Expression of purine metabolism-related enzymes by microglial cells in the developing rat brain

Journal of Comparative Neurology

Volumn 398, Issue 3, 1998, Pages 333-346

  Dalmau, Ishar ^a   Vela, José Miguel ^a   González, Berta ^a   Castellano, Bernardo ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

Author keywords

5' nucleotidase; Neuroglia; Nucleoside diphosphatase; Nucleoside triphosphatase; Purine nucleoside phosphorylase

Indexed keywords

5' NUCLEOTIDASE; NUCLEOSIDE DIPHOSPHATASE; NUCLEOSIDE TRIPHOSPHATASE; PURINE; PURINE NUCLEOSIDE PHOSPHORYLASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; CELL DIFFERENTIATION; CELL STRUCTURE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; FEMALE; HIPPOCAMPUS; MALE; MICROGLIA; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PURINE METABOLISM; RAT; WHITE MATTER;

ANIMALS; BIOLOGICAL MARKERS; BRAIN; BRAIN CHEMISTRY; CELL DIFFERENTIATION; FEMALE; IMMUNOHISTOCHEMISTRY; MICROGLIA; PREGNANCY; PURINES; RATS; RATS, WISTAR;

EID: 0032585044     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19980831)398:3<333::AID-CNE3>3.0.CO;2-0     Document Type: Article

References (103)

