Cellular model of neuronal atrophy induced by DYNC1I1 deficiency reveals protective roles of RAS-RAF-MEK signaling

Protein and Cell

Volumn 7, Issue 9, 2016, Pages 638-650

  Liu, Zhi Dong ^a   Zhang, Su ^a,b   Hao, Jian Jin ^a   Xie, Tao Rong ^a   Kang, Jian Sheng ^a,b  

^a Chinese Academy of Sciences   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

atrophy; autophagy; dynein intermediate chain; hippocampal neuron; mitochondria; RAS RAF MEK pathway

Indexed keywords

B RAF KINASE; CYTOPLASMIC DYNEIN; DYNEIN INTERMEDIATE CHAIN 1I1; K RAS PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE; MOLECULAR MOTOR; PROTEIN KINASE B; RAF PROTEIN; RAS PROTEIN; UNCLASSIFIED DRUG; BRAF PROTEIN, HUMAN; DYNC1LI1 PROTEIN, HUMAN; DYNC1LI1 PROTEIN, MOUSE; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE;

ARTICLE; AUTOPHAGY; BRAIN ATROPHY; CONTROLLED STUDY; DEGENERATIVE DISEASE; DISORDERS OF MITOCHONDRIAL FUNCTIONS; GENE SILENCING; HIPPOCAMPUS; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; NEURONAL ATROPHY; PRIORITY JOURNAL; PROTEIN DEFICIENCY; ANIMAL; CELL LINE; GENETICS; KNOCKOUT MOUSE; METABOLISM; MOUSE; PATHOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; CELL LINE; CYTOPLASMIC DYNEINS; HIPPOCAMPUS; MAP KINASE KINASE KINASES; MAP KINASE SIGNALING SYSTEM; MICE; MICE, KNOCKOUT; NEURODEGENERATIVE DISEASES; PROTO-ONCOGENE PROTEINS B-RAF; RAS PROTEINS;

EID: 84981250076     PISSN: 1674800X     EISSN: 16748018     Source Type: Journal    
DOI: 10.1007/s13238-016-0301-6     Document Type: Article

References (48)

