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PubMed2005

Laminin alpha5 is required for dental epithelium growth and polarity and the development of tooth bud and shape.

In tooth development, the oral ectoderm and mesenchyme coordinately and reciprocally interact through the basement membrane for their growth and differentiation to form the proper shape and size of the tooth. Laminin alpha5 subunit-containing laminin-10/11 (LM-511/521) is the major laminin in the tooth germ basement membrane. Here, we have examined the role of laminin alpha5 (Lama5) in tooth development using laminin alpha5-null mouse primary dental epithelium and tooth germ organ cultures. Lama5-null mice develop a small tooth germ with defective cusp formation and have reduced proliferation of dental epithelium. Also, cell polarity and formation of the monolayer of the inner dental epithelium are disturbed. The enamel knot, a signaling center for tooth germ development, is defective, and there is a significant reduction of Shh and Fgf4 expression in the dental epithelium. In the absence of laminin alpha5, the basement membrane in the inner dental epithelium becomes discontinuous. In normal mice, integrin alpha6beta4, a receptor for laminin alpha5, is strongly localized at the basal layer of the epithelium, whereas in mutant mice, integrin alpha6beta4 is expressed around the cell surface. In primary dental epithelium culture, laminin-10/11 promotes cell growth, spreading, and filopodia-like microspike formation. This promotion is inhibited by anti-integrin alpha6 and beta4 antibodies and by phosphatidylinositol 3-kinase inhibitors and dominant negative Rho-GTPase family proteins Cdc42 and Rac. In organ culture, anti-integrin alpha6 antibody and wortmannin reduce tooth germ size and shape. Our studies demonstrate that laminin alpha5 is required for the proliferation and polarity of basal epithelial cells and suggest that the interaction between laminin-10/11-integrin alpha6beta4 and the phosphatidylinositol 3-kinase-Cdc42/Rac pathways play an important role in determining the size and shape of tooth germ.

Animals↗

PubMed2006

The molecular basis of neurosensory cell formation in ear development: a blueprint for hair cell and sensory neuron regeneration?

The inner ear of mammals uses neurosensory cells derived from the embryonic ear for mechanoelectric transduction of vestibular and auditory stimuli (the hair cells) and conducts this information to the brain via sensory neurons. As with most other neurons of mammals, lost hair cells and sensory neurons are not spontaneously replaced and result instead in age-dependent progressive hearing loss. We review the molecular basis of neurosensory development in the mouse ear to provide a blueprint for possible enhancement of therapeutically useful transformation of stem cells into lost neurosensory cells. We identify several readily available adult sources of stem cells that express, like the ectoderm-derived ear, genes known to be essential for ear development. Use of these stem cells combined with molecular insights into neurosensory cell specification and proliferation regulation of the ear, might allow for neurosensory regeneration of mammalian ears in the near future.

Animals↗

PubMed1996

Unusual aspects of inner cell mass formation, endoderm differentiation, Reichert's membrane development, and amniogenesis in the lesser bulldog bat, Noctilio albiventris.

BACKGROUND AND METHODS: The early embryogenesis of the lesser bulldog bat, Noctilio albiventris (family Noctilionidae), was examined histologically in 59 pregnant females collected from a reproductively synchronized population in Colombia. RESULTS: Early blastocysts of Noctilio are unusual in lacking a typical inner cell mass. Instead, cells inside of the trophoblast are dispersed for a period as a monolayer. A typical inner cell mass (ICM) only forms and becomes properly oriented after the initiation of implantation. Several features of Reichert's membrane in this species are also noteworthy: it develops between the ICM and trophoblast and between the parietal endoderm and trophoblast; it becomes linked to a meshwork of basal laminalike material that extends into the ICM; and it appears to be continuous, or fused, with prominent basal laminae that develop within the cytotrophoblastic villi that radiate throughout the preplacenta. Amniogenesis occurs by cavitation and converts the ICM into a hollow epiblastic vesicle. Gastrulation commences before this vesicle exhibits obvious differentiation into an embryonic shield and amniotic ectoderm. CONCLUSIONS: Because development and proper orientation of a typical ICM in Noctilio occur after the initiation of implantation, these may involve the migration of cells on the interior of the blastocyst and/or an unusual method of early endoderm differentiation. The possibility exists that epiblast, endoderm, and cytotrophoblast may all contribute to the secretion of Reichert's membrane in this bat. Although the early embryogenesis of Noctilio exhibits many similarities to that in phyllostomid bats, substantial differences also exist between these closely related species.

