Ciliary behaviour and mechano-transduction in the embryonic node: Computational testing of hypotheses

Medical Engineering and Physics

Volumn 33, Issue 7, 2011, Pages 857-867

  Chen, Duanduan ^a   Norris, Dominic ^b   Ventikos, Yiannis ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b MRC MAMMALIAN GENETICS UNIT   (United Kingdom)

Author keywords

Computational fluid dynamics; Dynein activation; Embryonic node; Finite element analysis; Fluid structure interaction; Primary cilia

Indexed keywords

ACTIVATION PATTERNS; CLOCKWISE ROTATION; COMPUTATIONAL MODEL; COMPUTATIONAL TECHNIQUE; COMPUTATIONAL TESTING; DEFORMABLE MESH; DYNEIN ACTIVATION; EMBRYONIC NODE; EMBRYONIC STRUCTURES; GRID DEFORMATION TECHNIQUE; LEFT-RIGHT SYMMETRY; MECHANOSENSORS; MECHANOTRANSDUCTION; MOTOR PROTEINS; PRIMARY CILIA; PROTEIN ACTIVITY; PROTEIN MOTORS; ROTATIONAL MOTION; UNIDIRECTIONAL FLOW; UNSTEADY TRANSPORT; WHIRLING MOTION;

ACTIVATION ANALYSIS; COMPUTATIONAL FLUID DYNAMICS; DEFORMATION; FLUID STRUCTURE INTERACTION; FLUIDS; MAMMALS; PROTEINS; ROTATION;

FINITE ELEMENT METHOD;

AXONEMAL DYNEIN; MOLECULAR MOTOR;

ARTICLE; AXOPLASM FLOW; CILIARY MOTILITY; COMPUTATIONAL FLUID DYNAMICS; EMBRYONIC STRUCTURES; FINITE ELEMENT ANALYSIS; FLOW RATE; FLUID FLOW; MECHANOTRANSDUCTION; MICROTUBULE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN STRUCTURE; SIMULATION;

CILIA; COMPUTER SIMULATION; DYNEINS; EMBRYO, MAMMALIAN; FINITE ELEMENT ANALYSIS; HYDRODYNAMICS; MECHANOTRANSDUCTION, CELLULAR; MODELS, BIOLOGICAL; MOVEMENT; PRESSURE; STRESS, MECHANICAL;

EID: 79961027271     PISSN: 13504533     EISSN: 18734030     Source Type: Journal    
DOI: 10.1016/j.medengphy.2010.10.020     Document Type: Article

References (62)

