Exosomes/tricalcium phosphate combination scaffolds can enhance bone regeneration by activating the PI3K/Akt signaling pathway

Stem Cell Research and Therapy

Volumn 7, Issue 1, 2016, Pages

  Zhang, Jieyuan ^a   Liu, Xiaolin ^a   Li, Haiyan ^b   Chen, Chunyuan ^c   Hu, Bin ^a   Niu, Xin ^a   Li, Qing ^a   Zhao, Bizeng ^a   Xie, Zongping ^a   Wang, Yang ^a  

^a SHANGHAI JIAO TONG UNIVERSITY AFFILIATED SIXTH PEOPLE S HOSPITAL   (China)

^b SHANGHAI JIAO TONG UNIVERSITY   (China)

^c NANCHANG UNIVERSITY   (China)

Author keywords

Bone regeneration; Exosomes; iPS MSCs; Microarray; PI3K Akt; Tricalcium phosphate

Indexed keywords

ALIZARIN RED S; ALKALINE PHOSPHATASE; CALCIUM PHOSPHATE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOINFORMATICS; BONE DEFECT; BONE DEVELOPMENT; BONE MARROW DERIVED MESENCHYMAL STEM CELL; BONE REGENERATION; BONE REMODELING; CALVARIA; CELL COUNTING; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVATION; EXOSOME; GENE EXPRESSION PROFILING; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IN VITRO STUDY; INDUCED PLURIPOTENT STEM CELL; INTERNALIZATION; NONHUMAN; PRIORITY JOURNAL; RAT; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TISSUE SCAFFOLD; ANIMAL; CELL CULTURE; CELL DIFFERENTIATION; CELL MOTION; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; INJURIES; MESENCHYMAL STROMA CELL; METABOLISM; SECRETION (PROCESS); SKULL; SPRAGUE DAWLEY RAT; TRANSPLANTATION;

ANIMALS; BONE REGENERATION; CALCIUM PHOSPHATES; CELL DIFFERENTIATION; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; EXOSOMES; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MESENCHYMAL STROMAL CELLS; OSTEOGENESIS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; SKULL; TISSUE SCAFFOLDS;

EID: 84988603175     PISSN: None     EISSN: 17576512     Source Type: Journal    
DOI: 10.1186/s13287-016-0391-3     Document Type: Article

References (46)

