Cushing's syndrome and fetal features resurgence in adrenal cortex-specific Prkar1a knockout mice

PLoS Genetics

Volumn 6, Issue 6, 2010, Pages 1-16

  Sahut Barnola, Isabelle ^a   de Joussineau, Cyrille ^a   Val, Pierre ^a   Lambert Langlais, Sarah ^a   Damon, Christelle ^a   Lefrançois Martinez, Anne Marie ^a   Pointud, Jean Christophe ^a   Marceau, Geoffroy ^a,b   Sapin, Vincent ^a,b   Tissier, Frédérique ^c   Ragazzon, Bruno ^c   Bertherat, Jérôme ^c   Kirschner, Lawrence S ^d   Stratakis, Constantine A ^e   Martinez, Antoine ^a  

^a UNIVERSITÉ CLERMONT AUVERGNE   (France)

^b SERVICE DE RHUMATOLOGIE   (France)

^c INSERM   (France)

^d OHIO STATE UNIVERSITY   (United States)

^e EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE REGULATORY SUBUNIT IALPHA; HYDROCORTISONE; CORTICOTROPIN; PRKAR1A PROTEIN, MOUSE; STEROID 17ALPHA MONOOXYGENASE;

ADRENAL CORTEX; ADRENAL CORTEX CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL EXPANSION; CELL PROLIFERATION; CONTROLLED STUDY; CUSHING SYNDROME; ENZYME ACTIVITY; FEMALE; GENE EXPRESSION; HUMAN; HUMAN TISSUE; IN VIVO STUDY; KNOCKOUT MOUSE; MALE; MOUSE; NONHUMAN; PATHOGENESIS; STEROIDOGENESIS; ANIMAL; GENETICS; METABOLISM; MOUSE MUTANT; PATHOLOGY; PRENATAL DEVELOPMENT; SIGNAL TRANSDUCTION;

MUS;

ADRENAL CORTEX; ADRENOCORTICOTROPIC HORMONE; ANIMALS; CELL PROLIFERATION; CUSHING SYNDROME; CYCLIC AMP-DEPENDENT PROTEIN KINASE RIALPHA SUBUNIT; CYCLIC AMP-DEPENDENT PROTEIN KINASES; FEMALE; HUMANS; MALE; MICE; MICE, KNOCKOUT; SIGNAL TRANSDUCTION; STEROID 17-ALPHA-HYDROXYLASE;

EID: 77954152314     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1000980     Document Type: Article

References (61)

