From development to dysfunction: Microglia and the complement cascade in CNS homeostasis

Ageing Research Reviews

Volumn 12, Issue 3, 2013, Pages 749-756

  Zabel, Matthew K ^a   Kirsch, Wolff M ^a  

^a LOMA LINDA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

C1q; C3; CD11b; CR1; CR3; CX3CR1; Fractalkine; Phagocytosis

Indexed keywords

CD11B ANTIGEN; CHEMOKINE RECEPTOR CX3CR1; COMPLEMENT; COMPLEMENT COMPONENT C1Q; COMPLEMENT COMPONENT C3B; COMPLEMENT COMPONENT C3B RECEPTOR; FRACTALKINE; OPSONIN;

ALZHEIMER DISEASE; BRAIN DEVELOPMENT; BRAIN DYSFUNCTION; BRAIN FUNCTION; CELL FUNCTION; CELL INTERACTION; CELL STRUCTURE; CENTRAL NERVOUS SYSTEM; HOMEOSTASIS; HUMAN; INNATE IMMUNITY; MICROGLIA; NEUROPROTECTION; NONHUMAN; PATHOGENESIS; PROTEIN INTERACTION; REVIEW; SYNAPSE; SYNAPTOGENESIS;

C1Q; C3; CD11B; CR1; CR3; CX3CR1; FRACTALKINE; PHAGOCYTOSIS;

ALZHEIMER DISEASE; ANIMALS; BRAIN; COMPLEMENT SYSTEM PROTEINS; HUMANS; IMMUNITY, INNATE; MICROGLIA; SYNAPSES;

EID: 84881551407     PISSN: 15681637     EISSN: 18729649     Source Type: Journal    
DOI: 10.1016/j.arr.2013.02.001     Document Type: Review

References (71)

