Nutrition Research and Practice

The Korean Nutrition Society (한국영양학회)
권호 표지
DOI QR코드

DOI QR Code

Opuntia humifusa stems rich in quercetin and isorhamnetin alleviate insulin resistance in high-fat diet-fed rats

  • Young-Min Lee (Department of Practical Science Education, Gyeongin National University of Education) ;
  • Yeonjeong Choi (Department of Food and Nutrition, Gyeongsang National University) ;
  • Eunseo Kim (Department of Food and Nutrition, Gyeongsang National University) ;
  • In-Guk Hwang (Functional Food Division, National Institute of Agricultural Sciences, Rural Development Administration) ;
  • Yoona Kim (Department of Food and Nutrition, Institute of Agriculture and Life Science, Gyeongsang National University)
  • Received : 2024.01.29
  • Accepted : 2024.05.09
  • Published : 2024.08.01
Download PDF
⟨ Previous Next ⟩

Abstract

BACKGROUND/OBJECTIVES: Obesity, characterized by abnormal fat accumulation and metabolic disturbances, presents a significant health challenge. Opuntia humifusa Raf., commonly known as Korean Cheonnyuncho, is rich in various beneficial compounds and has demonstrated antioxidant and anti-inflammatory effects. However, its potential impact on glucose and lipid metabolism, particularly in obese rats, remains unexplored. We aimed to investigate whether O. humifusa stems and fruits could beneficially alter glucose metabolism and lipid profiles in a rat model of high-fat diet (HFD)-induced obesity. MATERIALS/METHODS: Thirty-two rats were allocated into 4 groups: normal diet (NF), HFD control (HF), HFD treated with 2% O. humifusa stems (HF-OS), and HFD treated with 2% O. humifusa fruits (HF-OF). Experimental diets were administered for 6 weeks. At the end of the treatment, liver and fat tissues were isolated, and serum was collected for biochemical analysis. The major flavonoid from O. humifusa stems and fruits was identified and quantified. RESULTS: After 6 weeks of treatment, the serum fasting glucose concentration in the HF-OS group was significantly lower than that in the HF group. Serum fasting insulin concentrations in both HF-OS and HF-OF groups tended to be lower than those in the HF group, indicating a significant improvement in insulin sensitivity in the HF-OS group. Additionally, the HF-OS group exhibited a tendency towards the restoration of adiponectin levels to that of the NF group. CONCLUSION: The 2% O. humifusa stems contain abundant quercetin and isorhamnetin, which alter fasting blood glucose levels in rats fed a HFD, leading to a favorable improvement in insulin resistance.

Keywords

Acknowledgement

The authors would like to thank Minkyung Je, Kyeonghoon Kang, Gyeonghye Baek, and Jimin Jeong for their valuable contributions in obtaining samples after the animals were euthanized.

