CoChat
Sign Up
Cited by 222

The DOI matches its Crossref record; 3 of the 3 references it cites were found in a registry or an index.

Extracellular Vesicles Modulate the Glioblastoma Microenvironment via a Tumor Suppression Signaling Network Directed by miR-1

Bronisz, Agnieszka, Wang, Yan, Nowicki, Michal O., Peruzzi, Pierpaolo, Ansari, Khairul I., Ogawa, Daisuke, Balaj, Leonora, De Rienzo, Gianluca, Mineo, Marco, Nakano, Ichiro, Ostrowski, Michael C., Hochberg, Fred, Weissleder, Ralph, Lawler, Sean E., Chiocca, E. Antonio, Godlewski, Jakub·2014·Cancer Research
DOI 10.1158/0008-5472.can-13-2650PMC PMC3928601

Published version of a preprint

Open this paper in CoChat — free account

Abstract

Extracellular vesicles have emerged as important mediators of intercellular communication in cancer, including by conveying tumor-promoting microRNAs between cells, but their regulation is poorly understood. In this study, we report the findings of a comparative microRNA profiling and functional analysis in human glioblastoma that identifies miR-1 as an orchestrator of extracellular vesicle function and glioblastoma growth and invasion. Ectopic expression of miR-1 in glioblastoma cells blocked in vivo growth, neovascularization, and invasiveness. These effects were associated with a role for miR-1 in intercellular communication in the microenvironment mediated by extracellular vesicles released by cancer stem–like glioblastoma cells. An extracellular vesicle–dependent phenotype defined by glioblastoma invasion, neurosphere growth, and endothelial tube formation was mitigated by loading miR-1 into glioblastoma-derived extracellular vesicles. Protein cargo in extracellular vesicles was characterized to learn how miR-1 directed extracellular vesicle function. The mRNA encoding Annexin A2 (ANXA2), one of the most abundant proteins in glioblastoma-derived extracellular vesicles, was found to be a direct target of miR-1 control. In addition, extracellular vesicle–derived miR-1 along with other ANXA2 extracellular vesicle networking partners targeted multiple pro-oncogenic signals in cells within the glioblastoma microenvironment. Together, our results showed how extracellular vesicle signaling promotes the malignant character of glioblastoma and how ectopic expression of miR-1 can mitigate this character, with possible implications for how to develop a unique miRNA-based therapy for glioblastoma management. Cancer Res; 74(3); 738–50. ©2013 AACR.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1158/0008-5472.can-13-2650

Cites

3 of 3 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Flagged first, then by citations

