Open Journal Systems





Formation of cell spheroids using Standing Surface Acoustic Wave (SSAW)

VIEWS - 603 (Abstract) 224 (PDF)
Yannapol Sriphutkiat, Surasak Kasetsirikul, Yufeng Zhou

Abstract


3D bioprinting becomes one of the popular approaches in the tissue engineering. In this emerging application, bioink is crucial for fabrication and functionality of constructed tissue. The use of cell spheroids as bioink can enhance the cell-cell interaction and subsequently the growth and differentiation of cells in the 3D printed construct with the minimal amount of other biomaterials. However, the conventional methods of preparing the cell spheroids have several limitations, such as long culture time, low-throughput, and medium modification. In this study, the formation of cell spheroids by SSAW was evaluated both numerically and experimentally in order to overcome the aforementioned limitations. The effects of excitation frequencies on the cell accumulation time, diameter of formed cell spheroids, and subsequently, the growth and viability of cell spheroids in the culture media over time were studied. Using the high-frequency (24.9 MHz) excitation, cell accumulation time to the pressure nodes could be reduced in comparison to that of the low-frequency (10.4 MHz) excitation, but in a smaller spheroid size. SSAW excitation at both frequencies does not affect the cell viabilities up to 7 days, > 90% with no statistical difference compared with the control group. In summary, SSAW can effectively prepare the cell spheroids as bioink for the future 3D bioprinting and various biotechnology applications (e.g., pharmaceutical drug screening and tissue engineering).

Keywords


standing surface acoustic wave (SSAW); cell spheroid; cell viability; bioink

Full Text:

PDF

References


Ng W L, Wang S, Yeong W Y, et al., 2016, Skin bioprinting: Impending reality or fantasy? Trends Biotechnol, 35(3): 278. http://dx.doi.org/10.1016/j.tibtech.2016.04.006

Ng W L, Tan J, Yeong W Y, et al., 2018, Proof-of-concept: 3D bioprinting of pigmented human skin constructs. Biofabrication, 10.

Suntornnond R, Tan E Y S, An J, et al., 2017, A highly printable and biocompatible hydrogel composite for direct printing of soft and perfusable vasculature-like structures. Sci Rep, 7(1): 16902. http://dx.doi.org/10.1038/s41598–017–17198–0

Olubamiji A D, Izadifar Z, Si J L, et al., 2016, Modulating mechanical behaviour of 3D-printed cartilage-mimetic PCL scaffolds: Influence of molecular weight and pore geometry. Biofabrication, 8(2): 025020. http://dx.doi.org/10.1088/1758–5090/8/2/025020

Sing S L, An J, Yeong W Y, et al., 2016, Laser and electron-beam powder-bed additive manufacturing of metallic implants: A review on processes, materials and designs. J Orthop Res, 34(3): 369–385. http://dx.doi.org/10.1002/jor.23075

Zhuang P, Sun A X, An J, et al., 2018, 3D neural tissue models: From spheroids to bioprinting. Biomaterials, 154: 113–133. http://dx.doi.org/10.1016/j.biomaterials.2017.10.002

Lee J M, Sing S L, Tan E Y S, et al., 2016, Bioprinting in cardiovascular tissue engineering: A review. Int J Bioprint, 2: 27–36. http://dx.doi.org/10.18063/Ijb.2016.02.006

Kolesky D B, Truby R L, Gladman A, et al., 2014, 3D bioprinting of vascularized, heterogeneous cell-laden tissue constructs. Adv Mater, 26(19): 3124–3130. http://dx.doi.org/10.1002/adma.201305506

Murphy S V, Atala A, 2014, 3D bioprinting of tissues and organs. Nat Biotechnology, 32(8): 773–785. http://dx.doi.org/10.1038/nbt.2958

Mehrban N, Teoh G Z, Birchall M A, 2016, 3D bioprinting for tissue engineering: Stem cells in hydrogels. Int J Bioprint, 2: 6–19. http://dx.doi.org/10.18063/Ijb.2016.01.006

