Ciliary beat co-ordination by calcium

Biology of the Cell

Volumn 103, Issue 4, 2011, Pages 159-169

  Schmid, Andreas ^a   Salathe, Matthias ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

Acetylcholine (Ach); Calcium; Ciliary beat frequency (CBF); Pannexin; Purinergic signalling; Synchronization

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CALCIUM; CHOLINERGIC RECEPTOR; PURINERGIC RECEPTOR;

CALCIUM CELL LEVEL; CILIARY MOTILITY; ENZYME ACTIVITY; HUMAN; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY EPITHELIUM; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CALCIUM; CILIA; HUMANS; MUCOCILIARY CLEARANCE; RESPIRATORY MUCOSA;

EID: 79952746347     PISSN: 02484900     EISSN: 1768322X     Source Type: Journal    
DOI: 10.1042/BC20100120     Document Type: Review

References (85)

1. Aiello, E. and Sleigh, M.A. (1972) The metachronal wave of lateral cilia of Mytilus edulis. J. Cell Biol. 54, 493-506
2. Andrade, Y.N., Fernandes, J., Vazquez, E., Fernandez-Fernandez, J.M., Arniges, M., Sanchez, T.M., Villalon, M. and Valverde, M.A. (2005) TRPV4 channel is involved in the coupling of fluid viscosity changes to epithelial ciliary activity. J. Cell Biol. 168, 869-874 (Pubitemid 40403090)
3. Andrivon, C. (1988) Membrane control of ciliary movement in ciliates. Biol. Cell 63, 133-142
4. 2+ entry via TRPV4 channel is defective in cystic fibrosis airway epithelia. J. Biol. Chem. 279, 54062-54068
5. Boitano, S., Dirksen, E.R. and Sanderson, M.J. (1992) Intercellular propagation of calcium waves mediated by inositol trisphosphate. Science 258, 292-295
6. 2+ redistribution. Cell Calcium 30, 361-371
7. Braiman, A. and Priel, Z. (2008) Efficient mucociliary transport relies on efficient regulation of ciliary beating. Respir. Physiol. Neurobiol. 163, 202-207
8. 2+-dependent and -independent manner. Am. J. Physiol. 275, C790-C797
9. 2+ gradient in the cytosol of electrically non-excitable cells. J. Theor. Biol. 206, 115-130
10. Buck, J. and Buck, E. (1968) Mechanism of rhythmic synchronous flashing of firefliesFireflies of Southeast Asia may use anticipatory time-measuring in synchronizing their flashing. Science 159, 1319-1327
11. Contreras, J.E., Saez, J.C., Bukauskas, F.F. and Bennett, M.V. (2003) Gating and regulation of connexin 43 (Cx43) hemichannels. Proc. Natl. Acad. Sci. U.S.A. 100, 11388-11393
12. Cotrina, M.L., Lin, J.H., Alves-Rodrigues, A., Liu, S., Li, J., Azmi-Ghadimi, H., Kang, J., Naus, C.C. and Nedergaard, M. (1998) Connexins regulate calcium signaling by controlling ATP release. Proc. Natl. Acad. Sci. U.S.A. 95, 15735-15740
13. Cotrina, M.L., Lin, J.H., Lopez-Garcia, J.C., Naus, C.C. and Nedergaard, M. (2000) ATP-mediated glia signaling. J. Neurosci. 20, 2835-2844 (Pubitemid 30220308)
14. Delmotte, P. and Sanderson, M.J. (2006) Ciliary beat frequency is maintained at a maximal rate in the small airways of mouse lung slices. Am. J. Respir. Cell. Mol. Biol. 35, 110-117
15. Di Benedetto, G., Magnus, C.J., Gray, P.T. and Mehta, A. (1991) Calcium regulation of ciliary beat frequency in human respiratory epithelium in vitro. J. Physiol. 439, 103-113
16. Dymek, E.E. and Smith, E.F. (2007) A conserved CaM- and radial spoke associated complex mediates regulation of flagellar dynein activity. J. Cell. Biol. 179, 515-526
17. Evans, J.H. and Sanderson, M.J. (1999) Intracellular calcium oscillations induced by ATP in airway epithelial cells. Am. J. Physiol. 277, L30-L41
18. Evans, W.H., De Vuyst, E. and Leybaert, L. (2006) The gap junction cellular internet: connexin hemichannels enter the signalling limelight. Biochem. J. 397, 1-14 (Pubitemid 44032830)
19. 3 sensitizes TRPV4 channel to the mechano- and osmotransducing messenger 5′-6′-epoxyeicosatrienoic acid. J. Cell. Biol. 181, 143-155
