Homing of antibody secreting cells

Immunological Reviews

Volumn 194, Issue , 2003, Pages 48-60

  Cyster, Jason G ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; CHEMOKINE RECEPTOR; CHEMOKINE RECEPTOR CCR10; CHEMOKINE RECEPTOR CCR9; CHEMOKINE RECEPTOR CXCR4; IMMUNOGLOBULIN; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; INTEGRIN; LECTIN; STROMAL CELL DERIVED FACTOR 1; UNCLASSIFIED DRUG;

ANTIBODY PRODUCTION; B LYMPHOCYTE; BONE MARROW; CELL DIFFERENTIATION; CELL FUNCTION; CELL MIGRATION; CELL SECRETION; CELLULAR DISTRIBUTION; CIRCULATION; EFFECTOR CELL; EPITHELIUM; IMMUNOGLOBULIN PRODUCTION; LYMPHOID ORGAN; MUCOSA; PLASMA CELL; PRIORITY JOURNAL; REVIEW; TRANSCYTOSIS;

ANIMALS; ANTIBODIES; B-LYMPHOCYTES; CELL ADHESION MOLECULES; CELL MOVEMENT; HUMANS; IMMUNE SYSTEM; RECEPTORS, CHEMOKINE;

EID: 0037660968     PISSN: 01052896     EISSN: None     Source Type: Journal    
DOI: 10.1034/j.1600-065X.2003.00041.x     Document Type: Review

References (118)

1. Chaperon EA, Selner JC, Claman HN. Migration of antibody-forming cells and antigen-sensitive precursors between spleen, thymus and bone marrow. Immunology 1968;14:553-561.
2. Rudzik O, Perey DY, Bienenstock J. Differential IgA repopulation after transfer of autologous and allogeneic rabbit Peyer's patch cells. J Immunol 1975;114:40-44.
3. Benner R, van Oudenaren A, de Ruiter H. Antibody formation in mouse bone marrow. IX. Peripheral lymphoid organs are involved in the initiation of bone marrow antibody formation. Cell Immunol 1977;34:125-137.
4. van Rooijen N, Kors N, Van Nienwmegen R, Eikelenboom P. The development of specific antibody-containing cells and the localization of extracellular antibody in the follicles of the spleen of rabbits after administration of free or liposome associated albumin antigen. Anat Rec 1983;206:189-198.
5. Jacob J, Kassir R, Kelsoe G. In situ studies of the primary immune response to (4-hydroxy-3-nitrophenyl)acetyl. I. The architecture and dynamics of responding cell populations. J Exp Med 1991;173:1165-1175.
6. Liu YJ, Zhang J, Lane PJ, Chan EY, MacLennan IC. Sites of specific B cell activation in primary and secondary responses to T cell-dependent and T cell-independent antigens. Eur J Immunol 1991;21:2951-2962.
7. Sze DM, Toellner KM, Garcia de Vinuesa C, Taylor DR, MacLennan IC. Intrinsic constraint on plasmablast growth and extrinsic limits of plasma cell survival. J Exp Med 2000;192:813-821.
8. Garcia de Vinuesa C, O'Leary P, Sze DM, Toellner KM, MacLennan IC. T-independent type 2 antigens induce B cell proliferation in multiple splenic sites, but exponential growth is confined to extrafollicular foci. Eur J Immunol 1999;29:1314-1323.
9. Kosco MH, Burton GF, Kapasi ZF, Szakal AK, Tew JG. Antibody-forming cell induction during an early phase of germinal centre development and its delay with ageing. Immunology 1989;68:312-318.
10. Luther SA, Gulbranson-Judge A, Acha-Orbea H, MacLennan IC. Viral superantigen drives extrafollicular and follicular B cell differentiation leading to virus-specific antibody production. J Exp Med 1997;185:551-562.
11. Benner R, Hijmans W, Haaijman JJ. The bone marrow: the major source of serum immunoglobulins, but still a neglected site of antibody formation. Clin Exp Immunol 1981;46:1-8.
12. Lamm ME, Phillips-Quagliata JM. Origin and homing of intestinal IgA antibody-secreting cells. J Exp Med 2002;195:F5-F8.
