ArticleScience translational medicine2018
Metarrestin, a perinucleolar compartment inhibitor, effectively suppresses metastasis.
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Article in Science translational medicine, 2018. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 48 papers.
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48citing papers in PubMed
3.1field-weighted citation impact, top 8% of its field
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Who cites it
48 citing papers in PubMed, 73 citations in OpenAlex.
- Development and characterization of endolysosomal trafficking targeting chimera degraders of αJournal of advanced research · 2026Article
- Nucleolar proteomics identifies S100A16 as a key nucleolar protein driving breast cancer metastasis.Cell death & disease · 2025Article
- Anticancer drug development against ribosome synthesis and the nucleolus.Biochemical Society transactions · 2025Article
- Targeting Eukaryotic Elongation Factor 1A: How Small-Molecule Inhibitors Suppress Tumor Growth via Diverse Pathways.International journal of molecular sciences · 2025Review
- Nucleolar beacon for monitoring nucleolar morphology and proteomics in living cells.Science advances · 2025Article
- Small Molecule with Big Impact: Metarrestin Targets the Perinucleolar Compartment in Cancer Metastasis.Cells · 2024Review
- The perinucleolar compartment: structure, function, and utility in anti-cancer drug development.Nucleus (Austin, Tex.) · 2024Article
- Crossing boundaries of light microscopy resolution discerns novel assemblies in the nucleolus.Histochemistry and cell biology · 2024Article
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- Targeting EMT using low-dose Teniposide by downregulating ZEB2-driven activation of RNA polymerase I in breast cancer.Cell death & disease · 2024Article
- Discovery of a nitroaromatic nannocystin with potent in vivo anticancer activity against colorectal cancer by targeting AKT1.Acta pharmacologica Sinica · 2024Article
- K-Homology Type Splicing Regulatory Protein: Mechanism of Action in Cancer and Immune Disorders.Critical reviews in eukaryotic gene expression · 2024Article
- Downregulation of stromal syntenin sustains AML development.EMBO molecular medicine · 2023Article
- Nucleolar structure connects with global nuclear organization.Molecular biology of the cell · 2023Article
- Determination of metarrestin (ML-246) in human plasma for a first-in-human clinical pharmacokinetic application by a simple and efficient uHPLC-MS/MS assay.Journal of chromatography. B, Analytical technologies in the biomedical and life sciences · 2023Article
- Article
- Nucleolar structure connects with global nuclear organization.bioRxiv : the preprint server for biology · 2023Article
- Anticancer Small-Molecule Agents Targeting Eukaryotic Elongation Factor 1A: State of the Art.International journal of molecular sciences · 2023Review
- Advancing translational science education.Clinical and translational science · 2022Review
- Ribosome Biogenesis: A Central Player in Cancer Metastasis and Therapeutic Resistance.Cancer research · 2022Review
Corrections and comments
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Authors and funding
48 authors at 10 institutions in 1 country.
Kevin J FrankowskiSpecialized Chemistry Center, The University of Kansas, Lawrence, KS 66047, USA.ORCID 0000-0002-7173-6352
Chen WangDepartment of Cell and Molecular Biology, Northwestern University, Chicago, IL 60611, USA.
Samarjit PatnaikNIH (National Institutes of Health) Chemical Genomics Center, National Center for Advancing Translational Sciences, NIH, Rockville, MD, 20850, USA.ORCID 0000-0002-4265-7620
Frank J SchoenenSpecialized Chemistry Center, The University of Kansas, Lawrence, KS 66047, USA.
Noel SouthallNIH (National Institutes of Health) Chemical Genomics Center, National Center for Advancing Translational Sciences, NIH, Rockville, MD, 20850, USA.ORCID 0000-0003-4500-880X
Dandan LiThoracic and Gastrointestinal Oncology Branch, National Cancer Institute, NIH, Bethesda, MD 20892, USA.
Yaroslav TeperThoracic and Gastrointestinal Oncology Branch, National Cancer Institute, NIH, Bethesda, MD 20892, USA.
Wei SunNIH (National Institutes of Health) Chemical Genomics Center, National Center for Advancing Translational Sciences, NIH, Rockville, MD, 20850, USA.ORCID 0000-0001-6742-1393
Irawati KandelaCenter for Developmental Therapeutics, Robert H. Lurie Comprehensive Cancer Center, Northwestern University, Evanston, IL 60208, USA.ORCID 0000-0002-8646-9357
Deqing HuDepartment of Biochemistry and Molecular Genetics, Feinberg School of Medicine, Northwestern University, Chicago, IL 60611, USA.
Christopher DextrasNIH (National Institutes of Health) Chemical Genomics Center, National Center for Advancing Translational Sciences, NIH, Rockville, MD, 20850, USA.ORCID 0000-0002-3070-6106
Zachary KnottsThoracic and Gastrointestinal Oncology Branch, National Cancer Institute, NIH, Bethesda, MD 20892, USA.ORCID 0000-0001-7557-1922
Yansong BianThoracic and Gastrointestinal Oncology Branch, National Cancer Institute, NIH, Bethesda, MD 20892, USA.
