Dietary protein: Carbohydrate balance is a critical modulator of lifespan and reproduction in Drosophila melanogaster: A test using a chemically defined diet

Journal of Insect Physiology

Volumn 75, Issue , 2015, Pages 12-19

  Lee, Kwang Pum ^a  

^a Seoul National University   (South Korea)

Author keywords

Ageing; Drosophila melanogaster; Fecundity; Lifespan; Lipid storage; Protein:carbohydrate balance

Indexed keywords

ARTIFICIAL DIET; DIET; EGG PRODUCTION; FECUNDITY; FITNESS; FLY; LIPID; MORTALITY; PROTEIN; REPRODUCTIVE SUCCESS; SENESCENCE; SUGAR; YEAST;

ANIMALIA; DROSOPHILA MELANOGASTER; HEXAPODA;

CARBOHYDRATE DIET; PROTEIN INTAKE;

AGING; ANIMAL; CARBOHYDRATE DIET; DROSOPHILA MELANOGASTER; ELEMENTAL DIET; FEMALE; FERTILITY; LONGEVITY; METABOLISM; PHYSIOLOGY; PROTEIN INTAKE; REPRODUCTION;

AGING; ANIMALS; DIETARY CARBOHYDRATES; DIETARY PROTEINS; DROSOPHILA MELANOGASTER; FEMALE; FERTILITY; FOOD, FORMULATED; LONGEVITY; REPRODUCTION;

EID: 84924694425     PISSN: 00221910     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jinsphys.2015.02.007     Document Type: Article

References (68)

