A switch in retrograde signaling from survival to stress in rapid-onset neurodegeneration

Journal of Neuroscience

Volumn 29, Issue 31, 2009, Pages 9903-9917

  Perlson, Eran ^a   Jeong, Goo Bo ^b,c   Ross, Jenny L ^a,d   Dixit, Ram ^a,e   Wallace, Karen E ^a   Kalb, Robert G ^b   Holzbaur, Erika L F ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^c Gachon University College of Medicine   (South Korea)

^d UNIVERSITY OF MASSACHUSETTS   (United States)

^e WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 8; COPPER ZINC SUPEROXIDE DISMUTASE; COPPER ZINC SUPEROXIDE DISMUTASE1; DYNACTIN; DYNEIN ADENOSINE TRIPHOSPHATASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; NEUROTROPHIN RECEPTOR P75; PROTEIN TYROSINE KINASE; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL MOTILITY; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME REGULATION; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NERVE DEGENERATION; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

ANIMALS; AXONAL TRANSPORT; CELL SURVIVAL; CELLS, CULTURED; COCULTURE TECHNIQUES; DISEASE MODELS, ANIMAL; DYNEIN ATPASE; GANGLIA, SPINAL; MICE; MICE, TRANSGENIC; MICROTUBULE-ASSOCIATED PROTEINS; MOTOR NEURONS; NERVE DEGENERATION; NEURODEGENERATIVE DISEASES; NEUROGLIA; NEURONS; RATS; SIGNAL TRANSDUCTION; SUPEROXIDE DISMUTASE; TIME FACTORS;

EID: 68549121208     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0813-09.2009     Document Type: Article

References (53)

