A Risk PRODH Haplotype Affects Sensorimotor Gating, Memory, Schizotypy, and Anxiety in Healthy Male Subjects

Biological Psychiatry

Volumn 65, Issue 12, 2009, Pages 1063-1070

  Roussos, Panos ^a   Giakoumaki, Stella G ^a   Bitsios, Panos ^a  

^a UNIVERSITY OF CRETE   (Greece)

Author keywords

Prepulse inhibition; PRODH; schizotypy; trait anxiety; verbal memory; working memory

Indexed keywords

ADENINE; CYTOSINE; GUANINE; PROLINE DEHYDROGENASE;

ADULT; ANXIETY; ARTICLE; CONTROLLED STUDY; GENETIC ASSOCIATION; GENETIC PREDISPOSITION; GENETIC RISK; GENETIC TRAIT; HAPLOTYPE; HETEROZYGOTE; HUMAN; MALE; PHENOTYPE; PRIORITY JOURNAL; PSYCHOSIS; RISK ASSESSMENT; SCHIZOPHRENIA; SENSORIMOTOR FUNCTION; SINGLE NUCLEOTIDE POLYMORPHISM; VERBAL MEMORY; WORKING MEMORY;

ADULT; ANXIETY; COHORT STUDIES; GENE FREQUENCY; GENOTYPE; HAPLOTYPES; HUMANS; MALE; MEMORY; MEMORY, SHORT-TERM; PROLINE OXIDASE; QUESTIONNAIRES; SCHIZOTYPAL PERSONALITY DISORDER; STARTLE REACTION; VERBAL LEARNING;

EID: 67349160223     PISSN: 00063223     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biopsych.2009.01.003     Document Type: Article

References (101)

