Enhanced osteogenesis of human mesenchymal stem cells by periodic heat shock in self-assembling peptide hydrogel

Tissue Engineering - Part A

Volumn 19, Issue 5-6, 2013, Pages 716-728

  Chen, Jing ^a   Shi, Zhong Dong ^a   Ji, Xinying ^a   Morales, Jorge ^b   Zhang, Jingwei ^a   Kaur, Navneet ^a   Wang, Sihong ^a  

^a City College of New York   (United States)

^b CITY COLLEGE OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE; HYDROGELS; PEPTIDES; PHOSPHATASES; STEM CELLS; THREE DIMENSIONAL COMPUTER GRAPHICS; TISSUE CULTURE; TISSUE ENGINEERING; TRANSCRIPTION FACTORS;

3D CULTURE; ALKALINE PHOSPHATASE ACTIVITY; BONE MORPHOGENETIC PROTEIN-2; BONE REGENERATION; BONE TISSUE ENGINEERING; CALCIUM DEPOSITION; CULTURE PLATES; HEAT SHOCK PROTEIN 70; HEAT-SHOCK; HUMAN BONE MARROW; HUMAN MESENCHYMAL STEM CELLS; IN-VIVO; OSTEOGENESIS; OSTEOGENIC DIFFERENTIATION; OSTEOPONTIN; OSTERIX; PEPTIDE HYDROGELS; PURAMATRIX; SELF-ASSEMBLING PEPTIDES; THERMAL REGULATION; TISSUE CULTURE PLATES;

TWO DIMENSIONAL;

ALKALINE PHOSPHATASE; BIOLOGICAL MARKER; CALCIUM; HEAT SHOCK PROTEIN; MINERAL; PEPTIDE; RADA16 I; RADA16-I; HYDROGEL;

ADULT; ARTICLE; BONE DEVELOPMENT; BONE MINERALIZATION; CELL DIFFERENTIATION; CELL SEPARATION; CELL SHAPE; CYTOLOGY; DRUG EFFECT; ENZYMOLOGY; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; GENETICS; HEAT SHOCK RESPONSE; HUMAN; HYDROGEL; MESENCHYMAL STROMA CELL; METABOLISM; STAINING; DRUG EFFECTS; PHARMACOLOGY;

ADULT; ALKALINE PHOSPHATASE; BIOLOGICAL MARKERS; CALCIFICATION, PHYSIOLOGIC; CALCIUM; CELL DIFFERENTIATION; CELL SEPARATION; CELL SHAPE; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; HEAT-SHOCK PROTEINS; HEAT-SHOCK RESPONSE; HUMANS; HYDROGEL; MESENCHYMAL STROMAL CELLS; MINERALS; OSTEOGENESIS; PEPTIDES; STAINING AND LABELING;

EID: 84873300146     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2012.0070     Document Type: Article

References (53)