Amnion↗

PubMed2003

Morphological assessment of preimplantation embryo quality in cattle.

The extensive use of embryo technologies has emphasized the need for assessing embryo quality by morphological techniques, such as transmission electron microscopy, immunocytochemistry for confocal laser scanning microscopy and fluorescence in situ hybridization. By a combination of these techniques, it has been possible to demonstrate: (i) that rRNA gene activation, as monitored by embryonic nucleolar development, is comparable in bovine embryos developed in vivo and produced in vitro, whereas reconstructed nuclear transfer embryos may be deviant, (ii) that generating embryos by both in vitro production and reconstruction by nuclear transfer is associated with increased occurrence of apoptosis, in particular in the inner cell mass of blastocysts, and (iii) that these two embryo production techniques are associated with increased occurrence of mixoploidy that is, embryos presenting a large population of normal diploid cells and a small population of abnormal haploid or polyploid cells. It is clear that blastocysts that appear healthy at stereomicroscopy may have subcellular defects. Therefore, the possibility of long-term evaluation in vitro of embryos after hatching has been examined. However, whereas embryos developing in vivo after hatching present a number of well defined developmental milestones, such as elongation of the trophoblast, formation of hypoblast and epiblast followed by differentiation of endoderm, mesoderm and ectoderm, in vitro culture systems for development beyond the blastocyst stage currently allow the embryo to complete only a single milestone, namely hypoblast formation.

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PubMed2006

Characterization and in vitro differentiation potential of a new human embryonic stem cell line, ReliCellhES1.

Human embryonic stem cells (hESCs) are an exceptionally useful tool for studies of human development and represent a potential source for transplantation therapies. At present, only a limited number of hESCs lines representing a very small sample of genetic diversity of the human populations are available. Here, we report the derivation and characterization of a new hESC line, ReliCellhES1. These cells, established from the inner cell mass (ICM) on mouse embryonic feeder (MEF) layer, satisfy the criteria that characterize pluripotent hESCs: The cell line expresses high levels of cell surface markers (such as SSEA-3, SSAEA-4, TRA-1-60 and TRA-1-81), transcription factor Oct-4, alkaline phosphatase (AP) and telomerase. The cell line retains normal karyotype in long-term culture and has a distinct identity as revealed by DNA fingerprinting by short tandem repeat (STR) analysis. Further, upon examination of the in vitro differentiation potential, ReliCellhES1 was found to be capable of giving rise to dopaminergic neurons, cardiomyocytes, pancreatic islets, and hepatocyte-like cells belonging to ectoderm, mesoderm, and endoderm lineages, respectively. To our knowledge, this is the first report of a well-characterized hES cell line from the Indian subcontinent.

Animals↗

PubMed1992

Tropic effects of otic epithelium on cochleo-vestibular ganglion fiber growth in vitro.

Sensory nerve fibers of the cochleo-vestibular ganglion (CVG) innervate the otic epithelium in the early chick embryo by directed growth. To see if the target tissue could exert a tropic influence, we co-cultured CVGs from chick embryos (Hamburger-Hamilton stages 16-30) in a 3D collagen matrix with their normal target epithelium or with other epithelial tissues taken from the same or different stages of development. The pattern of neurite outgrowth and the viability of the CVG after five days in vitro were assessed histologically with a silver method. On the basis of the patterns of neurite outgrowth directed toward the epithelium, the cultures were classified as having slightly, mostly, exclusively, or no directed outgrowth. Of 49 cultures containing otic epithelium, 33 had mostly or exclusively directed growth patterns. This effect did not depend on any particular stage difference between co-cultures or on their viability in vitro. Cultures of non-sensory otic epithelium (endolymphatic duct) also presented directed growth patterns. Co-cultures with ectoderm from forelimb or visceral arch had little, if any, directed growth. The directed growth could not be explained simply as a result of guidance by non-neuronal cells or of the viability of the explants. The results are consistent with the hypothesis that the otic epithelium provides a tropic factor that attracts growing CVG fibers.

Animals↗

PubMed1989

Chimeras between parthenogenetic or androgenetic blastomeres and normal embryos: allocation to the inner cell mass and trophectoderm.

