Increased expression of endoplasmic reticulum stress and unfolded protein response genes in peripheral blood mononuclear cells from patients with limited cutaneous systemic sclerosis and pulmonary arterial hypertension

Arthritis and Rheumatism

Volumn 65, Issue 5, 2013, Pages 1357-1366

  Lenna, Stefania ^a,c   Farina, Alessandra G ^a   Martyanov, Viktor ^b   Christmann, Romy B ^a   Wood, Tammara A ^b   Farber, Harrison W ^a   Scorza, Raffaella ^c   Whitfield, Michael L ^b   Lafyatis, Robert ^a   Trojanowska, Maria ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b DARTMOUTH MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF MILAN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; ACTIVATING TRANSCRIPTION FACTOR 6; BIOLOGICAL MARKER; DNAJB1 PROTEIN; GLUCOSE REGULATED PROTEIN 78; HEAT SHOCK PROTEIN; INTERFERON REGULATORY FACTOR 4; INTERLEUKIN 6; THAPSIGARGIN; UNCLASSIFIED DRUG; X BOX BINDING PROTEIN 1;

ARTICLE; CELL STIMULATION; CONTROLLED STUDY; DISEASE SEVERITY; DNA MICROARRAY; ENDOPLASMIC RETICULUM STRESS; GENE CONTROL; GENE EXPRESSION; HUMAN; HUMAN CELL; LUNG ARTERY PRESSURE; MAJOR CLINICAL STUDY; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PULMONARY HYPERTENSION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCLERODERMA; SYSTEMIC SCLEROSIS; UNFOLDED PROTEIN RESPONSE; UPREGULATION;

ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION REGULATION; HUMANS; HYPERTENSION, PULMONARY; LEUKOCYTES, MONONUCLEAR; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SCLERODERMA, LIMITED; SEVERITY OF ILLNESS INDEX; THAPSIGARGIN; UNFOLDED PROTEIN RESPONSE; UP-REGULATION;

EID: 84876523418     PISSN: 00043591     EISSN: 15290131     Source Type: Journal    
DOI: 10.1002/art.37891     Document Type: Article

References (48)

