Neuron-Glia Cross Talk in Rat Striatum after Transient Forebrain Ischemia

  • Michele Zoli
  • Giuseppe Biagini
  • Rosaria Ferrari
  • Patrizia Pedrazzi
  • Luigi F. Agnati
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 429)

Abstract

Striatum is highly vulnerable to transient forebrain ischemia induced by the 4 vessel occlusion (4V0) method (Brierley 1976. Pulsinelli et al. 1982, Zini et al. 1990a). Massive degeneration and loss of Nissl-stained neurons occur within 24 hr from an ischemia of long duration (30 min) (Pulsinelli et al. 1982). Neuronal loss is mainly restricted to the lateral part of caudate-putamen (Pulsinelli et al. 1982, Zini et al. 1990a). Cellular alterations include loss of medium-size spiny projection neurons (Pulsinelli et al. 1982, Francis and Pulsinelli 1982), largely corresponding to dopaminoceptive neurons (Benfenati et al. 1989, Zoli et al. 1989), and increase in reactive astrocytes (Pulsinelli et al. 1982, Grimaldi et al. 1990) and microglia (Gehrmann et al. 1982). On the other hand, large cholinergie (Francis and Pulsinelli 1982) and medium-size aspiny somatostatin (SS)/neuropeptide Y (NPY)-containing interneurons are resistant to the ischemic insult (Pulsinelli et al. 1982, Grimaldi et al. 1990). In a few instances, such as in the case of SS and NPY immunoreactivity (IR), the initial loss is followed by full recovery within 7 (SS) or 40 (NPY) days post-ischemia (Grimaldi et al. 1990). However, it is not known whether some kind of recovery is present for the bulk of medium-size spiny projections neurons after the first days post-ischemia.

Keywords

Glial Fibrillary Acidic Protein Reactive Astrocyte Microdialysis Probe Polyamine Metabolism Polyamine Level 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Agnati L.F., Fuxe K., Davalli P., Zini I., Corti A., Zoli M. Striatal ornithine decarboxylase activity following neurotoxic and mechanical lesions of the mesostriatal dopamine system of the male rat. Acta Physiol. Scand. 125 (1985a) 173–175Google Scholar
  2. Agnati L.F., Fuxe K., Zoli M., Davalli P., Corti A., Zini I., Toffano G. Effects of neurotoxic and mechanical lesions of the mesostriatal dopamine pathway on striatal polyamine levels in the rat: modulation by chronic ganglioside GM I treatment. Neurosci. Lett. 61 (1985b) 339–344PubMedCrossRefGoogle Scholar
  3. Agnati L.P., Fuxe K., Zini I., Davalli P., Corti A., Calza L., Toffano G., Zoli M., Piccinini G., Goldstein M. Effects of lesions and ganglioside GM I treatment on polyamine levels and nigral DA neurons. A role of putrescine in the neurotrophic activity of gangliosides. Acta Physiol. Scand. 124 (1985e) 499–506Google Scholar
  4. Agnati L.F., Fuxe K., Zoli M., Zini I., Härfstrand A., Toffano G., Goldstein M. Morphometrical and microdensitometrical studies on phenylethanolamine-N-methyltransferase and neuropeptide Y immunoreactive neurons in the rostra) medulla oblongata of the adult and old male rats. Neuroscience 26 (1988) 461–478PubMedCrossRefGoogle Scholar
  5. Agnati L.F., Zoli M., Strömberg I., Fuxe K. Intercellular communication in the brain: Wiring versus volume transmission. Neuroscience 69 (1995) 711–726.Google Scholar
  6. Astrup J. Siesjo B.K., Symon L. Threshold in cerebral ischemia–the ischemic penumbra. Stroke 12 (1981) 723–725PubMedCrossRefGoogle Scholar
