Skip to main content
SpringerLink
Log in

Fucoxanthin restrains oxidative stress induced by retinol deficiency through modulation of Na+Ka+-ATPase and antioxidant enzyme activities in rats

  • ORIGINAL CONTRIBUTION
  • Published:
European Journal of Nutrition Aims and scope Submit manuscript

An Erratum to this article was published on 01 April 2009

Abstract

Background

Retinol deficiency is a major public health problem world wide, affecting children and women, in particular. It causes a variety of disorders in the body affecting various cellular functions.

Aim of the study

To study the effect of fucoxanthin (FUCO), a non-provitamin-A carotenoid in comparison with retinol (ROH) on changes in antioxidant molecules, lipid peroxidation and membrane bound enzymes in tissue and microsomes, induced by ROH deficiency in rats.

Methods

After induction of ROH deficiency by feeding a diet devoid of ROH for 8 weeks, rats were divided into two groups (n = 20/group) and administered orally a dose of either FUCO (0.83 µmol) or ROH (0.87 µmol). A group of ROH deficient rats (n = 5) and rats (n = 5) fed with ROH sufficient diet was considered as baseline and control groups respectively. Over a period of 8 h, activity of catalase (CAT), glutathione transferase (GST), level of lipid peroxidation (LPx), fatty acids in plasma, liver and liver microsomes and activity of Na+K+-ATPase in liver microsomes were evaluated.

Results

ROH restriction increased LPx (P < 0.05) in liver (~19%) and plasma (~34%) while the activities of CAT (90 ± 1%) and GST (17 ± 4%) decreased compared to control. Significant elevation (91%) was observed for Na+K+-ATPase activity in liver microsomes of ROH deficient when compared to control group and levels were lowered on administration of ROH (37–69%) and FUCO (51–57%), towards control over a period of 8 h. ROH and FUCO suppressed (P < 0.05) the LPx level (%) in plasma (34–62, 7–85), liver homogenate (9–71, 24–72) and liver microsomes (83–92, 61–87), while the activities of CAT in plasma (89–97%, 91–95%) and liver microsomes (84–93%, 85–93%) and GST in liver homogenate (43–53%, 44–51%) and liver microsomes (36–52%, 22–51%) were increased (P < 0.05) compared to ROH deficient group.

Conclusions

Results show that FUCO, a non-provitamin-A carotenoid protects cell membrane by modulating Na+K+-ATPase (51–57% lowering) and the activities of CAT and GST at the tissue and microsomal level which are affected by ROH deficiency. This may be due to its antioxidant nature. These in turn reduce LPx caused by ROH deficiency.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Aebi H (1984) Catalase in vitro. In: Packer L (ed) Oxygen radicals in biological systems. Methods Enzymol, Academic Press Inc., Orlando, 105:121–126

  2. American Institute of Nutrition (1977) Report of the American Institute of Nutrition Ad. Hoc Committee on standards for nutritional studies. J Nutr 170:1340–1348

    Google Scholar 

  3. Ames BN (1966) Assay of inorganic phosphate, total phosphate and phosphatases. In: Neufeld EF, Ginsburg V (eds) Complex carbohydrates. Methods Enzymol, Academic Press Inc., New York, 8:115–118

  4. Anzulovich AC, Oliveros BL, Munoz E, Martinez LD, Gimenez MS (2000) Nutritional vitamin A deficiency alters antioxidant defenses and modifies the liver histoarchitecture in rat. J Trace Elem Exp Med 13:343–357

    Article  CAS  Google Scholar 

  5. Asai A, Sugawara T, Ono H, Nagao A (2004) Biotransformation of fucoxanthinol into amarouciaxanthin in mice and HEPG2 cells: formation and cytotoxicity of fucoxanthin metabolites. Drug Metabol Disp 32:205–211

    Article  CAS  Google Scholar 

  6. Barber T, Borras E, Torres L, Garcia C, Cabezuelo F, Lloret A, Pallardo FV, Vina JR (2000) Vitamin A deficiency causes oxidative damage to liver mitochondria in rats. Free Rad Biol Med 29:1–7

