Simulated microgravity inhibits L-type calcium channel currents partially by the up-regulation of miR-103 in MC3T3-E1 osteoblasts

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Sun, Zhongyang ^a   Cao, Xinsheng ^a   Zhang, Zhuo ^b   Hu, Zebing ^a   Zhang, Lianchang ^a   Wang, Han ^a   Zhou, Hua ^a   Li, Dongtao ^c   Zhang, Shu ^a   Xie, Manjiang ^a  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^c NAVY GENERAL HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

1,4 DIHYDRO 2,6 DIMETHYL 5 NITRO 4 [2 (TRIFLUOROMETHYL)PHENYL] 3 PYRIDINECARBOXYLIC ACID METHYL ESTER; CACNA1C PROTEIN, MOUSE; CALCIUM; CALCIUM CHANNEL BLOCKING AGENT; CALCIUM CHANNEL L TYPE; MICRORNA; MIRN103 MICRORNA, MOUSE; NIFEDIPINE; SMALL INTERFERING RNA;

ANIMAL; CELL LINE; CHEMISTRY; CYTOLOGY; DOWN REGULATION; DRUG EFFECTS; FLUORESCENCE MICROSCOPY; GENETICS; IMMUNOHISTOCHEMISTRY; METABOLISM; MOUSE; OSTEOBLAST; RNA INTERFERENCE; UPREGULATION; WEIGHTLESSNESS;

3-PYRIDINECARBOXYLIC ACID, 1,4-DIHYDRO-2,6-DIMETHYL-5-NITRO-4-(2-(TRIFLUOROMETHYL)PHENYL)-, METHYL ESTER; ANIMALS; CALCIUM; CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS, L-TYPE; CELL LINE; DOWN-REGULATION; IMMUNOHISTOCHEMISTRY; MICE; MICRORNAS; MICROSCOPY, FLUORESCENCE; NIFEDIPINE; OSTEOBLASTS; RNA INTERFERENCE; RNA, SMALL INTERFERING; UP-REGULATION; WEIGHTLESSNESS;

EID: 84951264358     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep08077     Document Type: Article

References (62)

