Disulfide-containing high mobility group box-1 promotes N-methyl-d-aspartate receptor function and excitotoxicity by activating toll-like receptor 4-dependent signaling in hippocampal neurons

Antioxidants and Redox Signaling

Volumn 21, Issue 12, 2014, Pages 1726-1740

  Balosso, Silvia ^a   Liu, Jaron ^b   Bianchi, Marco E ^b   Vezzani, Annamaria ^a  

^a MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

^b SAN RAFFAELE HOSPITAL   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADVANCED GLYCATION END PRODUCT RECEPTOR; CALCIUM ION; DISULFIDE; HIGH MOBILITY GROUP B1 PROTEIN; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 1BETA; KAINIC ACID; LIPOPOLYSACCHARIDE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; TOLL LIKE RECEPTOR 4; HMGB1 PROTEIN, MOUSE; TLR4 PROTEIN, MOUSE;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; CELL DEATH; CHANNEL GATING; COMPETITIVE INHIBITION; EXCITOTOXICITY; FIBROBLAST; HIPPOCAMPAL NEURONAL CULTURE; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MALE; MOLECULAR INTERACTION; MOUSE; NERVE CELL; NONHUMAN; OXIDATION REDUCTION STATE; PHASE CONTRAST MICROSCOPY; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PYRAMIDAL NERVE CELL; RHODOBACTER SPHAEROIDES; SEIZURE; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; CHEMISTRY; CYTOLOGY; KNOCKOUT MOUSE; METABOLISM; OXIDATION REDUCTION REACTION;

ANIMALS; DISULFIDES; HIPPOCAMPUS; HMGB1 PROTEIN; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURONS; OXIDATION-REDUCTION; RECEPTORS, N-METHYL-D-ASPARTATE; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4;

EID: 84903549187     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2013.5349     Document Type: Article

References (74)

