The mechanics of the primary cilium: An intricate structure with complex function

Journal of Biomechanics

Volumn 45, Issue 1, 2012, Pages 17-26

  Hoey, David A ^a,b   Downs, Matthew E ^a   Jacobs, Christopher R ^a  

^a CITY UNIVERSITY OF NEW YORK   (United States)

^b ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

Author keywords

Cellular mechanosensor; Mechanics; Model; Primary cilium; Structure

Indexed keywords

BENDING RESISTANCE; BIOCHEMICAL CHANGES; CELLULAR BEHAVIORS; CELLULAR MECHANOSENSOR; CELLULAR RESPONSE; CELLULAR STRUCTURE; COMPLEX FUNCTIONS; EXTRACELLULAR ENVIRONMENTS; INTRICATE STRUCTURES; LOAD BEARING; MECHANICAL BEHAVIOR; MECHANICAL LOADING; MECHANICAL MODELING; MECHANICAL STATE; MECHANOSENSING; MECHANOSENSITIVITY; PRIMARY CILIUM; RESEARCH AREAS; SIGNALING PATHWAYS; STRUCTURAL FEATURE; STRUCTURAL PERFORMANCE; TISSUE HOMEOSTASIS;

MECHANICS; MODELS; STRUCTURE (COMPOSITION); TISSUE;

MECHANISMS;

MICROTUBULE ASSOCIATED PROTEIN; POLYCYSTIN 1; POLYCYSTIN 2;

BONE; CELL ADHESION; CELL FUNCTION; CELL ORGANELLE; CELL STRUCTURE; CELLULAR DISTRIBUTION; DENDRITE; EUKARYOTIC FLAGELLUM; KIDNEY; LIVER; MECHANICAL STIMULATION; MECHANOTRANSDUCTION; MICROTUBULE; NERVE CELL; PRIMARY CILIUM; PRIORITY JOURNAL; REVIEW;

ANIMALS; CELLULAR MICROENVIRONMENT; CILIA; HOMEOSTASIS; HUMANS; MECHANOTRANSDUCTION, CELLULAR;

EID: 83555176400     PISSN: 00219290     EISSN: 18732380     Source Type: Journal    
DOI: 10.1016/j.jbiomech.2011.08.008     Document Type: Review

References (73)

