Journal of Korean Neurosurgical Society

The Korean Neurosurgical Society (대한신경외과학회)
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Association of HLA-DR and -DQ Genes with Familial Moyamoya Disease in Koreans

  • Hong, Seok-Ho (Department of Neurosurgery, Seoul National University College of Medicine) ;
  • Wang, Kyu-Chang (Department of Neurosurgery, Seoul National University College of Medicine) ;
  • Kim, Seung-Ki (Department of Neurosurgery, Seoul National University College of Medicine) ;
  • Cho, Byung-Kyu (Department of Neurosurgery, Seoul National University College of Medicine) ;
  • Park, Myoung-Hee (Laboratory Medicine, Seoul National University College of Medicine)
  • Published : 2009.12.28
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Abstract

Objective : Moyamoya disease (MMD) is an uncommon cerebrovascular disorder, characterized by progressive occlusion at the terminal portion of the internal carotid artery. Incidence of the disease is high in East Asia and familial MMD accounts for about 15% of the disease. Although the pathogenesis is unknown, association of HLA class I or II alleles with MMD has been reported with conflicting results. We investigated whether there is a difference in HLA class II association between familial and non-familial forms of the disease. Methods : A total of 70 Korean children with MMD, including 16 familial cases (10 probands), and 207 healthy controls were studied. Among familial cases, only 10 probands were used for the HLA frequency analysis. High resolution HLA-DRB1 and DQB1 genotyping was performed using polymerase chain reaction (PCR)-sequence specific oligonucleotide hybridization and PCR-single strand conformation polymorphism methods. Results : The phenotype frequencies of HLA-DRB1*1302 (70.0%) and DQB1*0609 (40.0%) were significantly increased in familial MMD compared to both controls [vs. 15.5%, corrected p ($p_c$) = 0.008, odds ratio (OR) = 12.76; vs. 4.3%, $p_c\;=\;0.02$, OR = 14.67] and non-familial MMD patients (vs. 14.8%, $p_c\;=\;0.02$, OR = 13.42; vs. 1.9%, $p_c\;=\;0.02$, OR = 35.33). The frequencies of DRB1 and DQB1 alleles in non-familial MMD patients were not significantly different from those in controls. Conclusion : Our findings suggest that the genetic polymorphism of HLA class II genes or other closely linked disease relevant gene(s) could be a genetic predisposing factor for familial MMD.