1. Barker PA (2004) p75NTR is positively promiscuous: novel partners and new insights. Neuron 42:529-533.
2. Boillée S, Yamanaka K, Lobsiger CS, Copeland NG, Jenkins NA, Kassiotis G, Kollias G, Cleveland DW (2006) Onset and progression in inherited ALS determined by motor neurons and microglia. Science 312:1389-1392.
3. Bowman AB, Kamal A, Ritchings BW, Philp AV, McGrail M, Gindhart JG, Goldstein LS (2000) Kinesin-dependent axonal transport is mediated by the sunday driver (SYD) protein. Cell 103:583-594.
4. Campenot RB (1992) Compartmented culture analysis of nerve growth. In: Cell-cell interactions: a practical approach (B. Stevenson, D. Paul, and W. Gallin, eds), pp 275-298. New York: Oxford UP.
5. Glued transports caspase-8 to drive retrograde olfactory receptor neuron apoptosis. J Neurosci 25:6092-6104.
6. Cavalli V, Kujala P, Klumperman J, Goldstein LS (2005) Sunday Driver links axonal transport to damage signaling. J Cell Biol 168:775-787.
7. Caviston J, Ross J, Antony S, Tokito M, Holzbaur E (2007) Huntingtin facilitates dynein/dynactin-mediated vesicle transport. Proc Natl Acad Sci U S A 104:10045-10050.
8. Chao MV (2003) Neurotrophins and their receptors: a convergence point for many signalling pathways. Nat Rev Neurosci 4:299-309.
9. Chen XJ, 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.
10. Chevalier-Larsen E, Holzbaur EL (2006) Axonal transport and neurodegenerative disease. Biochim Biophys Acta 1762:1094-1108.
11. Clement AM, Nguyen MD, Roberts EA, Garcia ML, Boillée S, Rule M, McMahon AP, Doucette W, Siwek D, Ferrante RJ, Brown RH Jr, Julien JP, Goldstein LS, Cleveland DW (2003) Wild-type nonneuronal cells extend survival of SOD1 mutant motor neurons in ALS mice Science [Erratum (2003) 302:568] 302:113-117.
12. Deinhardt K, Salinas S, Verastegui C, Watson R, Worth D, Hanrahan S, Bucci C, Schiavo G (2006) Rab5 and Rab7 control endocytic sorting along the axonal retrograde transport pathway. Neuron 52:293-305.
13. Delcroix JD, Valletta JS, Wu C, Hunt SJ, Kowal AS, Mobley WC (2003) NGF signaling in sensory neurons: evidence that early endosomes carry NGF retrograde signals. Neuron 39:69-84.
14. De Vos KJ, Chapman AL, Tennant ME, Manser C, Tudor EL, Lau KF, Brownlees J, Ackerley S, Shaw PJ, McLoughlin DM, Shaw CE, Leigh PN, Miller CC, Grierson AJ (2007) Familial amyotrophic lateral sclerosis-linked SOD1 mutants perturb fast axonal transport to reduce axonal mitochondria content. Hum Mol Genet 16:2720-2728.
15. Di Giorgio FP, Carrasco MA, Siao MC, Maniatis T, Eggan K (2007) Non-cell autonomous effect of glia on motor neurons in an embryonic stem cell-based ALS model. Nat Neurosci 10:608-614.
16. Friedman DS, Vale RD (1999) Single-molecule analysis of kinesin motility reveals regulation by the cargo-binding tail domain. Nat Cell Biol 1:293-297.
17. Fryer HJ, Knox RJ, Strittmatter SM, Kalb RG (1999) Excitotoxic death of a subset of embryonic rat motor neurons in vitro. J Neurochem 72:500-513.
18. Gonatas NK, Stieber A, Gonatas JO (2006) Fragmentation of the Golgi apparatus in neurodegenerative diseases and cell death. J Neurol Sci 246:21-30.
19. Gould TW, Buss RR, Vinsant S, Prevette D, Sun W, Knudson CM, Milligan CE, Oppenheim RW (2006) Complete dissociation of motor neuron death from motor dysfunction by Bax deletion in a mouse model of ALS. J Neurosci 26:8774-8786.
20. Gross SP (2004) Hither and yon: a review of bi-directional microtubule-based transport. Phys Biol 1:R1-R11.
21. Gurney ME, Pu H, Chiu AY, Dal Canto MC, Polchow CY, Alexander DD, Caliendo J, Hentati A, Kwon YW, Deng HX (1994) Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation. Science [Erratum (1995) 269:149] 264:1772-1775.
22. Hafezparast M, Klocke R, Ruhrberg C, Marquardt A, Ahmad-Annuar A, Bowen S, Lalli G, Witherden AS, Hummerich H, Nicholson S, Morgan PJ, Oozageer R, Priestley JV, Averill S, King VR, Ball S, Peters J, Toda T, Yamamoto A, Hiraoka Y, et al. (2003) Mutations in dynein link motor neuron degeneration to defects in retrograde transport. Science 300:808-812.
23. Heerssen HM, Pazyra MF, Segal RA (2004) Dynein motors transport activated Trks to promote survival of target-dependent neurons. Nat Neurosci 7:596-604.
24. Henderson CE, Camu W, Mettling C, Gouin A, Poulsen K, Karihaloo M, Rullamas J, Evans T, McMahon SB, Armanini MP (1993) Neurotrophins promote motor neuron survival and are present in embryonic limb bud. Nature 363:266-270.
25. Horiuchi D, Collins CA, Bhat P, Barkus RV, Diantonio A, Saxton WM (2007) Control of a kinesin-cargo linkage mechanism by JNK pathway kinases. Curr Biol 17:1313-1317.
26. Jaarsma D, Holstege JC, Troost D, Davis M, Kennis J, Haasdijk ED, de Jong VJ (1996) Induction of c-Jun immunoreactivity in spinal cord and brainstem neurons in a transgenic mouse model for amyotrophic lateral sclerosis. Neurosci Lett 219:179-182.
27. Jaarsma D, Teuling E, Haasdijk ED, De Zeeuw CI, Hoogenraad CC (2008) Neuron-specific expression of mutant superoxide dismutase is sufficient to induce amyotrophic lateral sclerosis in transgenic mice. J Neurosci 28:2075-2088.