Ji S, Guvendiren M, 2017, Recent advances in bioink design for 3D bioprinting of tissues and organs. Front Bioeng Biotechnol, 5: 23. http://dx.doi.org/10.3389/fbioe.2017.00023

Lin R Z, Chang H Y, 2008, Recent advances in three-dimensional multicellular spheroid culture for biomedical research. Biotechnol J, 3(9–10): 1172–1184. http://dx.doi.org/10.1002/biot.200700228

Page H, Flood P, Reynaud E G, 2013, Three-dimensional tissue cultures: Current trends and beyond. Cell Tissue Res, 352(1): 123–131. http://dx.doi.org/10.1007/s00441–012–1441–5

LeCluyse E L, Bullock P L, Parkinson A, 1996, Strategies for restoration and maintenance of normal hepatic structure and function in long-term cultures of rat hepatocytes. Adv Drug Deliv Rev, 22(1): 133–186. http://dx.doi.org/10.1016/S0169–409x(96)00418–8

Shepherd J A, Kerlikowske K, Ma L, et al., 2011, Volume of mammographic density and risk of breast cancer. Cancer Epidemiol Biomarkers Prev, 20(7): 1473–1482. http://dx.doi.org/10.1158/1055–9965.EPI–10–1150

Yuasa C, Tomita Y, Shono M, et al., 1993, Importance of cell aggregation for expression of liver functions and regeneration demonstrated with primary cultured hepatocytes. J Cell Physiol, 156(3): 522–530. http://dx.doi.org/10.1002/jcp.1041560311

Takabatake H, Koide N, Tsuji T, 1991, Encapsulated multicellular spheroids of rat hepatocytes produce albumin and urea in a spouted bed circulating culture system. Artif Organs, 15(6): 474–80.

Landry J, Bernier D, Ouellet C, et al., 1985, Spheroidal aggregate culture of rat liver cells: Histotypic reorganization, biomatrix deposition, and maintenance of functional activities. J Cell Biol, 101(3): 914–923. http://dx.doi.org/https://doi.org/10.1083/jcb.101.3.914

Edmondson R, Broglie J J, Adcock A F, et al., 2014, Three-dimensional cell culture systems and their applications in drug discovery and cell-based biosensors. Assay Drug Dev technol, 12(4): 207–218. http://dx.doi.org/10.1089/adt.2014.573

Imamura Y, Mukohara T, Shimono Y, et al., 2015, Comparison of 2D-and 3D-culture models as drug-testing platforms in breast cancer. Oncol Rep, 33(4): 1837–1843. http://dx.doi.org/10.3892/or.2015.3767

Xu J S, Ma M W, Purcell W M, 2003, Characterisation of some cytotoxic endpoints using rat liver and HepG2 spheroids as in vitro models and their application in hepatotoxicity studies. I. Glucose metabolism and enzyme release as cytotoxic markers. Toxicol Appl Pharmacol, 189(2): 112–119. http://dx.doi.org/10.1016/S0041–008x(03)00089–9

Mandal B B, Kundu S C, 2009, Cell proliferation and migration in silk fibroin 3D scaffolds. Biomaterials, 30(15): 2956–2965. http://dx.doi.org/10.1016/j.biomaterials.2009.02.006

Young E W, Beebe D J, 2010, Fundamentals of microfluidic cell culture in controlled microenvironments. Chem Soc Rev, 39(3): 1036–1048. http://dx.doi.org/10.1039/b909900j

Norotte C, Marga F S, Niklason L E, et al., 2009, Scaffold-free vascular tissue engineering using bioprinting. Biomaterials, 30(30): 5910–5917. http://dx.doi.org/10.1016/j.biomaterials.2009.06.034

Ozbolat I T, Yu Y, 2013, Bioprinting toward organ fabrication: Challenges and future trends. IEEE Trans Biomed Eng, 60(3): 691–699. http://dx.doi.org/10.1109/TBME.2013.2243912

