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2004, Number 1

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Vet Mex 2004; 35 (1)

Characteristics of the immune response of pigs infected with porcine rubulavirus

Hernández J, Reyes-Leyva J, Ramírez H, Valenzuela O, Zenteno E

Language: English/Spanish
References: 133
Page: 65-74
PDF size: 316.33 Kb.


ABSTRACT

Porcine rubulavirus is responsible for blue eye disease in porcine, which is characterized by neurological signs, corneal opacity and high mortality in young pigs. Reproductive disorders such as epididymitis and testicular atrophy are also common in sexually mature pigs. Since its identification at the beginning of 1980´s, many researches have identified the main molecular, pathological, biological and immunological characteristics of the disease. This review discusses the recent advances related to the humoral and cellular immune response to porcine rubulavirus. The importance of the Hemagglutinin-Neuraminidase (HN) protein as an inducer of specific antibodies during infection and the importance of CD4+CD8- lymphocytes during early immune responses and CD4+CD8+ lymphocytes in memory response are also discussed.


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  2. virus hemaglutinante. Memorias del XVII Congreso de la Asociación de Médico Veterinarios Especialistas en Cerdos; 1981, Puerto Vallarta, México. 1981:43.

  3. Stephano A, Gay G, Ramírez T. Encephalomyelitis, reproductive failure and corneal opacity (blue eye) in pigs, associate with a paramixovirus infection. Vet Rec 1988;122: 6-10.

  4. Moreno-López J, Correa-Girón P, Martínez A, Ericsson A. Characterization of a paramixovirus isolated from the brain of a piglet in México. Arch Virol 1986;91:221-231.

  5. Stephano A. Blue eye diseases. In: Leman AD, Straw BF, Mengeling WL, Allaire AD, Taylor DJ, editors. Porcine Diseases. Ames, Ia: Iowa State University press, 1994:237-241.

  6. Hernández J, Ramírez H, Zenteno R, Monrroy J, Reyes-Leyva J, Zenteno E. Neumonitis inducida por el rubulavirus porcino. Rev Inst Nac Enferm Resp 1997;10:250-255.

  7. Ramírez-Mendoza H, Hernández-Jaúregui P, Reyes-Leyva J, Zenteno E, Moreno-López J, Kennedy S. Lesions in the reproductive tract of boars experimental infected with porcine rubulavirus. J Comp Pathol 1997;117:237-252.

  8. Ramírez-Mendoza H. Fisiopatología del paramixovirus del Ojo Azul a nivel testicular. (tesis de doctorado). México (Distrito Federal) México: Universidad Nacional Autónoma de México, 2000.

  9. Allan GM, MacNeilly F, Walker Y, Linné T, Moreno-López J, Hernández P, et al. A sequential study of experimental porcine paramyxovirus (LPMV) infection of pigs: immunostaining of cryostat sections and virus isolation. J Vet Diagn Invest 1996;8:405-413.

  10. MacNeilly F, Walker I, Allan G, Foster C, Linné T, Merza M, et al. A comparative study on the use of virus and antibody detection techniques for the diagnosis of La Piedad Michoacán paramyxovirus (LPMv) infection in pigs. J Vet Diagn Invest, 1997; 9: 3-9.

  11. Espinosa S. Evaluación de semen de verracos inoculados con el virus de la enfermedad del Ojo Azul (tesis de maestría). México (Distrito Federal) México: Universidad Nacional Autónoma de México, 2001.

  12. Rima B, Alexander BJ, Billeter MA, Collins PL, Kingsbury DW, Lipkind MA, et al. Family Paramyxoviridae, In: Murphy FA, Fauquet CM, Bishop DHL, Ghabrial SA, Jarvis AW, Matelli GP, et al., editors. Virus taxonomy: Classification and nomenclature of viruses. New York: Springer-Verlag, 1995:265-274.

  13. Sundqvist A, Berg M, Moreno-López J, Linné T. The hemagglutinin-neuraminidase glycoprotein of the porcine paramyxovirus LMPV: comparison with other paramyxovirus revealed the closest relationship to simian virus 5 and mumps virus. Arch Virol 1991;122:331-278.

