Involvement of Na+/Ca2+ exchanger in migration and contraction of rat cultured tendon fibroblasts

Journal of Physiology

Volumn 587, Issue 22, 2009, Pages 5345-5359

  Sakamoto, Kazuho ^a   Owada, Yuki ^a   Shikama, Yayoi ^a   Wada, Ikuo ^a   Waguri, Satoshi ^b   Iwamoto, Takahiro ^c   Kimura, Junko ^a  

^a Department of Pharmacology ^*  (Japan)

^b FUKUSHIMA MEDICAL UNIVERSITY   (Japan)

^c FUKUOKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

2 [2 [4 (4 NITROBENZYLOXY)PHENYL]ETHYL]ISOTHIOUREA METHANESULFONATE; 2 [4 (2,5 DIFLUOROBENZYLOXY)PHENOXY] 5 ETHOXYANILINE; CALCIUM ION; MESSENGER RNA; SODIUM CALCIUM EXCHANGE PROTEIN; SODIUM CALCIUM EXCHANGE PROTEIN 1.3; SODIUM CALCIUM EXCHANGE PROTEIN 1.7; SODIUM CALCIUM EXCHANGE PROTEIN 2; SODIUM CALCIUM EXCHANGE PROTEIN 3; UNCLASSIFIED DRUG; ISOPROTEIN; SMALL INTERFERING RNA; SODIUM CALCIUM EXCHANGE PROTEIN 1; SODIUM ION;

ACHILLES TENDON; ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL ISOLATION; CELL MEMBRANE; CELL MEMBRANE POTENTIAL; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; EXTRACELLULAR SPACE; FIBROBLAST; FLUOROMETRY; IMMUNOFLUORESCENCE MICROSCOPY; MUSCLE FIBER CONTRACTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SODIUM CELL LEVEL; WESTERN BLOTTING; ANALYTICAL PARAMETERS; CELL MIGRATION ASSAY; CELL MOTILITY; CELLULAR DISTRIBUTION; EXTRACELLULAR SODIUM; FIBROBLAST CULTURE; GENE EXPRESSION; GENE SILENCING; IMMUNOHISTOCHEMISTRY; MALE; MUSCLE FIBER MEMBRANE STEADY POTENTIAL; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SCRATCH ASSAY; SEQUENCE ANALYSIS; TENDON FIBROBLAST; WOUND HEALING;

ACHILLES TENDON; ANIMALS; CELL MOVEMENT; CELLS, CULTURED; FIBROBLASTS; MALE; MEMBRANE POTENTIALS; MUSCLE CONTRACTION; RATS; RATS, WISTAR; SODIUM-CALCIUM EXCHANGER; THIOUREA; WOUND HEALING;

EID: 70649108030     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2009.172080     Document Type: Article

References (55)