1. Abbracchio, M.P., F. Cattabeni, F. Clementi, and E. Sher (1989) Adenosine receptors linked to adenylate cyclase activity in human neuroblastoma cells: Modulation during cell differentiation. Neuroscience 30:819-825.
2. Abbracchio, M.P., M.J. Saffrey, V. Hopker, and G. Burnstock (1994) Modulation of astroglial cell proliferation by analogues of adenosine and ATP in primary cultures of rat striatum. Neuroscience 59:67-76.
3. Abbracchio, M.P., S. Ceruti, D. Barbieri, C. Franceschi, W. Malorni, L. Biondo, G. Burnstock, and F. Cattabeni (1995a) A novel action for adenosine: Apoptosis of astroglial cells in rat brain primary cultures. Biochem. Biophys. Res. Commun. 213:908-915.
4. Abbracchio, M.P., S. Ceruti, R. Langfelder, F. Cattabeni, M.J. Saffrey, and G. Burnstock (1995b) Effects of ATP analogues and basic fibroblast growth factor on astroglial cell differentiation in primary cultures of rat striatum. Int. J. Dev. Neurosci. 13:685-693.
5. Acanín, L., J.M. Vela, B. González, and B. Castellano (1994) Demonstration of poly-N-acetyl lactosamine residues in ameboid and ramified microglial cells in rat brain by tomato lectin binding. J. Histochem, Cytochem. 42:1033-1041.
6. Auger, M.J. and J.A. Ross (1992) The biology of the macrophage. In C.E. Lewis and J.O.D. McGee (eds): The Natural Immune System. The Macrophage. New York: Oxford University Press, pp. 1-74.
7. Ashwell, K. (1991) The distribution of microglial and cell death in the fetal rat forebrain. Dev. Brain Res. 58:1-12.
8. Bignami, A., L.F. Eng, D. Dahl, and T. Uyeda (1972) Localization of the glial fibrillary acidic protein in astrocytes by immunofluorescence. Brain Res. 43:429-435.
9. Boya, J., J.L. Calvo, A.L. Carbonell, and A. Borregon (1991) A lectin histochemistry study on the development of rat microglial cells. J. Anat. 175:229-236.
10. Bronte, V., B. Macino, A. Zambon, A. Rosato, S. Mandruzzato, P. Zanovello, and D. Collavo (1996) Protein tyrosine kinases and phosphatases control apoptosis induced by extracellular adenosine 5′-triphosphate. Biochem. Biophys. Res. Commun. 218:344-351.
11. Burnstock, G. (1990) Overview. Purinergic mechanisms. Ann. NY Acad. Sci. 603:1-17.
12. Burnstock, G. (1993) Physiological and pathological roles of purines: An update. Drug Dev. Res. 28:195-206.
13. Castellano, B., B. González, B.R. Finsen, and J. Zimmer (1990) Histochemical demonstration of purine nucleoside phosphorylase (PNPase) in microglial and astroglial cells of adult rat brain. J. Histochem. Cytochem. 38:1535-1539.
14. Castellano, B., B. González, M.B. Jensen, E.B. Pedersen, B.R. Finsen, and J. Zimmer (1991a) A double staining technique for simultaneous demonstration of astrocytes and microglia in brain sections and astroglial cell cultures. J. Histochem. Cytochem. 35:561-568.
15. Castellano, B., B. González, I. Dalmau, and J.M. Vela (1991b) Identification and distribution of microglial cells in the cerebral cortex of the lizard: A histochemical technique. J. Comp. Neurol. 311:434-444.
16. Cline, M.J. and M.A.S. Moore (1972) Embryonic origin of the mouse macrophage. Blood 39:842-849.
17. Chugani, D.C., N.L. Kedersha, and L.H. Rome (1991) Vault immunofluorescence in the brain: New insights regarding the origin of microglia. J. Neurosci. 11:256-268.
18. Cossmann, P.H., P.S. Eggli, B. Christ, and H. Kurz (1997) Mesodermderived cells proliferate in the embryonic central nervous system: Confocal microscopy and three-dimensional visualization. Histochem. Cell Biol. 107:205-213.
19. Cuadros, M.A., C. Martin, P. Coltey, A. Almendros, and J. Navascués (1993) First appearance, distribution, and origin of macrophages in the early development of the avian central nervous system. J. Comp. Neurol. 330:113-129.
