The systemic angiogenic response during bone healing

Archives of Orthopaedic and Trauma Surgery

Volumn 129, Issue 7, 2009, Pages 989-997

  Weiss, Stefan ^a   Zimmermann, Gerald ^b   Pufe, Thomas ^c   Varoga, Deike ^d   Henle, Philipp ^a,e  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b BG UNFALLKLINIK LUDWIGSHAFEN   (Germany)

^c UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

^d UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^e UNIVERSITY OF BERN   (Switzerland)

Author keywords

Angiogenesis; Endochondral bone formation; Fracture healing; Nonunion

Indexed keywords

ANGIOGENIN; ANGIOPOIETIN 2; BASIC FIBROBLAST GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR AB; PLEIOTROPHIN; VASCULOTROPIN;

ADULT; AGED; ANGIOGENESIS; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENCHONDRAL OSSIFICATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FRACTURE HEALING; FRACTURE NONUNION; HUMAN; OSSIFICATION; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; REFERENCE VALUE;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; BONE AND BONES; CYTOKINES; FRACTURE HEALING; FRACTURES, UNUNITED; HUMANS; MIDDLE AGED; NEOVASCULARIZATION, PHYSIOLOGIC; PROSPECTIVE STUDIES; YOUNG ADULT;

EID: 67649652196     PISSN: 09368051     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00402-008-0777-5     Document Type: Article

References (50)

