The Classical Complement Cascade Mediates CNS Synapse Elimination

Cell

Volumn 131, Issue 6, 2007, Pages 1164-1178

  Stevens, Beth ^a   Allen, Nicola J ^a   Vazquez, Luis E ^a   Howell, Gareth R ^b,c   Christopherson, Karen S ^a   Nouri, Navid ^a   Micheva, Kristina D ^a   Mehalow, Adrienne K ^b,c   Huberman, Andrew D ^a   Stafford, Benjamin ^d   Sher, Alexander ^d   Litke, Alan M ^d   Lambris, John D ^e   Smith, Stephen J ^a   John, Simon W M ^b,c   Barres, Ben A ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c JACKSON LABORATORY   (United States)

^d UNIVERSITY OF CALIFORNIA SANTA CRUZ   (United States)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

CELLIMMUNO; HUMDISEASE; MOLNEURO

Indexed keywords

COMPLEMENT COMPONENT C1Q; COMPLEMENT COMPONENT C3;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DOWN REGULATION; GLAUCOMA; IMMUNOREACTIVITY; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RETINA GANGLION CELL; SYNAPTIC MEMBRANE; UPREGULATION;

MUS;

EID: 36849076770     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2007.10.036     Document Type: Article

References (47)

1. Barnum S.R. Complement in central nervous system inflammation. Immunol. Res. 26 (2002) 7-13
2. Bishop D.L., Misgeld T., Walsh M.K., Gan W.B., and Lichtman J.W. Axon branch removal at developing synapses by axosome shedding. Neuron 44 (2004) 651-661
3. Bjartmar L., Huberman A.D., Ullian E.M., Renteria R.C., Liu X., Xu W., Prezioso J., Susman M.W., Stellwagen D., Stokes C.C., et al. Neuronal pentraxins mediate synaptic refinement in the developing visual system. J. Neurosci. 26 (2006) 6269-6281
4. Botto M., Dell'Agnola C., Bygrave A.E., Thompson E.M., Cook H.T., Petry F., Loos M., Pandolfi P.P., and Walport M.J. Homozygous C1q deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nat. Genet. 19 (1998) 56-59
5. Boulanger L.M., and Shatz C.J. Immune signalling in neural development, synaptic plasticity and disease. Nat. Rev. Neurosci. 5 (2004) 521-531
6. Christopherson K.S., Ullian E.M., Stokes C.C., Mullowney C.E., Hell J.W., Agah A., Lawler J., Mosher D.F., Bornstein P., and Barres B.A. Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis. Cell 120 (2005) 421-433
7. Cowell R.M., Plane J.M., and Silverstein F.S. Complement activation contributes to hypoxic-ischemic brain injury in neonatal rats. J. Neurosci. 23 (2003) 9459-9468
8. Dalmau I., Finsen B., Zimmer J., Gonzalez B., and Castellano B. Development of microglia in the postnatal rat hippocampus. Hippocampus 8 (1998) 458-474
9. Dangond F., Hwang D., Camelo S., Pasinelli P., Frosch M.P., Stephanopoulos G., Stephanopoulos G., Brown Jr. R.H., and Gullans S.R. Molecular signature of late-stage human ALS revealed by expression profiling of postmortem spinal cord gray matter. Physiol. Genomics 16 (2004) 229-239
10. Fiske B.K., and Brunjes P.C. Microglial activation in the developing rat olfactory bulb. Neuroscience 96 (2000) 807-815
11. Fonseca M.I., Kawas C.H., Troncoso J.C., and Tenner A.J. Neuronal localization of C1q in preclinical Alzheimer's disease. Neurobiol. Dis. 15 (2004) 40-46
12. Gasque P. Complement: a unique innate immune sensor for danger signals. Mol. Immunol. 41 (2004) 1089-1098
13. Gasque P., Singhrao S.K., Neal J.W., Wang P., Sayah S., Fontaine M., and Morgan B.P. The receptor for complement anaphylatoxin C3a is expressed by myeloid cells and nonmyeloid cells in inflamed human central nervous system: analysis in multiple sclerosis and bacterial meningitis. J. Immunol. 160 (1998) 3543-3554
14. Hirai H., Pang Z., Bao D., Miyazaki T., Li L., Miura E., Parris J., Rong Y., Watanabe M., Yuzaki M., and Morgan J.I. Cbln1 is essential for synaptic integrity and plasticity in the cerebellum. Nat. Neurosci. 8 (2005) 1534-1541
15. Hooks B.M., and Chen C. Distinct roles for spontaneous and visual activity in remodeling of the retinogeniculate synapse. Neuron 52 (2006) 281-291
16. Howell G.R., Libby R.T., Marchant J.K., Wilson L.A., Cosma I.M., Smith R.S., Anderson M.G., and John S.W. Absence of glaucoma in DBA/2J mice homozygous for wild-type versions of Gpnmb and Tyrp1. BMC Genet. 8 (2007) 45
17. Hua J.Y., and Smith S.J. Neural activity and the dynamics of central nervous system development. Nat. Neurosci. 7 (2004) 327-332
18. Huberman A.D. Mechanisms of eye-specific visual circuit development. Curr. Opin. Neurobiol. 17 (2007) 73-80
19. Huh G.S., Boulanger L.M., Du H., Riquelme P.A., Brotz T.M., and Shatz C.J. Functional requirement for class I MHC in CNS development and plasticity. Science 290 (2000) 2155-2159
20. Jaubert-Miazza L., Green E., Lo F.S., Bui K., Mills J., and Guido W. Structural and functional composition of the developing retinogeniculate pathway in the mouse. Vis. Neurosci. 22 (2005) 661-676
