Impact of Ultrasound Therapy on Stem Cell Differentiation - A Systematic Review

Author(s): Abdollah Amini, Sufan Chien*, Mohammad Bayat*

Journal Name: Current Stem Cell Research & Therapy

Volume 15 , Issue 5 , 2020


Become EABM
Become Reviewer
Call for Editor

Abstract:

Objective: This is a systematic review of the effects of low-intensity pulsed ultrasound (LIPUS) on stem cell differentiation.

Background Data: Recent studies have investigated several types of stem cells from different sources in the body. These stem cells should strictly be certified and promoted for cell therapies before being used in medical applications. LIPUS has been used extensively in treatment centers and in research to promote stem cell differentiation, function, and proliferation.

Materials and Methods: The databases of PubMed, Google Scholar, and Scopus were searched for abstracts and full-text scientific papers published from 1989-2019 that reported the application of LIPUS on stem cell differentiation. Related English language articles were found using the following defined keywords: low-intensity pulsed ultrasound, stem cell, differentiation. Criteria for inclusion in the review were: LIPUS with frequencies of 1–3 MHz and pulsed ultrasound intensity of <500 mW/cm2. Duration, exposure time, and cell sources were taken into consideration.

Results: Fifty-two articles were selected based on the inclusion criteria. Most articles demonstrated that the application of LIPUS had positive effects on stem cell differentiation. However, some authors recommended that LIPUS combined with other physical therapy aides was more effective in stem cell differentiation.

Conclusion: LIPUS significantly increases the level of stem cell differentiation in cells derived mainly from bone marrow mesenchymal stem cells. There is a need for further studies to analyze the effect of LIPUS on cells derived from other sources, particularly adipose tissue-derived mesenchymal stem cells, for treating hard diseases, such as osteoporosis and diabetic foot ulcer. Due to a lack of reporting on standard LIPUS parameters in the field, more experiments comparing the protocols for standardization of LIPUS parameters are needed to establish the best protocol, which would allow for the best results.

Keywords: Low-Intensity pulsed ultrasound, stem cell, stem cell differentiation, mesenchymal stem cells, embryonic stem cells, induced pluripotent stem cells, adult stem cells.

[1]
Mao AS, Mooney DJ. Regenerative medicine: Current therapies and future directions. Proc Natl Acad Sci USA 2015; 112(47): 14452-9.
[http://dx.doi.org/10.1073/pnas.1508520112]
[2]
Dąbrowska AM, Skopiński P. Stem cells in regenerative medicine - from laboratory to clinical application - the eye. Cent Eur J Immunol 2017; 42(2): 173-80.
[http://dx.doi.org/10.5114/ceji.2017.69360]
[3]
Cerqueira MT, Pirraco RP, Marques AP. Stem cells in skin wound healing: are we there yet? Adv Wound Care (New Rochelle) 2016; 5(4): 164-75.
[http://dx.doi.org/10.1089/wound.2014.0607]
[4]
Tuan RS, Boland G, Tuli R. Adult mesenchymal stem cells and cell-based tissue engineering. Arthritis Res Ther 2003; 5(1): 32-45.
[http://dx.doi.org/10.1186/ar614]
[5]
Fekrazad R, Asefi S, Allahdadi M, Kalhori KA. Effect of photo-biomodulation on mesenchymal stem cells. Photomed Laser Surg 2016; 34(11): 533-42.
[http://dx.doi.org/10.1089/pho.2015.4029]
[6]
van Dartel DA, Zeijen NJ, de la Fonteyne LJ, van Schooten FJ, Piersma AH. Disentangling cellular proliferation and differentiation in the embryonic stem cell test, and its impact on the experimental protocol. Reprod Toxicol 2009; 28(2): 254-61.
[http://dx.doi.org/10.1016/j.reprotox.2009.03.017]
[7]
Baksh D, Song L, Tuan RS. Adult mesenchymal stem cells: characterization, differentiation, and application in cell and gene therapy. J Cell Mol Med 2004; 8(3): 301-16.
