C5a/CD88 signaling alters blood-brain barrier integrity in lupus through nuclear factor-κB

Journal of Neurochemistry

Volumn 119, Issue 5, 2011, Pages 1041-1051

  Jacob, Alexander ^a   Hack, Bradley ^a   Chen, Peili ^a   Quigg, Richard J ^a   Alexander, Jessy J ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

blood brain barrier; C5a; complement; inflammation

Indexed keywords

CASPASE 3; COMPLEMENT COMPONENT C5A; COMPLEMENT COMPONENT C5A RECEPTOR; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DNA; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN ZO1; TRANSCRIPTION FACTOR RELA;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BLOOD BRAIN BARRIER; BRAIN BLOOD VESSEL; CELL NUCLEUS; COMPLEMENT ACTIVATION; COMPLEMENT SYSTEM; CONTROLLED STUDY; DRUG TARGETING; ENDOTHELIUM CELL; ENZYME ACTIVITY; IMMUNOFLUORESCENCE; INFLAMMATION; MICROENVIRONMENT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; SYSTEMIC LUPUS ERYTHEMATOSUS;

ANIMALS; APOPTOSIS; BLOOD-BRAIN BARRIER; CELL LINE, TRANSFORMED; COMPLEMENT C5A; ENDOTHELIAL CELLS; LUPUS ERYTHEMATOSUS, SYSTEMIC; MICE; MICE, INBRED C57BL; NF-KAPPA B; PRIMARY CELL CULTURE; RECEPTOR, ANAPHYLATOXIN C5A; SIGNAL TRANSDUCTION;

EID: 81255160569     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2011.07490.x     Document Type: Article

References (66)

