Adrenocortical stem cells in health and disease

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Adrenocortical stem cells in health and disease
  • Yates, R. et al. Adrenocortical development, maintenance, and disease. Curr. Top. Dev. Biol. 106, 239–312 (2013).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Tsilosani, A., Gao, C. & Zhang, W. Aldosterone-regulated sodium transport and blood pressure. Front. Physiol. 13, 770375 (2022).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Douglass, A. M. et al. Neural basis for fasting activation of the hypothalamic–pituitary–adrenal axis. Nature 620, 154–162 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Matzke, C. C., Kusch, J. M., Janz, D. M. & Lane, J. E. Perceived predation risk predicts glucocorticoid hormones, but not reproductive success in a colonial rodent. Horm. Behav. 143, 105200 (2022).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Wirth, M. M. Hormones, stress, and cognition: the effects of glucocorticoids and oxytocin on memory. Adapt. Hum. Behav. Physiol. 1, 177–201 (2015).

    Article 

    Google Scholar 

  • Li, J. X. & Cummins, C. L. Fresh insights into glucocorticoid-induced diabetes mellitus and new therapeutic directions. Nat. Rev. Endocrinol. 18, 540–557 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Nguyen, T. V. et al. Interactive effects of dehydroepiandrosterone and testosterone on cortical thickness during early brain development. J. Neurosci. 33, 10840–10848 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Dumontet, T. & Martinez, A. Adrenal androgens, adrenarche, and zona reticularis: a human affair? Mol. Cell Endocrinol. 528, 111239 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Hammer, G. D. & Basham, K. J. Stem cell function and plasticity in the normal physiology of the adrenal cortex. Mol. Cell Endocrinol. 519, 111043 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Lerario, A. M., Moraitis, A. & Hammer, G. D. Genetics and epigenetics of adrenocortical tumors. Mol. Cell Endocrinol. 386, 67–84 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Scheys, J. O., Heaton, J. H. & Hammer, G. D. Evidence of adrenal failure in aging Dax1-deficient mice. Endocrinology 152, 3430–3439 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Cheng, K. et al. The developmental origin and the specification of the adrenal cortex in humans and cynomolgus monkeys. Sci. Adv. 8, eabn8485 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Ross, I. L. & Louw, G. J. Embryological and molecular development of the adrenal glands. Clin. Anat. 28, 235–242 (2015).

    Article 
    PubMed 

    Google Scholar 

  • Bandiera, R. et al. WT1 maintains adrenal-gonadal primordium identity and marks a population of AGP-like progenitors within the adrenal gland. Dev. Cell 27, 5–18 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Neirijnck, Y. et al. Single-cell transcriptomic profiling redefines the origin and specification of early adrenogonadal progenitors. Cell Rep. 42, 112191 (2023).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Kim, J. H. & Choi, M. H. Embryonic development and adult regeneration of the adrenal gland. Endocrinol. Metab. 35, 765–773 (2020).

    Article 
    CAS 

    Google Scholar 

  • Val, P., Martinez-Barbera, J. P. & Swain, A. Adrenal development is initiated by Cited2 and Wt1 through modulation of Sf-1 dosage. Development 134, 2349–2358 (2007).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Moore, A. W., McInnes, L., Kreidberg, J., Hastie, N. D. & Schedl, A. YAC complementation shows a requirement for Wt1 in the development of epicardium, adrenal gland and throughout nephrogenesis. Development 126, 1845–1857 (1999).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Bamforth, S. D. et al. Cardiac malformations, adrenal agenesis, neural crest defects and exencephaly in mice lacking Cited2, a new Tfap2 co-activator. Nat. Genet. 29, 469–474 (2001).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Parker, K. L. & Schimmer, B. P. Steroidogenic factor 1: a key determinant of endocrine development and function. Endocr. Rev. 18, 361–377 (1997).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Abou Nader, N. & Boyer, A. Adrenal cortex development and maintenance: knowledge acquired from mouse models. Endocrinology 162, bqab187 (2021).

    Article 
    PubMed 

    Google Scholar 

  • Akkuratova, N., Faure, L., Kameneva, P., Kastriti, M. E. & Adameyko, I. Developmental heterogeneity of embryonic neuroendocrine chromaffin cells and their maturation dynamics. Front. Endocrinol. 13, 1020000 (2022).