1. Karayiorgou M., and Gogos J.A. The molecular genetics of the 22q11-associated schizophrenia. Brain Res 132 (2004) 95-104
2. Xu B., Roos J.L., Levy S., van Rensburg E.J., Gogos J.A., and Karayiorgou M. Strong association of de novo copy number mutations with sporadic schizophrenia. Nat Genet 40 (2008) 880-885
3. The International Schizophrenia Consortium. Rare chromosomal deletions and duplications increase risk of schizophrenia. Nature 455 (2008) 237-241
4. Gogos J.A., Santha M., Takacs Z., Beck K.D., Luine V., Lucas L.R., et al. The gene encoding proline dehydrogenase modulates sensorimotor gating in mice. Nat Genet 21 (1999) 434-439
5. Pearlson G.D. Neurobiology of schizophrenia. Ann Neurol 48 (2000) 556-566
6. Liu H., Abecasis G.R., Heath S.C., Knowles A., Demars S., Chen Y.J., et al. Genetic variation in the 22q11 locus and susceptibility to schizophrenia. PNAS 99 (2002) 16859-16864
7. Liu H., Heath S.C., Sobin C., Roos J.L., Galke B.L., Blundell M.L., et al. Genetic variation at the 22q11 PRODH2/DGCR6 locus presents an unusual pattern and increases susceptibility to schizophrenia. PNAS 99 (2002) 3717-3722
8. Li T., Ma X., Sham P.C., Sun X., Hu X., Wang Q., et al. Evidence for association between novel polymorphisms in the PRODH gene and schizophrenia in a Chinese population. Am J Med Genet B Neuropsychiatr Genet 129B (2004) 13-15
9. Li T., Ma X., Hu X., Wang Y., Yan C., Meng H., et al. PRODH gene is associated with executive function in schizophrenic families. Am J Med Genet B Neuropsychiatr Genet 147B (2008) 654-657
10. Fan J.B., Ma J., Zhang C.S., Tang J.X., Gu N.F., Feng G.Y., et al. A family-based association study of T1945C polymorphism in the proline dehydrogenase gene and schizophrenia in the Chinese population. Neurosci Lett 338 (2003) 252-254
11. Williams H.J., Williams N., Spurlock G., Norton N., Ivanov D., McCreadie R.G., et al. Association between PRODH and schizophrenia is not confirmed. Mol Psychiatry 8 (2003) 644-645
12. Glaser B., Moskvina V., Kirov G., Murphy K.C., Williams H., Williams N., et al. Analysis of ProDH, COMT and ZDHHC8 risk variants does not support individual or interactive effects on schizophrenia susceptibility. Schizophr Res 87 (2006) 21-27
13. Paterlini M., Zakharenko S.S., Lai W.S., Qin J., Zhang H., Mukai J., et al. Transcriptional and behavioral interaction between 22q11.2 orthologs modulates schizophrenia-related phenotypes in mice. Nat Neurosci 8 (2005) 1586-1594
14. Braff D.L., and Geyer M.A. Sensorimotor gating and schizophrenia. Human and animal model studies. Arch Gen Psychiatry 47 (1990) 181-188
15. Sitskoorn M.M., Aleman A., Ebisch S.J., Appels M.C., and Kahn R.S. Cognitive deficits in relatives of patients with schizophrenia: A meta-analysis. Schizophr Res 71 (2004) 285-295
16. Sobin C., Kiley-Brabeck K., and Karayiorgou M. Associations between prepulse inhibition and executive visual attention in children with the 22q11 deletion syndrome. Mol Psychiatry 10 (2005) 553-562
17. Braff D.L., and Light G.A. The use of neurophysiological endophenotypes to understand the genetic basis of schizophrenia. Dial Clin Neurosci 7 (2005) 125-135
18. Anokhin A.P., Heath A.C., Myers E., Ralano A., and Wood S. Genetic influences on prepulse inhibition of startle reflex in humans. Neurosci Lett 353 (2003) 45-48
19. Cadenhead K.S., Swerdlow N.R., Shafer K.M., Diaz M., and Braff D.L. Modulation of the startle response and startle laterality in relatives of schizophrenic patients and in subjects with schizotypal personality disorder: Evidence of inhibitory deficits. Am J Psychiatry 157 (2000) 1660-1668
