HMGB1 contributes to regeneration after spinal cord injury in adult zebrafish

Molecular Neurobiology

Volumn 49, Issue 1, 2014, Pages 472-483

  Fang, Ping ^a   Pan, Hong Chao ^a   Lin, Stanley Li ^a   Zhang, Wen Qing ^c   Rauvala, Heikki ^d   Schachner, Melitta ^a   Shen, Yan Qin ^a,b  

^a SHANTOU UNIVERSITY MEDICAL COLLEGE   (China)

^b JIANGNAN UNIVERSITY   (China)

^c SOUTHERN MEDICAL UNIVERSITY   (China)

^d UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Amphoterin; HMGB1; Neurovascular; Regeneration; Spinal cord injury; Zebrafish

Indexed keywords

GREEN FLUORESCENT PROTEIN; HIGH MOBILITY GROUP B1 PROTEIN; MESSENGER RNA; MORPHOLINO OLIGONUCLEOTIDE;

ADULT; ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; CELL NUCLEUS; CONTROLLED STUDY; CYTOPLASM; ENDOTHELIUM CELL; IMMUNOFLUORESCENCE; IMMUNOHISTOLOGY; IN SITU HYBRIDIZATION; INFLAMMATION; MOTONEURON NUCLEUS; NERVE FIBER GROWTH; NERVE REGENERATION; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVIEW; SPINAL CORD INJURY; SPINAL CORD REGENERATION; SPINAL CORD TRANSSECTION; TRANSGENIC ANIMAL; WESTERN BLOTTING; ZEBRA FISH;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; HMGB1 PROTEIN; NERVE REGENERATION; RECOVERY OF FUNCTION; SPINAL CORD INJURIES; ZEBRAFISH;

EID: 84894374794     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-013-8533-4     Document Type: Review

References (41)

