Primary cilia of cells of cardiovascular apparatus
Authors:
J. Dvořák 1; V. Sitorová 2; D. H. Nikolov 2; J. Mokrý 3; I. Richter 4,5; S. Filip 1; A. Ryška 2; J. Petera 1
Authors‘ workplace:
Klinika onkologie a radioterapie Lékařské fakulty UK a FN Hradec Králové, přednosta prof. MUDr. Jiří Petera, Ph. D.
1; Fingerlandův ústav patologie Lékařské fakulty UK a FN Hradec Králové, přednosta prof. MUDr. Aleš Ryška, Ph. D.
2; Ústav histologie a embryologie Lékařské fakulty UK a FN Hradec Králové, přednosta prof. MUDr. Jaroslav Mokrý, Ph. D.
3; Oddělení klinické onkologie Krajské nemocnice Liberec, a. s., Liberec, přednosta prim. MUDr. Jiří Bartoš, MBA
4; Lékařská fakulta UK a FN Hradec Králové, děkan prof. MUDr. RNDr. Miroslav Červinka, CSc.
5
Published in:
Vnitř Lék 2012; 58(12): 938-942
Category:
Review
Overview
The primary cilium is a mechanosensory, solitary, non-motile microtubule-based structure that in the quiescent phase of the cell cycle projects from the surface of the majority of human cells, including embryonal, stem and mesenchymal cells, fibroblasts, myoblasts, cardiomyocytes, vascular smooth muscle and endothelial cells. Primary cilia are in increased frequency also present on the surface of endothelial cells in atherosclerotic predilection sites, lipoid streaks and dots and atheromatous plaques. The primary cilium is formed from the mother centriole. Primary cilia are currently studied in mechanobiology of cardiovascular apparatus and their role in cell migration, cell cycle control and atherogenesis. The aim of this paper is to provide a review of the current knowledge on the primary cilia of cells of cardiovascular apparatus.
Key words:
primary cilia – cardiomyocytes – endothelial cells – vascular smooth muscle cells – atherosclerosis
Sources
1. Satir P, Pedersen LB, Christensen ST. The primary cilium at a glance. J Cell Sci 2010; 123: 499–503.
2. Plotnikova OV, Golemis EA, Pugacheva EN. Cell cycle-dependent ciliogenesis and cancer. Cancer Res 2008; 68: 2058–2061.
3. Dvořák J, Sitorová V, Hadži Nikolov D et al. Primary cilium – antenna-like structure on the surface of most mammalian cell types. J Phys Conf Ser 2011; 329: 12–22.
4. Pugacheva EN, Jablonski SA, Hartman TRm Henske EP, Golemis EA. HEF1-dependent Aurora A activation induces disassembly of the primary cilium. Cell 2007; 129: 1351–1363.
5. Dvořák J, Sitorová V, Hadži Nikolov D et al. Primární řasinky a jejich biologické funkce. Onkologie 2011; 5: 234–238.
6. Zhu D, Shi S, Wang H, Liao K. Growth arrest induces primary-cilium formation and sensitizes IGF-1-receptor signaling during differentiation induction of 3T3-L1 preadipocytes. J Cell Sci 2009; 122: 2760–2768.
7. Jenkins D. Hedgehog signalling: emerging evidence for non-canonical pathways. Cell Signal 2009; 21: 1023–1034.
8. Clement CA, Kristensen SG, Møllrd K et al. The primary cilium coordinates early cardiogenesis and hedgehog signaling in cardiomyocyte differentiation. J Cell Sci 2009; 122: 3070–3082.
9. Myklebust R, Engedal H, Saetersdal TS, Ulstein M. Primary 9 + 0 cilia in the embryonic and the adult human heart. Anat Embryol (Berl) 1977; 151: 127–139.
10. Schatten H, Sun QY. The significant role of centrosomes in stem cell division and differentiation. Microsc Microanal 2011; 17: 506–512.
11. Proulx-Bonneau S, Annabi B. The primary cilium as a biomarker in the hypoxic adaptation of bone marrow-derived mesenchymal stromal cells: a role for the secreted frizzled-related proteins. Biomark Insights 2011; 6: 107–118.
12. Egorova AD, Khedoe PP, Goumans MJ et al. Lack of primary cilia primes shear-induced endothelial-to-mesenchymal transition. Circ Res 2011; 108: 1093–1101.
13. Bystrevskaya VB, Lichkun VV, Antonov AS, Perov NA. An ultrastructural study of centriolar complexes in adult and embryonic human aortic endothelial cells. Tissue Cell 1988; 20: 493–503.
14. Haust MD. Endothelial cilia in human aortic atherosclerotic lesions. Virchows Arch A Pathol Anat Histopathol 1987; 410: 317–326.
15. Lu CJ, Du H, Wu J et al. Non-random distribution and sensory functions of primary cilia in vascular smooth muscle cells. Kidney Blood Press Res 2008; 31: 171–184.
16. Haust MD. Ciliated smooth muscle cells in aortic atherosclerotic lesions of rabbit. Atherosclerosis 1984; 50: 283–293.
