Role of CaM kinase II and ERK activation in thrombin-induced endothelial cell barrier dysfunction

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 285, Issue 1 29-1, 2003, Pages

  Borbiev, Talaibek ^a   Verin, Alexander D ^a   Birukova, Anna ^a   Liu, Feng ^a   Crow, Michael T ^a   Garcia, Joe G N ^a,b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS ASTHMA AND ALLERGY CENTER   (United States)

Author keywords

Caldesmon; Extracellular signal regulated kinase; Thrombin; Transendothelial electrical resistance

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; ACTIN; CALDESMON; CALMODULIN; CALMODULIN DEPENDENT PROTEIN KINASE II; MITOGEN ACTIVATED PROTEIN KINASE; MYOSIN; N [2 [[N [3 (4 CHLOROPHENYL) 2 PROPENYL] N METHYLAMINO]METHYL]PHENYL] N (2 HYDROXYETHYL) 4 METHOXYBENZENESULFONAMIDE; PHOSPHOTRANSFERASE; THROMBIN; UNCLASSIFIED DRUG; VIRUS ENZYME;

ACTIN FILAMENT; ADENOVIRUS; ANIMAL CELL; ARTERY ENDOTHELIUM; ARTICLE; CATTLE; CONTROLLED STUDY; ELECTRIC RESISTANCE; ENDOTHELIUM CELL; ENDOTHELIUM LESION; ENZYME ACTIVATION; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOPRECIPITATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PULMONARY ARTERY;

EID: 0038000525     PISSN: 10400605     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajplung.00460.2001     Document Type: Article

References (57)

