Vitamin D insufficiency and schizophrenia risk: Evaluation of hyperprolinemia as a mediator of association

Schizophrenia Research

Volumn 156, Issue 1, 2014, Pages 15-22

  Clelland, James D ^a,b   Read, Laura L ^a,b   Drouet, Valérie ^c   Kaon, Angela ^a   Kelly, Alexandra ^c   Duff, Karen E ^c,d   Nadrich, Robert H ^b,e   Rajparia, Amit ^b,e   Clelland, Catherine L ^c  

^a NATHAN S KLINE INSTITUTE FOR PSYCHIATRIC RESEARCH   (United States)

^b NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

^c NewYork Presbyterian Hospital   (United States)

^d NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

^e BELLEVUE HOSPITAL CENTER   (United States)

Author keywords

Hyperprolinemia; Mediator; Proline; Schizophrenia; Treatment; Vitamin D insufficiency

Indexed keywords

CALCIFEDIOL; PROLINE; PROLINE DEHYDROGENASE; 25-HYDROXYVITAMIN D; PRODH PROTEIN, HUMAN; VITAMIN D;

ADULT; AGED; AMINO ACID BLOOD LEVEL; ARTICLE; CLINICAL EVALUATION; CONTROLLED STUDY; DISEASE ASSOCIATION; ENZYME BLOOD LEVEL; FEMALE; GENE EXPRESSION REGULATION; HUMAN; HYPERPROLINEMIA; INTELLIGENCE QUOTIENT; MAJOR CLINICAL STUDY; MALE; PHENOTYPE; PRIORITY JOURNAL; PRODH GENE; PROTEIN EXPRESSION; RISK ASSESSMENT; SCHIZOPHRENIA; VITAMIN BLOOD LEVEL; VITAMIN D DEFICIENCY; ADOLESCENT; ANALOGS AND DERIVATIVES; BLOOD; COMPLICATION; DEFICIENCY; DIET RESTRICTION; DISORDERS OF AMINO ACID AND PROTEIN METABOLISM; GENETIC PREDISPOSITION; GENETICS; METABOLISM; MIDDLE AGED; MUTATION; RISK FACTOR; STATISTICAL MODEL; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; AMINO ACID METABOLISM, INBORN ERRORS; FASTING; FEMALE; GENETIC PREDISPOSITION TO DISEASE; HUMANS; MALE; MIDDLE AGED; MODELS, STATISTICAL; MUTATION; PROLINE; PROLINE OXIDASE; RISK FACTORS; SCHIZOPHRENIA; VITAMIN D; VITAMIN D DEFICIENCY; YOUNG ADULT;

EID: 84899923365     PISSN: 09209964     EISSN: 15732509     Source Type: Journal    
DOI: 10.1016/j.schres.2014.03.017     Document Type: Article

References (56)

