S6 kinase inhibits intrinsic axon regeneration capacity via AMP kinase in Caenorhabditis elegans

Journal of Neuroscience

Volumn 34, Issue 3, 2014, Pages 758-763

  Hubert, Thomas ^a   Wu, Zilu ^a   Chisholm, Andrew D ^a   Jin, Yishi ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

AMP kinase; Caenorhabditis elegans; DLK kinase; Laser axotomy; Ribosomal S6 kinase

Indexed keywords

ADENYLATE KINASE; METFORMIN; MITOGEN ACTIVATED PROTEIN KINASE; PHENFORMIN; S6 KINASE;

ANIMAL EXPERIMENT; ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; MOLECULAR BIOLOGY; NERVE FIBER REGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RIBOSOME; SIGNAL TRANSDUCTION;

AMP KINASE; CAENORHABDITIS ELEGANS; DLK KINASE; LASER AXOTOMY; RIBOSOMAL S6 KINASE;

ADENYLATE KINASE; ANIMALS; AXONS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; NERVE REGENERATION; PROTEIN-SERINE-THREONINE KINASES; RIBOSOMAL PROTEIN S6 KINASES, 70-KDA; TRANSGENES;

EID: 84892398602     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2886-13.2014     Document Type: Article

References (36)

1. Aguilar V, Alliouachene S, Sotiropoulos A, Sobering A, Athea Y, Djouadi F, Miraux S, Thiaudière E, Foretz M, Viollet B, Diolez P, Bastin J, Benit P, Rustin P, Carling D, Sandri M, Ventura-Clapier R, PendeM (2007) S6 kinase deletion suppresses muscle growth adaptations to nutrient availability by activating AMP kinase. Cell Metab 5:476-487. CrossRef Medline
2. Apfeld J, O'Connor G, McDonagh T, DiStefano PS, Curtis R (2004) The AMP-activated protein kinase AAK-2 links energy levels and insulin-like signals to lifespan in C. elegans. Genes Dev 18:3004-3009. CrossRef Medline
3. Blackmore MG, WangZ, Lerch JK, Motti D, ZhangYP, Shields CB, Lee JK, Goldberg JL, Lemmon VP, Bixby JL (2012) Kruppel-like Factor 7 engineered for transcriptional activationpromotesaxonregeneration in the adult corticospinal tract. Proc Natl Acad Sci US A109:7517-7522. CrossRef Medline
4. Cabreiro F, Au C, Leung KY, Vergara-Irigaray N, Cochemé HM, Noori T, Weinkove D, Schuster E, Greene ND, Gems D (2013) Metformin retards aging in C. elegans by altering microbial folate and methionine metabolism. Cell 153:228-239. CrossRef Medline
5. Cai D, Qiu J, Cao Z, McAtee M, Bregman BS, Filbin MT (2001) Neuronal cyclic AMP controls the developmental loss in ability of axons to regenerate. J Neurosci 21:4731-4739. Medline
6. Chen D, Thomas EL, Kapahi P (2009) HIF-1 modulates dietary restrictionmediated lifespan extension via IRE-1 in Caenorhabditis elegans. PLoS Genet 5:e1000486. CrossRef Medline
7. Chen L, Chisholm AD (2011) Axon regeneration mechanisms: insights from C. elegans. Trends Cell Biol 21:577-584. CrossRef Medline
8. Chen L, Wang Z, Ghosh-Roy A, Hubert T, Yan D, O'Rourke S, Bowerman B, Wu Z, Jin Y, Chisholm AD (2011) Axon regeneration pathways identified by systematic genetic screening in C. elegans. Neuron 71:1043-1057. CrossRef Medline
9. Christie KJ, Webber CA, Martinez JA, Singh B, ZochodneDW (2010) PTEN inhibition to facilitate intrinsic regenerative outgrowth of adult peripheral axons. J Neurosci 30:9306-9315. CrossRef Medline
10. El Bejjani R, Hammarlund M (2012) Notch signaling inhibits axon regeneration. Neuron 73:268-278. CrossRef Medline
11. Gao Y, Deng K, Hou J, Bryson JB, Barco A, Nikulina E, Spencer T, Mellado W, Kandel ER, Filbin MT (2004) Activated CREB is sufficient to overcome inhibitors in myelin and promote spinal axon regeneration in vivo. Neuron 44:609-621. CrossRef Medline
12. Ghosh-Roy A, Goncharov A, Jin Y, Chisholm AD (2012) Kinesin-13 and tubulin posttranslational modifications regulate microtubule growth in axon regeneration. Dev Cell 23:716-728. CrossRef Medline
13. Goldberg JL, Klassen MP, Hua Y, Barres BA (2002) Amacrine-signaled loss of intrinsic axon growth ability by retinal ganglion cells. Science 296: 1860-1864. CrossRef Medline
14. Hammarlund M, Nix P, Hauth L, Jorgensen EM, Bastiani M (2009) Axon regeneration requires a conservedMAPkinase pathway. Science 323:802-806. CrossRef Medline
15. Hawley SA, Gadalla AE, Olsen GS, Hardie DG (2002) The antidiabetic drug metformin activates the AMP-activated protein kinase cascade via an adenine nucleotide-independent mechanism. Diabetes 51:2420-2425. CrossRef Medline