John NortonDepartment of Cell and Molecular Biology, Northwestern University, Chicago, IL 60611, USA.
Steve TitusNIH (National Institutes of Health) Chemical Genomics Center, National Center for Advancing Translational Sciences, NIH, Rockville, MD, 20850, USA.
Marzena A LewandowskaDepartment of Cell and Molecular Biology, Northwestern University, Chicago, IL 60611, USA.
Yiping WenDepartment of Cell and Molecular Biology, Northwestern University, Chicago, IL 60611, USA.
Katherine I FarleyDepartments of Molecular Biophysics and Biochemistry, Genetics, and Therapeutic Radiology, Yale University and Yale School of Medicine, New Haven, CT 06520, USA.ORCID 0000-0002-5552-2434
Lesley Mathews GrinerNIH (National Institutes of Health) Chemical Genomics Center, National Center for Advancing Translational Sciences, NIH, Rockville, MD, 20850, USA.ORCID 0000-0001-9847-1107
Jamey SultanNIH (National Institutes of Health) Chemical Genomics Center, National Center for Advancing Translational Sciences, NIH, Rockville, MD, 20850, USA.ORCID 0000-0002-1971-0243
Zhaojing MengCancer Research Technology Program, Frederick National Laboratory for Cancer Research, Leidos Biomedical Research Inc., Frederick, MD 21702, USA.ORCID 0000-0001-8808-5325
Ming ZhouCancer Research Technology Program, Frederick National Laboratory for Cancer Research, Leidos Biomedical Research Inc., Frederick, MD 21702, USA.ORCID 0000-0002-7460-550X
Tomas VilimasCenter for Advanced Preclinical Research, Frederick National Laboratory for Cancer Research, Leidos Biomedical Research Inc., Fort Detrick, Frederick, MD 21702, USA.
Astin S PowersLaboratory of Pathology, Center for Cancer Research, NIH, Bethesda, MD 20892, USA.ORCID 0000-0002-6514-2670
Serguei KozlovCenter for Advanced Preclinical Research, Frederick National Laboratory for Cancer Research, Leidos Biomedical Research Inc., Fort Detrick, Frederick, MD 21702, USA.ORCID 0000-0001-5253-2867
Kunio NagashimaElectron Microscope Laboratory, Leidos Biomedical Research Inc., Frederick National Laboratory for Cancer Research, Frederick, MD 21701, USA.ORCID 0000-0002-0381-8532
Humair S QuadriThoracic and Gastrointestinal Oncology Branch, National Cancer Institute, NIH, Bethesda, MD 20892, USA.ORCID 0000-0003-1708-5269
Min FangDepartment of Developmental, Molecular and Chemical Biology, Tufts University School of Medicine, Boston, MA 02111, USA.
Charles LongDepartment of Cell and Molecular Biology, Northwestern University, Chicago, IL 60611, USA.ORCID 0000-0003-3835-8537
Ojus KhanolkarDepartment of Cell and Molecular Biology, Northwestern University, Chicago, IL 60611, USA.
Warren ChenDepartment of Cell and Molecular Biology, Northwestern University, Chicago, IL 60611, USA.
Jinsol KangDepartment of Cell and Molecular Biology, Northwestern University, Chicago, IL 60611, USA.
Helen HuangDepartment of Cell and Molecular Biology, Northwestern University, Chicago, IL 60611, USA.
Eric ChowDepartment of Cell and Molecular Biology, Northwestern University, Chicago, IL 60611, USA.ORCID 0000-0002-1421-6502
Esthermanya GoldbergDepartment of Cell and Molecular Biology, Northwestern University, Chicago, IL 60611, USA.ORCID 0000-0002-4343-9203
Coral FeldmanDepartment of Cell and Molecular Biology, Northwestern University, Chicago, IL 60611, USA.
Romi XiDepartment of Cell and Molecular Biology, Northwestern University, Chicago, IL 60611, USA.
Hye Rim KimDepartment of Human Genetics, Cancer Biology Graduate Program, Emory University School of Medicine, Atlanta, GA 30322, USA.ORCID 0000-0002-6879-2644
Gary SahagianDepartment of Developmental, Molecular and Chemical Biology, Tufts University School of Medicine, Boston, MA 02111, USA.ORCID 0000-0002-0812-4943
Susan J BasergaDepartments of Molecular Biophysics and Biochemistry, Genetics, and Therapeutic Radiology, Yale University and Yale School of Medicine, New Haven, CT 06520, USA.
Andrew MazarCenter for Developmental Therapeutics, Robert H. Lurie Comprehensive Cancer Center, Northwestern University, Evanston, IL 60208, USA.
Marc FerrerNIH (National Institutes of Health) Chemical Genomics Center, National Center for Advancing Translational Sciences, NIH, Rockville, MD, 20850, USA.
