Significance and Therapeutic Value of miRNAs in Embryonal Neural Tumors
Abstract
:1. Introduction
2. Embryonal Tumors of the Central and Peripheral Nervous System
3. microRNAs
4. miRNAs in Embryonic Cell Function and Tumor Development
5. Role of miRNAs in Embryonal Neuronal Tumors
5.1. Medulloblastoma
Tumor | miRNA regulation | Validated or putative targets | Potential function | References |
---|---|---|---|---|
MB Reviewed in [101,102,103,104] | miR-17/92 Up | TSP-1, Bmi-1, PTEN, PP2A | Enhances proliferation, angiogenesis and confers growth advantage to MBs | [90,105,106] |
Let-7 Down | RAS STAT3 | Disregulation leads to a less differentiated cellular state | [107,108] | |
miR-199b-5p Down | HES1 Notch pathway ErbB2 | Inhibits tumor growth and metastasis. Its restoration blocks expression of several cancer stem-cell genes | [109] | |
miR-34a Down | Notch ligand Delta-like 1 (Dll1) | Negatively regulates cell proliferation, and induces apoptosis and neural differentiation in MB cells | [110] | |
miR-214 Up | Gli1 | Undefined | [27] | |
miR-125a Down | t-TrkC | Its restoration decreases proliferation, augments apoptosis, and promotes arrest of MB tumor cell growth. | [107] | |
miR-9 Down | REST/NRSF, Hes1 | Inhibits MB cell proliferation and promotes differentiation | [107,111] | |
miR-125b miR-324-5p miR-326 Down | PKM2, SMO, Notch | Inhibits MB cell proliferation, and reduces the size and number of MB cell colonies | [27,112] | |
miR-124a Down | CDK6, SLC16A1, REST, BAF34a, RB1, t-TrkC | Cell cycle regulation. Inhibits proliferation and induces apoptosis | [25,65,88,113,114] | |
* (miR-30b and miR-30d) Up | Undefined Both miRNAs are part of an amplicon containing the KHDRBS3 gene on 8q24.22 in MB cell lines | Undefined | [115] | |
miR-218 Down | EGFR, Bcl-2, B-catenin and MAPK9 | Iinduces apoptosis, inhibits MB tumor growth and invasiveness | [116,117] | |
* miR-31 and miR-153 Down | Undefined. however, miR-153 is found in high ErbB2 expressing MB | Undefined | [107,117] | |
miR-106b Up | p21 | Cell cycle arrest | [107,116] | |
miR-128a miR-128b miR-181b Down | Bmi-1 | Inhibits growth of MB cells. miR-128a, alters the intracellular redox state and promotes cellular senescence in MB cancer stem cells, which are thought to be resistant to therapy due to their low ROS states | [91,118] | |
MB Reviewed in [101,102,103,104] | miR-21 Up | PDCD4. | Pro-metastatic miRNA in MB. Involved in mitotic signaling, cell cycle, cell migration | [100] |
miR-183~96~182 cluster Up | Undefined, however knockdown of the full miR-183~96~182 cluster results in enrichment of genes associated with apoptosis and dysregulation of the PI3K/AKT/mTOR signaling axis | Regulates multiple biological programs that converge to support the maintenance and metastatic potential of MB | [119] | |
* miR-216, miR-135b, miR-217, miR-592, miR-340 Up | Undefined | Undefined | [95] | |
* miR-92b, miR-23a, miR-27a, miR-146b, miR-22 Down | Undefined | Undefined | [95] | |
miR-148a. Up. | Undefined | Undefined | [120] | |
sPNET [103] | * miR-517c miR- 520g Up | Undefined | Undefined | [121] |
* miR-19a, miR-106b and miR-19 Up | Undefined | Undefined | [107] | |
AT/RT | miR-9 Down | Undefined | Undefined | [107,111] |
miR-517c, miR-520g Up | miR-517c WNT/JNK signaling miR-520g ABCG2. | Undefined | [121,122] | |
miR-221, miR-222 Up | p27Kip1 | Promotes proliferation through cell cycle progression in AT/RT cells | [123] | |