1. Ali DW and Salter MW. Nmda receptor regulation by src kinase signalling in excitatory synaptic transmission and plasticity. Curr Opin Neurobiol 11: 336-342, 2001.
2. Andersson U and Rauvala H. Introduction: Hmgb1 in inflammation and innate immunity. J Intern Med 270: 296-300, 2011.
3. Andrassy M, Volz HC, Igwe JC, Funke B, Eichberger SN, Kaya Z, Buss S, Autschbach F, Pleger ST, Lukic IK, Bea F, Hardt SE, Humpert PM, Bianchi ME, Mairbaurl H, Nawroth PP, Remppis A, Katus HA, and Bierhaus A. High-mobility group box-1 in ischemia-reperfusion injury of the heart. Circulation 117: 3216-3226, 2008.
4. Balosso S, Maroso M, Sanchez-Alavez M, Ravizza T, Frasca A, Bartfai T, and Vezzani A. A novel non-transcriptional pathway mediates the proconvulsive effects of interleukin-1beta. Brain 131: 3256-3265, 2008.
5. Bianchi ME. Damps, pamps and alarmins: all we need to know about danger. J Leukoc Biol 81: 1-5, 2007.
6. Bianchi ME and Manfredi AA. High-mobility group box 1 (hmgb1) protein at the crossroads between innate and adaptive immunity. Immunol Rev 220: 35-46, 2007.
7. Caso JR, Pradillo JM, Hurtado O, Leza JC, Moro MA, and Lizasoain I. Toll-like receptor 4 is involved in subacute stress-induced neuroinflammation and in the worsening of experimental stroke. Stroke 39: 1314-1320, 2008.
8. Chavan SS, Huerta PT, Robbiati S, Valdes-Ferrer SI, Ochani M, Dancho M, Frankfurt M, Volpe BT, Tracey KJ, and Diamond B. Hmgb1 mediates cognitive impairment in sepsis survivors. Mol Med 18: 930-937, 2012.
9. Chiarugi A. Characterization of the molecular events following impairment of nf-kappab-driven transcription in neurons. Brain Res Mol Brain Res 109: 179-188, 2002.
10. Coats SR, Pham TT, Bainbridge BW, Reife RA, and Darveau RP. Md-2 mediates the ability of tetra-acylated and pentaacylated lipopolysaccharides to antagonize Escherichia coli lipopolysaccharide at the tlr4 signaling complex. J Immunol 175: 4490-4498, 2005.
11. Crews FT, Qin L, Sheedy D, Vetreno RP, and Zou J. High mobility group box 1/toll-like receptor danger signaling increases brain neuroimmune activation in alcohol dependence. Biol Psychiatry 73: 602-612, 2012.
12. Diogenes A, Ferraz CC, Akopian AN, Henry MA, and Hargreaves KM. Lps sensitizes trpv1 via activation of tlr4 in trigeminal sensory neurons. J Dent Res 90: 759-764, 2011.
13. Fang P, Schachner M, and Shen YQ. Hmgb1 in development and diseases of the central nervous system. Mol Neurobiol 45: 499-506, 2012.
14. Faraco G, Fossati S, Bianchi ME, Patrone M, Pedrazzi M, Sparatore B, Moroni F, and Chiarugi A. High mobility group box 1 protein is released by neural cells upon different stresses and worsens ischemic neurodegeneration in vitro and in vivo. J Neurochem 103: 590-603, 2007.
15. Forder JP and Tymianski M. Postsynaptic mechanisms of excitotoxicity: involvement of postsynaptic density proteins, radicals, and oxidant molecules. Neuroscience 158: 293-300, 2009.
16. Frasca A, Aalbers M, Frigerio F, Fiordaliso F, Salio M, Gobbi M, Cagnotto A, Gardoni F, Battaglia GS, Hoogland G, Di Luca M, and Vezzani A. Misplaced nmda receptors in epileptogenesis contribute to excitotoxicity. Neurobiol Dis 43: 507-515, 2011.
17. Gao HM, Zhou H, Zhang F, Wilson BC, Kam W, and Hong JS. Hmgb1 acts on microglia mac1 to mediate chronic neuroinflammation that drives progressive neurodegeneration. J Neurosci 31: 1081-1092, 2011.
18. Gao TL, Yuan XT, Yang D, Dai HL, Wang WJ, Peng X, Shao HJ, Jin ZF, and Fu ZJ. Expression of hmgb1 and rage in rat and human brains after traumatic brain injury. J Trauma Acute Care Surg 72: 643-649, 2012.
19. Hanke JH, Gardner JP, Dow RL, Changelian PS, Brissette WH, Weringer EJ, Pollok BA, and Connelly PA. Discovery of a novel, potent, and src family-selective tyrosine kinase inhibitor. Study of lck- and fynt-dependent t cell activation. J Biol Chem 271: 695-701, 1996.
