Memory B cells of mice and humans

Annual Review of Immunology

Volumn 35, Issue , 2017, Pages 255-284

  Weisel, Florian ^a   Shlomchik, Mark ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

B cell subsets; Germinal center; Immune memory; Memory B cell; Plasma cell; Vaccine

Indexed keywords

IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; TRANSCRIPTOME; VACCINE;

ADOPTIVE TRANSFER; AGNOSTIC; BURNOUT; CELL DIFFERENTIATION; CYTOMEGALOVIRUS INFECTION; FLOW CYTOMETRY; GENE EXPRESSION; GERMINAL CENTER; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGICAL MEMORY; INFLUENZA; LYMPHOID TISSUE; MEMORY CELL; MOUSE; NONHUMAN; PERIPHERAL LYMPHOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; ANIMAL; B LYMPHOCYTE; B LYMPHOCYTE SUBPOPULATION; HUMORAL IMMUNITY; IMMUNOLOGY; LYMPHOCYTE ACTIVATION;

ANIMALS; B-LYMPHOCYTE SUBSETS; B-LYMPHOCYTES; HUMANS; IMMUNITY, HUMORAL; IMMUNOLOGIC MEMORY; LYMPHOCYTE ACTIVATION; MICE; TRANSCRIPTOME; VACCINES;

EID: 85018250708     PISSN: 07320582     EISSN: 15453278     Source Type: Book Series    
DOI: 10.1146/annurev-immunol-041015-055531     Document Type: Review

References (193)

1. Netea MG, Latz E, Mills KHG, O'Neill LAJ. 2015. Innate immune memory: a paradigm shift in understanding host defense. Nat. Immunol. 16:675-79
2. Yamane H, Paul WE. 2012. Memory CD4+ T cells: fate determination, positive feedback and plasticity. Cell. Mol. Life Sci. 69:1577-83
3. Restifo NP, Gattinoni L. 2013. Lineage relationship of effector and memory T cells. Curr. Opin. Immunol. 25:556-63
4. Harris DP, Haynes L, Sayles PC, Durso DK, Eaton SM, et al. 2000. Reciprocal regulation of polarized cytokine production by effector B and T cells. Nat. Immunol. 1:475-82
5. Lund FE, Garvy BA, Randall TD, Harris DP. 2005. Regulatory roles for cytokine-producing B cells in infection and autoimmune disease. Curr. Dir. Autoimmun. 8:25-54
6. Duddy M, Niino M, Adatia F, Hebert S, Freedman M, et al. 2007. Distinct effector cytokine profiles of memory and naive human B cell subsets and implication in multiple sclerosis. J. Immunol. 178:6092-99
7. Slifka MK, Antia R, Whitmire JK, Ahmed R. 1998. Humoral immunity due to long-lived plasma cells. Immunity 8:363-72
8. Hammarlund E, Lewis MW, Hansen SG, Strelow LI, Nelson JA, et al. 2003. Duration of antiviral immunity after smallpox vaccination. Nat. Med. 9:1131-37
9. Obukhanych TV, Nussenzweig MC. 2006. T-independent type II immune responses generate memory B cells. J. Exp. Med. 203:305-10
10. Taillardet M, Haffar G, Mondiere P, Asensio M-J, Gheit H, et al. 2009. The thymus-independent immunity conferred by a pneumococcal polysaccharide is mediated by long-lived plasma cells. Blood 114:4432-40
11. McHeyzer-Williams MG, Nossal GJV, Lalor PA. 1991. Molecular characterization of single memory B cells. Nature 350:502-5
12. Pierce SK, Liu W. 2013. Encoding immunological memory in the initiation of B-cell receptor signaling. Cold Spring Harb. Symp. Quant. Biol. 78:231-37
13. Anderson SM, Tomayko MM, Shlomchik MJ. 2006. Intrinsic properties of human and murine memory B cells. Immunol. Rev. 211:280-94
14. Tomayko MM, Steinel NC, Anderson SM, Shlomchik MJ. 2010. Cutting edge: hierarchy of maturity of murine memory B cell subsets. J. Immunol. 185:7146-50
15. Tomayko MM, Anderson SM, Brayton CE, Sadanand S, Steinel NC, et al. 2008. Systematic comparison of gene expression between murine memory and naive B cells demonstrates that memory B cells have unique signaling capabilities. J. Immunol. 181:27-38
16. Anderson SM, Hannum LG, Shlomchik MJ. 2006. Cutting edge: memory B cell survival and function in the absence of secreted antibody and immune complexes on follicular dendritic cells. J. Immunol. 176:4515-19
17. Anderson SM, Tomayko MM, Ahuja A, Haberman AM, Shlomchik MJ. 2007. New markers for murine memory B cells that define mutated and unmutated subsets. J. Exp. Med. 204:2103-14
18. Dogan I, Bertocci B, Vilmont V, Delbos F, Megret J, et al. 2009. Multiple layers of B cell memory with different effector functions. Nat. Immunol. 10:1292-99
19. Hougs L, Juul L, Ditzel HJ, Heilmann C, Svejgaard A, Barington T. 1999. The first dose of a Haemophilus influenzae type B conjugate vaccine reactivates memory B cells: evidence for extensive clonal selection, intraclonal affinity maturation, and multiple isotype switches to IgA2. J. Immunol. 162:224-37
20. Frolich D, Giesecke C, Mei HE, Reiter K, Daridon C, et al. 2010. Secondary immunization generates clonally related antigen-specific plasma cells and memory B cells. J. Immunol. 185:3103-10
