Water dynamics in MCF-7 breast cancer cells: a neutron scattering descriptive study

Martins, Murillo L.; Dinitzen, Alexander B.; Mamontov, Eugene; Rudić, Svemir; Pereira, José E.  M.; Hartmann-Petersen, Rasmus; Herwig, Kenneth W.; Bordallo, Heloisa N.

doi:10.1038/s41598-019-45056-8

Title: Water dynamics in MCF-7 breast cancer cells: a neutron scattering descriptive study

Journal Article · 17 June 2019 · Scientific Reports

DOI: https://doi.org/10.1038/s41598-019-45056-8 · OSTI ID:1624477

Martins, Murillo L. ^[1]; Dinitzen, Alexander B. ^[2]; Mamontov, Eugene ^[3]; Rudić, Svemir ^[4]; Pereira, José E. M. ^[5];

^[2]; Herwig, Kenneth W. ^[3];

^[6]

Univ. of Copenhagen (Denmark). The Niels Bohr Inst.; Pontifical Catholic Univ. of Goias, Goiania (Brazil). System and Production Engineering Graduate Program; DOE/OSTI
Univ. of Copenhagen (Denmark). Dept. of Biology
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Neutron Sciences Directorate. Neutron Scattering Division
Rutherford Appleton Lab., Chilton (United Kingdom). ISIS Neutron Source Facility
Univ. of Copenhagen (Denmark). The Niels Bohr Inst.
Univ. of Copenhagen (Denmark). The Niels Bohr Inst.; European Spallation Source (ESS), Lund (Sweden)

Water mobility in cancer cells could be a powerful parameter to predict the progression or remission of tumors. In the present descriptive work, new insight into this concept was achieved by combining neutron scattering and thermal analyses. The results provide the frst step to untangle the role played by water dynamics in breast cancer cells (MCF-7) after treatment with a chemotherapy drug. By thermal analyses, the cells were probed as micrometric reservoirs of bulk-like and confned water populations. Under this perspective we showed that the drug clearly alters the properties of the confned water. We have independently validated this idea by accessing the cellular water dynamics using inelastic neutron scattering. Finally, analysis of the quasi-elastic neutron scattering data allows us to hypothesize that, in this particular cell line, difusion increases in the intracellular water in response to the action of the drug on the nanosecond timescale.

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Research Organization:: Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Neutron Sciences Directorate. Neutron Scattering Division

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities Division

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1624477

Journal Information:: Scientific Reports, Journal Name: Scientific Reports Journal Issue: 1 Vol. 9; ISSN 2045-2322

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (43)