1. Ma L, Yu YM, Guo Y, Hart RP, Schachner M (2012) Cysteine- and glycine-rich protein 1a is involved in spinal cord regeneration in adult zebrafish. Eur J Neurosci 35:353-365
2. Fang P, Schachner M, Shen YQ (2012) HMGB1 in development and diseases of the central nervous system. Mol Neurobiol 45:499-506
3. Guazzi S, Strangio A, Franzi AT, Bianchi ME (2003) HMGB1, an architectural chromatin protein and extracellular signalling factor, has a spatially and temporally restricted expression pattern in mouse brain. Gene Expr Patterns 3:29-33
4. Enokido Y, Yoshitake A, Ito H, Okazawa H (2008) Age-dependent change of HMGB1 and DNA double-strand break accumulation in mouse brain. Biochem Biophys Res Commun 376:128-133
5. Daston MM, Ratner N (1994) Amphoterin (P30, HMG-1) and RIP are early markers of oligodendrocytes in the developing rat spinal cord. J Neurocytol 23:323-332
6. Tenenbaum T, Essmann F, Adam R, Seibt A, Janicke RU, Novotny GE, Galla HJ, Schroten H (2006) Cell death, caspase activation, and HMGB1 release of porcine choroid plexus epithelial cells during Streptococcus suis infection in vitro. Brain Res 1100:1-12
7. Gao HM, Zhou H, Zhang F, Wilson BC, Kam W, Hong JS (2011) HMGB1 acts on microglia Mac1 to mediate chronic neuroinflammation that drives progressive neurodegeneration. J Neurosci 31:1081-1092
8. Zhao X, Kuja-Panula J, Rouhiainen A, Chen YC, Panula P, Rauvala H (2011) High mobility group box-1 (HMGB1; amphoterin) is required for zebrafish brain development. J Biol Chem 286:23200-23213
9. Chou DK, Evans JE, Jungalwala FB (2001) Identity of nuclear high-mobility-group protein, HMG-1, and sulfoglucuronyl carbohydrate-binding protein, SBP-1, in brain. J Neurochem 77:120-131
10. Merenmies J, Pihlaskari R, Laitinen J, Wartiovaara J, Rauvala H (1991) 30-kDa heparin-binding protein of brain (amphoterin) involved in neurite outgrowth. Amino acid sequence and localization in the filopodia of the advancing plasma membrane. J Biol Chem 266:16722-16729
11. Rauvala H, Pihlaskari R (1987) Isolation and some characteristics of an adhesive factor of brain that enhances neurite outgrowth in central neurons. J Biol Chem 262:16625-16635
12. Kawabata H, Setoguchi T, Yone K, Souda M, Yoshida H, Kawahara K, Maruyama I, Komiya S (2010) High mobility group box 1 is upregulated after spinal cord injury and is associated with neuronal cell apoptosis. Spine 35:1109-1115 (Phila Pa 1976)
13. Kim JB, Sig Choi J, Yu YM, Nam K, Piao CS, Kim SW, Lee MH, Han PL, Park JS, Lee JK (2006) HMGB1, a novel cytokine-like mediator linking acute neuronal death and delayed neuroinflammation in the postischemic brain. J Neurosci 26:6413-6421
14. Blanco P, Palucka AK, Pascual V, Banchereau J (2008) Dendritic cells and cytokines in human inflammatory and autoimmune diseases. Cytokine Growth Factor Rev 19:41-52
15. Rauvala H, Rouhiainen A (2010) Physiological and pathophysiological outcomes of the interactions of HMGB1 with cell surface receptors. Biochim Biophys Acta 1799:164-170
16. Tian J, Avalos AM, Mao SY, Chen B, Senthil K, Wu H, Parroche P, Drabic S, Golenbock D, Sirois C et al (2007) Toll-like receptor 9-dependent activation by DNA-containing immune complexes is mediated by HMGB1 and RAGE. Nat Immunol 8:487-496
17. Urbonaviciute V, Furnrohr BG, Meister S, Munoz L, Heyder P, De Marchis F, Bianchi ME, Kirschning C, Wagner H, Manfredi AA et al (2008) Induction of inflammatory and immune responses by HMGB1-nucleosome complexes: implications for the pathogenesis of SLE. J Exp Med 205:3007-3018
18. Wahamaa H, Schierbeck H, Hreggvidsdottir HS, Palmblad K, Aveberger AC, Andersson U, Harris HE (2011) High mobility group box protein 1 in complex with lipopolysaccharide or IL-1 promotes an increased inflammatory phenotype in synovial fibroblasts. Arthritis Res Ther 13:R136
19. Huang Y, Xie K, Li J, Xu N, Gong G, Wang G, Yu Y, Dong H, Xiong L (2011) Beneficial effects of hydrogen gas against spinal cord ischemia-reperfusion injury in rabbits. Brain Res 10:125-136
20. Wang Q, Ding Q, Zhou Y, Gou X, Hou L, Chen S, Zhu Z, Xiong L (2009) Ethyl pyruvate attenuates spinal cord ischemic injury with a wide therapeutic window through inhibiting high-mobility group box 1 release in rabbits. Anesthesiology 110:1279-1286