  7. Balasingam V., Tejada-Berges T., Wright E., Bouckova R., Yong V.W. Reactive astrogliosis in the neonatal mouse brain and its modulation by cytokines. J. Neurosci. 14 (1994) 846–856PubMedGoogle Scholar
  8. Baudry M., Najm 1. Kainate-induced seizure activity stimulates the polyamine interconersion pathway in rat brain. Neurosci. Lett. 171 (1994) 151–154PubMedCrossRefGoogle Scholar
  9. Beal M.F., Kowall N.W., Ellison D.W., Mazureck M.F., Swartz K.J., Martin J.B. Replication of the neurochemical characteristics of Huntington’s disease by quinolinic acid. Nature 321 (1986) 168–171.PubMedCrossRefGoogle Scholar
  10. Beck K.D., Lamballe F., Rudiger K., Barbacid M., Schauwecker PE., McNeill T.H., Finch C.E., Hefti F., Day J.R. Induction of non-catalytic trkB neurotrophin receptors during axonal sprouting in the adult hippocampus. J Neurosci. 13 (1993) 4001–4014PubMedGoogle Scholar
  11. Benfenati F., Merlo Pich E., Grimaldi R., Zoli M., Fuxe K., “Toffano G., Agnati L.F. Transient forebrain ischemia produces multiple deficits in dopamine DI transmission in the lateral neostriatum of the rat. Brain Res. 498 (1989)376–380Google Scholar
  12. Biagini G., Frasoldati A., Fuxe K., Agnati L.F. The concept of astrocyte-kinetic drug in the treatment of neurodegenerative diseases: Evidence for L-deprenyl-induced activation of reactive astrocytes. Neurochem. Int. 25 (1994) 17–22PubMedCrossRefGoogle Scholar
  13. Bignami A., Dahl D. Differentiation of astrocytes in the cerebellar cortex and the pyramidal tracts of the newborn rat. An immunofluorescence study with antibodies to a protein specific to astrocytes. Brain Res. 49 (1973) 393–402PubMedCrossRefGoogle Scholar
  14. Bignami A., Dahl D., Rueger DG. Glial fibrillary acidic (GFA) protein in normal neuronal cells and in pathological conditions, in Federoff S, Hertz L (eds): Advances in cellular neurobiology, vol I. New York, Academic Press, 1980, pp 285–310Google Scholar
  15. Brierley J. Cerebral hypoxia, in Blackwood W, Corsellis J (eds): Grenficld’s Neuropathology, London. Edward Arnold, 1976, pp 43–85Google Scholar
  16. Brock T.O., O’Callaghan J.P. Quantitative changes in the synaptic vesicle proteins, synapsin I and p38, and the astrocyte specific protein, glial fibrillary acidic protein, are associated with chemical-induced injury to the rat central nervous system. J Neurosci. 7 (1987) 931–942PubMedGoogle Scholar
  17. Casero R.A., Pegg A.E., Spermidine/spennine NI-acetyltransferase–the turning point in polyamine metabolism. FASEB J. 7 (1993) 653–661PubMedGoogle Scholar
  18. Cheng H-W., Jiang T., Brown S.A., Pasinetti G.M., Finch C.E., McNeill H. Response of striatal astrocytes to neuronal deafferentiation: an imtnunocytochemical an ultrastructural study. Neuroscience 62 (1994) 425–439PubMedCrossRefGoogle Scholar
  19. Cooper S.M. Intercellular signaling in neuronal-glial networks. Biosystems 34 (1995) 65–85PubMedCrossRefGoogle Scholar
  20. Desiderio M.A., Davalli P., Perin A. Simultaneous determination of y-aminobutyric acid and polyamines by high performance liquid chromatography. J. Chromatograph. 419 (1987) 285–290Google Scholar
  21. Desiderio M.A., Zini 1., Davalli P., Zoli M., Corti A., Fuxe K., Agnati L.F. Polyamines, ornithine decarboxylase, and diamine oxidase in the substantia nigra and striatum of the male rat after hemitransection. J. Neurochem. 51 (1988)25–31Google Scholar
