Negative regulation of human growth hormone gene expression by insulin is dependent on hypoxia-inducible factor binding in primary non-tumor pituitary cells

Journal of Biological Chemistry

Volumn 287, Issue 40, 2012, Pages 33282-33292

  Vakili, Hana ^a   Jin, Yan ^a   Cattini, Peter A ^a  

^a UNIVERSITY OF MANITOBA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMATIN REMODELING; DNA BINDING; DNA-PROTEIN INTERACTION; DOSE-DEPENDENT; DOWN-REGULATION; GROWTH HORMONES; HISTONE DEACETYLASES; HUMAN GROWTH HORMONE; HYPERACETYLATION; HYPOXIA-INDUCIBLE FACTOR 1; HYPOXIA-INDUCIBLE FACTORS; IN-SITU; INSULIN REGULATION; INSULIN TREATMENT; MULTIPLE LEVELS; PROMOTER REGION; RNA INTERFERENCE; TRANSGENIC MICE; TUMOR CELLS;

CELL CULTURE; CELLS; GENE EXPRESSION; MAMMALS; NUCLEOTIDES; RNA; TUMORS;

INSULIN;

ECHINOMYCIN; GROWTH HORMONE; HISTONE DEACETYLASE; HISTONE H3; HISTONE H4; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INSULIN; RNA; TRANSCRIPTION FACTOR; TRICHOSTATIN A;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING SITE; CELL HYPOXIA; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; DOWN REGULATION; ENZYME INHIBITION; GENE; GENE EXPRESSION REGULATION; GENE LOCUS; GROWTH HORMONE GENE; GROWTH HORMONE SECRETING CELL; HISTONE ACETYLATION; HORMONE ACTION; HYPOPHYSIS CELL; INSULIN RESPONSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN DNA BINDING; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

ANIMALS; ANOXIA; BASE SEQUENCE; CHROMATIN; FEMALE; GENE EXPRESSION REGULATION; HUMAN GROWTH HORMONE; HUMANS; HYPERINSULINISM; HYPOXIA-INDUCIBLE FACTOR 1; INSULIN; MALE; MICE; MICE, TRANSGENIC; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; PITUITARY GLAND; PROTEIN BINDING; RNA; SEQUENCE HOMOLOGY, NUCLEIC ACID;

MUS; MUS MUSCULUS;

EID: 84866924369     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.380949     Document Type: Article

References (78)