1. Araujo IM, Carreira BP, Pereira T, Santos PF, Soulet D, Inacio A, Bahr BA, Carvalho AP, Ambrosio AF, Carvalho CM. Changes in calcium dynamics following the reversal of the sodium-calcium exchanger have a key role in AMPA receptor-mediated neurodegeneration via calpain activation in hippocampal neurons. Cell Death Differ 2007, 14:1635-1646.
2. Bell E, Ivarsson B, Merrill C. Production of a tissue-like structure by contraction of collagen lattices by human fibroblasts of different proliferative potential in vitro. Proc Natl Acad Sci U S A 1979, 76:1274-1278.
3. Bhatt A, Kaverina I, Otey C, Huttenlocher A. Regulation of focal complex composition and disassembly by the calcium-dependent protease calpain. J Cell Sci 2002, 115:3415-3425.
4. Blaustein MP. Physiological effects of endogenous ouabain: control of intracellular Ca2+ stores and cell responsiveness. Am J Physiol Cell Physiol 1993, 264:C1367-1387.
5. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 1987, 162:156-159.
6. Condrescu M, Reeves JP. Actin-dependent regulation of the cardiac Na+/Ca2+ exchanger. Am J Physiol Cell Physiol 2006, 290:C691-701.
7. Dong H, Dunn J, Lytton J. Stoichiometry of the cardiac Na+/Ca2+ exchanger NCX1.1 measured in transfected HEK cells. Biophys J 2002, 82:1943-1952.
8. Dreval V, Dieterich P, Stock C, Schwab A. The role of Ca2+ transport across the plasma membrane for cell migration. Cell Physiol Biochem 2005, 16:119-126.
9. Elias CL, Xue XH, Marshall CR, Omelchenko A, Hryshko LV, Tibbits GF. Temperature dependence of cloned mammalian and salmonid cardiac Na+/Ca2+ exchanger isoforms. Am J Physiol Cell Physiol 2001, 281:C993-C1000.
10. Fu SC, Cheuk YC, Chan KM, Hung LK, Wong MW. Is cultured tendon fibroblast a good model to study tendon healing?. J Orthop Res 2008, 26:374-383.
11. Fujioka Y, Komeda M, Matsuoka S. Stoichiometry of Na+-Ca2+ exchange in inside-out patches excised from guinea-pig ventricular myocytes. J Physiol 2000, 523:339-351.
12. Gabbiani G, Majno G. Dupuytren's contracture: fibroblast contraction? An ultrastructural study. Am J Pathol 1972, 66:131-146.
13. Gough AH, Taylor DL. Fluorescence anisotropy imaging microscopy maps calmodulin binding during cellular contraction and locomotion. J Cell Biol 1993, 121:1095-1107.
14. Hahn K, DeBiasio R, Taylor DL. Patterns of elevated free calcium and calmodulin activation in living cells. Nature 1992, 359:736-738.
15. Hinata M, Yamamura H, Li L, Watanabe Y, Watano T, Imaizumi Y, Kimura J. Stoichiometry of Na+-Ca2+ exchange is 3:1 in guinea-pig ventricular myocytes. J Physiol 2002, 545:453-461.
16. Hinata M, Kimura J. Forefront of Na+/Ca2+ exchanger studies: stoichiometry of cardiac Na+/Ca2+ exchanger; 3:1 or 4:1?. J Pharmacol Sci 2004, 96:15-18.
17. Holzapfel G, Wehland J, Weber K. Calcium control of actin-myosin based contraction in triton models of mouse 3T3 fibroblasts is mediated by the myosin light chain kinase (MLCK)-calmodulin complex. Exp Cell Res 1983, 148:117-126.
18. Hove-Madsen L, Llach A, Tort L. Na+/Ca2+-exchange activity regulates contraction and SR Ca2+ content in rainbow trout atrial myocytes. Am J Physiol Regul Integr Comp Physiol 2000, 279:R1856-1864.
19. Ifuku M, Farber K, Okuno Y, Yamakawa Y, Miyamoto T, Nolte C, Merrino VF, Kita S, Iwamoto T, Komuro I, Wang B, Cheung G, Ishikawa E, Ooboshi H, Bader M, Wada K, Kettenmann H, Noda M. Bradykinin-induced microglial migration mediated by B1-bradykinin receptors depends on Ca2+ influx via reverse-mode activity of the Na+/Ca2+ exchanger. J Neurosci 2007, 27:13065-13073.
