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Measles pp 73-87 | Cite as

Ferrets as a Model for Morbillivirus Pathogenesis, Complications, and Vaccines

  • S. Pillet
  • N. Svitek
  • V. von MesslingEmail author
Chapter
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 330)

The ferret is a standard laboratory animal that can be accommodated in most animal facilities. While not susceptible to measles, ferrets are a natural host of canine distemper virus (CDV), the closely related carnivore morbillivirus. CDV infection in ferrets reproduces all clinical signs associated with measles in humans, including the typical rash, fever, general immunosuppression, gastrointestinal and respiratory involvement, and neurological complications. Due to this similarity, experimental CDV infection of ferrets is frequently used to assess the efficacy of novel vaccines, and to characterize pathogenesis mechanisms. In addition, direct intracranial inoculation of measles isolates from subacute sclerosing panencephali-tis (SSPE) patients results in an SSPE-like disease in animals that survive the acute phase. Since the advent of reverse genetics systems that allow the targeted manipulation of viral genomes, the model has been used to evaluate the contribution of the accessory proteins C and V, and signalling lymphocyte activation molecule (SLAM)-binding to immunosuppression and overall pathogenesis. Similarly produced green fluorescent protein-expressing derivatives that maintain parental virulence have been instrumental in the direct visualization of systemic dissemination and neuroinvasion. As more immunological tools become available for this model, its contribution to our understanding of morbillivirus—host interactions is expected to increase.

Keywords

Measle Virus Canine Distemper Virus Maternal Antibody Measle Vaccine Subacute Sclerosing Panencephalitis 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Alldinger S, Wunschmann A, Baumgartner W, Voss C, Kremmer E (1996) Up-regulation of major histocompatibility complex class II antigen expression in the central nervous system of dogs with spontaneous canine distemper virus encephalitis. Acta Neuropathol 92:273 – 280PubMedCrossRefGoogle Scholar
  2. Appel MJ, Harris WV (1988) Antibody titers in domestic ferret jills and their kits to canine distemper virus vaccine. J Am Vet Med Assoc 193:332 – 333PubMedGoogle Scholar
  3. Appel MJ, Shek WR, Summers BA (1982) Lymphocyte-mediated immune cytotoxicity in dogs infected with virulent canine distemper virus. Infect Immun 37:592 – 600PubMedGoogle Scholar
  4. Appel MJ, Shek WR, Shesberadaran H, Norrby E (1984) Measles virus and inactivated canine distemper virus induce incomplete immunity to canine distemper. Arch Virol 82:73 – 82PubMedCrossRefGoogle Scholar
  5. Appel MJ, Summers BA (1995) Pathogenicity of morbilliviruses for terrestrial carnivores. Vet Microbiol 44:187 – 191PubMedCrossRefGoogle Scholar
  6. Atabani SF, Byrnes AA, Jaye A, Kidd IM, Magnusen AF, Whittle H, Karp CL (2001) Natural measles causes prolonged suppression of interleukin-12 production. J Infect Dis 184:1 – 9PubMedCrossRefGoogle Scholar
  7. Axthelm MK, Krakowka S (1987) Canine distemper virus: the early blood-brain barrier lesion. Acta Neuropathol 75:27 – 33PubMedCrossRefGoogle Scholar
  8. Bonami F, Rudd PA, von Messling V (2007) Disease duration determines canine distemper virus neurovirulence. J Virol 81:12066 – 12070PubMedCrossRefGoogle Scholar