* miR-520b, miR-629, miR-498, miR-373 Up | Undefined | Undefined | [95] | |
* miR-140, let-7b, miR-139, miR-153, miR-376b Down | Undefined | Undefined | [95] | |
let-7 miRNA family Down | HMGA2 | Suppresses proliferation and colony formation and abolishes the invasive potential | [124] | |
NB Adapted from [102] | miR-17-92 Up | DKK3, CDKN1A, BIM, ER-α, MEF2D | Increases proliferation, decreases apoptosis and inhibits TGF-β signaling. miR-17-5p inhibition abolish growth of therapy-resistant NB in vitro as well as in vivo | [125,126,127,128,129,130,131] |
miR-124 Undefined | AHR | Inhibits apoptosis and differentiation | [127,128,129,130] | |
miR-181 Up | ATM | Undefined | [125] | |
miR-21 Up | PTEN | Promotes proliferation, and decreases sensitivity to chemotherapy | [127,128,129,130] | |
miR-380-5p Up | P53 | Decreases apoptosis | [132] | |
miR-15a Up | RECK | Promotes migration through the induction of MMP-9 expression | [133] | |
* miRNA-125a/b Induced upon treatment with RA | Modulate expression of the TrkC neurotrophin receptor | Undefined | [94,134] | |
miR-184 Undefined | Akt2 downstream effector of the pro-survival pathway PI3K | Pro-apoptotic effects. Mediates proliferation reduction and inhibition of tumor growth in an orthotopic murine model of NB | [135] | |
miR-128 Undefined | Reelin and DCX | Mediates differentiation, reduces motility, invasiveness, and growth of NB cells | [136] | |
miR-34a miR-34c miR-410,487b Down | E2F3, BCL2, CCND1, CDK4, MYCN, P53 | Inhibits proliferation and induces apoptosisEctopic expression of miR-34a leads to cell-cycle arrest in NB lines | [127,134,135,137,138,139] | |
miR-542-5p Expressed in favorable NB, absent in unfavorable NB | GRIN3A, SH3GLB2, SNIP | Inhibits tumor growth, invasiveness and metastasis. | [125,140] | |
miR-628 Expressed in favorable NB, absent in unfavorable NB | Undefined | Undefined | [125,140] | |
miR-let-7 Down-regulated in NB with MYCN amplification | MYCN | Inhibits proliferation and induces differentiation. Altered expression of let-7 leads to a less differentiated cellular state | [141] | |
miR-101 Down-regulated in NB with MYCN amplification | MYCN | Inhibits proliferation and clonogenic growth | [141] | |
NB Adapted from [102] | miR-885-5p Down | CDK2, MCM5 | Inhibits cell cycle progression and survival | [142] |
miR-27b Down | PPARγ | Inhibits tumor growth | [143] | |
miR-138 Down | Undefined | Decreases viability and growth | [144] | |
miR-137 Down | KDM1A | Inhibits proliferation and induces apoptosis | [145] | |
miR-204 Down | BCL2, NTRK2. | Increases sensitivity to cisplatin and etoposide | [146,147] | |
miR-190 Down in aggressive NB with unknown mechanism | NEUROD1 | Inhibits TrkB pathwayand aggressive phenotypes. | [147] | |
miR-10a/b Down | NCOR2 miR-10a/b | Induces differentiation | [148] | |
miR-335 Down | ROCK1, MAPK1, LRG1 | Inhibits migration and invasion | [149,150] | |
miR-363 Down | Undefined | Inhibits invasiveness and metastasis | [149] | |
miR-9 Down | MMP-14 | Inhibits the invasion, metastasis, and angiogenesis | [151] | |
miR-145 Down | HIF-2α | Inhibits NB cell growth, invasion, metastasis and angiogenesis | [152] | |
* miR-140 let-7b miR-139 miR-153 miR-376b Down | Undefined | Undefined | [95] | |
let-7a3/let-7b miRNA Down | HMGA2 | Undefined | [124] |
