Reduced removal of synaptic terminals from axotomized spinal motoneurons in the absence of complement C3

Experimental Neurology

Volumn 237, Issue 1, 2012, Pages 8-17

  Berg, Alexander ^a   Zelano, Johan ^a,b   Stephan, Alexander ^c   Thams, Sebastian ^a   Barres, Ben A ^c   Pekny, Milos ^d   Pekna, Marcela ^d   Cullheim, Staffan ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UPPSALA UNIVERSITY   (Sweden)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

Complement proteins; Motoneuron; Peripheral nerve lesion; Synaptic plasticity

Indexed keywords

BETA AMYLASE; CD68 ANTIGEN; COMPLEMENT COMPONENT C1; COMPLEMENT COMPONENT C3; GLIAL FIBRILLARY ACIDIC PROTEIN; NEUROMODULIN; SYNAPTOPHYSIN; VESICULAR INHIBITORY AMINO ACID TRANSPORTER;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CONTROLLED STUDY; ELECTRON MICROSCOPY; FEMALE; GRIP STRENGTH; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MOUSE; MUSCLE REINNERVATION; NERVE ENDING; NERVE FIBER TRANSECTION; NERVE INJURY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SCIATIC NERVE INJURY; SEQUENCE HOMOLOGY; SPINAL CORD MOTONEURON; SYNAPTOSOME; UPREGULATION;

ANIMALS; AXOTOMY; COMPLEMENT C1Q; COMPLEMENT C3; GENE EXPRESSION REGULATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOTOR NEURONS; NEURAL INHIBITION; PRESYNAPTIC TERMINALS; RECOVERY OF FUNCTION; SCIATIC NERVE; SYNAPSES;

EID: 84863686504     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2012.06.008     Document Type: Article

References (49)

