Lactobacilli and Bifidobacteria enhance mucosal B cell responses and differentially modulate systemic antibody responses to an oral human rotavirus vaccine in a neonatal gnotobiotic pig disease model

Gut Microbes

Volumn 5, Issue 5, 2014, Pages 639-651

  Kandasamy, Sukumar ^a   Chattha, Kuldeep S ^a   Vlasova, Anastasia N ^a   Rajashekara, Gireesh ^a   Saif, Linda J ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

B cell responses; Human rotavirus; Neonatal diarrhea; Probiotics; Vaccine

Indexed keywords

APRIL PROTEIN; B CELL ACTIVATING FACTOR; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 6; INTERLEUKIN 8; PROBIOTIC AGENT; ROTAVIRUS VACCINE; TRANSFORMING GROWTH FACTOR BETA; CYTOKINE; VIRUS ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ANTIBODY SECRETING CELL; ANTIBODY TITER; ARTICLE; B LYMPHOCYTE; BACTERIAL COLONIZATION; BIFIDOBACTERIUM ANIMALIS; COLONY FORMING UNIT; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME LINKED IMMUNOSPOT ASSAY; FLOW CYTOMETRY; GNOTOBIOTICS; IMMUNE RESPONSE; LACTOBACILLUS RHAMNOSUS; MUCOSAL IMMUNITY; NONHUMAN; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ANIMAL; BIFIDOBACTERIUM; BLOOD; DISEASE MODEL; FECES; GASTROINTESTINAL TRACT; GERMFREE ANIMAL; GROWTH, DEVELOPMENT AND AGING; HUMAN; IMMUNOLOGY; ORAL DRUG ADMINISTRATION; PATHOLOGY; PIG; ROTAVIRUS INFECTIONS; SECRETION (PROCESS); VIROLOGY; VIRUS SHEDDING;

ANIMALIA; BACTERIA (MICROORGANISMS); BIFIDOBACTERIUM ANIMALIS; HUMAN ROTAVIRUS A; LACTOBACILLUS RHAMNOSUS; ROTAVIRUS; SUIDAE;

ADMINISTRATION, ORAL; ANIMALS; ANTIBODIES, VIRAL; B-LYMPHOCYTES; BIFIDOBACTERIUM; CYTOKINES; DISEASE MODELS, ANIMAL; FECES; GASTROINTESTINAL TRACT; GERM-FREE LIFE; HUMANS; IMMUNITY, MUCOSAL; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; LACTOBACILLUS RHAMNOSUS; ROTAVIRUS INFECTIONS; ROTAVIRUS VACCINES; SWINE; VIRUS SHEDDING;

EID: 84922021717     PISSN: 19490976     EISSN: 19490984     Source Type: Journal    
DOI: 10.4161/19490976.2014.969972     Document Type: Article

References (66)

