Reproduction, development, ecotoxicology, and cell regulation

Published on April 7, 2015 Updated on March 29, 2016
Reproduction, development, ecotoxicology, and cell regulation
In order to understand some aspects of reproductive biology, several animal models are studied. The species studied essentially belong to Pisces (Osteichtyans), Amphibia, with more particularly Caecilians, and Reptilia. Several Mammalia living in arid areas are also studied and more especially small rodents. A part of studies is done with several collaborations, such as USTHB (Algiers, Algeria), Bejaia University (Algeria). Earthworms have also been studied such as bio-indicators, in collaborations with Oslo University and Bioforsk (Norway).

1. Osteichtyans (bony fish)

The works concern the sexual differentiation and reproductive cycles of fish economically important, such as the Black Bass (Micropterus salmoides), or having to be preserved, such as Apron (Zingel asper)-Christine Chevalier PhD, 2007).

In Micropterus salmoides, results have shown the sexual cycles of both males and females living in plain were quicker than that of animals living in mountain. In this mast case, the female sexual cycle is biennial, contrarily to the populations of plain in which cycle is annual. Temperature is the main physical factor acting on reproductive cycle.

In Zingel asper living in natural conditions, reproductive cycles have been described.
A study done in collaboration with Bejaia University (Algeria), concerns the reproductive cycles of Barbus callensis, living in polluted and non-polluted areas. Reproductive biology of animals of this species belonging to theses populations are still little known, but these animals present an economic interest. Males and females sexual cycles have been described. Some individuals captured in polluted areas presented hermaphroditism and intersex characteristics. The presence of endocrine disruptors in the river could be responsible of these sexual malformations.

publications

CHEVALIER, C., DE CONTO, C., EXBRAYAT, J.-M., 2008.- Apoptosis in Zingel asper (Percidae) ovarian and testicular development. Cybium, 32 (2) suppl.: 228-229.

CHEVALIER ,C. , DE CONTO, C. , EXBRAYAT, J-M. 2011. Reproductive Biology of the endangered percid Zingel asper in captivity: a histological description of the male reproductive cycle. Folia Histochemica et Cytobiologica. 49, (3), 2011 pp 486-496.

DE CONTO, C., CHEVALIER, C., EXBRAYAT, J.-M., 2008.- Histological study of Zingel asper (Percidae) sexual maturation : patterns of ovarian and testicular development. Cybium, 32 (2) suppl.: 230-231.
DJOUDAD-KADJI, H., KHERRAZ, A., CHEVALIER, C., IGUER-OUADA, M., EXBRAYAT , J.-M., 2013 (paru 2014). Etude de la dynamique testiculaire de l'espèce Barbus callensis(VALENCIENNES, 1842) en fonction des paramètres macroscopiques et microscopiques. Rev. Fr. Histotechnol.: 26 (1): 43-57
DJOUDAD-KADJI, H., BENSLIMANE, S.,CHEVALIER, C., KADJI, B., EXBRAYAT, J.-M, IGUER-OUADA, M. 2013. First observation of intersex in barbel Barbus callensis (Valenciennes, 1842) collected in Soummam River (Algeria). Cybium, 36 (4): 531-538
DJOUDAD-KADJI, H., KADJI, B., BENSLIMANE, S., EXBRAYAT, J.-M, IGUER-OUADA, M., CHEVALIER, C. 2012. Description histologique des diofférents stades de développement ovocytaire de Barvus callensis (Valenciennes, 1842) dans l'oued Soummam (Algérie). Rev. Fr. Histotechnol., 25 (1) : 11-19
DJOUDAD-KADJI, H., BENSLIMANE, S., CHEVALIER, C., KADJI , B., EXBRAYAT, J.-M., IGUER-OUADA, M., 2011. Visualisation des coupes histologiques des follicules ovariens de Barbus callensis : variation de fixateurs et de colorants. Rev. Fr. Histotech., 24 (1) :21-28.

2. Caecilian amphibians

Gymnophionan amphibians (still called Apoda or Caecilians) are elongated animals, without neither girdle nor limbs. They are generally described as blind, their eyes being covered with the skin of the skull; they have developed a pair of particular sensorial organs, the tentacles directly linked to the vomero-nasal organs. Their anatomy is narrowly linked to their burrowing mode of life. These animals are good models to study the adaptations to a biotope with a strong selection pressure.

A more particularly studied Gymnophionan species is Typhlonectes compressicauda, living in South America. The population studied is coming from Kaw marshes, in French Guiana. These animals are submitted to a wet tropical climate, with a rainy season from January until June, and dry season from July until December.

