Enumeration of gut-homing β7-positive, pathogen-specific antibody-secreting cells in whole blood from enterotoxigenic Escherichia coliand Vibrio cholerae-infected patients, determined using an enzyme-linked immunosorbent spot assay technique

Clinical and Vaccine Immunology

Volumn 23, Issue 1, 2016, Pages 27-36

  Bhuiyan, Taufiqur Rahman ^a   Hoq, Mohammad Rubel ^a   Nishat, Naoshin Sharmin ^a   Al Mahbuba, Deena ^a   Rashu, Rasheduzzaman ^a   Islam, Kamrul ^a   Hossain, Lazina ^a   Dey, Ayan ^b   Harris, Jason B ^c   Ryan, Edward T ^c   Calderwood, Stephen B ^c   Svennerholm, Ann Mari ^d   Qadri, Firdausi ^a  

^a INTERNATIONAL CENTRE FOR DIARRHOEAL DISEASE RESEARCH   (Bangladesh)

^b International Vaccine Institute   (South Korea)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; BETA7 PROTEIN; CELL SURFACE MARKER; CHOLERA TOXIN B SUBUNIT; IMMUNOGLOBULIN; UNCLASSIFIED DRUG; BETA INTEGRIN; BETA7 INTEGRIN; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G;

ADULT; ANTIBODY SECRETING CELL; ARTICLE; BACTERIAL STRAIN; BANGLADESH; BLOOD SAMPLING; CELL HOMING; CELL ISOLATION; CHOLERA; CLINICAL ARTICLE; CONTROLLED STUDY; DIARRHEA; ENTEROTOXIGENIC ESCHERICHIA COLI; ENTEROTOXIGENIC ESCHERICHIA COLI INFECTION; ENZYME LINKED IMMUNOSPOT ASSAY; ESCHERICHIA COLI INFECTION; FEMALE; HUMAN; HUMAN CELL; IMMUNE RESPONSE; MALE; NONHUMAN; PRIORITY JOURNAL; VIBRIO CHOLERAE; BLOOD; IMMUNOGLOBULIN PRODUCING CELL; IMMUNOLOGY; INTESTINE; MICROBIOLOGY; MUCOSAL IMMUNITY; PROCEDURES; YOUNG ADULT;

ADULT; ANTIBODY-PRODUCING CELLS; CHOLERA; ENTEROTOXIGENIC ESCHERICHIA COLI; ENZYME-LINKED IMMUNOSPOT ASSAY; ESCHERICHIA COLI INFECTIONS; FEMALE; HUMANS; IMMUNITY, MUCOSAL; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; INTEGRIN BETA CHAINS; INTESTINES; MALE; VIBRIO CHOLERAE; YOUNG ADULT;

EID: 84954356980     PISSN: 15566811     EISSN: 1556679X     Source Type: Journal    
DOI: 10.1128/CVI.00526-15     Document Type: Article

References (48)