20. Hong L.E., Wonodi I., Stine O.C., Mitchell B.D., and Thaker G.K. Evidence of missense mutations on the neuregulin 1 gene affecting function of prepulse inhibition. Biol Psychiatry 63 (2008) 17-23
21. Roussos P., Giakoumaki S.G., Rogdaki M., Pavlakis S., Frangou S., and Bitsios P. Prepulse inhibition of the startle reflex depends on the catechol O-methyltransferase Val158Met gene polymorphism. Psychol Med 8 (2008) 1-8
22. Roussos P., Giakoumaki S.G., and Bitsios P. The dopamine D(3) receptor Ser9Gly polymorphism modulates prepulse inhibition of the acoustic startle reflex. Biol Psychiatry 64 (2008) 235-240
23. Snitz B.E., Macdonald A.W., and Carter C.S. Cognitive deficits in unaffected first-degree relatives of schizophrenia patients: A meta-analytic review of putative endophenotypes. Schizophr Bull 32 (2006) 179-194
24. Fanous A.H., and Kendler K.S. The genetic relationship of personality to major depression and schizophrenia. Neurotoxicity Res 6 (2004) 43-50
25. Lewandowski K.E., Barrantes-Vidal N., Nelson-Gray R.O., Clancy C., Kepley H.O., and Kwapil T.R. Anxiety and depression symptoms in psychometrically identified schizotypy. Schizophr Res 83 (2006) 225-235
26. Yung A.R., Phillips L.J., Yuen H.P., Francey S.M., McFarlane C.A., Hallgren M., et al. Psychosis prediction: 12-month follow up of a high-risk ("prodromal") group. Schizophr Res 60 (2003) 21-32
27. Pritchard J.K., Stephens M., and Donnelly P. Inference of population structure using multilocus genotype data. Genetics 155 (2000) 945-959
28. Sheehan D.V., Lecrubier Y., Sheehan K.H., Amorim P., Janavs J., and Weiller E. The Mini-International Neuropsychiatric Interview (M.I.N.I.): The development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. J Clin Psychiatry 59 (1998) 22-33
29. Maxwell M.E. Manual for the FIGS (1992), National Institute of Mental Health, Bethesda, MD
30. Wechsler D. WAIS-III WMS-III: Technical manual (1997), Psychological Corporation, San Antonio, TX
31. Giakoumaki S.G., Roussos P., and Bitsios P. Improvement of prepulse inhibition and executive function by the COMT inhibitor tolcapone depends on COMT Val158Met polymorphism. [published online ahead of print June 4]. Neuropsychopharmacology (2008) doi:10.1038/npp.2008.82
32. Claridge G.S., and Broks P. Schizotypy and hemisphere function: I. Theoretical considerations and the measurement of schizotypy. Pers Individ Diff 5 (1984) 633-648
33. Spielberger C.D. Manual for the state-trait anxiety inventory (1983), Consulting Psychologists Press, Palo Alto, CA
34. Kelley M.P., and Coursey R.D. Factor structure of schizotypy scales. Pers Individ Diff 13 (1992) 723-731
35. Barrett J.C., Fry B., Maller J., and Daly M.J. Haploview: Analysis and visualization of LD and haplotype maps. Bioinformatics 21 (2005) 263-265
36. Dudbridge F. Pedigree disequilibrium tests for multilocus haplotypes. Genet Epidemiol 25 (2003) 115-121
37. Benjamini Y., and Hochberg Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J R Stat Soc 57 (1995) 289-300
38. So H.C., Chen R.Y., Chen E.Y., Cheung E.F., Li T., and Sham P.C. An association study of RGS4 polymorphisms with clinical phenotypes of schizophrenia in a Chinese population. Am J Med Genet B Neuropsychiatr Genet 147B (2008) 77-85
39. Brewer W.J., Francey S.M., Wood S.J., Jackson H.J., Pantelis C., Phillips L.J., et al. Memory impairments identified in people at ultra-high risk for psychosis who later develop first-episode psychosis. Am J Psychiatry 162 (2005) 71-78
40. Claridge G. Theoretical background issues. In: Claridge G. (Ed). Schizotypy: Implications for Illness and Health (1997), Oxford University Press, Oxford 3-18
