Animal models of pituitary neoplasia

Molecular and Cellular Endocrinology

Volumn 421, Issue , 2016, Pages 68-81

  Lines, K E ^a   Stevenson, M ^a   Thakker, R V ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Adenoma; Carcinoma; Mouse; Multiple endocrine neoplasia type 1; Pituitary; Rat

Indexed keywords

COMPLEMENTARY DNA; MEN1 PROTEIN, HUMAN; ONCOPROTEIN;

ARTICLE; CARCINOGENESIS; DISEASE ASSOCIATION; DISEASE MODEL; DNA SEQUENCE; EMBRYONIC STEM CELL; GENE; GENE DELETION; GENE EDITING; GENE OVEREXPRESSION; GENETIC ASSOCIATION; GENETIC PROCEDURES; HUMAN; HYPOPHYSIS TUMOR; MULTIPLE ENDOCRINE NEOPLASIA TYPE 1; MUTATIONAL ANALYSIS; NONHUMAN; PITUITARY TRANSFORMING GENE; PRIORITY JOURNAL; TISSUE SPECIFICITY; ANIMAL; ANIMAL MODEL; GENETICS; MOUSE; PATHOLOGY; PITUITARY NEOPLASMS; RAT; ZEBRA FISH;

ANIMALS; HUMANS; MICE; MODELS, ANIMAL; PITUITARY NEOPLASMS; PROTO-ONCOGENE PROTEINS; RATS; ZEBRAFISH;

EID: 84953636268     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2015.08.024     Document Type: Article

References (136)

1. Abbud R.A., Takumi I., Barker E.M., Ren S.G., Chen D.Y., Wawrowsky K., Melmed S. Early multipotential pituitary focal hyperplasia in the alpha-subunit of glycoprotein hormone-driven pituitary tumor-transforming gene transgenic mice. Mol. Endocrinol. 2005, 19:1383-1391.
2. Acevedo-Arozena A., Wells S., Potter P., Kelly M., Cox R.D., Brown S.D. ENU mutagenesis, a way forward to understand gene function. Annu. Rev. Genomics Hum. Genet. 2008, 9:49-69.
3. Agarwal S.K., Mateo C.M., Marx S.J. Rare germline mutations in cyclin-dependent kinase inhibitor genes in multiple endocrine neoplasia type 1 and related states. J. Clin. Endocrinol. Metab. 2009, 94:1826-1834.
4. Alatzoglou K.S., Andoniadou C.L., Kelberman D., Buchanan C.R., Crolla J., Arriazu M.C., Roubicek M., Moncet D., Martinez-Barbera J.P., Dattani M.T. SOX2 haploinsufficiency is associated with slow progressing hypothalamo-pituitary tumours. Hum. Mutat. 2011, 32:1376-1380.
5. Angotzi A.R., Mungpakdee S., Stefansson S., Male R., Chourrout D. Involvement of Prop1 homeobox gene in the early development of fish pituitary gland. Gen. Comp. Endocrinol. 2011, 171:332-340.
6. Asa S.L., Kovacs K., Hammer G.D., Liu B., Roos B.A., Low M.J. Pituitary corticotroph hyperplasia in rats implanted with a medullary thyroid carcinoma cell line transfected with a corticotropin-releasing hormone complementary deoxyribonucleic acid expression vector. Endocrinology 1992, 131:715-720.
7. Asa S.L., Kovacs K., Stefaneanu L., Horvath E., Billestrup N., Gonzalez-Manchon C., Vale W. Pituitary adenomas in mice transgenic for growth hormone-releasing hormone. Endocrinology 1992, 131:2083-2089.
8. Asa S.L., Kelly M.A., Grandy D.K., Low M.J. Pituitary lactotroph adenomas develop after prolonged lactotroph hyperplasia in dopamine D2 receptor-deficient mice. Endocrinology 1999, 140:5348-5355.
9. Bahar A., Simpson D.J., Cutty S.J., Bicknell J.E., Hoban P.R., Holley S., Mourtada-Maarbouni M., Williams G.T., Clayton R.N., Farrell W.E. Isolation and characterization of a novel pituitary tumor apoptosis gene. Mol. Endocrinol. 2004, 18:1827-1839.
10. Bai F., Chan H.L., Smith M.D., Kiyokawa H., Pei X.H. p19Ink4d is a tumor suppressor and controls pituitary anterior lobe cell proliferation. Mol. Cell Biol. 2014, 34:2121-2134.
11. Beckers A., Aaltonen L.A., Daly A.F., Karhu A. Familial isolated pituitary adenomas (FIPA) and the pituitary adenoma predisposition due to mutations in the aryl hydrocarbon receptor interacting protein (AIP) gene. Endocr. Rev. 2013, 34:239-277.
12. Bello M.J., De Campos J.M., Isla A., Casartelli C., Rey J.A. Promoter CpG methylation of multiple genes in pituitary adenomas: frequent involvement of caspase-8. Oncol. Rep. 2006, 15:443-448.
