Transcriptome analysis of MENX-associated rat pituitary adenomas identifies novel molecular mechanisms involved in the pathogenesis of human pituitary gonadotroph adenomas

Acta Neuropathologica

Volumn 126, Issue 1, 2013, Pages 137-150

  Lee, Misu ^a   Marinoni, Ilaria ^a,f   Irmler, Martin ^a   Psaras, Tsambika ^b   Honegger, Jürgen B ^b   Beschorner, Rudi ^b   Anastasov, Natasa ^a   Beckers, Johannes ^a,c   Theodoropoulou, Marily ^d   Roncaroli, Federico ^e   Pellegata, Natalia S ^a  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^d MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

^e IMPERIAL COLLEGE LONDON   (United Kingdom)

^f UNIVERSITY OF BERN   (Switzerland)

Author keywords

CYP11A1; MENX model; NUSAP1; Pituitary gonadotroph adenoma; Transcriptome analysis

Indexed keywords

CHOLESTEROL MONOOXYGENASE (SIDE CHAIN CLEAVING); TRANSCRIPTOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; CYP11A1 GENE; GENE; GENE CONTROL; GONADOTROPH ADENOMA; GONADOTROPIN SECRETING CELL; HUMAN; HUMAN TISSUE; IN VITRO STUDY; MOUSE; MULTIPLE ENDOCRINE NEOPLASIA; NONHUMAN; NUCLEOTIDE SEQUENCE; NUSAP1 GENE; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; UPREGULATION;

ADENOMA; ANIMALS; BIOSTATISTICS; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; CHOLESTEROL SIDE-CHAIN CLEAVAGE ENZYME; COMPUTATIONAL BIOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GONADOTROPINS, PITUITARY; GREEN FLUORESCENT PROTEINS; HUMANS; MICROARRAY ANALYSIS; MICROTUBULE-ASSOCIATED PROTEINS; PITUITARY NEOPLASMS; RATS; RNA INTERFERENCE; TRANSCRIPTION FACTORS; TRANSFECTION;

EID: 84879601809     PISSN: 00016322     EISSN: 14320533     Source Type: Journal    
DOI: 10.1007/s00401-013-1132-7     Document Type: Article

References (46)

