The human testis-determining factor SRY localizes in midbrain dopamine neurons and regulates multiple components of catecholamine synthesis and metabolism

Journal of Neurochemistry

Volumn 122, Issue 2, 2012, Pages 260-271

  Czech, Daniel P ^a,b   Lee, Joohyung ^a   Sim, Helena ^a   Parish, Clare L ^c   Vilain, Eric ^d   Harley, Vincent R ^a,b  

^a MONASH MEDICAL CENTRE   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c FLOREY INSTITUTE OF NEUROSCIENCE AND MENTAL HEALTH   (Australia)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

basal ganglia; catecholamine; dopamine; Parkinson's disease; sex determination; sexual dimorphism

Indexed keywords

AMINE OXIDASE (FLAVIN CONTAINING) ISOENZYME A; AROMATIC LEVO AMINO ACID DECARBOXYLASE; CATECHOLAMINE; DOPAMINE; DOPAMINE 2 RECEPTOR; DOPAMINE BETA MONOOXYGENASE; GLUTAMATE DECARBOXYLASE; NUCLEAR RECEPTOR RELATED FACTOR 1; RETINOIC ACID; TESTIS DETERMINING FACTOR; TYROSINE 3 MONOOXYGENASE;

ADULT; AGED; ARTICLE; CATECHOLAMINE METABOLISM; CATECHOLAMINE SYNTHESIS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; EXTRACELLULAR SPACE; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; MALE; MESENCEPHALON; NERVE CELL DIFFERENTIATION; NEUROBLASTOMA CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SEX DIFFERENCE; SRY GENE; SUBSTANTIA NIGRA PARS COMPACTA; SUBSTANTIA NIGRA PARS RETICULATA; TRANSCRIPTION REGULATION; VENTRAL TEGMENTUM;

ADULT; AGED; BLOTTING, WESTERN; CATECHOLAMINES; CELLS, CULTURED; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DOPAMINE; DOPAMINERGIC NEURONS; ELECTROCHEMISTRY; FEMALE; GENES, SRY; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MESENCEPHALON; MIDDLE AGED; PLASMIDS; REAL-TIME POLYMERASE CHAIN REACTION; RNA; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SUBSTANTIA NIGRA; TESTIS; TISSUE BANKS; TRANSFECTION; TYROSINE 3-MONOOXYGENASE;

RODENTIA;

EID: 84863328535     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2012.07782.x     Document Type: Article

References (63)