  14. Berg M, Sundqvist A, Moreno-López J, Linné T. Identification of the porcine paramyxovirus LPMV matrix protein gene: comparative sequence análisis with other paramyxoviruses. J Gen Virol 1991;72:1045-1050.

  15. Berg M, Hjertner B, Moreno-López J, Linné T. The P gene of the porcine paramyxovirus LPMV encodes three possible polipeptides, P, V, and C; the P protein mRNA is edited. J Gen Virol 1992;73:1195-1200.

  16. Berg M, Bergvall AC, Svenda M, Sundqvist A, Moreno-López J, Linné T. Analysis of the fusion protein gene of the porcine rubulavirus LPMV: comparative analysis of paramyxoviruses F proteins. Virus Genes 1997;14:55-61.

  17. Wolinsky JS. Mumps. In: Fields BN, Knipe DM, Howley PM, editors. Fields in Virology. Filadelfia-Nueva York: Lippincott-Raven Publishers, 1996:1243-1266.

  18. Hernández J, Ramírez H, Carreón R, Mercado C, Lascuraín R, Hernández-Jaúregui P, et al. Several isolates of the Porcine Paramyxovirus can be sorted into two groups with different behavior. Memorias del

  19. III Congreso Internacional de Virología Veterinaria. Interlaken, Suiza. 1994:P1-6

  20. Sundqvist A, Berg M, Hernández-Jaúregui P, Linné T, and Moreno-López J. The structural proteins

  21. of a porcine paramyxovirus (LPMV). J Gen Virol 1990;71:609-613.

  22. Reyes-Leyva J, Hernández-Jaúregui P, Montaño L, Zenteno E. The porcine paramyxovirus LPM specifically recognize sialil (2-3) lactose-containing structures. Arch Virol 1993;133:195-200.

  23. Espinosa B, Reyes J, Hernández-Jaúregui P, Zenteno R, Ramírez H, Hernández J, et al. Carbohydrate specificity and porcine rubulavirus infectivity. In: Morilla A, Zimmerman J, Ion K, editors. Trends in Viral Emerging Diseases of Porcine. Ames, Ia:Iowa State University Press, 2002:81-85.

  24. Reyes-Leyva J, Espinosa B, Hernández J, Zenteno R, Vallejo V, Hernández-Jaúregui P, et al. E. NeuAca-2,3Gal-glycoconjugate expression determinates cell susceptibility to the porcine rubulavirus LPMV. Com Biochem Physiol 1997;118B:237-332.

  25. Vallejo V, Reyes-Leyva J, Hernández J, Ramírez H, Delannoy P, Zenteno E. Differential expression of sialic acid on porcine organs during the maturation process. Comp Biochem Physiol Biochem Mol Biol 2000;126:415-424.

  26. Hernández J, Reyes-Leyva J, Zenteno R, Ramírez H, Hernández-Jaúregui P, and Zenteno E. Immunity to

  27. porcine rubulavirus infection in adult porcine. Vet Immunol Immunopathol 1998;64:367-381.

  28. Hernández-Jáuregui P, Sundqvist A, Fuentes M, Díaz A, Reyes-Leyva J, Hernández E, Moreno-López J. Correlación entre las pruebas de virus neutralización, inhibición de la hemoaglutinación y ELISA en sueros vacunales y de brote para anticuerpos contra el Paramixovirus del Síndrome del Ojo Azul en cerdos. Vet Mex 1992;23:217-222.

  29. Zenteno R. Purificación y predicción de determinantes antigénicos y de estructura secundaria en la hemaglutinina-neuraminidasa del paramixovirus porcino de La Piedad Michoacán. (tesis de maestría).

  30. México (Distrito Federal) México: Universidad Nacional Autónoma de México, 1997.

  31. Ray R, Compans RW. Paramyxoviruses. In: Van Regenmortel MHB, Neurath AR editors. Immunochemistry of viruses II. The basis for serodiagnosis and vaccines. New York:Elsevier, 1990: 217-236.

