Laboratoire de régénération et neurogénèse adulte

Mots-clés: hydre, cnidaire, régénération, remodelage cellulaire, plasticité du développement, homéostase, blessure, réparation tissulaire, contrôle de la croissance tissulaire, mise en place du schéma corporel, prolifération compensatrice induite par l’apoptose, voies de signalisation, évolution, neurogénèse

1. Résumé

Une question fascinante en biologie est celle posée par la variation du potentiel de régénération à l’intérieur du royaume animal: en effet si de nombreuses espèces sont douées de régénération, la plupart des mammifères ont vraisemblablement perdu ce potentiel. Dans notre laboratoire nous utilisons l’Hydre d’eau douce qui fournit un modèle puissant pour comprendre l’équilibre entre le maintien d’un état homéostatique très dynamique et l’activation de programmes de régénération. Les questions sur lesquelles nous nous penchons sont les suivantes:

  • HOMEOSTASIE et REGENERATION: Quels sont les mécanismes cellulaires et moléculaires qui maintiennent l’homéostasie et quell est leur rôle dans la régénération?
  • CELLULES SOUCHES et CELLULES DIFFERENCIEES: Quelles sont les contributions respectives des cellules souches et des cellules différenciées dans ces processus?
  • MEMOIRE: Quels sont les mécanismes de mémoire qui permettent d’activer le bon programme au bon endroit, c’est à dire la régénération du pied d’un côté, la régénération de la tête de l’autre?
  • NEUROGENESE ADULTE: Quelle est la circuitrie génétique qui conduit à la neurogénèse de novo puisque l’animal reconstitue complètement son système nerveux apical lors de la régénération de la tête?
  • VIEILLISSEMENT: Quels sont les mécanismes de non-vieillissement qui permettent de maintenir accessibles les programmes de développement, régénération et bourgeonnement, quelque soit l’âge de l’animal?
  • EVOLUTION: Lesquels de ces mécanismes ont été conservés au cours de l’évolution?

Afin d’élucider ces questions, nous cherchons à identifier par interférence à l’ARN (ARNi) les cascades de signalisation qui gouvernent la plasticité cellulaire et développementale de l’Hydre. Nous avons récemment montré que la prolifération compensatrice induite par l’apoptose joue un rôle important pour régénérer une tête après bisection au milieu de la colonne corporelle. De façon intéressante, la prolifération compensatrice induite par l’apoptose joue également un rôle important chez le tétard de Xénope qui régénère sa queue, chez la larve de Drosophile qui régénère ses disques imaginaux ou même chez les rongeurs qui régénèrent leur peau ou leur foie. Ces avancées suggèrent qu’il existe des voies communes chez les animaux pour activer un processus de régénération (voir revues récentes [1, 2]).

Figure 1: Schéma montrant la position de l’Hydre dans l’arbre des métazoaires. Parmi les cnidaires, les anthozoaires (coraux, anémonde de mer) sont exclusivement des polypes tandis que les médusozoaires alternant les phases polype et méduse au cours de leur cycle de vie. L’Hydre est un médusozoaire qui a perdu le stade méduse et vit donc exclusivement sous la forme polype.

2. Le modèle de l’Hydre en quelques mots

L’Hydre appartient au phylum des cnidaires, un groupe frère des bilatériens (Fig.1). L’anatomie de l’Hydre est simple: c’est en fait un tube qui est différencié aux deux extrémités. Au pôle apical l’animal différencie la région de la tête, formée d’un orifice bouche/anus entouré d’un cercle de tentacules qui servent à attraper la nourriture (l’Hydre est carnivore); au pôle basal, l’animal différencie un disque basal qui lui permet de se fixer. Les tissus sont formés de deux couches cellulaires, l’ectoderme et l’endoderme, séparées par une matrice extracellulaire la mésoglée. L’Hydre differencie tous les types cellulaires nécessaires à la digestion, la sécrétion, la transmission neuro-musculaire, la reproduction sexuée. Ces différents types cellulaires dérivent de trois populations dictinctes de cellules souches: les cellules épithéliales de l’ectoderme, les cellules épithéliales de l’endoderme et les cellules interstitielles qui sont multipotentes [3, 4]. En effet les cellules interstitielles peuvent tout au long de la vie de l’animal se différencier en cellules somatiques (neurones, cellules mécano-sensorielles - cellules urticantes nommées nématocytes ou cnidocytes -, cellules glandulaires) mais aussi en cellules germinales (ovocytes, spermatozoides).

Au cours des 25 dernières années, il a été montré que les gènes codant pour des protéines impliquées dans les voies de signalisation contrôlant les différents comportements cellulaires ou les processus de développement, avaient été extrêmement conservés au cours de l’évolution des métazoaires. Le séquençage du génome de deux espèces de cnidaires (Nematostella vectensis – anémone de mer - et tout récemment Hydra magnipapillata) a confirmé ce haut niveau de conservation génique entre les cnidaires et les vertébrés, renforçant encore la valeur du modèle de l’Hydre [5, 6].

3. Analyse fonctionnelle de la circuitrie génétique soutenant la régénération de l’Hydre

Grâce à l’ARN interférence (ARNi) par nourrissage nous avons pu mettre en évidence des phénotypes partagés par l’homme et l’Hydre

Chez certains vers, il est possible d’éteindre l’expression d’un gène donné en nourrissant les animaux avec des bactéries qui ont au préalable exprimé des ARN double-brins correspondant à ce gène [7-9]. Nous avons adapté cette stratégie à l’Hydre (Fig. 2) et ainsi pu démontrer qu’il s’agit d’une méthode non toxique pour l’Hydre, qui induit progressivement et efficacement des phénotypes spécifiques de chaque gène [10-13].

