Table of Contents
Chemotherapy Research and Practice
Volume 2011 (2011), Article ID 315418, 14 pages
http://dx.doi.org/10.1155/2011/315418
Review Article

Developing Central Nervous System and Vulnerability to Platinum Compounds

1Laboratorio di Biologia Cellulare e Neurobiologia, Dipartimento di Biologia Animale, Università di Pavia, Via Ferrata 1, 27100 Pavia, Italy
2Istituto di Genetica Molecolare del CNR, Sezione di Istochimica e Citometria, Via Ferrata 1, 27100 Pavia, Italy
3Dipartimento di Scienze e Tecnologie Biologiche ed Ambientali, Università del Salento, 73100 Lecce, Italy

Received 1 October 2010; Accepted 21 December 2010

Academic Editor: Vito Lorusso

Copyright © 2011 G. Bernocchi 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. W. Rzeski, S. Pruskil, A. Macke et al., “Anticancers agents are potent neurotoxins in vitro and in vivo,” Annals of Neurology, vol. 56, no. 3, pp. 351–360, 2004. View at Publisher · View at Google Scholar · View at Scopus
  2. P. M. Rodier, “Developing brain as a target of toxicity,” Environmental Health Perspectives, vol. 103, no. 6, pp. 73–76, 1995. View at Google Scholar · View at Scopus
  3. S. A. Ferguson, M. G. Paule, and R. R. Holson, “Functional effects of methylazoxymethanol-induced cerebellar hypoplasia in rats,” Neurotoxicology and Teratology, vol. 18, no. 5, pp. 529–537, 1996. View at Publisher · View at Google Scholar · View at Scopus
  4. T. Fujii, “Transgenerational effects of maternal exposure to chemicals on the functional development of the brain in the offspring,” Cancer Causes and Control, vol. 8, no. 3, pp. 524–528, 1997. View at Publisher · View at Google Scholar · View at Scopus
  5. J. Altman, “Morphological development of the rat cerebellum and some of its mechanisms,” in The Cerebellum-New Vistas, S. L. Palay and V. Chan-Palay, Eds., pp. 8–49, Springer, Berlin, Germany, 1982. View at Google Scholar
  6. S. A. Ferguson, “Neuroanatomical and functional alterations resulting from early postnatal cerebellar insults in rodents,” Pharmacology Biochemistry and Behavior, vol. 55, no. 4, pp. 663–671, 1996. View at Publisher · View at Google Scholar · View at Scopus
  7. S. R. McWhinney, R. M. Goldberg, and H. L. McLeod, “Platinum neurotoxicity pharmacogenetics,” Molecular Cancer Therapeutics, vol. 8, no. 1, pp. 10–16, 2009. View at Publisher · View at Google Scholar · View at Scopus
  8. A. W. Prestayko, J. C. D'Aoust, B. F. Issell, and S. T. Crooke, “Cisplatin (cis-diamminedichloroplatinum II),” Cancer Treatment Reviews, vol. 6, no. 1, pp. 17–39, 1979. View at Google Scholar · View at Scopus
  9. S. Sugimoto, Y. L. Yamamoto, S. Nagahiro, and M. Diksic, “Permeability change and brain tissue damage after intracarotid administration of cisplatin studied by double-tracer autoradiography in rats,” Journal of Neuro-Oncology, vol. 24, no. 3, pp. 229–240, 1995. View at Publisher · View at Google Scholar · View at Scopus
  10. A. Wick, W. Wick, J. Hirrlinger et al., “Chemotherapy-induced cell death in primary cerebellar granule neurons but not in astrocytes: in vitro paradigm of differential neurotoxicity,” Journal of Neurochemistry, vol. 91, no. 5, pp. 1067–1074, 2004. View at Publisher · View at Google Scholar · View at Scopus
  11. M. M. K. Shahzad, G. Lopez-Berestein, and A. K. Sood, “Novel strategies for reversing platinum resistance,” Drug Resistance Updates, vol. 12, no. 6, pp. 148–152, 2009. View at Publisher · View at Google Scholar · View at Scopus
  12. M. B. Pisu, E. Roda, S. Guioli, D. Avella, M. G. Bottone, and G. Bernocchi, “Proliferation and migration of granule cells in the developing rat cerebellum: cisplatin effects,” The Anatomical Record Part A, vol. 287, no. 2, pp. 1226–1235, 2005. View at Publisher · View at Google Scholar · View at Scopus
