Sexual dimorphism in an animal model of Sjögren's syndrome: A potential role for Th17 cells

Biology Open

Volumn 4, Issue 11, 2015, Pages 1410-1419

  Voigt, Alexandria ^a   Esfandiary, Lida ^a   Nguyen, Cuong Q ^a,b  

^a University of Florida College of Veterinary Medicine   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF DENTISTRY   (United States)

Author keywords

Animal model; Sexual dimorphism; Sj gren's syndrome; Th17 cells

Indexed keywords

AUTOANTIBODY; CD3 ANTIGEN;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; CELL PROLIFERATION; CONTROLLED STUDY; DISEASE COURSE; DISEASE SEVERITY; FEMALE; INFLAMMATION; LYMPHOCYTIC INFILTRATION; MALE; MOUSE; NONHUMAN; SALIVARY GLAND; SEX DIFFERENCE; SIALOADENITIS; SJOEGREN SYNDROME; T LYMPHOCYTE; TH17 CELL;

EID: 84982860382     PISSN: None     EISSN: 20466390     Source Type: Journal    
DOI: 10.1242/bio.013771     Document Type: Article

References (52)

1. Bacman, S., Berra, A., Sterin-Borda, L. and Borda, E. (2001). Muscarinic acetylcholine receptor antibodies as a new marker of dry eye Sjogren syndrome. Invest. Ophthalmol. Vis. Sci. 42, 321-327.
2. Bolstad, A. I. and Jonsson, R. (2002). Genetic aspects of Sjogren's syndrome. Arthritis Res. 4, 353-359.
3. Brayer, J., Lowry, J., Cha, S., Robinson, C. P., Yamachika, S., Peck, A. B. and Humphreys-Beher, M. G. (2000). Alleles from chromosomes 1 and 3 of NOD mice combine to influence Sjogren's syndrome-like autoimmune exocrinopathy. J. Rheumatol. 27, 1896-1904.
4. Burger, H. G., Dudley, E. C., Robertson, D. M. and Dennerstein, L. (2002). Hormonal changes in the menopause transition. Recent Prog. Hormone Res. 57, 257-275.
5. Cha, S., Nagashima, H., Brown, V. B., Peck, A. B. and Humphreys-Beher, M. G. (2002a). Two NOD Idd-associated intervals contribute synergistically to the development of autoimmune exocrinopathy (Sjögren's syndrome) on a healthy murine background. Arthritis. Rheum. 46, 1390-1398.
6. Cha, S., Nagashima, H., Peck, A. B. and Humphreys-Beher, M. G. (2002b). IDD3 and IDD5 alleles from nod mice mediate Sjogren's syndrome-like autoimmunity. Adv. Exp. Med. Biol. 506, 1035-1039.
7. Chiorini, J. A., Cihakova, D., Ouellette, C. E. and Caturegli, P. (2009). Sjögren syndrome: advances in the pathogenesis from animal models. J. Autoimmun. 33, 190-196.
8. Čiháková, D., Talor, M. V., Barin, J. G., Baldeviano, G. C., Fairweather, D., Rose, N. R. and Burek, C. L. (2009). Sex differences in a murine model of Sjögren's syndrome. Ann. N. Y. Acad. Sci. 1173, 378-383.
9. Cutolo, M., Seriolo, B., Villaggio, B., Pizzorni, C., Craviotto, C. and Sulli, A. (2002). Androgens and estrogens modulate the immune and inflammatory responses in rheumatoid arthritis. Ann. N. Y. Acad. Sci. 966, 131-142.
10. Dawson, L. J., Fox, P. C. and Smith, P. M. (2006). Sjogrens syndrome-the nonapoptotic model of glandular hypofunction. Rheumatology 45, 792-798.
11. Delaleu, N., Jonsson, R. and Koller, M. M. (2005). Sjogren's syndrome. Eur. J. Oral Sci. 113, 101-113.
12. Delaleu, N., Nguyen, C. Q., Tekle, K. M., Jonsson, R. and Peck, A. B. (2013). Transcriptional landscapes of emerging autoimmunity: transient aberrations in the targeted tissue's extracellular milieu precede immune responses in Sjögren's syndrome. Arthritis Res. Ther. 15, R174.
13. Fijak, M., Schneider, E., Klug, J., Bhushan, S., Hackstein, H., Schuler, G., Wygrecka, M., Gromoll, J. and Meinhardt, A. (2011). Testosterone replacement effectively inhibits the development of experimental autoimmune orchitis in rats: evidence for a direct role of testosterone on regulatory T cell expansion. J. Immunol. 186, 5162-5172.
14. Fox, R. I. and Kang, H. I. (1992). Pathogenesis of Sjogren's syndrome. Rheum. Dis. Clin. North Am. 18, 517-538.
