Table of Contents Author Guidelines Submit a Manuscript
Oxidative Medicine and Cellular Longevity
Volume 2014, Article ID 678371, 13 pages
http://dx.doi.org/10.1155/2014/678371
Research Article

Effect of Staurosporine in the Morphology and Viability of Cerebellar Astrocytes: Role of Reactive Oxygen Species and NADPH Oxidase

División de Neurociencias, Instituto de Fisiología Celular, Universidad Nacional Autónoma de México, Apartado Postal 70-253, 04510 México, DF, Mexico

Received 20 March 2014; Revised 20 June 2014; Accepted 23 June 2014; Published 17 August 2014

Academic Editor: Felipe Dal-Pizzol

Copyright © 2014 Mauricio Olguín-Albuerne 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. R. W. Oppenheim, D. Prevette, M. Tytell, and S. Homma, “Naturally occurring and induced neuronal death in the chick embryo in vivo requires protein and RNA synthesis: evidence for the role of cell death genes,” Developmental Biology, vol. 138, no. 1, pp. 104–113, 1990. View at Publisher · View at Google Scholar · View at Scopus
  2. J. Yuan and B. A. Yankner, “Apoptosis in the nervous system,” Nature, vol. 407, no. 6805, pp. 802–809, 2000. View at Publisher · View at Google Scholar · View at Scopus
  3. J. F. Kerr, A. H. Wyllie, and A. R. Currie, “Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics,” British Journal of Cancer, vol. 26, no. 4, pp. 239–257, 1972. View at Publisher · View at Google Scholar · View at Scopus
  4. N. A. Thornberry and Y. Lazebnik, “Caspases: enemies within,” Science, vol. 281, no. 5381, pp. 1312–1316, 1998. View at Publisher · View at Google Scholar · View at Scopus
  5. L. S. Brewton, L. Haddad, and E. C. Azmitia, “Colchicine-induced cytoskeletal collapse and apoptosis in N-18 neuroblastoma cultures is rapidly reversed by applied S-100β,” Brain Research, vol. 912, no. 1, pp. 9–16, 2001. View at Publisher · View at Google Scholar · View at Scopus
  6. S. B. Shelton and G. V. W. Johnson, “Tau and HMW tau phosphorylation and compartmentalization in apoptotic neuronal PC12 cells,” Journal of Neuroscience Research, vol. 66, no. 2, pp. 203–213, 2001. View at Publisher · View at Google Scholar · View at Scopus
  7. T. Mashima, M. Naito, and T. Tsuruo, “Caspase-mediated cleavage of cytoskeletal actin plays a positive role in the process of morphological apoptosis,” Oncogene, vol. 18, no. 15, pp. 2423–2430, 1999. View at Publisher · View at Google Scholar · View at Scopus
  8. A. Ortega and J. Morán, “Role of cytoskeleton proteins in the morphological changes during apoptotic cell death of cerebellar granule neurons,” Neurochemical Research, vol. 36, no. 1, pp. 93–102, 2011. View at Publisher · View at Google Scholar · View at Scopus
  9. A. F. Castoldi, S. Barni, I. Turin, C. Gandini, and L. Manzo, “Early acute necrosis, delayed apoptosis and cytoskeletal breakdown in cultured cerebellar granule neurons exposed to methylmercury,” Journal of Neuroscience Research, vol. 59, no. 6, pp. 775–787, 2000. View at Publisher · View at Google Scholar
  10. J. Y. Chang and J. Z. Wang, “Morphological and biochemical changes during programmed cell death of rat cerebellar granule cells,” Neurochemical Research, vol. 22, no. 1, pp. 43–48, 1997. View at Publisher · View at Google Scholar · View at Scopus
