Serotonin transporter polymorphism alters citalopram effects on human pain responses to physical pain

NeuroImage

Volumn 135, Issue , 2016, Pages 186-196

  Ma, Yina ^a,b   Wang, Chenbo ^a   Luo, Siyang ^a   Li, Bingfeng ^a   Wager, Tor D ^c   Zhang, Wenxia ^a   Rao, Yi ^a   Han, Shihui ^a  

^a PEKING UNIVERSITY   (China)

^b BEIJING NORMAL UNIVERSITY   (China)

^c UNIVERSITY OF COLORADO   (United States)

Author keywords

5 HTTLPR; FMRI; Pain perception; Personalized medicine; SSRI

Indexed keywords

CITALOPRAM; PLACEBO; SEROTONIN; SEROTONIN TRANSPORTER; ANALGESIC AGENT; SEROTONIN UPTAKE INHIBITOR;

5 HTTLPR GENE; ADULT; ANALGESIA; ANTERIOR INSULA; ARTICLE; BRAIN FUNCTION; CEREBELLUM; CINGULATE GYRUS; CONTROLLED STUDY; DOUBLE BLIND PROCEDURE; ELECTROSTIMULATION; FRONTAL CORTEX; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GENE; GENETIC POLYMORPHISM; GENETIC VARIATION; GENOTYPE; HOMOZYGOSITY; HUMAN; HUMAN EXPERIMENT; INFORMATION PROCESSING; MALE; NEUROBIOLOGY; NEUROIMAGING; NOCICEPTION; NORMAL HUMAN; PAIN; PAIN THRESHOLD; POLYMERASE CHAIN REACTION; PREDICTION; PRIORITY JOURNAL; THALAMUS; TREATMENT RESPONSE; VOLUNTEER; YOUNG ADULT; DRUG EFFECTS; FEMALE; GENETICS; PAIN MEASUREMENT; PHARMACOGENETIC TESTING; PLACEBO EFFECT; PROCEDURES; RANDOMIZED CONTROLLED TRIAL; SINGLE NUCLEOTIDE POLYMORPHISM; TREATMENT OUTCOME;

ANALGESICS; CITALOPRAM; DOUBLE-BLIND METHOD; FEMALE; HUMANS; MALE; PAIN MEASUREMENT; PAIN PERCEPTION; PAIN THRESHOLD; PHARMACOGENOMIC TESTING; PLACEBO EFFECT; POLYMORPHISM, SINGLE NUCLEOTIDE; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS; SEROTONIN UPTAKE INHIBITORS; TREATMENT OUTCOME; YOUNG ADULT;

EID: 84965003000     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2016.04.064     Document Type: Article

References (86)