1. Andrew JG, Hoyland JA, Freemont AJ, Marsh DR (1995) Platelet-derived growth factor expression in normally healing human fractures. Bone 16(4):455-460
2. Badet J, Soncin F, N'Guyen T, Barritault D (1990) In vivo and in vitro studies of angiogenin - a potent angiogenic factor. Blood Coagul Fibrinolysis 1(6):721-724
3. Barnes GL, Kostenuik PJ, Gerstenfeld LC, Einhorn TA (1999) Growth factor regulation of fracture repair. J Bone Miner Res 14(11):1805-1815
4. Bolander ME (1992) Regulation of fracture repair by growth factors. Proc Soc Exp Biol Med 200(2):165-170
5. Bourque WT, Gross M, Hall BK (1993) Expression of four growth factors during fracture repair. Int J Dev Biol 37(4):573-579
6. Burgmann H, Hollenstein U, Maca T, Zedwitz-Liebenstein K, Thalhammer F, Koppensteiner R et al (1996) Increased serum laminin and angiogenin concentrations in patients with peripheral arterial occlusive disease. J Clin Pathol 49(6):508-510
7. Chua CC, Hamdy RC, Chua BH (2000) Mechanism of transforming growth factor-beta1-induced expression of vascular endothelial growth factor in murine osteoblastic MC3T3-E1 cells. Biochim Biophys Acta 1497(1):69-76
8. Einhorn TA, Simon G, Devlin VJ, Warman J, Sidhu SP, Vigorita VJ (1990) The osteogenic response to distant skeletal injury. J Bone Joint Surg Am 72(9):1374-1378
9. Gazit D, Karmish M, Holzman L, Bab I (1990) Regenerating marrow induces systemic increase in osteo- and chondrogenesis. Endocrinology 126(5):2607-2613
10. Gerber HP, Vu TH, Ryan AM, Kowalski J, Werb Z, Ferrara N (1999) VEGF couples hypertrophic cartilage remodeling, ossification and angiogenesis during endochondral bone formation. Nat Med 5(6):623-628
11. Gerstenfeld LC, Cho TJ, Kon T, Aizawa T, Tsay A, Fitch J et al (2003) Impaired fracture healing in the absence of TNF-alpha signaling: The role of TNF-alpha in endochondral cartilage resorption. J Bone Miner Res 18(9):1584-1592
12. Gong ZY, Zhou SX, Gu XM, Li DC, Sun ML (2003) Effect of recombinant human basic fibroblast growth factor on angiogenesis during mandible fracture healing in rabbits. Chin J Traumatol 6(4):242-244
13. Grotendorst GR (1984) Alteration of the chemotactic response of NIH/3T3 cells to PDGF by growth factors, transformation, and tumor promoters. Cell 36(2):279-285
14. Henle P, Zimmermann G, Weiss S (2005) Matrix metalloproteinases and failed fracture healing. Bone 37(6):791-798
15. Horner A, Bord S, Kelsall AW, Coleman N, Compston JE (2001) Tie2 ligands angiopoietin-1 and angiopoietin-2 are coexpressed with vascular endothelial cell growth factor in growing human bone. Bone 28(1):65-71
16. Horner A, Bord S, Kemp P, Grainger D, Compston JE (1996) Distribution of platelet-derived growth factor (PDGF) a chain mRNA, protein, and PDGF-alpha receptor in rapidly forming human bone. Bone 19(4):353-362
17. Hu G, Riordan JF, Vallee BL (1994) Angiogenin promotes invasiveness of cultured endothelial cells by stimulation of cell-associated proteolytic activities. Proc Natl Acad Sci USA 91(25):12096-12100
18. Imai S, Kaksonen M, Raulo E, Kinnunen T, Fages C, Meng X et al (1998) Osteoblast recruitment and bone formation enhanced by cell matrix-associated heparin-binding growth-associated molecule (HB-GAM). J Cell Biol 143(4):1113-1128
19. Ivaska KK et al (2007) Effect of fracture on bone turnover markers: A longitudinal study comparing marker levels before and after injury in 113 elderly women. J Bone Miner Res 22(8):1155-1164
20. Kadomatsu K, Muramatsu T (2004) Midkine and pleiotrophin in neural development and cancer. Cancer Lett 204(2):127-143
21. Kaspar D, Neidlinger-Wilke C, Holbein O, Claes L, Ignatius A (2003) Mitogens are increased in the systemic circulation during bone callus healing. J Orthop Res 21(2):320-325
22. Klaushofer K, Peterlik M (1994) Pathophysiology of fracture healing. Radiologe 34(12):709-714
23. Kurdy NM, Weiss JB, Bate A (1996) Endothelial stimulating angiogenic factor in early fracture healing. Injury 27(2):143-145
24. Laing AJ, Dillon JP, Condon ET, Street JT, Wang JH, McGuinness AJ, Redmond HP (2007) Mobilization of endothelial precursor cells: Systemic vascular response to musculoskeletal trauma. J Orthop Res 25(1):44-50
25. Lehmann W, Edgar CM, Wang K, Cho TJ, Barnes GL, Kakar S et al (2005) Tumor necrosis factor alpha (TNF-alpha) coordinately regulates the expression of specific matrix metalloproteinases (MMPS) and angiogenic factors during fracture healing. Bone 36(2):300-310
26. Lehmann W, Schinke T, Schilling AF, Catala-Lehnen P, Gebauer M, Pogoda P et al (2004) Absence of mouse pleiotrophin does not affect bone formation in vivo. Bone 35(6):1247-1255
