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Published in: BMC Complementary Medicine and Therapies 1/2019

Open Access 01-12-2019 | Insulins | Research article

Rosmarinic acid improves hypertension and skeletal muscle glucose transport in angiotensin II-treated rats

Authors: Mujalin Prasannarong, Vitoon Saengsirisuwan, Juthamard Surapongchai, Jariya Buniam, Natsasi Chukijrungroat, Yupaporn Rattanavichit

Published in: BMC Complementary Medicine and Therapies | Issue 1/2019

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Abstract

Background

Rosmarinic acid (RA) is a natural pure compound from herbs belonging to the Lamiaceae family, such as rosemary, sage, basil, and mint. The antioxidant, angiotensin-converting enzyme inhibitory, and vasodilatory effects of RA have been revealed. Angiotensin II (ANG II) is a potent agent that generates hypertension and oxidative stress. Hypertension and skeletal muscle insulin resistance are strongly related. The aim of this study was to evaluate the effects of acute and chronic RA treatment on blood pressure and skeletal muscle glucose transport in ANG II-induced hypertensive rats.

Methods

Eight-week-old male Sprague Dawley rats were separated into SHAM and ANG II-infused (250 ng/kg/min) groups. ANG II rats were treated with or without acute or chronic RA at 10, 20, or 40 mg/kg. At the end of the experiment, body weight, liver and heart weights, oral glucose tolerance, skeletal muscle glucose transport activity, and signaling proteins were evaluated.

Results

Both acute and chronic RA treatment decreased systolic, diastolic, and mean arterial blood pressure. Only acute RA at 40 mg/kg resulted in a reduction of fasting plasma glucose levels and an induction of skeletal muscle glucose transport activity. These effects might involve increased ERK activity in skeletal muscle. Meanwhile, chronic RA treatment with 10, 20, and 40 mg/kg prevented ANG II-induced hyperglycemia.

