Complement and blood-brain barrier integrity

Molecular Immunology

Volumn 61, Issue 2, 2014, Pages 149-152

  Jacob, Alexander ^a   Alexander, Jessy John ^a  

^a UNIVERSITY AT BUFFALO   (United States)

Author keywords

Blood brain barrier; Complement; Neurodegeneration

Indexed keywords

COMPLEMENT; COMPLEMENT COMPONENT C5A; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR C5AR1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MICRORNA; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; BLOOD BRAIN BARRIER; COMPLEMENT ACTIVATION; ENDOTHELIUM CELL; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MYELOOPTIC NEUROPATHY; PRIORITY JOURNAL; REVIEW; SEPSIS; SYSTEMIC LUPUS ERYTHEMATOSUS;

BLOOD-BRAIN BARRIER; COMPLEMENT; NEURODEGENERATION;

ANIMALS; BIOLOGICAL TRANSPORT; BLOOD-BRAIN BARRIER; COMPLEMENT SYSTEM PROTEINS; HUMANS; INFLAMMATION; NEURODEGENERATIVE DISEASES; PERMEABILITY;

EID: 84907598455     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2014.06.039     Document Type: Review

References (71)

1. Abbott N.J., Mendonca L.L., Dolman D.E. The blood-brain barrier in systemic lupus erythematosus. Lupus 2003, 12:908-915.
2. Abbott N.J., Ronnback L., Hansson E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat. Rev. Neurosci. 2006, 7:41-53.
3. Alexander J.J., Anderson A.J., Barnum S.R., Stevens B., Tenner A.J. The complement cascade: Yin-Yang in neuroinflammation-neuro-protection and -degeneration. J. Neurochem. 2008, 107:1169-1187.
4. Antonelli-Orlidge A., Saunders K.B., Smith S.R., D'Amore P.A. An activated form of transforming growth factor beta is produced by cocultures of endothelial cells and pericytes. Proc. Natl. Acad. Sci. U.S.A. 1989, 86:4544-4548.
5. Armulik A., Genové G., Mäe M., Nisancioglu M.H., Wallgard E., Niaudet C., He L., Norlin J., Lindblom P., Strittmatter K., Johansson B.R., Betsholtz C. Pericytes regulate the blood-brain barrier. Nature 2010, 468:557-561.
6. Asgari N., Khorooshi R., Lillevang S.T., Owens T. Complement-dependent pathogenicity of brain-specific antibodies in cerebrospinal fluid. J. Neuroimmunol. 2013, 15:76-82.
7. Banks W.A., Farr S.A., Morley J.E. Permeability of the blood-brain barrier to albumin and insulin in the young and aged SAMP8 mouse. J. Gerontol. A: Biol. Sci. Med. Sci. 2000, 55:B601-B606.
8. Bonauer A., Boon R.A., Dimmeler S. Vascular microRNAs. Curr. Drug Targets 2010, 11:943-949.
9. Brown R.C., Morris A.P., O'Neil R.G. Tight junction protein expression and barrier properties of immortalized mouse brain microvessel endothelial cells. Brain Res. 2007, 1130:17-30.
10. Carroll M.C. The lupus paradox. Nat. Genet. 1998, 19:3-4.
11. Crane J.W., Buller K.M. Systemic blockade of complement C5a receptors reduces lipopolysacharride-induced responses in the paraventricular nucleus and the central amygdala. Neurosci. Lett. 2007, 424:10-15.
12. Crone C., Olesen S.P. Electrical resistance of brain microvascular endothelium. Brain Res. 1982, 241:49-55.
13. D'Andrea M.R. Evidence that immunoglobulin-positive neurons in Alzheimer's disease are dying via the classical antibody-dependent complement pathway. Am. J. Alzheimers Dis. Other Demen. 2005, 20:144-150.
14. Daneman R., Zhou L., Kebede A.A., Barres B.A. Pericytes are required for blood-brain barrier integrity during embryogenesis. Nature 2010, 468:562-566.
15. Davson H., Zlokovic B.V., Rakic L., Segal M.B. An Introduction to the Blood-Brain Barrier 1993, Macmillan, London.