  11. E. Bonfoco, S. Ceccatelli, L. Manzo, and P. Nicotera, “Colchicine induces apoptosis in cerebellar granule cells,” Experimental Cell Research, vol. 218, no. 1, pp. 189–200, 1995. View at Publisher · View at Google Scholar · View at Scopus
  12. N. Canu, L. Dus, C. Barbato et al., “Tau cleavage and dephosphorylation in cerebellar granule neurons undergoing apoptosis,” Journal of Neuroscience, vol. 18, no. 18, pp. 7061–7074, 1998. View at Google Scholar · View at Scopus
  13. A. M. Gorman, E. Bonfoco, B. Zhivotovsky, S. Orrenius, and S. Ceccatelli, “Cytochrome c release and caspase-3 activation during colchicine-induced apoptosis of cerebellar granule cells,” European Journal of Neuroscience, vol. 11, no. 3, pp. 1067–1072, 1999. View at Publisher · View at Google Scholar · View at Scopus
  14. J. Kim, K. Mitsukawa, M. K. Yamada, N. Nishiyama, N. Matsuki, and Y. Ikegaya, “Cytoskeleton disruption causes apoptotic degeneration of dentate granule cells in hippocampal slice cultures,” Neuropharmacology, vol. 42, no. 8, pp. 1109–1118, 2002. View at Publisher · View at Google Scholar · View at Scopus
  15. B. W. Kristensen, H. Noer, J. B. Gramsbergen, J. Zimmer, and J. Noraberg, “Colchicine induces apoptosis in organotypic hippocampal slice cultures,” Brain Research, vol. 964, no. 2, pp. 264–278, 2003. View at Publisher · View at Google Scholar · View at Scopus
  16. E. G. Jordà, E. Verdaguer, A. Jimenez et al., “Evaluation of the neuronal apoptotic pathways involved in cytoskeletal disruption-induced apoptosis,” Biochemical Pharmacology, vol. 70, no. 3, pp. 470–780, 2005. View at Publisher · View at Google Scholar · View at Scopus
  17. G. J. Müller, M. A. Geist, L. M. Veng et al., “A role for mixed lineage kinases in granule cell apoptosis induced by cytoskeletal disruption,” Journal of Neurochemistry, vol. 96, no. 5, pp. 1242–1252, 2006. View at Publisher · View at Google Scholar · View at Scopus
  18. A. Bretscher, “Microfilament structure and function in the cortical cytoskeleton,” Annual Review of Cell Biology, vol. 7, pp. 337–374, 1991. View at Publisher · View at Google Scholar · View at Scopus
  19. R. W. Keane, A. Srinivasan, L. M. Foster et al., “Activation of CPP32 during apoptosis of neurons and astrocytes,” Journal of Neuroscience Research, vol. 48, no. 2, pp. 168–180, 1997. View at Publisher · View at Google Scholar
  20. M. W. Karaman, S. Herrgard, D. K. Treiber et al., “A quantitative analysis of kinase inhibitor selectivity,” Nature Biotechnology, vol. 26, no. 1, pp. 127–132, 2008. View at Publisher · View at Google Scholar · View at Scopus
  21. K. Abe, M. Yoshida, T. Usui, S. Horinouchi, and T. Beppu, “Highly synchronous culture of fibroblasts from G2 block caused by staurosporine, a potent inhibitor of protein kinases,” Experimental Cell Research, vol. 192, no. 1, pp. 122–127, 1991. View at Publisher · View at Google Scholar · View at Scopus
  22. T. Okazaki, Y. Kato, T. Mochizuki, M. Tashima, H. Sawada, and H. Uchino, “Staurosporine, a novel protein kinase inhibitor, enhances HL-60-cell differentiation induced by various compounds,” Experimental Hematology, vol. 16, no. 1, pp. 42–48, 1988. View at Google Scholar · View at Scopus
  23. T. Yue, C. Wang, A. M. Romanic et al., “Staurosporine-induced apoptosis in cardiomyocytes: a potential role of caspase-3,” Journal of Molecular and Cellular Cardiology, vol. 30, no. 3, pp. 495–507, 1998. View at Publisher · View at Google Scholar · View at Scopus
