Skip to main content

Advertisement

SpringerLink
Log in

Extension of Drosophila lifespan by Rosa damascena associated with an increased sensitivity to heat

  • Research Article
  • Published:
Biogerontology Aims and scope Submit manuscript

Abstract

Rosa damascena, or Damask rose, is a rose hybrid commonly harvested for rose oil used in perfumery and for rose water used to flavor food. The petal extract of R. damascena was recently found to decrease Drosophila melanogaster mortality without impairing reproductive fitness or metabolic rate. Here, we report that R. damascena extended both mean and maximum lifespan of the fly. The extract also protected against oxidative stress in flies, predominantly in females. However, it did not alter mitochondrial respiration or content, superoxide production, or the major antioxidant defenses, superoxide dismutase and catalase. The extract increased survival in both sexes when exposed to reduced iron, though surprisingly, it sensitized both sexes to heat stress (survival at 37°C), and appeared to down-regulate the major heat shock protein HSP70 and the small mitochondrial heat shock protein HSP22, at 25°C and after heat shock (4 h at 37°C). We hypothesize that R. damascena extends lifespan by protecting against iron, which concomitantly leads to decreased HSP expression and compromising heat tolerance.

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

  • Awai M, Narasaki M, Yamanoi Y, Seno S (1979) Induction of diabetes in animals by parenteral administration of ferric nitrilotriacetate. A model of experimental hemochromatosis. Am J Pathol 95(3):663–673

    PubMed  CAS  Google Scholar 

  • Awale S, Tohda C, Tezuka Y, Miyazaki M, Kadota S (2009) Protective Effects of Rosa damascena and its active constituent on A{beta}(25-35)-induced neuritic atrophy. Evidence Based Complement Altern Med. doi:10.1093/ecam/nep149

  • Ballinger SW (2005) Mitochondrial dysfunction in cardiovascular disease. Free Radic Biol Med 38(10):1278–1295. doi:10.1016/j.freeradbiomed.2005.02.014

    Article  PubMed  CAS  Google Scholar 

  • Baron M, Kudin AP, Kunz WS (2007) Mitochondrial dysfunction in neurodegenerative disorders. Biochem Soc Trans 35(Pt 5):1228–1231. doi:10.1042/BST0351228

    PubMed  CAS  Google Scholar 

  • Bartke A (2011) Single-gene mutations and healthy ageing in mammals. Philos Trans Roy Soc Lond B 366(1561):28–34. doi:10.1098/rstb.2010.0281

    Article  CAS  Google Scholar 

  • Basim E, Basim H (2003) Antibacterial activity of Rosa damascena essential oil. Fitoterapia 74(4):394–396

    Article  PubMed  CAS  Google Scholar 

  • 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. doi:10.1038/nature05354

    Article  PubMed  CAS  Google Scholar 

  • Beckman KB, Ames BN (1998) The free radical theory of aging matures. Physiol Rev 78(2):547–581

    PubMed  CAS  Google Scholar 

  • Beers RF Jr, Sizer IW (1952) A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem 195(1):133–140

    PubMed  CAS  Google Scholar 

  • Bhole D, Allikian MJ, Tower J (2004) Doxycycline-regulated over-expression of hsp22 has negative effects on stress resistance and life span in adult Drosophila melanogaster. Mech Ageing Dev 125(9):651–663. doi:10.1016/j.mad.2004.08.010

    Article  PubMed  CAS  Google Scholar 

  • Bjedov I, Toivonen JM, Kerr F, Slack C, Jacobson J, Foley A, Partridge L (2010) Mechanisms of life span extension by rapamycin in the fruit fly Drosophila melanogaster. Cell Metab 11(1):35–46. doi:10.1016/j.cmet.2009.11.010

    Article  PubMed  CAS  Google Scholar 

  • Chen H, Zheng C, Zhang Y, Chang YZ, Qian ZM, Shen X (2006) Heat shock protein 27 downregulates the transferrin receptor 1-mediated iron uptake. Int J Biochem Cell Biol 38(8):1402–1416. doi:10.1016/j.biocel.2006.02.006

