First trimester development of the human nigrostriatal dopamine system

Experimental Neurology

Volumn 139, Issue 2, 1996, Pages 227-237

  Almqvist, Per M ^a   Åkesson, Elisabet ^a   Wahlberg, Lars U ^a   Pschera, Helmut ^a   Seiger, Åke ^a   Sundström, Erik ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

DOPAMINE; TYROSINE 3 MONOOXYGENASE;

ARTICLE; BRAIN DEVELOPMENT; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; EMBRYO; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN TISSUE; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; NIGRONEOSTRIATAL SYSTEM; NORMAL HUMAN; PRIORITY JOURNAL;

EID: 0030157834     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1006/exnr.1996.0096     Document Type: Article

References (59)

1. 1. ALTMAN, J., AND S. A. BAYER. 1981. Development of the brain stem in the rat. V. Thymidine-radiographic study of the time of origin of neurons in the midbrain tegmentum. J. Comp. Neurol. 198: 677-716.
2. 2. ANGEVINE, J. B., JR. 1970. Time of neuron origin in the diencephalon of the mouse. J. Comp. Neurol. 139: 129-187.
3. 3. COCHARD, P., M. GOLDSTEIN, AND I. B. BLACK. 1978. Ontogenetic appearance and disappearance of tyrosine hydroxylase and catecholamines in the rat embryo. Proc. Natl. Acad. Sci. USA 75: 2986-2990.
4. 4. COKER, III. G. T., L. VINNEDGE, AND K. L. O'MALLEY. 1988. Characterization of rat and human tyrosine hydroxylase genes: functional expression of both promoters in neuronal and nonneuronal cell types. Biochem. Biophys. Res. Commun. 157: 1341-1347.
5. 5. DI PORZIO, U., A. ZUDDAS, D. B. COSENZA-MURPHY, AND J. L. BARKER. 1990. Early appearance of tyrosine hydroxylase immunoreactive cells in the mesencephalon of mouse embryos. Int. J. Dev. Neurosci. 8: 523-532.
6. 6. ENGLAND, M. A. 1988. A Color Atlas of Life before Birth. Normal Fetal Development. Wolfe Medical Publications, London.
7. 7. FINE, A. 1994. Human fetal tissue research: Practice, prospects and policy. Cell Transplant. 3: 113-145.
8. 8. FISZMAN, M. L., A. ZUDDAS, M. I. MASANA, J. L. BARKER, AND U. DI PORZIO. 1991. Dopamine synthesis preceeds dopamine uptake in the embryonic rat mesencephalic neurons. J. Neurochem. 56: 392-399.
9. 9. FOSTER, G. A., M. SCHULTZBERG, M. GOLDSTEIN, AND T. HÖKFELT. 1985. Ontogeny of phenylethanolamine N-methyltransferase- and tyrosine hydroxylase-like immunoreactivity in presumtive adrenaline neurons of the foetal rat central nervous system. J. Comp. Neurol. 236: 348-381.
10. 10. FREEMAN, T. B., M. S. SPENCE, B. D. BOSS, D. H. SPECTOR, R. E. STRECKER, C. W. OLANOW, AND J. H. KORDOWER. 1991. Development of dopaminergic neurons in the human substantia nigra. Exp. Neurol. 113: 344-353.
11. 11. FREEMAN, T. B., P. R. SANBERG, G. M. NAUERT, B. D. BOSS, D. SPECTOR, C. W. OLANOW, AND J. H. KORDOWER 1995. The influence of donor age on the survival of solid and suspension intrapenchymal human embryonic nigral grafts. Cell Transplant. 4:141-154.
