Fisheries and Aquatic Sciences

The Korean Society of Fisheries and Aquatic Science (한국수산과학회)
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Preventive effects of sea cucumber (Apostichopus japonicus) ethanol extract on palmitate-induced vascular injury in vivo

  • Zhang, Chunying (Department of Marine Bio and Medical Sciences, Hanseo University) ;
  • Cha, Seon-Heui (Department of Marine Bio and Medical Sciences, Hanseo University)
  • Received : 2022.01.13
  • Accepted : 2022.01.31
  • Published : 2022.02.28
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Abstract

Cardiovascular diseases (CVDs) have posed serious public health problems, accounting for nearly 30% of mortality worldwide and their incidence is still increasing. Therefore, new treatment resources are necessary to prevent or manage the ever-increasing population of patients with CVDs. Sea cucumber is well known for its medical and health benefit effects, but it is not well known what/how effect it has on vascular disease. In the present study, we examined the protect effect of sea cucumber, Apostichopus japonicus 80% ethanol extract (AJE) on zebrafish embryo with the stimulation of free fatty acid, palmitate (PA). In vivo study showed that AJE can attenuate PA-induced toxicity through relieving the rapid heartbeat, increasing the survival rate and reducing the malformation in both wild type and Tg (fli1a:eGFP) transgenic zebrafish lines. Additionally, compare with PA treated embryos, the yolk sac area, body length, axial vascular segment (AVS) and intersegmental vessel (ISV) of the co-treatment group of AJE and PA were comparable to the control group. Moreover, AJE lowered the expression of inducible nitric oxide synthase (iNOS), nitric oxide (NO) and inflammation-related genes induced by PA, and inhibited PA-induced vascular development disorders. Our data preliminarily verify that AJE could be a candidate resource for the prevention or therapy of CVDs.

Keywords

Acknowledgement

This research supported by research supporting program of the Hanseo University in 2021.