1. Arrington ED, Smith WJ, Chambers HG, Bucknell AL, Davino NA. Complications of iliac crest bone graft harvesting. Clin Orthop Relat Res. 1996;(329):300-9.
2. Berrey Jr BH, Lord CF, Gebhardt MC, Mankin HJ. Fractures of allografts. Frequency, treatment, and end-results. J Bone Joint Surg Am. 1990;72(6):825-33.
3. Fujibayashi S, Kim HM, Neo M, Uchida M, Kokubo T, Nakamura T. Repair of segmental long bone defect in rabbit femur using bioactive titanium cylindrical mesh cage. Biomaterials. 2003;24(20):3445-51.
4. Zhou H, Xiao C, Wang Y, Bi X, Ge S, Fan X. In vivo efficacy of bone marrow stromal cells coated with beta-tricalcium phosphate for the reconstruction of orbital defects in canines. Invest Ophthalmol Vis Sci. 2011;52(3):1735-41.
5. Katagiri W, Osugi M, Kawai T, Hibi H. First-in-human study and clinical case reports of the alveolar bone regeneration with the secretome from human mesenchymal stem cells. Head Face Med. 2016;12(1):5.
6. Yuan H, Fernandes H, Habibovic P, de Boer J, Barradas AM, de Ruiter A, et al. Osteoinductive ceramics as a synthetic alternative to autologous bone grafting. Proc Natl Acad Sci U S A. 2010;107(31):13614-9.
7. Zhang J, Guan J, Zhang C, Wang H, Huang W, Guo S, et al. Bioactive borate glass promotes the repair of radius segmental bone defects by enhancing the osteogenic differentiation of BMSCs. Biomed Mater. 2015;10(6):065011.
8. Han P, Xu M, Chang J, Chakravorty N, Wu C, Xiao Y. Lithium release from beta-tricalcium phosphate inducing cementogenic and osteogenic differentiation of both hPDLCs and hBMSCs. Biomater Sci. 2014;2:1230-43.
9. Guan J, Zhang J, Zhu Z, Niu X, Guo S, Wang Y, et al. Bone morphogenetic protein 2 gene transduction enhances the osteogenic potential of human urine-derived stem cells. Stem Cell Res Ther. 2015;6:5.
10. Kamolz LP, Keck M, Kasper C. Wharton's jelly mesenchymal stem cells promote wound healing and tissue regeneration. Stem Cell Res Ther. 2014;5(3):62.
11. Liang X, Ding Y, Zhang Y, Tse HF, Lian Q. Paracrine mechanisms of mesenchymal stem cell-based therapy: current status and perspectives. Cell Transplant. 2014;23(9):1045-59.
12. Baglio SR, Pegtel DM, Baldini N. Mesenchymal stem cell secreted vesicles provide novel opportunities in (stem) cell-free therapy. Front Physiol. 2012;3:359.
13. Hu GW, Li Q, Niu X, Hu B, Liu J, Zhou SM, et al. Exosomes secreted by human-induced pluripotent stem cell-derived mesenchymal stem cells attenuate limb ischemia by promoting angiogenesis in mice. Stem Cell Res Ther. 2015;6:10.
14. De Jong OG, Van Balkom BW, Schiffelers RM, Bouten CV, Verhaar MC. Extracellular vesicles: potential roles in regenerative medicine. Front Immunol. 2014;5:608.
15. Nakamura Y, Miyaki S, Ishitobi H, Matsuyama S, Nakasa T, Kamei N, et al. Mesenchymal-stem-cell-derived exosomes accelerate skeletal muscle regeneration. FEBS Lett. 2015;589(11):1257-65.
16. Zhang B, Yin Y, Lai RC, Tan SS, Choo AB, Lim SK. Mesenchymal stem cells secrete immunologically active exosomes. Stem Cells Dev. 2014;23(11):1233-44.
17. Jiang ZZ, Liu YM, Niu X, Yin JY, Hu B, Guo SC, et al. Exosomes secreted by human urine-derived stem cells could prevent kidney complications from type I diabetes in rats. Stem Cell Res Ther. 2016;7(1):24.
18. Burger D, Vinas JL, Akbari S, Dehak H, Knoll W, Gutsol A, et al. Human endothelial colony-forming cells protect against acute kidney injury: role of exosomes. Am J Pathol. 2015;185(8):2309-23.
19. Xin H, Li Y, Chopp M. Exosomes/miRNAs as mediating cell-based therapy of stroke. Front Cell Neurosci. 2014;8:377.
20. Doeppner TR, Herz J, Gorgens A, Schlechter J, Ludwig AK, Radtke S, et al. Extracellular vesicles improve post-stroke neuroregeneration and prevent postischemic immunosuppression. Stem Cells Transl Med. 2015;4(10):1131-43.
21. Lian Q, Zhang Y, Zhang J, Zhang HK, Wu X, Zhang Y, et al. Functional mesenchymal stem cells derived from human induced pluripotent stem cells attenuate limb ischemia in mice. Circulation. 2010;121(9):1113-23.
22. Fu QL, Chow YY, Sun SJ, Zeng QX, Li HB, Shi JB, et al. Mesenchymal stem cells derived from human induced pluripotent stem cells modulate T-cell phenotypes in allergic rhinitis. Allergy. 2012;67(10):1215-22.
23. Villa-Diaz LG, Brown SE, Liu Y, Ross AM, Lahann J, Parent JM, et al. Derivation of mesenchymal stem cells from human induced pluripotent stem cells cultured on synthetic substrates. Stem Cells. 2012;30(6):1174-81.
24. Zhang J, Guan J, Niu X, Hu G, Guo S, Li Q, et al. Exosomes released from human induced pluripotent stem cells-derived MSCs facilitate cutaneous wound healing by promoting collagen synthesis and angiogenesis. J Transl Med. 2015;13:49.