12. 12. GARVER, D. L., AND J. R. SLADEK, JR. 1975. Monoamine distribution in the primate brain. I. Catecholamine-containing perikarya in the brain stem of Macaca speciosa. J. Comp. Neurol. 159: 289-304.
13. 13. GRIMA, B., A. LAMOUROUX, C. BONI, J. F. JULIEN, F. JAVOY-AGID, AND J. MALLET. 1987. A single human gene encoding multiple tyrosine hydroxylases with different predicted functional characteristics. Nature 326: 707-711.
14. 14. HANAWAY, J., J. A. MCCONNELL, AND M. G. NETSKY. 1970. Cytoarchitecture of the substantia nigra in the rat. Am. J. Anat. 129: 417-438.
15. 15. HAYCOCK, J. W. 1993. Multiple forms of tyrosine hydroxylase in human neuroblastoma cells: Quantitation with isoform-specific antibodies. J. Neurochem. 60: 493-502.
16. 16. HERMAN, J., AND N. ARBOUS. 1994. Dopaminergic neural grafts after fifteen years: Results and perspectives. Prog. Neurobiol. 44: 1-35.
17. 17. HORELLOU, P., B. LE BOURDELLES, J. CLOT-HUMBERT, B. GUIBERT, V. LEVIEL, AND J. MALLET. 1988. Multiple human tyrosine hydroxylase enzymes, generated through alternative splicing, have different specific activities in Xenopus oocytes. J. Neurochem. 51: 652-655.
18. 18. HSU, S. M., L. RAINE, AND H. FANGER. 1981. The use of antiavidin antibody and avidin-biotin-peroxidase complex in immunoperoxidase technics. Am. J. Clin. Pathol. 75: 816-821.
19. 19. IWATA, N., K. KOBAYASHI, T. SASAOKA, H. HIDAKA, AND T. NAGATSU. 1992. Structure of the mouse tyrosine hydroxylase gene. Biochem. Biophys. Res. Commun. 182: 348-354.
20. 20. JUNIEN, C., AND O. W. MCBRIDE. 1989. Report of the committee on the genetic constitution of chromosomal 11. Cytogenet. Cell Genet. 51: 226-258. [Review]
21. 21. KANEDA, N., K. KOBAYASHI, H. ICHINOSE, F. KISHI, A. NAKAZAWA, Y. KUROSAWA, K. FUJITA, AND T. NAGATSU. 1987. Isolation of a novel cDNA clone for human tyrosine hydroxylase: Alternative RNA splicing produces four kinds of mRNA from a single gene. Biochem. Biophys. Res. Commun. 146: 971-975.
22. 22. KANEDA, N., K. KOBAYASHI, H. ICHINOSE, T. SASAOKA, A. ISHII, K. KIUCHI, Y. KUROSAWA, K. FUJITA, AND T. NAGATSU. 1990. Molecular biological approaches to catecholamine neurotransmitters and brain aging. In T. Nagatsu and O. Hayaishi, Eds., Aging of the Brain: Cellular and Molecular Aspect of Brain Aging and Alzheimer's Disease. Japan Sci. Soc., Tokyo.
23. 23. KELLER, R., A. OKE, I. MEFFORD, AND R. N. ADAMS. 1976. Liquid Chromatographie analysis of catecholamines routine assay for regional brain mapping. Life Sci. 19: 995-1004.
24. 24. KOBAYASHI, K., K. KIUCHI, A. ISHII, N. KANEDA, Y. KUROSAWA, K. FUJITA, AND T. NAGATSU. 1988. Expression of four types of human tyrosine hydroxylase in COS cells. FEBS Lett. 238: 431-434.
25. 25. KONTUR, P. J., C. LERANTH, D. E. REDMOND, JR., R. H. ROTH, AND R. J. ROBBINS. 1993. Tyrosine hydroxylase immunoreactivity and monoamine and metabolite levels in cryopreserved human fetal ventral mesencephalon. Exp. Neurol. 121: 172-180.
26. 26. KORDOWER, J., T. B. FREEMAN, AND B. J. SNOW. 1995. Neuropathological evidence of graft survival and striatal reinnervation after the transplantation of fetal mesencephalic tissue in a patient with Parkinson's disease. N. Engl. J. Med. 332: 1118-1124.