20. Dalmau, I., B. Castellano, E.B. Pedersen, B. Finsen, J. Zimmer, and B. Gonzalez (1996) Reduction of the microglial cell number in rat primary glial cell cultures by exogenous addition of dibutyryl cyclic adenosine monophosphate. J. Neuroimmunol. 70:123-129.
21. Dalmau, I., B. Finsen, N. Tønder, J. Zimmer, B. González, and B. Castellano (1997a) Development of microglia in the prenatal rat hippocampus. J. Comp. Neurol. 377:70-84.
22. Dalmau, I., J.M. Vela, B. González, and B. Castellano (1997b) Expression of LFA-1α and ICAM-1 in the developing rat brain: A potential mechanism for the recruitment of microglial cell precursors. Dev. Brain Res. 103:163-170.
23. Dalziel, H.H. and D.P. Westfall (1994) Receptors for adenine nucleotides and nucleosides: Subclassification, distribution, and molecular characterization. Pharmacol. Rev. 46:449-466.
24. Del Río Hortega, P. (1920) El tercer elemento de los centros nerviosos. III.-Naturaleza probable de la microglía. Bol. Soc. Esp. Biol. 8:154-166.
25. Del Río Hortega, P. (1921) El tercer elemento de los centros nerviosos. Histogénesis y evolución normal; éxodo y distribución regional de la microglía. Mem. Real Esp. Hist. Nat. 11:213-268.
26. Del Río Hortega, P. (1932) Microglia. In W. Penfield (ed): Cytology and Cellular Pathology of the Nervous System. Vol 2. New York: Paul B. Hoeber, pp. 481-534.
27. Ditrich, H. (1986) Brain macrophages in cerebellar cell cultures. Tissue Cell. 18:645-658.
28. Eng, L.F., J.J. Vanderhaeghen, A. Bignami, and B. Gerstl (1971) An acidic protein isolated from fibrous astrocytes. Brain Res. 28:351-354.
29. Fedoroff, S. (1995) Development of microglia. In H. Kettenmann and B.R. Ransom (eds): Neuroglia. New York: Oxford University Press, pp. 162-181.
30. Finsen, B., N. Tønder, G.F. Xavier, J.C. Sørensen, and J. Zimmer (1993) Induction of microglial immunomolecules by anterogradely degenerating mossy fibers in the rat hippocampal formation. J. Chem. Neuroanat. 6:267-275.
31. Fredholm, B.B., B. Johansson, I. van der Ploeg, P.S. Hu, and S. Jin (1993) Neuromodulatory roles of purines. Drug Dev. Res. 28:349-353.
32. Fredholm, B.B., M.P. Abbracchio, G. Burnstock, J.W. Daly, T.K. Harden, K.A. Jacobson, P. Leff, and M. Williams (1994) Nomenclature and classification of purinoreceptors. Pharmacol. Rev. 40:143-156.
33. Fujimoto, E., A. Miki, and H. Mizoguti (1987) Histochemical studies of the differentiation of microglial cells in the cerebral hemispheres of chick embryos and chicks. Histochemistry 87:209-216.
34. Fujimoto, E., A. Miki, and H. Mizoguti (1989) Histochemical studies of the differentiation of microglial cells in the cerebral hemispheres of chick embryos and chicks. J. Anat. 166:253-264.
35. Griffith, D.A. and S.M. Jarvis, (1996) Nucleoside and nucleobase transport systems of mammalian cells. Biochim. Biophys. Acta 1286:153-181.
36. Grondal, E.J., A. Janetzko, and H. Zimmermann (1988). Monospecific antiserum against 5′-nucleotidase from torpedo electric organ: Immunocytochemical distribution of the enzyme and its association with Shwann cell membranes. Neuroscience 24:351-363.
37. Guroff, G., G. Dickens, D. End, and C. Londos (1981) The action of adenosine analogs on PC12 cells. J. Neurochem. 37:1431-1439.
38. Heilbronn, A., V. Maienschein, K. Carstensen, W. Gann, and H. Zimmermann (1995) Crucial role of ecto-5′-nucleotidase in differentiation and survival of developing neural cells. Neuroreport 7:257-261.
39. Hösli, E. and L. Hösli (1988) Autoradiographic studies on the uptake of adenosine and on binding of adenosine analogues in neurones and astrocytes of cultured rat cerebellum and spinal cord. Neuroscience 24:621-628.
40. Ibrahim, M.Z.M., Y. Khreis, and D.S. Koshayan (1974) The histochemical identification of microglia. J. Neurol. Sci. 22:211-233.
41. Imamoto, K. and C.P. Leblond (1978) Radioautographic investigation of gliogenesis in the corpus callosum of young rats. II. Origin of microglial cells. J. Comp. Neurol. 180:139-163.