[http://dx.doi.org/10.1111/j.1582-4934.2004.tb00320.x]
[8]
Wu Y, Chen L, Scott PG, Tredget EE. Mesenchymal stem cells enhance wound healing through differentiation and angiogenesis. Stem Cells 2007; 25(10): 2648-59.
[http://dx.doi.org/10.1634/stemcells.2007-0226]
[9]
Altman GH, Horan RL, Martin I, et al. Cell differentiation by mechanical stress. FASEB J 2002; 16(2): 270-2.
[http://dx.doi.org/10.1096/fj.01-0656fje]
[10]
Stein A, Benayahu D, Maltz L, Oron U. Low-level laser irradiation promotes proliferation and differentiation of human osteoblasts in vitro. Photomed Laser Surg 2005; 23(2): 161-6.
[http://dx.doi.org/10.1089/pho.2005.23.161]
[11]
Hou JF, Zhang H, Yuan X, Li J, Wei YJ, Hu SS. In vitro effects of low-level laser irradiation for bone marrow mesenchymal stem cells: proliferation, growth factors secretion and myogenic differentiation. Lasers Surg Med 2008; 40(10): 726-33.
[http://dx.doi.org/10.1002/lsm.20709]
[12]
Hawkins D, Houreld N, Abrahamse H. Low level laser therapy (LLLT) as an effective therapeutic modality for delayed wound healing. Ann N Y Acad Sci 2005; 1056(1): 486-93.
[http://dx.doi.org/10.1196/annals.1352.040]
[13]
Ginani F, Soares DM, Barreto MP, Barboza CA. Effect of low-level laser therapy on mesenchymal stem cell proliferation: a systematic review. Lasers Med Sci 2015; 30(8): 2189-94.
[http://dx.doi.org/10.1007/s10103-015-1730-9]
[14]
Bayat M, Virdi A, Rezaei F, Chien S. Comparison of the in vitro effects of low-level laser therapy and low-intensity pulsed ultrasound therapy on bony cells and stem cells. Prog Biophys Mol Biol 2018; 133: 36-48.
[http://dx.doi.org/10.1016/j.pbiomolbio.2017.11.001]
[15]
Kusuyama J, Bandow K, Shamoto M, Kakimoto K, Ohnishi T, Matsuguchi T. Low intensity pulsed ultrasound (LIPUS) influences the multilineage differentiation of mesenchymal stem and progenitor cell lines through ROCK-Cot/Tpl2-MEK-ERK signaling pathway. J Biol Chem 2014; 289(15): 10330-44.
[http://dx.doi.org/10.1074/jbc.M113.546382]
[16]
Lee HJ, Choi BH, Min BH, Son YS, Park SR. Low-intensity ultrasound stimulation enhances chondrogenic differentiation in alginate culture of mesenchymal stem cells. Artif Organs 2006; 30(9): 707-15.
[http://dx.doi.org/10.1111/j.1525-1594.2006.00288.x]
[17]
Miller DL, Smith NB, Bailey MR, Czarnota GJ, Hynynen K, Makin IRS. Bioeffects Committee of the American Institute of Ultrasound in Medicine. Overview of therapeutic ultrasound applications and safety considerations. J Ultrasound Med 2012; 31(4): 623-34.
[http://dx.doi.org/10.7863/jum.2012.31.4.623]
[18]
Qin L, Lu H, Fok P, et al. Low-intensity pulsed ultrasound accelerates osteogenesis at bone-tendon healing junction. Ultrasound Med Biol 2006; 32(12): 1905-11.
[http://dx.doi.org/10.1016/j.ultrasmedbio.2006.06.028]
[19]
Duck FA. The propagation of ultrasound through tissueThe safe use of ultrasound in medical diagnosis. London: The British In-stitute of Radiology 2012; pp. 4-17.
[20]
Zhou X, Castro NJ, Zhu W, et al. Improved human bone marrow mesenchymal stem cell osteogenesis in 3D bioprinted tissue scaffolds with low intensity pulsed ultrasound stimulation. Sci Rep 2016; 6: 32876.