    Article 

    Google Scholar 

  • Ishimoto, H. & Jaffe, R. B. Development and function of the human fetal adrenal cortex: a key component in the feto-placental unit. Endocr. Rev. 32, 317–355 (2011).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • King, P., Paul, A. & Laufer, E. Shh signaling regulates adrenocortical development and identifies progenitors of steroidogenic lineages. Proc. Natl Acad. Sci. USA 106, 21185–21190 (2009).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Wood, M. A. et al. Fetal adrenal capsular cells serve as progenitor cells for steroidogenic and stromal adrenocortical cell lineages in M. musculus. Development 140, 4522–4532 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Finco, I., Lerario, A. M. & Hammer, G. D. Sonic Hedgehog and WNT signaling promote adrenal gland regeneration in male mice. Endocrinology 159, 579–596 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Huang, C. C., Miyagawa, S., Matsumaru, D., Parker, K. L. & Yao, H. H. Progenitor cell expansion and organ size of mouse adrenal is regulated by sonic hedgehog. Endocrinology 151, 1119–1128 (2010).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Zubair, M., Parker, K. L. & Morohashi, K. Developmental links between the fetal and adult zones of the adrenal cortex revealed by lineage tracing. Mol. Cell Biol. 28, 7030–7040 (2008).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Ingham, P. W. Hedgehog signaling. Curr. Top. Dev. Biol. 149, 1–58 (2022).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Grainger, S. & Willert, K. Mechanisms of Wnt signaling and control. Wiley Interdiscip. Rev. Syst. Biol. Med. 10, e1422 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Vidal, V. et al. The adrenal capsule is a signaling center controlling cell renewal and zonation through Rspo3. Genes. Dev. 30, 1389–1394 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Kim, J. E. et al. Single cell and genetic analyses reveal conserved populations and signaling mechanisms of gastrointestinal stromal niches. Nat. Commun. 11, 334 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Drelon, C., Berthon, A., Mathieu, M., Martinez, A. & Val, P. Adrenal cortex tissue homeostasis and zonation: a WNT perspective. Mol. Cell Endocrinol. 408, 156–164 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Lucas, C. et al. Loss of LGR4/GPR48 causes severe neonatal salt wasting due to disrupted WNT signaling altering adrenal zonation. J. Clin. Invest. 133, e164915 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Hasenmajer, V. et al. Rare forms of genetic paediatric adrenal insufficiency: excluding congenital adrenal hyperplasia. Rev. Endocr. Metab. Disord. 24, 345–363 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Basham, K. J. et al. A ZNRF3-dependent Wnt/beta-catenin signaling gradient is required for adrenal homeostasis. Genes Dev. 33, 209–220 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Drelon, C. et al. PKA inhibits WNT signalling in adrenal cortex zonation and prevents malignant tumour development. Nat. Commun. 7, 12751 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Schulte, D. M., Shapiro, I., Reincke, M. & Beuschlein, F. Expression and spatio-temporal distribution of differentiation and proliferation markers during mouse adrenal development. Gene Expr. Patterns 7, 72–81 (2007).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Zubair, M., Ishihara, S., Oka, S., Okumura, K. & Morohashi, K. Two-step regulation of Ad4BP/SF-1 gene transcription during fetal adrenal development: initiation by a Hox–Pbx1–Prep1 complex and maintenance via autoregulation by Ad4BP/SF-1. Mol. Cell Biol. 26, 4111–4121 (2006).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Pihlajoki, M., Dorner, J., Cochran, R. S., Heikinheimo, M. & Wilson, D. B. Adrenocortical zonation, renewal, and remodeling. Front. Endocrinol. 6, 27 (2015).

    Article 

    Google Scholar 

  • Havelock, J. C., Auchus, R. J. & Rainey, W. E. The rise in adrenal androgen biosynthesis: adrenarche. Semin. Reprod. Med. 22, 337–347 (2004).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Freedman, B. D. et al. Adrenocortical zonation results from lineage conversion of differentiated zona glomerulosa cells. Dev. Cell 26, 666–673 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Zajicek, G., Ariel, I. & Arber, N. The streaming adrenal cortex: direct evidence of centripetal migration of adrenocytes by estimation of cell turnover rate. J. Endocrinol. 111, 477–482 (1986).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Dumontet, T. et al. PKA signaling drives reticularis differentiation and sexually dimorphic adrenal cortex renewal. JCI Insight 3, e98394 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Grabek, A. et al. The adult adrenal cortex undergoes rapid tissue renewal in a sex-specific manner. Cell Stem Cell 25, 290–296 e292 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Kim, A. C. et al. Targeted disruption of beta-catenin in Sf1-expressing cells impairs development and maintenance of the adrenal cortex. Development 135, 2593–2602 (2008).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Borges, K. S. et al. Non-canonical Wnt signaling triggered by WNT2B drives adrenal aldosterone production. Preprint at bioRxiv (2024).