  32. Abbas AK, Lichtman AH, Pober JS. Cellular and molecular immunology. 4 ed. Philadelphia Pennsylvania, W.B. Saunders, 2000.

  33. Griffit D, Ward B, Esolen L. Pathogenesis of mézales virus infection: a hypothesis for altered immune response. J Infect Dis 1994;170:S24-31.

  34. Griffit D, Bellini W. Measles Virus. In: Fields BN, Knipe DM, Howley PM, editors. Fields in Virology. Philadelphia. New York: Lippincott-Raven Publishers, 1996:1267-1312.

  35. Fujinami RS, and Oldstone MBA. Alterations in expression of measles virus polypeptides by antibody: molecular events in antibody induced antigenic modulation. J Immunol 1980;125:78-85.

  36. Hjertner B, Wiman AC, Svenda M, Berg M, Moreno-Lopez J, Linne T. Multiple factors including subgenomic RNAs and reduced viral protein expresión are associated with a persistent infection by porcine rubulavirus (LPMV). Arch Virol 1998;143:425-39.

  37. Wiman AC, Hjertner B, Linné T, Herron B, Allan G, McNeilly F, et al. Porcine rubulavirus LPMV RNA persists in the central nervous system of pigs after recovery from acute infection. J Neurovirol 1998;4:545-52.

  38. Hjertner B, Linné T, Moreno-López J. Establishment and characterization of a porcine rubulavirus (LPMV) persistent infection in porcine kidney cells. Acta Vet Scand 1997;38:213-24.

  39. Kasel JA, Frank AL, Keitel WA, Taber LH, Glezen WP. Acquisition of serum antibodies to specific viral glycoproteins of parainfluenza virus 3 in children. J Virol 1984;52:828-32.

  40. Reyes-Leyva J, Espinosa B, Santos G, Zenteno R, Hernández J, Vallejo V, et al. Purification and characterization of the hemagglutinin-neuraminidase of porcine rubulavirus LPMV. Glycoconj J 1999;16:517-522.

  41. Zenteno R, Hernández J, Espinosa B, Hernández-Jaúregui P, Reyes J, Zenteno E. Secondary structure prediction of the hemagglutinin neuraminidase from a porcine rubulavirus. Arch Virol 1998;143:333-352.

  42. Pescovitz M.D, Lunney J K, Sachs DH. Preparation and characterization of monoclonal antibodies reactive with porcine PBL. J Immunol 1984;133:368-373.

  43. Yang H, Parkhouse RM. Phenotypic classification of porcine lymphocytes sub-populations in blood and lymphoid tissues. Immunology 1996;89:76-83.

  44. Saalmueller A, Redheads M J, Buhring H J, Jonjic S, Koszinowski UH. Simultaneous expression of CD4 and CD8 antigens by a substantial proportion of resting porcine T lymphocytes. Eur J Immunol 1987;17:1297-1302.

  45. Pescovitz MD, Sakapoulos AG, Gaddy JA, Husmman RJ, Zuckemann FA. Porcine peripheral blood CD4+/CD8+ dual expressing T cells. Vet Immunol Immunopathol 1994;43:53-62.

  46. Zuckermann FA. Extrathymic CD4/CD8 doublepositive T cells. Vet Immunol Immunopathol 1999;72:55-66.

  47. Ward BJ, Johnson RT, Vaisberg A, Jaúregui E, Griffin DE. Cytokine production in vitro and the lymphoproliferative defect of natural measles virus infection. Clin Immunol Immunopathol 1991;61:236-48.

  48. Drew T. A review of evidence for immunosuppression due to Porcine Reproductive and Respiratory Syndrome Virus. Vet Rec 2000;31:27-39.

  49. Zuckermann F, Husmann RJ. Functional and phenotypic analysis of the peripheral blood CD4/CD8 double-positive T cells. Immunology 1996;87:500-512.

  50. Ivanoska D, Cuperlovic K, Lunney JK. Peripheral blood mononuclear cells subsets during Trichinella spiralis infection in pigs. Res Vet Sci 1990;49:92-97.