Conclusions

Both acute and chronic RA treatment attenuated ANG II-induced cardiometabolic abnormalities in rats. Therefore, RA would be an alternative strategy for improving skeletal muscle glucose transport and protecting against ANG II-induced hypertension and hyperglycemia.
Literature
1.
go back to reference Li QL, Li BG, Zhang Y, Gao XP, Li CQ, Zhang GL. Three angiotensin-converting enzyme inhibitors from Rabdosia coetsa. Phytomedicine. 2008;15:386–8.CrossRef Li QL, Li BG, Zhang Y, Gao XP, Li CQ, Zhang GL. Three angiotensin-converting enzyme inhibitors from Rabdosia coetsa. Phytomedicine. 2008;15:386–8.CrossRef
2.
go back to reference Karthik D, Viswanathan P, Anuradha CV. Administration of rosmarinic acid reduces cardiopathology and blood pressure through inhibition of p22phox NADPH oxidase in fructose-fed hypertensive rats. J Cardiovasc Pharmacol. 2011;58:514–21.CrossRef Karthik D, Viswanathan P, Anuradha CV. Administration of rosmarinic acid reduces cardiopathology and blood pressure through inhibition of p22phox NADPH oxidase in fructose-fed hypertensive rats. J Cardiovasc Pharmacol. 2011;58:514–21.CrossRef
3.
go back to reference Govindaraj J, Sorimuthu Pillai S. Rosmarinic acid modulates the antioxidant status and protects pancreatic tissues from glucolipotoxicity mediated oxidative stress in high-fat diet: streptozotocin-induced diabetic rats. Mol Cell Biochem. 2015;404:143–59.CrossRef Govindaraj J, Sorimuthu Pillai S. Rosmarinic acid modulates the antioxidant status and protects pancreatic tissues from glucolipotoxicity mediated oxidative stress in high-fat diet: streptozotocin-induced diabetic rats. Mol Cell Biochem. 2015;404:143–59.CrossRef
4.
go back to reference Runtuwene J, Cheng KC, Asakawa A, Amitani H, Amitani M, Morinaga A,et al. Rosmarinic acid ameliorates hyperglycemia and insulin sensitivity in diabetic rats, potentially by modulating the expression of PEPCK and GLUT4. Drug Des Devel Ther. 2016;10:2193–202.CrossRef Runtuwene J, Cheng KC, Asakawa A, Amitani H, Amitani M, Morinaga A,et al. Rosmarinic acid ameliorates hyperglycemia and insulin sensitivity in diabetic rats, potentially by modulating the expression of PEPCK and GLUT4. Drug Des Devel Ther. 2016;10:2193–202.CrossRef
5.
go back to reference Csibi A, Communi D, Müller N, Bottari SP. Angiotensin II inhibits insulin-stimulated GLUT4 translocation and Akt activation through tyrosine nitration-dependent mechanisms. PLoS One. 2010;5:e10070.CrossRef Csibi A, Communi D, Müller N, Bottari SP. Angiotensin II inhibits insulin-stimulated GLUT4 translocation and Akt activation through tyrosine nitration-dependent mechanisms. PLoS One. 2010;5:e10070.CrossRef
6.
go back to reference Diamond-Stanic MK, Henriksen EJ. Direct inhibition by angiotensin II of insulin-dependent glucose transport activity in mammalian skeletal muscle involves a ROS-dependent mechanism. Arch Physiol Biochem. 2010;116:88–95.CrossRef Diamond-Stanic MK, Henriksen EJ. Direct inhibition by angiotensin II of insulin-dependent glucose transport activity in mammalian skeletal muscle involves a ROS-dependent mechanism. Arch Physiol Biochem. 2010;116:88–95.CrossRef
7.
go back to reference Prasannarong M, Santos FR, Henriksen EJ. ANG-(1-7) reduces ANG II-induced insulin resistance by enhancing Akt phosphorylation via a mas receptor-dependent mechanism in rat skeletal muscle. Biochem Biophys Res Commun. 2012;426:369–73.CrossRef Prasannarong M, Santos FR, Henriksen EJ. ANG-(1-7) reduces ANG II-induced insulin resistance by enhancing Akt phosphorylation via a mas receptor-dependent mechanism in rat skeletal muscle. Biochem Biophys Res Commun. 2012;426:369–73.CrossRef
8.
go back to reference Kim DS, Kim HR, Woo ER, Hong ST, Chae HJ, Chae SW. Inhibitory effects of rosmarinic acid on adriamycin-induced apoptosis in H9c2 cardiac muscle cells by inhibiting reactive oxygen species and the activations of c-Jun N-terminal kinase and extracellular signal-regulated kinase. Biochem Pharmacol. 2005;70:1066–78.CrossRef Kim DS, Kim HR, Woo ER, Hong ST, Chae HJ, Chae SW. Inhibitory effects of rosmarinic acid on adriamycin-induced apoptosis in H9c2 cardiac muscle cells by inhibiting reactive oxygen species and the activations of c-Jun N-terminal kinase and extracellular signal-regulated kinase. Biochem Pharmacol. 2005;70:1066–78.CrossRef