  • Nishimoto, K., Harris, R. B., Rainey, W. E. & Seki, T. Sodium deficiency regulates rat adrenal zona glomerulosa gene expression. Endocrinology 155, 1363–1372 (2014).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Bielohuby, M. et al. Growth analysis of the mouse adrenal gland from weaning to adulthood: time- and gender-dependent alterations of cell size and number in the cortical compartment. Am. J. Physiol. Endocrinol. Metab. 293, E139–E146 (2007).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Holland, J. H. Signals and Boundaries: Building Blocks for Complex Adaptive Systems (MIT Press, 2014).

  • Chu, Y., Xing, Y. & Hammer, G. Unravelling the role of CDK7-mediated SF1 serine 203 phosphorylation in adrenal homeostasis. J. Endocr. Soc. 6, A135–A136 (2022).

    Article 
    PubMed Central 

    Google Scholar 

  • Sandhoff, T. W. & McLean, M. P. Repression of the rat steroidogenic acute regulatory (StAR) protein gene by PGF2α is modulated by the negative transcription factor DAX-1. Endocrine 10, 83–91 (1999).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Khalfallah, O., Rouleau, M., Barbry, P., Bardoni, B. & Lalli, E. Dax-1 knockdown in mouse embryonic stem cells induces loss of pluripotency and multilineage differentiation. Stem Cell 27, 1529–1537 (2009).

    Article 
    CAS 

    Google Scholar 

  • Zhang, J. et al. Dax1 and Nanog act in parallel to stabilize mouse embryonic stem cells and induced pluripotency. Nat. Commun. 5, 5042 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Zhang, W. et al. nr0b1 (DAX1) loss of function in zebrafish causes hypothalamic defects via abnormal progenitor proliferation and differentiation. J. Genet. Genomics 49, 217–229 (2022).

    Article 
    PubMed 

    Google Scholar 

  • Achermann, J. C., Silverman, B. L., Habiby, R. L. & Jameson, J. L. Presymptomatic diagnosis of X-linked adrenal hypoplasia congenita by analysis of DAX1. J. Pediatr. 137, 878–881 (2000).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Gummow, B. M., Scheys, J. O., Cancelli, V. R. & Hammer, G. D. Reciprocal regulation of a glucocorticoid receptor-steroidogenic factor-1 transcription complex on the Dax-1 promoter by glucocorticoids and adrenocorticotropic hormone in the adrenal cortex. Mol. Endocrinol. 20, 2711–2723 (2006).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Ganuza, M. et al. Genetic inactivation of Cdk7 leads to cell cycle arrest and induces premature aging due to adult stem cell exhaustion. EMBO J. 31, 2498–2510 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Leal, L. F. et al. Inhibition of the Tcf/β-catenin complex increases apoptosis and impairs adrenocortical tumor cell proliferation and adrenal steroidogenesis. Oncotarget 6, 43016–43032 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Chu, Y., Ho, W. J. & Dunn, J. C. Basic fibroblast growth factor delivery enhances adrenal cortical cellular regeneration. Tissue Eng. A 15, 2093–2101 (2009).

    Article 
    CAS 

    Google Scholar 

  • Looyenga, B. D. & Hammer, G. D. Origin and identity of adrenocortical tumors in inhibin knockout mice: implications for cellular plasticity in the adrenal cortex. Mol. Endocrinol. 20, 2848–2863 (2006).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Ornitz, D. M. & Itoh, N. The fibroblast growth factor signaling pathway. Wiley Interdiscip. Rev. Dev. Biol. 4, 215–266 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Forbes, B. E., Blyth, A. J. & Wit, J. M. Disorders of IGFs and IGF-1R signaling pathways. Mol. Cell Endocrinol. 518, 111035 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Mesiano, S., Mellon, S. H. & Jaffe, R. B. Mitogenic action, regulation, and localization of insulin-like growth factors in the human fetal adrenal gland. J. Clin. Endocrinol. Metab. 76, 968–976 (1993).

    CAS 
    PubMed 

    Google Scholar 

  • Basile, D. P. & Holzwarth, M. A. Basic fibroblast growth factor may mediate proliferation in the compensatory adrenal growth response. Am. J. Physiol. 265, R1253–R1261 (1993).

