Laboratory of regeneration and adult neurogenesis

Laboratory director

Prof. Brigitte Galliot
  • Associate Professor

+41 22 379 67 74
4055B (Sciences III)
4, Bvd d'Yvoy
CH-1205 Geneva

Research topics

  1. Summary
  2. The Hydra model system in few words
  3. Functional analysis of the genetic circuitry supporting regeneration in Hydra
  4. The emergence of neurogenesis and apical patterning in metazoans
  5. References

Keywords: hydra, cnidarian, regeneration, cellular remodelling, developmental plasticity, homeostasis, injury, wound healing, growth control, patterning, apoptosis-induced compensatory proliferation, signaling, evolution, neurogenesis

1. Summary

A fascinating, unanswered question in biology is how some organisms respond to injury by regenerating the missing body structure, whereas other have lost this potential. Here we propose to use the freshwater Hydra polyp as regeneration model organism to tackle this question. Indeed, Hydra is a simple animal that provides a powerful model system to understand how a highly dynamic homeostasis contributes to link wound healing to tissue repair and regeneration. The questions we address in our research are the following:

  • HOMEOSTASIS & REGENERATION: What are the cellular and molecular mechanisms that maintain homeostasis in Hydra and drive regeneration after bisection?
  • STEM CELLS: What are the respective functions of the stem cells and the differentiated cells in these processes?
  • MEMORY: What are the memory mechanisms that allow the regenerating tip to regrow the appropriate missing structure, i.e. a head on one side and a foot on the other side of the bisection?
  • ADULT NEUROGENESIS: What is the genetic circuitry that leads to de novo neurogenesis in cnidarians?
  • AGING: What are the mechanisms that keep the developmental program(s) such as head regeneration, foot regeneration and asexual reproduction (budding) accessible all along the hydra life?
  • EVOLUTION: Which of these mechanisms have been conserved along evolution?

To elucidate these questions, we want identify thanks to RNA interference (RNAi) the signaling cascades that govern cellular and developmental plasticity in Hydra. We recently showed that apoptosis-induced compensatory proliferation provides a mechanism to launch a complex regeneration program such as head regeneration. Interestingly apoptosis-induced compensatory proliferation seems to be also at work when Xenopus regenerates its tail, when Drosophila larvae regenerates their imaginal discs or even when rodents regenerate their skin or their liver (for recent reviews see [1, 2]). These results suggest that there might be some common paths to launch a regenerative response.

Figure 1: Schema depicting the position of Hydra in the metazoan tree. Among cnidarians, anthozoans (corals, sea anemones) live exclusively as polyps, whereas medusozoans (jellyfish) alternate between the medusa and polyp stages during their life cycle. Hydra is a freshwater polyp that lost the medusa stage.

2. The Hydra model system in few words

Hydra belongs to Cnidaria, a sister group to bilaterians (Fig.1). The anatomy of Hydra is rather simple: this is basically a bilayered tube that shows an apical-basal polarity, with at one extremity a head region that includes a mouth/anus opening and a ring of tentacles to actively catch the food (Hydra are carnivorous), and at the other extremity a basal disc. Its cellular organization is rather simple, with two cell layers, the ectoderm and the endoderm separated by an extracellular collagenoeous matrix, the mesogolea. Hydra differentiates all cell types required for neuro-muscular transmission, digestion, secretion and sexual reproduction. These different cell types differentiate from three distinct stem cell populations: myoepithelial cells located in the ectoderm, myoepithelial cells located in the endoderm and interstitial cells that are multipotent stem cells giving rise to neurons, mechano-sensory cells (nematocytes or cnidocytes), gland cells and gametes [3, 4].

Over the past 25 years, the genes encoding the signaling proteins that control and execute various cellular behaviors and developmental processes were shown to be present in all animals. The recent sequencing of the genome of two cnidarian species (Nematostella vectensis – sea anemone - and Hydra magnipapillata) indeed confirmed this high level of gene conservation from cnidarians to vertebrates. This definitively supports the relevance of Hydra as a model system to investigate complex biological questions [5, 6].