Dans le cas du gène Kazal1 qui produit un inhibiteur de protéases, l’ARNi induit une autophagie massive des cellules glandulaires qui produisent Kazal1 et des cellules digestives voisines qui normalement utilisent Kazal1. En effet en l’absence de Kazal1, les protéases ne sont pas bloquées et digèrent le contenu des cellules qui les produisent. Les souris mutées pour le gène de type Kazal SPINK3 développent également une autophagie massive au sein de leur pancréas et du tube digestif immédiatement après la naissance. Chez l’homme certaines pancréatites chroniques sont également dues à une autophagie excessive liée à des mutations du gène SPINK1. C’est la preuve de la conservation de la fonction des gènes de type Kazal de l’Hydre à l’homme, soutenant la valeur paradigmatique du système modèle de l’Hydre.

Cette stratégie de l’ARN interférence par nourrissage nous ouvre maintenant la possibilité de cribler un grand nombre de gènes pour identifier leur fonction au cours de la régénération.

Gene silencing by RNA interference in Hydra

Figure 2: Eteignage de l’expression des gènes par ARN interférence par nourrissage chez l’Hydre. Cette stratégie, initialement développée chez le nématode [7, 8] a été adaptée pour les planaires [9] et par notre laboratoire pour les polypes d’Hydre [10-12]. Les ARNs double-brins d’un gène cible sont tout d’abord produits par la bactérie HT115, puis les polypes d’Hydre sont nourris tous les deux jours avec un mélange agarose-bactéries. La glutathione sert à induire l’ouverture de la bouche des polypes. Le nombre de nourrissages requis pour obtenir un phénotype varie suivant le type cellulaire où s’exprime le gène cible, le niveau d’expression de ce gène et la stabilité de la protéine correspondante.

L’Hydre utilise la mort cellulaire et l’activation de la voie Wnt3-bcatenin pour régénérer sa tête

L’activation de la cascade de signalisation Wnt3-bcatenin, qui est parfaitement conservée chez l’Hydre, est nécessaire à la régénération de la tête [14, 15]. Nous avons récemment montré que la bisection induit une vague d’apoptose dans les bourgeons destinés à régénérer une tête mais pas dans ceux destinés à régénérer un pied [13]. Ces cellules en apoptose jouent en fait un rôle moteur dans le processus de régénération car très transitoirement elles délivrent le signal Wnt3 aux cellules adjacentes qui se divisent alors rapidement. En effet si l’apoptose est bloquée ou si la production du signal Wnt3 est inhibée, la prolifération cellulaire et la régénération de la tête sont abolies mais l’addition de signal Wnt3 dans le milieu suffit à sauver le processus de régénération. Une autre expérience a mis en évidence cette fonction de la mort cellulaire dans le processus de régénération de la tête: il suffit d’induire l’apoptose dans les bourgeons destines à régénérer un pied pour activer la voie Wnt3-bcatenin et obtenir des hydres qui régénèrent une tête à la place du pied (Figure 3).

Bi-headed Hydra resulting from the ectopic apoptosis-induced activation of the Wnt3-bcatenin pathway

Figure 3: Hydre à deux têtes résultant de l’induction ectopique de l’apoptose au niveau du bourgeon de régénération du pied. Normalement des Hydres coupées en deux moitiés régénèrent un pied à partir de la moitié apicale et une tête à partir de la moitié basale. Ici des moités apicales ont été brièvement chauffées au niveau de la plaie pour induire un niveau élevé d’apoptose. Cette apoptose ectopique induit alors l’activation de la voie de signalisation Wnt3-bcatenin, ce qui suffit à convertir la régénération du pied en régénération de la tête (voir discussion dans [1, 2]).

La régulation asymmétrique de la cascade MAPK ➜ RSK ➜ CREB ➜ CBP après bisection

La cascade MAPK/CREB semble jouer un rôle précoce dans l’induction de la régénération de la tête. En effet la protéine CREB (cAMP Response Element Binding protein) est un facteur de transcription qui interagit avec des partenaires différents lorsqu’il lie le motif CRE après bisection [16]. De plus CREB est soumis à une série de régulations différentes dans le bourgeon destiné à régénérer une tête et dans celui destine à régénérer un pied: du côté régénérant la tête CREB est immédiatement phosphorylé par la kinase RSK [17] et son expression est rapidement augmentée [18]. Chez les vertébrés, la forme phosphorylée de CREB lie le régulateur chromatinien CBP pour moduler l’expression de gènes cibles. La protéine CBP d’Hydre contient également un domaine liant CREB et lorsque l’expression des gènes RSK, CREB ou CBP est éteinte, ni la vague immédiate d’apoptose, ni le remodelage cellulaire normalement observé dans les bourgeons régénérant une tête n’ont lieu (Chera and Galliot, submitted). Nous cherchons actuellement à comprendre comment cette voie de signalisation permet de “lire” le stress de l’amputation pour activer un programme de régénération spécifique et complexe, celui de la formation de novo de la tête de l’Hydre.

4. L’émergence de la neurogénèse et de la différenciation apicale chez les métazoaires

Chez l’Hydre adulte la neurogénèse est constamment maintenue et le système nerveux apical très dense se forme au cours du bourgeonnement ou bien est complètement régénéré après décapitation [19-21]. Chez les animaux à symétrie bilatérale dont l’ancêtre commun avait déjà un système nerveux centralisé et des organes sensoriels, les gènes à homéoboite des classes ANTP et PAIRED jouent un rôle majeur au cours du développement du système nerveux [22-24]. Chaque classe comprend un grand nombre de familles qui, pour la plupart, se sont diversifiées très tôt au cours de l’évolution animale, précédant l’origine des cnidaires [25-27]. Ceci pose la question de la fonction de ces familles de gènes chez les cnidaires (qui différencient un système nerveux sophistiqué) et chez les porifères (qui n’ont pas de système nerveux) [21].

