The role of gap junctions and mechanical loading on mineral formation in a collagen-I scaffold seeded with osteoprogenitor cells

Tissue Engineering - Part A

Volumn 21, Issue 9-10, 2015, Pages 1720-1732

  Damaraju, Swathi ^a   Matyas, John R ^a   Rancourt, Derrick E ^a   Duncan, Neil A ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BONE; COLLAGEN; CYTOLOGY; DEFECTS; DISSOCIATION; FLUORESCENCE; MINERALOGY; PHOTOBLEACHING; POLYMERASE CHAIN REACTION; STEM CELLS; TISSUE;

CELL MATRIX INTERACTIONS; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; INTERCELLULAR COMMUNICATIONS; MECHANICAL STIMULATION; MURINE EMBRYONIC STEM CELLS; OSTEOBLAST DIFFERENTIATION; REVERSE TRANSCRIPTASE- POLYMERASE CHAIN REACTION; TISSUE-ENGINEERED SCAFFOLDS;

SCAFFOLDS (BIOLOGY);

CATHEPSIN B; COLLAGEN TYPE 1; CONNEXIN 43; OCTAMER TRANSCRIPTION FACTOR 4; OSTEOCALCIN; TRANSCRIPTION FACTOR RUNX2; TRANSCRIPTION FACTOR SOX2; VERY LATE ACTIVATION ANTIGEN 5; OCTANOL;

ANIMAL CELL; ARTICLE; BONE MINERALIZATION; CELL COMMUNICATION; CELL CONTACT; CELL DIFFERENTIATION; CELL VIABILITY; COMPRESSION; CONTROLLED STUDY; EMBRYONIC STEM CELL; EXTRACELLULAR MATRIX; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GAP JUNCTION; IN VITRO STUDY; MOUSE; NONHUMAN; OSTEOBLAST; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ANIMAL; BIOMECHANICS; BONE; BOVINE; CELL SURVIVAL; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; METABOLISM; MOUSE EMBRYONIC STEM CELL; REAL TIME POLYMERASE CHAIN REACTION; STEM CELL; TISSUE SCAFFOLD; TUNEL ASSAY; WEIGHT BEARING;

MURINAE;

1-OCTANOL; ANIMALS; BIOMECHANICAL PHENOMENA; BONE AND BONES; CALCIFICATION, PHYSIOLOGIC; CATTLE; CELL DIFFERENTIATION; CELL SURVIVAL; COLLAGEN TYPE I; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; FLUORESCENT ANTIBODY TECHNIQUE; GAP JUNCTIONS; GENE EXPRESSION REGULATION; IN SITU NICK-END LABELING; MICE; MOUSE EMBRYONIC STEM CELLS; OSTEOBLASTS; REAL-TIME POLYMERASE CHAIN REACTION; STEM CELLS; TISSUE SCAFFOLDS; WEIGHT-BEARING;

EID: 84929494344     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2014.0522     Document Type: Article

References (60)

