Haem oxygenase 1 expression is altered in monocytes from patients with systemic lupus erythematosus

Immunology

Volumn 136, Issue 4, 2012, Pages 414-424

  Herrada, Andrés A ^a   Llanos, Carolina ^a,b   Mackern Oberti, Juan P ^a,b   Carreño, Leandro J ^a   Henriquez, Carla ^b   Gómez, Roberto S ^a   Gutierrez, Miguel A ^b   Anegon, Ignacio ^c   Jacobelli, Sergio H ^a,b   Kalergis, Alexis M ^a,b,c  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^b PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^c INSERM   (France)

Author keywords

Haem oxygenase 1; Monocyte; Systemic lupus erythematosus

Indexed keywords

BILIVERDIN; CARBON MONOXIDE; CD14 ANTIGEN; CD4 ANTIGEN; CD69 ANTIGEN; CD86 ANTIGEN; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GLYCOPROTEIN P 15095; HEME OXYGENASE 1; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR ALPHA; IRON; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MESSENGER RNA;

ADULT; ARTICLE; AUTOIMMUNE DISEASE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL TYPE; CLINICAL ARTICLE; CONTROLLED STUDY; DENDRITIC CELL; DISEASE COURSE; ENZYME MECHANISM; FEMALE; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; IMMUNOGENICITY; MALE; MONOCYTE; PATHOGENESIS; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SYSTEMIC LUPUS ERYTHEMATOSUS; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; UPREGULATION;

ADULT; ANIMALS; ANTIGENS, CD14; ARTHRITIS, RHEUMATOID; CD4-POSITIVE T-LYMPHOCYTES; DENDRITIC CELLS; FEMALE; HEME OXYGENASE-1; HUMANS; LUPUS ERYTHEMATOSUS, SYSTEMIC; LYMPHOCYTE ACTIVATION; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MIDDLE AGED; MONOCYTES; RECEPTORS, IGG; RNA, MESSENGER; YOUNG ADULT;

EID: 84863199441     PISSN: 00192805     EISSN: 13652567     Source Type: Journal    
DOI: 10.1111/j.1365-2567.2012.03598.x     Document Type: Article

References (60)

