Endothelial MKK3 is a critical mediator of lethal murine endotoxemia and acute lung injury

Journal of Immunology

Volumn 190, Issue 3, 2013, Pages 1264-1275

  Mannam, Praveen ^a   Zhang, Xuchen ^a   Shan, Peiying ^a   Zhang, Yi ^a   Shinn, Amanda S ^a   Zhang, Yitao ^a   Lee, Patty J ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; LIPOPOLYSACCHARIDE; MALONALDEHYDE; MITOGEN ACTIVATED PROTEIN KINASE KINASE 3; MYELOPEROXIDASE; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR AP 1; VASCULAR CELL ADHESION MOLECULE 1;

ACUTE LUNG INJURY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CELL DEATH; CELL TRANSPORT; CONTROLLED STUDY; DISEASE MODEL; ENDOTHELIUM CELL; ENDOTOXEMIA; ENZYME DEFICIENCY; INFLAMMATORY CELL; LUNG ENDOTHELIUM; LUNG LAVAGE; LUNG PARENCHYMA; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEPSIS;

ACUTE LUNG INJURY; ANIMALS; APOPTOSIS; BRONCHOALVEOLAR LAVAGE FLUID; CHEMOTAXIS, LEUKOCYTE; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; ENDOTOXEMIA; INTERCELLULAR ADHESION MOLECULE-1; LIPOPOLYSACCHARIDES; LUNG; MAP KINASE KINASE 3; MICE; MICE, KNOCKOUT; MITOCHONDRIA; NEUTROPHIL ACTIVATION; NF-KAPPA B; PERITONITIS; RADIATION CHIMERA; REACTIVE OXYGEN SPECIES; RNA, SMALL INTERFERING; SEPSIS; TRANSCRIPTION FACTOR AP-1;

EID: 84872724089     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1202012     Document Type: Article

References (49)