[http://dx.doi.org/10.1038/srep32876]
[21]
Xie S, Jiang X, Wang R, et al. Low-intensity pulsed ultrasound promotes the proliferation of human bone mesenchymal stem cells by activating PI3K/AKt signaling pathways. J Cell Biochem 2019; 120(9): 15823-33.
[http://dx.doi.org/10.1002/jcb.28853]
[22]
Hormozi MZ. 2015.
[23]
Ikeda K, Takayama T, Suzuki N, Shimada K, Otsuka K, Ito K. Effects of low-intensity pulsed ultrasound on the differentiation of C2C12 cells. Life Sci 2006; 79(20): 1936-43.
[http://dx.doi.org/10.1016/j.lfs.2006.06.029]
[24]
Mostafa NZ, Uludağ H, Dederich DN, Doschak MR, El-Bialy TH. 2009.
[25]
Wu L, Lin L, Qin Y-X. Enhancement of cell ingrowth, proliferation, and early differentiation in a three-dimensional silicon carbide scaffold using low-intensity pulsed ultrasound. Tissue Eng Part A 2015; 21(1-2): 53-61.
[http://dx.doi.org/10.1089/ten.tea.2013.0597]
[26]
Li L, Yang Z, Zhang H, Chen W, Chen M, Zhu Z. Low-intensity pulsed ultrasound regulates proliferation and differentiation of osteoblasts through osteocytes. Biochem Biophys Res Commun 2012; 418(2): 296-300.
[http://dx.doi.org/10.1016/j.bbrc.2012.01.014]
[27]
Gleizal A, Ferreira S, Lavandier B, Simon B, Béziat JL, Béra JC. 2010.
[28]
Angle SR, Sena K, Sumner DR, Virdi AS. Osteogenic differentiation of rat bone marrow stromal cells by various intensities of low-intensity pulsed ultrasound. Ultrasonics 2011; 51(3): 281-8.
[http://dx.doi.org/10.1016/j.ultras.2010.09.004]
[29]
Yang M-H, Lim K-T, Choung P-H, Cho C-S, Chung JH. Application of ultrasound stimulation in bone tissue engineering. Int J Stem Cells 2010; 3(2): 74-9.
[http://dx.doi.org/10.15283/ijsc.2010.3.2.74]
[30]
Cui JH, Park K, Park SR, Min B-H. Effects of low-intensity ultrasound on chondrogenic differentiation of mesenchymal stem cells embedded in polyglycolic acid: an in vivo study. Tissue Eng 2006; 12(1): 75-82.
[http://dx.doi.org/10.1089/ten.2006.12.75]
[31]
Kusuyama J, Seong CH, Bandow K, Kakimoto K, Ohnishi T, Matsuguchi T. I–2 Low Intensity Pulsed Ultrasound (LIPUS) Helps to Maintain the Undifferentiated Status of Mesenchymal Stem Cells. J Orthop Trauma 2015; 29(5): S2.
[http://dx.doi.org/10.1097/01.bot.0000462953.87235.74]
[32]
Kusuyama J, Nakamura T, Ohnishi T, Eiraku N, Noguchi K, Matsuguchi T. Low-Intensity Pulsed Ultrasound (LIPUS) Promotes BMP9-Induced Osteogenesis and Suppresses Inflammatory Responses in Human Periodontal Ligament-Derived Stem Cells. J Orthop Trauma 2017; 31(7): S4.
[http://dx.doi.org/10.1097/01.bot.0000520897.92470.70]
[33]
Hu B, Zhang Y, Zhou J, et al. Low-intensity pulsed ultrasound stimulation facilitates osteogenic differentiation of human periodontal ligament cells. PLoS One 2014; 9(4)e95168
[http://dx.doi.org/10.1371/journal.pone.0095168]
[34]
Ren L, Yang Z, Song J, Wang Z, Deng F, Li W. Involvement of p38 MAPK pathway in low intensity pulsed ultrasound induced osteogenic differentiation of human periodontal ligament cells. Ultrasonics 2013; 53(3): 686-90.
