Development of Adrenal Cortex Zonation

Endocrinology and Metabolism Clinics of North America

Volumn 44, Issue 2, 2015, Pages 243-274

  Xing, Yewei ^a   Lerario, Antonio M ^a   Rainey, William ^a   Hammer, Gary D ^b  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Adrenal cortex; Development; Steroidogenesis; Zonation

Indexed keywords

17 HYDROXYPREGNENOLONE; ALDOSTERONE; ANDROGEN; ANGIOTENSINOGEN; BETA CATENIN; CORTICOTROPIN; CORTICOTROPIN RELEASING FACTOR; CYTOCHROME P450 17; FIBRONECTIN; GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; HYDROCORTISONE; LAMININ; MELANOCORTIN 2 RECEPTOR; MESSENGER RNA; MINERALOCORTICOID; NUCLEAR RECEPTOR DAX 1; PRASTERONE; PROTEIN P53; SOMATOMEDIN B; SOMATOMEDIN C; SONIC HEDGEHOG PROTEIN; STEROID 17ALPHA MONOOXYGENASE; STEROIDOGENIC FACTOR 1; UROCORTIN I; UROCORTIN II; UROCORTIN III; WNT PROTEIN; WT1 PROTEIN;

ADRENAL BLOOD FLOW; ADRENAL CELL; ADRENAL CORTEX TUMOR; ADRENAL CORTEX ZONATION; ADRENAL HYPERPLASIA; ADRENAL HYPOPLASIA; ADRENAL INNERVATION; ADRENARCHE; ADRENOGONADAL PRIMORDIUM; ANATOMIC LANDMARK; CARCINOGENESIS; CELL DIFFERENTIATION; CHROMAFFIN CELL; DAX1 GENE; DEFINITIVE ZONE; EXTRACELLULAR MATRIX; FETAL ZONE FORMATION; FETUS DEVELOPMENT; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE MUTATION; HORMONE SYNTHESIS; HUMAN; HYPOPLASIA; INNERVATION; MESODERM; MOLECULAR DYNAMICS; NONHUMAN; ORGANOGENESIS; PATHOPHYSIOLOGY; POSTNATAL DEVELOPMENT; PRIMORDIUM; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PUBERTY; REGULATORY MECHANISM; REVIEW; SF1 GENE; SIGNAL TRANSDUCTION; STEM CELL; STEROIDOGENESIS; TELOMERE HOMEOSTASIS; WNT SIGNALING PATHWAY; ZONA FASCICULATA; ZONA GLOMERULOSA; ADRENAL CORTEX; EMBRYOLOGY; GROWTH, DEVELOPMENT AND AGING; METABOLISM; ZONA RETICULARIS;

ERINACEIDAE;

ADRENAL CORTEX; ANDROGENS; CELL DIFFERENTIATION; GLUCOCORTICOIDS; HEDGEHOG PROTEINS; HUMANS; MINERALOCORTICOIDS; PUBERTY; STEM CELLS; ZONA FASCICULATA; ZONA GLOMERULOSA; ZONA RETICULARIS;

EID: 84930332156     PISSN: 08898529     EISSN: 15584410     Source Type: Journal    
DOI: 10.1016/j.ecl.2015.02.001     Document Type: Review

References (216)

1. Gruenwald P. Embryonic and postnatal development of the adrenal cortex, particularly the zona glomerulosa and accessory nodules. Anat Rec 1946, 95:391-421.
2. Hatano O., Takakusu A., Nomura M., et al. Identical origin of adrenal cortex and gonad revealed by expression profiles of Ad4BP/SF-1. Genes Cells 1996, 1(7):663-671.
3. Luo X., Ikeda Y., Parker K.L. A cell-specific nuclear receptor is essential for adrenal and gonadal development and sexual differentiation. Cell 1994, 77(4):481-490.
4. Morohashi K. The ontogenesis of the steroidogenic tissues. Genes Cells 1997, 2(2):95-106.
5. Le Douarin N.M., Teillet M.A. Experimental analysis of the migration and differentiation of neuroblasts of the autonomic nervous system and of neurectodermal mesenchymal derivatives, using a biological cell marking technique. Dev Biol 1974, 41(1):162-184.
6. Doupe A.J., Landis S.C., Patterson P.H. Environmental influences in the development of neural crest derivatives: glucocorticoids, growth factors, and chromaffin cell plasticity. J Neurosci 1985, 5(8):2119-2142.
7. Hillarp N.A., Hokfelt B. Evidence of adrenaline and noradrenaline in separate adrenal medullary cells. Acta Physiol Scand 1953, 30(1):55-68.
8. Ce K., Hammer G.D. Recent insights into organogenesis of the adrenal cortex. Trends Endocrinol Metab 2002, 13(5):200-208.
9. Ehrhart-Bornstein M., Hinson J.P., Bornstein S.R., et al. Intraadrenal interactions in the regulation of adrenocortical steroidogenesis. Endocr Rev 1998, 19(2):101-143.
10. Seidl K., Unsicker K. The determination of the adrenal medullary cell fate during embryogenesis. Dev Biol 1989, 136(2):481-490.
11. Finotto S., Krieglstein K., Schober A., et al. Analysis of mice carrying targeted mutations of the glucocorticoid receptor gene argues against an essential role of glucocorticoid signalling for generating adrenal chromaffin cells. Development 1999, 126(13):2935-2944.
12. Gut P., Huber K., Lohr J., et al. Lack of an adrenal cortex in Sf1 mutant mice is compatible with the generation and differentiation of chromaffin cells. Development 2005, 132(20):4611-4619.
13. Bland M., Fowkes R.C., Ingraham H.A. Differential requirement for steroidogenic factor-1 gene dosage in adrenal development versus endocrine function. Mol Endocrinol 2004, 18(4):941-952.
14. Huber K., Combs S., Ernsberger U., et al. Generation of neuroendocrine chromaffin cells from sympathoadrenal progenitors: beyond the glucocorticoid hypothesis. Ann N Y Acad Sci 2002, 971:554-559.
