Advertisement

Heart Failure Reviews

, Volume 24, Issue 1, pp 155–166 | Cite as

Lanosteryl triterpenes from Protorhus longifolia as a cardioprotective agent: a mini review

  • Nonhlakanipho F. Sangweni
  • Phiwayinkosi V. Dludla
  • Rebamang A. Mosa
  • Abidemi P. Kappo
  • Andy Opoku
  • Christo J. F. Muller
  • Rabia Johnson
Article
  • 105 Downloads

Abstract

The epidemic of cardiovascular diseases is a global phenomenon that is exaggerated by the growing prevalence of diabetes mellitus. Coronary artery disease and diabetic cardiomyopathy are the major cardiovascular complications responsible for exacerbated myocardial infarction in diabetic individuals. Increasing research has identified hyperglycemia and hyperlipidemia as key factors driving the augmentation of oxidative stress and a pro-inflammatory response that usually results in increased fibrosis and reduced cardiac efficiency. While current antidiabetic agents remain active in attenuating diabetes-associated complications, overtime, their efficacy proves limited in protecting the hearts of diabetic individuals. This has led to a considerable increase in the number of natural products that are screened for their antidiabetic and cardioprotective properties. These natural products may present essential ameliorative properties relevant to their use as a monotherapy or as an adjunct to current drug agents in combating diabetes and its associated cardiovascular complications. Recent findings have suggested that triterpenes isolated from Protorhus longifolia (Benrh.) Engl., a plant species endemic to Southern Africa, display strong antioxidant and antidiabetic properties that may potentially protect against diabetes-induced cardiovascular complications. Thus, in addition to discussing the pathophysiology associated with diabetes-induced cardiovascular injury, available evidence pertaining to the cardiovascular protective potential of lanosteryl triterpenes from Protorhus longifolia will be discussed.

Keywords

Cardiovascular diseases Diabetic cardiomyopathy Diabetes Protorhus longifolia Triterpenes 

Notes

Author contributions

NF Sangweni, PV Dludla, and R Johnson equally contributed to the conceptualization, design, and writing of the manuscript. All authors, including NF Sangweni, PV Dludla, RA Mosa, AP Kappo, A Opoku, C Muller, and R Johnson edited and approved the final draft of the manuscript.

Funding information

The authors acknowledge the financial support from the South African Medical Research Council/Biomedical Research and Innovation Platform (baseline funding), and the research reported in this publication was supported by the South African Medical Research Council through funding received from the South African National Treasury under the South African Medical Research Council’s Research Strengthening and Capacity Development Funding Opportunity for Selected Universities Initiative (Grant No. PC 57009). Its contents are solely the responsibility of the authors and do not necessarily represent the official views of the South African Medical Research Council. We would also like to acknowledge the National Research Foundation for the financial support (Thuthuka Grant (UID107261)).

Compliance with ethical standards

The manuscript does not contain clinical studies or patient data.

Conflict of interest

The authors declare that they have no conflicts of interest.

