PINK1 deficiency attenuates astrocyte proliferation through mitochondrial dysfunction, reduced AKT and increased p38 MAPK activation, and downregulation of EGFR

GLIA

Volumn 61, Issue 5, 2013, Pages 800-812

  Choi, Insup ^a   Kim, Jun ^a   Jeong, Hey Kyeong ^a   Kim, Beomsue ^a   Jou, Ilo ^a   Park, Myun ^a   Chen, Linan ^b   Kang, Un Jung ^b   Zhuang, Xiaoxi ^b   Joe, Eun hye ^a  

^a Ajou University School of Medicine   (South Korea)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

Astrocyte; Parkinson's disease; PINK1; Proliferation

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ADENOSINE TRIPHOSPHATE; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; GLUCOSE; MITOGEN ACTIVATED PROTEIN KINASE P38; OLIGOMYCIN; PHLORETIN; PHOSPHOTRANSFERASE; PROTEIN KINASE B; PTEN INDUCED PUTATIVE KINASE 1; REACTIVE OXYGEN METABOLITE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; EGFR PROTEIN, MOUSE; PROTEIN KINASE; PTEN-INDUCED PUTATIVE KINASE;

ANIMAL CELL; ARTICLE; ASTROCYTOSIS; CELL CULTURE; CELL LEVEL; CONTROLLED STUDY; COW; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME ACTIVATION; ENZYME DEFICIENCY; ENZYME INHIBITION; ENZYME SYNTHESIS; GENE SILENCING; GLUCOSE TRANSPORT; KNOCKOUT MOUSE; MASS; MEMBRANE POTENTIAL; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR DOWN REGULATION; SERUM; WOUND HEALING; 129 MOUSE; ANIMAL; ANTAGONISTS AND INHIBITORS; ASTROCYTE; BIOSYNTHESIS; BOVINAE; C57BL MOUSE; CELL PROLIFERATION; DEFICIENCY; DOWN REGULATION; GENETICS; METABOLISM; MITOCHONDRION; PATHOLOGY; UPREGULATION;

ANIMALS; ASTROCYTES; CATTLE; CELL PROLIFERATION; CELLS, CULTURED; DOWN-REGULATION; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIA; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROTEIN KINASES; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR, EPIDERMAL GROWTH FACTOR; UP-REGULATION;

EID: 84883168748     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22475     Document Type: Article

References (75)