1. Bass T.M., Grandison R.C., Wong R., Martinez P., Partridge L., Piper M.D.W. Optimization of dietary restriction protocols in Drosophila. J. Gerontol. Ser. A: Biol. Sci. Med. Sci. 2007, 62:1071-1081.
2. Behmer S.T. Insect herbivore nutrient regulation. Annu. Rev. Entomol. 2009, 54:165-187.
3. Broadway R.M., Duffey S.S. The effect of dietary protein on the growth and digestive physiology of larval Heliothis zea and Spodoptera exigua. J. Insect Physiol. 1986, 32:673-680.
4. Bruce K.D., Hoxha S., Carvalho G.B., Yamada R., Wang H.-D., Karayan P., He S., Brummel T., Kapahi P., Ja W.W. High carbohydrate-low protein consumption maximizes Drosophila lifespan. Exp. Gerontol. 2013, 48:1129-1135.
5. Chippindale A.K., Leroi A.M., Kim S.B., Rose M.R. Phenotypic plasticity and selection in Drosophila life-history evolution. I. Nutrition and the cost of reproduction. J. Evol. Biol. 1993, 6:171-193.
6. Clancy D.J., Kennington W.J. A simple method to achieve consistent larval density in bottle cultures. Drosophila Inf. Serv. 2001, 84:168-169.
7. Colman R.J., Anderson R.M., Johnson S.C., Kastman E.K., Kosmatka K.J., Beasley T.M., Allison D.B., Cruzen C., Simmons H.A., Kemnitz J.W., Weindruch R. Caloric restriction delays disease onset and mortality in rhesus monkeys. Science 2009, 325:201-204.
8. Dussutour A., Simpson S.J. Ant workers die young and colonies collapse when fed a high-protein diet. Proc. Roy. Soc. London Ser. B 2012, 279:2402-2408.
9. Fanson B.G., Taylor P.W. Protein:carbohydrate ratios explain life span patterns found in Queensland fruit fly on diets varying in yeast:sugar ratios. Age 2012, 34:1361-1368.
10. Fanson B.G., Weldon C.W., Pérez-Staples D., Simpson S.J., Taylor P.W. Nutrients, not caloric restriction, extend lifespan in Queensland fruit flies (Bactrocera tryoni). Aging Cell 2009, 8:514-523.
11. Flatt T. Survival costs of reproduction in Drosophila. Exp. Gerontol. 2011, 46:369-375.
12. Fortini M.E., Skupski M.P., Boguski M.S., Hariharan I.K. A survey of human disease gene counterparts in the Drosophila genome. J. Cell Biol. 2000, 150:23-30.
13. Fukui H.H., Xiu L.A., Curtsinger J.W. Slowing of age-specific mortality rates in Drosophila melanogaster. Exp. Gerontol. 1993, 28:585-599.
14. Good T.P., Tatar M. Age-specific mortality and reproduction respond to adult dietary restriction in Drosophila melanogaster. J. Insect Physiol. 2001, 47:1467-1473.
15. Grandison R.C., Piper M.D.W., Partridge L. Amino-acid imbalance explains extension of lifespan by dietary restriction in Drosophila. Nature 2009, 462:1061-1064.
16. Hansen M., Flatt T., Aguilaniu H. Reproduction, fat metabolism, and lifespan: what is the connection?. Cell Metab. 2013, 17:10-19.
17. Harshman L.G., Zera A.J. The cost of reproduction: the devil in the details. Trends Ecol. Evol. 2006, 22:80-86.
18. Hubert H.B., Feinleib M., McNamara P.M., Castelli W.P. Obesity as an independent risk factor for cardiovascular disease: a 26-year follow up of participants in the Framingham Heart Study. Circulation 1983, 67:968-977.
19. Ja W.W., Carvalho G.B., Zid B.M., Mak E.M., Brummel T., Benzer S. Water- and nutrient-dependent effects of dietary restriction on Drosophila lifespan. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:18633-18637.
20. 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.
21. Kapahi P., Zid B.M., Harper T., Koslover D., Sapin V., Benzer S. Regulation of lifespan in Drosophila by modulation of genes in the TOR signaling pathway. Curr. Biol. 2004, 14:885-890.
22. Kenyon C.J. The genetics of ageing. Nature 2010, 464:504-512.
23. Lee E.T. Statistical Methods for Survival Data Analysis 1992, Wiley, New York.
24. Lee K.P. The interactive effects of protein quality and macronutrient imbalance on nutrient balancing in an insect herbivore. J. Exp. Biol. 2007, 210:3236-3244.
25. Lee K.P., Jang T. Exploring the nutritional basis of starvation resistance in Drosophila melanogaster. Funct. Ecol. 2014, 28:1144-1155.
26. Lee K.P., Behmer S.T., Simpson S.J., Raubenhemer D. A geometric analysis of nutrient regulation in the generalist caterpillar Spodoptera littoralis (Boisduval). J. Insect Physiol. 2002, 48:655-665.
27. Lee K.P., Simpson S.J., Clissold F.J., Brooks R., Ballard J.W.O., Taylor P.W., Soran N., Raubenheimer D. Lifespan and reproduction in Drosophila: new insights from nutritional geometry. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:2498-2503.
28. Lee K.P., Kim J.S., Min K.J. Sexual dimorphism in nutrient intake and lifespan is mediated by mating in Drosophila melanogaster. Anim. Behav. 2013, 86:987-992.
29. Lee W.-C., Micchelli C.A. Development and characterization of a chemically defined food for Drosophila. PLoS One 2013, 8:e67308.
30. Lushchak O.V., Gospodaryov D.V., Rovenko B.M., Glovyak A.D., Yurkevych I.S., Klyuba V.P., Shcherbij M.V., Lushchak V.I. Balance between macronutrients affects life span and functional senescence in fruit fly Drosophila melanogaster. J. Gerontol. Ser. A: Biol. Sci. Med. Sci. 2011, 67:118-125.
31. Mair W., Dillin A. Aging and survival: the genetics of life span extension by dietary restriction. Annu. Rev. Biochem. 2008, 77:727-754.
32. Mair W., Goymer P., Pletcher S.D., Partridge L. Demography of dietary restriction and death in Drosophila. Science 2003, 301:1731-1733.
33. Mair W., Piper M.D.W., Partridge L. Calories do not explain extension of lifespan by dietary restriction in Drosophila. PLoS Biol. 2005, 3:e223.
34. Maklakov A.A., Simpson S.J., Zajitschek F., Hall M.D., Dessmann J., Clissold F., Raubenheimer D., Bonduriansky R., Brooks R.C. Sex-specific fitness effects of nutrient intake on reproduction and lifespan. Curr. Biol. 2008, 18:1062-1066.