1. Sjogren YM, Tomicic S, Lundberg A, Bottcher MF, Bjorksten B, Sverremark-Ekstrom E, Jenmalm MC. Influence of early gut microbiota on the maturation of childhood mucosal and systemic immune responses. Clin Exp Allergy: J Brit Soc Allergy Clin Immunol 2009; 39:1842-51; PMID:19735274; http://dx.doi. org/10.1111/j.1365-2222.2009.03326.x
2. Gaboriau-Routhiau V, Rakotobe S, Lecuyer E, Mulder I, Lan A, Bridonneau C, Rochet V, Pisi A, De Paepe M, Brandi G, et al. The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses. Immunity 2009; 31:677-89; PMID:19833089; http://dx. doi.org/10.1016/j.immuni.2009.08.020
3. Ivanov, II, Frutos Rde L, Manel N, Yoshinaga K, Rifkin DB, Sartor RB, Finlay BB, Littman DR. Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe 2008; 4:337-49; PMID:18854238; http://dx.doi.org/10.1016/j.chom.2008.09.009
4. Christensen HR, Frokiaer H, Pestka JJ. Lactobacilli differentially modulate expression of cytokines and maturation surface markers in murine dendritic cells. J Immunol 2002; 168:171-8; http://dx.doi.org/10.4049/ jimmunol.168.1.171
5. Ibnou-Zekri N, Blum S, Schiffrin EJ, von der Weid T. Divergent patterns of colonization and immune response elicited from two intestinal Lactobacillus strains that display similar properties in vitro. Infect Immun 2003; 71:428-36; PMID:12496193; http://dx. doi.org/10.1128/IAI.71.1.428-436.2003
6. Rudin A, Lundell AC. Infant B cell memory and gut bacterial colonization. Gut Microbes 2012; 3:474-5; PMID:22892691; http://dx.doi.org/10.4161/gmic. 21419
7. Lundell AC, Bjornsson V, Ljung A, Ceder M, Johansen S, Lindhagen G, Tornhage CJ, Adlerberth I, Wold AE, Rudin A. Infant B cell memory differentiation and early gut bacterial colonization. J Immunol 2012; 188:4315- 22; PMID:22490441; http://dx.doi.org/10.4049/ jimmunol.1103223
8. Macpherson AJ, Uhr T. Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria. Science 2004; 303:1662-5; PMID:15016999; http:// dx.doi.org/10.1126/science.1091334
9. Hapfelmeier S, Lawson MA, Slack E, Kirundi JK, Stoel M, Heikenwalder M, Cahenzli J, Velykoredko Y, Balmer ML, Endt K, et al. Reversible microbial colonization of germ-free mice reveals the dynamics of IgA immune responses. Science 2010; 328:1705-9; PMID:20576892; http://dx.doi.org/10.1126/science. 1188454
10. Parashar UD, Gibson CJ, Bresee JS, Glass RI. Rotavirus and severe childhood diarrhea. Emer Infect Dis 2006; 12:304-6; PMID:16494759; http://dx.doi.org/ 10.3201/eid1202.050006
11. Tate JE, Burton AH, Boschi-Pinto C, Steele AD, Duque J, Parashar UD, Network WH-cGRS. 2008 estimate of worldwide rotavirus-associated mortality in children younger than 5 years before the introduction of universal rotavirus vaccination programmes: a systematic review and meta-analysis. Lancet Infect Dis 2012; 12:136-41; PMID:22030330; http://dx.doi.org/ 10.1016/S1473-3099(11)70253-5
12. Vesikari T, Prymula R, Schuster V, Tejedor JC, Cohen R, Bouckenooghe A, Damaso S, Han HH. Efficacy and immunogenicity of live-attenuated human rotavirus vaccine in breast-fed and formulafed European infants. Pediatr Infect DisJ 2012; 31:509-13; PMID:22228235; http://dx.doi.org/ 10.1097/INF.0b013e3182489cac
13. Esposito DH, Tate JE, Kang G, Parashar UD. Projected impact and cost-effectiveness of a rotavirus vaccination program in India, 2008. Clin Infect Dis: An Off Pub Infect Dis Soc Am 2011; 52:171-7; PMID:21288839; http://dx.doi. org/10.1093/cid/ciq094