    CAS 
    PubMed 

    Google Scholar 

  • Lepique, A. P. et al. c-Myc protein is stabilized by fibroblast growth factor 2 and destabilized by ACTH to control cell cycle in mouse Y1 adrenocortical cells. J. Mol. Endocrinol. 33, 623–638 (2004).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Gospodarowicz, D., Ill, C. R., Hornsby, P. J. & Gill, G. N. Control of bovine adrenal cortical cell proliferation by fibroblast growth factor. Lack of effect of epidermal growth factor. Endocrinology 100, 1080–1089 (1977).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Crickard, K., Ill, C. R. & Jaffe, R. B. Control of proliferation of human fetal adrenal cells in vitro. J. Clin. Endocrinol. Metab. 53, 790–796 (1981).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Gospodarowicz, D. & Handley, H. H. Stimulation of division of Y1 adrenal cells by a growth factor isolated from bovine pituitary glands. Endocrinology 97, 102–107 (1975).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Guasti, L., Candy Sze, W. C., McKay, T., Grose, R. & King, P. J. FGF signalling through Fgfr2 isoform IIIb regulates adrenal cortex development. Mol. Cell Endocrinol. 371, 182–188 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Kim, Y. et al. Fibroblast growth factor receptor 2 regulates proliferation and Sertoli differentiation during male sex determination. Proc. Natl Acad. Sci. USA 104, 16558–16563 (2007).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Hafner, R., Bohnenpoll, T., Rudat, C., Schultheiss, T. M. & Kispert, A. Fgfr2 is required for the expansion of the early adrenocortical primordium. Mol. Cell Endocrinol. 413, 168–177 (2015).

    Article 
    PubMed 

    Google Scholar 

  • Laufer, E., Kesper, D., Vortkamp, A. & King, P. Sonic hedgehog signaling during adrenal development. Mol. Cell Endocrinol. 351, 19–27 (2012).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Else, T. et al. Adrenocortical carcinoma. Endocr. Rev. 35, 282–326 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Nanba, K. et al. Molecular heterogeneity in aldosterone-producing adenomas. J. Clin. Endocrinol. Metab. 101, 999–1007 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Fassnacht, M. et al. European Society of Endocrinology Clinical Practice Guidelines on the management of adrenocortical carcinoma in adults, in collaboration with the European Network for the Study of Adrenal Tumors. Eur. J. Endocrinol. 179, G1–G46 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Scadden, D. T. Nice neighborhood: emerging concepts of the stem cell niche. Cell 157, 41–50 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Hoggatt, J., Kfoury, Y. & Scadden, D. T. Hematopoietic stem cell niche in health and disease. Annu. Rev. Pathol. 11, 555–581 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Zheng, S. et al. Comprehensive pan-genomic characterization of adrenocortical carcinoma. Cancer Cell 29, 723–736 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Gomes, D. C. et al. Sonic hedgehog signaling is active in human adrenal cortex development and deregulated in adrenocortical tumors. J. Clin. Endocrinol. Metab. 99, E1209–E1216 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Boulkroun, S. et al. Aldosterone-producing adenoma formation in the adrenal cortex involves expression of stem/progenitor cell markers. Endocrinology 152, 4753–4763 (2011).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Goh, G. et al. Recurrent activating mutation in PRKACA in cortisol-producing adrenal tumors. Nat. Genet. 46, 613–617 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Marquardt, A. et al. Identifying new potential biomarkers in adrenocortical tumors based on mRNA expression data using machine learning. Cancers 13, 4671 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Mohan, D. R. et al. β-catenin-driven differentiation is a tissue-specific epigenetic vulnerability in adrenal cancer. Cancer Res. 83, 2123–2141 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Heaton, J. H. et al. Progression to adrenocortical tumorigenesis in mice and humans through insulin-like growth factor 2 and β-catenin. Am. J. Pathol. 181, 1017–1033 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Pinto, E. M. et al. Genomic landscape of paediatric adrenocortical tumours. Nat. Commun. 6, 6302 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Werminghaus, P. et al. Hedgehog-signaling is upregulated in non-producing human adrenal adenomas and antagonism of hedgehog-signaling inhibits proliferation of NCI-H295R cells and an immortalized primary human adrenal cell line. J. Steroid Biochem. Mol. Biol. 139, 7–15 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Mateska, I., Nanda, K., Dye, N. A., Alexaki, V. I. & Eaton, S. Range of SHH signaling in adrenal gland is limited by membrane contact to cells with primary cilia. J. Cell Biol. 219, e201910087 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Borges, K. S. et al. Wnt/β-catenin activation cooperates with loss of p53 to cause adrenocortical carcinoma in mice. Oncogene 39, 5282–5291 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Berthon, A. et al. Constitutive β-catenin activation induces adrenal hyperplasia and promotes adrenal cancer development. Hum. Mol. Genet. 19, 1561–1576 (2010).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Wilmouth, J. J. Jr. et al. Sexually dimorphic activation of innate antitumor immunity prevents adrenocortical carcinoma development. Sci. Adv. 8, eadd0422 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Reutens, A. T. et al. Clinical and functional effects of mutations in the DAX-1 gene in patients with adrenal hypoplasia congenita. J. Clin. Endocrinol. Metab. 84, 504–511 (1999).