1. Banks GT, Fisher EM (2008) Cytoplasmic dynein could be key to understanding neurodegeneration. Genome Biol 9:214
2. Becker RE, Greig NH, Giacobini E (2008) Why do so many drugs for Alzheimer’s disease fail in development? Time for new methods and new practices? J Alzheimers Dis 15:303–325
3. Boylan KLM, Hays TS (2002) The gene for the intermediate chain subunit of cytoplasmic dynein is essential in Drosophila. Genetics 162:1211–1220
4. Brunet A, Datta SR, Greenberg ME (2001) Transcription-dependent and -independent control of neuronal survival by the PI3K–Akt signaling pathway. Curr Opin Neurobiol 11:297–305
5. Chao MV (2003) Neurotrophins and their receptors: a convergence point for many signalling pathways. Nat Rev Neurosci 4:299–309
6. Chen X-J, Levedakou EN, Millen KJ, Wollmann RL, Soliven B, Popko B (2007) Proprioceptive sensory neuropathy in mice with a mutation in the cytoplasmic dynein heavy chain 1 gene. J Neurosci 27:14515–14524
7. Chin PC, Liu L, Morrison BE, Siddiq A, Ratan RR, Bottiglieri T, D’Mello SR (2004) The c-Raf inhibitor GW5074 provides neuroprotection in vitro and in an animal model of neurodegeneration through a MEK-ERK and Akt-independent mechanism. J Neurochem 90:595–608
8. Craig LA, Hong NS, McDonald RJ (2011) Revisiting the cholinergic hypothesis in the development of Alzheimer’s disease. Neurosci Biobehav Rev 35:1397–1409
9. Dotti CG, Sullivan CA, Banker GA (1988) The establishment of polarity by hippocampal neurons in culture. J Neurosci 8:1454–1468
10. Eschbach J, Dupuis L (2011) Cytoplasmic dynein in neurodegeneration. Pharmacol Ther 130:348–363
11. Fiordalisi JJ, Johnson RL II, Ülkü AS, Der CJ, Cox AD (2001) Mammalian expression vectors for Ras family proteins: generation and use of expression constructs to analyze Ras family function. In: Der CJ, Balch WE (eds) Methods in enzymology. Academic Press, San Diego, pp 3–36
12. Fox NC, Schott JM (2004) Imaging cerebral atrophy: normal ageing to Alzheimer’s disease. Lancet 363:392–394
13. Freeman SH, Kandel R, Cruz L, Rozkalne A, Newell K, Frosch MP, Hedley-Whyte ET, Locascio JJ, Lipsitz L, Hyman BT (2008) Preservation of neuronal number despite age-related cortical brain atrophy in elderly subjects without Alzheimer disease. J Neuropathol Exp Neurol 67:1205–1212
14. Galabova-Kovacs G, Kolbus A, Matzen D, Meissl K, Piazzolla D, Rubiolo C, Steinitz K, Baccarini M (2006) ERK and beyond: insights from B-Raf and Raf-1 conditional knockouts. Cell Cycle Georget. Tex 5:1514–1518
15. Ha J, Lo KW-H, Myers KR, Carr TM, Humsi MK, Rasoul BA, Segal RA, Pfister KK (2008) A neuron-specific cytoplasmic dynein isoform preferentially transports TrkB signaling endosomes. J Cell Biol 181:1027–1039
16. Hafezparast M, Klocke R, Ruhrberg C, Marquardt A, Ahmad-Annuar A, Bowen S, Lalli G, Witherden AS, Hummerich H, Nicholson S et al (2003) Mutations in dynein link motor neuron degeneration to defects in retrograde transport. Science 300:808–812
17. Heumann R, Goemans C, Bartsch D, Lingenhöhl K, Waldmeier PC, Hengerer B, Allegrini PR, Schellander K, Wagner EF, Arendt T et al (2000) Transgenic activation of Ras in neurons promotes hypertrophy and protects from lesion-induced degeneration. J Cell Biol 151:1537–1548
18. Holzbaur ELF, Vallee RB (1994) Dyneins: molecular structure and cellular function. Annu Rev Cell Biol 10:339–372
19. Kapitein LC, Schlager MA, Kuijpers M, Wulf PS, van Spronsen M, MacKintosh FC, Hoogenraad CC (2010) Mixed microtubules steer dynein-driven cargo transport into dendrites. Curr Biol 20:290–299
20. Karran E, Mercken M, Strooper BD (2011) The amyloid cascade hypothesis for Alzheimer’s disease: an appraisal for the development of therapeutics. Nat. Rev. Drug Discov. 10:698–712
21. Kimura S, Noda T, Yoshimori T (2008) Dynein-dependent movement of autophagosomes mediates efficient encounters with lysosomes. Cell Struct Funct 33:109–122
22. Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, Agholme L, Agnello M, Agostinis P, Aguirre-Ghiso JA et al (2012) Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 8:445–544
23. Kumar V, Zhang M-X, Swank MW, Kunz J, Wu G-Y (2005) Regulation of dendritic morphogenesis by Ras–PI3K–Akt–mTOR and Ras–MAPK signaling pathways. J Neurosci 25:11288–11299
24. Lalli G (2014) Regulation of neuronal polarity. Exp Cell Res 328:267–275
25. Lipka J, Kuijpers M, Jaworski J, Hoogenraad CC (2013) Mutations in cytoplasmic dynein and its regulators cause malformations of cortical development and neurodegenerative diseases. Biochem Soc Trans 41:1605–1612