Research works printed but not linked: 46

  1. Hess, 2004, Adult glioma incidence trends in United States, 1977–2000, Cancer, 101, 2293, 10.1002/cncr.20621 · DOI
  2. Furnari, 2007, Malignant astrocytic glioma: genetics, biology, and paths to treatment, Genes Dev, 21, 2683, 10.1101/gad.1596707 · DOI · Paper page
  3. Lefranc, 2005, Possible future issues in the treatment of glioblastomas: special emphasis on cell migration and the resistance of migrating glioblastoma cells to apoptosis, J Clin Oncol, 23, 2411, 10.1200/JCO.2005.03.089 · DOI
  4. Lathia, 2011, Deadly teamwork: neural cancer stem cells and the tumor microenvironment, Cell Stem Cell, 8, 482, 10.1016/j.stem.2011.04.013 · DOI
  5. Calabrese, 2007, A perivascular niche for brain tumor stem cells, Cancer Cell, 11, 69, 10.1016/j.ccr.2006.11.020 · DOI
  6. Charles, 2011, The brain tumor microenvironment, Glia, 59, 1169, 10.1002/glia.21136 · DOI · Paper page
  7. Bonavia, 2011, Heterogeneity maintenance in glioblastoma: a social network, Cancer Res, 71, 4055, 10.1158/0008-5472.CAN-11-0153 · DOI
  8. van der Vos, 2011, Brain tumor microvesicles: insights into intercellular communication in the nervous system, Cell Mol Neurobiol, 31, 949, 10.1007/s10571-011-9697-y · DOI
  9. Peinado, 2012, Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET, Nat Med, 18, 883, 10.1038/nm.2753 · DOI · Paper page
  10. Mittelbrunn, 2011, Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells, Nat Commun, 2, 282, 10.1038/ncomms1285 · DOI
  11. Kucharzewska, 2013, Exosomes reflect the hypoxic status of glioma cells and mediate hypoxia-dependent activation of vascular cells during tumor development, Proc Natl Acad Sci U S A, 110, 7312, 10.1073/pnas.1220998110 · DOI · Paper page
  12. Skog, 2008, Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers, Nat Cell Biol, 10, 1470, 10.1038/ncb1800 · DOI · Paper page
  13. Janga, 2011, MicroRNAs as post-transcriptional machines and their interplay with cellular networks, Adv Exp Med Biol, 722, 59, 10.1007/978-1-4614-0332-6_4 · DOI
  14. Ferdin, 2010, Non-coding RNAs: identification of cancer-associated microRNAs by gene profiling, Technol Cancer Res Treat, 9, 123, 10.1177/153303461000900202 · DOI
  15. Godlewski, 2010, MicroRNAs and glioblastoma; the stem cell connection, Cell Death Differ, 17, 221, 10.1038/cdd.2009.71 · DOI · Paper page
  16. Nohata, 2012, microRNA-1/133a and microRNA-206/133b clusters: dysregulation and functional roles in human cancers, Oncotarget, 3, 9, 10.18632/oncotarget.424 · DOI
  17. Lokman, 2011, The role of annexin A2 in tumorigenesis and cancer progression, Cancer Microenviron, 4, 199, 10.1007/s12307-011-0064-9 · DOI
  18. An, 2009, Identification of gliotropic factors that induce human stem cell migration to malignant tumor, J Proteome Res, 8, 2873, 10.1021/pr900020q · DOI
  19. Zhai, 2011, Annexin A2 promotes glioma cell invasion and tumor progression, J Neurosci, 31, 14346, 10.1523/JNEUROSCI.3299-11.2011 · DOI
  20. Singh, 2003, Identification of a cancer stem cell in human brain tumors, Cancer Res, 63, 5821
  21. Giannini, 2005, Patient tumor EGFR and PDGFRA gene amplifications retained in an invasive intracranial xenograft model of glioblastoma multiforme, Neuro-oncology, 7, 164, 10.1215/S1152851704000821 · DOI
  22. Godlewski, 2010, MicroRNA-451 regulates LKB1/AMPK signaling and allows adaptation to metabolic stress in glioma cells, Mol Cell, 37, 620, 10.1016/j.molcel.2010.02.018 · DOI
  23. Williams, 2011, Indirubins decrease glioma invasion by blocking migratory phenotypes in both the tumor and stromal endothelial cell compartments, Cancer Res, 71, 5374, 10.1158/0008-5472.CAN-10-3026 · DOI
  24. Rothhammer, 2007, Functional implication of BMP4 expression on angiogenesis in malignant melanoma, Oncogene, 26, 4158, 10.1038/sj.onc.1210182 · DOI
  25. Bronisz, 2006, Microphthalmia-associated transcription factor interactions with 14-3-3 modulate differentiation of committed myeloid precursors, Mol Biol Cell, 17, 3897, 10.1091/mbc.e06-05-0470 · DOI
  26. Godlewski, 2008, Targeting of the Bmi-1 oncogene/stem cell renewal factor by microRNA-128 inhibits glioma proliferation and self-renewal, Cancer Res, 68, 9125, 10.1158/0008-5472.CAN-08-2629 · DOI · Paper page
