Transient developmental expression of monoamine transporters in the rodent forebrain

Journal of Comparative Neurology

Volumn 401, Issue 4, 1998, Pages 506-524

  Lebrand, Cecile ^a   Cases, Olivier ^a   Wehrlé, Rosine ^a   Blakely, Randy D ^b   Edwards, Robert H ^c   Gaspar, Patricia ^a  

^a PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Development; Norepinephrine transporter; Sensory pathways; Serotonin transporter; Thalamus; Vesicular monoamine transporter

Indexed keywords

CARRIER PROTEIN; NORADRENALIN; SEROTONIN;

ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; FOREBRAIN; GENE EXPRESSION REGULATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN TRANSPORT; SEROTONIN BRAIN LEVEL; TISSUE DISTRIBUTION;

EID: 0032583187     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(sici)1096-9861(19981130)401:4<506::aid-cne5>3.0.co;2-%23     Document Type: Article

References (79)

1. Adelbrecht, C., Y. Agid , and R. Raisman-Vozari (1996) Effect of the weaver mutation on the expression of dopamine membrane transporter, tyrosine hydroxylase and vesicular monoamine transporter in dopaminergic neurons of the substantia nigra and the ventral tegmental area. Brain Res. Mol. Brain Res. 43:291-300.
2. Altman, J. and S.A. Bayer (1995) Atlas of Prenatal Rat Brain Development. Boca Raton: CRC Press.
3. Auvinen, S. and P. Panula (1988) Development of histamine-immunoractive neurons in the rat brain. J. Comp. Neurol. 276:289-303.
4. Barker, E.L. and R.D. Blakely (1995) Norepinephrine and serotonin transporters: Molecular targets of antidepressant drugs. In F.E. Bloom and D.J. Kupfer (eds): Psychopharmacology: The Fourth Generation of Progress. New York: Raven Press, pp. 321-333.
5. Bayer, S.A. (1985) Hippocampal region. In G. Paxinos (ed): The Rat Nervous System. Kensington: Academic Press, pp 335-352.
6. Beaudet, A. and L. Descarries (1984) Fine structure of monoamine axon terminals in cerebral cortex. In Descarries L, T.R. Reader, and H.H. Jasper (eds): Monoamine Innervation of Cerebral Cortex. New York: Alan R. Liss, pp 77-94.
7. Bengel, D., D.L. Murphy, A.M. Andrews, C.H. Wichems, D. Feltner, A.Heils, R. Mossner, H. Westphal, and K.-P. Lesch (1996) Targeted disruption of the murine serotonin transporter gene. Soc. Neurosci. Abst. 1:508.
8. Bennett-Clarke, C.A., M.J. Leslie, R.D. Lane, and R.W. Rhoades (1994) Effect of serotonin depletion on vibrissa-related patterns of thalamic afferents in the rat's somatosensory cortex. J. Neurosci. 14:7594-7607.
9. Berendse, H.W. and H.J. Groenewegen (1991) Restricted cortical termination fields of the midline and intracortical thalamic nuclei in the rat. Neuroscience 42:73-102.
10. Berger, B., C. Verney, P. Gaspar, and A. Febvret (1985) Transient expression of TH immunoreactivity in some neurons of the rat neocortex during postnatal development. Dev. Brain Res. 23:141-144.
11. Blakely, R.D., H.E. Berson, R.T. Fremeau, M.G. Caron, M.M. Peek, H.K. Prince, and C.C. Bradley (1991) Cloning and expression of a functional serotonin tranporter from rat brain. Nature 354:66-70.
12. Blakely, R.D., L.J. De Felice, and H.C. Hartzell (1994) Molecular physiology of norepinephrine and serotonin transporters. J. Exp. Biol. 196:263-281.
13. Blue, M.E. and J.G. Parnavelas (1983) The formation and maturation of synapses in the visual cortex of the rat. I. Quantitative analysis. J. Neurocytol. 12:599-616.
14. Blue, M.E.,R.S. Erzurumlu, and S. Jhaveri (1991) A comparison of pattern formation by thalamocortical and serotonergic afferents in the rat barrel field cortex. Cereb. Cortex 1:380-389.
15. Brüning, G., O. Liangos, and H. G. Baumgarten (1997) Prenatal development of the serotonin transporter in mouse brain. Cell Tissue Res. 289:211-221.
16. Buznikov, G.A. and Y.B. Shmukler (1981) Possible role of "prenervous" neurotransmitters in cellular interactions of early embryogenesis. Neurochem. Res. 6:55-68.
