Cord‐like Mosaic Patches in the Adrenal Cortex are Fractal: Implications for Growth and Development

Iannaccone, Philip M.; Morley, Steven D.; Skimina, Timothy A.; Mullins, John J.; Landini, Gabriel

doi:10.1096/fj.02-0451fje

Cited by 22 publications

(22 citation statements)

References 20 publications

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“…Quantitative comparison of radial adrenocortical stripe patterns in the experimental groups used in Validity of the 21-OH/LacZ Transgenic Mouse this study shows that they all displayed a similar corrected stripe number, suggesting that the stripe patterns in all three groups of mice are established by similar cell lineage mechanisms, irrespective of the means of generating mosaicism. This conclusion is supported by evidence from a different approach, which has established that the adrenocortical stripes displayed in rat aggregation chimeras and 21-OH/LacZ transgenic mice and rats are all fractal objects possessing identical fractal dimensions (16).…”

Section: Discussionmentioning

confidence: 82%

Validity of the 21‐OH/LacZTransgenic Mouse as a Model for Studying Adrenocortical Cell Lineage

Morley

et al. 2004

Endocrine Research

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Mosaic beta-galactosidase reporter staining patterns in the adult adrenal cortex of 21-OH/LacZ transgenic mice were compared to those observed in mouse chimeras and X-inactivation mosaics, which are known to have a lineage basis. This revealed similar patterns of blue and white radial stripes in all three experimental groups. Each blue stripe may contain one or more blue coherent clones of cells but this was taken into account by correcting the observed stripe numbers for the effects of different proportions of LacZ-positive (blue) and LacZ-negative (unstained) cells between adrenals. The corrected stripe numbers were similar in all three experimental groups, which supports the hypothesis that the stripes in the adrenals of 21-OH/LacZ transgenic mice are formed in a similar way to those in chimeras and X-inactivation mosaics (i.e., they have a lineage basis). This suggests that the 21-OH/LacZ transgenic mouse is likely to be a valid model for studying steroidogenic cell lineage in the adrenal cortex, thereby providing additional support for the centripetal migration hypothesis of adrenocortical cytogenesis.

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Section: Discussionmentioning

confidence: 82%

Validity of the 21‐OH/LacZTransgenic Mouse as a Model for Studying Adrenocortical Cell Lineage

Morley

et al. 2004

Endocrine Research

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“…In our study, we found three phenotypes of adrenal cortex cords: monophenotypic EGFP-positive cords, monophenotypic EGFP-negative cords, and polyphenotypic cords, indicating that adrenal cortex cords are of polyclonal embryonic origin. Iannaccone et al (2003) reported that the adrenal cortex can regenerate after extirpation of the organ, which leaves only a remnant of the zona glomerulosa. Along with the results of our present study, this suggests that there may be a common histogenesis of the three functionally distinct zones, the zona glomerulosa, the zona fasciculata, and the zona reticularis.…”

Section: Discussionmentioning

confidence: 99%

Polyclonal origin of hormone-producing cell populations evaluated as a direct in situ demonstration in EGFP/BALB/C chimeric mice

Sudo²,

Tezuka³

et al. 2010

Journal of Endocrinology

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We report the first demonstration of the embryonal patch patterns of endocrine organs and the polyclonality of hormone-producing cell populations using chimeric mice produced by aggregation of C57BL/6-Tg(CAG-EGFP)C14-Y01-FM131Osb transgenic mice and BALB/C mice. Confocal laser scanning microscopy (CLSM) analysis for enhanced green fluorescent protein (EGFP) and immunohistochemistry with anti-EGFP antibody revealed that all endocrine organs of chimeric mice had a mosaic appearance of EGFP-positive patches and EGFP-negative patches. The patches composed of EGFP-positive cells were distinctive in their size and shape. The pituitary patches were large and irregular, representing a geographical pattern. In contrast, parathyroid, pancreatic islet, and adrenal medulla patches were small and demarcated, representing an island-like pattern. Thyroid follicles and adrenal cortex cords showed a mixture of monophenotypia and polyphenotypia, indicating polyclonal embryonic origin. Furthermore, we studied the tissue clonality of hormone-producing cell populations in the pituitary, thyroid, and pancreatic islets using a combination method of CLSM for EGFP and immunohistochemistry for hormones. All the pituitary cell populations of GH, prolactin, TSH, FSH, LH, and ACTH, the calcitonin-producing cell population in the thyroid, and the insulin-and glucagonproducing cell populations in pancreatic islets had mosaic patterns in EGFP expression in the chimeric mice, suggesting polyclonal embryonic origin. In conclusion, the different patch patterns of the endocrine organs could contribute to the understanding of embryonic development and organization of endocrine organs. Furthermore, we clearly demonstrate that all hormone-producing cell populations are of polyclonal embryonic origin, derived from more than two progenitor cells.