20. Hanke ML and Kielian T. Toll-like receptors in health and disease in the brain: mechanisms and therapeutic potential. Clin Sci (Lond) 121: 367-387, 2011.
21. Hayakawa K, Mishima K, Irie K, Hazekawa M, Mishima S, Fujioka M, Orito K, Egashira N, Katsurabayashi S, Takasaki K, Iwasaki K, and Fujiwara M. Cannabidiol prevents a postischemic injury progressively induced by cerebral ischemia via a high-mobility group box1-inhibiting mechanism. Neuropharmacology 55: 1280-1286, 2008.
22. Hoppe G, Talcott KE, Bhattacharya SK, Crabb JW, and Sears JE. Molecular basis for the redox control of nuclear transport of the structural chromatin protein hmgb1. Exp Cell Res 312: 3526-3538, 2006.
23. Hou XY, Liu Y, and Zhang GY. Pp2, a potent inhibitor of src family kinases, protects against hippocampal ca1 pyramidal cell death after transient global brain ischemia. Neurosci Lett 420: 235-239, 2007.
24. Hreggvidsdottir HS, Ostberg T, Wahamaa H, Schierbeck H, Aveberger AC, Klevenvall L, Palmblad K, Ottosson L, Andersson U, and Harris HE. The alarmin hmgb1 acts in synergy with endogenous and exogenous danger signals to promote inflammation. J Leukoc Biol 86: 655-662, 2009.
25. Huang Y, Smith DE, Ibanez-Sandoval O, Sims JE, and Friedman WJ. Neuron-specific effects of interleukin-1beta are mediated by a novel isoform of the il-1 receptor accessory protein. J Neurosci 31: 18048-18059, 2011.
26. Iori V, Maroso M, Rizzi M, Iyer AM, Vertemara R, Carli M, Agresti A, Antonelli A, Bianchi ME, Aronica E, Ravizza T, and Vezzani A. Receptor for advanced glycation endproducts is upregulated in temporal lobe epilepsy and contributes to experimental seizures. Neurobiol Dis 58: 102-114, 2013.
27. Kalia LV, Kalia SK, and Salter MW. Nmda receptors in clinical neurology: excitatory times ahead. Lancet Neurol 7: 742-755, 2008.
28. Kim ID, Lim CM, Kim JB, Nam HY, Nam K, Kim SW, Park JS, and Lee JK. Neuroprotection by biodegradable pamam ester (e-pam-r)-mediated hmgb1 sirna delivery in primary cortical cultures and in the postischemic brain. J Control Release 142: 422-430, 2010.
29. Kim J, Wan CK, S JOC, Shaikh SB, and Nicholson LF. The role of receptor for advanced glycation end products (rage) in neuronal differentiation. J Neurosci Res 90: 1136-1147, 2012.
30. Kim JB, Sig Choi J, Yu YM, Nam K, Piao CS, Kim SW, Lee MH, Han PL, Park JS, and Lee JK. Hmgb1, a novel cytokinelike mediator linking acute neuronal death and delayed neuroinflammation in the postischemic brain. J Neurosci 26: 6413-6421, 2006.
31. Kim SW, Lim CM, Kim JB, Shin JH, Lee S, Lee M, and Lee JK. Extracellular hmgb1 released by nmda treatment confers neuronal apoptosis via rage-p38 mapk/erk signaling pathway. Neurotox Res 20: 159-169, 2011.
32. Koh JY and Choi DW. Quantitative determination of glutamate mediated cortical neuronal injury in cell culture by lactate dehydrogenase efflux assay. J Neurosci Methods 20: 83-90, 1987.
33. Kolesnick R and Golde DW. The sphingomyelin pathway in tumor necrosis factor and interleukin-1 signaling. Cell 77: 325-328, 1994.
34. Koss DJ, Riedel G, and Platt B. Intracellular ca2 + stores modulate soccs and nmda receptors via tyrosine kinases in rat hippocampal neurons. Cell Calcium 46: 39-48, 2009.
35. Liliensiek B, Weigand MA, Bierhaus A, Nicklas W, Kasper M, Hofer S, Plachky J, Grone HJ, Kurschus FC, Schmidt AM, Yan SD, Martin E, Schleicher E, Stern DM, Hammerling GG, Nawroth PP, and Arnold B. Receptor for advanced glycation end products (rage) regulates sepsis but not the adaptive immune response. J Clin Invest 113: 1641-1650, 2004.
36. Lobner D. Comparison of the ldh and mtt assays for quantifying cell death: validity for neuronal apoptosis? J Neurosci Methods 96: 147-152, 2000.
37. Maroso M, Balosso S, Ravizza T, Liu J, Aronica E, Iyer AM, Rossetti C, Molteni M, Casalgrandi M, Manfredi AA, Bianchi ME, and Vezzani A. Toll-like receptor 4 and high-mobility group box-1 are involved in ictogenesis and can be targeted to reduce seizures. Nat Med 16: 413-419, 2010.
