Acute effect of high-intensity interval training exercise on redox status in the ovaries of rats fed a high-fat diet
Rodrigo L. Furtado A , Jonathan Elias R. Martins B , Maria Alice F. Oliveira C , Denise D. Guerreiro D , Naiza A. R. de Sá D , Alex S. M. Ferraz B , Vânia M. Ceccatto E , Ana Paula R. Rodrigues D and Valdevane R. Araújo
A C F
+ Author Affiliations
- Author Affiliations
A Graduate Program in Physiological Sciences, Higher Institute of Biomedical Sciences, State University of Ceará, Fortaleza, CE, 60714-903, Brazil.
B Institute of Physical Education and Sports, Federal University of Ceará, Fortaleza, CE, 60455760, Brazil.
C Microscopy Laboratory of Health Sciences Center, State University of Ceará, Fortaleza, CE, 60714-903, Brazil.
D Laboratory of Manipulation of Oocytes and Preantral Follicles, Veterinary Faculty, State University of Ceará, Fortaleza, CE, 60714-903, Brazil.
E Laboratory of Biochemistry and Gene Expression, Higher Institute of Biomedical Sciences, State University of Ceará, Fortaleza, CE, 60714-903, Brazil.
F Corresponding author. Email: valdevane.araujo@gmail.com
Reproduction, Fertility and Development 33(12) 713-724 https://doi.org/10.1071/RD20326
Submitted: 12 December 2020 Accepted: 5 May 2021 Published: 27 August 2021
Abstract
This study demonstrates the effect of a single high-intensity interval training (HIIT) session on the redox status of rat ovaries with excess adiposity. Forty Wistar female rats (mean (±s.e.m.) weight 94.40 ± 13.40 g) were divided into two groups and fed either a standard diet (SD) or a high-fat diet (HFD) for 62 days. At the end of this period, the rats were subjected to a single HIIT session and were killed 24 h after exercise. Both groups subjected to exercise (SDex and HFDex) generated a significantly higher antioxidant environment by presenting a higher thiol content, which represents a lower oxidation rate of GSH than their respective controls (SD and HFD). The percentage of morphologically normal primary follicles decreased, whereas that of antral follicles increased, in the SDex group. In addition, the HFD group had a higher percentage of degenerated antral follicles than the SD and SDex groups. Cells immunoreactive for α-smooth muscle actin were seen in the cortical stroma and thecal layer enclosing late secondary and tertiary follicles in all groups. Moreover, heme oxygenase and cytochrome P450 family 19 subfamily A member 1 (Cyp19A1) labelling was seen in all antral follicles. Progesterone concentrations were significantly higher in the HFDex than SDex group. In conclusion, this study indicates that a single session of HIIT may result in an improvement in ovary redox status because of metabolic muscle activity by inducing physiological adaptation after exercise in a paracrine manner.
Keywords: adipose tissue, antral follicle, ovary, oxidative stress.
References
Aebi, H. (1984). Catalase in vitro. Methods Enzymol. 105, 121–126.| Catalase in vitro.Crossref | GoogleScholarGoogle Scholar | 6727660PubMed |
Agarwal, A., Gupta, S., and Sharma, R. (2005). Oxidative stress and its implications in female infertility–a clinician’s perspective. Reprod. Biomed. Online 11, 641–650.
| Oxidative stress and its implications in female infertility–a clinician’s perspective.Crossref | GoogleScholarGoogle Scholar | 16409717PubMed |
Al-Eisa, E., Gabr, S. A., and Alghadir, A. H. (2017). Effects of supervised aerobic training on the levels of anti-Mullerian hormone and adiposity measures in women with normo-ovulatory and polycystic ovary syndrome. J. Pak. Med. Assoc. 67, 499–507.
| 28420905PubMed |
Araújo, V. R., Silva, C. M. G., Magalhães, D. M., Silva, G. M., Báo, S. N., Silva, J. R. V., Figueiredo, J. R., and Rodrigues, A. P. R. (2010). Effect of Bone Morphogenetic Protein-7 (BMP-7) on in vitro survival of caprine preantral follicles. Pesq. Vet. Bras. 30, 305.