  9. Brown HR, Thormar H, Barshatzky M, Wisniewski HM (1985) Localization of measles virus antigens in subacute sclerosing panencephalitis in ferrets. Lab Anim Sci 35:233 – 237PubMedGoogle Scholar
  10. Bush M, Montali RJ, Brownstein D, James AE Jr, Appel MJ (1976) Vaccine-induced canine distemper in a lesser panda. J Am Vet Med Assoc 169:959 – 960PubMedGoogle Scholar
  11. Cabasso VJ, Stebbins MR, Cox HR (1953) Active immunization of ferrets by simultaneous injections of avianized canine distemper vaccine and anticanine distemper hyperimmune serum. Cornell Vet 43:179 – 183PubMedGoogle Scholar
  12. Carpenter JW, Appel MJ, Erickson RC, Novilla MN (1976) Fatal vaccine-induced canine distemper virus infection in black-footed ferrets. J Am Vet Med Assoc 169:961 – 964PubMedGoogle Scholar
  13. Chalmers WS, Baxendale W (1994) A comparison of canine distemper vaccine and measles vaccine for the prevention of canine distemper in young puppies. Vet Rec 135:349 – 353PubMedGoogle Scholar
  14. Cherpillod P, Tipold A, Griot-Wenk M, Cardozo C, Schmid I, Fatzer R, Schobesberger M, Zurbriggen R, Bruckner L, Roch F et al (2000) DNA vaccine encoding nucleocapsid and surface proteins of wild type canine distemper virus protects its natural host against distemper. Vaccine 18:2927 – 2936PubMedCrossRefGoogle Scholar
  15. Confer AW, Kahn DE, Koestner A, Krakowka S (1975) Biological properties of a canine distemper virus isolate associated with demyelinating encephalomyelitis. Infect Immun 11:835 – 844PubMedGoogle Scholar
  16. Dahl L, Jensen TH, Gottschalck E, Karlskov-Mortensen P, Jensen TD, Nielsen L, Andersen MK, Buckland R, Wild TF, Blixenkrone-Moller M (2004) Immunization with plasmid DNA encoding the hemagglutinin and the nucleoprotein confers robust protection against a lethal canine distemper virus challenge. Vaccine 22:3642 – 3648PubMedCrossRefGoogle Scholar
  17. Danesh A, Seneviratne C, Cameron CM, Banner D, Devries ME, Kelvin AA, Xu L, Ran L, Bosinger SE, Rowe T et al (2008) Cloning, expression and characterization of ferret CXCL10. Mol Immunol 45:1288 – 1297PubMedCrossRefGoogle Scholar
  18. Devaux P, von Messling V, Songsungthong W, Springfeld C, Cattaneo R (2007) Tyrosine 110 in the measles virus phosphoprotein is required to block STAT1 phosphorylation. Virology 360: 72 – 83PubMedCrossRefGoogle Scholar
  19. Dorries R, Ter Meulen V (1984) Detection and identification of virus-specific, oligoclonal IgG in unconcentrated cerebrospinal fluid by immunoblot technique. J Neuroimmunol 7:77 – 89PubMedCrossRefGoogle Scholar
  20. Ek-Kommonen C, Rudback E, Anttila M, Aho M, Huovilainen A (2003) Canine distemper of vaccine origin in European mink, Mustela lutreola — a case report. Vet Microbiol 92:289 – 293PubMedCrossRefGoogle Scholar
  21. Fischer L, Tronel JP, Pardo-David C, Tanner P, Colombet G, Minke J, Audonnet JC (2002) Vaccination of puppies born to immune dams with a canine adenovirus-based vaccine protects against a canine distemper virus challenge. Vaccine 20:3485 – 3497PubMedCrossRefGoogle Scholar
  22. Fischer L, Tronel JP, Minke J, Barzu S, Baudu P, Audonnet JC (2003) Vaccination of puppies with a lipid-formulated plasmid vaccine protects against a severe canine distemper virus challenge. Vaccine 21:1099 – 1102PubMedCrossRefGoogle Scholar
  23. Fontana JM, Bankamp B, Bellini WJ, Rota PA (2008) Regulation of interferon signaling by the C and V proteins from attenuated and wild-type strains of measles virus. Virology 374:71 – 81PubMedCrossRefGoogle Scholar
  24. Fox JG (1998) Biology and diseases of the ferret. Wiley-Blackwell, New YorkGoogle Scholar
