Contributions of immunohistochemistry and in situ hybridization to the functional analysis of pituitary adenomas

Journal of Histochemistry and Cytochemistry

Volumn 48, Issue 4, 2000, Pages 445-458

  Osamura, R Yoshiyuki ^a   Tahara, Shigeyuki ^b   Kurotani, Reiko ^a   Sanno, Naoko ^b   Matsuno, Akira ^c   Teramoto, Akira ^b  

^a TOKAI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b NIPPON MEDICAL SCHOOL   (Japan)

^c TEIKYO UNIVERSITY CHIBA MEDICAL CENTER   (Japan)

Author keywords

Immunohistochemistry; In situ hybridization; Nuclear receptor steroid receptor pituitary hormone hypothalamic hormone; Pituitary adenoma; Transcription factor

Indexed keywords

CELL NUCLEUS RECEPTOR; CORTICOTROPIN; FOLLITROPIN; GROWTH HORMONE; HORMONE; HORMONE PRECURSOR; HYPOPHYSIS HORMONE; HYPOTHALAMUS HORMONE; ISOPROPAMIDE IODIDE; LUTEINIZING HORMONE; MESSENGER RNA; PEPTIDE; PROLACTIN; PROTEIN; STEROID RECEPTOR; THYROTROPIN; TRANSCRIPTION FACTOR;

HUMAN; HYPOPHYSIS ADENOMA; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; NONHUMAN; PRIORITY JOURNAL; REVIEW;

EID: 0034115119     PISSN: 00221554     EISSN: None     Source Type: Journal    
DOI: 10.1177/002215540004800401     Document Type: Review

References (119)