28. Karki S, Holzbaur EL (1995) Affinity chromatography demonstrates a direct binding between cytoplasmic dynein and the dynactin complex. J Biol Chem 270:28806-28811.
29. Kenchappa RS, Zampieri N, Chao MV, Barker PA, Teng HK, Hempstead BL, Carter BD (2006) Ligand-dependent cleavage of the P75 neurotrophin receptor is necessary for NRIF nuclear translocation and apoptosis in sympathetic neurons. Neuron 50:219-232.
30. Kieran D, Hafezparast M, Bohnert S, Dick JR, Martin J, Schiavo G, Fisher EM, Greensmith L (2005) A mutation in dynein rescues axonal transport defects and extends the life span of ALS mice. J Cell Biol 169:561-567.
31. Küst BM, Brouwer N, Mantingh IJ, Boddeke HW, Copray JC (2003) Reduced p75NTR expression delays disease onset only in female mice of a transgenic model of familial amyotrophic lateral sclerosis. Amyotroph Lateral Scler Other Motor Neuron Disord 4:100-105.
32. LaMonte BH, Wallace KE, Holloway BA, Shelly SS, Ascaño J, Tokito M, Van Winkle T, Howland DS, Holzbaur EL (2002) Disruption of dynein /dynactin inhibits axonal transport in motor neurons causing late-onset progressive degeneration. Neuron 34:715-727.
33. Lee R, Kermani P, Teng KK, Hempstead BL (2001) Regulation of cell survival by secreted proneurotrophins. Science 294:1945-1948.
34. Ligon LA, LaMonte BH, Wallace KE, Weber N, Kalb RG, Holzbaur EL (2005) Mutant superoxide dismutase disrupts cytoplasmic dynein in motor neurons. Neuroreport 16:533-536.
35. Lino MM, Schneider C, Caroni P (2002) Accumulation of SOD1 mutants in postnatal motoneurons does not cause motoneuron pathology or motoneuron disease. J Neurosci 22:4825-4832.
36. Lu B, Pang PT, Woo NH (2005) The yin and yang of neurotrophin action. Nat Rev Neurosci 6:603-614.
37. Morfini G, Pigino G, Szebenyi G, You Y, Pollema S, Brady ST (2006) JNK mediates pathogenic effects of polyglutamine-expanded androgen receptor on fast axonal transport. Nat Neurosci 9:907-916.
38. Nagai M, Re DB, Nagata T, Chalazonitis A, Jessell TM, Wichterle H, Przedborski S (2007) Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons. Nat Neurosci 10:615-622.
39. Neve RL, Howe HR, Hong S, Kalb RG (1997) Introduction of the glutamate receptor subunit 1 into motor neurons in vitro and in vivo using a recombinant herpes simplex virus. Neuroscience 79:435-447.
40. Petri S, Kiaei M, Wille E, Calingasan NY, Flint Beal M (2006) Loss of Fas ligand-function improves survival in G93A-transgenic ALS mice. J Neurol Sci 251:44-49.
41. Puls I, Jonnakuty C, LaMonte BH, Holzbaur EL, Tokito M, Mann E, Floeter MK, Bidus K, Drayna D, Oh SJ, Brown RH Jr, Ludlow CL, Fischbeck KH (2003) Mutant dynactin in motor neuron disease. Nat Genet 33:455-456.
42. Puls I, Oh SJ, Sumner CJ, Wallace KE, Floeter MK, Mann EA, Kennedy WR, Wendelschafer-Crabb G, Vortmeyer A, Powers R, Finnegan K, Holzbaur EL, Fischbeck KH, Ludlow CL (2005) Distal spinal and bulbar muscular atrophy caused by dynactin mutation. Ann Neurol 57:687-694.
43. Puthalakath H, Huang DC, O'Reilly LA, King SM, Strasser A (1999) The proapoptotic activity of the Bcl-2 family member Bim is regulated by interaction with the dynein motor complex. Mol Cell 3:287-296.
44. Raoul C, Estévez AG, Nishimune H, Cleveland DW, deLapeyrière O, Henderson CE, Haase G, Pettmann B (2002) Motoneuron death triggered by a specific pathway downstream of Fas. Potentiation by ALS-linked SOD1 mutations. Neuron 35:1067-1083.
45. Ross JL, Wallace K, Shuman H, Goldman YE, Holzbaur EL (2006) Processive bidirectional motion of dynein-dynactin complexes in vitro. Nat Cell Biol 8:562-570.
46. Schenck A, Goto-Silva L, Collinet C, Rhinn M, Giner A, Habermann B, Brand M, Zerial M (2008) The endosomal protein Appl1 mediates Akt substrate specificity and cell survival in vertebrate development. Cell 133:468-497.
47. Verhey KJ, Meyer D, Deehan R, Blenis J, Schnapp BJ, Rapoport TA, Margolis B (2001) Cargo of kinesin identified as JIP scaffolding proteins and associated signaling molecules. J Cell Biol 152:959-970.
48. Williamson TL, Cleveland DW (1999) Slowing of axonal transport is a very early event in the toxicity of ALS-linked SOD1 mutants to motor neurons. Nat Neurosci 2:50-56.
49. Yano H, Chao MV (2004) Mechanisms of neurotrophin receptor vesicular transport. J Neurobiol 58:244-257.
50. Yano H, Lee FS, Kong H, Chuang J, Arevalo J, Perez P, Sung C, Chao MV (2001) Association of Trk neurotrophin receptors with components of the cytoplasmic dynein motor. J Neurosci 21:RC125.
51. Ye H, Kuruvilla R, Zweifel LS, Ginty DD (2003) Evidence in support of signaling endosome-based retrograde survival of sympathetic neurons. Neuron 39:57-68.
52. Zhang B, Tu P, Abtahian F, Trojanowski JQ, Lee VM (1997) Neurofilaments and orthograde transport are reduced in ventral root axons of transgenic mice that express human SOD1 with a G93A mutation. J Cell Biol 139:1307-1315.
53. Zhang F, Ström AL, Fukada K, Lee S, Hayward LJ, A Zhu H (2007) Interaction between familial amyotrophic lateral sclerosis (ALS)-linked SOD1 mutants and the dynein complex. J Biol Chem 282:16691-16699.