Cytometry by time-of-flight immunophenotyping identifies a blood Sjögren's signature correlating with disease activity and glandular inflammation

Journal of Allergy and Clinical Immunology

Volumn 137, Issue 6, 2016, Pages 1809-1821.e12

  Mingueneau, Michael ^a   Boudaoud, Saida ^b,c   Haskett, Scott ^a   Reynolds, Taylor L ^a   Nocturne, Gaetane ^b,c,d   Norton, Elizabeth ^a   Zhang, Xueli ^a   Constant, Myrtha ^a   Park, Daniel ^a   Wang, Wenting ^a   Lazure, Thierry ^b,c,d   Le Pajolec, Christine ^d   Ergun, Ayla ^a   Mariette, Xavier ^b,c,d  

^a BIOGEN   (United States)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c INSERM   (France)

^d BICÊTRE HOSPITAL   (France)

Author keywords

autoimmunity; biomarker discovery; cytometry by time of flight; immunophenotyping; mass cytometry; patient stratification; Sj gren's syndrome; therapeutic target

Indexed keywords

BIOLOGICAL MARKER;

ARTICLE; B LYMPHOCYTE DIFFERENTIATION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOMETRY; DISEASE ACTIVITY; DISEASE ASSOCIATION; EPITHELIUM CELL; HOSPITAL BASED CASE CONTROL STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOPHENOTYPING; LYMPHOCYTE COUNT; MEMORY CELL; OBSERVATIONAL STUDY; PLASMA CELL; PLASMABLAST; PLASMACYTOID DENDRITIC CELL; PRIMARY SJOEGREN SYNDROME; PRIORITY JOURNAL; SALIVARY GLAND BIOPSY; SIALOADENITIS; SJOEGREN SYNDROME; T LYMPHOCYTE ACTIVATION; TIME OF FLIGHT MASS CYTOMETRY; ADULT; BIOLOGY; BIOPSY; CLUSTER ANALYSIS; FEMALE; FLOW CYTOMETRY; MALE; METABOLISM; MIDDLE AGED; MINOR SALIVA GLAND; PATHOLOGY; PROCEDURES; REPRODUCIBILITY; SALIVARY GLAND; SJOGREN'S SYNDROME;

ADULT; BIOMARKERS; BIOPSY; CD8-POSITIVE T-LYMPHOCYTES; CLUSTER ANALYSIS; COMPUTATIONAL BIOLOGY; FEMALE; FLOW CYTOMETRY; HUMANS; IMMUNOHISTOCHEMISTRY; IMMUNOPHENOTYPING; MALE; MIDDLE AGED; PLASMA CELLS; REPRODUCIBILITY OF RESULTS; SALIVARY GLANDS; SALIVARY GLANDS, MINOR; SJOGREN'S SYNDROME;

EID: 84961904335     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2016.01.024     Document Type: Article

References (47)