  13. M. L. Graham, J. E. Herndon, J. R. Casey et al., “High-dose chemotherapy with autologous stem-cell rescue in patients with recurrent and high-risk pediatric brain tumors,” Journal of Clinical Oncology, vol. 15, no. 5, pp. 1814–1823, 1997. View at Google Scholar · View at Scopus
  14. J. Holmes, J. Stanko, M. Varchenko et al., “Comparative neurotoxicity of oxaliplatin, cisplatin, and ormaplatin in a wistar rat model,” Toxicological Sciences, vol. 46, no. 2, pp. 342–351, 1998. View at Publisher · View at Google Scholar · View at Scopus
  15. R. F. Borch, “The platinum antitumor drugs,” in Metabolism and Action of Anticancer Drugs, G. Powis and R. A. Proum, Eds., pp. 163–193, Taylor and Francis, London, UK, 1987. View at Google Scholar
  16. J. Schiffer, N. Walach, A. Nyska, G. Lushkov, S. Rothman, and L. Pollak, “Brain effect of intracarotid administration of cisplatinum,” Neurological Research, vol. 18, no. 1, pp. 87–88, 1996. View at Google Scholar · View at Scopus
  17. R. W. Gregg, J. M. Molepo, V. J. A. Monpetit et al., “Cisplatin neurotoxicity: the relationship between dosage, time, and platinum concentration in neurologic tissues, and morphologic evidence of toxicity,” Journal of Clinical Oncology, vol. 10, no. 5, pp. 795–803, 1992. View at Google Scholar · View at Scopus
  18. L. Troy, K. McFarland, S. Littman-Power et al., “Cisplatin-based therapy: a neurological and neuropsychological review,” Psycho-Oncology, vol. 9, no. 1, pp. 29–39, 2000. View at Publisher · View at Google Scholar · View at Scopus
  19. M. Stillman and J. P. Cata, “Management of chemotherapy-induced peripheral neuropathy,” Current Pain and Headache Reports, vol. 10, no. 4, pp. 279–287, 2006. View at Publisher · View at Google Scholar · View at Scopus
  20. B. Dunlap and J. A. Paice, “Chemotherapy-induces peripheral neuropathy: a need for standardization in measurement,” The Journal of Supportive Oncology, vol. 4, no. 8, pp. 398–399, 2006. View at Google Scholar · View at Scopus
  21. J. K. Sul and L. M. DeAngelis, “Neurologic complications of cancer chemotherapy,” Seminars in Oncology, vol. 33, no. 3, pp. 324–332, 2006. View at Publisher · View at Google Scholar · View at Scopus
  22. M. J. McKeage, T. Hsu, D. Screnci, G. Haddad, and B. C. Baguley, “Nucleolar damage correlates with neurotoxicity induced by different platinum drugs,” British Journal of Cancer, vol. 85, no. 8, pp. 1219–1225, 2001. View at Publisher · View at Google Scholar · View at Scopus
  23. E. Scherini and G. Bernocchi, “CisDDP treatment and development of the rat cerebellum,” Progress in Neurobiology, vol. 42, no. 2, pp. 161–196, 1994. View at Publisher · View at Google Scholar · View at Scopus
  24. M. B. Pisu, S. Guioli, E. Conforti, and G. Bernocchi, “Signal molecules and receptors in the differential development of cerebellum lobules. Acute effects of cisplatin on nitric oxide and glutamate systems in Purkinje cell population,” Developmental Brain Research, vol. 145, no. 2, pp. 229–240, 2003. View at Publisher · View at Google Scholar · View at Scopus
  25. E. Roda, D. Avella, M. B. Pisu, and G. Bernocchi, “Monoamine receptors and immature cerebellum cytoarchitecture after cisplatin injury,” Journal of Chemical Neuroanatomy, vol. 33, no. 1, pp. 42–52, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. M. B. Pisu, E. Roda, D. Avella, and G. Bernocchi, “Developmental plasticity of rat cerebellar cortex after cisplatin injury: inhibitory synapses and differentiating Purkinje neurons,” Neuroscience, vol. 129, no. 3, pp. 655–664, 2004. View at Publisher · View at Google Scholar · View at Scopus
