Set7 Deletion Prevents Glucose Intolerance and Improves the Recovery of Cardiac Function after Ischemia and Reperfusion in Obese Female Mice

Carregando...
Imagem de Miniatura
Citações na Scopus
3
Tipo de produção
article
Data de publicação
2022
Título da Revista
ISSN da Revista
Título do Volume
Editora
CELL PHYSIOL BIOCHEM PRESS GMBH CO KG
Autores
MIRANDA, J. B.
LUNARDON, G.
LIMA, V. M.
SILVA, T. de Oliveira
LINO, C. A.
SILVA, I. B. da
LU, Y. W.
LIU, J.
Citação
CELLULAR PHYSIOLOGY AND BIOCHEMISTRY, v.56, n.3, p.293-309, 2022
Projetos de Pesquisa
Unidades Organizacionais
Fascículo
Resumo
Background/Aims: An obesogenic diet (high fat and sugar, low fiber) is associated with an increased risk for metabolic and cardiovascular disorders. Previous studies have demonstrated that epigenetic changes can modify gene transcription and protein function, playing a key role in the development of several diseases. The methyltransferase Set7 methylates histone and non-histone proteins, influencing diverse biological and pathological processes. However, the functional role of Set7 in obesity-associated metabolic and cardiovascular complications is unknown. Methods: Wild type and Set7 knockout female mice were fed a normal diet or an obesogenic diet for 12 weeks. Body weight gain and glucose tolerance were measured. The 3T3-L1 cells were used to determine the role of Set7 in white adipogenic differentiation. Cardiac morphology and function were evaluated by histology and echocardiography. An ex vivo Langendorff perfusion system was used to model cardiac ischemia/reperfusion (I/R). Results: Here, we report that Set7 protein levels were enhanced in the heart and perigonadal adipose tissue (PAT) of female mice fed an obesogenic diet. Significantly, loss of Set7 prevented obesogenic diet-induced glucose intolerance in female mice although it did not affect the obesogenic diet-induced increase in body weight gain and adiposity in these animals, nor did Set7 inhibition change white adipogenic differentiation in vitro. In addition, loss of Set7 prevented the compromised cardiac functional recovery following ischemia and reperfusion (I/R) injury in obesogenic diet-fed female mice; however, deletion of Set7 did not influence obesogenic diet-induced cardiac hypertrophy nor the hemodynamic and echocardiographic parameters. Conclusion: These data indicate that Set7 plays a key role in obesogenic dietinduced glucose intolerance and compromised myocardial functional recovery after I/R in obese female mice. © 2022 Published The Author(s)
Palavras-chave
Female, Glucose intolerance, Ischemia and reperfusion, Obesity, Obesogenic diet, Set7
Referências
  1. Blüher, M, Obesity: global epidemiology and pathogenesis (2019) Nat Rev Endocrinol, 15, pp. 288-298
  2. Arnold, AP, Cassis, LA, Eghbali, M, Reue, K, Sandberg, K, Sex Hormones and Sex Chromosomes Cause Sex Differences in the Development of Cardiovascular Diseases (2017) Arterioscler Thromb Vasc Biol, 37, pp. 746-756
  3. Halland, H, Lønnebakken, MT, Pristaj, N, Saeed, S, Midtbø, H, Einarsen, E, Gerdts, E, Sex differences in subclinical cardiac disease in overweight and obesity (the FATCOR study) (2018) Nutr Metab Cardiovasc Dis, 28, pp. 1054-1060
  4. Manrique-Acevedo, C, Chinnakotla, B, Padilla, J, Martinez-Lemus, LA, Gozal, D, Obesity and cardiovascular disease in women (2020) Int J Obes, 44, pp. 1210-1226
