Marginal zone B cells

Annual Review of Immunology

Volumn 23, Issue , 2005, Pages 161-196

  Pillai, Shiv ^a   Cariappa, Annaiah ^a   Moran, Stewart T ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

B cell receptor; Follicular B cells; Notch2; Transitional B cells

Indexed keywords

B LYMPHOCYTE RECEPTOR; NOTCH RECEPTOR; NOTCH2 RECEPTOR; UNCLASSIFIED DRUG;

AUTOIMMUNE DISEASE; B LYMPHOCYTE; B LYMPHOCYTE DIFFERENTIATION; CELL LINE; CYTOARCHITECTURE; HOST RESISTANCE; HUMAN; IMMUNE RESPONSE; IMMUNOLOGY; INNATE IMMUNITY; LYMPHOCYTE FUNCTION; LYMPHOID ORGAN; MARGINAL ZONE B LYMPHOCYTE; MUCOSA ASSOCIATED LYMPHOID TISSUE LYMPHOMA; NONHUMAN; PHENOTYPE; PRIMATE; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; SPLEEN;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; B-LYMPHOCYTE SUBSETS; CELL DIFFERENTIATION; IMMUNITY, NATURAL; MICE; MICROCIRCULATION; MODELS, IMMUNOLOGICAL; RECEPTORS, ANTIGEN, B-CELL; SIGNAL TRANSDUCTION; SPLEEN;

EID: 12344273628     PISSN: 07320582     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.immunol.23.021704.115728     Document Type: Review

References (158)

1. Weidenreich F. 1901. Das Gefasssystem der menschlichen Milz. Arch. Mikrosk. Anat. 58:247-376
2. MacNeal WJ. 1929. The circulation of blood through the spleen pulp. Arch. Pathol. 7:215-27
3. Rraal G. 1992. Cells in the marginal zone of the spleen. Int. Rev. Cytol. 132:31-74
4. Spencer J, Perry ME, Dunn-Walters DK. 1998. Human marginal-zone B cells. Immunol. Today 19:421-26
5. Martin F, Kearney JF. 2002. Marginal-zone B cells. Nat. Rev. Immunol. 2:323-35
6. Zandvoort A, Timens W. 2002. The dual function of the splenic marginal zone: essential for initiation of anti-TI-2 responses but also vital in the general first-line defense against blood-borne antigens. Clin. Exp. Immunol. 130:4-11
7. Hardy RR, Hayakawa K. 2001. B cell development pathways. Annu. Rev. Immunol. 19:595-621
8. Martin F, Kearney JF. 2000. B-cell subsets and the mature preimmune repertoire. Marginal zone and B1 B cells as part of a "natural immune memory.? Immunol. Rev. 175:70-79
9. Cariappa A, Pillai S. 2002. Antigen-dependent B-cell development. Curr. Opin. Immunol. 14:241-49
10. Pillai S, Cariappa A, Moran ST. 2004. Positive selection and lineage commitment during peripheral B-lymphocyte development. Immunol. Rev. 197:206-18
11. Snook T. 1964. Studies on the perifollicular region of the rat's spleen. Anat. Rec. 148:149-59
12. Yamamoto K, Kobayashi T, Murakami T. 1982. Arterial terminals in the rat spleen as demonstrated by scanning electron microscopy of vascular casts. Scan. Electron Microsc. 1982:455-58
13. Schmidt EE, MacDonald IC, Groom AC. 1993. Comparative aspects of splenic microcirculatory pathways in mammals: the region bordering the white pulp. Scan. Microsc. 7:613-28
14. 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
15. Steiniger B, Barth P, Hellinger A. 2001. The perifollicular and marginal zones of the human splenic white pulp: Do fibroblasts guide lymphocyte immigration? Am. J. Pathol. 159:501-12
16. Steiniger B, Ruttinger L, Barth PJ. 2003. The three-dimensional structure of human splenic white pulp compartments. J. Histochem. Cytochem. 51:655-64
17. -/- donors to wild-type hosts: implications for the generation of architectural events in lymphoid B cell domains. J. Immunol. 161:3836-43
18. Fu YX, Chaplin DD. 1999. Development and maturation of secondary lymphoid tissues. Annu. Rev. Immunol. 17:399-433
