Injury-Induced Decline of Intrinsic Regenerative Ability Revealed by Quantitative Proteomics

Neuron

Volumn 86, Issue 4, 2015, Pages 1000-1014

  Belin, Stephane ^a   Nawabi, Homaira ^a   Wang, Chen ^a   Tang, Shaojun ^a   Latremoliere, Alban ^a   Warren, Peter ^a   Schorle, Hubert ^b   Uncu, Ceren ^a   Woolf, Clifford J ^a   He, Zhigang ^a   Steen, Judith A ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF BONN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HUNTINGTIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MYC PROTEIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; SUPPRESSOR OF CYTOKINE SIGNALING 3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL GROWTH; CELL METABOLISM; CELL REGENERATION; CELL SURVIVAL; CONTROLLED STUDY; CYTOSKELETON; DOWN REGULATION; MOUSE; NERVE FIBER REGENERATION; NONHUMAN; OPTIC NERVE; OPTIC NERVE INJURY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEOMICS; RETINA GANGLION CELL; ANIMAL; C57BL MOUSE; DISEASE MODEL; METABOLISM; NERVE CELL; NERVE FIBER; NERVE FIBER TRANSECTION; NERVE REGENERATION; PATHOLOGY; PHYSIOLOGY; PROCEDURES; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

ANIMALS; AXONS; AXOTOMY; CELL SURVIVAL; DISEASE MODELS, ANIMAL; MICE, INBRED C57BL; MICE, TRANSGENIC; NERVE REGENERATION; NEURONS; OPTIC NERVE; OPTIC NERVE INJURIES; PROTEOMICS; RETINAL GANGLION CELLS; SIGNAL TRANSDUCTION;

EID: 84929858738     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2015.03.060     Document Type: Article

References (56)

