The role of oxygen during fracture healing

Bone

Volumn 52, Issue 1, 2013, Pages 220-229

  Lu, Chuanyong ^a,c   Saless, Neema ^a   Wang, Xiaodong ^a   Sinha, Arjun ^a   Decker, Sebastian ^a   Kazakia, Galateia ^a   Hou, Huagang ^b   Williams, Benjamin ^b   Swartz, Harold M ^b   Hunt, Thomas K ^a   Miclau, Theodore ^a   Marcucio, Ralph S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b DARTMOUTH MEDICAL SCHOOL   (United States)

^c SUNY Downstate Medical Center   (United States)

Author keywords

Angiogenesis; Fracture; Hyperoxia; Hypoxia; Oxygen

Indexed keywords

OXYGEN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE DEVELOPMENT; BONE REMODELING; BONE TISSUE; CALLUS; CELL ACTIVITY; CELL DIFFERENTIATION; CELL MOTION; CHONDROGENESIS; FRACTURE HEALING; FRACTURE NONUNION; HYPEROXIA; HYPOXIA; INFLAMMATORY CELL; ISCHEMIA; MACROPHAGE MIGRATION; MALE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; OSSIFICATION; OXYGEN TENSION; OXYGEN TISSUE LEVEL; STEM CELL; TIBIA FRACTURE; VASCULARIZATION;

ANIMALS; CELL DIFFERENTIATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; FRACTURE HEALING; MICE; OXYGEN; STEM CELLS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84867897196     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2012.09.037     Document Type: Article

References (51)