Wei ZhengNIH (National Institutes of Health) Chemical Genomics Center, National Center for Advancing Translational Sciences, NIH, Rockville, MD, 20850, USA.ORCID 0000-0003-1034-0757
Ali ShilatifardDepartment of Biochemistry and Molecular Genetics, Feinberg School of Medicine, Northwestern University, Chicago, IL 60611, USA.ORCID 0000-0002-7490-2854
Jeffrey AubéSpecialized Chemistry Center, The University of Kansas, Lawrence, KS 66047, USA.ORCID 0000-0003-1049-5767
Udo RudloffThoracic and Gastrointestinal Oncology Branch, National Cancer Institute, NIH, Bethesda, MD 20892, USA. s-huang2@northwestern.edu maruganj@mail.nih.gov rudloffu@mail.nih.gov.ORCID 0000-0003-2137-9040
Juan Jose MaruganNIH (National Institutes of Health) Chemical Genomics Center, National Center for Advancing Translational Sciences, NIH, Rockville, MD, 20850, USA. s-huang2@northwestern.edu maruganj@mail.nih.gov rudloffu@mail.nih.gov.ORCID 0000-0002-3951-7061
Sui HuangDepartment of Cell and Molecular Biology, Northwestern University, Chicago, IL 60611, USA. s-huang2@northwestern.edu maruganj@mail.nih.gov rudloffu@mail.nih.gov.ORCID 0000-0002-2400-4319
Northwestern University · USNational Center for Advancing Translational Sciences · USNational Cancer Institute · USLeidos (United States) · USUniversity of Kansas · USRobert H. Lurie Comprehensive Cancer Center of Northwestern UniversityTufts University · USYale University · USCenter for Cancer Research · USEmory University · US
Funding
Tumor Environment and Metastasis (TEAM) Research ProgramP30CA060553 · NCI · NORTHWESTERN UNIVERSITY AT CHICAGO · PI Daniela E Matei · 1993 to 2026
$153.9MSkill Development for Diverse Scientific Careers: A New Course Predoctoral Program in Cellular and Molecular BiologyT32GM007223 · NIGMS · YALE UNIVERSITY · PI BASERGA, SUSAN J · 1985 to 2019
$31.0MDrug Repurposing Screening for Rare and Neglected DiseasesZIATR000018 · NCATS · NATIONAL CENTER FOR ADVANCING TRANSLATIONAL SCIENCES · PI ZHENG, WEI · 2015 to 2025
$24.6MPreclinical drug development in pancreatic cancerZIABC011267 · NCI · DIVISION OF BASIC SCIENCES - NCI · PI RUDLOFF, UDO · 2010 to 2025
$23.9MUniversity of Kansas Specialized Chemistry CenterU54HG005031 · NHGRI · UNIVERSITY OF KANSAS LAWRENCE · PI AUBE, JEFFREY · 2008 to 2013
$21.5MProgression of Metarrestin that Reduces PNC Prevalence and Elucidation of its Mechanism of ActionZIATR000208 · NCATS · NATIONAL CENTER FOR ADVANCING TRANSLATIONAL SCIENCES · PI MARUGAN, JUAN · 2015 to 2025
$3.4MThe Structure and Function of Perinucleolar CompartmentR01GM078555 · NIGMS · NORTHWESTERN UNIVERSITY AT CHICAGO · PI HUANG, SUI · 2007 to 2015
$2.6MKey factors in human ribosome biogenesisR01GM115710 · NIGMS · YALE UNIVERSITY · PI BASERGA, SUSAN J · 2015 to 2018
$1.6MPAX9, ribosome biogenesis, and congenital diseaseF31DE026946 · NIDCR · YALE UNIVERSITY · PI FARLEY, KATHERINE IRENE · 2017 to 2019
$81kNCI NIH HHS P30 CA060553NHGRI NIH HHS U54 HG005031NIDCR NIH HHS F31 DE026946NIGMS NIH HHS R01 GM078555NIGMS NIH HHS R01 GM115710NIGMS NIH HHS T32 GM007223
Abstract
Metastasis remains a leading cause of cancer mortality due to the lack of specific inhibitors against this complex process. To identify compounds selectively targeting the metastatic state, we used the perinucleolar compartment (PNC), a complex nuclear structure associated with metastatic behaviors of cancer cells, as a phenotypic marker for a high-content screen of over 140,000 structurally diverse compounds. Metarrestin, obtained through optimization of a screening hit, disassembles PNCs in multiple cancer cell lines, inhibits invasion in vitro, suppresses metastatic development in three mouse models of human cancer, and extends survival of mice in a metastatic pancreatic cancer xenograft model with no organ toxicity or discernable adverse effects. Metarrestin disrupts the nucleolar structure and inhibits RNA polymerase (Pol) I transcription, at least in part by interacting with the translation elongation factor eEF1A2. Thus, metarrestin represents a potential therapeutic approach for the treatment of metastatic cancer.
Indexed as
AnimalsCell Line, TumorCell NucleolusCell ProliferationChromatinDNA, RibosomalHumansMaleMiceNeoplasm InvasivenessNeoplasm MetastasisPancreatic NeoplasmsPeptide Elongation Factor 1Promoter Regions, GeneticPyrimidinesPyrrolesChromatinDNA, RibosomalEEF1A2 protein, humanmetarrestinPeptide Elongation Factor 1PyrimidinesPyrrolesRNA Polymerase IRNA Precursors
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