miRNAs up/down regulated in high-risk NB | miRNAs up-regulated in metastatic NB | miRNAs up/down regulated as a marker for poor survival of NB | miRNAs up/down regulated in unfavorable NB |
---|---|---|---|
↑miR-18b, ↑miR-20a, ↑miR-22, | miR-24, | ↑miR-380-5p, ↑miR-17-92 | ↑miR-181, ↑miR-21, |
and ↑miR-129 and ↓miR-30b, | miR-342-3p, | miR-18a and miR-19a | ↓miR-30c, ↓miR-149, |
↓miR-146a, ↓miR-190, ↓miR-204, ↓miR-215, ↓miR-299-5p, ↓miR-362, ↓miR-382, ↓miR-411, ↓miR-424, ↓miR-425, ↓miR-487b, ↓miR-532, ↓miR-629, ↓miR-656, ↓miR-660, ↓miR-668, ↓miR-744, ↓miR-758, ↓miR-873, ↓miR-885-5p, and ↓miR-1197, miR-30c, ↓miR-149, ↓miR-195, miR-324-5p and ↓miR-331 | miR-345, miR-483-3p, and miR-486-5p. miR-17-92 | (correlates with increased event-free survival and favorable disease outcome). ↑miR-184 (increases overall survival). ↑miR-204 (associated with a favourable clinical outcome and increases sensitivity to chemotherapy). | ↓miR-195, ↓miR-324-5p ↓and miR-331 |
5.1.2. MB Subgroups Have Distinct miRNA Profiles
5.2. Supratentorial Primitive Neuroectodermal Tumors
miRNAs Aberrantly Expressed in sPNET
5.3. Atypical Teratoid/Rhabdoid Tumors (AT/RT)
miRNAs Aberrantly Expressed in AT/RT
5.4. Neuroblastoma
MicroRNAs Aberrantly Expressed in NB
miRNAs associated withsignaling pathways involved in MB classification/pathogenesis | miRNAs associated with MB and neuronal stem cell biology | miRNAs associated with metastasis in MB | miRNAs associated with risk stratification/outcome prediction | ||
---|---|---|---|---|---|
↓miR-125b, ↓miR-326, and ↓miR-324–5p, ↑miR-214 and ↓miR-92 (associates with SHH) [27] | miR-17/92 (promotes neural stem cells development, modulating its cell-fate decision and are also involved in cancer stem cells and in MBs biology) [204] | miR-21, miR-182 (promotes metastasis)miR-182 contributes to leptomeningeal metastatic dissemination in non-SHH-MB [166] | Tumor suppressor miR-31 and miR-153 (down-regulated in clinical high risk MB patients) [91,107] | ||
↑miR-183~96~182 (associates with genetic amplification of MYC in the most clinically aggressive MB subgroup) [119,166] | miR-199b-5p (negatively regulates MB tumor stem-cell positive to CD133 antigen) [109] | miR-193a, miR-224/miR-452 cluster,, and miR-148a (potential metastasis suppressive activity) [160] | Oncogene miR-183~96~182 (highly expressed in the most clinically aggressive MB subgroup) [119] | ||
↑miR-17-92 (correlates with SHH as well as c-MYC/MYCN activation in MB) [162] | miR-125b, miR-324-5p, and miR-326 (regulate SHH signaling in cerebellar granule neuron precursors and MB cells) [27] | miR-199-5p (confreres inhibition of MB metastasis) [109] | Tumor suppressor miR-9 (downregulation is a predictive marker for poor prognosis in MB) [111] | ||
miR-10b, ↑miR-135a, miR-135b, ↑miR-125b and ↓miR-153 (associated with ErbB2 overexpressing MB tumors) [91,107] | miR-7, miR-9, and ↓miR-124 (associated with MB and Neuronal Differentiation) [103,104,111] | Tumor suppressor miR-199-5p (low expression is a predictor for a poor-risk MB class) [109] | |||
↓miR-181b, miR-128a, and ↓miR-128b (associated with c-MYC overexpressing MBs) [91,107] | miR324-5p and miR326 (promote progressive events in MBs) [27] | ||||
↓miR-199b and ↓miR-326 miR34a (associated with Notch Signaling pathway) [109] | Tumor suppressor miR-128b miR-181b low expression (correlates with MB disease risk) [91,107] | ||||