1. Acampora D, Mazan S, Francesca T, Avantaggiato V, Tremblay JJ, Lazzaro D, Carlo A, Mariano A, Macchia PE, Corte G, Macchia V, Drouin J, Brulet P, Simeone A (1998) Transient dwarfism and hypogonadism in mice lacking Otx1 revel prepubescent stage-specific control of pituitary levels of GH, FSH and LH. Development 125:1229-1239
2. Aguado F, Majo G, Ruiz-Montasell B, Canals JM, Casanova A, Marsal J, Blasi J (1996) Expression of synaptosomal-associated protein SNAP-25 in endocrine anterior pituitary cells. Eur J Cell Biol 69:351-359
3. Allenby G, Bocquel MT, Saunders M, Kazmer S, Speck J, Rosenberger M, Lovey A, Kastner P, Grippo JF, Chambon P, Levin AA (1993) Retinoc acid receptors and retinoid X receptors. Interactions with endogenous retinoic acids. Proc Natl Acad Sci USA 90:30-34
4. Asa SL, Pu LA, Lew AM (1993) Cell type-specific expression of the pituitary transcription activator Pit-1 in the human pituitary and pituitary adenomas. J Clin Endocrinol Metab 77:1275-1280
5. Asa SL, Bamberger AM, Cao B, Wong M, Parker KL, Ezzat S (1996) The transcription activator steroidogenic factor-1 is preferentially expressed in the human pituitary gonadotroph. J Clin Ednocrinol Metab 81:2165-2170
6. Bach I, Carriere C, Ostendorff HP, Andersen B, Rosenfeld MG (1997) A family of LIM domain-associated cofactors confer transcriptional synergism between LIM and Otx homeodomain proteins. Genes Dev 11:1370-1380
7. Baldini G, Hohl T, Lin HY, Lodish HF (1992) Cloning of a Rab3 isotype predominately expressed in adipocytes. Proc Natl Acad Sci USA 89:5049-5052
8. Berrodin TJ, Marks MS, Ozato K, Linney E, Lazar MA (1992) Heterodimerization among thyroid hormone receptor, retinoic acid receptor, retinoid X receptor, COUP transcription factor and an endogenous liver protein. Mol Endocrinol 6:1469-1487
9. Bloomquist BT, Eipper BA, Mains RE (1991) Prohormone-converting enzymes: regulation and evaluation of function using antisense RNA. Mol Endocrinol 5:2014-2024
10. Bodner M, Castrillo JL, Theill LE, Deerinck T, Ellisman M, Karin M (1988) The pituitary-specific transcription factor GHF-1 is a homeobox-containing protein. Cell 55:505-518
11. Bourne HR (1988) Do GTPases direct membrane traffic in secretion? Cell 53:669-671
12. Camper SA, Saunders TL, Katz RW (1990) The Pit-1transcription factor gene is a candidate for the murine Snell dwarf mutation. Genomics 8:586-590
13. Castrillo JL, Theill LE, Karin M (1991) Function of the homeodomein protein GHF 1 in pituitary cell proliferation. Science 253:197-199
14. Chance RE, Ellis RM, Bromer WW (1968) Porcine proinsulin: characterization and amino acid sequence. Science 161:165-167
15. Chretien M, Li CH (1967) Isolation, purification, and characterization of γ-lipotropic hormone from sheep pituitary glands. Can J Biochem 45:1163-1174
16. Craxton M, Goedert M (1995) Synaptotagmin V: a novel synaptotagmin isoform expressed in rat brain. FEBS Lett 361:196-200
17. Davis KD, Berrodin TJ, Stelmach JE, Winkler JD, Lazar MA (1994) Endogenous retinoid X receptors can function as hormone receptors in pituitary cells. Mol Cell Biol 14:7105-7110
18. Destephano DB, Lloyd RV, Pike AM, Wilson BS (1988) Pituitary adenomas: an immunohistochemical study of hormone production and chromogranin localization. Am J Pathol 116:464-472
19. Dolle P, Castrillo JL, Theill LE, Deerinck T, Ellisman M, Karin M (1990) Expression of GHF-1 protein in mouse pituitaries correlates both temporally and spatially with the onset of growth hormone gene activity. Cell 60:809-820
20. Evans RM (1988) The steroid and thyroid hormone receptor superfamily. Science 240:889-895
21. Fischer von Mollard G, Mignery G, Baumert M, Perin MS, Hanson TJ, Burger PM, Jahn R, Sudhof TC (1990) Rab3 is a small GTP binding protein exclusively localized to synaptic vesicles. Proc Natl Acad Sci USA 87:1988-1992
