Human BLyS facilitates engraftment of human PBL derived B cells in immunodeficient mice

PLoS ONE

Volumn 3, Issue 9, 2008, Pages

  Schmidt, Madelyn R ^a   Appel, Michael C ^b   Giassi, Lisa J ^a   Greiner, Dale L ^a   Shultz, Leonard D ^c   Woodland, Robert T ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^c JACKSON LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B CELL ACTIVATING FACTOR; IMMUNOGLOBULIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PNEUMOCOCCUS VACCINE; PROTEIN P52; RECOMBINANT PROTEIN; BLYS RECEPTOR; CD19 ANTIGEN; TUMOR NECROSIS FACTOR RECEPTOR; UNCLASSIFIED DRUG;

ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ARTICLE; B LYMPHOCYTE; CELL SURVIVAL; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; EX VIVO STUDY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNE DEFICIENCY; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOGLOBULIN BLOOD LEVEL; IMMUNOHISTOCHEMISTRY; LYMPHOCYTE ACTIVATION; LYMPHOCYTE CULTURE; MOUSE; NONHUMAN; PERIPHERAL LYMPHOCYTE; RECIPIENT; SIGNAL TRANSDUCTION; T LYMPHOCYTE; THYMUS; WESTERN BLOTTING; ANIMAL; BIOSYNTHESIS; CELL NUCLEUS; CELL SEPARATION; CHEMISTRY; CYTOLOGY; METABOLISM; MOUSE MUTANT; NONOBESE DIABETIC MOUSE; PHYSIOLOGY;

MURINAE; MUS;

ANIMALS; ANTIGENS, CD19; B-LYMPHOCYTES; CELL NUCLEUS; CELL SEPARATION; FLOW CYTOMETRY; HUMANS; MICE; MICE, INBRED NOD; MICE, SCID; NF-KAPPA B; PNEUMOCOCCAL VACCINES; RECEPTORS, TUMOR NECROSIS FACTOR; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION;

EID: 52649106011     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0003192     Document Type: Article

References (73)