    Article  PubMed  CAS  Google Scholar 

  • Choi J, Rees HD, Weintraub ST, Levey AI, Chin LS, Li L (2005) Oxidative modifications and aggregation of Cu,Zn-superoxide dismutase associated with Alzheimer and Parkinson diseases. J Biol Chem 280(12):11648–11655. doi:10.1074/jbc.M414327200

    Article  PubMed  CAS  Google Scholar 

  • Davis JM, Murphy EA, Carmichael MD, Davis B (2009) Quercetin increases brain and muscle mitochondrial biogenesis and exercise tolerance. Am J Physiol Regul Integr Comp Physiol 296(4):R1071–R1077. doi:10.1152/ajpregu.90925.2008

    Article  PubMed  CAS  Google Scholar 

  • Dunkov B, Georgieva T (2006) Insect iron binding proteins: insights from the genomes. Insect Biochem Mol Biol 36(4):300–309. doi:10.1016/j.ibmb.2006.01.007

    Article  PubMed  CAS  Google Scholar 

  • Fearon IM, Faux SP (2009) Oxidative stress and cardiovascular disease: novel tools give (free) radical insight. J Mol Cell Cardiol 47(3):372–381. doi:10.1016/j.yjmcc.2009.05.013

    Article  PubMed  CAS  Google Scholar 

  • Friedman DB, Johnson TE (1988) A mutation in the age-1 gene in Caenorhabditis elegans lengthens life and reduces hermaphrodite fertility. Genetics 118(1):75–86

    PubMed  CAS  Google Scholar 

  • Giannakou ME, Partridge L (2007) Role of insulin-like signalling in Drosophila lifespan. Trends Biochem Sci 32(4):180–188. doi:10.1016/j.tibs.2007.02.007

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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. doi:10.1038/nature08221

    PubMed  CAS  Google Scholar 

  • Hausladen A, Fridovich I (1996) Measuring nitric oxide and superoxide: rate constants for aconitase reactivity. Methods Enzymol 269:37–41

    Article  PubMed  CAS  Google Scholar 

  • Henchcliffe C, Beal MF (2008) Mitochondrial biology and oxidative stress in Parkinson disease pathogenesis. Nat Clin Pract Neurol 4(11):600–609. doi:10.1038/ncpneuro0924

    Article  PubMed  CAS  Google Scholar 

  • Jafari M, Zarban A, Pham S, Wang T (2008) Rosa damascena decreased mortality in adult Drosophila. J Med Food 11(1):9–13. doi:10.1089/jmf.2007.546

    Article  PubMed  CAS  Google Scholar 

  • Johannsen DL, Ravussin E (2009) The role of mitochondria in health and disease. Curr Opin Pharmacol 9(6):780–786. doi:10.1016/j.coph.2009.09.002

    Article  PubMed  CAS  Google Scholar 

  • Kampkotter A, Timpel C, Zurawski RF, Ruhl S, Chovolou Y, Proksch P, Watjen W (2008) Increase of stress resistance and lifespan of Caenorhabditis elegans by quercetin. Comp Biochem Physiol B 149(2):314–323. doi:10.1016/j.cbpb.2007.10.004

    Article  PubMed  Google Scholar 

  • Kenyon CJ (2010) The genetics of ageing. Nature 464(7288):504–512. doi:10.1038/nature08980

    Article  PubMed  CAS  Google Scholar 

  • King V, Tower J (1999) Aging-specific expression of Drosophila hsp22. Dev Biol 207(1):107–118. doi:10.1006/dbio.1998.9147

    Article  PubMed  CAS  Google Scholar 

  • Kirkwood TB, Austad SN (2000) Why do we age? Nature 408(6809):233–238. doi:10.1038/35041682

    Article  PubMed  CAS  Google Scholar 

  • Kondapalli KC, Kok NM, Dancis A, Stemmler TL (2008) Drosophila frataxin: an iron chaperone during cellular Fe-S cluster bioassembly. Biochemistry 47(26):6917–6927. doi:10.1021/bi800366d

    Article  PubMed  CAS  Google Scholar 

  • Kumar N, Bhandari P, Singh B, Gupta AP, Kaul VK (2008) Reversed phase-HPLC for rapid determination of polyphenols in flowers of rose species. J Sep Sci 31(2):262–267. doi:10.1002/jssc.200700372