14. Madhi SA, Cunliffe NA, Steele D, Witte D, Kirsten M, Louw C, Ngwira B, Victor JC, Gillard PH, Cheuvart BB, et al. Effect of human rotavirus vaccine on severe diarrhea in African infants. New Eng J Med 2010; 362:289-98; PMID:20107214; http://dx.doi.org/ 10.1056/NEJMoa0904797
15. Franco MA, Greenberg HB. Role of B cells and cytotoxic T lymphocytes in clearance of and immunity to rotavirus infection in mice. J Virol 1995; 69:7800-6; PMID:7494291
16. Lagos R, Fasano A, Wasserman SS, Prado V, San Martin O, Abrego P, Losonsky GA, Alegria S, Levine MM. Effect of small bowel bacterial overgrowth on the immunogenicity of single-dose live oral cholera vaccine CVD 103-HgR. J Infect Dis 1999; 180:1709-12; PMID:10515838; http://dx.doi.org/10.1086/315051
17. Levine MM. Immunogenicity and efficacy of oral vaccines in developing countries: lessons from a live cholera vaccine. BMC Biol 2010; 8:129; PMID:20920375; http://dx.doi.org/10.1186/1741-7007-8-129
18. Hallander HO, Paniagua M, Espinoza F, Askelof P, Corrales E, Ringman M, Storsaeter J. Calibrated serological techniques demonstrate significant different serum response rates to an oral killed cholera vaccine between Swedish and Nicaraguan children. Vaccine 2002; 21:138-45; PMID:12443672; http://dx.doi.org/ 10.1016/S0264-410X(02)00348-1
19. Ferreira RB, Antunes LC, Finlay BB. Should the human microbiome be considered when developing vaccines? PLoS Pathogens 2010; 6:e1001190; PMID:21124987; http://dx.doi.org/10.1371/journal. ppat.1001190
20. Serazin AC, Shackelton LA, Wilson C, Bhan MK. Improving the performance of enteric vaccines in the developing world. Nat Immunol 2010; 11:769-73; PMID:20720580; http://dx.doi.org/10.1038/ni0910- 769
21. Turroni F, Peano C, Pass DA, Foroni E, Severgnini M, Claesson MJ, Kerr C, Hourihane J, Murray D, Fuligni F, et al. Diversity of bifidobacteria within the infant gut microbiota. PloS One 2012; 7:e36957; PMID:22606315; http://dx.doi.org/10.1371/journal. pone.0036957
22. Rubaltelli FF, Biadaioli R, Pecile P, Nicoletti P. Intestinal flora in breast- and bottle-fed infants. J Perinatal Med 1998; 26:186-91; PMID:9773376; http://dx.doi. org/10.1515/jpme.1998.26.3.186
23. Alvarez-Olmos MI, Oberhelman RA. Probiotic agents and infectious diseases: a modern perspective on a traditional therapy. Clin Infect Dis: An Off Pub Infect Dis Soc Am 2001; 32:1567-76; PMID:11340528; http:// dx.doi.org/10.1086/320518
24. Isolauri E, Joensuu J, Suomalainen H, Luomala M, Vesikari T. Improved immunogenicity of oral D x RRV reassortant rotavirus vaccine by Lactobacillus casei GG. Vaccine 1995; 13:310-2; PMID:7631519; http:// dx.doi.org/10.1016/0264-410X(95)93319-5
25. Holscher HD, Czerkies LA, Cekola P, Litov R, Benbow M, Santema S, Alexander DD, Perez V, Sun S, Saavedra JM, et al. Bifidobacterium lactis Bb12 enhances intestinal antibody response in formula-fed infants: a randomized, double-blind, controlled trial. JPEN J Parenter Enter Nutr 2012; 36:106S-17S; PMID:22237870; http://dx.doi.org/10.1177/014860- 7111430817
26. Fukushima Y, Kawata Y, Hara H, Terada A, Mitsuoka T. Effect of a probiotic formula on intestinal immunoglobulin A production in healthy children. Int J food Microbiol 1998; 42:39-44; PMID:9706796; http://dx. doi.org/10.1016/S0168-1605(98)00056-7
27. Gueimonde M, Sakata S, Kalliomaki M, Isolauri E, Benno Y, Salminen S. Effect of maternal consumption of lactobacillus GG on transfer and establishment of fecal bifidobacterial microbiota in neonates. J Pediatr Gastroenterol Nutr 2006; 42:166-70; PMID:16456409; http://dx.doi.org/10.1097/01.mpg. 0000189346.25172.fd
