Bone morphogenetic protein-2, -6, and -7 differently regulate osteogenic differentiation of human periodontal ligament stem cells

Journal of Biomedical Materials Research - Part B Applied Biomaterials

Volumn 102, Issue 1, 2014, Pages 119-130

  Hakki, Sema S ^a   Bozkurt, Buket ^a   Hakki, Erdogan E ^a   Kayis, Seyit Ali ^a   Turac, Gizem ^b   Yilmaz, Irem ^b   Karaoz, Erdal ^b  

^a SELCUK UNIVERSITY   (Turkey)

^b KOCAELI UNIVERSITY   (Turkey)

Author keywords

BMP 2; BMP 6; BMP 7; osteogenic differentiation; periodontal ligament stem cells

Indexed keywords

BMP-2; BMP-6; BMP-7; OSTEOGENIC DIFFERENTIATION; PERIODONTAL LIGAMENT;

BIOMINERALIZATION; BONE; GENE EXPRESSION; MINERALOGY; STEM CELLS; TISSUE ENGINEERING;

TISSUE;

5' NUCLEOTIDASE; ACTIVATED LEUKOCYTE CELL ADHESION MOLECULE; BETA1 INTEGRIN; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 6; BONE SIALOPROTEIN; COLLAGEN TYPE 1; COMMON ACUTE LYMPHOBLASTIC LEUKEMIA ANTIGEN; ENDOGLIN; HERMES ANTIGEN; HLA A ANTIGEN; HLA B ANTIGEN; HLA C ANTIGEN; MESSENGER RNA; MICROSOMAL AMINOPEPTIDASE; OSTEOCALCIN; OSTEOGENIC PROTEIN 1; OSTEOPONTIN; THY 1 ANTIGEN; TRANSCRIPTION FACTOR RUNX2; VASCULAR CELL ADHESION MOLECULE 1; BMP2 PROTEIN, HUMAN; BMP6 PROTEIN, HUMAN; BMP7 PROTEIN, HUMAN; RECOMBINANT PROTEIN; RUNX2 PROTEIN, HUMAN;

ADULT; ARTICLE; BIOMINERALIZATION; BONE DEVELOPMENT; BONE MINERALIZATION; CELL DIFFERENTIATION; CELL ISOLATION; CELL PROLIFERATION; CLINICAL ARTICLE; CONTROLLED STUDY; DOSE RESPONSE; FEMALE; GENE EXPRESSION; HISTOCHEMISTRY; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MALE; MOLAR TOOTH; OSTEOBLAST; PERIODONTAL LIGAMENT; PERIODONTAL LIGAMENT STEM CELL; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; STEM CELL; TISSUE ENGINEERING; TOOTH DISEASE; ADOLESCENT; ADULT STEM CELL; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; YOUNG ADULT;

ADOLESCENT; ADULT STEM CELLS; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 6; BONE MORPHOGENETIC PROTEIN 7; CALCIFICATION, PHYSIOLOGIC; CELL DIFFERENTIATION; CELL PROLIFERATION; CORE BINDING FACTOR ALPHA 1 SUBUNIT; FEMALE; GENE EXPRESSION REGULATION; HUMANS; INTEGRIN-BINDING SIALOPROTEIN; MALE; OSTEOCALCIN; OSTEOGENESIS; OSTEOPONTIN; PERIODONTAL LIGAMENT; RECOMBINANT PROTEINS; RNA, MESSENGER; YOUNG ADULT;

EID: 84890312853     PISSN: 15524973     EISSN: 15524981     Source Type: Journal    
DOI: 10.1002/jbm.b.32988     Document Type: Article

References (60)

