Decreased expression of cyclic adenosine monophosphate-regulated aldose reductase (AKR1B1) is associated with malignancy in human sporadic adrenocortical tumors

Journal of Clinical Endocrinology and Metabolism

Volumn 89, Issue 6, 2004, Pages 3010-3019

  Lefrançois Martinez, Anne Marie ^a   Bertherat, Jérôme ^b   Val, Pierre ^a   Tournaire, Colette ^a   Gallo Payet, Nicole ^c   Hyndman, David ^d   Veyssière, Georges ^a   Bertagna, Xavier ^b   Jean, Claude ^a   Martinez, Antoine ^a  

^a UNIVERSITÉ CLERMONT AUVERGNE   (France)

^b INSERM   (France)

^c UNIVERSITY OF SHERBROOKE   (Canada)

^d QUEEN S UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE REDUCTASE;

ADRENAL CORTEX CELL; ADRENAL CORTEX TUMOR; ADRENAL GLAND; ADULT; AGED; AKR1B1 GENE; CLINICAL ARTICLE; CONFERENCE PAPER; CONTROLLED STUDY; DISEASE ASSOCIATION; FEMALE; GENE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; LIPID PEROXIDATION; MALE; ORTHOLOGY; PRIORITY JOURNAL; X CHROMOSOME;

ADENOMA; ADRENAL CORTEX; ADRENAL CORTEX NEOPLASMS; ALDEHYDE REDUCTASE; AMINO ACID SEQUENCE; CAPROATES; CELLS, CULTURED; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; FETUS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MOLECULAR SEQUENCE DATA; RNA, MESSENGER; SIGNAL TRANSDUCTION;

MURINAE;

EID: 2942668375     PISSN: 0021972X     EISSN: None     Source Type: Journal    
DOI: 10.1210/jc.2003-031830     Document Type: Conference Paper

References (71)

