Th17 responses and natural IgM antibodies are related to gut microbiota composition in systemic lupus erythematosus patients

Scientific Reports

Volumn 6, Issue , 2016, Pages

  López, Patricia ^a   De Paz, Banesa ^a,b   Rodríguez Carrio, Javier ^a   Hevia, Arancha ^b   Sánchez, Borja ^b   Margolles, Abelardo ^b   Suárez, Ana ^a  

^a UNIVERSITY OF OVIEDO   (Spain)

^b DEPARTMENT OF MICROBIOLOGY AND BIOCHEMISTRY OF DAIRY PRODUCTS   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; IL6 PROTEIN, HUMAN; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; INTERLEUKIN 17; INTERLEUKIN 6;

AGED; BIFIDOBACTERIUM BIFIDUM; BLOOD; CASE CONTROL STUDY; CELL DIFFERENTIATION; CLOSTRIDIUM; CYTOLOGY; DENDRITIC CELL; FEMALE; FLOW CYTOMETRY; HUMAN; IMMUNOLOGY; INTESTINE FLORA; METABOLISM; MIDDLE AGED; MONOCYTE; PATHOGENICITY; SYSTEMIC LUPUS ERYTHEMATOSUS; TH17 CELL;

AGED; BIFIDOBACTERIUM BIFIDUM; CASE-CONTROL STUDIES; CELL DIFFERENTIATION; CLOSTRIDIUM; CYTOKINES; DENDRITIC CELLS; FEMALE; FLOW CYTOMETRY; GASTROINTESTINAL MICROBIOME; HUMANS; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; INTERLEUKIN-17; INTERLEUKIN-6; LUPUS ERYTHEMATOSUS, SYSTEMIC; MIDDLE AGED; MONOCYTES; TH17 CELLS;

EID: 84962660904     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep24072     Document Type: Article

References (57)

