Using comparative anatomy in the axotomy model to identify distinct roles for microglia and astrocytes in synaptic stripping

Neuron Glia Biology

Volumn 7, Issue 1, 2012, Pages 55-66

  Jinno, Shozo ^a   Yamada, Jun ^a  

^a KYUSHU UNIVERSITY   (Japan)

Author keywords

Axotomy; comparative anatomy; glial augmentation; neuronal survival; synaptic stripping

Indexed keywords

ARTICLE; ASTROCYTE; CELL FUNCTION; CELL SURVIVAL; CELL VIABILITY; COMPARATIVE ANATOMY; FACIAL NERVE; HUMAN; MICROGLIA; MOUSE STRAIN; NERVE CELL LESION; NERVE ENDING; NERVE FIBER REGENERATION; NERVE FIBER TRANSECTION; NEUROPROTECTION; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; RAT STRAIN; SPECIES DIFFERENCE; STRAIN DIFFERENCE; SYNAPSE; SYNAPTIC STRIPPING;

ANATOMY, COMPARATIVE; ANIMALS; ASTROCYTES; AXOTOMY; CELL PROLIFERATION; FACIAL NERVE DISEASES; HUMANS; MICE; MICROGLIA; NEURONS; RATS; SPECIES SPECIFICITY; SYNAPTIC TRANSMISSION; WOUNDS AND INJURIES;

MUS; RATTUS;

EID: 84864722164     PISSN: 1740925X     EISSN: 17410533     Source Type: Journal    
DOI: 10.1017/S1740925X11000135     Document Type: Article

References (101)