In this species, the sexual cycle of males is discontinuous with both spermatogenesis and breeding during the wet season; germ cells fill the testes and are stocked during the sexual rest, at dry season. Female are viviparous, with a biennial sexual cycle. This cycle is characterized by a first year devoted to pregnancy (February to September-October) and a second year of sexual quiescence. Some endocrine adaptations, narrowly to seasonal variations, regulate this cycle and allow gestation. At gestation, the oviducts are transformed in uterus. Each one is submitted to several histophysiological modifications according to the development of embryos.

The embryos first develop from their yolk mass; some buds cover their body, then the ectotrophoblast, a transitory ventral structure, develops. This structure is certainly implicated in the exchanges with the intra-uterine fluid. After the intra-uterine hatching, the embryos are equipped with fetal teeth persisting to the birth, with which they grasp the uterine wall, ingesting the secretions and the epithelial cells. At the end of development, the gills are transformed in two giant blades, enveloping the embryo that look like to be contained into a cocoon. These gills are narrowly applied against the uterine wall, resembling to the epitheliochorial placenta of some mammals.

The normal table of development has been published (Sammouri et al,, 1990). At presents, the development of each organ is deeply studied from a rich collection of histological sections and preparations for transmission electron microscopy.

The female sexual cycle of the direct-developing African species Boulengerula taitanus is studied. B. taitanus is a species living in Taita Hills (Kenya). The female sexual cycle is annual with a period of quiescence from March to August, a phase at which the animal is prepared to reproduction in September-October, and the reproductive period from November to February which ends with egg-laying during a short rainy season. The variations of oviducts in which fertilization occurs are parallel to that of ovaries. This cycle can be narrowly superimposed to which of males previously studied by Measey et al. (2008). A study showed the variations of several hormones (from ovaries and pituitary) and their receptors in female genital tract.

A comparative study between the viviparous T. compressicauda and the direct egg-laying B. taitanus showed several variations narrowly linked to the two reproductive cycles (Michel Raquet PhD, 2014).
In Boulengerula boulengeri, a very little known species coming from Tanzania, the ovaries and oviducts have been described during the reproductive period..

publications

EXBRAYAT, J-M., ESTABEL, J. 2006. Anatomy with particular reference to the reproductive system. In EXBRAYAT J;-M. (ed) Reproductive Biology and Phylogeny of Gymnophiona. Science Publishers Inc. 79-155.
MEASEY, G.J., SMITA, M., BEYO, R.S., OOMMEN, O.V., 2008. Year-round spermatogenic activity in an oviparous subterranean Caecilian, Boulengurula taitanus Loveridge 1935 (Amphibia Gymnophiona Caeciliidae). Tropical Zoology, 21: 109-122.
RAQUET, M., 2008. Modalités de la reproduction chez les femelles de Boulengerula taitanus, Amphibien Gymnophione. Diplôme de l'E.P.H.E.,129 p. Lyon,
RAQUET, M. 2014. Variations saisonnières et régulation hormonale des voies génitales femelles chez un amphibien ovipare et un amphibien vivipare. Thèse Doct. EPHE, Lyon.

RAQUET, M., MEASEY, J., EXBRAYAT, J.-M., 2011. Premières observations histologiques de l'oviducte de Boulengerula taitanus, Loveridge, 1935, Amphibien Gymnophione. Rev. Fr. Histotech., 24 (1) :29-38.
SAMMOURI, R., RENOUS, S., EXBRAYAT, J.-M., LESCURE, J. 1990. Développement embryonnaire de Typhlonectes compressicaudus (Amphibia Gymnophiona). Ann. Sci. nat., Zool., Paris, 13ème sér., 11 : 135 - 163.
SERCLERAT, H., MEASEY, J., EXBRAYAT, J.-M., CHEVALIER, C., 2011.Etude histologique des ovaires d'un Amphibien Gymnophione Boulengerula boulengeri pendant la période de reproduction. Rev. Fr. Histotech., 24 (1) :39-45.

3. Anuran amphibians


The male sexual cycles of African anurans are mainly of a continuous type, i.e. the testes contain all the germ cell categories throughout the year. The females, lesser studied than the males, possess a continuous oogenesis; the ovulation is observed when the climatic conditions are favorable.

