Table of Contents Author Guidelines Submit a Manuscript
Oxidative Medicine and Cellular Longevity
Volume 2014 (2014), Article ID 840951, 11 pages
http://dx.doi.org/10.1155/2014/840951
Research Article

Taurine Rescues Cisplatin-Induced Muscle Atrophy In Vitro: A Morphological Study

1Division of Anatomy and Physiopathology, Department of Clinical and Experimental Sciences, Brescia University, Viale Europa 11, 25123 Brescia, Italy
2Department of Molecular and Translational Medicine, Brescia University, Viale Europa 11, 25123 Brescia, Italy
3Department of Information Engineering, CNR-IDASC Sensor Laboratory, Brescia University, Via Valotti 9, 25123 Brescia, Italy
4Istituto Zooprofilattico Sperimentale della Lombardia e Dell’Emilia-Romagna, Via A. Bianchi 7/9, 25124 Brescia, Italy

Received 24 January 2014; Revised 27 March 2014; Accepted 17 April 2014; Published 13 May 2014

Academic Editor: Elaine Hatanaka

Copyright © 2014 Alessandra Stacchiotti et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. D. J. Glass, “Signaling pathways perturbing muscle mass,” Current Opinion in Clinical Nutrition and Metabolic Care, vol. 13, no. 3, pp. 225–229, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. M. Vinciguerra, A. Musaro, and N. Rosenthal, “Regulation of muscle atrophy in aging and disease,” Advances in Experimental Medicine and Biology, vol. 694, pp. 211–233, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. M. Sandri, “Signaling in muscle atrophy and hypertrophy,” Physiology, vol. 23, no. 3, pp. 160–170, 2008. View at Publisher · View at Google Scholar · View at Scopus
  4. A. Fanzani, A. Zanola, F. Rovetta, S. Rossi, and M. F. Aleo, “Cisplatin triggers atrophy of skeletal C2C12 myotubes via impairment of Akt signalling pathway and subsequent increment activity of proteasome and autophagy systems,” Toxicology and Applied Pharmacology, vol. 250, no. 3, pp. 312–321, 2011. View at Publisher · View at Google Scholar · View at Scopus
  5. C. Mammucari, G. Milan, V. Romanello et al., “FoxO3 controls autophagy in skeletal muscle in vivo,” Cell Metabolism, vol. 6, no. 6, pp. 458–471, 2007. View at Publisher · View at Google Scholar · View at Scopus
  6. C. Mammucari, S. Schiaffino, and M. Sandri, “Downstream of Akt: FoxO3 and mTOR in the regulation of autophagy in skeletal muscle,” Autophagy, vol. 4, no. 4, pp. 524–526, 2008. View at Google Scholar · View at Scopus
  7. E. Masiero, L. Agatea, C. Mammucari et al., “Autophagy is required to maintain muscle mass,” Cell Metabolism, vol. 10, no. 6, pp. 507–515, 2009. View at Publisher · View at Google Scholar · View at Scopus
  8. F. Madeo, N. Tavernarakis, and G. Kroemer, “Can autophagy promote longevity?” Nature Cell Biology, vol. 12, no. 9, pp. 842–846, 2010. View at Publisher · View at Google Scholar · View at Scopus
  9. D. J. Klionsky, “Autophagy: from phenomenology to molecular understanding in less than a decade,” Nature Reviews Molecular Cell Biology, vol. 8, no. 11, pp. 931–937, 2007. View at Publisher · View at Google Scholar · View at Scopus
  10. R. Rezzani, A. Stacchiotti, and L. F. Rodella, “Morphological and biochemical studies on aging and autophagy,” Ageing Research Reviews, vol. 11, no. 1, pp. 10–31, 2012. View at Publisher · View at Google Scholar · View at Scopus
  11. R. J. Huxtable, “Physiological actions of taurine,” Physiological Reviews, vol. 72, no. 1, pp. 101–164, 1992. View at Google Scholar · View at Scopus
  12. S. Roysommuti, J. Azuma, K. Takahashi et al., “Taurine cytoprotection: from cell to system,” Thai Journal of Physiological Sciences, vol. 16, no. 2, pp. 17–27, 2003. View at Google Scholar
