High-mobility group box 1 induces neuron autophagy in a rat spinal root avulsion model

Neuroscience

Volumn 315, Issue , 2016, Pages 286-295

  Zhu, L ^a   Huang, G ^b   Sheng, J ^c   Fu, Q ^a   Chen, A ^a  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

^b SECOND MILITARY MEDICAL UNIVERSITY   (China)

^c SECOND MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Autophagy; HMGB1; Spinal root avulsion

Indexed keywords

HIGH MOBILITY GROUP B1 PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; MICROTUBULE ASSOCIATED PROTEIN LIGHT CHAIN 3 II; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN P62; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; ANTIBODY; HBP1 PROTEIN, RAT; NEUROPROTECTIVE AGENT;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; AVULSION INJURY; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; MALE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RAT; SPINAL CORD NERVE CELL; SPINAL CORD VENTRAL HORN; SPINAL ROOT; SPINAL ROOT AVULSION; ANIMAL; ANTAGONISTS AND INHIBITORS; ANTERIOR HORN CELL; CELL CULTURE; DISEASE MODEL; DRUG EFFECTS; INJURIES; LUMBAR VERTEBRA; METABOLISM; NERVE CELL; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT;

ANIMALS; ANTERIOR HORN CELLS; ANTIBODIES; AUTOPHAGY; CELL SURVIVAL; CELLS, CULTURED; DISEASE MODELS, ANIMAL; HMGB1 PROTEIN; LUMBAR VERTEBRAE; MALE; MAP KINASE SIGNALING SYSTEM; NEURONS; NEUROPROTECTIVE AGENTS; RATS, SPRAGUE-DAWLEY; SPINAL NERVE ROOTS;

EID: 84952705468     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2015.12.020     Document Type: Article

References (52)