1. Barbui C., Signoretti A., Mule S., Boso M., Cipriani A. Does the addition of a second antipsychotic drug improve clozapine treatment?. Schizophr. Bull. 2008, 35(2):458-468.
2. Baron R.M., Kenny D.A. The moderator-mediator variable distinction in social psychological research: conceptual, strategic, and statistical considerations. J. Pers. Soc. Psychol. 1986, 51(6):1173-1182.
3. Baxter C.F., Baldwin R.A., Davis J.L., Flood J.F. High proline levels in the brains of mice as related to specific learning deficits. Pharmacol. Biochem. Behav. 1985, 22(6):1053-1059.
4. Belvederi Murri M., Respino M., Masotti M., Innamorati M., Mondelli V., Pariante C., Amore M. Vitamin D and psychosis: mini meta-analysis. Schizophr. Res. 2013, 150(1):235-239.
5. Berg A.O., Melle I., Torjesen P.A., Lien L., Hauff E., Andreassen O.A. A cross-sectional study of vitamin D deficiency among immigrants and Norwegians with psychosis compared to the general population. J. Clin. Psychiatry 2010, 71(12):1598-1604.
6. Bossé Y., Maghni K., Hudson T.J. 1alpha,25-dihydroxy-vitamin D3 stimulation of bronchial smooth muscle cells induces autocrine, contractility, and remodeling processes. Physiol. Genomics 2007, 29(2):161-168.
7. Clelland C.L., Read L.L., Baraldi A.N., Bart C.P., Pappas C.A., Panek L.J., Nadrich R.H., Clelland J.D. Evidence for association of hyperprolinemia with schizophrenia and a measure of clinical outcome. Schizophr. Res. 2011, 131(1-3):139-145.
8. Cohen S.M., Nadler J.V. Proline-induced inhibition of glutamate release in hippocampal area CA1. Brain Res. 1997, 769:333-339.
9. Crews M., Lally J., Gardner-Sood P., Howes O., Bonaccorso S., Smith S., Murray R.M., Di Forti M., Gaughran F. Vitamin D deficiency in first episode psychosis: a case-control study. Schizophr. Res. 2013, 150(2-3):533-537.
10. Crum R.M., Anthony J.C., Bassett S.S., Folstein M.F. Population-based norms for the Mini-Mental State Examination by age and educational level. JAMA 1993, 269(18):2386-2391.
11. Davis J.M., Spaide J.K., Himwich H.E. Effects of tranylcypromine and l-cysteine on plasma amino acids in controls and schizophrenic patients. Am. J. Clin. Nutr. 1972, 25(3):302-310.
12. Dingman W., Sporn M.B. The penetration of proline and proline derivatives into brain. J. Neurochem. 1959, 4(2):148-153.
13. Doknic M., Maric N.P., Britvic D., Pekic S., Damjanovic A., Miljic D., Stojanovic M., Radojicic Z., Jasovic Gasic M., Popovic V. Bone remodeling, bone mass and weight gain in patients with stabilized schizophrenia in real-life conditions treated with long-acting injectable risperidone. Neuroendocrinology 2011, 94(3):246-254.
14. Efrom M.L. Familial hyperprolinemia. Report of a second case, associated with congenital renal malformations, hereditary hematuria and mild mental retardation, with demonstration of an enzyme defect. N. Engl. J. Med. 1965, 272:1243-1254.
15. Eyles D.W., Burne T.H., McGrath J.J. Vitamin D, effects on brain development, adult brain function and the links between low levels of vitamin D and neuropsychiatric disease. Front. Neuroendocrinol. 2013, 34(1):47-64.
16. Ferreira A.G., da Cunha A.A., Scherer E.B., Machado F.R., da Cunha M.J., Braga A., Mussulini B.H., Moreira J.D., Wofchuk S., Souza D.O., Wyse A.T. Evidence that hyperprolinemia alters glutamatergic homeostasis in rat brain: neuroprotector effect of guanosine. Neurochem. Res. 2012, 37(1):205-213.
17. Garland C.F., French C.B., Baggerly L.L., Heaney R.P. Vitamin D supplement doses and serum 25-hydroxyvitamin D in the range associated with cancer prevention. Anticancer Res. 2011, 31(2):607-611.
18. Girgis R.R., Javitch J.A., Lieberman J.A. Antipsychotic drug mechanisms: links between therapeutic effects, metabolic side effects and the insulin signaling pathway. Mol. Psychiatry 2008, 13:918-929.
19. Gogos J.A., Santha M., Takacs Z., Beck K.D., Luine V., Lucas L.R., Nadler J.V., Karayiorgou M. The gene encoding proline dehydrogenase modulates sensorimotor gating in mice. Nat. Genet. 1999, 21(4):434-439.
20. Gracious B.L., Finucane T.L., Friedman-Campbell M., Messing S., Parkhurst M.N. Vitamin D deficiency and psychotic features in mentally ill adolescents: a cross-sectional study. BMC Psychiatry 2012, 12:38.