[http://dx.doi.org/10.1016/j.ultras.2012.10.008]
[35]
Inubushi T, Tanaka E, Rego EB, et al. Effects of ultrasound on the proliferation and differentiation of cementoblast lineage cells. J Periodontol 2008; 79(10): 1984-90.
[http://dx.doi.org/10.1902/jop.2008.080081]
[36]
Gao Q, Walmsley AD, Cooper PR, Scheven BA. Ultrasound stimulation of different dental stem cell populations: role of mi-togen-activated protein kinase signaling. J Endod 2016; 42(3): 425-31.
[http://dx.doi.org/10.1016/j.joen.2015.12.019]
[37]
Lv Y, Zhao P, Chen G, Sha Y, Yang L. Effects of low-intensity pulsed ultrasound on cell viability, proliferation and neural differentiation of induced pluripotent stem cells-derived neural crest stem cells. Biotechnol Lett 2013; 35(12): 2201-12.
[http://dx.doi.org/10.1007/s10529-013-1313-4]
[38]
Nishida T, Kubota S, Aoyama E, Yamanaka N, Lyons KM, Takigawa M. Low-intensity pulsed ultrasound (LIPUS) treatment of cultured chondrocytes stimulates production of CCN family protein 2 (CCN2), a protein involved in the regeneration of articular cartilage: mechanism underlying this stimulation. Osteoarthritis Cartilage 2017; 25(5): 759-69.
[http://dx.doi.org/10.1016/j.joca.2016.10.003]
[39]
Suzuki A, Takayama T, Suzuki N, Sato M, Fukuda T, Ito K. Daily low-intensity pulsed ultrasound-mediated osteogenic differentiation in rat osteoblasts. Acta Biochim Biophys Sin (Shanghai) 2009; 41(2): 108-15.
[http://dx.doi.org/10.1093/abbs/gmn012]
[40]
El-Bialy T, Alhadlaq A, Wong B, Kucharski C. Ultrasound effect on neural differentiation of gingival stem/progenitor cells. Ann Biomed Eng 2014; 42(7): 1406-12.
[http://dx.doi.org/10.1007/s10439-014-1013-9]
[41]
Abrunhosa VM, Soares CP, Batista Possidonio AC, et al. Induction of skeletal muscle differentiation in vitro by therapeutic ultrasound. Ultrasound Med Biol 2014; 40(3): 504-12.
[http://dx.doi.org/10.1016/j.ultrasmedbio.2013.10.013]
[42]
Appleford MR, Oh S, Cole JA, Protivínský J, Ong JL. Ultrasound effect on osteoblast precursor cells in trabecular calcium phosphate scaffolds. Biomaterials 2007; 28(32): 4788-94.
[http://dx.doi.org/10.1016/j.biomaterials.2007.06.010]
[43]
Teo A, Morshedi A, Wang JC, Zhou Y, Lim M. Enhancement of Cardiomyogenesis in Murine Stem Cells by Low-Intensity Ultrasound. J Ultrasound Med 2017; 36(8): 1693-706.
[http://dx.doi.org/10.7863/ultra.16.12042]
[44]
Zhang Z, Ma Y, Guo S, He Y, Bai G, Zhang W. Low-intensity pulsed ultrasound stimulation facilitates in vitro osteogenic differentiation of human adipose-derived stem cells via up-regulation of heat shock protein (HSP)70, HSP90, and bone morphogenetic protein (BMP) signaling pathway. Biosci Rep 2018; 38(3)BSR20180087
[http://dx.doi.org/10.1042/BSR20180087]
[45]
Xu P, Gul-Uludag H, Ang WT, et al. Low-intensity pulsed ultrasound-mediated stimulation of hematopoietic stem/progenitor cell viability, proliferation and differentiation in vitro. Biotechnol Lett 2012; 34(10): 1965-73.
[http://dx.doi.org/10.1007/s10529-012-0984-6]
[46]
Wang X, Lin Q, Zhang T, et al. Low-intensity pulsed ultrasound promotes chondrogenesis of mesenchymal stem cells via regulation of autophagy. Stem Cell Res Ther 2019; 10(1): 41.