21. Jennings C. Developmental neurobiology. Death of a synapse. Nature 372 (1994) 498-499
22. John S.W., Anderson M.G., and Smith R.S. Mouse genetics: a tool to help unlock the mechanisms of glaucoma. J. Glaucoma 8 (1999) 400-412
23. Johnson S.A., Pasinetti G.M., and Finch C.E. Expression of complement C1qB and C4 mRNAs during rat brain development. Brain Res. Dev. Brain Res. 80 (1994) 163-174
24. Katz L.C., and Shatz C.J. Synaptic activity and the construction of cortical circuits. Science 274 (1996) 1133-1138
25. Libby R.T., Anderson M.G., Pang I.H., Robinson Z.H., Savinova O.V., Cosma I.M., Snow A., Wilson L.A., Smith R.S., Clark A.F., and John S.W. Inherited glaucoma in DBA/2J mice: pertinent disease features for studying the neurodegeneration. Vis. Neurosci. 22 (2005) 637-648
26. Maslinska D., Laure-Kamionowska M., and Kaliszek A. Morphological forms and localization of microglial cells in the developing human cerebellum. Folia Neuropathol. 36 (1998) 145-151
27. Mastellos D., and Lambris J.D. Complement: more than a 'guard' against invading pathogens?. Trends Immunol. 23 (2002) 485-491
28. Meyer-Franke A., Kaplan M., Pfrieger F., and Barres B. Characterization of the signaling interactions that promote the survival and growthof developing retinal ganglion cells in culture. Neuron 15 (1995) 805-819
29. Micheva K.D., and Smith S.J. Array tomography: a new tool for imaging the molecular architecture and ultrastructure of neural circuits. Neuron 55 (2007) 25-36
30. Mitchell D.A., Kirby L., Paulin S.M., Villiers C.L., and Sim R.B. Prion protein activates and fixes complement directly via the classical pathway: implications for the mechanism of scrapie agent propagation in lymphoid tissue. Mol. Immunol. 44 (2007) 2997-3004
31. Morgan B.P., and Gasque P. Expression of complement in the brain: role in health and disease. Immunol. Today 17 (1996) 461-466
32. Muller C.M., and Best J. Ocular dominance plasticity in adult cat visual cortex after transplantation of cultured astrocytes. Nature 342 (1989) 427-430
33. Nauta A.J., Bottazzi B., Mantovani A., Salvatori G., Kishore U., Schwaeble W.J., Gingras A.R., Tzima S., Vivanco F., Egido J., et al. Biochemical and functional characterization of the interaction between pentraxin 3 and C1q. Eur. J. Immunol. 33 (2003) 465-473
34. Nilsson L.G., Sikstrom C., Adolfsson R., Erngrund K., Nylander P.O., and Beckman L. Genetic markers associated with high versus low performance on episodic memory tasks. Behav. Genet. 26 (1996) 555-562
35. Prasad S.S., and Cynader M.S. Identification of cDNA clones expressed selectively during the critical period for visual cortex development by subtractive hybridization. Brain Res. 639 (1994) 73-84
36. Ritch R., Shields M.B., and Krupin T. The Glaucomas: Clinical Science. Second Edition (1996), Mosby-Year Book, St Louis, MO
37. Sahu A., and Lambris J.D. Complement inhibitors: a resurgent concept in anti-inflammatory therapeutics. Immunopharmacology 49 (2000) 133-148
38. Sanes J.R., and Lichtman J.W. Development of the vertebrate neuromuscular junction. Annu. Rev. Neurosci. 22 (1999) 389-442
39. Schaeren-Wiemers N., and Gerfin-Moser A. A single protocol to detect transcripts of various types and expression levels in neural tissue and cultured cells: in situ hybridization using digoxigenin-labelled cRNA probes. Histochemistry 100 (1993) 431-440
40. Schiefer J., Kampe K., Dodt H.U., Zieglgansberger W., and Kreutzberg G.W. Microglial motility in the rat facial nucleus following peripheral axotomy. J. Neurocytol. 28 (1999) 439-453
41. Selkoe D.J. Alzheimer's disease is a synaptic failure. Science 298 (2002) 789-791
42. Singhrao S.K., Neal J.W., Rushmere N.K., Morgan B.P., and Gasque P. Spontaneous classical pathway activation and deficiency of membrane regulators render human neurons susceptible to complement lysis. Am. J. Pathol. 157 (2000) 905-918
43. Stasi K., Nagel D., Yang X., Wang R.F., Ren L., Podos S.M., Mittag T., and Danias J. Complement component 1Q (C1Q) upregulation in retina of murine, primate, and human glaucomatous eyes. Invest. Ophthalmol. Vis. Sci. 47 (2006) 1024-1029
44. Steele M.R., Inman D.M., Calkins D.J., Horner P.J., and Vetter M.L. Microarray analysis of retinal gene expression in the DBA/2J model of glaucoma. Invest. Ophthalmol. Vis. Sci. 47 (2006) 977-985
45. Torborg C.L., and Feller M.B. Unbiased analysis of bulk axonal segregation patterns. J. Neurosci. Methods 135 (2004) 17-26
46. Ullian E.M., Sapperstein S.K., Christopherson K.S., and Barres B.A. Control of synapse number by glia. Science 291 (2001) 657-661
47. Wang J.T., Kunzevitzky N.J., Dugas J.C., Cameron M., Barres B.A., and Goldberg J.L. Disease gene candidates revealed by expression profiling of retinal ganglion cell development. J. Neurosci. 27 (2007) 8593-8603