1. Adams M., Smith U.M., Logan C.V., Johnson C.A. Recent advances in the molecular pathology, cell biology and genetics of ciliopathies. Journal of Medical Genetics 2008, 45:257-267.
2. Albrecht-Buehler G., Bushnell A. The ultrastructure of primary cilia in quiescent 3T3 cells. Experimental Cell Research 1980, 126:427-437.
3. Alieva I.B., Nadezhdina E.S., Vaisberg E.A., Vorobjev I.A. Microtubule and intermediate filament patterns around the centrosome in interphase cells. The Centrosome 1992, 15:103-129.
4. Badano J.L., Mitsuma N., Beales P.L., Katsanis N. The ciliopathies: an emerging class of human genetic disorders. Annual Review of Genomics and Human Genetics 2006, 7:125-148.
5. Berbari N.F., O'Connor A.K., Haycraft C.J., Yoder B.K. The primary cilium as a complex signaling center. Current Biology 2009, 19:R526-535.
6. 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. Current Biology 2010, 20:182-187.
7. Boisvieux-Ulrich E., Sandoz D. Determination of ciliary polarity precedes differentiation in the epithelial cells of quail oviduct. Biology of the Cell 1991, 72:3-14.
8. Chang W., Gruber D., Chari S., Kitazawa H., Hamazumi Y., Hisanaga S., Bulinski J.C. Phosphorylation of MAP4 affects microtubule properties and cell cycle progression. Journal of Cell Science 2001, 114:2879-2887.
9. Davenport J.R., Yoder B.K. An incredible decade for the primary cilium: a look at a once-forgotten organelle. American Journal of Physiology Renal Physiology 2005, 289:F1159-1169.
10. Downing K.H., Sui H. Structural insights into microtubule doublet interactions in axonemes. Current Opinion in Structural Biology 2007, 17:253-259.
11. Ernstrom G.G., Chalfie M. Genetics of sensory mechanotransduction. Annual Review of Genetics 2002, 36:411-453.
12. Fariss R.N., Molday R.S., Fisher S.K., Matsumoto B. Evidence from normal and degenerating photoreceptors that two outer segment integral membrane proteins have separate transport pathways. Journal of Comparative Neurology 1997, 387:148-156.
13. Felgner H., Frank R., Biernat J., Mandelkow E.M., Mandelkow E., Ludin B., Matus A., Schliwa M. Domains of neuronal microtubule-associated proteins and flexural rigidity of microtubules. Journal of Cell Biology 1997, 138:1067-1075.
14. Felgner H., Frank R., Schliwa M. Flexural rigidity of microtubules measured with the use of optical tweezers. Journal of Cell Science 1996, 109(2):509-516.
15. Gardner K., Arnoczky S.P., Lavagnino M. Effect of in vitro stress-deprivation and cyclic loading on the length of tendon cell cilia in situ. Journal of Orthopaedic Research 2011, 29:582-587.
16. Geiger R.C., Kaufman C.D., Lam A.P., Budinger G.R., Dean D.A. Tubulin acetylation and histone deacetylase 6 activity in the lung under cyclic load. American Journal of Respiratory Cell and Molecular Biology 2009, 40:76-82.
17. Gilula N.B., Satir P. The ciliary necklace. A ciliary membrane specialization. Journal of Cell Biology 1972, 53:494-509.
18. Gradilone S.A., Masyuk A.I., Splinter P.L., Banales J.M., Huang B.Q., Tietz P.S., Masyuk T.V., Larusso N.F. Cholangiocyte cilia express TRPV4 and detect changes in luminal tonicity inducing bicarbonate secretion. Proceedings of the National Academy of Sciences USA 2007, 104:19138-19143.
19. Gudima G.O., Vorob'ev I.A., Chentsov Iu S. Behavior of the cell center in the distribution of fibroblasts. Nauchnye Dokiady Vysshei Shkoly, Biologicheskie Nauki 1983, 45-50.
20. Gudima G.O., Vorob'ev I.A., Chentsov Iu S. Structural change in the cell center during fibroblast polarization and movement. Tsitologiia 1983, 25:883-888.
21. Hagiwara H., Aoki T., Fujimoto T. Ultrastructural observation on 'transitional tubules' in human oviductal ciliogenic cells. Journal of Anatomy 1997, 191(2):285-290.
22. Hagiwara H., Aoki T., Ohwada N., Fujimoto T. Development of striated rootlets during ciliogenesis in the human oviduct epithelium. Cell and Tissue Research 1997, 290:39-42.
23. Hagiwara H., Harada S., Maeda S., Aoki T., Ohwada N., Takata K. Ultrastructural and immunohistochemical study of the basal apparatus of solitary cilia in the human oviduct epithelium. Journal of Anatomy 2002, 200:89-96.
24. Hagiwara H., Takata K. Depolymerization of microtubules by colcemid induces the formation of elongated and centriole-nonassociated striated rootlets in PtK(2) cells. Cell and Tissue Research 2002, 309:287-292.
