CpG oligodeoxynucleotide promotes protective immunity in the enteric mucosa and suppresses enterotoxigenic E. coli in the weaning piglets

International Immunopharmacology

Volumn 10, Issue 10, 2010, Pages 1249-1260

  Cheng, Qing ^a   Jiang, Zhenggu ^b   Xu, Chenchao ^a   Li, Huazhou ^b   Cao, Ding ^a   Yang, Zhaihan ^b   Cao, Guangjun ^a   Linghua, Zhang ^a  

^a SOUTH CHINA AGRICULTURAL UNIVERSITY   (China)

^b Swine Seed Breeding Center of Guangzhou   (China)

Author keywords

CpG ODN; Enterotoxigenic Escherichia coli; Innate immunity; Piglets

Indexed keywords

BACTERIAL TOXIN; BETA DEFENSIN; CATHELICIDIN; CPG OLIGODEOXYNUCLEOTIDE; CXCL11 CHEMOKINE; ENTEROTOXIN; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; INTERLEUKIN 12; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; PR 39; PROTEGRIN; RANTES;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ANTIBODY SPECIFICITY; ARTICLE; BACTERIAL INFECTION; BACTERIUM; CLEARANCE; CONTRAST; CONTROLLED STUDY; CYTOKINE PRODUCTION; DELIVERY; ENTEROTOXIGENIC ESCHERICHIA COLI; HUMAN; INFECTION; INNATE IMMUNITY; INTESTINE MUCOSA; MUCOSAL IMMUNITY; NONHUMAN; PATHOGENESIS; PIGLET; PRIORITY JOURNAL; PROTECTION; PROTEIN EXPRESSION; WEANING;

ANIMALS; CPG ISLANDS; CYTOKINES; ENTEROTOXIGENIC ESCHERICHIA COLI; INTESTINAL MUCOSA; OLIGODEOXYRIBONUCLEOTIDES; RNA, MESSENGER; SWINE; SWINE DISEASES; WEANING;

EID: 77957242875     PISSN: 15675769     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.intimp.2010.07.006     Document Type: Article

References (54)

