Bradykinin enhances Sindbis virus infection in human brain microvascular endothelial cells

Virology

Volumn 422, Issue 1, 2012, Pages 81-91

  Rust, Naiara Miranda ^a   Papa, Michelle Premazzi ^a   Scovino, Aline Miranda ^a   da Silva, Mayara Marques Carneiro ^b   Calzavara Silva, Carlos Eduardo ^b   Marques, Ernesto Torres de Azevedo ^b   Peçanha, Ligia Maria Torres ^a   Scharfstein, Julio ^a   Arruda, Luciana B ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b INSTITUTO OSWALDO CRUZ   (Brazil)

Author keywords

Apoptosis; Bradykinin; Endothelial cells; Sindbis

Indexed keywords

BRADYKININ; BRADYKININ B2 RECEPTOR; BRADYKININ B2 RECEPTOR ANTAGONIST; CAPTOPRIL; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; WORTMANNIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BRAIN INFECTION; CELL SURVIVAL; CONTROLLED STUDY; DISEASE ASSOCIATION; DRUG EFFICACY; ENZYME INHIBITION; ENZYME REGULATION; FEMALE; HUMAN; HUMAN CELL; MALE; MICROVASCULAR ENDOTHELIAL CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SINDBIS VIRUS; TREATMENT RESPONSE; VASCULAR DISEASE; VIRUS INFECTION; VIRUS LOAD; VIRUS REPLICATION;

ALPHAVIRUS INFECTIONS; ANIMALS; APOPTOSIS; BRADYKININ; BRAIN; CELL LINE; CELL SURVIVAL; CERCOPITHECUS AETHIOPS; ENDOTHELIAL CELLS; FEMALE; HUMANS; MALE; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED BALB C; PHOSPHATIDYLINOSITOL 3-KINASES; RECEPTOR, BRADYKININ B2; SINDBIS VIRUS; VERO CELLS; VIRAL LOAD; VIRAL PROTEINS; VIRUS REPLICATION;

ARBOVIRUS; MUS; SINDBIS VIRUS;

EID: 82355190157     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2011.10.003     Document Type: Article

References (69)