1. Qadri F, Svennerholm AM, Faruque AS, Sack RB. 2005. Enterotoxigenic Escherichia coli in developing countries: epidemiology, microbiology, clinical features, treatment, and prevention. Clin Microbiol Rev 18:465-483. http://dx.doi.org/10.1128/CMR.18.3.465-483.2005.
2. Kosek M, Bern C, Guerrant RL. 2003. The global burden of diarrhoeal disease, as estimated from studies published between 1992 and 2000. Bull World Health Organ 81:197-204.
3. Gaastra W, Svennerholm AM. 1996. Colonization factors of human enterotoxigenic Escherichia coli (ETEC). Trends Microbiol 4:444-452.http://dx.doi.org/10.1016/0966-842X(96)10068-8.
4. Levine MM. 1990. Modern vaccines. Enteric infections. Lancet 335: 958-961.
5. Svennerholm AM, Holmgren J. 1995. Oral vaccines against cholera and enterotoxigenic Escherichia coli diarrhea. Adv Exp Med Biol 371B:1623-1628.
6. Helander A, Hansson GC, Svennerholm AM. 1997. Binding of enterotoxigenic Escherichia coli to isolated enterocytes and intestinal mucus. Microb Pathog 23:335-346. http://dx.doi.org/10.1006/mpat.1997.0163.
7. Isidean SD, Riddle MS, Savarino SJ, Porter CK. 2011. A systematic review of ETEC epidemiology focusing on colonization factor and toxin expression. Vaccine 29:6167-6178. http://dx.doi.org/10.1016/j.vaccine.2011.06.084.
8. Plotkin SA. 2008. Vaccines: correlates of vaccine-induced immunity. Clin Infect Dis 47:401-409. http://dx.doi.org/10.1086/589862.
9. Quiding M, Nordstrom I, Kilander A, Andersson G, Hanson LA, Holmgren J, Czerkinsky C. 1991. Intestinal immune responses in humans. Oral cholera vaccination induces strong intestinal antibody responses and interferon-gamma production and evokes local immunological memory. J Clin Invest 88:143-148.
10. Kozlowski PA, Cu-Uvin S, Neutra MR, Flanigan TP. 1997. Comparison of the oral, rectal, and vaginal immunization routes for induction of antibodies in rectal and genital tract secretions of women. Infect Immun 65: 1387-1394.
11. Lycke N, Lindholm L, Holmgren J. 1985. Cholera antibody production in vitro by peripheral blood lymphocytes following oral immunization of humans and mice. Clin Exp Immunol 62:39-47.
12. Kantele A, Kantele JM, Savilahti E, Westerholm M, Arvilommi H, Lazarovits A, Butcher EC, Makela PH. 1997. Homing potentials of circulating lymphocytes in humans depend on the site of activation: oral, but not parenteral, typhoid vaccination induces circulating antibodysecreting cells that all bear homing receptors directing them to the gut. J Immunol 158:574-579.
13. Saletti G, Cuburu N, Yang JS, Dey A, Czerkinsky C. 2013. Enzymelinked immunospot assays for direct ex vivo measurement of vaccineinduced human humoral immune responses in blood. Nat Protoc 8:1073-1087. http://dx.doi.org/10.1038/nprot.2013.058.
14. Saxon A, Stevens RH. 1979. Stimulation and regulation of human IgE production in vitro using peripheral blood lymphocytes. Clin Immunol Immunopathol 14:474-488. http://dx.doi.org/10.1016/0090-1229(79)90100-4.
15. Yarchoan R, Murphy BR, Strober W, Schneider HS, Nelson DL. 1981. Specific anti-influenza virus antibody production in vitro by human peripheral blood mononuclear cells. J Immunol 127:2588-2594.
16. Qadri F, Ahmed F, Karim MM, Wenneras C, Begum YA, Abdus Salam M, Albert MJ, McGhee JR. 1999. Lipopolysaccharide-and cholera toxinspecific subclass distribution of B-cell responses in cholera. Clin Diagn Lab Immunol 6:812-818.
17. Alam MM, Aktar A, Afrin S, Rahman MA, Aktar S, Uddin T, Al Mahbuba D, Chowdhury F, Khan AI, Bhuiyan TR, Begum YA, Ryan ET, Calderwood SB, Svennerholm AM, Qadri F. 2014. Antigen-specific memory B-cell responses to enterotoxigenic Escherichia coli infection in Bangladeshi adults. PLoS Negl Trop Dis 8:e2822. http://dx.doi.org/10.1371/journal.pntd.0002822.
18. Qadri F, Das SK, Faruque AS, Fuchs GJ, Albert MJ, Sack RB, Svennerholm AM. 2000. Prevalence of toxin types and colonization factors in enterotoxigenic Escherichia coli isolated during a 2-year period from diarrheal patients in Bangladesh. J Clin Microbiol 38:27-31.
19. Rodas C, Iniguez V, Qadri F, Wiklund G, Svennerholm AM, Sjoling A. 2009. Development of multiplex PCR assays for detection of enterotoxigenic Escherichia coli colonization factors and toxins. J Clin Microbiol 47:1218-1220. http://dx.doi.org/10.1128/JCM.00316-09.
