Exosomal MiRNAs in Pediatric Cancers
Abstract
:1. Introduction
2. MiRNAs: Biogenesis and Functions
3. Exosomal MiRNAs: Biogenesis, Sorting, and Function
4. Role of Exosomal MiRNAs in Cancer
5. Exosomal MiRNAs in Pediatric Cancers
5.1. Neuroblastoma
5.2. Hepatoblastoma
5.3. Osteosarcoma
5.4. Ewing’s Sarcoma
5.5. Rhabdomyosarcoma
5.6. NRSTS (Non-Rhabdomyosarcoma Soft Tissue Sarcoma)
5.7. Brain Tumors
5.8. Leukemias
5.9. Lymphomas
6. Conclusions
Funding
Acknowledgments
Conflicts of Interest
Abbreviations
mRNA | Messenger RNA |
RISC | RNA-induced silencing complex |
ESCRT | Endosomal sorting complex required for transport |
TSG101 | Tumor-susceptibility gene 101 |
ALIX | ALG-2 interacting protein X |
MVB | Microvesicular bodies |
SMase | Sphingomyelinase |
hnRNP | Heterogeneous nuclear ribonucleoproteins |
miRISC | miRNA-induced silencing complex |
AGO2 | Argonaute protein 2 |
CRC | Colon rectal cancer |
HUVEC | Human umbilical vascular endothelial cells |
TMZ | Temozolomide |
GBM | Glioblastoma |
XRCC4 | X-ray repair cross-completing 4 |
ER | Estrogen receptor |
M | Macrophage |
MAPK | Mitogen-activated protein kinase |
STAT | Signal transducer and activator of transcription |
RFXAP | Regulatory factor X-associated protein |
MHC class II | Major histocompatibility complex class II |
NB | Neuroblastoma |
AHR | Aryl hydrocarbon receptor |
IL | Interleukin |
TERF1 | Telomeric repeat binding factor-1 |
NK | Natural killer |
AURKA | Aurora Kinase A |
TGF | Transforming growth factor |
HC | Healthy control |
NEDD4 | Neural precursor cell-expressed developmentally downregulated gene 4 |
HB | Hepatoblastoma |
FAP | Familial adenomatous polyposis |
OS | Osteosarcoma |
CALN1 | Calneuron-1 |
NGS | Next generation sequencing |
EV | Extracellular vesicle |
GO | Gene ontology |
CAF | Cancer-associated fibroblast |
SCAI | Suppressor of cancer cell invasion |
EWS | Ewing’s sarcoma |
CD | Cluster of differentiation |
NF-kB | Nuclear factor kappa-light-chain-enhancer of activated B cells |
RMS | Rhabdomyosarcoma |
ARMS | Alveolar rhabdomyosarcoma |
ERMS | Embryonal rhabdomyosarcoma |
PAX | Paired box |
FOXO1 | Forkhead box protein O1 |
NRSTS | Non-rhabdomyosarcoma soft tissue sarcoma |
SS | Synovial sarcoma |
TKI | Tyrosine kinase inhibitor |
TRIP6 | Thyroid hormone receptor interactor 6 |
LMNA | Lamin A |
SIRT3 | Sirtuin 3 |
MSC | Mesenchymal stromal cell |
DSRCT | Desmoplastic small round cell tumor |
CNS | Central nervous system |
pHGG | Pediatric high-grade glioma |
DIPG | Diffuse intrinsic pontine glioma |
GSCs | Pediatric glioma stem cells |
NSCs | Neuronal stem cells |
PTEN | Phosphatase and tensin homolog |
TET3 | Tet methylcytosine dioxygenase 3 |
SERTAD1 | Serta domain-containing protein 1 |
ATRT | Atypical teratoid/rhabdoid tumor |
ALL | Acute lymphocytic leukemia |
AML | Acute myeloid leukemia |
BM | Bone marrow |
NGS | Nod scid gamma |
WHO | World Health Organization |
HL | Hodgkin lymphoma |
NHL | Non-Hodgkin lymphoma |
BL | Burkitt lymphoma |
DLBCL | Diffuse large B-cell lymphoma |
PMLBCL | Primary mediastinal large B-cell lymphoma |
ALCL | Anaplastic large cell lymphoma |
LL | Lymphoblastic lymphoma |
References
- Ilié, M.; Hofman, P. Pros: Can tissue biopsy be replaced by liquid biopsy? Transl. Lung Cancer Res. 2016, 5, 420–423. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Atay, S.; Godwin, A.K. Tumor-derived exosomes: A message delivery system for tumor progression. Commun. Integr. Biol. 2014, 7, e28231. [Google Scholar] [CrossRef] [PubMed]
- Lakkaraju, A.; Rodriguez-Boulan, E. Itinerant exosomes: Emerging roles in cell and tissue polarity. Trends Cell Biol. 2008, 18, 199–209. [Google Scholar] [CrossRef] [PubMed]
- Taylor, D.D.; Lyons, K.S.; Gerçel-Taylor, C. Shed membrane fragment-associated markers for endometrial and ovarian cancers. Gynecol. Oncol. 2002, 84, 443–448. [Google Scholar] [CrossRef] [PubMed]
- Taylor, D.D.; Zacharias, W.; Gercel-Taylor, C. Exosome isolation for proteomic analyses and RNA profiling. Methods Mol. Biol. 2011, 728, 235–246. [Google Scholar]
- Colletti, M.; Petretto, A.; Galardi, A.; Di Paolo, V.; Tomao, L.; Lavarello, C.; Inglese, E.; Bruschi, M.; Lopez, A.A.; Pascucci, L.; et al. Proteomic Analysis of Neuroblastoma-Derived Exosomes: New Insights into a Metastatic Signature. Proteomics 2017, 17, 23–24. [Google Scholar] [CrossRef]
- Taylor, D.D.; Gercel-Taylor, C. MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol. Oncol. 2008, 110, 13–21. [Google Scholar] [CrossRef]
- Villarroya-Beltri, C.; Gutiérrez-Vázquez, C.; Sánchez-Cabo, F.; Pérez-Hernández, D.; Vázquez, J.; Martin-Cofreces, N.; Martinez-Herrera, D.J.; Pascual-Montano, A.; Mittelbrunn, M.; Sánchez-Madrid, F. Sumoylated hnRNPA2B1 controls the sorting of miRNAs into exosomes through binding to specific motifs. Nat. Commun. 2013, 4, 2980. [Google Scholar] [CrossRef] [Green Version]
- Macfarlane, L.A.; Murphy, P.R. MicroRNA: Biogenesis, Function and Role in Cancer. Curr. Genom. 2010, 11, 537–561. [Google Scholar] [CrossRef] [Green Version]
- Kloosterman, W.P.; Plasterk, R.H. The diverse functions of microRNAs in animal development and disease. Dev. Cell. 2006, 11, 441–450. [Google Scholar] [CrossRef]
