Impaired angiogenesis during fracture healing in GPCR Kinase 2 interacting protein-1 (GIT1) knock out mice

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Yin, Guoyong ^a,b   Sheu, Tzong Jen ^a   Menon, Prashanthi ^a   Pang, Jinjiang ^a   Ho, Hsin Chiu ^a   Shi, Shanshan ^a   Xie, Chao ^a   Smolock, Elaine ^a   Yan, Chen ^a   Zuscik, Michael J ^a   Berk, Bradford C ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b NANJING MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ACID PHOSPHATASE TARTRATE RESISTANT ISOENZYME; CD31 ANTIGEN; COLLAGEN TYPE 2; G PROTEIN COUPLED RECEPTOR KINASE 2 INTERACTING PROTEIN 1; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 2; CELL CYCLE PROTEIN; GIT2 PROTEIN, MOUSE; PHOSPHOPROTEIN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BLOOD VESSEL; CALLUS; CARTILAGE CELL; CARTILAGE MATRIX; CELL PROLIFERATION; CONTROLLED STUDY; FRACTURE HEALING; MICRO-COMPUTED TOMOGRAPHY; MOUSE; NONHUMAN; OSTEOCLAST; ANIMAL; BONE; BONE REMODELING; C57BL MOUSE; CYTOLOGY; GENE EXPRESSION; GENETICS; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY; RADIOGRAPHY; VASCULARIZATION;

ANIMALS; BONE AND BONES; BONE REMODELING; BONY CALLUS; CELL CYCLE PROTEINS; CHONDROCYTES; FRACTURE HEALING; GENE EXPRESSION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEOVASCULARIZATION, PHYSIOLOGIC; OSTEOCLASTS; PHOSPHOPROTEINS; X-RAY MICROTOMOGRAPHY;

EID: 84896801533     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0089127     Document Type: Article

References (47)

