A botanical containing freeze dried açai pulp promotes healthy aging and reduces oxidative damage in sod1 knockdown flies

Abstract

Superoxide dismutase 1 (SOD1), a critical enzyme against oxidative stress, is implicated in aging and degenerative diseases. We previously showed that a nutraceutical containing freeze-dried açai pulp promotes survival of flies fed a high-fat diet or sod1 knockdown flies fed a standard diet. Here, we investigated the effect of açai supplementation initiated at the early or late young adulthood on lifespan, physiological function, and oxidative damage in sod1 knockdown flies. We found that Açai supplementation extended lifespan even when started at the age of 10 days, which is the time shortly before the mortality rate of flies accelerated. Life-long açai supplementation increased lifetime reproductive output in sod1 knockdown flies. Our molecular studies indicate that açai supplementation reduced the protein levels of genes involved in oxidative stress response, cellular growth, and nutrient metabolism. Açai supplementation also affected the protein levels of ribosomal proteins. In addition, açai supplementation decreased the transcript levels of genes involved in oxidative stress response and gluconeogenesis, while increasing the transcript levels of mitochondrial biogenesis genes. Moreover, açai supplementation reduced the level of 4-hydroxynonenal-protein adducts, a lipid peroxidation marker. Our findings suggest that açai supplementation promotes healthy aging in sod1-deficient flies partly through reducing oxidative damage, and modulating nutrient metabolism and oxidative stress response pathways. Our findings provide a foundation to further evaluate the viability of using açai as an effective dietary intervention to promote healthy aging and alleviate symptoms of diseases with a high level of oxidative stress.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Alavez S, Vantipalli MC, Zucker DJ, Klang IM, Lithgow GJ (2011) Amyloid-binding compounds maintain protein homeostasis during ageing and extend lifespan. Nature 472(7342):226–229

    PubMed  Article  CAS  Google Scholar 

  2. Ang ET, Tai YK, Lo SQ, Seet R, Soong TW (2010) Neurodegenerative diseases: exercising toward neurogenesis and neuroregeneration. Front Ag Neurosci 2:25

    Google Scholar 

  3. Ashburner M (1989) Drosophila: A laboratory handbook. Cold Spring Harbor Laboratory Press, Plainview

    Google Scholar 

  4. Bao Y, Fenwick R (2004) Phytochemicals in health and disease. Oxidative stress and disease 12. Marcel Dekker, New York

    Google Scholar 

  5. Barak Y, Aizenberg D (2010) Is dementia preventable? Focus on Alzheimer's disease. Expert Rev Neurother 10(11):1689–1698

    PubMed  Article  Google Scholar 

  6. Barbieri M, Rizzo MR, Papa M, Boccardi V, Esposito A, White MF, Paolisso G (2010) The IRS2 Gly1057Asp variant is associated with human longevity. J Gerontol A Biol Sci Med Sci 65(3):282–286. doi:10.1093/gerona/glp154

    PubMed  Article  Google Scholar 

  7. Bass TM, Grandison RC, Wong R, Martinez P, Partridge L, Piper MD (2007) Optimization of dietary restriction protocols in Drosophila. J Gerontol A Biol Sci Med Sci 62(10):1071–1081

    PubMed  Article  Google Scholar 

  8. Baur JA, Pearson KJ, Price NL, Jamieson HA, Lerin C, Kalra A, Prabhu VV, Allard JS, Lopez-Lluch G, Lewis K, Pistell PJ, Poosala S, Becker KG, Boss O, Gwinn D, Wang M, Ramaswamy S, Fishbein KW, Spencer RG, Lakatta EG, Le Couteur D, Shaw RJ, Navas P, Puigserver P, Ingram DK, de Cabo R, Sinclair DA (2006) Resveratrol improves health and survival of mice on a high-calorie diet. Nature 444(7117):337–342

    PubMed  Article  CAS  Google Scholar 

  9. Boyd O, Weng P, Sun X, Alberico T, Laslo M, Obenland DM, Kern B, Zou S (2011) Nectarine promotes longevity in Drosophila melanogaster. Free Radic Biol Med 50(11):1669–1678

