The influence of redox modulation on hypoxic endothelial cell metabolic and proteomic profiles through a small thiol-based compound tuning glutathione and thioredoxin systems.
I-152
ROS
antioxidant
endothelial cells
glutathione
hypoxia
redox
thioredoxin
Journal
BioFactors (Oxford, England)
ISSN: 1872-8081
Titre abrégé: Biofactors
Pays: Netherlands
ID NLM: 8807441
Informations de publication
Date de publication:
06 Jul 2023
06 Jul 2023
Historique:
received:
10
03
2023
accepted:
16
06
2023
medline:
6
7
2023
pubmed:
6
7
2023
entrez:
6
7
2023
Statut:
aheadofprint
Résumé
Reduction in oxygen levels is a key feature in the physiology of the bone marrow (BM) niche where hematopoiesis occurs. The BM niche is a highly vascularized tissue and endothelial cells (ECs) support and regulate blood cell formation from hematopoietic stem cells (HSCs). While in vivo studies are limited, ECs when cultured in vitro at low O
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : PRIN
ID : 2017Z5LR5Z
Informations de copyright
© 2023 The Authors. BioFactors published by Wiley Periodicals LLC on behalf of International Union of Biochemistry and Molecular Biology.
Références
Müller N, Warwick T, Noack K, Malacarne PF, Cooper AJL, Weissmann N, et al. Reactive oxygen species differentially modulate the metabolic and transcriptomic response of endothelial cells. Antioxidants. 2022;11(2):434.
Bruschi M, Vanzolini T, Sahu N, Balduini A, Magnani M, Fraternale A. Functionalized 3D scaffolds for engineering the hematopoietic niche. Front Bioeng Biotechnol. 2022;10:968086.
Bruschi M, Agarwal P, Bhutani N. Induced pluripotent stem cells-derived chondrocyte progenitors. iPSC Derived Progenitors. 2022;13:159-76.
Dienemann S, Schmidt V, Fleischhammer T, Mueller JH, Lavrentieva A. Comparative analysis of hypoxic response of human microvascular and umbilical vein endothelial cells in 2D and 3D cell culture systems. J Cell Physiol. 2023;238:1111-20.
Morganti C, Cabezas-Wallscheid N, Ito K. Metabolic regulation of hematopoietic stem cells. HemaSphere. 2022;6(7):e740.
Zhang CC, Sadek HA. Hypoxia and metabolic properties of hematopoietic stem cells. Antioxid Redox Signal. 2014;20(12):1891-901.
Mann Z, Sengar M, Verma YK, Rajalingam R, Raghav PK. Hematopoietic stem cell factors: their functional role in self-renewal and clinical aspects. Front Cell Dev Biol. 2022;10:10.
Jang Y-Y, Sharkis SJ. A low level of reactive oxygen species selects for primitive hematopoietic stem cells that may reside in the low-oxygenic niche. Blood. 2007;110(8):3056-63.
Henry E, Souissi-Sahraoui I, Deynoux M, Lefèvre A, Barroca V, Campalans A, et al. Human hematopoietic stem/progenitor cells display reactive oxygen species-dependent long-term hematopoietic defects after exposure to low doses of ionizing radiations. Haematologica. 2020;105(8):2044-55.
Baldea I, Teacoe I, Olteanu DE, Vaida-Voievod C, Clichici A, Sirbu A, et al. Effects of different hypoxia degrees on endothelial cell cultures-time course study. Mech Ageing Dev. 2018;172:45-50.
Cao H, Yu D, Yan X, Wang B, Yu Z, Song Y, et al. Hypoxia destroys the microstructure of microtubules and causes dysfunction of endothelial cells via the PI3K/Stathmin1 pathway. Cell Biosci. 2019;9(1):20.
Abaci HE, Truitt R, Luong E, Drazer G, Gerecht S. Adaptation to oxygen deprivation in cultures of human pluripotent stem cells, endothelial progenitor cells, and umbilical vein endothelial cells. Am J Physiol Cell Physiol. 2010;298(6):C1527-37.
Li X, Zhang Q, Nasser M, Xu L, Zhang X, Zhu P, et al. Oxygen homeostasis and cardiovascular disease: a role for HIF? Biomed Pharmacother. 2020;128:110338.
