Genetic variation in the vesicular monoamine transporter: Preliminary associations with cognitive outcomes after severe traumatic brain injury

Journal of Head Trauma Rehabilitation

Volumn 32, Issue 2, 2017, Pages E24-E34

  Markos, Steven M ^a   Failla, Michelle D ^a   Ritter, Anne C ^a   Dixon, C Edward ^a,b,c   Conley, Yvette P ^e   Ricker, Joseph H ^d   Arenth, Patricia M ^a   Juengst, Shannon B ^a   Wagner, Amy K ^a,b,c  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

^c UNIVERSITY OF PITTSBURGH   (United States)

^d NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF PITTSBURGH GRADUATE SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

Cognition; Depression; Genetic polymorphism; Rehabilomics; Traumatic brain injury; Vesicular monoamine transporter type 2 (VMAT2)

Indexed keywords

VESICULAR MONOAMINE TRANSPORTER 2; VESICULAR MONOAMINE TRANSPORTER;

ADOLESCENT; ADULT; AGE; AGED; ARTICLE; COGNITIVE DEFECT; DNA FLANKING REGION; FEMALE; GENE FREQUENCY; GENE LINKAGE DISEQUILIBRIUM; GENETIC ASSOCIATION; GENETIC VARIABILITY; GENETIC VARIATION; GENOTYPE; HOMOZYGOTE; HUMAN; INJURY SEVERITY; MAJOR CLINICAL STUDY; MALE; NEUROTRANSMISSION; SINGLE NUCLEOTIDE POLYMORPHISM; TRAUMATIC BRAIN INJURY; COHORT ANALYSIS; COMPLICATION; GENETICS; GLASGOW COMA SCALE; INJURY SCALE; MIDDLE AGED; PATHOPHYSIOLOGY; PROGNOSIS; RETROSPECTIVE STUDY; RISK ASSESSMENT; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; BRAIN INJURIES, TRAUMATIC; COGNITION DISORDERS; COHORT STUDIES; FEMALE; GENETIC VARIATION; GLASGOW COMA SCALE; HUMANS; INJURY SEVERITY SCORE; MALE; MIDDLE AGED; POLYMORPHISM, SINGLE NUCLEOTIDE; PROGNOSIS; RETROSPECTIVE STUDIES; RISK ASSESSMENT; VESICULAR MONOAMINE TRANSPORT PROTEINS; YOUNG ADULT;

EID: 85016337874     PISSN: 08859701     EISSN: 1550509X     Source Type: Journal    
DOI: 10.1097/HTR.0000000000000224     Document Type: Article

References (94)

