Skip to main content
SpringerLink
Log in

A pharmacological investigation of Hippophae salicifolia (HS) and Hippophae rhamnoides turkestanica (HRT) against multiple stress (C-H-R): an experimental study using rat model

  • Original Paper
  • Published:
Cell Stress and Chaperones Aims and scope

Abstract

Hippophae salicifolia (HS) and Hippophae rhamnoides turkestanica (HRT) are abundantly found species of Hippophae in Himalayan region of India. As these plants thrive under extreme climatic conditions, it is suspected that these plants must have a unique adaptogenic property against high-altitude stress. To keeping these views in our mind, the present study was planned to evaluate the mechanism of action of aqueous extract of HS and aqueous extract of HRT against multiple stress [cold-hypoxia-restraint (C-H-R)] for their adaptogenic activity. The present study reported the adaptogenic activity of HS in facilitating tolerance to multiple stress, CHR in rats. Pre-treatment with aqueous extract of HS significantly attenuated reactive oxygen species (ROS) production, protein oxidation, and lipid peroxidation and also showed role in maintaining antioxidant status as similar to control rats. Since protein oxidation was decreased by pre-treatment of HS, protein homeostasis was also sustained by regulation of heat shock proteins (HSP70 and HSP60). Interestingly, heme oxygenase-1 (HO-1), Vascular Endothelial Growth Factor (VEGF), and nitric oxide (NO) level was also increased in HS pre-treated rats depicted its adaptogenic activity against multiple stress, CHR. Conclusively, aqueous extract of HS could use an adaptogen for high altitude-associated multiple stress (CHR).

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
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Anyasor GN, Ogunwenmo KO, Oyelana OA, Akpofunure BE (2010) Phytochemical constituents and antioxidant activities of aqueous and methanol stem extracts of Costus afer Ker Gawl. (Costaceae). Afr J Biotechnol 9:4880–4884

    CAS  Google Scholar 

  • Askew EW (1995) Environmental and physical stress and nutrient requirements. Am J Clin Nutr 61:631S–637S

    CAS  PubMed  Google Scholar 

  • Askew EW (1997) Nutrition and performance in hot, cold, and high altitude environments. In: Wolinsky I (ed) Nutrition in exercise and sport, 3rd edn. CRC Press, Boca Raton, pp 597–619

    Google Scholar 

  • Beckman RP, Mizzen LA, Welch WJ (1990) Interaction of HSP70 with newly synthesized proteins: implications for protein folding and assembly. Science 248:850–854

    Article  Google Scholar 

  • Beveridge T, Li TSC, Oomah BD, Smith A (1999) Seabuckthorn products: manufacture and composition. J Agric Food Chem 47:3480–3488

    Article  CAS  PubMed  Google Scholar 

  • Blau HM, Banfi A (2001) The well-tempered vessel. Nat Med 7:532–534

    Article  CAS  PubMed  Google Scholar 

  • Boucher JL, Moali C, Tenu JP (1999) Nitric oxide biosynthesis, nitric oxide synthase inhibitors and arginase competition for L-arginine utilization. Cell Mol Life Sci 55:1015–1028

    Article  CAS  PubMed  Google Scholar 

  • Brero A, Ramella R, Fitou A, Dati C, Alloatti G, Gallo MP (2010) Neuregulin-1beta1 rapidly modulates nitric oxide synthesis and calcium handling in rat cardiomyocytes. Cardiovasc Res 88:443–452

    Article  CAS  PubMed  Google Scholar 

  • Carmeliet P, Jain RK (2000) Angiogenesis in cancer and other diseases. Nature 407:249–257

    Article  CAS  PubMed  Google Scholar 

  • Cathcart R, Schwiers E, Ames BN (1983) Detection of pico mole levels of hyderoperoxides using fluorescent dichlorofluoroscein assay. Anal Biochem 134:111–116

    Article  CAS  PubMed  Google Scholar 

  • Chiang HL, Terlecky SR, Plant CP, Dice JF (1989) A role for a 70-kilodalton heat shock protein in lysosomal degradation of intracellular proteins. Science 246:382–385

    Article  CAS  PubMed  Google Scholar 

  • Connolly DT (1991) Vascular permeability factor: a unique regulator of blood vessel function. J Cell Biochem 47(3):219–223

    Article  CAS  PubMed  Google Scholar 

  • Connolly DT, Heuelman DM, Nelson R, Olander JV, Eppley BL, Delfino JJ, Siegel NR, Limgruber RM, Feder J (1989) Tumor vascular permeability factor stimulates endothelial cell growth and angiogenesis. J Clin Invest 84:1470–1478