Samanta D, Semenza GL. Maintenance of redox homeostasis by hypoxia-inducible factors. Redox Biol. 2017;13:331-5.
Antonelli A, Scarpa ES, Magnani M. Human red blood cells modulate cytokine expression in monocytes/macrophages under anoxic conditions. Front Physiol. 2021;12:632682.
Smith KA, Waypa GB, Schumacker PT. Redox signaling during hypoxia in mammalian cells. Redox Biol. 2017;13:228-34.
Bagulho A, Vilas-Boas F, Pena A, Peneda C, Santos FC, Jerónimo A, et al. The extracellular matrix modulates H2O2 degradation and redox signaling in endothelial cells. Redox Biol. 2015;6:454-60.
Oiry J, Mialocq P, Puy J-Y, Fretier P, Dereuddre-Bosquet N, Dormont D, et al. Synthesis and biological evaluation in human monocyte-derived macrophages of N-(N-acetyl-L-cysteinyl)-S-acetylcysteamine analogues with potent antioxidant and anti-HIV activities. J Med Chem. 2004;47(7):1789-95.
Paul BD, Snyder SH. Therapeutic applications of Cysteamine and Cystamine in neurodegenerative and neuropsychiatric diseases. Front Neurol. 2019;10:1315.
Wilmer MJ, Kluijtmans LAJ, van der Velden TJ, Willems PH, Scheffer PG, Masereeuw R, et al. Cysteamine restores glutathione redox status in cultured cystinotic proximal tubular epithelial cells. Biochim Biophys Acta. 2011;1812(6):643-51.
Atallah C, Charcosset C, Greige-Gerges H. Challenges for cysteamine stabilization, quantification, and biological effects improvement. J Pharm Anal. 2020;10(6):499-516.
Schmitt B, Vicenzi M, Garrel C, Denis FM. Effects of N-acetylcysteine, oral glutathione (GSH) and a novel sublingual form of GSH on oxidative stress markers: a comparative crossover study. Redox Biol. 2015;6:198-205.
Oiry J, Mialocq P, Puy JY, Fretier P, Clayette P, Dormont D, et al. NAC/MEA conjugate: a new potent antioxidant which increases the GSH level in various cell lines. Bioorg Med Chem Lett. 2001;11(9):1189-91.
Brundu S, Palma L, Picceri GG, Ligi D, Orlandi C, Galluzzi L, et al. Glutathione depletion is linked with Th2 polarization in mice with a retrovirus-induced immunodeficiency syndrome, murine AIDS: role of Proglutathione molecules as immunotherapeutics. J Virol. 2016;90(16):7118-30.
Crinelli R, Zara C, Galluzzi L, Buffi G, Ceccarini C, Smietana M, et al. Activation of NRF2 and ATF4 signaling by the pro-glutathione molecule I-152, a co-drug of N-acetyl-cysteine and cysteamine. Antioxidants. 2021;10(2):175.
Rushworth GF, Megson IL. Existing and potential therapeutic uses for N-acetylcysteine: the need for conversion to intracellular glutathione for antioxidant benefits. Pharmacol Ther. 2014;141(2):150-9.
Xiao W, Loscalzo J. Metabolic responses to reductive stress. Antioxid Redox Signal. 2020;32(18):1330-47.
Mansfield KD, Simon MC, Keith B. Hypoxic reduction in cellular glutathione levels requires mitochondrial reactive oxygen species. J Appl Physiol. 2004;97(4):1358-66.
Jaganjac M, Milkovic L, Sunjic SB, Zarkovic N. The NRF2, Thioredoxin, and glutathione system in tumorigenesis and anticancer therapies. Antioxidants. 2020;9(11):1151.
Tonelli C, Chio IIC, Tuveson DA. Transcriptional regulation by Nrf2. Antioxid Redox Signal. 2018;29(17):1727-45.
Chen X, Cao X, Xiao W, Li B, Xue Q. PRDX5 as a novel binding partner in Nrf2-mediated NSCLC progression under oxidative stress. Aging. 2020;12(1):122-37.
Bolduc J, Koruza K, Luo T, Malo Pueyo J, Vo TN, Ezeriņa D, et al. Peroxiredoxins wear many hats: factors that fashion their peroxide sensing personalities. Redox Biol. 2021;42:101959.
