Palmitoylation controls DLK localization, interactions and activity to ensure effective axonal injury signaling

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 3, 2016, Pages 763-768

  Holland, Sabrina M ^a   Collura, Kaitlin M ^a   Ketschek, Andrea ^a   Noma, Kentaro ^b,c   Ferguson, Toby A ^a,d   Jin, Yishi ^b,c   Gallo, Gianluca ^a   Thomas, Gareth M ^a  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c NEUROBIOLOGY SECTION   (United States)

^d BIOGEN   (United States)

Author keywords

C jun; JNK; MAPK; Regeneration; Trafficking

Indexed keywords

CYSTEINE; DUAL LEUCINE ZIPPER KINASE; LEUCINE ZIPPER PROTEIN; MICROTUBULE ASSOCIATED PROTEIN 2; MITOGEN ACTIVATED PROTEIN KINASE 12; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4; MITOGEN ACTIVATED PROTEIN KINASE KINASE 7; SHORT HAIRPIN RNA; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; CAENORHABDITIS ELEGANS PROTEIN; DLK-1 PROTEIN, C ELEGANS; FLUORESCENT DYE; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; MITOGEN-ACTIVATED PROTEIN KINASE KINASE KINASE 12; PROTEIN BINDING; SMALL INTERFERING RNA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AXONAL INJURY; CELL MIGRATION; CHEMICAL INTERACTION; CLINICAL EFFECTIVENESS; CONTROLLED STUDY; ENZYME ACTIVITY; GENE SILENCING; MEMBRANE VESICLE; MICROTUBULE; MOLECULAR BIOLOGY; NERVE CELL; NERVE FIBER; NONHUMAN; PALMITOYLATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN TARGETING; RAT; SENSORY NERVE; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; AMINO ACID SEQUENCE; ANIMAL; AXON; BIOLOGICAL MODEL; CAENORHABDITIS ELEGANS; CHEMISTRY; CONSERVED SEQUENCE; GENETIC TRANSFECTION; HEK293 CELL LINE; HUMAN; LIPOYLATION; METABOLISM; MICROFLUIDICS; MOLECULAR EVOLUTION; MOLECULAR GENETICS; MUTATION; PATHOLOGY; PHOSPHORYLATION; PROTEIN MULTIMERIZATION; PROTEIN TRANSPORT; TRANSPORT VESICLE;

AMINO ACID SEQUENCE; ANIMALS; AXONS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CONSERVED SEQUENCE; EVOLUTION, MOLECULAR; FLUORESCENT DYES; GENE KNOCKDOWN TECHNIQUES; HEK293 CELLS; HUMANS; LIPOYLATION; MAP KINASE KINASE KINASES; MICROFLUIDICS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MUTATION; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN TRANSPORT; RATS; RNA, SMALL INTERFERING; SENSORY RECEPTOR CELLS; SIGNAL TRANSDUCTION; TRANSFECTION; TRANSPORT VESICLES;

EID: 84955242253     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1514123113     Document Type: Article

References (53)