1. von Muhlen CA, Tan EM. Autoantibodies in the diagnosis of systemic rheumatic diseases. Semin Arthritis Rheum 1995; 24:323-58.
2. Feist E, Dorner T, Kuckelkorn U, Schmidtke G, Micheel B, Hiepe F, Burmester GR, Kloetzel PM. Proteasome alpha-type subunit C9 is a primary target of autoantibodies in sera of patients with myositis and systemic lupus erythematosus. J Exp Med 1996; 184:1313-8.
3. Rumore PM, Steinman CR. Endogenous circulating DNA in systemic lupus erythematosus. Occurrence as multimeric complexes bound to histone. J Clin Invest 1990; 86:69-74.
4. Brown EE, Edberg JC, Kimberly RP. Fc receptor genes and the systemic lupus erythematosus diathesis. Autoimmunity 2007; 40:567-81.
5. Anolik JH. B cell biology and dysfunction in SLE. Bull NYU Hosp Jt Dis 2007; 65:182-6.
6. Cohen PL. T- and B-cell abnormalities in systemic lupus. J Invest Dermatol 1993; 100:69S-72S.
7. Driver CB, Ishimori M, Weisman MH. The B cell in systemic lupus erythaematosus: a rational target for more effective therapy. Ann Rheum Dis 2008; 67:1374-81.
8. Chen YF, Morel L. Genetics of T cell defects in lupus. Cell Mol Immunol 2005; 2:403-9.
9. + T cell autoreactivity to self-MHC in New Zealand hybrid mice. Clin Immunol 2001; 98:95-103.
10. Takeno M, Nagafuchi H, Kaneko S et al. Autoreactive T cell clones from patients with systemic lupus erythematosus support polyclonal autoantibody production. J Immunol 1997; 158:3529-38.
11. Shirakawa F, Yamashita U, Suzuki H. Reduced function of HLA-DR-positive monocytes in patients with systemic lupus erythematosus (SLE). J Clin Immunol 1985; 5:396-403.
12. Steinbach F, Henke F, Krause B, Thiele B, Burmester GR, Hiepe F. Monocytes from systemic lupus erythematous patients are severely altered in phenotype and lineage flexibility. Ann Rheum Dis 2000; 59:283-8.
13. Iruretagoyena MI, Wiesendanger M, Kalergis AM. The dendritic cell-T cell synapse as a determinant of autoimmune pathogenesis. Curr Pharm Des 2006; 12:131-47.
14. Kalergis AM, Iruretagoyena MI, Barrientos MJ et al. Modulation of nuclear factor-kappaB activity can influence the susceptibility to systemic lupus erythematosus. Immunology 2009; 1(Suppl.):e306-14.
15. Scheinecker C, Zwolfer B, Koller M, Manner G, Smolen JS. Alterations of dendritic cells in systemic lupus erythematosus: phenotypic and functional deficiencies. Arthritis Rheum 2001; 44:856-65.
16. Gerl V, Lischka A, Panne D et al. Blood dendritic cells in systemic lupus erythematosus exhibit altered activation state and chemokine receptor function. Ann Rheum Dis 2010; 69:1370-7.
17. Carreno LJ, Pacheco R, Gutierrez MA, Jacobelli S, Kalergis AM. Disease activity in systemic lupus erythematosus is associated with an altered expression of low-affinity Fc gamma receptors and costimulatory molecules on dendritic cells. Immunology 2009; 128:334-41.
18. Carreno LJ, Riedel CA, Kalergis AM. Induction of tolerogenic dendritic cells by NF-kappaB blockade and Fcgamma receptor modulation. Methods Mol Biol 2010; 677:339-53.
19. Abraham NG, Kappas A. Pharmacological and clinical aspects of heme oxygenase. Pharmacol Rev 2008; 60:79-127.
20. Ryter SW, Alam J, Choi AM. Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol Rev 2006; 86:583-650.
21. Maines MD, Trakshel GM, Kutty RK. Characterization of two constitutive forms of rat liver microsomal heme oxygenase. Only one molecular species of the enzyme is inducible. J Biol Chem 1986; 261:411-9.
22. Cruse I, Maines MD. Evidence suggesting that the two forms of heme oxygenase are products of different genes. J Biol Chem 1988; 263:3348-53.
23. McCoubrey WK Jr, Huang TJ, Maines MD. Isolation and characterization of a cDNA from the rat brain that encodes hemoprotein heme oxygenase-3. Eur J Biochem 1997; 247:725-32.
24. Blancou P, Tardif V, Simon T, Remy S, Carreno L, Kalergis A, Anegon I. Immunoregulatory properties of heme oxygenase-1. Methods Mol Biol 2010; 677:247-68.
25. Otterbein LE, Choi AM. Heme oxygenase: colors of defense against cellular stress. Am J Physiol Lung Cell Mol Physiol 2000; 279:L1029-37.
26. Stocker R, Yamamoto Y, McDonagh AF, Glazer AN, Ames BN. Bilirubin is an antioxidant of possible physiological importance. Science 1987; 235:1043-6.
27. Yamashita K, McDaid J, Ollinger R et al. Biliverdin, a natural product of heme catabolism, induces tolerance to cardiac allografts. Faseb J 2004; 18:765-7.
28. Remy S, Blancou P, Tesson L et al. Carbon monoxide inhibits TLR-induced dendritic cell immunogenicity. J Immunol 2009; 182:1877-84.
29. Bilban M, Haschemi A, Wegiel B, Chin BY, Wagner O, Otterbein LE. Heme oxygenase and carbon monoxide initiate homeostatic signaling. J Mol Med 2008; 86:267-79.
30. Chauveau C, Remy S, Royer PJ et al. Heme oxygenase-1 expression inhibits dendritic cell maturation and proinflammatory function but conserves IL-10 expression. Blood 2005; 106:1694-702.
31. Lang D, Reuter S, Buzescu T, August C, Heidenreich S. Heme-induced heme oxygenase-1 (HO-1) in human monocytes inhibits apoptosis despite caspase-3 up-regulation. Int Immunol 2005; 17:155-65.
32. Yachie A, Toma T, Mizuno K, Okamoto H, Shimura S, Ohta K, Kasahara Y, Koizumi S. Heme oxygenase-1 production by peripheral blood monocytes during acute inflammatory illnesses of children. Exp Biol Med (Maywood) 2003; 228:550-6.
