CHEMICAL ENGINEERING METHODS IN ANALYSES OF 3D CANCER CELL CULTURES: HYDRODYNAMIC AND MASS TRANSPORT CONSIDERATIONS

Scientific paper

Authors

  • Mia Radonjić Faculty of Technology and Metallurgy, University of Belgrade, Belgrade, Serbia and Innovation Center of the Faculty of Technology and Metallurgy, Belgrade, Serbia https://orcid.org/0000-0003-3376-4317
  • Jelena Petrović Faculty of Technology and Metallurgy, University of Belgrade, Belgrade, Serbia + Innovation Center of the Faculty of Technology and Metallurgy, Belgrade, Serbia https://orcid.org/0000-0001-9161-4806
  • Milena Milivojević Institute of Molecular Genetics and Genetic Engineering, University of Belgrade, Belgrade, Serbia
  • Milena Stevanović Institute of Molecular Genetics and Genetic Engineering, University of Belgrade, Belgrade, Serbia + Faculty of Biology, University of Belgrade, Belgrade, Serbia and Serbian Academy of Sciences and Arts, Belgrade, Serbia https://orcid.org/0000-0003-4286-7334
  • Jasmina Stojkovska Faculty of Technology and Metallurgy, University of Belgrade, Belgrade, Serbia and Innovation Center of the Faculty of Technology and Metallurgy, Belgrade, Serbia
  • Bojana Obradović Faculty of Technology and Metallurgy, University of Belgrade, Karnegijeva 4, Belgrade, Serbia https://orcid.org/0000-0002-7276-0442

DOI:

https://doi.org/10.2298/CICEQ210607033R

Keywords:

tumor engineering, alginate hydrogel, perfusion bioreactor, mathematical modeling, glioma C6 cell line, embryonic teratocarcinoma NT2/D1 cell line

Abstract

A multidisciplinary approach based on experiments and mathematical modeling was used in biomimetic system development for three-dimensional (3D) cultures of cancer cells. Specifically, two cancer cell lines, human embryonic teratocarcinoma NT2/D1 and rat glioma C6, were immobilized in alginate microbeads and microfibers, respectively, and cultured under static and flow conditions in perfusion bioreactors. At the same time, chemical engineering methods were applied to explain the obtained results. The superficial medium velocity of 80 μm s-1 induced lower viability of NT2/D1 cells in superficial microbead zones, implying adverse effects of fluid shear stresses estimated as ∼67 mPa. On the contrary, similar velocity (100 μm s-1) enhanced the proliferation of C6 glioma cells within microfibers compared to static controls. An additional study of silver release from nanocomposite Ag/honey/alginate microfibers under perfusion indicated that the medium partially flows through the hydrogel (interstitial velocity of ∼10 nm s-1). Thus, a diffusion-advection-reaction model described the mass transport to immobilized cells within microfibers. Substances with diffusion coefficients of ∼10-9-10-11 m2 s-1 are sufficiently supplied by diffusion only, while those with significantly lower diffusivities (∼10-19 m2 s-1) require additional convective transport. The present study demonstrates the selection and contribution of chemical engineering methods in tumor model system development.

References

H. Sung, J. Ferlay, R.L. Siegel, M. Laversanne, I. Soerjomataram, A. Jemal, F. Bray, Ca-Cancer J. Clin. 71 (2021) 209-249.

M. Kapałczyńska, T. Kolenda, W. Przybyła, M. Zajączkowska, A. Teresiak, V. Filas, M. Ibbs, R. Bliźniak, Ł. Łuczewski, K. Lamperska, Arch. Med. Sci. 14 (2018) 910-919.

H. Ungefroren, S. Sebens, D. Seidl, H. Lehnert, R. Hass, Cell Commun. Signaling 9 (2011) 1-8.

J.A. Hickman, R. Graeser, R. de Hoogt, S. Vidic, C. Brito, M. Gutekunst, H. van der Kuip, Biotechnol. J. 9 (2014) 1115-1128.