1. Abbott N. J., Mendonca L. L., and, Dolman D. E., (2003) The blood-brain barrier in systemic lupus erythematosus. Lupus 12, 908-915. (Pubitemid 38082086)
2. Abbott N. J., Ronnback L., and, Hansson E., (2006) Astrocyte-endothelial interactions at the blood-brain barrier. Nat. Rev. Neurosci. 7, 41-53. (Pubitemid 41828930)
3. Albrecht E. A., Chinnaiyan A. M., Varambally S., Kumar-Sinha C., Barrette T. R., Sarma J. V., and, Ward P. A., (2004) C5a-induced gene expression in human umbilical vein endothelial cells. Am. J. Pathol. 164, 849-859. (Pubitemid 38235467)
4. Alexander J. J., Bao L., Jacob A., Kraus D. M., Holers V. M., and, Quigg R. J., (2003) Administration of the soluble complement inhibitor, Crry-Ig, reduces inflammation and aquaporin 4 expression in lupus cerebritis. Biochim. Biophys. Acta 1639, 169-176. (Pubitemid 37421424)
5. Alexander J. J., Jacob A., Bao L., MacDonald R. L., and, Quigg R. J., (2005) Complement-dependent apoptosis and inflammatory gene changes in murine lupus cerebritis. J. Immunol. 175, 8312-8319. (Pubitemid 41798397)
6. Alexander J. J., Jacob A., Vezina P., Sekine H., Gilkeson G. S., and, Quigg R. J., (2007) Absence of functional alternative complement pathway alleviates lupus cerebritis. Eur. J. Immunol. 37, 1691-1701. (Pubitemid 46939502)
7. Alexander J. J., Anderson A. J., Barnum S. R., Stevens B., and, Tenner A. J., (2008) The complement cascade: Yin-Yang in neuroinflammation - neuro-protection and -degeneration. J. Neurochem. 107, 1169-1187.
8. Barnum S. R., (2002) Complement in central nervous system inflammation. Immunol. Res. 26, 7-13. (Pubitemid 35177479)
9. Brown R. C., Morris A. P., and, O'Neil R. G., (2007) Tight junction protein expression and barrier properties of immortalized mouse brain microvessel endothelial cells. Brain Res. 1130, 17-30. (Pubitemid 46053886)
10. Buyon J. P., Tamerius J., Belmont H. M., and, Abramson S. B., (1992) Assessment of disease activity and impending flare in patients with systemic lupus erythematosus. Comparison of the use of complement split products and conventional measurements of complement. Arthritis Rheum. 35, 1028-1037.
11. Carroll M. C., (1998) The lupus paradox. Nat. Genet. 19, 3-4. (Pubitemid 28242011)
12. Carroll M. C., (2004) A protective role for innate immunity in systemic lupus erythematosus. Nat. Rev. Immunol. 4, 825-831. (Pubitemid 39336298)
13. Carroll M. C., and, Fischer M. B., (1997) Complement and the immune response. Curr. Opin. Immunol. 9, 64-69. (Pubitemid 27095899)
14. Chen N. J., Mirtsos C., Suh D., Lu Y. C., Lin W. J., McKerlie C., Lee T., Baribault H., Tian H., and, Yeh W. C., (2007) C5L2 is critical for the biological activities of the anaphylatoxins C5a and C3a. Nature 446, 203-207. (Pubitemid 46398661)
15. Davies D. C., (2002a) Blood-brain barrier breakdown and oedema formation in systemic sepsis and human brain tumours. J. Anat. 200, 528-529.
16. Davies D. C., (2002b) Blood-brain barrier breakdown in septic encephalopathy and brain tumours. J. Anat. 200, 639-646. (Pubitemid 34823055)
17. Davson H., and, Segal M. B., (1995) Physiology of the CSF and the Blood-Brain Barrier. CRC, New York.
18. Davson H., Zlokovic B. V., Rakic L., and, Segal M. B., (1993) An Introduction to the Blood-Brain Barrier. Macmillan, London.
19. Diamond B., Kowal C., Huerta P. T., Aranow C., Mackay M., DeGiorgio L. A., Lee J., Triantafyllopoulou A., Cohen-Solal J., and, Volpe B. T., (2006) Immunity and acquired alterations in cognition and emotion: lessons from SLE. Adv. Immunol. 89, 289-320.
20. Ducruet A. F., Zacharia B. E., Hickman Z. L., Grobelny B. T., Yeh M. L., Sosunov S. A., and, Connolly Jr E. S., (2009) The complement cascade as a therapeutic target in intracerebral hemorrhage. Exp. Neurol. 219, 398-403.
21. Farkas I., Baranyi L., Takahashi M., Fukuda A., Liposits Z., Yamamoto T., and, Okada H., (1998) A neuronal C5a receptor and an associated apoptotic signal transduction pathway. J. Physiol. 507 (Pt 3), 679-687. (Pubitemid 28143569)
22. Finch A. M., Wong A. K., Paczkowski N. J., Wadi S. K., Craik D. J., Fairlie D. P., and, Taylor S. M., (1999) Low-molecular-weight peptidic and cyclic antagonists of the receptor for the complement factor C5a. J. Med. Chem. 42, 1965-1974. (Pubitemid 29269629)
23. Flierl M. A., Rittirsch D., Chen A. J., Nadeau B. A., Day D. E., Sarma J. V., Huber-Lang M. S., and, Ward P. A., (2008) The complement anaphylatoxin C5a induces apoptosis in adrenomedullary cells during experimental sepsis. PLoS ONE 3, e2560.
