Epistasis between polymorphisms in COMT, ESR1, and GCH1 influences COMT enzyme activity and pain

Pain

Volumn 155, Issue 11, 2014, Pages 2390-2399

  Smith, Shad B ^a   Reenilä, Ilkka ^b   Männistö, Pekka T ^b   Slade, Gary D ^a   Maixner, William ^a   Diatchenko, Luda ^a,c   Nackley, Andrea G ^a  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b UNIVERSITY OF HELSINKI   (Finland)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

Catecholamines; Fibromyalgia; Gene expression; Gene gene interaction; Temporomandibular disorders

Indexed keywords

5,10 METHYLENETETRAHYDROFOLATE REDUCTASE (FADH2); CATECHOL METHYLTRANSFERASE; ESTROGEN RECEPTOR ALPHA; GUANOSINE TRIPHOSPHATE CYCLOHYDROLASE I; METHIONINE; VALINE; COMT PROTEIN, HUMAN; ESTROGEN RECEPTOR ALPHA, HUMAN; METHYLENETETRAHYDROFOLATE REDUCTASE (NADPH2);

ADULT; ALLELE; ARTICLE; CONTROLLED STUDY; DISTRESS SYNDROME; ENZYME ACTIVITY; EPISTASIS; FEMALE; GENE INTERACTION; GENE LINKAGE DISEQUILIBRIUM; GENETIC ASSOCIATION; GENETIC VARIABILITY; GENOTYPE; HAPLOTYPE; HETEROZYGOTE; HUMAN; JAW DISEASE; MAJOR CLINICAL STUDY; MUSCULOSKELETAL PAIN; NOCICEPTION; OUTCOME ASSESSMENT; PAIN; PAIN THRESHOLD; PHENOTYPE; PRIORITY JOURNAL; RISK FACTOR; SELF REPORT; SINGLE NUCLEOTIDE POLYMORPHISM; ADOLESCENT; CASE CONTROL STUDY; ENZYMOLOGY; GENETICS; METABOLISM; MIDDLE AGED; MOOD DISORDERS; PSYCHOLOGY; RETROSPECTIVE STUDY; YOUNG ADULT;

ADOLESCENT; ADULT; CASE-CONTROL STUDIES; CATECHOL O-METHYLTRANSFERASE; EPISTASIS, GENETIC; ESTROGEN RECEPTOR ALPHA; FEMALE; GENOTYPE; GTP CYCLOHYDROLASE; HUMANS; METHYLENETETRAHYDROFOLATE REDUCTASE (NADPH2); MIDDLE AGED; MOOD DISORDERS; PAIN; PAIN PERCEPTION; POLYMORPHISM, SINGLE NUCLEOTIDE; RETROSPECTIVE STUDIES; YOUNG ADULT;

EID: 84923571639     PISSN: 03043959     EISSN: 18726623     Source Type: Journal    
DOI: 10.1016/j.pain.2014.09.009     Document Type: Article

References (72)

