1,25-DihydroxyVitamin D regulates expression of the tryptophan hydroxylase 2 and leptin genes: Implication for behavioral influences of Vitamin D

FASEB Journal

Volumn 29, Issue 9, 2015, Pages 4023-4035

  Kaneko, Ichiro ^a,b   Sabir, Marya S ^b   Dussik, Christopher M ^b   Whitfield, G Kerr ^a   Karrys, Amitis ^a,b   Hsieh, Jui Cheng ^a   Haussler, Mark R ^a   Meyer, Mark B ^c   Pike, J Wesley ^c   Jurutka, Peter W ^a,b  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^b ARIZONA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Chromatin immunoprecipitation; Cis regulatory module; CNS; Neuropsychiatric disorders; Serotonin

Indexed keywords

CALCITRIOL; LEPTIN; MESSENGER RNA; RETINOID X RECEPTOR; SEROTONIN; TRYPTOPHAN HYDROXYLASE 2; VITAMIN D RECEPTOR; TPH2 PROTEIN, HUMAN; TPH2 PROTEIN, MOUSE; TRYPTOPHAN HYDROXYLASE;

ADIPOCYTE; ANIMAL CELL; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; EMBRYO; ENZYME SYNTHESIS; GENE EXPRESSION; GENE SEQUENCE; GENETIC TRANSCRIPTION; GLIOBLASTOMA CELL LINE; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; RAT; REPORTER GENE; SEQUENCE ANALYSIS; SEROTONIN BRAIN LEVEL; 3T3 CELL LINE; ANIMAL; ANIMAL BEHAVIOR; AUTISM; BIOSYNTHESIS; DNA RESPONSIVE ELEMENT; DRUG EFFECTS; FEEDING BEHAVIOR; GENE EXPRESSION REGULATION; HEK293 CELL LINE; METABOLISM; MOUSE; TUMOR CELL LINE;

3T3-L1 CELLS; ANIMALS; AUTISTIC DISORDER; BEHAVIOR, ANIMAL; CALCITRIOL; CELL LINE, TUMOR; FEEDING BEHAVIOR; GENE EXPRESSION REGULATION; HEK293 CELLS; HUMANS; LEPTIN; MICE; RESPONSE ELEMENTS; RNA, MESSENGER; TRYPTOPHAN HYDROXYLASE;

EID: 84952717270     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.14-269811     Document Type: Article

References (43)

