Cited by 212Multiple Sclerosis Research StudiesGenetic Associations and EpidemiologyPsoriasis: Treatment and Pathogenesis

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HLA-DR15 Haplotype and Multiple Sclerosis: A HuGE Review

Schmidt, Hollie, Williamson, Dhelia, Ashley-Koch, Allison·2007·American Journal of Epidemiology

DOI 10.1093/aje/kwk118

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Abstract

An association between multiple sclerosis (MS) and the human leukocyte antigen (HLA) complex, a dense cluster of genes on the short arm of chromosome 6, was first noted over 30 years ago. In Caucasian populations of Northern European descent, the DR15 haplotype (DRB1*1501-DQA1*0102-DQB1*0602) has been hypothesized to be the primary HLA genetic susceptibility factor for MS. However, studies of other populations have produced varying results. Thus, the authors reviewed the literature for articles on the association between the DR15 haplotype and MS. They identified 72 papers meeting the inclusion criteria: human genetic studies written in English that were published between 1993 and 2004 and that reported allele frequencies for HLA-DRB1*1501, HLA-DQA1*0102, or HLA-DQB1*0602 or the frequency of the DRB1*1501-DQA1*0102-DQB1*0602 haplotype. Most of the studies identified used a case-control design (n = 60), while the remainder used a family-based design (n = 22). In most of these papers, investigators reported a higher frequency of the DR15 haplotype and/or its component alleles among MS cases than among controls. However, the authors' confidence in these results is tempered by factors related to study design that may have biased the outcomes.

