Loss of transcription factor early growth response gene 1 results in impaired endochondral bone repair

Bone

Volumn 49, Issue 4, 2011, Pages 743-752

  Reumann, Marie K ^a   Strachna, Olga ^a   Yagerman, Sarah ^a   Torrecilla, Daniel ^a   Kim, Jihye ^a   Doty, Stephen B ^b   Lukashova, Lyudmila ^c   Boskey, Adele L ^c   Mayer Kuckuk, Philipp ^a  

^a Bone Cell Biology and Imaging Laboratory   (United States)

^b Analytical Microscopy Laboratory   (United States)

^c HOSPITAL FOR SPECIAL SURGERY   (United States)

Author keywords

Bone healing; Early growth response gene; Endochondral bone formation; Fracture repair; Transcription factor

Indexed keywords

FIBRIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; BONE MINERALIZATION; BONE REMODELING; BONE STRUCTURE; CALLUS; CONTROLLED STUDY; DEVELOPMENTAL GENE; DISEASE DURATION; EARLY GROWTH RESPONSE GENE 1; ENCHONDRAL OSSIFICATION; FRACTURE HEALING; GENE FUNCTION; GENE LOSS; MOUSE; NONHUMAN; RIB FRACTURE; SKELETAL MUSCLE; VASCULARIZATION; WILD TYPE;

ANIMALS; BIOLOGICAL MARKERS; BONE AND BONES; BONE RESORPTION; BONY CALLUS; EARLY GROWTH RESPONSE PROTEIN 1; FIBRIN; FRACTURE HEALING; FRACTURES, BONE; MICE; MUSCLE, SKELETAL; OSTEOGENESIS; OSTEOTOMY; RIBS;

EID: 80052284891     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2011.06.023     Document Type: Article

References (67)

