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Genetic Profiling Reveals Cross-Contamination and Misidentification of 6 Adenoid Cystic Carcinoma Cell Lines: ACC2, ACC3, ACCM, ACCNS, ACCS and CAC2

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Phuchareon, Janyaporn, Ohta, Yoshihito, Woo, Jonathan M., Eisele, David W., Tetsu, Osamu·2009·PLoS ONE

DOI 10.1371/journal.pone.0006040PMC PMC2698276

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Abstract

Adenoid cystic carcinoma (ACC) is the second most common malignant neoplasm of the salivary glands. Most patients survive more than 5 years after surgery and postoperative radiation therapy. The 10 year survival rate, however, drops to 40%, due to locoregional recurrences and distant metastases. Improving long-term survival in ACC requires the development of more effective systemic therapies based on a better understanding of the biologic behavior of ACC. Much preclinical research in this field involves the use of cultured cells and, to date, several ACC cell lines have been established. Authentication of these cell lines, however, has not been reported. We performed DNA fingerprint analysis on six ACC cell lines using short tandem repeat (STR) examinations and found that all six cell lines had been contaminated with other cells. ACC2, ACC3, and ACCM were determined to be cervical cancer cells (HeLa cells), whereas the ACCS cell line was composed of T24 urinary bladder cancer cells. ACCNS and CAC2 cells were contaminated with cells derived from non-human mammalian species: the cells labeled ACCNS were mouse cells and the CAC2 cells were rat cells. These observations suggest that future studies using ACC cell lines should include cell line authentication to avoid the use of contaminated or non-human cells.

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Figure 1 HeLa contaiminated-ACC2, ACC3, and ACCM demonstrate a variation in the von Willebrand factor gene (vWA). Electrophoretic profiles of the vWA marker for HeLa, ACC2/Sa, ACC2/Zh, ACC3, and ACCM are shown. Complete STR profiling is shown in Table 1 and Figures S2, S3, S4, S5, S6, S7, S8, S9, S10. A multiplex PCR reaction was performed using two-color detection fluorescent dye-linked primers. One ng of each genomic DNA was independently amplified in a 25 µl reaction volume. The amplified PCR products were separated by capillary electrophoresis on a 3730xI DNA Analyzer (Applied Biosystems) and analyzed using GeneMapper v4.0 software (Applied Biosystems). Cell lines for the study were generously provided by Drs. Takashi Saku (ACC2/Sa and ACC3), Naishuo Zhu (ACC2/Zh), Kanemitsu Shirasuna (ACCS), Noriaki Tanaka (ACCM and ACCNS), and Ruy Jaeger (CAC2). HeLa cells were purchased from the ATCC.CC BY · PubMed Central

Figure 2 ACCNS cells were mouse cells and CAC2 cells were rat cells. A cytochrome C oxidase subunit I (COI) DNA barcoding assay was performed using multiplex species-specific primer sets for 12 species (+, lanes 3, 5, 6 and 7) or 11 species-specific sets without mouse primers (−, lanes 2 and 4). The PCR products were separated in a 2% agarose gel and visualized with ethidium bromide following amplification of 5′ end of COI region. Lanes 1 and 8: 100 bp ladders. Lanes 2 and 3: ACCNS. Lanes 4 and 5: CAC2. Lane 6: Mixed DNA template from 12 species. Lane 7: no template DNA. The animals and expected PCR product sizes were as follows; human (391 bp), cat (341 bp), Chinese hamster (315 bp), rhesus monkey (287 bp), horse (243 bp), African green monkey (222 bp), rat (196 bp), dog (172 bp), mouse (150 bp), rabbit (136 bp), goat (117 bp), and cow (102 bp). The PCR products were sequenced to confirm that they contained the species-specific nucleotide sequence.CC BY · PubMed Central