19. Ettinger R, Munson SH, Chao CC, Vadeboncoeur M, Toma J, McDevitt HO. 2001. A critical role for lymphotoxin-β receptor in the development of diabetes in nonobese diabetic mice. J. Exp. Med. 193:1333-40
20. Shinkura R, Kitada K, Matsuda F, Tashiro K, Ikuta K, et al. 1999. Alymphoplasia is caused by a point mutation in the mouse gene encoding NF-κB-inducing kinase. Nat. Genet. 22:74-77
21. Yin L, Wu L, Wesche H, Arthur CD, White JM, et al. 2001. Defective lymphotoxin-β receptor-induced NF-κB transcriptional activity in NIK-deficient mice. Science 291:2162-65
22. Senftleben U, Cao Y, Xiao G, Greten FR, Krahn G, et al. 2001. Activation by IKKα of a second, evolutionary conserved, NF-κB signaling pathway. Science 293:1495-99
23. Matsushima A, Kaisho T, Rennert PD, Nakano H, Kurosawa K, et al. 2001. Essential role of nuclear factor (NF)-κB-inducing kinase and inhibitor of κB (IκB) kinase α in NF-κB activation through lymphotoxin β receptor, but not through tumor necrosis factor receptor I. J. Exp. Med. 193:631-36
24. Banks TA, Rouse BT, Kerley MK, Blair PJ, Godfrey VL, et al. 1995. Lymphotoxin-α-deficient mice. Effects on secondary lymphoid organ development and humoral immune responsiveness. J. Immunol. 155:1685-93
25. De Togni P, Goellner J, Ruddle NH, Streeter PR, Pick A, et al. 1994. Abnormal development of peripheral lymphoid organs in mice deficient in lymphotoxin. Science 264:703-7
26. Metlay JP, Witmer-Pack MD, Agger R, Crowley MT, Lawless D, Steinman RM. 1990. The distinct leukocyte integrins of mouse spleen dendritic cells as identified with new hamster monoclonal antibodies. J. Exp. Med. 171:1753-71
27. Leenen PJ, Radosevic K, Voerman JS, Salomon B, van Rooijen N, et al. 1998. Heterogeneity of mouse spleen dendritic cells: in vivo phagocytic activity, expression of macrophage markers, and subpopulation turnover. J. Immunol. 160:2166-73
28. Balazs M, Martin F, Zhou T, Kearney J. 2002. Blood dendritic cells interact with splenic marginal zone B cells to initiate T-independent immune responses. Immunity 17:341-52
29. Kraal G, Janse M. 1986. Marginal metallophilic cells of the mouse spleen identified by a monoclonal antibody. Immunology 58:665-69
30. Dijkstra CD, Van Vliet E, Dopp EA, van der Lelij AA, Kraal G. 1985. Marginal zone macrophages identified by a monoclonal antibody: characterization of immuno- and enzyme-histochemical properties and functional capacities. Immunology 55:23-30
31. Elomaa O, Kangas M, Sahlberg C, Tuukkanen J, Sormunen R, et al. 1995. Cloning of a novel bacteria-binding receptor structurally related to scavenger receptors and expressed in a subset of macrophages. Cell 80:603-9
32. Humphrey JH, Grennan D. 1981. Different macrophage populations distinguished by means of fluorescent polysaccharides. Recognition and properties of marginal-zone macrophages. Eur. J. Immunol. 11:221-28
33. Karlsson MC, Guinamard R, Holland S, Sankala M, Steinman RM, Ravetch JV. 2003. Macrophages control the retention and trafficking of B lymphocytes in the splenic marginal zone. J. Exp. Med. 198:333-40
34. Goldschneider I, McGregor DD. 1973. Anatomical distribution of T and B lymphocytes in the rat. Development of lymphocyte-specific antisera. J. Exp. Med. 138:1443-65
35. MacLennan IC. 1982. Lymphocytes of splenic marginal zons: a distinct B-cell lineage. Immunol. Today 3:305-7
36. Gray D, MacLennan IC, Bazin H, Khan M. 1982. Migrant mu+ delta+ and static mu+ delta- B lymphocyte subsets. Eur. J. Immunol. 12:564-69
