Investigation of endocannabinoid system genes suggests association between peroxisome proliferator activator receptor-α gene (PPARA) and schizophrenia

European Neuropsychopharmacology

Volumn 23, Issue 7, 2013, Pages 749-759

  Costa, Marta ^a   Squassina, Alessio ^a   Congiu, Donatella ^a   Chillotti, Caterina ^b   Niola, Paola ^a   Galderisi, Silvana ^c   Pistis, Marco ^a   Del Zompo, Maria ^a,b  

^a UNIVERSITY OF CAGLIARI   (Italy)

^b University Hospital Agency of Cagliari (AOUCA)   (Italy)

^c SECOND UNIVERSITY OF NAPLES   (Italy)

Author keywords

Cannabinoid system; CNR1; FAAH; NAPE PLD; PPARA; Schizophrenia

Indexed keywords

CANNABINOID 1 RECEPTOR; ENDOCANNABINOID; FATTY ACID AMIDASE; N ACYLPHOSPHATIDYLETHANOLAMINE PHOSPHOLIPASE D; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PHOSPHOLIPASE D; UNCLASSIFIED DRUG;

ADULT; ARTICLE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; GENE FREQUENCY; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENOTYPE; HAPLOTYPE MAP; HUMAN; ITALY; MAJOR CLINICAL STUDY; MALE; MENTAL PATIENT; MULTICENTER STUDY; PATHOPHYSIOLOGY; PRIORITY JOURNAL; SCHIZOPHRENIA; SINGLE NUCLEOTIDE POLYMORPHISM;

ADULT; DATABASES, GENETIC; ENDOCANNABINOIDS; EUROPEAN CONTINENTAL ANCESTRY GROUP; FEMALE; GENETIC ASSOCIATION STUDIES; GENETIC PREDISPOSITION TO DISEASE; GENOTYPE; HAPLOTYPES; HUMANS; ITALY; MALE; POLYMORPHISM, SINGLE NUCLEOTIDE; PPAR ALPHA; SCHIZOPHRENIA;

EID: 84876010270     PISSN: 0924977X     EISSN: 18737862     Source Type: Journal    
DOI: 10.1016/j.euroneuro.2012.07.007     Document Type: Article

References (53)