13. Cyster JG. Chemokines and cell migration in secondary lymphoid organs. Science 1999;286:2098-2102.
14. Zlotnik A, Yoshie O. Chemokines: a new classification system and their role in immunity. Immunity 2000;12:121-127.
15. Baggiolini M. Chemokines and leukocyte traffic. Nature 1998;392:565-568.
16. Förster R, Mattis AE, Kremmer E, Wolf E, Brem G, Lipp M. A putative chemokine receptor, BLR1, directs B cell migration to defined lymphoid organs and specific anatomic compartments of the spleen. Cell 1996;87:1037-1047.
17. Ansel KM, et al. A chemokine driven positive feedback loop organizes lymphoid follicles. Nature 2000;406:309-314.
18. Ansel KM, Harris RB, Cyster JG. CXCL13 is required for B1 cell homing, natural antibody production, and body cavity immunity. Immunity 2002;16:67-76.
19. Cyster JG, Ngo VN, Ekland EH, Gunn MD, Sedgwick JD, Ansel KM. Chemokines and B-cell homing to follicles. Curr Top Microbiol Immunol 1999;246:87-92.
20. Bowman EP, et al. Developmental switches in chemokine response profiles during B cell differentiation and maturation. J Exp Med 2000;191:1303-1318.
21. Gunn MD, et al. Mice lacking expression of secondary lymphoid organ chemokine have defects in lymphocyte homing and dendritic cell localization. J Exp Med 1999;189:451-460.
22. Förster R, et al. CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs. Cell 1999;99:23-33.
23. Okada T, et al. Chemokine requirements for B cell entry to lymph nodes and Peyer's patches. J Exp Med 2002;196:65-75.
24. Reif K, et al. Balanced responsiveness to chemoattractants from adjacent zones determines B-cell position. Nature 2002;416:94-99.
25. Toellner KM, Gulbranson-Judge A, Taylor DR, Sze DM, MacLennan IC. Immunoglobulin switch transcript production in vivo related to the site and time of antigen-specific B cell activation. J Exp Med 1996;183:2303-2312.
26. Tashiro K, Tada H, Heilker R, Shirozu M, Nakano T, Honjo T. Signal sequence trap a cloning strategy for secreted proteins and type I membrane proteins. Science 1993;261:600-603.
27. Nagasawa T, Kikutani H, Kishimoto T. Molecular cloning and structure of a preB-cell growth-stimulating factor. Proc Natl Acad Sci USA 1994;91:2305-2309.
28. Bleul CC, Fuhlbrigge RC, Casasnovas JM, Aiuti A, Springer TA. A highly efficacious lymphocyte chemoattractant, stromal cell-derived factor 1 (SDF-1). J Exp Med 1996;184:1101-1109.
29. Nagasawa T, et al. Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF/SDF-1. Nature 1996;382:635-638.
30. Zou YR, Kottmann AH, Kuroda M, Taniuchi I, Littman DR. Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature 1998;393:595-599.
31. Ma Q, et al. Impaired B-lymphopoiesis, myelopoiesis, and derailed cerebellar neuron migration in CXCR4- and SDF-1-deficient mice. Proc Natl Acad Sci USA 1998;95:9448-9453.
32. Hargreaves DC, et al. A coordinated change in chemokine responsiveness guides plasma cell movements. J Exp Med 2001;194:45-56.
33. Cyster JG, Ansel KM, Ngo VN, Hargreaves DC, Lu TT. Traffic patterns of B cells and plasma cells. Adv Exp Med Biol 2002;512:35-41.
34. Wehrli N, et al. Changing responsiveness to chemokines allows medullary plasmablasts to leave lymph nodes. Eur J Immunol 2001;31:609-616.
35. Hauser AE, et al. Chemotactic responsiveness toward ligands for CXCR3 and CXCR4 is regulated on plasma blasts during the time course of a memory immune response. J Immunol 2002;169:1277-1282.
36. Bowman EP, et al. The intestinal chemokine thymus-expressed chemokine (CCL25) attracts IgA antibody-secreting cells. J Exp Med 2002;195:269-275.
37. Luther SA, et al. Differing activities of homeostatic chemokines CCL19, CCL21, and CXCL12 in lymphocyte and dendritic cell recruitment and lymphoid neogenesis. J Immunol 2002;169:424-433.
38. Casamayor-Palleja M, et al. Expression of macrophage inflammatory protein-3alpha, stromal cell-derived factor-1, and B-cell-attracting chemokine-1 identifies the tonsil crypt as an attractive site for B cells. Blood 2001;97:3992-3994.