  51. Hernández J, Garfias Y, Nieto A, Mercado C, Montaño L, Zenteno E. Comparative evaluation of the CD4+CD8+ and CD4+CD8- lymphocytes in the immune response to porcine rubulavirus. Vet Immunol Immunopathol 2001;79:249-259.

  52. Summerfield A, Rhiza H, Saalmueller A. Functional characterization of porcine CD+4CD8+ extrathymic T lymphocytes. Cell Immunol 1996;168:291-296.

  53. Murail-Krishna K, Altman JD, Sures M, Sourdive DJD, Zajac AJ, Miller JD, et al. Counting antigen-specific CD8 T cells: a re-evaluation of bystander activation during viral infection. Immunity 1998;8:177-187.

  54. Rodríguez-Ropon A, Hernández-Jaúregui P, Sánchez-Torres L, Favila-Castillo L, Estrada-Parra S, Moreno-Lopez J, et al. Apoptosis in lymph nodes and changes in lymphocyte subpopulations in peripheral blood of pigs infected with porcine rubulavirus. J Comp Pathol 2003;128:1:8.

  55. Tripp RA, Hou S, McMickle A, Houston J, Doherty PC. Recruitment and proliferation of CD8+ T cells in respiratory virus infections. J Immunol 1995;154:6013-6021.

  56. Page G, Wang F, Hahn E. Interaction of pseudorabies virus with porcine peripheral blood lymphocytes. J Leukoc Biol 1992;52:441-48.

  57. Bradley RW, Swain LM. T cell memory. Annu Rev Immunol 1998;16:201-223.

  58. Galvan M, Murali-Krishna K, Lua L, Baum L, Ahmed R. Alterations in cell surface carbohydrates on T cells from virally infected mice can distinguís effector-memory CD8+ T cells from naïve cells. J Immunol 1998;161:641-648.

  59. Lascurain R, Porras F, Baez R, Chavez R, Martínez-Cairo S, Alvarez G, et al. Amaranthus leucocarpus recognizes human naive T cell subpopulations. Immunol Inevest 1997;26:579-587.

  60. Hernández J, Garfias Y, Reyes-Leyva J, Chávez R, Lascurain R, Zenteno E. Peanut and Amaranthus leucocarpus lectins discriminate between memory and naïve/quiescent porcine lymphocytes. Vet Immunol Immunopathol 84 2002;84:71-82.

  61. Ober BT, Summerfield A, Mattlimger C, Weismuller KH, Jung G, Pfaff E, et al. Vaccine-induced, pseudorabies virus- specific, extrathymic CD4+CD8+memory T-helper cells in porcine. J Virol 1998;72:4866-4873.

  62. Zinkernagel RM, Bachmann F, Kundis TE, Ochen S, Pirchet H, Hengartner H. On immunological memory. Annu Rev Immunol 1996;14:333-368.

  63. Hernández J. Estudio de la respuesta inmune celular y humoral en cerdos infectados experimentalmente con el rubulavirus porcino. (tesis de maestría). México (Distrito Federal) México: Universidad Nacional Autónoma de México, 1997.

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  71. Stephano A, Gay G, Ramírez T. Encephalomyelitis, reproductive failure and corneal opacity (blue eye) in pigs, associate with a paramixovirus infection. Vet Rec 1988;122: 6-10.

  72. Moreno-López J, Correa-Girón P, Martínez A, Ericsson A. Characterization of a paramixovirus isolated from the brain of a piglet in México. Arch Virol 1986;91:221-231.

  73. Stephano A. Blue eye diseases. In: Leman AD, Straw BF, Mengeling WL, Allaire AD, Taylor DJ, editors. Porcine Diseases. Ames, Ia: Iowa State University press, 1994:237-241.

  74. Hernández J, Ramírez H, Zenteno R, Monrroy J, Reyes-Leyva J, Zenteno E. Neumonitis inducida por el rubulavirus porcino. Rev Inst Nac Enferm Resp 1997;10:250-255.

  75. Ramírez-Mendoza H, Hernández-Jaúregui P, Reyes-Leyva J, Zenteno E, Moreno-López J, Kennedy S. Lesions in the reproductive tract of boars experimental infected with porcine rubulavirus. J Comp Pathol 1997;117:237-252.