21. Giesecke C, Frolich D, Reiter K, Mei HE, Wirries I, et al. 2014. Tissue distribution and dependence of responsiveness of human antigen-specific memory B cells. J. Immunol. 192:3091-100
22. Pape KA, Taylor JJ, Maul RW, Gearhart PJ, Jenkins MK. 2011. Different B cell populations mediate early and late memory during an endogenous immune response. Science 331:1203-7
23. Taylor JJ, Pape KA, Jenkins MK. 2012. A germinal center-independent pathway generates unswitched memory B cells early in the primary response. J. Exp. Med. 209:597-606
24. Hayakawa K, Ishii R, Yamasaki K, Kishimoto T, Hardy RR. 1987. Isolation of high-affinity memory B cells: phycoerythrin as a probe for antigen-binding cells. PNAS 84:1379-83
25. Schittek B, Rajewsky K. 1990. Maintenance of B-cell memory by long-lived cells generated from proliferating precursors. Nature 346:749-51
26. Schittek B, Rajewsky K, Forster I. 1991. Dividing cells in bone marrow and spleen incorporate bromodeoxyuridine with high efficiency. Eur. J. Immunol. 21:235-38
27. Weisel FJ, Appelt UK, Schneider AM, Horlitz JU, van Rooijen N, et al. 2010. Unique requirements for reactivation of virus-specific memory B lymphocytes. J. Immunol. 185:4011-21
28. Silvy A, Lagresle C, Bella C, Defrance T. 1996. The differentiation of human memory B cells into specific antibody-secreting cells is CD40 independent. Eur. J. Immunol. 26:517-24
29. Crotty S, Felgner P, Davies H, Glidewell J, Villarreal L, Ahmed R. 2003. Cutting edge: long-term B cell memory in humans after smallpox vaccination. J. Immunol. 171:4969-73
30. Bernasconi NL, Traggiai E, Lanzavecchia A. 2002. Maintenance of serological memory by polyclonal activation of human memory B cells. Science 298:2199-202
31. Clarke ET, Williams NA, Findlow J, Borrow R, Heyderman RS, Finn A. 2013. Polysaccharide-specific memoryBcells generated by conjugate vaccines in humans conform to theCD27+IgG+ isotype-switched memory B cell phenotype and require contact-dependent signals from bystander T cells activated by bacterial proteins to differentiate into plasma cells. J. Immunol. 191:6071-83
32. Joo HM, He Y, Sangster MY. 2008. Broad dispersion and lung localization of virus-specific memory B cells induced by influenza pneumonia. PNAS 105:3485-90
33. Dal Porto JM, Haberman AM, Shlomchik MJ, Kelsoe G. 1998. Antigen drives very low affinity B cells to become plasmacytes and enter germinal centers. J. Immunol. 161:5373-81
34. Dal Porto JM, Haberman AM, Kelsoe G, Shlomchik MJ. 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. 195:1215-21
35. Di Niro R, Lee SJ, Vander Heiden JA, Elsner RA, Trivedi N, et al. 2015. Salmonella infection drives promiscuous B cell activation followed by extrafollicular affinity maturation. Immunity 43:120-31
36. Wrammert J, Smith K, Miller J, Langley WA, Kokko K, et al. 2008. Rapid cloning of high-affinity human monoclonal antibodies against influenza virus. Nature 453:667-71
37. Wrammert J, Onlamoon N, Akondy RS, Perng GC, Polsrila K, et al. 2012. Rapid and massive virusspecific plasmablast responses during acute dengue virus infection in humans. J. Virol. 86:2911-18
38. Klein U, Kuppers R, Rajewsky K. 1997. Evidence for a large compartment of IgM-expressing memory B cells in humans. Blood 89:1288-98
39. Tangye SG, Liu YJ, Aversa G, Phillips JH, de Vries JE. 1998. Identification of functional human splenic memory B cells by expression of CD148 and CD27. J. Exp. Med. 188:1691-703
40. Tangye SG, Avery DT, Deenick EK, Hodgkin PD. 2003. Intrinsic differences in the proliferation of naive and memory human B cells as amechanism for enhanced secondary immune responses. J. Immunol. 170:686-94
41. Good KL, Bryant VL, Tangye SG. 2006. Kinetics of human B cell behavior and amplification of proliferative responses following stimulation with IL-21. J. Immunol. 177:5236-47
42. Good KL, Avery DT, Tangye SG. 2009. Resting human memory B cells are intrinsically programmed for enhanced survival and responsiveness to diverse stimuli compared to naive B cells. J. Immunol. 182:890-901
43. Tangye SG, Tarlinton DM. 2009. Memory B cells: effectors of long-lived immune responses. Eur. J. Immunol. 39:2065-75
44. Bernasconi NL, Onai N, Lanzavecchia A. 2003. A role for Toll-like receptors in acquired immunity: up-regulation of TLR9 by BCR triggering in naive B cells and constitutive expression in memory B cells. Blood 101:4500-4
45. Arpin C, Banchereau J, Liu Y-J. 1997. Memory B cells are biased towards terminal differentiation: a strategy that may prevent repertoire freezing. J. Exp. Med. 186:931-40