1. Dickson K.F., Katzman S., Paiement G. The importance of the blood supply in the healing of tibial fractures. Contemp Orthop 1995, 30:489-493.
2. Brinker M.R., Bailey D.E. Fracture healing in tibia fractures with an associated vascular injury. J Trauma 1997, 42:11-19.
3. Lu C., Miclau T., Hu D., et al. Ischemia leads to delayed union during fracture healing: a mouse model. J Orthop Res 2007, 25:51-61.
4. Lu C., Rollins M., Hou H., et al. Tibial fracture decreases oxygen levels at the site of injury. Iowa Orthop J 2008, 28:14-21.
5. Zhang X., Schwarz E.M., Young D.A., et al. Cyclooxygenase-2 regulates mesenchymal cell differentiation into the osteoblast lineage and is critically involved in bone repair. J Clin Invest 2002, 109:1405-1415.
6. Xie C., Liang B., Xue M., et al. Rescue of impaired fracture healing in COX-2-/- mice via activation of prostaglandin E2 receptor subtype 4. Am J Pathol 2009, 175:772-785.
7. Kivirikko K.I., Prockop D.J. Enzymatic hydroxylation of proline and lysine in protocollagen. Proc Natl Acad Sci U S A 1967, 57:782-789.
8. Fong G.H. Regulation of angiogenesis by oxygen sensing mechanisms. J Mol Med 2009, 87:549-560.
9. Lin Q., Lee Y.J., Yun Z. Differentiation arrest by hypoxia. J Biol Chem 2006, 281:30678-30683.
10. Thom S.R., Bhopale V.M., Velazquez O.C., et al. Stem cell mobilization by hyperbaric oxygen. Am J Physiol Heart Circ Physiol 2006, 290:H1378-H1386.
11. Gallagher K.A., Liu Z.J., Xiao M., et al. Diabetic impairments in NO-mediated endothelial progenitor cell mobilization and homing are reversed by hyperoxia and SDF-1 alpha. J Clin Invest 2007, 117:1249-1259.
12. Liu Z.J., Velazquez O.C. Hyperoxia, endothelial progenitor cell mobilization, and diabetic wound healing. Antioxid Redox Signal 2008, 10:1869-1882.
13. Ceradini D.J., Kulkarni A.R., Callaghan M.J., et al. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat Med 2004, 10:858-864.
14. Wu D., Malda J., Crawford R., et al. Effects of hyperbaric oxygen on proliferation and differentiation of osteoblasts from human alveolar bone. Connect Tissue Res 2007, 48:206-213.
15. Nicolaije C., Koedam M., van Leeuwen J.P. Decreased oxygen tension lowers reactive oxygen species and apoptosis and inhibits osteoblast matrix mineralization through changes in early osteoblast differentiation. J Cell Physiol 2012, 227:1309-1318.
16. Hirao M., Hashimoto J., Yamasaki N., et al. Oxygen tension is an important mediator of the transformation of osteoblasts to osteocytes. J Bone Miner Metab 2007, 25:266-276.
17. Genetos D.C., Toupadakis C.A., Raheja L.F., et al. Hypoxia decreases sclerostin expression and increases Wnt signaling in osteoblasts. J Cell Biochem 2010, 110:457-467.
18. Tseng W.P., Yang S.N., Lai C.H., et al. Hypoxia induces BMP-2 expression via ILK, Akt, mTOR, and HIF-1 pathways in osteoblasts. J Cell Physiol 2010, 223:810-818.
19. Steinbrech D.S., Mehrara B.J., Saadeh P.B., et al. Hypoxia increases insulinlike growth factor gene expression in rat osteoblasts. Ann Plast Surg 2000, 44:529-534. discussion 534-5.
20. Steinbrech D.S., Mehrara B.J., Saadeh P.B., et al. Hypoxia regulates VEGF expression and cellular proliferation by osteoblasts in vitro. Plast Reconstr Surg 1999, 104:738-747.
21. Lin C., McGough R., Aswad B., et al. Hypoxia induces HIF-1alpha and VEGF expression in chondrosarcoma cells and chondrocytes. J Orthop Res 2004, 22:1175-1181.
22. Coyle C.H., Izzo N.J., Chu C.R. Sustained hypoxia enhances chondrocyte matrix synthesis. J Orthop Res 2009, 27:793-799.
23. Duval E., Leclercq S., Elissalde J.M., et al. Hypoxia-inducible factor 1alpha inhibits the fibroblast-like markers type I and type III collagen during hypoxia-induced chondrocyte redifferentiation: hypoxia not only induces type II collagen and aggrecan, but it also inhibits type I and type III collagen in the hypoxia-inducible factor 1alpha-dependent redifferentiation of chondrocytes. Arthritis Rheum 2009, 60:3038-3048.
24. Henderson J.H., Ginley N.M., Caplan A.I., et al. Low oxygen tension during incubation periods of chondrocyte expansion is sufficient to enhance postexpansion chondrogenesis. Tissue Eng Part A 2010, 16:1585-1593.
25. Rajpurohit R., Koch C.J., Tao Z., et al. Adaptation of chondrocytes to low oxygen tension: relationship between hypoxia and cellular metabolism. J Cell Physiol 1996, 168:424-432.
26. Farnum C.E., Lenox M., Zipfel W., et al. In vivo delivery of fluoresceinated dextrans to the murine growth plate: imaging of three vascular routes by multiphoton microscopy. Anat Rec A Discov Mol Cell Evol Biol 2006, 288:91-103.
27. Arnett T.R., Gibbons D.C., Utting J.C., et al. Hypoxia is a major stimulator of osteoclast formation and bone resorption. J Cell Physiol 2003, 196:2-8.
28. Muzylak M., Price J.S., Horton M.A. Hypoxia induces giant osteoclast formation and extensive bone resorption in the cat. Calcif Tissue Int 2006, 79:301-309.
29. Hunt T.K., Aslam R., Hussain Z., et al. Lactate, with oxygen, incites angiogenesis. Adv Exp Med Biol 2008, 614:73-80.
30. Hunt T.K., Aslam R.S., Beckert S., et al. Aerobically derived lactate stimulates revascularization and tissue repair via redox mechanisms. Antioxid Redox Signal 2007, 9:1115-1124.
31. Milovanova T.N., Bhopale V.M., Sorokina E.M., et al. Hyperbaric oxygen stimulates vasculogenic stem cell growth and differentiation in vivo. J Appl Physiol 2009, 106:711-728.
32. Lu C., Saless N., Hu D., et al. Mechanical stability affects angiogenesis during early fracture healing. J Orthop Trauma 2011, 25:494-499.
33. Lu C., Miclau T., Hu D., et al. Cellular basis for age-related changes in fracture repair. J Orthop Res 2005, 23:1300-1307.
34. Lu C., Hansen E., Sapozhnikova A., et al. Effect of age on vascularization during fracture repair. J Orthop Res 2008, 26:1384-1389.
35. Xing Z., Lu C., Hu D., et al. Multiple roles for CCR2 during fracture healing. Dis Model Mech 2010, 3:451-458.
36. 2 measurements by electron paramagnetic resonance oximetry: current status and future potential for experimental and clinical studies. Antioxid Redox Signal 2007, 9:1169-1182.
37. Goldman R.J. Hyperbaric oxygen therapy for wound healing and limb salvage: a systematic review. PM R 2009, 1:471-489.
38. Hunt T.K., Ellison E.C., Sen C.K. Oxygen: at the foundation of wound healing-introduction. World J Surg 2004, 28:291-293.
39. Yablon I.G., Cruess R.L. The effect of hyperbaric oxygen on fracture healing in rats. J Trauma 1968, 8:186-202.
40. Bennett M.H., Stanford R., Turner R. Hyperbaric oxygen therapy for promoting fracture healing and treating fracture non-union. Cochrane Database Syst Rev 2005, CD004712.
41. Shen X., Wan C., Ramaswamy G., et al. Prolyl hydroxylase inhibitors increase neoangiogenesis and callus formation following femur fracture in mice. J Orthop Res 2009, 27:1298-1305.
42. Knighton D.R., Silver I.A., Hunt T.K. Regulation of wound-healing angiogenesis-effect of oxygen gradients and inspired oxygen concentration. Surgery 1981, 90:262-270.
43. James J.H., Luchette F.A., McCarter F.D., et al. Lactate is an unreliable indicator of tissue hypoxia in injury or sepsis. Lancet 1999, 354:505-508.
44. Gladden L.B. Lactate metabolism: a new paradigm for the third millennium. J Physiol 2004, 558:5-30.
45. Hirao M., Tamai N., Tsumaki N., et al. Oxygen tension regulates chondrocyte differentiation and function during endochondral ossification. J Biol Chem 2006, 281:31079-31092.
46. Lafont J.E., Talma S., Hopfgarten C., et al. Hypoxia promotes the differentiated human articular chondrocyte phenotype through SOX9-dependent and -independent pathways. J Biol Chem 2008, 283:4778-4786.
47. Kitaori T., Ito H., Schwarz E.M., et al. Stromal cell-derived factor 1/CXCR4 signaling is critical for the recruitment of mesenchymal stem cells to the fracture site during skeletal repair in a mouse model. Arthritis Rheum 2009, 60:813-823.
48. Zhang X., Naik A., Xie C., et al. Periosteal stem cells are essential for bone revitalization and repair. J Musculoskelet Neuronal Interact 2005, 5:360-362.
49. Colnot C. Skeletal cell fate decisions within periosteum and bone marrow during bone regeneration. J Bone Miner Res 2009, 24:274-282.
50. Caplan A.I., Correa D. The MSC: an injury drugstore. Cell Stem Cell 2011, 9:11-15.
51. Trabold O., Wagner S., Wicke C., et al. Lactate and oxygen constitute a fundamental regulatory mechanism in wound healing. Wound Repair Regen 2003, 11:504-509.