MKK3 and -6-dependent activation of p38α MAP kinase is required for cytoskeletal changes in pulmonary microvascular endothelial cells induced by ICAM-1 ligation

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 288, Issue 2 32-2, 2005, Pages

  Wang, Qin ^a   Yerukhimovich, Michael ^a   Gaarde, William A ^b   Popoff, Ian J ^c   Doerschuk, Claire M ^a,d  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ISIS PHARMACEUTICALS   (United States)

^c PFIZER INC   (United States)

^d CASE WESTERN RESERVE UNIVERSITY   (United States)

Author keywords

Actin; Inflammation; Intercellular adhesion molecule; Mitogen activated protein kinase kinase 3 6; Neutrophil; Tumor necrosis factor

Indexed keywords

ACTIN; HEAT SHOCK PROTEIN 27; INTERCELLULAR ADHESION MOLECULE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE KINASE 6; MITOGEN ACTIVATED PROTEIN KINASE P38; SMALL INTERFERING RNA;

ACTIN POLYMERIZATION; ARTICLE; CELL ADHESION; CELL JUNCTION; CELL MIGRATION; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOSKELETON; ENDOTHELIUM CELL; ENZYME ACTIVATION; HUMAN; HUMAN CELL; LUNG BLOOD VESSEL; MICROVASCULATURE; NEUTROPHIL; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MODIFICATION;

ACTINS; CELL ADHESION; CELL MOVEMENT; CELLS, CULTURED; CROSS-LINKING REAGENTS; CYTOSKELETON; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; HEAT-SHOCK PROTEINS; HUMANS; INTERCELLULAR ADHESION MOLECULE-1; ISOENZYMES; LUNG; MAP KINASE KINASE 3; MAP KINASE KINASE 6; NEOPLASM PROTEINS; NEUTROPHILS; OLIGONUCLEOTIDES, ANTISENSE; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; SIGNAL TRANSDUCTION;

EID: 12144256835     PISSN: 10400605     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajplung.00292.2004     Document Type: Article

References (40)

