ERRATUM: Antioxidant Activity and Cardioprotective Potential of Nanoemulsion Mix of Rosmarinus officinalis and Centella asiatica in Gestational Diabetes Mellitus Zebrafish Larvae Model
Main Article Content
Abstract
Hyperglycemia affects approximately 16.7% of pregnancies worldwide, with gestational diabetes mellitus (GDM) accounting for nearly 84% of these cases. GDM, characterized by glucose intolerance during pregnancy, presents significant health risks. Rosmarinus officinalis (RO) and Centella asiatica (CA) are known for their antidiabetic and antioxidant properties, including the ability to enhance insulin secretion and inhibit phosphoenolpyruvate carboxykinase (PEPCK) expression in the gluconeogenesis pathway. This study aims to assess the impact of a nanoemulsion of RO and CA combination (RO-CA) on heart rate, superoxide dismutase (SOD), nuclear factor erythroid 2-related factor 2a (Nrf2a), sirtuin 1 (SIRT-1), and tyrosine hydroxylase (TH) expression in zebrafish larvae model of GDM. GDM was induced by exposure of zebrafish embryo to a 3% glucose solution in an embryonic medium. The GDM phenotype was confirmed by elevated PEPCK expression as a hyperglycemia marker. GDM zebrafish was administered RO-CA nanoemulsion at concentrations of 2.5, 5, and 10 µg/mL.from 2 hpf to 72 hpf. Heart rate was monitored using stereoscopic imaging connected to a camera, while expression levels of PEPCK, Nrf2a, SOD, SIRT-1, and TH were quantified using reverse transcriptase polymerase chain reaction (RT-PCR). Results revealed a significant decrease in PEPCK expression in the treatment groups compared to the glucose untreated group. Notably, the nanoemulsion maintained heart rate frequency and upregulated Nrf2a, SOD, SIRT-1, and TH expression, particularly at a concentration of 2.5 µg/mL. Overall, these findings suggest that the RO-CA nanoemulsion exhibits enhanced antioxidant activity and holds promise as a potential cardioprotective agent in GDM.
Downloads
Article Details
Section
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
How to Cite
References
Woodside A and Bradford H. Exercise and the Prevention of Gestational Diabetes Mellitus. Nurs Womens Health. 2021; 25:304–311.
American Diabetes Association. Classification and diagnosis of diabetes. Diabetes Care. 2017; 40:S11–24.
International Diabetes Federation. IDF Diabetes Atlas 10th edition 2021. [Online]. 2021 [cited 2022 Dec 11]. Available from: https://diabetesatlas.org/atlas/tenth-edition/
Wang C and Yang H. Diagnosis, prevention and management of gestational diabetes mellitus. Chronic Dis Transl Med. 2016; 2:199–203.
Johns EC, Denison FC, Norman JE, Reynolds RM. Gestational Diabetes Mellitus: Mechanisms, Treatment, and Complications. Trends Endocrinol Metab. 2018; 29:743–754.
de Mendonça ELSS, Fragoso MBT, de Oliveira JM, Xavier JA, Goulart MOF, de Oliveira ACM. Gestational Diabetes Mellitus: The Crosslink among Inflammation, Nitroxidative Stress, Intestinal Microbiota and Alternative Therapies. Antioxid. 2022; 11(1):129.
Tozour J, Hughes F, Carrier A, Vieau D, Delahaye F. Prenatal hyperglycemia exposure and cellular stress, a sugar-coated view of early programming of metabolic diseases. Biomolecules. 2020; 10:1–17.
Topcuoglu S, Karatekin G, Yavuz T, Arman D, Kaya A, Gursoy T, Ovali F. The relationship between the oxidative stress and the cardiac hypertrophy in infants of diabetic mothers. Diabetes Res Clin Pract. 2015; 109:104–109.
Samanth J, Padmakumar R, Vasudeva A, Lewis L, Nayak K, Nayak V. Persistent subclinical myocardial dysfunction among infants of diabetic mothers. J Diabetes Complications. 2022; 36(1):108079.
Wu Y, Liu B, Sun Y, Du Y, Santillan MK, Santillan DA, Snetselaar LG, Bao W. Association of maternal prepregnancy diabetes and gestational diabetes mellitus with congenital anomalies of the newborn. Diabetes Care. 2020; 43:2983–2990.
Al-Biltagi M, El razaky O, El Amrousy D. Cardiac changes in infants of diabetic mothers. World J Diabetes. 2021; 12:1233–1247.