1. Bareyre F.M., Kerschensteiner M., Raineteau O., Mettenleiter T.C., Weinmann O., Schwab M.E. The injured spinal cord spontaneously forms a new intraspinal circuit in adult rats. Nat. Neurosci. 2004, 7:269-277.
2. Blackmore M.G., Wang Z., Lerch J.K., Motti D., Zhang Y.P., Shields C.B., Lee J.K., Goldberg J.L., Lemmon V.P., Bixby J.L. Krüppel-like Factor 7 engineered for transcriptional activation promotes axon regeneration in the adult corticospinal tract. Proc. Natl. Acad. Sci. USA 2012, 109:7517-7522.
3. Bradke F., Fawcett J.W., Spira M.E. Assembly of a new growth cone after axotomy: the precursor to axon regeneration. Nat. Rev. Neurosci. 2012, 13:183-193.
4. Cai D., Qiu J., Cao Z., McAtee M., Bregman B.S., Filbin M.T. Neuronal cyclic AMP controls the developmental loss in ability of axons to regenerate. J.Neurosci. 2001, 21:4731-4739.
5. Chen A., Springer J.E. Neuroproteomic methods in spinal cord injury. Methods Mol. Biol. 2009, 566:57-67.
6. Chen L., Wang Z., Ghosh-Roy A., Hubert T., Yan D., O'Rourke S., Bowerman B., Wu Z., Jin Y., Chisholm A.D. Axon regeneration pathways identified by systematic genetic screening in C.elegans. Neuron 2011, 71:1043-1057.
7. Chierzi S., Ratto G.M., Verma P., Fawcett J.W. The ability ofaxons to regenerate their growth cones depends on axonal type and age, and is regulated by calcium, cAMP and ERK. Eur. J. Neurosci. 2005, 21:2051-2062.
8. Costigan M., Befort K., Karchewski L., Griffin R.S., D'Urso D., Allchorne A., Sitarski J., Mannion J.W., Pratt R.E., Woolf C.J. Replicate high-density rat genome oligonucleotide microarrays reveal hundreds of regulated genes in the dorsal root ganglion after peripheral nerve injury. BMC Neurosci. 2002, 3:16.
9. Dang C.V. MYC, metabolism, cell growth, and tumorigenesis. Cold Spring Harb. Perspect. Med. 2013, 3:a014217.
10. de Lima S., Koriyama Y., Kurimoto T., Oliveira J.T., Yin Y., Li Y., Gilbert H.Y., Fagiolini M., Martinez A.M., Benowitz L. Full-length axon regeneration in the adult mouse optic nerve and partial recovery of simple visual behaviors. Proc. Natl. Acad. Sci. USA 2012, 109:9149-9154.
11. Dodt H.U., Leischner U., Schierloh A., Jährling N., Mauch C.P., Deininger K., Deussing J.M., Eder M., Zieglgänsberger W., Becker K. Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain. Nat. Methods 2007, 4:331-336.
12. Dupraz S., Grassi D., Karnas D., Nieto Guil A.F., Hicks D., Quiroga S. The insulin-like growth factor 1 receptor is essential for axonal regeneration in adult central nervous system neurons. PLoS ONE 2013, 8:e54462.
13. Fawcett J.W. Overcoming inhibition in the damaged spinal cord. J.Neurotrauma 2006, 23:371-383.
14. Filbin M.T. Myelin-associated inhibitors of axonal regeneration in the adult mammalian CNS. Nat. Rev. Neurosci. 2003, 4:703-713.
15. Fischer D., Petkova V., Thanos S., Benowitz L.I. Switching mature retinal ganglion cells to a robust growth state invivo: gene expression and synergy with RhoA inactivation. J.Neurosci. 2004, 24:8726-8740.
16. Ghosh-Roy A., Wu Z., Goncharov A., Jin Y., Chisholm A.D. Calcium and cyclic AMP promote axonal regeneration in Caenorhabditis elegans and require DLK-1 kinase. J.Neurosci. 2010, 30:3175-3183.
17. Goldberg J.L., Espinosa J.S., Xu Y., Davidson N., Kovacs G.T., Barres B.A. Retinal ganglion cells do not extend axons by default: promotion by neurotrophic signaling and electrical activity. Neuron 2002, 33:689-702.
18. Goldberg J.L., Klassen M.P., Hua Y., Barres B.A. Amacrine-signaled loss of intrinsic axon growth ability by retinal ganglion cells. Science 2002, 296:1860-1864.
19. Griffin T.J., Xie H., Bandhakavi S., Popko J., Mohan A., Carlis J.V., Higgins L. iTRAQ reagent-based quantitative proteomic analysis on a linear ion trap mass spectrometer. J.Proteome Res. 2007, 6:4200-4209.
