Streptococcal M1 protein triggers chemokine formation, neutrophil infiltration, and lung injury in an NFAT-dependent manner

Journal of Leukocyte Biology

Volumn 97, Issue 6, 2015, Pages 1003-1010

  Zhang, Songen ^a   Zhang, Su ^a   Garcia Vaz, Eliana ^a   Herwald, Heiko ^b   Gomez, Maria F ^a   Thorlacius, Henrik ^a  

^a LUND UNIVERSITY   (Sweden)

^b LUND UNIVERSITY   (Sweden)

Author keywords

Infection; Leukocytes; Migration; Sepsis

Indexed keywords

A 285222; ALPHA CHEMOKINE; BACTERIAL PROTEIN; CD11B ANTIGEN; PROTEIN INHIBITOR; RESPIRATORY TRACT AGENT; STREPTOCOCCAL M1 PROTEIN; TRANSCRIPTION FACTOR NFAT; UNCLASSIFIED DRUG; BACTERIAL ANTIGEN; CARRIER PROTEIN; LUCIFERASE; OUTER MEMBRANE PROTEIN; PYRAZOLE DERIVATIVE; STREPTOCOCCAL M PROTEIN;

ACUTE LUNG INJURY; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE RESPONSE; FEMALE; FLOW CYTOMETRY; HISTOLOGY; LEUKOCYTE ACTIVATION; LEUKOCYTE COUNT; LEUKOCYTE DIFFERENTIAL COUNT; LIVER; LUNG; LUNG EDEMA; LUNG INFILTRATE; MOUSE; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPLEEN; STREPTOCOCCUS INFECTION; STREPTOCOCCUS PYOGENES; TRANSCRIPTION REGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; CHEMICALLY INDUCED; CHEMISTRY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; INTRAVENOUS DRUG ADMINISTRATION; LUNG INJURY; PATHOLOGY; PULMONARY EDEMA; REPORTER GENE; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

MUS; STREPTOCOCCUS PYOGENES;

ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL OUTER MEMBRANE PROTEINS; CARRIER PROTEINS; CHEMOKINES, CXC; FEMALE; GENE EXPRESSION REGULATION; GENES, REPORTER; HOST-PATHOGEN INTERACTIONS; INJECTIONS, INTRAVENOUS; LIVER; LUCIFERASES; LUNG; LUNG INJURY; MACROPHAGE-1 ANTIGEN; MICE; MICE, TRANSGENIC; NEUTROPHIL INFILTRATION; NFATC TRANSCRIPTION FACTORS; PULMONARY EDEMA; PYRAZOLES; SIGNAL TRANSDUCTION; SPLEEN; STREPTOCOCCUS PYOGENES;

EID: 84930240561     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.3HI0214-123RR     Document Type: Article

References (47)