  24. A. J. Krohn, E. Preis, and J. H. M. Prehn, “Staurosporine-induced apoptosis of cultured rat hippocampal neurons involves caspase-1-like proteases as upstream initiators and increased production of superoxide as a main downstream effector,” Journal of Neuroscience, vol. 18, no. 20, pp. 8186–8197, 1998. View at Google Scholar · View at Scopus
  25. M. D. Jacobson, M. Weil, and M. C. Raff, “Role of Ced-3/ICE-family proteases in staurosporine-induced programmed cell death,” Journal of Cell Biology, vol. 133, no. 5, pp. 1041–1051, 1996. View at Publisher · View at Google Scholar · View at Scopus
  26. H. Chae, J. Kang, J. Byun et al., “Molecular mechanism of staurosporine-induced apoptosis in osteoblasts,” Pharmacological Research, vol. 42, no. 4, pp. 373–381, 2000. View at Publisher · View at Google Scholar · View at Scopus
  27. Y. Ramiro-Cortés, A. Guemez-Gamboa, and J. Morán, “Reactive oxygen species participate in the p38-mediated apoptosis induced by potassium deprivation and staurosporine in cerebellar granule neurons,” International Journal of Biochemistry and Cell Biology, vol. 43, no. 9, pp. 1373–1382, 2011. View at Publisher · View at Google Scholar · View at Scopus
  28. A. Valencia and J. Morn, “Role of oxidative stress in the apoptotic cell death of cultured cerebellar granule neurons,” Journal of Neuroscience Research, vol. 64, no. 3, pp. 284–297, 2001. View at Publisher · View at Google Scholar · View at Scopus
  29. A. Coyoy, A. Valencia, A. Guemez-Gamboa, and J. Morán, “Role of NADPH oxidase in the apoptotic death of cultured cerebellar granule neurons,” Free Radical Biology and Medicine, vol. 45, no. 8, pp. 1056–1064, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. M. R. Sánchez-Carbente, S. Castro-Obregón, L. Covarrubias, and V. Narváez, “Motoneuronal death during spinal cord development is mediated by oxidative stress,” Cell Death and Differentiation, vol. 12, no. 3, pp. 279–291, 2005. View at Publisher · View at Google Scholar · View at Scopus
  31. Y. Ramiro-Cortés and J. Morán, “Role of oxidative stress and JNK pathway in apoptotic death induced by potassium deprivation and staurosporine in cerebellar granule neurons,” Neurochemistry International, vol. 55, no. 7, pp. 581–592, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. H. M. Shen and S. Pervaiz, “TNF receptor superfamily-induced cell death: redox-dependent execution,” The FASEB Journal, vol. 20, no. 10, pp. 1589–1598, 2006. View at Publisher · View at Google Scholar · View at Scopus
  33. Z. Nayernia, V. Jaquet, and K. H. Krause, “New insights on NOX enzymes in the central nervous system,” Antioxidants & Redox Signaling, vol. 20, no. 17, pp. 2815–2837, 2014. View at Google Scholar
  34. S. Sorce and K. Krause, “NOX enzymes in the central nervous system: from signaling to disease,” Antioxidants and Redox Signaling, vol. 11, no. 10, pp. 2481–2504, 2009. View at Publisher · View at Google Scholar · View at Scopus
  35. D. W. Infanger, R. V. Sharma, and R. L. Davisson, “NADPH oxidases of the brain: distribution, regulation, and function,” Antioxidants and Redox Signaling, vol. 8, no. 9-10, pp. 1583–1596, 2006. View at Publisher · View at Google Scholar · View at Scopus
  36. J. L. Marín-Teva, I. Dusart, C. Colin, A. Gervais, N. van Rooijen, and M. Mallat, “Microglia promote the death of developing Purkinje cells,” Neuron, vol. 41, no. 4, pp. 535–547, 2004. View at Publisher · View at Google Scholar · View at Scopus
