HLA and pharmacogenetics of drug hypersensitivity

Pharmacogenomics

Volumn 13, Issue 11, 2012, Pages 1285-1306

  Pavlos, Rebecca ^a   Mallal, Simon ^a,b   Phillips, Elizabeth ^a,b,c,d  

^a MURDOCH UNIVERSITY   (Australia)

^b ROYAL PERTH HOSPITAL   (Australia)

^c SIR CHARLES GAIRDNER HOSPITAL   (Australia)

^d UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

altered peptide repertoire; DILI; DRESS; human leukocyte antigen; hypersensitivity; major histocompatibility complex; pharmacogenetics; pharmacogenomics; Stevens Johnson syndrome; toxic epidermal necrolysis; translation

Indexed keywords

ABACAVIR; ALLOPURINOL; AMINOPENICILLIN; AMOXICILLIN PLUS CLAVULANIC ACID; ANTICONVULSIVE AGENT; ANTIRETROVIRUS AGENT; BETA LACTAM ANTIBIOTIC; CARBAMAZEPINE; CLOZAPINE; EFAVIRENZ; FEPRAZONE; FLUCLOXACILLIN; FOSAMPRENAVIR; HLA ANTIGEN; ISONIAZID; LAMOTRIGINE; LEVAMISOLE; LUMIRACOXIB; METHAZOLAMIDE; NEVIRAPINE; NONSTEROID ANTIINFLAMMATORY AGENT; OXCARBAZEPINE; OXICAM DERIVATIVE; PHENOBARBITAL; PHENYTOIN; SULFAMETHOXAZOLE; SULFONAMIDE; TETRACYCLINE DERIVATIVE; UNINDEXED DRUG; XIMELAGATRAN;

AGRANULOCYTOSIS; AMINO ACID SUBSTITUTION; ANAPHYLAXIS; ARTICLE; CD4 LYMPHOCYTE COUNT; CD8+ T LYMPHOCYTE; CRYSTAL STRUCTURE; CYTOTOXIC T LYMPHOCYTE; DELAYED HYPERSENSITIVITY; DELAYED RASH; DRESS SYNDROME; DRUG ERUPTION; DRUG FEVER; DRUG HYPERSENSITIVITY; DRUG RECHALLENGE; FIXED DRUG ERUPTION; GASTROINTESTINAL SYMPTOM; GENE FREQUENCY; GENE LINKAGE DISEQUILIBRIUM; GENETIC ASSOCIATION; GENETIC PREDISPOSITION; GENETIC RISK; GENETIC SCREENING; GENETIC SUSCEPTIBILITY; GOUT; HETEROZYGOTE; HLA TYPING; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HYPERURICEMIA; HYPOTENSION; IMMUNOPATHOGENESIS; LUPUS LIKE SYNDROME; MACULOPAPULAR RASH; MALAISE; PHARMACOGENETICS; POLYMERASE CHAIN REACTION; PREDICTIVE VALUE; RASH; SEROTYPE; SIDE EFFECT; SKIN MANIFESTATION; STEVENS JOHNSON SYNDROME; TOXIC EPIDERMAL NECROLYSIS; TOXIC HEPATITIS; VIRUS REACTIVATION;

ALLELES; BIOMARKERS, PHARMACOLOGICAL; DRUG HYPERSENSITIVITY; DRUG TOXICITY; EPIDERMAL NECROLYSIS, TOXIC; HLA ANTIGENS; HUMANS; PHARMACOGENETICS; STEVENS-JOHNSON SYNDROME;

EID: 84865516911     PISSN: 14622416     EISSN: 17448042     Source Type: Journal    
DOI: 10.2217/pgs.12.108     Document Type: Article

References (176)