Les gènes à homéoboite de la classe PAIRED

Parmi les familles de gènes de la classe Paired impliquées dans la spécification du cerveau et des organes sensoriels chez les bilatériens, plusieurs sont exprimées dans le système nerveux des cnidaires [28-32]. Parmi ceux-ci, le gène prd-la est exprimé dans les précurseurs neuronaux et les neurones apicaux de l’Hydre adulte; cependant après bisection, ce gène est précocément et transitoirement exprimé dans la couche endodermale du bourgeon régénérant la tête. Cette double régulation suggère que ce gène est impliqué non seulement dans la neurogénèse mais également dans l’activité organisatrice de la tête en permettant des interactions inductives depuis l’endoderme vers l’ectoderme sus-jacent [19, 28]. Ce résultat est étonnant car chez les vertébrés, certains gènes paired-like ont une fonction similaire lorsque l’activité organisatrice de la tête se met en place au cours du développement précoce, suggérant des mécanismes moléculaires conservés [33].

Les gènes à homéoboite de la classe Hox/ParaHox

Si les cnidaires expriment un grand nombre de familles de gènes de la classe ANTP, toutes les familles Hox utilisées par les bilatéraux ne sont pas présentes et les gènes de type Hox n’ont pas été identifiés chez les porifères, suggérant que ces gènes “Hox-like” de cnidaires représentent en fait les gènes proto-Hox [26, 34-36]. Parmi ceux-ci, le gène cnox-2 (orthologue du gène ParaHox Gsx) est particulièrement intéressant car il est spécifiquement exprimé au cours de la neurogénèse apicale, chez le polype intact mais aussi au cours du bourgeonnement ou de la régénération de la tête [11, 26, 37]. Lorsque l’expression de cnox- 2 est éteinte par ARNi, le système nerveux apical n’est plus renouvellé et ne se forme plus correctement. Chez les vertébrés et chez la mouche Gsx est également impliqué dans la neurogénèse [38]. Ces données suggèrent une fonction neurogénique des gènes cnox- 2/Gsx très conservée au cours de l’évolution ainsi qu’un lien fonctionnel établi très tôt au cours de l’évolution animale entre neurogénèse et différenciation apicale/antérieure [11, 20, 36].

Références

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Equipe

Brigitte Galliot
Professeur(e) honoraire Leader

Pr Brigitte Galliot

+41 22 379 67 74
brigitte.galliot@unige.ch
Bureau 4002B (Sciences III)
Wanda Christa Buzgariu
Adjoint(e) scientifique

Dr Wanda Christa Buzgariu

+41 22 379 67 66
wanda.buzgariu@unige.ch
Bureau 4009 (Sciences III)

