Lack of galectin-1 or galectin-3 alters B cell deletion and anergy in an autoantibody transgene model

Glycobiology

Volumn 23, Issue 7, 2013, Pages 893-903

  Clark, Amy G ^a   Weston, Melissa L ^a   Foster, Mary H ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

autoimmunity; CD62L; CD86; humoral immunity; MHCII

Indexed keywords

AUTOANTIBODY; CD86 ANTIGEN; GALECTIN 1; GALECTIN 3; IMMUNOGLOBULIN M; LAMININ ANTIBODY; LIPOPOLYSACCHARIDE; PROTEIN ANTIBODY; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; B LYMPHOCYTE; B LYMPHOCYTE DIFFERENTIATION; CELL FATE; CELL SURVIVAL; CLONAL ANERGY; CONTROLLED STUDY; GENE DELETION; GENE INACTIVATION; IMMUNOLOGICAL TOLERANCE; LYMPHOCYTE ACTIVATION; LYMPHOCYTE COUNT; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPLEEN CELL; SPLEEN LYMPHOCYTE; SPLEEN WEIGHT; TRANSGENIC MOUSE;

AUTOIMMUNITY; CD62L; CD86; HUMORAL IMMUNITY; MHCII;

ANIMALS; AUTOANTIBODIES; B-LYMPHOCYTES; CLONAL ANERGY; CLONAL DELETION; GALECTIN 1; GALECTIN 3; LAMININ; MICE; MICE, KNOCKOUT; TRANSGENES;

EID: 84882791504     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwt026     Document Type: Article

References (58)

