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Endocrine, Metabolic & Immune Disorders - Drug Targets

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ISSN (Print): 1871-5303
ISSN (Online): 2212-3873

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Research Article

Chronic Inorganic Nitrate Administration Increases the Expression of Genes Involved in the Browning of Gonadal Adipose Tissue in Ovariectomized Rats

Author(s): Nasibeh Yousefzadeh, Sajad Jeddi and Asghar Ghasemi*

Volume 24, Issue 7, 2024

Published on: 02 November, 2023

Page: [820 - 831] Pages: 12

DOI: 10.2174/0118715303239481231030043730

Price: $65

Abstract

Background and Objective: Nitrate, as nitric oxide (NO) donor, has been suggested as a nutrition-based treatment for decreasing the risk of menopause-related obesity. This study aimed to specify the effects of chronic inorganic nitrate administration on uncoupling protein-1 (UCP-1), peroxisome proliferator-activated-receptor-γ (PPAR-γ) coactivator-1α (PGC-1α), and PPAR-γ expression in gonadal adipose tissue (GAT) of ovariectomized (OVX) rats.

Methods: Female rats were assigned to 3 groups: Control, OVX, and OVX+nitrate (n=7/group), which consumed water containing inorganic nitrate (100 mg/L) for 9 months. At month 9, GAT was used for the measurement of NO metabolites (NOx), mRNA levels of NO synthases (endothelial (eNOS), inducible (iNOS), neuronal (nNOS)), and mRNA and protein levels of UCP-1, PGC-1α, and PPAR-γ.

Results: OVX rats had lower NOx concentration (45%) and eNOS (38%) and nNOS (30%) expression in GAT that was restored to normal values following nitrate administration. OVX rats had significantly lower mRNA and protein levels of UCP-1 (83% and 30%), PGC-1α (65% and 39%), and PPAR-γ (66% and 34.5%) in GAT. Chronic inorganic nitrate administration in OVXrats increased mRNA and protein levels of UCP-1 (128% and 34%), PGC-1α (115% and 43%), and PPAR-γ (236% and 38%), respectively.

Conclusion: In OVX rats, chronic nitrate administration increased gene and protein levels of UCP-1, PGC-1α, and PPAR-γ in GAT, indicating the anti-obesity effects of nitrate are partially mediated by the white adipose tissue (WAT) browning. Moreover, the stimulatory effect of inorganic nitrate on the WAT browning in OVX rats was associated with blunting the OVXinduced NO deficiency in GAT.

Keywords: Nitrate, nitric oxide, female rats, gonadal adipose tissue, browning of WAT, anti-obesity effects.