46. Ehrhardt GRA, Hsu JT, Gartland L, Leu C-M, Zhang S, et al. 2005. Expression of the immunoregulatory molecule FcRH4 defines a distinctive tissue-based population ofmemory B cells. J. Exp.Med. 202:783-91
47. Fecteau JF, Cote G, Neron S. 2006. A new memory CD27-IgG+ B cell population in peripheral blood expressing VH genes with low frequency of somatic mutation. J. Immunol. 177:3728-36
48. Wei C, Anolik J, Cappione A, Zheng B, Pugh-Bernard A, et al. 2007. A new population of cells lacking expression of CD27 represents a notable component of the B cell memory compartment in systemic lupus erythematosus. J. Immunol. 178:6624-33
49. Kaech SM, Wherry EJ, Ahmed R. 2002. Effector and memory T-cell differentiation: implications for vaccine development. Nat. Rev. Immunol. 2:251-62
50. Beura LK, Hamilton SE, Bi K, Schenkel JM, Odumade OA, et al. 2016. Normalizing the environment recapitulates adult human immune traits in laboratory mice. Nature 532:512-16
51. Reese TA, Bi K, Kambal A, Filali-Mouhim A, Beura LK, et al. 2016. Sequential infection with common pathogens promotes human-like immune gene expression and altered vaccine response. Cell Host Microbe 19:713-19
52. Macallan DC, Wallace DL, Zhang Y, Ghattas H, Asquith B, et al. 2005. B-cell kinetics in humans: rapid turnover of peripheral blood memory cells. Blood 105:3633-40
53. Wirths S, Lanzavecchia A. 2005. ABCB1 transporter discriminates human resting naive B cells from cycling transitional and memory B cells. Eur. J. Immunol. 35:3433-41
54. Anderson S, Tomayko M, Ahuja A, Haberman A, Shlomchik M. 2007. Newmarkers formurinememory B cells that define mutated and unmutated subsets. J. Exp. Med. 204:2103-14
55. Weisel FJ, Zuccarino-Catania GV, Chikina M, Shlomchik MJ. 2016. A temporal switch in the germinal center determines differential output of memory B and plasma cells. Immunity 44:116-30
56. Onodera T, Takahashi Y, Yokoi Y, Ato M, Kodama Y, et al. 2012. Memory B cells in the lung participate in protective humoral immune responses to pulmonary influenza virus reinfection. PNAS 109:2485-90
57. Bemark M, Bergqvist P, Stensson A, Holmberg A, Mattsson J, Lycke NY. 2011. A unique role of the cholera toxin A1-DD adjuvant for long-term plasma and memory B cell development. J. Immunol. 186:1399-410
58. Lindner C, Thomsen I, Wahl B, Ugur M, Sethi MK, et al. 2015. Diversification of memory B cells drives the continuous adaptation of secretory antibodies to gut microbiota. Nat. Immunol. 16:880-88
59. Krishnamurty AT, Thouvenel CD, Portugal S, Keitany GJ, Kim KS, et al. 2016. Somatically hypermutated Plasmodium-specific IgM+ memory B cells are rapid, plastic, early responders upon malaria rechallenge. Immunity 45:402-14
60. Driver DJ, McHeyzer-Williams LJ, Cool M, Stetson DB, McHeyzer-Williams MG. 2001. Development and maintenance of a B220-memory B cell compartment. J. Immunol. 167:1393-405
61. Bell J, Gray D. 2003. Antigen-capturing cells can masquerade as memory B cells. J. Exp. Med. 197:1233-44
62. Wolniak KL, Noelle RJ, Waldschmidt TJ. 2006. Characterization of (4-hydroxy-3-nitrophenyl)acetyl (NP)-specific germinal center B cells and antigen-binding B220-cells after primary NP challenge in mice. J. Immunol. 177:2072-79
63. Dell CL, Lu Y, Claflin JL. 1989. Molecular analysis of clonal stability and longevity in B cell memory. J. Immunol. 143:3364-70
64. Vajdy M, Lycke N. 1995. Mucosal memory B cells retain the ability to produce IgM antibodies 2 years after oral immunization. Immunology 86:336-42
65. Jones DD, Wilmore JR, Allman D. 2015. Cellular dynamics of memory B cell populations: IgM+ and IgG+ memory B cells persist indefinitely as quiescent cells. J. Immunol. 195:4753-59
66. Gitlin AD, vonBoehmer L, Gazumyan A, Shulman Z, Oliveira TY, Nussenzweig MC. 2016. Independent roles of switching and hypermutation in the development and persistence of B lymphocyte memory. Immunity 44:769-81
67. Bar-Or A, Oliveira EM, Anderson DE, Krieger JI, Duddy M, et al. 2001. Immunological memory: contribution of memory B cells expressing costimulatory molecules in the resting state. J. Immunol. 167:5669-77
68. Airoldi I, Raffaghello L, Cocco C, Guglielmino R, Roncella S, et al. 2004. Heterogeneous expression of interleukin-18 and its receptor in B-cell lymphoproliferative disorders deriving from naive, germinal center, and memory B lymphocytes. Clin. Cancer Res. 10:144-54