1. Langlois JA, Rutland-BrownW,Wald MM. The epidemiology and impact of traumatic brain injury: A brief overview. J Head Trauma Rehabil. 2006;21(5):375-378.
2. Marshall S, Bayley M, McCullagh S, Velikonja D, Berrigan L. Clinical practice guidelines for mild traumatic brain injury and persistent symptoms. Can Fam Physician. 2012;58(3):257-267.
3. Cristofori I, Levin HS. Traumatic brain injury and cognition. Handb Clin Neurol. 2015;128:579-611.
4. Thurman DJ, Alverson C, Dunn KA, Guerrero J, Sniezek JE. Traumatic brain injury in theUnited States: A public health perspective. J Head Trauma Rehabil. 1999;14(6):602-6015.
5. Arciniegas DB, Held K, Wagner P. Cognitive impairment following traumatic brain injury. Curr Treat Options Neurol. 2002;4(1): 43-57.
6. Bombardier CH, Fann JR, Temkin NR, Esselman PC, Barber J, Dikmen SS. Rates of major depressive disorder and clinical outcomes following traumatic brain injury. JAMA. 2010;303(19):1938-1945.
7. Jorge RE, Robinson RG, Moser D, Tateno A, Crespo-Facorro B, Arndt S. Major depression following traumatic brain injury. Arch Gen Psychiatry. 2004;61(1):42-50.
8. Rapoport MJ, McCullagh S, Shammi P, Feinstein A. Cognitive impairment associated with major depression following mild and moderate traumatic brain injury. J Neuropsychiatry Clin Neurosci. 2005;17(1):61-65.
9. Satz P, Forney DL, Zaucha K, et al. Depression, cognition, and functional correlates of recovery outcome after traumatic brain injury. Brain Inj. 1998;12(7):537-553.
10. Failla MD, Juengst SB,Graham KM, Arenth P, Wagner AK. Effects of depression and antidepressant use on cognitive deficits and functional cognition following severe traumatic brain injury. J Head Trauma Rehabil. In Press.
11. Bornstein RA, Miller HB, van Schoor JT. Neuropsychological deficit and emotional disturbance in head-injured patients. J Neurosurg. 1989;70(4):509-513.
12. Rapoport M, McCauley S, Levin H, Song J, Feinstein A. The role of injury severity in neurobehavioral outcome 3 months after traumatic brain injury. Neuropsychiatry Neuropsychol Behav Neurol. 2002;15(2):123-132.
13. Gfeller JD, Chibnall JT, Duckro PN. Postconcussion symptoms and cognitive functioning in posttraumatic headache patients. Headache. 1994;34(9):503-507.
14. Andersson S, Bergedalen AM. Cognitive correlates of apathy in traumatic brain injury. Neuropsychiatry Neuropsychol Behav Neurol. 2002;15(3):184-191.
15. Larson EB, Zollman FS. The effect of sleep medications on cognitive recovery from traumatic brain injury. J Head Trauma Rehabil. 2010;25(1):61-67.
16. Bushnik T, Englander J, Wright J. Patterns of fatigue and its correlates over the first 2 years after traumatic brain injury. J Head Trauma Rehabil. 2008;23(1):25-32.
17. Ruhe HG, Mason NS, Schene AH. Mood is indirectly related to serotonin, norepinephrine and dopamine levels in humans: A meta-analysis of monoamine depletion studies. Mol Psychiatry. 2007;12(4):331-359.
18. Logue SF, Gould TJ. The neural and genetic basis of executive function: attention, cognitive flexibility, and response inhibition. Pharmacol Biochem Behav. 2014;123:45-54.
19. Blasi G, Mattay VS, Bertolino A, et al. Effect of catechol-Omethyltransferase val158met genotype on attentional control. J Neurosci. 2005;25(20):5038-5045.
20. Stefanis NC, van Os J, Avramopoulos D, Smyrnis N, Evdokimidis I, Stefanis CN. Effect of COMT Val158Met polymorphism on the Continuous Performance Test, Identical PairsVersion: tuning rather than improving performance. Am J Psychiatry. 2005;162(9):1752-174.
21. Stelzel C, Basten U, Montag C, Reuter M, Fiebach CJ. Frontostriatal involvement in task switching depends on genetic differences in d2 receptor density. J Neurosci. 2010;30(42):14205-14212.
22. Kramer UM, Rojo N, Schüle R, et al. ADHD candidate gene (DRD4 exon III) affects inhibitory control in a healthy sample. BMC Neurosci. 2009;10:150.
23. Nomura M, Kusumi I, Kaneko M, et al. Involvement of a polymorphism in the 5-HT2A receptor gene in impulsive behavior. Psychopharmacology (Berl). 2006;187(1):30-35.
24. Bales JW, Wagner AK, Kline AE, Dixon CE. Persistent cognitive dysfunction after traumatic brain injury: A dopamine hypothesis. Neurosci Biobehav Rev. 2009;33(7):981-1003.
