Biology of ciliated epithelia

Group leader : L. Kodjabachian

Our team aims to understand ciliated epithelia biology.


In all vertebrates, specialized ciliated tissues are covered with cells harboring dozens of motile cilia, beating coordinately to generate directional fluid flow. Multiciliated cells help airway cleansing, ovum implantation and cerebrospinal fluid circulation.


Scanning Electron Microscopy photograph of the mature ciliated epidermis. Green: Multiciliated cell. Red: Mucus secretory cell (also called goblet cell). Dark brown: Smal secretory cell (produces serotonin). Yellow: Ionocyte.

Thus, several human pathologies caused by ciliary defects are characterized by chronic respiratory distress, brain abnormalities and reduced fertility. However, the biology of multiciliated cells remains poorly understood, due to the paucity of accessible in vivo models. Our team studies the embryonic skin of the amphibian Xenopus laevis, which is proving very powerful to reveal molecular and cellular principles of multiciliogenesis conserved with humans.

The Xenopus laevis embryo is easily amenable to manipulation of protein-coding genes as well as non-coding RNAs (microRNAs, long non coding RNAs) through micro-injection of mRNA constructs or antisense morpholinos, from the time of fertilization. The ciliated epidermis is particularly suited for functional analysis as it can be targeted specifically and lies at the surface of the embryo, which facilitates light and electron microscopy imaging. This tissue can also easily be exposed to pharmacological compounds and recombinant proteins at various stages of its development, and subjected to transgenesis to trace and manipulate the various cell types that compose it.

This picture shows the epidermis of a xenope tailbud-stage embryo, allowing study of ciliogenesis.

Transverse section through the epidermis of a tailbud-stage embryo. Nuclei are stained with DAPI in blue. Basal cells are stained by immunostaining against P63 in white. Multiciliated cells are stained by fluorescent in situ hybridization against alpha-tubulin in green. Ionocytes are stained by fluorescent in situ hybridization against the ATPase V1A in red.

Ciliogenesis has emerged as a key biological phenomenon in many developmental and physiological processes. Deficient ciliogenesis is the cause of numerous diseases, collectively called ciliopathies. Cilia can be motile and help generate biological fluid flows, or immotile and function as sensing and signalling platforms. Ciliogenesis is a complex process, which mobilizes several hundreds of distinct proteins. Additional complexity is coming with the differentiation into multiciliated cells that require a dramatic reorganization of the microtubular network and a 20-fold increase in the apical cell membrane.

In certain chronic airway diseases, regeneration of a functional mucociliary epithelium is important for proper healing. From this prospect, understanding the mechanisms governing the biosynthesis of multiciliated cells is a fundamental issue with high biomedical relevance.

The embryonic Xenopus laevis epidermis contains a mucociliary epithelium similar to the one covering our airways. In both cases, the epithelium is composed of mucus-secreting cells and of multiciliated cells, and represents the first line of defense against germs and pollutants. In Xenopus, the mature epithelium is set in place through four successive steps :

The four steps of ciliated epithelium formation.

Our team currently studies steps 2 to 4: i. specification of the various cell types present in the epidermis. ii. insertion of ciliated cell precursors in the superficial epithelial layer. iii. differentiation of multiciliated cells. We focus on the roles in these processes of signalling pathways and microRNAs, as the former often control cell fate decisions whereas the latter often control developmental transitions and differentiation. Our long-term goal is to generate an integrated view of the key mechanisms necessary to build and maintain the functional mucociliary epithelium that are conserved in humans.

Selected publications


A live-imaging protocol to track cell movement in the Xenopus embryo

Chuyen A, Daian F, Pasini A, Kodjabachian L.
STAR Protoc . 2021 Nov 2;2(4):100928. doi: 10.1016/j.xpro.2021.100928. eCollection 2021 Dec 17. PMID: 34778847


The Scf/Kit pathway implements self-organised epithelial patterning.

Alexandre Chuyen, Charlotte Rulquin, Fabrice Daian, Virginie Thomé, Raphaël Clément, Laurent Kodjabachian, Andrea Pasini
Dev Cell . 2021 Mar 22;56(6):795-810.e7. doi: 10.1016/j.devcel.2021.02.026. PMID: 33756121


Biology of multiciliated cells

Camille Boutin, Laurent Kodjabachian
Curr Opin Genet Dev . 2019 Jun;56:1-7. doi: 10.1016/j.gde.2019.04.006 PMID: 31102978


CDC20B is required for deuterosome-mediated centriole production in multiciliated cells.

