Differential impairment of catecholaminergic cell maturation and survival by genetic mitochondrial complex II dysfunction

Molecular and Cellular Biology

Volumn 32, Issue 16, 2012, Pages 3347-3357

  Díaz Castro, Blanca ^a,b   Pintado, C Oscar ^a   García Flores, Paula ^a,b   López Barneo, José ^a,b   Piruat, José I ^a,b  

^a HOSPITAL UNIVERSITARIO VIRGEN DEL ROCÍO   (Spain)

^b CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CRE RECOMBINASE; SUCCINATE DEHYDROGENASE (UBIQUINONE);

ADRENAL MEDULLA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CAROTID BODY; CATECHOLAMINE NERVE CELL; CELL COUNT; CELL LOSS; CELL MATURATION; CELL POPULATION; CELL SURVIVAL; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DOPAMINERGIC NERVE CELL; EMBRYO; ENZYME DEFECT; ENZYME INDUCTION; FEMALE; GENE DELETION; GENETIC DISORDER; HETEROZYGOTE; LOCUS CERULEUS; MESENCEPHALON; MOUSE; NONHUMAN; PARAGANGLIOMA; PARKINSON DISEASE; PHEOCHROMOCYTOMA; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; SUBSTANTIA NIGRA; SUPERIOR CERVICAL GANGLION; TISSUE SPECIFICITY;

ADENOSINE TRIPHOSPHATE; ALLELES; ANIMALS; CATECHOLAMINES; CELL DEATH; DISEASE MODELS, ANIMAL; DNA, MITOCHONDRIAL; ELECTRON TRANSPORT COMPLEX II; GENE EXPRESSION REGULATION, NEOPLASTIC; GENOTYPE; MEMBRANE PROTEINS; MICE; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; MITOCHONDRIA; MODELS, GENETIC; NEURONS; OXYGEN; RNA, MESSENGER;

EID: 84865141195     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00128-12     Document Type: Article

References (58)

