Deficiency of MAPK-activated protein kinase 2 (MK2) prevents adverse remodelling and promotes endothelial healing after arterial injury

Thrombosis and Haemostasis

Volumn 112, Issue 6, 2014, Pages 1264-1276

  Kapopara, Piyushkumar R ^a   von Felden, Johann ^a   Soehnlein, Oliver ^b,c,d   Wang, Yong ^a   Christian Napp, L ^a   Sonnenschein, Kristina ^a   Wollert, Kai C ^a   Schieffer, Bernhard ^a   Gaestel, Matthias ^a   Bauersachs, Johann ^a   Bavendiek, Udo ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

^d DZHK GERMAN CENTRE FOR CARDIOVASCULAR RESEARCH   (Germany)

Author keywords

Arterial remodelling; Inflammation; Leukocytes; MK2; Reendothelialisation

Indexed keywords

CCL2 PROTEIN, MOUSE; CCL5 PROTEIN, MOUSE; LOW DENSITY LIPOPROTEIN RECEPTOR; MAP-KINASE-ACTIVATED KINASE 2; MONOCYTE CHEMOTACTIC PROTEIN 1; PROTEIN SERINE THREONINE KINASE; RANTES; SIGNAL PEPTIDE;

ANIMAL; C57BL MOUSE; CAROTID ARTERY INJURY; CELL ADHESION; CELL CULTURE; CELL MOTION; CELL PROLIFERATION; COMMON CAROTID ARTERY; COMPLICATION; DEFICIENCY; DISEASE MODEL; ENZYMOLOGY; EPITHELIZATION; GENETICS; HYPERCHOLESTEROLEMIA; HYPERPLASIA; INFLAMMATION; INJURIES; KNOCKOUT MOUSE; LEUKOCYTE; METABOLISM; NEOINTIMA; PATHOLOGY; SMOOTH MUSCLE FIBER; VASCULAR ENDOTHELIUM; VASCULAR REMODELING; VASCULAR SMOOTH MUSCLE; WOUND HEALING;

ANIMALS; CAROTID ARTERY INJURIES; CAROTID ARTERY, COMMON; CELL ADHESION; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; CHEMOKINE CCL2; CHEMOKINE CCL5; DISEASE MODELS, ANIMAL; ENDOTHELIUM, VASCULAR; HYPERCHOLESTEROLEMIA; HYPERPLASIA; INFLAMMATION; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LEUKOCYTES; MICE, INBRED C57BL; MICE, KNOCKOUT; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NEOINTIMA; PROTEIN-SERINE-THREONINE KINASES; RE-EPITHELIALIZATION; RECEPTORS, LDL; VASCULAR REMODELING; WOUND HEALING;

EID: 84914165691     PISSN: 03406245     EISSN: None     Source Type: Journal    
DOI: 10.1160/TH14-02-0174     Document Type: Article

References (49)

