Endothelial primary cilia inhibit atherosclerosis

EMBO Reports

Volumn 17, Issue 2, 2016, Pages 156-166

  Dinsmore, Colin ^a   Reiter, Jeremy F ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTRAFLAGELLAR TRANSPORT 88; PEPTIDES AND PROTEINS; UNCLASSIFIED DRUG; APOLIPOPROTEIN E; TG737RPW PROTEIN, MOUSE; TUMOR SUPPRESSOR PROTEIN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ATHEROSCLEROSIS; BLOOD VESSEL; CONTROLLED STUDY; DISEASE PREDISPOSITION; ENDOTHELIUM CELL; EUKARYOTIC FLAGELLUM; GENE DELETION; GENE EXPRESSION; MOUSE; NONHUMAN; PRIORITY JOURNAL; ADVERSE EFFECTS; ANIMAL; AORTA; CILIUM; FEMALE; GENETICS; LIPID DIET; MALE; METABOLISM; PATHOLOGY; PLAQUE, ATHEROSCLEROTIC; VASCULAR ENDOTHELIUM;

ANIMALS; AORTA; APOLIPOPROTEINS E; ATHEROSCLEROSIS; CILIA; DIET, HIGH-FAT; ENDOTHELIUM, VASCULAR; FEMALE; MALE; MICE; PLAQUE, ATHEROSCLEROTIC; TUMOR SUPPRESSOR PROTEINS;

EID: 84957428383     PISSN: 1469221X     EISSN: 14693178     Source Type: Journal    
DOI: 10.15252/embr.201541019     Document Type: Article

References (54)