In Amietophrynus regularis (Bufo regularis), one of the species studied by our group, we have previously shown that, in a population coming from Lomé (Togo), characterized by a large variability of rainy season, and a semi-arid climate, the male and female were always ready for reproduction if the rain begins to fall down. For that, in addition to the quantitative variations of genital tracts, we have observed several weak but well true variations of pituitary and Leydig-like cells of testes.
Amietophrynus mauritanicus (Bufo mauritanicus), a close species, is a toad living in North Africa. We are studying the sexual cycle of this species in a population living in the region of Beni-Belaid, characterized by a Mediterranean climate. This work is done in collaboration with the University of Jijel (Algeria) and the National Institute of Agronomy in Algiers (Algeria).Genital tracts have been described in both males and females. Sexual cycles are continuous in the two sexes. Yet, reproduction seems linked to the seasonal variations. The animals are submitted to a long wet season the beginning of which being in September. Rainfalls increase till December, then decrease from January until May. Then, a dry season occurs. Egg-laying and mating are observed at the end of wet season consequently to decreasing of rainfalls (Omar Kisserli PhD, 2010).

publications

KISSERLI, O., EXBRAYAT, J.-M., 2006- Premières données sur le cycle de reproduction des mâles de Bufo mauritanicus (Schlegel) dans la zone humide de Beni-Belaid (Jijel, Algérie). Bull. Soc. Herp. Fr. 120: 5-13.
KISSERLI, O., DOUMANDJI, S., EXBRAYAT, J.-M., 2011. Reproductive cycles in Bufo mauritanicus (Schlegel, 1841) of wet area of Beni-Belaïd (Jijel, Algeria), Basic and Applied Herpetology,25: 65-71.
KISSERLI, O., EXBRAYAT, J.-M. 2013. Histologie et immunohistochimie des organes de reproduction de Bufo mauritanicus Schlegel, 1841. Bull. Soc. Herp. Fr., 145-146: 101-112

4. Vertebrates from arid and semi-arid areas


The species living in arid and semi-arid regions are adapted to the climate at which they are submitted. These adaptations concern the regulation of hydro mineral balance. A work has been done in collaboration with USTHB, Algiers, Algeria, to study the repartition of neuro-secretory cells that are responsible to the elaboration of hormones implicated in this regulation.

Other adaptations concern the reproduction. Sexual cycles were studied in Uromastyx acanthinura (the dobb), an Agamid lizard, and in several mammal species living in the South-Algerian Sahara (station of Beni-Abbes).

These studies have been the subject of several collaborative programs between our university and the university Houari Boumediene of Algiers (USTHB). This collaboration is always effective.
The results of our studies have been the subject of several thesis, publications and colloquiums. In 2006, a publication untitled Mecanismes adaptatifs des petits vertébrés des zones arides et semi-arides (adaptive mechanisms in small Vertebrates living in arid and semi-arid areas) grouped a lot of communications and conferences about this work. Other results were presented at the Algero-French colloquium Biodiversité animale en zones arides et semi-arides: écophysiologie de la reproduction et métabolisme (Animal biodiversity in arid and semi-arid areas: ecophysiology of reproduction and metabolism)