A series of chimeras was generated by injecting single normal, parthenogenetic, or androgenetic blastomeres carrying transgenic markers under the zona pellucida of nontransgenic eight-cell embryos. These chimeras were cultured to the blastocyst stage and sectioned, and the transgenic component was detected by in situ hybridization. No statistically significant difference was found among the normal, parthenogenetic, and androgenetic chimeras in the number of chimeric blastocysts with a transgenic contribution to the inner cell mass (ICM), the trophectoderm, or both the ICM and trophectoderm. Since androgenetic and parthenogenetic cells were present in chimeras at a high frequency in both the ICM and trophectoderm at the blastocyst stage, but not in similar chimeras at late gastrulation, these cells must not respond normally to developmental signals subsequent to blastocyst formation and prior to late gastrulation.

Animals↗

PubMed1990

Nude mice are not hairless. A morphological study.

In the present study, the morphological aspect of the skin and the hairs of athymic, macroscopically nude mice (NMRI, nu/nu) was investigated by descriptive light- and electron-microscopical methods and compared with the appearance of the skin and the hairs in normally haired mice (NMRI). These morphological studies revealed that athymic, macroscopically nude mice are not at all hairless, but have about the same number of hair bulbs, embedded in the hypodermis, as normally haired animals. However, within the hair follicles of athymic mice, the keratinization processes are obviously deeply impaired, resulting in the formation of short, crippled and bent hair shafts which only seldom emerge from the hair follicles. The cuticles of the inner root sheath and the hair are not built up, the cortex of the hair being composed by abnormal globular aggregates. The epidermis shows similar disturbances of keratinization, which are reflected by the presence of only few and thin bundles of tonofilaments in the basal, spinous and granular layers of the epidermis and, in the stratum corneum, by bizarrely formed and irregularly arranged lamellae of corneocytes, separated from one another. These results demonstrate that athymic, nude mice are not hairless but that the development and differentiation of hairs are severely injured in this mouse mutant. Analogously, the keratinization of the epidermis is also impaired. In view of the previously shown ectodermal defect as primary cause for the dysgenesis of the thymus, it seems to be probable that defects of the ectoderm are actually the common reason for both the thymus dysgenesis and the severe disturbances of hair development in 'athymic, nude' mice.

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PubMed2006

Spectrum of nonterminal myelocystoceles.

OBJECTIVE: To present the magnetic resonance imaging features, clinical findings, and possible embryologic bases for nonterminal myelocystoceles, a distinct subset of closed spinal dysraphisms. METHODS: We retrospectively analyzed imaging series and clinical records from five newborns and one older child with skin-covered soft tissue masses along the posterior midline spine. Spinal (6 patients) and brain (5 patients) magnetic resonance imaging was performed before surgical repair and compared with clinical findings, observations at surgery, and final lesion histology. RESULTS: The lesions affected the cervical (n = 3), thoracic (n = 2), and lumbar (n = 1) regions. In each case, the dome of the mass was covered by thickened, dystrophic epithelium with no subcutaneous fat, whereas the base and lateral walls of the mass were covered by normal skin. All patients were neurologically intact at presentation. In three cases, a stalk emanated from the dorsal normal spinal cord, crossed a narrow posterior bony spina bifida, and coursed through a posterior meningocele to attach to the inner aspect of its dome. The other three cases showed dissection of a hydromyelic cavity into the stalk, converting it into a second "cyst" within the meningocele. Concurrent anomalies included focal hydromyelia immediately cranial to the origin of the posterior stalk (n = 2), mild Chiari II malformation (n = 3), triventricular hydrocephalus from aqueductal stenosis (n = 1), filar lipoma (n = 1), and presumed neurenteric cyst (n = 1). At surgery, the sac was resected in all cases, but intradural exploration and untethering was performed in only three children. Embryologic considerations indicate that the spectrum of these lesions likely arises from partial limited closure of the neural tube, failed disjunction of the cutaneous ectoderm, and variable degrees of hydromyelia. CONCLUSION: The nonterminal myelocystocele is a distinct form of closed spinal dysraphism characterized by a skin-covered meningocele, which is either crossed by a fibroneurovascular stalk that extends from the dorsal aspect of the spinal cord to attach to the dome of the meningocele (abortive form, or myelocystocele manqué) or contains a hydromyelic cavity that is continuous with the ependymal canal of the spinal cord (complete form).

