Sex difference in pathology of the ageing gut mediates the greater response of female lifespan to dietary restriction

eLife

Volumn 5, Issue FEBRUARY2016, 2016, Pages

  Regan, Jennifer C ^a   Khericha, Mobina ^a   Dobson, Adam J ^a   Bolukbasi, Ekin ^a   Rattanavirotkul, Nattaphong ^a   Partridge, Linda ^a,b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b MAX PLANCK INSTITUTE FOR BIOLOGY OF AGEING   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AGING; ARTICLE; ASSAY; BACTERIAL LOAD; DETERIORATION; DIET RESTRICTION; DROSOPHILA; FEEDING ASSAY; FEMALE; GENDER; GUT DETERIORATION; IMMUNOHISTOCHEMISTRY; INTESTINAL STEM CELL; INTESTINE; INTESTINE INFECTION; LIFESPAN; LONGEVITY; MALE; MOUTH INFECTION; NONHUMAN; PROTEIN INTAKE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEX DIFFERENCE; SURVIVAL ASSAY; XENOBIOTIC STRESS; ANIMAL; DIET; GASTROINTESTINAL TRACT; PHYSIOLOGY; PROCEDURES; SEXUAL DEVELOPMENT;

AGING; ANIMALS; DIET; DROSOPHILA; FEMALE; GASTROINTESTINAL TRACT; LONGEVITY; MALE; SEX CHARACTERISTICS;

EID: 84961904341     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.10956     Document Type: Article

References (60)

