Osteocyte differentiation is regulated by extracellular matrix stiffness and intercellular separation

Journal of the Mechanical Behavior of Biomedical Materials

Volumn 28, Issue , 2013, Pages 183-194

  Mullen, C A ^a   Haugh, M G ^a   Schaffler, M B ^b   Majeska, R J ^b   McNamara, L M ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^b City College of New York   (United States)

Author keywords

Bone; Cellular differentiation; Extracellular mechanical environment; Osteoblast; Osteocyte

Indexed keywords

ALKALINE PHOSPHATASE; CELLULAR DIFFERENTIATION; CHEMICAL COMPOSITIONS; DENTIN MATRIX PROTEINS; EXTRACELLULAR MATRICES; MECHANICAL ENVIRONMENT; OSTEOBLAST DIFFERENTIATION; OSTEOCYTES;

BONE; CYTOLOGY; FLOW MEASUREMENT; MINERALOGY; MORPHOLOGY; PHOSPHATASES; PROTEINS; STIFFNESS; SUBSTRATES;

OSTEOBLASTS;

ALKALINE PHOSPHATASE; COLLAGEN TYPE 1; DENTIN MATRIX PROTEIN 1; SCLEROSTIN;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL SEPARATION; CHEMICAL COMPOSITION; CONTROLLED STUDY; DENSITY; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; GENE EXPRESSION; MINERALIZATION; MOUSE; NONHUMAN; OSTEOBLAST; OSTEOCYTE; PRIORITY JOURNAL; RIGIDITY;

BONE; CELLULAR DIFFERENTIATION; EXTRACELLULAR MECHANICAL ENVIRONMENT; OSTEOBLAST; OSTEOCYTE;

3T3 CELLS; ALKALINE PHOSPHATASE; ANIMALS; BIOMECHANICAL PHENOMENA; CELL DIFFERENTIATION; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; MECHANICAL PROCESSES; MICE; MINERALS; OSTEOCYTES;

EID: 84883206752     PISSN: 17516161     EISSN: 18780180     Source Type: Journal    
DOI: 10.1016/j.jmbbm.2013.06.013     Document Type: Article

References (71)