  37. J. Hur, P. Lee, M. J. Kim, Y. Kim, and Y. Cho, “Ischemia-activated microglia induces neuronal injury via activation of gp91phox NADPH oxidase,” Biochemical and Biophysical Research Communications, vol. 391, no. 3, pp. 1526–1530, 2010. View at Publisher · View at Google Scholar · View at Scopus
  38. D. Zhu, C. Hu, W. Sheng et al., “NAD(P)H oxidase-mediated reactive oxygen species production alters astrocyte membrane molecular order via phospholipase A2,” Biochemical Journal, vol. 421, no. 2, pp. 201–210, 2009. View at Publisher · View at Google Scholar · View at Scopus
  39. J. D. Lambeth, “NOX enzymes and the biology of reactive oxygen,” Nature Reviews Immunology, vol. 4, no. 3, pp. 181–189, 2004. View at Publisher · View at Google Scholar · View at Scopus
  40. Q. Liu, J. Kang, and R. Zheng, “NADPH oxidase produces reactive oxygen species and maintains survival of rat astrocytes,” Cell Biochemistry and Function, vol. 23, no. 2, pp. 93–100, 2005. View at Publisher · View at Google Scholar · View at Scopus
  41. D. G. Souza, B. Bellaver, D. O. Souza, and A. Quincozes-Santos, “Characterization of adult rat astrocyte cultures,” PLoS ONE, vol. 8, no. 3, Article ID e60282, 2013. View at Publisher · View at Google Scholar · View at Scopus
  42. D. I. Brown and K. K. Griendling, “Nox proteins in signal transduction,” Free Radical Biology and Medicine, vol. 47, no. 9, pp. 1239–1253, 2009. View at Publisher · View at Google Scholar · View at Scopus
  43. F. Klamt, S. Zdanov, R. L. Levine et al., “Oxidant-induced apoptosis is mediated by oxidation of the actin-regulatory protein cofilin,” Nature Cell Biology, vol. 11, no. 10, pp. 1241–2146, 2009. View at Publisher · View at Google Scholar
  44. M. Klemke, G. H. Wabnitz, F. Funke, B. Funk, H. Kirchgessner, and Y. Samstag, “Oxidation of cofilin mediates T cell hyporesponsiveness under oxidative stress conditions,” Immunity, vol. 29, no. 3, pp. 404–413, 2008. View at Publisher · View at Google Scholar · View at Scopus
  45. S. O. Loureiro, L. Heimfarth, E. B. S. Scherer et al., “Cytoskeleton of cortical astrocytes as a target to proline through oxidative stress mechanisms,” Experimental Cell Research, vol. 319, no. 3, pp. 89–104, 2013. View at Publisher · View at Google Scholar · View at Scopus
  46. D. Zhu, K. S. Tan, X. Zhang, A. Y. Sun, G. Y. Sun, and J. C.-. Lee, “Hydrogen peroxide alters membrane and cytoskeleton properties and increases intercellular connections in astrocytes,” Journal of Cell Science, vol. 118, no. 16, pp. 3695–3703, 2005. View at Publisher · View at Google Scholar · View at Scopus
  47. J. Moran and A. J. Patel, “Stimulation of the N-methyl-D-aspartate receptor promotes the biochemical differentiation of cerebellar granule neurons and not astrocytes,” Brain Research, vol. 486, no. 1, pp. 15–25, 1989. View at Publisher · View at Google Scholar · View at Scopus
  48. R. Balazs, O. S. Jorgensen, and N. Hack, “N-methyl-D-aspartate promotes the survival of cerebellar granule cells in culture,” Neuroscience, vol. 27, no. 2, pp. 437–451, 1988. View at Publisher · View at Google Scholar · View at Scopus
  49. J. B. Schulz, M. Weller, and T. Klockgether, “Potassium deprivation-induced apoptosis of cerebellar granule neurons: a sequential requirement for new mRNA and protein synthesis, ICE-like protease activity, and reactive oxygen species,” Journal of Neuroscience, vol. 16, no. 15, pp. 4696–4706, 1996. View at Google Scholar · View at Scopus