1. Altenberger T, Bilban M, Auer M et al (2006) Identification of DLK1 variants in pituitary- and neuroendocrine tumors. Biochem Biophys Res Commun 340:995-1005. doi: 10.1016/j.bbrc.2005.12.094
2. Anastasov N, Klier M, Koch I et al (2009) Efficient shRNA delivery into B and T lymphoma cells using lentiviral vector-mediated transfer. J Hematopathol 2:9-19. doi: 10.1007/s12308-008-0020-x
3. Bogunovic D, O'Neill DW, Belitskaya-Levy I et al (2009) Immune profile and mitotic index of metastatic melanoma lesions enhance clinical staging in predicting patient survival. Proc Natl Acad Sci USA 106:20429-20434. doi: 10.1073/pnas.0905139106
4. Chen DT, Nasir A, Culhane A et al (2010) Proliferative genes dominate malignancy-risk gene signature in histologically-normal breast tissue. Breast Cancer Res Treat 119:335-346. doi: 10.1007/s10549-009-0344-y
5. Cheunsuchon P, Zhou Y, Zhang X et al (2011) Silencing of the imprinted DLK1-MEG3 locus in human clinically nonfunctioning pituitary adenomas. Am J Pathol 179:2120-2130. doi: 10.1016/j.ajpath.2011.07.002
6. Davis SW, Castinetti F, Carvalho LR et al (2010) Molecular mechanisms of pituitary organogenesis: in search of novel regulatory genes. Mol Cell Endocrinol 323:4-19. doi: 10.1016/j.mce.2009.12.012
7. Derouet-Humbert E, Roemer K, Bureik M (2005) Adrenodoxin (Adx) and CYP11A1 (P450scc) induce apoptosis by the generation of reactive oxygen species in mitochondria. Biol Chem 386:453-461. doi: 10.1515/BC.2005.054
8. Doghman M, Karpova T, Rodrigues GA et al (2007) Increased steroidogenic factor-1 dosage triggers adrenocortical cell proliferation and cancer. Mol Endocrinol 21:2968-2987. doi: 10.1210/me.2007-0120
9. Elston MS, Gill AJ, Conaglen JV et al (2008) Wnt pathway inhibitors are strongly down-regulated in pituitary tumors. Endocrinology 149:1235-1242. doi: 10.1210/en.2007-0542
10. Ericson J, Norlin S, Jessell TM, Edlund T (1998) Integrated FGF and BMP signaling controls the progression of progenitor cell differentiation and the emergence of pattern in the embryonic anterior pituitary. Development 125:1005-1015
11. Evans CO, Young AN, Brown MR et al (2001) Novel patterns of gene expression in pituitary adenomas identified by complementary deoxyribonucleic acid microarrays and quantitative reverse transcription-polymerase chain reaction. J Clin Endocrinol Metab 86:3097-3107. doi: 10.1210/jc.86.7.3097
12. Galland F, Lacroix L, Saulnier P et al (2010) Differential gene expression profiles of invasive and non-invasive non-functioning pituitary adenomas based on microarray analysis. Endocr Relat Cancer 17:361-371. doi: 10.1677/ERC-10-0018
13. Gejman R, Batista DL, Zhong Y et al (2008) Selective loss of MEG3 expression and intergenic differentially methylated region hypermethylation in the MEG3/DLK1 locus in human clinically nonfunctioning pituitary adenomas. J Clin Endocrinol Metab 93:4119-4125. doi: 10.1210/jc.2007-2633
14. Greenman Y, Stern N (2009) Non-functioning pituitary adenomas. Best Pract Res Clin Endocrinol Metab 23:625-638. doi: 10.1016/j.beem.2009.05.005
15. Gulzar ZG, McKenney JK, Brooks JD (2013) Increased expression of NuSAP in recurrent prostate cancer is mediated by E2F1. Oncogene 32:70-77. doi: 10.1038/onc.2012.27
16. Guo IC, Shih MC, Lan HC, Hsu NC, Hu MC, Chung BC (2007) Transcriptional regulation of human CYP11A1 in gonads and adrenals. J Biomed Sci 14:509-515. doi: 10.1007/s11373-007-9177-z
17. Hammer F, Compagnone NA, Vigne JL, Bair SR, Mellon SH (2004) Transcriptional regulation of P450scc gene expression in the embryonic rodent nervous system. Endocrinology 145:901-912. doi: 10.1210/en.2003-0125
18. Hardy J (1979) The transsphenoidal surgical approach to the pituitary. Hosp Pract 14:81-89
19. Hussaini IM, Trotter C, Zhao Y et al (2007) Matrix metalloproteinase-9 is differentially expressed in nonfunctioning invasive and noninvasive pituitary adenomas and increases invasion in human pituitary adenoma cell line. Am J Pathol 170:356-365. doi: 10.2353/ajpath.2007.060736
20. Ikuyama S, Mu YM, Ohe K et al (1998) Expression of an orphan nuclear receptor DAX-1 in human pituitary adenomas. Clin Endocrinol 48:647-654. doi: 10.1046/j.1365-2265.1998.00477.x
21. Iyer J, Moghe S, Furukawa M, Tsai MY (2011) What's Nu(SAP) in mitosis and cancer? Cell Signal 23:991-998. doi: 10.1016/j.cellsig.2010.11.006
22. Jiang Z, Gui S, Zhang Y (2012) Analysis of differential gene expression in plurihormonal pituitary adenomas using bead-based fiber-optic arrays. J Neurooncol 108:341-348. doi: 10.1007/s11060-011-0792-1
23. Kelberman D, Rizzoti K, Lovell-Badge R, Robinson IC, Dattani MT (2009) Genetic regulation of pituitary gland development in human and mouse. Endocr Rev 30:790-829. doi: 10.1210/er.2009-0008
24. Lee M, Theodoropoulou M, Graw J, Roncaroli F, Zatelli MC, Pellegata NS (2011) Levels of p27 sensitize to dual PI3 K/mTOR inhibition. Mol Cancer Ther 10:1450-1459. doi: 10.1158/1535-7163.MCT-11-0188
