Anti-high mobility group box 1 antibody exerts neuroprotection in a rat model of Parkinson's disease

Experimental Neurology

Volumn 275, Issue , 2016, Pages 220-231

  Sasaki, Tatsuya ^a   Liu, Keyue ^a   Agari, Takashi ^a   Yasuhara, Takao ^a   Morimoto, Jun ^a   Okazaki, Mihoko ^a   Takeuchi, Hayato ^a   Toyoshima, Atsuhiko ^a   Sasada, Susumu ^a   Shinko, Aiko ^a   Kondo, Akihiko ^a   Kameda, Masahiro ^a   Miyazaki, Ikuko ^a   Asanuma, Masato ^a   Borlongan, Cesario V ^b   Nishibori, Masahiro ^a   Date, Isao ^a  

^a OKAYAMA UNIVERSITY   (Japan)

^b UNIVERSITY OF SOUTH FLORIDA   (United States)

Author keywords

Antibody therapy; Blood brain barrier; High mobility group box 1; Inflammation; Neuroprotection; Parkinson's disease

Indexed keywords

HIGH MOBILITY GROUP B1 PROTEIN; HIGH MOBILITY GROUP BOX 1 ANTIBODY; INTERLEUKIN 1BETA; INTERLEUKIN 6; MONOCLONAL ANTIBODY; OXIDOPAMINE; UNCLASSIFIED DRUG; NEUROPROTECTIVE AGENT; NEUTRALIZING ANTIBODY;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; CELL ACTIVATION; CELL NUCLEUS; CELL TRANSPORT; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINERGIC NERVE CELL; DOPAMINERGIC TRANSMISSION; FEMALE; MICROGLIA; NERVOUS SYSTEM INFLAMMATION; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; SUBSTANTIA NIGRA PARS COMPACTA; ANIMAL; DISEASE MODEL; DRUG EFFECTS; IMMUNOLOGY; PARKINSON DISEASE, SECONDARY; PATHOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; ANTIBODIES, NEUTRALIZING; CORPUS STRIATUM; DISEASE MODELS, ANIMAL; DOPAMINERGIC NEURONS; FEMALE; HMGB1 PROTEIN; NEUROPROTECTIVE AGENTS; OXIDOPAMINE; PARKINSON DISEASE, SECONDARY; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84947798703     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2015.11.003     Document Type: Article

References (48)