1. Atkins G.J., Welldon K.J., Wijenayaka A.R., Bonewald L.F., Findlay D.M. Vitamin K promotes mineralization, osteoblast-to-osteocyte transition, and an anticatabolic phenotype by γ-carboxylation-dependent and -independent mechanisms. American Journal of Physiology- Cell Physiology 2009, 297:C1358-C1367.
2. Birmingham E., Niebur G.L., Mchugh P.E., Shaw G., Barry F.P., Mcnamara L.M. Osteogenic differentiation of mesenchymal stem cells is regulated by osteocyte and osteoblast cells in a simplified bone niche. European Cells and Materials 2012, 23:13-27.
3. Bitar M., Brown R.A., Salih V., Kidane A.G., Knowles J.C., Nazhat S.N. Effect of cell density on osteoblastic differentiation and matrix degradation of biomimetic dense collagen scaffolds. Biomacromolecules 2007, 9:129-135.
4. Boivin G., Morel G., Lian J.B., Anthoine-Terrier C., Dubois P.M., Meunier P.J. Localization of endogenous osteocalcin in neonatal rat bone and its absence in articular cartilage: Effect of warfarin treatment. Virchows Archives 1990, 417:505-512.
5. Bonewald L.F. Establishment and characterization of an osteocyte-like cell line, MLO-Y4. Journal of Bone and Mineral Metabolism 1999, 17:61-65.
6. Boukhechba F., Balaguer T., Michiels J.-F., Ackermann K., Quincey D., Bouler J.-M., Pyerin W., CARLE G.F., Rochet N. Human primary osteocyte differentiation in a 3D culture system. Journal of Bone and Mineral Research 2009, 24:1927-1935.
7. Brennan O., O'Brien F.J., Mcnamara L.M. Estrogen plus estrogen receptor antagonists alter mineral production by osteoblasts in vitro. Hormone and Metabolic Research 2012, 44:154.
8. Brounais B., Chipoy C., Mori K., Charrier C., Battaglia S., Pilet P., Richards C.D., HEYMANN D., Rédini F., Blanchard F. Oncostatin M induces bone loss and sensitizes rat osteosarcoma to the antitumor effect of Midostaurin in vivo. Clinical Cancer Research 2008, 14:5400-5409.
9. Dallas S.L., Bonewald L.F. Dynamics of the transition from osteoblast to osteocyte. Annals of the New York Academy of Sciences 2010, 1192:437-443.
10. Dean D., Boyan B., Muniz O., Howell D., Schwartz Z. Vitamin D metabolites regulate matrix vesicle metalloproteinase content in a cell maturation-dependent manner. Calcified Tissue International 1996, 59:109-116.
11. Donahue H.J. Gap junctional intercellular communication in bone: a cellular basis for mechanostat set point. Calcified Tissue International 1998, 62.
12. Doty S. Morphological evidence of gap junctions between bone cells. Calcified Tissue International 1981, 33:509-512.
13. Engler A.J., Sen S., Sweeney H.L., Discher D.E. Matrix elasticity directs stem cell lineage specification. Cell 2006, 126:677-689.
14. Estell, E.G. 2012. Substrate Stiffness and Adhesivity Influence Neuron Axonal Growth. Biological Engineering, University of Maine.
15. Evans N.D., Minelli C., Gentleman E., Lapointe V., Patankar S.N., Kallivretaki M., Chen X., Roberts C.J., Stevens M.M. Substrate stiffness affects early differentiation events in embryonic stem cells. European Cells and Materials 2009, 18:1-14.
16. Feng H., Lu Y.E., Tsutsui Xie, Kunieda Castranio, Bonewald Scott, Mishina The Dentin matrix protein 1 (Dmp1) is specifically expressed in mineralized, but not soft, tissues during development. Journal of Dental Research 2003, 82:776-780.
17. Franz-Odendaal T.A., Hall B.K., Witten P.E. Buried alive: how osteoblasts become osteocytes. Developmental Dynamics 2006, 235:176-190.
18. Georges M., Meaney, Sawyer, Janmey Matrices with compliance comparable to that of brain tissue select neuronal over glial growth n mixed cortical cultures. Biophysical Journal 2006, 90:3012-3018.
19. Gooi J.H., Pompolo S., Karsdal M.A., Kulkarni N.H., Kalajzic I., Mcahren S.H.M., Han B., Onyia J.E., Ho P.W.M., Gillespie M.T., Walsh N.C., Chia L.Y., Quinn J.M.W., Martin T.J., Sims N.A. Calcitonin impairs the anabolic effect of PTH in young rats and stimulates expression of sclerostin by osteocytes. Bone 2010, 46:1486-1497.
