Dielectrophoresis (DEP), a nonlinear electrokinetic technique caused by Maxwell–Wagner interfacial polarization of neutral particles in an electrolyte solution, is a powerful cell manipulation method used widely for various applications such as enrichment, trapping, and sorting of heterogeneous cell populations. While conventional cell characterization and sorting methods require tagging or labeling of cells, DEP has the potential to manipulate cells in a label-free way. Due to its unique ability to characterize and sort cells without the need of labeling, there is renewed interest in using DEP for stem cell research and regenerative medicine. Stem cells have the potential to differentiate into various lineages, but achieving homogeneous cell phenotypes from an initially heterogeneous cell population is a challenge. Using DEP to efficiently and affordably identify, sort, and enrich either undifferentiated or differentiated stem cell populations in a label-free way would advance their potential uses for applications in tissue engineering and regenerative medicine. This review summarizes recent, significant research findings regarding the electrophysiological characterization of stem cells, with a focus on cellular dielectric properties, i.e., permittivity and conductivity, and on studies that have obtained these measurements using techniques that preserve cell viability, such as crossover frequency. Potential applications for DEP in regenerative medicine are also discussed. Overall, DEP is a promising technique and, when used to characterize, sort, and enrich stem cells, will advance stem cell-based regenerative therapies.
References
1.
M. S.
Talary
, K. I.
Mills
, T.
Hoy
, A. K.
Burnett
, and R.
Pethig
, “Dielectrophoretic separation and enrichment of CD34+ cell subpopulation from bone marrow and peripheral blood stem cells
,” Med. Biol. Eng. Comput.
33
, 235
(1995
).2.
M.
Stephens
, M. S.
Talary
, R.
Pethig
, A. K.
Burnett
, and K. I.
Mills
, “The dielectrophoresis enrichment of CD34+ cells from peripheral blood stem cell harvests
,” Bone Marrow Transplant.
18
(4
), 777
–782
(1996
).3.
Y.
Huang
, J.
Yang
, X. B.
Wang
, F. F.
Becker
, and P. R.
Gascoyne
, “The removal of human breast cancer cells from hematopoietic CD34+ stem cells by dielectrophoretic field-flow-fractionation
,” J. Hematother. Stem Cell Res.
8
(5
), 481
–490
(1999
).4.
A. P.
Lee
, M.
Aghaamoo
, T. N. G.
Adams
, and L. A.
Flanagan
, “It's electric: When technology gives a boost to stem cell science
,” Curr. Stem Cell Rep.
4
(2
), 116
–126
(2018
).5.
T. N. G.
Adams
, A. Y. L.
Jiang
, P. D.
Vyas
, and L. A.
Flanagan
, “Separation of neural stem cells by whole cell membrane capacitance using dielectrophoresis
,” Methods
133
, 91
–103
(2018
).6.
T. N. G.
Adams
, P. A.
Turner
, A. V.
Janorkar
, F.
Zhao
, and A. R.
Minerick
, “Characterizing the dielectric properties of human mesenchymal stem cells and the effects of charged elastin-like polypeptide copolymer treatment
,” Biomicrofluidics
8
(5
), 054109
(2014
).7.
L. A.
Flanagan
et al, “Unique dielectric properties distinguish stem cells and their differentiated progeny
,” Stem Cells
26
(3
), 656
–665
(2008
).8.
A.
Ismail
, M. P.
Hughes
, H. J.
Mulhall
, R. O.
Oreffo
, and F. H.
Labeed
, “Characterization of human skeletal stem and bone cell populations using dielectrophoresis
,” J. Tissue Eng. Regen. Med.
9
(2
), 162
–168
(2015
).9.
H.
Song
et al, “Continuous-flow sorting of stem cells and differentiation products based on dielectrophoresis
,” Lab Chip
15
, 1320
(2015
).10.
A. Y. L.
Jiang
et al, “High-throughput continuous dielectrophoretic separation of neural stem cells
,” Biomicrofluidics
13
(6
), 064111
(2019
).11.
