High-Mobility Group Box-1 and Its Potential Role in Perioperative Neurocognitive Disorders
Abstract
:1. HMGB1: An Ubiquitous and Multifunctional Protein Involved in Inflammation
1.1. Nomenclature
1.2. Structure
1.3. Post-Translational Modifications
1.4. Extracellular Release
1.5. Functions
1.6. Molecular Signaling for Inflammation
1.7. Anti-Inflammatory Signaling
2. Perioperative Neurocognitive Disorders
2.1. Terminology
2.2. Healthcare Impact of Perioperative Neurocognitive Disorders (PND)
2.3. Inflammatory Pathogenesis of Perioperative Neurocognitive Disorders
2.4. Other Effects of HMGB1 on the Pathogenic Mechanisms Leading to PND
3. Attenuation of HMGB1-Induced Neuroinflammation
3.1. Protein Compounds
- Monoclonal Antibody Directed at HMGB1
- Persistent cognitive impairment after severe sepsis remains a major challenge for survivors [63]. In a murine sepsis model involving cecal ligation and puncture (“CLP”), the elevated serum HMGB1 levels peaked 3 to 4 weeks postinjury and only returned to baseline levels by week 12; associated with these changes, the mice exhibited a significant decline in spatial memory for up to four months [64]. Administration of anti-HMGB1 antibody on days 7, 9 and 11 after the injury led to significantly reduced serum HMGB1 levels, as well as a significant improvement in spatial memory [64];
- HMGB1 release was studied in murine models of electroshock and pentylenetetrazole (PTZ)-induced convulsions. Administration of neutralizing HMGB1 was associated with a decrease in seizures in both models [65]. Anti-HMGB1 antibody administration also led to a decrease in release and translocation into the cytosol HMGB1 from the nuclei of hippocampal neurons and astrocytes. Pilocarpine induced seizures in mice were associated with BBB opening (as measured by Evans Blue leakage); exposure to the anti-HMGB1 antibody inhibited BBB leakage [66]. Pilocarpine-induced seizures are accompanied by activated microglia and astrocytes in the hippocampal CA1 region; anti-HMGB1 antibody administration attenuated glial activation [67];
- Outcome after exposure to anti-HMGB1 antibody was studied in a fluid percussion induced TBI model in mice [66]. The TBI-induced elevated circulating levels of HMGB1 and microglial activation (as evidenced by CD68 positivity) were both attenuated; functionally, TBI-induced impairment in cognition (assessed in the Morris Water Maze) and locomotion (assessed in the rotarod) were improved with anti-HMGB1 antibody [66].
- B.
- Recombinant Box A
- Because HMGB1 binds to its receptors through Box A, strategies have been considered in which recombinant Box A is administered as a decoy preventing natural binding of the ligand to its signaling pathways on the surface of immunocytes. In an in vitro assay involving cultured macrophages, stimulation with HMGB1 to release TNF-α and IL-1β was prevented dose-dependently with recombinant Box A [68];
- In vivo experiments examining outcome in LPS-exposed mice, recombinant Box A improved survival and surviving mice were more alert and active and resumed feeding earlier [68];
- In a CLP model of sepsis, survival was improved even when the administration of recombinant Box A was administered 24 h postinjury [68].
3.2. Non-Protein Compounds
- Glycyrrhizin
- In a spinal cord ischemia–reperfusion injury (IRI) murine model circulating levels of HMGB1, IL-6, IL-1β and TNF-α were significantly lowered by glycyrrhizin [70] than in those of the control group from 2 to 72 h after reperfusion. Functionally, the degree of paraplegia in the hind-limbs was also significantly improved by glycyrrhizin [70];
- Obesity induced by a high-fat, high-fructose diet (HFHFD) in rats for 14 weeks results in systemic and neuroinflammation as well as cognitive decline. Rats that were exposed to glycyrrhizin for the final 6 weeks of the HFHFD had significant reduction in plasma and hippocampal levels of HMGB1, IL-6, IL-1β and TNF-α [71]. Similarly, diet-induced decline in spatial memory (Y maze paradigm) was prevented with glycyrrhizin [72];
- In a TBI model, rats that were treated after injury with glycyrrhizin expressed lower levels of HMGB1 in microglia/macrophages and the activated microglia changed to the M2 reparative phenotype 5 days after TBI [71]. Rotarod testing revealed a decrease in maximal speed needed to stay on the rotarod 1 day after TBI, whereas rats treated with glycyrrhizin had an improved maximal speed [71].
- B.
- Polyunsaturated Fatty Acid (PUFA)
- C.
- Flavonoid (Baicalin)
- Adult mice subjected to LPS-induced sickness behavior have glial activation (both microglia and astrocytes) with high HMGB1 levels in the hippocampal glia [74]. Exposure to baicalin prevented glial activation and elevated hippocampal proinflammatory cytokines; functionally, the LPS-induced cognitive decline (assessed in the Morris Water Maze was significantly improved [74].
4. Identification of Patients Prone to Enhanced Neuroinflammation/PND
4.1. Non-Modifiable Patient-Related Factors That Affect Development of PND
- Age
- B.
- Gender
- C.
- Genetic and Racial Factors
4.2. Pre-Existing Medical Diseases That Affect Development of PND
- Atrial fibrillation (AF)
- B.
- Obesity, diabetes mellitus and the metabolic syndrome
- C.
- Obstructive Sleep Apnea (OSA)
- D.
- Gut Microbiota
- E.
