HLA-DR

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ligand (Staphylococcal enterotoxin 1-C peptide:pkyvkqntlklat) within the binding pocket of DR αβ101
DR1 binding pocket with ligand PDB 2G9H [1]
major histocompatibility complex, class II, DR
Structure
Type Cell surface receptor
Subunit αβ-heterodimer
MMDB 40432
Identifiers
alpha
Symbol(s) HLA-DRA, HLA-DRA1
Entrez 3122
OMIM 142860
Identifiers
beta 1
beta 3
Symbol(s) HLA-DRB1 HLA-DRB3
Entrez 3123 3125
OMIM 142857
Identifiers
beta 4
beta 5
Symbol(s) HLA-DRB4 HLA-DRB5
Entrez 3126 3127
OMIM 604776
Shared data
Locus chr.6 6p21.31

HLA-DR is a major histocompatibility complex, class II, cell surface receptor encoded by the human leukocyte antigen complex on chromosome 6 region 6p21.31. Receptor is frequently found with ligand, a peptide of 9 amino acids in length or longer, within the binding groove. The receptor/peptide complex is a ligand for T-cell receptor (TCR). HLA, human leukocyte antigens, were originally defined as cell surface antigens that mediate graft-versus-host disease, which resulted in the rejection of tissue transplants in HLA mismatched donors. Identification of these antigens has lead to greater success and longevity in organ transplant.

HLA-DR is also involved in several autoimmune conditions, disease susceptibility and disease resistance. It is also closely linked to HLA-DQ and this linkage often makes it difficult to resolve the more causative factor in disease.

Molecules particularly HLA-DR are upregulated in response to signalling. In the instance of an infection the peptide (such as the staphlococcal enterotoxin I peptide show in the two illustrations) is bound into a DR molecule and presented to a few of a great many T-cell receptors found on T-helper cells. These cells then bind to antigens on the surface of B-cells stimulating B-cell proliferation.

Contents

[edit] Function

Illustration of DR receptor presenting antigen to TCR on T-helper cell
Illustration of DR receptor presenting antigen to TCR on T-helper cell

The primary function of HLA-DR is to present peptide antigens, potentially foreign in origin, to the immune system for the purpose of eliciting or suppressing T-(helper)-cell responses that eventually lead to the production of antibodies against the same peptide antigen. Antigen presenting cells (macropahges, B-cells and dendritic cells) are the cells in which DR are typically found. Increased abundance of DR 'antigen' on the cell surface is often in response to stimulation, and, therefore, DR is also a marker for immune stimulation.

[edit] Structure

HLA-DR is a αβ heterodimer, cell surface receptor, each subunit contains 2 extracellular domains, a membrane spanning domain and a cytoplasmic tail. Both α and β chains are anchored in the membrane. The N-terminal domain of the mature protein forms an alpha-helix that forms the exposed part of the binding groove, the C-terminal cytoplasmic region interact with the other chain forming a beta-sheet under the binding groove spanning to the cell membrane. The majority of the peptide contact positions are in the 1st 80 residues of each chain.