    Article  PubMed  CAS  Google Scholar 

  • Kurapati R, Passananti HB, Rose MR, Tower J (2000) Increased hsp22 RNA levels in Drosophila lines genetically selected for increased longevity. J Gerontol A Biol Sci Med Sci 55(11):B552–B559

    Article  PubMed  CAS  Google Scholar 

  • Lagouge M, Argmann C, Gerhart-Hines Z, Meziane H, Lerin C, Daussin F, Messadeq N, Milne J, Lambert P, Elliott P, Geny B, Laakso M, Puigserver P, Auwerx J (2006) Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha. Cell 127(6):1109–1122. doi:10.1016/j.cell.2006.11.013

    Article  PubMed  CAS  Google Scholar 

  • Lapointe J, Hekimi S (2010) When a theory of aging ages badly. Cell Mol Life Sci 67(1):1–8. doi:10.1007/s00018-009-0138-8

    Article  PubMed  CAS  Google Scholar 

  • Loghmani-Khouzani H, Sabzi Fini O, Safari J (2007) Essential oil composition of Rosa damascena mill cultivated in central Iran. Sci Iran 14(4):316–319

    CAS  Google Scholar 

  • Magwere T, Goodall S, Skepper J, Mair W, Brand MD, Partridge L (2006) The effect of dietary restriction on mitochondrial protein density and flight muscle mitochondrial morphology in Drosophila. J Gerontol A Biol Sci Med Sci 61(1):36–47

    Article  PubMed  Google Scholar 

  • Martin LJ (2006) Mitochondriopathy in Parkinson disease and amyotrophic lateral sclerosis. J Neuropathol Exp Neurol 65(12):1103–1110. doi:10.1097/01.jnen.0000248541.05552.c4

    Article  PubMed  CAS  Google Scholar 

  • Massie HR, Aiello VR, Williams TR (1993) Inhibition of iron absorption prolongs the life span of Drosophila. Mech Ageing Dev 67(3):227–237

    Article  PubMed  CAS  Google Scholar 

  • Miller RA, Harrison DE, Astle CM, Baur JA, Boyd AR, de Cabo R, Fernandez E, Flurkey K, Javors MA, Nelson JF, Orihuela CJ, Pletcher S, Sharp ZD, Sinclair D, Starnes JW, Wilkinson JE, Nadon NL, Strong R (2011) Rapamycin, but not resveratrol or simvastatin, extends life span of genetically heterogeneous mice. J Gerontol A Biol Sci Med Sci 66(2):191–201. doi:10.1093/gerona/glq178

    Article  PubMed  Google Scholar 

  • Morrow G, Samson M, Michaud S, Tanguay RM (2004) Overexpression of the small mitochondrial Hsp22 extends Drosophila life span and increases resistance to oxidative stress. FASEB J 18(3):598–599. doi:10.1096/fj.03-0860fje

    PubMed  CAS  Google Scholar 

  • Nisoli E, Tonello C, Cardile A, Cozzi V, Bracale R, Tedesco L, Falcone S, Valerio A, Cantoni O, Clementi E, Moncada S, Carruba MO (2005) Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS. Science 310(5746):314–317. doi:10.1126/science.1117728

    Article  PubMed  CAS  Google Scholar 

  • Ramezani R, Moghimi A, Rakhshandeh H, Ejtehadi H, Kheirabadi M (2008) The effect of Rosa damascena essential oil on the amygdala electrical kindling seizures in rat. Pak J Biol Sci 11(5):746–751

    Article  PubMed  Google Scholar 

  • Robinson KM, Janes MS, Pehar M, Monette JS, Ross MF, Hagen TM, Murphy MP, Beckman JS (2006) Selective fluorescent imaging of superoxide in vivo using ethidium-based probes. Proc Natl Acad Sci USA 103(41):15038–15043. doi:10.1073/pnas.0601945103

    Google Scholar 

  • Rose MR, Charlesworth B (1981) Genetics of life history in Drosophila melanogaster. I. Sib analysis of adult females. Genetics 97(1):173–186

    PubMed  CAS  Google Scholar 

  • Rose MR, Drapeau MD, Yazdi PG, Shah KH, Moise DB, Thakar RR, Rauser CL, Mueller LD (2002) Evolution of late-life mortality in Drosophila melanogaster. Evolution 56(10):1982–1991