1. Ahlers SJ, Elens LL, van Gulik L, van Schaik RH, van Dongen EP, Bruins P, Tibboel D, Knibbe CA. The Val158Met polymorphism of the COMT gene is associated with increased pain sensitivity in morphine-treated patients undergoing a painful procedure after cardiac surgery. Br J Clin Pharmacol 2013;75:1506-15.
2. Antoniades C, Shirodaria C, Van Assche T, Cunnington C, Tegeder I, Lotsch J, Guzik TJ, Leeson P, Diesch J, Tousoulis D, Stefanadis C, Costigan M, Woolf CJ, Alp NJ, Channon KM. GCH1 haplotype determines vascular and plasma biopterin availability in coronary artery disease effects on vascular superoxide production and endothelial function. J Am Coll Cardiol 2008;52:158-65.
3. Barbosa FR, Matsuda JB, Mazucato M, de Castro Franca S, Zingaretti SM, da Silva LM, Martinez-Rossi NM, Junior MF, Marins M, Fachin AL. Influence of catechol-O-methyltransferase (COMT) gene polymorphisms in pain sensibility of Brazilian fibromialgia patients. Rheumatol Int 2012;32:427-30.
4. Barnett JH, Heron J, Ring SM, Golding J, Goldman D, Xu K, Jones PB. Genderspecific effects of the catechol-O-methyltransferase Val108/158Met polymorphism on cognitive function in children. Am J Psychiatry 2007;164:142-9.
5. Belfer I, Schreiber KL, Shaffer JR, Shnol H, Blaney K, Morando A, Englert D, Greco C, Brufsky A, Ahrendt G, Kehlet H, Edwards RR, Bovbjerg DH. Persistent postmastectomy pain in breast cancer survivors: Analysis of clinical, demographic, and psychosocial factors. J Pain 2013;14:1185-95.
6. Boada M, Antunez C, Lopez-Arrieta J, Caruz A, Moreno-Rey C, Ramirez-Lorca R, Moron FJ, Hernandez I, Mauleon A, Rosende-Roca M, Martinez-Lage P, Marin J, Tarraga L, Alegret M, Pedrajas JR, Urda N, Royo JL, Saez ME, Gayan J, Gonzalez-Perez A, Real LM, Ruiz A, Galan JJ. Estrogen receptor alpha gene variants are associated with Alzheimer's disease. Neurobiol Aging 2012;198:e15-24.
7. Boudikova B, Szumlanski C, Maidak B, Weinshilboum R. Human liver catechol-O-methyltransferase pharmacogenetics. Clin Pharmacol Ther 1990;48:381-9.
8. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976;72:248-54.
9. Bray NJ, Buckland PR, Williams NM, Williams HJ, Norton N, Owen MJ, O'Donovan MC. A haplotype implicated in schizophrenia susceptibility is associated with reduced COMT expression in human brain. Am J Hum Genet 2003;73:152-61.
10. Carlsson GE, Le Resche L. Epidemiology of temporomandibular disorders. In: Sessle BJ, Bryant PS, Dionne RA, editors. Temporomandibular disorders and related pain conditions, vol. 4. Seattle: IASP Press; 1995. p. 211-26.
11. Chen H, Nackley A, Miller V, Diatchenko L, Maixner W. Multisystem dysregulation in painful temporomandibular disorders. J Pain 2013;14:983-96.
12. Chen H, Slade G, Lim PF, Miller V, Maixner W, Diatchenko L. Relationship between temporomandibular disorders, widespread palpation tenderness, and multiple pain conditions: A case-control study. J Pain 2012;13: 1016-27.
13. Chen LX, Fang Q, Chen Q, Guo J, Wang ZZ, Chen Y, Wang R. Study in vitro and in vivo of nociceptin/orphanin FQ(1-13)NH2 analogues substituting N-Me-Gly for Gly2 or Gly3. Peptides 2004;25:1349-54.
14. Chen X, Levine JD. Epinephrine-induced excitation and sensitization of rat Cfiber nociceptors. J Pain 2005;6:439-46.
15. Cohen H, Neumann L, Glazer Y, Ebstein RP, Buskila D. The relationship between a common catechol-O-methyltransferase (COMT) polymorphism val(158) met and fibromyalgia. Clin Exp Rheumatol 2009;27:S51-56.
16. Cohen S, Kamarck T, Mermelstein R. A global measure of perceived stress. J Health Soc Behav 1983;24:385-96.
17. Derogatis LR, Lipman RS, Covi L. SCL-90: An outpatient psychiatric rating scale-preliminary report. Psychopharmacol Bull 1973;9:13-28.
18. Devlin B, Roeder K. Genomic control for association studies. Biometrics 1999;55:997-1004.