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Sutedja, N. A., Otten, H. G., Cats, E. A., Piepers, S., Veldink, J. H., van der Pol, W. L., & van den Berg, L. H. (2010) · Neurology · doi:10.1212/wnl.0b013e3181d3e2f6 · Cited by 29
HLA-DRB1 allele heterogeneity influences multiple sclerosis severity as well as risk in Western Australia
Wu, J.-S., JAMES, I. R., Qiu, W., Castley, A. S. L., Christiansen, F., Carroll, W. M., Mastaglia, F. L., & Kermode, A. G. (2009) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2009.11.015 · Cited by 29
“Among the over 600 HLA-DRB1 alleles sequenced to date, the dominant association iswith theHLA-DRB1⁎1501allelewhich is found in over 50% of MS cases in all Caucasian populations so far studied (Schmidt et al., 2007) and which is more likely to be transmitted through the maternal line (Ramagopalan et al.”
HLA‐DRB1 and multiple sclerosis in Argentina
Patrucco, L., Larriba, J., Redal, M. A., Rojas, J. I., Argibay, P. F., & Cristiano, E. (2009) · European Journal of Neurology · doi:10.1111/j.1468-1331.2008.02523.x · Cited by 29
“The results of our study are in accordance with other Caucasian MS surveys that have found that HLADRB1*15 allele is strongly associated with MS disease [1,3,5] (Table 2).”
Result
Contributions of vitamin D response elements and HLA promoters to multiple sclerosis risk
Nolan, D. A., Castley, A. S. L., Tschochner, M., JAMES, I. R., Qiu, W., Sayer, D. C., Christiansen, F., Witt, C. S., Mastaglia, F. L., Carroll, W. M., et al. (2012) · Neurology · doi:10.1212/wnl.0b013e318263c407 · Cited by 28
Association of HLA-DRB1*1501 tagging rs3135388 gene polymorphism with multiple sclerosis
Benešová, Y., Vašků, A., Štourač, P., Hladíková, M., Fiala, A., & Bednařík, J. (2012) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2012.10.014 · Cited by 28
“(Schmidt et al., 2007).”
BackgroundResultInfluential
HLA associations with multiple sclerosis in Greece
Kouri, I., Papakonstantinou, S., Bempes, V., Vasiliadis, H. S., Kyritsis, A. P., & Pelidou, S. (2011) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2011.06.037 · Cited by 28
“Recently, Schmidt et al reviewed 70 papers on the association between the DR15 haplotype andMS and reported a higher frequency of the DR15 haplotype and/or its component alleles among MS cases than among controls [9].”
Immunopharmacological role of the Leukotriene Receptor Antagonists and inhibitors of leukotrienes generating enzymes in Multiple Sclerosis
Mirshafiey, A., & Jadidi‐Niaragh, F. (2010) · Immunopharmacology and Immunotoxicology · doi:10.3109/08923970903283662 · Cited by 28
“Through these genes, there are robust association between the HLA locus and susceptibility to MS [16], particularly DR15 haplotype and three alleles of DR2 haplotype, including DRB1*1501, DRB5*0101 and DQB1*0602 [17–19].”
Background
Pediatric Multiple Sclerosis: Genes, Environment, and a Comprehensive Therapeutic Approach
Cappa, R. N., Theroux, L. M., & Brenton, J. N. (2017) · Pediatric Neurology · doi:10.1016/j.pediatrneurol.2017.07.005 · Cited by 29
HLA DR and DQ alleles and haplotypes associated with clinical response to glatiramer acetate in multiple sclerosis
Dhib-Jalbut, S. S., Valenzuela, R. M., Ito, K., Kaufman, M., Picone, M. A., & Buyske, S. G. (2013) · Multiple Sclerosis and Related Disorders · doi:10.1016/j.msard.2013.02.005 · Cited by 27
“Genetic susceptibility in multiple sclerosis (MS) has been inferred from its association with HLA class-II major histocompatibility antigens which control cell mediated immunity (Schmidt et al., 2007).”
BackgroundResult
Clinical effectiveness and cost-effectiveness of beta-interferon and glatiramer acetate for treating multiple sclerosis: systematic review and economic evaluation
Meléndez‐Torres, G. J., Auguste, P., Armoiry, X., Maheswaran, H., Court, R. A., Madan, J. J., Kan, A., Lin, S., Counsell, C. E., Patterson, J. V., et al. (2017) · Health Technology Assessment · doi:10.3310/hta21520 · Cited by 27
Associated autoimmune diseases in patients with multifocal motor neuropathy and their family members
Cats, E. A., Bertens, A. S., Veldink, J. H., van den Berg, L. H., & van der Pol, W. L. (2011) · Journal of Neurology · doi:10.1007/s00415-011-6315-3 · Cited by 27
“We previously found that HLA-DRB1*15 is more prevalent among patients with MMN than in population based controls [15] similar to patients with MS [13].”
Result
The role of ERAP1 in autoinflammation and autoimmunity
Pepelyayeva, Y., & Amalfitano, A. (2019) · Human Immunology · doi:10.1016/j.humimm.2019.02.013 · Cited by 27
Association of HLA‐DRB1*15 allele and CSF oligoclonal bands in a Spanish multiple sclerosis cohort
Romero-Pinel, L., Martínez‐Yélamos, S., Bau, L., Matas, E., Gubieras, L., Pujal, J. M., Morandeira, F., Bas, J., & Arbizu, T. (2011) · European Journal of Neurology · doi:10.1111/j.1468-1331.2011.03379.x · Cited by 26
“Multiple sclerosis (MS) is an autoimmune demyelinating complex genetic disease in which the association with the HLA-DR2 haplotype has been well established in most studied populations [1].”
Background
Environmental Factors Related to Multiple Sclerosis in Indian Population
Malli, C., Pandit, L., D’Cunha, A., & Mustafa, S. (2015) · PLoS ONE · doi:10.1371/journal.pone.0124064 · Cited by 26
“Availability of suitable environmental triggers may determine the prevalence of autoimmune disorders such as MS given that genetic susceptibility is the same in most parts of the world [27].”
Background