1. Martin, G. S. (2012) Sepsis, severe sepsis and septic shock: changes in incidence, pathogens and outcomes. Expert Rev. Anti Infect. Ther. 10, 701–706.
2. Angus, D. C., van der Poll, T. (2013) Severe sepsis and septic shock. N. Engl. J. Med. 369, 840–851.
3. Cunningham, M. W. (2000) Pathogenesis of group A streptococcal infections. Clin. Microbiol. Rev. 13, 470–511.
4. Herwald, H., Cramer, H., Mörgelin, M., Russell, W., Sollenberg, U., Norrby-Teglund, A., Flodgaard, H., Lindbom, L., Björck, L. (2004) M Protein, a classical bacterial virulence determinant, forms complexes with fibrinogen that induce vascular leakage. Cell 116, 367–379.
5. Påhlman, L. I., Mörgelin, M., Eckert, J., Johansson, L., Russell, W., Riesbeck, K., Soehnlein, O., Lindbom, L., Norrby-Teglund, A., Schumann, R. R., Björck, L., Herwald, H. (2006) Streptococcal M protein: a multipotent and powerful inducer of inflammation. J. Immunol. 177, 1221–1228.
6. Soehnlein, O., Oehmcke, S., Ma, X., Rothfuchs, A. G., Frithiof, R., van Rooijen, N., Mörgelin, M., Herwald, H., Lindbom, L. (2008) Neutrophil degranulation mediates severe lung damage triggered by streptococcal M1 protein. Eur. Respir. J. 32, 405–412.
7. Kamochi, M., Kamochi, F., Kim, Y. B., Sawh, S., Sanders, J. M., Sarembock, I., Green, S., Young, J. S., Ley, K., Fu, S. M., Rose, Jr., C. E. (1999) P-selectin and ICAM-1 mediate endotoxin-induced neutrophil recruitment and injury to the lung and liver. Am. J. Physiol. 277, L310–L319.
8. Grommes, J., Soehnlein, O. (2011) Contribution of neutrophils to acute lung injury. Mol. Med. 17, 293–307.
9. Stevens, D. L. (1995) Streptococcal toxic-shock syndrome: spectrum of disease, pathogenesis, and new concepts in treatment. Emerg. Infect. Dis. 1, 69–78.
10. Asaduzzaman, M., Zhang, S., Lavasani, S., Wang, Y., Thorlacius, H. (2008) LFA-1 and MAC-1 mediate pulmonary recruitment of neutrophils and tissue damage in abdominal sepsis. Shock 30, 254–259.
11. Hasan, Z., Palani, K., Rahman, M., Thorlacius, H. (2011) Targeting CD44 expressed on neutrophils inhibits lung damage in abdominal sepsis. Shock 35, 567–572.
12. Klintman, D., Li, X., Thorlacius, H. (2004) Important role of P-selectin for leukocyte recruitment, hepatocellular injury, and apoptosis in endotoxemic mice. Clin. Diagn. Lab. Immunol. 11, 56–62.
13. Zhang, S., Song, L., Wang, Y., Herwald, H., Thorlacius, H. (2013) Targeting CD162 protects against streptococcal M1 protein-evoked neutrophil recruitment and lung injury. Am. J. Physiol. Lung Cell. Mol. Physiol. 305, L756–L763.
14. Zhang, X. W., Liu, Q., Wang, Y., Thorlacius, H. (2001) CXC chemokines, MIP-2 and KC, induce P-selectin-dependent neutrophil rolling and extravascular migration in vivo. Br. J. Pharmacol. 133, 413–421.
15. Zhang, S., Zhang, S., Rahman, M., Herwald, H., Thorlacius, H. (2011) Streptococcal M1 protein-induced lung injury is independent of platelets in mice. Shock 35, 86–91.
16. Feske, S. (2007) Calcium signalling in lymphocyte activation and disease. Nat. Rev. Immunol. 7, 690–702.
17. Li, H., Rao, A., Hogan, P. G. (2011) Interaction of calcineurin with substrates and targeting proteins. Trends Cell Biol. 21, 91–103.
18. Rusnak, F., Mertz, P. (2000) Calcineurin: form and function. Physiol. Rev. 80, 1483–1521.
19. Okamura, H., Aramburu, J., García-Rodríguez, C., Viola, J. P., Raghavan, A., Tahiliani, M., Zhang, X., Qin, J., Hogan, P. G., Rao, A. (2000) Concerted dephosphorylation of the transcription factor NFAT1 induces a conformational switch that regulates transcriptional activity. Mol. Cell 6, 539–550.
