NCAM and polysialyltransferase profiles match dopaminergic marker gene expression but polysialic acid is dispensable for development of the midbrain dopamine system

Journal of Neurochemistry

Volumn 110, Issue 5, 2009, Pages 1661-1673

  Schiff, Miriam ^a,b   Weinhold, Birgit ^a   Grothe, Claudia ^a,b   Hildebrandt, Herbert ^a,b  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b CENTER FOR SYSTEMS NEUROSCIENCE   (Germany)

Author keywords

Dopaminergic differentiation; Marker gene analysis; Neural cell adhesion molecule; Neurogenesis; Polysialic acid; Ventral midbrain development

Indexed keywords

DOPAMINE; DOPAMINE TRANSPORTER; MESSENGER RNA; NERVE CELL ADHESION MOLECULE; NESTIN; POLYSIALIC ACID; POLYSIALYLTRANSFERASE; SIALYLTRANSFERASE; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL COUNT; CONTROLLED STUDY; DOPAMINERGIC SYSTEM; EMBRYO; FEMALE; GENE EXPRESSION; GLIA; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; MARKER GENE; MESENCEPHALON; MICROSCOPY; MOUSE; NERVE CELL CULTURE; NONHUMAN; PIA MATER; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; RNA EXTRACTION;

ANIMALS; CELLS, CULTURED; DOPAMINE; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENETIC MARKERS; MESENCEPHALON; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; NEURAL CELL ADHESION MOLECULES; PREGNANCY; RNA, MESSENGER; SIALIC ACIDS; SIALYLTRANSFERASES;

MUS;

EID: 68949205194     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2009.06267.x     Document Type: Article

References (47)

