Multi-directional differentiation potential of subpopulations of mesenchymal stem cells isolated from human skeletal muscle expressing different myogenic and endothelial markers

doi:10.3969/j.issn.2095-4344.2017.13.023

Abstract

Abstract:

BACKGROUND: Mesenchymal stem cells from human skeletal muscle exhibit multi-directional differentiation potential under the influence of osteogenic proteins such as bone morphogenetic protein 4 (BMP4). But the differentiation of a specific cell subpopulation is not yet clear.
OBJECTIVE: To characterize the multi-directional differentiation potential of mesenchymal stem cells from human skeletal muscle based on the expression of different surface markers.
METHODS: Four different subpopulations were isolated from the human skeletal muscle by fluorescence-activated cell sorting based on their expression of the myogenic-specific marker CD56 and the endothelial-specific markers CD34 and CD144, including CD56⁺, CD56⁺CD34⁺CD144⁺, CD34⁺CD144⁺, and unsorted groups. Osteogenic differentiation of the four groups of the cells was displayed by Von Kossa staining after the treatment with BMP4 alone or BMP4 plus transforming growth factor β3. Chondrogenic differentiation of these cells was displayed by Alcian blue staining. Bone metabolism was assessed by alkaline phosphatase staining.
RESULTS AND CONCLUSION: No significant difference in the bone metabolism was found among four groups after the treatment with BMP4 (P > 0.05). Osteogenic and chondrogenic potentials of the four cell subpopulations were significantly different. Under the same osteogenic induction, the CD56⁺ cells exhibited strongest potential for osteogenic differentiation; and under the same chondrogenic induction, the CD56⁺CD34⁺CD144⁺cells exhibited better potential for chondrogenic differentiation than the CD56⁺ cells. These findings indicate that the osteogenic and chondrogenic potentials are intimately associated with the type of mesenchymal stem cells from human skeletal muscle: the CD56⁺ cells are closely related to the osteogenic potential, while the CD56⁺CD34⁺CD144⁺ cells have stronger chondrogenic potential.

中国组织工程研究杂志出版内容重点：干细胞；骨髓干细胞；造血干细胞；脂肪干细胞；肿瘤干细胞；胚胎干细胞；脐带脐血干细胞；干细胞诱导；干细胞分化；组织工程

Key words: Stem Cells, Tissue Engineering, Cell Differentiation

CLC Number:

R394.2

Zhao Ya-guang, Li Yi, Song Zhuo-yue, Li Guang-heng. Multi-directional differentiation potential of subpopulations of mesenchymal stem cells isolated from human skeletal muscle expressing different myogenic and endothelial markers[J]. Chinese Journal of Tissue Engineering Research, 2017, 21(13): 2108-2113.

Figures/Tables 1

References

[1] Li G, Peng H, Corsi K, et al. Differential effect of BMP4 on NIH/3T3 and C2C12 cells: implications for endochondral bone formation. J Bone Miner Res. 2005;20(9):1611-1123.

[2] Li G, Zheng B, Meszaros LB, et al. Identification and characterization of chondrogenic progenitor cells in the fascia of postnatal skeletal muscle. J Mol Cell Biol. 2011;3(6):369-377.

[3] Afizah H, Hui JH. Mesenchymal stem cell therapy for osteoarthritis. Clin Transl Med. 2016;7(3):177-182.

[4] Stem cells may be coming therapy for bone and joint injuries. Post-traumatic arthritis (PTA), a form of osteoarthritis, may no longer be the norm following joint injury. Duke Med Health News. 2013;19(12):6.

[5] Ackerman IN, Osborne RH. Obesity and increased burden of hip and knee joint disease in Australia: results from a national survey. BMC Musculoskeletal Disorders. 2012;13:254.

[6] Barry F, Murphy M. Mesenchymal stem cells in joint disease and repair. Nat Rev Rheumatol. 2013;9(10):584-594.

[7] Grassel S, Lorenz J. Tissue-engineering strategies to repair chondral and osteochondral tissue in osteoarthritis: use of mesenchymal stem cells. Cur Rheumatol Rep. 2014;16(10): 452.

[8] Tuan RS, Boland G, Tuli R. Adult mesenchymal stem cells and cell-based tissue engineering. Arthritis Res Ther. 2003; 5(1):32-45.

[9] Wang Y, Yuan M, Guo QY, et al. Mesenchymal stem cells for treating articular cartilage defects and osteoarthritis. Cell Transplantation. 2015;24(9):1661-1678.

[10] Bashir J, Sherman A, Lee H, et al. Mesenchymal stem cell therapies in the treatment of musculoskeletal diseases. PM R. 2014;6(1):61-69.

[11] Burke J, Hunter M, Kolhe R, et al. Therapeutic potential of mesenchymal stem cell based therapy for osteoarthritis. 2016;5(1):27.

[12] Caldwell KL, Wang J. Cell-based articular cartilage repair: the link between development and regeneration. Osteoarthritis and cartilage. 2015;23(3):351-362.

[13] Crisan M, Yap S, Casteilla L, et al. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell stem cell. 2008;3(3):301-313.

[14] Kim YS, Choi YJ, Koh YG. Mesenchymal stem cell implantation in knee osteoarthritis: an assessment of the factors influencing clinical outcomes. Am J Sports Med. 2015; 43(9):2293-2301.

[15] Richardson SM, Kalamegam G, Pushparaj PN, et al. Mesenchymal stem cells in regenerative medicine: Focus on articular cartilage and intervertebral disc regeneration. Methods (San Diego, Calif). 2016;99:69-80.