1. Einhorn TA (1998) The cell and molecular biology of fracture healing. ClinOrthop: S7-21.
2. Gerstenfeld LC, Cullinane DM, Barnes GL, Graves DT, Einhorn TA (2003) Fracture healing as a post-natal developmental process: molecular, spatial, and temporal aspects of its regulation. JCell Biochem 88: 873-884. (Pubitemid 36337032)
3. Marsell R, Einhorn TA (2011) The biology of fracture healing. Injury 42: 551-555.
4. Thompson Z, Miclau T, Hu D, Helms JA (2002) A model for intramembranous ossification during fracture healing. Journal of Orthopaedic Research 20: 1091-1098.
5. Li G, White G, Connolly C, Marsh D (2002) Cell proliferation and apoptosis during fracture healing. J Bone Miner Res 17: 791-799. (Pubitemid 34441895)
6. Kon T, Cho TJ, Aizawa T, Yamazaki M, Nooh N, et al. (2001) Expression of osteoprotegerin, receptor activator of NF-kappaB ligand (osteoprotegerin ligand) and related proinflammatory cytokines during fracture healing. Journal of Bone and Mineral Research 16: 1004-1014. (Pubitemid 32467144)
7. Mountziaris PM, Mikos AG (2008) Modulation of the inflammatory response for enhanced bone tissue regeneration. Tissue Eng Part B Rev 14: 179-186. (Pubitemid 351839215)
8. Ai-Aql ZS, Alagl AS, Graves DT, Gerstenfeld LC, Einhorn TA (2008) Molecular mechanisms controlling bone formation during fracture healing and distraction osteogenesis. J Dent Res 87: 107-118.
9. Gerstenfeld LC, Sacks DJ, Pelis M, Mason ZD, Graves DT, et al. (2009) Comparison of effects of the bisphosphonate alendronate versus the RANKL inhibitor denosumab on murine fracture healing. J Bone Miner Res 24: 196-208.
10. Maes C, Kobayashi T, Selig MK, Torrekens S, Roth SI, et al. (2010) Osteoblast precursors, but not mature osteoblasts, move into developing and fractured bones along with invading blood vessels. Dev Cell 19: 329-344.
11. Pufe T, Wildemann B, Petersen W, Mentlein R, Raschke M, et al. (2002) Quantitative measurement of the splice variants 120 and 164 of the angiogenic peptide vascular endothelial growth factor in the time flow of fracture healing: a study in the rat. Cell Tissue Res 309: 387-392. (Pubitemid 34994877)
12. Eckardt H, Bundgaard KG, Christensen KS, Lind M, Hansen ES, 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)
13. Ferguson C, Alpern E, Miclau T, Helms JA (1999) Does adult fracture repair recapitulate embryonic skeletal formation? Mechanisms of Development 87: 57-66. (Pubitemid 29428086)
14. Glowacki J (1998) Angiogenesis in fracture repair. Clin Orthop Relat Res: S82-89.
15. Gerber HP, Vu TH, Ryan AM, Kowalski J, Werb Z, et al. (1999) VEGF couples hypertrophic cartilage remodeling, ossification and angiogenesis during endochondral bone formation. NatMed 5: 623-628. (Pubitemid 29289424)
16. Athanasopoulos AN, Schneider D, Keiper T, Alt V, Pendurthi UR, et al. (2007) Vascular endothelial growth factor (VEGF)-induced up-regulation of CCN1 in osteoblasts mediates proangiogenic activities in endothelial cells and promotes fracture healing. Journal of Biological Chemistry 282: 26746-26753. (Pubitemid 47501957)
17. Hausman MR, Schaffler MB, Majeska RJ (2001) Prevention of fracture healing in rats by an inhibitor of angiogenesis. Bone 29: 560-564. (Pubitemid 33124299)
18. Premont RT, Claing A, Vitale N, Freeman JL, Pitcher JA, et al. (1998) beta2-Adrenergic receptor regulation by GIT1, a G protein-coupled receptor kinase-associated ADP ribosylation factor GTPase-activating protein. Proc Natl Acad Sci U S A 95: 14082-14087. (Pubitemid 28549324)
19. Natarajan K, Yin G, Berk BC (2004) Scaffolds direct Src-specific signaling in response to angiotensin II: new roles for Cas and GIT1. Mol Pharmacol 65: 822-825. (Pubitemid 38420486)
20. Haendeler J, Yin G, Hojo Y, Saito Y, Melaragno M, et al. (2003) GIT1 mediates Src-dependent activation of phospholipase Cgamma by angiotensin II and epidermal growth factor. J Biol Chem 278: 49936-49944. (Pubitemid 37548829)
21. Yin G, Haendeler J, Yan C, Berk BC (2004) GIT1 functions as a scaffold for MEK1-extracellular signal-regulated kinase 1 and 2 activation by angiotensin II and epidermal growth factor. Mol Cell Biol 24: 875-885. (Pubitemid 38057937)
22. Pang J, Hoefen R, Pryhuber GS, Wang J, Yin G, et al. (2009) G-protein-coupled receptor kinase interacting protein-1 is required for pulmonary vascular development. Circulation 119: 1524-1532.
23. Wang J, Taba Y, Pang J, Yin G, Yan C, et al. (2009) GIT1 mediates VEGF-induced podosome formation in endothelial cells: critical role for PLCgamma. Arterioscler Thromb Vasc Biol 29: 202-208.
24. Menon P, Yin G, Smolock EM, Zuscik MJ, Yan C, et al. (2010) GPCR kinase 2 interacting protein 1 (GIT1) regulates osteoclast function and bone mass. J Cell Physiol 225: 777-785.
25. Xie C, Liang B, Xue M, Lin AS, Loiselle A, et al. (2009) Rescue of impaired fracture healing in COX-2-/- mice via activation of prostaglandin E2 receptor subtype 4. AmJPathol 175: 772-785.
