Effect of Adeno-Associated Virus-Transfected Mesenchymal Stem Cells Containing Agents on Bone Formation in Extended Inter-Premaxillary Suture in Rats
,
Abstract
Introduction: The aim of this study was to investigate the histomorphometric effects of bone marrow-derived mesenchymal stem cells (MSCs) transfected with Adeno Associated Virus (AAV) and containing bone morphogenic protein 7 (Bmp7) or osteoprotegerin (OPG) on bone formation after injection into inter-premaxillary suture in rats with Bmp7 or OPG alone.Materials and Methods: In 4 groups (each group n:9), different chemical solutions, namely AAV-Bmp7, AAV-OPG and AAV-Bmp7-OPG and AAV-EGF (control group) were injected into the interpremaxillary suture of rats. Bone volumes (BV), soft tissue volume (STV) and total bone volumes (TBV) of 10μm serial selection with hemotoxylin and eosin staining were calculated according to the Cavalieri principle. Each point in the region of interest was 1000μm3.Results: The BV for AAV-Bmp7, AAV-OPG, AAV-Bmp7-OPG and AAV-EGF were 46.98±1.50 mm3, 49.40±4.72mm3, 42.58±2.89mm3 and 38.82±0.76mm3, respectively. The STV was 11.53±0.99, 13.31±1.88, 8.00±4.43 and 9.57±1.90mm3 for Bmp7, OPG, AAV-Bmp7-OPG and AAV-EGF, respectively. TBV was 58.34±2.28mm3, 63.83±5.17mm3, 53.74±3.34mm3 and 48.13±1.54mm3 for AAV-Bmp7, AAV-OPG, AAV-Bmp7-OPG and AAV-EGF, respectively. The comparison between BV, STV, TBV for AAV-OPG showed a statistically significant difference (p=0.001) compared to AAV-Bmp7 or AAV-Bmp7-OPG and AAV-EGF.Conclusion: During tooth movement and bone remodeling, the ratio of soft and bone tissues is maintained by OPG. Although Bmp7 is not as effective as OPG in bone remodeling, both can reduce the retention time and the risk of recurrence. Keywords: Histomorphometry; Bmp 7; OPG; Maxillary expansion; Orthodontics; Rats.
1. Haas AJ. Palatal expansion: just the beginning of dentofacial orthopedics. Am J Orthod 1970; 57(3), 219-55.
2. Adkins MD, Nanda RS, Currier GF. Arch perimeter changes on rapid palatal expansion. Am J Orthod Dentofacial Orthop. 1990; 97(3), 194-9.
3. Sawada M, Shimizu N. Stimulation of bone formation in the expanding mid-palatal suture by transforming growth factor beta 1 in the rat. Eur J Orthod 1996;18:169-79.
4. Muchitsch A P , Winsauer H, Wendl B, Pichelmayer M, Kuljuh E, Szalay A, Muchitsch M. Remodelling of the palatal dome following rapid maxillary expansion (RME): laser scan-quantifications during a low growth period. Orthod Craniofac Res 2012;15(1):30-8.
5. Timms DJ. Long term follow-up of cases treated by rapid maxillary expansion. Trans Eur Orthod Soc 1976;52:211–5.
6. Nicholson PT, Plint DA. A long term study of rapid maxillary expansion and bone grafting in cleft lip and palate patients. Eur J Orthod 1989;11:186-92.
7. Proffit WR, Fields HW. Maxillary deficiency. In Proffit WR, editor. Contemporary orthodontics. 2nd ed. St Louis: Mosby- Year Book,1992:237-40.
8. Gunyuz M, Germec Cakan D, Tozlu M. Periodontal, dentoalveolar and skeletal effects of tooth borne and tooth-bone borne expansion appliances. Am J Orthod 2015; 148:97-109.
9. Reitan F, Rygh P. Biomechanical principles and reactions. In: Graber TM, Vandarsdall RL, editors. Orthodontics: current principles and techniques. 2nd ed. St Louis: Mosby-Year Book; 1994:96-192.
10. Handelman CS. The anterior alveolus: its importance in limiting orthodontic treatment and its influence on the occurrence of iatrogenic sequelae. Angle Orthod 1996;66:95-109.
11. Fuhrmann R. Three-dimensional interpretation of periodontal lesions and remodeling during orthodontic treatment. Part III. J Orofac Orthop 1996;57:224-37.
