Skip to main content
Log in

Plantago maxima leaves extract inhibits adipogenic action of a high-fat diet in female Wistar rats

  • Original Contribution
  • Published:
European Journal of Nutrition Aims and scope Submit manuscript

Abstract

Purpose

The primary objective of this study is to investigate the content of biologically active compounds producing an antioxidant effect in Plantago maxima and their influence on main mechanisms of dietary obesity development.

Methods

Biologically active compounds in P. maxima were tested using paper chromatography. In in vivo experiment, high-fat-fed Wistar rats obtained P. maxima water extract for 3 months. Morphometric parameters, weight gain, serum adipokines, and cytokines, as well as oxidative stress biomarkers in rats’ tissues were evaluated. Gut microflora was also examined.

Results

Plantago maxima leaves used in the experiment contained significant amount of flavonoids, iridoids, phenol carboxylic acids, and tannins and ascorbic acid. Our in vivo experiment data demonstrate that P. maxima water extract prevents excessive adiposity in a diet-induced model. P. maxima consumption reduced serum leptin (twofold), macrophage chemoattractant protein-1 (sevenfold), tumor-necrosis factor-α (25 %), and interleukine-6 (26 %) levels. P. maxima water extract decreased adipose tissue oxidative stress biomarkers in rats fed a high-fat diet. In addition, increased bacterial growth in the diet-induced obesity model was reversed by the P. maxima extract treatment.

Conclusion

Plantago maxima water extract possessed antiadipogenic, antidiabetic, antiinflammatory, antioxidant activity, and normalized gut microflora in a rat model of diet-induced excessive adiposity due to a high content of biologically active compounds.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

Abbreviations

AC:

Abdominal circumference

AI:

Adiposity index

ANOVA:

Analysis of variance

AT:

Adipose tissue

BAAW:

n-Butanol–acetic acid–water

BMI:

Body mass index

CD:

Conjugated dienes

CFU:

Colony-forming units

CT:

Conjugated trienes

ELISA:

Enzyme-linked immunosorbent assay

HFD:

High-fat diet

IL-6:

Interleukine-6

LPS:

Lipopolysaccharide

MCP-1:

Macrophage chemoattractant protein-1

MDSA:

Microvessel density per specific area

PC:

Protein carbonyls

PMAT:

Parametrial adipose tissue

RPAT:

Retroperitoneal adipose tissue

STD:

Standard diet

TBARS:

Thiobarbituric acid-reactive substances

TC:

Thoracic circumference

TCC:

Total caloric consumption

TLC:

Total liquid consumption

TNF-α:

Tumor-necrosis factor-α

T-SH:

Total thiols

References

  1. Chiesi M, Huppertz C, Hofbauer KG (2001) Pharmacotherapy of obesity: targets and perspectives. Trends Pharmacol Sci 22(5):247–254

    Article  CAS  Google Scholar 

  2. González-Castejón M, Rodriguez-Casado A (2011) Dietary phytochemicals and their potential effects on obesity: a review. Pharmacol Res 64(5):438–455

    Article  CAS  Google Scholar 

  3. Matsuzawa-Nagata N, Takamura T, Ando H, Nakamura S, Kurita S, Misu H, Ota T, Yokoyama M, Honda M, Miyamoto K, Kaneko S (2008) Increased oxidative stress precedes the onset of high-fat diet-induced insulin resistance and obesity. Metabolism 57(8):1071–1077

    Article  CAS  Google Scholar 

  4. Mangge H, Summers K, Almer G, Prassl R, Weghuber D, Schnedl W, Fuchs D (2013) Antioxidant food supplements and obesity-related inflammation. Curr Med Chem 20(18):2330–2337

    Article  CAS  Google Scholar 

  5. Beara IN, Lesjak MM, Jovin ED, Balog KJ, Anackov GT, Orcić DZ, Mimica-Dukić NM (2009) Plantain (Plantago L.) species as novel sources of flavonoid antioxidants. J Agric Food Chem 57(19):9268–9273

    Article  CAS  Google Scholar 

  6. Vysochina GI, Kukushkina TA, Kotsupii OV, Zagurskaya YV, Bayandina II (2011) Flora of the forest-steppe zone of West Siberia as a source of biologically active compounds. Contemp Probl Ecol 4(2):202–211

    Article  Google Scholar 

  7. Hannan JM, Ali L, Khaleque J, Akhter M, Flatt PR, Abdel-Wahab YH (2006) Aqueous extracts of husks of Plantago ovata reduce hyperglycaemia in type 1 and type 2 diabetes by inhibition of intestinal glucose absorption. Br J Nutr 96(1):131–137