1. Andrassy M., Volz H.C., Igwe J.C., Funke B., Eichberger S.N., Kaya Z., Buss S., Autschbach F., Pleger S.T., Lukic I.K., Bea F., Hardt S.E., Humpert P.M., Bianchi M.E., Mairbaurl H., Nawroth P.P., Remppis A., Katus H.A., Bierhaus A. High-mobility group box-1 in ischemia-reperfusion injury of the heart. Circulation 2008, 117:3216-3226.
2. Casula M., Iyer A.M., Spliet W.G., Anink J.J., Steentjes K., Sta M., Troost D., Aronica E. Toll-like receptor signaling in amyotrophic lateral sclerosis spinal cord tissue. Neuroscience 2011, 179:233-243.
3. Chen P.S., Peng G.S., Li G., Yang S., Wu X., Wang C.C., Wilson B., Lu R.B., Gean P.W., Chuang D.M., Hong J.S. Valproate protects dopaminergic neurons in midbrain neuron/glia cultures by stimulating the release of neurotrophic factors from astrocytes. Mol. Psychiatry 2006, 11:1116-1125.
4. Cicchetti F., Brownell A.L., Williams K., Chen Y.I., Livni E., Isacson O. Neuroinflammation of the nigrostriatal pathway during progressive 6-OHDA dopamine degeneration in rats monitored by immunohistochemistry and PET imaging. Eur. J. Neurosci. 2002, 15:991-998.
5. Depino A.M., Earl C., Kaczmarczyk E., Ferrari C., Besedovsky H., del Rey A., Pitossi F.J., Oertel W.H. Microglial activation with atypical proinflammatory cytokine expression in a rat model of Parkinson's disease. Eur. J. Neurosci. 2003, 18:2731-2742.
6. Diaz-Corrales F.J., Miyazaki I., Asanuma M., Ruano D., Rios R.M. Centrosomal aggregates and Golgi fragmentation disrupt vesicular trafficking of DAT. Neurobiol. Aging 2012, 33:2462-2477.
7. Fiuza C., Bustin M., Talwar S., Tropea M., Gerstenberger E., Shelhamer J.H., Suffredini A.F. Inflammation-promoting activity of HMGB1 on human microvascular endothelial cells. Blood 2003, 101:2652-2660.
8. Gao H.M., Zhou H., Zhang F., Wilson B.C., Kam W., Hong J.S. HMGB1 acts on microglia Mac1 to mediate chronic neuroinflammation that drives progressive neurodegeneration. J. Neurosci. 2011, 1081-1092.
9. Hamada T., Torikai M., Kuwazuru A., Tanaka M., Horai N., Fukuda T., Yamada S., Nagayama S., Hashiguchi K., Sunahara N., Fukuzaki K., Nagata R., Komiya S., Maruyama I., Fukuda T., Abeyama K. Extracellular high mobility group box chromosomal protein 1 is a coupling factor for hypoxia and inflammation in arthritis. Arthritis Rheum. 2008, 58:2675-2685.
10. He Y., Appel S., Le W. Minocycline inhibits microglial activation and protects nigral cells after 6-hydroxydopamine injection into mouse striatum. Brain Res. 2001, 909:187-193.
11. Hirsch E.C., Hunot S. Neuroinflammation in Parkinson's disease: a target for neuroprotection?. Lancet Neurol. 2009, 8:382-397.
12. Imamura K., Hishikawa N., Sawada M., Nagatsu T., Yoshida M., Hashizume Y. Distribution of major histocompatibility complex class II-positive microglia and cytokine profile of Parkinson's disease brains. Acta Neuropathol. 2003, 106:518-526.
13. Kawabata H., Setoguchi T., Yone K., Souda M., Yoshida H., Kawahara K., Maruyama I., Komiya S. High mobility group box 1 is upregulated after spinal cord injury and is associated with neuronal cell apoptosis. Spine 2010, 35:1109-1115.
14. Kim J.B., Sig Choi J., Yu Y.M., Nam K., Piao C.S., Kim S.W., Lee M.H., Han P.L., Park J.S., Lee J.K. HMGB1, a novel cytokine-like mediator linking acute neuronal death and delayed neuroinflammation in the postischemic brain. J. Neurosci. 2006, 26:6413-6421.
15. Knott C., Stern G., Kingsbury A., Welcher A.A., Wilkin G.P. Elevated glial brain-derived neurotrophic factor in Parkinson's diseased nigra. Parkinsonism Relat. Disord. 2002, 8:329-341.
16. Kortekaas R., Leenders K.L., van Oostrom J.C., Vaalburg W., Bart J., Willemsen A.T., Hendrikse N.H. Blood-brain barrier dysfunction in parkinsonian midbrain in vivo. Ann. Neurol. 2005, 57:176-179.
