Development of inhibitory antibodies to therapeutic factor VIII in severe hemophilia A is associated with microsatellite polymorphisms in the HMOX1 promoter

Haematologica

Volumn 98, Issue 10, 2013, Pages 1650-1655

  Repessé, Yohann ^a,b,c,h   Peyron, Ivan ^a,b,c   Dimitrov, Jordan D ^a,b,c   Dasgupta, Suryasarathi ^e   Moshai, Elika Farrokhi ^a,b,c   Costa, Catherine ^f   Borel Derlon, Annie ^h   Guillet, Benoit ⁱ   D'Oiron, Roseline ^j   Aouba, Achille ^k   Rothschild, Chantal ^k   Oldenburg, Johannes ^g   Pavlova, Anna ^g   Kaveri, Srinivas V ^a,b,c,d,l   Lacroix Desmazes, Sébastien ^a,b,c,d,l  

^a CENTRE DE RECHERCHE DES CORDELIERS   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d INSERM   (France)

^e BRIGHAM AND WOMEN S HOSPITAL   (United States)

^f HENRI MONDOR HOSPITAL   (France)

^g UNIVERSITY HOSPITAL BONN   (Germany)

^h CAEN UNIVERSITY HOSPITAL   (France)

ⁱ UNIVERSITÉ DE RENNES 1   (France)

^j UNIVERSITÉ PARIS SACLAY   (France)

^k HÔPITAL NECKER ENFANTS MALADES   (France)

^l INDIAN COUNCIL OF MEDICAL RESEARCH   (India)

more..

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD CLOTTING FACTOR 8; HEME OXYGENASE 1;

ARTICLE; CASE CONTROL STUDY; CONTROLLED STUDY; DNA POLYMORPHISM; DNA SEQUENCE; GENE EXPRESSION; GENE FREQUENCY; GENE MUTATION; GENOTYPE; HEMOPHILIA A; HUMAN; IMMUNOGENICITY; MAJOR CLINICAL STUDY; POLYMERASE CHAIN REACTION; POLYMORPHIC LOCUS; PROMOTER REGION; SINGLE NUCLEOTIDE POLYMORPHISM;

ANTIBODIES; CASE-CONTROL STUDIES; FACTOR VIII; HEME OXYGENASE-1; HEMOPHILIA A; HUMANS; MICROSATELLITE REPEATS; POLYMORPHISM, SINGLE NUCLEOTIDE; PROMOTER REGIONS, GENETIC; SEVERITY OF ILLNESS INDEX;

EID: 84884966904     PISSN: 03906078     EISSN: 15928721     Source Type: Journal    
DOI: 10.3324/haematol.2013.084665     Document Type: Article

References (43)

