Yersinia enterocolitica promotes robust mucosal inflammatory T-cell immunity in murine neonates

Infection and Immunity

Volumn 78, Issue 8, 2010, Pages 3595-3608

  Echeverry, Andrea ^a   Saijo, Shinobu ^b   Schesser, Kurt ^a   Adkins, Becky ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; ANTIGEN; GAMMA INTERFERON; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2A; INTERLEUKIN 17; BACTERIAL ANTIGEN; BACTERIUM ANTIBODY; IMMUNOGLOBULIN G; LCRV PROTEIN, YERSINIA; PORE FORMING CYTOTOXIC PROTEIN;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ANTIGEN PRESENTING CELL; ARTICLE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL POPULATION; CELLULAR IMMUNITY; CONTROLLED STUDY; FEMALE; IMMUNOGLOBULIN BLOOD LEVEL; LYMPH NODE; MOUSE; MOUTH INFECTION; MOUTH MUCOSA; MUCOSA INFLAMMATION; NEWBORN; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; T LYMPHOCYTE; YERSINIA ENTEROCOLITICA; ANIMAL; BAGG ALBINO MOUSE; BLOOD; C57BL MOUSE; IMMUNOLOGY; INNATE IMMUNITY; INTESTINE MUCOSA; MICROBIOLOGY; SECRETION; YERSINIA INFECTION;

ANIMALS; ANIMALS, NEWBORN; ANTIBODIES, BACTERIAL; ANTIGENS, BACTERIAL; B-LYMPHOCYTES; CD4-POSITIVE T-LYMPHOCYTES; FEMALE; IMMUNITY, INNATE; IMMUNOGLOBULIN G; INTERFERON-GAMMA; INTERLEUKIN-17; INTESTINAL MUCOSA; LYMPH NODES; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; PORE FORMING CYTOTOXIC PROTEINS; YERSINIA ENTEROCOLITICA; YERSINIA INFECTIONS;

EID: 77955302687     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01272-09     Document Type: Article

References (78)

1. Abolhassani, M., M. Lagranderie, I. Caminshi, F. Romain, A. M. Balazuc, M. C. Wagner, M. Tanguy, L. Fiette, I. Sobhani, G. Milon, and G. Marchal. 2006. Similar functional activity of dendritic cells recruited to the mesenteric lymph nodes of newborn and adult mice after the rectal delivery of Mycobacterium bovis BCG. Microbes Infect. 8:2341-2351. (Pubitemid 44499048)
2. Adkins, B., Y. Bu, E. Cepero, and R. Perez. 2000. Exclusive Th2 primary effector function in spleens but mixed Th1/Th2 function in lymph nodes of murine neonates. J. Immunol. 164:2347-2353. (Pubitemid 30115461)
3. h1 memory effector function in murine neonates. J. Immunol. 166:918-925.
4. Adkins, B., Y. Bu, and P. Guevara. 2002. Murine neonatal CD4+ lymph node cells are highly deficient in the development of antigen-specific Th1 function in adoptive adult hosts. J. Immunol. 169:4998-5004. (Pubitemid 35217167)
5. Adkins, B., C. Leclerc, and S. Marshall-Clarke. 2004. Neonatal adaptive immunity comes of age. Nat. Rev. Immunol. 4:553-564.
6. Autenrieth, I. B., V. Kempf, T. Sprinz, S. Preger, and A. Schnell. 1996. Defense mechanisms in Peyer's patches and mesenteric lymph nodes against Yersinia enterocolitica involve integrins and cytokines. Infect. Immun. 64: 1357-1368.
7. Autenrieth, I. B., A. Tingle, A. Reske-Kunz, and J. Heesemann. 1992. T lymphocytes mediate protection against Yersinia enterocolitica in mice: characterization of murine T-cell clones specific for Y. enterocolitica. Infect. Immun. 60:1140-1149.
