Inflammation alters regional mitochondrial Ca2+ in human airway smooth muscle cells

American Journal of Physiology - Cell Physiology

Volumn 303, Issue 3, 2012, Pages

  Delmotte, Philippe ^a   Yang, Binxia ^a   Thompson, Michael A ^a   Pabelick, Christina M ^a   Prakash, Y S ^a   Sieck, Gary C ^a  

^a MAYO CLINIC   (United States)

Author keywords

Bronchial smooth muscle; Calcium regulation; Inflammation; Lung; Mitochondrial calcium uniporter; Mitochondrial sodium calcium exchange; Sarcoplasmic reticulum

Indexed keywords

7 CHLORO 5 (2 CHLOROPHENYL) 1,5 DIHYDRO 4,1 BENZOTHIAZEPIN 2(3H) ONE; HISTAMINE; INTERLEUKIN 13; MITOCHONDRIAL CALCIUM UNIPORTER; MITOCHONDRIAL PROTEIN; SODIUM CALCIUM EXCHANGE PROTEIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ARTICLE; BRONCHUS MUSCLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; HUMAN TISSUE; INFLAMMATION; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; PRIORITY JOURNAL;

ANILINE COMPOUNDS; BRONCHI; CALCIUM; CALCIUM SIGNALING; CELLS, CULTURED; CLONAZEPAM; HETEROCYCLIC COMPOUNDS, 3-RING; HISTAMINE; HUMANS; INFLAMMATION; INTERLEUKIN-13; MICROSCOPY, FLUORESCENCE; MITOCHONDRIA; MYOCYTES, SMOOTH MUSCLE; RUTHENIUM COMPOUNDS; SODIUM-CALCIUM EXCHANGER; THIAZEPINES; TUMOR NECROSIS FACTOR-ALPHA; XANTHENES;

VASCONCELLEA CANDICANS;

EID: 84864518544     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00414.2011     Document Type: Article

References (84)