1. Jones E, Yang X,. Mesenchymal stem cells and bone regeneration: current status. Injury 2011; 42: 562-568.
2. Kawate K, Yajima H, Ohgushi H, Kotobuki N, Sugimoto K, Ohmura T, Kobata Y, Shigematsu K, Kawamura K, Tamai K, Takakura Y,. Tissue-engineered approach for the treatment of steroid-induced osteonecrosis of the femoral head: transplantation of autologous mesenchymal stem cells cultured with beta-tricalcium phosphate ceramics and free vascularized fibula. Artif Organs 2006; 30: 960-962.
3. Khojasteh A, Behnia H, Dashti SG, Stevens M,. Current trends in mesenchymal stem cell application in bone augmentation: a review of the literature. J Oral Maxillofac Surg 2012; 70: 972-982.
4. Kon E, Filardo G, Roffi A, Di Martino A, Hamdan M, De Pasqual L, Merli ML, Marcacci M,. Bone regeneration with mesenchymal stem cells. Clin Cases Miner Bone Metab 2012; 9: 24-27.
5. Morishita T, Honoki K, Ohgushi H, Kotobuki N, Matsushima A, Takakura Y,. Tissue engineering approach to the treatment of bone tumors: three cases of cultured bone grafts derived from patients' mesenchymal stem cells. Artif Organs 2006; 30: 115-118.
6. Quarto R, Mastrogiacomo M, Cancedda R, Kutepov SM, Mukhachev V, Lavroukov A, Kon E, Marcacci M,. Repair of large bone defects with the use of autologous bone marrow stromal cells. N Engl J Med 200; 344: 385-386.
7. Marcacci M, Kon E, Moukhachev V, Lavroukov A, Kutepov S, Quarto R, Mastrogiacomo M, Cancedda R,. Stem cells associated with macroporous bioceramics for long bone repair: 6- to 7-year outcome of a pilot clinical study. Tissue Eng 2007; 13: 947-955.
8. Khojasteh A, Eslaminejad MB, Nazarian H,. Mesenchymal stem cells enhance bone regeneration in rat calvarial critical size defects more than platelete-rich plasma. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2008; 106: 356-362.
9. Warnke PH, Springer IN, Wiltfang J, Acil Y, Eufinger H, Wehmöller M, Russo PA, Bolte H, Sherry E, Behrens E, Terheyden H.Growth and transplantation of a custom vascularised bone graft in a man. Lancet 2004; 364: 766-770.
10. Yamada Y, Ito K, Nakamura S, Ueda M, Nagasaka T,. Promising cell-based therapy for bone regeneration using stem cells from deciduous teeth, dental pulp, and bone marrow. Cell Transplant 2011; 20: 1003-1013.
11. Zannettino AC, Paton S, Arthur A, Khor F, Itescu S, Gimble JM, Gronthos S,. Multipotential human adipose-derived stromal stem cells exhibit a perivascular phenotype in vitro and in vivo. J Cell Physiol 2008; 214: 413-421.
12. Hynes K, Menicanin D, Gronthos S, Bartold PM,. Clinical utility of stem cells for periodontal regeneration. Periodontol 2000 2012; 59: 203-227.
13. Karaöz E, Demircan PC, Saǧlam O, Aksoy A, Kaymaz F, Duruksu G,. Human dental pulp stem cells demonstrate better neural and epithelial stem cell properties than bone marrow-derived mesenchymal stem cells. Histochem Cell Biol 2011; 136: 455-473.
14. Karaöz E, Doǧan BN, Aksoy A, Gacar G, Akyüz S, Ayhan S, Genç ZS, Yürüker S, Duruksu G, Demircan PC, Sariboyaci AE,. Isolation and in vitro characterisation of dental pulp stem cells from natal teeth. Histochem Cell Biol 2010; 133: 95-112.
15. Seo BM, Miura M, Gronthos S, Bartold PM, Batouli S, Brahim J, Young M, Robey PG, Wang CY, Shi S,. Investigation of multipotent postnatal stem cells from human periodontal ligament. Lancet 2004; 364: 149-155.
16. Trubiani O, Orsini G, Zini N, Di Iorio D, Piccirilli M, Piattelli A, Caputi S,. Regenerative potential of human periodontal ligament derived stem cells on three-dimensional biomaterials: a morphological report. J Biomed Mater Res A 2008; 87: 986-993.
17. Vakhrushev IV, Antonov EN, Popova AV, Konstantinova EV, Karalkin PA, Kholodenko IV, Lupatov AY, Popov VK, Bagratashvili VN, Yarygin KN,. Design of tissue engineering implants for bone tissue regeneration of the basis of new generation polylactoglycolide scaffolds and multipotent mesenchymal stem cells from human exfoliated deciduous teeth (SHED cells). Bull Exp Biol Med 2012; 153: 143-7.
18. Wada N, Menicanin D, Shi S, Bartold PM, Gronthos S,. Immunomodulatory properties of human periodontal ligament stem cells. J Cell Physiol 2009; 219: 667-676.
