Molecular characterization of the early B cell response to pulmonary Cryptococcus neoformans infection

Journal of Immunology

Volumn 189, Issue 12, 2012, Pages 5820-5830

  Rohatgi, Soma ^a   Pirofski, Liise Anne ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN M;

ANIMAL CELL; ANTIBODY RESPONSE; ARTICLE; B LYMPHOCYTE; BINDING AFFINITY; BINDING SITE; CELL FUNCTION; CELL SPECIFICITY; CONTROLLED STUDY; CRYPTOCOCCUS NEOFORMANS; DISEASE ASSOCIATION; DNA SEQUENCE; ENZYME LINKED IMMUNOSPOT ASSAY; FLOW CYTOMETRY; FUNGAL GENE; FUNGAL STRAIN; FUNGUS IDENTIFICATION; GENE IDENTIFICATION; IMMUNE RESPONSE; IMMUNOGLOBULIN V REGION H CHAIN 11 GENE; IMMUNOGLOBULIN V REGION H CHAIN 12 GENE; IMMUNOGLOBULIN V REGION H CHAIN GENE; INNATE IMMUNITY; LUNG ALVEOLUS MACROPHAGE; LUNG CAVITY; LYMPHOCYTE COUNT; LYMPHOCYTE SUBPOPULATION; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PERITONEAL CAVITY; PHAGOCYTOSIS; PRIORITY JOURNAL; PULMONARY CRYPTOCOCCOSIS; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; SPECIES DIVERSITY;

ANIMALS; B-LYMPHOCYTE SUBSETS; CRYPTOCOCCOSIS; CRYPTOCOCCUS NEOFORMANS; IMMUNOGLOBULIN HEAVY CHAINS; IMMUNOGLOBULIN VARIABLE REGION; LUNG DISEASES, FUNGAL; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; PERITONEAL CAVITY;

EID: 84871158166     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1201514     Document Type: Article

References (92)

1. + T cells in the protective inflammatory response to a pulmonary cryptococcal infection. J. Leukoc. Biol. 55: 35-42.
2. + T cells. J. Exp. Med. 173: 793-800.
3. Dromer, F., J. Salamero, A. Contrepois, C. Carbon, and P. Yeni. 1987. Production, characterization, and antibody specificity of a mouse monoclonal antibody reactive with Cryptococcus neoformans capsular polysaccharide. Infect. Immun. 55: 742-748. (Pubitemid 17021970)
4. Eckert, T. F., and T. R. Kozel. 1987. Production and characterization of monoclonal antibodies specific for Cryptococcus neoformans capsular polysaccharide. Infect. Immun. 55: 1895-1899.
5. Mukherjee, S., S. C. Lee, and A. Casadevall. 1995. Antibodies to Cryptococcus neoformans glucuronoxylomannan enhance antifungal activity of murine macrophages. Infect. Immun. 63: 573-579.
6. Casadevall, A., W. Cleare, M. Feldmesser, A. Glatman-Freedman, D. L. Goldman, T. R. Kozel, N. Lendvai, J. Mukherjee, L. A. Pirofski, J. Rivera, et al. 1998. Characterization of a murine monoclonal antibody to Cryptococcus neoformans polysaccharide that is a candidate for human therapeutic studies. Antimicrob. Agents Chemother. 42: 1437-1446. (Pubitemid 28257647)
7. Fleuridor, R., A. Lees, and L. Pirofski. 2001. A cryptococcal capsular polysaccharide mimotope prolongs the survival of mice with Cryptococcus neoformans infection. J. Immunol. 166: 1087-1096. (Pubitemid 32060267)
8. Dromer, F., J. Charreire, A. Contrepois, C. Carbon, and P. Yeni. 1987. Protection of mice against experimental cryptococcosis by anti-Cryptococcus neoformans monoclonal antibody. Infect. Immun. 55: 749-752. (Pubitemid 17021971)
9. Schlageter, A. M., and T. R. Kozel. 1990. Opsonization of Cryptococcus neoformans by a family of isotype-switch variant antibodies specific for the capsular polysaccharide. Infect. Immun. 58: 1914-1918. (Pubitemid 20176391)
10. Shapiro, S., D. O. Beenhouwer, M. Feldmesser, C. Taborda, M. C. Carroll, A. Casadevall, and M. D. Scharff. 2002. Immunoglobulin G monoclonal antibodies to Cryptococcus neoformans protect mice deficient in complement component C3. Infect. Immun. 70: 2598-2604. (Pubitemid 34408405)
11. Miller, M. F., T. G. Mitchell, W. J. Storkus, and J. R. Dawson. 1990. Human natural killer cells do not inhibit growth of Cryptococcus neoformans in the absence of antibody. Infect. Immun. 58: 639-645. (Pubitemid 20072625)
12. Nabavi, N., and J. W. Murphy. 1986. Antibody-dependent natural killer cellmediated growth inhibition of Cryptococcus neoformans. Infect. Immun. 51: 556-562. (Pubitemid 16212134)
13. Torosantucci, A., P. Chiani, C. Bromuro, F. De Bernardis, A. S. Palma, Y. Liu, G. Mignogna, B. Maras, M. Colone, A. Stringaro, et al. 2009. Protection by anti-β-glucan antibodies is associated with restricted β-1,3 glucan binding specificity and inhibition of fungal growth and adherence. PLoS ONE 4: e5392.
