Expansion of B-1a cells with germline heavy chain sequence in lupus mice

Frontiers in Immunology

Volumn 7, Issue MAR, 2016, Pages

  Holodick, Nichol E ^a   Zeumer, Leilani ^b   Rothstein, Thomas L ^a,c   Morel, Laurence ^b  

^a FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^c DONALD AND BARBARA ZUCKER SCHOOL OF MEDICINE AT HOFSTRA NORTHWELL   (United States)

Author keywords

Autoimmunity; B cells; B 1 cells; Lupus erythematosus; Mouse model; Natural antibodies; Repertoire analysis; Systemic

Indexed keywords

CD45 ANTIGEN; CELL ANTIBODY; IMMUNOGLOBULIN M;

ALLELE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOIMMUNITY; B 1A CELL; B LYMPHOCYTE; CONTROLLED STUDY; FETUS; GENE AMPLIFICATION; GERM LINE; HEAVY CHAIN; IMMUNOGLOBULIN GENE; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; SEQUENCE ANALYSIS; SYSTEMIC LUPUS ERYTHEMATOSUS;

EID: 84964575138     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2016.00108     Document Type: Article

References (54)

1. Herzenberg LA, Tung JW. B cell lineages: documented at last! Nat Immunol (2006) 7:225-6. doi: 10.1038/ni0306-225.
2. Rothstein TL, Griffin DO, Holodick NE, Quach TD, Kaku H. Human B-1 cells take the stage. Ann N Y Acad Sci (2013) 1285:97-114. doi:10.1111/nyas.12137.
3. Hardy RR, Hayakawa K. B cell development pathways. Annu Rev Immunol (2001) 19:595-621. doi:10.1146/annurev.immunol.19.1.595.
4. Rothstein TL. Cutting edge commentary: two B-1 or not to be one. J Immunol (2002) 168:4257-61. doi:10.4049/jimmunol.168.9.4257.
5. Wong SC, Chew WK, Tan JE, Melendez AJ, Francis F, Lam KP. Peritoneal CD5+ B-1 cells have signaling properties similar to tolerant B cells. J Biol Chem (2002) 277:30707-15. doi:10.1074/jbc. M202460200.
6. Holodick NE, Tumang JR, Rothstein TL. Continual signaling is responsible for constitutive ERK phosphorylation in B-1a cells. Mol Immunol (2009) 46:3029-36. doi:10.1016/j.molimm.2009.06.011.
7. Zhong X, Gao W, Degauque N, Bai C, Lu Y, Kenny J, et al. Reciprocal generation of Th1/Th17 and T(reg) cells by B1 and B2 B cells. Eur J Immunol (2007) 37:2400-4. doi:10.1002/eji.200737296.
8. Baumgarth N. The double life of a B-1 cell: self-reactivity selects for protective effector functions. Nat Rev Immunol (2011) 11:34-46. doi:10.1038/nri2901.
9. Ehrenstein MR, Notley CA. The importance of natural IgM: scavenger, protector and regulator. Nat Rev Immunol (2010) 10:778-86. doi:10.1038/nri2849.
10. Feeney AJ. Lack of N regions in fetal and neonatal mouse immunoglobulin V-D-J junctional sequences. J Exp Med (1990) 172:1377-90. doi:10.1084/jem.172.5.1377.
11. Pennell CA, Arnold LW, Haughton G, Clarke SH. Restricted Ig variable region gene expression among Ly-1+ B cell lymphomas. J Immunol (1988) 141:2788-96.
12. Hardy RR, Carmack CE, Shinton SA, Riblet RJ, Hayakawa K. A single VH gene is utilized predominantly in anti-BrMRBC hybridomas derived from purified Ly-1 B cells. Definition of the VH11 family. J Immunol (1989) 142:3643-51.
13. Wang H, Clarke SH. Positive selection focuses the VH12 B-cell repertoire towards a single B1 specificity with survival function. Immunol Rev (2004) 197:51-9. doi:10.1111/j.0105-2896.2004.0098.x.
14. Su SD, Ward MM, Apicella MA, Ward RE. The primary B cell response to the O/core region of bacterial lipopolysaccharide is restricted to the Ly-1 lineage. J Immunol (1991) 146:327-31.
15. Ochsenbein AF, Fehr T, Lutz C, Suter M, Brombacher F, Hengartner H, et al. Control of early viral and bacterial distribution and disease by natural antibodies. Science (1999) 286:2156-9. doi:10.1126/science.286.5447.2156.
16. Baumgarth N, Herman OC, Jager GC, Brown LE, Herzenberg LA, Chen J. B-1 and B-2 cell-derived immunoglobulin M antibodies are nonredundant components of the protective response to influenza virus infection. J Exp Med (2000) 192:271-80. doi:10.1084/jem.192.2.271.
17. Haas KM, Poe JC, Steeber DA, Tedder TF. B-1a and B-1b cells exhibit distinct developmental requirements and have unique functional roles in innate and adaptive immunity to S. pneumoniae. Immunity (2005) 23:7-18. doi:10.1016/j.immuni.2005.04.011.