References

  1. 1.
    Baskaran K, Kizar Ahamath B, Radha Shanmugasundaram K, Shanmugasundaram ER (1990) Antidiabetic effect of a leaf extract from Gymnema sylvestre in non-insulin-dependent diabetes mellitus patients. J Ethnopharmacol 30(3):295–300CrossRefGoogle Scholar
  2. 2.
    Manickam M, Ramanathan M, Jahromi MA, Chansouria JP, Ray AB (1997) Antihyperglycemic activity of phenolics from Pterocarpus marsupium. J Nat Prod 60(6):609–610.  https://doi.org/10.1021/np9607013 CrossRefPubMedGoogle Scholar
  3. 3.
    Sheela CG, Augusti KT (1992) Antidiabetic effects of S-allyl cysteine sulphoxide isolated from garlic Allium sativum Linn. Indian J Exp Biol 30(6):523–526PubMedGoogle Scholar
  4. 4.
    Bailey CJ (2017) Metformin: historical overview. Diabetologia 60(9):1566–1576.  https://doi.org/10.1007/s00125-017-4318-z CrossRefPubMedGoogle Scholar
  5. 5.
    Rios JL, Francini F, Schinella GR (2015) Natural products for the treatment of type 2 diabetes mellitus. Planta Med 81(12–13):975–994.  https://doi.org/10.1055/s-0035-1546131 CrossRefPubMedGoogle Scholar
  6. 6.
    Rosiak M, Postula M, Kaplon-Cieslicka A, Trzepla E, Czlonkowski A, Filipiak KJ, Opolski G (2013) Metformin treatment may be associated with decreased levels of NT-proBNP in patients with type 2 diabetes. Adv Med Sci 58(2):362–368.  https://doi.org/10.2478/ams-2013-0009 CrossRefPubMedGoogle Scholar
  7. 7.
    Yin M, van der Horst IC, van Melle JP, Qian C, van Gilst WH, Sillje HH, de Boer RA (2011) Metformin improves cardiac function in a nondiabetic rat model of post-MI heart failure. Am J Phys Heart Circ Phys 301(2):H459–H468.  https://doi.org/10.1152/ajpheart.00054 CrossRefGoogle Scholar
  8. 8.
    Florez H, Pan Q, Ackermann RT, Marrero DG, Barrett-Connor E, Delahanty L, Kriska A, Saudek CD, Goldberg RB, Rubin RR (2012) Impact of lifestyle intervention and metformin on health-related quality of life: the diabetes prevention program randomized trial. J Gen Intern Med 27(12):1594–1601.  https://doi.org/10.1007/s11606-012-2122-5 CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Rojas LBA, Gomes MB (2013) Metformin: an old but still the best treatment for type 2 diabetes. Diabetol Metab Syndr 5:6.  https://doi.org/10.1186/1758-5996-5-6 CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Adeghate E, Kalasz H, Veress G, Tekes K (2010) Medicinal chemistry of drugs used in diabetic cardiomyopathy. Curr Med Chem 17(6):517–551(35).  https://doi.org/10.2174/092986710790416281 CrossRefPubMedGoogle Scholar
  11. 11.
    Khavandi K, Khavandi A, Asghar O, Greenstein A, Withers S, Anthony M, Heagerty AM, Rayaz A, Malik RA (2009) Diabetic cardiomyopathy—a distinct disease? Best Pract Res Clin Endocrinol Metab 23(3):347–360.  https://doi.org/10.1016/j.beem.2008.10.016 CrossRefPubMedGoogle Scholar
  12. 12.
    Statistics South Africa (2018) Prevalence of non-communicable dieases. Available at http://www.statssa.gov.za/publications/11025.pdf, Accessed 26 Mar 2018
  13. 13.
    International Diabetes Federation (2017) International Diabetes Federation diabetes atlas. Eight edition. Accessed 30 Jan 2018Google Scholar
  14. 14.
    Van Wyk BE (2015) A review of commercially important African medicinal plants. J Ethnopharmacol 176:118–134.  https://doi.org/10.1016/j.jep.2015.10.031 CrossRefPubMedGoogle Scholar
  15. 15.
    Marnewick JL, Rautenbach F, Venter I, Neethling H, Blackhurst DM, Wolmarans P, Macharia M (2011) Effects of rooibos (Aspalathus linearis) on oxidative stress and biochemical parameters in adults at risk for cardiovascular disease. J Ethnopharmacol 133(1):46–52.  https://doi.org/10.1016/j.jep.2010.08.061 CrossRefPubMedGoogle Scholar
