Current insights in microbiome shifts in Sjogren'S syndrome and possible therapeutic interventions

Frontiers in Immunology

Volumn 9, Issue MAY, 2018, Pages

  Tsigalou, Christina ^a   Stavropoulou, Elisavet ^b   Bezirtzoglou, Eugenia ^a  

^a DEMOCRITUS UNIVERSITY OF THRACE   (Greece)

^b LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

Dysbiosis; Microbiome; Prebiotics; Probiotics; Sjogren's syndrome; Therapeutic microbiota manipulations

Indexed keywords

PREBIOTIC AGENT; PROBIOTIC AGENT;

AUTOIMMUNITY; DIETARY COMPLIANCE; DISEASE SEVERITY; HUMAN; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; IMMUNOPATHOGENESIS; INTESTINE FLORA; LYMPHOCYTIC INFILTRATION; MICROBIAL DIVERSITY; MICROBIOME; MOUTH FLORA; NEXT GENERATION SEQUENCING; NONHUMAN; PERSONALIZED MEDICINE; SHORT SURVEY; SJOEGREN SYNDROME;

EID: 85047458246     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2018.01106     Document Type: Short Survey

References (72)

1. Moutsopoulos HM. Sjögren's syndrome: autoimmune epithelitis. Clin Immunol Immunopathol (1994) 72(2):162-5. doi:10.1006/clin.1994.1123
2. Ramos-Casals M, Brito-Zerón P, Kostov B, Sisó-Almirall A, Bosch X, Buss D, et al. Google-driven search for big data in autoimmune geoepidemiology: analysis of 394,827 patients with systemic autoimmune diseases. Autoimmun Rev (2015) 14(8):670-9. doi:10.1016/j.autrev.2015.03.008
3. Humphreys-Beher MG, Brinkley L, Purushotham KR, Wang PL, Dusek D, Nakagawa Y, et al. Characterization of antinuclear autoantibodies present in the serum from nonobese diabetic (NOD) mice. Clin Immunol Immunopathol (1993) 68:350-6. doi:10.1006/clin.1993.1137
4. Humphreys-Beher MG, Hu Y, Nakagawa Y, Wang PL, Purushotham KR. Utilization of the non-obese diabetic (NOD) mouse as an animal model for the study of secondary Sjogren's syndrome. Adv Exp Med Biol (1994) 350:631-6. doi:10.1007/978-1-4615-2417-5_105
5. Robinson CP, Yamamoto H, Peck AB, Humphreys-Beher MG. Genetically programmed development of salivary gland abnormalities in the NOD (nonobese diabetic)-scid mouse in the absence of detectable lymphocytic infiltration: a potential trigger for sialoadenitis of NOD mice. Clin Immunol Immunopathol (1996) 79:50-9. doi:10.1006/clin.1996.0050
6. de Paiva CS, Jones DB, Stern ME, Bian F, Moore QL, Corbiere S, et al. Altered mucosal microbiome diversity and disease severity in Sjögren syndrome. Sci Rep (2016) 6:23561. doi:10.1038/srep23561
7. Spachidou MP, Bourazopoulou E, Maratheftis CI, Kapsogeorgou EK, Moutsopoulos HM, Tzioufas AG. Expression of functional toll-like receptors by salivary gland epithelial cells: increased mRNA expression in cells derived from patients with primary Sjogren's syndrome. Clin Exp Immunol (2007) 147:497-503. doi:10.1111/j.1365-2249.2006.03311.x
8. Garcia-Carrasco M, Fuentes-Alexandro S, Escarcega RO, Salgado G, Riebeling C, Cervera R. Pathophysiology of Sjogren's syndrome. Arch Med Res (2006) 37:921-32. doi:10.1016/j.arcmed.2006.08.002
9. Daridon C, Devauchelle V, Hutin P, Berre RL, Martins-Carvalho C, Bendaoud B. Aberrant expression of BAFF by B lymphocytes infiltrating the salivary glands of patients with primary Sjögren's syndrome. Arthritis Rheum (2007) 56:1134-44. doi:10.1002/art.22458
10. Groom J, Kalled SL, Cutler AH, Olson C, Woodcock SA, Schneider P. Association of BAFF/BLyS overexpression and altered B cell differentiation with Sjogren's syndrome. J Clin Invest (2002) 109:59-68. doi:10.1172/JCI0214121