14. Torosantucci, A., C. Bromuro, P. Chiani, F. De Bernardis, F. Berti, C. Galli, F. Norelli, C. Bellucci, L. Polonelli, P. Costantino, et al. 2005. A novel glycoconjugate vaccine against fungal pathogens. J. Exp. Med. 202: 597-606. (Pubitemid 41258184)
15. Mukherjee, J., A. Casadevall, and M. D. Scharff. 1993. Molecular characterization of the humoral responses to Cryptococcus neoformans infection and glucuronoxylomannan-tetanus toxoid conjugate immunization. J. Exp. Med. 177: 1105-1116. (Pubitemid 23097399)
16. Casadevall, A., M. DeShaw, M. Fan, F. Dromer, T. R. Kozel, and L. A. Pirofski. 1994. Molecular and idiotypic analysis of antibodies to Cryptococcus neoformans glucuronoxylomannan. Infect. Immun. 62: 3864-3872. (Pubitemid 24264331)
17. Maitta, R. W., K. Datta, Q. Chang, R. X. Luo, B. Witover, K. Subramaniam, and L. A. Pirofski. 2004. Protective and nonprotective human immunoglobulin M monoclonal antibodies to Cryptococcus neoformans glucuronoxylomannan manifest different specificities and gene use profiles. Infect. Immun. 72: 4810-4818. (Pubitemid 38989341)
18. Maitta, R. W., K. Datta, A. Lees, S. S. Belouski, and L. A. Pirofski. 2004. Immunogenicity and efficacy of Cryptococcus neoformans capsular polysaccharide glucuronoxylomannan peptide mimotope-protein conjugates in human immunoglobulin transgenic mice. Infect. Immun. 72: 196-208. (Pubitemid 38018177)
19. Pirofski, L. A. 2001. Polysaccharides, mimotopes and vaccines for fungal and encapsulated pathogens. Trends Microbiol. 9: 445-451.
20. Moir, S., and A. S. Fauci. 2009. B cells in HIV infection and disease. Nat. Rev. Immunol. 9: 235-245.
21. Carsetti, R., M. M. Rosado, S. Donnanno, V. Guazzi, A. Soresina, A. Meini, A. Plebani, F. Aiuti, and I. Quinti. 2005. The loss of IgM memory B cells correlates with clinical disease in common variable immunodeficiency. J. Allergy Clin. Immunol. 115: 412-417. (Pubitemid 40215112)
22. Rapaka, R. R., D. M. Ricks, J. F. Alcorn, K. Chen, S. A. Khader, M. Zheng, S. Plevy, E. Bengté n, and J. K. Kolls. 2010. Conserved natural IgM antibodies mediate innate and adaptive immunity against the opportunistic fungus Pneumocystis murina. J. Exp. Med. 207: 2907-2919.
23. Baumgarth, N. 2011. The double life of a B-1 cell: self-reactivity selects for protective effector functions. Nat. Rev. Immunol. 11: 34-46.
24. + memory B cell expression predicts HIV-associated cryptococcosis status. J. Infect. Dis. 200: 244-251.
25. Fleuridor, R., R. H. Lyles, and L. Pirofski. 1999. Quantitative and qualitative differences in the serum antibody profiles of human immunodeficiency virusinfected persons with and without Cryptococcus neoformans meningitis. J. Infect. Dis. 180: 1526-1535. (Pubitemid 29506454)
26. Pirofski, L., R. Lui, M. DeShaw, A. B. Kressel, and Z. Zhong. 1995. Analysis of human monoclonal antibodies elicited by vaccination with a Cryptococcus neoformans glucuronoxylomannan capsular polysaccharide vaccine. Infect. Immun. 63: 3005-3014.