1. Duncan, R. L. & Turner, C. H. Mechanotransduction and the functional response of bone to mechanical strain. Calcif Tissue Int 57, 344-358 (1995).
2. Nishizuka, Y. Intracellular signaling by hydrolysis of phospholipids and activation of protein kinase C. Science 258, 607-614 (1992).
3. Riggs, B. L., Khosla, S. & Melton, L. R. A unitary model for involutional osteoporosis: estrogen deficiency causes both type I and type II osteoporosis in postmenopausal women and contributes to bone loss in aging men. J BoneMiner Res 13, 763-773 (1998).
4. Yagodovsky, V. S., Triftanidi, L. A. & Gorokhova, G. P. Space flight effects on skeletal bones of rats (light and electron microscopic examination). Aviat Space Environ Med 47, 734-738 (1976).
5. Morey, E. R. & Baylink, D. J. Inhibition of bone formation during space flight. Science 201, 1138-1141 (1978).
6. Jee, W. S., Wronski, T. J., Morey, E. R. & Kimmel, D. B. Effects of spaceflight on trabecular bone in rats. Am J Physiol 244, R310-R314 (1983).
7. Wronski, T. J. & Morey, E. R. Effect of spaceflight on periosteal bone formation in rats. Am J Physiol 244, R305-R309 (1983).
8. Zerath, E. et al. Effects of spaceflight on bone mineralization in the rhesus monkey. J Appl Physiol (1985) 81, 194-200 (1996).
9. Patterson-Buckendahl, P. et al. Fragility and composition of growing rat bone after one week in spaceflight. Am J Physiol 252, R240-R246 (1987).
10. Doty, S. B., Morey-Holton, E. R., Durnova, G. N. & Kaplansky, A. S. Morphological studies of bone and tendon. J Appl Physiol (1985) 73, 10S-13S (1992).
11. Zerath, E. et al. Spaceflight inhibits bone formation independent of corticosteroid status in growing rats. J Bone Miner Res 15, 1310-1320 (2000).
12. Vico, L. et al. Effects of long-term microgravity exposure on cancellous and cortical weight-bearing bones of cosmonauts. Lancet 355, 1607-1611 (2000).
13. Landis, W. J., Hodgens, K. J., Block, D., Toma, C. D. & Gerstenfeld, L. C. Spaceflight effects on cultured embryonic chick bone cells. J Bone Miner Res 15, 1099-1112 (2000).
14. Pardo, S. J. et al. Simulated microgravity using the Random Positioning Machine inhibits differentiation and alters gene expression profiles of 2T3 preosteoblasts. Am J Physiol Cell Physiol 288, C1211-21 (2005).
15. Bergh, J. J., Shao, Y., Puente, E., Duncan, R. L. & Farach-Carson,M. C. Osteoblast Ca21 permeability and voltage-sensitive Ca21 channel expression is temporally regulated by 1, 25-dihydroxyvitamin D3. Am J Physiol Cell Physiol 290, C822-C831 (2006).
16. Bergh, J. J., Shao, Y., Akanbi, K. & Farach-Carson, M. C. Rodent osteoblastic cells express voltage-sensitive calcium channels lacking a gamma subunit. Calcif Tissue Int 73, 502-510 (2003).
17. Duncan, R. L., Akanbi, K. A. & Farach-Carson, M. C. Calcium signals and calcium channels in osteoblastic cells. Semin Nephrol 18, 178-190 (1998).
18. Liu, R. et al. Ribozyme ablation demonstrates that the cardiac subtype of the voltage-sensitive calcium channel is the molecular transducer of 1, 25-dihydroxyvitamin D3-stimulated calcium influx in osteoblastic cells. J Biol Chem 275, 8711-8718 (2000).
19. Iqbal, J. & Zaidi, M. Molecular regulation of mechanotransduction. Biochem Biophys Res Commun 328, 751-755 (2005).
20. Guggino, S. E., Lajeunesse, D., Wagner, J. A. & Snyder, S. H. Bone remodeling signaled by a dihydropyridine-and phenylalkylamine-sensitive calcium channel. Proc Natl Acad Sci U S A 86, 2957-2960 (1989).
21. Ritchie, C. K., Maercklein, P. B. & Fitzpatrick, L. A. Direct effect of calcium channel antagonists on osteoclast function: alterations in bone resorption and intracellular calcium concentrations. Endocrinology 135, 996-1003 (1994).
22. Vadiakas, G. P. & Banes, A. J. Verapamil decreases cyclic load-induced calcium incorporation in ROS 17/2.8 osteosarcoma cell cultures. Matrix 12, 439-447 (1992).
23. Li, J., Duncan, R. L., Burr, D. B. & Turner, C. H. L-type calcium channels mediate mechanically induced bone formation in vivo. J Bone Miner Res 17, 1795-1800 (2002).
24. Walker, L. M., Publicover, S. J., Preston, M. R., Said, A. M. & El, H. A. Calciumchannel activation and matrix protein upregulation in bone cells in response to mechanical strain. J Cell Biochem 79, 648-661 (2000).
25. Li, J., Duncan, R. L., Burr, D. B., Gattone, V. H. & Turner, C. H. Parathyroid hormone enhances mechanically induced bone formation, possibly involving Ltype voltage-sensitive calcium channels. Endocrinology 144, 1226-1233 (2003).
26. Zanello, L. P. & Norman, A. 1a, 25(OH)2 vitamin D3 actions on ion channels in osteoblasts. Steroids 71, 291-297 (2006).
27. Ambros, V. The functions of animal microRNAs. Nature 431, 350-355 (2004).
28. Bartel, D. P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281-297 (2004).
29. Bartel, D. P. MicroRNAs: target recognition and regulatory functions. Cell 136, 215-233 (2009).
30. Fabian, M. R., Sonenberg, N. & Filipowicz, W. Regulation of mRNA translation and stability by microRNAs. Annu Rev Biochem 79, 351-379 (2010).
31. Rau, F. et al. Misregulation of miR-1 processing is associated with heart defects in myotonic dystrophy. Nat Struct Mol Biol 18, 840-845 (2011).
32. Zhang, Y. et al. Overexpression of microRNA-1 causes atrioventricular block in rodents. Int J Biol Sci 9, 455-462 (2013).
33. Ripke, S. et al. Genome-wide association study identifies five new schizophrenia loci. Nat Genet 43, 969-976 (2011).
34. Guella, I. et al. Analysis of miR-137 expression and rs1625579 in dorsolateral prefrontal cortex. J Psychiatr Res 47, 1215-1221 (2013).
