Social environment mediates cancer progression in Drosophila

The influence of oncogenic phenomena on the ecology and evolution of animal species is becoming an important research topic. Similar to host–pathogen interactions, cancer negatively affects host fitness, which should lead to the selection of host control mechanisms, including behavioral traits that best minimize the proliferation of malignant cells. Social behavior is suggested to influence tumor progression. While the ecological benefits of sociality in gregarious species are widely acknowledged, only limited data are available on the role of the social environment on cancer progression. Here, we exposed adult Drosophila, with colorectal-like tumors, to different social environments. We show how subtle variations in social structure have dramatic effects on the progression of tumor growth. Finally, we reveal that flies can discriminate between individuals at different stages of tumor development and selectively choose their social environment accordingly. Our study demonstrates the reciprocal links between cancer and social interactions and how sociality may impact health and fitness in animals and its potential implications for disease ecology.This work was supported by the ANR (Blanc project EVOCAN to F.T. and project DROSONET to F.M. and C.S.), the CNRS (INEE and INSB), Fondation ARC (1555286 to J.M. and F.M.), The French league against Cancer (M27218 to J.M.), IDEEV program (to F.M.), by an International Associated Laboratory Project France/Australia, by the French-Australian Science Innovation Collaboration Program Early Career Fellowship (B.U.), by André Hoffmann (Fondation MAVA), Fyssen Foundation (to F.M. and E.H. D.) and the French Government (fellowship 2015–155 to M.D.)

A Fatty Acid anabolic pathway in specialized-cells of female Drosophila remotely controls sperm delivery to the oocytes

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Fig 3 -

Oogenesis and mating: (A-B) Oenocytes (yellow dotted-line in A1-3) and stage 9–10 (*) and late (#) egg chambers (B1-3) of promE-gal4 females either control (A1, B1), or directing FASN3-RNAi (A2, B2) or CG6432-RNAi (A3, B3); tissues were dissected 10 days after mating; lipids and nuclei were labelled with Nile Red (red) and DAPI (silver), respectively; scale bars: 40μm (A1-3) and 100μm (B1-3). (C) Mating choice of single wild-type males in the presence of two females, one control and one expressing either FASN3-RNAi (purple) or CG6432-RNAi (green); bars represent the percentage of copulation with control (black) or RNAi-expressing (purple and green) females; males tend to prefer CG6432-RNAi females although not significantly; (N) represents the numbers of choice tests. (D-F) eggs (D) and pupae (E) from promE-gal4 females either control (black) or expressing FASN3-RNAi (purple) or CG6432-RNAi (green); three 3–5 day old females were mated with three males for one day, then, males were removed and females transferred in new tubes every day over a 6-day period; index of fertility (F) were evaluated as the ratio of prepupae to eggs (total numbers). Bars correspond to the mean values of 9–10 replicates and represent the numbers of eggs (D) and pupae (E) obtained from each egg collection.</p

Fig 5 -

Egg activation defect: (A-C) Eggs laid by promE-gal4 10-day old virgin females either control (A), or directing FASN3-RNAi (B) or CG6432-RNAi (C); eggs were collected for 2hrs and nuclei labeled with DAPI (silver); scale bars: 40μm. (D) Numbers of nuclei counted in imaged eggs. (E) Resistance to bleach lysis of eggs laid by promE-gal4 fertilized females either control (black), or directing FASN3-RNAi (purple) or CG6432-RNAi (green); bars correspond to the mean values from 27 independent tests, each containing 25 eggs per genotype. (F) Western-blotting to Smaug from protein extracts of dissected ovaries or eggs laid by promE-gal4 10-day old females either virgin or fertilized; ovaries and unfertilized eggs were from control females, fertilized eggs were from females either control or directing FASN3-RNAi or CG6432-RNAi. The bottom graph compares the means of four independent blots, where the band intensity of Smaug was normalized to that of the tubulin loading-control. (G-L) Confocal imaging of eggs laid by promE-gal4 10-day old fertilized females either control (G: metaphase-II first zygotic division), or directing CG6432-RNAi (two nuclei visible in H, three in I) or FASN3-RNAi (two nuclei visible in J, three in K and L; flagella connect two nuclei in L); nuclei are stained with DAPI (silver), flagella (L) with an anti-acetylated-tubulin (red). Arrows indicate nuclei likely of female (red) or male (bleu) origin. Collection for control and mutant eggs last 15 min and 1h, respectively; scale bars: 40 μm. Bleach dechorionation resulted in dramatic lysis of most eggs laid by FASN3- or CG6432-oeKD females.</p

Screening for sterility.

(A) 1407-gal4>UAS-RNAi females crossed to Canton-S males were let to lay eggs during six days (D) in three successive vials and the progeny was counted at adult emergence. The y-axis indicates total numbers (cumulative) of emerging flies after 2, 4 and 6 days. For each genotype, values are mean of emerging flies from 20 females maintained in separate tubes. (B) Reciprocal crosses to test male fertility. (PDF)</p