3. Functional analysis of the genetic circuitry supporting regeneration in Hydra

Gene silencing through RNAi by feeding identifies cellular phenotypes that are shared between Hydra and man

RNAi gene silencing obtained by feeding the animal on dsRNA-producing bacteria was first described in C. elegans and more recently adapted to planarians [7-9]. We adapted this strategy to Hydra (Fig. 2) and proved that this method that is harmless, stepwise and efficient, can induce gene-specific phenotypes [10-13]. In case of the protease inhibitor Kazal1that isspecifically expressed in gland cells of the gastrodermis, RNAi silencing induces a massive autophagy that extends to the digestive cells. This phenotype, which mimics the human SPINK1/mouse SPINK3 pancreatic phenotype, provides the first example of a conserved cellular mechanism from cnidarians to mammals, an example that definitely strengthen the paradigmatic value of this little animal.

This strategy offers the possibility of systematic RNAi screens in Hydra.

Gene silencing by RNA interference in Hydra
Figure 2: Gene silencing by RNA interference in Hydra. The dsRNA feeding strategy developed in nematodes [7, 8] and planarians [9] was adapted to Hydra polyps. Double-stranded RNAs are produced in bacteria and Hydra polyps are repeatedly fed with the bacteria-agarose mixture {Chera, 2006 #212; Buzgariu, 2008 #174}.

4. The apoptosis-dependent activation of the Wnt pathway in head-regenerating tips.

The canonical Wnt pathway is perfectly conserved in Hydra and required for the head to regenerate properly [14, 15]. We recently showed that an asymmetrical wave of apoptosis occurs immediately after mid-gastric bisection affecting 50% of the cells in head-regenerating tips but less than 7% in foot-regenerating ones [13]. Apoptotic cells actually transiently release the Wnt3 signal that activates b-catenin in the surrounding S-phase cells. Indeed progenitors migrate towards the wound, accumulate underneath the apoptotic zone and rapidly divide forming a proliferative zone. Upon inhibition of apoptosis by caspase inhibitors, or upon Wnt3 or b-catenin RNAi silencing, cell proliferation and head regeneration are abolished, whereas simply adding exogenous Wnt3 fully rescues these processes. Conversely
induction of apoptosis in foot-regenerating tips converts them to regenerate heads through the activation of the Wnt3/b-catenin pathway. Hence the level of apoptosis appears critical to trigger compensatory proliferation and head regeneration through the Wnt pathway.

Bi-headed Hydra resulting from the ectopic apoptosis-induced activation of the Wnt3-bcatenin pathway
Figure 3: Bi-headed Hydra resulting from the ectopic apoptosis-induced activation of the Wnt3-bcatenin pathway. Hydra polyps bisected at mid-gastric position regenerate a head from the lower half and a basal disc from the upper one. Here Hydra upper halves were forced to regenerate a head instead of a basal disc. This was obtained by inducing a high level of apoptosis in foot-regenerating tips by briefly heating them immediately after bisection. Ectopic apoptosis leads to the activation of the Wnt3-bcatenin pathway as observed in head-regenerating stumps and therefore converted foot regeneration to head regeneration (see in [1, 2]).

The immediate asymmetric regulation of the MAPK ➜ RSK ➜ CREB ➜ CBP pathway

The MAPK/CREB pathway seems to play a key role in the induction of the head regeneration process. Indeed the cAMP Response Element Binding (CREB) protein is a transcription factor that likely interacts with distinct partners in CRE-binding complexes immediately after bisection [16], and exhibits a series of immediate regulations in the head- but not in the foot-regenerating tips as an RSK-dependent phosphorylation [17] and a rapid up-regulation of the CREB gene expression [18]. In vertebrates, the phosphorylated form of CREB binds to the chromatin modifyer CBP in order to modulate gene expression. Similarly the Hydra CBP encodes a CREB-binding domain and silencing of either RSK or CREB or CBP prevents the immediate wave of apoptosis and the cellular reorganization normally observed in head-regenerating tips (Chera and Galliot, submitted). We are currently investigating how this signaling pathway can sense the stress of amputation to activate a head regeneration program.

