Sintered anorganic bone graft increases autocrine expression of VEGF, MMP-2 and MMP-9 during repair of critical-size bone defects

Journal of Molecular Histology

Volumn 45, Issue 4, 2014, Pages 447-461

  Rocha, Caroline Andrade ^a   Cestari, Tania Mary ^a   Vidotti, Hugo Alberto ^a   De Assis, Gerson Francisco ^a   Garlet, Gustavo Pompermaier ^a   Taga, Rumio ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Anorganic bovine bone; Bone healing; Critical size bone defect; Metalloproteinase; Vascular endothelial growth factor

Indexed keywords

FLUNIXIN MEGLUMINE; GELATINASE A; GELATINASE B; VASCULOTROPIN; VASCULOTROPIN A;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; AUTOCRINE EFFECT; BLOOD CLOT; BONE DEFECT; BONE GRAFT; BONE REMODELING; BONE TREPHINE; CONNECTIVE TISSUE CELL; CONTROLLED STUDY; FIBROBLAST; FRACTURE HEALING; GENE EXPRESSION; HYPOTHESIS; IMMUNOHISTOCHEMISTRY; MALE; MORPHOMETRICS; NONHUMAN; OSSIFICATION; OSTEOBLAST; PRIORITY JOURNAL; RAT; SKULL DEFECT; ANIMAL; BONE; BONE TRANSPLANTATION; METABOLISM; PHYSIOLOGY; WISTAR RAT; WOUND HEALING;

BOVINAE; RATTUS;

ANIMALS; BONE AND BONES; BONE TRANSPLANTATION; MALE; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; RATS; RATS, WISTAR; VASCULAR ENDOTHELIAL GROWTH FACTOR A; WOUND HEALING;

EID: 84904336418     PISSN: 15672379     EISSN: 15672387     Source Type: Journal    
DOI: 10.1007/s10735-014-9565-4     Document Type: Article

References (55)