1. Odle J., Zijlstra T., Donovan S.M. Intestinal effects of milkborne growth factors in neonates of agricultural importance. J Anim Sci 1996, 74:2509-2522.
2. Frydendahl K. Prevalence of serogroups and virulence genes in Escherichia coli associated with post-weaning diarrhea and edema disease in pigs and a comparison of diagnostic approaches. Vet Microbiol 2002, 85:169-182.
3. Hampson D.J. Alternations in piglet small intestinal structure at weaning. Res Vet Sci 1986, 40:32-40.
4. Hampson D.J., Kidder D.E. Influence of creep feeding and weaning on brush border enzyme activities in the piglet small intestine. Res Vet Sci 1986, 40:24-31.
5. Monroe S., Polk R. Antimicrobial use and bacterial resistance. Curr Opin Microbiol 2000, 3:496-501.
6. Schwarz S., Kehrenberg C., Walsh T.R. Use of antimicrobial agents in veterinary medicine and food animal production. Int J Antimicrob Agents 2001, 17:431-437.
7. Murray B.E. New aspects of antimicrobial resistance and the resulting therapeutic dilemmas. J Infect Dis 1991, 163:1185-1194.
8. Neu H.C. The crisis in antibiotic resistance. Science 1992, 257:1064-1073.
9. Levy S.B. The challenge of antibiotic resistance. Sci Am 1998, 278:32-39.
10. Krieg A.M. The role of CpG motifs in innate immunity. Curr Opin Immunol 2000, 12:35-43.
11. Krieg A.M., Yi A., Matson S., Waldschmidt T.J., Bishop G.A., Teasdale R., et al. CpG motifs in bacterial DNA trigger direct B-cell activation. Nature 1995, 374:546-548.
12. Klinman D.M., Yi A.K., Beaucage S.L., Conover J., Krieg A.M. CpG motifs present in bacteria DNA rapidly induce lymphocytes to secrete interleukin 6, interleukin 12, and interferon gamma. Proc Natl Acad Sci USA 1996, 93:2879-2883.
13. Krieg A.M. CpG motifs in bacterial DNA and their immune effects. Annu Rev Immunol 2002, 20:709-760.
14. Krieg A.M. Therapeutic potential of Toll-like receptor 9 activation. Nat Rev Drug Discov 2006, 5:471-484.
15. Harandi A.M., 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(2):953-962.
16. Ashkar A.A., Bauer S., Mitchell W.J., Vieira J., Rosenthal K.L. Local delivery of CpG oligodeoxynucleotides induces rapid changes in the genital mucosa and inhibits replication, but not entry, of herpes simplex virus type 2. J Virol 2003, 77(16):8948-8956.
17. Olbrich A.R., Schimmer S., Heeg K., Schepers K., Schumacher T.N., Dittmer U. Effective postexposure treatment of retrovirus-induced disease with immunostimulatory DNA containing CpG motifs. J Virol 2002, 76(22):11397-11404.
18. Verthelyi D., Gursel M., Kenney R.T., Lifson J.D., Liu S., Mican J., et al. CpG oligodeoxynucleotides protect normal and SIV-infected macaques from Leishmania infection. J Immunol 2003, 170(9):4717-4723.
19. Juffermans N.P., Leemans J.C., Florquin S., Verbon A., Kolk A.H., Speelman P., et al. CpG oligodeoxynucleotides enhance host defense during murine tuberculosis. Infect Immun 2002, 70(1):147-152.
20. Van der Stede Y., Cox E., Verdonck F., Vancaeneghem S., Goddeeris B.M. Reduced faecal excretion of F4+-E. coli by the intramuscular immunisation of suckling piglets by the addition of 1a, 25-dihydroxyvitamin D3 or CpG-oligodeoxynucleotides. Vaccine 2003, 21:1023-1032.
21. Hancock R.E., Sahl H.G. Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat Biotechnol 2006, 24:1551-1557.
22. Cheng Q., Xu C.C., Zhang L.H., Li J.Q., Cao T., Zhang M.R. Administered CpG Oligodeoxynucleotide induces mRNA expression of CXC and CC chemokines at the intestinal mucosa and PBMCs in piglets. Int Immunopharmacol 2010, 10:611-618.
23. Kamstrup S., Daniela V., Dennis M.K. Response of porcine peripheral blood mononuclear cells to CpG-containing oligodeoxynucleotides. Vet Microbiol 2001, 78(4):353-362.
24. Zhang L.H., Tian X.S., Zhou F.Z. In vivo immunostimulatory effects of CpG ODN in newborn piglets. Mol Immunol 2007, 44(6):1238-1244.
25. Zhang L.H., Tian X.S., Zhou F.Z. In vivo oral administration effects of various oligodeoxynucleotides containing synthetic immunostimulatory motifs in the immune response to pseudorabies attenuated virus vaccine in newborn piglets. Vaccine 2008, 26:224-233.
26. Nichani A.K., Kaushik R.S., Mena A., Popowych Y., Dent D., Townsend H.G., et al. CpG oligodeoxynucleotide induction of antiviral effector molecules in sheep. Cell Immunol 2004, 227:24-37.
27. Nichani A.K., Mena A., Kaushik R.S., Mutwiri G.K., Townsend H.G., Hecker R., et al. Stimulation of innate immune responses by CpG oligodeoxynucleotide in newborn lambs can reduce bovine herpesvirus-1 shedding. Oligonucleotides 2006, 16:58-67.
28. Michael J.M., Risini D.W., Arthur M.K., Heather L.D. CpG ODN is an effective oral adjuvant to protein antigens in mice. Vaccine 2001, 19:950-957.
29. Giardeau J.P. A new in vitro technique for attachment to intestinal villi using enteropathogenic Escherichia coli. Ann Microbiol 1980, 131B:31-37.