42. Jensen, M., B. González, B. Castellano, and J. Zimmer (1994) Microglial and astroglial reactions to anterograde axonal degeneration: A histochemical and immunocytochemical study of the adult rat fascia dentata after entorhinal path lesions. Exp. Brain Res. 98:245-260.
43. Jørgensen, M.B., B.R. Finsen, M.B. Jensen, B. Castellano, N. Diemer, and J. Zimmer (1993) Microglial and astroglial reactions to ischemic and kainic acid-induced lesions of the adult rat hippocampus. Exp. Neurol. 120:70-88.
44. Kaur, C., E.A. Ling, and W.C. Wong (1984) Cytochemical localization of 5′-nucleotidase in ameboid microglial cells in postnatal rats. J. Anat. 139:1-7.
45. Kaur, C., E.A. Ling, and W.C. Wong (1987) Origin and fate of neural macrophages in a stab wound of the brain of the young rat. J. Anat. 154:215-227.
46. Kettenmann, H., R. Banati, and W. Walz (1993) Electrophysiological behavior of microglia. Glia 7:93-101.
47. Kim, J.K., M.P. Rathbone, P.J. Middlemiss, D.W. Hughes, and R.W. Smith (1991) Purinergic stimulation of astroblast proliferation: Guanosine and its nucleotides stimulate cell division in chick astroblasts. J. Neurosci. Res. 28:442-455.
48. Kreutzberg, G.W. and K.D. Barron (1978) 5′-nucleotidase of microglial cells in the facial nucleus during axonal reaction. J. Neurocytol. 7:601-610.
49. Kreutzberg, G.W. and S.T. Hussain (1984) Cytochemical localization of 5′-nucleotidase activity in retinal photoreceptor cells. Neuroscience 11:857-866.
50. Kreutzberg, G.W., K.D. Barron, and P. Shubert (1978) Cytochemical localization of 5′-nucleotidase in glial plasma membranes. Brain Res. 158:247-257.
51. Kreutzberg, G.W., D. Heymann, and M. Reddington (1986) 5′-nucleotidase in the nervous system. In GW. Kreutzberg, M. Reddington, and H. Zimmermann (eds): Cellular Biology of Ectoenzymes. Berlin, Heidelberg, New York: Springer-Verlag, pp. 147-164.
52. Lawson, L.J., V.H. Perry, P. Dri, and S. Gordon (1990) Heterogeneity in the distribution and morphology of microglia in the normal adult mouse brain. Neuroscience 39:151-170.
53. Ling, E.A. (1977) Light and electron microscopic demonstration of some lysosomal enzymes in the amoeboid microglia in neonatal rat brain. J. Anat. 123:637-648.
54. Ling, E.A. (1979) Transformation of monocytes into amoeboid microglia and into microglia in the corpus callosum of postnatal rats, as shown by labelling monocytes by carbon particles. J. Anat. 128:847-858.
55. Ling, E.A. (1981) The origin and nature of microglia. In S. Federoff and L. Hertz (eds): Advance in Cellular Neurobiology. Vol II. New York: Academic Press, pp. 33-82.
56. Ling, E.A. and W.C. Wong (1993) The origin and nature of ramified and amoeboid microglia: A historical review and current contents. Glia 7:9-18.
57. Ling, E.A., D. Penney, and C.P. Leblond (1980) Use of carbon labelling to demonstrate the role of blood monocytes as precursors of the "amoeboid cells" present in the corpus callosum of postnatal rats. J. Comp. Neurol. 193:631-657.
58. López-García, C., J. Nacher, B. Castellano, J.A. Luís de la Iglesia, and A. Molowny (1994) Transitory disappearance of microglia during the regeneration of the lizard medial cortex. Glia 12:52-61.
59. Matz, H. and L. Hertz, (1989) Adenosine metabolism of neurons and astrocytes in primary cultures. J. Neurosci. Res. 24:260-267.
60. Muller, M.M., M. Kraupp, P. Chiba, and H. Rumpold (1983) Regulation of purine uptake in normal and neoplastic cells. Adv. Enzyme Regul. 21:239-256.
61. Murabe, Y. and Y. Sano (1982) Morphological studies on neuroglia. VI. Postnatal development of microglial cells. Cell Tissue Res. 225:469-485.
62. Naito, M., K. Takahashi, and S. Nishikawa (1990) Development, differentiation, and maturation of macrophages in the fetal mouse liver. J. Leukoc. Biol. 48:27-37.