1. Shultz LD, Ishikawa F, Greiner DL (2007) Humanized mice in translational biomedical research. Nat Rev Immunol 7: 118-130.
2. Manz MG (2007) Human-Hemato-Lymphoid-System Mice: Opportunities and Challenges. Immunity 26: 537-541.
3. Macchiarini F, Manz MG, Palucka AK, Shultz LD (2005) Humanized mice: are we there yet? J Exp Med 202: 1307-1311.
4. Di Ianni M, Terenzi A, Falzetti F, Bartoli A, Di Florio S, et al. (2002) Homing and survival of thymidine kinase-transduced human T cells in NOD/ SCID mice. Cancer Gene Ther 9: 756-761.
5. Goldman JP, Blundell MP, Lopes L, Kinnon C, Di Santo JP, et al. (1998) Enhanced human cell engraftment in mice deficient in RAG2 and the common cytokine receptor gamma chain. Br J Haematol 103: 335-342.
6. Hiramatsu H, Nishikomori R, Heike T, Ito M, Kobayashi K, et al. (2003) Complete reconstitution of human lymphocytes from cord blood CD34+ cells using the NOD/SCID/gammacnull mice model. Blood 102: 873-880
7. Kerre TC, De Smet G, De Smedt M, Zippelius A, Pittet MJ, et al. (2002) Adapted NOD/SCID model supports development of phenotypically and functionally mature T cells from human umbilical cord blood CD34(+) cells. Blood 99: 1620-1626.
8. Kikuchi K, Lian ZX, He XS, Arisari AA, Ishibashi M, et al. (2003) Appearance of human plasma cells following differentiation of human B cells in NOD/SCID mouse spleen. Clin Dev Immunol 10: 197-202.
9. Shultz LD, Lang PA, Christianson SW, Gott B, Lyons B, et al. (2000) NOD/ LtSz-Rag1null mice: an immunodeficient and radioresistant model for engraftment of human hematolymphoid cells, HIV infection, and adoptive transfer of NOD mouse diabetogenic T cells. J Immunol 164: 2496-2507.
10. Shultz LD, Banuelos S, Lyons B, Samuels R, Burzenski L, et al. (2003) NOD/LtSz-Rag1nullPfpnull mice: a new model system with increased levels of human peripheral leukocyte and hematopoietic stem-cell engraftment. Transplantation 76: 1036-1042.
11. Traggiai E, Chicha L, Mazzucchelli L, Bronz L, Piffaretti JC, et al. (2004) Development of a human adaptive immune system in cord blood cell-transplanted mice. Science 304: 104-107.
12. Shultz LD, Lyons BL, Burzenski LM, Gott B, Chen X, et al. (2005) Human Lymphoid and Myeloid Cell Development in NOD/LtSz-scid IL2R{gamma}-null Mice Engrafted with Mobilized Human Hemopoietic Stem Cells. J Immunol 174: 6477-6489.
13. Wagar EJ, Cromwell MA, Shultz LD, Woda BA, Sullivan JL, et al. (2000) Regulation of human cell engraftment and development of EBV-related lymphoproliferative disorders in Hu-PBL-scid mice. J Immunol 165: 518-527.
14. Kraus M, Alimzhanov MB, Rajewsky N, Rajewsky K (2004) Survival of resting mature B lymphocytes depends on BCR signaling via the Igalpha/ beta heterodimer. Cell 117: 787-800.
15. Mackay F, Browning JL (2002) BAFF: a fundamental survival factor for B cells. Nat Rev Immunol 2: 465-475.
16. Mackay F, Schneider P, Rennert P, Browning J (2003) BAFF AND APRIL: a tutorial on B cell survival. Annu Rev Immunol 21: 231-264.
17. Rolink AG, Tschopp J, Schneider P, Melchers F (2002) BAFF is a survival and maturation factor for mouse B cells. Eur J Immunol 32: 2004-2010.
18. Bossen C, Schneider P (2006) BAFF, APRIL and their receptors: structure, function and signaling. Semin Immunol 18: 263-275.
19. Claudio E, Brown K, Park S, Wang H, Siebenlist U (2002) BAFF-induced NEMO-independent processing of NF-kappa B2 in maturing B cells. Nat Immunol 3: 958-965.
20. Sasaki Y, Derudder E, Hobeika E, Pelanda R, Reth M, et al. (2006) Canonical NF-kappaB activity, dispensable for B cell development, replaces BAFF-receptor signals and promotes B cell proliferation upon activation. Immunity 24: 729-739.
21. Sasaki Y, Casola S, Kutok JL, Rajewsky K, Schmidt-Supprian M (2004) TNF family member B cell-activating factor (BAFF) receptor-dependent and -independent roles for BAFF in B cell physiology. J Immunol 173: 2245-2252.
22. Gordon NC, Pan B, Hymowitz SG, Yin J, Kelley RF, et al. (2003) BAFF/BLyS receptor 3 comprises a minimal TNF receptor-like module that encodes a highly focused ligand-binding site. Biochemistry 42: 5977-5983.
23. Kim HM, Yu KS, Lee ME, Shin DR, Kim YS, et al. (2003) Crystal structure of the BAFF-BAFF-R complex and its implications for receptor activation. Nat Struct Biol 10: 342-348.
24. Hase H, Kanno Y, Kojima M, Hasegawa K, Sakurai D, et al. (2004) BAFF/ BLyS can potentiate B-cell selection with the B-cell coreceptor complex. Blood 103: 2257-2265.