1. Anderson S., Thompson A., Krenzel E., and, Teicher M., (2002) Pubertal changes in gonadal hormones do not underlie adolescent dopamine receptor overproduction. Psychoneuroendocrinology 27, 683-691. (Pubitemid 34655719)
2. Andrews P. W., (1984) Retinoic acid induces neuronal differentiation of a cloned human embryonal carcinoma cell line in vitro. Dev Biol 103, 285-293.
3. Arnold A., and, Burgoyne P., (2004) Are XX and XY brain cells intrinsically different? Trends Endocrinol. Metab. 15, 6-11. (Pubitemid 38198093)
4. Baron-Cohen S., Knickmeyer R., and, Belmonte M,. (2005) Sex differences in the brain: implications for explaining autism. Science 310, 819-823. (Pubitemid 41567334)
5. Becker J., and, Beer M., (1986) The influence of estrogen on nigrostriatal dopamine activity: behaviour and neurochemical evidence for both pre- and postsynaptic components. Behavior Brain Research 19, 27-33. (Pubitemid 16168022)
6. Cantuti-Castelvetri I., Keller-McGandy C., Bouzou B., Asteris G., Clark T. W., Frosch M. P., and, Standaert D. G,. (2007) Effects of gender on nigral gene expression and Parkinson's disease. Neurobiology of Disease 26, 606-614. (Pubitemid 46756328)
7. Carrer H. F., and, Cambiasso M. J., (2002) Sexual differentiation of the brain: gene, Estrogen, and Neurotrophic factors. Cell. Mol. Neurobiol. 22, 479-500. (Pubitemid 36169205)
8. Carruth L. L., Reisert I., and, Arnold A. P., (2002) Sex chromosome genes directly affect brain sexual differentiation. Nat. Neurosci. 5, 933-934.
9. Cebrian C., and, Prensa L., (2010) Basal ganglia and thalamic input from neurons located within the ventral tier cell cluster region of the substantia nigra pars compacta in the rat. J. Comp. Neurol. 518, 1283-1300.
10. Clepet C., Schafer A. J., Sinclair A. H., Palmer M. S., Lovell-Badge R., and, Goodfellow P. N., (1993) The human SRY transcript. Hum. Mol. Genet. 2, 2007-2012. (Pubitemid 24003391)
11. Czlonkowska A., Ciesielska A., Gromadzka G., and, Kurkowska-Jastrzebska I., (2005) Estrogen and cytokines production-the possible cause of gender differences in neurological diseases. Curr. Pharm. Des. 11, 1017-1030. (Pubitemid 40331302)
12. DeLisi L. E., (1997) Gender and age at onset of schizophrenia. Br. J. Psychiatry 171, 188.
13. Dewing P., Chiang C. W., Sinchak K., et al. (2006) Direct regulation of adult brain function by the male-specific factor SRY. Curr. Biol. 16, 415-420. (Pubitemid 43259353)
14. Dluzen D., and, McDermott J., (2004) Developmental and genetic influences upon gender differences in methamphetamine-induced nigrostriatal dopaminergic neurotoxicity. Ann. N. Y. Acad. Sci. 1025, 205-220. (Pubitemid 39643864)
15. Dubin R., and, Ostrer H., (1994) Sry is a transcriptional activator. Mol. Biol. 8, 1182-1192. (Pubitemid 24292595)
16. Ely D., Milsted A., Bertram J., Ciotti M., Dunphy G., and, Turner M., (2007) Sry delivery to the adrenal medulla increases blood pressure and adrenal medullary tyrosine hydroxylase of normotensive WKY rats. BioMed Central Cardiovascular Disorders 7, 6-22.
17. Ely D., Milsted A., Dunphy G., Boehme S., Dunmire J., Hart M., Toot J., Martins A., and, Turner M., (2009) Delivery of sry1, but not sry2, to the kidney increases blood pressure and sns indices in normotensive wky rats. BMC Physiology 9, 1-13.
18. Fearnley J., and, Lees A., (1991) Ageing and Parkinson's disease: substantia nigra regional selectivity. Brain 114, 2283-2301.
19. Gillies G. E., and, McArthur S., (2010) Estrogen actions in the brain and the basis for differential action in men and women: a case for sex-specific medicines. Pharmacol. Rev. 62, 155-198.
20. Goldstein J. M., (1988) Gender differences in the course of schizophrenia. Am. J. Psychiatry 145, 684-689.
21. Haber S., Ryoo H., Cox C., and, Lu W., (1995) Subsets of midbrain dopaminergic neurons in monkeys are distinguished by different levels of mRNA for the dopamine transporter: comparison with the mRNA for the D2 receptor tyrosine hydroxylase and calbindin immunoreactivity. Journal of Comparative Neurology 362, 400-410.
22. Hacker A., Capel B., Goodfellow P., and, Lovell-Badge R., (1995) Expression of Sry, the mouse sex determining gene. Developmental Biology 121, 1603-1614.
23. Harley V., Clarkson M., and, Argentaro A., (2003a) The Molecular Action and Regulation of the Testis Determining Factors, SRY (Sex-Determining Region on the Y Chromosome) and SOX-9 [SRY-Related High-Mobility Group (HMG) Box 9]. Endocrine Reviews 24, 466-487. (Pubitemid 37056241)
