publication . Article . 2017

Stochasticity enables BCR-independent germinal center initiation and antibody affinity maturation.

Silver, Jared; Zuo, Teng; Chaudhary, Neha; Kumari, Rupa; Tong, Pei; Giguere, Sophie; Granato, Alessandra; Donthula, Rakesh; Devereaux, Colby; Wesemann, Duane R.;
Open Access
  • Published: 15 Dec 2017 Journal: Journal of Experimental Medicine, volume 215, pages 77-90 (issn: 0022-1007, eissn: 1540-9538, Copyright policy)
  • Publisher: Rockefeller University Press
Abstract
Whether Ig engagement by antigen is required to initiate somatic evolution and affinity maturation is not well defined. Silver and colleagues show that germinal center flexibility permits nonspecific B cells to achieve de novo antigen recognition and antibody affinity maturation.
Subjects
free text keywords: Immunology, Immunology and Allergy, Research Articles, Brief Definitive Report
Funded by
NIH| Decrypting IgE B Cell Immunobiology
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 1R01AI121394-01
  • Funding stream: NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES
34 references, page 1 of 3

Barnett B.E., Ciocca M.L., Goenka R., Barnett L.G., Wu J., Laufer T.M., Burkhardt J.K., Cancro M.P., and Reiner S.L.2012 Asymmetric B cell division in the germinal center reaction. Science.335:342–344. 10.1126/science.1213495 22174128 [OpenAIRE] [PubMed] [DOI]

Cumbers S.J., Williams G.T., Davies S.L., Grenfell R.L., Takeda S., Batista F.D., Sale J.E., and Neuberger M.S.2002 Generation and iterative affinity maturation of antibodies in vitro using hypermutating B-cell lines. Nat. Biotechnol.20:1129–1134. 10.1038/nbt752 12379869 [OpenAIRE] [PubMed] [DOI]

Curotto de Lafaille M.A., Muriglan S., Sunshine M.J., Lei Y., Kutchukhidze N., Furtado G.C., Wensky A.K., Olivares-Villagómez D., and Lafaille J.J.2001 Hyper immunoglobulin E response in mice with monoclonal populations of B and T lymphocytes. J. Exp. Med.194:1349–1359. 10.1084/jem.194.9.1349 11696599 [OpenAIRE] [PubMed] [DOI]

Dal Porto J.M., Haberman A.M., Kelsoe G., and Shlomchik M.J.2002 Very low affinity B cells form germinal centers, become memory B cells, and participate in secondary immune responses when higher affinity competition is reduced. J. Exp. Med.195:1215–1221. 10.1084/jem.20011550 11994427 [OpenAIRE] [PubMed] [DOI]

De Silva N.S., and Klein U.2015 Dynamics of B cells in germinal centres. Nat. Rev. Immunol.15:137–148. 10.1038/nri3804 25656706 [OpenAIRE] [PubMed] [DOI]

Di Niro R., Lee S.J., Vander Heiden J.A., Elsner R.A., Trivedi N., Bannock J.M., Gupta N.T., Kleinstein S.H., Vigneault F., Gilbert T.J., 2015 Salmonella infection drives promiscuous B cell activation followed by extrafollicular affinity maturation. Immunity.43:120–131. 10.1016/j.immuni.2015.06.013 26187411 [OpenAIRE] [PubMed] [DOI]

Dougan S.K., Ogata S., Hu C.C., Grotenbreg G.M., Guillen E., Jaenisch R., and Ploegh H.L.2012 IgG1+ ovalbumin-specific B-cell transnuclear mice show class switch recombination in rare allelically included B cells. Proc. Natl. Acad. Sci. USA.109:13739–13744. 10.1073/pnas.1210273109 22869725 [OpenAIRE] [PubMed] [DOI]

Dwyer D.F., Woodruff M.C., Carroll M.C., Austen K.F., and Gurish M.F.2014 B cells regulate CD4+ T cell responses to papain following B cell receptor-independent papain uptake. J. Immunol.193:529–539. 10.4049/jimmunol.1303247 24928991 [OpenAIRE] [PubMed] [DOI]

