SLUG Is Expressed in Endothelial Cells Lacking Primary Cilia to Promote Cellular Calcification

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 35, Issue 3, 2015, Pages 616-627

  Sánchez Duffhues, Gonzalo ^a   De Vinuesa, Amaya García ^a   Lindeman, Jan H ^b   Mulder Stapel, Adri ^b   DeRuiter, Marco C ^a   Van Munsteren, Conny ^a   Goumans, Marie José ^a   Hierck, Beerend P ^a   Dijke, Peter Ten ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b Department of Vascular Surgery ^*  (Netherlands)

Author keywords

atherosclerosis; BMP receptor; cilia; transforming growth factors

Indexed keywords

BETA CATENIN; BONE MORPHOGENETIC PROTEIN 6; BONE MORPHOGENETIC PROTEIN RECEPTOR 1; CD31 ANTIGEN; COLLAGEN TYPE 1; COLLAGEN TYPE 1ALPHA; DECAPENTAPLEGIC PROTEIN; IFT88 PROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR; MESSENGER RNA; PROTEIN; SIP 1 PROTEIN; SMAD1 PROTEIN; SMAD4 PROTEIN; SMAD5 PROTEIN; SMAD8 PROTEIN; TRANSCRIPTION FACTOR OSTERIX; TRANSCRIPTION FACTOR RUNX2; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR TWIST; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA1 RECEPTOR; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL CADHERIN; VON WILLEBRAND FACTOR; BONE MORPHOGENETIC PROTEIN; CTNNB1 PROTEIN, MOUSE; RECEPTOR REGULATED SMAD PROTEIN; SNAIL FAMILY TRANSCRIPTION FACTORS; TG737RPW PROTEIN, MOUSE; TRANSCRIPTION FACTOR; TUMOR SUPPRESSOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATHEROSCLEROSIS; BLOOD VESSEL CALCIFICATION; CELL ACTIVATION; CELL COUNT; CELL DIFFERENTIATION; CELL FUNCTION; CELL STIMULATION; CELL TRANSDIFFERENTIATION; CONTROLLED STUDY; DISEASE COURSE; DOWN REGULATION; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME ACTIVITY; EUKARYOTIC FLAGELLUM; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; MINERALIZATION; MOUSE; NEOINTIMA; NONHUMAN; OSTEOBLAST; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; UPREGULATION; VASA VASORUM; ANIMAL; AORTA DISEASE; BONE DEVELOPMENT; CELL CULTURE; DEFICIENCY; DISEASE MODEL; GENETIC TRANSFECTION; GENETICS; KNOCKOUT MOUSE; METABOLISM; MUTANT MOUSE STRAIN; MUTATION; PATHOLOGY; PHOSPHORYLATION; UMBILICAL VEIN ENDOTHELIAL CELL;

ANIMALS; AORTIC DISEASES; ATHEROSCLEROSIS; BETA CATENIN; BONE MORPHOGENETIC PROTEINS; CELL TRANSDIFFERENTIATION; CELLS, CULTURED; CILIA; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MICE, KNOCKOUT; MICE, MUTANT STRAINS; MUTATION; OSTEOBLASTS; OSTEOGENESIS; PHOSPHORYLATION; RECEPTORS, LDL; SIGNAL TRANSDUCTION; SMAD PROTEINS, RECEPTOR-REGULATED; TRANSCRIPTION FACTORS; TRANSFECTION; TUMOR SUPPRESSOR PROTEINS; VASCULAR CALCIFICATION;

EID: 84922227983     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.115.305268     Document Type: Article

References (52)