20. Fujiu, K., Nakayama, Y., Yanagisawa, A., Sokabe, M. and Yoshimura, K. (2009) Chlamydomonas CAV2 encodes a voltage- dependent calcium channel required for the flagellar waveform conversion. Curr. Biol. 19, 133-139
21. Gheber, L. and Priel, Z. (1989) Synchronization between beating cilia. Biophys. J. 55, 183-191 (Pubitemid 19033367)
22. Gheber, L., Korngreen, A. and Priel, Z. (1998) Effect of viscosity on metachrony in mucus propelling cilia. Cell Motil. Cytoskeleton 39, 9-20 (Pubitemid 28042455)
23. 2+ channels in sea urchin sperm. FEBS Lett. 579, 6667-6672
24. Gray, J. (1930) The mechanism of ciliary movement. VI. Photographica and stroboscopic analysis of ciliary movement. Proc. R. Soc. Lond. B 107, 313-332
25. Guirao, B. and Joanny, J.F. (2007) Spontaneous creation of macroscopic flow and metachronal waves in an array of cilia. Biophys. J. 92, 1900-1917 (Pubitemid 46495255)
26. Hayashi, T., Kawakami, M., Sasaki, S., Katsumata, T., Mori, H., Yoshida, H. and Nakahari, T. (2005) ATP regulation of ciliary beat frequency in rat tracheal and distal airway epithelium. Exp. Physiol. 90, 535-544
27. Homolya, L., Steinberg, T.H. and Boucher, R.C. (2000) Cell to cell communication in response to mechanical stress via bilateral release of ATP and UTP in polarized epithelia. J. Cell. Biol. 150, 1349-1360
28. Hu, Q., Milenkovic, L., Jin, H., Scott, M.P., Nachury, M.V., Spiliotis, E.T. and Nelson, W.J. (2010) A septin diffusion barrier at the base of the primary cilium maintains ciliary membrane protein distribution. Science 329, 436-439
29. Huang, Y.J., Maruyama, Y., Dvoryanchikov, G., Pereira, E., Chaudhari, N. and Roper, S.D. (2007) The role of pannexin 1 hemichannels in ATP release and cell-cell communication in mouse taste buds. Proc. Natl. Acad. Sci. U.S.A. 104, 6436-6441
30. Irvine, R.F. (2003) 20 years of Ins(1,4,5)P3, and 40 years before. Nat. Rev. Mol. Cell. Biol. 4, 586-590
31. 2+ waves in ciliated tracheal epithelial cells. Respir Res. 7, 105
32. Katan, M. (1998) Families of phosphoinositide-specific phospholipase C: structure and function. Biochim. Biophys. Acta 1436, 5-17
33. Kinosita, H. and Murakami, A. (1967) Control of ciliary motion. Physiol. Rev. 47, 53-82
34. Koenigsberger, M., Sauser, R. and Meister, J.J. (2005) Emergent properties of electrically coupled smooth muscle cells. Bull. Math. Biol. 67, 1253-1272
35. Korngreen, A. and Priel, Z. (1996) Purinergic stimulation of rabbit ciliated airway epithelia: control by multiple calcium sources. J. Physiol. 497, 53-66 (Pubitemid 26397672)
36. Korngreen, A., Ma, W., Priel, Z. and Silberberg, S.D. (1998) Extracellular ATP directly gates a cation-selective channel in rabbit airway ciliated epithelial cells. J. Physiol. 508, 703-720 (Pubitemid 28220726)
37. Laitinen, A. (1985) Autonomic innervation of the human respiratory tract as revealed by histochemical and ultrastructural methods. Eur. J. Respir. Dis. Suppl. 140, 1-42
38. Levin, R., Braiman, A. and Priel, Z. (1997) Protein kinase C induced calcium influx and sustained enhancement of ciliary beating by extracellular ATP. Cell Calcium 21, 103-113 (Pubitemid 27105834)
39. Lieb, T., Frei, C.W., Frohock, J.I., Bookman, R.J. and Salathe, M. (2002) Prolonged increase in ciliary beat frequency after short-term purinergic stimulation in human airway epithelial cells. J. Physiol. 538, 633-646 (Pubitemid 35175386)
40. Liedtke, W., Choe, Y., Marti-Renom, M.A., Bell, A.M., Denis, C.S., Sali, A., Hudspeth, A.J., Friedman, J.M. and Heller, S. (2000) Vanilloid receptor-related osmotically activated channel (VR-OAC), a candidate vertebrate osmoreceptor. Cell 103, 525-535
41. Liedtke, W., Tobin, D.M., Bargmann, C.I. and Friedman, J.M. (2003) Mammalian TRPV4 (VR-OAC) directs behavioral responses to osmotic and mechanical stimuli in Caenorhabditis elegans. Proc. Natl. Acad. Sci. U.S.A. 100 (Suppl. 2), 14531-14536 (Pubitemid 37499277)
