Mesenchyme-Dependent Morphogenesis and Epithelium-Specific Cytodifferentiation in Mouse Mammary Gland

Sakakura, Teruyo; Nishizuka, Yasuaki; Dawe, Clyde J.

doi:10.1126/science.827022

Cited by 338 publications

(166 citation statements)

References 7 publications

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“…The mesenchyme is instructive and provides critical information to drive mammary differentiation. For example, mammary mesenchyme can induce embryonic epidermis from dorsal or midventral sites to form mammary buds that will undergo functional differentiation and milk synthesis (Cunha et al, 1995), whereas recombination of embryonic mammary epithelial cells with salivary mesenchyme produces epithelial salivary structures (Sakakura, Nishizuka, & Dawe, 1976). …”

Section: Cell Origin and Plasticitymentioning

confidence: 99%

Mammary epithelial cell: Influence of extracellular matrix composition and organization during development and tumorigenesis

Kass

Erler

Dembo

et al. 2007

The International Journal of Biochemistry & Cell Biology

275

220

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Stromal-epithelial interactions regulate mammary gland development and are critical for the maintenance of tissue homeostasis. The extracellular matrix, which is a proteinaceous component of the stroma, regulates mammary epithelial growth, survival, migration and differentiation through a repertoire of transmembrane receptors, of which integrins are the best characterized. Integrins modulate cell fate by reciprocally transducing biochemical and biophysical cues between the cell and the extracellular matrix, facilitating processes such as embryonic branching morphogenesis and lactation in the mammary gland. During breast development and cancer progression, the extracellular matrix is dynamically altered such that its composition, turnover, processing and orientation change dramatically. These modifications influence mammary epithelial cell shape, and modulate growth factor and hormonal responses to regulate processes including branching morphogenesis and alveolar differentiation. Malignant transformation of the breast is also associated with significant matrix remodeling and a progressive stiffening of the stroma that can enhance mammary epithelial cell growth, perturb breast tissue organization, and promote cell invasion and survival. In this review, we discuss the role of stromal-epithelial interactions in normal and malignant mammary epithelial cell behavior. We specifically focus on how dynamic modulation of the biochemical and biophysical properties of the extracellular matrix elicit a dialogue with the mammary epithelium through transmembrane integrin receptors to influence tissue morphogenesis, homeostasis and malignant transformation. Keywords NIH Public AccessAuthor Manuscript Int J Biochem Cell Biol. Author manuscript; available in PMC 2009 March 19. Published in final edited form as:Int J Biochem Cell Biol. 2007 ; 39(11): 1987-1994. doi:10.1016/j.biocel.2007.025. NIH-PA Author ManuscriptNIH-PA Author Manuscript NIH-PA Author ManuscriptCell facts• Stromal-epithelial interactions regulate mammary epithelial cell growth and differentiation during embryonic and postnatal development.• The spatial organization and composition of the extracellular matrix influence mammary epithelial cell behavior.• Alterations in extracellular matrix receptor expression can enable malignant transformation of the mammary epithelial cells.• Differences in the biophysical properties of the extracellular matrix due to an increase in deposit and/or cross-linking can induce the malignant transformation of mammary epithelial cells.

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Section: Cell Origin and Plasticitymentioning

confidence: 99%

Mammary epithelial cell: Influence of extracellular matrix composition and organization during development and tumorigenesis

Kass

Erler

Dembo

et al. 2007

The International Journal of Biochemistry & Cell Biology

275

220

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“…Indeed, the importance of this local communication and, in particular, the instructive nature of the mesenchyme now seems undeniable. For instance, embryonic mammary epithelium forms salivary rather than mammary-like structures if it is recombined with salivary gland mesenchyme and then engrafted underneath the renal capsule of a host mouse, although the epithelium still retains its ability to produce milk proteins in response to prolactin [10]. Moreover, when prospective pituitary epithelium from e8.5 Rathke's pouch is transplanted together with salivary mesenchyme, it forms salivary-like structures that in this instance contain differentiated α-amylase-producing acini [11].…”

