Early BAFF receptor blockade mitigates murine Sjögren's syndrome: Concomitant targeting of CXCL13 and the BAFF receptor prevents salivary hypofunction

Clinical Immunology

Volumn 164, Issue , 2016, Pages 85-94

  Sharma, Arjun ^a   Kiripolsky, Jeremy ^a,g   Klimatcheva, Ekaterina ^b   Howell, Alan ^b   Fereidouni, Farzad ^c   Levenson, Richard ^c   Rothstein, Thomas L ^d,e   Kramer, Jill M ^a,d,e,f  

^a UNIVERSITY AT BUFFALO   (United States)

^b VACCINEX INC   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

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

^f Northwell Health   (United States)

^g ROSWELL PARK CANCER INSTITUTE   (United States)

Author keywords

Autoantibody; BAFF receptor; CXCL13; Salivary hypofunction; Sialadenitis; Sj gren's syndrome

Indexed keywords

AUTOANTIBODY; B CELL ACTIVATING FACTOR RECEPTOR; B CELL ACTIVATING FACTOR RECEPTOR BLOCKING AGENT; CXCL13 ANTIBODY; CXCL13 CHEMOKINE; CYTOKINE RECEPTOR ANTAGONIST; IMMUNOGLOBULIN; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN M ANTIBODY; MONOCLONAL ANTIBODY; UNCLASSIFIED DRUG; ANTIBODY; CXCL13 PROTEIN, MOUSE; TNFRSF13C PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY BLOOD LEVEL; ANTIBODY TITER; ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; DISEASE COURSE; DRUG EFFICACY; DRUG TARGETING; FEMALE; IMMUNOGLOBULIN BLOOD LEVEL; LYMPHOCYTE COUNT; MOUSE; NONHUMAN; NONOBESE DIABETIC MOUSE; PRIORITY JOURNAL; RECEPTOR BLOCKING; SALIVARY GLAND DISEASE; SALIVARY HYPOFUNCTION; SALIVATION; SIALOADENITIS; SIGNAL TRANSDUCTION; SJOEGREN SYNDROME; ANIMAL; ANTAGONISTS AND INHIBITORS; DISEASE MODEL; IMMUNOLOGY; METABOLISM; PATHOLOGY; PHYSIOLOGY; SALIVA; SALIVARY GLAND; SIALADENITIS; SJOGREN'S SYNDROME;

ANIMALS; ANTIBODIES; B-CELL ACTIVATION FACTOR RECEPTOR; CHEMOKINE CXCL13; DISEASE MODELS, ANIMAL; FEMALE; MICE; MICE, INBRED NOD; SALIVA; SALIVARY GLANDS; SIALADENITIS; SJOGREN'S SYNDROME;

EID: 84957899995     PISSN: 15216616     EISSN: 15217035     Source Type: Journal    
DOI: 10.1016/j.clim.2016.01.015     Document Type: Article

References (69)