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Background
Harvesting Human Prostate Tissue Material and Culturing Primary Prostate Epithelial Cells
Frame, F. M., Pellacani, D., Collins, A. T., & Maitland, N. J. (2016) · Methods in molecular biology · doi:10.1007/978-1-4939-3724-0_12 · Cited by 18
Genetic rearrangements, hotspot mutations, and microRNA expression in the progression of metastatic adenoid cystic carcinoma of the salivary gland
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“As previous in vitro studies on the involvement of miRNA in the metastatic progression of ACC has been hampered by cross-contamination, data from human samples has not been available until now [15].”
Background
Establishment, authenticity, and characterization of cervical cancer cell lines
Martinez, M. D. L. Z., Mendoza, C. M. L., Salazar, J. T., García-Carrancá, A. M., Cervantes, M. A. C., & Alcántara-Quintana, L. E. (2022) · Molecular & Cellular Oncology · doi:10.1080/23723556.2022.2078628 · Cited by 17
Cross-Contamination of a UROtsa Stock with T24 Cells – Molecular Comparison of Different Cell Lines and Stocks
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Tackling the Human Cell Line and Tissue Misidentification Problem Is Needed for Reproducible Biomedical Research
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Authentication of the R06E Fruit Bat Cell Line
Jordan, I., Munster, V. J., & Sandig, V. (2012) · Viruses · doi:10.3390/v4050889 · Cited by 16
Clinical and molecular insights into adenoid cystic carcinoma: Neural crest‐like stemness as a target
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Current landscape and future directions of therapeutic approaches for adenoid cystic carcinoma of the salivary glands (Review)
Stawarz, K., Durzyńska, M., Galazka, A., Gorzelnik, A., Zwoliński, J., Paszkowska, M., Bieńkowska‐Pluta, K., & Misiak-Gałązka, M. (2025) · Oncology Letters · doi:10.3892/ol.2025.14899 · Cited by 15
“The ACC2, ACC3 and ACCM cell lines were primarily contaminated with cervical cancer cells, while the ACCS cell line was composed of T24 urinary bladder cancer cells (11).”
Establishment and characterization of an oral tongue squamous cell carcinoma cell line from a never-smoking patient
Wang, S. J., Asthana, S., van Zante, A., Heaton, C. M., Phuchareon, J., Stein, L. C., Higuchi, S., Kishimoto, T., Chiu, C. Y., Olshen, A. B., et al. (2017) · Oral Oncology · doi:10.1016/j.oraloncology.2017.03.020 · Cited by 14
“Cell culture The following cell lines were from the American Type Culture Collection: SCC-4, SCC-25, CAL27, HeLa, SW480, 293T, and WI-38.”
BackgroundInfluentialSelf-citation
Molecular features of adenoid cystic carcinoma with an emphasis on micro RNA expression
Andreasen, S. (2018) · Apmis · doi:10.1111/apm.12828 · Cited by 14
“in vitro studies, but the cell lines used have since been shown to be severely contaminated with various non-ACC cells (153).”
Background
SIVmac₂₃₉-Nef down-regulates cell surface expression of CXCR4 in tumor cells and inhibits proliferation, migration and angiogenesis.
Cai, C., Rodepeter, F. R., Rossmann, A., Teymoortash, A., Lee, J.-S., Quint, K., Fazio, P. D., Ocker, M., Werner, J. A., & Mandić, R. (2012) · PubMed · Cited by 14
Thyroid cancer cell lines: Critical models to study thyroid cancer biology and new therapeutic targets
Schweppe, R. E. (2012) · Frontiers in Endocrinology · doi:10.3389/fendo.2012.00081 · Cited by 13
Comprehensive molecular characterization of adenoid cystic carcinoma reveals tumor suppressors as novel drivers and prognostic biomarkers
Persson, M., Andersson, M. K., Sahlin, P., Mitani, Y., Brandwein‐Weber, M., Frierson, H. F., Moskaluk, C. A., Fonseca, I., Ferrarotto, R., Boecker, W., et al. (2023) · The Journal of Pathology · doi:10.1002/path.6172 · Cited by 13
Classification of cancer cell death with spectral dimensionality reduction and generalized eigenvalues
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“To his day, the most accurate way of discriminating among various ells is through genetic profiling (gene expression) [7] or identificaion with biomarkers, which can take long time, requires expensive quipment and trained personnel [8].”
Background
IGRhCellID: integrated genomic resources of human cell lines for identification
Shiau, C.-K., Gu, D.-L., Chen, C., Lin, C.-H., & Jou, Y. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq1075 · Cited by 12
Contamination of Primary Human Corneal Epithelial Cells With an SV40-Transformed Human Corneal Epithelial Cell Line: A Lesson for Cell Biologists in Good Laboratory Practice
Girolamo, N. D., Chow, S., Richardson, A., & Wakefield, D. (2016) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.15-18783 · Cited by 12
Robustin-silicoidentification of cancer cell lines based on next generation sequencing
Otto, R., Sers, C., & Leser, U. (2017) · Oncotarget · doi:10.18632/oncotarget.16110 · Cited by 12
“Oncotarget34315www.impactjournals.com/oncotarget Three factors have been found to be associated with false negative (FN) predictions: About 100 of the 546 FN-predictions for weight 1.0 occurred between queryreference pairs that were defined as identical by the goldstandard due to either cross-contamination (e.g. ACCS…”
BackgroundInfluential
Keeping It Clean: The Cell Culture Quality Control Experience at the National Center for Advancing Translational Sciences
Roth, J. S., Lee, T. D., Cheff, D. M., Gosztyla, M. L., Asawa, R. R., Danchik, C., Michael, S., Simeonov, A. M., Klumpp-Thomas, C. A., Wilson, K. M., et al. (2020) · SLAS DISCOVERY · doi:10.1177/2472555220911451 · Cited by 15
Establishment and genomic characterization of primary salivary duct carcinoma cell line
Li, J., Mitani, Y., Rao, P. H., Perlaky, L., Liu, B., Weber, R. S., & El‐Naggar, A. K. (2017) · Oral Oncology · doi:10.1016/j.oraloncology.2017.04.007 · Cited by 11
