ERK5 protein promotes, whereas MEK1 protein differentially regulates, the toll-like receptor 2 protein-dependent activation of human endothelial cells and monocytes

Journal of Biological Chemistry

Volumn 287, Issue 32, 2012, Pages 26478-26494

  Wilhelmsen, Kevin ^a   Mesa, Kailin R ^a   Lucero, Jennifer ^a   Xu, Fengyun ^a   Hellman, Judith ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL TYPES; ENDOTHELIAL FUNCTION; HUMAN ENDOTHELIAL CELLS; HUMAN LUNG; HUMAN MONOCYTES; HUMAN NEUTROPHIL; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; INFLAMMATORY MEDIATORS; INFLAMMATORY SIGNALING; KEY REGULATORS; MICROVASCULAR; SIGNALING PATHWAYS; TLR SIGNALING; TOLL-LIKE RECEPTOR 2; UP-REGULATION;

BLOOD VESSELS; COAGULATION; ENDOTHELIAL CELLS; PROTEINS; SIGNALING;

BODY FLUIDS;

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 7; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE P38; STRESS ACTIVATED PROTEIN KINASE; TOLL LIKE RECEPTOR 2;

ARTICLE; CELL ACTIVATION; CELL SPECIFICITY; CELL TYPE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; HUMAN; HUMAN CELL; INFLAMMATION; INTRACELLULAR SIGNALING; LEUKOCYTE ADHERENCE; LUNG ENDOTHELIUM; MICROVASCULAR ENDOTHELIAL CELL; MOLECULAR RECOGNITION; MONOCYTE; NEUTROPHIL; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RECEPTOR UPREGULATION; UMBILICAL VEIN ENDOTHELIAL CELL;

CELL ADHESION; CELL LINE; ELECTROPHORETIC MOBILITY SHIFT ASSAY; ENDOTHELIUM, VASCULAR; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HUMANS; MAP KINASE KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 7; MONOCYTES; NF-KAPPA B; REAL-TIME POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 2; UP-REGULATION;

EID: 84864555333     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.359489     Document Type: Article

References (70)

