Adrenal gland tumorigenesis after gonadectomy in mice is a complex genetic trait driven by epistatic loci

Endocrinology

Volumn 149, Issue 2, 2008, Pages 651-661

  Bernichtein, Sophie ^a   Petretto, Enrico ^a   Jamieson, Stacey ^a   Goel, Anuj ^a   Aitman, Timothy J ^a   Mangion, Jonathan M ^a   Huhtaniemi, Ilpo T ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

LUTEINIZING HORMONE RECEPTOR; SECRETED FRIZZLED RELATED PROTEIN 1;

ADRENAL HYPERPLASIA; ADRENAL TUMOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CHROMOSOME 18; CHROMOSOME 7; CHROMOSOME 8; CONTROLLED STUDY; FEMALE; GENETIC EPISTASIS; GENETIC LINKAGE; GENETIC TRAIT; GONADECTOMY; LUTEINIZING HORMONE BLOOD LEVEL; LUTEINIZING HORMONE RELEASE; MALE; MOUSE; NONHUMAN; OBESITY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE TRAIT LOCUS; UPREGULATION; WEIGHT GAIN;

ADRENAL GLAND NEOPLASMS; ANIMALS; EPIGENESIS, GENETIC; FEMALE; GENOMICS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LINKAGE (GENETICS); MALE; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, INBRED DBA; OBESITY; OVARIECTOMY; PHENOTYPE; POSTMENOPAUSE; QUANTITATIVE TRAIT LOCI; RECEPTORS, LH; SPECIES SPECIFICITY;

EID: 38549163370     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2007-0925     Document Type: Article

References (52)