8. Barrier, M., S. Lacroix-Lamande, R. Mancassola, G. Auray, N. Bernardet, A. M. Chausse, S. Uematsu, S. Akira, and F. Laurent. 2006. Oral and intraperitoneal administration of phosphorothioate oligodeoxynucleotides leads to control of Cryptosporidium parvum infection in neonatal mice. J. Infect. Dis. 193:1400-1407.
9. Barrios, C., P. Brawand, M. Berney, C. Brandt, P. H. Lambert, and C. A. Siegrist. 1996. Neonatal and early life immune responses to various forms of vaccine antigens qualitatively differ from adult responses: predominance of a Th2-biased pattern which persists after adult boosting. Eur. J. Immunol. 26:1489-1496.
10. Baselski, V., R. Briggs, and C. Parker. 1977. Intestinal fluid accumulation induced by oral challenge with Vibrio cholerae or cholera toxin in infant mice. Infect. Immun. 15:704-712.
11. Bjarnarson, S. P., H. Jakobsen, G. Del Giudice, E. Trannoy, C. A. Siegrist, and I. Jonsdottir. 2005. The advantage of mucosal immunization for polysaccharide-specific memory responses in early life. Eur. J. Immunol. 35: 1037-1045.
12. Bowman, L. M., and P. G. Holt. 2001. Selective enhancement of systemic Th1 immunity in immunologically immature rats with an orally administered bacterial extract. Infect. Immun. 69:3719-3727.
13. Branger, C. G., A. Torres-Escobar, W. Sun, R. Perry, J. Fetherston, K. L. Roland, and R. Curtiss III. 2009. Oral vaccination with LcrV from Yersinia pestis KIM delivered by live attenuated Salmonella enterica serovar Typhimurium elicits a protective immune response against challenge with Yersinia pseudotuberculosis and Yersinia enterocolitica. Vaccine 27:5363-5370.
14. Brynjolfsson, S. F., S. P. Bjarnarson, E. Mori, G. Del Giudice, and I. Jonsdottir. 2008. Neonatal immune response and serum bactericidal activity induced by a meningococcal conjugate vaccine is enhanced by LT-K63 and CpG2006. Vaccine 26:4557-4562.
15. Burns-Guydish, S. M., I. N. Olomu, H. Zhao, R. J. Wong, D. K. Stevenson, and C. H. Contag. 2005. Monitoring age-related susceptibility of young mice to oral Salmonella enterica serovar Typhimurium infection using an in vivo murine model. Pediatr. Res. 58:153-158.
16. - vaccine strain is safe and effective in young BALB/c mice. Neonatology 91:114-120.
17. Capozzo, A. V., L. Cuberos, M. M. Levine, and M. F. Pasetti. 2004. Mucosally delivered Salmonella live vector vaccines elicit potent immune responses against a foreign antigen in neonatal mice born to naive and immune mothers. Infect. Immun. 72:4637-4646.
18. Daniel, C., F. Sebbane, S. Poiret, D. Goudercourt, J. Dewulf, C. Mullet, M. Simonet, and B. Pot. 2009. Protection against Yersinia pseudotuberculosis infection conferred by a Lactococcus lactis mucosal delivery vector secreting LcrV. Vaccine 27:1141-1144.
19. Duchet-Suchaux, M., C. Le Maitre, and A. Bertin. 1990. Differences in susceptibility of inbred and outbred infant mice to enterotoxigenic Escherichia coli of bovine, porcine and human origin. J. Med. Microbiol. 31:185-190.
20. Echeverry, A., K. Schesser, and B. Adkins. 2007. Murine neonates are highly resistant to Yersinia enterocolitica following orogastric exposure. Infect. Immun. 75:2234-2243.
21. Fadel, S., and M. Sarzotti. 2000. Cellular immune responses in neonates. Int. Rev. Immunol. 19:173-193.
22. + T cell responses to herpes simplex virus type 2 in neonatal mice. J. Immunol. 180:1556-1564.