25. Zou L, Luo Y, Chen M, Wang G, Ding M, Petersen CC, et al. A simple method for deriving functional MSCs and applied for osteogenesis in 3D scaffolds. Sci Rep. 2013;3:2243.
26. Ghosh-Choudhury N, Abboud SL, Nishimura R, Celeste A, Mahimainathan L, Choudhury GG. Requirement of BMP-2-induced phosphatidylinositol 3-kinase and Akt serine/threonine kinase in osteoblast differentiation and Smad-dependent BMP-2 gene transcription. J Biol Chem. 2002;277(36):33361-8.
27. Fujita T, Azuma Y, Fukuyama R, Hattori Y, Yoshida C, Koida M, et al. Runx2 induces osteoblast and chondrocyte differentiation and enhances their migration by coupling with PI3K-Akt signaling. J Cell Biol. 2004;166(1):85-95.
28. Suzuki E, Ochiai-Shino H, Aoki H, Onodera S, Saito A, Saito A, et al. Akt activation is required for TGF-beta1-induced osteoblast differentiation of MC3T3-E1 pre-osteoblasts. PLoS One. 2014;9(12), e112566.
29. Yokota J, Chosa N, Sawada S, Okubo N, Takahashi N, Hasegawa T, et al. PDGF-induced PI3K-mediated signaling enhances the TGF-beta-induced osteogenic differentiation of human mesenchymal stem cells in a TGF-beta-activated MEK-dependent manner. Int J Mol Med. 2014;33(3):534-42.
30. Radcliff K, Tang TB, Lim J, Zhang Z, Abedin M, Demer LL, et al. Insulin-like growth factor-I regulates proliferation and osteoblastic differentiation of calcifying vascular cells via extracellular signal-regulated protein kinase and phosphatidylinositol 3-kinase pathways. Circ Res. 2005;96(4):398-400.
31. Debiais F, Lefevre G, Lemonnier J, Le Mee S, Lasmoles F, Mascarelli F, et al. Fibroblast growth factor-2 induces osteoblast survival through a phosphatidylinositol 3-kinase-dependent, -beta-catenin-independent signaling pathway. Exp Cell Res. 2004;297(1):235-46.
32. Osugi M, Katagiri W, Yoshimi R, Inukai T, Hibi H, Ueda M. Conditioned media from mesenchymal stem cells enhanced bone regeneration in rat calvarial bone defects. Tissue Eng Part A. 2012;18(13-14):1479-89.
33. Wang KX, Xu LL, Rui YF, Huang S, Lin SE, Xiong JH, et al. The effects of secretion factors from umbilical cord derived mesenchymal stem cells on osteogenic differentiation of mesenchymal stem cells. PLoS One. 2015;10(3), e0120593.
34. Lai RC, Arslan F, Lee MM, Sze NS, Choo A, Chen TS, et al. Exosome secreted by MSC reduces myocardial ischemia/reperfusion injury. Stem Cell Res. 2010;4(3):214-22.
35. Zhang Y, Chopp M, Meng Y, Katakowski M, Xin H, Mahmood A, et al. Effect of exosomes derived from multipluripotent mesenchymal stromal cells on functional recovery and neurovascular plasticity in rats after traumatic brain injury. J Neurosurg. 2015;122(4):856-67.
36. Rahman MJ, Regn D, Bashratyan R, Dai YD. Exosomes released by islet-derived mesenchymal stem cells trigger autoimmune responses in NOD mice. Diabetes. 2014;63(3):1008-20.
37. Zou D, Zhang Z, He J, Zhu S, Wang S, Zhang W, et al. Repairing critical-sized calvarial defects with BMSCs modified by a constitutively active form of hypoxia-inducible factor-1alpha and a phosphate cement scaffold. Biomaterials. 2011;32(36):9707-18.
38. Wang Y, Han ZB, Song YP, Han ZC. Safety of mesenchymal stem cells for clinical application. Stem Cells Int. 2012;2012:652034.
39. Lai RC, Arslan F, Tan SS, Tan B, Choo A, Lee MM, et al. Derivation and characterization of human fetal MSCs: an alternative cell source for large-scale production of cardioprotective microparticles. J Mol Cell Cardiol. 2010;48(6):1215-24.
40. Lai RC, Yeo RW, Tan KH, Lim SK. Mesenchymal stem cell exosome ameliorates reperfusion injury through proteomic complementation. Regen Med. 2013;8(2):197-209.
41. Deschaseaux F, Sensebe L, Heymann D. Mechanisms of bone repair and regeneration. Trends Mol Med. 2009;15(9):417-29.
42. Camussi G, Deregibus MC, Bruno S, Cantaluppi V, Biancone L. Exosomes/microvesicles as a mechanism of cell-to-cell communication. Kidney Int. 2010;78(9):838-48.
43. Zhang B, Wang M, Gong A, Zhang X, Wu X, Zhu Y, et al. HucMSC-exosome mediated-Wnt4 signaling is required for cutaneous wound healing. Stem Cells. 2015;33(7):2158-68.
44. Shabbir A, Cox A, Rodriguez-Menocal L, Salgado M, Van Badiavas E. Mesenchymal stem cell exosomes induce proliferation and migration of normal and chronic wound fibroblasts, and enhance angiogenesis in vitro. Stem Cells Dev. 2015;24(14):1635-47.
45. Tsai KS, Kao SY, Wang CY, Wang YJ, Wang JP, Hung SC. Type I collagen promotes proliferation and osteogenesis of human mesenchymal stem cells via activation of ERK and Akt pathways. J Biomed Mater Res A. 2010;94(3):673-82.
46. Zhou F, Yang Y, Xing D. Bcl-2 and Bcl-xL play important roles in the crosstalk between autophagy and apoptosis. FEBS J. 2011;278(3):403-13.