Neurotoxin-induced ER stress in mouse dopaminergic neurons involves downregulation of TRPC1 and inhibition of AKT/mTOR signaling

Journal of Clinical Investigation

Volumn 122, Issue 4, 2012, Pages 1354-1367

  Selvaraj, Senthil ^a   Sun, Yuyang ^a   Watt, John A ^a   Wang, Shouping ^a   Lei, Saobo ^a   Birnbaumer, Lutz ^b   Singh, Brij B ^a  

^a UNIVERSITY OF NORTH DAKOTA SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^b NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; MAMMALIAN TARGET OF RAPAMYCIN; NEUROTOXIN; PROTEIN KINASE B; STROMAL INTERACTION MOLECULE 1; TRANSIENT RECEPTOR POTENTIAL CHANNEL 1;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM HOMEOSTASIS; CANCER CELL CULTURE; CELL LOSS; CELL LYSATE; CELL SURVIVAL; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DOWN REGULATION; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVITY; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; INTRACELLULAR SIGNALING; MALE; MOUSE; NEUROBLASTOMA CELL; NEUROPROTECTION; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SUBSTANTIA NIGRA; TUMOR CELL LINE; UNFOLDED PROTEIN RESPONSE;

1-METHYL-4-PHENYL-1,2,3,6-TETRAHYDROPYRIDINE; ANIMALS; BRAIN CHEMISTRY; CALCIUM SIGNALING; CELL LINE, TUMOR; DOPAMINERGIC NEURONS; DOWN-REGULATION; ENDOPLASMIC RETICULUM STRESS; HUMANS; MALE; MEMBRANE GLYCOPROTEINS; MICE; NERVE TISSUE PROTEINS; NEUROBLASTOMA; PARKINSONIAN DISORDERS; PROTO-ONCOGENE PROTEINS C-AKT; RNA INTERFERENCE; RNA, SMALL INTERFERING; SUBSTANTIA NIGRA; TOR SERINE-THREONINE KINASES; TRPC CATION CHANNELS; UNFOLDED PROTEIN RESPONSE;

EID: 84859717205     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI61332     Document Type: Article

References (60)