Revinski, DR., Zaragosi, L-E., Boutin, C., Ruiz Garcia, S., Deprez, M., Rosnet, O., Thomé, V., Mercey, O., Paquet, A., Pons, N., Marcet, B*., Kodjabachian, L*. and Barbry, P*. Equal contribution, corresponding authors*.
Nature Communications. 9:4668. PMID: 30405130


Nodal–Activin pathway is a conserved neural induction signal in chordates

Yann Le Petillon, Guillaume Luxardi, Pierluigi Scerbo, Marie Cibois, Anthony Leon, Lucie Subirana, Manuel Irimia, Laurent Kodjabachian, Hector Escriva and Stephanie Bertrand
Nature Ecology & Evolution PMID: 28782045


Lineage commitment of embryonic cells involves MEK1-dependent clearance of pluripotency regulator Ventx2.

Scerbo P, Marchal L, Kodjabachian L.
Elife. 2017 Jun 27;6. pii: e21526. PMID: 28654420


BMP signalling controls the construction of vertebrate mucociliary epithelia.

Cibois M, Luxardi G, Chevalier B, Thomé V, Mercey O, Zaragosi LE, Barbry P, Pasini A, Marcet B, Kodjabachian L.
Development. 2015 Jul 1;142(13):2352-63. PMID: 26092849


Control of vertebrate multiciliogenesis by miR-449 through direct repression of the Delta/Notch pathway.

Marcet B, Chevalier B , Luxardi G , Coraux C , Zaragosi LE, Cibois M, Robbe-Sermesant K, Jolly T, Cardinaud B, Moreilhon C, Giovannini-Chami L, Nawrocki-Raby B, Birembaut P, Waldmann R, Kodjabachian L*, Barbry P*. ( co-second authors) (*co-senior authors) Highlighted on CNRS website, CNRS Le Journal and One Year with CNRS 2011.
Nat Cell Biol. 2011 Jun;13(6):693-9. PMID: 21602795


Distinct Xenopus Nodal ligands sequentially induce mesendoderm and control gastrulation movements in parallel to the Wnt/PCP pathway.

Luxardi G, Marchal L, Thomé V, Kodjabachian L.
Development. 2010 Feb;137(3):417-26. PMID: 20056679


BMP inhibition initiates neural induction via FGF signaling and Zic genes.

Marchal L, Luxardi G, Thomé V, Kodjabachian L.
Proc Natl Acad Sci U S A. 2009 Oct 13;106(41):17437-42. PMID: 19805078


Neural induction in Xenopus requires early FGF signalling in addition to BMP inhibition.

Delaune E, Lemaire P, Kodjabachian L.
Development. 2005 Jan;132(2):299-310. PMID: 15590738


ECT2 associated to PRICKLE1 are poor-prognosis markers in triple-negative breast cancer

Daulat AM, Finetti P, Revinski D, Silveira Wagner M, Camoin L, Audebert S, Birnbaum D, Kodjabachian L, Borg JP, Bertucci F.
Br J Cancer . 2019 Apr;120(9):931-940. doi: 10.1038/s41416-019-0448-z. Epub 2019 Apr 11. PMID: 30971775


Notch1 is asymmetrically distributed from the beginning of embryogenesis and controls the ventral center

Castro Colabianchi, AM*, Revinski, DR*, Encinas, PI., Baez, MV., Monti, RJ., Abinal, MR., Kodjabachian, L., Franchini, LF. and López, SL.
Development. 145(14). pii: dev159368. PMID: 29866901


A Bioresistant Nitroxide Spin Label for In-Cell EPR Spectroscopy: In Vitro and In Oocytes Protein Structural Dynamics Studies.

Karthikeyan G, Bonucci A, Casano G, Gerbaud G, Abel S, Thomé V, Kodjabachian L, Magalon A, Guigliarelli B, Belle V, Ouari O, Mileo E.
Angew Chem Int Ed Engl. 2018 Jan 26;57(5):1366-1370. doi: 10.1002/anie.201710184. PMID: 29227566


Animal multicellularity and polarity without Wnt signaling.

Schenkelaars Q, Pratlong M, Kodjabachian L, Fierro-Constain L, Vacelet J, Le Bivic A, Renard E, Borchiellini C.
Sci Rep. 2017 Nov 13;7(1):15383. doi: 10.1038/s41598-017-15557-5. PMID: 29133828


Planar cell polarity in ciliated epithelia.

Walentek, P., Boutin, C. and Kodjabachian, L.
Cell Polarity in Development and Disease (ed. DW Houston), Elsevier.


MicroRNAs as key regulators of GTPase-mediated apical actin reorganization in multiciliated epithelia

Mercey O, Kodjabachian L, Barbry P, Marcet B.
Small GTPases . 2016 Apr 2;7(2):54-8. doi: 10.1080/21541248.2016.1151099. PMID: 27144998


Identification of p62/SQSTM1 as a component of non-canonical Wnt VANGL2-JNK signalling in breast cancer.