- Gangaraju, V.K.; Lin, H. MicroRNAs: Key regulators of stem cells. Nat. Rev. Mol. Cell. Biol. 2009, 10, 116–125. [Google Scholar] [CrossRef] [PubMed]
- Bushati, N.; Cohen, S.M. MicroRNA functions. Annu. Rev. Cell. Dev. Biol. 2007, 23, 175–205. [Google Scholar] [CrossRef] [PubMed]
- Dwivedi, Y. Evidence demonstrating role of microRNAs in the etiopathology of major depression. J. Chem. Neuroanat. 2011, 42, 142–156. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wollert, T.; Hurley, J.H. Molecular mechanism of multivesicular body biogenesis by ESCRT complexes. Nature 2010, 46, 4864–4869. [Google Scholar]
- Bebelman, M.P.; Smit, M.J.; Pegtel, D.M.; Baglio, S.R. Biogenesis and function of extracellular vesicles in cancer. Pharm. Ther. 2018, 188, 1–11. [Google Scholar] [CrossRef] [PubMed]
- Matsumura, T.; Sugimachi, K.; Iinuma, H.; Takahashi, Y.; Kurashige, J.; Sawada, G.; Ueda, M.; Uchi, R.; Ueo, H.; Takano, Y.; et al. Exosomal microRNA in serum is a novel biomarker of recurrence in human colorectal cancer. Br. J. Cancer 2015, 113, 275–281. [Google Scholar] [CrossRef] [PubMed]
- Van Giau, V.; An, S.S. Emergence of exosomal miRNAs as a diagnostic biomarker for Alzheimer’s disease. J. Neurol. Sci. 2016, 360, 141–152. [Google Scholar] [CrossRef] [PubMed]
- Guduric-Fuchs, J.; O’Connor, A.; Camp, B.; O’Neill, C.L.; Medina, R.J.; Simpson, D.A. Selective extracellular vesicle-mediated export of an overlapping set of microRNAs from multiple cell types. BMC Genom. 2012, 13, 357. [Google Scholar] [CrossRef]
- Squadrito, M.L.; Baer, C.; Burdet, F.; Maderna, C.; Gilfillan, G.D.; Lyle, R.; Ibberson, M.; De Palma, M. Endogenous RNAs modulate microRNA sorting to exosomes and transfer to acceptor cells. Cell Rep. 2014, 8, 1432–1446. [Google Scholar] [CrossRef]
- Kosaka, N.; Iguchi, H.; Hagiwara, K.; Yoshioka, Y.; Takeshita, F.; Ochiya, T. Neutral sphingomyelinase 2 (nSMase2)-dependent exosomal transfer of angiogenic microRNAs regulate cancer cell metastasis. J. Biol. Chem. 2013, 288, 10849–10859. [Google Scholar] [CrossRef]
- Koppers-Lalic, D.; Hackenberg, M.; Bijnsdorp, I.V.; van Eijndhoven, M.A.J.; Sadek, P.; Sie, D.; Zini, N.; Middeldorp, J.M.; Ylstra, B.; de Menezes, R.X.; et al. Nontemplated nucleotide additions distinguish the small RNA composition in cells from exosomes. Cell Rep. 2014, 8, 1649–1658. [Google Scholar] [CrossRef] [PubMed]
- Ghayad, S.E.; Rammal, G.; Ghamloush, F.; Basma, H.; Nasr, R.; Diab-Assaf, M.; Chelala, C.; Saab, R. Exosomes derived from embryonal and alveolar rhabdomyosarcoma carry differential miRNA cargo and promote invasion of recipient fibroblasts. Sci. Rep. 2016, 6, 37088. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Umezu, T.; Ohyashiki, K.; Kuroda, M.; Ohyashiki, J.H. Leukemia cell to endothelial cell communication via exosomal miRNAs. Oncogene 2013, 32, 2747–2755. [Google Scholar] [CrossRef] [PubMed]
- Yamada, N.; Tsujimura, N.; Kumazaki, M.; Shinohara, H.; Taniguchi, K.; Nakagawa, Y.; Naoe, T.; Akao, Y. Colorectal cancer cell-derived microvesicles containing microRNA-1246 promote angiogenesis by activating Smad 1/5/8 signaling elicited by PML down-regulation in endothelial cells. Biochim. Biophys. Acta 2014, 1839, 1256–1272. [Google Scholar] [CrossRef] [PubMed]
- Fong, M.Y.; Zhou, W.; Liu, L.; Alontaga, A.Y.; Chandra, M.; Ashby, J.; Chow, A.; O’Connor, S.T.; Li, S.; Chin, A.R.; et al. Breast-cancer-secreted miR-122 reprograms glucose metabolism in premetastatic niche to promote metastasis. Nat. Cell Biol. 2015, 17, 183–194. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Corcoran, C.; Rani, S.; O’Driscoll, L. miR-34a is an intracellular and exosomal predictive biomarker for response to docetaxel with clinical relevance to prostate cancer progression. Prostate 2014, 74, 1320–1334. [Google Scholar] [CrossRef] [PubMed]
- Zeng, A.; Wei, Z.; Yan, W.; Yin, J.; Huang, X.; Zhou, X.; Li, R.; Shen, F.; Wu, W.; Wang, X.; et al. Exosomal transfer of miR-151a enhances chemosensitivity to temozolomide in drug-resistant glioblastoma. Cancer Lett. 2018, 436, 10–21. [Google Scholar] [CrossRef] [PubMed]
- Wei, Y.; Lai, X.; Yu, S.; Chen, S.; Ma, Y.; Zhang, Y.; Li, H.; Zhu, X.; Yao, L.; Zhang, J. Exosomal miR-221/222 enhances tamoxifen resistance in recipient ER-positive breast cancer cells. Breast Cancer Res. Treat. 2014, 147, 423–431. [Google Scholar] [CrossRef] [PubMed]
- Trivedi, M.; Talekar, M.; Shah, P.; Ouyang, Q.; Amiji, M. Modification of tumor cell exosome content by transfection with wt-p53 and microRNA-125b expressing plasmid DNA and its effect on macrophage polarization. Oncogenesis 2016, 5, e250. [Google Scholar] [CrossRef]
- Ying, X.; Wu, Q.; Wu, X.; Zhu, Q.; Wang, X.; Jiang, L.; Chen, X.; Wang, X. Epithelial ovarian cancer-secreted exosomal miR-222-3p induces polarization of tumor-associated macrophages. Oncotarget 2016, 7, 43076–43087. [Google Scholar] [CrossRef]
- Ye, S.B.; Li, Z.L.; Luo, D.H.; Huang, B.J.; Chen, Y.S.; Zhang, X.S.; Cui, J.; Zeng, Y.X.; Li, J. Tumor-derived exosomes promote tumor progression and T-cell dysfunction through the regulation of enriched exosomal microRNAs in human nasopharyngeal carcinoma. Oncotarget 2014, 5, 5439–5452. [Google Scholar] [CrossRef] [PubMed]