    CAS 
    PubMed 

    Google Scholar 

  • Lyraki, R. et al. Crosstalk between androgen receptor and WNT/β-catenin signaling causes sex-specific adrenocortical hyperplasia in mice. Dis. Model. Mech. 16, dmm050053 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Kamilaris, C. D. C., Hannah-Shmouni, F. & Stratakis, C. A. Adrenocortical tumorigenesis: lessons from genetics. Best Pract. Res. Clin. Endocrinol. Metab. 34, 101428 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Lapunzina, P. Risk of tumorigenesis in overgrowth syndromes: a comprehensive review. Am. J. Med. Genet. C 137C, 53–71 (2005).

    Article 

    Google Scholar 

  • Husebye, E. S., Pearce, S. H., Krone, N. P. & Kampe, O. Adrenal insufficiency. Lancet 397, 613–629 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Holmes, L. A survey of bar coding in Canadian teaching hospitals. Dimens. Health Serv. 64, 23–25 (1987).

    CAS 
    PubMed 

    Google Scholar 

  • Ferraz-de-Souza, B., Lin, L. & Achermann, J. C. Steroidogenic factor-1 (SF-1, NR5A1) and human disease. Mol. Cell Endocrinol. 336, 198–205 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Bland, M. L. et al. Haploinsufficiency of steroidogenic factor-1 in mice disrupts adrenal development leading to an impaired stress response. Proc. Natl Acad. Sci. USA 97, 14488–14493 (2000).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Arboleda, V. A. et al. Mutations in the PCNA-binding domain of CDKN1C cause IMAGe syndrome. Nat. Genet. 44, 788–792 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Ma, Y. et al. CDKN1C negatively regulates RNA polymerase II C-terminal domain phosphorylation in an E2F1-dependent manner. J. Biol. Chem. 285, 9813–9822 (2010).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Lewis, A. E. et al. Phosphorylation of steroidogenic factor 1 is mediated by cyclin-dependent kinase 7. Mol. Endocrinol. 22, 91–104 (2008).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Alheim, K. et al. Identification of a functional glucocorticoid response element in the promoter of the cyclin-dependent kinase inhibitor p57Kip2. J. Mol. Endocrinol. 30, 359–368 (2003).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Lin, K. T. & Wang, L. H. New dimension of glucocorticoids in cancer treatment. Steroids 111, 84–88 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Castelo-Branco, G. et al. Differential regulation of midbrain dopaminergic neuron development by Wnt-1, Wnt-3a, and Wnt-5a. Proc. Natl Acad. Sci. USA 100, 12747–12752 (2003).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Biesecker, L. G. GLI3-Related Pallister–Hall Syndrome in GeneReviews (eds Adam, M. P. et al.) (University of Washington, 2000).

  • Bose, J., Grotewold, L. & Ruther, U. Pallister–Hall syndrome phenotype in mice mutant for Gli3. Hum. Mol. Genet. 11, 1129–1135 (2002).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Mandel, H. et al. SERKAL syndrome: an autosomal-recessive disorder caused by a loss-of-function mutation in WNT4. Am. J. Hum. Genet. 82, 39–47 (2008).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Giordano, R. et al. Improvement of anthropometric and metabolic parameters, and quality of life following treatment with dual-release hydrocortisone in patients with Addison’s disease. Endocrine 51, 360–368 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Whitaker, M. et al. An oral multiparticulate, modified-release, hydrocortisone replacement therapy that provides physiological cortisol exposure. Clin. Endocrinol. 80, 554–561 (2014).

    Article 
    CAS 

    Google Scholar 

  • Quinkler, M., Miodini Nilsen, R., Zopf, K., Ventz, M. & Oksnes, M. Modified-release hydrocortisone decreases BMI and HbA1c in patients with primary and secondary adrenal insufficiency. Eur. J. Endocrinol. 172, 619–626 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Johannsson, G. et al. Improved cortisol exposure-time profile and outcome in patients with adrenal insufficiency: a prospective randomized trial of a novel hydrocortisone dual-release formulation. J. Clin. Endocrinol. Metab. 97, 473–481 (2012).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Graves, L. E. et al. Future directions for adrenal insufficiency: cellular transplantation and genetic therapies. J. Clin. Endocrinol. Metab. 108, 1273–1289 (2023).

