Transcriptome profiling reveals differentially expressed transcripts between the human adrenal zona fasciculata and zona reticularis

Journal of Clinical Endocrinology and Metabolism

Volumn 99, Issue 3, 2014, Pages

  Rege, Juilee ^a,b   Nakamura, Yasuhiro ^c   Wang, Tao ^b   Merchen, Todd D ^b   Sasano, Hironobu ^c   Rainey, William E ^a,b  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b MEDICAL COLLEGE OF GEORGIA   (United States)

^c TOHOKU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

3(OR 17)BETA HYDROXYSTEROID DEHYDROGENASE; CYTOCHROME B5; FATTY ACID TRANSPORTER; LYMPHOID ENHANCER FACTOR 1; NEPHROBLASTOMA OVEREXPRESSED PROTEIN; RNA; SOLUTE CARRIER FAMILY 27; SULFOTRANSFERASE; TESTOSTERONE 17BETA DEHYDROGENASE; TETRASPANIN 12; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ADRENAL CORTEX; ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MICROARRAY ANALYSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; STEROIDOGENESIS; UPREGULATION; ZONA FASCICULATA;

ADULT; COENZYME A LIGASES; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; IMMUNOHISTOCHEMISTRY; METABOLIC NETWORKS AND PATHWAYS; MICROARRAY ANALYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TETRASPANINS; ZONA FASCICULATA; ZONA RETICULARIS;

EID: 84895779531     PISSN: 0021972X     EISSN: 19457197     Source Type: Journal    
DOI: 10.1210/jc.2013-3198     Document Type: Article

References (78)

