Skip to main content

Advertisement

SpringerLink
Log in

BM-MSCs and Bio-Oss complexes enhanced new bone formation during maxillary sinus floor augmentation by promoting differentiation of BM-MSCs

  • Published:
In Vitro Cellular & Developmental Biology - Animal Aims and scope Submit manuscript

Abstract

Bone marrow-derived mesenchymal stem cells (BM-MSCs) have been recognized as a new strategy for maxillary sinus floor elevation. However, little is known concerning the effect of the biomechanical pressure (i.e., sinus pressure, masticatory pressure, and respiration) on the differentiation of BM-MSCs and the formation of new bone during maxillary sinus floor elevation. The differentiation of BM-MSCs into osteoblasts was examined in vitro under cyclic compressive pressure using the Flexcell® pressure system, and by immunohistochemical analysis, qRT-PCR, and Western blot. Micro-CT was used to detect bone formation and allow image reconstruction of the entire maxillary sinus floor elevation area. Differentiation of BM-MSCs into osteoblasts was significantly increased under cyclic compressive pressure. The formation of new bone was enhanced after implantation of the pressured complex of BM-MSCs and Bio-Oss during maxillary sinus floor elevation. The pressured complex of BM-MSCs and Bio-Oss promoted new bone formation and maturation in the rabbit maxillary sinus. Stem cell therapy combined with this tissue engineering technique could be effectively used in maxillary sinus elevation and bone regeneration.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7
Figure 8
Figure 9
Figure 10

Similar content being viewed by others

References

  • Ando K, Imai S, Isoya E et al (2009) Effect of dynamic compressive loading and its combination with a growth factor on the chondrocytic phenotype of 3-dimensional scaffold-embedded chondrocytes. Acta Orthop 80(6):724–733

    Article  PubMed  PubMed Central  Google Scholar 

  • Asai S, Shimizu Y, Ooya K (2002) Maxillary sinus augmentation model in rabbits: effect of occluded nasal ostium on new bone formation. Clin Oral Implants Res 13:405–409

    Article  PubMed  Google Scholar 

  • Bai C, Hou L, Ma Y, Chen L, Zhang M, Guan W (2013) Isolation and characterization of mesenchymal stem cells from chicken bone marrow. Cell Tissue Bank 14:437–451

    Article  CAS  PubMed  Google Scholar 

  • Bershadsky AD, Balaban NQ, Geiger B (2003) Adhesion-dependent cell mechanosensitivity. Annu Rev Cell Dev Biol 19:677–695

    Article  CAS  PubMed  Google Scholar 

  • Bian L, Fong JV, Lima EG, Stoker AM, Ateshian GA, Cook JL, Hung CT (2010) Dynamic mechanical loading enhances functional properties of tissue-engineered cartilage using mature canine chondrocytes. Tissue Eng Part A 16:1781–1790

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boyne PJ, James RA (1980) Grafting of the maxillary sinus floor with autogenous marrow and bone. J Oral Surg 38:613–616

    CAS  PubMed  Google Scholar 

  • Chen YJ, Huang CH, Lee IC, Lee YT, Chen MH, Young TH (2008) Effects of cyclic mechanical stretching on the mRNA expression of tendon/ligament-related and osteoblast-specific genes in human mesenchymal stem cells. Connect Tissue Res 49:7–14

    Article  CAS  PubMed  Google Scholar 

  • Connelly JT, Vanderploeg EJ, Mouw JK, Wilson CG, Levenston ME (2010) Tensile loading modulates bone marrow stromal cell differentiation and the development of engineered fibrocartilage constructs. Tissue Eng Part A 16:1913–1923

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Delaine-Smith RM, Reilly GC (2012) Mesenchymal stem cell responses to mechanical stimuli. Muscles Ligaments Tendons J 2:169–180

    PubMed  PubMed Central  Google Scholar 

  • Durak O, Tsai LH (2014) Human induced pluripotent stem cells: now open to discovery. Cell Stem Cell 15:4–6