Abnormalities, Multiple↗

PubMed1998

Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4.

Oct4 is a mammalian POU transcription factor expressed by early embryo cells and germ cells. We report that the activity of Oct4 is essential for the identity of the pluripotential founder cell population in the mammalian embryo. Oct4-deficient embryos develop to the blastocyst stage, but the inner cell mass cells are not pluripotent. Instead, they are restricted to differentiation along the extraembryonic trophoblast lineage. Furthermore, in the absence of a true inner cell mass, trophoblast proliferation is not maintained in Oct4-/- embryos. Expansion of trophoblast precursors is restored, however, by an Oct4 target gene product, fibroblast growth factor-4. Therefore, Oct4 also determines paracrine growth factor signaling from stem cells to the trophectoderm.

Animals↗

PubMed2006

The CryoLoop facilitates re-vitrification of embryos at four successive stages of development without impairing embryo growth.

BACKGROUND: Vitrification has been shown to be an effective method of cryopreservation, but little is known about re-vitrification of embryos. This study investigated the effect of re-vitrification on mouse embryo preimplantation development and viability post-transfer. METHODS: Mouse embryos at the 1-cell stage were vitrified using the CryoLoop technique. Embryos were warmed and then re-vitrified successively at the 2-, 8-cell and blastocyst stages. The effects of multiple rounds of vitrification on development, differentiation and viability were assessed and compared with non-vitrified embryos. RESULTS: Development to the 8-cell stage on day 3 and blastocyst on day 5 were not affected by re-vitrification. However, better hatching rates were observed in the non-vitrified control group. Total cell number and the number of cells allocated to the inner cell mass (ICM) were not different between treatments. The percentage of ICM development was also not different between treatments. Implantation rate and fetal weights were the same between treatments. However, overall there were fewer fetuses per embryo transferred in the re-vitrified group. CONCLUSION: Re-vitrification of mouse embryos has minimal effect on preimplantation embryo development or implantation potential.

Animals↗

PubMed1998

Fibroblast growth factor receptor 2 (FGFR2)-mediated reciprocal regulation loop between FGF8 and FGF10 is essential for limb induction.

FGFR2 is a membrane-spanning tyrosine kinase that serves as a high affinity receptor for several members of the fibroblast growth factor (FGF) family. To explore functions of FGF/FGFR2 signals in development, we have mutated FGFR2 by deleting the entire immunoglobin-like domain III of the receptor. We showed that murine FGFR2 is essential for chorioallantoic fusion and placenta trophoblast cell proliferation. Fgfr2(DeltaIgIII/DeltaIgIII) embryos displayed two distinct defects that resulted in failures in formation of a functional placenta. About one third of the mutants failed to form the chorioallantoic fusion junction and the remaining mutants did not have the labyrinthine portion of the placenta. Consequently, all mutants died at 10-11 days of gestation. Interestingly, Fgfr2(DeltaIgIII/DeltaIgIII) embryos do not form limb buds. Consistent with this defect, the expression of Fgf8, an apical ectodermal factor, is absent in the mutant presumptive limb ectoderm, and the expression of Fgf10, a mesenchymally expressed limb bud initiator, is down regulated in the underlying mesoderm. These findings provide direct genetic evidence that FGF/FGFR2 signals are absolutely required for vertebrate limb induction and that an FGFR2 signal is essential for the reciprocal regulation loop between FGF8 and FGF10 during limb induction.

Animals↗

PubMed2006

Confinement and clearance of OCT4 in the porcine embryo at stereomicroscopically defined stages around gastrulation.