  76. Ramírez-Mendoza H. Fisiopatología del paramixovirus del Ojo Azul a nivel testicular. (tesis de doctorado). México (Distrito Federal) México: Universidad Nacional Autónoma de México, 2000.

  77. Allan GM, MacNeilly F, Walker Y, Linné T, Moreno-López J, Hernández P, et al. A sequential study of experimental porcine paramyxovirus (LPMV) infection of pigs: immunostaining of cryostat sections and virus isolation. J Vet Diagn Invest 1996;8:405-413.

  78. MacNeilly F, Walker I, Allan G, Foster C, Linné T, Merza M, et al. A comparative study on the use of virus and antibody detection techniques for the diagnosis of La Piedad Michoacán paramyxovirus (LPMv) infection in pigs. J Vet Diagn Invest, 1997; 9: 3-9.

  79. Espinosa S. Evaluación de semen de verracos inoculados con el virus de la enfermedad del Ojo Azul (tesis de maestría). México (Distrito Federal) México: Universidad Nacional Autónoma de México, 2001.

  80. Rima B, Alexander BJ, Billeter MA, Collins PL, Kingsbury DW, Lipkind MA, et al. Family Paramyxoviridae, In: Murphy FA, Fauquet CM, Bishop DHL, Ghabrial SA, Jarvis AW, Matelli GP, et al., editors. Virus taxonomy: Classification and nomenclature of viruses. New York: Springer-Verlag, 1995:265-274.

  81. Sundqvist A, Berg M, Moreno-López J, Linné T. The hemagglutinin-neuraminidase glycoprotein of the porcine paramyxovirus LMPV: comparison with other paramyxovirus revealed the closest relationship to simian virus 5 and mumps virus. Arch Virol 1991;122:331-278.

  82. Berg M, Sundqvist A, Moreno-López J, Linné T. Identification of the porcine paramyxovirus LPMV matrix protein gene: comparative sequence análisis with other paramyxoviruses. J Gen Virol 1991;72:1045-1050.

  83. Berg M, Hjertner B, Moreno-López J, Linné T. The P gene of the porcine paramyxovirus LPMV encodes three possible polipeptides, P, V, and C; the P protein mRNA is edited. J Gen Virol 1992;73:1195-1200.

  84. Berg M, Bergvall AC, Svenda M, Sundqvist A, Moreno-López J, Linné T. Analysis of the fusion protein gene of the porcine rubulavirus LPMV: comparative analysis of paramyxoviruses F proteins. Virus Genes 1997;14:55-61.

  85. Wolinsky JS. Mumps. In: Fields BN, Knipe DM, Howley PM, editors. Fields in Virology. Filadelfia-Nueva York: Lippincott-Raven Publishers, 1996:1243-1266.

  86. Hernández J, Ramírez H, Carreón R, Mercado C, Lascuraín R, Hernández-Jaúregui P, et al. Several isolates of the Porcine Paramyxovirus can be sorted into two groups with different behavior. Memorias del III Congreso Internacional de Virología Veterinaria. Interlaken, Suiza. 1994:P1-6

  87. Sundqvist A, Berg M, Hernández-Jaúregui P, Linné T, and Moreno-López J. The structural proteins of a porcine paramyxovirus (LPMV). J Gen Virol 1990;71:609-613.

  88. Reyes-Leyva J, Hernández-Jaúregui P, Montaño L, Zenteno E. The porcine paramyxovirus LPM specifically recognize sialil (2-3) lactose-containing structures. Arch Virol 1993;133:195-200.

  89. Espinosa B, Reyes J, Hernández-Jaúregui P, Zenteno R, Ramírez H, Hernández J, et al. Carbohydrate specificity and porcine rubulavirus infectivity. In: Morilla A, Zimmerman J, Ion K, editors. Trends in Viral Emerging Diseases of Porcine. Ames, Ia:Iowa State University Press, 2002:81-85.