  25. Gans HA, Arvin AM, Galinus J, Logan L, DeHovitz R, Maldonado Y (1998) Deficiency of the humoral immune response to measles vaccine in infants immunized at age 6 months. JAMA 280:527 – 532PubMedCrossRefGoogle Scholar
  26. Gill JM, Hartley WJ, Hodgkinson NL (1988) An outbreak of post-vaccinal suspected distemperlike encephalitis in farmed ferrets ( Mustela putorius furo) NZ Vet J 36:173 – 176Google Scholar
  27. Gillespie JH, Rickard CG (1956) Encephalitis in dogs produced by distemper virus. Am J Vet Res 17:103 – 108PubMedGoogle Scholar
  28. Gorham JR, Leader RW, Gutierrez JC (1954) Distemper immunization of ferrets by nebulization with egg adapted virus. Science 119:125 – 126PubMedCrossRefGoogle Scholar
  29. Greenacre CB (2003) Incidence of adverse events in ferrets vaccinated with distemper or rabies vaccine: 143 cases (1995 – 2001) J Am Vet Med Assoc 223:663 – 665 virology, 5 th edn. Philadelphia, Lippincott Williams Wilkins, pp 1550 – 1585Google Scholar
  30. Griot C, Moser C, Cherpillod P, Bruckner L, Wittek R, Zurbriggen A, Zurbriggen R (2004) Early DNA vaccination of puppies against canine distemper in the presence of maternally derived immunity. Vaccine 22:650 – 654PubMedCrossRefGoogle Scholar
  31. Hoover JP, Baldwin CA, Rupprecht CE (1989) Serologic response of domestic ferrets ( Mustela puto-rius furo) to canine distemper and rabies virus vaccines. J Am Vet Med Assoc 194:234 – 238PubMedGoogle Scholar
  32. Hsu KH, Lubeck MD, Bhat BM, Bhat RA, Kostek B, Selling BH, Mizutani S, Davis AR, Hung PP (1994) Efficacy of adenovirus-vectored respiratory syncytial virus vaccines in a new ferret model. Vaccine 12:607 – 612PubMedCrossRefGoogle Scholar
  33. Katz M, Rorke LB, Masland WS, Koprowski H, Tucker SH (1968) Transmission of an encepha-litogenic agent from brains of patients with subacute sclerosing panencephalitis to ferrets. Preliminary report. N Engl J Med 279:793 – 798PubMedGoogle Scholar
  34. Kauffman CA, Bergman AG, O'Connor RP (1982) Distemper virus infection in ferrets: an animal model of measles-induced immunosuppression. Clin Exp Immunol 47:617 – 625PubMedGoogle Scholar
  35. Krakowka S (1982) Mechanisms of in vitro immunosuppression in canine distemper virus infection. J Clin Lab Immunol 8:187 – 196PubMedGoogle Scholar
  36. Krakowka S, Cockerell G, Koestner A (1975) Effects of canine distemper virus infection on lym-phoid function in vitro and in vivo. Infect Immun 11:1069 – 1078PubMedGoogle Scholar
  37. Krakowka S, Axthelm MK, Johnsen GC (1985) Canine distemper virus. In: Olsen RG, Krakowka S, Blakeslee JR (eds) Comparative pathobiology of viral diseases. Boca Raton, FL, CRC, pp 137 – 164Google Scholar
  38. Krakowka S, Ringler SS, Lewis M, Olsen RG, Axthelm MK (1987) Immunosuppression by canine distemper virus: modulation of in vitro immunoglobulin synthesis, interleukin release and prostaglandin E2 production. Vet Immunol Immunopathol 15:181 – 201PubMedCrossRefGoogle Scholar
  39. Loeffler IK, Howard J, Montali RJ, Hayek LA, Dubovi E, Zhang Z, Yan Q, Guo W, Wildt DE (2007) Serosurvey of ex situ giant pandas ( Ailuropoda melanoleuca) and red pandas ( Ailurus fulgens) in China with implications for species conservation. J Zoo Wildl Med 38:559 – 566PubMedCrossRefGoogle Scholar
  40. Maher JA, DeStefano J (2004) The ferret: an animal model to study influenza virus. Lab Anim (NY) 33:50 – 53CrossRefGoogle Scholar
  41. McCullough B, Krakowka S, Koestner A (1974) Experimental canine distemper virus-induced lymphoid depletion. Am J Pathol 74:155 – 170PubMedGoogle Scholar