17. Cases, O., T. Vitalis, I. Seif, E. De Maeyer, C. Sotelo, and P. Gaspar (1996) Lack of barrels in the somatosensory cortex of monoamine oxidase A deficient mice: Role of excess serotonin during the critical period. Neuron 16:197-307.
18. Cases, O., C. Lebrand, B. Giros, T. Vitalis, E. De Maeyer, M. G. Caron, D. J. Price, P. Gaspar, and I. Seif (1998) Plasma membrane transporters of serotonin, dopamine, and norepinephrine mediate serotonin accumulation in atypical locations in the developing brain of monoamine oxidase A knockouts. J. Neurosci. 18:6914-6927.
19. Caviness, V.S. and D.O. Frost (1980) Tangential organization of thalamic projections to the neocortex in the mouse. J. Comp. Neurol. 194:335-367.
20. Cechetto, F.D. and C.B. Saper (1988) Evidence for a viscerotopic sensory representation in the cortex and thalamus in the rat. J. Comp. Neurol. 262:27-45.
21. Champagnat, J. and G. Fortin (1997) Primordial respiratory-like rhythm generation in the vertebrate embryo. T.I.N.S. 20:119-124.
22. D'Amato, R., M.E. Blue, B.L. Largent, D.R. Lynch, D.J. Ledbetter, M.E. Molliver, and S.H. Snyder (1987) Ontogeny of the serotonergic projection to rat neocortex: Transient expression of a dense innervation to primary sensory areas. Proc. Natl. Acad. Sci. USA 84:4322-4326.
23. Erickson, J.D., L. Eiden, and B. Hoffman (1992) Expression cloning of a reserpine-sensitive vesicular monoamine transporter. Proc. Natl. Acad. Sci. USA 89:10993-10997.
24. Faull, R.L.M. and W.R. Mehler (1985) Thalamus. In Paxinos G (ed): The Rat Nervous System. Kensington: Academic Press, pp. 129-168.
25. Fishkes, H. and G. Rudnick (1981) Bioenergetics of serotonin transport by membrane vesicles derived from platelets dense granules. J. Biol. Chem. 257:5671-5677.
26. Fon, E.A., B.C. Sun, E. Pothos, N. Killeen, D. Sulzer, and R.H. Edwards (1997) Vesicular transport regulates monoamine storage and release but is not essential for amphetamine action. Neuron 19:1271-1283.
27. Fontaine, B. and J.P. Changeux (1989) Localization of nicotinic acetylcholine receptor a subunit transcripts during myogenesis and motor endplate development in the chick. J. Cell Biol. 108:1025-1037.
28. Franklin, K.B.J. and G. Paxinos (1997) The Mouse Brain in Stereotaxic Coordinates. San Diego: Academic Press.
29. Frost, D.O. and V.S. Caviness (1980) Radial organization of thalamic projections to the neocortex in the mouse. J. Comp. Neurol. 194:369-393.
30. Fujimiya, M., H. Kimura, and T. Maeda (1986) Postnatal development of serotonin nerve fibers in the somatosensory cortex of mice studied by immunohistochemistry. J. Comp. Neurol. 246:191-201.
31. Fuxe, K. and L.F. Agnati (1991) Two principal modes of electrochemical communication in the brain: Volume versus wiring transmission. In K. Fuxe and L.F. Agnati (eds): Volume Transmission in the Brain. New York: Raven Press, pp. 1-9.
32. Hanley, M.R. (1989) Mitogenic neurotransmitters. Nature 340:97.
33. Hansson, S.R., E. Mezey, and B.J. Hoffman (1998) Serotonin transporter messenger RNA in the developing rat brain : Early expression in serotonergic neurons and transient expression in non-serotonergic neurons. Neuroscience 83:1185-1201.
34. Henry, J.P. and D. Scherman (1989) Radioligands of the vesicular transporter and their use as markers of monoamine storage vesicles. Biochem. Pharamacol. 38:2395-2404.
35. Herkenham, M. (1980) Laminar organization of thalamic projections to the rat neocortex. Science. 207:532-535.
36. Hoffman, B.J., E. Mezey, and M.J. Brownstein (1991) Cloning of a serotonin transporter affected by antidepressants. Science 254:579-580.
37. Igvy-May, N., H. Tamir, and M.D. Gershon (1994) Synaptic properties of serotonergic growth cones in developing rat brain. J. Neurosci. 14:1011-129.
38. Jones, E.G. (1983) The thalamus. In: Chemical Neuroanatomy. New York: Raven Press, pp. 257-293.
39. Kanner, B. and S. Schuldiner (1987) Mechanism of transport and storage of neurotransmitters. Crit. Rev. Biochem 22:1-38.
40. Katz, L.C. and C.J. Shatz (1996) Synaptic activity and the construction of cortical circuits. Science 274:1133-1138.