19. Diatchenko L, Slade GD, Nackley AG, Bhalang K, Sigurdsson A, Belfer I, Goldman D, Xu K, Shabalina SA, Shagin D, Max MB, Makarov SS, Maixner W. Genetic basis for individual variations in pain perception and the development of a chronic pain condition. Hum Mol Genet 2005;14:135-43.
20. Domschke K, Deckert J, O'Donovan MC, Glatt SJ. Meta-analysis of COMT val158met in panic disorder: ethnic heterogeneity and gender specificity. Am J Med Genet B Neuropsychiatr Genet 2007;144B:667-73.
21. Dworkin SF, LeResche L. Research diagnostic criteria for temporomandibular disorders: review, criteria, examinations and specifications, critique. J Craniomandib Disord 1992;6:301-55.
22. Fan W, Huang F, Wu Z, Zhu X, Li D, He H. The role of nitric oxide in orofacial pain. Nitric Oxide 2012;26:32-7.
23. Fernandez-de-Las-Penas C, Ambite-Quesada S, Gil-Crujera A, Cigaran-Mendez M, Penacoba-Puente C. Catechol-O-methyltransferase Val158Met polymorphism influences anxiety, depression, and disability, but not pressure pain sensitivity, in women with fibromyalgia syndrome. J Pain 2012;13:1068-74.
24. Fernandez-de-las-Penas C, Fernandez-Lao C, Cantarero-Villanueva I, Ambite-Quesada S, Rivas-Martinez I, del Moral-Avila R, Arroyo-Morales M. Catechol-Omethyltransferase genotype (Val158met) modulates cancer-related fatigue and pain sensitivity in breast cancer survivors. Breast Cancer Res Treat 2012;133:405-12.
25. Gasparotto AS, Sprinz E, Lazzaretti RK, Kuhmmer R, Silveira JM, Basso RP, Pinheiro CA, Silveira MF, Ribeiro JP, Mattevi VS. Genetic polymorphisms in estrogen receptors and sexual dimorphism in fat redistribution in HIV-infected patients on HAART. AIDS 2012;26:19-26.
26. George SZ, Wallace MR, Wright TW, Moser MW, Greenfield III WH, Sack BK, Herbstman DM, Fillingim RB. Evidence for a biopsychosocial influence on shoulder pain: pain catastrophizing and catechol-O-methyltransferase (COMT) diplotype predict clinical pain ratings. PAIN- 2008;136:53-61.
27. Goldstein DS. Catecholamines and stress. Endocr Regul 2003;37:69-80.
28. Gracely RH. Evaluation of multi-dimensional pain scales. PAIN- 1992;48:297-300.
29. Gursoy S, Erdal E, Herken H, Madenci E, Alasehirli B, Erdal N. Significance of catechol-O-methyltransferase gene polymorphism in fibromyalgia syndrome. Rheumatol Int 2003;23:104-7.
30. Harden RN, Rudin NJ, Bruehl S, Kee W, Parikh DK, Kooch J, Duc T, Gracely RH. Increased systemic catecholamines in complex regional pain syndrome and relationship to psychological factors: A pilot study. Anesth Analg 2004;99:1478-85.
31. Harrison PJ, Tunbridge EM. Catechol-O-methyltransferase (COMT): A gene contributing to sex differences in brain function, and to sexual dimorphism in the predisposition to psychiatric disorders. Neuropsychopharmacology 2008;33:3037-45.
32. Hickey OT, Nugent NF, Burke SM, Hafeez P, Mudrakouski AL, Shorten GD. Persistent pain after mastectomy with reconstruction. J Clin Anesth 2011;23:482-8.
33. Huo L, Straub RE, Roca C, Schmidt PJ, Shi K, Vakkalanka R, Weinberger DR, Rubinow DR. Risk for premenstrual dysphoric disorder is associated with genetic variation in ESR1, the estrogen receptor alpha gene. Biol Psychiatry 2007;62:925-33.
34. Jaeger B, Reeves JL. Quantification of changes in myofascial trigger point sensitivity with the pressure algometer following passive stretch. PAIN- 1986;27:203-10.
35. Jiang H, Xie T, Ramsden DB, Ho SL. Human catechol-O-methyltransferase down-regulation by estradiol. Neuropharmacology 2003;45:1011-8.
36. Karayiorgou M, Altemus M, Galke BL, Goldman D, Murphy DL, Ott J, Gogos JA. Genotype determining low catechol-O-methyltransferase activity as a risk factor for obsessive-compulsive disorder. Proc Natl Acad Sci USA 1997;94:4572-5.
37. Kelly TN, Rebholz CM, Gu D, Hixson JE, Rice TK, Cao J, Chen J, Li J, Lu F, Ma J, Mu J, Whelton PK, He J. Analysis of sex hormone genes reveals gender differences in the genetic etiology of blood pressure salt sensitivity: the GenSalt study. Am J Hypertens 2013;26:191-200.