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Day AJ, Williamson G (2001) Biomarkers for exposure to dietary flavonoids: a review of the current evidence for identification of quercetin glycosides in plasma. Br J Nutr 86:S105–S110

    Article  CAS  PubMed  Google Scholar 

  • Dong DL, Zhang Y, Lin DH, Chen J, Patschan S, Goligorsky MS, Nasjletti A, Yang BF, Wang WH (2007) Carbon monoxide stimulates the Ca2_ activated big conductance K channels in cultured human endothelial cells. Hypertension 50:643–651

    Article  CAS  PubMed  Google Scholar 

  • Eccleston C, Baoru Y, Tahvonen R, Kallio H, Rimbach GH, Minihane AM (2002) Effects of an antioxidant-rich juice (sea-buckthorn) on risk factors for coronary heart disease in humans. J Nut Biochem 13:346–354

    Article  CAS  Google Scholar 

  • Fandrey J (2004) Oxygen-dependent and tissue-specific regulation of erythropoietin gene expression. Am J Physiol Regul Integr Comp Physiol 286(6):R977–R988

    Article  CAS  PubMed  Google Scholar 

  • Forsythe JA, Jiang BH, Iyer NV, Agani F, Leung SW, Koos RD, Semenza GL (1996) Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol 16(9):4604–4613

    CAS  PubMed Central  PubMed  Google Scholar 

  • Geetha S, Sairam M, Mongia SS, Singh V, Ilavazhagan G, Sawhney RC (2003) Evaluation of antioxidant activity of leaf extract of sea-buckthorn (Hippophae rhamnoides L.) on chromium(VI) induced oxidative stress in albino rats. J Ethnopharmacol 87:247–251

    Article  CAS  PubMed  Google Scholar 

  • Goyal AK, Basistha BC, Sen A, Middha SK (2011) Antioxidant profiling of Hippophae salicifolia growing in sacred forests of Sikkim, India. Funct Plant Biol 38:697–701

    Article  CAS  Google Scholar 

  • Hazel JR (1995) Thermal adaptation in biological membranes: is homeoviscous adaptation the explanation? Annu Rev Physiol 57:19–42

    Article  CAS  PubMed  Google Scholar 

  • Hissin PJ, Hilf R (1973) A fluorometric method for the determination of oxidized and reduced glutathione in tissue. Anal Biochem 74:214–226

    Article  Google Scholar 

  • Hu B, Tomita M (2007) The Hsp70 chaperone system maintains high concentrations of active proteins and suppresses ATP consumption during heat shock. Syst Synth Biol 1(1):47–58

    Article  PubMed Central  PubMed  Google Scholar 

  • Hu B, Mayer MP, Tomita M (2006) Modeling HSP70-mediated protein folding. Biophys J 91(2):496–507

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hunt C, Morimoto RI (1985) Conserved features of eukaryotic hsp70 genes revealed by comparison with the nucleotide sequence of human hsp70. Proc Natl Acad Sci U S A 82:6455

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ilavazhagan G, Bansal A, Prasad D, Thomas P, Sharma SK, Kain AK, Kumar D, Selvamurthy W (2001) Effect of vitamin E supplementation on hypoxia-induced oxidative damage in male albino rats. Aviat Space Environ Med 72:899–903

    CAS  PubMed  Google Scholar 

  • Joanny P, Steinberg J, Robach P, Richalet JP, Gortan C, Gardette B, Jammes Y (2001) Operation Everest III (Comex’97): the effect of simulated sever hypobaric hypoxia on lipid peroxidation and antioxidant defence systems in human blood at rest and after maximal exercise. Resuscitation 49:307–314

    Article  CAS  PubMed  Google Scholar 

  • Jung HJ, Yang MZ, Kwon KH, Yenari MA, Choi YJ, Lee WT (2010) Endogenous agmatine inhibits cerebral vascular matrix metalloproteinases expression by regulating activating transcription factor 3 and endothelial nitric oxide synthesis. Curr Neurovasc Res 7:201–212

    Article  CAS  PubMed  Google Scholar 

  • Kakkar P, Das B, Viswanathan PN (1984) A modified spectrophotometric assay of superoxide dismutase. Indian J Biochem Biophys 21:130–132

    CAS  PubMed  Google Scholar 

  • Kostic DA, Mitic SS, Mitic MN, Zarubica AR, Velickovic JM, Dordevic AS, Randelovic SS (2010) Phenolic contents, antioxidant and antimicrobial activity of Papaver rhoeas L. extracts from southeast Serbia. J Med Plant Res 4:1727–1732