1. Abraham E., Arcaroli J., Carmody A., Wang H., Tracey K.J. HMG-1 as a mediator of acute lung inflammation. J Immunol 2000, 165:2950-2954.
2. Adhami F., Liao G., Morozov Y.M., Schloemer A., Schmithorst V.J., Lorenz J.N., Dunn R.S., Vorhees C.V., Wills-Karp M., Degen J.L., Davis R.J., Mizushima N., Rakic P., Dardzinski B.J., Holland S.K., Sharp F.R., Kuan C.Y. Cerebral ischemia-hypoxia induces intravascular coagulation and autophagy. Am J Pathol 2006, 169:566-583.
3. Bjorkoy G., Lamark T., Brech A., Outzen H., Perander M., Overvatn A., Stenmark H., Johansen T. P62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J Cell Biol 2005, 171:603-614.
4. Boya P., Gonzalez-Polo R.A., Casares N., Perfettini J.L., Dessen P., Larochette N., Metivier D., Meley D., Souquere S., Yoshimori T., Pierron G., Codogno P., Kroemer G. Inhibition of macroautophagy triggers apoptosis. Mol Cell Biol 2005, 25:1025-1040.
5. Chen H.C., Fong T.H., Lee A.W., Chiu W.T. Autophagy is activated in injured neurons and inhibited by methylprednisolone after experimental spinal cord injury. Spine 2012, 37:470-475.
6. Czaja M.J., Ding W.X., Donohue T.M., Friedman S.L., Kim J.S., Komatsu M., Lemasters J.J., Lemoine A., Lin J.D., Ou J.H., Perlmutter D.H., Randall G., Ray R.B., Tsung A., Yin X.M. Functions of autophagy in normal and diseased liver. Autophagy 2013, 9:1131-1158.
7. Diskin T., Tal-Or P., Erlich S., Mizrachy L., Alexandrovich A., Shohami E., Pinkas-Kramarski R. Closed head injury induces upregulation of Beclin 1 at the cortical site of injury. J Neurotrauma 2005, 22:750-762.
8. Erlich S., Alexandrovich A., Shohami E., Pinkas-Kramarski R. Rapamycin is a neuroprotective treatment for traumatic brain injury. Neurobiol Dis 2007, 26:86-93.
9. Gardella S., Andrei C., Ferrera D., Lotti L.V., Torrisi M.R., Bianchi M.E., Rubartelli A. The nuclear protein HMGB1 is secreted by monocytes via a non-classical, vesicle-mediated secretory pathway. EMBO Rep 2002, 3:995-1001.
10. Geng Y., Kohli L., Klocke B.J., Roth K.A. Chloroquine-induced autophagic vacuole accumulation and cell death in glioma cells is p53 independent. Neuro Oncol 2010, 12:473-481.
11. Gurusamy N., Das D.K. Detection of cell death by autophagy. Methods Mol Biol 2009, 559:95-103.
12. He Y., Wan S., Hua Y., Keep R.F., Xi G. Autophagy after experimental intracerebral hemorrhage. J Cereb Blood Flow Metab 2008, 28:897-905.
13. Hommes D.W., Peppelenbosch M.P., van Deventer S.J. Mitogen activated protein (MAP) kinase signal transduction pathways and novel anti-inflammatory targets. Gut 2003, 52:144-151.
14. Jiang X.Y., Fu S.L., Nie B.M., Li Y., Lin L., Yin L., Wang Y.X., Lu P.H., Xu X.M. Methods for isolating highly-enriched embryonic spinal cord neurons: a comparison between enzymatic and mechanical dissociations. J Neurosci Methods 2006, 158:13-18.
15. Jiang X., Chen X., Shen D., Chen A. Anterior cornual motoneuron regression pattern after sacral plexus avulsion in rats. Acta Neurochir (Wien) 2014, 156:1599-1604.
16. Kanno H., Ozawa H., Sekiguchi A., Yamaya S., Itoi E. Induction of autophagy and autophagic cell death in damaged neural tissue after acute spinal cord injury in mice. Spine (Phila Pa 1976) 2011, 36:E1427-E1434.
17. Kim S.W., Lim C.M., Kim J.B., Shin J.H., Lee S., Lee M., Lee J.K. Extracellular HMGB1 released by NMDA treatment confers neuronal apoptosis via RAGE-p38 MAPK/ERK signaling pathway. Neurotox Res 2011, 20:159-169.
18. Klionsky D.J., Emr S.D. Autophagy as a regulated pathway of cellular degradation. Science 2000, 290:1717-1721.
19. Koliatsos V.E., Price W.L., Pardo C.A., Price D.L. Ventral root avulsion: an experimental model of death of adult motor neurons. J Comp Neurol 1994, 342:35-44.
20. Kondo Y., Kanzawa T., Sawaya R., Kondo S. The role of autophagy in cancer development and response to therapy. Nat Rev Cancer 2005, 5:726-734.
21. Korenic A., Andjus P., Radenovic L., Spasojevic I. The role of autophagy and lipolysis in survival of astrocytes under nutrient deprivation. Neurosci Lett 2015, 595:128-133.
22. Kroemer G., Jaattela M. Lysosomes and autophagy in cell death control. Nat Rev Cancer 2005, 5:886-897.
23. Kyriakis J.M., Avruch J. Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol Rev 2001, 81:807-869.
24. Levine B., Kroemer G. Autophagy in the pathogenesis of disease. Cell 2008, 132:27-42.
25. Liang Y., Hou C., Kong J., Wen H., Zheng X., Wu L., Huang H., Chen Y. HMGB1 binding to receptor for advanced glycation end products enhances inflammatory responses of human bronchial epithelial cells by activating p38 MAPK and ERK1/2. Mol Cell Biochem 2015, 405:63-71.
26. Liu C.L., Chen S., Dietrich D., Hu B.R. Changes in autophagy after traumatic brain injury. J Cereb Blood Flow Metab 2008, 28:674-683.
