Role for Primary Cilia as Flow Detectors in the Cardiovascular System

International Review of Cell and Molecular Biology

Volumn 290, Issue , 2011, Pages 87-119

  Van der Heiden, Kim ^a,b   Egorova, Anastasia D ^a   Poelmann, Robert E ^a   Wentzel, Jolanda J ^b   Hierck, Beerend P ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

Biomechanics; Cardiovascular system; Mechanosensation; Primary cilia; Shear stress; Signaling

Indexed keywords

ALPHA TUBULIN; AXONEMAL DYNEIN; BETA CATENIN; BETA TUBULIN; CALCIUM ION; ENDOTHELIAL NITRIC OXIDE SYNTHASE; ENDOTHELIN 1; GAMMA TUBULIN; KINESIN 2; KRUPPEL LIKE FACTOR 2; PLATELET DERIVED GROWTH FACTOR; POLYCYSTIN; SONIC HEDGEHOG PROTEIN; SURVIVIN; WNT PROTEIN;

AMINO ACID SEQUENCE; ANOSMIA; APOPTOSIS; ATHEROGENESIS; ATHEROSCLEROSIS; AXONEME; BIOMECHANICS; BLOOD FLOW; BLOOD FLOW VELOCITY; BLOOD PRESSURE; BLOOD VESSEL WALL; BOOK; CALCIUM TRANSPORT; CARBOXY TERMINAL SEQUENCE; CARDIOVASCULAR SYSTEM; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL CYCLE S PHASE; CELL FATE; CELL MATURATION; CELL MIGRATION; CELL MOTILITY; CELL NUCLEUS; CELL POLARITY; CELL PROLIFERATION; CELL TRANSPORT; CENTRIOLE; CENTROSOME; CILIOGENESIS; COMPUTATIONAL FLUID DYNAMICS; CONGENITAL MALFORMATION; DIABETES MELLITUS; ENDOTHELIUM CELL; EUKARYOTIC FLAGELLUM; GAP JUNCTION; GENE MUTATION; GOLGI COMPLEX; HEART CONTRACTION; HEART DEVELOPMENT; HEART HEMODYNAMICS; HUMAN; HYPERTENSION; IMMOTILE CILIUM; INTRACELLULAR SIGNALING; KARTAGENER SYNDROME; KIDNEY POLYCYSTIC DISEASE; KINETOSOME; LEUKOCYTE MIGRATION; MICROTUBULE; MICROTUBULE ORGANIZING CENTER; MITOSIS INHIBITION; MITOSIS SPINDLE; MOTILE CILIUM; NONHUMAN; OBESITY; OSCILLATION; OSTEOBLAST; OSTEOCYTE; PERCEPTION DEAFNESS; POLYPLOIDY; PRIMARY CILIUM; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RETINITIS PIGMENTOSA; SHEAR STRESS; SITUS INVERSUS; UPREGULATION; VASCULAR ENDOTHELIUM; VASCULARIZATION; VESTIBULAR DISORDER;

EID: 80052090159     PISSN: 19376448     EISSN: 19376448     Source Type: Book Series    
DOI: 10.1016/B978-0-12-386037-8.00004-1     Document Type: Chapter

References (177)

1. Abdul-Majeed S., Nauli S.M. Calcium-mediated mechanisms of cystic expansion. Biochim. Biophys. Acta 2010, DOI: 10.1016/j.bbad.2010.09.016, Epub.
2. AbouAlaiwi W.A., Takahashi M., Mell B.R., Jones T.J., Ratnam S., Kolb R.J., et al. Ciliary polycystin-2 is a mechanosensitive calcium channel involved in nitric oxide signaling cascades. Circ. Res. 2009, 104:860-869.
3. AbouAlaiwi W.A., Ratnam S., Booth R.L., Shah J.V., Nauli S.M. Endothelial cells from humans and mice with polycystic kidney disease are characterized by polyploidy and chromosome segregation defects through survivin down-regulation. Hum. Mol. Genet. 2011, 20:354-367.
4. Baiker M., Westerweel J., Hierck B.P. 3-D Visualisation of Chicken Embryo Vasculature. Assessment of Staining Methods for Geometric Vessel Reconstruction and Numerical Simulation of Blood Flow-Induced Wall Shear Stress 2009, VDM Verlag Dr. Müller Aktiengesellschaft & Co. KG, Saarbrücken, Germany.
5. Baker K., Beales P.L. Making sense of cilia in disease: the human ciliopathies. Am. J. Med. Genet. C Semin. Med. Genet. 2009, 151C:281-295.
6. Baker A.B., Groothuis A., Jonas M., Ettenson D.S., Shazly T., Zcharia E., et al. Heparanase alters arterial structure, mechanics, and repair following endovascular stenting in mice. Circ. Res. 2009, 104:380-387.
7. Banzi M., Aguiari G., Trimi V., Mangolini A., Pinton P., Witzgall R., et al. Polycystin-1 promotes PKCalpha-mediated NF-kappaB activation in kidney cells. Biochem. Biophys. Res. Commun. 2006, 350:257-262.
8. Baujat G., Le M.M. Ellis-van Creveld syndrome. Orphanet J. Rare Dis. 2007, 2:27.
9. Beales P.L., Elcioglu N., Woolf A.S., Parker D., Flinter F.A. New criteria for improved diagnosis of Bardet-Biedl syndrome: results of a population survey. J. Med. Genet. 1999, 36:437-446.