1. Luque, R. M., and Kineman, R. D. (2006) Impact of obesity on the growth hormone axis. Evidence for a direct inhibitory effect of hyperinsulinemia on pituitary function. Endocrinology 147, 2754-2763 (Pubitemid 43764612)
2. Buettner, R., Newgard, C. B., Rhodes, C. J., and O'Doherty, R. M. (2000) Correction of diet-induced hyperglycemia, hyperinsulinemia, and skeletal muscle insulin resistance by moderate hyperleptinemia. Am. J. Physiol. Endocrinol Metab. 278, E563-E569 (Pubitemid 30149402)
3. Brothers, K. J., Wu, S., DiVall, S. A., Messmer, M. R., Kahn, C. R., Miller, R. S., Radovick, S., Wondisford, F. E., and Wolfe, A. (2010) Rescue of obesity-induced infertility in female mice due to a pituitary-specific knockout of the insulin receptor. Cell Metab. 12, 295-305
4. Pataky, Z., Bobbioni-Harsch, E., and Golay, A. (2010) Obesity. A complex growing challenge. Exp. Clin. Endocrinol. Diabetes 118, 427-433
5. De Marinis, L., Bianchi, A., Mancini, A., Gentilella, R., Perrelli, M., Giampietro, A., Porcelli, T., Tilaro, L., Fusco, A., Valle, D., and Tacchino, R. M. (2004) Growth hormone secretion and leptin in morbid obesity before and after biliopancreatic diversion. Relationships with insulin and body composition. J. Clin. Endocrinol. Metab. 89, 174-180 (Pubitemid 38183878)
6. Lanzi, R., Luzi, L., Caumo, A., Andreotti, A. C., Manzoni, M. F., Malighetti, M. E., Sereni, L. P., and Pontiroli, A. E. (1999) Elevated insulin levels contribute to the reduced growth hormone (GH) response to GH-releasing hormone in obese subjects. Metabolism 48, 1152-1156 (Pubitemid 29418286)
7. Lanzi, R., Manzoni, M. F., Andreotti, A. C., Malighetti, M. E., Bianchi, E., Sereni, L. P., Caumo, A., Luzi, L., and Pontiroli, A. E. (1997) Evidence for an inhibitory effect of physiological levels of insulin on the growth hormone (GH) response to GH-releasing hormone in healthy subjects. J. Clin. Endocrinol. Metab. 82, 2239-2243 (Pubitemid 27287591)
8. Scacchi, M., Orsini, F., Cattaneo, A., Grasso, A., Filippini, B., Pecori Giraldi, F., Fatti, L. M., Moro, M., and Cavagnini, F. (2010) The diagnosis of GH deficiency in obese patients. A reappraisal with GHRH plus arginine testing after pharmacological blockade of lipolysis. Eur. J. Endocrinol. 163, 201-206
9. Pijl, H., Langendonk, J. G., Burggraaf, J., Frölich, M., Cohen, A. F., Veldhuis, J. D., and Meinders, A. E. (2001) Altered neuroregulation of GH secretion in viscerally obese premenopausal women. J. Clin. Endocrinol. Metab. 86, 5509-5515 (Pubitemid 33070282)
10. Procopio, M., Maccario, M., Grottoli, S., Oleandri, S. E., Boffano, G. M., Camanni, F., and Ghigo, E. (1995) Short-term fasting in obesity fails to restore the blunted GH responsiveness to GH-releasing hormone alone or combined with arginine. Clin Endocrinol. (Oxf.) 43, 665-669 (Pubitemid 26015010)
11. Maccario, M., Procopio, M., Grottoli, S., Oleandri, S. E., Razzore, P., Camanni, F., and Ghigo, E. (1995) In obesity the somatotrope response to either growth hormone-releasing hormone or arginine is inhibited by somatostatin or pirenzepine but not by glucose. J. Clin. Endocrinol. Metab. 80, 3774-3778
12. Luque, R. M., Gahete, M. D., Valentine, R. J., and Kineman, R. D. (2006) Examination of the direct effects of metabolic factors on somatotrope function in a non-human primate model, Papio anubis. J. Mol. Endocrinol. 37, 25-38 (Pubitemid 44288603)
13. Prager, D., and Melmed, S. (1988) Insulin regulates expression of the human growth hormone gene in transfected cells. J. Biol. Chem. 263, 16580-16585 (Pubitemid 18268835)
14. Prager, D., Gebremedhin, S., and Melmed, S. (1990) An insulin-induced DNA-binding protein for the human growth hormone gene. J. Clin. Invest. 85, 1680-1685 (Pubitemid 20176467)