  42. McKenna MC, Bell SK (1997) Classification of mammals above the species level. Columbia University Press, New YorkGoogle Scholar
  43. McQuaid S, Cosby SL, Koffi K, Honde M, Kirk J, Lucas SB (1998) Distribution of measles virus in the central nervous system of HIV-seropositive children. Acta Neuropathol 96:637 – 642PubMedCrossRefGoogle Scholar
  44. Mehta PD, Thormar H (1979) Immunological studies of subacute measles encephalitis in ferrets: similarities to human subacute sclerosing panencephalitis. J Clin Microbiol 9:601 – 604PubMedGoogle Scholar
  45. Moody KD, Bowman TA, Lang CM (1985) Laboratory management of the ferret for biomedical research. Lab Anim Sci 35:272 – 279PubMedGoogle Scholar
  46. Morris JA, Coburn DR, O'Connor JR (1954) Rapid protection of ferrets against fully virulent distemper virus with nebulized attenuated distemper virus. Cornell Vet 44:198 – 207PubMedGoogle Scholar
  47. Moss WJ, Ryon JJ, Monze M, Griffin DE (2002) Differential regulation of interleukin (IL)-4, IL-5, and IL-10 during measles in Zambian children. J Infect Dis 186:879 – 887PubMedCrossRefGoogle Scholar
  48. Nagano I, Nakamura S, Yoshioka M, Kogure K (1991) Immunocytochemical analysis of the cellular infiltrate in brain lesions in subacute sclerosing panencephalitis. Neurology 41:1639 – 1642PubMedGoogle Scholar
  49. Ochi A, Danesh A, Seneviratne C, Banner D, Devries ME, Rowe T, Xu L, Ran L, Czub M, Bosinger SE et al (2008) Cloning, expression and immunoassay detection of ferret IFN-gamma. Dev Comp Immunol 32:890 – 897PubMedCrossRefGoogle Scholar
  50. Ohno S, Ono N, Takeda M, Takeuchi K, Yanagi Y (2004) Dissection of measles virus V protein in relation to its ability to block alpha/beta interferon signal transduction. J Gen Virol 85:2991 – 2999PubMedCrossRefGoogle Scholar
  51. Osterhaus AD, Fouchier RA, Kuiken T (2004) The aetiology of SARS: Koch's postulates fulfilled. Philos Trans R Soc Lond B Biol Sci 359:1081 – 1082PubMedCrossRefGoogle Scholar
  52. Palosaari H, Parisien JP, Rodriguez JJ, Ulane CM, Horvath CM (2003) STAT protein interference and suppression of cytokine signal transduction by measles virus V protein. J Virol 77:7635 – 7644PubMedCrossRefGoogle Scholar
  53. Pardo MC, Bauman JE, Mackowiak M (1997) Protection of dogs against canine distemper by vaccination with a canarypox virus recombinant expressing canine distemper virus fusion and hemagglutinin glycoproteins. Am J Vet Res 58:833 – 836PubMedGoogle Scholar
  54. Pardo MC, Tanner P, Bauman J, Silver K, Fischer L (2007) Immunization of puppies in the presence of maternally derived antibodies against canine distemper virus. J Comp Pathol 137 Suppl 1:S72 – S75PubMedCrossRefGoogle Scholar
  55. Pearson GL (1977) Vaccine-induced canine distemper virus in black-footed ferrets. J Am Vet Med Assoc 170:103, 106, 109Google Scholar
  56. Pollock RV, Carmichael LE (1982) Maternally derived immunity to canine parvovirus infection: transfer, decline, and interference with vaccination. J Am Vet Med Assoc 180:37 – 42PubMedGoogle Scholar
  57. Qin Q, Wei F, Li M, Dubovi EJ, Loeffler IK (2007) Serosurvey of infectious disease agents of carnivores in captive red pandas ( Ailurus fulgens) in China. J Zoo Wildl Med 38:42 – 50PubMedCrossRefGoogle Scholar
  58. Quesenberry KE (1996) Basic approach to veterinary care. In: Hillyer E V, Quesenberry KE (eds) Ferrets, rabbits, and rodents: clinical medicine and surgery. W.B. Saunders, Philadelphia, pp 14 – 25Google Scholar