1. Gibbons GH, Dzau VJ. The emerging concept of vascular remodelling. N Engl J Med 1994; 330: 1431–1438.
2. Otsuka F, Finn AV, Yazdani SK, et al. The importance of the endothelium in atherothrombosis and coronary stenting. Nat Rev Cardiol 2012; 9: 439–453.
3. Inoue T, Croce K, Morooka T, et al. Vascular inflammation and repair: implications for re-endothelialisation, restenosis, and stent thrombosis. JACC Cardiovasc Interv 2011; 4: 1057–1066.
4. Costa MA, Simon DI. Molecular basis of restenosis and drug-eluting stents. Circulation 2005; 111: 2257–2273.
5. Stokoe D, Campbell DG, Nakielny S, et al. MAPKAP kinase-2; a novel protein kinase activated by mitogen-activated protein kinase. EMBO J 1992; 11: 3985–3994.
6. Gaestel M. MAPKAP kinases – MKs – two's company, three's a crowd. Nat Rev Mol Cell Biol 2006; 7: 120–130.
7. Neininger A, Kontoyiannis D, Kotlyarov A, et al. MK2 targets AU-rich elements and regulates biosynthesis of tumor necrosis factor and interleukin-6 independently at different post-transcriptional levels. J Biol Chem 2002; 277: 3065–3068.
8. Kobayashi M, Nishita M, Mishima T, et al. MAPKAPK-2-mediated LIM-kinase activation is critical for VEGF-induced actin remodelling and cell migration. EMBO J 2006; 25: 713–726.
9. Kotlyarov A, Yannoni Y, Fritz S, et al. Distinct cellular functions of MK2. Mol Cell Biol 2002; 22: 4827–4835.
10. Manke IA, Nguyen A, Lim D, et al. MAPKAP kinase-2 is a cell cycle checkpoint kinase that regulates the G2/M transition and S phase progression in response to UV irradiation. Mol Cell 2005; 17: 37–48.
11. Kotlyarov A, Neininger A, Schubert C, et al. MAPKAP kinase 2 is essential for LPS-induced TNF-αα biosynthesis. Nat Cell Biol 1999; 1: 94–97.
12. Jagavelu K, Tietge UJF, Gaestel M, et al. Systemic Deficiency of the MAP Kinase-Activated Protein Kinase 2 Reduces Atherosclerosis in Hypercholestero-lemic Mice. Circ Res 2007; 101: 1104–1112.
13. Schober A, Manka D, von Hundeishausen P, et al. Deposition of Platelet RANTES Triggering Monocyte Recruitment Requires P-Selectin and Is Involved in Neointima Formation After Arterial Injury. Circulation 2002; 106: 1523–1529.
14. Lindner V, Fingerle J, Reidy MA. Mouse model of arterial injury. Circ Res 1993; 73: 792–796.
15. Brouchet L, Krust A, Dupont S, et al. Estradiol Accelerates Reendothelialisation in Mouse Carotid Artery Through Estrogen Receptor-a but Not Estrogen Receptor-β. Circulation 2001; 103: 423–428.
16. Soehnlein O, Wantha S, Simsekyilmaz S, et al. Neutrophil-Derived Cathelicidin Protects from Neointimal Hyperplasia. Sci Transl Med 2011; 3: 103ra198.
17. Hartwell DW, Mayadas TN, Berger G, et al. Role of P-selectin cytoplasmic domain in granular targeting in vivo and in early inflammatory responses. J Cell Biol 1998; 143: 1129–1141.
18. Grote K, Flach I, Luchtefeld M, et al. Mechanical stretch enhances mRNA expression and proenzyme release of matrix metalloproteinase-2 (MMP-2) via NAD(P)H oxidase-derived reactive oxygen species. Circ Res 2003; 92: e80–86.
19. Curcio A, Torella D, Indolfi C. Mechanisms of Smooth Muscle Cell Proliferation and Endothelial Regeneration After Vascular Injury and Stenting – Approach to Therapy -. Circ J 2011; 75: 1287–1296.
20. Van Belle E, Tio FO, Chen D, et al. Passivation of metallic stents after arterial gene transfer of phVEGF165 inhibits thrombus formation and intimai thickening. J Am Coll Cardiol 1997; 29: 1371–1379.
21. Carmeliet P, Moons L, Stassen JM, et al. Vascular wound healing and neointima formation induced by perivascular electric injury in mice. Am J Pathol 1997; 150: 761–776.
22. Manka DR, Wiegman P, Din S, et al. Arterial injury increases expression of inflammatory adhesion molecules in the carotid arteries of apolipoprotein-E-deficient mice. J Vasc Res 1999; 36: 372–378.
23. Schober A, Weber C. Mechanisms of monocyte recruitment in vascular repair after injury. Antioxid Redox Signal 2005; 7: 1249–1257.
24. Kovacic JC, Gupta R, Lee AC, et al. Stat3-dependent acute Rantes production in vascular smooth muscle cells modulates inflammation following arterial injury in mice. J Clin Invest 2010; 120: 303–314.
25. von Hundelshausen P, Weber KSC, Huo Y, et al. RANTES Deposition by Platelets Triggers Monocyte Arrest on Inflamed and Atherosclerotic Endothelium. Circulation 2001; 103: 1772–1777.