H. A.
Pohl
, “The motion and precipitation of suspensoids in divergent electric fields
,” J. Appl. Phys.
22
(7
), 869
–871
(1951
).12.
H. A.
Pohl
and I.
Hawk
, “Separation of living and dead cells by dielectrophoresis
,” Science
152
(3722
), 647
–649
(1966
).13.
B. H.
Lapizco-Encinas
, B. A.
Simmons
, E. B.
Cummings
, and Y.
Fintschenko
, “Dielectrophoretic concentration and separation of live and dead bacteria in an array of insulators
,” Anal. Chem.
76
(6
), 1571
–1579
(2004
).14.
Z. R.
Gagnon
, “Cellular dielectrophoresis: Applications to the characterization, manipulation, separation and patterning of cells
,” Electrophoresis
32
(18
), 2466
–2487
(2011
).15.
Z.
Cao
et al, “Dielectrophoresis-based protein enrichment for a highly sensitive immunoassay using Ag/SiO2 nanorod arrays
,” Small
14
(12
), 1703265
(2018
).16.
R.
Pethig
, “Review—Where is dielectrophoresis (DEP) going?
” J. Electrochem. Soc.
164
(5
), B3049
–B3055
(2016
).17.
N. A.
Rahman
, F.
Ibrahim
, and B.
Yafouz
, “Dielectrophoresis for biomedical sciences applications: A review
,” Sensors
17
, 449
(2017
).18.
A.
Thiel
, A.
Scheffold
, and A.
Radbruch
, “Immunomagnetic cell sorting - pushing the limits
,” Immunotechnology
4
, 89
–96
(1998
).19.
T.
Zhou
, Y.
Ming
, S. F.
Perry
, and S.
Tatic-Lucic
, “Estimation of the physical properties of neurons and glial cells using dielectrophoresis crossover frequency
,” J. Biol. Phys.
42
, 571
(2016
).20.
E. O.
Adekanmbi
, M. W.
Ueti
, B.
Rinaldi
, C. E.
Suarez
, and S. K.
Srivastava
, “Insulator-based dielectrophoretic diagnostic tool for babesiosis
,” Biomicrofluidics
10
(3
), 033108
(2016
).21.
P.
Weng
, I.
Chen
, C.
Yeh
, P.
Chen
, and J.
Juang
, “Size-dependent dielectrophoretic crossover frequency of spherical particles
,” Biomicrofluidics
10
, 011909
(2016
).22.
R.
Pethig
and D. B.
Kell
, “The passive electrical properties of biological systems: Their significance in physiology, biophysics and biotechnology
,” Phys. Med. Biol.
32
, 933
(1987
).23.
D.
Kim
, M.
Sonker
, and A.
Ros
, “Dielectrophoresis: From molecular to micrometer-scale analytes
,” Anal. Chem.
91
(1
), 277
–295
(2019
).24.
S.
Chang
and Y. H.
Cho
, “A continuous size-dependent particle separator using a negative dielectrophoretic virtual pillar array
,” Lab Chip
8
(11
), 1930
–1936
(2008
).25.
V.
Calero
, P.
Garcia-Sanchez
, C.
Honrado
, A.
Ramos
, and H.
Morgan
, “AC electrokinetic biased deterministic lateral displacement for tunable particle separation
,” Lab Chip
19
(8
), 1386
–1396
(2019
).26.
C.
Huang
, S. M.
Santana
, H.
Liu
, N. H.
Bander
, B. G.
Hawkins
, and B. J.
Kirby
, “Characterization of a hybrid dielectrophoresis and immunocapture microfluidic system for cancer cell capture
,” Electrophoresis
34
(20–21
), 2970
–2979
(2013
).27.
N.
Allahrabbi
, Y. S.
Chia
, M. S.
Saifullah
, K. M.
Lim
, and L. Y.
Yung
, “A hybrid dielectrophoretic system for trapping of microorganisms from water
,” Biomicrofluidics
9
(3
), 034110
(2015
).28.
S.
Yan
, J.
Zhang
, D.
Yuan
, and W.
