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Side populations from cervical-cancer-derived cell lines have stem-cell-like properties

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Abstract

The target cells for the transforming mutations caused by high-risk human papillomavirus (HPV) infection could be the stem cells of the uterine cervical epithelium, generating particular cancer stem cells (CSCs). The aim of this study was to identify and characterize the CSCs from cervical-cancer-derived cell lines. The ability of SiHa, CaLo, and C-33A cell lines to efflux Hoechst 33342 was evaluated by flow cytometry and cells from the corresponding side populations (SPs) and nonside populations (NSPs) were analyzed for their cell-cycle status (pyronin Y) and their mRNA levels of ABC transporter family members (with qPCR). Specific markers (α6-integrinbri/CD71dim, CK17) of normal epithelial stem cells were evaluated by flow cytometry. The biological properties of these cells were analyzed, including their colony heterogeneity, repopulation, and anchorage-independent colony formation. We identified SPs (around 3 %) in the SiHa and CaLo cell lines, more than 70 % of which were in G0 phase and strongly expressed ABC transporters (predominantly ABCG2 and ABCB1). The SP from CaLo cells showed an α6-integrinbri/CDdim pattern, whereas the SP from the SiHa cells showed an α6-integrin−/CDdim pattern. Recultured cells from the SPs of both cell lines generated both SPs and NSPs, and had higher clonogenic potential to form mainly holoclones and greater colony-forming efficiency under anchorage-independent growth conditions than the cells from the NSPs or total cell populations. Interestingly, we identified no SP in the HPV-uninfected C-33A cell line, and it did not express ABCG2 or other members of the ABC transporters (ABCB1, ABCC1, or ABCA3).

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Abbreviations

SP:

Side population

NSP:

Nonside population

CSCs:

Cancer stem cells

RNA:

Ribonucleic acid

HPV:

Human papillomavirus

DMEM:

Dulbecco’s modified Eagle’s medium

F12:

Nutrient mixture F12

FITC:

Fluorescein isothiocyanate

HEK293:

Human embryonic kidney 293 cells

FBS:

Fetal bovine serum

PE:

Phycoerythrin

PY:

Pyronin Y

qPCR:

Quantitative polymerase chain reaction

RT-qPCR:

Reverse transcription-quantitative PCR

ΔΔCt:

Double delta Ct

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Acknowledgments

We gratefully acknowledge Pedro Chavez for his helpful technical assistance and Victor Rosales for his technical support with the cell sorting techniques and data analysis. This work was supported by a grant from CONACyT (Project No. 105174). JVT received a scholarship from CONACyT (173031).

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Authors and Affiliations

  1. Laboratory of Research in Cancer Molecular and Cell Biology, Departamento de Genética y Biología Molecular, CINVESTAV-IPN, Av. Instituto Politécnico Nacional 2508, Col. San Pedro Zacatenco, CP 07360, Mexico, DF, Mexico

    Jairo Villanueva-Toledo, Alberto Ponciano-Gómez & Efraín Garrido

  2. Unidad de Investigación Biomédica en Cáncer, División de Investigación Básica, Instituto Nacional de Cancerología, Secretaría de Salud, CP 14080, Mexico, DF, Mexico

    Elizabeth Ortiz-Sánchez

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  1. Jairo Villanueva-Toledo
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  4. Efraín Garrido
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Correspondence to Efraín Garrido.

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Villanueva-Toledo, J., Ponciano-Gómez, A., Ortiz-Sánchez, E. et al. Side populations from cervical-cancer-derived cell lines have stem-cell-like properties. Mol Biol Rep 41, 1993–2004 (2014). https://doi.org/10.1007/s11033-014-3047-3

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