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[1]
World Obesity Federation. World Obesity Atlas; , 2022. Available from: https://s3-eu-west-1.amazonaws.com/wof-files/World_Obesit y_Atlas_2022.pdf
[2]
World Obesity Federation. World Obesity Atlas; , 2023. Available from: https://s3-eu-west-1.amazonaws.com/wof-files/World_Obesit y_Atlas_2023_Report.pdf
[3]
Lovejoy, J.C. The menopause and obesity. Prim. Care, 2003, 30(2), 317-325.
[http://dx.doi.org/10.1016/S0095-4543(03)00012-5] [PMID: 14567150]
[4]
Simkinsilverman, L.; Wing, R.R.; Hansen, D.H.; Klem, M.L.; Pasagianmacaulay, A.; Meilahn, E.N.; Kuller, L.H. Prevention of cardiovascular risk factor elevations in healthy premenopausal women. Prev. Med., 1995, 24(5), 509-517.
[http://dx.doi.org/10.1006/pmed.1995.1081] [PMID: 8524727]
[5]
Li, Q.; Wang, X.; Ni, Y.; Hao, H.; Liu, Z.; Wen, S.; Shao, X.; Wu, X.; Yu, W.; Hu, W. Epidemiological characteristics and risk factors of T2DM in Chinese premenopausal and postmenopausal women. Lipids Health Dis., 2019, 18(1), 155.
[http://dx.doi.org/10.1186/s12944-019-1091-7] [PMID: 31315681]
[6]
Chen, J.L.; Guo, J.; Mao, P.; Yang, J.; Jiang, S.; He, W.; Lin, C.X.; Lien, K. Are the factors associated with overweight/general obesity and abdominal obesity different depending on menopausal status? PLoS One, 2021, 16(2), e0245150.
[http://dx.doi.org/10.1371/journal.pone.0245150] [PMID: 33539356]
[7]
Rosselli, M.; Imthurn, B.; Keller, P.J.; Jackson, E.K.; Dubey, R.K. Circulating nitric oxide (nitrite/nitrate) levels in postmenopausal women substituted with 17 beta-estradiol and norethisterone acetate. A two-year follow-up study. Hypertension, 1995, 25(4), 848-853.
[http://dx.doi.org/10.1161/01.HYP.25.4.848] [PMID: 7721443]
[8]
Kim, F.; Pham, M.; Maloney, E.; Rizzo, N.O.; Morton, G.J.; Wisse, B.E.; Kirk, E.A.; Chait, A.; Schwartz, M.W. Vascular inflammation, insulin resistance, and reduced nitric oxide production precede the onset of peripheral insulin resistance. Arterioscler. Thromb. Vasc. Biol., 2008, 28(11), 1982-1988.
[http://dx.doi.org/10.1161/ATVBAHA.108.169722] [PMID: 18772497]
[9]
Yousefzadeh, N.; Jeddi, S.; Shokri, M.; Afzali, H.; Norouzirad, R.; Kashfi, K.; Ghasemi, A. Long term sodium nitrate administration positively impacts metabolic and obesity indices in ovariectomized rats. Arch. Med. Res., 2022, 53(2), 147-156.
[http://dx.doi.org/10.1016/j.arcmed.2021.09.007] [PMID: 34696904]
[10]
Franquesa, M.; Pujol-Busquets, G.; García-Fernández, E.; Rico, L.; Shamirian-Pulido, L.; Aguilar-Martínez, A.; Medina, F.; Serra-Majem, L.; Bach-Faig, A. Mediterranean diet and cardiodiabesity: A systematic review through evidence-based answers to key clinical questions. Nutrients, 2019, 11(3), 655.
[http://dx.doi.org/10.3390/nu11030655] [PMID: 30889891]
[11]
Jackson, J.; Patterson, A.J.; MacDonald-Wicks, L.; McEvoy, M. The role of inorganic nitrate and nitrite in CVD. Nutr. Res. Rev., 2017, 30(2), 247-264.
[http://dx.doi.org/10.1017/S0954422417000105] [PMID: 28566109]
[12]
Shannon, O.M.; Stephan, B.C.M.; Minihane, A.M.; Mathers, J.C.; Siervo, M. Nitric oxide boosting effects of the Mediterranean diet: A potential mechanism of action. J. Gerontol. A Biol. Sci. Med. Sci., 2018, 73(7), 902-904.
[http://dx.doi.org/10.1093/gerona/gly087] [PMID: 29684102]