Li
, “Hybrid microfluidics combined with active and passive approaches for continuous cell separation
,” Electrophoresis
38
(2
), 238
–249
(2017
).29.
G. H.
Markx
, L.
Carney
, M.
Littlefair
, A.
Sebastian
, and A. M.
Buckle
, “Recreating the hematon: Microfabrication of artificial haematopoietic stem cell microniches in vitro using dielectrophoresis
,” Biomed. Microdevices
11
(1
), 143
–150
(2009
).30.
R.
Arya
, H.
Komal
, A.
Sankaranarayanan
, and R.
Krishnamurthy
, “Applications of dielectrophoresis in the field of medical sciences
,” Int. J. S. Res. Sci. Technol.
4
, 328
–341
(2019
).31.
E. O.
Adekanmbi
and S. K.
Srivastava
, “Dielectrophoretic applications for disease diagnostics using lab-on-a-chip platforms
,” Lab Chip
16
, 2148
(2016
).32.
G. R.
Ballantyne
and P. N.
Holtham
, “Application of dielectrophoresis for the separation of minerals
,” Miner. Eng.
23
(4
), 350
–358
(2010
).33.
E. G.
Cen
, C.
Dalton
, Y.
Li
, S.
Adamia
, L. M.
Pilarski
, and K. V. I. S.
Kaler
, “A combined dielectrophoresis, traveling wave dielectrophoresis and electrorotation microchip for the manipulation and characterization of human malignant cells
,” J. Microbiol. Methods
58
(3
), 387
–401
(2004
).34.
H.
Du
, W. H.
Li
, D. F.
Chen
, and C.
Shu
, “Manipulation of bioparticles using traveling wave dielectrophoresis: Numerical approach
,” Int. J. Mech. Mater. Design
1
(2
), 115
–130
(2004
).35.
T.
Sun
, H.
Morgan
, and N. G.
Green
, “Analytical solutions of AC electrokinetics in interdigitated electrode arrays: Electric field, dielectrophoretic and traveling-wave dielectrophoretic forces
,” Phys. Rev. E Stat. Nonlin. Soft Matter Phys.
76
(4
), 046610
(2007
).36.
E.
Choi
, B.
Kim
, and J.-Y.
Park
, “Extremely large-area travelling-wave dielectrophoresis microbead separator using a multilayered bus bar
,” J. Sensor Sci. Technol.
18
(2
), 139
–146
(2009
).37.
M.
Marczak
and H.
Diesinger
, “Traveling wave dielectrophoresis micropump based on the dispersion of a capacitive electrode layer
,” J. Appl. Phys.
105
(12
), 124511
(2009
).38.
I. F.
Cheng
, V. E.
Froude
, Y.
Zhu
, H.-C.
Chang
, and H.-C.
Chang
, “A continuous high-throughput bioparticle sorter based on 3D traveling-wave dielectrophoresis
,” Lab Chip
9
(22
), 3193
–3201
(2009
).39.
C.
Eunpyo
, K.
Byungkyu
, and P.
Jungyul
, “High-throughput microparticle separation using gradient traveling wave dielectrophoresis
,” J. Micromech. Microeng.
19
(12
), 125014
(2009
).40.
B.
Zhu
and S. K.
Murthy
, “Stem cell separation technologies
,” Curr. Opin. Chem. Eng.
2
(1
), 3
–7
(2014
).41.
J.
Yang
et al, “Dielectrophoresis-based microfluidic separation and detection systems
,” Int. J. Adv. Manuf. Syst.
3
(2
), 1
–12
(2000
).42.
R.
Pethig
, A.
Menachery
, S.
Pells
, and P. De
Sousa
, “Dielectrophoresis: A review of applications for stem cell research
,” BioMed Res. Int.
2010
, 182581
.43.
E. O.
Adekanmbi
, A. T.
Giduthuri
, S.
Waymire
, and S. K.
Srivastava
, “Utilization of dielectrophoresis for the quantification of rare earth elements adsorbed on Cupriavidus necator
,” ACS Sustainable Chem. Eng.