1. Dauer W, Przedborski S. Parkinson's disease: mechanisms and models. Neuron. 2003;39(6):889-909. (Pubitemid 37130207)
2. Marras C, Lang A. changing concepts in Parkinson disease: moving beyond the decade of the brain. Neurology. 2008;70(21):1996-2003.
3. Abou-Sleiman PM, Muqit MM, Wood NW. Expanding insights of mitochondrial dysfunction in Parkinson's disease. Nat Rev Neurosci. 2006;7(3):207-219. (Pubitemid 43292466)
4. Chan CS, et al. 'Rejuvenation' protects neurons in mouse models of Parkinson's disease. Nature. 2007;447(7148):1081-1086. (Pubitemid 47014425)
5. Bezprozvanny I. Calcium signaling and neurodegenerative diseases. Trends Mol Med. 2009;15(3):89-100.
6. Balch WE, Morimoto RI, Dillin A, Kelly JW. Adapting proteostasis for disease intervention. Science. 2008;319(5865):916-919. (Pubitemid 351263754)
7. Paschen W, Mengesdorf T. Endoplasmic reticulum stress response and neurodegeneration. Cell Calcium. 2005;38(3-4):409-415. (Pubitemid 41283279)
8. Hiller MM, Finger A, Schweiger M, Wolf DH. ER degradation of a misfolded luminal protein by the cytosolic ubiquitin-proteasome pathway. Science. 1996;273(5282):1725-1728. (Pubitemid 26317791)
9. Boyce M, Yuan J. Cellular response to endoplasmic reticulum stress: a matter of life or death. Cell Death Differ. 2006;13(3):363-373.
10. Harding HP, Calfon M, Urano F, Novoa I, Ron D. Transcriptional and translational control in the Mammalian unfolded protein response. Annu Rev Cell Dev Biol. 2002;18:575-599. (Pubitemid 35387362)
11. Chiba K, Trevor A, Castagnoli N Jr. Metabolism of the neurotoxic tertiary amine, MPTP, by brain monoamine oxidase. Biochem Biophys Res Commun. 1984;120(2):574-578. (Pubitemid 14101750)
12. Przedborski S, Tieu K, Perier C, Vila M. MPTP as a mitochondrial neurotoxic model of Parkinson's disease. J Bioenerg Biomembr. 2004;36(4):375-379. (Pubitemid 39619844)
13. Kitahama K, Denney RM, Maeda T, Jouvet M. Distribution of type B monoamine oxidase immunoreactivity in the cat brain with reference to enzyme histochemistry. NeuroScience. 1991;44(1):185-204.
14. Lotharius J, Dugan LL, O'Malley KL. Distinct mechanisms underlie neurotoxin-mediated cell death in cultured dopaminergic neurons. J Neurosci. 1999;19(4):1284-1293. (Pubitemid 29088911)
15. Javitch JA, D'Amato RJ, Strittmatter SM, Snyder SH. Parkinsonism-inducing neurotoxin, N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine: uptake of the metabolite N-methyl-4-phenylpyridine by dopamine neurons explains selective toxicity. Proc Natl Acad Sci U S A. 1985;82(7):2173-2177. (Pubitemid 15056491)
16. Holtz WA, O'Malley KL. Parkinsonian mimetics induce aspects of unfolded protein response in death of dopaminergic neurons. J Biol Chem. 2003;278(21):19367-19377. (Pubitemid 36799332)
17. Hoozemans JJ, van Haastert ES, Eikelenboom P, de Vos RA, Rozemuller JM, Scheper W. Activation of the unfolded protein response in Parkinson's disease. Biochem Biophys Res Commun. 2007;354(3):707-711. (Pubitemid 46186242)
18. Bollimuntha S, Singh BB, Shavali S, Sharma SK, Ebadi M. TRPC1-mediated inhibition of 1-methyl-4-phenylpyridinium ion neurotoxicity in human SH-SY5Y neuroblastoma cells. J Biol Chem. 2005;280(3):2132-2140.
19. Selvaraj S, Watt JA, Singh BB. TRPC1 inhibits apoptotic cell degeneration induced by dopaminergic neurotoxin MPTP/MPP(+). Cell Calcium. 2009;46(3):209-218.
20. Montell C. Physiology, phylogeny, and functions of the TRP superfamily of cation channels. Sci STKE. 2001;2001(90):re1.
21. Liao Y, Erxleben C, Yildirim E, Abramowitz J, Armstrong DL, Birnbaumer L. Orai proteins interact with TRPC channels and confer responsiveness to store depletion. Proc Natl Acad Sci U S A. 2007;104(11):4682-4687. (Pubitemid 47186285)
22. 2+ concentrations. Annu Rev Pharmacol Toxicol. 2009;49:395-426.
23. Putney JW. Physiological mechanisms of TRPC activation. Pflugers Arch. 2005;451(1):29-34. (Pubitemid 41424904)
24. Cahalan MD. STIMulating store-operated Ca(2+) entry. Nat Cell Biol. 2009;11(6):669-677.
25. Parekh AB, Penner R. Store depletion and calcium influx. Physiol Rev. 1997;77(4):901-930. (Pubitemid 27459576)
26. Liu X, et al. Attenuation of store-operated Ca2+ current impairs salivary gland fluid secretion in TRPC1(-/-) mice. Proc Natl Acad Sci U S A. 2007; 104(44):17542-17547. (Pubitemid 350219874)
27. Yuan JP, Zeng W, Dorwart MR, Choi YJ, Worley PF, Muallem S. SOAR and the polybasic STIM1 domains gate and regulate Orai channels. Nat Cell Biol. 2009;11(3):337-343.
28. Wang Y, Deng X, Gill DL. Calcium signaling by STIM and Orai: intimate coupling details revealed. SciSignal. 2010;3(148):pe42.
29. 2+ entry. Proc Natl Acad Sci U S A. 2009;106(9):3202-3206.
30. Riccio A, et al. mRNA distribution analysis of human TRPC family in CNS and peripheral tissues. Brain Res Mol Brain Res. 2002;109(1-2):95-104. (Pubitemid 36082877)