20. Iwamoto T, Watano T, Shigekawa M. A novel isothiourea derivative selectively inhibits the reverse mode of Na+/Ca2+ exchange in cells expressing NCX1. J Biol Chem 1996, 271:22391-22397.
21. Iwamoto T, Wakabayashi S, Imagawa T, Shigekawa M. Na+/Ca2+ exchanger overexpression impairs calcium signalling in fibroblasts: inhibition of the [Ca2+] increase at the cell periphery and retardation of cell adhesion. Eur J Cell Biol 1998, 76:228-236.
22. Iwamoto T, Kita S, Uehara A, Imanaga I, Matsuda T, Baba A, Katsuragi T. Molecular determinants of Na+/Ca2+ exchange (NCX1) inhibition by SEA0400. J Biol Chem 2004, 279:7544-7553.
23. Kimura J, Noma A, Irisawa H. Na-Ca exchange current in mammalian heart cells. Nature 1986, 319:596-597.
24. Kimura J, Miyamae S, Noma A. Identification of sodium-calcium exchange current in single ventricular cells of guinea-pig. J Physiol 1987, 384:199-222.
25. Kofuji P, Lederer WJ, Schulze DH. Mutually exclusive and cassette exons underlie alternatively spliced isoforms of the Na/Ca exchanger. J Biol Chem 1994, 269:5145-5149.
26. Kolin DL, Wiseman PW. Advances in image correlation spectroscopy: measuring number densities, aggregation states, and dynamics of fluorescently labelled macromolecules in cells. Cell Biochem Biophys 2007, 49:141-164.
27. Kraft R. The Na+/Ca2+ exchange inhibitor KB-R7943 potently blocks TRPC channels. Biochem Biophys Res Commun 2007, 361:230-236.
28. Larionov A, Krause A, Miller W. A standard curve based method for relative real time PCR data processing. BMC Bioinformatics 2005, 21:62.
29. Li JP, Kajiya H, Okabe K. Three Na+/Ca2+ exchanger (NCX) variants are expressed in mouse osteoclasts and mediate calcium transport during bone resorption. Endocrinology 2007, 148:2116-2125.
30. Liang CC, Park AY, Guan JL. In vitro scratch assay: a convenient and inexpensive method for analysis of cell migration in vitro. Nat Protoc 2007, 2:329-333.
31. Maeda S, Matsuoka I, Iwamoto T, Kurose H, Kimura J. Down-regulation of Na+/Ca2+ exchanger by fluvastatin in rat cardiomyoblast H9c2 cells: involvement of RhoB in Na+/Ca2+ exchanger mRNA stability. Mol Pharmacol 2005, 68:414-420.
32. Matsuda T, Arakawa N, Takuma K, Kishida Y, Kawasaki Y, Sakaue M, Takahashi K, Takahashi T, Suzuki T, Ota T, Hamano-Takahashi A, Onishi M, Tanaka Y, Kameo K, Baba A. SEA0400, a novel and selective inhibitor of the Na+-Ca2+ exchanger, attenuates reperfusion injury in the in vitro and in vivo cerebral ischemic models. J Pharmacol Exp Ther 2001, 298:249-256.
33. Moolenaar WH, Yarden Y, de Laat SW, Schlessinger J. Epidermal growth factor induces electrically silent Na+ influx in human fibroblasts. J Biol Chem 1982, 257:8502-8506.
34. Nakamura T, Arii S, Monden K, Furutani M, Takeda Y, Imamura M, Tominaga M, Okada Y. Expression of the Na+/Ca2+ exchanger emerges in hepatic stellate cells after activation in association with liver fibrosis. Proc Natl Acad Sci U S A 1998, 95:5389-5394.
35. Newport ML, Tucker RL. New perspectives on extensor tendon repair and implications for rehabilitation. J Hand Ther 2005, 18:175-181.
36. Philipson KD, Longoni S, Ward R. Purification of the cardiac Na+-Ca2+ exchange protein. Biochim Biophys Acta 1988, 45:298-306.
37. Pellegrin S, Mellor H. Actin stress fibres. J Cell Sci 2007, 120:3491-3499.
38. Poburko D, Liao CH, Lemos VS, Lin E, Maruyama Y, Cole WC, van Breemen C. Transient receptor potential channel 6-mediated, localized cytosolic [Na+] transients drive Na+/Ca2+ exchanger-mediated Ca2+ entry in purinergically stimulated aorta smooth muscle cells. Circ Res 2007, 101:1030-1038.