The emergence of neurogenesis and apical patterning in metazoans

In Hydra neurogenesis takes place continuously in the adult polyp but the dense apical nervous system also forms de novo in budding and regenerating animals [19- 21]. In bilaterian animals whose ancestor already had a centralized nervous system and sensory organs, the homeobox genes of the ANTP and PAIRED class play a major role in the developing central nervous system [22-24]. Each class includes a large number of families that for most of them diversified quite early in animal evolution, preceding the divergence of Cnidaria [25-27]. This raises the question of the function of these gene families in cnidarians (that differentiate a sophisticated nervous system) and in poriferans (that have no nervous system)[21].

The PAIRED-class homeobox genes

Among evolutionary conserved gene families involved in the specification of brain and sensory organs in bilaterians, several are expressed in the nervous system of cnidarians [28-32]. Among these, the paired-class homeobox gene prdl-a, is expressed in apical nerve cells in adult polyps but after bisection, transiently in endodermal cells of the head-regenerating tip. This result suggested that prdl-a is involved in Hydra head organizer activity through inductive interactions from endoderm to the overlying ectoderm [19, 28]. This result was puzzling as some paired- like genes perform similar tasks at the time head organizer activity is established in mammals, suggesting that molecular mechanisms of anterior patterning can be traced back to cnidarians [33].

The Hox/ParaHox genes

Most ANTP-class gene families do have cnidarian counterparts although Hox-related families are not all present and less similar. In fact Hox-like genes were not found in poriferan, therefore, cnidarian Hox-like genes can be considered as representative of the proto-Hox genes [26, 34-36]. Out of them, cnox-2, theortholog of the paraHox Gsx gene, stimulates interest as its expression is restricted to the precursors of the neuronal and nematocyte cell lineages and cnox-2 is also upregulated during de novo apical neurogenesis at the time head is forming, during budding and in regenerating polyps [11, 26, 37]. When cnox-2 expression is silenced via RNAi, alterations of the apical nervous system and apical patterning process are observed. In vertebrates and Drosophila, Gsx is also involved in neurogenesis [38]. These data suggest an evolutionarily-conserved function for cnox-2/Gsx in neurogenesis and a possible functional link between neurogenesis and apical patterning established quite early in animal evolution [11, 20, 36].