21. Shibasaki M, Sasaki M, Miura M, Mizukoshi K, Ueno H, Hashimoto S, Tanaka Y, Amaya F (2010) Induction of high mobility group box-1 in dorsal root ganglion contributes to pain hypersensitivity after peripheral nerve injury. Pain 149:514-521
22. Hayakawa K, Pham LD, Katusic ZS, Arai K, Lo EH (2012) Astrocytic high-mobility group box 1 promotes endothelial progenitor cell-mediated neurovascular remodeling during stroke recovery. Proc Natl Acad Sci U S A 109:7505-7510
23. Lawson ND, Weinstein BM (2002) In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev Biol 248:307-318
24. Fang P, Lin JF, Pan HC, Shen YQ, Schachner M (2012) A surgery protocol for adult zebrafish spinal cord injury. J Genet Genomics 39:481-487
25. Goff LA, Bowers J, Schwalm J, Howerton K, Getts RC, Hart RP (2004) Evaluation of sense-strand mRNA amplification by comparative quantitative PCR. BMC Genomics 5:76
26. Song G, Li Q, Long Y, Hackett PB, Cui Z (2012) Effective expression-independent gene trapping and mutagenesis mediated by Sleeping Beauty transposon. J Genet Genomics 39:503-520
27. Pei DS, Sun YH, Chen SP, Wang YP, Hu W, Zhu ZY (2007) Zebrafish GAPDH can be used as a reference gene for expression analysis in cross-subfamily cloned embryos. Analytical biochemistry 363:291-293
28. Bernhardt RR, Tongiorgi E, Anzini P, Schachner M (1996) Increased expression of specific recognition molecules by retinal ganglion cells and by optic pathway glia accompanies the successful regeneration of retinal axons in adult zebrafish. J Comp Neurol 376:253-264
29. Lin JF, Pan HC, Ma LP, Shen YQ, Schachner M (2012) The Cell Neural Adhesion Molecule Contactin-2 (TAG-1) is beneficial for functional recovery after spinal cord injury in adult zebrafish. PLoS One 7:e52376
30. Guo Y, Ma L, Cristofanilli M, Hart RP, Hao A, Schachner M (2011) Transcription factor Sox11b is involved in spinal cord regeneration in adult zebrafish. Neuroscience 172:329-341
31. Pan HC, Lin JF, Ma LP, Shen YQ, Schachner M (2013) Major vault protein promotes locomotor recovery and regeneration after spinal cord injury in adult zebrafish. Eur J Neurosci 37:203-211
32. Nasevicius A, Ekker SC (2000) Effective targeted gene 'knockdown' in zebrafish. Nat Genet 26:216-220
33. Becker CG, Lieberoth BC, Morellini F, Feldner J, Becker T, Schachner M (2004) L1.1 is involved in spinal cord regeneration in adult zebrafish. J Neurosci 24:7837-7842
34. Becker T, Wullimann MF, Becker CG, Bernhardt RR, Schachner M (1997) Axonal regrowth after spinal cord transection in adult zebrafish. J Comp Neurol 377:577-595
35. Yu YM, Cristofanilli M, Valiveti A, Ma L, Yoo M, Morellini F, Schachner M (2011) The extracellular matrix glycoprotein tenascin-C promotes locomotor recovery after spinal cord injury in adult zebrafish. Neuroscience 183:238-250
36. Hugnot JP, Franzen R (2011) The spinal cord ependymal region: a stem cell niche in the caudal central nervous system. Front Biosci 16:1044-1059
37. Becker T, Becker CG (2001) Regenerating descending axons preferentially reroute to the gray matter in the presence of a general macrophage/microglial reaction caudal to a spinal transection in adult zebrafish. J Comp Neurol 433:131-147
38. Muhammad S, Barakat W, Stoyanov S, Murikinati S, Yang H, Tracey KJ, Bendszus M, Rossetti G, Nawroth PP, Bierhaus A et al (2008) The HMGB1 receptor RAGE mediates ischemic brain damage. J Neurosci 28:12023-12031
39. Kyritsis N, Kizil C, Zocher S, Kroehne V, Kaslin J, Freudenreich D, Iltzsche A, Brand M (2012) Acute inflammation initiates the regenerative response in the adult zebrafish brain. Science 338:1353-1356
40. Kitahara T, Takeishi Y, Harada M, Niizeki T, Suzuki S, Sasaki T, Ishino M, Bilim O, Nakajima O, Kubota I (2008) High-mobility group box 1 restores cardiac function after myocardial infarction in transgenic mice. Cardiovasc Res 80:40-46
41. Lei C, Lin S, Zhang C, Tao W, Dong W, Hao Z, Liu M, Wu B (2013) Effects of high-mobility group box1 on cerebral angiogenesis and neurogenesis after intracerebral hemorrhage. Neuroscience 229:12-19