Endotoxin-induced vascular endothelial cell migration is dependent on TLR4/NF-κB pathway, NAD(P)H oxidase activation, and transient receptor potential melastatin 7 calcium channel activity

International Journal of Biochemistry and Cell Biology

Volumn 55, Issue , 2014, Pages 11-23

  Sarmiento, Daniela ^a   Montorfano, Ignacio ^a   Cáceres, Mónica ^b   Echeverría, César ^a,d   Fernández, Ricardo ^a   Cabello Verrugio, Claudio ^a   Cerda, Oscar ^b   Tapia, Pablo ^c   Simon, Felipe ^a,e  

^a UNIVERSIDAD ANDRÉS BELLO   (Chile)

^b UNIVERSITY OF CHILE   (Chile)

^c PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^d UNIVERSIDAD BERNARDO O'HIGGINS   (Chile)

^e Pontificia Universidad Católica de Chile   (Chile)

Author keywords

Endothelial cell migration; Endothelial dysfunction; Inflammation; Lipopolysaccharide; TRPM7

Indexed keywords

2 AMINOETHOXYDIPHENYLBORANE; ACETYLCYSTEINE; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; APOCYNIN; CATALASE; CHELERYTHRINE; CLI 095; COLLAGEN; CRYSTAL VIOLET; DIPHENYLIODONIUM SALT; DITHIOTHREITOL; ENDOTOXIN; FOCAL ADHESION KINASE; GADOLINIUM; GADOLINIUM 3; I KAPPA B KINASE INHIBITOR; IKK 16; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOPOLYSACCHARIDE; MESSENGER RNA; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SMALL INTERFERING RNA; TOLL LIKE RECEPTOR 4; TRANSIENT RECEPTOR POTENTIAL CHANNEL M7; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL CADHERIN; WEDELOLACTONE; ZINC 2; ZINC ION; CALCIUM; PROTEIN KINASE C; PROTEIN SERINE THREONINE KINASE; REACTIVE OXYGEN METABOLITE; TLR4 PROTEIN, HUMAN; TRANSIENT RECEPTOR POTENTIAL CHANNEL M; TRPM7 PROTEIN, HUMAN; ALLOPURINOL; ROTENONE; XANTHINE OXIDASE;

ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL ADHESION; CELL ADHESION ASSAY; CELL ISOLATION; CELL MIGRATION; CELL MIGRATION ASSAY; CELL PROLIFERATION; CELL SPREADING; CELL VIABILITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; FLOW CYTOMETRY; FOCAL ADHESION; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; INTRACELLULAR SIGNALING; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIMARY CELL CULTURE; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; UMBILICAL VEIN ENDOTHELIAL CELL; VASCULAR ENDOTHELIUM; WESTERN BLOTTING; WOUND CLOSURE; BIOLOGICAL MODEL; CELL CULTURE; CELL MOTION; CYTOLOGY; DOSE RESPONSE; DRUG EFFECTS; GENETICS; METABOLISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; ENZYME INHIBITION; GENETIC TRANSFECTION;

BLOTTING, WESTERN; CALCIUM; CELL ADHESION; CELL MOVEMENT; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME ACTIVATION; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; LIPOPOLYSACCHARIDES; MODELS, BIOLOGICAL; NADPH OXIDASE; NF-KAPPA B; PROTEIN KINASE C; PROTEIN-SERINE-THREONINE KINASES; REACTIVE OXYGEN SPECIES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTORS; TOLL-LIKE RECEPTOR 4; TRPM CATION CHANNELS;

EID: 84906545194     PISSN: 13572725     EISSN: 18785875     Source Type: Journal    
DOI: 10.1016/j.biocel.2014.08.001     Document Type: Article

References (55)