12. Saito S, Shimizu N. Stimulatory effects of low-power laser irradiation on bone regeneration in midpalatal suture during expansion in the rat. Am J Orthod 1997; 111:525–32.
13. Lee K, Sugiyama H, Imoto S, Tanne K. Effects of bisphosphonate on the remodeling of rat sagittal suture after rapid expansion. Angle Orthod 2001;71: 265-73.
14. Ozturk F, Babacan H, Inan S, Gumus C. Effects of bisphosphonates on sutural bone formation and relapse: A histologic and immunohistochemical study. Am J Orthod 2011;140: 31-4.
15. Uysal T, Amasyali M, Enhos S, Karslioglu Y, Yilmaz F, Gunhan O. Effect of vitamin C on bone formation in the expanded inter-premaxillary suture. Early bone changes. J Orofac Orthop 2011;72: 290-300.
16. Uysal T, Amasyali M, Enhos S, Sonmez MF, Sagdic D. Effect of ED-71, a new active vitamin D analog, on bone formation in an orthopedically expanded suture in rats. A histomorphometric study. Eur J Dent 2009;3: 165-72.
17. Uysal T, Amasyali M, Olmez H, Karslioglu Y, Gunhan O. Stimulation of bone formation in the expanding inter-premaxillary suture by vitamin E, in rat. Korean J Orthod 2009;39: 5.
18. Uysal T, Gorgulu S, Yagci A, Karslioglu Y, Gunhan O, Sagdic D. Effect of resveratrol on bone formation in the expanded inter-premaxillary suture: early bone changes. Orthod Craniofac Res 2011;14: 80-7.
19. Kara MI, Erciyas K, Altan AB, Ozkut M, Ay S, Inan S. Thymoquinone accelerates new bone formation in the rapid maxillary expansion procedure. J Arch Oral Bio 2012;57: 357-63.
20. Ekizer A, Uysal T, Guray E, Yuksel Y. Light-emitting diode photobiomodulation: Effect on bone formation in orthopedically expanded suture in rats-early bone changes. Lasers Med Sci 2013;28(5): 1263-70.
21. Uysal T, Amasyali M, Olmez H, Enhos S, Karslioglu Y, Gunhan O. Effect of periosteal stimulation therapy on bone formation in orthopedically expanded suture in rats. Orthod Craniofac Res 2010;13: 89-95.
22. Altan AB, Bicakci AA, Avunduk MC, Esen H. The effect of dosage on the efficiency of LLLT in new bone formation at the expanded suture in rats. Lasers Med Sci 2015;30(1):255-62.
23. Hofbauer LC, Khosla S, Dunstan CR, Lacey DL, Boyle WJ, Riggs BL. The roles of osteoprotegerin ligand in the paracrine regulation of bone resorbtion. J Bone Miner Res 2000; 15:2-12.
24. Simonet WS, Lacey DL, Dunstan CR, Kelley M, Chang MS, Luthy R. Osteoprotegerin: anovel secreted protein involved in the regulation of bone density. Cell 1997;89:309-319.
25. Udagawa N, Takahashi N, Jimi E, Matsuzaki K, Tsurukai T, Itoh K. Osteoblast/stromal cells stimulate osteoclast activation through expression of osteoclast differentiation factor/RANKL but not macrophage colony-stimulating factor. Bone 1999;25:517-523.
26. Yasuda H, Shima N, Nakagawa N, Yamaguchi K, Kinosaki M, Goto M. A novel molecular mechanism modulating osteoclast differentiation and function. Bone. 1999; 25:109-13.
1. 27 Lacey DL, Timms E, Tan HL, Kelly MJ, Dunstan CR, Burgess T, Elliott R, Colombero A; Elliott G, Scully S, Hsu H, Sıllivan J, Hawkins N, Dany E, Capparelli C, Eli A, Qian YX, Kaufman S, Sarosi I, Shalhoub V, Senaldi G, Guo J, Delaney J, Boyle WWJ. Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell. 1998; 93:3597-602.
28. Matsuzaki K, Udawaga N, Takahashi N, Yamaguchi K, Yasuda, Shima N, Morinaga T, Toyama Y, Yabe Y, Higashio K, Suda T. Osteoclast differentiaiton factor (ODF) induces osteoclast-like cell formation in human peripheral blood mononuclear cell cultures. Biochem Biophys Res Common 1998;246:199-204.