10. Beckers L., Heeneman S., Wang L., Burkly L.C., Rousch M.M., Davidson N.O., et al. Disruption of hedgehog signalling in ApoE-/- mice reduces plasma lipid levels, but increases atherosclerosis due to enhanced lipid uptake by macrophages. J. Pathol. 2007, 212:420-428.
11. Bell A. The pipe and the pinwheel: is pressure an effective stimulus for the 9+0 primary cilium?. Cell Biol. Int. 2008, 32:462-468.
12. Bergmann C., Fliegauf M., Bruchle N.O., Frank V., Olbrich H., Kirschner J., et al. Loss of nephrocystin-3 function can cause embryonic lethality, Meckel-Gruber-like syndrome, situs inversus, and renal-hepatic-pancreatic dysplasia. Am. J. Hum. Genet. 2008, 82:959-970.
13. Besschetnova T.Y., Kolpakova-Hart E., Guan Y., Zhou J., Olsen B.R., Shah J.V. Identification of signaling pathways regulating primary cilium length and flow-mediated adaptation. Curr. Biol. 2010, 20:182-187.
14. Birney Y.A., Sweeney C.H., Cappadona C.R., Sitzmann J.V., Cummins P.M., Redmond E.M., et al. Pulse pressure-induced transmural fluid flux increases bovine aortic smooth muscle cell apoptosis in a mitogen activated protein kinase dependent manner. J. Vasc. Res. 2004, 41:364-374.
15. Bisgrove B.W., Yost H.J. The roles of cilia in developmental disorders and disease. Development 2006, 133:4131-4143.
16. Blacque O.E., Li C., Inglis P.N., Esmail M.A., Ou G., Mah A.K., et al. The WD repeat-containing protein IFTA-1 is required for retrograde intraflagellar transport. Mol. Biol. Cell 2006, 17:5053-5062.
17. Bystrevskaya V.B., Lichkun V.V., Antonov A.S., Perov N.A. An ultrastructural study of centriolar complexes in adult and embryonic human aortic endothelial cells. Tissue Cell 1988, 20:493-503.
18. Califano J.P., Reinhart-King C.A. Exogenous and endogenous force regulation of endothelial cell behavior. J. Biomech. 2010, 43:79-86.
19. Cappadona C., Redmond E.M., Theodorakis N.G., McKillop I.H., Hendrickson R., Chhabra A., et al. Phenotype dictates the growth response of vascular smooth muscle cells to pulse pressure in vitro. Exp. Cell Res. 1999, 250:174-186.
20. Chauvet V., Tian X., Husson H., Grimm D.H., Wang T., Hiesberger T., et al. Mechanical stimuli induce cleavage and nuclear translocation of the polycystin-1 C terminus. J. Clin. Invest. 2004, 114:1433-1443.
21. Chen C.P. Meckel syndrome: genetics, perinatal findings, and differential diagnosis. Taiwan. J. Obstet. Gynecol. 2007, 46:9-14.
22. Chen Q., Li W., Quan Z., Sumpio B.E. Modulation of vascular smooth muscle cell alignment by cyclic strain is dependent on reactive oxygen species and P38 mitogen-activated protein kinase. J. Vasc. Surg. 2003, 37:660-668.
23. Cheng C., Tempel D., van Haperen R., van der B.A., Grosveld F., Daemen M.J., et al. Atherosclerotic lesion size and vulnerability are determined by patterns of fluid shear stress. Circulation 2006, 113:2744-2753.
24. Cheng C., Helderman F., Tempel D., Segers D., Hierck B.P., Poelmann R.E., et al. Large variations in absolute wall shear stress levels within one species and between species. Atherosclerosis 2007, 195:225-235.
25. Cohen M.M. Hedgehog signaling update. Am. J. Med. Genet. 2010, 152A:1875-1914.
26. Corbit K.C., Aanstad P., Singla V., Norman A.R., Stainier D.Y., Reiter J.F. Vertebrate smoothened functions at the primary cilium. Nature 2005, 437:1018-1021.
27. Corbit K.C., Shyer A.E., Dowdle W.E., Gaulden J., Singla V., Reiter J.F. Kif3a constrains beta-catenin-dependent Wnt signalling through dual ciliary and non-ciliary mechanisms. Nat. Cell Biol. 2008, 10:70-76.
28. Cuhlmann S., Van der Heiden K., Saliba D., Tremoleda J.L., Khalil M., Zakkar M., et al. Disturbed blood flow induces RelA expression via c-Jun N-terminal kinase 1: a novel mode of NF-{kappa}B regulation that promotes arterial inflammation. Circ. Res. 2011, 108:950-959.
29. Cunningham K.S., Gotlieb A.I. The role of shear stress in the pathogenesis of atherosclerosis. Lab. Invest. 2005, 85:9-23.
30. D'Angelo A., Franco B. The dynamic cilium in human diseases. Pathogenetics 2009, 2:3.
31. Dai G., Kaazempur-Mofrad M.R., Natarajan S., Zhang Y., Vaughn S., Blackman B.R., et al. Distinct endothelial phenotypes evoked by arterial waveforms derived from atherosclerosis-susceptible and -resistant regions of human vasculature. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:14871-14876.
32. Davies P.F. Flow-mediated endothelial mechanotransduction. Physiol. Rev. 1995, 75:519-560.
33. Davis E.E., Brueckner M., Katsanis N. The emerging complexity of the vertebrate cilium: new functional roles for an ancient organelle. Dev. Cell 2006, 11:9-19.