[edit] Genetics

The genetics of HLA-DR is complex. HLA-DR is encoded by several loci

  • α-chain
    • DRA (DRA1) locus
      • functional variation in mature DRA gene products is absent
      • (see table) reduces the potential functional combinations from ~1400 to ~400 (table is not exact because new alleles are continually being added not all new alleles are functional variants of the mature subunits.
28 (of 75) Most common DR-DQ haplotypes in Caucasian Americans
DR DR-DQ DR DQ Freq
Serotype haplotype B1 A1 B1 %[2] rank
DR1 DR1-DQ5 0101 0101 0501 9. 1 4
0102 0101 0501 1. 4 15
0103 0101 0501 0. 5 25
DR3 DR3-DQ2 0301 0501 0201 13. 1 2
DR4 DR4-DQ7 0401 0300 0301 5. 4 7
0407 0300 0301 0. 9 19
DR4-DQ8 0401 0300 0302 5. 0 8
0402 0300 0302 1. 0 17
0403 0300 0302 0. 4 26
0404 0300 0302 3. 9 9
0405 0300 0302 0. 3 28
DR7 DR7-DQ2 0701 0201 0202 11. 1 3
DR7-DQ9 0701 0201 0303 3. 7 10
DR8 DR8-DQ4 0801 0401 0402 2. 2 13
DR8-DQ7 0803 0601 0301 0. 1 rare
DR9 DR9-DQ9 0901 0300 0303 0. 8 20
DR10 DR10-DQ5 1001 0104 0501 0. 7 22
DR11 DR11-DQ7 1101 0505 0301 5. 6 5
1103 0505 0301 0. 3 27
1104 0505 0301 2. 7 12
DR12 DR12-DQ7 1201 0505 0301 1. 1 10
DR13 DR13-DQ6 1301 0103 0603 5. 6 6
1302 0102 0604 3. 4 11
1302 0102 0609 0. 7 22
DR13-DQ7 1303 0505 0301 0. 7 21
DR14 DR14-DQ5 1401 0104 0503 2. 0 14
DR15 DR15-DQ6 1501 0102 0602 14. 2 1
1502 0103 0602 0. 7 24
DR16 DR16-DQ5 1601 0102 0502 1. 0 18
  • β-chain [3]
    • DRB1 locus (ubiquitous)
      • very large number of functionally variable gene products.
    • DRB3 locus (variable-associated with certain DR types)
      • modest number of functionally variable gene products.
    • DRB4 locus (variable-associated with certain DR types)
      • modest number of functionally variable gene products.
    • DRB5 locus (variable-associated with certain DR types)
      • modest number of functionally variable gene products.
  • linkage (See Table)
    • DQA1 and DQB1
      • Linkage disequilibrium exists for many DR-DQ types.
    • Nomenclature issues. Some older studies may refer to DR15 or 16 as DR2 and DQ5 and DQ6 as DQ1 therefore a haplotype DR2-DQ1 is usually referring to DR15-DQ6 but could be referring to DR16-DQ5. DR5 is used to refer to DR11 and DR12, in which case DQ3 might be used. In these instances DQ3 almost always can be interpreted as DQ7, but DR5 is most often DR11 and less frequently DR12. Similar issues exist for DR6 versus DR13 and DR14. DR6-DQ1 can refer to either DR13-DQ6 or less frequently DR14-DQ5, but DR6-DQ3 or DR6-DQ7 generally refers to DR13-DQ7. Even older literature has more confusing designations. By looking at the change of disease association with improved testing we can see how science has evolved over time.

[edit] Evolution and Allele Frequencies

There is a relatively extreme level of allelic diversity at HLA DRB1, it is second only to HLA-B locus in number of allelic variants, these two probably top coding sequence variation rate within human genome. This means HLA-DRB1 is rapidly evolving, much more rapidly than almost all other genomic loci. Much of the variation at HLA DRB1 occurs at peptide contact positions in the binding groove, as a result many of the alleles alter the way the DR binds peptide ligands and changes the repertoire each receptor can bind. This means that most of the changes are functional in nature, and therefore are under selection. In the HLA region, genes are under heterozygous or balancing selection, although certain alleles appear to be under positive or negative selection, either in the past or present
HLA generally evolve through a process of gene conversion a form of short distance or 'abortive' recombination. Functional motifs in other HLA are transferred to form new alleles, and frequently new DR isoforms. HLA-DR represents an extreme example of this. A survey of X-linked chromosome reveals that most human loci have undergone fixation within the last 600,000 years, and diploid loci have undergone significant proportion of fixation in that period of time. The level of deep branching at X-linked loci indicates loci were close to fixation or fixed at the end of the human population bottleneck ~150 kya. The HLA-DR locus represents a major exception to this observation[4]. Based on distribution of mjor groupings in the Human population it is possible to assert that more than a dozen major variants survived the constriction. This observation is supported by the concept of a heterozygous selection coefficient operating on the HLA-DR, and at the HLA-DRB1 locus to a greater degree relative to HLA-DQB1 and HLA-DPB1. Most of the HLA alleles currently present in the human population can be explained by gene conversion between these ancient ancestral types[5], some that persist into the extant population.