1. Aldskogius H., Liu L., Svensson M. Glial responses to synaptic damage and plasticity. J. Neurosci. Res. 1999, 58:33-41.
2. Alvarez F.J., Titus-Mitchell H.E., Bullinger K.L., Kraszpulski M., Nardelli P., Cope T.C. Permanent central synaptic disconnection of proprioceptors after nerve injury and regeneration: I. Loss of VGLUT1/IA synapses on motoneurons. J. Neurophysiol. 2011, 106:2450-2470.
3. Barron K. Comparative observations on the cytologic reactions of central and peripheral nerve cells to axotomy. Spinal Cord Reconstruction 1983, 7-39. Raven Press, New York. C.C. Kao, R.P. Bunge, P.J. Reier (Eds.).
4. Blinzinger K., Kreutzberg G. Displacement of synaptic terminals from regenerating motoneurons by microglial cells. Z. Zellforsch. Mikrosk. Anat. 1968, 85:145-157.
5. Botto M., Dell'Agnola C., Bygrave A.E., Thompson E.M., Cook H.T., Petry F., Loos M., Pandolfi P.P., Walport M.J. Homozygous C1q deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nat. Genet. 1998, 19:56-59.
6. Bruck W., Friede R.L. Anti-macrophage CR3 antibody blocks myelin phagocytosis by macrophages in vitro. Acta Neuropathol. 1990, 80:415-418.
7. Carlstedt T., Cullheim S. Spinal cord motoneuron maintenance, injury and repair. Prog. Brain Res. 2000, 127:501-514.
8. Chen D.H. Qualitative and quantitative study of synaptic displacement in chromatolyzed spinal motoneurons of the cat. J. Comp. Neurol. 1978, 177:635-664.
9. Chu Y., Jin X., Parada I., Pesic A., Stevens B., Barres B., Prince D.A. Enhanced synaptic connectivity and epilepsy in C1q knockout mice. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:7975-7980.
10. Conradi S. Ultrastructure and distribution of neuronal and glial elements on the motoneuron surface in the lumbosacral spinal cord of the adult cat. Acta Physiol. Scand. Suppl. 1969, 332:5-48.
11. Cope T.C., Bonasera S.J., Nichols T.R. Reinnervated muscles fail to produce stretch reflexes. J. Neurophysiol. 1994, 71:817-820.
12. Cullheim S., Kellerth J.O., Conradi S. Evidence for direct synaptic interconnections between cat spinal alpha-motoneurons via the recurrent axon collaterals: a morphological study using intracellular injection of horseradish peroxidase. Brain Res. 1977, 132:1-10.
13. Dagerlind A., Friberg K., Bean A.J., Hökfelt T. Sensitive mRNA detection using unfixed tissue: combined radioactive and non-radioactive in situ hybridization histochemistry. Histochemistry 1992, 98:39-49.
14. Dailey A.T., Avellino A.M., Benthem L., Silver J., Kliot M. Complement depletion reduces macrophage infiltration and activation during Wallerian degeneration and axonal regeneration. J. Neurosci. 1998, 18:6713-6722.
15. Davis-Lopez de Carrizosa M.A., Morado-Diaz C.J., Tena J.J., Benitez-Temino B., Pecero M.L., Morcuende S.R., de la Cruz R.R., Pastor A.M. Complementary actions of BDNF and neurotrophin-3 on the firing patterns and synaptic composition of motoneurons. J. Neurosci. 2009, 29:575-587.
16. Fan R., DeFilippis K., Van Nostrand W.E. Induction of complement proteins in a mouse model for cerebral microvascular A beta deposition. J. Neuroinflammation 2007, 4:22.
17. Freria C.M., Zanon R.G., Santos L.M., Oliveira A.L. Major histocompatibility complex class I expression and glial reaction influence spinal motoneuron synaptic plasticity during the course of experimental autoimmune encephalomyelitis. J. Comp. Neurol. 2010, 518:990-1007.
18. Gasque P. Complement: a unique innate immune sensor for danger signals. Mol. Immunol. 2004, 41:1089-1098.
19. Grant G., Arvidsson J. Transganglionic degeneration in trigeminal primary sensory neurons. Brain Res. 1975, 95:265-279.
20. Ip W.K., Takahashi K., Ezekowitz R.A., Stuart L.M. Mannose-binding lectin and innate immunity. Immunol. Rev. 2009, 230:9-21.
21. Karns L.R., Ng S.C., Freeman J.A., Fishman M.C. Cloning of complementary DNA for GAP-43, a neuronal growth-related protein. Science 1987, 236:597-600.
22. Lagerbäck P.A., Ronnevi L.O., Cullheim S., Kellerth J.O. An ultrastructural study of the synaptic contacts of alpha-motoneuron axon collaterals. I. Contacts in lamina IX and with identified alpha-motoneurone dendrites in lamina VII. Brain Res. 1981, 207:247-266.
23. Lindå H., Piehl F., Dagerlind A., Verge V.M., Arvidsson U., Cullheim S., Risling M., Ulfhake B., Hökfelt T. Expression of GAP-43 mRNA in the adult mammalian spinal cord under normal conditions and after different types of lesions, with special reference to motoneurons. Exp. Brain Res. 1992, 91:284-295.
24. Lindå H., Shupliakov O., Örnung G., Ottersen O.P., Storm-Mathisen J., Risling M., Cullheim S. Ultrastructural evidence for a preferential elimination of glutamate-immunoreactive synaptic terminals from spinal motoneurons after intramedullary axotomy. J. Comp. Neurol. 2000, 425:10-23.
25. Mattsson P., Morgan B.P., Svensson M. Complement activation and CD59 expression in the motor facial nucleus following intracranial transection of the facial nerve in the adult rat. J. Neuroimmunol. 1998, 91:180-189.