34. Dawe H.R., Farr H., Gull K. Centriole/basal body morphogenesis and migration during ciliogenesis in animal cells. J. Cell Sci. 2007, 120:7-15.
35. Deane J.A., Cole D.G., Seeley E.S., Diener D.R., Rosenbaum J.L. Localization of intraflagellar transport protein IFT52 identifies basal body transitional fibers as the docking site for IFT particles. Curr. Biol. 2001, 11:1586-1590.
36. Dejana E. The role of Wnt signaling in physiological and pathological angiogenesis. Circ. Res. 2010, 107:943-952.
37. Dekker R.J., Van Soest S., Fontijn R.D., Salamanca S., de Groot P.G., VanBavel E., et al. Prolonged fluid shear stress induces a distinct set of endothelial cell genes, most specifically lung Krüppel-like factor (KLF2). Blood 2002, 100:1689-1698.
38. Dekker R.J., van Thienen J.V., Elderkamp Y.W., Seppen J., de Vries C.J.M., Biessen E.A.L., et al. Endothelial KLF2 links local arterial shear stress levels to the expression of vascular-tone regulating genes. Am. J. Pathol. 2005, 167:609-618.
39. Dekker R.J., Boon R.A., Rondaij M.G., Kragt A., Volger O.L., Elderkamp Y.W., et al. KLF2 provokes a gene expression pattern that establishes functional quiescent differentiation of the endothelium. Blood 2006, 107:4354-4363.
40. Doxsey S. Re-evaluating centrosome function. Nat. Rev. Mol. Cell Biol. 2001, 2:688-698.
41. Ecder T., Schrier R.W. Cardiovascular abnormalities in autosomal-dominant polycystic kidney disease. Nat. Rev. Nephrol. 2009, 5:221-228.
42. Egorova A.D., Khedoe P.P., Goumans M.J., Yoder B.K., Nauli S.M., ten Dijke P., et al. Lack of primary cilia primes shear-induced endothelial-to-mesenchymal transition. Circ. Res. 2011, 108:1093-1101.
43. Elbedour K., Zucker N., Zalzstein E., Barki Y., Carmi R. Cardiac abnormalities in the Bardet-Biedl syndrome: echocardiographic studies of 22 patients. Am. J. Med. Genet. 1994, 52:164-169.
44. Elmali M., Ozmen Z., Ceyhun M., Tokatlioglu O., Incesu L., Diren B. Joubert syndrome with atrial septal defect and persistent left superior vena cava. Diagn. Interv. Radiol. 2007, 13:94-96.
45. Feistel K., Blum M. Three types of cilia including a novel 9+4 axoneme on the notochordal plate of the rabbit embryo. Dev. Dyn. 2006, 235:3348-3358.
46. Ferrante M.I., Romio L., Castro S., Collins J.E., Goulding D.A., Stemple D.L., et al. Convergent extension movements and ciliary function are mediated by ofd1, a zebrafish orthologue of the human oral-facial-digital type 1 syndrome gene. Hum. Mol. Genet. 2009, 18:289-303.
47. Fischer E., Pontoglio M. Planar cell polarity and cilia. Semin. Cell Dev. Biol. 2009, 20:998-1005.
48. Florian J.A., Kosky J.R., Ainslie K., Pang Z.Y., Dull R.O., Tarbell J.M. Heparan sulfate proteoglycan is a mechanosensor on endothelial cells. Circ. Res. 2003, 93:E136-E142.
49. Fuchs E., Karakesisoglou I. Bridging cytoskeletal intersections. Genes Dev. 2001, 15:1-14.
50. Fuller S.D., Gowen B.E., Reinsch S., Sawyer A., Buendia B., Wepf R., et al. The core of the mammalian centriole contains gamma-tubulin. Curr. Biol. 1995, 5:1384-1393.
51. Gallagher B.C. Primary cilia of the corneal endothelium. Am. J. Anat. 1980, 159:475-484.
52. Germino G.G. Linking cilia to Wnts. Nat. Genet. 2005, 37:455-457.
53. Gittenberger-de Groot A.C., Vrancken Peeters M.P.F.M., Mentink M.M.T., Gourdie R.G., Poelmann R.E. Epicardium-derived cells contribute a novel population to the myocardial wall and the atrioventricular cushions. Circ. Res. 1998, 82:1043-1052.
54. Gittenberger-de Groot A.C., Jongbloed M.R.M., DeRuiter M.C., Bartelings M.M., Poelmann R.E. Embryology of congenital heart disease. Cardiology 2010, 1391-1402. Mosby, Philadelphia. M.H. Crawford, J.P. DiMarco, W.J. Paulus (Eds.).
55. Goetz S.C., Anderson K.V. The primary cilium: a signalling centre during vertebrate development. Nat. Rev. Genet. 2010, 11:331-344.
56. Gonzalez-Perrett S., Kim K., Ibarra C., Damiano A.E., Zotta E., Batelli M., et al. Polycystin-2, the protein mutated in autosomal dominant polycystic kidney disease (ADPKD), is a Ca2+-permeable nonselective cation channel. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:1182-1187.
57. Gouverneur M., Berg B., Nieuwdorp M., Stroes E., Vink H. Vasculoprotective properties of the endothelial glycocalyx: effects of fluid shear stress. J. Intern. Med. 2006, 259:393-400.