1. Aarum J., Sandberg K., Haeberlein S.L., Persson M.A. Migration and differentiation of neural precursor cells can be directed by microglia. Proceedings of the National Academy of Sciences of the United States of America 2003, 100:15983-15988.
2. Afagh A., Cummings B.J., Cribbs D.H., Cotman C.W., Tenner A.J. Localization and cell association of C1q in Alzheimer's disease brain. Experimental Neurology 1996, 138:22-32.
3. Bachstetter A.D., Morganti J.M., Jernberg J., Schlunk A., Mitchell S.H., Brewster K.W., Hudson C.E., Cole M.J., Harrison J.K., Bickford P.C., Gemma C. Fractalkine and CX 3 CR1 regulate hippocampal neurogenesis in adult and aged rats. Neurobiology of Aging 2011, 32:2030-2044.
4. Balice-Gordon R.J., Lichtman J.W. Long-term synapse loss induced by focal blockade of postsynaptic receptors. Nature 1994, 372:519-524.
5. Bamberger M.E., Harris M.E., McDonald D.R., Husemann J., Landreth G.E. A cell surface receptor complex for fibrillar beta-amyloid mediates microglial activation. Journal of Neuroscience 2003, 23:2665-2674.
6. Bazan J.F., Bacon K.B., Hardiman G., Wang W., Soo K., Rossi D., Greaves D.R., Zlotnik A., Schall T.J. A new class of membrane-bound chemokine with a CX3C motif. Nature 1997, 385:640-644.
7. Bhaskar K., Konerth M., Kokiko-Cochran O.N., Cardona A., Ransohoff R.M., Lamb B.T. Regulation of tau pathology by the microglial fractalkine receptor. Neuron 2010, 68:19-31.
8. Biffi A., Shulman J.M., Jagiella J.M., Cortellini L., Ayres A.M., Schwab K., Brown D.L., Silliman S.L., Selim M., Worrall B.B., Meschia J.F., Slowik A., De Jager P.L., Greenberg S.M., Schneider J.A., Bennett D.A., Rosand J. Genetic variation at CR1 increases risk of cerebral amyloid angiopathy. Neurology 2012, 78:334-341.
9. Blinzinger K., Kreutzberg G. Displacement of synaptic terminals from regenerating motoneurons by microglial cells. Zeitschrift fur Zellforschung und Mikroskopische Anatomie 1968, 85:145-157.
10. Boulanger L.M. Immune proteins in brain development and synaptic plasticity. Neuron 2009, 64:93-109.
11. Boulanger L.M., Shatz C.J. Immune signalling in neural development, synaptic plasticity and disease. Nature Reviews Neuroscience 2004, 5:521-531.
12. Cardona A.E., Pioro E.P., Sasse M.E., Kostenko V., Cardona S.M., Dijkstra I.M., Huang D., Kidd G., Dombrowski S., Dutta R., Lee J.C., Cook D.N., Jung S., Lira S.A., Littman D.R., Ransohoff R.M. Control of microglial neurotoxicity by the fractalkine receptor. Nature Neuroscience 2006, 9:917-924.
13. Castello M., Soriano S. Rational heterodoxy: cholesterol reformation of the amyloid doctrine. Ageing Research Reviews 2012, 23:282-288.
14. Cho S.H., Sun B., Zhou Y., Kauppinen T.M., Halabisky B., Wes P., Ransohoff R.M., Gan L. CX3CR1 modulates microglial activation and protects against plaque-independent cognitive deficits in a mouse model of Alzheimer's disease. Journal of Biological Chemistry 2011.
15. Chu Y., Jin X., Parada I., Pesic A., Stevens B., Barres B., Prince D.A. Enhanced synaptic connectivity and epilepsy in C1q knockout mice. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:7975-7980.
16. Eikelenboom P., Stam F.C. Immunoglobulins and complement factors in senile plaques. An immunoperoxidase study. Acta Neuropathologica 1982, 57:239-242.
17. Farber K., Cheung G., Mitchell D., Wallis R., Weihe E., Schwaeble W., Kettenmann H. C1q, the recognition subcomponent of the classical pathway of complement, drives microglial activation. Journal of Neuroscience Research 2009, 87:644-652.
18. Fonseca M.I., Kawas C.H., Troncoso J.C., Tenner A.J. Neuronal localization of C1q in preclinical Alzheimer's disease. Neurobiology of Disease 2004, 15:40-46.
19. Fonseca M.I., Zhou J., Botto M., Tenner A.J. Absence of C1q leads to less neuropathology in transgenic mouse models of Alzheimer's disease. Journal of Neuroscience 2004, 24:6457-6465.
20. Fraser D.A., Pisalyaput K., Tenner A.J. C1q enhances microglial clearance of apoptotic neurons and neuronal blebs, and modulates subsequent inflammatory cytokine production. Journal of Neurochemistry 2010, 112:733-743.
21. Galea I., Bechmann I., Perry V.H. What is immune privilege (not)?. Trends in Immunology 2007, 28:12-18.
22. Gemma C., Bachstetter A.D., Bickford P.C. Neuron-microglia dialogue and hippocampal neurogenesis in the aged brain. Aging & Disease 2010, 1:232-244.
23. Giulian D., Baker T.J. Characterization of ameboid microglia isolated from developing mammalian brain. Journal of Neuroscience 1986, 6:2163-2178.
24. Harrison J.K., Jiang Y., Chen S., Xia Y., Maciejewski D., McNamara R.K., Streit W.J., Salafranca M.N., Adhikari S., Thompson D.A., Botti P., Bacon K.B., Feng L. Role for neuronally derived fractalkine in mediating interactions between neurons and CX3CR1-expressing microglia. Proceedings of the National Academy of Sciences of the United States of America 1998, 95:10896-10901.