- Neurological diseases
5. Conclusions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Bianchi, M.E.; Agresti, A. HMG proteins: Dynamic players in gene regulation and differentiation. Curr. Opin. Genet. Dev. 2005, 15, 496–506. [Google Scholar] [CrossRef] [PubMed]
- Sessa, L.; Bianchi, M.E. The evolution of High Mobility Group Box (HMGB) chromatin proteins in multicellular animals. Gene 2007, 387, 133–140. [Google Scholar] [CrossRef] [PubMed]
- Müller, S.; Ronfani, L.; Bianchi, M.E. Regulated expression and subcellular localization of HMGB1, a chromatin protein with a cytokine function. J. Intern. Med. 2004, 255, 332–343. [Google Scholar] [CrossRef] [Green Version]
- Bonaldi, T.; Talamo, F.; Scaffidi, P.; Ferrera, D.; Porto, A.; Bachi, A.; Rubartelli, A.; Agresti, A.; Bianchi, M.E. Monocytic cells hyperacetylate chromatin protein HMGB1 to redirect it towards secretion. EMBO J. 2003, 22, 5551–5560. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Stros, M. HMGB proteins: Interaction with DNA and chromatin. Biochem. Biophys. Acta 2010, 1799, 101–113. [Google Scholar] [PubMed]
- Knapp, S.; Müller, S.; Digilio, G.; Bonaldi, T.; Bianchi, M.E.; Musco, G. The long acidic tail of high mobility group box 1 (HMGB1) protein forms an extended and flexible structure that interacts with specific residues within and between the HMG boxes. Biochemistry 2004, 43, 11992–11997. [Google Scholar] [CrossRef]
- Stott, K.; Watson, M.; Howe, F.S.; Grossmann, J.G.; Thomas, J.O. Tail-mediated collapse of HMGB1 is dynamic and occurs via differential binding of the acidic tail to the A and B domains. J. Mol. Biol. 2010, 403, 706–722. [Google Scholar] [CrossRef]
- Yang, H.; Lundbäck, P.; Ottosson, L.; Erlandsson-Harris, H.; Venereau, E.; Bianchi, M.E.; Al-Abed, Y.; Andersson, U.; Tracey, K.J. Redox modifications of cysteine residues regulate the cytokine activity of HMGB1. Mol. Med. 2021, 27, 58. [Google Scholar] [CrossRef]
- Deng, M.; Scott, M.J.; Fan, J.; Billiar, T.R. Location is the key to function: HMGB1 in sepsis and trauma-induced inflammation. J. Leukoc. Biol. 2019, 106, 161–169. [Google Scholar] [CrossRef]
- Youn, J.H.; Shin, J.-S. Nucleocytoplasmic shuttling of HMGB1 is regulated by phosphorylation that redirects it toward secretion. J. Immunol. 2006, 177, 7889–7897. [Google Scholar] [CrossRef] [Green Version]
- Yang, H.; Antoine, D.J.; Andersson, U.; Tracey, K.J. The many faces of HMGB1: Molecular structure-functional activity in inflammation, apoptosis, and chemotaxis. J. Leukoc. Biol. 2013, 93, 865–873. [Google Scholar] [CrossRef] [Green Version]
- Scaffidi, P.; Misteli, T.; Bianchi, M.E. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 2002, 418, 191–195. [Google Scholar] [CrossRef]
- Wang, H.; Bloom, O.; Zhang, M.; Vishnubhakat, J.M.; Ombrellino, M.; Che, J.; Frazier, A.; Yang, H.; Ivanova, S.; Borovikova, L.; et al. HMG-1 as a late mediator of endotoxin lethality in mice. Science 1999, 285, 248–251. [Google Scholar] [CrossRef]
- Andersson, U.; Tracey, K.J. HMGB1 is a therapeutic target for sterile inflammation and infection. Annu. Rev. Immunol. 2011, 29, 139–162. [Google Scholar] [CrossRef] [Green Version]
- Ge, Y.; Huang, M.; Yao, Y.-M. The Effect and Regulatory Mechanism of High Mobility Group Box-1 Protein on Immune Cells in Inflammatory Diseases. Cells 2021, 10, 1044. [Google Scholar] [CrossRef]
- Yang, H.; Wang, H.; Chavan, S.S.; Andersson, U. High Mobility Group Box Protein 1 (HMGB1): The Prototypical Endogenous Danger Molecule. Mol. Med. 2015, 21 (Suppl. 1), S6–S12. [Google Scholar] [CrossRef] [PubMed]
- Tang, D.; Kang, R.; Livesey, K.M.; Zeh 3rd, H.J.; Lotze, M.T. High mobility group box 1 (HMGB1) activates an autophagic response to oxidative stress. Antioxid. Redox Signal. 2011, 15, 2185–2195. [Google Scholar] [CrossRef]
- Huttunen, H.J.; Fages, C.; Kuja-Panula, J.; Ridley, A.J.; Rauvala, H. Receptor for advanced glycation end products-binding COOH-terminal motif of amphoterin inhibits invasive migration and metastasis. Cancer Res. 2002, 62, 4805–4811. [Google Scholar]
- Kierdorf, K.; Fritz, G. RAGE regulation and signaling in inflammation and beyond. J. Leukoc. Biol. 2013, 94, 55–68. [Google Scholar] [CrossRef] [PubMed]