1. Arnold J. Ein beitrag zu der feiner struktur und dem chemismus der nebennieren. Virchows Arch. 1866;35:64-107.
2. Vinson GP. Adrenocortical zonation and ACTH. Microsc Res Tech. 2003;61:227-239. (Pubitemid 36621433)
3. Vinson GP, Ho MM. Origins of zonation: the adrenocortical model of tissue development and differentiation. Clin Exp Pharmacol Physiol Suppl. 1998;25:S91-S96. (Pubitemid 28498856)
4. Hornsby PJ. Biosynthesis of DHEA(S) by the human adrenal cortex and its age-related decline. Ann NY Acad Sci. 1995;774:29-46. (Pubitemid 26140358)
5. Parker LN, Odell WD. Control of adrenal androgen secretion. Endocr Rev. 1980;1:392-410.
6. Wang W, Yang L, Suwa T, Casson PR, Hornsby PJ. Differentially expressed genes in zona reticularis cells of the human adrenal cortex. Mol Cell Endocrinol. 2001;173:127-134. (Pubitemid 32149638)
7. Cutler GB Jr, Loriaux DL. Andrenarche and its relationship to the onset of puberty. Fed Proc. 1980;39:2384-2390.
8. Miller WL. Androgen synthesis in adrenarche. Rev Endocr Metab Disord. 2009;10:3-17.
9. Labrie F. Intracrinology. Mol Cell Endocrinol. 1991;78:C113-C118.
10. Aiba M, Fujibayashi M. Alteration of subcapsular adrenocortical zonation in humans with aging: the progenitor zone predominates over the previously well-developed zona glomerulosa after 40 years of age. J Histochem Cytochem. 2011;59:557-564.
11. Domalik LJ, Chaplin DD, Kirkman MS, et al. Different isozymes of mouse 11β-hydroxylase produce mineralocorticoids and glucocorticoids. Mol Endocrinol. 1991;5:1853-1861.
12. Gell JS, Carr BR, Sasano H, et al. Adrenarche results from development of a 3β-hydroxysteroid dehydrogenase-deficient adrenal reticularis. J Clin Endocrinol Metab. 1998;83:3695-3701. (Pubitemid 28500911)
13. Nishimoto K, Nakagawa K, Li D, et al. Adrenocortical zonation in humans under normal and pathological conditions. J Clin Endocrinol Metab. 2010;95:2296-2305.
14. Suzuki T, Sasano H, Takeyama J, et al. Developmental changes in steroidogenic enzymes in human postnatal adrenal cortex: immunohistochemical studies. Clin Endocrinol (Oxf). 2000;53:739-747. (Pubitemid 32096686)
15. Brock BJ, Waterman MR. Biochemical differences between rat and human cytochrome P450c17 support the different steroidogenic needs of these two species. Biochemistry. 1999;38:1598-1606.
16. Miller WL. Early steps in androgen biosynthesis: from cholesterol to DHEA. Baillieres Clin Endocrinol Metab. 1998;12:67-81. (Pubitemid 28495390)
17. Nakamura Y, Gang HX, Suzuki T, Sasano H, Rainey WE. Adrenal changes associated with adrenarche. Rev Endocr Metab Disord. 2009;10:19-26.
18. Endoh A, Kristiansen SB, Casson PR, Buster JE, Hornsby PJ. The zona reticularis is the site of biosynthesis of dehydroepiandrosterone and dehydroepiandrosterone sulfate in the adult human adrenal cortex resulting from its low expression of 3β-hydroxysteroid dehydrogenase. J Clin Endocrinol Metab. 1996;81:3558-3565. (Pubitemid 26339915)
19. Sasano H, Mori T, Sasano N, Nagura H, Mason JI. Immunolocalization of 3β-hydroxysteroid dehydrogenase in human ovary. J Reprod Fertil. 1990;89:743-751. (Pubitemid 20238693)
20. Conley AJ, Bird IM. The role of cytochrome P450 17α-hydroxylase and 3β-hydroxysteroid dehydrogenase in the integration of gonadal and adrenal steroidogenesis via the δ5 and δ4 pathways of steroidogenesis in mammals. Biol Reprod. 1997;56:789-799. (Pubitemid 27150405)
21. Rainey WE, Carr BR, Sasano H, Suzuki T, Mason JI. Dissecting human adrenal androgen production. Trends Endocrinol Metab. 2002;13:234-239. (Pubitemid 36733967)
22. Nakamura Y, Hornsby PJ, Casson P, et al. Type 5 17β-hydroxysteroid dehydrogenase (AKR1C3) contributes to testosterone production in the adrenal reticularis. J Clin Endocrinol Metab. 2009;94:2192-2198.
23. 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;98:1182-1188.
24. Wang T, Satoh F, Morimoto R, et al. Gene expression profiles in aldosterone-producing adenomas and adjacent adrenal glands. Eur J Endocrinol. 2011;164:613-619.
25. Nakamura Y, Felizola SJ, Kurotaki Y, et al. Cyclin D1 (CCND1) expression is involved in estrogen receptor β (ERβ) in human prostate cancer. Prostate. 2013;73:590-595.
26. Strott CA. Sulfonation and molecular action. Endocr Rev. 2002;23:703-732. (Pubitemid 35203256)
27. Belloni AS, Mazzocchi G, Mantero F, Nussdorfer GG. The human adrenal cortex: ultrastructure and base-line morphometric data. J Submicrosc Cytol. 1987;19:657-668.