41. Krejci, E., B. Gasnier, D. Botton, M.F. Isambert, C. Sagne, J. Gagnon, J. Massoulie, and J.P. Henry (1993) Expression and regulation of the bovine vesicular monoamine transporter gene. FEBS Lett. 335:27-32.
42. Kristt, D.A. (1979) Development of neocortical circuitry: quantitative ultrastructutral analysis of putative monoaminergic synapses. Brain Res. 178:69-88.
43. Lauder, J.M., H. Tamir, and T.W. Sadler (1988) Serotonin and morphogenesis. I. Sites of serotonin uptake and binding protein immunoreactivity in the midgestation mouse embryo. Development 102:709-720.
44. Lebrand, C., O. Cases, C. Aldebrecht, A. Doye, C. Alvarez, S. El-Mestikawy, I. Seif, and P. Gaspar (1996) Transient uptake and storage of serotonin in developing thalamic neurons. Neuron 17:823-835.
45. Lee, S.L., W.W. Wang, B.J. Moore, and B.L. Fanburg (1991) Dual effect of serotonin on growth of bovine pulmonary artery smooth muscle cells in culture. Circulation Res. 68:1362-1368.
46. Li, X.-G., S.L. Florence, and J.H. Kaas (1990) Areal distributions of cortical neurons projecting to different levels of the caudal brain stem and spinal cord in rats. Somatosensory Motor Res. 7:315-335.
47. Lidov, H.G.W. and M. E. Molliver (1982) An immunohistochemical study of serotonin neuron development in the rat: Ascending pathways and terminals fields. Brain. Res. Bull. 8:389-430.
48. Lindvall, O. and A. Björklund (1978) Organization of catecholamine neurons in the rat nervous system. In Iveresen L.L., and S.D. Iversen (eds): Handbook of Psychopharmacology, Vol 9. New York: Plenum Publishing Corporation, pp. 139-230.
49. Liu, Y., D. Peter, A. Roghani, S. Schuldiner, G.G. Privé, D. Eisenberg, N. Brecha, and R.H. Edwards (1992) A cDNA that suppresses MPP+ toxicity encodes a vesicular amine transporter. Cell 70:539-551.
50. Liu, Y. and R.H. Edwards (1997) The role of vesicular transport proteins in synaptic transmission and neural degeneration. Annu. Rev. Neurosci. 20:125-156.
51. Lockerbie, R.O., V.E. Miller, and K.H. Pfenninger (1991) Regulated plasma-lemmal expansion in nerve growth cones. J. Cell Biol. 112:1215-1227.
52. Olson, L. and A. Seiger (1972) Early prenatal ontogeny of central monoamine neurons in the rat: Fluorescence histochemical observations. Z. Anat. Entwickl. -Gesch. 137:301-316.
53. Osterheld-Haas, M.C. and J.P. Hornung (1996) Laminar development of the mouse barrel cortex : Effects of neurotoxins against monoamines. Exp. Brain Res. 110:183-195.
54. Ottersen, O.P. and J. Storm-Mathisen (1984) Neurons containing or accumulating transmitter amino acids. In A. Björklund, T. Hökfelt, and M. J. Kuhar (eds): Handbook of Chemical Neuroanatomy, Vol. 3: Classical Transmitters and Receptors in the CNS. Amsterdam: Elsevier, pp. 141-246.
55. Pacholczyk, T., R.D. Blakely, and S.G. Amara (1991) Expression cloning of a cocaine and antidepressant-sensitive human norepinephrinee transporter. Nature 350:350-354.
56. Paxinos, G. and C. Watson (1986) The Rat Brain in Stereotaxic Coordinates. San Diego: Academic Press.
57. Peter, D., Y. Liu, C. Stermini, R. de Giorgio, N. Brecha, and R.H. Edwards (1995) Differential expression of two vesicular monoamine transporters. J. Neurosci. 15:6179-6188.
58. Qian, Y., H.E. Melikian, D.B. Rye, A.I. Levey, and R.D. Blakely (1995) Identification and characterization of antidepressant-sensitive serotonin transporter proteins using site-specific antibodies. J. Neurosci. 15:1261-1274.
59. Rhoades, R.W., C.A. Bennett-Clarke, N.L. Chiaia, F.A. White, G.J. McDonald, J.H. Haring, and M.F. Jacquin (1990) Development and lesion induced reorganization of the cortical representation of the rat's body surface as revealed by immunocytochemistry for serotonin. J. Comp. Neurol. 293:190-207.
60. Roubertoux, P.L., M. Nosten-Bertrand, C. Cohen-Salmon, and L. L'Hotellier (1992) Behavioral development: A tool for genetic analysis in mice. In D. Goldowitz, D.Wahlsten, and R.E. Wimer (eds):Techniques for the Genetic Analysis of Brain and Behavior: Focus on the Mouse. Amsterdam: Elsevier, pp. 423-441.
