Evidence of in vivo osteoinduction in adult rat bone by adeno-Runx2 intra-femoral delivery

Journal of Cellular Biochemistry

Volumn 103, Issue 6, 2008, Pages 1912-1924

  Bhat, Bheem M ^a   Robinson, John A ^a   Coleburn, Valerie E ^a   Zhao, Weiguang ^a,b   Kharode, Yogendra ^a  

^a PFIZER INC   (United States)

^b SANOFI   (France)

Author keywords

Adeno; BMP 2; Gene therapy; Intra femoral; OSE2; Osteogenesis; Runx2

Indexed keywords

ADENOVIRUS VECTOR; RECOMBINANT BONE MORPHOGENETIC PROTEIN 2; TRANSCRIPTION FACTOR RUNX2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE DENSITY; BONE DEVELOPMENT; BONE DISEASE; BONE MINERALIZATION; BONE REGENERATION; CALVARIA; CELL ISOLATION; EMBRYO; FEMUR; FEMUR SHAFT; GENE OVEREXPRESSION; GENETIC TRANSDUCTION; HUMAN; HUMAN CELL; IN VIVO GENE TRANSFER; MALE; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; PERIOSTEUM; PRIORITY JOURNAL; PROTEIN INDUCTION; PROTEIN SYNTHESIS REGULATION; TRABECULAR BONE; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY;

ADENOVIRIDAE; AMINO ACID SEQUENCE; ANIMALS; BONE DENSITY; BONE MORPHOGENETIC PROTEINS; CELL LINE; CORE BINDING FACTOR ALPHA 1 SUBUNIT; FEMUR; GENE TRANSFER TECHNIQUES; HUMANS; MALE; MESENCHYMAL STEM CELLS; MICE; MOLECULAR SEQUENCE DATA; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT PROTEINS; SKULL; TRANSFORMING GROWTH FACTOR BETA;

ADENOVIRIDAE; RATTUS;

EID: 41849125289     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.21581     Document Type: Article

References (58)

