A novel device for elimination of cancer cells from blood specimens.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
23 06 2020
Historique:
received: 08 03 2019
accepted: 29 05 2020
entrez: 25 6 2020
pubmed: 25 6 2020
medline: 1 12 2020
Statut: epublish

Résumé

Circulating tumor cells (CTCs) are derivatives of solid cancerous lesions that detach from the tumor mass and enter the blood circulation. CTCs are considered to be the precursors of metastasis in several cancer types. They are present in the blood of cancer patients as single cells or clusters, with the latter being associated with a higher metastatic potential. Methods to eliminate CTCs from the bloodstream are currently lacking. Here, we took advantage of the lower shear stress-resistance of cancer cells compared to blood cells, and developed a device that can eliminate cancer cells without blood damage. The device consists of an axial pump and a coupled rotating throttle, controllable to prevent local blood flow impairment, yet maintaining a constant shear performance. When processing cancer cells through our device, we observe cancer cell-cluster disruption and viability reduction of single cancer cells, without noticeable effects on human blood cells. When injecting cancer cell-containing samples into tumor-free recipient mice, processed samples fail to generate metastasis. Together, our data show that a selective disruption of cancer cells is possible while preserving blood cells, paving the way towards the development of novel, implantable tools for CTC disruption and metastasis prevention.

Identifiants

pubmed: 32576883
doi: 10.1038/s41598-020-67071-w
pii: 10.1038/s41598-020-67071-w
pmc: PMC7311454
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

