Glutamine sustains energy metabolism and alleviates liver injury in burn sepsis by promoting the assembly of mitochondrial HSP60-HSP10 complex via SIRT4 dependent protein deacetylation

References

• Jeschke MG, van Baar ME, Choudhry MA, et al. Burn injury. Nat Rev Dis Primers. 2020;6:11, doi:10.1038/s41572-020-0145-5
   PubMed Web of Science ®Google Scholar
• Zhang P, Zou B, Liou YC, et al. The pathogenesis and diagnosis of sepsis post burn injury. Burns Trauma. 2021;9:a47.
   Web of Science ®Google Scholar
• Singer M, Deutschman CS, Seymour CW, et al. The third international consensus definitions for sepsis and septic shock (Sepsis-3). JAMA-J Am Med Assoc. 2016;315:801–810. doi:10.1001/jama.2016.0287
   PubMed Web of Science ®Google Scholar
• Gong Y, Long X, Xu H, et al. The changes and prognostic value of liver function in young adults with severe burn: a retrospective observational study. Medicine (Baltimore). 2018;97:e13721, doi:10.1097/MD.0000000000013721
   PubMed Web of Science ®Google Scholar
• Song J, de Libero J, Wolf SE. Hepatic autophagy after severe burn in response to endoplasmic reticulum stress. J Surg Res. 2014;187:128–133. doi:10.1016/j.jss.2013.09.042
   PubMed Web of Science ®Google Scholar
• Bohanon FJ, Nunez LO, Herndon DN, et al. Burn trauma acutely increases the respiratory capacity and function of liver mitochondria. Shock. 2018;49:466–473. doi:10.1097/SHK.0000000000000935
   PubMed Web of Science ®Google Scholar
• Mainali R, Zabalawi M, Long D, et al. Dichloroacetate reverses sepsis-induced hepatic metabolic dysfunction. eLife. 2021;10.
   PubMed Web of Science ®Google Scholar
• Moreira E, Burghi G, Manzanares W. Update on metabolism and nutrition therapy in critically ill burn patients. Med Intensiva (Engl Ed). 2018;42:306–316. doi:10.1016/j.medin.2017.07.007
   PubMed Web of Science ®Google Scholar
• Ghaly P, Iliopoulos J, Ahmad M. The role of nutrition in wound healing: an overview. Br J Nurs. 2021;30:S38–S42. doi:10.12968/bjon.2021.30.5.S38
   PubMedGoogle Scholar
• Palmieri B, Vadala M, Laurino C. Nutrition in wound healing: investigation of the molecular mechanisms, a narrative review. J Wound Care. 2019;28:683–693. doi:10.12968/jowc.2019.28.10.683
   PubMed Web of Science ®Google Scholar
• Rodriguez NA, Jeschke MG, Williams FN, et al. Nutrition in burns: Galveston contributions. J Parenter Enter Nutr. 2011;35:704–714. doi:10.1177/0148607111417446
   PubMed Web of Science ®Google Scholar
• Liesa M, Shirihai OS. Mitochondrial dynamics in the regulation of nutrient utilization and energy expenditure. Cell Metab. 2013;17:491–506. doi:10.1016/j.cmet.2013.03.002
   PubMed Web of Science ®Google Scholar
• Fernandez-Vizarra E, Zeviani M. Mitochondrial disorders of the OXPHOS system. FEBS Lett. 2021;595:1062–1106. doi:10.1002/1873-3468.13995
   PubMed Web of Science ®Google Scholar
• Hansen J, Svenstrup K, Ang D, et al. A novel mutation in the HSPD1 gene in a patient with hereditary spastic paraplegia. J Neurol. 2007;254:897–900. doi:10.1007/s00415-006-0470-y
   PubMed Web of Science ®Google Scholar
• Martin J. Molecular chaperones and mitochondrial protein folding. J Bioenerg Biomembr. 1997;29:35–43. doi:10.1023/A:1022407705182
   PubMed Web of Science ®Google Scholar
• Sousa JS, D’Imprima E, Vonck J. Mitochondrial respiratory chain complexes. Subcell Biochem. 2018;87:167–227. doi:10.1007/978-981-10-7757-9_7
   PubMedGoogle Scholar
• Yadav K, Yadav A, Vashistha P, et al. Protein misfolding diseases and therapeutic approaches. Curr Protein Pept Sci. 2019;20:1226–1245. doi:10.2174/1389203720666190610092840
   PubMed Web of Science ®Google Scholar
• Lu Z, Chen Y, Aponte AM, et al. Prolonged fasting identifies heat shock protein 10 as a Sirtuin 3 substrate: elucidating a new mechanism linking mitochondrial protein acetylation to fatty acid oxidation enzyme folding and function. J Biol Chem. 2015;290(4):2466–2476.