1. Humbert M, Morrell NW, Archer SL, Stenmark KR, MacLean MR, Lang IM, et al. Cellular and molecular pathobiology of pulmonary arterial hypertension. J Am Coll Cardiol 2004; 43: 13S-24S.
2. Le Pavec J, Humbert M, Mouthon L, Hassoun PM,. Systemic sclerosis-associated pulmonary arterial hypertension. Am J Respir Crit Care Med 2010; 181: 1285-93.
3. MacGregor AJ, Canavan R, Knight C, Denton CP, Davar J, Coghlan J, et al. Pulmonary hypertension in systemic sclerosis: risk factors for progression and consequences for survival. Rheumatology (Oxford) 2001; 40: 453-9.
4. Steen V, Medsger TA Jr., Predictors of isolated pulmonary hypertension in patients with systemic sclerosis and limited cutaneous involvement. Arthritis Rheum 2003; 48: 516-22.
5. Hassoun PM, Mouthon L, Barbera JA, Eddahibi S, Flores SC, Grimminger F, et al. Inflammation, growth factors, and pulmonary vascular remodeling. J Am Coll Cardiol 2009; 54: S10-9.
6. Dorfmuller P, Humbert M, Perros F, Sanchez O, Simonneau G, Muller KM, et al. Fibrous remodeling of the pulmonary venous system in pulmonary arterial hypertension associated with connective tissue diseases. Hum Pathol 2007; 38: 893-902.
7. Tuder RM,. Pathology of pulmonary arterial hypertension. Semin Respir Crit Care Med 2009; 30: 376-85.
8. Ron D, Walter P,. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 2007; 8: 519-29.
9. Wang S, Kaufman RJ,. The impact of the unfolded protein response on human disease. J Cell Biol 2012; 197: 857-67.
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. Hotamisligil GS,. Endoplasmic reticulum stress and atherosclerosis. Nat Med 2010; 16: 396-9.
12. Hotamisligil GS,. Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell 2010; 140: 900-17.
13. Kaser A, Martinez-Naves E, Blumberg RS,. Endoplasmic reticulum stress: implications for inflammatory bowel disease pathogenesis. Curr Opin Gastroenterol 2010; 26: 318-26.
14. Salminen A, Kauppinen A, Suuronen T, Kaarniranta K, Ojala J,. ER stress in Alzheimer's disease: a novel neuronal trigger for inflammation and Alzheimer's pathology. J Neuroinflammation 2009; 6: 41.
15. Todd DJ, Lee AH, Glimcher LH,. The endoplasmic reticulum stress response in immunity and autoimmunity. Nat Rev Immunol 2008; 8: 663-74.
16. Gargalovic PS, Gharavi NM, Clark MJ, Pagnon J, Yang WP, He A, et al. The unfolded protein response is an important regulator of inflammatory genes in endothelial cells. Arterioscler Thromb Vasc Biol 2006; 26: 2490-6.
17. + monocytes are vulnerable and functionally impaired under endoplasmic reticulum stress in patients with type 2 diabetes. Diabetes 2010; 59: 634-43.
18. Zhang K, Kaufman RJ,. From endoplasmic-reticulum stress to the inflammatory response. Nature 2008; 454: 455-62.
19. Kaser A, Blumberg RS,. Endoplasmic reticulum stress and intestinal inflammation. Mucosal Immunol 2010; 3: 11-6.
20. Arnett FC, Howard RF, Tan F, Moulds JM, Bias WB, Durban E, et al. Increased prevalence of systemic sclerosis in a Native American tribe in Oklahoma: association with an Amerindian HLA haplotype. Arthritis Rheum 1996; 39: 1362-70.
21. Santaniello A, Salazar G, Lenna S, Antonioli R, Colombo G, Beretta L, et al. HLA-B35 upregulates the production of endothelin-1 in HLA-transfected cells: a possible pathogenetic role in pulmonary hypertension. Tissue Antigens 2006; 68: 239-44.
22. Scorza R, Caronni M, Bazzi S, Nador F, Beretta L, Antonioli R, et al. Post-menopause is the main risk factor for developing isolated pulmonary hypertension in systemic sclerosis. Ann N Y Acad Sci 2002; 966: 238-46.
23. Lenna S, Townsend DM, Tan FK, Kapanadze B, Markiewicz M, Trojanowska M, et al. HLA-B35 upregulates endothelin-1 and downregulates endothelial nitric oxide synthase via endoplasmic reticulum stress response in endothelial cells. J Immunol 2010; 184: 4654-61.
24. LeRoy EC, Black C, Fleischmajer R, Jablonska S, Krieg T, Medsger TA Jr, et al. Scleroderma (systemic sclerosis): classification, subsets and pathogenesis. J Rheumatol 1988; 15: 202-5.
25. McGoon MD, Krichman A, Farber HW, Barst RJ, Raskob GE, Liou TG, et al. Design of the REVEAL registry for US patients with pulmonary arterial hypertension. Mayo Clin Proc 2008; 83: 923-31.
26. Milano A, Pendergrass SA, Sargent JL, George LK, McCalmont TH, Connolly MK, et al. Molecular subsets in the gene expression signatures of scleroderma skin. PLoS One 2008; 3: e2696.
