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Probiotic Dahi containing Lactobacillus acidophilus and Bifidobacterium bifidum alleviates age-inflicted oxidative stress and improves expression of biomarkers of ageing in mice

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Abstract

The potential benefiting effects of probiotic Dahi on age-inflicted accumulation of oxidation products, antioxidant enzymes and expression of biomarkers of ageing were evaluated in mice. Probiotic Dahi were prepared by co-culturing in buffalo milk (3% fat) Dahi bacteria (Lactococcus lactis ssp. cremoris NCDC-86 and Lactococcus lactis ssp. lactis biovar diacetylactis NCDC-60) along with selected strain of Lactobacillus acidophilus LaVK2 (La-Dahi) or combined L. acidophilus and Bifidobacterium bifidum BbVK3 (LaBb-Dahi). Four groups of 12 months old mice (6 each) were fed for 4 months supplements (5 g/day) of buffalo milk (3% fat), Dahi, La-Dahi and LaBb-Dahi, respectively, with basal diet. The activities of catalase (CAT) and glutathione peroxidase (GPx) declined and the contents of oxidation products, thiobarbituric acid reactive substances (TBARS) and protein carbonyls, increased in red blood corpuscles (RBCs), liver, kidney and heart tissues and superoxide dismutase (SOD) activity increased in RBCs and hepatic tissues during ageing of mice. Feeding ageing mice with La-Dahi or LaBb-Dahi increased CAT activity in all the four tissues, and GPx activity in RBCs and hepatic tissue, and a significant decline in TBARS in plasma, kidney and hepatic tissues and protein carbonyls in plasma. Feeding mice with probiotic Dahi also reversed age related decline in expression of biomarkers of ageing, peroxisome proliferators activated receptor-α, senescence marker protein-30 (SMP-30) and klotho in hepatic and kidney tissues. The present study suggests that probiotic Dahi containing selected strains of bacteria can be used as a potential nutraceutical intervention to combat oxidative stress and molecular alterations associated with ageing.

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References

  1. Harman D (1956) Aging: a theory based on free radical and radiation chemistry. J Gerontol 11:298–300

    PubMed  CAS  Google Scholar 

  2. Cabalas-Picot I, Nicole A, Clement M, Bourke J, Signet P (1992) Age-related changes in antioxidant enzymes and lipid peroxidation, oxidative damage and aging in brains of control and transgenic mice overexpressing copper/zinc superoxide dismutase. Mutat Res 275:281–293. doi:10.1016/0921-8734(92)90032-K

    Google Scholar 

  3. Toyokuni S (1999) Reactive oxygen species-induced molecular damage and its application in pathology. Pathol Int 49:91–102. doi:10.1046/j.1440-1827.1999.00829.x

    Article  PubMed  CAS  Google Scholar 

  4. Poynter ME, Daynes RA (1998) Peroxisome proliferator-activated receptor a activation modulates cellular redox status, represses nuclear factor-kB signaling, and reduces inflammatory cytokine production in aging. J Biol Chem 273:32833–32841. doi:10.1074/jbc.273.49.32833

    Article  PubMed  CAS  Google Scholar 

  5. Jung KJ, Maruyama N, Ishigami A, Yu BP, Chung HY (2006) The redox-sensitive DNA binding sites responsible for age-related downregulation of SMP-30 by ERK pathway and reversal by calorie restriction. Antioxid Redox Signal 8:671–680. doi:10.1089/ars.2006.8.671

    Article  PubMed  CAS  Google Scholar 

  6. Shih PH, Yen GC (2007) Differential expressions of antioxidant status in aging rats: the role of transcriptional factor Nrf2 and MAPK signaling pathway. Biogerontology 8:71–80. doi:10.1007/s10522-006-9033-y

    Article  PubMed  CAS  Google Scholar 

  7. Metchnikoff E (1908) The prolongation of life. Putnam, New York

    Google Scholar 

  8. Korpela R, Peuhkuri K, Lahteenmaki T, Sievi E, Saxelin M, Vapaatalo H (1997) Lactobacillus rhamnosus GG shows antioxidative properties in vascular endothelial culture. Milchwissenschaft 52:503–505

    CAS  Google Scholar 

  9. Kullisaar T, Zilmer M, Mikelsaar M, Vihalemm T, Annuk H, Kairane C, Kilk A (2002) Two antioxidative lactobacilli strains as promising probiotics. Int J Food Microbiol 72:215–224. doi:10.1016/S0168-1605(01)00674-2