22. Fischer von Mollard G, Stahl B, Khokhlatchev A, Sudhof TC, Jahn R (1994a) Rab3C is a synaptic vesicle protein that dissociates from synaptic vesicles after stimulation of exocytosis. J Biol Chem 269:10971-10974
23. Fischer von Mollard G, Stahl B, Li C, Sudhof TC, Jahn R (1994b) Rab proteins in regulated exocytosis. Trends Biochem Sci 19:164-168
24. Fischer von Mollard G, Sudhof TC, Jahn R (1991) A small GTP-binding protein dissociates from synaptic vesicles during exocytosis. Nature 349:79-81
25. Friend KE, Chiou YK, Laws ER (1993) Pit-1 messenger ribonucleic acid is differentially expressed in human pituitary adenomas. J Clin Endocrinol Metab 77:1281-1286
26. Gage PJ, Brinkmeier ML, Scarlett LM, Knapp LT, Camper SA, Mahon KA (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
27. Geppert M, Bolshakov VY, Siegelbaum SA, Takei K, Camilli PD, Hammer RE, Sudhof TC (1994) The role of Rab3A in neurotransmitter release. Nature 369:493-497
28. Hamada K, Gleason SL, Levi B-Z, Hirschfeld S, Appella E, Ozato K (1989) H-2RIIBP, a member of the nuclear hormone receptor superfamily that binds to both the regulatory element of major histocompatibility class I genes and the estrogen response element. Proc Natl Acad Sci USA 86: 8289-8293
29. Hashimoto K, Koga M, Kouhara H, Arita N, Hayakawa T, Kishimoto T, Sato B (1994) Expression patterns of messenger ribonucleic acids encoding prohormone convertases (PC2 and PC3) in human pituitary adenomas. Clin Endocrinol 41:185-191
30. Haugen BR, Gordon DF, Nelson AR, Wood WM, Ridgway EC (1994) The combination of Pit-1 and Pit-1T have a synergistic stimulatory effect on the thyrotropin β-subunit promoter but not the growth hormone or prolactin promoters. Mol Endocrinol 8:1574-1582
31. Hermesz E, Mackem S, Mahon KA (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
32. Heyman RA, Mangelsdorf DJ, Dyck JA, Stein RB, Eichele G, Evans RM, Thaller C (1992) 9-cis-Retinoid acid is a high affinity ligand for the retinoid X receptor. Cell 68:397-406
33. 2+-dependent exocytosis from adrenal chromaffin cells. J Biol Chem 269:10229-10234
34. Holz RW, Senter RA, Uhler MD (1995) Investigation by transient transfection of the effects on regulated exocytosis of Rab3a. Methods Enzymol 257:221-231
35. Honda S, Morohashi K, Nomura M, Takeya M, Kitajima M, Omura T (1993) Ad4BP regulating steroidogenic P-450 genes is a member of steroid hormone receptor superfamily. J Biol Chem 268:7494-7502.
36. Horvath E, Kovacs K (1980) Pathology of the pituitary gland. In Ezrin C, Horvath E, Kaufman B, Kovacs K, Weiss MH, eds. Pituitary Diseases. Boca Raton, FL, CRC Press, 1-83
37. Horvath E, Kovacs K (1992) Ultrastructural diagnosis of human pituitary adenomas. Microsc Res Tech 20:107-135
38. Ingraham HA, Chen, RP, Mangalam HJ, Elsholtz HP, Flynn SE, Lin CR, Simmons DM, Swanson L, Rosenfeld MG (1988) A tissue-specific transcription factor containing a homeodomain specifies a pituitary phenotype. Cell 55:519-529
39. Ingraham HA, Lala DS, Ikeda Y, Luo X, Shen WH, Nachtigal MW, Abbud R, Nilson JH, Parker KL (1994) The nuclear receptor steroidogenic factor 1 acts at multiple levels of the reproductive axis. Genes Dev 8:2302-2312
40. Inoue K, Hattori M, Sakai T, Inukai S, Fujimoto N, Ito A (1990) Establishment of a series of pituitary clonal cell lines differing in morphology, hormone secretion, and response to estrogen. Endocrinology 126:2313-2320
41. Itoh Y, Tanaka S, Takekoshi S, Itoh J, Osamura RY (1996) Prohormone converties (PC1/3 and PC2) in rat and human pancreas and islet cell tumors: subcellular immunohistochemical analysis Pathol Int 46:726-737
42. Johannes L, Lledo PM, Roa M, Vincent JD, Henry JP, Darchen F (1994) The GTPase Rab3a negatively controls calcium-dependent exocytosis in neuroendocrine cells. EMBO J 13:2029-2037
43. Keller H, Givel F, Perroud M, Wahli W (1995) Signaling cross-talk between peroxisome proliferator-activated receptor/retinoid X receptor and estrogen receptor through estrogen response elements. Mol Endocrinol 9:794-804
