Mathematical modelling of calcium wave propagation in mammalian airway epithelium: Evidence for regenerative ATP release

Experimental Physiology

Volumn 95, Issue 1, 2010, Pages 232-249

  Warren, N J ^a   Tawhai, M H ^a   Crampin, E J ^a,b  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE (CALCIUM); ADENOSINE TRIPHOSPHATE; CALCIUM ION; INOSITOL 1,4,5 TRISPHOSPHATE;

ARTICLE; BIOLOGICAL MODEL; CALCIUM TRANSPORT; CELL CULTURE; CELL MEMBRANE; CELL STIMULATION; DIFFUSION; ENDOPLASMIC RETICULUM; EPITHELIUM CELL; GAP JUNCTION; MATHEMATICAL MODEL; MECHANICAL STIMULATION; NONHUMAN; PARACRINE SIGNALING; PHOTOLYSIS; REGENERATION; RESPIRATORY EPITHELIUM;

EID: 74049104868     PISSN: 09580670     EISSN: 1469445X     Source Type: Journal    
DOI: 10.1113/expphysiol.2009.049585     Document Type: Article

References (59)

1. Allbritton N, Meyer T Stryer L (1992). Range of messenger action of calcium ion and inositol 1,4,5-trisphosphate. Science 258, 1812 1815.
2. Bennett MR, Farnell L Gibson WG (2005). A quantitative model of purinergic junctional transmission of calcium waves in astrocyte networks. Biophys J 89, 2235 2250.
3. Boitano S, Dirksen E Sanderson M (1992). Intercellular propagation of calcium waves mediated by inositol trisphosphate. Science 258, 292 295.
4. 2+ signaling through gap junctions in airway cells. Am J Physiol Lung Cell Mol Physiol 279, L623 L630.
5. 2+-conducting ion channels in mechanically-induced signal transduction of airway epithelial cells. J Cell Sci 107, 3037 3044.
6. Boudreault F Grygorczyk R (2004). Cell swelling-induced ATP release is tightly dependent on intracellular calcium elevations. J Physiol 561, 499- 513.
7. Braet K, Aspeslagh S, Vandamme W, Willecke K, Martin PEM, Evans WH Leybaert L (2003). Pharmacological sensitivity of ATP release triggered by photoliberation of inositol-1,4,5-trisphosphate and zero extracellular calcium in brain endothelial cells. J Cell Physiol 197, 205 213.
8. Braet K, Vandamme W, Martin PEM, Evans WH Leybaert L (2003). Photoliberating inositol-1,4,5-trisphosphate triggers ATP release that is blocked by the connexin mimetic peptide gap 26. Cell Calcium 33, 37 48.
9. Brenner S Scott L (1994). The Mathematical Theory of Finite Element Methods, Texts in Applied Mathematics, 1st edn. Springer-Verlag, New York.
10. Charles A, Naus C, Zhu D, Kidder G, Dirksen E Sanderson M (1992). Intercellular calcium signaling via gap junctions in glioma cells. J Cell Biol 118, 195 201.
11. Coco S, Calegari F, Pravettoni E, Pozzi D, Taverna E, Rosa P, Matteoli M Verderio C (2003). Storage and release of ATP from astrocytes in culture. J Biol Chem 278, 1354 1362.
12. De Vuyst E, Decrock E, Cabooter L, Dubyak GR, Naus CG, Evans WH Leybaert L (2006). Intracellular calcium changes trigger connexin 32 hemichannel opening. EMBO J 25, 34 44.
13. Evans JH Sanderson MJ (1999). Intracellular calcium oscillations induced by ATP in airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 277, L30 L41.
14. Gin E, Crampin EJ, Brown DA, Shuttleworth TJ, Yule DI Sneyd J (2007). A mathematical model of fluid secretion from a parotid acinar cell. J Theor Biol 248, 64 80.
15. Gomes P, Srinivas SP, Van Driessche W, Vereecke J Himpens B (2005). ATP release through connexin hemichannels in corneal endothelial cells. Invest Ophthalmol Visual Sci 46, 1208 1218.
16. Hansen M, Boitano S, Dirksen E Sanderson M (1993). Intercellular calcium signaling induced by extracellular adenosine 5′-triphosphate and mechanical stimulation in airway epithelial cells. J Cell Sci 106, 995 1004.