26. Ito H, Koefoed M, Tiyapatanaputi P, Gromov K, Goater JJ, et al. (2005) Remodeling of cortical bone allografts mediated by adherent rAAV-RANKL and VEGF gene therapy. NatMed 11: 291-297. (Pubitemid 40460557)
27. Zhang X, Xie C, Lin AS, Ito H, Awad H, et al. (2005) Periosteal progenitor cell fate in segmental cortical bone graft transplantations: implications for functional tissue engineering. Journal of Bone and Mineral Research 20: 2124-2137. (Pubitemid 41698776)
28. Dhillon RS, Xie C, Tyler W, Calvi LM, Awad HA, et al. (2013) PTH-enhanced structural allograft healing is associated with decreased angiopoietin-2- mediated arteriogenesis, mast cell accumulation, and fibrosis. J Bone Miner Res 28: 586-597.
29. Duvall CL, Taylor WR, Weiss D, Guldberg RE (2004) Quantitative microcomputed tomography analysis of collateral vessel development after ischemic injury. Am J Physiol Heart Circ Physiol 287: H302-310. (Pubitemid 38802366)
30. Zhang X, Schwarz EM, Young DA, Puzas JE, Rosier RN, et al. (2002) Cyclooxygenase-2 regulates mesenchymal cell differentiation into the osteoblast lineage and is critically involved in bone repair. JClinInvest 109: 1405-1415. (Pubitemid 34596166)
31. Naik AA, Xie C, Zuscik MJ, Kingsley P, Schwarz EM, et al. (2009) Reduced COX-2 expression in aged mice is associated with impaired fracture healing. Journal of Bone and Mineral Research 24: 251-264.
32. Konishi H, Wu J, Cooke JP (2010) Chronic exposure to nicotine impairs cholinergic angiogenesis. Vasc Med 15: 47-54.
33. Arasapam G, Scherer M, Cool JC, Foster BK, Xian CJ (2006) Roles of COX-2 and iNOS in the bony repair of the injured growth plate cartilage. J Cell Biochem 99: 450-461. (Pubitemid 44435562)
34. Boyce BF, Xing L (2008) Functions of RANKL/RANK/OPG in bone modeling and remodeling. Arch Biochem Biophys 473: 139-146.
35. Alarcon T, Gonzalez-Montalvo JI, Gotor P, Madero R, Otero A (2011) Activities of daily living after hip fracture: profile and rate of recovery during 2 years of follow-up. Osteoporos Int 22: 1609-1613.
36. Brenneman SK, Barrett-Connor E, Sajjan S, Markson LE, Siris ES (2006) Impact of recent fracture on health-related quality of life in postmenopausal women. J Bone Miner Res 21: 809-816. (Pubitemid 43787987)
37. Ding R, McCarthy ML, Houseknecht E, Ziegfeld S, Knight VM, et al. (2006) The health-related quality of life of children with an extremity fracture: a one-year follow-up study. J Pediatr Orthop 26: 157-163. (Pubitemid 44357078)
38. Giannoudis PV, Harwood PJ, Kontakis G, Allami M, Macdonald D, et al. (2009) Long-term quality of life in trauma patients following the full spectrum of tibial injury (fasciotomy, closed fracture, grade IIIB/IIIC open fracture and amputation). Injury 40: 213-219.
39. Lonnroos E, Kautiainen H, Sund R, Karppi P, Hartikainen S, et al. (2009) Utilization of inpatient care before and after hip fracture: a population-based study. Osteoporos Int 20: 879-886.
40. Olerud P, Ahrengart L, Soderqvist A, Saving J, Tidermark J (2010) Quality of life and functional outcome after a 2-part proximal humeral fracture: a prospective cohort study on 50 patients treated with a locking plate. J Shoulder Elbow Surg 19: 814-822.
41. Silverman SL, Shen W, Minshall ME, Xie S, Moses KH (2007) Prevalence of depressive symptoms in postmenopausal women with low bone mineral density and/or prevalent vertebral fracture: results from the Multiple Outcomes of Raloxifene Evaluation (MORE) study. J Rheumatol 34: 140-144. (Pubitemid 46106574)
42. Schindeler A, McDonald MM, Bokko P, Little DG (2008) Bone remodeling during fracture repair: The cellular picture. Semin Cell Dev Biol 19: 459-466.
43. Zhang X, Naik A, Xie C, Reynolds D, Palmer J, et al. (2005) Periosteal stem cells are essential for bone revitalization and repair. JMusculoskeletNeuronalInteract 5: 360-362.
44. Zuscik MJ, O'Keefe RJ (2009) Skeletal Healing. In: Rosen CJ, editor. Primer on the Metabolic Bone Diseases and Disorders of Mineral Metabolism: American Society of Bone and Mineral Research. 61-65.
45. Street J, Bao M, deGuzman L, Bunting S, Peale FV Jr, et al. (2002) Vascular endothelial growth factor stimulates bone repair by promoting angiogenesis and bone turnover. ProcNatlAcadSciUSA 99: 9656-9661. (Pubitemid 34831103)
46. Moulton KS, Heller E, Konerding MA, Flynn E, Palinski W, et al. (1999) Angiogenesis inhibitors endostatin or TNP-470 reduce intimal neovascularization and plaque growth in apolipoprotein E-deficient mice. Circulation 99: 1726-1732. (Pubitemid 29162486)
47. Rui Z, Li X, Fan J, Ren Y, Yuan Y, et al. (2012) GIT1Y321 phosphorylation is required for ERK1/2- and PDGF-dependent VEGF secretion from osteoblasts to promote angiogenesis and bone healing. Int J Mol Med 30: 819-825.