5. References

  1. Galliot, B., and Chera, S. (2010) The Hydra model: disclosing an apoptosis-driven generator of Wnt-based regeneration. Trends Cell Biol in press
  2. Galliot, B., and Ghila, L. (2010) Cell plasticity in homeostasis and regeneration. Mol Reprod Dev in press
  3. Steele, R.E. (2002) Developmental signaling in Hydra: what does it take to build a “simple” animal? Dev Biol 248, 199-219
  4. Galliot, B., Miljkovic-Licina, M., de Rosa, R., and Chera, S. (2006) Hydra, a niche for cell and developmental plasticity. Semin Cell Dev Biol 17, 492-502
  5. Putnam, N.H., Srivastava, M., Hellsten, U., Dirks, B., Chapman, J., Salamov, A., Terry, A., Shapiro, H., et al. (2007) Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317, 86-94
  6. Chapman, J.A., Kirkness, E.F., Simakov, O., Hampson, S.E., Mitros, T., Weinmaier, T., Rattei, T., Balasubramanian, P.G., et al. (2010) The dynamic genome of Hydra. Nature 464, 592-596
  7. Timmons, L., Court, D.L., and Fire, A. (2001) Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene 263, 103-112
  8. Kamath, R.S., Martinez-Campos, M., Zipperlen, P., Fraser, A.G., and Ahringer, J. (2001) Effectiveness of specific RNA-mediated interference through ingested double-stranded RNA in Caenorhabditis elegans. Genome Biol 2, RESEARCH0002
  9. Newmark, P.A., Reddien, P.W., Cebria, F., and Sanchez Alvarado, A. (2003) Ingestion of bacterially expressed double-stranded RNA inhibits gene expression in planarians. Proc Natl Acad Sci U S A 100 Suppl 1, 11861-11865
  10. Chera, S., de Rosa, R., Miljkovic-Licina, M., Dobretz, K., Ghila, L., Kaloulis, K., and Galliot, B. (2006)
    Silencing of the hydra serine protease inhibitor Kazal1 gene mimics the human SPINK1 pancreatic phenotype. J Cell Sci 119, 846-857
  11. Miljkovic-Licina, M., Chera, S., Ghila, L., and Galliot, B. (2007) Head regeneration in wild-type hydra requires de novo neurogenesis. Development 134, 1191-1201
  12. Buzgariu, W., Chera, S., and Galliot, B. (2008) Methods to investigate autophagy during starvation and regeneration in hydra. Methods Enzymol 451, 409-437
  13. Chera, S., Ghila, L., Dobretz, K., Wenger, Y., Bauer, C., Buzgariu, W., Martinou, J.C., and Galliot, B. (2009) Apoptotic cells provide an unexpected source of Wnt3 signaling to drive hydra head regeneration. Dev Cell 17, 279-289
  14. Hobmayer, B., Rentzsch, F., Kuhn, K., Happel, C.M., von Laue, C.C., Snyder, P., Rothbacher, U., and Holstein, T.W. (2000) WNT signalling molecules act in axis formation in the diploblastic metazoan Hydra. Nature 407, 186-189
  15. Lengfeld, T., Watanabe, H., Simakov, O., Lindgens, D., Gee, L., Law, L., Schmidt, H.A., Ozbek, S., et al. (2009) Multiple Wnts are involved in Hydra organizer formation and regeneration. Dev Biol 330, 186-199
  16. Galliot, B., Welschof, M., Schuckert, O., Hoffmeister, S., and Schaller, H.C. (1995) The cAMP response element binding protein is involved in hydra regeneration. Development 121, 1205-1216
  17. Kaloulis, K., Chera, S., Hassel, M., Gauchat, D., and Galliot, B. (2004) Reactivation of developmental programs: the cAMP-response element-binding protein pathway is involved in hydra head regeneration. Proc Natl Acad Sci U S A 101, 2363-2368
  18. Chera, S., Kaloulis, K., and Galliot, B. (2007) The cAMP response element binding protein (CREB) as an integrative HUB selector in metazoans: clues from the hydra model system. Biosystems 87, 191-203
  19. Miljkovic-Licina, M., Gauchat, D., and Galliot, B. (2004) Neuronal evolution: analysis of regulatory genes in a first-evolved nervous system, the hydra nervous system. Biosystems 76, 75-87
  20. Galliot, B., Quiquand, M., Ghila, L., de Rosa, R., Miljkovic-Licina, M., and Chera, S. (2009) Origins of neurogenesis, a cnidarian view. Dev Biol 332, 2-24