15. Peritz, L. N., Fodor, E. J., Silversides, D. W., Cattini, P. A., Baxter, J. D., and Eberhardt, N. L. (1988) The human growth hormone gene contains both positive and negative control elements. J. Biol. Chem. 263, 5005-5007
16. Lefevre, C., Imagawa, M., Dana, S., Grindlay, J., Bodner, M., and Karin, M. (1987) Tissue-specific expression of the human growth hormone gene is conferred in part by the binding of a specific transacting factor. EMBOJ. 6, 971-981
17. Schödel, J., Oikonomopoulos, S., Ragoussis, J., Pugh, C. W., Ratcliffe, P. J., and Mole, D. R. (2011) High resolution genome-wide mapping of HIF-binding sites by ChIP-seq. Blood 117, e207-e217
18. 2-dependent degradation domain via the ubiquitin-proteasome pathway. Proc. Natl. Acad. Sci. U.S.A. 95, 7987-7992
19. Löfstedt, T., Jögi, A., Sigvardsson, M., Gradin, K., Poellinger, L., Påhlman, S., and Axelson, H. (2004) Induction of ID2 expression by hypoxia-inducible factor-1. A role in dedifferentiation of hypoxic neuroblastoma cells. J. Biol. Chem. 279, 39223-39231 (Pubitemid 39258183)
20. Weidemann, A., and Johnson, R. S. (2008) Biology of HIF-1α. Cell Death Differ. 15, 621-627
21. Adams, J. M., Difazio, L. T., Rolandelli, R. H., Luján, J. J., Haskó, G., Csóka, B., Selmeczy, Z., and Németh, Z. H. (2009) HIF-1. A key mediator in hypoxia. Acta Physiol. Hung. 96, 19-28
22. Ratan, R. R., Siddiq, A., Aminova, L., Lange, P. S., Langley, B., Ayoub, I., Gensert, J., and Chavez, J. (2004) Translation of ischemic preconditioning to the patient. Prolyl hydroxylase inhibition and hypoxia-inducible factor-1 as novel targets for stroke therapy. Stroke 35, 2687-2689 (Pubitemid 39458369)
23. Cheng, K., Ho, K., Stokes, R., Scott, C., Lau, S. M., Hawthorne, W. J., O'Connell, P. J., Loudovaris, T., Kay, T. W., Kulkarni, R. N., Okada, T., Wang, X. L., Yim, S. H., Shah, Y., Grey, S. T., Biankin, A. V., Kench, J. G., Laybutt, D. R., Gonzalez, F. J., Kahn, C. R., and Gunton, J. E. (2010) Hypoxia-inducible factor-1α regulates β cell function in mouse and human islets. J. Clin. Invest. 120, 2171-2183
24. Zhang, X., Lam, K. S., Ye, H., Chung, S. K., Zhou, M., Wang, Y., and Xu, A. (2010) Adipose tissue-specific inhibition of hypoxia-inducible factor 1α induces obesity and glucose intolerance by impeding energy expenditure in mice. J. Biol. Chem. 285, 32869-32877
25. Weng, Q., Zhang, J., Cao, J., Xia, Q., Wang, D., Hu, Y., Sheng, R., Wu, H., Zhu, D., Zhu, H., He, Q., and Yang, B. (2010) Q39, a quinoxaline 1,4-Di-N-oxide derivative, inhibits hypoxia-inducible factor-1α expression and the Akt/mTOR/4E-BP1 signaling pathway in human hepatoma cells. Investig. New Drugs 9, 1177-1187
26. Erman, A., Wabitsch, M., and Goodyer, C. G. (2011) Human growth hormone receptor (GHR) expression in obesity. II. Regulation of the human GHR gene by obesity-related factors. Int. J. Obes. (Lond.) 35, 1520-1529
27. Zelzer, E., Levy, Y., Kahana, C., Shilo, B. Z., Rubinstein, M., and Cohen, B. (1998) Insulin induces transcription of target genes through the hypoxia-inducible factor HIF-1α/ARNT. EMBO J. 17, 5085-5094 (Pubitemid 28408474)
28. Wang, L., Zhou, W., Gou, S., Wang, T., Liu, T., and Wang, C. (2010) Insulin promotes proliferative vitality and invasive capability of pancreatic cancer cells via hypoxia-inducible factor 1α pathway. J. Huazhong Univ. Sci. Technolog. Med. Sci. 30, 349-353
29. Kietzmann, T., Samoylenko, A., Roth, U., and Jungermann, K. (2003) Hypoxia-inducible factor-1 and hypoxia response elements mediate the induction of plasminogen activator inhibitor-1 gene expression by insulin in primary rat hepatocytes. Blood 101, 907-914 (Pubitemid 36139358)