11. Vlachogiannis NI, Nezos A, Tzioufas AG, Koutsilieris M, Moutsopoulos HM, Mavragani CP. Increased frequency of the PTPN22W* variant in primary Sjogren's Syndrome: association with low type I IFN scores. Clin Immunol (2016) 173:157-60. doi:10.1016/j.clim.2016.10.015
12. Johnsen SJ, Gudlaugsson E, Skaland I, Janssen EA, Jonsson MV, Helgeland L, et al. Low protein A20 in minor salivary glands is associated with lymphoma in primary Sjögren's Syndrome. Scand J Immunol (2016) 83(3):181-7. doi:10.1111/sji.12405
13. Williams AEG, Choi K, Chan AL, Lee YJ, Reeves WH, Bubb MR, et al. Sjögren's syndrome-associated microRNAs in CD14+ monocytes unveils targeted TGFβ signaling. Arthritis Res Ther (2016) 18:95. doi:10.1186/s13075-016-0987-0
14. Cole MB, Quach H, Quach D, Baker A, Taylor KE, Barcellos LF, et al. Epigenetic signatures of salivary gland inflammation in Sjögren's syndrome. Arthritis Rheumatol (2016) 68(12):2936-44. doi:10.1002/art.39792
15. Wang J, Peng H, Tian J, Ma J, Tang X, Rui K, et al. Upregulation of long noncoding RNA TMEVPG1 enhances T helper type 1 cell response in patients with Sjögren syndrome. Immunol Res (2016) 64(2):489. doi:10.1007/s12026-015-8715-4
16. Nair JJ, Singh TP. Sjogren's syndrome: review of the aetiology, pathophysiology & potential therapeutic interventions. J Clin Exp Dent (2017) 9(4):e584-9. doi:10.4317/jced.53605
17. Ferro F, Marcucci E, Orlandi M, Baldini C, Bartoloni-Bocci E. One year in review 2017: primary Sjögren's syndrome. Clin Exp Rheumatol (2017) 35(2):179-91
18. Fragkioudaki S, Mavragani CP, Moutsopoulos HM. Predicting the risk for lymphoma development in Sjogren syndrome: an easy tool for clinical use. Medicine (Baltimore) (2016) 95(25):e3766. doi:10.1097/MD.0000000000003766
19. Birt JA, Tan Y, Mozaffarian N. Sjögren's syndrome: managed care data from a large United States population highlight real-world health care burden and lack of treatment options. Clin Exp Rheumatol (2017) 35(1):98-107
20. Lipsky PE. Systemic lupus erythematosus: an autoimmune disease of B cell hyperactivity. Nat Immunol (2001) 2:764-6. doi:10.1038/ni0901-764
21. Furie R, Stohl W, Ginzler EM, Becker M, Mishra N, Chatham W, et al. Biologic activity and safety of belimumab, a neutralizing anti-B-lymphocyte stimulator (BLyS) monoclonal antibody: a phase I trial in patients with systemic lupus erythematosus. Arthritis Res Ther (2008) 10:R109. doi:10.1186/ar2506
22. Dall'Era M, Chakravarty E, Wallace D, Genovese M, Weisman M, Kavanaugh A, et al. Reduced B lymphocyte and immunoglobulin levels after atacicept treatment in patients with systemic lupus erythematosus: results of a multicenter, phase Ib, double-blind, placebo-controlled, dose-escalating trial. Arthritis Rheum (2007) 56:4142-50. doi:10.1002/art.23047
23. Vugmeyster Y, Seshasayee D, Chang W, Storn A, Howell K, Sa S, et al. A soluble BAFF antagonist, BR3-Fc, decreases peripheral blood B cells and lymphoid tissue marginal zone and follicular B cells in cynomolgus monkeys. Am J Pathol (2006) 168:476-89. doi:10.2353/ajpath.2006.050600
24. Pijpe J, van ImhoffGW, Spijkervet FK, Roodenburg JL, Wolbink GJ, Mansour K. Rituximab treatment in patients with primary Sjogren's syndrome: an open-label phase II study. Arthritis Rheum (2005) 52:2740-50. doi:10.1002/art.21260