- LeBlanc, P.M.; Doggett, T.A.; Choi, J.; Hancock, M.A.; Durocher, Y.; Frank, F.; Nagar, B.; Ferguson, T.A.; Saleh, M. An immunogenic peptide in the A-box of HMGB1 protein reverses apoptosis-induced tolerance through RAGE receptor. J. Biol. Chem. 2014, 289, 7777–7786. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Deng, M.; Tang, Y.; Li, W.; Wang, X.; Zhang, R.; Zhang, X.; Zhao, X.; Liu, J.; Tang, C.; Liu, Z.; et al. The Endotoxin Delivery Protein HMGB1 Mediates Caspase-11-Dependent Lethality in Sepsis. Immunity 2018, 49, 740–753. [Google Scholar] [CrossRef] [Green Version]
- Venereau, E.; Casalgrandi, M.; Schiraldi, M.; Antoine, D.J.; Cattaneo, A.; De Marchis, F.; Liu, J.; Antonelli, A.; Preti, A.; Raeli, L.; et al. Mutually exclusive redox forms of HMGB1 promote cell recruitment or proinflammatory cytokine release. J. Exp. Med. 2012, 209, 1519–1528. [Google Scholar] [CrossRef] [Green Version]
- Yang, H.; Wang, H.; Levine, Y.A.; Gunasekaran, M.K.; Wang, Y.; Addorisio, M.; Zhu, S.; Li, W.; Li, J.; de Kleijn, D.P.; et al. Identification of CD163 as an antiinflammatory receptor for HMGB1-haptoglobin complexes. JCI Insight 2018, 3, e126617. [Google Scholar] [CrossRef] [Green Version]
- Huber, R.; Meier, B.; Otsuka, A.; Fenini, G.; Satoh, T.; Gehrke, S.; Widmer, D.; Levesque, M.P.; Mangana, J.; Kerl, K.; et al. Tumour hypoxia promotes melanoma growth and metastasis via High Mobility Group Box-1 and M2-like macrophages. Sci. Rep. 2016, 6, 29914. [Google Scholar] [CrossRef] [Green Version]
- Son, M.; Porat, A.; He, M.; Suurmond, J.; Santiago-Schwarz, F.; Andersson, U.; Coleman, T.R.; Volpe, B.T.; Tracey, K.J.; Al-Abed, Y.; et al. C1q and HMGB1 reciprocally regulate human macrophage polarization. Blood 2016, 128, 2218–2228. [Google Scholar] [CrossRef] [Green Version]
- Wild, C.A.; Bergmann, C.; Fritz, G.; Schuler, P.; Hoffmann, T.K.; Lotfi, R.; Westendorf, A.; Brandau, S.; Lang, S. HMGB1 conveys immunosuppressive characteristics on regulatory and conventional T cells. Int. Immunol. 2012, 24, 485–494. [Google Scholar] [CrossRef] [Green Version]
- Bandala-Sanchez, E.; Bediaga, N.G.; Goddard-Borger, E.D.; Ngui, K.; Naselli, G.; Stone, N.L.; Neale, A.M.; Pearce, L.A.; Wardak, A.; Czabotar, P.; et al. CD52 glycan binds the proinflammatory B box of HMGB1 to engage the Siglec-10 receptor and suppress human T cell function. Proc. Natl. Acad. Sci. USA 2018, 115, 7783–7788. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Savage, G.H. Insanity following the use of anaesthetics in operations. BMJ 1887, 3, 1199–1200. [Google Scholar] [CrossRef]
- Bedford, P.D. Adverse cerebral effects of anaesthesia on old people. Lancet 1955, 269, 259–263. [Google Scholar] [CrossRef]
- Moller, J.T.; Cluitmans, P.; Rasmussen, L.S.; Houx, P.; Rasmussen, H.; Canet, J.; Rabbitt, P.; Jolles, J.; Larsen, K.; Hanning, C.D.; et al. Long-term postoperative cognitive dysfunction in the elderly ISPOCD1 study. ISPOCD investigators. International Study of Post-Operative Cognitive Dysfunction. Lancet 1998, 351, 857–861. [Google Scholar] [CrossRef]
- Everd, L.; Silbert, B.; Knopman, D.S.; Scott, D.A.; DeKosky, S.T.; Rasmussen, L.S.; Oh, E.S.; Crosby, G.; Berger, M.; Eckenhoff, R.G. Nomenclature Consensus Working Group. Recommendations for the Nomenclature of Cognitive Change Associated with Anaesthesia and Surgery-2018. Anesthesiology 2018, 129, 872–879. [Google Scholar] [CrossRef] [PubMed]
- Ferri, C.P.; Jacob, K.S. Dementia in low-income and middle-income countries: Different realities mandate tailored solutions. PLoS Med. 2017, 14, e1002271. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yemm, H.; Robinson, D.L.; Paddick, S.M.; Dotchin, C.; Goodson, M.L.; Narytnyk, A.; Poole, M.; Mc Ardle, R. Instrumental Activities of Daily Living Scales to Detect Cognitive Impairment and Dementia in Low- and Middle-Income Countries: A Systematic Review. J. Alzheimers. Dis. 2021. [Google Scholar] [CrossRef]