1. Eshki M, Allanore L, Musette P et al. Twelve-year analysis of severe cases of drug reaction with eosinophilia and systemic symptoms: a cause of unpredictable multiorgan failure. Arch. Dermatol. 145, 67-72 (2009).
2. Kano Y, Shiohara T. The variable clinical picture of drug-induced hypersensitivity syndrome/drug rash with eosinophilia and systemic symptoms in relation to the eliciting drug. Immunol. Allergy Clin. North Am. 29, 481-501 (2009).
3. Shiohara T, Inaoka M, Kano Y. Drug-induced hypersensitivity syndrome (DIHS): a reaction induced by a complex interplay among herpesviruses and antiviral and antidrug immune responses. Allergol. Int. 55, 1-8 (2006).
4. Tohyama M, Hashimoto K, Yasukawa M et al. Association of human herpesvirus 6 reactivation with the flaring and severity of drug-induced hypersensitivity syndrome. Br. J. Dermatol. 157, 934-940 (2007). (Pubitemid 47583515)
5. Andrews E, Daly AK. Flucloxacillin-induced liver injury. Toxicology 254, 158-163 (2008).
6. Daly AK, Day CP. Genetic association studies in drug-induced liver injury. Semin. Liver Dis. 29, 400-411 (2009).
7. Daly AK, Day CP. Genetic association studies in drug-induced liver injury. Drug Metab. Rev. 44, 116-126 (2012).
8. Pirmohamed M, Aithal GP, Behr E, Daly A, Roden D. The phenotype standardization project: improving pharmacogenetic studies of serious adverse drug reactions. Clin. Pharmacol. Ther. 89, 784-785 (2011).
9. Castrejon JL, Lavergne SN, El-Sheikh A et al. Metabolic and chemical origins of cross-reactive immunological reactions to arylamine benzenesulfonamides. T-cell responses to hydroxylamine and nitroso derivatives. Chem. Res. Toxicol. 23, 184-192 (2010).
10. Naisbitt DJ, Britschgi M, Wong G et al. Hypersensitivity reactions to carbamazepine. characterization of the specificity, phenotype, and cytokine profile of drug-specific T cell clones. Mol. Pharmacol. 63, 732-741 (2003). (Pubitemid 36297347)
11. Naisbitt DJ, Farrell J, Wong G et al. Characterization of drug-specific T cells in lamotrigine hypersensitivity. J. Allergy Clin. Immunol. 111, 1393-1403 (2003). (Pubitemid 36683697)
12. Wu Y, Sanderson JP, Farrell J et al. Activation of T cells by carbamazepine and carbamazepine metabolites. J. Allergy Clin. Immunol. 118, 233-241 (2006). (Pubitemid 43964854)
13. Chessman D, Kostenko L, Lethborg T et al. Human leukocyte antigen Class I-restricted activation of CD8+ T cells provides the immunogenetic basis of a systemic drug hypersensitivity. Immunity 28, 822-832 (2008). (Pubitemid 351784513)
14. Martin AM, Almeida CA, Cameron P et al. Immune responses to abacavir in antigen-presenting cells from hypersensitive patients. AIDS 21, 1233-1244 (2007). (Pubitemid 46883477)
15. Padovan E, Mauri-Hellweg D, Pichler WJ, Weltzien HU. T cell recognition of penicillin G: structural features determining antigenic specificity. Eur. J. Immunol. 26, 42-48 (1996). (Pubitemid 26028410)
16. Naisbitt DJ, Gordon SF, Pirmohamed M et al. Antigenicity and immunogenicity of sulphamethoxazole: demonstration of metabolism-dependent haptenation and T-cell proliferation in vivo. Br. J. Pharmacol. 133, 295-305 (2001). (Pubitemid 32507049)
17. Pichler W, Yawalkar N, Schmid S, Helbling A. Pathogenesis of drug-induced exanthems. Allergy 57, 884-893 (2002).
18. Schnyder B, Mauri-Hellweg D, Zanni M, Bettens F, Pichler WJ. Direct, MHC-dependent presentation of the drug sulfamethoxazole to human alphabeta T cell clones. J. Clin. Invest. 100, 136-141 (1997). (Pubitemid 27311251)
19. Sieben S, Kawakubo Y, Al Masaoudi T, Merk HF, Blomeke B. Delayed-type hypersensitivity reaction to paraphenylenediamine is mediated by 2 different pathways of antigen recognition by specific alphabeta human T-cell clones. J. Allergy Clin. Immunol. 109, 1005-1011 (2002). (Pubitemid 34634313)
20. Zanni MP, von Greyerz S, Schnyder B, Wendland T, Pichler WJ. Allele-unrestricted presentation of lidocaine by HLA-DR molecules to specific alphabeta+ T cell clones. Int. Immunol. 10, 507-515 (1998). (Pubitemid 28182108)
21. Wei CY, Chung WH, Huang HW, Chen YT, Hung SI. Direct interaction between HLA-B and carbamazepine activates T cells in patients with Stevens-Johnson syndrome. J. Allergy Clin. Immunol. 129(6), 1562-1569. e5 (2012).
22. Yang CW, Hung SI, Juo CG et al. HLA-B*1502-bound peptides: implications for the pathogenesis of carbamazepine-induced Stevens-Johnson syndrome. J. Allergy Clin. Immunol. 120, 870-877 (2007).
23. Bharadwaj M, Illing P, Theodossis A et al. Drug hypersensitivity and human leukocyte antigens of the major histocompatibility complex. Annu. Rev. Pharmacol. Toxicol. 52, 401-431 (2012).
24. Illing PT, Vivian JP, Dudek NL et al. Immune self-reactivity triggered by drug-modified HLA-peptide repertoire. Nature 486(7404), 554-548 (2012).
25. Norcross MA, Luo S, Lu L et al. Abacavir induces loading of novel self-peptides into HLA-B*57.01: an autoimmune model for HLA-associated drug hypersensitivity. AIDS 26(11), F21-F29 (2012).