[http://dx.doi.org/10.1186/s13287-019-1142-z]
[47]
Xia P, Wang X, Qu Y, et al. TGF-β1-induced chondrogenesis of bone marrow mesenchymal stem cells is promoted by low-intensity pulsed ultrasound through the integrin-mTOR signaling pathway. Stem Cell Res Ther 2017; 8(1): 281.
[http://dx.doi.org/10.1186/s13287-017-0733-9]
[48]
Yoon JH, Roh EY, Shin S, et al. Introducing pulsed low-intensity ultrasound to culturing human umbilical cord-derived mesenchymal stem cells. Biotechnol Lett 2009; 31(3): 329-35.
[http://dx.doi.org/10.1007/s10529-008-9872-5]
[49]
Aliabouzar M, Lee SJ, Zhou X, Zhang GL, Sarkar K. Effects of scaffold microstructure and low intensity pulsed ultrasound on chondrogenic differentiation of human mesenchymal stem cells. Biotechnol Bioeng 2018; 115(2): 495-506.
[http://dx.doi.org/10.1002/bit.26480]
[50]
Yue Y, Yang X, Wei X, et al. Osteogenic differentiation of adipose-derived stem cells prompted by low-intensity pulsed ultrasound. Cell Prolif 2013; 46(3): 320-7.
[http://dx.doi.org/10.1111/cpr.12035]
[51]
Lim K, Kim J, Seonwoo H, Park SH, Choung P-H, Chung JH. In vitro effects of low-intensity pulsed ultrasound stimulation on the osteogenic differentiation of human alveolar bone-derived mesenchymal stem cells for tooth tissue engineering 2013.
[52]
He R, Chen J, Jiang J, et al. Synergies of accelerating differentiation of bone marrow mesenchymal stem cells induced by low intensity pulsed ultrasound, osteogenic and endothelial inductive agent. Artif Cells Nanomed Biotechnol 2019; 47(1): 674-84.
[http://dx.doi.org/10.1080/21691401.2019.1576704]
[53]
Li F, Liu Y, Cai Y, et al. Ultrasound irradiation combined with hepatocyte growth factor accelerate the hepatic differentiation of human bone marrow mesenchymal stem cells. Ultrasound Med Biol 2018; 44(5): 1044-52.
[http://dx.doi.org/10.1016/j.ultrasmedbio.2018.01.005]
[54]
Costa V, Carina V, Fontana S, et al. Osteogenic commitment and differentiation of human mesenchymal stem cells by low-intensity pulsed ultrasound stimulation. J Cell Physiol 2018; 233(2): 1558-73.
[http://dx.doi.org/10.1002/jcp.26058]
[55]
Carina V, Costa V, Raimondi L, et al. Effect of low-intensity pulsed ultrasound on osteogenic human mesenchymal stem cells commitment in a new bone scaffold. J Appl Biomater Funct Mater 2017; 15(3): e215-22.
[http://dx.doi.org/10.5301/jabfm.5000342]
[56]
Aliabouzar M, Zhang LG, Sarkar K. Lipid coated microbubbles and low intensity pulsed ultrasound enhance chondrogenesis of human mesenchymal stem cells in 3D printed scaffolds. Sci Rep 2016; 6: 37728.
[http://dx.doi.org/10.1038/srep37728]
[57]
Chiu C-Y, Tsai T-L, Vanderby R Jr, Bradica G, Lou S-L, Li W-J. Osteoblastogenesis of mesenchymal stem cells in 3-D culture enhanced by low-Intensity pulsed ultrasound through soluble re-ceptor activator of nuclear factor kappa B ligand. Ultrasound Med Biol 2015; 41(7): 1842-52.
[http://dx.doi.org/10.1016/j.ultrasmedbio.2015.03.017]
[58]
Wang Y, Peng W, Liu X, et al. Study of bilineage differentiation of human-bone-marrow-derived mesenchymal stem cells in oxidized sodium alginate/N-succinyl chitosan hydrogels and synergistic effects of RGD modification and low-intensity pulsed ultrasound. Acta Biomater 2014; 10(6): 2518-28.