1. Abramov AY, Gegg M, Grunewald A, Wood NW, Klein C, Schapira AH. Bioenergetic consequences of PINK1 mutations in Parkinson disease. PLoS One 2011;6:e25622.
2. Anderson CM, Swanson RA. Astrocyte glutamate transport: review of properties, regulation, and physiological functions. Glia 2000;32:1-14.
3. Bajetto A, Barbero S, Bonavia R, Piccioli P, Pirani P, Florio T, Schettini G. Stromal cell-derived factor-1alpha induces astrocyte proliferation through the activation of extracellular signal-regulated kinases 1/2 pathway. J Neurochem 2001;77:1226-1236.
4. Barbeito LH, Pehar M, Cassina P, Vargas MR, Peluffo H, Viera L, Estevez AG, Beckman JS. A role for astrocytes in motor neuron loss in amyotrophic lateral sclerosis. Brain Res Brain Res Rev 2004;47:263-274.
5. Beilina A, Van Der Brug M, Ahmad R, Kesavapany S, Miller DW, Petsko GA, Cookson MR. Mutations in PTEN-induced putative kinase 1 associated with recessive parkinsonism have differential effects on protein stability. Proc Natl Acad Sci USA 2005;102:5703-5708.
6. Boger HA, Middaugh LD, Zaman V, Hoffer B, Granholm AC. Differential effects of the dopamine neurotoxin MPTP in animals with a partial deletion of the GDNF receptor, GFR alpha1, gene. Brain Res 2008;1241:18-28.
7. Brown AM, Ransom BR. Astrocyte glycogen and brain energy metabolism. Glia 2007;55:1263-1271.
8. Bush TG, Puvanachandra N, Horner CH, Polito A, Ostenfeld T, Svendsen CN, Mucke L, Johnson MH, Sofroniew MV. Leukocyte infiltration, neuronal degeneration, and neurite outgrowth after ablation of scar-forming, reactive astrocytes in adult transgenic mice. Neuron 1999;23:297-308.
9. Chih CP, Roberts EL Jr. Energy substrates for neurons during neural activity: A critical review of the astrocyte-neuron lactate shuttle hypothesis. J Cereb Blood Flow Metab 2003;23:1263-1281.
10. Costa S, Planchenault T, Charriere-Bertrand C, Mouchel Y, Fages C, Juliano S, Lefrancois T, Barlovatz-Meimon G, Tardy M. Astroglial permissivity for neuritic outgrowth in neuron-astrocyte cocultures depends on regulation of laminin bioavailability. Glia 2002;37:105-113.
11. Coulter DA, Eid T. Astrocytic regulation of glutamate homeostasis in epilepsy. Glia 2012;60:1215-1226.
12. Dawson TM, Ko HS, Dawson VL. Genetic animal models of Parkinson's disease. Neuron 2010;66:646-661.
13. Demetrius L. Of mice and men. When it comes to studying ageing and the means to slow it down, mice are not just small humans. EMBO Rep 2005;6: 39-44.
14. Deng H, Jankovic J, Guo Y, Xie W, Le W. Small interfering RNA targeting the PINK1 induces apoptosis in dopaminergic cells SH-SY5Y. Biochem Biophys Res Commun 2005;337:1133-1138.
15. Faulkner JR, Herrmann JE, Woo MJ, Tansey KE, Doan NB, Sofroniew MV. Reactive astrocytes protect tissue and preserve function after spinal cord injury. J Neurosci 2004;24:2143-2155.
16. Fernandez-Gonzalez A, Perez-Otano I, Morgan JI. MPTP selectively induces haem oxygenase-1 expression in striatal astrocytes. Eur J Neurosci 2000;12: 1573-1583.
17. Ferrer I, Blanco R, Carmona M, Puig B, Barrachina M, Gomez C, Ambrosio S. Active, phosphorylation-dependent mitogen-activated protein kinase (MAPK/ ERK), stress-activated protein kinase/c-Jun N-terminal kinase (SAPK/JNK), and p38 kinase expression in Parkinson's disease and Dementia with Lewy bodies. J Neural Transm 2001;108:1383-1396.
18. Fougerousse F, Bullen P, Herasse M, Lindsay S, Richard I, Wilson D, Suel L, Durand M, Robson S, Abitbol M, Beckmann JS, Strachan T. Human-mouse differences in the embryonic expression patterns of developmental control genes and disease genes. Hum Mol Genet 2000;9:165-173.
19. Fraser MM, Zhu X, Kwon CH, Uhlmann EJ, Gutmann DH, Baker SJ. Pten loss causes hypertrophy and increased proliferation of astrocytes in vivo. Cancer Res 2004;64:7773-7779.