20. Gu G., Nars M., Hentunen T., Metsikkö K., Väänänen H. Isolated primary osteocytes express functional gap junctions in vitro. Cell and Tissue Research 2006, 323:263-271.
21. Gupta R.R., Yoo D.J., Hebert C., Niger C., Stains J.P. Induction of an osteocyte-like phenotype by fibroblast growth factor-2. Biochemical and Biophysical Research Communications 2010, 402(258-264).
22. Haugh M.G., Murphy C.M., Mckiernan R.C., Altenbuchner C., O'Brien F.J. Crosslinking and mechanical properties significantly influence cell attachment, proliferation, and migration within collagen glycosaminoglycan scaffolds. Tissue Engineering Part A 2011, 17:1201-1208.
23. Hentunen T. MLO-Y4 Cell Line as a Tool to Study the Regulatory Functions of Osteocytes 2010, RSCI, Dublin.
24. Holy C.E., Shoichet M.S., Davies J.E. Engineering three-dimensional bone tissue in vitro using biodegradable scaffolds: investigating initial cell-seeding density and culture period. Journal of Biomedical Materials Research 2000, 51:376-382.
25. Hsiong S.X., Carampin P., Kong H.-J., Lee K.Y., Mooney D.J. Differentiation stage alters matrix control of stem cells. Journal of Biomedical Materials Research Part A 2008, 87A:145-156.
26. Hurley M.M., Abreu C., Harrison J.R., Lichtler A.C., Raisz L.G., Kream B.E. Basic fibroblast growth factor inhibits type I collagen gene expression in osteoblastic MC3T3-E1 cells. Journal of Biological Chemistry 1993, 268:5588-5593.
27. Huveneers S., Danen E.H.J. Adhesion signaling-crosstalk between integrins, Src and Rho. Journal of Cell Science 2009, 122:1059-1069.
28. Igarashi M., Kamiya N., Ito K., Takagi M. In situ localization and in vitro expression of osteoblast/osteocyte factor 45 mRNA during bone cell differentiation. The Histochemical Journal 2002, 34:255-263.
29. Jee W.S.S. Integrated bone tissue physiology: anatomy and physiology. Bone Mechanics Handbook 2001, CRC Press, LLC Boca Raton. 2 ed. S.C. Cowin (Ed.).
30. Kamioka H., Ishihara Y., Ris H., Murshid S.A., Sugawara Y., Takano-Yamamoto T., Lim S.S. Primary cultures of chick osteocytes retain functional gap junctions between osteocytes and between osteocytes and osteoblasts. Microscopy and Microanalysis 2007, 13:108-117.
31. Kato Y., Boskey A., Spevak L., Dallas M., Hori M., Bonewald L.F. Establishment of an osteoid preosteocyte-like cell MLO-A5 that spontaneously mineralizes in culture. Journal of Bone and Mineral Research 2001, 16:1622-1633.
32. Kato Y., Windle J.J., Koop B.A., Mundy G.R., Bonewald L.F. Establishment of an osteocyte-like cell line, MLO-Y4. Journal of Bone and Mineral Research 1997, 12:2014-2023.
33. Khatiwala C.B., Peyton S.R., Putnam A.J. Intrinsic mechanical properties of the extracellular matrix affect the behavior of pre-osteoblastic MC3T3-E1 cells. American Journal of Physiology-Cell Physiology 2006, 290:C1640-C1650.
34. Khatiwala, C.B., Peyton, S.R., Putnam, A.J., 2006b. Osteogenic differentiation of Mc3t3-E1 cells regulated by substrate stiffness requires mapk activation. In: Proceedings of the Sixth Annual Meeting of the American Institute of Chemical Engineers, Cell Adhesion and Migration, San Francisco, CA, pp 338a.
35. Kim K., Dean D., Mikos A.G., Fisher J.P. Effect of initial cell seeding density on early osteogenic signal expression of rat bone marrow stromal cells cultured on cross-linked poly(propylene fumarate) disks. Biomacromolecules 2009, 10:1810-1817.
36. Klein-Nulend J., Der Plas V.A.N., Semeins A., Ajubi C., Frangos N., Nijweide J., Burger, E.P. Sensitivity of osteocytes to biomechanical stress in vitro. The FASEB Journal 1995, 9:441-445.
37. Kong, H.J., Polte, T.R., Alsberg, E., Mooney, D.J., 2005. FRET measurements of cell-traction forces and nano-scale clustering of adhesion ligands varied by substrate stiffness. Proceedings of the National Academy of Sciences of the United States of America 102, 4300-4305.