33. Smith EL, Shmerling RH. The American College of Rheumatology criteria for the classification of systemic lupus erythematosus: strengths, weaknesses, and opportunities for improvement. Lupus 1999; 8:586-95.
34. Mendoza-Naranjo A, Saez PJ, Johansson CC et al. Functional gap junctions facilitate melanoma antigen transfer and cross-presentation between human dendritic cells. J Immunol 2007; 178:6949-57.
35. Blancou P, Anegon I. Editorial: Heme oxygenase-1 and dendritic cells: what else? J Leukoc Biol 2010; 87:185-7.
36. Pae HO, Oh GS, Choi BM, Chae SC, Chung HT. Differential expressions of heme oxygenase-1 gene in CD25- and CD25+ subsets of human CD4+ T cells. Biochem Biophys Res Commun 2003; 306:701-5.
37. Bolland S, Ravetch JV. Spontaneous autoimmune disease in Fc(gamma)RIIB-deficient mice results from strain-specific epistasis. Immunity 2000; 13:277-85.
38. Li M, Peterson S, Husney D, Inaba M, Guo K, Kappas A, Ikehara S, Abraham NG. Long-lasting expression of HO-1 delays progression of type I diabetes in NOD mice. Cell Cycle 2007; 6:567-71.
39. Pamplona A, Ferreira A, Balla J et al. Heme oxygenase-1 and carbon monoxide suppress the pathogenesis of experimental cerebral malaria. Nat Med 2007; 13:703-10.
40. Lee IT, Luo SF, Lee CW et al. Overexpression of HO-1 protects against TNF-alpha-mediated airway inflammation by down-regulation of TNFR1-dependent oxidative stress. Am J Pathol 2009; 175:519-32.
41. Poss KD, Tonegawa S. Heme oxygenase 1 is required for mammalian iron reutilization. Proc Natl Acad Sci U S A 1997; 94:10919-24.
42. Kapturczak MH, Wasserfall C, Brusko T, Campbell-Thompson M, Ellis TM, Atkinson MA, Agarwal A. Heme oxygenase-1 modulates early inflammatory responses: evidence from the heme oxygenase-1-deficient mouse. Am J Pathol 2004; 165:1045-53.
43. Burt TD, Seu L, Mold JE, Kappas A, McCune JM. Naive human T cells are activated and proliferate in response to the heme oxygenase-1 inhibitor tin mesoporphyrin. J Immunol 2010; 185:5279-88.
44. Yuan W, DiMartino SJ, Redecha PB, Ivashkiv LB, Salmon JE. Systemic lupus erythematosus monocytes are less responsive to interleukin-10 in the presence of immune complexes. Arthritis Rheum 2011; 63:212-8.
45. Tsokos GC, Kovacs B, Sfikakis PP, Theocharis S, Vogelgesang S, Via CS. Defective antigen-presenting cell function in patients with systemic lupus erythematosus. Arthritis Rheum 1996; 39:600-9.
46. Koch N, Jung M, Sabat R, Kratzschmar J, Docke WD, Asadullah K, Volk HD, Grutz G. IL-10 protects monocytes and macrophages from complement-mediated lysis. J Leukoc Biol 2009; 86:155-66.
47. Kim T, Kanayama Y, Negoro N, Okamura M, Takeda T, Inoue T. Serum levels of interferons in patients with systemic lupus erythematosus. Clin Exp Immunol 1987; 70:562-9.
48. Theofilopoulos AN, Koundouris S, Kono DH, Lawson BR. The role of IFN-gamma in systemic lupus erythematosus: a challenge to the Th1/Th2 paradigm in autoimmunity. Arthritis Res 2001; 3:136-41.
49. Udono-Fujimori R, Takahashi K, Takeda K, Furuyama K, Kaneko K, Takahashi S, Tamai M, Shibahara S. Expression of heme oxygenase-1 is repressed by interferon-gamma and induced by hypoxia in human retinal pigment epithelial cells. Eur J Biochem 2004; 271:3076-84.
50. Gaipl US, Munoz LE, Grossmayer G et al. Clearance deficiency and systemic lupus erythematosus (SLE). J Autoimmun 2007; 3:114-21.
51. Munoz LE, Gaipl US, Franz S, Sheriff A, Voll RE, Kalden JR, Herrmann M. SLE - a disease of clearance deficiency? Rheumatology (Oxford) 2005; 44:1101-7.
52. McCluskey RT. Evidence for an immune complex disorder in systemic lupus erythematosus (SLE). Am J Kidney Dis 1982; 1(Suppl. 1):119-25.
53. Chung SW, Liu X, Macias AA, Baron RM, Perrella MA. Heme oxygenase-1-derived carbon monoxide enhances the host defense response to microbial sepsis in mice. J Clin Invest 2008; 118:239-47.
54. Lavrovsky Y, Schwartzman ML, Levere RD, Kappas A, Abraham NG. Identification of binding sites for transcription factors NF-kappa B and AP-2 in the promoter region of the human heme oxygenase 1 gene. Proc Natl Acad Sci U S A 1994; 91:5987-91.
55. Yamada N, Yamaya M, Okinaga S, Nakayama K, Sekizawa K, Shibahara S, Sasaki H. Microsatellite polymorphism in the heme oxygenase-1 gene promoter is associated with susceptibility to emphysema. Am J Hum Genet 2000; 66:187-95.
56. Chen YH, Lin SJ, Lin MW et al. Microsatellite polymorphism in promoter of heme oxygenase-1 gene is associated with susceptibility to coronary artery disease in type 2 diabetic patients. Hum Genet 2002; 111:1-8.
57. Wu MM, Chiou HY, Lee TC et al. GT-repeat polymorphism in the heme oxygenase-1 gene promoter and the risk of carotid atherosclerosis related to arsenic exposure. J Biomed Sci 2010; 17:70.
58. Song F, Li X, Zhang M, Yao P, Yang N, Sun X, Hu FB, Liu L. Association between heme oxygenase-1 gene promoter polymorphisms and type 2 diabetes in a Chinese population. Am J Epidemiol 2009; 170:747-56.
59. Rueda B, Oliver J, Robledo G et al. HO-1 promoter polymorphism associated with rheumatoid arthritis. Arthritis Rheum 2007; 56:3953-8.
60. Takeda Y, Takeno M, Iwasaki M et al. Chemical induction of HO-1 suppresses lupus nephritis by reducing local iNOS expression and synthesis of anti-dsDNA antibody. Clin Exp Immunol 2004; 138:237-44.