8
(3
), 1353
–1361
(2020
).44.
N.
Alinezhadbalalami
, T. A.
Douglas
, N.
Balani
, S. S.
Verbridge
, and R. V.
Davalos
, “The feasibility of using dielectrophoresis for isolation of glioblastoma subpopulations with increased stemness
,” Electrophoresis
40
(18–19
), 2592
–2600
(2019
).45.
H.
Morgan
and N. G.
Green
, AC Electrokinetics Colloids and Nanoparticles
(Research Studies Press
, 2003
).46.
Y.
Feldman
, I.
Ermolina
, and Y.
Hayashi
, “Time domain dielectric spectroscopy study of biological systems
,” IEEE Trans. Dielectr. Electr. Insul.
10
(5
), 728
–753
(2003
).47.
B.
Bavnbek
, B.
Klösgen
, J.
Larsen
, F.
Pociot
, and E.
Renström
, BetaSys: Systems Biology of Regulated Exocytosis in Pancreatic Beta-Cells
(Springer
, 2011
).48.
J.
Gimsa
, P.
Marszalek
, U.
Loewe
, and T. Y.
Tsong
, “Dielectrophoresis and electrorotation of neurospora slime and murine myeloma cells
,” Biophys. J.
60
, 749
(1991
).49.
L.
Yang
, P. P.
Banada
, A. K.
Bhunia
, and R.
Bashir
, “Effects of dielectrophoresis on growth, viability and immuno-reactivity of Listeria monocytogenes
,” J. Biol. Eng.
2
, 6
(2008
).50.
J.
Zhang
, Z.
Song
, Q.
Liu
, and Y.
Song
, “Recent advances in dielectrophoresis-based cell viability assessment
,” Electrophoresis
41
(10-11
), 917
–932
(2020
).51.
V.
Nerguizian
, I.
Stiharu
, N.
Al-Azzam
, B.
Yassine-Diab
, and A.
Alazzam
, “The effect of dielectrophoresis on living cells: Crossover frequencies and deregulation in gene expression
,” The Analyst
144
(12
), 3853
–3860
(2019
).52.
J.
Lu
, C. A.
Barrios
, A. R.
Dickson
, J. L.
Nourse
, A. P.
Lee
, and L. A.
Flanagan
, “Advancing practical usage of microtechnology: a study of the functional consequences of dielectrophoresis on neural stem cells
,” Integr. Biol. (Camb)
4
(10
), 1223
–1236
(2012
).53.
M. J.
Łos
, A.
Skubis
, and S.
Ghavami
, “Stem cells
,” in Stem Cells and Biomaterials for Regenerative Medicine
, edited by M. J.
Łos
, A.
Hudecki
, and E.
Wiecheć
(Academic
, 2019
), Chap. 2, pp. 5
–16
.54.
W.
Zakrzewski
, M.
Dobrzyński
, M.
Szymonowicz
, and Z.
Rybak
, “Stem cells: past, present, and future
,” Stem Cell Res. Ther.
10
(1
), 68
(2019
).55.
K.
MacCord
, “Germ layers
,” in Embryo Project Encyclopedia
(Arizona State University
, 2003
).56.
A. E.
EL Barky
, E. M. M.
Ali
, and T. M.
Mohamed
, “Stem cells, classifications and their clinical applications
,” Am. J. Pharmacol. Ther.
1
(1
), 001
–007
(2017
).57.
A.
Hima Bindu
and B.
Srilatha
, “Potency of various types of stem cells and their transplantation
,” J. Stem Cell Res. Ther.
1
(3
), 115
(2011
).58.
A.
Biswas
and R.
Hutchins
, “Embryonic stem cells
,” Stem Cells Dev.
16
(2
), 213
–222
(2007
).59.
A.
El-Badawy
et al, “Adipose stem cells display higher regenerative capacities and more adaptable electro-kinetic properties compared to bone marrow-derived mesenchymal stromal cells
,” Sci. Rep.
6
(1
), 37801
(2016
).60.
R.