27. Liu L., Yang M., Kang R., Wang Z., Zhao Y., Yu Y., Xie M., Yin X., Livesey K.M., Lotze M.T., Tang D., Cao L. HMGB1-induced autophagy promotes chemotherapy resistance in leukemia cells. Leukemia 2011, 25:23-31.
28. Lotze M.T., Tracey K.J. High-mobility group box 1 protein (HMGB1): nuclear weapon in the immune arsenal. Nat Rev Immunol 2005, 5:331-342.
29. Mantell L.L., Parrish W.R., Ulloa L. Hmgb-1 as a therapeutic target for infectious and inflammatory disorders. Shock 2006, 25:4-11.
30. Mizushima N. Methods for monitoring autophagy. Int J Biochem Cell Biol 2004, 36:2491-2502.
31. Mizushima N., Yoshimori T. How to interpret LC3 immunoblotting. Autophagy 2007, 3:542-545.
32. Mizushima N., Yoshimori T., Levine B. Methods in mammalian autophagy research. Cell 2010, 140:313-326.
33. Muller S., Scaffidi P., Degryse B., Bonaldi T., Ronfani L., Agresti A., Beltrame M., Bianchi M.E. New EMBO members' review: the double life of HMGB1 chromatin protein: architectural factor and extracellular signal. EMBO J 2001, 20:4337-4340.
34. Nixon R.A., Cataldo A.M., Mathews P.M. The endosomal-lysosomal system of neurons in Alzheimer's disease pathogenesis: a review. Neurochem Res 2000, 25:1161-1172.
35. Penas C., Pascual-Font A., Mancuso R., Fores J., Casas C., Navarro X. Sigma receptor agonist 2-(4-morpholinethyl)1 phenylcyclohexanecarboxylate (Pre084) increases GDNF and BiP expression and promotes neuroprotection after root avulsion injury. J Neurotrauma 2011, 28:831-840.
36. Qin Z.H., Gu Z.L. Huntingtin processing in pathogenesis of Huntington disease. Acta Pharmacol Sin 2004, 25:1243-1249.
37. Rabinowitz J.D., White E. Autophagy and metabolism. Science 2010, 330:1344-1348.
38. Rami A., Langhagen A., Steiger S. Focal cerebral ischemia induces upregulation of Beclin 1 and autophagy-like cell death. Neurobiol Dis 2008, 29:132-141.
39. Scaffidi P., Misteli T., Bianchi M.E. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 2002, 418:191-195.
40. Sekiguchi A., Kanno H., Ozawa H., Yamaya S., Itoi E. Rapamycin promotes autophagy and reduces neural tissue damage and locomotor impairment after spinal cord injury in mice. J Neurotrauma 2012, 29:946-956.
41. Shintani T., Klionsky D.J. Autophagy in health and disease: a double-edged sword. Science 2004, 306:990-995.
42. Suzuki C., Isaka Y., Takabatake Y., Tanaka H., Koike M., Shibata M., Uchiyama Y., Takahara S., Imai E. Participation of autophagy in renal ischemia/reperfusion injury. Biochem Biophys Res Commun 2008, 368:100-106.
43. Tang D., Shi Y., Jang L., Wang K., Xiao W., Xiao X. Heat shock response inhibits release of high mobility group box 1 protein induced by endotoxin in murine macrophages. Shock 2005, 23:434-440.
44. Tang D., Shi Y., Kang R., Li T., Xiao W., Wang H., Xiao X. Hydrogen peroxide stimulates macrophages and monocytes to actively release HMGB1. J Leukoc Biol 2007, 81:741-747.
45. Tang D., Kang R., Cheh C.W., Livesey K.M., Liang X., Schapiro N.E., Benschop R., Sparvero L.J., Amoscato A.A., Tracey K.J., Zeh H.J., Lotze M.T. HMGB1 release and redox regulates autophagy and apoptosis in cancer cells. Oncogene 2010, 29:5299-5310.
46. Tanida I., Ueno T., Kominami E. LC3 conjugation system in mammalian autophagy. Int J Biochem Cell Biol 2004, 36:2503-2518.
47. Torres-Espin A., Corona-Quintanilla D.L., Fores J., Allodi I., Gonzalez F., Udina E., Navarro X. Neuroprotection and axonal regeneration after lumbar ventral root avulsion by re-implantation and mesenchymal stem cells transplant combined therapy. Neurotherapeutics 2013, 10:354-368.
48. Tsung A., Sahai R., Tanaka H., Nakao A., Fink M.P., Lotze M.T., Yang H., Li J., Tracey K.J., Geller D.A., Billiar T.R. The nuclear factor HMGB1 mediates hepatic injury after murine liver ischemia-reperfusion. J Exp Med 2005, 201:1135-1143.
49. Wang L., Yu L., Zhang T., Wang L., Leng Z., Guan Y., Wang X. HMGB1 enhances embryonic neural stem cell proliferation by activating the MAPK signaling pathway. Biotechnol Lett 2014, 36:1631-1639.
50. Wen Y.D., Sheng R., Zhang L.S., Han R., Zhang X., Zhang X.D., Han F., Fukunaga K., Qin Z.H. Neuronal injury in rat model of permanent focal cerebral ischemia is associated with activation of autophagic and lysosomal pathways. Autophagy 2008, 4:762-769.
51. Zhang Q.Y., Wu L.Q., Zhang T., Han Y.F., Lin X. Autophagy-mediated HMGB1 release promotes gastric cancer cell survival via RAGE activation of extracellular signal-regulated kinases 1/2. Oncol Rep 2015, 33:1630-1638.
52. Zou J.Y., Crews F.T. Release of neuronal HMGB1 by ethanol through decreased HDAC activity activates brain neuroimmune signaling. PLoS One 2014, 9:e87915.