1. Angata K., Huckaby V., Ranscht B., Terskikh A., Marth J. D. Fukuda M. (2007) Polysialic acid-directed migration and differentiation of neural precursors is essential for mouse brain development. Mol. Cell. Biol. 27, 6659 6668.
2. Bartsch U., Kirchhoff F. Schachner M. (1990) Highly sialylated N-CAM is expressed in adult mouse optic nerve and retina. J. Neurocytol. 19, 550 565.
3. Bringmann A., Pannicke T., Grosche J., Francke M., Wiedemann P., Skatchkov S. N., Osborne N. N. Reichenbach A. (2006) Muller cells in the healthy and diseased retina. Prog. Retin. Eye Res. 25, 397 424.
4. Burgess A., Wainwright S. R., Shihabuddin L. S., Rutishauser U., Seki T. Aubert I. (2008) Polysialic acid regulates the clustering, migration, and neuronal differentiation of progenitor cells in the adult hippocampus. Dev. Neurobiol. 68, 1580 1590.
5. Decker L., Avellana-Adalid V., Nait-Oumesmar B., Durbec P. Baron-van Evercooren A. (2000) Oligodendrocyte precursor migration and differentiation: combined effects of PSA residues, growth factors, and substrates. Mol. Cell. Neurosci. 16, 422 439.
6. Doherty P. Walsh F. S. (1996) CAM-FGF receptor interactions: a model for axonal growth. Mol. Cell. Neurosci. 8, 99 111.
7. Frosch M., Gorgen I., Boulnois G. J., Timmis K. N. Bitter-Suermann D. (1985) NZB mouse system for production of monoclonal antibodies to weak bacterial antigens: isolation of an IgG antibody to the polysaccharide capsules of Escherichia coli K1 and group B meningococci. Proc. Natl Acad. Sci. USA 82, 1194 1198.
8. Galuska S. P., Oltmann-Norden I., Geyer H., Weinhold B., Kuchelmeister K., Hildebrandt H., Gerardy-Schahn R., Geyer R. Mühlenhoff M. (2006) Polysialic acid profiles of mice expressing variant allelic combinations of the polysialyltransferases ST8SiaII and ST8SiaIV. J. Biol. Chem. 281, 31605 31615.
9. Gascon E., Vutskits L. Kiss J. Z. (2007) Polysialic acid-neural cell adhesion molecule in brain plasticity: from synapses to integration of new neurons. Brain Res. Rev. 56, 101 118.
10. Grothe C. Timmer M. (2007) The physiological and pharmacological role of basic fibroblast growth factor in the dopaminergic nigrostriatal system. Brain Res. Rev. 54, 80 91.
11. Guillery R. W. (2002) On counting and counting errors. J. Comp. Neurol. 447, 1 7.
12. Hekmat A., Bitter-Suermann D. Schachner M. (1990) Immunocytological localization of the highly polysialylated form of the neural cell adhesion molecule during development of the murine cerebellar cortex. J. Comp. Neurol. 291, 457 467.
13. Herman J. P., Victor J. C. Sanes J. R. (1993) Developmentally regulated and spatially restricted antigens of radial glial cells. Dev. Dyn. 197, 307 318.
14. Hildebrandt H., Mühlenhoff M., Weinhold B. Gerardy-Schahn R. (2007) Dissecting polysialic acid and NCAM functions in brain development. J. Neurochem. 1 103 Suppl) 56 64.
15. Hildebrandt H., Mühlenhoff M. Gerardy-Schahn R. (2008) Polysialylation of NCAM. Neurochem. Res. [e-pub ahead of print, DOI: 10.1007/s11064-008-9724-7].
16. Kawano H., Ohyama K., Kawamura K. and Nagatsu I. (1995) Migration of dopaminergic neurons in the embryonic mesencephalon of mice. Dev. Brain Res. 86, 101 113.
17. Kiselyov V. V. (2008) NCAM and the FGF-receptor. Neurochem. Res. [e-pub ahead of print, DOI: 10.1007/s11064-008-9666-0].
18. Lauder J. M. and Bloom F. E. (1974) Ontogeny of monoamine neurons in the locus coeruleus, Raphe nuclei and substantia nigra of the rat. I. Cell differentiation. J. Comp. Neurol. 155, 469 481.
19. Li H., Babiarz J., Woodbury J., Kane-Goldsmith N. Grumet M. (2004) Spatiotemporal heterogeneity of CNS radial glial cells and their transition to restricted precursors. Dev. Biol. 271, 225 238.
20. Liss B. Roeper J. (2008) Individual dopamine midbrain neurons: functional diversity and flexibility in health and disease. Brain Res. Rev. 58, 314 321.
21. Maness P. F. Schachner M. (2007) Neural recognition molecules of the immunoglobulin superfamily: signaling transducers of axon guidance and neuronal migration. Nat. Neurosci. 10, 19 26.
22. Nikkhah G., Olsson M., Eberhard J., Bentlage C., Cunningham M. G. Björklund A. (1994) A microtransplantation approach for cell suspension grafting in the rat Parkinson model: a detailed account of the methodology. Neuroscience 63, 57 72.
23. Oltmann-Norden I., Galuska S. P., Hildebrandt H., Geyer R., Gerardy-Schahn R., Geyer H. Mühlenhoff M. (2008) Impact of the polysialyltransferases ST8SiaII and ST8SiaIV on polysialic acid synthesis during postnatal mouse brain development. J. Biol. Chem. 283, 1463 1471.
