Endotoxin induces fibrosis in vascular endothelial cells through a mechanism dependent on transient receptor protein melastatin 7 activity

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Echeverría, Cesar ^a   Montorfano, Ignacio ^a   Hermosilla, Tamara ^c   Armisén, Ricardo ^c   Velásquez, Luis A ^a,d   Cabello Verrugio, Claudio ^a   Varela, Diego ^c   Simon, Felipe ^a,b  

^a UNIVERSIDAD ANDRÉS BELLO   (Chile)

^b Facultad de Medicina Universidad Andrés Bello   (Chile)

^c UNIVERSITY OF CHILE   (Chile)

^d CENTER FOR THE DEVELOPMENT OF NANOSCIENCE AND NANOTECHNOLOGY CEDENNA   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL; ENDOTOXIN; LIPOPOLYSACCHARIDE; MEMBRANE PROTEIN; TRANSIENT RECEPTOR POTENTIAL MELASTATIN 7; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; CALCIUM; SCLEROPROTEIN; TRANSIENT RECEPTOR POTENTIAL CHANNEL M; TRPM7 PROTEIN, HUMAN;

ARTICLE; CALCIUM CELL LEVEL; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; ENDOTOXEMIA; ENZYME ACTIVITY; ENZYME REPRESSION; EXTRACELLULAR MATRIX; FIBROBLAST; FIBROSIS; HUMAN; HUMAN CELL; MICROVASCULAR ENDOTHELIAL CELL; MOLECULAR IMAGING; PROTEIN EXPRESSION; PROTEIN FUNCTION; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; INTRACELLULAR SPACE; METABOLISM; PATHOLOGY; TOXICITY; UMBILICAL VEIN ENDOTHELIAL CELL;

BIOLOGICAL MARKERS; CALCIUM; ENDOTOXINS; EXTRACELLULAR MATRIX PROTEINS; FIBROBLASTS; FIBROSIS; GENE EXPRESSION REGULATION; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; INTRACELLULAR SPACE; LIPOPOLYSACCHARIDES; TRPM CATION CHANNELS;

EID: 84899414548     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0094146     Document Type: Article

References (63)