25. Skopouli FN, Jagiello P, Tsifetaki N, Moutsopoulos HM. Methotrexate in primary Sjogren's syndrome. Clin Exp Rheumatol (1996) 14:555-8
26. Clinical Trials.gov [Internet]. National Library of Medicine (US); Identifier NCT01782235, Efficacy of Tocilizumab (ETAP) (2017). Available from: https://clinicaltrials.gov/ct2/show/NCT01782235 (Accessed: March 12, 2014)
27. Zarco MF, Vess TJ, Ginsburg GS. The oral microbiome in health and disease and the potential impact on personalized dental medicine. Oral Dis (2012) 18:109-20. doi:10.1111/j.1601-0825.2011.01851.x
28. Human Microbiome Project C. A framework for human microbiome research. Nature (2012) 486:215-21. doi:10.1038/nature11209
29. Human Microbiome Project C. Structure, function and diversity of the healthy human microbiome. Nature (2012) 486:207-14. doi:10.1038/nature11234
30. Zoetendal EG, Rajilic-Stojanovic M, de Vos WM. High-throughput diversity and functionality analysis of the gastrointestinal tract microbiota. Gut (2008) 57:1605-15. doi:10.1136/gut.2007.133603
31. Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR, et al. Enterotypes of the human gut microbiome. Nature (2011) 473:174-80. doi:10.1038/nature09944
32. Segata N, Haake SK, Mannon P, Lemon KP, Waldron L, Gevers D, et al. Composition of the adult digestive tract bacterial microbiome based on seven mouth surfaces, tonsils, throat and stool samples. Genome Biol (2012) 13:R42. doi:10.1186/gb-2012-13-6-r42
33. Bezirtzoglou E, Stavropoulou E. Immunology and probiotic impact of the newborn and young children intestinal microflora. Anaerobe (2011) 17(6):369-74. doi:10.1016/j.anaerobe.2011.03.010
34. Koren O, Knights D, Gonzalez A, Waldron L, Segata N, Knight R, et al. A guide to enterotypes across the human body: meta-analysis of microbial community structures in human microbiome datasets. PLoS Comput Biol (2013) 9:e1002863. doi:10.1371/journal.pcbi.1002863
35. Slingerland AE, Schwabkey Z, Wiesnoski DH, Jenq RR. Clinical evidence for the microbiome in inflammatory diseases. Front Immunol (2017) 8:400. doi:10.3389/fimmu.2017.00400
36. Belizário JE, Napolitano M. Human microbiomes and their roles in dysbiosis, common diseases, and novel therapeutic approaches. Front Microbiol (2015) 6:1050. doi:10.3389/fmicb.2015.01050
37. Chervonsky AV. Influence of microbial environment on autoimmunity. Nat Immunol (2010) 11:28-35. doi:10.1038/ni.1801
38. Yurkovetskiy L, Pickard J, Chervonsky A. Microbiota and autoimmunity: exploring new avenues. Cell Host Microbe (2015) 17(5):548-52. doi:10.1016/j.chom.2015.04.010
39. Kagohashi Y, Tatewaki R, Takebe E, Naora H, Abiru N, Kobayashi M, et al. Maternal EFA composition affects the pathogenesis of type 1 diabetes in NOD mouse offspring. Zool Sci (2006) 23:1221-1221
40. Markle JG, Frank DN, Mortin-Toth S, Robertson CE, Feazel LM, Rolle-Kampczyk U, et al. Sex differences in the gut microbiome drive hormone-dependent regulation of autoimmunity. Science (2013) 339:1084-8. doi:10.1126/science.1233521
41. Yurkovetskiy L, Burrows M, Khan AA, Graham L, Volchkov P, Becker L, et al. Gender bias in autoimmunity is influenced by microbiota. Immunity (2013) 39:400-12. doi:10.1016/j.immuni.2013.08.013
42. Van der Meulen TA, Harmsen H, Bootsma H, Spijkervet F, Kroese F, Vissink A. The microbiome-systemic diseases connection. Oral Dis (2016) 22(8):719-34. doi:10.1111/odi.12472