24. Parish C. L., Castelo-Branco G., Rawal N., Tonnesen J., Sorensen A. T., Salto C., Kokaia M., Lindvall O. Arenas E. (2008) Wnt5a-treated midbrain neural stem cells improve dopamine cell replacement therapy in parkinsonian mice. J. Clin. Invest. 118, 149 160.
25. Paxinos G. Franklin K. B. J. (2001) The Mouse Brain in Stereotaxic Coordinates. Academic Press, Sydney.
26. Perlmann T. Wallén-Mackenzie A. (2004) Nurr1, an orphan nuclear receptor with essential functions in developing dopamine cells. Cell Tissue Res. 318, 45 52.
27. Perrone-Capano C. Di Porzio U. (2000) Genetic and epigenetic control of midbrain dopaminergic neuron development. Int. J. Dev. Biol. 44, 679 687.
28. Pinto L. Götz M. (2007) Radial glial cell heterogeneity: the source of diverse progeny in the CNS. Prog. Neurobiol. 83, 2 23.
29. Probstmeier R., Bilz A. Schneider-Schaulies J. (1994) Expression of the neural cell adhesion molecule and polysialic acid during early mouse embryogenesis. J. Neurosci. Res. 37, 324 335.
30. Röckle I., Seidenfaden R., Weinhold B., Mühlenhoff M., Gerardy-Schahn R. Hildebrandt H. (2008) Polysialic acid controls NCAM-induced differentiation of neuronal precursors into calretinin-positive olfactory bulb interneurons. Dev. Neurobiol. 68, 1170 1184.
31. Rutishauser U. (2008) Polysialic acid in the plasticity of the developing and adult vertebrate nervous system. Nat. Rev. Neurosci. 9, 26 35.
32. Saucedo-Cardenas O., Quintana-Hau J. D., Le W. D., Smidt M. P., Cox J. J., De Mayo F., Burbach J. P. Conneely O. M. (1998) Nurr1 is essential for the induction of the dopaminergic phenotype and the survival of ventral mesencephalic late dopaminergic precursor neurons. Proc. Natl Acad. Sci. USA 95, 4013 4018.
33. Seidenfaden R., Krauter A., Schertzinger F., Gerardy-Schahn R. Hildebrandt H. (2003) Polysialic acid directs tumor cell growth by controlling heterophilic neural cell adhesion molecule interactions. Mol. Cell. Biol. 23, 5908 5918.
34. Seidenfaden R., Krauter A. Hildebrandt H. (2006) The neural cell adhesion molecule NCAM regulates neuritogenesis by multiple mechanisms of interaction. Neurochem. Int. 49, 1 11.
35. Seki T. Arai Y. (1993) Distribution and possible roles of the highly polysialylated neural cell adhesion molecule (NCAM-H) in the developing and adult central nervous system. Neurosci. Res. 17, 265 290.
36. Shults C. W. Kimber T. A. (1992) Mesencephalic dopaminergic cells exhibit increased density of neural cell adhesion molecule and polysialic acid during development. Dev. Brain Res. 65, 161 172.
37. Shults C. W., Hashimoto R., Brady R. M. Gage F. H. (1990) Dopaminergic cells align along radial glia in the developing mesencephalon of the rat. Neuroscience 38, 427 436.
38. Smidt M. P. Burbach J. P. (2007) How to make a mesodiencephalic dopaminergic neuron. Nat. Rev. Neurosci. 8, 21 32.
39. Smidt M. P., van Schaick H. S., Lanctot C., Tremblay J. J., Cox J. J., van der Kleij A. A., Wolterink G., Drouin J. Burbach J. P. (1997) A homeodomain gene Ptx3 has highly restricted brain expression in mesencephalic dopaminergic neurons. Proc. Natl Acad. Sci. USA 94, 13305 13310.
40. Smidt M. P., Smits S. M. Burbach J. P. (2004) Homeobox gene Pitx3 and its role in the development of dopamine neurons of the substantia nigra. Cell Tissue Res. 318, 35 43.
41. Storch A., Ludolph A. C. Schwarz J. (2004) Dopamine transporter: involvement in selective dopaminergic neurotoxicity and degeneration. J. Neural Transm. 111, 1267 1286.
42. Stummeyer K., Dickmanns A., Mühlenhoff M., Gerardy-Schahn R. Ficner R. (2005) Crystal structure of the polysialic acid-degrading endosialidase of bacteriophage K1F. Nat. Struct. Mol. Biol. 12, 90 96.
43. Timmer M., Grosskreutz J., Schlesinger F., Krampfl K., Wesemann M., Just L., Bufler J. Grothe C. (2006) Dopaminergic properties and function after grafting of attached neural precursor cultures. Neurobiol. Dis. 21, 587 606.
44. Vitalis T., Cases O. Parnavelas J. G. (2005) Development of the dopaminergic neurons in the rodent brainstem. Exp. Neurol. 1 191 Suppl) S104 S112.
45. Volpicelli F., Perrone-Capano C., Da Pozzo P., Colucci-D'Amato L. Di Porzio U. (2004) Modulation of nurr1 gene expression in mesencephalic dopaminergic neurones. J. Neurochem. 88, 1283 1294.
46. Wallén A., Zetterstrom R. H., Solomin L., Arvidsson M., Olson L. Perlmann T. (1999) Fate of mesencephalic AHD2-expressing dopamine progenitor cells in NURR1 mutant mice. Exp. Cell Res. 253, 737 746.
47. Weinhold B., Seidenfaden R., Röckle I., Mühlenhoff M., Schertzinger F., Conzelmann S., Marth J. D., Gerardy-Schahn R. Hildebrandt H. (2005) Genetic ablation of polysialic acid causes severe neurodevelopmental defects rescued by deletion of the neural cell adhesion molecule. J. Biol. Chem. 280, 42971 42977.