Low-frequency, low-magnitude vibrations (LFLM) enhances chondrogenic differentiation potential of human adipose derived mesenchymal stromal stem cells (hASCs)

. 2016 ; 4 () : e1637. [epub] 20160225

Status PubMed-not-MEDLINE Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid26966645

The aim of this study was to evaluate if low-frequency, low-magnitude vibrations (LFLM) could enhance chondrogenic differentiation potential of human adipose derived mesenchymal stem cells (hASCs) with simultaneous inhibition of their adipogenic properties for biomedical purposes. We developed a prototype device that induces low-magnitude (0.3 g) low-frequency vibrations with the following frequencies: 25, 35 and 45 Hz. Afterwards, we used human adipose derived mesenchymal stem cell (hASCS), to investigate their cellular response to the mechanical signals. We have also evaluated hASCs morphological and proliferative activity changes in response to each frequency. Induction of chondrogenesis in hASCs, under the influence of a 35 Hz signal leads to most effective and stable cartilaginous tissue formation through highest secretion of Bone Morphogenetic Protein 2 (BMP-2), and Collagen type II, with low concentration of Collagen type I. These results correlated well with appropriate gene expression level. Simultaneously, we observed significant up-regulation of α3, α4, β1 and β3 integrins in chondroblast progenitor cells treated with 35 Hz vibrations, as well as Sox-9. Interestingly, we noticed that application of 35 Hz frequencies significantly inhibited adipogenesis of hASCs. The obtained results suggest that application of LFLM vibrations together with stem cell therapy might be a promising tool in cartilage regeneration.

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Akiyama H. Control of chondrogenesis by the transcription factor Sox9. Modern Rheumatology. 2008;18:213–219. doi: 10.3109/s10165-008-0048-x. PubMed DOI

Albelda SM, Buck CA. Integrins and other cell adhesion molecules. FASEB Journal. 1990;4(11):2868–2880. PubMed

Baer PC, Geiger H. Adipose-derived mesenchymal stromal/stem cells: tissue localization, characterization, and heterogeneity. Stem Cells. 2012;2012 doi: 10.1155/2012/812693. 812693. PubMed DOI PMC

Bell DM, Leung KK, Wheatley SC, Ng LJ, Zhou S, Ling KW, Sham MH, Koopman P, Tam PP, Cheah KS. SOX9 directly regulates the type-II collagen gene. Nature Genetics. 1997;16(2):174–178. doi: 10.1038/ng0697-174. PubMed DOI

Brandt KD. Effects of nonsteroidal anti-inflammatory drugs on chondrocyte metabolism in vitro and in vivo. American Journal of Medicine. 1987;83(5A):29–34. PubMed

Brittberg M, Lindahl A, Nilsson A, Ohlsson C, Isaksson O, Peterson L. Treatment of deep cartilage defects in the knee with autologous chondrocyte transplantation. New England Journal of Medicine. 1994;331:889–895. doi: 10.1056/NEJM199410063311401. PubMed DOI

Cashion A, Caballero M, Halevi A, Pappa A, Dennis RG, Van Aalst JA. Programmable mechanobioreactor for exploration of the effects of periodic vibratory stimulus on mesenchymal stem cell differentiation. BioResearch Open Access. 2014;3(1):19–28. doi: 10.1089/biores.2013.0048. PubMed DOI PMC

Chomczynski P, Sacchi N. Single-step method for RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Analytical Biochemistry. 1987;162:156–159. PubMed

Choudhery MS, Badowski M, Muise A, Pierce J, Harris DT. Donor age negatively impacts adipose tissue-derived mesenchymal stem cell expansion and differentiation. Journal of Translational Medicine. 2014;12(7):8. doi: 10.1186/1479-5876-12-8. PubMed DOI PMC

Chung C, Burdick JA. Engineering cartilage tissue. Advanced Drug Delivery Reviews. 2008;60(2):243–262. doi: 10.1016/j.addr.2007.08.027. PubMed DOI PMC