15. Unsicker K., Huber K., Schutz G., et al. The chromaffin cell and its development. Neurochem Res 2005, 30(6-7):921-925.
16. Johannisson E. The foetal adrenal cortex in the human. Its ultrastructure at different stages of development and in different functional states. Acta Endocrinol (Copenh) 1968, 58(130):7.
17. Goto M., Piper Hanley K., Marcos J., et al. In humans, early cortisol biosynthesis provides a mechanism to safeguard female sexual development. J Clin Invest 2006, 116(4):953-960.
18. Hanley N.A., Rainey W.E., Wilson D.I., et al. Expression profiles of SF-1, DAX1, and CYP17 in the human fetal adrenal gland: potential interactions in gene regulation. Mol Endocrinol 2001, 15(1):57-68.
19. Achermann J.C., Meeks J.J., Jameson J.L. Phenotypic spectrum of mutations in DAX-1 and SF-1. Mol Cell Endocrinol 2001, 185(1-2):17-25.
20. El-Khairi R., Martinez-Aguayo A., Ferraz-de-Souza B., et al. Role of DAX-1 (NR0B1) and steroidogenic factor-1 (NR5A1) in human adrenal function. Endocr Dev 2011, 20:38-46.
21. Wong M., Ikeda Y., Luo X., et al. Steroidogenic factor 1 plays multiple roles in endocrine development and function. Recent Prog Horm Res 1997, 52:167-182.
22. Doghman M., Karpova T., Rodrigues G.A., et al. Increased steroidogenic factor-1 dosage triggers adrenocortical cell proliferation and cancer. Mol Endocrinol 2007, 21(12):2968-2987.
23. Val P., Martinez-Barbera J.P., Swain A. Adrenal development is initiated by Cited2 and Wt1 through modulation of Sf-1 dosage. Development 2007, 134(12):2349-2358.
24. Bandiera R., Vidal V.P., Motamedi F.J., et al. WT1 maintains adrenal-gonadal primordium identity and marks a population of AGP-like progenitors within the adrenal gland. Dev Cell 2013, 27(1):5-18.
25. Zubair M., Ishihara S., Oka S., et al. 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 2006, 26(11):4111-4121.
26. Zubair M., Parker K.L., Morohashi K.I. Developmental links between the fetal and adult zones of the adrenal cortex revealed by lineage tracing. Mol Cell Biol 2008, 28(23):7030-7040.
27. Ahmad I., Paterson W.F., Lin L., et al. A novel missense mutation in DAX-1 with an unusual presentation of X-linked adrenal hypoplasia congenita. Horm Res 2007, 68(1):32-37.
28. Mantovani G., De Menis E., Borretta G., et al. DAX1 and X-linked adrenal hypoplasia congenita: clinical and molecular analysis in five patients. Eur J Endocrinol 2006, 154(5):685-689.
29. Wood M., Hammer G.D. Adrenocortical stem and progenitor cells: unifying model of two proposed origins. Mol Cell Endocrinol 2011, 336(1-2):206-212.
30. Scheys J.O., Heaton J.H., Hammer G.D. Evidence of adrenal failure in aging Dax1-deficient mice. Endocrinology 2011, 152(9):3430-3439.
31. Gummow B.M., Scheys J.O., Cancelli V.R., et al. 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 2006, 20(11):2711-2723.
32. Kelly V.R., Hammer G.D. LRH-1 and Nanog regulate Dax1 transcription in mouse embryonic stem cells. Mol Cell Endocrinol 2011, 332(1-2):116-124.
33. Khalfallah O., Rouleau M., Barbry P., et al. Dax-1 knockdown in mouse embryonic stem cells induces loss of pluripotency and multilineage differentiation. Stem Cells 2009, 27(7):1529-1537.
34. Feek C.M., Marante D.J., Edwards C.R. The hypothalamic-pituitary-adrenal axis. Clin Endocrinol Metab 1983, 12(3):597-618.
35. Janes M., Chu K.M., Clark A.J., et al. Mechanisms of adrenocorticotropin-induced activation of extracellularly regulated kinase 1/2 mitogen-activated protein kinase in the human H295R adrenal cell line. Endocrinology 2008, 149(4):1898-1905.
36. Pepe G.J., Albrecht E.D. Regulation of the primate fetal adrenal cortex. Endocr Rev 1990, 11(1):151-176.
37. Rainey W., Rehman K.S., Carr B.R. Fetal and maternal adrenals in human pregnancy. Obstet Gynecol Clin North Am 2004, 31(4):817-835.
38. Beshay V., Carr B.R., Rainey W.E. The human fetal adrenal gland, corticotropin-releasing hormone, and parturition. Semin Reprod Med 2007, 25(1):14-20.
39. Hornsby P.J. Regulation of adrenocortical cell proliferation in culture. Endocr Res 1984, 10(3-4):259-281.
40. Simpson E.R., Waterman M.R. Regulation by ACTH of steroid hormone biosynthesis in the adrenal cortex. Can J Biochem Cell Biol 1983, 61(7):692-707.
41. LeRoith D., Roberts C.T. The insulin-like growth factor system and cancer. Cancer Lett 2003, 195(2):127-137.
42. Vale W., Spiess J., Rivier C., et al. Characterization of a 41-residue ovine hypothalamic peptide that stimulates secretion of corticotropin and beta-endorphin. Science 1981, 213(4514):1394-1397.
43. Spiess J., Rivier J., Rivier C., et al. Primary structure of corticotropin-releasing factor from ovine hypothalamus. Proc Natl Acad Sci U S A 1981, 78(10):6517-6521.
44. Takahashi K., Totsune K., Saruta M., et al. Expression of urocortin 3/stresscopin in human adrenal glands and adrenal tumors. Peptides 2006, 27(1):178-182.
45. Karteris E., Randeva H.S., Grammatopoulos D.K., et al. Expression and coupling characteristics of the CRH and orexin type 2 receptors in human fetal adrenals. J Clin Endocrinol Metab 2001, 86(9):4512-4519.