25. Donnemiller E, Brenneis C, Wissel J, et al. Impaired dopaminergic neurotransmission in patients with traumatic brain injury: A SPECT study using 123I-beta-CIT and 123I-IBZM. Eur J Nucl Med. 2000;27(9):1410-1414.
26. Wagner AK, Scanlon JM, Becker CR, et al. The influence of genetic variants on striatal dopamine transporter and D2 receptor binding after TBI. J Cereb Blood Flow Metab. 2014;34(8):1328-1339.
27. Henry JM, Talukder NK, Lee AB Jr,Walker ML. Cerebral traumainduced changes in corpus striatal dopamine receptor subtypes. J Invest Surg. 1997;10(5):281-286.
28. Yan HQ, Kline AE, Ma X, Hooghe-Peters EL, Marion DW, Dixon CE. Tyrosine hydroxylase, but not dopamine beta-hydroxylase, is increased in rat frontal cortex after traumatic brain injury. Neuroreport. 2001;12(11):2323-2327.
29. Seeman P, Tedesco JL, Lee T, et al. Dopamine receptors in the central nervous system. Fed Proc. 1978;37(2):131-136.
30. Baron JC, Comar D, Zarifian E, et al. Dopaminergic receptor sites in human brain: positron emission tomography. Neurology. 1985;35(1):16-24.
31. McDonald BC, Flashman LA, Saykin AJ. Executive dysfunction following traumatic brain injury: neural substrates and treatment strategies. Neurorehabilitation. 2002;17(4):333-344.
32. Erickson JD, SchaferMK, Bonner TI, Eiden LE, Weihe E. Distinct pharmacological properties and distribution in neurons and endocrine cells of two isoforms of the human vesicular monoamine transporter. Proc Natl Acad Sci U S A. 1996;93(10):5166-5171.
33. Sager JJ, Torres GE. Proteins interacting with monoamine transporters: current state and future challenges. Biochemistry. 2011;50(34):7295-7310.
34. Wimalasena K. Vesicular monoamine transporters: structurefunction, pharmacology, and medicinal chemistry. Med Res Rev. 2011;31(4):483-519.
35. Hanson GR, Sandoval V, Riddle E, Fleckenstein AE. Psychostimulants and vesicle trafficking: A novel mechanism and therapeutic implications. Ann N Y Acad Sci. 2004;1025:146-150.
36. Fehr C, Sommerlad D, Sander T, et al. Association of VMAT2 gene polymorphisms with alcohol dependence. J Neural Transm. 2013;120(8):1161-119.
37. Zai CC, Tiwari AK, Mazzoco M, et al. Association study of the vesicular monoamine transporter gene SLC18A2 with tardive dyskinesia. J Psychiatr Res. 2013;47(11):1760-1765.
38. Brighina L, Riva C, Bertola F, et al. Analysis of vesicular monoamine transporter 2 polymorphisms in Parkinson's disease. Neurobiol Aging. 2013;34(6):1712.e9-13.
39. Yang X, Xu P, Zhao Q, et al. Polymorphism in the vesicular monoamine transporter 2 gene decreases the risk of Parkinson's disease in Han Chinese men. Parkinsons Dis. 2015;2015: 903164.
40. Glatt CE, Wahner AD, White DJ, Ruiz-Linares A, Ritz B. Gainof-function haplotypes in the vesicular monoamine transporter promoter are protective for Parkinson disease in women. Hum Mol Genet. 2006;15(2):299-305.
41. Wagner AK. TBI translational rehabilitation research in the 21st Century: exploring a Rehabilomics research model. Eur J Phys Rehabil Med. 2010;46(4):549-556.
42. Wagner AK, Hammond FM, Sasser HC, Wiercisiewski D, Norton HJ. Use of injury severity variables in determining disability and community integration after traumatic brain injury. J Trauma. 2000;49(3):411-419.
43. Wagner AK, Amin KB, Niyonkuru C, et al. CSF Bcl-2 and cytochrome C temporal profiles in outcome prediction for adults with severe TBI. J Cereb Blood Flow Metab. 2011;31(9):1886-1896.
44. Wagner AK, McCullough EH, Niyonkuru C, et al. Acute serum hormone levels: characterization and prognosis after severe traumatic brain injury. J Neurotrauma. 2011;28(6):871-888.
45. Wagner AK, Hammond FM, Grigsby JH, Norton HJ. The value of trauma scores: predicting discharge after traumatic brain injury. Am J PhysMed Rehabil. 2000;79(3):235-242.
46. Udekwu P, Kromhout-Schiro S, Vaslef S, Baker C, Oller D. Glasgow Coma Scale score,mortality, and functional outcome in headinjured patients. J Trauma. 2004;56(5):1084-1089.
47. Cifu DX, Keyser-Marcus L, Lopez E, et al. Acute predictors of successful return to work 1 year after traumatic brain injury: A multicenter analysis. Arch Phys Med Rehabil. 1997;78(2):125-131.