1. Accorsi-Mendonca T, Conz MB, Barros TC, de Sena LA, Soares Gde A, Granjeiro JM (2008) Physicochemical characterization of two deproteinized bovine xenografts. Braz Oral Res 22(1):5-10
2. Aherne W (1967) Methods of counting discrete tissue components in microscopical sections. J R Microsc Soc 87:493-508
3. Artzi Z, Nemcovsky CE, Tal H (2001) Efficacy of porous bovine bone mineral in various types of osseous deficiencies: clinical observations and literature review. Int J Periodontics Restor Dent 21(4):395-405 (Pubitemid 33672452)
4. Artzi Z, Kozlovsky A, Nemcovsky CE, Weinreb M (2005) The amount of newly formed bone in sinus grafting procedures depends on tissue depth as well as the type and residual amount of the grafted material. J Clin Periodontol 32(2):193-199. doi:10.1111/j.1600-051X.2005.00656.x (Pubitemid 40341855)
5. Bassil J, Senni K, Changotade S, Baroukh B, Kassis C, Naaman N, Godeau G (2011) Expression of MMP-2, 9 and 13 in newly formed bone after sinus augmentation using inorganic bovine bone in human. J Periodontal Res 46(6):756-762
6. Berendsen AD, Olsen BR (2014) How vascular endothelial growth factor-A (VEGF) regulates differentiation of mesenchymal stem cells. J Histochem Cytochem Off J Histochem Soc. doi:10.1369/0022155413516347
7. Boeck-Neto RJ, Artese L, Piattelli A, Shibli JA, Perrotti V, Piccirilli M, Marcantonio E Jr (2009) VEGF and MVD expression in sinus augmentation with autologous bone and several graft materials. Oral Dis 15(2):148-154
8. Bouletreau PJ, Warren SM, Spector JA, Peled ZM, Gerrets RP, Greenwald JA, Longaker MT (2002) Hypoxia and VEGF upregulate BMP-2 mRNA and protein expression in microvascular endothelial cells: implications for fracture healing. Plast Reconstr Surg 109(7):2384-2397 (Pubitemid 34556220)
9. Cawston TE, Young DA (2010) Proteinases involved in matrix turnover during cartilage and bone breakdown. Cell Tissue Res 339(1):221-235. doi:10.1007/s00441-009-0887-6
10. Cestari TM, Granjeiro JM, de Assis GF, Garlet GP, Taga R (2009) Bone repair and augmentation using block of sintered bovine-derived anorganic bone graft in cranial bone defect model. Clin Oral Implants Res 20(4):340-350. doi:10.1111/j.1600-0501. 2008.01659.x
11. Chen Y, Hanaoka M, Chen P, Droma Y, Voelkel NF, Kubo K (2009) Protective effect of beraprost sodium, a stable prostacyclin analog, in the development of cigarette smoke extract-induced emphysema. Am J Physiol Lung Cell Mol Physiol 296(4):L648- L656. doi:10.1152/ajplung.90270.2008
12. Chen D, Tian W, Li Y, Tang W, Zhang C (2012a) Osteoblast-specific transcription factor Osterix (Osx) and HIF-1alpha cooperatively regulate gene expression of vascular endothelial growth factor (VEGF). Biochem Biophys Res Commun 424(1):176-181
13. Chen D, Zhang X, Guo Y, Shi S, Mao X, Pan X, Cheng T (2012b) MMP-9 inhibition suppresses wear debris-induced inflammatory osteolysis through downregulation of RANK/RANKL in a murine osteolysis model. Int J Mol Med 30(6):1417-1423. doi:10.3892/ijmm 2012.1145
14. Cho JS, Kim HS, Um SH, Rhee SH (2013) Preparation of a novel anorganic bovine bone xenograft with enhanced bioactivity and osteoconductivity. J Biomed Mater Res B Appl Biomater 101(5):855-869. doi:10.1002/jbm.b.32890
15. Davis GE, Senger DR (2005) Endothelial extracellular matrix: biosynthesis, remodeling, and functions during vascular morphogenesis and neovessel stabilization. Circ Res 97(11):1093-1107
16. De Souza Nunes LS, De Oliveira RV, Holgado LA, Nary Filho H, Ribeiro DA, Matsumoto MA (2010) Immunoexpression of Cbfa-1/Runx2 and VEGF in sinus lift procedures using bone substitutes in rabbits. Clin Oral Implants Res 21(6):584-590
17. Degidi M, Artese L, Rubini C, Perrotti V, Iezzi G, Piattelli A (2006) Microvessel density and vascular endothelial growth factor expression in sinus augmentation using Bio-Oss. Oral Dis 12(5):469-475. doi:10.1111/j.1601-0825. 2006.01222.x (Pubitemid 44252539)
18. Ghajar CM, George SC, Putnam AJ (2008) Matrix metalloproteinase control of capillary morphogenesis. Crit Rev Eukaryot Gene Expr 18(3):251-278 (Pubitemid 351620287)
