Home LiteratureArticle Details
PMID: 15738268 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Sunday Driver links axonal transport to damage signaling.

The Journal of cell biology ·Vol. 168 ·No. 5 ·2005-02-28 ·Pages 775-87

Cavalli V, Kujala P, Klumperman J, Goldstein LS

Abstract

Neurons transmit long-range biochemical signals between cell bodies and distant axonal sites or termini. To test the hypothesis that signaling molecules are hitchhikers on axonal vesicles, we focused on the c-Jun NH2-terminal kinase (JNK) scaffolding protein Sunday Driver (syd), which has been proposed to link the molecular motor protein kinesin-1 to axonal vesicles. We found that syd and JNK3 are present on vesicular structures in axons, are transported in both the anterograde and retrograde axonal transport pathways, and interact with kinesin-I and the dynactin complex. Nerve injury induces local activation of JNK, primarily within axons, and activated JNK and syd are then transported primarily retrogradely. In axons, syd and activated JNK colocalize with p150Glued, a subunit of the dynactin complex, and with dynein. Finally, we found that injury induces an enhanced interaction between syd and dynactin. Thus, a mobile axonal JNK-syd complex may generate a transport-dependent axonal damage surveillance system.

MeSH Terms
Adaptor Proteins, Signal Transducing Animals Axons/metabolism Carrier Proteins/metabolism Drosophila Proteins/metabolism Dynactin Complex Fluorescent Antibody Technique Membrane Proteins/metabolism Mice Microtubule-Associated Proteins/metabolism Mitogen-Activated Protein Kinase 10/metabolism Nerve Tissue Proteins Protein Transport/physiology Sciatic Nerve/injuries,metabolism,surgery Signal Transduction/physiology
Chemicals
Adaptor Proteins, Signal Transducing Carrier Proteins Drosophila Proteins Dynactin Complex Mapk8ip3 protein, mouse Membrane Proteins Microtubule-Associated Proteins Nerve Tissue Proteins syd protein, Drosophila Mitogen-Activated Protein Kinase 10
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Cavalli Valeria
Department of Cellular and Molecular Medicine, Howard Hughes Medical Institute, University of California, San Diego, La Jolla, CA 92093, USA.
Kujala Pekka
Klumperman Judith
Goldstein Lawrence S B
References (51)
51 references, click to expand
  1. Interaction of a mitogen-activated protein kinase signaling module with the neuronal protein JIP3.
    Mol Cell Biol. 2000 Feb;20(3):1030-43 PMID: 10629060
  2. Peripheral axotomy induces long-term c-Jun amino-terminal kinase-1 activation and activator protein-1 binding activity by c-Jun and junD in adult rat dorsal root ganglia In vivo.
    J Neurosci. 1998 Feb 15;18(4):1318-28 PMID: 9454841
  3. Signal transduction by the JNK group of MAP kinases.
    Cell. 2000 Oct 13;103(2):239-52 PMID: 11057897
  4. Differential patterns of ERK and STAT3 phosphorylation after sciatic nerve transection in the rat.
    Exp Neurol. 2000 Dec;166(2):392-402 PMID: 11085904
  5. Beta-arrestin 2: a receptor-regulated MAPK scaffold for the activation of JNK3.
    Science. 2000 Nov 24;290(5496):1574-7 PMID: 11090355
  6. Kinesin-dependent axonal transport is mediated by the sunday driver (SYD) protein.
    Cell. 2000 Nov 10;103(4):583-94 PMID: 11106729
  7. Axonal transport of amyloid precursor protein is mediated by direct binding to the kinesin light chain subunit of kinesin-I.
    Neuron. 2000 Nov;28(2):449-59 PMID: 11144355
  8. Association of Trk neurotrophin receptors with components of the cytoplasmic dynein motor.
    J Neurosci. 2001 Feb 1;21(3):RC125 PMID: 11157096
  9. Cargo of kinesin identified as JIP scaffolding proteins and associated signaling molecules.