13. Bentley L., Esapa C.T., Nesbit M.A., Head R.A., Evans H., Lath D., Scudamore C.L., Hough T.A., Podrini C., Hannan F.M., Fraser W.D., Croucher P.I., Brown M.A., Brown S.D., Cox R.D., Thakker R.V. An N-ethyl-N-nitrosourea induced corticotropin-releasing hormone promoter mutation provides a mouse model for endogenous glucocorticoid excess. Endocrinology 2014, 155:908-922.
14. Bertolino P., Tong W.M., Galendo D., Wang Z.Q., Zhang C.X. Heterozygous Men1 mutant mice develop a range of endocrine tumors mimicking multiple endocrine neoplasia type 1. Mol. Endocrinol. 2003, 17:1880-1892.
15. Bertolino P., Tong W.M., Herrera P.L., Casse H., Zhang C.X., Wang Z.Q. Pancreatic beta-cell-specific ablation of the multiple endocrine neoplasia type 1 (MEN1) gene causes full penetrance of insulinoma development in mice. Cancer Res. 2003, 63:4836-4841.
16. Besson A., Gurian-West M., Chen X., Kelly-Spratt K.S., Kemp C.J., Roberts J.M. A pathway in quiescent cells that controls p27Kip1 stability, subcellular localization, and tumor suppression. Genes Dev. 2006, 20:47-64.
17. Biondi C., Gartside M., Tonks I., Paterson C., Hayward N.K., Kay G.F. Targeting and conditional inactivation of the murine Men1 locus using the Cre recombinase: loxP system. Genesis 2002, 32:150-151.
18. Biondi C.A., Gartside M.G., Waring P., Loffler K.A., Stark M.S., Magnuson M.A., Kay G.F., Hayward N.K. Conditional inactivation of the MEN1 gene leads to pancreatic and pituitary tumorigenesis but does not affect normal development of these tissues. Mol. Cell Biol. 2004, 24:3125-3131.
19. Buslei R., Kreutzer J., Hofmann B., Schmidt V., Siebzehnrubl F., Hahnen E., Eyupoglu I.Y., Fahlbusch R., Blumcke I. Abundant hypermethylation of SOCS-1 in clinically silent pituitary adenomas. Acta Neuropathol. 2006, 111:264-271.
20. Carlus M., Elies L., Fouque M.C., Maliver P., Schorsch F. Historical control data of neoplastic lesions in the Wistar Hannover Rat among eight 2-year carcinogenicity studies. Exp. Toxicol. Pathol. 2013, 65:243-253.
21. Chesnokova V., Kovacs K., Castro A.V., Zonis S., Melmed S. Pituitary hypoplasia in Pttg-/- mice is protective for Rb+/- pituitary tumorigenesis. Mol. Endocrinol. 2005, 19:2371-2379.
22. Cicenas J., Kalyan K., Sorokinas A., Jatulyte A., Valiunas D., Kaupinis A., Valius M. Highlights of the latest advances in research on CDK inhibitors. Cancers (Basel) 2014, 6:2224-2242.
23. Collins F.S., Rossant J., Wurst W. A mouse for all reasons. Cell 2007, 128:9-13.
24. Collins F.S., Finnell R.H., Rossant J., Wurst W. A new partner for the international knockout mouse consortium. Cell 2007, 129:235.
25. Crabtree J.S., Scacheri P.C., Ward J.M., Garrett-Beal L., Emmert-Buck M.R., Edgemon K.A., Lorang D., Libutti S.K., Chandrasekharappa S.C., Marx S.J., Spiegel A.M., Collins F.S. A mouse model of multiple endocrine neoplasia, type 1, develops multiple endocrine tumors. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:1118-1123.
26. Crabtree J.S., Scacheri P.C., Ward J.M., McNally S.R., Swain G.P., Montagna C., Hager J.H., Hanahan D., Edlund H., Magnuson M.A., Garrett-Beal L., Burns A.L., Ried T., Chandrasekharappa S.C., Marx S.J., Spiegel A.M., Collins F.S. Of mice and MEN1: Insulinomas in a conditional mouse knockout. Mol. Cell Biol. 2003, 23:6075-6085.
27. Cruz-Soto M.E., Scheiber M.D., Gregerson K.A., Boivin G.P., Horseman N.D. Pituitary tumorigenesis in prolactin gene-disrupted mice. Endocrinology 2002, 143:4429-4436.
28. Cushman L.J., Watkins-Chow D.E., Brinkmeier M.L., Raetzman L.T., Radak A.L., Lloyd R.V., Camper S.A. Persistent Prop1 expression delays gonadotrope differentiation and enhances pituitary tumor susceptibility. Hum. Mol. Genet. 2001, 10:1141-1153.
29. De Martino I., Visone R., Wierinckx A., Palmieri D., Ferraro A., Cappabianca P., Chiappetta G., Forzati F., Lombardi G., Colao A., Trouillas J., Fedele M., Fusco A. HMGA proteins up-regulate CCNB2 gene in mouse and human pituitary adenomas. Cancer Res. 2009, 69:1844-1850.