1. Rahman, A. & Isenberg, D. A. Systemic lupus erythematosus. N. Engl. J. Med. 358, 929-939 (2008).
2. Sanz, I. & Lee, F. E.-H. B cells as therapeutic targets in SLE. Nat. Rev. Rheumatol. 6, 326-337 (2010).
3. Zhu, J. & Paul, W. E. CD4+ T cells: fates, functions, and faults. Blood 112, 1557-1569 (2008).
4. Alunno, A. et al. Balance between Regulatory T and Th17 Cells in Systemic Lupus Erythematosus: The Old and the New. J. Immunol. Res. 2012, e823085 (2012).
5. Ma, J. et al. The imbalance between regulatory and IL-17-secreting CD4+ T cells in lupus patients. Clin. Rheumatol. 29, 1251-1258 (2010).
6. Talaat, R. M., Mohamed, S. F., Bassyouni, I. H. & Raouf, A. A. Th1/Th2/Th17/Treg cytokine imbalance in systemic lupus erythematosus (SLE) patients: Correlation with disease activity. Cytokine 72, 146-153 (2015).
7. Pan, H.-F. et al. Expression profiles of Th17 pathway related genes in human systemic lupus erythematosus. Mol. Biol. Rep. 40, 391-399 (2013).
8. Qu, N. et al. Pivotal Roles of T-Helper 17-Related Cytokines, IL-17, IL-22, and IL-23, in Inflammatory Diseases. J. Immunol. Res. 2013, e968549 (2013).
9. Chen, X. Q. et al. Plasma IL-17A is Increased in New-Onset SLE Patients and Associated with Disease Activity. J. Clin. Immunol. 30, 221-225 (2010).
10. Crispín, J. C. et al. Expanded double negative T cells in patients with systemic lupus erythematosus produce IL-17 and infiltrate the kidneys. J. Immunol. Baltim. Md 1950 181, 8761-8766 (2008).
11. Doreau, A. et al. Interleukin 17 acts in synergy with B cell-activating factor to influence B cell biology and the pathophysiology of systemic lupus erythematosus. Nat. Immunol. 10, 778-785 (2009).
12. Wang, Y. et al. Laser microdissection-based analysis of cytokine balance in the kidneys of patients with lupus nephritis. Clin. Exp. Immunol. 159, 1-10 (2010).
13. Shevach, E. M. Mechanisms of foxp3+ T regulatory cell-mediated suppression. Immunity 30, 636-645 (2009).
14. Fontenot, J. D., Gavin, M. A. & Rudensky, A. Y. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat. Immunol. 4, 330-336 (2003).
15. Feuerer, M., Hill, J. A., Mathis, D. & Benoist, C. Foxp3+ regulatory T cells: differentiation, specification, subphenotypes. Nat. Immunol. 10, 689-695 (2009).
16. Lyssuk, E. Y., Torgashina, A. V., Soloviev, S. K., Nassonov, E. L. & Bykovskaia, S. N. Reduced number and function of CD4+CD25highFoxP3+ regulatory T cells in patients with systemic lupus erythematosus. Adv. Exp. Med. Biol. 601, 113-119 (2007).
17. Valencia, X., Yarboro, C., Illei, G. & Lipsky, P. E. Deficient CD4+CD25high T Regulatory Cell Function in Patients with Active Systemic Lupus Erythematosus. J. Immunol. 178, 2579-2588 (2007).
18. Gómez, J., Prado, C., López, P., Suárez, A. & Gutiérrez, C. Conserved anti-proliferative effect and poor inhibition of TNFalpha secretion by regulatory CD4+CD25+ T cells in patients with systemic lupus erythematosus. Clin. Immunol. Orlando Fla 132, 385-392 (2009).
19. Round, J. L. & Mazmanian, S. K. The gut microbiota shapes intestinal immune responses during health and disease. Nat. Rev. Immunol. 9, 313-323 (2009).
20. Grönwall, C. & Silverman, G. J. Natural IgM: beneficial autoantibodies for the control of inflammatory and autoimmune disease. J. Clin. Immunol. 34 Suppl 1, S12-21 (2014).
21. Grönwall, C. et al. Relation of carotid plaque with natural IgM antibodies in patients with systemic lupus erythematosus. Clin. Immunol. 153, 1-7 (2014).
22. Chen, Y., Park, Y.-B., Patel, E. & Silverman, G. J. IgM Antibodies to Apoptosis-Associated Determinants Recruit C1q and Enhance Dendritic Cell Phagocytosis of Apoptotic Cells. J. Immunol. 182, 6031-6043 (2009).
23. López, P., González-Rodríguez, I., Gueimonde, M., Margolles, A. & Suárez, A. Immune response to Bifidobacterium bifidum strains support Treg/Th17 plasticity. PloS One 6, e24776 (2011).
24. López, P., Gueimonde, M., Margolles, A. & Suárez, A. Distinct Bifidobacterium strains drive different immune responses in vitro. Int. J. Food Microbiol. 138, 157-165 (2010).
25. Rescigno, M. et al. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat. Immunol. 2, 361-367 (2001).
26. Joffre, O., Nolte, M. A. & Spörri, R. & Reis e Sousa, C. Inflammatory signals in dendritic cell activation and the induction of adaptive immunity. Immunol. Rev. 227, 234-247 (2009).
27. Mazmanian, S. K., Round, J. L. & Kasper, D. L. A microbial symbiosis factor prevents intestinal inflammatory disease. Nature 453, 620-625 (2008).
28. Ivanov, I. I. et al. Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe 4, 337-349 (2008).