25. Kerschensteiner D., Morgan J.L., Parker E.D., Lewis R.M., Wong R.O. Neurotransmission selectively regulates synapse formation in parallel circuits in vivo. Nature 2009, 460:1016-1020.
26. Koenigsknecht J., Landreth G. Microglial phagocytosis of fibrillar beta-amyloid through a beta1 integrin-dependent mechanism. Journal of Neuroscience 2004, 24:9838-9846.
27. Koenigsknecht-Talboo J., Landreth G.E. Microglial phagocytosis induced by fibrillar beta-amyloid and IgGs are differentially regulated by proinflammatory cytokines. Journal of Neuroscience 2005, 25:8240-8249.
28. Koizumi S., Shigemoto-Mogami Y., Nasu-Tada K., Shinozaki Y., Ohsawa K., Tsuda M., Joshi B.V., Jacobson K.A., Kohsaka S., Inoue K. UDP acting at P2Y6 receptors is a mediator of microglial phagocytosis. Nature 2007, 446:1091-1095.
29. Kreutzberg G.W. Microglia: a sensor for pathological events in the CNS. Trends in Neurosciences 1996, 19:312-318.
30. Labrada L., Liang X.H., Zheng W., Johnston C., Levine B. Age-dependent resistance to lethal alphavirus encephalitis in mice: analysis of gene expression in the central nervous system and identification of a novel interferon-inducible protective gene, mouse ISG12. Journal of virology 2002, 76:11688-11703.
31. Lawson L.J., Perry V.H., Dri P., Gordon S. Heterogeneity in the distribution and morphology of microglia in the normal adult mouse brain. Neuroscience 1990, 39:151-170.
32. Liu Z., Condello C., Schain A., Harb R., Grutzendler J. CX3CR1 in microglia regulates brain amyloid deposition through selective protofibrillar amyloid-beta phagocytosis. Journal of Neuroscience 2010, 30:17091-17101.
33. Loeffler D.A., Camp D.M., Bennett D.A. Plaque complement activation and cognitive loss in Alzheimer's disease. Journal of Neuroinflammation 2008, 5:9.
34. Maffei A., Nataraj K., Nelson S.B., Turrigiano G.G. Potentiation of cortical inhibition by visual deprivation. Nature 2006, 443:81-84.
35. Maier M., Peng Y., Jiang L., Seabrook T.J., Carroll M.C., Lemere C.A. Complement C3 deficiency leads to accelerated amyloid beta plaque deposition and neurodegeneration and modulation of the microglia/macrophage phenotype in amyloid precursor protein transgenic mice. Journal of Neuroscience 2008, 28:6333-6341.
36. Mandrekar S., Jiang Q., Lee C.Y., Koenigsknecht-Talboo J., Holtzman D.M., Landreth G.E. Microglia mediate the clearance of soluble Abeta through fluid phase macropinocytosis. Journal of Neuroscience 2009, 29:4252-4262.
37. Marin-Teva J.L., Dusart I., Colin C., Gervais A., van Rooijen N., Mallat M. Microglia promote the death of developing Purkinje cells. Neuron 2004, 41:535-547.
38. Milligan C.E., Cunningham T.J., Levitt P. Differential immunochemical markers reveal the normal distribution of brain macrophages and microglia in the developing rat brain. The Journal of comparative neurology 1991, 314:125-135.
39. Mittelbronn M., Dietz K., Schluesener H.J., Meyermann R. Local distribution of microglia in the normal adult human central nervous system differs by up to one order of magnitude. Acta Neuropathologica 2001, 101:249-255.
40. Morioka T., Kalehua A.N., Streit W.J. The microglial reaction in the rat dorsal hippocampus following transient forebrain ischemia. Journal of Cerebral Blood Flow and Metabolism 1991, 11:966-973.
41. Napoli I., Neumann H. Microglial clearance function in health and disease. Neuroscience 2009, 158:1030-1038.
42. Neumann H., Kotter M.R., Franklin R.J. Debris clearance by microglia: an essential link between degeneration and regeneration. Brain 2009, 132:288-295.
43. Nimmerjahn A., Kirchhoff F., Helmchen F. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 2005, 308:1314-1318.
44. Nishida N., Walz T., Springer T.A. Structural transitions of complement component C3 and its activation products. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:19737-19742.
45. Norden, D.M., Godbout, J.P. Microglia of the aged brain: primed to be activated and resistant to regulation. Neuropathology & Applied Neurobiology [Epub ahead of print],, in press. doi:10.1111/j.1365-2990.2012.01306.x.
46. Ohsawa K., Irino Y., Nakamura Y., Akazawa C., Inoue K., Kohsaka S. Involvement of P2X4 and P2Y12 receptors in ATP-induced microglial chemotaxis. Glia 2007, 55:604-616.
47. Paolicelli R.C., Bolasco G., Pagani F., Maggi L., Scianni M., Panzanelli P., Giustetto M., Ferreira T.A., Guiducci E., Dumas L., Ragozzino D., Gross C.T. Synaptic pruning by microglia is necessary for normal brain development. Science 2011, 333:1456-1458.