  50. A. Atlante, S. Gagliardi, E. Marra, and P. Calissano, “Neuronal apoptosis in rats is accompanied by rapid impairment of cellular respiration and is prevented by scavengers of reactive oxygen species,” Neuroscience Letters, vol. 245, no. 3, pp. 127–130, 1998. View at Publisher · View at Google Scholar · View at Scopus
  51. A. Valencia and J. Moran, “Reactive oxygen species induce different cell death mechanisms in cultured neurons,” Free Radical Biology and Medicine, vol. 36, no. 9, pp. 1112–1125, 2004. View at Publisher · View at Google Scholar · View at Scopus
  52. J. Falsig, M. Latta, and M. Leist, “Defined inflammatory states in astrocyte cultures: correlation with susceptibility towards CD95-driven apoptosis,” Journal of Neurochemistry, vol. 88, no. 1, pp. 181–193, 2004. View at Google Scholar · View at Scopus
  53. R. Bertrand, E. Solary, P. O'Connor, K. W. Kohn, and Y. Pommier, “Induction of a common pathway of apoptosis by staurosporine,” Experimental Cell Research, vol. 211, no. 2, pp. 314–321, 1994. View at Publisher · View at Google Scholar · View at Scopus
  54. J. Šimenc and M. Lipnik-Štangelj, “Staurosporine induces apoptosis and necroptosis in cultured rat astrocytes,” Drug and Chemical Toxicology, vol. 35, no. 4, pp. 399–405, 2012. View at Publisher · View at Google Scholar · View at Scopus
  55. J. Simenc and M. Lipnik-Stangelj, “Staurosporine induces different cell death forms in cultured rat astrocytes,” Radiology and Oncology, vol. 46, no. 4, pp. 312–320, 2012. View at Publisher · View at Google Scholar · View at Scopus
  56. Z. Zhu and G. Reiser, “PAR-1 activation rescues astrocytes through the PI3K/Akt signaling pathway from chemically induced apoptosis that is exacerbated by gene silencing of beta-arrestin 1,” Neurochemistry International, vol. 67, pp. 46–56, 2014. View at Google Scholar
  57. I. D'Alimonte, P. Ballerini, E. Nargi et al., “Staurosporine-induced apoptosis in astrocytes is prevented by A1 adenosine receptor activation,” Neuroscience Letters, vol. 418, no. 1, pp. 66–71, 2007. View at Publisher · View at Google Scholar · View at Scopus
  58. T. Satoh, T. Numakawa, Y. Abiru et al., “Production of reactive oxygen species and release of L-glutamate during superoxide anion-induced cell death of cerebellar granule neurons,” Journal of Neurochemistry, vol. 70, no. 1, pp. 316–324, 1998. View at Google Scholar · View at Scopus
  59. K. M. Noh and J. Y. Koh, “Induction and activation by zinc of NADPH oxidase in cultured cortical neurons and astrocytes,” The Journal of Neuroscience, vol. 20, no. 23, 2000. View at Google Scholar · View at Scopus
  60. R. Reinehr, B. Gorg, S. Becker et al., “Hypoosmotic swelling and ammonia increase oxidative stress by NADPH oxidase in cultured astrocytes and vital brain slices,” Glia, vol. 55, no. 7, pp. 758–771, 2007. View at Publisher · View at Google Scholar · View at Scopus
  61. K. Bedard, V. Jaquet, and K. Krause, “NOX5: from basic biology to signaling and disease,” Free Radical Biology and Medicine, vol. 52, no. 4, pp. 725–734, 2012. View at Publisher · View at Google Scholar · View at Scopus