- Gou, R.Y.; Hsiej, T.T.; Marcantonio, E.R.; Cooper, Z.; Jones, R.N.; Travison, T.G.; Fong, T.G.; Abdeen, A.; Lange, J.; Earp, B.; et al. One-Year Medicare Costs Associated with Delirium in Older Patients Undergoing Major Elective Surgery. JAMA Surg. 2021, 156, 430–442. [Google Scholar] [CrossRef]
- Saczynski, J.S.; Marcantonio, E.R.; Quach, L.; Fong, T.G.; Gross, A.; Inouye, S.K.; Jones, R.N. Cognitive trajectories after postoperative delirium. NEJM 2012, 367, 30–39. [Google Scholar] [CrossRef] [Green Version]
- Davis, N.; Lee, M.; Lin, A.Y.; Lynch, L.; Monteleone, M.; Falzon, L.; Ispahany, N.; Lei, S. Postoperative cognitive function following general versus regional anesthesia: A systematic review. J. Neurosurg. Anesthesiol. 2014, 26, 369–376. [Google Scholar] [CrossRef] [Green Version]
- Wu, J.; Yin, Y.; Jin, M.; Li, B. The risk factors for postoperative delirium in adult patients after hip fracture surgery: A systematic review and meta-analysis. Int. J. Geriatr. Psychiatry 2021, 36, 3–14. [Google Scholar] [CrossRef]
- Evered, L.; Scott, D.A.; Silbert, B.; Maruff, P. Postoperative cognitive dysfunction is independent of type of surgery and anesthetic. Anesth. Analg. 2011, 112, 1179–1185. [Google Scholar] [CrossRef] [PubMed]
- Shaefi, S.; Mittel, A.; Loberman, D.; Ramakrishna, H. Off-Pump Versus On-Pump Coronary Artery Bypass Grafting-A Systematic Review and Analysis of Clinical Outcomes. J. Cardiothorac. Vasc. Anesth. 2019, 33, 232–244. [Google Scholar] [CrossRef]
- Wan, Y.; Xu, J.; Ma, D.; Zeng, Y.; Cibelli, M.; Maze, M. Postoperative impairment of cognitive function in rats: A possible role for cytokine-mediated inflammation in the hippocampus. Anesthesiology 2007, 106, 436–443. [Google Scholar] [CrossRef] [PubMed]
- Vacas, S.; Degos, V.; Tracey, K.J.; Maze, M. High-mobility group box 1 protein initiates postoperative cognitive decline by engaging bone marrow-derived macrophages. Anesthesiology 2014, 120, 1160–1167. [Google Scholar] [CrossRef] [Green Version]
- Matzinger, P. The danger model: A renewed sense of self. Science 2002, 296, 301–305. [Google Scholar] [CrossRef] [Green Version]
- O’ Connor, K.A.; Johnson, J.D.; Hansen, M.K.; Wieseler Frank, J.L.; Maksimova, E.; Watkins, L.R.; Maier, S.F. Peripheral and central proinflammatory cytokine response to a severe acute stressor. Brain Res. 2003, 991, 123–132. [Google Scholar] [CrossRef]
- Hu, J.; Vacas, S.; Feng, X.; Lutrin, D.; Uchida, Y.; Lai, I.K.; Maze, M. Dexmedetomidine Prevents Cognitive Decline by Enhancing Resolution of High Mobility Group Box 1 Protein-induced Inflammation through a Vagomimetic Action in Mice. Anesthesiology 2018, 128, 921–931. [Google Scholar] [CrossRef] [Green Version]
- Cibelli, M.; Fidalgo, A.R.; Terrando, N.; Ma, D.; Monaco, C.; Feldmann, M.; Takata, M.; Lever, I.J.; Nanchahal, J.; Fanselow, M.S.; et al. Role of interleukin-1beta in postoperative cognitive dysfunction. Ann. Neurol. 2010, 68, 360–368. [Google Scholar] [CrossRef] [Green Version]
- Terrando, N.; Monaco, C.; Ma, D.; Foxwell, B.M.J.; Feldmann, M.; Maze, M. Tumor necrosis factor-alpha triggers a cytokine cascade yielding postoperative cognitive decline. Proc. Natl. Acad. Sci. USA 2010, 107, 20518–20522. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Maze, M. Interleukin-6 is both necessary and sufficient to produce perioperative neurocognitive disorder in mice. Br. J. Anaesth. 2018, 120, 537–545. [Google Scholar]
- Terrando, N.; Eriksson, L.I.; Ryu, J.K.; Yang, T.; Monaco, C.; Feldmann, M.; Fagerlund, M.J.; Charo, I.F.; Akassoglou, K.; Maze, M. Resolving postoperative neuroinflammation and cognitive decline. Ann. Neurol. 2011, 70, 986–995. [Google Scholar] [CrossRef]
- Festoff, B.W.; Sajja, R.K.; Van Dreden, P.; Cucullo, L. HMGB1 and thrombin mediate the blood-brain barrier dysfunction acting as biomarkers of neuroinflammation and progression to neurodegeneration in Alzheimer’s disease. J. Neuroinflamm. 2016, 13, 194. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lu, Y.; Xu, Z.; Shen, F.; Lin, R.; Li, H.; Lv, X.; Liu, Z. Propofol Protects Against TNF-α-induced Blood-brain Barrier Disruption via the PIM-1/eNOS/NO Pathway. Curr. Neurovasc. Res. 2020, 17, 471–479. [Google Scholar] [CrossRef] [PubMed]