1. Ehrenforth S, Kreuz W, Scharrer I, Linde R, Funk M, Güngör T, et al. Incidence of development of factor VIII and factor IX inhibitors in haemophiliacs. Lancet. 1992; 339(8793):594-8.
2. Gouw SC, van den Berg HM. The multifactorial etiology of inhibitor development in hemophilia: genetics and environment. Semin Thromb Hemost. 2009;35(8):723-34.
3. Astermark J, Oldenburg J, Carlson J, Pavlova A, Kavakli K, Berntorp E, et al. Polymorphisms in the TNFA gene and the risk of inhibitor development in patients with hemophilia A. Blood. 2006;108(12): 3739-45.
4. Pavlova A, Delev D, Lacroix-Desmazes S, Schwaab R, Mende M, Fimmers R, et al. Impact of polymorphisms of the major histocompatibility complex class II, interleukin-10, tumor necrosis factor-alpha and cytotoxic T-lymphocyte antigen-4 genes on inhibitor development in severe hemophilia A. J Thromb Haemost. 2009;7(12):2006-15.
5. Astermark J, Oldenburg J, Pavlova A, Berntorp E, Lefvert AK. Polymorphisms in the IL10 but not in the IL1beta and IL4 genes are associated with inhibitor development in patients with hemophilia A. Blood. 2006;107(8):3167-72.
6. Lacroix-Desmazes S, Navarrete AM, Andre S, Bayry J, Kaveri SV, Dasgupta S. Dynamics of factor VIII interactions determine its immunologic fate in hemophilia A. Blood. 2008;112(2):240-9.
7. Eckhardt CL, van der Bom JG, van der Naald M, Peters M, Kamphuisen PW, Fijnvandraat K. Surgery and inhibitor development in hemophilia A: a systematic review. J Thromb Haemost. 2011;9(10):1948-58.
8. Skupsky J, Zhang AH, Su Y, Scott DW. A role for thrombin in the initiation of the immune response to therapeutic factor VIII. Blood. 2009;114(21):4741-8.
9. Meeks SL, Cox CL, Healey JF, Parker ET, Doshi BS, Gangadharan B, et al. A major determinant of the immunogenicity of factor VIII in a murine model is independent of its procoagulant function. Blood. 2012;120 (12):2512-20.
10. Gozzelino R, Jeney V, Soares MP. Mechanisms of cell protection by heme oxygenase-1 Annu Rev Pharmacol Toxicol. 2010;50:323-54.
11. Lee TS, Chau LY. Heme oxygenase-1 mediates the anti-inflammatory effect of interleukin-10 in mice. Nat Med. 2002;8(3):240-6.
12. Ryter SW, Alam J, Choi AM. Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol Rev. 2006;86(2):583-650.
13. Abraham NG, Kappas A. Pharmacological and clinical aspects of heme oxygenase. Pharmacological reviews. 2008;60(1):79-127.
14. Wagener FA, Volk HD, Willis D, Abraham NG, Soares MP, Adema GJ, et al. Different faces of the heme-heme oxygenase system in inflammation. Pharmacol Rev. 2003;55 (3):551-71.
15. Willis D, Moore AR, Frederick R, Willoughby DA. Heme oxygenase: a novel target for the modulation of the inflammatory response. Nat Med. 1996;2(1):87-90.
16. Soares MP, Marguti I, Cunha A, Larsen R. Immunoregulatory effects of HO-1: how does it work? Curr Opin Pharmacol. 2009;9 (4):482-9.
17. Takeda Y, Takeno M, Iwasaki M, Kobayashi H, Kirino Y, Ueda A, 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(2):237-44.
18. Chora AA, Fontoura P, Cunha A, Pais TF, Cardoso S, Ho PP, et al. Heme oxygenase-1 and carbon monoxide suppress autoimmune neuroinflammation. J Clin Invest. 2007;117 (2):438-47.
19. Soares MP, Lin Y, Anrather J, Csizmadia E, Takigami K, Sato K, et al. Expression of heme oxygenase-1 can determine cardiac xenograft survival. Nat Med. 1998;4(9): 1073-7.
20. Kapturczak MH, Wasserfall C, Brusko T, Campbell-Thompson M, Ellis TM, Atkinson MA, et al. Heme oxygenase-1 modulates early inflammatory responses: evidence from the heme oxygenase-1-deficient mouse. Am J Pathol. 2004;165(3):1045-53.
21. Dimitrov JD, Dasgupta S, Navarrete AM, Delignat S, Repesse Y, Meslier Y, et al. Induction of heme oxygenase-1 in factor VIII-deficient mice reduces the immune response to therapeutic factor VIII. Blood. 2010;115(13):2682-5.
22. Exner M, Minar E, Wagner O, Schillinger M. The role of heme oxygenase-1 promoter polymorphisms in human disease. Free Radic Biol Med. 2004;37(8):1097-104.