  22. Dienel G.A., Cruz N.F., Induction of brain ornithine decarboxylase during recovery from metabolic, mechanical, thermal or chemical injury. J. Neurochem. 42 (1984) 1053–1061.PubMedCrossRefGoogle Scholar
  23. du Bois M., Bowman P.D., Goldsten G.W. Cell proliferation after ischemic injury in gerbil brain. An immunocytochemical and autoradiographie study. Cell Tissue Res. 242 (1985) 17–23PubMedCrossRefGoogle Scholar
  24. Eng L.F. Glial fibrillary acidic protein (GFAP): the major protein of glial intermediate filaments in differentiated astrocytes. J. Neuroimmunol. 8 (1985) 203–214PubMedCrossRefGoogle Scholar
  25. Eng L.F., De Armond S.J. Immunocytochemical study of astrocytes, in normal development and diseas, in Federoff S, Hertz L (eds): Advances in cellular neurobiology, vol 3, New York, Academic Press, 1982. 145–171Google Scholar
  26. Ferraguti F., Zoli M., Aronsson M., Agnati L.F., Goldstein M., Filer D. Fuxe K. Distribution of glutamic acid de-carboxylase messenger RNA containing nerve cell populations of the male rat brain.I. Chem. Neuroanat. 3 (1990) 377–396Google Scholar
  27. Ferrante R.J., Kowall L.W., Beal M.F., Richardson E.P., Bir E.D., Martin J.B. Selective sparing of a class of striatal neurons in Huntington’s disease. Science 230 (1986) 561–563CrossRefGoogle Scholar
  28. Francis A., Pulsinelli W.A. Response of GABAergic and cholinergie neurons to transient cerebral ischemia. Brain Res. 243 (1982) 271–278PubMedCrossRefGoogle Scholar
  29. Gehrmann J., Bonnekoh P., Miyazawa T., Hossmann K-A., Kreutzberg G.W. Immunocytochemical study of an early microglial activation in ischemia. J. Cereb. Blood Flow Metab. 12 (1982) 257–269CrossRefGoogle Scholar
  30. Giulian D., Vaca K., Corpuz M. Brain glia release factors with opposing actions upon neuronal survival. J. Neuro-sci. 13 (1993) 29–37Google Scholar
  31. Grimaldi R., Zoli M., Agnati L.F., Ferraguti F., Fuxe K., Toffano G., Zini I. Effects of transient forebrain ischemia on peptidergic neurons and astroglial cells. Evidence for recovery of peptide immunoreactivities in neo-cortex and striatum but not hippocampal formation. Exp. Brain Res. 82 (1990) 123–136PubMedCrossRefGoogle Scholar
  32. Hansson E., Rönnback L. Astrocytes in glutamate neurotransmission. FASEB J. 9 (1995) 343–350 Heiss W-D., Graf R. The ischemic penumbra. Curr. Op. Neurol. 7 (1994) 11–19Google Scholar
  33. Hemmings H. Jr., Nestler E.J., Walaas I.S., Ouimet C.C., Greengard P. Protein phosphorylation and neuronal function: DARPP-32, an illustrative example, in Edelman GM, Gall WE, Cowan WM (eds): Synaptic function, New York, John Wiley, 1987, pp 213–240Google Scholar
  34. Hossmann K.A. Disturbances of cerebral protein synthesis and ischemic cell death. Prog. Brain Res. 96 (1993) 161–177Google Scholar
  35. Hossmann K.A. Viability thresholds and the penumbra of focal ischemia. Ann. Neurol. 36 (1994) 557–565Google Scholar
  36. Iänne J., Williams-Ashman H.G. On the purification of L-ornithine decarboxylase from rat prostate and effects of thiol compounds on the enzyme. J. Biol. Chem 246 (1971) 1725–1732Google Scholar
  37. Jänne J., Pösö H., Raina A. Polyamines in rapid growth and cancer. Biochem. Biophys. Acta 473 (1978) 241–293PubMedGoogle Scholar
  38. Johansson O., Hökfelt T. Elde R.P. Immunohistochemical distribution of somatostatin-like immunoreactivity in the central nervous system of the adult rat. Neuroscience 13 (1984) 265–339PubMedCrossRefGoogle Scholar