1. Afzal F, Pratap J, Ito K, Ito Y, Stein JL, van Wijnen AJ, Stein GS, Lian JB, Javed A. 2005. Smad function and intranuclear targeting share a Runx2 motif required for osteogenic lineage induction and BMP2 responsive transcription. J Cell Physiol 204:63-72.
2. Bae JS, Gutierrez S, Narla R, Pratap J, Devados R, van Wijnen AJ, Stein JL, Stein GS, Lian JB, Javed A. 2007. Reconstitution of Runx2/Cbfal-null cells identifies a requirement for BMP2 signaling through a Runx2 functional domain during osteoblast differentiation. J Cell Biochem 100:434-449.
3. Banerjee C, McCabe LR, Choi JY, Hiebert SW, Stein JL, Stein GS, Lian JB. 1997. Runt homology domain proteins in osteoblast differentiation: AML3/CBFA1 is a major component of a bone-specific complex. J Cell Biochem 66:1-8.
4. Barnes PW, Eby CS, Shimer G. 2004. An evaluation of the utility of performing body fluid counts on the coulter LH 750. Lab Hematol 10:127-131.
5. Bhat BM, Brady HA, Pursley MH, Wold WS. 1986. Deletion mutants that alter differential RNA processing in the E3 complex transcription unit of adenovirus. J Mol Biol 190:543-557.
6. Bhat BM, Robinson JA, Coleburn VE, Mangine A, Saginario C, Hsiao C, Bex F. 2000. Identification of different forms of human CBFA1 in osteoblasts and evaluation of their functional activity. J Bone Miner Res 18:S373.
7. Bhat BM, Coleburn VE, Dell VL, Borella L, Kharode YP, Pittman DD, Bex F. 2001. Development of intra-femoral gene delivery model in the rat using recombinant human adeno-BMP9 virus. J Bone Miner Res 16:S439.
8. Bodine PV, Komm BS. 1999. Evidence that conditionally immortalized human osteoblasts express an osteocalcin receptor. Bone 25:535-543.
9. Byers BA, Garcia AJ. 2004. Exogenous Runx2 expression enhances in vitro osteoblastic differentiation and mineralization in primary bone marrow stromal cells. Tissue Eng 10:1623-1632.
10. Byers BA, Guldberg RE, Garcia AJ. 2004. Synergy between genetic and tissue engineering: Runx2 overexpression and in vitro construct development enhance in vivo mineralization. Tissue Eng 10:1757-1766.
11. Byers BA, Guldberg RE, Hutmacher DW, Garcia AJ. 2005. Effects of Runx2 genetic engineering and in vitro maturation of tissue-engineered constructs on the repair of critical size bone defects. J Biomed Mater Res A 76:646-655.
12. Chadderdon RC, Shimer AL, Gilbertson LG, Kang JD. 2004. Advances in gene therapy for intervertebral disc degeneration. Spine J 4:341S-347S.
13. Ducy P, Karsenty G. 1995. Two distinct osteoblast-specific cis-acting elements control expression of a mouse osteocalcin gene. Mol Cell Biol 15:1858-1869.
14. Ducy P, Starbuck M, Priemel M, Shen J, Pinero G, Geoffroy V, Aiming M, Karsenty G. 1999. A Cbfal-dependent genetic pathway controls bone formation beyond embryonic development. Genes Dev 13:1025-1036.
15. Evans CH, Ghivizzani SC, Herndon JH, Robbins PD. 2005. Gene therapy for the treatment of musculoskeletal diseases. J Am Acad Orthop Surg 13:230-242.
16. Franceschi RT, Wang D, Krebsbach PH, Rutherford RB. 2000. Gene therapy for bone formation: In vitro and in vivo osteogenic activity of an adenovirus expressing B MP7. J Cell Biochem 78:476-486.
17. Gafni Y, Turgeman G, Liebergal M, Pelled G, Gazit Z, Gazit D. 2004. Stem cells as vehicles for orthopedic gene therapy. Gene Ther 11:417-426.
18. Gao YH, Shinki T, Yuasa T, Kataoka-Enomoto H, Komori T, Suda T, Yamaguchi A. 1998. Potential role of cbfa1, an essential transcriptional factor for osteoblast differentiation, in osteoclastogenesis: Regulation of mRNA expression of osteoclast differentiation factor (ODF). Biochem Biophys Res Commun 252:697-702.
19. Geoffroy V, Ducy P, Karsenty G. 1995. A PEBP2 alpha/AML-1-related factor increases osteocalcin promoter activity through its binding to an osteoblast-specific cis-acting element. J Biol Chem 270:30973-30979.