Bartoccini F, Retini M, Crinelli R, Menotta M, Fraternale A, Piersanti G. Dithiol based on l-cysteine and cysteamine as a disulfide-reducing agent. J Org Chem. 2022;87(15):10073-9.
Fraternale A, De Angelis M, De Santis R, et al. Targeting SARS-CoV-2 by synthetic dual-acting thiol compounds that inhibit spike/ACE2 interaction and viral protein production. FASEB J. 2023;37(2):e22741.
Fraternale A, Zara C, Pierigè F, Rossi L, Ligi D, Amagliani G, et al. Redox homeostasis as a target for new antimycobacterial agents. Int J Antimicrob Agents. 2020;56(4):106148.
Petrova B, Warren A, Vital NY, Culhane AJ, Maynard AG, Wong A, et al. Redox metabolism measurement in mammalian cells and tissues by LC-MS. Metabolites. 2021;11(5):313.
Motterlini R, Foresti R, Bassi R, Calabrese V, Clark JE, Green CJ. Endothelial heme oxygenase-1 induction by hypoxia. Modulation by inducible nitric-oxide synthase and S-nitrosothiols. J Biol Chem. 2000;275(18):13613-20.
Cohen EB, Geck RC, Toker A. Metabolic pathway alterations in microvascular endothelial cells in response to hypoxia. PLoS One. 2020;15(7):e0232072.
Fraternale A, Zara C, Di Mambro T, et al. I-152, a supplier of N-acetyl-cysteine and cysteamine, inhibits immunoglobulin secretion and plasma cell maturation in LP-BM5 murine leukemia retrovirus-infected mice by affecting the unfolded protein response. Biochim Biophys Acta Mol Basis Dis. 2020;1866(12):165922.
Wong BW, Marsch E, Treps L, Baes M, Carmeliet P. Endothelial cell metabolism in health and disease: impact of hypoxia. EMBO J. 2017;36(15):2187-203.
Xiao W, Wang R-S, Handy DE, Loscalzo J. NAD(H) and NADP(H) redox couples and cellular energy metabolism. Antioxid Redox Signal. 2018;28(3):251-72.
Sorgdrager FJH, Naudé PJW, Kema IP, Nollen EA, Deyn PPD. Tryptophan metabolism in Inflammaging: from biomarker to therapeutic target. Front Immunol. 2019;10:10.
Engl E, Garvert MM. A prophylactic role for creatine in hypoxia? J Neurosci. 2015;35(25):9249-51.
Clarke H, Hickner RC, Ormsbee MJ. The potential role of creatine in vascular health. Nutrients. 2021;13(3):857.
Arazi H, Eghbali E, Suzuki K. Creatine supplementation, physical exercise and oxidative stress markers: a review of the mechanisms and effectiveness. Nutrients. 2021;13(3):869.
Wu X, Zhang L, Miao Y, Yang J, Wang X, Wang CC, et al. Homocysteine causes vascular endothelial dysfunction by disrupting endoplasmic reticulum redox homeostasis. Redox Biol. 2019;20:46-59.
Antonelli A, Scarpa ES, Bruzzone S, Astigiano C, Piacente F, Bruschi M, et al. Anoxia rapidly induces changes in expression of a large and diverse set of genes in endothelial cells. Int J Mol Sci. 2023;24(6):5157.
Bartoszewski R, Moszyńska A, Serocki M, Cabaj A, Polten A, Ochocka R, et al. Primary endothelial cell-specific regulation of hypoxia-inducible factor (HIF)-1 and HIF-2 and their target gene expression profiles during hypoxia. FASEB J. 2019;33(7):7929-41.
Hashimoto T, Shibasaki F. Hypoxia-inducible factor as an angiogenic master switch. Front Pediatr. 2015;3:3.
Hansen JM, Zhang H, Jones DP. Differential oxidation of thioredoxin-1, thioredoxin-2, and glutathione by metal ions*. Free Radic Biol Med. 2006;40(1):138-45.
Hasan AA, Kalinina E, Tatarskiy V, Shtil A. The thioredoxin system of mammalian cells and its modulators. Biomedicine. 2022;10(7):1757.