The role of non-HLA single nucleotide polymorphisms in multiple sclerosis susceptibility
Bahreini, S. A., Jabalameli, M. R., Saadatnia, M., & Zahednasab, H. (2010) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2010.08.002 · Cited by 27
“Among the suspected susceptibility genes, HLA-DRB1 on chromosome 6p21 is the most remarkable locus contributed to MS genetic susceptibility (Schmidt et al., 2007).”
Background
Peptide mimotopes alter T cell function in cancer and autoimmunity
Slansky, J. E., & Nakayama, M. (2020) · Seminars in Immunology · doi:10.1016/j.smim.2020.101395 · Cited by 27
“Specific HLA alleles and haplotypes provide susceptibility or protection from the disease, such as susceptibility with DQ2 and DQ8 in celiac disease [49–51], DR3-DQ2/ DR4-DQ8 in type 1 diabetes [52–54], DQB1*0602 in narcolepsy [55, 56], and DR15-DQ6 in multiple sclerosis [57, 58].”
Background
Epigenetics in Multiple Sclerosis
Chan, V. S. F. (2020) · Advances in experimental medicine and biology · doi:10.1007/978-981-15-3449-2_12 · Cited by 27
Identification of Genetic Determinants of the Sexual Dimorphism in CNS Autoimmunity
Bearoff, F. M., Case, L. K., Krementsov, D. N., Wall, E. H., Saligrama, N., Blankenhorn, E. P., & Teuscher, C. (2015) · PLoS ONE · doi:10.1371/journal.pone.0117993 · Cited by 25
Macrophages and HLA-Class II Alleles in Multiple Sclerosis: Insights in Therapeutic Dynamics
Prapas, P., & Anagnostouli, M. C. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25137354 · Cited by 26
“DRB1*15:01 is often found in combination with DQB1*06:02 and DQA1*01:02 alleles [41]; this combination are risk markers for MS even though their functional role has been controversial.”
Background
Characterization of the major histocompatibility complex class II DOB, DPB1, and DQB1 alleles in cynomolgus macaques of Vietnamese origin
Ling, F., Wei, L., Wang, T., Wang, H., Zhuo, M., Du, H., Wang, J., & Wang, X. (2010) · Immunogenetics · doi:10.1007/s00251-010-0498-0 · Cited by 24
“It has been reported that HLA-DQB1 alleles have been associated as an increased risk of developing type 1 diabetes (Todd 1990; Todd 1997; Redondo et al. 2001), celiac disease (Murray et al. 2007), multiple sclerosis (Dyment et al. 1997; Schmidt et al. 2007, and narcolepsy (Kadotani et al. 1998).”
Background
TNFR2 limits proinflammatory astrocyte functions during EAE induced by pathogenic DR2b-restricted T cells
Raphael, I., Gomez‐Rivera, F., Raphael, R. A., Robinson, R. R., Nalawade, S. A., & Forsthuber, T. G. (2019) · JCI Insight · doi:10.1172/jci.insight.132527 · Cited by 24
“Discussion MS has both genetic and environmental predispositions, including HLA-DR2b (28).”
Background
Immunological tests and their interpretation in uveitis
Rathinam, S., Tuğal-Tutkun, İ., Agarwal, M., Vedhanayaki, R., Egriparmak, M., & Patnaik, G. (2020) · Indian Journal of Ophthalmology · doi:10.4103/ijo.ijo_570_20 · Cited by 22
“[119] Both idiopathic intermediate uveitis (pars planitis) and multiple sclerosis have been found to be associated with the HLA-DR15 subtype of HLA-DR2.”
Background
Haematopoietic Stem Cell Transplantation Results in Extensive Remodelling of the Clonal T Cell Repertoire in Multiple Sclerosis
Massey, J. C., Jackson, K., Singh, M., Hughes, B., Withers, B., Ford, C., Khoo, M., Hendrawan, K., Zaunders, J., Muylder, B. C.-D., et al. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.798300 · Cited by 26
Influence of HLA-DRB1 allele heterogeneity on disease risk and clinical course in a West Australian MS cohort: a high-resolution genotyping study
Wu, J.-S., JAMES, I. R., Qiu, W., Castley, A. S. L., Christiansen, F., Carroll, W. M., Mastaglia, F. L., & Kermode, A. G. (2010) · Multiple Sclerosis Journal · doi:10.1177/1352458510362997 · Cited by 22
“Of the more than 600 alleles so far identified at this locus the HLA-DRB1*1501 allele has been found in over 50% of cases of MS in most Caucasian populations studied.(3) Other alleles associated with an increased risk include HLA-DRB1*0301 (DR3 haplotype, or DR17), which has been reported in several populations,(4,5,6…”
Background
Autoantigens and autoantibodies in multiple sclerosis.
Mirshafiey, A., & Kianiaslani, M. (2013) · PubMed · Cited by 21
Replication analysis of variants associated with multiple sclerosis risk
Dashti, M., Ateyah, K., Alroughani, R., & Al-Temaimi, R. A. (2020) · Scientific Reports · doi:10.1038/s41598-020-64432-3 · Cited by 20
High resolution HLA analysis reveals independent class I haplotypes and amino-acid motifs protective for multiple sclerosis
Mack, S. J., Udell, J. B. M., Cohen, F., Osoegawa, K., Hawbecker, S. K., Noonan, D. A., Ladner, M. B., Goodridge, D., Trachtenberg, E., Oksenberg, J. R., et al. (2018) · Genes and Immunity · doi:10.1038/s41435-017-0006-8 · Cited by 20
“studies [4, 45, 46], DRB1*15:01~DQB1*06:02 confers very high disease risk in this population (OR= 3.”
Multiple sclerosis in Gypsies from southern Spain: prevalence, mitochondrial DNA haplogroups and HLA class II association
Fernández, Ó., Fernández, V., Martinez-Cabrera, V., Mayorga, C., Alonso, A., León, A., Arnal, C., Hens, M. J., Luque, G., de Ramón, E., et al. (2008) · Tissue Antigens · doi:10.1111/j.1399-0039.2008.01016.x · Cited by 20
6.7-kbp deletion in LILRA3 (ILT6) gene is associated with later onset of the multiple sclerosis in a Polish population
Wiśniewski, A., Wagner, M., Nowak, I., Bilińska, M. M., Pokryszko‐Dragan, A., Jasek, M., & Kuśnierczyk, P. (2012) · Human Immunology · doi:10.1016/j.humimm.2012.12.006 · Cited by 19