1. Rishal I, Fainzilber M (2014) Axon-soma communication in neuronal injury. Nat Rev Neurosci 15(1):32-42.
2. Abe N, Cavalli V (2008) Nerve injury signaling. Curr Opin Neurobiol 18(3):276-283.
3. Fan G, Merritt SE, Kortenjann M, Shaw PE, Holzman LB (1996) Dual leucine zipper-bearing kinase (DLK) activates p46SAPK and p38mapk but not ERK2. J Biol Chem 271(40):24788-24793.
4. Hammarlund M, Nix P, Hauth L, Jorgensen EM, Bastiani M (2009) Axon regeneration requires a conserved MAP kinase pathway. Science 323(5915):802-806.
5. Tedeschi A, Bradke F (2013) The DLK signalling pathway-A double-edged sword in neural development and regeneration. EMBO Rep 14(7):605-614.
6. Yan D, Wu Z, Chisholm AD, Jin Y (2009) The DLK-1 kinase promotes mRNA stability and local translation in C. elegans synapses and axon regeneration. Cell 138(5):1005-1018.
7. Shin JE, et al. (2012) Dual leucine zipper kinase is required for retrograde injury signaling and axonal regeneration. Neuron 74(6):1015-1022.
8. Xiong X, et al. (2010) Protein turnover of the Wallenda/DLK kinase regulates a retrograde response to axonal injury. J Cell Biol 191(1):211-223.
9. Ghosh AS, et al. (2011) DLK induces developmental neuronal degeneration via selective regulation of proapoptotic JNK activity. J Cell Biol 194(5):751-764.
10. Huntwork-Rodriguez S, et al. (2013) JNK-mediated phosphorylation of DLK suppresses its ubiquitination to promote neuronal apoptosis. J Cell Biol 202(5):747-763.
11. Yang J, et al. (2015) Pathological axonal death through a MAPK cascade that triggers a local energy deficit. Cell 160(1-2):161-176.
12. Lerch JK, et al. (2012) Isoform diversity and regulation in peripheral and central neurons revealed through RNA-Seq. PLoS One 7(1):e30417.
13. Gallo KA, Johnson GL (2002) Mixed-lineage kinase control of JNK and p38 MAPK pathways. Nat Rev Mol Cell Biol 3(9):663-672.
14. Lewcock JW, Genoud N, Lettieri K, Pfaff SL (2007) The ubiquitin ligase Phr1 regulates axon outgrowth through modulation of microtubule dynamics. Neuron 56(4):604-620.
15. Yan D, Jin Y (2012) Regulation of DLK-1 kinase activity by calcium-mediated dissociation from an inhibitory isoform. Neuron 76(3):534-548.
16. Fukata Y, Fukata M (2010) Protein palmitoylation in neuronal development and synaptic plasticity. Nat Rev Neurosci 11(3):161-175.
17. Kang R, et al. (2008) Neural palmitoyl-proteomics reveals dynamic synaptic palmitoylation. Nature 456(7224):904-909.
18. Thomas GM, Hayashi T, Chiu SL, Chen CM, Huganir RL (2012) Palmitoylation by DHHC5/8 targets GRIP1 to dendritic endosomes to regulate AMPA-R trafficking. Neuron 73(3):482-496.
19. Keith DJ, et al. (2012) Palmitoylation of A-kinase anchoring protein 79/150 regulates dendritic endosomal targeting and synaptic plasticity mechanisms. J Neurosci 32(21):7119-7136.
20. Oku S, Takahashi N, Fukata Y, Fukata M (2013) In silico screening for palmitoyl substrates reveals a role for DHHC1/3/10 (zDHHC1/3/11)-mediated neurochondrin palmitoylation in its targeting to Rab5-positive endosomes. J Biol Chem 288(27):19816-19829.
21. Cavalli V, Kujala P, Klumperman J, Goldstein LS (2005) Sunday Driver links axonal transport to damage signaling. J Cell Biol 168(5):775-787.
22. Itoh T, et al. (2014) ZPK/DLK and MKK4 form the critical gateway to axotomy-induced motoneuron death in neonates. J Neurosci 34(32):10729-10742.
23. Welsbie DS, et al. (2013) Functional genomic screening identifies dual leucine zipper kinase as a key mediator of retinal ganglion cell death. Proc Natl Acad Sci USA 110(10):4045-4050.
24. Shi SP, et al. (2013) The prediction of palmitoylation site locations using a multiple feature extraction method. J Mol Graph Model 40:125-130.
25. Jennings BC, et al. (2009) 2-Bromopalmitate and 2-(2-hydroxy-5-nitro-benzylidene)-benzo [b]thiophen-3-one inhibit DHHC-mediated palmitoylation in vitro. J Lipid Res 50(2):233-242.
26. Martin BR, Cravatt BF (2009) Large-scale profiling of protein palmitoylation in mammalian cells. Nat Methods 6(2):135-138.
27. Akimzhanov AM, Boehning D (2015) Rapid and transient palmitoylation of the tyrosine kinase Lck mediates Fas signaling. Proc Natl Acad Sci USA 112(38):11876-11880.