Dynamics of Protein and its Hydration Water: Neutron Scattering Studies on Fully Deuterated GFP Nickels, Jonathan D.; O’Neill, Hugh; Hong, Liang Biophysical Journal, Vol. 103, Issue 7 https://doi.org/10.1016/j.bpj.2012.08.046	journal	October 2012
Experimental determination of the nature of diffusive motions of water molecules at low temperatures Teixeira, J.; Bellissent-Funel, M. -C.; Chen, S. H. Physical Review A, Vol. 31, Issue 3 https://doi.org/10.1103/physreva.31.1913	journal	March 1985
Dynamics of Protein and its Hydration Water: Neutron Scattering Studies on Fully Deuterated GFP Nickels, Jonathan D.; O’Neill, Hugh; Hong, Liang Biophysical Journal, Vol. 103, Issue 7 https://doi.org/10.1016/j.bpj.2012.08.046	journal	October 2012
Inelastic Incoherent Neutron Scattering Measurements of Intact Cells and Tissues and Detection of Interfacial Water Ford, Robert C.; Ruffle, Stuart V.; Ramirez-Cuesta, Anibal J. Journal of the American Chemical Society, Vol. 126, Issue 14 https://doi.org/10.1021/ja0393269	journal	April 2004
Relaxational dynamics of water molecules at protein surface Dellerue, S.; Bellissent-Funel, M. -C. Chemical Physics, Vol. 258, Issue 2-3 https://doi.org/10.1016/s0301-0104(00)00181-6	journal	August 2000
The phonon theory of liquid thermodynamics Bolmatov, Dima; Brazhkin, Vadim; Trachenko, Kostya arXiv https://doi.org/10.48550/arxiv.1202.0459	text	January 2012
Inelastic Incoherent Neutron Scattering Measurements of Intact Cells and Tissues and Detection of Interfacial Water Ford, Robert C.; Ruffle, Stuart V.; Ramirez-Cuesta, Anibal J. Journal of the American Chemical Society, Vol. 126, Issue 14 https://doi.org/10.1021/ja0393269	journal	April 2004
Ultrasound-induced mild hyperthermia improves the anticancer efficacy of both Taxol® and paclitaxel-loaded nanocapsules Boissenot, Tanguy; Bordat, Alexandre; Larrat, Benoît Journal of Controlled Release, Vol. 264 https://doi.org/10.1016/j.jconrel.2017.08.041	journal	October 2017
Recent and future developments on TOSCA at ISIS Parker, Stewart F.; Fernandez-Alonso, Felix; Ramirez-Cuesta, Anibal J. Journal of Physics: Conference Series, Vol. 554 https://doi.org/10.1088/1742-6596/554/1/012003	journal	November 2014
Limitations and Prospects for Diffusion-Weighted MRI of the Prostate Bourne, Roger; Panagiotaki, Eleftheria Diagnostics, Vol. 6, Issue 2 https://doi.org/10.3390/diagnostics6020021	journal	May 2016
Inelastic Incoherent Neutron Scattering Studies of Water Interacting with Biological Macromolecules Ruffle, Stuart V.; Michalarias, Ilias; Li, Ji-Chen Journal of the American Chemical Society, Vol. 124, Issue 4 https://doi.org/10.1021/ja016277w	journal	January 2002
A time-of-flight backscattering spectrometer at the Spallation Neutron Source, BASIS Mamontov, E.; Herwig, K. W. Review of Scientific Instruments, Vol. 82, Issue 8 https://doi.org/10.1063/1.3626214	journal	August 2011
Experimental determination of the nature of diffusive motions of water molecules at low temperatures Teixeira, J.; Bellissent-Funel, M. -C.; Chen, S. H. Physical Review A, Vol. 31, Issue 3 https://doi.org/10.1103/PhysRevA.31.1913	journal	March 1985
The phonon theory of liquid thermodynamics Bolmatov, D.; Brazhkin, V. V.; Trachenko, K. Scientific Reports, Vol. 2, Issue 1 https://doi.org/10.1038/srep00421	journal	May 2012
Differential Scanning Calorimetry Study of the Structure of Water Confined within AOT Lamellar Mesophases Prouzet, Eric; Brubach, Jean-Blaise; Roy, Pascale The Journal of Physical Chemistry B, Vol. 114, Issue 24 https://doi.org/10.1021/jp101176v	journal	June 2010
Water Dynamics in Hardened Ordinary Portland Cement Paste or Concrete: From Quasielastic Neutron Scattering Bordallo, Heloisa N.; Aldridge, Laurence P.; Desmedt, Arnaud The Journal of Physical Chemistry B, Vol. 110, Issue 36 https://doi.org/10.1021/jp062922f	journal	September 2006
Dynamics of Water in Na _x CoO ₂ · y H ₂ O Jalarvo, Niina; Bordallo, Heloisa N.; Aliouane, Nadir The Journal of Physical Chemistry B, Vol. 112, Issue 3 https://doi.org/10.1021/jp074398y	journal	January 2008
Dynamics of Water in Na _x CoO ₂ · y H ₂ O Jalarvo, Niina; Bordallo, Heloisa N.; Aliouane, Nadir The Journal of Physical Chemistry B, Vol. 112, Issue 3 https://doi.org/10.1021/jp074398y	journal	January 2008
Calorimetric signatures of human cancer cells and their nuclei Todinova, S.; Stoyanova, E.; Krumova, S. Thermochimica Acta, Vol. 623 https://doi.org/10.1016/j.tca.2015.11.002	journal	January 2016
Limitations and Prospects for Diffusion-Weighted MRI of the Prostate Bourne, Roger; Panagiotaki, Eleftheria Diagnostics, Vol. 6, Issue 2 https://doi.org/10.3390/diagnostics6020021	journal	May 2016
Early Increases in Breast Tumor Xenograft Water Mobility in Response to Paclitaxel Therapy Detected by Non-Invasive Diffusion Magnetic Resonance Imaging Galons, Jean-Philippe; Altbach, Maria I.; Paine-Murrieta, Gillian D. Neoplasia, Vol. 1, Issue 2 https://doi.org/10.1038/sj.neo.7900009	journal	June 1999