27. Subramaniam, K. S., K. Datta, E. Quintero, C. Manix, M. S. Marks, and L. A. Pirofski. 2010. The absence of serum IgM enhances the susceptibility of mice to pulmonary challenge with Cryptococcus neoformans. J. Immunol. 184: 5755-5767.
28. H derived from a natural anti-keratin antibody. Cell. Microbiol. 9: 306-315.
29. Rachini, A., D. Pietrella, P. Lupo, A. Torosantucci, P. Chiani, C. Bromuro, C. Proietti, F. Bistoni, A. Cassone, and A. Vecchiarelli. 2007. An anti-β-glucan monoclonal antibody inhibits growth and capsule formation of Cryptococcus neoformans in vitro and exerts therapeutic, anticryptococcal activity in vivo. Infect. Immun. 75: 5085-5094. (Pubitemid 350033595)
30. Monga, D. P., R. Kumar, L. N. Mohapatra, and A. N. Malaviya. 1979. Experimental cryptococcosis in normal and B-cell-deficient mice. Infect. Immun. 26: 1-3. (Pubitemid 10248621)
31. Aguirre, K. M., and L. L. Johnson. 1997. A role for B cells in resistance to Cryptococcus neoformans in mice. Infect. Immun. 65: 525-530. (Pubitemid 27053220)
32. Feldmesser, M., A. Mednick, and A. Casadevall. 2002. Antibody-mediated protection in murine Cryptococcus neoformans infection is associated with pleotrophic effects on cytokine and leukocyte responses. Infect. Immun. 70: 1571-1580. (Pubitemid 34163437)
33. Rivera, J., O. Zaragoza, and A. Casadevall. 2005. Antibody-mediated protection against Cryptococcus neoformans pulmonary infection is dependent on B cells. Infect. Immun. 73: 1141-1150. (Pubitemid 40165774)
34. Marquis, G., S. Montplaisir, M. Pelletier, S. Mousseau, and P. Auger. 1985. Genetic resistance to murine cryptococcosis: increased susceptibility in the CBA/N XID mutant strain of mice. Infect. Immun. 47: 282-287. (Pubitemid 15194624)
35. Haas, K. M., J. C. Poe, D. A. Steeber, and T. F. Tedder. 2005. B-1a and B-1b cells exhibit distinct developmental requirements and have unique functional roles in innate and adaptive immunity to S. pneumoniae. Immunity 23: 7-18. (Pubitemid 41019653)
36. Hardy, R. R. 2006. B-1 B cell development. J. Immunol. 177: 2749-2754. (Pubitemid 44277787)
37. Ghosn, E. E., R. Yamamoto, S. Hamanaka, Y. Yang, L. A. Herzenberg, H. Nakauchi, and L. A. Herzenberg. 2012. Distinct B-cell lineage commitment distinguishes adult bone marrow hematopoietic stem cells. Proc. Natl. Acad. Sci. USA 109: 5394-5398.
38. Carsetti, R., M. M. Rosado, and H. Wardmann. 2004. Peripheral development of B cells in mouse and man. Immunol. Rev. 197: 179-191. (Pubitemid 38142176)
39. Almeida, S. R., L. S. Aroeira, E. Frymuller, M. A. Dias, C. S. Bogsan, J. D. Lopes, and M. Mariano. 2001. Mouse B-1 cell-derived mononuclear phagocyte, a novel cellular component of acute non-specific inflammatory exudate. Int. Immunol. 13: 1193-1201. (Pubitemid 32903909)
40. Ghosn, E. E., M. Russo, and S. R. Almeida. 2006. Nitric oxide-dependent killing of Cryptococcus neoformans by B-1-derived mononuclear phagocyte. J. Leukoc. Biol. 80: 36-44. (Pubitemid 44835524)
41. Ghosh, S., S. A. Hoselton, and J. M. Schuh. 2012. μ-Chain-deficient mice possess B-1 cells and produce IgG and IgE, but Not IgA, following systemic sensitization and inhalational challenge in a fungal asthma model. J. Immunol. 189: 1322-1329.
42. Subramaniam, K. S., K. Datta, M. S. Marks, and L. A. Pirofski. 2010. Improved survival of mice deficient in secretory immunoglobulin M following systemic infection with Cryptococcus neoformans. Infect. Immun. 78: 441-452.