1. Alexopoulos N, Raggi P, Calcification in atherosclerosis. Nat Rev Cardiol 2009 6 681 688. doi: 10.1038/nrcardio.2009.165
2. Johnson RC, Leopold JA, Loscalzo J, Vascular calcification: pathobiological mechanisms and clinical implications. Circ Res 2006 99 1044 1059. doi: 10.1161/01.RES.0000249379.55535.21
3. Doherty TM, Asotra K, Fitzpatrick LA, Qiao JH, Wilkin DJ, Detrano RC, Dunstan CR, Shah PK, Rajavashisth TB, Calcification in atherosclerosis: bone biology and chronic inflammation at the arterial crossroads. Proc Natl Acad Sci USA 2003 100 11201 11206. doi: 10.1073/pnas.1932554100
4. Boström K, Watson KE, Horn S, Wortham C, Herman IM, Demer LL, Bone morphogenetic protein expression in human atherosclrotic lesions. J Clin Invest 1993 91 1800 109. doi: 10.1172/JCI116391
5. Dhore CR, Cleutjens JP, Lutgens E, Cleutjens KB, Geusens PP, Kitslaar PJ, Tordoir JH, Spronk HM, Vermeer C, Daemen MJ, Differential expression of bone matrix regulatory proteins in human atherosclerotic plaques. Arterioscler Thromb Vasc Biol 2001 21 1998 2003
6. Miyazono K, Kamiya Y, Morikawa M, Bone morphogenetic protein receptors and signal transduction. J Biochem 2010 147 35 51. doi: 10.1093/jb/mvp148
7. Heldin CH, Miyazono K, ten Dijke P, TGF-β signalling from cell membrane to nucleus through SMAD proteins. Nature 1997 390 465 471. doi: 10.1038/37284
8. Hruska KA, Mathew S, Saab G, Bone morphogenetic proteins in vascular calcification. Circ Res 2005 97 105 114. doi: 10.1161/01.RES.00000175571.53833.6c
9. Sánchez-Duffhues G, García de Vinuesa A, ten Dijke P, Bone Morphogenetic Proteins Signal Transduction in Vascular Diseases 2012 New York, NY Nova Science Publishers 99 118
10. Hu Y, Zhang Z, Torsney E, Afzal AR, Davison F, Metzler B, Xu Q, Abundant progenitor cells in the adventitia contribute to atherosclerosis of vein grafts in ApoE-deficient mice. J Clin Invest 2004 113 1258 1265. doi: 10.1172/JCI19628
11. Shao JS, Cai J, Towler DA, Molecular mechanisms of vascular calcification: lessons learned from the aorta. Arterioscler Thromb Vasc Biol 2006 26 1423 1430. doi: 10.1161/01.ATV.0000220441.42041.20
12. Chen PY, Qin L, Barnes C, Charisse K, Yi T, Zhang X, Ali R, Medina PP, Yu J, Slack FJ, Anderson DG, Kotelianski V, Wang F, Tellides G, Simons M, FGF regulates TGF-β signaling and endothelial-to-mesenchymal transition via control of let-7 miRNA expression. Cell Rep 2012 2 1684 1696. doi: 10.1016/j.celrep.2012.10.021
13. Frid MG, Kale VA, Stenmark KR, Mature vascular endothelium can give rise to smooth muscle cells via endothelial-mesenchymal transdifferentiation: in vitro analysis. Circ Res 2002 90 1189 1196
14. Kumarswamy R, Volkmann I, Jazbutyte V, Dangwal S, Park DH, Thum T, Transforming growth factor-β-induced endothelial-to-mesenchymal transition is partly mediated by microRNA-21. Arterioscler Thromb Vasc Biol 2012 32 361 369. doi: 10.1161/ATVBAHA.111.234286
15. Mahler GJ, Farrar EJ, Butcher JT, Inflammatory cytokines promote mesenchymal transformation in embryonic and adult valve endothelial cells. Arterioscler Thromb Vasc Biol 2013 33 121 130. doi: 10.1161/ATVBAHA.112.300504
16. Yao Y, Jumabay M, Ly A, Radparvar M, Cubberly MR, Boström KI, A role for the endothelium in vascular calcification. Circ Res 2013 113 495 504. doi: 10.1161/CIRCRESAHA.113.301792
17. Saito A, EMT and EndMT: regulated in similar ways? J Biochem 2013 153 493 495. doi: 10.1093/jb/mvt032
18. Medici D, Potenta S, Kalluri R, Transforming growth factor-β2 promotes Snail-mediated endothelial-mesenchymal transition through convergence of Smad-dependent and Smad-independent signalling. Biochem J 2011 437 515 520. doi: 10.1042/BJ20101500