    Article  CAS  Google Scholar 

  7. Bhosale P, Bernstein PS (2005) Synergistic effects of zeaxanthin and its binding protein in the prevention of lipid membrane oxidation. Biochem Biophys Acta 1740:116–121

    CAS  Google Scholar 

  8. Chandini SK, Ganesan P, Bhaskar N (2008) In-vitro antioxidant activities of three selected brown seaweeds of India. Food Chem 107:707–713

    Article  CAS  Google Scholar 

  9. Ciaccio M, Valenza M, Tesoriere L, Bongiorno A, Albiero R, Livrea MA (1993) Vitamin A inhibits doxorubicin-induced membrane lipid peroxidation in rat tissues in vivo. Arch Biochem Biophys 302:103–108

    Article  CAS  Google Scholar 

  10. Fang YZ, Yan Wu G (2002) Free radicals, antioxidants, and nutrition. Nutrition 18:872–879

    Article  CAS  Google Scholar 

  11. Gatica L, Alvarez S, Gomez N, Zago MP, Oteiza P, Oliveros L, Gimenez MS (2005) Vitamin A deficiency induces prooxidant environment and inflammation in rat aorta. Free Rad Res 39:621–628

    Article  CAS  Google Scholar 

  12. Gluthenberg C, Alin P, Mannervik B (1985) Glutathione transferase from rat testis. In: Meister A (ed) Glutamate, glutamine, glutathione and related compounds. Methods Enzymol, Academic Press Inc., Orlando, 113:507–510

  13. Grolier P, Cisti A, Danbeze M, Narbonne JF (1991) The influence of dietary vitamin A intake on microsomal membrane fluidity and lipid composition. Nutr Res 11:567–574

    Article  CAS  Google Scholar 

  14. Hamm MW, Chan V, Wolf G (1987) Liver microsomal membrane fluidity and lipid characteristics in vitamin A deficient rats. Biochem J 245:907–910

    CAS  Google Scholar 

  15. Haugan JA, Akermann T, Jensen LS (1992) Isolation of fucoxanthin and peridinin. In: Packer L (ed) Carotenoids part A: chemistry, separation, quantitation and antioxidants: Methods in enzymology. Academic Press Inc., Orlando, 213:231–245

  16. Kang HW, Bhimidi GR, Odom DP, Brun PJ, Fernandez ML, McGrane MM (2007) Altered lipid catabolism in the vitamin A deficient liver. Mol Cell Endocrinol 271:18–27

    Article  CAS  Google Scholar 

  17. Kaplay SS (1978) Erythrocyte membrane Na+ and K+ activated adenosine triphosphatase in PCM. J Clin Nutr 31:579–584

    CAS  Google Scholar 

  18. Kaul S, Krishnakantha TP (1997) Influence of retinol deficiency and curcumin/turmeric feeding on tissue microsomal membrane lipid peroxidation and fatty acids in rats. Mol Cell Biochem 175:43–48

    Article  CAS  Google Scholar 

  19. Kotake-Nara E, Kushiro M, Zhang H, Sugawara T, Miyashita K, Nagao A (2001) Carotenoids affect proliferation of human prostate cancer cells. J Nutr 131:3303–3306

    CAS  Google Scholar 

  20. Lowry OH, Rosebrough WJ, Farr AL, Randall RS (1951) Protein measurement with folin phenol reagent. J Biol Chem 193:265–275

    CAS  Google Scholar 

  21. Matsuno T (1991) Xanthophylls as precursors of retinoids. Pure Appl Chem 1:81–88

    Article  Google Scholar 

  22. Morrison WR, Smith LM (1964) Preparation of fatty acid methyl esters and dimethylacetals from boron fluoride-methanol. J Lipid Res 5:600–608