1. Ley, K., Laudanna, C., Cybulsky, M. I., and Nourshargh, S. (2007) Getting to the site of inflammation. The leukocyte adhesion cascade updated. Nat. Rev. Immunol. 7, 678-689 (Pubitemid 47327397)
2. Hickey, M. J., and Kubes, P. (2009) Intravascular immunity, The host-pathogen encounter in blood vessels. Nat. Rev. Immunol. 9, 364-375
3. Hotchkiss, R. S., and Karl, I. E. (2003) The pathophysiology and treatment of sepsis. N. Engl. J. Med. 348, 138-150 (Pubitemid 36056721)
4. Aird, W. C. (2003) The role of the endothelium in severe sepsis and multiple organ dysfunction syndrome. Blood 101, 3765-3777
5. Rittirsch, D., Flierl, M. A., and Ward, P. A. (2008) Harmful molecular mechanisms in sepsis. Nat. Rev. Immunol. 8, 776-787
6. Pober, J. S., and Sessa, W. C. (2007) Evolving functions of endothelial cells in inflammation. Nat. Rev. Immunol. 7, 803-815 (Pubitemid 47480307)
7. Takeuchi, O., and Akira, S. (2010) Pattern recognition receptors and inflammation. Cell 140, 805-820
8. Lin, Q., Li, M., Fang, D., Fang, J., and Su, S. B. (2011) The essential roles of Toll-like receptor signaling pathways in sterile inflammatory diseases. Int. Immunopharmacol. 11, 1422-1432
9. Kang, J. Y., and Lee, J. O. (2011) Structural biology of the Toll-like receptor family. Annu. Rev. Biochem. 80, 917-941
10. Zähringer, U., Lindner, B., Inamura, S., Heine, H., and Alexander, C. (2008) TLR2- promiscuous or specific? A critical re-evaluation of a receptor expressing apparent broad specificity. Immunobiology 213, 205-224
11. Jin, M. S., Kim, S. E., Heo, J. Y., Lee, M. E., Kim, H. M., Paik, S. G., Lee, H., and Lee, J. O. (2007) Crystal structure of the TLR1-TLR2 heterodimer induced by binding of a triacylated lipopeptide. Cell 130, 1071-1082 (Pubitemid 47410281)
12. Kang, J. Y., Nan, X., Jin, M. S., Youn, S. J., Ryu, Y. H., Mah, S., Han, S. H., Lee, H., Paik, S. G., and Lee, J. O. (2009) Recognition of lipopeptide patterns by Toll-like receptor 2-Toll-like receptor 6 heterodimer. Immunity 31, 873-884
13. Talreja, J., Kabir, M. H., B Filla, M., Stechschulte, D. J., and Dileepan, K. N. (2004) Histamine induces Toll-like receptor 2 and 4 expression in endothelial cells and enhances sensitivity to Gram-positive and Gram-negative bacterial cell wall components. Immunology 113, 224-233 (Pubitemid 39312450)
14. Li, Y., Xiang, M., Yuan, Y., Xiao, G., Zhang, J., Jiang, Y., Vodovotz, Y., Billiar, T. R., Wilson, M. A., and Fan, J. (2009) Hemorrhagic shock augments lung endothelial cell activation. Role of temporal alterations of TLR4 and TLR2. Am. J. Physiol. Regul. Integr. Comp. Physiol. 297, R1670-R1680
15. Grote, K., Schuett, H., Salguero, G., Grothusen, C., Jagielska, J., Drexler, H., Mühlradt, P. F., and Schieffer, B. (2010) Toll-like receptor 2/6 stimulation promotes angiogenesis via GM-CSF as a potential strategy for immune defense and tissue regeneration. Blood 115, 2543-2552
16. Shin, H. S., Xu, F., Bagchi, A., Herrup, E., Prakash, A., Valentine, C., Kulkarni, H., Wilhelmsen, K., Warren, S., and Hellman, J. (2011) Bacterial lipoprotein TLR2 agonists broadly modulate endothelial function and coagulation pathways in vitro and in vivo. J. Immunol. 186, 1119-1130
17. Satta, N., Kruithof, E. K., Reber, G., and de Moerloose, P. (2008) Induction of TLR2 expression by inflammatory stimuli is required for endothelial cell responses to lipopeptides. Mol. Immunol. 46, 145-157
18. Fan, J., Frey, R. S., and Malik, A. B. (2003) TLR4 signaling induces TLR2 expression in endothelial cells via neutrophil NADPH oxidase. J. Clin. Invest. 112, 1234-1243 (Pubitemid 38056300)
19. Faure, E., Thomas, L., Xu, H., Medvedev, A., Equils, O., and Arditi, M. (2001) Bacterial lipopolysaccharide and IFNγ induce Toll-like receptor 2 and Toll-like receptor 4 expression in human endothelial cells. Role of NF-κB activation. J. Immunol. 166, 2018-2024 (Pubitemid 32114690)
