Rapamycin activates autophagy and improves myelination in explant cultures from neuropathic mice

Journal of Neuroscience

Volumn 30, Issue 34, 2010, Pages 11388-11397

  Rangaraju, Sunitha ^a   Verrier, Jonathan D ^a   Madorsky, Irina ^a   Nicks, Jessica ^a   Dunn Jr , William A ^b   Notterpek, Lucia ^a,b  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOPHAGY PROTEIN 12; AUTOPHAGY PROTEIN 5; MYELIN; MYELIN PROTEIN; PERIPHERAL MYELIN PROTEIN 22; POLYUBIQUITIN; RAPAMYCIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHAGY; CONTROLLED STUDY; DOSE TIME EFFECT RELATION; EXPLANT; GENOTYPE; LOCOMOTION; MALE; MOTOR PERFORMANCE; MOUSE; MYELINATION; NEUROPATHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCHWANN CELL; SPINAL GANGLION;

ANIMALS; AUTOPHAGY; DEMYELINATING DISEASES; FEMALE; GENE KNOCKDOWN TECHNIQUES; MALE; MICE; MICE, NEUROLOGIC MUTANTS; MYELIN SHEATH; NERVE FIBERS, MYELINATED; NEURALGIA; ORGAN CULTURE TECHNIQUES; SIROLIMUS;

EID: 77956124566     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1356-10.2010     Document Type: Article

References (58)