    Article  PubMed  CAS  Google Scholar 

  10. Rajpal S, Kansal VK (2008) Buffalo milk probiotic dahi containing Lactobacillus acidophilus, Bifidobacterium bifidum and Lactococcus lactis reduces gastrointestinal cancer induced by dimethylhydrazine dihydrochloride in rats. Milchwissenschaft 63:122–125

    CAS  Google Scholar 

  11. Rajpal S, Kansal VK (2009) Probiotic dahi containing Lactobacillus acidophilus and Bifidobacterium bifidum attenuates diet induced hypercholesterolemia in rats. Milchwissenschaft 64:21–25

    CAS  Google Scholar 

  12. Rajpal S, Kansal VK (2009) Probiotic dahi containing Lactobacillus acidophilus and Bifidobacterium bifidum stimulates immune system in mice. Milchwissenschaft 64:147–150

    CAS  Google Scholar 

  13. Kumar A, Singh NK, Sinha PR (2010) Inhibition of 1,2-dimethylhydrazine induced colon genotoxicity in rats by the administration of probiotic curd. Mol Biol Rep 37:1373–1376. doi:10.1007/s11033-009-9519-1

    Article  PubMed  CAS  Google Scholar 

  14. Kumar A, Singh NK, Sinha PR, Kumar R (2010) Intervention of Acidophilus-casei dahi and wheat bran against molecular alteration in colon carcinogenesis. Mol Biol Rep 37:621–627. doi:10.1007/s11033-009-9649-5

    Article  PubMed  CAS  Google Scholar 

  15. Yadav H, Jain S, Sinha PR (2008) Oral administration of dahi containing probiotic Lactobacillus acidophilus and Lactobacillus casei delayed the progression of streptozotocin-induced diabetes in rats. J Dairy Res 75:189–195. doi:10.1017/S0022029908003129

    Article  PubMed  CAS  Google Scholar 

  16. AOAC (2005) In: Horowitz W (eds) Official methods of analysis, vol 45, 18th edn. Association of Official Analytical Chemists, Gaithersburg, pp 75–76

  17. Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

    Article  PubMed  CAS  Google Scholar 

  18. Marklund S, Marklund G (1974) Involvement of superoxide dismutase anion radical in autooxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem 42:469–474. doi:10.1111/j.1432-1033.1974.tb03714.x

    Article  Google Scholar 

  19. Paglia DE, Valentine WN (1967) Studies on quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70:158–169

    PubMed  CAS  Google Scholar 

  20. Uchiyama M, Mihara M (1978) Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Anal Biochem 86:271–278. doi:10.1016/0003-2697(78)90342-1

    Article  PubMed  CAS  Google Scholar 

  21. Bejma J, Ji LL (1999) Aging and acute exercise enhance free radical generation in rat skeletal muscle. J Appl Physiol 87:465–470

    PubMed  CAS  Google Scholar 

  22. Levine RL, Garland D, Oliver CN, Amici A, Climent I, Lenz AG, Ahn BW, Shaltiel S, Stadtman E (1990) Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol 186:464–478. doi:10.1016/0076-6879(90)86141-H

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  24. Drabkin DL (1950) Spectrophotometric studies. XV. Hydration of macro sized crystals of human hemoglobin, and osmotic concentrations in red cells. J Biol Chem 185:231–245

    PubMed  CAS  Google Scholar 

  25. Niho N, Mutoh M, Takahashi M, Tsutsumi K, Sugimura T, Wakabayashi K (2005) Concurrent suppression of hyperlipidemia and intestinal polyp formation by NO-1886, increasing lipoprotein lipase activity in Min mice. Proc Natl Acad Sci USA 102:2970–2974. doi:10.1073/pnas.0500153102

    Article  PubMed  CAS  Google Scholar 

  26. Sobocanec S, Balog T, Sverko V, Marotti T (2005) Met-enkephalin modulation of age-related changes in red cell antioxidant status. Physiol Res 54:97–104

    PubMed  CAS  Google Scholar 

  27. Chipalkatti S, De AK, Aiyar AS (1983) Effect of diet restriction on some biochemical parameters related to aging in mice. J Nutr 113:944–950

    PubMed  CAS  Google Scholar 

  28. Yen TC, King KL, Lee HC, Yeh SH, Wei YH (1994) Age-dependent increase of mitochondrial DNA deletions together with lipid peroxides and superoxide dismutase in human liver mitochondria. Free Radic Biol Med 16:207–214. doi:10.1016/0891-5849(94)90145-7

    Article  PubMed  CAS  Google Scholar 

  29. Navarro-Arévalo A, Sánchez-del-Pino MJ (1998) Age and exercise-related changes in lipid peroxidation and superoxide dismutase activity in liver and soleus muscle tissues of rats. Mech Ageing Dev 104:91–102. doi:10.1016/S0047-6374(98)00061-X