16. Jenö P, Ballou LM, Novak-Hofer I, Thomas G (1988) Identification and characterization of a mitogen-activated S6 kinase. Proc Natl Acad Sci U S A 85:406-410. CrossRef Medline
17. Liu K, Tedeschi A, Park KK, He Z (2011) Neuronal intrinsic mechanisms of axon regeneration. Annu Rev Neurosci 34:131-152. CrossRef Medline
18. Lu P, Wang Y, Graham L, McHale K, Gao M, Wu D, Brock J, Blesch A, Rosenzweig ES, Havton LA, Zheng B, Conner JM, Marsala M, Tuszynski MH (2012) Long-distance growth and connectivity of neural stem cells after severe spinal cord injury. Cell 150:1264-1273. CrossRef Medline
19. Magnuson B, Ekim B, Fingar DC (2012) Regulation and function of ribosomal protein S6 kinase (S6K) within mTOR signalling networks. Biochem J 441:1-21. CrossRef Medline
20. Mair W, Morantte I, Rodrigues AP, Manning G, Montminy M, Shaw RJ, Dillin A (2011) Lifespan extension induced by AMPK and calcineurin is mediated by CRTC-1 and CREB. Nature 470:404-408. CrossRef Medline
21. Mello CC, Kramer JM, Stinchcomb D, Ambros V (1991) Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J 10:3959-3970. Medline
22. Meyuhas O (2008) Physiological roles of ribosomal protein S6: one of its kind. Int Rev Cell Mol Biol 268:1-37. CrossRef Medline
23. Mihaylova MM, Shaw RJ (2011) TheAMPKsignalling pathway coordinates cell growth, autophagy and metabolism. Nat Cell Biol 13:1016-1023. CrossRef Medline
24. Onken B, Driscoll M (2010) Metformin induces a dietary restriction-like state and the oxidative stress response to extend C. elegans healthspan via AMPK, LKB1, and SKN-1. PLoS One 5:e8758. CrossRef Medline
25. Park KK, Liu K, Hu Y, Smith PD, Wang C, Cai B, Xu B, Connolly L, Kramvis I, Sahin M, HeZ (2008) Promoting axon regeneration in the adultCNSby modulation of the PTEN/mTOR pathway. Science 322:963-966. CrossRef Medline
26. Pende M, Um SH, Mieulet V, Sticker M, Goss VL, Mestan J, Mueller M, Fumagalli S, Kozma SC, Thomas G (2004) S6K1(-/-)/S6K2(-/-) mice exhibit perinatal lethality and rapamycin-sensitive 5'-terminal oligopyrimidine mRNAtranslation and reveal a mitogen-activated protein kinase-dependent S6 kinase pathway. Mol Cell Biol 24:3112-3124. CrossRef Medline
27. Pinan-Lucarre B, Gabel CV, Reina CP, Hulme SE, Shevkoplyas SS, Slone RD, Xue J, Qiao Y, Weisberg S, Roodhouse K, Sun L, Whitesides GM, Samuel A, Driscoll M (2012) The core apoptotic executioner proteins CED-3 and CED-4 promote initiation of neuronal regeneration in Caenorhabditis elegans. PLoS Biol 10:e1001331. CrossRef Medline
28. Pullen N, ThomasG (1997) The modular phosphorylation and activation of p70s6k. FEBS Lett 410:78-82. CrossRef Medline
29. Schwab ME, Bartholdi D (1996) Degeneration and regeneration of axons in the lesioned spinal cord. Physiol Rev 76:319-370. Medline
30. Selman C, Tullet JM, Wieser D, Irvine E, Lingard SJ, Choudhury AI, Claret M, Al-Qassab H, Carmignac D, Ramadani F, WoodsA, Robinson IC, Schuster E, Batterham RL, Kozma SC, Thomas G, Carling D, Okkenhaug K, Thornton JM, Partridge L, et al. (2009) Ribosomal protein S6 kinase 1 signaling regulates mammalian life span. Science 326:140-144. CrossRef Medline
31. Sheaffer KL, Updike DL, Mango SE (2008) The Target of Rapamycin pathway antagonizes pha-4/FoxA to control development and aging. Curr Biol 18:1355-1364. CrossRef Medline
32. von Manteuffel SR, Dennis PB, Pullen N, Gingras AC, Sonenberg N, Thomas G (1997) The insulin-induced signalling pathway leading to S6 and initiation factor 4E binding protein 1 phosphorylation bifurcates at a rapamycin-sensitive point immediately upstream of p70s6k. Mol Cell Biol 17:5426-5436. Medline
33. Wu Z, Ghosh-Roy A, Yanik MF, Zhang JZ, Jin Y, Chisholm AD (2007) Caenorhabditis elegans neuronal regeneration is influenced by life stage, ephrin signaling, and synaptic branching. Proc Natl Acad Sci U S A 18: 15132-15137. CrossRef Medline
34. Yan D, Jin Y (2012) Regulation of DLK-1 kinase activity by calcium-mediated dissociation from an inhibitory isoform. Neuron 76:534-548. CrossRef Medline
35. 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 138:1005-1018. CrossRef Medline
36. Yiu G, He Z (2006) Glial inhibition of CNS axon regeneration. Nat Rev Neurosci 7:617-627. CrossRef Medline