1. Drosse, I., Volkmer, E., Capanna, R., De Biase, P., Mutschler, W., and Schieker, M. Tissue engineering for bone defect healing: an update on a multi-component approach. Inj Int J Care Inj 39S2, S9, 2008.
2. Schroeder, J.E., and Mosheiff, R. Tissue engineering approaches for bone repair: concepts and evidence. Injury 42, 609, 2011.
3. Catagni, M.A., Guerreschi, F., Holman, J.A., and Cattaneo, R. Distraction osteogenesis in the treatment of stiff hypertrophic nonunions using the Ilizarov apparatus. Clin Orthop Relat Res 301, 159, 1994.
4. Cancedda, R., Giannoni, P., and Mastrogiacomo, M. A tissue engineering approach to bone repair in large animal models and in clinical practice. Biomaterials 28, 4240, 2007.
5. Mckibbin, B. The Biology of Fracture Healing in Long Bones. J Bone Jt Surg 60-B, 150, 1978.
6. Geris, L., Sloten, J.V., and Van Oosterwyck, H. Connecting biology and mechanics in fracture healing: an integrated mathematical modeling framework for the study of nonunions. Biomech Model Mechanobiol 9, 713, 2010.
7. Igwe, J.C., Mikael, P.E., and Nukavarapu, S.P. Design, fabrication and in vitro evaluation of a novel polymerhydrogel hybrid scaffold for bone tissue engineering. J Tissue Eng Regen Med 8, 131, 2014.
8. Tan, F., Xu, X., Deng, T., Yin, M., Zhang, X., and Wang, J. Fabrication of positively charged poly(ethylene glycol)-diacrylate hydrogel as a bone tissue engineering scaffold. Biomed Mater 7, 055009, 2012.
9. Ferreira, A.M., Gentile, P., Chiono, V., and Ciardelli, G. Collagen for bone tissue regeneration. Acta Biomater 8, 3191, 2012.
10. Dumont, C., Burchhardt, H., Dresing, K., Rudy, T., Bohr, S., and Stürmer, K.M. Free scapular or parascapular flaps for soft tissue damage accompanying talus or calcaneus fractures. Chirurg 78, 643, 2007.
11. Dumont, C., Fuchs, M., Burchhardt, H., Appelt, D., Bohr, S., and Stürmer, K.M. Clinical results of absorbable plates for displaced metacarpal fractures. J Hand Surg Am 32, 491, 2007.
12. Fuchs, M., Burchhardt, H., Dresing, K., Radebold, T., and Stürmer, K.M. Resection of the calcaneus as a treatment option in osteitis following an open calcaneus fracture. Unfallchirurg 103, 602, 2000.
13. Balcarek, P., Burchhardt, H., and Stürmer, K.M. Minimally invasive removal of a broken femoral nail. Unfallchirurg 108, 419, 2005.
14. Keller, G. Embryonic stem cell differentiation: emergence of a new era in biology and medicine. Genes Dev 19, 1129, 2005.
15. Krawetz, R.J., Taiani, J.T., Wu, Y.E., Liu, S., Meng, G., Matyas, J.R., et al. Collagen I scaffolds cross-linked with beta-glycerol phosphate induce osteogenic differentiation of embryonic stem cells in vitro and regulate their tumorigenic potential in vivo. Tissue Eng 18, 1014, 2012.
16. Damaraju, S., Matyas, J.R., Rancourt, D., and Duncan, N. The effect of mechanical stimulation on mineralization in differentiating osteoblasts in collagen-I scaffolds. Tissue Eng Part A 20, 3142, 2014.
17. Batra, N., Kar, R., and Jiang, J.X. Gap junctions and hemichannels in signal transmission, function and development of bone. Biochim Biophys Acta 1818, 1909, 2012.
18. Jiang, J.X., Siller-Jackson, A.J., and Burra, S. Roles of gap junctions and hemichannels in bone cell functions and in signal transmission of mechanical stress. Front Biosci 12, 1450, 2007.
19. Dale, B., Gualtieri, R., Talevi, R., Tosti, E., Santella, L., and Elder, K. Intercellular communication in the early human embryo. Mol Reprod Dev 29, 22, 1991.
20. Stains, J.P., and Civitelli, R. Cell-to-cell interactions in bone. Biochem Biophys Res Commun 328, 721, 2005.
21. Sims, N.A., and Martin, T.J. Coupling the activities of bone formation and resorption: A multitude of signals within the basic multicellular unit. Bonekey Rep 3, 481, 2014.
22. Tonna, S., and Sims, N.A. Talking among ourselves: paracrine control of bone formation within the osteoblast lineage. Calcif Tissue Int 94, 35, 2014.