publications

BARKA-DAHANE, Z., BENDJELLOUL, M., ESTABEL, J., EXBRAYAT, J.-M., 2010. The distribution of vasotocin and mesotocin immunoreactivity in the hypothalamic magnocellular neurosecretory nuclei of the Saharan herbivorous lizard, Uromastix acanthinurus Bell, 1825 (Sauria-Agamidae). Histol. Histopathol., 25 (2): 159-175
BELHOCINE, M., GERNIGON-SPYCHALOWICZ, T., JACOB, M.-P., BENAZZOUG, Y., EXBRAYAT, J.-M., 2010. Immunoexpression of gelatinase (MMP2 and MMP9) in the seminal vesicle and the ventral proste of Libyan jird (Meriones libycus) during seasonal cycle of reproduction Histol. Histopathol., 25 (5) : 619-636.
BENMANSOUR-HAMMOUCHE, S., REMANA, S., EXBRAYAT, J.-M., 2012. Immunolocalization of hepatic estrogen and progesterone receptors in the female lizard Uromastyx acanthinura. C.R. Biologies, 335: 445-453.
BOUBEKRI, A., GERNIGON-SPYCHALOWICZ, T., KHAMMAR, F., EXBRAYAT, J.-M. 2009. Morphometry and immunohistochemistry of follicles growth and steroidogenesis in saharian wild sand rat, Psammomys obesus ovary. Folia histochemica et cytobiologica, 47 (5): S59-S66
BOUBEKRI, A., GERNIGON, T., KHAMMAR, F., EXBRAYAT, J.-M., 2013. Variations saisonnières histo-physiologiques de l'oviducte du rat des sables Psammomys obesus, gerbillidé diurne. Bull. Soc. Zool. Fr., 138 (1-4): 27-35
BOUKENAOUI, N., MOUDILOU, E., CHEVALIER, C., AMIRAT, Z., EXBRAYAT, J.-M., KHAMMAR, F., 2012. Postnatal changes in testicular development and androgen receptors immunolocalization in D'Man ram lambs Folia Histochemica et Cytobiologica, 50 (1): 38-45.
HAMMOUCHE, S., GERNIGON, T., EXBRAYAT, J.-M., 2009. Correlation between ovarian steroidogeneisand -endorphin in the Lizard Uromastyx acanthinura: immunohistochemical approach. Folia histochemica et cytobiologica, 47 (5): S95-S100.
KACI-OUCHFOUN, N., IZEMRANE, D., BOUDRISSA, A., GERNIGON, T., KHAMMAR, F., EXBRAYAT, J.M. 2013. Transgelin an androgen-dependent protein identified in the seminal vesicles of three Saharan rodents. Theriogenology, 80: 748-757
MENAD, R., SMAI, S., MOUDILOU, E., KHAMMAR, F., EXBRAYAT , J.-M., GERNIGON-SPYCHALOWICZ, T., 2014. Immunolocalization of estrogen and androgen receptors in the caput epididymidis of the fat sand rat (Psammomys obesus): Effects of seasonal variations, castration and efferent duct ligation. Acta Histochem. 116:559-569
SMAÏ-HAMDIDOUCHE, S., GERNIGON-SPYCHALOWICZ, T., KHAMMAR, K., EXBRAYAT, J.-M., 2013. Ovarian function of the algerian wild Libyan jird, Meriones libycus during seasonal reproductive cycle: histological and immunohistochemical expression. Histol. Histopathol. 28: 101-114.

5. Ecotoxicology: the effects of molecules on integrate organisms.

Consequently to other thematic, the laboratory was recognized for histological methods and more especially for the detection of apoptosis on tissues. So, several collaborative works have been done. The laboratory participates to a study about the effects of nanoparticles (particle less than 100 nm diameter) on earthworms, considered such as bio-indicators. This work is done with the Oslo University and Bioforsk (Norway). The presence of nanoparticles in the external medium can provoke morphological variations and degenerations of organs in contact with these nanoparticles.

publications

LAPIED, E., MOUDILOU, E., NAHMANI, J. Y., EXBRAYAT, J.-M., 2008. Programmed cell death in earthworms during the first steps of tissue regeneration. 15th International colloqium on soil zoology, August 25-29, 2008, Curitiba, Parana, Brasil. Abstract
LAPIED, E. MOUDILOU, E., EXBRAYAT, J.-M., OUGHTON, D.E., JONER, J. E., 2010. Silver nanoparticle exposure causes apoptotic response in the earthworm Lumbricus terrestris (Oligochaeta). Nanomedicine. 5 (6): 975-984.
LAPIED, E., NAHMANI, J.Y., MOUDILOU, E., CHAURAND, P., LABILLE, J., ROSE, J., EXBRAYAT, J.-M., OUGHTON, D., JONER, E.J., 2011. Ecotoxicological effects of an aged TiO2 nanocomposite measured as apoptosis in the anecic earthworm Lumbricus terrestris after exposure through water, food and soil. Environment International, 37: 1105-110.

6. Embryonic development of rare species

For more than 30 years, the Caecilians (Gymnophiona) are the subject of a lot of studies of the laboratory. Gymnophionan amphibians are burrowing or secondarily aquatic species, living in tropical areas. These animals are difficult to capture and, consequently, their embryonic development is still little known and in only some species.

The first stages of development have been described in oviparous species Ichthyophis glutinosus, and Hypogeophis rostratus (Sarasin and Sarasin, 1887-1890; Brauer, 1897). More recently, the normal table of Ichthyophis glutinosus has been reviewed and completed by Breckenridge et al. (1979 till 1987). In 1990, our own laboratory published a normal table of development of Typhlonectes compressicauda with searchers of Paris National History Museum (Sammouri et al., 1990). In 2000, Dunker, Wake and Olson described the development of the oviparous Ichthyophis kohtaoensis.