[edit] Disease associations

Because DR alleles are in disequilibrium with HLA-DQ loci, early studies often cannot resolve exact disease association. In such cases the DR-DQ haplotype will be referred to. See table above on DR-DQ linkage in caucasians. (*#### = DRB1*####)

[edit] DR1

Diseases associated with DR1 serotypes or cognate alleles are: seronegative[6]-rheumatoid arthritis[7][8], penicillamine-induced myasthenia[9], and schizophrenia[10]


[edit] DR2

DR2 is a broad antigen serotype made up of split antigens DR15 and DR16 serotypes. Diseases associated with DR2 serotypes or cognate alleles are: Goodpasture syndrome, multiple sclerosis[19], and narcolepsy, tuberculoid leprosy[20], Hashimoto's thyroiditis[21], ulcerative colitis(Japanese)[22], biliary cirrhosis and autoimmune hepatitis[23]

[edit] DR15

Goodpasture syndrome[24], early age onset multiple schlerosis[25], pernicious anaemia[26]

  • 15:DQA1*0102:DQB1*0602 haplotype: cervical cancer (human papillomavirus infection)[27]
  • *1501: Goodpasture syndrome[28][29], juvenile rheumatoid arthritis [30], allergic bronchopulmonary aspergillosis[31], multiple schlerosis[32], systemic lupus erythematosus[33], cervical cancer (human papillomavirus infection)[34], and Sjogren's syndrome associated with systemic lupus erythematosus[35]
    • *1501:DQA1*0102:DQB1*0602 haplotype: cervical cancer (human papillomavirus infection)[34]
  • *1502: Systemic lupus erythematosus[36], systemic sclerosis (SSc) & anti-DNA topoisomerase I (anti-topo I) antibody[37]
    • *1502:DQA1*????:DQB1*0501 haplotype: Systemic lupus erythematosus[36]
  • *1503: Trypannosome cruzi infection with cardiomyopathy[38], allergic bronchopulmonary aspergillosis[39], multiple sclerosis[32], cervical cancer (human papillomavirus infection)[27]

[edit] DR16

Chaga's cardiomyopathy[40], rheumatic heart disease[41], coronary artery ectasia[42], and

  • *1601: Tubeculousis risk[43]
    • *1601:DQA1*0102:DQB1*0502 haplotype: Tubeculousis risk [43]
  • *1602: Juvenile rheumatoid arthritis[30], rheumatic heart disease[41], Takayasu arteritis[44], systemic sclerosis (SSc) & anti-DNA topoisomerase I (anti-topo I) antibody [37][45], melioidosis (Burkholderia pseudomallei infection)[46]
    • *1602:DQA1*0102:DQB1*0502 haplotype: graves disease[47][48], cervical caner (human papilloma virus infection)[49], schleroderma[50]
    • *1602:DQA1*05:DQB1*0301 haplotype: rheumatic heart disease[41], systemic schlerosis[51]


[edit] DR3

DR3 is composed to the DR17 and DR18 split 'antigens' serotypes. Diseases associated with DR2 serotypes or cognate alleles are: early-age onset myasthenia gravis, and opportunistic infections in AIDS[citation needed]. DRB1 alleles covered by DR17 and DR18 include rare *0305, *0306 alleles

[edit] DR17

non-chronic sarcoidosis[52][53], infantile spasm/epilepsy[54], rabies vaccine-induced autoimmune encephalomyelitis[55] and cardiovascular hypertrophy in subjects with arterial hypertension[56]

[edit] DR18

rheumatoid polyarthritis[72]


[edit] DR4

DR4 serotype is a diverse subgroup of antigens composed of several alleles. Diseases associated with DR4 serotype or cognate alleles are: extraarticular[73]rheumatoid arthritis[74], hydralazine-induced female systemic lupus erythematosus[75],pemphigoid gestationis[76], phemphigus foliaceus[77], hypertrophic obstructive cardiomyopathy[78], IgA nephropathy[79]