38. Lee PJ, Delaney P, Keogh J, Sleeman D, Shorten GD. Catecholamine-omethyltransferase polymorphisms are associated with postoperative pain intensity. Clin J Pain 2011;27:93-101.
39. Lorr M, Mcnair DM. Profie of Mood States-Bipolar form (POMS-BI). San Diego, CA: Educational and Industrial Testing Service; 1988.
40. Lotsch J, Belfer I, Kirchhof A, Mishra BK, Max MB, Doehring A, Costigan M, Woolf CJ, Geisslinger G, Tegeder I. Reliable screening for a pain-protective haplotype in the GTP cyclohydrolase 1 gene (GCH1) through the use of 3 or fewer single nucleotide polymorphisms. Clin Chem 2007;53:1010-5.
41. Lotta T, Vidgren J, Tilgmann C, Ulmanen I, Melen K, Julkunen I, Taskinen J. Kinetics of human soluble and membrane-bound catechol Omethyltransferase: A revised mechanism and description of the thermolabile variant of the enzyme. Biochemistry 1995;34:4202-10.
42. Lundstrom K, Salminen M, Jalanko A, Savolainen R, Ulmanen I. Cloning and characterization of human placental catechol-O-methyltransferase cDNA. DNA Cell Biol 1991;10:181-9.
43. Lupo PJ, Chapa C, Nousome D, Duhon C, Canfield MA, Shaw GM, Finnell RH, Zhu H. A GCH1 haplotype and risk of neural tube defects in the National Birth Defects Prevention Study. Mol Genet Metab 2012;107:592-5.
44. Matsuda JB, Barbosa FR, Morel LJ, Franca Sde C, Zingaretti SM, da Silva LM, Pereira AM, Marins M, Fachin AL. Serotonin receptor (5-HT 2A) and catechol-O-methyltransferase (COMT) gene polymorphisms: triggers of fibromyalgia? Rev Bras Reumatol 2010;50:141-9.
45. Muntjewerff JW, Gellekink H, den Heijer M, Hoogendoorn ML, Kahn RS, Sinke RJ, Blom HJ. Polymorphisms in catechol-O-methyltransferase and methylenetetrahydrofolate reductase in relation to the risk of schizophrenia. Eur Neuropsychopharmacol 2008;18:99-106.
46. Nackley AG, Shabalina SA, Tchivileva IE, Satterfield K, Korchynskyi O, Makarov SS, Maixner W, Diatchenko L. Human catechol-O-methyltransferase haplotypes modulate protein expression by altering mRNA secondary structure. Science 2006;314:1930-3.
47. Nagatsu T, Ichinose H. Regulation of pteridine-requiring enzymes by the cofactor tetrahydrobiopterin. Mol Neurobiol 1999;19:79-96.
48. Olsson CA, Anney RJ, Lotfi-Miri M, Byrnes GB, Williamson R, Patton GC. Association between the COMT Val158Met polymorphism and propensity to anxiety in an Australian population-based longitudinal study of adolescent health. Psychiatr Genet 2005;15:109-15.
49. Price DD, Hu JW, Dubner R, Gracely RH. Peripheral suppression of first pain and central summation of second pain evoked by noxious heat pulses. PAIN- 1977;3:57-68.
50. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira M, Bender D, Maller J, Sklar P, de Bakker P, Daly M, Sham P. PLINK: A tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 2007;81:559-75.
51. Raja SN. Role of the sympathetic nervous system in acute pain and inflammation. Ann Med 1995;27:241-6.
52. Ramachandran R, Ploug KB, Hay-Schmidt A, Olesen J, Jansen-Olesen I, Gupta S. Nitric oxide synthase (NOS) in the trigeminal vascular system and other brain structures related to pain in rats. Neurosci Lett 2010;484:192-6.
53. Scanlon PD, Raymond FA, Weinshilboum RM. Catechol-O-methyltransferase: thermolabile enzyme in erythrocytes of subjects homozygous for allele for low activity. Science 1979;203:63-5.
54. Schmidtko A, Tegeder I, Geisslinger G. No NO, no pain? The role of nitric oxide and cGMP in spinal pain processing. Trends Neurosci 2009;32: 339-46.
55. Schultz E, Nissinen E, Kaakkola S. Determination of catechol-Omethyltransferase activity in erythrocytes by high performance liquid chromatography with electrochemical detection. Biomed Chromatogr 1989;3:64-7.
56. Shield AJ, Thomae BA, Eckloff BW, Wieben ED, Weinshilboum RM. Human catechol O-methyltransferase genetic variation: gene resequencing and functional characterization of variant allozymes. Mol Psychiatry 2004;9:151-60.