   Web of Science ®Google Scholar
• Hu C, Yang J, Qi Z, et al. Heat shock proteins: biological functions, pathological roles, and therapeutic opportunities. MedComm. 2022;3:e161, doi:10.1002/mco2.161
   PubMedGoogle Scholar
• Ostermann J, Horwich AL, Neupert W, et al. Protein folding in mitochondria requires complex formation with HSP60 and ATP hydrolysis. Nature. 1989;341:125–130. doi:10.1038/341125a0
   PubMed Web of Science ®Google Scholar
• Bie AS, Comert C, Korner R, et al. An inventory of interactors of the human HSP60/HSP10 chaperonin in the mitochondrial matrix space. Cell Stress Chaperones. 2020;25:407–416. doi:10.1007/s12192-020-01080-6
   PubMed Web of Science ®Google Scholar
• Davison EJ, Pennington K, Hung CC, et al. Proteomic analysis of increased parkin expression and its interactants provides evidence for a role in modulation of mitochondrial function. Proteomics. 2009;9:4284–4297. doi:10.1002/pmic.200900126
   PubMed Web of Science ®Google Scholar
• Weiss C, Jebara F, Nisemblat S, et al. Dynamic complexes in the chaperonin-mediated protein folding cycle. Front Mol Biosci. 2016;3:80.
   PubMed Web of Science ®Google Scholar
• Magnoni R, Palmfeldt J, Hansen J, et al. The HSP60 folding machinery is crucial for manganese superoxide dismutase folding and function. Free Radic Res. 2014;48:168–179. doi:10.3109/10715762.2013.858147
   PubMed Web of Science ®Google Scholar
• Shin CS, Meng S, Garbis SD, et al. LONP1 and mtHSP70 cooperate to promote mitochondrial protein folding. Nat Commun. 2021;12:265, doi:10.1038/s41467-020-20597-z
   PubMed Web of Science ®Google Scholar
• Venkatesh S, Suzuki CK. HSP60 takes a hit: inhibition of mitochondrial protein folding. Cell Chem Biol. 2017;24:543–545. doi:10.1016/j.chembiol.2017.05.011
   PubMed Web of Science ®Google Scholar
• Comert C, Fernandez-Guerra P, Bross P. A cell model for HSP60 deficiencies: modeling different levels of chaperonopathies leading to oxidative stress and mitochondrial dysfunction. Methods Mol Biol. 2019;1873:225–239. doi:10.1007/978-1-4939-8820-4_14
   PubMedGoogle Scholar
• Lau S, Patnaik N, Sayen MR, et al. Simultaneous overexpression of two stress proteins in rat cardiomyocytes and myogenic cells confers protection against ischemia-induced injury. Circulation. 1997;96:2287–2294. doi:10.1161/01.CIR.96.7.2287
   PubMed Web of Science ®Google Scholar
• Hartmann R, Licks F, Schemitt EG, et al. Effect of glutamine on liver injuries induced by intestinal ischemia-reperfusion in rats. Nutr Hosp. 2017;34:548–554. doi:10.20960/nh.643
   PubMed Web of Science ®Google Scholar
• Schemitt EG, Hartmann RM, Colares JR, et al. Protective action of glutamine in rats with severe acute liver failure. World J Hepatol. 2019;11:273–286. doi:10.4254/wjh.v11.i3.273
   PubMed Web of Science ®Google Scholar
• Sozen S, Kisakurek M, Yildiz F, et al. The effects of glutamine on hepatic ischemia reperfusion injury in rats. Hippokratia. 2011;15:161–166.