10181

Références

Stewart, B. W. & Wild, C. P. World Cancer Report 2014. 630p (World Health Organization, 2014).
Talmadge, J. E. & Fidler, I. J. AACR centennial series: the biology of cancer metastasis: historical perspective. Cancer research. 0008–5472, https://doi.org/10.1158/0008-5472.CAN-10-1040 (2010).
Gkountela, S. & Aceto, N. Stem-like features of cancer cells on their way to metastasis. Biology direct. 11(1), 33 (2016).
doi: 10.1186/s13062-016-0135-4
Gkountela, S., Szczerba, B., Donato, C. & Aceto, N. Recent advances in the biology of human circulating tumor cells and metastasis. ESMO open. 1(4), e000078 (2016).
doi: 10.1136/esmoopen-2016-000078
Seyfried, T. N. & Huysentruyt, L. C. On the origin of cancer metastasis. Critical reviews in oncogenesis. 18(1-2), 43 (2013).
doi: 10.1615/CritRevOncog.v18.i1-2.40
Mohme, M., Riethdorf, S. & Pantel, K. Circulating and disseminated tumor cells – mechanisms of immune surveillance and escape. Nat. Rev. Clin. Oncol. 14, 155–167 (2017).
doi: 10.1038/nrclinonc.2016.144
Aceto, N., Toner, M. Maheswaran, S. & Haber, D. A. En route to metastasis: circulating tumor cell clusters and epithelial-to-mesenchymal transition. Trends in cancer. 1(1), 44–52 (2015).
doi: 10.1016/j.trecan.2015.07.006
Gkountela, S. et al. Circulating tumor cell clustering shapes DNA methylation to enable metastasis seeding. Cell. 176(1-2), 98–112 (2019).
doi: 10.1016/j.cell.2018.11.046
Szczerba, B. M. et al. Neutrophils escort circulating tumor cells to enable cell cycle progression. Nature. https://doi.org/10.1038/s41586-019-0915-y (2019).
doi: 10.1038/s41586-019-0915-y pubmed: 31485072
Alix-Panabieres, C. & Pantel, K. Challenges in circulating tumor cells research. Nat. Rev. Cancer. 14, 623–631 (2014).
doi: 10.1038/nrc3820
Paoletti, C. & Hayes, D. F. Circulating tumor cells. In Novel Biomarkers in the Continuum of Breast Cancer (pp. 235-258). Springer, Cham (2016).
Yoon, H. J., Kozminsky, M. & Nagrath, S. Emerging role of nanomaterials in circulating tumor cell isolation and analysis. ACS nano 8(3), 1995–2017 (2014).
doi: 10.1021/nn5004277
Nagrath, S. et al. Isolation of rare circulating tumor cells in cancer patients by microchip technology. Nature 450(7173), 1235 (2007).
doi: 10.1038/nature06385
Kim, T. H. et al. A temporary indwelling intravascular aphaeretic system for in vivo enrichment of circulating tumor cells. Nature communications 10(1), 1478 (2019).
doi: 10.1038/s41467-019-09439-9
Gorges, T. M. et al. Enumeration and molecular characterization of tumor cells in lung cancer patients using a novel in vivo device for capturing circulating tumor cells. Clinical Cancer Research 22(9), 2197–2206 (2016).
doi: 10.1158/1078-0432.CCR-15-1416
Vermesh, O. et al. An intravascular magnetic wire for the high-throughput retrieval of circulating tumor cells in vivo. Nature biomedical engineering 2(9), 696 (2018).
doi: 10.1038/s41551-018-0257-3
Dong, J. F. et al. ADAMTS-13 rapidly cleaves newly secreted ultralarge von Willebrand factor multimers on the endothelial surface under flowing conditions. Blood. 100(12), 4033–4039 (2002).
doi: 10.1182/blood-2002-05-1401
Zhang, X., Halvorsen, K., Zhang, C.-Z., Wong, W. P. & Springer, T. A. Mechanoenzymatic cleavage of the ultralarge vascular protein von Willebrand factor. Science. 324(5932), 1330–1334 (2009).
doi: 10.1126/science.1170905
Bagnall, J. S. et al. Deformability of tumor cells versus blood cells. Scientific reports. 5, 18542 (2015).
doi: 10.1038/srep18542
Regmi, S., Fu, A. & Luo, K. Q. High shear stresses under exercise condition destroy circulating tumor cells in a microfluidic system. Scientific reports. 7, 39975 (2017).
doi: 10.1038/srep39975
Brown, D. et al. Phylogenetic analysis of metastatic progression in breast cancer using somatic mutations and copy number aberrations. Nature communications 8, 14944 (2017).
doi: 10.1038/ncomms14944
Reiter, J. G. et al. Reconstructing metastatic seeding patterns of human cancers. Nature communications 8, 14114 (2017).
doi: 10.1038/ncomms14114
McPherson, A. et al. Divergent modes of clonal spread and intraperitoneal mixing in high-grade serous ovarian cancer. Nature genetics 48(7), 758 (2016).
doi: 10.1038/ng.3573
Mathenge, E. G. et al. Core needle biopsy of breast cancer tumors increases distant metastases in a mouse model. Neoplasia 16(11), 950–960 (2014).
doi: 10.1016/j.neo.2014.09.004
Kusukawa, J. et al. Dissemination of cancer cells into circulation occurs by incisional biopsy of oral squamous cell carcinoma. Journal of oral pathology & medicine 29(7), 303–307 (2000).
doi: 10.1034/j.1600-0714.2000.290703.x
Hu, X. C. & Chow, L. W. Fine needle aspiration may shed breast cells into peripheral blood as determined by RT-PCR. Oncology 59(3), 217–222 (2000).
doi: 10.1159/000012164
Louha, M. et al. Liver resection and needle liver biopsy cause hematogenous dissemination of liver cells. Hepatology 29(3), 879–882 (1999).
doi: 10.1002/hep.510290348
Yamaguchi, K., Takagi, Y., Aoki, S., Futamura, M. & Saji, S. Significant detection of circulating cancer cells in the blood by reverse transcriptase–polymerase chain reaction during colorectal cancer resection. Annals of surgery 232(1), 58 (2000).
doi: 10.1097/00000658-200007000-00009
Juratli, M. A. et al. Real‐time monitoring of circulating tumor cell release during tumor manipulation using in vivo photoacoustic and fluorescent flow cytometry. Head & neck 36(8), 1207–1215 (2014).
doi: 10.1002/hed.23439
Moreno, J. G. et al. Transrectal ultrasound-guided biopsy causes hematogenous dissemination of prostate cells as determined by RT-PCR. Urology 49(4), 515–520 (1997).
doi: 10.1016/S0090-4295(97)00016-2
Hara, N. et al. Frequency of PSA-mRNA-bearing cells in the peripheral blood of patients after prostate biopsy. British journal of cancer 85(4), 557 (2001).
doi: 10.1054/bjoc.2001.1924
Coumans, F. A., Ligthart, S. T., Uhr, J. W. & Terstappen, L. W. Challenges in the enumeration and phenotyping of CTC. Clinical Cancer Research 18(20), 5711–5718 (2012).
doi: 10.1158/1078-0432.CCR-12-1585
Legendre, D. et al. Computational fluid dynamics investigation of a centrifugal blood pump. Artificial organs 32(4), 342–348 (2008).
doi: 10.1111/j.1525-1594.2008.00552.x
Moosavi, M. H. & Fatouraee, N. Flow simulation of a diaphragm-type ventricular assist device with structural interactions. In 2007 29th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (pp. 1027–1030). IEEE (2007, August).
Untaroiu, A., Wood, H. G. & Allaire, P. E. Numerical evaluation of blood damage in a magnetically levitated heart pump. Biomedical sciences instrumentation 45, 220–225 (2009).
pubmed: 19369766
Mizunuma, H. & Nakajima, R. Experimental study on shear stress distributions in a centrifugal blood pump. Artificial organs 31(7), 550–559 (2007).
doi: 10.1111/j.1525-1594.2007.00421.x
Watanabe, N., Sakota, D., Ohuchi, K. & Takatani, S. Deformability of red blood cells and its relation to blood trauma in rotary blood pumps. Artificial organs 31(5), 352–358 (2007).
doi: 10.1111/j.1525-1594.2007.00392.x
Hashimoto, S., Otani, H. & Imamura, H. Effect of aging on deformability of erythrocytes in shear flow. Journal of Systemics Cybernetics and Informatics 3(1), 90–93 (2005).
Sakota, D. et al. Mechanical damage of red blood cells by rotary blood pumps: selective destruction of aged red blood cells and subhemolytic trauma. Artificial organs 32(10), 785–791 (2008).
doi: 10.1111/j.1525-1594.2008.00631.x
Sakota, D., Sakamoto, R., Yokoyama, N., Kobayashi, M. & Takatani, S. Glucose Depletion Enhances Sensitivity to Shear Stress‐induced Mechanical Damage in Red Blood Cells by Rotary Blood Pumps. Artificial organs 33(9), 733–739 (2009).
doi: 10.1111/j.1525-1594.2009.00898.x
Sallam, A. M. & Hwang, N. H. Human red blood cell hemolysis in a turbulent shear flow: contribution of Reynolds shear stresses. Biorheology 21(6), 783–797 (1984).
doi: 10.3233/BIR-1984-21605
Girdhar, G. & Bluestein, D. Biological effects of dynamic shear stress in cardiovascular pathologies and devices. Expert review of medical devices 5(2), 167–181 (2008).
doi: 10.1586/17434440.5.2.167
Heilmann, C. Scherstress-bedingte Komplikationen der mechanischen Herzunterstützung. Habilitation thesis Albert-Ludwigs-University Freiburg (2012).
Faghih, M. M. & Sharp, M. K. Modeling and prediction of flow-induced hemolysis: a review. Biomechanics and Modeling in Mechanobiology 18, 845–881 (2019).
doi: 10.1007/s10237-019-01137-1
Chen, Z. et al. Paradoxical Effect of Nonphysiological Shear Stress on Platelets and von Willebrand Factor. Artificial organs 40(7), 659–668, https://doi.org/10.1111/aor.12606 (2016).
doi: 10.1111/aor.12606 pubmed: 26582038
Hosseini, H. et al. Early dissemination seeds metastasis in breast cancer. Nature. 540(7634), 552–558, https://doi.org/10.1038/nature20785 (2016 Dec 22).