1. Low H.Z., Witte T. Aspects of innate immunity in Sjögren's syndrome. Arthritis Res. Ther. 2011, 13:218.
2. Mavragani C.P., Moutsopoulos H.M. Sjögren's syndrome. Annu. Rev. Pathol. 2014, 9:273-285.
3. Daniels T.E., Cox D., Shiboski C.H., Schiødt M., Wu A., Lanfranchi H., Umehara H., Zhao Y., Challacombe S., Lam M.Y., De Souza Y., Schiødt J., Holm H., Bisio P.A., Gandolfo M.S., Sawaki T., Li M., Zhang W., Varghese-Jacob B., Ibsen P., Keszler A., Kurose N., Nojima T., Odell E., Criswell L.A., Jordan R., Greenspan J.S., S.s.I.C.C.A.R.Groups Associations between salivary gland histopathologic diagnoses and phenotypic features of Sjögren's syndrome among 1726 registry participants. Arthritis Rheum. 2011, 63:2021-2030.
4. Vitali C., Bombardieri S., Jonsson R., Moutsopoulos H.M., Alexander E.L., Carsons S.E., Daniels T.E., Fox P.C., Fox R.I., Kassan S.S., Pillemer S.R., Talal N., Weisman M.H., E.S.G.o.C.C.f.S.s.Syndrome Classification criteria for Sjögren's syndrome: a revised version of the European criteria proposed by the American-European Consensus Group. Ann. Rheum. Dis. 2002, 61:554-558.
5. Shiboski S.C., Shiboski C.H., Criswell L., Baer A., Challacombe S., Lanfranchi H., Schiødt M., Umehara H., Vivino F., Zhao Y., Dong Y., Greenspan D., Heidenreich A.M., Helin P., Kirkham B., Kitagawa K., Larkin G., Li M., Lietman T., Lindegaard J., McNamara N., Sack K., Shirlaw P., Sugai S., Vollenweider C., Whitcher J., Wu A., Zhang S., Zhang W., Greenspan J., Daniels T., S.s.I.C.C.A.S.R.Groups American College of Rheumatology classification criteria for Sjögren's syndrome: a data-driven, expert consensus approach in the Sjögren's International Collaborative Clinical Alliance cohort. Arthritis Care Res. (Hoboken) 2012, 64:475-487.
6. Christodoulou M.I., Kapsogeorgou E.K., Moutsopoulos H.M. Characteristics of the minor salivary gland infiltrates in Sjögren's syndrome. J. Autoimmun. 2010, 34:400-407.
7. Tengnér P., Halse A.K., Haga H.J., Jonsson R., Wahren-Herlenius M. Detection of anti-Ro/SSA and anti-La/SSB autoantibody-producing cells in salivary glands from patients with Sjögren's syndrome. Arthritis Rheum. 1998, 41:2238-2248.
8. Halse A., Harley J.B., Kroneld U., Jonsson R. Ro/SS-A-reactive B lymphocytes in salivary glands and peripheral blood of patients with Sjögren's syndrome. Clin. Exp. Immunol. 1999, 115:203-207.
9. Hansen A., Lipsky P.E., Dörner T. B cells in Sjögren's syndrome: indications for disturbed selection and differentiation in ectopic lymphoid tissue. Arthritis Res. Ther. 2007, 9:218.
10. Hansen A., Odendahl M., Reiter K., Jacobi A.M., Feist E., Scholze J., Burmester G.R., Lipsky P.E., Dorner T. Diminished peripheral blood memory B cells and accumulation of memory B cells in the salivary glands of patients with Sjögren's syndrome. Arthritis Rheum. 2002, 46:2160-2171.
11. Roberts M.E., Kaminski D., Jenks S.A., Maguire C., Ching K., Burbelo P.D., Iadarola M.J., Rosenberg A., Coca A., Anolik J., Sanz I. Primary Sjögren's syndrome is characterized by distinct phenotypic and transcriptional profiles of IgD+ unswitched memory B cells. Arthritis Rheumatol. 2014, 66:2558-2569.
12. Hansen A., Reiter K., Ziprian T., Jacobi A., Hoffmann A., Gosemann M., Scholze J., Lipsky P.E., Dorner T. Dysregulation of chemokine receptor expression and function by B cells of patients with primary Sjögren's syndrome. Arthritis Rheum. 2005, 52:2109-2119.
13. Youinou P., Devauchelle V., Hutin P., Le Berre R., Saraux A., Pers J.O. A conspicuous role for B cells In Sjögren's syndrome. Clin. Rev. Allergy Immunol. 2007, 32:231-237.