16. Davson H., Segal M.B. Physiology of the CSF and the Blood-Brain Barrier 1995, CRC, New York, NY, USA.
17. deBoer A.G., Gaillard P.J. Blood-brain barrier dysfunction and recovery. J. Neural Transm. 2006, 113:455-462.
18. DeGiorgio L.A., Konstantinov K.N., Lee S.C., Hardin J.A., Volpe B.T., Diamond B. A subset of lupus anti-DNA antibodies cross-reacts with the NR2 glutamate receptor in systemic lupus erythematosus. Nat. Med. 2001, 7:1189-1193.
19. Diamond B. Antibodies and the brain: lessons from lupus. J. Immunol. 2010, 185:2637-2640.
20. Eadon, M.T., Jacob, A., Cunningham, P.N., Quigg, R.J., Garcia, J.G., Alexander, J.J. Transcriptional profiling reveals that C5a alters miRNA in brain endothelial cells. Immunology. 2014 May 6. (epub ahead of print). doi:10.1111/imm.12314.
21. Engelhardt S., Patkar S., Ogunshola O.O. Cell-specific blood-brain barrier regulation in health and disease: a focus on hypoxia. Br. J. Pharmacol. 2014, 171:1210-1230.
22. Filipowicz W., Bhattacharyya S.N., Sonenberg N. Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight?. Nat. Rev. Genet. 2008, 9:102-114.
23. Flaherty P., Radhakrishnan M.L., Dinh T., Rebres R.A., Roach T.I., Jordan M.I., Arkin A.P. A dual receptor crosstalk model of G-protein-coupled signal transduction. PLoS Comput. Biol. 2008, 4:e1000185.
24. Flierl M.A., Stahel P.F., Rittirsch D., Huber-Lang M., Niederbichler A.D., Hoesel L.M., Touban B.M., Morgan S.J., Smith W.R., Ward P.A., Ipaktchi K. Inhibition of complement C5a prevents breakdown of the blood-brain barrier and pituitary dysfunction in experimental sepsis. Crit. Care 2009, 13:R12.
25. Fonseca M.I., Ager R.R., Chu S.H., Yazan O., Sanderson S.D., LaFerla F.M., Taylor S.M., Woodruff T.M., Tenner A.J. Treatment with a C5aR1 antagonist decreases pathology and enhances behavioral performance in murine models of Alzheimer's disease. J. Immunol. 2009, 183:1375-1383.
26. Frigerio S., Gelati M., Ciusani E., Corsini E., Dufour A., Massa G., et al. Immunocompetence of human microvascular brain endothelial cells:cytokine regulation of IL-1beta, MCP-1, IL-10, sICAM-1and sVCAM-1. J. Neurol. 1998, 245:444.
27. Gasque P., Singhrao S.K., Neal J.W., Wang P., Sayah S., Fontaine M., 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. 1998, 160:3543-3554.
28. Hanly J.G., Robichaud J., Fisk J.D. Anti-NR2 glutamate receptor antibodies and cognitive function in systemic lupus erythematosus. J. Rheumatol. 2006, 33:1553-1558.
29. Hawkins B.T., Egleton R.D. Fluorescence imaging of blood-brain barrier disruption. J. Neurosci. Methods 2006, 151:262-267.
30. Hoarau J.J., Krejbich-Trotot P., Jaffar-Bandjee M.C., Das T., Thon-Hon G.V., Kumar S., Neal J.W., Gasque P. Activation and control of CNS innate immune responses in health and diseases: a balancing act finely tuned by neuroimmune regulators (NIReg). CNS Neurol Disord.: Drug Targets 2011, 2:25-43.
31. Iadecola C., Nedergaard M. Glial regulation of the cerebral microvasculature. Nat. Neurosci. 2007, 10:1369-1376.
32. Ischenko A., Sayah S., Patte C., Andreev S., Gasque P., Schouft M.T., Vaudry H., Fontaine M. Expression of a functional anaphylatoxin C3a receptor by astrocytes. J. Neurochem. 1998, 71:2487-2496.
33. Jacob A., Hack B., Chiang E., Garcia J.G., Quigg R.J., Alexander J.J. C5a alters blood-brain barrier integrity in experimental lupus. FASEB J. 2010, 24:1682-1688.
34. Jacob A., Brorson J.R., Alexander J.J. Septic encephalopathy: inflammation in man and mouse. Neurochem. Int. 2011, 58:472-476.