    Article 
    PubMed 

    Google Scholar 

  • Markmann, S. et al. Biology of the adrenal gland cortex obviates effective use of adeno-associated virus vectors to treat hereditary adrenal disorders. Hum. Gene Ther. 29, 403–412 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Tajima, T. et al. Restoration of adrenal steroidogenesis by adenovirus-mediated transfer of human cytochrome P450 21-hydroxylase into the adrenal gland of 21-hydroxylase-deficient mice. Gene Ther. 6, 1898–1903 (1999).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Onuma, H., Sato, Y. & Harashima, H. Lipid nanoparticle-based ribonucleoprotein delivery for in vivo genome editing. J. Control. Rel. 355, 406–416 (2023).

    Article 
    CAS 

    Google Scholar 

  • Dammes, N. et al. Conformation-sensitive targeting of lipid nanoparticles for RNA therapeutics. Nat. Nanotechnol. 16, 1030–1038 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Cruz, L. J., Rezaei, S., Grosveld, F., Philipsen, S. & Eich, C. Nanoparticles targeting hematopoietic stem and progenitor cells: multimodal carriers for the treatment of hematological diseases. Front. Genome Edit. 4, 1030285 (2022).

    Article 

    Google Scholar 

  • Xu, J. et al. Oligodendrocyte progenitor cell-specific delivery of lipid nanoparticles loaded with Olig2 synthetically modified messenger RNA for ischemic stroke therapy. Acta Biomater. 174, 297–313 (2024).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Tang, Y. et al. Nanoparticle-based RNAi therapeutics targeting cancer stem cells: update and prospective. Pharmaceutics 13, 2116 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Ye, C. et al. Overexpression of FZD7 is associated with poor survival in patients with colon cancer. Pathol. Res. Pract. 215, 152478 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Zeng, Z. et al. LGR4 overexpression is associated with clinical parameters and poor prognosis of serous ovarian cancer. Cancer Biomark 28, 65–72 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Ordaz-Ramos, A., Rosales-Gallegos, V. H., Melendez-Zajgla, J., Maldonado, V. & Vazquez-Santillan, K. The role of LGR4 (GPR48) in normal and cancer processes. Int. J. Mol. Sci. 22, 4690 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • King, T. D., Zhang, W., Suto, M. J. & Li, Y. Frizzled7 as an emerging target for cancer therapy. Cell Signal. 24, 846–851 (2012).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Nickho, H. et al. Developing and characterization of single chain variable fragment (scFv) antibody against frizzled 7 (Fzd7) receptor. Bioengineered 8, 501–510 (2017).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Khodaverdi, E., Shabani, A. A., Madanchi, H. & Farahmand, L. Synthesis of the scFv fragment of anti-Frizzled-7 antibody and evaluation of its effects on triple-negative breast cancer in vitro study. Clin. Transl. Oncol. 26, 231–238 (2024).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Cao, J. et al. Selective targeting and eradication of LGR5+ cancer stem cells using RSPO-conjugated doxorubicin liposomes. Mol. Cancer Ther. 17, 1475–1485 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Graves, L. E. et al. AAV-delivered hepato-adrenal cooperativity in steroidogenesis: implications for gene therapy for congenital adrenal hyperplasia. Mol. Ther. Meth. Clin. Dev. 32, 101232 (2024).

    Article 
    CAS 

    Google Scholar 

  • Balyura, M. et al. Transplantation of bovine adrenocortical cells encapsulated in alginate. Proc. Natl Acad. Sci. USA 112, 2527–2532 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Zupekan, T. & Dunn, J. C. Adrenocortical cell transplantation reverses a murine model of adrenal failure. J. Pediat. Surg. 46, 1208–1213 (2011).

    Article 
    PubMed 

    Google Scholar 

  • Thomas, M., Wang, X. & Hornsby, P. J. Human adrenocortical cell xenotransplantation: model of cotransplantation of human adrenocortical cells and 3T3 cells in scid mice to form vascularized functional tissue and prevent adrenal insufficiency. Xenotransplantation 9, 58–67 (2002).