- Ding, G.; Zhou, L.; Qian, Y.; Fu, M.; Chen, J.; Chen, J.; Xiang, J.; Wu, Z.; Jiang, G.; Cao, L. Pancreatic cancer-derived exosomes transfer miRNAs to dendritic cells and inhibit RFXAP expression via miR-212-3p. Oncotarget 2015, 6, 29877–29888. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bhome, R.; Goh, R.W.; Bullock, M.D.; Pillar, N.; Thirdborough, S.M.; Mellone, M.; Mirnezami, R.; Galea, D.; Veselkov, K.; Gu, Q.; et al. Exosomal microRNAs derived from colorectal cancer-associated fibroblasts: Role in driving cancer progression. Aging (Albany N. Y.) 2017, 9, 2666–2694. [Google Scholar] [CrossRef] [PubMed]
- Hashimoto, K.; Ochi, H.; Sunamura, S.; Kosaka, N.; Mabuchi, Y.; Fukuda, T.; Yao, K.; Kanda, H.; Ae, K.; Okawa, A.; et al. Cancer-secreted hsa-miR-940 induces an osteoblastic phenotype in the bone metastatic microenvironment via targeting ARHGAP1 and FAM134A. Proc. Natl. Acad. Sci. USA 2018, 115, 2204–2209. [Google Scholar] [CrossRef] [Green Version]
- Haug, B.H.; Hald, Ø.H.; Utnes, P.; Roth, S.A.; Løkke, C.; Flægstad, T.; Einvik, C. Exosome-like Extracellular Vesicles from MYCN-amplified Neuroblastoma Cells Contain Oncogenic miRNAs. Anticancer Res. 2015, 35, 2521–2530. [Google Scholar] [PubMed]
- Feng, S.; Cao, Z.; Wang, X. Role of aryl hydrocarbon receptor in cancer. Biochim. Biophys. Acta 2013, 1836, 197–210. [Google Scholar] [CrossRef] [PubMed]
- Wu, P.Y.; Liao, Y.F.; Juan, H.F.; Huang, H.C.; Wang, B.J.; Lu, Y.L.; Yu, I.S.; Shih, Y.Y.; Jeng, Y.M.; Hsu, W.M.; et al. Aryl hydrocarbon receptor downregulates MYCN expression and promotes cell differentiation of neuroblastoma. PLoS ONE 2014, 9, e88795. [Google Scholar] [CrossRef] [PubMed]
- Challagundla, K.B.; Wise, P.M.; Neviani, P.; Chava, H.; Murtadha, M.; Xu, T.; Kennedy, R.; Ivan, C.; Zhang, X.; Vannini, I.; et al. Exosome-mediated transfer of microRNAs within the tumor microenvironment and neuroblastoma resistance to chemotherapy. J. Natl. Cancer Inst. 2015, 13, 107. [Google Scholar] [CrossRef] [PubMed]
- Deville, L.; Hillion, J.; Pendino, F.; Samy, M.; Nguyen, E.; Ségal-Bendirdjian, E. hTERT promotes imatinib resistance in chronic myeloid leukemia cells: Therapeutic implications. Mol. Cancer Ther. 2011, 10, 711–719. [Google Scholar] [CrossRef]
- Guo, X.L.; Ma, N.N.; Zhou, F.G.; Zhang, L.; Bu, X.X.; Sun, K.; Song, J.R.; Li, R.; Zhang, B.H.; Wu, M.C.; et al. Up-regulation of hTERT expression by low-dose cisplatin cisplatin contributes to chemotherapy resistance in human hepatocellular cancer cells. Oncol. Rep. 2009, 22, 549–556. [Google Scholar]
- Smith, V.; Dai, F.; Spitz, M.; Peters, G.J.; Fiebig, H.H.; Hussain, A.; Burger, A.M. Telomerase activity and telomere length in human tumor cells with acquired resistance to anticancer agents. J. Chemother. 2009, 21, 542–549. [Google Scholar] [CrossRef] [PubMed]
- Neviani, P.; Wise, P.M.; Murtadha, M.; Liu, C.W.; Wu, C.H.; Jong, A.Y.; Seeger, R.C.; Fabbri, M. Natural Killer-Derived Exosomal miR-186 Inhibits Neuroblastoma Growth and Immune Escape Mechanisms. Cancer Res. 2019, 79, 1151–1164. [Google Scholar] [CrossRef] [PubMed]
- Ma, J.; Xu, M.; Yin, M.; Hong, J.; Chen, H.; Gao, Y.; Xie, C.; Shen, N.; Gu, S.; Mo, X. Exosomal hsa-miR199a-3p Promotes Proliferation and Migration in Neuroblastoma. Front. Oncol. 2019, 9, 459. [Google Scholar] [CrossRef] [PubMed]
- Schnater, J.M.; Köhler, S.E.; Lamers, W.H.; von Schweinitz, D.; Aronson, D.C. Where do we stand with hepatoblastoma? A review. Cancer 2003, 98, 668–678. [Google Scholar] [CrossRef] [PubMed]
- Vishnoi, J.R.; Sasidhar, A.; Misra, S.; Pareek, P.; Khera, S.; Kumar, S.; Jain, A. Hepatoblastoma in a Young Adult: A Rare Case Report and Review of the Literature. J. Gastrointest. Cancer 2019, 1–6. [Google Scholar] [CrossRef] [PubMed]
- Hamada, Y.; Takada, K.; Fukunaga, S.; Hioki, K. Hepatoblastoma associated with Beckwith-Wiedemann syndrome and hemihypertrophy. Pediatr. Surg. Int. 2003, 19, 112–114. [Google Scholar] [PubMed]
- Jiao, C.; Jiao, X.; Zhu, A.; Ge, J.; Xu, X. Exosomal miR-34s panel as potential novel diagnostic and prognostic biomarker in patients with hepatoblastoma. J. Pediatr. Surg. 2017, 52, 618–624. [Google Scholar] [CrossRef] [PubMed]
- Bommer, G.T.; Gerin, I.; Feng, Y.; Kaczorowski, A.J.; Kuick, R.; Love, R.E.; Zhai, Y.; Giordano, T.J.; Qin, Z.S.; Moore, B.B.; et al. p53-mediated activation of miRNA34 candidate tumor-suppressor genes. Curr. Biol. 2007, 17, 1298–1307. [Google Scholar] [CrossRef] [PubMed]
- Vogt, M.; Munding, J.; Grüner, M.; Liffers, S.T.; Verdoodt, B.; Hauk, J.; Steinstraesser, L.; Tannapfel, A.; Hermeking, H. Frequent concomitant inactivation of miR-34a and miR-34b/c by CpG methylation in colorectal, pancreatic, mammary, ovarian, urothelial, and renal cell carcinomas and soft tissue sarcomas. Virchows Arch. 2011, 458, 313–322. [Google Scholar] [CrossRef]
- Liu, W.; Chen, S.; Liu, B. Diagnostic and prognostic values of serum exosomal microRNA-21 in children with hepatoblastoma: A Chinese population-based study. Pediatr. Surg. Int. 2016, 32, 1059–1065. [Google Scholar] [CrossRef]