23. Fernandez, M. I., A. Thuizat, T. Pedron, M. Neutra, A. Phalipon, and P. J. Sansonetti. 2003. A newborn mouse model for the study of intestinal pathogenesis of shigellosis. Cell Microbiol. 5:481-491.
24. Garvy, B. A., and A. G. Harmsen. 1996. The importance of neutrophils in resistance to pneumococcal pneumonia in adult and neonatal mice. Inflammation 20:499-512.
25. Genovese, F., G. Mancuso, M. Cuzzola, C. Biondo, C. Beninati, D. Delfino, and G. Teti. 1999. Role of IL-10 in a neonatal mouse listeriosis model. J. Immunol. 163:2777-2782. (Pubitemid 29399205)
26. Reference deleted.
27. Hale, C., I. R. Humphreys, T. Hussell, F. Bowe, S. Clare, D. Pickard, A. Preston, G. Del Giudice, and G. Dougan. 2004. Mucosal immunisation of murine neonates using whole cell and acellular pertussis vaccines. Vaccine 22:3595-3602. (Pubitemid 39099635)
28. Handley, S. A., P. H. Dube, and V. L. Miller. 2006. Histamine signaling through the H2 receptor in the Peyer's patch is important for controlling Yersinia enterocolitica infection. Proc. Natl. Acad. Sci. U. S. A. 103:9268-9273.
29. Huang, C. F., C. C. Wang, T. C. Wu, K. G. Wu, C. C. Lee, and H. J. Peng. 2008. Neonatal sublingual vaccination with Salmonella proteins and adjuvant cholera toxin or CpG oligodeoxynucleotides induces mucosal and systemic immunity in mice. J. Pediatr. Gastroenterol. Nutr. 46:262-271.
30. Ishigame, H., S. Kakuta, T. Nagai, M. Kadoki, A. Nambu, Y. Komiyama, N. Fujikado, Y. Tanahashi, A. Akitsu, H. Kotaki, K. Sudo, S. Nakae, C. Sasakawa, and Y. Iwakura. 2009. Differential roles of interleukin-17A and -17F in host defense against mucoepithelial bacterial infection and allergic responses. Immunity 30:108-119.
31. Ito, S., K. J. Ishii, M. Gursel, H. Shirotra, A. Ihata, and D. M. Klinman. 2005. CpG oligodeoxynucleotides enhance neonatal resistance to Listeria infection. J. Immunol. 174:777-782. (Pubitemid 40094272)
32. Ivanov, I. I., K. Atarashi, N. Manel, E. L. Brodie, T. Shima, U. Karaoz, D. Wei, K. C. Goldfarb, C. A. Santee, S. V. Lynch, T. Tanoue, A. Imaoka, K. Itoh, K. Takeda, Y. Umesaki, K. Honda, and D. R. Littman. 2009. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 139:485-498.
33. Ivanov, I. I., L. Frutos Rde, N. Manel, K. Yoshinaga, D. B. Rifkin, R. B. Sartor, B. B. Finlay, and D. R. Littman. 2008. Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe 4:337-349.
34. Jakobsen, H., S. Bjarnarson, G. Del Giudice, M. Moreau, C. A. Siegrist, and I. Jonsdottir. 2002. Intranasal immunization with pneumococcal conjugate vaccines with LT-K63, a nontoxic mutant of heat-labile enterotoxin, as adjuvant rapidly induces protective immunity against lethal pneumococcal infections in neonatal mice. Infect. Immun. 70:1443-1452.
35. Jupelli, M., M. N. Guentzel, P. A. Meier, G. Zhong, A. K. Murthy, and B. P. Arulanandam. 2008. Endogenous IFN-γ production is induced and required for protective immunity against pulmonary chlamydial infection in neonatal mice. J. Immunol. 180:4148-4155.