26. Maday S, Wallace KE, Holzbaur ELF (2012) Autophagosomes initiate distally and mature during transport toward the cell soma in primary neurons. J Cell Biol 196:407–417
27. Mazzoni IE, Saı̈d FA, Aloyz R, Miller FD, Kaplan D (1999) Ras regulates sympathetic neuron survival by suppressing the p53-mediated cell death pathway. J Neurosci 19:9716–9727
28. Mitchell DJ, Blasier KR, Jeffery ED, Ross MW, Pullikuth AK, Suo D, Park J, Smiley WR, Lo KW-H, Shabanowitz J et al (2012) Trk activation of the ERK1/2 kinase pathway stimulates intermediate chain phosphorylation and recruits cytoplasmic dynein to signaling endosomes for retrograde axonal transport. J Neurosci 32:15495–15510
29. Moreira PI, Zhu X, Wang X, Lee H, Nunomura A, Petersen RB, Perry G, Smith MA (2010) Mitochondria: a therapeutic target in neurodegeneration. Biochim Biophys Acta 1802:212–220
30. Myers KR, Lo KW-H, Lye RJ, Kogoy JM, Soura V, Hafezparast M, Pfister KK (2007) Intermediate chain subunit as a probe for cytoplasmic dynein function: biochemical analyses and live cell imaging in PC12 cells. J Neurosci Res 85:2640–2647
31. Pakkenberg B, Pelvig D, Marner L, Bundgaard MJ, Gundersen HJG, Nyengaard JR, Regeur L (2003) Aging and the human neocortex. Exp Gerontol 38:95–99
32. Payne BAI, Chinnery PF (2015) Mitochondrial dysfunction in aging: much progress but many unresolved questions. Biochim. Biophys. Acta BBA - Bioenerg. 1847:1347–1353
33. Pfister KK, Fisher EMC, Gibbons IR, Hays TS, Holzbaur ELF, McIntosh JR, Porter ME, Schroer TA, Vaughan KT, Witman GB et al (2005) Cytoplasmic dynein nomenclature. J Cell Biol 171:411–413
34. Ravikumar B, Acevedo-Arozena A, Imarisio S, Berger Z, Vacher C, O’Kane CJ, Brown SDM, Rubinsztein DC (2005) Dynein mutations impair autophagic clearance of aggregate-prone proteins. Nat Genet 37:771–776
35. Regeur L, Badsberg Jensen G, Pakkenberg H, Evans SM, Pakkenberg B (1994) No global neocortical nerve cell loss in brains from patients with senile dementia of Alzheimer’s type. Neurobiol Aging 15:347–352
36. Rosse C, Boeckeler K, Linch M, Radtke S, Frith D, Barnouin K, Morsi AS, Hafezparast M, Howell M, Parker PJ (2012) Binding of dynein intermediate chain 2 to paxillin controls focal adhesion dynamics and migration. J Cell Sci 125:3733–3738
37. Scaduto RC Jr, Grotyohann LW (1999) Measurement of mitochondrial membrane potential using fluorescent rhodamine derivatives. Biophys J 76:469–477
38. Schott JM, Fox NC, Frost C, Scahill RI, Janssen JC, Chan D, Jenkins R, Rossor MN (2003) Assessing the onset of structural change in familial Alzheimer’s disease. Ann Neurol 53:181–188
39. Slack C, Alic N, Foley A, Cabecinha M, Hoddinott MP, Partridge L (2015) The Ras-Erk-ETS-signaling pathway is a drug target for longevity. Cell 162:72–83
40. Song A, Wang D, Chen G, Li Y, Luo J, Duan S, Poo M (2009) A selective filter for cytoplasmic transport at the axon initial segment. Cell 136:1148–1160
41. Soo KY, Farg M, Atkin JD (2011) Molecular motor proteins and amyotrophic lateral sclerosis. Int J Mol Sci 12:9057–9082
42. Swaab DF, Hofman MA, Lucassen PJ, Salehi A, Uylings HBM (1994) Neuronal atrophy, not cell death, is the main hallmark of Alzheimer’s disease. Neurobiol Aging 15:369–371
43. Vaughan PS, Leszyk JD, Vaughan KT (2001) Cytoplasmic dynein intermediate chain phosphorylation regulates binding to dynactin. J Biol Chem 276:26171–26179
44. Wang J, Whiteman MW, Lian H, Wang G, Singh A, Huang D, Denmark T (2009) A non-canonical MEK/ERK signaling pathway regulates autophagy via regulating beclin 1. J Biol Chem 284:21412–21424
45. Xie Y, Zhou B, Lin M-Y, Wang S, Foust KD, Sheng Z-H (2015) Endolysosomal deficits augment mitochondria pathology in spinal motor neurons of asymptomatic fALS mice. Neuron 87:355–370
46. Yamaguchi T, Kakefuda R, Tajima N, Sowa Y, Sakai T (2011) Antitumor activities of JTP-74057 (GSK1120212), a novel MEK1/2 inhibitor, on colorectal cancer cell lines in vitro and in vivo. Int J Oncol 39:23–31
47. Zheng Y, Wildonger J, Ye B, Zhang Y, Kita A, Younger SH, Zimmerman S, Jan LY, Jan YN (2008) Dynein is required for polarized dendritic transport and uniform microtubule orientation in axons. Nat Cell Biol 10:1172–1180
48. Zhong J, Li X, McNamee C, Chen AP, Baccarini M, Snider WD (2007) Raf kinase signaling functions in sensory neuron differentiation and axon growth in vivo. Nat Neurosci 10:598–607