Cited by 626MicroRNA in disease regulationCancer-related molecular mechanisms researchCancer-related Molecular Pathways

The DOI matches its Crossref record; 70 of the 74 references it cites were found in a registry or an index; 14 of the 43 sources its claims cite were checked for support.

Modulation of K-Ras-Dependent Lung Tumorigenesis by MicroRNA-21

Open access
Hatley, Mark E., Patrick, David M., Garcia, Matthew R., Richardson, James A., Bassel-Duby, Rhonda, van Rooij, Eva, Olson, Eric N.·2010·Cancer Cell

Abstract

Lung cancer is the leading cause of cancer-related deaths in the world, and non-small-cell lung cancer (NSCLC) accounts for 80% of cases. MicroRNA-21 (miR-21) expression is increased and predicts poor survival in NSCLC. Although miR-21 function has been studied in vitro with cancer cell lines, the role of miR-21 in tumor development in vivo is unknown. We utilize transgenic mice with loss-of-function and gain-of-function miR-21 alleles combined with a model of NSCLC to determine the role of miR-21 in lung cancer. We show that overexpression of miR-21 enhances tumorigenesis and that genetic deletion of miR-21 partially protects against tumor formation. MiR-21 drives tumorigenesis through inhibition of negative regulators of the Ras/MEK/ERK pathway and inhibition of apoptosis.

Overview

AI snapshot

Written from the paper’s full text.

TL;DR

In a K-rasLA2 mouse model of NSCLC, miR-21 overexpression increased lung tumor number/area and proliferation, while miR-21 deletion reduced tumor burden and sensitized transformed MEFs to doxorubicin-induced apoptosis. miR-21 acts as a tumor promoter by repressing Ras/MEK/ERK negative regulators (Spry1, Spry2, Btg2, Pdcd4) and pro-apoptotic genes (Apaf1, Faslg, Pdcd4, RhoB).

Key findings

  • CAG-miR-21;K-rasLA2 mice overexpressing miR-21 4–6 fold had significantly more gross lung tumors at 18 weeks and increased microscopic tumor number and total tumor area versus K-rasLA2 littermates; tumors showed increased proliferation, but survival did not differ, possibly due to decreased thymic tumor incidence.
  • miR-21−/−;K-rasLA2 mice had significantly fewer surface lung tumors at 20 weeks and decreased total tumor area; no adenocarcinomas were noted in any of 14 miR-21−/−/K-rasLA2 animals evaluated, and miR-21 deletion did not alter Ki67 proliferation.
  • miR-21 overexpression alone was not sufficient for tumorigenesis: CAG-miR-21 mice without K-rasLA2 (n = 39) followed up to 555 days showed no tumors.
  • Reporter assays showed 13 of 24 putative mouse miR-21 target 3′UTRs were repressed by miR-21, with mutation of the miR-21 site abrogating repression in 11; in tumors, miR-21 overexpression decreased Spry1, Spry2, Btg2, Pdcd4, Apaf1, Faslg, and RhoB and increased ERK phosphorylation. K-ras activation increased miR-21 expression 4-fold; miR-21−/− MEFs formed fewer soft agar colonies and smaller xenograft tumors and showed increased doxorubicin-induced apoptosis.

Methods

  • Generated conditional CAG-miR-21 overexpressing and miR-21−/− mice, crossed to the K-rasLA2 NSCLC model; comparisons were to littermate controls, with tumor burden assessed by H&E/ImageJ, proliferation by Ki67, and apoptosis by TUNEL.
  • MEFs from wild-type and miR-21−/− mice were immortalized with SV40 large T/small t and transformed with H-rasG12V; assays included soft agar, xenografts, doxorubicin treatment (100 nM–10 μM for 12 h), and TUNEL (1 μM for 12 h).
  • Luciferase reporter assays tested 24 putative miR-21 target 3′UTRs; Western blots were performed on micro-dissected tumors; statistics used two-tailed unpaired Student’s t-test with p < 0.05 considered significant.

Limitations

  • No formal limitations section is present; the authors state miR-21 overexpression alone was not sufficient for tumorigenesis and that tumors arising after miR-21 deletion may have developed escape mechanisms, possibly explaining latency.
  • The text notes miR-21 deletion did not alter apoptosis in lung lesions, suggesting those tumors escaped miR-21 regulatory effects; no adenocarcinomas were observed in 14 miR-21−/−;K-rasLA2 animals, a limited sample for that endpoint.
  • Evident from the text: all mice used were of mixed genetic backgrounds, and findings are from a mouse K-rasLA2 model and transformed MEFs, so human NSCLC causality and therapeutic implications remain to be tested.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1016/j.ccr.2010.08.013

Cites

70 of 70 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Verification

Claims the paper makes

14 of 43 cited sources checked · 6 supported · 0 flagged · accuracy not yet measured

Show all 69 claims

  • Probably not a substantial claim. 25
  • It may state two separate claims as one. 35
48 of 48
  • The paper relies on this without support.