   PubMed Web of Science ®Google Scholar
• Wu D, Su S, Zha X, et al. Glutamine promotes O-GlcNAcylation of G6PD and inhibits AGR2 S-glutathionylation to maintain the intestinal mucus barrier in burned septic mice. Redox Biol. 2023;59:102581, doi:10.1016/j.redox.2022.102581
   PubMed Web of Science ®Google Scholar
• Zhu Y, Chen X, Lu Y, et al. Roles of the fibroblast growth factor signal transduction system in tissue injury repair. Burns Trauma. 2022;10:c41, doi:10.1093/burnst/tkac005
   Web of Science ®Google Scholar
• Canto C, Menzies KJ, Auwerx J. Nad+ metabolism and the control of energy homeostasis: a balancing act between mitochondria and the nucleus. Cell Metab. 2015;22:31–53. doi:10.1016/j.cmet.2015.05.023
   PubMed Web of Science ®Google Scholar
• Houtkooper RH, Canto C, Wanders RJ, et al. The secret life of NAD+: an old metabolite controlling new metabolic signaling pathways. Endocr Rev. 2010;31:194–223. doi:10.1210/er.2009-0026
   PubMed Web of Science ®Google Scholar
• Wischmeyer PE. Glutamine in burn injury. Nutr Clin Pract. 2019;34:681–687. doi:10.1002/ncp.10362
   PubMed Web of Science ®Google Scholar
• Yang H, Yang T, Baur JA, et al. Nutrient-sensitive mitochondrial NAD+ levels dictate cell survival. Cell. 2007;130:1095–1107. doi:10.1016/j.cell.2007.07.035
   PubMed Web of Science ®Google Scholar
• Hernandez A, Patil NK, Bohannon JK. A murine model of full-thickness scald burn injury with subsequent wound and systemic bacterial infection. Methods Mol Biol. 2021;2321:111–120. doi:10.1007/978-1-0716-1488-4_10
   PubMedGoogle Scholar
• Patil NK, Bohannon JK, Luan L, et al. Flt3 ligand treatment attenuates T cell dysfunction and improves survival in a murine model of burn wound sepsis. Shock. 2017;47:40–51. doi:10.1097/SHK.0000000000000688
   PubMed Web of Science ®Google Scholar
• Faezi S, Sattari M, Mahdavi M, et al. Passive immunisation against Pseudomonas aeruginosa recombinant flagellin in an experimental model of burn wound sepsis. Burns. 2011;37:865–872. doi:10.1016/j.burns.2010.12.003
   PubMed Web of Science ®Google Scholar
• Fan S, Wu D, Xia L, et al. Establishment and evaluation of a mouse model of burn wound sepsis. Chinese J Comp Med. 2022;32:7–13.1.
   Google Scholar
• Zou Y, Wang A, Huang L, et al. Illuminating NAD+ metabolism in live cells and In vivo using a genetically encoded fluorescent sensor. Dev Cell. 2020;53:240–252.
   PubMed Web of Science ®Google Scholar
• Caruso BC, Marino GA, Lo CF, et al. Curcumin affects HSP60 folding activity and levels in neuroblastoma cells. Int J Mol Sci. 2020;21(2):661.