[13]
Bahadoran, Z.; Jeddi, S.; Gheibi, S.; Mirmiran, P.; Kashfi, K.; Ghasemi, A. Inorganic nitrate, a natural anti-obesity agent: A systematic review and meta-analysis of animal studies. EXCLI J., 2020, 19, 972-983.
[http://dx.doi.org/10.1155/2018/7969750] [PMID: 32788911]
[14]
Khorasani, V.; Jeddi, S.; Yaghmaei, P.; Tohidi, M.; Ghasemi, A. Effect of long-term sodium nitrate administration on diabetes-induced anemia and glucose homeostasis in obese type 2 diabetic male rats. Nitric Oxide, 2019, 86, 21-30.
[http://dx.doi.org/10.1016/j.niox.2019.02.003] [PMID: 30772502]
[15]
Carlström, M.; Larsen, F.J.; Nyström, T.; Hezel, M.; Borniquel, S.; Weitzberg, E.; Lundberg, J.O. Dietary inorganic nitrate reverses features of metabolic syndrome in endothelial nitric oxide synthase-deficient mice. Proc. Natl. Acad. Sci. USA, 2010, 107(41), 17716-17720.
[http://dx.doi.org/10.1073/pnas.1008872107] [PMID: 20876122]
[16]
Roberts, L.D.; Ashmore, T.; Kotwica, A.O.; Murfitt, S.A.; Fernandez, B.O.; Feelisch, M.; Murray, A.J.; Griffin, J.L. Inorganic nitrate promotes the browning of white adipose tissue through the nitrate-nitrite-nitric oxide pathway. Diabetes, 2015, 64(2), 471-484.
[http://dx.doi.org/10.2337/db14-0496] [PMID: 25249574]
[17]
van Marken Lichtenbelt, W.D.; Vanhommerig, J.W.; Smulders, N.M.; Drossaerts, J.M.A.F.L.; Kemerink, G.J.; Bouvy, N.D.; Schrauwen, P.; Teule, G.J.J. Cold-activated brown adipose tissue in healthy men. N. Engl. J. Med., 2009, 360(15), 1500-1508.
[http://dx.doi.org/10.1056/NEJMoa0808718] [PMID: 19357405]
[18]
Shen, H.H.; Huang, S.Y.; Kung, C.W.; Chen, S.Y.; Chen, Y.F.; Cheng, P.Y.; Lam, K.K.; Lee, Y.M. Genistein ameliorated obesity accompanied with adipose tissue browning and attenuation of hepatic lipogenesis in ovariectomized rats with high-fat diet. J. Nutr. Biochem., 2019, 67, 111-122.
[http://dx.doi.org/10.1016/j.jnutbio.2019.02.001] [PMID: 30884354]
[19]
Sievers, W.; Rathner, J.A.; Kettle, C.; Zacharias, A.; Irving, H.R.; Green, R.A. The capacity for oestrogen to influence obesity through brown adipose tissue thermogenesis in animal models: A systematic review and meta-analysis. Obes. Sci. Pract., 2019, 5(6), 592-602.
[http://dx.doi.org/10.1002/osp4.368] [PMID: 31890250]
[20]
Cypess, A.M.; Lehman, S.; Williams, G.; Tal, I.; Rodman, D.; Goldfine, A.B.; Kuo, F.C.; Palmer, E.L.; Tseng, Y.H.; Doria, A.; Kolodny, G.M.; Kahn, C.R. Identification and importance of brown adipose tissue in adult humans. N. Engl. J. Med., 2009, 360(15), 1509-1517.
[http://dx.doi.org/10.1056/NEJMoa0810780] [PMID: 19357406]
[21]
Kontani, Y.; Wang, Y.; Kimura, K.; Inokuma, K.I.; Saito, M.; Suzuki-Miura, T.; Wang, Z.; Sato, Y.; Mori, N.; Yamashita, H. UCP1 deficiency increases susceptibility to diet-induced obesity with age. Aging Cell, 2005, 4(3), 147-155.
[http://dx.doi.org/10.1111/j.1474-9726.2005.00157.x] [PMID: 15924571]
[22]
Gupta, D.; Kono, T.; Evans-Molina, C. The role of peroxisome proliferator-activated receptor γ in pancreatic β cell function and survival: Therapeutic implications for the treatment of type 2 diabetes mellitus. Diabetes Obes. Metab., 2010, 12(12), 1036-1047.
[http://dx.doi.org/10.1111/j.1463-1326.2010.01299.x] [PMID: 20977574]
[23]