30. Yoshida, D., Kim, K., Noha, M., and Teramoto, A. (2006) Anti-apoptotic action by hypoxia-inducible factor 1-α in human pituitary adenoma cell line, HP-75 in hypoxic condition. J. Neurooncol. 78, 217-225 (Pubitemid 44018814)
31. Deleted in proof
32. Jin, Y., Lu, S. Y., Fresnoza, A., Detillieux, K. A., Duckworth, M. L., and Cattini, P. A. (2009) Differential placental hormone gene expression during pregnancy in a transgenic mouse containing the human growth hormone/chorionic somatomammotropin locus. Placenta 30, 226-235
33. Jones, B. K., Monks, B. R., Liebhaber, S. A., and Cooke, N. E. (1995) The human growth hormone gene is regulated by a multicomponent locus control region. Mol. Cell. Biol. 15, 7010-7021
34. Vakili, H., Jin, Y., Nagy, J. I., and Cattini, P. A. (2011) Transgenic mice expressing the human growth hormone gene provide a model system to study human growth hormone synthesis and secretion in non-tumor-derived pituitary cells. Differential effects of dexamethasone and thyroid hormone. Mol. Cell. Endocrinol. 345, 48-57
35. Aza-Carmona, M., Shears, D. J., Yuste-Checa, P., Barca-Tierno, V., Hisado-Oliva, A., Belinchón, A., Benito-Sanz, S., Rodríguez, J. I., Argente, J., Campos-Barros, A., Scambler, P. J., and Heath, K. E. (2011) SHOX interacts with the chondrogenic transcription factors SOX5 and SOX6 to activate the aggrecan enhancer. Hum. Mol. Genet. 20, 1547-1559
36. Norquay, L. D., Yang, X., Jin, Y., Detillieux, K. A., and Cattini, P. A. (2006) Hepatocyte nuclear factor-3α binding at P sequences of the human growth hormone locus is associated with pituitary repressor function. Mol. Endocrinol. 20, 598-607 (Pubitemid 43291211)
37. Nam, S. Y., Ko, Y. S., Jung, J., Yoon, J., Kim, Y. H., Choi, Y. J., Park, J. W., Chang, M. S., Kim, W. H., and Lee, B. L. (2011) A hypoxia-dependent up-regulation of hypoxia-inducible factor-1 by nuclear factor-κB promotes gastric tumor growth and angiogenesis. Br J. Cancer 104, 166-174
38. Yang, X., Jin, Y., and Cattini, P. A. (2010) Appearance of the pituitary factor Pit-1 increases chromatin remodeling at hypersensitive site III in the human GH locus. J. Mol. Endocrinol. 45, 19-32
39. Yochum, G. S., McWeeney, S., Rajaraman, V., Cleland, R., Peters, S., and Goodman, R. H. (2007) Serial analysis of chromatin occupancy identifies β-catenin target genes in colorectal carcinoma cells. Proc. Natl. Acad. Sci. U.S.A. 104, 3324-3329 (Pubitemid 46364158)
40. Lytras, A., and Cattini, P.A. (1994) Human chorionic somatomammotropin gene enhancer activity is dependent on the blockade of a repressor mechanism. Mol. Endocrinol. 8, 478-489 (Pubitemid 24114738)
41. Sirito, M., Lin, Q., Maity, T., and Sawadogo, M. (1994) Ubiquitous expression of the 43- and 44-kDa forms of transcription factor USF in mammalian cells. Nucleic Acids Res. 22, 427-433 (Pubitemid 24160865)
42. Xi, L., Taher, M., Yin, C., Salloum, F., and Kukreja, R. C. (2004) Cobalt chloride induces delayed cardiac preconditioning in mice through selective activation of HIF-1α and AP-1 and iNOS signaling. Am. J. Physiol. Heart Circ. Physiol. 287, H2369-H2375 (Pubitemid 39557104)
43. Fukuda, R., Kelly, B., and Semenza, G. L. (2003) Vascular endothelial growth factor gene expression in colon cancer cells exposed to prostaglandin E2 is mediated by hypoxia-inducible factor 1. Cancer Res. 63, 2330-2334 (Pubitemid 36538645)
44. Vidal, S., Lloyd, R. V., Moya, L., Scheithauer, B. W., and Kovacs, K. (2002) Expression and distribution of vascular endothelial growth factor receptor Flk-1 in the rat pituitary. J. Histochem. Cytochem. 50, 533-540 (Pubitemid 34250592)
45. Lombardero, M., Vidal, S., Hurta, R., Román, A., Kovacs, K., Lloyd, R. V., and Scheithauer, B. W. (2006) Modulation of VEGF/Flk-1 receptor expression in the rat pituitary GH3 cell line by growth factors. Pituitary 9, 137-143 (Pubitemid 44463444)
