Fluorescent oxygen sensitive microbead incorporation for measuring oxygen tension in cell aggregates.

Animals; Biological Assay/methods; Cell Aggregation/physiology; Cell Line; Chondrocytes/cytology/metabolism; Mice; Microspheres; Molecular Imaging/methods; Oximetry/methods; Oxygen/analysis; Oxygen Consumption/physiology; Spectrometry, Fluorescence/methods

Abstract :

[en] Molecular oxygen is a main regulator of various cell functions. Imaging methods designed as screening tools for fast, in situ, 3D and non-interfering measurement of oxygen tension in the cellular microenvironment would serve great purpose in identifying and monitoring this vital and pivotal signalling molecule. We describe the use of dual luminophore oxygen sensitive microbeads to measure absolute oxygen concentrations in cellular aggregates. Stable microbead integration, a prerequisite for their practical application, was ensured by a site-specific delivery method that is based on the interactions between streptavidin and biotin. The spatial stability introduced by this method allowed for long term measurements of oxygen tension without interfering with the cell aggregation process. By making multiple calibration experiments we further demonstrated the potential of these sensors to measure local oxygen tension in optically dense cellular environments.

Disciplines :

Engineering, computing & technology: Multidisciplinary, general & others

Author, co-author :

Lambrechts, Dennis

Roeffaers, Maarten

Kerckhofs, Greet ; Université de Liège - ULiège > Département d'aérospatiale et mécanique > Génie biomécanique

Roberts, Scott J.

Hofkens, Johan

Van de Putte, Tom

Van Oosterwyck, Hans

Schrooten, Jan

Language :

English

Title :

Fluorescent oxygen sensitive microbead incorporation for measuring oxygen tension in cell aggregates.

Publication date :

2013

Journal title :

Biomaterials

ISSN :

0142-9612

eISSN :

1878-5905

Publisher :

IPC Science and Technology Press, Netherlands

Volume :

Issue :

Pages :

922-9

Peer reviewed :

Peer Reviewed verified by ORBi

Commentary :

Available on ORBi :

since 14 November 2013

Statistics

Number of views

71 (1 by ULiège)

