Over-expression of mitogen-activated protein kinase phosphatase-2 enhances adhesion molecule expression and protects against apoptosis in human endothelial cells

British Journal of Pharmacology

Volumn 161, Issue 4, 2010, Pages 782-798

  Al Mutairi, Mashael ^a   Al Harthi, Sameer ^a   Cadalbert, Laurence ^a   Plevin, Robin ^a  

^a UNIVERSITY OF STRATHCLYDE   (United Kingdom)

Author keywords

apoptosis; caspase; endothelial cell dysfunction; JNK; MAP kinase phosphatase 2

Indexed keywords

CASPASE 3; CELL ADHESION MOLECULE; HISTONE H2AX; I KAPPA B KINASE ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE PHOSPHATASE; MITOGEN ACTIVATED PROTEIN KINASE PHOSPHATASE 2; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1;

APOPTOSIS; ARTICLE; CELL DAMAGE; CONTROLLED STUDY; ENDOTHELIAL DYSFUNCTION; ENZYME ACTIVATION; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; WESTERN BLOTTING;

ADENOVIRIDAE; APOPTOSIS; CELLS, CULTURED; DUAL-SPECIFICITY PHOSPHATASES; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; GENE EXPRESSION; HUMANS; INTERCELLULAR ADHESION MOLECULE-1; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MITOGEN-ACTIVATED PROTEIN KINASE PHOSPHATASES; NF-KAPPA B; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA; UMBILICAL VEINS; VASCULAR CELL ADHESION MOLECULE-1;

EID: 77957224853     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2010.00952.x     Document Type: Article

References (64)