1. M. Aarts, K. Iihara, W.L. Wei, Z.G. Xiong, M. Arundine, W. Cerwinski, J.F. MacDonald, and M. Tymianski A key role for TRPM7 channels in anoxic neuronal death Cell 115 2003 863 877 (Pubitemid 38058498)
2. E. Baldoli, S. Castiglioni, and J.A. Maier Regulation and function of TRPM7 in human endothelial cells: TRPM7 as a potential novel regulator of endothelial function PLoS One 8 2013 e59891
3. A. Becerra, C. Echeverria, D. Varela, D. Sarmiento, R. Armisen, F. Nunez-Villena, M. Montecinos, and F. Simon Transient receptor potential melastatin 4 inhibition prevents lipopolysaccharide-induced endothelial cell death Cardiovasc Res 91 2011 677 684
4. R.A. Brundage, K.E. Fogarty, R.A. Tuft, and F.S. Fay Calcium gradients underlying polarization and chemotaxis of eosinophils Science 254 1991 703 706 (Pubitemid 21917391)
5. L.A. Cary, J.F. Chang, and J.L. Guan Stimulation of cell migration by overexpression of focal adhesion kinase and its association with Src and Fyn J Cell Sci 109 Pt 7 1996 1787 1794 (Pubitemid 26248624)
6. H.C. Chen, P.A. Appeddu, H. Isoda, and J.L. Guan Phosphorylation of tyrosine 397 in focal adhesion kinase is required for binding phosphatidylinositol 3-kinase J Biol Chem 271 1996 26329 26334 (Pubitemid 26347485)
7. J.P. Chen, Y. Luan, C.X. You, X.H. Chen, R.C. Luo, and R. Li TRPM7 regulates the migration of human nasopharyngeal carcinoma cell by mediating Ca(2 +) influx Cell Calcium 47 2010 425 432
8. S.M. Dauphinee, A. Clayton, A. Hussainkhel, C. Yang, Y.J. Park, M.E. Fuller, J. Blonder, T.D. Veenstra, and A. Karsan SASH1 is a scaffold molecule in endothelial TLR4 signaling J Immunol 191 2013 892 901
9. S.M. Dauphinee, and A. Karsan Lipopolysaccharide signaling in endothelial cells Lab Invest 86 2006 9 22 (Pubitemid 43250964)
10. S. Dimmeler, S. Brinkmann, and E. Neugebauer Endotoxin-induced changes of endothelial cell viability and permeability: protective effect of a 21-aminosteroid Eur J Pharmacol 287 1995 257 261 (Pubitemid 26005582)
11. C. Echeverria, I. Montorfano, T. Hermosilla, R. Armisen, L.A. Velasquez, C. Cabello-Verrugio, D. Varela, and F. Simon Endotoxin Induces Fibrosis in Vascular Endothelial Cells through a Mechanism Dependent on Transient Receptor Protein Melastatin 7 Activity PLoS One 9 2014 e94146
12. C. Echeverria, I. Montorfano, D. Sarmiento, A. Becerra, F. Nunez-Villena, X.F. Figueroa, C. Cabello-Verrugio, A.A. Elorza, C. Riedel, and F. Simon Lipopolysaccharide induces a fibrotic-like phenotype in endothelial cells J Cell Mol Med 17 2013 800 814
13. B.L. Eide, C.W. Turck, and J.A. Escobedo Identification of Tyr-397 as the primary site of tyrosine phosphorylation and pp60src association in the focal adhesion kinase, pp125FAK Mol Cell Biol 15 1995 2819 2827
14. M.J. Goumans, A.J. van Zonneveld, and D.P. Ten Transforming growth factor beta-induced endothelial-to-mesenchymal transition: a switch to cardiac fibrosis Trends Cardiovasc Med 18 2008 293 298
15. U. Grandel, and F. Grimminger Endothelial responses to bacterial toxins in sepsis Crit Rev Immunol 23 2003 267 299 (Pubitemid 37549551)
16. M.C. Hermosura, M.K. Monteilh-Zoller, A.M. Scharenberg, R. Penner, and A. Fleig Dissociation of the store-operated calcium current I(CRAC) and the Mg-nucleotide-regulated metal ion current MagNuM J Physiol 539 2002 445 458 (Pubitemid 35175400)
17. R.S. Hotchkiss, and I.E. Karl The pathophysiology and treatment of sepsis N Engl J Med 348 2003 138 150 (Pubitemid 36056721)
18. O. Huet, L. Dupic, A. Harrois, and J. Duranteau Oxidative stress and endothelial dysfunction during sepsis Front Biosci 16 2011 1986 1995
19. K. Inoue, D. Branigan, and Z.G. Xiong Zinc-induced neurotoxicity mediated by transient receptor potential melastatin 7 channels J Biol Chem 285 2010 7430 7439