20. Crabtree, G. R., Olson, E. N. (2002) NFAT signaling: choreographing the social lives of cells. Cell 109 (Suppl), S67–S79.
21. Horsley, V., Pavlath, G. K. (2002) NFAT: ubiquitous regulator of cell differentiation and adaptation. J. Cell Biol. 156, 771–774.
22. Mancini, M., Toker, A. (2009) NFAT proteins: emerging roles in cancer progression. Nat. Rev. Cancer 9, 810–820.
23. Shaw, J. P., Utz, P. J., Durand, D. B., Toole, J. J., Emmel, E. A., Crabtree, G. R. (1988) Identification of a putative regulator of early T cell activation genes. Science 241, 202–205.
24. Rao, A., Luo, C., Hogan, P. G. (1997) Transcription factors of the NFAT family: regulation and function. Annu. Rev. Immunol. 15, 707–747.
25. Wilkins, B. J., Dai, Y. S., Bueno, O. F., Parsons, S. A., Xu, J., Plank, D. M., Jones, F., Kimball, T. R., Molkentin, J. D. (2004) Calcineurin/NFAT coupling participates in pathological, but not physiological, cardiac hypertrophy. Circ. Res. 94, 110–118.
26. Collin, M., Olsén, A. (2000) Generation of a mature streptococcal cysteine proteinase is dependent on cell wall-anchored M1 protein. Mol. Microbiol. 36, 1306–1318.
27. Awla, D., Zetterqvist, A. V., Abdulla, A., Camello, C., Berglund, L. M., Spegel, P., Pozo, M. J., Camello, P. J., Regner, S., Gomez, M. F., Thorlacius, H. (2012) NFATc3 regulates trypsinogen activation, neutrophil recruitment, and tissue damage in acute pancreatitis in mice. Gastroenterology 143, 1352–1360.e1–7.
28. Nilsson, L. M., Sun, Z. W., Nilsson, J., Nordström, I., Chen, Y. W., Molkentin, J. D., Wide-Swensson, D., Hellstrand, P., Lydrup, M. L., Gomez, M. F. (2007) Novel blocker of NFAT activation inhibits IL-6 production in human myometrial arteries and reduces vascular smooth muscle cell proliferation. Am. J. Physiol. Cell Physiol. 292, C1167–C1178.
29. Hasan, Z., Rahman, M., Palani, K., Syk, I., Jeppsson, B., Thorlacius, H. (2013) Geranylgeranyl transferase regulates CXC chemokine formation in alveolar macrophages and neutrophil recruitment in septic lung injury. Am. J. Physiol. Lung Cell. Mol. Physiol. 304, L221–L229.
30. Borzone, G., Liberona, L., Olmos, P., Sáez, C., Meneses, M., Reyes, T., Moreno, R., Lisboa, C. (2007) Rat and hamster species differences in susceptibility to elastase-induced pulmonary emphysema relate to differences in elastase inhibitory capacity. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293, R1342–R1349.
31. Trevillyan, J. M., Chiou, X. G., Chen, Y. W., Ballaron, S. J., Sheets, M. P., Smith, M. L., Wiedeman, P. E., Warrior, U., Wilkins, J., Gubbins, E. J., Gagne, G. D., Fagerland, J., Carter, G. W., Luly, J. R., Mollison, K. W., Djuric, S. W. (2001) Potent inhibition of NFAT activation and T cell cytokine production by novel low molecular weight pyrazole compounds. J. Biol. Chem. 276, 48118–48126.
32. Zhang, S., Rahman, M., Zhang, S., Herwald, H., Qi, Z., Jeppsson, B., Thorlacius, H. (2012) Streptococcal M1 protein-provoked CXC chemokine formation, neutrophil recruitment and lung damage are regulated by Rho-kinase signaling. J. Innate Immun. 4, 399–408.
33. Zhang, S., Rahman, M., Zhang, S., Jeppsson, B., Herwald, H., Thorlacius, H. (2012) Streptococcal m1 protein triggers farnesyltransferasedependent formation of CXC chemokines in alveolar macrophages and neutrophil infiltration of the lungs. Infect. Immun. 80, 3952–3959.