1. 2+/calmodulin-dependent protein kinase II in the mitogen-activated protein kinase signaling cascade of cultured rat aortic vascular smooth muscle cells. Circ Res 81: 575-584, 1997.
2. Adam LP and Hathaway DR. Identification of mitogen-activated protein kinase phosphorylation sequences in mammalian h-caldesmon. FEBS Lett 322: 56-60, 1993.
3. 3 integrin complex is reversed by activated calcium/calmodulin-dependent protein kinase II. J Clin Invest 100: 693-704, 1997.
4. Birukov KG, Csortos C, Marzilli L, Dudek S, Ma SF, Bresnick AR, Verin AD, Cotter RJ, and Garcia JG. Differential regulation of alternatively spliced endothelial cell myosin light chain kinase isoforms by p60(Src). J Biol Chem 276: 8567-8573, 2001.
5. Borbiev T, Verin AD, Shi S, Liu F, and Garcia JGN. Regulation of endothelial cell barrier function by calcium/calmodulin-dependent protein kinase II. Am J Physiol Lung Cell Mol Physiol 280: L983-L990, 2001.
6. Braun AP and Schulman H. The multifunctional calcium/calmodulin-dependent protein kinase: from form to function. Annu Rev Physiol 57: 417-445, 1995.
7. Castellino F, Ono S, Matsumura F, and Luini A. Essential role of caldesmon in the actin filament reorganization induced by glucocorticoids. J Cell Biol 131: 1223-1230, 1995.
8. Childs T, Watson MH, Sanghera JS, Campbell DL, Pelech SL, and Mak AS. Phosphorylation of smooth muscle caldesmon by mitogen-activated protein (MAP) kinase and expression of MAP kinase in differentiated smooth muscle cells. J Biol Chem 267: 22853-22859, 1992.
9. D'Angelo G, Graceffa P, Wang CLA, Wrangle J, and Adam LP. Mammal- specific, ERK-dependent, caldesmon phosphorylation in smooth muscle. J Biol Chem 274: 30115-30121, 1999.
10. Dessy C, Kim I, Sougnez CL, Laporte R, and Morgan KG. A role for MAP kinase in differentiated smooth muscle contraction evoked by α-adrenoceptor stimulation. Am J Physiol Cell Physiol 275: C1081-C1086, 1998.
11. Dudek SM and Garcia JGN. Cytoskeletal regulation of pulmonary vascular permeability. J Appl Physiol 91: 1487-1500, 2001.
12. Foster DB, Shen LH, Kelly J, Thibault P, Van Eyk JP, and Mak AS. Phosphorylation of caldesmon by p21-activated kinase. J Biol Chem 275: 1959-1965, 2000.
13. Franklin MT, Wang CL, and Adam LP. Stretch-dependent activation and desensitization of mitogen-activated protein kinase in carotid arteries. Am J Physiol Cell Physiol 273: C1819-C1827, 1997.
14. Garcia JG, Birnboim AS, Bizios R, Del Vecchio PJ, Fenton JW, and Malik AB. Thrombin-induced increases in albumin clearance across cultured endothelial monolayers. J Cell Physiol 128:96-104, 1986.
15. Garcia JG, Davis HW, and Patterson CE. Regulation of endothelial gap formation and barrier dysfunction: role of myosin light chain phosphorylation. J Cell Physiol 163: 510-522, 1995.
16. Garcia JG, Fenton JW, and Natarajan V. Thrombin stimulated phospholipase D activity in HUVEC. Regulation by phospholipase C, protein kinase C, and cAMP. Blood 79: 2056-2067, 1992.
17. Garcia JG, Lazar V, Gilbert-McClain LI, Gallagher PJ, and Verin AD. Myosin light chain kinase in endothelium: molecular cloning and regulation. Am J Respir Cell Mol Biol 16: 489-494, 1997.
18. Garcia JG, Liu F, Verin AD, Birukova A, Dechert MA, Gerthoffer WT, Bamburg JR, and English D. Sphingosine 1-phosphate promotes endothelial cell barrier integrity by Edgdependent cytoskeletal rearrangement. J Clin Invest 108: 689-701, 2001.
19. 2+ mobilization, barrier dysfunction, prostaglandin synthesis, and platelet-derived growth factor mRNA expression in cultured endothelium. J Cell Physiol 156: 541-549, 1993.
20. Garcia JG, Schaphorst KL, Verin AD, Vepa S, Patterson CE, and Natarajan V. Diperoxovanadate alters endothelial cell focal contacts and barrier function: role of tyrosine phosphorylation. J Appl Physiol 89: 2333-2343, 2000.
21. Gerthoffer WT, Yamboliev IA, Pohl J, Haynes R, Dang S, and McHugh J. Activation of MAP kinases in airway smooth muscle. Am J Physiol Lung Cell Mol Physiol 272: L244-L252, 1997.
22. Gerthoffer WT, Yamboliev IA, Shearer M, Pohl J, Haynes R, Dang S, Sato K, and Sellers JR. Activation of MAP kinases and phosphorylation of caldesmon in canine colonic smooth muscle. J Physiol 495: 597-609, 1996.
23. Goncharova EA, Shirinsky VP, Shevelev AY, Marston SB, and Vorotnikov AV. Actomyosin cross-linking by caldesmon in non-muscle cells. FEBS Lett 497: 113-117, 2001.
24. Gorenne I, Su X, and Moreland RS. Inhibition of p42 and p44 MAP kinase does not alter smooth muscle contraction in swine carotid artery. Am J Physiol Heart Circ Physiol 275: H131-H138, 1998.
25. Helfman DM, Levy ET, Berthier C, Shtutman M, Riveline D, Grosheva I, Lachish-Zalait A, Elbaum M, and Bershadsky AD. Caldesmon inhibits nonmuscle cell contractility and interferes with the formation of focal adhesions. Mol Biol Cell 10: 3097-3112, 1999.
26. Hemric ME, Lu FWM, Shrager R, Carey J, and Chalovich JM. Reversal of caldesmon binding to myosin with calcium-calmodulin or by phosphorylating caldesmon. J Biol Chem 268: 15305-15311, 1993.
