Enhancement of glycolysis-dependent DNA repair regulated by FOXO1 knockdown via PFKFB3 attenuates hyperglycemia-induced endothelial oxidative stress injury

Harding, 2019, Global trends in diabetes complications: a review of current evidence, Diabetologia, 62, 3, 10.1007/s00125-018-4711-2 Saeedi, 2019, Global and regional diabetes prevalence estimates for 2019 and projections for 2030 and 2045: results from the international diabetes federation diabetes atlas, vol. 157 Hammes, 2018, Diabetic retinopathy: hyperglycaemia, oxidative stress and beyond, Diabetologia, 61, 29, 10.1007/s00125-017-4435-8 Brownlee, 2005, The pathobiology of diabetic complications: a unifying mechanism, Diabetes, 54, 1615, 10.2337/diabetes.54.6.1615 Du, 2003, Inhibition of GAPDH activity by poly(ADP-ribose) polymerase activates three major pathways of hyperglycemic damage in endothelial cells, J. Clin. Invest., 112, 1049, 10.1172/JCI18127 Lorenzi, 1986, High glucose induces DNA damage in cultured human endothelial cells, J. Clin. Invest., 77, 322, 10.1172/JCI112295 Quagliaro, 2003, Intermittent high glucose enhances apoptosis related to oxidative stress in human umbilical vein endothelial cells: the role of protein kinase C and NAD(P)H-oxidase activation, Diabetes, 52, 2795, 10.2337/diabetes.52.11.2795 He, 2014, Ginkgo biloba attenuates oxidative DNA damage of human umbilical vein endothelial cells induced by intermittent high glucose, Pharmazie, 69, 203 Zeng, 2017, [The role of DNA double-strain damage repairing mechanisms in diabetic atheroscolersis], J. Sichuan Univ. Med. Sci., 48, 191 Kumar, 2020, Compromised DNA repair is responsible for diabetes-associated fibrosis, EMBO J., 39, 10.15252/embj.2019103477 Pang, 2012, Altered expression of base excision repair genes in response to high glucose-induced oxidative stress in HepG2 hepatocytes, Med. Sci. Mon. Int. Med. J. Exp. Clin. Res. : Int. Med. J. Exper. Clin. Res., 18, Br281 Mizukami, 2014, Involvement of oxidative stress-induced DNA damage, endoplasmic reticulum stress, and autophagy deficits in the decline of beta-cell mass in Japanese type 2 diabetic patients, Diabetes Care, 37, 1966, 10.2337/dc13-2018 Tornovsky-Babeay, 2014, Type 2 diabetes and congenital hyperinsulinism cause DNA double-strand breaks and p53 activity in beta cells, Cell Metabol., 19, 109, 10.1016/j.cmet.2013.11.007 Bhatt, 2015, Preserved DNA damage checkpoint pathway protects against complications in long-standing type 1 diabetes, Cell Metabol., 22, 239, 10.1016/j.cmet.2015.07.015 Li, 2022, FBXW7 alleviates hyperglycemia-induced endothelial oxidative stress injury via ROS and PARP inhibition, Redox Biol., 58, 10.1016/j.redox.2022.102530 Kitamura, 2013, The role of FOXO1 in beta-cell failure and type 2 diabetes mellitus, Nat. Rev. Endocrinol., 9, 615, 10.1038/nrendo.2013.157 Ponugoti, 2012, Role of forkhead transcription factors in diabetes-induced oxidative stress, Exp. Diabetes Res., 2012, 10.1155/2012/939751 Jian, 2020, METTL14 aggravates endothelial inflammation and atherosclerosis by increasing FOXO1 N6-methyladeosine modifications, Theranostics, 10, 8939, 10.7150/thno.45178 Battiprolu, 2012, Metabolic stress-induced activation of FoxO1 triggers diabetic cardiomyopathy in mice, J. Clin. Invest., 122, 1109, 10.1172/JCI60329 Gopal, 2021, FoxO1 inhibition alleviates type 2 diabetes-related diastolic dysfunction by increasing myocardial pyruvate dehydrogenase activity, Cell Rep., 35, 10.1016/j.celrep.2021.108935 Zhang, 2012, Hepatic suppression of Foxo1 and Foxo3 causes hypoglycemia and hyperlipidemia in mice, Endocrinology, 153, 631, 10.1210/en.2011-1527 Zhang, 2006, FoxO1 regulates multiple metabolic pathways in the liver: effects on