9.
go back to reference Nie H, Peng Z, Lao N, Wang H, Chen Y, Fang Z, et al. Rosmarinic acid ameliorates PTSD-like symptoms in a rat model and promotes cell proliferation in the hippocampus. Prog Neuro-Psychopharmacol Biol Psychiatry. 2014;51:16–22.CrossRef Nie H, Peng Z, Lao N, Wang H, Chen Y, Fang Z, et al. Rosmarinic acid ameliorates PTSD-like symptoms in a rat model and promotes cell proliferation in the hippocampus. Prog Neuro-Psychopharmacol Biol Psychiatry. 2014;51:16–22.CrossRef
10.
go back to reference Chen HC, Bandyopadhyay G, Sajan MP, Kanoh Y, Standaert M, Farese RV Jr, et al. Activation of the ERK pathway and atypical protein kinase C isoforms in exercise- and aminoimidazole-4-carboxamide-1-beta-D-riboside (AICAR)-stimulated glucose transport. J Biol Chem. 2002;277:23554–62.CrossRef Chen HC, Bandyopadhyay G, Sajan MP, Kanoh Y, Standaert M, Farese RV Jr, et al. Activation of the ERK pathway and atypical protein kinase C isoforms in exercise- and aminoimidazole-4-carboxamide-1-beta-D-riboside (AICAR)-stimulated glucose transport. J Biol Chem. 2002;277:23554–62.CrossRef
11.
go back to reference Konishi Y, Hitomi Y, Yoshida M, Yoshioka E. Pharmacokinetic study of caffeic and rosmarinic acids in rats after oral administration. J Agric Food Chem. 2005;53:4740–6.CrossRef Konishi Y, Hitomi Y, Yoshida M, Yoshioka E. Pharmacokinetic study of caffeic and rosmarinic acids in rats after oral administration. J Agric Food Chem. 2005;53:4740–6.CrossRef
12.
go back to reference Ritschel WA, Starzacher A, Sabouni A, Hussain AS, Koch HP. Percutaneous absorption of rosmarinic acid in the rat. Methods Find Exp Clin Pharmacol. 1989;11:345–52.PubMed Ritschel WA, Starzacher A, Sabouni A, Hussain AS, Koch HP. Percutaneous absorption of rosmarinic acid in the rat. Methods Find Exp Clin Pharmacol. 1989;11:345–52.PubMed
13.
go back to reference Prasannarong M, Saengsirisuwan V, Piyachaturawat P, Suksamrarn A. Improvements of insulin resistance in ovariectomized rats by a novel phytoestrogen from Curcuma comosa Roxb. BMC Complement Altern Med. 2012;12:28.CrossRef Prasannarong M, Saengsirisuwan V, Piyachaturawat P, Suksamrarn A. Improvements of insulin resistance in ovariectomized rats by a novel phytoestrogen from Curcuma comosa Roxb. BMC Complement Altern Med. 2012;12:28.CrossRef
14.
go back to reference Saengsirisuwan V, Pongseeda S, Prasannarong M, Vichaiwong K, Toskulkao C. Modulation of insulin resistance in ovariectomized rats by endurance exercise training and estrogen replacement. Metabolism. 2009;58:38–47.CrossRef Saengsirisuwan V, Pongseeda S, Prasannarong M, Vichaiwong K, Toskulkao C. Modulation of insulin resistance in ovariectomized rats by endurance exercise training and estrogen replacement. Metabolism. 2009;58:38–47.CrossRef
15.
go back to reference Henriksen EJ, Halseth AE. Early alterations in soleus GLUT-4, glucose transport, and glycogen in voluntary running rats. J Appl Physiol. 1994;76:1862–7.CrossRef Henriksen EJ, Halseth AE. Early alterations in soleus GLUT-4, glucose transport, and glycogen in voluntary running rats. J Appl Physiol. 1994;76:1862–7.CrossRef
16.
go back to reference Ferreira LG, Evora PRB, Capellini VK, Albuquerque AA, Carvalho MTM, Gomes RADS, et al. Effect of rosmarinic acid on the arterial blood pressure in normotensive and hypertensive rats: role of ACE. Phytomedicine. 2018;38:158–65.CrossRef Ferreira LG, Evora PRB, Capellini VK, Albuquerque AA, Carvalho MTM, Gomes RADS, et al. Effect of rosmarinic acid on the arterial blood pressure in normotensive and hypertensive rats: role of ACE. Phytomedicine. 2018;38:158–65.CrossRef
17.