46. Fukuda T., Takahashi K., Suzuki T., et al. Urocortin 1, urocortin 3/stresscopin, and corticotropin-releasing factor receptors in human adrenal and its disorders. J Clin Endocrinol Metab 2005, 90(8):4671-4678.
47. Dermitzaki E., Tsatsanis C., Minas V., et al. Corticotropin-releasing factor (CRF) and the urocortins differentially regulate catecholamine secretion in human and rat adrenals, in a CRF receptor type-specific manner. Endocrinology 2007, 148(4):1524-1538.
48. Sirinanni R., Rehman K.S., Carr B.R., et al. Corticotropin-releasing hormone directly stimulates cortisol and the cortisol biosynthetic pathway in human fetal adrenal cells. J Clin Endocrinol Metab 2005, 90(1):279-285.
49. Andreis P.G., Neri G., Nussdorfer G.G. Corticotropin-releasing hormone (CRH) directly stimulates corticosterone secretion by the rat adrenal gland. Endocrinology 1991, 128(2):1198-1200.
50. Willenberg H.S., Bornstein S.R., Hiroi N., et al. Effects of a novel corticotropin-releasing-hormone receptor type I antagonist on human adrenal function. Mol Psychiatry 2000, 5(2):137-141.
51. Schwartz J., Huo J.S., Piwien-Pilipuk G. Growth hormone regulated gene expression. Minerva Endocrinol 2002, 27(4):231-241.
52. Backlin C., Rastad J., Skogseid B., et al. Immunohistochemical expression of insulin-like growth factor 1 and its receptor in normal and neoplastic human adrenal cortex. Anticancer Res 1995, 15(6B):2453-2459.
53. Brice A.L., Cheetham J.E., Bolton V.N., et al. Temporal changes in the expression of the insulin-like growth factor II gene associated with tissue maturation in the human fetus. Development 1989, 106(3):543-554.
54. Coulter C.L., Goldsmith P.C., Mesiano S., et al. Functional maturation of the primate fetal adrenal in vivo: I. Role of insulin-like growth factors (IGFs), IGF-I receptor, and IGF binding proteins in growth regulation. Endocrinology 1996, 137(10):4487-4498.
55. Bendall S.C., Stewart M.H., Menendez P., et al. IGF and FGF cooperatively establish the regulatory stem cell niche of pluripotent human cells in vitro. Nature 2007, 448(7157):1015-1021.
56. Jiang F., Frederick T.J., Wood T.L. IGF-I synergizes with FGF-2 to stimulate oligodendrocyte progenitor entry into the cell cycle. Dev Biol 2001, 232(2):414-423.
57. Pitetti J.L., Calvel P., Romero Y., et al. Insulin and IGF1 receptors are essential for XX and XY gonadal differentiation and adrenal development in mice. PLoS Genet 2013, 9(1):e1003160.
58. Morohashi K., Zubair M. The fetal and adult adrenal cortex. Mol Cell Endocrinol 2011, 336(1-2):193-197.
59. Zubair M., Oka S., Parker K.L., et al. Transgenic expression of Ad4BP/SF-1 in fetal adrenal progenitor cells leads to ectopic adrenal formation. Mol Endocrinol 2009, 23(10):1657-1667.
60. Schulte D., Shapiro I., Reincke M., et al. Expression and spatio-temporal distribution of differentiation and proliferation markers during mouse adrenal development. Gene Expr Patterns 2007, 7(1-2):72-81.
61. Guasti L., Paul A., Laufer E., et al. Localization of Sonic hedgehog secreting and receiving cells in the developing and adult rat adrenal cortex. Mol Cell Endocrinol 2011, 336(1-2):117-122.
62. King P., Paul A., Laufer E. Shh signaling regulates adrenocortical development and identifies progenitors of steroidogenic lineages. Proc Natl Acad Sci U S A 2009, 106(50):21185-21190.
63. Wood M.A., Acharya A., Finco I., et al. Fetal adrenal capsular cells serve as progenitor cells for steroidogenic and stromal adrenocortical cell lineages in M. musculus. Development 2013, 140(22):4522-4532.
64. Ishimoto H., Jaffe R.B. Development and function of the human fetal adrenal cortex: a key component in the feto-placental unit. Endocr Rev 2011, 32(3):317-355.
65. Havelock J., Auchus R.J., Rainey W.E. The rise in adrenal androgen biosynthesis: adrenarche. Semin Reprod Med 2004, 22(4):337-347.
66. Rosenfield R.L., Lucky A.W. Acne, hirsutism, and alopecia in adolescent girls. Clinical expressions of androgen excess. Endocrinol Metab Clin North Am 1993, 22(3):507-532.
67. Corvalan C., Uauy R., Mericq V. Obesity is positively associated with dehydroepiandrosterone sulfate concentrations at 7 y in Chilean children of normal birth weight. Am J Clin Nutr 2013, 97(2):318-325.
68. l'Allemand D., Schmidt S., Rousson V., et al. Associations between body mass, leptin, IGF-I and circulating adrenal androgens in children with obesity and premature adrenarche. Eur J Endocrinol 2002, 146(4):537-543.
69. Saenger P., Dimartino-Nardi J. Premature adrenarche. J Endocrinol Invest 2001, 24(9):724-733.
70. Pintor C., Loche S., Faedda A., et al. Adrenal androgens in obese boys before and after weight loss. Horm Metab Res 1984, 16(10):544-548.
71. Howard E. The effect of dietary factors on the adrenal X zone. Fed Proc 1947, 6(1 Pt 2):133.
72. Tanaka S., Matsuzawa A. What mouse contributed the first representation of the adrenal cortex X zone?. Jikken Dobutsu 1993, 42(3):305-316. [in Japanese].
73. Nishimoto K., Nakagawa K., Li D., et al. Adrenocortical zonation in humans under normal and pathological conditions. J Clin Endocrinol Metab 2010, 95(5):2296-2305.