Kleiner, S.; Mepani, R.J.; Laznik, D.; Ye, L.; Jurczak, M.J.; Jornayvaz, F.R.; Estall, J.L.; Chatterjee Bhowmick, D.; Shulman, G.I.; Spiegelman, B.M. Development of insulin resistance in mice lacking PGC-1α in adipose tissues. Proc. Natl. Acad. Sci. USA, 2012, 109(24), 9635-9640.
[http://dx.doi.org/10.1073/pnas.1207287109] [PMID: 22645355]
[24]
Peleli, M.; Ferreira, D.M.S.; Tarnawski, L.; McCann Haworth, S.; Xuechen, L.; Zhuge, Z.; Newton, P.T.; Massart, J.; Chagin, A.S.; Olofsson, P.S.; Ruas, J.L.; Weitzberg, E.; Lundberg, J.O.; Carlström, M. Dietary nitrate attenuates high-fat diet-induced obesity via mechanisms involving higher adipocyte respiration and alterations in inflammatory status. Redox Biol., 2020, 28, 101387.
[http://dx.doi.org/10.1016/j.redox.2019.101387] [PMID: 31765889]
[25]
Jeddi, S.; Yousefzadeh, N.; Afzali, H.; Ghasemi, A. Long-term nitrate administration increases expression of browning genes in epididymal adipose tissue of male type 2 diabetic rats. Gene, 2021, 766, 145155.
[http://dx.doi.org/10.1016/j.gene.2020.145155] [PMID: 32950634]
[26]
Flegal, K.M.; Kruszon-Moran, D.; Carroll, M.D.; Fryar, C.D.; Ogden, C.L. Trends in obesity among adults in the United States, 2005 to 2014. JAMA, 2016, 315(21), 2284-2291.
[http://dx.doi.org/10.1001/jama.2016.6458] [PMID: 27272580]
[27]
Clayton, J.A.; Collins, F.S. Policy: NIH to balance sex in cell and animal studies. Nature, 2014, 509(7500), 282-283.
[http://dx.doi.org/10.1038/509282a] [PMID: 24834516]
[28]
Jackson, J.K.; Patterson, A.J.; MacDonald-Wicks, L.K.; Oldmeadow, C.; McEvoy, M.A. The role of inorganic nitrate and nitrite in cardiovascular disease risk factors: A systematic review and meta-analysis of human evidence. Nutr. Rev., 2018, 76(5), 348-371.
[http://dx.doi.org/10.1093/nutrit/nuy005] [PMID: 29506204]
[29]
Kapil, V.; Milsom, A.B.; Okorie, M.; Maleki-Toyserkani, S.; Akram, F.; Rehman, F.; Arghandawi, S.; Pearl, V.; Benjamin, N.; Loukogeorgakis, S.; MacAllister, R.; Hobbs, A.J.; Webb, A.J.; Ahluwalia, A. Inorganic nitrate supplementation lowers blood pressure in humans: Role for nitrite-derived NO. Hypertension, 2010, 56(2), 274-281.
[http://dx.doi.org/10.1161/HYPERTENSIONAHA.110.153536] [PMID: 20585108]
[30]
Wang, Q.; Zhang, M.; Xu, M.; Gu, W.; Xi, Y.; Qi, L.; Li, B.; Wang, W. Brown adipose tissue activation is inversely related to central obesity and metabolic parameters in adult human. PLoS One, 2015, 10(4), e0123795-e0123795.
[http://dx.doi.org/10.1371/journal.pone.0123795] [PMID: 25894250]
[31]
Nookaew, I.; Svensson, P.A.; Jacobson, P.; Jernås, M.; Taube, M.; Larsson, I.; Andersson-Assarsson, J.C.; Sjöström, L.; Froguel, P.; Walley, A.; Nielsen, J.; Carlsson, L.M.S. Adipose tissue resting energy expenditure and expression of genes involved in mitochondrial function are higher in women than in men. J. Clin. Endocrinol. Metab., 2013, 98(2), E370-E378.
[http://dx.doi.org/10.1210/jc.2012-2764] [PMID: 23264395]
[32]
Yousefzadeh, N.; Jeddi, S.; Afzali, H.; Kashfi, K.; Ghasemi, A. Chronic nitrate administration increases the expression the genes involved in the browning of white adipose tissue in female rats. Cell Biochem. Funct., 2022, 40(7), 750-759.
[http://dx.doi.org/10.1002/cbf.3741] [PMID: 36098488]
[33]
