Development of immunoglobulin M memory to both a T-cell-independent and a T-cell-dependent antigen following infection with Vibrio cholerae O1 in Bangladesh - PubMed
doi: 10.1128/IAI.00868-09. Epub 2009 Oct 26.
Abdullah A Tarique, Azim Hossain, Mohammad Murshid Alam, Mohammad Arifuzzaman, Nayeema Akhtar, Fahima Chowdhury, Ashraful I Khan, Regina C Larocque, Jason B Harris, Edward T Ryan, Firdausi Qadri, Stephen B Calderwood
Affiliations
- PMID: 19858296
- PMCID: PMC2798198
- DOI: 10.1128/IAI.00868-09
Development of immunoglobulin M memory to both a T-cell-independent and a T-cell-dependent antigen following infection with Vibrio cholerae O1 in Bangladesh
Emily A Kendall et al. Infect Immun. 2010 Jan.
Abstract
Vibrio cholerae O1 can cause severe watery diarrhea that can be life-threatening without treatment. Infection results in long-lasting protection against subsequent disease. Development of memory B cells of the immunoglobulin G (IgG) and IgA isotypes to V. cholerae O1 antigens, including serotype-specific lipopolysaccharide (LPS) and the B subunit of cholera toxin (CTB), after cholera infection has been demonstrated. Memory B cells of the IgM isotype may play a role in long-term protection, particularly against T-cell-independent antigens, but IgM memory has not been studied in V. cholerae O1 infection. Therefore, we assayed acute- and convalescent-phase blood samples from cholera patients for the presence of memory B cells that produce cholera antigen-specific IgM antibody upon polyclonal stimulation in in vitro culture. We also examined the development of serological and antibody-secreting cell responses following infection. Subjects developed significant IgM memory responses by day 30 after infection, both to the T-cell-independent antigen LPS and to the T-cell-dependent antigen CTB. No significant corresponding elevations in plasma IgM antibodies or circulating IgM antibody-secreting cells to CTB were detected. In 17 subjects followed to day 90 after infection, significant persistence of elevated IgM memory responses was not observed. The IgM memory response to CTB was negatively correlated with the IgG plasma antibody response to CTB, and there was a trend toward negative correlation between the IgM memory and IgA plasma antibody responses to LPS. We did not observe an association between the IgM memory response to LPS and the vibriocidal titer.
Figures
![FIG. 1.](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/2972/2798198/bdef9a706f85/zii0011083610001.gif)
IgA, IgG, and IgM serological responses to CTB and LPS antigens in cholera patients at near baseline (day 2 after onset of illness), acute stage (day 7), and convalescence (day 30). *, Significant elevation (P < 0.002) in comparison to day 2.
![FIG. 2.](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/2972/2798198/56139ed0ec6e/zii0011083610002.gif)
Antigen-specific circulating ASCs of IgA, IgG, and IgM isotypes in cholera patients 2, 7, and 30 days after onset of illness. *, P < 0.05 in comparison to day 2; n = 15, six of whom were included in other analyses.
![FIG. 3.](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/2972/2798198/744b0842c594/zii0011083610003.gif)
Antigen-specific B-cell memory responses of IgA, IgG, and IgM isotypes in cholera patients 2, 30, and 90 days after onset of illness, determined from ELISA measurements of lymphocyte culture supernatant specimens. *, P < 0.05 in comparison to day 2.
Similar articles
-
Aktar A, Rahman MA, Afrin S, Akter A, Uddin T, Yasmin T, Sami MIN, Dash P, Jahan SR, Chowdhury F, Khan AI, LaRocque RC, Charles RC, Bhuiyan TR, Mandlik A, Kelly M, Kováč P, Xu P, Calderwood SB, Harris JB, Qadri F, Ryan ET. Aktar A, et al. PLoS Negl Trop Dis. 2018 Apr 23;12(4):e0006399. doi: 10.1371/journal.pntd.0006399. eCollection 2018 Apr. PLoS Negl Trop Dis. 2018. PMID: 29684006 Free PMC article.
-
Antigen-specific memory B-cell responses to Vibrio cholerae O1 infection in Bangladesh.
Harris AM, Bhuiyan MS, Chowdhury F, Khan AI, Hossain A, Kendall EA, Rahman A, LaRocque RC, Wrammert J, Ryan ET, Qadri F, Calderwood SB, Harris JB. Harris AM, et al. Infect Immun. 2009 Sep;77(9):3850-6. doi: 10.1128/IAI.00369-09. Epub 2009 Jun 15. Infect Immun. 2009. PMID: 19528207 Free PMC article.
-
Aktar A, Rahman MA, Afrin S, Faruk MO, Uddin T, Akter A, Sami MIN, Yasmin T, Chowdhury F, Khan AI, Leung DT, LaRocque RC, Charles RC, Bhuiyan TR, Mandlik A, Kelly M, Kováč P, Xu P, Calderwood SB, Harris JB, Qadri F, Ryan ET. Aktar A, et al. Clin Vaccine Immunol. 2016 May 6;23(5):427-435. doi: 10.1128/CVI.00647-15. Print 2016 May. Clin Vaccine Immunol. 2016. PMID: 27009211 Free PMC article.