1. Arseneault L., Cannon M., Poulton R., Murray R., Caspi A., Moffitt T.E. Cannabis use in adolescence and risk for adult psychosis: longitudinal prospective study. BMJ 2002, 325:1212-1213.
2. Athanasiu L., Mattingsdal M., Kähler A.K., Brown A., Gustafsson O., Agartz I., Giegling I., Muglia P., Cichon S., Rietschel M., Pietiläinen O.P., Peltonen L., Bramon E., Collier D., Clair D.S., Sigurdsson E., Petursson H., Rujescu D., Melle I., Steen V.M., Djurovic S., Andreassen O.A. Gene variants associated with schizophrenia in a Norwegian genome-wide study are replicated in a large European cohort. J. Psychiatr. Res. 2010, 44:748-753.
3. Benvenuti F., Lattanzi F., De Gori A., Tarli P. Activity of some derivatives of palmitoylethanolamide on carragenine-induced edema in the rat paw. Boll. Soc. Ital. Biol. Sper. 1968, 44:809-813.
4. Cao Q., Martinez M., Zhang J., Sanders A.R., Badner J.A., Cravchik A., Markey C.J., Beshah E., Guroff J.J., Maxwell M.E., Kazuba D.M., Whiten R., Goldin L.R., Gershon E.S., Gejman P.V. Suggestive evidence for a schizophrenia susceptibility locus on chromosome 6q and a confirmation in an independent series of pedigrees. Genomics 1997, 43:1-8.
5. Caspi A., Moffitt T.E., Cannon M., McClay J., Murray R., Harrington H., Taylor A., Arseneault L., Williams B., Braithwaite A., Poulton R., Craig I.W. Moderation of the effect of adolescent-onset cannabis use on adult psychosis by a functional polymorphism in the catechol-O-methyltransferase gene: longitudinal evidence of a gene X environment interaction. Biol. Psychiatry 2005, 57:1117-1127.
6. Ceccarini J., De Hert M., van Winkel R., Koethe D., Bormans G., Leweke M., Peuskens J., Van Laere K. In vivo PET imaging of cerebral type 1 cannabinoid receptor availability in patients with schizophrenia. Schizophr. Res. 2010, 117:170.
7. Chavarría-Siles I., Contreras-Rojas J., Hare E., Walss-Bass C., Quezada P., Dassori A., Contreras S., Medina R., Ramírez M., Salazar R., Raventos H., Escamilla M.A. Cannabinoid receptor 1 gene (CNR1) and susceptibility to a quantitative phenotype for hebephrenic schizophrenia. Am. J. Med. Genet. B Neuropsychiatr. Genet. 2008, 147:279-284.
8. Cravatt B.F., Giang D.K., Mayfield S.P., Boger D.L., Lerner R.A., Gilula N.B. Molecular characterization of an enzyme that degrades neuromodulatory fatty-acid amides. Nature 1996, 384:83-87.
9. Dalton V.S., Long L.E., Weickert C.S., Zavitsanou K. Paranoid schizophrenia is characterized by increased CB1 receptor binding in the dorsolateral prefrontal cortex. Neuropsychopharmacology 2011, 36:1620-1630.
10. De Marchi N., De Petrocellis L., Orlando P., Daniele F., Fezza F., Di Marzo V. Endocannabinoid signalling in the blood of patients with schizophrenia. Lipids Health Dis. 2003, 19:2-5.
11. Dean B., Sundram S., Bradbury R., Scarr E., Copolov D. Studies on [3H]CP-55940 binding in the human central nervous system: regional specific changes in density of cannabinoid-1 receptors associated with schizophrenia and cannabis use. Neuroscience 2001, 103:9-15.
12. Desvergne B., Wahli W. Peroxisome proliferator-activated receptors: nuclear control of metabolism. Endocr. Rev. 1999, 20:649-688.
13. Devane W.A., Hanus L., Breuer A., Pertwee R.G., Stevenson L.A., Griffin G., Gibson D., Mandelbaum A., Etinger A., Mechoulam R. Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 1992, 258:1946-1949.
14. Doherty J.L., O'Donovan M.C., Owen M.J. Recent genomic advances in schizophrenia. Clin. Genet. 2012, 81:103-109.
15. Dupont W.D., Plummer W.D. Power and sample size calculations for studies involving linear regression. Controlled Clin. Trials 1998, 19:589-601.
16. Flavell D.M., Pineda Torra I., Jamshidi Y., Evans D., Diamond J.R., Elkeles R.S., Bujac S.R., Miller G., Talmud P.J., Staels B., Humphries S.E. Variation in the PPAR-alpha gene is associated with altered function in vitro and plasma lipid concentrations in type II diabetic subjects. Diabetologia 2000, 43:673-680.
17. Fruchart J., Duriez P., Staels B. Peroxisome proliferator-activated receptor-alpha activators regulate genes governing lipoprotein metabolism, vascular inflammation and atherosclerosis. Curr. Opin. Lipidol. 1999, 10:245-257.