Hoot S., McGuire A.T., Cohen K.W., Strong R.K., Hangartner L., Klein F., Diskin R., Scheid J.F., Sather D.N., Burton D.R., and Stamatatos L.2013 Recombinant HIV envelope proteins fail to engage germlin e versions of anti-CD4bs bNAbs. PLoS Pathog.9:e1003106 10.1371/journal.ppat.1003106 23300456 [OpenAIRE] [PubMed] [DOI]

Hwang J.K., Alt F.W., and Yeap L.S.2015 Related mechanisms of antibody somatic hypermutation and class switch recombination. Microbiol. Spectr.3:MDNA3-0037-2014 10.1128/microbiolspec.MDNA3-0037-2014 [DOI]

Jellison E.R., Guay H.M., Szomolanyi-Tsuda E., and Welsh R.M.2007 Dynamics and magnitude of virus-induced polyclonal B cell activation mediated by BCR-independent presentation of viral antigen. Eur. J. Immunol.37:119–128. 10.1002/eji.200636516 17163452 [OpenAIRE] [PubMed] [DOI]

Jung D., Giallourakis C., Mostoslavsky R., and Alt F.W.2006 Mechanism and control of V(D)J recombination at the immunoglobulin heavy chain locus. Annu. Rev. Immunol.24:541–570. 10.1146/annurev.immunol.23.021704.115830 16551259 [OpenAIRE] [PubMed] [DOI]

Kakiuchi T., Chesnut R.W., and Grey H.M.1983 B cells as antigen-presenting cells: The requirement for B cell activation. J. Immunol.131:109–114.6190900 [PubMed]

Kuraoka M., Schmidt A.G., Nojima T., Feng F., Watanabe A., Kitamura D., Harrison S.C., Kepler T.B., and Kelsoe G.2016 Complex antigens drive permissive clonal selection in germinal centers. Immunity.44:542–552. 10.1016/j.immuni.2016.02.010 26948373 [OpenAIRE] [PubMed] [DOI]

Leung S., Smith D., Myc A., Morry J., and Baker J.R.Jr 2013 OT-II TCR transgenic mice fail to produce anti-ovalbumin antibodies upon vaccination. Cell. Immunol.282:79–84. 10.1016/j.cellimm.2012.12.006 23770715 [OpenAIRE] [PubMed] [DOI]

34 references, page 1 of 3
Abstract
Whether Ig engagement by antigen is required to initiate somatic evolution and affinity maturation is not well defined. Silver and colleagues show that germinal center flexibility permits nonspecific B cells to achieve de novo antigen recognition and antibody affinity maturation.
Subjects
free text keywords: Immunology, Immunology and Allergy, Research Articles, Brief Definitive Report
Funded by
NIH| Decrypting IgE B Cell Immunobiology
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 1R01AI121394-01
  • Funding stream: NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES
34 references, page 1 of 3

Barnett B.E., Ciocca M.L., Goenka R., Barnett L.G., Wu J., Laufer T.M., Burkhardt J.K., Cancro M.P., and Reiner S.L.2012 Asymmetric B cell division in the germinal center reaction. Science.335:342–344. 10.1126/science.1213495 22174128 [OpenAIRE] [PubMed] [DOI]

Cumbers S.J., Williams G.T., Davies S.L., Grenfell R.L., Takeda S., Batista F.D., Sale J.E., and Neuberger M.S.2002 Generation and iterative affinity maturation of antibodies in vitro using hypermutating B-cell lines. Nat. Biotechnol.20:1129–1134. 10.1038/nbt752 12379869 [OpenAIRE] [PubMed] [DOI]

Curotto de Lafaille M.A., Muriglan S., Sunshine M.J., Lei Y., Kutchukhidze N., Furtado G.C., Wensky A.K., Olivares-Villagómez D., and Lafaille J.J.2001 Hyper immunoglobulin E response in mice with monoclonal populations of B and T lymphocytes. J. Exp. Med.194:1349–1359. 10.1084/jem.194.9.1349 11696599 [OpenAIRE] [PubMed] [DOI]