  13. C. A. Goodman, D. Horvath, C. Stathis et al., “Taurine supplementation increases skeletal muscle force production and protects muscle function during and after high-frequency in vitro stimulation,” Journal of Applied Physiology, vol. 107, no. 1, pp. 144–154, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. R. Dawson Jr., M. Biasetti, S. Messina, and J. Dominy, “The cytoprotective role of taurine in exercise-induced muscle injury,” Amino Acids, vol. 22, no. 4, pp. 309–324, 2002. View at Publisher · View at Google Scholar · View at Scopus
  15. Y. Li, Z. Hu, B. Chen et al., “Taurine attenuates methamphetamine-induced autophagy and apoptosis in PC12 cells through mTOR signaling pathway,” Toxicology Letters, vol. 215, no. 1, pp. 1–7, 2012. View at Publisher · View at Google Scholar
  16. F. Rovetta, A. Stacchiotti, A. Consiglio et al., “ER signaling regulation drives the switch between autophagy and apoptosis in NRK-52E cells exposed to cisplatin,” Experimental Cell Research, vol. 318, no. 3, pp. 238–250, 2012. View at Publisher · View at Google Scholar · View at Scopus
  17. R. Leon, H. Wu, Y. Jin et al., “Protective function of taurine in glutamate-induced apoptosis in cultured neurons,” Journal of Neuroscience Research, vol. 87, no. 5, pp. 1185–1194, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. S. Burattini, R. Ferri, M. Battistelli, R. Curci, F. Luchetti, and E. Falcieri, “C2C12 murine myoblasts as a model of skeletal muscle development: morpho-functional characterization,” European Journal of Histochemistry, vol. 48, no. 3, pp. 223–233, 2004. View at Google Scholar · View at Scopus
  19. C. Pan, G. S. Giraldo, H. Prentice, and J.-Y. Wu, “Taurine protection of PC12 cells against endoplasmic reticulum stress induced by oxidative stress,” Journal of Biomedical Science, vol. 17, no. 1, article S17, 2010. View at Publisher · View at Google Scholar · View at Scopus
  20. P. O. Seglen and P. B. Gordon, “3-methyladenine: specific inhibitor of autophagic/lysosomal protein degradation in isolated rat hepatocytes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 79, no. 6, pp. 1889–1892, 1982. View at Google Scholar · View at Scopus
  21. A. Stacchiotti, G. Corsetti, A. Lavazza et al., “Microscopic features of mitochondria rejuvenation by amino acids,” in Current Microscopy Contributions to Advances in Science and Technology, A. Mendez-Vilas, Ed., pp. 286–294, Formatex, 2012. View at Google Scholar
  22. R. Curci, M. Battistelli, S. Burattini et al., “Surface and inner cell behaviour along skeletal muscle cell in vitro differentiation,” Micron, vol. 39, no. 7, pp. 843–851, 2008. View at Publisher · View at Google Scholar · View at Scopus
  23. S. Salucci, M. Battistelli, S. Burattini et al., “C2C12 myoblast sensitivity to different apoptotic chemical triggers,” Micron, vol. 41, no. 8, pp. 966–973, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. I. Tanida, T. Ueno, and E. Kominami, “LC3 and autophagy,” Methods in Molecular Biology, vol. 445, pp. 77–88, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. N. Mizushima, A. Yamamoto, M. Matsui, T. Yoshimori, and Y. Ohsumi, “In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker,” Molecular Biology of the Cell, vol. 15, no. 3, pp. 1101–1111, 2004. View at Publisher · View at Google Scholar · View at Scopus