20. Frey MR, Dise RS, Edelblum KL, Polk DB. p38 kinase regulates epidermal growth factor receptor downregulation and cellular migration. EMBO J 2006; 25:5683-5692.
21. Gandhi S, Muqit MM, Stanyer L, Healy DG, Abou-Sleiman PM, Hargreaves I, Heales S, Ganguly M, Parsons L, Lees AJ. PINK1 protein in normal human brain and Parkinson's disease. Brain 2006;129:1720-1731.
22. Gandhi S, Wood-Kaczmar A, Yao Z, Plun-Favreau H, Deas E, Klupsch K, Downward J, Latchman DS, Tabrizi SJ, Wood NW. PINK1-associated Parkinson's disease is caused by neuronal vulnerability to calcium-induced cell death. Mol Cell 2009;33:627-638.
23. Ginis I, Luo Y, Miura T, Thies S, Brandenberger R, Gerecht-Nir S, Amit M, Hoke A, Carpenter MK, Itskovitz-Eldor J, Rao MS. Differences between human and mouse embryonic stem cells. Dev Biol 2004;269:360-380.
24. Gispert S, Ricciardi F, Kurz A, Azizov M, Hoepken HH, Becker D, Voos W, Leuner K, Muller WE, Kudin AP. Parkinson phenotype in aged PINK1- deficient mice is accompanied by progressive mitochondrial dysfunction in absence of neurodegeneration. PLoS One 2009;4:e5777.
25. Gross ER, Hsu AK, Gross GJ. The JAK/STAT pathway is essential for opioidinduced cardioprotection: JAK2 as a mediator of STAT3, Akt, and GSK-3 beta. Am J Physiol Heart Circ Physiol 2006;291:827-834.
26. Haque ME, Thomas KJ, D'Souza C, Callaghan S, Kitada T, Slack RS, Fraser P, Cookson MR, Tandon A, Park DS. Cytoplasmic Pink1 activity protects neurons from dopaminergic neurotoxin MPTP. Proc Natl Acad Sci USA 2008; 105:1716-1721.
27. Herrmann JE, Imura T, Song B, Qi J, Ao Y, Nguyen TK, Korsak RA, Takeda K, Akira S, Sofroniew MV. STAT3 is a critical regulator of astrogliosis and scar formation after spinal cord injury. J Neurosci 2008;28:7231-7243.
28. Hinterkeuser S, Schroder W, Hager G, Seifert G, Blumcke I, Elger CE, Schramm J, Steinhauser C. Astrocytes in the hippocampus of patients with temporal lobe epilepsy display changes in potassium conductances. Eur J Neurosci 2000;12:2087-2096.
29. Hu X, Chen J, Wang L, Ivashkiv LB. Crosstalk among Jak-STAT, Toll-like receptor, and ITAM-dependent pathways in macrophage activation. J Leukoc Biol 2007;82:237-243.
30. Ishikawa S, Taira T, Takahashi-Niki K, Niki T, Ariga H, Iguchi-Ariga SM. Human DJ-1-specific transcriptional activation of tyrosine hydroxylase gene. J Biol Chem 2010;285:39718-39731.
31. Karunakaran S, Saeed U, Mishra M, Valli RK, Joshi SD, Meka DP, Seth P, Ravindranath V. Selective activation of p38 mitogen-activated protein kinase in dopaminergic neurons of substantia nigra leads to nuclear translocation of p53 in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-treated mice. J Neurosci 2008;28:12500-12509.
32. Kim JH, Min KJ, Seol W, Jou I, Joe EH. Astrocytes in injury states rapidly produce anti-inflammatory factors and attenuate microglial inflammatory responses. J Neurochem 2010;115:1161-1171.
33. Kitada T, Pisani A, Porter DR, Yamaguchi H, Tscherter A, Martella G, Bonsi P, Zhang C, Pothos EN, Shen J. Impaired dopamine release and synaptic plasticity in the striatum of PINK1-deficient mice. Proc Natl Acad Sci USA 2007;104:11441-11446.
34. Kitada T, Tong Y, Gautier CA, Shen J. Absence of nigral degeneration in aged parkin/DJ-1/PINK1 triple knockout mice. J Neurochem 2009;111: 696-702.
35. Kohutnicka M, Lewandowska E, Kurkowska-Jastrzebska I, Czlonkowski A, Czlonkowska A. Microglial and astrocytic involvement in a murine model of Parkinson's disease induced by 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP). Immunopharmacology 1998;39:167-180.
36. Kojima A, Tator CH. Intrathecal administration of epidermal growth factor and fibroblast growth factor 2 promotes ependymal proliferation and functional recovery after spinal cord injury in adult rats. J Neurotrauma 2002; 19:223-238.