1. Haussler,M.R.,Whitfield, G. K., Kaneko, I., Haussler, C. A., Hsieh, D., Hsieh, J. C., and Jurutka, P. W. (2013) Molecular mechanisms of vitamin D action. Calcif. Tissue Int. 92, 77-98
2. Haussler, M. R., Jurutka, P. W., Mizwicki, M., and Norman, A. W. (2011) Vitamin D receptor (VDR)-mediated actions of 1a,25 (OH)?vitamin D?: genomic and non-genomic mechanisms. Best Pract. Res. Clin. Endocrinol. Metab. 25,543-559
3. Pike, J. W., and Meyer, M. B. (2014) Fundamentals of vitamin D hormone-regulated gene expression. J. Steroid Biochem. Mol. Biol. 144, 5-11
4. Pike, J. W., Lee, S. M., and Meyer, M. B. (2014) Regulation of gene expression by 1,25-dihydroxy vitamin D3 in bone cells: exploiting new approaches and defining new mechanisms. Bonekey Rep 3,482
5. Harms, L. R., Burne, T. H., Eyles, D. W., and McGrath, J. J. (2011) Vitamin D and the brain. Best Pract. Res. Clin. Endocrinol. Metab. 25, 657-669
6. Eyles, D. W., Smith, S., Kinobe, R., Hewison, M., and McGrath, J. J. (2005) Distribution of the vitamin D receptor and 1 alphahydroxylase in human brain. J. Chem. Neuroanat. 29,21-30
7. Lesch, K. P. (2005) Serotonergic gene inactivation in mice: models for anxiety and aggression? Novartis Found. Symp. 268, 111-140; discussion 140-116, 167-170
8. Wrase, J., Reimold, M., Puls, I., Kienast, T., and Heinz, A. (2006) Serotonergic dysfunction: brain imaging and behavioral correlates. Cogn.Affect.Behav.Neurosci.6,53-61
9. Lovenberg, W., Jequier, E., and Sjoerdsma, A. (1967) Tryptophan hydroxylation: measurement in pineal gland, brainstem, and carcinoid tumor. Science 155,217-219
10. Gutknecht, L., Kriegebaum, C., Waider, J., Schmitt, A., and Lesch, K. P. (2009) Spatio-temporal expression of tryptophan hydroxylase isoforms in murine and human brain: convergent data from Tph2 knockout mice. Eur. Neuropsychopharmacol. 19, 266-282
11. Zhang, X., Beaulieu, J. M., Sotnikova, T. D., Gainetdinov, R. R., and Caron, M. G. (2004) Tryptophan hydroxylase-2 controls brain serotonin synthesis. Science 305, 217
12. Remes Lenicov, F., Lemonde, S., Czesak, M., Mosher, T. M., and Albert, P. R. (2007) Cell-type specific induction of tryptophan hydroxylase-2 transcription by calcium mobilization. J. Neurochem. 103, 2047-2057
13. Patrick, R. P., and Ames, B. N. (2014) Vitamin D hormone regulates serotonin synthesis, part 1: relevance for autism. FASEB J. 28, 2398-2413
14. Morash, B., Li, A., Murphy, P. R., Wilkinson, M., and Ur, E. (1999) Leptin gene expressionin the brain and pituitarygland. Endocrinology 140, 5995-5998
15. Wrann, C. D., and Rosen, E. D. (2012) New insights into adipocytespecific leptin gene expression. Adipocyte 1,168-172
16. Menendez, C., Lage, M., Peino, R., Baldelli, R., Concheiro, P., Diéguez, C., and Casanueva, F. F. (2001) Retinoic acid and vitamin D (3) powerfully inhibit in vitro leptin secretion by human adipose tissue. J. Endocrinol. 170,425-431
17. Kong, J., Chen, Y., Zhu, G., Zhao, Q., and Li, Y. C. (2013) 1,25-Dihydroxyvitamin D3 upregulates leptin expression in mouse adipose tissue. J. Endocrinol. 216, 265-271
18. Narvaez, C. J., Matthews, D., Broun, E., Chan, M., and Welsh, J. (2009) Lean phenotype and resistance to diet-induced obesity in vitamin D receptor knockout mice correlates with induction of uncoupling protein-1 in white adipose tissue. Endocrinology 150, 651-661
19. Malloy, P. J., and Feldman, B. J. (2013) Cell-autonomous regulation of brown fat identity gene UCP1 by unliganded vitamin D receptor. Mol. Endocrinol. 27, 1632-1642
20. Hsieh, J. C., Whitfield, G. K., Jurutka, P. W., Haussler, C. A., Thatcher, M. L., Thompson, P. D., Dang, H. T., Galligan, M. A., Oza, A. K., and Haussler, M. R. (2003) Two basic amino acids C-terminal of the proximal box specify functional binding of the vitamin D receptor to its rat osteocalcin deoxyribonucleic acid-responsive element. Endocrinology 144, 5065-5080
21. Mix, H., Widjaja, A., Jandl, O., Cornberg, M., Kaul, A., Göke, M., Beil, W., Kuske, M., Brabant, G., Manns, M. P., and Wagner, S. (2000) Expression of leptin and leptin receptor isoforms in the human stomach. Gut 47, 481-486
22. Meyer, M. B., Benkusky, N. A., Lee, C. H., and Pike, J. W. (2014) Genomic determinants of gene regulation by 1,25-dihydroxyvitamin D3 during osteoblast-lineage cell differentiation. J. Biol. Chem. 289, 19539-19554
23. Meyer, M. B., Benkusky, N. A., and Pike, J. W. (2014) The RUNX2 cistrome in osteoblasts: characterization, down-regulation following differentiation, and relationship to gene expression. J. Biol. Chem. 289, 16016-16031