    CAS  Google Scholar 

  • LeBel CP, Ischiropoulos H, Bondy SC (1992) Evaluation of the probe 2′,7′-dichlorofluorescein as an indicator of reactive oxygen species formation and oxidative stress. Chem Res Toxicol 5:227–231

    Article  CAS  PubMed  Google Scholar 

  • Levett DZ, Fernandez BO, Riley HL, Martin DS, Mitchell K, Leckstrom CA, Ince C, Whipp BJ, Mythen MG, Montgomery HE, Grocott MP, Feelisch M (2011) The role of nitrogen oxides in human adaptation to hypoxia. Sci Rep 1:109. doi:10.1038/srep00109

    Article  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Levine RL, Williams J, Stadtman ER, Shacter E (1994) Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol 233:346–57

  • Levy AP, Levy NS, Wegner S, Goldberg MA (1995) Transcriptional regulation of the rat vascular endothelial growth factor gene by hypoxia. J Biol Chem 270(22):13333–13340

    Article  CAS  PubMed  Google Scholar 

  • Li H, Wang Z, Liu Y (2003) Review in the studies on tannins activity of cancer prevention and anticancer. Zhong Yao Cai 26:444–448

    PubMed  Google Scholar 

  • Lu R (1992) Seabuckthorn: a multipurpose plant species for fragile mountains. ICIMOD Occasional Paper No. 20, Kathmandou, Nepal; p 62

  • MacMillan-Crow LA, Crow JP, Thompson JA (1998) Peroxynitrite-mediated inactivation of manganese superoxide dismutase involves nitration and oxidation of critical tyrosine residues. Biochem 37:1613–1622

  • Mohanraj P, Merola AJ, Wright VP, Clanton TL (1998) Antioxidants protect rat diaphragmatic muscle function under hypoxic conditions. J Appl Physiol 84:1960–1966

    CAS  PubMed  Google Scholar 

  • Moncada S, Palmer RM, Higgs EA (1991) Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev 43(2):109–142

    CAS  PubMed  Google Scholar 

  • Morimoto RI (1998) Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev 12(24):3788–3796

    Article  CAS  PubMed  Google Scholar 

  • Morimoto RI, Kline MP, Bimston DN, Cotto JJ (1997) The heat-shock response: regulation and function of heat-shock proteins and molecular chaperones. Essays Biochem 32:17–29

    CAS  PubMed  Google Scholar 

  • Negi PS, Chauhan AS, Sadia GA, Rohinishree YS, Ramteke RS (2005) Antioxidant and antibacterial activities of various sea-buckthorn (Hippophae rhamnoides L.) seed extracts. Food Chem 92:119–124

    Article  CAS  Google Scholar 

  • Ollinger R, Yamashita K, Bilban M, Erat A, Kogler P, Thomas M, Csizmadia E, Usheva A, Margreiter R, Bach FH (2007) Bilirubin and biliverdin treatment of atherosclerotic diseases. Cell Cycle 6:39–43

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Pant M, Lal A, Rani A (2014) Hippophae salcifolia D Don-A plant with multifarious benefits. Int J Pharm Pharm Sci 6(11):37–40

    Google Scholar 

  • Paula FBA, Gouvea CMCP, Alfredo PP, Salgado I (2005) Protective action of a hexane crude extract of pterodon emarginatus fruits against oxidative and nitrosative stress induced by acute exercise in rats. BMC Complement Altern Med 5:17

    Article  PubMed Central  PubMed  Google Scholar 

  • Polla BS, Kantengwa S, Francois D, Salvioli S, Franceschi C, Marsac C (1996) Mitochondria are selective targets for the protective effects of heat shock against oxidative injury. Proc Natl Acad Sci 93:6458–6463

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Radak Z, Asano K, Lee KC, Ohno H, Nakamura A, Nakamoto H, Goto S (1997) High altitude training increases reactive carbonyl derivatives but not lipid peroxidation in skeletal muscle of rats. Free Radic Biol Med 22:1109–1114

    Article  CAS  PubMed  Google Scholar 

  • Ramachandran U, Divekar HM, Grover SK, Srivastava KK (1990) New experimental model for evaluation of adaptogenic products. J Ethnopharmacol 29:275–281

    Article  CAS  PubMed  Google Scholar 

  • Ranjith A, Kumar SK, Venugopalan VV, Arumughan C, Sawhney RC, Singh V (2006) Fatty acids, tocols and carotenoids in pulp oil of three Sea Buckthron species (Hippophae rhamnoides, H. salicifolia, and H. tibetana) grown in the Indian Himalayas. JAOCS 83:359–364