31. Liu CY, Kaufman RJ. The unfolded protein response. J Cell Sci. 2003;116(pt 10):1861-1862. (Pubitemid 36622284)
32. 2+ channels. J Biol Chem. 2003;278(13):11337-11343.
33. Salinas M, Martin D, Alvarez A, Cuadrado A. Akt1/PKBalpha protects PC12 cells against the parkinsonism- inducing neurotoxin 1-methyl-4-phenyl-pyridinium and reduces the levels of oxygen-free radicals. Mol Cell Neurosci. 2001;17(1):67-77. (Pubitemid 32113539)
34. Hofmann T, Obukhov AG, Schaefer M, Harteneck C, Gudermann T, Schultz G. Direct activation of human TRPC6 and TRPC3 channels by diacylglycerol. Nature. 1999;397(6716):259-263.
35. Mattson MP. ER calcium and Alzheimer's disease: in a state of flux. Sci Signal. 2010;3(114):pe10.
36. Nguyen HN, Wang C, Perry DC. Depletion of intracellular calcium stores is toxic to SH-SY5Y neuronal cells. Brain Res. 2002;924(2):159-166. (Pubitemid 34102304)
37. Rizzuto R, et al. Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2+ responses. Science. 1998;280(5370):1763-1766. (Pubitemid 28283502)
38. Chigurupati S, et al. The homocysteine-inducible endoplasmic reticulum stress protein counteracts calcium store depletion and induction of CCAAT enhancer-binding protein homologous protein in a neurotoxin model of Parkinson disease. J Biol Chem. 2009;284(27):18323-18333.
39. Brandman O, Liou J, Park WS, Meyer T. STIM2 is a feedback regulator that stabilizes basal cytosolic and endoplasmic reticulum Ca2+ levels. Cell. 2007;131(7):1327-1339. (Pubitemid 350297421)
40. 2+ entry depends on mitochondrial Ca2+ uptake. EMBO J. 2002;21(24):6744-6754.
41. Hoth M, Button DC, Lewis RS. Mitochondrial control of calcium-channel gating: a mechanism for sustained signaling and transcriptional activation in T lymphocytes. Proc Natl Acad Sci U S A. 2000;97(19):10607-10612.
42. 2+ influx. Curr Biol. 2005;15(13):1235-1241.
43. Lewis RS. The molecular choreography of a store-operated calcium channel. Nature. 2007; 446(7133):284-287. (Pubitemid 46426160)
44. Park CY, Shcheglovitov A, Dolmetsch R. The CRAC channel activator STIM1 binds and inhibits L-type voltage-gated calcium channels. Science. 2010;330(6000):101-105.
45. Wang Y, et al. The calcium store sensor, STIM1, reciprocally controls Orai and CaV1.2 channels. Science. 2010;330(6000):105-109.
46. Chan CS, et al. Rejuvenation' protects neurons in mouse models of Parkinson's disease. Nature. 2007;447(7148):1081-1086. (Pubitemid 47014425)
47. Wang GX, Poo MM. Requirement of TRPC channels in netrin-1-induced chemotropic turning of nerve growth cones. Nature. 2005;434(7035):898-904. (Pubitemid 40559002)
48. Talavera K, Nilius B, Voets T. Neuronal TRP channels: thermometers, pathfinders and life-savers. Trends Neurosci. 2008;31(6):287-295.
49. Yao H, et al. Involvement of TRPC channels in CCL2-mediated neuroprotection against tat toxicity. J Neurosci. 2009;29(6):1657-1669.
50. Inoue H, et al. Inhibition of the leucine-rich repeat protein LINGO-1 enhances survival, structure, and function of dopaminergic neurons in Parkinson's disease models. Proc Natl Acad Sci U S A. 2007;104(36):14430-14435. (Pubitemid 350003278)
51. Malagelada C, Jin ZH, Jackson-Lewis V, Przedborski S, Greene LA. Rapamycin protects against neuron death in in vitro and in vivo models of Parkinson's disease. J Neurosci. 2010;30(3):1166-1175.
52. Cross DA, Alessi DR, Cohen P, Andjelkovich M, Hemmings BA. Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature. 1995;378(6559):785-789. (Pubitemid 26004411)
53. Brunet A, Datta SR, Greenberg ME. Transcription-dependent and -independent control of neuronal survival by the PI3K-Akt signaling pathway. Curr Opin Neurobiol. 2001;11(3):297-305. (Pubitemid 32524094)
54. del Peso L, Gonzalez-Garcia M, Page C, Herrera R, Nunez G. Interleukin-3-induced phosphorylation of BAD through the protein kinase Akt. Science. 1997;278(5338):687-689. (Pubitemid 27464966)
55. Di Nardo A, et al. Tuberous sclerosis complex activity is required to control neuronal stress responses in an mTOR-dependent manner. J Neurosci. 2009;29(18):5926-5937.
56. Malagelada C, Jin ZH, Greene LA. RTP801 is induced in Parkinson's disease and mediates neuron death by inhibiting Akt phosphorylation /activation. J Neurosci. 2008;28(53):14363-14371.
57. Deguil J, Chavant F, Lafay-Chebassier C, Pérault-Pochat MC, Fauconneau B, Pain S. Neuroprotective effect of PACAP on translational control alteration and cognitive decline in MPTP parkinsonian mice. Neurotox Res. 2010;17(2):142-155.
58. Pani B, et al. Activation of TRPC1 by STIM1 in ERPM microdomains involves release of the channel from its scaffold caveolin-1. Proc Natl Acad Sci U S A. 2009;106(47):20087-20092.
59. Ong HL, et al. Dynamic assembly of TRPC1-STIM1-Orai1 ternary complex is involved in store-operated calcium influx. J Biol Chem. 2007;282(12):9105-9116.
60. Hoehn M, Yahr M. Parkinsonism: onset, progression and mortality. Neurology. 1967;17(5):427-442.