  27. Datta, 2008, Methylation mediated silencing of MicroRNA-1 gene and its role in hepatocellular carcinogenesis, Cancer Res, 68, 5049, 10.1158/0008-5472.CAN-07-6655 · DOI
  28. Reid, 2012, miRNA profiling in colorectal cancer highlights miR-1 involvement in MET-dependent proliferation, Mol Cancer Res, 10, 504, 10.1158/1541-7786.MCR-11-0342 · DOI
  29. Shao, 2012, Protein typing of circulating microvesicles allows real-time monitoring of glioblastoma therapy, Nat Med, 18, 1835, 10.1038/nm.2994 · DOI
  30. Liu, 2013, Exosomes from murine-derived GL26 cells promote glioblastoma tumor growth by reducing number and function of CD8+T cells, Asian Pac J Cancer Prev, 14, 309, 10.7314/APJCP.2013.14.1.309 · DOI
  31. Ferretti, 2008, Concerted microRNA control of Hedgehog signalling in cerebellar neuronal progenitor and tumour cells, EMBO J, 27, 2616, 10.1038/emboj.2008.172 · DOI
  32. Kefas, 2008, microRNA-7 inhibits the epidermal growth factor receptor and the Akt pathway and is down-regulated in glioblastoma, Cancer Res, 68, 3566, 10.1158/0008-5472.CAN-07-6639 · DOI · Paper page
  33. Peruzzi, 2013, MicroRNA-128 coordinately targets Polycomb Repressor Complexes in glioma stem cells, Neuro-oncology, 15, 1212, 10.1093/neuonc/not055 · DOI · Paper page
  34. Bronisz, 2012, Reprogramming of the tumour microenvironment by stromal PTEN-regulated miR-320, Nat Cell Biol, 14, 159, 10.1038/ncb2396 · DOI
  35. Katakowski, 2013, Exosomes from marrow stromal cells expressing miR-146b inhibit glioma growth, Cancer Lett, 335, 201, 10.1016/j.canlet.2013.02.019 · DOI · Paper page
  36. Fleming, 2013, Differential expression of miR-1, a putative tumor suppressing microRNA, in cancer resistant and cancer susceptible mice, PeerJ, 1, e68, 10.7717/peerj.68 · DOI
  37. Hudson, 2012, MicroRNA-1 is a candidate tumor suppressor and prognostic marker in human prostate cancer, Nucleic Acids Res, 40, 3689, 10.1093/nar/gkr1222 · DOI
  38. Nasser, 2008, Down-regulation of micro-RNA-1 (miR-1) in lung cancer. Suppression of tumorigenic property of lung cancer cells and their sensitization to doxorubicin-induced apoptosis by miR-1, J Biol Chem, 283, 33394, 10.1074/jbc.M804788200 · DOI
  39. Bader, 2010, The promise of microRNA replacement therapy, Cancer Res, 70, 7027, 10.1158/0008-5472.CAN-10-2010 · DOI
  40. Matsuda, 2012, Targeting JNK for therapeutic depletion of stem-like glioblastoma cells, Sci Rep, 2, 516, 10.1038/srep00516 · DOI
  41. Yoon, 2012, c-Jun N-terminal kinase has a pivotal role in the maintenance of self-renewal and tumorigenicity in glioma stem-like cells, Oncogene, 31, 4655, 10.1038/onc.2011.634 · DOI
  42. Abdouh, 2009, BMI1 sustains human glioblastoma multiforme stem cell renewal, J Neurosci, 29, 8884, 10.1523/JNEUROSCI.0968-09.2009 · DOI
  43. Rak, 2013, Extracellular vesicles - biomarkers and effectors of the cellular interactome in cancer, Front Pharmacol, 4, 21, 10.3389/fphar.2013.00021 · DOI
  44. Hedhli, 2012, The annexin A2/S100A10 system in health and disease: emerging paradigms, J Biomed Biotechnol, 2012, 406273, 10.1155/2012/406273 · DOI
  45. Mussunoor, 2008, The role of annexins in tumour development and progression, J Pathol, 216, 131, 10.1002/path.2400 · DOI
  46. Gao, 2013, Correlation of expression levels of ANXA2, PGAM1, and CALR with glioma grade and prognosis, J Neurosurg, 118, 846, 10.3171/2012.9.JNS112134 · DOI

Cited by

Sorted by citations

Metadata

Authors
Bronisz, A., Wang, Y., Nowicki, M. O., Peruzzi, P., Ansari, K. I., Ogawa, D., Balaj, L., De Rienzo, G., Mineo, M., Nakano, I., Ostrowski, M. C., Hochberg, F., Weissleder, R., Lawler, S. E., Chiocca, E. A., & Godlewski, J.
Affiliations
Authors' Affiliations: 1Harvey Cushing Neuro-oncology Laboratories, Department of Neurosurgery, Brigham and Women's Hospital, Harvard Medical School, Boston; 2Neuroscience Center at Massachusetts General Hospital, Charlestown, Massachusetts; Departments of 3Neurological Surgery and 4Molecular and Cellular Biochemistry, The Ohio State University Medical Center, Columbus, Ohio
Venue
Cancer Research
Publisher
American Association for Cancer Research (AACR)
Published
2014-02-01
Volume
74
Issue
3
Pages
738-750
ISSN
  • 0008-5472
  • 1538-7445
DOI
10.1158/0008-5472.can-13-2650
PMC
PMC3928601
Cited by
222
References
3
Language
en

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review