Kandarakov O, Belyavsky A, Semenova E. Bone marrow niches of hematopoietic stem and progenitor cells. Int J Mol Sci. 2022;23(8):4462.
King KY, Goodell MA. Inflammatory modulation of hematopoietic stem cells: viewing the hematopoietic stem cell as a foundation for the immune response. Nat Rev Immunol. 2011;11(10):685-92.
Kikuchi A, Pradhan-Sundd T, Singh S, Nagarajan S, Loizos N, Monga SP. Platelet-derived growth factor receptor α contributes to human hepatic stellate cell proliferation and migration. Am J Pathol. 2017;187(10):2273-87.
Babicki S, Arndt D, Marcu A, Liang Y, Grant JR, Maciejewski A, et al. Heatmapper: web-enabled heat mapping for all. Nucleic Acids Res. 2016;44(W1):W147-53.
Szklarczyk D, Gable AL, Nastou KC, Lyon D, Kirsch R, Pyysalo S, et al. The STRING database in 2021: customizable protein-protein networks, and functional characterization of user-uploaded gene/measurement sets. Nucleic Acids Res. 2021;49(D1):D605-12.
Jensen LJ, Kuhn M, Stark M, Chaffron S, Creevey C, Muller J, et al. STRING 8-a global view on proteins and their functional interactions in 630 organisms. Nucleic Acids Res. 2009;37(Database issue):D412-6.
Aoyama K, Nakaki T. Inhibition of GTRAP3-18 may increase neuroprotective glutathione (GSH) synthesis. Int J Mol Sci. 2012;13(9):12017-35.
Lu SC. Regulation of hepatic glutathione synthesis: current concepts and controversies. FASEB J. 1999;13(10):1169-83.
Ji Y, Bennett BM. Activation of microsomal glutathione S-transferase by peroxynitrite. Mol Pharmacol. 2003;63(1):136-46.
Munro D, Banh S, Sotiri E, Tamanna N, Treberg JR. The thioredoxin and glutathione-dependent H2O2 consumption pathways in muscle mitochondria: involvement in H2O2 metabolism and consequence to H2O2 efflux assays. Free Radic Biol Med. 2016;96:334-46.
Congrains A, Bianco J, Rosa RG, Mancuso RI, Saad STO. 3D scaffolds to model the hematopoietic stem cell niche: applications and perspectives. Materials. 2021;14(3):569.
Nombela-Arrieta C, Silberstein LE. The science behind the hypoxic niche of hematopoietic stem and progenitors. Hematology. 2014;2014(1):542-7.
Bruschi M, Sahu N, Singla M, Grandi F, Agarwal P, Chu C, et al. A quick and efficient method for the generation of immunomodulatory mesenchymal stromal cell from human induced pluripotent stem cell. Tissue Eng Part A. 2021;28:433-46.
Wilkinson AC, Nakauchi H. Stabilizing hematopoietic stem cells in vitro. Curr Opin Genet Dev. 2020;64:1-5.
Wang X, Cooper S, Broxmeyer HE, Kapur R. Nuclear translocation of TFE3 under hypoxia enhances the engraftment of human hematopoietic stem cells. Leukemia. 2022;36(8):2144-8.
Bozhilov YK, Hsu I, Brown EJ, Wilkinson AC. In vitro human Haematopoietic stem cell expansion and differentiation. Cell. 2023;12(6):896.
Hadland B, Varnum-Finney B, Dozono S, Dignum T, Nourigat-McKay C, Heck AM, et al. Engineering a niche supporting hematopoietic stem cell development using integrated single-cell transcriptomics. Nat Commun. 2022;13(1):1584.
Warpsinski G, Smith MJ, Srivastava S, Keeley TP, Siow RCM, Fraser PA, et al. Nrf2-regulated redox signaling in brain endothelial cells adapted to physiological oxygen levels: consequences for sulforaphane mediated protection against hypoxia-reoxygenation. Redox Biol. 2020;37:101708.
Yang C, Zhang X, Ge X, He C, Liu S, Yang S, et al. N-Acetylcysteine protects against cobalt chloride-induced endothelial dysfunction by enhancing glucose-6-phosphate dehydrogenase activity. FEBS Open Bio. 2022;12(8):1475-88.