  • *0401: multiple sclerosis[80], rheumatoid arthritis[81], type 1 diabetes[82][83], lyme disease induced arthritis[84]
  • *0402: drug-triggered[85]/idiopathic pemphigus vulgaris[86], type 1 diabetes[87], SLE associated anti-cardiolipin and anti-beta2GPI[88]
  • *0403: polycystic ovary syndrome[89], SLE associated anti-cardiolipin and anti-beta2GPI[90]
  • *0404: anti-citrullinated fibrinogen[91] in rheumatoid arthritis[92], autoimmune hepatitis[93]
  • *0405: rheumatoid arthritis[94], Autoimmune hepatitis[95], type 1 diabetes[96][97]
    • as part of :DQA1*0303-DQB1*0401 haplotype: type III autoimmune polyglandular syndrome[98], autoimmune hepatitis [99], autoimmune pancreatitis[100]
    • as part of :DQA1*03-DQB1*0302 haplotype: Type 1 diabetes[101][102]
  • *0406: caspase-8 autoantibodies silicosis-systemic sclerosis (SSc)-systemic lupus erythematosus (SLE)[103]
  • DR4-DQ8 juvenile diabetes,coeliac disease, rheumatoid arthritis[104]
  • *0409: T. cruzi infection with cardiomyopathy[38]



[edit] DR5

- persistent generalized lymphadenopathy (PGL)[105] and Kaposi sarcoma in AIDS[106], juvenile rheumatoid arthritis[107][108], goitrous autoimmune thyroiditis[109][110], mycosis fungoides[111], polyglandular deficiency syndrome[112], systemic sclerosis[113][114], childhood epilepsy[115], early-onset alopecia areata[116], short-ragweed Ra6 allergy[117], primary antiphospholipid syndrome[118], and increased longevity in the Dutch[119]

[edit] DR11

Diseases associated with DR11 serotype or cognate alleles are: Grape anaphylaxis[120], well-differentiated thyroid cancer[121], low antibody production in Hepatitis C[122]*

  • *11: systemic sclerosis (SSc) & anti-DNA topoisomerase I (anti-topo I) antibody [37]
  • *11:DQA1*0505:DQBA1*0301 haplotype: Trans-haplotype isoform celiac disease[123]
  • *1101: Anti-Ro/SSA with anti-La/SSB antibodies in neonatal lupus erythematosus [124], mite sensitive asthma[125], cervical cancer risk (HPV?)[126]
    • *1101:DQA1*0505:DQB1*0301 haplotype: Anti-Ro/SSA with anti-La/SSB antibodies in neonatal lupus erythematosus[124], mite sensitive asthma[125]
  • *1102: Tiopronin intolerance in rheumatoid arthritis[127]
    • *1102:DQA1*0505:DQB1*0301 haplotype: hepatitis B virus persistence[128]
  • *1104: pauciarticular juvenil rheumatoid arthritisJuvenile rheumatoid arthritis[30]

[edit] DR12

Vulval lichen schlerosis [129]

  • *12
    • *12:DQA1*0505:DQBA1*0301 haplotype: Trans-haplotype isoform celiac disease[123], primary antiphospholipid syndrome[130], Tiopronin intolerance in rheumatoid arthritis[127], adult chronic articular Still's disease[131]
    • *1201:DRB3*01/03: colorectal cancer[132]


[edit] DR6

DR6 is a broad-antigen serotype that is further split into DR13 and DR14 antigen serotypes.

[edit] DR13

  • *1302: Early childhood myastenia gravis[133]
    • *1032:DQA1*0102:DQB1*0604: Early childhood myastenia gravis[133]

[edit] DR14

  • *14
    • *14:DQ5 haplotype: increased risk for non-AChR autoantibodies in myasthenia gravis.
  • *1402: juvenile rheumatoid arthritis[30], increased longevity in Okinawans.


[edit] DR7

psoriasis vulgaris

  • *07: T. cruzi infection with cardiomyopathy[38]

[edit] DR8

papillary thyroid carcinomas [134], early onset pauciarticular juvenile chronic arthritis[135][136], primary biliary cirrhosis[137]

  • *0801: primary biliary cirrhosis[138]
  • *0803: primary biliary cirrhosis[138]

[edit] DR9

  • *0901: Early childhood myastenia gravis[133]
    • *0901:DQA1*0301:DQB1*0303 haplotype: Early childhood myastenia gravis[133]

[edit] DR10

DR10 sertoype or cognate alleles are associated with: Lichen planus[139]

