The C2 fragment from Neisseria meningitidis antigen NHBA increases endothelial permeability by destabilizing adherens junctions

Cellular Microbiology

Volumn 16, Issue 6, 2014, Pages 925-937

  Casellato, Alessandro ^a   Rossi Paccani, Silvia ^b   Barrile, Riccardo ^b   Bossi, Fleur ^c   Ciucchi, Laura ^b   Codolo, Gaia ^a,d   Pizza, Mariagrazia ^b   Aricò, Beatrice ^b   De Bernard, Marina ^a,d  

^a VENETIAN INSTITUTE OF MOLECULAR MEDICINE   (Italy)

^b NOVARTIS VACCINES AND DIAGNOSTICS   (Italy)

^c UNIVERSITY OF TRIESTE   (Italy)

^d UNIVERSITY OF PADOVA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ANTIGEN; NEISSERIAL HEPARIN BINDING ANTIGEN; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL CADHERIN; VIRULENCE FACTOR;

ANIMAL CELL; ARTICLE; BLOOD VESSEL PERMEABILITY; CELL JUNCTION; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; ENDOCYTOSIS; HUMAN; HUMAN CELL; INTERNALIZATION; MENINGOCOCCEMIA; MICROVASCULAR ENDOTHELIAL CELL; MICROVASCULATURE; MITOCHONDRION; MOUSE; NEISSERIA MENINGITIDIS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; VASCULAR ENDOTHELIUM; CELL LINE; DRUG EFFECTS; ENDOTHELIUM CELL; GENETICS; METABOLISM; PERMEABILITY; PHYSIOLOGY;

BACTERIA (MICROORGANISMS); NEISSERIA MENINGITIDIS;

ADHERENS JUNCTIONS; ANTIGENS, BACTERIAL; CELL LINE; ENDOTHELIAL CELLS; HUMANS; NEISSERIA MENINGITIDIS; PERMEABILITY; VIRULENCE FACTORS;

EID: 84900542541     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12250     Document Type: Article

References (41)