14. Mackay F., Woodcock S.A., Lawton P., Ambrose C., Baetscher M., Schneider P., Tschopp J., Browning J.L. Mice transgenic for BAFF develop lymphocytic disorders along with autoimmune manifestations. J. Exp. Med. 1999, 190:1697-1710.
15. Lied G.A., Berstad A. Functional and clinical aspects of the B-cell-activating factor (BAFF): a narrative review. Scand. J. Immunol. 2011, 73:1-7.
16. Moisini I., Davidson A. BAFF: a local and systemic target in autoimmune diseases. Clin. Exp. Immunol. 2009, 158:155-163.
17. Morimoto S., Nakano S., Watanabe T., Tamayama Y., Mitsuo A., Nakiri Y., Suzuki J., Nozawa K., Amano H., Tokano Y., Kobata T., Takasaki Y. Expression of B-cell activating factor of the tumour necrosis factor family (BAFF) in T cells in active systemic lupus erythematosus: the role of BAFF in T cell-dependent B cell pathogenic autoantibody production. Rheumatology (Oxford) 2007, 46:1083-1086.
18. Ng L.G., Sutherland A.P., Newton R., Qian F., Cachero T.G., Scott M.L., Thompson J.S., Wheway J., Chtanova T., Groom J., Sutton I.J., Xin C., Tangye S.G., Kalled S.L., Mackay F., Mackay C.R. B cell-activating factor belonging to the TNF family (BAFF)-is the principal BAFF receptor facilitating BAFF costimulation of circulating T and B cells. J. Immunol. 2004, 173:807-817.
19. Mackay F., Schneider P. Cracking the BAFF code. Nat. Rev. Immunol. 2009, 9:491-502.
20. Enzler T., Bonizzi G., Silverman G.J., Otero D.C., Widhopf G.F., Anzelon-Mills A., Rickert R.C., Karin M. Alternative and classical NF-kappa B signaling retain autoreactive B cells in the splenic marginal zone and result in lupus-like disease. Immunity 2006, 25:403-415.
21. Thompson J.S., Bixler S.A., Qian F., Vora K., Scott M.L., Cachero T.G., Hession C., Schneider P., Sizing I.D., Mullen C., Strauch K., Zafari M., Benjamin C.D., Tschopp J., Browning J.L., Ambrose C. BAFF-R, a newly identified TNF receptor that specifically interacts with BAFF. Science 2001, 293:2108-2111.
22. Thien M., Phan T.G., Gardam S., Amesbury M., Basten A., Mackay F., Brink R. Excess BAFF rescues self-reactive B cells from peripheral deletion and allows them to enter forbidden follicular and marginal zone niches. Immunity 2004, 20:785-798.
23. Daridon C., Devauchelle V., Hutin P., Le Berre R., Martins-Carvalho C., Bendaoud B., Dueymes M., Saraux A., Youinou P., Pers J.O. Aberrant expression of BAFF by B lymphocytes infiltrating the salivary glands of patients with primary Sjögren's syndrome. Arthritis Rheum. 2007, 56:1134-1144.
24. Gottenberg J.E., Cagnard N., Lucchesi C., Letourneur F., Mistou S., Lazure T., Jacques S., Ba N., Ittah M., Lepajolec C., Labetoulle M., Ardizzone M., Sibilia J., Fournier C., Chiocchia G., Mariette X. Activation of IFN pathways and plasmacytoid dendritic cell recruitment in target organs of primary Sjögren's syndrome. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:2770-2775.
25. Groom J., Kalled S.L., Cutler A.H., Olson C., Woodcock S.A., Schneider P., Tschopp J., Cachero T.G., Batten M., Wheway J., Mauri D., Cavill D., Gordon T.P., Mackay C.R., Mackay F. Association of BAFF/BLyS overexpression and altered B cell differentiation with Sjögren's syndrome. J. Clin. Invest. 2002, 109:59-68.
26. Szodoray P., Alex P., Jonsson M.V., Knowlton N., Dozmorov I., Nakken B., Delaleu N., Jonsson R., Centola M. Distinct profiles of Sjögren's syndrome patients with ectopic salivary gland germinal centers revealed by serum cytokines and BAFF. Clin. Immunol. 2005, 117:168-176.