17. Hansen M, Boitano S, Dirksen E Sanderson M (1995). A role for phospholipase C activity but not ryanodine receptors in the initiation and propagation of intercellular calcium waves. J Cell Sci 108, 2583 2590.
18. Hayashi T, Kawakami M, Sasaki S, Katsumata T, Mori H, Yoshida H Nakahari T (2005). ATP regulation of ciliary beat frequency in rat tracheal and distal airway epithelium. Exp Physiol 90, 535 544.
19. Hofer T, Venance L Giaume C (2002). Control and plasticity of intercellular calcium waves in astrocytes: a modeling approach. J Neurosci 22, 4850 4859.
20. Homolya L, Steinberg TH Boucher RC (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.
21. 2+ oscillations. Biophys J 71, 3477 3487.
22. Ko K, Jo M, McCracken K Kim K (1997). ATP-induced mucin release from cultured airway goblet cells involves, in part, activation of protein kinase C. Am J Respir Cell Mol Biol 16, 194 198.
23. Kojic N, Kojic M Tschumperlin DJ (2006). Computational modeling of extracellular mechanotransduction. Biophys J 90, 4261 4270.
24. Kreda SM, Okada SF, van Heusden CA, O'Neal W, Gabriel S, Abdullah L, Davis CW, Boucher RC Lazarowski ER (2007). Coordinated release of nucleotides and mucin from human airway epithelial Calu-3 cells. J Physiol 584, 245 259.
25. 2+. Biophys J 77, 629 638.
26. Lazarowski ER, Boucher RC Harden TK (2003). Mechanisms of release of nucleotides and integration of their action as P2X- and P2Y-receptor activating molecules. Mol Pharmacol 64, 785 795.
27. LeBeau AP, Yule DI, Groblewski GE Sneyd J (1999). Agonist-dependent phosphorylation of the inositol 1,4,5-trisphosphate receptor: a possible mechanism for agonist-specific calcium oscillations in pancreatic acinar cells. J Gen Physiol 113, 851 872.
28. 2 receptors in smooth muscle cells. Biophys J 88, 1507 1523.
29. Lemon G, Gibson WG Bennett MR (2003a). Metabotropic receptor activation, desensitization and sequestration - I: modelling calcium and inositol 1,4,5-trisphosphate dynamics following receptor activation. J Theor Biol 223, 93 111. (Pubitemid 36627548)
30. Lemon G, Gibson WG Bennett MR (2003b). Metabotropic receptor activation, desensitization and sequestration - II: modelling the dynamics of the pleckstrin homology domain. J Theor Biol 223, 113 129. (Pubitemid 36627549)
31. Leybaert L, Paemeleire K, Strahonja A Sanderson MJ (1998). Inositoltriphosphate-dependent intercellular calcium signaling in and between astrocytes and endothelial cells. Glia 24, 398 407.
32. Li H, Liu TF, Lazrak A, Peracchia C, Goldberg GS, Lampe PD Johnson RG (1996). Properties and regulation of gap junctional hemichannels in the plasma membranes of cultured cells. J Cell Biol 134, 1019 1030.
33. Liu J Ewing R (2005). An operator splitting method for nonlinear reactive transport equations and its implementation based on dll and com. Current Trends in High Performance Computing and Its Applications 6, 93 102.
34. Mercer RR, Russell ML, Roggli VL Crapo JD (1994). Cell number and distribution in human and rat airways. Am J Respir Cell Mol Biol 10, 613 624.
35. 2+ in the presence of calmodulin. Biochem J 248, 489 493.
36. Nakahari T (2007). Regulation of ciliary beat frequency in airways: shear stress, ATP action, and its modulation. Am J Physiol Lung Cell Mol Physiol 292, L612 L613.
37. Okada SF, Nicholas RA, Kreda SM, Lazarowski ER Boucher RC (2006). Physiological regulation of ATP release at the apical surface of human airway epithelia. J Biol Chem 281, 22992 23002.
