Mitotane exhibits dual effects on steroidogenic enzymes gene transcription under basal and cAMP-stimulating microenvironments in NCI-H295 cells

Toxicology

Volumn 298, Issue 1-3, 2012, Pages 14-23

  Lin, Chia Wen ^a   Chang, Yen Hwa ^b   Pu, Hsiao Fung ^a  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

^b TAIPEI VETERANS GENERAL HOSPITAL   (Taiwan)

Author keywords

ACC; Adrenal; Cushing's syndrome; Mitotane; Steroidogenesis

Indexed keywords

CHOLESTEROL MONOOXYGENASE (SIDE CHAIN CLEAVING); CYCLIC AMP; CYTOCHROME P450 17; HYDROCORTISONE; MESSENGER RNA; MITOTANE; STEROID 21 MONOOXYGENASE;

ARTICLE; BIOSYNTHESIS; CANCER CELL CULTURE; CELL DEATH; GENE; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MICROENVIRONMENT; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; STAR GENE; STEROIDOGENESIS;

ADRENAL CORTEX NEOPLASMS; ADRENOCORTICAL CARCINOMA; ANTINEOPLASTIC AGENTS, HORMONAL; CELL LINE, TUMOR; CYCLIC AMP; ENZYME INDUCTION; ENZYME INHIBITORS; HUMANS; HYDROCORTISONE; MITOTANE; STEROID HYDROXYLASES; TRANSCRIPTION, GENETIC; TUMOR MICROENVIRONMENT;

EID: 84861929167     PISSN: 0300483X     EISSN: 18793185     Source Type: Journal    
DOI: 10.1016/j.tox.2012.04.007     Document Type: Article

References (57)