42. Locovei, S., Bao, L. and Dahl, G. (2006) Pannexin 1 in erythrocytes: function without a gap. Proc. Natl. Acad. Sci. U.S.A. 103, 7655-7659
43. Lorenzo, I.M., Liedtke, W., Sanderson, M.J. and Valverde, M.A. (2008) TRPV4 channel participates in receptor-operated calcium entry and ciliary beat frequency regulation in mouse airway epithelial cells. Proc. Natl. Acad. Sci. U.S.A. 105, 12611-12616
44. Ma, W., Silberberg, S.D. and Priel, Z. (2002) Distinct axonemal processes underlie spontaneous and stimulated airway ciliary activity. J. Gen. Physiol. 120, 875-885
45. Ma, W., Korngreen, A., Weil, S., Cohen, E.B., Priel, A., Kuzin, L. and Silberberg, S.D. (2006) Pore properties and pharmacological features of the P2X receptor channel in airway ciliated cells. J. Physiol. 571, 503-517 (Pubitemid 43329544)
46. Matsuda, A., Yoshimura, K., Sineshchekov, O.A., Hirono, M. and Kamiya, R. (1998) Isolation and characterization of novel Chlamydomonas mutants that display phototaxis but not photophobic response. Cell Motil. Cytoskeleton 41, 353-362 (Pubitemid 29086470)
47. Morse, D.M., Smullen, J.L. and Davis, C.W. (2001) Differential effects of UTP, ATP, and adenosine on ciliary activity of human nasal epithelial cells. Am. J. Physiol. Cell Physiol. 280, C1485-C1497
48. Murata, Y., Iwasaki, H., Sasaki, M., Inaba, K. and Okamura, Y. (2005) Phosphoinositide phosphatase activity coupled to an intrinsic voltage sensor. Nature 435, 1239-1243 (Pubitemid 40943089)
49. Naito, Y. and Kaneko, H. (1972) Reactivated triton-extracted models of Paramecium: modification of ciliary movement by calcium ions. Science 176, 523-524
50. Niedermayer, T., Eckhardt, B. and Lenz, P. (2008) Synchronization, phase locking, and metachronal wave formation in ciliary chains. Chaos 18, 037128
51. Nishizuka, Y. (1988) The molecular heterogeneity of protein kinase C and its implications for cellular regulation. Nature 334, 661-665
52. Nlend, M.C., Schmid, A., Sutto, Z., Ransford, G.A., Conner, G.E., Fregien, N. and Salathe, M. (2007) Calcium-mediated, purinergic stimulation and polarized localization of calcium-sensitive adenylyl cyclase isoforms in human airway epithelia. FEBS Lett. 581, 3241-3246 (Pubitemid 46977371)
53. Okuno, M. and Hiramoto, Y. (1976) Mechanical stimulation of starfish sperm flagella. J. Exp. Biol. 65, 401-413
54. Pazour, G.J., Agrin, N., Leszyk, J. and Witman, G.B. (2005) Proteomic analysis of a eukaryotic cilium. J. Cell. Biol. 170, 103-113
55. Petersen, O.H. and Verkhratsky, A. (2007) Endoplasmic reticulum calcium tunnels integrate signalling in polarised cells. Cell Calcium 42, 373-378 (Pubitemid 47264014)
56. Quarmby, L. (2009) Ciliary ion channels: location, location, location. Curr. Biol. 19, R158-R160
57. Ramirez, J.M., Tryba, A.K. and Pena, F. (2004) Pacemaker neurons and neuronal networks: an integrative view. Curr. Opin. Neurobiol. 14, 665-674
58. Ransford, G.A., Fregien, N., Qiu, F., Dahl, G., Conner, G.E. and Salathe, M. (2009) Pannexin 1 contributes to ATP release in airway epithelia. Am. J. Respir. Cell Mol. Biol. 41, 525-534
59. Rasmussen, H. and Rasmussen, J.E. (1990) Calcium as intracellular messenger: from simplicity to complexity. Curr. Top. Cell. Regul. 31, 1-109
60. 2+. Mol. Biol. Cell 18, 3620-3634
61. Salathe, M. (2007) Regulation of mammalian ciliary beating. Annu. Rev. Physiol. 69, 401-422
62. i and ciliary beating in cultured tracheal epithelial cells. J. Cell Sci. 108, 431-440
63. Salathe, M. and Bookman, R.J. (1999) Mode of Ca2+ action on ciliary beat frequency in single ovine airway epithelial cells. J. Physiol. 520, 851-865 (Pubitemid 29533041)
64. 2+ and ciliary beating. Am. J. Physiol. 272, L301-L310
65. Salathe, M., Ivonnet, P.I., Lieb, T. and Bookman, R.J. (2001) Agonist-stimulated calcium decreases in ovine ciliated airway epithelial cells: role of mitochondria. J. Physiol. 531, 13-26 (Pubitemid 32178023)