36. Kamath, A. T., A.-F. Rochat, M. P. Valenti, E. M. Agger, K. Lingnau, P. Andersen, P.-H. Lambert, and C.-A. Siegrist. 2008. Adult-like anti-mycobacterial T cell and in vivo dendritic cell responses following neonatal immunization with Ag85B-ESAT-6 in the IC31 adjuvant. PLoS One 3:e3683.
37. Kamath, A. T., A. F. Rochat, D. Christensen, E. M. Agger, P. Andersen, P. H. Lambert, and C. A. Siegrist. 2009. A Liposome-based mycobacterial vaccine induces potent adult and neonatal multifunctional T cells through the exquisite targeting of dendritic cells. PLoS One 4:e5771.
38. Keilbaugh, S. A., M. E. Shin, R. F. Banchereau, L. D. McVay, N. Boyko, D. Artis, J. J. Cebra, and G. D. Wu. 2005. Activation of RegIIIβ/γ and interferon-γ expression in the intestinal tract of SCID mice: an innate response to bacterial colonisation of the gut. Gut 54:623-629.
39. + regulatory T cells on the immune response to rotavirus infection. Vaccine 26:5601-5611.
40. Kitamura, D., J. Roes, R. Kuhn, and K. Rajewsky. 1991. A B cell-deficient mouse by targeted disruption of the membrane exon of the immunoglobulin μ chain gene. Nature 350:423-426. (Pubitemid 21912244)
41. Kollmann, T. R., J. Crabtree, A. Rein-Weston, D. Blimkie, F. Thommai, X. Y. Wang, P. M. Lavoie, J. Furlong, E. S. Fortuno III, A. M. Hajjar, N. R. Hawkins, S. G. Self, and C. B. Wilson. 2009. Neonatal innate TLR-mediated responses are distinct from those of adults. J. Immunol. 183:7150-7160.
42. Kollmann, T. R., B. Reikie, D. Blimkie, S. S. Way, A. M. Hajjar, K. Arispe, A. Shaulov, and C. B. Wilson. 2007. Induction of protective immunity to Listeria monocytogenes in neonates. J. Immunol. 178:3695-3701. (Pubitemid 46417637)
43. + regulatory T cells. Proc. Natl. Acad. Sci. U. S. A. 105:18460-18465.
44. Kovarik, J., M. Gaillard, X. Martinez, P. Bozzotti, P. H. Lambert, T. F. Wild, and C. A. Siegrist. 2001. Induction of adult-like antibody, Th1, and CTL responses to measles hemagglutinin by early life murine immunization with an attenuated vaccinia-derived NYVAC(K1L) viral vector. Virology 285:12-20. (Pubitemid 32589003)
45. Leav, B. A., M. Yoshida, K. Rogers, S. Cohen, N. Godiwala, R. S. Blumberg, and H. Ward. 2005. An early intestinal mucosal source of gamma interferon is associated with resistance to and control of Cryptosporidium parvum infection in mice. Infect. Immun. 73:8425-8428.
46. Lee, H. H., C. M. Hoeman, J. C. Hardaway, F. B. Guloglu, J. S. Ellis, R. Jain, R. Divekar, D. M. Tartar, C. L. Haymaker, and H. Zaghouani. 2008. Delayed maturation of an IL-12-producing dendritic cell subset explains the early Th2 bias in neonatal immunity. J. Exp. Med. 205:2269-2280.
47. Levy, O., E. E. Suter, R. L. Miller, and M. R. Wessels. 2006. Unique efficacy of Toll-like receptor 8 agonists in activating human neonatal antigen-presenting cells. Blood 108:1284-1290. (Pubitemid 44232026)
48. Li, L., H. H. Lee, J. J. Bell, R. K. Gregg, J. S. Ellis, A. Gessner, and H. Zaghouani. 2004. IL-4 utilizes an alternative receptor to drive apoptosis of Th1 cells and skews neonatal immunity toward Th2. Immunity 20:429-440. (Pubitemid 38482121)
49. Liang, S. C., X.-Y. Tan, D. P. Luxenberg, R. Karim, K. Dunussi-Joannopoulos, M. Collins, and L. A. Fouser. 2006. Interleukin (IL)-22 and IL-17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides. J. Exp. Med. 203:2271-2279.
