Journal of Equine Veterinary Science
Volume 28, Issue 7 , Pages 419-426 , July 2008

CpG-Induced Stimulation of Cytokine Expression by Peripheral Blood Mononuclear Cells of Foals and Their Dams

  • Tong Liu, PhD

      Affiliations

    • Department of Large Animal Clinical Sciences, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, TX
    • ,
  • Jessica Nerren, PhD

      Affiliations

    • Department of Large Animal Clinical Sciences, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, TX
    • ,
  • Jennifer Murrell

      Affiliations

    • Department of Large Animal Clinical Sciences, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, TX
    • ,
  • Veronique Juillard, PhD

      Affiliations

    • Merial SAS Discovery, Lyon, France
    • ,
  • Hanane El Garch

      Affiliations

    • Merial SAS Discovery, Lyon, France
    • ,
  • Ronald Martens, DVM

      Affiliations

    • Department of Large Animal Clinical Sciences, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, TX
    • ,
  • Noah Cohen, VMD, MPH, PhD, DACVIM

      Affiliations

    • Department of Large Animal Clinical Sciences, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, TX
    • Corresponding Author InformationReprint requests: Noah D. Cohen, VMD, MPH, PhD, DACVIM, Professor, Department of Large Animal Clinical Sciences, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, Texas 77843-4475.