23. Mullender, M., El Haj, A., Yang, Y., van Duin, M., Burger, E., and Klein-Nulend, J. Mechanotransduction of bone cells in vitro: mechanobiology of bone tissue. Med Biol Eng Comput 42, 14, 2004.
24. Boppart, M.D., Kimmel, D.B., Yee J.A., and Cullen, D.M. Time course of osteoblast appearance after in vivo mechanical loading. Bone 23, 409, 1998.
25. Chen, J.-H., Liu, C., You, L., and Simmons, C.A. Boning up on Wolff's Law: Mechanical regulation of the cells that make and maintain bone. J Biomech 43, 108, 2010.
26. Hazenbiller, O. Micro-environmental factors directing differentiation of murine embryonic stem cells down osteogenic and chondrogenic lineages [master's thesis]. University of Calgary, p. 203, 2013. Available at http://theses.ucalgary .ca/handle/11023/554, accessed May, 2014.
27. Sanchez, C., Gabay, O., Salvat, C., Henrotin, Y.E., and Berenbaum, F. Mechanical loading highly increases IL-6 production and decreases OPG expression by osteoblasts. Osteoarthritis Cartilage 17, 473, 2009.
28. Sanchez, C., Pesesse, L., Gabay, O., Delcour, J.-P., Msika, P., Baudouin, C., et al. Regulation of subchondral bone osteoblast metabolism by cyclic compression. Arthritis Rheum 64, 1193, 2012.
29. Gabay, O., Hall, D., Berenbaum, F., Henrotin, Y., and Sanchez, C. Osteoarthritis and obesity: experimental models. Jt Bone Spine 75, 675, 2008.
30. Hanson, A.D., Marvel, S.W., Bernacki, S.H., Banes, A.J., van Aalst, J., and Loboa, E.G. Osteogenic effects of rest inserted and continuous cyclic tensile strain on hASC lines with disparate osteodifferentiation capabilities. Ann Biomed Eng 37, 955, 2009.
31. Gross, T.S., Poliachik, S.L., Ausk, B.J., Sanford, D.A., Becker, B.A., and Srinivasan, S. Why rest stimulates bone formation: A hypothesis based on complex adaptive phenomenon. Exerc Sport Sci Rev 32, 9, 2004.
32. Srinivasan, S., Ausk, B.J., Poliachik, S.L., Warner, S.E., Richardson, T.S., and Gross, T.S. Rest-inserted loading rapidly amplifies the response of bone to small increases in strain and load cycles. J Appl Physiol 102, 1945, 2007.
33. Kang, M.-N., Yoon, H.-H., Seo, Y.-K., and Park, J.-K. Effect of mechanical stimulation on the differentiation of cord stem cells. Connect Tissue Res 53, 149, 2012.
34. Li, S., Jia, X., Duance, V.C., and Blain, E.J. The effects of cyclic tensile strain on the organisation and expression of cytoskeletal elements in bovine intervertebral disc cells: an in vitro study. Eur Cell Mater 21, 508, 2011.
35. Qi, J., Chi, L., Wang, J., Sumanasinghe, R., Wall, M., Tsuzaki, M., et al. Modulation of collagen gel compaction by extracellular ATP is MAPK and NF-kappaB pathways dependent. Exp Cell Res 315, 1990, 2009.
36. Davidson, J.S., and Baumgarten, I.M. Glycyrrhetinic acid derivatives: A novel class of inhibitors of gap-junctional intercellular communication. Structure-activity relationships. J Pharmacol Exp Ther 246, 1104, 1988.
37. Schiller, P.C., D'Ippolito, G., Balkan, W., Roos, B.A., and Howard, G.A. Gap-junctional communication is required for the maturation process of osteoblastic cells in culture. Bone 28, 362, 2001.
38. Thorpe, S.D., Buckley, C.T., Steward, A.J., and Kelly, D.J. European Society of Biomechanics S.M. Perren Award 2012: the external mechanical environment can override the influence of local substrate in determining stem cell fate. J. Biomech 45, 2483, 2012.
39. Proulx, A., Merrifield, P.A., and Naus, C.C. Communication in myoblasts inhibits myogenin and MRF4 expression. Dev Genet 20, 133, 1997.
40. Hunter, C.J., Matyas, J.R., and Duncan, N.A. The functional significance of cell clusters in the notochordal nucleus pulposus: survival and signaling in the canine intervertebral disc. Spine (Phila. Pa. 1976) 29, 1099, 2004.
41. Desrochers, J., and Duncan, N.A. Intercellular communication via gap junctions affected by mechanical load in the bovine annulus fibrosus. Comput Methods Biomech Biomed Engin 17, 37, 2014.
