Authors: Frédéric Thomas; Klara Asselin; Nick MacDonald; Lionel Brazier; Jordan Meliani; Beata Ujvari; Antoine Marie Dujon

Source: Comptes Rendus, Biologies (Nov 2024)

Abstract

Cancer is a biological process that emerged at the end of the Precambrian era with the rise of multicellular organisms. Traditionally, cancer has been viewed primarily as a disease relevant to human and domesticated animal health, attracting attention mainly from oncologists.

In recent years, however, the community of ecologists and evolutionary biologists has recognized the pivotal role of cancer-related issues in the evolutionary paths of various species, influencing multiple facets of their biology. It has become evident that overlooking these issues is untenable for a comprehensive understanding of species evolution and ecosystem functioning.

In this article, we highlight some significant advancements in this field, also underscoring the pressing need to consider reciprocal interactions not only between cancer cells and their hosts but also with all entities comprising the holobiont. This reflection gains particular relevance as ecosystems face increasing pollution from mutagenic substances, resulting in a resurgence of cancer cases in wildlife.

Authors: Natasha Yadav, Anurag Nath, Pushplata Prasad Singh, Himadri B. Bohidar, Damien L. Callahan, Antoine M. Dujon, Luis O. B. Afonso and Aaron G. Schultz

Source: Environmental Science: Nano (Oct 2024)

Abstract

The rapid advancement of nanotechnology has led to the increasing application of metal oxide nanoparticles (NPs) in various fields, including agriculture, where they offer potential benefits such as improved nutrient delivery and pest control. However, concerns about their environmental impact necessitate a comprehensive assessment of their safety.

This study investigated the potential toxic effects of iron-based nanoparticles (NPs) on freshwater planarian and the influence of abiotic factors such as humic acid (HA) and UV exposure on their toxicity. Three different types of iron-based NPs were tested, including commercially available Sigma iron oxide magnetic NPs (Sig_IOMNPs), biologically synthesized BS_IOMNPs and Zn–Fe and bulk FeSO₄. Sigma and biogenic nanoparticles had predominantly magnetite (Fe₃O₄) structure whereas Zn–Fe possessed a bimetallic conformation. Interaction of these NPs with abiotic factors (HA and UV light) led to an increase in their hydrodynamic diameter.

In contrast to the commercial sources (Sig_IOMNPs and bulk FeSO₄), the biologically synthesized NPs did not cause any acute or sublethal toxicity to the planarian when alone or in combination with HA and UV. These results suggest that biologically synthesized iron-based NPs (Zn–Fe and BS_IOMNPs) may be a safe alternative to conventional bulk iron-based fertilizers.

This study highlights the importance of investigating the physicochemical changes of NPs in environmentally realistic conditions and assessing their potential toxicity to aquatic organisms. These findings can contribute to the development of safe and sustainable agricultural practices, promoting the use of iron-based NPs as a new generation of fertilizers.

Authors: Sophie Tissot, Jordan Meliani, Matthew Chee, Aurora M. Nedelcu, Justine Boutry, Jácint Tökölyi, Rodrigo Hamede, Benjamin Roche, Beata Ujvari, Frédéric Thomas & Antoine M. Dujon

Source: Scientific Reports (Sep 2024)

Abstract

Recent theoretical advances in the One Health approach have suggested that cancer pathologies should be given greater consideration, as cancers often render their hosts more vulnerable to infectious agents, which could turn them into super spreaders within ecosystems. Although biologically plausible, this hypothesis has not yet been validated experimentally.

Using a community of cnidarians of the Hydra genus (Hydra oligactis, Hydra viridissima, Hydra vulgaris) and a commensal ciliate species (Kerona pediculus) that colonizes them, we tested whether tumoral polyps of H. oligactis, compared to healthy ones, played an amplifying role in the number of ciliates, potentially resulting in a higher likelihood of infection for other community members through spillovers. Our results indicate that K. pediculus has a higher proliferation rate on tumoral polyps of H. oligactis than on healthy ones, which results in the infestation of other hydras. However, the magnitude of the spillover differed between recipient species.

This study provides to our knowledge the first elements of proof of concept that tumoral individuals in communities could act as super spreaders of symbionts within and between species, and thus affect biotic interactions and dynamics in ecosystems.

Authors: Margaux Bieuville, Antoine M. Dujon, Nynke Raven, Beata Ujvari, Pascal Pujol, Zahra Eslami-S, Catherine Alix Panabières, Jean-Pascal Capp, Frédéric Thomas

Source: Evolutionary Applications (Oct 2024)

Abstract

While it is recognised that most, if not all, multicellular organisms harbour neoplastic processes within their bodies, the timing of when these undesirable cell proliferations are most likely to occur and progress throughout the organism’s lifetime remains only partially documented. Due to the different mechanisms implicated in tumourigenesis, it is highly unlikely that this probability remains constant at all times and stages of life.