1. Albrecht EA, Sarma JV, Ward PA (2009). Activation by C5a of endothelial cell caspase 8 and cFLIP. Inflamm Res 58 : 30 37.
2. Bennett BL, Sasaki DT, Murray BW, O'Leary EC, Sakata ST, Xu W et al. (2001). SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc Natl Acad Sci U S A 98 : 13681 13686. (Pubitemid 33115958)
3. Cadalbert L, Sloss CM, Cameron P, Plevin R (2005). Conditional expression of MAP kinase phosphatase-2 protects against genotoxic stress-induced apoptosis by binding and selective dephosphorylation of nuclear activated c-Jun N-terminal kinase. Cell Signal 17 : 1254 1264. (Pubitemid 40982616)
4. Cameron P, Smith SJ, Giembycz MA, Rotondo D, Plevin R (2003). Verotoxin activates mitogen-activated protein kinase in human peripheral blood monocytes: role in apoptosis and proinflammatory cytokine release. Br J Pharmacol 140 : 1320 1330. (Pubitemid 38117437)
5. Chu Y, Solski PA, Khosravi-Far R, Der CJ, Kelly K (1996). The mitogen-activated protein kinase phosphatases PAC1, MKP-1, and MKP-2 have unique substrate specificities and reduced activity in vivo toward the ERK2 sevenmaker mutation. J Biol Chem 271 : 6497 6501. (Pubitemid 26095464)
6. Cines DB, Pollak ES, Buck CA, Loscalzo J, Zimmerman GA, McEver RP et al. (1998). Endothelial cells in physiology and in the pathophysiology of vascular disorders. Blood 91 : 3527 3561. (Pubitemid 28225719)
7. Daniel S, Arvelo MB, Patel VI, Longo CR, Shrikhande G, Shukri T et al. (2004). A20 protects endothelial cells from TNF-, Fas-, and NK-mediated cell death by inhibiting caspase 8 activation. Blood 104 : 2376 2384. (Pubitemid 39331836)
8. De Cesaris P, Starace D, Starace G, Filippini A, Stefanini M, Ziparo E (1999). Activation of Jun N-terminal kinase/stress-activated protein kinase pathway by tumor necrosis factor alpha leads to intercellular adhesion molecule-1 expression. J Biol Chem 274 : 28978 28982. (Pubitemid 29477054)
9. De Smaele E, Zazzeroni F, Papa S, Nguyen DU, Jin R, Jones J et al. (2001). Induction of gadd45beta by NF-kappaB downregulates pro-apoptotic JNK signalling. Nature 414 : 308 313. (Pubitemid 33097807)
10. Dhanasekaran DN, Reddy EP (2008). JNK signaling in apoptosis. Oncogene 27 : 6245 6251.
11. Esper RJ, Nordaby RA, Vilarino JO, Paragano A, Cacharron JL, Machado RA (2006). Endothelial dysfunction: a comprehensive appraisal. Cardiovasc Diabetol 5 : 4.
12. Fernandez-Capetillo O, Lee A, Nussenzweig M, Nussenzweig A (2004). H2AX: the histone guardian of the genome. DNA Repair (Amst) 3 : 959 967. (Pubitemid 38997938)
13. Fu YC, Yin SC, Chi CS, Hwang B, Hsu SL (2006). Norepinephrine induces apoptosis in neonatal rat endothelial cells via a ROS-dependent JNK activation pathway. Apoptosis 11 : 2053 2063. (Pubitemid 44691587)
14. George SJ, Baker AH, Angelini GD, Newby AC (1998a). Gene transfer of tissue inhibitor of metalloproteinase-2 inhibits metalloproteinase activity and neointima formation in human saphenous veins. Gene Ther 5 : 1552 1560. (Pubitemid 28517383)
15. George SJ, Johnson JL, Angelini GD, Newby AC, Baker AH (1998b). Adenovirus-mediated gene transfer of the human TIMP-1 gene inhibits smooth muscle cell migration and neointimal formation in human saphenous vein. Hum Gene Ther 9 : 867 877. (Pubitemid 28197373)
16. George SJ, Lloyd CT, Angelini GD, Newby AC, Baker AH (2000). Inhibition of late vein graft neointima formation in human and porcine models by adenovirus-mediated overexpression of tissue inhibitor of metalloproteinase-3. Circulation 101 : 296 304.
17. George SJ, Angelini GD, Capogrossi MC, Baker AH (2001). Wild-type p53 gene transfer inhibits neointima formation in human saphenous vein by modulation of smooth muscle cell migration and induction of apoptosis. Gene Ther 8 : 668 676.
18. Gomez AB, MacKenzie C, Paul A, Plevin R (2005). Selective inhibition of inhibitory kappa B kinase-beta abrogates induction of nitric oxide synthase in lipopolysaccharide-stimulated rat aortic smooth muscle cells. Br J Pharmacol 146 : 217 225. (Pubitemid 43079961)
19. Ho FM, Liu SH, Liau CS, Huang PJ, Lin-Shiau SY (2000). High glucose-induced apoptosis in human endothelial cells is mediated by sequential activations of c-Jun NH(2)-terminal kinase and caspase-3. Circulation 101 : 2618 2624.
20. Hosokawa Y, Hosokawa I, Ozaki K, Nakae H, Matsuo T (2006). Cytokines differentially regulate ICAM-1 and VCAM-1 expression on human gingival fibroblasts. Clin Exp Immunol 144 : 494 502. (Pubitemid 43799933)
21. Kamada S, Kikkawa U, Tsujimoto Y, Hunter T (2005). Nuclear translocation of caspase-3 is dependent on its proteolytic activation and recognition of a substrate-like protein(s). J Biol Chem 280 : 857 860.