Pethig
, “Dielectrophoresis: Status of the theory, technology, and applications
,” Biomicrofluidics
4
(2
), 022811
(2010
).61.
J.
Yoshioka
, Y.
Ohsugi
, T.
Yoshitomi
, T.
Yasukawa
, N.
Sasaki
, and K.
Yoshimoto
, “Label-free rapid separation and enrichment of bone marrow-derived mesenchymal stem cells from a heterogeneous cell mixture using a dielectrophoresis device
,” Sensors
18
, 3007
(2018
).62.
A. Y.
Wu
and D. M.
Morrow
, “Clinical use of dieletrophoresis separation for live adipose derived stem cells
,” J. Transl. Med.
10
, 99
(2012
).63.
J.
Vykoukal
, D. M.
Vykoukal
, S.
Freyberg
, E. U.
Alt
, and P.
Gascoyne
, “Enrichment of putative stem cells from adipose tissue using dielectrophoretic field-flow fractionation
,” Lab Chip
8
, 1386
(2008
).64.
D. Y.
Gao
et al, “Fundamental cryobiology of human hematopoietic progenitor cells I: Osmotic characteristics and volume distribution
,” Cryobiology
36
(1
), 40
–48
(1998
).65.
A. I.
Caplan
, “Mesenchymal stem cells: Time to change the name!
,” Stem Cells Transl. Med.
6
, 1445
–1451
(2017
).66.
S. D.
Subramony
et al, “The guidance of stem cell differentiation by substrate alignment and mechanical stimulation
,” Biomaterials
34
(8
), 1942
–1953
(2013
).67.
C. K.
Kuo
and R. S.
Tuan
, “Mechanoactive tenogenic differentiation of human mesenchymal stem cells
,” Tissue Eng. Part A
14
(10
), 1615
–1627
(2008
).68.
A. I.
Goncalves
et al, “Understanding the role of growth factors in modulating stem cell tenogenesis
,” PLoS One
8
(12
), e83734
(2013
).69.
N. R.
Schiele
, J. E.
Marturano
, and C. K.
Kuo
, “Mechanical factors in embryonic tendon development: Potential cues for stem cell tenogenesis
,” Curr. Opin. Biotechnol.
24
(5
), 834
–840
(2013
).70.
Y. H.
Li
et al, “The role of scleraxis in fate determination of mesenchymal stem cells for tenocyte differentiation
,” Sci. Rep.
5
, 13149
(2015
).71.
J. P.
Brown
, T. V.
Galassi
, M.
Stoppato
, N. R.
Schiele
, and C. K.
Kuo
, “Comparative analysis of mesenchymal stem cell and embryonic tendon progenitor cell response to embryonic tendon biochemical and mechanical factors
,” Stem Cell Res. Ther.
6
(1
), 89
(2015
).72.
M. T.
Harris
, D. L.
Butler
, G. P.
Boivin
, J. B.
Florer
, E. J.
Schantz
, and R. J.
Wenstrup
, “Mesenchymal stem cells used for rabbit tendon repair can form ectopic bone and express alkaline phosphatase activity in constructs
,” J. Orthop. Res.
22
(5
), 998
–1003
(2004
).73.
J. O.
Jeong
et al, “Malignant tumor formation after transplantation of short-term cultured bone marrow mesenchymal stem cells in experimental myocardial infarction and diabetic neuropathy
,” Circ. Res.
108
, 1340
–1347
(2011
).74.
H. A.
Awad
, G. P.
Boivin
, M. R.
Dressler
, F. N.
Smith
, R. G.
Young
, and D. L.
Butler
, “Repair of patellar tendon injuries using a cell-collagen composite
,” J. Orthop. Res.
21
(3
), 420
–431
(2003
).75.
J.
Ge
et al, “The size of mesenchymal stem cells is a significant cause of vascular obstructions and stroke
,” Stem Cell Rev. Rep.
10
(2
), 295
–303
(2014
).76.
L.
Liu
, L.
Tseng
, Q.
Ye
, Y. L.
Wu
, D. J.