19. Medici D, Hay ED, Olsen BR, Snail and Slug promote epithelial-mesenchymal transition through beta-catenin-T-cell factor-4-dependent expression of transforming growth factor-beta3. Mol Biol Cell 2008 19 4875 4887. doi: 10.1091/mbc.E08-05-0506
20. Kokudo T, Suzuki Y, Yoshimatsu Y, Yamazaki T, Watabe T, Miyazono K, Snail is required for TGF-β-induced endothelial-mesenchymal transition of embryonic stem cell-derived endothelial cells. J Cell Sci 2008 121 Pt 20 3317 3324. doi: 10.1242/jcs.028282
21. Rieder F, Kessler SP, West GA, Bhilocha S, de la Motte C, Sadler TM, Gopalan B, Stylianou E, Fiocchi C, Inflammation-induced endothelial-to-mesenchymal transition: a novel mechanism of intestinal fibrosis. Am J Pathol 2011 179 2660 2673. doi: 10.1016/j.ajpath.2011.07.042
22. Brade T, Männer J, Kühl M, The role of Wnt signalling in cardiac development and tissue remodelling in the mature heart. Cardiovasc Res 2006 72 198 209. doi: 10.1016/j.cardiores.2006.06.025
23. Chang AC, Fu Y, Garside VC, Niessen K, Chang L, Fuller M, Setiadi A, Smrz J, Kyle A, Minchinton A, Marra M, Hoodless PA, Karsan A, Notch initiates the endothelial-to-mesenchymal transition in the atrioventricular canal through autocrine activation of soluble guanylyl cyclase. Dev Cell 2011 21 288 300. doi: 10.1016/j.devcel.2011.06.022
24. Lamouille S, Xu J, Derynck R, Molecular mechanisms of epithelial-mesenchymal transition. Nat Rev Mol Cell Biol 2014 15 178 196. doi: 10.1038/nrm3758
25. Xu J, Lamouille S, Derynck R, TGF-β-induced epithelial to mesenchymal transition. Cell Res 2009 19 156 172. doi: 10.1038/cr.2009.5
26. Medici D, Shore EM, Lounev VY, Kaplan FS, Kalluri R, Olsen BR, Conversion of vascular endothelial cells into multipotent stem-like cells. Nat Med 2010 16 1400 1406. doi: 10.1038/nm.2252
27. Nigro P, Abe J, Berk BC, Flow shear stress and atherosclerosis: a matter of site specificity. Antioxid Redox Signal 2011 15 1405 1414. doi: 10.1089/ars.2010.3679
28. Van der Heiden K, Hierck BP, Krams R, de Crom R, Cheng C, Baiker M, Pourquie MJ, Alkemade FE, DeRuiter MC, Gittenberger-de Groot AC, Poelmann RE, Endothelial primary cilia in areas of disturbed flow are at the base of atherosclerosis. Atherosclerosis 2008 196 542 550. doi: 10.1016/j.atherosclerosis.2007.05.030
29. Chaldakov GN, The ciliated smooth muscle and endothelial cell. Atherosclerosis 1985 56 251 256
30. Haust MD, Ciliated smooth muscle cells in atherosclerotic lesions of human aorta. Am J Cardiovasc Pathol 1987 1 115 129
31. Iomini C, Tejada K, Mo W, Vaananen H, Piperno G, Primary cilia of human endothelial cells disassemble under laminar shear stress. J Cell Biol 2004 164 811 817. doi: 10.1083/jcb.200312133
32. Malone AM, Anderson CT, Tummala P, Kwon RY, Johnston TR, Stearns T, Jacobs CR, Primary cilia mediate mechanosensing in bone cells by a calcium-independent mechanism. Proc Natl Acad Sci USA 2007 104 13325 13330. doi: 10.1073/pnas.0700636104
33. Bodle JC, Rubenstein CD, Phillips ME, Bernacki SH, Qi J, Banes AJ, Loboa EG, Primary cilia: the chemical antenna regulating human adipose-derived stem cell osteogenesis. PLoS One 2013 8 e62554. doi: 10.1371/journal.pone.0062554
34. Egorova AD, van der Heiden K, Poelmann RE, Hierck BP, Primary cilia as biomechanical sensors in regulating endothelial function. Differentiation 2012 83 S56 S61. doi: 10.1016/j.diff.2011.11.007
35. Berbari NF, O'Connor AK, Haycraft CJ, Yoder BK, The primary cillium as a complex signaling center. Curr Biol 2009 19 R526 R535. doi: 10.1016/j.cub.2009.05.025
36. Ishikawa H, Marshall WF, Ciliogenesis: building the cell's antenna. Nat Rev Mol Cell Biol 2011 12 222 234. doi: 10.1038/nrm3085
37. Ando J, Yamamoto K, Flow detection and calcium signaling in vascular endothelial cells. Cardiovasc Res 2013 99 260 268