    Article  CAS  PubMed  Google Scholar 

  • Esposito M, Grusovin MG, Worthington HV, Coulthard P (2006) Interventions for replacing missing teeth: bone augmentation techniques for dental implant treatment. Cochrane Database Syst Rev: CD003607

  • Esposito M, Grusovin MG, Kwan S, Worthington HV, Coulthard P (2008) Interventions for replacing missing teeth: bone augmentation techniques for dental implant treatment. Cochrane Database Syst Rev: CD003607

  • Felice P, Marchetti C, Iezzi G, Piattelli A, Worthington H, Pellegrino G, Esposito M (2009) Vertical ridge augmentation of the atrophic posterior mandible with interpositional bloc grafts: bone from the iliac crest vs. bovine anorganic bone. Clinical and histological results up to one year after loading from a randomized-controlled clinical trial. Clin Oral Implants Res 20:1386–1393

    Article  PubMed  Google Scholar 

  • Feng ZY, An XL, Zhang BP, Ma HB, Wang J, Liu B (2010) Research progress of focal adhesions in cell biomechanics. J Clin Rehabil Tissue Eng Res 14:8843–8846

    CAS  Google Scholar 

  • Fox DB, Cook JL, Kuroki K, Cockrell M (2006) Effects of dynamic compressive load on collagen-based scaffolds seeded with fibroblast-like synoviocytes. Tissue Eng 12:1527–1537

    Article  CAS  PubMed  Google Scholar 

  • Friedenstein AJ, Chailakhjan RK, Lalykina KS (1970) The development of fibroblast colonies in monolayer cultures of guinea-pig bone marrow and spleen cells. Cell Tissue Kinet 3:393–403

    CAS  PubMed  Google Scholar 

  • Georgescu CE, Rusu MC, Sandulescu M, Enache AM, Didilescu AC (2012) Quantitative and qualitative bone analysis in the maxillary lateral region. Surg Radiol Anat 34:551–558

    Article  PubMed  Google Scholar 

  • Gilbert PM, Havenstrite KL, Magnusson KE, Sacco A, Leonardi NA, Kraft P, Nguyen NK, Thrun S, Lutolf MP, Blau HM (2010) Substrate elasticity regulates skeletal muscle stem cell self-renewal in culture. Science 329:1078–1081

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He JR, Yang ZQ, Li B (2008) Optimization of isolation and culture conditions of rabbit bone marrow mesenchymal stem cells. J Clin Rehabil Tissue Eng Res 12:8463–8467

    Google Scholar 

  • He C, Liang J, Deng LF (2011) Effect of hydrostatic compressive loading on the cytoskeletal structure of human bone marrow mesenchymal stem cells. J Clin Rehabil Tissue Engineer Res 14:8843–8846

    Google Scholar 

  • Hilding AC (1941) Experimental sinus surgery: effects of operative windows on normal sinuses. Ann Otol Rhinol Laryngol 50:379–392

    Article  Google Scholar 

  • Hollister SJ (2005) Porous scaffold design for tissue engineering. Nat Mater 4:518–524

    Article  CAS  PubMed  Google Scholar 

  • Hou M, Yang KM, Zhang H, Zhu WQ, Duan FJ, Wang H, Song YH, Wei YJ, Hu SS (2007) Transplantation of mesenchymal stem cells from human bone marrow improves damaged heart function in rats. Int J Cardiol 115:220–228

    Article  PubMed  Google Scholar 

  • Ikada Y (2006) Challenges in tissue engineering. J R Soc Interface 3:589–601

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jensen OT, Shulman LB, Block MS, Iacono VJ (1998) Report of the Sinus Consensus Conference of 1996. Int J Oral Maxillofac Implants 13(Suppl):11–45

    PubMed  Google Scholar 

  • Jones AC, Arns CH, Sheppard AP, Hutmacher DW, Milthorpe BK, Knackstedt MA (2007) Assessment of bone ingrowth into porous biomaterials using MICRO-CT. Biomaterials 28:2491–2504