Familial multiple sclerosis in Greece: Distinct clinical and imaging characteristics in comparison with the sporadic disease
Katsavos, S., Artemiadis, A., Davaki, P., Stamboulis, E., Kilindireas, K., & Anagnostouli, M. C. (2018) · Clinical Neurology and Neurosurgery · doi:10.1016/j.clineuro.2018.08.021 · Cited by 19
Clinical and transcriptional recovery profiles in pediatric and adult multiple sclerosis patients
Menascu, S., Khavkin, Y., Zilkha‐Falb, R., Dolev, M., Magalashvili, D., Achiron, A., & Gurevich, M. (2020) · Annals of Clinical and Translational Neurology · doi:10.1002/acn3.51244 · Cited by 20
Multiple sclerosis in Colombia and other Latin American Countries
Toro, J., Cárdenas‐Robledo, S., Martínez, C., Urrutia, J., & Díaz, C. (2012) · Multiple Sclerosis and Related Disorders · doi:10.1016/j.msard.2012.09.001 · Cited by 19
“(2010) did not find an association between MS frequency and HLA-DRB1n1501, which is the allele most consistently associated with MS worldwide (Schmidt et al., 2007; Hafler et al., 2007; Esposito et al., 2010), including Latin American countries such as Mexico (Al aez et al.”
Background
Interleukin 2 Receptor α Gene Polymorphism and Risk of Multiple Sclerosis: A Meta-Analysis
Wang, L., Zhang, D.-M., Xu, Y.-M., & Sun, S.-L. (2011) · Journal of International Medical Research · doi:10.1177/147323001103900505 · Cited by 19
Genetic factors and multiple sclerosis in the Moroccan population: A role for HLA class II
Ouadghiri, S., Taoussi, K. E. A., Brick, C., Benhaddou, E. H. A., Benseffaj, N., Benomar, A., Yahyaoui, M., & Essakalli, M. (2013) · Pathologie Biologie · doi:10.1016/j.patbio.2013.05.002 · Cited by 18
The polymorphisms of human leukocyte antigen loci may contribute to the susceptibility and severity of severe aplastic anemia in Chinese patients
Wang, M., Nie, N., Feng, S., Shi, J., Ge, M., Li, X., Shao, Y., Huang, J., & Zheng, Y. (2014) · Human Immunology · doi:10.1016/j.humimm.2014.06.011 · Cited by 18
Sex-Specific Environmental Impacts on Initiation and Progression of Multiple Sclerosis
Leffler, J., Trend, S., Gorman, S., & Hart, P. H. (2022) · Frontiers in Neurology · doi:10.3389/fneur.2022.835162 · Cited by 19
“There are several risk factors for MS, including genetic polymorphisms, relating mainly to variants in HLA-DR, where HLA-DRB115:01 has the strongest link with increased risk of MS (13).”
Background
ALCAM — Novel multiple sclerosis locus interfering with HLA-DRB1*1501
Wagner, M., Wiśniewski, A., Bilińska, M. M., Pokryszko‐Dragan, A., Nowak, I., Kuśnierczyk, P., & Jasek, M. (2013) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2013.02.015 · Cited by 18
“This association on almost the same cohort of patients and controls was earlier detected in our laboratory and described by Wiśniewski et al. (2013). This result is in line with those obtained in most European populations (Schmidt et al.”
Result
Tumor necrosis factor polymorphisms associated with tumor necrosis factor production influence the risk of idiopathic intermediate uveitis.
Atan, D., Heissigerova, J., Kuffová, L., Hogan, A. C., Kilmartin, D. J., Forrester, J. V., Bidwell, J. L., Dick, A. D., & Churchill, A. (2013) · Europe PMC (PubMed Central) · Cited by 17
Vitamin D receptor biochemical and genetic profiling and HLA-class II genotyping among Lebanese with multiple sclerosis — A pilot study
Yamout, B., Karaky, N., Mahfouz, R. A., Jaber, F., Estaitieh, N., Shammaa, D. M. R., Abbas, F., Hoteit, R. M., & Daher, R. T. (2016) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2016.02.008 · Cited by 17
“Furthermore, no interaction between DRB1*15 and DRB1*08 was observed in our study; a combination usually known to increase the susceptibility to MS (Schmidt et al., 2007).”
Multiple Sclerosis: Epidemiology, Genetics, Symptoms, and Unmet Needs
Moreno‐Torres, I., Muñoz, J. S., & García‐Merino, A. (2019) · Royal Society of Chemistry eBooks · doi:10.1039/9781788016070-00001 · Cited by 18
An impact of air pollution on moderate to severe relapses among multiple sclerosis patients
Elgabsi, M., Novack, L., Yarza, S., Elgabsi, M., Shtein, A., & Ifergane, G. (2021) · Multiple Sclerosis and Related Disorders · doi:10.1016/j.msard.2021.103043 · Cited by 17
FutureMS cohort profile: a Scottish multicentre inception cohort study of relapsing-remitting multiple sclerosis
Kearns, P. K. A., Martin, S. J., Chang, J. C., Meijboom, R., York, E. N., Chen, Y., Weaver, C., Stenson, A., Hafezi, K., Thomson, S., et al. (2022) · BMJ Open · doi:10.1136/bmjopen-2021-058506 · Cited by 16
HLA-DRB1*15:01 and Epstein–Barr virus in a multiple sclerosis patient with psoriasis, nasopharyngeal and breast cancers. Lessons for possible hidden links for autoimmunity and cancer
Anagnostouli, M. C., Anagnostoulis, G., Katsavos, S., Panagiotou, M., Kararizou, E. G., & Davaki, P. (2014) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2014.02.003 · Cited by 17
“The various different conditions and subsequent treatments previously analyzed are summarized in Table 2, with comments on possible HLA and EBV correlations, based on the international literature [1,2,6–8,22–32].”
Method
Occupational Exposure and Risk of Central Nervous System Demyelination
Valery, P. C., Lucas, R. M., Williams, D. B., Pender, M. P., Chapman, C., Coulthard, A., Dear, K. B. G., Dwyer, T., Kilpatrick, T. J., McMichael, A. J., et al. (2013) · American Journal of Epidemiology · doi:10.1093/aje/kws361 · Cited by 17