1. Aksamitiene E., Achanta S., Kolch W., Kholodenko B.N., Hoek J.B., Kiyatkin A. Prolactin-stimulated activation of ERK1/2 mitogen-activated protein kinases is controlled by PI3-kinase/Rac/PAK signaling pathway in breast cancer cells. Cell. Signal. 2011, 23(11):1794-1805.
2. Aliberti J., Viola J.P., Vieira-de-Abreu A., Bozza P.T., Sher A., Scharfstein J. Cutting edge: bradykinin induces IL-12 production by dendritic cells: a danger signal that drives Th1 polarization. J. Immunol. 2003, 170(11):5349-5353.
3. Assunção-Miranda I., Bozza M.T., Da Poian A.T. Contribution of macrophage migration inhibitory factor to the pathogenesis of dengue virus infection. J. Med. Virol. 2010, 82(1):164-174.
4. Austin C.E., Faussner A., Robinson H.E., Chakravarty S., Kyle D.J., Bathon J.M., Pround D. Stable expression of the human kinin B1 receptor in Chinese hamster ovary cells. Characterization of ligand binding and effector pathways. J. Biol. Chem. 1997, 272(17):11420-11425.
5. Barnett J.K., Cruse L.W., Proud D. Kinins are generated in nasal secretions during influenza A infections in ferrets. Am. Rev. Respir. Dis. 1990, 142(1):162-166.
6. Bengtson S.H., Eddleston J., Christiansen S.C., Zuraw B.L. Double-stranded RNA increases kinin B1 receptor expression and function in human airway epithelial cells. Int. Immunopharmacol. 2007, 7:1880-1887.
7. Bhoola K.D., Figueroa C.D., Worthy K. Bioregulation of kinins: kallikreins, kininogens, and kininases. Pharmacol. Rev. 1992, 44:1-80.
8. Bledsoe G., Crickman S., Mao J., Xia C.F., Murakami H., Chao L., Chao J. Kallikrein/kinin protects against gentamicin-induced nephrotoxicity by inhibition of inflammation and apoptosis. Nephrol. Dial. Transplant. 2006, 21:624-633.
9. Bovenzi V., Savard M., Morin J.E., Cuerrier C.M., Grandbois M., Gobiel F. Bradykinin protects against brain microvascular endothelial cell death induced by pathophysiological stimuli. J. Cell. Physiol. 2010, 222:168-176.
10. Calabrese L.H., Naides S.J. Viral arthritis. Infect. Dis. Clin. North Am. 2005, 19:963-980.
11. Chai K.X., Chen L.M., Chao J., Chao L. Kallistatin: a novel human serine proteinase inhibitor. Molecular cloning, tissue distribution, and expression in Escherichia coli. J. Biol. Chem. 1993, 268(32):24498-24505.
12. Chatuverdi U.C., Dhawan R., Khanna M., Mathur A. Breakdown of the blood-brain barrier during dengue virus infection mice. J. Gen. Virol. 1991, 72:859-866.
13. Christiansen S.C., Eddleston J., Bengtson S.H., Jenkins G.R., Sarnoff R.B., Turner R.B., Gwaltney J.M., Zuraw B.L. Experimental rhinovirus infection increases human tissue kallikrein activation in allergic subjects. Int. Arch. Allergy Immunol. 2008, 147:299-304.
14. Dhanushkodi N.R., Mohankumar V., Pokkali S., Raju R. Lipopolysaccharide inhibits Sindbis virus-induced IP-10 release in human peripheral blood mononuclear cells. Viral Immunol. 2011, 24(3):237-243.
15. Folkerts G., Vlieger J.W., de Vries A., Faas S., van Der Linde H., Engels F., Jong J.C., Verheyen F.A., Van Heuven-Nolsen D., Nijkamp F.P. Virus- and bradykinin-induced airway hyperresponsiveness in guinea pigs. Am. J. Respir. Crit. Care Med. 2000, 161(5):1666-1671.
16. Fraser J.R. Epidemic polyarthritis and Ross River virus disease. Clin. Rheum. Dis. 1986, 12:369-388.
17. Greco S., Storelli C., Marsigliante S. Protein kinase C (PKC)-/-'mediate the PKC/Akt-dependent phosphorylation of extracellular signal-regulated kinases 1 and 2 in MGCF-7 cells stimulated by bradykinin. J. Endocrinol. 2006, 188:79-89.
18. Griffin D.E. Neuronal cell death in alphavirus encephalomyelitis. Curr. Top. Microbiol. Immunol. 2005, 289:57-77.