    Article  CAS  Google Scholar 

  8. Yoshida T, Rikimaru K, Sakai M, Nishibe S, Fujikawa T, Tamura Y (2013) Plantago lanceolata L. leaves prevent obesity in C57BL/6 J mice fed a high-fat diet. Nat Prod Res 27(11):982–987

    Google Scholar 

  9. Barua CC, Pal SK, Roy JD, Buragohain B, Talukdar A, Barua AG, Borah P (2011) Studies on the anti-inflammatory properties of Plantago erosa leaf extract in rodents. J Ethnopharmacol 134(1):62–66

    Article  CAS  Google Scholar 

  10. Solà R, Bruckert E, Valls RM, Narejos S, Luque X, Castro-Cabezas M, Doménech G, Torres F, Heras M, Farrés X, Vaquer JV, Martínez JM, Almaraz MC, Anguera A (2010) Soluble fibre (Plantago ovata husk) reduces plasma low-density lipoprotein (LDL) cholesterol, triglycerides, insulin, oxidised LDL and systolic blood pressure in hypercholesterolaemic patients: a randomised trial. Atherosclerosis 211(2):630–637

    Article  CAS  Google Scholar 

  11. Gröger D, Simchen P (1967) Zur Kentnis iridoider Pflanzenstoffe. Pharmazie 22(6):315–317

    Google Scholar 

  12. Scalbert A (1992) Quantitative methods for the estimation of tannins in plant tissues. In: Hemingway RW, Laks PS (eds) Plant polyphenols: synthesis, properties, significance. Plenum Press, New York, pp 259–280

    Chapter  Google Scholar 

  13. Chang C, Yang M, Wen H, Chern J (2002) Estimation of total flavonoid content in propolis by two complementary colorimetric methods. J Food Drug Anal 10:178–182

    CAS  Google Scholar 

  14. Cunniff PA (1998) Official methods of analysis of AOAC international, 16th edn.

  15. Trim AR, Hill R (1952) The preparation and properties of aucubin, asperuloside and some related glycosides. Biochem J 50(3):310–319

    CAS  Google Scholar 

  16. Petrichenko VM, Sukhinina TV, Babiyan LK, Shramm NI (2006) Chemical composition and antioxidant properties of biologically active compounds from Euphrasia brevipila. Pharm Chem J 40(6):312–316

    Article  CAS  Google Scholar 

  17. Taylor BA, Phillips SJ (1996) Detection of obesity QTLs on mouse chromosomes 1 and 7 by selective DNA pooling. Genomics 34(3):389–398

    Article  CAS  Google Scholar 

  18. Christie WW (1993) Preparation of lipid extracts from tissues. Adv Lipid Methodol 2:195–213

    Google Scholar 

  19. Hu ML (1994) Measurement of protein thiol groups and glutathione in plasma. Methods Enzymol 233:380–385

    Article  CAS  Google Scholar 

  20. Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95(2):351–358

    Article  CAS  Google Scholar 

  21. Levine RL, Garland D, Oliver CN, Amici A, Climent I, Lenz AG, Ahn BW, Shaltiel S, Stadtman ER (1990) Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol 186:464–478

    Article  CAS  Google Scholar 

  22. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265–275

    CAS  Google Scholar 

  23. Placer ZA (1970) Lipid peroxidation in vivo. In: Nutrition proceedings of the eighth international congress. Excerpta Medica, Amsterdam, pp 100–105

  24. Kim RS, LaBella FS (1987) Comparison of analytical methods for monitoring autoxidation profiles of authentic lipids. J Lipid Res 28(9):1110–1117

    CAS  Google Scholar 

  25. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7(9):405–410

    Article  CAS  Google Scholar 

  26. Okorodudu DO, Jumean MF, Montori VM, Romero-Corral A, Somers VK, Erwin PJ, Lopez-Jimenez F (2010) Diagnostic performance of body mass index to identify obesity as defined by body adiposity: a systematic review and meta-analysis. Int J Obes (Lond) 34(5):791–799

    Article  CAS  Google Scholar 

  27. Enriori PJ, Evans AE, Sinnayah P, Cowley MA (2006) Leptin resistance and obesity. Obesity (Silver Spring) 14(s5):254–258

    Google Scholar 

  28. Maury E, Brichard SM (2010) Adipokine dysregulation, adipose tissue inflammation and metabolic syndrome. Mol Cell Endocrinol 314(1):1–16