1. Abiven G., Coste J., Groussin L., Anract P., Tissier F., Legmann P., Dousset B., Bertagna X., Bertherat J. 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.
2. Allolio B., Fassnacht M. Clinical review: adrenocortical carcinoma: clinical update. J. Clin. Endocrinol. Metab. 2006, 91:2027-2037.
3. Arola J., Heikkila P., Voutilainen R., Kahri A.I. Role of adenylate cyclase-cyclic AMP-dependent signal transduction in the ACTH-induced biphasic growth effect of rat adrenocortical cells in primary culture. J. Endocrinol. 1993, 139:451-461.
4. Asp V., Lindstrom V., Olsson J.A., Bergstrom U., Brandt I. Cytotoxicity and decreased corticosterone production in adrenocortical Y-1 cells by 3-methylsulfonyl-DDE and structurally related molecules. Arch. Toxicol. 2009, 83:389-396.
5. Asp V., Ulleras E., Lindstrom V., Bergstrom U., Oskarsson A., Brandt I. Biphasic hormonal responses to the adrenocorticolytic DDT metabolite 3-methylsulfonyl-DDE in human cells. Toxicol. Appl. Pharmacol. 2010, 242:281-289.
6. Cai W., Counsell R.E., Djanegara T., Schteingart D.E., Sinsheimer J.E., Wotring L.L. Metabolic activation and binding of mitotane in adrenal cortex homogenates. J. Pharm. Sci. 1995, 84:134-138.
7. Daffara F., De Francia S., Reimondo G., Zaggia B., Aroasio E., Porpiglia F., Volante M., Termine A., Di Carlo F., Dogliotti L., Angeli A., Berruti A., Terzolo M. Prospective evaluation of mitotane toxicity in adrenocortical cancer patients treated adjuvantly. Endocr. Relat. Cancer 2008, 15:1043-1053.
8. Ferreira J.G., Cruz C.D., Neves D., Pignatelli D. Increased extracellular signal regulated kinases phosphorylation in the adrenal gland in response to chronic ACTH treatment. J. Endocrinol. 2007, 192:647-658.
9. Gallo-Payet N., Payet M.D. Mechanism of action of ACTH: beyond cAMP. Microsc. Res. Tech. 2003, 61:275-287.
10. Gazdar A.F., Oie H.K., Shackleton C.H., Chen T.R., Triche T.J., Myers C.E., Chrousos G.P., Brennan M.F., Stein C.A., La Rocca R.V. Establishment and characterization of a human adrenocortical carcinoma cell line that expresses multiple pathways of steroid biosynthesis. Cancer Res. 1990, 50:5488-5496.
11. Gonzalez R.J., Tamm E.P., Ng C., Phan A.T., Vassilopoulou-Sellin R., Perrier N.D., Evans D.B., Lee J.E. Response to mitotane predicts outcome in patients with recurrent adrenal cortical carcinoma. Surgery 2007, 142:867-875. discussion 867-875.
12. Hart M.M., Straw J.A. Studies on the site of action of o,p'-DDD in the dog adrenal cortex. 1. Inhibition of ACTH-mediated pregnenolone synthesis. Steroids 1971, 17:559-574.
13. Hermansson V., Asp V., Bergman A., Bergstrom U., Brandt I. Comparative CYP-dependent binding of the adrenocortical toxicants 3-methylsulfonyl-DDE and o,p'-DDD in Y-1 adrenal cells. Arch. Toxicol. 2007, 81:793-801.
14. Hermsen I.G., Fassnacht M., Terzolo M., Houterman S., den Hartigh J., Leboulleux S., Daffara F., Berruti A., Chadarevian R., Schlumberger M., Allolio B., Haak H.R., Baudin E. Plasma concentrations of o,p'DDD, o,p'DDA, and o,p'DDE as predictors of tumor response to mitotane in adrenocortical carcinoma: results of a retrospective ENS@T multicenter study. J. Clin. Endocrinol. Metab. 2011, 96:1844-1851.
15. Hoivik E.A., Lewis A.E., Aumo L., Bakke M. Molecular aspects of steroidogenic factor 1 (SF-1). Mol. Cell. Endocrinol. 2010, 315:27-39.
16. Hsu H.T., Chang Y.C., Chiu Y.N., Liu C.L., Chang K.J., Guo I.C. Leptin interferes with adrenocorticotropin/3',5'-cyclic adenosine monophosphate (cAMP) signaling, possibly through a Janus kinase 2-phosphatidylinositol 3-kinase/Akt-phosphodiesterase 3-cAMP pathway, to down-regulate cholesterol side-chain cleavage cytochrome P450 enzyme in human adrenocortical NCI-H295 cell line. J. Clin. Endocrinol. Metab. 2006, 91:2761-2769.
17. Hum D.W., Miller W.L. Transcriptional regulation of human genes for steroidogenic enzymes. Clin. Chem. 1993, 39:333-340.