Puvirajesinghe TM, Bertucci F, Jain A, Scerbo P, Belotti E, Audebert S, Sebbagh M, Lopez M, Brech A, Finetti P, Charafe-Jauffret E, Chaffanet M, Castellano R, Restouin A, Marchetto S, Collette Y, Gonçalvès A, Macara I, Birnbaum D, Kodjabachian L, Johansen T, Borg JP.
Nat Commun. 2016 Jan 12;7:10318. PMID: 26754771


The PTK7 and ROR2 Protein Receptors Interact in the Vertebrate WNT/Planar Cell Polarity (PCP) Pathway

Martinez S, Scerbo P, Giordano M, Daulat AM, Lhoumeau AC, Thomé V, Kodjabachian L, Borg JP.
J Biol Chem. 2015 Dec 18;290(51):30562-72. PMID: 26499793


miR-34/449 control apical actin network formation during multiciliogenesis through small GTPase pathways

Chevalier B, Adamiok A, Mercey O, Revinski DR, Zaragosi LE, Pasini A, Kodjabachian L, Barbry P, Marcet B.
Nat Commun. 2015 Sep 18;6:8386. PMID: 26381333


Induction and Differentiation of the Xenopus Ciliated Embryonic Epidermis.

Cibois, M., Scerbo, P., Thomé, V., Pasini, A. and Kodjabachian, L.
Xenopus Development (eds M. Kloc and J. Z. Kubiak), John Wiley & Sons, Inc, Oxford. doi: 10.1002/9781118492833.ch7


Dysregulation of Wnt Inhibitory Factor 1 (Wif1) expression result in aberrant Wnt-β-catenin signaling and cell death of the cloaca endoderm, and anorectal malformations.

Ng RC, Matsumaru D, Ho AS, Garcia-Barceló MM, Yuan ZW, Smith D, Kodjabachian L, Tam PK, Yamada G, Lui VC
Cell Death Differ. 2014 Jun;21(6):978-89. PMID: 24632949


Xenopus embryonic epidermis as a mucociliary cellular ecosystem to assess the effect of sex hormones in a non-reproductive context.

Castillo-Briceno P, Kodjabachian L.
Front Zool. 2014 Feb 6;11(1):9. PMID: 24502321


On the Origin and Evolutionary History of NANOG.

Scerbo P, Markov GV, Vivien C, Kodjabachian L, Demeneix B, Coen L, Girardot F.
PLoS One. 2014 Jan 17;9(1):e85104. PMID: 24465486


A gene regulation network controlled by Celf1 protein-rbpj mRNA interaction in Xenopus somite segmentation.

Cibois M, Gautier-Courteille C, Kodjabachian L, Paillard L.
Biol Open. 2013 Aug 30;2(10):1078-83. PMID: 24167718


The human PDZome: a gateway to PDZ mediated functions.

Belotti E, Polanowska J, Daulat AM, Audebert S, Thome V, Lissitzky JC, Lembo F, Biblek K, Omi S, Lenfant N, Gangar A, Montcouquiol M, Santoni MJ, Sebbagh M, Aurrand-Lions M, Angers S, Kodjabachian L, Reboul J, Borg JP.
Mol Cell Proteomics. 2013 May 30. PMID: 23722234


Ventx factors function as Nanog-like guardians of developmental potential in Xenopus.

Scerbo P, Girardot F, Vivien C, Markov GV, Luxardi G, Demeneix B, Kodjabachian L, Coen L.
PLoS One. 2012;7(5):e36855. PMID: 22606298


An essential role for transcription before the MBT in Xenopus laevis.

Skirkanich J, Luxardi G, Yang J, Kodjabachian L, Klein PS.
Dev Biol. 2011 Sep 15;357(2):478-91. PMID: 21741375


MicroRNA-based silencing of Delta/Notch signaling promotes multiple cilia formation.

Marcet B, Chevalier B, Coraux C, Kodjabachian L, Barbry P.
Cell Cycle. 2011 Sep 1;10(17):2858-64. PMID: 21857154


MicroRNA control biosynthesis of motile cilia in vertebrates.

Chevalier B, Kodjabachian L, Coraux C, Barbry P, Marcet B.
Med Sci (Paris). 2011 Jun-Jul;27(6-7):671-3. PMID: 21718654


PTK7: a cell polarity receptor with multiple facets.

Lhoumeau AC, Puppo F, Prébet T, Kodjabachian L, Borg JP.
Cell Cycle. 2011 Apr 15;10(8):1233-6. PMID: 21415598


Protein tyrosine kinase 7 has a conserved role in Wnt/β-catenin canonical signalling.