References

  1. Boutari C, Mantzoros CS. A 2022 update on the epidemiology of obesity and a call to action: as its twin COVID-19 pandemic appears to be receding, the obesity and dysmetabolism pandemic continues to rage on. Metabolism 2022;133:155217.
  2. Hill JO, Wyatt HR, Peters JC. Energy balance and obesity. Circulation 2012;126:126-32. https://doi.org/10.1161/CIRCULATIONAHA.111.087213
  3. Woolcott OO, Seuring T. Prevalence trends in obesity defined by the relative fat mass (RFM) index among adults in the United States: 1999-2018. Metabolism 2022;128:155027.
  4. Kivimaki M, Strandberg T, Pentti J, Nyberg ST, Frank P, Jokela M, Ervasti J, Suominen SB, Vahtera J, Sipila PN, et al. Body-mass index and risk of obesity-related complex multimorbidity: an observational multicohort study. Lancet Diabetes Endocrinol 2022;10:253-63. https://doi.org/10.1016/S2213-8587(22)00033-X
  5. Petrie JR, Guzik TJ, Touyz RM. Diabetes, hypertension, and cardiovascular disease: clinical insights and vascular mechanisms. Can J Cardiol 2018;34:575-84.  https://doi.org/10.1016/j.cjca.2017.12.005
  6. Emerging Risk Factors Collaboration, Wormser D, Kaptoge S, Di Angelantonio E, Wood AM, Pennells L, Thompson A, Sarwar N, Kizer JR, Lawlor DA, et al. Separate and combined associations of body-mass index and abdominal adiposity with cardiovascular disease: collaborative analysis of 58 prospective studies. Lancet 2011;377:1085-95. https://doi.org/10.1016/S0140-6736(11)60105-0
  7. Mayor S. Being overweight may raise risk of eight more cancers, review finds. BMJ 2016;354:i4650.
  8. Fabbrini E, Sullivan S, Klein S. Obesity and nonalcoholic fatty liver disease: biochemical, metabolic, and clinical implications. Hepatology 2010;51:679-89. https://doi.org/10.1002/hep.23280
  9. Francque SM, Dirinck E. NAFLD prevalence and severity in overweight and obese populations. Lancet Gastroenterol Hepatol 2023;8:2-3. https://doi.org/10.1016/S2468-1253(22)00375-2
  10. Tyrrell J, Mulugeta A, Wood AR, Zhou A, Beaumont RN, Tuke MA, Jones SE, Ruth KS, Yaghootkar H, Sharp S, et al. Using genetics to understand the causal influence of higher BMI on depression. Int J Epidemiol 2019;48:834-48. https://doi.org/10.1093/ije/dyy223
  11. Mili N, Paschou SA, Goulis DG, Dimopoulos MA, Lambrinoudaki I, Psaltopoulou T. Obesity, metabolic syndrome, and cancer: pathophysiological and therapeutic associations. Endocrine 2021;74:478-97. https://doi.org/10.1007/s12020-021-02884-x
  12. Taylor R. Pathogenesis of type 2 diabetes: tracing the reverse route from cure to cause. Diabetologia 2008;51:1781-9. https://doi.org/10.1007/s00125-008-1116-7
  13. Larsson SC, Burgess S. Causal role of high body mass index in multiple chronic diseases: a systematic review and meta-analysis of Mendelian randomization studies. BMC Med 2021;19:320.
  14. Kotsis V, Jordan J, Micic D, Finer N, Leitner DR, Toplak H, Tokgozoglu L, Athyros V, Elisaf M, Filippatos TD, et al. Obesity and cardiovascular risk: a call for action from the European Society of Hypertension Working Group of Obesity, Diabetes and the High-risk Patient and European Association for the Study of Obesity: part A: mechanisms of obesity induced hypertension, diabetes and dyslipidemia and practice guidelines for treatment. J Hypertens 2018;36:1427-40. https://doi.org/10.1097/HJH.0000000000001730
  15. Flegal KM, Kit BK, Orpana H, Graubard BI. Association of all-cause mortality with overweight and obesity using standard body mass index categories: a systematic review and meta-analysis. JAMA 2013;309:71-82. https://doi.org/10.1001/jama.2012.113905
  16. Jia H, Lubetkin EI. Trends in quality-adjusted life-years lost contributed by smoking and obesity. Am J Prev Med 2010;38:138-44. https://doi.org/10.1016/j.amepre.2009.09.043
  17. Kolotkin RL, Meter K, Williams GR. Quality of life and obesity. Obes Rev 2001;2:219-29. https://doi.org/10.1046/j.1467-789X.2001.00040.x