27. Killedar S.J., Eckenrode S.E., McIndoe R.A., She J.X., Nguyen C.Q., Peck A.B., Cha S. Early pathogenic events associated with Sjögren's syndrome (SjS)-like disease of the NOD mouse using microarray analysis. Lab. Investig. 2006, 86:1243-1260.
28. Pereira J.P., Kelly L.M., Cyster J.G. Finding the right niche: B-cell migration in the early phases of T-dependent antibody responses. Int. Immunol. 2010, 22:413-419.
29. Förster R., Emrich T., Kremmer E., Lipp M. Expression of the G-protein-coupled receptor BLR1 defines mature, recirculating B cells and a subset of T-helper memory cells. Blood 1994, 84:830-840.
30. Kramer J.M., Klimatcheva E., Rothstein T.L. CXCL13 is elevated in Sjögren's syndrome in mice and humans and is implicated in disease pathogenesis. J. Leukoc. Biol. 2013, 94:1079-1089.
31. Barone F., Bombardieri M., Manzo A., Blades M.C., Morgan P.R., Challacombe S.J., Valesini G., Pitzalis C. Association of CXCL13 and CCL21 expression with the progressive organization of lymphoid-like structures in Sjögren's syndrome. Arthritis Rheum. 2005, 52:1773-1784.
32. Salomonsson S., Jonsson M.V., Skarstein K., Brokstad K.A., Hjelmström P., Wahren-Herlenius M., Jonsson R. Cellular basis of ectopic germinal center formation and autoantibody production in the target organ of patients with Sjögren's syndrome. Arthritis Rheum. 2003, 48:3187-3201.
33. Barone F., Bombardieri M., Rosado M.M., Morgan P.R., Challacombe S.J., De Vita S., Carsetti R., Spencer J., Valesini G., Pitzalis C. CXCL13, CCL21, and CXCL12 expression in salivary glands of patients with Sjögren's syndrome and MALT lymphoma: association with reactive and malignant areas of lymphoid organization. J. Immunol. 2008, 180:5130-5140.
34. Amft N., Curnow S.J., Scheel-Toellner D., Devadas A., Oates J., Crocker J., Hamburger J., Ainsworth J., Mathews J., Salmon M., Bowman S.J., Buckley C.D. Ectopic expression of the B cell-attracting chemokine BCA-(CXCL13) on endothelial cells and within lymphoid follicles contributes to the establishment of germinal center-like structures in Sjögren's syndrome. Arthritis Rheum. 2001, 44:2633-2641.
35. Hjelmervik T.O., Petersen K., Jonassen I., Jonsson R., Bolstad A.I. Gene expression profiling of minor salivary glands clearly distinguishes primary Sjögren's syndrome patients from healthy control subjects. Arthritis Rheum. 2005, 52:1534-1544.
36. Fava R.A., Kennedy S.M., Wood S.G., Bolstad A.I., Bienkowska J., Papandile A., Mavragani C.P., Gatumu M., Skarstein K., Kelly J.A., Browning J.L. Lymphotoxin-beta receptor blockade reduces CXCL13 in lacrimal glands and improves corneal integrity in the NOD Model of Sjögren's syndrome. Arthritis Res. Ther. 2011, 13:R182.
37. Gatumu M.K., Skarstein K., Papandile A., Browning J.L., Fava R.A., Bolstad A.I. Blockade of lymphotoxin-beta receptor signaling reduces aspects of Sjögren's syndrome in salivary glands of non-obese diabetic mice. Arthritis Res. Ther. 2009, 11:R24.
38. Badr G., Borhis G., Lefevre E.A., Chaoul N., Deshayes F., Dessirier V., Lapree G., Tsapis A., Richard Y. BAFF enhances chemotaxis of primary human B cells: a particular synergy between BAFF and CXCL13 on memory B cells. Blood 2008, 111:2744-2754.
39. Digman M.A., Caiolfa V.R., Zamai M., Gratton E. The phasor approach to fluorescence lifetime imaging analysis. Biophys. J. 2008, 94:L14-L16.
40. Fereidouni F., Esposito A., Blab G.A., Gerritsen H.C. A modified phasor approach for analyzing time-gated fluorescence lifetime images. J. Microsc. 2011, 244:248-258.