In the areas of developmental biology and embryonic stem cell research, reliable molecular markers of pluripotency and early lineage commitment are sparse in large animal species. In this study, we present morphological and immunohistochemical findings on the porcine embryo in the period around gastrulation, days 8-17 postinsemination, introducing a stereomicroscopical staging system in this species. In embryos at the expanding hatched blastocyst stage, OCT4 is confined to the inner cell mass. Following detachment of the hypoblast, and formation of the embryonic disk, this marker of pluripotency was selectively observed in the epiblast. A prominent crescent-shaped thickening at the posterior region of the embryonic disk marked the first polarization within this structure reflecting incipient cell ingression. Following differentiation of the epiblast, clearance of OCT4 from the three germ layers was observed at defined stages, suggesting correlations to lineage specification. In the endoderm, clearance of OCT4 was apparent from early during its formation at the primitive streak stage. The endoderm harbored progenitors of the "fourth germ layer," the primordial germ cells (PGCs), the only cells maintaining expression of OCT4 at the end of gastrulation. In the ectodermal and mesodermal cell lineages, OCT4 became undetectable at the neural groove and somite stage, respectively. As in the mouse, PGCs showed onset of c-kit expression when located in extraembryonal compartments. They appeared to follow the endoderm during extraembryonal allocation and the mesoderm on return to the genital ridge.

Animals↗

PubMed2001

Formation of the middle ear: recent progress on the developmental and molecular mechanisms.

The middle ear allows animals to hear while moving in an aerial medium. It is composed of a cavity harbouring a chain of three ossicles that transmit vibrations produced by airborne sound in the tympanic membrane into the inner ear, where they are converted into neural impulses. The middle ear develops in the branchial arches, and this requires sequential interactions between the epithelia and the underlying mesenchyme. Gene-inactivation experiments have identified genes required for the formation of different middle ear components. Some encode for signalling molecules, including Endothelin1 and Fgf8, probable mediators of epithelial-mesenchymal interactions. Other genes, including Eya1, Prx1, Hoxa1, Hoxa2, Dlx1, Dlx2, Dlx5, and Gsc, are most likely involved in patterning and morphogenetic processes in the neural crest-derived mesenchyme. Mechanisms controlling formation of a functional tympanic membrane are also discussed. Basically, the tympanic ring, which serves as support for the tympanic membrane, directs invagination of the first pharyngeal cleft ectoderm to form the external acoustic meatus (EAM), which provides the outer layer of the membrane. Gsc and Prx1 are essential for tympanic ring development. While invaginating, the EAM controls skeletogenesis in the underlying mesenchyme to form the manubrium of the malleus, the link between the membrane and the middle ear ossicles.

Animals↗

PubMed1978

Expression of a high molecular weight cell surface glycoprotein (LETS protein) by preimplantation mouse embryos and teratocarcinoma stem cells.

The expression of a high molecular weight cell surface glycoprotein (LETS, fibronectin) by preimplantation mouse embryos as well as cultured teratocarcinoma stem cells was detected by using indirect immunofluorescent staining. When each stage of preimplantation embryonic development was tested for the presence of LETS protein, none was observed on two-cell, four-cell, or eight-cell embryos, or on the morula or the outer cell layer (trophectoderm) of the early or late blastocyst. However, when the inner cell mass was isolated by immunosurgery, positive staining was observed. The intensity of the staining was significantly greater on the inner cell mass isolated from the expanded (day 4) blastocyst than on that from the early (day 3) blastocyst. Certain established cell lines of teratocarcinoma stem cells (embryonal carcinoma cells) also express cell surface LETS protein. "Nullipotent" (Nulli-SCC-1) as well as pluripotent (PSA 1) embryonal carcinoma cell lines have deposits of LETS protein concentrated in areas of cell-cell contact. In addition, a teratocarcinoma-derived endodermal cell line (PYS) was found to be capable of depositing LETS onto the substratum in a fibrillar network.Taken together, our results indicate that LETS protein is synthesized at a specific stage of preimplantation mouse embryonic development. In particular, they suggest that LETS protein is a product of the embryonic ectoderm, and that some types of embryonic endoderm are also capable of synthesizing this protein.

Animals↗

PubMed2002

The urethral plate--does it grow into the genital tubercle or within it?

OBJECTIVE: To determine whether the urethral plate grows into the genital tubercle or develops within it. MATERIALS AND METHODS: Sprague-Dawley rat embryos were examined at 11-21 days of gestation and compared with available human embryo sections. Rat embryos were examined by a combination of light microscopy, dissection, serial histological section and immunohistochemistry. RESULTS: In rat embryos the urethral plate extended to the tip of the genital tubercle from the earliest stages of genital tubercle development. The plate formed from adherence in the sagittal plane of the inner walls of the primitive cloacal cavity. The urethral plate continued to extend to the tip of the genital tubercle throughout penile development in the male and developed a lumen ahead of the advancing perineal mesenchyme. In the female the perineal side of the urethral plate disintegrated by massive apoptosis. This loss of perineal substance allowed the genital tubercle to collapse on itself and left the urogenital opening at the base of the genital tubercle. Human embryos also showed the presence of the urethral plate at the tip of the genital tubercle throughout genital tubercle development. CONCLUSION: The urethral plate forms ab initio within the genital tubercle and extends to the tip; it does not grow into the genital tubercle as is often described. The contribution of ectodermal ingrowth to urethral development at the tip of the penis is minimal.