1. Riedemann NC, Guo RF, Ward PA (2003) The enigma of sepsis. J Clin Invest 112: 460-467. (Pubitemid 38056327)
2. Pinsky MR (2004) Dysregulation of the immune response in severe sepsis. Am J Med Sci 328: 220-229.
3. Rivers EP, Ahrens T (2008) Improving outcomes for severe sepsis and septic shock: tools for early identification of at-risk patients and treatment protocol implementation. Crit Care Clin 24: S1-47.
4. Winters BD, Eberlein M, Leung J, Needham DM, Pronovost PJ, et al. (2010) Long-term mortality and quality of life in sepsis: a systematic review. Crit Care Med 38: 1276-1283.
5. Schletter J, Heine H, Ulmer AJ, Rietschel ET (1995) Molecular mechanisms of endotoxin activity. Arch Microbiol 164: 383-389. (Pubitemid 26018509)
6. Peters K, Unger RE, Brunner J, Kirkpatrick CJ (2003) Molecular basis of endothelial dysfunction in sepsis. Cardiovasc Res 60: 49-57. (Pubitemid 38373475)
7. Grandel U, Grimminger F (2003) Endothelial responses to bacterial toxins in sepsis. Crit Rev Immunol 23: 267-299. (Pubitemid 37549551)
8. Karima R, Matsumoto S, Higashi H, Matsushima K (1999) The molecular pathogenesis of endotoxic shock and organ failure. Mol Med Today 5: 123-132. (Pubitemid 29282266)
9. Huet O, Dupic L, Harrois A, Duranteau J (2011) Oxidative stress and endothelial dysfunction during sepsis. Front Biosci 16: 1986-1995.
10. Simon F, Fernandez R (2009) Early lipopolysaccharide-induced reactive oxygen species production evokes necrotic cell death in human umbilical vein endothelial cells. J Hypertens 27: 1202-1216.
11. Dauphinee SM, Karsan A (2006) Lipopolysaccharide signaling in endothelial cells. Lab Invest 86: 9-22. (Pubitemid 43250964)
12. Matsuda N, Hattori Y (2007) Vascular biology in sepsis: pathophysiological and therapeutic significance of vascular dysfunction. J Smooth Muscle Res 43: 117-137.
13. Becerra A, Echeverria C, Varela D, Sarmiento D, Armisen R, et al. (2011) Transient receptor potential melastatin 4 inhibition prevents lipopolysaccharide-induced endothelial cell death. Cardiovasc Res 91: 677-684.
14. Echeverria C, Montorfano I, Sarmiento D, Becerra A, Nunez-Villena F, et al. (2013) Lipopolysaccharide induces a fibrotic-like phenotype in endothelial cells. J Cell Mol Med 17: 800-814.
15. Potenta S, Zeisberg E, Kalluri R (2008) The role of endothelial-to- mesenchymal transition in cancer progression. Br J Cancer 99: 1375-1379.
16. Zeisberg EM, Potenta S, Xie L, Zeisberg M, Kalluri R (2007) Discovery of endothelial to mesenchymal transition as a source for carcinoma-associated fibroblasts. Cancer Res 67: 10123-10128. (Pubitemid 350070783)
17. Kumaran C, Shivakumar K (2002) Calcium- and superoxide anion-mediated mitogenic action of substance P on cardiac fibroblasts. Am J Physiol Heart Circ Physiol 282: H1855-H1862. (Pubitemid 34654856)
18. Shivakumar K, Kumaran C (2001) L-type calcium channel blockers and EGTA enhance superoxide production in cardiac fibroblasts. J Mol Cell Cardiol 33: 373-377. (Pubitemid 32537934)
19. Yang KL, Chang WT, Chuang CC, Hung KC, Li EI (2008) Antagonizing TGFbeta induced liver fibrosis by a retinoic acid derivative through regulation of ROS and calcium influx. Biochem Biophys Res Commun 365: 484-489.
20. Cabello-Verrugio C, Acuna MJ, Morales MG, Becerra A, Simon F, et al. (2011) Fibrotic response induced by angiotensin-II requires NAD(P)H oxidase-induced reactive oxygen species (ROS) in skeletal muscle cells. Biochem Biophys Res Commun 410: 665-670.
21. Colston JT, Chandrasekar B, Freeman GL (2002) A novel peroxide-induced calcium transient regulates interleukin-6 expression in cardiac-derived fibroblasts. J Biol Chem 277: 23477-23483. (Pubitemid 34952182)
22. Tran PO, Hinman LE, Unger GM, Sammak PJ (1999) 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: 319-326. (Pubitemid 29393994)