24. Harley V., Layfield S., Mitchell C., Forwood J., John A., Briggs L., McDowall S., and, Jans D., (2003b) Defective importin beta recognition and nuclear import of the sex-determinig factor SRY are associated with XY sex-reversing mutations. Proc. Natl Acad. Sci. USA 100, 7045-7050. (Pubitemid 36706390)
25. Iwawaki T., Kohno K., and, Kobayashi K., (2000) Identification of a potential nurr1 response element that activates the tyrosine hydroxylase gene promoter in cultured cells. Biochemical and Biophyscial Research Communications 274, 590-595. (Pubitemid 30663665)
26. Ji J., and, Dluzen D., (2008) Sex differences in striatal dopaminergic function within heterozygous mutant dopamine transporter knock-out mice. Journal of Neural Transmission 115, 809-817.
27. Jin H., Romano G., Marshall C., Donaldson A., Suon S., and, Iacovitti L., (2006) Tyrosine hydroxylase gene regulation in human neuronal progenitor cells does not depend on Nurr1 as in the murine and rat systems. J. Cell. Physiol. 207, 49-57.
28. Kim K., Kim C., Hwang D., Seo H., Chung S., Hong S., Lim J., Anderson T., and, Isacson O., (2003) Orphan nuclear receptor Nurr1 directly transactivates the promoter activity of the tyrosine hydroxylase gene in a cell-specific manner. J. Neurochem. 85, 622-634. (Pubitemid 36531925)
29. Knower K., Sim H., McClive P., Bowles J., Koopman P., Sinclai A., and, Harley V., (2007) Characterisation of urogenital ridge gene expression in the human embryonal carcinoma cell line NT2/D1. Sexual Development 1, 114-126. (Pubitemid 46714639)
30. Knower K., Kelly S., Ludbrook L., Bagheri-Fam S., Sim H., Bernard P., Sekido R., Lovelle-Badge R., and, Harley V., (2011) Failure of SOX9 regulation in 46XY disorders of sex development with SRY, SOX9 and Sf1 mutations. PLoS ONE 6, e17751.
31. Lahr G., Maxson S., Mayer A., Just W., Pilgrim C., and, Reisert I., (1995) Transcription of the Y chromosomal gene, Sry, in adult mouse brain. Mol. Brain Res. 33, 179-182.
32. Lau Y., and, Li Y., (2009) The human and mouse sex-determining SRY genes repress the Rspo1/Beta-catenin signaling. Journal of Genetics and Genomics 36, 193-202.
33. Ma Y.-Y., Kong S.-Z., Yang L.-J., Meng J.-L., Lv L.-C., and, He M., (2007) Sexual dimorphisms of dopaminergic neurons in rat substantia nigra. Acta Physiologica Sinica 59, 753-758.
34. Martinat C., Bacci J., Leete T., et al. (2006) Cooperative transcription activation by Nurr1 and Pitx3 induces embryonic stem cell maturation to the midbrain dopamine neuron phenotype. Proceedings of the National Academy of Science of the United States of America 103, 2874-2879.
35. Mayer A., Lahr G., Swaab D. F., Pilgrim C., and, Reisert I., (1998) The Y-chromosomal genes SRY and ZFY are transcribed in adult human brain. Neurogenetics 1, 281-288. (Pubitemid 128685086)
36. Mayer A., Mosler G., Just W., Pilgrim C., and, Reisert I., (2000) Developmental profile of Sry transcripts in mouse brain. Neurogenetics 3, 25-30.
37. McArthur S., McHale E., and, Gillies G., (2007) The size and distribution of midbrain dopaminergic populations are permanently altered by perinatal glucocorticoid exposure in a sex- region- and time-specific manner. Neuropsychopharmacology 32, 1462-1476. (Pubitemid 46920154)
38. Misiuta I., Anderson L., McGrogan M., Sanberg P., Willing A., and, Zigova T., (2003) The transcription factor Nurr1 in human NT2 cells and hNT neurons. Dev. Brain Res. 145, 107-115. (Pubitemid 38368646)
39. Milsted A., Serova L., Sabban E., Dunphy G., Turner M., and, Ely D., (2004) Regulation of tyrosine hydroxylase gene transcription by Sry. Neuroscience Letters 369, 203-207. (Pubitemid 39298909)
40. Mozley L., Gur R., Mozley P., and, Gur R., (2001) Striatal dopamine transporters and cognitive functioning in healthy men and women. Am. J. Psychiatry 158, 1492-1499. (Pubitemid 32847251)
41. Munro C., McCaul M., Wong D., et al. (2006) Sex differences in striatal dopamine release in healthy adults. Biol. Psychiatry 59, 966-974.
42. Murray H., Pillai A., McArthur S., Razvi N., Dalta K., Dexter D., and, Gillies G,. (2003) Dose- and sex-dependent effects of the neurotoxin 6-hydroxydopamine on the nigrostriatal dopaminergic pathway of adult rats: differential actions of estrogen in males and females. Neuroscience 116, 213-222. (Pubitemid 36110447)
43. Nelson P., Kondziolka D., Wechsler L., et al. (2002) Clonal human (hnt) neuron grafts for stroketherapy neuropathology in a patient 27 months after implantation. Am. J. Pathol. 160, 1201-1206. (Pubitemid 34411623)