    Article 
    PubMed 

    Google Scholar 

  • Gondo, S. et al. Adipose tissue-derived and bone marrow-derived mesenchymal cells develop into different lineage of steroidogenic cells by forced expression of steroidogenic factor 1. Endocrinology 149, 4717–4725 (2008).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Yanase, T. et al. Differentiation and regeneration of adrenal tissues: an initial step toward regeneration therapy for steroid insufficiency. Endocr. J. 53, 449–459 (2006).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Yazawa, T. et al. Differentiation of adult stem cells derived from bone marrow stroma into Leydig or adrenocortical cells. Endocrinology 147, 4104–4111 (2006).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Yazawa, T. et al. Differentiation of mesenchymal stem cells and embryonic stem cells into steroidogenic cells using steroidogenic factor-1 and liver receptor homolog-1. Mol. Cell Endocrinol. 336, 127–132 (2011).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Tanaka, T. et al. Steroidogenic factor 1/adrenal 4 binding protein transforms human bone marrow mesenchymal cells into steroidogenic cells. J. Mol. Endocrinol. 39, 343–350 (2007).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Gondo, S. et al. SF-1/Ad4BP transforms primary long-term cultured bone marrow cells into ACTH-responsive steroidogenic cells. Genes Cell 9, 1239–1247 (2004).

    Article 
    CAS 

    Google Scholar 

  • Tanaka, T. et al. Extension of survival in bilaterally adrenalectomized mice by implantation of SF-1/Ad4BP-induced steroidogenic cells. Endocrinology 161, bqaa007 (2020).

    Article 
    PubMed 

    Google Scholar 

  • Crawford, P. A., Sadovsky, Y. & Milbrandt, J. Nuclear receptor steroidogenic factor 1 directs embryonic stem cells toward the steroidogenic lineage. Mol. Cell Biol. 17, 3997–4006 (1997).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Oikonomakos, I. et al. In vitro differentiation of mouse pluripotent stem cells into corticosteroid-producing adrenocortical cells. Stem Cell Rep. 19, 1289–1303 (2024).

    Article 
    CAS 

    Google Scholar 

  • Ruiz-Babot, G. et al. Generation of glucocorticoid-producing cells derived from human pluripotent stem cells. Cell Rep. Meth. 3, 100627 (2023).

    Article 
    CAS 

    Google Scholar 

  • Sakata, Y. et al. Reconstitution of human adrenocortical specification and steroidogenesis using induced pluripotent stem cells. Dev. Cell 57, 2566–2583 e2568 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Cabrera-Salcedo, C., Kumar, P., Hwa, V. & Dauber, A. IMAGe and related undergrowth syndromes: the complex spectrum of gain-of-function CDKN1C mutations. Pediat. Endocrinol. Rev. 14, 289–297 (2017).

    Google Scholar 

  • Mathieu, M. et al. Steroidogenic differentiation and PKA signaling are programmed by histone methyltransferase EZH2 in the adrenal cortex. Proc. Natl Acad. Sci. USA 115, E12265–E12274 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Pitetti, J. L. et al. Insulin and IGF1 receptors are essential for XX and XY gonadal differentiation and adrenal development in mice. PLoS Genet. 9, e1003160 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Suntharalingham, J. P., Buonocore, F., Duncan, A. J. & Achermann, J. C. DAX-1 (NR0B1) and steroidogenic factor-1 (SF-1, NR5A1) in human disease. Best Pract. Res. Clin. Endocrinol. Metab. 29, 607–619 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Luo, X., Ikeda, Y. & Parker, K. L. A cell-specific nuclear receptor is essential for adrenal and gonadal development and sexual differentiation. Cell 77, 481–490 (1994).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Stallings, N. R. et al. Development of a transgenic green fluorescent protein lineage marker for steroidogenic factor 1. Endocr. Res. 28, 497–504 (2002).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Hobeika, C. et al. Day surgery for acute appendicitis in adults: a prospective series of 102 patients. Surg. Laparosc. Endosc. Percutan. Tech. 27, 158–162 (2017).