18. Igaz P., Tombol Z., Szabo P.M., Liko I., Racz K. Steroid biosynthesis inhibitors in the therapy of hypercortisolism: theory and practice. Curr. Med. Chem. 2008, 15:2734-2747.
19. Ilan Z., Yaron Z. Suppression by organochlorines of the response to adrenocorticotrophin of the interrenal tissue in Sarotherodon aureus (Teleostei). J. Endocrinol. 1980, 87:185-193.
20. Jorgensen E.H., Balm P.H., Christiansen J.S., Plotitsyna N., Ingebrigtsen K. Influence of o'p-DDD on the physiological response to stress in Arctic charr (Salvelinus alpinus). Aquat. Toxicol. 2001, 54:179-193.
21. Kamenicky P., Droumaguet C., Salenave S., Blanchard A., Jublanc C., Gautier J.F., Brailly-Tabard S., Leboulleux S., Schlumberger M., Baudin E., Chanson P., Young J. Mitotane, metyrapone, and ketoconazole combination therapy as an alternative to rescue adrenalectomy for severe ACTH-dependent Cushing's syndrome. J. Clin. Endocrinol. Metab. 2011, 96:2796-2804.
22. Korth-Schutz S., Levine L.S., Roth J.A., Saenger P., New M.I. Virilizing adrenal tumor in a child suppressed with dexamethasone for three years. Effect of o,p'-DDD on serum and urinary androgens. J. Clin. Endocrinol. Metab. 1977, 44:433-439.
23. Lacroix M., Hontela A. The organochlorine o,p'-DDD disrupts the adrenal steroidogenic signaling pathway in rainbow trout (Oncorhynchus mykiss). Toxicol. Appl. Pharmacol. 2003, 190:197-205.
24. Li L.A., Wang P.W., Chang L.W. Polychlorinated biphenyl 126 stimulates basal and inducible aldosterone biosynthesis of human adrenocortical H295R cells. Toxicol. Appl. Pharmacol. 2004, 195:92-102.
25. Libe R., Fratticci A., Bertherat J. Adrenocortical cancer: pathophysiology and clinical management. Endocr. Relat. Cancer 2007, 14:13-28.
26. Lin T.C., Chien S.C., Hsu P.C., Li L.A. Mechanistic study of polychlorinated biphenyl 126-induced CYP11B1 and CYP11B2 up-regulation. Endocrinology 2006, 147:1536-1544.
27. Lindhe O., Skogseid B., Brandt I. Cytochrome P450-catalyzed binding of 3-methylsulfonyl-DDE and o,p'-DDD in human adrenal zona fasciculata/reticularis. J. Clin. Endocrinol. Metab. 2002, 87:1319-1326.
28. Lindholm J., Juul S., Jorgensen J.O., Astrup J., Bjerre P., Feldt-Rasmussen U., Hagen C., Jorgensen J., Kosteljanetz M., Kristensen L., Laurberg P., Schmidt K., Weeke J. Incidence and late prognosis of Cushing's syndrome: a population-based study. J. Clin. Endocrinol. Metab. 2001, 86:117-123.
29. Lisurek M., Bernhardt R. Modulation of aldosterone and cortisol synthesis on the molecular level. Mol. Cell. Endocrinol. 2004, 215:149-159.
30. Luton J.P., Cerdas S., Billaud L., Thomas G., Guilhaume B., Bertagna X., Laudat M.H., Louvel A., Chapuis Y., Blondeau P., et al. Clinical features of adrenocortical carcinoma, prognostic factors, and the effect of mitotane therapy. N. Engl. J. Med. 1990, 322:1195-1201.
31. Morishita K., Okumura H., Ito N., Takahashi N. Primary culture system of adrenocortical cells from dogs to evaluate direct effects of chemicals on steroidogenesis. Toxicology 2001, 165:171-178.
32. Nelson A.A., Woodard G. Severe adrenal cortical atrophy (cytotoxic) and hepatic damage produced in dogs by feeding 2,2-bis(parachlorophenyl)-1,1-dichloroethane (DDD or TDE). Arch. Pathol. 1949, 48:387-394.
33. Newell-Price J., Bertagna X., Grossman A.B., Nieman L.K. Cushing's syndrome. Lancet 2006, 367:1605-1617.
34. Ojima M., Saito M., Fukuchi S. The effects of o,p'-DDD on human adrenal steroid synthesis. Nippon Naibunpi Gakkai Zasshi 1984, 60:852-871.
35. Ojima M., Saitoh M., Itoh N., Kusano Y., Fukuchi S., Naganuma H. The effects of o,p'-DDD on adrenal steroidogenesis and hepatic steroid metabolism. Nippon Naibunpi Gakkai Zasshi 1985, 61:168-178.
36. Oskarsson A., Ulleras E., Plant K.E., Hinson J.P., Goldfarb P.S. Steroidogenic gene expression in H295R cells and the human adrenal gland: adrenotoxic effects of lindane in vitro. J. Appl. Toxicol. 2006, 26:484-492.
37. Phan A.T. Adrenal cortical carcinoma - review of current knowledge and treatment practices. Hematol. Oncol. Clin. North Am. 2007, 21:489-507.