19. Heissig B, Hattori K, Dias S, Friedrich M, Ferris B, Hackett NR, Crystal RG, Besmer P, Lyden D, Moore MA, Werb Z, Rafii S (2002) Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand. Cell 109(5):625-637 (Pubitemid 34628725)
20. Heissig B, Hattori K, Friedrich M, Rafii S, Werb Z (2003) Angiogenesis: vascular remodeling of the extracellular matrix involves metalloproteinases. Curr Opin Hematol 10(2):136-141 (Pubitemid 36207969)
21. Heissig B, Ohki-Koizumi M, Tashiro Y, Gritli I, Sato-Kusubata K, Hattori K (2012) New functions of the fibrinolytic system in bone marrow cell-derived angiogenesis. Int J Hematol 95(2):131-137. doi:10.1007/s12185-012-1016-y
22. Iezzi G, Degidi M, Scarano A, Petrone G, Piattelli A (2007) Anorganic bone matrix retrieved 14 years after a sinus augmentation procedure: a histologic and histomorphometric evaluation. J Periodontol 78(10):2057-2061
23. Itagaki T, Honma T, Takahashi I, Echigo S, Sasano Y (2008) Quantitative analysis and localization of mRNA transcripts of type I collagen, osteocalcin, MMP 2, MMP 8, and MMP 13 during bone healing in a rat calvarial experimental defect model. Anat Rec 291(8):1038-1046. doi:10.1002/ar.20717
24. Joschek S, Nies B, Krotz R, Goferich A (2000) Chemical and physicochemical characterization of porous hydroxyapatite ceramics made of natural bone. Biomaterials 21(16):1645-1658. doi:10.1016/S0142961200000363 (Pubitemid 30347307)
25. Karsdal MA, Larsen L, Engsig MT, Lou H, Ferreras M, Lochter A, Delaisse JM, Foged NT (2002) Matrix metalloproteinase-dependent activation of latent transforming growth factor-beta controls the conversion of osteoblasts into osteocytes by blocking osteoblast apoptosis. J Biol Chem 277(46):44061-44067. doi:10.1074/jbc.M207205200 (Pubitemid 36157833)
26. Kong D, Li Y, Wang Z, Banerjee S, Sarkar FH (2007) Inhibition of angiogenesis and invasion by 3,3′ -diindolylmethane is mediated by the nuclear factor-κB downstream target genes MMP-9 and uPA that regulated bioavailability of vascular endothelial growth factor in prostate cancer. Cancer Res 67(7):3310-3319 (Pubitemid 46724870)
27. Maitre B, Boussat S, Jean D, Gouge M, Brochard L, Housset B, Adnot S, Delclaux C (2001) Vascular endothelial growth factor synthesis in the acute phase of experimental and clinical lung injury. Eur Respir J 18(1):100-106 (Pubitemid 32720382)
28. Matsumoto MA, Caviquioli G, Biguetti CC, de Andrade Holgado L, Saraiva PP, Renno AC, Kawakami RY (2012) A novel bioactive vitroceramic presents similar biological responses as autogenous bone grafts. J Mater Sci Mater Med 23(6):1447-1456. doi:10.1007/s10856-012-4612-8
29. Meury T, Verrier S, Alini M (2006) Human endothelial cells inhibit BMSC differentiation into mature osteoblasts in vitro by interfering with osterix expression. J Cell Biochem 98(4):992-1006 (Pubitemid 43993412)
30. Moreschi E, Biguetti CC, Comparim E, De Andrade HL, Ribeiro-Junior PD, Nary-Filho H, Matsumoto MA (2013) Cyclooxygenase- 2 inhibition does not impair block bone grafts healing in rabbit model. J Mol Histol 44(6):723-731. doi:10.1007/s10735-013-9519-2
31. Niida S, Kaku M, Amano H, Yoshida H, Kataoka H, Nishikawa S, Tanne K, Maeda N, Kodama H (1999) Vascular endothelial growth factor can substitute for macrophage colony-stimulating factor in the support of osteoclastic bone resorption. J Exp Med 190(2):293-298 (Pubitemid 29354921)
32. Ohtsubo S, Matsuda M, Takekawa M (2003) Angiogenesis after sintered bone implantation in rat parietal bone. Histol Histopathol 18(1):153-163 (Pubitemid 36040457)
33. Ortega N, Behonick D, Stickens D, Werb Z (2003) How proteases regulate bone morphogenesis. Ann N Y Acad Sci 995:109-116 (Pubitemid 36706618)
34. Ortega N, Behonick DJ, Werb Z (2004) Matrix remodeling during endochondral ossification. Trends Cell Biol 14(2):86-93 (Pubitemid 38186642)
35. Ozdemir MT, Kir MC (2011) Repair of long bone defects with demineralized bone matrix and autogenous bone composite. Indian J Orthop 45(3):226-230. doi:10.4103/0019-5413.80040IJOrtho-45-226