Number of downloads

243 (1 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

Bibliography

Griffith L.G., Swartz M.A. Capturing complex 3D tissue physiology in vitro. Nat Rev Mol Cell Bio 2006, 7:211-224.
Glicklis R., Merchuk J.C., Cohen S. Modeling mass transfer in hepatocyte spheroids via cell viability, spheroid size, and hepatocellular functions. Biotechnol Bioeng 2004, 86:672-680.
Demol J., Lambrechts D., Geris L., Schrooten J., Van Oosterwyck H. Towards a quantitative understanding of oxygen tension and cell density evolution in fibrin hydrogels. Biomaterials 2011, 32:107-118.
Beard D.A., Qian H. Chemical biophysics: quantitative analysis of cellular systems 2008, Cambridge University Press, New York.
Radisic M., Malda J., Epping E., Geng W.L., Langer R., Vunjak-Novakovic G. Oxygen gradients correlate with cell density and cell viability in engineered cardiac tissue. Biotechnol Bioeng 2006, 93:332-343.
Derda R., Laromaine A., Mammoto A., Tang S.K., Mammoto T., Ingber D.E., et al. Paper-supported 3D cell culture for tissue-based bioassays. Proc Natl Acad Sci U S A 2009, 106:18457-18462.
Kim J.W., Tchernyshyov I., Semenza G.L., Dang C.V. HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab 2006, 3:177-185.
Lahiri S., Roy A., Baby S.M., Hoshi T., Semenza G.L., Prabhakar N.R. Oxygen sensing in the body. Prog Biophys Mol Biol 2006, 91:249-286.
Hochachka P.W., Lutz P.L. Mechanism, origin, and evolution of anoxia tolerance in animals. Comp Biochem Physiol B 2001, 130:435-459.
Hochachka P.W., Buck L.T., Doll C.J., Land S.C. Unifying theory of hypoxia tolerance: molecular metabolic defense and rescue mechanisms for surviving oxygen lack. Proc Natl Acad Sci U S A 1996, 93:9493-9498.
Karsenty G., Wagner E.F. Reaching a genetic and molecular understanding of skeletal development. Dev Cell. 2002, 2:389-406.
Hall B.K., Miyake T. Divide, accumulate, differentiate: cell condensation in skeletal development revisited. Int J Dev Biol 1995, 39:881-893.
Archer C.W., Rooney P., Wolpert L. Cell-shape and cartilage differentiation of early chick limb bud cells in culture. Cell Differ Dev 1982, 11:245-251.
Abbott J., Holtzer H. Loss of phenotypic traits by differentiated cells.v. effect of 5-bromodeoxyuridine on cloned chondrocytes. Proc Natl Acad Sci U S A 1968, 59:1144-1151.
Caplan A.I., Koutroup S. Control of muscle and cartilage development in chick limb - role of differential vascularization. J Embryol Exp Morphol 1973, 29:571-583.
Lambrechts D., Schrooten J., Van de Putte T., Van Oosterwyck H. Computational modeling of mass transport and its relation to cell behavior in tissue engineering constructs. Studies in mechanobiology, tissue engineering and biomaterials 2012, Springer-Verlag, Berlin Heidelberg. L. Geris (Ed.).
Welter J.F., Solchaga L.A., Penick K.J. Simplification of aggregate culture of human mesenchymal stem cells as a chondrogenic screening assay. Biotechniques 2007, 42:732-737.
Lenas P., Moos M., Luyten F.P. Developmental engineering: a new paradigm for the design and manufacturing of cell-based products. Part I: from three-dimensional cell growth to biomimetics of in vivo development. Tissue Eng Part B Rev 2009, 15:381-394.
Barbero A., Scotti C., Tonnarelli B., Papadimitropoulos A., Scherberich A., Schaeren S., et al. Recapitulation of endochondral bone formation using human adult mesenchymal stem cells as a paradigm for developmental engineering. Proc Natl Acad Sci U S A 2010, 107:7251-7256.
Wolf F., Candrian C., Wendt D., Farhadi J., Heberer M., Martin I., et al. Cartilage tissue engineering using pre-aggregated human articular chondrocytes. Eur Cell Mater 2008, 16:92-99.
Gallez B., Baudelet C., Jordan B.F. Assessment of tumor oxygenation by electron paramagnetic resonance: principles and applications. NMR Biomed 2004, 17:240-262.
Vikram D.S., Zweier J.L., Kuppusamy P. Methods for noninvasive imaging of tissue hypoxia. Antioxid Redox Signal 2007, 9:1745-1756.
Grucker D. Oxymetry by magnetic resonance: applications to animal biology and medicine. Prog Nucl Mag Res Sp 2000, 36:241-270.