44. 3 signaling. Nature 355:446-449
45. Konzak KE, Moore DD (1992) Functional isoforms of Pit-1 generated by alternative messenger RNA splicing. Mol Endocrinol 6:241-247
46. Kovacs K, Horvath E (1986) Tumors of the Pituitary Gland. Atlas of Tumor Pathology. Fascicle 21, 2nd ser. Washington DC, Armed Forces Institute of Pathology.
47. Kovacs K, Horvath E (1987) Pathology of pituitary tumors. Endocrinol Metab Clin North Am 16:529-551
48. Lala DS, Rice DA, Parker KL (1992) Steroidogenic factor 1, a key regulator of steroidoginic enzyme expression, is the mouse homolog of fushi tarazu-factor 1. Mol Endocrinol 6:1249-1258
49. Lamonerie T, Tremblay JJ, Lanctot C, Therrien M, Gauthier Y, Drouin J (1996) Ptx1, a bicoid-related homeo box transcription factor involved in transcription of the pro-opiomelanocortin gene. Genes Dev 10:1284-1295
50. Lee JE, Hollenberg SM, Snider L, Turner DL, Lipnick N, Weintraub H (1995) Conversion of Xenopus ectoderm into neurons by NeuroD, a basic helix-loop-helix protein. Science 268:836-844
51. Leid M, Kastner P, Lyons R, Nakashatri H, Saunders M, Zacharewski T, Chen J-Y, Staub A, Garneri J-M, Mader S, Chambon P (1992) Purification, cloning, and RXR identity of the HeLa cell factor with which RAR or TR heterodimerizes to bind target sequences efficiently. Cell 68:377-395
52. Levine AA, Sturzenbecker LJ, Kazmer S, Bosakowski T, Huselton C, Allenby G, Speck J, Kratqeisen C, Rosenberger M, Lovery A, Grippo JF (1992) 9-cis-Retinoic acid stereoisomer binds and activates the nuclear receptor RXRα. Nature 355:359-361
53. 2+-dependent and -independent activities of neural and non-neural synaptotagmins. Nature 375:594-599
54. Li S, Crenshaw EB, Rawson EJ, Simmons DM, Swanson LW, Rosenfeld MG (1990) Dwarf locus mutants lacking three pituitary cell types result from mutations in the POU-domain gene Pit-1. Nature 347:528-533
55. 2+-dependent exocytosis in rat anterior pituitary cells. Nature 364:540-544
56. Lloyd RV, Iacangelo A, Eiden LE, Cano M, Jin L, Grimes M (1989) Chromogranin A and B messenger ribonucleic acids in pituitary and other normal and neoplastic human endocrine tissues. Lab Invest 60:548-556
57. Lloyd RV, Jin L (1994) Analysis of chromogranin/secretogranin messenger RNAs in human pituitary adenomas. Diagn Mol Pathol 3:38-45
58. Lloyd RV, Jin L (1995) In situ hybridization analysis of chromogranin A and B mRNAs in neuroendocrine tumors with digoxigenin-labeled oligonucleotide probe cocktails. Diagn Mol Pathol 143-151
59. Lloyd RV, Jin L, Fields K, Chandler WF, Horvath E, Stefaneanu L, Kovacs K (1991) Analysis of pituitary hormones and chromogranin A mRNAs in null cell adenomas, oncocytomas, and gonadotroph adenomas by in situ hybridization. Am J Pathol 139:553-564
60. Lloyd RV, Jin L, Song J (1990) Ultrastructural localization of prolactin and chromogranin B messenger ribonucleic acids with biotinylated oligonucleotide probes in cultured pituitary cells. Lab Invest 63:413-419
61. Lloyd RV, Long Jin, Qian X, Scheithauer BW, Young WF Jr, Davis DH (1995) Analysis of the chromogranin A post-translational product pancreastatin and the prohormone convertases PC2 and PC3 in normal and neoplastic human pituitarics. Am J Pathol 146:1188-1198
62. Lopes MB, Gaylinn BD, Thorner MO, Stoler MH (1997) Growth hormone-releasing hormone receptor mRNA in acromegalic pituitary tumors. Am J Pathol 150:1885-1891
63. Luo X, Ikeda Y, Parker KL (1994) A cell-specific nuclear receptor is essential for adrenal and gonadal development and sexual differentiation. Cell 77:481-490
64. Mangalam HJ, Albert VR, Ingraham HA, Kapiloff M, Wilson L, Nelson C, Elsholtz H, Rosenfeld MG (1989) A pituitary POU domain protein, Pit-1 activates both growth hormones and prolactin promoters transcriptionally. Genes Dev 3:946-958
