Prolyl hydroxylase inhibitors increase neoangiogenesis and callus formation following femur fracture in mice

Journal of Orthopaedic Research

Volumn 27, Issue 10, 2009, Pages 1298-1305

  Shen, Xing ^a,b   Wan, Chao ^c   Ramaswamy, Girish ^d   Mavalli, Mahendra ^c   Wang, Ying ^c   Duvall, Craig L ^e   Lian, Fu Deng ^b   Guldberg, Robert E ^e   Eberhart, Alan ^d   Clemens, Thomas L ^c   Gilbert, Shawn R ^b  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b Kentucky   (United States)

^c University of Alabama at Birmingham   (United States)

^d and Radiation Oncology   (United States)

^e GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Fracture healing; Hypoxia inducible factor; Prolyl hydroxylase inhibitor; Vascularity

Indexed keywords

ANGIOGENIC FACTOR; COMPLEMENTARY DNA; DEFEROXAMINE; DIMETHYLOXALYLGLYCINE; ENZYME INHIBITOR; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MESSENGER RNA; MIMOSINE; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; PROLYL HYDROXYLASE INHIBITOR; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOMECHANICS; BONE INJURY; BONE MARROW; CALLUS; COMPUTED TOMOGRAPHY SCANNER; CONTROLLED STUDY; ENZYME INHIBITION; FEMUR; FEMUR FRACTURE; FRACTURE HEALING; HISTOLOGY; LOADING TEST; MALE; MESENCHYME CELL; METATARSAL BONE; MICRO-COMPUTED TOMOGRAPHY; MOUSE; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; NUCLEOTIDE SEQUENCE; OSSIFICATION; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; STROMA CELL; TIBIA; TISSUE REPAIR; WESTERN BLOTTING;

AMINO ACIDS, DICARBOXYLIC; ANIMALS; BONY CALLUS; CELL PROLIFERATION; DEFEROXAMINE; ENDOTHELIUM, VASCULAR; FEMORAL FRACTURES; HYPOXIA-INDUCIBLE FACTOR 1; MALE; MICE; MICE, INBRED C57BL; MIMOSINE; MODELS, ANIMAL; NEOVASCULARIZATION, PHYSIOLOGIC; PROCOLLAGEN-PROLINE DIOXYGENASE; RNA, MESSENGER; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 70349220913     PISSN: 07360266     EISSN: None     Source Type: Journal    
DOI: 10.1002/jor.20886     Document Type: Article

References (39)

