ArticleNature communications2016
A miR-192-EGR1-HOXB9 regulatory network controls the angiogenic switch in cancer.
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In one paragraph
Article in Nature communications, 2016. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 77 papers, 1 of them a synthesis that pooled it.
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77citing papers in PubMed, 1 pooled it
8.0field-weighted citation impact, top 2% of its field
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Who cites it
77 citing papers in PubMed, 1 synthesis or guideline pooled it, 119 citations in OpenAlex.
- Liposomal delivery of gene therapy for ovarian cancer: a systematic review.Reproductive biology and endocrinology : RB&E · 2023Pooled it
- Single-Cell RNA Sequencing Identifies MMP11Advanced science (Weinheim, Baden-Wurttemberg, Germany) · 2025Article
- Value of Bioinformatics Models for Predicting Translational Control of Angiogenesis.Circulation research · 2025Review
- Molecular mechanisms of miR-192 in cancer: a biomarker and therapeutic target.Cancer cell international · 2025Review
- HOXA9 versus HOXB9; particular focus on their controversial role in tumor pathogenesis.Journal of applied genetics · 2024Review
- Circulating micrornas as potential diagnostic biomarkers for cervical intraepithelial neoplasia and cervical cancer: a systematic review and meta-analysis.Discover oncology · 2024Review
- miR-146a inhibits ovarian tumor growthMolecular therapy oncolytics · 2023Article
- EGR1 Regulation of Vasculogenic Mimicry in the MDA-MB-231 Triple-Negative Breast Cancer Cell Line through the Upregulation of KLF4 Expression.International journal of molecular sciences · 2023Article
- Targeting miRNAs and Other Non-Coding RNAs as a Therapeutic Approach: An Update.Non-coding RNA · 2023Review
- The JNK-EGR1 signaling axis promotes TNF-α-induced endothelial differentiation of human mesenchymal stem cells via VEGFR2 expression.Cell death and differentiation · 2023Article
- HOXB9 Overexpression Confers Chemoresistance to Ovarian Cancer Cells by Inducing ERCC-1, MRP-2, and XIAP.International journal of molecular sciences · 2023Article
- Visual analytics identifies key miRNAs for differentiating peripancreatic paraganglioma and pancreatic neuroendocrine tumors.Frontiers in endocrinology · 2023Article
- MicroRNAs in T Cell-Immunotherapy.International journal of molecular sciences · 2022Review
- Chemical Factory-Guaranteed Enhanced Chemodynamic Therapy for Orthotopic Liver Cancer.Advanced science (Weinheim, Baden-Wurttemberg, Germany) · 2022Article
- Circulating miRNAs and Vascular Injury Markers Associate with Cardiovascular Function in Older Patients Reaching End-Stage Kidney Disease.Non-coding RNA · 2022Article
- Anti-angiogenic therapy in ovarian cancer: current situation & prospects.The Indian journal of medical research · 2021Review
- LncRNA XIST upregulates TRIM25 via negatively regulating miR-192 in hepatitis B virus-related hepatocellular carcinoma.Molecular medicine (Cambridge, Mass.) · 2021Article
- Dysregulation of exosomal miR-192 and miR-194 expression in lung adenocarcinoma patients.Saudi journal of biological sciences · 2021Article
- Therapeutic Targeting of MicroRNAs in the Tumor Microenvironment.International journal of molecular sciences · 2021Review
- MiRNAs as Anti-Angiogenic Adjuvant Therapy in Cancer: Synopsis and Potential.Frontiers in oncology · 2021Review
17 more citing papers are in PubMed but not listed here.
Corrections and comments
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Authors and funding
37 authors at 5 institutions in 5 countries.
Sherry Y WuDepartment of Gynecologic Oncology, The University of Texas MD Anderson Cancer Center, Houston, Texas 77030, USA.
Rajesha RupaimooleDepartment of Gynecologic Oncology, The University of Texas MD Anderson Cancer Center, Houston, Texas 77030, USA.
Fangrong ShenDepartment of Gynecologic Oncology, The University of Texas MD Anderson Cancer Center, Houston, Texas 77030, USA.
Sunila PradeepDepartment of Gynecologic Oncology, The University of Texas MD Anderson Cancer Center, Houston, Texas 77030, USA.
Chad V PecotDivision of Cancer Medicine, The University of Texas MD Anderson Cancer Center, Houston, Texas 77030, USA.
Cristina IvanDepartment of Gynecologic Oncology, The University of Texas MD Anderson Cancer Center, Houston, Texas 77030, USA.ORCID http://orcid.org/0000-0002-4848-0168
Archana S NagarajaDepartment of Gynecologic Oncology, The University of Texas MD Anderson Cancer Center, Houston, Texas 77030, USA.
Kshipra M GharpureDepartment of Gynecologic Oncology, The University of Texas MD Anderson Cancer Center, Houston, Texas 77030, USA.
Elizabeth PhamDepartment of Gynecologic Oncology, The University of Texas MD Anderson Cancer Center, Houston, Texas 77030, USA.