Ciombor DM, Aaron RK. The role of electrical stimulation in bone repair. Foot and Ankle Clinics. 2005;10:579–593. doi: 10.1016/j.fcl.2005.06.006. PubMed DOI

Collino F, Deregibus MC, Bruno S, Sterpone L, Aghemo G, Viltono L, Camussi G. Microvesicles derived from adult human bone marrow and tissue specific mesenchymal stem cells shuttle selected pattern of miRNAs. PLoS ONE. 2010;5(7):e1637. doi: 10.1371/journal.pone.0011803. PubMed DOI PMC

Edwards JH, Reilly GC. Vibration stimuli and the differentiation of musculoskeletal progenitor cells: Review of results in vitro and in vivo. World Journal of Stem Cells. 2015;7(3):568–582. doi: 10.4252/wjsc.v7.i3.568. PubMed DOI PMC

El-Mowafi H, Mohsen M. The effect of low-intensity pulsed ultrasound on callus maturation in tibial distraction osteogenesis. International Orthopaedics. 2005;29:121–124. doi: 10.1007/s00264-004-0625-3. PubMed DOI PMC

Foley KT, Mroz TE, Arnold PM, Chandler HC, Jr, Dixon RA, Girasole GJ, Renkens KL, Jr, Riew KD, Sasso RC, Smith RC, Tung H, Wecht DA, Whiting DM. Randomized, prospective, and controlled clinical trial of pulsed electromagnetic field stimulation for cervical fusion. The Spine Journal. 2008;8:436–442. doi: 10.1016/j.spinee.2007.06.006. PubMed DOI

Giancotti FG, Ruoslahti E. Integrin signaling. Science. 1999;285(5430):1028–1032. doi: 10.1126/science.285.5430.1028. PubMed DOI

Goessler UR, Bugert P, Bieback K, Stern-Straeter J, Bran G, Sadick H, Hörmann K, Riedel F. In vitro analysis of integrin expression in stem cells from bone marrow and cord blood during chondrogenic differentiation. Journal of Cellular and Molecular Medicine. 2009;13(6):1175–1184. doi: 10.1111/j.1582-4934.2008.00451.x. PubMed DOI PMC

Grzesiak J, Marycz K, Czogala J, Wrzeszcz K, Nicpon J. Comparison of behavior, morphology and morphometry of equine and canine adipose derived mesenchymal stem cells in culture. International Journal of Morphology. 2011;29:1012–1017. doi: 10.4067/S0717-95022011000300059. DOI

Hammerick KE, James AW, Huang Z, Prinz FB, Longaker MT. Pulsed direct current electric fields enhance osteogenesis in adipose-derived stromal cells. Tissue Engineering Part A. 2009;16(3):917–931. doi: 10.1089/ten.TEA.2009.0267. PubMed DOI PMC

Hass R, Kasper C, Bohm S, Jacobs R. Different populations and sources of human mesenchymal stem cells (MSC): a comparison of adult and neonatal tissue-derived MSC. Cell Communication and Signaling. 2011;9:12. doi: 10.1186/1478-811X-9-12. PubMed DOI PMC

Hering TM. Regulation of chondrocyte gene expression. Frontiers in Bioscience. 1999;4:D743–D761. doi: 10.2741/Hering. PubMed DOI

Hynes RO. Integrins: versatility, modulation, and signaling in cell adhesion. Cell. 1992;69(1):11–25. doi: 10.1016/0092-8674(92)90115-S. PubMed DOI

Iyer SS, Rojas M. Anti-inflammatory effects of mesenchymal stem cells: novel concept for future therapies. Expert Opinion on Biological Therapy. 2008;8(5):569–581. doi: 10.1517/14712598.8.5.569. PubMed DOI

Kim HJ, Im GI. The effects of ERK1/2 inhibitor on the chondrogenesis of bone marrow- and adipose tissue-derived multipotent mesenchymal stromal cells. Tissue Engineering. Part A. 2010;16(3) doi: 10.1089/ten.TEA.2009.0070. 851e60. PubMed DOI

