Epigenetic control of neurotransmitter expression in olfactory bulb interneurons

International Journal of Developmental Neuroscience

Volumn 31, Issue 6, 2013, Pages 415-423

  Banerjee, Kasturi ^a   Akiba, Yosuke ^a   Baker, Harriet ^a,b   Cave, John W ^a,b  

^a BURKE MEDICAL RESEARCH INSTITUTE   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Adult neurogenesis; Dopamine; GABA; Glutamic acid decarboxylase; Olfactory bulb; Tyrosine hydroxylase

Indexed keywords

4 AMINOBUTYRIC ACID; DOPAMINE; GLUTAMIC ACID DECARBOXYLASE 1; GLUTAMIC ACID DECARBOXYLASE 2; HISTONE DEACETYLASE; HISTONE DEACETYLASE 2; HISTONE H3; NEUROTRANSMITTER; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG;

ADULT ANIMAL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; CONTROLLED STUDY; DOPAMINERGIC SYSTEM; DOPAMINERGIC TRANSMISSION; EPIGENETIC REPRESSION; EPIGENETICS; GABAERGIC TRANSMISSION; GAD1 GENE; GENE; GENETIC TRANSCRIPTION; HDAC2 GENE; HISTONE ACETYLATION; INTERNEURON; MOUSE; NEUROBLAST; NONHUMAN; OLFACTORY BULB; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; REGULATORY MECHANISM; SMELLING; SYNAPSE; TH GENE;

ACETYLATED HISTONE H3; ACH3; ADULT NEUROGENESIS; CHIP; CHROMATIN IMMUNOPRECIPITATION; DOPAMINE; GABA; GAD; GAMMA AMINOBUTYRIC ACID; GLUTAMIC ACID DECARBOXYLASE; HDAC; HISTONE DEACETYLASE; NEURAL RESTRICTIVE SILENCER ELEMENTS; NRSE; OB; OLFACTORY BULB; QPCR; QUANTITATIVE POLYMERASE CHAIN REACTION; RMS; ROSTRAL MIGRATORY STREAM; SUBVENTRICULAR ZONE; SVZ; TH; TRICHOSTATIN A; TSA; TYROSINE HYDROXYLASE;

ANIMALS; EPIGENOMICS; GENE EXPRESSION REGULATION; HUMANS; INTERNEURONS; NEUROTRANSMITTER AGENTS; OLFACTORY BULB;

EID: 84880043534     PISSN: 07365748     EISSN: 1873474X     Source Type: Journal    
DOI: 10.1016/j.ijdevneu.2012.11.009     Document Type: Article

References (85)

