Persistent Prop1 expression delays gonadotrope differentiation and enhances pituitary tumor susceptibility

Human Molecular Genetics

Volumn 10, Issue 11, 2001, Pages 1141-1153

  Cushman, Lisa J ^a   Watkins Chow, Dawn E ^a   Brinkmeier, Michelle L ^a   Raetzman, Lori T ^a   Radak, Amy L ^a   Lloyd, Ricardo V ^b   Camper, Sally A ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; HOMEODOMAIN PROTEIN; TRANSCRIPTION FACTOR; TRANSITION FACTOR PROP 1; UNCLASSIFIED DRUG;

ADENOHYPOPHYSIS; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER SUSCEPTIBILITY; CELL DIFFERENTIATION; CELL FUNCTION; CONTROLLED STUDY; DELAYED PUBERTY; DEVELOPMENT; ENDOCRINE DISEASE; ENDOCRINE TUMOR; FEMALE; GENE MUTATION; GENE SILENCING; GONADOTROPE; HORMONE SYNTHESIS; HYPOGONADISM; HYPOPHYSIS ADENOMA; HYPOPHYSIS CELL; HYPOPHYSIS TUMOR; HYPOTHYROIDISM; MALE; MOUSE; NONHUMAN; PRIMORDIAL GERM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RATHKE CLEFT CYST; REGULATORY MECHANISM; THYROTROPE;

ANIMALIA;

EID: 0035872952     PISSN: 09646906     EISSN: None     Source Type: Journal    
DOI: 10.1093/hmg/10.11.1141     Document Type: Article

References (70)

1. Procter, A.M., Phillips, J.A., III and Cooper, D.N. (1998) The molecular genetics of growth hormone deficiency. Hum. Genet., 103, 255-272.
2. Asa, S. and Ezzat, S. (1998) The cytogenesis and pathogenesis of pituitary adenomas. Endocr. Rev., 19, 798-827.
3. Watkins-Chow, D.E. and Camper, S.A. (1998) How many homeobox genes does it take to make a pituitary gland? Trends Genet., 14, 284-290.
4. Dasen, J.S. and Rosenfeld, M.G. (1999) Combinatorial codes in signaling and synergy: lessons from pituitary development. Curr. Opin. Genet. Dev., 9, 566-574.
5. Carbajo-Perez, E., Motegi, M. and Watanabe, Y.G. (1989) Cell proliferation in the anterior pituitary of mice during growth. Biomed. Res., 10, 275-281.
6. Japon, M.A., Rubinstein, M. and Low, M.J. (1994) In situ hybridization analysis of anterior pituitary hormone gene expression during fetal mouse development. J. Histochem. Cytochem., 42, 1117-1125.
7. Somson, M.W., Wu, W., Dasen, J.S., Flynn, S.E., Norman, D.J., O'Connell, S.M., Gukovsky, I., Carrière, C., Ryan, A.K., Miller, A.P. et al. (1996) Pituitary lineage determination by the Prophet of Pit-1 homeodomain factor defective in Ames dwarfism. Nature, 384, 327-333.
8. Gage, P.J., Roller, M.L., Saunders, T.L., Scarlett, L.M. and Camper, S.A. (1996) Anterior pituitary cells defective in the cell autonomous factor, df, undergo cell lineage specification but not expansion. Development, 122, 151-160.
9. Tang, K., Bartke, A., Gardiner, C.S., Wagner, T.E. and Yun, J.S. (1993) Gonadotropin secretion, synthesis, and gene expression in human growth hormone transgenic mice and in Ames dwarf mice. Endocrinology, 132, 2518-2524.
10. Wu, W., Cogan, J.D., Pfaffle, R.W., Dasen, J.S., Frisch, H., O'Connell, S.M., Flynn, S.E., Brown, M.R., Mullis, P.E., Parks, J.S. et al. (1998) Mutations in PROP1 cause familial combined pituitary hormone deficiency. Nature Genet., 18, 147-149.