Dal Porto J.M., Haberman A.M., Kelsoe G., and Shlomchik M.J.2002 Very low affinity B cells form germinal centers, become memory B cells, and participate in secondary immune responses when higher affinity competition is reduced. J. Exp. Med.195:1215–1221. 10.1084/jem.20011550 11994427 [OpenAIRE] [PubMed] [DOI]

De Silva N.S., and Klein U.2015 Dynamics of B cells in germinal centres. Nat. Rev. Immunol.15:137–148. 10.1038/nri3804 25656706 [OpenAIRE] [PubMed] [DOI]

Di Niro R., Lee S.J., Vander Heiden J.A., Elsner R.A., Trivedi N., Bannock J.M., Gupta N.T., Kleinstein S.H., Vigneault F., Gilbert T.J., 2015 Salmonella infection drives promiscuous B cell activation followed by extrafollicular affinity maturation. Immunity.43:120–131. 10.1016/j.immuni.2015.06.013 26187411 [OpenAIRE] [PubMed] [DOI]

Dougan S.K., Ogata S., Hu C.C., Grotenbreg G.M., Guillen E., Jaenisch R., and Ploegh H.L.2012 IgG1+ ovalbumin-specific B-cell transnuclear mice show class switch recombination in rare allelically included B cells. Proc. Natl. Acad. Sci. USA.109:13739–13744. 10.1073/pnas.1210273109 22869725 [OpenAIRE] [PubMed] [DOI]

Dwyer D.F., Woodruff M.C., Carroll M.C., Austen K.F., and Gurish M.F.2014 B cells regulate CD4+ T cell responses to papain following B cell receptor-independent papain uptake. J. Immunol.193:529–539. 10.4049/jimmunol.1303247 24928991 [OpenAIRE] [PubMed] [DOI]

Hoot S., McGuire A.T., Cohen K.W., Strong R.K., Hangartner L., Klein F., Diskin R., Scheid J.F., Sather D.N., Burton D.R., and Stamatatos L.2013 Recombinant HIV envelope proteins fail to engage germlin e versions of anti-CD4bs bNAbs. PLoS Pathog.9:e1003106 10.1371/journal.ppat.1003106 23300456 [OpenAIRE] [PubMed] [DOI]

Hwang J.K., Alt F.W., and Yeap L.S.2015 Related mechanisms of antibody somatic hypermutation and class switch recombination. Microbiol. Spectr.3:MDNA3-0037-2014 10.1128/microbiolspec.MDNA3-0037-2014 [DOI]

Jellison E.R., Guay H.M., Szomolanyi-Tsuda E., and Welsh R.M.2007 Dynamics and magnitude of virus-induced polyclonal B cell activation mediated by BCR-independent presentation of viral antigen. Eur. J. Immunol.37:119–128. 10.1002/eji.200636516 17163452 [OpenAIRE] [PubMed] [DOI]

Jung D., Giallourakis C., Mostoslavsky R., and Alt F.W.2006 Mechanism and control of V(D)J recombination at the immunoglobulin heavy chain locus. Annu. Rev. Immunol.24:541–570. 10.1146/annurev.immunol.23.021704.115830 16551259 [OpenAIRE] [PubMed] [DOI]

Kakiuchi T., Chesnut R.W., and Grey H.M.1983 B cells as antigen-presenting cells: The requirement for B cell activation. J. Immunol.131:109–114.6190900 [PubMed]

Kuraoka M., Schmidt A.G., Nojima T., Feng F., Watanabe A., Kitamura D., Harrison S.C., Kepler T.B., and Kelsoe G.2016 Complex antigens drive permissive clonal selection in germinal centers. Immunity.44:542–552. 10.1016/j.immuni.2016.02.010 26948373 [OpenAIRE] [PubMed] [DOI]

Leung S., Smith D., Myc A., Morry J., and Baker J.R.Jr 2013 OT-II TCR transgenic mice fail to produce anti-ovalbumin antibodies upon vaccination. Cell. Immunol.282:79–84. 10.1016/j.cellimm.2012.12.006 23770715 [OpenAIRE] [PubMed] [DOI]

34 references, page 1 of 3
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