26. Schober A, Zernecke A, Liehn EA, et al. Crucial role of the CCL2/CCR2 axis in neointimal hyperplasia after arterial injury in hyperlipidemic mice involves early monocyte recruitment and CCL2 presentation on platelets. Circ Res 2004; 95: 1125–1133.
27. Liehn EA, Piccinini AM, Koenen RR, et al. A new monocyte chemotactic protein-1/chemokine CC motif ligand-2 competitor limiting neointima formation and myocardial ischemia/reperfusion injury in mice. J Am Coll Cardiol 2010; 56: 1847–1857.
28. Soehnlein O, Drechsler M, Doring Y, et al. Distinct functions of chemokine receptor axes in the atherogenic mobilisation and recruitment of classical monocytes. EMBO Mol Med 2013; 5: 471–481.
29. Zernecke A, Liehn EA, Gao JL, et al. Deficiency in CCR5 but not CCR1 protects against neointima formation in atherosclerosis-prone mice: involvement of IL-10. Blood 2006; 107: 4240–4243.
30. Gorska MM, Liang Q, Stafford SJ, et al. MK2 controls the level of negative feedback in the NF-kappaB pathway and is essential for vascular permeability and airway inflammation. J Exp Med 2007; 204: 1637–1652.
31. Clark AR, Dean JLE, Saklatvala J. Post-transcriptional regulation of gene expression by mitogen-activated protein kinase p38. FEBS Lett 2003; 546: 37–44.
32. Waterhouse CC, Joseph RR, Winsor GL, et al. Monocyte chemoattractant protein-1 production by intestinal epithelial cells in vitro: a role for p38 in epithelial chemokine expression. J Interferon Cytokine Res 2001; 21: 223–230.
33. Frevel MAE, Bakheet T, Silva AM, et al. p38 Mitogen-Activated Protein Kinase-Dependent and -Independent Signaling of mRNA Stability of AU-Rich Element-Containing Transcripts. Mol Cell Biol 2003; 23: 425–436.
34. Sauer I, Schaljo B, Vogl C, et al. Interferons limit inflammatory responses by induction of tristetraprolin. Blood 2006; 107: 4790–4797.
35. Stoecklin G, Stubbs T, Kedersha N, et al. MK2-induced tristetraprolin: 14-3-3 complexes prevent stress granule association and ARE-mRNA decay. EMBO J 2004; 23: 1313–1324.
36. King CA. Kaposi's sarcoma-associated herpesvirus kaposin B induces unique monophosphorylation of STAT3 at serine 727 and MK2-mediated inactivation of the STAT3 transcriptional repressor TRIM28. J Virol 2013; 87: 8779–8791.
37. Liu H, Ning H, Men H, et al. Regulation of CCL5 expression in smooth muscle cells following arterial injury. PLoS One 2012; 7: e30873.
38. Boettger T, Beetz N, Kostin S, et al. Acquisition of the contractile phenotype by murine arterial smooth muscle cells depends on the Mirl43/145 gene cluster. J Clin Invest 2009; 119: 2634–2647.
39. Owens GK, Kumar MS, Wamhoff BR. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev 2004; 84: 767–801.
40. Hedges JC, Dechert MA, Yamboliev IA, et al. A Role for p38MAPK/HSP27 Pathway in Smooth Muscle Cell Migration. J Biol Chem 1999; 274: 24211–24219.
41. Garcia-Cardena G, Comander J, Anderson KR, et al. Biomechanical activation of vascular endothelium as a determinant of its functional phenotype. Proc Natl Acad Sci USA 2001; 98: 4478–4485.
42. Proctor BM, Jin X, Lupu TS, et al. Requirement for p38 mitogen-activated protein kinase activity in neointima formation after vascular injury. Circulation 2008; 118: 658–666.
43. Kou B, Ni J, Vatish M, et al. Xanthine oxidase interaction with vascular endothelial growth factor in human endothelial cell angiogenesis. Microcirculation 2008; 15: 251–267.
44. de Olano N, Koo CY, Monteiro LJ, et al. The p38 MAPK-MK2 axis regulates E2F1 and FOXM1 expression after epirubicin treatment. Mol Cancer Res 2012; 10: 1189–1202.
45. Zachariadis M, Gorgoulis VG E2F1 (E2F transcription factor 1). Atlas Genet Cytogenet Oncol Haematol 2008; 812–816.
46. Roux PP, Blenis J. ERK and p38 MAPK-activated protein kinases: a family of protein kinases with diverse biological functions. Microbiol Mol Biol Rev 2004; 68: 320–344.
47. Aird WC. Endothelial cell heterogeneity. Cold Spring Harb Perspect Med 2012; 2: a006429.
48. Lacorre DA, Baekkevold ES, Garrido I, et al. Plasticity of endothelial cells: rapid dedifferentiation of freshly isolated high endothelial venule endothelial cells outside the lymphoid tissue microenvironment. Blood 2004; 103: 4164–4172.
49. Burridge KA, Friedman MH. Environment and vascular bed origin influence differences in endothelial transcriptional profiles of coronary and iliac arteries. Am J Physiol Heart Circ Physiol 2010; 299: H837–846.