    J Cell Biol. 2001 Mar 5;152(5):959-70 PMID: 11238452
  10. Axonal transport of TNF-alpha in painful neuropathy: distribution of ligand tracer and TNF receptors.
    J Neuroimmunol. 2001 Mar 1;114(1-2):48-56 PMID: 11240015
  11. RISK-1: a novel MAPK homologue in axoplasm that is activated and retrogradely transported after nerve injury.
    J Neurobiol. 2001 Apr;47(1):67-79 PMID: 11257614
  12. Retrograde transport of transcription factor NF-kappa B in living neurons.
    J Biol Chem. 2001 Apr 13;276(15):11821-9 PMID: 11096106
  13. Requirement of the JIP1 scaffold protein for stress-induced JNK activation.
    Genes Dev. 2001 Sep 15;15(18):2421-32 PMID: 11562351
  14. Neuronal injury increases retrograde axonal transport of the neurotrophins to spinal sensory neurons and motor neurons via multiple receptor mechanisms.
    Mol Cell Neurosci. 1998 Oct;12(3):105-18 PMID: 9790733
  15. Cytoplasmic dynein and dynactin in cell division and intracellular transport.
    Curr Opin Cell Biol. 1999 Feb;11(1):45-53 PMID: 10047518
  16. The Jnk1 and Jnk2 protein kinases are required for regional specific apoptosis during early brain development.
    Neuron. 1999 Apr;22(4):667-76 PMID: 10230788
  17. The JIP group of mitogen-activated protein kinase scaffold proteins.
    Mol Cell Biol. 1999 Oct;19(10):7245-54 PMID: 10490659
  18. JSAP1, a novel jun N-terminal protein kinase (JNK)-binding protein that functions as a Scaffold factor in the JNK signaling pathway.
    Mol Cell Biol. 1999 Nov;19(11):7539-48 PMID: 10523642
  19. UNC-16, a JNK-signaling scaffold protein, regulates vesicle transport in C. elegans.
    Neuron. 2001 Dec 6;32(5):787-800 PMID: 11738026
  20. Coordination of opposite-polarity microtubule motors.
    J Cell Biol. 2002 Feb 18;156(4):715-24 PMID: 11854311
  21. Glutamate-receptor-interacting protein GRIP1 directly steers kinesin to dendrites.
    Nature. 2002 May 2;417(6884):83-7 PMID: 11986669
  22. Pincher, a pinocytic chaperone for nerve growth factor/TrkA signaling endosomes.
    J Cell Biol. 2002 May 13;157(4):679-91 PMID: 12011113
  23. High-resolution imaging demonstrates dynein-based vesicular transport of activated Trk receptors.
    J Neurobiol. 2002 Jun 15;51(4):302-12 PMID: 12150505
  24. Differential nucleocytoplasmic shuttling of beta-arrestins. Characterization of a leucine-rich nuclear export signal in beta-arrestin2.
    J Biol Chem. 2002 Oct 4;277(40):37693-701 PMID: 12167659
  25. Dynactin is required for bidirectional organelle transport.
    J Cell Biol. 2003 Feb 3;160(3):297-301 PMID: 12551954
  26. JNK1 is required for maintenance of neuronal microtubules and controls phosphorylation of microtubule-associated proteins.
    Dev Cell. 2003 Apr;4(4):521-33 PMID: 12689591
  27. Abnormal neurofilament transport caused by targeted disruption of neuronal kinesin heavy chain KIF5A.
    J Cell Biol. 2003 Apr 14;161(1):55-66 PMID: 12682084
  28. Enhanced activation of axonally transported stress-activated protein kinases in peripheral nerve in diabetic neuropathy is prevented by neurotrophin-3.
    Brain. 2003 Jul;126(Pt 7):1671-82 PMID: 12805110
  29. NGF signaling in sensory neurons: evidence that early endosomes carry NGF retrograde signals.
    Neuron. 2003 Jul 3;39(1):69-84 PMID: 12848933
  30. Rapid electrical and delayed molecular signals regulate the serum response element after nerve injury: convergence of injury and learning signals.
    J Neurobiol. 2003 Nov;57(2):204-20 PMID: 14556286
  31. Peripheral axon crush elevates transport of p75NTR in the central projection of sensory neurones of rats.
    Neurosci Lett. 2003 Nov 20;351(3):181-5 PMID: 14623136
  32. Axoplasmic importins enable retrograde injury signaling in lesioned nerve.