1. Kraus, V.B. Pathogenesis and treatment of osteoarthritis. Med Clin N Am 81, 85, 1997
2. Marion, N.W., and Mao, J.J. Mesenchymal stem cells and tissue engineering. In: Lanza, R., and Klimanskaya, I., eds. Stem Cell Tools and Other Experimental Protocols. San Diego: Elsevier Academic Press, Inc., 2006, pp. 339-361
3. Shen FH, Z.Q., Lv, Q., Choi, L., Balian, G., Li, X., and Laurencin, C.T. Osteogenic differentiation of adipose-derived stromal cells treated with GDF-5 cultured on a novel three-dimensional sintered microsphere matrix. Spine J 6, 615, 2006
4. Misawa, H., Kobayashi, N., Soto-Gutierrez, A., Chen, Y., Yoshida, A., Rivas-Carrillo, J.D., et al. PuraMatrix (TM) fa-cilitates bone regeneration in bone defects of calvaria in mice. Cell Transplant 15, 2006
5. Mao, J.J. Stem-cell-driven regeneration of synovial joints. Biol Cell 97, 2005
6. Shih, Y.R.V., Chen, C.N., Tsai, S.W., Wang, Y.J., and Lee, O.K. Growth of mesenchymal stem cells on electrospun type I collagen nanofibers. Stem Cells 24, 2006
7. Hamada, K., Hirose, M., Yamashita, T., and Ohgushil, H. Spatial distribution of mineralized bone matrix produced by marrow mesenchymal stem cells in self-assembling peptide hydrogel scaffold. J Biomed Mater Res Part A 84A, 2008
8. Kim, H.K., Shim, W.S., Kim, S.E., Lee, K.H., Kang, E., Kim, J.H., et al. Injectable in situ-forming pH/thermo-sensitive hy-drogel for bone tissue engineering. Tissue Eng Part A 15, 2009
9. Moreau, J.L., and Xu, H.H.K. Mesenchymal stem cell pro-liferation and differentiation on an injectable calcium phos-phate-chitosan composite scaffold. Biomaterials 30, 2009
10. Chun, C., Lim, H.J., Hong, K.Y., Park, K.H., and Song, S.C The use of injectable, thermosensitive poly(organophosphazene)-RGD conjugates for the enhancement of mesenchymal stem cell osteogenic differentiation. Biomaterials 30, 2009
11. Alhadlaq, A., and Mao, J.J. Mesenchymal stem cells: isola-tion and therapeutics. Stem Cells Dev 13, 2004
12. Kratchmarova, I., Blagoev, B., Haack-Sorensen, M., Kassem, M., and Mann, M. Mechanism of divergent growth factor effects in mesenchymal stem cell differentiation. Science 308, 2005
13. Hughes, F.J., Turner, W., Belibasakis, G., and Martuscelli, G. Effects of growth factors and cytokines on osteoblast dif-ferentiation. Periodontol 2000 41, 2006
14. David, V., Martin, A., Lafage-Proust, M.H., Malaval, L., Peyroche, S., Jones, D.B., et al. Mechanical loading down-regulates peroxisome proliferator-activated receptor gamma in bone marrow stromal cells and favors osteoblastogenesis at the expense of adipogenesis. Endocrinology 148, 2007
15. Ogawa, H. [Effects of the localized thermal enhancement on new bone formation following mechanical expansion of the rat sagittal suture]. Nippon Kyosei Shika Gakkai Zasshi 49, 1990
16. Brookes, M., Richards, D.J., and Singh, M. Vascular sequelae of experimental osteotomy. Angiology 21, 1970
17. Takahashi, K.A., Tonomura, H., Arai, Y., Terauchi, R, Honjo, K., Hiraoka, N., et al. Hyperthermia for the treatment of articular cartilage with osteoarthritis. Int J Hyperthermia 25, 2009
18. Doyle, J.R., and Smart, B.W. Stimulation of bone growth by short-wave diathermy. J Bone Joint Surg-Am Vol 45, 1963
19. Richards, V., and Stofer, R The stimulation of bone growth by internal heating. Surgery 46, 1959
20. Brodin, H. Longitudinal bone growth, the nutrition of the epiphyseal cartilages and the local blood supply; an experi-mental study in the rabbit. Acta Orthop Scand Suppl 20,1955
21. Shui C, S.A. Mild heat shock induces proliferation, alkaline phosphatase activity, and mineralization in human bone marrow stromal cells and Mg-63 cells in vitro. J Bone Miner Res 16, 731, 2001
22. Ye, C.P., Heng, B.C., Liu, H., Toh, W.S., and Cao, T. Culture media conditioned by heat-shocked osteoblasts enhances the osteogenesis of bone marrow-derived mesenchymal stromal cells. Cell Biochem Funct 25, 2007
23. Nørgaard, R., Kassem, M., Rattan, S.I. Heat shock-induced enhancement of osteoblastic differentiation of hTERT-immortalized mesenchymal stem cells. Ann N Y Acad Sci 1067, 443, 2006
24. Trieb, K., Blahovec, H., and Kubista, B. Effects of hyper-thermia on heat shock protein expression, alkaline phos-phatase activity and proliferation in human osteosarcoma cells. Cell Biochem Funct 25, 2007
25. Genove, E., Shen, C., Zhang, S.G., and Semino, C.E. The effect of functionalized self-assembling peptide scaffolds on human aortic endothelial cell function. Biomaterials 26,2005
26. Elastic properties and Young's modulus for some materials. www.engineeringtoolbox.com/young-modulus-d-417.html
27. Winer, J.P., Janmey, P.A., McCormick, M.E., and Funaki, M. Bone marrow-derived human mesenchymal stem cells be-come quiescent on soft substrates but remain responsive to chemical or mechanical stimuli. Tissue Eng Part A 15, 2009