Section: Introductionmentioning

confidence: 99%

The ADAM17–amphiregulin–EGFR Axis in Mammary Development and Cancer

Sternlicht

Sunnarborg

2008

J Mammary Gland Biol Neoplasia

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In order to fulfill its function of producing and delivering sufficient milk to newborn mammalian offspring, the mammary gland first has to form an extensive ductal network. As in all phases of mammary development, hormonal cues elicit local intra-and inter-cellular signaling cascades that regulate ductal growth and differentiation. Among other things, ductal development requires the epidermal growth factor receptor (EGFR), its ligand amphiregulin (AREG), and the transmembrane metalloproteinase AD-AM17, which can cleave and release AREG from the cell surface so that it may interact with its receptor. Tissue recombination and transplantation studies demonstrate that EGFR phosphorylation and ductal development proceed only when ADAM17 and AREG are expressed on mammary epithelial cells and EGFR is present on stromal cells, and that local administration of soluble AREG can rescue the development of ADAM17-deficient transplants. Thus proper mammary morphogenesis requires the ADAM17-mediated release of AREG from ductal epithelial cells, the subsequent activation of EGFR on stromal cells, and EGFR-dependent stromal responses that in return elicit a new set of epithelial responses, all culminating in the formation of a fully functional ductal tree. This, however, raises new issues concerning what may act upstream, downstream or in parallel with the ADAM17-AREG-EGFR axis, how it may become hijacked or corrupted during the onset and evolution of cancer, and how such ill effects may be confronted.

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“…In contrast to its effect on the epithelial branching pattern, mesenchyme appears to have little or no effect on the fate of the epithelial cells. In heterotypic tissue recombinations, the well-demonstrated capacity of submandibular mesenchyme to impose its own compact pattern of branching on other epithelia was assessed after recombination with epithelial rudiments of the parotid (Lawson, 1972), mammary gland (Sakakura et al, 1976), and embryonic palatal epithelium destined to become adult oral and nasal epithelium (Tyler and Koch, 1977). In each case, the mesenchyme forced on the epithelium a salivary-like branching pattern; however, the type of cytodifferentiation obtained remained obdurately typical of the original epithelial phenotype.…”

Section: (6) Origin Of the Three Major Types Of Salivary Glandsmentioning

confidence: 99%

Salivary Glands: A Paradigm for Diversity of Gland Development

Denny

Ball

Redman

1997

Critical Reviews in Oral Biology & Medicine

179

171

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The major salivary glands of mammals are represented by three pairs of organs that cooperate functionally to produce saliva for the oral cavity. While each type of gland produces a signature secretion that complements the secretions from the other glands, there is also redundancy as evidenced by secretion of functionally similar and, in some cases, identical products in the three glands. This, along with their common late initiation of development, in fetal terms, their similarities in developmental pattern, and their proximate sites of origin, suggests that a common regulatory cascade may have been shared until shortly before the onset of overt gland development. Furthermore, occasional ectopic differentiation of individual mature secretory cells in the wrong" gland suggests that control mechanisms responsible for the distinctive cellular composition of each gland also share many common steps, with only minor differences providing the impetus for diversification. To begin to address this area, we examine here the origins of the salivary glands by reviewing the expression patterns of several genes with known morphogenetic potential that may be involved based on developmental timing and location. The possibility that factors leading to determination of the sites of mammalian salivary gland development might be homologous to the regulatory cascade leading to salivarv gland formation in Drosophila is also evaluated. In a subsequent section, cellular phenotypes of neonatal and adult glands are compared and evaluated for insights into the mechanisms and lineages leading to cellular diversification. Finally, the phenomena of proliferation, repair, and regeneration in adult salivary glands are reviewed, with emphasis on the extent to which the cellular diversity is reversible and which cell type other than stem cells has the ability to redifferentiate into other cell types.

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Mesenchyme-Dependent Morphogenesis and Epithelium-Specific Cytodifferentiation in Mouse Mammary Gland

Cited by 338 publications

References 7 publications

Mammary epithelial cell: Influence of extracellular matrix composition and organization during development and tumorigenesis

Mammary epithelial cell: Influence of extracellular matrix composition and organization during development and tumorigenesis

The ADAM17–amphiregulin–EGFR Axis in Mammary Development and Cancer

Salivary Glands: A Paradigm for Diversity of Gland Development

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