- Jo, V.Y.; Fletcher, C.D.M. WHO classification of soft tissue tumours: an update based on the 2013 (4th) edition. Pathology 2014, 46, 95–104. [Google Scholar] [CrossRef] [PubMed]
- Ritter, J.; Bielack, S.S. Osteosarcoma. Ann. Oncol. 2010, 21, 320–325. [Google Scholar] [CrossRef] [PubMed]
- Kansara, M.; Teng, M.W.; Smyth, M.J.; Thomas, D.M. Translational biology of osteosarcoma. Nat. Rev. Cancer 2014, 14, 722–735. [Google Scholar] [CrossRef] [PubMed]
- Bhattasali, O.; Vo, A.T.; Roth, M.; Geller, D.; Randall, R.L.; Gorlick, R.; Gill, J. Variability in the reported management of pulmonary metastases in osteosarcoma. Cancer Med. 2015, 4, 523–531. [Google Scholar] [CrossRef] [PubMed]
- Bernthal, N.M.; Federman, N.; Eilber, F.R.; Nelson, S.D.; Eckardt, J.J.; Eilber, F.C.; Tap, W.D. Long-term results (>25 years) of a randomized, prospective clinical trial evaluating chemotherapy in patients with high-grade, operable osteosarcoma. Cancer 2012, 118, 5888–5893. [Google Scholar] [CrossRef]
- Gong, L.; Bao, Q.; Hu, C.; Wang, J.; Zhou, Q.; Wei, L.; Tong, L.; Zhang, W.; Shen, Y. Exosomal miR-675 from metastatic osteosarcoma promotes cell migration and invasion by targeting CALN1. Biochem. Biophys. Res. Commun. 2018, 500, 170–176. [Google Scholar] [CrossRef] [PubMed]
- Zheng, Y.; Lu, X.; Xu, L.; Chen, Z.; Li, Q.; Yuan, J. MicroRNA-675 promotes glioma cell proliferation and motility by negatively regulating retinoblastoma 1. Hum. Pathol. 2017, 69, 63–71. [Google Scholar] [CrossRef] [PubMed]
- Costa, V.; Lo Dico, A.; Rizzo, A.; Rajata, F.; Tripodi, M.; Alessandro, R.; Conigliaro, A. MiR-675-5p supports hypoxia induced epithelial to mesenchymal transition in colon cancer cells. Oncotarget 2017, 8, 24292–24302. [Google Scholar] [CrossRef]
- Li, H.; Yu, B.; Li, J.; Su, L.; Yan, M.; Zhu, Z.; Liu, B. Overexpression of lncRNA H19 enhances carcinogenesis and metastasis of gastric cancer. Oncotarget 2014, 5, 2318–2329. [Google Scholar] [CrossRef] [Green Version]
- Jerez, S.; Araya, H.; Hevia, D.; Irarrázaval, C.E.; Thaler, R.; van Wijnen, A.J.; Galindo, M. Extracellular vesicles from osteosarcoma cell lines contain miRNAs associated with cell adhesion and apoptosis. Gene 2019, 710, 246–257. [Google Scholar] [CrossRef]
- He, H.; Ni, J.; Huang, J. Molecular mechanisms of chemoresistance in osteosarcoma. Oncol. Lett. 2014, 7, 1352–1362. [Google Scholar] [CrossRef] [PubMed]
- Xu, J.F.; Wang, Y.P.; Zhang, S.J.; Chen, Y.; Gu, H.F.; Dou, X.F.; Xia, B.; Bi, Q.; Fan, S.W. Exosomes containing differential expression of microRNA and mRNA in osteosarcoma that can predict response to chemotherapy. Oncotarget 2017, 8, 75968–75978. [Google Scholar] [CrossRef] [PubMed]
- Labernadie, A.; Kato, T.; Brugues, A.; Serra-Picamal, X.; Derzsi, S.; Arwert, E.; Weston, A.; Gonzalez- Tarrago, V.; Elosegui-Artola, A.; Albertazzi, L.; et al. A mechanically active heterotypic E-cadherin/N-cadherin adhesion enables fibroblasts to drive cancer cell invasion. Nat. Cell Biol. 2017, 19, 224–237. [Google Scholar] [CrossRef] [PubMed]
- Garcia-Silva, S.; Peinado, H. Melanosomes foster a tumour niche by activating CAFs. Nat. Cell Biol. 2016, 18, 911–913. [Google Scholar] [CrossRef] [PubMed]
- Lin, L.; Liu, D.; Liang, H.; Xue, L.; Su, C.; Liu, M. MiR-1228 promotes breast cancer cell growth and metastasis through targeting SCAI protein. Int. J. Clin. Exp. Pathol. 2015, 8, 6646–6655. [Google Scholar]
- Zhang, Y.; Dai, J.; Deng, H.; Wan, H.; Liu, M.; Wang, J.; Li, S.; Li, X.; Tang, H. miR-1228 promotes the proliferation and metastasis of hepatoma cells through a p53 forward feedback loop. Br. J. Cancer 2015, 112, 365–374. [Google Scholar] [CrossRef]
- Wang, J.W.; Wu, X.F.; Gu, X.J.; Jiang, X.H. Exosomal miR-1228 from cancer-associated fibroblasts promotes cell migration and invasion of osteosarcoma by directly targeting SCAI. Oncol. Res. Featur. Preclin. Clin. Cancer Ther. 2019. [Google Scholar] [CrossRef]
- Fujiwara, T.; Uotani, K.; Yoshida, A.; Morita, T.; Nezu, Y.; Kobayashi, E.; Yoshida, A.; Uehara, T.; Omori, T.; Sugiu, K.; et al. Clinical significance of circulating miR-25-3p as a novel diagnostic and prognostic biomarker in osteosarcoma. Oncotarget 2017, 8, 33375–33392. [Google Scholar] [CrossRef]
- Wang, X.H.; Cai, P.; Wang, M.H.; Wang, Z. microRNA-25 promotes osteosarcoma cell proliferation by targeting the cell-cycle inhibitor p27. Mol. Med. Rep. 2014, 10, 855–859. [Google Scholar] [CrossRef]
- Xu, X.; Chen, Z.; Zhao, X.; Wang, J.; Ding, D.; Wang, Z.; Tan, F.; Tan, X.; Zhou, F.; Sun, J.; et al. MicroRNA-25 promotes cell migration and invasion in esophageal squamous cell carcinoma. Biochem. Biophys. Res. Commu. 2012, 421, 640–645. [Google Scholar] [CrossRef]
- Li, Q.; Zou, C.; Zou, C.; Han, Z.; Xiao, H.; Wei, H.; Wang, W.; Zhang, L.; Zhang, X.; Tang, Q. MicroRNA-25 functions as a potential tumor suppressor in colon cancer by targeting Smad7. Cancer Lett. 2013, 335, 168–174. [Google Scholar] [CrossRef]