Krause BJ, Casanello P, Dias AC, Arias P, Velarde V, Arenas GA, et al. Chronic intermittent hypoxia-induced vascular dysfunction in rats is reverted by N-Acetylcysteine supplementation and arginase inhibition. Front Physiol. 2018;9:901.
Khomenko T, Deng X, Sandor Z, Tarnawski AS, Szabo S. Cysteamine alters redox state, HIF-1α transcriptional interactions and reduces duodenal mucosal oxygenation: novel insight into the mechanisms of duodenal ulceration. Biochem Biophys Res Commun. 2004;317(1):121-7.
Shin YJ, Seo JM, Chung TY, Hyon JY, Wee WR. Effect of cysteamine on oxidative stress-induced cell death of human corneal endothelial cells. Curr Eye Res. 2011;36(10):910-7.
Samuni Y, Goldstein S, Dean OM, Berk M. The chemistry and biological activities of N-acetylcysteine. Biochim Biophys Acta. 2013;1830(8):4117-29.
Martín-Sabroso C, Alonso-González M, Fernández-Carballido A, Aparicio-Blanco J, Córdoba-Díaz D, Navarro-García F, et al. Limitations and challenges in the stability of cysteamine eye drop compounded formulations. Pharmaceuticals. 2021;15(1):2.
Ezeriņa D, Takano Y, Hanaoka K, Urano Y, Dick TP. N-acetyl cysteine functions as a fast-acting antioxidant by triggering intracellular H2S and sulfane sulfur production. Cell Chem Biol. 2018;25(4):447-459.e4.
Dai X, Wang K, Fan J, Liu H, Fan X, Lin Q, et al. Nrf2 transcriptional upregulation of IDH2 to tune mitochondrial dynamics and rescue angiogenic function of diabetic EPCs. Redox Biol. 2022;56:102449.
Cano M, Datta S, Wang L, Liu T, Flores-Bellver M, Sachdeva M, et al. Nrf2 deficiency decreases NADPH from impaired IDH shuttle and pentose phosphate pathway in retinal pigmented epithelial cells to magnify oxidative stress-induced mitochondrial dysfunction. Aging Cell. 2021;20(8):e13444.
Le Gal K, Schmidt EE, Sayin VI. Cellular redox homeostasis. Antioxidants. 2021;10(9):1377.
Tanaka LY, Oliveira PVS, Laurindo FRM. Peri/epicellular thiol oxidoreductases as mediators of extracellular redox signaling. Antioxid Redox Signal. 2020;33(4):280-307.
Kocabas F, Xie L, Xie J, Yu Z, DeBerardinis RJ, Kimura W, et al. Hypoxic metabolism in human hematopoietic stem cells. Cell Biosci. 2015;5(1):39.
Tajima M, Kurashima Y, Sugiyama K, Ogura T, Sakagami H. The redox state of glutathione regulates the hypoxic induction of HIF-1. Eur J Pharmacol. 2009;606(1):45-9.
Gerber H-P, Ferrara N. The role of VEGF in normal and neoplastic hematopoiesis. J Mol Med (Berl). 2003;81(1):20-31.
Cohen T, Nahari D, Cerem LW, Neufeld G, Levi B-Z. Interleukin 6 induces the expression of vascular endothelial growth factor (*). J Biol Chem. 1996;271(2):736-41.
Fu X, Zhai S, Yuan J. Interleukin-6 (IL-6) triggers the malignancy of hemangioma cells via activation of HIF-1α/VEGFA signals. Eur J Pharmacol. 2018;841:82-9.
Pearlstein DP, Ali MH, Mungai PT, Hynes KL, Gewertz BL, Schumacker PT. Role of mitochondrial oxidant generation in endothelial cell responses to hypoxia. Arterioscler Thromb Vasc Biol. 2002;22(4):566-73.
Ali MH, Schlidt SA, Chandel NS, Hynes KL, Schumacker PT, Gewertz BL. Endothelial permeability and IL-6 production during hypoxia: role of ROS in signal transduction. Am J Physiol. 1999;277(5):L1057-65.
Tarbell J, Mahmoud M, Corti A, Cardoso L, Caro C. The role of oxygen transport in atherosclerosis and vascular disease. J R Soc Interface. 2020;17(165):20190732.