Examination of the relationship between astrocyte morphology and laminar boundaries in the molecular layer of adult dentate gyrus

Journal of Comparative Neurology

Volumn 462, Issue 2, 2003, Pages 241-251

  Bushong, Eric A ^a   Martone, Maryann E ^a,b   Ellisman, Mark H ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Compartments; Development; EphA; Glia; N CAM; Patterning

Indexed keywords

EPHRIN; NERVE CELL ADHESION MOLECULE;

ANIMAL CELL; ANTIBODY LABELING; ARTICLE; ASTROCYTE; CELL COMPARTMENTALIZATION; CELL FUNCTION; CELL POLARITY; CELL STRUCTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DENTATE GYRUS; GLIA CELL; MALE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RAT; SOMATIC CELL;

AGE FACTORS; ANIMALS; ASTROCYTES; BIOLOGICAL MARKERS; CELL SIZE; DENTATE GYRUS; MALE; NEURAL CELL ADHESION MOLECULES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, EPHA4;

EID: 0038340889     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.10728     Document Type: Article

References (78)

1. Angevine JB Jr. 1965. Time of neuron origin in the hippocampal region. An autoradiographic study in the mouse. Exp Neurol Suppl 2:1-70.
2. 2+ elevations in astrocytes in hippocampal slices. J Neurosci 22:2443-2450.
3. Bechmann I, Nitsch R. 1997. Astrocytes and microglial cells incorporate degenerating fibers following entorhinal lesion: a light, confocal, and electron microscopical study using a phagocytosis-dependent labeling technique. Glia 20:145-154.
4. Bechmann I, Nitsch R. 2000. Involvement of non-neuronal cells in entorhinal-hippocampal reorganization following lesions. Ann NY Acad Sci 911:192-206.
5. Beggs HE, Soriano P, Maness PF. 1994. NCAM-dependent neurite outgrowth is inhibited in neurons from Fyn-minus mice. J Cell Biol 127:825-833.
6. Benson DL, Colman DR, Huntley GW. 2001. Molecules, maps and synapse specificity. Nat Rev Neurosci 2:899-909.
7. Blumcke I, Eggli P, Celio MR. 1995. Relationship between astrocytic processes and "perineuronal nets" in rat neocortex. Glia 15:131-140.
8. Bolam JP, Izzo PN, Graybiel AM. 1988. Cellular substrate of the histochemically defined striosome/matrix system of the caudate nucleus: a combined Golgi and immunocytochemical study in cat and ferret. Neuroscience 24:853-875.
9. Bruses JL, Rutishauser U. 2001. Roles, regulation, and mechanism of polysialic acid function during neural development. Biochimie 83:635-643.
10. Buhl EH, Schwerdtfeger WK, Germroth P. 1990. Intracellular injection of neurons in fixed brain tissue combined with other neuroanatomical techniques at the light and electron microscopic level. In: Bjorklund A, Hokfelt T, Wouterlood FG, van den Pol AN, editors. Handbook of chemical nNeuroanatomy. Vol. 8: Analysis of neuronal microcircuits and synaptic interactions. Amsterdam: Elsevier Science Publishers. p 273-304.
11. Bushong EA, Martone ME, Ellisman MH. 2001. Protoplasmic astrocytes conform to 'hidden boundaries' in rat dentate gyrus. Soc Neurosci Abstr 27:1325.
12. Bushong EA, Martone ME, Jones YZ, Ellisman MH. 2002. Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains. J Neurosci 22:183-192.
13. Castellani V, Yue Y, Gao PP, Zhou R, Bolz J. 1998. Dual action of a ligand for Eph receptor tyrosine kinases on specific populations of axons during the development of cortical circuits. J Neurosci 18:4663-4672.
14. Crossin KL, Krushel LA. 2000. Cellular signaling by neural cell adhesion molecules of the immunoglobulin superfamily. Dev Dyn 218:260-279.
15. Dani JW, Chernjavsky A, Smith SJ. 1992. Neuronal activity triggers calcium waves in hippocampal astrocyte networks. Neuron 8:429-440.