19. Zhang QZ, Nguyen AL, Yu WH, Le AD,. Human oral mucosa and gingiva: a unique reservoir for mesenchymal stem cells. J Dent Res 2012; 91: 1011-1018.
20. Erices A, Conget P, Minguell JJ,. Mesenchymal progenitor cells in human umbilical cord blood. Br J Haematol. 2000; 109: 235-242.
21. Wang B, Huang S, Pan L, Jia S,. Enhancement of bone formation by genetically engineered human umbilical cord-derived mesenchymal stem cells expressing osterix. Oral Surg Oral Med Oral Pathol Oral Radiol. 2012 Jul 19. [Epub ahead of print].
22. Jones BA, Pei M,. Synovium-derived stem cells: a tissue-specific stem cell for cartilage engineering and regeneration. Tissue Eng Part B Rev 2012; 18: 301-311.
23. Kisiel AH, McDuffee LA, Masaoud E, Bailey TR, Esparza Gonzalez BP, Nino-Fong R,. Isolation, characterization, and in vitro proliferation of canine mesenchymal stem cells derived from bone marrow, adipose tissue, muscle, and periosteum. Am J Vet Res 2012; 73: 1305-1317.
24. Vaculik C, Schuster C, Bauer W, Iram N, Pfisterer K, Kramer G, Reinisch A, Strunk D, Elbe-Bürger A,. Human dermis harbors distinct mesenchymal stromal cell subsets. J Invest Dermatol 2012; 132: 563-574.
25. Koh YG, Choi YJ,. Infrapatellar fat pad-derived mesenchymal stem cell therapy for knee osteoarthritis. Knee 2012; 19: 902-907.
26. Huselstein C, Li Y, He X,. Mesenchymal stem cells for cartilage engineering. Biomed Mater Eng 2012; 22: 69-80.
27. Dorman LJ, Tucci M, Benghuzzi H, In vitro effects of bmp-2, bmp-7, and bmp-13 on proliferation and differentation of mouse mesenchymal stem cells. Biomed Sci Instrum 2012; 48: 81-87.
28. Mizrahi O, Sheyn D, Tawackoli W, Kallai I, Oh A, Su S, Da X, Zarrini P, Cook-Wiens G, Gazit D, Gazit Z,. BMP-6 is more efficient in bone formation than BMP-2 when overexpressed in mesenchymal stem cells. Gene Ther 2012; Jun 21. doi: 10.1038/gt.2012.45. [Epub ahead of print].
29. Phipps MC, Xu Y, Bellis SL,. Delivery of platelet-derived growth factor as a chemotactic factor for mesenchymal stem cells by bone-mimetic electrospun scaffolds. PLoS One. 2012; 7: e40831. Epub 2012 Jul 12.
30. Renner JN, Kim Y, Liu JC,. Bone morphogenetic protein-derived peptide promotes chondrogenic differentiation of human mesenchymal stem cells. Tissue Eng Part A 2012; 18: 2581-2589.
31. Akman AC, Seda Tiǧli R, Gümüşderelioǧlu M, Nohutcu RM,. Bone morphogenetic protein-6-loaded chitosan scaffolds enhance the osteoblastic characteristics of MC3T3-E1 cells. Artif Organs 2010; 34: 65-74.
32. Chen D, Zhao M, Mundy GR,. Bone morphogenetic proteins. Growth Factors 2004; 22: 233-241.
33. Hakki SS, Foster BL, Nagatomo KJ, Bozkurt SB, Hakki EE, Somerman MJ, Nohutcu RM,. Bone morphogenetic protein-7 enhances cementoblast function in vitro. J Periodontol 2010; 81: 1663-1674.
34. Kang SW, Bae JH, Park SA, Kim WD, Park MS, Ko YJ, Jang HS, Park JH,. Combination therapy with BMP-2 and BMSCs enhances bone healing efficacy of PCL scaffold fabricated using the 3D plotting system in a large segmental defect model. Biotechnol Lett 2012; 34: 1375-1384.
35. Kim HK, Kim JH, Park DS, Park KS, Kang SS, Lee JS, Jeong MH, Yoon TR,. Osteogenesis induced by a bone forming peptide from the prodomain region of BMP-7. Biomaterials 2012; 33: 7057-7063.
36. Kishigami S, Mishina Y,. BMP signaling and early embryonic patterning. Cytokine Growth Factor Rev 2005; 16: 265-278.
37. Kamiya N,. The role of BMPs in bone anabolism and their potential targets SOST and DKK1. Curr Mol Pharmacol 2012; 5: 153-163.
38. Gautschi OP, Frey SP, Zellweger R,. Bone morphogenetic proteins in clinical applications. ANZ J Surg. 2007; 77: 626-631.
39. Vukicevic S, Grgurevic L,. BMP-6 and mesenchymal stem cell differentiation. Cytokine Growth Factor Rev 2009; 20: 441-448.
40. Garrison KR, Shemilt I, Donell S, Ryder JJ, Mugford M, Harvey I, Song F, Alt V,. Bone morphogenetic protein (BMP) for fracture healing in adults. Cochrane Database Syst Rev 2010;: CD006950.
41. O'hEireamhoin S, Quinlan JF, Rourke KO,. The use of bone morphogenetic protein 7 in fracture non-unions. Orthop Surg 2011; 3: 40-44.
