A pituitary-salivary mixed gland induced by tissue recombination of embryonic pituitary epithelium and embryonic submandibular gland mesenchyme in mice

doi:10.1016/0012-1606(85)90097-1

Developmental Biology

Volume 110, Issue 2, August 1985, Pages 382-391

https://doi.org/10.1016/0012-1606(85)90097-1 Get rights and content

Abstract

Renal subcapsular syngrafts of Day 9 to 11 mouse embryonic pituitary epithelium with Day 14 mouse embryonic submandibular gland mesenchyme produced mixed organs that include residual cleft structure surrounded by anterior pituitary cells some which are stained by anti-ACTH antiserum and submandibular gland-like structure with differentiated acinar cells which are stained by anti-α-amylase antiserum. However, when Day 8.5 or 12 embryonic pituitary epithelium was recombined with submandibular gland mesenchyme and syngrafted, development of submandibular gland-like or anterior pituitary tissues resulted, respectively. Thus, during organogenesis of the mouse anterior pituitary, there exists a developmental stage (Day 8.5–11 in utero), when prospective pituitary epithelium can respond to heterotypic submandibular gland mesenchyme with the development of a submandibular gland-like tissue.

References (15)

D. Dhouailly et al.
The specification of feather and scale protein synthesis in epidermal-dermal recombinations
Dev. Biol
(1978)
L. Frati et al.
Purification of α-amylase from C₃H mouse submaxillary gland by gel filtration
J. Chromatogr
(1970)
P. Sengel
Study of organogenesis by dissociation and reassociation of embryonic rudiments in vitro
G.R. Cunha
Stromal induction and specification of morphogenesis and cytodifferentiation of the epithelia of the Müllerian ducts and urogenital sinus during development of the uterus and vagina in mice
J. Exp. Zool
(1976)
G.R. Cunha et al.
Epithelial-mesenchymal interactions in prostatic development. I. Morphological observations of prostatic inductions by urogenital sinus mesenchyme in epithelium of the adult rodent urinary bladder
J. Cell. Biol
(1983)
R. Fleischmajer et al.
Epithelial-Mesenchyme Interactions
(1968)
J. Gearhart et al.
An immunofluorescence procedure for the tissue localization of glucosephosphate isomerase
J. Histochem. Cytochem
(1980)

There are more references available in the full text version of this article.

Cited by (42)

Induced pluripotent stem cell-derived salivary glands
2021, iPSCs in Tissue Engineering
Salivary glands are exocrine glands composed of several cell types including ductal, acinar, and basal/myoepithelial cells. Salivary glands, through the production of saliva, play essential roles in the maintenance of proper oral health such as the digestion of starch, swallowing, and the maintenance of teeth. Pluripotent stem cell–derived organoids are three-dimensional self-organizing structures that have recently emerged as a novel model system for investigating embryonic development and disease progression. Organoids serve as a valuable tool in developmental and physiological research, disease modeling, drug screening, and potential cell-based therapies. Organoids can be grown in vitro from pluripotent stem cells by the stepwise manipulation of molecular signals that mimic the signaling cues present during in vivo organ development. Recently, we reported the generation of salivary gland organoids using mouse embryonic stem cells. The salivary gland organoid showed a similar morphology and gene expression profile to the embryonic salivary gland. Moreover, orthotopically engrafted salivary gland organoids exhibited characteristics of mature salivary glands, including saliva secretion. The culture methods used, as well as transplant model, are therefore expected to be a promising model for the understanding of salivary gland development and diseases.
Exosomal MicroRNA Transport from Salivary Mesenchyme Regulates Epithelial Progenitor Expansion during Organogenesis
2017, Developmental Cell
Citation Excerpt :
The mesenchyme and epithelium can be separated, cell membranes fluorescently labeled, and the tissue recombined in ex vivo culture to study, for example, exosomal transport during SMG organogenesis. Classic mesenchyme/epithelium recombination experiments using different organs showed that the mesenchyme is inductive to the epithelium, inducing cell proliferation, differentiation, and ultimately its morphogenesis (Kusakabe et al., 1985; Sakakura et al., 1976; Grobstein, 1953a, 1953b). These mobile inductive signals from the mesenchyme have been mainly attributed to secreted signals, such as growth factors and extracellular matrix.
Epithelial-mesenchymal interactions involve fundamental communication between tissues during organogenesis and are primarily regulated by growth factors and extracellular matrix. It is unclear whether RNA-containing exosomes are mobile genetic signals regulating epithelial-mesenchymal interactions. Here we identify that exosomes loaded with mesenchyme-specific mature microRNA contribute mobile genetic signals from mesenchyme to epithelium. The mature mesenchymal miR-133b-3p, loaded into exosomes, was transported from mesenchyme to the salivary epithelium, which did not express primary miR-133b-3p. Knockdown of miR-133b-3p in culture decreased endbud morphogenesis, reduced proliferation of epithelial KIT⁺ progenitors, and increased expression of a target gene, Disco-interacting protein 2 homolog B (Dip2b). DIP2B, which is involved in DNA methylation, was localized with 5-methylcytosine in the prophase nucleus of a subset of KIT⁺ progenitors during mitosis. In summary, exosomal transport of miR-133b-3p from mesenchyme to epithelium decreases DIP2B, which may function as an epigenetic regulator of genes responsible for KIT⁺ progenitor expansion during organogenesis.
Retinoic acid regulates embryonic development of mammalian submandibular salivary glands
2015, Developmental Biology
Citation Excerpt :
Despite the developmental importance of this early event, no other molecule has been identified that marks or overlaps with the future SMG domain at this early stage. Development of SMG involves dynamic interactions between epithelium and mesenchyme (Kratochwil, 1969; Kusakabe et al., 1985; Tucker, 2007; Wells et al., 2013). Our observation that the E12.5 SMG mesenchyme expresses Rdh10, while SMG epithelium at that stage experiences active RA signaling (Fig. 5A and B) suggests that diffusion of the metabolic product RA or the intermediate atRAL away from the site of synthesis in the mesenchyme into the adjacent epithelium may be one means of interaction between these two tissue types.
Organogenesis is orchestrated by cell and tissue interactions mediated by molecular signals. Identification of relevant signals, and the tissues that generate and receive them, are important goals of developmental research. Here, we demonstrate that Retinoic Acid (RA) is a critical signaling molecule important for morphogenesis of mammalian submandibular salivary glands (SMG). By examining late stage RA deficient embryos of Rdh10 mutant mice we show that SMG development requires RA in a dose-dependent manner. Additionally, we find that active RA signaling occurs in SMG tissues, arising earlier than any other known marker of SMG development and persisting throughout gland morphogenesis. At the initial bud stage of development, we find RA production occurs in SMG mesenchyme, while RA signaling occurs in epithelium. We also demonstrate active RA signaling occurs in glands cultured ex vivo, and treatment with an inhibitor of RA signaling blocks growth and branching. Together these data identify RA signaling as a direct regulator of SMG organogenesis.
Submandibular gland epithelial development and the importance of junctions
2023, Tissue Barriers
Single-cell RNA sequencing reveals PDFGRα<sup>+</sup> stromal cell subpopulations that promote proacinar cell differentiation in embryonic salivary gland organoids
2022, Development (Cambridge)
Salivary gland tissues and derived primary and metastatic neoplasms: unusual pitfalls in the work-up of sellar lesions. A systematic review
2021, Journal of Endocrinological Investigation