48. Dawson JD, Uc EY, Anderson SW, Johnson AM, Rizzo M. Neuropsychological predictors of driving errors in older adults. J Am Geriatr Soc. 2010;58(6):1090-1096.
49. Green RE, Colella B, Christensen B, et al. Examining moderators of cognitive recovery trajectories aftermoderate to severe traumatic brain injury. Arch Phys Med Rehabil. 2008;89(12 Suppl):S16-S24.
50. van Veelen NM, Grootens KP, Peuskens J, et al. Short-term neurocognitive effects of treatment with ziprasidone and olanzapine in recent onset schizophrenia. Schizophr Res. 2010;120(1-3):191-198.
51. Bell KR, Temkin NR, Esselman PC, et al. The effect of a scheduled telephone intervention on outcome after moderate to severe traumatic brain injury: A randomized trial. Arch Phys Med Rehabil. 2005;86(5):851-856.
52. Wagner AK, Brett CA, McCullough EH, et al. Persistent hypogonadism influences estradiol synthesis, cognition and outcome in males after severe TBI. Brain Inj. 2012;26(10):1226-1242.
53. Larrabee GJ, Curtiss G. Construct validity of various verbal and visual memory tests. J Clin Exp Neuropsychol. 1995;17(4):536-547.
54. Borkowski JG, Benton AL, Spreen O. Word fluency and brain damage. Neuropsychologia. 1967;5(2):135-140.
55. Delis DC, Kramer JH. California Verbal Learning Test. Psychological Corporation; 2000.
56. Reitan RM,Wolfson D. The Halstead-Reitan Neuropsychological Test Battery: Theory and Clinical Interpretation. Neuropsychology Press; 1985.
57. Trenerry MR. Stroop Neuropsychological Screening Test Manual. Psychological Assessment Resources; 1989.
58. Keith RA, Granger CV, Hamilton BB, Sherwin FS. The functional independence measure: A new tool for rehabilitation. Adv Clin Rehabil. 1987;1:6-18.
59. Kroenke K, Spitzer RL,Williams JB. The PHQ-9: validity of a brief depression severity measure. JGen Intern Med. 2001;16(9):606-613.
60. Hart T, Hoffman JM, Pretz C, Kennedy R, Clark AN, Brenner LA. A longitudinal study of major and minor depression following traumatic brain injury. Arch Phys Med Rehabil. 2012;93(8):1343-1349.
61. Fann JR, Bombardier CH, Dikmen S, et al. Validity of the Patient Health Questionnaire-9 in assessing depression following traumatic brain injury. J Head Trauma Rehabil. 2005;20(6):501-511.
62. Comings DE, MacMurray JP. Molecular heterosis: A review. Mol GenetMetab. 2000;71(1-2):19-31.
63. Miller SA, Dykes DD, Polesky HF. A simple salting out procedure for extracting DNA from human nucleated cells. NucleicAcids Res. 1988;16(3):1215.
64. Barrett JC, Fry B, Maller J, Daly MJ. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics. 2005;21(2):263-265.
65. Li J, Ji L. Adjusting multiple testing in multilocus analyses using the eigenvalues of a correlation matrix. Heredity (Edinb). 2005;95(3):221-227.
66. Failla MD, Burkhardt JN, Miller MA, et al. Variants of SLC6A4 in depression risk following severe TBI. Brain Inj. 2013;27(6):696-706.
67. Darrah SD, Miller MA, Ren D, et al. Genetic variability in glutamic acid decarboxylase genes: associations with posttraumatic seizures after severe TBI. Epilepsy Res. 2013;103(2-3):180-194.
68. Gao WM, Chadha MS, Kline AE, et al. Immunohistochemical analysis of histone H3 acetylation and methylation-evidence for altered epigenetic signaling following traumatic brain injury in immature rats. Brain Res. 2006;1070(1):31-34.
69. NCBI. Reference SNP (refSNP) Cluster Report: rs3632260. http://www.ncbi.nlm.nih.gov/SNP/snp ref.cgi?rs=rs363226. Accessed September 27, 2015.
70. Ward LD, Kellis M. HaploReg: A resource for exploring chromatin states, conservation, and regulatory motif alterations within sets of genetically linked variants. Nucleic Acids Res. 2012;40(Database issue):D930-D934.
71. Eiden LE, Weihe E. VMAT2: A dynamic regulator of brain monoaminergic neuronal function interacting with drugs of abuse. Ann N Y Acad Sci. 2011;1216:86-98.
72. Narendran R, Lopresti BJ, Martinez D, et al. In vivo evidence for low striatal vesicular monoamine transporter 2 (VMAT2) availability in cocaine abusers. Am J Psychiatry. 2012;169(1):55-63.