37. Larsen NJ, Ambrosi G, Mullett SJ, Berman SB, Hinkle DA. DJ-1 knock-down impairs astrocyte mitochondrial function. Neuroscience 2011;24:251-264.
38. Lin W, Kang UJ. Characterization of PINK1 processing, stability, and subcellular localization. J Neurochem 2008;106:464-474.
39. Lin W, Kang UJ. Structural determinants of PINK1 topology and dual subcellular distribution. BMC Cell Biol 2010;11:90.
40. Liu W, Vives-Bauza C, Acin-Perez R, Yamamoto A, Tan Y, Li Y, Magrane J, Stavarache MA, Shaffer S, Chang S. PINK1 defect causes mitochondrial dysfunction, proteasomal deficit and alpha-synuclein aggregation in cell culture models of Parkinson's disease. PLoS One 2009;4:e4597.
41. Ma M, Basso DM, Walters P, Stokes BT, Jakeman LB. Behavioral and histological outcomes following graded spinal cord contusion injury in the C57Bl/6 mouse. Exp Neurol 2001;169:239-254.
42. Mestas J, Hughes CC. Of mice and not men: differences between mouse and human immunology. J Immunol 2004;172:2731-2738.
43. Mills RD, Sim CH, Mok SS, Mulhern TD, Culvenor JG, Cheng HC. Biochemical aspects of the neuroprotective mechanism of PTEN-induced kinase-1 (PINK1). J Neurochem 2008;105:18-33.
44. Min KJ, Yang MS, Kim SU, Jou I, Joe EH. Astrocytes induce hemeoxygenase- 1 expression in microglia: A feasible mechanism for preventing excessive brain inflammation. J Neurosci 2006;26:1880-1887.
45. Mirza B, Hadberg H, Thomsen P, Moos T. The absence of reactive astrocytosis is indicative of a unique inflammatory process in Parkinson's disease. Neuroscience 2000;95:425-432.
46. Mullett SJ, Hinkle DA. DJ-1 knock-down in astrocytes impairs astrocytemediated neuroprotection against rotenone. Neurobiol Dis 2009;33:28-36.
47. Myer DJ, Gurkoff GG, Lee SM, Hovda DA, Sofroniew MV. Essential protective roles of reactive astrocytes in traumatic brain injury. Brain 2006; 129:2761-2772.
48. Pellerin L, Bouzier-Sore AK, Aubert A, Serres S, Merle M, Costalat R, Magistretti PJ. Activity-dependent regulation of energy metabolism by astrocytes: An update. Glia 2007;55:1251-1262.
49. Platanias LC. The p38 mitogen-activated protein kinase pathway and its role in interferon signaling. Pharmacol Ther 2003;98:129-142.
50. Rawlings JS, Rosler KM, Harrison DA. The JAK/STAT signaling pathway. J Cell Sci 2004;117:1281-1283.
51. Sarafian TA, Montes C, Imura T, Qi J, Coppola G, Geschwind DH, Sofroniew MV. Disruption of astrocyte STAT3 signaling decreases mitochondrial function and increases oxidative stress in vitro. PLoS One 2010;3:e9532.
52. Sim CH, Lio DS, Mok SS, Masters CL, Hill AF, Culvenor JG, Cheng HC. Cterminal truncation and Parkinson's disease-associated mutations downregulate the protein serine/threonine kinase activity of PTEN-induced kinase- 1. Hum Mol Genet 2006;15:3251-3262.
53. Simard M, Nedergaard M. The neurobiology of glia in the context of water and ion homeostasis. Neuroscience 2004;129:877-896.
54. Sofroniew MV. Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci 2009;32:638-647.
55. Solano RM, Casarejos MJ, Menéndez-Cuervo J, Rodriguez-Navarro JA, García de Yébenes J, Mena MA. Glial dysfunction in parkin null mice: effects of aging. J Neurosci 2008;28:598-611.
56. Song YJ, Halliday GM, Holton JL, Lashley T, O'Sullivan SS, McCann H, Lees AJ, Ozawa T, Williams DR, Lockhart PJ. Degeneration in different parkinsonian syndromes relates to astrocyte type and astrocyte protein expression. J Neuropathol Exp Neurol 2009;68:1073-1083.
57. Stromberg I, Bjorklund H, Dahl D, Jonsson G, Sundstrom E, Olson L. Astrocyte responses to dopaminergic denervations by 6-hydroxydopamine and 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine as evidenced by glial fibrillary acidic protein immunohistochemistry. Brain Res Bull 1986;17: 225-236.