11. Parker, G.E., Sloop, K.W. and Rhodes, S.J. (2001) Transciptional control of the development and function of the hypothalamic-pituitary axis. In Eugster, E.A. and Pescovitz, O.H. (eds). Developmental Endocrinology: for Research to Clinical Practice. Humana Press, Totowa, NJ, in press.
12. Dattani, M.T. and Robinson, I.C. (2000) The molecular basis for developmental disorders of the pituitary gland in man. Clin. Genet., 57, 337-346.
13. Cogan, J., Wu, W., Phillips, J.I., Arnhold, I., Agapito, A., Fofanova, O., Osorio, M., Bircan, I., Moreno, A. and Mendonca, B. (1998) The PROP1 2-base pair deletion is a common cause of combined pituitary hormone deficiency. J. Clin. Endocrinol. Metab., 83, 3346-3349.
14. Pernasetti, F., Toledo, S.P., Vasilyev, V.V., Hayashida, C.Y., Cogan, J.D., Ferrari, C., Lourenco, D.M. and Mellon, P.L. (2000) Impaired adrenocorticotropin-adrenal axis in combined pituitary hormone deficiency caused by a two-base pair deletion (301-302delAG) in the prophet of Pit-1 gene. J. Clin. Endocrinol. Metab., 85, 390-397.
15. Flück, C., Deladoey, J., Rutishauser, K., Eblé, A., Marti, U., Wu, W. and Mullis, P.E. (1998) Phenotypic variability in familial combined pituitary hormone deficiency caused by a PROP1 gene mutation resulting in the substitution of Arg→Cys at codon 120 (R120C)*. J. Clin. Endocrinol. Metab., 83, 3727-3734.
16. Hermesz, E., Mackem, S. and Mahon, K.A. (1996) Rpx: A novel anterior-restricted homeobox gene progressively activated in the prechordal plate, anterior neural plate, and Rathke's pouch of the mouse embryo. Development, 122, 41-52.
17. Anderson, B., Pearse, R.V., II, Jenne, K., Sornson, M., Lin, S.-C., Bartke, A. and Rosenfeld, M.G. (1995) The Ames dwarf gene is required for Pit-1 gene activation. Dev. Biol., 172, 495-503.
18. Gage, P.J., Brinkmeier, M.L., Scarlett, L.M., Knapp, L.T., Camper, S.A. and Mahon, K.A. (1996) The Ames dwarf gene, df, is required early in pituitary ontogeny for the extinction of Rpx transcription and initiation of lineage specific cell proliferation. Mol. Endocrinol., 10, 1570-1581.
19. Li. S., Crenshaw, E.B. III, Rawson, E.J., Simmons, D.M., Swanson, L.W. and Rosenfeld, M.G. (1990) Dwarf locus mutants lacking three pituitary cell types result from mutations in the POU-domain gene Pit-1. Nature, 347, 528-533.
20. Kendall, S.K., Gordon, D.F., Birkmeier, T.S., Petrey, D., Sarapura, V.D., O'Shea, K.S., Wood, W.M., Lloyd, R.V., Ridgway, E.C. and Camper, S.A. (1994) Enhancer-mediated high level expression of mouse pituitary glycoprotein hormone α-subunit transgene in thyrotropes, gonadotropes, and developing pituitary gland. Mol. Endocrinol., 8, 1420-1433.
21. Burrows, H.L., Birkmeier, T.S., Seasholtz, A.F. and Camper, S.A. (1996) Targeted ablation of cells in the pituitary primordia of transgenic mice. Mol. Endocrinol., 10, 1467-1477.
22. Bartke, A. (1965) The response of two types of dwarf mice to growth hormone, thyrotropin, and thyroxine. Gen. Comp. Endocrinol., 5, 418-426.
23. Kulig, E., Camper, S.A., Kuecker, S., Jin, L. and Lloyd, R.V. (1998) Remodeling of hyperplastic pituitaries in hypothyroid α-subunit knockout mice after thyroxine and 17β-estradiol treatment: role of apoptosis. Endocr. Pathol., 9, 261-274.
24. Alarid, E.T., Windle, J.J., Whyte, D.B. and Mellon, P.L. (1996) Immortalization of pituitary cells at discrete stages of development by directed oncogenesis in transgenic mice. Development, 122, 3319-3329.
