Osteoblast-restricted Disruption of the Growth Hormone Receptor in Mice Results in Sexually Dimorphic Skeletal Phenotypes

Bone Research

Volumn 1, Issue , 2013, Pages 85-97

  Singhal, Vandana ^a   Goh, Brian C ^a   Bouxsein, Mary L ^b   Faugere, Marie Claude ^c   Digirolamo, Douglas J ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF KENTUCKY MEDICAL CENTER   (United States)

Author keywords

bone; Growth hormone; knockout mice; osteoblasts; sexual dimorphism

Indexed keywords

EID: 84879227062     PISSN: 20954700     EISSN: 20956231     Source Type: Journal    
DOI: 10.4248/BR201301006     Document Type: Article

References (52)

1. Karsenty G. Bone formation and factors affecting this process. Matrix Biol. 2000 ;19:85-89.
2. Mundy GR, Boyce B, Hughes D, Wright K, Bonewald L, Dallas S, Harris S, Ghosh-Choudhury N, Chen D, Dunstan C. The effects of cytokines and growth factors on osteoblastic cells. Bone. 1995;17:71S-75S.
3. Miller WL, Eberhardt NL. Structure and evolution of the growth hormone gene family. Endocr Rev. 1983;4:97-130.
4. Yang N, Langenheim JF, Wang X, Jiang J, Chen WY, Frank SJ. Activation of growth hormone receptors by growth hormone and growth hormone antagonist dimers: Insights into receptor triggering. Mol Endocrinol. 2008;22:978-988.
5. Argetsinger LS, Campbell GS, Yang X, Witthuhn BA, Silvennoinen O, Ihle JN, Carter-Su C. Identification of JAK2 as a growth hormone receptor-associated tyrosine kinase. Cell. 1993;74:237-244.
6. Foster CM, Shafer JA, Rozsa FW, Wang XY, Lewis SD, Renken DA, Natale JE, Schwartz J, Carter-Su C. Growth hormone promoted tyrosyl phosphorylation of growth hormone receptors in murine 3T3-F442A fibroblasts and adipocytes. Biochemistry. 1988;27:326-334.
7. Silva CM, Day RN, Weber MJ, Thorner MO. Human growth hormone (GH) receptor is characterized as the 134-kilodalton tyrosine-phosphorylated protein activated by GH treatment in IM-9 cells. Endocrinology. 1993;133:2307-2312.
8. Bergad PL, Shih HM, Towle HC, Schwarzenberg SJ, Berry SA. Growth hormone induction of hepatic serine protease inhibitor 2.1 transcription is mediated by a Stat5-related factor binding synergistically to two gamma-activated sites. J Biol Chem. 1995; 270:24903-24910.
9. Campbell GS, Meyer DJ, Raz R, Levy DE, Schwartz J, Carter-Su C. Activation of acute phase response factor (APRF)/Stat3 trans-cription factor by growth hormone. J Biol Chem. 1995;270: 3974-3979.
10. Choi HK, Waxman DJ. Pulsatility of growth hormone (GH) signalling in liver cells: Role of the JAK-STAT5b pathway in GH action. Growth Horm IGF Res. 2000;10 Suppl B:S1-S8.
11. Delesque-Touchard N, Park SH, Waxman DJ. Synergistic action of hepatocyte nuclear factors 3 and 6 on CYP2C12 gene expression and suppression by growth hormone-activated STAT5b. Proposed model for female specific expression of CYP2C12 in adult rat liver. J Biol Chem. 2000;275:34173-34182.
12. Lahuna O, Rastegar M, Maiter D, Thissen JP, Lemaigre FP, Rousseau GG. Involvement of STAT5 (signal transducer and activator of transcription 5) and HNF-4 (hepatocyte nuclear factor 4) in the transcriptional control of the hnf6 gene by growth hormone. Mol Endocrinol. 2000;14:285-294.
13. Meyer DJ, Campbell GS, Cochran BH, Argetsinger LS, Larner AC, Finbloom DS, Carter-Su C, Schwartz J. Growth hormone induces a DNA binding factor related to the interferon-stimulated 91-kDa transcription factor. J Biol Chem. 1994;269:4701-4704.
14. Sotiropoulos A, Moutoussamy S, Binart N, Kelly PA, Finidori J. The membrane proximal region of the cytoplasmic domain of the growth hormone receptor is involved in the activation of Stat 3. FEBS Lett. 1995;369:169-172.
15. Waxman DJ. Growth hormone pulse-activated STAT5 signalling: A unique regulatory mechanism governing sexual dimorphism of liver gene expression. Novartis Found Symp. 2000;227:61-74.