1. Alonso G, Ambrosino C, Jones M, and Nebreda AR. Differential activation of p38 mitogen-activated protein kinase isoforms depending on signal strength. J Biol Chem 275: 40641-40648, 2000.
2. Ambrosino C, Mace G, Galban S, Fritsch C, Vintersten K, Black E, Gorospe M, and Nebreda AR. Negative feedback regulation of MKK6 mRNA stability by p38alpha mitogen-activated protein kinase. Mol Cell Biol 23: 370-381, 2003.
3. Barreiro O, Yanez-Mo M, Serrador JM, Montoya MC, Vicente-Manzanares M, Tejedor R, Furthmayr H, and Sanchez-Madrid F. Dynamic interaction of VCAM-1 and ICAM-1 with moesin and ezrin in a novel endothelial docking structure for adherent leukocytes. J Cell Biol 157: 1233-1245, 2002.
4. Benndorf R, Hayess K, Ryazantsev S, Wieske M, Behlke J, and Lutsch G. Phosphorylation and supramolecular organization of murine small heat shock protein HSP25 abolish its actin polymerization-inhibiting activity. J Biol Chem 269: 20780-20784, 1994.
5. Carman CV, Jun CD, Salas A, and Springer TA. Endothelial cells proactively form microvilli-like membrane projections upon intercellular adhesion molecule 1 engagement of leukocyte LFA-I. J Immunol 171: 6135-6144, 2003.
6. Cheung PC, Campbell DG, Nebreda AR, and Cohen P. Feedback control of the protein kinase TAK1 by SAPK2a/p38alpha. EMBO J 22: 5793-5805, 2003.
7. Clayton A, Evans RA, Pettit E, Hallett M, Williams JD, and Steadman R. Cellular activation through the ligation of intercellular adhesion molecule-1. J Cell Sci 111: 443-453, 1998.
8. Cuenda A, Cohen P, Buee-Scherrer V, and Goedert M. Activation of stress-activated protein kinase-3 (SAPK3) by cytokines and cellular stresses is mediated via SAPKK3 (MKK6); comparison of the specificities of SAPK3 and SAPK2 (RK/p38). EMBO J 16: 295-305, 1997.
9. Dashti SR, Efimova T, and Eckert RL. MEK7-dependent activation of p38 MAP kinase in keratinocytes. J Biol Chem 276: 8059-8063, 2001.
10. Derijard B, Raingeaud J, Barrett T, Wu IH, Han J, Ulevitch RJ, and Davis RJ. Independent human MAP-kinase signal transduction pathways defined by MEK and MKK isoforms. Science 267: 682-685, 1995.
11. Durieu-Trautmann O, Chaverot N, Cazaubon S, Strosberg AD, and Couraud PO. Intercellular adhesion molecule 1 activation induces tyrosine phosphorylation of the cytoskeleton-associated protein cortactin in brain microvessel endothelial cells. J Biol Chem 269: 12536-12540, 1994.
12. Enslen H, Branche DM, and Davis RJ. Molecular determinants that mediate selective activation of p38 MAP kinase isoforms. EMBO J 19: 1301-1311, 2000.
13. Enslen H, Raingeaud J, and Davis RJ. Selective activation of p38 mitogen-activated protein (MAP) kinase isoforms by the MAP kinase kinases MKK3 and MKK6. J Biol Chem 273: 1741-1748, 1998.
14. Etienne-Manneville S, Manneville JB, Adamson P, Wilbourn B, Greenwood J, and Couraud PO. ICAM-1-coupled cytoskeletal rearrangements and transendothelial lymphocyte migration involve intracellular calcium signaling in brain endothelial cell lines. J Immunol 165: 3375-3383, 2000.
15. Freshney NW, Rawlinson L, Guesdon F, Jones E, Cowley S, Hsuan J, and Saklatvala J. Interleukin-1 activates a novel protein kinase cascade that results in the phosphorylation of Hsp27. Cell 78: 1039-1049, 1994.
16. Ge B, Gram H, Di Padova F, Huang B, New L, Ulevitch RJ, Luo Y, and Han J. MAPKK-independent activation of p38alpha mediated by TAB1-dependent autophosphorylation of p38alpha. Science 295: 1291-1294, 2002.
17. Ge B, Xiong X, Jing Q, Mosley JL, Filose A, Bian D, Huang S, and Han J. TAB1beta (transforming growth factor-beta-activated protein kinase 1-binding protein 1beta), a novel splicing variant of TAB1 that interacts with p38alpha but not TAK1. J Biol Chem 278: 2286-2293, 2003.
18. Greenwood J, Amos CL, Walters CE, Couraud PO, Lyck R, Engelhardt B, and Adamson P. Intracellular domain of brain endothelial intercellular adhesion molecule-1 is essential for T lymphocyte-mediated signaling and migration. J Immunol 171: 2099-2108, 2003.
19. Hale KK, Trollinger D, Rihanek M, and Manthey CL. Differential expression and activation of p38 mitogen-activated protein kinase alpha, beta, gamma, and delta in inflammatory cell lineages. J Immunol 162: 4246-4252, 1999.
20. Hedges JC, Dechert MA, Yamboliev IA, Martin JL, Hickey E, Weber LA, and Gerthoffer WT. A role for p38(MAPK)/HSP27 pathway in smooth muscle cell migration. J Biol Chem 274: 24211-24219, 1999.