| Effect of Bone Morphogenetic Protein-7 (BMP-7) on in vitro survival of caprine preantral follicles.Crossref | GoogleScholarGoogle Scholar |
Araújo, V. R., Gastal, M. O., Figueiredo, J. R., and Gastal, E. L. (2014). In vitro culture of bovine preantral follicles: a review. Reprod. Biol. Endocrinol. 12, 78.
| In vitro culture of bovine preantral follicles: a review.Crossref | GoogleScholarGoogle Scholar | 25117631PubMed |
Banerjee, A. K., Mandal, A., Chanda, D., and Chakraborti, S. (2003). Oxidant, antioxidant and physical exercise. Mol. Cell. Biochem. 253, 307–312.
| Oxidant, antioxidant and physical exercise.Crossref | GoogleScholarGoogle Scholar | 14619981PubMed |
Bannister, J. V., and Calabrese, L. (1987). Assays for superoxide dismutase. Methods Biochem. Anal. 32, 279–312.
| Assays for superoxide dismutase.Crossref | GoogleScholarGoogle Scholar | 3033431PubMed |
Barbieri, R. L. (2001). The initial fertility consultation: recommendations concerning cigarette smoking, body mass index, and alcohol and caffeine consumption. Am. J. Obstet. Gynecol. 185, 1168–1173.
| The initial fertility consultation: recommendations concerning cigarette smoking, body mass index, and alcohol and caffeine consumption.Crossref | GoogleScholarGoogle Scholar | 11717652PubMed |
Barlow, J. P., and Solomon, T. P. (2018). Do skeletal muscle-secreted factors influence the function of pancreatic beta-cells? Am. J. Physiol. Endocrinol. Metab. 314, E297–E307.
| Do skeletal muscle-secreted factors influence the function of pancreatic beta-cells?Crossref | GoogleScholarGoogle Scholar | 29208613PubMed |
Bartness, T. J., Polk, D. R., McGriff, W. R., Youngstrom, T. G., and DiGirolamo, M. (1992). Reversal of high-fat diet-induced obesity in female rats. Am. J. Physiol. 263, R790–R797.
| Reversal of high-fat diet-induced obesity in female rats.Crossref | GoogleScholarGoogle Scholar | 1415790PubMed |
Berryman, J. W. (2010). Exercise is medicine: a historical perspective. Curr. Sports Med. Rep. 9, 195–201.
| Exercise is medicine: a historical perspective.Crossref | GoogleScholarGoogle Scholar | 20622536PubMed |
Berzosa, C., Cebrián, I., Fuentes-Broto, L., Gómez-Trullén, E., Piedrafita, E., Martínez-Ballarín, E., et al. (2011). Acute exercise increases plasma total antioxidant status and antioxidant enzyme activities in untrained men. J. Biomed. Biotechnol. 2011, 540458.
| Acute exercise increases plasma total antioxidant status and antioxidant enzyme activities in untrained men.Crossref | GoogleScholarGoogle Scholar | 21436993PubMed |
Boozer, C. N., Schoenbach, G. I. S. E. L. A., and Atkinson, R. L. (1995). Dietary fat and adiposity: a dose-response relationship in adult male rats fed isocalorically. Am. J. Physiol. 268, E546–E550.
| Dietary fat and adiposity: a dose-response relationship in adult male rats fed isocalorically.Crossref | GoogleScholarGoogle Scholar | 7733250PubMed |
Boudoures, A. L., Chi, M., Thompson, A., Zhang, W., and Moley, K. H. (2016). The effects of voluntary exercise on oocyte quality in a diet-induced obese murine model. Reproduction 151, 261–270.
| The effects of voluntary exercise on oocyte quality in a diet-induced obese murine model.Crossref | GoogleScholarGoogle Scholar | 26700938PubMed |
Bradford, M. M. (1976). A rapid and sensitive method for thequantitation of microgram quantities of protein using theprinciples of protein dye-binding. Anal. Biochem. 72, 248–254.
| A rapid and sensitive method for thequantitation of microgram quantities of protein using theprinciples of protein dye-binding.Crossref | GoogleScholarGoogle Scholar | 942051PubMed |
Brandão, B. B., Souza, L. M., Trombetta, B. N. O., Pastre, C. M., Papoti, M., and Seraphim, P. M. (2013). Double effort test for evaluation of aerobic capacity of diet-induced obese rats. Rev. Bras. Med. Esporte 19, 214–218.