74. Nakamura Y., Maekawa T., Felizola S.J., et al. Adrenal CYP11B1/2 expression in primary aldosteronism: immunohistochemical analysis using novel monoclonal antibodies. Mol Cell Endocrinol 2014, 392(1-2):73-79.
75. Gomez-Sanchez C.E., Qi X., Velarde-Miranda C., et al. Development of monoclonal antibodies against human CYP11B1 and CYP11B2. Mol Cell Endocrinol 2014, 383(1-2):111-117.
76. Chamoux E., Otis M., Gallo-Payet N. A connection between extracellular matrix and hormonal signals during the development of the human fetal adrenal gland. Braz J Med Biol Res 2005, 38(10):1495-1503.
77. Chamoux E., Narcy A., Lehoux J.G., et al. Fibronectin, laminin, and collagen IV as modulators of cell behavior during adrenal gland development in the human fetus. J Clin Endocrinol Metab 2002, 87(4):1819-1828.
78. Chamoux E., Bolduc L., Lehoux J.G., et al. Identification of extracellular matrix components and their integrin receptors in the human fetal adrenal gland. J Clin Endocrinol Metab 2001, 86(5):2090-2098.
79. Otis M., Campbell S., Payet M.D., et al. Expression of extracellular matrix proteins and integrins in rat adrenal gland: importance for ACTH-associated functions. J Endocrinol 2007, 193(3):331-347.
80. Cheng C.Y., Hornsby P.J. Expression of 11 beta-hydroxylase and 21-hydroxylase in long-term cultures of bovine adrenocortical cells requires extracellular matrix factors. Endocrinology 1992, 130(5):2883-2889.
81. Filippi L., Sardella B., Ciorra A., et al. Tumor thrombus in the renal vein from an adrenal metastasis of lung cancer: 18FDG PET/CT findings. Cancer Biother Radiopharm 2014, 29(5):189-192.
82. Puech A., Pages A., Comelade P. Cutaneous metastases as the first manifestation of a cancer of the lungs; adrenal metastasis; terminal acute adrenal insufficiency. Montp Med 1955, 47(6):565-566. [in French].
83. Onuigbo W.I. Lung cancer metastasis to adrenal cortical adenomas. J Pathol Bacteriol 1963, 86:541-543.
84. Lever J.D. Observations on the adrenal blood vessels in the rat. J Anat 1952, 86(4):459-467.
85. Anson B.J., Cauldwell E.W., Beaton L.E., et al. The blood supply of the kidney, suprarenal gland, and associated structures. Surg Gynecol Obstet 1947, 84(3):313-320.
86. Johnstone F.R. The suprarenal veins. Am J Surg 1957, 94(4):615-620.
87. Monkhouse W.S., Khalique A. The adrenal and renal veins of man and their connections with azygos and lumbar veins. J Anat 1986, 146:105-115.
88. Gagnon R. The venous drainage of the human adrenal gland. Rev Can Biol 1956, 14(4):350-359.
89. Engeland W.C. Functional innervation of the adrenal cortex by the splanchnic nerve. Horm Metab Res 1998, 30(6-7):311-314.
90. Hinson J.P., Cameron L.A., Purbrick A., et al. The role of neuropeptides in the regulation of adrenal vascular tone: effects of vasoactive intestinal polypeptide, substance P, neuropeptide Y, neurotensin, Met-enkephalin, and Leu-enkephalin on perfusion medium flow rate in the intact perfused rat adrenal. Regul Pept 1994, 51(1):55-61.
91. Li Q., Johansson H., Kjellman M., et al. Neuroendocrine differentiation and nerves in human adrenal cortex and cortical lesions. APMIS 1998, 106(8):807-817.
92. Burnay M.M., Python C.P., Vallotton M.B., et al. Role of the capacitative calcium influx in the activation of steroidogenesis by angiotensin-II in adrenal glomerulosa cells. Endocrinology 1994, 135(2):751-758.
93. Johnson B.B., Lieberman A.H., Mulrow P.J. Aldosterone excretion in normal subjects depleted of sodium and potassium. J Clin Invest 1957, 36(6 Part 1):757-766.
94. Laragh J.H., Stoerk H.C. A study of the mechanism of secretion of the sodium-retaining hormone (aldosterone). J Clin Invest 1957, 36(3):383-392.
95. McCaa R.E., Gillespie J.B. Effects of captopril and enalapril on sodium excretion and blood pressure in sodium-deficient dogs. Fed Proc 1984, 43(5):1336-1341.
96. Deane H.W., Bergner G.E. Chemical and cytochemical studies of the rat's adrenal cortex following the administration of pituitary adrenocorticotropic hormone (ACTH). J Clin Endocrinol Metab 1947, 7(6):457.
97. Hills A.G., Thorn G.W. An estimation of the quantity of 11-17-oxysteroid excretion by the human adrenal stimulated by ACTH. J Clin Endocrinol Metab 1948, 8(7):606.
98. Mason H.L., Power M.H., Rynearson E.H., et al. Results of administration of anterior pituitary adrenocorticotropic hormone to a normal human being. J Biol Chem 1947, 169(1):223.
99. Ingle D.J., Prestrud M.C., Li C.H. A further study of the essentiality of the adrenal cortex in mediating the metabolic effects of adrenocorticotrophic hormone. Endocrinology 1948, 43(4):202-207.
100. Bellamy D., Leonard R.A. The effect of cortisol on the activity of glutamate-pyruvate transaminase and the formation of glycogen and urea in starved rats. Biochem J 1964, 93(2):331-336.
101. Sie H.G., Hablanian A., Fishman W.H. Solubilization of mouse liver glycogen synthetase and phosphorylase during starvation glycogenolysis and its reversal by cortisol. Nature 1964, 201:393-394.
102. Bandy H.E., Darrach M., Newsom S.E., et al. Metabolism of adrenal steroids in the mouse. I. Observations on 20alpha-dihydrocorticosterone and corticosterone in the plasma of mice treated with corticotropin. Can J Biochem Physiol 1956, 34(5):913-918.