1. Andriopoulou, P., Navarro, P., Zanetti, A., Lampugnani, M.G., and Dejana, E. (1999) Histamine induces tyrosine phosphorylation of endothelial cell-to-cell adherens junctions. Arterioscler Thromb Vasc Biol 19: 2286-2297.
2. Belousov, V.V., Fradkov, A.F., Lukyanov, K.A., Staroverov, D.B., Shakhbazov, K.S., Terskikh, A.V., and Lukyanov, S. (2006) Genetically encoded fluorescent indicator for intracellular hydrogen peroxide. Nat Methods 3: 281-286.
3. Borgese, N., Gazzoni, I., Barberi, M., Colombo, S., and Pedrazzini, E. (2001) Targeting of a tail-anchored protein to endoplasmic reticulum and mitochondrial outer membrane by independent but competing pathways. Mol Biol Cell 12: 2482-2496.
4. Boveris, A., Oshino, N., and Chance, B. (1972) The cellular production of hydrogen peroxide. Biochem J 128: 617-630.
5. Caesar, N.M., Myers, K.A., and Fan, X. (2013) Neisseria meningitidis serogroup B vaccine development. Microb Pathog 57: 33-40.
6. Chance, B., Sies, H., and Boveris, A. (1979) Hydroperoxide metabolism in mammalian organs. Physiol Rev 59: 527-605.
7. Chen, T., Swanson, J., Wilson, J., and Belland, R.J. (1995) Heparin protects Opa+ Neisseria gonorrhoeae from the bactericidal action of normal human serum. Infect Immun 63: 1790-1795.
8. Coureuil, M., Mikaty, G., Miller, F., Lecuyer, H., Bernard, C., Bourdoulous, S., etal. (2009) Meningococcal type IV pili recruit the polarity complex to cross the brain endothelium. Science 325: 83-87.
9. Coureuil, M., Lecuyer, H., Scott, M.G., Boularan, C., Enslen, H., Soyer, M., etal. (2010) Meningococcus Hijacks a beta2-adrenoceptor/beta-Arrestin pathway to cross brain microvasculature endothelium. Cell 143: 1149-1160.
10. Coureuil, M., Join-Lambert, O., Lecuyer, H., Bourdoulous, S., Marullo, S., and Nassif, X. (2013) Pathogenesis of meningococcemia. Cold Spring Harb Perspect Med 3: pii: a012393. doi: 10.1101/cshperspect.a012393.
11. Donnelly, J., Medini, D., Boccadifuoco, G., Biolchi, A., Ward, J., Frasch, C., etal. (2010) Qualitative and quantitative assessment of meningococcal antigens to evaluate the potential strain coverage of protein-based vaccines. Proc Natl Acad Sci USA 107: 19490-19495.
12. Dupin, N., Lecuyer, H., Carlotti, A., Poyart, C., Coureuil, M., Chanal, J., etal. (2012) Chronic meningococcemia cutaneous lesions involve meningococcal perivascular invasion through the remodeling of endothelial barriers. Clin Infect Dis 54: 1162-1165.
13. Gallagher, J.T., and Lyon, M. (2000) Molecular structure of heparan sulfate and interactions with growth factors and morphogens. In Proteoglycans: Structure, Biology and Molecular Interactions. Iozzo, R.V. (ed.). New York, NY: Marcel Dekker Inc. pp. 27-59.
14. Gavard, J., and Gutkind, J.S. (2006) VEGF controls endothelial-cell permeability by promoting the beta-arrestin-dependent endocytosis of VE-cadherin. Nat Cell Biol 8: 1223-1234.
15. Giannoni, E., Taddei, M.L., and Chiarugi, P. (2010) Src redox regulation: again in the front line. Free Radic Biol Med 49: 516-527.
16. Grazia Lampugnani, M., Zanetti, A., Corada, M., Takahashi, T., Balconi, G., Breviario, F., etal. (2003) Contact inhibition of VEGF-induced proliferation requires vascular endothelial cadherin, beta-catenin, and the phosphatase DEP-1/CD148. J Cell Biol 161: 793-804.
17. von Heijne, G. (1986) Mitochondrial targeting sequences may form amphiphilic helices. EMBO J 5: 1335-1342.
18. Iozzo, R.V. (1998) Matrix proteoglycans: from molecular design to cellular function. Annu Rev Biochem 67: 609-652.
19. Lampugnani, M.G., Zanetti, A., Breviario, F., Balconi, G., Orsenigo, F., Corada, M., etal. (2002) VE-cadherin regulates endothelial actin activating Rac and increasing membrane association of Tiam. Mol Biol Cell 13: 1175-1189.
20. Lee, M., Choy, W.C., and Abid, M.R. (2011) Direct sensing of endothelial oxidants by vascular endothelial growth factor receptor-2 and c-Src. PLoS ONE 6: e28454.
21. Loschen, G., Flohe, L., and Chance, B. (1971) Respiratory chain linked H(2)O(2) production in pigeon heart mitochondria. FEBS Lett 18: 261-264.
22. Lukyanov, K.A., and Belousov, V.V. (2013) Genetically encoded fluorescent redox sensors. Biochim Biophys Acta 1840: 745-756.
23. Melican, K., Michea Veloso, P., Martin, T., Bruneval, P., and Dumenil, G. (2013) Adhesion of Neisseria meningitidis to dermal vessels leads to local vascular damage and purpura in a humanized mouse model. PLoS Pathog 9: e1003139.