  39. Junier M.-P., Coulpier M., Le Forestier N., Cadusseau J., Suzuki F., Peschanski M., Dreyfus P.A. Transforming Growth Factor a (TGFa) expression in degenerating motoneurons of the murine mutanet wohller: a neuronal signal for astrogliosis ? J. Neurosci. 14 (1994) 4206–4216PubMedGoogle Scholar
  40. Kawaguchi Y., Wilson C.J., Augood S.J. Emson PC: Striatal interneurones: chemical. physiological and morphological characterization. Trends Neurosci. 18 (1995) 527–535PubMedCrossRefGoogle Scholar
  41. Kerkerian L., Salin P., Nieoullon A. Cortical regulation of striatal neuropeptide Y (NPY)-containing neurons in the rat. Fur. J. Neurosci. 2 (1989) 181–189Google Scholar
  42. Kleihues P., Hossmannn K.A., Pegg A.E., Kobayashi K., Zimmermann V. Resuscitation of the monkey brain after one hour complete ischemia. III. Indications of metabolic recovery. Brain Res. 95 (1975) 61–73PubMedCrossRefGoogle Scholar
  43. Kogure K., Kato H. Altered gene expression in cerebral ischemia. Stroke 24 (1993) 2121–2127PubMedCrossRefGoogle Scholar
  44. Kondo Y., Ogawa N., Asanuma M., Ota Z., Mori A. Regional differences in late-onset iron deposition, ferritin, transferrin, astrocytes proliferation and microglial activation after transient forebrain ischemia. J. Cereb. Blood Flow Metab. 15 (1995) 216–226PubMedCrossRefGoogle Scholar
  45. Krause G.S., Tiffany B.R. Suppression of protein synthesis in the reperfused brain. Stroke 24 (1993) 747–755.PubMedCrossRefGoogle Scholar
  46. Largo C., Cuevas P. Somjen G.G., Martin del Rio R., Hen-eras O. The effect of depressing glial function in rat brain in situ on ion homeostasis, synaptic transmission, and neuron survival. J. Neurosci. 16 (1996) 1219–1229PubMedGoogle Scholar
  47. Ludwin S.K. Reaction of oligodendrocytes to trauma and implantation. A combined autoradiographic and immunohistochemical study. Lab. Invest. 52 (1985) 20–30.PubMedGoogle Scholar
  48. Manthorpe M., Rudge J.S., Varon S. Astroglial cell contributions to neuronal survival and neuritic growth, in Federoff S, Vernadakis A (eds): Astrocytes. New York, Academic Press, 1986, pp 315–376Google Scholar
  49. Mathewson A.J., Berry M. Observations on astrocyte response to a cerebral stab wound in adult rats. Brain Res. 327 (1985) 61–69PubMedCrossRefGoogle Scholar
  50. Matthews D.A., Cotman C.W., Lynch G. An electron microscopic study of lesion-induced synaptogenesis in the dentate gyrus of the adult rat. 1. Magnitude and time course of degeneration. Brain Res. 115 (1976) 1–21PubMedCrossRefGoogle Scholar
  51. Miller M., Cleef M., Röhn G., Bonnekoh P., Pajunen A.E.I., Bernstein H.G., Paschen W. Ornithine decarboxylase in reversible cerebral ischemia. An immunohistochemcial study. Acta Neuropathol. 83 (1991) 39–45CrossRefGoogle Scholar
  52. Needels D.L., Nieto-Sampedro M., Cotman C.W. Induction ofa neurite-promoting factor in rat brain following injury or deafferentation. Neuroscience 18 (1986) 517–526.PubMedCrossRefGoogle Scholar
  53. Nieto-Sampedro M., Lewis E.R., Cotman C.W., Manthorpe M., Skaper S.D., Barbin G., Longo F.M., Varon S. Brain injury causes a time-dependent increase in neuronotrophic activity at the lesion site. Science 217 (1982) 860–861PubMedCrossRefGoogle Scholar
  54. Paschen W., Schmidt-Kastner R., Djuricic B., Meese C., Linn F., Hossmann K.A. Polyamine changes in reversible cerebral ischemia. J. Neurochem. 49 (1987) 35–37CrossRefGoogle Scholar