1. Milbrandt J. A nerve growth factor-induced gene encodes a possible transcriptional regulatory factor. Science 1987, 238:797-799.
2. Lau L.F., Nathans D. Expression of a set of growth-related immediate early genes in BALB/c 3T3 cells: coordinate regulation with c-fos or c-myc. Proc Natl Acad Sci U S A 1987, 84:1182-1186.
3. Lemaire P., Revelant O., Bravo R., Charnay P. Two mouse genes encoding potential transcription factors with identical DNA-binding domains are activated by growth factors in cultured cells. Proc Natl Acad Sci U S A 1988, 85:4691-4695.
4. Lim R.W., Varnum B.C., Herschman H.R. Cloning of tetradecanoyl phorbol ester-induced 'primary response' sequences and their expression in density-arrested Swiss 3T3 cells and a TPA non-proliferative variant. Oncogene 1987, 1:263-270.
5. Sukhatme V.P., Cao X.M., Chang L.C., Tsai-Morris C.H., Stamenkovich D., Ferreira P.C., et al. A zinc finger-encoding gene coregulated with c-fos during growth and differentiation, and after cellular depolarization. Cell 1988, 53:37-43.
6. Khachigian L.M. Early growth response-1 in cardiovascular pathobiology. Circ Res 2006, 98:186-191.
7. Thiel G., Cibelli G. Regulation of life and death by the zinc finger transcription factor EGR-1. J Cell Physiol 2002, 193:287-292.
8. Khachigian L.M., Collins T. Early growth response factor 1: a pleiotropic mediator of inducible gene expression. J Mol Med 1998, 76:613-616.
9. Khachigian L.M. Early growth response-1: blocking angiogenesis by shooting the messenger. Cell Cycle 2004, 3:10-11.
10. Lo L.W., Cheng J.J., Chiu J.J., Wung B.S., Liu Y.C., Wang D.L. Endothelial exposure to hypoxia induces EGR-1 expression involving PKCalpha-mediated Ras/Raf-1/ERK1/2 pathway. J Cell Physiol 2001, 188:304-312.
11. Yan S.F., Fujita T., Lu J., Okada K., Shan Zou Y., Mackman N., et al. EGR-1, a master switch coordinating upregulation of divergent gene families underlying ischemic stress. Nat Med 2000, 6:1355-1361.
12. Ham J., Eilers A., Whitfield J., Neame S.J., Shah B. c-Jun and the transcriptional control of neuronal apoptosis. Biochem Pharmacol 2000, 60:1015-1021.
13. Scharnhorst V., Menke A.L., Attema J., Haneveld J.K., Riteco N., van Steenbrugge G.J., et al. EGR-1 enhances tumor growth and modulates the effect of the Wilms' tumor 1 gene products on tumorigenicity. Oncogene 2000, 19:791-800.
14. Huang R.P., Liu C., Fan Y., Mercola D., Adamson E.D. EGR-1 negatively regulates human tumor cell growth via the DNA-binding domain. Cancer Res 1995, 55:5054-5062.
15. Perez-Castillo A., Pipaon C., Garcia I., Alemany S. NGFI-A gene expression is necessary for T lymphocyte proliferation. J Biol Chem 1993, 268:19445-19450.
16. Biesiada E., Razandi M., Levin E.R. EGR-1 activates basic fibroblast growth factor transcription. Mechanistic implications for astrocyte proliferation. J Biol Chem 1996, 271:18576-18581.
17. Hofer G., Grimmer C., Sukhatme V.P., Sterzel R.B., Rupprecht H.D. Transcription factor EGR-1 regulates glomerular mesangial cell proliferation. J Biol Chem 1996, 271:28306-28310.
18. Kaufmann K., Thiel G. Epidermal growth factor and platelet-derived growth factor induce expression of EGR-1, a zinc finger transcription factor, in human malignant glioma cells. J Neurol Sci 2001, 189:83-91.
19. Kaufmann K., Thiel G. Epidermal growth factor and thrombin induced proliferation of immortalized human keratinocytes is coupled to the synthesis of EGR-1, a zinc finger transcriptional regulator. J Cell Biochem 2002, 85:381-391.
20. Lee S.L., Tourtellotte L.C., Wesselschmidt R.L., Milbrandt J. Growth and differentiation proceeds normally in cells deficient in the immediate early gene NGFI-A. J Biol Chem 1995, 270:9971-9977.
21. Cibelli G., Policastro V., Rossler O.G., Thiel G. Nitric oxide-induced programmed cell death in human neuroblastoma cells is accompanied by the synthesis of EGR-1, a zinc finger transcription factor. J Neurosci Res 2002, 67:450-460.
22. Messmer U.K., Brune B. Nitric oxide-induced apoptosis: p53-dependent and p53-independent signalling pathways. Biochem J 1996, 319(Pt 1):299-305.
23. Behrens A., Sibilia M., Wagner E.F. Amino-terminal phosphorylation of c-Jun regulates stress-induced apoptosis and cellular proliferation. Nat Genet 1999, 21:326-329.
24. Le-Niculescu H., Bonfoco E., Kasuya Y., Claret F.X., Green D.R., Karin M. Withdrawal of survival factors results in activation of the JNK pathway in neuronal cells leading to Fas ligand induction and cell death. Mol Cell Biol 1999, 19:751-763.