19. Griffin D.E., Levine B., Tyor W.R., Tucker P.C., Hardwick J.M. Age-dependent susceptibility to fatal encephalitis: alphavirus infection of neurons. Arch. Virol. Suppl. 1994, 9:31-39.
20. Harris M.B., Ju H., Venema V.J., Liang H., Zou R., Michell B.J., Chen Z.P., Kemp B.E., Venema R.C. Reciprocal phosphorylation and regulation of endothelial nitric-oxide synthase in response to bradykinin stimulation. J. Biol. Chem. 2001, 276:16587-16591.
21. Heitsch H. Bradykinin B2 receptor as a potential therapeutic target. Drug News Perspect. 2000, 13(4):213-225.
22. Ho W.Z., Lai J.P., Li Y., Douglas S.D. HIV enhances Substance P expression in human immune cells. FASEB J. 2002, 16:616-618.
23. Irani D.N., Griffin D.E. Regulation of lymphocyte homing into the brain during viral encephalitis at various stages of infection. J. Immunol. 1996, 156:3850-3857.
24. Irusta P.M., Hardwick J.M. Neuronal apoptosis pathways in Sindbis virus encephalitis. Prog. Mol. Subcell. Biol. 2004, 36:71-93.
25. Jaffar-Bandjee M.C., Das T., Hoarau J.J., Krejbich Trotot P., Denizot M., Ribera A., Roques P., Gasque P. Chikungunya virus takes centre stage in virally induced arthritis: possible cellular and molecular mechanisms to pathogenesis. Microbes Infect. 2009, 11(14-15):1206-1218.
26. Johnson R.T., McFarland H.F., Levy S.E. Age-dependent resistance to viral encephalitis: studies of infections due to Sindbis virus in mice. J. Infect. Dis. 1972, 125:257-262.
27. Kaman W.E., Wolterink A.F., Bader M., Boele L.C., van der Kleij D. The bradykinin B2 receptor in the early immune response against Listeria infection. Med. Microbiol. Immunol. 2009, 198(1):39-46.
28. Kerr D.A., Larsen T., Cook S.H., Fannjiang Y.R., Choi E., Griffin D.E., Hardwick J.M., Irani D.N. BCL-2 and BAX protect adult mice from lethal Sindbis virus infection but do not protect spinal cord motor neurons or prevent paralysis. J. Virol. 2002, 76(20):10393-10400.
29. Kim J.V., Kang S.S., Dustin M.L., McGavern D.B. Myelomonocytic cell recruitment causes fatal CNS vascular injury during acute viral meningitis. Nature 2009, 457(7226):191-195.
30. Krieg T., Qin Q., Philipp S., Alexeyev M.F., Cohen M.V., Downey J.M. Acetylcholine and bradykinin trigger preconditioning in the heart through a pathway that includes Akt and NOS. Am. J. Physiol. Heart Circ. Physiol. 2004, 287(6):H2606-H2611.
31. Labrada L., Liang S.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. J. Virol. 2002, 76(22):11688-11703.
32. Laine M., Luukkainen R., Toivanen A. Sindbis viruses and other alphaviruses as cause of human arthritic disease. J. Intern. Med. 2004, 256:457-471.
33. Lee C.J., Liao C.L., Lin Y.L. Flavivirus activates phosphatidylinositol 3-kinase signaling to block caspase-dependent apoptotic cell death at the early stage of virus infection. J. Virol. 2005, 79(13):8388-8399.
34. Levine B. Apoptosis in viral infections of neurons: a protective or phatologic host response?. Curr. Top. Microbiol. Immunol. 2002, 265:95-118.
35. Lewis J., Oyler G.A., Ueno K., Fannjiang Y.R., Chau B.N., Vornov J., Korsmeyer S.J., Zou S., Hardwick J.M. Inhibition of virus-induced neuronal apoptosis by Bax. Nat. Med. 1999, 5(7):832-835.
36. Li Y., Douglas S.D., Song L., Sun S., Ho W.Z. Substance P enhances HIV-1 replication in latently infected human immune cells. J. Neuroimmunol. 2001, 121:67-75.
37. Lustig S., Jackson A.C., Hahn C.S., Griffin D.E., Strauss E.G., Strauss J.H. Molecular basis of Sindbis virus neurovirulence in mice. J. Virol. 1988, 62:2329-2336.
