Ramalin inhibits VCAM-1 expression and adhesion of monocyte to vascular smooth muscle cells through MAPK and PADI4-dependent NF-κB and AP-1 pathways

Bioscience, Biotechnology and Biochemistry

Volumn 79, Issue 4, 2015, Pages 539-552

  Park, Bongkyun ^a   Yim, Joung Han ^b   Lee, Hong Kum ^b   Kim, Byung Oh ^c   Pyo, Suhkneung ^a  

^a Sungkyunkwan University   (South Korea)

^b Korea Research Institute of Ships and Ocean Engineering   (South Korea)

^c Kyungpook National University   (South Korea)

Author keywords

Adhesion molecules; Inflammation; PADI4; Ramalin; Transcription factor

Indexed keywords

BIOMOLECULES; CELL ADHESION; CELL CULTURE; DISEASES; TRANSCRIPTION; TRANSCRIPTION FACTORS;

ADHESION MOLECULES; INFLAMMATION; MONOCYTIC LEUKEMIA CELLS; PADI4; RAMALIN; REACTIVE OXYGEN SPECIES; VASCULAR CELL ADHESION MOLECULE-1; VASCULAR SMOOTH MUSCLE CELLS;

MOLECULES;

RAMALINA;

ANTIOXIDANT; GLUTAMIC ACID DERIVATIVE; HYDROLASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MAPK1 PROTEIN, HUMAN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4; MITOGEN ACTIVATED PROTEIN KINASE P38; PEPTIDYLARGININE DEIMINASE TYPE IV; RAMALIN; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR AP 1; TUMOR NECROSIS FACTOR ALPHA; VASCULAR CELL ADHESION MOLECULE 1;

ANTAGONISTS AND INHIBITORS; CELL ADHESION; CELL LINE; COCULTURE; CYTOLOGY; DOSE RESPONSE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; LICHEN (ORGANISM); METABOLISM; MONOCYTE; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; VASCULAR SMOOTH MUSCLE;

ANTIOXIDANTS; CELL ADHESION; CELL LINE; COCULTURE TECHNIQUES; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION REGULATION; GLUTAMATES; HYDROLASES; LICHENS; MAP KINASE KINASE 4; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MONOCYTES; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NF-KAPPA B; P38 MITOGEN-ACTIVATED PROTEIN KINASES; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR AP-1; TUMOR NECROSIS FACTOR-ALPHA; VASCULAR CELL ADHESION MOLECULE-1;

EID: 84927647057     PISSN: 09168451     EISSN: 13476947     Source Type: Journal    
DOI: 10.1080/09168451.2014.991681     Document Type: Article

References (51)