- Feng, X.; Valdearcos, M.; Uchida, Y.; Lutrin, D.; Maze, M.; Koliwad, S.K. Microglia mediate postoperative hippocampal inflammation and cognitive decline in mice. JCI Insight 2017, 2, e91229. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kelly, A.; Lynch, A.; Nolan, Y.; Queenan, P.; Whittaker, E.; O’Neill, L.A.; Lynch, M.A. The anti-inflammatory cytokine, interleukin (IL)-10, blocks the inhibitory effect of IL-1 beta on long term potentiation. A role for JNK. J. Biol. Chem. 2001, 276, 45564–45572. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yang, T.; Xu, G.; Newton, P.T.; Chagin, A.S.; Mkrtchian, S.; Carlstrom, M.; Zhang, X.-M.; Harris, R.A.; Cooter, M.; Berger, M.; et al. Maresin 1 attenuates neuroinflammation in a mouse model of perioperative neurocognitive disorders. Br. J. Anaesth. 2019, 122, 350–360. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hirsch, J.; Vacas, S.; Terrando, N.; Yuan, M.; Sands, L.P.; Kramer, J.; Bozic, K.; Maze, M.; Leung, J.M. Perioperative cerebrospinal fluid and plasma inflammatory markers after orthopedic surgery. J. Neuroinflamm. 2016, 13, 211. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Danielson, M.; Reinsfelt, B.; Westerlind, A.; Zetterberg, H.; Blennow, K.; Ricksten, S.-E. Effects of methylprednisolone on blood-brain barrier and cerebral inflammation in cardiac surgery-a randomized trial. J. Neuroinflamm. 2018, 15, 283. [Google Scholar] [CrossRef]
- Berger, M.; Oyeyemi, D.; Olurinde, M.O.; Whitson, H.E.; Weinhold, K.J.; Woldorff, M.G.; Lipsitz, L.A.; Moretti, E.; Giattino, G.M.; Roberts, K.C.; et al. The INTUIT Study: Investigating Neuroinflammation Underlying Postoperative Cognitive Dysfunction. J. Am. Geriatr. Soc. 2019, 67, 794–798. [Google Scholar] [CrossRef]
- Forsberg, A.; Cervenka, S.; Fagerlund, M.J.; Rasmussen, L.S.; Zetterberg, H.; Harris, H.E.; Stridh, P.; Christensson, E.; Granstrom, A.; Schening, A.; et al. The immune response of the human brain to abdominal surgery. Ann. Neurol. 2017, 81, 572–582. [Google Scholar] [CrossRef]
- Zhang, J.; Takahashi, H.K.; Liu, K.; Wake, H.; Liu, R.; Maruo, T.; Date, I.; Yoshino, T.; Ohtsuka, A.; Mori, S.; et al. Anti-high mobility group box-1 monoclonal antibody protects the blood-brain barrier from ischemia-induced disruption in rats. Stroke 2011, 42, 1420–1428. [Google Scholar] [CrossRef] [Green Version]
- Okuma, Y.; Liu, K.; Wake, H.; Zhang, J.; Maruo, T.; Date, I.; Yoshino, T.; Ohtsuka, A.; Otani, N.; Tomura, S.; et al. Anti-high mobility group box-1 antibody therapy for traumatic brain injury. Ann. Neurol. 2012, 72, 373–384. [Google Scholar] [CrossRef] [Green Version]
- 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. [Google Scholar] [CrossRef]
- Shi, Y.; Zhang, L.; Teng, J.; Miao, W. HMGB1 mediates microglia activation via the TLR4/NF-κB pathway in coriaria lactone induced epilepsy. Mol. Med. Rep. 2018, 17, 5125–5131. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Terrando, N.; Yang, T.; Wang, X.; Fang, J.; Cao, M.; Andersson, U.; Erlandsson, H.H.; Ouyang, W.; Tong, J. Systemic HMGB1 Neutralization Prevents Postoperative Neurocognitive Dysfunction in Aged Rats. Front. Immunol. 2016, 7, 114. [Google Scholar]
- Rengel, K.F.; Hayhurst, C.J.; Pandharipande, P.P.; Hughes, C.G. Long-term Cognitive and Functional Impairments after Critical Illness. Anesth. Analg. 2019, 128, 772–780. [Google Scholar] [CrossRef] [PubMed]
- Chavan, S.S.; Huerta, P.T.; Robbiati, S.; Valdes-Ferrer, S.I.; Ochani, M.; Dancho, M.; Frankfurt, M.; Volpe, B.T.; Tracey, K.J.; Diamond, B. HMGB1 mediates cognitive impairment in sepsis survivors. Mol. Med. 2012, 18, 930–937. [Google Scholar] [CrossRef] [PubMed]
- Zhao, J.; Wang, Y.; Xu, C.; Liu, K.; Wang, Y.; Chen, L.; Wu, X.; Gao, F.; Guo, Y.; Zhu, J.; et al. Therapeutic potential of an anti-high mobility group box-1 monoclonal antibody in epilepsy. Brain Behav. Immun. 2017, 64, 308–319. [Google Scholar] [CrossRef] [PubMed]
- Okuma, Y.; Wake, H.; Teshigawara, K.; Takahashi, Y.; Hishikawa, T.; Mori, S.; Takahashi, H.K.; Date, I.; Nishibori, M. Anti-High Mobility Group Box 1 Antibody Therapy May Prevent Cognitive Dysfunction After Traumatic Brain Injury. World Neurosurg. 2019, 122, e864–e871. [Google Scholar] [CrossRef]