    PubMed  Article  CAS  Google Scholar 

  10. Chakravarty K, Cassuto H, Reshef L, Hanson RW (2005) Factors that control the tissue-specific transcription of the gene for phosphoenolpyruvate carboxykinase-C. Crit Rev Biochem Mol Biol 40(3):129–154. doi:10.1080/10409230590935479

    PubMed  Article  CAS  Google Scholar 

  11. Civitarese AE, Smith SR, Ravussin E (2007) Diet, energy metabolism and mitochondrial biogenesis. Curr Opin Clin Nutr Metab Care 10(6):679–687. doi:10.1097/MCO.0b013e3282f0ecd2.00075197-200711000-00005

    PubMed  Article  CAS  Google Scholar 

  12. Feio CA, Izar MC, Ihara SS, Kasmas SH, Martins CM, Feio MN, Maues LA, Borges NC, Moreno RA, Povoa RM, Fonseca FA (2011) Euterpe Oleracea (Acai) Modifies Sterol Metabolism and Attenuates Experimentally-Induced Atherosclerosis. J Atherosclerosis Thromb

  13. Ferrara N, Rinaldi B, Corbi G, Conti V, Stiuso P, Boccuti S, Rengo G, Rossi F, Filippelli A (2008) Exercise training promotes SIRT1 activity in aged rats. Rejuvenation Res 11(1):139–150

    PubMed  Article  CAS  Google Scholar 

  14. Fontana L, Partridge L, Longo VD (2010) Extending healthy life span—from yeast to humans. Sci 328(5976):321–326

    Article  CAS  Google Scholar 

  15. Fridovich I (1995) Superoxide radical and superoxide dismutases. Annu Rev Biochem 64:97–112. doi:10.1146/annurev.bi.64.070195.000525

    PubMed  Article  CAS  Google Scholar 

  16. Harman D (1956) Aging: a theory based on free radical and radiation chemistry. J Gerontol 11(3):298–300

    PubMed  Article  CAS  Google Scholar 

  17. Harrison DE, Strong R, Sharp ZD, Nelson JF, Astle CM, Flurkey K, Nadon NL, Wilkinson JE, Frenkel K, Carter CS, Pahor M, Javors MA, Fernandez E, Miller RA (2009) Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature 460(7253):392–395

    PubMed  CAS  Google Scholar 

  18. Heli H, Mirtorabi S, Karimian K (2011) Advances in iron chelation: an update. Expert Rev Neurother 21(6):819–856

    CAS  Google Scholar 

  19. Hung CW, Chen YC, Hsieh WL, Chiou SH, Kao CL (2010) Ageing and neurodegenerative diseases. Ageing Res Rev 9(Suppl 1):S36–46

    PubMed  Article  Google Scholar 

  20. Ja WW, Carvalho GB, Mak EM, de la Rosa NN, Fang AY, Liong JC, Brummel T, Benzer S (2007) Prandiology of Drosophila and the CAFE assay. Proc Natl Acad Sci U S A 104(20):8253–8256

    PubMed  Article  CAS  Google Scholar 

  21. Jasper H, Benes V, Schwager C, Sauer S, Clauder-Munster S, Ansorge W, Bohmann D (2001) The genomic response of the Drosophila embryo to JNK signaling. Dev Cell 1(4):579–586

    PubMed  Article  CAS  Google Scholar 

  22. Joseph JA, Shukitt-Hale B, Lau FC (2007) Fruit polyphenols and their effects on neuronal signaling and behavior in senescence. Ann N Y Acad Sci 1100:470–485. doi:10.1196/annals.1395.052

    PubMed  Article  CAS  Google Scholar 

  23. Joseph JA, Shukitt-Hale B, Willis LM (2009) Grape juice, berries, and walnuts affect brain aging and behavior. J Nutr 139(9):1813S–1817S. doi:10.3945/jn.109.108266

    PubMed  Article  CAS  Google Scholar 

  24. Karpac J, Jasper H (2009) Insulin and JNK: optimizing metabolic homeostasis and lifespan. Trends Endocrinol Metab 20(3):100–106. doi:10.1016/j.tem.2008.11.004

    PubMed  Article  CAS  Google Scholar 

  25. Kim J, Guan KL (2011) Amino Acid Signaling in TOR Activation. Annu Rev Biochem 80:1001–1032

    PubMed  Article  CAS  Google Scholar 

  26. Kohen R, Nyska A (2002) Oxidation of biological systems: oxidative stress phenomena, antioxidants, redox reactions, and methods for their quantification. Toxicol Pathol 30(6):620–650