1. Aguilera-Aguirre L, Bacsi A, Saavedra-Molina A, Kurosky A, Sur S, Boldogh I. Mitochondrial dysfunction increases allergic airway inflammation. J Immunol 183: 5379-5387, 2009.
2. Amrani Y. TNF-alpha and calcium signaling in airway smooth muscle cells: a never-ending story with promising therapeutic relevance. Am J Respir Cell Mol Biol 36: 387-388, 2007.
3. Amrani Y, Chen H, Panettieri RA Jr. Activation of tumor necrosis factor receptor 1 in airway smooth muscle: a potential pathway that modulates bronchial hyper-responsiveness in asthma? Respir Res 1: 49-53, 2000.
4. Amrani Y, Panettieri RA Jr. Modulation of calcium homeostasis as a mechanism for altering smooth muscle responsiveness in asthma. Curr Opin Allergy Clin Immunol 2: 39-45, 2002.
5. 2+ entry in porcine airway smooth muscle. Am J Physiol Lung Cell Mol Physiol 286: L909-L917, 2004.
6. Balemba OB, Bartoo AC, Nelson MT, Mawe GM. Role of mitochondria in spontaneous rhythmic activity and intracellular calcium waves in the guinea pig gallbladder smooth muscle. Am J Physiol Gastrointest Liver Physiol 294: G467-G476, 2008.
7. Baughman JM, Perocchi F, Girgis HS, Plovanich M, Belcher-Timme CA, Sancak Y, Bao XR, Strittmatter L, Goldberger O, Bogorad RL, Koteliansky V, Mootha VK. Integrative genomics identifies MCU as an essential component of the mitochondrial calcium uniporter. Nature 476: 341-345, 2011.
8. Bernardi P. Mitochondrial transport of cations: channels, exchangers, and permeability transition. Physiol Rev 79: 1127-1155, 1999.
9. i signaling dynamics and metabolism by perinuclear mitochondria in mouse parotid acinar cells. J Biol Chem 279: 12909-12917, 2004.
10. Carafoli E. The fateful encounter of mitochondria with calcium: how did it happen? Biochim Biophys Acta 1797: 595-606, 2010.
11. Chalmers S, McCarron JG. Inhibition of mitochondrial calcium uptake rather than efflux impedes calcium release by inositol-1,4,5-trisphosphatesensitive receptors. Cell Calcium 46: 107-113, 2009.
12. 2+ oscillations in smooth muscle. J Cell Sci 121: 75-85, 2008.
13. 2. Am J Physiol Lung Cell Mol Physiol 298: L178-L188, 2010.
14. Ca currents in smooth muscle cells of rat cerebral arteries. J Physiol 556: 755-771, 2004.
15. 2+ release is inhibited by mitochondrial depolarization. Biochem J 347: 593-600, 2000.
16. 2+ exchange. Trends Pharmacol Sci 14: 408-413, 1993.
17. 2+ exchanger in the regulation of oxidative phosphorylation in isolated heart mitochondria. J Biol Chem 268: 938-947, 1993.
18. Csordas G, Varnai P, Golenar T, Sheu SS, Hajnoczky G. Calcium transport across the inner mitochondrial membrane: molecular mechanisms and pharmacology. Mol Cell Endocrinol 353: 109-113, 2012.
19. 2+ and ROS take center stage to orchestrate TNF-alpha-mediated inflammatory responses. J Clin Invest 121: 1683-1685, 2011.
20. Dai J, Kuo KH, Leo JM, van Breemen C, Lee CH. Rearrangement of the close contact between the mitochondria and the sarcoplasmic reticulum in airway smooth muscle. Cell Calcium 37: 333-340, 2005.
21. De Stefani D, Raffaello A, Teardo E, Szabo I, Rizzuto R. A fortykilodalton protein of the inner membrane is the mitochondrial calcium uniporter. Nature 476: 336-340, 2011.
22. Drago I, Pizzo P, Pozzan T. After half a century mitochondrial calcium in-and efflux machineries reveal themselves. EMBO J 30: 4119-4125, 2011.
23. Duchen MR. Mitochondria and calcium: from cell signalling to cell death. J Physiol 529: 57-68, 2000.
24. Duszynski J, Koziel R, Brutkowski W, Szczepanowska J, Zablocki K. The regulatory role of mitochondria in capacitative calcium entry. Biochim Biophys Acta 1757: 380-387, 2006.
25. Franzini-Armstrong C. ER-mitochondria communication. How privileged? Physiology (Bethesda) 22: 261-268, 2007.