21. Huot J, Houle F, Marceau F, and Landry J. Oxidative stress-induced actin reorganization mediated by the p38 mitogen-activated protein kinase/heat shock protein 27 pathway in vascular endothelial cells. Circ Res 80: 383-392, 1997.
22. Johnson GL and Lapadat R. Mitogen-activated protein kinase pathways mediated by ERK, JNK, and p38 protein kinases. Science 298: 1911-1912, 2002.
23. Kumar S, McDonnell PC, Gum RJ, Hand AT, Lee JC, and Young PR. Novel homologues of CSBP/p38 MAP kinase: activation, substrate specificity and sensitivity to inhibition by pyridinyl imidazoles. Biochem Biophys Res Commun 235: 533-538, 1997.
24. Kyriakis JM and Avruch J. Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol Rev 81: 807-869, 2001.
25. Lavoie JN, Hickey E, Weber LA, and Landry J. Modulation of actin microfilament dynamics and fluid phase pinocytosis by phosphorylation of heat shock protein 27. J Biol Chem 268: 24210-24214, 1993.
26. Lin A, Minden A, Martinetto H, Claret FX, Lange-Carter C, Mercurio F, Johnson GL, and Karin M. Identification of a dual specificity kinase that activates the Jun kinases and p38-Mpk2. Science 268: 286-290, 1995.
27. Lyck R, Reiss Y, Gerwin N, Greenwood J, Adamson P, and Engelhardt B. T-cell interaction with ICAM-1/ICAM-2 double-deficient brain endothelium in vitro: the cytoplasmic tail of endothelial ICAM-1 is necessary for transendothelial migration of Tcells. Blood 102: 3675-3683, 2003.
28. Mudgett JS, Ding J, Guh-Siesel L, Chartrain NA, Yang L, Gopal S, and Shen MM. Essential role for p38alpha mitogen-activated protein kinase in placental angiogenesis. Proc Natl Acad Sci USA 97: 10454-10459, 2000.
29. Razandi M, Pedram A, and Levin ER. Estrogen signals to the preservation of endothelial cell form and function. J Biol Chem 275: 38540-38546, 2000.
30. Rouse J, Cohen P, Trigon S, Morange M, Alonso-Llamazares A, Zamanillo D, Hunt T, and Nebreda AR. A novel kinase cascade triggered by stress and heat shock that stimulates MAPKAP kinase-2 and phosphorylation of the small heat shock proteins. Cell 78: 1027-1037, 1994.
31. Rousseau S, Houle F, Landry J, and Huot J. p38 MAP kinase activation by vascular endothelial growth factor mediates actin reorganization and cell migration in human endothelial cells. Oncogens 15: 2169-2177, 1997.
32. Sans E, Delachanal E, and Duperray A. Analysis of the roles of ICAM-1 in neutrophil transmigration using a reconstituted mammalian cell expression model: implication of ICAM-1 cytoplasmic domain and Rho-dependent signaling pathway. J Immunol 166: 544-551, 2001.
33. Tamura K, Sudo T, Senftleben U, Dadak AM, Johnson R, and Karin M. Requirement for p38alpha in erythropoietin expression: a role for stress kinases in erythropoiesis. Cell 102: 221-231, 2000.
34. Tanno M, Bassi R, Gorog DA, Saurin AT, Jiang J, Heads RJ, Martin JL, Davis RJ, Flavell RA, and Marber MS. Diverse mechanisms of myocardial p38 mitogen-activated protein kinase activation: evidence for MKK-independent activation by a TAB1-associated mechanism contributing to injury during myocardial ischemia. Circ Res 93: 254-261, 2003.
35. Wang Q, Chiang ET, Lim M, Lai J, Rogers R, Janmey PA, Shepro D, and Doerschuk CM. Changes in the biomechanical properties of neutrophils and endothelial cells during adhesion. Blood 97: 660-668, 2001.
36. Wang Q and Doerschuk CM. Neutrophil-induced changes in the biomechanical properties of endothelial cells: roles of ICAM-1 and reactive oxygen species. J Immunol 164: 6487-6494, 2000.
37. Wang Q and Doerschuk CM. The p38 mitogen-activated protein kinase mediates cytoskeletal remodeling in pulmonary microvascular endothelial cells upon intracellular adhesion molecule-1 ligation. J Immunol 166: 6877-6884, 2001.
38. Wang Q, Pfeiffer GR II, and Gaarde WA. Activation of SRC tyrosine kinases in response to ICAM-1 ligation in pulmonary microvascular endothelial cells. J Biol Chem 278: 47731-47743, 2003.
39. Widmann C, Gibson S, Jarpe MB, and Johnson GL. Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human. Physiol Rev 79: 143-180, 1999.
40. Wojciak-Stothard B, Williams L, and Ridley AJ. Monocyte adhesion and spreading on human endothelial cells is dependent on Rho-regulated receptor clustering. J Cell Biol 145: 1293-1307, 1999.