28. Zhang, S.G., Holmes, T., Lockshin, C., and Rich, A. Spon-taneous assembly of a self-complementary oligopeptide to form a stable macroscopic membrane. Proc Natl Acad Sci USA90, 1993
29. Zhang, S.G., Holmes, T.C., Dipersio, C.M., Hynes, R.O., Su, X., and Rich, A. Self-complementary oligopeptide matrices support mammalian-cell attachment. Biomaterials 16, 1995
30. Semino, C.E., Kasahara, J., Hayashi, Y., and Zhang, S.G Entrapment of migrating hippocampal neural cells in three-dimensional peptide nanofiber scaffold. Tissue Eng 10, 2004
31. Wang, S., Nagrath, D., Chen, P.C., Berthiaume, F., and Yarmush, M.L. Three-dimensional primary hepatocyte cul-ture in synthetic self-assembling peptide hydrogel. Tissue Eng Part A 14, 2008
32. Semino, C.E., Merok, J.R., Crane, G.G., Panagiotakos, G., and Zhang, S.G. Functional differentiation of hepatocyte-like spheroid structures from putative liver progenitor cells in three-dimensional peptide scaffolds. Differentiation 71, 2003
33. Kisiday, J., Jin, M., Kurz, B., Hung, H., Semino, C., Zhang, S., et al. Self-assembling peptide hydrogel fosters chondrocyte extracellular matrix production and cell division: implica-tions for cartilage tissue repair. Proc Natl Acad Sci U S A 99, 2002
34. Bokhari, M.A., Akay, G., Zhang, S.G., and Birch, M.A. En-hancement of osteoblast growth and differentiation in vitro on a peptide hydrogel-polyHIPE polymer hybrid material. Biomaterials 26, 2005
35. Dickhut, A., Gottwald, E., Steck, E., Heisel, C., and Richter, W. Chondrogenesis of mesenchymal stem cells in gel-like biomaterials in vitro and in vivo. Front Biosci 13, 2008
36. Erickson, I.E., Huang, A.H., Chung, C., Li, R.T., Burdick, J.A., and Mauck, R.L. Differential maturation and structure-function relationships in mesenchymal stem cell- and chondrocyte-seeded hydrogels. Tissue Eng Part A 15, 2009
37. Yoshimi, R., Yamada, Y., Ito, K., Nakamura, S., Abe, A., Nagasaka, T., et al. Self-assembling peptide nanofiber scaf-folds, platelet-rich plasma, and mesenchymal stem cells for injectable bone regeneration with tissue engineering. J Cra-niofac Surg 20, 2009
38. Lim, C.L., Byrne, C., and Lee, J.K.W. Human thermoregu-lation and measurement of body temperature in exercise and clinical settings. Ann Acad Med Singap 37, 2008
39. Jaiswal, N., Haynesworth, S.E., Caplan, A.I., and Bruder, S.P. Osteogenic differentiation of purified, culture-expanded human mesenchymal stem cells in vitro. J Cell Biochem 64, 1997
40. Goldstein, J., Newbury, D., Joy, D., Lyman, C., Echlin, P., Lifshin, et al. Scanning Electron Microscopy and X-Ray Mi-croanalysis, third edition. New York: Springer, 2003
41. Hee, C.K., Jonikas, M.A., and Nicoll, S.B. Influence of three-dimensional scaffold on the expression of osteogenic differ-entiation markers by human dermal fibroblasts. Biomaterials 27, 2006
42. Hirata, A., Sugahara, T., and Nakamura, H. Localization of Runx2, osterix, and osteopontin in tooth root formation in rat molars. J Histochem Cytochem 57, 2009
43. Johnsen, S.A., Subramaniam, M., Ruesink, T.J., and Spels-berg, T.C. Opposing roles of osterix and TGF beta inducible early gene in osteoblast differentiation downstream of Cbfa1/Runx2. J Bone Miner Res 17, 2002
44. Cao, Y., Zhou, Z.C., de Crombrugghe, B., Nakashima, K., Guan, H., Duan, X.P., et al. Osterix, a transcription factor for osteoblast differentiation, mediates antitumor activity in murine osteosarcoma. Cancer Res 65, 2005
45. Nakamura, H., Kenmotsu, S., Sakai, H., and Ozawa, H. Localization of CD44, the hyaluronate receptor, on the plasma-membrane of osteocytes and osteoclasts in rat tibiae. Cell Tissue Res 280, 1995
46. Friedman, M.S., Long, M.W., and Hankenson, K.D. Osteo-genic differentiation of human mesenchymal stem cells is regulated by bone morphogenetic protein-6. J Cell Biochem 98, 2006
47. Kern, B., Shen, J.H., Starbuck, M., and Karsenty, G. Cbfa1 contributes to the osteoblast-specific expression of type I collagen genes. J Biol Chem 276, 2001
48. Even-Ram, S., Artym, V., and Yamada, K.M. Matrix control of stem cell fate. Cell 126, 2006
49. Kostenko, S., and Moens, U. Heat shock protein 27 phos-phorylation: kinases, phosphatases, functions and pathol-ogy. Cell Mol Life Sci 66, 2009
50. Turturici, G., Geraci, F., Candela, M.E., Giudice, G., Gon-zalez, F., and Sconzo, G. Hsp70 localizes differently from chaperone Hsc70 in mouse mesoangioblasts under physio-logical growth conditions. J Mol Histol 39, 2008
51. Sreedhar, A.S., Kalmar, E., Csermely, P., and Shen, Y.F. Hsp90 isoforms: functions, expression and clinical impor-tance. FEBS Lett 562, 2004
52. Hilscher, B., and Hilscher, W. Kinetics of gametogenesis .2. Comparative autoradiographic studies of oogonia and multiplying prospermatogonia of wistar rat. Cell Tissue Res 190, 1978
53. Vanmuylder, N., Werry-Huet, A., Rooze, M., and Louryan, S. Heat shock protein HSP86 expression during mouse em-bryo development, especially in the germ-line. Anat Em-bryol 205, 2002