35. Jacob A., Hack B., Chen P., Quigg R.J., Alexander J.J. C5a/CD88 signaling alters blood-brain barrier integrity in lupus through nuclear factor-κB. J. Neurochem. 2011, 119:1041-1051.
36. Jaffer H., Adjei I.M., Labhasetwar V. Optical imaging to map blood-brain barrier leakage. Sci. Rep. 2013, 3:3117.
37. Jauneau A.C., Ischenko A., Chan P., et al. Complement component anaphylatoxins upregulate chemokine expression by human astrocytes. FEBS Lett. 2003, 537:17-22.
38. Kim D.D., Song W.C., Membrane complement regulatory proteins Clin. Immunol. 2006, 118:127-136.
39. Kim H., Erdman L.K., Lu Z., Serghides L., Zhong K., Dhabangi A., Musoke C., Gerard C., Cserti-Gazdewich C., Liles W.C., Kain K.C. Functional roles for C5a and C5aR1 but not C5L2 in the pathogenesis of human and experimental cerebral malaria. Infect. Immun. 2014, 82:371-379.
40. Klohs J., Steinbrink J., Bourayou R., Mueller S., Cordell R., Licha K., Schirner M., Dirnagl U., Lindauer U., Wunder A. Near-infrared fluorescence imaging with fluorescently labeled albumin: a novel method for non-invasive optical imaging of blood-brain barrier impairment after focal cerebral ischemia in mice. J. Neurosci. Methods 2009, 180:126-132.
41. Kook S.Y., Seok Hong H., Moon M., Mook-Jung I. Disruption of blood-brain barrier in Alzheimer disease pathogenesis. Tissue Barriers 2013, 1:e23993.
42. Lévi-Strauss M., Mallat M. Primary cultures of murine astrocytes produce C3 and factor B, two components of the alternative pathway of complement activation. J. Immunol. 1987, 139:2361-2366.
43. Lucas S.M., Rothwell N.J., Gibson R.M. The role of inflammation in CNS injury and disease. Br. J. Pharmacol. 2006, 147(Suppl. 1):S232-S240.
44. Markiewicz M., Richard E., Marks N., Ludwicka-Bradley A. Impact of endothelial microparticles on coagulation, inflammation, and angiogenesis in age-related vascular diseases. J. Aging Res. 2013, 2013:734509.
45. Minn A., Ghersi-Egea J.F., Perrin R., Leininger B., Siest G. Drug metabolizing enzymes in the brain and cerebral microvessels. Brain Res. 1991, 16:65-82.
46. Mukherjee P., Pasinetti G.M. The role of complement anaphylatoxin C5a in neurodegeneration: implications in Alzheimer's disease. J. Neuroimmunol. 2000, 105:124-130. (review).
47. Mukherjee P., Pasinetti G.M. Complement anaphylatoxin C5a neuroprotects through mitogen-activated protein kinase-dependent inhibition of caspase 3. J. Neurochem. 2001, 77:43-49.
48. Mulligan S.J., MacVicar B.A. Calcium transients in astrocyte endfeet cause cerebrovascular constrictions. Nature 2004, 431:195-199.
49. Muoio V., Persson P.B., Sendeski M.M. The neurovascular unit - concept review. Acta Physiol. (Oxf.) 2014, 210:790-798.
50. Naik A., Cucullo L. In vitro blood-brain barrier models: current and perspective technologies. J. Pharm. Sci. 2012, 101:1337-1354.
51. Nishimura Y., Yata K., Nomoto T., Ogiwara T., Watanabe K., Shintou T., Tsuboyama A., Okano M., Umemoto N., Zhang Z., Kawabata M., Zhang B., Kuroyanagi J., Shimada Y., Miyazaki T., Imamura T., Tomimoto H., Tanaka T. Identification of a novel indoline derivative for in vivo fluorescent imaging of blood-brain barrier disruption in animal models. ACS Chem. Neurosci. 2013, 4:1183-1193.
52. Osaka H., Mukherjee P., Aisen P.S., Pasinetti G.M. Complement-derived anaphylatoxin C5a protects against glutamate-mediated neurotoxicity. J. Cell Biochem. 1999, 73:303-311.
53. Paul D., Cowan A.E., Ge S., Pachter J.S. Novel 3D analysis of Claudin-5 reveals significant endothelial heterogeneity among CNS microvessels. Microvasc. Res. 2013, 86:1-10.