↑miR-193a, ↑miR-224/↑miR-23b, ↑miR-365 and ↑miR-148a (over-expressed in the WNT signaling associated MB) [120,160] | |||||
↑miR-let7g, ↑miR-19a, ↑miR-106b and ↑miR-191distinguish MB differing in histotypes (anaplastic, classic and desmoplastic [107] |
6. Role of miRNAs as Biomarkers
7. Risk Stratification and Outcome Prediction
7.1. Prediction of Clinical Outcome in MB
7.2. Prediction of Clinical Outcome in NB
8. Pros and Cons of the miRNAs as Biomarkers for Embryonal Neural Tumors
9. miRNAs as Potential Cancer Therapeutics
microRNAs | Theraputic Potential | Models Investigated | Reference |
---|---|---|---|
* miR124 | The adverse prognostic markers in MB (CDK6 SLC16A1D) are regulated by miR-124 Overexpression of the tumor suppressor miR124 decreases MB cell growth in vitro and in xenograft tumors in mice suggesting possible use of miR-124 restoration in MB therapy | D283, D341, D384, D425, D458, ONS-76 MB cell lines. D425 xenograft tumors in mice. | [88,113] |
* miR199b-5p | miR199b-5p target Notch effector HES1, which is involved in MB pathogenesis. miR199b-5p overexpression impairs the clonogenic potential of MB cell lines. Moreover MB tumor infection by adenovirus carrying miR199b-5p in a xenograft model reduces the tumor burden in vivo suggesting possible use of miR199b-5p as an adjuvant therapy | Daoy cell line and Daoy xanograft mouse model. | [109] |
* miR34a | miR-34a is a regulator of the Notch ligand Dll1. Down-regulation of Dll1 expression by miR-34a negatively regulates cell proliferation, and induces apoptosis and neural differentiation in MB cells. In addition infection of adenoviruses carrying the precursor miR-34a induces neurogenesis, reduces tumor burden, and confers chemosensitivity in mice xenografts, | Daoy cell line and Daoy xanograft mouse model. | [236] |
* miR125b, miR324-5p, miR326 | miR125b, miR324-5p, miR326 suppress Hedgehog signaling which controls cerebellar granule cell progenitor (GCP) development as well as neoplastic transformation into MB. Overexpression of these miRNA increases GCP differentiation and inhibits MB cell proliferation, and colonies formation. | Daoy and D283 cell lines. | [27] |
* miR128a | By targeting the Bmi-1 oncogene, miR-128a inhibits growth of MB cells and alters the intracellular redox state of the tumor cells and thereby promotes cellular senescence in MB cells. | Daoy, ONS-76 cell lines. | [118] |
* miR383 | Tumor suppressor miR-383 is down-regulated in MB. Overexpression of miR383 inhibits MB cell growth through targeting PRDX3 | Daoy, D283, D341, D384, D425, D458, ONS-76 cell lines. | [237] |
* miR9, miR125a | miR-9 and miR-125a are tumor suppressors that are downregulated in MB patient with poor survival. Rescued expression miR-9 and miR-125a promotes MB cell growth arrest and apoptosis by targeting truncated TrkC isoform or notch signal via His1. | D283 and Daoy cell lines. D341, D425 | [107,111] |
* miR218 | miR-218 is significantly underexpressed in MB. miR-218 target multiple cancer associated genes such as REST, CDK6, RICTOR and CTSB in MB cells. Re-expression of miR-218 resultes in a decrease in MB cell growth, colony formation, cell migration, invasion, and tumor sphere size. | Daoy, D283, D341, D425, D458 and UW228 cell lines. | [238] |