27. De Hoon MJ, Imoto S, Nolan J, Miyano S,. Open source clustering software. Bioinformatics 2004; 20: 1453-4.
28. Reimand J, Kull M, Peterson H, Hansen J, Vilo J,. g:Profiler-a web-based toolset for functional profiling of gene lists from large-scale experiments. Nucleic Acids Res 2007; 35: W193-200.
29. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, et al, the Gene Ontology Consortium. Gene ontology: tool for the unification of biology. Nat Genet 2000; 25: 25-9.
30. Ogata H, Goto S, Sato K, Fujibuchi W, Bono H, Kanehisa M,. KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res 1999; 27: 29-34.
31. Joshi-Tope G, Gillespie M, Vastrik I, D'Eustachio P, Schmidt E, de Bono B, et al. Reactome: a knowledgebase of biological pathways. Nucleic Acids Res 2005; 33: D428-32.
32. Pendergrass SA, Hayes E, Farina G, Lemaire R, Farber HW, Whitfield ML, et al. Limited systemic sclerosis patients with pulmonary arterial hypertension show biomarkers of inflammation and vascular injury. PLoS One 2010; 5: e12106.
33. Christmann RB, Hayes E, Pendergrass S, Padilla C, Farina G, Affandi AJ, et al. Interferon and alternative activation of monocyte/macrophages in systemic sclerosis-associated pulmonary arterial hypertension. Arthritis Rheum 2011; 63: 1718-28.
34. Gourh P, Arnett FC, Assassi S, Tan FK, Huang M, Diekman L, et al. Plasma cytokine profiles in systemic sclerosis: associations with autoantibody subsets and clinical manifestations. Arthritis Res Ther 2009; 11: R147.
35. Tan FK, Zhou X, Mayes MD, Gourh P, Guo X, Marcum C, et al. Signatures of differentially regulated interferon gene expression and vasculotrophism in the peripheral blood cells of systemic sclerosis patients. Rheumatology (Oxford) 2006; 45: 694-702.
36. York MR, Nagai T, Mangini AJ, Lemaire R, van Seventer JM, Lafyatis R,. A macrophage marker, Siglec-1, is increased on circulating monocytes in patients with systemic sclerosis and induced by type I interferons and Toll-like receptor agonists. Arthritis Rheum 2007; 56: 1010-20.
37. Dombroski BA, Nayak RR, Ewens KG, Ankener W, Cheung VG, Spielman RS,. Gene expression and genetic variation in response to endoplasmic reticulum stress in human cells. Am J Hum Genet 2010; 86: 719-29.
38. Cantero-Recasens G, Fandos C, Rubio-Moscardo F, Valverde MA, Vicente R,. The asthma-associated ORMDL3 gene product regulates endoplasmic reticulum-mediated calcium signaling and cellular stress. Hum Mol Genet 2010; 19: 111-21.
39. Kaser A, Lee AH, Franke A, Glickman JN, Zeissig S, Tilg H, et al. XBP1 links ER stress to intestinal inflammation and confers genetic risk for human inflammatory bowel disease. Cell 2008; 134: 743-56.
40. 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-β induction via X-box binding protein 1. Eur J Immunol 2008; 38: 1194-203.
41. Biswas PS, Bhagat G, Pernis AB,. IRF4 and its regulators: evolving insights into the pathogenesis of inflammatory arthritis? Immunol Rev 2010; 233: 79-96.
42. Negishi H, Ohba Y, Yanai H, Takaoka A, Honma K, Yui K, et al. Negative regulation of Toll-like-receptor signaling by IRF-4. Proc Natl Acad Sci U S A 2005; 102: 15989-94.
43. Radstake TR, Gorlova O, Rueda B, Martin JE, Alizadeh BZ, Palomino-Morales R, et al. Genome-wide association study of systemic sclerosis identifies CD247 as a new susceptibility locus. Nat Genet 2010; 42: 426-9.
44. He B,. Viruses, endoplasmic reticulum stress, and interferon responses. Cell Death Differ 2006; 13: 393-403.
45. Arnson Y, Amital H, Guiducci S, Matucci-Cerinic M, Valentini G, Barzilai O, et al. The role of infections in the immunopathogensis of systemic sclerosis-evidence from serological studies. Ann N Y Acad Sci 2009; 1173: 627-32.
46. Pandey JP, LeRoy EC,. Human cytomegalovirus and the vasculopathies of autoimmune diseases (especially scleroderma), allograft rejection, and coronary restenosis. Arthritis Rheum 1998; 41: 10-5.
47. Vaughan JH, Shaw PX, Nguyen MD, Medsger TA Jr, Wright TM, Metcalf JS, et al. Evidence of activation of 2 herpesviruses, Epstein-Barr virus and cytomegalovirus, in systemic sclerosis and normal skins. J Rheumatol 2000; 27: 821-3.
48. Van Bon L, Popa C, Huijbens R, Vonk M, York M, Simms R, et al. Distinct evolution of TLR-mediated dendritic cell cytokine secretion in patients with limited and diffuse cutaneous systemic sclerosis. Ann Rheum Dis 2010; 69: 1539-47.