1. Aiken L.S., West S.G. Multiple Regression: Testing and Interpreting Interactions 1991, Sage, Newbury Park, CA.
2. Apkarian A.V., Bushnell M.C., Treede R.D., Zubieta J.K. Human brain mechanisms of pain perception and regulation in health and disease. Eur. J. Pain 2005, 9:463-484.
3. Atlas L.Y., Lindquist M.A., Bolger N., Wager T.D. Brain mediators of the effects of noxious heat on pain. Pain 2014, 155:1632-1648.
4. Baliki M.N., Geha P.Y., Apkarian A.V. Parsing pain perception between nociceptive representation and magnitude estimation. J. Neurophysiol. 2009, 101:875-887.
5. Bandolier Extra (Evidence-based health care). Acute pain. The 2007 Oxford league table of analgesic efficacy. Bandolier. Available from: . http://www.medicine.ox.ac.uk/bandolier/booth/painpag/acutrev/analgesics/leagtab.html.
6. Bengel D., Murphy D.L., Andrews A.M., Wichems C.H., Feltner D., Heils A., Mössner R., Westphal H., Lesch K.P. Altered brain serotonin homeostasis and locomotor insensitivity to 3, 4-methylenedioxymethamphetamine ("ecstasy") in serotonin transporter-deficient mice. Mol. Pharmacol. 1998, 53:649-655.
7. Bruehl S., Apkarian A.V., Ballantyne J.C., Berger A., Borsook D., Chen W.G., Farrar J.T., Haythornthwaite J.A., Horn S.D., Iadarola M.J., Inturrisi C.E. Personalized medicine and opioid analgesic prescribing for chronic pain: opportunities and challenges. J. Pain 2013, 14:103-113.
8. Bushnell M.C., Duncan G.H., Hofbauer R.K., Ha B., Chen J.I., Carrier B. Pain perception: is there a role for primary somatosensory cortex?. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:7705-7709.
9. Bushnell M.C., Ceko M., Low L.A. Cognitive and emotional control of pain and its disruption in chronic pain. Nat. Rev. Neurosci. 2013, 14:502-511.
10. Carlsson K., Andersson J., Petrovic P., Petersson K.M., Ohman A., Ingvar M. Predictability modulates the affective and sensory-discriminative neural processing of pain. Neuroimage 2006, 32:1804-1814.
11. Chesterton L.S., Barlas P., Foster N.E., Baxter G.D., Wright C.C. Gender differences in pressure pain threshold in healthy humans. Pain 2003, 101:259-266.
12. Chopra K., Arora V. An intricate relationship between pain and depression: clinical correlates, coactivation factors and therapeutic targets. Expert Opin. Ther. Targets 2014, 18:159-176.
13. Chua P., Krams M., Toni I., Passingham R., Dolan R. A functional anatomy of anticipatory anxiety. NeuroImage 1999, 9:563-571.
14. Coghill R.C. Individual differences in the subjective experience of pain: new insights into mechanisms and models. Headache 2010, 50:1531-1535.
15. Coghill R.C., Sang C.N., Maisog J.M., Iadarola M.J. Pain intensity processing within the human brain: a bilateral, distributed mechanism. J. Neurophysiol. 1999, 82:1934-1943.
16. Coghill R.C., McHaffie J.G., Yen Y.F. Neural correlates of interindividual differences in the subjective experience of pain. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:8538-8542.
17. Cohen H., Buskila D., Neumann L., Ebstein R.P. Confirmation of an association between fibromyalgia and serotonin transporter promoter region (5-HTTLPR) polymorphism, and relationship to anxiety-related personality traits. Arthritis Rheum. 2002, 46:845-847.
18. Craig A.D. Significance of the insula for the evolution of human awareness of feelings from the body. Ann. N. Y. Acad. Sci. 2011, 1225:72-82.
19. Dib-Hajj S.D., Waxman S.G. Translational pain research: lessons from genetics and genomics. Sci. Transl. Med. 2014, 6:249sr4.
20. Drabant E.M., Ramel W., Edge M.D., Hyde L.W., Kuo J.R., Goldin P.R., Hariri A.R., Gross J.J. Neural mechanisms underlying 5-HTTLPR-related sensitivity to acute stress. Am. J. Psychiatry 2012, 169:397-405.
21. Fillingim R.B., King C.D., Ribeiro-Dasilva M.C., Rahim-Williams B., Riley J.L. Sex, gender, and pain: a review of recent clinical and experimental findings. J. Pain 2009, 10:447-485.
22. Finnerup N.B., Attal N., Haroutounian S., McNicol E., Baron R., Dworkin R.H., Gilron I., Haanpää M., Hansson P., Jensen T.S., Kamerman P.R. Pharmacotherapy for neuropathic pain in adults: a systematic review and meta-analysis. Lancet Neurol. 2015, 14:162-173.
