Mitochondrial dysfunction driven by the LRRK2-mediated pathway is associated with loss of Purkinje cells and motor coordination deficits in diabetic rat model

Cell Death and Disease

Volumn 5, Issue 5, 2014, Pages

  Yang, S ^a   Xia, C ^a   Li, S ^a   Du, L ^a   Zhang, L ^a   Hu, Y ^a  

^a NANJING NORMAL UNIVERSITY   (China)

Author keywords

LRRK2; Mitochondria; Motor coordination deficit; Purkinje cell; Streptozotocin diabetic rat model

Indexed keywords

CHEMOKINE; CYTOKINE; DYNAMIN I; LEUCINE RICH REPEAT KINASE 2; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 2; MITOCHONDRIAL PROTEIN; PROTEIN P62; STREPTOZOCIN; TAU PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHAGOSOME; CEREBELLUM; CONTROLLED STUDY; DIABETIC NEUROPATHY; GENE OVEREXPRESSION; HYPERGLYCEMIA; IN VITRO STUDY; MITOCHONDRION; MOTOR COORDINATION; NERVE ENDING; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PURKINJE CELL; RAT; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; SWELLING;

ANIMALS; AUTOPHAGY; CELLS, CULTURED; CYTOKINES; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC NEUROPATHIES; DYNAMINS; HEAT-SHOCK PROTEINS; INFLAMMATION MEDIATORS; LYSOSOMAL-ASSOCIATED MEMBRANE PROTEIN 2; MICROTUBULE-ASSOCIATED PROTEINS; MITOCHONDRIA; MOTOR ACTIVITY; NERVE DEGENERATION; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PURKINJE CELLS; RATS; RATS, WISTAR; ROTAROD PERFORMANCE TEST; SIGNAL TRANSDUCTION; TAU PROTEINS; TIME FACTORS; TRANSFECTION;

EID: 84901017315     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2014.184     Document Type: Article

References (49)

