Early treatment with hydroxychloroquine prevents the development of endothelial dysfunction in a murine model of systemic lupus erythematosus

Arthritis Research and Therapy

Volumn 17, Issue 1, 2015, Pages

  Virdis, Agostino ^a   Tani, Chiara ^a   Duranti, Emiliano ^a   Vagnani, Sabrina ^a   Carli, Linda ^a,b   Kühl, Anja A ^c   Solini, Anna ^a   Baldini, Chiara ^a   Talarico, Rosaria ^a   Bombardieri, Stefano ^a   Taddei, Stefano ^a   Mosca, Marta ^a  

^a UNIVERSITY OF PISA   (Italy)

^b UNIVERSITY OF SIENA   (Italy)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

APOCYNIN; ASCORBIC ACID; DOUBLE STRANDED DNA ANTIBODY; HYDROETHIDINE; HYDROXYCHLOROQUINE; NITRIC OXIDE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; ANTIOXIDANT; ANTIRHEUMATIC AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY TITER; ANTIOXIDANT ACTIVITY; ARTICLE; BLOOD SAMPLING; CONTROLLED STUDY; DISEASE ACTIVITY; DISEASE CONTROL; DRUG MECHANISM; DRUG RESPONSE; EARLY INTERVENTION; ENDOTHELIAL DYSFUNCTION; FEMALE; KIDNEY; MESENTERIC ARTERY; MOUSE; NONHUMAN; PROTEINURIA; SYSTEMIC LUPUS ERYTHEMATOSUS; URINALYSIS; ANIMAL; C57BL MOUSE; COMPLICATION; DISEASE MODEL; DRUG EFFECTS; METABOLISM; NEW ZEALAND BLACK MOUSE; VASCULAR DISEASES; VASCULAR ENDOTHELIUM;

ANIMALS; ANTIOXIDANTS; ANTIRHEUMATIC AGENTS; DISEASE MODELS, ANIMAL; ENDOTHELIUM, VASCULAR; FEMALE; HYDROXYCHLOROQUINE; LUPUS ERYTHEMATOSUS, SYSTEMIC; MICE; MICE, INBRED C57BL; MICE, INBRED NZB; REACTIVE OXYGEN SPECIES; VASCULAR DISEASES;

EID: 84943426853     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/s13075-015-0790-3     Document Type: Article

References (37)

