Early and sustained activation of autophagy in degenerating axons after spinal cord injury

Brain Pathology

Volumn 25, Issue 2, 2015, Pages 157-170

  Ribas, Vinicius Toledo ^a   Schnepf, Bianca ^a   Challagundla, Malleswari ^a   Koch, Jan Christoph ^a   Bähr, Mathias ^a,b   Lingor, Paul ^a,b  

^a UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^b Center for Nanoscale Microscopy and Molecular Physiology of the Brain (CNMPB)   (Germany)

Author keywords

Atg5; Atg7; autophagosome; axonal lesion; LC3; ULK1

Indexed keywords

AUTOPHAGY PROTEIN 5; AUTOPHAGY PROTEIN 7; PROTEIN; UNC 51 LIKE KINASE 1 PROTEIN; UNCLASSIFIED DRUG; ATG5 PROTEIN, RAT; ATG7 PROTEIN, RAT; LC3 PROTEIN, RAT; MICROTUBULE ASSOCIATED PROTEIN; SIGNAL PEPTIDE; UBIQUITIN PROTEIN LIGASE; ULK1 PROTEIN, RAT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; BRAIN MITOCHONDRION; CELL VACUOLE; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOSKELETON; ELECTRON MICROSCOPY; FEMALE; FLUORESCENCE MICROSCOPY; IMMUNOHISTOCHEMISTRY; NERVE FIBER; NERVE FIBER DEGENERATION; NONHUMAN; OLIGODENDROGLIA; QUANTITATIVE ANALYSIS; RAT; REGULATORY MECHANISM; RUBROSPINAL TRACT; SPINAL CORD INJURY; UPREGULATION; ANIMAL; METABOLISM; NERVE DEGENERATION; PATHOLOGY; ULTRASTRUCTURE; WISTAR RAT;

ANIMALS; AUTOPHAGY; AXONS; FEMALE; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; NERVE DEGENERATION; PROTEINS; RATS; RATS, WISTAR; SPINAL CORD INJURIES; UBIQUITIN-ACTIVATING ENZYMES; UP-REGULATION;

EID: 84922741226     PISSN: 10156305     EISSN: 17503639     Source Type: Journal    
DOI: 10.1111/bpa.12170     Document Type: Article

References (37)