69. Ehrhardt GR, Hijikata A, Kitamura H, Ohara O, Wang JY, Cooper MD. 2008. Discriminating gene expression profiles of memory B cell subpopulations. J. Exp. Med. 205:1807-17
70. Weiss GE, Crompton PD, Li S, Walsh LA, Moir S, et al. 2009. Atypical memory B cells are greatly expanded in individuals living in a malaria-endemic area. J. Immunol. 183:2176-82
71. Llinas L, Lazaro A, de Salort J, Matesanz-Isabel J, Sintes J, Engel P. 2011. Expression profiles of novel cell surface molecules on B-cell subsets and plasma cells as analyzed by flow cytometry. Immunol. Lett. 134:113-21
72. Li H, Borrego F, Nagata S, Tolnay M. 2016. Fc receptor-like 5 expression distinguishes two distinct subsets of human circulating tissue-like memory B cells. J. Immunol. 196:4064-74
73. Sullivan RT, Kim CC, Fontana MF, Feeney ME, Jagannathan P, et al. 2015. FCRL5 delineates functionally impaired memory B cells associated with Plasmodium falciparum exposure. PLOS Pathog. 11:e1004894
74. Isnardi I, Ng Y-S, Menard L, Meyers G, Saadoun D, et al. 2010. Complement receptor 2/CD21-human naive B cells contain mostly autoreactive unresponsive clones. Blood 115:5026-36
75. Rakhmanov M, Keller B, Gutenberger S, Foerster C, Hoenig M, et al. 2009. Circulating CD21low B cells in common variable immunodeficiency resemble tissue homing, innate-like B cells. PNAS 106:13451-56
76. Moir S, Ho J, Malaspina A, Wang W, DiPoto AC, et al. 2008. Evidence for HIV-associated B cell exhaustion in a dysfunctional memory B cell compartment in HIV-infected viremic individuals. J. Exp. Med. 205:1797-805
77. Charles ED, Brunetti C, Marukian S, Ritola KD, Talal AH, et al. 2011. Clonal B cells in patients with hepatitis C virus-associated mixed cryoglobulinemia contain an expanded anergicCD21low B-cell subset. Blood 117:5425-37
78. Dauby N, Kummert C, Lecomte S, Liesnard C, Delforge ML, et al. 2014. Primary human cytomegalovirus infection induces the expansion of virus-specific activated and atypical memory B cells. J. Infect. Dis. 210:1275-85
79. Portugal S, Tipton CM, Sohn H, Kone Y, Wang J, et al. 2015. Malaria-associated atypical memory B cells exhibit markedly reduced B cell receptor signaling and effector function. eLife 4:e07218
80. Nicholas MW, Dooley MA, Hogan SL, Anolik J, Looney J, et al. 2008. A novel subset of memory B cells is enriched in autoreactivity and correlates with adverse outcomes in SLE. Clin. Immunol. 126:189-201
81. Wakabayashi C, Adachi T, Wienands J, Tsubata T. 2002. A distinct signaling pathway used by the IgG-containing B cell antigen receptor. Science 298:2392-95
82. Martin SW, Goodnow CC. 2002. Burst-enhancing role of the IgG membrane tail as a molecular determinant of memory. Nat. Immunol. 3:182-88
83. Xu Y, Xu L, Zhao M, Xu C, Fan Y, et al. 2014. No receptor stands alone: IgG B-cell receptor intrinsic and extrinsic mechanisms contribute to antibody memory. Cell Res. 24:651-64
84. Lutz J, Dittmann K, Bosl MR, Winkler TH, Wienands J, Engels N. 2016. Reactivation of IgG-switched memory B cells by BCR-intrinsic signal amplification promotes IgG antibody production. Nat. Commun. 6:8575
85. Wienands J, Engels N. 2016. The memory function of the B cell antigen receptor. Curr. Top. Microbiol. Immunol. 393:107-21
86. Zuccarino-Catania GV, Sadanand S, Weisel FJ, Tomayko MM, Meng H, et al. 2014. CD80 and PDL2 define functionally distinct memory B cell subsets that are independent of antibody isotype. Nat. Immunol. 15:631-37
87. Kometani K, Nakagawa R, Shinnakasu R, Kaji T, Rybouchkin A, et al. 2013. Repression of the transcription factor Bach2 contributes to predisposition of IgG1 memory B cells toward plasma cell differentiation. Immunity 39:136-47
88. Jash A, Wang Y, Weisel FJ, Scharer CD, Boss JM, et al. 2016. ZBTB32 restricts the duration of memory B cell recall responses. J. Immunol. 197:1159-68
89. Good KL, Tangye SG. 2007. Decreased expression of Kruppel-like factors in memory B cells induces the rapid response typical of secondary antibody responses. PNAS 104:13420-25
90. Seifert M, Przekopowitz M, Taudien S, Lollies A, Ronge V, et al. 2015. Functional capacities of human IgM memory B cells in early inflammatory responses and secondary germinal center reactions. PNAS 112:E546-55
91. Davey AM, Pierce SK. 2012. Intrinsic differences in the initiation of B cell receptor signaling favor responses of human IgG+ memory B cells over IgM+ naive B cells. J. Immunol. 188:3332-41
92. Takahashi Y, Ohta H, Takemori T. 2001. Fas is required for clonal selection in germinal centers and the subsequent establishment of the memory B cell repertoire. Immunity 14:181-92