46. Formica, J. V., and Waring, M. J. (1983) Effect of phosphate and amino acids on echinomycin biosynthesis by Streptomyces echinatus. Antimicrob. Agents Chemother. 24, 735-741 (Pubitemid 14203876)
47. Van Dyke, M. M., and Dervan, P. B. (1984) Echinomycin binding sites on DNA. Science 225, 1122-1127 (Pubitemid 14029093)
48. Kato, H., Tamamizu-Kato, S., and Shibasaki, F. (2004) Histone deacetylase 7 associates with hypoxia-inducible factor 1α and increases transcriptional activity. J. Biol. Chem. 279, 41966-41974 (Pubitemid 39313647)
49. Lee, K. J., Lee, K. Y., and Lee, Y. M. (2010) Down-regulation of a tumor suppressor RECK by hypoxia through recruitment of HDAC1 and HIF-1α to reverse HRE site in the promoter. Biochim. Biophys. Acta 1803, 608-616
50. Qian, D. Z., Kachhap, S. K., Collis, S. J., Verheul, H. M., Carducci, M. A., Atadja, P., and Pili, R. (2006) Class II histone deacetylases are associated with VHL-independent regulation of hypoxia-inducible factor 1α. Cancer Res. 66, 8814-8821 (Pubitemid 44449199)
51. Du, J., Chen, Y., Li, Q., Han, X., Cheng, C., Wang, Z., Danielpour, D., Dunwoodie, S. L., Bunting, K. D., and Yang, Y. C. (2012) HIF-1α deletion partially rescues defects of hematopoietic stem cell quiescence caused by Cited2 deficiency. Blood 119, 2789-2798
52. He, Q., Gao, Z., Yin, J., Zhang, J., Yun, Z., and Ye, J. (2011) Regulation of HIF-1α activity in adipose tissue by obesity-associated factors, adipogenesis, insulin, and hypoxia. Am. J. Physiol. Endocrinol. Metab. 300, E877-E885
53. Rajendran, R., Garva, R., Krstic-Demonacos, M., and Demonacos, C. (2011) Sirtuins. Molecular traffic lights in the crossroad of oxidative stress, chromatin remodeling, and transcription.J. Biomed. Biotechnol. 2011, 368276
54. Elefant, F., Cooke, N. E., and Liebhaber, S. A. (2000) Targeted recruitment of histone acetyltransferase activity to a locus control region. J. Biol. Chem. 275, 13827-13834 (Pubitemid 30257456)
55. Elefant, F., Su, Y., Liebhaber, S. A., and Cooke, N. E. (2000) Patterns of histone acetylation suggest dual pathways for gene activation by a bifunctional locus control region. EMBO J. 19, 6814-6822 (Pubitemid 32011674)
56. Ho, Y., Elefant, F., Cooke, N., and Liebhaber, S. (2002) A defined locus control region determinant links chromatin domain acetylation with long-range gene activation. Mol. Cell 9, 291-302 (Pubitemid 34195555)
57. Ho, Y., Tadevosyan, A., Liebhaber, S. A., and Cooke, N. E. (2008) The juxtaposition of a promoter with a locus control region transcriptional domain activates gene expression. EMBO Rep. 9, 891-898
58. Lee, Y. S., Sohn, D. H., Han, D., Lee, H. W., Seong, R. H., and Kim, J. B. (2007) Chromatin remodeling complex interacts with ADD1/SREBP1c to mediate insulin-dependent regulation of gene expression. Mol. Cell. Biol. 27, 438-452 (Pubitemid 46080115)
59. Rönsch, K., Jäger, M., Schöpflin, A., Danciu, M., Lassmann, S., and Hecht, A. (2011) Class I and III HDACs and loss of active chromatin features contribute to epigenetic silencing of CDX1 and EPHB tumor suppressor genes in colorectal cancer. Epigenetics 6, 610-622
60. Yang, S., Mulder, H., Holm, C., and Edén, S. (2004) Effects of growth hormone on the function of β-adrenoceptor subtypes in rat adipocytes. Obes. Res. 12, 330-339 (Pubitemid 41132557)
61. Cornford, A. S., Barkan, A. L., and Horowitz, J. F. (2011) Rapid suppression of growth hormone concentration by overeating. Potential mediation by hyperinsulinemia. J. Clin. Endocrinol. Metab. 96, 824-830
62. Luque, R. M., Lin, Q., Córdoba-Chacón, J., Subbaiah, P. V., Buch, T., Waisman, A., Vankelecom, H., and Kineman, R. D. (2011) Metabolic impact of adult-onset, isolated, growth hormone deficiency (AOiGHD) due to destruction of pituitary somatotropes. PLoS One 6, e15767