    PubMed  Article  CAS  Google Scholar 

  27. Lee KS, Lee BS, Semnani S, Avanesian A, Um CY, Jeon HJ, Seong KM, Yu K, Min KJ, Jafari M (2010) Curcumin extends life span, improves health span, and modulates the expression of age-associated aging genes in Drosophila melanogaster. Rejuvenation Res 13(5):561–570

    PubMed  Article  CAS  Google Scholar 

  28. Liu RH (2004) Potential synergy of phytochemicals in cancer prevention: mechanism of action. J Nutr 134(12 Suppl):3479S–3485S. doi:134/12/3479S

    PubMed  CAS  Google Scholar 

  29. Magnuson B, Peppard A, Auer Flomenhoft D (2011) Hypocaloric considerations in patients with potentially hypometabolic disease States. Nutr Clin Pract 26(3):253–260

    PubMed  Article  Google Scholar 

  30. Mahapatra CT, Bond J, Rand DM, Rand MD (2010) Identification of methylmercury tolerance gene candidates in Drosophila. Toxicol Sci 116(1):225–238

    PubMed  Article  CAS  Google Scholar 

  31. Obrenovich ME, Nair NG, Beyaz A, Aliev G, Reddy VP (2010) The role of polyphenolic antioxidants in health, disease, and aging. Rejuvenation Res 13(6):631–643

    PubMed  Article  CAS  Google Scholar 

  32. Okamoto K, Kihira T, Kobashi G, Washio M, Sasaki S, Yokoyama T, Miyake Y, Sakamoto N, Inaba Y, Nagai M (2009) Fruit and vegetable intake and risk of amyotrophic lateral sclerosis in Japan. Neuroepidemiology 32(4):251–256

    PubMed  Article  CAS  Google Scholar 

  33. Pan MH, Lai CS, Dushenkov S, Ho CT (2009) Modulation of inflammatory genes by natural dietary bioactive compounds. J Agric Food Chem 57(11):4467–4477. doi:10.1021/jf900612n

    PubMed  Article  CAS  Google Scholar 

  34. Peng C, Chan HY, Huang Y, Yu H, Chen ZY (2011) Apple polyphenols extend the mean lifespan of Drosophila melanogaster. J Agric Food Chem 59(5):2097–2106

    PubMed  Article  CAS  Google Scholar 

  35. Perez VI, Bokov A, Remmen HV, Mele J, Ran Q, Ikeno Y, Richardson A (2009) Is the oxidative stress theory of aging dead? Biochim Biophys Acta 1790(10):1005–1014. doi:10.1016/j.bbagen.2009.06.003

    PubMed  Article  CAS  Google Scholar 

  36. Phillips JP, Campbell SD, Michaud D, Charbonneau M, Hilliker AJ (1989) Null mutation of copper/zinc superoxide dismutase in Drosophila confers hypersensitivity to paraquat and reduced longevity. Proc Natl Acad Sci U S A 86(8):2761–2765

    PubMed  Article  CAS  Google Scholar 

  37. Phillips JP, Tainer JA, Getzoff ED, Boulianne GL, Kirby K, Hilliker AJ (1995) Subunit-destabilizing mutations in Drosophila copper/zinc superoxide dismutase: neuropathology and a model of dimer dysequilibrium. Proc Natl Acad Sci U S A 92(19):8574–8578

    PubMed  Article  CAS  Google Scholar 

  38. Poulose SM, Fisher DR, Larson JA, Bielinski DF, Rimando AM, Carey AN, Schauss AG, Shukitt-Hale B (2012) Anthocyanin-rich acai (Euterpe oleracea Mart.) fruit pulp fractions attenuate inflammatory stress signaling in mouse brain BV-2 microglial cells. J Agric Food Chem 60(4):1084–1093. doi:10.1021/jf203989k

    PubMed  Article  CAS  Google Scholar 

  39. Radyuk SN, Klichko VI, Spinola B, Sohal RS, Orr WC (2001) The peroxiredoxin gene family in Drosophila melanogaster. Free Radic Biol Med 31(9):1090–1100