22. Karahashi H, Michelsen KS, Arditi M (2009). Lipopolysaccharide-induced apoptosis in transformed bovine brain endothelial cells and human dermal microvessel endothelial cells: the role of JNK. J Immunol 182 : 7280 7286.
23. Keyse SM (2008). Dual-specificity MAP kinase phosphatases (MKPs) and cancer. Cancer Metastasis Rev 27 : 253 261.
24. Kinner A, Wu W, Staudt C, Iliakis G (2008). Gamma-H2AX in recognition and signaling of DNA double-strand breaks in the context of chromatin. Nucleic Acids Res 36 : 5678 5694.
25. Kobuchi H, Roy S, Sen CK, Nguyen HG, Packer L (1999). Quercetin inhibits inducible ICAM-1 expression in human endothelial cells through the JNK pathway. Am J Physiol 277 : C403 C411. (Pubitemid 29458175)
26. Lu C, Zhu F, Cho YY, Tang F, Zykova T, Ma WY et al. (2006). Cell apoptosis: requirement of H2AX in DNA ladder formation, but not for the activation of caspase-3. Mol Cell 23 : 121 132. (Pubitemid 43963445)
27. MacKenzie CJ, Ritchie E, Paul A, Plevin R (2007). IKKalpha and IKKbeta function in TNFalpha-stimulated adhesion molecule expression in human aortic smooth muscle cells. Cell Signal 19 : 75 80. (Pubitemid 44883366)
28. Mavria G, Vercoulen Y, Yeo M, Paterson H, Karasarides M, Marais R et al. (2006). ERK-MAPK signaling opposes rho-kinase to promote endothelial cell survival and sprouting during angiogenesis. Cancer Cell 9 : 33 44. (Pubitemid 43069509)
29. Min W, Pober JS (1997). TNF initiates E-selectin transcription in human endothelial cells through parallel TRAF-NF-kappa B and TRAF-RAC/CDC42-JNK-c-Jun/ ATF2 pathways. J Immunol 159 : 3508 3518. (Pubitemid 127482110)
30. Misra-Press A, Rim CS, Yao H, Roberson MS, Stork PJ (1995). A novel mitogen-activated protein kinase phosphatase. Structure, expression, and regulation. J Biol Chem 270 : 14587 14596.
31. Naderer T, McConville MJ (2008). The Leishmania-macrophage interaction: a metabolic perspective. Cell Microbiol 10 : 301 308.
32. Nakagami H, Morishita R, Yamamoto K, Yoshimura SI, Taniyama Y, Aoki M et al. (2001). Phosphorylation of p38 mitogen-activated protein kinase downstream of bax-caspase-3 pathway leads to cell death induced by high d-glucose in human endothelial cells. Diabetes 50 : 1472 1481. (Pubitemid 32500182)
33. Nicklin SA, White SJ, Nicol CG, Von Seggern DJ, Baker AH (2004). In vitro and in vivo characterisation of endothelial cell selective adenoviral vectors. J Gene Med 6 : 300 308. (Pubitemid 40228047)
34. Nieminen R, Leinonen S, Lahti A, Vuolteenaho K, Jalonen U, Kankaanranta H et al. (2005). Inhibitors of mitogen-activated protein kinases downregulate COX-2 expression in human chondrocytes. Mediators Inflamm 2005 : 249 255. (Pubitemid 41577414)
35. Nieminen R, Lahti A, Jalonen U, Kankaanranta H, Moilanen E (2006). JNK inhibitor SP600125 reduces COX-2 expression by attenuating mRNA in activated murine J774 macrophages. Int Immunopharmacol 6 : 987 996.
36. Papa S, Bubici C, Zazzeroni F, Pham CG, Kuntzen C, Knabb JR et al. (2006). The NF-kappaB-mediated control of the JNK cascade in the antagonism of programmed cell death in health and disease. Cell Death Differ 13 : 712 729.
37. Pintus G, Tadolini B, Posadino AM, Sanna B, Debidda M, Carru C et al. (2003). PKC/Raf/MEK/ERK signaling pathway modulates native-LDL-induced E2F-1 gene expression and endothelial cell proliferation. Cardiovasc Res 59 : 934 944. (Pubitemid 38366249)
38. Rahman A, Anwar KN, True AL, Malik AB (1999). Thrombin-induced p65 homodimer binding to downstream NF-kappa B site of the promoter mediates endothelial ICAM-1 expression and neutrophil adhesion. J Immunol 162 : 5466 5476. (Pubitemid 29307157)
39. Rahman A, Anwar KN, Minhajuddin M, Bijli KM, Javaid K, True AL et al. (2004). cAMP Targeting of p38 MAP kinase inhibits thrombin-induced NF-kappaB activation and ICAM-1 expression in endothelial cells. Am J Physiol Lung Cell Mol Physiol 287 : L1017 L1024. (Pubitemid 39391032)
40. Ramachandran A, Moellering D, Go YM, Shiva S, Levonen AL, Jo H et al. (2002). Activation of c-Jun N-terminal kinase and apoptosis in endothelial cells mediated by endogenous generation of hydrogen peroxide. Biol Chem 383 : 693 701. (Pubitemid 34506306)
41. Robinson CJ, Sloss CM, Plevin R (2001). Inactivation of JNK activity by mitogen-activated protein kinase phosphatase-2 in EAhy926 endothelial cells is dependent upon agonist-specific JNK translocation to the nucleus. Cell Signal 13 : 29 41. (Pubitemid 32222970)
42. Rosini P, De Chiara G, Bonini P, Lucibello M, Marcocci ME, Garaci E et al. (2004). Nerve growth factor-dependent survival of CESS B cell line is mediated by increased expression and decreased degradation of MAPK phosphatase 1. J Biol Chem 279 : 14016 14023. (Pubitemid 38468936)
43. Rossig L, Haendeler J, Mallat Z, Hugel B, Freyssinet JM, Tedgui A et al. (2000). Congestive heart failure induces endothelial cell apoptosis: protective role of carvedilol. J Am Coll Cardiol 36 : 2081 2089.