26. Ostrov DA, Grant BJ, Pompeu YA et al. Drug hypersensitivity caused by alteration of the MHC-presented self-peptide repertoire. Proc. Natl Acad. Sci. USA 109(25), 9959-9964 (2012).
27. Cutrell AG, Hernandez JE, Fleming JW et al. Updated clinical risk factor analysis of suspected hypersensitivity reactions to abacavir. Ann. Pharmacother. 38, 2171-2172 (2004). (Pubitemid 40169396)
28. Shapiro M, Ward KM, Stern JJ. A near-fatal hypersensitivity reaction to abacavir: case report and literature review. AIDS Read. 11, 222-226 (2001). (Pubitemid 32332270)
29. Symonds W, Cutrell A, Edwards M et al. Risk factor analysis of hypersensitivity reactions to abacavir. Clin. Ther. 24, 565-573 (2002). (Pubitemid 34492878)
30. Hetherington S, Hughes AR, Mosteller M et al. Genetic variations in HLA-B region and hypersensitivity reactions to abacavir. Lancet 359, 1121-1122 (2002). (Pubitemid 34270738)
31. Mallal S, Nolan D, Witt C et al. Association between presence of HLA-B*5701, HLA-DR7, and HLA-DQ3 and hypersensitivity to HIV-1 reverse-transcriptase inhibitor abacavir. Lancet 359, 727-732 (2002). (Pubitemid 34215071)
32. Hughes AR, Mosteller M, Bansal AT et al. Association of genetic variations in HLA-B region with hypersensitivity to abacavir in some, but not all, populations. Pharmacogenomics 5, 203-211 (2004). (Pubitemid 38351278)
33. Cao K, Hollenbach J, Shi X et al. Analysis of the frequencies of HLA-A, B, and C alleles and haplotypes in the five major ethnic groups of the United States reveals high levels of diversity in these loci and contrasting distribution patterns in these populations. Hum. Immunol. 62, 1009-1030 (2001). (Pubitemid 32835065)
34. Mallal S, Phillips E, Carosi G et al. HLA-B*5701 screening for hypersensitivity to abacavir. N. Engl. J. Med. 358, 568-579 (2008).
35. Phillips EJ, Arribas J, Fitch N, Givens N. Characteristics of abacavir hypersensitivity diagnoses according to HLA-B*5701 status and subsequent abacavir patch test result. Presented at: 11th European AIDS Conference. Madrid, Spain, October 24-27 2007 (P9.7/04).
36. Saag M, Balu R, Phillips E et al. High sensitivity of human leukocyte antigen-b*5701 as a marker for immunologically confirmed abacavir hypersensitivity in white and black patients. Clin. Infect. Dis. 46, 1111-1118 (2008). (Pubitemid 351589880)
37. Hammond E, Almeida CA, Mamotte C et al. External quality assessment of HLA-B*5701 reporting: an international multicentre survey. Antivir. Ther. 12, 1027-1032 (2007). (Pubitemid 350114982)
38. Hughes DA, Vilar FJ, Ward CC et al. Cost-effectiveness analysis of HLA B*5701 genotyping in preventing abacavir hypersensitivity. Pharmacogenetics 14, 335-342 (2004). (Pubitemid 38813687)
39. Schackman BR, Scott CA, Walensky RP et al. The cost-effectiveness of HLA-B*5701 genetic screening to guide initial antiretroviral therapy for HIV. AIDS 22, 2025-2033 (2008).
40. Phillips EJ, Sullivan JR, Knowles SR, Shear NH. Utility of patch testing in patients with hypersensitivity syndromes associated with abacavir. AIDS 16, 2223-2225 (2002). (Pubitemid 35387279)
41. Almeida CA, Martin AM, Nolan D et al. Cytokine profiling in abacavir hypersensitivity patients. Antivir. Ther. 13, 281-288 (2008). (Pubitemid 351535379)
42. Gomez P, Montserrat V, Marcilla M, Paradela A, de Castro JA. B*2707 differs in peptide specificity from B*2705 and B*2704 as much as from HLA-B27 subtypes not associated to spondyloarthritis. Eur. J. Immunol. 36, 1867-1881 (2006). (Pubitemid 44089053)
43. Zernich D, Purcell AW, Macdonald WA et al. Natural HLA Class I polymorphism controls the pathway of antigen presentation and susceptibility to viral evasion. J. Exp. Med. 200, 13-24 (2004). (Pubitemid 38924724)
44. Adam J, Eriksson KK, Schnyder B et al. Avidity determines T-cell reactivity in abacavir hypersensitivity. Eur. J. Immunol. 42(7), 1706-1716 (2012).
45. Knowles SR, Shapiro LE, Shear NH. Anticonvulsant hypersensitivity syndrome: incidence, prevention and management. Drug Saf. 21, 489-501 (1999). (Pubitemid 30021105)
46. Chung WH, Hung SI, Hong HS et al. Medical genetics: a marker for Stevens-Johnson syndrome. Nature 428, 486 (2004).
47. Hung SI, Chung WH, Jee SH et al. Genetic susceptibility to carbamazepine-induced cutaneous adverse drug reactions. Pharmacogenet. Genomics 16, 297-306 (2006).
48. Man CB, Kwan P, Baum L et al. Association between HLA-B*1502 allele and antiepileptic drug-induced cutaneous reactions in Han Chinese. Epilepsia 48, 1015-1018 (2007). (Pubitemid 46763406)
49. Wang Q, Zhou JQ, Zhou LM et al. Association between HLA-B*1502 allele and carbamazepine-induced severe cutaneous adverse reactions in Han people of southern China mainland. Seizure 20, 446-448 (2011).
50. Wu XT, Hu FY, An DM et al. Association between carbamazepine-induced cutaneous adverse drug reactions and the HLA-B*1502 allele among patients in central China. Epilepsy Behav. 19, 405-408 (2010).