21. Heaney R.P. Vitamin D in health and disease. Clin. J. Am. Soc. Nephrol. 2008, 3(5):1535-1541.
22. Heaney R.P., Davies K.M., Chen T.C., Holick M.F., Barger-Lux M.J. Human serum 25-hydroxycholecalciferol response to extended oral dosing with cholecalciferol. Am. J. Clin. Nutr. 2003, 77(1):204-210.
23. Heaney R.P., Holick M.F. Why the IOM recommendations for vitamin D are deficient. J. Bone Miner. Res. 2011, 26(3):455-457.
24. Hedelin M., Löf M., Olsson M., Lewander T., Nilsson B., Hultman C.M., Weiderpass E. Dietary intake of fish, omega-3, omega-6 polyunsaturated fatty acids and vitamin D and the prevalence of psychotic-like symptoms in a cohort of 33,000 women from the general population. BMC Psychiatry 2010, 10:38.
25. Holick M.F., Binkley N.C., Bischoff-Ferrari H.A., Gordon C.M., Hanley D.A., Heaney R.P., Murad M.H., Weaver C.M., Society Endocrine Evaluation, treatment, and prevention of vitamin D deficiency: an Endocrine Society clinical practice guideline. J. Clin. Endocrinol. Metab. 2011, 96(7):1911-1930.
26. Holick M.F., Binkley N.C., Bischoff-Ferrari H.A., Gordon C.M., Hanley D.A., Heaney R.P., Murad M.H., Weaver C.M. Guidelines for preventing and treating vitamin D deficiency and insufficiency revisited. J. Clin. Endocrinol. Metab. 2012, 97(4):1153-1158.
27. Humble M.B., Gustafsson S., Bejerot S. Low serum levels of 25-hydroxyvitamin D (25-OHD) among psychiatric out-patients in Sweden: relations with season, age, ethnic origin and psychiatric diagnosis. J. Steroid Biochem. Mol. Biol. 2010, 121(1-2):467-470.
28. Institute of Medicine (IOM) Dietary Reference Intakes for Calcium and Vitamin D 2011, The National Academies Press, Washington, DC, (released November 2010).
29. Itzhaky D., Amital D., Gorden K., Bogomolni A., Arnson Y., Amital H. Low serum vitamin D concentrations in patients with schizophrenia. Isr. Med. Assoc. J. 2012, 14(2):88-92.
30. Jacquet H., Berthelot J., Bonnemains C., Simard G., Saugier-Veber P., Raux G., Campion D., Bonneau D., Frebourg T. The severe form of type I hyperprolinaemia results from homozygous inactivation of the PRODH gene. J. Med. Genet. 2003, 40(1):e7.
31. Jacquet H., Demily C., Houy E., Hecketsweiler B., Bou J., Raux G., Lerond J., Allio G., Haouzir S., Tillaux A., Bellegou C., Fouldrin G., Delamillieure P., Ménard J.F., Dollfus S., D'Amato T., Petit M., Thibaut F., Frébourg T., Campion D. Hyperprolinemia is a risk factor for schizoaffective disorder. Mol. Psychiatry 2005, 10(5):479-485.
32. Karayiorgou M., Gogos J.A. The molecular genetics of the 22q11-associated schizophrenia. Brain Res. Mol. Brain Res. 2004, 132(2):95-104.
33. Kenny D.A., Kashy D., Bolger N. Data analysis in social psychology. Handbook of Social Psychology 1998, 233-265. McGraw-Hill Press, New York. Fourth ed. D. Gilbert, S. Fiske, G. Lindzey (Eds.).
34. Llewellyn D.J., Lang I.A., Langa K.M., Muniz-Terrera G., Phillips C.L., Cherubini A., Ferrucci L., Melzer D. Vitamin D and risk of cognitive decline in elderly persons. Arch. Intern. Med. 2011, 170(13):1135-1141.
35. McGrath J. Is it time to trial vitamin D supplements for the prevention of schizophrenia?. Acta Psychiatr. Scand. 2010, 121(5):321-324.
36. McGrath J., Saari K., Hakko H., Jokelainen J., Jones P., Järvelin M.R., Chant D., Isohanni M. Vitamin D supplementation during the first year of life and risk of schizophrenia: a Finnish birth cohort study. Schizophr. Res. 2004, 67(2-3):237-245.
37. McGrath J.J., Burne T.H., Féron F., Mackay-Sim A., Eyles D.W. Developmental vitamin D deficiency and risk of schizophrenia: a 10-year update. Schizophr. Bull. 2010, 36(6):1073-1078.
38. McGrath J.J., Eyles D.W., Pedersen C.B., Anderson C., Ko P., Burne T.H., Norgaard-Pedersen B., Hougaard D.M., Mortensen P.B. Neonatal vitamin D status and risk of schizophrenia: a population-based case-control study. Arch. Gen. Psychiatry 2010, 67(9):889-894.
39. Menkes D.B., Lancaster K., Grant M., Marsh R.W., Dean P., du Toit S.A. Vitamin D status of psychiatric inpatients in New Zealand's Waikato region. BMC Psychiatry 2012, 12:68.