58. Gouverneur M., Spaan J.A., Pannekoek H., Fontijn R.D., Vink H. Fluid shear stress stimulates incorporation of hyaluronan into endothelial cell glycocalyx. Am. J. Physiol. Heart Circ. Physiol. 2006, 290:H458-H462.
59. Griffin M.D., Torres V.E., Grande J.P., Kumar R. Vascular expression of polycystin. J. Am. Soc. Nephrol. 1997, 8:616-626.
60. Groen H.C., Gijsen F.J., van der Lugt A., Ferguson M.S., Hatsukami T.S., van der Steen A.F., et al. Plaque rupture in the carotid artery is localized at the high shear stress region: a case report. Stroke 2007, 38:2379-2381.
61. Groenendijk B.C.W., Hierck B.P., Gittenberger-de Groot A.C., Poelmann R.E. Development-related changes in the expression of shear stress responsive genes KLF-2, ET-1, and NOS-3 in the developing cardiovascular system of chicken embryos. Dev. Dyn. 2004, 230:57-68.
62. Groenendijk B.C.W., Hierck B.P., Vrolijk J., Baiker M., Pourquie M.J.B.M., Gittenberger-de Groot A.C., et al. Changes in shear stress-related gene expression after experimentally altered venous return in the chicken embryo. Circ. Res. 2005, 96:1291-1298.
63. Groenendijk B.C.W., Van der Heiden K., Hierck B.P., Poelmann R.E. The role of shear stress on ET-1, KLF2, and NOS-3 expression in the developing cardiovascular system of chicken embryos in a venous ligation model. Physiology (Bethesda) 2007, 22:380-389.
64. Groenendijk B.C.W., Vennemann P., Stekelenburg-de Vos S., Wladimiroff J.W., Nieuwstadt F.T.M., Westerweel J., et al. The endothelin-1 pathway and the development of cardiovascular defects in the hemodynamically challenged chicken embryo. J. Vasc. Res. 2008, 45:54-68.
65. Hagiwara H., Ohwada N., Takata K. Cell biology of normal and abnormal ciliogenesis in the ciliated epithelium. Int. Rev. Cytol. 2004, 234:101-141.
66. Harris P.C. 2008 Homer W Smith Award: insights into the pathogenesis of polycystic kidney disease from gene discovery. J. Am. Soc. Nephrol. 2009, 20:1188-1198.
67. Harris P.C., Torres V.E. Polycystic kidney disease. Annu. Rev. Med. 2009, 60:321-337.
68. Hassane S., Claij N., Lantinga-van Leeuwen I.S., van Munsteren J.C., Van Lent N., Hanemaaijer R., et al. Pathogenic sequence for dissecting aneurysm formation in a hypomorphic polycystic kidney disease 1 mouse model. Arterioscler. Thromb. Vasc. Biol. 2007, 27:2177-2183.
69. Hassane S., Claij N., Jodar M., Dedman A., Lauritzen I., Duprat F., et al. Pkd1-inactivation in vascular smooth muscle cells and adaptation to hypertension. Lab. Invest. 2011, 91:24-32.
70. Haust M.D. Endothelial cilia in human aortic atherosclerosic lesions. Virchows Arch. 1987, 410:317-326.
71. Haycraft C.J., Banizs B., Aydin-Son Y., Zhang Q., Michaud E.J., Yoder B.K. Gli2 and Gli3 localize to cilia and require the intraflagellar transport protein polaris for processing and function. PLoS Genet. 2005, 1:e53.
72. Helderman F., Segers D., de Crom R., Hierck B.P., Poelmann R.E., Evans P.C., et al. Effect of shear stress on vascular inflammation and plaque development. Curr. Opin. Lipidol. 2007, 18:527-533.
73. Helmke B.P., Davies P.F. The cytoskeleton under external fluid mechanical forces: hemodynamic forces acting on the endothelium. Ann. Biomed. Eng. 2002, 30:284-296.
74. Hierck B.P., Van der Heiden K., Alkemade F.E., van de Pas S., van Thienen J.V., Groenendijk B.C.W., et al. Primary cilia sensitize endothelial cells for fluid shear stress. Dev. Dyn. 2008, 237:725-735.
75. Hierck B.P., Van der Heiden K., Poelmann R.E. Fluid shear stress and inner curve remodeling of the embryonic heart. choosing the right lane!. ScientificWorldJournal 2008, 8:212-222.
76. Hogers B., DeRuiter M.C., Gittenberger-de Groot A.C., Poelmann R.E. Unilateral vitelline vein ligation alters intracardiac blood flow patterns and morphogenesis in the chick embryo. Circ. Res. 1997, 80:473-481.
77. Hogers B., DeRuiter M.C., Gittenberger-de Groot A.C., Poelmann R.E. Extraembryonic venous obstructions lead to cardiovascular malformations and can be embryolethal. Cardiovasc. Res. 1999, 41:87-99.
78. Huang B., Rifkin M.R., Luck D.J. Temperature-sensitive mutations affecting flagellar assembly and function in Chlamydomonas reinhardtii. J. Cell Biol. 1977, 72:67-85.
79. Iomini C., Babaev-Khaimov V., Sassaroli M., Piperno G. Protein particles in chlamydomonas flagella undergo a transport cycle consisting of four phases. J. Cell Biol. 2001, 153:13-24.
80. 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.