    Article  PubMed  Google Scholar 

  30. Thomas RP, Guigneaux M, Wood T, Evers BM (2002) Age-associated changes in gene expression patterns in the liver. J Gastrointest Surg 6:445–453. doi:10.1016/S1091-255X(01)00010-5

    Article  PubMed  Google Scholar 

  31. Muchová J, Sustrová M, Garaiová I, Liptáková A, Blazícek P, Kvasnicka P, Pueschel S, Duracková Z (2001) Influence of age on activities of antioxidant enzymes and lipid peroxidation products in erythrocytes and neutrophils of Down syndrome patients. Free Radic Biol Med 31:499–508. doi:10.1016/S0891-5849(01)00609-8

    Article  PubMed  Google Scholar 

  32. Huang TT, Carlson EJ, Gillespie AM, Shi Y, Epstein CJ (2000) Ubiquitous overexpression of CuZn superoxide dismutase does not extend life span in mice. J Gerontol A Biol Sci Med Sci 55:B5–B9. doi:10.1093/gerona/55.1.B5

    Article  PubMed  CAS  Google Scholar 

  33. Wu S, Li Q, Du M, Li SY, Ren J (2007) Cardiac-specific overexpression of catalase prolongs lifespan and attenuates ageing-induced cardiomyocyte contractile dysfunction and protein damage. Clin Exp Pharmacol Physiol 34:81–87. doi:10.1111/j.1440-1681.2007.04540.x

    Article  PubMed  Google Scholar 

  34. Mutlu-Türkoğlu U, Ilhan E, Oztezcan S, Kuru A, Aykaç-Toker G, Uysal M (2003) Age-related increases in plasma malondialdehyde and protein carbonyl levels and lymphocyte DNA damage in elderly subjects. Clin Biochem 36:397–400. doi:10.1016/S0009-9120(03)00035-3

    Article  PubMed  Google Scholar 

  35. Navarro A, Gomez C, López-Cepero JM, Boveris A (2004) Beneficial effects of moderate exercise on mice aging: survival, behavior, oxidative stress, and mitochondrial electron transfer. Am J Physiol Regul Integr Comp Physiol 286:R505–R511. doi:10.1152/ajpregu.00208.2003

    Article  PubMed  CAS  Google Scholar 

  36. Vittorini S, Paradiso C, Donati A, Cavallini G, Masini M, Gori Z, Pollera M, Bergamini E (1999) The age-related accumulation of protein carbonyl in rat liver correlates with the age-related decline in liver proteolytic activities. J Gerontol A Biol Sci Med Sci 54:B318–B323. doi:10.1093/gerona/54.8.B318

    Article  PubMed  CAS  Google Scholar 

  37. Conconi M, Friguet B (1997) Proteasome inactivation upon aging and on oxidation-effect of HSP 90. Mol Biol Rep 24:45–50. doi:10.1023/A:1006852506884

    Article  PubMed  CAS  Google Scholar 

  38. Gemant A (1979) Inhibitors of oxidative degradation of protein: gerontological implications. Mol Biol Rep 4:203–206. doi:10.1007/BF00777554

    Article  PubMed  CAS  Google Scholar 

  39. Zommara M, Toubo H, Sakono M, Imaizumi K (1998) Prevention of peroxidative stress in rats fed on a low vitamin E containing diet by supplementing with a fermented bovine milk whey preparation: effect of lactic acid and β-lactoglobulin on the antiperoxidative action. Biosci Biotechnol Biochem 62:710–717. doi:10.1271/bbb.62.710

    Article  PubMed  CAS  Google Scholar 

  40. Lutgendorff F, Nijmeijer RM, Sandström PA, Trulsson LM, Magnusson KE, Timmerman HM, van Minnen LP, Rijkers GT, Gooszen HG, Akkermans LM, Söderholm JD (2009) Probiotics prevent intestinal barrier dysfunction in acute pancreatitis in rats via induction of ileal mucosal glutathione biosynthesis. PLoS One 4:e4512

    Article  PubMed  Google Scholar 

  41. Zommara M, Tachibana N, Sakono M, Suzuki Y, Oda T, Hashiba H, Imaizumi PhK (1996) Whey from cultured skim milk decreases serum cholesterol and increases antioxidant enzymes in liver and red blood cells in rats. Nutr Res 16:293–302. doi:10.1016/0271-5317(96)00013-9

    Article  CAS  Google Scholar 

  42. Yadav H, Jain S, Sinha PR (2007) Antidiabetic effect of probiotic dahi containing Lactobacillus acidophilus and Lactobacillus casei in high fructose fed rats. Nutrition 23:62–68. doi:10.1016/j.nut.2006.09.002