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References

  1. Aoyagi M, Fukai N, Yamamoto M, Nakagawa K, Matsushima Y, Yamamoto K : Early development of intimal thickening in superficial temporal arteries in patients with moyamoya disease. Stroke 27 : 1750-1754, 1996 https://doi.org/10.1161/01.STR.27.10.1750
  2. Aoyagi M, Ogami K, Matsushima Y, Shikata M, Yamamoto M, Yamamoto K : Human leukocyte antigen in patients with moyamoya disease. Stroke 26 : 415-417, 1995 https://doi.org/10.1161/01.STR.26.3.415
  3. Bannai M, Tokunaga K, Lin L, Kuwata S, Mazda T, Amaki I, et al. : Discrimination of human HLA-DRB1 alleles by PCR-SSCP (singlestrand conformation polymorphism) method. Eur J Immunogenet 21 : 1-9, 1994 https://doi.org/10.1111/j.1744-313X.1994.tb00170.x
  4. Fujimura M, Watanabe M, Narisawa A, Shimizu H, Tominaga T : Increased expression of serum matrix metalloproteinase-9 in patients with moyamoya disease. Surg Neurol [Epub ahead of print], 2009 https://doi.org/10.1016/j.surneu.2008.10.009
  5. Fukui M : Guidelines for the diagnosis and treatment of spontaneous occlusion of the circle of willis (‘moyamoya’ diseases). Research Committee on Spontaneous Occlusion of the Circle of Willis (Moyamoya Disease) of the Ministry of Health and Welfare, Japan. Clin Neurol Neurosurg 99 : S238-S240, 1997
  6. Fukui M, Kono S, Sueishi K, Ikezaki K : Moyamoya disease. Neuropathology 20 : S61-S64, 2000 https://doi.org/10.1046/j.1440-1789.2000.00300.x
  7. Goto Y, Yonekawa Y : Worldwide distribution of moyamoya disease. Neurol Med Chir (Tokyo) 32 : 883-886, 1992 https://doi.org/10.2176/nmc.32.883
  8. Han H, Pyo CW, Yoo DS, Huh PW, Cho KS, Kim DS : Associations of Moyamoya patients with HLA class I and class II alleles in the Korean population. J Korean Med Sci 18 : 876-880, 2003 https://doi.org/10.3346/jkms.2003.18.6.876
  9. Hashitaka H, Liu W, Mineharu Y, Inoue K, Takenaka K, Ikeda H, et al. : [Current knowledge on the genetic factors involved in moyamoya disease.] Brain Nerve 60 : 1261-1269, 2008
  10. Houkin K, Yoshimoto T, Abe H, Nagashima K, Nagashima M, Takeda M, et al. : Role of basic fibroblast growth factor in the pathogenesis of moyamoya disease. Neurosurg Focus 5 : 1-5, 1998
  11. Ikeda H, Sasaki T, Yoshimoto T, Fukui M, Arinami T : Mapping of a familial moyamoya disease gene to chromosome 3p24.2-p26. Am J Hum Genet 64 : 533-537, 1999 https://doi.org/10.1086/302243
  12. Inoue TK, Ikezaki K, Sasazuki T, Matsushima T, Fukui M : Analysis of class II genes of human leukocyte antigen in patients with moyamoya disease. Clinical Neurol Neurosurg 99: S234-S237, 1997
  13. Inoue TK, Ikezaki K, Sasazuki T, Matsushima T, Fukui M : Linkage analysis of moyamoya disease on chromosome 6. J Child Neurol 15 : 179-182, 2000 https://doi.org/10.1177/088307380001500307
  14. Inoue TK, Ikezaki K, Sasazuki T, Ono T, Kamikawaji N, Matsushima T, et al. : DNA typing of HLA in the patients with moyamoya disease. Jpn J Hum Genet 42 : 507-515, 1997 https://doi.org/10.1007/BF02767027
  15. Kang HS, Kim SK, Cho BK, Kim YY, Hwang YS, Wang KC : Single nucleotide polymorphisms of tissue inhibitor of metalloproteinase genes in familial moyamoya disease. Neurosurgery 58 : 1074-1080, 2006 https://doi.org/10.1227/01.NEU.0000215854.66011.4F
  16. Kim SK, Yoo JI, Cho BK, Hong SJ, Kim YK, Moon JA, et al. : Elevation of CRABP-I in the cerebrospinal fluid of patients with moyamoya disease. Stroke 34 : 2835-2841, 2003 https://doi.org/10.1161/01.STR.0000100159.43123.D7
  17. Kitahara T, Okumura K, Semba A, Yamaura A, Makino H : Genetic and immunologic analysis on moya-moya. J Neurol Neurosurg Psychiatry 45 : 1048-1052, 1982 https://doi.org/10.1136/jnnp.45.11.1048