1. Archer SL, Huang J, Henry T, Peterson D, Weir EK. 1993. A redoxbased O2 sensor in rat pulmonary vasculature. Circ. Res. 73:1100-1112.
2. Arenas E, Trupp M, Akerud P, Ibanez CF. 1995. GDNF prevents degeneration and promotes the phenotype of brain noradrenergic neurons in vivo. Neuron 15:1465-1473.
3. Bardella C, Pollard PJ, Tomlinson I. 2011. SDH mutations in cancer. Biochim. Biophys. Acta 1807:1432-1443.
4. Bayley JP, et al. 2009. Sdhd and SDHD/H19 knockout mice do not develop paraganglioma or pheochromocytoma. PLoS One 4:e7987.
5. Baysal BE. 2008. Clinical and molecular progress in hereditary paraganglioma. J. Med. Genet. 45:689-694.
6. Baysal BE, et al. 2000. Mutations in SDHD, a mitochondrial complex II gene, in hereditary paraganglioma. Science 287:848-851.
7. Betarbet R, et al. 2000. Chronic systemic pesticide exposure reproduces features of Parkinson's disease. Nat. Neurosci. 3:1301-1306.
8. Briere JJ, et al. 2005. Mitochondrial succinate is instrumental for HIF1alpha nuclear translocation in SDHA-mutant fibroblasts under normoxic conditions. Hum. Mol. Genet. 14:3263-3269.
9. Burke RE. 2003. Postnatal developmental programmed cell death in dopamine neurons. Ann. N. Y. Acad. Sci. 991:69-79.
10. Chan CS, Gertler TS, Surmeier DJ. 2010. A molecular basis for the increased vulnerability of substantia nigra dopamine neurons in aging and Parkinson's disease. Mov. Disord. 25 (Suppl. 1):S63-S70.
11. Chan CS, et al. 2007. 'Rejuvenation' protects neurons in mouse models of Parkinson's disease. Nature 447:1081-1086.
12. Chandel NS, et al. 1998. Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc. Natl. Acad. Sci. U. S. A. 95:11715-11720.
13. Collier TJ, Kanaan NM, Kordower JH. 2011. Ageing as a primary risk factor for Parkinson's disease: evidence from studies of non-human primates. Nat. Rev. Neurosci. 12:359-366.
14. Dauer W, Przedborski S. 2003. Parkinson's disease: mechanisms and models. Neuron 39:889-909.
15. Dawson TM, Dawson VL. 2003. Molecular pathways of neurodegeneration in Parkinson's disease. Science 302:819-822.
16. Ekstrand MI, et al. 2007. Progressive parkinsonism in mice with respiratory-chain-deficient dopamine neurons. Proc. Natl. Acad. Sci. U. S. A. 104:1325-1330.
17. Fredriksson A, Fredriksson M, Eriksson P. 1993. Neonatal exposure to paraquat or MPTP induces permanent changes in striatum dopamine and behavior in adult mice. Toxicol. Appl. Pharmacol. 122:258-264.
18. Guzman JN, et al. 2010. Oxidant stress evoked by pacemaking in dopaminergic neurons is attenuated by DJ-1. Nature 468:696-700.
19. Guzy RD, Sharma B, Bell E, Chandel NS, Schumacker PT. 2008. Loss of the SdhB, but not the SdhA, subunit of complex II triggers reactive oxygen species-dependent hypoxia-inducible factor activation and tumorigenesis. Mol. Cell. Biol. 28:718-731.
20. Hayashi S, McMahon AP. 2002. Efficient recombination in diverse tissues by a tamoxifen-inducible form of Cre: a tool for temporally regulated gene activation/inactivation in the mouse. Dev. Biol. 244:305-318.
21. Hederstedt L. 2003. Structural biology. Complex II is complex too. Science 299:671-672.
22. Hensen EF, et al. 2004. Somatic loss of maternal chromosome 11 causes parent-of-origin-dependent inheritance in SDHD-linked paraganglioma and phaeochromocytoma families. Oncogene 23:4076-4083.
23. Hidalgo-Figueroa M, Bonilla S, Gutierrez F, Pascual A, Lopez-Barneo J. 2012. GDNF Is predominantly expressed in the PV+neostriatal interneuronal ensemble in normal mouse and after injury of the nigrostriatal pathway. J. Neurosci. 32:864-872.
24. Ishii T, et al. 2011. Mitochondrial reactive oxygen species generation by the SDHC V69E mutation causes low birth weight and neonatal growth retardation. Mitochondrion 11:155-165.
25. Ishii T, et al. 2005. A mutation in the SDHC gene of complex II increases oxidative stress, resulting in apoptosis and tumorigenesis. Cancer Res. 65:203-209.
26. Jackson-Lewis V, et al. 2000. Developmental cell death in dopaminergic neurons of the substantia nigra of mice. J. Comp. Neurol. 424:476-488.
27. Kitada T, Tong Y, Gautier CA, Shen J. 2009. Absence of nigral degeneration in aged parkin/DJ-1/PINK1 triple knockout mice. J. Neurochem. 111:696-702.
28. Langston JW, and Ballard PA, Jr. 1983. Parkinson's disease in a chemist working with 1-methyl-4-phenyl-1,2,5,6-tetrahydropyridine. N. Engl. J. Med. 309:310.
29. Lindeberg J, et al. 2004. Transgenic expression of Cre recombinase from the tyrosine hydroxylase locus. Genesis 40:67-73.