81. Johnson K.A., Rosenbaum J.L. Polarity of flagellar assembly in Chlamydomonas. J. Cell Biol. 1992, 119:1605-1611.
82. Katritsis D., Kaiktsis L., Chaniotis A., Pantos J., Efstathopoulos E.P., Marmarelis V. Wall shear stress: theoretical considerations and methods of measurement. Prog. Cardiovasc. Dis. 2007, 49:307-329.
83. Kim E., Arnould T., Sellin L.K., Benzing T., Fan M.J., Gruning W., et al. The polycystic kidney disease 1 gene product modulates Wnt signaling. J. Biol. Chem. 1999, 274:4947-4953.
84. Kim J.C., Badano J.L., Sibold S., Esmail M.A., Hill J., Hoskins B.E., et al. The Bardet-Biedl protein BBS4 targets cargo to the pericentriolar region and is required for microtubule anchoring and cell cycle progression. Nat. Genet. 2004, 36:462-470.
85. Kim J., Lee J.E., Heynen-Genel S., Suyama E., Ono K., Lee K., et al. Functional genomic screen for modulators of ciliogenesis and cilium length. Nature 2010, 464:1048-1051.
86. Kocaman O., Oflaz H., Yekeler E., Dursun M., Erdogan D., Demirel S., et al. Endothelial dysfunction and increased carotid intima-media thickness in patients with autosomal dominant polycystic kidney disease. Am. J. Kidney Dis. 2004, 43:854-860.
87. Kou B., Zhang J., Singer D.R. Effects of cyclic strain on endothelial cell apoptosis and tubulogenesis are dependent on ROS production via NAD(P)H subunit p22phox. Microvasc. Res. 2009, 77:125-133.
88. Lancaster M.A., Gleeson J.G. Cystic kidney disease: the role of Wnt signaling. Trends Mol. Med. 2010, 16:349-360.
89. Lehoux S., Castier Y., Tedgui A. Molecular mechanisms of the vascular responses to haemodynamic forces. J. Intern. Med. 2006, 259:381-392.
90. Levin M., Johnson A.L., Stern C.D., Kuehn M., Tabin C. A molecular pathway determining left-right asymmetry in chick embryogenesis. Cell 1995, 82:803-814.
91. Li Y.S., Haga J.H., Chien S. Molecular basis of the effects of shear stress on vascular endothelial cells. J. Biomech. 2005, 38:1949-1971.
92. Liu W., Xu S., Woda C., Kim P., Weinbaum S., Satlin L.M. Effect of flow and stretch on the [Ca2+]i response of principal and intercalated cells in cortical collecting duct. Am. J. Physiol. Renal Physiol. 2003, 285:F998-F1012.
93. Low S.H., Vasanth S., Larson C.H., Mukherjee S., Sharma N., Kinter M.T., et al. Polycystin-1, STAT6, and P100 function in a pathway that transduces ciliary mechanosensation and is activated in polycystic kidney disease. Dev. Cell 2006, 10:57-69.
94. Lu C.J., Du H., Wu J., Jansen D.A., Jordan K.L., Xu N., et al. Non-random distribution and sensory functions of primary cilia in vascular smooth muscle cells. Kidney Blood Press. Res. 2008, 31:171-184.
95. Mahajan R., Kumar B.Y., Kumar S., Kumar G.V. Anesthetic management of A patient with Bardet-Biedl syndrome and dilated cardiomyopathy. Minerva Anestesiol. 2007, 73:191-194.
96. Malone A.M.D., Anderson C.T., Tummala P., Stearns T., Jacobs C.R. Primary cilia mediate PGE2 release in MC3T3-E1 osteoblasts. Mol. Cell. Biomech. 2006, 3:207-208.
97. Malone A.M., Anderson C.T., Tummala P., Kwon R.Y., Johnston T.R., Stearns T., et al. Primary cilia mediate mechanosensing in bone cells by a calcium-independent mechanism. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:13325-13330.
98. Masyuk A.I., Masyuk T.V., Splinter P.L., Huang B.Q., Stroope A.J., Larusso N.F. Cholangiocyte cilia detect changes in luminal fluid flow and transmit them into intracellular Ca2+ and cAMP signaling. Gastroenterology 2006, 131:911-920.
99. McGrath J., Brueckner M. Cilia are at the heart of vertebrate left-right asymmetry. Curr. Opin. Genet. Dev. 2003, 13:385-392.
100. McGrath J., Somlo S., Makova S., Tian X., Brueckner M. Two populations of node monocilia initiate left-right asymmetry in the mouse. Cell 2003, 114:61-73.
101. McKean P.G., Baines A., Vaughan S., Gull K. Gamma-tubulin functions in the nucleation of a discrete subset of microtubules in the eukaryotic flagellum. Curr. Biol. 2003, 13:598-602.
102. Megens R.T., Reitsma S., Schiffers P.H., Hilgers R.H., De Mey J.G., Slaaf D.W., et al. Two-photon microscopy of vital murine elastic and muscular arteries. Combined structural and functional imaging with subcellular resolution. J. Vasc. Res. 2007, 44:87-98.
103. Merrill A.E., Merriman B., Farrington-Rock C., Camacho N., Sebald E.T., Funari V.A., et al. Ciliary abnormalities due to defects in the retrograde transport protein DYNC2H1 in short-rib polydactyly syndrome. Am. J. Hum. Genet. 2009, 84:542-549.
104. Mochizuki S., Vink H., Hiramatsu O., Kajita T., Shigeto F., Spaan J.A., et al. Role of hyaluronic acid glycosaminoglycans in shear-induced endothelium-derived nitric oxide release. Am. J. Physiol. Heart Circ. Physiol. 2003, 285:H722-H726.
