Life-extending ovariectomy in grasshoppers increases somatic storage, but dietary restriction with an equivalent feeding rate does not

Experimental Gerontology

Volumn 48, Issue 9, 2013, Pages 966-972

  Hatle, John D ^a   Kellenberger, James W ^a   Viray, Ephraim ^a   Smith, Alicia M ^a   Hahn, Daniel A ^b  

^a UNIVERSITY OF NORTH FLORIDA   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

Fat storage; Feeding rate; Mitochondria; Reduced reproduction; Romalea microptera

Indexed keywords

BETA ACTIN; CYTOCHROME B; MESSENGER RNA; VITELLOGENIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BETA ACTIN GENE; CAELIFERA; CELL COUNT; CONTROLLED STUDY; DIET RESTRICTION; FAT BODY; FAT MASS; FEEDING BEHAVIOR; FEMALE; GENE EXPRESSION; HEMOLYMPH; HEXAMERIN 90 GENE; LIFE EXTENSION; LIPID STORAGE; MITOCHONDRIAL GENE; MITOCHONDRION; NONHUMAN; OVARIECTOMY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SURVIVAL RATE; VITELLOGENIN GENE;

FAT STORAGE; FEEDING RATE; MITOCHONDRIA; REDUCED REPRODUCTION; ROMALEA MICROPTERA;

AGING; ANIMALS; ANTIOXIDANTS; CALORIC RESTRICTION; FAT BODY; FEEDING BEHAVIOR; FEMALE; GRASSHOPPERS; HEMOLYMPH; KAPLAN-MEIER ESTIMATE; LIFE EXPECTANCY; LONGEVITY; MITOCHONDRIA; OVARIECTOMY; REPRODUCTION;

EID: 84881093560     PISSN: 05315565     EISSN: 18736815     Source Type: Journal    
DOI: 10.1016/j.exger.2013.06.006     Document Type: Article

References (41)