25. Gururajan M., Simmons A., Dasu T., Spear B.T., Calulot C., Robertson D.A., et al. Early growth response genes regulate B cell development, proliferation, and immune response. J Immunol 2008, 181:4590-4602.
26. Lee S.L., Sadovsky Y., Swirnoff A.H., Polish J.A., Goda P., Gavrilina G., et al. Luteinizing hormone deficiency and female infertility in mice lacking the transcription factor NGFI-A (EGR-1). Science 1996, 273:1219-1221.
27. Khachigian L.M., Lindner V., Williams A.J., Collins T. EGR-1-induced endothelial gene expression: a common theme in vascular injury. Science 1996, 271:1427-1431.
28. Hashimoto J., Yoshikawa H., Takaoka K., Shimizu N., Masuhara K., Tsuda T., et al. Inhibitory effects of tumor necrosis factor alpha on fracture healing in rats. Bone 1989, 10:453-457.
29. Wittrant Y., Gorin Y., Mohan S., Wagner B., Abboud-Werner S.L. Colony-stimulating factor-1 (CSF-1) directly inhibits receptor activator of nuclear factor-{kappa}B ligand (RANKL) expression by osteoblasts. Endocrinology 2009, 150:4977-4988.
30. Handschel J., Berr K., Depprich R.A., Kubler N.R., Naujoks C., Wiesmann H.P., et al. Induction of osteogenic markers in differentially treated cultures of embryonic stem cells. Head Face Med 2008, 4:10.
31. Kanamoto T., Mizuhashi K., Terada K., Minami T., Yoshikawa H., Furukawa T. Isolation and characterization of a novel plasma membrane protein, osteoblast induction factor (obif), associated with osteoblast differentiation. BMC Dev Biol 2009, 9:70.
32. Yu M., Moreno J.L., Stains J.P., Keegan A.D. Complex regulation of tartrate-resistant acid phosphatase (TRAP) expression by interleukin 4 (IL-4): IL-4 indirectly suppresses receptor activator of NF-kappaB ligand (RANKL)-mediated TRAP expression but modestly induces its expression directly. J Biol Chem 2009, 284:32968-32979.
33. Combs M.D., Yutzey K.E. VEGF and RANKL regulation of NFATc1 in heart valve development. Circ Res 2009, 105:565-574.
34. Kurata K., Maruyama S., Kato S., Sato W., Yamamoto J., Ozaki T., et al. Tissue-type plasminogen activator deficiency attenuates peritoneal fibrosis in mice. Am J Physiol Renal Physiol 2009, 297:F1510-F1517.
35. Ito T., Tokunaga K., Maruyama H., Kawashima H., Kitahara H., Horikoshi T., et al. Coxsackievirus and adenovirus receptor (CAR)-positive immature osteoblasts as targets of adenovirus-mediated gene transfer for fracture healing. Gene Ther 2003, 10:1623-1628.
36. Li M., Amizuka N., Oda K., Tokunaga K., Ito T., Takeuchi K., et al. Histochemical evidence of the initial chondrogenesis and osteogenesis in the periosteum of a rib fractured model: implications of osteocyte involvement in periosteal chondrogenesis. Microsc Res Tech 2004, 64:330-342.
37. Nakase T., Nomura S., Yoshikawa H., Hashimoto J., Hirota S., Kitamura Y., et al. Transient and localized expression of bone morphogenetic protein 4 messenger RNA during fracture healing. J Bone Miner Res 1994, 9:651-659.
38. Yamagiwa H., Tokunaga K., Hayami T., Hatano H., Uchida M., Endo N., et al. Expression of metalloproteinase-13 (Collagenase-3) is induced during fracture healing in mice. Bone 1999, 25:197-203.
39. Tan L., Peng H., Osaki M., Choy B.K., Auron P.E., Sandell L.J., et al. EGR-1 mediates transcriptional repression of COL2A1 promoter activity by interleukin-1beta. J Biol Chem 2003, 278:17688-17700.
40. Min I.M., Pietramaggiori G., Kim F.S., Passegue E., Stevenson K.E., Wagers A.J. The transcription factor EGR1 controls both the proliferation and localization of hematopoietic stem cells. Cell Stem Cell 2008, 2:380-391.
41. Nunamaker D.M. Experimental models of fracture repair. Clin Orthop Relat Res 1998, S56-S65.
42. Reumann M.K., Nair T., Strachna O., Boskey A.L., Mayer-Kuckuk P. Production of VEGF receptor 1 and 2 mRNA and protein during endochondral bone repair is differential and healing phase specific. J Appl Physiol 2010, 109:1930-1938.
43. Einhorn T.A. The cell and molecular biology of fracture healing. Clin Orthop Relat Res 1998, S7-S21.
44. Mackman N. Regulation of the tissue factor gene. Thromb Haemost 1997, 78:747-754.
45. Yan S.F., Zou Y.S., Gao Y., Zhai C., Mackman N., Lee S.L., et al. Tissue factor transcription driven by EGR-1 is a critical mechanism of murine pulmonary fibrin deposition in hypoxia. Proc Natl Acad Sci U S A 1998, 95:8298-8303.
46. Liao H., Hyman M.C., Lawrence D.A., Pinsky D.J. Molecular regulation of the PAI-1 gene by hypoxia: contributions of EGR-1, HIF-1alpha, and C/EBPalpha. FASEB J 2007, 21:935-949.