1. Abad-Díez JM, Calderón-Larrañaga A, Poncel-Falcó A, Poblador-Plou B, Calderón-Meza J, Sicras-Mainar M, Clerencia-Sierra M, Prados-Torres A. 2014. Age and gender differences in the prevalence and patterns of multimorbidity in the older population. BMC Geriatrics 14:75. doi: 10.1186/1471-2318-14-75
2. Alpatov WW. 1930. Phenotypical variation in body and cell size of Drosophila melanogaster. Biological Bulletin 58:85-103. doi: 10.2307/1537121
3. Ayyaz A, Li H, Jasper H. 2015. Haemocytes control stem cell activity in the Drosophila intestine. Nature Cell Biology 17:736-748. doi: 10.1038/ncb3174
4. Barnett K, Mercer SW, Norbury M, Watt G, Wyke S, Guthrie B. 2012. Epidemiology of multimorbidity and implications for health care, research, and medical education: a cross-sectional study. The Lancet 380:37-43.doi: 10.1016/S0140-6736(12)60240-2
5. Basset A, Khush RS, Braun A, Gardan L, Boccard F, Hoffmann JA, Lemaitre B. 2000. The phytopathogenic bacteria erwinia carotovora infects Drosophila and activates an immune response. Proceedings of the National Academy of Sciences of the United States of America 97:3376-3381. doi: 10.1073/pnas.97.7.3376
6. Biteau B, Hochmuth CE, Jasper H. 2008. JNK activity in somatic stem cells causes loss of tissue homeostasis in the aging Drosophila gut. Cell Stem Cell 3:442-455. doi: 10.1016/j.stem.2008.07.024
7. Biteau B, Karpac J, Supoyo S, DeGennaro M, Lehmann R, Jasper H. 2010. Lifespan extension by preserving proliferative homeostasis in Drosophila. PLoS Genetics 6:e1001159-e1001159. doi:10.1371/journal.pgen.1001159
8. 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 Metabolism 11:35-46. doi: 10.1016/j.cmet.2009.11.010
9. Boyle M, Wong C, Rocha M, Jones DL. 2007. Decline in self-renewal factors contributes to aging of the stem cell niche in the Drosophila testis. Cell Stem Cell 1:470-478. doi: 10.1016/j.stem.2007.08.002
10. Bretman A, Westmancoat JD, Gage MJ, Chapman T. 2011. Males use multiple, redundant cues to detect mating rivals. Current Biology 21:617-622. doi: 10.1016/j.cub.2011.03.008
11. Broderick NA, Buchon N, Lemaitre B. 2014. Microbiota-induced changes in drosophila melanogaster host gene expression and gut morphology. mBio 5:e01117-14. doi: 10.1128/mBio.01117-14
12. Buchon N, Broderick NA, Poidevin M, Pradervand S, Lemaitre B. 2009. Drosophila intestinal response to bacterial infection: activation of host defense and stem cell proliferation. Cell Host & Microbe 5:200-211. doi: 10.1016/j.chom.2009.01.003
13. Buchon N, Osman D, David FP, Fang HY, Boquete JP, Deplancke B, Lemaitre B. 2013. Morphological and molecular characterization of adult midgut compartmentalization in drosophila. Cell Reports 3:1725-1738. doi: 10.1016/j.celrep.2013.04.001
14. Camus MF, Clancy DJ, Dowling DK. 2012. Mitochondria, maternal inheritance, and male aging. Current Biology 22:1717-1721. doi: 10.1016/j.cub.2012.07.018
15. Chang L, Heitkemper MM. 2002. Gender differences in irritable bowel syndrome. Gastroenterology 123:1686-1701. doi: 10.1053/gast.2002.36603
16. Chatterjee M, Ip YT. 2009. Pathogenic stimulation of intestinal stem cell response in Drosophila. Journal of Cellular Physiology 220:664-671. doi: 10.1002/jcp.21808
17. Choi NH, Kim JG, Yang DJ, Kim YS, Yoo M. 2008. Age-related changes in Drosophila midgut are associated with PVF2, a PDGF/VEGF-like growth factor. Aging Cell 7:318-334. doi: 10.1111/j.1474-9726.2008.00380.x
18. Choi NH, Lucchetta E, Ohlstein B. 2011. Nonautonomous regulation of Drosophila midgut stem cell proliferation by the insulin-signaling pathway. Proceedings of the National Academy of Sciences of the United States of America 108:18702-18707. doi: 10.1073/pnas.1109348108
19. Clancy DJ, Gems D, Harshman LG, Oldham S, Stocker H, Hafen E, Leevers SJ, Partridge L. 2001. Extension of life-span by loss of CHICO, a Drosophila insulin receptor substrate protein. Science 292:104-106. doi: 10.1126/science.1057991
20. Clark RI, Salazar A, Yamada R, Fitz-Gibbon S, Morselli M, Alcaraz J, Rana A, Rera M, Pellegrini M, William WJ, Walker DW. 2015. Distinct shifts in microbiota composition during Drosophila aging impair intestinal function and drive mortality. Cell Reports 12:1656-1667. doi: 10.1016/j.celrep.2015.08.004