65. Mangelsdorf DJ, Borgmeyer U, Heyman RA, Zhou JY, Ong ES, Oro AE, Kakizuka A, Evans RM (1992) Characterization of three RXR genes that mediate the action of 9-cis retinoic acid. Genes Dev 6:329-344
66. Mangelsdorf DJ, Ong ES, Dyck JA, Evans RM (1990) Nuclear receptor that identifies a novel retinoic acid response pathway. Nature 345:224-229
67. Mano H, Mori R, Ozawa T, Takeyama K, Yoshizawa Y, Kojima R, Arao Y, Masushige S, Kato S (1994) Positive and negative regulation of retinoid X receptor gene expression by thyroid hormone in the rat. J Biol Chem 269:1591-1594
68. Marks MS, Hallenheck PL, Nagata T, Segars JH, Appella E, Nikodem VM, Ozato K (1992) H2RIIBP (RXRβ) heterodimerization provides a mechanism for combinatorial diversity in the regulation of retinoic acid and thyroid hormone responsive genes. EMBO J 11:1419-1435
69. Marqueze B, Boudier JA, Mizuta M, Inagaki N, Seino S, Seagar M (1995) Cellular localization of synaptotagmin I, II, and III mRNAs in the central nervous system and pituitary and adrenal glands of the rat. J Neurosci 15:4906-4917
70. Matteoli M, Takei K, Cameron R, Hurlbut P, Johnston PA, Sudhof TC, Jahn R, Camilli PD (1991) Association of Rab3A with synaptic vesicles at late step of the secretory pathway. J Cell Biol 115:625-633
71. Mizoguchi A, Kim S, Ueda T, Kikuchi A, Yorifuji H, Hirokawa N, Takai Y (1990) Localization and subcellular distribution of smg p25A, a ras p21-like GTP-binding protein, in rat brain. J Biol Chem 265:11872-11879
72. Mizuta M, Inagaki N, Nemoto Y, Matsukura S, Takahashi M, Seino S (1994) Synaptotagmin III is a novel isoform of rat synaptotagmin expressed in endocrine and neuronal cells. J Biol Chem 269:11675-11678
73. Morohashi K, Honda S, Inomata Y, Handa H, Omura T (1992) A common trans-acting factor, Ad4-binding protein, to the promoters of steroidogenic P-450s. J Biol Chem 267:17913-17919
74. Morohashi K, Zanger UM, Honda S, Hara M, Waterman MR, Omura T (1993) Activation of CYP11A and CYP11B gene promoters by the steroidogenic cell-specific transcription factor, Ad4BP. Mol Endocrinol 7:1196-1204
75. Nakayama K, Ishida N, Shirane M, Inomata A, Inoue T, Shishido N, Horii I, Loh DY, Nakayama K (1996) Mice lacking p27 (Kip1) display increased body size, multiple organ hyperplasia, retinal dysplasia, and pituitary tumors. Cell May 85:707-720
76. Naya FJ, Stellrecht CMM, Tsai MJ (1995) Tissue-specific regulation of the insulin gene by a novel basic helix-loop-helix transcription factor. Genes Dev 9:1009-1019
77. Ohagi S, LaMendola J, LeBeau MM, Espinosa R III, Takeda J, Smeekens SP, Chan SJ, Steiner DF (1992) Identification and analysis of the gene encoding human PC2, a prohormone convertase expressed in neuroendocrine tissues. Proc Natl Acad Sci USA 89:4977-4981
78. Osamura RY, Chretien M, Marcinkiewicz M (1988) Ultrastructural localization of secretory granule constituent chromogranin and 7B2. Pathol Res Pract 183:617-619
79. Osamura RY, Oda K, Utsunomiya H, Inada K, Umemura S, Shibuya M, Katakami H, Voss JW, Mayo KF, Rosenfeld MG (1993) Immunohistochemical expression of PIT-1 protein in pituitary glands of human GRF transgenic mice: its relationship with hormonal expressions. Endocrinol J 40:133-139
80. Osamura RY, Sanno N, Teramoto A (1995) Clinical and cytofuntional classification of pituitary adenomas: proposal of a new classification. Endocrine Pathology 6:253-256
81. Otoh Y, Tanaka S, Takekoshi S, Itoh J, Osamura RY (1996) Prohormone convertases (PC1/PC3 and PC2) in rat and human pancreas and islet cell tumors: subcellular immunohistochemical analysis. Pathol Int 46:726-737
82. Pellegrini I, Barlier A, Gunz G (1994) Pit-1 gene expression in the human pituitary and pituitary adenomas. J Clin Endocrinol Metab 79:189-196
83. Phaffle RW, Di Mattia GE, Parks JS (1992) Mutation of the POU-specific domain of Pit-1 and hypopituitarism without pituitary hypoplasia. Science 257:1118-1121