30. Lopez-Barneo J, Ortega-Saenz P, Piruat JI, Garcia-Fernandez M. 2006. Oxygen-sensing by ion channels and mitochondrial function in carotid body glomus cells. Novartis Found. Symp. 272:54-64.
31. Maher LJ, III, et al. 2011. Mouse models of human familial paraganglioma. In Martin JF (ed), Pheochromocytoma-a new view of the old problem. Intech, Rijeka, Croatia. http://www.intechopen.com/books/pheochromocytoma-a-new-view-of-the-old-problem/mouse-models-of-human-familial-paraganglioma.
32. Mejias R, et al. 2006. Neuroprotection by transgenic expression of glucose-6-phosphate dehydrogenase in dopaminergic nigrostriatal neurons of mice. J. Neurosci. 26:4500-4508.
33. Minguez-Castellanos A, et al. 2007. Do alpha-synuclein aggregates in autonomic plexuses predate Lewy body disorders?: a cohort study. Neurology 68:2012-2018.
34. Muller U. 2011. Pathological mechanisms and parent-of-origin effects in hereditary paraganglioma/pheochromocytoma (PGL/PCC). Neurogenetics 12:175-181.
35. Ohkawa H, Ohishi N, Yagi K. 1979. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal. Biochem. 95:351-358.
36. Ortega-Saenz P, Pardal R, Garcia-Fernandez M, Lopez-Barneo J. 2003. Rotenone selectively occludes sensitivity to hypoxia in rat carotid body glomus cells. J. Physiol. 548:789-800.
37. Pardal R, Ortega-Saenz P, Duran R, Lopez-Barneo J. 2007. Glia-like stem cells sustain physiologic neurogenesis in the adult mammalian carotid body. Cell 131:364-377.
38. Pascual A, et al. 2008. Absolute requirement of GDNF for adult catecholaminergic neuron survival. Nat. Neurosci. 11:755-761.
39. Perier C, Bove J, Vila M. 2012. Mitochondria and programmed cell death in Parkinson's disease: apoptosis and beyond. Antioxid. Redox Signal. 16:883-895.
40. Piruat JI, Pintado CO, Ortega-Saenz P, Roche M, Lopez-Barneo J. 2004. The mitochondrial SDHD gene is required for early embryogenesis, and its partial deficiency results in persistent carotid body glomus cell activation with full responsiveness to hypoxia. Mol. Cell. Biol. 24:10933-10940.
41. Pollard PJ, et al. 2005. Accumulation of Krebs cycle intermediates and over-expression of HIF1alpha in tumours which result from germline FH and SDH mutations. Hum. Mol. Genet. 14:2231-2239.
42. Ruan K, Song G, Ouyang G. 2009. Role of hypoxia in the hallmarks of human cancer. J. Cell Biochem. 107:1053-1062.
43. Rustin P, Munnich A, Rotig A. 2002. Succinate dehydrogenase and human diseases: new insights into a well-known enzyme. Eur. J. Hum. Genet. 10:289-291.
44. Santos JH, Mandavilli BS, Van Houten B. 2002. Measuring oxidative mtDNA damage and repair using quantitative PCR. Methods Mol. Biol. 197:159-176.
45. Sawada H, et al. 2007. Activated microglia affect the nigro-striatal dopamine neurons differently in neonatal and aged mice treated with 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. J. Neurosci. Res. 85:1752-1761.
46. Schapira AH. 2008. Mitochondrial dysfunction in neurodegenerative diseases. Neurochem. Res. 33:2502-2509.
47. Schapira AH, Jenner P. 2011. Etiology and pathogenesis of Parkinson's disease. Mov. Disord. 26:1049-1055.
48. Schapira AH, et al. 1992. Mitochondrial function in Parkinson's disease. The Royal Kings and Queens Parkinson's Disease Research Group. Ann. Neurol. 32(Suppl):S116 -S124.
49. Schon EA, Przedborski S. 2011. Mitochondria: the next (neurode)generation. Neuron 70:1033-1053.
50. Searle GJ, Hartness ME, Hoareau R, Peers C, Kemp PJ. 2002. Lack of contribution of mitochondrial electron transport to acute O2 sensing in model airway chemoreceptors. Biochem. Biophys. Res. Commun. 291: 332-337.
51. Selak MA, et al. 2005. Succinate links TCA cycle dysfunction to oncogenesis by inhibiting HIF-alpha prolyl hydroxylase. Cancer Cell 7:77-85.
52. Soriano P. 1999. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21:70-71.
53. Sulzer D. 2007. Multiple hit hypotheses for dopamine neuron loss in Parkinson's disease. Trends Neurosci. 30:244-250.
54. Tolosa E, Gaig C, Santamaria J, Compta Y. 2009. Diagnosis and the premotor phase of Parkinson disease. Neurology 72:S12-20.
55. Vila M, Ramonet D, Perier C. 2008. Mitochondrial alterations in Parkinson's disease: new clues. J. Neurochem. 107:317-328.
56. Villadiego J, et al. 2005. Selective glial cell line-derived neurotropic factor production in adult dopaminergic carotid body cells in situ and after intrastriatal transplantation. J. Neurosci. 25:4091-4098.
57. Wilcox CS, Pearlman A. 2008. Chemistry and antihypertensive effects of tempol and other nitroxides. Pharmacol. Rev. 60:418-469.
58. Yankovskaya V, et al. 2003. Architecture of succinate dehydrogenase and reactive oxygen species generation. Science 299:700-704.