  16. 16.
    Johnson R, Dludla PV, Ferreira D, Muller CJF, Joubert E (2018) Aspalathin from rooibos (Aspalathus linearis): a bioactive C-glucosyl dihydrochalcone with potential to target the metabolic syndrome. Planta Med 84:568–583.  https://doi.org/10.1055/s-0044-100622 CrossRefPubMedGoogle Scholar
  17. 17.
    Dludla PV, Joubert E, Muller CJF, Louw J, Johnson R (2017a) Hyperglycemia-induced oxidative stress and heart disease-cardioprotective effects of rooibos flavonoids and phenylpyruvic acid-2-O-beta-D-glucoside. Nutr Metab 14:45.  https://doi.org/10.1186/s12986-017-0200-8 CrossRefGoogle Scholar
  18. 18.
    Muller CJ, Malherbe CJ, Chellan N, Yagasaki K, Miura Y, Joubert E (2016) Potential of rooibos, its major C-glucosyl flavonoids, and Z-2-(β-D-glucopyranosyloxy)-3-phenylpropenoic acid in prevention of metabolic syndrome. Crit Rev Food Sci Nutr 58(2):227–246.  https://doi.org/10.1080/10408398.2016.1157568 CrossRefGoogle Scholar
  19. 19.
    Mosa RA, Naidoo JJ, Nkomo FS, Mazibuko SE, Muller CJ, Opoku AR (2014) In vitro antihyperlipidemic potential of triterpenes from stem bark of Protorhus longifolia. Planta Med 80(18):1685–1691.  https://doi.org/10.1055/s-0034-1383262 CrossRefPubMedGoogle Scholar
  20. 20.
    Mosa RA, Cele NT, Opoku AR (2015) Anticoagulant and anti-inflammatory activity of a triterpene from Protorhus longifolia stem bark. J Med Plant Res 9(19):613–619.  https://doi.org/10.5897/JMPR2015.5740 CrossRefGoogle Scholar
  21. 21.
    Mosa RA, Cele ND, Mabhida SE, Shabalala SC, Penduka D, Opoku AR (2015) In vivo antihyperglycemic activity of a lanosteryl triterpene from Protorhus longifolia. Molecules 20(7):13374–13383.  https://doi.org/10.3390/molecules200713374 CrossRefPubMedGoogle Scholar
  22. 22.
    Putta S, Nagendra SA, Eswar KK, Challa S, Gjumrakch A, Madhihalli BD, Mysore SS, Ramith R, Farhan RZ, Nagendra PMN, Ramakrishna C, Pidugu VR, Yallappa S, Bhadrapura LD (2016) Therapeutic potentials of triterpenes in diabetes and its associated complications. Curr Top Med Chem 16(23):2532–2542(11)CrossRefGoogle Scholar
  23. 23.
    Nazaruk J, Borzym-Kluczyk M (2015) The role of triterpenes in the management of diabetes mellitus and its complications. Phytochem Rev 14(4):675–690.  https://doi.org/10.1007/s11101-014-9369-x CrossRefPubMedGoogle Scholar
  24. 24.
    Mosa RA, Hlophe NB, Ngema NT, Penduka D, Lawal OA, Opoku AR (2016) Cardioprotective potential of a lanosteryl triterpene from Protorhus longifolia. Pharm Biol 54(12):3244–3248.  https://doi.org/10.1080/13880209.2016.1223144 CrossRefPubMedGoogle Scholar
  25. 25.
    Machaba KE, Cobongela SZ, Mosa RA, Oladipupo LA, Djarova TG, Opoku AR (2014) In vivo anti-hyperlipidemic activity of the triterpene from the stem bark of Protorhus longifolia (Benrh) Engl. Lipids Health Dis 13:131.  https://doi.org/10.1186/1476-511X-13-131 CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Mosa RA, Gwala PE, Oyedeji AO, Opoku AR (2011a) In vitro anti-platelet aggregation, antioxidant and cytotoxic activity of extracts of some Zulu medicinal plants. J Nat Prod 4(2011):136–146Google Scholar
  27. 27.
    Mosa RA, Shode FO, Singh M, Opoku AR (2011b) Triterpenes from the stem bark of Protorhus longifolia exhibit anti-platelet aggregation activity. Afr J Pharm Pharmacol 5(24):2698–2714.  https://doi.org/10.5897/AJPP11.534 CrossRefGoogle Scholar
  28. 28.
    World Health Organization (2017) The top 10 causes of death. Available at http://www.who.int/mediacentre/factsheets/fs310/en/. Accessed 31 Jan 2018
  29. 29.