42. Batra, N., Burra, S., Siller-Jackson, A.J., Gu, S., Xia, X., and Weber, G.F. Mechanical stress-activated integrin a5b1 induces opening of connexin 43 hemichannels. PNAS 109, 3359, 2012.
43. Song, I.-H., Caplan, A.I., and Dennis, J.E. In vitro dexamethasone pretreatment enhances bone formation of human mesenchymal stem cells in vivo. J Orthop Res 27, 916, 2009.
44. Sheehan, D.C., and Hrapchak, B.B. Theory and Practice of Histotechnology. Columbus, OH: Battelle Press, 1987.
45. Villanueva, A.R., Kujawa, M., Mathews, C.H., and Parfitt, A.M. Identification of the mineralization front: comparison of a modified toluidine blue stain with tetracycline fluorescence. Metab Bone Dis Relat Res 5, 41, 1983.
46. Möller, B., Wiltfang, J., Acil, Y., Gierloff, M., Lippross, S., and Terheyden, H. Prevention of the surface resorption of bone grafts by topical application of bisphosphonate on different carrier materials. Clin Oral Investig 18, 2203, 2014.
47. Halpern, J., Lynch, C.C., Fleming, J., Hamming, D., Martin, M.D., Schwartz, H.S., et al. The application of a murine bone bioreactor as a model of tumor: bone interaction. Clin Exp Metastasis 23, 345, 2006.
48. Moursi, A.M., Globus, R.K., and Damsky, C.H. Interactions between integrin receptors and fibronectin are required for calvarial osteoblast differentiation in vitro. J Cell Sci 110 (Pt 1), 2187, 1997.
49. Schmittgen, T.D., and Livak, K.J. Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3, 1101, 2008.
50. Kuchipudi, S.V., Tellabati, M., Nelli, R.K., White, G.A., Perez, B.B., Sebastian, S., et al. 18S rRNA is a reliable normalisation gene for real time PCR based on influenza virus infected cells. Virol J 9, 230, 2012.
51. Nyström, K., Biller, M., Grahn, A., Lindh, M., Larson, G., and Olofsson, S. Real time PCR for monitoring regulation of host gene expression in herpes simplex virus type 1-infected human diploid cells. J Virol Methods 118, 83, 2004.
52. Bas, A., Forsberg, G., Hammarström, S., and Hammarström, M.-L. Utility of the housekeeping genes 18S rRNA, beta-actin and glyceraldehyde-3-phosphate-dehydrogenase for normalization in real-time quantitative reverse transcriptase-polymerase chain reaction analysis of gene expression in human T lymphocytes. Scand J Immunol 59, 566, 2004.
53. Wredenberg, A., Wibom, R., Wilhelmsson, H., Graff, C., Wiener, H.H., Burden, S.J., et al. Increased mitochondrial mass in mitochondrial myopathy mice. Proc Natl Acad Sci USA 99, 15066, 2002.
54. Baker, B.A., Rao, K.M.K., Mercer, R.R., Geronilla, K.B., Kashon, M.L., Miller, G.R., et al. Quantitative histology and MGF gene expression in rats following SSC exercise in vivo. Med Sci Sports Exerc 38, 463, 2006.
55. Cheng, B., Zhao, S., Luo, J., Sprague, E., Bonewald, L.F., and Jiang, J.X. Expression of functional gap junctions and regulation by fluid flow in osteocyte-like MLO-Y4 cells. J Bone Miner Res 16, 249, 2001.
56. Waggett, A.D., Benjamin, M., and Ralphs, J.R. Connexin 32 and 43 gap junctions differentially modulate tenocyte response to cyclic mechanical load. Eur J Cell Biol 85, 1145, 2006.
57. Genetos, D.C., Kephart, C.J., Zhang, Y., Yellowley, C.E., and Donahue, H.J. Oscillating fluid flow activation of gap junction hemichannels induces ATP release from MLO-Y4 osteocytes. J Cell Physiol 212, 207, 2007.
58. Taylor, A.F., Saunders, M.M., Shingle, D.L., Cimbala, J.M., Zhou, Z., and Donahue, H.J. Mechanically stimulated osteocytes regulate osteoblastic activity via gap junctions. Am J Physiol Cell Physiol 292, C545, 2007.
59. Gramsch, B., Gabriel, M., Wiemann, M., Grummer, R., Winterhager, E., Bingmann, D., and Schirrmacher, K. Enhancement of connexin 43 expression increases proliferation and differentiation of an osteoblast-like cell line. Exp Cell Res 264, 397, 2001.
60. Lecanda, F., Towler, D.A., Ziambaras, K., Cheng, S.L., Koval, M., Steinberg, T.H., et al. Gap junctional communication modulates gene expression in osteoblastic cells. Mol Biol Cell 9, 2249, 1998.