15. Grimaldi, C. M., Cleary, J., Dagtas, A. S., Moussai, D. and Diamond, B. (2002). Estrogen alters thresholds for B cell apoptosis and activation. J. Clin. Invest. 109, 1625-1633.
16. Hu, Y., Nakagawa, Y., Purushotham, K. R. and Humphreys-Beher, M. G. (1992). Functional changes in salivary glands of autoimmune disease-prone NOD mice. Am. J. Physiol. 263, E607-E614.
17. Humphreys-Beher, M. G., Brinkley, L., Purushotham, K. R., Wang, P.-L., Nakagawa, Y., Dusek, D., Kerr, M., Chegini, N. and Chan, E. K. L. (1993). Characterization of antinuclear autoantibodies present in the serum from nonobese diabetic (NOD) mice. Clin. Immunol. Immunopathol. 68, 350-356.
18. Humphreys-Beher, M. G., Hu, Y., Nakagawa, Y., Wang, P.-L. and Purushotham, K. R. (1994). Utilization of the non-obese diabetic (NOD) mouse as an animal model for the study of secondary Sjögren's syndrome. Adv. Exp. Med. Biol. 350, 631-636.
19. Hunger, R. E., Carnaud, C., Vogt, I. and Mueller, C. (1998). Male gonadal environment paradoxically promotes dacryoadenitis in nonobese diabetic mice. J. Clin. Invest. 101, 1300-1309.
20. Janeway, C. A., Travers, P., Walport, M. J. and Shlomchick, M. (2001). Immunobiology: The Immune System in Health and Disease. New York: Garland Publishing.
21. Jeganathan, V., Peeva, E. and Diamond, B. (2014). Hormonal milieu at time of B cell activation controls duration of autoantibody response. J. Autoimmun. 53, 46-54.
22. Jonsson, R., Dowman, S. J. and Gordon, T. (2004). Sjogren's syndrome. In Arthritis and Allied Conditions-A Textbook in Rheumatology (ed. W. J. Koopman and L. W. Moreland), pp. 1681-1705. Philadelphia, PA: Lippincott Williams & Wilkins.
23. Khan, D., Dai, R., Karpuzoglu, E. and Ahmed, S. A. (2010). Estrogen increases, whereas IL-27 and IFN-gamma decrease, splenocyte IL-17 production in WT mice. Eur. J. Immunol. 40, 2549-2556.
24. Killedar, S. Y., Eckenrode, S. E., McIndoe, R. A., She, J.-X., Nguyen, C. Q., Peck, A. B. and Cha, S. R. (2006). Early pathogenic events associated with Sjögren's syndrome (SjS)-like disease of the nod mouse using microarray analysis. Lab. Invest. 86, 1243-1260.
25. Kissick, H. T., Sanda, M. G., Dunn, L. K., Pellegrini, K. L., On, S. T., Noel, J. K. and Arredouani, M. S. (2014). Androgens alter T-cell immunity by inhibiting T-helper 1 differentiation. Proc. Natl. Acad. Sci. USA 111, 9887-9892.
26. Konttinen, Y. T., Fuellen, G., Bing, Y., Porola, P., Stegaev, V., Trokovic, N., Falk, S. S. I., Liu, Y., Szodoray, P. and Takakubo, Y. (2012). Sex steroids in Sjögren's syndrome. J. Autoimmun. 39, 49-56.
27. Lavoie, T. N., Lee, B. H. and Nguyen, C. Q. (2011). Current concepts: mouse models of Sjögren's syndrome. J. Biomed. Biotechnol. 2011, 549107.
28. Manoussakis, M. N., Tsinti, M., Kapsogeorgou, E. K. and Moutsopoulos, H. M. (2012). The salivary gland epithelial cells of patients with primary Sjögren's syndrome manifest significantly reduced responsiveness to 17beta-estradiol. J. Autoimmun. 39, 64-68.
29. McClellan, A. J., Volpe, E. A., Zhang, X., Darlington, G. J., Li, D.-Q., Pflugfelder, S. C. and de Paiva, C. S. (2014). Ocular surface disease and dacryoadenitis in aging C57BL/6 mice. Am. J. Pathol. 184, 631-643.
30. Mostafa, S., Seamon, V. and Azzarolo, A. M. (2012). Influence of sex hormones and genetic predisposition in Sjögren's syndrome: a new clue to the immunopathogenesis of dry eye disease. Exp. Eye Res. 96, 88-97.
31. Nguyen, C. Q. and Peck, A. B. (2009). Unraveling the pathophysiology of Sjogren syndrome-associated dry eye disease. Ocul. Surf. 7, 11-27.
32. Nguyen, K. H.-T., Brayer, J., Cha, S., Diggs, S., Yasunari, U., Hilal, G., Peck, A. B. and Humphreys-Beher, M. G. (2000). Evidence for antimuscarinic acetylcholine receptor antibody-mediated secretory dysfunction in nod mice. Arthritis Rheum. 43, 2297-2306.
