:1369-72.

Volkert M. Studies on immunological tolerance to LCMV. 2. Treatment of virus carrier mice by adoptive immunization. Acta Pathol Microbiol Scand 1963; 57: 465–87.

von Herrath MG. Regulation of virally induced autoimmunity and immunopathology: contribution of LCMV transgenic models to understanding autoimmune insulin-dependent diabetes mellitus. Curr Top Microbiol Immunol 2002; 263:145-75.

Walker DH and Murphy FA. Pathology and pathogenesis of arenavirus infections. Curr Top Microbiol Immunol 1987; 133:89-113.

Walsh CM, Matloubian M, Liu CC, Ueda R, Kurahara CG et al. Immune function in mice lacking the perforin gene. Proc Natl Acad Sci U S A 1994; 91:10854-8.

Welsh RM Jr and. Zinkernagel RM. Heterospecifi c cytotoxic cell activity induced during the fi rst three days of acute lymphocytic choriomeningitis virus infection in mice. Nature 1977; 268:646-8.

Zaragoza C, Ocampo CJ, Saura M, McMillan A and Lowenstein CJ. Nitric oxide inhibition of coxsackievirus replication in vitro. J Clin Invest 1997; 100:1760-7.

Zinkernagel RM and Doherty PC. Restriction of in vitro T cell-mediated cytotoxicity in lymphocytic choriomeningitis within a syngeneic or semiallogeneic system. Nature 1974; 248:701-2.

Zinkernagel RM, Dunlop MB, Blanden RV, Doherty PC and Shreffl er DC. H-2 compatibility requirement for virus-specifi c T-cell-mediated cytolysis. Evaluation of the role of H-2I region and non-H-2 genes in regulating immune response. J Exp Med 1976; 144:519-32.

Zinkernagel RM, Haenseler E, Leist T, Cerny A, Hengartner H et al. T cell-mediated hepatitis in mice infected with lymphocytic choriomeningitis virus. Liver cell destruction by H-2 class I-restricted virus-specifi c cytotoxic T cells as a physiological correlate of the 51Cr-release assay? J Exp Med 1986; 164:1075-92.

Downloads

Published

2009-09-08

How to Cite

Rodas G., J. D., Hewson, R., & Salvato, M. S. (2009). Contribution of the murine and primate models to the study of arenaviral diseases and hemorrhagic fevers. Revista Colombiana De Ciencias Pecuarias, 22(3), 8. https://doi.org/10.17533/udea.rccp.324453

Issue

Section

Original research articles

Similar Articles

> >> 

You may also start an advanced similarity search for this article.