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Neurogenesis and neuronal migration of dopaminergic neurons during mesencephalon development in mice

  • Kim, Mun-ki (Research Institute of Life Science & Department of Veterinary Medicine, Gyeongsang National University) ;
  • Lee, Si-Joon (Research Institute of Life Science & Department of Veterinary Medicine, Gyeongsang National University) ;
  • Vasudevan, Anju (Angiogenesis and Brain Development Laboratory, McLean Hospital/Harvard Medical School) ;
  • Won, Chungkil (Research Institute of Life Science & Department of Veterinary Medicine, Gyeongsang National University)
  • Received : 2018.11.18
  • Accepted : 2018.12.21
  • Published : 2018.12.31

Abstract

Dopaminergic neurons are one of the major neuronal components in the brain. Mesencephalon dopamine (DA) neurogenesis takes place in the ventricular zone of the floor plate, when DA progenitors divide to generate postmitotic cells. These cells migrate through the intermediate zone while they differentiate and become DA neurons on reaching the mantle zone. However, neurogenesis and neuronal migration on dopaminergic neurons remain largely unexplored in the mesencephalon development. This study presents neurogenesis and neuronal migration patterns of dopaminergic neurons during mesencephalic development of the mouse. Neurons from embryonic day (E) 10-14 were labelled by a single injection of 5-bromodeoxyuridine and immunohistochemistry was performed. The neurogenesis occurred mainly at the E10 and E11, which was uniformly distributed in the mesencephalic region, but neurons after E13 were observed only in the dorsal mesencephalon. At the postnatal day 0 (P0), E10 generated neurons were spread out uniformly in the whole mesencephalon whereas E11-originated neurons were clearly depleted in the red nucleus region. DA neurons mainly originated in the ventromedial mesencephalon at the early embryonic stage especially E10 to E11. DA neurons after E12 were only observed in the ventral mesencephalon. At E17, E10 labelled neurons were only observed in the substantia nigra (SN) region. Our study demonstrated that major neurogenesis occurred at E10 and E11. However, neuronal migration continued until neonatal period during mesencephalic development.

Keywords

Acknowledgement

Supported by : National Research Foundation of Korea (NRF)

References

  1. Altman J, Bayer SA. 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 1981;198:677-716. https://doi.org/10.1002/cne.901980409
  2. Arenas E, Denham M, Villaescusa JC. How to make a midbrain dopaminergic neuron. Development 2015; 142:1918-1936. https://doi.org/10.1242/dev.097394
  3. Corbin JG, Nery S, Fishell G. Telencephalic cells take a tangent: non-radial migration in the mammalian forebrain. Nat Neurosci 2001;4:1177-1182. https://doi.org/10.1038/nn749
  4. Hatten ME. New directions in neuronal migration. Science 2002;297:1660-1663. https://doi.org/10.1126/science.1074572
  5. Marin O, Rubenstein JLR. A long, remarkable journey: tangential migration in the telencephalon. Nat Rev Neurosci 2001;2:780-790.
  6. Nadarajah B, Parnavelas JG. Modes of neuronal migration in the developing cerebral cortex. Nat Rev Neurosci 2002;3:423-432. https://doi.org/10.1038/nrn845
  7. Parnavelas JG. The origin and migration of cortical neurons: new vistas. Trends Neurosci 2000;23:126-131. https://doi.org/10.1016/S0166-2236(00)01553-8
  8. Korotkova TM, Ponomarenko AA, Brown RE, Haas HL. Functional diversity of ventral midbrain dopamine and GABAergic neurons. Mol Neurobiol 2004;29:243-259. https://doi.org/10.1385/MN:29:3:243
  9. Vasudevan A, Won C, Li S, Erdelyi F, Szabo G, Kim KS. Dopaminergic neurons modulate GABA neuron migration in the embryonic midbrain. Development 2012;139:3136-3141. https://doi.org/10.1242/dev.078394
  10. Bjorklund A, Dunnett SB. Dopamine neuron systems in the brain: an update. Trends Neurosci 2007;30:194-202. https://doi.org/10.1016/j.tins.2007.03.006
  11. Schultz W. Reward signaling by dopamine neurons. Neuroscientist 2001;7:293-302. https://doi.org/10.1177/107385840100700406
  12. Nair-Roberts RG, Chatelain-Badie SD, Benson E, White-Cooper H, Bolam JP, Ungless MA. Stereological estimates of dopaminergic, GABAergic and glutamatergic neurons in the ventral tegmental area, substantia nigra and retrorubral field in the rat. Neuroscience 2008;152:1024-1031. https://doi.org/10.1016/j.neuroscience.2008.01.046
  13. Ori-McKenney KM, Vallee RB. Neuronal migration defects in the Loa dynein mutant mouse. Neural Dev 2000;6.
  14. Lewandowski TA, Ponce RA, Charleston JS, Hong S, Faustman EM. Changes in cell cycle parameters and cell number in the rat midbrain during organogenesis. Dev Brain Res 2003;141:117-128. https://doi.org/10.1016/S0165-3806(03)00004-X
  15. Smidt MP, Burbach JPH. How to make a mesodiencephalic dopaminergic neuron. Nat Rev Neurosci 2007;8:21-32. https://doi.org/10.1038/nrn2039
  16. Bayer SA, Wills KV, Triarhou LC, Ghetti B. Time of neuron origin and gradients of neurogenesis in midbrain dopaminergic neurons in the mouse. Exp Brain Res 1995;105:191-199.
  17. Castelo-Branco G, Wagner J, Rodriguez FJ, Kele J, Sousa K, Rawal N, Pasolli HA, Fuchs E, Kitajewski J, Arenas E. Differential regulation of midbrain dopaminergic neuron development by Wnt-1, Wnt-3a, and Wnt-5a. Proc Natl Acad Sci USA. 2003;100:12747-12752. https://doi.org/10.1073/pnas.1534900100
  18. Foster GA, Schultzberg M, Kokfelt T, Goldstein M, Hemmings HC Jr, Ouimet CC, Walaas SI, Greengard P. Ontogeny of the dopamine and cyclic adenosine-3':5'-monophosphate-regulated phosphoprotein (DARPP-32) in the pre- and postnatal mouse central nervous system. Int J Dev Neurosci 1988;6:367-386. https://doi.org/10.1016/0736-5748(88)90020-2
  19. Kawano H, Ohyama K, Kawamura K, Nagatsu I. Migration of dopaminergic neurons in the embryonic mesencephalon of mice. Brain Res Dev Brain Res 1995;86:101-113. https://doi.org/10.1016/0165-3806(95)00018-9
  20. Bayer SA, Wills KV, Triarhou LC, Thomas JD, Ghetti B. Systematic differences in time of dopaminergic neuron origin between normal mice and homozygous weaver mutants. Exp Brain Res 1995;105:200-208.

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