  18. Kuroda S, Houkin K : Moyamoya disease : current concepts and future perspectives. Lancet Neurol 7 : 1056-1066, 2008 https://doi.org/10.1016/S1474-4422(08)70240-0
  19. McManus DP, Ross AG, Williams GM, Sleigh AC, Wiest P, Erlich H, et al. : HLA class II antigens positively and negatively associated with hepatosplenic schistosomiasis in a Chinese population. Int J Parasitol 31 : 674-680, 2001 https://doi.org/10.1016/S0020-7519(01)00132-1
  20. Mineharu Y, Liu W, Inoue K, Matsuura N, Inoue S, Takenaka K, et al. : Autosomal dominant moyamoya disease maps to chromosome 17q25.3. Neurology 70 : 2357-2363, 2008 https://doi.org/10.1212/01.wnl.0000291012.49986.f9
  21. Mineharu Y, Takenaka K, Yamakawa H, Inoue K, Ikeda H, Kikuta KI, et al. : Inheritance pattern of familial moyamoya disease : autosomal dominant mode and genomic imprinting. J Neurol Neurosurg Psychiatry 77 : 1025-1029, 2006 https://doi.org/10.1136/jnnp.2006.096040
  22. Nanba R, Kuroda S, Ishikawa T, Houkin K, Iwasaki Y : Increased expression of hepatocyte growth factor in cerebrospinal fluid and intracranial artery in moyamoya disease. Stroke 35 : 2837-2842, 2004 https://doi.org/10.1161/01.STR.0000148237.13659.e6
  23. Park MH, Whang DH, Kang SJ : High resolution HLA-DQB1 typing by combination of PCR-RFLP and PCR-SSCP. Hum Immunol 60 : 901-907, 1999 https://doi.org/10.1016/S0198-8859(99)00069-5
  24. Park YJ, Park H, Park MH : TNF-$\alpha$ promoter polymorphisms and extended HLA and TNF-$\alpha$ haplotypes in Koreans based on 100 families. Tissue Antigens 63 : 75-79, 2004 https://doi.org/10.1111/j.1399-0039.2004.00148.x
  25. Saito S, Ota S, Yamada E, Inoko H, Ota M : Allele frequencies and haplotypic associations defined by allelic DNA typing at HLA class I and class II loci in the Japanese population. Tissue Antigens 56 : 522-529, 2000 https://doi.org/10.1034/j.1399-0039.2000.560606.x
  26. Sakurai K, Horiuchi Y, Ikeda H, Ikezaki K, Yoshimoto T, Fukui M, et al. : A novel susceptibility locus for moyamoya disease on chromosome 8q23. J Hum Genet 49 : 278-281, 2004 https://doi.org/10.1007/s10038-004-0143-6
  27. Shi Y, Patel S, Niculescu R, Chung W, Desrochers P, Zalewski A : Role of matrix metalloproteinases and their tissue inhibitors in the regulation of coronary cell migration. Arterioscler Thromb Vasc Biol 19 : 1150-1155, 1999 https://doi.org/10.1161/01.ATV.19.5.1150
  28. Song EY, Park MH, Kang SJ, Park HJ, Kim BC, Tokunaga K, et al. : HLA class II allele and haplotype frequencies in Koreans based on 107 families. Tissue Antigens 59 : 475-486, 2002 https://doi.org/10.1034/j.1399-0039.2002.590604.x
  29. Soriano SG, Cowan DB, Proctor MR, Scott RM : Levels of soluble adhesion molecules are elevated in the cerebrospinal fluid of children with moyamoya syndrome. Neurosurgery 50 : 544-549, 2002 https://doi.org/10.1097/00006123-200203000-00022
  30. Wakai K, Tamakoshi A, Ikezaki K, Fukui M, Kawamura T, Aoki R, et al. : Epidemiological features of moyamoya disease in Japan : findings from a nationwide survey. Clin Neurol Neurosurg 99 : S1-S5, 1997 https://doi.org/10.1016/S0303-8467(97)00031-0
  31. Yamauchi T, Houkin K, Tada M, Abe H : Familial occurrence of moyamoya disease. Clin Neurol Neurosurg 99 : S162-S167, 1997
  32. Yamauchi T, Tada M, Houkin K, Tanaka T, Nakamura Y, Kuroda S, et al. : Linkage of familial moyamoya disease (spontaneous occlusion of the circle of Willis) to chromosome 17q25. Stroke 31 : 930-935, 2000 https://doi.org/10.1161/01.STR.31.4.930

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