105. Molin D.G.M., DeRuiter M.C., Wisse L.J., Mohamad A., Doetschman T., Poelmann R.E., et al. Altered apoptosis pattern during pharyngeal arch artery remodelling is associated with aortic arch malformations in Tgf beta 2 knock-out mice. Cardiovasc. Res. 2002, 56:312-322.
106. Moon R.T., Bowerman B., Boutros M., Perrimon N. The promise and perils of Wnt signaling through beta-catenin. Science 2002, 296:1644-1646.
107. Morgan D., Eley L., Sayer J., Strachan T., Yates L.M., Craighead A.S., et al. Expression analyses and interaction with the anaphase promoting complex protein Apc2 suggest a role for inversin in primary cilia and involvement in the cell cycle. Hum. Mol. Genet. 2002, 11:3345-3350.
108. Morris R.L., Scholey J.M. Heterotrimeric kinesin-II is required for the assembly of motile 9+2 Ciliary axonemes on sea urchin embryos. J. Cell Biol. 1997, 138:1009-1022.
109. Nachury M.V., Loktev A.V., Zhang Q., Westlake C.J., Peranen J., Merdes A., et al. A core complex of BBS proteins cooperates with the GTPase Rab8 to promote ciliary membrane biogenesis. Cell 2007, 129:1201-1213.
110. Nauli S.M., Alenghat F.J., Luo Y., Williams E., Vassilev P., Lil X.G., et al. Polycystins 1 and 2 mediate mechanosensation in the primary cilium of kidney cells. Nat. Genet. 2003, 33:129-137.
111. Nauli S.M., Kawanabe Y., Kaminski J.J., Pearce W.J., Ingber D.E., Zhou J. Endothelial cilia are fluid-shear sensors that regulate calcium signaling and nitric oxide production through polycystin-1. Circulation 2008, 117:1161-1171.
112. Nonaka S., Tanaka Y., Okada Y., Takeda S., Harada A., Kanai Y., et al. Randomization of left-right asymmetry due to loss of nodal cilia generating leftward flow of extraembryonic fluid in mice lacking KIF3B motor protein. Cell 1998, 95:829-837.
113. Ong A.C.M., Ward C.J., Butler R.J., Biddolph S., Bowker C., Torra P., et al. Coordinate expression of the autosomal dominant polycystic kidney disease proteins, polycystin-2 and polycystin-1, in normal and cystic tissue. Am. J. Pathol. 1999, 154:1721-1729.
114. Otto E.A., Schermer B., Obara T., O'Toole J.F., Hiller K.S., Mueller A.M., et al. Mutations in INVS encoding inversin causes nephronophthisis type 2, linking renal cystic disease to the function of primary cilia and left-right axis determination. Nat. Genet. 2003, 34:413-420.
115. Partridge J., Carlsen H., Enesa K., Chaudhury H., Zakkar M., Luong L., et al. Laminar shear stress acts as a switch to regulate divergent functions of NF-{kappa}B in endothelial cells. FASEB J. 2007, 21:3553-3561.
116. Pazour G.J., Dickert B.L., Witman G.B. The DHC1b (DHC2) isoform of cytoplasmic dynein is required for flagellar assembly. J. Cell Biol. 1999, 144:473-481.
117. Pedersen L.B., Rosenbaum J.L. Intraflagellar transport (IFT) role in ciliary assembly, resorption and signalling. Curr. Top. Dev. Biol. 2008, 85:23-61.
118. Poelma C., Van der Heiden K., Hierck B.P., Poelmann R.E., Westerweel J. Measurements of the wall shear stress distribution in the outflow tract of an embryonic chicken heart. J. R. Soc. Interface 2010, 7:91-103.
119. Poelmann R.E. The head-process and the formation of the definitive endoderm in the mouse embryo. Anat. Embryol. 1981, 162:41-49.
120. Poelmann R.E., Mikawa T., Gittenberger-de Groot A.C. Neural crest cells in outflow tract septation of the embryonic chicken heart: differentiation and apoptosis. Dev. Dyn. 1998, 212:373-384.
121. Poelmann R.E., Gittenberger-de Groot A.C., Hierck B.P. The development of the heart and microcirculation: role of shear stress. Med. Biol. Eng. Comput. 2008, 46:479-484.
122. Poelmann R.E., Van der Heiden K., Gittenberger-de Groot A.C., Hierck B.P. Deciphering the endothelial shear stress sensor. Circulation 2008, 117:1124-1126.
123. Porter M.E., Bower R., Knott J.A., Byrd P., Dentler W. Cytoplasmic dynein heavy chain 1b is required for flagellar assembly in Chlamydomonas. Mol. Biol. Cell 1999, 10:693-712.
124. Praetorius H.A., Spring K.R. Bending the MDCK cell primary cilium increases intracellular calcium. J. Membr. Biol. 2001, 184:71-79.
125. Praetorius H.A., Spring K.R. Removal of the MDCK cell primary cilium abolishes flow sensing. J. Membr. Biol. 2003, 191:69-76.
126. Praetorius H.A., Spring K.R. A physiological view of the primary cilium. Annu. Rev. Physiol. 2005, 67:515-529.
127. Pugacheva E.N., Jablonski S.A., Hartman T.R., Henske E.P., Golemis E.A. HEF1-dependent Aurora A activation induces disassembly of the primary cilium. Cell 2007, 129:1351-1363.