    Statistics South Africa (2017) Mortality and causes of death, 2015. Available at http://www.statssa.gov.za/publications/P03093/P030932015.pdf, Accessed 30 Jan 2018
  30. 30.
    Yilmaz S, Canpolat U, Aydogdu S, Abboud HE (2015) Diabetic cardiomyopathy; summary of 41 years. Korean Circ J 45(4):266–272.  https://doi.org/10.4070/kcj.2015.45.4.266 CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Dandamudi S, Slusser J, Mahoney DW, Redfield MM, Rodeheffer RJ, Chen HH (2014) The prevalence of diabetic cardiomyopathy: a population-based study in Olmsted County, Minnesota. J Card Fail 20(5):304–309.  https://doi.org/10.1016/j.cardfail.2014.02.007 CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Aronson D, Edelman ER (2014) Coronary artery disease and diabetes mellitus. Cardiol Clin 32(3):439–455.  https://doi.org/10.1016/j.ccl.2014.04.001 CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Boudina S, Abel ED (2007) Diabetic cardiomyopathy revisited. Circulation 115(25):3213–3223.  https://doi.org/10.1161/CIRCULATIONAHA.106.679597 CrossRefPubMedGoogle Scholar
  34. 34.
    Boudina S, Sena S, Theobald H, Sheng X, Wright JJ, Hu XX, Aziz S, Johnson JI, Bugger H, Zaha VG, Abel ED (2007) Mitochondrial energetics in the heart in obesity-related diabetes: direct evidence for increased uncoupled respiration and activation of uncoupling proteins. Diabetes 56(10):2457–2466.  https://doi.org/10.2337/db07-0481 CrossRefPubMedGoogle Scholar
  35. 35.
    Ansley DM, Wang B (2013) Oxidative stress and myocardial injury in the diabetic heart. J Pathol 229(2):232–241.  https://doi.org/10.1002/path.4113 CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Loganathan R, Bilgen M, Al-Hafez B, Alenezy MD, Smirnova IV (2006) Cardiac dysfunction in the diabetic rat: quantitative evaluation using high resolution magnetic resonance imaging. Cardiovasc Diabetol 5(7):7.  https://doi.org/10.1186/1475-2840-5-7 CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Cai L, Li W, Wang G, Guo L, Jiang Y, Kang YJ (2002) Hyperglycemia-induced apoptosis in mouse myocardium: mitochondrial cytochrome C-mediated caspase-3 activation pathway. Diabetes 51(6):1938–1948CrossRefGoogle Scholar
  38. 38.
    Marfella R, Di Filippo C, Portoghese M, Barbieri M, Ferraraccio F, Siniscalchi M, Cacciapuoti F, Rossi F, D’Amico M, Paolisso G (2009) Myocardial lipid accumulation in patients with pressure-overloaded heart and metabolic syndrome. J Lipid Res 50(11):2314–2323.  https://doi.org/10.1194/jlr.P900032-JLR200 CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Garg R, Aggarwal S, Kumar R, Sharma G (2015) Association of atherosclerosis with dyslipidemia and co-morbid conditions: a descriptive study. J Nat Sci Biol Med 6(1):163–168.  https://doi.org/10.4103/0976-9668.149117 CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Miller M (2009) Dyslipidemia and cardiovascular risk: the importance of early prevention. QJM 102(9):657–667.  https://doi.org/10.1093/qjmed/hcp065 CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Kengne AP, Dzudie A, Sobngwi E (2008) Heart failure in sub-Saharan Africa: a literature review with emphasis on individuals with diabetes. Vasc Health Risk Manag 4(1):123–130CrossRefGoogle Scholar
  42. 42.
    Nigro G, Comi LI, Politano L, Bain RJ (1990) The incidence and evolution of cardiomyopathy in Duchenne muscular dystrophy. Int J Cardiol 26(3):271–277CrossRefGoogle Scholar
  43. 43.
    Boudina S, Abel ED (2010) Diabetic cardiomyopathy, causes and effects. Rev Endocr Metab Disord 11(1):31–39.  https://doi.org/10.1007/s11154-010-9131-7 CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Rubler S, Dlugash J, Yuceoglu YZ, Kumral T, Branwood AW, Grishman A (1972) New type of cardiomyopathy associated with diabetic glomerulosclerosis. Am J Cardiol 30(6):595–602CrossRefGoogle Scholar