18. Fu J., Gaetani S., Oveisi F., Lo Verme J., Serrano A., Rodriguez De Fonseca F., Rosengarth A., Luecke H., Di Giacomo B., Tarzia G., Piomelli D. Oleylethanolamide regulates feeding and body weight through activation of the nuclear receptor PPAR-alpha. Nature 2003, 425:90-93.
19. Gabriel S.B., Schaffner S.F., Nguyen H., Moore J.M., Roy J., Blumenstiel B., Higgins J., DeFelice M., Lochner A., Faggart M., Liu-Cordero S.N., Rotimi C., Adeyemo A., Cooper R., Ward R., Lander E.S., Daly M.J., Altshuler D. The structure of haplotype blocks in the human genome. Science 2002, 296:2225-2229.
20. Giuffrida A., Leweke F.M., Gerth C.W., Schreiber D., Koethe D., Faulhaber J., Klosterkotter J., Piomelli D. Cerebrospinal anandamide levels are elevated in acute schizophrenia and are inversely correlated with psychotic symptoms. Neuropsychopharmacology 2004, 29:2108-2114.
21. Hamdani N., Tabeze J.P., Ramoz N., Ades J., Hamon M., Sarfati Y., Boni C., Gorwood P. The CNR1 gene as a pharmacogenetic factor for antipsychotics rather than a susceptibility gene for schizophrenia. Eur. Neuropsychopharmacol. 2008, 18:34-40.
22. Ishiguro H., Okubo Y., Ohtsuki T., Yamakawa-Kobayashi K., Arinami T. Mutation analysis of the retinoid X receptor beta, nuclear-related receptor 1, and peroxisome proliferator-activated receptor alpha genes in schizophrenia and alcohol dependence: possible haplotype association of nuclear-related receptor 1 gene to alcohol dependence. Am. J. Med. Genet. 2002, 114:15-23.
23. Ishiguro H., Horiuchi Y., Ishikawa M., Koga M., Imai K., Suzuki Y., Morikawa M., Inada T., Watanabe Y., Takahashi M., Someya T., Ujike H., Iwata N., Ozaki N., Onaivi E.S., Kunugi H., Sasaki T., Itokawa M., Arai M., Niizato K., Iritani S., Naka I., Ohashi J., Kakita A., Takahashi H., Nawa H., Arinami T. Brain cannabinoid CB2 receptor in schizophrenia. Biol. Psychiatry 2010, 67:974-982.
24. Kovasznay B., Fleischer J., Tanenberg-Karant M., Jandorf L., Miller A.D., Bromet E. Substance use disorder and the early course of illness in schizophrenia and affective psychosis. Schizophr. Bull. 1997, 23:195-201.
25. Lahiri D.K., Nurnberger J.I. A rapid non-enzymatic method for the preparation of HMW DNA from blood for RFLP studies. Nucleic Acids Res. 1991, 19:5444.
26. Leroy S., Griffon N., Bourdel M.C., Olie J.P., Poirier M.F., Krebs M.O. Schizophrenia and the cannabinoid receptor type 1 (CB1): association study using a single-base polymorphism in coding exon 1. Am. J. Med. Genet. 2001, 105:749-752.
27. Leweke F.M, Giuffrida A., Wurster U., Emrich H.M., Piomelli D. Elevated endogenous cannabinoids in schizophrenia. Neuroreport 1999, 10:1665-1669.
28. Leweke F.M., Giuffrida A., Koethe D., Schreiber D., Nolden B.M., Kranaster L., Neatby M.A., Schneider M., Gerth C.W., Hellmich M., Klosterkotter J., Piomelli D. Anandamide levels in cerebrospinal fluid of first-episode schizophrenic patients: impact of cannabis use. Schizophr. Res. 2007, 94:29-36.
29. Linszen D.H., Dingemans P.M., Lenior M.E. Cannabis abuse and the course of recent-onset schizophrenic disorders. Arch. Gen. Psychiatry 1994, 51:273-279.
30. Mackie K., Stella N. Cannabinoid receptors and endocannabinoids: evidence for new players. AAPS J. 2006, 8:E298-E306.
31. Malone D.T., Kearn C.S., Chongue L., Mackie K., Taylor D.A. Effect of social isolation on CB1 and D2 receptor and fatty acid amide hydrolase expression in rats. Neuroscience 2008, 152:265-272.
32. Mameli-Engvall M., Evrard A., Pons S., Maskos U., Svensson T.H., Changeux J.P., Faure P. Hierarchical control of dopamine neuron-firing patterns by nicotinic receptors. Neuron 2006, 50:911-921.
33. Matsumoto J., Sugiura Y., Yuki D., Hayasaka T., Goto-Inoue N., Zaima N., Kunii Y., Wada A., Yang Q., Nishiura K., Akatsu H., Hori A., Hashizume Y., Yamamoto T., Ikemoto K., Setou M., Niwa S. Abnormal phospholipids distribution in the prefrontal cortex from a patient with schizophrenia revealed by matrix-assisted laser desorption/ionization imaging mass spectrometry. Anal. Bioanal. Chem. 2011, 400:1933-1943.