1. Mantero F, Terzolo M, Arnaldi G, Osella G, Masini AM, Ali A, Giovagnetti M, Opocher G, Angeli A 2000 A survey on adrenal incidentaloma in Italy. Study Group on Adrenal Tumors of the Italian Society of Endocrinology. J Clin Endocrinol Metab 85:637-644
2. Thompson GB, Young Jr WF 2003 Adrenal incidentaloma. Curr Opin Oncol 15:84-90
3. Fidler WJ 1977 Ovarian thecal metaplasia in adrenal glands. Am J Clin Pathol 67:318-323
4. Givens JR, Andersen RN, Wiser WL, Coleman SA, Fish SA 1974 A gonadotropin-responsive adrenocortical adenoma. J Clin Endocrinol Metab 38:126-133
5. Romberger CF, Wong TW 1989 Thecal metaplasia in the adrenal gland of a man with acquired bilateral testicular atrophy. Arch Pathol Lab Med 113:1071-1075
6. Bertherat J, Mosnier-Pudar H, Bertagna X 2002 Adrenal incidentalomas. Curr Opin Oncol 14:58-63
7. Lacroix A, Baldacchino V, Bourdeau I, Hamet P, Tremblay J 2004 Cushing's syndrome variants secondary to aberrant hormone receptors. Trends Endocrinol Metab 15:375-382
8. Christopoulos S, Bourdeau I, Lacroix A 2005 Clinical and subclinical ACTH-independent macronodular adrenal hyperplasia and aberrant hormone receptors. Horm Res 64:119-131
9. Wy LA, Carlson HE, Kane P, Li X, Lei ZM, Rao CV 2002 Pregnancy-associated Cushing's syndrome secondary to a luteinizing hormone/human chorionic gonadotropin receptor-positive adrenal carcinoma. Gynecol Endocrinol 16:413-417
10. Bielinska M, Kiiveri S, Parviainen H, Männistö S, Heikinheimo M, Wilson DB 2006 Gonadectomy-induced adrenocortical neoplasia in the domestic ferret (Mustela putorius furo) and laboratory mouse. Vet Pathol 43:97-117
11. Kananen K, Markkula M, Mikola M, Rainio EM, McNeilly A, Huhtaniemi I 1996 Gonadectomy permits adrenocortical tumorigenesis in mice transgenic for the mouse inhibin α-subunit promoter/simian virus 40 T-antigen fusion gene: evidence for negative autoregulation of the inhibin α-subunit gene. Mol Endocrinol 10:1667-1677
12. Kero J, Poutanen M, Zhang FP, Rahman N, McNicol AM, Nilson JH, Keri RA, Huhtaniemi IT 2000 Elevated luteinizing hormone induces expression of its receptor and promotes steroidogenesis in the adrenal cortex. J Clin Invest 105:633-641
13. Bielinska M, Genova E, Boime I, Parviainen H, Kiiveri S, Leppäluoto J, Rahman N, Heikinheimo M, Wilson DB 2005 Gonadotropin-induced adrenocortical neoplasia in NU/J nude mice. Endocrinology 146:3975-3984
14. Bielinska M, Parviainen H, Porter-Tinge SB, Kiiveri S, Genova E, Rahman N, Huhtaniemi IT, Muglia LJ, Heikinheimo M, Wilson DB 2003 Mouse strain susceptibility to gonadectomy-induced adrenocortical tumor formation correlates with the expression of GATA-4 and luteinizing hormone receptor. Endocrinology 144:4123-4133
15. Rahman NA, Kiiveri S, Rivero-Muller A, Levallet J, Vierre S, Kero J, Wilson DB, Heikinheimo M, Huhtaniemi I 2004 Adrenocortical tumorigenesis in transgenic mice expressing the inhibin α-subunit promoter/simian virus 40 T-antigen transgene: relationship between ectopic expression of luteinizing hormone receptor and transcription factor GATA-4. Mol Endocrinol 18:2553-2569
16. Fekete E, Woolley GW, Little CC 1941 Histological changes following ovariectomy in mice. J Exp Med 74:1-8
17. Woolley GW, Little CC 1945 The incidence of adrenal cortical carcinoma in gonadectomized female mice of the extreme dilution strain. Cancer Res 5:193-202
18. Krishna Murthy AS, Brezak MA, Baez AG 1970 Postcastrational adrenal tumors in two strains of mice: morphologic, histochemical, and chromatographic studies. J Natl Cancer Inst 45:1211-1222
19. Haavisto AM, Pettersson K, Bergendahl M, Perheentupa A, Roser JF, Huhtaniemi I 1993 A supersensitive immunofluorometric assay for rat luteinizing hormone. Endocrinology 132:1687-1691
20. Bergendahl M, Perheentupa A, Huhtaniemi I 1989 Effect of short-term starvation on reproductive hormone gene expression, secretion and receptor levels in male rats. J Endocrinol 121:409-417
21. Lander ES, Green P 1987 Construction of multilocus genetic linkage maps in humans. Proc Natl Acad Sci USA 84:2363-2367
22. Lincoln SE, Lander ES 1992 Systematic detection of errors in genetic linkage data. Genomics 14:604-610
23. Broman KW, Wu H, Sen S, Churchill GA 2003 R/qtl: QTL mapping in experimental crosses. Bioinformatics 19:889-890
24. Churchill GA, Doerge RW 1994 Empirical threshold values for quantitative trait mapping. Genetics 138:963-971
25. Dupuis J, Siegmund D 1999 Statistical methods for mapping quantitative trait loci from a dense set of markers. Genetics 151:373-386
26. Kruglyak L, Lander ES 1995 A nonparametric approach for mapping quantitative trait loci. Genetics 139:1421-1428
27. Broman KW 2003 Mapping quantitative trait loci in the case of a spike in the phenotype distribution. Genetics 163:1169-1175
28. Haley CS, Knott SA 1992 A simple regression method for mapping quantitative trait loci in line crosses using flanking markers. Heredity 69:315-324