18. Gronwall C, Vas J, Silverman GJ. Protective roles of natural IgM antibodies. Front Immunol (2012) 3:66. doi:10.3389/fimmu.2012.00066.
19. Mercolino TJ, Arnold LW, Hawkins LA, Haughton G. Normal mouse peritoneum contains a large population of Ly-1+ (CD5) B cells that recognize phosphatidyl choline. Relationship to cells that secrete hemolytic antibody specific for autologous erythrocytes. J Exp Med (1988) 168:687-98. doi:10.1084/jem.168.2.687.
20. Baumgarth N, Tung JW, Herzenberg LA. Inherent specificities in natural antibodies: a key to immune defense against pathogen invasion. Springer Semin Immunopathol (2005) 26:347-62. doi:10.1007/s00281-004-0182-2.
21. Xu Z, Butfiloski EJ, Sobel ES, Morel L. Mechanisms of peritoneal B-1a cells accumulation induced by murine lupus susceptibility locus Sle2. J Immunol (2004) 173:6050-8. doi:10.4049/jimmunol.173.10.6050.
22. Mohan C, Morel L, Yang P, Wakeland EK. Accumulation of splenic B1a cells with potent antigen-presenting capability in NZM2410 lupus-prone mice. Arthritis Rheum (1998) 41:1652-62. doi:10.1002/1529-0131(199809)41:9<1652::AID-ART17>3.0.CO;2-W.
23. Xu Z, Morel L. Contribution of B-1a cells to systemic lupus erythematosus in the NZM2410 mouse model. Ann N Y Acad Sci (2015) 1362:215-23. doi:10.1111/nyas.12607.
24. Iizuka J, Katagiri Y, Tada N, Murakami M, Ikeda T, Sato M, et al. Introduction of an osteopontin gene confers the increase in B1 cell population and the production of anti-DNA autoantibodies. Lab Invest (1998) 78:1523-33.
25. Reap EA, Sobel ES, Cohen PL, Eisenberg RA. Conventional B cells, not B-1 cells, are responsible for producing autoantibodies in lpr mice. J Exp Med (1993) 177:69-78. doi:10.1084/jem.177.1.69.
26. Atencio S, Amano H, Izui S, Kotzin BL. Separation of the New Zealand Black genetic contribution to lupus from New Zealand Black determined expansions of marginal zone B and B1a cells. J Immunol (2004) 172:4159-66. doi:10.4049/jimmunol.172.7.4159.
27. Xu Z, Potula HH, Vallurupalli A, Perry D, Baker H, Croker BP, et al. Cyclin-dependent kinase inhibitor Cdkn2c regulates B cell homeostasis and function in the NZM2410-derived murine lupus susceptibility locus Sle2c1. J Immunol (2011) 186:6673-82. doi:10.4049/jimmunol.1002544.
28. Potula HH, Xu Z, Zeumer L, Sang A, Croker BP, Morel L. Cyclin-dependent kinase inhibitor Cdkn2c deficiency promotes B1a cell expansion and autoimmunity in a mouse model of lupus. J Immunol (2012) 189:2931-40. doi:10.4049/jimmunol.1200556.
29. Morel L, Croker BP, Blenman KR, Mohan C, Huang G, Gilkeson G, et al. Genetic reconstitution of systemic lupus erythematosus immunopathology with polycongenic murine strains. Proc Natl Acad Sci U S A (2000) 97:6670-5. doi:10.1073/pnas.97.12.6670.
30. Kantor AB, Merrill CE, Herzenberg LA, Hillson JL. An unbiased analysis of V(H)-D-J(H) sequences from B-1a, B-1b, and conventional B cells. J Immunol (1997) 158:1175-86.
31. Gregoire KE, Goldschneider I, Barton RW, Bollum FJ. Ontogeny of terminal deoxynucleotidyl transferase-positive cells in lymphohemopoietic tissues of rat and mouse. J Immunol (1979) 123:1347-52.
32. Zemlin M, Ippolito GC, Zemlin C, Link J, Monestier M, Schroeder HW Jr. Adult lupus-prone MRL/MpJ2+ mice express a primary antibody repertoire that differs in CDR-H3 length distribution and hydrophobicity from that expressed in the C3H parental strain. Mol Immunol (2005) 42:789-98. doi:10.1016/j.molimm.2004.07.049.
33. Radic MZ, Mackle J, Erikson J, Mol C, Anderson WF, Weigert M. Residues that mediate DNA binding of autoimmune antibodies. J Immunol (1993) 150:4966-77.
34. Kirkham PM, Schroeder HW Jr. Antibody structure and the evolution of immunoglobulin V gene segments. Semin Immunol (1994) 6:347-60. doi:10.1006/smim.1994.1045.
35. Gu H, Kitamura D, Rajewsky K. B cell development regulated by gene rearrangement: arrest of maturation by membrane-bound D mu protein and selection of DH element reading frames. Cell (1991) 65:47-54. doi:10.1016/0092-8674(91)90406-O.
36. Forster I, Rajewsky K. Expansion and functional activity of Ly-1+ B cells upon transfer of peritoneal cells into allotype-congenic, newborn mice. Eur J Immunol (1987) 17:521-8. doi:10.1002/eji.1830170414.