44. Ohashi T., Hanabuchi S., Suzuki R., Kato H., Masuda T., and, Kannagi M,. (2002) Correlation of major histocompatibility complex class i downregulation with resistance of human t-cell leukemia virus type 1-infected t cells to cytotoxic t-lymphocyte killing in a rat model. J. Virol. 74, 9610-9616.
45. Parish C., Castelo-Branco G., Rawal N., Tonnesen J., Sorensen A., Salto C., Kokaia M., Lindvall O., and, Arenas E., (2008) Wnt5a-treated midbrain neural stem cells improve dopamine cell replacement threapy in parkisonian mice. Journal of Clinical Investigation 118, 149-160.
46. Pleasure S., Page C., and, Lee V., (1992) Pure, postmitotic, polarized human neurons derived from NTera 2 cells provide a system for expressing exogenous proteins in terminally differentiated neurons. The Journal of Neuroscience 12, 1802-1815.
47. Reisert I., and, Pilgrim C., (1991) Sexual differentiation of monoaminergic neurons-genetic or epigenetic? Trends in Neuroscience 14, 468-473.
48. Riccardi P., Park S., Anderson S., Doop M., Ansari M., Schmidt D., and, Baldwin R., (2011) Sex differences in the relationship of regional dopamine release to affect and cognitive function in striatal and extrastriatal regions using positron emission tomography and [18F]fallypride. Synapse 65, 99-102.
49. Romano G., Suon S., Jin H., Donaldson A., and, Iacovitti L., (2005) Characterization of five evolutionary conserved regions of the human tyrosine hydroxylase (th) promoter: implications for the engineering of a human th minimal promoter assembled in a self-inactivating lentiviral vector system. J. Cell. Physiol. 204, 666-677. (Pubitemid 40934663)
50. Romano G., Macaluso M., Lucchetti C., and, Iacovitti L., (2007) Transcription and epigenetic profile of the promoter, first exon and first intron of the human tyrosine hydroxylase gene. J. Cell. Physiol. 211, 431-438. (Pubitemid 46580096)
51. Sekido R., and, Lovell-Badge R., (2008) Sex determination involves synergistic action of SRY and SF1 on a specific Sox9 enhancer. Nature 453, 930-934. (Pubitemid 351832560)
52. Sim H., Rimmer K., Kelly S., Ludbrook L., Clayton A., and, Harley V., (2005) Defective calmodulin-mediated nuclear transport of the sex determining region of the y chromosome (sry) in xy sex reversal. Mol. Endocrinol. 19, 1884-1892. (Pubitemid 41007899)
53. Smith Y., and, Villalba R,. (2008) Striatal and extrastriatal dopamine in the basal ganglia: an overview of its anatomical organization in normal and parkinsonian brains. Mov. Disord. 23, S534-S5347.
54. Sutton E., Hughes J., White S., et al. (2011) Identification of SOX3 as an XX male sex reversal gene in mice and humans. Journal of Clinical Investigation 121, 328-321.
55. Tao Q., Fan X. J., Li T., Tang Y., Yang D., and, Le W,. (2011) Gender segregation in gene expression and vulnerability to oxidative stress induced injury in ventral mesencephalic cultures of dopamine neurons. J. Neurosci. Res. 90, 167-178.
56. Walker Q., Rooney M., Woightman R., and, Kuhn C., (2000) Dopamine release and uptake are greater in female than male rat striatum as measured by fast cyclic voltammetry. Neuroscience 9, 5.
57. Wise R., (2009) Roles for nigrostriatal-not just mesocorticolimbic- dopamine in reward and addiction. Cell Press 32, 517-524.
58. Woolley S., O'Malley B., Lydon J., and, Crews D., (2006) Genotype differences in behavior and tyrosine hydroxylase expression between wild-type and progesterone receptor knockout mice. Behavioual Brain Research 167, 197-204. (Pubitemid 43099779)
59. Wooten G., Curre L., Bovbjerg V., Lee J., and, Patrie J., (2004) Are men at greater risk for Parkinson's disease than women? J. Neurol. Neurosurg. Psychiatry 7, 5.
60. Wu J., Chen K., li Y., Lau Y., and, Shih J., (2009) Regulation of monoamine oxidase A by the SRY gene on the Y chromosome. Federation of American Societies for Experimental Biology Journal 23, 4029-4038.
61. Zhang D., Yang S., Yang C., Jin G., and, Zhen X., (2008) Estrogen regulates responses of dopamine neurons in the ventral tegmental area to cocaine. Psychopharmacology 199, 625-635.
62. Zhang K., Zhang L., Rao F., Brar B., Rodriguez-Flores J., Taupenot L., and, O'Connor D., (2010) Human tyrosonie hydroxylase natural genetic variation: delineation of functional transcriptional control motifs disrupted in the proximal promoter. Circulation Cardiovasular Genetics 3, 187-198.
63. Zigova T., Barroso L., Willing A., Saporta S., McGrogan M., Freeman T., and, Sanberg P., (2000) Dopaminergic phenotype of hNT cells in vitro. Dev. Brain Res. 122, 87-90. (Pubitemid 30468476)