  5. Toedebusch, R, Belenchia, A, Pulakat, L, Diabetic Cardiomyopathy: Impact of Biological Sex on Disease Development and Molecular Signatures (2018) Front Physiol, 9, p. 453
  6. Bortolin, RC, Vargas, AR, Gasparotto, J, Chaves, PR, Schnorr, CE, Martinello, KB, Silveira, AK, Moreira, JCF, A new animal diet based on human Western diet is a robust diet-induced obesity model: comparison to high-fat and cafeteria diets in term of metabolic and gut microbiota disruption (2018) Int J Obes, 42, pp. 525-534
  7. Bagchi, RA, Weeks, KL, Histone deacetylases in cardiovascular and metabolic diseases (2019) J Mol Cell Cardiol, 130, pp. 151-159
  8. Deiuliis, JA, MicroRNAs as regulators of metabolic disease: pathophysiologic significance and emerging role as biomarkers and therapeutics (2016) Int J Obes, 40, pp. 88-101
  9. Loh, M, Zhou, L, Ng, HK, Chambers, JC, Epigenetic disturbances in obesity and diabetes: Epidemiological and functional insights (2019) Mol Metab, 27, pp. S33-S41
  10. Ouni, M, Schürmann, A, Epigenetic contribution to obesity (2020) Mamm Genome, 31, pp. 134-145
  11. Wang, H, Cao, R, Xia, L, Erdjument-Bromage, H, Borchers, C, Tempst, P, Zhang, Y, Purification and Functional Characterization of a Histone H3-Lysine 4-Specific Methyltransferase (2001) Mol Cell, 8, pp. 1207-1217
  12. Nishioka, K, Set9, a novel histone H3 methyltransferase that facilitates transcription by precluding histone tail modifications required for heterochromatin formation (2002) Genes Dev, 16, pp. 479-489
  13. Tao, Y, Neppl, RL, Huang, ZP, Chen, J, Tang, RH, Cao, R, Zhang, Y, Wang, DZ, The histone methyltransferase Set7/9 promotes myoblast differentiation and myofibril assembly (2011) J Cell Biol, 194, pp. 551-565
  14. He, S, Owen, DR, Jelinsky, SA, Lin, LL, Lysine Methyltransferase SETD7 (SET7/9) Regulates ROS Signaling through mitochondria and NFE2L2/ARE pathway (2015) Sci Rep, 5, p. 14368
  15. Evans-Molina, C, Robbins, RD, Kono, T, Tersey, SA, Vestermark, GL, Nunemaker, CS, Garmey, JC, Mirmira, RG, Peroxisome Proliferator-Activated Receptor γ Activation Restores Islet Function in Diabetic Mice through Reduction of Endoplasmic Reticulum Stress and Maintenance of Euchromatin Structure (2009) Mol Cell Biol, 29, pp. 2053-2067
  16. Sun, G, Reddy, MA, Yuan, H, Lanting, L, Kato, M, Natarajan, R, Epigenetic Histone Methylation Modulates Fibrotic Gene Expression (2010) J Am Soc Nephrol, 21, pp. 2069-2080
  17. Batista I de, AA, Helguero, LA, Biological processes and signal transduction pathways regulated by the protein methyltransferase SETD7 and their significance in cancer (2018) Signal Transduct Target Ther, 3, p. 19
  18. Subramanian, K, Jia, D, Kapoor-Vazirani, P, Powell, DR, Collins, RE, Sharma, D, Peng, J, Vertino, PM, Regulation of Estrogen Receptor α by the SET7 Lysine Methyltransferase (2008) Mol Cell, 30, pp. 336-347
  19. Chuikov, S, Kurash, JK, Wilson, JR, Xiao, B, Justin, N, Ivanov, GS, McKinney, K, Reinberg, D, Regulation of p53 activity through lysine methylation (2004) Nature, 432, pp. 353-360
  20. Calnan, DR, Webb, AE, White, JL, Stowe, TR, Goswami, T, Shi, X, Espejo, A, Brunet, A, Methylation by Set9 modulates FoxO3 stability and transcriptional activity (2012) Aging (Albany NY), 4, pp. 462-479