References

  1. Aires RD, Capettini LSA, Silva JF, Rodrigues-Machado MG, Pinho V, Teixeira MM, et al. Paraquat poisoning induces TNF-α-dependent iNOS/NO mediated hyporesponsiveness of the aorta to vasoconstrictors in rats. PLOS ONE. 2013;8:e73562. https://doi.org/10.1371/journal.pone.0073562
  2. Besedina A. NO-synthase activity in patients with coronary heart disease associated with hypertension of different age groups. J Med Biochem. 2016;35:43-9. https://doi.org/10.1515/jomb-2015-0008
  3. Carter AM. Complement activation: an emerging player in the pathogenesis of cardiovascular disease. Scientifica. 2012;2012:402783. https://doi.org/10.6064/2012/402783
  4. Chen S, Hu Y, Ye X, Li G, Yu G, Xue C, et al. Sequence determination and anticoagulant and antithrombotic activities of a novel sulfated fucan isolated from the sea cucumber Isostichopus badionotus. Biochim Biophys Acta Gen Subj. 2012;1820:989-1000. https://doi.org/10.1016/j.bbagen.2012.03.002
  5. Csiszar A, Ungvari Z, Edwards JG, Kaminski P, Wolin MS, Koller A, et al. Aging-induced phenotypic changes and oxidative stress impair coronary arteriolar function. Circ Res. 2002;90:1159-66. https://doi.org/10.1161/01.RES.0000020401.61826.EA
  6. D'Oria R, Schipani R, Leonardini A, Natalicchio A, Perrini S, Cignarelli A, et al. The role of oxidative stress in cardiac disease: from physiological response to injury factor. Oxid Med Cell Longev. 2020;2020:5732956.
  7. Ebbesson SOE, Voruganti VS, Higgins PB, Fabsitz RR, Ebbesson LO, Laston S, et al. Fatty acids linked to cardiovascular mortality are associated with risk factors. Int J Circumpolar Health. 2015;74:28055. https://doi.org/10.3402/ijch.v74.28055
  8. Ganta VC, Annex BH. LMO2 (LIM domain only 2) and endothelial cell migration in developmental and postnatal angiogenesis. Arterioscler Thromb Vasc Biol. 2017;37:1806-8. https://doi.org/10.1161/ATVBAHA.117.309953
  9. Giudicessi JR, Ackerman MJ, Camilleri M. Cardiovascular safety of prokinetic agents: a focus on drug-induced arrhythmias. Neurogastroenterol Motil. 2018;30:e13302. https://doi.org/10.1111/nmo.13302
  10. Hossain A, Dave D, Shahidi F. Northern sea cucumber (Cucumaria frondosa): a potential candidate for functional food, nutraceutical, and pharmaceutical sector. Mar Drugs. 2020;18:274. https://doi.org/10.3390/md18050274
  11. Hu S, Wang J, Li Z, Fu J, Wang Y, Xue C. Hpyerglycemic effect of a mixture of sea cucumber and Cordyceps sinensis in streptozotocin-induced diabetic rat. J Ocean Univ China. 2013;13:271-7. https://doi.org/10.1007/s11802-014-2073-z
  12. Kaptoge S, Pennells L, De Bacquer D, Cooney MT, Kavousi M, Stevens G, et al. World Health Organization cardiovascular disease risk charts: revised models to estimate risk in 21 global regions. Lancet Glob Health. 2019;7:E1332-45. https://doi.org/10.1016/S2214-109X(19)30318-3
  13. Kareh M, El Nahas R, Al-Aaraj L, Al-Ghadban S, Naser Al Deen N, Saliba N, et al. Anti-proliferative and anti-inflammatory activities of the sea cucumber Holothuria polii aqueous extract. SAGE Open Med. 2018;6:2050312118809541. https://doi.org/10.1177/2050312118809541
  14. Kim NY, Choi WY, Heo SJ, Kang DH, Lee HY. Anti-skin cancer activities of Apostichopus japonicus extracts from low-temperature ultrasonification process. J Healthc Eng. 2017;2017:6504890.
  15. Lawson ND, Weinstein BM. In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev Biol. 2002;248:307-18. https://doi.org/10.1006/dbio.2002.0711
  16. Lee JL, Sinnathurai P, Buchbinder R, Hill C, Lassere M, March L. Biologics and cardiovascular events in inflammatory arthritis: a prospective national cohort study. Arthritis Res Ther. 2018;20:171. https://doi.org/10.1186/s13075-018-1669-x
  17. Li S, Dang YY, Oi Lam Che G, Kwan YW, Chan SW, Leung GPH, et al. VEGFR tyrosine kinase inhibitor II (VRI) induced vascular insufficiency in zebrafish as a model for studying vascular toxicity and vascular preservation. Toxicol Appl Pharmacol. 2014;280:408-20. https://doi.org/10.1016/j.taap.2014.09.005