Calle, E. E., and Kaaks, R. (2004). Overweight, obesity and cancer: epidemiological evidence and proposed mechanisms. Nat. Rev. Cancer 4, 579–591.
| Overweight, obesity and cancer: epidemiological evidence and proposed mechanisms.Crossref | GoogleScholarGoogle Scholar | 15286738PubMed |
Ciarrocca, M., Capozzella, A., Tomei, F., Tomei, G., and Caciari, T. (2013). Exposure to cadmium in male urban and rural workers and effects on FSH, LH and testosterone. Chemosphere 90, 2077–2084.
| Exposure to cadmium in male urban and rural workers and effects on FSH, LH and testosterone.Crossref | GoogleScholarGoogle Scholar | 23290941PubMed |
De Angelis, K., Rodrigues, B., Zanesco, A., et al. (2017). The importance of animal studies in Exercise Science. Motriz: Rev. Educ. Fis. 23, e101625.
| The importance of animal studies in Exercise Science.Crossref | GoogleScholarGoogle Scholar |
Eichner, E. R. (2017). Exercise Is Medicine, But the Dosing Can Be Dicey. Curr. Sports Med. Rep. 16, 59–60.
| Exercise Is Medicine, But the Dosing Can Be Dicey.Crossref | GoogleScholarGoogle Scholar | 28282346PubMed |
Ellman, G. L. (1959). Tissue sulfhydryl groups. Arch. Biochem. Biophys. 82, 70–77.
| Tissue sulfhydryl groups.Crossref | GoogleScholarGoogle Scholar | 13650640PubMed |
Estadella, D., Oyama, L., Dâmaso, A. R., Ribeiro, E. B., and Nascimento, C. M. O. (2004). Effect of palatable hyperlipidic diet on lipid metabolism of sedentary and exercised rats. Nutrition 20, 218–224.
| Effect of palatable hyperlipidic diet on lipid metabolism of sedentary and exercised rats.Crossref | GoogleScholarGoogle Scholar | 14962690PubMed |
Flohé, L., and Günzler, W. A. (1984). Assays of glutathione peroxidase. Methods Enzymol. 105, 114–120.
| Assays of glutathione peroxidase.Crossref | GoogleScholarGoogle Scholar | 6727659PubMed |
Forney, J. P., Milewich, L., Chen, G. T., Garlock, J. L., Schwarz, B. E., Edman, C. D., and Macdonald, P. C. (1981). Aromatization of Androstenedione to Estrone by Human Adipose Tissue in Vitro. Correlation with Adipose Tissue Mass, Age, and Endometrial Neoplasia. J. Clin. Endocrinol. Metab. 53, 192–199.
| Aromatization of Androstenedione to Estrone by Human Adipose Tissue in Vitro. Correlation with Adipose Tissue Mass, Age, and Endometrial Neoplasia.Crossref | GoogleScholarGoogle Scholar | 7240376PubMed |
Foyer, C. H., Lopez‐Delgado, H., Dat, J. F., and Scott, I. M. (1997). Hydrogen peroxide‐and glutathione‐associated mechanisms of acclimatory stress tolerance and signalling. Physiol. Plant. 100, 241–254.
| Hydrogen peroxide‐and glutathione‐associated mechanisms of acclimatory stress tolerance and signalling.Crossref | GoogleScholarGoogle Scholar |
Frühbeis, C., Helmig, S., Tug, S., Simon, P., and Krämer-Albers, E. M. (2015). Physical exercise induces rapid release of small extracellular vesicles into the circulation. J. Extracell. Vesicles 4, 28239.