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Jia, Y., Liu, Y., Yang, H., & Yao, F. (2024) · MedComm · doi:10.1002/mco2.734 · Cited by 10
The Epigenesis of Salivary Glands Carcinoma: From Field Cancerization to Carcinogenesis
Lazim, N. M., Yousaf, A., Abusalah, M. A. H., Sulong, S., Ismail, Z. I. M., Mohamud, R., Abu-Harirah, H. A., AlRamadneh, T. N., Hassan, R., & Abdullah, B. (2023) · Cancers · doi:10.3390/cancers15072111 · Cited by 9
Identification of methylated genes in salivary gland adenoid cystic carcinoma xenografts using global demethylation and methylation microarray screening
Ling, S., Rettig, E. M., Tan, M., Chang, X., Wang, Z., Brait, M., Bishop, J. A., Fertig, E. J., Considine, M., Wick, M. J., et al. (2016) · International Journal of Oncology · doi:10.3892/ijo.2016.3532 · Cited by 9
“Our approach was to circumvent the lack of viable ACC cell lines (20) by using primary xenograft tumor models, in an attempt to identify relevant genes exhibiting differential promoter methylation.”
Method
The cross-contaminated cell lines of adenoid cystic carcinoma: A crucial concern
Chen, W., Liu, N., & Zhang, S.-L. (2017) · Translational Surgery · doi:10.4103/2468-5585.200513 · Cited by 8
Immunohistochemical expression of caspases 9 and 3 in adenoid cystic carcinoma of salivary glands and association with clinicopathological parameters.
Dožić, B., Glumac, S., Boričić, N., Dožić, M., Aničić, B., & Boričić, I. (2016) · PubMed · Cited by 8
Elevated TARP promotes proliferation and metastasis of salivary adenoid cystic carcinoma
Yue, H., Cai, Y., Song, Y., Meng, L., Chen, X., Wang, M., Bian, Z., & Wang, R. (2016) · Oral Surgery Oral Medicine Oral Pathology and Oral Radiology · doi:10.1016/j.oooo.2016.11.023 · Cited by 7
Establishment and characterization of an orthotopic sinonasal squamous cell carcinoma mouse model
Costales, M., López, F., García–Inclán, C., Fernández, S., Marcos, C. Á., Llorente, J. L., & Hermsen, M. A. J. A. (2014) · Head & Neck · doi:10.1002/hed.23832 · Cited by 6
“Gelbard et al(21) used 2 aggressive tumor cell lines: DM14 is a highly metastatic clone of cell line TU167 of an SCC of the floor of the mouth, and ACC3 was, in fact, not an adenoid cystic carcinoma cell line, but HeLa.(23,24) Our cell line, SCCNC4, was derived from a T2N1M0 primary maxillary sinus SCC.”
Method
Low expression of endothelin receptor B (EDNRB) is related to H3K9me3 binding with the EDNRB promoter region and is associated with the clinical T tumor stage in salivary adenoid cystic carcinoma
Xia, R., Wang, Z., Zhang, C., Hu, Y., Zhou, R., Wang, L., Tian, Z., & Jiang, L. (2015) · Oral Surgery Oral Medicine Oral Pathology and Oral Radiology · doi:10.1016/j.oooo.2015.04.015 · Cited by 6
Challenges and Advances in the Development of Cell Lines and Xenografts
Schweppe, R. E., & Korch, C. T. (2018) · Advances in Molecular Pathology · doi:10.1016/j.yamp.2018.07.004 · Cited by 6
Human Cell Line Authentication: The Critical First Step in Any Project Using Human Cell Lines
McLaren, R. S., Reid, Y. A., & Storts, D. R. (2012) · Methods in molecular biology · doi:10.1007/978-1-62703-230-8_21 · Cited by 5
Mutational and immunologic Landscape in malignant Salivary Gland Tumors harbor the potential for novel therapeutic strategies
Witte, H. M., Gebauer, N., & Steinestel, K. (2022) · Critical Reviews in Oncology/Hematology · doi:10.1016/j.critrevonc.2022.103592 · Cited by 5
Cell‐type‐specific tumour sensitivity identified with a bromodomain targeting PROTAC in adenoid cystic carcinoma
Rose, A. J., Fleming, M. M., Francis, J. C., Ning, J., Patrikeev, A., Chauhan, R., Harrington, K. J., & Swain, A. (2023) · The Journal of Pathology · doi:10.1002/path.6209 · Cited by 4
“There are few bona ﬁ de ACC cell lines, and most do not retain consistent MYB expression if a translocation is present [17,18].”
Background
Sodium Iodide Symporter Expression in Adenoid Cystic Carcinoma of the Head and Neck
Gainor, D. L., Chute, D. J., & Lorenz, R. R. (2015) · JAMA Otolaryngology–Head & Neck Surgery · doi:10.1001/jamaoto.2015.0970 · Cited by 4
Characterization of uniquely tumorigenic cancer stem cells in salivary gland adenoid cystic carcinoma
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“Phuchareon and colleagues identi ﬁ ed the cross contamination of 6 ACC cell lines widely used to study this disease (47).”
Deciphering NOTCH1 as a Biomarker in Adenoid Cystic Carcinoma: Insights From a Systematic Review With Meta‐Analysis
Slivar, I. D. S., Zanesco, B. D. A., Martins, M. D., Matos, L. L., Nunes, F. D., Schuch, L. F., & Wagner, V. P. (2025) · Journal of Oral Pathology and Medicine · doi:10.1111/jop.70028 · Cited by 3
“While the organoids have been obtained from ACC validated patient-derived xenograft (PDX) models, caution must be taken in the analysis of the second study as the cell line used (ACCM) has been shown to be contaminated with HeLa [32].”
Transcriptomic Prediction of Pig Liver-Enriched Gene 1 Functions in a Liver Cell Line
Zhang, Z., Wang, Z., Dang, Y., Wang, J., Jayaprakash, S., Wang, H., & He, J. H. (2020) · Genes · doi:10.3390/genes11040412 · Cited by 3
Establishment and characterization of cMYB-expressing human salivary adenoid cystic carcinoma cell lines (UM-HACC-14, UM-HACC-6) and matching patient-derived xenograft model (UM-PDX-HACC-14)
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Peer Review #1 of "On the reproducibility of science: unique identification of research resources in the biomedical literature (v0.1)"
(2013) · PeerJ · doi:10.7287/peerj.148v0.1/reviews/1
Peer Review #2 of "On the reproducibility of science: unique identification of research resources in the biomedical literature (v0.1)"
(2013) · PeerJ · doi:10.7287/peerj.148v0.1/reviews/2
Peer Review #2 of "On the reproducibility of science: unique identification of research resources in the biomedical literature (v0.2)"
(2013) · PeerJ · doi:10.7287/peerj.148v0.2/reviews/2