27. 27. LAEMMLI, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
28. 28. LAUDER, J. M., AND F. E. BLOOM. 1974. Ontogeny of the monoamine neurons in the locus coeruleus, raphe nuclei of the rat. I. Cell differentiation. J. Comp. Neurol. 155: 469-482.
29. 29. LAUDER, J. M., J. A. WALLACE, H. KREBS, P. PETRUSZ, AND K. MCCARTHY. 1982. In vivo and in vitro development of serotonergic neurons. Brain Res. Bull. 9: 605-625.
30. 30. LEVITT, P., AND P. RAKIC. 1982. The time of genesis, embryonic origin and differentiation of the brain stem monoamine neurons in the rhesus monkey. Dev. Brain Res. 4: 35-57.
31. 31. MANIATIS, T., E. F. FRITSCH, AND J. SAMBROCK. 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
32. 32. MARCHAND, R., AND L. LAJOIE. 1986. Histogenesis of the striato-pallidal system in the rat. Neuroscience 17: 573-590.
33. 32a. MARKWELL, M. A., S. U. HAAS, L. L. BIEBER, AND M. E. TOLBERT. 1978. A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal. Biochem. 87: 206-210.
34. 33. NAGATSU, T. 1991. Genes for human catecholamine-synthesizing enzymes. Neurosci. Res. 12: 315-345.
35. 34. NAGATSU, T., M. LEVITT, AND S. UDENFRIEND. 1964. Tyrosine hydroxylase: The initial step in the norepinephrine biosynthesis. J. Biol. Chem. 239: 2910-2917.
36. 35. NOBIN, A., AND A. BJÖRKLUND. 1973. Topography of the monoamine neuron systems in the human brain as revealed in fetuses. Acta Physiol. Scand. (Suppl.) 388: 1-40.
37. 36. OLSON, L., AND Å. SEIGER 1972. Early prenatal ontogeny of central monoamine neurons in the rat: Fluorescence histochemical observations. Z. Anat. Entwicklungsgesch. 137: 301-316.
38. 37. OLSON, L., L. O. BORE'US, AND Å. SEIGER. 1973. Histochemical demonstration and mapping of 5-hydroxytryptamine- and catecholamine-containing neuron system in the human fetal brain. Z. Anat. Entwicklungsgesch. 139: 259-282.
39. 38. OLSON, L., I. STRÖMBERG, M. BYGDEMAN, A.-CH. GRANHOLM, B. HOFFER, R. FREEDMAN, AND Å. SEIGER. 1987. Human fetal tissues grafted to rodent hosts: Structural and functional observations of brain, adrenal and heart tissues in oculo. Exp. Brain Res. 67: 163-178.
40. 39. O'RAHILLY, R., AND F. MÜLLER. 1992. Human Embryology & Teratology. Wiley-Liss, New York.
41. 40. O'RAHILLY, R., AND F. MÜLLER. 1994. The Embryonic Human Brain. Wiley-Liss, New York.
42. 41. PARÉS-HERBUTÉ, N., L. TAPIA-ARANCIBA, AND H. ASTIER. 1989. Ontogeny of the metencephalic, mesencephalic and diencephalic content of catecholamines as measured by high performance liquid chromatography with electrochemical detection. Int. J. Dev. Neurosci. 7: 73-79.
43. 42. PEARSON, J., L. BRANDEIS, AND M. GOLDSTEIN. 1980. Appearance of tyrosine hydroxylase immunoreactivity in the human embryo. Dev. Neurosci. 3: 140-150.
44. 43. PICKEL, V. M., L. A. SPECHT, K. K. SUMAL, T. H. JOH, D. J. REIS, AND A. HERVONEN. 1980. Immunocytochemical localization of tyrosine hydroxylase in the human fetal nervous system. J. Comp. Neurol. 194: 465-474.