1. Adrian E.K. Jr., Williams M.G. and George F.C. (1978) Fine structure of reactive cells in injured nervous tissue labeled with 3H-thymidine injectedbefore injury. Journal of Comparative Neurology 180, 815-839.
2. Aldskogius H. (1978) Lipid accumulation in axotomized adult rabbit vagal neurons. Electron microscopical observations. Brain Research 140, 349-353.
3. Aldskogius H. (1982) Glial cell responses in the adult rabbit dorsal motor vagal nucleus during axon reaction. Neuropathology and Applied Neurobiology 8, 341-349.
4. Aldskogius H., Barron K.D. and Regal R. (1980) Axon reaction in dorsal motor vagal and hypoglossal neurons of the adult rat. Light microscopy and RNA-cytochemistry. Journal of Comparative Neurology 193, 165-177.
5. Araque A. and Perea G. (2004) Glial modulation ofsynaptic transmission in culture. Glia 47, 241-248.
6. Arvidsson J. and Aldskogius H. (1982) Effect of repeated hypoglossal nerve lesions on the number of neurons in the hypoglossal nucleus of adult rats. Experimental Neurology 75, 520-524.
7. Banati R.B., Gehrmann J., Schubert P. and Kreutzberg G.W. (1993) Cytotoxicity of microglia. Glia 7, 111-118.
8. Barron K.D. (2004) The axotomy response. Journal of Neurological Science220, 119-121.
9. Barron K.D., Marciano F.F., Amundson R. and Mankes R. (1990) Perineuronal glial responses after axotomy of central and peripheral axons. A comparison. Brain Research 523, 219-229.
10. Biber K., Neumann H., Inoue K. and Boddeke H.W. (2007) Neuronal 'On' and 'Off' signals control microglia. Trends in Neurosciences 30, 596-602.
11. Blinzinger K. and Kreutzberg G. (1968) Displacement ofsynaptic term-inals from regenerating motoneurons by microglial cells. Zeitschriftfür Zellforschung und Mikroskopische Anatomie 85 145-157.
12. Blackburn D., Sargsyan S., Monk P.N. and Shaw P.J. (2009) Astrocyte function and role in motor neuron disease: a future therapeutic target? Glia 57, 1251-1264.
13. Borke R.C. (1982) Perisomatic changes in the maturing hypoglossal nucleus after axon injury. Journal of Neurocytology 11, 463-485.
14. Cajal Y.R. (1928) Cajal's degeneration and regeneration of the nervous system. In DeFilipe J. & Jones E.G. (eds) History of Neuroscience No. 5. New York: Oxford University Press, 1991.
15. Cardona A.E., Pioro E.P., Sasse M.E., Kostenko V., Cardona S.M., Dijkstra I.M. et al. (2006) Control of microglial neurotoxicity by the fractalkine receptor. Nature Neuroscience 9, 917-924.
16. Carlson J., Lais A.C. and Dyck P.J. (1979) Axonal atrophy from perma-nent peripheral axotomy in adult cat. Journal of Neuropathology and Experimental Neurology 38, 579-585.
17. Castonguay A., Lévesque S. and Robitaille R. (2001) Glial cells as active partners in synaptic functions. Progress in Brain Research 132, 227-240.
18. Chen D.H. (1978) Qualitative and quantitative study ofsynaptic displace-ment in chromatolyzed spinal motoneurons of the cat. Journal of Comparative Neurology 177, 635-664.
19. Cova J.L. and Aldskogius H. (1986) Effect of axotomy on perineuronal glial cells in the hypoglossal and dorsal motor vagal nuclei of the cat. Experimental Neurology 93, 662-667.
20. de Bilbao F., Giannakopoulos P., Srinivasan A. and Dubois-Dauphin M. (2000) In vivo study of motoneuron death induced by nerve injury in mice deficient in the caspase 1/interleukin1 beta-converting enzyme. Neuroscience 98, 573-583.
21. Davalos D., Grutzendler J., Yang G., Kim J.V., Zuo Y., Jung S. et al. (2005) ATP mediates rapid microglial response to local brain injury in vivo. Nature Neuroscience 8, 752-758.
22. Emirandetti A., Graciele Zanon R., Sabha M. Jr. and de Oliveira A.L. (2006) Astrocyte reactivity influences the number ofpresynaptic terminals apposed to spinal motoneurons after axotomy. Brain Research 1095, 35-42.
23. Ferri C.C., Ghasemlou N., Bisby M.A. and Kawaja M.D. (2002) Nerve growth factor alters p75 neurotrophin receptor-induced effects in mouse facial motoneurons following axotomy. Brain Research 950, 180-185.
24. Gowing G., Vallières L. and Julien J.P. (2006) Mouse model for ablation ofproliferating microglia in acute CNS injuries. Glia 53, 331-337.
25. Graeber M.B., Tetzlaff W., Streit W.J. and Kreutzberg G.W. (1988) Microglial cells but not astrocytes undergo mitosis following rat facial nerve axotomy. Neuroscience Letters 85, 317-321.
26. Graeber M.B., Bise K. and Mehraein P. (1993) Synaptic stripping in the human facial nucleus. Acta Neuropathologica 86, 179-181.
27. Graeber M.B. and Streit W.J. (2010) Microglia: biology and pathology. Acta Neuropathologica 119, 89-105.