1. U.S. Bone and Joint Decade. 2008. The burden of musculoskeletal diseases in the United States. Rosemont, IL: AAOS. p 268.
2. Eckardt H, Ding M, Lind M, et al. 2005. Recombinant human vascular endothelial growth factor enhances bone healing in an experimental nonunion model. J Bone Joint Surg Br 87:1434-1438. (Pubitemid 41511813)
3. Street J, Bao M, deGuzman L, et al. 2002. Vascular endothelial growth factor stimulates bone repair by promoting angiogenesis and bone turnover. Proc Natl Acad Sci USA 99:9656-9661.
4. Murnaghan M, Li G, Marsh DR. 2006. Nonsteroidal antiinflammatory drug-induced fracture nonunion: an inhibition of angiogenesis? J Bone Joint Surg Am 88(Suppl 3):140-147.
5. Li R, Stewart DJ, von Schroeder HP, et al. 2008. Effect of cell-based VEGF gene therapy on healing of a segmental bone defect. J Orthop Res 27:8-14.
6. Eckardt H, Bundgaard KG, Christensen KS, et al. 2003. Effects of locally applied vascular endothelial growth factor (VEGF) and VEGF-inhibitor to the rabbit tibia during distraction osteogenesis. J Orthop Res 21:335-340. (Pubitemid 36322555)
7. Wan C, Gilbert SR, Wang Y, et al. 2008. Activation of the hypoxia-inducible factor-1alpha pathway accelerates bone regeneration. Proc Natl Acad Sci USA 105:686-691. (Pubitemid 351171769)
8. Huang LE, Gu J, Schau M, Bunn HF. 1998. Regulation of hypoxia-inducible factor 1alpha is mediated by an O2-dependent degradation domain via the ubiquitin-proteasome pathway. Proc Natl Acad Sci USA 95:7987-7992. (Pubitemid 28326053)
9. Ivan M, Kondo K, Yang H, et al. 2001. HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science 292:464-468. (Pubitemid 32335941)
10. Wang GL, Semenza GL. 1993. Desferrioxamine induces erythropoietin gene expression and hypoxia-inducible factor 1 DNA-binding activity: implications for models of hypoxia signal transduction. Blood 82:3610-3615.
11. Warnecke C, Griethe W, Weidemann A, et al. 2003. Activation of the hypoxia-inducible factor-pathway and stimulation of angiogenesis by application of prolyl hydroxylase inhibitors. Faseb J 17:1186-1188.
12. Chau NM, Rogers P, Aherne W, et al. 2005. Identification of novel small molecule inhibitors of hypoxia-inducible factor-1 that differentially block hypoxia-inducible factor-1 activity and hypoxia-inducible factor-1alpha induction in response to hypoxic stress and growth factors. Cancer Res 65:4918-4928. (Pubitemid 40740832)
13. Rapisarda A, Uranchimeg B, Scudiero DA, et al. 2002. Identification of small molecule inhibitors of hypoxia-inducible factor 1 transcriptional activation pathway. Cancer Res 62:4316-4324. (Pubitemid 34827288)
14. Wang Y, Wan C, Deng L, et al. 2007. The hypoxia-inducible factor alpha pathway couples angiogenesis to osteogenesis during skeletal development. J Clin Invest 117:1616-1626. (Pubitemid 46871346)
15. Duvall CL, Taylor WR, Weiss D, et al. 2007. Impaired angiogenesis, early callus formation, and late stage remodeling in fracture healing of osteopontin deficient mice. J Bone Miner Res 22:286-297. (Pubitemid 46167799)
16. Gerstenfeld LC, Alkhiary YM, Krall EA, et al. 2006. Three-dimensional reconstruction of fracture callus morphogenesis. J Histochem Cytochem 54:1215-1228.
17. Bickel M, Baringhaus KH, Gerl M, et al. 1998. Selective inhibition of hepatic collagen accumulation in experimental liver fibrosis in rats by a new prolyl 4-hydroxylase inhibitor. Hepatology 28:404-411. (Pubitemid 28363666)
18. Komatsu DE, Bosch-Marce M, Semenza GL, et al. 2007. Enhanced bone regeneration associated with decreased apoptosis in mice with partial HIF-1alpha deficiency. J Bone Miner Res 22:366-374. (Pubitemid 46797119)
19. Greijer AE, van der Wall E. 2004. The role of hypoxia inducible factor 1 (HIF-1) in hypoxia induced apoptosis. J Clin Pathol 57:1009-1014. (Pubitemid 39331346)
20. Ilizarov GA. 1989. The tension-stress effect on the genesis and growth of tissues. Part I. The influence of stability of fixation and soft-tissue preservation. Clin Orthop Relat Res 238:249-281.