| Physical exercise induces rapid release of small extracellular vesicles into the circulation.Crossref | GoogleScholarGoogle Scholar | 26142461PubMed |
Fujii, J., Iuchi, Y., and Okada, F. (2005). Fundamental roles of reactive oxygen species and protective mechanisms in the female reproductive system. Reprod. Biol. Endocrinol. 3, 43.
| Fundamental roles of reactive oxygen species and protective mechanisms in the female reproductive system.Crossref | GoogleScholarGoogle Scholar | 16137335PubMed |
Furukawa, S., Fujita, T., Shimabukuro, M., Iwaki, M., Yamada, Y., Nakajima, Y., Nakayama, O., Makishima, M., Matsuda, M., and Shimomura, I. (2004). Increased oxidative stress in obesity and its impact on metabolic syndrome. J. Clin. Invest. 114, 1752–1761.
| Increased oxidative stress in obesity and its impact on metabolic syndrome.Crossref | GoogleScholarGoogle Scholar | 15599400PubMed |
Gomez-Cabrera, M. C., Domenech, E., and Viña, J. (2008). Moderate exercise is an antioxidant: upregulation of antioxidant genes by training. Free Radic. Biol. Med. 44, 126–131.
| Moderate exercise is an antioxidant: upregulation of antioxidant genes by training.Crossref | GoogleScholarGoogle Scholar | 18191748PubMed |
Gorban de Lapertosa, S., Alvariñas, J., Elgart, J. F., Salzberg, S., Gagliardino, J. J., EduGest group (2020). The triad macrosomia, obesity, and hypertriglyceridemia in gestational diabetes. Diabetes Metab. Res. Rev. 36, e3302.
| The triad macrosomia, obesity, and hypertriglyceridemia in gestational diabetes.Crossref | GoogleScholarGoogle Scholar | 32068345PubMed |
Goutianos, G., Tzioura, A., Kyparos, A., Paschalis, V., Margaritelis, N. V., Veskoukis, A. S., et al. (2015). The rat adequately reflects human responses to exercise in blood biochemical profile: a comparative study. Physiol. Rep. 3, e12293.
| The rat adequately reflects human responses to exercise in blood biochemical profile: a comparative study.Crossref | GoogleScholarGoogle Scholar | 25677548PubMed |
Groussard, C., Maillard, F., Vazeille, E., Barnich, N., Sirvent, P., Otero, Y. F., et al. (2019). Tissue-specific oxidative stress modulation by exercise: A comparison between MICT and HIIT in an obese rat model. Oxid. Med. Cell. Longev. 2019, 1965364.
| Tissue-specific oxidative stress modulation by exercise: A comparison between MICT and HIIT in an obese rat model.Crossref | GoogleScholarGoogle Scholar | 31396298PubMed |
Hajizadeh Maleki, B., and Tartibian, B. (2020). High-intensity interval training modulates male factor infertility through anti-inflammatory and antioxidative mechanisms in infertile men: A randomized controlled trial. Cytokine 125, 154861.
| High-intensity interval training modulates male factor infertility through anti-inflammatory and antioxidative mechanisms in infertile men: A randomized controlled trial.Crossref | GoogleScholarGoogle Scholar | 31569012PubMed |
Hakimi, O., and Cameron, L. C. (2017). Effect of exercise on ovulation: a systematic review. Sports Med. 47, 1555–1567.
| Effect of exercise on ovulation: a systematic review.Crossref | GoogleScholarGoogle Scholar | 28035585PubMed |
Handschin, C., Chin, S., Li, P., Liu, F., Maratos-Flier, E., LeBrasseur, N. K., et al. (2007). Skeletal muscle fiber-type switching, exercise intolerance, and myopathy in PGC-1α muscle-specific knock-out animals. J. Biol. Chem. 282, 30014–30021.
| Skeletal muscle fiber-type switching, exercise intolerance, and myopathy in PGC-1α muscle-specific knock-out animals.Crossref | GoogleScholarGoogle Scholar | 17702743PubMed |
He, F., Li, J., Liu, Z., Chuang, C. C., Yang, W., and Zuo, L. (2016). Redox Mechanism of Reactive Oxygen Species in Exercise. Front. Physiol. 7, 486.