Krampera M, Pasini A, Pizzolo G, Cosmi L, Romagnani S, Annunziato F. Regenerative and immunomodulatory potential of mesenchymal stem cells. Current Opinion in Pharmacology. 2006;6(4):435–441. doi: 10.1016/j.coph.2006.02.008. PubMed DOI

Lau E, Al-Dujaili S, Guenther A, Liu D, Wang L, You L. Effect of low-magnitude, high-frequency vibration on osteocytes in the regulation of osteoclasts. Bone. 2010;46(6):1508–1515. doi: 10.1016/j.bone.2010.02.031. PubMed DOI PMC

Lee JW, Qi WN, Scully SP. The involvement of beta1 integrin in the modulation by collagen of chondrocyte-response to transforming growth factor-beta1. Journal of Orthopaedic Research. 2002;20(1):66–75. doi: 10.1016/S0736-0266(01)00073-0. PubMed DOI

Lin J, Zhang W, Jones A, Doherty M. Efficacy of topical non-steroidal anti-inflammatory drugs in the treatment of osteoarthritis: meta-analysis of randomised controlled trials. BMJ. 2004;329(7461):324–330. doi: 10.1136/bmj.38159.639028.7C. PubMed DOI PMC

Luu YK, Capilla E, Rosen CJ, Gilsanz V, Pessin JE, Judex S, Rubin CT. Mechanical stimulation of mesenchymal stem cell proliferation and differentiation promotes osteogenesis while preventing dietary-induced obesity. Journal of Bone and Mineral Research. 2009;24:50–61. doi: 10.1359/jbmr.080817. PubMed DOI PMC

Marędziak M, Marycz K, Lewandowski D, Siudzinska A, Śmieszek A. Static magnetic field enhances synthesis and secretion of membrane-derived microvesicles (MVs) rich in VEGF and BMP-2 in equine adipose-derived stromal cells (EqASCs)-a new approach in veterinary regenerative medicine. In Vitro Cellular & Developmental Biology—Animal. 2015;51(3):230–240. doi: 10.1007/s11626-014-9828-0. PubMed DOI PMC

Marędziak M, Marycz K, Śmieszek A, Lewandowski D, Nezir Yaşar Toker. The influence of static magnetic fields on canine and equine mesenchymal stem cells derived from adipose tissue. In Vitro Cellular & Developmental Biology—Animal. 2014;50:562–571. doi: 10.1007/s11626-013-9730-1. PubMed DOI PMC

Martino MM, Mochizuki M, Rothenfluh DA, Rempel SA, Hubbell JA, Barker TH. Controlling integrin specificity and stem cell differentiation in 2D and 3D environments through regulation of fibronectin domain stability. Biomaterials. 2009;30(6):1089–1097. doi: 10.1016/j.biomaterials.2008.10.047. PubMed DOI PMC

Marycz K, Grzesiak J, Wrzeszcz K, Golonka P. Adipose stem cell combined with plasma-based implant bone tissue differentiation in vitro and in a horse with a phalanx digitalis distalis fracture: a case report. Veterinarni Medicina. 2012;57(11):610–617. 2012.

Marycz K, Smieszek A, Grzesiak J, Donesz-Sikorska A, Krzak-Ros J. Application of bone marrow and adipose-derived mesenchymal stem cells for testing the biocompatibility of metal-based biomaterials functionalized with ascorbic acid. Biomedical Materials. 2013;8 doi: 10.1088/1748-6041/8/6/065004. 065004. PubMed DOI

Marycz K, Toker NY, Grzesiak J, Wrzeszcz K, Golonka P. The therapeutic effect of autogenic adipose derived stem cells combined with autogenic platelet rich plasma in tendons disorders hi horses in vitro and in vivo research. Journal of Animal and Veterinary Advances. 2012;11(23):4324–4331. doi: 10.3923/javaa.2012.4324.4331. 2012. DOI