39. Garcia De Vinuesa C, et al. Dendritic cells associated with plasmablast survival. Eur J Immunol 1999;29:3712-3721.
40. Ngo VN, et al. Lymphotoxin alpha/beta and tumor necrosis factor are required for stromal cell expression of homing chemokines in B and T cell areas of the spleen. J Exp Med 1999;189:403-412.
41. Ma Q, Jones D, Springer TA. The chemokine receptor CXCR4 is required for the retention of B lineage and granulocytic precursors within the bone marrow microenvironment. Immunity 1999;10:463-471.
42. Egawa T, et al. The earliest stages of B cell development require a chemokine stromal cell-derived factor/pre-B cell growth-stimulating factor. Immunity 2001;15:323-334.
43. Kawano MM, Mihara K, Huang N, Tsujimoto T, Kuramoto A. Differentiation of early plasma cells on bone marrow stromal cells requires interleukin-6 for escaping from apoptosis. Blood 1995;85:487-494.
44. Smith KGC, Hewitson TD, Nossal GJV, Tarlinton DM. The phenotype and fate of the antibody-forming cells of the splenic foci. Eur J Immunol 1996;26:444-448.
45. Slifka MK, Matloubian M, Ahmed R. Bone marrow is a major site of long-term antibody production after acute viral infection. J Virol 1995;69:1895-1902.
46. Sawada S, et al. Disturbed CD4+ T cell homeostasis and in vitro HIV-1 susceptibility in transgenic mice expressing T cell line-tropic HIV-1 receptors. J Exp Med 1998;187:1439-1449.
47. Sanz-Rodriguez F, Hidalgo A, Teixido J. Chemokine stromal cell-derived factor-1 alpha modulates VLA-4 integrin-mediated multiple myeloma cell adhesion to CS-1/fibronectin and VCAM-1. Blood 2001;97:346-351.
48. Burger JA, Burger M, Kipps TJ. Chronic lymphocytic leukemia B cells express functional CXCR4 chemokine receptors that mediate spontaneous migration beneath bone marrow stromal cells. Blood 1999;94:3658-3667.
49. Burger JA, Zvaifler NJ, Tsukada N, Firestein GS, Kipps TJ. Fibroblast-like synoviocytes support B-cell pseudoemperipolesis via a stromal cell-derived factor-1- and CD106 (VCAM-1)-dependent mechanism. J Clin Invest 2001;107:305-315.
50. Zhan F, Tian E, Bumm K, Smith R, Barlogie B, Shaughnessy J. Gene expression profiling of human plasma cell differentiation and classification of multiple myeloma based on similarities to distinct stages of late stage B-cell development. Blood 2003;101:1128-1140.
51. Burger JA, Tsukada N, Burger M, Zvaifler NJ, Dell'Aquila M, Kipps TJ. Blood-derived nurse-like cells protect chronic lymphocytic leukemia B cells from spontaneous apoptosis through stromal cell-derived factor-1. Blood 2000;96:2655-2663.
52. Foussat A, et al. Production of stromal cell-derived factor-1 by mesothelial cells and effects of this chemokine on peritoneal B lymphocytes. Eur J Immunol 2001;31:350-359.
53. Wurbel MA, et al. Mice lacking the CCR9 CC-chemokine receptor show a mild impairment of early T- and B-cell development and a reduction in T-cell receptor gammadelta(+) gut intraepithelial lymphocytes. Blood 2001;98:2626-2632.
54. Uehara S, Grinberg A, Farber JM, Love PE. A role for CCR9 in T lymphocyte development and migration. J Immunol 2002;168:2811-2819.
55. Wurbel MA, et al. The chemokine TECK is expressed by thymic and intestinal epithelial cells and attracts double- and single-positive thymocytes expressing the TECK receptor CCR9. Eur J Immunol 2000;30:262-271.
56. Kunkel EJ, et al. Lymphocyte CC chemokine receptor 9 and epithelial thymus-expressed chemokine (TECK) expression distinguish the small intestinal immune compartment: epithelial expression of tissue-specific chemokines as an organizing principle in regional immunity. J Exp Med 2000;192:761-768.
57. Papadakis KA, et al. The role of thymus-expressed chemokine and its receptor CCR9 on lymphocytes in the regional specialization of the mucosal immune system. J Immunol 2000;165:5069-5076.