Publications

Page
Organizer formation, organizer maintenance and epithelial cell plasticity in Hydra: Role of the Wnt3/β-catenin/TCF/Sp5/Zic4 gene network.
2025
Cells & development
Auteurs: Galliot, Wenger
Voir la publication
The experimental and conceptual knowledge in 1909 led to the discovery of the Hydra head organizer through transplantation experiments between pigmented and non-pigmented animals; a discovery followed by numerous transplantations demonstrating cross-regulation between activating and inhibiting components distributed along the body axis. This experimental work inspired mathematicians, engineers, physicists and computer scientists to develop theoretical models predicting the principles of developmental mechanisms. Today, we know that the Wnt/β-catenin/Sp5/Zic4 gene regulatory network (GRN) links organizer activity, morphogenesis and cellular identity in Hydra, with variable conformations depending on the region or epithelial layer, and varied phenotypes depending on which GRN element is misregulated. In intact animals, Wnt/β-catenin signaling acts as the head activator at the tip of the hypostome, restricted by Sp5 in the other regions of the animal. Moreover, in the tentacle ring, Sp5 and Zic4 act epistatically to support tentacle differentiation and prevent basal disc differentiation. Along the body column, Sp5 is self-repressed in the epidermis and acts as a head inhibitor along the gastrodermis. Other players modulate these activities, such as TSP and Margin/RAX apically, Notch signaling in the tentacle zone, Dkk1/2/4 and HAS-7 in the body column. In the developmental context of regeneration, cells below the amputation zone switch from repressed to locally de novo activated head organizer status, a transition driven by immediate symmetrical and asymmetrical metabolic changes that lead to gene expression regulations involving components and modulators of Wnt/β-catenin signaling, early-pulse and early-late transient both often symmetrical, together with sustained ones, specific to head regeneration.
The Gene Network That Regulates Head Organizer Activity in Is Differentially Regulated in Epidermis and Gastrodermis.
2024
Biomedicines
Auteurs: Iglesias Ollé L, Perruchoud C, Sanchez PGL, Vogg MC, Galliot B
Voir la publication
head formation depends on an organizing center in which Wnt/β-catenin signaling, that plays an inductive role, positively regulates and , with Sp5 limiting expression and Zic4 triggering tentacle formation. Using transgenic lines in which the promoter drives eGFP expression in either the epidermis or gastrodermis, we show that promoter activity is differentially regulated in each epithelial layer. In intact animals, epidermal GFP activity is strong apically and weak along the body column, while in the gastrodermis, it is maximal in the tentacle ring region and maintained at a high level along the upper body column. During apical regeneration, :GFP is activated early in the gastrodermis and later in the epidermis. Alsterpaullone treatment induces a shift in apical expression towards the body column where it forms transient circular figures in the epidermis. Upon (RNAi), GFP activity is down-regulated in the epidermis while bud-like structures expressing GFP in the gastrodermis develop. (RNAi) reveals a negative autoregulation in the epidermis, but not in the gastrodermis. These differential regulations in the epidermis and gastrodermis highlight the distinct architectures of the network in the hypostome, tentacle base and body column of intact animals, as well as in the buds and apical and basal regenerating tips.
The transcription factor Zic4 promotes tentacle formation and prevents epithelial transdifferentiation in Hydra
2022
Science advances
Auteurs: Vogg MC, Ferenc J, Buzgariu WC, Perruchoud C, Sanchez PGL, Beccari L, Nuninger C, Le Cras Y, Delucinge-Vivier C, Papasaikas P, Vincent S, Galliot B, Tsiairis CD
Voir la publication
The molecular mechanisms that maintain cellular identities and prevent dedifferentiation or transdifferentiation remain mysterious. However, both processes are transiently used during animal regeneration. Therefore, organisms that regenerate their organs, appendages, or even their whole body offer a fruitful paradigm to investigate the regulation of cell fate stability. Here, we used as a model system and show that Zic4, whose expression is controlled by Wnt3/β-catenin signaling and the Sp5 transcription factor, plays a key role in tentacle formation and tentacle maintenance. Reducing expression suffices to induce transdifferentiation of tentacle epithelial cells into foot epithelial cells. This switch requires the reentry of tentacle battery cells into the cell cycle without cell division and is accompanied by degeneration of nematocytes embedded in these cells. These results indicate that maintenance of cell fate by a Wnt-controlled mechanism is a key process both during homeostasis and during regeneration.
Combining RNAi-Mediated β-Catenin Inhibition and Reaggregation to Study Hydra Whole-Body Regeneration.
2022
Methods in molecular biology (Clifton, N.J.)
Auteurs: Vogg MC, Galliot B
Voir la publication
In addition to its ability to regenerate any amputated body part, the Hydra freshwater polyp shows the amazing ability to regenerate as a full polyp after a complete dissociation of its tissues. The developmental processes at work in reaggregates undergoing whole-body regeneration can be investigated at the molecular level by RNA interference (RNAi). Here we provide a protocol that combines β-catenin RNAi with reaggregation. This protocol serves as a basis to generate "RNAi-reaggregates," followed by the extraction of high-quality RNA for the precise quantification of gene expression by real-time PCR. This protocol is efficient, providing both a molecular signature, with the significant downregulation of β-catenin and Wnt3, as well as a robust phenotype, the lack of axis formation, which is observed in all reaggregates.
Studying Stem Cell Biology in Intact and Whole-Body Regenerating Hydra by Flow Cytometry.
2022
Methods in molecular biology (Clifton, N.J.)
Auteurs: Buzgariu W, Aubry-Lachainaye JP, Galliot B
Voir la publication
The freshwater Hydra polyp is a versatile model to study whole-body regeneration from a developmental as well as a cellular point of view. The outstanding regenerative capacities of Hydra are based on its three populations of adult stem cells located in the central body column of the animal. There, these three populations, gastrodermal epithelial, epidermal epithelial, and interstitial, continuously cycle in homeostatic conditions, and their activity is locally regulated after mid-gastric bisection. Moreover, they present an unusual cycling behavior with a short G1 phase and a pausing in G2. This particular cell cycle has been studied for a long time with classical microscopic methods. We describe here two flow cytometry methods that provide accurate and reproducible quantitative data to monitor cell cycle regulation in homeostatic and regenerative contexts. We also present a cell sorting procedure based on flow cytometry, whereby stem cells expressing a fluorescent reporter protein in transgenic lines can be enriched for use in applications such as transcriptomic, proteomic, or cell cycle analysis.