Giribabu N, Karim K, Kilari EK, Nelli SR, Salleh N. Oral administration of Centella asiatica (L.) Urb leave aqueous extract ameliorates cerebral oxidative stress, inflammation, and apoptosis in male rats with type-2 diabetes. Inflammopharm. 2020; 28:1599–1622.
Khotimah H, Alita SNP, Anindhita D, Weningtyas A, Prima WE, Kalsum U, Rahayu M, Handayani D, Nandar SK. Ethanolic extract of Salacca zalacca peel reduce IL-1β and apoptosis in high glucose induced zebrafish embryo. GSC Bio Pharm Sci. 2021; 16:024–33.
Alqudah A, Eastwood KA, Jerotic D, Todd N, Hoch D, McNally R, Obradovic D, Dugalic S, Hunter AJ, Holmes VA, McCance DR, Young IS, Watson CJ, Robson T, Desoye G, Grieve DJ, McClements L. FKBPL and SIRT-1 Are Downregulated by Diabetes in Pregnancy Impacting on Angiogenesis and Endothelial Function. Front Endocrinol (Lausanne). 2021; 12:650328.
D’Onofrio N, Servillo L, Balestrieri ML. SIRT1 and SIRT6 Signaling Pathways in Cardiovascular Disease Protection. Antioxid Redox Signal. 2018; 28:711–732.
Mishra M, Duraisamy AJ, Kowluru RA. Sirt1: A guardian of the development of diabetic retinopathy. Diabetes. 2018; 67:745–754.
Grassam-Rowe A, Ou X, Lei M. Novel cardiac cell subpopulations: Pnmt-derived cardiomyocytes. Open Biol. 2020; 10(8):200095.
Habecker BA, Anderson ME, Birren SJ, Fukuda K, Herring N, Hoover DB, Kanazawa H, Paterson DJ, Ripplinger CM. Molecular and cellular neurocardiology: development, and cellular and molecular adaptations to heart disease. J Physiol. 2016; 594:3853–3875.
Nasri H, Shirzad H, Baradaran A, Rafieian-Kopaei M. Antioxidant plants and diabetes mellitus. J Res Med Sci. 2015; 20(5):491-502.
Whalen K and Taylor J. Gestational Diabetes Mellitus. Endocrinology/Nephrology 2017. 7-26 p.
Alam S, Sarker MMR, Sultana TN, Chowdhury MNR, Rashid MA, Chaity NI, Zhao C, Xiao J, Hafez EE, Khan SA, Mohamed IN. Antidiabetic Phytochemicals From Medicinal Plants: Prospective Candidates for New Drug Discovery and Development. Front Endocrinol (Lausanne). 2022; 13:800714.
Marella S and Tollamadugu NVKVP. Nanotechnological approaches for the development of herbal drugs in treatment of diabetes mellitus – a critical review. IET Nanobiotechnol. 2018; 12:549–556.
Ngo YL, Lau CH, Chua LS. Review on rosmarinic acid extraction, fractionation and its anti-diabetic potential. Food Chem Toxicol. 2018; 121:687–700.
Shiravi A, Akbari A, Mohammadi Z, Khalilian MS, Zeinalian A, Zeinalian M. Rosemary and its protective potencies against COVID-19 and other cytokine storm associated infections: A molecular review. Med J Nutr Metab. 2021; 14:401–416.
Colica C, Renzo L Di, Aiello V, De Lorenzo A, Abenavoli L. Rev Recent Clin. 2018.
Kompelly A, Kompelly S, Vasudha B, Narender B. Rosmarinus officinalis L.: an update review of its phytochemistry and biological activity. J Drug Deliv Ther. 2019; 9:323–330.
Naseema A, Kovooru L, Behera AK, Kumar KPP, Srivastava P. A critical review of synthesis procedures, applications and future potential of nanoemulsions. Adv Colloid Interface Sci. 2021; 287:102318.
Bonifácio BV, Silva PB, Ramos MA, Negri KM, Bauab TM, Chorilli M. Nanotechnology-based drug delivery systems and herbal medicines: a review. Int J Nanomedicine. 2014;9:1-15.
Aslam MS, Ahmad MS, Mamat AS, Ahmad MZ, Salam F. An update review on polyherbal formulation: A global perspective. Sys Rev Pharm. 2016; 7:35–41.
Karole S, Shrivastava S, Thomas S, Soni B, Khan S, Dubey J, Dubey SP, Khan N, Jain DK. Polyherbal Formulation Concept for Synergic Action: A Review. J Drug Deliv Ther. 2019; 9:453–466.
Ainurofiq A, Wiyono N, Warni R, Choiri S. Assessment of the synergistic effect of a poly-herbals combination on the antioxidant activity through a statistical approach. F1000Res. 2022; 11:1327.