38. Menke J.G., Borkowski J.A., Bierilo K.K., MacNeil T., Derrick A.W., Schneck K.A., Ransom R.W., Linemeyer D.L., Hess J.F. Expression cloning of human B1 bradykinin receptor. J. Biol. Chem. 1994, 269(34):21583-21586.
39. Monteiro A.C., Schmitz V., Morrot A., de Arruda L.B., Nagajyothi F., Granato A., Pesquero J.B., Müller-Esterl W., Tanowitz H.B., Scharfstein J. Bradykinin B2 Receptors of dendritic cells, acting as sensors of kinins proteolytically released by Trypanosoma cruzi, are critical for the development of protective type-1 responses. PLoS Pathog. 2007, 3(11):e185.
40. Monteiro A.C., Scovino A., Raposo S., Gaze V.M., Cruz C., Svensjö E., Narciso M.S., Colombo A.P., Pesquero J.B., Feres-Filho E., Nguyen K.A., Sroka A., Potempa J., Scharfstein J. Kinin danger signals proteolytically released by gingipain induce Fimbriae-specific IFN-gamma- and IL-17-producing T cells in mice infected intramucosally with Porphyromonas gingivalis. J. Immunol. 2009, 183(6):3700-3711.
41. Naclerio R.M., Proud D., Lichtenstein L.M., Kagey-Sobotka A., Hendley J.O., Sorrentino J., Gwaltney J.M. Kinins are generated during experimental rhinovirus colds. J. Infect. Dis. 1988, 157(1):133-142.
42. Nikolskaia O.V., de A.Lima A.P., Kim Y.V., Lonsdale-Eccles J.D., Scharfstein J., Grab D.J. Blood-brain barrier traversal by African trypanosomes requires calcium signaling induced by parasite cysteine protease. J. Clin. Invest. 2006, 116:2739-2747.
43. Penna C., Mancardi D., Raimondo S., Geuna S., Pagliaro P. The paradigm of postconditioning to protect the heart. J. Cell. Mol. Med. 2008, 12(2):435-458.
44. Prado G.N., Taylor L., Zhou X., Ricupero D., Mierke D.F., Polgar P. Mechanisms regulating the expression, self-maintenance, and signaling-function of the bradykinin B2 and B1 receptors. J. Cell. Phisiol. 2002, 193:275-286.
45. Proud D., Naclerio R.M., Gwaltney J.M., Hendley J.O. Kinins are generated in nasal secretions during natural rhinovirus colds. J. Infect. Dis. 1990, 161(1):120-123.
46. Regoli D., Rhaleb N.E., Dion S., Drapeau G. New selective bradykinin receptor antagonists and bradykinin B2 receptor characterization. Trends Pharmacol. Sci. 1990, 11:156-161.
47. Roberts M.S., Woods A.J., Dale T.C., Van Der Sluijs P., Norman J.C. Protein kinase B/Akt acts via glycogen synthase kinse 3 to regulate recycling of alpha v beta 3 and alpha 5 beta 1 integrins. Mol. Cell. Biol. 2004, 24:1505-1515.
48. Roulston A., Marcellus R.C., Branton P.E. Viruses and apoptosis. Ann. Rev. Microbiol. 1999, 53:577-628.
49. Ryman K.D., Gardner C.L., Meier K.V., Biron C.A., Johnston R.E., Klimstra W.B. Early restriction of alphavirus replication and dissemination contributes to age-dependent attenuation of systemic hyperinflammatory disease. J. Gen. Virol. 2007, 88:518-529.
50. Sammels L.M., Lindsay M.D., Poidinger M., Coelen R.J., Mackenzie J.S. Geographic distribution and evolution of Sindbis virus in Australia. J. Gen. Virol. 1999, 80:739-748.
51. Sarid R., Ben-Moshe T., Kazimirsky G., Weisberg S., Appel E., Kobiler D., Lustig S., Brodie C. vFLIP protects PC-12 cells from apoptosis induced by Sindbis virus: implications for the role of TNF-a. Cell Death Differ. 2001, 8:1224-1231.
52. Stins M.F., Prasadarao N.V., Zhou J., Arditi M., Kim K.S. Bovine brain microvascular endothelial cells transfected with SV40-large T antigen: development of an immortalized cell line to study pathophysiology of CNS disease. In Vitro Cell. Dev. Biol. Anim. 1997, 33:243-247.
53. Strauss J.H., Strauss E.G. The alphaviruses: gene expression, replication and evolution. Microbiol. Rev. 1994, 58:491-562.