    PubMed  Article  CAS  Google Scholar 

  40. Rosen DR, Siddique T, Patterson D, Figlewicz DA, Sapp P, Hentati A, Donaldson D, Goto J, O'Regan JP, Deng HX et al (1993) Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 362(6415):59–62

    PubMed  Article  CAS  Google Scholar 

  41. Salmon AB, Richardson A, Perez VI (2010) Update on the oxidative stress theory of aging: does oxidative stress play a role in aging or healthy aging? Free Radic Biol Med 48(5):642–655

    PubMed  Article  CAS  Google Scholar 

  42. Schauss AG, Wu X, Prior RL, Ou B, Huang D, Owens J, Agarwal A, Jensen GS, Hart AN, Shanbrom E (2006a) Antioxidant capacity and other bioactivities of the freeze-dried Amazonian palm berry, Euterpe oleraceae Mart. (acai). J Agric Food Chem 54(22):8604–8610. doi:10.1021/jf0609779

    PubMed  Article  CAS  Google Scholar 

  43. Schauss AG, Wu X, Prior RL, Ou B, Patel D, Huang D, Kababick JP (2006b) Phytochemical and nutrient composition of the freeze-dried amazonian palm berry, Euterpe oleraceae Mart. (acai). J Agric Food Chem 54(22):8598–8603. doi:10.1021/jf060976g

    Article  CAS  Google Scholar 

  44. Srivastava RA (2009) Fenofibrate ameliorates diabetic and dyslipidemic profiles in KKAy mice partly via down-regulation of 11beta-HSD1, PEPCK and DGAT2. Comparison of PPARalpha, PPARgamma, and liver x receptor agonists. Eur J Pharmacol 607(1–3):258–263. doi:10.1016/j.ejphar.2009.02.024

    PubMed  Article  CAS  Google Scholar 

  45. Stoner GD, Wang LS, Seguin C, Rocha C, Stoner K, Chiu S, Kinghorn AD (2010) Multiple berry types prevent N-nitrosomethylbenzylamine-induced esophageal cancer in rats. Pharmaceut Res 27(6):1138–1145

    Article  CAS  Google Scholar 

  46. Sun X, Seeberger J, Alberico T, Wang C, Wheeler CT, Schauss AG, Zou S (2010) Açai palm fruit (Euterpe oleracea Mart.) pulp improves survival of flies on a high fat diet. Exp Gerontol 45(3):243–251

    PubMed  Article  CAS  Google Scholar 

  47. Toda T, Sunagawa T, Kanda T, Tagashira M, Shirasawa T, Shimizu T (2011) Apple procyanidins suppress amyloid beta-protein aggregation. Biochem Res Int 2011:784698

    PubMed  Google Scholar 

  48. Udani JK, Singh BB, Singh VJ, Barrett ML (2011) Effects of Açai (Euterpe oleracea Mart.) berry preparation on metabolic parameters in a healthy overweight population: a pilot study. Nutr J 10:45

    PubMed  Article  CAS  Google Scholar 

  49. Unno K, Ishikawa Y, Takabayashi F, Sasaki T, Takamori N, Iguchi K, Hoshino M (2008) Daily ingestion of green tea catechins from adulthood suppressed brain dysfunction in aged mice. Biofactors 34(4):263–271

    PubMed  Article  Google Scholar 

  50. Vina J, Lloret A, Giraldo E, Badia MC, Alonso MD (2011) Antioxidant pathways in Alzheimer's disease: possibilities of intervention. Curr Pharm Des 17(35):3861–3864

    PubMed  Article  CAS  Google Scholar 

  51. Wang MC, Bohmann D, Jasper H (2003) JNK signaling confers tolerance to oxidative stress and extends lifespan in Drosophila. Dev Cell 5(5):811–816

    PubMed  Article  CAS  Google Scholar 

  52. Wang MC, Bohmann D, Jasper H (2005) JNK extends life span and limits growth by antagonizing cellular and organism-wide responses to insulin signaling. Cell 121(1):115–125

    PubMed  Article  CAS  Google Scholar 

  53. Wang G, Wu WW, Zeng W, Chou CL, Shen RF (2006) Label-free protein quantification using LC-coupled ion trap or FT mass spectrometry: reproducibility, linearity, and application with complex proteomes. J Proteome Res 5(5):1214–1223