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“…Later, pulse chase experiments involving radioactive-thymidine or BrdU studies reveal a predominant labeling of subcapsular cells followed by labeling in cells that are increasingly centripetal and exclusively in the inner cortical zones (Wright et al 1973;Zajicek et al 1986). More recent molecular tracking studies support the process of centripetal and clonogenic repopulation of the adrenal cortex (Ford and Young 1963;Iannaccone et al 2003). Chimeric and transgenic mice harboring a β-galactosidase reporter, under the control of several adrenocortical-specific promoters, reveal radial expression of the transgene from the outer zG to inner zF (Weinberg et al 1985;Iannaccone et al 2003).…”

mentioning

confidence: 93%

“…More recent molecular tracking studies support the process of centripetal and clonogenic repopulation of the adrenal cortex (Ford and Young 1963;Iannaccone et al 2003). Chimeric and transgenic mice harboring a β-galactosidase reporter, under the control of several adrenocortical-specific promoters, reveal radial expression of the transgene from the outer zG to inner zF (Weinberg et al 1985;Iannaccone et al 2003). Taken together, these studies suggest that the adrenal parenchyma is composed of clonally expanded cells that extend centripetally in a cord-like fashion from the outermost layers of the cortex to the innermost cortico-medullary boundary.…”

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confidence: 95%

Adrenocortical cells with stem/progenitor cell properties: Recent advances

Kim

Hammer

2007

Molecular and Cellular Endocrinology

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The existence and location of undifferentiated cells with the capability of maintaining the homeostasis of the adrenal cortex have long been sought. These cells are thought to remain mostly quiescent with a potential to commit to self-renewal processes or terminal differentiation to homeostatically repopulate the organ. In addition, in response to physiologic stress, the undifferentiated cells undergo rapid proliferation to accommodate organismic need. Sufficient adrenocortical proliferative capacity lasting the lifespan of the host has been demonstrated through cell transplantation and enucleation experiments. Labeling experiments with tritium, BrdU, or trypan blue, as well as transgenic assays support the clonogenic identity and location of these undefined cells within the gland periphery. We define undifferentiated adrenocortical cells as cells devoid of steroidogenic gene expression, and differentiated cells as cells with steroidogenic capacity. In this review, we discuss historic developmental studies together with recent molecular examinations that aim to characterize such populations of cells.Keywords stem cell; progenitor cell; NR5A1 (SF1, AD4BP); NR0B1 (DAX1, AHCH); inhibin; differentiation Adrenal Anatomy and Developmental MilestonesThe development of the adrenal gland occurs in discrete phases. During the 4 th week of human gestation, coelomic epithelial cells and/or the underlying mesonephric mesenchymal cells residing between the primitive urogenital ridge and the dorsal mesentery begin to proliferate and migrate from the mesonephros to form the earliest manifestation of developing steroidogenic tissue, the adrenogonadal primordium (Sucheston and Cannon 1968;Mesiano and Jaffe 1997). The caudal aspect of this structure, the adrenal primordia is organized into cord-like ultra-structures consistent with steroidogenic potential. This developmental program culminates with the separation of the gonadal and adrenal primordia into discrete fetal organs by the 8 th week of gestation (Sucheston and Cannon 1968;Mesiano and Jaffe 1997 Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. Following the formation of the early adrenal primordia, referred to as the fetal adrenal zone (fetal cortex), the development of the definitive zone (definitive cortex) is initiated. While early researchers assumed that the definitive cortex arose from the fetal cortex, histological observations indicated that the adult/definitive cortex arises from the migration of a distinct population of cells from the coelomic epithelium and/or the underlying mesonephric mesenchyme (Keene and Hewer...

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Cord‐like Mosaic Patches in the Adrenal Cortex are Fractal: Implications for Growth and Development

Cited by 22 publications

References 20 publications

Validity of the 21‐OH/LacZTransgenic Mouse as a Model for Studying Adrenocortical Cell Lineage

Validity of the 21‐OH/LacZTransgenic Mouse as a Model for Studying Adrenocortical Cell Lineage

Polyclonal origin of hormone-producing cell populations evaluated as a direct in situ demonstration in EGFP/BALB/C chimeric mice

Adrenocortical cells with stem/progenitor cell properties: Recent advances

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