1. Chan EYW, Kir S, Tooze SA, (2007) Sirna screening of the kinome identifies ULK1 as a multidomain modulator of autophagy. J Biol Chem 282: 25464-25474.
2. Chen H-C, Fong T-H, Lee A-W, Chiu W-T, (2012) Autophagy is activated in injured neurons and inhibited by methylprednisolone after experimental spinal cord injury. Spine (Phila. PA. 1976) 37: 470-475.
3. Cheng H-C, Kim SR, Oo TF, Kareva T, Yarygina O, Rzhetskaya M, et al (2011) Akt suppresses retrograde degeneration of dopaminergic axons by inhibition of macroautophagy. J Neurosci 31: 2125-2135.
4. Geng J, Klionsky DJ, (2008) The atg8 and atg12 ubiquitin-like conjugation systems in macroautophagy. "Protein modifications: beyond the usual suspects" review series. EMBO Rep 9: 859-864.
5. Ghislat G, Patron M, Rizzuto R, Knecht E, (2012) Withdrawal of essential amino acids increases autophagy by a pathway involving Ca2+/calmodulin- dependent kinase kinase- (CaMKK-). J Biol Chem 287: 38625-38636.
6. Gumy LF, Tan CL, Fawcett JW, (2010) The role of local protein synthesis and degradation in axon regeneration. Exp Neurol 223: 28-37.
7. Hao H-H, Wang L, Guo Z-J, Bai L, Zhang R-P, Shuang W-B, et al (2013) Valproic acid reduces autophagy and promotes functional recovery after spinal cord injury in rats. Neurosci Bull 29: 484-492.
8. Hara T, Nakamura K, Matsui M, Yamamoto A, Nakahara Y, Suzuki-Migishima R, et al (2006) Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 441: 885-889.
9. Hosokawa N, Hara T, Kaizuka T, Kishi C, Takamura A, Miura Y, et al (2009) Nutrient-dependent mtorc1 association with the ULK1-Atg13-FIP200 complex required for autophagy. Mol Biol Cell 20: 1981-1991.
10. Hou H, Zhang L, Zhang L, Tang P, (2014) Acute spinal cord injury in rats should target activated autophagy. J Neurosurg Spine 20: 568-577.
11. Ichimura Y, Kirisako T, Takao T, Satomi Y, Shimonishi Y, Ishihara N, et al (2000) A ubiquitin-like system mediates protein lipidation. Nature 408: 488-492.
12. Itakura E, Mizushima N, (2010) Characterization of autophagosome formation site by a hierarchical analysis of mammalian atg proteins. Autophagy 6: 764-776.
13. Jung CH, Jun CB, Ro S-H, Kim Y-M, Otto NM, Cao J, et al (2009) ULK-Atg13-FIP200 complexes mediate mTOR signaling to the autophagy machinery. Mol Biol Cell 20: 1992-2003.
14. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, et al (2000) LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 19: 5720-5728.
15. Kanno H, Ozawa H, Sekiguchi A, Itoi E, (2009) Spinal cord injury induces upregulation of Beclin 1 and promotes autophagic cell death. Neurobiol Dis 33: 143-148.
16. Kanno H, Ozawa H, Sekiguchi A, Yamaya S, Itoi E, (2011) Induction of autophagy and autophagic cell death in damaged neural tissue after acute spinal cord injury in mice. Spine (Phila, PA 1976) 36: E1427-E1434.
17. Kerschensteiner M, Schwab ME, Lichtman JW, Misgeld T, (2005) In vivo imaging of axonal degeneration and regeneration in the injured spinal cord. Nat Med 11: 572-577.
18. Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, et al (2012) Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 8: 445-544.
19. Knöferle J, Koch JC, Ostendorf T, Michel U, Planchamp V, Vutova P, et al (2010) Mechanisms of acute axonal degeneration in the optic nerve in vivo. Proc Natl Acad Sci USA 107: 6064-6069.
20. Komatsu M, Wang QJ, Holstein GR, Friedrich VL, Iwata J, Kominami E, et al (2007) Essential role for autophagy protein atg7 in the maintenance of axonal homeostasis and the prevention of axonal degeneration. Proc Natl Acad Sci USA 104: 14489-14494.
21. Lingor P, Koch JC, Tönges L, Bähr M, (2012) Axonal degeneration as a therapeutic target in the CNS. Cell Tissue Res 349: 289-311.
22. Maday S, Wallace KE, Holzbaur ELF, (2012) Autophagosomes initiate distally and mature during transport toward the cell soma in primary neurons. J Cell Biol 196: 407-417.
23. Mizushima N, Kuma A, Kobayashi Y, Yamamoto A, Matsubae M, Takao T, et al (2003) Mouse apg16l, a novel wd-repeat protein, targets to the autophagic isolation membrane with the apg12-apg5 conjugate. J Cell Sci 116: 1679-1688.
24. Mizushima N, Noda T, Yoshimori T, Tanaka Y, Ishii T, George MD, et al (1998) A protein conjugation system essential for autophagy. Nature 395: 395-398.
25. Mizushima N, Yamamoto A, Hatano M, Kobayashi Y, Kabeya Y, Suzuki K, et al (2001) Dissection of autophagosome formation using apg5-deficient mouse embryonic stem cells. J Cell Biol 152: 657-668.
26. Raff MC, Whitmore A V, Finn JT, (2002) Axonal self-destruction and neurodegeneration. Science 296: 868-871.
27. Roberts-Lewis JM, Savage MJ, Marcy VR, Pinsker LR, Siman R, (1994) Immunolocalization of calpain i-mediated spectrin degradation to vulnerable neurons in the ischemic gerbil brain. J Neurosci 14: 3934-3944.
28. Rubinsztein DC, Difiglia M, Heintz N, Nixon RA, Qin Z, Ravikumar B, et al (2005) Autophagy and its possible roles in nervous system diseases. Autophagy 1: 11-22.
29. Shang L, Chen S, Du F, Li S, Zhao L, Wang X, (2011) Nutrient starvation elicits an acute autophagic response mediated by ULK1 dephosphorylation and its subsequent dissociation from AMPK. Proc Natl Acad Sci USA 108: 4788-4793.
30. Shi Y, Kim S, Huff TB, Borgens RB, Park K, Shi R, Cheng J-X, (2010) Effective repair of traumatically injured spinal cord by nanoscale block copolymer micelles. Nat Nanotechnol 5: 80-87.
31. Smith PM, Jeffery ND, (2006) Histological and ultrastructural analysis of white matter damage after naturally-occurring spinal cord injury. Brain Pathol 16: 99-109.
32. Tang P, Hou H, Zhang L, Lan X, Mao Z, Liu D, et al (2013) Autophagy reduces neuronal damage and promotes locomotor recovery via inhibition of apoptosis after spinal cord injury in rats. Mol Neurobiol 49: 276-287.
33. Yang Y, Coleman M, Zhang L, Zheng X, Yue Z, (2013) Autophagy in axonal and dendritic degeneration. Trends Neurosci 36: 418-428.
34. Yang Y, Fukui K, Koike T, Zheng X, (2007) Induction of autophagy in neurite degeneration of mouse superior cervical ganglion neurons. Eur J Neurosci 26: 2979-2988.
35. Yang Y, Xu K, Koike T, Zheng X, (2008) Transport of autophagosomes in neurites of pc12 cells during serum deprivation. Autophagy 4: 243-245.
36. Yang Z, Klionsky DJ, (2010) Mammalian autophagy: core molecular machinery and signaling regulation. Curr Opin Cell Biol 22: 124-131.
37. Yue Z, (2007) Regulation of neuronal autophagy in axon: implication of autophagy in axonal function and dysfunction/degeneration. Autophagy 3: 139-141.