29. Krajewska-Wlodarczyk M, Stompor T. Osteoporosis and vascular calcification in rheumatoid arthritis-the role of osteoprotegerin and sclerostin. Pol Merkur Lekarski. 2017;21:41-47.
30. Jayash SN, Hashim NM, Misran M, Baharuddin NA. Formulation and in vitro and in vivo evaluation of a new osteoprotegerin-chitosan gel for bone tissue regeneration. J Biomed Mater Res A. 2017;105:398-407.
31. Pountos I, Jones E, Tzioupis C, McGonagle D, Giannoudis PV. Growing bone and cartilage. The role of mesenchymal stem cells. J Bone Joint Surg Br. 2006;88:421-426.
32. Bilic R, Simic P, Jelic M, Stern-Padovan R, Dodig D, Pompe van Meerdervoort H, Martinovic S, IvankovicD, Pecina M, Vukicevic S. Osteogenic protein-1 (BMP-7) accelerates healing of scaphoid non-union with proximal pole sclerosis. Int Orthop. 2006 Apr; 30(2): 128–134.
33. Diwan AD, Leong A, Appleyard R, Bhargav D, Fang ZM, Wei A. Bone morphogenetic protein-7 accelerates fracture healing in osteoporotic rats. Indian J Orthop. 2013; 47(6): 540–46.
34. Mantripragada VP, Jayasuriya AC. Injectable chitosan microparticles incorporating bone morphogenetic protein-7 for bone tissue regeneration. J Biomed Mater Res A. 2014;102:4276-89.
35. Fortier LA. Stem cells: classifications, controversies and clinical applications. Vet Surg. 2005;34(5):415-23
36. Campagnoli C, Roberts IA, Kumar S, Bennett PR, Bellantuono I, Fisk NM. Identification of mesenchymal stem/progenitor cells in human first-trimester fetal blood, liver, and bone marrow. Blood. 200;98(8):2396–2402.
37. Zuk PA, Zhu M, Ashjian P, De Ugarte DA, Huang JI, Mizuno H, Alfonso ZC, Fraser JK, Benhaim P, Hedrick MH. Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 2002;13(12):4279–95.
38. Morsczeck C, Gotz W, Schierholz J, Zeilhofer F, Kühn U, Möhl C, Sippel C, Hoffmann KH. Isolation of precursor cells (PCs) from human dental follicles of wisdom teeth. Matrix Biol 2005;24(2):155–65.
39. Lindroos B, Maenpaa K, Ylikomi T, Oja H, Suuronen R, Miettinen S. Characterisation of human dental stem cells and buccal mucosa fibroblasts. Biochem Biophys Res Commun 2008;368(2):329–35.
40. Yalvac ME, Ramazanoglu M, Gumru OZ, Sahin F, Palotas A, Rizvanov AA. Comparison and optimisation of transfection of human dental follicle cells, a novel source of stem cells, with different chemical methods and electro-poration. Neurochem Res 2009; 34: 1272–7.
41. Barry FP, Murphy JM. Mesencymal stem cells: clinical applications and biological chacterization. The International Journal of Biochemistry and Cell Biology. 2004; 36(4):568-584.
42. Gehl, J. Electroporation: theory and methods, perspectives for drug delivery, gene therapy and research. Acta Physiol Scand. 2003;177, 437-47.
43. Grieger, J.C. Samulski, R.J., Adeno-associated virus as a gene therapy vector: vector development, production and clinical applications. Adv Biochem Eng Biotechnol. 2005; 99, 119-45.
44. Kunze, M., Huber, A., Krajewski, A., Lowden, E., Schuhmann, N., Buening, H., Hallek, M., Noack, M., Perabo, L., 2009. Efficient gene transfer to periodontal ligament cells and human gingival fibroblasts by adeno-associated virus vectors. J Dent. 37, 502-8.
45. Grieger, J.C., Choi, V.W., Samulski, R.J., 2006. Production and characterization of adeno-associated viral vectors. Nat Protoc. 1, 1412-28.
46. Yalcin-Ulker GM, Cumbul A, Duygu-Capar G, Uslu U, Sencift K. Preventive Effect of Phosphodiesterase Inhibitor Pentoxifylline against Medication-Related Osteonecrosis of the Jaw: An Animal Study. J Oral Maxillofac Sur 2017;75:2354-2368.