29. Gaboriau-Routhiau, V. et al. The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses. Immunity 31, 677-689 (2009).
30. Yurkovetskiy, L. et al. Gender bias in autoimmunity is influenced by microbiota. Immunity 39, 400-412 (2013).
31. Markle, J. G. M. et al. Sex Differences in the Gut Microbiome Drive Hormone-Dependent Regulation of Autoimmunity. Science 339, 1084-1088 (2013).
32. Garrett, W. S. et al. Enterobacteriaceae act in concert with the gut microbiota to induce spontaneous and maternally transmitted colitis. Cell Host Microbe 8, 292-300 (2010).
33. Frank, D. N. et al. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc. Natl. Acad. Sci. 104, 13780-13785 (2007).
34. Yeoh, N., Burton, J. P., Suppiah, P., Reid, G. & Stebbings, S. The role of the microbiome in rheumatic diseases. Curr. Rheumatol. Rep. 15, 314 (2013).
35. Wen, L. et al. Innate immunity and intestinal microbiota in the development of Type 1 diabetes. Nature 455, 1109-1113 (2008).
36. Lee, Y. K., Menezes, J. S., Umesaki, Y. & Mazmanian, S. K. Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis. Proc. Natl. Acad. Sci. 108, 4615-4622 (2011).
37. Larsen, N. et al. Gut Microbiota in Human Adults with Type 2 Diabetes Differs from Non-Diabetic Adults. PLoS ONE 5, e9085 (2010).
38. Man, S. M., Kaakoush, N. O. & Mitchell, H. M. The role of bacteria and pattern-recognition receptors in Crohn's disease. Nat. Rev. Gastroenterol. Hepatol. 8, 152-168 (2011).
39. Hevia, A. et al. Intestinal dysbiosis associated with systemic lupus erythematosus. mBio 5, e01548-01514 (2014).
40. Turnbaugh, P. J. et al. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444, 1027-1031 (2006).
41. López, P. et al. Interaction of Bifidobacterium bifidum LMG13195 with HT29 cells influences regulatory-T-cell-associated chemokine receptor expression. Appl. Environ. Microbiol. 78, 2850-2857 (2012).
42. Atarashi, K. et al. Induction of Colonic Regulatory T Cells by Indigenous Clostridium Species. Science 331, 337-341 (2011).
43. Atarashi, K. et al. Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature 500, 232-236 (2013).
44. Ueno, A. et al. Increased prevalence of circulating novel IL-17 secreting Foxp3 expressing CD4+ T cells and defective suppressive function of circulating Foxp3+ regulatory cells support plasticity between Th17 and regulatory T cells in inflammatory bowel disease patients. Inflamm. Bowel Dis. 19, 2522-2534 (2013).
45. Hall, J. A. et al. Commensal DNA Limits Regulatory T Cell Conversion and is a Natural Adjuvant of Intestinal Immune Responses. Immunity 29, 637-649 (2008).
46. Murai, M., Krause, P., Cheroutre, H. & Kronenberg, M. Regulatory T-cell stability and plasticity in mucosal and systemic immune systems. Mucosal Immunol. 3, 443-449 (2010).
47. Farkas, A. M. et al. Induction of Th17 cells by segmented filamentous bacteria in the murine intestine. J. Immunol. Methods 421, 104-111 (2015).
48. Zheng, B. et al. Bifidobacterium breve attenuates murine dextran sodium sulfate-induced colitis and increases regulatory T cell responses. PloS One 9, e95441 (2014).
49. Grönwall, C. et al. MAPK phosphatase-1 is required for regulatory natural autoantibody-mediated inhibition of TLR responses. Proc. Natl. Acad. Sci. USA 109, 19745-19750 (2012).
50. Bao, S., Husband, A. J. & Beagley, K. W. B1 B cell numbers and antibodies against phosphorylcholine and LPS are increased in IL-6 gene knockout mice. Cell. Immunol. 198, 139-142 (1999).
51. Su, J. et al. Natural antibodies against phosphorylcholine as potential protective factors in SLE. Rheumatology 47, 1144-1150 (2008).
52. Faria-Neto, J. R. et al. Passive immunization with monoclonal IgM antibodies against phosphorylcholine reduces accelerated vein graft atherosclerosis in apolipoprotein E-null mice. Atherosclerosis 189, 83-90 (2006).
53. Milani, C. et al. Assessing the Fecal Microbiota: An Optimized Ion Torrent 16S rRNA Gene-Based Analysis Protocol. PLoS ONE 8, e68739 (2013).
54. Courtois, S. et al. Quantification of bacterial subgroups in soil: comparison of DNA extracted directly from soil or from cells previously released by density gradient centrifugation. Environ. Microbiol. 3, 431-439 (2001).
55. Arnett, F. C. et al. The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum. 31, 315-324 (1988).
56. Gómez, J. et al. Systemic lupus erythematosus in Asturias, Spain: clinical and serologic features. Medicine (Baltimore) 85, 157-168 (2006).
57. López, P., Mozo, L., Gutiérrez, C. & Suárez, A. Epidemiology of systemic lupus erythematosus in a northern Spanish population: gender and age influence on immunological features. Lupus 12, 860-865 (2003).