1. Latronico AC, Chrousos GP 1997 Extensive personal experience: adrenocortical tumors. J Clin Endocrinol Metab 82:1317-1324
2. Kopf D, Goretzki P, Lehnen H 2001 Clinical management of malignant adrenal tumors. J Cancer Res Clin Oncol 127:143-155
3. Gicquel C, Bertagna X, Schneid H, Francillard-Leblond M, Luton JP, Girard F, Le Bouc Y 1994 Rearrangements at 11p15 locus and overexpression of insulin like growth factor II gene in sporadic adrenocortical tumors. J Clin Endocrinol Metab 78:1444-1453
4. Liu J, Kahri AI, Heikkila P, Voutilainen R 1997 Ribonucleic acid expression of the clustered imprinted genes, p57KIP2, insulin-like growth factor II, and H19, in adrenal tumors and cultured adrenal cells. J Clin Endocrinol Metab 82:1766-1771
5. Gicquel C, Raffin-Sanson ML, Gaston V, Bertagna X, Plouin PF, Schlumberger M, Louvel A, Luton JP, Le Bouc Y 1997 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 82:2559-2565
6. Bourcigaux N, Gaston V, Logie A, Bertagna X, Le Bouc Y, Gicquel C 2000 High expression of cyclin E and G1 CDK and loss of function of p57KIP2 are involved in proliferation of malignant sporadic adrenocortical tumors. J Clin Endocrinol Metab 85:322-330
7. Bornstein S, Stratakis C, Chrousos G 1999 Adrenocortical tumors: recent advances in basic concepts and clinical management. Ann Intern Med 130:759-771
8. Lin S, Lee Y, Tsai J 1994 Mutations of the p53 gene in human functional adrenal neoplasms. J Clin Endocrinol Metab 78:483-491
9. Gicquel C, Bertagna X, Le Bouc Y 1995 Recent advances in the pathogenesis of adrenocortical tumours. Eur J Endocrinol 133:133-144
10. Heppner C, Reincke M, Agarwal SK, Mora P, Allolio B, Burns AL, Spiegel AM, Marx SJ 1999 MEN1 gene analysis in sporadic adrenocortical neoplasms. J Clin Endocrinol Metab 84:216-219
11. Gortz B, Roth J, Speel EJ, Krahenmann A, De Krijger RR, Matias-Guiu X, Muletta-Feurer S, Rutmann K, Saremaslani P, Heitz PU, Komminoth P 1999 MEN1 gene mutation analysis of sporadic adrenocortical lesions. Int J Cancer 80:373-379
12. Schulte KM, Mengel M, Heinze M, Simon D, Scheuring S, Kohrer K, Roher HD 2000 Complete sequencing and messenger ribonucleic acid expression analysis of the MEN I gene in adrenal cancer. J Clin Endocrinol Metab 85:441-448
13. Gicquel C, Bertagna X, Gaston V, Coste J, Louvel A, Baudin E, Bertherat J, Chapuis Y, Duclos JM, Schlumberger M, Plouin PF, Luton JP, Le Bouc Y 2001 Molecular markers and long-term recurrences in a large cohort of patients with sporadic adrenocortical tumors. Cancer Res 61:6762-6767
14. Hyndman D, Bauman DR, Heredia VV, Penning TM 2003 The aldo-keto reductase superfamily home page. Chem Biol Interact 143-144:621-631
15. Kinoshita J, Nishimura C 1988 The involvement of aldose reductase in diabetic complications. Diabetes Metab Rev 4:323-337
16. Lee AY, Chung SK, Chung SS 1995 Demonstration that polyol accumulation is responsible for diabetic cataract by the use of transgenic mice expressing the aldose reductase gene in the lens. Proc Natl Acad Sci USA 92:2780-2784
17. Grimshaw CE, Mathur EJ 1989 Immunoquantitation of aldose reductase in human tissues. Anal Biochem 176:66-71
18. Matsuura K, Deyashiki Y, Bunai Y, Ohya I, Hara A 1996 Aldose reductase is a major reductase for isocaproaldehyde, a product of side chain cleavage of cholesterol, in human and animal adrenal glands. Arch Biochem Biophys 328:265-288
19. Lefrançois-Martinez A, Tournaire C, Martinez A, Berger M, Daoudal S, Tritsch D, Veyssiere G, Jean C 1999 Product of side-chain cleavage of cholesterol, isocaproaldehyde, is an endogenous specific substrate of mouse vas deferens protein, an aldose reductase-like protein in adrenocortical cells. J Biol Chem 274:32875-32880