A. Nyga, U. Cheema, M. Loizidou, J. Cell Commun. Signaling 5 (2011) 239-248.

M.D. Szeto, G. Chakraborty, J. Hadley, R. Rockne, M. Muzi, E.C. Alvord, K.A. Krohn, A.M. Spence, K.R. Swanson, Cancer Res. 69 (2009) 4502-4509.

N. Filipovic, T. Djukic, I. Saveljic, P. Milenkovic, G. Jovicic, M. Djuric, Comput. Methods Programs Biomed. 115 (2014) 162-170.

P. Caccavale, M.V. De Bonis, G. Marino, G. Ruocco, Int. Commun. Heat Mass Transfer 117 (2020) 104781.

T. Chen, N.F. Kirkby, R. Jena, Comput. Methods Programs Biomed. 108 (2012) 973-983.

D. Karami, N. Richbourg, V. Sikavitsas, Cancer Lett. (N. Y., NY, U. S.) 449 (2019) 178-185.

D. Massai, G. Isu, D. Madeddu, G. Cerino, A. Falco, C. Frati, D. Gallo, M.A. Deriu, G. Falvo D’Urso Labate, F. Quaini, A. Audenino, U. Morbiducci, PloS One 11 (2016) e0154610.

J.E. Trachtenberg, M. Santoro, C. Williams III, C.M. Piard, B.T. Smith, J.K. Placone, B.A. Menegaz, E.R. Molina, S.-E. Lamhamedi-Cherradi, J.A. Ludwig, V.I. Sikavitsas, J.P. Fisher, A.G. Mikos, ACS Biomater. Sci. Eng. 4 (2018) 347-356.

C.M. Novak, E.N. Horst, C.C. Taylor, C.Z. Liu, G. Mehta, Biotechnol. Bioeng. 116 (2019) 3084-3097.

V.S. Shirure, S.F. Lam, B. Shergill, Y.E. Chu, N.R. Ng, S.C. George, Lab Chip 20 (2020) 3036-3050.

K.Y. Lee, D.J. Mooney, Prog. Polym. Sci. 37 (2012) 106-126.

K.I. Draget, G. Skjåk-Bræk, O. Smidsrød, Int. J. Biol. Macromol. 21 (1997) 47-55.

P. Sánchez, R.M. Hernández, J.L. Pedraz, G. Orive, in

Immobilization of Enzymes and Cells, Humana Press, Totowa, NJ (2013) 313-325.

B.R. Lee, K.H. Lee, E. Kang, D.S. Kim, S.H. Lee, Biomicrofluidics 5 (2011) 022208.

F.M. Kievit, S.J. Florczyk, M.C. Leung, O. Veiseh, J.O. Park, M.L. Disis, M. Zhang, Biomaterials 31 (2010) 5903-5910.

M. Leung, F.M. Kievit, S.J. Florczyk, O. Veiseh, J. Wu, J.O. Park, M. Zhang, Pharm. Res. 27 (2010) 1939-1948.

S.J. Florczyk, G. Liu, F.M. Kievit, A.M. Lewis, J.D. Wu, M. Zhang, Adv. Healthcare Mater. 1 (2012) 590-599.

Q. Wang, S. Li, Y. Xie, W. Yu, Y. Xiong, X. Ma, Q. Yuan, Hepatol. Res. 35 (2006) 96-103.

M.L. Tang, X.J. Bai, Y. Li, X.J. Dai, F. Yang, Curr. Med. Sci. 38 (2018) 809-817.

C. Liu, D.L. Mejia, B. Chiang, K.E. Luker, G.D. Luker, Acta Biomater. 75 (2018) 213-225.

N. Chaicharoenaudomrung, P. Kunhorm, W. Promjantuek, N. Heebkaew, N. Rujanapun, P. Noisa, J. Cell. Physiol. 234 (2019) 20085-20097.