66. Sanderson, M.J. and Dirksen, E.R. (1986) Mechanosensitivity of cultured ciliated cells from the mammalian respiratory tract: implications for the regulation of mucociliary transport. Proc. Natl. Acad. Sci. U.S.A. 83, 7302-7306
67. Sanderson, M.J., Chow, I. and Dirksen, E.R. (1988) Intercellular communication between ciliated cells in culture. Am. J. Physiol. 254, C63-C74
68. Schmid, A., Bai, G., Schmid, N., Zaccolo, M., Ostrowski, L.E., Conner, G.E., Fregien, N. and Salathe, M. (2006) Real-time analysis of cAMP-mediated regulation of ciliary motility in single primary human airway epithelial cells. J. Cell. Sci. 119, 4176-4186
69. Seybold, Z.V., Mariassy, A.T., Stroh, D., Kim, C.S., Gazeroglu, H. and Wanner, A. (1990) Mucociliary interaction in vitro: effects of physiological and inflammatory stimuli. J. Appl. Physiol. 68, 1421-1426
70. Shah, A.S., Ben-Shahar, Y., Moninger, T.O., Kline, J.N. and Welsh, M.J. (2009) Motile cilia of human airway epithelia are chemosensory. Science 325, 1131-1134
71. Smith, E.F. (2002) Regulation of flagellar dynein by calcium and a role for an axonemal calmodulin and calmodulin-dependent kinase. Mol. Biol. Cell 13, 3303-3313
72. Spungin, B. and Silberberg, A. (1984) Stimulation of mucus secretion, ciliary activity, and transport in frog palate epithelium. Am. J. Physiol. 247, C299-C308
73. Stout, C.E., Costantin, J.L., Naus, C.C. and Charles, A.C. (2002) Intercellular calcium signaling in astrocytes via ATP release through connexin hemichannels. J. Biol. Chem. 277, 10482-10488
74. Stuehr, D.J., Santolini, J., Wang, Z.Q., Wei, C.C. and Adak, S. (2004) Update on mechanism and catalytic regulation in the NO synthases. J. Biol. Chem. 279, 36167-36170
75. Tamm, S.L., Sonneborn, T.M. and Dippell, R.V. (1975) The role of cortical orientation in the control of the direction of ciliary beat in Paramecium. J. Cell. Biol. 64, 98-112
76. Tapparel, C., Reymond, A., Girardet, C., Guillou, L., Lyle, R., Lamon, C., Hutter, P. and Antonarakis, S.E. (2003) The TPTE gene family: cellular expression, subcellular localization and alternative splicing. Gene 323, 189-199 (Pubitemid 37501099)
77. Tarran, R., Argent, B.E. and Gray, M.A. (2000) Regulation of a hyperpolarization-activated chloride current in murine respiratory ciliated cells. J. Physiol. 524, 353-364 (Pubitemid 30229502)
78. Tarran, R., Button, B., Picher, M., Paradiso, A.M., Ribeiro, C.M., Lazarowski, E.R., Zhang, L., Collins, P.L., Pickles, R.J., Fredberg, J.J. et al. (2005) Normal and cystic fibrosis airway surface liquid homeostasis. The effects of phasic shear stress and viral infections. J. Biol. Chem. 280, 35751-35759
79. i enhances ciliary activity in rabbit trachea. J. Physiol. 516, 179-190
80. Warren, N.J., Tawhai, M.H. and Crampin, E.J. (2010) Mathematical modelling of calcium wave propagation in mammalian airway epithelium: evidence for regenerative ATP release. Exp. Physiol. 95, 232-249
81. Wessler, I.K. and Kirkpatrick, C.J. (2001) The Non-neuronal cholinergic system: an emerging drug target in the airways. Pulm. Pharmacol. Ther. 14, 423-434
82. 2+, purinergic signaling, tonicity, and viscosity. Am. J. Physiol. Lung Cell Mol. Physiol. 292, L614-L624
83. Zagoory, O., Braiman, A., Gheber, L. and Priel, Z. (2001) Role of calcium and calmodulin in ciliary stimulation induced by acetylcholine. Am. J. Physiol. Cell Physiol. 280, C100-C109
84. Zagoory, O., Braiman, A. and Priel, Z. (2002) The mechanism of ciliary stimulation by acetylcholine: roles of calcium, PKA, and PKG. J. Gen. Physiol. 119, 329-339 (Pubitemid 34311171)
85. Zhang, L. and Sanderson, M.J. (2003) Oscillations in ciliary beat frequency and intracellular calcium concentration in rabbit tracheal epithelial cells induced by ATP. J. Physiol. 546, 733-749 (Pubitemid 36204509)