39. Pollard TD, Borisy GG. Cellular motility driven by assembly and disassembly of actin filaments. Cell 2003, 112:453-465.
40. Quednau BD, Nicoll DA, Philipson KD. Tissue specificity and alternative splicing of the Na+/Ca2+ exchanger isoforms NCX1, NCX2, and NCX3 in rat. Am J Physiol Cell Physiol 1997, 272:C1250-1261.
41. Quednau BD, Nicoll DA, Philipson KD. The sodium/calcium exchanger family-SLC8. Pflugers Arch 2004, 447:543-548.
42. Raizman JE, Komljenovic J, Chang R, Deng C, Bedosky KM, Rattan SG, Cunnington RH, Freed DH, Dixon IM. The participation of the Na+-Ca2+ exchanger in primary cardiac myofibroblast migration, contraction, and proliferation. J Cell Physiol 2007, 213:540-551.
43. Reuter H, Henderson SA, Han T, Matsuda T, Baba A, Ross RS, Goldhaber JI, Philipson KD. Knockout mice for pharmacological screening: testing the specificity of Na+-Ca2+ exchange inhibitors. Circ Res 2002, 91:90-92.
44. Romero JR, Rivera A, Lanca V, Bicho MD, Conlin PR, Ricupero DA. Na+/Ca2+ exchanger activity modulates connective tissue growth factor mRNA expression in transforming growth factor β1- and Des-Arg10-kallidin-stimulated myofibroblasts. J Biol Chem 2005, 280:14378-14384.
45. Tanaka H, Nishimaru K, Aikawa T, Hirayama W, Tanaka Y, Shigenobu K. Effect of SEA0400, a novel inhibitor of sodium-calcium exchanger, on myocardial ionic currents. Br J Pharmacol 2002, 135:1096-1100.
46. Van Eylen F, Kamagate A, Herchuelz A. A new Na/Ca exchanger splicing pattern identified in situ leads to a functionally active 70kDa NH2-terminal protein. Cell Calcium 2001, 30:191-198.
47. Wahl M, Gruenstein E. Intracellular free Ca2+ in the cell cycle in human fibroblasts: transitions between G1 and G0 and progression into S phase. Mol Biol Cell 1993, 4:293-302.
48. Wall ME, Banes AJ. Early responses to mechanical load in tendon: role for calcium signalling, gap junctions and intercellular communication. J Musculoskelet Neuronal Interact 2005, 5:70-84.
49. Watano T, Kimura J, Morita T, Nakanishi H. A novel antagonist, No. 7943, of the Na+/Ca2+ exchange current in guinea-pig cardiac ventricular cells. Br J Pharmacol 1996, 119:555-563.
50. Wei C, Wang X, Chen M, Ouyang K, Song LS, Cheng H. Calcium flickers steer cell migration. Nature 2009, 457:901-905.
51. Weiler A, Unterhauser FN, Bail HJ, Huning M, Haas NP. α-Smooth muscle actin is expressed by fibroblastic cells of the ovine anterior cruciate ligament and its free tendon graft during remodelling. J Orthop Res 2002, 20:310-317.
52. Yokoyama U, Minamisawa S, Quan H, Ghatak S, Akaike T, Segi-Nishida E, Iwasaki S, Iwamoto M, Misra S, Tamura K, Hori H, Yokota S, Toole BP, Sugimoto Y, Ishikawa Y. Chronic activation of the prostaglandin receptor EP4 promotes hyaluronan-mediated neointimal formation in the ductus arteriosus. J Clin Invest 2006, 116:3026-3034.
53. Zhang S, Yuan JX, Barrett KE, Dong H. Role of Na+/Ca2+ exchange in regulating cytosolic Ca2+ in cultured human pulmonary artery smooth muscle cells. Am J Physiol Cell Physiol 2005, 288:C245-C252.
54. Zhang S, Dong H, Rubin LJ, Yuan JX. Upregulation of Na+/Ca2+ exchanger contributes to the enhanced Ca2+ entry in pulmonary artery smooth muscle cells from patients with idiopathic pulmonary arterial hypertension. Am J Physiol Cell Physiol 2007, 292:C2297-C2305.
55. Zhao S, Fernald RD. Comprehensive algorithm for quantitative real-time polymerase chain reaction. J Comput Biol 2005, 12:1047-1064.