1. Bogacka I., Xie H., Bray G.A., Smith S.R. Pioglitazone induces mitochondrial biogenesis in human subcutaneous adipose tissue in vivo. Diabetes 2005, 54:1392-1399.
2. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle protein-dye binding. Anal. Biochem. 1976, 72:248-254.
3. Carvalho G.B., Kapahi P., Benzer S. Compensatory ingestion upon dietary restriction in Drosophila melanogaster. Nat. Methods 2005, 2:813-815.
4. Crawford D., Libina N., Kenyon C. Caenorhabditis elegans integrates food and reproductive signals in life span determination. Aging Cell 2007, 6:715-721.
5. Drewry M.D., Williams J.M., Hatle J.D. Life-extending dietary restriction and ovariectomy result in similar feeding rates but different physiological responses in grasshoppers. Exp. Gerontol. 2011, 46:781-786.
6. Fei H., Martin T.R., Jaskowiak K.M., Hatle J.D., Whitman D.W., Borst D.W. Starvation affects vitellogenin production but not vitellogenin mRNA levels in the lubber grasshopper, Romalea microptera. J. Insect Physiol. 2005, 51:435-443.
7. Flatt T. Survival costs of reproduction in Drosophila. Exp. Gerontol. 2011, 46:369-375.
8. Flatt T., Min K.-J., D'Alterio C., Viklla-Cuesta E., Cumbers J., Lehmann R., Jones D.L., Tatar M. Drosophila germ-line modulation of insulin signaling and lifespan. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:6368-6373.
9. Fronstin R.B., Hatle J.D. A cumulative feeding threshold required for vitellogenesis can be obviated with juvenile hormone treatment in lubber grasshoppers. J. Exp. Biol. 2008, 211:79-85.
10. Ghazi A., Henis-Korenblit S., Kenyon C. A transcription elongation factor that links signals from the reproductive system to lifespan extension in Caenorhabditis elegans. PLoS Genet. 2009, 5:e1000639.
11. Goudeau J., Bellemin S., Toselli-Mollereau E., Shamalnasab M., Chen Y., Aguilaniu H. Fatty acid desaturation links germ cell loss to longevity through NHR-80/HNF4 in C. elegans. PLoS Genet. 2011, 9:e1000599.
12. Guarente L. Mitochondria-a nexus for aging calorie restriction, and sirtuins?. Cell 2008, 132:171-176.
13. Gunawardene E.U., Stephenson R.E., Hatle J.D., Juliano S.A. Are reproductive tactics determined by local ecology in the eastern lubber grasshopper Romalea microptera (Orthoptera: Acrididae)?. Fla. Entomol. 2004, 87:119-123.
14. Hansen M., Flatt T., Aguilaniu H. Reproduction, fat metabolism, and life span: what is the connection?. Cell Metab. 2013, 17:10-19.
15. Hathaway M., Hatle J.D., Li S., Ding X., Barry T., Hong F., Wood H., Borst D.W. Characterization of hexamerin proteins and their mRNAs in the adult lubber grasshopper: the effects of nutrition and juvenile hormone on their levels. Comp. Biochem. Physiol. A 2009, 154:323-332.
16. Hatle J.D., Borst D.W., Eskew M.E., Juliano S.A. Maximum titers of vitellogenin and total hemolymph protein occur during the canalized phase of grasshopper egg production. Physiol. Biochem. Zool. 2001, 74:885-893.
17. Hatle J.D., Crowley M.C., Andrews A.L., Juliano S.A. Geographic variation of reproductive tactics in lubber grasshoppers. Oecologia 2002, 132:517-523.
18. Hatle J.D., Salazar B.A., Whitman D.W. Survival advantage of sluggish individuals in aggregations of aposematic prey, during encounters with ambush predators. Evol. Ecol. 2002, 16:415-431.
19. Hatle J.D., Juliano S.A., Borst D.W. Hemolymph ecdysteroids do not affect vitellogenesis in the lubber grasshopper. Arch. Insect Biochem. Physiol. 2003, 52:45-57.
20. Hatle J.D., Waskey T., Juliano S.A. Plasticity of grasshopper vitellogenin production in response to diet is primarily a result of changes in fat body mass. J. Comp. Physiol. B 2006, 176:27-34.
21. Hatle J.D., Wells S.M., Fuller L.E., Allen I.C., Gordy L.J., Melnyk S., Quattrochi J. Calorie restriction and late-onset calorie restriction extend lifespan but do not alter protein storage in female grasshoppers. Mech. Ageing Dev. 2006, 127:883-891.
22. Hatle J.D., Paterson C.S., Jawaid I., Lentz C., Wells S.M., Fronstin R.B. Protein accumulation underlying lifespan extension via ovariectomy in grasshoppers is consistent with the disposable soma hypothesis but is not due to dietary restriction. Exp. Gerontol. 2008, 43:900-908.
23. Jang Y.C., Pérez V.I., Song W., Lustgarten M.S., Salmon A.B., Mele J., Qi W., Liu Y., Liang H., Chaudhuri A., Ikeno Y., Epstein C.J., Van Remmen H., Richardson A. Overexpression of Mn superoxide dismutase does not increase life span in mice. J. Gerontol. A: Biol. Sci. 2009, 64:1114-1125.
24. Judd E.T., Wessels F.J., Drewry M.D., Grove M., Wright K., Hahn D.A., Hatle J.D. Ovariectomy in grasshoppers increases somatic storage, but proportional allocation of ingested nutrients to somatic tissues is unchanged. Aging Cell 2011, 10:972-979.
25. Kirkwood T.B.L., Kowald A. The free-radical theory of ageing - older, wiser and still alive. BioEssays 2012, 34:692-700.
26. Lee E.T., Wang J.W. Statistical Methods for Survival Data Analysis 2003, Wiley-Interscience, Boulder, CO, USA. third ed.
27. Lopez-Lluch G., Hunt N., Jones B., Zhu M., Jamieson H., Hilmer S., Cascajo M.V., Allard J., Ingram D.K., Navas P., de Cabo R. Calorie restriction induces mitochondrial biogenesis and bioenergetic efficiency. Proc. Natl. Acad. Sci. 2006, 103:1768-1773.
28. McCormick M., Chen K., Ramaswamy P., Kenyon C. New genes that extend Caenorhabditis elegans' lifespan in response to reproductive signals. Aging Cell 2012, 11:192-202.
29. Minor R.K., Chang J.W., de Cabo R. Hungry for life: how the arcuate nucleus and neuropeptide Y may play a critical role in mediating the benefits of calorie restriction. Mol. Cell. Endocrinol. 2009, 299:79-88.
30. Minor R.K., Lopez M., Younts C.M., Jones B., Pearson K., Anson R.M., Dieguez C., de Cabo R. The arcuate nucleus and neuropeptide Y contribute to the antitumorigenic effect of calorie restriction. Aging Cell 2011, 10:483-492.
31. Muller F.L., Lustgarten M.S., Jang Y., Richardson A., Van Remmen H. Trends in oxidative aging theories. Free Radic. Biol. Med. 2007, 43:477-503.
32. Mutun S., Borst D.W. Intraspecific mitochondrial DNA variation and historical biogeography of the Eastern Lubber Grasshopper, Romalea microptera. Ann. Entomol. Soc. Am. 2004, 97:681-696.
33. Nakagawa S., Lagisz M., Hector K.L., Spencer H.G. Comparative and meta-analytic insights into life-extension via dietary restriction. Aging Cell 2012, 11:401-409.
34. Nijhout H.F. Insect Hormones 1994, Princeton University Press, Princeton.
35. O'Rourke E.J., Soukas A.A., Carr C.E., Ruvkun G. C. elegans major fats are stored in vesicles distinct from lysosome-related organelles. Cell Metab. 2009, 10:430-435.
36. Partridge L., Gems D., Withers D.J. Sex and death: what is the connection?. Cell 2005, 120:461-472.
37. Re R., Pellegrini N., Proteggente A., Pannala A., Yang M., Rice-Evans C. Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic. Biol. Med. 1999, 26:1231-1237.
38. Salmon A.B., Richardson A., Perez V.I. Update on the oxidative stress theory of aging: does oxidative stress play a role in aging or healthy aging?. Free Radic. Biol. Med. 2010, 48:642-655.
39. SAS Institute Inc. SAS/STAT User's Guide, Version 8 1999, vols. 1-5. SAS Institute Inc., Cary, NC, USA.
40. Williams J.B., Roberts S.P., Elekonich M.M. Age and natural metabolically intensive behavior affect oxidative stress and anti-oxidant mechanisms. Exp. Gerontol. 2008, 43:538-549.
41. Zhang Y., Ikeno Y., Qi W., Chaudhuri A., Li Y., Bokov A., Thorpe S.R., Baynes J.W., Epstein C., Richardson A., Van Remmen H. Mice deficient in both Mn superoxide dismutase and glutathioneperoxidase-1have increased oxidative damage and a greater incidence of pathology but no reduction in longevity. J. Gerontol. A: Biol. Sci. 2009, 64:1212-1220.