43. Mukherjee, J., M. D. Scharff, and A. Casadevall. 1992. Protective murine monoclonal antibodies to Cryptococcus neoformans. Infect. Immun. 60: 4534-4541.
44. Szymczak, W. A., R. S. Sellers, and L. A. Pirofski. 2012. IL-23 dampens the allergic response to Cryptococcus neoformans through IL-17-independent and -dependent mechanisms. Am. J. Pathol. 180: 1547-1559.
45. Cole, L. E., Y. Yang, K. L. Elkins, E. T. Fernandez, N. Qureshi, M. J. Shlomchik, L. A. Herzenberg, L. A. Herzenberg, and S. N. Vogel. 2009. Antigen-specific B-1a antibodies induced by Francisella tularensis LPS provide long-term protection against F. tularensis LVS challenge. Proc. Natl. Acad. Sci. USA 106: 4343-4348.
46. Newman, J., J. S. Rice, C. Wang, S. L. Harris, and B. Diamond. 2003. Identification of an antigen-specific B cell population. J. Immunol. Methods 272: 177-187. (Pubitemid 36050754)
47. Nimrichter, L., S. Frases, L. P. Cinelli, N. B. Viana, A. Nakouzi, L. R. Travassos, A. Casadevall, and M. L. Rodrigues. 2007. Self-aggregation of Cryptococcus neoformans capsular glucuronoxylomannan is dependent on divalent cations. Eukaryot. Cell 6: 1400-1410. (Pubitemid 47257709)
48. Tiller, T., C. E. Busse, and H. Wardemann. 2009. Cloning and expression of murine Ig genes from single B cells. J. Immunol. Methods 350: 183-193.
49. Kantor, A. B., C. E. Merrill, J. D. MacKenzie, L. A. Herzenberg, and J. L. Hillson. 1995. Development of the antibody repertoire as revealed by single-cell PCR of FACS-sorted B-cell subsets. Ann. N. Y. Acad. Sci. 764: 224-227. (Pubitemid 26136167)
50. Rohatgi, S., P. Ganju, and D. Sehgal. 2008. Systematic design and testing of nested (RT-)PCR primers for specific amplification of mouse rearranged/ expressed immunoglobulin variable region genes from small number of B cells. J. Immunol. Methods 339: 205-219.
51. H-less heavy chain gene usage and avidity maturation. J. Immunol. 182: 5570-5585.
52. Bogsan, C. S., R. R. Novaes e Brito, Mda. C. Palos, R. A. Mortara, S. R. Almeida, J. D. Lopes, and M. Mariano. 2005. B-1 cells are pivotal for in vivo inflammatory giant cell formation. Int. J. Exp. Pathol. 86: 257-265. (Pubitemid 41074391)
53. Murakami, M., H. Yoshioka, T. Shirai, T. Tsubata, and T. Honjo. 1995. Prevention of autoimmune symptoms in autoimmune-prone mice by elimination of B-1 cells. Int. Immunol. 7: 877-882.
54. + B-1 cells in EAE pathogenesis. Autoimmunity 41: 353-362.
55. Renner, B., D. Strassheim, C. R. Amura, L. Kulik, D. Ljubanovic, M. J. Glogowska, K. Takahashi, M. C. Carroll, V. M. Holers, and J. M. Thurman. 2010. B cell subsets contribute to renal injury and renal protection after ischemia/ reperfusion. J. Immunol. 185: 4393-4400.
56. H sequences from B-1a, B-1b, and conventional B cells. J. Immunol. 158: 1175-1186.
57. Tornberg, U. C., and D. Holmberg. 1995. B-1a, B-1b and B-2 B cells display unique VHDJH repertoires formed at different stages of ontogeny and under different selection pressures. EMBO J. 14: 1680-1689.
58. Kirkham, P. M., F. Mortari, J. A. Newton, and H. W. Schroeder, Jr. 1992. Immunoglobulin VH clan and family identity predicts variable domain structure and may influence antigen binding. EMBO J. 11: 603-609.