20. Wilhelmsen, K., Mesa, K. R., Prakash, A., Xu, F., and Hellman, J. (2011) Activation of endothelial TLR2 by bacterial lipoprotein upregulates proteins specific for the neutrophil response. Innate Immun, in press
21. Haehnel, V., Schwarzfischer, L., Fenton, M. J., and Rehli, M. (2002) Transcriptional regulation of the human toll-like receptor 2 gene in monocytes and macrophages. J. Immunol. 168, 5629-5637 (Pubitemid 34556144)
22. Vallabhapurapu, S., and Karin, M. (2009) Regulation and function of NF-κB transcription factors in the immune system. Annu. Rev. Immunol. 27, 693-733
23. Scheidereit, C. (2006) IκB kinase complexes. Gateways to NF-κB activation and transcription. Oncogene 25, 6685-6705
24. Perkins, N. D. (2006) Post-translational modifications regulating the activity and function of the nuclear factor κB pathway. Oncogene 25, 6717-6730
25. Verstak, B., Nagpal, K., Bottomley, S. P., Golenbock, D. T., Hertzog, P. J., and Mansell, A. (2009) MyD88 adapter-like (Mal)/TIRAP interaction with TRAF6 is critical for TLR2- and TLR4-mediated NF-κB proinflammatory responses. J. Biol. Chem. 284, 24192-24203
26. Cargnello, M., and Roux, P. P. (2011) Activation and function of the MAPKs and their substrates, the MAPK-activated protein kinases. Microbiol. Mol. Biol. Rev. 75, 50-83
27. Horng, T., Barton, G. M., Flavell, R. A., and Medzhitov, R. (2002) The adaptor molecule TIRAP provides signaling specificity for Toll-like receptors. Nature 420, 329-333 (Pubitemid 35398189)
28. Farhat, K., Riekenberg, S., Heine, H., Debarry, J., Lang, R., Mages, J., Buwitt-Beckmann, U., Röschmann, K., Jung, G., Wiesmüller, K. H., and Ulmer, A. J. (2008) Heterodimerization of TLR2 with TLR1 or TLR6 expands the ligand spectrum but does not lead to differential signaling. J. Leukoc. Biol. 83, 692-701 (Pubitemid 351966879)
29. Zhu, W., Downey, J. S., Gu, J., Di Padova, F., Gram, H., and Han, J. (2000) Regulation of TNF expression by multiple mitogen-activated protein kinase pathways. J. Immunol. 164, 6349-6358 (Pubitemid 30408816)
30. Miller, M. (2009) The importance of being flexible. The case of basic region leucine zipper transcriptional regulators. Curr. Protein Pept. Sci. 10, 244-269
31. Cuadrado, A., and Nebreda, A. R. (2010) Mechanisms and functions of p38 MAPK signaling. Biochem. J. 429, 403-417
32. Anderson, P. (2008) Post-transcriptional control of cytokine production. Nat. Immunol. 9, 353-359
33. Collins, T., Read, M. A., Neish, A. S., Whitley, M. Z., Thanos, D., and Maniatis, T. (1995) Transcriptional regulation of endothelial cell adhesion molecules. NF-κB and cytokine-inducible enhancers. FASEB J. 9, 899-909
34. Ye, X., Ding, J., Zhou, X., Chen, G., and Liu, S. F. (2008) Divergent roles of endothelial NF-κB in multiple organ injury and bacterial clearance in mouse models of sepsis. J. Exp. Med. 205, 1303-1315 (Pubitemid 351831488)
35. Read, M. A., Whitley, M. Z., Gupta, S., Pierce, J. W., Best, J., Davis, R. J., and Collins, T. (1997) Tumor necrosis factor α-induced E-selectin expression is activated by the nuclear factor-κB and c-JUN N-terminal kinase/p38 mitogen-activated protein kinase pathways. J. Biol. Chem. 272, 2753-2761 (Pubitemid 27053319)
36. Daigneault, M., Preston, J. A., Marriott, H. M., Whyte, M. K., and Dockrell, D. H. (2010) The identification of markers of macrophage differentiation in PMA-stimulated THP-1 cells and monocyte-derived macrophages. PLoS One 5, e8668
37. Nuzzi, P. A., Lokuta, M. A., and Huttenlocher, A. (2007) Analysis of neutrophil chemotaxis. Methods Mol. Biol. 370, 23-36