1. Levin M. Left-right asymmetry in embryonic development: a comprehensive review. Mech Dev 2005, 122(1):3-25.
2. Capdevila J., Vogan K.J., Tabin C.J., Izpisua Belmonte J.C. Mechanisms of left-right determination in vertebrates. Cell 2000, 101(1):9-21.
3. van der Baan S., Veerman A.J., Weltevreden E., Feenstra L. Primary ciliary dyskinesia; ciliary activity and ultrastructure in 11 patients with Kartagener syndrome. Ned Tijdschr Geneeskd 1982, 126(52):2376-2379.
4. Walter R.J., Malech H.L., Oliver J.M. Cell motility and microtubules in cultured fibroblasts from patients with Kartagener syndrome. Cell Motil 1983, 3(2):185-197.
5. Takeda S., Yonekawa Y., Tanaka Y., Okada Y., Nonaka S., Hirokawa N. Left-right asymmetry and kinesin superfamily protein KIF3A: new insights in determination of laterality and mesoderm induction by kif3A(-/-) mice analysis. J Cell Biol 1999, 145(4):825-836.
6. 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(6):829-837.
7. Okada Y., Nonaka S., Tanaka Y., Saijoh Y., Hamada H., Hirokawa N. Abnormal nodal flow precedes situs inversus in iv and inv mice. Mol Cell 1999, 4(4):459-468.
8. Essner J.J., Vogan K.J., Wagner M.K., Tabin C.J., Yost H.J., Brueckner M. Conserved function for embryonic nodal cilia. Nature 2002, 418(6893):37-38.
9. Hamada H., Meno C., Watanabe D., Saijoh Y. Establishment of vertebrate left-right asymmetry. Nat Rev Genet 2002, 3(2):103-113.
10. Marszalek J.R., Ruiz-Lozano P., Roberts E., Chien K.R., Goldstein L.S. Situs inversus and embryonic ciliary morphogenesis defects in mouse mutants lacking the KIF3A subunit of kinesin-II. Proc Natl Acad Sci USA 1999, 96(9):5043-5048.
11. Hirokawa N., Tanaka Y., Okada Y., Takeda S. Nodal flow and the generation of left-right asymmetry. Cell 2006, 125(1):33-45.
12. Yost H.J. Left-right asymmetry: nodal cilia make and catch a wave. Curr Biol 2003, 13(20):R808-R809.
13. Goggin P. Private Communication. Biomedical Imaging Unit. Southampton University.
14. Burgess S.A., Walker M.L., Sakakibara H., Knight P.J., Oiwa K. Dynein structure and power stroke. Nature 2003, 421(6924):715-718.
15. Cartwright J.H., Piro O., Tuval I. Fluid-dynamical basis of the embryonic development of left-right asymmetry in vertebrates. Proc Natl Acad Sci USA 2004, 101(19):7234-7239.
16. Nonaka S., Yoshiba S., Watanabe D., Ikeuchi S., Goto T., Marshall W.F., et al. De novo formation of left-right asymmetry by posterior tilt of nodal cilia. PLoS Biol 2005, 3(8):pe268.
17. Sulik K., Dehart D.B., Iangaki T., Carson J.L., Vrablic T., Gesteland K., et al. Morphogenesis of the murine node and notochordal plate. Dev Dyn 1994, 201(3):260-278.
18. Tabin C.J., Vogan K.J. A two-cilia model for vertebrate left-right axis specification. Genes Dev 2003, 17(1):1-6.
19. Nonaka S., Shiratori H., Saijoh Y., Hamada H. Determination of left-right patterning of the mouse embryo by artificial nodal flow. Nature 2002, 418(6893):96-99.
20. Tanaka Y., Okada Y., Hirokawa N. FGF-induced vesicular release of Sonic hedgehog and retinoic acid in leftward nodal flow is critical for left-right determination. Nature 2005, 435(7039):172-177.
21. 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(1):61-73.
22. Pazour G.J., Witman G.B. The vertebrate primary cilium is a sensory organelle. Curr Opin Cell Biol 2003, 15(1):105-110.
23. Karcher C., Fischer A., Schweickert A., Bitzer E., Horie S., Witzgall R., et al. Lack of a laterality phenotype in Pkd1 knock-out embryos correlates with absence of polycystin-1 in nodal cilia. Differentiation 2005, 73(8):425-432.
24. Shiratori H., Hamada H. The left-right axis in the mouse: from origin to morphology. Development 2006, 133(11):2095-2104.
25. Shiba D., Takamatsu T., Yokoyama T. Primary cilia of inv/inv mouse renal epithelial cells sense physiological fluid flow: bending of primary cilia and Ca2+ influx. Cell Struct Funct 2005, 30(2):93-100.
26. Praetorius H.A., Spring K.R. Bending the MDCK cell primary cilium increases intracellular calcium. J Membr Biol 2001, 184(1):71-79.
27. Praetorius H.A., Frokiaer J., Nielsen S., Spring K.R. Bending the primary cilium opens Ca2+-sensitive intermediate-conductance K+ channels in MDCK cells. J Membr Biol 2003, 191(3):193-200.
28. Pennekamp P., Karcher C., Fischer A., Schweickert A., Skryabin B., Horst J., et al. The ion channel polycystin-2 is required for left-right axis determination in mice. Curr Biol 2002, 12(11):938-943.
29. Taylor G. Analysis of the swimming of microscopic organisms. Proc R Soc Lond Ser B-Biol Sci 1951, 139(894):141-1141.
30. Taylor B.L., Koshland D.E. Reversal of flagellar rotation in monotrichous and peritrichous bacteria: generation of changes in direction. J Bacteriol 1974, 119(2):640-642.