In Ichthyophis kohtaoensis, the development occurs in an egg protected by the mother which is rolled around the egg clutch. The development is of telolecithal type, i. e., the yolk is concentrated to a pole of the egg and the development affects only the animal pole. It is a partial cleavage. The embryo develops from its yolk vesicle, triradiated gills develop and, after hatching, the aquatic larva slowly metamorphoses itself during several months before to attempt its definitive aspect. Similar observations have been done in Ichthyophis beddomei.

In the viviparous Typhlonectes compressicauda, the embryonic development is entirely accomplished in the uterine part of oviducts. During the first part of development, the embryo uses the yolk such as an energetic source. A lot of buds covering all the body and the presence of an ectotrophoblast, a thin ventral structure, are certainly implicated into the exchanges with the uterine fluid the injection of radio-active thymidine showed the existence of exchanges between the mother and the intrauterine embryos. After the intra uterine hatching, the embryos are equipped with a fetal dentition which persist to parturition. The embryos can eat the uterine secretions and also the epithelial cells of the uterus. Embryos also are adelphophageous, the most developed of them eating the smallest and dead ones. At the end of development, the gills are highly developed and transformed into two vesicular blades enveloping the animal, one gills being a coat, and the other a hook. The embryo seems to be enveloped in a cocoon. The external part of gills is narrowly applied against the connective tissue of uterine giving an exchange structure which can be compared to a meso-chorial placenta found in certain mammals. During the pregnancy, an immunity protection of embryos has been shown in females bearing embryos. Metamorphosis has also been described.

For several years, the development of several organs of this rare species has been published: skin, brain, gills, gut, hematopoietic organs, pituitary, thyroid, gonads and germ cells, kidneys (pronephroi and mesonephroi), lungs, interregnal glands. Anlagen of members have been found in Typhlonectes compressicauda; they regress at metamorphosis.

Several collaborative works permitted to study other species (Ichthyophis beddomei).

publications

ANJUBAULT, E., EXBRAYAT, J.-M., 2006.- Embryonic development of gonads and sexual maturity. In Exbrayat J;-M. (ed) Reproductive Biology and Phylogeny of Gymnophiona. Science Publishers Inc. 291-302.
BASTIT, M., EXBRAYAT, J.-M., 2011. Embryonic development of kidneys in viviparous Typhlonectes compressicauda (Amphibia, Gymnophiona); Basic and Applied Herpetology, 25: 33-42.
BRUN, C., EXBRAYAT, J.-M., 2006.- Description de l'œil au cours du développement embryonnaire de Typhlonectes compressicauda (Amphibien Gymnophione). Bull. Soc. Zool. Fr., 13 (4): 261-273.
EXBRAYAT, J.-M., 2006.- Modes of parity. In Exbrayat J;-M. (ed) Reproductive Biology and Phylogeny of Gymnophiona. Science Publishers Inc. 303-323.
EXBRAYAT, J.-M., 2006. Fertilization and development. In Exbrayat J;-M. (ed) Reproductive Biology and Phylogeny of Gymnophiona. Science Publishers Inc. 359-386.
EXBRAYAT, J.-M., HRAOUI-BLOQUET, S., 2006.- Viviparity in Typhlonectes compressicauda. In Exbrayat J;-M. (ed) Reproductive Biology and Phylogeny of Gymnophiona. Science Publishers Inc. 325-357.
RAQUET, M., EXBRAYAT, J.-M., 2007.- Embryonic development of the hypophysis and thyroid gland in Typhlonectes compressicauda (Dumeril and Bibron, 1841), Amphibia, Gymnophiona. J. Herp., 41 (4): 702-711.

7. Apoptosis and development


The apoptosis or programmed cell death (PCD) is a fundamental phenomenon implicated, as well as mitosis, in a harmonious embryonic development, in cell renewal, in growth of the organisms. A deficit in controlling apoptosis originates some teratologic features, cell deficiencies (Alzheimer's disease for instance), or still a cancer development.

Our laboratory is implicated in the study of the importance of apoptosis. For that, an important activity is devoted to the study of Xenopus laevis (the clawed toad) development and the results are shared with that of other teams working on cancer or neurodegenerative diseases.

This research axis started in 1996 and developed in 1999 consequently to a PPF (pluri formation program) proposed by E.P.H.E. The study focalized on the importance of glutamate receptors for embryonic development. Programmed cell death (PCD or apoptosis) was one of the main points examined. The animal models were anuran amphibians and especially Xenopus laevis. This work then continued with the study of relationships between these receptors and calpains. Calpains are proteins implicated in the regulation of cell death. This project implicated several research teams, more especially belonging to E.P.H.E.