1. Angus, D. C., W. T. Linde-Zwirble, J. Lidicker, G. Clermont, J. Carcillo, and M. R. Pinsky. 2001. Epidemiology of severe sepsis in the United States: Analysis of incidence, outcome, and associated costs of care. Crit. Care Med. 29: 1303-1310. (Pubitemid 32641789)
2. Ono, K., and J. Han. 2000. The p38 signal transduction pathway: Activation and function. Cell. Signal. 12: 1-13. (Pubitemid 30017963)
3. Han, J., J. D. Lee, L. Bibbs, and R. J. Ulevitch. 1994. A MAP kinase targeted by endotoxin and hyperosmolarity in mammalian cells. Science 265: 808-811. (Pubitemid 24266145)
4. Han, J., X. Wang, Y. Jiang, R. J. Ulevitch, and S. Lin. 1997. Identification and characterization of a predominant isoform of humanMKK3. FEBS Lett. 403: 19-22. (Pubitemid 27079801)
5. Dérijard, B., J. Raingeaud, T. Barrett, I. H. Wu, J. Han, R. J. Ulevitch, and R. J. Davis. 1995. Independent human MAP-kinase signal transduction pathways defined by MEK and MKK isoforms. Science 267: 682-685.
6. Wysk, M., D. D. Yang, H. T. Lu, R. A. Flavell, and R. J. Davis. 1999. Requirement of mitogen-activated protein kinase kinase 3 (MKK3) for tumor necrosis factor-induced cytokine expression. Proc. Natl. Acad. Sci. USA 96: 3763-3768. (Pubitemid 29168984)
7. Lu, H. T., D. D. Yang, M. Wysk, E. Gatti, I. Mellman, R. J. Davis, and R. A. Flavell. 1999. Defective IL-12 production in mitogen-activated protein (MAP) kinase kinase 3 (Mkk3)-deficient mice. EMBO J. 18: 1845-1857. (Pubitemid 29158528)
8. Pellizzari, R., C. Guidi-Rontani, G. Vitale, M. Mock, and C. Montecucco. 1999. Anthrax lethal factor cleaves MKK3 in macrophages and inhibits the LPS/ IFNgamma-induced release of NO and TNFalpha. FEBS Lett. 462: 199-204.
9. Zhang, X., P. Shan, J. Alam, R. J. Davis, R. A. Flavell, and P. J. Lee. 2003. Carbon monoxide modulates Fas/Fas ligand, caspases, and Bcl-2 family proteins via the p38alpha mitogen-activated protein kinase pathway during ischemiareperfusion lung injury. J. Biol. Chem. 278: 22061-22070. (Pubitemid 36792616)
10. Zhang, X., P. Shan, J. Alam, X. Y. Fu, and P. J. Lee. 2005. Carbon monoxide differentially modulates STAT1 and STAT3 and inhibits apoptosis via a phosphatidylinositol 3-kinase/Akt and p38 kinase-dependent STAT3 pathway during anoxia-reoxygenation injury. J. Biol. Chem. 280: 8714-8721. (Pubitemid 40409558)
11. Otterbein, L. E., S. L. Otterbein, E. Ifedigbo, F. Liu, D. E. Morse, C. Fearns, R. J. Ulevitch, R. Knickelbein, R. A. Flavell, and A. M. Choi. 2003. MKK3 mitogen-activated protein kinase pathway mediates carbon monoxide-induced protection against oxidant-induced lung injury. Am. J. Pathol. 163: 2555-2563. (Pubitemid 37466496)
12. Dolinay, T., W. Wu, N. Kaminski, E. Ifedigbo, A. M. Kaynar, M. Szilasi, S. C. Watkins, S. W. Ryter, A. Hoetzel, and A. M. Choi. 2008. Mitogen-activated protein kinases regulate susceptibility to ventilator-induced lung injury. PLoS One 3: E1601.
13. Lim, A. K., D. J. Nikolic-Paterson, F. Y. Ma, E. Ozols, M. C. Thomas, R. A. Flavell, R. J. Davis, and G. H. Tesch. 2009. Role of MKK3-p38 MAPK signalling in the development of type 2 diabetes and renal injury in obese db/db mice. Diabetologia 52: 347-358.
14. Ma, F. Y., G. H. Tesch, R. A. Flavell, R. J. Davis, and D. J. Nikolic-Paterson. 2007. MKK3-p38 signaling promotes apoptosis and the early inflammatory response in the obstructed mouse kidney. Am. J. Physiol. Renal Physiol. 293: F1556-F1563. (Pubitemid 350085991)
15. Wang, Y., H. X. Ji, J. N. Zheng, D. S. Pei, S. Q. Hu, and S. L. Qiu. 2009. Protective effect of selenite on renal ischemia/reperfusion injury through inhibiting ASK1-MKK3-p38 signal pathway. Redox Rep. 14: 243-250.
16. Fukuda, K., G. H. Tesch, F. Y. Yap, J. M. Forbes, R. A. Flavell, R. J. Davis, and D. J. Nikolic-Paterson. 2008. MKK3 signalling plays an essential role in leukocyte-mediated pancreatic injury in the multiple low-dose streptozotocin model. Lab. Invest. 88: 398-407. (Pubitemid 351432770)