    Article 
    PubMed 

    Google Scholar 

  • Dufour, D. et al. Loss of SUMO-specific protease 2 causes isolated glucocorticoid deficiency by blocking adrenal cortex zonal transdifferentiation in mice. Nat. Commun. 13, 7858 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Maharaj, A. et al. Sphingosine-1-phosphate lyase (SGPL1) deficiency is associated with mitochondrial dysfunction. J. Steroid Biochem. Mol. Biol. 202, 105730 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Ching, S. & Vilain, E. Targeted disruption of Sonic Hedgehog in the mouse adrenal leads to adrenocortical hypoplasia. Genesis 47, 628–637 (2009).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Beuschlein, F. et al. Cortisol producing adrenal adenoma—a new manifestation of Gardner’s syndrome. Endocr. Res. 26, 783–790 (2000).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Vouillarmet, J. et al. Aldosterone-producing adenoma with a somatic KCNJ5 mutation revealing APC-dependent familial adenomatous polyposis. J. Clin. Endocrinol. Metab. 101, 3874–3878 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Gagnon, N. et al. Small adrenal incidentaloma becoming an aggressive adrenocortical carcinoma in a patient carrying a germline APC variant. Endocrine 68, 203–209 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Bhandaru, M. et al. Hyperaldosteronism, hypervolemia, and increased blood pressure in mice expressing defective APC. Am. J. Physiol. Regul. Integr. Comp. Physiol 297, R571–R575 (2009).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Brioude, F. et al. Expert consensus document: clinical and molecular diagnosis, screening and management of Beckwith–Wiedemann syndrome: an international consensus statement. Nat. Rev. Endocrinol. 14, 229–249 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Lavoie, J. M. et al. Whole-genome and transcriptome analysis of advanced adrenocortical cancer highlights multiple alterations affecting epigenome and DNA repair pathways. Cold Spring Harb. Mol. Case Stud. 8, a006148 (2022).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Nazha, B. et al. Blood-based next-generation sequencing in adrenocortical carcinoma. Oncologist 27, 462–468 (2022).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Zhou, J. et al. Somatic mutations of GNA11 and GNAQ in CTNNB1-mutant aldosterone-producing adenomas presenting in puberty, pregnancy or menopause. Nat. Genet. 53, 1360–1372 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Pignatti, E. et al. β-catenin causes adrenal hyperplasia by blocking zonal transdifferentiation. Cell Rep. 31, 107524 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • De Martino, M. C. et al. Molecular screening for a personalized treatment approach in advanced adrenocortical cancer. J. Clin. Endocrinol. Metab. 98, 4080–4088 (2013).

    Article 
    PubMed 

    Google Scholar 

  • Tamburello, M. et al. FGF/FGFR signaling in adrenocortical development and tumorigenesis: novel potential therapeutic targets in adrenocortical carcinoma. Endocrine 77, 411–418 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Pozdeyev, N. et al. Targeted genomic analysis of 364 adrenocortical carcinomas. Endocr. Relat. Cancer 28, 671–681 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Almeida, M. Q. et al. Steroidogenic factor 1 overexpression and gene amplification are more frequent in adrenocortical tumors from children than from adults. J. Clin. Endocrinol. Metab. 95, 1458–1462 (2010).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Cao, Y. et al. Activating hotspot L205R mutation in PRKACA and adrenal Cushing’s syndrome. Science 344, 913–917 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Vaduva, P., Bonnet, F. & Bertherat, J. Molecular basis of primary aldosteronism and adrenal Cushing syndrome. J. Endocr. Soc. 4, bvaa075 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Perez-Rivas, L. G. et al. TP53 mutations in functional corticotroph tumors are linked to invasion and worse clinical outcome. Acta Neuropathol. Commun. 10, 139 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Kratz, C. P. et al. Analysis of the Li–Fraumeni spectrum based on an international germline TP53 variant data set: an international agency for research on cancer TP53 database analysis. JAMA Oncol. 7, 1800–1805 (2021).

    Article 
    PubMed 

    Google Scholar 

  • Warde, K. M. et al. Senescence-induced immune remodeling facilitates metastatic adrenal cancer in a sex-dimorphic manner. Nat. Aging 3, 846–865 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Del Valle, I. et al. An integrated single-cell analysis of human adrenal cortex development. JCI Insight 8, e168177 (2023).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Xing, Y., Morohashi, K. I., Ingraham, H. A. & Hammer, G. D. Timing of adrenal regression controlled by synergistic interaction between Sf1 SUMOylation and Dax1. Development 144, 3798–3807 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Spencer, S. J., Mesiano, S., Lee, J. Y. & Jaffe, R. B. Proliferation and apoptosis in the human adrenal cortex during the fetal and perinatal periods: implications for growth and remodeling. J. Clin. Endocrinol. Metab. 84, 1110–1115 (1999).

    CAS 
    PubMed 

    Google Scholar 

  • Niepoth, N. et al. Evolution of a novel adrenal cell type that promotes parental care. Nature 629, 1082–1090 (2024).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Dumontet, T. et al. Hormonal and spatial control of SUMOylation in the human and mouse adrenal cortex. FASEB J. 33, 10218–10230 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Heikkila, M. et al. Wnt-4 deficiency alters mouse adrenal cortex function, reducing aldosterone production. Endocrinology 143, 4358–4365 (2002).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Leng, S., Carlone, D. L., Guagliardo, N. A., Barrett, P. Q. & Breault, D. T. Rosette morphology in zona glomerulosa formation and function. Mol. Cell Endocrinol. 530, 111287 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Leng, S. et al. β-Catenin and FGFR2 regulate postnatal rosette-based adrenocortical morphogenesis. Nat. Commun. 11, 1680 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

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