38. Martin D, Bustos GA, Bowe MA, Bray SD, and Nadler JV. Autoreceptor regulation of glutamate and aspartate release from slices of the hippocampal ca1 area. J Neurochem 56: 1647-1655, 1991.
39. Mazarati A, Maroso M, Iori V, Vezzani A, and Carli M. High-mobility group box-1 impairs memory in mice through both toll-like receptor 4 and receptor for advanced glycation end products. Exp Neurol 232: 143-148, 2011.
40. O'Neill LA and Bowie AG. The family of five: Tir-domaincontaining adaptors in toll-like receptor signalling. Nat Rev Immunol 7: 353-364, 2007.
41. 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 HK, Mori S, and Nishibori M. Antihigh mobility group box-1 antibody therapy for traumatic brain injury. Ann Neurol 72: 373-384, 2012.
42. Pedrazzi M, Averna M, Sparatore B, Patrone M, Salamino F, Marcoli M, Maura G, Cervetto C, Frattaroli D, Pontremoli S, and Melloni E. Potentiation of nmda receptor-dependent cell responses by extracellular high mobility group box 1 protein. PLoS One 7: e44518, 2012.
43. Pedrazzi M, Patrone M, Passalacqua M, Ranzato E, Colamassaro D, Sparatore B, Pontremoli S, and Melloni E. Selective proinflammatory activation of astrocytes by highmobility group box 1 protein signaling. J Immunol 179: 8525-8532, 2007.
44. Qiu J, Nishimura M, Wang Y, Sims JR, Qiu S, Savitz SI, Salomone S, and Moskowitz MA. Early release of hmgb-1 from neurons after the onset of brain ischemia. J Cereb Blood Flow Metab 28: 927-938, 2008.
45. Rauvala H and Rouhiainen A. Physiological and pathophysiological outcomes of the interactions of hmgb1 with cell surface receptors. Biochim Biophys Acta 1799: 164-170, 2010.
46. Rong LL, Trojaborg W, Qu W, Kostov K, Yan SD, Gooch C, Szabolcs M, Hays AP, and Schmidt AM. Antagonism of rage suppresses peripheral nerve regeneration. FASEB J 18: 1812-1817, 2004.
47. Rubartelli A and Lotze MT. Inside, outside, upside down: damage-associated molecular-pattern molecules (damps) and redox. Trends Immunol 28: 429-436, 2007.
48. Sahu D, Debnath P, Takayama Y, and Iwahara J. Redox properties of the a-domain of the hmgb1 protein. FEBS Lett 582: 3973-3978, 2008.
49. Salter MW and Kalia LV. Src kinases: a hub for nmda receptor regulation. Nat Rev Neurosci 5: 317-328, 2004.
50. Sanchez-Alavez M, Tabarean IV, Behrens MM, and Bartfai T. Ceramide mediates the rapid phase of febrile response to il-1beta. Proc Natl Acad Sci U S A 103: 2904-2908, 2006.
51. Senatore A, Colleoni S, Verderio C, Restelli E, Morini R, Condliffe SB, Bertani I, Mantovani S, Canovi M, Micotti E, Forloni G, Dolphin AC, Matteoli M, Gobbi M, and Chiesa R. Mutant prp suppresses glutamatergic neurotransmission in cerebellar granule neurons by impairing membrane delivery of vgcc alpha(2)delta-1 subunit. Neuron 74: 300-313, 2012.
52. Sha Y, Zmijewski J, Xu Z, and Abraham E. Hmgb1 develops enhanced proinflammatory activity by binding to cytokines. J Immunol 180: 2531-2537, 2008.
53. Su X, Wang H, Zhao J, Pan H, and Mao L. Beneficial effects of ethyl pyruvate through inhibiting high-mobility group box 1 expression and tlr4/nf-kappab pathway after traumatic brain injury in the rat. Mediators Inflamm 2011: 807142, 2011.
54. Suarez LM, Suarez F, Del Olmo N, Ruiz M, Gonzalez-Escalada JR, and Solis JM. Presynaptic nmda autoreceptors facilitate axon excitability: a new molecular target for the anticonvulsant gabapentin. Eur J Neurosci 21: 197-209, 2005.
55. Tang D, Billiar TR, and Lotze MT. A janus tale of two active high mobility group box 1 (hmgb1) redox states. Mol Med 18: 1360-1362, 2012.
56. Tang D, Kang R, Zeh HJ, 3rd, and Lotze MT. High-mobility group box 1, oxidative stress, and disease. Antioxid Redox Signal 14: 1315-1335, 2011.
57. Tsakiri N, Kimber I, Rothwell NJ, and Pinteaux E. Interleukin-1-induced interleukin-6 synthesis is mediated by the neutral sphingomyelinase/src kinase pathway in neurones. Br J Pharmacol 153: 775-783, 2008.