Hiroto HatakeyamaDepartment of Gynecologic Oncology, The University of Texas MD Anderson Cancer Center, Houston, Texas 77030, USA.
Michael H McGuireDepartment of Gynecologic Oncology, The University of Texas MD Anderson Cancer Center, Houston, Texas 77030, USA.
Monika HaemmerleDepartment of Gynecologic Oncology, The University of Texas MD Anderson Cancer Center, Houston, Texas 77030, USA.
Viviana Vidal-AnayaDepartment of Gynecologic Oncology, The University of Texas MD Anderson Cancer Center, Houston, Texas 77030, USA.
Courtney OlsenDepartment of Gynecologic Oncology, The University of Texas MD Anderson Cancer Center, Houston, Texas 77030, USA.ORCID http://orcid.org/0000-0003-2685-0217
Cristian Rodriguez-AguayoDivision of Cancer Medicine, The University of Texas MD Anderson Cancer Center, Houston, Texas 77030, USA.ORCID http://orcid.org/0000-0002-7880-7723
Justyna FilantDepartment of Gynecologic Oncology, The University of Texas MD Anderson Cancer Center, Houston, Texas 77030, USA.
Ehsan A EhsanipourDepartment of Cancer Biology, The University of Texas MD Anderson Cancer Center, Houston, Texas 77030, USA.
Shelley M HerbrichDepartment of Gynecologic Oncology, The University of Texas MD Anderson Cancer Center, Houston, Texas 77030, USA.
Sourindra N MaitiDivision of Pediatrics, The University of Texas MD Anderson Cancer Center, Houston, Texas 77030, USA.
Li HuangDepartment of Cancer Biology, The University of Texas MD Anderson Cancer Center, Houston, Texas 77030, USA.
Ji Hoon KimDepartment of Systems Biology, The University of Texas MD Anderson Cancer Center, Houston, Texas 77030, USA.ORCID http://orcid.org/0000-0003-3924-0434
Xinna ZhangCenter for RNA Interference and Non-Coding RNA, The University of Texas MD Anderson Cancer Center, Houston, Texas 77030, USA.
Hee-Dong HanDepartment of Gynecologic Oncology, The University of Texas MD Anderson Cancer Center, Houston, Texas 77030, USA.
Guillermo N Armaiz-PenaDepartment of Gynecologic Oncology, The University of Texas MD Anderson Cancer Center, Houston, Texas 77030, USA.
Elena G SeviourDepartment of Systems Biology, The University of Texas MD Anderson Cancer Center, Houston, Texas 77030, USA.
Sue TuckerDepartment of Bioinformatics, The University of Texas MD Anderson Cancer Center, Houston, Texas 77030, USA.
Min ZhangDepartment of Pharmaceutical Sciences, University of Pittsburgh, Pittsburgh, Pennsylvania 15213, USA.
Da YangDepartment of Pharmaceutical Sciences, University of Pittsburgh, Pittsburgh, Pennsylvania 15213, USA.
Laurence J N CooperDivision of Pediatrics, The University of Texas MD Anderson Cancer Center, Houston, Texas 77030, USA.ORCID http://orcid.org/0000-0003-1460-3905
Rouba Ali-FehmiDepartment of Pathology, Wayne State University School of Medicine, Karmanos Cancer Institute, Detroit, Michigan 48201, USA.
Menashe Bar-EliDepartment of Cancer Biology, The University of Texas MD Anderson Cancer Center, Houston, Texas 77030, USA.
Ju-Seog LeeDepartment of Systems Biology, The University of Texas MD Anderson Cancer Center, Houston, Texas 77030, USA.
Prahlad T RamDepartment of Systems Biology, The University of Texas MD Anderson Cancer Center, Houston, Texas 77030, USA.
Keith A BaggerlyDepartment of Bioinformatics, The University of Texas MD Anderson Cancer Center, Houston, Texas 77030, USA.
Gabriel Lopez-BeresteinDepartment of Medicine, The University of North Carolina, Chapel Hill, North Carolina 27599 USA.
Mien-Chie HungDepartment of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center, Houston, Texas 77030, USA.
Anil K SoodDepartment of Gynecologic Oncology, The University of Texas MD Anderson Cancer Center, Houston, Texas 77030, USA.