1. Roman de Mettelinge T, Delbaere K, Calders P, Gysel T, Van Den Noortgate N, Cambier D. The impact of peripheral neuropathy and cognitive decrements on gait in older adults with type 2 diabetes mellitus. Arch Phys Med Rehabil 2013; 94: 1074-1079.
2. Di Domenico F, Sultana R, Ferree A, Smith K, Barone E, Perluigi M et al. Redox proteomics analyses of the influence of co-expression of wild-type or mutated LRRK2 and Tau on C. elegans protein expression and oxidative modification: Relevance to Parkinson disease. Antioxid Redox Signal 2012; 17: 1490-1506.
3. Lin CH, Tsai PI, Wu RM, Chien CT. LRRK2 G2019S mutation induces dendrite degeneration through mislocalization and phosphorylation of tau by recruiting autoactivated GSK3ss. J Neurosci 2010; 30: 13138-13149.
4. Melrose HL, Dachsel JC, Behrouz B, Lincoln SJ, Yue M, Hinkle KM et al. Impaired dopaminergic neurotransmission and microtubule-associated protein tau alterations in human LRRK2 transgenic mice. Neurobiol Dis 2010; 40: 503-517.
5. Miklossy J, Qing H, Guo JP, Yu S, Wszolek ZK, Calne D et al. Lrrk2 and chronic inflammation are linked to pallido-ponto-nigral degeneration caused by the N279K tau mutation. Acta Neuropathol 2007; 114: 243-254.
6. Kawakami F, Yabata T, Ohta E, Maekawa T, Shimada N, Suzuki M et al. LRRK2 phosphorylates tubulin-associated tau but not the free molecule: LRRK2-mediated regulation of the tau-tubulin association and neurite outgrowth. PLoS One 2012; 7: e30834.
7. Braun AP. Convergent signaling events underlie dopamine-mediated inhibition of CaV3.2 T-type calcium channels. Channels 2009; 3: 381-382.
8. Sarantis K, Matsokis N, Angelatou F. Synergistic interactions of dopamine D1 and glutamate NMDA receptors in rat hippocampus and prefrontal cortex: involvement of ERK1/2 signaling. Neuroscience 2009; 163: 1135-1145.
9. Lebel M, Patenaude C, Allyson J, Massicotte G, Cyr M. Dopamine D1 receptor activation induces tau phosphorylation via cdk5 and GSK3 signaling pathways. Neuropharmacology 2009; 57: 392-402.
10. Kim YS, Shin JH, Hall FS, Linden DJ. Dopamine signaling is required for depolarizationinduced slow current in cerebellar Purkinje cells. J Neurosci 2009; 29: 8530-8538.
11. Vincent AM, Callaghan BC, Smith AL, Feldman EL. Diabetic neuropathy: Cellular mechanisms as therapeutic targets. Nat Rev Neurol 7: 573-583.
12. Chen PC Lao CL, Chen JC. The D(3) dopamine receptor inhibits dopamine release in PC-12/hD3 cells by autoreceptor signaling via PP-2B, CK1, and Cdk-5. J Neurochem 2009; 110: 1180-1190.
13. Manschot SM, Biessels GJ, de Valk H, Algra A, Rutten GE, van der Grond J et al. Metabolic and vascular determinants of impaired cognitive performance and abnormalities on brain magnetic resonance imaging in patients with type 2 diabetes. Diabetologia 2007; 50: 2388-2397.
14. Selvarajah D, Wilkinson ID, Davies J, Gandhi R, Tesfaye S. Central nervous system involvement in diabetic neuropathy. Curr Diab Rep 2011; 11: 310-322.
15. Melrose HL, Kinloch RA, Cox PJ, Field MJ, Collins D, Williams D. [3H] pregabalin binding is increased in ipsilateral dorsal horn following chronic constriction injury. Neurosci Lett 2007; 417: 187-192.
16. Drolet RE, Sanders JM, Kern JT. Leucine-rich repeat kinase 2 (LRRK2) cellular biology: A review of recent advances in identifying physiological substrates and cellular functions. J Neurogenet 25: 140-151.
17. Gomez-Suaga P, Fdez E, Blanca Ramirez M, Hilfiker S. A link between autophagy and the pathophysiology of LRRK2 in Parkinson's disease. Parkinsons Dis 2012; 2012: 324521.
18. Gomez-Suaga P, Luzon-Toro B, Churamani D, Zhang L, Bloor-Young D, Patel S et al. Leucine-rich repeat kinase 2 regulates autophagy through a calcium-dependent pathway involving NAADP. Hum Mol Genet 2012; 21: 511-525.
19. Drolet RE, Sanders JM, Kern JT. Leucine-rich repeat kinase 2 (LRRK2) cellular biology: A review of recent advances in identifying physiological substrates and cellular functions. J Neurogenet 2011; 25: 140-151.
20. Greggio E, Cookson MR. Leucine-rich repeat kinase 2 mutations and Parkinson's disease: three questions. ASN Neuro 2009; 1: e00002.
21. Shin YK, Jang SY, Lee HK, Jung J, Suh DJ, Seo SY et al. Pathological adaptive responses of Schwann cells to endoplasmic reticulum stress in bortezomib-induced peripheral neuropathy. Glia 2010; 58: 1961-1976.
22. Locke S. Axons, Schwann cells, and diabetic neuropathy. Bull NY Acad Med 1967; 43: 784-791.