37. Gray D, McConnell I, Kumararatne DS, MacLennan IC, Humphrey JH, Bazin H. 1984. Marginal zone B cells express CR1 and CR2 receptors. Eur. J. Immunol. 14:47-52
38. Takahashi K, Kozono Y, Waldschmidt TJ, Berthiaume D, Quigg RJ, et al. 1997. Mouse complement receptors type 1 (CR1;CD35) and type 2 (CR2;CD21): expression on normal B cell subpopulations and decreased levels during the development of autoimmunity in MRL/lpr mice. J. Immunol. 159:1557-69
39. Oliver AM, Martin F, Gartland GL, Carter RH, Kearney JF. 1997. Marginal zone B cells exhibit unique activation, proliferative and immunoglobulin secretory responses. Eur. J. Immunol. 27:2366-74
40. high lymphocytes enriched in the splenic marginal zone generate effector cells more rapidly than the bulk of follicular B cells. J. Immunol. 162:7198-207
41. Waldschmidt TJ, Kroese FG, Tygrett LT, Conrad DH, Lynch RG. 1991. The expression of B cell surface receptors. III. The murine low-affinity IgE Fc receptor is not expressed on Ly 1 or 'Ly 1-like' B cells. Int. Immunol. 3:305-15
42. Hsu SM. 1985. Phenotypic expression of B lymphocytes. III. Marginal zone B cells in the spleen are characterized by the expression of Tac and alkaline phosphatase. J. Immunol. 135:123-30
43. Lu TT, Cyster JG. 2002. Integrin-mediated long-term B cell retention in the splenic marginal zone. Science 297:409-12
44. Hao Z, Rajewsky K. 2001. Homeostasis of peripheral B cells in the absence of B cell influx from the bone marrow. J. Exp. Med. 194:1151-64
45. Kumararatne DS, Gagnon RF, Smart Y. 1980. Selective loss of large lymphocytes from the marginal zone of the white pulp in rat spleens following a single dose of cyclophosphamide. A study using quantitative histological methods. Immunology 40:123-31
46. Lortan J, Gray D, Kumararatne DS, Platteau B, Bazin H. MacLennan IC. 1985. Regulation of the size of the recirculating B cell pool of adult rats. Adv. Exp. Med. Biol. 186:593-601
47. Timens W, Boes A, Rozeboom-Uiterwijk T, Poppema S. 1989. Immaturity of the human splenic marginal zone in infancy. Possible contribution to the deficient infant immune response. J. Immunol. 143:3200-6
48. Kruschinski C, Zidan M, Debertin AS, von Horsten S, Pabst R. 2004. Age-dependent development of the splenic marginal zone in human infants is associated with different causes of death. Hum. Pathol. 35:113-21
49. hi and exhibit unique signaling characteristics. J. Immunol. 149:2533-40
50. hi splenic B cells are an immature developmental intermediate in the production of long-lived marrow-derived B cells. J. Immunol. 151:4431-44
51. Allman D, Lindsley RC, DeMuth W, Rudd K, Shinton SA, Hardy RR. 2001. Resolution of three nonproliferative immature splenic B cell subsets reveals multiple selection points during peripheral B cell maturation. J. Immunol. 167:6834-40
52. Schiemann B, Gommerman JL, Vora K, Cachero TG, Shulga-Morskaya S, et al. 2001. An essential role for BAFF in the normal development of B cells through a BCMA-independent pathway. Science 293:2111-14
53. Thompson JS, Bixler SA, Qian F, Vora K, Scott ML, et al. 2001. BAFF-R, a newly identified TNF receptor that specifically interacts with BAFF. Science 293:2108-11
54. Schneider P, Takatsuka H, Wilson A, Mackay F, Tardivel A, et al. 2001. Maturation of marginal zone and follicular B cells requires B cell activating factor of the tumor necrosis factor family and is independent of B cell maturation antigen. J. Exp. Med. 194:1691-97