Percie du Sert, N.; Hurst, V.; Ahluwalia, A.; Alam, S.; Avey, M.T.; Baker, M.; Browne, W.J.; Clark, A.; Cuthill, I.C.; Dirnagl, U.; Emerson, M.; Garner, P.; Holgate, S.T.; Howells, D.W.; Karp, N.A.; Lazic, S.E.; Lidster, K.; MacCallum, C.J.; Macleod, M.; Pearl, E.J.; Petersen, O.H.; Rawle, F.; Reynolds, P.; Rooney, K.; Sena, E.S.; Silberberg, S.D.; Steckler, T.; Würbel, H. The ARRIVE guidelines 2.0: Updated guidelines for reporting animal research. PLoS Biol., 2020, 18(7), e3000410.
[http://dx.doi.org/10.1371/journal.pbio.3000410] [PMID: 32663219]
[34]
Yousefzadeh, N.; Kashfi, K.; Jeddi, S.; Ghasemi, A. Ovariectomized rat model of osteoporosis: A practical guide. EXCLI J., 2020, 19, 89-107.
[http://dx.doi.org/10.17179/excli2019-1990] [PMID: 32038119]
[35]
Bate, S.T.; Clark, R.A. The design and statistical analysis of animal experiments, Cambridge University; Press, 2014, pp. 13-133.
[http://dx.doi.org/10.1017/CBO9781139344319]
[36]
Gheibi, S.; Jeddi, S.; Carlström, M.; Kashfi, K.; Ghasemi, A. Hydrogen sulfide potentiates the favorable metabolic effects of inorganic nitrite in type 2 diabetic rats. Nitric Oxide, 2019, 92, 60-72.
[http://dx.doi.org/10.1016/j.niox.2019.08.006] [PMID: 31479766]
[37]
Bakhtiarzadeh, F.; Siavoshi, F.; Gheibi, S.; Kashfi, K.; Samadi, R.; Jeddi, S.; Ghasemi, A. Effects of long-term oral nitrate administration on adiposity in normal adult female rats. Life Sci., 2018, 210, 76-85.
[http://dx.doi.org/10.1016/j.lfs.2018.08.032] [PMID: 30118772]
[38]
Khalifi, S.; Rahimipour, A.; Jeddi, S.; Ghanbari, M.; Kazerouni, F.; Ghasemi, A. Dietary nitrate improves glucose tolerance and lipid profile in an animal model of hyperglycemia. Nitric Oxide, 2015, 44, 24-30.
[http://dx.doi.org/10.1016/j.niox.2014.11.011] [PMID: 25461274]
[39]
Jeddi, S.; Khalifi, S.; Ghanbari, M.; Bageripour, F.; Ghasemi, A. Effects of nitrate intake on myocardial ischemia-reperfusion injury in diabetic rats. Arq. Bras. Cardiol., 2016, 107(4), 339-347.
[http://dx.doi.org/10.5935/abc.20160137] [PMID: 27849257]
[40]
Yousefzadeh, N.; Jeddi, S.; Kashfi, K.; Ghasemi, A. Long-term inorganic nitrate administration protects against ovariectomy-induced osteoporosis in rats. EXCLI J., 2022, 21, 1151-1166.
[http://dx.doi.org/10.17179/excli2022-5082] [PMID: 36320805]
[41]
Yousefzadeh, N.; Jeddi, S.; Zarkesh, M.; Norouzirad, R.; Kashfi, K.; Ghasemi, A. Protective effects of long-term nitrate administration against ovariectomy-induced kidney dysfunction in rats. Pharmacol. Rep., 2023, 75(4), 979-994.
[http://dx.doi.org/10.1007/s43440-023-00499-9] [PMID: 37258800]
[42]
Bahadoran, Z.; Norouzirad, R.; Mirmiran, P.; Gaeini, Z.; Jeddi, S.; Shokri, M.; Azizi, F.; Ghasemi, A. Effect of inorganic nitrate on metabolic parameters in patients with type 2 diabetes: A 24-week randomized double-blind placebo-controlled clinical trial. Nitric Oxide, 2021, 107, 58-65.
[http://dx.doi.org/10.1016/j.niox.2020.12.005] [PMID: 33340674]
[43]
Miranda, K.M.; Espey, M.G.; Wink, D.A. A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide, 2001, 5(1), 62-71.
[http://dx.doi.org/10.1006/niox.2000.0319] [PMID: 11178938]
[44]
Ghasemi, A.; Hedayati, M.; Biabani, H. Protein precipitation methods evaluated for determination of serum nitric oxide end products by the Griess assay. J. Med. Sci. Res., 2007, 2, 29-32.
[45]