25. Jameson, J.L. (1996) Inherited disorders of the gonadotropin hormones. Mol. Cell. Endocrinol, 125, 143-149.
26. Risma, K.A., Clay, C.M., Nett, T.M., Yun, J. and Nilson, J.H. (1995) Targeted overexpression of luteinizing hormone in transgenic mice leads to infertility, polycystic ovaries, and ovarian tumors. Proc. Natl Acad. Sci. USA, 92, 1322-1326.
27. Shenker, A., Laue, L., Kosugi, S., Merendino, J.J., Jr. Minegishi, T. and Cutler, G.B., Jr (1993) A constitutively activating mutation of the luteinizing hormone receptor in familial male precocious puberty. Nature, 365, 652-654.
28. Risma, K.A., Hirshfield, A.N. and Nilson, J.H. (1997) Elevated luteinizing hormone in prepubertal transgenic mice causes hyperandrogenemia, precocious puberty, and substantial ovarian pathology. Endocrinology, 138, 3540-3547.
29. Lyon, M.F., Cattanach, B.M. and Charlton, H.M. (1981) In Austin, C.R. and Edwards, R.G. (eds), Mechanisms of Sex Differentiation in Animals and Man, Academic Press, New York, NY, pp. 329-275.
30. Charlton, H.M., Halpin, D.M., Iddon, C., Rosie, R., Levy, G., McDowell, I.F., Megson, A., Morris, J.F., Bramwell, A., Speight, A. et al. (1983) The effects of daily administration of single and multiple injections of gonadotropin-releasing hormone on pituitary and gonadal function in the hypogonadal (hpg) mouse. Endocrinology, 113, 535-544.
31. Nishizono, H., Soji, T. and Herbert, D.C. (1993) Intercellular communication within the rat anterior pituitary gland: V. Changes in cell-to-cell communications is a function of the timing of castration in male rats. Anat. Rec., 235, 577-582.
32. Lloyd, R.V. (1993) Ultrastructural diagnosis of pituitary adenomas and hyperplasias. In Livolsi, V.A. (ed.), Surgical Pathology of the Pituitary Gland, Vol. 27. W.B. Saunders Co., Philadelphia, PA, 52-84.
33. Kovacs, K. and Asa, S.L. (1991) Functional Endocrine Pathology, Vol. 1. Blackwell Scientific Publications, Boston, MA.
34. Yoshida, J., Kobayashi, T., Kageyama, N. and Kanzaki, M. (1977) Symptomatic Rathke's cleft cyst. Morphological study with light and electron microscopy and tissue culture. J. Neurosurg., 47, 451-458.
35. Steinberg, G.K., Koenig, G.H. and Golden, J.B. (1982) Symptomatic Rathke's cleft cysts. Report of two cases. J. Neurosurg., 56, 290-295.
36. Fofanova, O., Takamura, N., Kinoshita, E., Vorontsov, A., Vladimirova, V., Dedov, I., Peterkova, V. and Yamashita, S. (2000) MR imaging of the pituitary gland in children and young adults with congenital combined pituitary hormone deficiency associated with PROP1 mutations. Am. J. Roentgenol., 174, 555-559.
37. Helfand, M. and Redfern, C.C. (1998) Clinical guideline, part 2. Screening for thyroid disease: an update. American College of Physicians [Published erratum appears in Ann. Intern. Med. (1999), 130, 246.]. Ann. Intern. Med., 129, 144-158.
38. Windle, J.J., Weiner, R.I. and Mellon, P.L. (1990) Cell lines of the pituitary gonadotrope lineage derived by targeted oncogenesis in transgenic mice. Mol. Endocrinol., 4, 597-603.
39. Lee, S.L., Sadovsky, Y., Swirnoff, A.M., Polish, J.A., Coda, P., Gavrilina, G. and Milbrandt, J. (1996) Luteinizing hormone deficiency and female infertility in mice lacking the transcription factor NGF1-A (Egr-1). Science, 273, 1219-1221.