1. Amici SA, Dunn WA Jr, Notterpek L (2007) Developmental abnormalities in the nerves of peripheral myelin protein 22-deficient mice. J Neurosci Res 85:238-249.
2. Archelos JJ, Roggenbuck K, Schneider-Schaulies J, Linington C, Toyka KV, Hartung HP (1993) Production and characterization of monoclonal antibodies to the extracellular domain of P0. J Neurosci Res 35:46-53. (Pubitemid 23143631)
3. Bolis A, Coviello S, Visigalli I, Taveggia C, Bachi A, Chishti AH, Hanada T, Quattrini A, Previtali SC, Biffi A, Bolino A (2009) Dlg1, Sec8, and Mtmr2 regulate membrane homeostasis in Schwann cell myelination. J Neurosci 29:8858-8870.
4. Caccamo A, Majumder S, Richardson A, Strong R, Oddo S (2010) Molecular interplay between mammalian target of rapamycin (mTOR), amyloid-beta, and Tau: effects on cognitive impairments. J Biol Chem 285:13107-13120.
5. Dreux M, Gastaminza P, Wieland SF, Chisari FV (2009) The autophagy machinery is required to initiate hepatitis C virus replication. Proc Natl Acad Sci U S A 106:14046-14051.
6. Einheber S, Milner TA, Giancotti F, Salzer JL (1993) Axonal regulation of Schwann cell integrin expression suggests a role for alpha 6 beta 4 in myelination. J Cell Biol 123:1223-1236. (Pubitemid 23352430)
7. Eldridge CF, Bunge MB, Bunge RP, Wood PM (1987) Differentiation of axon-related Schwann cells in vitro. I. Ascorbic acid regulates basal lamina assembly and myelin formation. J Cell Biol 105:1023-1034.
8. Fortun J, Dunn WA Jr, Joy S, Li J, Notterpek L (2003) Emerging role for autophagy in the removal of aggresomes in Schwann cells. J Neurosci 23:10672-10680. (Pubitemid 37485281)
9. Fortun J, Li J, Go J, Fenstermaker A, Fletcher BS, Notterpek L (2005) Impaired proteasome activity and accumulation of ubiquitinated substrates in a hereditary neuropathy model. J Neurochem 92:1531-1541. (Pubitemid 40389221)
10. Fortun J, Go JC, Li J, Amici SA, Dunn WA Jr, Notterpek L (2006) Alterations in degradative pathways and protein aggregation in a neuropathy model based on PMP22 overexpression. Neurobiol Dis 22:153-164.
11. Fortun J, Verrier JD, Go JC, Madorsky I, Dunn WA, Notterpek L (2007) The formation of peripheral myelin protein 22 aggregates is hindered by the enhancement of autophagy and expression of cytoplasmic chaperones. Neurobiol Dis 25:252-265. (Pubitemid 46124007)
12. Foster DA, Toschi A (2009) Targeting mTOR with rapamycin: one dose does not fit all. Cell Cycle 8:1026-1029.
13. Harrison DE, Strong R, Sharp ZD, Nelson JF, Astle CM, Flurkey K, Nadon NL, Wilkinson JE, Frenkel K, Carter CS, Pahor M, Javors MA, Fernandez E, Miller RA (2009) Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature 460:392-395.
14. Hartung HP, Jung S, Stoll G, Zielasek J, Schmidt B, Archelos JJ, Toyka KV (1992) Inflammatory mediators in demyelinating disorders of the CNS and PNS. J Neuroimmunol 40:197-210.
15. Hasse B, Bosse F, Hanenberg H, Müller HW (2004) Peripheral myelin protein 22 kDa and protein zero: domain specific trans-interactions. Mol Cell Neurosci 27:370-378. (Pubitemid 39539992)
16. Huxley C, Passage E, Manson A, Putzu G, Figarella-Branger D, Pellissier JF, Fontés M (1996) Construction of a mouse model of Charcot-Marie-Tooth disease type 1A by pronuclear injection of human YAC DNA. Hum Mol Genet 5:563-569. (Pubitemid 26141268)
17. Huxley C, Passage E, Robertson AM, Youl B, Huston S, Manson A, Sabéran- Djoniedi D, Figarella-Branger D, Pellissier JF, Thomas PK, Fontés M (1998) Correlation between varying levels of PMP22 expression and the degree of demyelination and reduction in nerve conduction velocity in transgenic mice. Hum Mol Genet 7:449-458. (Pubitemid 28120635)
18. Jaeger PA, Wyss-Coray T (2009) All-you-can-eat: autophagy in neurodegeneration and neuroprotection. Mol Neurodegener 4:16.
19. Kahan BD (2008) Fifteen years of clinical studies and clinical practice in renal transplantation: reviewing outcomes with de novo use of sirolimus in combination with cyclosporine. Transplant Proc 40:S17-20.
20. King MA, Hands S, Hafiz F, Mizushima N, Tolkovsky AM, Wyttenbach A (2008) Rapamycin inhibits polyglutamine aggregation independently of autophagy by reducing protein synthesis. Mol Pharmacol 73:1052-1063.
21. Komatsu M, Ichimura Y (2010) Physiological significance of selective degradation of p62 by autophagy. FEBS Lett 584:1374-1378.
22. Komatsu M, Waguri S, Chiba T, Murata S, Iwata J, Tanida I, Ueno T, Koike M, Uchiyama Y, Kominami E, Tanaka K (2006) Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 441:880-884.
23. Kuhn G, Lie A, Wilms S, Müller HW (1993) Coexpression of PMP22 gene with MBP and P0 during de novo myelination and nerve repair. Glia 8:256-264.
24. Li Y, Tennekoon GI, Birnbaum M, Marchionni MA, Rutkowski JL (2001) Neuregulin signaling through a PI3K/Akt/Bad pathway in Schwann cell survival. Mol Cell Neurosci 17:761-767.
25. Madorsky I, Opalach K, Waber A, Verrier JD, Solmo C, Foster T, Dunn WA Jr, Notterpek L (2009) Intermittent fasting alleviates the neuropathic phenotype in a mouse model of Charcot-Marie-Tooth disease. Neurobiol Dis 34:146-154.
26. Maiuri MC, Zalckvar E, Kimchi A, Kroemer G (2007) Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat Rev Mol Cell Biol 8:741-752.
27. Malagelada C, Jin ZH, Jackson-Lewis V, Przedborski S, Greene LA (2010) Rapamycin protects against neuron death in in vitro and in vivo models of Parkinson's disease. J Neurosci 30:1166-1175.
28. Meikle L, Pollizzi K, Egnor A, Kramvis I, Lane H, Sahin M, Kwiatkowski DJ (2008) Response of a neuronal model of tuberous sclerosis to mammalian target of rapamycin (mTOR) inhibitors: effects on mTORC1 and Akt signaling lead to improved survival and function. J Neurosci 28:5422-5432.