38. Hierck BP, Van der Heiden K, Alkemade FE, Van de Pas S, Van Thienen JV, Groenendijk BC, Bax WH, Van der Laarse A, Deruiter MC, Horrevoets AJ, Poelmann RE, Primary cilia sensitize endothelial cells for fluid shear stress. Dev Dyn 2008 237 725 735. doi: 10.1002/dvdy.21472
39. Nauli SM, Kawanabe Y, Kaminski JJ, Pearce WJ, Ingber DE, Zhou J, Endothelial cilia are fluid shear sensors that regulate calcium signaling and nitric oxide production through polycystin-1. Circulation 2008 117 1161 1171. doi: 10.1161/CIRCULATIONAHA.107.710111
40. Egorova AD, Khedoe PP, Goumans MJ, Yoder BK, Nauli SM, ten Dijke P, Poelmann RE, Hierck BP, Lack of primary cilia primes shear-induced endothelial-to-mesenchymal transition. Circ Res 2011 108 1093 1101. doi: 10.1161/CIRCRESAHA.110.231860
41. Lehman JM, Michaud EJ, Schoeb TR, Aydin-Son Y, Miller M, Yoder BK, The Oak Ridge Polycystic Kidney mouse: modeling ciliopathies of mice and men. Dev Dyn 2008 237 1960 1971. doi: 10.1002/dvdy.21515
42. Aboualaiwi WA, Muntean BS, Ratnam S, Joe B, Liu L, Booth RL, Rodriguez I, Herbert BS, Bacallao RL, Fruttiger M, Mak TW, Zhou J, Nauli SM, Survivin-induced abnormal ploidy contributes to cystic kidney and aneurysm formation. Circulation 2014 129 660 672. doi: 10.1161/CIRCULATIONAHA.113.005746
43. Egorova AD, Van der Heiden K, Van de Pas S, Vennemann P, Poelma C, DeRuiter MC, Goumans MJ, Gittenberger-de Groot AC, ten Dijke P, Poelmann RE, Hierck BP, Tgfβ/Alk5 signaling is required for shear stress induced klf2 expression in embryonic endothelial cells. Dev Dyn 2011 240 1670 1680. doi: 10.1002/dvdy.22660
44. Moreno PR, Purushothaman KR, Fuster V, Echeverri D, Truszczynska H, Sharma SK, Badimon JJ, O'Connor WN, Plaque neovascularization is increased in ruptured atherosclerotic lesions of human aorta: implications for plaque vulnerability. Circulation 2004 110 2032 2038. doi: 10.1161/01.CIR.0000143233.87854.23
45. Libby P, Ridker PM, Hansson GK, Progress and challenges in translating the biology of atherosclerosis. Nature 2011 473 317 325. doi: 10.1038/nature10146
46. van Dijk RA, Engels CC, Schaapherder AF, Mulder-Stapel A, ten Dijke P, Hamming JF, Lindeman JH, Visualizing TGF-β and BMP signaling in human atherosclerosis: a histological evaluation based on Smad activation. Histol Histopathol 2012 27 387 396
47. Mulligan-Kehoe MJ, Simons M, Vasa vasorum in normal and diseased arteries. Circulation 2014 129 2557 2566. doi: 10.1161/CIRCULATIONAHA.113.007189
48. Virmani R, Kolodgie FD, Burke AP, Farb A, Schwartz SM, Lessons from sudden coronary death: a comprehensive morphological classification scheme for atherosclerotic lesions. Arterioscler Thromb Vasc Biol 2000 20 1262 1275
49. Derwall M, Malhotra R, Lai CS, Beppu Y, Aikawa E, Seehra JS, Zapol WM, Bloch KD, Yu PB, Inhibition of bone morphogenetic protein signaling reduces vascular calcification and atherosclerosis. Arterioscler Thromb Vasc Biol 2012 32 613 622. doi: 10.1161/ATVBAHA.111.242594
50. Chen PY, Qin L, Tellides G, Simons M, Fibroblast growth factor receptor 1 is a key inhibitor of TGF/β signaling in the endothelium. Sci Signal 2014 7 ra90. doi: 10.1126/scisignal.2005504
51. Liu D, Cui W, Liu B, Hu H, Liu J, Xie R, Yang X, Gu G, Zhang J, Zheng H, Atorvastatin protects vascular smooth muscle cells from TGF-β1-stimulated calcification by inducing autophagy via suppression of the β-catenin pathway. Cell Physiol Biochem 2014 33 129 141. doi: 10.1159/000356656
52. Qiao L, Nishimura T, Shi L, Sessions D, Thrasher A, Trudell JR, Berry GJ, Pearl RG, Kao PN, Endothelial fate mapping in mice with pulmonary hypertension. Circulation 2014 129 692 703. doi: 10.1161/CIRCULATIONAHA.113.003734