    PubMed  Article  CAS  Google Scholar 

  54. Whitworth AJ, Theodore DA, Greene JC, Benes H, Wes PD, Pallanck LJ (2005) Increased glutathione S-transferase activity rescues dopaminergic neuron loss in a Drosophila model of Parkinson's disease. Proc Natl Acad Sci U S A 102(22):8024–8029

    PubMed  Article  CAS  Google Scholar 

  55. Wood ZA, Poole LB, Karplus PA (2003) Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling. Sci 300(5619):650–653. doi:10.1126/science.1080405.300/5619/650

    Article  CAS  Google Scholar 

  56. Wu WW, Wang G, Yu MJ, Knepper MA, Shen RF (2007) Identification and quantification of basic and acidic proteins using solution-based two-dimensional protein fractionation and label-free or 18O-labeling mass spectrometry. J Proteome Res 6(7):2447–2459

    PubMed  Article  CAS  Google Scholar 

  57. Xie C, Kang J, Burris R, Ferguson ME, Schauss AG, Nagarajan S, Wu X (2011a) Acai juice attenuates atherosclerosis in ApoE deficient mice through antioxidant and anti-inflammatory activities. Atheroscler 216(2):327–333

    Article  CAS  Google Scholar 

  58. Xie C, Kang J, Li Z, Schauss AG, Badger TM, Nagarajan S, Wu T, Wu X (2012) The acai flavonoid velutin is a potent anti-inflammatory agent: blockade of LPS-mediated TNF-alpha and IL-6 production through inhibiting NF-kappaB activation and MAPK pathway. J Nutr Biochem (in press)

  59. Xu J, Marzetti E, Seo AY, Kim JS, Prolla TA, Leeuwenburgh C (2010) The emerging role of iron dyshomeostasis in the mitochondrial decay of aging. Mech Ageing Dev 131(7–8):487–493

    PubMed  Article  CAS  Google Scholar 

  60. Zhang J, Marshall KE, Westwood JT, Clark MS, Sinclair BJ (2011) Divergent transcriptomic responses to repeated and single cold exposures in Drosophila melanogaster. J Exp Biol 214(Pt 23):4021–4029

    PubMed  Article  Google Scholar 

  61. Zimniak P (2008) Detoxification reactions: relevance to aging. Ageing Res Rev 7(4):281–300

    PubMed  Article  CAS  Google Scholar 

  62. Zoncu R, Efeyan A, Sabatini DM (2011) mTOR: from growth signal integration to cancer, diabetes and ageing. Nat Rev Mol Cell Biol 12(1):21–35

    PubMed  Article  CAS  Google Scholar 

  63. Zou S, Carey JR, Liedo P, Ingram DK, Yu B, Ghaedian R (2010) Prolongevity effects of an oregano and cranberry extract are diet dependent in the Mexican fruit fly (Anastrepha ludens). J Gerontol A Biol Sci 65(1):41–50

    Article  Google Scholar 

  64. Zou S, Carey JR, Liedo P, Ingram DK, Yu B (2011) Prolongevity effects of a botanical with oregano and cranberry extracts in Mexican fruit flies: examining interactions of diet restriction and age. Age (Dordrecht, Netherlands) 34(2):269-279

Download references

Acknowledgments

We thank Alex Schauss to provide us the açai pulp extract and thank Ed Spangler, Alex Schauss, Don Ingram, Jim Carey, and Pablo Liedo for critical reading of the manuscript. This work was supported by funding from the Intramural Research Program of the National Institute on Aging, NIH to S.Z. and a research grant from the NIH Office of Dietary Supplements to X.P. and S.Z.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Sige Zou.

Additional information

Mara Laslo and Xiaoping Sun contributed equally to this project.

About this article

Cite this article

Laslo, M., Sun, X., Hsiao, C. et al. A botanical containing freeze dried açai pulp promotes healthy aging and reduces oxidative damage in sod1 knockdown flies. AGE 35, 1117–1132 (2013). https://doi.org/10.1007/s11357-012-9437-3

Download citation

Keywords

  • Aging intervention
  • Açai
  • Superoxide dismutase 1
  • Lifespan
  • Oxidative stress
  • Reproductive aging
  • Drosophila melanogaster