  45. 45.
    Lionetti V, Stanley WC, Recchia FA (2011) Modulating fatty acid oxidation in heart failure. Cardiovasc Res 90(2):202–209.  https://doi.org/10.1093/cvr/cvr038 CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Lopaschuk GD, Ussher JR, Folmes CD, Jaswal JS, Stanley WC (2010) Myocardial fatty acid metabolism in health and disease. Physiol Rev 90(1):207–258.  https://doi.org/10.1152/physrev.00015.2009 CrossRefPubMedGoogle Scholar
  47. 47.
    Randle PJ, Garland PB, Hales CN, Newsholme EA (1963) The glucose fatty-acid cycle. Its role in insulin sensitivity and the metabolic disturbances of diabetes mellitus. Lancet 1(7285):785–789CrossRefGoogle Scholar
  48. 48.
    Johnson R, Dludla P, Joubert E, February F, Mazibuko S, Ghoor S, Muller C, Louw J (2016) Aspalathin, a dihydrochalcone C-glucoside, protects H9c2 cardiomyocytes against high glucose induced shifts in substrate preference and apoptosis. Mol Nutr Food Res 60(4):922–934.  https://doi.org/10.1002/mnfr.201500656 CrossRefPubMedGoogle Scholar
  49. 49.
    Long YC, Zierath JR (2006) AMP-activated protein kinase signaling in metabolic regulation. J Clin Invest 116(7):1776–1783.  https://doi.org/10.1172/jci29044 CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Tsai JY, Villegas-Montoya C, Boland BB, Blasier Z, Egbejimi O, Gonzalez R, Kueht M, McElfresh TA, Brewer RA, Chandler MP, Bray MS, Young ME (2013) Influence of dark phase restricted high fat feeding on myocardial adaptation in mice. J Mol Cell Cardiol 55:147–155.  https://doi.org/10.1016/j.yjmcc.2012.09.010 CrossRefPubMedGoogle Scholar
  51. 51.
    Bugger H, Abel ED (2014) Molecular mechanisms of diabetic cardiomyopathy. Diabetologia 57(4):660–671.  https://doi.org/10.1007/s00125-014-3171-6 CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Taegtmeyer H, McNulty P, Young ME (2002) Adaptation and maladaptation of the heart in diabetes: part I: general concepts. Circulation 105(14):1727–1733CrossRefGoogle Scholar
  53. 53.
    Galluzzi L, Bravo-San Pedro JM, Vitale I, Aaronson SA, Abrams JM, Adam D, Alnemri ES, Altucci L, Andrews D, Annicchiarico-Petruzzelli M, Baehrecke EH, Bazan NG, Bertrand MJ, Bianchi K, Blagosklonny MV, Blomgren K, Borner C, Bredesen DE, Brenner C, Campanella M, Candi E, Cecconi F, Chan FK, Chandel NS, Cheng EH, Chipuk JE, Cidlowski JA, Ciechanover A, Dawson TM, Dawson VL, De Laurenzi V, De Maria R, Debatin KM, Di Daniele N, Dixit VM, Dynlacht BD, El-Deiry WS, Fimia GM, Flavell RA, Fulda S, Garrido C, Gougeon ML, Green DR, Gronemeyer H, Hajnoczky G, Hardwick JM, Hengartner MO, Ichijo H, Joseph B, Jost PJ, Kaufmann T, Kepp O, Klionsky DJ, Knight RA, Kumar S, Lemasters JJ, Levine B, Linkermann A, Lipton SA, Lockshin RA, Lopez-Otin C, Lugli E, Madeo F, Malorni W, Marine JC, Martin SJ, Martinou JC, Medema JP, Meier P, Melino S, Mizushima N, Moll U, Munoz-Pinedo C, Nunez G, Oberst A, Panaretakis T, Penninger JM, Peter ME, Piacentini M, Pinton P, Prehn JH, Puthalakath H, Rabinovich GA, Ravichandran KS, Rizzuto R, Rodrigues CM, Rubinsztein DC, Rudel T, Shi Y, Simon HU, Stockwell BR, Szabadkai G, Tait SW, Tang HL, Tavernarakis N, Tsujimoto Y, Vanden Berghe T, Vandenabeele P, Villunger A, Wagner EF, Walczak H, White E, Wood WG, Yuan J, Zakeri Z, Zhivotovsky B, Melino G, Kroemer G (2015) Essential versus accessory aspects of cell death: recommendations of the NCCD 2015. Cell Death Differ 22(1):58–73.  https://doi.org/10.1038/cdd.2014.137 CrossRefPubMedGoogle Scholar