1. B. Qin, J. Wang, Z. Yang, M. Yang, N. Ma, F. Huang, and et al. Epidemiology of primary Sjogren's syndrome: a systematic review and meta-analysis Ann Rheum Dis 74 2015 1983 1989
2. G. Nocturne, and X. Mariette Sjogren syndrome-associated lymphomas: an update on pathogenesis and management Br J Haematol 168 2015 317 327
3. G. Nocturne, and X. Mariette Advances in understanding the pathogenesis of primary Sjogren's syndrome Nat Rev Rheumatol 9 2013 544 556
4. B.A. Fisher, R.M. Brown, S.J. Bowman, and F. Barone A review of salivary gland histopathology in primary Sjogren's syndrome with a focus on its potential as a clinical trials biomarker Ann Rheum Dis 74 2015 1645 1650
5. S. Rusakiewicz, G. Nocturne, T. Lazure, M. Semeraro, C. Flament, S. Caillat-Zucman, and et al. NCR3/NKp30 contributes to pathogenesis in primary Sjogren's syndrome Sci Transl Med 5 2013 195ra196
6. S.C. Bendall, E.F. Simonds, P. Qiu, el-AD. Amir, P.O. Krutzik, R. Finck, and et al. Single-cell mass cytometry of differential immune and drug responses across a human hematopoietic continuum Science 332 2011 687 696
7. S.C. Bendall, K.L. Davis, el-AD. Amir, M.D. Tadmor, E.F. Simonds, T.J. Chen, and et al. Single-cell trajectory detection uncovers progression and regulatory coordination in human B cell development Cell 157 2014 714 725
8. J.H. Levine, E.F. Simonds, S.C. Bendall, K.L. Davis, el-AD. Amir, M.D. Tadmor, and et al. Data-driven phenotypic dissection of AML reveals progenitor-like cells that correlate with prognosis Cell 162 2015 184 197
9. E.W. Newell, N. Sigal, S.C. Bendall, G.P. Nolan, and M.M. Davis Cytometry by time-of-flight shows combinatorial cytokine expression and virus-specific cell niches within a continuum of CD8+ T cell phenotypes Immunity 36 2012 142 152
10. M. Mingueneau, S. Krishnaswamy, M.H. Spitzer, S.C. Bendall, E.L. Stone, S.M. Hedrick, and et al. Single-cell mass cytometry of TCR signaling: amplification of small initial differences results in low ERK activation in NOD mice Proc Natl Acad Sci U S A 111 2014 16466 16471
11. H.G. Polikowsky, C.E. Wogsland, K.E. Diggins, K. Huse, and J.M. Irish Cutting edge: redox signaling hypersensitivity distinguishes human germinal center B cells J Immunol 195 2015 1364 1367
12. R.K. Cheung, and P.J. Utz Screening: CyTOF - the next generation of cell detection Nat Rev Rheumatol 7 2011 502 503
13. A.F. Nassar, H. Ogura, and A.V. Wisnewski Impact of recent innovations in the use of mass cytometry in support of drug development Drug Discov Today 20 2015 1169 1175
14. B. Gaudilliere, G.K. Fragiadakis, R.V. Bruggner, M. Nicolau, R. Finck, M. Tingle, and et al. Clinical recovery from surgery correlates with single-cell immune signatures Sci Transl Med 6 2014 255ra131
15. W.E. O'Gorman, E.W. Hsieh, E.S. Savig, P.F. Gherardini, J.D. Hernandez, L. Hansmann, and et al. Single-cell systems-level analysis of human Toll-like receptor activation defines a chemokine signature in patients with systemic lupus erythematosus J Allergy Clin Immunol 136 2015 1326 1336
16. B. Gaudilliere, E.A. Ganio, M. Tingle, H.L. Lancero, G.K. Fragiadakis, Q.J. Baca, and et al. Implementing mass cytometry at the bedside to study the immunological basis of human diseases: distinctive immune features in patients with a history of term or preterm birth Cytometry A 87 2015 817 829
17. A. Han, E.W. Newell, J. Glanville, N. Fernandez-Becker, C. Khosla, Y.H. Chien, and et al. Dietary gluten triggers concomitant activation of CD4+ and CD8+ alphabeta T cells and gammadelta T cells in celiac disease Proc Natl Acad Sci U S A 110 2013 13073 13078
18. L. Hansmann, L. Blum, C.H. Ju, M. Liedtke, W.H. Robinson, and M.M. Davis Mass cytometry analysis shows that a novel memory phenotype B cell is expanded in multiple myeloma Cancer Immunol Res 3 2015 650 660
19. Y. Yao, R. Liu, M.S. Shin, M. Trentalange, H. Allore, A. Nassar, and et al. CyTOF supports efficient detection of immune cell subsets from small samples J Immunol Methods 415 2014 1 5
20. C. Vitali, S. Bombardieri, R. Jonsson, H.M. Moutsopoulos, E.L. Alexander, S.E. Carsons, and et al. Classification criteria for Sjogren's syndrome: a revised version of the European criteria proposed by the American-European Consensus Group Ann Rheum Dis 61 2002 554 558
21. A.D. Amir el, K.L. Davis, M.D. Tadmor, E.F. Simonds, J.H. Levine, S.C. Bendall, and et al. viSNE enables visualization of high dimensional single-cell data and reveals phenotypic heterogeneity of leukemia Nat Biotechnol 31 2013 545 552
22. L. Quartuccio, C. Baldini, E. Bartoloni, R. Priori, F. Carubbi, L. Corazza, and et al. Anti-SSA/SSB-negative Sjogren's syndrome shows a lower prevalence of lymphoproliferative manifestations, and a lower risk of lymphoma evolution Autoimmun Rev 14 2015 1019 1022
23. E.S. Emamian, J.M. Leon, C.J. Lessard, M. Grandits, E.C. Baechler, and et al. Peripheral blood gene expression profiling in Sjogren's syndrome Genes Immun 10 2009 285 296