16. Deller T, Haas CA, Naumann T, Joester A, Faissner A, Frotscher M. 1997. Up-regulation of astrocyte-derived tenascin-C correlates with neurite outgrowth in the rat dentate gyrus after unilateral entorhinal cortex lesion. Neuroscience 81:829-846.
17. Deller T, Haas CA, Frotscher M. 2000. Reorganization of the rat fascia dentata after a unilateral entorhinal cortex lesion. Role of the extracellular matrix. Ann NY Acad Sci 911:207-220.
18. Derouiche A. 2000. Topical correlation of increased hippocampal glutamine synthetase immunoreactivity and glutamatergic terminal fields after entorhinal cortex lesion. Glia 29:386-391.
19. Distler C, Dreher Z, Stone J. 1991. Contact spacing among astrocytes in the central nervous system: an hypothesis of their structural role. Glia 4:484-494.
20. Doherty P, Williams E, Walsh FS. 1995. A soluble chimeric form of the L1 glycoprotein stimulates neurite outgrowth. Neuron 14:57-66.
21. Faissner A, Steindler D. 1995. Boundaries and inhibitory molecules in developing neural tissues. Glia 13:233-254.
22. Flanagan JG, Vanderhaeghen P. 1998. The ephrins and Eph receptors in neural development. Annu Rev Neurosci 21:309-345.
23. Gao PP, Yue Y, Cerretti DP, Dreyfus C, Zhou R. 1999. Ephrin-dependent growth and pruning of hippocampal axons. Proc Natl Acad Sci USA 96:4073-4077.
24. Gardner-Medwin AR. 1983. A study of the mechanisms by which potassium moves through brain tissue in the rat. J Physiol 335:353-374.
25. Grosche J, Matyash V, Möller T, Verkhratsky A, Reichenbach A, Kettenmann H. 1999. Microdomains for neuron-glia interaction: parallel fiber signaling to Bergmann glial cells. Nat Neurosci 2:139-143.
26. Haas CA, Rauch U, Thon N, Merten T, Deller T. 1999. Entorhinal cortex lesion in adult rats induces the expression of the neuronal chondroitin sulfate proteoglycan neurocan in reactive astrocytes. J Neurosci 19:9953-9963.
27. Hailer NP, Grampp A, Nitsch R. 1999. Proliferation of microglia and astrocytes in the dentate gyrus following entorhinal cortex lesion: a quantitative bromodeoxyuridine-labelling study. Eur J Neurosci 11:3359-3364.
28. Harlow E, Lane D. 1988. Antibodies: a laboratory manual. Cold Spring Harbor: Cold Spring Harbor Laboratory.
29. Irvine KD, Rauskolb C. 2001. Boundaries in development: formation and function. Annu Rev Cell Dev Biol 17:189-214.
30. Isaacs KR, Sirevaag AM, Marks AE, Chang FL, Greenough WT. 1993. A method for quantification of astrocytic processes reveals laminar differences in the dentate gyrus but not in CA1 of the hippocampal formation. J Neurosci Methods 48:141-148.
31. Jensen MB, Gonzalez B, Castellano B, Zimmer J. 1994. Microglial and astroglial reactions to anterograde axonal degeneration: a histochemical and immunocytochemical study of the adult rat fascia dentata after entorhinal perforant path lesions. Exp Brain Res 98:245-260.
32. Katz LC, Gilbert CD, Wiesel TN. 1989. Local circuits and ocular dominance columns in monkey striate cortex. J Neurosci 9:1389-1399.
33. Kelley MS, Steward O. 1993. The role of neuronal activity in upregulating GFAP mRNA levels after electrolytic lesions of the entorhinal cortex. Int J Dev Neurosci 11:105-115.
34. Kishi K, Stanfield BB, Cowan WM. 1979. A note on the distribution of glial cells in the molecular layer of the dentate gyrus. Brain Res Bull 4:35-41.
35. Klein R. 2001. Excitatory Eph receptors and adhesive ephrin ligands. Curr Opin Cell Biol 13:196-203.
36. Kosaka T, Hama K. 1986. Three-dimensional structure of astrocytes in the rat dentate gyrus. J Comp Neurol 249:242-260.