84. Poulin G, Turgeon B, Drouin J (1997) NeuroD1/β2 contributes to cell-specific transcription of the POMC gene. Mol Cell Biol 17:6673-6682
85. Radovick S, Nations M, Du Y (1992) A mutation in the POU-homeodomain of Pit-1 responsible for combined pituitary hormone deficiency. Science 257:1115-1118
86. Redecker P, Cetin Y, Grube D (1995) Differential distribution of synaptotagmin I and rab3 in the anterior pituitary or four mammalian species. Neuroendocrinology 62:101-110
87. Rosa P, Hille A, Lee RW, Zanini A, De Camilli P, Huttner WB (1985) Secretogranin I and II: two tyrosine-sulfated secretory proteins common to a variety of cells secreting peptides by the regulated pathway. J Cell Biol 101:1999-2011
88. Sanno N, Jin L, Qian X, Osamura RY, Scheithauer BW, Kovacs K, Lloyd RV (1997a) Gonadotropin-releasing hormone and gonadotropin-releasing hormone receptor messenger ribonucleic acids expression in nontumorous and neoplastic pituitaries. J Clin Endocrinol Metab 82:1974-1982
89. Sanno N, Sugawara A, Teramoto A, Abe Y, Yen PM, Chin WW, Osamura RY (1997b) Immunohistochemical expression of retinoid X receptor isoforms in human pituitaries and pituitary adenomas. Neuroendocrinology 65:299-306
90. Sanno N, Teramoto A, Inada K, Osamura Y (1992) Immunohistochemical and clinicoendocrinological studies of gonadotropin producing pituitary adenomas. No To Shinkei 44:745-753 (in Japanese)
91. Sanno N, Teramoto A, Matsuno A, Itoh J, Takekoshi S, Osamura RY (1996a) In situ hybridization analysis of Pit-1 mRNA and hormonal production in human pituitary adenomas. Acta Neuropathol (Berl) 91:263-268
92. Sanno N, Teramoto A, Matsuno A, Osamura RY (1996b) Expression of human Pit-1 product in the human pituitary and pituitary adenomas. Immunohistochemical studies using an antibody against synthetic human Pit-1 product. Arch Pathol Lab Med 120:73-77
93. Sanno N, Teramoto A, Matsuno A, Takekoshi S, Itoh J, Osamura RY (1996c) Expression of Pit-1 and estrogen receptor messenger RNA in prolactin-producing pituitary adenomas. Mod Pathol 9:526-533
94. Sanno N, Teramoto A, Osamura RY, Genka S, Katakami H, Jin L, Lloyd RV, Kovacs K (1997c) A growth hormone-releasing hormone-producing pancreatic islet cell tumor metastasized to the pituitary is associated with pituitary somatotroph hyperplasia and acromegaly. J Clin Endocrinol Metab 82:2731-2737
95. Sanno N, Teramoto A, Sugiyama M, Itoh Y, Osamura RY (1996d) Application of catalyzed signal amplification in immunodetection of gonadotropin subunits in clinically nonfunctioning pituitary adenomas. Am J Clin Pathol 106:16-21
96. Scopsi L, Gullo M, Rilke F, Martn S, Steiner DF (1995) Proprotein convertases (PC1/PC3, and PC2) in normal and neoplastic human tissues: their use as markers of neuroendocrine differentiation. J Clin Endocrinol Metab 81:294-301
97. Seidah NG, Chretien M (1992) Proprotein and prohormone convertases of the subtilisin family: recent developments and future perspectives. Trends Endocrinol Metab 3:133-140
98. Sheng HZ, Zhadanov AB, Mosinger B Jr, Fujii T, Bertuzzi S, Grinberg A, Lee EJ, Huang SP, Mahon KA, Westphal H (1996) Specification of pituitary cell lineages by the LIM homeobox gene Lhx3. Science 272:1004-1007
99. Simmons DW, Voss JW, Ingraham HA, Holloway JM, Broide RS, Rosenfeld MG, Swanson LW (1990) Pituitary cell phenotypes involve cell-specific Pit-1 mRNA translation and synergistic interactions with other transcription factors. Genes Dev 4:695-711
100. Sornson MW, Wu W, Dasen JS, Flynn SE, Norman DJ, O'Connell SM, Gukovsky I, Carriere C, Ryan AK, Miller AP, Zuo L, Gleiberman AS, Andersen B, Beamer WG, Rosenfeld MG (1996) Pituitary lineage determination by the prophet of Pit-1 homeodomain factor defective in Ames dwarfism. Nature 384:327-333
101. Stefaneanu L, Ryan N, Kovacs K (1988) Immunocytochemical localization of synaptophysin in human hypophyses and pituitary adenomas. Arch Pathol Lab Med 112:801-804