K. Xu, K. Ganapathy, T. Andl, Z. Wang, J.A. Copland, R. Chakrabarti, S.J. Florczyk, Biomaterials 217 (2019) 119311.

L.E. Marshall, K.F. Goliwas, L.M. Miller, A.D. Penman, A.R. Frost, J.L. Berry, J. Tissue Eng. Regener. Med. 11 (2017) 1242-1250.

M. Santoro, S.E. Lamhamedi-Cherradi, B.A. Menegaz, J.A. Ludwig, A.G. Mikos, Proc. Natl. Acad. Sci. U. S. A. 112 (2015) 10304-10309.

X. Wan, Z. Li, H. Ye, Z. Cui, Biotechnol. Lett. 38 (2016) 1389-1395.

M.G. Muraro, S. Muenst, V. Mele, L. Quagliata, G. Iezzi, A. Tzankov, W.P. Weber, G.C. Spagnoli, S.D. Soysal, OncoImmunology 6 (2017) e1331798.

X. Wan, S. Ball, F. Willenbrock, S. Yeh, N. Vlahov, D. Koennig, M. Green, G. Brown, S. Jeyaretna, Z. Li, Z. Cui, H. Ye, E. O’Neill, Sci. Rep. 7 (2017) 1-13.

C. Manfredonia, M.G. Muraro, C. Hirt, V. Mele, V. Governa, A. Papadimitropoulos, S. Däster, S.D. Soysal, R.A. Droeser, R. Mechera, D. Oertli, R. Rosso, M. Bolli, A. Zettl, L.M. Terracciano, G.C. Spagnoli, I. Martin, G. Iezzi, Adv. Biosyst. 3 (2019) 1800300.

C. Hirt, A. Papadimitropoulos, M.G. Muraro, V. Mele, E. Panopoulos, E. Cremonesi, R. Ivanek, E. Schultz-Thater, R. Droeser, C. Mengus, M. Hebeber, D. Oertli, G. Iezzi, P. Zajac, S. Eppenberger-Castori, L. Tornillo, L. Terracciano, I. Martin, G.C. Spagnoli, Biomaterials 62 (2015) 138-146.

F. Foglietta, G.C. Spagnoli, M.G. Muraro, M. Ballestri, A. Guerrini, C. Ferroni, A. Aluigi, G. Sotgiu, G. Varchi, Int. J. Nanomed. 13 (2018) 4847-4867.

H. Qazi, Z.-D. Shi, J.M. Tarbell, PloS One 6 (2011) e20348.

D.H. Tryoso, D.A. Good, J. Physiol. 515.2 (1999) 355-365.

L. Ziko, S. Riad, M. Amer, R. Zdero, H. Bougherara, A. Amleh, Biomed. Res. Int. 2015 (2015), ID 430569.

A. Marrella, A. Fedi, G. Varani, I. Vaccari, M. Fato, G. Firpo, P. Guida, N, Aceto, S. Scaglione, PLoS One 16 (2021) e0245536.

J. Stojkovska, B. Bugarski, B. Obradovic, J. Mater. Sci.: Mater. Med. 21 (2010) 2869-2879.

A. Osmokrovic, B. Obradovic, D. Bugarski, B. Bugarski, G. Vunjak-Novakovic, FME Trans. 34 (2006) 65-70.

J. Stojkovska, J. Zvicer, M. Milivojević, I. Petrović, M. Stevanović, B. Obradović, Hem. Ind. 74 (2020) 187-196.

J. Stojkovska, P. Petrovic, I. Jancic, M.T. Milenkovic, B. Obradovic, Appl. Microbiol. Biotechnol.103 (2019) 8529-8543.

J. Stojkovska, J. Zvicer, Ž. Jovanović, V. Mišković-Stanković, B. Obradović, J. Serb. Chem. Soc. 77 (2012) 1709-1722.

D.D. Kostic, I.S. Malagurski, B.M. Obradovic, Hem. Ind. 71 (2017) 383-394.

R.G. Holdich, Fundamentals of particle technology, Midland Information Technology and Publishing, Hathern, Leicestershire (2002) 45-54.