Cellular, Metabolic, and Developmental Dimensions of Whole-Body Regeneration in .
2021
Cold Spring Harbor perspectives in biology
Auteurs: Vogg MC, Buzgariu W, Suknovic NS, Galliot B
Voir la publication
Here we discuss the developmental and homeostatic conditions necessary for regeneration. is characterized by populations of adult stem cells paused in the G2 phase of the cell cycle, ready to respond to injury signals. The body column can be compared to a blastema-like structure, populated with multifunctional epithelial stem cells that show low sensitivity to proapoptotic signals, and high inducibility of autophagy that promotes resistance to stress and starvation. Intact polyps also exhibit a dynamic patterning along the oral-aboral axis under the control of homeostatic organizers whose activity results from regulatory loops between activators and inhibitors. As in bilaterians, injury triggers the immediate production of reactive oxygen species (ROS) signals that promote wound healing and contribute to the reactivation of developmental programs via cell death and the de novo formation of new organizing centers from somatic tissues. In aging , regeneration is rapidly lost as homeostatic conditions are no longer pro-regenerative.
The ULK1 kinase, a necessary component of the pro-regenerative and anti-aging machinery in Hydra.
2020
Mechanisms of ageing and development
Auteurs: Suknovic N, Tomczyk S, Colevret D, Perruchoud C, Galliot B
Voir la publication
Hydra vulgaris (Hv) has a high regenerative potential and negligible senescence, as its stem cell populations divide continuously. In contrast, the cold-sensitive H. oligactis (Ho_CS) rapidly develop an aging phenotype under stress, with epithelial stem cells deficient for autophagy, unable to maintain their self-renewal. Here we tested in aging, non-aging and regenerating Hydra the activity and regulation of the ULK1 kinase involved in autophagosome formation. In vitro kinase assays show that human ULK1 activity is activated by Hv extracts but repressed by Ho_CS extracts, reflecting the ability or inability of their respective epithelial cells to initiate autophagosome formation. The factors that keep ULK1 inactive in Ho_CS remain uncharacterized. Hv_Basel1 animals exposed to the ULK1 inhibitor SBI-0206965 no longer regenerate their head, indicating that the sustained autophagy flux recorded in regenerating Hv_AEP2 transgenic animals expressing the DsRed-GFP-LC3A autophagy tandem sensor is necessary. The SBI-0206965 treatment also alters the contractility of intact Hv_Basel1 animals, and leads to a progressive reduction of animal size in Hv_AEP2, similarly to what is observed in ULK1(RNAi) animals. We conclude that the evolutionarily-conserved role of ULK1 in autophagy initiation is crucial to maintain a dynamic homeostasis in Hydra, which supports regeneration efficiency and prevents aging.
The polymorphism of Hydra microsatellite sequences provides strain-specific signatures.
2020
PloS one
Auteurs: Schenkelaars Q, Perez-Cortes D, Perruchoud C, Galliot B
Voir la publication
Hydra are freshwater polyps widely studied for their amazing regenerative capacity, adult stem cell populations, low senescence and value as ecotoxicological marker. Many wild-type strains of H. vulgaris have been collected worldwide and maintained effectively under laboratory conditions by asexual reproduction, while stable transgenic lines have been continuously produced since 2006. Efforts are now needed to ensure the genetic characterization of all these strains, which despite similar morphologies, show significant variability in their response to gene expression silencing procedures, pharmacological treatments or environmental conditions. Here, we established a rapid and reliable procedure at the single polyp level to produce via PCR amplification of three distinct microsatellite sequences molecular signatures that distinguish between Hydra strains and species. The TG-rich region of an uncharacterized gene (ms-c25145) helps to distinguish between Eurasian H. vulgaris-Pallas strains (Hm-105, Basel1, Basel2 and reg-16), between Eurasian and North American H. vulgaris strains (H. carnea, AEP), and between the H. vulgaris and H. oligactis species. The AT-rich microsatellite sequences located in the AIP gene (Aryl Hydrocarbon Receptor Interaction Protein, ms-AIP) also differ between Eurasian and North American H. vulgaris strains. Finally, the AT-rich microsatellite located in the Myb-Like cyclin D-binding transcription factor1 gene (ms-DMTF1) gene helps to distinguish certain transgenic AEP lines. This study shows that the analysis of microsatellite sequences, which is capable of tracing genomic variations between closely related lineages of Hydra, provides a sensitive and robust tool for characterizing the Hydra strains.
Deficient autophagy in epithelial stem cells drives aging in the freshwater cnidarian .
2019
Development (Cambridge, England)
Auteurs: Tomczyk S, Suknovic N, Schenkelaars Q, Wenger Y, Ekundayo K, Buzgariu W, Bauer C, Fischer K, Austad S, Galliot B
Voir la publication
possesses three distinct stem cell populations that continuously self-renew and prevent aging in However sexual animals from the cold-sensitive ( strain develop an aging phenotype upon gametogenesis induction, initiated by the loss of interstitial stem cells. Animals stop regenerating, lose their active behaviors and die within three months. This phenotype is not observed in the cold-resistant strain. To dissect the mechanisms of aging we compared the self-renewal of epithelial stem cells in these two strains and found it irreversibly reduced in aging while sustained in non-aging We also identified a deficient autophagy in epithelial cells, with a constitutive deficiency in autophagosome formation as detected with the mCherry-eGFP-LC3A/B autophagy sensor, an inefficient response to starvation as evidenced by the accumulation of the autophagosome cargo protein p62/SQSTM1, and a poorly-inducible autophagy flux upon proteasome inhibition. In the non-aging animals, the blockade of autophagy by knocking-down suffices to induce aging. This study highlights the essential role of a dynamic autophagy flux to maintain epithelial stem cell renewal and prevent aging.
Model systems for regeneration: Hydra.
2019
Development (Cambridge, England)
Auteurs: Vogg MC, Galliot B, Tsiairis CD
Voir la publication
The freshwater polyp provides a potent model system for investigating the conditions that promote wound healing, reactivation of a developmental process and, ultimately, regeneration of an amputated body part. polyps can also be dissociated to the single cell level and can regenerate a complete body axis from aggregates, behaving as natural organoids. In recent years, the ability to exploit has been expanded with the advent of new live-imaging approaches, genetic manipulations that include stable transgenesis, gene silencing and genome editing, and the accumulation of high-throughput omics data. In this Primer, we provide an overview of as a model system for studying regeneration, highlighting recent results that question the classical self-enhancement and long-range inhibition model supposed to drive regeneration. We underscore the need for integrative explanations incorporating biochemical as well as mechanical signalling.