30. Donangelo I., Gutman S., Horvath E., Kovacs K., Wawrowsky K., Mount M., Melmed S. Pituitary tumor transforming gene overexpression facilitates pituitary tumor development. Endocrinology 2006, 147:4781-4791.
31. Dusing-Swartz S., Medina D., Butel J.S., Socher S.H. Mouse mammary tumor virus genome expression in chemical carcinogen-induced mammary tumors in low- and high-tumor-incidence mouse strains. Proc. Natl. Acad. Sci. U. S. A. 1979, 76:5360-5364.
32. Egashira N., Minematsu T., Miyai S., Takekoshi S., Camper S.A., Osamura R.Y. Pituitary changes in Prop1 transgenic mice: hormone producing tumors and signet-ring type gonadotropes. Acta Histochem. Cytochem. 2008, 41:47-57.
33. Ezzat S., Zheng L., Zhu X.F., Wu G.E., Asa S.L. Targeted expression of a human pituitary tumor-derived isoform of FGF receptor-4 recapitulates pituitary tumorigenesis. J. Clin. Investig. 2002, 109:69-78.
34. Fedele M., Battista S., Kenyon L., Baldassarre G., Fidanza V., Klein-Szanto A.J., Parlow A.F., Visone R., Pierantoni G.M., Outwater E., Santoro M., Croce C.M., Fusco A. Overexpression of the HMGA2 gene in transgenic mice leads to the onset of pituitary adenomas. Oncogene 2002, 21:3190-3198.
35. Fedele M., Pentimalli F., Baldassarre G., Battista S., Klein-Szanto A.J., Kenyon L., Visone R., De Martino I., Ciarmiello A., Arra C., Viglietto G., Croce C.M., Fusco A. Transgenic mice overexpressing the wild-type form of the HMGA1 gene develop mixed growth hormone/prolactin cell pituitary adenomas and natural killer cell lymphomas. Oncogene 2005, 24:3427-3435.
36. Fedele M., Visone R., De Martino I., Troncone G., Palmieri D., Battista S., Ciarmiello A., Pallante P., Arra C., Melillo R.M., Helin K., Croce C.M., Fusco A. HMGA2 induces pituitary tumorigenesis by enhancing E2F1 activity. Cancer Cell 2006, 9:459-471.
37. Fero M.L., Rivkin M., Tasch M., Porter P., Carow C.E., Firpo E., Polyak K., Tsai L.H., Broudy V., Perlmutter R.M., Kaushansky K., Roberts J.M. A syndrome of multiorgan hyperplasia with features of gigantism, tumorigenesis, and female sterility in p27(Kip1)-deficient mice. Cell 1996, 85:733-744.
38. Fero M.L., Randel E., Gurley K.E., Roberts J.M., Kemp C.J. The murine gene p27Kip1 is haplo-insufficient for tumour suppression. Nature 1998, 396:177-180.
39. Fisher E.M., Lana-Elola E., Watson S.D., Vassiliou G., Tybulewicz V.L. New approaches for modelling sporadic genetic disease in the mouse. Dis. Model Mech. 2009, 2:446-453.
40. Franklin D.S., Godfrey V.L., Lee H., Kovalev G.I., Schoonhoven R., Chen-Kiang S., Su L., Xiong Y. CDK inhibitors p18(INK4c) and p27(Kip1) mediate two separate pathways to collaboratively suppress pituitary tumorigenesis. Genes Dev. 1998, 12:2899-2911.
41. Friedel R.H., Plump A., Lu X., Spilker K., Jolicoeur C., Wong K., Venkatesh T.R., Yaron A., Hynes M., Chen B., Okada A., McConnell S.K., Rayburn H., Tessier-Lavigne M. Gene targeting using a promoterless gene trap vector ("targeted trapping") is an efficient method to mutate a large fraction of genes. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:13188-13193.
42. Fritz A., Walch A., Piotrowska K., Rosemann M., Schaffer E., Weber K., Timper A., Wildner G., Graw J., Hofler H., Atkinson M.J. Recessive transmission of a multiple endocrine neoplasia syndrome in the rat. Cancer Res. 2002, 62:3048-3051.
43. Gaston-Massuet C., Andoniadou C.L., Signore M., Jayakody S.A., Charolidi N., Kyeyune R., Vernay B., Jacques T.S., Taketo M.M., Le Tissier P., Dattani M.T., Martinez-Barbera J.P. Increased Wingless (Wnt) signaling in pituitary progenitor/stem cells gives rise to pituitary tumors in mice and humans. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:11482-11487.
44. Giacomini D., Paez-Pereda M., Theodoropoulou M., Labeur M., Refojo D., Gerez J., Chervin A., Berner S., Losa M., Buchfelder M., Renner U., Stalla G.K., Arzt E. Bone morphogenetic protein-4 inhibits corticotroph tumor cells: involvement in the retinoic acid inhibitory action. Endocrinology 2006, 147:247-256.
45. Gillam M.P., Nimbalkar D., Sun L., Christov K., Ray D., Kaldis P., Liu X., Kiyokawa H. MEN1 tumorigenesis in the pituitary and pancreatic islet requires Cdk4 but not Cdk2. Oncogene 2015, 34:932-938.