26. 2+ entry in airway smooth muscle cells. Pulm Pharmacol Ther 23: 182-189, 2010.
27. 2+ channels. Mol Cell 38: 280-290, 2010.
28. Girodet PO, Ozier A, Bara I, Tunon de Lara JM, Marthan R, Berger P. Airway remodeling in asthma: new mechanisms and potential for pharmacological intervention. Pharmacol Ther 130: 325-337, 2011.
29. 2+ uptake. EMBO J 21: 6744-6754, 2002.
30. Gunter TE, Buntinas L, Sparagna G, Eliseev R, Gunter K. Mitochondrial calcium transport: mechanisms and functions. Cell Calcium 28: 285-296, 2000.
31. Gunter TE, Gunter KK. Uptake of calcium by mitochondria: transport and possible function. IUBMB Life 52: 197-204, 2001.
32. Gunter TE, Yule DI, Gunter KK, Eliseev RA, Salter JD. Calcium and mitochondria. FEBS Lett 567: 96-102, 2004.
33. Hajnoczky G, Saotome M, Csordas G, Weaver D, Yi M. Calcium signalling and mitochondrial motility. Novartis Found Symp 287: 105-117; discussion 117-121, 2007.
34. 2+ oscillations. Cell Calcium 40: 53-61, 2006.
35. Hoth M, Button DC, Lewis RS. Mitochondrial control of calciumchannel gating: a mechanism for sustained signaling and transcriptional activation in T lymphocytes. Proc Natl Acad Sci USA 97: 10607-10612, 2000.
36. 2+ oscillations. EMBO Rep 7: 390-396, 2006.
37. 2+ entries in rat brown adipocytes. Am J Physiol Cell Physiol 292: C896-C908, 2007.
38. Maack C, O'Rourke B. Excitation-contraction coupling and mitochondrial energetics. Basic Res Cardiol 102: 369-392, 2007.
39. Mabalirajan U, Dinda AK, Kumar S, Roshan R, Gupta P, Sharma SK, Ghosh B. Mitochondrial structural changes and dysfunction are associated with experimental allergic asthma. J Immunol 181: 3540-3548, 2008.
40. 2+ store refilling. J Biol Chem 278: 44769-44779, 2003.
41. 2+ refilling of the endoplasmic reticulum. J Biol Chem 280: 12114-12122, 2005.
42. Marin J, Encabo A, Briones A, Garcia-Cohen EC, Alonso MJ. Mechanisms involved in the cellular calcium homeostasis in vascular smooth muscle: calcium pumps. Life Sci 64: 279-303, 1999.
43. 2+ uptake into mitochondria in vitro and in situ in single cardiac myocytes. J Biol Chem 273: 10223-10231, 1998.
44. 2+ transients that modulate secretion. Nat Cell Biol 2: 57-61, 2000.
45. 2+-dependent inactivation of calcium release-activated calcium/orai channels normally prevented by mitochondria. J Biol Chem 286: 16186-16196, 2011.
46. 2+ entry. J Cell Sci 123: 2553-2564, 2010.
47. 2+ exchange. Proc Natl Acad Sci USA 107: 436-441, 2010.
48. 2+ buffers. News Physiol Sci 18: 252-256, 2003.
49. 2+ entry: dynamic interplay between endoplasmic reticulum, mitochondria and plasma membrane. J Physiol 547: 333-348, 2003.
50. Parekh AB, Putney JW Jr. Store-operated calcium channels. Physiol Rev 85: 757-810, 2005.
51. Parthasarathi K, Ichimura H, Quadri S, Issekutz A, Bhattacharya J. Mitochondrial reactive oxygen species regulate spatial profile of proinflammatory responses in lung venular capillaries. J Immunol 169: 7078-7086, 2002.
52. 2+ uptake. Nature 467: 291-296, 2010.
53. Petersen OH, Petersen CC, Kasai H. Calcium and hormone action. Annu Rev Physiol 56: 297-319, 1994.
54. 2+ already in the submicromolar range: correlation with redox state. Cell Calcium 31: 97-104, 2002.
55. Poburko D, Santo-Domingo J, Demaurex N. Dynamic regulation of the mitochondrial proton gradient during cytosolic calcium elevations. J Biol Chem 286: 11672-11684, 2011.
56. Pozzan T, Rizzuto R. The renaissance of mitochondrial calcium transport. Eur J Biochem 267: 5269-5273, 2000.
57. Pozzan T, Rizzuto R, Volpe P, Meldolesi J. Molecular and cellular physiology of intracellular calcium stores. Physiol Rev 74: 595-636, 1994.
58. 2+ and force in airway smooth muscle. Am J Physiol Lung Cell Mol Physiol 291: L447-L456, 2006.