47. Cruz-Orive LM, Weibel ER. Recent stereological methods for cell biology: a brief survey. Am J Physiol 1990;258:148-56.
48. Gulec A, Cakirer Bakkalbasi B, Cumbul A, Uslu U, Alev B, Yarat A. Effects of local platelet rich plasma injection on the rate of orthodontic tooth movement in a rat model: A histomorphometric study. Am J Orthod 2017;151 (1), 92-103.
49. Storey E. Tissue response to the movement of bones. Am J Orthod 1973;64: 229-47.
50. Guerrero JA, Silva RS, de Abreu Lima IL, Rodrigues BCD, Barrioni BR, Amaral FA, Macari S. Maxillary suture expansion: a mouse model to explore the molecular effects of mechanically-induced bone remodeling. J Biomech 2020; 108:109880.
51 Martins MT, Vitorino VDM, Rodrigues LV, Lages EMB, Pretti H, Vale MP, Pordeus IA. Impact of Wearing Palatal Expanders on the Quality of Life of Children Aged 8 to 10 Years. Pesquisa Brasileira em Odontopediatria e Clínica Integrada 2021; 21.
52 52. Rungcharassaeng K, Caruso JM, Kan JY, Kim J, Taylor G. Factors affecting buccal bone changes of maxillary posterior teeth after rapid maxillary expansion. Am J Orthod 2007;132(4):428.e1-8.
53. Baysal A, Uysal T, Veli T, Ozer T, Karadede I, Hekimoglu S. Evaluation of alveolar bone loss following rapid maxillary expansion using cone-beam computed tomography. Korean J Orthod. 2013;43(2): 83–95.
54. Sun J, Eleniste PP, Utreja A, Turkkahraman H, Liu SSY, Bruzzaniti A. Pyk2 deficiency enhances bone mass during midpalatal suture expansion. Orthod Craniofac Res. 2020; 23(4), 501-8.
55. Baud’huin M, Duplomb L, Teletchea S, Lamoureux F, Ruiz-Velasco C, Maillasson M, Heymann D. Osteoprotegerin: multiple partners for multiple functions. Cytokine Growth Factor Rev. 2013; 24(5), 401-9.
56. Chen F, Bi D, Cheng C, Ma S, Liu Y, Cheng K. Bone morphogenetic protein 7 enhances the osteogenic differentiation of human dermal-derived CD105+ fibroblast cells through the Smad and MAPK pathways. Int J Mol Med. 2019;43(1):37-46.
57. Werle S, AbuNahleh K, Boehm H. Bone morphogenetic protein 7 and autologous bone graft in revision surgery for non-union after lumbar interbody fusion. Arch Orthop Trauma Surg. 2016;136(8):1041-9.
58. Sadikoglu TB, Nalbantgil D, Ulkur F, Ulas N. Effect of hyaluronic acid on bone formation in the expanded interpremaxillary suture in rats. Orthod Craniofac Res. 2016;19(3), 154-61.
2. Adkins MD, Nanda RS, Currier GF. Arch perimeter changes on rapid palatal expansion. Am J Orthod Dentofacial Orthop. 1990; 97(3), 194-9.
3. Sawada M, Shimizu N. Stimulation of bone formation in the expanding mid-palatal suture by transforming growth factor beta 1 in the rat. Eur J Orthod 1996;18:169-79.
4. Muchitsch A P , Winsauer H, Wendl B, Pichelmayer M, Kuljuh E, Szalay A, Muchitsch M. Remodelling of the palatal dome following rapid maxillary expansion (RME): laser scan-quantifications during a low growth period. Orthod Craniofac Res 2012;15(1):30-8.
5. Timms DJ. Long term follow-up of cases treated by rapid maxillary expansion. Trans Eur Orthod Soc 1976;52:211–5.
6. Nicholson PT, Plint DA. A long term study of rapid maxillary expansion and bone grafting in cleft lip and palate patients. Eur J Orthod 1989;11:186-92.
7. Proffit WR, Fields HW. Maxillary deficiency. In Proffit WR, editor. Contemporary orthodontics. 2nd ed. St Louis: Mosby- Year Book,1992:237-40.