20. Leung DT, Bhuiyan TR, Nishat NS, Hoq MR, Aktar A, Rahman MA, Uddin T, Khan AI, Chowdhury F, Charles RC, Harris JB, Calderwood SB, Qadri F, Ryan ET. 2014. Circulating mucosal associated invariant T cells are activated in Vibrio cholerae O1 infection and associated with lipopolysaccharide antibody responses. PLoS Negl Trop Dis 8:e3076. http://dx.doi.org/10.1371/journal.pntd.0003076.
21. Tobias J, Svennerholm AM. 2012. Strategies to overexpress enterotoxigenic Escherichia coli (ETEC) colonization factors for the construction of oral whole-cell inactivated ETEC vaccine candidates. Appl Microbiol Biotechnol 93:2291-2300. http://dx.doi.org/10.1007/s00253-012-3930-6.
22. Salmond RJ, Luross JA, Williams NA. 2002. Immune modulation by the cholera-like enterotoxins. Expert Rev Mol Med 4:1-16.
23. Qadri F, Saha A, Ahmed T, Al Tarique A, Begum YA, Svennerholm AM. 2007. Disease burden due to enterotoxigenic Escherichia coli in the first 2 years of life in an urban community in Bangladesh. Infect Immun 75: 3961-3968. http://dx.doi.org/10.1128/IAI.00459-07.
24. Svennerholm AM, Lundgren A. 2012. Recent progress toward an enterotoxigenic Escherichia coli vaccine. Expert Rev Vaccines 11:495-507. http://dx.doi.org/10.1586/erv.12.12.
25. Manz RA, Hauser AE, Hiepe F, Radbruch A. 2005. Maintenance of serum antibody levels. Annu Rev Immunol 23:367-386. http://dx.doi.org/10.1146/annurev.immunol.23.021704.115723.
26. Leach S, Lundgren A, Svennerholm AM. 2013. Different kinetics of circulating antibody-secreting cell responses after primary and booster oral immunizations: a tool for assessing immunological memory. Vaccine 31:3035-3038. http://dx.doi.org/10.1016/j.vaccine.2013.04.066.
27. Quiding-Järbrink M, Nordstrom I, Granstrom G, Kilander A, Jertborn M, Butcher EC, Lazarovits AI, Holmgren J, Czerkinsky C. 1997. Differential expression of tissue-specific adhesion molecules on human circulating antibody-forming cells after systemic, enteric, and nasal immunizations. A molecular basis for the compartmentalization of effector B cell responses. J Clin Invest 99:1281-1286.
28. Cyster JG. 2003. Homing of antibody secreting cells. Immunol Rev 194: 48-60. http://dx.doi.org/10.1034/j.1600-065X.2003.00041.x.
29. Qadri F, Wenneras C, Albert MJ, Hossain J, Mannoor K, Begum YA, Mohi G, Salam MA, Sack RB, Svennerholm AM. 1997. Comparison of immune responses in patients infected with Vibrio cholerae O139 and O1. Infect Immun 65:3571-3576.
30. Uddin T, Harris JB, Bhuiyan TR, Shirin T, Uddin MI, Khan AI, Chowdhury F, LaRocque RC, Alam NH, Ryan ET, Calderwood SB, Qadri F. 2011. Mucosal immunologic responses in cholera patients in Bangladesh. Clin Vaccine Immunol 18:506-512. http://dx.doi.org/10.1128/CVI.00481-10.
31. Qadri F, Makela PH, Holmgren J, Albert MJ, Mannoor K, Kantele A, Saha D, Salam MA, Kantele JM. 1998. Enteric infections in an endemic area induce a circulating antibody-secreting cell response with homing potentials to both mucosal and systemic tissues. J Infect Dis 177:1594-1599. http://dx.doi.org/10.1086/515306.
32. Alam MM, Riyadh MA, Fatema K, Rahman MA, Akhtar N, Ahmed T, Chowdhury MI, Chowdhury F, Calderwood SB, Harris JB, Ryan ET, Qadri F. 2011. Antigen-specific memory B-cell responses in Bangladeshi adults after one-or two-dose oral killed cholera vaccination and comparison with responses in patients with naturally acquired cholera. Clin Vaccine Immunol 18:844-850. http://dx.doi.org/10.1128/CVI.00562-10.
33. Svennerholm AM, Holmgren J. 1976. Synergistic protective effect in rabbits of immunization with Vibrio cholerae lipopolysaccharide and toxin/toxoid. Infect Immun 13:735-740.
34. Svennerholm AM, Holmgren J, Black R, Levine M, Merson M. 1983. Serologic differentiation between antitoxin responses to infection with Vibrio cholerae and enterotoxin-producing Escherichia coli. J Infect Dis 147:514-522. http://dx.doi.org/10.1093/infdis/147.3.514.