59. Nakouzi, A., and A. Casadevall. 2003. The function of conserved amino acids in or near the complementarity determining regions for related antibodies to Cryptococcus neoformans glucuronoxylomannan. Mol. Immunol. 40: 351-361. (Pubitemid 37176899)
60. Shiokawa, S., F. Mortari, J. O. Lima, C. Nuñez, F. E. Bertrand, III, P. M. Kirkham, S. Zhu, A. P. Dasanayake, and H. W. Schroeder, Jr. 1999. IgM heavy chain complementarity-determining region 3 diversity is constrained by genetic and somatic mechanisms until two months after birth. J. Immunol. 162: 6060-6070. (Pubitemid 29314965)
61. Zaragoza, O., M. Alvarez, A. Telzak, J. Rivera, and A. Casadevall. 2007. The relative susceptibility of mouse strains to pulmonary Cryptococcus neoformans infection is associated with pleiotropic differences in the immune response. Infect. Immun. 75: 2729-2739. (Pubitemid 46870153)
62. Choi, Y. S., and N. Baumgarth. 2008. Dual role for B-1a cells in immunity to influenza virus infection. J. Exp. Med. 205: 3053-3064.
63. Rothaeusler, K., and N. Baumgarth. 2010. B-cell fate decisions following influenza virus infection. Eur. J. Immunol. 40: 366-377.
64. Baumgarth, N., O. C. Herman, G. C. Jager, L. E. Brown, L. A. Herzenberg, and J. Chen. 2000. B-1 and B-2 cell-derived immunoglobulin M antibodies are nonredundant components of the protective response to influenza virus infection. J. Exp. Med. 192: 271-280. (Pubitemid 30470309)
65. Ansel, K. M., R. B. Harris, and J. G. Cyster. 2002. CXCL13 is required for B1 cell homing, natural antibody production, and body cavity immunity. Immunity 16: 67-76. (Pubitemid 34143217)
66. Oliveira, H. C., A. F. Popi, A. L. Bachi, S. Nonogaki, J. D. Lopes, and M. Mariano. 2010. B-1 cells modulate the kinetics of wound-healing process in mice. Immunobiology 215: 215-222.
67. + T cells. J. Leukoc. Biol. 91: 525-536.
68. Popi, A. F., D. S. Zamboni, R. A. Mortara, and M. Mariano. 2009. Microbicidal property of B1 cell derived mononuclear phagocyte. Immunobiology 214: 664-673.
69. Pietrella, D., A. Rachini, A. Torosantucci, P. Chiani, A. J. Brown, F. Bistoni, P. Costantino, P. Mosci, C. d'Enfert, R. Rappuoli, et al. 2010. A β-glucanconjugate vaccine and anti-β-glucan antibodies are effective against murine vaginal candidiasis as assessed by a novel in vivo imaging technique. Vaccine 28: 1717-1725.
70. Alugupalli, K. R., R. M. Gerstein, J. Chen, E. Szomolanyi-Tsuda, R. T. Woodland, and J. M. Leong. 2003. The resolution of relapsing fever borreliosis requires IgM and is concurrent with expansion of B1b lymphocytes. J. Immunol. 170: 3819-3827. (Pubitemid 36359252)
71. Alugupalli, K. R., J. M. Leong, R. T. Woodland, M. Muramatsu, T. Honjo, and R. M. Gerstein. 2004. B1b lymphocytes confer T cell-independent long-lasting immunity. Immunity 21: 379-390. (Pubitemid 39208339)
72. Arjunaraja, S., P. Massari, L. M. Wetzler, A. Lees, J. Colino, and C. M. Snapper. 2012. The nature of an in vivo anti-capsular polysaccharide response is markedly influenced by the composition and/or architecture of the bacterial subcapsular domain. J. Immunol. 188: 569-577.
73. Colino, J., L. Duke, S. Arjunaraja, Q. Chen, L. Liu, A. H. Lucas, and C. M. Snapper. 2012. Differential idiotype utilization for the in vivo type 14 capsular polysaccharide-specific Ig responses to intact Streptococcus pneumoniae versus a pneumococcal conjugate vaccine. J. Immunol. 189: 575-586.
74. Seidl, K. J., J. D. MacKenzie, D. Wang, A. B. Kantor, E. A. Kabat, L. A. Herzenberg, and L. A. Herzenberg. 1997. Frequent occurrence of identical heavy and light chain Ig rearrangements. Int. Immunol. 9: 689-702. (Pubitemid 27226392)
75. Hardy, R. R., C. E. Carmack, S. A. Shinton, R. J. Riblet, and K. Hayakawa. 1989. A single VH gene is utilized predominantly in anti-BrMRBC hybridomas derived from purified Ly-1 B cells. Definition of the VH11 family. J. Immunol. 142: 3643-3651. (Pubitemid 19137501)
76. +) B cells that recognize phosphatidyl choline. J. Exp. Med. 169: 1869-1877.