Ratner A.V., Muller H.H., Simpson B.B., Johnson D.E., Hurd R., Young S.W. Detection of tumors with F-19 magnetic-resonance-imaging. Invest Radiol 1987, 23:361-364.
Halevy R., Tormyshev V., Blank A. Microimaging of oxygen concentration near live photosynthetic cells by electron spin resonance. Biophys J 2010, 99:971-978.
Acosta M.A., Ymele-Leki P., Kostov Y.V., Leach J.B. Fluorescent microparticles for sensing cell microenvironment oxygen levels within 3D scaffolds. Biomaterials 2009, 30:3068-3074.
Acosta M.A., Velasquez M., Williams K., Ross J.M., Leach J.B. Fluorescent silica particles for monitoring oxygen levels in three-dimensional heterogeneous cellular structures. Biotechnol Bioeng 2012, 109:2663-2670.
Tare R.S., Howard D., Pound J.C., Roach H.I., Oreffo R.O.C. Development of tissue engineering strategies for cartilage generation: micromass and three dimensional cultures using human chondrocytes and an immortalized cell line. J Bone Miner Res 2005, 20:609-621.
De Bank P.A., Kellam B., Kendall D.A., Shakesheff K.M. Surface engineering of living myoblasts via selective periodate oxidation. Biotechnol Bioeng 2003, 81:800-808.
Grayson W.L., Frohlich M., Yeager K., Bhumiratana S., Chan M.E., Cannizzaro C., et al. Engineering anatomically shaped human bone grafts. Proc Natl Acad Sci U S A 2010, 107:3299-3304.
Lakowicz J.R. Principles of fluorescence spectroscopy 2006, Springer, Baltimore. 3rd ed.
Gothard D., Roberts S.J., Shakesheff K.M., Buttery L.D. Engineering embryonic stem-cell aggregation allows an enhanced osteogenic differentiation in vitro. Tissue Eng Part C-Me 2010, 16:583-595.
Huang B., Wu H.K., Kim S., Zare R.N. Coating of poly(dimethylsiloxane) with n-dodecyl-beta-D-maltoside to minimize nonspecific protein adsorption. Lab Chip 2005, 5:1005-1007.
Malda J., van Blitterswijk C.A., van Geffen M., Martens D.E., Tramper J., Riesle J. Low oxygen tension stimulates the redifferentiation of dedifferentiated adult human nasal chondrocytes. Osteoarthr Cartil 2004, 12:306-313.
Weiss H.E., Roberts S.J., Schrooten J., Luyten F.P. A semi-autonomous model of endochondral ossification for developmental tissue engineering. Tissue Eng Part A 2012, 18:1334-1343.
Tekin H., Anaya M., Brigham M.D., Nauman C., Langer R., Khademhosseini A. Stimuli-responsive microwells for formation and retrieval of cell aggregates. Lab Chip 2010, 10:2411-2418.
Witters D., Vergauwe N., Vermeir S., Ceyssens F., Liekens S., Puers R., et al. Biofunctionalization of electrowetting-on-dielectric digital microfluidic chips for miniaturized cell-based applications. Lab Chip 2011, 11:2790-2794.
Wu J., Wheeldon I., Guo Y., Lu T., Du Y., Wang B., et al. A sandwiched microarray platform for benchtop cell-based high throughput screening. Biomaterials 2011, 32:841-848.
Demas J.N., DeGraff B.A., Coleman P.B. Oxygen sensors based on luminescence quenching. Anal Chem 1999, 71:793a-800a.
Wilkinson F., Abdel-Shafi A.A. Mechanism of quenching of triplet states by molecular oxygen: biphenyl derivatives in different solvents. J Phys Chem A 1999, 103:5425-5435.
De Bank P.A., Hou Q.P., Warner R.M., Wood I.V., Ali B.E., MacNeil S., et al. Accelerated formation of multicellular 3-D structures by cell-to-cell cross-linking. Biotechnol Bioeng 2007, 97:1617-1625.
Place E.S., Evans N.D., Stevens M.M. Complexity in biomaterials for tissue engineering. Nat Mater 2009, 8:457-470.
Chapman-Smith A., Cronan J.E. In vivo enzymatic protein biotinylation. Biomol Eng 1999, 16:119-125.
Tannous B.A., Grimm J., Perry K.F., Chen J.W., Weissleder R., Breakefield X.O. Metabolic biotinylation of cell surface receptors for in vivo imaging. Nat Methods 2006, 3:391-396.
Zeng Y., Ramya T.N.C., Dirksen A., Dawson P.E., Paulson J.C. High-efficiency labeling of sialylated glycoproteins on living cells. Nat Methods 2009, 6:207-209.
Howarth M., Chivers C.E., Crozat E., Chu C., Moy V.T., Sherratt D.J. A streptavidin variant with slower biotin dissociation and increased mechanostability. Nat Methods 2010, 7. 391-U76.