63. Naito, M., S. Umeda, T. Yamamoto, H. Moriyama, H. Umezu, G. Hasegawa, H. Usuda, L.D. Shultz, and K. Takahashi (1996) Development, differentiation, and phenotypic heterogeneity of murine tissue macrophage. J. Leukoc. Biol. 59:133-138.
64. Navascués, J., M.A. Cuadros, and A. Almendros (1996) Development of microglia: Evidence from studies in the avian central nervous system. In E.A. Ling, C.K. Tan, and C.B.C. Tan (eds): Topical Issues in Microglial Research. Singapore: Singapore Neuroscience Association, pp. 43-64.
65. Neary, J.T., M.P. Rathbone, F. Cattabeni, M.P. Abbracchio, and G. Burnstock (1996) Trophic actions of extracellular nucleotides and nucleosides on glial and neuronal cells. Trends Neurosci. 19:13-18.
66. Norenberg, W., P. Illes, and P.J. Gebicke-Haerter (1994) Sodium channel in isolated human brain macrophages. Glia 10:165-172.
67. Novikoff, A.B. and S. Goldfisher (1961) Nucleoside diphosphatase activity in the Golgi apparatus and its usefulness for cytological studies. Proc. Natl. Acad. Sci. USA 47:802-810.
68. Parker, A.L., L.L. Likar, D.D. Dawicki, and S. Rounds (1996) Mechanism of ATP-induced leukocyte adherence to cultured pulmonary artery endothelial cells. Am J. Physiol. 270:659-703.
69. Perry, V.H. and S. Gordon (1991) Macrophages and the nervous system. Int. Rev. Cytol. 125:203-243.
70. Perry, V.H., D.A. Hume, and S. Gordon (1985) Immunohistochemical localization of macrophages and microglia in the adult and developing mouse brain. Neuroscience 15:313-326.
71. Qiu-Sheng, S., Y. Nakamura, P. Shubert, K. Rudolphi, and K. Kataoka (1996) Adenosine and propentofylline inhibit the proliferation of cultured microglial cells. Exp. Neurol. 137:345-349.
72. Rathbone, M.P., S. DeForge, B. DeLuca, B. Gabel, C. Laurenssen, P. Middlemiss, and S. Parkinson (1992a) Purinergic Stimulation of cell division and differentiation: Mechanisms and pharmacological implications. Med. Hypotheses 37:213-219.
73. Rathbone, M.P., L. Christjanson, S. DeForge, B. DeLuca, J.W. Gysbers, S. Hindley, M. Jovetich, P.J. Middlemiss, and S. Takhal (1992b) Extracellular purine nucleosides stimulate cell division and morphogenesis: Pathological and physiological implications. Med. Hypotheses 37:232-240.
74. Rathbone, M.P., P. Middlemiss, J.K. Kim, J.W. Gysbers, S. DeForge, R.W. Smith, D.W. Hughes (1992c) Adenosine and its nucleotides stimulate proliferation of chick astrocytes and human astrocytoma cells. Neurosci. Res. 13:1-17.
75. Sanyal, S. and A. De Ruiter (1985) Inosine diphosphatase as a histochemical marker of retinal microvasculature, with special reference to transformation of microglia. Cell Tissue Res. 241:291-297.
76. Schnitzer, J. (1989) Enzyme-histochemical demonstration of microglial cells in the adult and postnatal rabbit retina. J. Comp. Neurol. 282:249-263.
77. Schnitzer, J. and J. Sherer (1990) Microglial cell responses in the rabbit retina following transection of the optic nerve. J. Comp. Neurol. 302:779-791.
78. Schoen, S.W., M.B. Graeber, L. Toth, and G.W. Kreutzberg (1988) 5′-nucleotidase in postnatal ontogeny of rat cerebellum: A marker for migrating nerve cells? Dev. Brain Res. 39:125-136.
79. Schoen, S.W., B. Leutenecker, G.W. Kreutzberg, and W. Singer (1990) Ocular dominance plasticity and developmental changes of 5′-nucleotidase distributions in the kitten visual cortex. J. Comp. Neurol. 296:379-392.
80. Schoen, S.W., M.B. Graeber, L. Toth, and G.W. Kreutzberg (1991) Synaptic 5′-nucleotidase is transient and indicative of climbing fiber plasticity during the postnatal development of rat cerebellum. Dev. Brain Res. 61:125-138.
81. Schoen, S.W., M.B. Graeber, and G.W. Kreutzberg (1992) 5′-nucleotidase immunoreactivity of perineuronal microglia responding to rat facial nerve axotomy. Glia 6:314-317.