    The K-rasLA2 mouse model is a valid model of human NSCLC for studying miR-21.

    “To explore the role of miR-21 in the pathogenesis of NSCLC, we utilized the K-rasLA2 murine lung cancer model, which harbors a targeted, latent K-ras G12D allele that is activated by two distinct recombination events (Johnson et al., 2001).”
  • The paper relies on this without support.

    The level of miR-21 over-expression achieved in CAG-miR-21 mice (4–6 fold) is representative of the increased miR-21 expression in human NSCLC.

    “which globally over-expressed miR-21 4–6 fold over normal levels of expression (Figure S1B–D).”
  • The paper relies on this without support.

    The miR-21 knockout mice do not have compensatory molecular changes that confound the interpretation of tumorigenesis experiments.

    “Homozygous miR-21 knock-out mice are viable, fertile, and born in expected Mendelian ratios without any gross phenotypic differences compared to wild type or heterozygous littermates, and without a cardiac phenotype (D.P., E.V.R. and E.N.O., manuscript in preparation).”
  • The paper relies on this without support.

    The antibodies used in Western blots specifically detect the intended target proteins.

    “We isolated individual tumors from mice, made whole tumor lysates, and performed Western blots for putative miR-21 targets to address the effect of miR-21 expression on the protein levels of the miR-21 target genes in vivo within lung tumors.”
  • The paper relies on this without support.

    The luciferase reporter assays in COS cells reflect endogenous miR-21 target regulation in mouse lung tumors.

    “Reporter assays in COS cells revealed miR-21 dependent repression of 13 of the 24 3′UTRs”
  • The paper relies on this without support.

    MicroRNAs are small non-coding RNAs that are commonly dysregulated in human malignancies and play a substantial role in the pathogenesis and survival of many cancers.

    “MicroRNAs are small non-coding RNAs that are commonly dysregulated in human malignancies and play a substantial role in the pathogenesis and survival of many cancers.”
  • The paper relies on this without support.

    MiR-21 is over-expressed in the majority of human malignancies including non-small cell lung cancer (NSCLC).

    “MiR-21 is over-expressed in the majority of human malignancies including non-small cell lung cancer (NSCLC).”
  • The paper relies on this without support.

    It is not clear whether miR-21 determines important aspects of lung cancer pathogenesis or is instead simply a marker for advanced disease.

    “However, it is not clear whether miR-21 determines important aspects of lung cancer pathogenesis or is instead simply a marker for advanced disease.”
  • The paper relies on this without support.

    Spry1, Spry2, Btg2, and Pdcd4 act as negative regulators of the Ras/MEK/ERK pathway.

    “which act as negative regulators of the Ras/MEK/ERK pathway”
  • The paper relies on this without support.

    Apaf1, Faslg, Pdcd4 and RhoB promote apoptosis.

    “which promote apoptosis”
10 of 10

Citations

Cites

  • Untitled work

    Bartel (2004) · doi:10.1016/s0092-8674(04)00045-5 · Cited by 34,714

  • “Expression of approximately 30% of human proteins appears to be regulated by miRNAs (Lewis et al., 2005).”
  • MicroRNA signatures in human cancers

    Calin, G. A., & Croce, C. M. (2006) · Nature reviews. Cancer · doi:10.1038/nrc1997 · Cited by 7,668 · cited 2×

    “…including non-small-cell lung cancer (NSCLC) (Volinia et al., 2006), and are predictive of tumor classification, prognosis, and response to therapy (Calin and Croce, 2006). miRNA expression patterns are remarkably reliable markers of cancers; in some cases, they have even proven more reliable than…”
  • Oncomirs—MicroRNAs with a role in cancer

    Esquela-Kerscher, A., & Slack, F. J. (2006) · Nature Reviews Cancer · doi:10.1038/nrc1840 · Cited by 5,884 · cited 4×

    “MicroRNAs are evolutionarily conserved, endogenous, nonprotein-coding, 20–23 nucleotide single-stranded RNAs that negatively regulate gene expression in a sequence-specific manner (Cho, 2007; Esquela-Kerscher and Slack, 2006; Voorhoeve and Agami, 2007).”
    Influential
  • A microRNA expression signature of human solid tumors defines cancer gene targets

    Volinia, S., Calin, G. A., Liu, C.-G., Ambs, S., Cimmino, A., Petrocca, F., Visone, R., Iorio, M., Roldo, C., Ferracin, M., et al. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0510565103 · Cited by 5,697 · cited 4×