1. Carney JA, Gordon H, Carpenter PC, Shenoy BV, Go VL (1985) The complex of myxomas, spotty pigmentation, and endocrine overactivity. Medicine (Baltimore) 64: 270-283
2. Kirschner LS, Carney JA, Pack SD, Taymans SE, Giatzakis C, et al. (2000) Mutations of the gene encoding the protein kinase A type I-alpha regulatory subunit in patients with the Carney complex. Nat Genet 26: 89-92
3. Casey M, Vaughan CJ, He J, Hatcher CJ, Winter JM, et al. (2000) Mutations in the protein kinase A R1alpha regulatory subunit cause familial cardiac myxomas and Carney complex. J Clin Invest 106: R31-38
4. Groussin L, Jullian E, Perlemoine K, Louvel A, Leheup B, et al. (2002) Mutations of the PRKAR1A gene in Cushing's syndrome due to sporadic primary pigmented nodular adrenocortical disease. J Clin Endocrinol Metab 87: 4324-4329
5. Amieux PS, Howe DG, Knickerbocker H, Lee DC, Su T, et al. (2002) Increased basal cAMP-dependent protein kinase activity inhibits the formation of mesoderm-derived structures in the developing mouse embryo. J Biol Chem 277: 27294-27304
6. Kirschner LS, Kusewitt DF, Matyakhina L, Towns WH, 2nd, Carney JA, et al. (2005) A mouse model for the Carney complex tumor syndrome develops neoplasia in cyclic AMP-responsive tissues. Cancer Res 65: 4506-4514
7. Veugelers M, Wilkes D, Burton K, McDermott DA, Song Y, et al. (2004) Comparative PRKAR1A genotype-phenotype analyses in humans with Carney complex and prkar1a haploinsufficient mice. Proc Natl Acad Sci U S A 101: 14222-14227
8. Griffin KJ, Kirschner LS, Matyakhina L, Stergiopoulos SG, Robinson-White A, et al. (2004) A transgenic mouse bearing an antisense construct of regulatory subunit type 1A of protein kinase A develops endocrine and other tumours: comparison with Carney complex and other PRKAR1A induced lesions. J Med Genet 41: 923-931
9. Yin Z, Jones GN, Towns WH, 2nd, Zhang X, Abel ED, et al. (2008) Heart- specific ablation of Prkar1a causes failure of heart development and myxomagenesis. Circulation 117: 1414-1422
10. Yin Z, Williams-Simons L, Parlow AF, Asa S, Kirschner LS (2008) Pituitary- specific knockout of the Carney complex gene Prkar1a leads to pituitary tumorigenesis. Mol Endocrinol 22: 380-387
11. Jones GN, Tep C, Towns WH, 2nd, Mihai G, Tonks ID, et al. (2008) Tissue- specific ablation of Prkar1a causes schwannomas by suppressing neurofibroma- tosis protein production. Neoplasia 10: 1213-1221
12. Bertherat J, Horvath A, Groussin L, Grabar S, Boikos S, et al. (2009) Mutations in regulatory subunit type 1A of cyclic AMP-dependent protein kinase (PRKAR1A): phenotype analysis in 353 patients and 80 different genotypes. J Clin Endocrinol Metab.
13. Lambert-Langlais S, Val P, Guyot S, Ragazzon B, Sahut-Barnola I, et al. (2009) A transgenic mouse line with specific Cre recombinase expression in the adrenal cortex. Mol Cell Endocrinol 300: 197-204
14. Kim AC, Hammer GD (2007) Adrenocortical cells with stem/progenitor cell properties: recent advances. Mol Cell Endocrinol 265-266: 10-16
15. Parviainen H, Kiiveri S, Bielinska M, Rahman N, Huhtaniemi IT, et al. (2007) GATA transcription factors in adrenal development and tumors. Mol Cell Endocrinol 265-266: 17-22
16. King P, Paul A, Laufer E (2009) Shh signaling regulates adrenocortical development and identifies progenitors of steroidogenic lineages. Proc Natl Acad Sci U S A 106: 21185-21190
17. Kim AC, Barlaskar FM, Heaton JH, Else T, Kelly VR, et al. (2009) In search of adrenocortical stem and progenitor cells. Endocr Rev 30: 241-263
18. Kim AC, Reuter AL, Zubair M, Else T, Serecky K, et al. (2008) Targeted disruption of beta-catenin in Sf1-expressing cells impairs development and maintenance of the adrenal cortex. Development 135: 2593-2602
19. Thomas M, Keramidas M, Monchaux E, Feige JJ (2004) Dual hormonal regulation of endocrine tissue mass and vasculature by adrenocorticotropin in the adrenal cortex. Endocrinology 145: 4320-4329
20. Spencer SJ, Mesiano S, Lee JY, Jaffe RB (1999) 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
21. Beuschlein F, Looyenga BD, Bleasdale SE, Mutch C, Bavers DL, et al. (2003) Activin induces x-zone apoptosis that inhibits luteinizing hormone-dependent adrenocortical tumor formation in inhibin-deficient mice. Mol Cell Biol 23: 3951-3964