93. Inamine A, Takahashi Y, Baba N, Miyake K, Tokuhisa T, et al. 2005. Two waves of memory B-cell generation in the primary immune response. Int. Immunol. 17:581-89
94. Toyama H, Okada S, Hatano M, Takahashi Y, Takeda N, et al. 2002. Memory B cells without somatic hypermutation are generated from Bcl6-deficient B cells. Immunity 17:329-39
95. Kaji T, Ishige A, Hikida M, Taka J, Hijikata A, et al. 2012. Distinct cellular pathways select germlineencoded and somatically mutated antibodies into immunological memory. J. Exp. Med. 209:2079-97
96. Berkowska MA, Driessen GJA, Bikos V, Grosserichter-Wagener C, Stamatopoulos K, et al. 2011.Human memory B cells originate from three distinct germinal center-dependent and -independent maturation pathways. Blood 118:2150-58
97. Tangye SG, Good KL. 2007. Human IgM+CD27+ B cells: memory B cells or "memory" B cells? J. Immunol. 179:13-19
98. Schwickert TA, Victora GD, Fooksman DR, Kamphorst AO, Mugnier MR, et al. 2011. A dynamic T cell-limited checkpoint regulates affinity-dependent B cell entry into the germinal center. J. Exp. Med. 208:1243-52
99. Song H, Cerny J. 2003. Functional heterogeneity of marginal zone B cells revealed by their ability to generate both early antibody-forming cells and germinal centers with hypermutation and memory in response to a T-dependent antigen. J. Exp. Med. 198:1923-35
100. Baumgarth N. 2013. Innate-like B cells and their rules of engagement. Adv. Exp. Med. Biol. 785:57-66
101. Foote JB, Kearney JF. 2009. Generation of B cell memory to the bacterial polysaccharide a-1,3 dextran. J. Immunol. 183:6359-68
102. Alugupalli KR, Leong JM, Woodland RT, Muramatsu M, Honjo T, Gerstein RM. 2004. B1b lymphocytes confer T cell-independent long-lasting immunity. Immunity 21:379-90
103. Liu Y-J, Barthelemy C, de Bouteiller O, Arpin C, Durand I, Banchereau J. 1995. Memory B cells from human tonsils colonize mucosal epithelium and directly present antigen to T cells by rapid up-regulation of B7-1 and B7-2. Immunity 2:239-48
104. Dunn-Walters DK, Isaacson PG, Spencer J. 1996. Sequence analysis of rearranged IgVH genes from microdissected human Peyer's patch marginal zone B cells. Immunology 88:618-24
105. Mahanonda R, Champaiboon C, Subbalekha K, Sa-Ard-Iam N, Rattanathammatada W, et al. 2016. Human memory B cells in healthy gingiva, gingivitis, and periodontitis. J. Immunol. 197:715-25
106. Vajdy M, Lycke N. 1993. Stimulation of antigen-specificT-and B-cell memory in local as well as systemic lymphoid tissues following oral immunization with cholera toxin adjuvant. Immunology 80:197-203
107. Bemark M, Hazanov H, Stromberg A, Komban R, Holmqvist J, et al. 2016. Limited clonal relatedness between gut IgA plasma cells and memory B cells after oral immunization. Nat. Commun. 7:12698
108. Moyron-Quiroz JE, Rangel-Moreno J, Hartson L, Kusser K, Tighe MP, et al. 2006. Persistence and responsiveness of immunologicmemory in the absence of secondary lymphoid organs. Immunity 25:643-54
109. Bunker JJ, Flynn TM, Koval JC, Shaw DG, Meisel M, et al. 2015. Innate and adaptive humoral responses coat distinct commensal bacteria with immunoglobulin A. Immunity 43:541-53
110. Yuvaraj S, Dijkstra G, Burgerhof JG, Dammers PM, Stoel M, et al. 2009. Evidence for local expansion of IgA plasma cell precursors in human ileum. J. Immunol. 183:4871-78
111. Hapfelmeier S, Lawson MAE, Slack E, Kirundi JK, Stoel M, et al. 2010. Reversiblemicrobial colonization of germ-free mice reveals the dynamics of IgA immune responses. Science 328:1705-9
112. Martinoli C, Chiavelli A, Rescigno M. 2007. Entry route of Salmonella typhimurium directs the type of induced immune response. Immunity 27:975-84
113. Cunningham AF, Gaspal F, Serre K, Mohr E, Henderson IR, et al. 2007. Salmonella induces a switched antibody response without germinal centers that impedes the extracellular spread of infection. J. Immunol. 178:6200-7
114. Mittrucker HW, Raupach B, Kohler A, Kaufmann SH. 2000. Cutting edge: role of B lymphocytes in protective immunity against Salmonella typhimurium infection. J. Immunol. 164:1648-52
115. Liu YJ, Oldfield S, MacLennan IC. 1988. Memory B cells in T cell-dependent antibody responses colonize the splenic marginal zones. Eur. J. Immunol. 18:355-62
116. Steiniger B, Timphus E-M, Jacob R, Barth PJ. 2005. CD27+ B cells in human lymphatic organs: reevaluating the splenic marginal zone. Immunology 116:429-42