58. Agace WW, et al. Constitutive expression of stromal derived factor-1 by mucosal epithelia and its role in HIV transmission and propagation. Curr Biol 2000;10:325-328.
59. Fagarasan S, Kinoshita K, Muramatsu M, Ikuta K, Honjo T. In situ class switching and differentiation to IgA-producing cells in the gut lamina propria. Nature 2001;413:639-643.
60. Kroese FG, Butcher EC, Stall AM, Lalor PA, Adams S, Herzenberg LA. Many of the IgA producing plasma cells in murine gut are derived from self-replenishing precursors in the peritoneal cavity. Int Immunol 1989;1:75-84.
61. Newberry RD, McDonough JS, McDonald KG, Lorenz RG. Postgestational lymphotoxin/lymphotoxin beta receptor interactions are essential for the presence of intestinal B lymphocytes. J Immunol 2002;168:4988-4997.
62. Fagarasan S, et al. Alymphoplasia (aly)-type nuclear factor kappaB-inducing kinase (NIK) causes defects in secondary lymphoid tissue chemokine receptor signaling and homing of peritoneal cells to the gut-associated lymphatic tissue system. J Exp Med 2000;191:1477-1486.
63. Macpherson AJ, Gatto D, Sainsbury E, Harriman GR, Hengartner H, Zinkernagel RM. A primitive T cell-independent mechanism of intestinal mucosal IgA responses to commensal bacteria. Science 2000;288:2222-2226.
64. Kang HS, et al. Signaling via LTbetaR on the lamina propria stromal cells of the gut is required for IgA production. Nat Immunol 2002;3:576-582.
65. McDermott MR, Bienenstock J. Evidence for a common mucosal immunologic system. I. Migration of B immunoblasts into intestinal, respiratory, and genital tissues. J Immunol 1979;122:1892-1898.
66. Pierce NF, Cray WC Jr. Determinants of the localization, magnitude, and duration of a specific mucosal IgA plasma cell response in enterically immunized rats. J Immunol 1982;128:1311-1315.
67. Parr EL, Parr MB. Immunoglobulin G, plasma cells, and lymphocytes in the murine vagina after vaginal or parenteral immunization with attenuated herpes simplex virus type 2. J Virol 1998;72:5137-5145.
68. Wang W, et al. Identification of a novel chemokine (CCL28), which binds CCR10 (GPR2). J Biol Chem 2000;275:22313-22323.
69. Pan J, et al. A novel chemokine ligand for CCR10 and CCR3 expressed by epithelial cells in mucosal tissues. J Immunol 2000;165:2943-2949.
70. Morales J, et al. CTACK, a skin-associated chemokine that preferentially attracts skin-homing memory T cells. Proc Natl Acad Sci USA 1999;96:14470-14475.
71. Hromas R, Broxmeyer HE, Kim C, Christopherson K 2nd, Hou YH. Isolation of ALP, a novel divergent murine CC chemokine with a unique carboxy terminal extension. Biochem Biophys Res Commun 1999;258:737-740.
72. Ishikawa-Mochizuki I, et al. Molecular cloning of a novel CC chemokine, interleukin-11 receptor alpha-locus chemokine (ILC), which is located on chromosome 9p13 and a potential homologue of a CC chemokine encoded by molluscum contagiosum virus. FEBS Lett 1999;460:544-548.
73. Baird JW, et al. ESkine, a novel beta-chemokine, is differentially spliced to produce secretable and nuclear targeted isoforms. J Biol Chem 1999;274:33496-33503.
74. Finke D, Baribaud F, Diggelmann H, Acha-Orbea H. Extrafollicular plasmablast B cells play a key role in carrying retroviral infection to peripheral organs. J Immunol 2001;166:6266-6275.
75. Briskin M, et al. Human mucosal addressin cell adhesion molecule-1 is preferentially expressed in intestinal tract and associated lymphoid tissue. Am J Pathol 1997;151:97-110.
76. Kunkel EJ, Butcher EC. Chemokines and the tissue-specific migration of lymphocytes. Immunity 2002;16:1-4.
77. Campbell JJ, et al. Unique subpopulations of CD56+ NK and NK-T peripheral blood lymphocytes identified by chemokine receptor expression repertoire. J Immunol 2001;166:6477-6482.