29. Menzies FM, Huebener J, Renna M, Bonin M, Riess O, Rubinsztein DC (2010) Autophagy induction reduces mutant ataxin-3 levels and toxicity in a mouse model of spinocerebellar ataxia type 3. Brain 133:93-104.
30. Micallef J, Attarian S, Dubourg O, Gonnaud PM, Hogrel JY, Stojkovic T, Bernard R, Jouve E, Pitel S, Vacherot F, Remec JF, Jomir L, Azabou E, Al-Moussawi M, Lefebvre MN, Attolini L, Yaici S, Tanesse D, Fontes M, Pouget J, Blin O (2009) Effect of ascorbic acid in patients with Charcot-Marie-Tooth disease type 1A: a multicentre, randomised, double-blind, placebo-controlled trial. Lancet Neurol 8:1103-1110.
31. Mizushima N, Hara T (2006) Intracellular quality control by autophagy: how does autophagy prevent neurodegeneration? Autophagy 2:302-304.
32. Mizushima N, Yoshimori T (2007) How to interpret LC3 immunoblotting. Autophagy 3:542-545.
33. Muchowski PJ, Wacker JL (2005) Modulation of neurodegeneration by molecular chaperones. Nat Rev Neurosci 6:11-22.
34. Naef R, Suter U (1998) Many facets of the peripheral myelin protein PMP22 in myelination and disease. Microsc Res Tech 41:359-371.
35. Narayanan SP, Flores AI, Wang F, Macklin WB (2009) Akt signals through the mammalian target of rapamycin pathway to regulate CNS myelination. J Neurosci 29:6860-6870.
36. Nicholson SM, Gomès D, de Néchaud B, Bruzzone R (2001) Altered gene expression in Schwann cells of connexin32 knockout animals. J Neurosci Res 66:23-36.
37. Notterpek L, Shooter EM, Snipes GJ (1997) Upregulation of the endosomallysosomal pathway in the trembler-J neuropathy. J Neurosci 17:4190-4200. (Pubitemid 27220610)
38. Notterpek L, Snipes GJ, Shooter EM (1999) Temporal expression pattern of peripheral myelin protein 22 during in vivo and in vitro myelination. Glia 25:358-369. (Pubitemid 29083835)
39. Pareek S, Notterpek L, Snipes GJ, Naef R, Sossin W, Laliberté J, Iacampo S, Suter U, Shooter EM, Murphy RA (1997) Neurons promote the translocation of peripheral myelin protein 22 into myelin. J Neurosci 17:7754-7762. (Pubitemid 27426214)
40. Pareyson D, Marchesi C (2009) Diagnosis, natural history, and management of Charcot-Marie-Tooth disease. Lancet Neurol 8:654-667.
41. Rangaraju S, Madorsky I, Pileggi JG, Kamal A, Notterpek L (2008) Pharmacological induction of the heat shock response improves myelination in a neuropathic model. Neurobiol Dis 32:105-115.
42. Rangaraju S, Hankins D, Madorsky I, Madorsky E, Lee WH, Carter CS, Leeuwenburgh C, Notterpek L (2009) Molecular architecture of myelinated peripheral nerves is supported by calorie restriction with aging. Aging Cell 8:178-191.
43. Sabers CJ, Martin MM, Brunn GJ, Williams JM, Dumont FJ, Wiederrecht G, Abraham RT (1995) Isolation of a protein target of the FKBP12-rapamycin complex in mammalian cells. J Biol Chem 270:815-822.
44. Saito K, Araki Y, Kontani K, Nishina H, Katada T (2005) Novel role of the small GTPase Rheb: its implication in endocytic pathway independent of the activation of mammalian target of rapamycin. J Biochem 137:423-430. (Pubitemid 40628451)
45. Sanders CR, Ismail-Beigi F, McEnery MW (2001) Mutations of peripheral myelin protein 22 result in defective trafficking through mechanisms which may be common to diseases involving tetraspan membrane proteins. Biochemistry 40:9453-9459. (Pubitemid 32757883)
46. Sarbassov DD, Ali SM, Sengupta S, Sheen JH, Hsu PP, Bagley AF, Markhard AL, Sabatini DM (2006) Prolonged rapamycin treatment inhibits mTORC2 assembly and Akt/PKB. Mol Cell 22:159-168.
47. Sarkar S, Rubinsztein DC (2008) Small molecule enhancers of autophagy for neurodegenerative diseases. Mol Biosyst 4:895-901.
48. Sarkar S, Ravikumar B, Floto RA, Rubinsztein DC (2009) Rapamycin and mTOR-independent autophagy inducers ameliorate toxicity of polyglutamine- expanded huntingtin and related proteinopathies. Cell Death Differ 16:46-56.
49. Shy ME, Balsamo J, Lilien J, Kamholz J (2001) A molecular basis for hereditary motor and sensory neuropathy disorders. Curr Neurol Neurosci Rep 1:77-88.
50. Spilman P, Podlutskaya N, Hart MJ, Debnath J, Gorostiza O, Bredesen D, Richardson A, Strong R, Galvan V (2010) Inhibition of mTOR by rapamycin abolishes cognitive deficits and reduces amyloid-beta levels in a mouse model of Alzheimer's disease. PLoS One 5:e9979.
51. Stefani M, Dobson CM (2003) Protein aggregation and aggregate toxicity: new insights into protein folding, misfolding diseases and biological evolution. J Mol Med 81:678-699.
52. Suter U, Moskow JJ, Welcher AA, Snipes GJ, Kosaras B, Sidman RL, Buchberg AM, Shooter EM (1992) A leucine-to-proline mutation in the putative first transmembrane domain of the 22-kDa peripheral myelin protein in the trembler-J mouse. Proc Natl Acad Sci U S A 89:4382-4386.
53. Verdú E, Ceballos D, Vilches JJ, Navarro X (2000) Influence of aging on peripheral nerve function and regeneration. J Peripher Nerv Syst 5:191-208.
54. Wakatsuki S, Yumoto N, Komatsu K, Araki T, Sehara-Fujisawa A (2009) Roles of meltrin-beta/ADAM19 in progression of Schwann cell differentiation and myelination during sciatic nerve regeneration. J Biol Chem 284:2957-2966.
55. Winklhofer KF, Tatzelt J, Haass C (2008) The two faces of protein misfolding: gain- and loss-of-function in neurodegenerative diseases. EMBO J 27:336-349.
56. Winterstein C, Trotter J, Krämer-Albers EM (2008) Distinct endocytic recycling of myelin proteins promotes oligodendroglial membrane remodeling. J Cell Sci 121:834-842.
57. Yamamoto K, Seki T, Adachi N, Takahashi T, Tanaka S, Hide I, Saito N, Sakai N (2010) Mutant protein kinase C gamma that causes spinocerebellar ataxia type 14 (SCA14) is selectively degraded by autophagy. Genes Cells.
58. Yang Z, Klionsky DJ (2009) An overview of the molecular mechanism of autophagy. Curr Top Microbiol Immunol 335:1-32.