  18. Li Y, Luo H, Liu T, Zacksenhaus E, Ben-David Y. The ets transcription factor Fli-1 in development, cancer and disease. Oncogene. 2015;34:2022-31. https://doi.org/10.1038/onc.2014.162
  19. Liu F, Walmsley M, Rodaway A, Patient R. Fli1 acts at the top of the transcriptional network driving blood and endothelial development. Curr Biol. 2008;18:P1234-40.
  20. Liu H, Wang H. Early detection system of vascular disease and its application prospect. BioMed Res Int. 2016;2016:1723485.
  21. Liu HH, Ko WC, Hu ML. Hypolipidemic effect of glycosaminoglycans from the sea cucumber Metriatyla scabra in rats fed a cholesterol-supplemented diet. J Agric Food Chem. 2002;50:3602-6. https://doi.org/10.1021/jf020070k
  22. Liu X, Sun Z, Zhang M, Meng X, Xia X, Yuan W, et al. Antioxidant and antihyperlipidemic activities of polysaccharides from sea cucumber Apostichopus japonicus. Carbohydr Polym. 2012;90:1664-70. https://doi.org/10.1016/j.carbpol.2012.07.047
  23. Mansour MB, Balti R, Yacoubi L, Ollivier V, Chaubet F, Maaroufi RM. Primary structure and anticoagulant activity of fucoidan from the sea cucumber Holothuria polii. Int J Biol Macromol. 2019;121:1145-53. https://doi.org/10.1016/j.ijbiomac.2018.10.129
  24. Matrone G, Meng S, Gu Q, Lv J, Fang L, Chen K, et al. Lmo2 (LIM-domain-only 2) modulates Sphk1 (sphingosine kinase) and promotes endothelial cell migration. Arterioscler Thromb Vasc Biol. 2017;37:1860-8. https://doi.org/10.1161/ATVBAHA.117.309609
  25. McCormack MP, Young LF, Vasudevan S, De Graaf CA, Codrington R, Rabbitts TH, et al. The Lmo2 oncogene initiates leukemia in mice by inducing thymocyte self-renewal. Science. 2010;327:879-83. https://doi.org/10.1126/science.1182378
  26. Meng S, Matrone G, Lv J, Chen K, Wong WT, Cooke JP. LIM domain only 2 regulates endothelial proliferation, angiogenesis, and tissue regeneration. J Am Heart Assoc. 2016;5:e004117. https://doi.org/10.1161/JAHA.116.004117
  27. Miller V, Mente A, Dehghan M, Rangarajan S, Zhang X, Swaminathan S., et al. Fruit, vegetable, and legume intake, and cardiovascular disease and deaths in 18 countries (PURE): a prospective cohort study. Lancet. 2017;390:2037-49. https://doi.org/10.1016/S0140-6736(17)32253-5
  28. Monaco C, Nanchahal J, Taylor P, Feldmann M. Anti-TNF therapy: past, present and future. Int Immunol. 2015;27:55-62. https://doi.org/10.1093/intimm/dxu102
  29. Patan S. Vasculogenesis and angiogenesis as mechanisms of vascular network formation, growth and remodeling. J Neurooncol. 2000;50:1-15. https://doi.org/10.1023/A:1006493130855
  30. Patterson LJ, Gering M, Patient R. Scl is required for dorsal aorta as well as blood formation in zebrafish embryos. Blood. 2005;105:3502-11. https://doi.org/10.1182/blood-2004-09-3547
  31. Santhanam L, Lim HK, Lim HK, Miriel V, Brown T, Patel M., et al. Inducible NO synthase-dependent S-nitrosylation and activation of arginase1 contribute to age-related endothelial dysfunction. Circ Res. 2007;101:692-702. https://doi.org/10.1161/CIRCRESAHA.107.157727
  32. Sarmah S, Marrs JA. Zebrafish as a vertebrate model system to evaluate effects of environmental toxicants on cardiac development and function. Int J Mol Sci. 2016;17:2123. https://doi.org/10.3390/ijms17122123
  33. Seo D, Ginsburg GS, Goldschmidt-Clermont PJ. Gene expression analysis of cardiovascular diseases: novel insights into biology and clinical applications. J Am Coll Cardiol. 2006;48:227-35. https://doi.org/10.1016/j.jacc.2006.02.070
  34. Sinha S, Perdomo G, Brown NF, O'Doherty RM. Fatty acid-induced insulin resistance in L6 myotubes is prevented by inhibition of activation and nuclear localization of nuclear factor kappa B. J Biol Chem. 2004;279:41294-301. https://doi.org/10.1074/jbc.M406514200
  35. Stoclet JC, Muller B, Andriantsitohaina R, Kleschyov A. Overproduction of nitric oxide in pathophysiology of blood vessels. Biochemistry (Mosc). 1998;63:826-32.
