Host manipulation by cancer cells: Expectations, facts, and therapeutic implications

Tissot, Tazzio; Arnal, Audrey; Jacqueline, Camille M.; Poulin, Robert; Lefèvre, Thierry; Mery, Frédéric; Renaud, François; Roche, Benjamín; Massol, François; Ewald, Paul W.; Tasiemski, Aurélie; Újvári, Beáta; Thomas, Frédéric

doi:10.1002/bies.201500163

Cited by 20 publications

(22 citation statements)

References 89 publications

(91 reference statements)

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“…In later stages, the “damage is done” and cancer will be too advanced to maximally reap these benefits. These findings raise questions on the very early impact of internal oncogenic process on individual behavior and natural selection pressures on this process 45 . While, at this stage, tumors are not found to affect the survival of flies, cancer may affect fitness in other ways (e.g., reproductive competitiveness, vulnerability to predators etc).…”

Section: Discussionmentioning

confidence: 98%

Social environment mediates cancer progression in Drosophila

et al. 2018

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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.

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Section: Discussionmentioning

confidence: 98%

Social environment mediates cancer progression in Drosophila

et al. 2018

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“…Moreover, we observed that cancerous flies exhibit strong social attraction towards each other, especially at the beginning of tumor development. This raises questions on the very early impact of internal oncogenic process on individual behavior and natural selection pressures on this process [34]. For example, such attraction could be the result of an adaptive process, which reduces cancer progression.…”

Section: Discussionmentioning

confidence: 99%

An interaction between cancer progression and social environment in Drosophila

et al. 2017

Preprint

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The influence of oncogenic phenomena on the ecology and evolution of animal species is fast 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 one such trait, which is suggested to influence cancer 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. First, we show that cancerous flies kept in complete isolation exhibit increased tumor progression. Yet, more surprisingly, we find that cancerous flies, kept in groups with other noncancerous individuals, also develop tumors at a faster rate compared to those kept with other cancerous conspecifics, suggesting a strong impact of social group composition on cancer growth. Finally, we show that flies can discriminate between individuals at different stages of tumor growth and selectively choose their social environment accordingly. Control flies actively avoid flies with cancer but only at the later stages of tumor development, whereas cancerous flies display strong social interactions with cancerous flies in the early stages of tumor growth. Our study demonstrates the reciprocal links between cancer and social interactions, as well as highlighting how sociality impacts health and fitness in animals and its potential implications for disease ecology and ecosystem dynamics.

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“…Parasite-induced alterations of host phenotype have been reported in a wide range of protozoan and metazoan parasites (Hughes et al, 2012;Moore, 2002). Tissot et al (2016) recently explored this phenomenon in the context of malignancies, arguing that oncogenic selection, even though it occurs on a maximum of a few decades for the majority of cancers Ujvari, Gatenby, & Thomas, 2016), could favor variants that are able to manipulate their host similar to "true" parasitic/symbiotic organisms. Concerning eating behaviors, cancer cells could, for instance, modify host appetite in a quantitative/qualitative way that is favorable for the tumor, by inducing cravings for foods that give malignant cells fitness advantages Box 1 Why do changes in diet occur for cancer patients?…”

Section: Tumor Manipulationmentioning

confidence: 99%

“…Other factors, like chronic pain, analgesic treatments, tiredness, or cancer-associated depression, fear, and anxiety are known to result in a decreased appetite. over healthy cells, and/or inducing dysphoria, a general feeling of unease, until the hosts prioritize foods that enhance their fitness (Tissot et al, 2016). Manipulating host preference for novel food would be expected notably if malignant cells need nutrients that are not routinely consumed by the host.…”

Section: Tumor Manipulationmentioning

confidence: 99%

“…() recently explored this phenomenon in the context of malignancies, arguing that oncogenic selection, even though it occurs on a maximum of a few decades for the majority of cancers (Arnal et al., ; Ujvari, Gatenby, & Thomas, ), could favor variants that are able to manipulate their host similar to “true” parasitic/symbiotic organisms. Concerning eating behaviors, cancer cells could, for instance, modify host appetite in a quantitative/qualitative way that is favorable for the tumor, by inducing cravings for foods that give malignant cells fitness advantages over healthy cells, and/or inducing dysphoria, a general feeling of unease, until the hosts prioritize foods that enhance their fitness (Tissot et al., ). Manipulating host preference for novel food would be expected notably if malignant cells need nutrients that are not routinely consumed by the host.…”

Section: Introductionmentioning

confidence: 99%

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Changes in diet associated with cancer: An evolutionary perspective

Thomas

Rome

Mery

et al. 2017

Evolutionary Applications

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Changes in diet are frequently correlated with the occurrence and progression of malignant tumors (i.e., cancer) in both humans and other animals, but an integrated conceptual framework to interpret these changes still needs to be developed. Our aim is to provide a new perspective on dietary changes in tumor‐bearing individuals by adapting concepts from parasitology. Dietary changes may occur alongside tumor progression for several reasons: (i) as a pathological side effect with no adaptive value, (ii) as the result of self‐medication by the host to eradicate the tumor and/or to slow down its progression, (iii) as a result of host manipulation by the tumor that benefits its progression, and finally (iv) as a host tolerance strategy, to alleviate and repair damages caused by tumor progression. Surprisingly, this tolerance strategy can be beneficial for the host even if diet changes are beneficial to tumor progression, provided that cancer‐induced death occurs sufficiently late (i.e., when natural selection is weak). We argue that more data and a unifying evolutionary framework, especially during the early stages of tumorigenesis, are needed to understand the links between changes in diet and tumor progression. We argue that a focus on dietary changes accompanying tumor progression can offer novel preventive and therapeutic strategies against cancer.

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Host manipulation by cancer cells: Expectations, facts, and therapeutic implications

Cited by 20 publications

References 89 publications

Social environment mediates cancer progression in Drosophila

Social environment mediates cancer progression in Drosophila

An interaction between cancer progression and social environment in Drosophila

Changes in diet associated with cancer: An evolutionary perspective

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