[http://dx.doi.org/10.1016/j.actbio.2013.12.052]
[59]
Miyasaka M, Nakata H, Hao J, Kim Y-K, Kasugai S, Kuroda S. Low-intensity pulsed ultrasound stimulation enhances heat-shock protein 90 and mineralized nodule formation in mouse calvaria-derived osteoblasts. Tissue Eng Part A 2015; 21(23-24): 2829-39.
[http://dx.doi.org/10.1089/ten.tea.2015.0234]
[60]
Uddin SM, Qin Y-X. Enhancement of osteogenic differentiation and proliferation in human mesenchymal stem cells by a modified low intensity ultrasound stimulation under simulated microgravity. PLoS One 2013; 8(9)e73914
[http://dx.doi.org/10.1371/journal.pone.0073914]
[61]
Lee SY, Koh A, Niikura T, et al. Low-intensity pulsed ultrasound enhances BMP-7-induced osteogenic differentiation of human fracture hematoma-derived progenitor cells in vitro. J Orthop Trauma 2013; 27(1): 29-33.
[http://dx.doi.org/10.1097/BOT.0b013e3182519492]
[62]
Lai C-H, Chen S-C, Chiu L-H, et al. Effects of low-intensity pulsed ultrasound, dexamethasone/TGF-β1 and/or BMP-2 on the transcriptional expression of genes in human mesenchymal stem cells: chondrogenic vs. osteogenic differentiation. Ultrasound Med Biol 2010; 36(6): 1022-33.
[http://dx.doi.org/10.1016/j.ultrasmedbio.2010.03.014]
[63]
Schumann D, Kujat R, Zellner J, Angele M, Nerlich M, Mayr E, et al. Treatment of human mesenchymal stem cells with pulsed low intensity ultrasound enhances the chondrogenic phenotype in vitro 2006.
[64]
Kaur H, Siraki AG, Sharma M, et al. Reactive Oxygen Species Mediate Therapeutic Ultrasound-Induced, Mitogen-Activated Protein Kinase Activation in C28/I2 Chondrocytes. Ultrasound Med Biol 2018; 44(10): 2105-14.
[http://dx.doi.org/10.1016/j.ultrasmedbio.2018.05.025]
[65]
Jiang T, Xu T, Gu F, Chen A, Xiao Z, Zhang D. Osteogenic effect of low intensity pulsed ultrasound on rat adipose-derived stem cells in vitro. J Huazhong Univ Sci Technolog Med Sci 2012; 32(1): 75-81. Med Sci
[http://dx.doi.org/10.1007/s11596-012-0013-y]
[66]
Sena K, Angle SR, Kanaji A, et al. Low-intensity pulsed ultrasound (LIPUS) and cell-to-cell communication in bone marrow stromal cells. Ultrasonics 2011; 51(5): 639-44.
[http://dx.doi.org/10.1016/j.ultras.2011.01.007]
[67]
Sena K, Leven RM, Mazhar K, Sumner DR, Virdi AS. Early gene response to low-intensity pulsed ultrasound in rat osteoblastic cells. Ultrasound Med Biol 2005; 31(5): 703-8.
[http://dx.doi.org/10.1016/j.ultrasmedbio.2005.01.013]
[68]
Imai Y, Hasegawa T, Takeda D, et al. 2014.
[69]
Chen S-H, Wu C-C, Wang S-H, Li W-T. Growth and differentia-tion of osteoblasts regulated by low-intensity pulsed ultrasound of various exposure durations. J Med Biol Eng 2014; 34: 197-203.
[http://dx.doi.org/10.5405/jmbe.1346]
[70]
Koga T, Lee SY, Niikura T, et al. Effect of low-intensity pulsed ultrasound on bone morphogenetic protein 7-induced osteogenic differentiation of human nonunion tissue-derived cells in vitro. J Ultrasound Med 2013; 32(6): 915-22.
[http://dx.doi.org/10.7863/ultra.32.6.915]
[71]
Wu S, Kawahara Y, Manabe T, et al. Low-intensity pulsed ultrasound accelerates osteoblast differentiation and promotes bone formation in an osteoporosis rat model. Pathobiology 2009; 76(3): 99-107.