38. Kramer I., Halleux C., Keller H., Pegurri M., Gooi J.H., Weber P.B., Feng J.Q., Bonewald L.F., Kneissel M. Osteocyte Wnt/β-catenin signaling is required for normal bone homeostasis. Molecular and Cellular biology 2010, 30:3071-3085.
39. Krishnan V., Dhurjati R., Vogler E., Mastro A. Osteogenesis in vitro: from pre-osteoblasts to osteocytes. In Vitro Cellular & Developmental Biology-Animal 2010, 46:28-35.
40. Lanyon L.E. Osteocytes, strain detection, bone modeling and remodeling. Calcified Tissue International 1993, 53.
41. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2-δδCT method. Methods 2001, 25:402-408.
42. Lode A., Bernhardt A., GELINSKY M. Cultivation of human bone marrow stromal cells on three-dimensional scaffolds of mineralized collagen: influence of seeding density on colonization, proliferation and osteogenic differentiation. Journal of Tissue Engineering and Regenerative Medicine 2008, 2:400-407.
43. Marotti G., Palazzini S., Palumbo C., Ferretti M. Ultrastructural evidence of the existence of a dendritic network throughout the cells of the osteogenic lineage: the novel concept of wiring- and volume-transmission in bone. Bone 1996, 19. Suppl 3, 151S.
44. Mattinzoli D., Corbelli P.M.A., Ikehata M., Zennaro C., Armelloni S., Li M., Giardino L., Rastaldi M.P. A novel model of in vitro osteocytogenesis induced by retinoic acid treatment. European Cells and Materials 2012, 24:403-425.
45. McNamara L.M., Majeska R.J., Weinbaum S., Friedrich V., Schaffler M.B. Attachment of osteocyte cell processes to the bone matrix. The Anatomical Record: Advances in Integrative Anatomy and Evolutionary Biology 2009, 292:355-363.
46. Mikuni-Takagaki Y., Kakai Y., Satoyoshi M., Kawano E., Suzuki Y., Kawase T., Saito S. Matrix mineralization and the differentiation of osteocyte-like cells in culture. Journal of Bone and Mineral Research 1995, 10:231-242.
47. Nakano Y., Beertsen W., Vandenbos T., Kawamoto T., Oda K., Takano Y. Site-specific localization of two distinct phosphatases along the osteoblast plasma membrane: tissue non-specific alkaline phosphatase and plasma membrane calcium ATPase. Bone 2004, 35:1077-1085.
48. Oliver W.C., Pharr G.M. An improved technique for determining hardness and elastic modulus using load and displacement sensing indentation experiments. Journal of Materials Research 1992, 7:1564-1583.
49. Oshima A., Tanabe H., Yan T., Lowe G.N., Glackin C.A., Kudo A. A novel mechanism for the regulation of osteoblast differentiation: transcription of periostin, a member of the fasciclin I family, is regulated by the bHLH transcription factor, twist. Journal of Cellular Biochemistry 2002, 86:792-804.
50. Palazzini S., Palumbo C., Ferretti M., Marotti G. Stromal cell structure and relationships in perimedullary spaces of chick embryo shaft bones. Anatomy and Embryology 1998, 197:349-357.
51. Pelham, R.J., Wang, Y.-L., 1997. Cell locomotion and focal adhesions are regulated by substrate flexibility. Proceedings of the National Academy of Sciences of the United States of America 94, 13661-13665.
52. Poole K.E.S., Bezooijen V.A.N., Loveridge R.L., Hamersma N., Papapoulos H., Löwik S.E., Reeve, J.C.W. Sclerostin is a delayed secreted product of osteocytes that inhibits bone formation. The FASEB Journal 2005, 19:1842-1844.
53. Quarles L.D., Yohay D.A., Lever L.W., Caton R., Wenstrup R.J. Distinct proliferative and differentiated stages of murine MC3T3-E1 cells in culture: an in vitro model of osteoblast development. Journal of Bone and Mineral Research 1992, 7:683-692.
54. Rios H.F., Dusevich L.Y.,V., Eick D., Bonewald L.F., Feng J.Q. DMP1 is essential for osteocyte formation and function. Journal of Musculoskeletal & Neuronal Interactions 2005, 5:325-327.
55. Santos A., Bakker A., Willems H., Bravenboer N., Bronckers A., Klein-Nulend J. Mechanical loading stimulates BMP7, but not BMP2, production by osteocytes. Calcified Tissue International 2011, 89:318-326.