Authors: Schmidt, H., Williamson, D., & Ashley-Koch, A.
Affiliations: Accelerated Cure Project for Multiple Sclerosis (US)
Centers for Disease Control and Prevention (US)
ORCID: Schmidt, Hollie
Williamson, Dhelia
Venue: American Journal of Epidemiology
Publisher: Oxford University Press (OUP)
Published: 2007-02-28
Volume: 165
Issue: 10
Pages: 1097-1109
ISSN: 0002-9262 (ISSN-L)
1476-6256
DOI: 10.1093/aje/kwk118
OpenAlex: W2146798707
Cited by: 212
References: 146
Citations by year: 2026: 10 · 2025: 9 · 2024: 10 · 2023: 5 · 2022: 12 · 2021: 8 · 2020: 14 · 2019: 10 · 2018: 16 · 2017: 13 · 2016: 9 · 2015: 14 · 2014: 7 · 2013: 15 · 2012: 13
FWCI: 0.96
Type: journal article
Language: en
Open access: closed
Locations: American Journal of Epidemiology (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Clinical Neurology › Multiple Sclerosis Research Studies
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Associations and Epidemiology
Life Sciences › Immunology and Microbiology › Immunology › Psoriasis: Treatment and Pathogenesis
Keywords: multiple sclerosis, HLA-DRB1*1501, HLA-DQA1*0102, HLA-DQB1*0602, genetic susceptibility, HLA complex, allele frequency, case-control study, family-based association study, study design bias
MeSH terms: Alleles, Multigene Family, Haplotypes, HLA-D Antigens, Humans, Multiple Sclerosis

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HLA-DR15 Haplotype and Multiple Sclerosis: A HuGE Review

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