78. Amichay D, Gazzinelli RT, Karupiah G, Moench TR, Sher A, Farber JM. Genes for chemokines MuMig and Crg-2 are induced in protozoan and viral infections in response to IFN-gamma with patterns of tissue expression that suggest nonredundant roles in vivo. J Immunol 1996;157:4511-4520.
79. Cassese G, et al. Inflamed kidneys of NZB/W mice are a major site for the homeostasis of plasma cells. Eur J Immunol 2001;31:2726-2732.
80. Jones D, Benjamin RJ, Shahsafaei A, Dorfman DM. The chemokine receptor CXCR3 is expressed in a subset of B-cell lymphomas and is a marker of B-cell chronic lymphocytic leukemia. Blood 2000;95:627-632.
81. Park MK, et al. The CXC chemokine routine monokine induced by IFN-gamma (CXC chemokine ligand 9) is made by APCs, targets lymphocytes including activated B cells, and supports antibody responses to a bacterial pathogen in vivo. J Immunol 2002;169:1433-1443.
82. Kim HJ, Berek C. B cells in rheumatoid arthritis. Arthritis Res 2000;2:126-131.
83. Nanki T, et al. Stromal cell-derived factor-1-CXC chemokine receptor 4 interactions play a central role in CD4+ T cell accumulation in rheumatoid arthritis synovium. J Immunol 2000;165:6590-6598.
84. Gattass CR, King LB, Luster AD, Ashwell JD. Constitutive expression of interferon gamma-inducible protein 10 in lymphoid organs and inducible expression in T cells and thymocytes. J Exp Med 1994;179:1373-1378.
85. Trentin L, et al. The chemokine receptor CXCR3 is expressed on malignant B cells and mediates chemotaxis. J Clin Invest 1999;104:115-121.
86. Underhill GH, Minges-Wols HA, Fornek JL, Witte PL, Kansas GS. IgG plasma cells display a unique spectrum of leukocyte adhesion and homing molecules. Blood 2002;99:2905-2912.
87. Lu TT, Cyster JG. Integrin-mediated long-term B cell retention in the splenic marginal zone. Science 2002;297:409-412.
88. Van den Berg TK, Dopp EA, Breve JJ, Kraal G, Dijkstra CD. The heterogeneity of the reticulum of rat peripheral lymphoid organs identified by monoclonal antibodies. Eur J Immunol 1989;19:1747-1756.
89. Liakka KA, Autio-Harmainen HI. Distribution of the extracellular matrix proteins tenascin, fibronectin, and vitronectin in fetal, infant, and adult human spleens. J Histochem Cytochem 1992;40:1203-1210.
90. Berlin-Rufenach C, et al. Lymphocyte migration in lymphocyte function-associated antigen (LFA)-1-deficient mice. J Exp Med 1999;189:1467-1478.
91. Koni PA, Joshi SK, Temann UA, Olson D, Burkly L, Flavell RA. Conditional vascular cell adhesion molecule 1 deletion in mice. Impaired lymphocyte migration to bone marrow. J Exp Med 2001;193:741-754.
92. Leuker CE, Labow M, Muller W, Wagner N. Neonatally induced inactivation of the vascular cell adhesion molecule 1 gene impairs B cell localization and T cell-dependent humoral immune response. J Exp Med 2001;193:755-768.
93. Miyake K, Medina K, Ishihara K, Kimoto M, Auerbach R, Kincade PW. A VCAM-like adhesion molecule on murine bone marrow stromal cells mediates binding of lymphocyte precursors in culture. J Cell Biol 1991;114:557-565.
94. Bentley AM, et al. Expression of endothelial and leukocyte adhesion molecules interacellular adhesion molecule-1, E-selectin, and vascular cell adhesion molecule-1 in the bronchial mucosa in steady-state and allergen-induced asthma. J Allergy Clin Immunol 1993;92:857-868.
95. Finke D, Acha-Orbea H. Differential migration of in vivo primed B and T lymphocytes to lymphoid and nonlymphoid organs. Eur J Immunol 2001;31:2603-2611.
96. Hattori H, et al. VLA-5 in the plasma cell line, FR4ds, acts as a common regulator of VLA-4 and VLA-6 in spreading induced by fibronectin and laminin. Cell Immunol 1996;174:63-72.
97. Farstad IN, Halstensen TS, Lazarovits AI, Norstein J, Fausa O, Brandtzaeg P. Human intestinal B-cell blasts and plasma cells express the mucosal homing receptor integrin alpha 4 beta 7. Scand J Immunol 1995;42:662-672.