References 

  1. Van der Kolk H, Kraus H, Vink-Nooteboom M. Rhodococcus equi pneumonia in a foal. Equine Pract. 1999;21:6–9
  2. Martens RJ, Martens JG, Fiske RA. Rhodococcus equi foal pneumonia: pathogenesis and immunoprophylaxis. AAEP Proceedings. 1989;199–213
  3. Darrah PA, Monaco MC, Jain S, Hondalus MK, Golenbock DT, Mosser DM. Innate immune responses to Rhodococcus equi J Immunol. 2004;173:1914–1924
  4. Giguere S, Hondalus MK, Yager JA, Darrah P, Mosser DM, Prescott JF. Role of the 85-kilobase plasmid and plasmid-encoded virulence-associated protein A in intracellular survival and virulence of Rhodococcus equi. Infect Immun. 1999;67:3548–3557
  5. Patton KM, McGuire TC, Hines MT, Mealey RH, Hines SA. Rhodococcus equi-specific cytotoxic T lymphocytes in immune horses and development in asymptomatic foals. Infect Immun. 2005;73:2083–2093
  6. Prescott JF, Hoffman AM. Rhodococcus equi. Vet Clin North Am: Equine Pract. 1993;9:375–384
  7. Drancourt M, Bonnet E, Gallais H, Pelloux Y, Raoult D. Rhodococcus equi infection in patients with AIDS. J Infect. 1992;24:123–131
  8. Barouch DH, Letvin NL, Seder RA. The role of cytokine DNAs as vaccine adjuvants for optimizing cellular immune responses. Immunol Rev. 2004;202:266–274
  9. Kornbluth RS, Stone GW. Immunostimulatory combinations: designing the next generation of vaccine adjuvants. J Leukoc Biol. 2006;80:1084–1102
  10. Kanaly ST, Hines SA, Palmer GH. Failure of pulmonary clearance of Rhodococcus equi infection in CD4+ T-lymphocyte-deficient transgenic mice. Infect Immun. 1993;61:4929–4932
  11. Ross TL, Balson GA, Miners JS, Smith GD, Shewen PE, Prescott JF, et al. Role of CD4+, CD8+ and double negative T-cells in the protection of SCID/beige mice against respiratory challenge with Rhodococcus equi. Can J Vet Res. 1996;60:186–192
  12. Giguere S, Prescott JF. Equine immunity to bacteria. Vet Clin North Am: Equine Pract. 2000;16:29;iv
  13. Nordmann P, Ronco E, Nauciel C. Role of T-lymphocyte subsets in Rhodococcus equi infection. Infect Immun. 1992;60:2748–2752
  14. Meijer WG, Prescott JF. Rhodococcus equi. Vet Res. 2004;35:383–396
  15. Patton KM, McGuire TC, Fraser DG, Hines SA. Rhodococcus equi-infected macrophages are recognized and killed by CD8+ T lymphocytes in a major histocompatibility complex class I-unrestricted fashion. Infect Immun. 2004;72:7073–7083
  16. Chaffin MK, Cohen ND, Martens RJ, Edwards RF, Nevill M, Smith R. Hematologic and immunophenotypic factors associated with development of Rhodococcus equi pneumonia of foals at equine breeding farms with endemic infection. Vet Immunol Immunopathol. 2004;100:33–48
  17. Martens RJ, Cohen ND, Jones SL, Moore TA, Edwards JF. Protective role of neutrophils in mice experimentally infected with Rhodococcus equi. Infect Immun. 2005;73:7040–7042
  18. Lopez AM, Hecker R, Mutwiri G, van Drunen Littel-van den Hurk S, Babiuk LA, Townsend HG. Formulation with CpG ODN enhances antibody responses to an equine influenza virus vaccine. Vet Immunol Immunopathol. 2006;114:103–110
  19. Juffermans NP, Leemans JC, Florquin S, Verbon A, Kolk AH, Speelman P, et al. CpG oligodeoxynucleotides enhance host defense during murine tuberculosis. Infect Immun. 2002;70:147–152
  20. Bauer M, Redecke V, Ellwart J, Scherer B, Kremer J-P, Wagner H, et al. Bacterial CpG-DNA triggers activation and maturation of human CD11c-, CD123+ dendritic cells. J Immunol. 2001;166:5000–5007
  21. Krieg AM. CpG motifs in bacterial DNA and their immune effects. Ann Rev Immunol. 2002;20:709–760
  22. Yamamoto S, Yamamoto T, Nojima Y, Umemori K, Phalen S, McMurry DN, et al. Discovery of immunostimulatory CpG-DNA and its application to tuberculosis vaccine development. Jpn J Infect Dis. 2002;55:37–44
  23. Krieg AM. The role of CpG motifs in innate immunity. Curr Opin Immunol. 2000;12:35–43