1. Akiba Y., Cave J.W., Akiba N., Langley B., Ratan R.R., Baker H. Histone deacetylase inhibitors de-repress tyrosine hydroxylase expression in the olfactory bulb and rostral migratory stream. Biochemical and Biophysical Research Communications 2010, 393:673-677.
2. Allen Z.J., Waclaw R.R., Colbert M.C., Campbell K. Molecular identity of olfactory bulb interneurons: transcriptional codes of periglomerular neuron subtypes. Journal of Molecular Histology 2007, 38:517-525.
3. Aranyi T., Faucheux B.A., Khalfallah O., Vodjdani G., Biguet N.F., Mallet J., Meloni R. The tissue-specific methylation of the human tyrosine hydroxylase gene reveals new regulatory elements in the first exon. Journal of Neurochemistry 2005, 94:129-139.
4. Baker H., Kawano T., Margolis F.L., Joh T.H. Transneuronal regulation of tyrosine hydroxylase expression in olfactory bulb of mouse and rat. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 1983, 3:69-78.
5. Baker H., Morel K., Stone D.M., Maruniak J.A. Adult naris closure profoundly reduces tyrosine hydroxylase expression in mouse olfactory bulb. Brain Research 1993, 614:109-116.
6. Baker S.A., Baker K.A., Hagg T. Dopaminergic nigrostriatal projections regulate neural precursor proliferation in the adult mouse subventricular zone. The European Journal of Neuroscience 2004, 20:575-579.
7. Ballas N., Battaglioli E., Atouf F., Andres M.E., Chenoweth J., Anderson M.E., Burger C., Moniwa M., Davie J.R., Bowers W.J., Federoff H.J., Rose D.W., Rosenfeld M.G., Brehm P., Mandel G. Regulation of neuronal traits by a novel transcriptional complex. Neuron 2001, 31:353-365.
8. Ballas N., Grunseich C., Lu D.D., Speh J.C., Mandel G. REST and its corepressors mediate plasticity of neuronal gene chromatin throughout neurogenesis. Cell 2005, 121:645-657.
9. Banasr M., Hery M., Printemps R., Daszuta A. Serotonin-induced increases in adult cell proliferation and neurogenesis are mediated through different and common 5-HT receptor subtypes in the dentate gyrus and the subventricular zone. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology 2004, 29:450-460.
10. Bolteus A.J., Bordey A. GABA release and uptake regulate neuronal precursor migration in the postnatal subventricular zone. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 2004, 24:7623-7631.
11. Bovetti S., Gribaudo S., Puche A.C., De Marchis S., Fasolo A. From progenitors to integrated neurons: role of neurotransmitters in adult olfactory neurogenesis. Journal of Chemical Neuroanatomy 2011, 42:304-316.
12. Brezun J.M., Daszuta A. Depletion in serotonin decreases neurogenesis in the dentate gyrus and the subventricular zone of adult rats. Neuroscience 1999, 89:999-1002.
13. Brill M.S., Snapyan M., Wohlfrom H., Ninkovic J., Jawerka M., Mastick G.S., Ashery-Padan R., Saghatelyan A., Berninger B., Gotz M. A dlx2- and pax6-dependent transcriptional code for periglomerular neuron specification in the adult olfactory bulb. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 2008, 28:6439-6452.
14. Castiglione M., Calafiore M., Costa L., Sortino M.A., Nicoletti F., Copani A. Group I metabotropic glutamate receptors control proliferation, survival and differentiation of cultured neural progenitor cells isolated from the subventricular zone of adult mice. Neuropharmacology 2008, 55:560-567.
15. Cigola E., Volpe B.T., Lee J.W., Franzen L., Baker H. Tyrosine hydroxylase expression in primary cultures of olfactory bulb: role of L-type calcium channels. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 1998, 18:7638-7649.
16. Darcy D.P., Isaacson J.S. L-type calcium channels govern calcium signaling in migrating newborn neurons in the postnatal olfactory bulb. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 2009, 29:2510-2518.