- Raimondi, L.; De Luca, A.; Gallo, A.; Costa, V.; Russelli, G.; Cuscino, N.; Manno, M.; Raccosta, S.; Carina, V.; Bellavia, D.; et al. Osteosarcoma cell-derived exosomes affect tumor microenvironment by specific packaging of microRNAs. Carcinogenesis 2019. [Google Scholar] [CrossRef]
- Lawlor, E.R.; Sorensen, P.H. Twenty Years on: What Do We Really Know about Ewing Sarcoma and What Is the Path Forward? Crit. Rev. Oncog. 2015, 20, 155–171. [Google Scholar] [CrossRef] [Green Version]
- Ventura, S.; Aryee, D.N.; Felicetti, F.; De Feo, A.; Mancarella, C.; Manara, M.C.; Picci, P.; Colombo, M.P.; Kovar, H.; Carè, A.; et al. CD99 regulates neural differentiation of Ewing sarcoma cells through miR-34a-Notch-mediated control of NF-κB signaling. Oncogene 2016, 35, 3944–3954. [Google Scholar] [CrossRef]
- De Feo, A.; Sciandra, M.; Ferracin, M.; Felicetti, F.; Astolfi, A.; Pignochino, Y.; Picci, P.; Carè, A.; Scotlandi, K. Exosomes from CD99-deprived Ewing sarcoma cells reverse tumor malignancy by inhibiting cell migration and promoting neural differentiation. Cell Death Dis. 2019, 10, 471. [Google Scholar] [CrossRef]
- Ries, L.A.G.; Smith, M.A.; Gurney, J.G.; Linet, M.; Tamra, T.; Young, J.L.; Bunin, G.R. Cancer Incidence and Survival among Children and Adolescents; National Cancer Institute: Bethesda, MD, USA, 1999; pp. 111–123. [Google Scholar]
- Gurney, J.G.; Young, J.L.; Roffers, S.D.; Smith, M.A.; Bunin, G.R. SEER Pediatric Monograph. Natl. Cancer Inst. 2005. [Google Scholar]
- Skapek, S.X.; Ferrari, A.; Gupta, A.A.; Lupo, P.J.; Butler, E.; Shipley, J.; Barr, F.G.; Hawkins, D.S. Rhabdomyosarcoma. Nat. Rev. Dis. Primers 2019, 5, 1. [Google Scholar] [CrossRef]
- Mercado, G.E.; Barr, F.G. Fusions involving PAX and FOX genes in the molecular pathogenesis of alveolar rhabdomyosarcoma: Recent advances. Curr. Mol. Med. 2007, 7, 47–61. [Google Scholar] [CrossRef]
- Sorensen, P.H.; Lynch, J.C.; Qualman, S.J.; Tirabosco, R.; Lim, J.F.; Maurer, H.M.; Bridge, J.A.; Crist, W.M.; Triche, T.J.; Barr, F.G. PAX3-FKHR and PAX7-FKHR gene fusions are prognostic indicators in alveolar rhabdomyosarcoma: A report from the children’s oncology group. J. Clin. Oncol. 2002, 20, 2672–2679. [Google Scholar] [CrossRef]
- Kalluri, R.; Zeisberg, M. Fibroblasts in cancer. Nat. Rev. Cancer 2006, 6, 392–401. [Google Scholar] [CrossRef]
- Doyle, L.A. Sarcoma classification: An update based on the 2013 World Health Organization Classification of Tumors of Soft Tissue and Bone. Cancer 2014, 120, 1763–1774. [Google Scholar] [CrossRef]
- Goldblum, J.R.; Weiss, S.W.; Folpe, A.L. Enzinger and Weiss’s Soft Tissue Tumors E-Book; Elsevier Inc.: Amsterdam, The Netherlands, 2013; pp. 1052–1070. [Google Scholar]
- Kawai, A.; Woodruff, J.; Healey, J.H.; Brennan, M.F.; Antonescu, C.R.; Ladanyi, M. SYT-SSX gene fusion as a determinant of morphology and prognosis in synovial sarcoma. N. Engl. J. Med. 1998, 338, 153–160. [Google Scholar] [CrossRef]
- Hosaka, S.; Horiuchi, K.; Yoda, M.; Nakayama, R.; Tohmonda, T.; Susa, M.; Nakamura, M.; Chiba, K.; Toyama, Y.; Morioka, H. A novel multi-kinase inhibitor pazopanib suppresses growth of synovial sarcoma cells through inhibition of the PI3K-AKT pathway. J. Orthop. Res. 2012, 30, 1493–1498. [Google Scholar] [CrossRef]
- Rajendra, R.; Jones, R.L.; Pollack, S.M. Targeted treatment for advanced soft tissue sarcoma: Profile of pazopanib. Onco. Targets Ther. 2013, 6, 217–222. [Google Scholar]
- Shiozawa, K.; Shuting, J.; Yoshioka, Y.; Ochiya, T.; Kondo, T. Extracellular vesicle-encapsulated microRNA-761 enhances pazopanib resistance in synovial sarcoma. Biochem. Biophys. Res. Commun. 2018, 495, 1322–1327. [Google Scholar] [CrossRef]
- Nass, D.; Rosenwald, S.; Meiri, E.; Gilad, S.; Tabibian-Keissar, H.; Schlosberg, A.; Kuker, H.; Sion-Vardy, N.; Tobar, A.; Kharenko, O.; et al. MiR-92b and miR-9/9* are specifically expressed in brain primary tumors and can be used to differentiate primary from metastatic brain tumors. Brain Pathol. 2009, 19, 375–383. [Google Scholar] [CrossRef]
- Nowakowski, T.J.; Fotaki, V.; Pollock, A.; Sun, T.; Pratt, T.; Price, D.J. MicroRNA-92b regulates the development of intermediate cortical progenitors in embryonic mouse brain. Proc. Natl. Acad. Sci. USA 2013, 110, 7056–7061. [Google Scholar] [CrossRef] [Green Version]
- Uotani, K.; Fujiwara, T.; Yoshida, A.; Iwata, S.; Morita, T.; Kiyono, M.; Yokoo, S.; Kunisada, T.; Takeda, K.; Hasei, J.; et al. Circulating MicroRNA-92b-3p as a Novel Biomarker for Monitoring of Synovial Sarcoma. Sci. Rep. 2017, 7, 14634. [Google Scholar] [CrossRef]
- Thway, K.; Noujaim, J.; Zaidi, S.; Miah, A.B.; Benson, C.; Messiou, C.; Jones, R.L.; Fisher, C. Desmoplastic Small Round Cell Tumor: Pathology, Genetics, and Potential Therapeutic Strategies. Int. J. Surg. Pathol. 2016, 24, 672–684. [Google Scholar] [CrossRef]
- Colletti, M.; Paolini, A.; Galardi, A.; Paolo, V.D.; Pascucci, L.; Russo, I.; Angelis, B.; Peinado, H.; Vito, R.; Milano, G.M.; et al. Expression profiles of exosomal miRNAs isolated from plasma of patients with desmoplastic small round cell tumor. Epigenomics 2019, 11, 489–500. [Google Scholar] [CrossRef]