  • *1001: Ovarian cancer[140] and invasive squamous cell cervical cancer (SCC)[141]
    • *1001:DQA1*01:DQB1*05 haplotype: Rheumatoid arthritis[142]

[edit] DR51

The following HLA-DRB5 alleles are associated with disease:

  • *0101:
    • *0101:DRB1*1501 Multiple schlerosis[143], leprosy[144]

[edit] DR52

The following DRB3* alleles show association with disease:

  • *0101: Grave's Disease[145][146], pulmonary sarcoidosis[147]
    • *0101:DRB1*0301 : Lofgren's syndrome[148]
  • *0202: Grave's disease[146], serum IgG antibodies to Chlamydia pneumoniae with essential hypertension,[149], acute necrotizing encephalopathy[150]
  • *0301: weak association with anti-cardiolipin antibodies in SLE[151]
    • *0301:DRB1*1302: Crohn's diseaes[152]

[edit] DR53

The HLA-DRB4 alleles are associated with the following diseases:

  • *0101: Hashimoto's thyroiditis[153], vitiligo[154], primary biliary cirrhosis[155], clozapine-induced agranulocytosis[156], Vogt-Koyanagi-Harada [157]

[edit] Nomenclature

Number of Variant Alleles HLA-DR Loci
HLA-DR
HLA -A1 -B1 -B3 to -B51 Potential
Locus # # # Combinations
Alleles[3][158] 3 463 74 1635
Unique Polypeptide 2 394 57 902
Contact Variant 1 ~300 ~30 ~330
1DRB3, DRB4, DRB5 have variable presence in humans

Since DRA gene product is functionally invariable is not necessary to define in the nomenclature DR1 to DR18 serogroups and cognate allele groups. For details about serotypable alleles in each group see Marsh et al[3]. The values in the database change monthly however most of the new entries are very rare alleles. This information is current as of October 2006[158]

[edit] DRB1 Locus

DRB1*01 allele group

  • 21 Alleles: 16 proteins, 0 Nulls
  • DR1 Serotype: *0101, *0102, *0105, *0107, *0108, *0111, *0113, *0114
  • DR1/DR103: *0103
  • Serotype unknown: *0104, *0106, *0109, *0110, *0112, *0115, *0116


DRB1*03 allele group

  • 36 Alleles: 31 proteins
  • DR3(Only) Serotype: *0304, *0307
  • DR17(DR3) Serotype: *0301, (*0303), (*0304)
  • DR18(DR3) Serotype: *0302, *0303
  • Serotype unknown: *0305, *0306, *0308 to *0331


DRB1*04 allele group

  • 68 Alleles: 60 proteins
  • DR4 Serotype: *0401 to *0416
  • Serotype unknown: *0417 to *460


DRB1*07 allele group

  • 12 Alleles: 9 proteins, 1 null
  • DR7 Serotype: *0701, *0704
  • Serotype unknown: *0703, *0705 to *0709, *0711
  • Null: *0710N


DRB1*08 allele group

  • 39 Alleles: 32 proteins
  • DR8 Serotype: *0801 to *0807, and *0810 to *0812
  • Serotype unknown: *0808, *0809, *0813 to *0832


DRB1*09 allele group

  • 7 Alleles: 6 proteins
  • DR9 Serotype: *0901
  • Serotype unknown: *0902 to *0906


DRB1*10 allele group

  • 2 Alleles: 1 proteins
  • DR10 Serotype: *1001


DRB1*11 allele group

  • 73 Alleles: 57 proteins
  • DR11 (weak DR5) Serotype: *1101 to *1105, *1107 to *1110
  • DR5 (weak DR11) Serotype: *1106
  • Serotype unknown: *1111 to *1157


DRB1*12 allele group

  • 17 Alleles: 15 proteins
  • DR12 (weak or no DR5) Serotype: *1201 to *1203, *1206
  • Serotype unknown: *1204, *1205, *1207 to *1215


DRB1*13 allele group

  • 81 Alleles: 74 proteins
  • DR13 (weak or no DR6) Serotype: *1301, *1302, *1304, *1306, *1307, *1310, *1312 to *1314
  • DR6 (weak DR13) Serotype: *1308
  • DR13&Other serotypes: *1303, *1305, *1311,
  • Serotype unknown: *1309, *1315 to *1374