17. Haust MD. Ciliated smooth muscle cells in atherosclerotic lesions of human aorta. Am J Cardiovasc Pathol 1987; 1: 115–129.
18. Van der Heiden K, Hierck BP, Krams R et al. Endothelial primary cilia in areas of disturbed flow are at the base of atherosclerosis. Atherosclerosis 2008; 196: 542–550.
19. Van der Heiden K, Egorova AD, Poelmann RE, Wentzel JJ, Hierck BP. Role for primary cilia as flow detectors in the cardiovascular system. Int Rev Cell Mol Biol 2011; 290: 87–119.
20. Nauli SM, Jin X, Hierck BP. The mechanosensory role of primary cilia in vascular hypertension. Int J Vasc Med 2011; 2011: 276–281.
21. Berbari NF, Lewis JS, Bishop GA, Askwith CC, Mykytyn K. Bardet-Biedl syndrome proteins are required for the localization of G protein--coupled receptors to primary cilia. Proc Natl Acad Sci U S A 2008; 105: 4242–4246.
22. Davenport JR, Watts AJ, Roper VC et al. Disruption of intraflagellar transport in adult mice leads to obesity and slow-onset cystic kidney disease. Curr Biol 2007; 17: 1586–1594.
23. Nonaka S, Shiratori H, Saijoh Y, Hamada H. Determination of left-right patterning of the mouse embryo by artificial nodal flow. Nature 2002; 418: 96–99.
24. Leigh MW, Pittman JE, Carson JL et al. Clinical and genetic aspects of primary ciliary dyskinesia/Kartagener syndrome. Genet Med 2009; 11: 473–487.
25. Zimmermann KW. Beiträge zur Kenntniss einiger Drüsen und Epithelien. Arch Mikrosk Anat 1898; 52: 552–706.
26. Sorokin S. Centrioles and the formation of rudimentary cilia by fibroblasts and smooth muscle cells. J Cell Biol 1962; 15: 363–377.
27. Sorokin SP. Reconstructions of centriole formation and ciliogenesis in mammalian lungs. J Cell Sci 1968; 3: 207–230.
28. Seeley ES, Nachury MV. The perennial organelle: assembly and disassembly of the primary cilium. J Cell Sci 2010; 123: 511–518.
29. Marion V, Stoetzel C, Schlicht D et al. Transient ciliogenesis involving Bardet-Biedl syndrome proteins is a fundamental characteristic of adipogenic differentiation. Proc Natl Acad Sci U S A 2009; 106: 1820–1825.
30. Kraus MJ, Jirsová Z. A contribution to the solitary ciliogenesis. Folia Morphol (Praha) 1973; 21: 265–268.
31. Martínek J, Kraus R, Jirsová Z. Differentiation and occurrence of the individual cilium. In: Dvořák M (ed.) Biogenesis of Cell Organelles. Acta Facultatis Medicae Universitatis Brunensis 1974; 49: 261–263.
32. Fliegauf M, Benzing T, Omran H. When cilia go bad: cilia defects and ciliopathies. Nat Rev Mol Cell Biol 2007; 8: 880–893.
33. Bloodgood RA. Sensory reception is an attribute of both primary cilia and motile cilia. J Cell Sci 2010; 123: 505–509.
34. 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.
35. Van der Heiden K, Groenendijk BC, Hierck BP et al. Monocilia on chicken embryonic endocardium in low shear stress areas. Dev Dyn 2006; 235: 19–28.
36. Vennemann P, Kiger KT, Lindken R et al. In vivo micro particle image velocimetry measurements of blood-plasma in the embryonic avian heart. J Biomech 2006; 39: 1191–1200.
37. Poelmann RE, Van der Heiden K, Gittenberger-de Groot A, Hierck BP. Deciphering the endothelial shear stress sensor. Circulation 2008; 117: 1124–1126.
38. Cheng C, Helderman F, Tempel D et al. Large variations in absolute wall shear stress levels within one species and between species. Atherosclerosis 2007; 195: 225–235.
39. Besschetnova TY, Kolpakova-Hart E, Guan Y et al. Identification of signaling pathways regulating primary cilium length and flow-mediated adaptation. Curr Biol 2010; 20: 182–187.
40. Abdul-Majeed S, Nauli SM Dopamine receptor type 5 in the primary cilia has dual chemo- and mechano-sensory roles. Hypertension 2011; 58: 325–331.
41. Ando J, Yamamoto K. Vascular mechanobiology: endothelial cell responses to fluid shear stress. Circ J 2009; 73: 1983–1992.
42. 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.
43. Groenendijk BC, Hierck BP, Gittenberger-De Groot AC, Poelmann RE. 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.
44. AbouAlaiwi WA, Takahashi M, Mell BR et al. Ciliary polycystin-2 is a mechanosensitive calcium channel involved in nitric oxide signaling cascades. Circ Res 2009; 104: 860–869.
45. Katsumoto T, Higaki K, Ohno K, Onodera K. The orientation of primary cilia during the wound response in 3Y1 cells. Biol Cell 1994; 81: 17–21.
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Diabetology Endocrinology Internal medicineArticle was published in
Internal Medicine
2012 Issue 12
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