- Fu, L.; Liu, K.; Wake, H.; Teshigawara, K.; Yoshino, T.; Takahashi, H.; Mori, S.; Nishibori, M. Therapeutic effects of anti-HMGB1 monoclonal antibody on pilocarpine-induced status epilepticus in mice. Sci. Rep. 2017, 7, 1179. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yang, H.; Ochani, M.; Li, J.; Qiang, X.; Tanovic, M.; Harris, H.E.; Susarla, S.M.; Ulloa, L.; Wang, H.; DiRaimo, R.; et al. Reversing established sepsis with antagonists of endogenous high-mobility group box 1. Proc. Natl. Acad. Sci. USA 2004, 101, 296–301. [Google Scholar] [CrossRef] [Green Version]
- Mollica, L.; De Marchis, F.; Spitaleri, A.; Dallacosta, C.; Pennacchini, D.; Zamai, M.; Agresti, A.; Trisciuoglio, L.; Musco, G.; Bianchi, M.E. Glycyrrhizin binds to high-mobility group box 1 protein and inhibits its cytokine activities. Chem. Biol. 2007, 14, 431–441. [Google Scholar] [CrossRef] [Green Version]
- Gong, G.; Yuan, L.; Hu, L.; Wu, W.; Yin, L.; Hou, J.L.; Liu, Y.H.; Zhou, L.S. Glycyrrhizin attenuates rat ischemic spinal cord injury by suppressing inflammatory cytokines and HMGB1. Acta. Pharmacol. Sin. 2012, 33, 11–18. [Google Scholar] [CrossRef]
- Gao, T.; Chen, Z.; Chen, H.; Yuan, H.; Wang, Y.; Peng, X.; Wei, C.; Yang, J.; Xu, C. Inhibition of HMGB1 mediates neuroprotection of traumatic brain injury by modulating the microglia/macrophage polarization. Biochem. Biophys. Res. Commun. 2018, 497, 430–436. [Google Scholar] [CrossRef]
- Yu, M.; Huang, H.; Dong, S.; Sha, H.; Wei, W.; Liu, C. High mobility group box-1 mediates hippocampal inflammation and contributes to cognitive deficits in high-fat high-fructose diet-induced obese rats. Brain Behav. Immun. 2019, 82, 167–177. [Google Scholar] [CrossRef]
- Chen, X.; Wu, S.; Chen, C.; Xie, B.; Fang, Z.; Hu, W.; Chen, J.; Fu, H.; He, H. Omega-3 polyunsaturated fatty acid supplementation attenuates microglial-induced inflammation by inhibiting the HMGB1/TLR4/NF-κB pathway following experimental traumatic brain injury. J. Neuroinflamm. 2017, 14, 143. [Google Scholar] [CrossRef] [PubMed]
- Li, Y.; Lui, T.; Li, Y.; Han, D.; Hong, J.; Yang, N.; He, J.; Peng, R.; Mi, X.; Kuang, C.; et al. Baicalin Ameliorates Cognitive Impairment and Protects Microglia from LPS-Induced Neuroinflammation via the SIRT1/HMGB1 Pathway. Oxid. Med. Cell Longev. 2020, 4751349. [Google Scholar] [CrossRef]
- Geng, Y.; Munirathinam, G.; Palani, S.; Ross, J.E.; Wang, B.; Chen, A.; Zheng, G. HMGB1-Neutralizing IgM Antibody Is a Normal Component of Blood Plasma. J. Immunolog. 2020, 205, 407–413. [Google Scholar] [CrossRef] [PubMed]
- Newman, S.; Stygall, J.; Hirani, S.; Shaefi, S.; Maze, M.; Warltier, D.C. Postoperative Cognitive Dysfunction after Noncardiac Surgery. Anesthesiology 2007, 106, 572–590. [Google Scholar] [CrossRef] [PubMed]
- Chen, L.; Zhu, H.; Su, S.; Harshfield, G.; Sullivan, J.; Webb, C.; Blumenthal, J.A.; Wang, X.; Huang, Y.; Treiber, F.A.; et al. High-Mobility Group Box-1 Is Associated with Obesity, Inflammation, and Subclinical Cardiovascular Risk among Young Adults a Longitudinal Cohort Study. Arterioscler. Thromb. Vasc. Biol. 2020, 40, 2776–2784. [Google Scholar] [CrossRef]
- Chau, K.Y.; Lam, H.Y.P.; Lee, K.L.D. Estrogen Treatment Induces Elevated Expression of HMG1 in MCF-7 Cells. Exp. Cell Res. 1998, 241, 269–272. [Google Scholar] [CrossRef]
- Scovell, W.M. High Mobility Group Protein 1: A Collaborator in Nucleosome Dynamics and Estrogen-Responsive Gene Expression. World J. Biol. 2016, 7, 206–222. [Google Scholar] [CrossRef]
- Zhang, H.J.; Ma, X.H.; Ye, J.B.; Liu, C.Z.; Zhou, Z.Y. Systematic Review and Meta-Analysis of Risk Factor for Postoperative Delirium Following Spinal Surgery. J. Orthop. Surg. Res. 2020, 5, 509–517. [Google Scholar] [CrossRef]
- Crespo-Castrillo, A.; Arevalo, M.-A. Microglial and astrocytic function in physiological and pathological conditions: Estrogenic modulation. Int. J. Mol. Sci. 2020, 21, 3219. [Google Scholar] [CrossRef]