    Neuron. 2003 Dec 18;40(6):1095-104 PMID: 14687545
  33. From snails to sciatic nerve: Retrograde injury signaling from axon to soma in lesioned neurons.
    J Neurobiol. 2004 Feb 5;58(2):287-94 PMID: 14704959
  34. Scaffold protein JSAP1 is transported to growth cones of neurites independent of JNK signaling pathways in PC12h cells.
    Gene. 2004 Mar 31;329:51-60 PMID: 15033528
  35. STAT3 phosphorylation in injured axons before sensory and motor neuron nuclei: potential role for STAT3 as a retrograde signaling transcription factor.
    J Comp Neurol. 2004 Jul 5;474(4):535-45 PMID: 15174071
  36. The AP-1 transcription factor c-Jun is required for efficient axonal regeneration.
    Neuron. 2004 Jul 8;43(1):57-67 PMID: 15233917
  37. A neuronal isoform of protein kinase G couples mitogen-activated protein kinase nuclear import to axotomy-induced long-term hyperexcitability in Aplysia sensory neurons.
    J Neurosci. 2004 Aug 25;24(34):7583-95 PMID: 15329406
  38. The movement of membranous organelles in axons. Electron microscopic identification of anterogradely and retrogradely transported organelles.
    J Cell Biol. 1980 Mar;84(3):513-30 PMID: 6153657
  39. Phase separation of integral membrane proteins in Triton X-114 solution.
    J Biol Chem. 1981 Feb 25;256(4):1604-7 PMID: 6257680
  40. Retrograde transport by the microtubule-associated protein MAP 1C.
    Nature. 1987 Nov 12-18;330(6144):181-3 PMID: 3670402
  41. Immuno-localization of the insulin regulatable glucose transporter in brown adipose tissue of the rat.
    J Cell Biol. 1991 Apr;113(1):123-35 PMID: 2007617
  42. Long-term increase in the levels of c-jun mRNA and jun protein-like immunoreactivity in motor and sensory neurons following axon damage.
    Neurosci Lett. 1991 Aug 5;129(1):107-10 PMID: 1922958
  43. Selective expression of Jun proteins following axotomy and axonal transport block in peripheral nerves in the rat: evidence for a role in the regeneration process.
    Brain Res. 1991 Dec 6;566(1-2):198-207 PMID: 1726060
  44. NGF-stimulated retrograde transport of trkA in the mammalian nervous system.
    J Cell Biol. 1995 Jul;130(1):149-56 PMID: 7540615
  45. Retrograde axonal transport of signal transduction proteins in rat sciatic nerve.
    Brain Res. 1995 Aug 28;690(1):55-63 PMID: 7496807
  46. Priming events and retrograde injury signals. A new perspective on the cellular and molecular biology of nerve regeneration.
    Mol Neurobiol. 1996 Aug;13(1):61-79 PMID: 8892336
  47. The c-Jun transcription factor--bipotential mediator of neuronal death, survival and regeneration.
    Trends Neurosci. 1997 May;20(5):227-31 PMID: 9141200
  48. A nuclear localization signal targets proteins to the retrograde transport system, thereby evading uptake into organelles in aplysia axons.
    J Neurobiol. 1997 Aug;33(2):151-60 PMID: 9240371
  49. Absence of excitotoxicity-induced apoptosis in the hippocampus of mice lacking the Jnk3 gene.
    Nature. 1997 Oct 23;389(6653):865-70 PMID: 9349820
  50. The MAP kinase kinase kinase MLK2 co-localizes with activated JNK along microtubules and associates with kinesin superfamily motor KIF3.
    EMBO J. 1998 Jan 2;17(1):149-58 PMID: 9427749
  51. Axonal transport of activating transcription factor-2 is modulated by nerve growth factor in nociceptive neurons.
    J Neurosci. 1999 Sep 15;19(18):RC24 PMID: 10479717
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
DOI
10.1083/jcb.200410136
Published
2005-02-28
Pages
775-87
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2171809
Subset
IM
External Links
PubMed source DOI: 10.1083/jcb.200410136 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2