    PubMed  Google Scholar 

  • 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. doi:10.1016/j.freeradbiomed.2009.12.015

    Article  PubMed  CAS  Google Scholar 

  • Shokouhinejad N, Emaneini M, Aligholi M, Jabalameli F (2010) Antimicrobial effect of Rosa damascena extract on selected endodontic pathogens. J Calif Dent Assoc 38(2):123–126

    PubMed  Google Scholar 

  • Speakman JR, Selman C (2011) The free-radical damage theory: accumulating evidence against a simple link of oxidative stress to ageing and lifespan. Bioessays 33(4):255–259. doi:10.1002/bies.201000132

    Article  PubMed  Google Scholar 

  • Tower J (2011) Heat shock proteins and Drosophila aging. Exp Gerontol 46(5):355–362. doi:10.1016/j.exger.2010.09.002

    Article  PubMed  CAS  Google Scholar 

  • Vermeulen CJ, Loeschcke V (2007) Longevity and the stress response in Drosophila. Exp Gerontol 42(3):153–159. doi:10.1016/j.exger.2006.09.014

    Article  PubMed  CAS  Google Scholar 

  • Wallace DC (2005) A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annu Rev Genet 39:359–407. doi:10.1146/annurev.genet.39.110304.095751

    Article  PubMed  CAS  Google Scholar 

  • Wallace DC, Brown MD, Melov S, Graham B, Lott M (1998) Mitochondrial biology, degenerative diseases and aging. Biofactors 7(3):187–190

    Article  PubMed  CAS  Google Scholar 

  • Wang X, Su B, Perry G, Smith MA, Zhu X (2007) Insights into amyloid-beta-induced mitochondrial dysfunction in Alzheimer disease. Free Radic Biol Med 43(12):1569–1573. doi:10.1016/j.freeradbiomed.2007.09.007

    Article  PubMed  CAS  Google Scholar 

  • Williams AJ, Coakley J, Christodoulou J (1998) Automated analysis of mitochondrial enzymes in cultured skin fibroblasts. Anal Biochem 259(2):176–180. doi:10.1006/abio.1998.2624

    Google Scholar 

  • Winterbourn CC, Hawkins RE, Brian M, Carrell RW (1975) The estimation of red cell superoxide dismutase activity. J Lab Clin Med 85(2):337–341

    PubMed  CAS  Google Scholar 

  • 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. doi:10.1016/j.mad.2010.04.007

    Article  PubMed  CAS  Google Scholar 

  • Yang J, Tower J (2009) Expression of hsp22 and hsp70 transgenes is partially predictive of Drosophila survival under normal and stress conditions. J Gerontol A Biol Sci Med Sci 64(8):828–838. doi:10.1093/gerona/glp054

    Article  PubMed  Google Scholar 

  • Zhang X, Min X, Li C, Benjamin IJ, Qian B, Ding Z, Gao X, Yao Y, Ma Y, Cheng Y, Liu L (2010) Involvement of reductive stress in the cardiomyopathy in transgenic mice with cardiac-specific overexpression of heat shock protein 27. Hypertension 55(6):1412–1417. doi:10.1161/HYPERTENSIONAHA.109.147066

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank Dr. Douglas C. Wallace for the use of his equipment and facilities. This work was funded by an R21 grant awarded to MJ awarded by the National Center for Complementary and Alternative Medicine. The work presented in this manuscript was supported by NIH.

Author information

Authors and Affiliations

  1. Department of Pharmaceutical Sciences, University of California, 147 Biological Sciences Administration, Irvine, CA, 92697, USA

    Samuel E. Schriner, Niki S. Katoozi, Kevin Q. Pham, Maral Gazarian & Mahtab Jafari

  2. Birjand University of Medical Sciences, Birjand, Iran

    Asghar Zarban

Authors
  1. Samuel E. Schriner
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Niki S. Katoozi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kevin Q. Pham
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Maral Gazarian
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Asghar Zarban
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mahtab Jafari
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mahtab Jafari.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schriner, S.E., Katoozi, N.S., Pham, K.Q. et al. Extension of Drosophila lifespan by Rosa damascena associated with an increased sensitivity to heat. Biogerontology 13, 105–117 (2012). https://doi.org/10.1007/s10522-011-9357-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10522-011-9357-0

Keywords

Search

Navigation