    Article  CAS  Google Scholar 

  29. Keaney JF Jr, Larson MG, Vasan RS, Wilson PW, Lipinska I, Corey D, Massaro JM, Sutherland P, Vita JA, Benjamin EJ; Framingham Study (2003) Obesity and systemic oxidative stress: clinical correlates of oxidative stress in the Framingham Study. Arterioscler Thromb Vasc Biol 23(3):434–439

  30. DeLany JP, Windhauser MM, Champagne CM, Bray GA (2000) Differential oxidation of individual dietary fatty acids in humans. Am J Clin Nutr 72(4):905–911

    CAS  Google Scholar 

  31. Heim KE, Tagliaferro AR, Bobilya DJ (2002) Flavonoid antioxidants: chemistry, metabolism and structure-activity relationships. J Nutr Biochem 13(10):572–584

    Article  CAS  Google Scholar 

  32. Tundis R, Loizzo MR, Menichini F, Statti GA, Menichini F (2008) Biological and pharmacological activities of iridoids: recent developments. Mini Rev Med Chem 8(4):399–420

    Article  CAS  Google Scholar 

  33. Kadoma Y, Fujisawa S (2008) A comparative study of the radical-scavenging activity of the phenolcarboxylic acids caffeic acid, p-coumaric acid, chlorogenic acid and ferulic acid, with or without 2-mercaptoethanol, a thiol, using the induction period method. Molecules 13(10):2488–2499

    Article  CAS  Google Scholar 

  34. Hagerman AE, Riedl KM, Jones GA, Sovik KN, Ritchard NT, Hartfield PW, Riechel TL (1998) High molecular weight plant polyphenolics (tannins) as biological antioxidants. J Agric Food Chem 46:1887–1892

    Article  CAS  Google Scholar 

  35. Henson DE, Block G, Levine M (1991) Ascorbic acid: biologic functions and relation to cancer. J Natl Cancer Inst 83(8):547–550

    Article  CAS  Google Scholar 

  36. Srivastava SK, Yadav UC, Reddy AB, Saxena A, Tammali R, Shoeb M, Ansari NH, Bhatnagar A, Petrash MJ, Srivastava S, Ramana KV (2011) Aldose reductase inhibition suppresses oxidative stress-induced inflammatory disorders. Chem Biol Interact 191(1–3):330–338

    Article  CAS  Google Scholar 

  37. Vinayagamoorthi R, Bobby Z, Sridhar MG (2008) Antioxidants preserve redox balance and inhibit c-Jun-N-terminal kinase pathway while improving insulin signaling in fat-fed rats: evidence for the role of oxidative stress on IRS-1 serine phosphorylation and insulin resistance. J Endocrinol 197(2):287–296

    Article  CAS  Google Scholar 

  38. Maizels RM, Allen JE (2011) Immunology. Eosinophils forestall obesity. Science 332(6026):186–187

    Article  CAS  Google Scholar 

  39. Paoli P, Cirri P, Caselli A, Ranaldi F, Bruschi G, Santi A, Camici G (2013) The insulin-mimetic effect of Morin: a promising molecule in diabetes treatment. Biochim Biophys Acta 1830(4):3102–3111

    Article  CAS  Google Scholar 

  40. Cushnie TP, Lamb AJ (2005) Antimicrobial activity of flavonoids. Int J Antimicrob Agents 26(5):343–356

    Article  CAS  Google Scholar 

  41. Davini E, Javarone C, Trogolo C, Aureli P, Pasolini B (1986) The quantitative isolation and antimicrobial activity of the aglycone of aucubin. Phytochemistry 25(10):2420–2422

    Article  CAS  Google Scholar 

  42. Fu J, Cheng K, Zhang ZM, Fang RQ, Zhu HL (2010) Synthesis, structure and structure-activity relationship analysis of caffeic acid amides as potential antimicrobials. Eur J Med Chem 45(6):2638–2643

    Article  CAS  Google Scholar 

  43. Cani PD, Bibiloni R, Knauf C, Waget A, Neyrinck AM, Delzenne NM, Burcelin R (2008) Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes 57(6):1470–1481

    Article  CAS  Google Scholar 

  44. Phoem AN, Voravuthikunchai SP (2012) Growth stimulation/inhibition effect of medicinal plants on human intestinal microbiota. Food Sci Biotechnol 21(3):739–745

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alexey A. Tinkov.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tinkov, A.A., Nemereshina, O.N., Popova, E.V. et al. Plantago maxima leaves extract inhibits adipogenic action of a high-fat diet in female Wistar rats. Eur J Nutr 53, 831–842 (2014). https://doi.org/10.1007/s00394-013-0587-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00394-013-0587-6

Keywords

Navigation