24. J.E. Gottenberg, M. Busson, J. Cohen-Solal, F. Lavie, K. Abbed, R.P. Kimberly, and et al. Correlation of serum B lymphocyte stimulator and beta2 microglobulin with autoantibody secretion and systemic involvement in primary Sjogren's syndrome Ann Rheum Dis 64 2005 1050 1055
25. J.O. Bohnhorst, J.E. Thoen, J.B. Natvig, and K.M. Thompson Significantly depressed percentage of CD27+ (memory) B cells among peripheral blood B cells in patients with primary Sjogren's syndrome Scand J Immunol 54 2001 421 427
26. D. Cornec, A. Saraux, J.O. Pers, S. Jousse-Joulin, T. Marhadour, A.M. Roguedas-Contios, and et al. Diagnostic accuracy of blood B-cell subset profiling and autoimmunity markers in Sjogren's syndrome Arthritis Res Ther 16 2014 R15
27. P. Vogelsang, J.G. Brun, G. Oijordsbakken, K. Skarstein, R. Jonsson, and S. Appel Levels of plasmacytoid dendritic cells and type-2 myeloid dendritic cells are reduced in peripheral blood of patients with primary Sjogren's syndrome Ann Rheum Dis 69 2010 1235 1238
28. R. Tibshirani Regression shrinkage and selection via lasso J R Stat Soc B 58 1996 267 288
29. R. Seror, E. Theander, J.G. Brun, M. Ramos-Casals, V. Valim, T. Dörner, and et al. Validation of EULAR primary Sjogren's syndrome disease activity (ESSDAI) and patient indexes (ESSPRI) Ann Rheum Dis 74 2015 859 866
30. J.F. Piskurich, K.I. Lin, Y. Lin, Y. Wang, J.P. Ting, and K. Calame BLIMP-I mediates extinction of major histocompatibility class II transactivator expression in plasma cells Nat Immunol 1 2000 526 532
31. R.I. Fox, T. Bumol, R. Fantozzi, R. Bone, and R. Schreiber Expression of histocompatibility antigen HLA-DR by salivary gland epithelial cells in Sjogren's syndrome Arthritis Rheum 29 1986 1105 1111
32. M.N. Manoussakis, I.D. Dimitriou, E.K. Kapsogeorgou, G. Xanthou, S. Paikos, M. Polihronis, and et al. Expression of B7 costimulatory molecules by salivary gland epithelial cells in patients with Sjogren's syndrome Arthritis Rheum 42 1999 229 239
33. S. Tsunawaki, S. Nakamura, Y. Ohyama, M. Sasaki, A. Ikebe-Hiroki, A. Hiraki, and et al. Possible function of salivary gland epithelial cells as nonprofessional antigen-presenting cells in the development of Sjogren's syndrome J Rheumatol 29 2002 1884 1896
34. J.E. Gottenberg, N. Cagnard, C. Lucchesi, F. Letourneur, S. Mistou, T. Lazure, and et al. Activation of IFN pathways and plasmacytoid dendritic cell recruitment in target organs of primary Sjogren's syndrome Proc Natl Acad Sci U S A 103 2006 2770 2775
35. E.A. Szyszko, K.A. Brokstad, G. Oijordsbakken, M.V. Jonsson, R. Jonsson, and K. Skarstein Salivary glands of primary Sjogren's syndrome patients express factors vital for plasma cell survival Arthritis Res Ther 13 2011 R2
36. J.L. Halliley, C.M. Tipton, J. Liesveld, A.F. Rosenberg, J. Darce, I.V. Gregoretti, and et al. Long-lived plasma cells are contained within the CD19(-)CD38(hi)CD138(+) subset in human bone marrow Immunity 43 2015 132 145
37. M.B. Nishishinya, C.A. Pereda, S. Muñoz-Fernández, J.M. Pego-Reigosa, I. Rúa-Figueroa, J.L. Andreu, and et al. Identification of lymphoma predictors in patients with primary Sjogren's syndrome: a systematic literature review and meta-analysis Rheumatol Int 35 2015 17 26
38. G. Nocturne, A. Virone, W.F. Ng, V. Le Guern, E. Hachulla, D. Cornec, and et al. Rheumatoid factor and disease activity are independent predictors of lymphoma in primary Sjogren's Syndrome Arthritis Rheumatol 2015 Nov 25 [Epub ahead of print]
39. A. Nezos, F. Gravani, A. Tassidou, E.K. Kapsogeorgou, M. Voulgarelis, M. Koutsilieris, and et al. Type I and II interferon signatures in Sjogren's syndrome pathogenesis: Contributions in distinct clinical phenotypes and Sjogren's related lymphomagenesis J Autoimmun 63 2015 47 58
40. M.N. Manoussakis, and E.K. Kapsogeorgou The role of intrinsic epithelial activation in the pathogenesis of Sjogren's syndrome J Autoimmun 35 2010 219 224
41. M. Swiecki, Y. Wang, W. Vermi, S. Gilfillan, R.D. Schreiber, and M. Colonna Type I interferon negatively controls plasmacytoid dendritic cell numbers in vivo J Exp Med 208 2011 2367 2374
42. L. Quartuccio, C. Baldini, E. Bartoloni, R. Priori, F. Carubbi, L. Corazza, and et al. Anti-SSA/SSB-negative Sjogren's syndrome shows a lower prevalence of lymphoproliferative manifestations, and a lower risk of lymphoma evolution Autoimmun Rev 14 2015 1019 1022
43. E.S. Emamian, J.M. Leon, C.J. Lessard, M. Grandits, E.C. Baechler, P.M. Gaffney, and et al. Peripheral blood gene expression profiling in Sjogren's syndrome Genes Immun 10 2009 285 296
44. J.E. Gottenberg, M. Busson, J. Cohen-Solal, F. Lavie, K. Abbed, R.P. Kimberly, and et al. Correlation of serum B lymphocyte stimulator and beta2 microglobulin with autoantibody secretion and systemic involvement in primary Sjogren's syndrome Ann Rheum Dis 64 2005 1050 1055
45. M.I. Love, W. Huber, and S. Anders Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 Genome Biol 15 2014 550
46. R. Tibshirani Regression shrinkage and selection via lasso J Royal Stat Soc B 58 1996 267 288
47. J. Friedman, T. Hastie, and R. Tibshirani Regularization paths for generalized linear models via coordinate descent J Stat Softw 33 2010 1 22