Navarro-Gonzálvez, J.A.; García-Benayas, C.; Arenas, J. Semiautomated measurement of nitrate in biological fluids. Clin. Chem., 1998, 44(3), 679-681.
[http://dx.doi.org/10.1093/clinchem/44.3.679] [PMID: 9510886]
[46]
Pfaffl, M.W.; Horgan, G.W.; Dempfle, L. Relative expression software tool (REST(C)) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res., 2002, 30(9), 36e-36.
[http://dx.doi.org/10.1093/nar/30.9.e36] [PMID: 11972351]
[47]
Lee, S.; Lee, D.K. What is the proper way to apply the multiple comparison test? Korean J. Anesthesiol., 2018, 71(5), 353-360.
[http://dx.doi.org/10.4097/kja.d.18.00242] [PMID: 30157585]
[48]
Lirani-Galvão, A.P.R.; Chavassieux, P.; Portero-Muzy, N.; Bergamaschi, C.T.; Silva, O.L.; Carvalho, A.B.; Lazaretti-Castro, M.; Delmas, P.D. Low-intensity electrical stimulation counteracts the effects of ovariectomy on bone tissue of rats: effects on bone microarchitecture, viability of osteocytes, and nitric oxide expression. Calcif. Tissue Int., 2009, 84(6), 502-509.
[http://dx.doi.org/10.1007/s00223-009-9227-9] [PMID: 19458889]
[49]
Maric, C.; Xu, Q.; Sandberg, K.; Hinojosa-Laborde, C. Age-related renal disease in female Dahl salt-sensitive rats is attenuated with 172-estradiol supplementation by modulating nitric oxide synthase expression. Gend. Med., 2008, 5(2), 147-159.
[http://dx.doi.org/10.1016/j.genm.2008.05.002] [PMID: 18573482]
[50]
Xia, Y.; Krukoff, T.L. Estrogen induces nitric oxide production via activation of constitutive nitric oxide synthases in human neuroblastoma cells. Endocrinology, 2004, 145(10), 4550-4557.
[http://dx.doi.org/10.1210/en.2004-0327] [PMID: 15242984]
[51]
García-Durán, M.; de Frutos, T.; Díaz-Recasens, J.; García-Gálvez, G.; Jiménez, A.; Montón, M.; Farré, J.; de Miguel, L.S.; González-Fernández, F.; Arriero, M.M.; Rico, L.; García, R.; Casado, S.; López-Farré, A. Estrogen stimulates neuronal nitric oxide synthase protein expression in human neutrophils. Circ. Res., 1999, 85(11), 1020-1026.
[http://dx.doi.org/10.1161/01.RES.85.11.1020] [PMID: 10571532]
[52]
Hisamoto, K.; Ohmichi, M.; Kurachi, H.; Hayakawa, J.; Kanda, Y.; Nishio, Y.; Adachi, K.; Tasaka, K.; Miyoshi, E.; Fujiwara, N.; Taniguchi, N.; Murata, Y. Estrogen induces the Akt-dependent activation of endothelial nitric-oxide synthase in vascular endothelial cells. J. Biol. Chem., 2001, 276(5), 3459-3467.
[http://dx.doi.org/10.1074/jbc.M005036200] [PMID: 11044445]
[53]
Monsalve, E.; Oviedo, P.; Garcíapérez, M.; Tarín, J.; Cano, A.; Hermenegildo, C. Estradiol counteracts oxidized LDL-induced asymmetric dimethylarginine production by cultured human endothelial cells. Cardiovasc. Res., 2007, 73(1), 66-72.
[http://dx.doi.org/10.1016/j.cardiores.2006.09.020] [PMID: 17097077]
[54]
Dantas, A.P.V.; Tostes, R.C.A.; Fortes, Z.B.; Costa, S.G.; Nigro, D.; Carvalho, M.H.C. In vivo evidence for antioxidant potential of estrogen in microvessels of female spontaneously hypertensive rats. Hypertension, 2002, 39(2), 405-411.
[http://dx.doi.org/10.1161/hy0202.102993] [PMID: 11882581]
[55]
Sumi, D.; Ignarro, L.J. Estrogen-related receptor α1 up-regulates endothelial nitric oxide synthase expression. Proc. Natl. Acad. Sci. USA, 2003, 100(24), 14451-14456.
[http://dx.doi.org/10.1073/pnas.2235590100] [PMID: 14610283]
[56]