20. Geoffroy V, Kneissel M, Fournier B, Boyde A, Matthias P. 2002. High bone resorption in adult aging transgenic mice overexpressing cbfa1/runx2 in cells of the osteoblastic lineage. Mol Cell Biol 22:6222-6233.
21. Gersbach CA, Le Doux JM, Guldberg RE, Garcia AJ. 2006. Inducible regulation of Runx2-stimulated osteogenesis. Gene Ther 13:873-882.
22. Giuhani N, Colla S, Morandi F, Lazzaretti M, Sala R, Bonomini S, Grano M, Colucci S, Svaldi M, Rizzoli V. 2005. Myeloma cells block RUNX2/CBFA1 activity in human bone marrow osteoblast progenitors and inhibit osteoblast formation and differentiation. Blood 106:2472-2483.
23. Ji C, Casinghino S, Chang DJ, Chen Y, Javed A, Ito Y, Hiebert SW, Lian JB, Stein GS, McCarthy TL, Centrella M. 1998. CBFa(AML/PEBP2)-related elements in the TGF-beta type I receptor promoter and expression with osteoblast differentiation. J Cell Biochem 69:353-363.
24. Kadowaki A, Tsukazaki T, Hirata K, Shibata Y, Okubo Y, Bessho K, Komori T, Yoshida N, Yamaguchi A. 2004. Isolation and characterization of a mesenchymal cell line that differentiates into osteoblasts in response to BMP-2 from calvariae of GFP transgenic mice. Bone 34:993-1003.
25. Kimelman N, Pelled G, Helm GA, Huard J, Schwarz EM, Gazit D. 2007. Review: Gene- and stem cell-based therapeutics for bone regeneration and repair. Tissue Eng 13:1135-1150.
26. Komori T, Yagi H, Nomura S, Yamaguchi A, Sasaki K, Deguchi K, Shimizu Y, Bronson RT, Gao YH, Inada M, Sato M, Okamoto R, Kitamura Y, Yoshiki S, Kishimoto T. 1997. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 89:755-764.
27. Krishnan V, Moore TL, Ma YL, Helvering LM, Frolik CA, Valasek KM, Ducy P, Geiser AG. 2003. Parathyroid hormone bone anabolic action requires Cbfa1/Runx2-dependent signaling. Mol Endocrinol 17:423-435.
28. Lieberman JR, Ghivizzani SC, Evans CH. 2002. Gene transfer approaches to the healing of bone and cartilage. Mol Ther 6:141-147.
29. Liu W, Toyosawa S, Furuichi T, Kanatani N, Yoshida C, Liu Y, Himeno M, Narai S, Yamaguchi A, Komori T. 2001. Overexpression of Cbfa1 in osteoblasts inhibits osteoblast maturation and causes osteopenia with multiple fractures. J Cell Biol 155:157-166.
30. Liu T, Gao Y, Sakamoto K, Minamizato T, Furukawa K, Tsukazaki T, Shibata Y, Bessho K, Komori T, Yamaguchi A. 2007. BMP-2 promotes differentiation of osteoblasts and chondroblasts in Runx2-deficient cell lines. J Cell Physiol 211:728-735.
31. McCauslin CS, Wine J, Cheng L, Klarmann KD, Candotti F, Clausen PA, Spence SE, Keller JR. 2003. In vivo retroviral gene transfer by direct intrafemoral injection results in correction of the SCID phenotype in Jak3 knock-out animals. Blood 102:843-848.
32. Mundlos S, Otto F, Mundlos C, Mulliken JB, Aylsworth AS, Albright S, Lindhout D, Cole WG, Henn W, Knoll JH, Owen MJ, Mertelsmann R, Zabel BU, Olsen BR. 1997. Mutations involving the transcription factor CBFA1 cause cleidocranial dysplasia. Cell 89:773-779.
33. Mundy G, Garrett R, Harris S, Chan J, Chen D, Rossini G, Boyce B, Zhao M, Gutierrez G. 1999. Stimulation of bone formation in vitro and in rodents by statins. Science 286:1946-1949.
34. Musgrave DS, Bosch P, Ghivizzani S, Robbins PD, Evans CH, Huard J. 1999. Adenovirus-mediated direct gene therapy with bone morphogenetic protein-2 produces bone. Bone 24:541-547.
35. Paabo S, Bhat BM, Wold WS, Peterson PA. 1987. A short sequence in the COOH-terminus makes an adenovirus membrane glycoprotein a resident of the endoplasmic reticulum. Cell 50:311-317.
36. Phimphilai M, Zhao Z, Boules H, Roca H, Franceschi RT. 2006. BMP signaling is required for RUNX2-dependent induction of the osteoblast phenotype. J Bone Miner Res 21:637-646.
37. Porada CD, Tran ND, Zhao Y, Anderson WF, Zanjani ED. 2000. Neonatal gene therapy, transfer and expression of exogenous genes in neonatal sheep following direct injection of retroviral vectors into the bone marrow space. Exp Hematol 28:642-650.