1. Glutamate receptors were well studied in mammals and few works concerned lower vertebrates used such as model. The use of a dynamic technique helped us to show the glutamate ionotropic receptors are observed in earliest stages of development in Anuran. So, a mapping of neurons with glutamate receptors has been established for the first time in the brain of anuran amphibians. These observations suggested that AMPA/kainite receptors were implicated in the development of neuronal circuits in Amphibian.

2. Ontogenesis and morphogenesis are complex phenomena implicating several cell processes such as proliferation, differentiation, and cell death. PCD is one of these fundamental mechanisms. Anuran amphibians are particularly interesting models to study these physiological processes, for they are submitted to drastic modifications throughout the metamorphosis. In Xenopus laevis, PCD is observed from the earliest stages and it is maximal at hatching and metamorphosis. Ca++ is one of the factors modulating this kind of cell death. Its cytoplasm concentration can be modified by glutamate ionotropic receptors (AMPA/kainate receptors), lipases, endonucleases, and apoptosis can or cannot be set off.

Mapping of physiological apoptosis in the main organs has been done on several development stages of Xenopus tadpoles. From tail bud to metamorphosis, the number of apoptotic cells is highly variable according to both the stage of development and the organ. At metamorphosis, PCD is particularly observed in tail components such as muscles, skin and spinal cord.

Studies based upon immunohistochemical detection showed that glutamate ionotropic receptors (AMPA/kainate) were present and functional in several organs just after the hatching. In growing tadpoles, the consequences of exposition to an agonist (glutamate or kainite) and/or an antagonist (NBQX) of AMPA/kainate receptors were super activation or blocking of these receptors and action on brain development. So, these glutamate receptors were implicated in both synaptic transmission, and regulation of ionic homeostasis (Jeanne Estabel PhD, 2004).

Then apoptosis obtained after treatments were quantified and mapped. The immunoreactivities of different calpains have been observed using immunoflorescence technique. Calpains varied inversely to apoptosis. No evidence for direct correlation between PCD and action of calpains were shown (Nassima Mouterfi Diploma EPHE, 2008; Elara Moudilou PhD, 2012).

3. Relationships between PCD, cytoskeleton, have been studied in Xenopus laevis. The main ubiquitary calpain have been found in Xenopus whatever the development stage, and also in the adult. The highest level has been observed between neurula stage and metamorphosis, showing an important role of calpains in organogenesis and metamorphosis (Moudilou et al., 2010). A synthesis of the importance of apoptosis in embryonic development in amphibians has been published (Exbrayat et al., 2012).

A deepest study has been done. The study of the expression territories during embryonic development has been surveyed. qPCR analysis and western blotting allowed us to quantify the expression of main calpains. This wide study exceeds now he embryonic aspect to attempt the study of cell plasticity of organs of animals submitted to variable natural or artificial external conditions

publications

ABROUK-VEROT, L., BRUN, C., EXBRAYAT, J.- M., 2013. Expression patterns of CAPN1 and CAPN8b genes during embryogenesis in Xenopus laevis. CellBio, 2013 (2): 211-216
BRUN, C., MOUDILOU, E., BOUCHOT, C., ABROUK-VEROT, L., EXBRAYAT, J.-M. 2014. Relationships between calpains and glutamate- or kainate-induced apoptosis in Xenopus laevis tadpoles. Folia Histoch. Cytobiol., 51 (4): 300-311
EXBRAYAT, J.-M., MOUDILOU, E. N., ABROUK, L., BRUN, C., 2012. Apoptosis in amphibian development. Advances in Bioscience and Biotechnology, 2012, 3: 669-678
MOUTERFI, N., 2008. Répercussions de traitements pharmacologiques par des agonistes et un antagoniste des récepteurs ionotropes du glutamate sur l'apoptose et sur l'expression des calpaïnes chez Xenopus laevis. Diplôme EPHE, Lyon.
Moudilou, E.N., Mouterfi, N., Exbrayat, J.-M., Brun, C., 2010. Calpains expression during Xenopus laevis development. Tissue Cell. 42: 275-281.
Moudilou, E., 2012. Rôle des calpaïnes au cours du développement de Xenopus laevis et interactions possibles avec les récepteurs ionotropes du glutamate. Thèse Doct. Univ. Lyon 1.
Moudilou, E., Mouterfi, N., Verot-Abrouk, L., Exbrayat, J.-M., Brun, C., 2009. Expression des calpaïnes au cours du développement de Xenopus laevis. Club Amphibien 2009, Rennes, 6-8 juillet 2009. Résumés