28. Saif LJ, Ward LA, Yuan L, Rosen BI, To TL. The gnotobiotic piglet as a model for studies of disease pathogenesis and immunity to human rotaviruses. Arch Virol Supplementum 1996; 12:153-61; PMID:9015112
29. Zhang W, Azevedo MS, Gonzalez AM, Saif LJ, Van Nguyen T, Wen K, Yousef AE, Yuan L. Influence of probiotic Lactobacilli colonization on neonatal B cell responses in a gnotobiotic pig model of human rotavirus infection and disease. Veter Immunol Immunopathol 2008; 122:175-81; PMID:18023882; http://dx. doi.org/10.1016/j.vetimm.2007.10.003
30. Vlasova AN, Chattha KS, Kandasamy S, Liu Z, Esseili M, Shao L, Rajashekara G, Saif LJ. Lactobacilli and Bifidobacteria promote immune homeostasis by modulating innate immune responses to human rotavirus in neonatal gnotobiotic pigs. PloS One 2013; 8:e76962; PMID:24098572; http://dx.doi.org/10.1371/journal. pone.0076962
31. Chattha KS, Vlasova AN, Kandasamy S, Rajashekara G, Saif LJ. Divergent immunomodulating effects of probiotics on T cell responses to oral attenuated human rotavirus vaccine and virulent human rotavirus infection in a neonatal gnotobiotic piglet disease model. J Immunol 2013; 191:2446- 56; PMID:23918983; http://dx.doi.org/10.4049/ jimmunol.1300678
32. Sinkora M, Stepanova K, Butler JE, Francis D, Santiago- Mateo K, Potockova H, Karova K, Sinkorova J. Ileal Peyer's patches are not necessary for systemic B cell development and maintenance and do not contribute significantly to the overall B cell pool in swine. J Immunol 2011; 187:5150-61; PMID:22013120; http://dx.doi.org/10.4049/jimmunol.1101879
33. Narvaez CF, Franco MA, Angel J, Morton JM, Greenberg HB. Rotavirus differentially infects and polyclonally stimulates human B cells depending on their differentiation state and tissue of origin. J Virol 2010; 84:4543-55; PMID:20164228; http://dx.doi.org/ 10.1128/JVI.02550-09
34. Deal EM, Lahl K, Narvaez CF, Butcher EC, Greenberg HB. Plasmacytoid dendritic cells promote rotavirusinduced human and murine B cell responses. J Clin Invest 2013; 123:2464-74; PMID:23635775; http:// dx.doi.org/10.1172/JCI60945
35. Macpherson AJ, Geuking MB, McCoy KD. Immune responses that adapt the intestinal mucosa to commensal intestinal bacteria. Immunology 2005; 115:153-62; PMID:15885120; http://dx.doi.org/10.1111/j.1365- 2567.2005.02159.x
36. Iliev ID, Kitazawa H, Shimosato T, Katoh S, Morita H, He F, Hosoda M, Saito T. Strong immunostimulation in murine immune cells by Lactobacillus rhamnosus GG DNA containing novel oligodeoxynucleotide pattern. Cell Microbiol 2005; 7:403-14; PMID:15679843; http://dx.doi.org/10.1111/j.1462- 5822.2004.00470.x
37. Menard O, Gafa V, Kapel N, Rodriguez B, Butel MJ, Waligora-Dupriet AJ. Characterization of immunostimulatory CpG-rich sequences from different Bifidobacterium species. App Environ Microbiol 2010; 76:2846- 55; PMID:20208019; http://dx.doi.org/10.1128/ AEM.01714-09
38. Shimosato T, Kitazawa H, Katoh S, Tomioka Y, Karima R, Ueha S, Kawai Y, Hishinuma T, Matsushima K, Saito T. Swine Toll-like receptor 9(1) recognizes CpG motifs of human cell stimulant. Biochimica Et Biophysica Acta 2003; 1627:56-61; PMID:12759192; http://dx.doi.org/10.1016/S0167- 4781(03)00048-4