58. Tain LS, Mortiboys H, Tao RN, Ziviani E, Bandmann O, Whitworth AJ. Rapamycin activation of 4E-BP prevents parkinsonian dopaminergic neuron loss. Nat Neurosci 2009;12:1129-1135.
59. Talbott JF, Loy DN, Liu Y, Qiu MS, Bunge MB, Rao MS, Whittemore SR. Endogenous Nkx2.2+;/Olig2+; oligodendrocyte precursor cells fail to remyelinate the demyelinated adult rat spinal cord in the absence of astrocytes. Exp Neurol 2005;192:11-24.
60. Tom VJ, Doller CM, Malouf AT, Silver J. Astrocyte-associated fibronectin is critical for axonal regeneration in adult white matter. J Neurosci 2004;24: 9282-9290.
61. Tsuda M, Kohro Y, Yano T, Tsujikawa T, Kitano J, Tozaki-Saitoh H, Koyanagi S, Ohdo S, Ji RR, Salter MW. JAK-STAT3 pathway regulates spinal astrocyte proliferation and neuropathic pain maintenance in rats. Brain 2011;134: 1127-1139.
62. Valente EM, Abou-Sleiman PM, Caputo V, Muqit MM, Harvey K, Gispert S, Ali Z, Del Turco D, Bentivoglio AR, Healy DG, Albanese A, Nussbaum R, González-Maldonado R, Deller T, Salvi S, Cortelli P, Gilks WP, Latchman DS, Harvey RJ, Dallapiccola B, Auburger G, Wood NW. Hereditary early-onset Parkinson's disease caused by mutations in PINK1. Science 2004;304: 1158-1160.
63. Valente EM, Bentivoglio AR, Dixon PH, Ferraris A, Ialongo T, Frontali M, Albanese A, Wood NW. Localization of a novel locus for autosomal recessive early-onset parkinsonism, PARK6, on human chromosome 1p35-p36. Am J Hum Genet 2001;68:895-900.
64. Vergarajauregui S, San Miguel A, Puertollano R. Activation of p38 mitogenactivated protein kinase promotes epidermal growth factor receptor internalization. Traffic 2006;7:686-698.
65. Voskuhl RR, Peterson RS, Song B, Ao Y, Morales LB, Tiwari-Woodruff S, Sofroniew MV. Reactive astrocytes form scar-like perivascular barriers to leukocytes during adaptive immune inflammation of the CNS. J Neurosci 2009;29:11511-11522.
66. Whetstone WD, Hsu JY, Eisenberg M, Werb Z, Noble-Haeusslein LJ. Bloodspinal cord barrier after spinal cord injury: Relation to revascularization and wound healing. J Neurosci Res 2003;74:227-239.
67. White RE, Jakeman LB. Don't fence me in: Harnessing the beneficial roles of astrocytes for spinal cord repair. Restor Neurol Neurosci 2008;26: 197-214.
68. Wilhelmus MM, van der Pol SM, Jansen Q, Witte ME, van der Valk P, Rozemuller AJ, Drukarch B, de Vries HE, Van Horssen J. Association of Parkinson disease-related protein PINK1 with Alzheimer disease and multiple sclerosis brain lesions. Free Radic Biol Med 2011;50:469-476.
69. Wilson JX. Antioxidant defense of the brain: A role for astrocytes. Can J Physiol Pharmacol 1997;75:1149-1163.
70. Xiong H, Wang D, Chen L, Choo YS, Ma H, Tang C, Xia K, Jiang W, Ronai Z, Zhuang X. Parkin, PINK1, and DJ-1 form a ubiquitin E3 ligase complex promoting unfolded protein degradation. J Clin Invest 2009;119:650-660.
71. Xu M, Bruchas MR, Ippolito DL, Gendron L, Chavkin C. Sciatic nerve ligationinduced proliferation of spinal cord astrocytes is mediated by kappa opioid activation of p38 mitogen-activated protein kinase. J Neurosci 2007;27: 2570-2581.
72. Yang MS, Min KJ, Joe E. Multiple mechanisms that prevent excessive brain inflammation. J Neurosci Res 2007;85:2298-2305.
73. Yao Z, Gandhi S, Burchell VS, Plun-Favreau H, Wood NW, Abramov AY. Cell metabolism affects selective vulnerability in PINK1-associated Parkinson's disease. J Cell Sci 2011;124:4194-4202.
74. Zhou C, Huang Y, Shao Y, May J, Prou D, Perier C, Dauer W, Schon EA, Przedborski S. The kinase domain of mitochondrial PINK1 faces the cytoplasm. Proc Natl Acad Sci USA 2008;105:12022-12027.
75. Zhou R, Yazdi AS, Menu P, Tschopp J. A role for mitochondria in NLRP3 inflammasome activation. Nature 2011;469:221-225.