36. Page-McCaw A, Ewald AJ, Werb Z (2007) Matrix metalloproteinases and the regulation of tissue remodelling. Nat Rev Mol Cell Biol 8(3):221-233. doi:10.1038/nrm2125
37. Peng H, Usas A, Olshanski A, Ho AM, Gearhart B, Cooper GM, Huard J (2005) VEGF improves, whereas sFlt1 inhibits, BMP2-induced bone formation and bone healing through modulation of angiogenesis. J Bone Miner Res 20(11):2017-2027. doi:10.1359/JBMR.050708 (Pubitemid 41532787)
38. Portal-Nunez S, Lozano D, Esbrit P (2012) Role of angiogenesis on bone formation. Histol Histopathol 27(5):559-566
39. Schipani E, Maes C, Carmeliet G, Semenza GL (2009) Regulation of osteogenesis-angiogenesis coupling by HIFs and VEGF. J Bone Miner Res 24(8):1347-1353
40. Shum L, Rabie AB, Hagg U (2004) Vascular endothelial growth factor expression and bone formation in posterior glenoid fossa during stepwise mandibular advancement. Am J Orthod Dentofac Orthop 125(2):185-190 (Pubitemid 38199815)
41. Soker S, Machado M, Atala A (2000) Systems for therapeutic angiogenesis in tissue engineering. World J Urol 18(1):10-18
42. Stamenkovic I (2003) Extracellular matrix remodelling: the role of matrix metalloproteinases. J Pathol 200(4):448-464. doi:10.1002/path.1400
43. Sternlicht MD, Werb Z (2001) How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol 17:463-516. doi:10.1146/annurev.cellbio.17.1. 46317/1/463 (Pubitemid 33096184)
44. Sun X, Kang Y, Bao J, Zhang Y, Yang Y, Zhou X (2013) Modeling vascularized bone regeneration within a porous biodegradable CaP scaffold loaded with growth factors. Biomaterials 34(21):4971-4981. doi:10.1016/j.biomaterials. 2013.03.015
45. Traini T, Valentini P, Iezzi G, Piattelli A (2007) A histologic and histomorphometric evaluation of anorganic bovine bone retrieved 9 years after a sinus augmentation procedure. J Periodontol 78(5):955-961
46. Uchida S, Sakai A, Kudo H, Otomo H, Watanuki M, Tanaka M, Nagashima M, Nakamura T (2003) Vascular endothelial growth factor is expressed along with its receptors during the healing process of bone and bone marrow after drill-hole injury in rats. Bone 32(5):491-501. doi:10.1016/S8756-3282(03)00053-X (Pubitemid 39665708)
47. Weibel ER (1969) Stereological principles for morphometry in electron microscopic cytology. Int Rev Cytol 26:235-302
48. Wernike E, Montjovent MO, Liu Y, Wismeijer D, Hunziker EB, Siebenrock KA, Hofstetter W, Klenke FM (2010) VEGF incorporated into calcium phosphate ceramics promotes vascularisation and bone formation in vivo. Eur Cell Mater 19:30-40
49. Wu C, Zhou Y, Fan W, Han P, Chang J, Yuen J, Zhang M, Xiao Y (2012) Hypoxia-mimicking mesoporous bioactive glass scaffolds with controllable cobalt ion release for bone tissue engineering. Biomaterials 33(7):2076-2085
50. Wu C, Zhou Y, Xu M, Han P, Chen L, Chang J, Xiao Y (2013) Copper-containing mesoporous bioactive glass scaffolds with multifunctional properties of angiogenesis capacity, osteostimulation and antibacterial activity. Biomaterials 34(2):422-433
51. Yang YQ, Tan YY, Wong R, Wenden A, Zhang LK, Rabie AB (2012) The role of vascular endothelial growth factor in ossification. Int J Oral Sci 4:64-68
52. Zambuzzi WF, Oliveira RC, Pereira FL, Cestari TM, Taga R, Granjeiro JM (2006) Rat subcutaneous tissue response to macrogranular porous anorganic bovine bone graft. Braz Dent J 17(4):274-278
53. Zambuzzi WF, Fernandes GV, Iano FG, Fernandes MDS, Granjeiro JM, Oliveira RC (2012) Exploring anorganic bovine bone granules as osteoblast carriers for bone bioengineering: a study in rat critical-size calvarial defects. Braz Dent J 23(4):315-321
54. Zelzer E, Olsen BR (2005) Multiple roles of vascular endothelial growth factor (VEGF) in skeletal development, growth, and repair. Curr Top Dev Biol 65:169-187. doi:10.1016/S0070-2153(04)65006-X
55. Zelzer E, Mamluk R, Ferrara N, Johnson RS, Schipani E, Olsen BR (2004) VEGFA is necessary for chondrocyte survival during bone development. Development 131(9):2161-2171. doi:10.1242/dev.01053dev.01053 (Pubitemid 38702047)