55. Lam KP, Kuhn R, Rajewsky K. 1997. In vivo ablation of surface immunoglobulin on mature B cells by inducible gene targeting results in rapid cell death. Cell 90:1073-83
56. Kraus M, Alimzhanov MB, Rajewsky N, Rajewsky K. 2004. Survival of resting mature B lymphocytes depends on BCR signaling via the Igα/β heterodimer. Cell 117:787-800
57. Forster R, Mattis AE, 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
58. Reif K, Ekland EH, Ohl L, Nakano H, Lipp M, et al. 2002. Balanced responsiveness to chemoattractants from adjacent zones determines B-cell position. Nature 416:94-99
59. Cariappa A, Tang M, Parng C, Nebelitskiy E, Carroll M, et al. 2001. The follicular versus marginal zone B lymphocyte cell fate decision is regulated by Aiolos, Btk, and CD21. Immunity 14:603-15
60. Saito T, Chiba S, Ichikawa M, Kunisato A, Asai T, et al. 2003. Notch2 is preferentially expressed in mature B cells and indispensable for marginal zone B lineage development. Immunity 18:675-85
61. Loder F, Mutschler B, Ray RJ, Paige CJ, Sideras P, et al. 1999. B cell development in the spleen takes place in discrete steps and is determined by the quality of B cell receptor-derived signals. J. Exp. Med. 190:75-89
62. Hardy RR, Hayakawa K, Parks DR, Herzenberg LA. 1983. Demonstration of B-cell maturation in X-linked immunodeficient mice by simultaneous three-colour immunofluorescence. Nature 306:270-72
63. Khan WN, Alt FW, Gerstein RM, Malynn BA, Larsson I, et al. 1995. Defective B cell development and function in Btk-deficient mice. Immunity 3:283-99
64. Kerner JD, Appleby MW, Mohr RN, Chien S, Rawlings DJ, et al. 1995. Impaired expansion of mouse B cell progenitors lacking Btk. Immunity 3:301-12
65. Cariappa A, Kim TJ, Pillai S. 1999. Accelerated emigration of B lymphocytes in the Xid mouse. J. Immunol. 162:4417-23
66. + thymocytes, and B cell maturation. J. Exp. Med. 183:1707-18
67. Yamazaki T, Takeda K, Gotoh K, Takeshima H, Akira S, Kurosaki T. 2002. Essential immunoregulatory role for BCAP in B cell development and function. J. Exp. Med. 195:535-45
68. Fruman DA, Snapper SB, Yballe CM, Davidson L, Yu JY, et al. 1999. Impaired B cell development and proliferation in absence of phosphoinositide 3-kinase p85α. Science 283:393-97
69. Suzuki H, Terauchi Y, Fujiwara M, Aizawa S, Yazaki Y, et al. 1999. Xid-like immunodeficiency in mice with disruption of the p85α subunit of phosphoinositide 3-kinase. Science 283:390-92
70. Jumaa H, Wollscheid B, Mitterer M, Wienands J, Reth M, Nielsen PJ. 1999. Abnormal development and function of B lymphocytes in mice deficient for the signaling adaptor protein SLP-65. Immunity 11:547-54
71. Pappu R, Cheng AM, Li B, Gong Q, Chiu C, et al. 1999. Requirement for B cell linker protein (BLNK) in B cell development. Science 286:1949-54
72. Wang D, Feng J, Wen R, Marine JC, Sangster MY, et al. 2000, Phospholipase Cγ 2 is essential in the functions of B cell and several Fc receptors. Immunity 13:25-35
73. Wardemann H, Yurasov S, Schaefer A, Young JW, Meffre E, Nussenzweig MC. 2003. Predominant autoantibody production by early human B cell precursors. Science 301:1374-77
74. Rolink AG, Andersson J, Melchers F. 1998. Characterization of immature B cells by a novel monoclonal antibody, by turnover and by mitogen reactivity. Eur. J. Immunol. 28:3738-48
75. Hsu BL, Harless SM, Lindsley RC, Hubert DM, Cancro MP. 2002. Cutting edge: BLyS enables survival of transitional and mature B cells through distinct mediators. J. Immunol. 168:5993-96