77. Oliveira, D. L., L. Nimrichter, K. Miranda, S. Frases, K. F. Faull, A. Casadevall, and M. L. Rodrigues. 2009. Cryptococcus neoformans cryoultramicrotomy and vesicle fractionation reveals an intimate association between membrane lipids and glucuronoxylomannan. Fungal Genet. Biol. 46: 956-963.
78. Yoshikawa, S., Y. Kawano, Y. Minegishi, and H. Karasuyama. 2009. The skewed heavy-chain repertoire in peritoneal B-1 cells is predetermined by the selection via pre-B cell receptor during B cell ontogeny in the fetal liver. Int. Immunol. 21: 43-52.
79. Chattopadhyay, G., Q. Chen, J. Colino, A. Lees, and C. M. Snapper. 2009. Intact bacteria inhibit the induction of humoral immune responses to bacterial-derived and heterologous soluble T cell-dependent antigens. J. Immunol. 182: 2011-2019.
80. Nicola, A. M., S. Frases, and A. Casadevall. 2009. Lipophilic dye staining of Cryptococcus neoformans extracellular vesicles and capsule. Eukaryot. Cell 8: 1373-1380.
81. Silverman, G. J., S. P. Cary, D. C. Dwyer, L. Luo, R. Wagenknecht, and V. E. Curtiss. 2000. A B cell superantigen-induced persistent "Hole" in the B-1 repertoire. J. Exp. Med. 192: 87-98. (Pubitemid 30470809)
82. Foote, J. B., and J. F. Kearney. 2009. Generation of B cell memory to the bacterial polysaccharide a-1,3 dextran. J. Immunol. 183: 6359-6368.
83. Reese, A. J., and T. L. Doering. 2003. Cell wall a-1,3-glucan is required to anchor the Cryptococcus neoformans capsule. Mol. Microbiol. 50: 1401-1409. (Pubitemid 37475869)
84. Reese, A. J., A. Yoneda, J. A. Breger, A. Beauvais, H. Liu, C. L. Griffith, I. Bose, M. J. Kim, C. Skau, S. Yang, et al. 2007. Loss of cell wall a(1-3) glucan affects Cryptococcus neoformans from ultrastructure to virulence. Mol. Microbiol. 63: 1385-1398.
85. H is sufficient for most antibody specificities. Immunity 13: 37-45.
86. Ippolito, G. C., R. L. Schelonka, M. Zemlin, I. I. Ivanov, R. Kobayashi, C. Zemlin, G. L. Gartland, L. Nitschke, J. Pelkonen, K. Fujihashi, et al. 2006. Forced usage of positively charged amino acids in immunoglobulin CDR-H3 impairs B cell development and antibody production. J. Exp. Med. 203: 1567-1578. (Pubitemid 43877616)
87. Ivanov, I. I., R. L. Schelonka, Y. Zhuang, G. L. Gartland, M. Zemlin, and H. W. Schroeder, Jr. 2005. Development of the expressed Ig CDR-H3 repertoire is marked by focusing of constraints in length, amino acid use, and charge that are first established in early B cell progenitors. J. Immunol.174: 7773-80. (Pubitemid 40806284)
88. Mahmoud, T. I., H. W. Schroeder, Jr., and J. F. Kearney. 2011. Limiting CDR-H3 diversity abrogates the antibody response to the bacterial polysaccharide α 1→3 dextran. J. Immunol. 187: 879-886.
89. Mahmoud, T. I., and J. F. Kearney. 2010. Terminal deoxynucleotidyl transferase is required for an optimal response to the polysaccharide α-1,3 dextran. J. Immunol. 184: 851-858.
90. Casadevall, A., and M. D. Scharff. 1991. The mouse antibody response to infection with Cryptococcus neoformans: VH and VL usage in polysaccharide binding antibodies. J. Exp. Med. 174: 151-160.
91. Yang, Y., E. E. Ghosn, L. E. Cole, T. V. Obukhanych, P. Sadate-Ngatchou, S. N. Vogel, L. A. Herzenberg, and L. A. Herzenberg. 2012. Antigen-specific antibody responses in B-1a and their relationship to natural immunity. Proc. Natl. Acad. Sci. USA 109: 5382-5387.
92. Yang, Y., E. E. Ghosn, L. E. Cole, T. V. Obukhanych, P. Sadate-Ngatchou, S. N. Vogel, L. A. Herzenberg, and L. A. Herzenberg. 2012. Antigen-specific memory in B-1a and its relationship to natural immunity. Proc. Natl. Acad. Sci. USA 109: 5388-5393.