  26. S. Kimura, T. Noda, and T. Yoshimori, “Dynein-dependent movement of autophagosomes mediates efficient encounters with lysosomes,” Cell Structure and Function, vol. 33, no. 1, pp. 109–122, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. E. L. Eskelinen, “Fine structure of the autophagosome,” in Autophagosomes and Phagosome, V. Deretic, Ed., vol. 445 of Methods in Molecular Biology, pp. 11–28, 2008. View at Google Scholar
  28. D. J. Klionsky, F. C. Abdalla, H. Abeliovich et al., “Guidelines for the use and interpretation of assays for monitoring,” Autophagy, vol. 8, no. 4, pp. 1–100, 2012. View at Publisher · View at Google Scholar
  29. D. C. Camerino, D. Tricarico, S. Pierno et al., “Taurine and skeletal muscle disorders,” Neurochemical Research, vol. 29, no. 1, pp. 135–142, 2004. View at Publisher · View at Google Scholar · View at Scopus
  30. V. M. Gonzalez, M. A. Fuertes, C. Alonso, and J. M. Perez, “Is cisplatin-induced cell death always produced by apoptosis?” Molecular Pharmacology, vol. 59, no. 4, pp. 657–663, 2001. View at Google Scholar · View at Scopus
  31. S. M. Sancho-Martinez, L. Prieto-Garcia, M. Prieto et al., “Subcellular targets of cisplatin cytotoxicity: an integrated view,” Pharmacology & Therapeutics, vol. 136, no. 1, pp. 35–55, 2012. View at Publisher · View at Google Scholar
  32. S. Orrenius, V. O. Kaminskyy, and B. Zhivotovsky, “Autophagy in toxicology: cause or consequence?” Annual Review of Pharmacology and Toxicology, vol. 53, pp. 275–297, 2013. View at Publisher · View at Google Scholar
  33. C. de Palma, F. Morisi, S. Cheli et al., “Autophagy as a new therapeutic target in Duchenne muscular dystrophy,” Cell Death & Disease, vol. 3, article e418, 2012. View at Google Scholar
  34. E. Masiero and M. Sandri, “Autophagy inhibition induces atrophy and myopathy in adult skeletal muscles,” Autophagy, vol. 6, no. 2, pp. 307–309, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. A. Fanzani, V. M. Conraads, F. Penna, and W. Martinet, “Molecular and cellular mechanisms of skeletal muscle atrophy: an update,” Journal of Cachexia, Sarcopenia and Muscle, vol. 3, no. 3, pp. 163–179, 2012. View at Publisher · View at Google Scholar
  36. F. Penna, D. Costamagna, F. Pin et al., “Autophagic degradation contributes to muscle wasting in cancer cachexia,” The American Journal of Pathology, vol. 182, no. 4, pp. 1367–1378, 2013. View at Publisher · View at Google Scholar
  37. G. Kroemer and B. Levine, “Autophagic cell death: the story of a misnomer,” Nature Reviews Molecular Cell Biology, vol. 9, no. 12, pp. 1004–1010, 2008. View at Publisher · View at Google Scholar · View at Scopus
  38. E. Ferraro, A. M. Giammarioli, S. Caldarola et al., “The metabolic modulator trimetazidine triggers autophagy and counteract stress-induced atrophy in skeletal muscle myotubes,” The FEBS Journal, vol. 280, no. 20, pp. 5094–5108, 2013. View at Publisher · View at Google Scholar
  39. J. Lee, K.-H. Yang, C. O. Joe, and S.-S. Kang, “Formation of distinct inclusion bodies by inhibition of ubiquitin-proteasome and autophagy-lysosome pathways,” Biochemical and Biophysical Research Communications, vol. 404, no. 2, pp. 672–677, 2011. View at Publisher · View at Google Scholar · View at Scopus
  40. P. Grumati and P. Bonaldo, “Autophagy in skeletal muscle homeostasis and in muscular dystrophies,” Cells, vol. 1, no. 3, pp. 325–345, 2012. View at Publisher · View at Google Scholar
  41. R. Xiao, A. L. Ferry, and E. E. Dupont-Versteegden, “Cell death-resistance of differentiated myotubes is associated with enhanced anti-apoptotic mechanisms compared to myoblasts,” Apoptosis, vol. 16, no. 3, pp. 221–234, 2011. View at Publisher · View at Google Scholar · View at Scopus