51. Zhang Y, Wang J, Zhao LM et al. Strong association between HLA-B*1502 and carbamazepine-induced Stevens-Johnson syndrome and toxic epidermal necrolysis in mainland Han Chinese patients. Eur. J. Clin. Pharmacol. 67, 885-887 (2011).
52. Kulkantrakorn K, Tassaneeyakul W, Tiamkao S et al. HLA-B*1502 strongly predicts carbamazepine-induced Stevens-Johnson syndrome and toxic epidermal necrolysis in Thai patients with neuropathic pain. Pain Pract. 12(3), 202-208 (2011).
53. Mehta TY, Prajapati LM, Mittal B et al. Association of HLA-B*1502 allele and carbamazepine-induced Stevens-Johnson syndrome among Indians. Indian J. Dermatol. Venereol. Leprol. 75, 579-582 (2009).
54. Tassaneeyakul W, Tiamkao S, Jantararoungtong T et al. Association between HLA-B*1502 and carbamazepine-induced severe cutaneous adverse drug reactions in a Thai population. Epilepsia 51, 926-930 (2010).
55. Then SM, Rani ZZ, Raymond AA, Ratnaningrum S, Jamal R. Frequency of the HLA-B*1502 allele contributing to carbamazepine-induced hypersensitivity reactions in a cohort of Malaysian epilepsy patients. Asian Pac. J. Allergy Immunol. 29, 290-293 (2011).
56. Lonjou C, Thomas L, Borot N et al. A marker for Stevens-Johnson syndrome .: ethnicity matters. Pharmacogenomics J. 6, 265-268 (2006). (Pubitemid 44137953)
57. Ferrell PB Jr, McLeod HL. Carbamazepine, HLA-B*1502 and risk of Stevens-Johnson syndrome and toxic epidermal necrolysis: US FDA recommendations. Pharmacogenomics 9, 1543-1546 (2008).
58. Niihara H, Kakamu T, Fujita Y, Kaneko S, Morita E. HLA-A31 strongly associates with carbamazepine-induced adverse drug reactions but not with carbamazepine-induced lymphocyte proliferation in a Japanese population. J. Dermatol. 39(7), 594-601 (2011).
59. McCormack M, Alfirevic A, Bourgeois S et al. HLA-A*3101 and carbamazepine-induced hypersensitivity reactions in Europeans. N. Engl. J. Med. 364, 1134-1143 (2011).
60. Ozeki T, Mushiroda T, Yowang A et al. Genome-wide association study identifies HLA-A*3101 allele as a genetic risk factor for carbamazepine-induced cutaneous adverse drug reactions in Japanese population. Hum. Mol. Genet. 20, 1034-1041 (2011).
61. Kim SH, Lee KW, Song WJ et al. Carbamazepine-induced severe cutaneous adverse reactions and HLA genotypes in Koreans. Epilepsy Res. 97, 190-197 (2011).
62. Chen YC, Chu CY, Hsiao CH. Oxcarbazepine-induced Stevens-Johnson syndrome in a patient with HLA-B*1502 genotype. J. Eur. Acad. Dermatol. Venereol. 23, 702-703 (2009).
63. Hu FY, Wu XT, An DM et al. Phenytoin-induced Stevens-Johnson syndrome with negative HLA-B*1502 allele in mainland China: two cases. Seizure 20, 431-432 (2011).
64. Hung SI, Chung WH, Liu ZS et al. Common risk allele in aromatic antiepileptic-drug induced Stevens-Johnson syndrome and toxic epidermal necrolysis in Han Chinese. Pharmacogenomics 11, 349-356 (2010).
65. Lin LC, Lai PC, Yang SF, Yang RC. Oxcarbazepine-induced Stevens-Johnson syndrome: a case report. Kaohsiung J. Med. Sci. 25, 82-86 (2009).
66. An DM, Wu XT, Hu FY et al. Association study of lamotrigine-induced cutaneous adverse reactions and HLA-B*1502 in a Han Chinese population. Epilepsy Res. 92, 226-230 (2010).
67. Shi YW, Min FL, Liu XR et al. Hla-B alleles and lamotrigine-induced cutaneous adverse drug reactions in the Han Chinese population. Basic Clin. Pharmacol. Toxicol. 109, 42-46 (2011).
68. McCormack M, Urban TJ, Shianna KV et al. Genome-wide mapping for clinically relevant predictors of lamotrigine-and phenytoin-induced hypersensitivity reactions. Pharmacogenomics 13, 399-405 (2012).
69. Kazeem GR, Cox C, Aponte J et al. High-resolution HLA genotyping and severe cutaneous adverse reactions in lamotrigine-treated patients. Pharmacogenet. Genomics 19, 661-665 (2009).
70. Chow JC, Huang CW, Fang CW, Wu YJ, Tsai JJ. Lamotrigine-induced hypersensitivity syndrome in a Han Chinese patient with the HLA-B*5801 genotype. Neurol. Sci. doi:10.1007/s10072-012-0947-7 (2012) (Epub ahead of print).
71. Kaniwa N, Saito Y, Aihara M et al. HLA-B*1511 is a risk factor for carbamazepine-induced Stevens-Johnson syndrome and toxic epidermal necrolysis in Japanese patients. Epilepsia 51, 2461-2465 (2010).
72. Ikeda H, Takahashi Y, Yamazaki E et al. HLA Class I markers in Japanese patients with carbamazepine-induced cutaneous adverse reactions. Epilepsia 51, 297-300 (2010).
73. Ko TM, Chung WH, Wei CY et al. Shared and restricted T-cell receptor use is crucial for carbamazepine-induced Stevens-Johnson syndrome. J. Allergy Clin. Immunol. 128, 1266-1276.e11 (2011).
74. Pichler WJ, Naisbitt DJ, Park BK. Immune pathomechanism of drug hypersensitivity reactions. J. Allergy Clin. Immunol. 127, S74-S81 (2011).
75. Pollard RB, Robinson P, Dransfield K. Safety profile of nevirapine, a nonnucleoside reverse transcriptase inhibitor for the treatment of human immunodeficiency virus infection. Clin. Ther. 20, 1071-1092 (1998). (Pubitemid 29058411)
76. Gangar M, Arias G, O'Brien JG, Kemper CA. Frequency of cutaneous reactions on rechallenge with nevirapine and delavirdine. Ann. Pharmacother. 34, 839-842 (2000). (Pubitemid 30471262)