[16] Desiderio V, Tirino V, Papaccio G, et al. Bone defects: molecular and cellular therapeutic targets. Int J Biochem Cell Biol. 2014;51:75-78.

[17] Elkhenany H, Amelse L, Caldwell M, et al. Impact of the source and serial passaging of goat mesenchymal stem cells on osteogenic differentiation potential: implications for bone tissue engineering. J Animal Sci Biotechnol. 2016;7:16.

[18] Zheng B, Cao B, Crisan M, et al. Prospective identification of myogenic endothelial cells in human skeletal muscle. Nat Biotechnol. 2007;25(9):1025-1034.

[19] Zhang S, Yap AU, Toh WS. Stem Cells for Temporomandibular Joint Repair and Regeneration. Stem Cell Rev. 2015;11(5):728-742.

[20] Redman SN, Oldfield SF, Archer CW. Current strategies for articular cartilage repair. Eur Cells Mater. 2005;9:23-32.

[21] Li Z, Kupcsik L, Yao SJ, et al. Mechanical load modulates chondrogenesis of human mesenchymal stem cells through the TGF-beta pathway. J Cell Mol Med. 2010;14(6a): 1338-1346.

[22] Gharaibeh B, Lu A, Tebbets J, et al. Isolation of a slowly adhering cell fraction containing stem cells from murine skeletal muscle by the preplate technique. Nat Protocols. 2008;3(9):1501-1509.

[23] Jeong J, Shin K, Lee SB, et al. Patient-tailored application for Duchene muscular dystrophy on mdx mice based induced mesenchymal stem cells. Exp Mol Pathol. 2014;97(2): 253-258.

[24] Steinert AF, Proffen B, Kunz M, et al. Hypertrophy is induced during the in vitro chondrogenic differentiation of human mesenchymal stem cells by bone morphogenetic protein-2 and bone morphogenetic protein-4 gene transfer. Arthritis Res Ther. 2009;11(5):R148.

[25] Camilleri ET, Gustafson MP, Dudakovic A, et al. Identification and validation of multiple cell surface markers of clinical-grade adipose-derived mesenchymal stromal cells as novel release criteria for good manufacturing practice-compliant production. Stem Cell Res Ther. 2016;7(1): 107.

[26] Mardones R, Jofre CM, Minguell JJ. Cell therapy and tissue engineering approaches for cartilage repair and/or regeneration. Int J Stem Cells. 2015;8(1):48-53.

[27] Molligan J, Mitchell R, Schon L, et al. Influence of bone and muscle injuries on the osteogenic potential of muscle progenitors: contribution of tissue environment to heterotopic ossification. Stem Cells Transl Med. 2016;5(6):745-753.

[28] Wyles CC, Houdek MT, Behfar A, et al. Mesenchymal stem cell therapy for osteoarthritis: current perspectives. Stem Cells Cloning. 2015;8:117-124.

[29] Savkovic V, Li H, Seon JK, et al. Mesenchymal stem cells in cartilage regeneration. Cur Stem Cell Res Ther. 2014;9(6): 469-488.

[30] Pers YM, Ruiz M, Noel D, et al. Mesenchymal stem cells for the management of inflammation in osteoarthritis: state of the art and perspectives. Osteoarthritis Cartilage. 2015;23(11): 2027-2035.

[31] 蔡明轩,王美辰,徐治成,等.神经细胞分泌因子促进骨骼肌细胞生长[J].中国组织工程研究,2016,20(42):6324-6329.

[32] Lv L, Ge W, Liu Y, et al. Lysine-specific demethylase 1 inhibitor rescues the osteogenic ability of mesenchymal stem cells under osteoporotic conditions by modulating H3K4 methylation. Bone Res. 2016;4:16037.

[33] Gu H, Xiong Z, Yin X, et al. Bone regeneration in a rabbit ulna defect model: use of allogeneic adipose-derivedstem cells with low immunogenicity. Cell Tissue Res. 2014;358(2): 453-464.

[34] Fu WL, Zhou CY, Yu JK. A new source of mesenchymal stem cells for articular cartilage repair: MSCs derived from mobilized peripheral blood share similar biological characteristics in vitro and chondrogenesis in vivo as MSCs from bone marrow in a rabbit model. Am J Sports Med. 2014; 42(3):592-601.

[35] Liu Y, Ming L, Luo H, et al. Integration of a calcined bovine bone and BMSC-sheet 3D scaffold and the promotion of bone regeneration in large defects. Biomaterials. 2013;34(38): 9998-10006.

[36] Zhi W, Zhang C, Duan K, et al. A novel porous bioceramics scaffold by accumulating hydroxyapatite spherulites for large bone tissue engineering in vivo. II. Construct large volume of bone grafts. J Biomed Mater Res A. 2014;102(8):2491-501.

[37] Zhao Z, Wang Y, Peng J, et al. Improvement in nerve regeneration through a decellularized nerve graft by supplementation with bone marrow stromal cells in fibrin. Cell Transplant. 2014;23(1):97-110.

[38] Fu WL, Jia ZQ, Wang WP, et al. Proliferation and apoptosis property of mesenchymal stem cells derived from peripheral blood under the culture conditions of hypoxia and serum deprivation. Chin Med J (Engl). 2011;124(23):3959-3967.

[39] Zhang Y, Wang F, Chen J, et al. Bone marrow-derived mesenchymal stem cells versus bone marrow nucleated cells in the treatment of chondral defects. Int Orthop. 2012;36(5): 1079-1086.