  42. S. Salucci, S. Burattini, V. Baldassarri et al., “The peculiar apoptotic behavior of skeletal muscle cells,” Histology and Histopathology, vol. 28, no. 8, pp. 1073–1087, 2013. View at Google Scholar
  43. N. Raben, V. Hill, L. Shea et al., “Suppression of autophagy in skeletal muscle uncovers the accumulation of ubiquitinated proteins and their potential role in muscle damage in Pompe disease,” Human Molecular Genetics, vol. 17, no. 24, pp. 3897–3908, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. P. Mukhopadhyay, B. Horváth, Z. Zsengellér et al., “Mitochondrial-targeted antioxidants represent a promising approach for prevention of cisplatin-induced nephropathy,” Free Radical Biology and Medicine, vol. 52, no. 2, pp. 497–506, 2012. View at Publisher · View at Google Scholar · View at Scopus
  45. T. Bouckenooghe, C. Remacle, and B. Reusens, “Is taurine a functional nutrient?” Current Opinion in Clinical Nutrition and Metabolic Care, vol. 9, no. 6, pp. 728–733, 2006. View at Publisher · View at Google Scholar · View at Scopus
  46. T. Ito, S. Oishi, M. Takai et al., “Cardiac and skeletal muscle abnormality in taurine transporter-knockout mice,” Journal of Biomedical Science, vol. 17, supplement 1, article S20, 2010. View at Publisher · View at Google Scholar · View at Scopus
  47. M. C. Pansani, P. S. Azevedo, B. P. Rafacho et al., “Atrophic cardiac remodeling induced by taurine deficiency in Wistar rats,” PLoS ONE, vol. 7, no. 7, Article ID e41439, 2012. View at Publisher · View at Google Scholar
  48. Y. Uozumi, T. Ito, K. Takahashi et al., “Myogenic induction of taurine transporter prevents dexamethasone-induced muscle atrophy,” Advances in Experimental Medicine and Biology, vol. 583, pp. 265–270, 2006. View at Publisher · View at Google Scholar · View at Scopus
  49. T. Takatani, K. Takahashi, Y. Uozumi et al., “Taurine prevents the ischemia-induced apoptosis in cultured neonatal rat cardiomyocytes through Akt/caspase-9 pathway,” Biochemical and Biophysical Research Communications, vol. 316, no. 2, pp. 484–489, 2004. View at Publisher · View at Google Scholar · View at Scopus
  50. Y. Yang, Y. Zhang, X. Liu et al., “Exogenous taurine attenuates mitochondrial oxidative stress and endoplasmic reticulum stress in rat cardiomyocytes,” Acta Biochimica et Biophysica Sinica, vol. 45, no. 5, pp. 359–367, 2013. View at Publisher · View at Google Scholar
  51. G. Santin, L. Scietti, P. Veneroni, S. Barni, G. Bernocchi, and M. G. Bottone, “Effects of cisplatin in neuroblastoma rat cells: damage to cellular organelles,” International Journal of Cell Biology, vol. 2012, Article ID 424072, 6 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  52. M. Sun and C. Xu, “Neuroprotective mechanism of taurine due to up-regulating calpastatin and down-regulating calpain and caspase-3 during focal cerebral ischemia,” Cellular and Molecular Neurobiology, vol. 28, no. 4, pp. 593–611, 2008. View at Publisher · View at Google Scholar · View at Scopus
  53. T. Kim and A. K. Kim, “Taurine enhances anticancer activity of cisplatin in human cervical cancer cells,” in TaurIne 8, A. El Idrissi and W. J. L'Amoreaux, Eds., vol. 776 of Advances in Experimental Medicine and Biology, pp. 189–198, 2013. View at Publisher · View at Google Scholar
  54. W. Bursch, A. Karwan, M. Mayer et al., “Cell death and autophagy: cytokines, drugs, and nutritional factors,” Toxicology, vol. 254, no. 3, pp. 147–157, 2008. View at Publisher · View at Google Scholar · View at Scopus