Shen, H.H.; Yang, C.Y.; Kung, C.W.; Chen, S.Y.; Wu, H.M.; Cheng, P.Y.; Lam, K.K.; Lee, Y.M. Raloxifene inhibits adipose tissue inflammation and adipogenesis through Wnt regulation in ovariectomized rats and 3 T3-L1 cells. J. Biomed. Sci., 2019, 26(1), 62-62.
[http://dx.doi.org/10.1186/s12929-019-0556-3] [PMID: 31470850]
[57]
do Valle Gomes-Gatto, C.; Duarte, F.O.; Stotzer, U.S.; Rodrigues, M.F.C.; de Andrade Perez, S.E.; Selistre-de-Araujo, H.S. Estrogen deficiency in ovariectomized rats: Can resistance training re-establish angiogenesis in visceral adipose tissue? Clinics, 2016, 71(9), 528-536.
[http://dx.doi.org/10.6061/clinics/2016(09)08] [PMID: 27652835]
[58]
Bové, M.; Monto, F.; Guillem-Llobat, P.; Ivorra, M.D.; Noguera, M.A.; Zambrano, A.; Sirerol-Piquer, M.S.; Requena, A.C.; García-Alonso, M.; Tejerina, T.; Real, J.T.; Fariñas, I.; D’Ocon, P. NT3/TrkC pathway modulates the expression of UCP-1 and adipocyte size in human and rodent adipose tissue. Front. Endocrinol., 2021, 12, 630097.
[http://dx.doi.org/10.3389/fendo.2021.630097] [PMID: 33815288]
[59]
Chen, Y.J.; Lin, C.W.; Peng, Y.J.; Huang, C.W.; Chien, Y.S.; Huang, T.H.; Liao, P.X.; Yang, W.Y.; Wang, M.H.; Mersmann, H.J.; Wu, S.C.; Chuang, T.Y.; Lin, Y.Y.; Kuo, W.H.; Ding, S.T. Overexpression of adiponectin receptor 1 inhibits brown and beige adipose tissue activity in mice. Int. J. Mol. Sci., 2021, 22(2), 906.
[http://dx.doi.org/10.3390/ijms22020906] [PMID: 33477525]
[60]
Chou, T.J.; Lu, C.W.; Liao, C.C.; Chiang, C.H.; Huang, C.C.; Huang, K.C. Ovariectomy interferes with proteomes of brown adipose tissue in rats. Int. J. Med. Sci., 2022, 19(3), 499-510.
[http://dx.doi.org/10.7150/ijms.66996] [PMID: 35370469]
[61]
Pedersen, S.B.; Bruun, J.M.; Kristensen, K.; Richelsen, B. Regulation of UCP1, UCP2, and UCP3 mRNA expression in brown adipose tissue, white adipose tissue, and skeletal muscle in rats by estrogen. Biochem. Biophys. Res. Commun., 2001, 288(1), 191-197.
[http://dx.doi.org/10.1006/bbrc.2001.5763] [PMID: 11594772]
[62]
Kaikaew, K.; Grefhorst, A.; Visser, J.A. Sex differences in brown adipose tissue function: Sex hormones, glucocorticoids, and their crosstalk. Front. Endocrinol., 2021, 12(1), 652444.
[http://dx.doi.org/10.3389/fendo.2021.652444] [PMID: 33927694]
[63]
Fletcher, L.A.; Kim, K.; Leitner, B.P.; Cassimatis, T.M.; O’Mara, A.E.; Johnson, J.W.; Halprin, M.S.; McGehee, S.M.; Brychta, R.J.; Cypess, A.M.; Chen, K.Y. Sexual dimorphisms in adult human brown adipose tissue. Obesity, 2020, 28(2), 241-246.
[http://dx.doi.org/10.1002/oby.22698] [PMID: 31970907]
[64]
Yoshioka, K.; Yoshida, T.; Wakabayashi, Y.; Nishioka, H.; Kondo, M. Reduced brown adipose tissue thermogenesis of obese rats after ovariectomy. Endocrinol. Jpn., 1988, 35(4), 537-543.
[http://dx.doi.org/10.1507/endocrj1954.35.537] [PMID: 2850906]
[65]
Zhou, Z.; Moore, T.M.; Drew, B.G.; Ribas, V.; Wanagat, J.; Civelek, M.; Segawa, M.; Wolf, D.M.; Norheim, F.; Seldin, M.M.; Strumwasser, A.R.; Whitney, K.A.; Lester, E.; Reddish, B.R.; Vergnes, L.; Reue, K.; Rajbhandari, P.; Tontonoz, P.; Lee, J.; Mahata, S.K.; Hewitt, S.C.; Shirihai, O.; Gastonbury, C.; Small, K.S.; Laakso, M.; Jensen, J.; Lee, S.; Drevon, C.A.; Korach, K.S.; Lusis, A.J.; Hevener, A.L. Estrogen receptor α controls metabolism in white and brown adipocytes by regulating Polg1 and mitochondrial remodeling. Sci. Transl. Med., 2020, 12(555), eaax8096.