- Jones, C.; Karajannis, M.A.; Jones, D.T.; Kieran, M.W.; Monje, M.; Baker, S.J.; Becher, O.J.; Cho, Y.J.; Gupta, N.; Hawkins, C.; et al. Pediatric high-grade glioma: Biologically and clinically in need of new thinking. Neuro. Oncol. 2017, 19, 153–161. [Google Scholar] [CrossRef]
- Tűzesi, Á.; Kling, T.; Wenger, A.; Lunavat, T.R.; Jang, S.C.; Rydenhag, B.; Lötvall, J.; Pollard, S.M.; Danielsson, A.; Carén, H. Pediatric brain tumor cells release exosomes with a miRNA repertoire that differs from exosomes secreted by normal cells. Oncotarget 2017, 8, 90164–90175. [Google Scholar] [CrossRef]
- Yang, Y.P.; Nguyen, P.N.N.; Ma, H.I.; Ho, W.J.; Chen, Y.W.; Chien, Y.; Yarmishyn, A.A.; Huang, P.I.; Lo, W.L.; Wang, C.Y.; et al. Tumor Mesenchymal Stromal Cells Regulate Cell Migration of Atypical Teratoid Rhabdoid Tumor through Exosome-Mediated miR155/SMARCA4 Pathway. Cancers (Basel) 2019, 11, 720. [Google Scholar] [CrossRef]
- De Carvalho, I.N.; de Freitas, R.M.; Vargas, F.R. Translating microRNAs into biomarkers: What is new for pediatric cancer? Med. Oncol. 2016, 33, 49. [Google Scholar] [CrossRef]
- de Oliveira, J.C.; Molinari, R.G.; Baroni, M.; Salomão, K.B.; Pezuk, J.A.; Brassesco, M.S. MiRNA dysregulation in childhood hematological cancer. Int. J. Mol. Sci. 2018, 19, 2688. [Google Scholar] [CrossRef]
- Gulino, R.; Forte, S.; Parenti, R.; Memeo, L.; Gulisano, M. MicroRNA and pediatric tumors: Future perspectives. Acta. Histochem. 2015, 117, 339–354. [Google Scholar] [CrossRef]
- Metayer, C.; Milne, E.; Clavel, J.; Infante-Rivard, C.; Petridou, E.; Taylor, M.; Schüz, J.; Spector, L.G.; Dockerty, J.D.; Magnani, C.; et al. The Childhood Leukemia International Consortium. Cancer Epidemiol. 2013, 37, 336–347. [Google Scholar] [CrossRef] [Green Version]
- Amitay, E.L.; Keinan-Boker, L. Breastfeeding and Childhood Leukemia Incidence: A Meta-analysis and Systematic Review. JAMA Pediatr. 2015, 169, e151025. [Google Scholar] [CrossRef]
- Madhusoodhan, P.P.; Carroll, W.L.; Bhatla, T. Progress and Prospects in Pediatric Leukemia. Curr. Probl. Pediatr. Adolesc. Health Care 2016, 46, 229–241. [Google Scholar] [CrossRef]
- Seth, R.; Singh, A. Leukemias in Children. Indian J. Pediatr. 2015, 82, 817–824. [Google Scholar] [CrossRef]
- Fayyad-Kazan, H.; Bitar, N.; Najar, M.; Lewalle, P.; Fayyad-Kazan, M.; Badran, R.; Hamade, E.; Daher, A.; Hussein, N.; ElDirani, R.; et al. Circulating miR-150 and miR-342 in plasma are novel potential biomarkers for acute myeloid leukemia. J. Transl. Med. 2013, 7, 11–31. [Google Scholar] [CrossRef]
- Yan, W.; Xu, L.; Sun, Z.; Lin, Y.; Zhang, W.; Chen, J.; Hu, S.; Shen, B. MicroRNA biomarker identification for pediatric acute myeloid leukemia based on a novel bioinformatics model. Oncotarget 2015, 6, 26424–26436. [Google Scholar] [CrossRef] [Green Version]
- Swellam, M.; El-Khazragy, N. Clinical impact of circulating microRNAs as blood-based marker in childhood acute lymphoblastic leukemia. Tumour Biol. 2016, 37, 10571–10576. [Google Scholar] [CrossRef]
- Chen, B.; Luan, C.; Yang, Z. The functional role of microRNA in acute lymphoblastic leukemia: Relevance for diagnosis, differential diagnosis, prognosis, and therapy. Onco. Targets Ther. 2015, 8, 2903–2914. [Google Scholar] [CrossRef]
- Shafik, R.E.; Abd El Wahab, N.; Senoun, S.A.; El Taweel, M.A.; Ebeid, E. Expression of micro-RNA 128 and let-7b in pediatric acute lymphoblastic leukemia cases. Asian Pac. J. Cancer Prev. 2018, 19, 2263–2267. [Google Scholar]
- De Oliveira, J.C.; Scrideli, C.A.; Brassesco, M.S.; Morales, A.G.; Pezuk, J.A.; Queiroz Rde, P.; Yunes, J.A.; Brandalise, S.R.; Tone, L.G. Differential MiRNA expression in childhood acute lymphoblastic leukemia and association with clinical and biological features. Leuk. Res. 2012, 36, 293–298. [Google Scholar] [CrossRef]
- De Oliveira, J.C.; Brassesco, M.S.; Scrideli, C.A.; Tone, L.G.; Narendran, A. MicroRNA expression and activity in pediatric acute lymphoblastic leukemia (ALL). Pediatr. Blood Cancer 2012, 59, 599–604. [Google Scholar] [CrossRef]
- Schotte, D.; Chau, J.C.; Sylvester, G.; Liu, G.; Chen, C.; van der Velden, V.H.; Broekhuis, M.J.; Peters, T.C.; Pieters, R.; den Boer, M.L. Identification of new microRNA genes and aberrant microRNA profiles in childhood acute lymphoblastic leukemia. Leukemia 2009, 23, 313–322. [Google Scholar] [CrossRef]
- Zhang, H.; Luo, X.Q.; Zhang, P.; Huang, L.B.; Zheng, Y.S.; Wu, J.; Zhou, H.; Qu, L.H.; Xu, L.; Chen, Y.Q. MicroRNA patterns associated with clinical prognostic parameters and CNS relapse prediction in pediatric acute leukemia. PLoS ONE 2009, 4, e7826. [Google Scholar] [CrossRef]
- Garzon, R.; Heaphy, C.E.; Havelange, V.; Fabbri, M.; Volinia, S.; Tsao, T.; Zanesi, N.; Kornblau, S.M.; Marcucci, G.; Calin, G.A.; et al. MicroRNA 29b functions in acute myeloid leukemia. Blood 2009, 114, 5331–5341. [Google Scholar] [CrossRef] [Green Version]
- Marcucci, G.; Mrózek, K.; Radmacher, M.D.; Garzon, R.; Bloomfield, C.D. The prognostic and functional role of microRNAs in acute myeloid leukemia. Blood 2011, 117, 1121–1129. [Google Scholar] [CrossRef] [Green Version]