E. Fröhlich, G. Bonstingl, A. Höfler, C. Meindl, G. Leitinger, T.R. Pieber, E. Roblegg, Toxicol. In Vitro 27 (2013) 409-417.

M.J. Mitchell, M.R. King, Front. Oncol. 3 (2013) 44.

Y. Chen, R. Cairns, I. Papandreou, A. Koong, N.C. Denko, PloS One 4 (2009) e7033.

A. Gomes, L. Guillaume, D.R. Grimes, J. Fehrenbach, V. Lobjois, B. Ducommun, PloS One 11 (2016) e0161239.

Y. Shen, X. Li, D. Dong, B. Zhang, Y. Xue, P. Shang, Am. J. Cancer Res. 8 (2018) 916-931.

D. Kostic, S. Vidovic, B. Obradovic, J. Nanopart. Res. 18 (2016) 76-92.

A.C. Hulst, H.J.H. Hens, R.M. Buitelaar, J. Tramper, Biotechnol. Tech. 3 (1989) 199-204.

T.L. Place, F.E. Domann, A.J. Case, Free Radical Biol. Med. 113 (2017) 311-322.

B.A. Wagner, S. Venkataraman, G.R. Buettner, Free Radical Biol. Med. 51 (2011) 700-712.

X. Hong, Y. Meng, S.N. Kalkanis, J. Biol. Methods 3 (2016) e51.

A. Ciechanover, A.L. Schwartz, A. Dautry-Varsat, H.F. Lodish, J. Biol. Chem. 258 (1983) 9681-9689.

R. Zadro, B. Pokrić, Z. Pučar, Anal. Biochem. 117 (1981) 238-244.

P. Aisen, I. Listowsky, Annu. Rev. Biochem. 49 (1980) 357-393.

J.R. Kanwar, G. Mahidhara, R.K. Kanwar, Nanomedicine 7 (2012) 1521-1550.

J. Wally, S.K. Buchanan, BioMetals 20 (2007) 249-262.

Downloads

Published

17.09.2021 — Updated on 25.05.2022

Issue

Vol. 28 No. 3 (2022)

Section

Articles

License

Copyright (c) 2022 Mia Radonjić, Jelena Petrović, Milena Milojević, Milena Stevanović, Jasmina Stojkovska, Bojana Obradović

Creative Commons License

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

Authors who publish with this journal agree to the following terms:

Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.

Authors grant to the Publisher the following rights to the manuscript, including any supplemental material, and any parts, extracts or elements thereof:

  • the right to reproduce and distribute the Manuscript in printed form, including print-on-demand;
  • the right to produce prepublications, reprints, and special editions of the Manuscript;
  • the right to translate the Manuscript into other languages;
  • the right to reproduce the Manuscript using photomechanical or similar means including, but not limited to photocopy, and the right to distribute these reproductions;
  • the right to reproduce and distribute the Manuscript electronically or optically on any and all data carriers or storage media – especially in machine readable/digitalized form on data carriers such as hard drive, CD-Rom, DVD, Blu-ray Disc (BD), Mini-Disk, data tape – and the right to reproduce and distribute the Article via these data carriers; 
  • the right to store the Manuscript in databases, including online databases, and the right of transmission of the Manuscript in all technical systems and modes;
  • the right to make the Manuscript available to the public or to closed user groups on individual demand, for use on monitors or other readers (including e-books), and in printable form for the user, either via the internet, other online services, or via internal or external networks.

How to Cite

CHEMICAL ENGINEERING METHODS IN ANALYSES OF 3D CANCER CELL CULTURES: HYDRODYNAMIC AND MASS TRANSPORT CONSIDERATIONS: Scientific paper. (2022). Chemical Industry & Chemical Engineering Quarterly, 28(3), 211-223. https://doi.org/10.2298/CICEQ210607033R

Similar Articles

1-10 of 134

You may also start an advanced similarity search for this article.