34. Zhang, S., Rahman, M., Zhang, S., Qi, Z., Herwald, H., Thorlacius, H. (2011) Simvastatin regulates CXC chemokine formation in streptococcal M1 protein-induced neutrophil infiltration in the lung. Am. J. Physiol. Lung Cell. Mol. Physiol. 300, L930–L939.
35. Zhang, S., Rahman, M., Zhang, S., Wang, Y., Herwald, H., Jeppsson, B., Thorlacius, H. (2012) p38 Mitogen-activated protein kinase signaling regulates streptococcal M1 protein-induced neutrophil activation and lung injury. J. Leukoc. Biol. 91, 137–145.
36. Graef, I. A., Chen, F., Chen, L., Kuo, A., Crabtree, G. R. (2001) Signals transduced by Ca(2+)/calcineurin and NFATc3/c4 pattern the developing vasculature. Cell 105, 863–875.
37. Graef, I. A., Wang, F., Charron, F., Chen, L., Neilson, J., Tessier-Lavigne, M., Crabtree, G. R. (2003) Neurotrophins and netrins require calcineurin/NFAT signaling to stimulate outgrowth of embryonic axons. Cell 113, 657–670.
38. Olson, E. N., Williams, R. S. (2000) Calcineurin signaling and muscle remodeling. Cell 101, 689–692.
39. Feske, S., Okamura, H., Hogan, P. G., Rao, A. (2003) Ca2+/calcineurin signalling in cells of the immune system. Biochem. Biophys. Res. Commun. 311, 1117–1132.
40. Zetterqvist, A. V., Berglund, L. M., Blanco, F., Garcia-Vaz, E., Wigren, M., Dunér, P., Andersson, A. M., To, F., Spegel, P., Nilsson, J., Bengtsson, E., Gomez, M. F. (2013) Inhibition of nuclear factor of activated T-cells (NFAT) suppresses accelerated atherosclerosis in diabetic mice. PLoS ONE 8, e65020.
41. Ghosh, S., Koralov, S. B., Stevanovic, I., Sundrud, M. S., Sasaki, Y., Rajewsky, K., Rao, A., Müller, M. R. (2010) Hyperactivation of nuclear factor of activated T cells 1 (NFAT1) in T cells attenuates severity of murine autoimmune encephalomyelitis. Proc. Natl. Acad. Sci. USA 107, 15169–15174.
42. Zhang, S., Hwaiz, R., Rahman, M., Herwald, H., Thorlacius, H. (2014) Ras regulates alveolar macrophage formation of CXC chemokines and neutrophil activation in streptococcal M1 protein-induced lung injury. Eur. J. Pharmacol. 733, 45–53.
43. Menezes, G. B., Lee, W. Y., Zhou, H., Waterhouse, C. C., Cara, D. C., Kubes, P. (2009) Selective down-regulation of neutrophil Mac-1 in endotoxemic hepatic microcirculation via IL-10. J. Immunol. 183, 7557–7568.
44. Corbel, M., Lagente, V., Théret, N., Germain, N., Clément, B., Boichot, E. (1999) Comparative effects of betamethasone, cyclosporin and nedocromil sodium in acute pulmonary inflammation and metalloproteinase activities in bronchoalveolar lavage fluid from mice exposed to lipopolysaccharide. Pulm. Pharmacol. Ther. 12, 165–171.
45. Chiu, C. C., Huang, Y. T., Chuang, H. L., Chen, H. H., Chung, T. C. (2009) Co-exposure of lipopolysaccharide and Pseudomonas aeruginosa exotoxin A-induced multiple organ injury in rats. Immunopharmacol. Immunotoxicol. 31, 75–82.
46. Wesselborg, S., Fruman, D. A., Sagoo, J. K., Bierer, B. E., Burakoff, S. J. (1996) Identification of a physical interaction between calcineurin and nuclear factor of activated T cells (NFATp). J. Biol. Chem. 271, 1274–1277.
47. Nilsson-Berglund, L. M., Zetterqvist, A. V., Nilsson-Ohman, J., Sigvardsson, M., González Bosc, L. V., Smith, M. L., Salehi, A., Agardh, E., Fredrikson, G. N., Agardh, C. D., Nilsson, J., Wamhoff, B. R., Hultgårdh-Nilsson, A., Gomez, M. F. (2010) Nuclear factor of activated T cells regulates osteopontin expression in arterial smooth muscle in response to diabetes-induced hyperglycemia. Arterioscler. Thromb. Vasc. Biol. 30, 218–224.