Lee J, Sato M, Kim H, et al., 2011, Transplantation of scaffold-free spheroids composed of synovium-derived cells and chondrocytes for the treatment of cartilage defects of the knee. Eur Cell Mater, 22: 275–290. http://dx.doi.org/https://doi.org/10.22203/ecm.v022a21

Timmins N E, Dietmair S, Nielsen L K, 2004, Hanging-drop multicellular spheroids as a model of tumour angiogenesis. Angiogenesis, 7(2): 97–103. http://dx.doi.org/10.1007/s10456–004–8911–7

Albrecht D R, Underhill G H, Wassermann T B, et al., 2006, Probing the role of multicellular organization in three-dimensional microenvironments. Nat Methods, 3(5): 369–375. http://dx.doi.org/10.1038/nmeth873

Souza G R, Molina J R, Raphael R M, et al., 2010, Three-dimensional tissue culture based on magnetic cell levitation. Nat Nanotechnol, 5(4): 291–296, http://dx.doi.org/10.1038/nnano.2010.23

Ingram M, Techy G B, Saroufeem R, et al., 1997, Three-dimensional growth patterns of various human tumor cell lines in simulated microgravity of a NASA bioreactor. In Vitro Cell Dev Biol Anim, 33(6): 459–466. http://dx.doi.org/10.1007/s11626–997–0064–8

Napolitano A P, Chai P, Dean D M, et al., 2007, Dynamics of the self-assembly of complex cellular aggregates on micromolded nonadhesive hydrogels. Tissue Eng, 13(8): 2087–2094. http://dx.doi.org/10.1089/ten.2006.0190

Semino C E, Merok J R, Crane G G, et al., 2003, Functional differentiation of hepatocyte-like spheroid structures from putative liver progenitor cells in three-dimensional peptide scaffolds. Differentiation, 71(4–5): 262–270. http://dx.doi.org/10.1046/j.1432–0436.2003.7104503.x

Ng W L, Lee J M, Yeong W Y, et al., 2017, Microvalve-based bioprinting–Process, bio-inks and applications. Biomater Sci, 5(4): 632–647. http://dx.doi.org/10.1039/c6bm00861e

Faulkner-Jones A, Greenhough S, King J A, et al., 2013, Development of a valve-based cell printer for the formation of human embryonic stem cell spheroid aggregates. Biofabrication, 5(1): 015013. http://dx.doi.org/10.1088/1758–5082/5/1/015013

Bazou D, Kearney R, Mansergh F, et al., 2011, Gene expression analysis of mouse embryonic stem cells following levitation in an ultrasound standing wave trap. Ultrasound Med Biol, 37(2): 321–330. http://dx.doi.org/10.1016/j.ultrasmedbio.2010.10.019

Chen K, Wu M, Guo F, et al., 2016, Rapid formation of size-controllable multicellular spheroids via 3D acoustic tweezers. Lab Chip, 16(14): 2636–2643. http://dx.doi.org/10.1039/c6lc00444j

Collins D J, Morahan B, Garcia-Bustos J, et al., 2015, Two-dimensional single-cell patterning with one cell per well driven by surface acoustic waves. Nat Commun, 6: 8686. http://dx.doi.org/10.1038/ncomms9686

Wiklund M, 2012, Acoustofluidics 12: Biocompatibility and cell viability in microfluidic acoustic resonators. Lab Chip, 12(11): 2018–2028. http://dx.doi.org/10.1039/c2lc40201g

Ohlin M, Iranmanesh I, Christakou A E, et al., 2015, Temperature-controlled MPa-pressure ultrasonic cell manipulation in a microfluidic chip. Lab Chip, 15(16): 3341–3349. http://dx.doi.org/10.1039/c5lc00490j

Glynne-Jones P, Hill M, 2013, Acoustofluidics 23: Acoustic manipulation combined with other force fields. Lab Chip, 13(6): 1003–1010. http://dx.doi.org/10.1039/c3lc41369a

Bruus H, 2012, Acoustofluidics 7: The acoustic radiation force on small particles. Lab Chip, 12(6): 1014–1021. http://dx.doi.org/10.1039/c2lc21068a