25. Shulga-Morskaya S, Dobles M, Walsh ME, Ng LG, MacKay F, et al. (2004) B cell-activating factor belonging to the TNF family acts through separate receptors to support B cell survival and T cell-independent antibody formation. J Immunol 173: 2331-2341.
26. Zhang X, Park CS, Yoon SO, Li L, Hsu YM, et al. (2005) BAFF supports human B cell differentiation in the lymphoid follicles through distinct receptors. Int Immunol 17: 779-788.
27. Avery DT, Kalled SL, Ellyard JI, Ambrose C, Bixler SA, et al. (2003) BAFF selectively enhances the survival of plasmablasts generated from human memory B cells. J Clin Invest 112: 286-297.
28. Stohl W (2002) B lymphocyte stimulator protein levels in systemic lupus erythematosus and other diseases. Curr Rheumatol Rep 4: 345-350.
29. Collins CE, Gavin AL, Migone TS, Hilbert DM, Nemazee D, et al. (2006) B lymphocyte stimulator (BLyS) isoforms in systemic lupus erythematosus: disease activity correlates better with blood leukocyte BLyS mRNA levels than with plasma BLyS protein levels. Arthritis Res Ther 8: R6.
30. Stohl W (2006) Therapeutic targeting of B lymphocyte stimulator (BLyS) in the rheumatic diseases. Endocr Metab Immune Disord Drug Targets 6: 351-358.
31. Stewart DM, McAvoy MJ, Hilbert DM, Nelson DL (2003) B lymphocytes from individuals with common variable immunodeficiency respond to B lymphocyte stimulator (BLyS protein) in vitro. Clin Immunol 109: 137-143.
32. Losi CG, Salzer U, Gatta R, Lougaris V, Cattaneo G, et al. (2006) Mutational analysis of human BLyS in patients with common variable immunodeficiency. J Clin Immunol 26: 396-399.
33. He B, Chadburn A, Jou E, Schattner EJ, Knowles DM, et al. (2004) Lympnoma B cells evade apoptosis through the TNF family members BAFF/ BLyS and APRIL. J Immunol 172: 3268-3279.
34. Baker KP (2004) BLyS-an essential survival factor for B cells: basic biology, links to pathology and therapeutic target. Autoimmun Rev 3: 368-375.
35. Novak AJ, Darce JR, Arendt BK, Harder B, Henderson K, et al. (2004) Expression of BCMA, TACI, and BAFF-R in multiple myeloma: a mechanism for growth and survival. Blood 103: 689-694.
36. Oren DA, Li Y, Volovik Y, Morris TS, Dharia C, et al. (2002) Structural basis of BLyS receptor recognition. Nat Struct Biol 9: 288-292.
37. Cuss AK, Avery DT, Cannons JL, Yu LJ, Nichols KE, et al. (2006) Expansion of functionally immature transitional B cells is associated with human-immunodeficient states characterized by impaired humoral immunity. J Immunol 176: 1506-1516.
38. Sims GP, Ettinger R, Shirota Y, Yarboro CH, Illei GG, et al. (2005) Identification and characterization of circulating human transitional B cells. Blood 105: 4390-4398.
39. Day ES, Cachero TG, Qian F, Sun Y, Wen D, et al. (2005) Selectivity of BAFF/BLyS and APRIL for binding to the TNF family receptors BAFFR/BR3 and BCMA. Biochemistry 44: 1919-1931.
40. Thompson JS, Schneider P, Kalled SL, Wang L, Lefevre EA, et al. (2000) BAFF binds to the tumor necrosis factor receptor-like molecule B cell maturation antigen and is important for maintaining the peripheral B cell population. J Exp Med 192: 129-135.
41. Patke A, Mecklenbrauker I, Tarakhovsky A (2004) Survival signaling in resting B cells. Curr Opin Immunol 16: 251-255.
42. Kanakaraj P, Migone TS, Nardelli B, Ullrich S, Li Y, et al. (2001) BLyS binds to B cells with high affinity and induces activation of the transcription factors NF-kappaB and ELF-1 Cytokine 13: 25-31.
43. Ramakrishnan P, Wang W, Wallach D (2004) Receptor-specific signaling for both the alternative and the canonical NF-kappaB activation pathways by NF-kappaB-inducing kinase. Immunity 21: 477-489.
44. Enzler T, Bonizzi G, Silverman GJ, Otero DC, Widhopf GF, et al. (2006) Alternative and classical NF-kappa B signaling retain autoreactive B cells in the splenic marginal zone and result in lupus-like disease. Immunity 25: 403-415.
45. Cabatingan MS, Schmidt MR, Sen R, Woodland RT (2002) Naive B lymphocytes undergo homeostatic proliferation in response to B cell deficit. J Immunol 169: 6795-6805.
46. Woodland RT, Schmidt MR (2005) Homeostatic proliferation of B cells. Semin Immunol 17: 209-217.
47. Woodland RT, Schmidt MR, Thompson CB (2006) BLyS and B cell homeostasis. Semin Immunol 18: 318-326.
48. Tavernier J, Devos R, Van der Heyden J, Hauquier G, Bauden R, et al. (1989) Expression of human and murine interleukin-5 in eukaryotic systems. DNA 8: 491-501.