28. Raffalli-Mathieu F, Mannervik B. Human glutathione transferase A3-3 active as steroid double-bond isomerase. Methods Enzymol. 2005;401:265-278. (Pubitemid 43052398)
29. Neville AM, O'Hare MJ. The Human Adrenal Cortex. Berlin: Springer Verlag; 1981.
30. Raffalli-Mathieu F, Orre C, Stridsberg M, Hansson Edalat M, Mannervik B. Targeting human glutathione transferase A3-3 attenuates progesterone production in human steroidogenic cells. Biochem J. 2008;414:103-109.
31. Gimeno RE. Fatty acid transport proteins. Curr Opin Lipidol. 2007;18:271-276. (Pubitemid 46743050)
32. Melton EM, Cerny RL, Watkins PA, DiRusso CC, Black PN. Human fatty acid transport protein 2a/very long chain acyl-CoA synthetase 1 (FATP2a/Acsvl1) has a preference in mediating the channeling of exogenous n-3 fatty acids into phosphatidylinositol. J Biol Chem. 2011;286:30670-30679.
33. Melton EM, Cerny RL, Dirusso CC, Black PN. Overexpression of human fatty acid transport protein 2/very long chain acyl-CoA synthetase 1 (FATP2/Acsvl1) reveals distinct patterns of trafficking of exogenous fatty acids. Biochem Biophys Res Commun. 2013;440:743-748.
34. Pignatelli D, Ferreira J, Vendeira P, Magalhaes MC, Vinson GP. Proliferation of capsular stem cells induced by ACTH in the rat adrenal cortex. Endocr Res. 2002;28:683-691. (Pubitemid 36042537)
35. 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. 1986;111:477-482. (Pubitemid 17207239)
36. Parker CR Jr, Mixon RL, Brissie RM, Grizzle WE. Aging alters zonation in the adrenal cortex of men. J Clin Endocrinol Metab. 1997;82:3898-3901. (Pubitemid 27509391)
37. Staton BA, Mixon RL, Dharia S, Brissie RM, Parker CR Jr. Is reduced cell size the mechanism for shrinkage of the adrenal zona reticularis in aging? Endocr Res. 2004;30:529-534. (Pubitemid 40070125)
38. Hui XG, Akahira J, Suzuki T, et al. Development of the human adrenal zona reticularis: morphometric and immunohistochemical studies from birth to adolescence. J Endocrinol. 2009;203:241-252.
39. Sasano H, Imatani A, Shizawa S, Suzuki T, Nagura H. Cell proliferation and apoptosis in normal and pathologic human adrenal. Mod Pathol. 1995;8:11-17.
40. Berthon A, Martinez A, Bertherat J, Val P. Wnt/β-catenin signalling in adrenal physiology and tumour development. Mol Cell Endocrinol. 2012;351:87-95.
41. El Wakil A, Lalli E. The Wnt/β-catenin pathway in adrenocortical development and cancer. Mol Cell Endocrinol. 2011;332:32-37.
42. Heikkila M, Peltoketo H, Leppaluoto J, Ilves M, Vuolteenaho O, Vainio S. Wnt-4 deficiency alters mouse adrenal cortex function, reducing aldosterone production. Endocrinology. 2002;143:4358-4365. (Pubitemid 35239569)
43. Kim AC, Reuter AL, Zubair M, et al. Targeted disruption of β-catenin in Sf1-expressing cells impairs development and maintenance of the adrenal cortex. Development. 2008;135:2593-2602.
44. Suwa T, Chen M, Hawks CL, Hornsby PJ. Zonal expression of dickkopf-3 and components of the Wnt signalling pathways in the human adrenal cortex. J Endocrinol. 2003;178:149-158. (Pubitemid 36927019)
45. Boulkroun S, Samson-Couterie B, Golib-Dzib JF, et al. Aldosterone-producing adenoma formation in the adrenal cortex involves expression of stem/progenitor cell markers. Endocrinology. 2011;152:4753-4763.
46. Giordano TJ, Kuick R, Else T, et al. Molecular classification and prognostication of adrenocortical tumors by transcriptome profiling. Clin Cancer Res. 2009;15:668-676.
47. He TC, Sparks AB, Rago C, et al. Identification of c-MYC as a target of the APC pathway. Science. 1998;281:1509-1512. (Pubitemid 28425575)
48. Tetsu O, McCormick F. β-Catenin regulates expression of cyclinD1 in colon carcinoma cells. Nature. 1999;398:422-426. (Pubitemid 29180374)
49. Yan Y, Tang D, Chen M, et al. Axin2 controls bone remodeling through the β-catenin-BMP signaling pathway in adult mice. J Cell Sci. 2009;122:3566-3578.
50. Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P. Molecular Biology of the Cell. 5th ed. New York: Garland Science, Taylor, Francis Group; 2008.
51. Else T. Telomeres and telomerase in adrenocortical tissue maintenance, carcinogenesis, and aging. J Mol Endocrinol. 2009;43:131-141.
52. Vlangos CN, O'Connor BC, Morley MJ, Krause AS, Osawa GA, Keegan CE. Caudal regression in adrenocortical dysplasia (acd) mice is caused by telomere dysfunction with subsequent p53-dependent apoptosis. Dev Biol. 2009;334:418-428.