| Redox Mechanism of Reactive Oxygen Species in Exercise.Crossref | GoogleScholarGoogle Scholar | 27872595PubMed |
He, Y., Lu, Y., Zhu, Q., Wang, Y., Lindheim, S. R., Qi, J., et al. (2019). Influence of metabolic syndrome on female fertility and in vitro fertilization outcomes in PCOS women. Am. J. Obstet. Gynecol. 221, 138.e1–138.e12.
| Influence of metabolic syndrome on female fertility and in vitro fertilization outcomes in PCOS women.Crossref | GoogleScholarGoogle Scholar |
Henríquez-Olguín, C., Renani, L. B., Arab-Ceschia, L., Raun, S. H., Bhatia, A., Li, Z., et al. (2019). Adaptations to high-intensity interval training in skeletal muscle require NADPH oxidase 2. Redox Biol. 24, 101188.
| Adaptations to high-intensity interval training in skeletal muscle require NADPH oxidase 2.Crossref | GoogleScholarGoogle Scholar | 30959461PubMed |
Hou, Y. J., Zhu, C. C., Duan, X., Liu, H. L., Wang, Q., and Sun, S. C. (2016). Both diet and gene mutation induced obesity affect oocyte quality in mice. Sci. Rep. 6, 18858.
| Both diet and gene mutation induced obesity affect oocyte quality in mice.Crossref | GoogleScholarGoogle Scholar | 26732298PubMed |
Ikemoto, S., Tsunoda, N., Maruyama, K., Itakura, H., and Ezaki, O. (1996). High-fat diet-induced hyperglycemia and obesity in mice: differential effects of dietary oils. Metabolism 45, 1539–1546.
| High-fat diet-induced hyperglycemia and obesity in mice: differential effects of dietary oils.Crossref | GoogleScholarGoogle Scholar | 8969289PubMed |
Lee, T. S., and Chau, L. Y. (2002). Heme oxygenase-1 mediates the anti-inflammatory effect of interleukin-10 in mice. Nat. Med. 8, 240–246.
| Heme oxygenase-1 mediates the anti-inflammatory effect of interleukin-10 in mice.Crossref | GoogleScholarGoogle Scholar | 11875494PubMed |
Luke, B. (2017). Adverse effects of female obesity and interaction with race on reproductive potential. Fertil. Steril. 107, 868–877.
| Adverse effects of female obesity and interaction with race on reproductive potential.Crossref | GoogleScholarGoogle Scholar | 28366413PubMed |
Marcondes, F. K., Bianchi, F. J., and Tanno, A. P. (2002). Determination of the estrous cycle phases of rats: some helpful considerations. Braz. J. Biol. 62, 609–614.
| Determination of the estrous cycle phases of rats: some helpful considerations.Crossref | GoogleScholarGoogle Scholar | 12659010PubMed |
Maslov, L. N., Naryzhnaya, N. V., Boshchenko, A. A., Popov, S. V., Ivanov, V. V., and Oeltgen, P. R. (2018). Is oxidative stress of adipocytes a cause or a consequence of the metabolic syndrome? J. Clin. Transl. Endocrinol. 15, 1–5.
| Is oxidative stress of adipocytes a cause or a consequence of the metabolic syndrome?Crossref | GoogleScholarGoogle Scholar | 30479968PubMed |
Motterlini, R., Foresti, R., Bassi, R., Calabrese, V., Clark, J. E., and Green, C. J. (2000). Endothelial Heme Oxygenase-1 Induction by Hypoxia modulation by inducible nitric-oxide synthase ands-nitrosothiols. J. Biol. Chem. 275, 13613–13620.
| Endothelial Heme Oxygenase-1 Induction by Hypoxia modulation by inducible nitric-oxide synthase ands-nitrosothiols.Crossref | GoogleScholarGoogle Scholar | 10788478PubMed |
Neufer, P. D., Bamman, M. M., Muoio, D. M., Bouchard, C., Cooper, D. M., Goodpaster, B. H., et al. (2015). Understanding the cellular and molecular mechanisms of physical activity-induced health benefits. Cell Metab. 22, 4–11.