gluconeogenic, glycolytic, and lipogenic gene expression, J. Biol. Chem., 281, 10105, 10.1074/jbc.M600272200 Xiong, 2013, Deletion of hepatic FoxO1/3/4 genes in mice significantly impacts on glucose metabolism through downregulation of gluconeogenesis and upregulation of glycolysis, PLoS One, 8, 10.1371/journal.pone.0074340 Wilhelm, 2016, FOXO1 couples metabolic activity and growth state in the vascular endothelium, Nature, 529, 216, 10.1038/nature16498 Behl, 2009, FOXO1 plays an important role in enhanced microvascular cell apoptosis and microvascular cell loss in type 1 and type 2 diabetic rats, Diabetes, 58, 917, 10.2337/db08-0537 Jang, 2013, Metabolism: sweet enticements to move, Nature, 500, 409, 10.1038/nature12549 Bankoglu, 2021, Cell survival after DNA damage in the comet assay, Arch. Toxicol., 95, 3803, 10.1007/s00204-021-03164-3 Di Micco, 2021, Cellular senescence in ageing: from mechanisms to therapeutic opportunities, Nat. Rev. Mol. Cell Biol., 22, 75, 10.1038/s41580-020-00314-w Blackford, 2017, ATM, ATR, and DNA-PK: the trinity at the heart of the DNA damage response, Molecular cell, 66, 801, 10.1016/j.molcel.2017.05.015 Scully, 2019, DNA double-strand break repair-pathway choice in somatic mammalian cells, Nat. Rev. Mol. Cell Biol., 20, 698, 10.1038/s41580-019-0152-0 De Bock, 2013, Role of PFKFB3-driven glycolysis in vessel sprouting, Cell, 154, 651, 10.1016/j.cell.2013.06.037 Sabbatinelli, 2019, Where metabolism meets senescence: focus on endothelial cells, Front. Physiol., 10, 1523, 10.3389/fphys.2019.01523 Rajman, 2018, Therapeutic potential of NAD-boosting molecules: the in vivo evidence, Cell Metabol., 27, 529, 10.1016/j.cmet.2018.02.011 Tang, 2014, Mitochondria, endothelial cell function, and vascular diseases, Front. Physiol., 5, 175, 10.3389/fphys.2014.00175 Passos, 2010, Feedback between p21 and reactive oxygen production is necessary for cell senescence, Mol. Syst. Biol., 6, 347, 10.1038/msb.2010.5 Oliveira, 2021, Effects of the novel PFKFB3 inhibitor KAN0438757 on colorectal cancer cells and its systemic toxicity evaluation in vivo, Cancers, 13, 10.3390/cancers13051011 Kanwar, 2009, Role of glyceraldehyde 3-phosphate dehydrogenase in the development and progression of diabetic retinopathy, Diabetes, 58, 227, 10.2337/db08-1025 Clark, 2002, The microvasculature in insulin resistance and type 2 diabetes, Semin. Vasc. Med., 2, 21, 10.1055/s-2002-23506 Patton, 2002, The effects of high ambient glucose on the radiosensitivity of retinal microvascular endothelial cells and pericytes, Curr. Eye Res., 24, 51, 10.1076/ceyr.24.1.51.5433 Viebahn, 1991, Synergism between diabetic and radiation retinopathy: case report and review, Br. J. Ophthalmol., 75, 629, 10.1136/bjo.75.10.629 Bhatt, 2015, Transient elevation of glycolysis confers radio-resistance by facilitating DNA repair in cells, BMC Cancer, 15, 335, 10.1186/s12885-015-1368-9 Efimova, 2016, Linking cancer metabolism to DNA repair and accelerated senescence, Mol. Cancer Res., 14, 173, 10.1158/1541-7786.MCR-15-0263 Giovannucci, 2010, Diabetes and cancer: a consensus report, Diabetes Care, 33, 1674, 10.2337/dc10-0666 Lee, 2015, Evidence for DNA damage as a biological link between diabetes and cancer, Chin. Med. J., 128, 1543, 10.4103/0366-6999.157693 Yang, 2005, Activated IGF-1R inhibits hyperglycemia-induced DNA damage and promotes DNA repair by homologous recombination, Am. J. Physiol. Ren. Physiol., 289, F1144, 10.1152/ajprenal.00094.2005 Wang, 2013, Redox homeostasis: the linchpin in stem cell self-renewal and differentiation, Cell Death Dis., 4, e537, 10.1038/cddis.2013.50 Klotz, 2015, Redox regulation of FoxO transcription factors, Redox Biol., 6, 51, 10.1016/j.redox.2015.06.019 Tajes Orduna, 