  18. Finkelstein EA, Trogdon JG, Cohen JW, Dietz W. Annual medical spending attributable to obesity: payer-and service-specific estimates. Health Aff (Millwood) 2009;28:w822-31. https://doi.org/10.1377/hlthaff.28.5.w822
  19. Okunogbe A, Nugent R, Spencer G, Ralston J, Wilding J. Economic impacts of overweight and obesity: current and future estimates for eight countries. BMJ Glob Health 2021;6:e006351.
  20. Okunogbe A, Nugent R, Spencer G, Powis J, Ralston J, Wilding J. Economic impacts of overweight and obesity: current and future estimates for 161 countries. BMJ Glob Health 2022;7:e009773.
  21. Anderson EF. The Cactus Family. Portland (OR): Timber Press; 2001. 
  22. Goldstein G, Nobel PS. Water relations and low-temperature acclimation for cactus species varying in freezing tolerance. Plant Physiol 1994;104:675-81. https://doi.org/10.1104/pp.104.2.675
  23. Del Socorro Santos Diaz M, Barba de la Rosa AP, Helies-Toussaint C, Gueraud F, Negre-Salvayre A. Opuntia spp.: characterization and benefits in chronic diseases. Oxid Med Cell Longev 2017;2017:8634249.
  24. Yoon JA, Hahm SW, Park JE, Son YS. Total polyphenol and flavonoid of fruit extract of Opuntia humifusa and its inhibitory effect on the growth of MCF-7 human breast cancer cells. J Korean Soc Food Sci Nutr 2009;38:1679-84. https://doi.org/10.3746/jkfn.2009.38.12.1679
  25. Yoon JA, Hahm SW, Son YS. Nutrients contents in different parts of pickly pear (Opuntia humifusa) and possible anti-breast cancer effect. J Korean Soc Food Sci Nutr 2009;22:485-91. 
  26. Hahm SW, Park J, Son YS. Opuntia humifusa stems lower blood glucose and cholesterol levels in streptozotocin-induced diabetic rats. Nutr Res 2011;31:479-87. https://doi.org/10.1016/j.nutres.2011.05.002
  27. Cho JY, Park SC, Kim TW, Kim KS, Song JC, Kim SK, Lee HM, Sung HJ, Park HJ, Song YB, et al. Radical scavenging and anti-inflammatory activity of extracts from Opuntia humifusa Raf. J Pharm Pharmacol 2006;58:113-9. https://doi.org/10.1211/jpp.58.1.0014
  28. Kim J, Jho KH, Choi YH, Nam SY. Chemopreventive effect of cactus (Opuntia humifusa) extracts: radical scavenging activity, pro-apoptosis, and anti-inflammatory effect in human colon (SW480) and breast cancer (MCF7) cells. Food Funct 2013;4:681-8. https://doi.org/10.1039/c3fo30287c
  29. Yeo JY, Hwang KW, Park SY. Anti-inflammatory effect of neo-lignan isoamericanin A via suppression of NF-κB in liposaccharide-stimulated RAW 264.7 cells. Trop J Pharm Res 2020;19:1857-62.  https://doi.org/10.4314/tjpr.v19i9.9
  30. Hahm SW, Park J, Son YS. Opuntia humifusa partitioned extracts inhibit the growth of U87MG human glioblastoma cells. Plant Foods Hum Nutr 2010;65:247-52. https://doi.org/10.1007/s11130-010-0188-y
  31. Lee SH, Kim HW, Lee MK, Kim YJ, Asamenew G, Cha YS, Kim JB. Phenolic profiling and quantitative determination of common sage (Salvia plebeia R. Br.) by UPLC-DAD-QTOF/MS. Eur Food Res Technol 2018;244:1637-46.  https://doi.org/10.1007/s00217-018-3076-6
  32. Kim HW, Lee SH, Yoo SM, Chung MN, Kim JB, Kehraus S, Koenig GM. Identification and quantification of hydroxybenzoyl and hydroxycinnamoyl derivatives from Korean sweet potato cultivars by UPLC-DAD-QToF/MS. J Food Compos Anal 2021;100:103905.
  33. Mosser RE, Maulis MF, Moulle VS, Dunn JC, Carboneau BA, Arasi K, Pappan K, Poitout V, Gannon M. High-fat diet-induced β-cell proliferation occurs prior to insulin resistance in C57Bl/6J male mice. Am J Physiol Endocrinol Metab 2015;308:E573-82. https://doi.org/10.1152/ajpendo.00460.2014
  34. Antunes LC, Elkfury JL, Jornada MN, Foletto KC, Bertoluci MC. Validation of HOMA-IR in a model of insulin-resistance induced by a high-fat diet in Wistar rats. Arch Endocrinol Metab 2016;60:138-42. https://doi.org/10.1590/2359-3997000000169
  35. Nemati M, Zardooz H, Rostamkhani F, Abadi A, Foroughi F. High-fat diet effects on metabolic responses to chronic stress. Arch Physiol Biochem 2017;123:182-91. https://doi.org/10.1080/13813455.2017.1295083