[http://dx.doi.org/10.1159/000209387]
[72]
Takayama T, Suzuki N, Ikeda K, et al. Low-intensity pulsed ultrasound stimulates osteogenic differentiation in ROS 17/2.8 cells. Life Sci 2007; 80(10): 965-71.
[http://dx.doi.org/10.1016/j.lfs.2006.11.037]
[73]
Mukai S, Ito H, Nakagawa Y, Akiyama H, Miyamoto M, Nakamura T. Transforming growth factor-β1 mediates the effects of low-intensity pulsed ultrasound in chondrocytes. Ultrasound Med Biol 2005; 31(12): 1713-21.
[http://dx.doi.org/10.1016/j.ultrasmedbio.2005.07.012]
[74]
Korstjens CM, Nolte PA, Burger EH, et al. Stimulation of bone cell differentiation by low-intensity ultrasound--a histomorphometric in vitro study. J Orthop Res 2004; 22(3): 495-500.
[http://dx.doi.org/10.1016/j.orthres.2003.09.011]
[75]
Leung KS, Cheung WH, Zhang C, Lee KM, Lo HK. Low intensity pulsed ultrasound stimulates osteogenic activity of human periosteal cells. Clin Orthop Relat Res 2004; (418): 253-9.
[http://dx.doi.org/10.1097/00003086-200401000-00044]
[76]
Saito M, Fujii K, Tanaka T, Soshi S. Effect of low- and high-intensity pulsed ultrasound on collagen post-translational modifications in MC3T3-E1 osteoblasts. Calcif Tissue Int 2004; 75(5): 384-95.
[http://dx.doi.org/10.1007/s00223-004-0292-9]
[77]
Feisst V, Meidinger S, Locke MB. From bench to bedside: use of human adipose-derived stem cells. Stem Cells Cloning 2015; 8: 149-62.
[78]
Schäffler A, Büchler C. Concise review: adipose tissue-derived stromal cells--basic and clinical implications for novel cell-based therapies. Stem Cells 2007; 25(4): 818-27.
[http://dx.doi.org/10.1634/stemcells.2006-0589]
[79]
Hwang NS, Varghese S, Elisseeff J. Controlled differentiation of stem cells. Adv Drug Deliv Rev 2008; 60(2): 199-214.
[http://dx.doi.org/10.1016/j.addr.2007.08.036]
[80]
Maxson S, Lopez EA, Yoo D, Danilkovitch-Miagkova A, Leroux MA. Concise review: role of mesenchymal stem cells in wound repair. Stem Cells Transl Med 2012; 1(2): 142-9.
[http://dx.doi.org/10.5966/sctm.2011-0018]
[81]
Kim H, Han JW, Lee JY, et al. Diabetic mesenchymal stem cells are ineffective for improving limb ischemia due to their impaired angiogenic capability. Cell Transplant 2015; 24(8): 1571-84.
[http://dx.doi.org/10.3727/096368914X682792]
[82]
Yao B, Huang S, Gao D, Xie J, Liu N, Fu X. Age-associated changes in regenerative capabilities of mesenchymal stem cell: impact on chronic wounds repair. Int Wound J 2016; 13(6): 1252-9.
[http://dx.doi.org/10.1111/iwj.12491]
[83]
Duscher D, Barrera J, Wong VW, et al. Stem cells in wound heal-ing: the future of regenerative medicine? A mini-review. Gerontology 2016; 62(2): 216-25.
[http://dx.doi.org/10.1159/000381877]
[84]
Choudhery MS, Badowski M, Muise A, Pierce J, Harris DT. Donor age negatively impacts adipose tissue-derived mesenchymal stem cell expansion and differentiation. J Transl Med 2014; 12(1): 8.
[http://dx.doi.org/10.1186/1479-5876-12-8]
[85]
van de Vyver M. Intrinsic mesenchymal stem cell dysfunction in diabetes mellitus: implications for autologous cell therapy. Stem Cells Dev 2017; 26(14): 1042-53.