46. Gittleman H., Ostrom Q.T., Farah P.D., Ondracek A., Chen Y., Wolinsky Y., Kruchko C., Singer J., Kshettry V.R., Laws E.R., Sloan A.E., Selman W.R., Barnholtz-Sloan J.S. Descriptive epidemiology of pituitary tumors in the United States, 2004-2009. J. Neurosurg. 2014, 121:527-535.
47. Gordon J.W., Scangos G.A., Plotkin D.J., Barbosa J.A., Ruddle F.H. Genetic transformation of mouse embryos by microinjection of purified DNA. Proc. Natl. Acad. Sci. U. S. A. 1980, 77:7380-7384.
48. Guidi C.J., Mudhasani R., Hoover K., Koff A., Leav I., Imbalzano A.N., Jones S.N. Functional interaction of the retinoblastoma and Ini1/Snf5 tumor suppressors in cell growth and pituitary tumorigenesis. Cancer Res. 2006, 66:8076-8082.
49. Hall B., Limaye A., Kulkarni A.B. Overview: generation of gene knockout mice. Curr. Protoc. Cell Biol. 2009, 12:1-17. (Chapter 19), Unit 19 12 19.
50. Harding B., Lemos M.C., Reed A.A., Walls G.V., Jeyabalan J., Bowl M.R., Tateossian H., Sullivan N., Hough T., Fraser W.D., Ansorge O., Cheeseman M.T., Thakker R.V. Multiple endocrine neoplasia type 1 knockout mice develop parathyroid, pancreatic, pituitary and adrenal tumours with hypercalcaemia, hypophosphataemia and hypercorticosteronaemia. Endocr. Relat. Cancer 2009, 16:1313-1327.
51. Haruyama N., Cho A., Kulkarni A.B. Overview: engineering transgenic constructs and mice. Curr. Protoc. Cell Biol. 2009, 10. (Chapter 19), Unit 19.
52. Harvey M., Vogel H., Lee E.Y., Bradley A., Donehower L.A. Mice deficient in both p53 and Rb develop tumors primarily of endocrine origin. Cancer Res. 1995, 55:1146-1151.
53. Helseth A., Siegal G.P., Haug E., Bautch V.L. Transgenic mice that develop pituitary tumors. A model for Cushing's disease. Am. J. Pathol. 1992, 140:1071-1080.
54. Hiyama H., Kubo O., Kawamata T., Ishizaki R., Hori T. Expression of cyclin kinase inhibitor p21/WAF1 protein in pituitary adenomas: correlations with endocrine activity, but not cell proliferation. Acta Neurochir. (Wien) 2002, 144:481-488.
55. Jacks T., Fazeli A., Schmitt E.M., Bronson R.T., Goodell M.A., Weinberg R.A. Effects of an Rb mutation in the mouse. Nature 1992, 359:295-300.
56. Jaffrain-Rea M.L., Rotondi S., Alesse E. New insights in the pathogenesis of pituitary tumours. Hot Topics in Endocrine and Endocrine-related Diseases 2013, D.M. Fedele (Ed.).
57. Jian F., Cao Y., Bian L., Sun Q. USP8: a novel therapeutic target for Cushing's disease. Endocrine 2015, 10.1007/s12020-015-0682-y.
58. Jordan S., Lidhar K., Korbonits M., Lowe D.G., Grossman A.B. Cyclin D and cyclin E expression in normal and adenomatous pituitary. Eur. J. Endocrinol. 2000, 143:R1-R6.
59. Karga H.J., Alexander J.M., Hedleywhyte E.T., Klibanski A., Jameson J.L. Ras mutations in human pituitary-tumors. J. Clin. Endocrinol. Metab. 1992, 74:914-919.
60. Kawashima S.T., Usui T., Sano T., Iogawa H., Hagiwara H., Tamanaha T., Tagami T., Naruse M., Hojo M., Takahashi J.A., Shimatsu A. P53 gene mutation in an atypical corticotroph adenoma with Cushing's disease. Clin. Endocrinol. (Oxf) 2009, 70:656-657.
61. Kelly M.A., Rubinstein M., Asa S.L., Zhang G., Saez C., Bunzow J.R., Allen R.G., Hnasko R., Ben-Jonathan N., Grandy D.K., Low M.J. Pituitary lactotroph hyperplasia and chronic hyperprolactinemia in dopamine D2 receptor-deficient mice. Neuron 1997, 19:103-113.
62. Kirschner L.S. PRKAR1A and the evolution of pituitary tumors. Mol. Cell. Endocrinol. 2010, 326:3-7.
63. Kiyokawa H., Kineman R.D., Manova-Todorova K.O., Soares V.C., Hoffman E.S., Ono M., Khanam D., Hayday A.C., Frohman L.A., Koff A. Enhanced growth of mice lacking the cyclin-dependent kinase inhibitor function of p27(Kip1). Cell 1996, 85:721-732.