  24. Mutwiri G, Pontarollo R, Babiuk S, Griebel P, van Drunen Littel-van den Hurk S, Mena A, et al. Biological activity of immunostimulatory CpG DNA motifs in domestic animals. Vet Immunol Immunopathol. 2003;91:89–103
  25. Wilson HL, Dar A, Napper SK, Lopez AM, Babiuk LA, Mutwiri GK. Immune mechanisms and therapeutic potential of CpG oligodeoxynucleotides. Int Rev Immunol. 2006;25:183–213
  26. Krieg AM. CpG motifs: the active ingredient in bacterial extracts?. Nat Med. 2003;9:831–835
  27. Tokunaga T, Yamamoto H, Shimada S. Antitumor activity of deoxyribonucleic acid fraction from Mycobacterium bovis BCG.I. Isolation, physicochemical characterization, and antitumor activity. J Nat Cancer Inst. 1984;72:955–962
  28. Vollmer J, Janosch A, Laucht M, Ballas ZK, Schetter C, Krieg AM. Highly immunostimulatory CpG-free oligodeoxynucleotides for activation of human leukocytes. Antisense Nucl Acid Drug Devel. 2002;12:165–175
  29. Zhang Y, Shoda L, Brayton K, Estes DM, Palmer GH, Brown WC. Induction of interleukin-6 and interleukin-12 in bovine B lymphocytes, monocytes, and macrophages by a CpG oligodeoxynucleotide (ODN 2059) containing the GTCGTT motif. J Interfer Cytokine Res. 2001;21:871–881
  30. Ray N, Krieg AM. Oral pretreatment of mice with CpG DNA reduces susceptibility to oral or intraperitoneal challenge with virulent Listeria moncytogenes. Infect Immun. 2003;71:4398–4404
  31. Hemmi H, Takeuchi O, Kawai T, Kaisho T, Sato S, Sanjo H, et al. A Toll-like receptor recognizes bacterial DNA. Nature. 2000;408:740–745
  32. Krieg AM. Mechanisms and applications of immune stimulatory CpG oligodeoxynucleotides. Biochim Biophys Acta. 1999;1489:107–116
  33. Hartmann G, Battiany J, Poeck H, Wagner M, Kerkmann M, Lubenow N, et al. Rational design of new CpG oligonucleotides that combine B cell activation with high IFN-α; induction in plasmacytoid dendritic cells. Eur J Immunol. 2003;33:1633–1641
  34. Marshall JD, Fearon K, Abbate C, Subramanian S, Yee P, Gregorio J, et al. Identification of a novel CpG DNA class and motif that optimally stimulate B cell and plasmacytoid dendritic cell functions. J Leukoc Biol. 2003;73:781–792
  35. Jurk M, Schulte B, Kritzler A, Noll B, Uhlmann E, Wader T. C-Class CpG ODN: sequence requirements and characterization of immunostimulatory activities on mRNA level. Immunobiology. 2004;209:141–154
  36. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2- delta delta method. Methods. 2001;25:402–408
  37. Ainsworth DM, Eicker SW, Yeagar AE, Sweeney CR, Viel L, Tesarowski D, et al. Associations between physical examination, laboratory, and radiographic findings and outcome and subsequent racing performance of foals with Rhodococcus equi infection: 115 cases (1984-1992). J Am Vet Med Assoc. 1998;213:510–515
  38. Boyd NK, Cohen ND, Lim WS, Martens RJ, Chaffin MK, Ball JM. Temporal changes in cytokine expression of foals during the first month of life. Vet Immunol Immunopathol. 2003;92:75–85
  39. Prescott JF, Yager JA. The control of Rhodococcus equi pneumonia in foals. In:  Plowright W,  Rossdale PD,  Wade JF editor. Equine infectious diseases VI. Newmarket. UK: R&W Publications; 1992;p. 21–25
  40. Breathnach CC, Sturgill-Wright T, Stiltner JL, Adams AA, Lunn DP, Horohov DW. Foals are interferon gamma-deficient at birth. Vet Immunol Immunopathol. 2006;112:199–209
  41. Chaffin MK, Cohen ND, Martens RJ, Edwards RF, Nevill M. Foal-related risk factors associated with development of Rhodococcus equi pneumonia on farms with endemic infection. J Am Vet Med Assoc. 2003;223:1791–1799
  42. Martens RJ, Cohen ND, Chaffin MK, Takai S, Doherty CL, Angulo AB, et al. Evaluation of 5 serologic assays to detect Rhodococcus equi pneumonia in foals. J Am Vet Med Assoc. 2002;221:825–833
  43. Gold JR, Perkins GA, Erb HN, Ainsworth DM. Cytokine profiles of peripheral blood mononuclear cells isolated from septic and healthy neonatal foals. J Vet Intern Med. 2007;21:482–488