28. Greensmith L., Mentis G.Z. and Vrbová G. (1994) Blockade of N-methyl-D-aspartate receptors by MK-801 (dizocilpine maleate) rescues motoneurones in developing rats. Developmental Brain Research 81, 162-170.
29. Halassa M.M. and Haydon P.G. (2010) Integrated brain circuits: astrocy-tic networks modulate neuronal activity and behavior. Annual Review ofPhysiology 72, 335-355.
30. Haydon P.G. (2001) GLIA: listening and talking to the synapse. Nature Reviews Neuroscience 2, 185-193.
31. Horner P.J. and Palmer T.D. (2003) New roles for astrocytes: the night-life of an 'astrocyte'. La vida loca! Trends in Neurosciences 26, 597-603.
32. Hornung J.P., Koppel H. and Clarke P.G. (1989) Endocytosis and autop hagy in dying neurons: an ultrastructural study in chick embryos. Journal ofComparative Neurology 283, 425-437.
33. Hottinger A.F., Azzouz M., Déglon N., Aebischer P. and Zurn A.D. (2000) Complete and long-term rescue oflesioned adult motoneurons by lentiviral-mediated expression of glial cell line-derived neuro-trophic factor in the facial nucleus. Journal of Neuroscience 20, 5587-5593.
34. Huang Y.H. and Bergles D.E. (2004) Glutamate transporters bring com-petition to the synapse. Current Opinion in Neurobiology 14, 346-352.
35. Jarosinski K.W. and Massa P.T. (2002) Interferon regulatory factor-1 is required for interferon-gamma-induced MHC class I genes in astro-cytes. Journal of Neuroimmunology 122, 74-84.
36. Johnson I.P. and Duberley R.M. (1998) Motoneuron survival and expression of neuropeptides and neurotrophic factor receptors follow-ing axotomy in adult and ageing rats. Neuroscience 84, 141-150.
37. Kiryu-Seo S., Hirayama T., Kato R. and Kiyama H. (2005) Noxa is a critical mediator of p53dependent motor neuron death after nerve injury in adult mouse. Journal of Neuroscience 25, 1442-1447.
38. Kiryu-Seo S., Gamo K., Tachibana T., Tanaka K. and Kiyama H. (2006) Unique anti-apoptotic activity of EAAC1 in injured motor neurons. EMBO Journal 25, 3411-3421.
39. Kou S.Y., Chiu A.Y. and Patterson P.H. (1995) Differential regulation of motor neuron survival and choline acetyltransferase expression fol-lowing axotomy. Journal of Neurobiology 27, 561-572.
40. Koizumi S. and Inoue K. (1997) Inhibition by ATP of calcium oscil-lations in rat cultured hippocampal neurons. British Journal of Pharmacology 122, 51-58.
41. Koizumi S., Fujishita K., Tsuda M., Shigemoto-Mogami Y. and Inoue K. (2003). Dynamic inhibition ofexcitatory synaptic transmission by astrocyte-derived ATP in hippocampal cultures. Proceedings of the National Academy ofSciences of the U.S.A. 100, 11023-11028.
42. Kuno M. and Llinas R. (1970) Alterations ofsynaptic action in chroma-tolysed motoneurones of the cat. Journal ofPhysiology 210, 823-838.
43. Laiwand R., Werman R. and Yarom Y. (1987) Time course and distri bution of motoneuronal loss in the dorsal motor vagal nucleus of guinea pig after cervical vagotomy. Journal of Comparative Neurology 256, 527-537.
44. Laskawi R. and Wolff J.R. (1996) Changes in glial fibrillary acidic protein immunoreactivity in the rat facial nucleus following various types of nerve lesions. European Archives of Oto-Rhino-Laryngology 253, 475-480.
45. Latov N., Nilaver G., Zimmerman E.A., Johnson W.G., Silverman A.J., Defendini R. et al. (1979) Fibrillary astrocytes proliferate in response to brain injury: a study combining immunoperoxidase technique for glial fibrillary acidic protein and radioautography of tritiated thymi-dine. Developmental Biology 72, 381-384.
46. Lepore A.C., Rauck B., Dejea C., Pardo A.C., Rao M.S., Rothstein J.D. et al. (2008) Focal transplantation-based astrocyte replacement is neu-roprotective in a model of motor neuron disease. Nature Neuroscience 11, 1294-1301.
47. Lindå H., Hammarberg H., Cullheim S., Levinovitz A., Khademi M. and Olsson T. (1998) Expression of MHC class I and beta2-microglobulin in rat spinal motoneurons: regulatory influences by IFN-gamma and axotomy. Experimental Neurology 150, 282-295.
48. Lindå H., Shupliakov O., Ornung G., Ottersen O.P., Storm-Mathisen J., Risling M. et al. (2000) Ultrastructural evidence for a preferential elimination of glutamate-immunoreactive synaptic terminals from spinal motoneurons after intramedullary axotomy. Journal of Comparative Neurology 425, 10-23.
49. Lidman O., Olsson T. and Piehl F. (1999) Expression of nonclassical MHC class I (RT1-U) in certain neuronal populations of the central nervous system. European Journal of Neuroscience 11, 4468-4472.
50. Marchetti B. and Abbracchio M.P. (2005) To be or not to be (inflamed)-is that the question in anti-inflammatory drug therapy ofneurodegen-erative disorders? Trends in Pharmacological Sciences 26, 517-525.