23. Gatch M.B., Negus S.S., Mello N.K. Antinociceptive effects of monoamine reuptake inhibitors administered alone or in combination with mu opioid agonists in rhesus monkeys. Psychopharmacology 1998, 135:99-106.
24. Hariri A.R., Mattay V.S., Tessitore A., Kolachana B., Fera F., Goldman D., Egan M.F., Weinberger D.R. Serotonin transporter genetic variation and the response of the human amygdala. Science 2002, 297:400-403.
25. Hu X.Z., Rush A.J., Charney D., Wilson A.F., Sorant A.J., Papanicolaou G.J., Fava M., Trivedi M.H., Wisniewski S.R., Laje G., Paddock S. Association between a functional serotonin transporter promoter polymorphism and citalopram treatment in adult outpatients with major depression. Arch. Gen. Psychiatry 2007, 64:783-792.
26. Jackson P.L., Meltzoff A.N., Decety J. How do we perceive the pain of others? A window into the neural processes involved in empathy. NeuroImage 2005, 24:771-779.
27. Kano M., Farmer A.D., Aziz Q., Giampietro V.P., Brammer M.J., Williams S.C., Fukudo S., Coen S.J. Sex differences in brain response to anticipated and experienced visceral pain in healthy subjects. Am. J. Physiol. Gastrointest. Liver Physio. 2013, 304:G687-G699.
28. Kapur S., Phillips A.G., Insel T.R. Why has it taken so long for biological psychiatry to develop clinical tests and what to do about it?. Mol. Psychiatry 2012, 17:1174-1179.
29. Katona C., Peveler R., Dowrick C., Wessely S., Feinmann C., Gask L., Lloyd H., de C Williams A.C., Wager E. Pain symptoms in depression: definition and clinical significance. Clin. Med. 2005, 5:390-395.
30. Kim D.K., Lim S.W., Lee S., Sohn S.E., Kim S., Hahn C.G., Carroll B.J. Serotonin transporter gene polymorphism and antidepressant response. Neuroreport 2000, 11:215-219.
31. Kim H., Neubert J.K., San Miguel A., Xu K., Krishnaraju R.K., Iadarola M.J., Goldman D., Dionne R.A. Genetic influence on variability in human acute experimental pain sensitivity associated with gender, ethnicity and psychological temperament. Pain 2004, 109:488-496.
32. Koyama T., McHaffie J.G., Laurienti P.J., Coghill R.C. The subjective experience of pain: where expectations become reality. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:12950-12955.
33. Kupers R., Frokjaer V.G., Naert A., Christensen R., Budtz-Joergensen E., Kehlet H., Knudsen G.M. A PET [18F]altanserin study of 5-HT2A receptor binding in the human brain and responses to painful heat stimulation. NeuroImage 2009, 44:1001-1007.
34. Kupers R., Frokjaer V.G., Erritzoe D., Naert A., Budtz-Joergensen E., Nielsen F.A., Kehlet H., Knudsen G.M. Serotonin transporter binding in the hypothalamus correlates negatively with tonic heat pain ratings in healthy subjects: a [11C]DASB PET study. NeuroImage 2011, 54:1336-1343.
35. Lanier L.H. Variability in the pain threshold. Science 1943, 97:49-50.
36. Lee Y.C., Chen P.P. A review of SSRIs and SNRIs in neuropathic pain. Expert. Opin. Pharmacother. 2010, 11:2813-2825.
37. Lee B.T., Ham B.J. Serotonergic genes and amygdala activity in response to negative affective facial stimuli in Korean women. Genes Brain Behav. 2008, 7:899-905.
38. Lesch K.P., Heils A. Serotonergic gene transcriptional control regions: targets for antidepressant drug development?. Int. J. Neuropsychopharmacol. 2000, 3:67-79.
39. Lesch K.P., Bengel D., Heils A., Sabol S.Z., Greenberg B.D., Petri S., Benjamin J., Müller C.R., Hamer D.H., Murphy D.L. Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science 1996, 274:1527-1531.
40. Levine J.D., Gordon N.C., Smith R., Fields H.L. Analgesic responses to morphine and placebo in individuals with postoperative pain. Pain 1981, 10:379-389.
41. Lindstedt F., Lonsdorf T.B., Schalling M., Kosek E., Ingvar M. Perception of thermal pain and the thermal grill illusion is associated with polymorphisms in the serotonin transporter gene. PLoS One 2011, 6.
42. Long H., Liu B., Hou B., Wang C., Li J., Qin W., Wang D., Zhou Y., Kendrick K., Yu C., Jiang T. The long rather than the short allele of 5-HTTLPR predisposes Han Chinese to anxiety and reduced connectivity between prefrontal cortex and amygdala. Neurosci. Bull. 2013, 29:4-15.
43. Lötsch J., Geisslinger G., Tegeder I. Genetic modulation of the pharmacological treatment of pain. Pharmacol. Ther. 2009, 124:168-184.