| Understanding the cellular and molecular mechanisms of physical activity-induced health benefits.Crossref | GoogleScholarGoogle Scholar | 26073496PubMed |
Osório Alves, J., Pereira, L. M., Monteiro, I. C. C. R., dos Santos, L. H. P., Ferraz, A. S. M., Loureiro, A. C. C., et al. (2020). Strenuous acute exercise induces slow and fast twitch-dependent NADPH oxidase expression in rat skeletal muscle. Antioxidants 9, 57.
| Strenuous acute exercise induces slow and fast twitch-dependent NADPH oxidase expression in rat skeletal muscle.Crossref | GoogleScholarGoogle Scholar |
Pedersen, B. K. J. (2011). Muscles and their myokines. J. Exp. Biol. 214, 337–346.
| Muscles and their myokines.Crossref | GoogleScholarGoogle Scholar |
Powers, S. K., and Jackson, M. J. (2008). Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production. Physiol. Rev. 88, 1243–1276.
| Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production.Crossref | GoogleScholarGoogle Scholar | 18923182PubMed |
Radak, Z., Zhao, Z., Koltai, E., Ohno, H., and Atalay, M. (2013). Oxygen consumption and usage during physical exercise: the balance between oxidative stress and ROS-dependent adaptive signaling. Antioxid. Redox Signal. 18, 1208–1246.
| Oxygen consumption and usage during physical exercise: the balance between oxidative stress and ROS-dependent adaptive signaling.Crossref | GoogleScholarGoogle Scholar | 22978553PubMed |
Reid, M. B. (2015). Redox interventions to increase exercise performance. J. Physiol. 594, 5125–5133.
| Redox interventions to increase exercise performance.Crossref | GoogleScholarGoogle Scholar | 26584644PubMed |
Ruder, E. H., Hartman, T. J., Blumberg, J., and Goldman, M. B. (2008). Oxidative stress and antioxidants: exposure and impact on female fertility. Hum. Reprod. Update 14, 345–357.
| Oxidative stress and antioxidants: exposure and impact on female fertility.Crossref | GoogleScholarGoogle Scholar | 18535004PubMed |
Samjoo, I. A., Safdar, A., Hamadeh, M. J., Raha, S., and Tarnopolsky, M. A. (2013). The effect of endurance exercise on both skeletal muscle and systemic oxidative stress in previously sedentary obese men. Nutr. Diabetes 3, e88.
| The effect of endurance exercise on both skeletal muscle and systemic oxidative stress in previously sedentary obese men.Crossref | GoogleScholarGoogle Scholar | 24042701PubMed |
Srinivasan, K., Viswanad, B., Asrat, L., Kaul, C. L., and Ramarao, P. (2005). Combination of high-fat diet-fed and low-dose streptozotocin-treated rat: a model for type 2 diabetes and pharmacological screening. Pharmacol. Res. 52, 313–320.
| Combination of high-fat diet-fed and low-dose streptozotocin-treated rat: a model for type 2 diabetes and pharmacological screening.Crossref | GoogleScholarGoogle Scholar | 15979893PubMed |
Strowitzki, T., Halser, B., and Demant, T. (2002). Body fat distribution, insulin sensitivity, ovarian dysfunction and serum lipoproteins in patients with polycystic ovary syndrome. Gynecol. Endocrinol. 16, 45–51.
| Body fat distribution, insulin sensitivity, ovarian dysfunction and serum lipoproteins in patients with polycystic ovary syndrome.Crossref | GoogleScholarGoogle Scholar | 11915581PubMed |
Takahashi, H., Nara, Y., and Tuzimura, K. (1978). Fluorometric Determination of Glutathione by N-(9-Acridinyl)-maleimide and Its Application to Biological Materials. Agric. Biol. Chem. 42, 769–774.
| Fluorometric Determination of Glutathione by N-(9-Acridinyl)-maleimide and Its Application to Biological Materials.Crossref | GoogleScholarGoogle Scholar |
Tanaka, S., Akaike, T., Fang, J., Beppu, T., Ogawa, M., Tamura, F., et al. (2003). Antiapoptotic effect of haem oxygenase-1 induced by nitric oxide in experimental solid tumour. Br. J. Cancer 88, 902–909.