In this article, we summarise what is known about this variation, considering the roles of age, season and circadian rhythm. While most studies requiring that level of detail be done on humans, we also review available evidence in other animal species. For each of these timescales, we identify mechanisms or biological functions shaping the variation. When possible, we show that evolutionary processes likely played a role, either directly to regulate the cancer risk or indirectly through trade-offs.

We find that neoplastic risk varies with age in a more complex way than predicted by early epidemiological models: rather than resulting from mutations alone, tumour development is dictated by tissue- and age-specific processes. Similarly, the seasonal cycle can be associated with risk variation in some species with life-history events such as sexual competition or mating being timed according to the season. Lastly, we show that the circadian cycle influences tumourigenesis in physiological, pathological and therapeutic contexts. We also highlight two biological functions at the core of these variations across our three timescales: immunity and metabolism. Finally, we show that our understanding of the entanglement between tumourigenic processes and biological cycles is constrained by the limited number of species for which we have extensive data.

Improving our knowledge of the periods of vulnerability to the onset and/or progression of (malignant) tumours is a key issue that deserves further investigation, as it is key to successful cancer prevention strategies.

Authors: Frédéric Thomas, James DeGregori, Andriy Marusyk, Antoine M Dujon, Beata Ujvari, Jean-Pascal Capp, Robert Gatenby, Aurora M Nedelcu

Source: Evolution, Medicine, and Public Health (Sep 2024)

Abstract

Tumorigenesis is commonly attributed to Darwinian processes involving natural selection among cells and groups of cells. However, progressing tumors are those that also achieve an appropriate group phenotypic composition (GPC).

Yet, the selective processes acting on tumor GPCs are distinct from that associated with classical Darwinian evolution (i.e. natural selection based on differential reproductive success) as tumors are not genuine evolutionary individuals and do not exhibit heritable variation in fitness.

This complex evolutionary scenario is analogous to the recently proposed concept of ‘selection for function’ invoked for the evolution of both living and non-living systems.

Therefore, we argue that it is inaccurate to assert that Darwinian processes alone account for all the aspects characterizing tumorigenesis and cancer progression; rather, by producing the genetic and phenotypic diversity required for creating novel GPCs, these processes fuel the evolutionary success of tumors that is dependent on selection for function at the tumor level.

Authors: Sophie Tissot, Jordan Meliani, Justine Boutry, Lionel Brazier, Jácint Tökölyi, Benjamin Roche, Beata Ujvari, Aurora M. Nedelcu, Frédéric Thomas and Antoine M. Dujon

Source: Proceedings of the Royal Society B: Biological Sciences (Sep 2024)

Abstract

While most cancers are not transmissible, there are rare cases where cancer cells can spread between individuals and even across species, leading to epidemics. Despite their significance, the origins of such cancers remain elusive due to late detection in host populations. Using Hydra oligactis, which exhibits spontaneous tumour development that in some strains became vertically transmitted, this study presents the first experimental observation of the evolution of a transmissible tumour.

Specifically, we assessed the initial vertical transmission rate of spontaneous tumours and explored the potential for optimizing this rate through artificial selection. One of the hydra strains, which evolved transmissible tumours over five generations, was characterized by analysis of cell type and bacteriome, and assessment of life-history traits.

Our findings indicate that tumour transmission can be immediate for some strains and can be enhanced by selection. The resulting tumours are characterized by overproliferation of large interstitial stem cells and are not associated with a specific bacteriome. Furthermore, despite only five generations of transmission, these tumours induced notable alterations in host life-history traits, hinting at a compensatory response.

This work, therefore, makes the first contribution to understanding the conditions of transmissible cancer emergence and their short-term consequences for the host.

Authors: Emy Beaumont, Jacques Brodeur, Frédéric Thomas, Antoine M. Dujon, Sonia Lupien

Source: Psychoneuroendocrinology (Feb 2024)

Abstract

Background: Schizophrenia is a mental illness that affects approximately 24 million people worldwide. Vulnerability to schizophrenia has been linked by some epidemiologic studies to Toxoplasma gondii (TG), an intracellular protozoan parasite that can form permanent cysts in the brain. Knowing that stress can increase the permeability of the blood-brain barrier, we hypothesized that stress could facilitate brain infection by TG, thus promoting the development of schizophrenia symptoms. The objective of this study was to test if different types of stress: acute stress (salivary cortisol), chronic stress (hair cortisol), or childhood adversity (Childhood Experiences of Violence Questionnaire), modulate the link between TG (TG antibodies in serum) and schizophrenia.

Method: Data and biospecimens (saliva, hair and serum) from 226 schizophrenic patients and 129 controls from the Signature Bank of the Centre de recherche de l’Institut Universitaire en Santé Mentale de Montréal were analysed. Hypothesis was tested using logistic regressions. Sex and age were included as covariates.

Results: Interaction effects revealed that the relation between TG seropositivity and the risk of developing schizophrenia was modulated by levels of hair cortisol (chronic stress; OR = 3.97, CI₉₅ = 1.01- 15.71, p=.049). However, salivary cortisol (acute stress; OR = 1.72, CI₉₅ = 0.60-4.95, p=.315) and childhood adversity (OR = 1.01, CI₉₅ = 0.85-1.19, p=.931) did not increase the risk of schizophrenia in TG infected patients.