73. Vergo S, Johansen JL, Leist M, Lotharius J. Vesicular monoamine transporter 2 regulates the sensitivity of rat dopaminergic neurons to disturbed cytosolic dopamine levels. Brain Res. 2007;1185:18-32.
74. Cruz-Muros I, Afonso-Oramas D, Abreu P, Rodríguez M, González MC, González-Hernández T. Deglycosylation and subcellular redistribution of VMAT2 in themesostriatal system during normal aging. Neurobiol Aging. 2008;29(11):1702-1711.
75. Lin Z, Zhao Y, Chung CY, et al. High regulatability favors genetic selection in SLC18A2, a vesicular monoamine transporter essential for life. Faseb J. 2010;24(7):2191-200.
76. Lin Z, Walther D, Yu XY, Li S, Drgon T, Uhl GR. SLC18A2 promoter haplotypes and identification of a novel protective factor against alcoholism. HumMol Genet. 2005;14(10):1393-1404.
77. Cartier EA, Parra LA, Baust TB, et al. A biochemical and functional protein complex involving dopamine synthesis and transport into synaptic vesicles. J Biol Chem. 2010;285(3):1957-1966.
78. Kim ST, Choi JH, Chang JW, Kim SW, Hwang O. Immobilization stress causes increases in tetrahydrobiopterin, dopamine, and neuromelanin and oxidative damage in the nigrostriatal system. J Neurochem. 2005;95(1):89-98.
79. Wagner AK, Ren D, Conley YP, et al. Sex and genetic associations with cerebrospinal fluid dopamine and metabolite production after severe traumatic brain injury. JNeurosurg. 2007;106(4):538-547.
80. Renner C, Hummelsheim H, Kopczak A, et al. The influence of gender on the injury severity, course and outcome of traumatic brain injury. Brain Inj. 2012;26(11):1360-1371.
81. Utomo WK, Gabbe BJ, Simpson PM, Cameron PA. Predictors of in-hospital mortality and 6-month functional outcomes in older adults after moderate to severe traumatic brain injury. Injury. 2009;40(9):973-977.
82. Nelson DW, Rudehill A, MacCallum RM, et al. Multivariate outcome prediction in traumatic brain injury with focus on laboratory values. J Neurotrauma. 2012;29(17):2613-2624.
83. Ponsford JL, Myles PS, Cooper DJ, et al. Gender differences in outcome in patients with hypotension and severe traumatic brain injury. Injury. 2008;39(1):67-76.
84. Farace E, Alves WM. Do women fare worse? A metaanalysis of gender differences in outcome after traumatic brain injury. Neurosurg Focus. 2000;8(1):e6.
85. Brown SB, Colantonio A, Kim H. Gender differences in discharge destination among older adults following traumatic brain injury. Health Care Women Int. 2012;33(10):896-904.
86. Ponsford J. Factors contributing to outcome following traumatic brain injury. Neurorehabilitation. 2013;32(4):803-815.
87. Mosenthal AC, Lavery RF, AddisM, et al. Isolated traumatic brain injury: age is an independent predictor of mortality and early outcome. J Trauma. 2002;52(5):907-911.
88. Draper K, Ponsford J, SchonbergerM. Psychosocial and emotional outcomes 10 years following traumatic brain injury. JHeadTrauma Rehabil. 2007;22(5):278-287.
89. Crownover J, Galang G, Wagner A. Rehabilitation considerations for traumatic brain injury in the geriatric population: epidemiology, neurobiology, prognosis, and management. Curr Transl Geriatr Exp Gerontol Rep. 2012;1(3):149-158.
90. Pedroli E, Cipresso P, Serino S, Pallavicini F, Albani G, Riva G. Virtual Multiple Errands Test: reliability, usability and possible applications. Stud Health Technol Inform. 2013;191: 38-42.
91. Alderman N, Burgess PW, Knight C, Henman C. Ecological validity of a simplified version of the multiple errands shopping test. J Int Neuropsychol Soc. 2003;9(1):31-44.
92. Olsen AS, Sozda CN, Cheng JP, Hoffman AN, Kline AE. Traumatic brain injury-induced cognitive and histological deficits are attenuated by delayed and chronic treatment with the 5-HT1A-receptor agonist buspirone. J Neurotrauma. 2012;29(10): 1898-1907.
93. Davidson J, Cusimano MD, Bendena WG. Post-traumatic brain injury: genetic susceptibility to outcome. Neuroscientist. 2015;21(4):424-441.
94. Myrga JM, Failla MD, Ricker JH, et al. A dopamine pathway gene risk score for cognitive recovery following traumatic brain injury: methodological considerations, preliminary findings, and interactions with sex [published online ahead of print November 17, 2015]. J Head Trauma Rehabil. doi: 10.1097/HTR.0000000000000199.