Combining BrdU-Labeling to Detection of Neuronal Markers to Monitor Adult Neurogenesis in Hydra.
2019
Methods in molecular biology (Clifton, N.J.)
Auteurs: Buzgariu W, Curchod ML, Perruchoud C, Galliot B
Voir la publication
The nervous system is produced and maintained in adult Hydra through the continuous production of nerve cells and mechanosensory cells (nematocytes or cnidocytes). De novo neurogenesis occurs slowly in intact animals that replace their dying nerve cells, at a faster rate in animals regenerating their head as a complete apical nervous system is built in few days. To dissect the molecular mechanisms that underlie these properties, a precise monitoring of the markers of neurogenesis and nematogenesis is required. Here we describe the conditions for an efficient BrdU-labeling coupled to an immunodetection of neuronal markers, either regulators of neurogenesis, here the homeoprotein prdl-a, or neuropeptides such as RFamide or Hym-355. This method can be performed on whole-mount animals as well as on macerated tissues when cells retain their morphology. Moreover, when antibodies are not available, BrdU-labeling can be combined with the analysis of gene expression by whole-mount in situ hybridization. This co-immunodetection procedure is well adapted to visualize and quantify the dynamics of de novo neurogenesis. Upon continuous BrdU labeling, the repeated measurements of BrdU-labeling indexes in specific cellular populations provide a precise monitoring of nematogenesis as well as neurogenesis, in homeostatic or developmental conditions.
Loss of Neurogenesis in Aging Hydra.
2019
Developmental neurobiology
Auteurs: Tomczyk S, Buzgariu W, Perruchoud C, Fisher K, Austad S, Galliot B
Voir la publication
In Hydra the nervous system is composed of neurons and mechanosensory cells that differentiate from interstitial stem cells (ISCs), which also provide gland cells and germ cells. The adult nervous system is actively maintained through continuous de novo neurogenesis that occurs at two distinct paces, slow in intact animals and fast in regenerating ones. Surprisingly Hydra vulgaris survive the elimination of cycling interstitial cells and the subsequent loss of neurogenesis if force-fed. By contrast, H. oligactis animals exposed to cold temperature undergo gametogenesis and a concomitant progressive loss of neurogenesis. In the cold-sensitive strain Ho_CS, this loss irreversibly leads to aging and animal death. Within four weeks, Ho_CS animals lose their contractility, feeding response, and reaction to light. Meanwhile, two positive regulators of neurogenesis, the homeoprotein prdl-a and the neuropeptide Hym-355, are no longer expressed, while the "old" RFamide-expressing neurons persist. A comparative transcriptomic analysis performed in cold-sensitive and cold-resistant strains confirms the downregulation of classical neuronal markers during aging but also shows the upregulation of putative regulators of neurotransmission and neurogenesis such as AHR, FGFR, FoxJ3, Fral2, Jagged, Meis1, Notch, Otx1, and TCF15. The switch of Fral2 expression from neurons to germ cells suggests that in aging animals, the neurogenic program active in ISCs is re-routed to germ cells, preventing de novo neurogenesis and impacting animal survival.
An evolutionarily-conserved Wnt3/β-catenin/Sp5 feedback loop restricts head organizer activity in Hydra.
2019
Nature communications
Auteurs: Vogg MC, Beccari L, Iglesias Ollé L, Rampon C, Vriz S, Perruchoud C, Wenger Y, Galliot B
Voir la publication
Polyps of the cnidarian Hydra maintain their adult anatomy through two developmental organizers, the head organizer located apically and the foot organizer basally. The head organizer is made of two antagonistic cross-reacting components, an activator, driving apical differentiation and an inhibitor, preventing ectopic head formation. Here we characterize the head inhibitor by comparing planarian genes down-regulated when β-catenin is silenced to Hydra genes displaying a graded apical-to-basal expression and an up-regulation during head regeneration. We identify Sp5 as a transcription factor that fulfills the head inhibitor properties: leading to a robust multiheaded phenotype when knocked-down in Hydra, acting as a transcriptional repressor of Wnt3 and positively regulated by Wnt/β-catenin signaling. Hydra and zebrafish Sp5 repress Wnt3 promoter activity while Hydra Sp5 also activates its own expression, likely via β-catenin/TCF interaction. This work identifies Sp5 as a potent feedback loop inhibitor of Wnt/β-catenin signaling, a function conserved across eumetazoan evolution.
Modern genomic tools reveal the structural and cellular diversity of cnidarian nervous systems.
2019
Current opinion in neurobiology
Auteurs: Rentzsch F, Juliano C, Galliot B
Voir la publication
Cnidarians shared a common ancestor with bilaterians more than 600 million years ago. This sister group relationship gives them an informative phylogenetic position for understanding the fascinating morphological and molecular cell type diversity of bilaterian nervous systems. Moreover, cnidarians display novel features such as endodermal neurogenesis and independently evolved centralizations, which provide a platform for understanding the evolution of nervous system innovations. In recent years, the application of modern genomic tools has significantly advanced our understanding of cnidarian nervous system structure and function. For example, transgenic reporter lines and gene knockdown experiments in several cnidarian species reveal a significant degree of conservation in the neurogenesis gene regulatory program, while single cell RNA sequencing projects are providing a much deeper understanding of cnidarian neural cell type diversity. At the level of neural function, the physiological properties of ion channels have been described and calcium imaging of the nervous system in whole animals has allowed for the identification of neural circuits underlying specific behaviours. Cnidarians have arrived in the modern era of molecular neurobiology and are primed to provide exciting new insights into the early evolution of nervous systems.
Non-developmental dimensions of adult regeneration in Hydra.
2018
The International journal of developmental biology
Auteurs: Galliot B, Buzgariu W, Schenkelaars Q, Wenger Y
Voir la publication