** miR-17-92 | Activation of miR-17-92 cluster is known as a marker for poor prognosis and poor survival of NB. miR-17-92 affect multiple cancer pathways including DKK3, CDKN1A, BIM, ER-α, MEF2D Its activation increases proliferation, decreases apoptosis and inhibits TGF-β signaling. Aggressive NB evade the cytostatic TGFβ-pathway through miR-17-92 directed targeting of the pathway. Reactivation of TGFβ-signaling through miR-17-92 inhibition could be a promising therapeutic approach for NB | SHEP NB cell line xanograft mouse model. | [131] |
** miR-21 | Oncogenic miR-21 promotes the proliferation and decreased sensitivity to chemotherapy of human NB cells. Ectopic expression of pre-miR-21 lower the level of tumor suppressor PTEN mRNA and protein and in NB cells. Transfection of anti-miR-21 increases the PTEN expression. However, others reported that inhibition of miR-21 did not affect proliferation of NB cells, suggesting that the precise biological functions of miR-21 in NB still warrant further studies. | SH-SY5Y and BE(2)-M17 NB cell lines | [129] |
** miR-380-5p | miR-380 which is highly expressed in NB repress p53-mediated apoptosis, and is associated with poor outcome in NB with MYCN amplification. miR-380 overexpression cooperates with activated HRAS oncoprotein and form tumors in mice. Inhibition of miR-380-5p in embryonic stem or NB cells results in induction of p53, and apoptotic cell death. In vivo delivery of a miR-380-5p antagonist decreases tumor size in NB orthotopic mouse model suggesting a promising potential therapeutic ability to miR-380 inhibitors | TH-MYCN transgenic mice of NB Orthotopic NB model | [132] |
** miR-15a | miR-15a promotes the migration of NB cells through targeting the RECK-MMP-9 axis. Suppression of miR-15a decreases the migration and invasion whereas overexpression increases the migration ability of NB cell lines. These findings provide insights into the role of miR-15 in NB migration and invasion and qualify miR-15a as a potential therapeutic target. | GI-LA-N and SK-N-SH cell lines | [133] |
** miR-34a | Tumor suppressive miR-34 family members targets MYCN and inhibit the growth of NB cell lines In addition, other genes also targeted by miR-34a, including E2F3, BCL2, CCND1 and CDK4 were found to be involved in cell proliferation or apoptosis Over expression of miR-34a in NB cell lines induces cell cycle arrest decreases cell number and induces apoptosis. miR-34a significantly reduces tumor growth in an in vivo orthotopic murine model. | Kelly, SK-N-AS cell lines NB1691luc NB cell lines NB xanograft mouse model | [135] |
9.1. miRNA Antagonists
9.2. miRNA Replacement Therapy
9.3. Challenges of miRNA-based Therapies
10. Concluding Remarks
Acknowledgements
Author Contributions
Conflicts of Interest
References
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Shalaby, T.; Fiaschetti, G.; Baumgartner, M.; Grotzer, M.A. Significance and Therapeutic Value of miRNAs in Embryonal Neural Tumors. Molecules 2014, 19, 5821-5862. https://doi.org/10.3390/molecules19055821
Shalaby T, Fiaschetti G, Baumgartner M, Grotzer MA. Significance and Therapeutic Value of miRNAs in Embryonal Neural Tumors. Molecules. 2014; 19(5):5821-5862. https://doi.org/10.3390/molecules19055821
Chicago/Turabian StyleShalaby, Tarek, Giulio Fiaschetti, Martin Baumgartner, and Michael A. Grotzer. 2014. "Significance and Therapeutic Value of miRNAs in Embryonal Neural Tumors" Molecules 19, no. 5: 5821-5862. https://doi.org/10.3390/molecules19055821