17. Lee H.J., Suk J.E., Patrick C., Bae E.J., Cho J.H., Rho S., Hwang D., Masliah E., Lee S.J. Direct transfer of alpha-synuclein from neuron to astroglia causes inflammatory responses in synucleinopathies. J. Biol. Chem. 2010, 285:9262-9272.
18. Lin L.F., Doherty D.H., Lile J.D., Bektesh S., Collins F. GDNF: a glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons. Science 1993, 260:1130-1132. (New York, N.Y.).
19. Lindersson E.K., Hojrup P., Gai W.P., Locker D., Martin D., Jensen P.H. Alpha-synuclein filaments bind the transcriptional regulator HMGB-1. Neuroreport 2004, 15:2735-2739.
20. Liu K., Mori S., Takahashi H.K., Tomono Y., Wake H., Kanke T., Sato Y., Hiraga N., Adachi N., Yoshino T., Nishibori M. Anti-high mobility group box 1 monoclonal antibody ameliorates brain infarction induced by transient ischemia in rats. FASEB J.: Off. Publ. Fed. Am. Soc. Exp. Biol. 2007, 21:3904-3916.
21. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)). Method. Methods 2001, 25:402-408. (San Diego, Calif.).
22. 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.
23. McGeer P.L., Itagaki S., Boyes B.E., McGeer E.G. Reactive microglia are positive for HLA-DR in the substantia nigra of Parkinson's and Alzheimer's disease brains. Neurology 1988, 38:1285-1291.
24. Miklossy J., Doudet D.D., Schwab C., Yu S., McGeer E.G., McGeer P.L. Role of ICAM-1 in persisting inflammation in Parkinson disease and MPTP monkeys. Exp. Neurol. 2006, 197:275-283.
25. More S.V., Kumar H., Kim I.S., Song S.Y., Choi D.K. Cellular and molecular mediators of neuroinflammation in the pathogenesis of Parkinson's disease. Mediat. Inflamm. 2013, 2013:952375.
26. Nakamura Y., Morioka N., Abe H., Zhang F.F., Hisaoka-Nakashima K., Liu K., Nishibori M., Nakata Y. Neuropathic pain in rats with a partial sciatic nerve ligation is alleviated by intravenous injection of monoclonal antibody to high mobility group box-1. PLoS One 2013, 8.
27. Okuma Y., Liu K., Wake H., Zhang J., Maruo T., Date I., Yoshino T., Ohtsuka A., Otani N., Tomura S., Shima K., Yamamoto Y., Yamamoto H., Takahashi H.K., Mori S., Nishibori M. Anti-high mobility group box-1 antibody therapy for traumatic brain injury. Ann. Neurol. 2012, 72:373-384.
28. Pabon M.M., Bachstetter A.D., Hudson C.E., Gemma C., Bickford P.C. CX3CL1 reduces neurotoxicity and microglial activation in a rat model of Parkinson's disease. J. Neuroinflammation 2011, 8:9.
29. Park J.S., Svetkauskaite D., He Q., Kim J.Y., Strassheim D., Ishizaka A., Abraham E. Involvement of toll-like receptors 2 and 4 in cellular activation by high mobility group box 1 protein. J. Biol. Chem. 2004, 279:7370-7377.
30. Qiu J., Nishimura M., Wang Y., Sims J.R., Qiu S., Savitz S.I., Salomone S., Moskowitz M.A. Early release of HMGB-1 from neurons after the onset of brain ischemia. J. Cereb. Blood Flow Metab. 2008, 28:927-938.
31. Raman K.G., Sappington P.L., Yang R., Levy R.M., Prince J.M., Liu S., Watkins S.K., Schmidt A.M., Billiar T.R., Fink M.P. The role of RAGE in the pathogenesis of intestinal barrier dysfunction after hemorrhagic shock. Am. J. Physiol. Gastrointest. Liver Physiol. 2006, 291:G556-G565.
32. Ransohoff R.M., Perry V.H. Microglial physiology: unique stimuli, specialized responses. Annu. Rev. Immunol. 2009, 27:119-145.
33. Roof R.L., Schielke G.P., Ren X., Hall E.D. A comparison of long-term functional outcome after 2 middle cerebral artery occlusion models in rats. Stroke; A J. Cereb. circ. 2001, 32:2648-2657.
34. Saura J., Pares M., Bove J., Pezzi S., Alberch J., Marin C., Tolosa E., Marti M.J. Intranigral infusion of interleukin-1beta activates astrocytes and protects from subsequent 6-hydroxydopamine neurotoxicity. J. Neurochem. 2003, 85:651-661.