8. Gunyuz M, Germec Cakan D, Tozlu M. Periodontal, dentoalveolar and skeletal effects of tooth borne and tooth-bone borne expansion appliances. Am J Orthod 2015; 148:97-109.
9. Reitan F, Rygh P. Biomechanical principles and reactions. In: Graber TM, Vandarsdall RL, editors. Orthodontics: current principles and techniques. 2nd ed. St Louis: Mosby-Year Book; 1994:96-192.
10. Handelman CS. The anterior alveolus: its importance in limiting orthodontic treatment and its influence on the occurrence of iatrogenic sequelae. Angle Orthod 1996;66:95-109.
11. Fuhrmann R. Three-dimensional interpretation of periodontal lesions and remodeling during orthodontic treatment. Part III. J Orofac Orthop 1996;57:224-37.
12. Saito S, Shimizu N. Stimulatory effects of low-power laser irradiation on bone regeneration in midpalatal suture during expansion in the rat. Am J Orthod 1997; 111:525–32.
13. Lee K, Sugiyama H, Imoto S, Tanne K. Effects of bisphosphonate on the remodeling of rat sagittal suture after rapid expansion. Angle Orthod 2001;71: 265-73.
14. Ozturk F, Babacan H, Inan S, Gumus C. Effects of bisphosphonates on sutural bone formation and relapse: A histologic and immunohistochemical study. Am J Orthod 2011;140: 31-4.
15. Uysal T, Amasyali M, Enhos S, Karslioglu Y, Yilmaz F, Gunhan O. Effect of vitamin C on bone formation in the expanded inter-premaxillary suture. Early bone changes. J Orofac Orthop 2011;72: 290-300.
16. Uysal T, Amasyali M, Enhos S, Sonmez MF, Sagdic D. Effect of ED-71, a new active vitamin D analog, on bone formation in an orthopedically expanded suture in rats. A histomorphometric study. Eur J Dent 2009;3: 165-72.
17. Uysal T, Amasyali M, Olmez H, Karslioglu Y, Gunhan O. Stimulation of bone formation in the expanding inter-premaxillary suture by vitamin E, in rat. Korean J Orthod 2009;39: 5.
18. Uysal T, Gorgulu S, Yagci A, Karslioglu Y, Gunhan O, Sagdic D. Effect of resveratrol on bone formation in the expanded inter-premaxillary suture: early bone changes. Orthod Craniofac Res 2011;14: 80-7.
19. Kara MI, Erciyas K, Altan AB, Ozkut M, Ay S, Inan S. Thymoquinone accelerates new bone formation in the rapid maxillary expansion procedure. J Arch Oral Bio 2012;57: 357-63.
20. Ekizer A, Uysal T, Guray E, Yuksel Y. Light-emitting diode photobiomodulation: Effect on bone formation in orthopedically expanded suture in rats-early bone changes. Lasers Med Sci 2013;28(5): 1263-70.
21. Uysal T, Amasyali M, Olmez H, Enhos S, Karslioglu Y, Gunhan O. Effect of periosteal stimulation therapy on bone formation in orthopedically expanded suture in rats. Orthod Craniofac Res 2010;13: 89-95.
22. Altan AB, Bicakci AA, Avunduk MC, Esen H. The effect of dosage on the efficiency of LLLT in new bone formation at the expanded suture in rats. Lasers Med Sci 2015;30(1):255-62.
23. Hofbauer LC, Khosla S, Dunstan CR, Lacey DL, Boyle WJ, Riggs BL. The roles of osteoprotegerin ligand in the paracrine regulation of bone resorbtion. J Bone Miner Res 2000; 15:2-12.
24. Simonet WS, Lacey DL, Dunstan CR, Kelley M, Chang MS, Luthy R. Osteoprotegerin: anovel secreted protein involved in the regulation of bone density. Cell 1997;89:309-319.
25. Udagawa N, Takahashi N, Jimi E, Matsuzaki K, Tsurukai T, Itoh K. Osteoblast/stromal cells stimulate osteoclast activation through expression of osteoclast differentiation factor/RANKL but not macrophage colony-stimulating factor. Bone 1999;25:517-523.
26. Yasuda H, Shima N, Nakagawa N, Yamaguchi K, Kinosaki M, Goto M. A novel molecular mechanism modulating osteoclast differentiation and function. Bone. 1999; 25:109-13.