29. Solberg LC, Baum AE, Ahmadiyeh N, Shimomura K, Li R, Turek FW, Churchill GA, Takahashi JS, Redei EE 2004 Sex- and lineage-specific inheritance of depression-like behavior in the rat. Mamm Genome 15:648-662
30. Cervino AC, Gosink M, Fallahi M, Pascal B, Mader C, Tsinoremas NF 2006 A comprehensive mouse IBD database for the efficient localization of quantitative trait loci. Mamm Genome 17:565-574
31. Lynch M, Walsh B 1998 Genetics and analysis of quantitative traits. Sunderland, MA: Sinauer Associates Inc.
32. Beuschlein F, Looyenga BD, Bleasdale SE, Mutch C, Bavers DL, Parlow AF, Nilson JH, Hammer GD 2003 Activin induces x-zone apoptosis that inhibits luteinizing hormone-dependent adrenocortical tumor formation in inhibindeficient mice. Mol Cell Biol 23:3951-3964
33. Mazzuco TL, Chabre O, Feige JJ, Thomas M 2006 Aberrant expression of human luteinizing hormone receptor by adrenocortical cells is sufficient to provoke both hyperplasia and Cushing's syndrome features. J Clin Endocrinol Metab 91:196-203
34. Mazzuco TL, Chabre O, Sturm N, Feige JJ, Thomas M 2006 Ectopic expression of the gastric inhibitory polypeptide receptor gene is a sufficient genetic event to induce benign adrenocortical tumor in a xenotransplantation model. Endocrinology 147:782-790
35. Kiiveri S, Liu J, Heikkila P, Arola J, Lehtonen E, Voutilainen R, Heikinheimo M 2004 Transcription factors GATA-4 and GATA-6 in human adrenocortical tumors. Endocr Res 30:919-923
36. Huseby RA, Bittner JJ 1951 Differences in adrenal responsiveness to post-castrational alteration as evidenced by transplanted adrenal tissue. Cancer Res 11:954-961
37. Beamer WG, Sweet HO, Bronson RT, Shire JG, Orth DN, Davisson MT 1994 Adrenocortical dysplasia: a mouse model system for adrenocortical insufficiency. J Endocrinol 141:33-43
38. Keegan CE, Hutz JE, Else T, Adamska M, Shah SP, Kent AE, Howes JM, Beamer WG, Hammer GD 2005 Urogenital and caudal dysgenesis in adrenocortical dysplasia (acd) mice is caused by a splicing mutation in a novel telomeric regulator. Hum Mol Genet 14:113-123
39. French AJ, Petroni G, Thibideau SN, Smolkin M, Bissonette E, Roviello F, Harper JC, Koch BR, Anderson SA, Hebbring SJ, Powell SM 2004 Allelic imbalance of 8p indicates poor survival in gastric cancer. J Mol Diagn 6:243-252
40. Diament AL, Warden CH 2004 Multiple linked mouse chromosome 7 loci influence body fat mass. Int J Obes Relat Metab Disord 28:199-210
41. Taylor BA, Phillips SJ 1997 Obesity QTLs on mouse chromosomes 2 and 17. Genomics 43:249-257
42. Itoi-Babaya M, Ikegami H, Fujisawa T, Ueda H, Nojima K, Babaya N, Kobayashi M, Noso S, Kawaguchi Y, Yamaji K, Shibata M, Ogihara T 2007 Fatty liver and obesity: phenotypically correlated but genetically distinct traits in a mouse model of type 2 diabetes. Diabetologia 50:1641-1648
43. Lin PI, Vance JM, Pericak-Vance MA, Martin ER 2007 No gene is an island: the flip-flop phenomenon. Am J Hum Genet 80:531-538
44. Finch PW, He X, Kelley MJ, Uren A, Schaudies RP, Popescu NC, Rudikoff S, Aaronson SA, Varmus HE, Rubin JS 1997 Purification and molecular cloning of a secreted, Frizzled-related antagonist of Wnt action. Proc Natl Acad Sci USA 94:6770-6775
45. Moon RT, Kohn AD, De Ferrari GV, Kaykas A 2004 WNT and β-catenin signalling: diseases and therapies. Nat Rev Genet 5:691-701
46. Veeck J, Niederacher D, An H, Klopocki E, Wiesmann F, Betz B, Galm O, Camara O, Durst M, Kristiansen G, Huszka C, Knuchel R, Dahl E 2006 Aberrant methylation of the Wnt antagonist SFRP1 in breast cancer is associated with unfavourable prognosis. Oncogene 25:3479-3488
47. Dahl E, Wiesmann F, Woenckhaus M, Stoehr R, Wild PJ, Veeck J, Knuchel R, Klopocki E, Sauter G, Simon R, Wieland WF, Walter B, Denzinger S, Hartmann A, Hammerschmied CG 2007 Frequent loss of SFRP1 expression in multiple human solid tumours: association with aberrant promoter methylation in renal cell carcinoma. Oncogene 26:5680-5691
48. Johnsen IK, Slawik M, Shapiro I, Hartmann MF, Wudy SA, Looyenga BD, Hammer GD, Reincke M, Beuschlein F 2006 Gonadectomy in mice of the inbred strain CE/J induces proliferation of sub-capsular adrenal cells expressing gonadal marker genes. J Endocrinol 190:47-57
49. Zajicek G, Ariel I, Arber N 1986 The streaming adrenal cortex: direct evidence of centripetal migration of adrenocytes by estimation of cell turnover rate. J Endocrinol 111:477-482
50. Kataoka Y, Ikehara Y, Hattori T 1996 Cell proliferation and renewal of mouse adrenal cortex. J Anat 188(Pt 2):375-381
51. Looyenga BD, Hammer GD 2006 Origin and identity of adrenocortical tumors in inhibin knockout mice: implications for cellular plasticity in the adrenal cortex. Mol Endocrinol 20:2848-2863
52. Nusse R 2005 Wnt signaling in disease and in development. Cell Res 15:28-32