go back to reference Liu Q, Tian J, Xu Y, Li C, Meng X, Fu F. Protective effect of RA on myocardial infarction-induced cardiac fibrosis via AT1R/p38 MAPK pathway signaling and modulation of the ACE2/ACE ratio. J Agric Food Chem. 2016;64(35):6716–22.CrossRef Liu Q, Tian J, Xu Y, Li C, Meng X, Fu F. Protective effect of RA on myocardial infarction-induced cardiac fibrosis via AT1R/p38 MAPK pathway signaling and modulation of the ACE2/ACE ratio. J Agric Food Chem. 2016;64(35):6716–22.CrossRef
18.
go back to reference Jayanthy G, Roshana Devi V, Ilango K, Subramanian SP. Rosmarinic acid mediates mitochondrial biogenesis in insulin resistant skeletal muscle through activation of AMPK. J Cell Biochem. 2017;118:1839–48.CrossRef Jayanthy G, Roshana Devi V, Ilango K, Subramanian SP. Rosmarinic acid mediates mitochondrial biogenesis in insulin resistant skeletal muscle through activation of AMPK. J Cell Biochem. 2017;118:1839–48.CrossRef
19.
go back to reference Vlavcheski F, Naimi M, Murphy B, Hudlicky T, Tsiani E. Rosmarinic acid, a rosemary extract polyphenol, increases skeletal muscle cell glucose uptake and activates AMPK. Molecules. 2017;22:E1669.CrossRef Vlavcheski F, Naimi M, Murphy B, Hudlicky T, Tsiani E. Rosmarinic acid, a rosemary extract polyphenol, increases skeletal muscle cell glucose uptake and activates AMPK. Molecules. 2017;22:E1669.CrossRef
20.
go back to reference Lee J, Kim YS, Park D. Rosmarinic acid induces melanogenesis through protein kinase a activation signaling. Biochem Pharmacol. 2007;74:960–8.CrossRef Lee J, Kim YS, Park D. Rosmarinic acid induces melanogenesis through protein kinase a activation signaling. Biochem Pharmacol. 2007;74:960–8.CrossRef
21.
go back to reference Sajan MP, Bandyopadhyay G, Miura A, Standaert ML, Nimal S, Longnus SL, et al. AICAR and metformin, but not exercise, increase muscle glucose transport through AMPK-, ERK-, and PDK1-dependent activation of atypical PKC. Am J Physiol Endocrinol Metab. 2010;298:E179–92.CrossRef Sajan MP, Bandyopadhyay G, Miura A, Standaert ML, Nimal S, Longnus SL, et al. AICAR and metformin, but not exercise, increase muscle glucose transport through AMPK-, ERK-, and PDK1-dependent activation of atypical PKC. Am J Physiol Endocrinol Metab. 2010;298:E179–92.CrossRef
22.
go back to reference Skipworth JR, Szabadkai G, Olde Damink SW, Leung PS, Humphries SE, Montgomery HE. Review article: pancreatic renin-angiotensin systems in health and disease. Aliment Pharmacol Ther. 2011;34:840–52.CrossRef Skipworth JR, Szabadkai G, Olde Damink SW, Leung PS, Humphries SE, Montgomery HE. Review article: pancreatic renin-angiotensin systems in health and disease. Aliment Pharmacol Ther. 2011;34:840–52.CrossRef
23.
go back to reference Mushtaq N, Schmatz R, Ahmed M, Pereira LB, da Costa P, Reichert KP, et al. Protective effect of rosmarinic acid against oxidative stress biomarkers in liver and kidney of strepotozotocin-induced diabetic rats. J Physiol Biochem. 2015;71:743–51.CrossRef Mushtaq N, Schmatz R, Ahmed M, Pereira LB, da Costa P, Reichert KP, et al. Protective effect of rosmarinic acid against oxidative stress biomarkers in liver and kidney of strepotozotocin-induced diabetic rats. J Physiol Biochem. 2015;71:743–51.CrossRef
24.
go back to reference Noguchi-Shinohara M, Ono K, Hamaguchi T, Iwasa K, Nagai T, Kobayashi S, et al. Pharmacokinetics, safety and tolerability of Melissa officinalis extract which contained rosmarinic acid in healthy individuals: a randomized controlled trial. PLoS One. 2015;10:e0126422.CrossRef Noguchi-Shinohara M, Ono K, Hamaguchi T, Iwasa K, Nagai T, Kobayashi S, et al. Pharmacokinetics, safety and tolerability of Melissa officinalis extract which contained rosmarinic acid in healthy individuals: a randomized controlled trial. PLoS One. 2015;10:e0126422.CrossRef
Metadata
Title
Rosmarinic acid improves hypertension and skeletal muscle glucose transport in angiotensin II-treated rats
Authors
Mujalin Prasannarong
Vitoon Saengsirisuwan
Juthamard Surapongchai
Jariya Buniam
Natsasi Chukijrungroat
Yupaporn Rattanavichit
Publication date
01-12-2019
Publisher
BioMed Central
Published in
BMC Complementary Medicine and Therapies / Issue 1/2019
Electronic ISSN: 2662-7671
DOI
https://doi.org/10.1186/s12906-019-2579-4

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