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Targeting of the Bmi-1 Oncogene/Stem Cell Renewal Factor by MicroRNA-128 Inhibits Glioma Proliferation and Self-Renewal
Abstract
MicroRNAs (miR) show characteristic expression signatures in various cancers and can profoundly affect cancer cell behavior. We carried out miR expression profiling of human glioblastoma specimens versus adjacent brain devoid of tumor. This revealed several significant alterations, including a pronounced reduction of miR-128 in tumor samples. miR-128 expression significantly reduced glioma cell proliferation in vitro and glioma xenograft growth in vivo. miR-128 caused a striking decrease in expression of the Bmi-1 oncogene, by direct regulation of the Bmi-1 mRNA 3′-untranslated region, through a single miR-128 binding site. In a panel of patient glioblastoma specimens, Bmi-1 expression was significantly up-regulated and miR-128 was down-regulated compared with normal brain. Bmi-1 functions in epigenetic silencing of certain genes through epigenetic chromatin modification. We found that miR-128 expression caused a decrease in histone methylation (H3K27me3) and Akt phosphorylation, and up-regulation of p21CIP1 levels, consistent with Bmi-1 down-regulation. Bmi-1 has also been shown to promote stem cell self-renewal; therefore, we investigated the effects of miR-128 overexpression in human glioma neurosphere cultures, possessing features of glioma “stem-like” cells. This showed that miR-128 specifically blocked glioma self-renewal consistent with Bmi-1 down-regulation. This is the first example of specific regulation by a miR of a neural stem cell self-renewal factor, implicating miRs that may normally regulate brain development as important biological and therapeutic targets against the “stem cell–like” characteristics of glioma. [Cancer Res 2008;68(22):9125–30]
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In the citing paper
“Previous miRNA profiling studies, based on miRNA microarrays and PCR arrays, have revealed a number of miRNAs to be altered in gliomas [9], [14]–[16].”
From Reduced Expression of Brain-Enriched microRNAs in Glioblastomas Permits Targeted Regulation of a Cell Death Gene (2011) · cites this paper as [14]
In the citing paper
“MiRNAs down-regulated in gliomas include miR-7, miR-124, miR-128, miR-137, and miR-181a/b [9], [14], [15], [18], [19].”
From Reduced Expression of Brain-Enriched microRNAs in Glioblastomas Permits Targeted Regulation of a Cell Death Gene (2011) · cites this paper as [14]
In the citing paper
“We also observed high read counts for miR-21, amongst other miRNAs, in all glioblastoma samples compared to non-tumor samples, congruent with previous studies showing that this miRNA is highly up-regulated in glioblastoma (Table S4) [5], [9], [14], [15]; however, there was variability in the values for miR-21 across the samples and thus, the miRNA did not meet the final FDR selection criteria.”
From Reduced Expression of Brain-Enriched microRNAs in Glioblastomas Permits Targeted Regulation of a Cell Death Gene (2011) · cites this paper as [14]
In the citing paper
“Finally, miR-128, which is also abundantly expressed in neurons, has been shown to target the Bmi-1 stem cell renewal factor [14].”
From Reduced Expression of Brain-Enriched microRNAs in Glioblastomas Permits Targeted Regulation of a Cell Death Gene (2011) · cites this paper as [14]
In the citing paper
“miR-128 is one of the most significantly and consistently down-regulated miRNAs in glioblastomas and glioblastoma cell lines according to data presented here (Fig. 1) as well as previous studies [9], [14], [15], [31].”
From Reduced Expression of Brain-Enriched microRNAs in Glioblastomas Permits Targeted Regulation of a Cell Death Gene (2011) · cites this paper as [14]
In the citing paper
“Interestingly, the growth and viability of both A172 and U373 cells was not significantly affected by the overexpression of miR-128 (Fig. 3B, S5), contrary to previous studies using other glioma cell types that may retain more stem-cell like characteristics [14], [41].”
From Reduced Expression of Brain-Enriched microRNAs in Glioblastomas Permits Targeted Regulation of a Cell Death Gene (2011) · cites this paper as [14]
In the citing paper
“miR-7, miR-124, and miR-128 have been reported to impair cell growth and proliferation when over-expressed in glioma-derived stem cells [14], [15], [19], [41].”
