Endoplasmic reticulum stress causes autophagy and apoptosis leading to cellular redistribution of the autoantigens Ro/Sjögren's syndrome-related antigen A (SSA) and La/SSB in salivary gland epithelial cells

Clinical and Experimental Immunology

Volumn 181, Issue 2, 2015, Pages 244-252

  Katsiougiannis, S ^a,b   Tenta, R ^a   Skopouli, F N ^a,c  

^a HAROKOPIO UNIVERSITY   (Greece)

^b UCLA SCHOOL OF DENTISTRY   (United States)

^c Athens Euroclinic   (Greece)

Author keywords

Apoptosis; Autoimmunity; Autophagy; Epithelial cells; ER stress; La SSB; Ro SSA; Sjogren's syndrome

Indexed keywords

AUTOANTIGEN; CHAPERONE; GLUCOSE REGULATED PROTEIN 78; LA ANTIGEN; RO AUTOANTIGEN; THAPSIGARGIN; UNCLASSIFIED DRUG; X BOX BINDING PROTEIN 1; DNA BINDING PROTEIN; HEAT SHOCK PROTEIN; LIGHT CHAIN 3, HUMAN; MAP1LC3A PROTEIN, HUMAN; MICROTUBULE ASSOCIATED PROTEIN; MOLECULAR CHAPERONE GRP78; REGULATORY FACTOR X TRANSCRIPTION FACTORS; RIBONUCLEOPROTEIN; SS-A ANTIGEN; SS-B ANTIGEN; TRANSCRIPTION FACTOR;

ANTIGEN BINDING; APOPTOSIS; ARTICLE; AUTOPHAGY; CELL DENSITY; CELL VIABILITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; EPITHELIUM CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; MAJOR HISTOCOMPATIBILITY COMPLEX; MINOR SALIVA GLAND; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN ISOLATION; SALIVARY GLAND BIOPSY; SJOEGREN SYNDROME; TH1 CELL; UNFOLDED PROTEIN RESPONSE; CELL LINE; CELL MEMBRANE; CYTOPLASM; DRUG EFFECTS; FEMALE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; PRIMARY CELL CULTURE; PROTEIN TRANSPORT;

APOPTOSIS; AUTOANTIGENS; AUTOPHAGY; CELL LINE; CELL MEMBRANE; CYTOPLASM; DNA-BINDING PROTEINS; ENDOPLASMIC RETICULUM STRESS; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION REGULATION; HEAT-SHOCK PROTEINS; HUMANS; MICROTUBULE-ASSOCIATED PROTEINS; PRIMARY CELL CULTURE; PROTEIN TRANSPORT; RIBONUCLEOPROTEINS; SALIVARY GLANDS, MINOR; SJOGREN'S SYNDROME; THAPSIGARGIN; TRANSCRIPTION FACTORS; UNFOLDED PROTEIN RESPONSE;

EID: 84937950544     PISSN: 00099104     EISSN: 13652249     Source Type: Journal    
DOI: 10.1111/cei.12638     Document Type: Article

References (32)