103. Halberg F., Albrecht P.G., Bittner J.J. Corticosterone rhythm of mouse adrenal in relation to serum corticosterone and sampling. Am J Physiol 1959, 197:1083-1085.
104. Halberg F., Haus E. Corticosterone in mouse adrenal in relation to sex and heterotopic pituitary isografting. Am J Physiol 1960, 199:859-862.
105. Ortega E., Rodriguez C., Strand L.J., et al. Effects of cloprednol and other corticosteroids on hypothalamic-pituitary-adrenal axis function. J Int Med Res 1976, 4(5):326-337.
106. Storrs F.J. Use and abuse of systemic corticosteroid therapy. J Am Acad Dermatol 1979, 1(2):95-106.
107. Conley A.J., Pattison J.C., Bird I.M. Variations in adrenal androgen production among (nonhuman) primates. Semin Reprod Med 2004, 22(4):311-326.
108. Davison B., Large D.M., Anderson D.C., et al. Basal steroid production by the zona reticularis of the guinea-pig adrenal cortex. J Steroid Biochem 1983, 18(3):285-290.
109. Hyatt P.J., Bhatt K., Tait J.F. Steroid biosynthesis by zona fasciculata and zona reticularis cells purified from the mammalian adrenal cortex. J Steroid Biochem 1983, 19(1C):953-959.
110. Kaufman F.R., Stanczyk F.Z., Matteri R.K., et al. Dehydroepiandrosterone and dehydroepiandrosterone sulfate metabolism in human genital skin. Fertil Steril 1990, 54(2):251-254.
111. Rosenfield R.L. Hirsutism and the variable response of the pilosebaceous unit to androgen. J Investig Dermatol Symp Proc 2005, 10(3):205-208.
112. Pelletier G. Expression of steroidogenic enzymes and sex-steroid receptors in human prostate. Best Pract Res Clin Endocrinol Metab 2008, 22(2):223-228.
113. Rege J., Nakamura Y., Satoh F., et al. Liquid chromatography-tandem mass spectrometry analysis of human adrenal vein 19-carbon steroids before and after ACTH stimulation. J Clin Endocrinol Metab 2013, 98(3):1182-1188.
114. Pabon J.E., Li X., Lei Z.M., et al. Novel presence of luteinizing hormone/chorionic gonadotropin receptors in human adrenal glands. J Clin Endocrinol Metab 1996, 81(6):2397-2400.
115. Jaffe R.B., Seron-Ferre M., Crickard K., et al. Regulation and function of the primate fetal adrenal gland and gonad. Recent Prog Horm Res 1981, 37:41-103.
116. Vuorenoja S., Rivero-Muller A., Kiiveri S., et al. Adrenocortical tumorigenesis, luteinizing hormone receptor and transcription factors GATA-4 and GATA-6. Mol Cell Endocrinol 2007, 269(1-2):38-45.
117. Lacroix A., Hamet P., Boutin J.M. Leuprolide acetate therapy in luteinizing hormone-dependent Cushing's syndrome. N Engl J Med 1999, 341(21):1577-1581.
118. Baker B.L. A comparison of the histological changes induced by experimental hyperadrenocorticalism and inanition. Recent Prog Horm Res 1952, 7:331.
119. Zwemer R.L., Wotton R.M., Norkus M.G. A study of corticoadrenal cells. Anat Rec 1938, 72(2):249-263.
120. Salmon T.N., Zwemer R.L. A study of the life history of cortico-adrenal gland cells of the rat by means of trypan blue injections. Anat Rec 1941, 80(4):421-429.
121. Malendowicz L.K., Dembinska M. Proliferation and distribution of adrenocortical cells in ACTH treated female hamsters. Folia Histochem Cytobiol 1990, 28(1-2):51-59.
122. Stachowiak A., Nussdorfer G.G., Malendowicz L.K. Proliferation and distribution of adrenocortical cells in the gland of ACTH- or dexamethasone-treated rats. Histol Histopathol 1990, 5(1):25-29.
123. Sasano H., Imatani A., Shizawa S., et al. Cell proliferation and apoptosis in normal and pathologic human adrenal. Mod Pathol 1995, 8(1):11-17.
124. Morley S.D., Viard I., Chung B.C., et al. Variegated expression of a mouse steroid 21-hydroxylase/beta- galactosidase transgene suggests centripetal migration of adrenocortical cells. Mol Endocrinol 1996, 10(5):585-598.
125. Ching S., Vilain E. Targeted disruption of Sonic Hedgehog in the mouse adrenal leads to adrenocortical hypoplasia. Genesis 2009, 47(9):628-637.
126. Huang C., Miyagawa S., Matsumaru D., et al. Progenitor cell expansion and organ size of mouse adrenal is regulated by sonic hedgehog. Endocrinology 2010, 151(3):1119-1128.
127. Alex K., Barlaskar F.M., Heaton J.H., et al. In search of adrenocortical stem and progenitor cells. Endocr Rev 2009, 30(3):241-263.
128. Kim A.C., Reuter A.L., Zubair M., et al. Targeted disruption of beta-catenin in Sf1-expressing cells impairs development and maintenance of the adrenal cortex. Development 2008, 135(15):2593-2602.
129. Berthon A., Sahut-Barnola I., Lambert-Langlais S., et al. Constitutive beta-catenin activation induces adrenal hyperplasia and promotes adrenal cancer development. Hum Mol Genet 2010, 19:1561-1576.
130. Assie G., Guillaud-Bataille M., Ragazzon B., et al. The pathophysiology, diagnosis and prognosis of adrenocortical tumors revisited by transcriptome analyses. Trends Endocrinol Metab 2010, 21(5):325-334.
131. Schteingart D.E., Doherty G.M., Gauger P.G., et al. Management of patients with adrenal cancer: recommendations of an international consensus conference. Endocr Relat Cancer 2005, 12(3):667-680.