  55. Paschen W., Röhn G., Meese C.O., Djuricic B., Schmidt-Kastner R. Polyamine metabolism in reversible cerebral ischemia: effect of cc-difluoromethylornithine. Brain Res. 453 (1988) 9–16PubMedCrossRefGoogle Scholar
  56. Paschen W., Csiba L., Röhn G., Bereczki D. Polyamine metabolism in transient focal ischemia of rat brain. Brain Rcs_ 566 (1991) 354–357CrossRefGoogle Scholar
  57. Paxinos G., Watson C. The rat brain in stereotaxic coordinates. London, Academic Press, 1982Google Scholar
  58. Pegg A.E. Recent advances in the biochemistry of polyamines in eukaryotes. Biochem. J. 234 (1986) 249–262PubMedGoogle Scholar
  59. Pegg A.E., McCann P.P. Polyamine metabolism and function. Am. J. Physiol. 243 (1982) C212 — C221Google Scholar
  60. Pegg A.E., McCann P.P. Polyamine metabolism and function in mammalian cells and protozoans. ISI Atlas Sci. Biochem. 1 (1988) 1 1–18Google Scholar
  61. Percz-Pinon M.A. Tao L., Nicholson C. Extracellular potassium, volume fraction, and tortuosity in rat hippocampal CAI, CA3, and cortical slices during ischemia. J. Neurophysiol. 74 (1995) 565–573Google Scholar
  62. Petito C.K., Morgello S., Felix J.C., Lesser M.L. The two patterns of reactive astrocytosis in postischemic rat brain.,l Cereb. Blood Flow Metab. 10 (1990) 850–859CrossRefGoogle Scholar
  63. Porcella A., Carter C., Fage D., Voltz C., Lloyd K.G., Serrano A., Scatton, B. The effects of N-methyl-D-aspartate and kainate lesions of the rat striatum on striatal ornithine decarboxylase activity and polyamine levels. Brain Rcs. 549 (1991) 205–212CrossRefGoogle Scholar
  64. Pulsinelli W.A., Brierley J.B. A new model of bilateral hemispheric ischemia on the unanesthetized rat. Stroke 10 (1979) 267–272PubMedCrossRefGoogle Scholar
  65. Pulsinelli W.A., Brierley J.B., Plum F. Temporal profile of neuronal damage in a model of transient forebrain ischemia. Ann. Neurol. 1 (1982) 491–498CrossRefGoogle Scholar
  66. Raisman G., Field P.M. A quantitative investigation of the development of collateral reinnervation after partial deafferentation of the septal nuclei. Brain Res. 50 (1973) 241–264PubMedCrossRefGoogle Scholar
  67. Reilly J.F., Kumari V.G. Alterations in Fibroblast Growth Factor receptor expression following brain injury. Exp. Neurol. 140 (1996) 139–150PubMedCrossRefGoogle Scholar
  68. Röhn G., Schlenker M., Paschen W. Activity of ornithine decarboxylase and S-adenosylmethionine decarboxylase in transient cerebral ischemia: relationship to the duration of vascular occlusion. Exp. Neurol. 117 (1992) 210–215PubMedCrossRefGoogle Scholar
  69. Scott R.H., Sutton K.G., Dolphin A.C. Interactions of polyamines with neuronal ion channels. Trends Neurosci. 16 (1993) 153–160PubMedCrossRefGoogle Scholar
  70. Seiler N., Bolkenius F.N., Knödgen B. The influence of catabolic reactions on polyamine excretion. Biochem. J. 225 (1985) 219–226PubMedGoogle Scholar
  71. Seiler N., Deckhardt K. Uptake of polyamines and related compounds into nerve endings. Adv. Pol. Res. 2 (1978) 101–107Google Scholar
  72. Snyder S.E., Li J., Schauwecker P.E., McNeill T.H., Salton S.R.J. mRNA expression in the developing and adult rat nervous system and induction of Rptp-Zeta/Beta and phosphacan mRNA following brain injury. Mol. Brain Res. 40 (1996) 79–96PubMedCrossRefGoogle Scholar
  73. Steindler D.A. Glial boundaries in the developing nervous system. Annu. Rev. Neurosci. 16 (1993) 445–470CrossRefGoogle Scholar