44. Lunn T.H., Frokjaer V.G., Hansen T.B., Kristensen P.W., Lind T., Kehlet H. Analgesic effect of perioperative escitalopram in high pain catastrophizing patients after total knee arthroplasty: a randomized, double-blind, placebo-controlled trial. Anesthesiology 2015, 122:884-894.
45. Ma Y. Neuropsychological mechanism underlying antidepressant effect: a systematic meta-analysis. Mol. Psychiatry 2015, 20:311-319.
46. Ma Y., Li B., Wang C., Shi Z., Sun Y., Sheng F., Zhang Y., Zhang W., Rao Y., Han S. 5-HTTLPR polymorphism modulates neural mechanisms of negative self-reflection. Cereb. Cortex 2014, 24:2421-2429.
47. Ma Y., Wang C., Li B., Zhang W., Rao Y., Han S. Does self-construal predict activity in the social brain network? A genetic moderation effect. Soc. Cogn. Affect. Neurosci. 2014, 9:1360-1367.
48. Ma Y., Li B., Zhang W., Rao Y., Han S. Allelic variation in 5-HTTLPR and the effects of citalopram on the emotional neural network. Br. J. Psychiatry 2015, 206:385-392.
49. Mandrioli R., Mercolini L., Saracino M.A., Raggi M.A. Selective serotonin reuptake inhibitors (SSRIs): therapeutic drug monitoring and pharmacological interactions. Curr. Med. Chem. 2012, 19:1846-1863.
50. Marziniak M., Mössner R., Schmitt A., Lesch K.P., Sommer C. A functional serotonin transporter gene polymorphism is associated with migraine with aura. Neurology 2005, 64:157-159.
51. Melnikova I. Pain market. Nat. Rev. Drug Discov. 2010, 9:589-590.
52. Millan M.J. Descending control of pain. Prog. Neurobiol. 2002, 66:355-474.
53. Mogil J.S. The genetic mediation of individual differences in sensitivity to pain and its inhibition. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:7744-7751.
54. Mogil J.S. Animal models of pain: progress and challenges. Nat. Rev. Neurosci. 2009, 10:283-294.
55. Mogil J.S., Wilson S.G., Chesler E.J., Rankin A.L., Nemmani K.V., Lariviere W.R., Groce M.K., Wallace M.R., Kaplan L., Staud R., Ness T.J. The melanocortin-1 receptor gene mediates female-specific mechanisms of analgesia in mice and humans. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:4867-4872.
56. Monat A., Averill J.R., Lazarus R.S. Anticipatory stress and coping reactions under various conditions of uncertainty. J. Pers. Soc. Psychol. 1972, 24:237-253.
57. Moulton E.A., Schmahmann J.D., Becerra L., Borsook D. The cerebellum and pain: passive integrator or active participator?. Brain Res. Rev. 2010, 65:14-27.
58. Nandam L.S., Hester R., Wagner J., Cummins T.D., Garner K., Dean A.J., Kim B.N., Nathan P.J., Mattingley J.B., Bellgrove M.A. Methylphenidate but not atomoxetine or citalopram modulates inhibitory control and response time variability. Biol. Psychiatry 2011, 69:902-904.
59. Norbury T.A., MacGregor A.J., Urwin J., Spector T.D., McMahon S.B. Heritability of responses to painful stimuli in women: a classical twin study. Brain 2007, 130:3041-3049.
60. Ostrowsky K., Magnin M., Ryvlin P., Isnard J., Guenot M., Mauguiere F. Representation of pain and somatic sensation in the human insula: a study of responses to direct electrical cortical stimulation. Cereb. Cortex 2002, 12:376-385.
61. Ota M., Fukushima H., Kulski J.K., Inoko H. Single nucleotide polymorphism detection by polymerase chain reaction-restriction fragment length polymorphism. Nat. Protoc. 2007, 2:2857-2864.
62. Otto M., Bach F.W., Jensen T.S., Brøsen K., Sindrup S.H. Escitalopram in painful polyneuropathy: a randomized, placebo-controlled, cross-over trial. Pain 2008, 139:275-283.
63. Palit S., Sheaff R.J., France C.R., McGlone S.T., Potter W.T., Harkness A.R., McNulty J.L., Bartley E.J., Hoffmann R., Monda J.K., Rhudy J.L. Serotonin transporter gene (5-HTTLPR) polymorphisms are associated with emotional modulation of pain but not emotional modulation of spinal nociception. Biol. Psychol. 2011, 86:360-369.
64. Palm F., Mössner R., Chen Y., He L., Gerlach M., Bischofs S., Riederer P., Lesch K.P., Sommer C. Reduced thermal hyperalgesia and enhanced peripheral nerve injury after hind paw inflammation in mice lacking the serotonin-transporter. Eur. J. Pain 2008, 12:790-797.
65. Peyron R., Laurent B., García-Larrea L. Functional imaging of brain responses to pain. A review and meta-analysis (2000). Neurophysiol. Clin. 2000, 30:263-288.