24. Menozzi, F.D., Rouse, J.H., Alavi, M., Laude-Sharp, M., Muller, J., Bischoff, R., etal. (1996) Identification of a heparin-binding hemagglutinin present in mycobacteria. J Exp Med 184: 993-1001.
25. Mitchell, D.J., Kim, D.T., Steinman, L., Fathman, C.G., and Rothbard, J.B. (2000) Polyarginine enters cells more efficiently than other polycationic homopolymers. J Pept Res 56: 318-325.
26. Monaghan-Benson, E., and Burridge, K. (2009) The regulation of vascular endothelial growth factor-induced microvascular permeability requires Rac and reactive oxygen species. J Biol Chem 284: 25602-25611.
27. Morand, P.C., Bille, E., Morelle, S., Eugene, E., Beretti, J.L., Wolfgang, M., etal. (2004) Type IV pilus retraction in pathogenic Neisseria is regulated by the PilC proteins. EMBO J 23: 2009-2017.
28. Mukhopadhyay, P., Rajesh, M., Hasko, G., Hawkins, B.J., Madesh, M., and Pacher, P. (2007) Simultaneous detection of apoptosis and mitochondrial superoxide production in live cells by flow cytometry and confocal microscopy. Nat Protoc 2: 2295-2301.
29. Nakase, I., Okumura, S., Katayama, S., Hirose, H., Pujals, S., Yamaguchi, H., etal. (2012) Transformation of an antimicrobial peptide into a plasma membrane-permeable, mitochondria-targeted peptide via the substitution of lysine with arginine. Chem Commun (Camb) 48: 11097-11099.
30. Orsenigo, F., Giampietro, C., Ferrari, A., Corada, M., Galaup, A., Sigismund, S., etal. (2012) Phosphorylation of VE-cadherin is modulated by haemodynamic forces and contributes to the regulation of vascular permeability in vivo. Nat Commun 3: 1208.
31. Ovstebo, R., Brandtzaeg, P., Brusletto, B., Haug, K.B., Lande, K., Hoiby, E.A., and Kierulf, P. (2004) Use of robotized DNA isolation and real-time PCR to quantify and identify close correlation between levels of Neisseria meningitidis DNA and lipopolysaccharides in plasma and cerebrospinal fluid from patients with systemic meningococcal disease. J Clin Microbiol 42: 2980-2987.
32. Paterson, A.D., Parton, R.G., Ferguson, C., Stow, J.L., and Yap, A.S. (2003) Characterization of E-cadherin endocytosis in isolated MCF-7 and chinese hamster ovary cells: the initial fate of unbound E-cadherin. J Biol Chem 278: 21050-21057.
33. Pathan, N., Faust, S.N., and Levin, M. (2003) Pathophysiology of meningococcal meningitis and septicaemia. Arch Dis Child 88: 601-607.
34. Serruto, D., Spadafina, T., Ciucchi, L., Lewis, L.A., Ram, S., Tontini, M., etal. (2010) Neisseria meningitidis GNA2132, a heparin-binding protein that induces protective immunity in humans. Proc Natl Acad Sci USA 107: 3770-3775.
35. Serruto, D., Bottomley, M.J., Ram, S., Giuliani, M.M., and Rappuoli, R. (2012) The new multicomponent vaccine against meningococcal serogroup B, 4CMenB: immunological, functional and structural characterization of the antigens. Vaccine 30 (Suppl. 2): B87-B97.
36. Shen, W., Li, S., Chung, S.H., Zhu, L., Stayt, J., Su, T., etal. (2011) Tyrosine phosphorylation of VE-cadherin and claudin-5 is associated with TGF-beta1-induced permeability of centrally derived vascular endothelium. Eur J Cell Biol 90: 323-332.
37. Vincent, P.A., Xiao, K., Buckley, K.M., and Kowalczyk, A.P. (2004) VE-cadherin: adhesion at arm's length. Am J Physiol Cell Physiol 286: C987-C997.
38. de Vries, F.P., Cole, R., Dankert, J., Frosch, M., and van Putten, J.P. (1998) Neisseria meningitidis producing the Opc adhesin binds epithelial cell proteoglycan receptors. Mol Microbiol 27: 1203-1212.
39. Weis, S.M., and Cheresh, D.A. (2005) Pathophysiological consequences of VEGF-induced vascular permeability. Nature 437: 497-504.
40. Xiao, K., Allison, D.F., Kottke, M.D., Summers, S., Sorescu, G.P., Faundez, V., and Kowalczyk, A.P. (2003) Mechanisms of VE-cadherin processing and degradation in microvascular endothelial cells. J Biol Chem 278: 19199-19208.
41. Zanetti, A., Lampugnani, M.G., Balconi, G., Breviario, F., Corada, M., Lanfrancone, L., and Dejana, E. (2002) Vascular endothelial growth factor induces SHC association with vascular endothelial cadherin: a potential feedback mechanism to control vascular endothelial growth factor receptor-2 signaling. Arterioscler Thromb Vasc Biol 22: 617-622.