24. Flierl M. A., Stahel P. F., Rittirsch D., et al. (2009) Inhibition of complement C5a prevents breakdown of the blood-brain barrier and pituitary dysfunction in experimental sepsis. Crit. Care 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., and, Tenner A. J., (2009) Treatment with a C5aR antagonist decreases pathology and enhances behavioral performance in murine models of Alzheimer's disease. J. Immunol. 183, 1375-1383.
26. Gasque P., Chan P., Fontaine M., Ischenko A., Lamacz M., Gotze O., and, Morgan B. P., (1995) Identification and characterization of the complement C5a anaphylatoxin receptor on human astrocytes. J. Immunol. 155, 4882-4889.
27. Gasque P., Singhrao S. K., Neal J. W., Gotze O., and, Morgan B. P., (1997) Expression of the receptor for complement C5a (CD88) is up-regulated on reactive astrocytes, microglia, and endothelial cells in the inflamed human central nervous system. Am. J. Pathol. 150, 31-41. (Pubitemid 27027093)
28. Goswami R., Kilkus J., Dawson S. A., and, Dawson G., (1999) Overexpression of Akt (protein kinase B) confers protection against apoptosis and prevents formation of ceramide in response to pro-apoptotic stimuli. J. Neurosci. Res. 57, 884-893. (Pubitemid 29416119)
29. Guo R. F., and, Ward P. A., (2005) Role of C5a in inflammatory responses. Annu. Rev. Immunol. 23, 821-852. (Pubitemid 40563186)
30. Guo R. F., Riedemann N. C., and, Ward P. A., (2004) Role of C5a-C5aR interaction in sepsis. Shock 21, 1-7.
31. He H. J., Zhu T. N., Xie Y., Fan J., Kole S., Saxena S., and, Bernier M., (2006) Pyrrolidine dithiocarbamate inhibits interleukin-6 signaling through impaired STAT3 activation and association with transcriptional coactivators in hepatocytes. J. Biol. Chem. 281, 31369-31379. (Pubitemid 46041401)
32. Hill H. D., and, Straka J. G., (1988) Protein determination using bicinchoninic acid in the presence of sulfhydryl reagents. Anal. Biochem. 170, 203-208.
33. Hopkins P., Belmont H. M., Buyon J., Philips M., Weissmann G., and, Abramson S. B., (1988) Increased levels of plasma anaphylatoxins in systemic lupus erythematosus predict flares of the disease and may elicit vascular injury in lupus cerebritis. Arthritis Rheum. 31, 632-641.
34. Huerta P. T., Kowal C., DeGiorgio L. A., Volpe B. T., and, Diamond B., (2006) Immunity and behavior: antibodies alter emotion. Proc. Natl Acad. Sci. USA 103, 678-683. (Pubitemid 43153085)
35. Ibrahim F. B., Pang S. J., and, Melendez A. J., (2004) Anaphylatoxin signaling in human neutrophils. A key role for sphingosine kinase. J. Biol. Chem. 279, 44802-44811. (Pubitemid 39430891)
36. Jacob A., Bao L., Brorson J., Quigg R. J., and, Alexander J. J., (2010a) C3aR inhibition reduces neurodegeneration in experimental lupus. Lupus 19, 73-82.
37. Jacob A., Hack B., Bai T., Brorson J. R., Quigg R. J., and, Alexander J. J., (2010b) Inhibition of C5a receptor alleviates experimental CNS lupus. J. Neuroimmunol. 221, 46-52.
38. Jacob A., Hack B., Chiang E., Garcia J. G., Quigg R. J., and, Alexander J. J., (2010c) C5a alters blood-brain barrier integrity in experimental lupus. FASEB J. 24 (6), 1682-8.
39. Lampugnani M. G., (2010) Endothelial adherens junctions and the actin cytoskeleton: an 'infinity net'? J. Biol. 9, 16.
40. Laudes I. J., Chu J. C., Huber-Lang M., et al. (2002) Expression and function of C5a receptor in mouse microvascular endothelial cells. J. Immunol. 169, 5962-5970. (Pubitemid 35299387)
41. Li G., Simon M. J., Cancel L. M., Shi Z. D., Ji X., Tarbell J. M., Morrison III B., and, Fu B. M., (2010) Permeability of endothelial and astrocyte cocultures: in vitro blood-brain barrier models for drug delivery studies. Ann. Biomed. Eng. 38, 2499-2511.
42. Ma T. Y., Iwamoto G. K., Hoa N. T., Akotia V., Pedram A., Boivin M. A., and, Said H. M., (2004) TNF-alpha-induced increase in intestinal epithelial tight junction permeability requires NF-kappa B activation. Am. J. Physiol. Gastrointest. Liver Physiol. 286, G367-G376. (Pubitemid 38250308)
43. Millan J., Cain R. J., Reglero-Real N., Bigarella C., Marcos-Ramiro B., Fernandez-Martin L., Correas I., and, Ridley A. J., (2010) Adherens junctions connect stress fibres between adjacent endothelial cells. BMC Biol. 8, 11.
44. Monsinjon T., Gasque P., Chan P., Ischenko A., Brady J. J., and, Fontaine M. C., (2003) Regulation by complement C3a and C5a anaphylatoxins of cytokine production in human umbilical vein endothelial cells. FASEB J. 17, 1003-1014. (Pubitemid 36681518)