The University of Texas MD Anderson Cancer Center · USUniversity of North Carolina at Chapel Hill · USUniversity of Pittsburgh · USSunnybrook Health Science Centre · CAWayne State University · US
Funding
Tumor Evolution and Metastasis ProgramP30CA016672 · NCI · UNIVERSITY OF TX MD ANDERSON CAN CTR · PI Scott Kopetz · 1985 to 2026
$290.8MUNIVERSITY OF TEXAS MD ANDERSON SPORE IN OVARIAN CANCERP50CA083639 · NCI · UNIVERSITY OF TX MD ANDERSON CAN CTR · PI BAST, ROBERT C · 1999 to 2015
$33.0MTargeting the PI3K Signaling Pathway in Endometrial CarcinomaP50CA098258 · NCI · UNIVERSITY OF TX MD ANDERSON CAN CTR · PI BODURKA, DIANE · 2003 to 2020
$32.0MTexas Center for Cancer NanomedicineU54CA151668 · NCI · UNIVERSITY OF TEXAS HLTH SCI CTR HOUSTON · PI FERRARI, MAURO · 2010 to 2014
$12.4MCenter for Systems Analysis of the Cancer RegulomeU24CA143835 · NCI · INSTITUTE FOR SYSTEMS BIOLOGY · PI SHMULEVICH, ILYA · 2009 to 2016
$10.6MTRAINING FOR ACADEMIC ONCOLOGY/HEMATOLOGYT32CA009666 · NCI · UNIVERSITY OF TX MD ANDERSON CAN CTR · PI Michael Davies, Courtney DiNardo · 1994 to 2026
$9.8MTraining of Academic Gynecologic OncologistsT32CA101642 · NCI · UNIVERSITY OF TX MD ANDERSON CAN CTR · PI ANIL K SOOD, Kathleen Schmeler · 2005 to 2026
$9.2MOvarian Cancer: Mechanisms of Neuroendocrine RegulationR01CA109298 · NCI · UNIVERSITY OF TX MD ANDERSON CAN CTR · PI SOOD, ANIL K · 2005 to 2017
$4.5MNanovectors for Characterization and Destruction of Breast Tumor VasculatureR01CA128797 · NCI · UNIVERSITY OF TEXAS HLTH SCI CTR HOUSTON · PI FERRARI, MAURO · 2007 to 2010
$1.7MNovel extra cellular RNA-based combinatorial RNA inhibition therapyUH2TR000943 · NCATS · UNIVERSITY OF TX MD ANDERSON CAN CTR · PI CALIN, GEORGE A., LOPEZ-BERESTEIN, GABRIEL · 2013 to 2014
$1.1MNew Reagents for RNA-based Therapeutic TechnologiesR44GM086937 · NIGMS · AM BIOTECHNOLOGIES, LLC · PI YANG, XIANBIN · 2013 to 2014
$997kNew Reagents for Synthesis of High Potency siRNAR44GM084552 · NIGMS · AM BIOTECHNOLOGIES, LLC · PI EVERS, BERNARD MARK, SOOD, ANIL K · 2010 to 2011
$949kNCATS NIH HHS UH2 TR000943NCI NIH HHS CA009666NCI NIH HHS CA016672NCI NIH HHS CA109298NCI NIH HHS CA128797NCI NIH HHS NCI CA016672NCI NIH HHS P30 CA016672NCI NIH HHS P30CA16672NCI NIH HHS P50 CA083639NCI NIH HHS P50 CA098258NCI NIH HHS R01 CA109298NCI NIH HHS R01 CA128797NCI NIH HHS T32 CA009666NCI NIH HHS T32 CA101642NCI NIH HHS U24 CA143835NCI NIH HHS U24CA143835NCI NIH HHS U54 CA151668NIGMS NIH HHS GM084552-04NIGMS NIH HHS GM086937-01NIGMS NIH HHS GM100777-01NIGMS NIH HHS R43 GM084552NIGMS NIH HHS R43 GM086937NIGMS NIH HHS R43 GM100777NIGMS NIH HHS R44 GM084552NIGMS NIH HHS R44 GM086937
Abstract
A deeper mechanistic understanding of tumour angiogenesis regulation is needed to improve current anti-angiogenic therapies. Here we present evidence from systems-based miRNA analyses of large-scale patient data sets along with in vitro and in vivo experiments that miR-192 is a key regulator of angiogenesis. The potent anti-angiogenic effect of miR-192 stems from its ability to globally downregulate angiogenic pathways in cancer cells through regulation of EGR1 and HOXB9. Low miR-192 expression in human tumours is predictive of poor clinical outcome in several cancer types. Using 1,2-dioleoyl-sn-glycero-3-phosphatidylcholine (DOPC) nanoliposomes, we show that miR-192 delivery leads to inhibition of tumour angiogenesis in multiple ovarian and renal tumour models, resulting in tumour regression and growth inhibition. This anti-angiogenic and anti-tumour effect is more robust than that observed with an anti-VEGF antibody. Collectively, these data identify miR-192 as a central node in tumour angiogenesis and support the use of miR-192 in an anti-angiogenesis therapy.
Indexed as
Gene Regulatory NetworksAnimalsCell Line, TumorDown-RegulationEarly Growth Response Protein 1FemaleGenetic TherapyHomeodomain ProteinsHumansKidney NeoplasmsMiceMicroRNAsNeovascularization, PathologicOvarian NeoplasmsPhosphatidylcholinesTumor Burden1,2-oleoylphosphatidylcholineEarly Growth Response Protein 1EGR1 protein, humanHomeodomain ProteinsHOXB9 protein, humanMicroRNAsMIRN192 microRNA, humanPhosphatidylcholines
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