41. Fereidouni F., Bader A.N., Gerritsen H.C. Spectral phasor analysis allows rapid and reliable unmixing of fluorescence microscopy spectral images. Opt. Express 2012, 20:12729-12741.
42. Fereidouni F., Bader A.N., Colonna A., Gerritsen H.C. Phasor analysis of multiphoton spectral images distinguishes autofluorescence components of in vivo human skin. J. Biophotonics 2014, 7:589-596.
43. Cha S., Peck A.B., Humphreys-Beher M.G. Progress in understanding autoimmune exocrinopathy using the non-obese diabetic mouse: an update. Crit. Rev. Oral Biol. Med. 2002, 13:5-16.
44. Malladi A.S., Sack K.E., Shiboski S.C., Shiboski C.H., Baer A.N., Banushree R., Dong Y., Helin P., Kirkham B.W., Li M., Sugai S., Umehara H., Vivino F.B., Vollenweider C.F., Zhang W., Zhao Y., Greenspan J.S., Daniels T.E., Criswell L.A. Primary Sjögren's syndrome as a systemic disease: a study of participants enrolled in an international Sjögren's syndrome registry. Arthritis Care Res. (Hoboken) 2012, 64:911-918.
45. Qi G., Hua H., Gao Y., Lin Q., Yu G.Y. Sialoadenitis progression in nonobese diabetic mice and its correlation with expression of apoptosis-associated proteins in salivary glands and serum IgG levels. Chin. Med. J. 2007, 120:1426-1431.
46. Ittah M., Miceli-Richard C., Eric Gottenberg J., Lavie F., Lazure T., Ba N., Sellam J., Lepajolec C., Mariette X. B cell-activating factor of the tumor necrosis factor family (BAFF) is expressed under stimulation by interferon in salivary gland epithelial cells in primary Sjögren's syndrome. Arthritis Res. Ther. 2006, 8:R51.
47. Salomonsson S., Larsson P., Tengnér P., Mellquist E., Hjelmström P., Wahren-Herlenius M. Expression of the B cell-attracting chemokine CXCL13 in the target organ and autoantibody production in ectopic lymphoid tissue in the chronic inflammatory disease Sjögren's syndrome. Scand. J. Immunol. 2002, 55:336-342.
48. Vosters J.L., Roescher N., Illei G.G., Chiorini J.A., Tak P.P. TACI-Fc gene therapy improves autoimmune sialadenitis but not salivary gland function in non-obese diabetic mice. Oral Dis. 2012, 18:365-374.
49. Ivanov I.I., Atarashi K., Manel N., Brodie E.L., Shima T., Karaoz U., Wei D., Goldfarb K.C., Santee C.A., Lynch S.V., Tanoue T., Imaoka A., Itoh K., Takeda K., Umesaki Y., Honda K., Littman D.R. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 2009, 139:485-498.
50. Ivanov I.I., Frutos Rde L., Manel N., Yoshinaga K., Rifkin D.B., Sartor R.B., Finlay B.B., Littman D.R. Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe 2008, 4:337-349.
51. Atarashi K., Nishimura J., Shima T., Umesaki Y., Yamamoto M., Onoue M., Yagita H., Ishii N., Evans R., Honda K., Takeda K. ATP drives lamina propria T(H)17 cell differentiation. Nature 2008, 455:808-812.
52. Wang Z., Friedrich C., Hagemann S.C., Korte W.H., Goharani N., Cording S., Eberl G., Sparwasser T., Lochner M. Regulatory T cells promote a protective Th17-associated immune response to intestinal bacterial infection with C. rodentium. Mucosal Immunol. 2014.
53. Darce J.R., Arendt B.K., Wu X., Jelinek D.F. Regulated expression of BAFF-binding receptors during human B cell differentiation. J. Immunol. 2007, 179:7276-7286.
54. Legler D.F., Loetscher M., Roos R.S., Clark-Lewis I., Baggiolini M., Moser B. B cell-attracting chemokine 1, a human CXC chemokine expressed in lymphoid tissues, selectively attracts B lymphocytes via BLR1/CXCR5. J. Exp. Med. 1998, 187:655-660.