1. 27 Lacey DL, Timms E, Tan HL, Kelly MJ, Dunstan CR, Burgess T, Elliott R, Colombero A; Elliott G, Scully S, Hsu H, Sıllivan J, Hawkins N, Dany E, Capparelli C, Eli A, Qian YX, Kaufman S, Sarosi I, Shalhoub V, Senaldi G, Guo J, Delaney J, Boyle WWJ. Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell. 1998; 93:3597-602.
28. Matsuzaki K, Udawaga N, Takahashi N, Yamaguchi K, Yasuda, Shima N, Morinaga T, Toyama Y, Yabe Y, Higashio K, Suda T. Osteoclast differentiaiton factor (ODF) induces osteoclast-like cell formation in human peripheral blood mononuclear cell cultures. Biochem Biophys Res Common 1998;246:199-204.
29. Krajewska-Wlodarczyk M, Stompor T. Osteoporosis and vascular calcification in rheumatoid arthritis-the role of osteoprotegerin and sclerostin. Pol Merkur Lekarski. 2017;21:41-47.
30. Jayash SN, Hashim NM, Misran M, Baharuddin NA. Formulation and in vitro and in vivo evaluation of a new osteoprotegerin-chitosan gel for bone tissue regeneration. J Biomed Mater Res A. 2017;105:398-407.
31. Pountos I, Jones E, Tzioupis C, McGonagle D, Giannoudis PV. Growing bone and cartilage. The role of mesenchymal stem cells. J Bone Joint Surg Br. 2006;88:421-426.
32. Bilic R, Simic P, Jelic M, Stern-Padovan R, Dodig D, Pompe van Meerdervoort H, Martinovic S, IvankovicD, Pecina M, Vukicevic S. Osteogenic protein-1 (BMP-7) accelerates healing of scaphoid non-union with proximal pole sclerosis. Int Orthop. 2006 Apr; 30(2): 128–134.
33. Diwan AD, Leong A, Appleyard R, Bhargav D, Fang ZM, Wei A. Bone morphogenetic protein-7 accelerates fracture healing in osteoporotic rats. Indian J Orthop. 2013; 47(6): 540–46.
34. Mantripragada VP, Jayasuriya AC. Injectable chitosan microparticles incorporating bone morphogenetic protein-7 for bone tissue regeneration. J Biomed Mater Res A. 2014;102:4276-89.
35. Fortier LA. Stem cells: classifications, controversies and clinical applications. Vet Surg. 2005;34(5):415-23
36. Campagnoli C, Roberts IA, Kumar S, Bennett PR, Bellantuono I, Fisk NM. Identification of mesenchymal stem/progenitor cells in human first-trimester fetal blood, liver, and bone marrow. Blood. 200;98(8):2396–2402.
37. Zuk PA, Zhu M, Ashjian P, De Ugarte DA, Huang JI, Mizuno H, Alfonso ZC, Fraser JK, Benhaim P, Hedrick MH. Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 2002;13(12):4279–95.
38. Morsczeck C, Gotz W, Schierholz J, Zeilhofer F, Kühn U, Möhl C, Sippel C, Hoffmann KH. Isolation of precursor cells (PCs) from human dental follicles of wisdom teeth. Matrix Biol 2005;24(2):155–65.
39. Lindroos B, Maenpaa K, Ylikomi T, Oja H, Suuronen R, Miettinen S. Characterisation of human dental stem cells and buccal mucosa fibroblasts. Biochem Biophys Res Commun 2008;368(2):329–35.
40. Yalvac ME, Ramazanoglu M, Gumru OZ, Sahin F, Palotas A, Rizvanov AA. Comparison and optimisation of transfection of human dental follicle cells, a novel source of stem cells, with different chemical methods and electro-poration. Neurochem Res 2009; 34: 1272–7.
41. Barry FP, Murphy JM. Mesencymal stem cells: clinical applications and biological chacterization. The International Journal of Biochemistry and Cell Biology. 2004; 36(4):568-584.
42. Gehl, J. Electroporation: theory and methods, perspectives for drug delivery, gene therapy and research. Acta Physiol Scand. 2003;177, 437-47.
43. Grieger, J.C. Samulski, R.J., Adeno-associated virus as a gene therapy vector: vector development, production and clinical applications. Adv Biochem Eng Biotechnol. 2005; 99, 119-45.