39. Massacand JC, Kaiser P, Ernst B, Tardivel A, Burki K, Schneider P, Harris NL. Intestinal bacteria condition dendritic cells to promote IgA production. PloS One 2008; 3:e2588; PMID:18596964; http://dx.doi.org/ 10.1371/journal.pone.0002588
40. He B, Xu W, Santini PA, Polydorides AD, Chiu A, Estrella J, Shan M, Chadburn A, Villanacci V, Plebani A, et al. Intestinal bacteria trigger T cell-independent immunoglobulin A(2) class switching by inducing epithelial- cell secretion of the cytokine APRIL. Immunity 2007; 26:812-26; PMID:17570691; http://dx.doi.org/ 10.1016/j.immuni.2007.04.014
41. Winzler C, Rovere P, Rescigno M, Granucci F, Penna G, Adorini L, Zimmermann VS, Davoust J, Ricciardi- Castagnoli P. Maturation stages of mouse dendritic cells in growth factor-dependent long-term cultures. J Exp Med 1997; 185:317-28; PMID:9016880; http:// dx.doi.org/10.1084/jem.185.2.317
42. Tezuka H, Abe Y, Asano J, Sato T, Liu J, Iwata M, Ohteki T. Prominent role for plasmacytoid dendritic cells in mucosal T cell-independent IgA induction. Immunity 2011; 34:247-57; PMID:21333555; http:// dx.doi.org/10.1016/j.immuni.2011.02.002
43. Krieg AM, Wagner H. Causing a commotion in the blood: immunotherapy progresses from bacteria to bacterial DNA. Immunol Today 2000; 21:521-6; PMID:11071532; http://dx.doi.org/10.1016/S0167- 5699(00)01719-9
44. Takahashi N, Kitazawa H, Shimosato T, Iwabuchi N, Xiao JZ, Iwatsuki K, Kokubo S, Saito T. An immunostimulatory DNA sequence from a probiotic strain of Bifidobacterium longum inhibits IgE production in vitro. FEMS Immunol Med Microbiol 2006; 46:461- 9; PMID:16553822; http://dx.doi.org/10.1111/ j.1574-695X.2006.00064.x
45. Blaas SH, Stieber-Gunckel M, Falk W, Obermeier F, Rogler G. CpG-oligodeoxynucleotides stimulate immunoglobulin A secretion in intestinal mucosal B cells. Clin Exp Immunol 2009; 155:534-40; PMID:19220839; http://dx.doi.org/10.1111/j.1365- 2249.2008.03855.x
46. Cognasse F, Acquart S, Beniguel L, Sabido O, Chavarin P, Genin C, Garraud O. Differential production of immunoglobulin classes and subclasses by mucosaltype human B-lymphocytes exposed in vitro to CpG oligodeoxynucleotides. Clin Chem Lab Med: CCLM/ FESCC 2005; 43:22-31; PMID:15653438; http://dx. doi.org/10.1515/CCLM.2005.003
47. Defrance T, Vanbervliet B, Briere F, Durand I, Rousset F, Banchereau J. Interleukin 10 and transforming growth factor beta cooperate to induce anti-CD40-activated naive human B cells to secrete immunoglobulin A. J Exp Med 1992; 175:671-82; PMID:1371300; http://dx.doi.org/10.1084/jem. 175.3.671
48. Menard O, Butel MJ, Gaboriau-Routhiau V, Waligora- Dupriet AJ. Gnotobiotic mouse immune response induced by Bifidobacterium sp. strains isolated from infants. App Environ Microbiol 2008; 74:660-6; PMID:18083875; http://dx.doi.org/ 10.1128/AEM.01261-07
49. van Ginkel FW, Wahl SM, Kearney JF, Kweon MN, Fujihashi K, Burrows PD, Kiyono H, McGhee JR. Partial IgA-deficiency with increased Th2-type cytokines in TGF-beta 1 knockout mice. J Immunol 1999; 163:1951-7; PMID:10438931
50. Sato A, Hashiguchi M, Toda E, Iwasaki A, Hachimura S, Kaminogawa S. CD11b CPeyer's patch dendritic cells secrete IL-6 and induce IgA secretion from naive B cells. J Immunol 2003; 171:3684-90; PMID:14500666; http:// dx.doi.org/10.4049/jimmunol.171.7.3684
51. Franco MA, Greenberg HB. Immunity to rotavirus in T cell deficient mice. Virology 1997; 238:169-79; PMID:9400590; http://dx.doi.org/10.1006/viro.1997. 8843
52. Artis D. Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut. Nat Rev Immunol 2008; 8:411-20; PMID:18469830; http://dx.doi.org/10.1038/nri2316