41. Andreasen N.C. A unitary model of schizophrenia: Bleuler's "fragmented phrene" as schizencephaly. Arch Gen Psychiatry 56 (1999) 781-787
42. Huppert J.D., and Smith T.E. Anxiety and schizophrenia: The interaction of subtypes of anxiety and psychotic symptoms. CNS Spectrums 10 (2005) 721-731
43. Hazlett H., Dawson M.E., Schell A.M., and Nuechterlein K.H. Electrodermal activity as a prodromal sign in schizophrenia. Biol Psychiatry 41 (1997) 111-113
44. Giakoumaki S.G., Bitsios P., and Frangou S. The level of prepulse inhibition in healthy individuals may index cortical modulation of early information processing. Brain Res 1078 (2006) 168-170
45. Bitsios P., Giakoumaki S.G., Theou K., and Frangou S. Increased prepulse inhibition of the acoustic startle response is associated with better strategy formation and execution times in healthy males. Neuropsychologia 44 (2006) 2494-2499
46. Light G.A., Braff D.L., Sprock J., Cadenhead K.S., and Swerdlow N.R. Prepulse inhibition of startle is positively associated with higher order cognition in women. Abstr Soc Neurosciences (2007) 806.17
47. Venables P. Input dysfunction in schizophrenia. In: Maher B.A. (Ed). Progress in Experimental Personality Research (1964), Academic Press, Orlando, FL
48. Frith C.D. Consciousness, information processing and schizophrenia. Br J Psychiatry 134 (1979) 225-235
49. Bishop S.J. Neurocognitive mechanisms of anxiety: An integrative account. Trends Cogn Sci 11 (2007) 307-316
50. Mohanty A., Heller W., Koven N.S., Fisher J.E., Herrington J.D., and Miller G.A. Specificity of emotion-related effects on attentional processing in schizotypy. Schizophrenia Res 103 (2008) 129-137
51. Mujica-Parodi L.R., Malaspina D., and Sackeim H.A. Logical processing, affect, and delusional thought in schizophrenia. Harv Rev Psychiatry 8 (2000) 73-83
52. Geyer M.A. The family of sensorimotor gating disorders: Comorbidities or diagnostic overlaps?. Neurotox Res 10 (2006) 211-220
53. Cavanna A.E., Robertson M.M., and Critchley H.D. Schizotypal personality traits in Gilles de la Tourette syndrome. Acta Neurol Scand 116 (2007) 385-391
54. Sobesky W.E., Hull C.E., and Hagerman R.J. Symptoms of schizotypal personality disorder in fragile X women. J Am Acad Child Adolesc Psychiatry 33 (1994) 247-255
55. Marshall J., White K., Weaver M., Flury Wetherill L., Hui S., et al. Specific psychiatric manifestations among preclinical Huntington disease mutation carriers. Arch Neurol 64 (2007) 116-121
56. Sobin C., Blundell M.L., Weiller F., Gavigan C., Haiman C., and Karayiorgou M. Evidence of a schizotypy subtype in OCD. J Psychiatr Res 34 (2000) 15-24
57. Einstein D.A., and Menzies R.G. Role of magical thinking in obsessive-compulsive symptoms in an undergraduate sample. Depress Anxiety 19 (2004) 174-179
58. Lee H.J., Cougle J.R., and Telch M.J. Thought-action fusion and its relationship to schizotypy and OCD symptoms. Behav Res Ther 43 (2005) 29-41
59. Poyurovsky M., and Koran L.M. Obsessive-compulsive disorder (OCD) with schizotypy vs. schizophrenia with OCD: Diagnostic dilemmas and therapeutic implications. J Psychiatr Res 39 (2005) 399-408
60. Holmes E.A., and Steel C. Schizotypy: A vulnerability factor for traumatic intrusions. J Nerv Ment Dis 192 (2004) 28-34
61. Marzillier S.L., and Steel C. Positive schizotypy and trauma-related intrusions. J Nerv Ment Dis 195 (2007) 60-64
62. Steel C., Mahmood M., and Holmes E.A. Positive schizotypy and trait dissociation as vulnerability factors for post-traumatic distress. Br J Clin Psychol 47 Pt 2 (2008) 245-249
63. Filion D.L., Dawson M.E., and Schell A.M. Modification of the acoustic startle-reflex eyeblink: A tool for investigating early and late attentional processes. Biol Psychol 35 (1993) 185-200