44. Kunze, M., Huber, A., Krajewski, A., Lowden, E., Schuhmann, N., Buening, H., Hallek, M., Noack, M., Perabo, L., 2009. Efficient gene transfer to periodontal ligament cells and human gingival fibroblasts by adeno-associated virus vectors. J Dent. 37, 502-8.
45. Grieger, J.C., Choi, V.W., Samulski, R.J., 2006. Production and characterization of adeno-associated viral vectors. Nat Protoc. 1, 1412-28.
46. Yalcin-Ulker GM, Cumbul A, Duygu-Capar G, Uslu U, Sencift K. Preventive Effect of Phosphodiesterase Inhibitor Pentoxifylline against Medication-Related Osteonecrosis of the Jaw: An Animal Study. J Oral Maxillofac Sur 2017;75:2354-2368.
47. Cruz-Orive LM, Weibel ER. Recent stereological methods for cell biology: a brief survey. Am J Physiol 1990;258:148-56.
48. Gulec A, Cakirer Bakkalbasi B, Cumbul A, Uslu U, Alev B, Yarat A. Effects of local platelet rich plasma injection on the rate of orthodontic tooth movement in a rat model: A histomorphometric study. Am J Orthod 2017;151 (1), 92-103.
49. Storey E. Tissue response to the movement of bones. Am J Orthod 1973;64: 229-47.
50. Guerrero JA, Silva RS, de Abreu Lima IL, Rodrigues BCD, Barrioni BR, Amaral FA, Macari S. Maxillary suture expansion: a mouse model to explore the molecular effects of mechanically-induced bone remodeling. J Biomech 2020; 108:109880.
51 Martins MT, Vitorino VDM, Rodrigues LV, Lages EMB, Pretti H, Vale MP, Pordeus IA. Impact of Wearing Palatal Expanders on the Quality of Life of Children Aged 8 to 10 Years. Pesquisa Brasileira em Odontopediatria e Clínica Integrada 2021; 21.
52 52. Rungcharassaeng K, Caruso JM, Kan JY, Kim J, Taylor G. Factors affecting buccal bone changes of maxillary posterior teeth after rapid maxillary expansion. Am J Orthod 2007;132(4):428.e1-8.
53. Baysal A, Uysal T, Veli T, Ozer T, Karadede I, Hekimoglu S. Evaluation of alveolar bone loss following rapid maxillary expansion using cone-beam computed tomography. Korean J Orthod. 2013;43(2): 83–95.
54. Sun J, Eleniste PP, Utreja A, Turkkahraman H, Liu SSY, Bruzzaniti A. Pyk2 deficiency enhances bone mass during midpalatal suture expansion. Orthod Craniofac Res. 2020; 23(4), 501-8.
55. Baud’huin M, Duplomb L, Teletchea S, Lamoureux F, Ruiz-Velasco C, Maillasson M, Heymann D. Osteoprotegerin: multiple partners for multiple functions. Cytokine Growth Factor Rev. 2013; 24(5), 401-9.
56. Chen F, Bi D, Cheng C, Ma S, Liu Y, Cheng K. Bone morphogenetic protein 7 enhances the osteogenic differentiation of human dermal-derived CD105+ fibroblast cells through the Smad and MAPK pathways. Int J Mol Med. 2019;43(1):37-46.
57. Werle S, AbuNahleh K, Boehm H. Bone morphogenetic protein 7 and autologous bone graft in revision surgery for non-union after lumbar interbody fusion. Arch Orthop Trauma Surg. 2016;136(8):1041-9.
58. Sadikoglu TB, Nalbantgil D, Ulkur F, Ulas N. Effect of hyaluronic acid on bone formation in the expanded interpremaxillary suture in rats. Orthod Craniofac Res. 2016;19(3), 154-61.
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| Issue | Vol 11, No 1 (Winter 2024) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/jcr.v11i1.16476 | |
| Keywords | ||
| Histomorphometry Bmp 7 OPG Maxillary expansion Orthodontics Rats | ||
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How to Cite
1.
Eraydın F, Cumbul A, Kurnaz M, Ozdemir F. Effect of Adeno-Associated Virus-Transfected Mesenchymal Stem Cells Containing Agents on Bone Formation in Extended Inter-Premaxillary Suture in Rats. J Craniomaxillofac Res. 2024;11(1):9-19.