1. Ippolito A, Petri M. An update on mortality in systemic lupus erythematosus. Clin Exp Rheumatol. 2008;26:S72-9.
2. Schoenfeld SR, Kasturi S, Costenbader KH. The epidemiology of atherosclerotic cardiovascular disease among patients with SLE: a systematic review. Semin Arthritis Rheum. 2013;43:77-95.
3. Esdaile JM, Abrahamowicz M, Grodzicky T, Li Y, Panaritis C, du Berger R, et al. Traditional Framingham risk factors fail to fully account for accelerated atherosclerosis in systemic lupus erythematosus. Arthritis Rheum. 2001;44:2331-7.
4. Roman MJ, Shanker BA, Davis A, Lockshin MD, Sammaritano L, Simantov R, et al. Prevalence and correlates of accelerated atherosclerosis in systemic lupus erythematosus. N Engl J Med. 2003;349:2399-406.
5. Flammer AJ, Anderson T, Celermajer DS, Creager MA, Deanfield J, Ganz P, et al. The assessment of endothelial function: from research into clinical practice. Circulation. 2012;126:753-67.
6. Ruiz-Irastorza G, Ramos-Casals M, Brito-Zeron P, Khamashta MA. Clinical efficacy and side effects of antimalarials in systemic lupus erythematosus: a systematic review. Ann Rheum Dis. 2010;69:20-8.
7. Fessler BJ, Alarcón GS, McGwin Jr G, Roseman J, Bastian HM, Friedman AW, et al. Systemic lupus erythematosus in three ethnic groups: XVI. Association of hydroxychloroquine use with reduced risk of damage accrual. Arthritis Rheum. 2005;52:1473-80.
8. Akhavan PS, Su J, Lou W, Gladman DD, Urowitz MB, Fortin PR. The early protective effect of hydroxychloroquine on the risk of cumulative damage in patients with systemic lupus erythematosus. J Rheumatol. 2013;40:831-41.
9. Pons-Estel GJ, Alarcón GS, González LA, Zhang J, Vilá LM, Reveille JD, et al. Possible protective effect of hydroxychloroquine on delaying the occurrence of integument damage in lupus: LXXI, data from a multiethnic cohort. Arthritis Care Res. 2010;62:393-400.
10. Willis R, Seif AM, McGwin Jr G, Martinez-Martinez LA, González EB, Dang N, et al. Effect of hydroxychloroquine treatment on pro-inflammatory cytokines and disease activity in SLE patients: data from LUMINA (LXXV), a multiethnic US cohort. Lupus. 2012;21:830-5.
11. Wallace DJ, Metzger AL, Stecher VJ, Turnbull BA, Kern PA. Cholesterol-lowering effect of hydroxychloroquine in patients with rheumatic disease: reversal of deleterious effects of steroids on lipids. Am J Med. 1990;89:322-6.
12. Petri M, Lakatta C, Magder L, Goldman D. Effect of prednisone and hydroxychloroquine on coronary artery disease risk factors in systemic lupus erythematosus: a longitudinal data analysis. Am J Med. 1994;96:254-9.
13. Borba EF, Bonfá E. Longterm beneficial effect of chloroquine diphosphate on lipoprotein profile in lupus patients with and without steroid therapy. J Rheumatol. 2001;28:780-5.
14. Belizna C. Hydroxychloroquine as an anti-thrombotic in antiphospholipid syndrome. Autoimmun Rev. 2015;14:358-62.
15. Selzer F, Sutton-Tyrrell K, Fitzgerald S, Tracy R, Kuller L, Manzi S. Vascular stiffness in women with systemic lupus erythematosus. Hypertension. 2001;37:1075-82.
16. Tanay A, Leibovitz E, Frayman A, Zimlichman R, Shargorodsky M, Gavish D. Vascular elasticity of systemic lupus erythematosus patients is associated with steroids and hydroxychloroquine treatment. Ann N Y Acad Sci. 2007;1108:24-34.
17. Gómez-Guzmán M, Jiménez R, Romero M, Sánchez M, Zarzuelo MJ, Gómez-Morales M, et al. Chronic hydroxychloroquine improves endothelial dysfunction and protects kidney in a mouse model of systemic lupus erythematosus. Hypertension. 2014;64:330-7.
18. James JA, Kim-Howard XR, Bruner BF, Jonsson MK, McClain MT, Arbuckle MR, et al. Hydroxychloroquine sulfate treatment is associated with later onset of systemic lupus erythematosus. Lupus. 2007;16:401-9.
19. Tao X, Fan F, Hoffmann V, Longo NS, Lipsky PE. Therapeutic impact of the ethyl acetate extract of Tripterygium wilfordii Hook F on nephritis in NZB/W F1 mice. Arthritis Res Ther. 2006;8:R24.