77. Taiwo BO. Nevirapine toxicity. Int. J. STD AIDS 17, 364-369; quiz 70 (2006).
78. Bersoff-Matcha SJ, Miller WC, Aberg JA et al. Sex differences in nevirapine rash. Clin. Infect. Dis. 32, 124-129 (2001). (Pubitemid 32150957)
79. Bonjoch A, Paredes R, Domingo P et al. Long-term safety and efficacy of nevirapine-based approaches in HIV type 1-infected patients. AIDS Res. Hum. Retroviruses 22, 321-329 (2006).
80. Gonzalez de Requena D, Nunez M, Jimenez-Nacher I, Soriano V. Liver toxicity caused by nevirapine. AIDS 16, 290-291 (2002). (Pubitemid 34118577)
81. Manfredi R, Calza L. Safety issues about nevirapine administration in HIV-infected pregnant women. J. Acquir. Immune. Defic. Syndr. 45, 365-368 (2007). (Pubitemid 47012390)
82. Peters PJ, Stringer J, McConnell MS et al. Nevirapine-associated hepatotoxicity was not predicted by CD4 count ≥250 cells/μl among women in Zambia, Thailand and Kenya. HIV Med. 11, 650-660 (2010).
83. Torti C, Costarelli S, De Silvestri A et al. Analysis of severe hepatic events associated with nevirapine-containing regimens. CD4+ T-cell count and gender in hepatitis C seropositive and seronegative patients. Drug Saf. 30, 1161-1169 (2007). (Pubitemid 350172857)
84. Martin AM, Nolan D, James I et al. Predisposition to nevirapine hypersensitivity associated with HLA-DRB1*0101 and abrogated by low CD4 T-cell counts. AIDS 19, 97-99 (2005). (Pubitemid 40111026)
85. Vitezica ZG, Milpied B, Lonjou C et al. HLA-DRB1*01 associated with cutaneous hypersensitivity induced by nevirapine and efavirenz. AIDS 22, 540-541 (2008). (Pubitemid 351317299)
86. Yuan J, Guo S, Hall D et al. Toxicogenomics of nevirapine-associated cutaneous and hepatic adverse events among populations of African, Asian, and European descent. AIDS 25(10), 1271-1280 (2011).
87. Littera R, Carcassi C, Masala A et al. HLA-dependent hypersensitivity to nevirapine in Sardinian HIV patients. AIDS 20, 1621-1626 (2006). (Pubitemid 44162404)
88. Gatanaga H, Yazaki H, Tanuma J et al. HLA-Cw8 primarily associated with hypersensitivity to nevirapine. AIDS 21, 264-265 (2007). (Pubitemid 46036947)
89. Gao S, Gui XE, Liang K et al. HLA-Dependent hypersensitivity reaction to nevirapine in Chinese Han HIV-infected patients. AIDS Res. Hum. Retroviruses 28(6), 540-543 (2011).
90. Chantarangsu S, Mushiroda T, Mahasirimongkol S et al. HLA-B*3505 allele is a strong predictor for nevirapine-induced skin adverse drug reactions in HIV-infected Thai patients. Pharmacogenet. Genomics 19, 139-146 (2009).
91. Chantarangsu S, Mushiroda T, Mahasirimongkol S et al. Genome-wide association study identifies variations in 6p21.3 associated with nevirapine-induced rash. Clin. Infect. Dis. 53, 341-348 (2011).
92. Likanonsakul S, Rattanatham T, Feangvad S et al. HLA-Cw*04 allele associated with nevirapine-induced rash in HIV-infected Thai patients. AIDS Res. Ther. 6, 22 (2009).
93. Phillips E, Keane N, Blyth C et al. Both HLA Class I restricted CD8+ and Class II Restricted CD4+ T cells are implicated in the pathogenesis of nevirapine hypersensitivity. Presented at: 51st ICAAC, Chicago, IL, USA, 17-20 September 2011 (H1-1399c).
94. Tiala I, Wakkinen J, Suomela S et al. The PSORS1 locus gene CCHCR1 affects keratinocyte proliferation in transgenic mice. Hum. Mol. Genet. 17, 1043-1051 (2008). (Pubitemid 351426038)
95. Tiala I, Suomela S, Huuhtanen J et al. The CCHCR1 (HCR) gene is relevant for skin steroidogenesis and downregulated in cultured psoriatic keratinocytes. J. Mol. Med. (Berl.) 85, 589-601 (2007). (Pubitemid 46870890)
96. Mahungu T, Smith C, Turner F et al. Cytochrome P450 2B6 516G-T is associated with plasma concentrations of nevirapine at both 200 mg twice daily and 400 mg once daily in an ethnically diverse population. HIV Med. 10, 310-317 (2009).
97. Chan SH, Tan T. HLA and allopurinol drug eruption. Dermatologica 179, 32-33 (1989). (Pubitemid 19172335)
98. Hung SI, Chung WH, Liou LB et al. HLA-B*5801 allele as a genetic marker for severe cutaneous adverse reactions caused by allopurinol. Proc. Natl Acad. Sci. USA 102, 4134-4139 (2005).
99. Dainichi T, Uchi H, Moroi Y, Furue M. Stevens-Johnson syndrome, drug-induced hypersensitivity syndrome and toxic epidermal necrolysis caused by allopurinol in patients with a common HLA allele: what causes the diversity? Dermatology 215, 86-88 (2007). (Pubitemid 46976024)
100. Kaniwa N, Saito Y, Aihara M et al. HLA-B locus in Japanese patients with anti-epileptics and allopurinol-related Stevens-Johnson syndrome and toxic epidermal necrolysis. Pharmacogenomics 9, 1617-1622 (2008).
101. Tassaneeyakul W, Jantararoungtong T, Chen P et al. Strong association between HLA-B*5801 and allopurinol-induced Stevens-Johnson syndrome and toxic epidermal necrolysis in a Thai population. Pharmacogenet. Genomics 19, 704-709 (2009).
102. Jung JW, Song WJ, Kim YS et al. HLA-B58 can help the clinical decision on starting allopurinol in patients with chronic renal insufficiency. Nephrol. Dial. Transplant. 26, 3567-3572 (2011).