55. Ansel K.M., Ngo V.N., Hyman P.L., Luther S.A., Förster R., Sedgwick J.D., Browning J.L., Lipp M., Cyster J.G. A chemokine-driven positive feedback loop organizes lymphoid follicles. Nature 2000, 406:309-314.
56. Rubin R.L., Tang F.L., Chan E.K., Pollard K.M., Tsay G., Tan E.M. IgG subclasses of autoantibodies in systemic lupus erythematosus, Sjögren's syndrome, and drug-induced autoimmunity. J. Immunol. 1986, 137:2528-2534.
57. Maran R., Dueymes M., Pennec Y.L., Casburn-Budd R., Shoenfeld Y., Youinou P. Predominance of IgG1 subclass of anti-Ro/SSA, but not anti-La/SSB antibodies in primary Sjögren's syndrome. J. Autoimmun. 1993, 6:379-387.
58. Nguyen C.Q., Ogunniyi A.O., Karabiyik A., Love J.C. Single-cell analysis reveals isotype-specific autoreactive B cell repertoires in Sjögren's syndrome. PLoS One 2013, 8:e58127.
59. Robinson C.P., Brayer J., Yamachika S., Esch T.R., Peck A.B., Stewart C.A., Peen E., Jonsson R., Humphreys-Beher M.G. Transfer of human serum IgG to nonobese diabetic Igmu null mice reveals a role for autoantibodies in the loss of secretory function of exocrine tissues in Sjögren's syndrome. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:7538-7543.
60. Dawson L.J., Stanbury J., Venn N., Hasdimir B., Rogers S.N., Smith P.M. Antimuscarinic antibodies in primary Sjögren's syndrome reversibly inhibit the mechanism of fluid secretion by human submandibular salivary acinar cells. Arthritis Rheum. 2006, 54:1165-1173.
61. Jin M., Hwang S.M., Koo N.Y., Kim B., Kho H.S., Choi S.Y., Song Y.W., Park K. Autoantibodies in Sjögren's syndrome patients acutely inhibit muscarinic receptor function. Oral Dis. 2012, 18:132-139.
62. Waterman S.A., Gordon T.P., Rischmueller M. Inhibitory effects of muscarinic receptor autoantibodies on parasympathetic neurotransmission in Sjögren's syndrome. Arthritis Rheum. 2000, 43:1647-1654.
63. He J., Qiang L., Ding Y., Wei P., Li Y.N., Hua H., Li Z.G. The role of muscarinic acetylcholine receptor type 3 polypeptide (M3RP205-220) antibody in the saliva of patients with primary Sjögren's syndrome. Clin. Exp. Rheumatol. 2012, 30:322-326.
64. Tsuboi H., Matsumoto I., Wakamatsu E., Nakamura Y., Iizuka M., Hayashi T., Goto D., Ito S., Sumida T. New epitopes and function of anti-M3 muscarinic acetylcholine receptor antibodies in patients with Sjögren's syndrome. Clin. Exp. Immunol. 2010, 162:53-61.
65. Szczerba B.M., Kaplonek P., Wolska N., Podsiadlowska A., Rybakowska P.D., Dey P., Rasmussen A., Grundahl K., Hefner K.S., Stone D.U., Young S., Lewis D.M., Radfar L., Scofield R.H., Sivils K.L., Bagavant H., Deshmukh U.S. Interaction between innate immunity and Ro52-induced antibody causes Sjögren's syndrome-like disorder in mice. Ann. Rheum. Dis. 2015.
66. Du M., Diss T.C., Xu C., Peng H., Isaacson P.G., Pan L. Ongoing mutation in MALT lymphoma immunoglobulin gene suggests that antigen stimulation plays a role in the clonal expansion. Leukemia 1996, 10:1190-1197.
67. Martin T., Weber J.C., Levallois H., Labouret N., Soley A., Koenig S., Korganow A.S., Pasquali J.L. Salivary gland lymphomas in patients with Sjögren's syndrome may frequently develop from rheumatoid factor B cells. Arthritis Rheum. 2000, 43:908-916.
68. Hansen A., Gosemann M., Pruss A., Reiter K., Ruzickova S., Lipsky P.E., Dörner T. Abnormalities in peripheral B cell memory of patients with primary Sjögren's syndrome. Arthritis Rheum. 2004, 50:1897-1908.
69. Jonsson R., Theander E., Sjöström B., Brokstad K., Henriksson G. Autoantibodies present before symptom onset in primary Sjögren syndrome. JAMA 2013, 310:1854-1855.