  21. Dhayalan, A, Kudithipudi, S, Rathert, P, Jeltsch, A, Specificity Analysis-Based Identification of New Methylation Targets of the SET7/9 Protein Lysine Methyltransferase (2011) Chem Biol, 18, pp. 111-120
  22. Shen, C, Wang, D, Liu, X, Gu, B, Du, Y, Wei, F, Cao, L, Zhu, W, SET7/9 regulates cancer cell proliferation by influencing β-catenin stability (2015) FASEB J, 29, pp. 4313-4323
  23. Maganti, A V., Maier, B, Tersey, SA, Sampley, ML, Mosley, AL, Özcan, S, Pachaiyappan, B, Mirmira, RG, Transcriptional Activity of the Islet β Cell Factor Pdx1 Is Augmented by Lysine Methylation Catalyzed by the Methyltransferase Set7/9 (2015) J Biol Chem, 290, pp. 9812-9822
  24. Aguilo, F, Li, S, Balasubramaniyan, N, Sancho, A, Benko, S, Zhang, F, Vashisht, A, Walsh, MJ, Deposition of 5-Methylcytosine on Enhancer RNAs Enables the Coactivator Function of PGC-1α (2016) Cell Rep, 14, pp. 479-492
  25. Liu, X, Wang, D, Zhao, Y, Tu, B, Zheng, Z, Wang, L, Wang, H, Zhu, WG, Methyltransferase Set7/9 regulates p53 activity by interacting with Sirtuin 1 (SIRT1) (2011) Proc Natl Acad Sci, 108, pp. 1925-1930
  26. Li, Y, Reddy, MA, Miao, F, Shanmugam, N, Yee, JK, Hawkins, D, Ren, B, Natarajan, R, Role of the Histone H3 Lysine 4 Methyltransferase, SET7/9, in the Regulation of NF-κB-dependent Inflammatory Genes (2008) J Biol Chem, 283, pp. 26771-26781
  27. Liu, X, Chen, Z, Xu, C, Leng, X, Cao, H, Ouyang, G, Xiao, W, Repression of hypoxia-inducible factor α signaling by Set7-mediated methylation (2015) Nucleic Acids Res, 43, pp. 5081-5098
  28. Sharma, N, Sankrityayan, H, Kale, A, Gaikwad, AB, Role of SET7/9 in the progression of ischemic renal injury in diabetic and non-diabetic rats (2020) Biochem Biophys Res Commun, 528, pp. 14-20
  29. Malek, V, Sharma, N, Gaikwad, AB, Simultaneous inhibition of neprilysin and activation of ACE2 prevented diabetic cardiomyopathy (2019) Pharmacol Reports, 71, pp. 958-967
  30. Kurash, JK, Lei, H, Shen, Q, Marston, WL, Granda, BW, Fan, H, Wall, D, Gaudet, F, Methylation of p53 by Set7/9 Mediates p53 Acetylation and Activity In Vivo (2008) Mol Cell, 29, pp. 392-400
  31. De Oliveira Silva, T, Lino, CA, Buzatto, VC, Fontes Asprino, P, Lu, YW, Lima, VM, Fonseca, RIB, Diniz, GP, Deletion of miRNA-22 Induces Cardiac Hypertrophy in Females but Attenuates Obesogenic Diet-Mediated Metabolic Disorders (2020) Cell Physiol Biochem, 54, pp. 1199-1217
  32. Festuccia, WT, Blanchard, PG, Belchior, T, Chimin, P, Paschoal, VA, Magdalon, J, Hirabara, SM, Deshaies, Y, PPARγ activation attenuates glucose intolerance induced by mTOR inhibition with rapamycin in rats (2014) Am J Physiol Metab, 306, pp. E1046-E1054
  33. Da Silva, IB, Gomes, DA, Alenina, N, Bader, M, dos Santos, RA, Barreto-Chaves, MLM, Cardioprotective effect of thyroid hormone is mediated by AT2 receptor and involves nitric oxide production via Akt activation in mice (2018) Heart Vessels, 33, pp. 671-681
  34. Guedes, EC, da Silva, IB, Lima, VM, Miranda, JB, Albuquerque, RP, Ferreira, JCB, Barreto-Chaves, MLM, Diniz, GP, High fat diet reduces the expression of miRNA-29b in heart and increases susceptibility of myocardium to ischemia/reperfusion injury (2019) J Cell Physiol, 234, pp. 9399-9407