43. Honda K, Littman DR. The microbiota in adaptive immune homeostasis and disease. Nature (2016) 535(7610):75-84. doi:10.1038/nature18848
44. Ivanov II, Atarashi K, Manel N, Brodie EL, Shima T, Karaoz U, et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell (2009) 139:485-98. doi:10.1016/j.cell.2009.09.033
45. Wu H-J, Ivanov II, Darce J, Hattori K, Shima T, Umesaki Y, et al. Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells. Immunity (2010) 32:815-27. doi:10.1016/j.immuni.2010.06.001
46. Puel A, Cypowyj S, Bustamante J, Wright JF, Liu L, Lim HK, et al. Chronic mucocutaneous candidiasis in humans with inborn errors of interleukin-17 immunity. Science (2011) 332:65-8. doi:10.1126/science.1200439
47. Okada S, Markle JG, Deenick EK, Mele F, Averbuch D, Lagos M, et al. Impairment of immunity to Candida and Mycobacterium in humans with bi-allelic RORC mutations. Science (2015) 349(6248):606-13. doi:10.1126/science.aaa4282
48. Mc Geachy MJ, Chen Y, Tato CM, Laurence A, Joyce-Shaikh B, Blumenschein WM, et al. The interleukin 23 receptor is essential for the terminal differentiation of interleukin 17-producing effector T helper cells in vivo. Nat Immunol (2009) 10:314-24. doi:10.1038/ni.1698
49. Coccia M, Harrison OJ, Schiering C, Asquith MJ, Becher B, Powrie F, et al. IL-1β mediates chronic intestinal inflammation by promoting the accumulation of IL-17A secreting innate lymphoid cells and CD4+ Th17 cells. J Exp Med (2012) 209:1595-609. doi:10.1084/jem.20111453
50. Atarashi K, Tanoue T, Oshima K, Suda W, Nagano Y, Nishikawa HT, et al. Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature (2013) 500:232-6. doi:10.1038/nature12331
51. Atarashi K, Tanoue T, Shima T, Imaoka A, Kuwahara T, Momose Y, et al. Induction of colonic regulatory T cells by indigenous Clostridium species. Science (2011) 331:337-41. doi:10.1126/science.1198469
52. Olszak T, An D, Zeissig S, Vera MP, Richter J, Franke A, et al. Microbial exposure during early life has persistent effects on natural killer T cell function. Science (2012) 336:489-93. doi:10.1126/science.1219328
53. Scharschmidt TC, Vasquez KS, Truong HA, Gearty SV, Pauli ML, Nosbaum A, et al. A wave of regulatory T cells into neonatal skin mediates tolerance to commensal microbes. Immunity (2015) 43:1011-21. doi:10.1016/j.immuni.2015.10.016
54. Lessard CJ, Ice JA, Maier-Moore J, Montgomery CG, Scofield H, Moser KL. Genetics, genomics, and proteomics of Sjögren's syndrome. 1st ed. In: Ramos-Casals M, Stone JH, Moutsopoulos HM, editors. Sjögren's Syndrome - Diagnosis and Therapeutics. London: Springer (2012). p. 11-2
55. Croia C, Astorri E, Murray-Brown W, Willis A, Brokstad KA, Sutcliffe N, et al. Implication of Epstein-Barr virus infection in disease-specific autoreactive B cell activation in ectopic lymphoid structures of Sjögren's syndrome. Arthritis Rheumatol (2014) 66:2545-57. doi:10.1002/art.38726
56. Gottenberg JE, Cagnard N, Lucchesi C, Letourneur F, Mistou S, Lazure T, et al. 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) 103:2770-5. doi:10.1073/pnas.0510837103
57. Almståhl A, Wikström M, Stenberg I, Jakobsson A, Fagerberg-Mohlin B. Oral microbiota associated with hyposalivation of different origins. Oral Microbiol Immunol (2003) 18:1-8. doi:10.1034/j.1399-302X.2003.180101.x