38. Yen, J., and Kramer, S. M. (1991) A rapid in vitro cytotoxicity assay for the detection of tumor necrosis factor on human BT-20 cells. J. Immunother. 10, 174-181
39. Livak, K. J., and Schmittgen, T. D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCt method. Methods 25, 402-408 (Pubitemid 34164012)
40. Willems, E., Leyns, L., and Vandesompele, J. (2008) Standardization of real-time PCR gene expression data from independent biological replicates. Anal. Biochem. 379, 127-129
41. Edgar, R., Domrachev, M., and Lash, A. E. (2002) Gene Expression Omnibus. NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 30, 207-210 (Pubitemid 34679544)
42. Schmidt, R. R., Pedersen, C. M., Qiao, Y., and Zähringer, U. (2011) Chemical synthesis of bacterial lipoteichoic acids. An insight on its biological significance. Org. Biomol. Chem. 9, 2040-2052
43. Mody, N., Leitch, J., Armstrong, C., Dixon, J., and Cohen, P. (2001) Effects of MAP kinase cascade inhibitors on the MKK5/ERK5 pathway. FEBS Lett. 502, 21-24 (Pubitemid 32722053)
44. Kamakura, S., Moriguchi, T., and Nishida, E. (1999) Activation of the protein kinase ERK5/BMK1 by receptor-tyrosine kinases. Identification and characterization of a signaling pathway to the nucleus. J. Biol. Chem. 274, 26563-26571
45. Petersen, B., Bloch, K. D., Ichinose, F., Shin, H. S., Shigematsu, M., Bagchi, A., Zapol, W. M., and Hellman, J. (2008) Activation of Toll-like receptor 2 impairs hypoxic pulmonary vasoconstriction in mice. Am. J. Physiol. Lung Cell. Mol. Physiol. 294, L300-L308 (Pubitemid 351253366)
46. Takeuchi, O., Hoshino, K., and Akira, S. (2000) Cutting edge. TLR2-deficient and MyD88-deficient mice are highly susceptible to Staphylococcus aureus infection. J. Immunol. 165, 5392-5396
47. Menzies, B. E., and Kourteva, I. (1998) Internalization of Staphylococcus aureus by endothelial cells induces apoptosis. Infect Immun 66, 5994-5998 (Pubitemid 28531863)
48. Beekhuizen, H., van de Gevel, J. S., Olsson, B., van Benten, I. J., and van Furth, R. (1997) Infection of human vascular endothelial cells with Staphylococcus aureus induces hyperadhesiveness for human monocytes and granulocytes. J. Immunol. 158, 774-782 (Pubitemid 127492654)
49. Shaul, Y. D., and Seger, R. (2007) The MEK/ERK cascade. From signaling specificity to diverse functions. Biochim. Biophys. Acta 1773, 1213-1226 (Pubitemid 47125968)
50. Chen, P., Li, J., Barnes, J., Kokkonen, G. C., Lee, J. C., and Liu, Y. (2002) Restraint of proinflammatory cytokine biosynthesis by mitogen-activated protein kinase phosphatase-1 in lipopolysaccharide-stimulated macrophages. J. Immunol. 169, 6408-6416 (Pubitemid 36903490)
51. Bertelsen, T., Iversen, L., Riis, J. L., Arthur, J. S., Bibby, B. M., Kragballe, K., and Johansen, C. (2011) The role of mitogen- and stress-activated protein kinase 1 and 2 in chronic skin inflammation in mice. Exp. Dermatol. 20, 140-145
52. Salojin, K. V., Owusu, I. B., Millerchip, K. A., Potter, M., Platt, K. A., and Oravecz, T. (2006) Essential role of MAPK phosphatase-1 in the negative control of innate immune responses. J. Immunol. 176, 1899-1907 (Pubitemid 43134335)
53. Rovida, E., Spinelli, E., Sdelci, S., Barbetti, V., Morandi, A., Giuntoli, S., and Dello Sbarba, P. (2008) ERK5/BMK1 is indispensable for optimal colony-stimulating factor 1 (CSF-1)-induced proliferation in macrophages in a Src-dependent fashion. J. Immunol. 180, 4166-4172
54. Roberts, O. L., Holmes, K., Müller, J., Cross, D. A., and Cross, M. J. (2009) ERK5 and the regulation of endothelial cell function. Biochem. Soc. Trans. 37, 1254-1259
55. Kato, Y., Zhao, M., Morikawa, A., Sugiyama, T., Chakravortty, D., Koide, N., Yoshida, T., Tapping, R. I., Yang, Y., Yokochi, T., and Lee, J. D. (2000) Big mitogen-activated kinase regulates multiple members of the MEF2 protein family. J. Biol. Chem. 275, 18534-18540 (Pubitemid 30414815)