98. Wagner N, et al. Critical role for beta7 integrins in formation of the gut-associated lymphoid tissue. Nature 1996;382:366-370.
99. van der Feltz MJ, de Groot N, Bayley JP, Lee SH, Verbeet MP, de Boer HA. Lymphocyte homing and Ig secretion in the murine mammary gland. Scand J Immunol 2001;54:292-300.
100. Rosen SD. Endothelial ligands for 1-selectin: from lymphocyte recirculation to allograft rejection. Am J Pathol 1999;155:1013-1020.
101. Xia L, et al. P-selectin glycoprotein ligand-1-deficient mice have impaired leukocyte tethering to E-selectin under flow. J Clin Invest 2002;109:939-950.
102. Schweitzer KM, et al. Constitutive expression of E-selectin and vascular cell adhesion molecule-1 on endothelial cells of hematopoietic tissues. Am J Pathol 1996;148:165-175.
103. Mazo IB, Gutierrez-Ramos JC, Frenette PS, Hynes RO, Wagner DD, von Andrian UH. Hematopoietic progenitor cell rolling in bone marrow microvessels: parallel contributions by endothelial selectins and vascular cell adhesion molecule 1. J Exp Med 1998;188:465-474.
104. Frenette PS, Subbarao S, Mazo IB, von Andrian UH, Wagner DD. Endothelial selectins and vascular cell adhesion molecule-1 promote hematopoietic progenitor homing to bone marrow. Proc Natl Acad Sci USA 1998;95:14423-14428.
105. Nitschke L, Floyd H, Ferguson DJ, Crocker PR. Identification of CD22 ligands on bone marrow sinusoidal endothelium implicated in CD22-dependent homing of recirculating B cells. J Exp Med 1999;189:1513-1518.
106. Calame KL. Plasma cells finding new light at the end of B cell development. Nat Immunol 2001;2:1103-1108.
107. Otipoby KL, et al. CD22 regulates thymus-independent responses and the lifespan of B cells. Nature 1996;384:634-637.
108. Nitschke L, Carsetti R, Ocker B, Keohler G, Lamers MC. CD22 is a negative regulator of B-cell receptor signalling. Curr Biol 1997;7:133-143.
109. Nitschke L, Floyd H, Crocker PR. New functions for the sialic acid-binding adhesion molecule CD22, a member of the growing family of Siglecs. Scand J Immunol 2001;53:227-234.
110. Razi N, Varki A. Masking and unmasking of the sialic acid-binding lectin activity of CD22 (Siglec-2) on B lymphocytes. Proc Natl Acad Sci USA 1998;95:7469-7474.
111. Coico RF, Bhogal BS, Thorbecke GJ. Relationship of germinal centers in lymphoid tissue to immunologic memory. VI. Transfer of B cell memory with lymph node cells fractionated according to their receptors for peanut agglutinin. J Immunol 1983;131:2254-2257.
112. Slupsky JR, et al. The peanut-agglutinin (PNA)-binding surface components of malignant plasma cells. Br J Haematol 1993;83:567-573.
113. Aizawa S, Tavassoli M. Marrow uptake of galactosyl-containing neoglycoproteins: implications in stem cell homing. Exp Hematol 1988;16:811-813.
114. Minges Wols HA, Underhill GH, Kansas GS, Witte PL. The role of bone marrow-derived stromal cells in the maintenance of plasma cell longevity. J Immunol 2002;169:4213-4221.
115. Goodnow CC, Cyster JG. Lymphocyte homing: the scent of a follicle. Curr Biol 1997;7:R219-R222.
116. Picker LJ, Siegelman MH. Lymphoid tissues and organs. In: Paul WE, ed. Fundamental immunology, vol. 4. Philadelphia: Lippincott-Raven, 1999:479-531.
117. Vassileva G, et al. The reduced expression of 6Ckine in the plt mouse results from the deletion of one of two 6Ckine genes. J Exp Med 1999;190:1183-1188.
118. Nakano H, Gunn MD. Gene duplications at the chemokine locus on mouse chromosome 4: multiple strain-specific haplotypes and the deletion of secondary lymphoid-organ chemokine and EBI-1 ligand chemokine genes in the plt mutation. J Immunol 2001;166:361-369.