102. Steiner DF, Cunningham D, Spiegelman L, Aten B (1967) Insulin biosynthesis: evidence for a precursor. Science 157:697-700
103. Steinfelder HJ, Hauser P, Nakayama Y, Radovick S, McClaskey JH, Taylor T, Weintraub BD, Wondisford FE (1991) Thyrotropin-releasing hormone regulation of human TSHB expression: role of a pituitary-specific transcription factor (Pit-1/GHF-1) and potential interaction with a thyroid hormone-inhibitory element. Proc Natl Acad Sci USA 88:3130-3134
104. Steinfelder HJ, Radovick S, Mroczynski MA, Hauser P, McClaskey JH, Weintraub BD, Wondisford FE (1992) Role of a pituitary specific transcription factor (Pit-1/GHF-1) or a closely related protein in cAMP regulation of human thyrotropin-β subunit gene expression. J Clin Invest 89:409-419
105. Stettler O, Nothias F, Tavitian B, Vernier P (1995) Double in situ hybridization reveals overlapping neuronal populations expressing the low molecular weight GTPases Rab3a and Rab3b in the rat brain. Eur J Neurosci 7:702-713
106. Sugawara A, Yen PM, Chin WW (1994) 9-cis-Retinoic acid regulation of rat growth hormone gene expression. Potential roles of multiple nuclear hormone receptors. Endocrinology 135:1956-1962
107. Tahara S, Sanno N, Teramoto A, Osamura RY (1999) Expression of Rab3, a Ras-related GTP-binding protein, in human nontumorous pituitaries and pituitary adenomas. Mod Pathol Jun 12:627-634
108. Takumi I, Steiner DF, Sanno N, Teramoto A, Osamura RY (1998) Localization of prohormone convertases 1/3 and 2 in the human pituitary gland and pituitary adenomas: analysis by immunohistochemistry, immunoelectron microscopy, and laser scanning microscopy. Mod Pathol 11:232-238
109. Tasaka K, Masumoto N, Mizuki J, Ikebuchi Y, Ohmichi M, Kurachi H, Miyake A, Murata Y (1998) Rab3B is essential for GnRH-induced gonadotrophin release from anterior pituitary cells. J Endocrinol 157:267-274
110. Thaper K, Kovacs K, Laws ER (1993) Pituitary adenomas: current concepts in classification. Histopathologist 3:39-57
111. Therrien M, Drouin J (1993) Cell-specific helix-loop-helix factor required for pituitary expression of the pro-opiomelanocortin gene. Mol Cell Biol 13:2342-2353
112. Thomas L, Betz H (1990) Synaptophysin binds to physophilin, a putative synaptic plasma membrane protein. J Cell Biol 111:2041-2052
113. Thomas PQ, Johnson BV, Rathjen J, Rathjen PD (1995) Sequence, genomic organization, and expression of the novel homeobox gene hesx1. J Biol Chem 270:3869-3875
114. Tremblay JJ, Lanctot C, Drouin J (1998) The pan-pituitary activator of transcription, Ptx1 (pituitary homeobox 1), acts in synergy with SF-1 and Pit-1 and is an upstream regulator of the Lim-homeodomain gene Lim3/Lhx3. Mol Endocrinol 12:428-441
115. Umemura S, Oda K, Utsunomiya H, Sanno N, Itoh J, Katakami H, Osamura RY (1995) Immunohistochemical characterization of "hyperplasia-adenoma sequence" in the pituitaries of transgenic mice expressing a human growth hormone-releasing factor gene. Tokai J Exp Clin Med 20:71-79
116. Windle JJ, Weiner RI, Mellon PL (1990) Cell lines of the pituitary gonadotrope lineage derived by targeted oncogenesis in transgenic mice. Mol Endocrinol 4:597-603
117. Yu VC, Delsert C, Andersen B, Holloway JM, Devary OV, Naar AM, Kim SY, Boutin J-M, Glass CK, Rosenfeld MG (1991) RXRβ: a coregulator that enhances binding of retinoic acid, thyroid hormone, and vitamin D receptors to their cognate response elements. Cell 67:1251-1266
118. Zahraoui A, Touchot N, Chardin P, Tavitian A (1989) The human rab genes encode a family of GTP-binding proteins related to yeast YPT1 and SFC4 products involved in secretion. J Biol Chem 264:12394-12401
119. Zhang X-K, Hoffmann B, Tran PB-V, Graupner G, Pfahl M (1992) Retinoid X receptor is an auxiliary protein for thyroid hormone and retinoic acid receptors. Nature 355:441-446