2009, An evaluation of the neuroprotective effects of melatonin in an in vitro experimental model of age-induced neuronal apoptosis, J. Pineal Res., 46, 262, 10.1111/j.1600-079X.2008.00656.x Huang, 2006, CDK2-dependent phosphorylation of FOXO1 as an apoptotic response to DNA damage, Science (New York, NY), 314, 294, 10.1126/science.1130512 Huang, 2007, CDK2 and FOXO1: a fork in the road for cell fate decisions, Cell Cycle, 6, 902, 10.4161/cc.6.8.4122 Halder, 2012, vol. 279, 2876 Zhu, 2022, Forkhead Box 1(FoxO1) mediates psychological stress-induced neuroinflammation, Neurol. Res., 1 Rodier, 2009, Persistent DNA damage signalling triggers senescence-associated inflammatory cytokine secretion, Nat. Cell Biol., 11, 973, 10.1038/ncb1909 Van Hove, 2020, Single-cell transcriptome analysis of the Akimba mouse retina reveals cell-type-specific insights into the pathobiology of diabetic retinopathy, Diabetologia, 63, 2235, 10.1007/s00125-020-05218-0 Ola, 2006, Analysis of glucose metabolism in diabetic rat retinas, Am. J. Physiol. Endocrinol. Metabol., 290, E1057, 10.1152/ajpendo.00323.2005 Shosha, 2022, Investigation of retinal metabolic function in type 1 diabetic akita mice, Front Cardiovasc Med, 9, 10.3389/fcvm.2022.900640 Rudnicki, 2018, Endothelial-specific FoxO1 depletion prevents obesity-related disorders by increasing vascular metabolism and growth, Elife, 7, 10.7554/eLife.39780 Cargill, 2021, Targeting MYC-enhanced glycolysis for the treatment of small cell lung cancer, Cancer Metabol., 9, 33, 10.1186/s40170-021-00270-9 Li, 2018, Acetylation accumulates PFKFB3 in cytoplasm to promote glycolysis and protects cells from cisplatin-induced apoptosis, Nat. Commun., 9, 508, 10.1038/s41467-018-02950-5 Gustafsson, 2018, Targeting PFKFB3 radiosensitizes cancer cells and suppresses homologous recombination, Nat. Commun., 9, 3872, 10.1038/s41467-018-06287-x Galindo, 2022, Nuances of PFKFB3 signaling in breast cancer, Clin. Breast Cancer, 22, e604, 10.1016/j.clbc.2022.01.002 Kuosmanen, 2018, MicroRNAs mediate the senescence-associated decline of NRF2 in endothelial cells, Redox Biol., 18, 77, 10.1016/j.redox.2018.06.007 Yang, 2019, Pyridostigmine regulates glucose metabolism and mitochondrial homeostasis to reduce myocardial vulnerability to injury in diabetic mice, Am. J. Physiol. Endocrinol. Metabol., 317, 10.1152/ajpendo.00569.2018 Qian, 2018, Boosting ATM activity alleviates aging and extends lifespan in a mouse model of progeria, Elife, 7, 10.7554/eLife.34836 Bartoli-Leonard, 2021, Loss of SIRT1 in diabetes accelerates DNA damage-induced vascular calcification, Cardiovasc. Res., 117, 836, 10.1093/cvr/cvaa134 Charron, 1999, Implicating PARP and NAD+ depletion in type I diabetes, Nat. Med., 5, 269, 10.1038/6479 Li, 2017, A conserved NAD(+) binding pocket that regulates protein-protein interactions during aging, Science (New York, NY), 355, 1312, 10.1126/science.aad8242 Clem, 2008, Small-molecule inhibition of 6-phosphofructo-2-kinase activity suppresses glycolytic flux and tumor growth, Mol. Cancer Therapeut., 7, 110, 10.1158/1535-7163.MCT-07-0482 Crespo-Garcia, 2021, Pathological angiogenesis in retinopathy engages cellular senescence and is amenable to therapeutic elimination via BCL-xL inhibition, Cell Metabol., 33, 818, 10.1016/j.cmet.2021.01.011 Sawasdichai, 2010, In situ subcellular fractionation of adherent and non-adherent mammalian cells, JoVE, 41, 1958 Arnoult, 2017, Regulation of DNA repair pathway choice in S and G2 phases by the NHEJ inhibitor CYREN, Nature, 549, 548, 10.1038/nature24023 Fukumoto, 2019, N(6)-Methylation of adenosine of FZD10 mRNA contributes to PARP inhibitor resistance, Cancer Res., 79, 2812, 10.1158/0008-5472.CAN-18-3592