1. Goetz SC, Anderson KV, (2010) The primary cilium: a signalling centre during vertebrate development. Nat Rev Genet 11: 331-344
2. Praetorius HA, (2015) The primary cilium as sensor of fluid flow: new building blocks to the model. Am J Physiol Cell Physiol 308: C198-C208
3. Praetorius HA, Spring KR, (2001) Bending the MDCK cell primary cilium increases intracellular calcium. J Membr Biol 184: 71-79
4. Praetorius HA, Frokiaer J, Nielsen S, Spring KR, (2003) Bending the primary cilium opens Ca2 + -sensitive intermediate-conductance K+ channels in MDCK cells. J Membr Biol 191: 193-200
5. Goetz JG, Steed E, Ferreira RR, Roth S, Ramspacher C, Boselli F, Charvin G, Liebling M, Wyart C, Schwab Y, et al, (2014) Endothelial cilia mediate low flow sensing during zebrafish vascular development. Cell Rep 6: 799-808
6. Hierck BP, Van Der Heiden K, Alkemade FE, Van de Pas S, Van Thienen JV, Groenendijk BCW, Bax WH, Van der Laarse A, Deruiter MC, Horrevoets AJG, et al, (2008) Primary cilia sensitize endothelial cells for fluid shear stress. Dev Dyn 237: 725-735
7. Nauli SM, Kawanabe Y, Kaminski JJ, Pearce WJ, Ingber DE, Zhou J, (2008) Endothelial cilia are fluid shear sensors that regulate calcium signaling and nitric oxide production through polycystin-1. Circulation 117: 1161-1171
8. Praetorius HA, Spring KR, (2003a) Removal of the MDCK cell primary cilium abolishes flow sensing. J Membr Biol 191: 69-76
9. Praetorius HA, Spring KR, (2003b) The renal cell primary cilium functions as a flow sensor. Curr Opin Nephrol Hypertens 12: 517-520
10. Van Der Heiden K, Hierck BP, Krams R, de Crom R, Cheng C, Baiker M, Pourquie MJBM, Alkemade FE, Deruiter MC, Gittenberger-De Groot AC, et al, (2008) Endothelial primary cilia in areas of disturbed flow are at the base of atherosclerosis. Atherosclerosis 196: 542-550
11. Caro CG, (2009) Discovery of the role of wall shear in atherosclerosis. Arterioscler Thromb Vasc Biol 29: 158-161
12. Suo J, Ferrara DE, Sorescu D, Guldberg RE, Taylor WR, Giddens DP, (2007) Hemodynamic shear stresses in mouse aortas: implications for atherogenesis. Arterioscler Thromb Vasc Biol 27: 346-351
13. Haycraft CJ, Zhang Q, Song B, Jackson WS, Detloff PJ, Serra R, Yoder BK, (2007) Intraflagellar transport is essential for endochondral bone formation. Development 134: 307-316
14. Braren R, Hu H, Kim YH, Beggs HE, Reichardt LF, Wang R, (2006) Endothelial FAK is essential for vascular network stability, cell survival, and lamellipodial formation. J Cell Biol 172: 151-162
15. White AC, Lavine KJ, Ornitz DM, (2007) FGF9 and SHH regulate mesenchymal Vegfa expression and development of the pulmonary capillary network. Development 134: 3743-3752
16. Mammoto A, Connor KM, Mammoto T, Yung CW, Huh D, Aderman CM, Mostoslavsky G, Smith LEH, Ingber DE, (2009) A mechanosensitive transcriptional mechanism that controls angiogenesis. Nature 457: 1103-1108
17. Yashiro K, Shiratori H, Hamada H, (2007) Haemodynamics determined by a genetic programme govern asymmetric development of the aortic arch. Nature 450: 285-288
18. Nicoli S, Standley C, Walker P, Hurlstone A, Fogarty KE, Lawson ND, (2010) MicroRNA-mediated integration of haemodynamics and Vegf signalling during angiogenesis. Nature 464: 1196-1200
19. Gimbrone MA, Topper JN, Nagel T, Anderson KR, Garcia-Cardena G, (2000) Endothelial dysfunction, hemodynamic forces, and atherogenesis. Ann N Y Acad Sci 902: 230-239 discussion 239-40.
20. Jones C, Roper VC, Foucher I, Qian D, Banizs B, Petit C, Yoder BK, Chen P, (2008) Ciliary proteins link basal body polarization to planar cell polarity regulation. Nat Genet 40: 69-77
21. Tkachenko E, Gutierrez E, Saikin SK, Fogelstrand P, Kim C, Groisman A, Ginsberg MH, (2013) The nucleus of endothelial cell as a sensor of blood flow direction. Biol Open 2: 1007-1012
22. Zadelaar S, Kleemann R, Verschuren L, de Vries-Van der Weij J, van der Hoorn J, Princen HM, Kooistra T, (2007) Mouse models for atherosclerosis and pharmaceutical modifiers. Arterioscler Thromb Vasc Biol 27: 1706-1721
23. Breslow JL, (1996) Mouse models of atherosclerosis. Science 272: 685-688
24. Finetti F, Paccani SR, Riparbelli MG, Giacomello E, Perinetti G, Pazour GJ, Rosenbaum JL, Baldari CT, (2009) Intraflagellar transport is required for polarized recycling of the TCR/CD3 complex to the immune synapse. Nat Cell Biol 11: 1332-1339
25. Hopkins PN, (2013) Molecular biology of Atherosclerosis. Physiol Rev 93: 1317-1542
26. Alam J, Cook JL, (2007) How many transcription factors does it take to turn on the heme oxygenase-1 gene? Am J Respir Cell Mol Biol 36: 166-174
27. AbouAlaiwi WA, Takahashi M, Mell BR, Jones TJ, Ratnam S, Kolb RJ, Nauli SM, (2009) Ciliary polycystin-2 is a mechanosensitive calcium channel involved in nitric oxide signaling cascades. Circ Res 104: 860-869
28. Garcia-Gonzalez MA, Outeda P, Zhou Q, Zhou F, Menezes LF, Qian F, Huso DL, Germino GG, Piontek KB, Watnick T, (2010) Pkd1 and Pkd2 Are required for normal placental development. PLoS ONE 5: e12821