37. Hayakawa K, Carmack CE, Hyman R, Hardy RR. Natural autoantibodies to thymocytes: origin, VH genes, fine specificities, and the role of Thy-1 glycoprotein. J Exp Med (1990) 172:869-78. doi:10.1084/jem.172.3.869.
38. Yang Y, Wang C, Yang Q, Kantor AB, Chu H, Ghosn EE, et al. Distinct mechanisms define murine B cell lineage immunoglobulin heavy chain (IgH) repertoires. Elife (2015) 4:e09083. doi:10.7554/eLife.09083.
39. Forster I, Gu H, Rajewsky K. Germline antibody V regions as determinants of clonal persistence and malignant growth in the B cell compartment. EMBO J (1988) 7:3693-703.
40. Tarlinton D, Stall AM, Herzenberg LA. Repetitive usage of immunoglobulin VH and D gene segments in CD5+ Ly-1 B clones of (NZB x NZW)F1 mice. EMBO J (1988) 7:3705-10.
41. Tornberg UC, Holmberg D. B-1a, B-1b and B-2 B cells display unique VHDJH repertoires formed at different stages of ontogeny and under different selection pressures. EMBO J (1995) 14:1680-9.
42. Stall AM, Farinas MC, Tarlinton DM, Lalor PA, Herzenberg LA, Strober S, et al. Ly-1 B-cell clones similar to human chronic lymphocytic leukemias routinely develop in older normal mice and young autoimmune (New Zealand Black-related) animals. Proc Natl Acad Sci U S A (1988) 85:7312-6. doi:10.1073/pnas.85.19.7312.
43. Gu H, Forster I, Rajewsky K. Sequence homologies, N sequence insertion and JH gene utilization in VHDJH joining: implications for the joining mechanism and the ontogenetic timing of Ly1 B cell and B-CLL progenitor generation. EMBO J (1990) 9:2133-40.
44. Wasserman R, Li YS, Shinton SA, Carmack CE, Manser T, Wiest DL, et al. A novel mechanism for B cell repertoire maturation based on response by B cell precursors to pre-B receptor assembly. J Exp Med (1998) 187:259-64. doi:10.1084/jem.187.2.259.
45. Hardy RR. Development of VH11+ B cells: a model for selection of B cells producing natural autoantibodies. Curr Dir Autoimmun (2003) 6:196-211. doi:10.1159/000066862.
46. Nguyen TT, Elsner RA, Baumgarth N. Natural IgM prevents autoimmunity by enforcing B cell central tolerance induction. J Immunol (2015) 194:1489-502. doi:10.4049/jimmunol.1401880.
47. Zhong X, Tumang JR, Gao W, Bai C, Rothstein TL. PD-L2 expression extends beyond dendritic cells/macrophages to B1 cells enriched for V(H)11/V(H)12 and phosphatidylcholine binding. Eur J Immunol (2007) 37:2405-10. doi:10.1002/eji.200737461.
48. Zhong X, Lau S, Bai C, Degauque N, Holodick NE, Steven SJ, et al. A novel subpopulation of B-1 cells is enriched with autoreactivity in normal and lupus-prone mice. Arthritis Rheum (2009) 60:3734-43. doi:10.1002/art.25015.
49. O'Garra A, Chang R, Go N, Hastings R, Haughton G, Howard M. Ly-1 B (B-1) cells are the main source of B cell-derived interleukin 10. Eur J Immunol (1992) 22:711-7. doi:10.1002/eji.1830220314.
50. Kaku H, Cheng KF, Al-Abed Y, Rothstein TL. A novel mechanism of B cell-mediated immune suppression through CD73 expression and adenosine production. J Immunol (2014) 193:5904-13. doi:10.4049/jimmunol.1400336.
51. Wang H, Shin DM, Abbasi S, Jain S, Kovalchuk AL, Beaty N, et al. Expression of plasma cell alloantigen 1 defines layered development of B-1a B-cell subsets with distinct innate-like functions. Proc Natl Acad Sci U S A (2012) 109:20077-82. doi:10.1073/pnas.1212428109.
52. Enghard P, Humrich JY, Chu VT, Grussie E, Hiepe F, Burmester GR, et al. Class switching and consecutive loss of dsDNA-reactive B1a B cells from the peritoneal cavity during murine lupus development. Eur J Immunol (2010) 40:1809-18. doi:10.1002/eji.200940050.
53. Boes M, Prodeus AP, Schmidt T, Carroll MC, Chen J. A critical role of natural immunoglobulin M in immediate defense against systemic bacterial infection. J Exp Med (1998) 188:2381-6. doi:10.1084/jem.188.12.2381.
54. Mehrad B, Park SJ, Akangire G, Standiford TJ, Wu T, Zhu J, et al. The lupus-susceptibility locus, Sle3, mediates enhanced resistance to bacterial infections. J Immunol (2006) 176:3233-9. doi:10.4049/jimmunol.176.5.3233.