  54. 54.
    Bo H, Jiang N, Ma G, Qu J, Zhang G, Cao D, Wen L, Liu S, Ji LL, Zhang Y (2008) Regulation of mitochondrial uncoupling respiration during exercise in rat heart: role of reactive oxygen species (ROS) and uncoupling protein 2. Free Radic Biol Med 44(7):1373–1381.  https://doi.org/10.1016/j.freeradbiomed.2007.12.033 CrossRefPubMedGoogle Scholar
  55. 55.
    Boehm EA, Jones BE, Radda GK, Veech RL, Clarke K (2001) Increased uncoupling proteins and decreased efficiency in palmitate-perfused hyperthyroid rat heart. Am J Phys Heart Circ Phys 280(3):H977–H983Google Scholar
  56. 56.
    Dludla PV, Muller CJ, Joubert E, Louw J, Essop MF, Gabuza KB, Ghoor S, Huisamen B, Johnson R (2017b) Aspalathin protects the heart against hyperglycemia-induced oxidative damage by up-regulating Nrf2 expression. Molecules 22(1).  https://doi.org/10.3390/molecules22010129
  57. 57.
    Johnson R, Dludla PV, Muller CJ, Huisamen B, Essop MF, Louw J (2017) The transcription profile unveils the cardioprotective effect of aspalathin against lipid toxicity in an in vitro H9c2 model. Molecules 22(2).  https://doi.org/10.3390/molecules22020219
  58. 58.
    He X, Kan H, Cai L, Ma Q (2009) Nrf2 is critical in defense against high glucose-induced oxidative damage in cardiomyocytes. J Mol Cell Cardiol 46(1):47–58.  https://doi.org/10.1016/j.yjmcc.2008.10.007 CrossRefPubMedGoogle Scholar
  59. 59.
    Satta SMA, Wilkinson FL, Alexander MY, White S (2017) The role of Nrf2 in cardiovascular function and disease. Oxidative medicine and cellular longevity. Oxidative Med Cell Longev 2017:18.  https://doi.org/10.1155/2017/9237263 CrossRefGoogle Scholar
  60. 60.
    An J, Chen Y, Huang Z (2004) Critical upstream signals of cytochrome C release induced by a novel Bcl-2 inhibitor. J Biol Chem 279(18):19133–19140.  https://doi.org/10.1074/jbc.M400295200 CrossRefPubMedGoogle Scholar
  61. 61.
    Cicek FA, Toy A, Tuncay E, Can B, Turan B (2014) Beta-blocker timolol alleviates hyperglycemia-induced cardiac damage via inhibition of endoplasmic reticulum stress. J Bioenerg Biomembr 46(5):377–387.  https://doi.org/10.1007/s10863-014-9568-6 CrossRefPubMedGoogle Scholar
  62. 62.
    Dludla PV, Muller CJ, Joubert E, Louw J, Gabuza KB, Huisamen B, Essop MF, Johnson R (2016) Phenylpyruvic Acid-2-O-beta-D-glucoside attenuates high glucose-induced apoptosis in H9c2 cardiomyocytes. Planta Med 82(17):1468–1474.  https://doi.org/10.1055/s-0042-110856 CrossRefPubMedGoogle Scholar
  63. 63.
    Elmore S (2007) Apoptosis: a review of programmed cell death. Toxicol Pathol 35(4):495–516.  https://doi.org/10.1080/01926230701320337 CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Crompton M (1999) The mitochondrial permeability transition pore and its role in cell death. Biochem J 341(Pt 2):233–249CrossRefGoogle Scholar
  65. 65.
    Gupta SK, Dongare S, Mathur R, Mohanty IR, Srivastava S, Mathur S, Nag TC (2015) Genistein ameliorates cardiac inflammation and oxidative stress in streptozotocin-induced diabetic cardiomyopathy in rats. Mol Cell Biochem 408(1–2):63–72.  https://doi.org/10.1007/s11010-015-2483-2 CrossRefPubMedGoogle Scholar
  66. 66.
    Suzuki H, Kayama Y, Sakamoto M, Iuchi H, Shimizu I, Yoshino T, Katoh D, Nagoshi T, Tojo K, Minamino T, Yoshimura M, Utsunomiya K (2015) Arachidonate 12/15-lipoxygenase-induced inflammation and oxidative stress are involved in the development of diabetic cardiomyopathy. Diabetes 64(2):618–630.  https://doi.org/10.2337/db13-1896 CrossRefPubMedGoogle Scholar
  67. 67.