21. Dutta D, Buchon N, Xiang J, Edgar BA. 2015. Regional cell specific RNA expression profiling of FACS isolated Drosophila intestinal cell populations. Current Protocols in Stem Cell Biology 34:2F21-2F214. doi: 10.1002/9780470151808.sc02f02s34
22. Fan X, Liang Q, Lian T, Wu Q, Gaur U, Li D, Yang D, Mao X, Jin Z, Li Y, Yang M. 2015. Rapamycin preserves gut homeostasis during Drosophila aging. Oncotarget 6:35274-35283. doi: 10.18632/oncotarget.5895
23. Fontana L, Partridge L. 2015. Promoting health and longevity through diet: from model organisms to humans. Cell 161:106-118. doi: 10.1016/j.cell.2015.02.020
24. French V, Feast M, Partridge L. 1998. Body size and cell size in Drosophila: the developmental response to temperature. Journal of Insect Physiology 44:1081-1089. doi: 10.1016/S0022-1910(98)00061-4
25. Gendrin M, Welchman DP, Poidevin M, Hervé M, Lemaitre B. 2009. Long-range activation of systemic immunity through peptidoglycan diffusion in Drosophila. PLoS Pathogens 5:e1000694. doi: 10.1371/journal.ppat.1000694
26. Guo L, Karpac J, Tran SL, Jasper H. 2014. PGRP-SC2 promotes gut immune homeostasis to limit commensal dysbiosis and extend lifespan. Cell 156:109-122. doi:10.1016/j.cell.2013.12.018
27. Ha EM, Oh CT, Bae YS, Lee WJ. 2005. A direct role for dual oxidase in Drosophila gut immunity. Science 310: 847-850. doi: 10.1126/science.1117311
28. Hammond KA. 1997. Adaptation of the maternal intestine during lactation. Journal of Mammary Gland Biology and Neoplasia 2:243-252. doi: 10.1023/A:1026332304435
29. Hur JH, Bahadorani S, Graniel J, Koehler CL, Ulgherait M, Rera M, Jones DL, Walker DW. 2013. Increased longevity mediated by yeast NDI1 expression in Drosophila intestinal stem and progenitor cells. Aging 5:662.
30. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. 2011. Global cancer statistics. CA: A Cancer Journal for Clinicians 61:69-90. doi: 10.3322/caac.20107
31. Jiang H, Patel PH, Kohlmaier A, Grenley MO, McEwen DG, Edgar BA. 2009. Cytokine/Jak/Stat signaling mediates regeneration and homeostasis in the Drosophila midgut. Cell 137:1343-1355. doi: 10.1016/j.cell.2009.05.014
32. Kim SE, Paik HY, Yoon H, Lee JE, Kim N, Sung MK. 2015. Sex-and gender-specific disparities in colorectal cancer risk. World Journal of Gastroenterology 21:5167. doi: 10.3748/wjg.v21.i17.5167
33. Lee G, Hall JC, Park JH. 2002. Doublesex gene expression in the central nervous system of Drosophila melanogaster. Journal of Neurogenetics 16:229-248. doi: 10.1080/01677060216292
34. Lee K, Simpson S, Clissold F, Brooks R, Ballard W, Taylor P, Soran N, Raubenheimer D. 2008. Lifespan and reproduction in Drosophila: new insights from nutritional geometry. Proceedings of the National Academy of Sciences of the United States of America 105:2498-2503. doi: 10.1073/pnas.0710787105
35. Mackenzie DK, Bussière LF, Tinsley MC. 2011. Senescence of the cellular immune response in Drosophila melanogaster. Experimental Gerontology 46:853-859. doi: 10.1016/j.exger.2011.07.004
36. Magwere T, Chapman T, Partridge L. 2004. Sex differences in the effect of dietary restriction on life span and mortality rates in female and male Drosophila melanogaster. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences 59:B3-B9. doi:10.1093/gerona/59.1.B3
37. Micchelli CA, Perrimon N. 2006. Evidence that stem cells reside in the adult Drosophila midgut epithelium. Nature 439:475-479. doi: 10.1038/nature04371
38. Ohlstein B, Spradling A. 2006. The adult Drosophila posterior midgut is maintained by pluripotent stem cells. Nature 439:470-474. doi:10.1038/nature04333
39. O’Brien LE, Soliman SS, Li X, Bilder D. 2011. Altered modes of stem cell division drive adaptive intestinal growth. Cell 147:603-614. doi: 10.1016/j.cell.2011.08.048
40. Partridge L, Andrews R. 1985. The effect of reproductive activity on the longevity of male Drosophila melanogaster is not caused by an acceleration of ageing. Journal of Insect Physiology 31:393-395. doi: 10.1016/0022-1910(85)90084-8
41. Patel PH, Dutta D, Edgar BA. 2015. Niche appropriation by Drosophila intestinal stem cell tumours. Nature Cell Biology 17:1182-1192. doi: 10.1038/ncb3214