35. Meydani M. Nutrition interventions in aging and age-associated disease. Ann. N.Y. Acad. Sci. 2006, 928:226-235.
36. Min K.J., Tatar M. Restriction of amino acids extends lifespan in Drosophila melanogaster. Mech. Ageing Dev. 2006, 127:643-646.
37. Min K.J., Flatt T., Kulaots I., Tatar M. Counting calories in Drosophila diet restriction. Exp. Gerontol. 2007, 42:247-251.
38. Mirzaei H., Suarez J.A., Longo V.D. Protein and amino acid restriction, aging and disease: from yeast to humans. Trends Endocrinol. Metab. 2014, 25:558-566.
39. Mokdad A.H., Ford E.S., Bowman B.A., Dietz W.H., Vinicor F., Bales V.S., Marks J.S. Prevalence of obesity, diabetes, and obesity-related health risk factors, 2001. J. Am. Med. Assoc. 2003, 289:76-79.
40. Musselman L.P., Fink J.L., Narzinski K., Ramachandran P.V., Hathiramani S.S., Cagan R.L., Baranski T.J. A high-sugar diet produces obesity and insulin resistance in wild-type Drosophila. Dis. Models Mech. 2011, 4:842-849.
41. Na J., Musselman L.P., Pendse J., Baranski T.J., Bodmer R., Ocorr K., Cagan R. A Drosophila model of high sugar diet-induced cardiomyopathy. PLoS Genet. 2013, 9:e1003175.
42. O'Brien D.M., Min K.J., Larsen T., Tatar M. Use of stable isotopes to examine how dietary restriction extends Drosophila lifespan. Curr. Biol. 2008, 18:R155-156.
43. Partridge L., Pletcher S.D., Mair W. Dietary restriction, mortality trajectories, risk and damage. Mech. Ageing Dev. 2005, 126:35-41.
44. Piper M.D.W., Partidge L., Raubenheimer D., Simpson S.J. Dietary restriction and aging: a unifying perspective. Cell Metab. 2011, 14:154-160.
45. Piper M.D.W., Blanc E., Leitão-Gonçalves R., Yang M., He X., Linford N.J., Hoddinott M.P., Hopfen C., Soultoukis G.A., Niemeyer C., Kerr F., Pletcher S.D., Ribeiro C., Partridge L. A holidic medium for Drosophila melanogaster. Nat. Methods 2013, 11:100-105.
46. Pletcher S.D., Khazaeli A.A., Curtsinger J.W. Why do life spans differ? Partitioning mean longevity differences in terms of age-specific mortality parameters. J. Gerontol. Ser. A: Biol. Sci. Med. Sci. 2000, 55:B381-B389.
47. Pletcher S.D., Macdonald S.J., Marguerie R., Certa U., Stearns S.C., Goldstein D.B., Partridge L. Genome-wide transcript profiles in aging and calorically restricted Drosophila melanogaster. Curr. Biol. 2002, 12:712-723.
48. Promislow D.E.L. Senescence in natural populations of mammals: a comparative study. Evolution 1991, 45:1869-1887.
49. Promislow D.E.L., Tatar M., Pletcher S., Carey J.R. Below-threshold mortality: implication for studies in evolution, ecology and demography. J. Evol. Biol. 1999, 12:314-328.
50. R Development Core Team, 2012. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. .
51. Raubenheimer D., Lee K.P., Simpson S.J. Does Bertrand's rule apply to macronutrients?. Proc. Roy. Soc. London Ser. B 2005, 272:2429-2434.
52. Roberts D.B. Drosophila: A Practical Approach 2003, Oxford University Press, Oxford. second ed.
53. Sang J.H. The quantitative nutritional requirements of Drosophila melanogaster. J. Exp. Biol. 1956, 33:45-72.
54. Sanz A., Caro P., Barja G. Protein restriction without strong caloric restriction decreases mitochondrial oxygen radical production and oxidative DNA damage in rat liver. J. Bioenergy Biomembr. 2004, 36:545-552.
55. Shanley D.P., Kirkwood T.B. Calorie restriction and aging: a life-history analysis. Evolution 2000, 54:740-750.
56. Simpson S.J., Raubenheimer D. Caloric restriction and aging revisited: the need for a geometric analysis of the nutritional bases of aging. J. Gerontol. Ser. A: Biol. Sci. Med. Sci. 2007, 62:707-713.
57. Simpson S.J., Raubenheimer D. Macronutrient balance and lifespan. Aging 2009, 1:875-880.
58. Simpson S.J., Raubenheimer D. The Nature of Nutrition: A Unifying Framework from Animal Adaptation to Human Obesity 2012, Princeton University Press, Princeton, NJ.
59. Simpson S.J., Sibly R.M., Lee K.P., Behmer S.T., Raubenheimer D. Optimal foraging when regulating intake of multiple nutrients. Anim. Behav. 2004, 68:1299-1311.
60. Skorupa D.A., Dervisefendic A., Zwiener J., Pletcher S.D. Dietary composition specifies consumption, obesity, and lifespan in Drosophila melanogaster. Aging Cell 2008, 7:478-490.
61. Solon-Biet S.M., McMahon A.C., Ballard J.W.O., Ruohonen K., Wu L.E., Cogger V.C., Warren A., Huang X., Pichaud N., Melvin R.G., Gokarn R., Khalil M., Turner N., Cooney G.J., Sinclair D.A., Raubenheimer D., Le Couteur D.G., Simpson S.J. The ratio of macronutrients, not caloric intake, dictates cardiometabolic health, aging, and longevity in ad libitum-fed mice. Cell Metab. 2014, 19:418-430.
62. Tatar M. The plate half-full: status of research on the mechanisms of dietary restriction in Drosophila melanogaster. Exp. Gerontol. 2011, 46:363-368.
63. Tatar M., Carey J.R. Sex mortality differentials in the bean beetle: reframing the question. Am. Nat. 1994, 144:165-175.
64. Tatar M., Post S., Yu K. Nutrient control of Drosophila longevity. Trends Endocrinol. Metab. 2014, 25:509-517.
65. Toms J.D., Lesperance M.L. Piecewise regression: a tool for identifying ecological thresholds. Ecology 2003, 84:2034-2041.
66. Troen A.M., French E.E., Roberts J.F., Selhub J., Ordovas J.M., Parnell L.D., Lai C.-Q. Lifespan modification by glucose and methionine in Drosophila melanogaster fed a chemically defined diet. Age 2007, 29:29-39.
67. Weindruch R., Walford R.L. The Retardation of Aging and Disease by Dietary Restriction 1988, Charles C. Thomas, Springfield, IL.
68. Zwaan B., Bijlisma R., Hoekstra R.F. Direct selection on life span in Drosophila melanogaster. Evolution 1995, 49:649-659.