  35. Lima, VM, Liu, J, Brandão, BB, Lino, CA, Balbino Silva, CS, Ribeiro, MAC, Oliveira, TE, Diniz, GP, miRNA-22 deletion limits white adipose expansion and activates brown fat to attenuate high-fat diet-induced fat mass accumulation (2021) Metabolism, 117, p. 154723
  36. Barsyte-Lovejoy, D, Li, F, Oudhoff, MJ, Tatlock, JH, Dong, A, Zeng, H, Wu, H, Fish, PV, (R)-PFI-2 is a potent and selective inhibitor of SETD7 methyltransferase activity in cells (2014) Proc Natl Acad Sci, 111, pp. 12853-12858
  37. Wakabayashi, K, Okamura, M, Tsutsumi, S, Nishikawa, NS, Tanaka, T, Sakakibara, I, Kitakami, J, Sakai, J, The Peroxisome Proliferator-Activated Receptor γ/Retinoid X Receptor α Heterodimer Targets the Histone Modification Enzyme PR-Set7/Setd8 Gene and Regulates Adipogenesis through a Positive Feedback Loop (2009) Mol Cell Biol, 29, pp. 3544-3555
  38. Hamidi, T, Singh, AK, Veland, N, Vemulapalli, V, Chen, J, Hardikar, S, Bao, J, Chen, T, Identification of Rpl29 as a major substrate of the lysine methyltransferase Set7/9 (2018) J Biol Chem, 293, pp. 12770-12780
  39. Blankesteijn, W, Vandeschans, V, Terhorst, P, Smits, J, The Wnt/frizzled/GSK-3β pathway: a novel therapeutic target for cardiac hypertrophy (2008) Trends Pharmacol Sci, 29, pp. 175-180
  40. Passariello, CL, Li, J, Dodge-Kafka, K, Kapiloff, MS, mAKAP—A Master Scaffold for Cardiac Remodeling (2015) J Cardiovasc Pharmacol, 65, pp. 218-225
  41. Tremblay, ML, Giguère, V, Phosphatases at the Heart of FoxO Metabolic Control (2008) Cell Metab, 7, pp. 101-103
  42. Song, H, Feng, X, Zhang, M, Jin, X, Xu, X, Wang, L, Ding, X, Zhang, Z, Crosstalk between lysine methylation and phosphorylation of ATG16L1 dictates the apoptosis of hypoxia/ reoxygenation-induced cardiomyocytes (2018) Autophagy, 14, pp. 825-844
  43. Dang, Y, Ma, X, Li, Y, Hao, Q, Xie, Y, Zhang, Q, Zhang, F, Qi, X, Inhibition of SETD7 protects cardiomyocytes against hypoxia/reoxygenation-induced injury through regulating Keap1/Nrf2 signaling (2018) Biomed Pharmacother, 106, pp. 842-849
  44. Lee, J, Shao, N, Paik, DT, Wu, H, Guo, H, Termglinchan, V, Churko, JM, Wu, JC, SETD7 Drives Cardiac Lineage Commitment through Stage-Specific Transcriptional Activation (2018) Cell Stem Cell, 22, pp. 428-444. , e5
  45. O’Sullivan, KE, Breen, EP, Gallagher, HC, Buggy, DJ, Hurley, JP, Understanding STAT3 signaling in cardiac ischemia (2016) Basic Res Cardiol, 111, p. 27
  46. Yang, J, Huang, J, Dasgupta, M, Sears, N, Miyagi, M, Wang, B, Chance, MR, Stark, GR, Reversible methylation of promoter-bound STAT3 by histone-modifying enzymes (2010) Proc Natl Acad Sci, 107, pp. 21499-21504
  47. De Souza, GO, Wasinski, F, Donato, J, Characterization of the metabolic differences between male and female C57BL/6 mice (2022) Life Sci, 301, p. 120636
  48. Casimiro, I, Stull, ND, Tersey, SA, Mirmira, RG, Phenotypic sexual dimorphism in response to dietary fat manipulation in C57BL/6J mice (2021) J Diabetes Complications, 35, p. 107795
  49. Griffin, C, Lanzetta, N, Eter, L, Singer, K, Sexually dimorphic myeloid inflammatory and metabolic responses to diet-induced obesity (2016) Am J Physiol Integr Comp Physiol, 311, pp. R211-R216
  50. Macotela, Y, Boucher, J, Tran, TT, Kahn, CR, Sex and Depot Differences in Adipocyte Insulin Sensitivity and Glucose Metabolism (2009) Diabetes, 58, pp. 803-812