59. Prakash YS, Kannan MS, Sieck GC. Regulation of intracellular calcium oscillations in porcine tracheal smooth muscle cells. Am J Physiol Cell Physiol 272: C966-C975, 1997.
60. Reddy PH. Mitochondrial dysfunction and oxidative stress in asthma: implications for mitochondria-targeted antioxidant therapeutics. Pharmaceuticals (Basel) 4: 429-456, 2011.
61. Risse PA, Jo T, Suarez F, Hirota N, Tolloczko B, Ferraro P, Grutter P, Martin JG. Interleukin-13 inhibits proliferation and enhances contractility of human airway smooth muscle cells without change in contractile phenotype. Am J Physiol Lung Cell Mol Physiol 300: L958-L966, 2011.
62. Rizzuto R, Bernardi P, Pozzan T. Mitochondria as all-round players of the calcium game. J Physiol 529: 37-47, 2000.
63. 2+ transfer from the ER to mitochondria: when, how and why. Biochim Biophys Acta 1787: 1342-1351, 2009.
64. 2+: molecular determinants and functional consequences. Physiol Rev 86: 369-408, 2006.
65. Romagnoli A, Aguiari P, De Stefani D, Leo S, Marchi S, Rimessi A, Zecchini E, Pinton P, Rizzuto R. Endoplasmic reticulum/mitochondria calcium cross-talk. Novartis Found Symp 287: 122-131, 2007.
66. 2+ removal in airway myocytes. Biophys J 86: 2583-2595, 2004.
67. Roux E, Noble PJ, Noble D, Marhl M. Modelling of calcium handling in airway myocytes. Prog Biophys Mol Biol 90: 64-87, 2006.
68. 2+ determines the severity of inflammation in mouse lung microvessels. J Clin Invest 121: 1986-1999, 2011.
69. Ruiz-Meana M, Fernandez-Sanz C, Garcia-Dorado D. The SR-mitochondria interaction: a new player in cardiac pathophysiology. Cardiovasc Res 88: 30-39, 2010.
70. Ryu SY, Beutner G, Kinnally K, Dirksen RT, Sheu SS. Single channel characterization of the mitochondrial ryanodine receptor in heart mitoplasts. J Biol Chem 286: 21324-21329, 2011.
71. Sakai Y, Kwan CY. Calcium regulation and contractile dysfunction of smooth muscle. Biol Signals 2: 305-312, 1993.
72. Sathish V, Delmotte PF, Thompson MA, Pabelick CM, Sieck GC, Prakash YS. Sodium-calcium exchange in intracellular calcium handling of human airway smooth muscle. PLoS One 6: e23662, 2011.
73. 2+ reuptake in porcine airway smooth muscle. Am J Physiol Lung Cell Mol Physiol 294: L787-L796, 2008.
74. 2+ reuptake in human airway smooth muscle. Am J Physiol Lung Cell Mol Physiol 297: L26-L34, 2009.
75. 2+ entry by CD38 in human airway smooth muscle. Am J Physiol Lung Cell Mol Physiol 294: L378-L385, 2008.
76. Slater EC, Cleland KW. The effect of calcium on the respiratory and phosphorylative activities of heart-muscle sarcosomes. Biochem J 55: 566-590, 1953.
77. Tirumurugaan KG, Jude JA, Kang BN, Panettieri RA, Walseth TF, Kannan MS. TNF-α induced CD38 expression in human airway smooth muscle cells: role of MAP kinases and transcription factors NF-B and AP-1. Am J Physiol Lung Cell Mol Physiol 292: L1385-L1395, 2007.
78. 2+ regulation in human airway smooth muscle. Am J Physiol Lung Cell Mol Physiol 298: L521-L530, 2010.
79. Trian T, Benard G, Begueret H, Rossignol R, Girodet PO, Ghosh D, Ousova O, Vernejoux JM, Marthan R, Tunon-de-Lara JM, Berger P. Bronchial smooth muscle remodeling involves calcium-dependent enhanced mitochondrial biogenesis in asthma. J Exp Med 204: 3173-3181, 2007.
80. 2+ with quin2. Methods Enzymol 172: 230-262, 1989.
81. 2+ entry in HeLa cells. Cell Calcium 36: 499-508, 2004.
82. Vasington FD, Murphy JV. Ca ion uptake by rat kidney mitochondria and its dependence on respiration and phosphorylation. J Biol Chem 237: 2670-2677, 1962.
83. 2+ uptake in canine colonic muscles. J Physiol 549: 207-218, 2003.
84. White TA, Xue A, Chini EN, Thompson M, Sieck GC, Wylam ME. Role of transient receptor potential C3 in TNF-alpha-enhanced calcium influx in human airway myocytes. Am J Respir Cell Mol Biol 35: 243-251, 2006.