38. Pratap J, Galindo M, Zaidi SK, Vradii D, Bhat BM, Robinson JA, Choi JY, Komori T, Stein JL, Lian JB, Stein GS, van Wijnen AJ. 2003. Cell growth regulatory role of Runx2 during proliferative expansion of preosteoblasts. Cancer Res 63:5357-5362.
39. Rossert JA, Chen SS, Eberspaecher H, Smith CN, de Crombrugghe B. 1996. Identification of a minimal sequence of the mouse pro-alpha 1(I) collagen promoter that confers high-level osteoblast expression in transgenic mice and that binds a protein selectively present in osteoblasts. Proc Natl Acad Sci USA 93:1027-1031.
40. Sadowski HB, Gilman MZ. 1993. Cell-free activation of a DNA-binding protein by epidermal growth factor. Nature 362:79-83.
41. Sadowski HB, Shuai K, Darnell JE Jr, Gilman MZ. 1993. A common nuclear signal transduction pathway activated by growth factor and cytokine receptors. Science 261:1739-1744.
42. Schreiber RE, Blease K, Ambrosio A, Amburn E, Sosnowski B, Sampath TK. 2005. Bone induction by AdBMP-2/collagen implants. J Bone Joint Surg Am 87:1059-1068.
43. Seeherman H, Wozney JM. 2005. Delivery of bone morphogenetic proteins for orthopedic tissue regeneration. Cytokine Growth Factor Rev 16:329-345.
44. Sevetson B, Taylor S, Pan Y. 2004. Cbfal/RUNX2 directs specific expression of the sclerosteosis gene (SOST). J Biol Chem 279:13849-13858.
45. Shimer AL, Chadderdon RC, Gilbertson LG, Kang JD. 2004. Gene therapy approaches for intervertebral disc degeneration. Spine 29:2770-2778.
46. Shuai K, Ziemiecki A, Wilks AF, Harpur AG, Sadowski HB, Gilman MZ, Darnell JE. 1993. Polypeptide signalling to the nucleus through tyrosine phosphorylation of Jak and Stat proteins. Nature 366:580-583.
47. Stanford CM, Jacobson PA, Eanes ED, Lembke LA, Midura RJ. 1995. Rapidly forming apatitic mineral in an osteoblastic cell line (UMR 106-01 BSP). J Biol Chem 270:9420-9428.
48. Stewart M, Terry A, Hu M, O'Hara M, Blyth K, Baxter E, Cameron E, Onions DE, Neil JC. 1997. Proviral insertions induce the expression of bone-specific isoforms of PEBP2alphaA (CBFA1): Evidence for a new myc collaborating oncogene. Proc Natl Acad Sci USA 94:8646-8651.
49. Urist MR, Huo YK, Brownell AG, Hohl WM, Buyske J, Lietze A, Tempst P, Hunkapiller M, DeLange RJ. 1984. Purification of bovine bone morphogenetic protein by hydroxyapatite chromatography. Proc Natl Acad Sci USA 81:371-375.
50. Westendorf JJ. 2006. Transcriptional co-repressors of Runx2. J Cell Biochem 98:54-64.
51. Wozney JM. 2002. Overview of bone morphogenetic proteins. Spine 27:S2-S8.
52. Wozney JM, Seeherman HJ. 2004. Protein-based tissue engineering in bone and cartilage repair. Curr Opin Biotechnol 15:392-398.
53. Yamaguchi A, Komori T, Suda T. 2000. Regulation of osteoblast differentiation mediated by bone morphogenetic proteins, hedgehogs, and Cbfa1. Endocr Rev 21:393-411.
54. Yang S, Wei D, Wang D, Phimphilai M, Krebsbach PH, Franceschi RT. 2003. In vitro and in vivo synergistic interactions between the Runx2/Cbfal transcription factor and bone morphogenetic protein-2 in stimulating osteoblast differentiation. J Bone Miner Res 18:705-715.
55. Young DW, Pratap J, Javed A, Weiner B, Ohkawa Y, van Wijnen A, Montecino M, Stein GS, Stein JL, Imbalzano AN, Lian JB. 2005. SWI/SNF chromatin remodeling complex is obligatory for BMP2-induced, Runx2-dependent skeletal gene expression that controls osteoblast differentiation. J Cell Biochem 94:720-730.
56. Zhang Y, Li Z, Thonar EJ, An HS, He TC, Pietryla D, Phillips FM. 2005. Transduced bovine articular chondrocytes affect the metabolism of cocultured nucleus pulposus cells in vitro: Implications for chondrocyte transplantation into the intervertebral disc. Spine 30:2601-2607.
57. Zhao Z, Zhao M, Xiao G, Franceschi RT. 2005. Gene transfer of the Runx2 transcription factor enhances osteogenic activity of bone marrow stromal cells in vitro and in vivo. Mol Ther 12:247-253.
58. Zheng H, Guo Z, Ma Q, Jia H, Dang G. 2004. Cbfa1/osf2 transduced bone marrow stromal cells facilitate bone formation in vitro and in vivo. Calcif Tissue Int 74:194-203.