42. Woo EJ,. Adverse events after recombinant human BMP2 in nonspinal orthopaedic procedures. Clin Orthop Relat Res. 2012 Nov 7. [Epub ahead of print].
43. Song K, Krause C, Shi S, Patterson M, Suto R, Grgurevic L, Vukicevic S, van Dinther M, Falb D, Ten Dijke P, Alaoui-Ismaili MH, Xiang. Identification of a key residue mediating bone morphogenetic protein (BMP)-6 resistance to noggin inhibition allows for engineered BMPs with superior agonist activity. J Biol Chem. 2010; 285: 12169-12180.
44. Xiang L, Liang C, Zhen-Yong K, Liang-Jun Y, Zhong-Liang D,. BMP9-induced osteogenetic differentiation and bone formation of muscle-derived stem cells. J Biomed Biotechnol. 2012; 2012: 610952.Epub 2012 Jan 26.
45. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop Dj, Horwitz E,. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006; 8: 315-317.
46. Horwitz EM, Le Blanc K, Dominici M, Mueller I, Slaper-Cortenbach I, Marini FC, Deans RJ, Krause DS, Keating A,; International Society for Cellular Therapy. Clarification of the nomenclature for MSC: The International Society for Cellular Therapy position statement. Cytotherapy 2005; 7: 393-395.
47. Hughes OR, Stewart R, Dimmick I, Jones EA,. A critical appraisal of factors affecting the accuracy of results obtained when using flow cytometry in stem cell investigations: where do you put your gates? Cytometry A 2009; 75: 803-810.
48. R Development Core Team R: A language and environment for statistical computing. R Foundation for Statistical Computing, 2012. Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org.
49. Akiyama K, Chen C, Gronthos S, Shi S,. Lineage differentiation of mesenchymal stem cells from dental pulp, apical papilla, and periodontal ligament. Methods Mol Biol 2012; 887: 111-121.
50. Gronthos S, Mankani M, Brahim J, Robey PG, Shi S,. Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo. Proc Natl Acad Sci U S A 2000; 97: 13625-13630.
51. Iwata T, Yamato M, Zhang Z, Mukobata S, Washio K, Ando T, Feijen J, Okano T, Ishikawa I,. Validation of human periodontal ligament-derived cells as a reliable source for cytotherapeutic use. J Clin Periodontol 2010; 37: 1088-1099.
52. Miura M, Gronthos S, Zhao M, Lu B, Fisher LW, Robey PG, Shi S,. SHED: stem cells from human exfoliated deciduous teeth. Proc Natl Acad Sci U S A. 2003; 100: 5807-5812.
53. Morsczeck C, Götz W, Schierholz J, Zeilhofer F, Kühn U, Möhl C, Sippel C, Hoffmann KH,. Isolation of precursor cells (PCs) from human dental follicle of wisdom teeth. Matrix Biol. 2005; 24: 155-165.
54. Tsumanuma Y, Iwata T, Washio K, Yoshida T, Yamada A, Takagi R, Ohno T, Lin K, Yamato M, Ishikawa I, Okano T, Izumi Y,. Comparison of different tissue-derived stem cell sheets for periodontal regeneration in a canine 1-wall defect model. Biomaterials 2011; 32: 5819-5825.
55. Fawzy El-Sayed KM, Dörfer C, Fändrich F, Gieseler F, Moustafa MH, Ungefroren H,. Adult Mesenchymal Stem Cells Explored in the Dental Field. Adv Biochem Eng Biotechnol 2012; Sep 1. [Epub ahead of print].
56. Lavery K, Hawley S, Swain P, Rooney R, Falb D, Alaoui-Ismaili MH.New insights into BMP-7 mediated osteoblastic differentiation of primary human mesenchymal stem cells. Bone 2009; 45: 27-41.
57. Luu HH, Song WX, Luo X, Manning D, Luo J, Deng ZL, Sharff KA, Montag AG, Haydon RC, He TC,. Distinct roles of bone morphogenetic proteins in osteogenic differentiation of mesenchymal stem cells. J Orthop Res 2007; 25: 665-677.
58. Qing W, Guang-Xing C, Lin G, Liu Y,. The osteogenic study of tissue engineering bone with BMP2 and BMP7 gene-modified rat adipose-derived stem cell. J Biomed Biotechnol 2012; 2012: 410879. Epub 2012 Jun 21.
59. Lavery K, Swain P, Falb D, Alaoui-Ismaili MH,. BMP-2/4 and BMP-6/7 differentially utilize cell surface receptors to induce osteoblastic differentiation of human bone marrow-derived mesenchymal stem cells. J Biol Chem 2008; 283: 20948-20958.
60. Moshaverinia A, Chen C, Akiyama K, Ansari S, Xu X, Chee WW, Schricker SR, Shi S,. Alginate hydrogel as a promising scaffold for dental-derived stem cells: an in vitro study. J Mater Sci Mater Med 2012; 23: 3041-3051.