128. Qin H., Rosenbaum J.L., Barr M.M. An autosomal recessive polycystic kidney disease gene homolog is involved in intraflagellar transport in C. elegans ciliated sensory neurons. Curr. Biol. 2001, 11:457-461.
129. Qin H., Wang Z., Diener D., Rosenbaum J. Intraflagellar transport protein 27 is a small G protein involved in cell-cycle control. Curr. Biol. 2007, 17:193-202.
130. Rabelink T.J., Luscher T.F. Endothelial nitric oxide synthase-host defense enzyme of the endothelium?. Arterioscler. Thromb. Vasc. Biol. 2006, 26:267-271.
131. Ramasubramanian A., Nerurkar N.L., Achtien K.H., Filas B.A., Voronov D.A., Taber L.A. On modeling morphogenesis of the looping heart following mechanical perturbations. J. Biomech. Eng. 2008, 130:061018.
132. Redmond E.M., Cahill P.A., Hirsch M., Wang Y.N., Sitzmann J.V., Okada S.S. Effect of pulse pressure on vascular smooth muscle cell migration: the role of urokinase and matrix metalloproteinase. Thromb. Haemost. 1999, 81:293-300.
133. Reitsma S., Oude Egbrink M.G., Vink H., van den Berg B.M., Lima P.V., Engels W., et al. Endothelial glycocalyx structure in the intact carotid artery: a two-photon laser scanning microscopy study. J. Vasc. Res. 2011, 48:297-306.
134. Resnick A., Hopfer U. Force-response considerations in ciliary mechanosensation. Biophys. J. 2007, 93:1380-1390.
135. Resnick N., Yahav H., Shay-Salit A., Shushy M., Schubert S., Zilberman L.C., et al. Fluid shear stress and the vascular endothelium: for better and for worse. Prog. Biophys. Mol. Biol. 2003, 81:177-199.
136. Rieder C.L., Jensen C.G., Jensen L.C. The resorption of primary cilia during mitosis in a vertebrate (PtK1) cell line. J. Ultrastruct. Res. 1979, 68:173-185.
137. Robert A., Margall-Ducos G., Guidotti J.E., Bregerie O., Celati C., Brechot C., et al. The intraflagellar transport component IFT88/polaris is a centrosomal protein regulating G1-S transition in non-ciliated cells. J. Cell Sci. 2007, 120:628-637.
138. Rochais F., Mesbah K., Kelly R.G. Signaling pathways controlling second heart field development. Circ. Res. 2009, 104:933-942.
139. Rohatgi R., Scott M.P. Patching the gaps in hedgehog signalling. Nat. Cell Biol. 2007, 9:1005-1009.
140. Rosenbaum J.L., Witman G.B. Intraflagellar transport. Nat. Rev. Mol. Cell Biol. 2002, 3:813-825.
141. Ross R. Mechanisms of disease-atherosclerosis-an inflammatory disease. N. Engl. J. Med. 1999, 340:115-126.
142. Rossi M., Lindken R., Hierck B.P., Westerweel J. Tapered microfluidic chip for the study of biochemical and mechanical response at subcellular level of endothelial cells to shear flow. Lab Chip 2009, 9:1403-1411.
143. Rydholm S., Zwartz G., Kowalewski J.M., Kamali-Zare P., Frisk T., Brismar H. Mechanical properties of primary cilia regulate the response to fluid flow. Am. J. Physiol. Renal Physiol. 2010, 298:F1096-F1102.
144. Satir P., Christensen S.T. Overview of structure and function of mammalian cilia. Annu. Rev. Physiol. 2007, 69:377-400.
145. Scholey J.M. Intraflagellar transport. Annu. Rev. Cell Dev. Biol. 2003, 19:423-443.
146. Schwartz E.A., Leonard M.L., Bizios R., Bowser S.S. Analysis and modeling of the primary cilium bending response to fluid shear. Am. J. Physiol. 1997, 272:F132-F138.
147. Shaaban A.M., Duerinckx A.J. Wall shear stress and early atherosclerosis: a review. Am. J. Roentgenol. 2000, 174:1657-1665.
148. Sharma N., Kosan Z.A., Stallworth J.E., Berbari N.F., Yoder B.K. Soluble levels of cytosolic tubulin regulate ciliary length control. Mol. Biol. Cell 2011, 22:806-816.
149. Simons M., Gloy J., Ganner A., Bullerkotte A., Bashkurov M., Kronig C., et al. Inversin, the gene product mutated in nephronophthisis type II, functions as a molecular switch between Wnt signaling pathways. Nat. Genet. 2005, 37:537-543.
150. Slager C.J., Wentzel J.J., Gijsen F.J., Schuurbiers J.C., van der Wal A.C., van der Steen A.F., et al. The role of shear stress in the generation of rupture-prone vulnerable plaques. Nat. Clin. Pract. Cardiovasc. Med. 2005, 2:401-407.
151. Slavotinek A.M., Biesecker L.G. Phenotypic overlap of McKusick-Kaufman syndrome with Bardet-Biedl syndrome: a literature review. Am. J. Med. Genet. 2000, 95:208-215.
152. Slough J., Cooney L., Brueckner M. Monocilia in the embryonic mouse heart suggest a direct role for cilia in cardiac morphogenesis. Dev. Dyn. 2008, 237:2304-2314.