20. Guertin D.A., Sabatini D.M. Defining the role of mTOR in cancer. Cancer Cell 2007, 12:9-22.
21. Hammarlund M., Nix P., Hauth L., Jorgensen E.M., Bastiani M. Axon regeneration requires a conserved MAP kinase pathway. Science 2009, 323:802-806.
22. Harel N.Y., Yigitkanli K., Fu Y., Cafferty W.B., Strittmatter S.M. Multimodal exercises simultaneously stimulating cortical and brainstem pathways after unilateral corticospinal lesion. Brain Res. 2013, 1538:17-25.
23. Holtmaat A., Svoboda K. Experience-dependent structural synaptic plasticity in the mammalian brain. Nat. Rev. Neurosci. 2009, 10:647-658.
24. Howell J.J., Ricoult S.J., Ben-Sahra I., Manning B.D. A growing role for mTOR in promoting anabolic metabolism. Biochem. Soc. Trans. 2013, 41:906-912.
25. Jäger R., Maurer J., Jacob A., Schorle H. Cell type-specific conditional regulation of the c-myc proto-oncogene by combining Cre/loxP recombination and tamoxifen-mediated activation. Genesis 2004, 38:145-150.
26. Kim M.S., Pinto S.M., Getnet D., Nirujogi R.S., Manda S.S., Chaerkady R., Madugundu A.K., Kelkar D.S., Isserlin R., Jain S., et al. A draft map of the human proteome. Nature 2014, 509:575-581.
27. Laplante M., Sabatini D.M. mTOR signaling in growth control and disease. Cell 2012, 149:274-293.
28. Lin C.Y., Lovén J., Rahl P.B., Paranal R.M., Burge C.B., Bradner J.E., Lee T.I., Young R.A. Transcriptional amplification in tumor cells with elevated c-Myc. Cell 2012, 151:56-67.
29. Liu K., Lu Y., Lee J.K., Samara R., Willenberg R., Sears-Kraxberger I., Tedeschi A., Park K.K., Jin D., Cai B., et al. PTEN deletion enhances the regenerative ability of adult corticospinal neurons. Nat. Neurosci. 2010, 13:1075-1081.
30. Luo X., Salgueiro Y., Beckerman S.R., Lemmon V.P., Tsoulfas P., Park K.K. Three-dimensional evaluation of retinal ganglion cell axon regeneration and pathfinding in whole mouse tissue after injury. Exp. Neurol. 2013, 247:653-662.
31. Magharious M., D'Onofrio P.M., Hollander A., Zhu P., Chen J., Koeberle P.D. Quantitative iTRAQ analysis of retinal ganglion cell degeneration after optic nerve crush. J.Proteome Res. 2011, 10:3344-3362.
32. Michaelevski I., Segal-Ruder Y., Rozenbaum M., Medzihradszky K.F., Shalem O., Coppola G., Horn-Saban S., Ben-Yaakov K., Dagan S.Y., Rishal I., et al. Signaling to transcription networks in the neuronal retrograde injury response. Sci. Signal. 2010, 3:ra53.
33. Moore D.L., Blackmore M.G., Hu Y., Kaestner K.H., Bixby J.L., Lemmon V.P., Goldberg J.L. KLF family members regulate intrinsic axon regeneration ability. Science 2009, 326:298-301.
34. Nawabi H., Briançon-Marjollet A., Clark C., Sanyas I., Takamatsu H., Okuno T., Kumanogoh A., Bozon M., Takeshima K., Yoshida Y., et al. A midline switch of receptor processing regulates commissural axon guidance in vertebrates. Genes Dev. 2010, 24:396-410.
35. Near S.L., Whalen L.R., Miller J.A., Ishii D.N. Insulin-like growth factor II stimulates motor nerve regeneration. Proc. Natl. Acad. Sci. USA 1992, 89:11716-11720.
36. Nie Z., Hu G., Wei G., Cui K., Yamane A., Resch W., Wang R., Green D.R., Tessarollo L., Casellas R., et al. c-Myc is a universal amplifier of expressed genes in lymphocytes and embryonic stem cells. Cell 2012, 151:68-79.
37. Park K.K., Liu K., Hu Y., Smith P.D., Wang C., Cai B., Xu B., Connolly L., Kramvis I., Sahin M., He Z. Promoting axon regeneration in the adult CNS by modulation of the PTEN/mTOR pathway. Science 2008, 322:963-966.
38. Park J., Al-Ramahi I., Tan Q., Mollema N., Diaz-Garcia J.R., Gallego-Flores T., Lu H.C., Lagalwar S., Duvick L., Kang H., et al. RAS-MAPK-MSK1 pathway modulates ataxin 1 protein levels and toxicity in SCA1. Nature 2013, 498:325-331.