Miller D, Smith N, Bailey M, Czarnota G, Hynynen K, Makin I, American Institute of Ultrasound in Medicine Bioeffects Committee Overview of therapeutic ultrasound applications and safety considerations. Journal of Ultrasound in Medicine. 2012;31(4):623–634. PubMed PMC

Miloro M, Miller JJ, Stoner JA. Low-level laser effect on mandibular distraction osteogenesis. Journal of Oral and Maxillofacial Surgery. 2007;65:168–176. doi: 10.1016/j.joms.2006.10.002. PubMed DOI

Mishra A, Tummala P, King A, Lee B, Kraus M, Tse V, Jacobs CR. Buffered platelet-rich plasma enhances mesenchymal stem cell proliferation and chondrogenic differentiation. Tissue Engineering Part C: Methods. 2009;15(3):431–435. doi: 10.1089/ten.tec.2008.0534. PubMed DOI PMC

Nicpoń J, Marycz K, Grzesiak J, Śmieszek A, Toker ZY. The advantages of autologus adipose derived mesenchymal stem cells (AdMSCs) over the non-steroidal anti-inflammatory drugs (NSAIDs) application for degenerative elbow joint disease treatment in dogs-Twelve cases. Kafkas Üniversitesi Veteriner Fakültesi Dergisi. 2014;20(3):345–350. doi: 10.9775/kvfd.2013.10105. DOI

Nikander R, Kannus P, Dastidar P, Hannula M, Harrison L, Cervinka T, Narra NG, Aktour R, Arola T, Eskola H, Soimakallio S, Heinonen A, Hyttinen J, Sievänen H. Targeted exercises against hip fragility. Osteoporosis International. 2009;20:1321–1328. doi: 10.1007/s00198-008-0785-x. PubMed DOI

Oh ES, Seo YK, Yoon HH, Cho H, Yoon MY, Park JK. Effects of sub-sonic vibration on the proliferation and maturation of 3T3-L1 cells. Life Sciences. 2011;88(3–4):169–177. doi: 10.1016/j.lfs.2010.11.007. Jan 17. PubMed DOI

Popov C, Burggraf M, Kreja L, Ignatius A, Schieker M, Docheva D. Mechanical stimulation of human tendon stem/progenitor cells results in upregulation of matrix proteins, integrins and MMPs, and activation of p38 and ERK1/2 kinases. BMC Molecular Biology. 2015;16:6. doi: 10.1186/s12867-015-0036-6. PubMed DOI PMC

Prè D, Ceccarelli G, Visai L, Benedetti L, Imbriani M, Cusella De Angelis MG, Magenes G. High-frequency vibration treatment of human bone marrow stromal cells increases differentiation toward bone tissue. Bone Marrow Research. 2013;2013 doi: 10.1155/2013/803450. 803450. PubMed DOI PMC

Raeissadat S, Rayegani S, Babaee M, Ghorbani E. The effect of platelet-rich plasma on pain, function, and quality of life of patients with knee osteoarthritis. Pain Research and Treatment. 2013;2013 doi: 10.1155/2013/165967. 165967. PubMed DOI PMC

Rubin C, Judex S, Qin YX. Low-level mechanical signals and their potential as a non-pharmacological intervention for osteoporosis. Age and Ageing. 2006;35:32–36. PubMed

Salter DM, Hughes DE, Simpson R, Gardner DL. Integrin expression by human articular chondrocytes. British Journal of Rheumatology. 1992;31(4):231–234. doi: 10.1093/rheumatology/31.4.231. PubMed DOI

Sen B, Xie Z, Case N, Styner M, Rubin CT, Rubin J. Mechanical signal influence on mesenchymal stem cell fate is enhanced by incorporation of refractory periods into the loading regimen. Journal of Biomechanics. 2011;44(4):593–599. doi: 10.1016/j.jbiomech.2010.11.022. PubMed DOI PMC