    Article  CAS  PubMed  Google Scholar 

  • Kadar K, Kiraly M, Porcsalmy B, Molnar B, Racz GZ, Blazsek J, Kallo K, Szabo EL, Gera I, Gerber G, Varga G (2009) Differentiation potential of stem cells from human dental origin—promise for tissue engineering. J Physiol Pharmacol 60(Suppl 7):167–175

    PubMed  Google Scholar 

  • Khetan S, Guvendiren M, Legant WR, Cohen DM, Chen CS, Burdick JA (2013) Degradation-mediated cellular traction directs stem cell fate in covalently crosslinked three-dimensional hydrogels. Nat Mater 12:458–465

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klein-Nulend J, Bacabac RG, Bakker AD (2012) Mechanical loading and how it affects bone cells: the role of the osteocyte cytoskeleton in maintaining our skeleton. Eur Cell Mater 24:278–291

    CAS  PubMed  Google Scholar 

  • Kopf J, Petersen A, Duda GN et al (2012) BMP2 and mechanical loading cooperatively regulate immediate early signaling events in the BMP pathway. BMC Biol 10:37–48

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Langer R, Vacanti JP (1993) Tissue engineering. Science 260:920–926

    Article  CAS  PubMed  Google Scholar 

  • Laurencin CT, Ambrosio AM, Borden MD, Cooper JA Jr (1999) Tissue engineering: orthopedic applications. Annu Rev Biomed Eng 1:19–46

    Article  CAS  PubMed  Google Scholar 

  • Lee BK, Choi SJ, Mack D, Oh SH (2011) Isolation of mesenchymal stem cells from the mandibular marrow aspirates. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 112:e86–e93

    Article  PubMed  Google Scholar 

  • Lin CS, Ning H, Lin G, Lue TF (2012) Is CD34 truly a negative marker for mesenchymal stromal cells? Cytotherapy 14:1159–1163

    Article  CAS  PubMed  Google Scholar 

  • Liu MT, Zhang QH (2010) Development of one new type of cytomechanics device. Stomatology 30:416–417

    Google Scholar 

  • Liu YK, Uemura T, Nemoto A et al (1997) Osteopontin involvement in integrin-mediated cell signaling and regulation of expression of alkaline phos- phatase during early differentiation of UMR cells. FEBS Lett 420(1):112–116

    Article  CAS  PubMed  Google Scholar 

  • Macias BR, Aspenberg P, Agholme F (2013) Paradoxical Sost gene expression response to mechanical unloading in metaphyseal bone. Bone 53(2):515–519

    Article  CAS  PubMed  Google Scholar 

  • Mafi P, Hindocha S, Mafi R, Griffin M, Khan WS (2011) Adult mesenchymal stem cells and cell surface characterization—a systematic review of the literature. Open Orthop J 5:253–260

    Article  Google Scholar 

  • Mangano C, Scarano A, Perrotti V, Iezzi G, Piattelli A (2007) Maxillary sinus augmentation with a porous synthetic hydroxyapatite and bovine-derived hydroxyapatite: a comparative clinical and histologic study. Int J Oral Maxillofac Implants 22:980–986

    PubMed  Google Scholar 

  • Marolt D, Knezevic M, Novakovic GV (2010) Bone tissue engineering with human stem cells. Stem Cell Res Ther 1:10

    Article  PubMed  Google Scholar 

  • Mathieu PS, Loboa EG (2012) Cytoskeletal and focal adhesion influences on mesenchymal stem cell shape, mechanical properties, and differentiation down osteogenic, adipogenic, and chondrogenic pathways. Tissue Eng Part B Rev 18:436–444

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matziolis G, Tuischer J, Kasper G et al (2006) Simulation of cell differentiation in fracture healing: mechanically loaded composite scaffolds in a novel bioreactor system. Tissue Eng 12(1):201–208

    Article  CAS  PubMed  Google Scholar 

  • Moy PK, Lundgren S, Holmes RE (1993) Maxillary sinus augmentation: histomorphometric analysis of graft materials for maxillary sinus floor augmentation. J Oral Maxillofac Surg 51:857–862