53. Fagarasan S, Kawamoto S, Kanagawa O, Suzuki K. Adaptive immune regulation in the gut: T cell-dependent and T cell-independent IgA synthesis. Ann Rev Immunol 2010; 28:243-73; PMID:20192805; http://dx.doi.org/10.1146/ annurev-immunol-030409-101314
54. Litinskiy MB, Nardelli B, Hilbert DM, He B, Schaffer A, Casali P, Cerutti A. DCs induce CD40-independent immunoglobulin class switching through BLyS and APRIL. Nat Immunol 2002; 3:822-9; PMID:12154359; http://dx.doi.org/10.1038/ni829
55. Blutt SE, Warfield KL, Lewis DE, Conner ME. Early response to rotavirus infection involvesmassive B cell activation. J Immunol 2002; 168:5716-21; PMID:12023371; http://dx.doi.org/10.4049/jimmunol.168.11.5716
56. Zhang W, Azevedo MS, Wen K, Gonzalez A, Saif LJ, Li G, Yousef AE, Yuan L. Probiotic Lactobacillus acidophilus enhances the immunogenicity of an oral rotavirus vaccine in gnotobiotic pigs. Vaccine 2008; 26:3655-61; PMID:18524434; http://dx.doi.org/ 10.1016/j.vaccine.2008.04.070
57. Yasui H, Kiyoshima J, Ushijima H. Passive protection against rotavirus-induced diarrhea of mouse pups born to and nursed by dams fed Bifidobacterium breve YIT4064. J Infect Dis 1995; 172:403-9; PMID:7622883; http://dx. doi.org/10.1093/infdis/172.2.403
58. Chae CS, Kwon HK, Hwang JS, Kim JE, Im SH. Prophylactic effect of probiotics on the development of experimental autoimmune myasthenia gravis. PloS One 2012; 7:e52119; PMID:23284891; http://dx.doi. org/10.1371/journal.pone.0052119
59. Avery DT, Bryant VL, Ma CS, de Waal Malefyt R, Tangye SG. IL-21-induced isotype switching to IgG and IgA by human naive B cells is differentially regulated by IL-4. J Immunol 2008; 181:1767-79; PMID:18641314; http://dx.doi.org/10.4049/jimmunol. 181.3.1767
60. Yuan L, Ward LA, Rosen BI, To TL, Saif LJ. Systematic and intestinal antibody-secreting cell responses and correlates of protective immunity to human rotavirus in a gnotobiotic pig model of disease. J Virol 1996; 70:3075-83; PMID:8627786
61. Schultz M, Gottl C, Young RJ, Iwen P, Vanderhoof JA. Administration of oral probiotic bacteria to pregnant women causes temporary infantile colonization. J Pediat Gastroenterol Nutr 2004; 38:293-7; PMID:15076629; http://dx.doi.org/10.1097/00005176-200403000-00012
62. Ismail IH, Oppedisano F, Joseph SJ, Boyle RJ, Robins- Browne RM, Tang ML. Prenatal administration of Lactobacillus rhamnosus has no effect on the diversity of the early infant gut microbiota. Pediat Allergy Immunol: Off Pub Eur Soc Pediat Allergy Immunol 2012; 23:255-8; PMID:22136660; http://dx.doi.org/ 10.1111/j.1399-3038.2011.01239.x
63. Meyer RC, Bohl EH, Kohler EM. Procurement and maintenance of germ-free seine for microbiological investigations. Appl Microbiol 1964; 12:295-300; PMID:14199016
64. Parreno V, Hodgins DC, de Arriba L, Kang SY, Yuan L, Ward LA, To TL, Saif LJ. Serum and intestinal isotype antibody responses to Wa human rotavirus in gnotobiotic pigs are modulated by maternal antibodies. J Gen Virol 1999; 80 (Pt 6):1417-28; PMID:10374959
65. Azevedo MS, Yuan L, Pouly S, Gonzales AM, Jeong KI, Nguyen TV, Saif LJ. Cytokine responses in gnotobiotic pigs after infection with virulent or attenuated human rotavirus. J Virol 2006; 80:372- 82; PMID:16352562; http://dx.doi.org/10.1128/ JVI.80.1.372-382.2006
66. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001; 25:402-8; PMID:11846609; http://dx.doi.org/ 10.1006/meth.2001.1262