Bain
, and C.
Ho
, “A new method for preparing mesenchymal stem cells and labeling with ferumoxytol for cell tracking by MRI
,” Sci. Rep.
6
(1
), 26271
(2016
).77.
E.
Schmelzer
, D. T.
McKeel
, and J. C.
Gerlach
, “Characterization of human mesenchymal stem cells from different tissues and their membrane encasement for prospective transplantation therapies
,” BioMed Res. Int.
2019
, 6376271
.78.
A.
Bajek
, N.
Gurtowska
, J.
Olkowska
, L.
Kazmierski
, M.
Maj
, and T.
Drewa
, “Adipose-derived stem cells as a tool in cell-based therapies
,” Arch. Immunol. Ther. Exp.
64
(6
), 443
–454
(2016
).79.
P. O.
Bagnaninchi
and N.
Drummond
, “Real-time label-free monitoring of adipose-derived stem cell differentiation with electric cell-substrate impedance sensing
,” Proc. Natl. Acad. Sci. USA
108
, 6462
(2011
).80.
“
Rapid analysis of human adipose- derived stem cells and 3T3-L1 differentiation toward adipocytes using the Scepter™ 2.0 cell counter
,” BioTechniques
53
(2
), 109
–111
(2012
).81.
S. M.
Ridge
, F. J.
Sullivan
, and S. A.
Glynn
, “Mesenchymal stem cells: Key players in cancer progression
,” Mol. Cancer
16
(1
), 31
(2017
).82.
H. Y.
Lee
and I. S.
Hong
, “Double-edged sword of mesenchymal stem cells: Cancer-promoting versus therapeutic potential
,” Cancer Sci.
108
(10
), 1939
–1946
(2017
).83.
U.
Kozlowska
et al, “Similarities and differences between mesenchymal stem/progenitor cells derived from various human tissues
,” World J. Stem Cells
11
(6
), 347
–374
(2019
).84.
M. F.
Pittenger
, D. E.
Discher
, B. M.
Péault
, D. G.
Phinney
, J. M.
Hare
, and A. I.
Caplan
, “Mesenchymal stem cell perspective: cell biology to clinical progress
,” npj Regenerative Med.
4
(1
), 22
(2019
).85.
J. H.
Sung
et al, “Isolation and characterization of mouse mesenchymal stem cells
,” Transplant. Proc.
40
(8
), 2649
–2654
(2008
).86.
M.
Baddoo
et al, “Characterization of mesenchymal stem cells isolated from murine bone marrow by negative selection
,” J. Cell. Biochem.
89
, 1235
(2003
).87.
Y.
Zhao
et al, “Electrical property characterization of neural stem cells in differentiation
,” PLoS One
11
(6
), e0158044
(2016
).88.
Y.
Liu
et al, “Identification of neural stem and progenitor cell subpopulations using DC insulator-based dielectrophoresis
,” The Analyst
144
(13
), 4066
–4072
(2019
).89.
T. W.
Lin
, L.
Cardenas
, and L. J.
Soslowsky
, “Biomechanics of tendon injury and repair
,” J. Biomechanics
37
(6
), 865
–877
(2004
).90.
R.
Schweitzer
et al, “Analysis of the tendon cell fate using Scleraxis, a specific marker for tendons and ligaments
,” Development
128
(19
), 3855
–3866
(2001
). http://www.ncbi.nlm.nih.gov/pubmed/11585810.91.
Y.
Ito
et al, “The Mohawk homeobox gene is a critical regulator of tendon differentiation
,” Proc. Natl. Acad. Sci. USA
107
(23
), 10538
–10542
(2010
).92.
K.
Otabe
et al, “Transcription factor Mohawk controls tenogenic differentiation of bone marrow mesenchymal stem cells in vitro and in vivo
,” J. Orthop. Res.
33
(1
), 1
–8
(2015
).93.
Z.
Yin
et al, “Single-cell analysis reveals a nestin+ tendon stem/progenitor cell population with strong tenogenic potentiality
,” Sci. Adv.