17. Zhang, X., P. Shan, G. Jiang, L. Cohn, and P. J. Lee. 2006. Toll-like receptor 4 deficiency causes pulmonary emphysema. J. Clin. Invest. 116: 3050-3059. (Pubitemid 44684490)
18. Kuhlencordt, P. J., E. Rosel, R. E. Gerszten, M. Morales-Ruiz, D. Dombkowski, W. J. Atkinson, F. Han, F. Preffer, A. Rosenzweig, W. C. Sessa, et al. 2004. Role of endothelial nitric oxide synthase in endothelial activation: Insights from eNOS knockout endothelial cells. Am. J. Physiol. Cell Physiol. 286: C1195-C1202. (Pubitemid 38506935)
19. Matute-Bello, G., C. W. Frevert, and T. R. Martin. 2008. Animal models of acute lung injury. Am. J. Physiol. Lung Cell. Mol. Physiol. 295: L379-L399.
20. Warn, P. A., M. W. Brampton, A. Sharp, G. Morrissey, N. Steel, D. W. Denning, and T. Priest. 2003. Infrared body temperature measurement of mice as an early predictor of death in experimental fungal infections. Lab. Anim. 37: 126-131. (Pubitemid 36470100)
21. Xu, H., J. A. Gonzalo, Y. St Pierre, I. R. Williams, T. S. Kupper, R. S. Cotran, T. A. Springer, and J. C. Gutierrez-Ramos. 1994. Leukocytosis and resistance to septic shock in intercellular adhesion molecule 1-deficient mice. J. Exp. Med. 180: 95-109. (Pubitemid 24181059)
22. McDonald, B., K. Pittman, G. B. Menezes, S. A. Hirota, I. Slaba, C. C. Waterhouse, P. L. Beck, D. A. Muruve, and P. Kubes. 2010. Intravascular danger signals guide neutrophils to sites of sterile inflammation. Science 330: 362-366.
23. De Plaen, I. G., X. B. Han, X. Liu, W. Hsueh, S. Ghosh, and M. J. May. 2006. Lipopolysaccharide induces CXCL2/macrophage inflammatory protein-2 gene expression in enterocytes via NF-kappaB activation: Independence from endogenous TNF-alpha and platelet-activating factor. Immunology 118: 153-163. (Pubitemid 43727420)
24. Kisseleva, T., L. Song, M. Vorontchikhina, N. Feirt, J. Kitajewski, and C. Schindler. 2006. NF-kappaB regulation of endothelial cell function during LPS-induced toxemia and cancer. J. Clin. Invest. 116: 2955-2963. (Pubitemid 44684480)
25. Roebuck, K. A. 1999. Oxidant stress regulation of IL-8 and ICAM-1 gene expression: Differential activation and binding of the transcription factors AP-1 and NF-kappaB (Review). [Review] Int. J. Mol. Med. 4: 223-230.
26. Fujioka, S., J. Niu, C. Schmidt, G. M. Sclabas, B. Peng, T. Uwagawa, Z. Li, D. B. Evans, J. L. Abbruzzese, and P. J. Chiao. 2004. NF-kappaB and AP-1 connection: Mechanism of NF-kappaB-dependent regulation of AP-1 activity. Mol. Cell. Biol. 24: 7806-7819. (Pubitemid 39121503)
27. Asehnoune, K., D. Strassheim, S. Mitra, J. Y. Kim, and E. Abraham. 2004. Involvement of reactive oxygen species in Toll-like receptor 4-dependent activation of NF-kappa B. J. Immunol. 172: 2522-2529. (Pubitemid 38182403)
28. Mukhopadhyay, P., M. Rajesh, K. Yoshihiro, G. Haskó, and P. Pacher. 2007. Simple quantitative detection of mitochondrial superoxide production in live cells. Biochem. Biophys. Res. Commun. 358: 203-208. (Pubitemid 46719103)
29. Dikalova, A. E., A. T. Bikineyeva, K. Budzyn, R. R. Nazarewicz, L. McCann, W. Lewis, D. G. Harrison, and S. I. Dikalov. 2010. Therapeutic targeting of mitochondrial superoxide in hypertension. Circ. Res. 107: 106-116.
30. Hotchkiss, R. S., and I. E. Karl. 2003. The pathophysiology and treatment of sepsis. N. Engl. J. Med. 348: 138-150. (Pubitemid 36056721)
31. Deans, K. J., M. Haley, C. Natanson, P. Q. Eichacker, and P. C. Minneci. 2005. Novel therapies for sepsis: A review. J. Trauma 58: 867-874. (Pubitemid 40592766)
32. Kepp, O., L. Galluzzi, and G. Kroemer. 2011. Mitochondrial control of the NLRP3 inflammasome. Nat. Immunol. 12: 199-200.
33. Zhang, Q., M. Raoof, Y. Chen, Y. Sumi, T. Sursal, W. Junger, K. Brohi, K. Itagaki, and C. J. Hauser. 2010. Circulating mitochondrial DAMPs cause inflammatory responses to injury. Nature 464: 104-107.