38. Paemeleire K, Martin PEM, Coleman SL, Fogarty KE, Carrington WA, Leybaert L, Tuft RA, Evans WH Sanderson MJ (2000). Intercellular calcium waves in HeLa cells expressing GFP-labeled connexin 43, 32, or 26. Mol Biol Cell 11, 1815 1827.
39. Pearson RA, Dale N, Llaudet E Mobbs P (2005). ATP released via gap junction hemichannels from the pigment epithelium regulates neural retinal progenitor proliferation. Neuron 46, 731 744.
40. Peracchia C (2004). Chemical gating of gap junction channels: roles of calcium, pH and calmodulin. Biochim Biophys Acta 1662, 61 80.
41. Reed W Satir P (1986). Spreading ciliary arrest in a mussel gill epithelium: characterization by quick fixation. J Cell Physiol 126, 191 205.
42. 2+ in epithelial cells. Cell Regul 1, 585 596.
43. Sanderson MJ, Chow I Dirksen ER (1988). Intercellular communication between ciliated cells in culture. Am J Physiol Cell Physiol 254, C63 C74.
44. Sanderson MJ Sleigh MA (1981). Ciliary activity of cultured rabbit tracheal epithelium: beat pattern and metachrony. J Cell Sci 47, 331 347.
45. Sneyd J, Charles AC Sanderson MJ (1994). A model for the propagation of intercellular calcium waves. Am J Physiol Cell Physiol 266, C293 C302.
46. Sneyd J, Falcke M, Dufour JF Fox C (2004). A comparison of three models of the inositol trisphosphate receptor. Progr Biophys Mol Biol 85, 121 140.
47. Sneyd J, Tsaneva-Atanasova K, Bruce JIE, Straub SV, Giovannucci DR Yule DI (2003). A model of calcium waves in pancreatic and parotid acinar cells. Biophys J 85, 1392 1405.
48. Sneyd J, Wetton BT, Charles AC Sanderson MJ (1995). Intercellular calcium waves mediated by diffusion of inositol trisphosphate: a two-dimensional model. Am J Physiol Cell Physiol 268, C1537 C1545.
49. 2 receptor. Mol Pharmacol 54, 485 494.
50. Tarran R (2004). Regulation of airway surface liquid volume and mucus transport by active ion transport. Proc Am Thorac Soc 1, 42 46.
51. Tarran R, Trout L, Donaldson SH Boucher RC (2006). Soluble mediators, not cilia, determine airway surface liquid volume in normal and cystic fibrosis superficial airway epithelia. J Gen Physiol 127, 591 604.
52. 2+-dependent ATP release from a549 cells involves synergistic autocrine stimulation by coreleased uridine nucleotides. J Physiol 584, 419 435.
53. Tschumperlin DJ, Dai G, Maly IV, Kikuchi T, Laiho LH, McVittie AK, Haley KJ, Lilly CM, So PT, Lauffenburger DA, Kamm RD Drazen JM (2004). Mechanotransduction through growth-factor shedding into the extracellular space. Nature 429, 83 86.
54. Warren NJ, Tawhai MH Crampin EJ (2009). A mathematical model of calcium-induced fluid secretion in airway epithelium. J Theor Biol 259, 837 849.
55. - pathways in cultured human airway epithelium. Am J Physiol Cell Physiol 256, C1033 C1044.
56. 2+ oscillations in airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 276, L669 L678.
57. Zhang L Sanderson MJ (2003). Oscillations in ciliary beat frequency and intracellular calcium concentration in rabbit tracheal epithelial cells induced by ATP. J Physiol 546, 733 749.
58. Zimmermann H, Braun N, Kegel B Heine P (1998). New insights into molecular structure and function of ectonucleotidases in the nervous system. Neurochem Int 32, 421 425.
59. Zuo P, Picher M, Okada SF, Lazarowski ER, Button B, Boucher RC Elston TC (2008). Mathematical model of nucleotide regulation on airway epithelia. Implications for airway homeostasis. J Biol Chem 283, 26805 26819.