64. Korsisaari N., Ross J., Wu X., Kowanetz M., Pal N., Hall L., Eastham-Anderson J., Forrest W.F., Van Bruggen N., Peale F.V., Ferrara N. Blocking vascular endothelial growth factor-A inhibits the growth of pituitary adenomas and lowers serum prolactin level in a mouse model of multiple endocrine neoplasia type 1. Clin. Cancer Res. 2008, 14:249-258.
65. Kumar T.R., Graham K.E., Asa S.L., Low M.J. Simian virus 40 T antigen-induced gonadotroph adenomas: a model of human null cell adenomas. Endocrinology 1998, 139:3342-3351.
66. Lemos M.C., Thakker R.V. Multiple endocrine neoplaslia type 1 (MEN 1): analysis of 1336 mutations reported in the first decade following identification of the gene. Hum. Mutat. 2008, 29:22-32.
67. Lemos M.C., Harding B., Reed A.A., Jeyabalan J., Walls G.V., Bowl M.R., Sharpe J., Wedden S., Moss J.E., Ross A., Davidson D., Thakker R.V. Genetic background influences embryonic lethality and the occurrence of neural tube defects in Men1 null mice: relevance to genetic modifiers. J. Endocrinol. 2009, 203:133-142.
68. Leontiou C.A., Gueorguiev M., van der Spuy J., Quinton R., Lolli F., Hassan S., Chahal H.S., Igreja S.C., Jordan S., Rowe J., Stolbrink M., Christian H.C., Wray J., Bishop-Bailey D., Berney D.M., Wass J.A., Popovic V., Ribeiro-Oliveira A., Gadelha M.R., Monson J.P., Akker S.A., Davis J.R., Clayton R.N., Yoshimoto K., Iwata T., Matsuno A., Eguchi K., Musat M., Flanagan D., Peters G., Bolger G.B., Chapple J.P., Frohman L.A., Grossman A.B., Korbonits M. The role of the aryl hydrocarbon receptor-interacting protein gene in familial and sporadic pituitary adenomas. J. Clin. Endocrinol. Metab. 2008, 93:2390-2401.
69. Levy A. Molecular and trophic mechanisms of tumorigenesis. Endocrinol. Metab. Clin. N. Am. 2008, 37:23.
70. Liu N.A., Jiang H., Ben-Shlomo A., Wawrowsky K., Fan X.M., Lin S., Melmed S. Targeting zebrafish and murine pituitary corticotroph tumors with a cyclin-dependent kinase (CDK) inhibitor. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:8414-8419.
71. Lloyd R.V., Ruebel K.H., Zhang S., Jin L. Pituitary hyperplasia in glycoprotein hormone alpha subunit-, p18(INK4C)-, and p27(kip-1)-null mice: analysis of proteins influencing p27(kip-1) ubiquitin degradation. Am. J. Pathol. 2002, 160:1171-1179.
72. Loffler K.A., Biondi C.A., Gartside M., Waring P., Stark M., Serewko-Auret M.M., Muller H.K., Hayward N.K., Kay G.F. Broad tumor spectrum in a mouse model of multiple endocrine neoplasia type 1. Int. J. Cancer 2007, 120:259-267.
73. Loffler K.A., Biondi C.A., Gartside M.G., Serewko-Auret M.M., Duncan R., Tonks I.D., Mould A.W., Waring P., Muller H.K., Kay G.F., Hayward N.K. Lack of augmentation of tumor spectrum or severity in dual heterozygous Men1 and Rb1 knockout mice. Oncogene 2007, 26:4009-4017.
74. Low M.J., Liu B., Hammer G.D., Rubinstein M., Allen R.G. Post-translational processing of proopiomelanocortin (POMC) in mouse pituitary melanotroph tumors induced by a POMC-simian virus 40 large T antigen transgene. J. Biol. Chem. 1993, 268:24967-24975.
75. Machens A., Schaaf L., Karges W., Frank-Raue K., Bartsch D.K., Rothmund M., Schneyer U., Goretzki P., Raue F., Dralle H. Age-related penetrance of endocrine tumours in multiple endocrine neoplasia type 1 (MEN1): a multicentre study of 258 gene carriers. Clin. Endocrinol. 2007, 67:613-622.
76. Mantovani G., Lania A.G., Spada A. GNAS imprinting and pituitary tumors. Mol. Cell. Endocrinol. 2010, 326:15-18.
77. Marinoni I., Lee M., Mountford S., Perren A., Bravi I., Jennen L., Feuchtinger A., Drouin J., Roncaroli F., Pellegata N.S. Characterization of MENX-associated pituitary tumours. Neuropathol. Appl. Neurobiol. 2013, 39:256-269.
78. Martin G.R. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc. Natl. Acad. Sci. U. S. A. 1981, 78:7634-7638.
79. McAndrew J., Paterson A.J., Asa S.L., McCarthy K.J., Kudlow J.E. Targeting of transforming growth factor-alpha expression to pituitary lactotrophs in transgenic mice results in selective lactotroph proliferation and adenomas. Endocrinology 1995, 136:4479-4488.
