The endosymbiont Wolbachia increases insulin/IGF-like signalling in Drosophila

被引:104
作者
Ikeya, Tomoatsu [1 ]
Broughton, Susan [1 ]
Alic, Nazif [1 ]
Grandison, Richard [1 ]
Partridge, Linda [1 ]
机构
[1] UCL, Inst Healthy Ageing & GEE, London WC1E 6BT, England
基金
英国惠康基金;
关键词
Drosophila; insulin-like signalling; Wolbachia; REGULATES LIFE-SPAN; CYTOPLASMIC INCOMPATIBILITY; FAT-BODY; CAENORHABDITIS-ELEGANS; DIETARY RESTRICTION; LIPID-METABOLISM; MELANOGASTER; RECEPTOR; GROWTH; INFECTION;
D O I
10.1098/rspb.2009.0778
中图分类号
Q [生物科学];
学科分类号
07 ; 0710 ; 09 ;
摘要
Insulin/IGF-like signalling (IIS) is an evolutionarily conserved pathway that has diverse functions in multi-cellular organisms. Mutations that reduce IIS can have pleiotropic effects on growth, development, metabolic homeostasis, fecundity, stress resistance and lifespan. IIS is also modified by extrinsic factors. For instance, in the fruitfly Drosophila melanogaster, both nutrition and stress can alter the activity of the pathway. Here, we test experimentally the hypothesis that a widespread endosymbiont of arthropods, Wolbachia pipientis, can alter the degree to which mutations in genes encoding IIS components affect IIS and its resultant phenotypes. Wolbachia infection, which is widespread in D. melanogaster in nature and has been estimated to infect 30 per cent of strains in the Bloomington stock centre, can affect broad aspects of insect physiology, particularly traits associated with reproduction. We measured a range of IIS-related phenotypes in flies ubiquitously mutant for IIS in the presence and absence of Wolbachia. We show that removal of Wolbachia further reduces IIS and hence enhances the mutant phenotypes, suggesting that Wolbachia normally acts to increase insulin signalling. This effect of Wolbachia infection on IIS could have an evolutionary explanation, and has some implications for studies of IIS in Drosophila and other organisms that harbour endosymbionts.
引用
收藏
页码:3799 / 3807
页数:9
相关论文
共 74 条
[1]   Tetracycline treatment influences mitochondrial metabolism and mtDNA density two generations after treatment in Drosophila [J].
Ballard, J. W. O. ;
Melvin, R. G. .
INSECT MOLECULAR BIOLOGY, 2007, 16 (06) :799-802
[2]   Optimization of dietary restriction protocols in Drosophila [J].
Bass, Timothy M. ;
Grandison, Richard C. ;
Wong, Richard ;
Martinez, Pedro ;
Partridge, Linda ;
Piper, Matthew D. W. .
JOURNALS OF GERONTOLOGY SERIES A-BIOLOGICAL SCIENCES AND MEDICAL SCIENCES, 2007, 62 (10) :1071-1081
[3]   Autonomous control of cell and organ size by CHICO, a Drosophila homolog of vertebrate IRS1-4 [J].
Böhni, R ;
Riesgo-Escovar, J ;
Oldham, S ;
Brogiolo, W ;
Stocker, H ;
Andruss, BF ;
Beckingham, K ;
Hafen, E .
CELL, 1999, 97 (07) :865-875
[4]  
Bourtzis K, 1996, GENETICS, V144, P1063
[5]   An evolutionarily conserved function of the Drosophila insulin receptor and insulin-like peptides in growth control [J].
Brogiolo, W ;
Stocker, H ;
Ikeya, T ;
Rintelen, F ;
Fernandez, R ;
Hafen, E .
CURRENT BIOLOGY, 2001, 11 (04) :213-221
[6]   Longer lifespan, altered metabolism, and stress resistance in Drosophila from ablation of cells making insulin-like ligands [J].
Broughton, SJ ;
Piper, MDW ;
Ikeya, T ;
Bass, TM ;
Jacobson, J ;
Driege, Y ;
Martinez, P ;
Hafen, E ;
Withers, DJ ;
Leevers, SJ ;
Partridge, L .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2005, 102 (08) :3105-3110
[7]   Evidence for Metabolic Provisioning by a Common Invertebrate Endosymbiont, Wolbachia pipientis, during Periods of Nutritional Stress [J].
Brownlie, Jeremy C. ;
Cass, Bodil N. ;
Riegler, Markus ;
Witsenburg, Joris J. ;
Iturbe-Ormaetxe, Inaki ;
McGraw, Elizabeth A. ;
O'Neill, Scott L. .
PLOS PATHOGENS, 2009, 5 (04)
[8]   Control of growth by the somatropic axis: Growth hormone and the insulin-like growth factors have related and independent roles [J].
Butler, AA ;
Le Roith, D .
ANNUAL REVIEW OF PHYSIOLOGY, 2001, 63 :141-164
[9]   Extension of life-span by loss of CHICO, a Drosophila insulin receptor substrate protein [J].
Clancy, DJ ;
Gems, D ;
Harshman, LG ;
Oldham, S ;
Stocker, H ;
Hafen, E ;
Leevers, SJ ;
Partridge, L .
SCIENCE, 2001, 292 (5514) :104-106
[10]   Widespread prevalence of Wolbachia in laboratory stocks and the implications for Drosophila research [J].
Clark, ME ;
Anderson, CL ;
Cande, J ;
Karr, TL .
GENETICS, 2005, 170 (04) :1667-1675