  36. Sun HJ, Wu ZY, Nie XW, Bian JS. Role of endothelial dysfunction in cardiovascular diseases: the link between inflammation and hydrogen sulfide. Front Pharmacol. 2020;10:1568. https://doi.org/10.3389/fphar.2019.01568
  37. Tang GY, Meng X, Li Y, Zhao CN, Liu Q, Li HB. Effects of vegetables on cardiovascular diseases and related mechanisms. Nutrients. 2017;9:857. https://doi.org/10.3390/nu9080857
  38. Thome MP, Filippi-Chiela EC, Villodre ES, Migliavaca CB, Onzi GR, Felipe KB, et al. Ratiometric analysis of acridine orange staining in the study of acidic organelles and autophagy. J Cell Sci. 2016;129:4622-32. https://doi.org/10.1242/jcs.195057
  39. Tufail T, Saeed F, Abbas M, Arshad MU, Nadeem MT, Bader ul Ain H, et al. Marine bioactives: potentials to reduce the incidence of cardiovascular disorders. Curr Top Nutraceutical Res. 2018;16.
  40. Umar S, van der Laarse A. Nitric oxide and nitric oxide synthase isoforms in the normal, hypertrophic, and failing heart. Mol Cell Biochem. 2010;333:191-201. https://doi.org/10.1007/s11010-009-0219-x
  41. Volpe CMO, Abreu LFM, Gomes PS, Gonzaga RM, Veloso CA, Nogueira-Machado JA. The production of nitric oxide, IL-6, and TNF-alpha in palmitate-stimulated PBMNCs is enhanced through hyperglycemia in diabetes. Oxid Med Cell Longev. 2014;2014:479587.
  42. Wang Z, Zhang H, Yuan W, Gong W, Tang H, Liu B, et al. Antifungal nortriterpene and triterpene glycosides from the sea cucumber Apostichopus japonicus Selenka. Food Chem. 2012;132:295-300. https://doi.org/10.1016/j.foodchem.2011.10.080
  43. World Health Organization [WHO]. Prevention of cardiovascular disease: guidelines for assessment and management of total cardiovascular risk. Geneva: World Health Organization; 2007.
  44. Yang J, Wang Y, Jiang T, Lv L, Zhang B, Lv Z. Depolymerized glycosaminoglycan and its anticoagulant activities from sea cucumber Apostichopus japonicus. Int J Biol Macromol. 2015a;72:699-705. https://doi.org/10.1016/j.ijbiomac.2014.09.025
  45. Yang J, Wang Y, Jiang T, Lv Z. Novel branch patterns and anticoagulant activity of glycosaminoglycan from sea cucumber Apostichopus japonicus. Int J Biol Macromol. 2015b;72:911-8. https://doi.org/10.1016/j.ijbiomac.2014.10.010
  46. Yuan S, Carter P, Bruzelius M, Vithayathil M, Kar S, Mason AM, et al. Effects of tumour necrosis factor on cardiovascular disease and cancer: a two-sample Mendelian randomization study. eBioMedicine. 2020;59:102956. https://doi.org/10.1016/j.ebiom.2020.102956
  47. Zhang H, Hao J, Sun X, Zhang Y, Wei Q. Circulating pro-angiogenic micro-ribonucleic acid in patients with coronary heart disease. Interact Cardiovasc Thorac Surg. 2018;27:336-42.
  48. Zhang H, Park Y, Wu J, Chen X, Lee S, Yang J, et al. Role of TNF-α in vascular dysfunction. Clin Sci. 2009;116:219-30. https://doi.org/10.1042/CS20080196
  49. Zhang J, Shan Y, Li Y, Luo X, Shi H. Palmitate impairs angiogenesis via suppression of cathepsin activity. Mol Med Rep. 2017;15:3644-50. https://doi.org/10.3892/mmr.2017.6463
  50. Zhi Y, Lu H, Duan Y, Sun W, Guan G, Dong Q, et al. Involvement of the nuclear factor-κB signaling pathway in the regulation of CXC chemokine receptor-4 expression in neuroblastoma cells induced by tumor necrosis factor-α. Int J Mol Med. 2015;35:349-57. https://doi.org/10.3892/ijmm.2014.2032
  51. Zhou DD, Luo M, Shang A, Mao QQ, Li BY, Gan RY, et al. Antioxidant food components for the prevention and treatment of cardiovascular diseases: effects, mechanisms, and clinical studies. Oxid Med Cell Longev. 2021;2021:6627355.
  52. Zhu H, Traver D, Davidson AJ, Dibiase A, Thisse C, Thisse B, et al. Regulation of the lmo2 promoter during hematopoietic and vascular development in zebrafish. Dev Biol. 2005;281:256-69. https://doi.org/10.1016/j.ydbio.2005.01.034
  53. Ziff OJ, Kotecha D. Digoxin: the good and the bad. Trends Cardiovasc Med. 2016;26:585-95. https://doi.org/10.1016/j.tcm.2016.03.011