22. Chen YG, Lui HM, Lin SL, Lee JM, Ying SY (2002) Regulation of cell proliferation, apoptosis, and carcinogenesis by activin. Exp Biol Med (Maywood) 227: 75-87
23. Holmes PV, Dickson AD (1971) X-zone degeneration in the adrenal glands of adult and immature female mice. J Anat 108: 159-168
24. Zubair M, Parker KL, Morohashi K (2008) Developmental links between the fetal and adult zones of the adrenal cortex revealed by lineage tracing. Mol Cell Biol 28: 7030-7040
25. Aigueperse C, Martinez A, Lefrancois-Martinez AM, Veyssiere G, Jean CI (1999) Cyclic AMP regulates expression of the gene coding for a mouse vas deferens protein related to the aldo-keto reductase superfamily in human and murine adrenocortical cells. J Endocrinol 160: 147-154
26. Hershkovitz L, Beuschlein F, Klammer S, Krup M, Weinstein Y (2007) Adrenal 20alpha-hydroxysteroid dehydrogenase in the mouse catabolizes progesterone and 11-deoxycorticosterone and is restricted to the X-zone. Endocrinology 148: 976-988
27. Keeney DS, Jenkins CM, Waterman MR (1995) Developmentally regulated expression of adrenal 17 alpha-hydroxylase cytochrome P450 in the mouse embryo. Endocrinology 136: 4872-4879
28. Gomez Muguruza MT, Chrousos GP (1989) Periodic Cushing syndrome in a short boy: usefulness of the ovine corticotropin releasing hormone test. J Pediatr 115: 270-273
29. Sarlis NJ, Chrousos GP, Doppman JL, Carney JA, Stratakis CA (1997) Primary pigmented nodular adrenocortical disease: reevaluation of a patient with carney complex 27 years after unilateral adrenalectomy. J Clin Endocrinol Metab 82: 1274-1278
30. Stratakis CA, Sarlis N, Kirschner LS, Carney JA, Doppman JL, et al. (1999) Paradoxical response to dexamethasone in the diagnosis of primary pigmented nodular adrenocortical disease. Ann Intern Med 131: 585-591
31. Bourdeau I, Lacroix A, Schurch W, Caron P, Antakly T, et al. (2003) Primary pigmented nodular adrenocortical disease: paradoxical responses of cortisol secretion to dexamethasone occur in vitro and are associated with increased expression of the glucocorticoid receptor. J Clin Endocrinol Metab 88: 3931-3937
32. Louiset E, Stratakis CA, Perraudin V, Griffin KJ, Libe R, et al. (2009) The paradoxical increase in cortisol secretion induced by dexamethasone in primary pigmented nodular adrenocortical disease involves a glucocorticoid receptor- mediated effect of dexamethasone on protein kinase A catalytic subunits. J Clin Endocrinol Metab 94: 2406-2413
33. Shenoy BV, Carpenter PC, Carney JA (1984) Bilateral primary pigmented nodular adrenocortical disease. Rare cause of the Cushing syndrome. Am J Surg Pathol 8: 335-344
34. Brunk UT, Terman A (2002) Lipofuscin: mechanisms of age-related accumu- lation and influence on cell function. Free Radic Biol Med 33: 611-619
35. Mavrakis M, Lippincott-Schwartz J, Stratakis CA, Bossis I (2006) Depletion of type IA regulatory subunit (RIalpha) of protein kinase A (PKA) in mammalian cells and tissues activates mTOR and causes autophagic deficiency. Hum Mol Genet 15: 2962-2971
36. Kurz T, Terman A, Brunk UT (2007) Autophagy, ageing and apoptosis: the role of oxidative stress and lysosomal iron. Arch Biochem Biophys 462: 220-230
37. Mavrakis M, Lippincott-Schwartz J, Stratakis CA, Bossis, I. (2007) mTOR kinase and the regulatory subunit of protein kinase A (PRKAR1A) spatially and functionally interact during autophagosome maturation. Autophagy 3: 151-153
38. Ruvinsky I, Meyuhas O (2006) Ribosomal protein S6 phosphorylation: from protein synthesis to cell size. Trends Biochem Sci 31: 342-348
39. Taylor SS, Buechler JA, Yonemoto, W. (1990) cAMP-dependent protein kinase: framework for a diverse family of regulatory enzymes. Annu Rev Biochem 59: 971-1005
40. Nadella KS, Kirschner LS (2005) Disruption of protein kinase a regulation causes immortalization and dysregulation of D-type cyclins. Cancer Res 65: 10307-10315
41. Horvath A, Mathyakina L, Vong Q, Baxendale V, Pang AL, et al. (2006) Serial analysis of gene expression in adrenocortical hyperplasia caused by a germline PRKAR1A mutation. J Clin Endocrinol Metab 91: 584-596
42. Iseli BE, Hedinger CE (1985) Histopathology and ultrastructure of primary adrenocortical nodular dysplasia with Cushing's syndrome. Histopathology 9: 1171-1194