  27. D. Avella, M. B. Pisu, E. Roda, M. Gravati, and G. Bernocchi, “Reorganization of the rat cerebellar cortex during postnatal development following cisplatin treatment,” Experimental Neurology, vol. 201, no. 1, pp. 131–143, 2006. View at Publisher · View at Google Scholar · View at Scopus
  28. A. J. Chou and R. Gorlick, “Chemotherapy resistance in osteosarcoma: current challenges and future directions,” Expert Review of Anticancer Therapy, vol. 6, no. 7, pp. 1075–1085, 2006. View at Publisher · View at Google Scholar · View at Scopus
  29. M. M. Gottesman, “Mechanisms of cancer drug resistance,” Annual Review of Medicine, vol. 53, pp. 615–627, 2002. View at Publisher · View at Google Scholar · View at Scopus
  30. G. Ricci, F. De Maria, G. Antonini et al., “7-nitro-2,1,3-benzoxadiazole derivatives, a new class of suicide inhibitors for glutathione S-transferases: mechanism of action of potential anticancer drugs,” The Journal of Biological Chemistry, vol. 280, no. 28, pp. 26397–26405, 2005. View at Publisher · View at Google Scholar · View at Scopus
  31. S. G. Chaney and A. Sancar, “DNA repair: enzymatic mechanisms and relevance to drug response,” Journal of the National Cancer Institute, vol. 88, no. 19, pp. 1346–1360, 1996. View at Google Scholar · View at Scopus
  32. T. Furuta, T. Ueda, G. Aune, A. Sarasin, K. H. Kraemer, and Y. Pommier, “Transcription-coupled nucleotide excision repair as a determinant of cisplatin sensitivity of human cells,” Cancer Research, vol. 62, no. 17, pp. 4899–4902, 2002. View at Google Scholar · View at Scopus
  33. D. J. Stewart, “Mechanisms of resistance to cisplatin and carboplatin,” Critical Reviews in Oncology/Hematology, vol. 63, no. 1, pp. 12–31, 2007. View at Publisher · View at Google Scholar · View at Scopus
  34. M. Sakamoto, A. Kondo, K. Kawasaki et al., “Analysis of gene expression profiles associated with cisplatin resistance in human ovarian cancer cell lines and tissues using cDNA microarray,” Human Cell, vol. 14, no. 4, pp. 305–315, 2001. View at Google Scholar · View at Scopus
  35. J. A. Green, L. J. Robertson, and A. H. Clark, “Glutathione S-transferase expression in benign and malignant ovarian tumours,” British Journal of Cancer, vol. 68, no. 2, pp. 235–239, 1993. View at Google Scholar · View at Scopus
  36. M. G. Bottone, C. Soldani, P. Veneroni, D. Avella, M. Pisu, and G. Bernocchi, “Cell proliferation, apoptosis and mitochondrial damage in rat B50 neuronal cells after cisplatin treatment,” Cell Proliferation, vol. 41, no. 3, pp. 506–520, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. X. J. Liang, S. Mukherjee, D. W. Shen, F. R. Maxfield, and M. M. Gottesman, “Endocytic recycling compartments altered in cisplatin-resistant cancer cells,” Cancer Research, vol. 66, no. 4, pp. 2346–2353, 2006. View at Publisher · View at Google Scholar · View at Scopus
  38. R. Safaei, B. J. Larson, T. C. Cheng et al., “Abnormal lysosomal trafficking and enhanced exosomal export of cisplatin in drug-resistant human ovarian carcinoma cells,” Molecular Cancer Therapeutics, vol. 4, no. 10, pp. 1595–1604, 2005. View at Publisher · View at Google Scholar · View at Scopus
  39. A. Andersson, H. Hedenmalm, B. Elfsson, and H. Ehrsson, “Determination of the acid dissociation constant for cis-diammineaquachloroplatinum(II) ion. A hydrolysis product of cisplatin,” Journal of Pharmaceutical Sciences, vol. 83, no. 6, pp. 859–862, 1994. View at Publisher · View at Google Scholar · View at Scopus
  40. H. Li and J. Yuan, “Deciphering the pathways of life and death,” Current Opinion in Cell Biology, vol. 11, no. 2, pp. 261–266, 1999. View at Publisher · View at Google Scholar · View at Scopus
  41. G. Santin, A. I. Scovassi, V. M. Piccolini et al., “Long-term effects of cisplatin in B50 neuroblastoma cells: mitochondria disfunction, and apoptosis autophagy,” in preparation.