  59. Rockborn G, Norrby E, Lannek N (1965) Comparison between the immunizing effect in dogs and ferrets of living distemper vaccines, attenuated in dog tissue cultures and embryonated eggs. Res Vet Sci 6:423 – 427PubMedGoogle Scholar
  60. Rudd PA, Cattaneo R, von Messling V (2006) Canine distemper virus uses both the anterograde and the hematogenous pathway for neuroinvasion. J Virol 80:9361 – 9370PubMedCrossRefGoogle Scholar
  61. Schluederberg A, Lamm SH, Landrigan PJ, Black FL (1973) Measles immunity in children vaccinated before one year of age. Am J Epidemiol 97:402 – 409PubMedGoogle Scholar
  62. Schneider-Schaulies J, Niewiesk S, Schneider-Schaulies S, ter Meulen V (1999) Measles virus in the CNS: the role of viral and host factors for the establishment and maintenance of a persistent infection. J Neurovirol 5:613 – 622PubMedCrossRefGoogle Scholar
  63. Schobesberger M, Summerfield A, Doherr MG, Zurbriggen A, Griot C (2005) Canine distemper virus-induced depletion of uninfected lymphocytes is associated with apoptosis. Vet Immunol Immunopathol 104:33 – 44PubMedCrossRefGoogle Scholar
  64. Senchak AJ, Sato AK, Vazquez R, Keller CE, Cable BB (2007) Characterization of transforming growth factors beta1 and 2 in ferrets ( Mustela putorius furo) Comp Med 57:594 – 596PubMedGoogle Scholar
  65. Shen DT, Gorham JR, Evermann JF, McKeirnan AJ (1984) Comparison of subcutaneous and intramuscular administration of a live attenuated distemper virus vaccine in ferrets. Vet Rec 114:42 – 43PubMedGoogle Scholar
  66. Sips GJ, Chesik D, Glazenburg L, Wilschut J, De Keyser J, Wilczak N (2007) Involvement of morbilliviruses in the pathogenesis of demyelinating disease. Rev Med Virol 17:223 – 244PubMedCrossRefGoogle Scholar
  67. Stephensen CB, Welter J, Thaker SR, Taylor J, Tartaglia J, Paoletti E (1997) Canine distemper virus (CDV) infection of ferrets as a model for testing Morbillivirus vaccine strategies: NYVAC- and ALVAC-based CDV recombinants protect against symptomatic infection. J Virol 71:1506 – 1513PubMedGoogle Scholar
  68. Strating A (1975) Measles vaccine in dogs: efficacy against aerosol challenge with virulent canine distemper virus. J Am Vet Med Assoc 167:59 – 62PubMedGoogle Scholar
  69. Summers BA, Greisen HA, Appel MJ (1979) Early events in canine distemper demyelinating encephalomyelitis. Acta Neuropathol 46:1 – 10PubMedCrossRefGoogle Scholar
  70. Summers BA, Greisen HA, Appel MJ (1984) Canine distemper encephalomyelitis: variation with virus strain. J Comp Pathol 94:65 – 75PubMedCrossRefGoogle Scholar
  71. Svitek N, von Messling V (2007) Early cytokine mRNA expression profiles predict Morbillivirus disease outcome in ferrets. Virology 362:404 – 410PubMedCrossRefGoogle Scholar
  72. Tetteh JK, Addae MM, Ishiwada N, Yempewu SM, Yamaguchi S, Ofori-Adjei D, Kamiya H, Komada Y, Akanmori BD (2003) Plasma levels of Th1 and Th2 cytokines in Ghanaian children with vaccine-modified measles. Eur Cytokine Netw 14:109 – 113PubMedGoogle Scholar
  73. Thormar H, Mehta PD, Lin FH, Brown HR, Wisniewski HM (1983) Presence of oligoclonal immunoglobulin G bands and lack of matrix protein antibodies in cerebrospinal fluids and sera of ferrets with measles virus encephalitis. Infect Immun 41:1205 – 1211PubMedGoogle Scholar
  74. Thormar H, Mehta PD, Barshatzky MR, Brown HR (1985) Measles virus encephalitis in ferrets as a model for subacute sclerosing panencephalitis. Lab Anim Sci 35:229 – 232PubMedGoogle Scholar
  75. Thormar H, Brown HR, Goller NL, Barshatzky MR, Wisniewski HM (1988) Transmission of measles virus encephalitis to ferrets by intracardiac inoculation of a cell-associated SSPE virus strain. APMIS 96:1125 – 1128PubMedCrossRefGoogle Scholar