24. Hiroi, R., and Handa, R. J. (2013) Estrogen receptor-b regulates human tryptophan hydroxylase-2 through an estrogen response element in the 59 untranslated region. J. Neurochem. 127,487-495
25. Terpening, C. M., Haussler, C. A., Jurutka, P. W., Galligan, M. A., Komm, B. S., and Haussler, M. R. (1991) The vitamin D-responsive element in the rat bone Gla protein gene is an imperfect direct repeat that cooperates with other cis-elements in 1,25-dihydroxyvitamin D3- mediated transcriptional activation. Mol. Endocrinol. 5, 373-385
26. Thompson,P.D.,Jurutka,P.W.,Whitfield,G.K.,Myskowski,S.M., Eichhorst, K. R., Dominguez, C. E., Haussler, C. A., and Haussler, M. R. (2002) Liganded VDR induces CYP3A4 in small intestinal and colon cancer cells via DR3 and ER6 vitamin D responsive elements. Biochem. Biophys. Res. Commun. 299,730-738
27. Kent,W.J.,Sugnet,C.W.,Furey,T.S.,Roskin,K.M.,Pringle,T.H., Zahler, A. M., and Haussler, D. (2002) The human genome browser at UCSC. Genome Res. 12,996-1006
28. Brown, J., Bianco, J. I., McGrath, J. J., and Eyles, D. W. (2003) 1,25-Dihydroxyvitamin D3 induces nerve growth factor, promotes neurite outgrowth and inhibits mitosis in embryonic rat hippocampal neurons. Neurosci. Lett. 343,139-143
29. Brewer, L. D., Thibault, V., Chen, K. C., Langub, M. C., Landfield, P. W., and Porter, N. M. (2001) Vitamin D hormone confers neuroprotection in parallel with downregulation of L-type calcium channel expression in hippocampal neurons. J. Neurosci. 21, 98-108
30. Wang, Y., Chiang, Y. H., Su, T. P., Hayashi, T., Morales, M., Hoffer, B. J., and Lin, S. Z. (2000) Vitamin D(3) attenuates cortical infarction induced by middle cerebral arterial ligation in rats. Neuropharmacology 39,873-880
31. Taniura, H., Ito, M., Sanada, N., Kuramoto, N., Ohno, Y., Nakamichi, N., and Yoneda, Y. (2006) Chronic vitamin D3 treatment protects against neurotoxicity by glutamate in association with upregulation of vitamin D receptor mRNA expression in cultured rat cortical neurons. J. Neurosci. Res. 83, 1179-1189
32. Jiang, P., Zhang, L. H., Cai, H. L., Li, H. D., Liu, Y. P., Tang, M. M., Dang, R. L., Zhu, W. Y., Xue, Y., and He, X. (2014) Neurochemical effects of chronic administration of calcitriol in rats. Nutrients 6, 6048-6059
33. Groves, N. J., Kesby, J. P., Eyles, D. W., McGrath, J. J., Mackay-Sim, A., and Burne, T. H. (2013) Adult vitamin D deficiency leads to behavioural and brain neurochemical alterations in C57BL/6J and BALB/c mice. Behav. Brain Res. 241,120-131
34. Yuksel, R. N., Altunsoy, N., Tikir, B., Cingi Kuluk, M., Unal, K., Goka, S., Aydemir, C., and Goka, E. (2014) Correlation between total vitamin D levels and psychotic psychopathology in patients with schizophrenia: therapeutic implications for add-on vitamin D augmentation. Ther. Adv. Psychopharmacol. 4,268-275
35. Cieslak, K., Feingold, J., Antonius, D., Walsh-Messinger, J., Dracxler, R., Rosedale, M., Aujero, N., Keefe, D., Goetz, D., Goetz, R., and Malaspina, D. (2014) Low vitamin D levels predict clinical features of schizophrenia. Schizophr. Res. 159,543-545
36. Keisala, T., Minasyan, A., Lou, Y. R., Zou, J., Kalueff, A. V., Pyykkö, I., and Tuohimaa, P. (2009) Premature aging in vitamin D receptor mutant mice. J. Steroid Biochem. Mol. Biol. 115, 91-97
37. Meyer, M. B., Goetsch, P. D., and Pike, J. W. (2010) Genome-wide analysis of the VDR/RXR cistrome in osteoblast cells provides new mechanistic insight into the actions of the vitamin D hormone. J. Steroid Biochem. Mol. Biol. 121,136-141
38. Pike, J. W., Meyer, M. B., Martowicz, M. L., Bishop, K. A., Lee, S. M., Nerenz, R. D., and Goetsch, P. D. (2010) Emerging regulatory paradigms for control of gene expression by 1,25-dihydroxyvitamin D3. J. Steroid Biochem. Mol. Biol. 121,130-135
39. Shen,W.,Wang,C.,Xia,L.,Fan,C.,Dong,H.,Deckelbaum,R.J.,and Qi, K. (2014) Epigenetic modification of the leptin promoter in dietinduced obese mice and the effects of N-3 polyunsaturated fatty acids. Sci. Rep. 4, 5282
40. Blumberg, J. M., Tzameli, I., Astapova, I., Lam, F. S., Flier, J. S., and Hollenberg, A. N. (2006) Complex role of the vitamin D receptor and its ligand in adipogenesis in 3T3-L1 cells. J. Biol. Chem. 281, 11205-11213
41. Kong, J., and Li, Y. C. (2006) Molecular mechanism of 1,25-dihydroxyvitamin D3 inhibition of adipogenesis in 3T3-L1 cells. Am. J. Physiol. Endocrinol. Metab. 290,E916-E924
42. Confavreux, C. B. (2011) Bone: from a reservoir of minerals to a regulator of energy metabolism. Kidney Int. Suppl. 121, S14-S19
43. Patrick, R. P., and Ames, B. N. (2015) Vitamin D and the omega-3 fatty acids control serotonin synthesis and action, part 2: relevance for ADHD, bipolar, schizophrenia, and impulsive behavior. FASEB J. 29,2207-2222