Sriphutkiat Y, Zhou Y, 2017, Particle manipulation using standing acoustic waves in the microchannel at dual-frequency excitation: Effect of power ratio. Sensor Actuat A Phys, 263: 521–529. http://dx.doi.org/10.1016/j.sna.2017.07.023

Burgess A, Vigneron S, Brioudes E, et al., 2010, Loss of human Greatwall results in G2 arrest and multiple mitotic defects due to deregulation of the cyclin B-Cdc2/PP2A balance. Pro Nati Acad Sci, 107(28): 12564–12569. http://dx.doi.org/10.1073/pnas.0914191107

McCloy R A, Rogers S, Caldon C E, et al., 2014, Partial inhibition of Cdk1 in G2 phase overrides the SAC and decouples mitotic events. Cell Cycle, 13(9): 1400–1412. http://dx.doi.org/10.4161/cc.28401

Cui X, Hartanto Y, Zhang H, 2017, Advances in multicellular spheroids formation. J R Soc Interface, 14: 20160877.

Chen Y, Li P, Huang P H, et al., 2014, Rare cell isolation and analysis in microfluidics. Lab Chip, 14(4): 626–645. http://dx.doi.org/10.1039/c3lc90136j

Ding X, Peng Z, Lin S C, et al., 2014, Cell separation using tilted-angle standing surface acoustic waves. Pro Nati Acad Sci USA, 111(36): 12992–12997. http://dx.doi.org/10.1073/pnas.1413325111

Sriphutkiat Y, Zhou Y, 2017, Particle Accumulation in a microchannel and its reduction by a standing surface acoustic wave (SSAW). Sensors, 17(1): 106. http://dx.doi.org/10.3390/s17010106

Hartono D, Liu Y, Tan P L, et al., 2011, On-chip measurements of cell compressibility via acoustic radiation. Lab Chip, 11(23): 4072–4080. http://dx.doi.org/10.1039/c1lc20687g

Nama N, Barnkob R, Mao Z, et al., 2015, Numerical study of acoustophoretic motion of particles in a PDMS microchannel driven by surface acoustic waves. Lab Chip, 15(12): 2700–2709. http://dx.doi.org/10.1039/c5lc00231a

Burguillos M A, Magnusson C, Nordin M, et al., 2013, Microchannel acoustophoresis does not impact survival or function of microglia, leukocytes or tumor cells. Plos One, 8: e64233. http://dx.doi.org/10.1371/journal.pone.0064233

Ding X Y, Shi J J, Lin S C S, et al., 2012, Tunable patterning of microparticles and cells using standing surface acoustic waves. Lab Chip, 12(14): 2491–2497. http://dx.doi.org/10.1039/c2lc21021e

Devendran C, Albrecht T, Brenker J, et al., 2016, The importance of travelling wave components in standing surface acoustic wave (SSAW) systems. Lab Chip, 16(19): 3756–3766. http://dx.doi.org/10.1039/c6lc00798h

Squires T, 2005, Microfluidics: Fluid physics at the nanoliter scale. Rev Mod Phys, 7(3): 977–1026. http://dx.doi.org/10.1103/RevModPhys.77.977

Lee P J, Hung P J, Rao V M, et al., 2006, Nanoliter scale microbioreactor array for quantitative cell biology. Biotechnol Bioeng, 94(1): 5–14. http://dx.doi.org/10.1002/bit.20745

Wang Z, Kim M C, Marquez M, et al., 2007, High-density microfluidic arrays for cell cytotoxicity analysis. Lab Chip, 7(6): 740–745. http://dx.doi.org/10.1039/b618734j

Melchels F P, Barradas A M, van Blitterswijk C A, et al., 2010, Effects of the architecture of tissue engineering scaffolds on cell seeding and culturing. Acta Biomater, 6(11): 4208–4217. http://dx.doi.org/10.1016/j.actbio.2010.06.012