    CAS  Google Scholar 

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

    Article  Google Scholar 

  24. Oliveros L, Vega V, Anzulovich AC, Ramirez D, Giminez M (2000) Vitamin A deficiency modifies antioxidant defenses and essential element contents in rat heart. Nutr Res 20:1139–1150

    Article  CAS  Google Scholar 

  25. Palacios A, Piergiacomi VA, Catala A (1996) Vitamin A supplementation inhibits chemiluminescence and lipid peroxidation in isolated rat liver microsomes and mitochondria. Mol Cell Biochem 154:77–82

    Article  CAS  Google Scholar 

  26. Rauchora H, Redvinkora J, Kalous M, Drahota Z (1995) The effect of lipid peroxidation on the activity of various membrane bound ATPase in rat kidney. Int J Biochem Cell Biol 27:251–255

    Article  Google Scholar 

  27. Ross AC (1999) Vitamin A. In: Maurice S, James O, Moshe S Catharine Ross A (eds) Modern nutrition in health and disease, 9th edn. Williams & Wilkins, Baltimore, p 305–313

  28. Sachindra NM, Sato E, Maeda H, Hosokawa M, Niwano Y, Kohno M, Miyashita K (2007) Radical scavenging and singlet oxygen quenching activity of marine carotenoid fucoxanthin and its metabolites. J Agric Food Chem 55:8516–8522

    Article  CAS  Google Scholar 

  29. Selvendrian K, Singh PVJ, Krishnan BK, Sakthisekaran D (2003) Cytoprotective effect of piperine against benzo(a)pyrene induced experimental lung cancer in Swiss albino mice with reference to lipid peroxidation and antioxidant enzymes. Fitoterapia 74:198–205

    Article  Google Scholar 

  30. Statsoft (1999) Statistics for Windows. Statsoft Inc., USA

    Google Scholar 

  31. Sugawara T, Baskaran V, Tsuzuki W, Nagao A (2002) Brown algae fucoxanthin is hydrolyzed to fucoxanthinol during absorption by caco-2 human intestinal cells and mice. J Nutr 132:946–951

    CAS  Google Scholar 

  32. Sujak A, Gabrielska J, Grudzinski W, Borc R, Mazurek P, Gruszecki WI (1999) Lutein and zeaxanthin as protectors of lipid membranes against oxidative damage: the structural aspects. Arch Biochem Biophys 371:301–307

    Article  CAS  Google Scholar 

  33. Yehuda G, Shamir YK (1971) Effect of urea sodium and calcium on microsomal ATPase activity in different parts of the kidney. Biochem Biophys Acta 233:133–136

    Article  Google Scholar 

Download references

Acknowledgement

This work was supported by the Department of Biotechnology, Govt. of India, for partial funding (Grant # BT/PR-6045/PID/20/227/2005). The first author acknowledges the grant of Research Fellowship by The University Grant Commission, India. Authors acknowledge the help of Ms. Asha M and Mr. Mukund PL in chromatographic analyses.

Author information

Authors and Affiliations

  1. Dept. of Biochemistry and Nutrition, Central Food Technological Research Institute, CSIR, Mysore, 570 020, Karnataka, India

    Ravi Kumar Sangeetha & Vallikannan Baskaran

  2. Dept. of Meat, Fish and Poultry Technology, Central Food Technological Research Institute, Mysore, India

    Narayan Bhaskar

Authors
  1. Ravi Kumar Sangeetha
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Narayan Bhaskar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Vallikannan Baskaran
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Vallikannan Baskaran.

Additional information

An erratum to this article is available at http://dx.doi.org/10.1007/s00394-009-0782-7.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ravi Kumar, S., Narayan, B. & Vallikannan, B. Fucoxanthin restrains oxidative stress induced by retinol deficiency through modulation of Na+Ka+-ATPase and antioxidant enzyme activities in rats. Eur J Nutr 47, 432–441 (2008). https://doi.org/10.1007/s00394-008-0745-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00394-008-0745-4

Keywords

Search

Navigation