66. Pezawas L., Meyer-Lindenberg A., Drabant E.M., Verchinski B.A., Munoz K.E., Kolachana B.S., Egan M.F., Mattay V.S., Hariri A.R., Weinberger D.R. 5-HTTLPR polymorphism impacts human cingulate-amygdala interactions: a genetic susceptibility mechanism for depression. Nat. Neurosci. 2005, 8:828-834.
67. Ploghaus A., Tracey I., Gati J.S., Clare S., Menon R.S., Matthews P.M., Rawlins J.N. Dissociating pain from its anticipation in the human brain. Science 1999, 284:1979-1981.
68. Rainville P., Duncan G.H., Price D.D., Carrier B., Bushnell M.C. Pain affect encoded in human anterior cingulate but not somatosensory cortex. Science 1997, 277:968-971.
69. Riley J.L.I., Robinson M.E., Wise E.A., Price D.D. A meta-analytic review of pain perception across the menstrual cycle. Pain 1999, 81:225-235.
70. Rocha A., Marques M.P., Coelho E.B., Lanchote V.L. Enantioselective analysis of citalopram and demethylcitalopram in human and rat plasma by chiral LC-MS/MS: application to pharmacokinetics. Chirality 2007, 19:793-801.
71. Serretti A., Kato M., De Ronchi D., Kinoshita T. Meta-analysis of serotonin transporter gene promoter polymorphism (5-HTTLPR) association with selective serotonin reuptake inhibitor efficacy in depressed patients. Mol. Psychiatry 2007, 12:247-257.
72. Sindrup S.H., Bjerre U., Dejgaard A., Brøsen K., Aaes-Jørgensen T., Gram L.F. The selective serotonin reuptake inhibitor citalopram relieves the symptoms of diabetic neuropathy. Clin. Pharmacol. Ther. 1992, 52:547-552.
73. Singer T., Seymour B., O'Doherty J., Kaube H., Dolan R.J., Frith C.D. Empathy for pain involves the affective but not sensory components of pain. Science 2004, 303:1157-1162.
74. Stening K., Eriksson O., Wahren L., Berg G., Hammar M., Blomqvist A. Pain sensations to the cold pressor test in normally menstruating women: comparison with men and relation to menstrual phase and serum sex steroid levels. Am. J. Phys. Regul. Integr. Comp. Phys. 2007, 293:R1711-R1716.
75. Tracey I., Mantyh P.W. The cerebral signature for pain perception and its modulation. Neuron 2007, 55:377-391.
76. Tsai S., Hong C., Cheng C. Serotonin transporter genetic polymorphisms and harm avoidance in the Chinese. Psychiatr. Genet. 2002, 12:165-168.
77. Vogel C., Mössner R., Gerlach M., Heinemann T., Murphy D.L., Riederer P., Lesch K.P., Sommer C. Absence of thermal hyperalgesia in serotonin transporter-deficient mice. J. Neurosci. 2003, 23:708-715.
78. Wager T.D., Rilling J.K., Smith E.E., Sokolik A., Casey K.L., Davidson R.J., Kosslyn S.M., Rose R.M., Cohen J.D. Placebo-induced changes in FMRI in the anticipation and experience of pain. Science 2004, 303:1162-1167.
79. Wager T.D., Atlas L.Y., Lindquist M.A., Roy M., Woo C.W., Kross E. An fMRI-based neurologic signature of physical pain. N. Engl. J. Med. 2013, 368:1388-1397.
80. Watson D., Clark L.A., Tellegen A. Development and validation of brief measures of positive and negative affect: the PANAS scales. J. Pers. Soc. Psychol. 1988, 54:1063-1070.
81. Whale R., Quested D.J., Laver D., Harrison P.J., Cowen P.J. Serotonin transporter (5-HTT) promoter genotype may influence the prolactin response to clomipramine. Psychopharmacology 2000, 150:120-122.
82. Woo C.W., Roy M., Buhle J.T., Wager T.D. Distinct brain systems mediate the effects of nociceptive input and self-regulation on pain. PLoS Biol. 2015, 13.
83. Xu X., Zuo X., Wang X., Han S. Do you feel my pain? Racial group membership modulates empathic neural responses. J. Neurosci. 2009, 29:8525-8529.
84. Zhang K., Xu Q., Xu Y., Yang H., Luo J., Sun Y., Sun N., Wang S., Shen Y. The combined effects of the 5-HTTLPR and 5-HTR1A genes modulates the relationship between negative life events and major depressive disorder in a Chinese population. J. Affect. Disord. 2009, 114:224-231.
85. Zhang L., Liu L., Li X., Song Y., Liu J. Serotonin transporter gene polymorphism (5-HTTLPR) influences trait anxiety by modulating the functional connectivity between the amygdala and insula in Han Chinese males. Hum. Brain Mapp. 2015, 10.1002/hbm.22803.
86. Zondervan K.T., Cardon L.R., Kennedy S.H., Martin N.G., Treloar S.A. Multivariate genetic analysis of chronic pelvic pain and associated phenotypes. Behav. Genet. 2005, 35:177-188.