42. Petkau K, Parsons BD, Duggal A, Foley E. 2014. A deregulated intestinal cell cycle program disrupts tissue homeostasis without affecting longevity in Drosophila. Journal of Biological Chemistry 289:28719-28729. doi: 10.1074/jbc.M114.578708
43. Regan JC, Partridge L. 2013. Gender and longevity: Why do men die earlier than women? Comparative and experimental evidence. Best Practice & Research Clinical Endocrinology & Metabolism 27:467-479. doi: 10.1016/j.beem.2013.05.016
44. Reiff T, Jacobson J, Cognigni P, Antonello Z, Ballesta E, Tan KJ, Yew JY, Dominguez M, Miguel-Aliaga I. 2015. Endocrine remodelling of the adult intestine sustains reproduction in Drosophila. eLife 4:e06930. doi: 10.7554/eLife.06930
45. Rera M, Azizi MJ, Walker DW. 2013. Organ-specific mediation of lifespan extension: more than a gut feeling? Ageing Research Reviews 12:436-444. doi: 10.1016/j.arr.2012.05.003
46. Rera M, Bahadorani S, Cho J, Koehler CL, Ulgherait M, Hur JH, Ansari WS, Lo T, Jones DL, Walker DW. 2011. Modulation of longevity and tissue homeostasis by the Drosophila PGC-1 homolog. Cell Metabolism 14:623-634. pp.. doi: 10.1016/j.cmet.2011.09.013
47. Rera M, Clark RI, Walker DW. 2012. Intestinal barrier dysfunction links metabolic and inflammatory markers of aging to death in Drosophila. Proceedings of the National Academy of Sciences of the United States of America 109:21528-21533. doi: 10.1073/pnas.1215849110
48. Salz HK. 2011. Sex determination in insects: a binary decision based on alternative splicing. Current Opinion in Genetics & Development 21:395-400. doi: 10.1016/j.gde.2011.03.001
49. Skorupa D, Dervisefendic A, Zwiener J, Pletcher S. 2008. Dietary composition specifies consumption, obesity, and lifespan in Drosophila melanogaster. Aging Cell 7:478-490. doi: 10.1111/j.1474-9726.2008.00400.x
50. Slack C, Giannakou ME, Foley A, Goss M, Partridge L. 2011. DFOXO-independent effects of reduced insulin-like signaling in Drosophila. Aging Cell 10:735-748. doi: 10.1111/j.1474-9726.2011.00707.x
51. Solon-Biet SM, Walters KA, Simanainen UK, McMahon AC, Ruohonen K, Ballard JWO, Raubenheimer D, Handelsman DJ, Le Couteur DG, Simpson SJ. 2015. Macronutrient balance, reproductive function, and lifespan in aging mice. Proceedings of the National Academy of Sciences of the United States of America 112:3481-3486. doi:10.1073/pnas.1422041112
52. Speakman JR. 2008. The physiological costs of reproduction in small mammals. Philosophical Transactions of the Royal Society B: Biological Sciences 363:375-398. doi:10.1098/rstb.2007.2145
53. Tatar M, Kopelman A, Epstein D, Tu MP, Yin CM, Garofalo RS. 2001. A mutant Drosophila insulin receptor homolog that extends life-span and impairs neuroendocrine function. Science 292:107-110. doi: 10.1126/science.1057987
54. Tu MP, Epstein D, Tatar M. 2002. The demography of slow aging in male and female Drosophila mutant for the insulin-receptor substrate homologue chico. Aging Cell 1:75-80. doi: 10.1046/j.1474-9728.2002.00010.x
55. Ulgherait M, Rana A, Rera M, Graniel J, Walker DW. 2014. AMPK modulates tissue and organismal aging in a non-cell-autonomous manner. Cell Reports 8:1767-1780. doi: 10.1016/j.celrep.2014.08.006
56. Veenstra JA, Sellami A. 2008. Regulatory peptides in fruit fly midgut. Cell and Tissue Research 334:499-516. doi: 10.1007/s00441-008-0708-3
57. Vincent CM, Sharp NP. 2014. Sexual antagonism for resistance and tolerance to infection in Drosophila melanogaster. Proceedings of the Royal Society B: Biological Sciences of the United States of America 281: 2014-0987. doi: 10.1098/rspb.2014.0987
58. Wang L, Karpac J, Jasper H. 2014. Promoting longevity by maintaining metabolic and proliferative homeostasis. Journal of Experimental Biology 217:109-118. doi:10.1242/jeb.089920
59. Wernli KJ, Wang Y, Zheng Y, Potter JD, Newcomb PA. 2009. The relationship between gravidity and parity and colorectal cancer risk. Journal of Women’s Health 18:995-1001. doi: 10.1089/jwh.2008.1068
60. Zaidman-Rémy A, Hervé M, Poidevin M, Pili-Floury S, Kim MS, Blanot D, Oh BH, Ueda R, Mengin-Lecreulx D, Lemaitre B. 2006. The Drosophila amidase PGRP-LB modulates the immune response to bacterial infection. Immunity 24:463-473. doi:10.1016/j.immuni.2006.02.012