76. Lesley R, Xu Y, Kalled SL, Hess DM, Schwab SR, et al. 2004. Reduced competitiveness of autoantigen-engaged B cells due to increased dependence on BAFF. Immunity 20:441-53
77. Thien M, Phan TG, Gardam S, Amesbury M, Basten A, et al. 2004. Excess BAFF rescues self-reactive B cells from peripheral deletion and allows them to enter forbidden follicular and marginal zone niches. Immunity 20:785-98
78. Neuberger MS. 1997. Antigen receptor signaling gives lymphocytes a long life. Cell 90:971-73
79. Pillai S. 1999. The chosen few? Positive selection and the generation of naive B lymphocytes. Immunity 10:493-502
80. Wang JH, Avitahl N, Cariappa A, Friedrich C, Ikeda T, et al. 1998. Aiolos regulates B cell activation and maturation to effector state. Immunity 9:543-53
81. Samardzic T, Marinkovic D, Danzer CP, Gerlach J, Nitschke L, Wirth T. 2002. Reduction of marginal zone B cells in CD22-deficient mice. Eur. J. Immunol. 32:561-67
82. Sun T, Clark MR, Storb U. 2002. A point mutation in the constant region of Ig lambda 1 prevents normal B cell development due to defective BCR signaling. Immunity 16:245-55
83. Kraus M, Pao LI, Reichlin A, Hu Y, Canono B, et al. 2001. Interference with immunoglobulin (Ig)α immunoreceptor tyrosine-based activation motif (ITAM) phosphorylation modulates or blocks B cell development, depending on the availability of an Igβ cytoplasmic tail. J. Exp. Med. 194:455-69
84. Hendriks RW, de Bruijn MF, Maas A, Dingjan GM, Karis A, Grosveld F. 1996. Inactivation of Btk by insertion of lacZ reveals defects in B cell development only past the pre-B cell stage. EMBO. J. 15:4862-72
85. Hayakawa K, Asano M, Shinton SA, Gui M, Allman D, et al. 1999. Positive selection of natural autoreactive B cells. Science 285:113-16
86. Martin F, Kearney JF. 2000. Positive selection from newly formed to marginal zone B cells depends on the rate of clonal production, CD19, and btk. Immunity 12:39-49
87. Casola S, Otipoby KL, Alimzhanov M, Humme S, Uyttersprot N, et al. 2004. B cell receptor signal strength determines B cell fate. Nat. Immunol. 5:317-27
88. Cabatingan MS, Schmidt MR, Sen R, Woodland RT. 2002. Naive B lymphocytes undergo homeostatic proliferation in response to B cell deficit. J. Immunol. 169:6795-805
89. Scher I, Sternberg AD, Berning AK, Paul WE. 1975. X-linked B-lymphocyte immune defect in CBA/N mice. II. Studies of the mechanisms underlying the immune defect. J. Exp. Med. 142:637-50
90. Anderson JS, Teutsch M, Dong Z, Wortis HH. 1996. An essential role for Bruton's [corrected] tyrosine kinase in the regulation of B-cell apoptosis. Proc. Natl. Acad. Sci. USA 93:10966-71
91. Brunner C, Marinkovic D, Klein J, Samardzic T, Nitschke L, Wirth T. 2003. B cell-specific transgenic expression of Bcl2 rescues early B lymphopoiesis but not B cell responses in BOB.1/OBF.1-deficient mice. J. Exp. Med. 197:1205-11
92. Okkenhaug K, Bilancio A, Farjot G, Priddle H, Sancho S, et al. 2002. Impaired B and T cell antigen receptor signaling in p110δ PI 3-kinase mutant mice. Science 297:1031-34
93. Clayton E, Bardi G, Bell SE, Chantry D, Downes CP, et al. 2002. A crucial role for the p110δ subunit of phosphatidylinositol 3-kinase in B cell development and activation. J. Exp. Med. 196:753-63
94. Jou ST, Carpino N, Takahashi Y, Piekorz R, Chao JR, et al. 2002. Essential, nonredundant role for the phosphoinositide 3-kinase p110δ in signaling by the B-cell receptor complex. Mol. Cell. Biol. 22:8580-91
95. Cariappa A, Liou HC, Horwitz BH, Pillai S. 2000. Nuclear factor κB is required for the development of marginal zone B lymphocytes. J. Exp. Med. 192:1175-82
