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CD15 immunoreactivity in the developing brain of a marsupial, the tammar wallaby (Macropus eugenii)

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Abstract

We have studied the distribution of the CD15 epitope in the developing brain of an Australian diprotodontid metatherian mammal, the tammar wallaby (Macropus eugenii), using immunohistochemistry in conjunction with hematoxylin and eosin staining. At the time of birth (28 days after conception), CD15 immunoreactivity labeled somata in the primordial plexiform layer of the parietal cortex in a similar position to that seen in the early fetal eutherian brain. CD15 immunoreactivity in the brain of the developing pouch-young wallaby was found to be localized on the surface of radial glia at boundaries between developmentally significant forebrain compartments in a similar distribution to that seen in developing eutherian brain. These were best seen in the developing diencephalon, delineating epithalamus, ventral and dorsal thalamus and hypothalamic anlage, and in the striatum. Immunoreactivity for CD15 identified radial glia marking the lateral migratory stream at the striatopallial boundary, peaking in intensity at P19 to P25. From P37 to P54, CD15 immunoreactivity also demarcated patch compartments in the developing striatum. In contrast, CD15 immunoreactivity in hindbrain structures showed some differences from the temporospatial pattern seen in eutherian brain. These may reflect the relatively early brainstem maturation required for the newborn wallaby to be able to traverse the distance from the maternal genital tract to the pouch. The wallaby provides a convenient model for testing hypotheses concerning the role of CD15 in forebrain development because all events in which CD15 may play a critical role in forebrain morphogenesis occur during pouch life, when the young wallaby is accessible to experimental manipulation.

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References

  • Ashwell KWS, Waite PME, Marotte L (1996) Ontogeny of the projection tracts and commissural fibres in the forebrain of the wallaby (Macropus eugenii): a comparison of timing with other mammals. Brain Behav Evol 47:8–22

    CAS  PubMed  Google Scholar 

  • Ashwell KWS, Mai JK (1997a) Developmental expression of the CD15-epitope in the brainstem and spinal cord of the mouse Anat Embryol 196:13–25

    Google Scholar 

  • Ashwell KWS, Mai JK (1997b) Transient developmental expression of CD15 in the motor and auditory cortex of the mouse. Dev Brain Res 100:143–148

    Article  CAS  Google Scholar 

  • Ashwell KWS, Mai JK (1997c) Developmental expression of the CD15 epitope in the hippocampus of the mouse. Cell Tissue Res 289:17–23

    Article  CAS  PubMed  Google Scholar 

  • Butcher LL, Hodge GK (1976) Postnatal development of acetylcholinesterase in the caudate-putamen nucleus and substantia nigra of rats. Brain Res 106:223–240

    Article  CAS  PubMed  Google Scholar 

  • Chapouton P, Gartner A, Gotz M (1999) The role of Pax6 in restricting cell migration between developing cortex and basal ganglia. Development 126:5569–5579

    CAS  PubMed  Google Scholar 

  • Clemens WA (1970) Mesozoic mammalian evolution. Ann Rev Ecol Systemat 1:357–390

    Article  Google Scholar 

  • Faull LM, Dragunow M, Villiger JW (1989) The distribution of neurotensin receptors and acetylcholinesterase in the human caudate nucleus: evidence for the existence of a third neurochemical compartment. Brain Res 488:381–386

    Article  CAS  PubMed  Google Scholar 

  • Fenderson BA, Holmes EH, Fukushi Y, Hakomori S (1986) Co-ordinate expression of X and Y haptens during murine embryogenesis. Dev Biol 114:12–21

    CAS  PubMed  Google Scholar 

  • Gleeson JG, Walsh CA (2000) Neuronal migration disorders: from genetic diseases to developmental mechanisms. Trends Neurosci 23:352–359

    Article  CAS  PubMed  Google Scholar 

  • Graybiel AM (1983) Compartmental organization of the mammalian striatum. Prog Brain Res 58:247–256

    CAS  PubMed  Google Scholar 

  • Graybiel AM (1984) Correspondence between the dopamine islands and striosomes of the mammalian striatum. Neurosci 13:1157–1187

    Article  CAS  Google Scholar 

  • Graybiel AM, Hickey TL (1982) Chemospecificity of ontogenetic units in the striatum: demonstration by combining [3H] thymidine autoradiography and histochemical staining. Proc Natl Acad Sci USA 79:198–202

    CAS  PubMed  Google Scholar 

  • Haber SN, Elde R (1982) The distribution of enkephalin immunoreactive fibres and terminals in the monkey central nervous system: an immunohistochemical study. Neurosci 7:1049–1095

    Article  CAS  Google Scholar 

  • Haber SN, Gdowski MJ (2004) The basal ganglia. In: Paxinos G, Mai JK (eds) The human nervous system, 2nd edn. Elsevier, San Diego, pp 676–738

  • Hakomori S-I (1992) Lex and related structures as adhesion molecules. Histochem J 24:771–776

    CAS  PubMed  Google Scholar 

  • Herkenham M, Pert CB (1981) Mosaic distribution of opiate receptors, parafascicular projections and acetylcholinesterase in the rat striatum. Nature 291:415–418