    “A large-scale survey to determine the miRNA signature of 540 tumor samples—including lung, breast, stomach, prostate, colon, and pancreatic tumors and their respective normal adjacent tissue—revealed miR-21 was the only miRNA upregulated in all these tumors (Volinia et al., 2006).”
    Influential
  • Combinatorial microRNA target predictions

    Krek, A., Grün, D., Poy, M. N., Wolf, R., Rosenberg, L., Epstein, E. J., MacMenamin, P., da Piedade, I., Gunsalus, K. C., Stoffel, M., et al. (2005) · Nature Genetics · doi:10.1038/ng1536 · Cited by 4,603 · cited 2×

    “, 2007), and PicTar (Krek et al., 2005).”
  • Silencing of microRNAs in vivo with ‘antagomirs’

    Krützfeldt, J., Rajewsky, N., Braich, R., Rajeev, K. G., Tuschl, T., Manoharan, M., & Stoffel, M. (2005) · Nature · doi:10.1038/nature04303 · Cited by 3,949 · cited 2×

    “Methods have been developed to manipulate miRNA function pharmacologically, facilitating the development of new cancer therapeutic strategies (Hutvagner et al., 2004; Krutzfeldt et al., 2005).”
  • MicroRNA Targeting Specificity in Mammals: Determinants beyond Seed Pairing

    Grimson, A., Farh, K. K.-H., Johnston, W. K., Garrett-Engele, P., Lim, L. P., & Bartel, D. P. (2007) · Molecular Cell · doi:10.1016/j.molcel.2007.06.017 · Cited by 3,766 · cited 2×

    “Can miR-21 Targets Multiple Tumor Suppressor Genes To identify miR-21 effectors responsible for phenotypes observed, we utilized two algorithms that predict the mRNA targets of miRNAs, TargetScan (Grimson et al., 2007), and PicTar (Krek et al.”
  • The impact of microRNAs on protein output

    Baek, D., Villén, J., Shin, C., Camargo, F. D., Gygi, S. P., & Bartel, D. P. (2008) · Nature · doi:10.1038/nature07242 · Cited by 3,592 · cited 2×

    “Through interactions with 30 UTRs, miRNAs can modulate the expression of many genes simultaneously, often regulating individual signaling pathways at multiple levels (Baek et al., 2008; Selbach et al., 2008).”
  • Widespread changes in protein synthesis induced by microRNAs

    Selbach, M., Schwanhäusser, B., Thierfelder, N., Fang, Z., Khanin, R., & Rajewsky, N. (2008) · Nature · doi:10.1038/nature07228 · Cited by 3,429 · cited 2×

    “Through interactions with 30 UTRs, miRNAs can modulate the expression of many genes simultaneously, often regulating individual signaling pathways at multiple levels (Baek et al., 2008; Selbach et al., 2008).”

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Metadata

Authors
Hatley, M. E., Patrick, D. M., Garcia, M. R., Richardson, J. A., Bassel-Duby, R., van Rooij, E., & Olson, E. N.
Affiliations
The University of Texas Southwestern Medical Center (US)
Corresponding author
Olson, Eric N.
Venue
Cancer Cell
Publisher
Elsevier BV
Published
2010-09
Volume
18
Issue
3
Pages
282-293
ISSN
1535-6108 (ISSN-L)
OpenAlex
W2169354377
Cited by
626
References
74
Citations by year
2026: 12 · 2025: 15 · 2024: 26 · 2023: 22 · 2022: 38 · 2021: 31 · 2020: 28 · 2019: 29 · 2018: 42 · 2017: 31 · 2016: 40 · 2015: 72 · 2014: 57 · 2013: 62 · 2012: 63
FWCI
16.52
Type
journal article
Language
en
Open access
Locations
  • Cancer Cell (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (submittedVersion)
  • PubMed Central (submittedVersion)
Funders
  • National Heart, Lung, and Blood Institute (R01HL093039)
  • National Cancer Institute
  • Eunice Kennedy Shriver National Institute of Child Health and Human Development (K12HD000850)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer-related molecular mechanisms research
  • Health Sciences › Medicine › Oncology › Cancer-related Molecular Pathways
Keywords
miR-21, KRAS, lung carcinogenesis, non-small cell lung cancer, Ras/MEK/ERK pathway, apoptosis inhibition, transgenic mouse model, tumor suppressor microRNA
MeSH terms
Animals, Carcinoma, Non-Small-Cell Lung, Cell Transformation, Neoplastic, Humans, Lung Neoplasms, Mice, Nude, Mice, Transgenic, Genes, ras, Signal Transduction, MicroRNAs, Cell Line, Tumor, Mice

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