51. Mart'in E.D., Fernández M., Perea G., Pascual O., Haydon P.G., Araque A. et al. (2007) Adenosine released by astrocytes contributes to hypoxia-induced modulation ofsynaptic transmission. Glia 55, 36-45.
52. Mattsson P., Meijer B. and Svensson M. (1999) Extensive neuronal cell death following intracranial transection of the facial nerve in the adult rat. Brain Research Bulletin 49, 333-341.
53. Mentis G.Z., Greensmith L. and Vrbova G. (1993) Motoneurons des tined to die are rescued by blocking N-methyl-D-aspartate receptors by MK-801. Neuroscience 54, 283-285.
54. Moran L.B. and Graeber M.B. (2004) The facial nerve axotomy model. Brain Research Reviews 44, 154-178.
55. Namikawa K., Honma M., Abe K., Takeda M., Mansur K., Obata T. et al. (2000) Akt/protein kinase B prevents injury-induced moto-neuron death and accelerates axonal regeneration. Journal of Neuroscience 20, 2875-2886.
56. Nimmerjahn A., Kirchhoff F. and Helmchen F. (2005) Resting micro-glial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308, 1314-1318.
57. Nissl F. (1894) Uber eine neue Untersuchungsmethode des Centralorgans speziell zur Feststellung der Lokalisation der Nervenzellen. Zentralbl Nervenheilkd Psychiatr 17, 337-344.
58. Oh C., Murray B., Bhattacharya N., Holland D. and Tatton W.G. (1994) (-)-Deprenyl alters the survival of adult murine facial motoneurons after axotomy: increases in vulnerable C57BL strain but decreases in motor neuron degeneration mutants. Journal of Neuroscience Research 38, 64-74.
59. Oliet S.H. and Poulain D.A. (1999) Adenosine-induced presynaptic inhi-bition of IPSCs and EPSCs in rat hypothalamic supraoptic nucleus neurones. Journal ofPhysiology 520, 815-825.
60. Oliveira A.L., Thams S., Lidman O., Piehl F., Hökfelt T., Kärre K. et al. (2004) A role for MHC class I molecules in synaptic plasticity and regeneration of neurons after axotomy. Proceedings of the National Academy ofSciences of the U.S.A. 101, 17843-17848.
61. Panatier A., Vallée J., Haber M., Murai K.K., Lacaille J.C. and Robitaille R. (2011) Astrocytes are endogenous regulators ofbasal transmission at central synapses. Cell 146, 785-798.
62. Pekny M. and Nilsson M. (2005) Astrocyte activation and reactive gliosis. Glia 50, 427-434.
63. Perea G., Navarrete M. and Araque A. (2009) Tripartite synapses: astro-cytes process and control synaptic information. Trends in Neurosciences 32, 421-431.
64. Petitto J.M., Huang Z., Lo J. and Streit W.J. (2003) IL 2 gene knockout affects T lymphocyte trafficking and the microglial response to regener-ating facial motor neurons. Journal of Neuroimmunology 134, 95-103.
65. Purves D. (1975) Functional and structural changes in mammalian sym-pathetic neurones following interruption of their axons. Journal of Physiology 252, 429-463.
66. Raivich G., Moreno-Flores M.T., Möller J.C. and Kreutzberg G.W. (1994) Inhibition of posttraumatic microglial proliferation in a genetic model of macrophage colony-stimulating factor deficiency in the mouse. European Journal of Neuroscience 6, 1615-1618.
67. Raivich G., Bohatschek M., Kloss C.U., Werner A., Jones L.L. and Kreutzberg G.W. (1999) Neuroglial activation repertoire in the injured brain: graded response, molecular mechanisms and cues to physiological function. Brain Research Reviews 30, 77-105.
68. Rall W. (1964) Theoretical significance of dendritic trees for neuronal input output relations. In Reiss R. (ed.) Neural Theory and Modeling. Stanford: Stanford University Press.
69. Reisert I., Wildemann G., Grab D. and Pilgrim C. (1984) The glial reac-tion in the course of axon regeneration: a stereological study of the rat hypoglossal nucleus. Journal ofComparative Neurology 229, 121-128.
70. Sabha M. Jr., Emirandetti A. Cullheim S. and De Oliveira A.L. (2008) MHC I expression and synaptic plasticity in different mice strains after axotomy. Synapse 62, 137-148.
71. Sánchez-Vives M.V. and Gallego R. (1993) Effects of axotomy or target atrophy on membrane properties of rat sympathetic ganglion cells. Journal ofPhysiology 471, 801-815.
72. Schelper R.L. and Adrian E.K. Jr. (1980) Non-specific esterase activity in reactive cells in injured nervous tissue labeled with 3H-thymidine or 125iododeoxyuridine injected before injury. Journal of Comparative Neurology 194, 829-844.
73. Schiefer J., Kampe K., Dodt H.U., Zieglgänsberger W. and Kreutzberg G.W. (1999) Microglial motility in the rat facial nucleus following per-ipheral axotomy. Journal of Neurocytology 28, 439-453.
74. Schwartz M., Butovsky O., Brück W. and Hanisch U.K. (2006) Microglial phenotype: is the commitment reversible? Trends in Neurosciences 29, 68-74.