2
(11
), e1600874
(2016
).94.
S. K.
Theodossiou
, J. B.
Murray
, and N. R.
Schiele
, “Cell-cell junctions in developing and adult tendons
,” Tissue Barriers
8
(1
), 1695491
(2020
).95.
S. H.
Richardson
, T.
Starborg
, Y.
Lu
, S. M.
Humphries
, R. S.
Meadows
, and K. E.
Kadler
, “Tendon development requires regulation of cell condensation and cell shape via cadherin-11-mediated cell-cell junctions
,” Mol. Cell. Biol.
27
(17
), 6218
–6228
(2007
).96.
R. L.
Stanley
, R. A.
Fleck
, D. L.
Becker
, A. E.
Goodship
, J. R.
Ralphs
, and J. C.
Patterson-Kane
, “Gap junction protein expression and cellularity: Comparison of immature and adult equine digital tendons
,” J. Anat.
211
, 325
–334
(2007
).97.
S. K.
Theodossiou
, J.
Tokle
, and N. R.
Schiele
, “TGFβ2-induced tenogenesis impacts cadherin and connexin cell-cell junction proteins in mesenchymal stem cells
,” Biochem. Biophys. Rev. Commun.
508
(3
), 889
–893
(2019
).98.
L. W.
Dunne
, T.
Iyyanki
, J.
Hubenak
, and A. B.
Mathur
, “Characterization of dielectrophoresis-aligned nanofibrous silk fibroin-chitosan scaffold and its interactions with endothelial cells for tissue engineering applications
,” Acta Biomater.
10
(8
), 3630
–3640
(2014
).99.
L. M.
Galatz
, L.
Gerstenfeld
, E.
Heber-Katz
, and S. A.
Rodeo
, “Tendon regeneration and scar formation: The concept of scarless healing
,” J. Orthop. Res.
33
(6
), 823
–831
(2015
).100.
K.
Howell
et al, “Novel model of tendon regeneration reveals distinct cell mechanisms underlying regenerative and fibrotic tendon healing
,” Sci. Rep.
7
, srep45238
(2017
).101.
S.
Thomopoulos
, W. C.
Parks
, D. B.
Rifkin
, and K. A.
Derwin
, “Mechanisms of tendon injury and repair
,” J. Orthop. Res.
33
(6
), 832
–839
(2015
).102.
R.
Yoshida
et al, “Murine supraspinatus tendon injury model to identify the cellular origins of rotator cuff healing
,” Connect. Tissue Res.
57
(6
), 507
–515
(2016
).103.
H. L.
Moser
et al, “Genetic lineage tracing of targeted cell populations during enthesis healing
,” J. Orthop. Res.
36
, 3275
–3284
(2018
).104.
C.
Ulbrich
et al, “The impact of simulated and real microgravity on bone cells and mesenchymal stem cells
,” Biomed. Res. Int.
2014
, 928507
.105.
D.
Grimm
et al, “The effects of microgravity on differentiation and cell growth in stem cells and cancer stem cells
,” Stem Cells Transl. Med.
9
, 882
–894
(2020
).106.
E. A.
Blaber
et al, “Microgravity reduces the differentiation and regenerative potential of embryonic stem cells
,” Stem Cells Dev.
24
(22
), 2605
–2611
(2015
).107.
D.
Grimm
et al, “Tissue engineering under microgravity conditions–use of stem cells and specialized cells
,” Stem Cells Dev.
27
(12
), 787
–804
(2018
).108.
R. P.
Schwarz
, T. J.
Goodwin
, and D. A.
Wolf
, “Cell culture for three-dimensional modeling in rotating-wall vessels: An application of simulated microgravity
,” J. Tissue Cult. Methods
14
(2
), 51
–57
(1992
).109.
S. L.
Wuest
, S.
Richard
, S.
Kopp
, D.
Grimm
, and M.
Egli
, “Simulated microgravity: critical review on the use of random positioning machines for mammalian cell culture
,” BioMed Res. Int.
2015
, 971474
.© 2020 Author(s).
2020
Author(s)
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