16. Waxman DJ, Ram PA, Park SH, Choi HK. Intermittent plasma growth hormone triggers tyrosine phosphorylation and nuclear translocation of a liver-expressed, Stat 5-related DNA binding protein. Proposed role as an intracellular regulator of male-specific liver gene transcription. J Biol Chem. 1995;270:13262-13270.
17. Costoya JA, Finidori J, Moutoussamy S, Searis R, Devesa J, Arce VM. Activation of growth hormone receptor delivers an antiapoptotic signal: Evidence for a role of Akt in this pathway. Endocrinology. 1999;140:5937-5943.
18. Liang L, Jiang J, Frank SJ. Insulin receptor substrate-1-mediated enhancement of growth hormone-induced mitogen-activated protein kinase activation. Endocrinology. 2000;141:3328-3336.
19. Campbell GS, Pang L, Miyasaka T, Saltiel AR, Carter-Su C. Stimulation by growth hormone of MAP kinase activity in 3T3-F442A fibroblasts. J Biol Chem. 1992;267:6074-6080.
20. Moller C, Hansson A, Enberg B, Lobie PE, Norstedt G. Growth hormone (GH) induction of tyrosine phosphorylation and activa-tion of mitogen-activated protein kinases in cells transfected with rat GH receptor cDNA. J Biol Chem. 1992;267:23403-23408.
21. Winston LA, Bertics PJ. Growth hormone stimulates the tyrosine phosphorylation of 42-A nd 45-kDa ERK-related proteins. J Biol Chem. 1992;267:4747-4751.
22. Frank SJ, Yi W, Zhao Y, Goldsmith JF, Gilliland G, Jiang J, Sakai I, Kraft AS. Regions of the JAK2 tyrosine kinase required for coupling to the growth hormone receptor. J Biol Chem. 1995;270: 14776-14785.
23. Sotiropoulos A, Perrot-Applanat M, Dinerstein H, Pallier A, Postel-Vinay MC, Finidori J, Kelly PA. Distinct cytoplasmic regions of the growth hormone receptor are required for activa-tion of JAK2, mitogen-activated protein kinase, and transcription. Endocrinology. 1994;135:1292-1298.
24. VanderKuur JA, Wang X, Zhang L, Campbell GS, Allevato G, Billestrup N, Norstedt G, Carter-Su C. Domains of the growth hormone receptor required for association and activation of JAK2 tyrosine kinase. J Biol Chem. 1994;269:21709-21717.
25. Dietrich P, Dragatsis I, Xuan S, Zeitlin S, Efstratiadis A. Conditional mutagenesis in mice with heat shock promoter-driven cre transgenes. Mamm Genome. 2000;11:196-205.
26. LeRoith D. Insulin-like growth factor I receptor signaling-overlapping or redundant pathways? Endocrinology. 2000;141: 1287-1288.
27. Hill PA, Tumber A, Meikle MC. Multiple extracellular signals promote osteoblast survival and apoptosis. Endocrinology. 1997;138:3849-3858.
28. Merriman HL, La Tour D, Linkhart TA, Mohan S, Baylink DJ, Strong DD. Insulin-like growth factor-I and insulin-like growth factor-II induce c-fos in mouse osteoblastic cells. Calcif Tissue Int. 1990;46:258-262.
29. Rydziel S, Delany AM, Canalis E. Insulin-like growth factor I inhibits the transcription of collagenase 3 in osteoblast cultures. J Cell Biochem. 1997;67:176-183.
30. Zhao G, Monier-Faugere MC, Langub MC, Geng Z, Nakayama T, Pike JW, Chernausek SD, Rosen CJ, Donahue LR, Malluche HH, Fagin JA, Clemens TL. Targeted overexpression of insulin-like growth factor I to osteoblasts of transgenic mice: Increased trabecular bone volume without increased osteoblast prolifer-A tion. Endocrinology. 2000;141:2674-2682.
31. Zhang M, Xuan S, Bouxsein ML, von Stechow D, Akeno N, Faugere MC, Malluche H, Zhao G, Rosen CJ, Efstratiadis A, Clemens TL. Osteoblast-specific knockout of the insulin-like growth factor (IGF) receptor gene reveals an essential role of IGF signaling in bone matrix mineralization. J Biol Chem. 2002; 277:44005-44012.
32. Barnard R, Ng KW, Martin TJ, Waters MJ. Growth hormone (GH) receptors in clonal osteoblast-like cells mediate a mitogenic response to GH. Endocrinology. 1991;128:1459-1464.
33. Nilsson A, Swolin D, Enerback S, Ohlsson C. Expression of functional growth hormone receptors in cultured human osteoblast-like cells. J Clin Endocrinol Metab. 1995;80:3483-3488.