  36. Kang J, Lee J, Kwon D, Song Y. Effect of Opuntia humifusa supplementation and acute exercise on insulin sensitivity and associations with PPAR-γ and PGC-1α protein expression in skeletal muscle of rats. Int J Mol Sci 2013;14:7140-54. https://doi.org/10.3390/ijms14047140
  37. Chandran M, Phillips SA, Ciaraldi T, Henry RR. Adiponectin: more than just another fat cell hormone? Diabetes Care 2003;26:2442-50. https://doi.org/10.2337/diacare.26.8.2442
  38. Menzaghi C, Trischitta V, Doria A. Genetic influences of adiponectin on insulin resistance, type 2 diabetes, and cardiovascular disease. Diabetes 2007;56:1198-209. https://doi.org/10.2337/db06-0506
  39. Katsiki N, Mantzoros C, Mikhailidis DP. Adiponectin, lipids and atherosclerosis. Curr Opin Lipidol 2017;28:347-54. https://doi.org/10.1097/MOL.0000000000000431
  40. Tschritter O, Fritsche A, Thamer C, Haap M, Shirkavand F, Rahe S, Staiger H, Maerker E, Haring H, Stumvoll M. Plasma adiponectin concentrations predict insulin sensitivity of both glucose and lipid metabolism. Diabetes 2003;52:239-43. https://doi.org/10.2337/diabetes.52.2.239
  41. Liu C, Feng X, Li Q, Wang Y, Li Q, Hua M. Adiponectin, TNF-α and inflammatory cytokines and risk of type 2 diabetes: a systematic review and meta-analysis. Cytokine 2016;86:100-9. https://doi.org/10.1016/j.cyto.2016.06.028
  42. Kim EK, Kwon KB, Song MY, Han MJ, Lee JH, Lee YR, Lee JH, Ryu DG, Park BH, Park JW. Flavonoids protect against cytokine-induced pancreatic beta-cell damage through suppression of nuclear factor κB activation. Pancreas 2007;35:e1-9. https://doi.org/10.1097/mpa.0b013e31811ed0d2
  43. Ouchi N, Walsh K. Adiponectin as an anti-inflammatory factor. Clin Chim Acta 2007;380:24-30. https://doi.org/10.1016/j.cca.2007.01.026
  44. Jung EY, Yeon SH, Suh HJ. Hypocholesterol effect of Opuntia humifusa extract on high cholesterol diet-induced hypercholesterolemic rats. J Korean Soc Food Sci Nutr 2014;43:485-90. https://doi.org/10.3746/jkfn.2014.43.4.485
  45. Baz L, Algarni S, Al-Thepyani M, Aldairi A, Gashlan H. Lycopene improves metabolic disorders and liver injury induced by a hight-fat diet in obese rats. Molecules 2022;27:7736.
  46. Park MK, Lee YJ, Kang ES. Hepatoprotective effect of Cheonnyuncho (Opuntia humifusa) extract in rats treated carbon tetrachloride. Korean J Food Sci Technol 2005;37:822-6. 
  47. Boucher P, de Lorgeril M, Salen P, Crozier P, Delaye J, Vallon JJ, Geyssant A, Dante R. Effect of dietary cholesterol on low density lipoprotein-receptor, 3-hydroxy-3-methylglutaryl-CoA reductase, and low density lipoprotein receptor-related protein mRNA expression in healthy humans. Lipids 1998;33:1177-86. https://doi.org/10.1007/s11745-998-0321-8
  48. Jiang H, Yamashita Y, Nakamura A, Croft K, Ashida H. Quercetin and its metabolite isorhamnetin promote glucose uptake through different signalling pathways in myotubes. Sci Rep 2019;9:2690.
  49. Kobori M, Masumoto S, Akimoto Y, Oike H. Chronic dietary intake of quercetin alleviates hepatic fat accumulation associated with consumption of a Western-style diet in C57/BL6J mice. Mol Nutr Food Res 2011;55:530-40. https://doi.org/10.1002/mnfr.201000392
  50. Matboli M, Saad M, Hasanin AH, A Saleh L, Baher W, Bekhet MM, Eissa S. New insight into the role of isorhamnetin as a regulator of insulin signaling pathway in type 2 diabetes mellitus rat model: molecular and computational approach. Biomed Pharmacother 2021;135:111176.
  51. Tundis R, Loizzo MR, Statti GA, Menichini F. Inhibitory effects on the digestive enzyme α-amylase of three Salsola species (Chenopodiaceae) in vitro. Pharmazie 2007;62:473-5.
  52. Yang EI, Lee CH, Che DN, Jang SI, Kim YS. Biological activities of water-soluble polysaccharides from Opuntia humifusa stem in high-fat-diet-fed mice. J Food Biochem 2019;43:e12806.