23. Kimpara T, Takeda A, Watanabe K, Itoyama Y, Ikawa S, Watanabe M, et al. Microsatellite polymorphism in the human heme oxygenase-1 gene promoter and its application in association studies with Alzheimer and Parkinson disease. Hum Genet. 1997;100 (1):145-7.
24. Okinaga S, Takahashi K, Takeda K, Yoshizawa M, Fujita H, Sasaki H, et al. Regulation of human heme oxygenase-1 gene expression under thermal stress. Blood. 1996;87(12):5074-84.
25. Yamada N, Yamaya M, Okinaga S, Nakayama K, Sekizawa K, Shibahara S, et al. Microsatellite polymorphism in the heme oxygenase-1 gene promoter is associated with susceptibility to emphysema. Am J Hum Genet. 2000;66(1):187-95.
26. Taha H, Skrzypek K, Guevara I, Nigisch A, Mustafa S, Grochot-Przeczek A, et al. Role of heme oxygenase-1 in human endothelial cells: lesson from the promoter allelic variants. Arterioscler Thromb Vasc Biol. 2010;30(8):1634-41.
27. Verbruggen B, Novakova I, Wessels H, Boezeman J, van den Berg M, Mauser-Bunschoten E. The Nijmegen modification of the Bethesda assay for factor VIII:C inhibitors: improved specificity and reliability. Thromb Haemost. 1995;73:247-51.
28. Miller SA, Dykes DD, Polesky HF. A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res. 1988;16(3):1215.
29. Gouw SC, van den Berg HM, Oldenburg J, Astermark J, de Groot PG, Margaglione M, et al. F8 gene mutation type and inhibitor development in patients with severe hemophilia A: systematic review and meta-analysis. Blood. 2012;119(12):2922-34.
30. Oldenburg J, El-Maarri O, Schwaab R. Inhibitor development in correlation to factor VIII genotypes. Haemophilia. 2002;8 (Suppl 2):23-9.
31. Rueda B, Oliver J, Robledo G, Lopez-Nevot MA, Balsa A, Pascual-Salcedo D, et al. HO-1 promoter polymorphism associated with rheumatoid arthritis. Arthritis Rheum. 2007;56(12):3953-8.
32. Astermark J, Donfield SM, Gomperts ED, Schwarz J, Menius ED, Pavlova A, et al. The polygenic nature of inhibitors in hemophilia A: results from the Hemophilia Inhibitor Genetics Study (HIGS) combined cohort. Blood. 2013;121(8):1446-54.
33. Arredondo M, Jorquera D, Carrasco E, Albala C, Hertrampf E. Microsatellite polymorphism in the heme oxygenase-1 gene promoter is associated with iron status in persons with type 2 diabetes mellitus. Am J Clin Nutr. 2007;86(5):1347-53.
34. Chen YH, Lin SJ, Lin MW, Tsai HL, Kuo SS, Chen JW, 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):1-8.
35. Hausmann M, Paul G, Kellermeier S, Frey I, Scholmerich J, Falk W, et al. (GT)N dinucleotide repeat polymorphism of haem oxygenase-1 promotor region is not associated with inflammatory bowel disease risk or disease course. Clin Exp Immunol. 2008;153 (1):81-5.
36. Skupsky J, Su Y, Lei TC, Scott DW. Tolerance induction by gene transfer to lymphocytes. Curr Gene Ther. 2007;7(5):369-80.
37. Hoots WK. Pathogenesis of hemophilic arthropathy. Semin Hematol. 2006;43(1 Suppl 1):S18-22.
38. Valentino LA. Blood-induced joint disease: the pathophysiology of hemophilic arthropathy. J Thromb Haemost. 2010;8(9): 1895-902.
39. Chauveau C, Remy S, Royer PJ, Hill M, Tanguy-Royer S, Hubert FX, et al. Heme oxygenase-1 expression inhibits dendritic cell maturation and proinflammatory function but conserves IL-10 expression. Blood. 2005;106(5):1694-702.
40. Remy S, Blancou P, Tesson L, Tardif V, Brion R, Royer PJ, et al. Carbon monoxide inhibits TLR-induced dendritic cell immunogenicity. J Immunol. 2009;182(4):1877-84.
41. Hirai H, Kubo H, Yamaya M, Nakayama K, Numasaki M, Kobayashi S, et al. Microsatellite polymorphism in heme oxygenase-1 gene promoter is associated with susceptibility to oxidant-induced apoptosis in lymphoblastoid cell lines. Blood. 2003;102(5):1619-21.
42. Brydun A, Watari Y, Yamamoto Y, Okuhara K, Teragawa H, Kono F, et al. Reduced expression of heme oxygenase-1 in patients with coronary atherosclerosis. Hypertens Res. 2007;30(4):341-8.
43. Motterlini R, Otterbein LE. The therapeutic potential of carbon monoxide. Nat Rev Drug Discov. 2010;9(9):728-43.