21. Pacicca DM, Patel N, Lee C, et al. 2003. Expression of angiogenic factors during distraction osteogenesis. Bone 33:889-898. (Pubitemid 37543565)
22. Gerstenfeld LC, Cullinane DM, Barnes GL, et al. 2003. Fracture healing as a post-natal developmental process: molecular, spatial, and temporal aspects of its regulation. J Cell Biochem 88:873-884.
23. Ferguson C, Alpern E, Miclau T, et al. 1999. Does adult fracture repair recapitulate embryonic skeletal formation? Mech Dev 87:57-66.
24. Peng H, Usas A, Olshanski A, et al. 2005. VEGF improves, whereas sFlt1 inhibits, BMP2-induced bone formation and bone healing through modulation of angiogenesis. J Bone Miner Res 20:2017-2027. (Pubitemid 41532787)
25. Geiger F, Bertram H, Berger I, et al. 2005. Vascular endothelial growth factor gene-activated matrix (VEGF165- GAM) enhances osteogenesis and angiogenesis in large segmental bone defects. J Bone Miner Res 20:2028-2035. (Pubitemid 41532788)
26. Kelly BD, Hackett SF, Hirota K, et al. 2003. Cell type-specific regulation of angiogenic growth factor gene expression and induction of angiogenesis in nonischemic tissue by a constitutively active form of hypoxia-inducible factor 1. Circ Res 93:1074-1081. (Pubitemid 37485038)
27. Yamakawa M, Liu LX, Date T, et al. 2003. Hypoxia-inducible factor-1 mediates activation of cultured vascular endothelial cells by inducing multiple angiogenic factors. Circ Res 93:664-673. (Pubitemid 37222163)
28. Rajpurohit R, Koch CJ, Tao Z, et al. 1996. Adaptation of chondrocytes to low oxygen tension: relationship between hypoxia and cellular metabolism. J Cell Physiol 168:424-432. (Pubitemid 26308754)
29. Ceradini DJ, Kulkarni AR, Callaghan MJ, et al. 2004. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat Med 10:858-864.
30. Dominici M, Pritchard C, Garlits JE, et al. 2004. Hematopoietic cells and osteoblasts are derived from a common marrow progenitor after bone marrow transplantation. Proc Natl Acad Sci USA 101:11761-11766. (Pubitemid 39095369)
31. Khosla S, Eghbali-Fatourechi GZ. 2006. Circulating cells with osteogenic potential. Ann N Y Acad Sci 1068:489-497.
32. Emans PJ, Spaapen F, Surtel DA, et al. 2007. A novel in vivo model to study endochondral bone formation; HIF-1alpha activation and BMP expression. Bone 40:409-418. (Pubitemid 46054546)
33. Robins JC, Akeno N, Mukherjee A, et al. 2005. Hypoxia induces chondrocyte-specific gene expression in mesenchymal cells in association with transcriptional activation of Sox9. Bone 37:313-322. (Pubitemid 41160490)
34. Kanichai M, Ferguson D, Prendergast PJ, et al. 2008. Hypoxia promotes chondrogenesis in rat mesenchymal stem cells: a role for AKT and hypoxia-inducible factor (HIF)-1alpha. J Cell Physiol 216:708-715.
35. Alcantara O, Reddy SV, Roodman GD, et al. 1994. Transcriptional regulation of the tartrate-resistant acid phosphatase (TRAP) gene by iron. Biochem J 298(Pt 2):421-425. (Pubitemid 24072487)
36. Fleckenstein E, Dirks W, Dehmel U, et al. 1996. Cloning and characterization of the human tartrate-resistant acid phosphatase (TRAP) gene. Leukemia 10:637-643. (Pubitemid 26144443)
37. Camacho M, Lopez-Belmonte J, Vila L. 1998. Rate of vasoconstrictor prostanoids released by endothelial cells depends on cyclooxygenase-2 expression and prostaglandin I synthase activity. Circ Res 83:353-365. (Pubitemid 28389965)
38. Grimmer C, Pfander D, Swoboda B, et al. 2007. Hypoxia-inducible factor 1alpha is involved in the prostaglandin metabolism of osteoarthritic cartilage through up-regulation of microsomal prostaglandin E synthase 1 in articular chondrocytes. Arthritis Rheum 56:4084-4094. (Pubitemid 350262336)
39. Tanji K, Imaizumi T, Matsumiya T, et al. 2001. Desferrioxamine, an iron chelator, upregulates cyclooxygenase-2 expression and prostaglandin production in a human macrophage cell line. Biochim Biophys Acta 1530:227-235.