  42. S. P. Moon, M. De Leon, and P. Devarajan, “Cisplatin induces apoptosis in LLC-PK1 cells via activation of mitochondrial pathways,” Journal of the American Society of Nephrology, vol. 13, no. 4, pp. 858–865, 2002. View at Google Scholar · View at Scopus
  43. L. Moretti, E. S. Yang, K. W. Kim, and B. Lu, “Autophagy signaling in cancer and its potential as novel target to improve anticancer therapy,” Drug Resistance Updates, vol. 10, no. 4-5, pp. 135–143, 2007. View at Publisher · View at Google Scholar · View at Scopus
  44. N. Chen and J. Debnath, “Autophagy and tumorigenesis,” FEBS Letters, vol. 584, no. 7, pp. 1427–1435, 2010. View at Publisher · View at Google Scholar · View at Scopus
  45. Y. Kondo, T. Kanzawa, R. Sawaya, and S. Kondo, “The role of autophagy in cancer development and response to therapy,” Nature Reviews Cancer, vol. 5, no. 9, pp. 726–734, 2005. View at Publisher · View at Google Scholar · View at Scopus
  46. A. Muscella, N. Calabriso, S. A. De Pascali et al., “New platinum(II) complexes containing both an O,O-chelated acetylacetonate ligand and a sulfur ligand in the platinum coordination sphere induce apoptosis in HeLa cervical carcinoma cells,” Biochemical Pharmacology, vol. 74, no. 1, pp. 28–40, 2007. View at Publisher · View at Google Scholar · View at Scopus
  47. E. J. Dropcho, “Neurotoxicity of cancer chemotherapy,” Seminars in Neurology, vol. 24, no. 4, pp. 419–426, 2004. View at Publisher · View at Google Scholar · View at Scopus
  48. I. Kostova, “Platinum complexes as anticancer agents,” Recent Patents on Anti-Cancer Drug Discovery, vol. 1, no. 1, pp. 1–22, 2006. View at Publisher · View at Google Scholar · View at Scopus
  49. E. S. McDonald, K. R. Randon, A. Knight, and A. J. Windebank, “Cisplatin preferentially binds to DNA in dorsal root ganglion neurons in vitro and in vivo: a potential mechanism for neurotoxicity,” Neurobiology of Disease, vol. 18, no. 2, pp. 305–313, 2005. View at Publisher · View at Google Scholar · View at Scopus
  50. R. Suk, S. Gurubhagavatula, S. Park et al., “Polymorphisms in ERCC1 and grade 3 or 4 toxicity in non-small cell lung cancer patients,” Clinical Cancer Research, vol. 11, no. 4, pp. 1534–1538, 2005. View at Publisher · View at Google Scholar · View at Scopus
  51. G. Bernocchi, E. Scherini, and R. Nano, “Developmental patterns in the rat cerebellum after cis-dichlorodiammineplatinum treatment,” Neuroscience, vol. 39, no. 1, pp. 179–188, 1990. View at Publisher · View at Google Scholar · View at Scopus
  52. S. A. De Pascali, P. Papadia, A. Ciccarese, C. Pacifico, and F. P. Fanizzi, “First examples of β-diketonate platinum(II) complexes with sulfoxide ligands,” European Journal of Inorganic Chemistry, no. 4, pp. 788–796, 2005. View at Publisher · View at Google Scholar · View at Scopus
  53. A. Muscella, N. Calabriso, F. P. Fanizzi et al., “[Pt(O,O-acac)(γ-acac)(DMS)], a new Pt compound exerting fast cytotoxicity in MCF-7 breast cancer cells via the mitochondrial apoptotic pathway,” British Journal of Pharmacology, vol. 153, no. 1, pp. 34–49, 2008. View at Publisher · View at Google Scholar · View at Scopus
  54. S. A. De Pascali, P. Papadia, S. Capoccia et al., “Hard/soft selectivity in ligand substitution reactions of β-diketonate platinum(II) complexes,” Dalton Transactions, no. 37, pp. 7786–7795, 2009. View at Publisher · View at Google Scholar · View at Scopus