    Suthahar N, Meijers WC, Brouwers FP, Heerspink HJL, Gansevoort RT, van der Harst P, Bakker SJL, de Boer RA (2018) Heart failure and inflammation-related biomarkers as predictors of new-onset diabetes in the general population. Int J Cardiol 250:188–194.  https://doi.org/10.1016/j.ijcard.2017.10.035 CrossRefPubMedGoogle Scholar
  68. 68.
    Battiprolu PK, Gillette TG, Wang ZV, Lavandero S, Hill JA (2010) Diabetic cardiomyopathy: mechanisms and therapeutic targets. Drug Discov Today Dis Mech 7(2):e135–e143.  https://doi.org/10.1016/j.ddmec.2010.08.001 CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Fang WJ, Wang CJ, He Y, Zhou YL, Peng XD, Liu SK (2017) Resveratrol alleviates diabetic cardiomyopathy in rats by improving mitochondrial function through PGC-1alpha deacetylation. Acta Pharmacol Sin 39:59–73.  https://doi.org/10.1038/aps.2017.50 CrossRefPubMedGoogle Scholar
  70. 70.
    Guimaraes JF, Muzio BP, Rosa CM, Nascimento AF, Sugizaki MM, Fernandes AA, Cicogna AC, Padovani CR, Okoshi MP, Okoshi K (2015) Rutin administration attenuates myocardial dysfunction in diabetic rats. Cardiovasc Diabetol 14:90.  https://doi.org/10.1186/s12933-015-0255-7 CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Chen WJ, Greulich S, van der Meer RW, Rijzewijk LJ, Lamb HJ, de Roos A, Smit JW, Romijn JA, Ruige JB, Lammertsma AA, Lubberink M, Diamant M, Ouwens DM (2013) Activin A is associated with impaired myocardial glucose metabolism and left ventricular remodeling in patients with uncomplicated type 2 diabetes. Cardiovasc Diabetol 12:150.  https://doi.org/10.1186/1475-2840-12-150 CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Sun X, Chen RC, Yang ZH, Sun GB, Wang M, Ma XJ, Yang LJ, Sun XB (2014) Taxifolin prevents diabetic cardiomyopathy in vivo and in vitro by inhibition of oxidative stress and cell apoptosis. Food Chem Toxicol 63:221–232.  https://doi.org/10.1016/j.fct.2013.11.013 CrossRefPubMedGoogle Scholar
  73. 73.
    Liu X, Zhu L, Tan J, Zhou X, Xiao L, Yang X, Wang B (2014) Glucosidase inhibitory activity and antioxidant activity of flavonoid compound and triterpenoid compound from Agrimonia Pilosa Ledeb. BMC Complement Altern Med 14:12.  https://doi.org/10.1186/1472-6882-14-12 CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Yang Y, Li C, Xiang X, Dai Z, Chang J, Zhang M, Cai H, Zhang H, Zhang M, Guo Y, Wu Z (2014) Ursolic acid prevents endoplasmic reticulum stress-mediated apoptosis induced by heat stress in mouse cardiac myocytes. J Mol Cell Cardiol 67:103–111.  https://doi.org/10.1016/j.yjmcc.2013.12.018 CrossRefPubMedGoogle Scholar
  75. 75.
    Hamid K, Ng I, Tallapragada VJ, Varadi L, Hibbs DE, Hanrahan J, Groundwater PW (2016) An investigation of the differential effects of ursane triterpenoids from Centella asiatica, and their semisynthetic analogues, on GABAA receptors. Chem Biol Drug Des 88(3):386–397.  https://doi.org/10.1111/cbdd.12766 CrossRefPubMedGoogle Scholar
  76. 76.
    Rodriguez-Rodriguez R (2015) Oleanolic acid and related triterpenoids from olives on vascular function: molecular mechanisms and therapeutic perspectives. Curr Med Chem 22(11):1414–1425CrossRefGoogle Scholar
  77. 77.
    Pergola PE, Raskin P, Toto RD, Meyer CJ, Huff JW, Grossman EB, Krauth M, Ruiz S, Audhya P, Christ-Schmidt H, Wittes J, Warnock DG (2011) Bardoxolone methyl and kidney function in CKD with type 2 diabetes. N Engl J Med 365(4):327–336.  https://doi.org/10.1056/NEJMoa1105351 CrossRefPubMedGoogle Scholar
  78. 78.
    Sidjui LS, Eyong KO, Hull KG (2017) Bioactive seco-lanostane-type triterpenoids from the roots of Leplaea mayombensis. J Nat Prod 80(10):2644–2651.  https://doi.org/10.1021/acs.jnatprod.7b00210
  79. 79.