40. Topilko, P., Schneider-Maunoury, S., Levi, G., Trembleau, A., Gourdji, D., Driancourt, M.-A., Rao, C.V. and Charnay, P. (1998) Multiple pituitary and ovarian detects in Krox-24 (NGF1-A, Egr-1)-targeted mice. Mol. Endocrinol., 12, 107-122.
41. Tortora, G.J. and Grabowski, S.R. (1996) In Roesch, B. (ed.), Principles of Anatomy and Physiology, HarperCollins Publishers, New York, NY, pp. 501-550.
42. Kendall, S.K., Samuelson, L.C., Saunders, T.L., Wood, R.I. and Camper, S.A. (1995) Targeted disruption of the pituitary glycoprolein hormone α-subunit produces hypogonadal and hypothyroid mice. Genes Dev., 9, 2007-2019.
43. Stahl, J., Kendall, S., Brinkmeier, M., Greco, T., Watkins-Chow, D., Canpos-Barros, A., Lloyd, R. and Camper, S. (1999) Thyroid hormone is essential for pituitary somatotropes and lactotropes. Endocrinology, 140, 1884-1892.
44. Luo, X., Ikeda, Y. and Parker, K.L. (1994) A cell-specific nuclear receptor is essential for adrenal and gonadal development and sexual differentiation. Cell, 77, 481-490.
45. Acampora, D., Mazan, S., Tuorto, F., Avantaggiato, V., Tremblay, J.J., Lazzaro, D., di Carlo, A., Mariano, A., Macchia, P.E., Corte, G. et al. (1998) Transient dwarfism and hypogonadism in mice lacking Otx1 reveal prepubescent stage-specific control of pituitary levels of GH. FSH and LH. Development, 125, 1229-1239.
46. Firulli, A. and Olson, E. (1997) Modular regulation of muscle gene transcription: a mechanism for muscle cell diversity. Trends Genet., 13, 364-369.
47. Knudson, A.G. (1996) Hereditary cancer: two hits revisited. J. Cancer Res. Clin. Oncol., 122, 135-140.
48. McComb, D.J., Kovacs, K., Beri, J., Zak, F., Milligan, J.V. and Shin, S.H. (1985) Pituitary gonadotroph adenomas in old Sprague-Dawley rats. J. Submicrosc. Cytol., 17, 517-530.
49. Asa, S. (1999) The pathology of pituitary tumors. Endocrinol. Metab. Clin. North Am., 28, 13-43.
50. Shimon, I. and Melmed, S. (1997) Genetic basis of endocrine disease: pituitary tumor pathogenesis. J. Clin. Endocrinol. Metab., 82, 1675-1681.
51. Kumar, T.R., Graham, K.E., Asa, S.L. and Low, M.J. (1998) Simian virus 40 T antigen-induced gonadotroph adenomas: a model for human null cell adenomas. Endocrinology, 139, 3342-3351.
52. Nakamura, Y., Usui, T., Mizuta, H., Murabe, H., Muro, S., Suda, M., Tanaka, K., Tanaka, I., Shimatsu, A. and Nakao, K. (1999) Characterization of Prophet of Pit-1 gene expression in normal pituitary and pituitary adenomas in humans. J. Clin. Endocrinol. Metab., 84, 1414-1419.
53. Nakamura, S., Ohtsuru, A., Takamura, N., Kitange, G., Tokunaga, Y., Yasunaga, A., Shibata, S. and Yamashita, S. (1999) Prop-1 gene expression in human pituitary tumors. J. Clin. Endocrinol. Metab., 84, 2581-2584.
54. Usui, T., Nakamura, Y., Mizuta, H., Murabe, H., Muro, S., Suda, M., Tanaka, I., Shimatsu, A. and Nakao, K. (2000) Functional significance of Prop-1 gene expression in pituitary adenomas. Endocr. J., 47, S85-S89.
55. Skelly, R.H., Korbonits, M., Grossman, A., Besser, G.M., Monson, J.P., Geddes, J.F. and Burrin, J.M. (2000) Expression of the pituitary transcription factor Ptx-1, hut not that of the trans-activating factor Prop-1, is reduced in human corticotroph adenomas and is associated with decreased α-subunit secretion. J. Clin. Endocrinol. Metab., 85, 2537-2542.