  55. D. L. Bodenner, P. C. Dedon, P. C. Keng, and R. F. Borch, “Effect of diethyldithiocarbamate on cis-diamminedichloroplatinum(II)-induced cytotoxicity, DNA cross-linking, and γ-glutamyl transpeptidase inhibition,” Cancer Research, vol. 46, no. 6, pp. 2745–2750, 1986. View at Google Scholar · View at Scopus
  56. J. Dietrich, R. Han, Y. Yang, M. Mayer-Pröschel, and M. Noble, “CNS progenitor cells and oligodendrocytes are targets of chemotherapeutic agents in vitro and in vivo,” Journal of Biology, vol. 5, article 22, 2006. View at Publisher · View at Google Scholar · View at Scopus
  57. P. M. Rodier, “Chronology of neuron development: animal studies and their clinical implications,” Developmental Medicine and Child Neurology, vol. 22, no. 4, pp. 525–545, 1980. View at Google Scholar · View at Scopus
  58. R. W. Oppenheim, “Cell death during development of the nervous system,” Annual Review of Neuroscience, vol. 14, pp. 453–501, 1991. View at Google Scholar · View at Scopus
  59. L. Lossi, S. Mioletti, and A. Merighi, “Synapse-independent and synapse-dependent apoptosis of cerebellar granule cells in postnatal rabbits occur at two subsequent but partly overlapping developmental stages,” Neuroscience, vol. 112, no. 3, pp. 509–523, 2002. View at Publisher · View at Google Scholar · View at Scopus
  60. L. Zhang and J. E. Goldman, “Generation of cerebellar interneurons from dividing progenitors in white matter,” Neuron, vol. 16, no. 1, pp. 47–54, 1996. View at Publisher · View at Google Scholar · View at Scopus
  61. M. Hoser, S. L. Baader, M. R. Bösl, A. Ihmer, M. Wegner, and E. Sock, “Prolonged glial expression of Sox4 in the CNS leads to architectural cerebellar defects and ataxia,” Journal of Neuroscience, vol. 27, no. 20, pp. 5495–5505, 2007. View at Publisher · View at Google Scholar · View at Scopus
  62. A. Sudarov and A. L. Joyner, “Cerebellum morphogenesis: the foliation pattern is orchestrated by multi-cellular anchoring centers,” Neural Development, vol. 2, no. 1, article 26, 2007. View at Publisher · View at Google Scholar · View at Scopus
  63. S. Cerri, V. M. Piccolini, and G. Bernocchi, “Postnatal development of the central nervous system: anomalies in the formation of cerebellum fissures,” The Anatomical Record, vol. 293, no. 3, pp. 492–501, 2010. View at Publisher · View at Google Scholar · View at Scopus
  64. M. L. Doughty, N. Delhaye-Bouchaud, and J. Mariani, “Quantitative analysis of cerebellar lobulation in normal and agranular rats,” The Journal of Comparative Neurology, vol. 399, no. 3, pp. 306–320, 1998. View at Google Scholar · View at Scopus
  65. M. Lafarga, M. A. Andres, E. Calle, and M. T. Berciano, “Reactive gliosis of immature Bergmann glia and microglial cell activation in response to cell death of granule cell precursors induced by methylazoxymethanol treatment in developing rat cerebellum,” Anatomy and Embryology, vol. 198, no. 2, pp. 111–122, 1998. View at Publisher · View at Google Scholar · View at Scopus
  66. P. M. Rodier, M. Aschner, and P. R. Sager, “Mitotic arrest in the developing CNS after prenatal exposure to methylmercury,” Neurobehavioral Toxicology and Teratology, vol. 6, no. 5, pp. 379–385, 1984. View at Google Scholar · View at Scopus
  67. B. H. Choi, “The effects of methylmercury on the developing brain,” Progress in Neurobiology, vol. 32, no. 6, pp. 447–470, 1989. View at Google Scholar · View at Scopus
  68. R. A. Ponce, T. J. Kavanagh, N. K. Mottet, S. G. Whittaker, and E. M. Faustman, “Effects of methyl mercury on the cell cycle of primary rat CNS cells in vitro,” Toxicology and Applied Pharmacology, vol. 127, no. 1, pp. 83–90, 1994. View at Publisher · View at Google Scholar · View at Scopus
