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Cytosolic delivery of nanolabels prevents their asymmetric inheritance and enables extended quantitative in vivo cell imaging

Ranhua Xiong UGent, Freya Joris, Sayuan Liang, Riet De Rycke UGent, Saskia Lippens UGent, Jo Demeester UGent, Andre Skirtach UGent, Koen Raemdonck UGent, Uwe Himmelreich, Stefaan De Smedt UGent, et al. (2016) NANO LETTERS. 16(10). p.5975-5986
abstract
Long-term in vivo imaging of cells is crucial for the understanding of cellular fate in biological processes in cancer research, immunology, or in cell-based therapies such as beta cell transplantation, in type I diabetes or stem cell therapy. Traditionally, cell labeling with the desired contrast agent occurs ex vivo via spontaneous endocytosis, which is a variable and slow process that requires optimization for each particular label-cell type combination. Following endocytic uptake, the contrast agents mostly remain entrapped in the endolysosomal compartment, which leads to signal instability, cytotoxicity, and asymmetric inheritance of the labels upon cell division. Here, we demonstrate that these disadvantages can be circumvented by delivering contrast agents directly into the cytoplasm via vapor nanobubble photoporation. Compared to classic endocytic uptake, photoporation resulted in :50 and 3 times higher loading of fluorescent dextrans and quantum dots, respectively, with improved signal stability and reduced cytotoxicity: Most: interestingly, cytosolic delivery by iihotoporation prevented asymmetric inheritance of labels by daughter cells over subsequent cell' generations. Instead, unequal inheritance of endocytosed labels resulted in a dramatic increase in polydispersity of the amount of labels per cell with each cell division, hindering accurate quantification of cell numbers in vivo over time. The combined benefits of cell labeling by photoporation resulted in a marked improvement in long-term cell visibility in vivo where an insulin producing cell line (INS-1E cell line) labeled with fluorescent dextrans could be tracked for up to two months in Swiss nude mice compared to 2-Weeks for cells labeled by endocytosis.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
Cell labeling cytosolic delivery, nanopaiticle inheritance, vapor nanobubble photoporation, in vivo cell tracking, quantum dots, NEURAL STEM-CELLS, QUANTUM DOTS, REPORTER GENE, LIVE CELLS, INTRACELLULAR DELIVERY, PLASMONIC NANOBUBBLES, ENDOSOMAL ESCAPE, CONTRAST AGENTS, TRACKING, DIVISION
journal title
NANO LETTERS
Nano Lett.
volume
16
issue
10
pages
5975 - 5986
Web of Science type
Article
Web of Science id
000385469800002
JCR category
MATERIALS SCIENCE, MULTIDISCIPLINARY
JCR impact factor
12.712 (2016)
JCR rank
11/275 (2016)
JCR quartile
1 (2016)
ISSN
1530-6984
1530-6992
DOI
10.1021/acs.nanolett.6b01411
project
Center for nano- and biophotonics (NB-Photonics)
language
English
UGent publication?
yes
classification
A1
copyright statement
I have transferred the copyright for this publication to the publisher
id
8522072
handle
http://hdl.handle.net/1854/LU-8522072
date created
2017-06-01 17:04:12
date last changed
2017-12-13 08:33:28
@article{8522072,
  abstract     = {Long-term in vivo imaging of cells is crucial for the understanding of cellular fate in biological processes in cancer research, immunology, or in cell-based therapies such as beta cell transplantation, in type I diabetes or stem cell therapy. Traditionally, cell labeling with the desired contrast agent occurs ex vivo via spontaneous endocytosis, which is a variable and slow process that requires optimization for each particular label-cell type combination. Following endocytic uptake, the contrast agents mostly remain entrapped in the endolysosomal compartment, which leads to signal instability, cytotoxicity, and asymmetric inheritance of the labels upon cell division. Here, we demonstrate that these disadvantages can be circumvented by delivering contrast agents directly into the cytoplasm via vapor nanobubble photoporation. Compared to classic endocytic uptake, photoporation resulted in :50 and 3 times higher loading of fluorescent dextrans and quantum dots, respectively, with improved signal stability and reduced cytotoxicity: Most: interestingly, cytosolic delivery by iihotoporation prevented asymmetric inheritance of labels by daughter cells over subsequent cell' generations. Instead, unequal inheritance of endocytosed labels resulted in a dramatic increase in polydispersity of the amount of labels per cell with each cell division, hindering accurate quantification of cell numbers in vivo over time. The combined benefits of cell labeling by photoporation resulted in a marked improvement in long-term cell visibility in vivo where an insulin producing cell line (INS-1E cell line) labeled with fluorescent dextrans could be tracked for up to two months in Swiss nude mice compared to 2-Weeks for cells labeled by endocytosis.},
  author       = {Xiong, Ranhua and Joris, Freya and Liang, Sayuan and De Rycke, Riet and Lippens, Saskia and Demeester, Jo and Skirtach, Andre and Raemdonck, Koen and Himmelreich, Uwe and De Smedt, Stefaan and Braeckmans, Kevin},
  issn         = {1530-6984},
  journal      = {NANO LETTERS},
  keyword      = {Cell labeling cytosolic delivery,nanopaiticle inheritance,vapor nanobubble photoporation,in vivo cell tracking,quantum dots,NEURAL STEM-CELLS,QUANTUM DOTS,REPORTER GENE,LIVE CELLS,INTRACELLULAR DELIVERY,PLASMONIC NANOBUBBLES,ENDOSOMAL ESCAPE,CONTRAST AGENTS,TRACKING,DIVISION},
  language     = {eng},
  number       = {10},
  pages        = {5975--5986},
  title        = {Cytosolic delivery of nanolabels prevents their asymmetric inheritance and enables extended quantitative in vivo cell imaging},
  url          = {http://dx.doi.org/10.1021/acs.nanolett.6b01411},
  volume       = {16},
  year         = {2016},
}

Chicago
Xiong, Ranhua, Freya Joris, Sayuan Liang, Riet De Rycke, Saskia Lippens, Jo Demeester, Andre Skirtach, et al. 2016. “Cytosolic Delivery of Nanolabels Prevents Their Asymmetric Inheritance and Enables Extended Quantitative in Vivo Cell Imaging.” Nano Letters 16 (10): 5975–5986.
APA
Xiong, R., Joris, F., Liang, S., De Rycke, R., Lippens, S., Demeester, J., Skirtach, A., et al. (2016). Cytosolic delivery of nanolabels prevents their asymmetric inheritance and enables extended quantitative in vivo cell imaging. NANO LETTERS, 16(10), 5975–5986.
Vancouver
1.
Xiong R, Joris F, Liang S, De Rycke R, Lippens S, Demeester J, et al. Cytosolic delivery of nanolabels prevents their asymmetric inheritance and enables extended quantitative in vivo cell imaging. NANO LETTERS. 2016;16(10):5975–86.
MLA
Xiong, Ranhua, Freya Joris, Sayuan Liang, et al. “Cytosolic Delivery of Nanolabels Prevents Their Asymmetric Inheritance and Enables Extended Quantitative in Vivo Cell Imaging.” NANO LETTERS 16.10 (2016): 5975–5986. Print.