23. Kimura C, Oike M, Koyama T, Ito Y (2001) Alterations of Ca2 + mobilizing properties in migrating endothelial cells. Am J Physiol Heart Circ Physiol 281: H745-H754.
24. Seccia TM, Maniero C, Belloni AS, Guidolin D, Pothen P, et al. (2008) Role of angiotensin II, endothelin-1 and L-type calcium channel in the development of glomerular, tubulointerstitial and perivascular fibrosis. J Hypertens 26: 2022-2029.
25. Matsuda H, Mori T, Kurumazuka D, Kitada K, Hayashi T, et al. (2011) Inhibitory effects of T/L-type calcium channel blockers on tubulointerstitial fibrosis in obstructed kidneys in rats. Urology 77: 249-15.
26. Mohamad HE, Askar ME, Hafez MM (2011) Management of cardiac fibrosis in diabetic rats; the role of peroxisome proliferator activated receptor gamma (PPAR-gamma) and calcium channel blockers (CCBs). Diabetol Metab Syndr 3: 4. 1758-5996
27. Ramires FJ, Sun Y, Weber KT (1998) Myocardial fibrosis associated with aldosterone or angiotensin II administration: attenuation by calcium channel blockade. J Mol Cell Cardiol 30: 475-483. (Pubitemid 28132727)
28. Ohyama T, Sato K, Kishimoto K, Yamazaki Y, Horiguchi N, et al. (2012) Azelnidipine is a calcium blocker that attenuates liver fibrosis and may increase antioxidant defence. Br J Pharmacol 165: 1173-1187.
29. Du J, Xie J, Zhang Z, Tsujikawa H, Fusco D, et al. (2010) TRPM7-mediated Ca2+ signals confer fibrogenesis in human atrial fibrillation. Circ Res 106: 992-1003.
30. Wei C, Wang X, Chen M, Ouyang K, Song LS, et al. (2009) Calcium flickers steer cell migration. Nature 457: 901-905.
31. Wei C, Wang X, Chen M, Ouyang K, Zheng M, et al. (2010) Flickering calcium microdomains signal turning of migrating cells. Can J Physiol Pharmacol 88: 105-110.
32. Monteilh-Zoller MK, Hermosura MC, Nadler MJ, Scharenberg AM, Penner R, et al. (2003) TRPM7 provides an ion channel mechanism for cellular entry of trace metal ions. J Gen Physiol 121: 49-60. (Pubitemid 36133936)
33. Nadler MJ, Hermosura MC, Inabe K, Perraud AL, Zhu Q, et al. (2001) LTRPC7 is a Mg.ATP-regulated divalent cation channel required for cell viability. Nature 411: 590-595. (Pubitemid 32531406)
34. Schmitz C, Perraud AL, Johnson CO, Inabe K, Smith MK, et al. (2003) Regulation of vertebrate cellular Mg2+ homeostasis by TRPM7. Cell 114: 191-200. (Pubitemid 36936913)
35. Simon F, Varela D, Cabello-Verrugio C (2013) Oxidative stress-modulated TRPM ion channels in cell dysfunction and pathological conditions in humans. Cell Signal 25: 1614-1624.
36. Clapham DE, Runnels LW, Strubing C (2001) The TRP ion channel family. Nat Rev Neurosci 2: 387-396. (Pubitemid 33674795)
37. Hermosilla T, Moreno C, Itfinca M, Altier C, Armisen R, et al. (2011) L-type calcium channel beta subunit modulates angiotensin II responses in cardiomyocytes. Channels (Austin) 5: 280-286.
38. Aarts M, Iihara K, Wei WL, Xiong ZG, Arundine M, et al. (2003) A key role for TRPM7 channels in anoxic neuronal death. Cell 115: 863-877. (Pubitemid 38058498)
39. Nunez-Villena F, Becerra A, Echeverria C, Briceno N, Porras O, et al. (2011) 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: 2425-2438.
40. Kozak JA, Cahalan MD (2003) MIC channels are inhibited by internal divalent cations but not ATP. Biophys J 84: 922-927.
41. Morales MG, Vazquez Y, Acuna MJ, Rivera JC, Simon F, et al. (2012) Angiotensin II-induced pro-fibrotic effects require p38MAPK activity and transforming growth factor beta 1 expression in skeletal muscle cells. Int J Biochem Cell Biol 44: 1993-2002.
42. Cabello-Verrugio C, Morales MG, Cabrera D, Vio CP, Brandan E (2012) Angiotensin II receptor type 1 blockade decreases CTGF/CCN2-mediated damage and fibrosis in normal and dystrophic skeletal muscles. J Cell Mol Med 16: 752-764.