  69. D. E. Bredesen, R. V. Rao, and P. Mehlen, “Cell death in the nervous system,” Nature, vol. 443, no. 7113, pp. 796–802, 2006. View at Publisher · View at Google Scholar · View at Scopus
  70. V. P. Nakka, A. Gusain, S. L. Mehta, and R. Raghubir, “Molecular mechanisms of apoptosis in cerebral ischemia: multiple neuroprotective opportunities,” Molecular Neurobiology, vol. 37, no. 1, pp. 7–32, 2007. View at Publisher · View at Google Scholar · View at Scopus
  71. 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
  72. R. S. Akhtar, J. M. Ness, and K. A. Roth, “Bcl-2 family regulation of neuronal development and neurodegeneration,” Biochimica et Biophysica Acta, vol. 1644, no. 2-3, pp. 189–203, 2004. View at Publisher · View at Google Scholar · View at Scopus
  73. V. Mares, E. Scherini, M. Biggiogera, and G. Bernocchi, “Influence of cis-dichlorodiammineplatinum on the structure of the immature rat cerebellum,” Experimental Neurology, vol. 91, no. 2, pp. 246–258, 1986. View at Google Scholar · View at Scopus
  74. S. Cerri, V. M. Piccolini, G. Santin et al., “The developmental neurotoxicity study of platinum compounds. Effects of cisplatin versus a novel Pt(II) complex on rat cerebellum,” Neurotoxicology and Teratology. In press. View at Publisher · View at Google Scholar
  75. I. Napoli and H. Neumann, “Microglial clearance function in health and disease,” Neuroscience, vol. 158, no. 3, pp. 1030–1038, 2009. View at Publisher · View at Google Scholar · View at Scopus
  76. 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
  77. H. Takeuchi, J. Wang, J. Kawanokuchi, N. Mitsuma, T. Mizuno, and A. Suzumura, “Interferon-γ induces microglial-activation-induced cell death: a hypothetical mechanism of relapse and remission in multiple sclerosis,” Neurobiology of Disease, vol. 22, no. 1, pp. 33–39, 2006. View at Publisher · View at Google Scholar · View at Scopus
  78. J. Hur, P. Lee, M. J. Kim, Y. Kim, and Y. W. 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
  79. N. B. Boneva, Y. Mori, D. B. Kaplamadzhiev et al., “Differential expression of FABP 3, 5, 7 in infantile and adult monkey cerebellum,” Neuroscience Research, vol. 68, no. 2, pp. 94–102, 2010. View at Publisher · View at Google Scholar
  80. F. Doetsch, J. M. García-Verdugo, and A. Alvarez-Buylla, “Regeneration of a germinal layer in the adult mammalian brain,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 20, pp. 11619–11624, 1999. View at Publisher · View at Google Scholar · View at Scopus
  81. J. S. Gill and A. J. Windebank, “Cisplatin-induced apoptosis in rat dorsal root ganglion neurons is associated with attempted entry into the cell cycle,” Journal of Clinical Investigation, vol. 101, no. 12, pp. 2842–2850, 1998. View at Google Scholar · View at Scopus
  82. M. A. Philbert, M. L. Billingsley, and K. R. Reuhl, “Mechanisms of injury in the central nervous system,” Toxicologic Pathology, vol. 28, no. 1, pp. 43–53, 2000. View at Google Scholar · View at Scopus
  83. M. G. Ormerod, C. O'Neill, D. Robertson, L. R. Kelland, and K. R. Harrap, “cis-diamminedichloroplatinum(II)-induced cell death through apoptosis in sensitive and resistant human ovarian carcinoma cell lines,” Cancer Chemotherapy and Pharmacology, vol. 37, no. 5, pp. 463–471, 1996. View at Google Scholar · View at Scopus