48. Perry V.H., O'Connor V. C1q: the perfect complement for a synaptic feast?. Nature Reviews Neuroscience 2008, 9:807-811.
49. Pocock J.M., Kettenmann H. Neurotransmitter receptors on microglia. Trends in Neurosciences 2007, 30:527-535.
50. Ramaglia V., Hughes T.R., Donev R.M., Ruseva M.M., Wu X., Huitinga I., Baas F., Neal J.W., Morgan B.P. C3-dependent mechanism of microglial priming relevant to multiple sclerosis. Proceedings of the National Academy of Sciences of the United States of America 2012.
51. Schafer D.P., Lehrman E.K., Kautzman A.G., Koyama R., Mardinly A.R., Yamasaki R., Ransohoff R.M., Greenberg M.E., Barres B.A., Stevens B. Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron 2012, 74:691-705.
52. Schiefer J., Kampe K., Dodt H.U., Zieglgansberger W., Kreutzberg G.W. Microglial motility in the rat facial nucleus following peripheral axotomy. Journal of neurocytology 1999, 28:439-453.
53. Sierra A., Encinas J.M., Deudero J.J., Chancey J.H., Enikolopov G., Overstreet-Wadiche L.S., Tsirka S.E., Maletic-Savatic M. Microglia shape adult hippocampal neurogenesis through apoptosis-coupled phagocytosis. Cell Stem Cell 2010, 7:483-495.
54. 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.
55. Streit W.J., Braak H., Xu Q.S., Bechmann I. Dystrophic (senescent) rather than activated microglial cells are associated with tau pathology and likely precede neurodegeneration in Alzheimer's disease. Acta Neuropathologica 2009, 118:475-486.
56. Terai K., Walker D.G., McGeer E.G., McGeer P.L. Neurons express proteins of the classical complement pathway in Alzheimer disease. Brain Research 1997, 769:385-390.
57. Trapp B.D., Wujek J.R., Criste G.A., Jalabi W., Yin X., Kidd G.J., Stohlman S., Ransohoff R. Evidence for synaptic stripping by cortical microglia. Glia 2007, 55:360-368.
58. Tremblay M.E., Lowery R.L., Majewska A.K. Microglial interactions with synapses are modulated by visual experience. PLoS Biology 2010, 8:e1000527.
59. Van der Laan L.J., Ruuls S.R., Weber K.S., Lodder I.J., Dopp E.A., Dijkstra C.D. Macrophage phagocytosis of myelin in vitro determined by flow cytometry: phagocytosis is mediated by CR3 and induces production of tumor necrosis factor-alpha and nitric oxide. Journal of Neuroimmunology 1996, 70:145-152.
60. Wake H., Moorhouse A.J., Jinno S., Kohsaka S., Nabekura J. Resting microglia directly monitor the functional state of synapses in vivo and determine the fate of ischemic terminals. Journal of Neuroscience 2009, 29:3974-3980.
61. Wakselman S., Bechade C., Roumier A., Bernard D., Triller A., Bessis A. Developmental neuronal death in hippocampus requires the microglial CD11b integrin and DAP12 immunoreceptor. Journal of Neuroscience 2008, 28:8138-8143.
62. Walton N.M., Sutter B.M., Laywell E.D., Levkoff L.H., Kearns S.M., Marshall G.P., Scheffler B., Steindler D.A. Microglia instruct subventricular zone neurogenesis. Glia 2006, 54:815-825.
63. Webster S., Bradt B., Rogers J., Cooper N. Aggregation state-dependent activation of the classical complement pathway by the amyloid beta peptide. Journal of Neurochemistry 1997, 69:388-398.
64. Webster S.D., Park M., Fonseca M.I., Tenner A.J. Structural and functional evidence for microglial expression of C1qR(P), the C1q receptor that enhances phagocytosis. Journal of Leukocyte Biology 2000, 67:109-116.
65. Webster S.D., Yang A.J., Margol L., Garzon-Rodriguez W., Glabe C.G., Tenner A.J. Complement component C1q modulates the phagocytosis of Abeta by microglia. Experimental Neurology 2000, 161:127-138.
66. Wiesel T.N., Hubel D.H. Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens. Journal of Neurophysiology 1965, 28:1029-1040.
67. Wyss-Coray T., Yan F., Lin A.H., Lambris J.D., Alexander J.J., Quigg R.J., Masliah E. Prominent neurodegeneration and increased plaque formation in complement-inhibited Alzheimer's mice. Proceedings of the National Academy of Sciences of the United States of America 2002, 99:10837-10842.
68. Yang, T.T., Lin, C., Hsu, C.T., Wang, T.F., Ke, F.Y., Kuo, Y.M. Differential distribution and activation of microglia in the brain of male C57BL/6J mice. Brain Structure & Function [Epub ahead of print],, in press. doi:10.1007/s00429-012-0446-x.
69. Yuzaki M. Synapse formation and maintenance by C1q family proteins: a new class of secreted synapse organizers. European Journal of Neuroscience 2010, 32:191-197.
70. Zabel, M., Schrag, M., Crofton, A., Tung, S., Beaufond, P., Van Ornam, J., DiNinni, A., Vinters, H.V., Coppola, G., Kirsch, W.M. A shift in microglial β-amyloid binding in Alzheimer's disease is associated with cerebral amyloid angiopathy. Brain Pathology [Epub ahead of print], in press.
71. 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. Journal of Neurochemistry 2008, 106:2080-2092.