| Antiapoptotic effect of haem oxygenase-1 induced by nitric oxide in experimental solid tumour.Crossref | GoogleScholarGoogle Scholar | 12644828PubMed |
Touati, S., Meziri, F., Devaux, S., Berthelot, A., Touyz, R. M., and Laurant, P. (2011). Exercise reverses metabolic syndrome in high-fat diet-induced obese rats. Med. Sci. Sports Exerc. 43, 398–407.
| Exercise reverses metabolic syndrome in high-fat diet-induced obese rats.Crossref | GoogleScholarGoogle Scholar | 20631645PubMed |
Turner-McGrievy, G. M., and Grant, B. L. (2015). Prevalence of body mass index and body weight cut-off points for in vitro fertilization treatment at US clinics and current clinic weight loss strategy recommendations. Hum. Fertil. (Camb.) 18, 215–219.
| Prevalence of body mass index and body weight cut-off points for in vitro fertilization treatment at US clinics and current clinic weight loss strategy recommendations.Crossref | GoogleScholarGoogle Scholar | 25895556PubMed |
Turturro, A., Witt, W. W., Lewis, S., Hass, B. S., Lipman, R. D., and Hart, R. W. (1999). Growth curves and survival characteristics of the animals used in the Biomarkers of Aging Program. J. Gerontol. A Biol. Sci. Med. Sci. 54, B492–B501.
| Growth curves and survival characteristics of the animals used in the Biomarkers of Aging Program.Crossref | GoogleScholarGoogle Scholar | 10619312PubMed |
Vechetti Jr, I. J., Valentino, T., Mobley, C. B., and McCarthy, J. J. (2021). The role of extracellular vesicles in skeletal muscle and systematic adaption to exercise. J. Physiol. 599, 845–861.
| The role of extracellular vesicles in skeletal muscle and systematic adaption to exercise.Crossref | GoogleScholarGoogle Scholar |
Woodfield, J. C., Baldi, J. C., and Clifford, K. (2019). What is the minimal dose of HIIT required to achieve pre‐operative benefit. Scand. J. Med. Sci. Sports 29, 1841.
| What is the minimal dose of HIIT required to achieve pre‐operative benefit.Crossref | GoogleScholarGoogle Scholar | 31408549PubMed |
Yudkin, J. S., Stehouwer, C., Emeis, J., and Coppack, S. (1999). C-reactive protein in healthy subjects: associations with obesity, insulin resistance, and endothelial dysfunction: a potential role for cytokines originating from adipose tissue? Arterioscler. Thromb. Vasc. Biol. 19, 972–978.
| C-reactive protein in healthy subjects: associations with obesity, insulin resistance, and endothelial dysfunction: a potential role for cytokines originating from adipose tissue?Crossref | GoogleScholarGoogle Scholar | 10195925PubMed |
Zamora, R., Vodovotz, Y., Aulak, K. S., Kim, P. K., Kane, J. M., Alarcon, L., et al. (2002). A DNA microarray study of nitric oxide-induced genes in mouse hepatocytes: implications for hepatic heme oxygenase-1 expression in ischemia/reperfusion. Nitric Oxide 7, 165–186.
| A DNA microarray study of nitric oxide-induced genes in mouse hepatocytes: implications for hepatic heme oxygenase-1 expression in ischemia/reperfusion.Crossref | GoogleScholarGoogle Scholar | 12381414PubMed |
Zheng, X., Price, C. A., Tremblay, Y., Lussier, J. G., and Carriere, P. D. (2008). Role of transforming growth factor-b1 in gene expression and activity of estradiol and progesterone-generating enzymes in FSH-stimulated bovine granulosa cells. Reproduction 136, 447–457.
| Role of transforming growth factor-b1 in gene expression and activity of estradiol and progesterone-generating enzymes in FSH-stimulated bovine granulosa cells.Crossref | GoogleScholarGoogle Scholar | 18635743PubMed |