- Schenning, K.J.; Murchison, C.F.; Mattek, N.C.; Kaye, J.A.; Quinn, J.F. Sex and Genetic Differences in Postoperative Cognitive Dysfunction: A Longitudinal Cohort Analysis. Biol. Sex. Dif. 2019, 10, 14. [Google Scholar] [CrossRef] [Green Version]
- Kornblit, B.; Munthe-Fog, L.; Petersen, S.L.; Madsen, H.O.; Vindeløv, L.; Garred, P. The Genetic Variation of the Human HMGB1 Gene. Tissue Antigens 2007, 70, 151–156. [Google Scholar] [CrossRef]
- Arias, F.; Chen, F.; Fong, T.G.; Shiff, H.; Alegria, M.; Marcantonio, E.R.; Gou, Y.; Jones, R.N.; Travison, T.G.; Schmitt, E.M.; et al. Social Disadvantage and Risk of Delirium Following Major Surgery. J. Am. Geriatr. Soc. 2020, 68, 2863–2871. [Google Scholar] [CrossRef]
- Hui, D.S.; Morley, J.E.; Mikolajczak, P.C.; Lee, R. Atrial Fibrillation: A Major Risk Factor for Cognitive Decline. Am. Heart J. 2015, 169, 448–456. [Google Scholar] [CrossRef]
- Banerjee, G.; Chan, E.; Ambler, G.; Wilson, D.; Cipolotti, L.; Shakeshaft, C.; Cohen, H.; Yousry, T.; Habil, M.; Al-Shahi Salman, R.; et al. Cognitive Impairment Before Atrial Fibrillation-Related Ischemic Events: Neuroimaging and Prognostic Associations. J. Am. Heart Assoc. 2020, 9, e014537. [Google Scholar] [CrossRef]
- Hu, X.-R.; Wang, X.H.; Liu, H.F.; Zhou, W.J.; Jiang, H. High Mobility Group Box 1 Protein: Possible Pathogenic Link to Atrial Fibrillation. Chin. Med. J. 2012, 125, 2346–2348. [Google Scholar] [PubMed]
- Qu, C.; Wang, X.-W.; Huang, C.; Qiu, F.; Xiang, X.-Y.; Lu, Z.-Q. High Mobility Group Box 1 Gene Polymorphism Is Associated with the Risk of Postoperative Atrial Fibrillation after Coronary Artery Bypass Surgery. J. Cardiothorac. Surg. 2015, 10, 1–7. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, L.; Liu, Y.; Li, X.; Qiu, C. Insights into the Genetic Basis of HMGB1 in Atrial Fibrillation in a Chinese Han Population. Cardiovasc. Diagn Ther. 2020, 10, 388–395. [Google Scholar] [CrossRef] [PubMed]
- Biscetti, F.; Rando, M.M.; Nardella, E.; Cecchini, A.L.; Pecorini, G.; Landolfi, R.; Flex, A. Molecular Sciences High Mobility Group Box-1 and Diabetes Mellitus Complications: State of the Art and Future Perspectives. Int. J. Mol. Sci. 2019, 20, 6258. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gunasekaran, M.K.; Viranaicken, W.; Girard, A.-C.; Festy, F.; Cesari, M.; Roche, R.; Hoareau, L. Inflammation Triggers High Mobility Group Box 1 (HMGB1) Secretion in Adipose Tissue, a Potential Link to Obesity. Cytokine 2013, 64, 103–111. [Google Scholar] [CrossRef] [PubMed]
- Lumeng, C.N. Innate Immune Activation in Obesity. Mol. Asp. Med. 2013, 34, 12–29. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Feinkohl, I.; Winterer, G.; Pischon, T. Obesity and Post-Operative Cognitive Dysfunction: A Systematic Review and Meta-Analysis. Diabetes Metab. Res. Rev. 2016, 32, 641–650. [Google Scholar] [CrossRef] [Green Version]
- Hudetz, J.A.; Patterson, K.M.; Amole, O.; Riley, A.; Pagel, P.S. Postoperative Cognitive Dysfunction after Noncardiac Surgery: Effects of Metabolic Syndrome. J. Anesth. 2011, 25, 337–344. [Google Scholar] [CrossRef]
- Peppard, P.E.; Young, T.; Barnet, J.H.; Palta, M.; Hagen, E.W.; Hla, K.M. Increased Prevalence of Sleep-Disordered Breathing in Adults. Am. J. Epidemiol. 2013, 177, 1006–1014. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lam, E.W.K.; Chung, F.; Wong, J. Sleep-Disordered Breathing, Postoperative Delirium, and Cognitive Impairment. Anesth. Analg. 2017, 124, 1624–1635. [Google Scholar] [CrossRef] [PubMed]
- Wagner, S.; Sutter, L.; Wagenblast, F.; Walther, A.; Schiff, J.-H. Short Term Cognitive Function after Sevoflurane Anesthesia in Patients Suspect to Obstructive Sleep Apnea Syndrome: An Observational Study. BMC Anesthesiol. 2021, 21, 150. [Google Scholar] [CrossRef]
- Wu, K.-M.; Lin, C.-C.; Chiu, C.-H.; Liaw, S.-F. Effect of Treatment by Nasal Continuous Positive Airway Pressure on Serum High Mobility Group Box-1 Protein in Obstructive Sleep Apnea. Chest 2010, 137, 303–309. [Google Scholar] [CrossRef]
- Liu, X.; Ma, Y.; Ouyang, R.; Zeng, Z.; Zhan, Z.; Lu, H.; Cui, Y.; Dai, Z.; Luo, L.; He, C.; et al. The Relationship between Inflammation and Neurocognitive Dysfunction in Obstructive Sleep Apnea Syndrome. J. Neuroinflamm. 2020, 17, 229. [Google Scholar] [CrossRef]