    Article  CAS  PubMed  Google Scholar 

  • Murphy MG, Cerchio K, Stoch SA et al (2005) Effect of L-000845704, all alphaVbeta3 integrin antagonist, on markers of bone turnover and bone mineral density in postmenopausal osteoporotic women. J Clin Endocrinol Metab 90(4):2022–2028

    Article  CAS  PubMed  Google Scholar 

  • Nickoloff BJ (1991) The human progenitor cell antigen (CD34) is localized on endothelial cells, dermal dendritic cells, and perifollicular cells in formalin-fixed normal skin, and on proliferating endothelial cells and stromal spindle-shaped cells in Kaposi’s sarcoma. Arch Dermatol 127:523–529

    Article  CAS  PubMed  Google Scholar 

  • Parfitt AM (1988) Bone histomorphometry: standardization of nomenclature, symbols and units. Summary of proposed system. Bone Miner 4:1–5

    CAS  PubMed  Google Scholar 

  • Roshan-Ghias A, Terrier A, Bourban PE, Pioletti DP (2010) In vivo cyclic loading as a potent stimulatory signal for bone formation inside tissue engineering scaffold. Eur Cell Mater 19:41–49

    CAS  PubMed  Google Scholar 

  • Salter DM, Robb JE, Wright MO (1997) Electrophysiological responses of human bone cells to mechanical stimulation: evidence for specific integrin function in mechanotransduction. J Bone Miner Res 12(7):1133–1141

    Article  CAS  PubMed  Google Scholar 

  • Sanchez C, Gabay O, Salvat C, Henrotin YE, Berenbaum F (2009) Mechanical loading highly increases IL-6 production and decreases OPG expression by osteoblasts. Osteoarthr Cartil 17:473–481

    Article  CAS  PubMed  Google Scholar 

  • Sartori S, Silvestri M, Forni F, Icaro Cornaglia A, Tesei P, Cattaneo V (2003) Ten-year follow-up in a maxillary sinus augmentation using anorganic bovine bone (Bio-Oss) A case report with histomorphometric evaluation. Clin Oral Implants Res 14:369–372

    Article  PubMed  Google Scholar 

  • Scharf KE, Lawson W, Shapiro JM, Gannon PJ (1995) Pressure measurements in the normal and occluded rabbit maxillary sinus. Laryngoscope 105:570–574

    Article  CAS  PubMed  Google Scholar 

  • Sen B, Xie Z, Case N, Ma M, Rubin C, Rubin J (2008) Mechanical strain inhibits adipogenesis in mesenchymal stem cells by stimulating a durable beta-catenin signal. Endocrinology 149:6065–6075

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sennerby L, Roos J (1998) Surgical determinants of clinical success of osseointegrated oral implants: a review of the literature. Int J Prosthodont 11:408–420

    CAS  PubMed  Google Scholar 

  • Shi Y, Li H, Zhang X, Fu Y, Huang Y, Lui PP, Tang T, Dai K (2011) Continuous cyclic mechanical tension inhibited Runx2 expression in mesenchymal stem cells through RhoA-ERK1/2 pathway. J Cell Physiol 226:2159–2169

    Article  CAS  PubMed  Google Scholar 

  • Smiler DG, Holmes RE (1987) Sinus lift procedure using porous hydroxyapatite: a preliminary clinical report. J Oral Implantol 13:239–253

    CAS  PubMed  Google Scholar 

  • Smiler DG, Johnson PW, Lozada JL, Misch C, Rosenlicht JL, Tatum OH Jr, Wagner JR (1992) Sinus lift grafts and endosseous implants. Treatment of the atrophic posterior maxilla. Dent Clin N Am 36:151–186, discussion 187–158

    CAS  PubMed  Google Scholar 

  • Tan SL, Ahmad TS, Selvaratnam L, Kamarul T (2013) Isolation, characterization and the multi-lineage differentiation potential of rabbit bone marrow-derived mesenchymal stem cells. J Anat 222:437–450

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tatum H Jr (1986) Maxillary and sinus implant reconstructions. Dent Clin N Am 30:207–229