40. Milaneschi Y., Hoogendijk W., Lips P., Heijboer A.C., Schoevers R., van Hemert A.M., Beekman A.T., Smit J.H., Penninx B.W. The association between low vitamin D and depressive disorders. Mol. Psychiatry 2013, (Apr 9, Epub ahead of print). 10.1038/mp.2013.36.
41. Nadler J. Sodium-dependent proline uptake in the rat hippocampal formation: association with ipsilateral-commissural projections of CA3 pyramidal cells. J. Neurochem. 1987, 49:1155-1160.
42. Nadler J.V., Bray S.D., Evenson D.A. Autoradiographic localization of proline uptake in excitatory hippocampal pathways. Hippocampus 1992, 2:269-278.
43. Orešič M., Tang J., Seppänen-Laakso T., Mattila I., Saarni S.E., Saarni S.I., Lönnqvist J., Sysi-Aho M., Hyötyläinen T., Perälä J., Suvisaari J. Metabolome in schizophrenia and other psychotic disorders: a general population-based study. Genome Med. 2011, 3(3):19.
44. Partti K., Heliövaara M., Impivaara O., Perälä J., Saarni S.I., Lönnqvist J., Suvisaari J.M. Skeletal status in psychotic disorders: a population-based study. Psychosom. Med. 2010, 2(9):933-940.
45. Paterlini M., Zakharenko S.S., Lai W.S., Qin J., Zhang H., Mukai J., Westphal K.G., Olivier B., Sulzer D., Pavlidis P., Siegelbaum S.A., Karayiorgou M., Gogos J.A. Transcriptional and behavioral interaction between 22q11.2 orthologs modulates schizophrenia-related phenotypes in mice. Nat. Neurosci. 2005, 8(11):1586-1594.
46. Phang J.M., Hu C.A., Valle D. Disorders of proline and hydroxyproline metabolism. Metabolic and Molecular Basis of Inherited Disease 2001, 1821-1838. McGraw-Hill Press, New York. C.R. Scriver, A.L. Beaudet, W.S. Sly, D. Valle (Eds.).
47. Rao M.L., Gross G., Strebel B., Bräunig P., Huber G., Klosterkötter J. Serum amino acids, central monoamines, and hormones in drug-naive, drug-free, and neuroleptic-treated schizophrenic patients and healthy subjects. Psychiatry Res. 1990, 34(3):243-257.
48. Raux G., Bumsel E., Hecketsweiler B., van Amelsvoort T., Zinkstok J., Manouvrier-Hanu S., Fantini C., Brévière G.M., Di Rosa G., Pustorino G., Vogels A., Swillen A., Legallic S., Bou J., Opolczynski G., Drouin-Garraud V., Lemarchand M., Philip N., Gérard-Desplanches A., Carlier M., Philippe A., Nolen M.C., Heron D., Sarda P., Lacombe D., Coizet C., Alembik Y., Layet V., Afenjar A., Hannequin D., Demily C., Petit M., Thibaut F., Frebourg T., Campion D. Involvement of hyperprolinemia in cognitive and psychiatric features of the 22q11 deletion syndrome. Hum. Mol. Genet. 2007, 16(1):83-91.
49. Rey-Sánchez P., Lavado-García J.M., Canal-Macías M.L., Gómez-Zubeldia M.A., Roncero-Martín R., Pedrera-Zamorano J.D. Ultrasound bone mass in schizophrenic patients on antipsychotic therapy. Hum. Psychopharmacol. 2009, 24(1):49-54.
50. Rosen C.J. Clinical practice. Vitamin D insufficiency. N. Engl. J. Med. 2011, 364(3):248-254.
51. Rosen C.J., Abrams S.A., Aloia J.F., Brannon P.M., Clinton S.K., Durazo-Arvizu R.A., Gallagher J.C., Gallo R.L., Jones G., Kovacs C.S., Manson J.E., Mayne S.T., Ross A.C., Shapses S.A., Taylor C.L. IOM committee members respond to Endocrine Society vitamin D guideline. J. Clin. Endocrinol. Metab. 2012, 97(4):1146-1152.
52. Shanti N.D., Shashikumar K.C., Desai P.V. Influence of proline on rat brain activities of alanine aminotransferase, aspartate aminotransferase and acid phosphatase. Neurochem. Res. 2004, 29(12):2197-2206.
53. Thompson T., Andreeff M., Studzinski G.P., Vassilev L.T. 1,25-dihydroxyvitamin D3 enhances the apoptotic activity of MDM2 antagonist nutlin-3a in acute myeloid leukemia cells expressing wild-type p53. Mol. Cancer Ther. 2010, 9(5):1158-1168.
54. Tolppanen A.M., Sayers A., Fraser W.D., Lewis G., Zammit S., McGrath J., Lawlor D.A. Serum 25-hydroxyvitamin d(3) and d(2) and non-clinical psychotic experiences in childhood. PLoS One 2012, 7(7):e41575.
55. Tomiya M., Fukushima T., Watanabe H., Fukami G., Fujisaki M., Iyo M., Hashimoto K., Mitsuhashi S., Toyo'oka T. Alterations in serum amino acid concentrations in male and female schizophrenic patients. Clin. Chim. Acta 2007, 380(1-2):186-190.
56. Wood R.J., Tchack L., Angelo G., Pratt R.E., Sonna L.A. DNA microarray analysis of vitamin D-induced gene expression in a human colon carcinoma cell line. Physiol. Genomics 2004, 17(2):122-129.