Puppo F*, Thomé V*, Lhoumeau AC, Cibois M, Gangar A, Lembo F, Belotti E, Marchetto S, Lécine P, Prébet T, Sebbagh M, Shin WS, Lee ST, Kodjabachian L ¶ , Borg JP ¶ . (*co-first authors) (¶ co-first authors)  
EMBO Rep. 2011 Jan;12(1):43-9. PMID: 21132015


Wnt inhibitory factor 1 is epigenetically silenced in human osteosarcoma, and targeted disruption accelerates osteosarcomagenesis in mice.

Kansara M, Tsang M, Kodjabachian L, Sims NA, Trivett MK, Ehrich M, Dobrovic A, Slavin J, Choong PF, Simmons PJ, Dawid IB, Thomas DM.
J Clin Invest. 2009 Apr;119(4):837-51. PMID: 19307728


Role of Siamois before and during gastrulation. In Gastrulation : From cells to embryo

Kodjabachian L, and Lemaire P.

New-York : Cold Spring Harbor Laboratory Press. (2004) (ed. C.D. Stern), pp 609-617


Siamois functions in the early blastula to induce Spemann's organiser.

Kodjabachian L, Lemaire P.
Mech Dev. 2001 Oct;108(1-2):71-9. PMID: 11578862


Morphogen gradients: nodal enters the stage.

Kodjabachian L.
Curr Biol. 2001 Aug 21;11(16):R655-8. PMID: 11525759


A study of Xlim1 function in the Spemann-Mangold organizer.

Kodjabachian L, Karavanov AA, Hikasa H, Hukriede NA, Aoki T, Taira M, Dawid IB.
Int J Dev Biol. 2001;45(1):209-18. PMID: 11291848


A new secreted protein that binds to Wnt proteins and inhibits their activities.

Hsieh JC*, Kodjabachian L*, Rebbert ML, Rattner A, Smallwood PM, Samos CH, Nusse R, Dawid IB, Nathans J. (*co-first authors)
Nature. 1999 Apr 1;398(6726):431-6. PMID: 10201374


Embryonic induction: is the Nieuwkoop centre a useful concept?

Kodjabachian L, Lemaire P.
Curr Biol. 1998 Dec 17-31;8(25):R918-21. PMID: 9889093


A role for the vegetally expressed Xenopus gene Mix.1 in endoderm formation and in the restriction of mesoderm to the marginal zone.

Lemaire P, Darras S, Caillol D, Kodjabachian L.
Development. 1998 Jul;125(13):2371-80. PMID: 9609820


Mutations in ccf, a novel Drosophila gene encoding a chromosomal factor, affect progression through mitosis and interact with Pc-G mutations.

Kodjabachian L, Delaage M, Maurel C, Miassod R, Jacq B, Rosset R.
EMBO J. 1998 Feb 16;17(4):1063-75. PMID: 9463384


The vertebrate organizer: structure and molecules.

Lemaire P, Kodjabachian L.
Trends Genet. 1996 Dec;12(12):525-31. PMID: 9257536


The homeobox gene Siamois is a target of the Wnt dorsalisation pathway and triggers organiser activity in the absence of mesoderm.

Carnac G, Kodjabachian L, Gurdon JB, Lemaire P.
Development. 1996 Oct;122(10):3055-65. PMID: 8898219


  • Barbry Team, Institute of Molecular and Cellular Pharmacology (Sophia-Antipolis)
  • Borg Team, Cancer Research Center of Marseille
  • Azimzadeh Team, Institut Jacques Monod (Paris)


Kodjabachian team, who studies ciologenesis and MicroRNAs is funded by the ANR

Kodjabachian team, who studies mucociliary epithelium and ciologenesis is funded by the Institut National du Cancer

Kodjabachian team, who studies ciliated epithelium on xenope is funded by the Fondation de Recherche Médicale

Kodjabachian team, who studies MicroRNAs is funded by the Association pour la Recherche contre le Cancer


Members more

  Athullya Baby Camille Boutin Claire Schirmer Virginie Thome  
Laurent Kodjabachian
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Laurent Kodjabachian


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Steviny Ramdani

MSc student

Athullya Baby
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Athullya Baby

PhD student

Camille Boutin
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Camille Boutin


Claire Schirmer
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Claire Schirmer

Technical staff

Virginie Thome
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Virginie Thome

Technical staff

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Amel Toudji-zouaz

Technical staff


  • Marie Cibois, Post-doc
  • Anna Adamiok, PhD
  • Patricia Castillo-Briceno, Post-doc
  • Guillaume Luxardi, PhD
  • Leslie Marchal, PhD
  • Emilie Delaune, PhD


Model organism
Biological process studied
  • Construction of a ciliated epithelium
Biological techniques
  • Micro-injection
  • Micro-surgery
  • Fluorescent In Situ Hybridization
  • Immunohistochemistry
  • Real-time PCR
  • Confocal microscopy
  • Electron microscopy
  • Morpholino-mediated knockdown


Xenbase : Xenopus laevis and Xenopus tropicalis biology and genomics resource