    CAS  Google Scholar 

  • Rongsen L (1992) Sea-buckthorn a multipurpose plant species for fragile mountain. ICIMOD Occasional paper no. 20. ICIMOD, Katmandu, Nepal

  • Setchell KD, Faughnan MS, Avades T, Zimmer-Nechemias L, Brown NM (2003) Comparing the pharmacokinetics of daidzein and genistein with the use of 13C-labeled tracers in premenopausal women. Am J Clin Nutr 77:411–419

    CAS  PubMed  Google Scholar 

  • Sharma P, Suryakumar G, Singh V, Misra K, Singh SB (2014) In vitro antioxidant profiling of seabuckthorn varieties and their adaptogenic response to high altitude-induced stress. Int J Biometeorol 58(8). doi:10.1007/s00484-014-0925-2

  • Singh V (2001) Seabuckthorn (Hippophae L.) A wonder plant of dry and temperate Himalayas. Department of Agro forestery and Environment, Himachal Pradesh Agriculture university, Palampur; p 1760-62

  • Sinha AK (1972) Colorimetric assay of catalase. Anal Biochem 47:389–394

    Article  CAS  PubMed  Google Scholar 

  • Stadtman ER (1993) Oxidation of free amino acids and amino acid residues in proteins by radiolysis and by metal-catalyzed reactions. Annu Rev Biochem 62:797–821

    Article  CAS  PubMed  Google Scholar 

  • Tenhunen R, Marver HS, Schmid R (1968) The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase. Proc Natl Acad Sci 61:748–755

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang R, Wu L (1997) The chemical modification of KCa channels by carbon monoxide in vascular smooth muscle cells. J Biol Chem 272:8222–8226

    Article  CAS  PubMed  Google Scholar 

  • Wang R, Wang Z, Wu L, Hanna ST, Peterson-Wakeman R (2001) Reduced vasorelaxant effect of carbon monoxide in diabetes and the underlying mechanisms. Diabetes 50:166–174

    Article  CAS  PubMed  Google Scholar 

  • Wink DA, Miranda KM, Espey MG, Pluta RM, Hewett SJ, Colton C, Vitek M, Feelisch M, Grisham MB (2001) Mechanisms of the antioxidant effects of nitric oxide. Antioxid Redox Signal 3(2):203–213

    Article  CAS  PubMed  Google Scholar 

  • Witko-Sarsat V, Friedlander M, Capeillere-Blandin C, Nguyen-Khoa T, Nguyen AT, Zingraff J, Jungers P, Descamps-Latscha B (1996) Advanced oxidation protein products as a novel marker of oxidative stress in uremia. Kidney Int 49:1304–1313

    Article  CAS  PubMed  Google Scholar 

  • Xing C (2003) Health protection and processing technology of seabuckthorn tea: In: Singh V editor. Seabuckthorn (Hippophae L.)-A multipurpose wonder plant, Indus Publishing Company; p 475–8

  • Xu L, Giffard RG (1997) HSP70 protects murine astrocytes from glucose deprivation injury. Neurosci Lett 224:9–12

    Article  CAS  PubMed  Google Scholar 

  • Yamakura F, Taka H, Fujimura T, Murayama K (1998) Inactivation of human manganese-superoxide dismutase by peroxynitrite is caused by exclusive nitration of tyrosine 34 to 3-nitrotyrosine. J Biol Chem 273:14085–14089

  • Yoshida T, Maulik N, Ho YS, Alam J, Das DK (2001) Hmox-1 constitutes an adaptive response to effect antioxidant cardioprotection. Circulation 103:1695–1701

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Authors thank Dr. Shashi Bala Singh, Director of the Establishment for her support and encouragement.

Conflict of interest

The authors have declared that no competing interests exist.

Author information

Authors and Affiliations

  1. Defence Institute of Physiology and Allied Sciences (DIPAS), Lucknow Road, Timarpur, Delhi, 110054, India

    Richa Rathor, Priyanka Sharma, Geetha Suryakumar & Lilly Ganju

Authors
  1. Richa Rathor
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Priyanka Sharma
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Geetha Suryakumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lilly Ganju
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Richa Rathor.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rathor, R., Sharma, P., Suryakumar, G. et al. A pharmacological investigation of Hippophae salicifolia (HS) and Hippophae rhamnoides turkestanica (HRT) against multiple stress (C-H-R): an experimental study using rat model. Cell Stress and Chaperones 20, 821–831 (2015). https://doi.org/10.1007/s12192-015-0603-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12192-015-0603-2

Keywords

Search

Navigation