20. Aigueperse C, Martinez A, Lefrançois-Martinez AM, Veyssiere G, Jean C 1999 Cyclic AMP regulates expression of the gene coding for a protein related to the aldo-keto reductase superfamily (MVDP) in human and murine adrenocortical cells. J Endocrinol 160:147-154
21. Martinez A, Lefrancois-Martinez AM, Manin M, Guyot S, Jean-Faucher C, Veyssiere G, Kahn A, Jean C 1999 5′-Flanking and intragenic sequences confer androgenic and developmental regulation of mouse aldose reductase-like gene in vas deferens and adrenal in transgenic mice. Endocrinology 140:1338-1348
22. Aigueperse C, Val P, Pacot C, Darne C, Lalli E, Sassone-Corsi P, Veyssiere G, Jean C, Martinez A 2001 SF-1 (steroidogenic factor-1), C/EBP (β CCAAT) enhancer binding protein, and ubiquitous transcription factors NF1 (nuclear factor 1) and SP1 (selective promoter factor 1) are required for regulation of the mouse aldose reductase-like gene (AKR1B7) expression in adrenocortical cells. Mol Endocrinol 15:93-111
23. Val P, Martinez A, Sahut-Barnola I, Jean C, Veyssiere G, Lefrancois-Martinez AM 2002 A 77-base pair LINE-like sequence elicits androgen-dependent mvdp/akr1-b7 expression in mouse vas deferens, but is dispensable for adrenal expression in rats. Endocrinology 143:3435-3448
24. Chinn AM, Ciais D, Bailly S, Chambaz E, LaMarre J, Feige JJ 2002 Identification of two novel ACTH-responsive genes encoding manganese-dependent superoxide dismutase (SOD2) and the zinc finger protein TIS11b [tetradecanoyl phorbol acetate (TPA)-inducible sequence 11b]. Mol Endocrinol 16: 1417-1427
25. Simpson E, Waterman M 1988 Regulation of the synthesis of steroidogenic enzymes in adrenocortical cells by ACTH. Annu Rev Physiol 50:427-440
26. Jefcoate C, McNamara B, Artemenko I, Yamazaki T 1992 Regulation of cholesterol movement to mitochondrial cytochrome P450scc in steroid hormone synthesis. J Steroid Biochem Mol Biol 43:751-767
27. Stocco D, Clark B 1997 The role of the steroidogenic acute regulatory protein in steroidogenesis. Steroids 62:29-36
28. Parker K, Schimmer B 1997 Steroidogenic factor 1: a key determinant of endocrine development and function. Endocr Rev 18:361-377
29. Zanaria E, Muscatelli F, Bardoni B, Strom T, Guioli S, Guo W, Lalli E, Moser C, Walker A, McCabe E, Meitinger T, Monaco A, Sassone-Corsi P, Camerino G 1994 An unusual member of the nuclear hormone receptor superfamily responsible for X-linked adrenal hypoplasia congenita. Nature 372:635-641
30. Luton JP, Martinez M, Coste J, Bertherat J 2000 Outcome in patients with adrenal incidentaloma selected for surgery: an analysis of 88 cases investigated in a single clinical center. Eur J Endocrinol 143:111-117
31. Luton JP, Cerdas S, Billaud L, Thomas G, Guilhaume B, Bertagna X, Laudat MH, Louvel A, Chapuis Y, Blondeau P, Bonnin A, Bricaire H 1990 Clinical features of adrenocortical carcinoma, prognostic factors, and the effect of mitotane therapy. N Engl J Med 322:1195-1201
32. Streeter G 1920 Weight, sitting height, head size, foot length and menstrual age of the human embryo. Contrib Embryol 11:143-179
33. Pailhoux E, Martinez A, Veyssiere G, Jean C 1990 Androgen-dependent protein from mouse vas deferens. J Biol Chem 265:19932-19936
34. Morel L, Brochard D, Manin M, Simon AM, Jean C, Veyssiere G 2001 Mouse seminal vesicle secretory protein of 99 amino acids (MSVSP99): characterization and hormonal and developmental regulation. J Androl 22:549-557
35. Staels B, Hum DW, Miller WL 1993 Regulation of steroidogenesis in NCI-H295 cells: a cellular model of the human fetal adrenal. Mol Endocrinol 7:423-433
36. Bohren K, Grimshaw C, Gabbay K 1992 Catalytic effectiveness of human aldose reductase. J Biol Chem 267:20965-20970