45. Mukherjee P., and, Pasinetti G. M., (2001) Complement anaphylatoxin C5a neuroprotects through mitogen-activated protein kinase-dependent inhibition of caspase 3. J. Neurochem. 77, 43-49. (Pubitemid 32245078)
46. Muller-Eberhard H. J., (1986) The membrane attack complex of complement. Annu. Rev. Immunol. 4, 503-528.
47. Muller-Eberhard H. J., (1988) Molecular organization and function of the complement system. Annu. Rev. Biochem. 57, 321-347.
48. Muller-Eberhard H. J., and, Schreiber R. D., (1980) Molecular biology and chemistry of the alternative pathway of complement. Adv. Immunol. 29, 1-53.
49. Nauta A. J., Daha M. R., Tijsma O., van de W. B., Tedesco F., and, Roos A., (2002) The membrane attack complex of complement induces caspase activation and apoptosis. Eur. J. Immunol. 32, 783-792. (Pubitemid 34257556)
50. Niculescu T., Weerth S., Soane L., Niculescu F., Rus V., Raine C. S., Shin M. L., and, Rus H., (2003) Effects of membrane attack complex of complement on apoptosis in experimental autoimmune encephalomyelitis. Ann. N Y Acad. Sci. 1010, 530-533. (Pubitemid 38265039)
51. Niculescu T., Weerth S., Niculescu F., Cudrici C., Rus V., Raine C. S., Shin M. L., and, Rus H., (2004) Effects of complement C5 on apoptosis in experimental autoimmune encephalomyelitis. J. Immunol. 172, 5702-5706. (Pubitemid 38542074)
52. Nishimura K., Harigai M., Omori M., Sato E., and, Hara M., (2008) Blood-brain barrier damage as a risk factor for corticosteroid-induced psychiatric disorders in systemic lupus erythematosus. Psychoneuroendocrinology 33, 395-403.
53. Nishiura H., Nonaka H., Revollo I. S., Semba U., Li Y., Ota Y., Irie A., Harada K., Kehrl J. H., and, Yamamoto T., (2009) Pro- and anti-apoptotic dual functions of the C5a receptor: involvement of regulator of G protein signaling 3 and extracellular signal-regulated kinase. Lab. Invest. 89 (6), 676-94.
54. Parry G. C., and, Mackman N., (1997) Role of cyclic AMP response element-binding protein in cyclic AMP inhibition of NF-kappaB-mediated transcription. J. Immunol. 159, 5450-5456. (Pubitemid 127470072)
55. Schraufstatter I. U., Trieu K., Sikora L., Sriramarao P., and, DiScipio R., (2002) Complement c3a and c5a induce different signal transduction cascades in endothelial cells. J. Immunol. 169, 2102-2110. (Pubitemid 34857676)
56. Short A., Wong A. K., Finch A. M., Haaima G., Shiels I. A., Fairlie D. P., and, Taylor S. M., (1999) Effects of a new C5a receptor antagonist on C5a- and endotoxin-induced neutropenia in the rat. Br. J. Pharmacol. 126, 551-554. (Pubitemid 29087828)
57. Singhrao S. K., Neal J. W., Morgan B. P., and, Gasque P., (1999) Increased complement biosynthesis by microglia and complement activation on neurons in Huntington's disease. Exp. Neurol. 159, 362-376. (Pubitemid 29485223)
58. Tenner A. J., and, Fonseca M. I., (2006) The double-edged flower: roles of complement protein C1q in neurodegenerative diseases. Adv. Exp. Med. Biol. 586, 153-176.
59. Thurman J. M., Lenderink A. M., Royer P. A., Coleman K. E., Zhou J., Lambris J. D., Nemenoff R. A., Quigg R. J., and, Holers V. M., (2007) C3a is required for the production of CXC chemokines by tubular epithelial cells after renal ishemia/reperfusion. J. Immunol. 178, 1819-1828. (Pubitemid 46154654)
60. Uwai M., Terui Y., Mishima Y., et al. (2000) A new apoptotic pathway for the complement factor B-derived fragment Bb. J. Cell. Physiol. 185, 280-292.
61. deVries B., Kohl J., Leclercq W. K., Wolfs T. G., van Bijnen A. A., Heeringa P., and, Buurman W. A., (2003) Complement factor C5a mediates renal ischemia-reperfusion injury independent from neutrophils. J. Immunol. 170, 3883-3889. (Pubitemid 36359260)
62. Wang H., Ding T., Brown N., Yamamoto Y., Prince L. S., Reese J., and, Paria B. C., (2008) Zonula occludens-1 (ZO-1) is involved in morula to blastocyst transformation in the mouse. Dev. Biol. 318, 112-125.
63. Ward P. A., (2008a) Role of the complement in experimental sepsis. J. Leukoc. Biol. 83, 467-470. (Pubitemid 351966852)
64. Ward P. A., (2008b) Sepsis, apoptosis and complement. Biochem. Pharmacol. 76, 1383-1388.
65. Woodruff T. M., Ager R. R., Tenner A. J., Noakes P. G., and, Taylor S. M., (2010) The role of the complement system and the activation fragment C5a in the central nervous system. Neuromol. Med. 12, 179-192.
66. Yuan W., Li G., Gil E. S., Lowe T. L., and, Fu B. M., (2010) Effect of surface charge of immortalized mouse cerebral endothelial cell monolayer on transport of charged solutes. Ann. Biomed. Eng. 38, 1463-1472.