Evidence map›Paper›PMID 30654687›Full record

ArticleAutophagy2019

MIR93 (microRNA -93) regulates tumorigenicity and therapy response of glioblastoma by targeting autophagy.

Tianzhi Huang, Xuechao Wan, Angel A Alvarez, C David James, Xiao Song, Yongyong Yang, Namratha Sastry, Ichiro Nakano, Erik P Sulman, Bo Hu and 1 more

Open access · bronzeAbstract read
In one paragraph

Article in Autophagy, 2019. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 92 papers.

0numbers the graph read from it
0cells of the map it votes in
92citing papers in PubMed
12.1field-weighted citation impact, top 1% of its field
1 · What the graph read from it

What it found

Each row is one number read from the abstract, on the scale the paper reported it, with its interval. Left of the dashed line favours the treatment, right favours the comparator. Under each row is the sentence it came from. New to these charts? A ten-minute tutorial.

The abstract states no effect estimate the extractor could read, or names no intervention and outcome on the map, so this paper lights no cell and moves no belief. It is still indexed, cited and linked below.

2 · The registry

The trial behind it

Trials whose registry record cites this paper, or whose number appears in the abstract. A trial that started after this paper was published is citing it as background, not reporting it.

Neither the registry nor the abstract names a trial number. If this is a trial report, that itself is worth knowing.

3 · Its place in the literature

Who cites it

92 citing papers in PubMed, 127 citations in OpenAlex.

  1. Article
  2. Review
  3. Review
  4. Article
  5. Article
  6. Article
  7. Review
  8. The Biological Role and Clinical Significance of BECLIN-1 in Cancer.International journal of molecular sciences · 2025
    Review
  9. Review
  10. Review
  11. Review
  12. Review
  13. Dual role of autophagy in bone metastasis: mechanistic insights and therapeutic targeting.American journal of clinical and experimental urology · 2025
    Review
  14. Review
  15. Review
  16. Article
  17. Review
  18. Regulation of autophagy by non-coding RNAs in human glioblastoma.Medical oncology (Northwood, London, England) · 2024
    Review
  19. Article
  20. Blockage of Autophagy for Cancer Therapy: A Comprehensive Review.International journal of molecular sciences · 2024
    Review

32 more citing papers are in PubMed but not listed here.

4 · The record

Corrections and comments

PubMed lists nothing against this paper. Absence here is not a guarantee, only a check that was made.

5 · Who and what money

Authors and funding

11 authors at 3 institutions in 1 country.

Tianzhi Huanga The Ken & Ruth Devee Department of Neurology, Lou and Jean Malnati Brain Tumor Institute , The Robert H. Lurie Comprehensive Cancer Center, Northwestern Universityd Feinberg School of Medicine , Chicago , IL , USA.
Xuechao Wana The Ken & Ruth Devee Department of Neurology, Lou and Jean Malnati Brain Tumor Institute , The Robert H. Lurie Comprehensive Cancer Center, Northwestern Universityd Feinberg School of Medicine , Chicago , IL , USA.
Angel A Alvareza The Ken & Ruth Devee Department of Neurology, Lou and Jean Malnati Brain Tumor Institute , The Robert H. Lurie Comprehensive Cancer Center, Northwestern Universityd Feinberg School of Medicine , Chicago , IL , USA.
C David Jamesb Department of Neurological Surgery , Lou and Jean Malnati Brain Tumor Institute, The Robert H. Lurie Comprehensive Cancer Center, Northwestern University Feinberg School of Medicine , Chicago , IL , USA.
Xiao Songa The Ken & Ruth Devee Department of Neurology, Lou and Jean Malnati Brain Tumor Institute , The Robert H. Lurie Comprehensive Cancer Center, Northwestern Universityd Feinberg School of Medicine , Chicago , IL , USA.
Yongyong Yanga The Ken & Ruth Devee Department of Neurology, Lou and Jean Malnati Brain Tumor Institute , The Robert H. Lurie Comprehensive Cancer Center, Northwestern Universityd Feinberg School of Medicine , Chicago , IL , USA.
Namratha Sastrya The Ken & Ruth Devee Department of Neurology, Lou and Jean Malnati Brain Tumor Institute , The Robert H. Lurie Comprehensive Cancer Center, Northwestern Universityd Feinberg School of Medicine , Chicago , IL , USA.ORCID 0000-0003-4056-6044
Ichiro Nakanoc Department of Neurosurgery , University of Alabama at Birmingham , Birmingham , AL , USA.
Erik P Sulmand Department of Radiation Oncology , The University of Texas M. D. Anderson Cancer Center, Department of Radiation Oncology , Houston , TX , USA.ORCID 0000-0003-4933-9120
Bo Hua The Ken & Ruth Devee Department of Neurology, Lou and Jean Malnati Brain Tumor Institute , The Robert H. Lurie Comprehensive Cancer Center, Northwestern Universityd Feinberg School of Medicine , Chicago , IL , USA.
Shi-Yuan Chenga The Ken & Ruth Devee Department of Neurology, Lou and Jean Malnati Brain Tumor Institute , The Robert H. Lurie Comprehensive Cancer Center, Northwestern Universityd Feinberg School of Medicine , Chicago , IL , USA.ORCID 0000-0003-1737-0588
Northwestern University · USThe University of Texas MD Anderson Cancer Center · USUniversity of Alabama at Birmingham · US