20. Virdis A, Colucci R, Fornai M, Blandizzi C, Duranti E, Pinto S, et al. Cyclooxygenase-2 inhibition improves vascular endothelial dysfunction in a rat model of endotoxic shock: role of iNOS and oxidative stress. J Pharmacol Exp Ther. 2005;312:945-53.
21. Paravicini TM, Touyz RM. NADPH oxidases, reactive oxygen species, and hypertension: clinical implications and therapeutic possibilities. Diabetes Care. 2008;31:S170-80.
22. Virdis A, Santini F, Colucci R, Duranti E, Salvetti G, Rugani I, et al. Vascular generation of tumor necrosis factor-aα reduces nitric oxide availability in small arteries from visceral fat of obese patients. J Am Coll Cardiol. 2011;58:238-47.
23. Thacker SG, Duquaine D, Park J, Kaplan MJ. Lupus-prone New Zealand Black/New Zealand White F1 mice display endothelial dysfunction and abnormal phenotype and function of endothelial progenitor cells. Lupus. 2010;19:288-99.
24. Ryan MJ, McLemore Jr GR. Hypertension and impaired vascular function in a female mouse model of systemic lupus erythematosus. Am J Physiol Regul Integr Comp Physiol. 2007;292:R736-42.
25. Gilbert EL, Ryan MJ. High dietary fat promotes visceral obesity and impaired endothelial function in female mice with systemic lupus erythematosus. Gend Med. 2011;8:150-5.
26. Thacker SG, Zhao W, Smith CK, Luo W, Wang H, Vivekanandan-Giri A, et al. Type I interferons modulate vascular function, repair, thrombosis, and plaque progression in murine models of lupus and atherosclerosis. Arthritis Rheum. 2012;64:2975-85.
27. Ghiadoni L, Tani C, Bruno RM, Armenia S, Raimo K, Plantinga Y, et al. Prognostic value of flow mediated dilation in patients with systemic lupus erythematosus: a pilot prospective cohort study. Atherosclerosis. 2014;236:381-4.
28. Ghiadoni L, Mosca M, Tani C, Virdis A, Taddei S, Bombardieri S. Clinical and methodological aspects of endothelial function in patients with systemic autoimmune diseases. Clin Exp Rheumatol. 2008;26:680-7.
29. Chin CW, Tan RS, Thumboo J. Endothelial function and arterial stiffness assessment as early surrogate markers of vascular risk in patients with systemic lupus erythematosus. Clin Exp Rheumatol. 2013;31:295-301.
30. Mak A, Liu Y, Ho RC. Endothelium-dependent but not endothelium-independent flow-mediated dilation is significantly reduced in patients with systemic lupus erythematosus without vascular events: a metaanalysis and metaregression. J Rheumatol. 2011;38:1296-303.
31. Taddei S, Virdis A, Ghiadoni L, Salvetti G, Bernini G, Magagna A, et al. Age-related reduction of nitric oxide availability and oxidative stress in humans. Hypertension. 2001;38:274-9.
32. Bruce IN. 'Not only... but also': factors that contribute to accelerated atherosclerosis and premature coronary heart disease in systemic lupus erythematosus. Rheumatology. 2005;44:1492-502.
33. Ghiadoni L, Cupisti A, Huang Y, Mattei P, Cardinal H, Favilla S, et al. Endothelial dysfunction and oxidative stress in chronic renal failure. J Nephrol. 2004;17:512-9.
34. Wallace DJ, Gudsoorkar VS, Weisman MH, Venuturupalli SR. New insights into mechanisms of therapeutic effects of antimalarial agents in SLE. Nat Rev Rheumatol. 2012;8:522-33.
35. Lu R, Przebinda A, Munroe ME, Guthridge JM, Merrill JT, James JA. Hydroxylchloroquine use is associated with decreased soluble TNF receptor levels in SLE patient samples [abstract 1922]. Arthritis Rheum. 2014;66:S845-6.
36. Sacre K, Criswell LA, McCune JM. Hydroxychloroquine is associated with impaired interferon-aα and tumor necrosis factor-aα production by plasmacytoid dendritic cells in systemic lupus erythematosus. Arthritis Res Ther. 2012;14:R155.
37. van den Borne BE, Dijkmans BA, de Rooij HH, le Cessie S, Verweij CL. Chloroquine and hydroxychloroquine equally affect tumor necrosis factor-aα, interleukin 6, and interferon-γ production by peripheral blood mononuclear cells. J Rheumatol. 1997;24:55-60.