117. Takemori T, Kaji T, Takahashi Y, Shimoda M, Rajewsky K. 2014. Generation of memory B cells inside and outside germinal centers. Eur. J. Immunol. 44:1258-64
118. Scholz JL, Crowley JE, Tomayko MM, Steinel N, O'Neill PJ, et al. 2008. BLyS inhibition eliminates primary B cells but leaves natural and acquired humoral immunity intact. PNAS 105:15517-22
119. Benson MJ, Dillon SR, Castigli E, Geha RS, Xu S, et al. 2008. Cutting edge: the dependence of plasma cells and independence of memory B cells on BAFF and APRIL. J. Immunol. 180:3655-59
120. Ackermann JA, Nys J, Schweighoffer E, McCleary S, Smithers N, Tybulewicz VLJ. 2015. Syk tyrosine kinase is critical for B cell antibody responses and memory B cell survival. J. Immunol. 194:4650-56
121. Kraus M, Alimzhanov MB, Rajewsky N, Rajewsky K. 2004. Survival of resting mature B lymphocytes depends on BCR signaling via the Iga/βheterodimer. Cell 117:787-800
122. Turner M, Gulbranson-Judge A, Quinn ME, Walters AE, MacLennan IC, Tybulewicz VL. 1997. Syk tyrosine kinase is required for the positive selection of immature B cells into the recirculating B cell pool. J. Exp. Med. 186:2013-21
123. Cornall RJ, Cheng AM, Pawson T, Goodnow CC. 2000. Role of Syk in B-cell development and antigenreceptor signaling. PNAS 97:1713-18
124. Hobeika E, Levit-Zerdoun E, Anastasopoulou V, Pohlmeyer R, Altmeier S, et al. 2015. CD19 and BAFF-R can signal to promote B-cell survival in the absence of Syk. EMBO J. 34:925-39
125. Torcia M, Bracci-Laudiero L, Lucibello M, Nencioni L, Labardi D, et al. 1996. Nerve growth factor is an autocrine survival factor for memory B lymphocytes. Cell 85:345-56
126. Bhattacharya D, Cheah MT, Franco CB, Hosen N, Pin CL, et al. 2007. Transcriptional profiling of antigen-dependent murine B cell differentiation and memory formation. J. Immunol. 179:6808-19
127. Luckey CJ, Bhattacharya D, Goldrath AW, Weissman IL, Benoist C, Mathis D. 2006. Memory T and memory B cells share a transcriptional program of self-renewal with long-term hematopoietic stem cells. PNAS 103:3304-9
128. Vieira P, Rajewsky K. 1990. Persistence of memory B cells in mice deprived of T cell help. Int. Immunol. 2:487-94
129. Tew JG, Phipps RP, Madnel TE. 1980. The follicular dendritic cell: long-term antigen retention during immunity. Immunol. Rev. 53:29-59
130. Kosco-Vilbois MH. 2003. Opinion: Are follicular dendritic cells really good for nothing? Nat. Rev. Immunol. 3:764-69
131. Gray D, Skarvall H. 1988. B-cell memory is short-lived in the absence of antigen. Nature 336:70-73
132. Maruyama M, Lam KP, Rajewsky K. 2000. Memory B-cell persistence is independent of persisting immunizing antigen. Nature 407:636-42
133. Hannum LG, Haberman AM, Anderson SM, Shlomchik MJ. 2000. Germinal center initiation, variable gene region hypermutation, and mutant B cell selection without detectable immune complexes on follicular dendritic cells. J. Exp. Med. 192:931-42
134. Haberman AM, Shlomchik MJ. 2003. Reassessing the function of immune-complex retention by follicular dendritic cells. Nat. Rev. Immunol. 3:757-64
135. Clybouw C, Fischer S, Auffredou MT, Hugues P, Alexia C, et al. 2011. Regulation of memory B-cell survival by the BH3-only protein Puma. Blood 118:4120-28
136. Vikstrom I, Carotta S, Luthje K, Peperzak V, Jost PJ, et al. 2010. Mcl-1 is essential for germinal center formation and B cell memory. Science 330:1095-99
137. Carrington EM, Vikstrom IB, Light A, Sutherland RM, Londrigan SL, et al. 2010. BH3 mimetics antagonizing restricted prosurvival Bcl-2 proteins represent another class of selective immune modulatory drugs. PNAS 107:10967-71
138. Shen P, Fillatreau S. 2015. Antibody-independent functions of B cells: a focus on cytokines. Nat. Rev. Immunol. 15:441-51
139. Amanna I, Slifka M. 2006. Quantitation of rare memory B cell populations by two independent and complementary approaches. J. Immunol. Methods 317:175-85
140. Bachmann M, Kundig T, Kalberer C, Hengartner H, Zinkernagel R. 1994. How many specific B cells are needed to protect against a virus? J. Immunol. 152:4235-41
141. Lalor PA, Nossal GJ, Sanderson RD, McHeyzer-Williams MG. 1992. Functional and molecular characterization of single, (4-hydroxy-3-nitrophenyl)acetyl (NP)-specific, IgG1 + B cells from antibodysecreting and memory B cell pathways in the C57BL/6 immune response to NP. Eur. J. Immunol. 22:3001-11
142. Li X, Vanitha D, Joo H, He Y, Rouse B, Sangster M. 2006. A strategy for selective, CD4+ T cellindependent activation of virus-specificmemory B cells for limiting dilution analysis. J. Immunol. Methods 313:110-18