96. Weih DS, Yilmaz ZB, Weih F. 2001. Essential role of RelB in germinal center and marginal zone formation and proper expression of homing chemokines. J. Immunol. 167:1909-19
97. Xue L, Morris SW, Orihuela C, Tuomanen E, Cui X, et al. 2003. Defective development and function of Bcl10-deficient follicular, marginal zone and B1 B cells. Nat. Immunol. 4:857-65
98. Ruefli-Brasse AA, French DM, Dixit VM. 2003. Regulation of NF-κB-dependent lymphocyte activation and development by paracaspase. Science 302:1581-84
99. Ruland J, Duncan GS, Wakeham A, Mak TW. 2003. Differential requirement for Malt1 in T and B cell antigen receptor signaling. Immunity 19:749-58
100. Egawa T, Albrecht B, Favier B, Sunshine MJ, Mirchandani K, et al. 2003. Requirement for CARMA1 in antigen receptor-induced NF-κB activation and lymphocyte proliferation. Curr. Biol. 13:1252-58
101. Hara H, Wada T, Bakal C, Kozieradzki I, Suzuki S, et al. 2003. The MAGUK family protein CARD11 is essential for lymphocyte activation. Immunity 18:763-75
102. Jun JE, Wilson LE, Vinuesa CG, Lesage S, Blery M, et al. 2003. Identifying the MAGUK protein Carma-1 as a central regulator of humoral immune responses and atopy by genome-wide mouse mutagenesis. Immunity 18:751-62
103. Zhou H, Wertz I, O'Rourke K, Ultsch M, Seshagiri S, et al. 2004. Bcl10 activates the NF-κB pathway through ubiquitination of NEMO. Nature 427:167-71
104. Samardzic T, Marinkovic D, Nielsen PJ, Nitschke L, Wirth T. 2002. BOB.1/OBF.1 deficiency affects marginal-zone B-cell compartment. Mol. Cell. Biol. 22:8320-31
105. Morgan TH. 1917. The theory of the gene. Am. Nat. 51:513-44
106. Radtke F, Wilson A, Mancini SJ, MacDonald HR. 2004. Notch regulation of lymphocyte development and function. Nat. Immunol. 5:247-53
107. Wu L, Sun T, Kobayashi K, Gao P, Griffin JD. 2002. Identification of a family of mastermind-like transcriptional coactivators for mammalian notch receptors. Mol. Cell. Biol. 22:7688-700
108. Tanigaki K, Han H, Yamamoto N, Tashiro K, Ikegawa M, et al. 2002. Notch-RBP-J signaling is involved in cell fate determination of marginal zone B cells. Nat. Immunol 3:443-50
109. Hozumi K, Negishi N, Suzuki D, Abe N, Sotomaru Y, et al. 2004. Delta-like 1 is necessary for the generation of marginal zone B cells but not T cells in vivo. Nat. Immunol. 5:638-44
110. Witt CM, Won WJ, Hurez V, Klug CA. 2003. Notch2 haploinsufficiency results in diminished B1 B cells and a severe reduction in marginal zone B cells. J. Immunol. 171:2783-88
111. Kuroda K, Han H, Tani S, Tanigaki K, Tun T, et al. 2003. Regulation of marginal zone B cell development by MINT, a suppressor of Notch/RBP-J signaling pathway. Immunity 18:301-12
112. Maillard I, Weng AP, Carpenter AC, Rodriguez CG, Sai H, et al. 2004. Mastermind critically regulates Notch-mediated lymphoid cell fate decisions. Blood 104:1696-702
113. Mackay F, Woodcock SA, Lawton P, Ambrose C, Baetscher M, et al. 1999. Mice transgenic for B AFF develop lymphocytic disorders along with autoimmune manifestations. J. Exp. Med. 190:1697-710
114. Khare SD, Sarosi I, Xia XZ, McCabe S, Miner K, et al. 2000. Severe B cell hyperplasia and autoimmune disease in TALL-1 transgenic mice. Proc. Natl. Acad. Sci. USA 97:3370-75
115. Loset GA, Roux KH, Zhu P, Michaelsen TE, Sandlie I. 2004. Differential segmental flexibility and reach dictate the antigen binding mode of chimeric IgD and IgM: implications for the function of the B cell receptor. J. Immunol. 172:2925-34
