The Role of Alleles in Susceptibility to Haloperidol-Induced Toxicity in Mice and Humans

1. Ohtsuki S, Terasaki T (2007) Contribution of carrier-mediated transport systems to the blood-brain barrier as a supporting and protecting interface for the brain; importance for CNS drug discovery and development. Pharm Res 24: 1745–1758. 17619998

2. Obermeier B, Daneman R, Ransohoff RM (2013) Development, maintenance and disruption of the blood-brain barrier. Nat Med 19: 1584–1596. doi: 10.1038/nm.3407 24309662

3. Beresford R, Ward A (1987) Haloperidol decanoate. A preliminary review of its pharmacodynamic and pharmacokinetic properties and therapeutic use in psychosis. Drugs 33: 31–49. 3545764

4. Parkes GE (1982) Haloperidol: profile of side effects. Johnson DAW, editor. Haloperidol decanoate and the treatment of chronic schizophrenia. New York: ADIS Press. pp. 58–63.

5. Soares-Weiser K, Fernandez HH (2007) Tardive dyskinesia. Semin Neurol 27: 159–169. 17390261

6. Crowley JJ, Kim Y, Szatkiewicz JP, Pratt AL, Quackenbush CR, et al. (2012) Genome-wide association mapping of loci for antipsychotic-induced extrapyramidal symptoms in mice. Mamm Genome 23: 322–335. doi: 10.1007/s00335-011-9385-8 22207321

7. Flint J, Valdar W, Shifman S, Mott R (2005) Strategies for mapping and cloning quantitative trait genes in rodents. Nat Rev Genet 6: 271–286. 15803197

8. Nadeau JH, Frankel WN (2000) The roads from phenotypic variation to gene discovery: mutagenesis versus QTLs. Nat Genet 25: 381–384. 10932178

9. Payseur BA, Place M (2007) Prospects for association mapping in classical inbred mouse strains. Genetics 175: 1999–2008. 17277361

10. Su WL, Sieberts SK, Kleinhanz RR, Lux K, Millstein J, et al. (2010) Assessing the prospects of genome-wide association studies performed in inbred mice. Mamm Genome 21: 143–152. doi: 10.1007/s00335-010-9249-7 20135320

11. Keane TM, Goodstadt L, Danecek P, White MA, Wong K, et al. (2011) Mouse genomic variation and its effect on phenotypes and gene regulation. Nature 477: 289–294. doi: 10.1038/nature10413 21921910

12. Zheng M, Dill D, Peltz G (2012) A better prognosis for genetic association studies in mice. Trends Genet 28: 62–69. doi: 10.1016/j.tig.2011.10.006 22118772

13. Lappalainen T, Sammeth M, Friedlander MR, t Hoen PA, Monlong J, et al. (2013) Transcriptome and genome sequencing uncovers functional variation in humans. Nature 501: 506–511. doi: 10.1038/nature12531 24037378

14. Liao G, Wang J, Guo J, Allard J, Cheng J, et al. (2004) In Silico Genetics: Identification of a Functional Element Regulating H2-Ea Gene Expression. Science 306: 690–695. 15499019

15. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754–1760. doi: 10.1093/bioinformatics/btp324 19451168

16. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, et al. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078–2079. doi: 10.1093/bioinformatics/btp352 19505943

17. Peltz G, Zaas AK, Zheng M, Solis NV, Zhang MX, et al. (2011) Next-generation computational genetic analysis: multiple complement alleles control survival after Candida Albicans infection. Infect Immun 79: 4472–4479. doi: 10.1128/IAI.05666-11 21875959

18. Wang J, Peltz G (2005) Haplotype-based computational genetic analysis in mice. computational genetics and genomics: new tools for understanding disease. Totowa (New Jersey): Humana Press Inc. pp. 51–70.

19. Hollander M, Wolfe DA (1973) Nonparametric statistical methods. New York: John Wiley & Sons. 4805339

20. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc B 57: 289–300.

21. Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG (2010) Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol 8: e1000412. doi: 10.1371/journal.pbio.1000412 20613859

22. Crowley JJ, Adkins DE, Pratt AL, Quackenbush CR, van den Oord EJ, et al. (2012) Antipsychotic-induced vacuous chewing movements and extrapyramidal side effects are highly heritable in mice. Pharmacogenomics J 12: 147–155. doi: 10.1038/tpj.2010.82 21079646

23. Eberlin LS, Ferreira CR, Dill AL, Ifa DR, Cheng L, et al. (2011) Nondestructive, histologically compatible tissue imaging by desorption electrospray ionization mass spectrometry. Chembiochem 12: 2129–2132. doi: 10.1002/cbic.201100411 21793152

24. Giegling I, Drago A, Schafer M, Hartmann AM, Sander T, et al. (2011) Lack of association between 71 variations located in candidate genes and response to acute haloperidol treatment. Psychopharmacology (Berl) 214: 719–728. doi: 10.1007/s00213-010-2080-8 21079921

25. Rohlfs RV, Weir BS (2008) Distributions of Hardy-Weinberg equilibrium test statistics. Genetics 180: 1609–1616. doi: 10.1534/genetics.108.088005 18791257

26. Kawanobe T, Kogure S, Nakamura S, Sato M, Katayama K, et al. (2012) Expression of human ABCB5 confers resistance to taxanes and anthracyclines. Biochem Biophys Res Commun 418: 736–741. doi: 10.1016/j.bbrc.2012.01.090 22306008

27. Frank NY, Margaryan A, Huang Y, Schatton T, Waaga-Gasser AM, et al. (2005) ABCB5-mediated doxorubicin transport and chemoresistance in human malignant melanoma. Cancer Res 65: 4320–4333. 15899824

28. Frank NY, Pendse SS, Lapchak PH, Margaryan A, Shlain D, et al. (2003) Regulation of progenitor cell fusion by ABCB5 P-glycoprotein, a novel human ATP-binding cassette transporter. J Biol Chem 278: 47156–47165. 12960149

29. Fukunaga-Kalabis M, Martinez G, Nguyen TK, Kim D, Santiago-Walker A, et al. (2010) Tenascin-C promotes melanoma progression by maintaining the ABCB5-positive side population. Oncogene 29: 6115–6124. doi: 10.1038/onc.2010.350 20729912

30. Wilson BJ, Schatton T, Zhan Q, Gasser M, Ma J, et al. (2011) ABCB5 identifies a therapy-refractory tumor cell population in colorectal cancer patients. Cancer Res 71: 5307–5316. doi: 10.1158/0008-5472.CAN-11-0221 21652540

31. Seeger MA, van Veen HW (2009) Molecular basis of multidrug transport by ABC transporters. Biochim Biophys Acta 1794: 725–737. doi: 10.1016/j.bbapap.2008.12.004 19135557

32. Nadeau JH, Singer JB, Matin A, Lander ES (2000) Analysing complex genetic traits with chromosome substitution strains. Nat Genet 24: 221–225. 10700173

33. Eyles DW, Avent KM, Stedman TJ, Pond SM (1997) Two pyridinium metabolites of haloperidol are present in the brain of patients at post-mortem. Life Sci 60: 529–534. 9042387

34. Igarashi K, Kasuya F, Fukui M, Usuki E, Castagnoli N Jr. (1995) Studies on the metabolism of haloperidol (HP): the role of CYP3A in the production of the neurotoxic pyridinium metabolite HPP+ found in rat brain following ip administration of HP. Life Sci 57: 2439–2446. 8847965

35. Bloomquist J, King E, Wright A, Mytilineou C, Kimura K, et al. (1994) 1-Methyl-4-phenylpyridinium-like neurotoxicity of a pyridinium metabolite derived from haloperidol: cell culture and neurotransmitter uptake studies. J Pharmacol Exp Ther 270: 822–830. 8071874

36. Rollema H, Skolnik M, D’Engelbronner J, Igarashi K, Usuki E, et al. (1994) MPP(+)-like neurotoxicity of a pyridinium metabolite derived from haloperidol: in vivo microdialysis and in vitro mitochondrial studies. J Pharmacol Exp Ther 268: 380–387. 8301579

37. Decleves X, Jacob A, Yousif S, Shawahna R, Potin S, et al. (2011) Interplay of drug metabolizing CYP450 enzymes and ABC transporters in the blood-brain barrier. Curr Drug Metab 12: 732–741. 21623707

38. Blandini F, Armentero MT (2012) Animal models of Parkinson’s disease. FEBS J 279: 1156–1166. doi: 10.1111/j.1742-4658.2012.08491.x 22251459

39. Ramsay RR, Singer TP (1986) Energy-dependent uptake of N-methyl-4-phenylpyridinium, the neurotoxic metabolite of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine, by mitochondria. J Biol Chem 261: 7585–7587. 3486869