1. Acosta-Rodriguez EV, Montes CL, Motran CC, Zuniga EI, Liu FT, Rabinovich GA, Gruppi A. 2004. Galectin-3 mediates IL-4-induced survival and differentiation of B cells: Functional cross-talk and implications during Trypanosoma cruzi infection. J Immunol. 172:493-502.
2. Amital H, Heilweil-Harel M, Ulmansky R, Harlev M, Toubi E, Hershko A, Naparstek Y. 2007. Antibodies against the VRT101 laminin epitope correlate with human SLE disease activity and can be removed by extracorporeal immunoadsorption. Rheumatology (Oxford). 46: 1433-1437.
3. Barboni EAM, Bawumia S, Hughes RC. 1999. Kinetic measurements of binding of galectin 3 to a laminin substratum. Glycoconj J. 16:365-373.
4. Barrionuevo P, Beigier-Bompadre M, Ilarregui JM, Toscano MA, Bianco GA, Isturiz MA, Rabinovich GA. 2007. A novel function for galectin-1 at the crossroad of innate and adaptive immunity: Galectin-1 regulates monocyte/ macrophage physiology through a nonapoptotic ERK-dependent pathway. J Immunol. 178:436-445.
5. Baum LG, Blackall DP, Arias-Magallano S, Nanigian D, Uh SY, Browne JM, Hoffmann D, Emmanouilides CE, Territo MC, Baldwin GC. 2003. Amelioration of graft versus host disease by galectin-1. Clin Immunol. 109:295-307.
6. Borriello F, Sethna MP, Boyd SD, Schweitzer AN, Tivol EA, Jacoby D, Strom TB, Simpson EM, Freeman GJ, Sharpe AH. 1997. B7-1 and B7-2 have overlapping, critical roles in immunoglobulin class switching and germinal center formation. Immunity. 6:303.
7. Brady GF, Congdon KL, Clark AG, Sackey FN, Rudolph EH, Radic MZ, Foster MH. 2004. Kappa editing rescues autoreactive B cells destined for deletion in mice transgenic for a dual specific anti-laminin Ig. J Immunol. 172:5313-5321.
8. Charles ED, Brunetti C, Marukian S, Ritola KD, Talal AH, Marks K, Jacobson IM, Rice CM, Dustin LB. 2011. Clonal B cells in patients with hepatitis C virus-associated mixed cryoglobulinemia contain an expanded anergic CD21low B-cell subset. Blood. 117:5425-5437.
9. Clark AG, Chen S, Zhang H, Brady GF, Ungewitter EK, Bradley JK, Sackey FN, Foster MH. 2007. Multifunctional regulators of cell growth are differentially expressed in anergic murine B cells. Mol Immunol. 44:1274-1285.
10. Clark AG, Mackin KM, Foster MH. 2011. Genetic elimination of alpha3(IV) collagen fails to rescue anti-collagen B cells. Immunol Lett. 141:134-139.
11. Colnot C, Fowlis D, Ripoche MA, Bouchaert I, Poirier F. 1998. Embryonic implantation in galectin 1/galectin 3 double mutant mice. Dev Dyn. 211:306-313.
12. Damle NK, Klussman K, Linsley PS, Aruffo A. 1992. Differential costimulatory effects of adhesion molecules B6, ICAM-1, LFA-3, and VCAM-1 on resting and antigen-primerd CD4+ T lymphocytes. J Immunol. 148:1985-1992.
13. Demetriou M, Granovsky M, Quaggin S, Dennis JW. 2001. Negative regulation of T-cell activation and autoimmunity by Mgat5 N-glycosylation. Nature. 409:733-739.
14. Demotte N, Stroobant V, Courtoy PJ, Van Der Smissen P, Colau D, Luescher IF, Hivroz C, Nicaise J, Squifflet J-L, Mourad M., et al. 2008. Restoring the association of the T cell receptor with CD8 reverses anergy in human tumorinfiltrating lymphocytes. Immunity. 28:414-424.
15. Ellestad KK, Tsutsui S, Noorbakhsh F, Warren KG, Yong VW, Pittman QJ, Power C. 2009. Early life exposure to lipopolysaccharide suppresses experimental autoimmune encephalomyelitis by promoting tolerogenic dendritic cells and regulatory T cells. J Immunol. 183:298-309.
16. Espeli M, Mancini SJC, Breton C, Poirier F, Schiff C. 2009. Impaired B-cell development at the pre-BII-cell stage in galectin-1-deficient mice dur to inefficient pre-BII/stromal cell interactions. Blood. 113:5878-5886.
17. Fitzsimons MM, Chen H, Foster MH. 2000. Diverse endogenous light chains contribute to basement membrane reactivity in nonautoimmune mice transgenic for an anti-laminin Ig heavy chain. Immunogenetics. 51:20-29.
18. Forsman H, Islander U, Andreasson E, Andersson A, Onnheim K, Karlstrom A, Savman K, Magnusson M, Brown KL, Karlsson A. 2011. Galectin 3 aggravates joint inflammation and destruction in antigen-induced arthritis. Arthritis Rheum. 63:445-454.