27. Li G, Bunn JR, Mushipe MT, He Q, Chen X (2005) Effects of pleiotrophin (PTN) over-expression on mouse long bone development, fracture healing and bone repair. Calcif Tissue Int 76(4):299-306
28. Lieberman JR, Daluiski A, Einhorn TA (2002) The role of growth factors in the repair of bone. Biology and clinical applications. J Bone Joint Surg Am 84-A(6):1032-1044
29. Maes C, Carmeliet P, Moermans K, Stockmans I, Smets N, Collen D et al (2002) Impaired angiogenesis and endochondral bone formation in mice lacking the vascular endothelial growth factor isoforms VEGF164 and VEGF188. Mech Dev 111(1-2):61-73
30. Maglione D, Guerriero V, Viglietto G, li-Bovi P, Persico MG (1991) Isolation of a human placenta cDNA coding for a protein related to the vascular permeability factor. Proc Natl Acad Sci USA 88(20):9267-9271
31. Mueller M, Schilling T, Minne HW, Ziegler R (1991) A systemic acceleratory phenomenon (SAP) accompanies the regional acceleratory phenomenon (RAP) during healing of a bone defect in the rat. J Bone Miner Res 6(4):401-410
32. Nakajima F, Ogasawara A, Goto K, Moriya H, Ninomiya Y, Einhorn TA et al (2001) Spatial and temporal gene expression in chondrogenesis during fracture healing and the effects of basic fibroblast growth factor. J Orthop Res 19(5):935-944
33. Narayanan AS, Engel LD, Page RC (1983) The effect of chronic inflammation on the composition of collagen types in human connective tissue. Coll Relat Res 3(4):323-334
34. Nash TJ, Howlett CR, Martin C, Steele J, Johnson KA, Hicklin DJ (1994) Effect of platelet-derived growth factor on tibial osteotomies in rabbits. Bone 15(2):203-208
35. Petersen W, Wildemann B, Pufe T, Raschke M, Schmidmaier G (2004) The angiogenic peptide pleiotrophin (PTN/HB-GAM) is expressed in fracture healing: An immunohistochemical study in rats. Arch Orthop Trauma Surg 124(9):603-607
36. Probst A, Spiegel HU (1997) Cellular mechanisms of bone repair. J Invest Surg 10(3):77-86
37. Radomsky ML, Aufdemorte TB, Swain LD, Fox WC, Spiro RC, Poser JW (1999) Novel formulation of fibroblast growth factor-2 in a hyaluronan gel accelerates fracture healing in nonhuman primates. J Orthop Res 17(4):607-614
38. Saadeh PB, Mehrara BJ, Steinbrech DS, Dudziak ME, Greenwald JA, Luchs JS et al (1999) Transforming growth factor-beta1 modulates the expression of vascular endothelial growth factor by osteoblasts. Am J Physiol 277(4 Pt 1):C628-C637
39. Saadeh PB, Mehrara BJ, Steinbrech DS, Spector JA, Greenwald JA, Chin GS et al (2000) Mechanisms of fibroblast growth factor-2 modulation of vascular endothelial growth factor expression by osteoblastic cells. Endocrinology 141(6):2075-2083
40. Shirley D, Marsh D, Jordan G, McQuaid S, Li G (2005) Systemic recruitment of osteoblastic cells in fracture healing. J Orthop Res 23(5):1013-1021
41. Street J, Winter D, Wang JH, Wakai A, McGuinness A, Redmond HP (2000) Is human fracture hematoma inherently angiogenic? Clin Orthop Relat Res 378:224-237
42. Tare RS, Oreffo RO, Clarke NM, Roach HI (2002) Pleiotrophin/ osteoblast-stimulating factor 1: Dissecting its diverse functions in bone formation. J Bone Miner Res 17(11):2009-2020
43. Tatsuyama K, Maezawa Y, Baba H, Imamura Y, Fukuda M (2000) Expression of various growth factors for cell proliferation and cytodifferentiation during fracture repair of bone. Eur J Histochem 44(3):269-278
44. Timlin M, Toomey D, Condron C, Power C, Street J, Murray P et al (2005) Fracture hematoma is a potent proinflammatory mediator of neutrophil function. J Trauma 58(6):1223-1229
45. Tzeng DY, Deuel TF, Huang JS, Senior RM, Boxer LA, Baehner RL (1984) Platelet-derived growth factor promotes polymorphonuclear leukocyte activation. Blood 64(5):1123-1128
46. Vortkamp A, Pathi S, Peretti GM, Caruso EM, Zaleske DJ, Tabin CJ (1998) Recapitulation of signals regulating embryonic bone formation during postnatal growth and in fracture repair. Mech Dev 71(1-2):65-76
47. Weiss S, Baumgart R, Jochum M, Strasburger CJ, Bidlingmaier M (2002) Systemic regulation of distraction osteogenesis: A cascade of biochemical factors. J Bone Miner Res 17(7):1280-1289
48. Weiss S, Zimmermann G, Baumgart R, Kasten P, Bidlingmaier M, Henle P (2005) Systemic regulation of angiogenesis and matrix degradation in bone regeneration-distraction osteogenesis compared to rigid fracture healing. Bone 37(6):781-790
49. Yeh HS, Chen H, Manyak SJ, Swift RA, Campbell RA, Wang C et al (2006) Serum pleiotrophin levels are elevated in multiple myeloma patients and correlate with disease status. Br J Haematol 133(5):526-529
50. Zimmermann G, Henle P, Kuesswetter M, Moghaddam A, Wentzensen A, Weiss S (2005) TGF-beta1 as a marker of delayed fracture healing. Bone 36(5):779-785