Conclusion: These results provide a step towards a better understanding of the role of stress in the association between TG and schizophrenia.

Authors: Antoine M. Dujon, Justine Boutry, Sophie Tissot, Jordan Meliani, Anna Miltiadous, Jácint Tokolyi, Beata Ujvari, Frédéric Thomas

Source: Science of The Total Environment (Aug 2024)

Abstract

Tumoural processes, ubiquitous phenomena in multicellular organisms, influence evolutionary trajectories of all species. To gain a holistic understanding of their impact on species’ biology, suitable laboratory models are required. Such models are characterised by a widespread availability, ease of cultivation, and reproducible tumour induction. It is especially important to explore, through experimental approaches, how tumoural processes alter ecosystem functioning.

The cnidarian Hydra oligactis is currently emerging as a promising model due to its development of both transmissible and non-transmissible tumours and the wide breadth of experiments that can be conducted with this species (at the individual, population, mechanistic, and evolutionary levels). However, tumoural hydras are, so far, only documented in Europe, and it is not clear if the phenomenon is local or widespread.

In this study we demonstrate that Australian hydras from two independent river networks develop tumours in the laboratory consisting of interstitial stem cells and display phenotypic alterations (supernumerary tentacles) akin to European counterparts. This finding confirms the value of this model for ecological and evolutionary research on host-tumour interactions.

Authors: Mathieu Giraudeau, Orsolya Vincze, Sophie M. Dupont, Tuul Sepp, Ciara Baines, Jean-Francois Lemaitre, Karin Lemberger, Sophie Gentès, Amy Boddy, Antoine M. Dujon, Georgina Bramwell, Valerie Harris, Beata Ujvari, Catherine Alix-Panabières, Stephane Lair, David Sayag, Dalia A. Conde, Fernando Colchero, Tara M. Harrison, Samuel Pavard, Benjamin Padilla-Morales, Damien Chevallier, Rodrigo Hamede, Benjamin Roche, Tamas Malkocs, Athena C. Aktipis, Carlo Maley, James DeGregori, Guillaume Le Loc’h, Frédéric Thomas

Source: Journal of Animal Ecology (Aug 2024)

Abstract

The last few years have seen a surge of interest from field ecologists and evolutionary biologists to study neoplasia and cancer in wildlife. This contributes to the One Health Approach, which investigates health issues at the intersection of people, wild and domestic animals, together with their changing environments. Nonetheless, the emerging field of wildlife cancer is currently constrained by methodological limitations in detecting cancer using non-invasive sampling. In addition, the suspected differential susceptibility and resistance of species to cancer often make the choice of a unique model species difficult for field biologists.

Here, we provide an overview of the importance of pursuing the study of cancer in non-model organisms and we review the currently available methods to detect, measure and quantify cancer in the wild, as well as the methodological limitations to be overcome to develop novel approaches inspired by diagnostic techniques used in human medicine.

The methodology we propose here will help understand and hopefully fight this major disease by generating general knowledge about cancer, variation in its rates, tumour-suppressor mechanisms across species as well as its link to life history and physiological characters. Moreover, this is expected to provide key information about cancer in wildlife, which is a top priority due to the accelerated anthropogenic change in the past decades that might favour cancer progression in wild populations.

Authors: Antoine M Dujon, Beata Ujvari, Sophie Tissot, Jordan Meliani, Océane Rieu, Nikita Stepanskyy, Rodrigo Hamede, Jácint Tokolyi, Aurora Nedelcu, Frédéric Thomas

Source: Evolutionary Applications (Aug 2024)

Abstract

Growing evidence indicates that human activities are causing cancer rates to rise in both human and wildlife populations. This is due to the inability of ancestral anti-cancer defences to cope with modern environmental risks. The evolutionary mismatch between modern oncogenic risks and evolved cancer defences has far-reaching effects on various biological aspects at different timeframes, demanding a comprehensive study of the biology and evolutionary ecology of the affected species.

Firstly, the increased activation of anti-cancer defences leads to excessive energy expenditure, affecting other biological functions and potentially causing health issues like autoimmune diseases. Secondly, tumorigenesis itself can impact important fitness-related parameters such as competitiveness, predator evasion, resistance to parasites, and dispersal capacity. Thirdly, rising cancer risks can influence the species’ life-history traits, often favoring early reproduction to offset fitness costs associated with cancer.

However, this strategy has its limits, and it may not ensure the sustainability of the species if cancer risks continue to rise. Lastly, some species may evolve additional anti-cancer defences, with uncertain consequences for their biology and future evolutionary path.

In summary, we argue that the effects of increased exposure to cancer-causing substances on wildlife are complex, ranging from immediate responses to long-term evolutionary changes. Understanding these processes, especially in the context of conservation biology, is urgently needed.