30. Asmi C.M., Tassakka A.R., Savan R., Watanuki H., Sakai M. The in vitro effects of CpG oligodeoxynucleotides on the expression of cytokine genes in the common carp (Cyprinus carpio L.) head kidney cells. Vet Immunol Immunopathol 2006, 110(1-2):79-85.
31. -{increment}{increment}Ct method. Methods 2001, 25:402-408.
32. Zhang L.H., Guo Y., Tian X.S., Zhou F.Z. CpG oligodinucleotides induce strong humoral and cellular responses to swine streptococcic septicemia vaccine in piglets in vivo. Int Immunopharmacol 2006, 6(3):342-350.
33. Wilson H.L., Dar A., Napper S.K. Marianela Lopez A, Babiuk LA, Mutwiri GK. Immune mechanisms and therapeutic potential of CpG oligodeoxynucleotides. Int Rev Immunol 2006, 25:183-213.
34. Gramzinski R.A., Doolan D.L., Sedegah M., Davis H.L., Krieg A.M., Hoffman S.L. Interleukin-12- and gamma interferon-dependent protection against malaria conferred by CpG oligodeoxynucleotide in mice. Infect Immun 2001, 69:1643-1649.
35. Elkins K.L., Rhinehart-Jones T.R., Stibitz S., Conover J.S., Klinman D.M. Bacterial DNA, containing CpG motifs stimulates lymphocyte-dependent protection of mice against lethal infection with intracellular bacteria. J Immunol 1999, 162(4):2291-2298.
36. Krieg A.M., Love-Homan L., Yi A.K., Harty J.T. CpG DNA, induces sustained IL-12 expression in vivo and resistance to Listeria monocytogenes challenge. J Immunol 1998, 161(5):2428-2434.
37. Zimmermann S., Egeter O., Hausmann S., Lipford G.B., Rocken M., Wagner H., et al. CpG oligodeoxynucleotides trigger protective and curative Th1 responses in lethal murine leishmaniasis. J Immunol 1998, 160(8):3627-3630.
38. Raghavan S., Nyström J., Fredriksson M., Holmgren J., Harandi A.M. Orally administered CpG oligodeoxynucleotide induces production of CXC and CC chemokines in the gastric mucosa and suppresses bacterial colonization in a mouse model of Helicobacter pylori infection. Infect Immun 2003, 71(12):7014-7022.
39. Gursel M., Verthelyi D., Gursel I., Ishii K.J., Klinman D.M. Differential and competitive activation of human immune cells by distinct classes of CpG oligodeoxynucleotide. J Leukoc Biol 2002, 71:813-820.
40. Dong L., Mori I.M., Hossain B.L., Kimura Y. An immunostimulatory oligodeoxynucleotide containing a cytidine-guanosine motif protects senescence-accelerated mice from lethal influenza virus by augmenting the T helper type 1 response. J Gen Virol 2003, 84:1623-1628.
41. Zlotnick A., Yoshie O. Chemokines: a new classification system and their role in immunity. Immunity 2000, 12:121-127.
42. Baggiolini M., Dewald B., Moser B. Interleukin-8 and related chemotactic cytokines-CXC and CC chemokines. Adv Immunol 1994, 55:97-179.
43. Moser B., Loetscher P. Lymphocyte traffic control by chemokines. Nat Immunol 2001, 2:123-128.
44. Taub D.D., Conlon K., Lloyd A.R., Oppenheim J.J., Kelvin D.J. Preferential migration of activated CD4 and CD8T cells in response to MIP-1 alpha and MIP-1 beta. Science 1993, 260:355-358.
45. Uguccioni M., Apuzzo M.D., Loetscher M., Dewald B., Baggiolini M. Actions of the chemotactic cytokines MCP-1, MCP-2, MCP-3, RANTES, MIP-1 alpha and MIP-1 beta on human monocytes. Eur J Immunol 1995, 25:64-68.
46. Johansson E.L., Rask C., Fredriksson M., Eriksson K., Czerkinsky C., Holmgren M. Antibodies and antibody-secreting cells in the female genital tract after vaginal or intranasal immunization with cholera toxin B subunit or conjugates. Infect Immunol 1998, 66(2):514-520.
47. Deng J.C., Moore T.A., Newstead M.W., Zeng X., Krieg A.M., Standiford T.J. CpG oligodeoxynucleotides stimulate protective innate immunity against pulmonary Klebsiella infection. J Immunol 2004, 173:5148-5155.
48. Beutler B. Innate immunity: an overview. Mol Immunol 2004, 40:845-859.
49. Bosi P., Gremokolini C., Trevisi P. Dietary regulations of the intestinal barrier function at weaning. Asian-australas J Anim Sci 2003, 16:596-608.
50. Van den Broeck W., Cox E., Goddeeris B.M. Receptor-dependent immune responses in pigs after oral immunisation with F4 fimbriae. Infect Immun 1999, 67:520-526.
51. Enioutina E.Y., Visic D., Daynes R.A. The induction of systemic and mucosal immune responses to antigen-adjuvant compositions administered into the skin: alterations in the migratory properties of dendritic cells appears to be important for stimulating mucosal immunity. Vaccine 2000, 18:2753-2767.
52. Taghavi A., Allan B., Mutwiri G., Foldvari M., Van Kessel A., Willson P., et al. Enhancement of immunoprotective effect of CpG ODN by formulation with polyphosphazenes against E. coli septicemia in neonatal chickens. Curr Drug Deliv 2009, 6:76-82.
53. Ioannou X.P., Griebel P., Hecker R., Babiuk L.A., van Drunen Littel-van den Hurk S. The immunogenicity and protective efficacy of bovine herpesvirus 1 glycoprotein D plus Emulsigen are increased by formulation with CpG oligodeoxynucleotides. J Virol 2002, 76:9002-9010.
54. Klinman D.M., Verthelyi D., Takeshita F., Ishii K.J. Immune recognition of foreign DNA: a cure for bioterrorism. Immunity 1999, 11:123-129.