    PubMed  Google Scholar 

  • Tomiyama T, Fukuda K, Yamazaki K, Hashimoto K, Ueda H, Mori S, Hamanishi C (2007) Cyclic compression loaded on cartilage explants enhances the production of reactive oxygen species. J Rheumatol 34:556–562

    CAS  PubMed  Google Scholar 

  • Trappmann B, Gautrot JE, Connelly JT, Strange DG, Li Y, Oyen ML, Cohen Stuart MA, Boehm H, Li B, Vogel V, Spatz JP, Watt FM, Huck WT (2012) Extracellular-matrix tethering regulates stem-cell fate. Nat Mater 11:642–649

    Article  CAS  PubMed  Google Scholar 

  • Villemure I, Chung MA, Seck CS, Kimm MH, Matyas JR, Duncan NA (2005) Static compressive loading reduces the mRNA expression of type II and X collagen in rat growth-plate chondrocytes during postnatal growth. Connect Tissue Res 46:211–219

    Article  CAS  PubMed  Google Scholar 

  • Woo I, Le BT (2004) Maxillary sinus floor elevation: review of anatomy and two techniques. Implant Dent 13:28–32

    Article  CAS  PubMed  Google Scholar 

  • Wood RM, Moore DL (1988) Grafting of the maxillary sinus with intraorally harvested autogenous bone prior to implant placement. Int J Oral Maxillofac Implants 3:209–214

    CAS  PubMed  Google Scholar 

  • Xu H, Shimizu Y, Asai S, Ooya K (2004) Grafting of deproteinized bone particles inhibits bone resorption after maxillary sinus floor elevation. Clin Oral Implants Res 15:126–133

    Article  PubMed  Google Scholar 

  • Yang C, Tibbitt MW, Basta L, Anseth KS (2014) Mechanical memory and dosing influence stem cell fate. Nat Mater 13:645–652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang JF, Zhou WW, Tang T, Hu JG, Yu JF, Yang YF, Zhou XM, Hu DX (2006) Transfection of human VEGF165 gene into bone marrow mesenchymal stem cells in rats. J Cent South Univ (Med Sci) 31:313–318

    CAS  Google Scholar 

  • Yu HS, Won JE, Jin GZ, Kim HW (2012) Construction of mesenchymal stem cell-containing collagen gel with a macrochanneled polycaprolactone scaffold and the flow perfusion culturing for bone tissue engineering. Biores Open Access 1:124–136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yurube T, Nishida K, Suzuki T, Kaneyama S, Zhang Z, Kakutani K, Maeno K, Takada T, Fujii M, Kurosaka M, Doita M (2010) Matrix metalloproteinase (MMP)-3 gene up-regulation in a rat tail compression loading-induced disc degeneration model. J Orthop Res 28:1026–1032

    CAS  PubMed  Google Scholar 

  • Zitzmann NU, Scharer P (1998) Sinus elevation procedures in the resorbed posterior maxilla. Comparison of the crestal and lateral approaches. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 85:8–17

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Implant Dentistry, The Affiliated Stomatology Hospital of Tongji University, 399 Yanchang Road, Shanghai, 200092, People’s Republic of China

    Qian Zhou, Bo-Han Yu & Zuo-Lin Wang

  2. Department of Prosthodontics, The Affiliated Stomatology Hospital of Tongji University, Shanghai, 200092, People’s Republic of China

    Wei-Cai Liu

Authors
  1. Qian Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bo-Han Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wei-Cai Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zuo-Lin Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zuo-Lin Wang.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Funding

This study was supported by a research grant (09411955100) to Tongji University by Prof. Zuolin Wang and the 2010 Shanghai Committee of Science and Technology, China (Grant No. IOXD1404500).

Additional information

Editor: Tetsuji Okamoto

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhou, Q., Yu, BH., Liu, WC. et al. BM-MSCs and Bio-Oss complexes enhanced new bone formation during maxillary sinus floor augmentation by promoting differentiation of BM-MSCs. In Vitro Cell.Dev.Biol.-Animal 52, 757–771 (2016). https://doi.org/10.1007/s11626-015-9995-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11626-015-9995-7

Keywords

Search

Navigation