64. Kumari V., Antonova E., and Geyer M.A. Prepulse inhibition and "psychosis-proneness" in healthy individuals: An fMRI study. Eur Psychiatry 23 (2008) 274-280
65. Swerdlow N.R., Filion D., Geyer M.A., and Braff D.L. "Normal" personality correlates of sensorimotor, cognitive, and visuospatial gating. Biol Psychiatry 37 (1995) 286-299
66. Simons R.F., and Giardina B.D. Reflex modification in psychosis-prone young adults. Psychophysiology 29 (1992) 8-16
67. Kumari V., Toone B., and Gray J.A. Habituation and prepulse inhibition of the acoustic startle reflex: effects of smoking status and psychosis-proneness. Pers Individ Dif 23 (1997) 183-191
68. Evans L.H., Gray N.S., and Snowden R.J. Prepulse inhibition of startle and its moderation by schizotypy and smoking. Psychophysiology 42 (2005) 223-231
69. Blumenthal T.D., and Creps C.L. Normal startle responding in psychosis-prone college students. Pers Individ Dif 17 (1994) 345-355
70. Lipp O.V., Siddle D.A.T., and Arnold S.L. Psychosis proneness in a non-clinical sample II: A multi-experimental study of "attentional malfunctioning.". Pers Individ Dif 17 (1994) 405-424
71. Cadenhead K., Kumar C., and Braff D. Clinical and experimental characteristics of "hypothetically psychosis prone" college students. J Psychiatr Res 30 (1996) 331-340
72. Swerdlow N.R., Geyer M.A., and Braff D.L. Neural circuit regulation of prepulse inhibition of startle in the rat: Current knowledge and future challenges. Psychopharmacology 156 (2001) 194-215
73. Geyer M.A., Swerdlow N.R., Mansbach R.S., and Braff D. Startle response models of sensorimotor gating and habituation deficits in schizophrenia. Brain Res Bull 25 (1990) 485-498
74. Perry W., and Braff D.L. Information-processing deficits and thought disorder in schizophrenia. Am J Psychiatry 151 (1994) 363-367
75. Perry W., Geyer M.A., and Braff D.L. Sensorimotor gating and thought disturbance measured in close temporal proximity in schizophrenic patients. Arch Gen Psychiatry 56 (1999) 277-281
76. Karper L.P., Freeman G.K., Grillon C., Morgan III C.A., Charney D.S., and Krystal J.H. Preliminary evidence of an association between sensorimotor gating and distractibility in psychosis. J Neuropsychiatry Clin Neurosci 8 (1996) 60-66
77. Goldman-Rakic P.S., and Selemon L.D. Functional and anatomical aspects of prefrontal pathology in schizophrenia. Schizophr Bull 23 (1997) 437-458
78. Bast T., and Feldon J. Hippocampal modulation of sensorimotor processes. Progr Neurobiol 70 (2003) 319-345
79. Wedzony K., Fijal K., Mackowiak M., Chocyk A., and Zajaczkowski W. Impact of postnatal blockade of N-methyl-d-aspartate receptors on rat behavior: A search for a new developmental model of schizophrenia. Neurosci 153 (2008) 1370-1379
80. Bender H.U., Almashanu S., Steel G., Hu C.A., Lin W.W., Willis A., et al. Functional consequences of PRODH missense mutations. Am J Hum Genet 76 (2005) 409-420
81. Phang J.M., Donald S.P., Pandhare J., and Liu Y. The metabolism of proline, a stress substrate, modulates carcinogenic pathways. Amino Acids 35 (2008) 681-690
82. Sauna Z.E., Kimchi-Sarfaty C., Ambudkar S.V., and Gottesman M.M. Silent polymorphisms speak: How they affect pharmacogenomics and the treatment of cancer. Cancer Res 67 (2007) 9609-9612
83. Choi D.W. Glutamate neurotoxicity and diseases of the nervous system. Neuron 1 (1988) 623-634
84. Ghiani C.A., Beltran-Parrazal L., Sforza D.M., Malvar J.S., Seksenyan A., Cole R., et al. Genetic program of neuronal differentiation and growth induced by specific activation of NMDA receptors. Neurochem Res 32 (2007) 363-376