37. Kuffler SW, Nicholls JG. 1966. The physiology of neuroglial cells. Ergeb Physiol 57:1-90.
38. Kuhn HG, Dickinson-Anson H, Gage FH. 1996. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 16:2027-2033.
39. Laywell ED, Steindler DA. 1991. Boundaries and wounds, glia and glycoconjugates. Cellular and molecular analyses of developmental partitions and adult brain lesions. Ann NY Acad Sci 633:122-141.
40. Lubke J, Egger V, Sakmann B, Feldmeyer D. 2000. Columnar organization of dendrites and axons of single and synaptically coupled excitatory spiny neurons in layer 4 of the rat barrel cortex. J Neurosci 20:5300-5311.
41. Lynch G, Matthews DA, Mosko S, Parks T, Cotman C. 1972. Induced acetylcholinesterase-rich layer in rat dentate gyrus following entorhinal lesions. Brain Res 42:311-318.
42. Martone ME, Holash JA, Bayardo A, Pasquale EB, Ellisman MH. 1997. Immunolocalization of the receptor tyrosine kinase EphA4 in the adult rat central nervous system. Brain Res 771:238-250.
43. Mellitzer G, Xu Q, Wilkinson DG, 1999. Eph receptors and ephrins restrict cell intermingling and communication. Nature 400:77-81.
44. Miller PD, Chung WW, Lagenaur CF, DeKosky ST. 1993. Regional distribution of neural cell adhesion molecule (N-CAM) and L1 in human and rodent hippocampus. J Comp Neurol 327:341-349.
45. Miller PD, Styren SD, Lagenaur CF, DeKosky ST. 1994. Embryonic neural cell adhesion molecule (N-CAM) is elevated in the denervated rat dentate gyrus. J Neurosci 14:4217-4225.
46. Moreno-Flores MT, Wandosell F. 1999. Up-regulation of Eph tyrosine kinase receptors after excitotoxic injury in adult hippocampus. Neuroscience 91:193-201.
47. Mugnaini E. 1986. Cell juctions of astrocytes, ependyma, and related cells in the mammalian central nervous system, wtih emphasis on the hypothesis of a generalized functional syncytium of supporting cells. In: Fedoroff S, Vernadakis A, Editors. Astrocytes. New York: Academic Press. p 329-371.
48. Nett WJ, Oloff SH, McCarthy KD. 2002. Hippocampal astrocytes in situ exhibit calcium oscillations that occur independent of neuronal activity. J Neurophysiol 87:528-537.
49. Neugebauer KM, Tomaselli KJ, Lilien J, Reichardt LF. 1988. N-cadherin, NCAM, and integrins promote retinal neurite outgrowth on astrocytes in vitro. J Cell Biol 107:1177-1187.
50. Nixdorf-Bergweiler BE, Albrecht D, Heinemann U. 1994. Developmental changes in the number, size, and orientation of GFAP-positive cells in the CA1 region of rat hippocampus. Glia 12:180-195.
51. Patrylo PR, Nowakowski RS. 1994. Morphology and distribution of astrocytes in the molecular layer of the dentate gyrus in NZB/BlNJ, Dreher, and C57BL/6J mice. Glia 10:1-9.
52. Powell EM, Meiners S, DiProspero NA, Geller HM. 1997. Mechanisms of astrocyte-directed neurite guidance. Cell Tissue Res 290:385-393.
53. Redies C. 2000. Cadherins in the central nervous system. Prog Neurobiol 61:611-648.
54. Romano JP. 1989. Bootstrap and randomization tests of some nonparametric hypothesis. Ann Stat 17:141-159.
55. Rose G, Lynch G, Cotman CW. 1976. Hypertrophy and redistribution of astrocytes in the deafferented dentate gyrus. Brain Res Bull 1:87-92.
56. Ruiz i Altaba A, Gitton Y, Dahmane N. 2001. Embryonic regionalization of the neocortex. Mech Dev 107:3-11.
57. Sajin B, Steindler DA. 1994. Cells on the edge: boundary astrocytes and neurons. Persp Dev Neurobiol 2:275-289.
58. Sanes JR, Yamagata M. 1999. Formation of lamina-specific synaptic connections. Curr Opin Neurobiol 9:79-87.
59. Savaskan NE, Nitsch R. 2001. Molecules involved in reactive sprouting in the hippocampus. Rev Neurosci 12:195-215.