50. Loeffler, D. I., K. Smolen, L. Aplin, B. Cai, and T. R. Kollmann. 2009. Fine-tuning the safety and immunogenicity of Listeria monocytogenes-based neonatal vaccine platforms. Vaccine 27:919-927.
51. Ma, Y., and A. C. Ross. 2005. The anti-tetanus immune response of neonatal mice is augmented by retinoic acid combined with polyriboinosinic: polyribocytidylic acid. Proc. Natl. Acad. Sci. U. S. A. 102:13556-13561.
52. Macpherson, A. J., and K. Smith. 2006. Mesenteric lymph nodes at the center of immune anatomy. J. Exp. Med. 203:497-500.
53. Marchant, A., T. Goetghebuer, M. O. Ota, I. Wolfe, S. J. Ceesay, D. De Groote, T. Corrah, S. Bennett, J. Wheeler, K. Huygen, P. Aaby, K. P. McAdam, and M. J. Newport. 1999. Newborns develop a Th1-type immune response to Mycobacterium bovis bacillus Calmette-Guerin vaccination. J. Immunol. 163:2249-2255. (Pubitemid 29382234)
54. Marin-Gallen, S., F. J. Perez-Cano, M. Castell, C. Castellote, and A. Franch. 2008. Intestinal intraepithelial NK and NKT cell ontogeny in Lewis rats. Dev. Comp. Immunol. 32:1405-1408.
55. Martinez, X., C. Brandt, F. Saddallah, C. Tougne, C. Barrios, F. Wild, G. Dougan, P. H. Lambert, and C. A. Siegrist. 1997. DNA immunization circumvents deficient induction of T helper type 1 and cytotoxic T lymphocyte responses in neonates and during early life. Proc. Natl. Acad. Sci. U. S. A. 94:8726-8731.
56. Min, B., R. McHugh, G. D. Sempowski, C. Mackall, G. Foucras, and W. E. Paul. 2003. Neonates support lymphopenia-induced proliferation. Immunity 18:131-140.
57. Pihlgren, M., C. Tougne, P. Bozzotti, A. Fulurija, M. A. Duchosal, P. H. Lambert, and C. A. Siegrist. 2003. Unresponsiveness to lymphoid-mediated signals at the neonatal follicular dendritic cell precursor level contributes to delayed germinal center induction and limitations of neonatal antibody responses to T-dependent antigens. J. Immunol. 170:2824-2832. (Pubitemid 36302152)
58. Reference deleted.
59. Ramirez, K., A. V. E. Capozzo, S. A. Lloyd, M. B. Sztein, J. P. Nataro, and M. F. Pasetti. 2009. Mucosally delivered Salmonella typhi expressing the Yersinia pestis F1 antigen elicits mucosal and systemic immunity early in life and primes the neonatal immune system for a vigorous anamnestic response to parenteral F1 boost. J. Immunol. 182:1211-1222.
60. Ramirez, K., Y. Ditamo, L. Rodriguez, W. L. Picking, M. L. van Roosmalen, K. Leenhouts, and M. F. Pasetti. 2010. Neonatal mucosal immunization with a non-living, non-genetically modified Lactococcus lactis vaccine carrier induces systemic and local Th1-type immunity and protects against lethal bacterial infection. Mucosal Immunol. 3:159-171.
61. Rhee, S. J., W. A. Walker, and B. J. Cherayil. 2005. Developmentally regulated intestinal expression of IFN-γ and its target genes and the age-specific response to enteric Salmonella infection. J. Immunol. 175:1127-1136.