47. Lucerna M., Mechtcheriakova D., Kadl A., Schabbauer G., Schafer R., Gruber F., et al. NAB2, a corepressor of EGR-1, inhibits vascular endothelial growth factor-mediated gene induction and angiogenic responses of endothelial cells. J Biol Chem 2003, 278:11433-11440.
48. Cui M.Z., Parry G.C., Oeth P., Larson H., Smith M., Huang R.P., et al. Transcriptional regulation of the tissue factor gene in human epithelial cells is mediated by Sp1 and EGR-1. J Biol Chem 1996, 271:2731-2739.
49. Gille J., Swerlick R.A., Caughman S.W. Transforming growth factor-alpha-induced transcriptional activation of the vascular permeability factor (VPF/VEGF) gene requires AP-2-dependent DNA binding and transactivation. EMBO J 1997, 16:750-759.
50. Shimoyamada H., Yazawa T., Sato H., Okudela K., Ishii J., Sakaeda M., Kashiwagi K., Suzuki T., Mitsui H., Woo T., Tajiri M., Ohmori T., Ogura T., Masuda M., Oshiro H., Kitamura H. Early growth response-1 induces and enhances vascular endothelial growth factor-a expression in lung cancer cells. Am J Pathol 2010, 177:70-83.
51. Houston P., Campbell C.J., Svaren J., Milbrandt J., Braddock M. The transcriptional corepressor NAB2 blocks EGR-1-mediated growth factor activation and angiogenesis. Biochem Biophys Res Commun 2001, 283:480-486.
52. Khachigian L.M., Williams A.J., Collins T. Interplay of Sp1 and EGR-1 in the proximal platelet-derived growth factor A-chain promoter in cultured vascular endothelial cells. J Biol Chem 1995, 270:27679-27686.
53. Shingu T., Bornstein P. Overlapping EGR-1 and Sp1 sites function in the regulation of transcription of the mouse thrombospondin 1 gene. J Biol Chem 1994, 269:32551-32557.
54. Bouchard F., Belanger S.D., Biron-Pain K., St-Pierre Y. EGR-1 activation by EGF inhibits MMP-9 expression and lymphoma growth. Blood 2010, 116:759-766.
55. Shin S.Y., Kim J.H., Baker A., Lim Y., Lee Y.H. Transcription factor EGR-1 is essential for maximal matrix metalloproteinase-9 transcription by tumor necrosis factor alpha. Mol Cancer Res 2010, 8:507-519.
56. Colnot C., Thompson Z., Miclau T., Werb Z., Helms J.A. Altered fracture repair in the absence of MMP9. Development 2003, 130:4123-4133.
57. Cenci S., Weitzmann M.N., Gentile M.A., Aisa M.C., Pacifici R. M-CSF neutralization and EGR-1 deficiency prevent ovariectomy-induced bone loss. J Clin Invest 2000, 105:1279-1287.
58. Kimble R.B., Srivastava S., Ross F.P., Matayoshi A., Pacifici R. Estrogen deficiency increases the ability of stromal cells to support murine osteoclastogenesis via an interleukin-1and tumor necrosis factor-mediated stimulation of macrophage colony-stimulating factor production. J Biol Chem 1996, 271:28890-28897.
59. Srivastava S., Weitzmann M.N., Kimble R.B., Rizzo M., Zahner M., Milbrandt J., et al. Estrogen blocks M-CSF gene expression and osteoclast formation by regulating phosphorylation of EGR-1 and its interaction with Sp-1. J Clin Invest 1998, 102:1850-1859.
60. Wagner E.F. Functions of AP1 (Fos/Jun) in bone development. Ann Rheum Dis 2002, 61(SUPPL. 2):ii40-ii42.
61. Wagner E.F. Bone development and inflammatory disease is regulated by AP-1 (Fos/Jun). Ann Rheum Dis 2010, 69(SUPPL 1):i86-i88.
62. Weidemann A., Johnson R.S. Biology of HIF-1alpha. Cell Death Differ 2008, 15:621-627.
63. Silverman E.S., Collins T. Pathways of EGR-1-mediated gene transcription in vascular biology. Am J Pathol 1999, 154:665-670.
64. Li B., Berman J., Wu P., Liu F., Tang J.T., Lin T.J. The early growth response factor-1 contributes to interleukin-13 production by mast cells in response to stem cell factor stimulation. J Immunotoxicol 2008, 5:163-171.
65. Sakamoto K.M., Fraser J.K., Lee H.J., Lehman E., Gasson J.C. Granulocyte-macrophage colony-stimulating factor and interleukin-3 signaling pathways converge on the CREB-binding site in the human EGR-1 promoter. Mol Cell Biol 1994, 14:5975-5985.
66. Hatton J.P., Pooran M., Li C.F., Luzzio C., Hughes-Fulford M. A short pulse of mechanical force induces gene expression and growth in MC3T3-E1 osteoblasts via an ERK 1/2 pathway. J Bone Miner Res 2003, 18:58-66.
67. Lee D.Y., Yeh C.R., Chang S.F., Lee P.L., Chien S., Cheng C.K., et al. Integrin-mediated expression of bone formation-related genes in osteoblast-like cells in response to fluid shear stress: roles of extracellular matrix, Shc, and mitogen-activated protein kinase. J Bone Miner Res 2008, 23:1140-1149.