[http://dx.doi.org/10.1126/scitranslmed.aax8096] [PMID: 32759275]
[66]
Martínez de Morentin, P.B.; González-García, I.; Martins, L.; Lage, R.; Fernández-Mallo, D.; Martínez-Sánchez, N.; Ruíz-Pino, F.; Liu, J.; Morgan, D.A.; Pinilla, L.; Gallego, R.; Saha, A.K.; Kalsbeek, A.; Fliers, E.; Bisschop, P.H.; Diéguez, C.; Nogueiras, R.; Rahmouni, K.; Tena-Sempere, M.; López, M. Estradiol regulates brown adipose tissue thermogenesis via hypothalamic AMPK. Cell Metab., 2014, 20(1), 41-53.
[http://dx.doi.org/10.1016/j.cmet.2014.03.031] [PMID: 24856932]
[67]
Ohtake, K.; Ehara, N.; Chiba, H.; Nakano, G.; Sonoda, K.; Ito, J.; Uchida, H.; Kobayashi, J. Dietary nitrite reverses features of postmenopausal metabolic syndrome induced by high-fat diet and ovariectomy in mice. Am. J. Physiol. Endocrinol. Metab., 2017, 312(4), E300-E308.
[http://dx.doi.org/10.1152/ajpendo.00360.2016] [PMID: 28196859]
[68]
Liu, X.; Zhang, Z.; Song, Y.; Xie, H.; Dong, M. An update on brown adipose tissue and obesity intervention: Function, regulation and therapeutic implications. Front. Endocrinol., 2023, 13, 1065263.
[http://dx.doi.org/10.3389/fendo.2022.1065263] [PMID: 36714578]
[69]
Veselik, D.J.; Divekar, S.; Dakshanamurthy, S.; Storchan, G.B.; Turner, J.M.A.; Graham, K.L.; Huang, L.; Stoica, A.; Martin, M.B. Activation of estrogen receptor-alpha by the anion nitrite. Cancer Res., 2008, 68(10), 3950-3958.
[http://dx.doi.org/10.1158/0008-5472.CAN-07-2783] [PMID: 18483281]
[70]
Reagan-Shaw, S.; Nihal, M.; Ahmad, N. Dose translation from animal to human studies revisited. FASEB J., 2008, 22(3), 659-661.
[http://dx.doi.org/10.1096/fj.07-9574LSF] [PMID: 17942826]
[71]
Salehzadeh, H.; Maleki, A.; Rezaee, R.; Shahmoradi, B.; Ponnet, K. The nitrate content of fresh and cooked vegetables and their health-related risks. PLoS One, 2020, 15(1), e0227551.
[http://dx.doi.org/10.1371/journal.pone.0227551] [PMID: 31917821]
[72]
Babateen, A.M.; Fornelli, G.; Donini, L.M.; Mathers, J.C.; Siervo, M. Assessment of dietary nitrate intake in humans: A systematic review. Am. J. Clin. Nutr., 2018, 108(4), 878-888.
[http://dx.doi.org/10.1093/ajcn/nqy108] [PMID: 30321271]
[73]
Lundberg, J.O.; Carlström, M.; Weitzberg, E. Metabolic effects of dietary nitrate in health and disease. Cell Metab., 2018, 28(1), 9-22.
[http://dx.doi.org/10.1016/j.cmet.2018.06.007] [PMID: 29972800]
[74]
Bryan, N.S.; Ivy, J.L. Inorganic nitrite and nitrate: Evidence to support consideration as dietary nutrients. Nutr. Res., 2015, 35(8), 643-654.
[http://dx.doi.org/10.1016/j.nutres.2015.06.001] [PMID: 26189149]
[75]
Capó, X.; Ferrer, M.D.; Olek, R.A.; Salaberry, E.; Suau, R.; Marí, B.; Llompart, I.; Tur, J.A.; Sureda, A.; Pons, A. Oral administration of sodium nitrate to metabolic syndrome patients attenuates mild inflammatory and oxidative responses to acute exercise. Antioxidants, 2020, 9(7), 596.
[http://dx.doi.org/10.3390/antiox9070596] [PMID: 32646062]
[76]
Bahadoran, Z.; Mirmiran, P.; Kashfi, K.; Ghasemi, A. Lost-in-translation of metabolic effects of inorganic nitrate in Type 2 Diabetes: Is ascorbic acid the answer? Int. J. Mol. Sci., 2021, 22(9), 4735.
[http://dx.doi.org/10.3390/ijms22094735] [PMID: 33947005]

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