26. Medzhitov R., Janeway C. Innate immune recognition: mechanisms and pathways. Immunol. Rev. 2000, 173:89-97.
27. Morgan B.P., Gasque P. Expression of complement in the brain: role in health and disease. Immunol. Today 1996, 17:461-466.
28. Novikov L.N., Novikova L.N., Holmberg P., Kellerth J. Exogenous brain-derived neurotrophic factor regulates the synaptic composition of axonally lesioned and normal adult rat motoneurons. Neuroscience 2000, 100:171-181.
29. Ohlsson M., Bellander B.M., Langmoen I.A., Svensson M. Complement activation following optic nerve crush in the adult rat. J. Neurotrauma 2003, 20:895-904.
30. Oliveira A.L., Hydling F., Olsson E., Shi T., Edwards R.H., Fujiyama F., Kaneko T., Hokfelt T., Cullheim S., Meister B. Cellular localization of three vesicular glutamate transporter mRNAs and proteins in rat spinal cord and dorsal root ganglia. Synapse 2003, 50:117-129.
31. Oliveira A.L., Thams S., Lidman O., Piehl F., Hökfelt T., Karre K., Lindå H., Cullheim S. A role for MHC class I molecules in synaptic plasticity and regeneration of neurons after axotomy. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:17843-17848.
32. Örnung G., Shupliakov O., Lindå H., Ottersen O.P., Storm-Mathisen J., Ulfhake B., Cullheim S. Qualitative and quantitative analysis of glycine- and GABA-immunoreactive nerve terminals on motoneuron cell bodies in the cat spinal cord: a postembedding electron microscopic study. J. Comp. Neurol. 1996, 365:413-426.
33. Örnung G., Ottersen O.P., Cullheim S., Ulfhake B. Distribution of glutamate-, glycine- and GABA-immunoreactive nerve terminals on dendrites in the cat spinal motor nucleus. Exp. Brain Res. 1998, 118:517-532.
34. Pekna M., Hietala M.A., Rosklint T., Betsholtz C., Pekny M. Targeted disruption of the murine gene coding for the third complement component (C3). Scand. J. Immunol. 1998, 47:25-29.
35. Perry V.H., O'Connor V. The role of microglia in synaptic stripping and synaptic degeneration: a revised perspective. ASN Neuro 2010, 2:e00047.
36. Piehl F., Ji R.R., Cullheim S., Hökfelt T., Lindholm D., Hughes R.A. Fibroblast growth factors regulate calcitonin gene-related peptide mRNA expression in rat motoneurons after lesion and in culture. Eur. J. Neurosci. 1995, 7:1739-1750.
37. Ragnarson B., Örnung G., Ottersen O.P., Grant G., Ulfhake B. Ultrastructural detection of neuronally transported choleragenoid by postembedding immunocytochemistry in freeze-substituted Lowicryl HM20 embedded tissue. J. Neurosci. Methods 1998, 80:129-136.
38. Rahpeymai Y., Hietala M.A., Wilhelmsson U., Fotheringham A., Davies I., Nilsson A.K., Zwirner J., Wetsel R.A., Gerard C., Pekny M., Pekna M. Complement: a novel factor in basal and ischemia-induced neurogenesis. EMBO J. 2006, 25:1364-1374.
39. Ramaglia V., Daha M.R., Baas F. The complement system in the peripheral nerve: friend or foe?. Mol. Immunol. 2008, 45:3865-3877.
40. Selkoe D.J. Alzheimer's disease is a synaptic failure. Science 2002, 298:789-791.
41. Shinjyo N., Stahlberg A., Dragunow M., Pekny M., Pekna M. Complement-derived anaphylatoxin C3a regulates in vitro differentiation and migration of neural progenitor cells. Stem Cells 2009, 27:2824-2832.
42. Stevens B., Allen N.J., Vazquez L.E., Howell G.R., Christopherson K.S., Nouri N., Micheva K.D., Mehalow A.K., Huberman A.D., Stafford B., Sher A., Litke A.M., Lambris J.D., Smith S.J., John S.W., Barres B.A. The classical complement cascade mediates CNS synapse elimination. Cell 2007, 131:1164-1178.
43. Sumner B.E. A quantitative analysis of boutons with different types of synapse in normal and injured hypoglossal nuclei. Exp. Neurol. 1975, 49:406-417.
44. Svensson M., Aldskogius H. Synaptic density of axotomized hypoglossal motoneurons following pharmacological blockade of the microglial cell proliferation. Exp. Neurol. 1993, 120:123-131.
45. Svensson M., Eriksson P., Persson J.K., Molander C., Arvidsson J., Aldskogius H. The response of central glia to peripheral nerve injury. Brain Res. Bull. 1993, 30:499-506.
46. Ulfhake B., Arvidsson U., Cullheim S., Hokfelt T., Brodin E., Verhofstad A., Visser T. An ultrastructural study of 5-hydroxytryptamine-, thyrotropin-releasing hormone- and substance P-immunoreactive axonal boutons in the motor nucleus of spinal cord segments L7-S1 in the adult cat. Neuroscience 1987, 23:917-929.
47. Zang da W., Lopes E.C., Cheema S.S. Loss of synaptophysin-positive boutons on lumbar motor neurons innervating the medial gastrocnemius muscle of the SOD1G93A G1H transgenic mouse model of ALS. J. Neurosci. Res. 2005, 79:694-699.
48. Zelano J., Berg A., Thams S., Hailer N.P., Cullheim S. SynCAM1 expression correlates with restoration of central synapses on spinal motoneurons after two different models of peripheral nerve injury. J. Comp. Neurol. 2009, 517:670-682.
49. Zhou J., Fonseca M.I., Pisalyaput K., Tenner A.J. Complement C3 and C4 expression in C1q sufficient and deficient mouse models of Alzheimer's disease. J. Neurochem. 2008, 106:2080-2092.