Funding

STINGing GBM: A First-in- Man Clinical Trial in Surgical Resectable Recurrent GBMP50CA221747 · NCI · NORTHWESTERN UNIVERSITY AT CHICAGO · PI Atique U. Ahmed · 2018 to 2026
$21.4M
TRAINING PROGRAM IN SIGNAL TRANSDUCTION AND CANCERT32CA070085 · NCI · NORTHWESTERN UNIVERSITY AT CHICAGO · PI LEONIDAS C. PLATANIAS · 1997 to 2026
$5.7M
Glioblastoma Phenotype Modulation Through miRNA Control of Wnt SignalingR01NS093843 · NINDS · NORTHWESTERN UNIVERSITY AT CHICAGO · PI CHENG, SHI-YUAN · 2015 to 2019
$1.8M
Autophagy Regulation of Glioblastoma Tumorigenesis and Responses to TherapyR01NS095634 · NINDS · NORTHWESTERN UNIVERSITY AT CHICAGO · PI CHENG, SHI-YUAN · 2015 to 2019
$1.7M
Radiation + Temozolomide Induced Mutation and Malignant Progression of GBMR01NS095642 · NINDS · NORTHWESTERN UNIVERSITY AT CHICAGO · PI JAMES, CHARLES DAVID · 2016 to 2020
$1.6M
NCI NIH HHS P50 CA221747NCI NIH HHS T32 CA070085NINDS NIH HHS R01 NS093843NINDS NIH HHS R01 NS095634NINDS NIH HHS R01 NS095642
6 · The paper itself

Abstract

Macroautophagy/autophagy is a natural intracellular process that maintains cellular homeostasis and protects cells from death under stress conditions. Autophagy sustains tumor survival and growth when induced by common cancer treatments, including IR and cytotoxic chemotherapy, thereby contributing to therapeutic resistance of tumors. In this study, we report that the expression of MIR93, noted in two clinically relevant tumor subtypes of GBM, influenced GSC phenotype as well as tumor response to therapy through its effects on autophagy. Our mechanistic studies revealed that MIR93 regulated autophagic activities in GSCs through simultaneous inhibition of multiple autophagy regulators, including BECN1/Beclin 1, ATG5, ATG4B, and SQSTM1/p62. Moreover, two first-line treatments for GBM, IR and temozolomide (TMZ), as well as rapamycin (Rap), the prototypic MTOR inhibitor, decreased MIR93 expression that, in turn, stimulated autophagic processes in GSCs. Inhibition of autophagy by ectopic MIR93 expression, or via autophagy inhibitors NSC (an ATG4B inhibitor) and CQ, enhanced the activity of IR and TMZ against GSCs. Collectively, our findings reveal a key role for MIR93 in the regulation of autophagy and suggest a combination treatment strategy involving the inhibition of autophagy while administering cytotoxic therapy. Abbreviations: ACTB: actin beta; ATG4B: autophagy related 4B cysteine peptidase; ATG5: autophagy related 5; BECN1: beclin 1; CL: classical; CQ: chloroquine diphosphate; CSCs: cancer stem cells; GBM: glioblastoma; GSCs: glioma stem-like cells; HEK: human embryonic kidney; IB: immunoblotting; IF: immunofluorescent staining; IR: irradiation; MAP1LC3/LC3: microtubule associated protein 1 light chain 3; MES: mesenchymal; MIR93: microRNA 93; MIRC: a control miRNA; miRNA/miR: microRNA; MTOR: mechanistic target of rapamycin kinase; NSC: NSC185085; PN: proneural; qRT-PCR: quantitative reverse transcription-polymerase chain reaction; Rap: rapamycin; SQSTM1/p62: sequestosome 1; TCGA: the cancer genome atlas; TMZ: temozolomide; WT: wild type; ZIP93: lentiviral miRZIP targeting MIR93; ZIPC: lentiviral miRZip targeting control miRNA.

Indexed as

AnimalsAutophagyAutophagy-Related ProteinsGliomaHEK293 CellsHumansMice, NudeMicroRNAsNeoplastic Stem CellsSirolimusTemozolomideTransplantation, HeterologousAutophagy-Related ProteinsMicroRNAsMIRN93 microRNA, humanSirolimusTemozolomideAutophagycancer stem cellglioblastomaglioma subtypesmicroRNAtherapy response

Identifiers

PMID30654687
PMCPMC6526840
OpenAlexW2911075773

What OpenQuestion holds

Textmetadata
Read underepoch 390

Registered trials

None linked

Read under generation 80e0d062 · epoch 390. Bibliography from PubMed, PubMed Central and OpenAlex; grants from NIH RePORTER; trial links from ClinicalTrials.gov; estimates, votes and beliefs from the OpenQuestion graph.