1. Price DT, Loscalzo J. Cellular adhesion molecules and atherogenesis. Am. J. Med. 1999;107:85-97.
2. Lusis A. Atherosclerosis. Nature. 2000;407:233-241.
3. Owens GK, Kumar MS, Wamhoff BR. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol. Rev. 2004;84:767-801.
4. Falk E. Pathogenesis of atherosclerosis. J. Am. Coll. Cardiol. 2006;47:C7-C12.
5. Braun M, Pietsch P, Schror K, Baumann G, Felix SB. Cellular adhesion molecules on vascular smooth muscle cells. Cardiovasc. Res. 1999;41:395-401.
6. Jang Y, Lincoff AM, Plow EF, Topol EJ. Cell adhesion molecules in coronary artery disease. J. Am. Coll. Cardiol. 1994;24:1591-1601.
7. Libby P, Li H. Vascular cell adhesion molecule-1 and smooth muscle cell activation during atherogenesis. J. Clin. Invest. 1993;92:538-539.
8. Cybulsky MI, Iiyama K, Li H, Zhu S, Chen M, Iiyama M, Davis V, Gutierrez-Ramos JC, Connelly PW, Milstone DS. A major role for VCAM-1, but not ICAM-1, in early atherosclerosis. J. Clin. Invest. 2001;107:1255-1262.
9. Huo Y, Ley K. Adhesion molecules and atherogenesis. Acta Physiol. Scand. 2001;173:35-43.
10. Acuña UM, Atha DE, Ma J, Nee MH, Kennelly EJ. Antioxidant capacities of ten edible North American plants. Phytother. Res. 2002;16:63-65.
11. Smith RL. Growth and production of Poa flabellata in relation to soil nutrient status and exposure at South Georgia. Antarctic Nutr. Cycles Food Web. 1985;Part 2:221-228.
12. Choudhary MI, Jalil S. Bioactive phenolic compounds from a medicinal lichen Usnea longissima. Phytochemistry. 2005;66: 2346-2350.
13. Oksanen I. Ecological and biotechnological aspects of lichens. Appl. Microbiol. Biotechnol. 2006;73:723-734.
14. Paudel B, Bhattarai HD, Lee JS, Hong SG, Shin HW, Yim JH. Antibacterial potential of Antarctic lichens against human pathogenic gram-positive bacteria. Phytother. Res. 2008;22: 1269-1271.
15. Paudel B, Bhattarai HD, Koh HY, Lee SG, Han SJ, Lee HK, Oh H, Shin HW, Yim JH. Ramalin, a novel nontoxic antioxidant compound from the Antarctic lichen Ramalina terebrata. Phytomedicine. 2011;18:1285-1290.
16. ∅vstedal DO, Smith RL. Lichens of Antarctica and South Georgia: a guide to their identification and ecology. Cambridge University Press, Cambridge, UK, 2001.
17. Byeon H, Park B, Yim JH, Lee HK, Moon E, Rhee D, Pyo S. Stereocalpin A inhibits the expression of adhesion molecules in activated vascular smooth muscle cells. Int. Immunopharmacol. 2012;12:315-325.
18. 38 Kinase and c-Jun N-terminal kinase oppositely regulates tumor necrosis factor α-induced vascular cell adhesion molecule-1 expression and cell adhesion in chondrosarcoma cells. Int. Union Biochem. Mol. Biol. Life. 2002;54:293-299.
19. Lee SR, Kwak JH, Kim HJ, Pyo S. Neuroprotective effects of kobophenol A against the withdrawal of tropic support, nitrosative stress, and mitochondrial damage in SH-SY5Y neuroblastoma cells. Bioorg. Med. Chem. Lett. 2007;17:1879-1882.
20. Cho S, Kang N, Park S, Kim B, Rhee D, Pyo S. Induction of apoptosis and expression of apoptosis related genes in human epithelial carcinoma cells by Helicobacter pylori VacA toxin. Toxicon. 2003;42:601-611.
21. Xie QW, Whisnant R, Nathan C. Promoter of the mouse gene encoding calcium-independent nitric oxide synthase confers inducibility by interferon gamma and bacterial lipopolysaccharide. J. Exp. Med. 1993;177:1779-1784.
22. Minami T, Abid MR, Zhang J, King G, Kodama T, Aird WC. Thrombin stimulation of vascular adhesion molecule-1 in endothelial cells is mediated by protein kinase C (PKC)-delta -NF-kappa B and PKC-zeta-GATA signaling pathways. J. Biol. Chem. 2003;278:6976-6984.
23. Angel P, Karin M. The role of Jun, Fos and the AP-1 complex in cell-proliferation and transformation. Biochim. Biophys. Acta. 1991;1072:129-157.
24. Beg AA, Finco TS, Nantermet PV, Baldwin Jr. AS Tumor necrosis factor and interleukin-1 lead to phosphorylation and loss of I kappa B alpha: a mechanism for NF-kappa B activation. Mol. Cell. Biol. 1993;13:3301-3310.
25. Kim J, Park H, Um SH, Sohn E, Kim B, Moon E, Rhee D, Pyo S. Sulforaphane suppresses vascular adhesion molecule-1 expression in TNF-α-stimulated mouse vascular smooth muscle cells: involvement of the MAPK, NF-κB and AP-1 signaling pathways. Vasc. Pharmacol. 2012;56:131-141.
26. Yoon JJ, Lee YJ, Kim JS, Kang DG, Lee HS. Protective role of betulinic acid on TNF-α-induced cell adhesion molecules in vascular endothelial cells. Biochem. Biophys. Res. Commun. 2010;391:96-101.
27. Zhang H, Wang S. Notoginsenoside R1 inhibits TNF-α-induced fibronectin production in smooth muscle cells via the ROS/ERK pathway. Free Radical Biol. Med. 2006;40:1664-1674.
28. Aharoni-Simon M, Reifen R, Tirosh O. ROS-production-mediated activation of AP-1 but not NF- κB inhibits glutamateinduced HT4 neuronal cell death. Antioxid. Redox Signal. 2006;8:1339-1349.