38. Quinn S.J., Williams G.H. Regulation of aldosterone secretion. Annu. Rev. Physiol. 1988, 50:409-426.
39. Rainey W.E., Bird I.M., Mason J.I. The NCI-H295 cell line: a pluripotent model for human adrenocortical studies. Mol. Cell. Endocrinol. 1994, 100:45-50.
40. Samandari E., Kempna P., Nuoffer J.M., Hofer G., Mullis P.E., Fluck C.E. Human adrenal corticocarcinoma NCI-H295R cells produce more androgens than NCI-H295A cells and differ in 3β-hydroxysteroid dehydrogenase type 2 and 17,20 lyase activities. J. Endocrinol. 2007, 195:459-472.
41. Schteingart D.E. Adjuvant mitotane therapy of adrenal cancer - use and controversy. N. Engl. J. Med. 2007, 356:2415-2418.
42. Schteingart D.E., Sinsheimer J.E., Counsell R.E., Abrams G.D., McClellan N., Djanegara T., Hines J., Ruangwises N., Benitez R., Wotring L.L. Comparison of the adrenalytic activity of mitotane and a methylated homolog on normal adrenal cortex and adrenal cortical carcinoma. Cancer Chemother. Pharmacol. 1993, 31:459-466.
43. Schwarte S., Brabant E.G., Bastian L., Bruns F. Cortisol as a possible marker of metastatic adrenocortical carcinoma: a case report with 3-year follow-up. Anticancer Res. 2007, 27:1917-1920.
44. Sewer M.B., Waterman M.R. ACTH modulation of transcription factors responsible for steroid hydroxylase gene expression in the adrenal cortex. Microsc. Res. Tech. 2003, 61:300-307.
45. Soreide J.A., Brabrand K., Thoresen S.O. Adrenal cortical carcinoma in Norway, 1970-1984. World J. Surg. 1992, 16:663-667.
46. Stigliano A., Cerquetti L., Borro M., Gentile G., Bucci B., Misiti S., Piergrossi P., Brunetti E., Simmaco M., Toscano V. Modulation of proteomic profile in H295R adrenocortical cell line induced by mitotane. Endocr. Relat. Cancer 2008, 15:1-10.
47. Stocco D.M. A StAR search: implications in controlling steroidgenesis. Biol. Reprod. 1997, 56:328-336.
48. Thomas M., Keramidas M., Monchaux E., Feige J.J. Role of adrenocorticotropic hormone in the development and maintenance of the adrenal cortical vasculature. Microsc. Res. Tech. 2003, 61:247-251.
49. Touitou Y., Bogdan A., Auzeby A., Dommergues J.P. Glucocorticoid and mineralocorticoid pathways in two adrenocortical carcinomas: comparison of the effects of o,p'-dichlorodiphenyldichloroethane, aminoglutethimide and 2-p-aminophenyl-2-phenylethylamine in vitro. J. Endocrinol. 1979, 82:87-94.
50. van Erp N.P., Guchelaar H.J., Ploeger B.A., Romijn J.A., Hartigh J., Gelderblom H. Mitotane has a strong and a durable inducing effect on CYP3A4 activity. Eur. J. Endocrinol. 2011, 164:621-626.
51. Wajchenberg B.L., Albergaria Pereira M.A., Medonca B.B., Latronico A.C., Campos Carneiro P., Alves V.A., Zerbini M.C., Liberman B., Carlos Gomes G., Kirschner M.A. Adrenocortical carcinoma: clinical and laboratory observations. Cancer 2000, 88:711-736.
52. Wandoloski M., Bussey K.J., Demeure M.J. Adrenocortical cancer. Surg. Clin. North Am. 2009, 89:1255-1267.
53. Waterman M.R., Simpson E.R. Regulation of steroid hydroxylase gene expression is multifactorial in nature. Recent Prog. Horm. Res. 1989, 45:533-563. discussion 563-536.
54. Wojtowicz A.K., Gregoraszczuk E.L., Ptak A., Falandysz J. Effect of single and repeated in vitro exposure of ovarian follicles to o,p'-DDT and p,p'-DDT and their metabolites. Pol. J. Pharmacol. 2004, 56:465-472.
55. Wojtowicz A.K., Kajta M., Gregoraszczuk E.L. DDT- and DDE-induced disruption of ovarian steroidogenesis in prepubertal porcine ovarian follicles: a possible interaction with the main steroidogenic enzymes and estrogen receptor β. J. Physiol. Pharmacol. 2007, 58:873-885.
56. Wojtowicz A.K., Milewicz T., Gregoraszczuk E.L. DDT and its metabolite DDE alter steroid hormone secretion in human term placental explants by regulation of aromatase activity. Toxicol. Lett. 2007, 173:24-30.
57. Zenkert S., Schubert B., Fassnacht M., Beuschlein F., Allolio B., Reincke M. Steroidogenic acute regulatory protein mRNA expression in adrenal tumours. Eur. J. Endocrinol. 2000, 142:294-299.