35. Shamsuzzaman S, Ahmed T, Mannoor K, Begum YA, Bardhan PK, Sack RB, Sack DA, Svennerholm AM, Holmgren J, Qadri F. 2009. Robust gut associated vaccine-specific antibody-secreting cell responses are detected at the mucosal surface of Bangladeshi subjects after immunization with an oral killed bivalent V. Cholerae O1/O139 whole cell cholera vaccine: comparison with other mucosal and systemic responses. Vaccine 27:1386-1392. http://dx.doi.org/10.1016/j.vaccine.2008.12.041.
36. Johnson RA, Uddin T, Aktar A, Mohasin M, Alam MM, Chowdhury F, Harris JB, LaRocque RC, Bufano MK, Yu Y, Wu-Freeman Y, Leung DT, Sarracino D, Krastins B, Charles RC, Xu P, Kovac P, Calderwood SB, Qadri F, Ryan ET. 2012. Comparison of immune responses to the O-specific polysaccharide and lipopolysaccharide of Vibrio cholerae O1 in Bangladeshi adult patients with cholera. Clin Vaccine Immunol 19:1712-1721. http://dx.doi.org/10.1128/CVI.00321-12.
37. Losonsky GA, Yunyongying J, Lim V, Reymann M, Lim YL, Wasserman SS, Levine MM. 1996. Factors influencing secondary vibriocidal immune responses: relevance for understanding immunity to cholera. Infect Immun 64:10-15.
38. Harris JB, LaRocque RC, Chowdhury F, Khan AI, Logvinenko T, Faruque AS, Ryan ET, Qadri F, Calderwood SB. 2008. Susceptibility to Vibrio cholerae infection in a cohort of household contacts of patients with cholera in Bangladesh. PLoS Negl Trop Dis 2:e221. http://dx.doi.org/10.1371/journal.pntd.0000221.
39. Rahman A, Rashu R, Bhuiyan TR, Chowdhury F, Khan AI, Islam K, LaRocque RC, Ryan ET, Wrammert J, Calderwood SB, Qadri F, Harris JB. 2013. Antibody-secreting cell responses after Vibrio cholerae O1 infection and oral cholera vaccination in adults in Bangladesh. Clin Vaccine Immunol 20:1592-1598. http://dx.doi.org/10.1128/CVI.00347-13.
40. Qadri F, Ahmed T, Ahmed F, Bradley Sack R, Sack DA, Svennerholm AM. 2003. Safety and immunogenicity of an oral, inactivated enterotoxigenic Escherichia coli plus cholera toxin B subunit vaccine in Bangladeshi children 18-36 months of age. Vaccine 21:2394-2403. http://dx.doi.org/10.1016/S0264-410X(03)00077-X.
41. Wennerås C, Svennerholm AM, Ahren C, Czerkinsky C. 1992. Antibody-secreting cells in human peripheral blood after oral immunization with an inactivated enterotoxigenic Escherichia coli vaccine. Infect Immun 60:2605-2611.
42. Qadri F, Ahmed F, Ahmed T, Svennerholm AM. 2006. Homologous and cross-reactive immune responses to enterotoxigenic Escherichia coli colonization factors in Bangladeshi children. Infect Immun 74:4512-4518. http://dx.doi.org/10.1128/IAI.00474-06.
43. Rudin A, Wiklund G, Wenneras C, Qadri F. 1997. Infection with colonization factor antigen I-expressing enterotoxigenic Escherichia coli boosts antibody responses against heterologous colonization factors in primed subjects. Epidemiol Infect 119:391-393. http://dx.doi.org/10.1017/S0950268897008200.
44. Rudin A, Svennerholm AM. 1994. Colonization factor antigens (CFAs) of enterotoxigenic Escherichia coli can prime and boost immune responses against heterologous CFAs. Microb Pathog 16:131-139. http://dx.doi.org/10.1006/mpat.1994.1014.
45. Qadri F, Ahmed T, Ahmed F, Bhuiyan MS, Mostofa MG, Cassels FJ, Helander A, Svennerholm AM. 2007. Mucosal and systemic immune responses in patients with diarrhea due to CS6-expressing enterotoxigenic Escherichia coli. Infect Immun 75:2269-2274. http://dx.doi.org/10.1128/IAI.01856-06.
46. Holmgren J, Bourgeois L, Carlin N, Clements J, Gustafsson B, Lundgren A, Nygren E, Tobias J, Walker R, Svennerholm AM. 2013. Development and preclinical evaluation of safety and immunogenicity of an oral ETEC vaccine containing inactivated E. Coli bacteria overexpressing colonization factors CFA/I, CS3, CS5 and CS6 combined with a hybrid LT/CT B subunit antigen, administered alone and together with dmLT adjuvant. Vaccine 31:2457-2464. http://dx.doi.org/10.1016/j.vaccine.2013.03.027.
47. Leung DT, Chowdhury F, Calderwood SB, Qadri F, Ryan ET. 2012. Immune responses to cholera in children. Expert Rev Anti Infect Ther 10:435-444. http://dx.doi.org/10.1586/eri.12.23.
48. Czerkinsky C, Andersson G, Ekre HP, Nilsson LA, Klareskog L, Ouchterlony O. 1988. Reverse ELISPOT assay for clonal analysis of cytokine production. I. Enumeration of gamma-interferon-secreting cells. J Immunol Methods 110:29-36.