  51. Winn, NC, Vieira-Potter, VJ, Gastecki, ML, Welly, RJ, Scroggins, RJ, Zidon, TM, Gaines, TL, Padilla, J, Loss of UCP1 exacerbates Western diet-induced glycemic dysregulation independent of changes in body weight in female mice (2017) Am J Physiol Integr Comp Physiol, 312, pp. R74-R84
  52. Jetton, TL, Flores-Bringas, P, Leahy, JL, Gupta, D, SetD7 (Set7/9) is a novel target of PPARγ that promotes the adaptive pancreatic β-cell glycemic response (2021) J Biol Chem, 297, p. 101250
  53. Son, MJ, Kim, WK, Oh, KJ, Park, A, Lee, DS, Han, BS, Lee, SC, Bae, KH, Methyltransferase and demethylase profiling studies during brown adipocyte differentiation (2016) BMB Rep, 49, pp. 388-393
  54. Son, MJ, Kim, WK, Park, A, Oh, KJ, Kim, JH, Han, BS, Kim, IC, Bae, KH, Set7/9, a methyltransferase, regulates the thermogenic program during brown adipocyte differentiation through the modulation of p53 acetylation (2016) Mol Cell Endocrinol, 431, pp. 46-53
  55. Elkouris, M, Kontaki, H, Stavropoulos, A, Antonoglou, A, Nikolaou, KC, Samiotaki, M, Szantai, E, Talianidis, I, SET9-Mediated Regulation of TGF-β Signaling Links Protein Methylation to Pulmonary Fibrosis (2016) Cell Rep, 15, pp. 2733-2744
  56. Sasaki, K, Doi, S, Nakashima, A, Irifuku, T, Yamada, K, Kokoroishi, K, Ueno, T, Masaki, T, Inhibition of SET Domain–Containing Lysine Methyltransferase 7/9 Ameliorates Renal Fibrosis (2016) J Am Soc Nephrol, 27, pp. 203-215
  57. Tamura, R, Doi, S, Nakashima, A, Sasaki, K, Maeda, K, Ueno, T, Masaki, T, Inhibition of the H3K4 methyltransferase SET7/9 ameliorates peritoneal fibrosis (2018) PLoS One, 13, p. e0196844
  58. Aoyagi, T, Higa, JK, Aoyagi, H, Yorichika, N, Shimada, BK, Matsui, T, Cardiac mTOR rescues the detrimental effects of diet-induced obesity in the heart after ischemia-reperfusion (2015) Am J Physiol Circ Physiol, 308, pp. H1530-H1539
  59. Liu, J, Wang, P, Zou, L, Qu, J, Litovsky, S, Umeda, P, Zhou, L, Lloyd, SG, High-fat, low-carbohydrate diet promotes arrhythmic death and increases myocardial ischemia-reperfusion injury in rats (2014) Am J Physiol Circ Physiol, 307, pp. H598-H608
  60. Thakker, GD, Frangogiannis, NG, Zymek, PT, Sharma, S, Raya, JL, Barger, PM, Taegtmeyer, H, Ballantyne, CM, Increased Myocardial Susceptibility to Repetitive Ischemia With High-fat diet-induced Obesit (2008) Obesity, 16, pp. 2593-2600
  61. Tan, Y, Mui, D, Toan, S, Zhu, P, Li, R, Zhou, H, SERCA Overexpression Improves Mitochondrial Quality Control and Attenuates Cardiac Microvascular Ischemia-Reperfusion Injury (2020) Mol Ther - Nucleic Acids, 22, pp. 696-707
  62. Vande Walle, L, Lamkanfi, M, Pyroptosis (2016) Curr Biol, 26, pp. R568-R572
  63. Shamas-Din, A, Kale, J, Leber, B, Andrews, DW, Mechanisms of Action of Bcl-2 Family Proteins (2013) Cold Spring Harb Perspect Biol, 5, pp. a008714-a008714
  64. Ballal, K, Wilson, CR, Harmancey, R, Taegtmeyer, H, Obesogenic high fat western diet induces oxidative stress and apoptosis in rat heart (2010) Mol Cell Biochem, 344, pp. 221-230
  65. Zhang, N, Ye, F, Zhu, W, Hu, D, Xiao, C, Nan, J, Su, S, Wang, J, Cardiac ankyrin repeat protein attenuates cardiomyocyte apoptosis by upregulation of Bcl-2 expression (2016) Biochim Biophys Acta - Mol Cell Res, 1863, pp. 3040-3049
  66. Sepúlveda, P, Encabo, A, Carbonell-Uberos, F, Miñana, MD, BCL-2 expression is mainly regulated by JAK/ STAT3 pathway in human CD34+ hematopoietic cells (2007) Cell Death Differ, 14, pp. 378-380