1. Moutsopoulos HM. Sjögren's syndrome: autoimmune epithelitis. Clin Immunol Immunopathol 1994; 72:162-5.
2. Yannopoulos DI, Roncin S, Lamour A, Pennec YL, Moutsopoulos HM, Youinou P. Conjunctival epithelial cells from patients with Sjögren's syndrome inappropriately express major histocompatibility complex molecules, La(SSB) antigen, and heat-shock proteins. J Clin Immunol 1992; 12:259-65.
3. Halse A, Harley JB, Kroneld U, Jonsson R. Ro/SSA reactive B lymphocytes in salivary glands and peripheral blood of patients with Sjogren's syndrome. Clin Exp Immunol 1999; 115:203-7.
4. Hu S, Vissink A, Arellano M et al. Identification of autoantibody biomarkers for primary Sjögren's syndrome using protein microarrays. Proteomics 2011; 11:1499-507.
5. Jonsson R, Theander E, Sjostrom B, Brokstad K, Henriksson G. Autoantibodies present before symptom onset in primary Sjögren syndrome. JAMA 2013; 310:1854-5.
6. Casciola-Rosen LA, Anhalt G, Rosen A. J. Autoantigens targeted in systemic lupus erythematosus are clustered in two populations of surface structures on apoptotic keratinocytes. J Exp Med 1994; 179:1317-30.
7. Okuma A, Hoshino K, Ohba T et al. Enhanced apoptosis by disruption of the STAT3-IκB-ζ signaling pathway in epithelial cells induces Sjogren's syndrome-like autoimmune disease. Immunity 2013; 38:450-60.
8. Castle D, Castle A. Intracellular transport and secretion of salivary proteins. Crit Rev Oral Biol Med 1998; 9:4-22.
9. Bravo R, Parra V, Gatica D et al. Endoplasmic reticulum and the unfolded protein response: dynamics and metabolic integration. Int Rev Cell Mol Biol 2013; 301:215-90.
10. Hetz C. The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat Rev Mol Cell Biol 2012; 13:89-102.
11. Vitali C, Bombardieri S, Jonsson R 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 2002; 61:554-8.
12. Chisholm D, Manson D. Labial salivary gland biopsy in Sjogren's disease. J Clin Pathol 1968; 21:656-60.
13. Lytton J, Westlin M, Hanley MR. Thapsigargin inhibits the sarcoplasmic or endoplasmic reticulum Ca-ATPase family of calcium pumps J Biol Chem 1991; 266:17067-71.
14. Bertolotti A. Zhang Y, Hendershot LM, Harding HP, Ron D. Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat Cell Biol 2000; 2:326-32.
15. Kohno K. Stress-sensing mechanisms in the unfolded protein response: similarities and differences between yeast and mammals. J Biochem 2010; 147:27-33.
16. Bhattacharya A, Eissa NT. Autophagy and autoimmunity cross-talks. Front Immunol 2013; 4:88.
17. Hu S, Gao K, Pollard R et al. Preclinical validation of salivary biomarkers for primary Sjögren's syndrome. Arthritis Care Res 2010; 62:1633-8.
18. Uchiyama Y. Autophagic cell death and its execution by lysosomal cathepsins. Arch Histol Cytol 2001; 64:233-46.
19. Miranda ME, Tseng CE, Rashbaum W et al. Accessibility of SSA/Ro and SSB/La antigens to maternal autoantibodies in apoptotic human fetal cardiac myocytes. J Immunol 1998; 161:5061-9.
20. Miranda-Carús ME, Askanase AD, Clancy RM et al. Anti-SSA/Ro and anti-SSB/La autoantibodies bind the surface of apoptotic fetal cardiocytes and promote secretion of TNF-alpha by macrophages. J Immunol 2000; 165:5345-51.
21. Fox RI, Chilton T, Scott S, Benton L, Howell FV, Vaughan . Potential role of Epstein-Barr virus in Sjögren's syndrome JH. Rheum Dis Clin North Am 1987; 13:275-92.
22. Triantafyllopoulou A, Tapinos N, Moutsopoulos HM. Evidence for coxsakie virus infection in primary Sjogren's syndrome. Arthritis Rheum 2004; 50:2897-902.
23. Mavragani CP, Crow MK. Activation of the type I interferon pathway in primary Sjogren's syndrome. J Autoimmun 2010; 35:225-31.
24. Hall JC, Casciola-Rosen L, Berger AE et al. Precise probes of type II interferon activity define the origin of interferon signatures in target tissues in rheumatic diseases. Proc Natl Acad Sci 2012; 109:17609-14.
25. Smith JA, Turner MJ, DeLay ML, Klenk EI, Sowders DP, Colbert RA. Endoplasmic reticulum stress and the unfolded protein response are linked to synergistic IFN-beta induction via X-box binding protein 1. Eur J Immunol 2008; 38:1194-203.
26. Liu YP, Zeng L, Tian A et al. Endoplasmic reticulum stress regulates the innate immunity critical transcription factor IRF3. J Immunol 2012; 189:4630-9.
27. Karaiskos D, Mavragani CP, Makaroni S et al. Stress, coping strategies and social support in patients with primary Sjögren's syndrome prior to disease onset: a retrospective case-control study. Ann Rheum Dis 2009; 68:40-6.
28. Mao W, Fukuoka S, Iwai C et al. Cardiomyocyte apoptosis in autoimmune cardiomyopathy: mediated via endoplasmic reticulum stress and exaggerated by norepinephrine. Am J Physiol Heart Circ Physiol 2007; 293:H1636-45.
29. Triantafilou K, Fradelizi D, Wilson K, Triantafilou M. GRP78, a coreceptor for coxsackie virus A9, interacts with major histocompatibility complex class I molecules which mediate virus internalization. J Virol 2002; 76:633-43.
30. Rosengren V, Johansson H, Lehtiö J, Fransson L, Sjöholm A, Ortsäter H. Thapsigargin down-regulates protein levels of GRP78/BiP in INS-1E cells. J Cell Biochem 2012; 113:1635-44.
31. Pirot P, Eizirik DL, Cardozo AK. Interferon-gamma potentiates endoplasmic reticulum stress-induced death by reducing pancreatic beta cell defense mechanisms. Diabetologia 2006; 49:1229-36.
32. Barcellos KS, Nonogaki S, Enokihara MM, Teixeira MS, Andrade LE. Differential expression Ro/SSA and La/SSB 52kDa, mRNA and protein in minor salivary glands from patients with primary Sjogren's syndrome. J Rheumatol 2007; 34:1283-92.