103. Kang HR, Jee YK, Kim YS et al. Positive and negative associations of HLA Class I alleles with allopurinol-induced SCARs in Koreans. Pharmacogenet. Genomics 21, 303-307 (2011).
104. Lonjou C, Borot N, Sekula P et al. A European study of HLA-B in Stevens-Johnson syndrome and toxic epidermal necrolysis related to five high-risk drugs. Pharmacogenet. Genomics 18, 99-107 (2008).
105. Lee MH, Stocker SL, Anderson J et al. Initiating allopurinol therapy: do we need to know the patient's HLA status? Intern. Med. J. 42(4), 411-416 (2011).
106. Genin E, Schumacher M, Roujeau JC et al. Genome-wide association study of Stevens-Johnson syndrome and toxic epidermal necrolysis in Europe. Orphanet. J. Rare Dis. 6, 52 (2011).
107. Tohkin M, Kaniwa N, Saito Y et al. A whole-genome association study of major determinants for allopurinol-related Stevens-Johnson syndrome and toxic epidermal necrolysis in Japanese patients. Pharmacogenomics J. doi:10.1038/tpj.2011.41 (2011) (Epub ahead of print).
108. Gandhi G, Buttar BS, Albert L, Hasan Q, Aggarwal RK. Psoriasis-associated genetic polymorphism in North Indian population in the CCHCR1 gene and in a genomic segment flanking the HLA-C region. Dis. Markers 31, 361-370 (2011).
109. Quinones-Lombrana A, Lopez-Soto A, Ballina-Garcia FJ et al. BAT1 promoter polymorphism is associated with rheumatoid arthritis susceptibility. J. Rheumatol. 35, 741-744 (2008). (Pubitemid 351747110)
110. Shibue T, Tsuchiya N, Komata T et al. Tumor necrosis factor alpha 5́-flanking region, tumor necrosis factor receptor II, and HLA-DRB1 polymorphisms in Japanese patients with rheumatoid arthritis. Arthritis Rheum. 43, 753-757 (2000).
111. Colombo S, Rauch A, Rotger M et al. The HCP5 single-nucleotide polymorphism. a simple screening tool for prediction of hypersensitivity reaction to abacavir. J. Infect. Dis. 198, 864-867 (2008).
112. Fellay J, Shianna KV, Ge D et al. A whole-genome association study of major determinants for host control of HIV-1. Science 317, 944-947 (2007). (Pubitemid 47301321)
113. Galvan CA, Elbarcha OC, Fernandez EJ, Beltramo DM, Soria NW. Rapid HCP5 single-nucleotide polymorphism genotyping: a simple allele-specific PCR method for prediction of hypersensitivity reaction to abacavir. Clin. Chim. Acta 412, 1382-1384 (2011).
114. Migueles SA, Rood JE, Berkley AM et al. Trivalent adenovirus type 5 HIV recombinant vaccine primes for modest cytotoxic capacity that is greatest in humans with protective HLA Class I alleles. PLoS Pathog. 7, e1002002 (2011).
115. Somkrua R, Eickman EE, Saokaew S, Lohitnavy M, Chaiyakunapruk N. Association of HLA-B*5801 allele and allopurinol-induced Stevens Johnson syndrome and toxic epidermal necrolysis: a systematic review and meta-analysis. BMC Med. Genet. 12, 118 (2011).
116. Nolan D. HLA-B*5701 screening prior to abacavir prescription: clinical and laboratory aspects. Crit. Rev. Clin. Lab. Sci. 46, 153-165 (2009).
117. Phillips EJ, Mallal SA. Pharmacogenetics of drug hypersensitivity. Pharmacogenomics 11, 973-987 (2010).
118. Park WB, Choe PG, Song KH et al. Should HLA-B*5701 screening be performed in every ethnic group before starting abacavir? Clin. Infect. Dis. 48, 365-367 (2009).
119. Sun HY, Hung CC, Lin PH et al. Incidence of abacavir hypersensitivity and its relationship with HLA-B*5701 in HIV-infected patients in Taiwan. J. Antimicrob. Chemother. 60, 599-604 (2007).
120. Martin MA, Klein TE, Dong BJ et al. Clinical pharmacogenetics implementation consortium guidelines for HLA-B genotype and abacavir dosing. Clin. Pharmacol. Ther. 91, 734-738 (2012).
121. Berka N, Gill JM, Liacini A, O'Bryan T, Khan FM. Human leukocyte antigen (HLA) and pharmacogenetics: screening for HLA-B*57:01 among human immunodeficiency virus-positive patients from southern Alberta. Hum. Immunol. 73, 164-167 (2012).
122. Parczewski M, Leszczyszyn-Pynka M, Wnuk A et al. Introduction of pharmacogenetic screening for the human leucocyte antigen (HLA) B*5701 variant in Polish HIV-infected patients. HIV Med. 11, 345-348 (2010).
123. Rauch A, Nolan D, Thurnheer C et al. Refining abacavir hypersensitivity diagnoses using a structured clinical assessment and genetic testing in the Swiss HIV Cohort Study. Antivir. Ther. 13, 1019-1028 (2008).
124. Wolf E, Blankenburg M, Bogner JR et al. Cost impact of prospective HLA-B*5701-screening prior to abacavir/lamivudine fixed dose combination use in Germany. Eur. J. Med. Res. 15, 145-151 (2010).
125. Zucman D, Truchis P, Majerholc C, Stegman S, Caillat-Zucman S. Prospective screening for human leukocyte antigen-B*5701 avoids abacavir hypersensitivity reaction in the ethnically mixed French HIV population. J. Acquir. Immune. Defic. Syndr. 45, 1-3 (2007). (Pubitemid 46684436)
126. Young B, Squires K, Patel P et al. First large, multicenter, open-label study utilizing HLA-B*5701 screening for abacavir hypersensitivity in North America. AIDS 22, 1673-1675 (2008).