Lichtner R B, Schirrmacher V, 1990, Cellular distribution and biological activity of epidermal growth factor receptors in A431 cells are influenced by cell-cell contact. J Cell Physiol, 144(2): 303–312. http://dx.doi.org/10.1002/jcp.1041440217

Henry C, Minier J P, Lefevre G, 2012, Towards a description of particulate fouling: From single particle deposition to clogging. Adv Colloid Interface Sci, 185–186: 34–76. http://dx.doi.org/10.1016/j.cis.2012.10.001

Mustin B, Stoeber B, 2016, Single layer deposition of polystyrene particles onto planar polydimethylsiloxane substrates. Langmuir, 32(1): 88–101. http://dx.doi.org/10.1021/acs.langmuir.5b02914

Devendran C, Albrecht T, Brenker J, et al., 2016, The importance of travelling wave components in standing surface acoustic wave (SSAW) systems. Lab Chip, 16(19): 3756–3766. http://dx.doi.org/10.1039/c6lc00798h

Drasdo D, Hohme S, 2005, A single-cell-based model of tumor growth in vitro: Monolayers and spheroids. Phys Biol, 2(3): 133–147. http://dx.doi.org/10.1088/1478-3975/2/3/001

Engelberg J A, Ropella G E, Hunt C A, 2008, Essential operating principles for tumor spheroid growth. BMC Syst Biol, 2: 110. http://dx.doi.org/10.1186/1752–0509–2–110

Zanoni M, Piccinini F, Arienti C, et al., 2016, 3D tumor spheroid models for in vitro therapeutic screening: A systematic approach to enhance the biological relevance of data obtained. Sci Rep, 6: 19103. http://dx.doi.org/10.1038/srep19103

Anada T, Fukuda J, Sai Y, et al., 2012, An oxygen-permeable spheroid culture system for the prevention of central hypoxia and necrosis of spheroids. Biomaterials, 33(33): 8430–8441. http://dx.doi.org/10.1016/j.biomaterials.2012.08.040

Glicklis R, Merchuk J C, Cohen S, 2004, Modeling mass transfer in hepatocyte spheroids via cell viability, spheroid size, and hepatocellular functions. Biotechnol Bioeng, 86(6): 672–680. http://dx.doi.org/10.1002/bit.20086

Lee J, Cuddihy M J, Cater G M, et al., 2009, Engineering liver tissue spheroids with inverted colloidal crystal scaffolds. Biomaterials, 30(27): 4687–4694. http://dx.doi.org/10.1016/j.biomaterials.2009.05.024

Curcio E, Salerno S, Barbieri G, et al., 2007, Mass transfer and metabolic reactions in hepatocyte spheroids cultured in rotating wall gas-permeable membrane system. Biomaterials, 28(36): 5487–5497. http://dx.doi.org/10.1016/j.biomaterials.2007.08.033

Fukuda J, Okamura K, Nakazawa K, et al., 2003, Efficacy of a polyurethane foam/spheroid artificial liver by using human hepatoblastoma cell line (Hep G2). Cell Transplant, 12(1): 51–58. http://dx.doi.org/10.3727/000000003783985151

Tamura T, Sakai Y, Nakazawa K, 2008, Two-dimensional microarray of HepG2 spheroids using collagen/polyethylene glycol micropatterned chip. J Mater Sci Mater M, 19(5): 2071–2077. http://dx.doi.org/10.1007/s10856–007–3305–1

Hirschhaeuser F, Menne H, Dittfeld C, et al., 2010, Multicellular tumor spheroids: An underestimated tool is catching up again. J Biotechnol, 148(1): 3–15. http://dx.doi.org/10.1016/j.jbiotec.2010.01.012




DOI: http://dx.doi.org/10.18063/ijb.v4i1.130

Refbacks

  • There are currently no refbacks.


Copyright (c) 2018 YANNAPOL SRIPHUTKIAT, Surasak Kasetsirikul, Yufeng Zhou

Creative Commons License
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

Recent Articles | About Journal | For Author | Fees | About Whioce

Copyright © Whioce Publishing Pte Ltd. All Rights Reserved.