29. Li P, Yao H, Zhang Z, Li M, Luo Y, Thompson PR, Gilmour DS, Wang Y. Regulation of p53 target gene expression by peptidylarginine deiminase 4. Cell Biol. 2008;28:4745-4758.
30. Jones JE, Causey CP, Knuckley B, Slack-Noyes JL, Thompson PR. Protein arginine deiminase 4 (PAD4): current understanding and future therapeutic potential. Curr. Opin. Drug Discovery Dev. 2009;12:616-627.
31. Luo Y, Arita K, Bhatia M, Knuckley B, Lee Y, Stallcup MR, Sato M, Thompson PR. Inhibitors and inactivators of protein arginine deiminase 4: functional and structural characterization. Biochemistry. 2006;45:11727-11736.
32. Barreiro O, Yanez-Mo M, Serrador JM, Montoya MC, Vicente-Manzanares M, Tejedor R, Furthmayr H, 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. 2002;157:1233-1245.
33. Ho AWY, Wong CK, Lam CWK. Tumor necrosis factor-α up-regulates the expression of CCL2 and adhesion molecules of human proximal tubular epithelial cells through MAPK signaling pathways. Immunobiology. 2008;213:533-544.
34. Rao GN, Delafontaine P, Runge MS. Thrombin stimulates phosphorylation of insulin-like growth factor-1 receptor, insulin receptor substrate-1, and phospholipase C-gamma 1 in rat aortic smooth muscle cells. J. Biol. Chem. 1995;270:27871-27875.
35. Law RE, Meehan WP, Xi XP, Graf K, Wuthrich DA, Coats W, Faxon D, Hsueh WA. Troglitazone inhibits vascular smooth muscle cell growth and intimal hyperplasia. J. Clin. Invest. 1996;98:1897-1905.
36. Hoshiya M, Awazu M. Trapidil inhibits platelet-derived growth factor-stimulated mitogen-activated protein kinase cascade. Hypertension. 1998;31:665-671.
37. Collins T, Read MA, Neish AS, Whitley MZ, Thanos D, Maniatis T. Transcriptional regulation of endothelial cell adhesion molecules: NF-kappa B and cytokine-inducible enhancers. J. Fed. Am. Soc. Exp. Biol. 1995;9:899-909.
38. Neish AS, Read MA, Thanos D, Pine R, Maniatis T, Collins T. Endothelial interferon regulatory factor 1 cooperates with NF-kappa B as a transcriptional activator of vascular cell adhesion molecule 1. Mol. Cell. Biol. 1995;15:2558-2569.
39. Neish AS, Khachigian LM, Park A, Baichwal VR, Collins T. Sp1 is a component of the cytokine-inducible enhancer in the promoter of vascular cell adhesion molecule-1. J. Biol. Chem. 1995;270:28903-28909.
40. Chen X, Dodd G, Kunsch C. Sulforaphane inhibits TNF-α-induced activation of p38 MAP kinase and VCAM-1 and MCP-1 expression in endothelial cells. Inflammation Res. 2009;58:513-521.
41. Sprague AH, Khalil RA. In flammatory cytokines in vascular dysfunction and vascular disease. Biochem. Pharmacol. 2009;78:539-552.
42. Kim HS, Loughran PA, Rao J, Billiar TR, Zuckerbraun BS. Carbon monoxide activates NF-kappaB via ROS generation and Akt pathways to protect against cell death of hepatocytes. Am. J. Physiol. Gastrointest. Liver Physiol. 2008;295:G146-G152.
43. Kisucka J, Chauhan AK, Patten IS, Yesilaltay A, Neumann C, Van Etten RA, Krieger M, Wagner DD. Peroxiredoxin1 prevents excessive endothelial activation and early atherosclerosis. Circ. Res. 2008;103:598-605.
44. Gosset P, Wallaert B, Tonnel A, Fourneau C. Thiol regulation of the production of TNF-α, IL-6 and IL-8 by human alveolar macrophages. Eur. Respir. J. 1999;14:98-105.
45. Gupta A, Rosenberger SF, Bowden GT. Increased ROS levels contribute to elevated transcription factor and MAP kinase activities in malignantly progressed mouse keratinocyte cell lines. Carcinogenesis. 1999;20:2063-2073.
46. Kunsch C, Medford RM. Oxidative stress as a regulator of gene expression in the vasculature. Circ. Res. 1999;85:753-766.
47. Griendling KK, Sorescu D, Lassegue B, Ushio-Fukai M. Modulation of protein kinase activity and gene expression by reactive oxygen species and their role in vascular physiology and pathophysiology. Arterioscler. Thromb. Vasc. Biol. 2000;20:2175-2183.
48. Guedes RP, Araújo AS, Janner D, Belló-Klein A, Ribeiro MFM, Partata WA. Increase in reactive oxygen species and activation of akt signaling pathway in neuropathic pain. Cell. Mol. Neurobiol. 2008;28:1049-1056.
49. Fan H, Sun B, Gu Q, Lafond-Walker A, Cao S, Becker LC. Oxygen radicals trigger activation of NF-kappaB and AP-1 and upregulation of ICAM-1 in reperfused canine heart. Am. J. Physiol. Heart Circ. Physiol. 2002;282:H1778-H1786.
50. Lee CW, Lin CC, Luo SF, Lee HC, Lee IT, Aird WC, Hwang TL, Yang CM. Tumor necrosis factor-alpha enhances neutrophil adhesiveness: induction of vascular cell adhesion molecule-1 via activation of Akt and CaM kinase II and modifications of histone acetyltransferase and histone deacetylase 4 in human tracheal smooth muscle cells. Mol. Pharmacol. 2008;73:1454-1464.
51. Rowlands DJ, Islam MN, Das SR, Huertas A, Quadri SK, Horiuchi K, Inamdar N, Emin MT, Lindert J, Ten VS, Bhattacharya S, Bhattacharya J. Activation of TNFR1 ectodomain shedding by mitochondrial Ca2+ determines the severity of inflammation in mouse lung microvessels. J. Clin. Invest. 2011;121:1986-1999.