85. Tibbo P., Hanstock C., Valiakalayil A., and Allen P. 3-T proton MRS investigation of glutamate and glutamine in adolescents at high genetic risk for schizophrenia. Am J Psychiatry 161 (2004) 1116-1118
86. Ohrmann P., Siegmund A., Suslow T., Pedersen A., Spitzberg K., Kersting A., et al. Cognitive impairment and in vivo metabolites in first-episode neuroleptic-naive and chronic medicated schizophrenic patients: A proton magnetic resonance spectroscopy study. J Psychiat Res 4 (2007) 625-634
87. Purdon S.E., Valiakalayil A., Hanstock C.C., Seres P., and Tibbo P. Elevated 3T proton MRS glutamate levels associated with poor Continuous Performance Test (CPT-0X) scores and genetic risk for schizophrenia. Schizophr Res 99 (2008) 218-224
88. Glantz L.A., Gilmore J.H., Lieberman J.A., and Jarskog L.F. Apoptotic mechanisms and the synaptic pathology of schizophrenia. Schizophr Res 81 (2006) 47-63
89. Wang C., McInnis J., Ross-Sanchez M., Shinnick-Gallagher P., Wiley J.L., and Johnson K.M. Long-term behavioral and neurodegenerative effects of perinatal phencyclidine administration: Implications for schizophrenia. Neurosci 107 (2001) 535-550
90. Wang C., McInnis J., West J.B., Bao J., Anastasio N., Guidry J.A., et al. Blockade of phencyclidine-induced cortical apoptosis and deficits in prepulse inhibition by M40403, a superoxide dismutase mimetic. J Pharmacol Exp Ther 304 (2003) 266-271
91. Abekawa T., Ito K., Nakagawa S., Nakato Y., and Koyama T. Olanzapine and risperidone block a high dose of methamphetamine-induced schizophrenia-like behavioral abnormalities and accompanied apoptosis in the medial prefrontal cortex. Schizophr Res 101 (2008) 84-94
92. Harris L.W., Sharp T., Gartlon J., Jones D.N., and Harrison P.J. Long-term behavioural, molecular and morphological effects of neonatal NMDA receptor antagonism. Eur J Neurosci 18 (2003) 1706-1710
93. Grottick A.J., Bagnol D., Phillips S., McDonald J., Behan D.P., Chalmers D.T., et al. Neurotransmission- and cellular stress-related gene expression associated with prepulse inhibition in mice. Brain Res 139 (2005) 153-162
94. Morgan C.J., and Curran H.V. Acute and chronic effects of ketamine upon human memory: A review. Psychopharmacology 188 (2006) 408-424
95. Bubenikova-Valesova V., Horacek J., Vrajova M., and Hoschl C. Models of schizophrenia in humans and animals based on inhibition of NMDA receptors. Neurosci Biobehav Rev 32 (2008) 1014-1023
96. Hovatta I., Tennant R.S., Helton R., Marr R.A., Singer O., Redwine J.M., et al. Glyoxalase 1 and glutathione reductase 1 regulate anxiety in mice. Nature 438 (2005) 662-666
97. Mathew S.J., Price R.B., and Charney D.S. Recent advances in the neurobiology of anxiety disorders: Implications for novel therapeutics. Am J Med Genet 148 (2008) 89-98
98. Phan K.L., Fitzgerald D.A., Cortese B.M., Seraji-Bozorgzad N., Tancer M.E., and Moore G.J. Anterior cingulate neurochemistry in social anxiety disorder: 1H-MRS at 4 Tesla. Neuroreport 16 (2005) 183-186
99. Maynard T.M., Haskell G.T., Peters A.Z., Sikich L., Lieberman J.A., and LaMantia A.S. A comprehensive analysis of 22q11 gene expression in the developing and adult brain. Proc Natl Acad Sci U S A 100 (2003) 14433-14438
100. Kempf L., Nicodemus K.K., Kolachana B., Vakkalanka R., Verchinkski B.A., and Egan M.F. Functional polymorphisms in PRODH are associated with risk and protection for schizophrenia and fronto-striatal structure and function. [published online ahead of print November 7]. PLoS Genet 4 (2008) e1000252 DOI: 10.1371/journal.pgen.1000252
101. Chapman L.J., Chapman J.P., Kwapil T.R., Eckblad M., and Zinser M.C. Putatively psychosis-prone subjects 10 years later. J Abnorm Psychol 103 (1994) 171-183