132. Berthon A., Drelon C., Ragazzon B., et al. WNT/beta-catenin signalling is activated in aldosterone-producing adenomas and controls aldosterone production. Hum Mol Genet 2014, 23(4):889-905.
133. Mizusaki H., Kawabe K., Mukai T., et al. Dax-1 (dosage-sensitive sex reversal-adrenal hypoplasia congenita critical region on the X chromosome, gene 1) gene transcription is regulated by wnt4 in the female developing gonad. Mol Endocrinol 2003, 17(4):507-519.
134. Walczak E.M., Kuick R., Finco I., et al. Wnt signaling inhibits adrenal steroidogenesis by cell-autonomous and non-cell-autonomous mechanisms. Mol Endocrinol 2014, 28(9):1471-1486.
135. Freedman B.D., Kempna P.B., Carlone D.L., et al. Adrenocortical zonation results from lineage conversion of differentiated zona glomerulosa cells. Dev Cell 2013, 26(6):666-673.
136. Arboleda V.A., Lee H., Parnaik R., et al. Mutations in the PCNA-binding domain of CDKN1C cause IMAGe syndrome. Nat Genet 2012, 44:788-792.
137. Achermann J.C., Ito M., Hindmarsh P.C., et al. A mutation in the gene encoding steroidogenic factor-1 causes XY sex reversal and adrenal failure in humans. Nat Genet 1999, 22(2):125-126.
138. Habiby R.L., Boepple P., Nachtigall L., et al. Adrenal hypoplasia congenita with hypogonadotropic hypogonadism: evidence that DAX-1 mutations lead to combined hypothalmic and pituitary defects in gonadotropin production. J Clin Invest 1996, 98(4):1055-1062.
139. Mandel H., Shemer R., Borochowitz Z.U., et al. SERKAL syndrome: an autosomal-recessive disorder caused by a loss-of-function mutation in WNT4. Am J Hum Genet 2008, 82(1):39-47.
140. Clark A.J., McLoughlin L., Grossman A. Familial glucocorticoid deficiency associated with point mutation in the adrenocorticotropin receptor. Lancet 1993, 341(8843):461-462.
141. Gineau L., Cognet C., Kara N., et al. Partial MCM4 deficiency in patients with growth retardation, adrenal insufficiency, and natural killer cell deficiency. J Clin Invest 2012, 122(3):821-832.
142. Hughes C.R., Guasti L., Meimaridou E., et al. MCM4 mutation causes adrenal failure, short stature, and natural killer cell deficiency in humans. J Clin Invest 2012, 122(3):814-820.
143. Meimaridou E., Kowalczyk J., Guasti L., et al. Mutations in NNT encoding nicotinamide nucleotide transhydrogenase cause familial glucocorticoid deficiency. Nat Genet 2012, 44:740-742.
144. Jackson R.S., Creemers J.W., Farooqi I.S., et al. Small-intestinal dysfunction accompanies the complex endocrinopathy of human proprotein convertase 1 deficiency. J Clin Invest 2003, 112(10):1550-1560.
145. Krude H., Biebermann H., Luck W., et al. Severe early-onset obesity, adrenal insufficiency and red hair pigmentation caused by POMC mutations in humans. Nat Genet 1998, 19(2):155-157.
146. Dattani M.T., Martinez-Barbera J.P., Thomas P.Q., et al. Mutations in the homeobox gene HESX1/Hesx1 associated with septo-optic dysplasia in human and mouse. Nat Genet 1998, 19:125-133.
147. Wu W., Cogan J.D., Pfäffle R.W., et al. Mutations in PROP1 cause familial combined pituitary hormone deficiency. Nat Genet 1998, 18:147-149.
148. Wettstein M., Diez L.F., Twohig M., et al. The role of birth injury and the consequences of inadequately treated hypogonadism in longstanding panhypopituitarism. Conn Med 1996, 60(10):583-586.
149. Cohen L.E. Genetic disorders of the pituitary. Curr Opin Endocrinol Diabetes Obes 2012, 19(1):33-39.
150. Speiser P.W., Azziz R., Baskin L.S., et al. Congenital adrenal hyperplasia due to steroid 21-hydroxylase deficiency: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab 2010, 95(9):4133-4160.
151. Nimkarn S., New M.I. Prenatal diagnosis and treatment of congenital adrenal hyperplasia. Horm Res 2007, 67(2):53-60.
152. Nimkarn S., Lin-Su K., New M.I. Steroid 21 hydroxylase deficiency congenital adrenal hyperplasia. Pediatr Clin North Am 2011, 58(5):1281-1300.
153. Hauffa B., Hiort O. P450 side-chain cleavage deficiency-a rare cause of congenital adrenal hyperplasia. Endocr Dev 2011, 20:54-62.
154. Krone N., Arlt W. Genetics of congenital adrenal hyperplasia. Best Pract Res Clin Endocrinol Metab 2009, 23(2):181-192.
155. Lekarev O., Mallet D., Yuen T., et al. Congenital lipoid adrenal hyperplasia (a rare form of adrenal insufficiency and ambiguous genitalia) caused by a novel mutation of the steroidogenic acute regulatory protein gene. Eur J Pediatr 2012, 171(5):787-793.
156. Louiset E., Duparc C., Young J., et al. Intraadrenal corticotropin in bilateral macronodular adrenal hyperplasia. N Engl J Med 2013, 369(22):2115-2125.
157. Groussin L., Jullian E., Perlemoine K., et al. Mutations of the PRKAR1A gene in Cushing's syndrome due to sporadic primary pigmented nodular adrenocortical disease. J Clin Endocrinol Metab 2002, 87:4324-4329.
158. Lacroix A. ACTH-independent macronodular adrenal hyperplasia. Best Pract Res Clin Endocrinol Metab 2009, 23:245-259.
159. Ghayee H.K., Rege J., Watumull L.M., et al. Clinical, biochemical, and molecular characterization of macronodular adrenocortical hyperplasia of the zona reticularis: a new syndrome. J Clin Endocrinol Metab 2011, 96:E243-E250.
