Abstract
We present new data on the effects of HBOT on human kidney (HK-2) cell metabolism using a SeaHorse XF Analyzer to evaluate separately the state of mitochondrial and glycolytic energy metabolism. The data are discussed in the context of the concept of cellular caloristasis networks. The information on the changes in cellular energy metabolism stimulated by HBOT presented here provides new insights into the cellular energy state and mitochondrial environment in which sHSPs function. These data will be useful in forming testable hypotheses about the functions of translocated sHSPs in human mitochondria responding to stressors.
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Bilban M, Haschemi A, Wegiel B, Chin BY, Wagner O, Otterbein LE (2008) Heme oxygenase and carbon monoxide initiate homeostatic signaling. J Mol Med (Berl) 86:267–279. https://doi.org/10.1007/s00109-007-0276-0
Bonorino C, Sistonen L, Eriksson J, Mezger V, Santoro G, Hightower LE (2018) The VIII international congress on stress proteins in biology and medicine: täynnä henkeä. Cell Stress Chaperones 23:171–177. https://doi.org/10.1007/s12192-018-0878-1
Cantó C (2017) The heat shock factor HSF1 juggles protein quality control and metabolic regulation. J Cell Biol 216:551–553. https://doi.org/10.1083/jcb.201701093
Choudhury R (2018) Hypoxia and hyperbaric oxygen therapy: a review. Int J Gen Med 11:431–442. https://doi.org/10.2147/IJGM.S172460
Dai S, Tang Z, Cao J, Zhou W, Li H, Sampson S, Dai C (2015) Suppression of the HSF1-mediated proteotoxic stress response by the metabolic stress sensor AMPK. EMBO J 34:275–293. https://doi.org/10.15252/embj.201489062
Edwards ML (2010) Hyperbaric oxygen therapy. Part 1: history and principles. J Vet Emerg Crit Care 20:284–297. https://doi.org/10.1111/j.1476-4431.2010.00535.x
Foretz M, Guigas B, Bertrand L, Pollak M, Viollet B (2014) Metformin: from mechanisms of action to therapies. Cell Metab 20:953–966. https://doi.org/10.1016/j.cmet.2014.09.018
Giudice A, Arra C, Turco MC (2010) Review of molecular mechanisms involved in the activation of the Nrf2-ARE signaling pathway by chemopreventive agents. Methods Mol Biol 647:37–74. https://doi.org/10.1007/978-1-60761-738-9_3
Godman CA, Chheda KP, Hightower LE, Perdrizet G, Shin D-G, Giardina C (2010a) Hyperbaric oxygen induces a cytoprotective and angiogenic response in human microvascular endothelial cells. Cell Stress Chaperones 15:431–442. https://doi.org/10.1007/s12192-009-0159-0
Godman CA, Joshi R, Giardina C, Perdrizet G, Hightower LE (2010c) Hyperbaric oxygen treatment induces antioxidant gene expression. Ann N Y Acad Sci 1197:178–183. https://doi.org/10.1111/j.1749-6632.2009.05393.x
Gómez-Díaz C, Villalba JM, Pérez-Vicente R, Crane FL, Navas P (1997) Ascorbate stabilization is stimulated in ρ°HL-60 cells by CoQ10increase at the plasma membrane. Biochem Biophys Res Commun 234:79–81. https://doi.org/10.1006/bbrc.1997.6582
Harrison LE, Giardina C, Hightower LE, Anderson C, Perdrizet GA (2018) Might hyperbaric oxygen therapy (HBOT) reduce renal injury in diabetic people with diabetes mellitus? From preclinical models to human metabolomics. Cell Stress Chaperones 23:1143–1152. https://doi.org/10.1007/s12192-018-0944-8
Herst PM, Berridge MV (2007) Cell surface oxygen consumption: a major contributor to cellular oxygen consumption in glycolytic cancer cell lines. Biochim Biophys Acta 1767:170–177. https://doi.org/10.1016/j.bbabio.2006.11.018
Hightower LE (1991) Heat shock, stress proteins, chaperones, and proteotoxicity. Cell 66:191–197. https://doi.org/10.1016/0092-8674(91)90611-2
Lane DJR, Lawen A (2009) Transplasma membrane electron transport comes in two flavors. Biofactors 34:191–200
Lunt SY, Vander Heiden MG (2011) Aerobic glycolysis: meeting the metabolic requirements of cell proliferation. Annu Rev Cell Dev Biol 27:441–464. https://doi.org/10.1146/annurev-cellbio-092910-154237
Matteucci E, Giampietro O (2000) Transmembrane electron transfer in diabetic nephropathy. Diabetes Care 23:994–999. https://doi.org/10.2337/diacare.23.7.994
Navas P, Villalba JM, de Cabo R (2007) The importance of plasma membrane coenzyme Q in aging and stress responses. Mitochondrion 7:S34–S40. https://doi.org/10.1016/j.mito.2007.02.010