   Web of Science ®Google Scholar
• Moisoi N, Klupsch K, Fedele V, et al. Mitochondrial dysfunction triggered by loss of HtrA2 results in the activation of a brain-specific transcriptional stress response. Cell Death Differ. 2009;16:449–464. doi:10.1038/cdd.2008.166
   PubMed Web of Science ®Google Scholar
• Lu Z, Bourdi M, Li JH, et al. SIRT3-dependent deacetylation exacerbates acetaminophen hepatotoxicity. EMBO Rep. 2011;12:840–846. doi:10.1038/embor.2011.121
   PubMed Web of Science ®Google Scholar
• Huttlin EL, Ting L, Bruckner RJ, et al. The BioPlex network: a systematic exploration of the human interactome. Cell. 2015;162:425–440. doi:10.1016/j.cell.2015.06.043
   PubMed Web of Science ®Google Scholar
• Huttlin EL, Bruckner RJ, Navarrete-Perea J, et al. Evolutionary assembly of cooperating cell types in an animal chemical defense system. Cell. 2021;184:6138–6156.e28. doi:10.1016/j.cell.2021.11.014
   PubMed Web of Science ®Google Scholar
• Huttlin EL, Bruckner RJ, Paulo JA, et al. Architecture of the human interactome defines protein communities and disease networks. Nature. 2017;545:505–509. doi:10.1038/nature22366
   PubMed Web of Science ®Google Scholar
• Oudemans-van SH, Bosman RJ, Treskes M, et al. Plasma glutamine depletion and patient outcome in acute ICU admissions. Intensive Care Med. 2001;27:84–90. doi:10.1007/s001340000703
   PubMed Web of Science ®Google Scholar
• Wischmeyer PE. Glutamine: role in critical illness and ongoing clinical trials. Curr Opin Gastroenterol. 2008;24:190–197. doi:10.1097/MOG.0b013e3282f4db94
   PubMed Web of Science ®Google Scholar
• Holecek M. Branched-chain amino acids and ammonia metabolism in liver disease: therapeutic implications. Nutrition. 2013;29:1186–1191. doi:10.1016/j.nut.2013.01.022
   PubMed Web of Science ®Google Scholar
• Cruzat VF, Rogero MM, Tirapegui J. Effects of supplementation with free glutamine and the dipeptide alanyl-glutamine on parameters of muscle damage and inflammation in rats submitted to prolonged exercise. Cell Biochem Funct. 2010;28:24–30. doi:10.1002/cbf.1611
   PubMed Web of Science ®Google Scholar
• Wu G. Amino acids: metabolism, functions, and nutrition. Amino Acids. 2009;37:1–17.
   PubMed Web of Science ®Google Scholar
• Prelack K, Dylewski M, Sheridan RL. Practical guidelines for nutritional management of burn injury and recovery. Burns. 2007;33:14–24. doi:10.1016/j.burns.2006.06.014
   PubMed Web of Science ®Google Scholar
• Rousseau AF, Losser MR, Ichai C, et al. ESPEN endorsed recommendations: nutritional therapy in major burns. Clin Nutr. 2013;32:497–502. doi:10.1016/j.clnu.2013.02.012
   PubMed Web of Science ®Google Scholar
• Singer P, Blaser AR, Berger MM, et al. ESPEN guideline on clinical nutrition in the intensive care unit. Clin Nutr. 2019;38:48–79. doi:10.1016/j.clnu.2018.08.037
   PubMed Web of Science ®Google Scholar
• Elke G, Hartl WH, Kreymann KG, et al. Clinical nutrition in critical care medicine - guideline of the German society for nutritional medicine (DGEM). Clin Nutr ESPEN. 2019;33:220–275. doi:10.1016/j.clnesp.2019.05.002
   PubMed Web of Science ®Google Scholar
• Olaniyi KS, Amusa OA, Oniyide AA, et al. Protective role of glutamine against cadmium-induced testicular dysfunction in Wistar rats: involvement of G6PD activity. Life Sci. 2020;242:117250.
   PubMed Web of Science ®Google Scholar
• Shah AM, Wang Z, Ma J. Glutamine metabolism and its role in immunity, a comprehensive review. Animals (Basel). 2020;10; doi:10.3390/ani10020326
   Google Scholar
• Aldarini N, Alhasawi AA, Thomas SC, et al. The role of glutamine synthetase in energy production and glutamine metabolism during oxidative stress. Antonie Van Leeuwenhoek. 2017;110:629–639. doi:10.1007/s10482-017-0829-3
   PubMed Web of Science ®Google Scholar
• Zhao RZ, Jiang S, Zhang L, et al. Mitochondrial electron transport chain, ROS generation and uncoupling (review). Int J Mol Med. 2019;44:3–15.