153. Smith E.F., Lefebvre P.A. The role of central apparatus components in flagellar motility and microtubule assembly. Cell Motil. Cytoskeleton 1997, 38:1-8.
154. Sorokin S. Centrioles and the formation of rudimentary cilia by fibroblasts and smooth muscle cells. J. Cell Biol. 1962, 15:363-377.
155. Stone D.L., Agarwala R., Schaffer A.A., Weber J.L., Vaske D., Oda T., et al. Genetic and physical mapping of the McKusick-Kaufman syndrome. Hum. Mol. Genet. 1998, 7:475-481.
156. Sumpio B.E., Jennings T.A., Merino M.J., Sullivan P.D. Adenoid cystic carcinoma of the breast. Data from the Connecticut tumor registry and a review of the literature. Ann. Surg. 1987, 205:295-301.
157. Tzima E. Role of small GTPases in endothelial cytoskeletal dynamics and the shear stress response. Circ. Res. 2006, 98:176-185.
158. Tzima E., Irani-Tehrani M., Kiosses W.B., Dejana E., Schultz D.A., Engelhardt B., et al. A mechanosensory complex that mediates the endothelial cell response to fluid shear stress. Nature 2005, 437:426-431.
159. Uzbekov R., Prigent C. Clockwise or anticlockwise? Turning the centriole triplets in the right direction!. FEBS Lett. 2007, 581:1251-1254.
160. van den Berg B.M., Spaan J.A.E., Rolf T.M., Vink H. Atherogenic region and diet diminish glycocalyx dimension and increase intima-to-media ratios at murine carotid artery bifurcation. Am. J. Physiol. Heart Circ. Physiol. 2006, 290:H915-H920.
161. van den Berg B.M., Spaan J.A., Vink H. Impaired glycocalyx barrier properties contribute to enhanced intimal low-density lipoprotein accumulation at the carotid artery bifurcation in mice. Pflugers Arch. 2009, 457:1199-1206.
162. Van der Heiden K., Groenendijk B.C.W., Hierck B.P., Hogers B., Koerten H.K., Mommaas A.M., et al. Monocilia on chicken embryonic endocardium in low shear stress areas. Dev. Dyn. 2006, 235:19-28.
163. Van der Heiden K., Hierck B.P., Krams R., de Crom R., Cheng C., Baiker M., et al. Endothelial primary cilia in areas of disturbed flow are at the base of atherosclerosis. Atherosclerosis 2008, 196:542-550.
164. Veeman M.T., Axelrod J.D., Moon R.T. A second canon. Functions and mechanisms of beta-catenin-independent Wnt signaling. Dev. Cell 2003, 5:367-377.
165. Vennemann P., Kiger K.T., Lindken R., Groenendijk B.C.W., Stekelenburg-de Vos S., ten Hagen T.L.M., et al. In vivo micro particle image velocimetry measurements of blood-plasma in the embryonic avian heart. J. Biomech. 2006, 39:1191-1200.
166. Vorobjev I.A., Chentsov Y.S. Centrioles in the cell cycle I. Epithelial cells. J. Cell Biol. 1982, 93:938-949.
167. Wang N., Miao H., Li Y.S., Zhang P., Haga J.H., Hu Y.L., et al. Shear stress regulation of Kruppel-like factor 2 expression is flow pattern-specific. Biochem. Biophys. Res. Commun. 2006, 341:1244-1251.
168. Watanabe D., Saijoh Y., Nonaka S., Sasaki G., Ikawa Y., Yokoyama T., et al. The left-right determinant Inversin is a component of node monocilia and other 9+0 cilia. Development 2003, 130:1725-1734.
169. Wedding K.L., Draney M.T., Herfkens R.J., Zarins C.K., Taylor C.A., Pelc N.J. Measurement of vessel wall strain using cine phase contrast MRI. J. Magn. Reson. Imaging 2002, 15:418-428.
170. Weimbs T. Polycystic kidney disease and renal injury repair: common pathways, fluid flow, and the function of polycystin-1. Am. J. Physiol. Renal Physiol. 2007, 293:F1423-F1432.
171. Wentzel J.J., Janssen E., Vos J., Schuurbiers J.C., Krams R., Serruys P.W., et al. Extension of increased atherosclerotic wall thickness into high shear stress regions is associated with loss of compensatory remodeling. Circulation 2003, 108:17-23.
172. Wheatley D.N., Wang A.M., Strugnell G.E. Expression of primary cilia in mammalian cells. Cell Biol. Int. 1996, 20:73-81.
173. Xiao Z., Zhang S., Mahlios J., Zhou G., Magenheimer B.S., Guo D., et al. Cilia-like structures and polycystin-1 in osteoblasts/osteocytes and associated abnormalities in skeletogenesis and Runx2 expression. J. Biol. Chem. 2006, 281:30884-30895.
174. Yang J., Adamian M., Li T.S. Rootletin interacts with C-Nap1 and may function as a physical linker between the pair of centrioles/basal bodies in cells. Mol. Biol. Cell 2006, 17:1033-1040.
175. Yost H.J. Left-right asymmetry: nodal cilia make and catch a wave. Curr. Biol. 2003, 13:R808-R809.
176. Zhou J. Polycystins and primary cilia: primers for cell cycle progression. Annu. Rev. Physiol. 2009, 71:83-113.
177. Zimmermann W. Uber einen zwischen aorten- und pulmonalbogen gelegenen Kiemarterienbogen beim Kaninchen. Anat. Anz. 1889, 4:720.