19. Foster MH, Fitzsimons MM. 1998. Lupus-like nephrotropic autoantibodies in nonautoimmune mice harboring an anti-laminin Ig heavy chain transgene. Mol Immunol. 35:83-94.
20. Foster MH, Sabbaga J, Line SRP, Thompson KS, Barrett KJ, Madaio MP. 1993. Molecular analysis of nephrotropic anti-laminin antibodies from an MRL/lpr autoimmune mouse. J Immunol. 151:814-824.
21. Freeman GJ, Borriello F, Hodes RJ, Reiser H, Gribben JG, Ng JW, Kim J, Goldberg JM, Hathcock K, Laszlo G., et al. 1993. Murine B7-2, an alternative CTLA4 counter-receptor that costimulates T cell proliferation and interleukin-2 production. J Exp Med. 178:2185.
22. Fulcher JA, Hashimi ST, Levroney EL, Pang M, Gurney KB, Baum LG, Lee B. 2006. Galectin-1-matured human monocyte-derived dendritic cells have enhanced migration through extracellular matrix. J Immunol. 177:216-226.
23. Futata EA, de Brito CA, Victor JR, Fusar AE, Oliveira CR, Maciel J. M., da Silva Duarte AJ, Sato MN. 2006. Long-term anergy in orally tolerized mice is linked to decreased B7.2 expression on B cells. Immunobiology. 211:157-166.
24. Gil CD, Gullo CE, Oliani SM. 2011. Effect of exogenous galectin-1 on leukocyte migration: Modulation of cytokine levels and adhesion molecules. Int J Clin Exp Pathol. 4:74-84.
25. Hanrotel-Saliou C, Segalen I, Le Meur Y, Youinou P, Renaudineau Y. 2011. Glomerular antibodies in lupus nephritis. Clinic Rev Allerg Immunol. 40:151-158.
26. Hartley S, Cooke M, Fulcher D, Harris A, Cory S, Basten A, Goodnow C. 1993. Elimination of self-reactive B lymphocytes proceeds in two stages: Arrested development and cell death. Cell. 72:325-335.
27. Hernandez JD, Baum LG. 2002. Ah, sweet mystery of death! Galectins and control of cell fate. Glycobiology. 12:127R-136R.
28. Hoyer KK, Pang M, Gui D, Shintaku IP, Kuwabara I, Liu FT, Said JW, Baum LG, Teitell MA. 2004. An anti-apoptotic role for galectin-3 in diffuse large B-cell lymphomas. Am J Pathol. 164:893-902.
29. Hsu DK, Yang RY, Pan Z, Yu L, Salomon DR, Fung-Leung WP, Liu FT. 2000. Targeted disruption of the galectin-3 gene results in attenuated peritoneal inflammatory responses. Am J Pathol. 156:1073-1083.
30. Jiang H-R, Rasebi ZA, Mensah-Brown E, Shahin A, Xu D, Goodyear CS, Fukada SY, Liu F-T, Liew FY, Lukic ML. 2009. Galectin-3 deficiency reduces the severity of experimental autoimmune encephalomyelitis. J Immunol. 182:1167-1173.
31. Kang EH, Moon KC, Lee EY, Lee YJ, Lee EB, Ahn C, Song YW. 2009. Renal expression of galectin-3 in systemic lupus erythematosus patients with nephritis. Lupus. 18:22-28.
32. Kuo P-L, Hung J-Y, Huang S-K, Chou S-H, Cheng D-E, Jong Y-J, Hung C-H, Yang C-J, Tsai Y-M, Hsu Y-L., et al. 2011. Lung cancer-derived galectin-1 mediates dendritic cell anergy through inhibitor of DNA binding 3/IL-10 signaling pathway. J Immunol. 186:1521-1530.
33. Lenschow D, Sperling A, Cooke M, Freeman G, Rhee L, Decker D, Gray G, Nadler L, Goodnow C, Bluestone J. 1994. Differential up-regulation of the B7-1 and B7-2 costimulatory molecules after Ig receptor engagement by antigen. J Immunol. 153:1990-1997.
34. Liu SD, Lee S, La Cava A, Motran CC, Hahn BH, Miceli MC. 2011. Galectin-1-induced down-regulation of T lymphocyte activation protects (NZB x NZW) F1 mice from lupus-like disease. Lupus. 20:473-484.
35. Liu FT, Rabinovich GA. 2005. Galectins as modulators of tumour progression. Nat Rev Cancer. 5:29-41.
36. Mourcin F, Breton C, Tellier J, Narang P, Chasson L, Jorquera A, Coles M, Schiff C, Mancini SJC. 2011. Galectin-1-expressing stromal cells constitute a specific niche for pre-BII cell development in mouse bone marrow. Blood. 117:6552-6561.
37. Oliveira FL, Brand C, Paula AA, Arcanjo KD, Hsu DK, Liu F-T, Takiya CM, Borojevic R, Chammas R, El-Cheikh MC. 2011. Lack of galectin-3 disturbs mesenteric lymph node homeostasis and B cell niches in the course of Schistosoma mansoni infection. PLoS One. 6:e19216.
38. Oliveira FL, Chammas R, Hsu DK, Liu FT, Borojevic R, Takiya CM, El-Cheikh MC. 2007. Kinetics of mobilization and differentiation of lymphohematopoietic cells during experimental murine schistosomiasis in galectin-3-/- mice. J Leukocyte Biol. 82:300-310.