  44. Langrish CL, Buddle JC, Thrasher AJ, Goldblatt D. Neonatal dendritic cells are intrinsically biased against Th-1 immune responses. Clin Exp Immunol. 2002;128:118–123
  45. Flynn J, Chan J, Triebold K, Dalton DK, Stewart TA, Bloom BR. An essential role for interferon in resistance to Mycobacterium tuberculosis infection. J Exp Med. 1993;178:2249–2254
  46. Kanaly ST, Hines SA, Palmer GH. Cytokine modulation alters pulmonary clearance of Rhodococcus equi and development of granulomatous pneumonia. Infect Immun. 1995;63:3037–3041
  47. Kohler AK, Stone DM, Hines MT, Byrne BA, Alperin DC, Norton LK, et al. Rhodococcus equi secreted antigens are immunogenic and stimulate a type 1 recall response in the lungs of horses immune to R. equi infection. Infect Immun. 2003;71:6329–6337
  48. McMurray DN. Determinants of vaccine-induced resistance in animal models of pulmonary tuberculosis. Scand J Infect Dis. 2001;33:175–178
  49. Jacks S, Giguere S, Crawford PC, Castleman WL. Experimental infection of neonatal foals with Rhodococcus equi triggers adult-like gamma interferon induction. Clin Vaccine Immunol. 2007;14:669–677
  50. Diehl S RM. The two faces of IL-6 on Th1/Th2 differentiation. Mol Immunol. 2002;39:531–536
  51. Dalrymple SA, Lucian LA, Slattery R, McNeil T, Aud DM, Fuchino S, et al. Interleukin-6-deficient mice are highly susceptible to Listeria monocytogenes infection: correlation with inefficient neutrophilia. Infect Immun. 1995;63:2262–2268
  52. Ladel CH, Blum C, Dreher A, Reifenberg K, Kopf M, Kaufmann SH. Lethal tuberculosis in interleukin-6-deficient mutant mice. Infect Immun. 1997;65:4843–4849
  53. Florido M, Goncalves AS, Silva RA, Ehlers S, Cooper AM, Appelberg R. Resistance of virulent Mycobacterium avium to gamma interferon-mediated antimicrobial activity suggests additional signals for induction of mycobacteriostasis. Infect Immun. 1999;67:3610–3618
  54. Goriely S, Goldman M. The interleukin-12 family: new players in transplantation immunity?. Am J Transplant. 2007;7:278–284
  55. Rudner XL, Happel KI, Young EA, Shellito JE. Interleukin-23 (IL-23)-IL-17 cytokine axis in murine Pneumocystis carinii infection. Infect Immun. 2007;75:3055–3061
  56. Watford WT, Moriguchi M, Morinobu A, O'Shea JJ. The biology of IL-12: coordinating innate and adaptive immune responses. Cytokine Growth Fact Rev. 2003;14:361–368
  57. Booth JS, Nichani AK, Benjamin P, Dar A, Krieg AM, Babiuk LA, et al. Innate immune responses induced by classes of CpG oligodeoxynucleotides in ovine lymph node and blood mononuclear cells. Vet Immunol Immunopathol. 2007;115:24–34
  58. Harandi AM, Eriksson K, Holmgren J. A protective role of locally administered immunostimulatory CpG oligodeoxynucleotide in a mouse model of genital herpes infection. J Virol. 2003;77:953–962
  59. Wernette CM, Smith BF, Barksdale ZL, Hecker R, Baker HJ. CpG oligodeoxynucleotides stimulate canine and feline immune cell proliferation. Vet Immunol Immunopathol. 2002;84:223–236
  60. Gramzinski RA, Doolan DL, Sedegah M, Davis HL, Krieg AM, Hoffman SL. Interleukin-12- and gamma interferon-dependent protection against malaria conferred by CpG oligodeoxynucleotide in mice. Infect Immun. 2001;69:1643–1649
  61. Jansky LRP, Kopecky J. Dynamics of cytokine production in human peripheral blood mononuclear cells stimulated by LPS or infected by Borrelia. Physiol Res. 2003;52:593–598
  62. Pontarollo RA, Rankin R, Babiuk LA, Godson DL, Griebel PJ, Hecker R, et al. Monocytes are required for optimum in vitro stimulation of bovine peripheral blood mononuclear cells by non-methylated CpG motifs. Vet Immunol Immunopathol. 2002;84:43–59

 Refereed

PII: S0737-0806(08)00188-3

doi: 10.1016/j.jevs.2008.05.005

Journal of Equine Veterinary Science
Volume 28, Issue 7 , Pages 419-426 , July 2008

Article Tools