39. Raineteau O., Schwab M.E. Plasticity of motor systems after incomplete spinal cord injury. Nat. Rev. Neurosci. 2001, 2:263-273.
40. Rosenzweig E.S., Courtine G., Jindrich D.L., Brock J.H., Ferguson A.R., Strand S.C., Nout Y.S., Roy R.R., Miller D.M., Beattie M.S., et al. Extensive spontaneous plasticity of corticospinal projections after primate spinal cord injury. Nat. Neurosci. 2010, 13:1505-1510.
41. Rossi F., Gianola S., Corvetti L. Regulation of intrinsic neuronal properties for axon growth and regeneration. Prog. Neurobiol. 2007, 81:1-28.
42. Saul K.E., Koke J.R., García D.M. Activating transcription factor 3 (ATF3) expression in the neural retina and optic nerve of zebrafish during optic nerve regeneration. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2010, 155:172-182.
43. Shaw R.J., Cantley L.C. Ras, PI(3)K and mTOR signalling controls tumour cell growth. Nature 2006, 441:424-430.
44. Smith P.D., Sun F., Park K.K., Cai B., Wang C., Kuwako K., Martinez-Carrasco I., Connolly L., He Z. SOCS3 deletion promotes optic nerve regeneration invivo. Neuron 2009, 64:617-623.
45. Staab C.A., Ceder R., Jägerbrink T., Nilsson J.A., Roberg K., Jörnvall H., Höög J.O., Grafström R.C. Bioinformatics processing of protein and transcript profiles of normal and transformed cell lines indicates functional impairment of transcriptional regulators in buccal carcinoma. J.Proteome Res. 2007, 6:3705-3717.
46. Sun F., Park K.K., Belin S., Wang D., Lu T., Chen G., Zhang K., Yeung C., Feng G., Yankner B.A., et al. Sustained axon regeneration induced by co-deletion of PTEN and SOCS3. Nature 2011, 480:372-375.
47. Sung Y.J., Povelones M., Ambron R.T. RISK-1: a novel MAPK homologue in axoplasm that is activated and retrogradely transported after nerve injury. J.Neurobiol. 2001, 47:67-79.
48. Tanabe K., Bonilla I., Winkles J.A., Strittmatter S.M. Fibroblast growth factor-inducible-14 is induced in axotomized neurons and promotes neurite outgrowth. J.Neurosci. 2003, 23:9675-9686.
49. Thompson A., Schäfer J., Kuhn K., Kienle S., Schwarz J., Schmidt G., Neumann T., Johnstone R., Mohammed A.K., Hamon C. Tandem mass tags: a novel quantification strategy for comparative analysis of complex protein mixtures by MS/MS. Anal. Chem. 2003, 75:1895-1904.
50. Toth C., Brussee V., Martinez J.A., McDonald D., Cunningham F.A., Zochodne D.W. Rescue and regeneration of injured peripheral nerve axons by intrathecal insulin. Neuroscience 2006, 139:429-449.
51. van den Brand R., Heutschi J., Barraud Q., DiGiovanna J., Bartholdi K., Huerlimann M., Friedli L., Vollenweider I., Moraud E.M., Duis S., et al. Restoring voluntary control of locomotion after paralyzing spinal cord injury. Science 2012, 336:1182-1185.
52. Watkins T.A., Wang B., Huntwork-Rodriguez S., Yang J., Jiang Z., Eastham-Anderson J., Modrusan Z., Kaminker J.S., Tessier-Lavigne M., Lewcock J.W. DLK initiates a transcriptional program that couples apoptotic and regenerative responses to axonal injury. Proc. Natl. Acad. Sci. USA 2013, 110:4039-4044.
53. Wilhelm M., Schlegl J., Hahne H., Moghaddas Gholami A., Lieberenz M., Savitski M.M., Ziegler E., Butzmann L., Gessulat S., Marx H., et al. Mass-spectrometry-based draft of the human proteome. Nature 2014, 509:582-587.
54. Xie J., Proud C.G. Crosstalk between mTOR complexes. Nat. Cell Biol. 2013, 15:1263-1265.
55. Zhu L.Q., Zheng H.Y., Peng C.X., Liu D., Li H.L., Wang Q., Wang J.Z. Protein phosphatase 2A facilitates axonogenesis by dephosphorylating CRMP2. J.Neurosci. 2010, 30:3839-3848.
56. Zukor K., Belin S., Wang C., Keelan N., Wang X., He Z. Short hairpin RNA against PTEN enhances regenerative growth of corticospinal tract axons after spinal cord injury. J.Neurosci. 2013, 33:15350-15361.