- Min, H.J.; Park, J.S.; Kim, K.S.; Kang, M.; Seo, J.H.; Yoon, J.H.; Kim, C.H.; Cho, H.J. Serum High-Mobility Group Box 1 Protein Level Correlates with the Lowest SaO2 in Patients with Sleep Apnea: A Preliminary Study. Braz. J. Otorhinolaryngol. 2021. [Google Scholar] [CrossRef]
- Benítez-Burraco, A.; Grabrucker, A.M.; Dinan, T.G.; Kelly, J.R.; Minuto, C.; Cryan, J.F.; Clarke, G. Cross Talk: The Microbiota and Neurodevelopmental Disorders. Front. Neurosci. 2017, 11, 490. [Google Scholar]
- Tang, W.; Meng, Z.; Li, N.; Liu, Y.; Li, L.; Chen, D.; Yang, Y.; Ling, Z.; Santos, A. Roles of Gut Microbiota in the Regulation of Hippocampal Plasticity, Inflammation, and Hippocampus-Dependent Behaviors. Front. Cell Infect. Microbiol. 2021, 10, 611014. [Google Scholar] [CrossRef] [PubMed]
- Xu, X.; Hu, Y.; Yan, E.; Zhan, G.; Liu, C.; Yang, C. Perioperative Neurocognitive Dysfunction: Thinking from the Gut? Aging 2020, 12, 15797–15817. [Google Scholar] [CrossRef] [PubMed]
- Zhan, G.; Hua, D.; Huang, N.; Wang, Y.; Li, S.; Zhou, Z.; Yang, N.; Jiang, R.; Zhu, B.; Yang, L.; et al. Anesthesia and Surgery Induce Cognitive Dysfunction in Elderly Male Mice: The Role of Gut Microbiota. Aging 2019, 11, 1778–1790. [Google Scholar] [CrossRef] [PubMed]
- Meng, F.; Li, N.; Li, D.; Song, B.; Li, L. The Presence of Elevated Circulating Trimethylamine N-Oxide Exaggerates Postoperative Cognitive Dysfunction in Aged Rats. Behav. Brain Res. 2019, 368, 111902. [Google Scholar] [CrossRef] [PubMed]
- Singh, G.B.; Zhang, Y.; Boini, K.M.; Koka, S. High Mobility Group Box 1 Mediates TMAO-Induced Endothelial Dysfunction. Int. J. Mol. Sci. 2019, 20, 3570. [Google Scholar] [CrossRef] [Green Version]
- Kant, I.M.J.; de Bresser, J.; van Montfort, S.J.T.; Slooter, A.J.C.; Hendrikse, J. MRI Markers of Neurodegenerative and Neurovascular Changes in Relation to Postoperative Delirium and Postoperative Cognitive Decline. Am. J. Geriatr. Psychiatry 2017, 25, 1048–1061. [Google Scholar] [CrossRef] [PubMed]
- Nishibori, M.; Wang, D.; Ousaka, D.; Wake, H. High Mobility Group Box-1 and Blood-Brain Barrier Disruption. Cells 2020, 9, 2650. [Google Scholar] [CrossRef]
- Paudel, Y.N.; Angelopoulou, E.; Piperi, C.; Othman, I.; Shaikh, M.F. Implication of HMGB1 Signaling Pathways in Amyotrophic Lateral Sclerosis (ALS): From Molecular Mechanisms to Pre-Clinical Results. Pharmacol. Res. 2020, 156, 104792. [Google Scholar] [CrossRef]
- Paudel, Y.N.; Angelopoulou, E.; Piperi, C.; Othman, I.; Aamir, K.; Farooq Shaikh, M. Impact of HMGB1, RAGE, and TLR4 in Alzheimer’s Disease (AD): From Risk Factors to Therapeutic Targeting. Cells 2020, 9, 383. [Google Scholar] [CrossRef] [Green Version]
- Kang, R.; Chen, R.; Zhang, Q.; Hou, W.; Wu, S.; Cao, L.; Huang, J.; Yu, Y.; Fan, X.G.; Yan, Z.; et al. HMGB1 in Health and Disease. Mol. Asp. Med. 1998, 40, 1–116. [Google Scholar]
- Ojeda, B.; Dueñas, M.; Salazar, A.; Antonio Mico, J.; Miguel Torres, L.; Failde, I. Factors Influencing Cognitive Impairment in Neuropathic and Musculoskeletal Pain and Fibromyalgia. Pain Med. 2018, 19, 499–510. [Google Scholar] [CrossRef] [Green Version]
- Otoshi, K.; Kikuchi, S.; Kato, K.; Sekiguchi, M.; Konno, S. Anti-HMGB1 Neutralization Antibody Improves Pain-Related Behavior Induced by Application of Autologous Nucleus Pulposus onto Nerve Roots in Rats. Spine 2011, 36, E692–E698. [Google Scholar] [CrossRef]
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Saxena, S.; Kruys, V.; De Jongh, R.; Vamecq, J.; Maze, M. High-Mobility Group Box-1 and Its Potential Role in Perioperative Neurocognitive Disorders. Cells 2021, 10, 2582. https://doi.org/10.3390/cells10102582
Saxena S, Kruys V, De Jongh R, Vamecq J, Maze M. High-Mobility Group Box-1 and Its Potential Role in Perioperative Neurocognitive Disorders. Cells. 2021; 10(10):2582. https://doi.org/10.3390/cells10102582
Chicago/Turabian StyleSaxena, Sarah, Véronique Kruys, Raf De Jongh, Joseph Vamecq, and Mervyn Maze. 2021. "High-Mobility Group Box-1 and Its Potential Role in Perioperative Neurocognitive Disorders" Cells 10, no. 10: 2582. https://doi.org/10.3390/cells10102582