56. Akita, S., Readhead, C., Stefaneanu, L., Fine, J., Tampanaru-Sarmesiu, A., Kovacs, K. and Melmed, S. (1997) Pituitary-directed leukemia inhibitory factor transgene forms Rathke's cleft cysts and impairs adult pituitary function. J. Clin. Invest., 99, 2462-2469.
57. Yano, H., Readhead, C., Nakashima, M., Ren, S. and Melmed, S. (1998) Pituitary-directed leukemia inhibitory factor transgene causes Cushing's syndrome: neuro-immune-endocrine modulation of pituitary development. Mol. Endocrinol., 12, 1708-1720.
58. Shen, M.M. and Leder, P. (1992) Leukemia inhibitory factor is expressed by the preimplantation uterus, selectively blocks primitive ectoderm formation in vitro. Proc. Natl Acad. Sci. USA, 91, 8240-8244.
59. Mark, M., Fijli, F.M. and Chambon, P. (1997) Homeobox genes in embryogenesis and pathogenesis. Pediatr. Res., 42, 421-429.
60. Ostrom, L., Tang, M., Gruss, P. and Dressler, G. (2000) Reduced Pax2 gene dosage increases apoptosis and slows the progression of renal cystic disease. Dev. Biol., 219, 250-258.
61. Pfeffer, P., Bouchard, M. and Busslinger, M. (2000) Pax2 and homeodomain proteins cooperatively regulate a 435 bp enhancer of the mouse Pax5 gene at the midbrain-hindbrain boundary. Development, 127, 1017-1028.
62. Freund, C., Horsford, D.J. and McInnes, R. (1996) Transcription factor genes and the developing eye: a genetic perspective. Hum. Mol. Genet., 5, 1471-1488.
63. Torres, M., Gomez-Pardo, E. Dressler, G.R. and Gruss, P. (1995) Pax-2 controls multiple steps of urogenital development. Development, 121, 4057-4065.
64. Keller, S.A., Jones, J.M., Boyle, A., Barrow, L.L., Killen, P.D., Green, D.G., Kapousta, N.V., Hitchcock, P.P., Swank, R.T. and Meisler, M.H. (1994) Kidney and retinal defects (Krd), a transgene-induced mutation with a deletion of mouse chromosome 19 that includes the Pax2 locus. Genomics, 23, 309-320.
65. 1Neu mutation is identical to a human PAX2 mutation in a family with renal-coloboma syndrome and results in developmental detects of the brain, ear, eye, and kidney. Proc. Natl Acad. Sci. USA, 93, 13870-13875.
66. Sanyanusin, P., Schimmenti, L.A., McNoe, L.A., Ward, T.A., Pierpont, M.E.M., Sullivan, M.J., Dobyns, W.B. and Eccles, M.R. (1995) Mutation of the Pax2 gene in a family with optic nerve colobomas, renal anomalies and vesicoureteral reflux. Nature Genet., 9, 358-364.
67. Dressler, G.R., Wilkinson, J.E., Rothenpieler, U.W., Patterson, L.T., Williams-Simons, L. and Westphal, H. (1993) Deregulation of Pax-2 expression in transgenic mice generates severe kidney abnormalities. Nature, 362, 65-67.
68. Winyard, P.J.D., Risdon, R.A., Sams, V.R., Dressler, G.R. and Woolf, A.S. (1996) The PAX2 transcription factor is expressed in cystic and hyperproliferative dysplastic epithelia in human kidney malformations. J. Clin. Invest., 98, 451-459.
69. Hogan, B., Beddington, R., Costantini, F. and Lacey, E. (1994) Manipulating the Mouse Embryo: A Laboratory Manual, Cold Spring Harbor Laboratory Press, Plainview, New York, NY.
70. Mannheim, B. (1996) Nonradioactive In Situ Hybridization Application Manual, 2nd ed., Boehringer Mannheim GmbH, Biochemica, Germany.