23. McCandless DW, Feussner GK, Lust WD, Passonneau JV. Sparing of metabolic stress in Purkinje cells after maximal electroshock. Proc Natl Acad Sci USA 1979; 76: 1482-1484.
24. MacKenzie-Graham A, Tiwari-Woodruff SK, Sharma G, Aguilar C, Vo KT, Strickland LV et al. Purkinje cell loss in experimental autoimmune encephalomyelitis. Neuroimage 2009; 48: 637-651.
25. Sudarov A. Defining the role of cerebellar purkinje cells in autism spectrum disorders. Cerebellum 2013; 12: 950-955.
26. Kasumu A, Bezprozvanny I. Deranged calcium signaling in Purkinje cells and pathogenesis in spinocerebellar ataxia 2 (SCA2) and other ataxias. Cerebellum 2012; 11: 630-639.
27. Wang QJ, Ding Y, Kohtz DS, Mizushima N, Cristea IM, Rout MP et al. Induction of autophagy in axonal dystrophy and degeneration. J Neurosci 2006; 26: 8057-8068.
28. Komatsu M, Waguri S, Chiba T, Murata S, Iwata J, Tanida I et al. Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 2006; 441: 880-884.
29. Jiang YQ, Wang XL, Cao XH, Ye ZY, Li L, Cai WQ. Increased heat shock transcription factor 1 in the cerebellum reverses the deficiency of Purkinje cells in Alzheimer's disease. Brain Res 2013; 1519: 105-111.
30. Rajput AH, Robinson CA, Rajput ML, Rajput A. Cerebellar Purkinje cell loss is not pathognomonic of essential tremor. Parkinsonism Relat Disord 2011; 17: 16-21.
31. Chan L, Terashima T, Urabe H, Lin F, Kojima H. Pathogenesis of diabetic neuropathy: Bad to the bone. Ann NY Acad Sci 2011; 1240: 70-76.
32. Weimann JM, Johansson CB, Trejo A, Blau HM. Stable reprogrammed heterokaryons form spontaneously in Purkinje neurons after bone marrow transplant. Nat Cell Biol 2003; 5: 959-966.
33. Wei M, Ong L, Smith MT, Ross FB, Schmid K, Hoey AJ et al. The streptozotocin-diabetic rat as a model of the chronic complications of human diabetes. Heart Lung Circ 2003; 12: 44-50.
34. Nishi A. [Role of Cdk5 in dopamine signaling and addiction]. Tanpakushitsu Kakusan Koso 2009; 54: 813-819.
35. Chakrabarti L, Eng J, Ivanov N, Garden GA, La Spada AR. Autophagy activation and enhanced mitophagy characterize the Purkinje cells of pcd mice prior to neuronal death. Mol Brain 2009; 2: 24.
36. Plowey ED, Cherra 3rd SJ, Liu YJ, Chu CT. Role of autophagy in G2019S-LRRK2- associated neurite shortening in differentiated SH-SY5Y cells. J Neurochem 2008; 105: 1048-1056.
37. Kawakami F, Yabata T, Ohta E, Maekawa T, Shimada N, Suzuki M et al. LRRK2 phosphorylates tubulin-associated tau but not the free molecule: LRRK2-mediated regulation of the tau-tubulin association and neurite outgrowth. PLoS One 7: e30834.
38. Wang X, Yan MH, Fujioka H, Liu J, Wilson-Delfosse A, Chen SG et al. LRRK2 regulates mitochondrial dynamics and function through direct interaction with DLP1. Hum Mol Genet 2012; 21: 1931-1944.
39. Yamano T, Shimada M, Fujizeki Y, Kawasaki H, Onaga A. Quantitative synaptic changes on Purkinje cell dendritic spines of rats born from streptozotocin-induced diabetic mothers. Brain Dev 1986; 8: 269-273.
40. Saha S, Liu-Yesucevitz L, Wolozin B. Regulation of Autophagy by LRRK2 in Caenorhabditis elegans. Neurodegener Dis 2014; 13: 110-113.
41. Avila J, Lucas JJ, Perez M, Hernandez F. Role of tau protein in both physiological and pathological conditions. Physiol Rev 2004; 84: 361-384.
42. Zhang Y, Tian Q, Zhang Q, Zhou X, Liu S, Wang JZ. Hyperphosphorylation of microtubuleassociated tau protein plays dual role in neurodegeneration and neuroprotection. Pathophysiol 2009; 16: 311-316.
43. Kageyama Y, Zhang Z, Roda R, Fukaya M, Wakabayashi J, Wakabayashi N et al. Mitochondrial division ensures the survival of postmitotic neurons by suppressing oxidative damage. J Cell Biol 197: 535-551.
44. Cameron NE. Role of endoplasmic reticulum stress in diabetic neuropathy. Diabetes 62: 696-697.
45. Portha B, Picon L, Rosselin G. Chemical diabetes in the adult rat as the spontaneous evolution of neonatal diabetes. Diabetologia 1979; 17: 371-377.
46. Blondel O, Bailbe D, Portha B. Relation of insulin deficiency to impaired insulin action in NIDDM adult rats given streptozocin as neonates. Diabetes 1989; 38: 610-617.
47. Heffner TG, Hartman JA, Seiden LS. A rapid method for the regional dissection of the rat brain. Pharmacol Biochem Behav 1980; 13: 453-456.
48. Taymans JM, Van den Haute C, Baekelandt V. Distribution of PINK1 and LRRK2 in rat and mouse brain. J Neurochem 2006; 98: 951-961.
49. Harris KM, Stevens JK. Dendritic spines of rat cerebellar Purkinje cells: serial electron microscopy with reference to their biophysical characteristics. J Neurosci 1988; 8: 4455-4469.