35. Lu, Y. et al. MicroRNA-328 contributes to adverse electrical remodeling in atrial fibrillation. Circulation 122, 2378-2387 (2010).
36. Wang, J. et al. Differential expressions of miRNAs in patients with nonvalvular atrial fibrillation. Zhonghua Yi Xue Za Zhi 92, 1816-1819 (2012).
37. Sadegh, M. K. et al. Deletion ofDicer in smooth muscle affects voiding pattern and reduces detrusor contractility and neuroeffector transmission. PLoS One 7, e35882 (2012).
38. Favereaux, A. et al. Bidirectional integrative regulation of Cav1.2 calcium channel by microRNA miR-103: role in pain. Embo J 30, 3830-3841 (2011).
39. Scott, A., Khan, K. M., Duronio, V. &Hart, D. A. Mechanotransduction in human bone: in vitro cellular physiology that underpins bone changes with exercise. Sports Med 38, 139-160 (2008).
40. Wang, Y. C., Zhang, S., Du, T. Y., Wang, B. & Sun, X.Q. Clinorotation upregulates inducible nitric oxide synthase by inhibiting AP-1 activation in human umbilical vein endothelial cells. J Cell Biochem 107, 357-363 (2009).
41. McAllister, T. N. & Frangos, J. A. Steady and transient fluid shear stress stimulate NO release in osteoblasts through distinct biochemical pathways. J Bone Miner Res 14, 930-936 (1999).
42. Genetos, D. C., Geist, D. J., Liu, D., Donahue, H. J. & Duncan, R. L. Fluid shearinduced ATP secretion mediates prostaglandin release in MC3T3-E1 osteoblasts. J Bone Miner Res 20, 41-49 (2005).
43. Chen, N. X., Geist, D. J., Genetos, D. C., Pavalko, F. M. & Duncan, R. L. Fluid shear-induced NFkB translocation in osteoblasts is mediated by intracellular calcium release. Bone 33, 399-410 (2003).
44. Li, J., Duncan, R. L., Burr, D. B. & Turner, C. H. L-type calcium channels mediate mechanically induced bone formation in vivo. J Bone Miner Res 17, 1795-1800 (2002).
45. Lieberherr, M. Effects of vitamin D3 metabolites on cytosolic free calcium in confluent mouse osteoblasts. J Biol Chem 262, 13168-13173 (1987).
46. Bidwell, J. P., Carter, W. B., Fryer, M. J. & Heath, H. R. Parathyroid hormone (PTH)-induced intracellular Ca21 signalling in naive and PTH-desensitized osteoblast-like cells (ROS 17/2.8): pharmacological characterization and evidence for synchronous oscillation of intracellular Ca21. Endocrinology 129, 2993-3000 (1991).
47. Duncan, R. L., Hruska, K. A. & Misler, S. Parathyroid hormone activation of stretch-activated cation channels in osteosarcoma cells (UMR-106.01). Febs Lett 307, 219-223 (1992).
48. Yamaguchi, D. T., Green, J., Kleeman, C. R. & Muallem, S. Characterization of volume-sensitive, calcium-permeating pathways in the osteosarcoma cell line UMR-106-01. J Biol Chem 264, 4383-4390 (1989).
49. Yang, L., Wang, Z.,Wang, B., Justice, N. J.& Zheng, H. Amyloid precursor protein regulates Cav1.2 L-type calcium channel levels and function to influence GABAergic short-term plasticity. J Neurosci 29, 15660-15668 (2009).
50. Ronkainen, J. J. et al. Ca21-calmodulin-dependent protein kinase II represses cardiac transcription of the L-type calcium channel a1C-subunit gene (Cacna1c) by DREAM translocation. J Physiol 589, 2669-2686 (2011).
51. Cui, J. et al. Correlation between oxidative stress and L-type calcium channel expression in the ventricular myocardia of selenium-deficient mice. J Int Med Res 40, 1677-1687 (2012).
52. Wang, X. T. et al. Cardiac L-type calcium channel alpha 1-subunit is increased by cyclic adenosine monophosphate: messenger RNA and protein expression in intact bone. J Bone Miner Res 15, 1275-1285 (2000).
53. Altier, C. et al. The Cavb subunit prevents RFP2-mediated ubiquitination and proteasomal degradation of L-type channels. Nat Neurosci 14, 173-180 (2011).
54. Rougier, J. S., Albesa, M., Abriel, H. &Viard, P. Neuronal precursor cell-expressed developmentally down-regulated 4-1 (NEDD4-1) controls the sorting of newly synthesized Cav1.2 calcium channels. J Biol Chem 286, 8829-38 (2011).
55. Kacena, M. A., Todd, P., Gerstenfeld, L. C. & Landis, W. J. Experiments with osteoblasts cultured under varying orientations with respect to the gravity vector. Cytotechnology 39, 147-154 (2002).
56. Barjaktarovic, Z. et al. Time-course of changes in amounts of specific proteins upon exposure to hyper-g, 2-D clinorotation, and 3-D random positioning of Arabidopsis cell cultures. J Exp Bot 58, 4357-4363 (2007).
57. Ryder, K. D. & Duncan, R. L. Parathyroid hormone enhances fluid shear-induced [Ca21]i signaling in osteoblastic cells through activation of mechanosensitive and voltage-sensitive Ca21 channels. J Bone Miner Res 16, 240-248 (2001).
58. Takeuchi, K. & Guggino, S. E. 24R, 25-(OH)2 vitamin D3 inhibits 1a, 25-(OH)2 vitamin D3 and testosterone potentiation of calcium channels in osteosarcoma cells. J Biol Chem 271, 33335-43 (1996).
59. Zanello, L. P. & Norman, A. W. Rapid modulation of osteoblast ion channel responses by 1a, 25(OH)2-vitamin D3 requires the presence of a functional vitamin D nuclear receptor. Proc Natl Acad Sci U S A 101, 1589-1594 (2004).
60. Xie, M. J., Zhang, L. F., Ma, J. & Cheng, H. W. Functional alterations in cerebrovascular K1 and Ca21 channels are comparable between simulated microgravity rat and SHR. Am J Physiol Heart Circ Physiol 289, H1265-H1276 (2005).
61. Thompson, W. R. et al. Association of the a2d1 subunit with Cav3.2 enhances membrane expression and regulates mechanically induced ATP release in MLOY4 osteocytes. J Bone Miner Res 26, 2125-2139 (2011).
62. Wang, H. et al. Chloride channel ClC-3 promotion of osteogenic differentiation through Runx2. J Cell Biochem 111, 49-58 (2010).