54. Ratelade J., Verkman A.S. Neuromyelitis optica: Aquaporin-4 based pathogenesis mechanisms and new therapies. Int. J. Biochem. Cell Biol. 2012, 44:1519-1530.
55. Reijerkerk A., Lopez-Ramirez M.A., van het Hof B., Drexhage J.A.R., Kamphuis W.W., Kooij G., Vos J.B., van der Pouw Kraan T.C.T.M., van Zonneveld A.J., Horrevoets A.J., Prat A., Romero I.A., de Vries H.E. MicroRNAs regulate human brain endothelial cell-barrier function in inflammation: implications for multiple sclerosis. J. Neurosci. 2013, 17:6857-6863.
56. Rice A., Liu Y., Michaelis M.L., Himes R.H., Georg G.I., Audus K.L. Chemical modification of paclitaxel (Taxol) reduces P-glycoprotein interactions and increases permeation across the blood-brain barrier in vitro and in situ. J. Med. Chem. 2005, 48:832-838.
57. Rock R.B., Peterson P.K. Microglia as a pharmacological target in infectious and inflammatory diseases of the brain. J. Neuroimmune Pharmacol. 2006, 1:117-126.
58. Sá-Pereira I., Brites D., Brito M.A. Neurovascular unit: a focus on pericytes. Mol. Neurobiol. 2012, 45:327-347.
59. Schäfer M.K., Schwaeble W.J., Post C., Salvati P., Calabresi M., Sim R.B., Petry F., Loos M., Weihe E. Complement C1q is dramatically up-regulated in brain microglia in response to transient global cerebral ischemia. J. Immunol. 2000, 164:5446-5452.
60. Siegel G.J., Agranoff, B.W., Albers, R.W., et al., 1999. Basic Neurochemistry: Molecular, Cellular and Medical Aspects, 6th ed. Lippincott-Raven, Philadelphia.
61. Singhrao S.K., Neal J.W., Rushmere N.K., Morgan B.P., Gasque P. Differential expression of individual complement regulators in the brain and choroid plexus. Lab Invest. 1999, 79:1247-1259.
62. Stone K.P., Kastin A.J., Pan W. NFκB is an unexpected major mediator of interleukin-15 signaling in cerebral endothelia. Cell Physiol. Biochem. 2011, 28:115-124.
63. Suárez Y., Sessa W.C. MicroRNAs as novel regulators of angiogenesis. Circ. Res. 2009, 104:442-454.
64. Tomizawa Y., Yokoyama K., Saiki S., Takahashi T., Matsuoka J., Hattori N. Blood-brain barrier disruption is more severe in neuromyelitis optica than in multiple sclerosis and correlates with clinical disability. J. Int. Med. Res. 2012, 40:1483-1491.
65. Van Beek J., Bernaudin M., Petit E., Gasque P., Nouvelot A., MacKenzie E.T., Fontaine M. Expression of receptors for complement anaphylatoxins C3a and C5a following permanent focal cerebral ischemia in the mouse. Exp. Neurol. 2000, 2:373-382.
66. Veerhuis R. Histological and direct evidence for the role of complement in the neuroinflammation of AD. Curr. Alzheimer Res. 2011, 2:34-58.
67. Verbeek M.M., Otte-Höller I., Ruiter D.J., de Waal R.M. Human brain pericytes as a model system to study the pathogenesis of cerebrovascular amyloidosis in Alzheimer's disease. Cell Mol. Biol. (Noisy-le-grand). 1999, 45:37-46.
68. Vercellotti G.M., Moldow C.F., Jacob H.S. Complement, oxidants, and endothelial injury: how a bedside observation opened a door to vascular biology. J. Clin. Invest. 2012, 122:3044-3045.
69. Ward P.A., Guo R.F., Riedemann N.C. Manipulation of the complement system for benefit in sepsis. Crit. Care Res. Pract. 2012, 2012:427607.
70. Zhang X., Kimura Y., Fang C., Zhou L., Sfyroera G., Lambris J.D., Wetsel R.A., Miwa T., Song W.C. Regulation of Toll-like receptor-mediated inflammatory response by complement in vivo. Blood 2007, 110:228-236.
71. Zlokovic B.V. The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron 2008, 57:178-201.