34. Carré, J. E., J. C. Orban, L. Re, K. Felsmann, W. Iffert, M. Bauer, H. B. Suliman, C. A. Piantadosi, T. M. Mayhew, P. Breen, et al. 2010. Survival in critical illness is associated with early activation of mitochondrial biogenesis. Am. J. Respir. Crit. Care Med. 182: 745-751.
35. Brealey, D., M. Brand, I. Hargreaves, S. Heales, J. Land, R. Smolenski, N. A. Davies, C. E. Cooper, and M. Singer. 2002. Association between mitochondrial dysfunction and severity and outcome of septic shock. Lancet 360: 219-223. (Pubitemid 34804650)
36. Tak, P. P., and G. S. Firestein. 2001. NF-kappaB: A key role in inflammatory diseases. J. Clin. Invest. 107: 7-11. (Pubitemid 32047405)
37. Sen, C. K., S. Khanna, A. Z. Reznick, S. Roy, and L. Packer. 1997. Glutathione regulation of tumor necrosis factor-alpha-induced NF-kappa B activation in skeletal muscle-derived L6 cells. Biochem. Biophys. Res. Commun. 237: 645-649. (Pubitemid 27434740)
38. Janssen-Heininger, Y. M., M. E. Poynter, and P. A. Baeuerle. 2000. Recent advances towards understanding redox mechanisms in the activation of nuclear factor kappaB. Free Radic. Biol. Med. 28: 1317-1327. (Pubitemid 30621476)
39. Schmidt, K. N., P. Amstad, P. Cerutti, and P. A. Baeuerle. 1995. The roles of hydrogen peroxide and superoxide as messengers in the activation of transcription factor NF-kappa B. Chem. Biol. 2: 13-22.
40. Fan, H., B. Sun, Q. Gu, A. Lafond-Walker, S. Cao, and L. C. Becker. 2002. Oxygen radicals trigger activation of NF-kappaB and AP-1 and upregulation of ICAM-1 in reperfused canine heart. Am. J. Physiol. Heart Circ. Physiol. 282: H1778-H1786. (Pubitemid 34654847)
41. Pantano, C., N. L. Reynaert, A. van der Vliet, and Y. M. Janssen-Heininger. 2006. Redox-sensitive kinases of the nuclear factor-kappaB signaling pathway. Antioxid. Redox Signal. 8: 1791-1806. (Pubitemid 44726352)
42. Poltorak, A., X. He, I. Smirnova, M. Y. Liu, C. Van Huffel, X. Du, D. Birdwell, E. Alejos, M. Silva, C. Galanos, et al. 1998. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: Mutations in Tlr4 gene. Science 282: 2085-2088. (Pubitemid 29001265)
43. Kawai, T., O. Adachi, T. Ogawa, K. Takeda, and S. Akira. 1999. Unresponsiveness of MyD88-deficient mice to endotoxin. Immunity 11: 115-122. (Pubitemid 29359962)
44. Haziot, A., E. Ferrero, F. Kontgen, N. Hijiya, S. Yamamoto, J. Silver, C. L. Stewart, and S. M. Goyert. 1996. Resistance to endotoxin shock and reduced dissemination of gram-negative bacteria in CD14-deficient mice. Immunity 4: 407-414. (Pubitemid 26174055)
45. Li, P., H. Allen, S. Banerjee, S. Franklin, L. Herzog, C. Johnston, J. McDowell, M. Paskind, L. Rodman, J. Salfeld, et al. 1995. Mice deficient in IL-1 betaconverting enzyme are defective in production of mature IL-1 beta and resistant to endotoxic shock. Cell 80: 401-411.
46. Oliver, F. J., J. Ménissier-de Murcia, C. Nacci, P. Decker, R. Andriantsitohaina, S. Muller, G. de la Rubia, J. C. Stoclet, and G. de Murcia. 1999. Resistance to endotoxic shock as a consequence of defective NF-kappaB activation in poly (ADP-ribose) polymerase-1 deficient mice. EMBO J. 18: 4446-4454. (Pubitemid 29391254)
47. Rahman, A., and F. Fazal. 2009. Hug tightly and say goodbye: Role of endothelial ICAM-1 in leukocyte transmigration. Antioxid. Redox Signal. 11: 823-839.
48. Lee, J. H., L. Del Sorbo, S. Uhlig, G. A. Porro, T. Whitehead, S. Voglis, M. Liu, A. S. Slutsky, and H. Zhang. 2004. Intercellular adhesion molecule-1 mediates cellular cross-talk between parenchymal and immune cells after lipopolysaccharide neutralization. J. Immunol. 172: 608-616. (Pubitemid 38020519)
49. Panés, J., M. A. Perry, D. C. Anderson, A. Manning, B. Leone, G. Cepinskas, C. L. Rosenbloom, M. Miyasaka, P. R. Kvietys, and D. N. Granger. 1995. Regional differences in constitutive and induced ICAM-1 expression in vivo. Am. J. Physiol. 269: H1955-H1964.