20. C. Kimura, M. Oike, T. Koyama, and Y. Ito Alterations of Ca2+ mobilizing properties in migrating endothelial cells Am J Physiol Heart Circ Physiol 281 2001 H745 H754
21. A. Kizu, D. Medici, and R. Kalluri Endothelial-mesenchymal transition as a novel mechanism for generating myofibroblasts during diabetic nephropathy Am J Pathol 175 2009 1371 1373
22. G. Kovacs, N. Montalbetti, A. Simonin, T. Danko, B. Balazs, A. Zsembery, and M.A. Hediger Inhibition of the human epithelial calcium channel TRPV6 by 2-aminoethoxydiphenyl borate (2-APB) Cell Calcium 52 2012 468 480
23. J.A. Kozak, and M.D. Cahalan MIC channels are inhibited by internal divalent cations but not ATP Biophys J 84 2003 922 927 (Pubitemid 36133418)
24. M. Lappas Anti-inflammatory properties of sirtuin 6 in human umbilical vein endothelial cells Mediators Inflamm 2012 2012 597514
25. C.A. Livasy, D. Moore, W.G. Cance, and R.A. Lininger Focal adhesion kinase overexpression in endometrial neoplasia Appl Immunohistochem Mol Morphol 12 2004 342 345 (Pubitemid 39602074)
26. A. Martini, R. Bruno, S. Mazzulla, A. Nocita, and G. Martino Angiotensin II regulates endothelial cell migration through calcium influx via T-type calcium channel in human umbilical vein endothelial cells Acta Physiol (Oxf) 198 2010 449 455
27. S.K. Mitra, D.A. Hanson, and D.D. Schlaepfer Focal adhesion kinase: in command and control of cell motility Nat Rev Mol Cell Biol 6 2005 56 68 (Pubitemid 40064899)
28. M.K. Monteilh-Zoller, M.C. Hermosura, M.J. Nadler, A.M. Scharenberg, R. Penner, and A. Fleig TRPM7 provides an ion channel mechanism for cellular entry of trace metal ions J Gen Physiol 121 2003 49 60 (Pubitemid 36133936)
29. M.J. Nadler, M.C. Hermosura, K. Inabe, A.L. Perraud, Q. Zhu, A.J. Stokes, T. Kurosaki, J.P. Kinet, R. Penner, A.M. Scharenberg, and A. Fleig LTRPC7 is a Mg.ATP-regulated divalent cation channel required for cell viability Nature 411 2001 590 595 (Pubitemid 32531406)
30. B. Nilius, G. Owsianik, T. Voets, and J.A. Peters Transient receptor potential cation channels in disease Physiol Rev 87 2007 165 217 (Pubitemid 46207713)
31. F. Nunez-Villena, A. Becerra, C. Echeverria, N. Briceno, O. Porras, R. Armisen, D. Varela, I. Montorfano, D. Sarmiento, and F. Simon Increased expression of the transient receptor potential melastatin 7 channel is critically involved in lipopolysaccharide-induced reactive oxygen species-mediated neuronal death Antioxid Redox Signal 15 2011 2425 2438
32. L.V. Owens, L. Xu, R.J. Craven, G.A. Dent, T.M. Weiner, L. Kornberg, E.T. Liu, and W.G. Cance Overexpression of the focal adhesion kinase (p125FAK) in invasive human tumors Cancer Res 55 1995 2752 2755
33. L.V. Owens, L. Xu, W.A. Marston, X. Yang, M.A. Farber, M.V. Iacocca, W.G. Cance, and B.A. Keagy Overexpression of the focal adhesion kinase (p125FAK) in the vascular smooth muscle cells of intimal hyperplasia J Vasc Surg 34 2001 344 349 (Pubitemid 33661134)
34. K. Peters, R.E. Unger, J. Brunner, and C.J. Kirkpatrick Molecular basis of endothelial dysfunction in sepsis Cardiovasc Res 60 2003 49 57 (Pubitemid 38373475)
35. S. Potenta, E. Zeisberg, and R. Kalluri The role of endothelial-to- mesenchymal transition in cancer progression Br J Cancer 99 2008 1375 1379
36. N.C. Riedemann, R.F. Guo, and P.A. Ward The enigma of sepsis J Clin Invest 112 2003 460 467 (Pubitemid 38056327)
37. L.W. Runnels, L. Yue, and D.E. Clapham The TRPM7 channel is inactivated by PIP(2) hydrolysis Nat Cell Biol 4 2002 329 336 (Pubitemid 34521027)
38. P. Rybarczyk, M. Gautier, F. Hague, I. Dhennin-Duthille, D. Chatelain, J. Kerr-Conte, F. Pattou, J.M. Regimbeau, H. Sevestre, and H. Ouadid-Ahidouch Transient receptor potential melastatin-related 7 channel is overexpressed in human pancreatic ductal adenocarcinomas and regulates human pancreatic cancer cell migration Int J Cancer 131 2012 E851 E861