80. Michael S.K., Brennan J., Robertson E.J. Efficient gene-specific expression of cre recombinase in the mouse embryo by targeted insertion of a novel IRES-Cre cassette into endogenous loci. Mech. Dev. 1999, 85:35-47.
81. Michaelis K.A., Knox A.J., Xu M., Kiseljak-Vassiliades K., Edwards M.G., Geraci M., Kleinschmidt-DeMasters B.K., Lillehei K.O., Wierman M.E. Identification of growth arrest and DNA-damage-inducible gene beta (GADD45 beta) as a novel tumor suppressor in pituitary gonadotrope tumors. Endocrinology 2011, 152:3603-3613.
82. Mitsui T., Ishida M., Izawa M., Arita J. Differences between rat strains in the development of PRL-secreting pituitary tumors with long-term estrogen treatment: In vitro insulin-like growth factor-1-induced lactotroph proliferation and gene expression are affected in Wistar-Kyoto rats with low estrogen-susceptibility. Endocr. J. 2013, 60:1251-1259.
83. Nakayama K., Ishida N., Shirane M., Inomata A., Inoue T., Shishido N., Horii I., Loh D.Y. Mice lacking p27(Kip1) display increased body size, multiple organ hyperplasia, retinal dysplasia, and pituitary tumors. Cell 1996, 85:707-720.
84. Pagotto U., Arzberger T., Theodoropoulou M., Grubler Y., Pantaloni C., Saeger W., Losa M., Journot L., Stalla G.K., Spengler D. The expression of the antiproliferative gene ZAC is lost or highly reduced in nonfunctioning pituitary adenomas. Cancer Res. 2000, 60:6794-6799.
85. Pardi E., Mariotti S., Pellegata N.S., Benfini K., Borsari S., Saponaro F., Torregrossa L., Cappai A., Satta C., Mastinu M., Marcocci C., Cetani F. Functional characterization of a CDKN1B mutation in a Sardinian kindred with multiple endocrine neoplasia type 4 (MEN4). Endocr. Connect. 2014.
86. Pei L., Melmed S. Isolation and characterization of a pituitary tumor-transforming gene (PTTG). Mol. Endocrinol. 1997, 11:433-441.
87. Pei L., Melmed S., Scheithauer B., Kovacs K., Benedict W.F., Prager D. Frequent loss of heterozygosity at the retinoblastoma susceptibility gene (RB) locus in aggressive pituitary-tumors - evidence for a chromosome-13 tumor-suppressor gene other than RB. Cancer Res. 1995, 55:1613-1616.
88. Pellegata N.S., Quintanilla-Martinez L., Siggelkow H., Samson E., Bink K., Hofler H., Fend F., Graw J., Atkinson M.J. Germ-line mutations in p27Kip1 cause a multiple endocrine neoplasia syndrome in rats and humans. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:15558-15563.
89. Peng H., Liu H., Zhao S., Wu J., Fan J., Liao J. Silencing of RASSF3 by DNA hypermethylation is associated with tumorigenesis in somatotroph adenomas. PLoS One 2013, 8:e59024.
90. Piret S.E., Thakker R.V. Mouse models for inherited endocrine and metabolic disorders. J. Endocrinol. 2011, 211:211-230.
91. Qian Z.R., Sano T., Yoshimoto K., Yamada S., Ishizuka A., Mizusawa N., Horiguchi H., Hirokawa M., Asa S.L. Inactivation of RASSF1A tumor suppressor gene by aberrant promoter hypermethylation in human pituitary adenomas. Lab. Invest. 2005, 85:464-473.
92. Qian Z.R., Sano T., Yoshimoto K., Asa S.L., Yamada S., Mizusawa N., Kudo E. Tumor-specific downregulation and methylation of the CDH13 (H-cadherin) and CDH1 (E-cadherin) genes correlate with aggressiveness of human pituitary adenomas. Mod. Pathol. 2007, 20:1269-1277.
93. Raappana A., Koivukangas J., Ebeling T., Pirila T. Incidence of pituitary adenomas in northern Finland in 1992-2007. J. Clin. Endocrinol. Metab. 2010, 95:4268-4275.
94. Raitila A., Lehtonen H.J., Arola J., Heliovaara E., Ahlsten M., Georgitsi M., Jalanko A., Paetau A., Aaltonen L.A., Karhu A. Mice with inactivation of aryl hydrocarbon receptor-interacting protein (Aip) display complete penetrance of pituitary adenomas with aberrant ARNT expression. Am. J. Pathol. 2010, 177:1969-1976.
95. Reincke M., Sbiera S., Hayakawa A., Theodoropoulou M., Osswald A., Beuschlein F., Meitinger T., Mizuno-Yamasaki E., Kawaguchi K., Saeki Y., Tanaka K., Wieland T., Graf E., Saeger W., Ronchi C.L., Allolio B., Buchfelder M., Strom T.M., Fassnacht M., Komada M. Mutations in the deubiquitinase gene USP8 cause Cushing's disease. Nat. Genet. 2015, 47:31-38.
96. Righi A., Jin L., Zhang S., Stilling G., Scheithauer B.W., Kovacs K., Lloyd R.V. Identification and consequences of galectin-3 expression in pituitary tumors. Mol. Cell Endocrinol. 2010, 326:8-14.