  62. J. W. Choi, C. Y. Shin, B. K. Yoo et al., “Glucose deprivation increases hydrogen peroxide level in immunostimulated rat primary astrocytes,” Journal of Neuroscience Research, vol. 75, no. 5, pp. 722–731, 2004. View at Publisher · View at Google Scholar · View at Scopus
  63. A. Guidarelli, L. Palomba, M. Fiorani, and O. Cantoni, “Susceptibility of rat astrocytes to DNA strand scission induced by activation of NADPH oxidase and collateral resistance to the effects of peroxynitrite,” Free Radical Biology and Medicine, vol. 45, no. 4, pp. 521–529, 2008. View at Publisher · View at Google Scholar · View at Scopus
  64. S. Pendyala, I. A. Gorshkova, P. V. Usatyuk et al., “Role of Nox4 and Nox2 in hyperoxia-induced reactive oxygen species generation and migration of human lung endothelial cells,” Antioxidants and Redox Signaling, vol. 11, no. 4, pp. 747–764, 2009. View at Publisher · View at Google Scholar · View at Scopus
  65. J. Huot, F. Houle, S. Rousseau, R. G. Deschesnes, G. M. Shah, and J. Landry, “SAPK2/p38-dependent F-actin reorganization regulates early membrane blebbing during stress-induced apoptosis,” Journal of Cell Biology, vol. 143, no. 5, pp. 1361–1373, 1998. View at Publisher · View at Google Scholar · View at Scopus
  66. P. C. Endresen, J. Fandrem, T. J. Eide, and J. Aarbakke, “Morphological modifications of apoptosis in HL-60 cells: effects of homocysteine and cytochalasins on apoptosis initiated by 3-deazaadenosine,” Virchows Archiv, vol. 426, no. 3, pp. 257–266, 1995. View at Google Scholar · View at Scopus
  67. M. V. Blagosklonny, P. Giannakakou, W. S. El-Deiry et al., “Raf-1/bcl-2 phosphorylation: a step from microtubule damage to cell death,” Cancer Research, vol. 57, no. 1, pp. 130–135, 1997. View at Google Scholar · View at Scopus
  68. V. Perez, T. Bouschet, C. Fernandez, J. Bockaert, and L. Journot, “Dynamic reorganization of the astrocyte actin cytoskeleton elicited by cAMP and PACAP: a role for phosphatidylinositol 3-kinase inhibition,” European Journal of Neuroscience, vol. 21, no. 1, pp. 26–32, 2005. View at Publisher · View at Google Scholar · View at Scopus
  69. N. Rouach, A. Pébay, W. Même et al., “S1P inhibits gap junctions in astrocytes: involvement of Gi and Rho GTPase/ROCK,” European Journal of Neuroscience, vol. 23, no. 6, pp. 1453–1464, 2006. View at Publisher · View at Google Scholar · View at Scopus
  70. A. Hall, “Rho GTpases and the actin cytoskeleton,” Science, vol. 279, no. 5350, pp. 509–514, 1998. View at Publisher · View at Google Scholar · View at Scopus
  71. C. J. Chen, Y. C. Ou, S. Lin, S. Liao, Y. S. Huang, and A. N. Chiang, “L-glutamate activates RhoA GTPase leading to suppression of astrocyte stellation,” European Journal of Neuroscience, vol. 23, no. 8, pp. 1977–1987, 2006. View at Publisher · View at Google Scholar · View at Scopus
  72. M. Burgos, S. Calvo, F. Molina et al., “PKCε induces astrocyte stellation by modulating multiple cytoskeletal proteins and interacting with Rho a signalling pathways: implications for neuroinflammation,” European Journal of Neuroscience, vol. 25, no. 4, pp. 1069–1078, 2007. View at Publisher · View at Google Scholar · View at Scopus
  73. T. A. Cook, T. Nagasaki, and G. G. Gundersen, “Rho guanosine triphosphatase mediates the selective stabilization of microtubules induced by lysophosphatidic acid,” The Journal of Cell Biology, vol. 141, no. 1, pp. 175–185, 1998. View at Publisher · View at Google Scholar · View at Scopus