54. Teodoro J.G., Branton P.E. Regulation of apoptosis by viral gene products. J. Virol. 1997, 71:1739-1746.
55. Trgovcich J., Aronson J.F., Eldridge J.C., Johnston R.E. TNF-α, interferon, and stress response induction as a function of age-related susceptibility to fatal Sindbis virus infection of mice. Virology 1999, 263:339-348.
56. Tripp R.A., Moore D., Winter J., Anderson L.J. Respiratory syncytial virus infection and G and/or SH protein expression contribute to Substance P, which mediates inflammation and enhanced pulmonary disease in BALB/c mice. J. Virol. 2000, 74(4):1614-1622.
57. Tseng J.C., Levin B., Hurtado A., Yee H., Perez Castro I., Jimenez M., Shamamian P., Jin R., Novick R.P., Pellicer A., Meruelo D. Systemic tumor targeting and killing by Sindbis viral vectors. Nat. Biotechnol. 2004, 22(1):70-77.
58. Valarcher J.F., Furze J., Wyld S.G., Cook R., Zimmer G., Herrler G., Taylor G. Bovine respiratory syncytial virus lacking the virokinin or with a mutation in furin cleavage site RA(R/K)R109 induces less pulmonary inflammation without impeding the induction of protective immunity in calves. J. Gen. Virol. 2006, 87:1659-1667.
59. Valenti C., Giuliani S., Cialdai C., Tramontana M., Maggi C. Anti-inflammatory synergy of MEN16132, a kinin B(2) receptor antagonist, and dexamethasone in carrageenan-induced knee joint arthritis in rats. Br. J. Pharmacol. 2010, 161(7):1616-1627.
60. Van der Meijden P.E., Heemsherk J.W. Polyphosphates: a link between platelet activation, intrinsic coagulation and inflammation?. Cell 2010, 139(6):1143-1156.
61. Wang C.R., Chen S.Y., Wu C.L., Liu M.F., Jin Y.T., Chao L., Chao J. Prophylactic adenovirus-mediated human kallistatin gene therapy suppresses rat arthritis by inhibiting angiogenesis and inflammation. Arthritis Rheum. 2005, 52(4):1319-1324.
62. Wang H., Blair C.D., Olson K.E., Clem R.J. Effects of inducing or inhibiting apoptosis on Sindbis virus replication in mosquito cells. J. Gen. Virol. 2008, 89(11):2651-2661.
63. Wang S., Dai Y., Fukuoka T., Yamanaka H., Kobayashi K., Obata K., Cui X., Tominaga M., Noguchi K. Phospholipase C and protein kinase A mediate bradykinin sensitization of TRPA1: a molecular mechanism of inflammatory pain. Brain 2008, 131(5):1241-1251.
64. Wollmann G., Tattersall P., van den Pol A.N. Targeting human glioblastoma cells: comparison of nine viruses with oncolytic potential. J. Virol. 2005, 79(10):6005-6022.
65. Xia C.F., Yin H., Borlongan C.V., Chao L., Chao J. Kallikrein gene transfer protects against ischemic stroke by promoting glial cell migration and inhibiting apoptosis. Hypertension 2004, 43(2):452-459.
66. Yao Y.Y., Yin H., Shen B., Smith R.S., Liu Y., Gao L., Chao L., Chao J. Tissue kallikrein promotes neovascularization and improves cardiac function by the Akt-glycogen synthase kinase-3beta pathway. Cardiovas. Res. 2008, 80:354-364.
67. Yin H., Chao L., Chao J. Kallikrein/Kinin protects against myocardial apoptosis after ischemia/reperfusion via Akt-glycogen synthase kinase-3 and Akt-Bad14-3-3 signaling pathways. J. Biol. Chem. 2005, 280(9):8022-8030.
68. Zhang W., Xu W., Xiong S. Macrophage differentiation and polarization via phosphatidylinositol 3-kinase/Akt-ERK signaling pathway conferred by serum amyloid P component. J. Immunol. 2011, 187(4):1764-1777.
69. Zimmer G., Rohn M., McGregor G.P., Schemann M., Conzelmann K.K., Herrler G. Virokinin, a bioactive peptide of the tachykinin family, is released from the fusion protein of bovine respiratory syncytial virus. J. Biol. Chem. 2003, 278(47):46854-46861.