Moukette BM, Ama Moor VJ, Biapa Nya CP, Nanfack P, Nzufo FT, Kenfack MA, Ngogang JY, Pieme CA. Antioxidant and Synergistic Antidiabetic Activities of a Three-Plant Preparation Used in Cameroon Folk Medicine. Int Sch Res Notices. 2017; 2017:1–7.
Hardianti M, Yuniarto A, Hasimun P. Review: Zebrafish (Danio rerio) Sebagai Model Obesitas dan Diabetes Melitus Tipe 2. J Sains Farm Klin. 2021; 8:69.
Zakaria F, Ibrahim WN, Ismail IS, Ahmad H, Manshoor N, Ismail N, Zainal Z, Shaari K. LCMS/MS Metabolite Profiling and Analysis of Acute Toxicity Effect of the Ethanolic Extract of Centella asiatica on Zebrafish Model. Pertanika J Sci Technol. 2019; 27:985–1003.
Jeevanandam J, Chan YS, Danquah MK. Zebrafish as a model organism to study nanomaterial toxicity. Emerging Sci J. 2019; 3:195–208.
Khotimah H, Prima WE, Weningtyas A, Aninditha D, Alita SNP, Kalsum U, Nandar SK, Rahayu M, Handayani D. Neuroprotective Activity and Antioxidant Effect of Salacca zalacca Peel Ethanol Extract on High Glucose Induced Zebrafish (Danio rerio) Embryo. Trop J Nat Prod Res. 2022; 5:2079–2084.
Cold Spring Harbor Laboratory. E3 medium (for zebrafish embryos). [Online]. 2011 [cited 2022 Dec 12]. Available from: https://cshprotocols.cshlp.org/content/2011/10/pdb.rec66449
Heckler K and Kroll J. Zebrafish as a model for the study of microvascular complications of diabetes and their mechanisms. Int J Mol Sci. 2017; 18(9):2002.
Van De Venter M, Didloff J, Reddy S, Swanepoel B, Govender S, Dambuza NS, Williams S, Koekemoer TC, Venables L. Wild-type zebrafish (Danio rerio) larvae as a vertebrate model for diabetes and comorbidities: A review. Animals. 2021; 11:1–21.
Konecke N. Addition of glucose solutions to aquatic environment of Danio rerio embryos in concentrations of 4 mM to 14 mM increases heart rate BPM for zebrafish exposed to elevated glucose levels. [Online]. 2011 [cited 2022 Dec 12]. Available from: https://bpb-us-w2.wpmucdn.com/sites.uwm.edu/dist/8/202/files/2018/06/Konecke_paper_zf_2018-zrtrec.pdf
Riffiani R, Chen FC, Zhang W, Wada T, Shimomura N, Yamaguchi T, Aimic T. Identification, characterization and expression of A-mating type genes in monokaryons and dikaryons of the edible mushroom Mycoleptodonoides aitchisonii (Bunaharitake). Mycosci. 2021; 62(2):106–114.
Reifenberger GC, Thomas BA, Rhodes DVL. Comparison of DNA Extraction and Amplification Techniques for Use with Engorged Hard-Bodied Ticks. Microorganism. 2022; 10(6):1254.
Kim I, Seok SH, Lee H-Y. Development of a Zebrafish Larvae Model for Diabetic Heart Failure With Reduced Ejection Fraction. Korean Circ J. 2023; 53:34.
Brearley MC, Daniel ZCTR, Loughna PT, Parr T, Brameld JM. The phosphoenolpyruvate carboxykinase (PEPCK) inhibitor, 3-mercaptopicolinic acid (3- MPA), induces myogenic differentiation in C2C12 cells. Sci Rep. 2020; 10(1):22177.
Runtuwene J, Cheng KC, Asakawa A, Amitani H, Amitani M, Morinaga A, Takimoto Y, Kairupan BHR, Inui A. Rosmarinic acid ameliorates hyperglycemia and insulin sensitivity in diabetic rats, potentially by modulating the expression of PEPCK and GLUT4. Drug Des Dev Ther. 2016; 10:2193–2202.
Alkhalidy H, Moore W, Wang A, Luo J, McMillan RP, Wang Y, Zhen W, Hulver MW, Liu D. Kaempferol ameliorates hyperglycemia through suppressing hepatic gluconeogenesis and enhancing hepatic insulin sensitivity in diet-induced obese mice. J Nutr Biochem. 2018; 58:90–101.
Mioc M, Prodea A, Racoviceanu R, Mioc A, Ghiulai R, Milan A, Voicu M, Mardale G, Soica C. Recent Advances Regarding the Molecular Mechanisms of Triterpenic Acids: A Review (Part II). Int J Mol Sci. 2022; 23(14):7740.