  21. Galliot, B. (2010) A Key Innovation in Evolution, the Emergence of Neurogenesis: Cellular and Molecular Cues from Cnidarian Nervous Systems. In Key Transitions in Animal Evolution (Schierwater, B., and De Salle, R., eds), 127-161, Science Publishers & CRC Press
  22. Pichaud, F., and Desplan, C. (2002) Pax genes and eye organogenesis. Curr Opin Genet Dev 12, 430-434
  23. Hirth, F., Kammermeier, L., Frei, E., Walldorf, U., Noll, M., and Reichert, H. (2003) An urbilaterian origin of the tripartite brain: developmental genetic insights from Drosophila. Development 130, 2365-2373
  24. Denes, A.S., Jekely, G., Steinmetz, P.R., Raible, F., Snyman, H., Prud'homme, B., Ferrier, D.E., Balavoine, G., et al. (2007) Molecular architecture of annelid nerve cord supports common origin of nervous system centralization in bilateria. Cell 129, 277-288
  25. Galliot, B., de Vargas, C., and Miller, D. (1999) Evolution of homeobox genes: Q50 Paired-like genes founded the Paired class. Dev Genes Evol 209, 186-197
  26. Gauchat, D., Mazet, F., Berney, C., Schummer, M., Kreger, S., Pawlowski, J., and Galliot, B. (2000)
    Evolution of Antp-class genes and differential expression of Hydra Hox/paraHox genes in anterior patterning. Proc Natl Acad Sci U S A 97, 4493-4498
  27. Ryan, J.F., Burton, P.M., Mazza, M.E., Kwong, G.K., Mullikin, J.C., and Finnerty, J.R. (2006) The cnidarian-bilaterian ancestor possessed at least 56 homeoboxes. Evidence from the starlet sea anemone, Nematostella vectensis. Genome Biol 7, R64
  28. Gauchat, D., Kreger, S., Holstein, T., and Galliot, B. (1998) prdl-a, a gene marker for hydra apical differentiation related to triploblastic paired-like head-specific genes. Development 125, 1637-1645
  29. Lindgens, D., Holstein, T.W., and Technau, U. (2004) Hyzic, the Hydra homolog of the zic/odd- paired gene, is involved in the early specification of the sensory nematocytes. Development 131, 191-201
  30. Gauchat, D., Escriva, H., Miljkovic-Licina, M., Chera, S., Langlois, M.C., Begue, A., Laudet, V., and Galliot, B. (2004) The orphan COUP-TF nuclear receptors are markers for neurogenesis from cnidarians to vertebrates. Dev Biol 275, 104-123
  31. Stierwald, M., Yanze, N., Bamert, R.P., Kammermeier, L., and Schmid, V. (2004) The Sine oculis/Six class family of homeobox genes in jellyfish with and without eyes: development and eye regeneration. Dev Biol 274, 70-81
  32. Marlow, H.Q., Srivastava, M., Matus, D.Q., Rokhsar, D., and Martindale, M.Q. (2009) Anatomy and development of the nervous system of Nematostella vectensis, an anthozoan cnidarian. Dev Neurobiol 69, 235-254
  33. Galliot, B., and Miller, D. (2000) Origin of anterior patterning. How old is our head? Trends Genet 16, 1-5
  34. Chourrout, D., Delsuc, F., Chourrout, P., Edvardsen, R.B., Rentzsch, F., Renfer, E., Jensen, M.F., Zhu, B., et al. (2006) Minimal ProtoHox cluster inferred from bilaterian and cnidarian Hox complements. Nature 442, 684-687
  35. Chiori, R., Jager, M., Denker, E., Wincker, P., Da Silva, C., Le Guyader, H., Manuel, M., and Queinnec, E. (2009) Are Hox genes ancestrally involved in axial patterning? Evidence from the hydrozoan Clytia hemisphaerica (Cnidaria). PLoS ONE 4, e4231
  36. Quiquand, M., Yanze, N., Schmich, J., Schmid, V., Galliot, B., and Piraino, S. (2009) More constraint on ParaHox than Hox gene families in early metazoan evolution. Dev Biol 328, 173-187
  37. Schummer, M., Scheurlen, I., Schaller, C., and Galliot, B. (1992) HOM/HOX homeobox genes are present in hydra (Chlorohydra viridissima) and are differentially expressed during regeneration. Embo J 11, 1815-1823
  38. Mieko Mizutani, C., and Bier, E. (2008) EvoDevo: the origins of BMP signalling in the neuroectoderm. Nat Rev Genet 9, 663-677