  74. Sykova E., Svoboda J., Polak J., Chvatal A. Extracellular volume fraction and diffusion characteristics during progressive ischemia and terminal anoxia in the spinal-cord of the rat. J. Cereb. Blood Flow Metab. 14 (1994) 301–311PubMedCrossRefGoogle Scholar
  75. Tsacopoulos M., Magistretti P.J. Metabolic coupling between glia and neurons. J. Neurosci. 16 (1996) 877–885Google Scholar
  76. Vincent S. R., Kimura H. Histochemical mapping of nitric oxide synthase in the rat brain. Neuroscience 46 (1992) 755–784PubMedCrossRefGoogle Scholar
  77. Zini I., Grimaldi R., Merlo Pich E., Zoli M., Fuxe K., Agnati L.F. Aspects of neural plasticity in the central nervous system. V. Studies on a model of transient forebrain ischemia in male Sprague dawley rats. Neurochem. Int. 16 (1990a) 451–468PubMedCrossRefGoogle Scholar
  78. Zini I., Zoli M., Grimaldi R., Merlo Pich E., Biagini G., Fuxe K., Agnati L.F. Evidence for a role of neosynthetized putrescine in the increase of glial fibrillary acidic protein immunoreactivity induced by a mechanical lesion in the rat brain. Neurosci. Lett. 120 (1990b) 13–16PubMedCrossRefGoogle Scholar
  79. Zoll M., Grimaldi R., Agnati L.F., Zini 1., Merlo Pich E., Toffano G., Fuxe K. Neurohistochemical studies on striatal lesions induced by transient forebrain ischemia. E.idence for protective effects of the ganglioside analogue AGF2. Neurosci. Res. Comm. 4 (1989) 153–158Google Scholar
  80. Zoli M., Zini I., Agnati LF., Guidolin D., Ferraguti F., Fuxe K. Aspects of neural plasticity in the central nervous system. 1. Computer-assisted image analysis methods. Neurochem. Int. 16 (1990) 383–418PubMedCrossRefGoogle Scholar
  81. Zoli M., Bettuzzi S., Ferraguti F., Ingletti M.C., Zini 1. Fuxe K., Agnati L.F., Corti A. Regional increase in orni-thine decarboxylase mRNA levels in the rat brain after partial mesodiencephalic hemitransection as revealed by in situ hybridization histochemistry. Neurochem. Int. 18 (1991) 347–52PubMedCrossRefGoogle Scholar
  82. Zoli M., Zini I., Grimaldi R., Biagini G., Agnati L.F. Effects of putrescine synthesis blockade on neuronal loss and astroglial reaction after transient forebrain ischemia. Int. J. Dev. Neurosci. 11 (1993) 175–187PubMedCrossRefGoogle Scholar
  83. Zoli, M., Le Novère, N., Hill, J.A. jr. and Changeux, J.P., Developmental regulation of nicotinic receptor subunit mRNAs in the rat central and peripheral nervous systems. J. Neurosci. 15 (1995) 1912–1939Google Scholar
  84. Zoli M., Pedrazzi P., Zini I., Agnati L.F. Spermidine/spermine N’-acetyltransferase mRNA levels show marked.ind region-specific changes in the early phase after transient forebrain ischemia. Mol. Brain Res. 38 (1996): 22–134CrossRefGoogle Scholar
  85. Zoli M., Grimaldi R., Ferrari R., Zini I, Agnati L.F. Short- and long-term changes in striatal neurons and astroglia after transient forebrain ischemia. Stroke (1997), in pressGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1997

Authors and Affiliations

  • Michele Zoli
    • 1
    • 2
  • Giuseppe Biagini
    • 1
    • 2
  • Rosaria Ferrari
    • 1
    • 2
  • Patrizia Pedrazzi
    • 1
    • 2
  • Luigi F. Agnati
    • 1
    • 2
  1. 1.Section of Physiology Department of Biomedical SciencesUniversity of ModenaItaly
  2. 2.Interuniversity Center for the Study of AgingMilanItaly

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