28. Deinhardt K, et al. (2006) Rab5 and Rab7 control endocytic sorting along the axonal retrograde transport pathway. Neuron 52(2):293-305.
29. Kaech S, Huang CF, Banker G (2012) Short-term high-resolution imaging of developing hippocampal neurons in culture. Cold Spring Harb Protoc 2012(3):340-343.
30. Taylor AM, et al. (2005) A microfluidic culture platform for CNS axonal injury, regeneration and transport. Nat Methods 2(8):599-605.
31. Mata M, Merritt SE, Fan G, Yu GG, Holzman LB (1996) Characterization of dual leucine zipper-bearing kinase, a mixed lineage kinase present in synaptic terminals whose phosphorylation state is regulated by membrane depolarization via calcineurin. J Biol Chem 271(28):16888-16896.
32. Abe N, et al. (2009) Sunday driver interacts with two distinct classes of axonal organelles. J Biol Chem 284(50):34628-34639.
33. Merritt SE, et al. (1999) The mixed lineage kinase DLK utilizes MKK7 and not MKK4 as substrate. J Biol Chem 274(15):10195-10202.
34. Kholodenko BN (2003) Four-dimensional organization of protein kinase signaling cascades: The roles of diffusion, endocytosis and molecular motors. J Exp Biol 206(Pt 12):2073-2082.
35. Drerup CM, Nechiporuk AV (2013) JNK-interacting protein 3 mediates the retrograde transport of activated c-Jun N-terminal kinase and lysosomes. PLoS Genet 9(2):e1003303.
36. Kay BK, Williamson MP, Sudol M (2000) The importance of being proline: The interaction of proline-rich motifs in signaling proteins with their cognate domains. FASEB J 14(2):231-241.
37. Reddy Chichili VP, Kumar V, Sivaraman J (2013) Linkers in the structural biology of protein-protein interactions. Protein Sci 22(2):153-167.
38. Kuznetsov IB, McDuffie M (2008) FlexPred: A web-server for predicting residue positions involved in conformational switches in proteins. Bioinformation 3(3):134-136.
39. Yamazaki M, et al. (2001) Differential palmitoylation of two mouse glutamate receptor interacting protein 1 forms with different N-terminal sequences. Neurosci Lett 304(1-2):81-84.
40. Levy AD, et al. (2011) Subcellular Golgi localization of stathmin family proteins is promoted by a specific set of DHHC palmitoyl transferases. Mol Biol Cell 22(11):1930-1942.
41. Holzman LB, Merritt SE, Fan G (1994) Identification, molecular cloning, and characterization of dual leucine zipper bearing kinase. A novel serine/threonine protein kinase that defines a second subfamily of mixed lineage kinases. J Biol Chem 269(49):30808-30817.
42. Hirai S, et al. (2005) Expression of MUK/DLK/ZPK, an activator of the JNK pathway, in the nervous systems of the developing mouse embryo. Gene Expr Patterns 5(4):517-523.
43. Collins CA, Wairkar YP, Johnson SL, DiAntonio A (2006) Highwire restrains synaptic growth by attenuating a MAP kinase signal. Neuron 51(1):57-69.
44. Nakata K, et al. (2005) Regulation of a DLK-1 and p38 MAP kinase pathway by the ubiquitin ligase RPM-1 is required for presynaptic development. Cell 120(3):407-420.
45. Patel S, et al. (2015) Discovery of dual leucine zipper kinase (DLK, MAP3K12) inhibitors with activity in neurodegeneration models. J Med Chem 58(1):401-418.
46. Chesarino NM, et al. (2014) Chemoproteomics reveals Toll-like receptor fatty acylation. BMC Biol 12(1):91.
47. Ren W, Jhala US, Du K (2013) Proteomic analysis of protein palmitoylation in adipocytes. Adipocyte 2(1):17-28.
48. George J, Soares C, Montersino A, Beique JC, Thomas GM (2015) Palmitoylation of LIM Kinase-1 ensures spine-specific actin polymerization and morphological plasticity. eLife 4:e06327.
49. Park JW, Vahidi B, Taylor AM, Rhee SW, Jeon NL (2006) Microfluidic culture platform for neuroscience research. Nat Protoc 1(4):2128-2136.
50. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77(1):71-94.
51. Yu H, et al. (2011) Lentiviral gene transfer into the dorsal root ganglion of adult rats. Mol Pain 7:63.
52. El Meskini R, et al. (2001) A signal sequence is sufficient for green fluorescent protein to be routed to regulated secretory granules. Endocrinology 142(2):864-873.
53. Mello CC, Kramer JM, Stinchcomb D, Ambros V (1991) Efficient gene transfer in C.elegans: Extrachromosomal maintenance and integration of transforming sequences. Embo J 10(12):3959-3970.