60. Schlessinger AR, Cowan WM, Gottlieb DI. 1975. An autoradiographic study of the time of origin and the pattern of granule cell migration in the dentate gyrus of the rat. J Comp Neurol 159:149-175.
61. Snow DM, Lemmon V, Carrino DA, Caplan AI, Silver J. 1990. Sulfated proteoglycans in astroglial barriers inhibit neurite outgrowth in vitro. Exp Neurol 109:111-130.
62. Soans C, Holash JA, Pasquale EB. 1994. Characterization of the expression of the Cek8 receptor-type tyrosine kinase during development and in tumor cell lines. Oncogene 9:3353-3361.
63. Steindler DA. 1993. Glial boundaries in the developing nervous system. Annu Rev Neurosci 16:445-470.
64. Steindler DA, Cooper NG. 1987. Glial and glycoconjugate boundaries during postnatal development of the central nervous system. Brain Res 433:27-38.
65. Steindler DA, Faissner A, Schachner M. 1989. Brain "cordones": transient boundaries of glia and adhesion molecules that define developing functional units. Comm Dev Neurobiol 1:29-60.
66. Steindler DA, O'Brien TF, Laywell E, Harrington K, Faissner A, Schachner M. 1990. Boundaries during normal and abnormal brain development: in vivo and in vitro studies of glia and glycoconjugates. Exp Neurol 109:35-56.
67. Steward O, Cotman CW, Lynch GS. 1974. Growth of a new fiber projection in the brain of adult rats: re-innervation of the dentate gyrus by the contralateral entorhinal cortex following ipsilateral entorhinal lesions. Exp Brain Res 20:45-66.
68. Steward O, Kelley MS, Torre ER. 1993. The process of reinnervation in the dentate gyrus of adult rats: temporal relationship between changes in the levels of glial fibrillary acidic protein (GFAP) and GFAP mRNA in reactive astrocytes. Exp Neurol 124:167-183.
69. Tarone G, Hirsch E, Brancaccio M, De Acetis M, Barberis L, Balzac F, Retta SF, Botta C, Altruda F, Silengo L, Retta F. 2000. Integrin function and regulation in development. Int J Dev Biol 44:725-731.
70. Thon N, Haas CA, Rauch U, Merten T, Fassler R, Frotscher M, Deller T. 2000. The chondroitin sulphate proteoglycan brevican is upregulated by astrocytes after entorhinal cortex lesions in adult rats. Eur J Neurosci 12:2547-2558.
71. Tomaselli KJ, Neugebauer KM, Bixby JL, Lilien J, Reichardt LF. 1988. N-cadherin and integrins: two receptor systems that mediate neuronal process outgrowth on astrocyte surfaces. Neuron 1:33-43.
72. Wilkinson DG. 2000. Eph receptors and ephrins: regulators of guidance and assembly. Int Rev Cytol 196:177-244.
73. Wilkinson DG. 2001. Multiple roles of EPH receptors and ephrins in neural development. Nat Rev Neurosci 2:155-164.
74. Wintergerst ES, Faissner A, Celio MR. 1996. The proteoglycan DSD-1-PG occurs in perineuronal nets around parvalbumin-immunoreactive interneurons of the rat cerebral cortex. Int J Dev Neurosci 14:249-255.
75. Woodhams PL. 1993. Laminar and region-specific cell surface markers in the entorhinal cortex and hippocampus. Hippocampus 3:183-189.
76. Wolff JR. 1976. The morphological organization of cortical neuroglia. In: Creutzfeldt O, editor. Handbook of electroencephalography and clinical neurophysiology. Amsterdam: Elsevier Scientific Publishing Company. p 26-43.
77. Yamamoto T, Ochalski A, Hertzberg EL, Nagy JI. 1990. On the organization of astrocytic gap junctions in rat brain as suggested by LM and EM immunohistochemistry of connexin43 expression. J Comp Neurol 302:853-883.
78. Zhou X, Suh J, Cerretti DP, Zhou R, DiCicco-Bloom E. 2001. Ephrins stimulate neurite outgrowth during early cortical neurogenesis. J Neurosci Res 66:1054-1063.