- Mott, J.L.; Kobayashi, S.; Bronk, S.F.; Gores, G.J. mir-29 regulates Mcl-1 protein expression and apoptosis. Oncogene 2007, 26, 6133–6140. [Google Scholar] [CrossRef] [Green Version]
- Johnnidis, J.B.; Harris, M.H.; Wheeler, R.T.; Stehling-Sun, S.; Lam, M.H.; Kirak, O.; Brummelkamp, T.R.; Fleming, M.D.; Camargo, F.D. Regulation of progenitor cell proliferation and granulocyte function by microRNA-223. Nature 2008, 451, 1125–1129. [Google Scholar] [CrossRef]
- Georgantas, R.W., 3rd; Hildreth, R.; Morisot, S.; Alder, J.; Liu, C.G.; Heimfeld, S.; Calin, G.A.; Croce, C.M.; Civin, C.I. CD34+ hematopoietic stem-progenitor cell microRNA expression and function: A circuit diagram of differentiation control. Proc. Natl. Acad. Sci. USA 2007, 104, 2750–2755. [Google Scholar] [CrossRef]
- O’Connell, R.M.; Rao, D.S.; Chaudhuri, A.A.; Boldin, M.P.; Taganov, K.D.; Nicoll, J.; Paquette, R.L.; Baltimore, D. Sustained expression of microRNA-155 in hematopoietic stem cells causes a myeloproliferative disorder. J. Exp. Med. 2008, 205, 585–594. [Google Scholar] [CrossRef]
- Lim, E.L.; Trinh, D.L.; Ries, R.E.; Wang, J.; Gerbing, R.B.; Ma, Y.; Topham, J.; Hughes, M.; Pleasance, E.; Mungall, A.J.; et al. MicroRNA Expression-Based Model Indicates Event-Free Survival in Pediatric Acute Myeloid Leukemia. J. Clin. Oncol. 2017, 35, 3964–3977. [Google Scholar] [CrossRef] [Green Version]
- Marcucci, G.; Maharry, K.; Radmacher, M.D.; Mrózek, K.; Vukosavljevic, T.; Paschka, P.; Whitman, S.P.; Langer, C.; Baldus, C.D.; Liu, C.G.; et al. Prognostic significance of, and gene and MicroRNA expression signatures associated with, CEBPA mutations in cytogenetically normal acute myeloid leukemia with high-risk molecular features: A cancer and leukemia group B study. J. Clin. Oncol. 2008, 26, 5078–5087. [Google Scholar] [CrossRef]
- Marcucci, G.; Radmacher, M.D.; Maharry, K.; Mrózek, K.; Ruppert, A.S.; Paschka, P.; Vukosavljevic, T.; Whitman, S.P.; Baldus, C.D.; Langer, C.; et al. MicroRNA expression in cytogenetically normal acute myeloid leukemia. N. Engl. J. Med. 2008, 358, 1919–1928. [Google Scholar] [CrossRef]
- Lin, X.; Wang, Z.; Wang, Y.; Feng, W. Serum MicroRNA-370 as a potential diagnostic and prognostic biomarker for pediatric acute myeloid leukemia. Int. J. Clin. Exp. Pathol. 2015, 8, 14658–14666. [Google Scholar]
- Peinado, H.; Alečković, M.; Lavotshkin, S.; Matei, I.; Costa-Silva, B.; Moreno-Bueno, G.; Hergueta-Redondo, M.; Williams, C.; García-Santos, G.; Ghajar, C.; et al. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat. Med. 2012, 18, 883–891. [Google Scholar] [CrossRef] [Green Version]
- Corcoran, C.; Rani, S.; O’Brien, K.; O’Neill, A.; Prencipe, M.; Sheikh, R.; Webb, G.; McDermott, R.; Watson, W.; Crown, J.; et al. Docetaxel-resistance in prostate cancer: Evaluating associated phenotypic changes and potential for resistance transfer via exosomes. PLoS ONE 2012, 7, e50999. [Google Scholar] [CrossRef] [PubMed]
- Hong, C.S.; Muller, L.; Boyiadzis, M.; Whiteside, T.L. Isolation and characterization of CD34+ blast-derived exosomes in acute myeloid leukemia. PLoS ONE 2014, 9, e103310. [Google Scholar] [CrossRef] [PubMed]
- Choi, D.; Lee, T.H.; Spinelli, C.; Chennakrishnaiah, S.; D’Asti, E.; Rak, J. Extracellular vesicle communication pathways as regulatory targets of oncogenic transformation. Semin. Cell Dev. Biol. 2017, 67, 11–22. [Google Scholar] [CrossRef] [PubMed]
- Kumar, B.; Garcia, M.; Murakami, J.L.; Chen, C.-C. Exosome-mediated microenvironment dysregulation in leukemia. Biochim. Biophys. Acta 2016, 1863, 464–470. [Google Scholar] [CrossRef] [PubMed]
- Liu, Y.; Cheng, Z.; Pang, Y.; Cui, L.; Qian, T.; Quan, L.; Zhao, H.; Shi, J.; Ke, X.; Fu, L. Role of microRNAs, circRNAs and long noncoding RNAs in acute myeloid leukemia. J. Hematol. Oncol. 2019, 12, 51. [Google Scholar] [CrossRef] [PubMed]
- Chowdhury, R.; Webber, J.P.; Gurney, M.; Mason, M.D.; Tabi, Z.; Clayton, A. Cancer exosomes trigger mesenchymal stem cell differentiation into pro-angiogenic and pro-invasive myofibroblasts. Oncotarget 2015, 6, 715–731. [Google Scholar] [CrossRef] [PubMed]
- Ohyashiki, J.H.; Umezu, T.; Ohyashiki, K. Exosomes promote bone marrow angiogenesis in hematologic neoplasia: The role of hypoxia. Curr. Opin. Hematol. 2016, 23, 268–273. [Google Scholar] [CrossRef] [PubMed]
- Huan, J.; Hornick, N.I.; Skinner, A.M.; Goloviznina, N.A.; Roberts, C.T.; Kurre, P. RNA trafficking by acute myeloid leukemia exosomes. Cancer Res. 2013, 73, 918–929. [Google Scholar] [CrossRef]
- Chen, Y.; Jacamo, R.; Konopleva, M.; Garzon, R.; Croce, C.; Andreeff, M. CXCR4 downregulation of let-7a drives chemoresistance in acute myeloid leukemia. J. Clin. Invest. 2013, 123, 2395–2407. [Google Scholar] [CrossRef] [Green Version]
- Farahani, M.; Rubbi, C.; Liu, L.; Slupsky, J.R.; Kalakonda, N. CLL Exosomes Modulate the Transcriptome and Behaviour of Recipient Stromal Cells and Are Selectively Enriched in miR-202-3p. PLoS ONE 2015, 10, e0141429. [Google Scholar] [CrossRef]
- Yeh, Y.Y.; Ozer, H.G.; Lehman, A.M.; Maddocks, K.; Yu, L.; Johnson, A.J.; Byrd, J.C. Characterization of CLL exosomes reveals a distinct microRNA signature and enhanced secretion by activation of BCR signaling. Blood 2015, 125, 3297–3305. [Google Scholar] [CrossRef]