127. Locharernkul C, Shotelersuk V, Hirankarn N. Pharmacogenetic screening of carbamazepine-induced severe cutaneous allergic reactions. J. Clin. Neurosci. 18, 1289-1294 (2011).
128. Chen P, Lin JJ, Lu CS et al. Carbamazepine-induced toxic effects and HLA-B*1502 screening in Taiwan. N. Engl. J. Med. 364, 1126-1133 (2011).
129. Phillips EJ, Mallal SA. HLA-B*1502 screening and toxic effects of carbamazepine. N. Engl. J. Med. 365, 672; author reply 3 (2011).
130. Airo P, Scarsi M, Malagoli A et al. The convenience of flow cytometry for HLA-B*5701 screening to prevent abacavir hypersensitivity reactions. J. Acquir. Immune Defic. Syndr. 51, 361-362 (2009).
131. Hammond E, Mamotte C, Nolan D, Mallal S. HLA-B*5701 typing: evaluation of an allele-specific polymerase chain reaction melting assay. Tissue Antigens 70, 58-61 (2007). (Pubitemid 46890273)
132. Kostenko L, Kjer-Nielsen L, Nicholson I et al. Rapid screening for the detection of HLA-B57 and HLA-B58 in prevention of drug hypersensitivity. Tissue Antigens 78, 11-20 (2011).
133. Martin AM, Nolan D, Mallal S. HLA-B*5701 typing by sequence-specific amplification: validation and comparison with sequence-based typing. Tissue Antigens 65, 571-574 (2005). (Pubitemid 40776308)
134. Rodríguez-Nóvoa S, Cuenca L, Morello J et al. Use of the HCP5 single nucleotide polymorphism to predict hypersensitivity reactions to abacavir: correlation with HLA-B*5701. J. Antimicrob. Chemother. 65, 1567-1569 (2010).
135. Sanchez-Giron F, Villegas-Torres B, Jaramillo-Villafuerte K et al. Association of the genetic marker for abacavir hypersensitivity HLA-B*5701 with HCP5 rs2395029 in Mexican Mestizos. Pharmacogenomics 12, 809-814 (2011).
136. Badulli C, Sestini R, Sbarsi I et al. Tag SNPs of the ancestral haplotype 57.1 do not substitute HLA-B*57.01 typing for eligibility to abacavir treatment in the Italian population. Pharmacogenomics 13, 247-249 (2012).
137. Maekawa K, Nishikawa J, Kaniwa N et al. Development of a rapid and inexpensive assay for detecting a surrogate genetic polymorphism of HLA-B*58.01: a partially predictive but useful biomarker for allopurinol-related Stevens-Johnson syndrome/toxic epidermal necrolysis in Japanese. Drug Metab. Pharmacokinet. doi:http://dx.doi.org/10.2133/dmpk. DMPK-11-NT-120 (2012) (Epub ahead of print).
138. Shear NH, Milpied B, Bruynzeel DP, Phillips EJ. A review of drug patch testing and implications for HIV clinicians. AIDS 22, 999-1007 (2008). (Pubitemid 351769738)
139. Cristallo AF, Schroeder J, Citterio A et al. A study of HLA Class I and Class II 4-digit allele level in Stevens-Johnson syndrome and toxic epidermal necrolysis. Int. J. Immunogenet. 38, 303-309 (2011).
140. Locharernkul C, Loplumlert J, Limotai C et al. Carbamazepine and phenytoin induced Stevens-Johnson syndrome is associated with HLA-B*1502 allele in Thai population. Epilepsia 49, 2087-2091 (2008).
141. Chang CC, Too CL, Murad S, Hussein SH. Association of HLA-B*1502 allele with carbamazepine-induced toxic epidermal necrolysis and Stevens-Johnson syndrome in the multi-ethnic Malaysian population. Int. J. Dermatol. 50, 221-224 (2011).
142. Kim SH, Kim M, Lee KW et al. HLA-B*5901 is strongly associated with methazolamide-induced Stevens-Johnson syndrome/toxic epidermal necrolysis. Pharmacogenomics 11, 879-884 (2010).
143. Roujeau JC, Huynh TN, Bracq C et al. Genetic susceptibility to toxic epidermal necrolysis. Arch. Dermatol. 123, 1171-1173 (1987). (Pubitemid 17119310)
144. Chiu L, Hu M, Ng M et al. Association between HLA-B*58.01 allele and severe cutaneous adverse reactions with allopurinol in Han Chinese in Hong Kong. Br. J. Dermatol. 167(1), 44-49 (2012).
145. Phillips EJ, Sanne I, Lederman M et al. Associations between HLA-DRBA*0102, HLA-B*5801 and hepatotoxicity in patients who initiated nevirapine containing regimens in South Africa. Presented at: 18th Conference on Retroviruses and Opportunistic Infections. MA, USA 27 February-1 March 2011 (Paper #949).
146. Alfirevic A, Jorgensen AL, Williamson PR et al. HLA-B locus in Caucasian patients with carbamazepine hypersensitivity. Pharmacogenomics 7, 813-818 (2006). (Pubitemid 44446732)
147. Romano A, De Santis A, Romito A et al. Delayed hypersensitivity to aminopenicillins is related to major histocompatibility complex genes. Ann. Allergy Asthma Immunol. 80, 433-437 (1998). (Pubitemid 28246777)
148. Hautekeete ML, Horsmans Y, Van Waeyenberge C et al. HLA association of amoxicillin-clavulanate-induced hepatitis. Gastroenterology 117, 1181-1186 (1999). (Pubitemid 29512678)
149. Lucena MI, Molokhia M, Shen Y et al. Susceptibility to amoxicillin-clavulanate-induced liver injury is influenced by multiple HLA Class I and II alleles. Gastroenterology 141, 338-347 (2011).
150. O'Donohue J, Oien KA, Donaldson P et al. Co-amoxiclav jaundice. clinical and histological features and HLA Class II association. Gut 47, 717-720 (2000).
151. Singer JB, Lewitzky S, Leroy E et al. A genome-wide study identifies HLA alleles associated with lumiracoxib-related liver injury. Nat. Genet. 42, 711-714 (2010).