31. Taylor J., Lee M.M., Edwards P.R., Ramsey C.H. A new type of flagellar variation associated with new antigens in the Salmonella group. J Gen Microbiol 1960, 23:583-588.
32. Gray J., Hancock G.J. The propulsion of sea-urchin spermatozoa. J Exp Biol 1955, 32(4):802-814.
33. Lighthill J. Flagellar hydrodynamics - Neumann, Jv lecture, 1975. Siam Rev 1976, 18(2):161-230.
34. Dresdner R.D., Katz D.F., Berger S.A. The propulsion by large-amplitude waves of uniflagellar microorganisms of finite length. J Fluid Mech 1980, 97(April):591-621.
35. Higdon J.J.L. Hydrodynamics of flagellar propulsion - helical waves. J Fluid Mech 1979, 94(Sep):331-351.
36. Higdon J.J.L. Generation of feeding currents by flagellar motions. J Fluid Mech 1979, 94(September):305-330.
37. Phanthien N., Trancong T., Ramia M. A boundary-element analysis of flagellar propulsion. J Fluid Mech 1987, 184:533-549.
38. Dillon R.H., Fauci L.J. An integrative model of internal axoneme mechanics and external fluid dynamics in ciliary beating. J Theor Biol 2000, 207(3):415-430.
39. Dillon R.H., Fauci L.J., Omoto C. Mathematical modeling of axoneme mechanics and fluid dynamics in ciliary and sperm motility. Dyn Contin Discret Impulsive Syst-Ser A-Math Anal 2003, 10(5):745-757.
40. Dillon R., Fauci L. A microscale model of bacterial and biofilm dynamics in porous media. Biotechnol Bioeng 2000, 68(5):536-547.
41. Chen D., Norris D., Ventikos Y. The active and passive ciliary motion in the embryo node: a computational fluid dynamics model. J Biomech 2009, 42(3):210-216.
42. Gueron S., Liron N. Ciliary motion modeling, and dynamic multicilia interactions. Biophys J 1992, 63(4):1045-1058.
43. Gueron S., Levit-Gurevich K., Liron N., Blum J.J. Cilia internal mechanism and metachronal coordination as the result of hydrodynamical coupling. Proc Natl Acad Sci USA 1997, 94(12):6001-6006.
44. Gueron S., Liron N. Simulations of three-dimensional ciliary beats and cilia interactions. Biophys J 1993, 65(1):499-507.
45. Mitran S.M. Metachronal wave formation in a model of pulmonary cilia. Comput Struct 2007, 85(11-14):763-774.
46. Okada Y., Takeda S., Tanaka Y., Belmonte J.C., Hirokawa N. Mechanism of nodal flow: a conserved symmetry breaking event in left-right axis determination. Cell 2005, 121(4):633-644.
47. Buceta J., Ibanes M., Rasskin-Gutman D., Okada Y., Hirokawa N., Izpisua-Belmonte J. Nodal cilia dynamics and the specification of the left/right axis in early vertebrate embryo development. Biophys J 2005, 89(4):2199-2209.
48. 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(1 Pt 2):F132-F138.
49. Baba S.A. Flexural rigidity and elastic-constant of cilia. J Exp Biol 1972, 56(2):459-467.
50. Venier P., Maggs A.C., Carlier M.F., Pantaloni D. Analysis of microtubule rigidity using hydrodynamic flow and thermal fluctuations. J Biol Chem 1994, 269(18):13353-13360.
51. Byfield F.J., Aranda-Espinoza H., Romanenko V.G., Rothblat G.H., Levitan I. Cholesterol depletion increases membrane stiffness of aortic endothelial cells. Biophys J 2004, 87(5):3336-3343.
52. Parsegian V.A., Fuller N., Rand R.P. Measured work of deformation and repulsion of lecithin bilayers. Proc Natl Acad Sci USA 1979, 76(6):2750-2754.
53. Fox L.A., Sale W.S. Direction of force generated by the inner row of dynein arms on flagellar microtubules. J Cell Biol 1987, 105(4):1781-1787.
54. Schmitz K.A., Holcomb-Wygle D.L., Oberski D.J., Lindemann C.B. Measurement of the force produced by an intact bull sperm flagellum in isometric arrest and estimation of the dynein stall force. Biophys J 2000, 79(1):468-478.
55. Seetharam R.N., Satir P. Coordination of outer arm dynein activity along axonemal doublet microtubules. Cell Motil Cytoskeleton 2008, 65(7):572-580.
56. Cartwright J.H., Piro N., Piro O., Tuval I. Embryonic nodal flow and the dynamics of nodal vesicular parcels. J R Soc Interface 2006.
57. Vandoormaal J.P., Raithby G.D. Enhancements of the simple method for predicting incompressible fluid-flows. Numer Heat Transfer 1984, 7(2):147-163.
58. Lonsdale G., Schuller A. Multigrid efficiency for complex flow simulations on distributed memory machines. Parallel Comput 1993, 19(1):23-32.
59. Zienkiewicz O.C. The finite element method in engineering science 1971, McGraw-Hill Publ, New York.
60. Johnson A.A., Tezduyar T.E. Mesh update strategies in parallel finite-element computations of flow problems with moving boundaries and interfaces. Comput Methods Appl Mech Eng 1994, 119(1-2):73-94.
61. Smith D.J., Blake J.R., Gaffney E.A. Fluid mechanics of nodal flow due to embryonic primary cilia. J R Soc Interface 2008, 5(22):567-573.
62. McGrath J., Brueckner M. Cilia are at the heart of vertebrate left-right asymmetry. Curr Opin Genet Dev 2003, 13(4):385-392.