45. 44. PRINCE, D. A. 1978. Neurophysiology of epilepsy. Annu. Rev. Neurosci. 1: 395-415.
46. 45. REISERT, I., R. SCHUSTER, R. ZIENECKER, AND C. PILGRIM. 1990. Prenatal development of mesencephalic and diencephalic dopaminergic systems in the male and female rat. Dev. Brain Res. 53: 222-229.
47. 46. REYNOLDS, B. A., AND S. WEISS. 1992. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 27: 1707-1710.
48. 47. REYNOLDS, B. A., A. TETZLAFF, AND S. WEISS. 1992. A multipotent EGF-responsive striatal embryonic progenitor cell produces neurons and astrocytes. J. Neurosci. 12: 4565-4574.
49. 48. SEIGER, Å., AND L. OLSON. 1973. Late prenatal ontogeny of central monoamine neurons in the rat: Fluorescence histochemical observations. Z. Anat. Entwicklungsgesch. 140: 281-318.
50. 49. SILANI, V., D. MARIANI, F. M. DONATO, C. GHEZZI, F. MAZZUCCHELLI, M. BUSCAGLIA, G. PARDI, AND G. SCARLATO. 1994. Development of dopaminergic neurons in the human mesencephalon and in vitro effects of basic fibroblast growth factor treatment. Exp. Neurol. 128: 59-76.
51. 50. SLADEK, J. R., JR, AND J. G. PARNAVELAS. 1975. Catecholamine-containing dendrites in the primate brain. Brain Res. 100: 657-662.
52. 51. SOLBERG, Y., W. F. SILVERMAN, AND Y. POLLACK. 1993. Prenatal ontogeny of tyrosine hydroxylase gene expression in the rat ventral mesencephalon. Dev. Brain Res. 73: 91-97.
53. 52. 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. 1. Early ontogeny. J. Comp. Neurol. 199: 233-253.
54. 53. SUNDSTRÖM, E., S. KÖLARE, F. SOUVERBIE, E.-B. SAMUELSSON, H. PSCHERA, N.-O. LUNELL, AND Å. SEIGER 1993. Neurochemical differentiation of human bulbospinal monoaminergic neurons during the first trimester. Dev. Brain Res. 175: 1-12.
55. 54. VANHALA, A., A. YAMATODANI, AND P. PANULA. 1994. Distribution of histamine-, 5-hydroxytryptamine-, and tyrosine hydroxylase-immunoreactive neurons and nerve fibers in developing rat brain. J. Comp. Neurol. 347: 101-114.
56. 55. VAN HORN, C. G., T. MAHALIK, B. HOFFER, M. BYGDEMAN, P. ALMQVIST, P. STIEG, Å. SEIGER, L. OLSON, AND I. STRÖMBERG. 1990. Behavioral and electrophysiological correlates of human mesencephalic dopaminergic xenograft function in the rat striatum. Brain Res. Bull. 25: 325-334.
57. 56. VERNEY, C., N. ZECEVIC, B. NICOLIC, C. ALVAREZ, AND B. BERGER 1991. Early evidence of catecholaminergic cell groups in 5- and 6-week-old human embryos using tyrosine hydroxylase and dopamine-β-hydroxylase immunocytochemistry. Neurosci. Lett. 131: 121-124.
58. 57. VOORN, P., A. KALSBEEK, B. JORRITSMA-BYHAM, AND H. J. GROENEWEGEN. 1988. The pre- and postnatal development of the dopaminergic cell groups in the ventral mesencephalon and the striatum of the rat. Neuroscience 25: 857-887.
59. 58. WIDNER, H., J. TETRUD, S. REHNCRONA, B. SNOW, P. BRUNDIN, B. GUSTAVII, A. BJÖRKLUND, O. LINDVALL, AND J. W. LANGSTON. 1992. Bilateral fetal mesencephalic grafting in two patients with parkinsonism induced by 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP). N. Engl. J. Med. 327: 1557-1563.