152. Kindmark A, Jawaid A, Harbron CG et al. Genome-wide pharmacogenetic investigation of a hepatic adverse event without clinical signs of immunopathology suggests an underlying immune pathogenesis. Pharmacogenomics J. 8, 186-195 (2008). (Pubitemid 351712643)
153. Daly AK, Aithal GP, Leathart JB et al. Genetic susceptibility to diclofenac-induced hepatotoxicity. contribution of UGT2B7, CYP2C8, and ABCC2 genotypes. Gastroenterology 132, 272-281 (2007). (Pubitemid 46108755)
154. Daly AK, Donaldson PT, Bhatnagar P et al. HLA-B*5701 genotype is a major determinant of drug-induced liver injury due to flucloxacillin. Nat. Genet. 41, 816-819 (2009).
155. Spraggs CF, Budde LR, Briley LP et al. HLA-DQA1*02.01 is a major risk factor for lapatinib-induced hepatotoxicity in women with advanced breast cancer. J. Clin. Oncol. 29, 667-673 (2011).
156. Pellicano R, Ciavarella G, Lomuto M, Di Giorgio G. Genetic susceptibility to fixed drug eruption: evidence for a link with HLA-B22. J. Am. Acad. Dermatol. 30, 52-54 (1994). (Pubitemid 24033819)
157. Pellicano R, Lomuto M, Ciavarella G, Di Giorgio G, Gasparini P. Fixed drug eruptions with feprazone are linked to HLA-B22. J. Am. Acad. Dermatol. 36, 782-784 (1997). (Pubitemid 27215370)
158. Ozkaya-Bayazit E, Akar U. Fixed drug eruption induced by trimethoprim-sulfamethoxazole: evidence for a link to HLA-A30 B13 Cw6 haplotype. J. Am. Acad. Dermatol. 45, 712-717 (2001). (Pubitemid 33032568)
159. Lieberman JA, Yunis J, Egea E et al. HLA-B38, DR4, DQw3 and clozapine-induced agranulocytosis in Jewish patients with schizophrenia. Arch. Gen. Psychiatry 47, 945-948 (1990). (Pubitemid 20348482)
160. Valevski A, Klein T, Gazit E et al. HLA-B38 and clozapine-induced agranulocytosis in Israeli Jewish schizophrenic patients. Eur. J. Immunogenet. 25, 11-13 (1998). (Pubitemid 28154401)
161. Athanasiou MC, Dettling M, Cascorbi I et al. Candidate gene analysis identifies a polymorphism in HLA-DQB1 associated with clozapine-induced agranulocytosis. J. Clin. Psychiatry 72, 458-463 (2011).
162. Dettling M, Cascorbi I, Opgen-Rhein C, Schaub R. Clozapine-induced agranulocytosis in schizophrenic Caucasians: confirming clues for associations with human leukocyte Class I and II antigens. Pharmacogenomics J. 7, 325-332 (2007). (Pubitemid 47471310)
163. Diez RA. HLA-B27 and agranulocytosis by levamisole. Immunol. Today 11, 270 (1990). (Pubitemid 20223320)
164. Batchelor JR, Welsh KI, Tinoco RM et al. Hydralazine-induced systemic lupus erythematosus: influence of HLA-DR and sex on susceptibility. Lancet 1, 1107-1109 (1980). (Pubitemid 10100366)
165. Vedove CD, Del Giglio M, Schena D, Girolomoni G. Drug-induced lupus erythematosus. Arch. Dermatol. Res. 301, 99-105 (2009).
166. Kim SH, Choi JH, Lee KW et al. The human leucocyte antigen- DRB1*1302-DQB1*0609-DPB1*0201 haplotype may be a strong genetic marker for aspirin-induced urticaria. Clin. Exp. Allergy 35, 339-344 (2005).
167. Kim SH, Hur GY, Choi JH, Park HS. Pharmacogenetics of aspirin-intolerant asthma. Pharmacogenomics 9, 85-91 (2008).
168. Rodriguez-Perez M, Gonzalez-Dominguez J, Mataran L, Garcia-Perez S, Salvatierra D. Association of HLA-DR5 with mucocutaneous lesions in patients with rheumatoid arthritis receiving gold sodium thiomalate. J. Rheumatol. 21, 41-43 (1994). (Pubitemid 24044915)
169. Speerstra F, Reekers P, van de Putte LB, Vandenbroucke JP. HLA associations in aurothioglucose-and d-penicillamine-induced haematotoxic reactions in rheumatoid arthritis. Tissue Antigens 26, 35-40 (1985). (Pubitemid 15059446)
170. Quiralte J, Sanchez-Garcia F, Torres MJ et al. Association of HLA-DR11 with the anaphylactoid reaction caused by nonsteroidal anti-inflammatory drugs. J. Allergy Clin. Immunol. 103, 685-689 (1999). (Pubitemid 29295578)
171. Garlepp MI, Dawkins RL, Christiansen FT. HLA antigens and acetylcholine receptor antibodies in penicillamine induced myasthenia gravis. Br. Med. J. 286, 1442-1443 (1983). (Pubitemid 13128645)
172. Pachoula-Papasteriades C, Boki K, Varla-Leftherioti M et al. HLA-A,-B, and-DR antigens in relation to gold and d-penicillamine toxicity in Greek patients with RA. Dis. Markers 4, 35-41 (1986). (Pubitemid 17201942)
173. Maier LA, McGrath DS, Sato H et al. Influence of MHC Class II in susceptibility to beryllium sensitization and chronic beryllium disease. J. Immunol. 171, 6910-6918 (2003). (Pubitemid 37532127)
174. Rosenman KD, Rossman M, Hertzberg V et al. HLA Class II DPB1 and DRB1 polymorphisms associated with genetic susceptibility to beryllium toxicity. Occup. Environ. Med. 68, 487-493 (2011).
175. Jonville-Bera AP, Crickx B, Aaron L, Hartingh I, Autret-Leca E. Strontium ranelate-induced DRESS syndrome: first two case reports. Allergy 64, 658-659 (2009).
176. Musette P, Brandi ML, Cacoub P et al. Treatment of osteoporosis. recognizing and managing cutaneous adverse reactions and drug-induced hypersensitivity. Osteoporos. Int. 21, 723-732 (2010).