An essential dimension of 3D regeneration in adult animals is developmental, with the formation of organizers from somatic tissues. These organizers produce signals that recruit surrounding cells and drive the restoration of the missing structures (organs, appendages, body parts). However, even in animals with a high regenerative potential, this developmental potential is not sufficient to achieve regeneration as homeostatic conditions at the time of injury need to be "pro-regenerative". In Hydra, we identified four distinct homeostatic properties that provide a pro-regenerative framework and we discuss here how these non-developmental properties impact regeneration. First, both the epithelial and the interstitial-derived cells are highly plastic along the animal body, a plasticity that offers several routes to achieve regeneration. Second, the abundant stocks of continuously self-renewing adult stem cells form a constitutive pro-blastema in the central body column, readily activated upon bisection. Third, the autophagy machinery in epithelial cells guarantees a high level of fitness and adaptation to detrimental environmental conditions, as evidenced by the loss of regeneration in animals where autophagy is dysfunctional. Fourth, the extracellular matrix, named mesoglea in Hydra, provides a dynamically-patterned environment where the molecular and mechanical signals induced by injury get translated into a regenerative process. We claim that these homeostatic pro-regenerative features contribute to define the high regenerative potential of adult Hydra.
Hydra, a model system for deciphering the mechanisms of aging and resistance to aging.
2018
Conn’s Handbook for models on human aging (Second Edition)
Auteurs: Schenkelaars Q., Tomczyk S., Wenger Y., Ekundayo K., Girard V., Buzgariu W., Austad S. and Galliot B.
Voir la publication
Conn's Handbook of Models for Human Aging, Second Edition, presents key aspects of biology, nutrition, factors affecting lifespan, methods of age determination, use in research and the disadvantages/advantages of use. Using a multidisciplinary approach, this updated edition is designed as the only comprehensive, current work that covers the diversity in aging models. Chapters on comparative models explore age-related diseases, including Alzheimer's, joint disease, cataracts, cancer and obesity. Also included are new tricks and approaches not available in primary publications. This must-have handbook is an indispensable resource for researchers interested in the mechanisms of aging, gerontologists, health professionals, allied health practitioners and students.
Impact of cycling cells and cell cycle regulation on Hydra regeneration.
2018
Developmental biology
Auteurs: Buzgariu W, Wenger Y, Tcaciuc N, Catunda-Lemos AP, Galliot B
Voir la publication
Hydra tissues are made from three distinct populations of stem cells that continuously cycle and pause in G2 instead of G1. To characterize the role of cell proliferation after mid-gastric bisection, we have (i) used flow cytometry and classical markers to monitor cell cycle modulations, (ii) quantified the transcriptomic regulations of 202 genes associated with cell proliferation during head and foot regeneration, and (iii) compared the impact of anti-proliferative treatments on regeneration efficiency. We confirm two previously reported events: an early mitotic wave in head-regenerating tips, when few cell cycle genes are up-regulated, and an early-late wave of proliferation on the second day, preceded by the up-regulation of 17 cell cycle genes. These regulations appear more intense after mid-gastric bisection than after decapitation, suggesting a position-dependent regulation of cell proliferation during head regeneration. Hydroxyurea, which blocks S-phase progression, delays head regeneration when applied before but not after bisection. This result is consistent with the fact that the Hydra central region is enriched in G2-paused adult stem cells, poised to divide upon injury, thus forming a necessary constitutive pro-blastema. However a prolonged exposure to hydroxyurea does not block regeneration as cells can differentiate apical structures without traversing S-phase, and also escape in few days the hydroxyurea-induced S-phase blockade. Thus Hydra head regeneration, which is a fast event, is highly plastic, relying on large stocks of adult stem cells paused in G2 at amputation time, which immediately divide to proliferate and/or differentiate apical structures even when S-phase is blocked.
Trends in tissue repair and regeneration.
2017
Development (Cambridge, England)
Auteurs: Galliot B, Crescenzi M, Jacinto A, Tajbakhsh S
Voir la publication
The 6th EMBO conference on the Molecular and Cellular Basis of Regeneration and Tissue Repair took place in Paestum (Italy) on the 17th-21st September, 2016. The 160 scientists who attended discussed the importance of cellular and tissue plasticity, biophysical aspects of regeneration, the diverse roles of injury-induced immune responses, strategies to reactivate regeneration in mammals, links between regeneration and ageing, and the impact of non-mammalian models on regenerative medicine.
How Somatic Adult Tissues Develop Organizer Activity.
2016
Current topics in developmental biology
Auteurs: Vogg MC, Wenger Y, Galliot B
Voir la publication
The growth and patterning of anatomical structures from specific cellular fields in developing organisms relies on organizing centers that instruct surrounding cells to modify their behavior, namely migration, proliferation, and differentiation. We discuss here how organizers can form in adult organisms, a process of utmost interest for regenerative medicine. Animals like Hydra and planarians, which maintain their shape and fitness thanks to a highly dynamic homeostasis, offer a useful paradigm to study adult organizers in steady-state conditions. Beside the homeostatic context, these model systems also offer the possibility to study how organizers form de novo from somatic adult tissues. Both extracellular matrix remodeling and caspase activation play a key role in this transition, acting as promoters of organizer formation in the vicinity of the wound. Their respective roles and the crosstalk between them just start to be deciphered.
Multi-functionality and plasticity characterize epithelial cells in Hydra.
2015
Tissue barriers
Auteurs: Buzgariu W, Al Haddad S, Tomczyk S, Wenger Y, Galliot B
Voir la publication
Epithelial sheets, a synapomorphy of all metazoans but porifers, are present as 2 layers in cnidarians, ectoderm and endoderm, joined at their basal side by an extra-cellular matrix named mesoglea. In the Hydra polyp, epithelial cells of the body column are unipotent stem cells that continuously self-renew and concomitantly express their epitheliomuscular features. These multifunctional contractile cells maintain homeostasis by providing a protective physical barrier, by digesting nutrients, by selecting a stable microbiota, and by rapidly closing wounds. In addition, epithelial cells are highly plastic, supporting the adaptation of Hydra to physiological and environmental changes, such as long starvation periods where survival relies on a highly dynamic autophagy flux. Epithelial cells also play key roles in developmental processes as evidenced by the organizer activity they develop to promote budding and regeneration. We propose here an integrative view of the homeostatic and developmental aspects of epithelial plasticity in Hydra.