39. Oliveira FL, Chammas R, Ricon L, Fermino ML, Bernardes ES, Hsu DK, Liu F-T, Borojevic R, El-Cheikh MC. 2009. Galectin-3 regulates peritoneal B1-cell differentiation into plasma cells. Glycobiology. 19:1248-1258.
40. Patterson RJ, Wang W, Wang JL. 2004. Understanding the biochemical activities of galectin-1 and galectin-3 in the nucleus. Glycoconj J. 19:499-506.
41. Poirier F, Robertson EJ. 1993. Normal development of mice carrying a null mutation in the gene encoding the L14 S-type lectin. Development. 119:1229-1236.
42. Rabinovich GA, Daly G, Dreja H, Tailor H, Riera CM, Hirabayashi J, Chernajovsky Y. 1999. Recombinant galectin-1 and its genetic delivery suppress collagen-induced arthritis via T cell apoptosis. J Exp Med. 190:385-398.
43. Rabinovich GA, Sotomayor CE, Riera CM, Bianco I, Correa SG. 2000. Evidence of a role for galectin-1 in acute inflammation. Eur J Immunol. 30:1331-1339.
44. Rabinovich GA, Toscano MA. 2009. Turning 'sweet' on immunity: Galectin-glycan interactions in immune tolerance and inflammation. Nat Rev Immunol. 9:338-352.
45. Rabinovich GA, van Kooyk Y, Cobb BA. 2012. Glycobiology of immune responses. Ann N Y Acad Sci. 1253:1-15.
46. Rathmell J, Fournier S, Weintraub B, Allison J, Goodnow CC. 1998. Repression of B7.2 on self-reactive B cells is essential to prevent proliferation and allow Fas-mediated deletion by CD4(+) T cells. J Exp Med. 188:651-659.
47. Reichert RA, Gallatin WM, Weissman IL, Butcher EC. 1983. Germinal center B cells lack homing receptors necessary for normal lymphocyte recirculation. J Exp Med. 157:813-827.
48. Rudolph EH, Congdon KL, Sackey FN, Fitzsimons MM, Foster MH. 2002. Humoral autoimmunity to basement membrane antigens is regulated in C57BL/6 and MRL/MpJ mice transgenic for anti-laminin Ig receptors. J Immunol. 168:5943-5953.
49. Santucci L, Fiorucci S, Cammilleri F, Servillo G, Federici B, Morelli A. 2000. Galectin-1 exerts immunomodulatory and protective effects on concanavalin A-induced hepatitis in mice. Hepatology. 31:399-406.
50. Santucci L, Fiorucci S, Rubinstein N, Mencarelli A, Palazzetti B, Federici B, Rabinovich GA, Morelli A. 2003. Galectin-1 suppresses experimental colitis in mice. Gastroenterology. 124:1381-1394.
51. Stillman BN, Hsu DK, Pang M, Brewer CF, Johnson P, Liu FT, Baum LG. 2006. Galectin-3 and galectin-1 bind distinct cell surface glycoprotein receptors to induce T cell death. J Immunol. 176:778-789.
52. Stowell SR, Qian Y, Karmakar S, Koyama NS, Dias-Baruffi M, Leffler H, McEver RP, Cummings RD. 2008. Differential roles of galectin-1 and galectin-3 in regulating leukocyte viability and cytokine secretion. J Immunol. 180:3091-3102.
53. Tabrizi SJ, Niiro H, Masui M, Yoshimoto G, Iino T, Kikushige Y, Wakasaki T, Baba E, Shimoda S, Miyamoto T., et al. 2009. T cell leukemia/lymphoma 1 and galectin-1 regulate survival/cell death pathways in human naive and IgM+ memory B cells through altering balances in Bcl-2 family proteins. J Immunol. 182:1490-1499.
54. Terrier B, Joly F, Vazquez T, Benech P, Rosenzwajg M, Carpentier W, Garrido M, Ghillani-Dalbin P, Klatzmann D, Cacoub P., et al. 2011. Expansion of functionally anergic CD21-/low marginal zone-like B cell clones in hepatitis C virus infection-related autoimmunity. J Immunol. 187:6550-6563.
55. Tsai C-M, Guan C-H, Hsieh H-W, Hsu T-L, Tu Z, Wu K-J, Lin C-H, Lin K-I. 2011. Galectin-1 and galectin-8 have redundant roles in promoting plasma cell formation. J Immunol. 187:1643-1652.
56. van Kooyk Y, Rabinovich GA. 2008. Protein-glycan interactions in the control of innate and adaptive immune responses. Nat Immunol. 9:593-601.
57. Volarevic V, Milovanovic M, Ljujic B, Pejnovic N, Arsenijevic N, Nilsson U, Leffler H, Lukic ML. 2012. Galectin-3 deficiency prevents concanavalin A-induced hepatitis in mice. Hepatology. 55:1954-1964.
58. Yu X, Siegel R, Roeder RG. 2006. Interaction of the B cell-specific transcriptional coactivator OCA-B and galectin-1 and a possible role in regulating BCR-mediated B cell proliferation. J Biol Chem. 281:15505-15516.