  76. van Moll P, Alldinger S, Baumgartner W, Adami M (1995) Distemper in wild carnivores: an epidemiological, histological and immunocytochemical study. Vet Microbiol 44:193 – 199PubMedCrossRefGoogle Scholar
  77. Vandevelde M, Zurbriggen A (2005) Demyelination in canine distemper virus infection: a review. Acta Neuropathol 109:56 – 68PubMedCrossRefGoogle Scholar
  78. Vandevelde M, Kristensen F, Kristensen B, Steck AJ, Kihm U (1982) Immunological and pathological findings in demyelinating encephalitis associated with canine distemper virus infection. Acta Neuropathol 56:1 – 8PubMedCrossRefGoogle Scholar
  79. Vandevelde M, Zurbriggen A, Steck A, Bichsel P (1986) Studies on the intrathecal humoral immune response in canine distemper encephalitis. J Neuroimmunol 11:41 – 51PubMedCrossRefGoogle Scholar
  80. von Messling V, Springfeld C, Devaux P, Cattaneo R (2003) A ferret model of canine distemper virus virulence and immunosuppression. J Virol 77:12579 – 12591CrossRefGoogle Scholar
  81. von Messling V, Milosevic D, Cattaneo R (2004) Tropism illuminated: lymphocyte-based pathways blazed by lethal morbillivirus through the host immune system. Proc Natl Acad Sci U S A 101:14216 – 14221CrossRefGoogle Scholar
  82. von Messling V, Svitek N, Cattaneo R (2006) Receptor (SLAM [CD150]) recognition and the V protein sustain swift lymphocyte-based invasion of mucosal tissue and lymphatic organs by a morbillivirus. J Virol 80:6084 – 6092CrossRefGoogle Scholar
  83. Welter J, Taylor J, Tartaglia J, Paoletti E, Stephensen CB (1999) Mucosal vaccination with recom-binant poxvirus vaccines protects ferrets against symptomatic CDV infection. Vaccine 17:308 – 318PubMedCrossRefGoogle Scholar
  84. Welter J, Taylor J, Tartaglia J, Paoletti E, Stephensen CB (2000) Vaccination against canine distemper virus infection in infant ferrets with and without maternal antibody protection, using recombinant attenuated poxvirus vaccines. J Virol 74:6358 – 6367PubMedCrossRefGoogle Scholar
  85. Wilkins J, Wehrle PF (1979) Additional evidence against measles vaccine administration to infants less than 12 months of age: altered immune response following active/passive immunization. J Pediatr 94:865 – 869PubMedCrossRefGoogle Scholar
  86. Williams ES, Anderson SL, Cavender J, Lynn C, List K, Hearn C, Appel MJ (1996) Vaccination of black-footed ferret ( Mustela nigripes) x Siberian polecat ( M. eversmanni) hybrids and domestic ferrets ( M. putorius furo)against canine distemper. J Wildl Dis 32:417 – 423PubMedGoogle Scholar
  87. Wimsatt J, Jay MT, Innes KE, Jessen M, Collins JK (2001) Serologic evaluation, efficacy, and safety of a commercial modified-live canine distemper vaccine in domestic ferrets. Am J Vet Res 62:736 – 740PubMedCrossRefGoogle Scholar
  88. Wimsatt J, Biggins D, Innes K, Taylor B, Garell D (2003) Evaluation of oral and subcutaneous delivery of an experimental canarypox recombinant canine distemper vaccine in the Siberian polecat ( Mustela eversmanni) J Zoo Wildl Med 34:25 – 35PubMedGoogle Scholar
  89. Zilliox MJ, Moss WJ, Griffin DE (2007) Gene expression changes in peripheral blood mononu-clear cells during measles virus infection. Clin Vaccine Immunol 14:918 – 923PubMedCrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2009

Authors and Affiliations

  1. 1.INRS-Institut Armand-FrappierUniversity of QuebecLavalCanada

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