29. Coxam B, Sabine A, Bower NI, Smith KA, Pichol-Thievend C, Skoczylas R, Astin JW, Frampton E, Jaquet M, Crosier PS, et al, (2014) Pkd1 regulates lymphatic vascular morphogenesis during development. Cell Rep 7: 623-633
30. Outeda P, Huso DL, Fisher SA, Halushka MK, Kim H, Qian F, Germino GG, Watnick T, (2014) Polycystin signaling is required for directed endothelial cell migration and lymphatic development. Cell Rep 7: 634-644
31. Ma M, Tian X, Igarashi P, Pazour GJ, Somlo S, (2013) Loss of cilia suppresses cyst growth in genetic models of autosomal dominant polycystic kidney disease. Nat Genet 45: 1004-1012
32. Kuhlencordt PJ, Gyurko R, Han F, Scherrer-Crosbie M, Aretz TH, Hajjar R, Picard MH, Huang PL, (2001) Accelerated atherosclerosis, aortic aneurysm formation, and ischemic heart disease in apolipoprotein E/endothelial nitric oxide synthase double-knockout mice. Circulation 104: 448-454
33. Vokes SA, Yatskievych TA, Heimark RL, McMahon J, Mcmahon AP, Antin PB, Krieg PA, (2004) Hedgehog signaling is essential for endothelial tube formation during vasculogenesis. Development 131: 4371-4380
34. Chinchilla P, Xiao L, Kazanietz MG, Riobo NA, (2010) Hedgehog proteins activate pro-angiogenic responses in endothelial cells through non-canonical signaling pathways. Cell Cycle 9: 570-579
35. Pola R, Ling LE, Silver M, Corbley MJ, Kearney M, Blake Pepinsky R, Shapiro R, Taylor FR, Baker DP, Asahara T, et al, (2001) The morphogen Sonic hedgehog is an indirect angiogenic agent upregulating two families of angiogenic growth factors. Nat Med 7: 706-711
36. Lawson ND, Vogel AM, Weinstein BM, (2002) sonic hedgehog and vascular endothelial growth factor act upstream of the Notch pathway during arterial endothelial differentiation. Dev Cell 3: 127-136
37. Alvarez JI, Dodelet-Devillers A, Kebir H, Ifergan I, Fabre PJ, Terouz S, Sabbagh M, Wosik K, Bourbonniere L, Bernard M, et al, (2011) The Hedgehog pathway promotes blood-brain barrier integrity and CNS immune quiescence. Science 334: 1727-1731
38. Williams C, Kim S-H, Ni TT, Mitchell L, Ro H, Penn JS, Baldwin SH, Solnica-Krezel L, Zhong TP, (2010) Hedgehog signaling induces arterial endothelial cell formation by repressing venous cell fate. Dev Biol 341: 196-204
39. Iomini C, Tejada K, Mo W, Vaananen H, Piperno G, (2004) Primary cilia of human endothelial cells disassemble under laminar shear stress. J Cell Biol 164: 811-817
40. Hahn C, Schwartz MA, (2009) Mechanotransduction in vascular physiology and atherogenesis. Nat Rev Mol Cell Biol 10: 53-62
41. Tzima E, Irani-Tehrani M, Kiosses WB, Dejana E, Schultz DA, Engelhardt B, Cao G, Delisser H, Schwartz MA, (2005) A mechanosensory complex that mediates the endothelial cell response to fluid shear stress. Nature 437: 426-431
42. Hoi Y, Zhou Y-Q, Zhang X, Henkelman RM, Steinman DA, (2011) Correlation between local hemodynamics and lesion distribution in a novel aortic regurgitation murine model of atherosclerosis. Ann Biomed Eng 39: 1414-1422
43. Haust MD, (1987) Endothelial cilia in human aortic atherosclerotic lesions. Virchows Arch A Pathol Anat Histopathol 410: 317-326
44. Bystrevskaya VB, Lichkun VV, Antonov AS, Perov NA, (1988) An ultrastructural study of centriolar complexes in adult and embryonic human aortic endothelial cells. Tissue Cell 20: 493-503
45. Bystrevskaya VB, Lichkun VV, Krushinsky AV, Smirnov VN, (1992) Centriole modification in human aortic endothelial cells. J Struct Biol 109: 1-12
46. Egorova AD, Khedoe PPSJ, Goumans M-JTH, Yoder BK, Nauli SM, Ten Dijke P, Poelmann RE, Hierck BP, (2011) Lack of primary cilia primes shear-induced endothelial-to-mesenchymal transition. Circ Res 108: 1093-1101
47. Ubil E, Duan J, Pillai ICL, Rosa-Garrido M, Wu Y, Bargiacchi F, Lu Y, Stanbouly S, Huang J, Rojas M, et al, (2014) Mesenchymal-endothelial transition contributes to cardiac neovascularization. Nature 514: 585-590
48. Sánchez-Duffhues G, de Vinuesa AG, Lindeman JH, Mulder-Stapel A, Deruiter MC, Van Munsteren C, Goumans MJ, Hierck BP, Ten Dijke P, (2015) SLUG is expressed in endothelial cells lacking primary cilia to promote cellular calcification. Arterioscler Thromb Vasc Biol 35: 616-627
49. Wann AK, Knight MM, (2012) Primary cilia elongation in response to interleukin-1 mediates the inflammatory response. Cell Mol Life Sci 69: 2967-2977
50. Wann AK, Thompson CL, Chapple JP, Knight MM, (2013) Interleukin-1β sequesters hypoxia inducible factor 2α to the primary cilium. Cilia 2: 17
51. Wann AK, Chapple JP, Knight MM, (2014) The primary cilium influences interleukin-1β-induced NFκB signalling by regulating IKK activity. Cell Signal 26: 1735-1742
52. Fernandez-Hernando C, Yu J, Suarez Y, Rahner C, Davalos A, Lasuncion MA, Sessa WC, (2009) Genetic evidence supporting a critical role of endothelial caveolin-1 during the progression of atherosclerosis. Cell Metab 10: 48-54
53. Ecder T, Schrier RW, (2009) Cardiovascular abnormalities in autosomal-dominant polycystic kidney disease. Nat Rev Nephrol 5: 221-228
54. Dudzinski DM, Michel T, (2007) Life history of eNOS: partners and pathways. Cardiovasc Res 75: 247-260