From Reduced Expression of Brain-Enriched microRNAs in Glioblastomas Permits Targeted Regulation of a Cell Death Gene (2011) · cites this paper as [14]
In the citing paper
“Several studies showed that up-regulation of miR-128-3p profoundly reduced the expression of core protein components of PRC1 and PRC2: BMI-1 (Polycomb complex protein BMI-1)77,126,127 and SUZ12 (Polycomb protein SUZ12),77,128,129 respectively.”
From MiR-128-3p – a gray eminence of the human central nervous system (2024) · cites this paper as [126]
In the citing paper
“As the functional consequences of miR-128-3p,77,126 re-establishment and repression of PRCs subunits, pronounced alterations in histone modifications,77 as well as loss of stem-like features by GSCs, were observed in vitro and in vivo, as clearly shown by down-regulation of CD133 (Prominin-1) expression.77,126”
From MiR-128-3p – a gray eminence of the human central nervous system (2024) · cites this paper as [126]
In the citing paper
“The reintroduction of miR-128-3p77,126 significantly inhibited the radiation-induced expression of PRC subunits and consequently enhanced the radiosensitivity of GSCs accompanied by substantial DNA damage.77,126”
From MiR-128-3p – a gray eminence of the human central nervous system (2024) · cites this paper as [126]
In the citing paper
“MiR-128-3p was found to be a potent regulator of the expression and activity of proteins forming polycomb repressive complexes (PRCs).”
From MiR-128-3p – a gray eminence of the human central nervous system (2024) · cites this paper as [126]
In the citing paper
“As the functional consequences of miR-128-3p,77,126 re-establishment and repression of PRCs subunits, pronounced alterations in histone modifications,77 as well as loss of stem-like features by GSCs, were observed in vitro and in vivo, as clearly shown by down-regulation of CD133 (Prominin-1) expression.77,126”
From MiR-128-3p – a gray eminence of the human central nervous system (2024) · cites this paper as [126]
In the citing paper
“MicroRNAs particularly enriched in the normal brain, such as miR-128-3p, are almost universally suppressed in glioblastoma cells, regardless of their cellular subtype.45,126,130,211”
From MiR-128-3p – a gray eminence of the human central nervous system (2024) · cites this paper as [126]
In the citing paper
“Some functional studies provided several targets of miR-128-3p in cancer and immune cells,126,130 thus supporting the rationale for its application to enhance antitumor and pro-immune activity.”
From MiR-128-3p – a gray eminence of the human central nervous system (2024) · cites this paper as [126]
In the citing paper
“More importantly, EVs originating from non-malignant cells do not propagate pro-tumorigenic signals to cancer cells and are not toxic to normal cells and tissues.69,77,126,130,221”
From MiR-128-3p – a gray eminence of the human central nervous system (2024) · cites this paper as [126]
Citations
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Flagged first, then by citations
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Adlakha, Y. K., & Saini, N. (2014) · Molecular Cancer · doi:10.1186/1476-4598-13-33 · Cited by 213
MiR-137: an important player in neural development and neoplastic transformation
Mahmoudi, E., & Cairns, M. J. (2017) · Molecular Psychiatry · doi:10.1038/mp.2016.150 · Cited by 198
Exosomes as bio-inspired nanocarriers for RNA delivery: preparation and applications
Amiri, A., Bagherifar, R., Ansari Dezfouli, E., Kiaie, S. H., Jafari, R., & Ramezani, R. (2022) · Journal of Translational Medicine · doi:10.1186/s12967-022-03325-7 · Cited by 186
Epigenetic mechanisms in glioblastoma multiforme
Nagarajan, R. P., & Costello, J. F. (2009) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2009.02.005 · Cited by 176
Skalsky, R. L., & Cullen, B. R. (2011) · PLoS ONE · doi:10.1371/journal.pone.0024248 · Cited by 170
Metadata
- Authors
- Godlewski, J., Nowicki, M. O., Bronisz, A., Williams, S., Otsuki, A., Nuovo, G., RayChaudhury, A., Newton, H. B., Chiocca, E. A., & Lawler, S.
- Affiliations
- 1Dardinger Laboratory for Neuro-oncology and Neurosciences, Department of Neurological Surgery,
- 2Department of Molecular and Cellular Biochemistry, and
- 3Department of Pathology, The Ohio State University Medical Center and James Comprehensive Cancer Center, Columbus, Ohio
- Venue
- Cancer Research
- Published
- 2008-11-14
- Volume
- 68
- Issue
- 22
- Pages
- 9125-9130
- ISSN
- 0008-5472
- 1538-7445
- Cited by
- 587
- References
- 1
- Language
- en
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