116. Agenes F, Freitas AA. 1999. Transfer of small resting B cells into immunodeficient hosts results in the selection of a self-renewing activated B cell population. J. Exp. Med. 189:319-30
117. Agenes F, Rosado MM, Freitas AA. 2000. Considerations on B cell homeostasis. Curr. Top. Microbiol. Immunol. 252:68-75
118. Dammers PM, de Boer NK, Deenen GJ, Nieuwenhuis P, Kroese FG. 1999. The origin of marginal zone B cells in the rat. Eur. J. Immunol. 29:1522-31
119. Lo CG, Lu TT, Cyster JG. 2003. Integrin-dependence of lymphocyte entry into the splenic white pulp. J. Exp. Med. 197:353-61
120. Cinamon G, Matloubian M, Lesneski MJ, 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
121. Dalwadi H, Wei B, Schrage M, Su TT, Rawlings DJ, Braun J. 2003. B cell developmental requirement for the Gαi2 gene. J. Immunol. 170:1707-15
122. Guinamard R, Okigaki M, Schlessinger J, Ravetch JV. 2000. Absence of marginal zone B cells in Pyk-2-deficient mice defines their role in the humoral response. Nat. Immunol. 1:31-36
123. Girkontaite I, Missy K, Sakk V, Harenberg A, Tedford K, et al. 2001. Lsc is required for marginal zone B cells, regulation of lymphocyte motility and immune responses. Nat. Immunol. 2:855-62
124. Fukui Y, Hashimoto O, Sanui T, Oono T, Koga H, et al. 2001. Haematopoietic cell-specific CDM family protein DOCK2 is essential for lymphocyte migration. Nature 412:826-31
125. Sanui T, Inayoshi A, Noda M, Iwata E, Stein JV, et al. 2003. DOCK2 regulates Rac activation and cytoskeletal reorganization through interaction with ELMO1. Blood 102:2948-50
126. Croker BA, Tarlinton DM, Cluse LA, Tuxen AJ, Light A, et al. 2002. The Rac2 guanosine triphosphatase regulates B lymphocyte antigen receptor responses and chemotaxis and is required for establishment of B-1a and marginal zone B lymphocytes. J. Immunol. 168:3376-86
127. Coil JA, Dickerman JD, Boulton E. 1978. Increased susceptibility of splenectomized mice to infection after exposure to an aerosolized suspension of type III Streptococcus pneumoniae. Infect. Immun. 21:412-16
128. Amlot PL, Grennan D, Humphrey JH. 1985. Splenic dependence of the antibody response to thymus-independent (TI-2) antigens. Eur. J. Immunol. 15:508-12
129. Harms G, Hardonk MJ, Timens W. 1996. In vitro complement-dependent binding and in vivo kinetics of pneumococcal polysaccharide TI-2 antigens in the rat spleen marginal zone and follicle. Infect. Immun. 64:4220-25
130. Mond JJ, Lees A, Snapper CM. 1995. T cell-independent antigens type 2. Annu. Rev. Immunol. 13:655-92
131. Likhite VV. 1976. Immunological impairment and susceptibility to infection after splenectomy. JAMA 236:1376-77
132. Holdsworth RJ, Irving AD, Cuschieri A. 1991. Postsplenectomy sepsis and its mortality rate: actual versus perceived risks. Br. J. Surg. 78:1031-38
133. Cowan MJ, Ammann AJ, Wara DW, Howie VM, Schultz L, et al. 1978. Pneumococcal polysaccharide immunization in infants and children. Pediatrics 62:721-27
134. Totapally BR, Walsh WT. 1998. Pneumococcal bacteremia in childhood: a 6-year experience in a community hospital. Chest 113:1207-14
135. Sha WC, Liou HC, Tuomanen EI, Baltimore D. 1995. Targeted disruption of the p50 subunit of NF-κB leads to multifocal defects in immune responses. Cell 80:321-30
136. Martin F, Oliver AM, Kearney JF. 2001. Marginal zone and B1 B cells unite in the early response against T-independent blood-borne particulate antigens. Immunity 14:617-29