33. Nguyen, C., Cornelius, J., Singson, E., Killedar, S., Cha, S. and Peck, A. B. (2006a). Role of complement and B lymphocytes in Sjögren's syndrome-like autoimmune exocrinopathy of NOD.B10-H2b mice. Mol. Immunol. 43, 1332-1339.
34. Nguyen, C., Singson, E., Kim, J.-Y., Cornelius, J. G., Attia, R., Doyle, M. E., Bulosan, M., Cha, S. and Peck, A. B. (2006b). Sjogren's syndrome-like disease of C57BL/6.NOD-Aec1 Aec2 mice: gender differences in keratoconjunctivitis sicca defined by a cross-over in the chromosome 3 Aec1 locus. Scand. J. Immunol. 64, 295-307.
35. Nguyen, C. Q., Hu, M. H., Li, Y., Stewart, C. and Peck, A. B. (2008). Salivary gland tissue expression of interleukin-23 and interleukin-17 in Sjögren's syndrome: findings in humans and mice. Arthritis Rheum. 58, 734-743.
36. Nikolov, N. P. and Illei, G. G. (2009). Pathogenesis of Sjögren's syndrome. Curr. Opin. Rheumatol. 21, 465-470.
37. Oertelt-Prigione, S. (2012). The influence of sex and gender on the immune response. Autoimmun. Rev. 11, A479-A485.
38. Peck, A. B. and Nguyen, C. Q. (2012). Transcriptome analysis of the interferonsignature defining the autoimmune process of Sjögren's syndrome. Scand. J. Immunol. 76, 237-245.
39. Peck, A. B., Nguyen, C. Q., Sharma, A., McIndoe, R. A. and She, J. X. (2011). The interferon-signature of Sjögren's syndrome: what does it say about the etiopathology of autoimmunity. J. Clin. Rheum. Musculoskelet. Med. 1, 1-17.
40. Pennell, L. M., Galligan, C. L. and Fish, E. N. (2012). Sex affects immunity. J. Autoimmun. 38, J282-J291.
41. Porola, P., Laine, M., Virkki, L., Poduval, P. and Konttinen, Y. T. (2007). The influence of sex steroids on Sjogren's syndrome. Ann. N. Y. Acad. Sci. 1108, 426-432.
42. Porola, P., Laine, M., Virtanen, I., Pollanen, R., Przybyla, B. D. and Konttinen, Y. T. (2010). Androgens and integrins in salivary glands in Sjogren's syndrome. J. Rheumatol. 37, 1181-1187.
43. Robinson, C. P., Yamamoto, H., Peck, A. B. and Humphreys-Beher, M. G. (1996). 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. 79, 50-59.
44. Robinson, C. P., Cornelius, J., Bounous, D. E., Yamamoto, H., Humphreys-Beher, M. G. and Peck, A. B. (1998). Characterization of the changing lymphocyte populations and cytokine expression in the exocrine tissues of autoimmune NOD mice. Autoimmunity 27, 29-44.
45. Spaan, M., Porola, P., Laine, M., Rozman, B., Azuma, M. and Konttinen, Y. T. (2009). Healthy human salivary glands contain a DHEA-sulphate processing intracrine machinery, which is deranged in primary Sjögren's syndrome. J. Cell. Mol. Med. 13, 1261-1270.
46. Sullivan, D. A. (1997). Sex hormones and Sjogren's syndrome. J. Rheumatol. Suppl. 50, 17-32.
47. Sullivan, D. A. (2004). Androgen deficiency & dry eye syndromes. Arch. Soc. Esp. Oftalmol. 79, 49-50.
48. Sumida, T., Tsuboi, H., Iizuka, M., Asashima, H. and Matsumoto, I. (2012). Anti-M3 muscarinic acetylcholine receptor antibodies in patients with Sjogren's syndrome. Mod. Rheumatol. 23, 841-845.
49. Toda, I., Wickham, L. A. and Sullivan, D. A. (1998). Gender and androgen treatment influence the expression of proto-oncogenes and apoptotic factors in lacrimal and salivary tissues of MRL/lpr mice. Clin. Immunol. Immunopathol. 86, 59-71.
50. Toda, I., Sullivan, B. D., Rocha, E. M., Da Silveira, L. A., Wickham, L. A. and Sullivan, D. A. (1999). Impact of gender on exocrine gland inflammation in mouse models of Sjögren's syndrome. Exp. Eye Res. 69, 355-366.
51. Valtysdottir, S. T., Wide, L. and Hallgren, R. (2001). Low serum dehydroepiandrosterone sulfate in women with primary Sjogren's syndrome as an isolated sign of impaired HPA axis function. J. Rheumatol. 28, 1259-1265.
52. Venkatesh, J., Peeva, E., Xu, X. and Diamond, B. (2006). Cutting edge: hormonal milieu, not antigenic specificity, determines the mature phenotype of autoreactive B cells. J. Immunol. 176, 3311-3314.