39. Sarmiento D, Montorfano I, Cerda O, Caceres M, Becerra A, Cabello-Verrugio C, Elorza AA, Riedel C, Tapia P, Velasquez LA, Varela D, Simon F. Increases in reactive oxygen species enhance vascular endothelial cell migration through a mechanism dependent on the transient receptor potential melastatin 4 ion channel. Microvasc Res 2014. In press. http://dx.doi.org/10. 1016/j.mvr.2014.02.001.
40. D.D. Schlaepfer, C.R. Hauck, and D.J. Sieg Signaling through focal adhesion kinase Prog Biophys Mol Biol 71 1999 435 478 (Pubitemid 29156312)
41. D.D. Schlaepfer, and S.K. Mitra Multiple connections link FAK to cell motility and invasion Curr Opin Genet Dev 14 2004 92 101 (Pubitemid 38167483)
42. C. Schmitz, A.L. Perraud, C.O. Johnson, K. Inabe, M.K. Smith, R. Penner, T. Kurosaki, A. Fleig, and A.M. Scharenberg Regulation of vertebrate cellular Mg2+ homeostasis by TRPM7 Cell 114 2003 191 200 (Pubitemid 36936913)
43. D.J. Sieg, C.R. Hauck, D. Ilic, C.K. Klingbeil, E. Schaefer, C.H. Damsky, and D.D. Schlaepfer FAK integrates growth-factor and integrin signals to promote cell migration Nat Cell Biol 2 2000 249 256
44. F. Simon, and R. Fernandez Early lipopolysaccharide-induced reactive oxygen species production evokes necrotic cell death in human umbilical vein endothelial cells J Hypertens 27 2009 1202 1216
45. F. Simon, D. Varela, and C. Cabello-Verrugio Oxidative stress-modulated TRPM ion channels in cell dysfunction and pathological conditions in humans Cell Signal 25 2013 1614 1624
46. J.P. Thiery, H. Acloque, R.Y. Huang, and M.A. Nieto Epithelial- mesenchymal transitions in development and disease Cell 139 2009 871 890
47. K. Togashi, H. Inada, and M. Tominaga Inhibition of the transient receptor potential cation channel TRPM2 by 2-aminoethoxydiphenyl borate (2-APB) Br J Pharmacol 153 2008 1324 1330 (Pubitemid 351415500)
48. P.O. Tran, L.E. Hinman, G.M. Unger, and P.J. Sammak A wound-induced [Ca2 + ]i increase and its transcriptional activation of immediate early genes is important in the regulation of motility Exp Cell Res 246 1999 319 326 (Pubitemid 29393994)
49. J. Waning, J. Vriens, G. Owsianik, L. Stuwe, S. Mally, A. Fabian, C. Frippiat, B. Nilius, and A. Schwab A novel function of capsaicin-sensitive TRPV1 channels: involvement in cell migration Cell Calcium 42 2007 17 25 (Pubitemid 46760451)
50. C. Wei, X. Wang, M. Chen, K. Ouyang, L.S. Song, and H. Cheng Calcium flickers steer cell migration Nature 457 2009 901 905
51. C. Wei, X. Wang, M. Chen, K. Ouyang, M. Zheng, and H. Cheng Flickering calcium microdomains signal turning of migrating cells Can J Physiol Pharmacol 88 2010 105 110
52. Y. Wu, A.J. Palad, W.J. Wasilenko, P.F. Blackmore, W.A. Pincus, G.L. Schechter, J.R. Spoonster, E.C. Kohn, and K.D. Somers Inhibition of head and neck squamous cell carcinoma growth and invasion by the calcium influx inhibitor carboxyamido-triazole Clin Cancer Res 3 1997 1915 1921 (Pubitemid 27505116)
53. S. Yang, and X.Y. Huang Ca2+ influx through L-type Ca2+ channels controls the trailing tail contraction in growth factor-induced fibroblast cell migration J Biol Chem 280 2005 27130 27137 (Pubitemid 41040751)
54. N. Yoshikawa, H. Ariyoshi, Y. Aono, M. Sakon, T. Kawasaki, and M. Monden Gradients in cytoplasmic calcium concentration ([Ca2 + ]i) in migrating human umbilical vein endothelial cells (HUVECs) stimulated by shear-stress Life Sci 65 1999 2643 2651
55. E.M. Zeisberg, S. Potenta, L. Xie, M. Zeisberg, and R. Kalluri Discovery of endothelial to mesenchymal transition as a source for carcinoma-associated fibroblasts Cancer Res 67 2007 10123 10128 (Pubitemid 350070783)