Plows JF, Stanley JL, Baker PN, Reynolds CM, Vickers MH. The pathophysiology of gestational diabetes mellitus. Int J Mol Sci. 2018; 19(11):3342.
Wu J, Sun X, Jiang Z, Jiang J, Xu L, Tian A, Sun X, Meng H, Li Y, Huang W, Jia Y, Wu H. Protective role of NRF2 in macrovascular complications of diabetes. J Cell Mol Med. 2020; 24:8903–8917.
Williams LM, Timme-Laragy AR, Goldstone JV, McArthur AG, Stegeman JJ, Smolowitz RM, Hahn ME. Developmental expression of the Nfe2-related factor (Nrf) transcription factor family in the zebrafish, Danio rerio. PLoS One. 2013; 8(10):e79574.
Sant KE, Sinno PP, Jacobs HM, Timme-Laragy AR. Nrf2a modulates the embryonic antioxidant response to perfluorooctanesulfonic acid (PFOS) in the zebrafish, Danio rerio. Aquat Toxicol. 2018; 198:92–102.
Rosa AC, Corsi D, Cavi N, Bruni N, Dosio F. Superoxide dismutase administration: A review of proposed human uses. Molecules. 2021; 26(7):1844.
Cheng X, Chapple SJ, Patel B, Puszyk W, Sugden D, Yin X, Mayr M, Siow RCM, Mann GE. Gestational diabetes mellitus impairs nrf2-mediated adaptive antioxidant defenses and redox signaling in fetal endothelial cells in utero. Diabetes. 2013; 62:4088–4097.
Sun B, Wu L, Wu Y, Zhang C, Qin L, Hayashi M, Kudo M, Gao M, Liu T. Therapeutic Potential of Centella asiatica and Its Triterpenes: A Review. Front Pharmacol. 2020; 11:568032.
Tebay LE, Robertson H, Durant ST, Vitale SR, Penning TM, Dinkova-Kostova AT, Hayes JD. Mechanisms of activation of the transcription factor Nrf2 by redox stressors, nutrient cues, and energy status and the pathways through which it attenuates degenerative disease. Free Rad Biol Med. 2015; 88:108–146.
Zolkepli H, Widodo RT, Mahmood S, Salim N, Awang K, Ahmad N, Othman R. A Review on the Delivery of Plant-Based Antidiabetic Agents Using Nanocarriers: Current Status and Their Role in Combatting Hyperglycaemia. Polymers (Basel). 2022; 14(15):2991.
Panossian L, Fenik P, Zhu Y, Zhan G, McBurney MW, Veasey S. SIRT1 regulation of wakefulness and senescence-like phenotype in wake neurons. J Neurosci. 2011; 31:4025–4036.
Ianni A, Yuan X, Bober E, Braun T. Sirtuins in the Cardiovascular System: Potential Targets in Pediatric Cardiology. Pediatr Cardiol. 2018; 39:983–992.
Bakovic M, Filipovic N, Ferhatovic Hamzic L, Kunac N, Zdrilic E, Vitlov Uljevic M, Kostic S, Puljak L, Vukojevic K. Changes in neurofilament 200 and tyrosine hydroxylase expression in the cardiac innervation of diabetic rats during aging. Cardiovasc Pathol. 2018; 32:38–43.
Grisanti LA. Diabetes and Arrhythmias: Pathophysiology, Mechanisms and Therapeutic Outcomes. Front Physiol. 2018; 9:1669.
Rahbardar MG and Hosseinzadeh H. Therapeutic effects of rosemary (Rosmarinus officinalis L.) and its active constituents on nervous system disorders. Iran J Basic Med Sci. 2020; 23:1100–1112.
Sun B, Hayashi M, Kudo M, Wu L, Qin L, Gao M, Liu T. Madecassoside Inhibits Body Weight Gain via Modulating SIRT1-AMPK Signaling Pathway and Activating Genes Related to Thermogenesis. Front Endocrinol (Lausanne). 2021; 12:627950.
Gopi M, Arambakkam Janardhanam V. Asiaticoside: Attenuation of rotenone induced oxidative burden in a rat model of hemiparkinsonism by maintaining the phosphoinositide-mediated synaptic integrity. Pharmacol Biochem Behav. 2017; 155:1–15.
Harwansh RK, Deshmukh R, Rahman MA. Nanoemulsion: Promising nanocarrier system for delivery of herbal bioactives. J Drug Deliv Sci Technol. 2019; 51:224–233.