97. Rosenberg D.W., Giardina C., Tanaka T. Mouse models for the study of colon carcinogenesis. Carcinogenesis 2009, 30:183-196.
98. Roussel-Gervais A., Bilodeau S., Vallette S., Berthelet F., Lacroix A., Figarella-Branger D., Brue T., Drouin J. Cooperation between cyclin e and p27(Kip1) in pituitary tumorigenesis. Mol. Endocrinol. 2010, 24:1835-1845.
99. Saez C., Japon M.A., Ramos-Morales F., Romero F., Segura D.I., Tortolero M., Pintor-Toro J.A. hpttg is over-expressed in pituitary adenomas and other primary epithelial neoplasias. Oncogene 1999, 18:5473-5476.
100. Salehi F., Kovacs K., Scheithauer B.W., Lloyd R.V., Cusimano M. Pituitary tumor-transforming gene in endocrine and other neoplasms: a review and update. Endocr Relat. Cancer 2008, 15:721-743.
101. Scheithauer B.W., Gaffey T.A., Lloyd R.V., Sebo T.J., Kovacs K.T., Horvath E., Yapicier O., Young W.F., Meyer F.B., Kuroki T., Riehle D.L., Laws E.R. Pathobiology of pituitary adenomas and carcinomas. Neurosurgery 2006, 59:341-353.
102. Schuff K.G., Hentges S.T., Kelly M.A., Binart N., Kelly P.A., Iuvone P.M., Asa S.L., Low M.J. Lack of prolactin receptor signaling in mice results in lactotroph proliferation and prolactinomas by dopamine-dependent and -independent mechanisms. J. Clin. Invest. 2002, 110:973-981.
103. Seruggia D., Montoliu L. The new CRISPR-Cas system: RNA-guided genome engineering to efficiently produce any desired genetic alteration in animals. Transgen. Res. 2014, 23:707-716.
104. Simpson D.J., Clayton R.N., Farrell W.E. Preferential loss of death associated protein kinase expression in invasive pituitary tumours is associated with either CpG island methylation or homozygous deletion. Oncogene 2002, 21:1217-1224.
105. Solnica-Krezel L., Schier A.F., Driever W. Efficient recovery of ENU-induced mutations from the zebrafish germline. Genetics 1994, 136:1401-1420.
106. Son W.C., Gopinath C. Early occurrence of spontaneous tumors in CD-1 mice and Sprague-Dawley rats. Toxicol. Pathol. 2004, 32:371-374.
107. Son W.C., Bell D., Taylor I., Mowat V. Profile of early occurring spontaneous tumors in Han Wistar rats. Toxicol. Pathol. 2010, 38:292-296.
108. Sotillo R., Dubus P., Martin J., de la Cueva E., Ortega S., Malumbres M., Barbacid M. Wide spectrum of tumors in knock-in mice carrying a Cdk4 protein insensitive to INK4 inhibitors. EMBO J. 2001, 20:6637-6647.
109. Sotillo R., Renner O., Dubus P., Ruiz-Cabello J., Martin-Caballero J., Barbacid M., Carnero A., Malumbres M. Cooperation between Cdk4 and p27kip1 in tumor development: a preclinical model to evaluate cell cycle inhibitors with therapeutic activity. Cancer Res. 2005, 65:3846-3852.
110. Stanford W.L., Cohn J.B., Cordes S.P. Gene-trap mutagenesis: past, present and beyond. Nat. Rev. Genet. 2001, 2:756-768.
111. Stefaneanu L., Rindi G., Horvath E., Murphy D., Polak J.M., Kovacs K. Morphology of adenohypophysial tumors in mice transgenic for vasopressin-SV40 hybrid oncogene. Endocrinology 1992, 130:1789-1795.
112. Stenzel-Poore M.P., Cameron V.A., Vaughan J., Sawchenko P.E., Vale W. Development of Cushing's syndrome in corticotropin-releasing factor transgenic mice. Endocrinology 1992, 130:3378-3386.
113. Stewart C., Parente F., Piehl F., Farnebo F., Quincey D., Silins G., Bergman L., Carle G.F., Lemmens I., Grimmond S., Xian C.Z., Khodei S., Teh B.T., Lagercrantz J., Siggers P., Calender A., Van de Vem V., Kas K., Weber G., Hayward N., Gaudray P., Larsson C. Characterization of the mouse Men1 gene and its expression during development. Oncogene 1998, 17:2485-2493.
114. Tanizaki Y., Jin L., Scheithauer B.W., Kovacs K., Roncaroli F., Lloyd R.V. P53 gene mutations in pituitary carcinomas. Endocr. Pathol. 2007, 18:217-222.
115. Thakker R.V. Multiple endocrine neoplasia type 1 (MEN1). Best. Pract. Res. Clin. Endocrinol. Metab. 2010, 24:355-370.