25. Hierck B.P., Van der Heiden K., Alkemade F.E., Van de Pas S., Van Thienen J.V., Groenendijk B.C., Bax W.H., Van der Laarse A., Deruiter M.C., Horrevoets A.J., Poelmann R.E. Primary cilia sensitize endothelial cells for fluid shear stress. Developmental Dynamics 2008, 237:725-735.
26. Hildebrandt F., Benzing T., Katsanis N. Ciliopathies. New England Journal of Medicine 2011, 364:1533-1543.
27. Holley M.C. The ciliary basal apparatus is adapted to the structure and mechanics of the epithelium. Tissue and Cell 1984, 16:287-310.
28. Kelly P.J., Pocock N.A., Sambrook P.N., Eisman J.A. Age and menopause-related changes in indices of bone turnover. The Journal of Clinical Endocrinology and Metabolism 1989, 69:1160-1165.
29. Kobayashi N., Hirokawa N. Cytoskeletal architecture and immunocytochemical localization of fodrin in the terminal web of the ciliated epithelial cell. Cell Motility and the Cytoskeleton 1988, 11:167-177.
30. Kwon R.Y., Temiyasathit S., Tummala P., Quah C.C., Jacobs C.R. Primary cilium-dependent mechanosensing is mediated by adenylyl cyclase 6 and cyclic AMP in bone cells. FASEB Journal 2010.
31. Linck R.W. Flagellar doublet microtubules-fractionation of minor components and alpha-tubulin from specific regions of a-tubule. Journal of Cell Science 1976, 20:405-439.
32. Linck R.W., Goggin M.J., Norrander J.M., Steffen W. Characterization of antibodies as probes for structural and biochemical studies of tektins from ciliary and flagellar microtubules. Journal of Cell Science 1987, 88(4):453-466.
33. 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. American Journal of Physiology Renal Physiology 2003, 285:F998-F1012.
34. Low S.H., Vasanth S., Larson C.H., Mukherjee S., Sharma N., Kinter M.T., Kane M.E., Obara T., Weimbs T. Polycystin-1, STAT6, and P100 function in a pathway that transduces ciliary mechanosensation and is activated in polycystic kidney disease. Developmental Cell 2006, 10:57-69.
35. Mahoney N.M., Goshima G., Douglass A.D., Vale R.D. Making microtubules and mitotic spindles in cells without functional centrosomes. Current Biology 2006, 16:564-569.
36. Malone A.M., Anderson C.T., Tummala P., Kwon R.Y., Johnston T.R., Stearns T., Jacobs C.R. Primary cilia mediate mechanosensing in bone cells by a calcium-independent mechanism. Proceedings of the National Academy of Sciences USA 2007, 104:13325-13330.
37. 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.
38. McGlashan S.R., Knight M.M., Chowdhury T.T., Joshi P., Jensen C.G., Kennedy S., Poole C.A. Mechanical loading modulates chondrocyte primary cilia incidence and length. Cell Biology International 2010, 34:441-446.
39. Menco B.P., Farbman A.I. Genesis of cilia and microvilli of rat nasal epithelia during pre-natal development. II. Olfactory epithelium, a morphometric analysis. Journal of Cell Science 1985, 78:311-336.
40. Mofrad M.R.K., Kamm R.D. Cellular Mechanotransduction: Diverse Perspectives from Molecules to Tissues 2010, Cambridge University Press, Cambridge; New York.
41. Nauli S.M., Alenghat F.J., Luo Y., Williams E., Vassilev P., Li X., Elia A.E., Lu W., Brown E.M., Quinn S.J., Ingber D.E., Zhou J. Polycystins 1 and 2 mediate mechanosensation in the primary cilium of kidney cells. Nature Genetics 2003, 33:129-137.
42. Nogales E., Whittaker M., Milligan R.A., Downing K.H. High-resolution model of the microtubule. Cell 1999, 96:79-88.
43. OBrien E.T., Salmon E.D., Erickson H.P. How calcium causes microtubule depolymerization. Cell Motility and the Cytoskeleton 1997, 36:125-135.
44. Odor D.L., Blandau R.J. Observations on the solitary cilium of rabbit oviductal epithelium: its motility and ultrastructure. American Journal of Anatomy 1985, 174:437-453.
45. Odor D.L., Blandau R.J. Observations on the solitary cilium of rabbit oviductal epithelium: its motility and ultrastructure. American Journal of Anatomy 1985, 174:437-453.
46. Pae S.S., Saunders J.C. Intra- and extracellular calcium modulates stereocilia stiffness on chick cochlear hair cells. Proceedings of the National Academy of Sciences USA 1994, 91:1153-1157.
47. Phan M.N., Leddy H.A., Votta B.J., Kumar S., Levy D.S., Lipshutz D.B., Lee S.H., Liedtke W., Guilak F. Functional characterization of TRPV4 as an osmotically sensitive ion channel in porcine articular chondrocytes. Arthritis and Rheumatism 2009, 60:3028-3037.
48. Poole C.A., Zhang Z.J., Ross J.M. The differential distribution of acetylated and detyrosinated alpha-tubulin in the microtubular cytoskeleton and primary cilia of hyaline cartilage chondrocytes. Journal of Anatomy 2001, 199:393-405.