35. Sawa H., Ueda T., Takeyama Y., Yasuda T., Shinzeki M., Nakajima T., Kuroda Y. Blockade of high mobility group box-1 protein attenuates experimental severe acute pancreatitis. World J. Gastroenterol. 2006, 12:7666-7670.
36. Schallert T., Fleming S.M., Leasure J.L., Tillerson J.L., Bland S.T. CNS plasticity and assessment of forelimb sensorimotor outcome in unilateral rat models of stroke, cortical ablation, parkinsonism and spinal cord injury. Neuropharmacology 2000, 39:777-787.
37. Shibasaki M., Sasaki M., Miura M., Mizukoshi K., Ueno H., Hashimoto S., Tanaka Y., Amaya F. Induction of high mobility group box-1 in dorsal root ganglion contributes to pain hypersensitivity after peripheral nerve injury. Pain 2010, 149:514-521.
38. Shichita T., Hasegawa E., Kimura A., Morita R., Sakaguchi R., Takada I., Sekiya T., Ooboshi H., Kitazono T., Yanagawa T., Ishii T., Takahashi H., Mori S., Nishibori M., Kuroda K., Akira S., Miyake K., Yoshimura A. Peroxiredoxin family proteins are key initiators of post-ischemic inflammation in the brain. Nat. Med. 2012, 18:911-917.
39. Shinko A., Agari T., Kameda M., Yasuhara T., Kondo A., Tayra J.T., Sato K., Sasaki T., Sasada S., Takeuchi H., Wakamori T., Borlongan C.V., Date I. Spinal cord stimulation exerts neuroprotective effects against experimental Parkinson's disease. PLoS One 2014, 9.
40. Song J.X., Lu J.H., Liu L.F., Chen L.L., Durairajan S.S., Yue Z., Zhang H.Q., Li M. HMGB1 is involved in autophagy inhibition caused by SNCA/alpha-synuclein overexpression: a process modulated by the natural autophagy inducer corynoxine B. Autophagy 2014, 10:144-154.
41. Sun Q., Wu W., Hu Y.C., Li H., Zhang D., Li S., Li W., Li W.D., Ma B., Zhu J.H., Zhou M.L., Hang C.H. Early release of high-mobility group box 1 (HMGB1) from neurons in experimental subarachnoid hemorrhage in vivo and in vitro. J. Neuroinflammation 2014, 11:106.
42. Tsung A., Tohme S., Billiar T.R. High Mobility Group Box-1 in Sterile Inflammation 2014, J. Intern. Med.
43. Wahamaa H., Schierbeck H., Hreggvidsdottir H.S., Palmblad K., Aveberger A.C., Andersson U., Harris H.E. High mobility group box protein 1 in complex with lipopolysaccharide or IL-1 promotes an increased inflammatory phenotype in synovial fibroblasts. Arthritis Res. Ther. 2011, 13:R136.
44. Wang H., Bloom O., Zhang M., Vishnubhakat J.M., Ombrellino M., Che J., Frazier A., Yang H., Ivanova S., Borovikova L., Manogue K.R., Faist E., Abraham E., Andersson J., Andersson U., Molina P.E., Abumrad N.N., Sama A., Tracey K.J. HMG-1 as a late mediator of endotoxin lethality in mice. Science 1999, 285:248-251. (New York, N.Y.).
45. Yang H., Ochani M., Li J., Qiang X., Tanovic M., Harris H.E., Susarla S.M., Ulloa L., Wang H., DiRaimo R., Czura C.J., Wang H., Roth J., Warren H.S., Fink M.P., Fenton M.J., Andersson U., Tracey K.J. Reversing established sepsis with antagonists of endogenous high-mobility group box 1. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:296-301.
46. Yang R., Harada T., Mollen K.P., Prince J.M., Levy R.M., Englert J.A., Gallowitsch-Puerta M., Yang L., Yang H., Tracey K.J., Harbrecht B.G., Billiar T.R., Fink M.P. Anti-HMGB1 neutralizing antibody ameliorates gut barrier dysfunction and improves survival after hemorrhagic shock. Mol. Med. 2006, 12:105-114. (Cambridge, Mass.).
47. Yasuda T., Ueda T., Takeyama Y., Shinzeki M., Sawa H., Nakajima T., Ajiki T., Fujino Y., Suzuki Y., Kuroda Y. Significant increase of serum high-mobility group box chromosomal protein 1 levels in patients with severe acute pancreatitis. Pancreas 2006, 33:359-363.
48. Zhang J., Takahashi H.K., Liu K., Wake H., Liu R., Maruo T., Date I., Yoshino T., Ohtsuka A., Mori S., Nishibori M. Anti-high mobility group box-1 monoclonal antibody protects the blood-brain barrier from ischemia-induced disruption in rats. Stroke; A J. cereb. circ. 2011, 42:1420-1428.