116. Thakker R.V. Multiple endocrine neoplasia type 1 (MEN1) and type 4 (MEN4). Mol. Cell. Endocrinol. 2013, (in press).
117. Tjornstrand A., Gunnarsson K., Evert M., Holmberg E., Ragnarsson O., Rosen T., Filipsson Nystrom H. The incidence rate of pituitary adenomas in western Sweden for the period 2001-2011. Eur. J. Endocrinol. 2014, 171:519-526.
118. Tsai K.Y., MacPherson D., Rubinson D.A., Nikitin A.Y., Bronson R., Mercer K.L., Crowley D., Jacks T. ARF mutation accelerates pituitary tumor development in Rb+/- mice. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:16865-16870.
119. Verges B., Boureille F., Goudet P., Murat A., Beckers A., Sassolas G., Cougard P., Chambe B., Montvernay C., Calender A., Grp Etud Neoplasies E. Pituitary disease in MEN type 1 (MEN1): data from the France-Belgium MEN1 multicenter study. J. Clin. Endocrinol. Metab. 2002, 87:457-465.
120. Vierimaa O., Georgitsi M., Lehtonen R., Vahteristo P., Kokko A., Raitila A., Tuppurainen K., Ebeling T.M., Salmela P.I., Paschke R., Gundogdu S., De Menis E., Makinen M.J., Launonen V., Karhu A., Aaltonen L.A. Pituitary adenoma predisposition caused by germline mutations in the AIP gene. Science 2006, 312:1228-1230.
121. Vlotides G., Eigler T., Melmed S. Pituitary tumor-transforming gene: physiology and implications for tumorigenesis. Endocr. Rev. 2007, 28:165-186.
122. Vooijs M., van der Valk M., te Riele H., Berns A. Flp-mediated tissue-specific inactivation of the retinoblastoma tumor suppressor gene in the mouse. Oncogene 1998, 17:1-12.
123. Vooijs M., Jonkers J., Lyons S., Berns A. Noninvasive imaging of spontaneous retinoblastoma pathway-dependent tumors in mice. Cancer Res. 2002, 62:1862-1867.
124. Waalkes M.P. Cadmium carcinogenesis. Mutat. Res. 2003, 533:107-120.
125. Walls G.V., Lemos M.C., Javid M., Bazan-Peregrino M., Jeyabalan J., Reed A.A.C., Harding B., Tyler D.J., Stuckey D.J., Piret S., Christie P.T., Ansorge O., Clarke K., Seymour L., Thakker R.V. MEN1 gene replacement therapy reduces proliferation rates in a mouse model of pituitary adenomas. Cancer Res. 2012, 72:5060-5068.
126. Wang H., Yang H., Shivalila C.S., Dawlaty M.M., Cheng A.W., Zhang F., Jaenisch R. One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell 2013, 153:910-918.
127. Weinberg R.A. The retinoblastoma protein and cell cycle control. Cell 1995, 81:323-330.
128. Westerman B.A., Blom M., Tanger E., van der Valk M., Song J.Y., van Santen M., Gadiot J., Cornelissen-Steijger P., Zevenhoven J., Prosser H.M., Uren A., Aronica E., van Lohuizen M. GFAP-Cre-mediated transgenic activation of Bmi1 results in pituitary tumors. PLoS One 2012, 7:e35943.
129. Wiklund J., Wertz N., Gorski J. A comparison of estrogen effects on uterine and pituitary growth and prolactin synthesis in F344 and Holtzman rats. Endocrinology 1981, 109:1700-1707.
130. Wiklund J., Rutledge J., Gorski J. A genetic model for the inheritance of pituitary tumor susceptibility in F344 rats. Endocrinology 1981, 109:1708-1714.
131. Yates C.J., Lines K.E., Thakker R.V. Molecular genetic advances in pituitary tumor development. Expert Rev. Endocrinol. Metab. 2014, 10:35-53.
132. Yin Z., Williams-Simons L., Parlow A.F., Asa S., Kirschner L.S. Pituitary-specific knockout of the Carney complex gene Prkar1a leads to pituitary tumorigenesis. Mol. Endocrinol. 2008, 22:380-387.
133. Zhang X., Rice K., Wang Y., Chen W., Zhong Y., Nakayama Y., Zhou Y., Klibanski A. Maternally expressed gene 3 (MEG3) noncoding Ribonucleic Acid: Isoform structure, expression, and functions. Endocrinology 2010, 151:939-947.
134. Zhou Y., Zhang X., Klibanski A. Genetic and epigenetic mutations of tumor suppressive genes in sporadic pituitary adenoma. Mol. Cell. Endocrinol. 2013.
135. Zhu X., Lee K., Asa S.L., Ezzat S. Epigenetic silencing through DNA and histone methylation of fibroblast growth factor receptor 2 in neoplastic pituitary cells. Am. J. Pathol. 2007, 170:1618-1628.
136. Zindy F., Nilsson L.M., Nguyen L., Meunier C., Smeyne R.J., Rehg J.E., Eberhart C., Sherr C.J., Roussel M.F. Hemangiosarcomas, medulloblastomas, and other tumors in Ink4c/p53-null mice. Cancer Res. 2003, 63:5420-5427.