37. Sahut-Barnola I, Lefrancois-Martinez AM, Jean C, Veyssiere G, Martinez A 2000 Adrenal tumorigenesis targeted by the corticotropin-regulated promoter of the aldo-keto reductase AKR1B7 gene in transgenic mice. Endocr Res 26: 885-898
38. Mesiano S, Jaffe RB 1997 Developmental and functional biology of the primate fetal adrenal cortex. Endocr Rev 18:378-401
39. Rainey WE, Bird IM, Sawetawan C, Hanley NA, McCarthy JL, McGee EA, Wester R, Mason JI 1993 Regulation of human adrenal carcinoma cell (NCI-H295) production of C19 steroids. J Clin Endocrinol Metab 77:731-737
40. Zenkert S, Schubert B, Fassnacht M, Beuschlein F, Allolio B, Reincke M 2000 Steroidogenic acute regulatory protein mRNA expression in adrenal tumours. Eur J Endocrinol 142:294-299
41. Grundmann U, Bohn H, Obermeier R, Amann E 1990 Cloning and prokaryotic expression of a biologically active human placental aldose reductase. DNA Cell Biol 9:149-157
42. Reincke M, Beuschlein F, Lalli E, Arlt W, Vay S, Sassone-Corsi P, Allolio B 1998 DAX-1 expression in human adrenocortical neoplasms: implications for steroidogenesis. J Clin Endocrinol Metab 83:2597-2600
43. Lau E, Cao D, Lin C, Chung S, Chung S 1995 Tissue-specific expression of two aldose reductase-like genes in mice: abundant expression of mouse vas deferens protein and fibroblast growth factor-regulated protein in the adrenal gland. Biochem J 312:609-615
44. Wilson DK, Tarle I, Petrash JM, Quiocho FA 1993 Refined 1.8 A structure of human aldose reductase complexed with the potent inhibitor zopolrestat. Proc Natl Acad Sci USA 90:9847-9851
45. Sasano H, Shizawa S, Suzuki T, Takayama K, Fukaya T, Morohashi K, Nagura H 1995 Ad4BP in the human adrenal cortex and its disorders. J Clin Endocrinol Metab 80:2378-2380
46. Shibata H, Ando T, Suzuki T, Kurihara I, Hayashi K, Hayashi M, Saito I, Murai M, Saruta T 1998 COUP-TFI expression in human adrenocortical adenomas: possible role in steroidogenesis. J Clin Endocrinol Metab 83:4520-4523
47. Vilain E, Guo W, Zhang YH, McCabe ER 1997 DAX1 gene expression upregulated by steroidogenic factor 1 in an adrenocortical carcinoma cell line. Biochem Mol Med 61:1-8
48. Hoyle C, Narvaez V, Alldus G, Lovell-Badge R, Swain A 2002 Dax1 expression is dependent on steroidogenic factor. 1 in the developing gonad. Mol Endocrinol 16:747-756
49. Bassett MH, Zhang Y, Clyne C, White PC, Rainey WE 2002 Differential regulation of aldosterone synthase and 11β-hydroxylase transcription by steroidogenic factor-1. J Mol Endocrinol 28:125-135
50. Fallo F, Pezzi V, Barzon L, Mulatero P, Veglio F, Sonino N, Mathis JM 2002 Quantitative assessment of CYP11B1 and CYP11B2 expression in aldosterone-producing adenomas. Eur J Endocrinol 147:795-802
51. Shibata H, Ikeda Y, Mukai T, Morohashi K, Kurihara I, Ando T, Suzuki T, Kobayashi S, Murai M, Saito I, Saruta T 2001 Expression profiles of COUP-TF, DAX-1, and SF-1 in the human adrenal gland and adrenocortical tumors: possible implications in steroidogenesis. Mol Genet Metab 74:206-216
52. Graham A, Brown L, Hedge P, Gammack A, Markham A 1991 Structure of the human aldose reductase gene. J Biol Chem 266:6872-6877
53. Rosenberg D, Groussin L, Jullian E, Perlemoine K, Medjane S, Louvel A, Bertagna X, Bertherat J 2003 Transcription factor 3′,5′-cyclic adenosine 5′-monophosphate-responsive element-binding protein (CREB) is decreased during human adrenal cortex tumorigenesis and fetal development. J Clin Endocrinol Metab 88:3958-3965
54. Reincke M, Mora P, Beuschlein F, Arlt W, Chrousos GP, Allolio B 1997 Deletion of the adrenocorticotropin receptor gene in human adrenocortical tumors: implications for tumorigenesis. J Clin Endocrinol Metab 82:3054-3058