Prata C, Grasso C, Loizzo S, Sega FV, Caliceti C, Zambonin L, Fiorentini D, Hakim G, Berridge MV, Landi L (2010) Inhibition of trans-plasma membrane electron transport: a potential anti-leukemic strategy. Leuk Res 34:1630–1635. https://doi.org/10.1016/j.leukres.2010.02.032
Qiao A, Jin X, Pang J, Moskophidis D, Mivechi NF (2017) The transcriptional regulator of the chaperone response HSF1 controls hepatic bioenergetics and protein homeostasis. J Cell Biol 216:723–741. https://doi.org/10.1083/jcb.201607091
Ritossa F (1962) A new puffing pattern induced by temperature shock and DNP in Drosophila. Experientia 18:571–573
Ritossa FM (1964) Experimental activation of specific loci in polytene chromosomes of Drosophila. Exp Cell Res 35:601–607
Ritossa F (1996) Discovery of the heat shock response. Cell Stress Chaperones 1:97–98
Samali A, Robertson JD, Peterson E, Manero F, van Zeijl L, Paul C, Cotgreave IA, Arrigo AP, Orrenius S (2001) Hsp27 protects mitochondria of thermotolerant cells against apoptotic stimuli. Cell Stress Chaperones 6:49–58
Santagata S, Mendillo ML, Tang YC, Subramanian A, Perley CC, Roche SP, Wong B, Narayan R, Kwon H, Koeva M, Amon A, Golub TR, Porco JA Jr, Whitesell L, Lindquist S (2013) Tight coordination of protein translation and HSF1 activation supports the anabolic malignant state. Science 341:1238303. https://doi.org/10.1126/science.1238303
Shi D-y, Xie F-Z, Zhai C, Stern JS, Liu Y, S-l L (2009) The role of cellular oxidative stress in regulating glycolysis energy metabolism in hepatoma cells. Mol Cancer 8:32–32. https://doi.org/10.1186/1476-4598-8-32
Stuart JA et al. (2018) How supraphysiological oxygen levels in standard cell culture affect oxygen-consuming reactions. Oxid Med Cell Longev Article ID 8238459:1–13 doi:https://doi.org/10.1155/2018/8238459
Swan CL, Sistonen L (2015) Cellular stress response cross talk maintains protein and energy homeostasis. EMBO J 34:267–269. https://doi.org/10.15252/embj.201490757
Thom SR (2009) Oxidative stress is fundamental to hyperbaric oxygen therapy. J Appl Physiol 106:988–995. https://doi.org/10.1152/japplphysiol.91004.2008
Verma R, Chopra A, Giardina C, Sabbisetti V, Smyth JA, Hightower LE, Perdrizet GA (2015) Hyperbaric oxygen therapy (HBOT) suppresses biomarkers of cell stress and kidney injury in diabetic mice. Cell Stress Chaperones 20:495–505. https://doi.org/10.1007/s12192-015-0574-3
Villalba JM, Navarro F, Córdoba F, Serrano A, Arroyo A, Crane FL, Navas P (1995) Coenzyme Q reductase from liver plasma membrane: purification and role in trans-plasma-membrane electron transport. Proc Natl Acad Sci U S A 92:4887–4891
Voegtlin C, Johnson JM, Dyer HA (1924) Quantitative estimation of the reducing power of normal and cancer tissue. J Pharmacol Exp Ther 24:305–334
Wittig R, Coy JF (2008) The role of glucose metabolism and glucose-associated signalling in cancer. Perspect Med Chem 1:64–82
Xiao W, Wang R-S, Handy DE, Loscalzo J (2018) NAD(H) and NADP(H) redox couples and cellular energy metabolism. Antioxid Redox Signal 28:251–272. https://doi.org/10.1089/ars.2017.7216
Zeng L, Tan J, Lu W, Lu T, Hu Z (2013) The potential role of small heat shock proteins in mitochondria. Cell Signal 25:2312–2319. https://doi.org/10.1016/j.cellsig.2013.07.027
Zhang G, Darshi M, Sharma K (2018) The Warburg effect in diabetic kidney disease. Semin Nephrol 38:111–120. https://doi.org/10.1016/j.semnephrol.2018.01.002
Acknowledgments
We wish to acknowledge the Life Support Technologies Group, Tarrytown, NY, and its founder and CEO Glenn J. Butler for generously providing the Small Round Experimental Hyperbaric Chamber, designed for cell cultures, used in these experiments. We thank Jared Fernandez, Agilent Technologies, Seahorse Bioscience, Santa Clara, CA, for helping us to evaluate cellular mitochondrial and glycolytic profiles. We also send our thanks to Carol Norris and Chris O’Connell, University of Connecticut, Flow Cytometry and Confocal Microscopy Facility, for their expert imaging help.
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Tezgin, D., Giardina, C., Perdrizet, G.A. et al. The effect of hyperbaric oxygen on mitochondrial and glycolytic energy metabolism: the caloristasis concept. Cell Stress and Chaperones 25, 667–677 (2020). https://doi.org/10.1007/s12192-020-01100-5
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DOI: https://doi.org/10.1007/s12192-020-01100-5