57. Slade GD, Conrad MS, Diatchenko L, Rashid NU, Zhong S, Smith S, Rhodes J, Medvedev A, Makarov S, Maixner W, Nackley AG. Cytokine biomarkers and chronic pain: Association of genes, transcription, and circulating proteins with temporomandibular disorders and widespread palpation tenderness. PAIN- 2011;152:2802-12.
58. Slade GD, Diatchenko L, Ohrbach R, Maixner W. Orthodontic treatment, genetic factors and risk of temporomandibular disorder. Semin Orthod 2008;14:146-56.
59. Sladek-Chelgren S, Weinshilboum RM. Catechol-O-methyltransferase biochemical genetics: human lymphocyte enzyme. Biochem Genet 1981;19:1037-53.
60. Tchivileva IE, Lim PF, Smith SB, Slade GD, Diatchenko L, McLean SA, Maixner W. Effect of catechol-O-methyltransferase polymorphism on response to propranolol therapy in chronic musculoskeletal pain: A randomized, doubleblind, placebo-controlled, crossover pilot study. Pharmacogenet Genomics 2010;20:239-48.
61. Tegeder I, Costigan M, Griffin RS, Abele A, Belfer I, Schmidt H, Ehnert C, Nejim J, Marian C, Scholz J, Wu T, Allchorne A, Diatchenko L, Binshtok AM, Goldman D, Adolph J, Sama S, Atlas SJ, Carlezon WA, Parsegian A, Lotsch J, Fillingim RB, Maixner W, Geisslinger G, Max MB, Woolf CJ. GTP cyclohydrolase and tetrahydrobiopterin regulate pain sensitivity and persistence. Nat Med 2006;12:1269-77.
62. Tenhunen J, Salminen M, Jalanko A, Ukkonen S, Ulmanen I. Structure of the rat catechol-O-methyltransferase gene: separate promoters are used to produce mRNAs for soluble and membrane-bound forms of the enzyme. DNA Cell Biol 1993;12:253-63.
63. Tsao D, Shabalina SA, Gauthier J, Dokholyan NV, Diatchenko L. Disruptive mRNA folding increases translational efficiency of catechol-Omethyltransferase variant. Nucleic Acids Res 2011;39:6201-12.
64. Tuomainen P, Reenila I, Mannisto PT. Validation of assay of catechol-Omethyltransferase activity in human erythrocytes. J Pharm Biomed Anal 1996;14:515-23.
65. van Meurs JB, Uitterlinden AG, Stolk L, Kerkhof HJ, Hofman A, Pols HA, Bierma-Zeinstra SM. A functional polymorphism in the catechol-O-methyltransferase gene is associated with osteoarthritis-related pain. Arthritis Rheum 2009;60:628-9.
66. Vargas-Alarcon G, Fragoso JM, Cruz-Robles D, Vargas A, Vargas A, Lao-Villadoniga JI, Garcia-Fructuoso F, Ramos-Kuri M, Hernandez F, Springall R, Bojalil R, Vallejo M, Martinez-Lavin M. Catechol-O-methyltransferase gene haplotypes in Mexican and Spanish patients with fibromyalgia. Arthritis Res Ther 2007;9:R110.
67. Voelker P, Sheese BE, Rothbart MK, Posner MI. Variations in catechol-Omethyltransferase gene interact with parenting to influence attention in early development. Neuroscience 2009;164:121-30.
68. Ware J, Kosinski M, Keller S. SF-12: how to score the SF-12 physical and mental health summary scales. Boston, Massachusetts: The Health Institute, New England Medical Center; 1995.
69. Weinshilboum RM. Human biochemical genetics of plasma dopamine-betahydroxylase and erythrocyte catechol-o-methyltransferase. Hum Genet Suppl 1978;1:101-12.
70. Wise PM, Dubal DB, Wilson ME, Rau SW, Liu Y. Estrogens: trophic and protective factors in the adult brain. Front Neuroendocrinol 2001;22:33-66.
71. Wolfe F, Smythe HA, Yunus MB, Bennett RM, Bombardier C, Goldenberg DL, Tugwell P, Campbell SM, Abeles M, Clark P, Fam Adel G, Farber Stephen J, Fiechtner Justus J, Franklin C Michael, Gatter Robert A, Hamaty Daniel, Lessard James, Lichtbroun Alan S, Masi Alfonse T, Mccain Glenn A, Reynolds W John, Romano Thomas J, Russell I Jon, Sheon Robert P. The American College of Rheumatology 1990 Criteria for the Classification of Fibromyalgia. Report of the Multicenter Criteria Committee. Arthritis Rheum 1990;33:160-72.
72. Zubieta JK, Heitzeg MM, Smith YR, Bueller JA, Xu K, Xu Y, Koeppe RA, Stohler CS, Goldman D. COMT val158met genotype affects mu-opioid neurotransmitter responses to a pain stressor. Science 2003;299:1240-3.