Auteurs

Agnes Weth (A)

Institute of Biomedical Mechatronics, Johannes Kepler University of Linz, Altenbergerstr. 69, 4040, Linz, Austria.

Ilona Krol (I)

Cancer Metastasis Laboratory, Department of Biomedicine, University of Basel and University Hospital Basel, 4058, Basel, Switzerland.

Kurt Priesner (K)

Griesmühle Ltd, Griesmühlweg 14, 4111, Walding, Austria.

Cinzia Donato (C)

Cancer Metastasis Laboratory, Department of Biomedicine, University of Basel and University Hospital Basel, 4058, Basel, Switzerland.

Stefan Pirker (S)

Department of Particulate Flow Modelling, Johannes Kepler University of Linz, Altenbergerstr. 69, 4040, Linz, Austria.

Christoph Wolf (C)

Institute of Biomedical Mechatronics, Johannes Kepler University of Linz, Altenbergerstr. 69, 4040, Linz, Austria.

Nicola Aceto (N)

Cancer Metastasis Laboratory, Department of Biomedicine, University of Basel and University Hospital Basel, 4058, Basel, Switzerland. nicola.aceto@unibas.ch.

Werner Baumgartner (W)

Institute of Biomedical Mechatronics, Johannes Kepler University of Linz, Altenbergerstr. 69, 4040, Linz, Austria. werner.baumgartner@jku.at.

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