63. Yakar, S., Setser, J., Zhao, H., Stannard, B., Haluzik, M., Glatt, V., Bouxsein, M. L., Kopchick, J. J., and LeRoith, D. (2004) Inhibition of growth hormone action improves insulin sensitivity in liver IGF-1-deficient mice. J. Clin. Invest. 113, 96-105 (Pubitemid 38541636)
64. Krawczak, M., Chuzhanova, N. A., and Cooper, D. N. (1999) Evolution of the proximal promoter region of the mammalian growth hormone gene. Gene 237, 143-151 (Pubitemid 29406205)
65. Møller, N., Gjedsted, J., Gormsen, L., Fuglsang, J., and Djurhuus, C. (2003) Effects of growth hormone on lipid metabolism in humans. Growth Horm. IGF Res. 13, S18-S21 (Pubitemid 37161650)
66. Takahashi, S., and Satozawa, N. (2002) The 20-kDa human growth hormone reduces body fat by increasing lipolysis and decreasing lipoprotein lipase activity. Horm. Res. 58, 157-164
67. Christoforidis, A., Maniadaki, I., and Stanhope, R. (2005) Growth hormone/insulin-like growth factor-1 axis during puberty. Pediatr. Endocrinol. Rev. 3, 5-10 (Pubitemid 43211471)
68. Scacchi, M., Pincelli, A. I., and Cavagnini, F. (1999) Growth hormone in obesity. Int. J. Obes. Relat. Metab. Disord. 23, 260-271 (Pubitemid 29118856)
69. Zhang, H., Zhang, G., Gonzalez, F. J., Park, S. M., and Cai, D. (2011) Hypoxia-inducible factor directs POMC gene to mediate hypothalamic glucose sensing and energy balance regulation. PLoS Biol. 9, e1001112
70. Jiang, C., Qu, A., Matsubara, T., Chanturiya, T., Jou, W., Gavrilova, O., Shah, Y. M., and Gonzalez, F. J. (2011) Disruption of hypoxia-inducible factor 1 in adipocytes improves insulin sensitivity and decreases adiposity in high fat diet-fed mice. Diabetes 60, 2484-2495
71. Krishnan, J., Danzer, C., Simka, T., Ukropec, J., Walter, K. M., Kumpf, S., Mirtschink, P., Ukropcova, B., Gasperikova, D., Pedrazzini, T., and Krek, W. (2012) Dietary obesity-associated Hif1α activation in adipocytes restricts fatty acid oxidation and energy expenditure via suppression of the Sirt2-NAD+ system. Genes Dev. 26, 259-270
72. Treins, C., Giorgetti-Peraldi, S., Murdaca, J., Semenza, G. L., and Van Obberghen, E. (2002) Insulin stimulates hypoxia-inducible factor 1 through a phosphatidylinositol 3-kinase/target of rapamycin-dependent signaling pathway. J. Biol. Chem. 277, 27975-27981 (Pubitemid 34966746)
73. Strasburger, C. J. (1990) Antigenic epitope mapping of the human growth hormone molecule. A strategy to standardize growth hormone immunoassays. Acta Paediatr. Scand. Suppl. 370, 82-86
74. Yi, S., Bernat, B., Pál, G., Kossiakoff, A., and Li, W. H. (2002) Functional promiscuity of squirrel monkey growth hormone receptor toward both primate and nonprimate growth hormones. Mol. Biol. Evol. 19, 1083-1092 (Pubitemid 34743232)
75. Nickel, B. E., Kardami, E., and Cattini, P. A. (1990) The human placental growth hormone variant is mitogenic for rat lymphoma Nb2 cells. Endocrinology 126, 971-976 (Pubitemid 20079510)
76. Wells, J. A., Cunningham, B. C., Fuh, G., Lowman, H. B., Bass, S. H., Mulkerrin, M. G., Ultsch, M., and deVos, A. M. (1993) The molecular basis for growth hormone-receptor interactions. Recent Prog. Horm. Res. 48, 253-275
77. Wells, J. A., and de Vos, A. M. (1993) Structure and function of human growth hormone. Implications for the hematopoietins. Annu. Rev. Biophys. Biomol. Struct. 22, 329-351 (Pubitemid 23180327)
78. Lira, S. A., Kalla, K. A., Glass, C. K., Drolet, D. W., and Rosenfeld, M. G. (1993) Synergistic interactions between Pit-1 and other elements are required for effective somatotroph rat growth hormone gene expression in transgenic mice. Mol. Endocrinol. 7, 694-701 (Pubitemid 23157748)