58. Um JW, Nygaard HB, Heiss JK, Kostylev MA, Stagi M, Vortmeyer A, Wisniewski T, Gunther EC, and Strittmatter SM. Alzheimer amyloid-beta oligomer bound to postsynaptic prion protein activates fyn to impair neurons. Nat Neurosci 15: 1227-1235, 2012.
59. Van Dongen AM. Biology of the Nmda Receptor. Boca Raton, FL: CRC Press, 2009, p. 342.
60. Vedder LC, Smith CC, Flannigan AE, and McMahon LL. Estradiol-induced increase in novel object recognition requires hippocampal nr2b-containing nmda receptors. Hippocampus 23: 108-115, 2013.
61. Venereau E, Casalgrandi M, Schiraldi M, Antoine DJ, Cattaneo A, De Marchis F, Liu J, Antonelli A, Preti A, Raeli L, Shams SS, Yang H, Varani L, Andersson U, Tracey KJ, Bachi A, Uguccioni M, and Bianchi ME. Mutually exclusive redox forms of hmgb1 promote cell recruitment or proinflammatory cytokine release. J Exp Med 209: 1519-1528, 2012.
62. Venereau E, Schiraldi M, Uguccioni M, and Bianchi ME. Hmgb1 and leukocyte migration during trauma and sterile inflammation. Mol Immunol 55: 76-82, 2013.
63. Verderio C, Pozzi D, Pravettoni E, Inverardi F, Schenk U, Coco S, Proux-Gillardeaux V, Galli T, Rossetto O, Frassoni C, and Matteoli M. Snap-25 modulation of calcium dynamics underlies differences in gabaergic and glutamatergic responsiveness to depolarization. Neuron 41: 599-610, 2004.
64. Viviani B, Bartesaghi S, Gardoni F, Vezzani A, Behrens MM, Bartfai T, Binaglia M, Corsini E, Di Luca M, Galli CL, and Marinovich M. Interleukin-1beta enhances nmda receptormediated intracellular calcium increase through activation of the src family of kinases. J Neurosci 23: 8692-8700, 2003.
65. Waldbaum S and Patel M. Mitochondria, oxidative stress, and temporal lobe epilepsy. Epilepsy Res 88: 23-45, 2010.
66. Wang Q, Wang F, Li X, Yang Q, Xu N, Huang Y, Zhang Q, Gou X, Chen S, and Xiong L. Electroacupuncture pretreatment attenuates cerebral ischemic injury through alpha7 nicotinic acetylcholine receptor-mediated inhibition of high-mobility group box 1 release in rats. J Neuroinflammation 9: 24, 2012.
67. Wong EH, Kemp JA, Priestley T, Knight AR, Woodruff GN, and Iversen LL. The anticonvulsant mk-801 is a potent nmethyl-d-aspartate antagonist. Proc Natl Acad Sci U S A 83: 7104-7108, 1986.
68. Yang H, Hreggvidsdottir HS, Palmblad K, Wang H, Ochani M, Li J, Lu B, Chavan S, Rosas-Ballina M, Al-Abed Y, Akira S, Bierhaus A, Erlandsson-Harris H, Andersson U, and Tracey KJ. A critical cysteine is required for hmgb1 binding to toll-like receptor 4 and activation of macrophage cytokine release. Proc Natl Acad Sci U S A 107: 11942-11947, 2010.
69. Yang H, Lundback P, Ottosson L, Erlandsson-Harris H, Venereau E, Bianchi ME, Al-Abed Y, Andersson U, Tracey KJ, and Antoine DJ. Redox modification of cysteine residues regulates the cytokine activity of high mobility group box-1 (hmgb1). Mol Med 18: 250-259, 2012.
70. Yang H, Ochani M, Li J, Qiang X, Tanovic M, Harris HE, Susarla SM, Ulloa L, Wang H, DiRaimo R, Czura CJ, Roth J, Warren HS, Fink MP, Fenton MJ, Andersson U, and Tracey KJ. Reversing established sepsis with antagonists of endogenous high-mobility group box 1. Proc Natl Acad Sci U S A 101: 296-301, 2004.
71. Yang H, Wang H, and Czura CJ, Tracey KJ. Hmgb1 as a cytokine and therapeutic target. J Endotoxin Res 8: 469-472, 2002.
72. Yang QW, Xiang J, Zhou Y, Zhong Q, and Li JC. Targeting hmgb1/tlr4 signaling as a novel approach to treatment of cerebral ischemia. Front Biosci (Schol Ed) 2: 1081-1091, 2010.
73. Yu XM, Askalan R, Keil GJ, 2nd, and Salter MW. Nmda channel regulation by channel-associated protein tyrosine kinase src. Science 275: 674-678, 1997.
74. Zeng C, Lee JT, Chen H, Chen S, Hsu CY, and Xu J. Amyloid-beta peptide enhances tumor necrosis factor-alphainduced inos through neutral sphingomyelinase/ceramide pathway in oligodendrocytes. J Neurochem 94: 703-712, 2005.