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Highlights in General Media about our Research (selection)

2017

Radio RTS la 1ère, CQFD by Silvio Dolzan, Pierre Bratschi. Il reste de la vie après la mort. Oct. 30 (9 min). https://www.rts.ch/play/radio/cqfd/audio/il-reste-de-la-vie-apres-la-mort?id=9002141

Le Temps, Brigitte Galliot et Denis Duboule: en constante évolution. by Sylvie Logean, Oct. 3. https://www.letemps.ch/sciences/2017/10/03/brigitte-galliot-denis-duboule-constante-evolution

2016

Radio RTS la 1ère, CQFD Rencontre avec Brigitte Galliot emission de S. Gabioud avec Adrien Zerbini (36 min). http://www.rts.ch/la-1ere/programmes/cqfd/8055408-rencontre-avec-brigitte-galliot-14-10-2016.html

2015 

Online Movie on the AcademiaNet Project (database of excellent female scientists). Bosch Stiftung. http://www.academia-net.org/project/

Jeunesse éternelle. Simples Immortels. Documentary movie by Romain Miranda for TSR (TV Swiss channel), “Mise au Point” Oct. 25, 2015. http://www.rts.ch/emissions/mise-au-point/7086228-conseil-federal-peages-urbains-jeunesse-eternelle.html

Interview on the channel RTS (Radio Télévision Suisse Romande), CQFD program 2015. Journalist: Bastien Confino.
L’hydre modifie son programme génétique

  • http://www.rts.ch/la-1ere/programmes/cqfd/7237869-l-hydre-modifie-son-programme-genetique-23-11-2015.html 
  • interview accessible on the site Avis d’Experts: http://avisdexperts.ch/videos/view/4613/10 (10 minutes)
    • Hydra can modify its genetic program. Science Daily, 23.11.2015
    • Las hidras pueden modificar su programa genético. Noticias de la Ciencia y la Tecnologia, 26.11.2015
    • Immortal Hydra Is Able To Genetically Modify Itself. IFL Science, 26.11.2015
    • Hydra genetically reprograms skin cells after losing its nerve. The Guardian, 27.11.2015
    • Comment survivre sans neurones. Pour la Science, 03.12.2015
    • L’hydre peut vivre sans cerveau. Elle n’est pas la seule. Le Matin, 04.12.2015
    • Ein leuchtender Jungbrunnen.  faz.net / Frankfurter Allgemeine Zeitung Online, 28.11.2015

2012

Interview on the channel RTS (Radio Télévision Suisse Romande), CQFD program 2015. Journalist: Bastien Confino.
L'hydre, du mythe à la science : http://www.rts.ch/la-1ere/programmes/cqfd/4469156-l-hydre-du-mythe-a-la-science-13-12-2012.html

2009

Report on the Evening News at the Swiss TV of the discovery of cell death and regeneration. DÉCOUVERTE SUR LA FACULTÉ DE RÉGÉNÉRATION DE L'HYDRE
This interview is accessible on the site Avis d’Experts: http://www.avisdexperts.ch/videos/view/925  (2’03 minutes)

 

Movies 

1999     

Galliot B. L’hydre, un embryon immortel.  (8 min) Université de Genève

2003     

Regeneration and Stem Cells (52 min) Documentary movie directed by Jean-Marie Cornuel produced by Télé-Images-Nature. www.teleimages.com/newsletter.htm

2007

L’immortalité? (70 min). 36°9, produced and directed by Mario Fossatti & Isabelle Moncada. Documentary movie produced by the TSR (Télévision Suisse Romande). (French)
http://www.rts.ch/play/tv/36-9/video/le-secret-de-lhydre?id=57661

2008    

Quand la science va à la plage!   Documentary movie directed by Claude-Julie Parisot, produced by KAMI products for ARTE channel.
http://boutique.arte.tv/f2355-quandlasciencevaalaplage

2009   

Einstein: Der Polyp mit dem Ewigen Leben. (3.30 min) Documentary movie produced by SF (Schweizer Fernsehen).

2014     

Immortels. (52 min) Directed by Sarah Lainé. Coproduction : DOCLAND YARD, AB PRODUCTIONS  for Encyclo (Science et Vie TV), a channel dedicated to discovery and scientific knowledge (French)
http://www.gedeonprogrammes.com/wp-content/uploads/2014/01/CATALOGUE-GEDEON_2_VF_BD2.pdf

 

Publications as Guest Editor of special issues

Galliot, B, Tanaka, E.M. Simon A. guest editors of “Cellular and Molecular Basis of Regeneration and Tissue Repair”. Cellular and Molecular Life Sciences, vol. 65, issue 1 (9 articles).

Galliot B. guest editor of « The Hydra model system » International Journal of Developmental Biology, vol 56, issues 6/7/8 (22 articles).

Galliot B. guest editor of “Mechanisms of Regeneration” (11 articles) Current Topics in Developmental Biology, 108,  http://www.sciencedirect.com/science/bookseries/00702153

 

Articles on Science and Society

2003

Galliot B. A lire avant de vous lancer dans une carrière de chercheuse. Médecine & Hygiène, 2459, 2303-2306. https://www.revmed.ch/RMS/2003/RMS-2459/1215

2007

Galliot B. La culture scientifique pour une honnête femme du 21ème siècle, est-ce encore possible ? édité par J-J Forney, Fondation Culture & Rencontre, Genève. https://archive-ouverte.unige.ch/unige:38931

2008

Gehring W, Galliot B and Piraino S. In memoriam: Volker Schmid. Int J Dev Biol, 52, 1013 – 1014.http://www.ijdb.ehu.es/web/paper/082708wg/in-memoriam-volker-schmid-1939-2008

2016

Lievens P, Galliot B, Floors F et al. Fundamental Research in HORIZON2020. LERU paper, in press.

Lievens P, Galliot B, Floors F et al. (LERU natural sciences working group). The strength of collaborative research for discovery in HORIZON2020. LERU note, https://www.leru.org/files/The-Strength-of-Collaborative-Research-for-Discovery-in-Horizon-2020-Full-paper.pdf

2017

Väänänen J, van Tienderen P, et al. (LERU Natural Sciences policy group). Four Golden Principles for enhancing the quality, access and impact of research infrastructures LERU note, https://www.leru.org/publications/four-golden-principles-for-enhancing-the-quality-access-and-impact-of-research-infrastructures

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