56. Kato, Y., Kravchenko, V. V., Tapping, R. I., Han, J., Ulevitch, R. J., and Lee, J. D. (1997) BMK1/ERK5 regulates serum-induced early gene expression through transcription factor MEF2C. EMBO J. 16, 7054-7066 (Pubitemid 27520805)
57. Han, T. H., and Prywes, R. (1995) Regulatory role of MEF2D in serum induction of the c-jun promoter. Mol. Cell. Biol. 15, 2907-2915
58. Sohn, S. J., Li, D., Lee, L. K., and Winoto, A. (2005) Transcriptional regulation of tissue-specific genes by the ERK5 mitogen-activated protein kinase. Mol. Cell. Biol. 25, 8553-8566 (Pubitemid 41369176)
59. SenBanerjee, S., Lin, Z., Atkins, G. B., Greif, D. M., Rao, R. M., Kumar, A., Feinberg, M. W., Chen, Z., Simon, D. I., Luscinskas, F. W., Michel, T. M., Gimbrone, M. A., Jr., García-Cardeña, G., and Jain, M. K. (2004) KLF2 Is a novel transcriptional regulator of endothelial proinflammatory activation. J. Exp. Med. 199, 1305-1315 (Pubitemid 38685723)
60. Lin, Z., Kumar, A., SenBanerjee, S., Staniszewski, K., Parmar, K., Vaughan, D. E., Gimbrone, M. A., Jr., Balasubramanian, V., García- Cardeña, G., and Jain, M. K. (2005) Kruppel-like factor 2 (KLF2) regulates endothelial thrombotic function. Circ. Res. 96, e48-57
61. Bhattacharya, R., Senbanerjee, S., Lin, Z., Mir, S., Hamik, A., Wang, P., Mukherjee, P., Mukhopadhyay, D., and Jain, M. K. (2005) Inhibition of vascular permeability factor/vascular endothelial growth factor-mediated angiogenesis by the Kruppel-like factor KLF2. J. Biol. Chem. 280, 28848-28851 (Pubitemid 41161328)
62. Atkins, G. B., and Jain, M. K. (2007) Role of Krüppel-like transcription factors in endothelial biology. Circ. Res. 100, 1686-1695 (Pubitemid 46987860)
63. Solan, J. L., and Lampe, P. D. (2009) Connexin43 phosphorylation. Structural changes and biological effects. Biochem. J. 419, 261-272
64. Cameron, S. J., Malik, S., Akaike, M., Lerner-Marmarosh, N., Yan, C., Lee, J. D., Abe, J., and Yang, J. (2003) Regulation of epidermal growth factor-induced connexin 43 gap junction communication by big mitogen-activated protein kinase1/ERK5 but not ERK1/2 kinase activation. J. Biol. Chem. 278, 18682-18688 (Pubitemid 36799496)
65. Winzen, R., Kracht, M., Ritter, B., Wilhelm, A., Chen, C. Y., Shyu, A. B., Müller, M., Gaestel, M., Resch, K., and Holtmann, H. (1999) The p38 MAP kinase pathway signals for cytokine-induced mRNA stabilization via MAP kinase-activated protein kinase 2 and an AU-rich region-targeted mechanism. EMBO J. 18, 4969-4980 (Pubitemid 29443799)
66. Sandler, H., and Stoecklin, G. (2008) Control of mRNA decay by phosphorylation of tristetraprolin. Biochem. Soc. Trans. 36, 491-496 (Pubitemid 351839361)
67. Vermeulen, L., De Wilde, G., Van Damme, P., Vanden Berghe, W., and Haegeman, G. (2003) Transcriptional activation of the NF-κB p65 subunit by mitogen- and stress-activated protein kinase-1 (MSK1). EMBO J. 22, 1313-1324 (Pubitemid 36362695)
68. Saccani, S., Pantano, S., and Natoli, G. (2002) p38-Dependent marking of inflammatory genes for increased NF-κB recruitment. Nat. Immunol. 3, 69-75 (Pubitemid 34065620)
69. Wang, X., Flynn, A., Waskiewicz, A. J., Webb, B. L., Vries, R. G., Baines, I. A., Cooper, J. A., and Proud, C. G. (1998) The phosphorylation of eukaryotic initiation factor eIF4E in response to phorbol esters, cell stresses, and cytokines is mediated by distinct MAP kinase pathways. J. Biol. Chem. 273, 9373-9377 (Pubitemid 28183016)
70. Ananieva, O., Darragh, J., Johansen, C., Carr, J. M., McIlrath, J., Park, J. M., Wingate, A., Monk, C. E., Toth, R., Santos, S. G., Iversen, L., and Arthur, J. S. (2008) The kinases MSK1 and MSK2 act as negative regulators of Toll-like receptor signaling. Nat. Immunol. 9, 1028-1036