143. Slifka M, Ahmed R. 1996. Limiting dilution analysis of virus-specific memory B cells by an ELISPOT assay. J. Immunol. Methods 199:37-46
144. Vanitha D, Joo H, Rouse B, Sangster M. 2007. Quantitative analysis of herpes simplex virus type 1-specific memory B cells generated by different routes of infection. Virology 360:136-42
145. Weiss U, Rajewsky K. 1990. The repertoire of somatic antibody mutants accumulating in the memory compartment after primary immunization is restricted through affinity maturation and mirrors that expressed in the secondary response. J. Exp. Med. 172:1681-89
146. Helmreich E, Kern M, Eisen H. 1961. The secretion of antibody by isolated lymph node cells. J. Biol. Chem. 236:464-73
147. Vieira P, Rajewsky K. 1988. The half-lives of serum immunoglobulins in adult mice. Eur. J. Immunol. 18:313-16
148. Tarlinton D, Good-Jacobson K. 2013. Diversity among memory B cells: origin, consequences, and utility. Science 341:1205-11
149. Good-Jacobson KL. 2014. Regulation of germinal center, B-cell memory, and plasma cell formation by histone modifiers. Front. Immunol. 5:596
150. Wienands J, Engels N. 2016. Control of memory B cell responses by extrinsic and intrinsic mechanisms. Immunol. Lett. 178:27-30
151. Engels N, Konig LM, Heemann C, Lutz J, Tsubata T, et al. 2009. Recruitment of the cytoplasmic adaptor Grb2 to surface IgG and IgE provides antigen receptor-intrinsic costimulation to class-switched B cells. Nat. Immunol. 10:1018-25
152. Engels N, Konig LM, Schulze W, Radtke D, Vanshylla K, et al. 2014. The immunoglobulin tail tyrosine motif upgrades memory-type BCRs by incorporating a Grb2-Btk signalling module. Nat. Commun. 5:5456
153. Ackermann JA, Radtke D, Maurberger A, Winkler TH, Nitschke L. 2011. Grb2 regulates B-cell maturation, B-cell memory responses and inhibits B-cell Ca2+ signalling. EMBO J. 30:1621-33
154. Hikida M, Casola S, Takahashi N, Kaji T, Takemori T, et al. 2009. PLC-γ2 is essential for formation and maintenance of memory B cells. J. Exp. Med. 206:681-89
155. Wakabayashi C, Adachi T, Wienands J, Tsubata T. 2002. A distinct signaling pathway used by the IgG-containing B cell antigen receptor. Science 298:2392-95
156. Waisman A, Kraus M, Seagal J, Ghosh S, Melamed D, et al. 2007. IgG1 B cell receptor signaling is inhibited by CD22 and promotes the development of B cells whose survival is less dependent on Iga/β. J. Exp. Med. 204:747-58
157. Shi Y, Agematsu K, Ochs HD, Sugane K. 2003. Functional analysis of human memory B-cell subpopulations: IgD+CD27+ B cells are crucial in secondary immune response by producing high affinity IgM. Clin. Immunol. 108:128-37
158. Hobeika E, Maity PC, Jumaa H. 2016. Control of B cell responsiveness by isotype and structural elements of the antigen receptor. Trends Immunol. 37:310-20
159. Ubelhart R, Hug E, Bach MP, Wossning T, Duhren-von Minden M, et al. 2015. Responsiveness of B cells is regulated by the hinge region of IgD. Nat. Immunol. 16:534-43
160. Cumano A, Rajewsky K. 1986. Clonal recruitment and somatic mutation in the generation of immunological memory to the hapten NP. EMBO J. 5:2459-68
161. Chen Z, Koralov SB, Gendelman M, Carroll MC, Kelsoe G. 2000. Humoral immune responses in Cr2-/-mice: enhanced affinity maturation but impaired antibody persistence. J. Immunol. 164:4522-32
162. Zotos D, Coquet JM, Zhang Y, Light A, D'Costa K, et al. 2010. IL-21 regulates germinal center B cell differentiation and proliferation through a B cell-intrinsic mechanism. J. Exp. Med. 207:365-78
163. Good-Jacobson KL, Szumilas CG, Chen L, Sharpe AH, Tomayko MM, Shlomchik MJ. 2010. PD-1 regulates germinal center B cell survival and the formation and affinity of long-lived plasma cells. Nat. Immunol. 11:535-42
164. Racine R, Jones DD, Chatterjee M, McLaughlin M, MacNamara KC, Winslow GM. 2010. Impaired germinal center responses and suppression of local IgG production during intracellular bacterial infection. J. Immunol. 184:5085-93
165. Yates JL, Racine R, McBride KM, Winslow GM. 2013.Tcell-dependent IgM memory B cells generated during bacterial infection are required for IgG responses to antigen challenge. J. Immunol. 191:1240-49
166. Haniuda K, Nojima T, Ohyama K, Kitamura D. 2011. Tolerance induction of IgG+ memory B cells by T cell-independent type II antigens. J. Immunol. 186:5620-28
167. Hebeis BJ, Klenovsek K, Rohwer P, Ritter U, Schneider A, et al. 2004. Activation of virus-specific memory B cells in the absence of T cell help. J. Exp. Med. 199:593-602