    CAS  PubMed  Google Scholar 

  • Mai JK (2002) CD15. In: Creighton TE (ed) Encyclopedia of molecular medicine. John Wiley Sons, New York, pp 555–558

  • Mai JK, Reifenberger G (1988) Distribution of the carbohydrate epitope 3-fucosyl-N-acetyl-lactosamine (FAL) in the adult human brain. J Chem Neuroanat 1:255–285

    CAS  PubMed  Google Scholar 

  • Mai JK, Schönlau CH (1992) Age-related expression patterns of the CD15-epitope in the human lateral geniculate nucleus (LGN). Histochem J 24:878–889

    CAS  PubMed  Google Scholar 

  • Mai JK, Andressen C, Ashwell KWS (1998) Demarcation of prosencephalic regions by CD15-positive radial glia. Eur J Neurosci 10:746–751

    Article  CAS  PubMed  Google Scholar 

  • Mai JK, Winking R, Ashwell KWS (1999a) Transient CD15 expression reflects stages of differentiation and maturation in the human subcortical central auditory pathway. J Comp Neurol 404:197–211

    Article  CAS  PubMed  Google Scholar 

  • Mai JK, Krajewski S, Reifenberger G, Genderski B, Lensing-Höhn S, Ashwell KWS (1999b) Spatiotemporal expression gradients of the carbohydrate antigen CD15 (Lewisx) during development of the human basal ganglia. Neuroscience 88:847–858

    Article  CAS  PubMed  Google Scholar 

  • Mai JK, Krajewski S, Ashwell KWS, Andressen C (2003) A CD15-immunoreactive subpopulation of radial glial cells in the developing human lateral ganglionic eminence Neuroembryology 2:64–71

    Google Scholar 

  • Mai JK, Ashwell KWS (2004) Fetal development of the human brain. In: Paxinos G, Mai JK (eds) The human nervous system, 2nd edn. Elsevier, San Diego, pp 49–94

  • Nastuk MA, Graybiel AM (1985) Patterns of muscarinic cholinergic binding in the striatum and their relation to dopamine islands and striosomes. J Comp Neurol 237:176–194

    CAS  PubMed  Google Scholar 

  • Puelles L, Rubenstein JLR (1993) Expression patterns of homeobox and other putative regulatory genes in the mouse embryonic forebrain suggest a neuromeric organization. Trends Neurosci 16:61–83

    Article  Google Scholar 

  • Rakic P (1972) Mode of cell migration to the superficial layers of fetal monkey cortex. J Comp Neurol 145:61–83

    CAS  PubMed  Google Scholar 

  • Rakic P (1988) Specification of cerebral cortical areas. Science 241:170–176

    CAS  PubMed  Google Scholar 

  • Renfree MB (1981) Marsupials: alternative mammals. Nature 293:100–101

    CAS  PubMed  Google Scholar 

  • Renfree MB, Holt AB, Green SW, Carr JP, Cheek DB (1982) Ontogeny of the brain in a marsupial (Macropus eugenii) throughout pouch life. I. Brain growth. Brain Behav Evol 20:57–71

    CAS  PubMed  Google Scholar 

  • Semba K, Fibiger HC (1988) Time of origin of cholinergic neurons in the rat basal forebrain. J Comp Neurol 269:87–95

    CAS  PubMed  Google Scholar 

  • Steindler DA, O’Brien TF, Cooper NG (1988) Glycoconjugate boundaries during early postnatal development of the neostriatal mosaic. J Comp Neurol 267:357–369

    CAS  PubMed  Google Scholar 

  • Tyndale-Biscoe CH (1973) Life of marsupials. Arnold, London.

  • Tyndale-Biscoe CH, Janssens PA (eds) (1988) The developing marsupial, models for biomedical research. Springer, Berlin Heidelberg New York

  • Zahm DS, Eggerman KV, Sprung RF, Wesche DE, Payne E (1990) Postnatal development of striatal neurotensin immunoreactivity in relation to clusters of substance P immunoreactive neurons and dopamine islands in the rat. J Comp Neurol 296:403–414

    CAS  PubMed  Google Scholar 

  • Zecevic N, Verney C (1995) Development of the catecholaminergic neurons in human embryos and fetuses, with special emphasis on the innervation of the cerebral cortex. J Comp Neurol 351:509–553

    CAS  PubMed  Google Scholar 

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Acknowledgements

We would like to thank Dr. Lauren Marotte for providing the wallaby material, and Sabine Lensing-Höhn and Marietta Kazimirek for performing the sectioning and immunohistochemistry. Dr. M Stark developed the hybridoma-derived antibody. This work was supported in part by a grant to KWSA from the Alexander von Humboldt Foundation.

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Correspondence to K. W. S. Ashwell.

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Ashwell, K.W.S., Mai, J.K. & Andressen, C. CD15 immunoreactivity in the developing brain of a marsupial, the tammar wallaby (Macropus eugenii). Anat Embryol 209, 157–168 (2004). https://doi.org/10.1007/s00429-004-0430-1

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