40. Ramsay RR, Salach JI, Singer TP (1986) Uptake of the neurotoxin 1-methyl-4-phenylpyridine (MPP+) by mitochondria and its relation to the inhibition of the mitochondrial oxidation of NAD+-linked substrates by MPP+. Biochem Biophys Res Commun 134: 743–748. 2868716

41. Javitch JA, Snyder SH (1984) Uptake of MPP(+) by dopamine neurons explains selectivity of parkinsonism-inducing neurotoxin, MPTP. Eur J Pharmacol 106: 455–456. 6335692

42. Nicklas WJ, Vyas I, Heikkila RE (1985) Inhibition of NADH-linked oxidation in brain mitochondria by 1-methyl-4-phenyl-pyridine, a metabolite of the neurotoxin, 1-methyl-4-phenyl-1,2,5,6-tetrahydropyridine. Life Sci 36: 2503–2508. 2861548

43. Viaggi C, Vaglini F, Pardini C, Sgado P, Caramelli A, et al. (2007) CYP 2E1 mutant mice are resistant to DDC-induced enhancement of MPTP toxicity. J Neural Transm Suppl: 159–163.

44. Markey SP, Johannessen JN, Chiueh CC, Burns RS, Herkenham MA (1984) Intraneuronal generation of a pyridinium metabolite may cause drug-induced parkinsonism. Nature 311: 464–467. 6332988

45. Javitch JA, Uhl GR, Snyder SH (1984) Parkinsonism-inducing neurotoxin, N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine: characterization and localization of receptor binding sites in rat and human brain. Proc Natl Acad Sci U S A 81: 4591–4595. 6611553

46. Rappold PM, Cui M, Chesser AS, Tibbett J, Grima JC, et al. (2011) Paraquat neurotoxicity is mediated by the dopamine transporter and organic cation transporter-3. Proc Natl Acad Sci U S A 108: 20766–20771. doi: 10.1073/pnas.1115141108 22143804

47. Miksys SL, Tyndale RF (2002) Drug-metabolizing cytochrome P450s in the brain. J Psychiatry Neurosci 27: 406–415. 12491573

48. Lowndes HE, Beiswanger CM, Philbert MA, Reuhl KR (1994) Substrates for neural metabolism of xenobiotics in adult and developing brain. Neurotoxicology 15: 61–73. 8090363

49. Manto M (2012) Toxic agents causing cerebellar ataxias. Handb Clin Neurol 103: 201–213. doi: 10.1016/B978-0-444-51892-7.00012-7 21827890

50. Muller DJ, Schulze TG, Knapp M, Held T, Krauss H, et al. (2001) Familial occurrence of tardive dyskinesia. Acta Psychiatr Scand 104: 375–379. 11722319

51. Bakker PR, van Harten PN, van Os J (2008) Antipsychotic-induced tardive dyskinesia and polymorphic variations in COMT, DRD2, CYP1A2 and MnSOD genes: a meta-analysis of pharmacogenetic interactions. Mol Psychiatry 13: 544–556. doi: 10.1038/sj.mp.4002142 18180754

52. Arranz MJ, de Leon J (2007) Pharmacogenetics and pharmacogenomics of schizophrenia: a review of last decade of research. Mol Psychiatry 12: 707–747. 17549063

53. Aberg K, Adkins DE, Bukszar J, Webb BT, Caroff SN, et al. (2010) Genomewide association study of movement-related adverse antipsychotic effects. Biol Psychiatry 67: 279–282. doi: 10.1016/j.biopsych.2009.08.036 19875103

54. Moitra K, Scally M, McGee K, Lancaster G, Gold B, et al. (2011) Molecular evolutionary analysis of ABCB5: the ancestral gene is a full transporter with potentially deleterious single nucleotide polymorphisms. PLoS One 6: e16318. doi: 10.1371/journal.pone.0016318 21298007

55. Correll CU, Schenk EM (2008) Tardive dyskinesia and new antipsychotics. Curr Opin Psychiatry 21: 151–156. doi: 10.1097/YCO.0b013e3282f53132 18332662

56. Trusheim MR, Burgess B, Hu SX, Long T, Averbuch SD, et al. (2011) Quantifying factors for the success of stratified medicine. Nat Rev Drug Discov 10: 817–833. doi: 10.1038/nrd3557 22037040

57. Guo Y, Shafer S, Weller P, Usuka J, Peltz G (2005) Pharmacogenomics and drug development. Pharmacogenomics 6: 857–864. 16296948