DRB1*14 allele group

  • 68 Alleles: 62 proteins
  • DR14 (weak or no DR6) Serotype: *1401, *1403 to *1405, *1407, *1410 to *1411, *1413 to *1414
  • DR6 (weak DR14) Serotype:
  • DR14&Other serotypes: *1402, *1406, *1408, *1415, *1418
  • Serotype unknown: *1409, *1419 to *1462
  • [Neural Network analysis assigned *1412, *1416, *1417 to broad group DR6, *1415 to DR8]


DRB1*15 allele group

  • 29 Alleles: 21 proteins, 1 Null
  • DR15 (weak or no DR2) Serotype: *1501 to *1505, *1507
  • Serotype unknown: *1506, *1508 to *1516, *1518 to *1522
  • Null: *1517N


DRB1*16 allele group

  • 13 Alleles: 10 proteins
  • DR16 (weak or no DR2) Serotype: *1601, *1602, *1604
  • DR2 (weak DR16) Serotype:
  • DR16&Other serotypes:
  • Serotype unknown: *1603, *1605, *1607 to *1611


[edit] DRB3 Locus

DRB3*01 allele group

  • 15 Alleles: 11 proteins
  • DR52 Serotype: *0101, *0102
  • Serotype unknown: *0103 to *0111

DRB3*02 allele group

  • 25 Alleles: 21 proteins
  • DR52 Serotype: *0201 to *0203
  • Serotype unknown: *0204 to *0221

DRB3*03 allele group

  • 4 Alleles: 3 proteins
  • DR52 Serotype: *0301,
  • Serotype unknown: *0302 to *0303


[edit] DRB4 Locus

  • 13 Alleles: 7 proteins, 4 Nulls
  • DR53 Serotype: *0101, *0103
  • Serotype unknown: *0102, *0104 to *0107
  • Nulls: *0101102N, *01030102N, *0201N, *0301N


[edit] DRB5 Locus

DRB5*01 allele group

  • 14 Alleles: 11 proteins, 2 Nulls
  • DR51 Serotype: *0101, *0102
  • Serotype unknown: *0103 to *0107, *0109, *0110 to *0113
  • Nulls: *0108N, *0110N

DRB5*02 allele group

  • 4 Alleles: 4 proteins
  • DR51 Serotype: *0202,
  • Serotype unknown: *0203 to *0205

[edit] DRB Linkage

DRB1 is linked with other DRB loci in 4 ways

No linkage.

  • DRB1*allele groups
    • *01
    • *08
    • *10

Linkage with DRB3.

  • DR3
    • *03
  • DR5
    • *11
    • *12
  • DR6
    • *13
    • *14

Linkage with DRB4

  • DRB1 allele groups.
    • *07
    • *09

Linked with DRB5 DRB1 allele groups.

  • DR2
    • *15
    • *16

[edit] External links

  • MeSH HLA-DR+antigens
  • Antoniades CG, Berry PA, Davies ET, Hussain M, Bernal W, Vergani D, Wendon J. (2006). "Reduced monocyte HLA-DR expression: A novel biomarker of disease severity and outcome in acetaminophen-induced acute liver failure.". Hepatology 44 (1): 34-43. PMID 16799971. 
  • Lekkou A, Karakantza M, Mouzaki A, Kalfarentzos F, Gogos C (2004). "Cytokine production and monocyte HLA-DR expression as predictors of outcome for patients with community-acquired severe infections.". Clin Diagn Lab Immunol 11 (1): 161-7. PMID 14715564. 