43. Aiba M, Hirayama A, Iri H, Kodama T, Fujimoto Y, et al. (1990) Primary adrenocortical micronodular dysplasia: enzyme histochemical and ultrastruc- tural studies of two cases with a review of the literature. Hum Pathol 21: 503-511
44. Zubair M, Ishihara S, Oka S, Okumura K, Morohashi K (2006) 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
45. Voutilainen R, Eramaa M, Ritvos O (1991) Hormonally regulated inhibin gene expression in human fetal and adult adrenals. J Clin Endocrinol Metab 73: 1026-1030
46. Ragazzon B, Cazabat L, Rizk-Rabin M, Assie G, Groussin L, et al. (2009) Inactivation of the Carney complex gene 1 (protein kinase A regulatory subunit 1A) inhibits SMAD3 expression and TGF beta-stimulated apoptosis in adrenocortical cells. Cancer Res 69: 7278-7284
47. Spencer SJ, Rabinovici J, Mesiano S, Goldsmith PC, Jaffe RB (1992) Activin and inhibin in the human adrenal gland. Regulation and differential effects in fetal and adult cells. J Clin Invest 90: 142-149
48. Ito M, Park Y, Weck J, Mayo KE, Jameson JL (2000) Synergistic activation of the inhibin alpha-promoter by steroidogenic factor-1 and cyclic adenosine 3',5'- monophosphate. Mol Endocrinol 14: 66-81
49. Vanttinen T, Kuulasmaa T, Liu J, Voutilainen R (2002) Expression of activin/ inhibin receptor and binding protein genes and regulation of activin/inhibin peptide secretion in human adrenocortical cells. J Clin Endocrinol Metab 87: 4257-4263
50. Kananen K, Markkula M, Mikola M, Rainio EM, McNeilly A, et al. (1996) Gonadectomy permits adrenocortical tumorigenesis in mice transgenic for the mouse inhibin alpha-subunit promoter/simian virus 40 T-antigen fusion gene: evidence for negative autoregulation of the inhibin alpha-subunit gene. Mol Endocrinol 10: 1667-1677
51. Farnworth PG, Stanton PG, Wang Y, Escalona R, Findlay JK, et al. (2006) Inhibins differentially antagonize activin and bone morphogenetic protein action in a mouse adrenocortical cell line. Endocrinology 147: 3462-3471
52. Grumbach MM, Biller BM, Braunstein GD, Campbell KK, Carney JA, et al. (2003) Management of the clinically inapparent adrenal mass (''incidentaloma''). Ann Intern Med 138: 424-429
53. Heikkila M, Peltoketo H, Leppaluoto J, Ilves M, Vuolteenaho O, et al. (2002) Wnt-4 deficiency alters mouse adrenal cortex function, reducing aldosterone production. Endocrinology 143: 4358-4365
54. Belloni AS, Mazzocchi G, Meneghelli V, Nussdorfer GG (1978) Cytogenesis in the rat adrenal cortex: evidence for an ACTH-induced centripetal cell migration from the zona glomerulosa. Arch Anat Histol Embryol 61: 195-205
55. Doghman M, Karpova T, Rodrigues GA, Arhatte M, De Moura J, et al. (2007) Increased steroidogenic factor-1 dosage triggers adrenocortical cell proliferation and cancer. Mol Endocrinol 21: 2968-2987
56. Berthon A, Sahut-Barnola I, Lambert-Langlais S, de Joussineau C, Damon- Soubeyrand C, et al. (2010) Constitutive {beta}-catenin activation induces adrenal hyperplasia and promotes adrenal cancer development. Hum Mol Genet.
57. Looyenga BD, Wiater E, Vale W, Hammer GD (2010) Inhibin-A antagonizes TGFbeta2 signaling by down-regulating cell surface expression of the TGFbeta coreceptor betaglycan. Mol Endocrinol 24: 608-620
58. Liu J, Matyakhina L, Han Z, Sandrini F, Bei T, et al. (2003) Molecular cloning, chromosomal localization of human peripheral-type benzodiazepine receptor and PKA regulatory subunit type 1A (PRKAR1A)-associated protein PAP7, and studies in PRKAR1A mutant cells and tissues. Faseb J 17: 1189-1191
59. Lefrancois-Martinez AM, Bertherat J, Val P, Tournaire C, Gallo-Payet N, et al. (2004) Decreased expression of cyclic adenosine monophosphate-regulated aldose reductase (AKR1B1) is associated with malignancy in human sporadic adrenocortical tumors. J Clin Endocrinol Metab 89: 3010-3019
60. Ragazzon B, Lefrancois-Martinez AM, Val P, Sahut-Barnola I, Tournaire C, et al. (2006) Adrenocorticotropin-dependent changes in SF-1/DAX-1 ratio influence steroidogenic genes expression in a novel model of glucocorticoid- producing adrenocortical cell lines derived from targeted tumorigenesis. Endocrinology 147: 1805-1818
61. Groussin L, Horvath A, Jullian E, Boikos S, Rene-Corail F, et al. (2006) A PRKAR1A mutation associated with primary pigmented nodular adrenocortical disease in 12 kindreds. J Clin Endocrinol Metab 91: 1943-1949.