43. Wykes RC, Lee M, Duffy SM, Yang W, Seward EP, et al. (2007) Functional transient receptor potential melastatin 7 channels are critical for human mast cell survival. J Immunol 179: 4045-4052.
44. Sahni J, Tamura R, Sweet IR, Scharenberg AM (2010) TRPM7 regulates quiescent/proliferative metabolic transitions in lymphocytes. Cell Cycle 9: 3565-3574.
45. Sun HS, Jackson MF, Martin LJ, Jansen K, Teves L, et al. (2009) Suppression of hippocampal TRPM7 protein prevents delayed neuronal death in brain ischemia. Nat Neurosci 12: 1300-1307.
46. Hermosura MC, Garruto RM (2007) TRPM7 and TRPM2-Candidate susceptibility genes for Western Pacific ALS and PD? Biochim Biophys Acta 1772: 822-835. (Pubitemid 47179881)
47. McNeill MS, Paulsen J, Bonde G, Burnight E, Hsu MY, et al. (2007) Cell death of melanophores in zebrafish trpm7 mutant embryos depends on melanin synthesis. J Invest Dermatol 127: 2020-2030. (Pubitemid 47075350)
48. Kim BJ, Nah SY, Jeon JH, So I, Kim SJ (2011) Transient receptor potential melastatin 7 channels are involved in ginsenoside Rg3-induced apoptosis in gastric cancer cells. Basic Clin Pharmacol Toxicol 109: 233-239.
49. Park HS, Chun JN, Jung HY, Choi C, Bae YS (2006) Role of NADPH oxidase 4 in lipopolysaccharide-induced proinflammatory responses by human aortic endothelial cells. Cardiovasc Res 72: 447-455. (Pubitemid 44665857)
50. Wuensch T, Thilo F, Krueger K, Scholze A, Ristow M, et al. (2010) High glucose-induced oxidative stress increases transient receptor potential channel expression in human monocytes. Diabetes 59: 844-849.
51. Runnels LW, Yue L, Clapham DE (2001) TRP-PLIK, a bifunctional protein with kinase and ion channel activities. Science 291: 1043-1047. (Pubitemid 32157413)
52. Berridge MJ, Bootman MD, Roderick HL (2003) Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 4: 517-529. (Pubitemid 36773404)
53. Targos B, Baranska J, Pomorski P (2005) Store-operated calcium entry in physiology and pathology of mammalian cells. Acta Biochim Pol 52: 397-409. (Pubitemid 41133774)
54. Marchand A, Abi-Gerges A, Saliba Y, Merlet E, Lompre AM (2012) Calcium signaling in vascular smooth muscle cells: from physiology to pathology. Adv Exp Med Biol 740: 795-810.
55. Simon F, Stutzin A (2008) Protein kinase C-mediated phosphorylation of p47 phox modulates platelet-derived growth factor-induced H2O2 generation and cell proliferation in human umbilical vein endothelial cells. Endothelium 15: 175-188.
56. Launay P, Cheng H, Srivatsan S, Penner R, Fleig A, et al. (2004) TRPM4 regulates calcium oscillations after T cell activation. Science 306: 1374-1377. (Pubitemid 39532514)
57. Launay P, Fleig A, Perraud AL, Scharenberg AM, Penner R, et al. (2002) TRPM4 is a Ca2+-activated nonselective cation channel mediating cell membrane depolarization. Cell 109: 397-407. (Pubitemid 34606881)
58. Nilius B, Prenen J, Droogmans G, Voets T, Vennekens R, et al. (2003) Voltage dependence of the Ca2+-activated cation channel TRPM4. J Biol Chem 278: 30813-30820. (Pubitemid 36994589)
59. Wynn TA (2008) Cellular and molecular mechanisms of fibrosis. J Pathol 214: 199-210.
60. Sorokin L (2010) The impact of the extracellular matrix on inflammation. Nat Rev Immunol 10: 712-723.
61. Hook M, McGavin MJ, Switalski LM, Raja R, Raucci G, et al. (1990) Interactions of bacteria with extracellular matrix proteins. Cell Differ Dev 32: 433-438.
62. Ivaska J, Heino J (2000) Adhesion receptors and cell invasion: mechanisms of integrin-guided degradation of extracellular matrix. Cell Mol Life Sci 57: 16-24. (Pubitemid 30105327)
63. Singh B, Fleury C, Jalalvand F, Riesbeck K (2012) Human pathogens utilize host extracellular matrix proteins laminin and collagen for adhesion and invasion of the host. FEMS Microbiol Rev 36: 1122-1180.