58. Szymula A, Rosenthal J, Szczerba BM, Bagavant H, Fu SM, Deshmukh US. T cell epitope mimicry between Sjögren's syndrome antigen A (SSA)/Ro60 and oral, gut, skin and vaginal bacteria. Clin Immunol (2014) 152:1-9. doi:10.1016/j.clim.2014.02.004
59. Lu M-C, Jheng C-H, Tsai T-Y, Koo M, Lai N-S. Increased dental visits in patients prior to diagnosis of primary Sjögren's syndrome: a population-based study in Taiwan. Rheumatol Int (2014) 34:1555-61. doi:10.1007/s00296-014-3003-5
60. West CE, Renz H, Jenmalm MC, Kozyrskyj AL, Allen KJ, Vuillermin P, et al. The gut microbiota and inflammatory noncommunicable diseases: associations and potentials for gut microbiota therapies. J Allergy Clin Immunol (2015) 135(1):3-13. doi:10.1016/j.jaci.2014.11.012
61. FAO/WHO. Guidelines for the evaluation of probiotics in food. Report of a Joint FAO/WHO Working Group on Drafting Guidelines for the Evaluation of Probiotics in Food. London, Ontario, Canada: World Health Organization (2002)
62. Stavropoulou E, Bezirtzoglou E. Human microbiota in aging and infection: a review. Crit Rev Food Sci Nutr (2017) 4:1-9. doi:10.1080/10408398.2017.1379469
63. Roberfroid MB. Prebiotics and probiotics: are they functional foods? Am J Clin Nutr (2000) 71(6 Suppl):1682S-7S. doi:10.1093/ajcn/71.6.1682S
64. Roberfroid M. Prebiotics: the concept revisited. J Nutr (2007) 137(3 Suppl 2):830S-7S. doi:10.1093/jn/137.3.830S
65. Nagata S, Asahara T, Ohta T, Yamada T, Kondo S, Bian L, et al. Effect of the continuous intake of probiotic-fermented milk containing Lactobacillus casei strain Shirota on fever in a mass outbreak of norovirus gastroenteritis and the faecal microflora in a health service facility for the aged. Br J Nutr (2011) 106:549-56. doi:10.1017/S000711451100064X
66. Dwivedi M, Kumar P, Laddha NC, Kemp EH. Induction of regulatory T cells: a role for probiotics and prebiotics to suppress autoimmunity. Autoimmun Rev (2016) 15(4):379-92. doi:10.1016/j.autrev.2016.01.002
67. Antiga E, Kretz CC, Klembt R, Massi D, Ruland V, Stumpf C, et al. Characterization of regulatory T cells in patients with dermatomyositis. J Autoimmun (2010) 35(4):342-50. doi:10.1016/j.jaut.2010.07.006
68. Miyara M, Amoura Z, Parizot C, Badoual C, Dorgham K, Trad S, et al. Global natural regulatory T cell depletion in active systemic lupus erythematosus. J Immunol (2005) 175(12):8392-400. doi:10.4049/jimmunol.175.12.8392
69. Dwivedi M, Kemp EH, Laddha NC, Mansuri MS, Weetman AP, Begum R. Regulatory T cells in vitiligo: implications for pathogenesis and therapeutics. Autoimmun Rev (2015) 14(1):49-56. doi:10.1016/j.autrev.2014.10.002
70. Konieczna P, Groeger D, Ziegler M, Frei R, Ferstl R, Shanahan F, et al. Bifidobacterium infantis 35624 administration induces Foxp3 T regulatory cells in human peripheral blood: potential role for myeloid and plasmacytoid dendritic cells. Gut (2012) 61(3):354-66. doi:10.1136/gutjnl-2011-300936
71. Shetty SA, Hugenholtz F, Lahti L, Smidt H, de Vos WM. Intestinal microbiome landscaping: insight in community assemblage and implications for microbial modulation strategies. FEMS Microbiol Rev (2017) 41(2):182-99. doi:10.1093/femsre/fuw045
72. Zamani B, Golkar HR, Farshbaf S, Emadi-Baygi M, Tajabadi-Ebrahimi M, Jafari P, et al. Clinical and metabolic response to probiotic supplementation in patients with rheumatoid arthritis: a randomized, double-blind, placebo-controlled trial. Int J Rheum Dis (2016) 19(9):869-79. doi:10.1111/1756-185X.12888