Sepúlveda JC, Tomé M, Fernández ME, Delgado M, Campisi J, Bernad A, González MA. Cell senescence abrogates the therapeutic potential of human mesenchymal stem cells in the lethal endotoxemia model. Stem Cells. 2014;32:1865–1877. doi: 10.1002/stem.1654. PubMed DOI PMC

Simmons CA, Matlis S, Thornton AJ, Chen S, Wang CY, Mooney DJ. Cyclic strain enhances matrix mineralization by adult human mesenchymal stem cells via the extracellular signal-regulated kinase (ERK1/2) signaling pathway. Journal of Biomechanics. 2003;36(8):1087–1096. doi: 10.1016/S0021-9290(03)00110-6. PubMed DOI

Taylor KF, Rafiee B, Tis JE, Inoue N. Low-intensity pulsed ultrasound does not enhance distraction callus in a rabbit model. Clinical Orthopaedics and Related Research. 2007;459:237–245. doi: 10.1097/BLO.0b013e31803c75b4. PubMed DOI

Tetta C, Consiglio AL, Bruno S, Tetta E, Gatti E, Dobreva M, Cremonesi F, Camussi G. The role of microvesicles derived from mesenchymal stem cells in tissue regeneration; a dream for tendon repair? Muscles Ligaments Tendons Journal. 2012;2(3):212–221. PubMed PMC

Tirkkonen L, Halonen H, Hyttinen J, Kuokkanen H, Sievänen H, Koivisto AM, Haimi S. The effects of vibration loading on adipose stem cell number, viability and differentiation towards bone-forming cells. Journal of The Royal Society Interface. 2011;8(65):1736–1747. doi: 10.1098/rsif.2011.0211. PubMed DOI PMC

Uzer G, Pongkitwitoon S, Ete Chan M, Judex S. Vibration induced osteogenic commitment of mesenchymal stem cells is enhanced by cytoskeletal remodeling but not fluid shear. Journal of Biomechanics. 2013;46:2296–2302. doi: 10.1016/j.jbiomech.2013.06.008. PubMed DOI PMC

Uzer G, Thompson WR, Sen B, Xie Z, Yen SS, Miller S, Bas G, Styner M, Rubin CT, Judex S, Burridge K, Rubin J. Cell mechanosensitivity to extremely low-magnitude signals is enabled by a LINCed nucleus. Stem Cells. 2015;33(6):2063–2076. doi: 10.1002/stem.2004. PubMed DOI PMC

Wehrle E, Liedert A, Heilmann A, Wehner T, Bindl R, Fischer L, Haffner-Luntzer M, Jakob F, Schinke T, Amling M, Ignatius A. The impact of low-magnitude high-frequency vibration on fracture healing is profoundly influenced by the oestrogen status in mice. Disease Models and Mechanisms. 2015;8(1):93–104. doi: 10.1242/dmm.018622. PubMed DOI PMC

Xie L, Rubin C, Judex S. Enhancement of the adolescent murine musculoskeletal system using low-level mechanical vibrations. Journal of Applied Physiology. 2008;104:1056–1062. doi: 10.1152/japplphysiol.00764.2007. PubMed DOI

Yoon IS, Chung CW, Sung JH, Cho HJ, Kim JS, Shim WS, Shim CK, Chung SJ, Kim DD. Proliferation and chondrogenic differentiation of human adipose-derived mesenchymal stem cells in porous hyaluronic acid scaffold. Journal of Bioscience and Bioengineering. 2011;112(4):402–408. doi: 10.1016/j.jbiosc.2011.06.018. PubMed DOI

Zhou G, Zheng Q, Engin F, Munivez E, Chen Y, Sebald E, Krakow D, Lee B. Dominance of SOX9 function over RUNX2 during skeletogenesis. Proceedings of the National Academy of Sciences of the United States of America. 2006;103(50):19004–19009. doi: 10.1073/pnas.0605170103. PubMed DOI PMC

Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ, Benhaim P, Lorenz HP, Hedrick MH. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Engineering. 2001;7:211–228. doi: 10.1089/107632701300062859. PubMed DOI

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