-
Muzembo BA, Kitahara K, Mitra D, Ohno A, Miyoshi SI. Muzembo BA, et al. Int J Environ Res Public Health. 2022 Jun 10;19(12):7141. doi: 10.3390/ijerph19127141. Int J Environ Res Public Health. 2022. PMID: 35742404 Free PMC article. Review.
-
Immunoglobulin M in Health and Diseases: How Far Have We Come and What Next?
Jones K, Savulescu AF, Brombacher F, Hadebe S. Jones K, et al. Front Immunol. 2020 Oct 30;11:595535. doi: 10.3389/fimmu.2020.595535. eCollection 2020. Front Immunol. 2020. PMID: 33193450 Free PMC article. Review.
Cited by
-
Uddin T, Aktar A, Xu P, Johnson RA, Rahman MA, Leung DT, Afrin S, Akter A, Alam MM, Rahman A, Chowdhury F, Khan AI, Bhuiyan TR, Bufano MK, Rashu R, Yu Y, Wu-Freeman Y, Harris JB, LaRocque RC, Charles RC, Kováč P, Calderwood SB, Ryan ET, Qadri F. Uddin T, et al. Am J Trop Med Hyg. 2014 May;90(5):873-81. doi: 10.4269/ajtmh.13-0498. Epub 2014 Mar 31. Am J Trop Med Hyg. 2014. PMID: 24686738 Free PMC article.
-
Hossain M, Islam K, Kelly M, Mayo Smith LM, Charles RC, Weil AA, Bhuiyan TR, Kováč P, Xu P, Calderwood SB, Simon JK, Chen WH, Lock M, Lyon CE, Kirkpatrick BD, Cohen M, Levine MM, Gurwith M, Leung DT, Azman AS, Harris JB, Qadri F, Ryan ET. Hossain M, et al. PLoS Negl Trop Dis. 2019 Nov 19;13(11):e0007874. doi: 10.1371/journal.pntd.0007874. eCollection 2019 Nov. PLoS Negl Trop Dis. 2019. PMID: 31743334 Free PMC article.
-
Falkard B, Charles RC, Matias WR, Mayo-Smith LM, Jerome JG, Offord ES, Xu P, Kováč P, Ryan ET, Qadri F, Franke MF, Ivers LC, Harris JB. Falkard B, et al. PLoS Negl Trop Dis. 2019 Jan 31;13(1):e0007057. doi: 10.1371/journal.pntd.0007057. eCollection 2019 Jan. PLoS Negl Trop Dis. 2019. PMID: 30703094 Free PMC article.
-
Alam MM, Riyadh MA, Fatema K, Rahman MA, Akhtar N, Ahmed T, Chowdhury MI, Chowdhury F, Calderwood SB, Harris JB, Ryan ET, Qadri F. Alam MM, et al. Clin Vaccine Immunol. 2011 May;18(5):844-50. doi: 10.1128/CVI.00562-10. Epub 2011 Feb 23. Clin Vaccine Immunol. 2011. PMID: 21346055 Free PMC article.
-
Immune responses to cholera in children.
Leung DT, Chowdhury F, Calderwood SB, Qadri F, Ryan ET. Leung DT, et al. Expert Rev Anti Infect Ther. 2012 Apr;10(4):435-44. doi: 10.1586/eri.12.23. Expert Rev Anti Infect Ther. 2012. PMID: 22512753 Free PMC article. Review.
References
-
- Ahmed, T., A. M. Svennerholm, A. Al Tarique, G. N. Sultana, and F. Qadri. 2009. Enhanced immunogenicity of an oral inactivated cholera vaccine in infants in Bangladesh obtained by zinc supplementation and by temporary withholding breast-feeding. Vaccine 27:1433-1439. - PubMed
-
- Bjornson, A. B., and P. A. Detmers. 1995. The pentameric structure of IgM is necessary to enhance opsonization of Bacteroides thetaiotaomicron and Bacteroides fragilis via the alternative complement pathway. Microb. Pathog. 19:117-128. - PubMed
-
- Capolunghi, F., S. Cascioli, E. Giorda, M. M. Rosado, A. Plebani, C. Auriti, G. Seganti, R. Zuntini, S. Ferrari, M. Cagliuso, I. Quinti, and R. Carsetti. 2008. CpG drives human transitional B cells to terminal differentiation and production of natural antibodies. J. Immunol. 180:800-808. - PubMed
-
- Clements, M. L., M. M. Levine, C. R. Young, R. E. Black, Y. L. Lim, R. M. Robins-Browne, and J. P. Craig. 1982. Magnitude, kinetics, and duration of vibriocidal antibody responses in North Americans after ingestion of Vibrio cholerae. J. Infect. Dis. 145:465-473. - PubMed
-
- Crotty, S., R. D. Aubert, J. Glidewell, and R. Ahmed. 2004. Tracking human antigen-specific memory B cells: a sensitive and generalized ELISPOT system. J. Immunol. Methods 286:111-122. - PubMed
Publication types
MeSH terms
Substances
Grants and funding
LinkOut - more resources
Full Text Sources
Medical
Miscellaneous