    Hill RA, Connolly JD (2017) Triterpenoids. Nat Prod Rep 34(1):90–122.  https://doi.org/10.1039/c6np00094 CrossRefPubMedGoogle Scholar
  80. 80.
    Lee I, Kim J, Ryoo I, Kim Y, Choo S, Yoo I, Min B, Na M, Hattori M, Bae K (2010a) Lanostane triterpenes from Ganoderma lucidum suppress the adipogenesis in 3T3-L1 cells through down-regulation of SREBP-1c. Bioorg Med Chem Lett 20(18):5577–5581.  https://doi.org/10.1016/j.bmcl.2010.06.093 CrossRefPubMedGoogle Scholar
  81. 81.
    Lee I, Seo J, Kim J, Kim H, Youn U, Lee J, Jung H, Na M, Hattori M, Min B, Bae K (2010b) Lanostane triterpenes from the fruiting bodies of Ganoderma lucidum and their inhibitory effects on adipocyte differentiation in 3T3-L1 cells. J Nat Prod 73(2):172–176.  https://doi.org/10.1021/np900578h CrossRefPubMedGoogle Scholar
  82. 82.
    Dold AP, Cocks ML (2002) The trade in medicinal plants in the Eastern Cape Province, South Africa. S Afr J Sci 98(11–12):589–597Google Scholar
  83. 83.
    Keirungi J, Fabricius C (2005) Selecting medicinal plants for cultivation at Nqabara on the Eastern Cape Wild Coast, South Africa. S Afr J Sci 101(11–12):497–501 doi: 10520/EJC96329Google Scholar
  84. 84.
    Lawson K (2015) Botanical and plant-derived drugs: global markets, BIO022G. Available at: https://www.bccresearch.com/market-research/biotechnology/botanical-plant-derived-drugs-report-bio022g
  85. 85.
    Joubert EDBD (2011) Rooibos (Aspalathus linearis) beyond the farm gate: from herbal tea to potential phytopharmaceutical. S Afr J Bot 77(4):869–886.  https://doi.org/10.1016/j.sajb.2011.07.004 CrossRefGoogle Scholar
  86. 86.
    Suleiman MM, McGaw LI, Naidoo V, Eloff J (2009) Detection of antimicrobial compounds by bioautography of different extracts of leaves of selected South African tree species. Afr J Tradit Complement Altern Med 7(1).  https://doi.org/10.4314/57269
  87. 87.
    Penduka D, Mosa R, Simelane M, Basson A, Okoh A, Opoku A (2014) Evaluation of the anti-Listeria potentials of some plant-derived triterpenes. Ann Clin Microbiol Antimicrob 13:37.  https://doi.org/10.1186/s12941-014-0037-1 CrossRefPubMedPubMedCentralGoogle Scholar
  88. 88.
    Sellers RS, Radi ZA, Khan NK (2010) Pathophysiology of cyclooxygenases in cardiovascular homeostasis. Vet Pathol 47(4):601–613.  https://doi.org/10.1177/0300985810364389 CrossRefPubMedGoogle Scholar
  89. 89.
    Kunutsor SK, Apekey TA, Khan H (2014) Liver enzymes and risk of cardiovascular disease in the general population: a meta-analysis of prospective cohort studies. Atherosclerosis 236(1):7–17.  https://doi.org/10.1016/j.atherosclerosis.2014.06.006 CrossRefPubMedGoogle Scholar
  90. 90.
    Zhou R, Xu Q, Zheng P, Yan L, Zheng J, Dai G (2008) Cardioprotective effect of fluvastatin on isoproterenol-induced myocardial infarction in rat. Eur J Pharmacol 586(1):244–250.  https://doi.org/10.1016/j.ejphar.2008.02.057 CrossRefPubMedGoogle Scholar
  91. 91.
    Mabhida SE, Mosa RA, Penduka D, Osunsanmi FO, Dludla PV, Tryana G, Djarova TG, Opuko AR (2017) A lanosteryl triterpene from Protorhus longifolia improves glucose tolerance and pancreatic beta cell ultrastructure in type 2 diabetic rats. Molecules 22(8):1252.  https://doi.org/10.3390/molecules22081252 CrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Biomedical Research and Innovation Platform (BRIP)South African Medical Research CouncilTygerbergSouth Africa
  2. 2.Department of Biochemistry and MicrobiologyUniversity of ZululandKwaDlangezwaSouth Africa
  3. 3.Division of Medical Physiology, Faculty of Health SciencesStellenbosch UniversityTygerbergSouth Africa

Personalised recommendations