17. Davila N.G., Blakemore L.J., Trombley P.Q. Dopamine modulates synaptic transmission between rat olfactory bulb neurons in culture. Journal of Neurophysiology 2003, 90:395-404.
18. De Marchis S., Temoney S., Erdelyi F., Bovetti S., Bovolin P., Szabo G., Puche A.C. GABAergic phenotypic differentiation of a subpopulation of subventricular derived migrating progenitors. The European Journal of Neuroscience 2004, 20:1307-1317.
19. Di Giorgi Gerevini V.D., Caruso A., Cappuccio I., Ricci Vitiani L., Romeo S., Della Rocca C., Gradini R., Melchiorri D., Nicoletti F. The mGlu5 metabotropic glutamate receptor is expressed in zones of active neurogenesis of the embryonic and postnatal brain. Brain Research. Developmental Brain Research 2004, 150:17-22.
20. Dong E., Agis-Balboa R.C., Simonini M.V., Grayson D.R., Costa E., Guidotti A. Reelin and glutamic acid decarboxylase67 promoter remodeling in an epigenetic methionine-induced mouse model of schizophrenia. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:12578-12583.
21. Dong E., Guidotti A., Grayson D.R., Costa E. Histone hyperacetylation induces demethylation of reelin and 67-kDa glutamic acid decarboxylase promoters. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:4676-4681.
22. Ennis M., Zhou F.M., Ciombor K.J., Aroniadou-Anderjaska V., Hayar A., Borrelli E., Zimmer L.A., Margolis F., Shipley M.T. Dopamine D2 receptor-mediated presynaptic inhibition of olfactory nerve terminals. Journal of Neurophysiology 2001, 86:2986-2997.
23. Fasano C.A., Phoenix T.N., Kokovay E., Lowry N., Elkabetz Y., Dimos J.T., Lemischka I.R., Studer L., Temple S. Bmi-1 cooperates with Foxg1 to maintain neural stem cell self-renewal in the forebrain. Genes and Development 2009, 23:561-574.
24. Feierstein C.E., Lazarini F., Wagner S., Gabellec M.M., de Chaumont F., Olivo-Marin J.C., Boussin F.D., Lledo P.M., Gheusi G. Disruption of adult neurogenesis in the olfactory bulb affects social interaction but not maternal behavior. Frontiers in Behavioral Neuroscience 2010, 4:176.
25. Ferron S.R., Charalambous M., Radford E., McEwen K., Wildner H., Hind E., Morante-Redolat J.M., Laborda J., Guillemot F., Bauer S.R., Farinas I., Ferguson-Smith A.C. Postnatal loss of Dlk1 imprinting in stem cells and niche astrocytes regulates neurogenesis. Nature 2011, 475:381-385.
26. Freundlieb N., Francois C., Tande D., Oertel W.H., Hirsch E.C., Hoglinger G.U. Dopaminergic substantia nigra neurons project topographically organized to the subventricular zone and stimulate precursor cell proliferation in aged primates. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 2006, 26:2321-2325.
27. Gandhi R., Luk K.C., Rymar V.V., Sadikot A.F. Group I mGluR5 metabotropic glutamate receptors regulate proliferation of neuronal progenitors in specific forebrain developmental domains. Journal of Neurochemistry 2008, 104:155-172.
28. Guidotti A., Auta J., Chen Y., Davis J.M., Dong E., Gavin D.P., Grayson D.R., Matrisciano F., Pinna G., Satta R., Sharma R.P., Tremolizzo L., Tueting P. Epigenetic GABAergic targets in schizophrenia and bipolar disorder. Neuropharmacology 2011, 60:1007-1016.
29. Hinds J.W. Autoradiographic study of histogenesis in the mouse olfactory bulb. I. Time of origin of neurons and neuroglia. The Journal of Comparative Neurology 1968, 134:287-304.
30. Hoglinger G.U., Rizk P., Muriel M.P., Duyckaerts C., Oertel W.H., Caille I., Hirsch E.C. Dopamine depletion impairs precursor cell proliferation in Parkinson disease. Nature Neuroscience 2004, 7:726-735.
31. Hsia A.Y., Vincent J.D., Lledo P.M. Dopamine depresses synaptic inputs into the olfactory bulb. Journal of Neurophysiology 1999, 82:1082-1085.
32. Hsieh J., Gage F.H. Chromatin remodeling in neural development and plasticity. Current Opinion in Cell Biology 2005, 17:664-671.