44. Rossig L, Dimmeler S, Zeiher AM (2001). Apoptosis in the vascular wall and atherosclerosis. Basic Res Cardiol 96 : 11 22. (Pubitemid 32117760)
45. Sabapathy K, Hu Y, Kallunki T, Schreiber M, David JP, Jochum W et al. (1999). JNK2 is required for efficient T-cell activation and apoptosis but not for normal lymphocyte development. Curr Biol 9 : 116 125. (Pubitemid 29087541)
46. Sanchez-Perez I, Benitah SA, Martinez-Gomariz M, Lacal JC, Perona R (2002). Cell stress and MEKK1-mediated c-Jun activation modulate NFkappaB activity and cell viability. Mol Biol Cell 13 : 2933 2945.
47. Scarabelli T, Stephanou A, Rayment N, Pasini E, Comini L, Curello S et al. (2001). Apoptosis of endothelial cells precedes myocyte cell apoptosis in ischemia/reperfusion injury. Circulation 104 : 253 256. (Pubitemid 32666943)
48. Scarabelli TM, Stephanou A, Pasini E, Comini L, Raddino R, Knight RA et al. (2002). Different signaling pathways induce apoptosis in endothelial cells and cardiac myocytes during ischemia/reperfusion injury. Circ Res 90 : 745 748. (Pubitemid 34640895)
49. Sharif F, Hynes SO, Cooney R, Howard L, McMahon J, Daly K et al. (2008). Gene-eluting stents: adenovirus-mediated delivery of eNOS to the blood vessel wall accelerates re-endothelialization and inhibits restenosis. Mol Ther 16 : 1674 1680.
50. Sloss CM, Cadalbert L, Finn SG, Fuller SJ, Plevin R (2005). Disruption of two putative nuclear localization sequences is required for cytosolic localization of mitogen-activated protein kinase phosphatase-2. Cell Signal 17 : 709 716. (Pubitemid 40250171)
51. Stehlik C, de Martin R, Kumabashiri I, Schmid JA, Binder BR, Lipp J (1998). Nuclear factor (NF)-kappaB-regulated X-chromosome-linked iap gene expression protects endothelial cells from tumor necrosis factor alpha-induced apoptosis. J Exp Med 188 : 211 216. (Pubitemid 28328620)
52. Suzuki T, Fukuo K, Suhara T, Yasuda O, Sato N, Takemura Y et al. (2003). Eicosapentaenoic acid protects endothelial cells against anoikis through restoration of cFLIP. Hypertension 42 : 342 348. (Pubitemid 37093483)
53. Tang G, Minemoto Y, Dibling B, Purcell NH, Li Z, Karin M et al. (2001). Inhibition of JNK activation through NF-kappaB target genes. Nature 414 : 313 317. (Pubitemid 33097808)
54. Tanner FC, Largiader T, Greutert H, Yang Z, Luscher TF (2004). Nitric oxide synthase gene transfer inhibits biological features of bypass graft disease in the human saphenous vein. J Thorac Cardiovasc Surg 127 : 20 26. (Pubitemid 38160461)
55. Tournier C, Hess P, Yang DD, Xu J, Turner TK, Nimnual A et al. (2000). Requirement of JNK for stress-induced activation of the cytochrome c-mediated death pathway. Science 288 : 870 874. (Pubitemid 30257738)
56. Tricot O, Mallat Z, Heymes C, Belmin J, Leseche G, Tedgui A (2000). Relation between endothelial cell apoptosis and blood flow direction in human atherosclerotic plaques. Circulation 101 : 2450 2453. (Pubitemid 30366245)
57. Wadgaonkar R, Pierce JW, Somnay K, Damico RL, Crow MT, Collins T et al. (2004). Regulation of c-Jun N-terminal kinase and p38 kinase pathways in endothelial cells. Am J Respir Cell Mol Biol 31 : 423 431. (Pubitemid 39330952)
58. Wang N, Verna L, Hardy S, Zhu Y, Ma KS, Birrer MJ et al. (1999). c-Jun triggers apoptosis in human vascular endothelial cells. Circ Res 85 : 387 393. (Pubitemid 29409615)
59. Wu G, Luo J, Rana JS, Laham R, Sellke FW, Li J (2006). Involvement of COX-2 in VEGF-induced angiogenesis via P38 and JNK pathways in vascular endothelial cells. Cardiovasc Res 69 : 512 519. (Pubitemid 43098807)
60. Xie D, Li Y, Reed EA, Odronic SI, Kontos CD, Annex BH (2006). An engineered vascular endothelial growth factor-activating transcription factor induces therapeutic angiogenesis in ApoE knockout mice with hindlimb ischemia. J Vasc Surg 44 : 166 175. (Pubitemid 43975290)
61. Yan W, Zhao K, Jiang Y, Huang Q, Wang J, Kan W et al. (2002). Role of p38 MAPK in ICAM-1 expression of vascular endothelial cells induced by lipopolysaccharide. Shock 17 : 433 438.
62. Yu PJ, Ferrari G, Pirelli L, Gulkarov I, Galloway AC, Mignatti P et al. (2007). Vascular injury and modulation of MAPKs: a targeted approach to therapy of restenosis. Cell Signal 19 : 1359 1371. (Pubitemid 46818925)
63. Yu Y, Sato JD (1999). MAP kinases, phosphatidylinositol 3-kinase, and p70 S6 kinase mediate the mitogenic response of human endothelial cells to vascular endothelial growth factor. J Cell Physiol 178 : 235 246. (Pubitemid 29034867)
64. Zhao J, Bolton EM, Bradley JA, Lever AM (2009). Lentiviral-mediated overexpression of Bcl-xL protects primary endothelial cells from ischemia/reperfusion injury-induced apoptosis. J Heart Lung Transplant 28 : 936 943.