75. Serpe C.J., Sanders V.M. and Jones K.J. (2000) Kinetics of facial moto-neuron loss following facial nerve transection in severe combined immunodeficient mice. Journal of Neuroscience Research 62, 273-278.
76. Sjöstrand J. (1965) Proliferative changes in glial cells during nerve regen-eration. Zeitschriftfür Zellforschung und Mikroskopische Anatomie 68, 481-493.
77. Sjöstrand J. (1971) Neuroglial proliferation in the hypoglossal nucleus after nerve injury. Experimental Neurology 30, 178-189.
78. Smith M.E., Gibbs M.A., Forno L.S. and Eng L.F. (1987) 3Hthymidine labeling of astrocytes in experimental allergic encephalomyelitis. Journal of Neuroimmunology 15, 309-321.
79. Snider W.D., Elliott J.L. and Yan Q. (1992) Axotomy-induced neuronal death during development. Journal of Neurobiology 23, 1231-1246.
80. Sofroniew M.V. (1999) Neuronal responses to axotomy. In Tuszynski M.H. & Kordower J. (eds) CNS Regeneration: Basic Science and Clinical Advances. New York: Academic Press.
81. Søreide A.J. (1981a) Variations in the axon reaction in animals ofdiffer-ent ages. A light microscopic study on the facial nucleus of the rat. Acta Anatomica (Basel) 110, 40-47.
82. Søreide A.J. (1981b) Variations in the perineuronal glial changes after different types of nerve lesion: light and electron microscopic investi-gations on the facial nucleus of the rat. Neuropathology and Applied Neurobiology 7, 195-204.
83. Sumner B.E. and Sutherland F.I. (1973) Quantitative electron microscopy on the injured hypoglossal nucleus in the rat. Journal of Neurocytology 2, 315-328.
84. Sumner B.E. (1979) Ultrastructural data, with special reference to bouton/glial relationships, from the hypoglossal nucleus after a second axotomy of the hypoglossal nerve. Experimental Brain Research 36, 107-118.
85. Svensson M. and Aldskogius H. (1993) Infusion ofcytosine-arabinoside into the cerebrospinal fluid of the rat brain inhibits the microglial cell proliferation after hypoglossal nerve injury. Glia 7, 286-298.
86. Svensson M., Mattsson P. and Aldskogius H. (1994) A bromodeoxyur idine labelling study of proliferating cells in the brainstem following hypoglossal nerve transection. Journal of Anatomy 185, 537-542.
87. Tetzlaff W., Graeber M.B., Bisby M.A. and Kreutzberg G.W. (1988) Increased glial fibrillary acidic protein synthesis in astrocytes during retrograde reaction of the rat facial nucleus. Glia 1, 90-95.
88. Torvik A. and Skjörten F. (1971a) Electron microscopic observations on nerve cell regeneration and degeneration after axon lesions. I. Changes in the nerve cell cytoplasm. Acta Neuropathologica 17, 248-264.
89. Torvik A. and Skjörten F. (1971b) Electron microscopic observations on nerve cell regeneration and degeneration after axon lesions. II. Changes in the glial cells. Acta Neuropathologica 17, 265-282.
90. Torvik A. and Søreide A.J. (1975) The perineuronal glial reaction after axotomy. Brain Research 95, 519-529.
91. Ulfhake B. and Cullheim S. (1988) Postnatal development of cat hind limb motoneurons. II: In vivo morphology of dendritic growth cones and the maturation of dendrite morphology. Journal of Comparative Neurology 278, 88-102.
92. van Rossum D. and Hanisch U.K. (2004) Microglia. Metabolic Brain Disease 19, 393-411.
93. Vilhardt F. (2005) Microglia: phagocyte and glia cell. International Journal ofBiochemistry and Cell Biology 37, 17-21.
94. Walz W. (1989) Role ofglial cells in the regulation of the brain ion micro-environment. Progress in Neurobiology 33, 309-333.
95. Watson W.E. (1972) Some quantitative observations upon the responses ofneuroglial cells which follow axotomy ofadjacent neurones. Journal ofPhysiology 225, 415-435.
96. Xin L., Richardson P.M., Gervais F. and Skamene E. (1990) A deficiency ofaxonal regeneration in C57BL/6J mice. Brain Research 510, 144-146.
97. Yamada J. and Jinno S. (2011) Alterations in neuronal survival and glial reactions after axotomy by ceftriaxone and minocycline in the mouse hypoglossal nucleus. Neuroscience Letters 504, 295-300.
98. Yamada J., Hayashi Y., Jinno S., Wu Z., Inoue K., Kohsaka S. et al. (2008) Reduced synaptic activity precedes synaptic stripping in vagal motoneurons after axotomy. Glia 56, 1448-1462.
99. Yamada J., Nakanishi H. and Jinno S. (2011) Differentialinvolvement of perineuronal astrocytes and microglia in synaptic stripping after hypo-glossal axotomy. Neuroscience 182, 1-10.
100. Yu W.H. (1988) Sex difference in neuronal loss induced by axotomy in the rat brain stem motor nuclei. Experimental Neurology 102, 230-235.
101. Zhang J.M., Wang H.K., Ye C.Q., Ge W., Chen Y., Jiang Z.l. et al. (2003) ATP released by astrocytes mediates glutamatergic activity-dependent heterosynaptic suppression. Neuron 40, 971-982.