View all citing articles on Scopus

^☆: This research was supported by Grants from the Ministry of Education, Science and Culture of Japan.

View full text

Article preview

Developmental Biology

Abstract

References (15)

The specification of feather and scale protein synthesis in epidermal-dermal recombinations

Dev. Biol

Purification of α-amylase from C₃H mouse submaxillary gland by gel filtration

J. Chromatogr

Study of organogenesis by dissociation and reassociation of embryonic rudiments in vitro

Stromal induction and specification of morphogenesis and cytodifferentiation of the epithelia of the Müllerian ducts and urogenital sinus during development of the uterus and vagina in mice

J. Exp. Zool

Epithelial-mesenchymal interactions in prostatic development. I. Morphological observations of prostatic inductions by urogenital sinus mesenchyme in epithelium of the adult rodent urinary bladder

J. Cell. Biol

Epithelial-Mesenchyme Interactions

An immunofluorescence procedure for the tissue localization of glucosephosphate isomerase

J. Histochem. Cytochem

Cited by (42)

Induced pluripotent stem cell-derived salivary glands

Exosomal MicroRNA Transport from Salivary Mesenchyme Regulates Epithelial Progenitor Expansion during Organogenesis

Retinoic acid regulates embryonic development of mammalian submandibular salivary glands

Submandibular gland epithelial development and the importance of junctions

Single-cell RNA sequencing reveals PDFGRα<sup>+</sup> stromal cell subpopulations that promote proacinar cell differentiation in embryonic salivary gland organoids

Salivary gland tissues and derived primary and metastatic neoplasms: unusual pitfalls in the work-up of sellar lesions. A systematic review

Full paperA pituitary-salivary mixed gland induced by tissue recombination of embryonic pituitary epithelium and embryonic submandibular gland mesenchyme in mice☆

Abstract

Dev. Biol

J. Chromatogr

Stromal induction and specification of morphogenesis and cytodifferentiation of the epithelia of the Müllerian ducts and urogenital sinus during development of the uterus and vagina in mice

J. Exp. Zool

Epithelial-mesenchymal interactions in prostatic development. I. Morphological observations of prostatic inductions by urogenital sinus mesenchyme in epithelium of the adult rodent urinary bladder

J. Cell. Biol

Epithelial-Mesenchyme Interactions

An immunofluorescence procedure for the tissue localization of glucosephosphate isomerase

J. Histochem. Cytochem

Full paper
A pituitary-salivary mixed gland induced by tissue recombination of embryonic pituitary epithelium and embryonic submandibular gland mesenchyme in mice☆