27. 2 and C in pig aortic endothelial cells synthesizing prostacyclin. J Biol Chem 257: 7151-7154, 1982.
28. Huber PAJ, Redwood CS, Avent ND, Tanner MJA, and Marston SB. Identification of functioning regulatory sites and a new myosin binding site in the C-terminal 288 amino acids of caldesmon expressed from a human clone. J Muscle Res Cell Motil 14: 385-391, 1993.
29. Humphrey MB, Herrera-Sosa H, Gonzalez G, Lee R, and Bryan J. Cloning of cDNAs encoding human caldesmons. Gene 112: 197-204, 1992.
30. Ikebe M and Reardon S. Phosphorylation of smooth muscle caldesmon by calmodulin-dependent protein kinase II. J Biol Chem 265: 17607-17612, 1990.
31. Katoh K, Kano Y, Amano M, Onishi H, Kaibuchi K, and Fujiwara K. Rho-kinase-mediated contraction of isolated stress fibers. J Cell Biol 153: 569-583, 2001.
32. Katoh K, Kano Y, Masuda M, Onishi H, and Fujiwara K. Isolation and contraction of the stress fiber. Mol Biol Cell 9: 1919-1938, 1998.
33. 2+-calmodulin-dependent protein kinase II-dependent activation of contractility in ferret aorta. J Physiol 526: 367-374, 2000.
34. Klemke RL, Cai S, Giannini AL, Gallagher PJ, de Lanerolle P, and Cheresh DA. Regulation of cell motility by mitogen-activated protein kinase. J Cell Biol 137: 481-492, 1997.
35. Liu Y, Zhuang S, Guo H, Mabuchi K, Lu RC, and Wang CLA. The major myosin-binding site of caldesmon resides near its N-terminal extreme. J Biol Chem 275: 10989-10994, 2000.
36. Lo SK, Perlman MB, Niehaus GD, and Malik AB. Thrombin-induced alterations in lung fluid balance in awake sheep. J Appl Physiol 58: 1421-1427, 1985.
37. Marston SB and Huber PAJ. Biochemistry of Smooth Muscle Contraction, edited by Barany M and Barany K. San Diego, CA: Academic, 1996, p.77-90.
38. Morrison DL, Sanghera JS, Stewart J, Sutherland C, Walsh MP, and Pelech SL. Phosphorylation and activation of smooth muscle myosin light chain kinase by MAP kinase and cyclin-dependent kinase-1. Biochem Cell Biol 74: 549-557, 1996.
39. 2+-ATPase activity by caldesmon. J Biol Chem 259: 13656-13659, 1984.
40. Ngai PK and Walsh MP. The effects of phosphorylation of smooth muscle caldesmon. Biochem J 244: 417-425, 1987.
41. 2+ sensitivity in rabbit smooth muscle. J Physiol 487: 283-289, 1995.
42. Petrache I, Verin AD, Crow MT, Birukova A, Liu F, and Garcia JGN. Differential effect of MLC kinase in TNF-α-induced endothelial cell apoptosis and barrier dysfunction. Am J Physiol Lung Cell Mol Physiol 280: L1168-L1178, 2001.
43. Ramsby ML, Makowski GS, and Khairallah EA. Differential detergent fractionation of isolated hepatocytes: biochemical, immunochemical and two-dimensional gel electrophoresis characterization of cytoskeletal and noncytoskeletal compartments. Electrophoresis 15: 265-277, 1994.
44. Rokolya A and Singer HA. Inhibition of CaM kinase II activation and force maintenance by KN-93 in arterial smooth muscle. Am J Physiol Cell Physiol 278: C537-C545, 2000.
45. Seger R and Krebs EG. The MAPK signaling cascade. FASEB J 9: 726-735, 1995.
46. Sobue K and Sellers JR. Caldesmon, a novel regulatory protein in smooth muscle and nonmuscle actomyosin systems. J Biol Chem 266: 12115-12118, 1991.
47. Sutherland C and Walsh MP. Phosphorylation of caldesmon prevents its interaction with smooth muscle myosin. J Biol Chem 264: 578-583, 1989.
48. 2+ sensitivity of myosin light chain phosphorylation within smooth muscle cells. J Biol Chem 269: 9912-9920, 1994.
49. Tansey MG, Word RA, Hidaka H, Singer HA, Schworer CM, Kamm KE, and Stull JT. Phosphorylation of myosin light chain kinase by the multifunctional calmodulin-dependent protein kinase II in smooth muscle cells. J Biol Chem 267: 12511-12516, 1992.
50. Verin AD, Liu F, Bogatcheva N, Borbiev T, Hershenson MB, Wang P, and Garcia JGN. Role of Ras-dependent ERK activation in phorbol ester-induced endothelial cell barrier dysfunction. Am J Physiol Lung Cell Mol Physiol 279: L360-L370, 2000.
51. Wang Z and Yang ZQ. Casein kinase II phosphorylation of caldesmon downregulates myosin-caldesmon interactions. Biochemistry 39: 11114-11120, 2000.
52. Watts SW. Serotonin activates the mitogen-activated protein kinase pathway in vascular smooth muscle: use of the mitogen-activated protein kinase kinase inhibitor PD-098059. J Pharmacol Exp Ther 279: 1541-1550, 1996.
53. Wysolmerski RB and Lagunoff D. Involvement of myosin light-chain kinase in endothelial cell retraction. Proc Natl Acad Sci USA 87: 16-20, 1990.
54. Wysolmerski RB and Lagunoff D. Regulation of permeabilized endothelial cell retraction by myosin phosphorylation. Am J Physiol Cell Physiol 261: C32-C40, 1991.
55. Yamakita Y, Yamashiro S, and Matsumura F. Microinjection of nonmuscle and smooth muscle caldesmon into fibroblasts and muscle cells. J Cell Biol 111: 2487-2498, 1990.
56. Yamakita Y, Yamashiro S, and Matsumura F. Characterization of mitotically phosphorylated caldesmon. J Biol Chem 267: 12022-12029, 1992.
57. Yamashiro S, Chern H, Yamakita Y, and Matsumura F. Mutant caldesmon lacking cdc2 phosphorylation sites delays M-phase entry and inhibits cytokinesis. Mol Biol Cell 12: 239-250, 2001.