137. Colino J, Shen Y, Snapper CM. 2002. Dendritic cells pulsed with intact Streptococcus pneumoniae elicit both protein-and polysaccharide-specific immunoglobulin isotype responses in vivo through distinct mechanisms. J. Exp. Med. 195:1-13
138. Mackay F, Ambrose C. 2003. The TNF family members BAFF and APRIL: the growing complexity. Cytokine Growth Factor Rev. 14:311-24
139. O'Connor BP, Raman VS, Erickson LD, Cook WJ, Weaver LK, et al. 2004. BCMA is essential for the survival of long-lived bone marrow plasma cells. J. Exp. Med. 199:91-98
140. Attanavanich K, Kearney JF. 2004. Marginal zone, but not follicular B cells, are potent activators of naive CD4 T cells. J. Immunol. 172:803-11
141. MacLennan IC, Toellner KM, Cunningham AF, Serre K, Sze DM, et al. 2003. Extrafollicular antibody responses. Immunol. Rev. 194:8-18
142. William J, Euler C, Christensen S, Shlomchik MJ. 2002. Evolution of autoantibody responses via somatic hypermutation outside of germinal centers. Science 297:2066-70
143. 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
144. Weller S, Braun MC, Tan BK, Rosenwald A, Cordier C, et al. 2004. Human blood IgM "memory" B cells are circulating splenic marginal zone B cells harboring a pre-diversified immunoglobulin repertoire. Blood. 104:3647-54
145. + peripheral blood B cells expressing the CD27 cell surface antigen carry somatically mutated variable region genes: CD27 as a general marker for somatically mutated (memory) B cells. J. Exp. Med. 188:1679-89
146. 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
147. Kruetzmann S, Rosado MM, Weber H, Germing U, Tournilhac O, et al. 2003. Human immunoglobulin M memory B cells controlling Streptococcus pneumoniae infections are generated in the spleen. J. Exp. Med. 197:939-45
148. Weller S, Faili A, Garcia C, Braun MC, Le Deist FF, et al. 2001. CD40-CD40L independent Ig gene hypermutation suggests a second B cell diversification pathway in humans. Proc. Natl. Acad. Sci. USA 98:1166-70
149. Bernasconi NL, Traggiai E, Lanzavecchia A. 2002. Maintenance of serological memory by polyclonal activation of human memory B cells. Science 298:2199-202
150. Li Y, Li H, Weigert M. 2002. Autoreactive B cells in the marginal zone that express dual receptors. J. Exp. Med. 195:181-88
151. Segundo C, Rodriguez C, Garcia-Poley A, Aguilar M, Gavilan I, et al. 2001. Thyroid-infiltrating B lymphocytes in Graves' disease are related to marginal zone and memory B cell compartments. Thyroid 11:525-30
152. Groom J, Kalled SL, Cutler AH, Olson C, Woodcock SA, et al. 2002. Association of BAFF/BLyS overexpression and altered B cell differentiation with Sjogren's syndrome. J. Clin. Invest. 109:59-68
153. Harris NL. 1999. Lymphoid proliferations of the salivary glands. Am. J. Clin. Pathol. 111:S94-103
154. + marginal zone B-cell compartment. Br. J. Haematol. 116:662-66
155. Fredrickson TN, Lennert K, Chattopadhyay SK, Morse HC 3rd, Hartley JW. 1999. Splenic marginal zone lymphomas of mice. Am. J. Pathol. 154:805-12
156. Cavalli F, Isaacson PG, Gascoyne RD, Zucca E. 2001. MALT lymphomas. Hematology (Am. Soc. Hematol Educ. Program) 2001:241-58
157. Quong MW, Martensson A, Langerak AW, Rivera RR, Nemazee D, Murre C. 2004. Receptor editing and marginal zone B cell development are regulated by the helix-loop-helix protein, E2A. J. Exp. Med. 199:1101-12
158. Becker-Herman S, Lantner F, Shachar I. 2002. Id2 negatively regulates B cell differentiation in the spleen. J. Immunol. 168:5507-13