   PubMed Web of Science ®Google Scholar
• Nolfi-Donegan D, Braganza A, Shiva S. Mitochondrial electron transport chain: Oxidative phosphorylation, oxidant production, and methods of measurement. Redox Biol. 2020;37:101674, doi:10.1016/j.redox.2020.101674
   PubMed Web of Science ®Google Scholar
• Rizwan H, Pal S, Sabnam S, et al. High glucose augments ROS generation regulates mitochondrial dysfunction and apoptosis via stress signalling cascades in keratinocytes. Life Sci. 2020;241:117148, doi:10.1016/j.lfs.2019.117148
   PubMed Web of Science ®Google Scholar
• Yun CW, Kim HJ, Lim JH, et al. Heat shock proteins: agents of cancer development and therapeutic targets in anti-cancer therapy. Cells. 2019;9(1):60.
   Web of Science ®Google Scholar
• Bross P, Fernandez-Guerra P. Disease-associated mutations in the HSPD1 gene encoding the large subunit of the mitochondrial HSP60/HSP10 chaperonin complex. Front Mol Biosci. 2016;3:49.
   PubMed Web of Science ®Google Scholar
• Hoter A, Rizk S, Naim HY. The multiple roles and therapeutic potential of molecular chaperones in prostate cancer. Cancers (Basel). 2019;11(8):1194.
   Web of Science ®Google Scholar
• Suryadevara V, Ramchandran R, Kamp DW, et al. Lipid mediators regulate pulmonary fibrosis: potential mechanisms and signaling pathways. Int J Mol Sci. 2020;21(12):4257.
   PubMed Web of Science ®Google Scholar
• Caruso BC, Alberti G, Vitale AM, et al. Hsp60 post-translational modifications: functional and pathological consequences. Front Mol Biosci. 2020;7:95.
   PubMed Web of Science ®Google Scholar
• Dai C. The heat-shock, or HSF1-mediated proteotoxic stress, response in cancer: from proteomic stability to oncogenesis. Philos Trans R Soc B-Biol Sci. 2018;373(1738):20160525.
   PubMed Web of Science ®Google Scholar
• Marino GA, Campanella C, Barone R, et al. Doxorubicin anti-tumor mechanisms include Hsp60 post-translational modifications leading to the Hsp60/p53 complex dissociation and instauration of replicative senescence. Cancer Lett. 2017;385:75–86. doi:10.1016/j.canlet.2016.10.045
   PubMed Web of Science ®Google Scholar
• Kim SC, Sprung R, Chen Y, et al. Substrate and functional diversity of lysine acetylation revealed by a proteomics survey. Mol Cell. 2006;23:607–618. doi:10.1016/j.molcel.2006.06.026
   PubMed Web of Science ®Google Scholar
• Schwer B, Eckersdorff M, Li Y, et al. Calorie restriction alters mitochondrial protein acetylation. Aging Cell. 2009;8:604–606. doi:10.1111/j.1474-9726.2009.00503.x
   PubMed Web of Science ®Google Scholar
• Li Y, Zhou Y, Wang F, et al. SIRT4 is the last puzzle of mitochondrial sirtuins. Bioorg Med Chem. 2018;26:3861–3865. doi:10.1016/j.bmc.2018.07.031
   PubMed Web of Science ®Google Scholar
• Min Z, Gao J, Yu Y. The roles of mitochondrial SIRT4 in cellular metabolism. Front Endocrinol. 2018;9:783.
   PubMed Web of Science ®Google Scholar
• Gertz M, Steegborn C. Using mitochondrial sirtuins as drug targets: disease implications and available compounds. Cell Mol Life Sci. 2016;73:2871–2896. doi:10.1007/s00018-016-2180-7
   PubMed Web of Science ®Google Scholar
• Nasrin N, Wu X, Fortier E, et al. SIRT4 regulates fatty acid oxidation and mitochondrial gene expression in liver and muscle cells. J Biol Chem. 2010;285:31995–32002. doi:10.1074/jbc.M110.124164
   PubMed Web of Science ®Google Scholar
• Tomaselli D, Steegborn C, Mai A, et al. Sirt4: A multifaceted enzyme at the crossroads of mitochondrial metabolism and cancer. Front Oncol. 2020;10:474.
   PubMed Web of Science ®Google Scholar