160. Hayashi Y., Takeda Y., Kaneko K., et al. A case of Cushing's syndrome due to ACTH-independent bilateral macronodular hyperplasia associated with excessive secretion of mineralocorticoids. Endocr J 1998, 45:485-491.
161. Lerario A.M., Moraitis A., Hammer G.D. Genetics and epigenetics of adrenocortical tumors. Mol Cell Endocrinol 2014, 386:67-84.
162. Espiard S., Ragazzon B., Bertherat J. Protein kinase A alterations in adrenocortical tumors. Horm Metab Res 2014, 8:8.
163. Grumbach M.M., Biller B.M., Braunstein G.D., et al. Management of the clinically inapparent adrenal mass ("incidentaloma"). Ann Intern Med 2003, 138:424-429.
164. Arnaldi G., Boscaro M. Adrenal incidentaloma. Best Pract Res Clin Endocrinol Metab 2012, 26:405-419.
165. Mulatero P., Stowasser M., Loh K.C., et al. Increased diagnosis of primary aldosteronism, including surgically correctable forms, in centers from five continents. J Clin Endocrinol Metab 2004, 89(3):1045-1050.
166. Fernandes-Rosa F.L., Williams T.A., Riester A., et al. Genetic spectrum and clinical correlates of somatic mutations in aldosterone-producing adenoma. Hypertension 2014, 64(2):354-361.
167. Choi M., Scholl U.I., Yue P., et al. K+ channel mutations in adrenal aldosterone-producing adenomas and hereditary hypertension. Science 2011, 331(6018):768-772.
168. Krapivinsky G., Gordon E.A., Wickman K., et al. The G-protein-gated atrial K+ channel IKACh is a heteromultimer of two inwardly rectifying K(+)-channel proteins. Nature 1995, 374(6518):135-141.
169. Monticone S., Hattangady N.G., Nishimoto K., et al. Effect of KCNJ5 mutations on gene expression in aldosterone-producing adenomas and adrenocortical cells. J Clin Endocrinol Metab 2012, 97(8):2011-3132.
170. Monticone S., Else T., Mulatero P., et al. Understanding primary aldosteronism: impact of next generation sequencing and expression profiling. Mol Cell Endocrinol 2015, 399:311-320.
171. Cao Y., He M., Gao Z., et al. Activating hotspot L205R mutation in PRKACA and adrenal Cushing's syndrome. Science 2014, 344:913-917.
172. Goh G., Scholl U.I., Healy J.M., et al. Recurrent activating mutation in PRKACA in cortisol-producing adrenal tumors. Nat Genet 2014, 46:613-617.
173. Sato Y., Maekawa S., Ishii R., et al. Recurrent somatic mutations underlie corticotropin-independent Cushing's syndrome. Science 2014, 344:917-920.
174. Kebebew E., Reiff E., Duh Q.Y., et al. Extent of disease at presentation and outcome for adrenocortical carcinoma: have we made progress?. World J Surg 2006, 30(5):872-878.
175. Kerkhofs T.M., Verhoeven R.H., Van der Zwan J.M., et al. Adrenocortical carcinoma: a population-based study on incidence and survival in the Netherlands since 1993. Eur J Cancer 2013, 49(11):2579-2586.
176. Abiven G., Coste J., Groussin L., et al. Clinical and biological features in the prognosis of adrenocortical cancer: poor outcome of cortisol-secreting tumors in a series of 202 consecutive patients. J Clin Endocrinol Metab 2006, 91:2650-2655.
177. Wajchenberg B.L., Albergaria Pereira M.A., Medonca B.B., et al. Adrenocortical carcinoma: clinical and laboratory observations. Cancer 2000, 88:711-736.
178. Fassnacht M., Allolio B. Clinical management of adrenocortical carcinoma. Best Pract Res Clin Endocrinol Metab 2009, 23:273-289.
179. Beuschlein F., Reincke M., Karl M., et al. Clonal composition of human adrenocortical neoplasms. Cancer Res 1994, 54:4927-4932.
180. Gicquel C., Leblond-Francillard M., Bertagna X., et al. Clonal analysis of human adrenocortical carcinomas and secreting adenomas. Clin Endocrinol 1994, 40:465-477.
181. Kartheuser A., Walon C., West S., et al. Familial adenomatous polyposis associated with multiple adrenal adenomas in a patient with a rare 3' APC mutation. J Med Genet 1999, 36:65-67.
182. Marshall W.H., Martin F.I., Mackay I.R. Gardner's syndrome with adrenal carcinoma. Australas Ann Med 1967, 16:242-244.
183. Kim W., Kim M., Jho E.H. Wnt/β-catenin signalling: from plasma membrane to nucleus. Biochem J 2013, 450:9-21.
184. Tissier F., Cavard C., Groussin L., et al. Mutations of beta-catenin in adrenocortical tumors: activation of the Wnt signaling pathway is a frequent event in both benign and malignant adrenocortical tumors. Cancer Res 2005, 65:7622-7627.
185. Tadjine M., Lampron A., Ouadi L., et al. Frequent mutations of beta-catenin gene in sporadic secreting adrenocortical adenomas. Clin Endocrinol 2008, 68:264-270.
186. Assié G., Letouzé E., Fassnacht M., et al. Integrated genomic characterization of adrenocortical carcinoma. Nat Genet 2014, 46:607-612.
187. Choufani S., Shuman C., Weksberg R. Beckwith-Wiedemann syndrome. Am J Med Genet C Semin Med Genet 2010, 154C:343-354.
188. Gicquel C., Bertagna X., Gaston V., et al. Molecular markers and long-term recurrences in a large cohort of patients with sporadic adrenocortical tumors. Cancer Res 2001, 61:6762-6767.
189. Giordano T.J., Kuick R., Else T., et al. Molecular classification and prognostication of adrenocortical tumors by transcriptome profiling. Clin Cancer Res 2009, 15:668-676.