34. Melis M., Perra S., Muntoni A.L., Pillolla G., Lutz B., Marsicano G., Di Marzo V., Gessa G.L., Pistis M. Prefrontal cortex stimulation induces 2-arachidonoyl-glycerol-mediated suppression of excitation in dopamine neurons. J. Neurosci. 2004, 24:10707-10715.
35. Melis M., Pistis M. Endocannabinoid signaling in midbrain dopamine neurons: more than physiology?. Curr. Neuropharmacol. 2007, 5:268-277.
36. Melis M., Pillolla G., Luchicchi A., Muntoni A.L., Yasar S., Goldberg S.R., Pistis M. Endogenous fatty acid ethanolamides suppress nicotine-induced activation of mesolimbic dopamine neurons through nuclear receptors. J. Neurosci. 2008, 28:13985-13994.
37. Melis M., Carta S., Fattore L., Tolu S., Yasar S., Goldberg S.R., Fratta W., Maskos U., Pistis M. Peroxisome proliferator-activated receptors-alpha modulate dopamine cell activity through nicotinic receptors. Biol. Psychiatry 2010, 68:256-264.
38. Moreno S., Farioli-Vecchioli S., Cerù M.P. Immunolocalization of peroxisome proliferator-activated receptors and retinoid X receptors in the adult rat CNS. Neuroscience 2004, 123:131-145.
39. Morita Y., Ujike H., Tanaka Y., Uchida N., Nomura A., Ohtani K., Kishimoto M., Morio A., Imamura T., Sakai A., Inada T., Harano M., Komiyama T., Yamada M., Sekine Y., Iwata N., Iyo M., Sora I., Ozaki N., Kuroda S. A nonsynonymous polymorphism in the human fatty acid amide hydrolase gene did not associate with either methamphetamine dependence or schizophrenia. Neurosci. Lett. 2005, 376:182-187.
40. O'Donovan M.C., Williams N.M., Owen M.J. Recent advances in the genetics of schizophrenia. Hum. Mol. Genet. 2003, R125-R133. (12 Spec No. 2).
41. Parolaro D., Realini N., Vigano D., Guidali C., Rubino T. The endocannabinoid system and psychiatric disorders. Exp. Neurol. 2010, 224:3-14.
42. Pistis M., Melis M. From surface to nuclear receptors: the endocannabinoid family extends its assets. Curr. Med. Chem. 2010, 17:1450-1467.
43. Robinson S.A., Loiacono R.E., Christopoulos A., Sexton P.M., Malone D.T. The effect of social isolation on rat brain expression of genes associated with endocannabinoid signaling. Brain Res. 2010, 1343:153-167.
44. Ross C.A., Margolis R.L., Reading S.A., Pletnikov M., Coyle J.T. Neurobiology of schizophrenia. Neuron 2006, 52:139-153.
45. Sadock B.J., Sadock V.A., Ruiz P. Kaplan & Sadock's Comprehensive Textbook of Psychiatry 2009, Lippincott Williams & Wilkins. ninth ed.
46. Sapone A., Peters J., Sakai S., Tomita S., Papiha S.S., Dai R., Friedman F.K., Gonzalez F.J. The human peroxisome proliferator-activated receptor alpha gene: identification and functional characterization of two natural allelic variants. Pharmacogenetics 2000, 10:321-333.
47. Schizophrenia Collaborative Linkage Group for Chromosome 22 A transmission disequilibrium and linkage analysis of D22S278 marker alleles in 574 families: further support for a susceptibility locus for schizophrenia at 22q12. Schizophr. Res. 1998, 32:115-121.
48. Schmitt A., Wilczek K., Blennow K., Maras A., Jatzko A., Petroianu G., Braus D.F., Gattaz W.F. Altered thalamic membrane phospholipids in schizophrenia: a postmortem study. Biol. Psychiatry 2004, 56:41-45.
49. Seifert J., Ossege S., Emrich H.M., Schneider U., Stuhrmann M. No association of CNR1 gene variations with susceptibility to schizophrenia. Neurosci. Lett. 2007, 426:29-33.
50. Sipe J.C., Chiang K., Gerber A.L., Beutler E., Cravatt B.F. A missense mutation in human fatty acid amide hydrolase associated with problem drug use. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:8394-8399.
51. Ueda N., Puffenbarger R.A., Yamamoto S., Deutsch D.G. The fatty acid amide hydrolase (FAAH). Chem. Phys. Lipids 2000, 108:107-121.
52. Ujike H., Takaki M., Nakata K., Tanaka Y., Takeda T., Kodama M., Fujiwara Y., Sakai A., Kuroda S. CNR1, central cannabinoid receptor gene, associated with susceptibility to hebephrenic schizophrenia. Mol. Psychiatry 2002, 7:515-518.
53. Wong D.F., Kuwabara H., Horti A.G., Raymont V., Brasic J., Guevara M., Ye W., Dannals R.F., Ravert H.T., Nandi A., Rahmim A., Ming J.E., Grachev I., Roy C., Cascella N. Quantification of cerebral cannabinoid receptors subtype 1 (CB1) in healthy subjects and schizophrenia by the novel PET radioligand [11C]OMAR. Neuroimage 2010, 52:1505-1513.