Animals↗

PubMed1989

Nuclear lamin antigens are developmentally regulated during porcine and bovine embryogenesis.

The nuclear lamins, proteins that reside on the inner face of the nuclear envelope, are thought to provide attachment sites for anchoring the chromatin to the nuclear envelope, thus facilitating the overall organization of the nucleus. The composition of the nuclear lamin proteins changes during differentiation and development in a variety of mammalian and nonmammalian tissues. Bovine and porcine oocytes and early embryos were prepared for immunocytochemical detection of nuclear lamins using three different antibodies (recognizing lamin B, lamins A/B/C, or lamins A/C). In both species, germinal vesicle nuclei and early cleavage stage nuclei react positively with the antibodies. However, on nuclei of bovine embryos, the A/C epitope was not detectable at the 16-cell stage, compact morula, spherical blastocyst, or the chorionic cell nuclei of a Day 35 conceptus, but was detectable on both amniotic and embryonic ectodermal cell nuclei of a Day 35 conceptus. All three antibodies reacted with nuclei from two bovine tissue culture cell lines (bovine embryonic cells and Madin-Darby bovine kidney cells) and one porcine kidney cell line. Nuclei in porcine embryos followed a similar pattern, except the loss of the A/C epitope occurred at the 8-cell stage and the epitope was absent from compact morula and spherical blastocyst stage nuclei. All interphase nuclei in both species reacted with both anti-lamin A/B/C and anti-lamin B antibodies, whereas metaphase chromosomes did not react with any of the lamin antibodies tested. The change in recognizing the lamin epitope occurred one cell cycle after the expected transition from maternal control to zygotic control of development. Nuclear transplantation showed that 16-cell stage porcine nuclei, which are lamin A/C negative, acquired the A/C epitope after transfer to an enucleated metaphase II oocyte. These results suggest that the A/C epitope is developmentally regulated.

Animals↗

PubMed1999

Programmed cell death and the morphogenesis of the hindbrain roof plate in the chick embryo.

The spatial and temporal distribution of apoptosis in the dorsal midline of the developing chick hindbrain was examined in relation to the development of the neuroepithelium and neural crest using scanning and transmission electron microscopy, immunocytochemistry and in situ hybridization. The pattern of TUNEL labeling and Slug expression in the dorsal midline at stages 10 and 11 differed from that at stages 12-15. At stages 10 and 11, TUNEL labeling and Slug expression were observed in the dorsal part of location II of rhombomere 1/2 (i.e., between the surface ectoderm and the neuroepithelium), but from stage 12 onward, they were observed in both the dorsal and ventral parts of location II. The implication is that whereas apoptosis may be restricted to a subpopulation of the early migrating neural crest at stages 10 and 11, it presumably occurs in subpopulations of both neural crest and neuroepithelial cells from stage 12 onward. Furthermore, as judged by the pattern of TUNEL labeling and Slug expression in r3 and r5, apoptosis in these two rhombomeres likely occurs in subpopulations of both neural crest and neuroepithelial cells. The eminence present in location I of r1/r2 between stages 10 and 12 consisted of both neural crest and neuroepithelial cells. These cells gradually underwent apoptosis until stage 12, when the eminence disappeared in most embryos. The formation of the inner (neuroepithelial) aspect of the hindbrain roof plate involved both cell migration from adjacent neuroepithelium and an alteration in the shapes of the cells, such that cells with flattened surfaces eventually lined the roof plate. During these processes, some of the neuroepithelial cells underwent apoptosis (i.e., in location IV). The results of this study thus demonstrate that subpopulations of both neuroepithelial and neural crest cells may be involved in programmed cell death in the hindbrain. Additionally, apoptosis in the hindbrain contributes significantly to morphogenetic thinning during roof plate formation.

Animals↗