55. Bertherat J, Groussin L, Sandrini F, Matyakhina L, Bei T, Stergiopoulos S, Papageorgiou T, Bourdeau I, Kirschner LS, Vincent-Dejean C, Perlemoine K, Gicquel C, Bertagna X, and Stratakis CA 2003 Molecular and functional analysis of PRKAR1A and its locus (17q22-24) in sporadic adrenocortical tumors: 17q losses, somatic mutations, and protein kinase A expression and activity. Cancer Res 63:5308-5319
56. Zeindl-Eberhart E, Jungblut P, Otto A, Kerler R, Rabes H 1997 Further characterization of a rat hepatoma-derived aldose-reductase-like protein. Eur J Biochem 247:792-800
57. Cao D, Fan S, Chung S 1998 Identification and characterization of a novel human aldose reductase like gene. J Biol Chem 273:11429-11435
58. Stadman E, Berlett B 1997 Reactive oxygen mediated protein oxidation in aging and disease. Chem Res Toxicol 10:485-494
59. Esterbauer H, Schaur R, Zollner H 1991 Chemistry and biochemistry of 4-hydroxynonenal malonaldehyde and related aldehydes. Free Radic Biol Med 11:81-128
60. Okamoto K, Toyokuni S, Uchida K, Ogawa O, Takenewa J, Kakehi Y, Kinoshita H, Hattori-Nakakuki Y, Hiai H, Yoshida O 1994 Formation of 8-hydroxy-2′- deoxyguanosine and 4-hydroxy-2-nonenal-modified proteins in human renal-cell carcinoma. Int J Cancer 58:825-829
61. Radu A, Moldovan N 1991 4-Hydroxynonenal reduces junctional communication between endothelial cells in culture. Exp Cell Res 196:121-126
62. Vander Jagt D, Kolb N, Vander Jagt T, Martinez F, Mills R, Young S, Vander Jagt D 1995 Substrate specificity of human aldose reductase: identification of 4-hydroxynonenal as an endogenous substrate. Biochim Biophys Acta 249: 117-126
63. Murray S, Davis K, Fishman L, Bornstein S 2000 α1 Connexin 43 gap junctions are decreased in human adrenocortical tumors. J Clin Endocrinol Metab 85: 890-895
64. Liu J, Heikkila P, Kahri A, Voutilainen R 1996 Expression of the steroidogenic acute regulatory protein mRNA in adrenal tumors and cultural adrenal cells. J Endocrinol 150:43-50
65. Kiiveri S, Siltanen S, Rahman N, Bielinska M, Lehto VP, Huhtaniemi IT, Muglia LJ, Wilson DB, Heikinheimo M 1999 Reciprocal changes in the expression of transcription factors GATA-4 and GATA-6 accompany adrenocortical tumorigenesis in mice and humans. Mol Med 5:490-501
66. Terzolo M, Boccuzzi A, Bovio S, Cappia S, De Giuli P, Ali A, Paccotti P, Porpiglia F, Fontana D, Angeli A 2001 Immunohistochemical assessment of Ki-67 in the differential diagnosis of adrenocortical tumors. Urology 57:176-182
67. De Fraipont F, El Atifi M, Gicquel C, Bertagna X, Chambaz EM, Feige JJ 2000 Expression of the angiogenesis markers vascular endothelial growth factor-A, thrombospondin-1, and platelet-derived endothelial cell growth factor in human sporadic adrenocortical tumors: correlation with genotypic alterations. J Clin Endocrinol Metab 85:4734-4741
68. Boulie N, Logié A, Gicquel C, Perin L, Le Bouc Y 1998 Increased levels of insulin-like growth factor II (IGF-II) and IGF-binding protein-2 are associated with malignancy in sporadic adrenocortical tumors. J Clin Endocrinol Metab 83:1713-1720
69. Weber M, Auernhamma C, Kiess W, Engelhardt D 1997 Insulin-like growth factor receptors in normal and tumorous adult human adrenocortical glands. Eur J Endocrinol 136:296-303
70. Donohue P, Alberts O, Hampton B, Winkles J 1994 A delayed-early gene activated by fibroblast growth factor-1 encodes a protein related to aldose reductase. J Biol Chem 269:8604-8609
71. Hyndman D, Flynn J 1998 Sequence and expression levels in human tissues of a new member of the aldo-keto reductase family. Biochim Biophys Acta 1399:198-202