  90. Reyes-Leyva J, Espinosa B, Hernández J, Zenteno R, Vallejo V, Hernández-Jaúregui P, et al. E. NeuAca-2,3Gal-glycoconjugate expression determinates cell susceptibility to the porcine rubulavirus LPMV. Com Biochem Physiol 1997;118B:237-332.

  91. Vallejo V, Reyes-Leyva J, Hernández J, Ramírez H, Delannoy P, Zenteno E. Differential expression of sialic acid on porcine organs during the maturation process. Comp Biochem Physiol Biochem Mol Biol 2000;126:415-424.

  92. Hernández J, Reyes-Leyva J, Zenteno R, Ramírez H, Hernández-Jaúregui P, and Zenteno E. Immunity to porcine rubulavirus infection in adult porcine. Vet Immunol Immunopathol 1998;64:367-381.

  93. Hernández-Jáuregui P, Sundqvist A, Fuentes M, Díaz A, Reyes-Leyva J, Hernández E, Moreno-López J. Correlación entre las pruebas de virus neutralización, inhibición de la hemoaglutinación y ELISA en sueros vacunales y de brote para anticuerpos contra el Paramixovirus del Síndrome del Ojo Azul en cerdos. Vet Mex 1992;23:217-222.

  94. Zenteno R. Purificación y predicción de determinantes antigénicos y de estructura secundaria en la hemaglutinina-neuraminidasa del paramixovirus porcino de La Piedad Michoacán. (tesis de maestría). México (Distrito Federal) México: Universidad Nacional Autónoma de México, 1997.

  95. Ray R, Compans RW. Paramyxoviruses. In: Van Regenmortel MHB, Neurath AR editors. Immunochemistry of viruses II. The basis for serodiagnosis and vaccines. New York:Elsevier, 1990: 217-236.

  96. Abbas AK, Lichtman AH, Pober JS. Cellular and molecular immunology. 4 ed. Philadelphia Pennsylvania, W.B. Saunders, 2000.

  97. Griffit D, Ward B, Esolen L. Pathogenesis of mézales virus infection: a hypothesis for altered immune response. J Infect Dis 1994;170:S24-31.

  98. Griffit D, Bellini W. Measles Virus. In: Fields BN, Knipe DM, Howley PM, editors. Fields in Virology. Philadelphia. New York: Lippincott-Raven Publishers, 1996:1267-1312.

  99. Fujinami RS, and Oldstone MBA. Alterations in expression of measles virus polypeptides by antibody: molecular events in antibody induced antigenic modulation. J Immunol 1980;125:78-85.

  100. Hjertner B, Wiman AC, Svenda M, Berg M, Moreno-Lopez J, Linne T. Multiple factors including subgenomic RNAs and reduced viral protein expresión are associated with a persistent infection by porcine rubulavirus (LPMV). Arch Virol 1998;143:425-39.

  101. Wiman AC, Hjertner B, Linné T, Herron B, Allan G, McNeilly F, et al. Porcine rubulavirus LPMV RNA persists in the central nervous system of pigs after recovery from acute infection. J Neurovirol 1998;4:545-52.

  102. Hjertner B, Linné T, Moreno-López J. Establishment and characterization of a porcine rubulavirus (LPMV) persistent infection in porcine kidney cells. Acta Vet Scand 1997;38:213-24.

  103. Kasel JA, Frank AL, Keitel WA, Taber LH, Glezen WP. Acquisition of serum antibodies to specific viral glycoproteins of parainfluenza virus 3 in children. J Virol 1984;52:828-32.

  104. Reyes-Leyva J, Espinosa B, Santos G, Zenteno R, Hernández J, Vallejo V, et al. Purification and characterization of the hemagglutinin-neuraminidase of porcine rubulavirus LPMV. Glycoconj J 1999;16:517-522.

  105. Zenteno R, Hernández J, Espinosa B, Hernández-Jaúregui P, Reyes J, Zenteno E. Secondary structure prediction of the hemagglutinin neuraminidase from a porcine rubulavirus. Arch Virol 1998;143:333-352.

  106. Pescovitz M.D, Lunney J K, Sachs DH. Preparation and characterization of monoclonal antibodies reactive with porcine PBL. J Immunol 1984;133:368-373.