Water Dynamics in Hardened Ordinary Portland Cement Paste or Concrete: From Quasielastic Neutron Scattering Bordallo, Heloisa N.; Aldridge, Laurence P.; Desmedt, Arnaud The Journal of Physical Chemistry B, Vol. 110, Issue 36 https://doi.org/10.1021/jp062922f	journal	September 2006
The phonon theory of liquid thermodynamics Bolmatov, D.; Brazhkin, V. V.; Trachenko, K. Scientific Reports, Vol. 2, Issue 1 https://doi.org/10.1038/srep00421	journal	May 2012
Diffusion-Weighted Magnetic Resonance Imaging as a Cancer Biomarker: Consensus and Recommendations Padhani, Anwar R.; Liu, Guoying; Mu-Koh, Dow Neoplasia, Vol. 11, Issue 2 https://doi.org/10.1593/neo.81328	journal	February 2009
DAVE: A Comprehensive Software Suite for the Reduction, Visualization, and Analysis of Low Energy Neutron Spectroscopic Data Azuah, Richard Tumanjong; Kneller, Larry R.; Qiu, Yiming Journal of Research of the National Institute of Standards and Technology, Vol. 114, Issue 6 https://doi.org/10.6028/jres.114.025	journal	November 2009
Ultrasound-induced mild hyperthermia improves the anticancer efficacy of both Taxol® and paclitaxel-loaded nanocapsules Boissenot, Tanguy; Bordat, Alexandre; Larrat, Benoît Journal of Controlled Release, Vol. 264 https://doi.org/10.1016/j.jconrel.2017.08.041	journal	October 2017
DSC analysis of human plasma in breast cancer patients Zapf, István; Fekecs, Tamás; Ferencz, Andrea Thermochimica Acta, Vol. 524, Issue 1-2 https://doi.org/10.1016/j.tca.2011.06.019	journal	September 2011
Relaxational dynamics of water molecules at protein surface Dellerue, S.; Bellissent-Funel, M. -C. Chemical Physics, Vol. 258, Issue 2-3 https://doi.org/10.1016/S0301-0104(00)00181-6	journal	August 2000
Paclitaxel resistance is associated with switch from apoptotic to autophagic cell death in MCF-7 breast cancer cells Ajabnoor, G. M. A.; Crook, T.; Coley, H. M. Cell Death & Disease, Vol. 3, Issue 1 https://doi.org/10.1038/cddis.2011.139	journal	January 2012
Picosecond orientational dynamics of water in living cells Tros, Martijn; Zheng, Linli; Hunger, Johannes Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-00858-0	journal	October 2017
Differential Scanning Calorimetry of Gliomas Chagovetz, Alexis A.; Quinn, Colette; Damarse, Neil Neurosurgery, Vol. 73, Issue 2 https://doi.org/10.1227/01.neu.0000430296.23799.cd	journal	April 2013
Demonstration of Non-Gaussian Restricted Diffusion in Tumor Cells Using Diffusion Time-Dependent Diffusion-Weighted Magnetic Resonance Imaging Contrast Hope, Tuva R.; White, Nathan S.; Kuperman, Joshua Frontiers in Oncology, Vol. 6 https://doi.org/10.3389/fonc.2016.00179	journal	August 2016
Microenvironmental regulation of tumor progression and metastasis Quail, Daniela F.; Joyce, Johanna A. Nature Medicine, Vol. 19, Issue 11 https://doi.org/10.1038/nm.3394	journal	November 2013
Microscopic diffusion processes measured in living planarians Mamontov, Eugene Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-22643-9	journal	March 2018
Differential Scanning Calorimetry of Gliomas Chagovetz, Alexis A.; Quinn, Colette; Damarse, Neil Neurosurgery, Vol. 73, Issue 2 https://doi.org/10.1227/01.neu.0000430296.23799.cd	journal	April 2013
Inelastic Incoherent Neutron Scattering Studies of Water Interacting with Biological Macromolecules Ruffle, Stuart V.; Michalarias, Ilias; Li, Ji-Chen Journal of the American Chemical Society, Vol. 124, Issue 4 https://doi.org/10.1021/ja016277w	journal	January 2002
DAVE: A Comprehensive Software Suite for the Reduction, Visualization, and Analysis of Low Energy Neutron Spectroscopic Data Azuah, Richard Tumanjong; Kneller, Larry R.; Qiu, Yiming Journal of Research of the National Institute of Standards and Technology, Vol. 114, Issue 6 https://doi.org/10.6028/jres.114.025	journal	November 2009
DSC analysis of human plasma in breast cancer patients Zapf, István; Fekecs, Tamás; Ferencz, Andrea Thermochimica Acta, Vol. 524, Issue 1-2 https://doi.org/10.1016/j.tca.2011.06.019	journal	September 2011
Nanoscale Mobility of Aqueous Polyacrylic Acid in Dental Restorative Cements Berg, Marcella C.; Benetti, Ana R.; Telling, Mark T. F. ACS Applied Materials & Interfaces, Vol. 10, Issue 12 https://doi.org/10.1021/acsami.7b15735	journal	March 2018
Recent and future developments on TOSCA at ISIS Parker, Stewart F.; Fernandez-Alonso, Felix; Ramirez-Cuesta, Anibal J. Journal of Physics: Conference Series, Vol. 554 https://doi.org/10.1088/1742-6596/554/1/012003	journal	November 2014
Differential Scanning Calorimetry Study of the Structure of Water Confined within AOT Lamellar Mesophases Prouzet, Eric; Brubach, Jean-Blaise; Roy, Pascale The Journal of Physical Chemistry B, Vol. 114, Issue 24 https://doi.org/10.1021/jp101176v	journal	June 2010
Diffusion-Weighted Magnetic Resonance Imaging as a Cancer Biomarker: Consensus and Recommendations Padhani, Anwar R.; Liu, Guoying; Mu-Koh, Dow Neoplasia, Vol. 11, Issue 2 https://doi.org/10.1593/neo.81328	journal	February 2009
Paclitaxel resistance is associated with switch from apoptotic to autophagic cell death in MCF-7 breast cancer cells Ajabnoor, G. M. A.; Crook, T.; Coley, H. M. Cell Death & Disease, Vol. 3, Issue 1 https://doi.org/10.1038/cddis.2011.139	journal	January 2012