49. McKenzie AN, Barry SC, Strath M, Sanderson CJ (1991) Structure-function analysis of interleukin-5 utilizing mouse/human chimeric molecules. Embo J 10: 1193-1199.
50. Williams IR, Unanue ER (1991) Characterization of accessory cell costimulation of Th1 cytokine synthesis. J Immunol 147: 3752-3760.
51. Yoshioka M, Mori Y, Miyazaki S, Miyamoto T, Yokomizo Y, et al. (1999) Biological Functions of recombinant bovine interleukin 6 expressed in a baculovirus system. Cytokine 11: 863-868.
52. Kumar CS, Muthukumaran G, Frost LJ, Noe M, Ahn YH, et al. (1989) Molecular characterization of the marine interferon gamma receptor cDNA. J Biol Chem 264: 17939-17946.
53. Smirnova AS, Andrade-Oliveira V, Gerbase-Delima M (2008) Identification of new splice variants of the genes BAFF and BCMA. Mol Immunol 45: 1179-1183.
54. Woodland RT, Fox CJ, Schmidt MR, Hammerman PS, Opferman JT, et al. (2008) Multiple signaling pathways promote B lymphocyte stimulator dependent B-cell growth and survival. Blood 111: 750-760.
55. Depraetere S, Verhoye L, Leclercq G, Leroux-Roels G (2001) Human B cell growth and differentiation in the spleen of immunodeficient mice. J Immunol 166: 2929-2936.
56. Tournoy KG, Depraetere S, Pauwels RA, Leroux-Roels GG (2000) Mouse strain and conditioning regimen determine survival and function of human leucocytes in immumodeficient mice. Clin Exp Immunol 119: 231-239.
57. Turgeon NA, Banuelos SJ, Shultz LD, Lyons BL, Iwakoshi N, et al. (2003) Alloimmune injury and rejection of human skin grafts on human peripheral blood lymphocyte-reconstituted non-obese diabetic severe combined immunodeficient beta2-microglobulin-null mice. Exp Biol Med (Maywood) 228: 1096-1104.
58. van Rijn RS, Simonetti ER, Hagenbeek A, Hogenes MC, de Weger RA, et al. (2003) A new xenograft model for graft-versus-host disease by intravenous transfer of human peripheral blood mononuclear cells in RAG2-/-gammac-/- double-mutant mice. Blood 102: 2522-2531.
59. Berney T, Molano RD, Pileggi A, Cattan P, Li H, et al. (2001) Patterns of engraftment in different strains of immunodeficient mice reconstituted with human peripheral blood lymphocytes. Transplantation 72: 133-140.
60. Cao T, Lazdina U, Desombere I, Vanlandschoot P, Milich DR, et al. (2001) Hepatitis B virus core antigen binds and activates naive human B cells in vivo: studies with a human PBL-NOD/SCID mouse model. J Virol 75: 6359-6366.
61. 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: 319-330.
62. Freitas AA, Rocha B (2000) Population biology of lymphocytes: the flight for survival. Annu Rev Immunol 18: 83-111.
63. Mackay F, Leung H (2006) The role of the BAFF/APRIL system on T cell function. Semin Immunol 18: 284-289.
64. Huard B, Schneider P, Mauri D, Tschopp J, French LE (2001) T cell costimulation by the TNF ligand BAFF. J Immunol 167: 6225-6231.
65. Ng LG, Mackay CR, Mackay F (2005) The BAFF/APRIL system: life beyond B lymphocytes. Mol Immunol 42: 763-772.
66. Ye Q, Wang L, Wells AD, Tao R, Han R, et al. (2004) BAFF binding to T cell-expressed BAFF-R costimulates T cell proliferation and alloresponses. Eur J Immunol 34: 2750-2759.
67. Prlic M, Jameson SC (2002) Homeostatic expansion versus antigen-driven proliferation: common ends by different means? Microbes Infect 4: 531-537.
68. Goldrath AW, Luckey CJ, Park R, Benoist C, Mathis D (2004) The molecular program induced in T cells undergoing homeostatic proliferation. Proc Natl Acad Sci U S A 101: 16885-16890.
69. Marleau AM, Sarvetnick N (2005) T cell homeostasis in tolerance and immunity. J Leukoc Biol 78: 575-584.
70. Diaz-de-Durana Y, Mantchev GT, Brain RJ, Franco A (2006) TACI-BLyS signaling via B-cell-dendritic cell cooperation is required for naive CD8+ T-cell priming in vivo. Blood 107: 594-601.
71. King M, Pearson T, Shultz LD, Leif J, Bottino R, et al. (2008) A new Hu-PBL model for the study of human islet alloreactivity based on NOD-scid mice bearing a targeted mutation in the IL-2 receptor gamma chain gene. Clin Immumol 126: 303-314.
72. Woodland RT, Schmidt MR, Korsmeyer SJ, Gravel KA (1996) Regulation of B cell survival in xid mice by the proto-oncogene bcl-2. J Immunol 156: 2143-2154.
73. Tam WF, Wang W, Sen R (2001) Cell-specific association and shuttling of IkappaBalpha provides a mechanism for nuclear NF-kappaB in B lymphocytes. Mol Cell Biol 21: 4837-4846.