    Article  PubMed  Google Scholar 

  43. Sohal RS, Orr WC (1992) Relationship between antioxidants, prooxidants, and the aging process. Ann N Y Acad Sci 663:74–84. doi:10.1111/j.1749-6632.1992.tb38651.x

    Article  PubMed  CAS  Google Scholar 

  44. Michiels C, Raes M, Toussaint O, Remacle J (1994) Importance of Se-glutathione peroxidase, catalase and Cu/Zn-SOD for cell survival against oxidative stress. Free Radic Biol Med 17:235–248. doi:10.1016/0891-5849(94)90079-5

    Article  PubMed  CAS  Google Scholar 

  45. Sanguino E, Ramón M, Michalik L, Wahli W, Alegret M, Sánchez RM, Vázquez-Carrera M, Laguna JC (2004) Lack of hypotriglyceridemic effect of gemfibrozil as a consequence of age-related changes in rat liver PPARα. Biochem Pharmacol 67:157–166. doi:10.1016/j.bcp.2003.08.034

    Article  PubMed  CAS  Google Scholar 

  46. Helen JA, Gulston MK, Bailey NJ, Cheng K, Zhang W, Clarke K, Griffin JL (2009) Metabolomics of the interaction between PPAR-a and age in the PPAR-a-null mouse. Mol Syst Biol 5:259–268. doi:10.1038/msb.2009.18

    Google Scholar 

  47. Suhara W, Koide H, Okuzawa T, Hayashi D, Hashimoto T, Kojo H (2009) Cow’s milk increases the activities of human nuclear receptors peroxisome proliferator-activated receptors alpha and delta and retinoid X receptor alpha involved in the regulation of energy homeostasis, obesity, and inflammation. J Dairy Sci 92:4180–4187. doi:10.3168/jds.2009-2186

    Article  PubMed  CAS  Google Scholar 

  48. Yamamoto M, Clark JD, Pastor JV, Gurnani P, Nandi A, Kurosu H, Miyoshi M, Ogawa Y, Castrillon DH, Rosenblatt KP, Kuro-o M (2005) Regulation of oxidative stress by the anti-aging hormone klotho. J Biol Chem 280:38029–38034. doi:10.1074/jbc.M509039200

    Article  PubMed  CAS  Google Scholar 

  49. Wang Y, Zhang H, Liu MF, Chen SH (2007) Study on antioxidation by lipoteichoic acid of Bifidobacterium. Chin J Gerontol 27 (in Chinese). doi:CNKI:SUN:ZLXZ.0.2007-13-012

  50. Pallottini V, Martini C, Pascolini A, Cavallini G, Gori Z, Bergamini E, Incerpi S, Trentalance A (2005) 3-Hydroxy-3-methylglutaryl coenzyme A reductase deregulation and age-related hypercholesterolemia: a new role for ROS. Mech Ageing Dev 126:845–851. doi:10.1016/j.mad.2005.02.009

    Article  PubMed  CAS  Google Scholar 

  51. Fukushima M, Nakano M (1996) Effects of mixture of organisms, Lactobacillus acidophilus or Streptococcus faecalis on cholesterol metabolism in rats fed on a fat- and cholesterol-enriched diet. Br J Nutr 76:857–867. doi:10.1079/BJN19960092

    Article  PubMed  CAS  Google Scholar 

  52. Jung KJ, Ishigami A, Maruyama N, Takahashi R, Goto S, Yu BP, Chung HY (2004) Modulation of gene expression of SMP-30 by LPS and calorie restriction during aging process. Exp Gerontol 39:1169–1177. doi:10.1016/j.exger.2004.04.005

    Article  PubMed  CAS  Google Scholar 

  53. Akhter T, Nakagawa T, Kobayashi A, Yamaguchi M (2007) Suppression of regucalcin mRNA expression in the hearts of rats administered with free radical compound: the administration-induced death is accelerated in regucalcin transgenic rats. Int J Mol Med 19:653–658

    PubMed  CAS  Google Scholar 

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Acknowledgments

The authors thankfully acknowledge the Council of Scientific and Industrial Research (CSIR), New Delhi, for awarding fellowship grants to one of the authors (Deepti Kaushal).

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Correspondence to Vinod K. Kansal.

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Kaushal, D., Kansal, V.K. Probiotic Dahi containing Lactobacillus acidophilus and Bifidobacterium bifidum alleviates age-inflicted oxidative stress and improves expression of biomarkers of ageing in mice. Mol Biol Rep 39, 1791–1799 (2012). https://doi.org/10.1007/s11033-011-0920-1

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