25. Machiavelli GA, Rivolta CM, Artese R, Basso A, Burdman JA (1998) Expression of c-myc and c-fos and binding sites for estradiol and progesterone in human pituitary tumors. Neurol Res 20:709-712
26. Marinoni I, Lee M, Mountford S et al (2013) Characterization of MENX-associated pituitary tumours. Neuropathol Appl Neurobiol 39:256-269. doi: 10.1111/j.1365-2990.2012.01278.x
27. Melmed S (2011) Pathogenesis of pituitary tumors. Nat Rev Endocrinol 7:257-266. doi: 10.1038/nrendo.2011.40
28. Michaelis KA, Knox AJ, Xu M et al (2011) Identification of growth arrest and DNA-damage-inducible gene beta (GADD45beta) as a novel tumor suppressor in pituitary gonadotrope tumors. Endocrinology 152:3603-3613. doi: 10.1210/en.2011-0109
29. Molatore S, Kiermaier E, Jung CB et al (2010) Characterization of a naturally-occurring p27 mutation predisposing to multiple endocrine tumors. Mol Cancer 9:116. doi: 10.1186/1476-4598-9-116
30. Molatore S, Liyanarachchi S, Irmler M et al (2010) Pheochromocytoma in rats with multiple endocrine neoplasia (MENX) shares gene expression patterns with human pheochromocytoma. Proc Natl Acad Sci USA 107:18493-18498. doi: 10.1073/pnas.1003956107
31. Moreno CS, Evans CO, Zhan X, Okor M, Desiderio DM, Oyesiku NM (2005) Novel molecular signaling and classification of human clinically nonfunctional pituitary adenomas identified by gene expression profiling and proteomic analyses. Cancer Res 65:10214-10222. doi: 10.1158/0008-5472.CAN-05-0884
32. Morris DG, Musat M, Czirjak S et al (2005) Differential gene expression in pituitary adenomas by oligonucleotide array analysis. Eur J Endocrinol/Eur Fed Endocr Soc 153:143-151. doi: 10.1530/eje.1.01937
33. Pellegata NS, Quintanilla-Martinez L, Siggelkow H et al (2006) Germ-line mutations in p27Kip1 cause a multiple endocrine neoplasia syndrome in rats and humans. Proc Natl Acad Sci USA 103:15558-15563. doi: 10.1073/pnas.0603877103
34. Pereira AM, Biermasz NR (2012) Treatment of nonfunctioning pituitary adenomas: what were the contributions of the last 10 years? A critical view. Ann Endocrinol 73:111-116. doi: 10.1016/j.ando.2012.04.002
35. Raemaekers T, Ribbeck K, Beaudouin J et al (2003) NuSAP, a novel microtubule-associated protein involved in mitotic spindle organization. J Cell Biol 162:1017-1029. doi: 10.1083/jcb.200302129
36. Rainer J, Sanchez-Cabo F, Stocker G, Sturn A, Trajanoski Z (2006) CARMAweb: comprehensive R- and bioconductor-based web service for microarray data analysis. Nucleic Acids Res 34:W498-W503. doi: 10.1093/nar/gkl038
37. Scheithauer BW, Kovacs K, Zorludemir S, Lloyd RV, Erdogan S, Slezak J (2008) Immunoexpression of androgen receptor in the nontumorous pituitary and in adenomas. Endocr Pathol 19:27-33. doi: 10.1007/s12022-007-9012-0
38. Teplyuk NM, Zhang Y, Lou Y et al (2009) The osteogenic transcription factor runx2 controls genes involved in sterol/steroid metabolism, including CYP11A1 in osteoblasts. Mol Endocrinol 23:849-861. doi: 10.1210/me.2008-0270
39. Ueta Y, Levy A, Powell MP et al (1998) Neuronal nitric oxide synthase gene expression in human pituitary tumours: a possible association with somatotroph adenomas and growth hormone-releasing hormone gene expression. Clin Endocrinol 49:29-38. doi: 10.1046/j.1365-2265.1998.00399.x
40. Val P, Martinez-Barbera JP, Swain A (2007) Adrenal development is initiated by Cited2 and Wt1 through modulation of Sf-1 dosage. Development 134:2349-2358. doi: 10.1242/dev.004390
41. Vigneron S, Prieto S, Bernis C, Labbe JC, Castro A, Lorca T (2004) Kinetochore localization of spindle checkpoint proteins: who controls whom? Mol Biol Cell 15:4584-4596. doi: 10.1091/mbc.E04-01-0051
42. Wang SM, Ooi LL, Hui KM (2011) Upregulation of Rac GTPase-activating protein 1 is significantly associated with the early recurrence of human hepatocellular carcinoma. Clin Cancer Res: Off J Am Assoc Cancer Res 17:6040-6051. doi: 10.1158/1078-0432.CCR-11-0557
43. Wierinckx A, Auger C, Devauchelle P et al (2007) A diagnostic marker set for invasion, proliferation, and aggressiveness of prolactin pituitary tumors. Endocr Relat Cancer 14:887-900. doi: 10.1677/ERC-07-0062
44. Yao X, Abrieu A, Zheng Y, Sullivan KF, Cleveland DW (2000) CENP-E forms a link between attachment of spindle microtubules to kinetochores and the mitotic checkpoint. Nat Cell Biol 2:484-491. doi: 10.1038/35019518
45. Zhan X, Desiderio DM (2010) Signaling pathway networks mined from human pituitary adenoma proteomics data. BMC Med Genomics 3:13. doi: 10.1186/1755-8794-3-13
46. Zou H, McGarry TJ, Bernal T, Kirschner MW (1999) Identification of a vertebrate sister-chromatid separation inhibitor involved in transformation and tumorigenesis. Science 285:418-422. doi: 10.1126/science.285.5426.418