33. Jawerka M., Colak D., Dimou L., Spiller C., Lagger S., Montgomery R.L., Olson E.N., Wurst W., Gottlicher M., Gotz M. The specific role of histone deacetylase 2 in adult neurogenesis. Neuron Glia Biology 2010, 6:93-107.
34. Joh T.H., Geghman C., Reis D. Immunochemical demonstration of increased accumulation of tyrosine hydroxylase protein in sympathetic ganglia and adrenal medulla elicited by reserpine. Proceedings of the National Academy of Sciences of the United States of America 1973, 70:2767-2771.
35. Katarova Z., Mugnaini E., Sekerkova G., Mann J.R., Aszodi A., Bosze Z., Greenspan R., Szabo G. Regulation of cell-type specific expression of lacZ by the 5'-flanking region of mouse GAD67 gene in the central nervous system of transgenic mice. The European Journal of Neuroscience 1998, 10:989-999.
36. Kessler M.A., Yang M., Gollomp K.L., Jin H., Iacovitti L. The human tyrosine hydroxylase gene promoter. Brain Research. Molecular Brain Research 2003, 112:8-23.
37. Kilbourne E.J., Osaka H., Sabban E.L. Hypomethylation of the rat tyrosine hydroxylase gene correlates with its expression in several cell types. Brain Research. Developmental Brain Research 1991, 58:143-146.
38. Kim T.E., Park M.J., Choi E.J., Lee H.S., Lee S.H., Yoon S.H., Oh C.K., Lee B.J., Kim S.U., Lee Y.S., Lee M.A. Cloning and cell type-specific regulation of the human tyrosine hydroxylase gene promoter. Biochemical and Biophysical Research Communications 2003, 312:1123-1131.
39. Kiyokage E., Pan Y.Z., Shao Z., Kobayashi K., Szabo G., Yanagawa Y., Obata K., Okano H., Toida K., Puche A.C., Shipley M.T. Molecular identity of periglomerular and short axon cells. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 2010, 30:1185-1196.
40. Kobayashi T., Ebihara S., Ishii K., Kobayashi T., Nishijima M., Endo S., Takaku A., Sakagami H., Kondo H., Tashiro F., Miyazaki J., Obata K., Tamura S., Yanagawa Y. Structural and functional characterization of mouse glutamate decarboxylase 67 gene promoter. Biochimica et Biophysica Acta 2003, 1628:156-168.
41. Kohwi M., Osumi N., Rubenstein J.L., Alvarez-Buylla A. Pax6 is required for making specific subpopulations of granule and periglomerular neurons in the olfactory bulb. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 2005, 25:6997-7003.
42. Kosaka K., Toida K., Aika Y., Kosaka T. How simple is the organization of the olfactory glomerulus?: the heterogeneity of so-called periglomerular cells. Neuroscience Research 1998, 30:101-110.
43. Kundakovic M., Chen Y., Guidotti A., Grayson D.R. The reelin and GAD67 promoters are activated by epigenetic drugs that facilitate the disruption of local repressor complexes. Molecular Pharmacology 2009, 75:342-354.
44. Lau C.G., Murthy V.N. Activity-dependent regulation of inhibition via GAD67. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 2012, 32:8521-8531.
45. Lazarini F., Lledo P.M. Is adult neurogenesis essential for olfaction?. Trends in Neurosciences 2011, 34:20-30.
46. Lazarini F., Mouthon M.A., Gheusi G., de Chaumont F., Olivo-Marin J.C., Lamarque S., Abrous D.N., Boussin F.D., Lledo P.M. Cellular and behavioral effects of cranial irradiation of the subventricular zone in adult mice. PloS One 2009, 4:e7017.
47. Lim D.A., Huang Y.C., Swigut T., Mirick A.L., Garcia-Verdugo J.M., Wysocka J., Ernst P., Alvarez-Buylla A. Chromatin remodelling factor Mll1 is essential for neurogenesis from postnatal neural stem cells. Nature 2009, 458:529-533.
48. Liu N., Cigola E., Tinti C., Jin B.K., Conti B., Volpe B.T., Baker H. Unique regulation of immediate early gene and tyrosine hydroxylase expression in the odor-deprived mouse olfactory bulb. Journal of Biological Chemistry 1999, 274:3042-3047.
49. Liu X., Wang Q., Haydar T.F., Bordey A. Nonsynaptic GABA signaling in postnatal subventricular zone controls proliferation of GFAP-expressing progenitors. Nature Neuroscience 2005, 8:1179-1187.