56. Stanford C.M., Jacobson P.A., Eanes E.D., Lembke L.A., Midura R.J. Rapidly forming apatitic mineral in an osteoblastic cell line (UMR 10601 BSP). Journal of Biological Chemistry 1995, 270:9420-9428.
57. Sudo H., Kodama H.A., Amagai Y., Yamamoto S., Kasai S. In vitro differentiation and calcification in a new clonal osteogenic cell line derived from newborn mouse calvaria. The Journal of Cell Biology 1983, 96:191-198.
58. Tanaka-Kamioka K., Kamioka H., Ris H., Lim S.-S. Osteocyte shape is dependent on actin filaments and osteocyte processes are unique actin-rich projections. Journal of Bone and Mineral Research 1998, 13:1555-1568.
59. Uchihashi K., Aoki S., Matsunobu A., Toda S. Osteoblast migration into type I collagen gel and differentiation to osteocyte-like cells within a self-produced mineralized matrix: a novel system for analyzing differentiation from osteoblast to osteocyte. Bone 2013, 52:102-110.
60. Weinreb M., Shinar D., Rodan G.A. Different pattern of alkaline phosphatase, osteopontin, and osteocalcin expression in developing rat bone visualized by in situ hybridization. Journal of Bone and Mineral Research 1990, 5:831-842.
61. Westbroek I., de Rooij K.E., Nijweide P.J. Osteocyte-specific monoclonal antibody MAb OB7.3 is directed against phex protein. Journal of Bone and Mineral Research 2002, 17:845-853.
62. Wilde J., Yokozeki M., Terai K., Kudo A., Moriyama K. The divergent expression of periostin mRNA in the periodontal ligament during experimental tooth movement. Cell and Tissue Research 2003, 312:345-351.
63. Wilson C.E., Dhert W.J.A., Blitterswijk V.a.n., Verbout, A.J.C.A., de Bruijn J.D. Evaluating 3D bone tissue engineered constructs with different seeding densities using the alamarBlue™ assay and the effect on in vivo bone formation. Journal of Materials Science: Materials in Medicine 2002, 13:1265-1269.
64. Winkler D.G., Sutherland M.K., Geoghegan J.C., Yu C., Hayes T., Skonier J.E., Shpektor D., Jonas M., Kovacevich B.R., Staehling-Hampton K., Appleby M., Brunkow M.E., Latham J.A. Osteocyte control of bone formation via sclerostin, a novel BMP antagonist. EMBO J 2003, 22:6267-6276.
65. Xiao Z., Zhang S., Mahlios J., Zhou G., Magenheimer B.S., Guo D., Dallas S.L., Maser R., Calvet J.P., Bonewald L., Quarles L.D. Cilia-like structures and polycystin-1 in osteoblasts/osteocytes and associated abnormalities in skeletogenesis and Runx2 expression. Journal of Biological Chemistry 2006, 281. (30884-30895).
66. Xie L. Streptolysin-O induces release of glycosylphosphatidylinositol-anchored alkaline phosphatase from ROS cells by vesiculation independently of phospholipase action. Biochemical Journal 1995, 305:529-537.
67. Yamaguchi D.T., Ma D., Lee A., Huang J., Gruber H.E. Isolation and characterization of gap junctions in the osteoblastic MC3T3-E1 cell line. Journal of Bone and Mineral Research 1994, 9:791-803.
68. Yang I.K., LU Y., Guo D., Harris M.A., Gluhak-Heinrich J., Bonewald L.F., Feng J.Q., Rowe D.W., Harris S.E. In vitro and in vivo study on osteocyte-specific mechanical signaling pathways. Journal of Musculoskeletal and Neuronal Interactions 2004, 4:386-387.
69. Yang M.A.H., Heinrich Jelica G.l.u.h.a.k., Dayong G.u.o., Bonewald Lynda F., Stephen a.n.d., Harris E. Gene expression signatures of a fibroblastoid preosteoblast and cuboidal osteoblast cell model compared to the MLO-Y4 osteocyte cell model. Bone 2009, 44:32-45.
70. Yellowley C.E., Li Z., Zhou Z., Jacobs C.R., Donahue H.J. Functional gap junctions between osteocytic and osteoblastic cells. Journal of Bone and Mineral Research 2000, 15:209-217.
71. Zhang K.,B.A.C., Ye L., Kotha S., Dallas M., Lu Y., ZHAO S., Harris M., Harris S.E., Feng J.Q., Bonewald L.F. E11/gp38 selective expression in osteocytes: regulation by mechanical strain and role in dendrite elongation. Molecular and Cellular biology 2006, 26:845-853.