Current team members

Dr Wanda Christa Buzgariu
  • Associate scientist

+41 22 379 67 66
4041 (Sciences III)
Dr Schippers Klaske
  • Postdoctoral Scholar

Dr Quentin Schenkelaars
  • Postdoctoral Scholar

+41 22 379 32 80
4027 (Sciences III)
Dr Matthias Vogg
  • Postdoctoral Scholar

+41 22 379 67 99
4055a (Sciences III)
Dr Yvan Wenger
  • Postdoctoral Scholar

+41 22 379 35 17
4041 (Sciences III)
Ms Sarah Al Haddad
  • PhD Student

+41 22 379 67 99
4055a (Sciences III)
Mr Nenad Suknovic
  • PhD Student

+41 22 379 32 80
4027 (Sciences III)
Mr Szymon Tomczyk
  • PhD Student

+41 22 379 67 59
4049B (Sciences III)
Ms Laura Bocanegra Moreno
  • Undergraduate Student

+41 22 379 67 59
4047 (Sciences III)
Ms Kazadi Bulundwe
  • Undergraduate Student

+41 22 379 67 59
4047 (Sciences III)
Mr Alessandro Cuozzo Vilá
  • Undergraduate Student

+41 22 379 35 17
4041 (Sciences III)
Ms Laura Iglesias Ollé
  • Undergraduate Student

022 379 67 99
4047 (Sciences III)
Ms Marie-Laure Curchod
  • Research assistant

+41 22 379 67 65
4047 (Sciences III)
Ms Mireille Guerrier
  • Research assistant

+41 22 379 67 99
4047 (Sciences III)
Ms Chrystelle Perruchoud
  • Research assistant

+41 22 379 67 59
4049B (Sciences III)
Mr Denis Benoni
  • Technical assistant

+41 22 379 66 67
2S014A (Sciences III)
Ms Valérie Mino
  • Secretary

+41 22 379 67 70
4002a (Sciences III)


Philos Trans R Soc Lond B Biol Sci. 2016 Jan 5;371(1685). pii: 20150040. doi: 10.1098/rstb.2015.0040. Pubmed

Loss of neurogenesis in Hydra leads to compensatory regulation of neurogenic and neurotransmission genes in epithelial cells.

Wenger Y, Buzgariu W, Galliot B

Front Genet. 2015 Aug 18;6:267. doi: 10.3389/fgene.2015.00267. eCollection 2015. Pubmed, link

The TALE face of Hox proteins in animal evolution.

Merabet S, Galliot B

DOI:10.1080/21688370.2015.1068908 link

Multifunctionality and plasticity characterize epithelial cells in Hydra

W Buzgariu, S Al Haddad, S Tomczyk, Y Wenger, B Galliot

Invertebr Reprod Dev. 2015 Jan 30;59(sup1):11-16. Epub 2014 Jun 19. Pubmed

Hydra, a powerful model for aging studies.

Tomczyk S, Fischer K, Austad S, Galliot B

Semin Immunol. 2014 Jul 30. pii: S1044-5323(14)00061-X. doi: 10.1016/j.smim.2014.06.004. Pubmed

Injury-induced immune responses in Hydra.

Wenger Y, Buzgariu W, Reiter S, Galliot B

Differentiation. 2014 Apr 2. pii: S0301-4681(14)00011-5. doi: 10.1016/j.diff.2014.03.001. Pubmed

Robust G2 pausing of adult stem cells in Hydra.

Buzgariu W, Crescenzi M, Galliot B

Curr Top Dev Biol. 2014;108:121-51. doi: 10.1016/B978-0-12-391498-9.00002-4. Pubmed

Cell death: a program to regenerate.

Vriz S, Reiter S, Galliot B

eLS, 3rd edition ed. John Wiley & Sons Ltd: Chichester, London. DOI: 10.1002/9780470015902.a0001096.pub3 link

Regeneration in Hydra

Galliot, B

Genome Biol Evol. 2013 Sep 23. Faculty1000 Prime Pubmed, link

Punctuated Emergences of Genetic and Phenotypic Innovations in Eumetazoan, Bilaterian, Euteleost and Hominidae ancestors.

Wenger Y, Galliot B

BMC Genomics. 2013 Mar 25;14(1):204. OPEN ACCESS / Highly accessed Pubmed, link

RNAseq versus genome-predicted transcriptomes: a large population of novel transcripts identified in an Illumina-454 Hydra transcriptome.

Wenger Y, Galliot B

Dev Genes Evol. 2013 Mar;223(1-2):39-52. Pubmed, 922 KB

Injury-induced asymmetric cell death as a driving force for head regeneration in Hydra.

Galliot B

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