50. Lois C., Alvarez-Buylla A. Long-distance neuronal migration in the adult mammalian brain. Science 1994, 264:1145-1148.
51. MacDonald J.L., Gin C.S., Roskams A.J. Stage-specific induction of DNA methyltransferases in olfactory receptor neuron development. Developmental Biology 2005, 288:461-473.
52. MacDonald J.L., Roskams A.J. Histone deacetylases 1 and 2 are expressed at distinct stages of neuro-glial development. Developmental Dynamics: An Official Publication of the American Association of Anatomists 2008, 237:2256-2267.
53. Macdonald J.L., Verster A., Berndt A., Roskams A.J. MBD2 and MeCP2 regulate distinct transitions in the stage-specific differentiation of olfactory receptor neurons. Molecular and Cellular Neurosciences 2010, 44:55-67.
54. Matrisciano F., Dong E., Gavin D.P., Nicoletti F., Guidotti A. Activation of group II metabotropic glutamate receptors promotes DNA demethylation in the mouse brain. Molecular Pharmacology 2011, 80:174-182.
55. Matsushita N., Okada H., Yasoshima Y., Takahashi K., Kiuchi K., Kobayashi K. Dynamics of tyrosine hydroxylase promoter activity during midbrain dopaminergic neuron development. Journal of Neurochemistry 2002, 82:295-304.
56. McMillian M.K., Mullis S.B., Wu G.C., Hudson P.M., Pennypacker K.R., Hong J.S. Regulation of tyrosine hydroxylase in olfactory bulb cultures: selective inhibition of depolarization-induced increase by endogenous opioids. Brain Research 1994, 658:105-111.
57. Molofsky A.V., Pardal R., Iwashita T., Park I.K., Clarke M.F., Morrison S.J. Bmi-1 dependence distinguishes neural stem cell self-renewal from progenitor proliferation. Nature 2003, 425:962-967.
58. Moreno M.M., Linster C., Escanilla O., Sacquet J., Didier A., Mandairon N. Olfactory perceptual learning requires adult neurogenesis. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:17980-17985.
59. O'Keeffe G.C., Barker R.A., Caldwell M.A. Dopaminergic modulation of neurogenesis in the subventricular zone of the adult brain. Cell Cycle 2009, 8:2888-2894.
60. O'Keeffe G.C., Tyers P., Aarsland D., Dalley J.W., Barker R.A., Caldwell M.A. Dopamine-induced proliferation of adult neural precursor cells in the mammalian subventricular zone is mediated through EGF. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:8754-8759.
61. Panzanelli P., Fritschy J.M., Yanagawa Y., Obata K., Sassoe-Pognetto M. GABAergic phenotype of periglomerular cells in the rodent olfactory bulb. The Journal of Comparative Neurology 2007, 502:990-1002.
62. Parrish-Aungst S., Kiyokage E., Szabo G., Yanagawa Y., Shipley M.T., Puche A.C. Sensory experience selectively regulates transmitter synthesis enzymes in interglomerular circuits. Brain Research 2011, 1382:70-76.
63. Parrish-Aungst S., Shipley M.T., Erdelyi F., Szabo G., Puche A.C. Quantitative analysis of neuronal diversity in the mouse olfactory bulb. The Journal of Comparative Neurology 2007, 501:825-836.
64. Pignatelli A., Ackman J.B., Vigetti D., Beltrami A.P., Zucchini S., Belluzzi O. A potential reservoir of immature dopaminergic replacement neurons in the adult mammalian olfactory bulb. Pflugers Archiv: European Journal of Physiology 2009, 457:899-915.
65. Plachez C., Puche A.C. Early specification of GAD67 subventricular derived olfactory interneurons. Journal of Molecular Histology 2012, 43:215-221.
66. Platel J.C., Dave K.A., Bordey A. Control of neuroblast production and migration by converging GABA and glutamate signals in the postnatal forebrain. The Journal of Physiology 2008, 586:3739-3743.
67. Platel J.C., Heintz T., Young S., Gordon V., Bordey A. Tonic activation of GLUK5 kainate receptors decreases neuroblast migration in whole-mounts of the subventricular zone. The Journal of Physiology 2008, 586:3783-3793.