61. Rudnick, G. and J. Clark (1993) From synapse to vesicle: The reuptake and storage of biogenic amine neurotransmitters. Biochem Biophys Acta 1144:249-263.
62. Ryugo, D.K. and H.P. Killackey (1974) Differential telencephalic projection of the medial and ventral divisions of the medial geniculate body of the rat. Brain Res. 82:173-177.
63. Schroeter, S. and R.D. Blakely (1996) Drug targets in the embryo: Studies on the cocaine and antidepressant-sensitive serotonin transporter Ann. NY Acad. Sci. 801:239-255.
64. Schroeter, S., A.I. Levey, and R.D. Blakely (1997) Polarized expression of the antidepressant-sensitive serotonin transporter in epinephrine-synthesizing chromaffin cells of the rat adrenal gland. Molec. Cell Neurosci. 9:170-184.
65. Shuey, D.L., T.W. Sadler, and J.M. Lauder (1992) Serotonin as a regulator of craniofacial morphogenesis: Site specific malformations following exposure to serotonin uptake inhibitors. Teratology 46:367-378.
66. Soeda, H., H. Tatsumi, and Y. Katayama (1997) Neurotransmitter release from growth cones of rat dorsal root ganglion neurons in culture. Neuroscience 77:1187-1199.
67. Specht, L.A., V.M. Pickel, T.H. Joh, and D.J. Reis (1981) Light microscopic immunocytochemical localization of tyrosine hydroxylase in prenatal rat brain. I. Early ontogeny. J. Comp. Neurol. 199:233-253.
68. Steinbusch, H.W.M. (1984) Serotonin-immunoreactive neurons and their projections in the CNS. In Björklund A, T. Hökfelt, M.J. Kuhar (eds): Handbook of Chemical Neuroanatomy, Vol 3: Classical Transmitters and Transmitter Receptors in the CNS. Amsterdam: Elsevier, pp. 68-125.
69. Stoykova, A., R. Fritsch, C. Walther, and P. Gruss (1996) Forebrain patterning defects in small eye mutant mice. Development 122:3453-3465.
70. Tao-Cheng, J.H. and F.C. Zhou (1997) Serotonin transporter is distributed on the plasma membrane along the axon but not the soma or dendrite in the rat brain. Soc. Neurosci. Abst. 1:405.
71. Upton, L.A., C. Lebrand, N. Salichon, P. Ezan, I. Seif, and P. Gaspar (1997) Serotonin uptake in retinal ganglion cells during development of normal and MAOA-knockout mice. Society for Neuroscience 23:256.8.
72. Vanhala, A., A. Yamatodani, and P. Panula (1998) Distribution of histamine-, 5-hydroxytrytamine and tyrosine hydroxylase-immunoreactive neurons and nerve fibers in developing rat brain. J. Comp. Neurol. 347:101-114.
73. Vanhatalo, S. and S. Soinila (1995) Release of false transmitter serotonin from the dopaminergic nerve terminals of the rat pituitary intermediate lobe. Neurosci. Res. 22:367-374.
74. Verney, C., P. Gaspar, A. Febvret, and B. Berger (1988) Transient tyrosine hydroxylase-like immunoreactive neurons contain somatostatin and substance P in the developing amygdala and bed nucleus of the stria terminalis of the rat. Dev. Brain Res. 42:45-58.
75. Vitalis, T., O. Cases, J. Callebert, J.M. Launay, D.J. Price, I. Seif, and P. Gaspar (1998) Effects of monoamine oxidase A inhibition on barrel formation in the mouse somatosensory cortex: Determination of a sensitive developmental period. J. Comp. Neurol. 393:169-184.
76. Wade, P.R., J. Chen, B. Jaffe, I.S. Kassem, R.D. Blakely, and M.D. Gershon (1996) Localisation and function of a 5-HT transporter in crypt epithelia of the gastrointestinal tract. J. Neurosci. 16:2352-2364.
77. Wallace, J.A. and J.M. Lauder (1983) Development of the serotonergic system in the rat embryo: An immunocytochemical study. Brain Res. Bull. 10:459-480.
78. Weihe, E., M.K-H. Schäfer, J.D. Erickson, and L.E. Eiden (1995) Localization of vesicular monoamine transporter isoforms (VMAT1 and VMAT2) to endocrine cells and neurons in rat. J. Molec. Neurosci. 5:149-164.
79. Xie, Z.P. and M.M. Poo (1986) initial events in the formation of neuromuscular synapse: Rapid induction of acetylcholine release from embryonic neuron. Proc. Natl. Acad. Sci. USA 83:7069-7073.