168. Koch G, Osmond DG, Julius MH, Benner R. 1981. The mechanism of thymus-dependent antibody formation in bone marrow. J. Immunol. 126:1447-51
169. Shepherd D, Noelle R. 1991. The lack of memory B cells in immune bone marrow. Transplantation 52:97-100
170. Slifka M, Antia R, Whitmire J, Ahmed R. 1998. Humoral immunity due to long-lived plasma cells. Immunity 8:363-72
171. Ochsenbein A, Pinschewer D, Sierro S, Horvath E, Hengartner H, Zinkernagel R. 2000. Protective longterm antibody memory by antigen-driven and T help-dependent differentiation of long-lived memory B cells to short-lived plasma cells independent of secondary lymphoid organs. PNAS 97:13263-68
172. Cinamon G, Matloubian M, Lesneski M, Xu Y, Low C, et al. 2004. Sphingosine 1-phosphate receptor 1 promotes B cell localization in the splenic marginal zone. Nat. Immunol. 5:713-20
173. Forster R, Mattis A, Kremmer E, Wolf E, Brem G, Lipp M. 1996. A putative chemokine receptor, BLR1, directs B cell migration to defined lymphoid organs and specific anatomic compartments of the spleen. Cell 87:1037-47
174. Onodera T, Hosono A, Odagiri T, Tashiro M, Kaminogawa S, et al. 2016. Whole-virion influenza vaccine recalls an early burst of high-affinity memory B cell response throughTLR signaling. J. Immunol. 196:4172-84
175. Boeckh M, Nichols W, Papanicolaou G, Rubin R, Wingard J, Zaia J. 2003. Cytomegalovirus in hematopoietic stem cell transplant recipients: current status, known challenges, and future strategies. Biol. Blood Marrow Transplant. 9:543-58
176. Klenovsek K, Weisel F, Schneider A, Appelt U, Jonjic S, et al. 2007. Protection from CMV infection in immunodeficient hosts by adoptive transfer of memory B cells. Blood 110:3472-79
177. Weinberger B, Herndler-Brandstetter D, Schwanninger A, Weiskopf D, Grubeck-Loebenstein B. 2008. Biology of immune responses to vaccines in elderly persons. Clin. Infect. Dis. 46:1078-84
178. Chiu C, Ellebedy AH, Wrammert J, Ahmed R. 2015. B cell responses to influenza infection and vaccination. Curr. Top. Microbiol. Immunol. 386:381-98
179. Yu X, Tsibane T, McGraw PA, House FS, Keefer CJ, et al. 2008. Neutralizing antibodies derived from the B cells of 1918 influenza pandemic survivors. Nature 455:532-36
180. Moyron-Quiroz JE, Rangel-Moreno J, Kusser K, Hartson L, Sprague F, et al. 2004. Role of inducible bronchus associated lymphoid tissue (iBALT) in respiratory immunity. Nat. Med. 10:927-34
181. Baumgarth N, Choi YS, Rothaeusler K, Yang Y, Herzenberg LA. 2008. B cell lineage contributions to antiviral host responses. Curr. Top. Microbiol. Immunol. 319:41-61
182. Adachi Y, Onodera T, Yamada Y, Daio R, Tsuiji M, et al. 2015. Distinct germinal center selection at local sites shapes memory B cell response to viral escape. J. Exp. Med. 212:1709-23
183. Pichyangkul S, Yongvanitchit K, Limsalakpetch A, Kum-Arb U, Im-Erbsin R, et al. 2015. Tissue distribution of memory T and B cells in rhesus monkeys following influenza A infection. J. Immunol. 195:4378-86
184. Li G-M, Chiu C, Wrammert J, McCausland M, Andrews SF, et al. 2012. Pandemic H1N1 influenza vaccine induces a recall response in humans that favors broadly cross-reactive memory B cells. PNAS 109:9047-52
185. Andrews SF, Huang Y, Kaur K, Popova LI, Ho IY, et al. 2015. Immune history profoundly affects broadly protective B cell responses to influenza. Sci. Transl. Med. 7:316ra192
186. Li Y, Myers JL, Bostick DL, Sullivan CB, Madara J, et al. 2013. Immune history shapes specificity of pandemic H1N1 influenza antibody responses. J. Exp. Med. 210:1493-500
187. Neu KE, Henry Dunand CJ, Wilson PC. 2016. Heads, stalks and everything else: How can antibodies eradicate influenza as a human disease? Curr. Opin. Immunol. 42:48-55
188. Moir S, Fauci AS. 2009. B cells in HIV infection and disease. Nat. Rev. Immunol. 9:235-45
189. Kwong PD, Mascola JR. 2012. Human antibodies that neutralize HIV-1: identification, structures, and B cell ontogenies. Immunity 37:412-25
190. Wu X, Zhou T, Zhu J, Zhang B, Georgiev I, et al. 2011. Focused evolution of HIV-1 neutralizing antibodies revealed by structures and deep sequencing. Science 333:1593-602
191. Lynch RM, Tran L, Louder MK, Schmidt SD, Cohen M, et al. 2012. The development of CD4 binding site antibodies during HIV-1 infection. J. Virol. 86:7588-95
192. Klein F, Mouquet H, Dosenovic P, Scheid JF, Scharf L, Nussenzweig MC. 2013. Antibodies in HIV-1 vaccine development and therapy. Science 341:1199-204
193. Mouquet H, Nussenzweig MC. 2013. HIV: roadmaps to a vaccine. Nature 496:441-42