53. Wood MA, Hammer GD. Adrenocortical stem and progenitor cells: unifying model of two proposed origins. Mol Cell Endocrinol. 2011;336:206-212.
54. de Lange T. Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev. 2005;19:2100-2110.
55. Junge HJ, Yang S, Burton JB, et al. TSPAN12 regulates retinal vascular development by promoting Norrin- but not Wnt-induced FZD4/β-catenin signaling. Cell. 2009;139:299-311.
56. Knoblich K, Wang HX, Sharma C, Fletcher AL, Turley SJ, Hemler ME. Tetraspanin TSPAN12 regulates tumor growth and metastasis and inhibits β-catenin degradation [published online August 18, 2013]. Cell Mol Life Sci. doi:10.1007/s00018-013-1444-8.
57. Ratcliffe J, Nakanishi M, Jaffe RB. Identification of definitive and fetal zone markers in the human fetal adrenal gland reveals putative developmental genes. J Clin Endocrinol Metab. 2003;88:3272-3277. (Pubitemid 36877504)
58. Doghman M, Arhatte M, Thibout H, et al. Nephroblastoma overexpressed/cysteine-rich protein 61/connective tissue growth factor/nephroblastoma overexpressed gene-3 (NOV/CCN3), a selective adrenocortical cell proapoptotic factor, is down-regulated in childhood adrenocortical tumors. J Clin Endocrinol Metab. 2007;92:3253-3260. (Pubitemid 47236400)
59. Hoerr N. The cells of the suprarenal cortex in the guinea pig. Am J Anat. 1931;48:139-197.
60. Nussdorfer GG. Cytophysiology of the adrenal cortex. Int Rev Cytol. 1986;98:1-405.
61. Wolkersdorfer GW, Ehrhart-Bornstein M, Brauer S, Marx C, Scherbaum WA, Bornstein SR. Differential regulation of apoptosis in the normal human adrenal gland. J Clin Endocrinol Metab. 1996;81:4129-4136. (Pubitemid 26380428)
62. Kacsoh B. Endocrine Physiology. New York: McGraw-Hill; 2000.
63. Kawaoi A. Ultrastructural zonation of the human adrenal cortex. Acta Pathol Jpn. 1969;19:115-149.
64. Sucheston ME, Cannon MS. Development of zonular patterns in the human adrenal gland. J Morphol. 1968;126:477-491.
65. Hornsby PJ. Aging of the human adrenal cortex. Sci Aging Knowledge Environ. 2004;2004:re6.
66. Khoury EL, Greenspan JS, Greenspan FS. Adrenocortical cells of the zona reticularis normally express HLA-DR antigenic determinants. Am J Pathol. 1987;127:580-591. (Pubitemid 17089819)
67. Marx C, Bornstein SR, Wolkersdorfer GW, Peter M, Sippell WG, Scherbaum WA. Relevance of major histocompatibility complex class II expression as a hallmark for the cellular differentiation in the human adrenal cortex. J Clin Endocrinol Metab. 1997;82:3136-3140. (Pubitemid 27385688)
68. Dharia S, Parker CR Jr. Adrenal androgens and aging. Semin Reprod Med. 2004;22:361-368. (Pubitemid 40030085)
69. Lebrethon MC, Jaillard C, Naville D, Begeot M, Saez JM. Effects of transforming growth factor-β1 on human adrenocortical fasciculata- reticularis cell differentiated functions. J Clin Endocrinol Metab. 1994;79:1033-1039. (Pubitemid 24342243)
70. Ehrhart-Bornstein M, Bornstein SR, Scherbaum WA. Sympathoadrenal system and immune system in the regulation of adrenocortical function. Eur J Endocrinol. 1996;135:19-26. (Pubitemid 26232700)
71. Hayashi Y, Hiyoshi T, Takemura T, Kurashima C, Hirokawa K. Focal lymphocytic infiltration in the adrenal cortex of the elderly: immunohistological analysis of infiltrating lymphocytes. Clin Exp Immunol. 1989;77:101-105. (Pubitemid 19198821)
72. Medema RH, Kops GJ, Bos JL, Burgering BM. AFX-like Forkhead transcription factors mediate cell-cycle regulation by Ras and PKB through p27kip1. Nature. 2000;404:782-787. (Pubitemid 30212408)
73. Vilchez D, Boyer L, Morantte I, et al. Increased proteasome activity in human embryonic stem cells is regulated by PSMD11. Nature. 2012;489:304-308.
74. Setsuie R, Wada K. The functions of UCH-L1 and its relation to neurodegenerative diseases. Neurochem Int. 2007;51:105-111. (Pubitemid 47179898)
75. Lichter DI, Danaee H, Pickard MD, et al. Sequence analysis of β-subunit genes of the 20S proteasome in patients with relapsed multiple myeloma treated with bortezomib or dexamethasone. Blood. 2012;120:4513-4516.
76. Ludwig S, Klitzsch A, Baniahmad A. The ING tumor suppressors in cellular senescence and chromatin. Cell Biosci. 2011;1:25.
77. Eskelinen EL, Illert AL, Tanaka Y, et al. Role of LAMP-2 in lysosome biogenesis and autophagy. Mol Biol Cell. 2002;13:3355-3368. (Pubitemid 35034269)
78. Wiley SR, Schooley K, Smolak PJ, et al. Identification and characterization of a new member of the TNF family that induces apoptosis. Immunity. 1995;3:673-682. (Pubitemid 26091143)