34. Scheven BA, Hamilton NJ, Fakkeldij TM, Duursma SA. Effects of recombinant human insulin-like growth factor I and II (IGF-I/-II) and growth hormone (GH) on the growth of normal adult human osteoblast-like cells and human osteogenic sarcoma cells. Growth Regul. 1991;1:160-167.
35. Slootweg MC, Salles JP, Ohlsson C, de Vries CP, Engelbregt MJ, Netelenbos JC. Growth hormone binds to a single high affinity receptor site on mouse osteoblasts: Modulation by retinoic acid and cell differentiation. J Endocrinol. 1996;150:465-472.
36. Slootweg MC, van Buul-Offers SC, Herrmann-Erlee MP, van der Meer JM, Duursma SA. Growth hormone is mitogenic for fetal mouse osteoblasts but not for undifferentiated bone cells. J Endocrinol. 1988;116:11-13.
37. Mohan S, Richman C, Guo R, Amaar Y, Donahue LR, Wergedal J, Baylink DJ. Insulin-like growth factor regulates peak bone mineral density in mice by both growth hormone-dependent and-independent mechanisms. Endocrinology. 2003;144:929-936.
38. Bikle D, Majumdar S, Laib A, Powell-Braxton L, Rosen C, Beamer W, Nauman E, Leary C, Halloran B. The skeletal structure of insulin-like growth factor I-deficient mice. J Bone Miner Res. 2001;16:2320-2329.
39. Fan Y, Menon RK, Cohen P, Hwang D, Clemens T, DiGirolamo DJ, Kopchick JJ, Le Roith D, Trucco M, Sperling MA. Liver-specific deletion of the growth hormone receptor reveals essential role of growth hormone signaling in hepatic lipid metabolism. J Biol Chem. 2009;284:19937-19944.
40. DiGirolamo DJ, Mukherjee A, Fulzele K, Gan Y, Cao X, Frank SJ, Clemens TL. Mode of growth hormone action in osteoblasts. J Biol Chem. 2007;282:31666-31674.
41. Edmondson SR, Russo VC, McFarlane AC, Wraight CJ, Werther GA. Interactions between growth hormone, insulin-like growth factor I, and basic fibroblast growth factor in melanocyte growth. J Clin Endocrinol Metab. 1999;84:1638-1644.
42. Langdahl BL, Kassem M, Moller MK, Eriksen EF. The effects of IGF-I and IGF-II on proliferation and differentiation of human osteoblasts and interactions with growth hormone. Eur J Clin Invest. 1998;28:176-183.
43. Huang Y, Kim S-O, Yang N, Jiang J, Frank SJ. Physical and functional interaction of growth hormone and insulin-like growth factor-I signaling elements. Mol Endocrinol. 2004;18:1471-1485.
44. Le Roith D, Bondy C, Yakar S, Liu JL, Butler A. The somatomedin hypothesis: 2001. Endocr Rev. 2001;22:53-74.
45. Rutter MM, Markoff E, Clayton L, Akeno N, Zhao G, Clemens TL, Chernausek SD. Osteoblast-specific expression of insulin-like growth factor-1 in bone of transgenic mice induces insulin-like growth factor binding protein-5. Bone. 2005;36:224-231.
46. Bautista CM, Baylink DJ, Mohan S. Isolation of a novel insulin-like growth factor (IGF) binding protein from human bone: A potential candidate for fixing IGF-II in human bone. Biochem Biophys Res Commun. 1991;176:756-763.
47. Jones JI, Gockerman A, Busby WH, Jr., Camacho-Hubner C, Clemmons DR. Extracellular matrix contains insulin-like growth factor binding protein-5: Potentiation of the effects of IGF-I. J Cell Biol. 1993;121:679-687.
48. Waxman DJ, O'Connor C. Growth hormone regulation of sex-dependent liver gene expression. Mol Endocrinol. 2006;20: 2613-2629.
49. Ogita M, Rached MT, Dworakowski E, Bilezikian JP, Kousteni S. Differentiation and proliferation of periosteal osteoblast pro-genitors are differentially regulated by estrogens and intermittent parathyroid hormone administration. Endocrinology. 2008;149: 5713-5723.
50. Olson LE, Ohlsson C, Mohan S. The role of GH/IGF-I-mediated mechanisms in sex differences in cortical bone size in mice. Calcif Tissue Int. 20118;8:1-8.
51. Gennari L, Nuti R, Bilezikian JP. Aromatase activity and bone homeostasis in men. J Clin Endocrinol Metab. 2004;89:5898-907.
52. Liongue C, Ward AC. Evolution of Class I cytokine receptors. BMC Evol Biol. 2007;7:120.