  84. T. Boulikas and M. Vougiouka, “Cisplatin and platinum drugs at the molecular level,” Oncology Reports, vol. 10, no. 6, pp. 1663–1682, 2003. View at Google Scholar · View at Scopus
  85. M. R. Celio, “Calcium binding proteins in the brain,” Italian Journal of Anatomy and Embryology, vol. 94, no. 3, pp. 227–236, 1989. View at Google Scholar · View at Scopus
  86. T. C. Kang, H. S. Kim, M. O. Seo et al., “The temporal alteration of GAD67/GAD65 ratio in the gerbil hippocampal complex following seizure,” Brain Research, vol. 920, no. 1-2, pp. 159–169, 2001. View at Publisher · View at Google Scholar · View at Scopus
  87. M. Esclapez, N. J. K. Tillakaratne, D. L. Kaufman, A. J. Tobin, and C. R. Houser, “Comparative localization of two forms of glutamic acid decarboxylase and their mRNAs in rat brain supports the concept of functional differences between the forms,” Journal of Neuroscience, vol. 14, no. 3, pp. 1834–1855, 1994. View at Google Scholar · View at Scopus
  88. R. P. Kleshcheva, “The development of components of the blood-brain barrier in the neocortex of the white rat,” Arkhiv Anatomii, Gistologii i Embriologii, vol. 95, no. 11, pp. 22–26, 1988. View at Google Scholar · View at Scopus
  89. K. Namikawa, M. Asakura, T. Minami, Y. Okazaki, E. Kadota, and S. Hashimoto, “Toxicity of cisplatin to the central nervous system of male rabbits,” Biological Trace Element Research, vol. 74, no. 3, pp. 223–225, 2000. View at Google Scholar · View at Scopus
  90. F. Sterzing, C. Grehn, J. Dinkel et al., “Severe reversible toxic encephalopathy induced by cisplatin in a patient with cervical carcinoma receiving combined radiochemotherapy,” Strahlentherapie und Onkologie, vol. 183, no. 9, pp. 487–489, 2007. View at Publisher · View at Google Scholar · View at Scopus
  91. R. I. Roelofs, W. Hrushesky, J. Rogin, and L. Rosenberg, “Peripheral sensory neuropathy and cisplatin chemotherapy,” Neurology, vol. 34, no. 7, pp. 934–938, 1984. View at Google Scholar · View at Scopus
  92. R. Chen, L. G. Cohen, and M. Hallett, “Nervous system reorganization following injury,” Neuroscience, vol. 111, no. 4, pp. 761–773, 2002. View at Publisher · View at Google Scholar · View at Scopus
  93. J. Altman, “Experimental reorganization of the cerebellar cortex. III. Regeneration of the external germinal layer and granule cell ectopia,” The Journal of Comparative Neurology, vol. 149, no. 2, pp. 153–180, 1973. View at Google Scholar · View at Scopus
  94. J. Altman, “Experimental reorganization of the cerebellar cortex. VII. Effects of late X irradiation schedules that interfere with cell acquisition after stellate cells are formed,” The Journal of Comparative Neurology, vol. 165, no. 1, pp. 65–76, 1976. View at Google Scholar · View at Scopus
  95. E. J. Lehning, C. D. Balaban, J. F. Ross, M. A. Reid, and R. M. LoPachin, “Acrylamide neuropathy I. Spatiotemporal characteristics of nerve cell damage in rat cerebellum,” NeuroToxicology, vol. 23, no. 3, pp. 397–414, 2002. View at Publisher · View at Google Scholar · View at Scopus
  96. I. Dusart, A. Ghoumari, R. Wehrle et al., “Cell death and axon regeneration of Purkinje cells after axotomy: challenges of classical hypotheses of axon regeneration,” Brain Research Reviews, vol. 49, no. 2, pp. 300–316, 2005. View at Publisher · View at Google Scholar · View at Scopus
  97. F. Rossi, S. Gianola, and L. Corvetti, “The strange case of Purkinje axon regeneration and plasticity,” The Cerebellum, vol. 5, no. 2, pp. 174–182, 2006. View at Publisher · View at Google Scholar · View at Scopus