49. Praetorius H.A., Spring K.R. Bending the MDCK cell primary cilium increases intracellular calcium. Journal of Membrane Biology 2001, 184:71-79.
50. Praetorius H.A., Spring K.R. Removal of the MDCK cell primary cilium abolishes flow sensing. Journal of Membrane Biology 2003, 191:69-76.
51. Praetorius H.A., Spring K.R. A physiological view of the primary cilium. Annual Review of Physiology 2005, 67:515-529.
52. Quarmby L. Ciliary ion channels: location, location, location. Current Biology 2009, 19:R158-160.
53. Resnick A., Hopfer U. Force-response considerations in ciliary mechanosensation. Biophysical Journal 2007, 93:1380-1390.
54. Rikmenspoel R., Sleigh M.A. Bending moments and elastic constants in cilia. Journal of Theoretical Biology 1970, 28:81-100.
55. Rohatgi R., Snell W.J. The ciliary membrane. Current Opinion in Cell Biology 2010.
56. Roth K.E., Rieder C.L., Bowser S.S. Flexible-substratum technique for viewing cells from the side: some in vivo properties of primary (9+0) cilia in cultured kidney epithelia. Journal of Cell Science 1988, 89(Pt 4):457-466.
57. 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. American Journal of Physiology Renal Physiology 2010.
58. Satir P., Gilula N.B. The cell junction in a lamellibranch gill ciliated epithelium: localization of pyroantimonate precipitate. Journal of Cell Biology 1970, 47:468-487.
59. Schwartz E.A., Leonard M.L., Bizios R., Bowser S.S. Analysis and modeling of the primary cilium bending response to fluid shear. American Journal of Physiology Renal Physiology 1997, 272:F132-F138.
60. Sellner W., Oberkanins C., Stockinger L., Wiche G. Ultrastructural localization of microtubule-associated proteins (MAP) 1 in cilia of the respiratory tract. European Journal of Cell Biology 1991, 55:248-254.
61. Shida T., Cueva J.G., Xu Z., Goodman M.B., Nachury M.V. The major alpha-tubulin K40 acetyltransferase alphaTAT1 promotes rapid ciliogenesis and efficient mechanosensation. Proceedings of the National Academy of Sciences USA 2010, 107:21517-21522.
62. Silvester N.R. The cilia of tetrahymena pyriformis: X-Ray diffraction by the ciliary membrane. Journal of Molecular Biology 1964, 8:11-19.
63. Singla V., Reiter J.F. The primary cilium as the cell's antenna: signaling at a sensory organelle. Science 2006, 313:629-633.
64. Sui H., Downing K.H. Molecular architecture of axonemal microtubule doublets revealed by cryo-electron tomography. Nature 2006, 442:475-478.
65. Takemura R., Okabe S., Umeyama T., Kanai Y., Cowan N.J., Hirokawa N. Increased microtubule stability and alpha tubulin acetylation in cells transfected with microtubule-associated proteins MAP1B, MAP2 or tau. Journal of Cell Science 1992, 103(4):953-964.
66. Veland I.R., Awan A., Pedersen L.B., Yoder B.K., Christensen S.T. Primary cilia and signaling pathways in mammalian development, health and disease. Nephron Physiology 2009, 111:39-53.
67. Westermann S., Weber K. Post-translational modifications regulate microtubule function. Nature Reviews Molecular Cell Biology 2003, 4:938-947.
68. Wheatley D.N. Nanobiology of the primary cilium-paradigm of a multifunctional nanomachine complex. Methods in Cell Biology 2008, 90:139-156.
69. Wiche G., Herrmann H., Dalton J.M., Foisner R., Leichtfried F.E., Lassmann H., Koszka C., Briones E. Molecular aspects of MAP-1 and MAP-2: microheterogeneity, in vitro localization and distribution in neuronal and nonneuronal cells. Annals of the New York Academy of Sciences 1986, 466:180-198.
70. Xiao Z.S., Quarles L.D. Role of the polycytin-primary cilia complex in bone development and mechanosensing. Annals of the New York Academy of Sciences 2010, 1192:410-421.
71. Yamamoto M., Kataoka K. Electron microscopic observation of the primary cilium in the pancreatic islets. Archivum Histologicum Japonicum 1986, 49:449-457.
72. Yang J., Gao J., Adamian M., Wen X.H., Pawlyk B., Zhang L., Sanderson M.J., Zuo J., Makino C.L., Li T. The ciliary rootlet maintains long-term stability of sensory cilia. Molecular and Cellular Biology 2005, 25:4129-4137.
73. Zhang M.Z., Mai W., Li C., Cho S.Y., Hao C., Moeckel G., Zhao R., Kim I., Wang J., Xiong H., Wang H., Sato Y., Wu Y., Nakanuma Y., Lilova M., Pei Y., Harris R.C., Li S., Coffey R.J., Sun L., Wu D., Chen X.Z., Breyer M.D., Zhao Z.J., McKanna J.A., Wu G. PKHD1 protein encoded by the gene for autosomal recessive polycystic kidney disease associates with basal bodies and primary cilia in renal epithelial cells. Proceedings of the National Academy of Sciences USA 2004, 101:2311-2316.