68. Puche A.C., Shipley M.T. Odor-induced, activity-dependent transneuronal gene induction in vitro: mediation by NMDA receptors. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 1999, 19:1359-1370.
69. Ramirez M., Gutierrez R. Activity-dependent expression of GAD67 in the granule cells of the rat hippocampus. Brain Research 2001, 917:139-146.
70. Roopra A., Sharling L., Wood I.C., Briggs T., Bachfischer U., Paquette A.J., Buckley N.J. Transcriptional repression by neuron-restrictive silencer factor is mediated via the Sin3-histone deacetylase complex. Molecular and Cellular Biology 2000, 20:2147-2157.
71. Saino-Saito S., Sasaki H., Volpe B.T., Kobayashi K., Berlin R., Baker H. Differentiation of the dopaminergic phenotype in the olfactory system of neonatal and adult mice. The Journal of Comparative Neurology 2004, 479:389-398.
72. Schimmel J.J., Crews L., Roffler-Tarlov S., Chikaraishi D.M. 4.5kb of the rat tyrosine hydroxylase 5' flanking sequence directs tissue specific expression during development and contains consensus sites for multiple transcription factors. Brain Research. Molecular Brain Research 1999, 74:1-14.
73. Sequerra E.B., Gardino P., Hedin-Pereira C., de Mello F.G. Putrescine as an important source of GABA in the postnatal rat subventricular zone. Neuroscience 2007, 146:489-493.
74. Sheikh B.N., Dixon M.P., Thomas T., Voss A.K. Querkopf is a key marker of self-renewal and multipotency of adult neural stem cells. Journal of Cell Science 2012, 125:295-309.
75. Sultan S., Mandairon N., Kermen F., Garcia S., Sacquet J., Didier A. Learning-dependent neurogenesis in the olfactory bulb determines long-term olfactory memory. FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology 2010, 24:2355-2363.
76. Szabo G., Katarova Z., Kortvely E., Greenspan R.J., Urban Z. Structure and the promoter region of the mouse gene encoding the 67-kD form of glutamic acid decarboxylase. DNA and Cell Biology 1996, 15:1081-1091.
77. Toida K. Synaptic organization of the olfactory bulb based on chemical coding of neurons. Anatomical Science International 2008, 83:207-217.
78. Valley M.T., Mullen T.R., Schultz L.C., Sagdullaev B.T., Firestein S. Ablation of mouse adult neurogenesis alters olfactory bulb structure and olfactory fear conditioning. Frontiers in Neuroscience 2009, 3:51.
79. Wang D.D., Krueger D.D., Bordey A. GABA depolarizes neuronal progenitors of the postnatal subventricular zone via GABAA receptor activation. The Journal of Physiology 2003, 550:785-800.
80. Wilson D.A., Sullivan R.M. The D2 antagonist spiperone mimics the effects of olfactory deprivation on mitral/tufted cell odor response patterns. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 1995, 15:5574-5581.
81. Wu H., Coskun V., Tao J., Xie W., Ge W., Yoshikawa K., Li E., Zhang Y., Sun Y.E. Dnmt3a-dependent nonpromoter DNA methylation facilitates transcription of neurogenic genes. Science 2010, 329:444-448.
82. Yanagawa Y., Kobayashi T., Kamei T., Ishii K., Nishijima M., Takaku A., Tamura S. Structure and alternative promoters of the mouse glutamic acid decarboxylase 67 gene. The Biochemical Journal 1997, 326(Pt 2):573-578.
83. Yang C., Kim H.S., Seo H., Kim K.S. Identification and characterization of potential cis-regulatory elements governing transcriptional activation of the rat tyrosine hydroxylase gene. Journal of Neurochemistry 1998, 71:1358-1368.
84. Yang J.W., Choi E.Y., Park M.J., Lee M.A. Expression of tyrosine hydroxylase is epigenetically regulated in neural stem cells. Biochemical and Biophysical Research Communications 2011, 414:712-718.
85. Young S.Z., Taylor M.M., Bordey A. Neurotransmitters couple brain activity to subventricular zone neurogenesis. The European Journal of Neuroscience 2011, 33:1123-1132.