[edit] References

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  2. ^ Klitz W, Maiers M, Spellman S, Baxter-Lowe LA, Schmeckpeper B, Williams TM, and Fernandez-Vina M (2003). "New HLA haplotype frequency reference standards: high-resolution and large sample typing of HLA DR-DQ haplotypes in a sample of European Americans.". Tissue Antigens 62 (4): 296-307. PMID 12974796. 
  3. ^ a b c Marsh SG, Albert ED, Bodmer WF, Bontrop RE, Dupont B, Erlich HA, Geraghty DE, Hansen JA, Hurley CK, Mach B, Mayr WR, Parham P, Petersdorf EW, Sasazuki T, Schreuder GM, Strominger JL, Svejgaard A, Terasaki PI, and Trowsdale J. (2005). "Nomenclature for factors of the HLA System, 2004.". Tissue antigens 65: 301-369. PMID 15787720. 
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  5. ^ Parham P, Ohta T (1996). "Population biology of antigen presentation by MHC class I molecules.". Science 272 (5258): 67-74. PMID 8600539. 
  6. ^ Bardin T, Legrand L, Naveau B, Marcelli-Barge A, Debeyre N, Lathrop G, Poirier J, Schmid M, Ryckewaert A, Dryll A (1985). "HLA antigens and seronegative rheumatoid arthritis.". Ann Rheum Dis 44 (1): 50-3. PMID 3855618. 
  7. ^ Schiff B, Mizrachi Y, Orgad S, Yaron M, Gazit E (1982). "Association of HLA-Aw31 and HLA-DR1 with adult rheumatoid arthritis.". Ann Rheum Dis 41 (4): 403-4. PMID 6981387. 
  8. ^ (1986) "HLA-DR antigens in rheumatoid arthritis. A Swiss collaborative study; final report. Swiss Federal Commission for the Rheumatic Diseases, Subcommission for Research.". Rheumatol Int 6 (2): 89-92. PMID 3489975. 
  9. ^ Delamere J, Jobson S, Mackintosh L, Wells L, Walton K (1983). "Penicillamine-induced myasthenia in rheumatoid arthritis: its clinical and genetic features.". Ann Rheum Dis 42 (5): 500-4. PMID 6605118. 
  10. ^ Narita K, Sasaki T, Akaho R, Okazaki Y, Kusumi I, Kato T, Hashimoto O, Fukuda R, Koyama T, Matsuo K, Okabe Y, Nanko S, Hohjoh H, Tokunaga K (2000). "Human leukocyte antigen and season of birth in Japanese patients with schizophrenia.". Am J Psychiatry 157 (7): 1173-5. PMID 10873932. 
  11. ^ del Mar Sáez-de-Ocariz M, Vega-Memije M, Zúñiga J, Salgado N, Ruíz J, Balbuena A, Domínguez-Soto L, Granados J (2005). "HLA-DRB1*0101 is associated with foliaceous pemphigus in Mexicans.". Int J Dermatol 44 (4): 350. PMID 15811100. 
  12. ^ Sabouri A, Saito M, Usuku K, Bajestan S, Mahmoudi M, Forughipour M, Sabouri Z, Abbaspour Z, Goharjoo M, Khayami E, Hasani A, Izumo S, Arimura K, Farid R, Osame M (2005). "Differences in viral and host genetic risk factors for development of human T-cell lymphotropic virus type 1 (HTLV-1)-associated myelopathy/tropical spastic paraparesis between Iranian and Japanese HTLV-1-infected individuals.". J Gen Virol 86 (Pt 3): 773-81. PMID 15722539. 
  13. ^ a b Cardoso C, Uthida-Tanaka A, Magalhães R, Magna L, Kraemer M. "Association between psoriasis vulgaris and MHC-DRB, -DQB genes as a contribution to disease diagnosis.". Eur J Dermatol 15 (3): 159-63. PMID 15908298. 
  14. ^ Bonagura V, Vambutas A, DeVoti J, Rosenthal D, Steinberg B, Abramson A, Shikowitz M, Gjertson D, Reed E (2004). "HLA alleles, IFN-gamma responses to HPV-11 E6, and disease severity in patients with recurrent respiratory papillomatosis.". Hum Immunol 65 (8): 773-82. PMID 15336778. 
  15. ^ a b >Levinson R, Park M, Rikkers S, Reed E, Smith J, Martin T, Rosenbaum J, Foster C, Sherman M, Holland G (2003). "Strong associations between specific HLA-DQ and HLA-DR alleles and the tubulointerstitial nephritis and uveitis syndrome.". Invest Ophthalmol Vis Sci 44 (2): 653-7. PMID 12556395. 
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