[http://dx.doi.org/10.1089/scd.2017.0025]
[86]
Cianfarani F, Toietta G, Di Rocco G, Cesareo E, Zambruno G, Odorisio T. Diabetes impairs adipose tissue-derived stem cell function and efficiency in promoting wound healing. Wound Repair Regen 2013; 21(4): 545-53.
[http://dx.doi.org/10.1111/wrr.12051]
[87]
Rennert RC, Sorkin M, Januszyk M, et al. Diabetes impairs the angiogenic potential of adipose-derived stem cells by selectively depleting cellular subpopulations. Stem Cell Res Ther 2014; 5(3): 79.
[http://dx.doi.org/10.1186/scrt468]
[88]
Bai Q, Desprat R, Klein B, Lemaître JM, De Vos J. Embryonic stem cells or induced pluripotent stem cells? A DNA integrity perspective. Curr Gene Ther 2013; 13(2): 93-8.
[http://dx.doi.org/10.2174/1566523211313020003]
[89]
Huang W-C, Ke M-W, Cheng C-C, et al. Therapeutic benefits of induced pluripotent stem cells in monocrotaline-induced pulmo-nary arterial hypertension. PLoS One 2016; 11(2)e0142476
[http://dx.doi.org/10.1371/journal.pone.0142476]
[90]
Musunuru K, Sheikh F, Gupta RM, et al. American Heart Association Council on Functional Genomics and Translational Biology; Council on Cardiovascular Disease in the Young; and Council on Cardiovascular and Stroke Nursing. Induced pluripotent stem cells for cardiovascular disease modeling and precision medicine: a scientific statement from the American Heart Associ-ation. Circulation. Circ Genom Precis Med 2018; 11(1)e000043
[http://dx.doi.org/10.1161/HCG.0000000000000043]
[91]
Ying ZM, Lin T, Yan SG. Low-intensity pulsed ultrasound therapy: a potential strategy to stimulate tendon-bone junction healing. J Zhejiang Univ Sci B 2012; 13(12): 955-63.
[http://dx.doi.org/10.1631/jzus.B1200129]
[92]
Harrison A, Lin S, Pounder N, Mikuni-Takagaki Y. Mode & mechanism of low intensity pulsed ultrasound (LIPUS) in fracture repair. Ultrasonics 2016; 70: 45-52.
[http://dx.doi.org/10.1016/j.ultras.2016.03.016]
[93]
Matsumoto K, Shimo T, Kurio N, et al. Low-intensity pulsed ultrasound stimulation promotes osteoblast differentiation through hedgehog signaling. J Cell Biochem 2018; 119(6): 4352-60.
[http://dx.doi.org/10.1002/jcb.26418]
[94]
Ling L, Wei T, He L, et al. Low-intensity pulsed ultrasound activates ERK1/2 and PI3K-Akt signalling pathways and promotes the proliferation of human amnion-derived mesenchymal stem cells. Cell Prolif 2017; 50(6)e12383
[http://dx.doi.org/10.1111/cpr.12383]
[95]
Cui JH, Park SR, Park K, Choi BH, Min BH. Preconditioning of mesenchymal stem cells with low-intensity ultrasound for cartilage formation in vivo. Tissue Eng 2007; 13(2): 351-60.
[http://dx.doi.org/10.1089/ten.2006.0080]
[96]
Yang KH, Parvizi J, Wang SJ, et al. Exposure to low-intensity ultrasound increases aggrecan gene expression in a rat femur fracture model. J Orthop Res 1996; 14(5): 802-9.
[http://dx.doi.org/10.1002/jor.1100140518]
[97]
Wang Y, Li J, Qiu Y, et al. Lowintensity pulsed ultrasound promotes periodontal ligament stem cell migration through TWIST1mediated SDF1 expression. Int J Mol Med 2018; 42(1): 322-30.
[http://dx.doi.org/10.3892/ijmm.2018.3592]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 15
ISSUE: 5
Year: 2020
Published on: 21 July, 2020
Page: [462 - 472]
Pages: 11
DOI: 10.2174/1574888X15666200225124934
Price: $65

Article Metrics

PDF: 17
HTML: 3
EPUB: 1
PRC: 1