62. Sarzotti, M., T. A. Dean, M. P. Remington, C. D. Ly, P. A. Furth, and D. S. Robbins. 1997. Induction of cytotoxic T cell responses in newborn mice by DNA immunization. Vaccine 15:795-797. (Pubitemid 27287958)
63. - lymphocytes during infection with Salmonella enterica serovar Enteritidis and has a mild effect in bacterial clearance. Int. Immunol. 20:1129-1138.
64. Shimomura, Y., A. Ogawa, M. Kawada, K. Sugimoto, E. Mizoguchi, H.-N. Shi, S. Pillai, A. K. Bhan, and A. Mizoguchi. 2008. A unique B2 B cell subset in the intestine. J. Exp. Med. 205:1343-1355.
65. Siegrist, C.-A., and R. Aspinall. 2009. B-cell responses to vaccination at the extremes of age. Nat. Rev. Immunol. 9:185-194.
66. Siegrist, C. A. 2001. Neonatal and early life vaccinology. Vaccine 19:3331-3346.
67. Sun, C.-M., L. Fiette, M. Tanguy, C. Leclerc, and R. Lo-Man. 2003. Ontogeny and innate properties of neonatal dendritic cells. Blood 102:585-591.
68. Takatori, H., Y. Kanno, W. T. Watford, C. M. Tato, G. Weiss, I. I. Ivanov, D. R. Littman, and J. J. O'Shea. 2009. Lymphoid tissue inducer-like cells are an innate source of IL-17 and IL-22. J. Exp. Med. 206:35-41.
69. Tourais-Esteves, I., N. Bernardet, S. Lacroix-Lamandé, S. Ferret-Bernard, and F. Laurent. 2008. Neonatal goats display a stronger Th1-type cytokine response to TLR ligands than adults. Dev. Comp. Immunol. 32:1231-1241.
70. VanCott, J. L., A. E. Prada, M. M. McNeal, S. C. Stone, M. Basu, B. Huffer, Jr., K. L. Smiley, M. Shao, J. A. Bean, J. D. Clements, A. H. C. Choi, and R. L. Ward. 2006. Mice develop effective but delayed protective immune responses when immunized as neonates either intranasally with nonliving VP6/LT(R192G) or orally with live rhesus rotavirus vaccine candidates. J. Virol. 80:4949-4961.
71. Vanden Eijnden, S., S. Goriely, D. De Wit, M. Goldman, and F. Willems. 2006. Preferential production of the IL-12(p40)/IL-23(p19) heterodimer by dendritic cells from human newborns. Eur. J. Immunol. 36:21-26.
72. + T lymphocytes. Eur. J. Immunol. 31:1531-1535.
73. Viboud, G. I., and J. B. Bliska. 2005. Yersinia outer proteins: role in modulation of host cell signaling responses and pathogenesis. Annu. Rev. Microbiol. 59:69-89.
74. Walker, W. E., and D. R. Goldstein. 2007. Neonatal B cells suppress innate Toll-like receptor immune responses and modulate alloimmunity. J. Immunol. 179:1700-1710.
75. Williams, M. A., and M. J. Bevan. 2004. Shortening the infectious period does not alter expansion of CD8 T cells but diminishes their capacity to differentiate into memory cells. J. Immunol. 173:6694-6702.
76. Wong, C. Y., G. Mayrhofer, M. W. Heuzenroeder, H. M. Atkinson, D. M. Quinn, and R. L. Flower. 1996. Measurement of virulence of aeromonads using a suckling mouse model of infection. FEMS Immunol. Med. Microbiol. 15:233-241.
77. Zheng, Y., P. A. Valdez, D. M. Danilenko, Y. Hu, S. M. Sa, Q. Gong, A. R. Abbas, Z. Modrusan, N. Ghilardi, F. J. de Sauvage, and W. Ouyang. 2008. Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat. Med. 14:282-289.
78. H17 cell differentiation by antagonizing RORγT function. Nature 453:236-240.