82. Schoen, S.W., G.W. Kreutzberg, and W. Singer (1993) Cytochemical redistribution of 5′-nucleotidase in the developing cat visual cortex. Eur. J. Neurosci. 5:210-222.
83. Simmonds, H.A. (1991) Purine metabolic disorders and neurological dysfunction. In T. Stone (ed): Adenosine in the Nervous System. London: Academic Press, pp. 247-265.
84. Sjöstrand, J. (1966) Changes of nucleoside phosphatase activity in the hypoglossal nucleus during nerve regeneration. Acta Physiol. Scand. 67:219-228.
85. Sorokin, S.P., R.F. Hoyt, Jr., D.G. Blunt, and N.A. McNelly (1992) Macrophage development: II. Early ontogeny of macrophage populations in brain, liver, and lungs of rat embryos as revealed by a lectin marker. Anat. Rec. 232:527-550.
86. Sørenaen, J.C., I. Dalmau, J. Zimmer, and B. Finsen (1996) Microglial reactions to tracer identified thalarmic neurons after frontal motocortex lesions in adult rats. Exp. Brain Res. 112:203-212.
87. Sperlágh, B. and S. Vizi (1996) Neuronal synthesis, storage and release of ATP. Semin. Neurosci. 8:175-186.
88. Streit, W.J. (1995) Microglial cells. In H. Kettenmann and B.R. Ransom (eds): Neuroglia. New York: Oxford University Press, pp. 85-96.
89. Sunderman, F.W. Jr., (1990) The clinical biochemistry of 5′-nucleotidase. Ann. Clin. Lab. Sci. 20:123-139.
90. Takahashi, K. and M. Naito (1993) Development, differentiation, and proliferation of macrophages in the ra yolk sac. Tissue Cell 25:351-362.
91. Takahashi, K., F. Yamamura, and M. Naito (1989) Differentiation, maturation, and proliferation of macrophages in the mouse yolk sac: A light-microscopic, enzyme-cytochemical, immunohistochemical, and ultrastructural study. J. Leukoc. Biol. 45:87-96.
92. Takahashi, K., M. Naito, and M. Takeya (1996) Development and heterogeneity of macrophages and their related cells through their differentiation pathways. Pathol. Int. 46:473-485.
93. Thomas, W.E. (1992) Brain macrophages: Evaluation of microglia and their functions. Brain Res. Rev. 17:61-74.
94. Vela, J.M., I. Dalmau, B. González, and B. Castellano (1995a) Morphology and distribution of microglial cells in the young and adult mouse cerebellum. J. Comp. Neurol. 361:602-616.
95. Vela, J.M., I. Dalmau, L. Acarín, B. González, B. Castellano (1995b) Microglial cell reaction in the gray and white matter in spinal cords from jumpy mice. An enzyme histochemical study at the light and electron microscope level. Brain Res. 694:287-298.
96. Vordrodt, A.W. and H.M. Wisniewski (1982) Plasmalemma-bound nucleoside diphosphatase as a cytochemical marker of central nervous system (CNS) mesodermal cells. J. Histochem. Cytochem. 30:418-424.
97. Wachstein, M. and E. Meisel (1957) Histochemistry of hepatic phosphatases at a physiological pH. Am. J. Clin. Pathol. 27:13-23.
98. Wang, D.J., N.N. Huang, and L.A. Heppel (1990) Extracellular ATP shows synergistic enhancement of DNA synthesis when combined with agents that are active in wound healing or as neurotransmitters. Biochem. Biophys. Res. Commun. 166:251-258.
99. 1-adenosine receptor gene expression in fetal rat brain. Dev. Brain Res. 94:205-223.
100. Wisniewski, H.M., A.W. Vordrodt, J. Wegiel, J. Morys, and A.S. Lossinsky (1990) Ultrastructure of the cells forming amyloid fibers in Alzheimer disease and scrapie. Am. J. Med. Genet. Suppl. 7:287-297.
101. Wu, P.H. and J.W. Phillis (1984) Uptake by central nervous tissues as a mechanism for the regulation of extracellular adenosine concentrations. Neurochem. Int. 6:613-1824.
102. Zimmermann, H (1994) Signalling via ATP in the nervous system. Trends Neurosci. 17:420-426.
103. Zoref-Shani, E., Y. Bromberg, G. Lilling, I. Gozes, S. Brosh, Y. Sidi. and O. Sperling (1995) Developmental changes in purine nucleotide metabolism in cultured rat astroglia. Int. J. Dev. Neurosci. 13:887-896.