190. Giordano T.J., Thomas D.G., Kuick R., et al. Distinct transcriptional profiles of adrenocortical tumors uncovered by DNA microarray analysis. Am J Pathol 2003, 162:521-531.
191. Gicquel C., Raffin-Sanson M.L., Gaston V., et al. Structural and functional abnormalities at 11p15 are associated with the malignant phenotype in sporadic adrenocortical tumors: study on a series of 82 tumors. J Clin Endocrinol Metab 1997, 82:2559-2565.
192. Weber M.M., Fottner C., Schmidt P., et al. Postnatal overexpression of insulin-like growth factor II in transgenic mice is associated with adrenocortical hyperplasia and enhanced steroidogenesis. Endocrinology 1999, 140:1537-1543.
193. Heaton J.H., Wood M.A., Kim A.C., et al. Progression to adrenocortical tumorigenesis in mice and humans through insulin-like growth factor 2 and beta-catenin. Am J Pathol 2012, 181(3):1017-1033.
194. Almeida M.Q., Fragoso M.C., Lotfi C.F., et al. Expression of insulin-like growth factor-II and its receptor in pediatric and adult adrenocortical tumors. J Clin Endocrinol Metab 2008, 93:3524-3531.
195. Barlaskar F.M., Spalding A.C., Heaton J.H., et al. Preclinical targeting of the type I insulin-like growth factor receptor in adrenocortical carcinoma. J Clin Endocrinol Metab 2009, 94:204-212.
196. Haluska P., Worden F., Olmos D., et al. Safety, tolerability, and pharmacokinetics of the anti-IGF-1R monoclonal antibody figitumumab in patients with refractory adrenocortical carcinoma. Cancer Chemother Pharmacol 2010, 65:765-773.
197. Lerario A.M., Worden F.P., Ramm C.A., et al. The combination of insulin-like growth factor receptor 1 (IGF1R) antibody cixutumumab and mitotane as a first-line therapy for patients with recurrent/metastatic adrenocortical carcinoma: a multi-institutional NCI-sponsored trial. Horm Cancer 2014, 5:232-239.
198. Naing A., Lorusso P., Fu S., et al. Insulin growth factor receptor (IGF-1R) antibody cixutumumab combined with the mTOR inhibitor temsirolimus in patients with metastatic adrenocortical carcinoma. Br J Cancer 2013, 108:826-830.
199. Li F.P., Fraumeni J.F., Mulvihill J.J., et al. A cancer family syndrome in twenty-four kindreds. Cancer Res 1988, 48:5358-5362.
200. Bougeard G., Sesboüé R., Baert-Desurmont S., et al. Molecular basis of the Li-Fraumeni syndrome: an update from the French LFS families. J Med Genet 2008, 45(8):535-538.
201. Libè R., Groussin L., Tissier F., et al. Somatic TP53 mutations are relatively rare among adrenocortical cancers with the frequent 17p13 loss of heterozygosity. Clin Cancer Res 2007, 13:844-850.
202. Waldmann J., Patsalis N., Fendrich V., et al. Clinical impact of TP53 alterations in adrenocortical carcinomas. Langenbecks Arch Surg 2012, 397:209-216.
203. Herrmann L.J., Heinze B., Fassnacht M., et al. TP53 germline mutations in adult patients with adrenocortical carcinoma. J Clin Endocrinol Metab 2012, 97:E476-E485.
204. Raymond V.M., Else T., Everett J.N., et al. Prevalence of germline TP53 mutations in a prospective series of unselected patients with adrenocortical carcinoma. J Clin Endocrinol Metab 2013, 98:E119-E125.
205. Ribeiro R.C., Sandrini F., Figueiredo B., et al. An inherited p53 mutation that contributes in a tissue-specific manner to pediatric adrenal cortical carcinoma. Proc Natl Acad Sci U S A 2001, 98:9330-9335.
206. Varley J.M., McGown G., Thorncroft M., et al. Are there low-penetrance TP53 Alleles? evidence from childhood adrenocortical tumors. Am J Hum Genet 1999, 65:995-1006.
207. Wagner J., Portwine C., Rabin K., et al. High frequency of germline p53 mutations in childhood adrenocortical cancer. J Natl Cancer Inst 1994, 86:1707-1710.
208. Choudhary B., Karande A.A., Raghavan S.C. Telomere and telomerase in stem cells: relevance in ageing and disease. Front Biosci 2012, 4:16-30.
209. Ju Z., Rudolph K.L. Telomeres and telomerase in stem cells during aging and disease. Genome Dyn 2006, 1:84-103.
210. Kim N.W., Piatyszek M.A., Prowse K.R., et al. Specific association of human telomerase activity with immortal cells and cancer. Science 1994, 266:2011-2015.
211. Keegan C.E., Hutz J.E., Else T., et al. Urogenital and caudal dysgenesis in adrenocortical dysplasia (acd) mice is caused by a splicing mutation in a novel telomeric regulator. Hum Mol Genet 2005, 14:113-123.
212. Else T., Trovato A., Kim A.C., et al. Genetic p53 deficiency partially rescues the adrenocortical dysplasia phenotype at the expense of increased tumorigenesis. Cancer Cell 2009, 15(6):465-476.
213. Shackleton M., Quintana E., Fearon E.R., et al. Heterogeneity in cancer: cancer stem cells versus clonal evolution. Cell 2009, 138:822-829.
214. Gupta P.B., Fillmore C.M., Jiang G., et al. Stochastic state transitions give rise to phenotypic equilibrium in populations of cancer cells. Cell 2011, 146:633-644.
215. Welte Y., Adjaye J., Lehrach H.R., et al. Cancer stem cells in solid tumors: elusive or illusive? Cell communication and signaling. Cell Commun Signal 2010, 8:6.
216. Lichtenauer U.D., Shapiro I., Geiger K., et al. Side population does not define stem cell-like cancer cells in the adrenocortical carcinoma cell line NCI h295R. Endocrinology 2008, 149(3):1314-1322.