Authors: Phuchareon, J., Ohta, Y., Woo, J. M., Eisele, D. W., & Tetsu, O.
Affiliations: University of California, San Francisco (US)
Corresponding author: Tetsu, Osamu
ORCID: Eisele, David W.
Tetsu, Osamu
Venue: PLoS ONE
Publisher: Public Library of Science (PLoS)
Published: 2009-06-25
Volume: 4
Issue: 6
Pages: e6040
ISSN: 1932-6203 (ISSN-L)
DOI: 10.1371/journal.pone.0006040
PMC: PMC2698276
OpenAlex: W2000248995
Cited by: 105
References: 46
Citations by year: 2026: 4 · 2025: 4 · 2024: 2 · 2023: 5 · 2022: 3 · 2021: 3 · 2020: 4 · 2019: 2 · 2018: 10 · 2017: 14 · 2016: 10 · 2015: 5 · 2014: 7 · 2013: 10 · 2012: 9
FWCI: 7.44
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (unspecified)
Locations: PLoS ONE (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Figshare (submittedVersion, cc-by)
Funders: Adenoid Cystic Carcinoma Research Foundation
Johns Hopkins University
University of California, San Francisco
Topics: Health Sciences › Medicine › Surgery › Salivary Gland Tumors Diagnosis and Treatment
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Identification and Quantification in Food
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic diversity and population structure
Keywords: adenoid cystic carcinoma, cell line contamination, cell line authentication, short tandem repeat profiling, DNA fingerprinting, HeLa cells, T24 cells, salivary gland carcinoma
MeSH terms: Alleles, Animals, Urinary Bladder Neoplasms, Carcinoma, Adenoid Cystic, Electron Transport Complex IV, HeLa Cells, Humans, Salivary Gland Neoplasms, Gene Expression Regulation, Neoplastic, Gene Expression Profiling, Cell Line, Tumor, Mice, Rats

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Genetic Profiling Reveals Cross-Contamination and Misidentification of 6 Adenoid Cystic Carcinoma Cell Lines: ACC2, ACC3, ACCM, ACCNS, ACCS and CAC2

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