  107. Yang H, Parkhouse RM. Phenotypic classification of porcine lymphocytes sub-populations in blood and lymphoid tissues. Immunology 1996;89:76-83.

  108. Saalmueller A, Redheads M J, Buhring H J, Jonjic S, Koszinowski UH. Simultaneous expression of CD4 and CD8 antigens by a substantial proportion of resting porcine T lymphocytes. Eur J Immunol 1987;17:1297-1302.

  109. Pescovitz MD, Sakapoulos AG, Gaddy JA, Husmman RJ, Zuckemann FA. Porcine peripheral blood CD4+/CD8+ dual expressing T cells. Vet Immunol Immunopathol 1994;43:53-62.

  110. Zuckermann FA. Extrathymic CD4/CD8 doublepositive T cells. Vet Immunol Immunopathol 1999;72:55-66.

  111. Ward BJ, Johnson RT, Vaisberg A, Jaúregui E, Griffin DE. Cytokine production in vitro and the lymphoproliferative defect of natural measles virus infection. Clin Immunol Immunopathol 1991;61:236-48.

  112. Drew T. A review of evidence for immunosuppression due to Porcine Reproductive and Respiratory Syndrome Virus. Vet Rec 2000;31:27-39.

  113. Zuckermann F, Husmann RJ. Functional and phenotypic analysis of the peripheral blood CD4/CD8 double-positive T cells. Immunology 1996;87:500-512.

  114. Ivanoska D, Cuperlovic K, Lunney JK. Peripheral blood mononuclear cells subsets during Trichinella spiralis infection in pigs. Res Vet Sci 1990;49:92-97.

  115. Hernández J, Garfias Y, Nieto A, Mercado C, Montaño L, Zenteno E. Comparative evaluation of the CD4+CD8+ and CD4+CD8- lymphocytes in the immune response to porcine rubulavirus. Vet Immunol Immunopathol 2001;79:249-259.

  116. Summerfield A, Rhiza H, Saalmueller A. Functional characterization of porcine CD+4CD8+ extrathymic T lymphocytes. Cell Immunol 1996;168:291-296.

  117. Murail-Krishna K, Altman JD, Sures M, Sourdive DJD, Zajac AJ, Miller JD, et al. Counting antigen-specific CD8 T cells: a re-evaluation of bystander activation during viral infection. Immunity 1998;8:177-187.

  118. Rodríguez-Ropon A, Hernández-Jaúregui P, Sánchez-Torres L, Favila-Castillo L, Estrada-Parra S, Moreno-Lopez J, et al. Apoptosis in lymph nodes and changes in lymphocyte subpopulations in peripheral blood of pigs infected with porcine rubulavirus. J Comp Pathol 2003;128:1:8.

  119. Tripp RA, Hou S, McMickle A, Houston J, Doherty PC. Recruitment and proliferation of CD8+ T cells in respiratory virus infections. J Immunol 1995;154:6013-6021.

  120. Page G, Wang F, Hahn E. Interaction of pseudorabies virus with porcine peripheral blood lymphocytes. J Leukoc Biol 1992;52:441-48.

  121. Bradley RW, Swain LM. T cell memory. Annu Rev Immunol 1998;16:201-223.

  122. Galvan M, Murali-Krishna K, Lua L, Baum L, Ahmed R. Alterations in cell surface carbohydrates on T cells from virally infected mice can distinguís effector-memory CD8+ T cells from naïve cells. J Immunol 1998;161:641-648.

  123. Lascurain R, Porras F, Baez R, Chavez R, Martínez-Cairo S, Alvarez G, et al. Amaranthus leucocarpus recognizes human naive T cell subpopulations. Immunol Inevest 1997;26:579-587.

  124. Hernández J, Garfias Y, Reyes-Leyva J, Chávez R, Lascurain R, Zenteno E. Peanut and Amaranthus leucocarpus lectins discriminate between memory and naïve/quiescent porcine lymphocytes. Vet Immunol Immunopathol 84 2002;84:71-82.

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