- Paggetti, J.; Haderk, F.; Seiffert, M.; Janji, B.; Distler, U.; Ammerlaan, W.; Kim, Y.J.; Adam, J.; Lichter, P.; Solary, E.; et al. Exosomes released by chronic lymphocytic leukemia cells induce the transition of stromal cells into cancer-associated fibroblasts. Blood 2015, 126, 1106–1117. [Google Scholar] [CrossRef] [Green Version]
- Trino, S.; Lamorte, D.; Caivano, A.; Laurenzana, I.; Tagliaferri, D.; Falco, G.; Del Vecchio, L.; Musto, P.; De Luca, L. Micrornas as new biomarkers for diagnosis and prognosis, and as potential therapeutic targets in acute myeloid leukemia. Int. J. Mol. Sci. 2018, 19, 460. [Google Scholar] [CrossRef]
- Hornick, N.I.; Huan, J.; Doron, B.; Goloviznina, N.A.; Lapidus, J.; Chang, B.H.; Kurre, P. Serum Exosome MicroRNA as a Minimally-Invasive Early Biomarker of AML. Sci. Rep. 2015, 5, 11295. [Google Scholar] [CrossRef]
- Allen, C.E.; Kelly, K.M.; Bollard, C.M. Pediatric lymphomas and histiocytic disorders of childhood. Pediatr. Clin. North Am. 2015, 62, 139–165. [Google Scholar] [CrossRef]
- Swerdlow, S.H.; Campo, E.; Pileri, S.A.; Harris, N.L.; Stein, H.; Siebert, R.; Advani, R.; Ghielmini, M.; Salles, G.A.; Zelenetz, A.D.; et al. The 2016 revision of the World Health Organization classification of lymphoid neoplasms. Blood 2016, 127, 2375–2390. [Google Scholar] [CrossRef] [Green Version]
- Jiang, M.; Bennani, N.N.; Feldman, A.L. Lymphoma classification update: T-cell lymphomas, Hodgkin lymphomas, and histiocytic/dendritic cell neoplasms. Expert Rev. Hematol. 2017, 10, 239–249. [Google Scholar] [CrossRef] [Green Version]
- Burkhardt, B.; Zimmermann, M.; Oschlies, I.; Niggli, F.; Mann, G.; Parwaresch, R.; Riehm, H.; Schrappe, M.; Reiter, A.; BFM Group. The impact of age and gender on biology, clinical features and treatment outcome of non-Hodgkin lymphoma in childhood and adolescence. Br. J. Haematol. 2005, 131, 39–49. [Google Scholar] [CrossRef]
- Sandlund, J.T. Non-Hodgkin Lymphoma in Children. Curr. Hematol. Malig. Rep. 2015, 10, 237–243. [Google Scholar] [CrossRef]
- Metzler, M.; Wilda, M.; Busch, K.; Viehmann, S.; Borkhardt, A. High expression of precursor microRNA-155/BIC RNA in children with Burkitt lymphoma. Genes Chromosomes Cancer 2004, 39, 167–169. [Google Scholar] [CrossRef]
- Kluiver, J.; Haralambieva, E.; de Jong, D.; Blokzijl, T.; Jacobs, S.; Kroesen, B.J.; Poppema, S.; van den Berg, A. Lack of BIC and microRNA miR-155 expression in primary cases of Burkitt lymphoma. Genes Chromosomes Cancer 2006, 45, 147–153. [Google Scholar] [CrossRef] [PubMed]
- Chabay, P.A.; Preciado, M.V. EBV primary infection in childhood and its relation to B-cell lymphoma development: A mini-review from a developing region. Int. J. Cancer 2013, 133, 1286–1292. [Google Scholar] [CrossRef] [PubMed]
- Yoon, C.; Kim, J.; Park, G.; Kim, S.; Kim, D.; Hur, D.Y.; Kim, B.; Kim, Y.S. Delivery of miR-155 to retinal pigment epithelial cells mediated by Burkitt’s lymphoma exosomes. Tumour Biol. 2016, 37, 313–321. [Google Scholar] [CrossRef] [PubMed]
- Di Lisio, L.; Sánchez-Beato, M.; Gómez-López, G.; Rodríguez, M.E.; Montes-Moreno, S.; Mollejo, M.; Menárguez, J.; Martínez, M.A.; Alves, F.J.; Pisano, D.G.; et al. MicroRNA signatures in B-cell lymphomas. Blood Cancer J. 2012, 2, e57. [Google Scholar] [CrossRef] [PubMed]
- Lenze, D.; Leoncini, L.; Hummel, M.; Volinia, S.; Liu, C.G.; Amato, T.; De Falco, G.; Githanga, J.; Horn, H.; Nyagol, J.; et al. The different epidemiologic subtypes of Burkitt lymphoma share a homogenous micro RNA profile distinct from diffuse large B-cell lymphoma. Leukemia 2011, 25, 1869–1876. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mangani, D.; Roberti, A.; Rizzolio, F.; Giordano, A. Emerging molecular networks in Burkitt’s lymphoma. J. Cell Biochem. 2013, 114, 35–38. [Google Scholar] [CrossRef] [PubMed]
- Zhuang, H.; Shen, J.; Zheng, Z.; Luo, X.; Gao, R.; Zhuang, X. MicroRNA-146a rs2910164 polymorphism and the risk of diffuse large B cell lymphoma in the Chinese Han population. Med. Oncol. 2014, 31, 306. [Google Scholar] [CrossRef] [PubMed]
- Zare, N.; Eskandari, N.; Mehrzad, V.; Javanmard, S.H. The expression level of hsa-miR-146a-5p in plasma-derived exosomes of patients with diffuse large B-cell lymphoma. J. Res. Med. Sci. 2019, 24, 10. [Google Scholar]
- Khare, D.; Goldschmidt, N.; Bardugo, A.; Gur-Wahnon, D.; Ben-Dov, I.Z.; Avni, B. Plasma microRNA profiling: Exploring better biomarkers for lymphoma surveillance. PLoS ONE 2017, 12, e0187722. [Google Scholar] [CrossRef]
- Feng, Y.; Zhong, M.; Zeng, S.; Wang, L.; Liu, P.; Xiao, X.; Liu, Y. Exosome-derived miRNAs as predictive biomarkers for diffuse large B-cell lymphoma chemotherapy resistance. Epigenomics 2019, 11, 35–51. [Google Scholar] [CrossRef]
Pediatric Tumor | Site of Exosomes | miRNA | Upregulated/ Downregulated | Function | References |
---|---|---|---|---|---|
Neuroblastoma | |||||
SK-N-BE(2)C and Kelly cells | Culture Media | miR-92a-3p, miR-23a-3p, miR-218-5p, miR-320a, miR-24-3p, miR-27b-3p, miR-16-5p, miR-25-3p, miR-21-5p- miR-125b-5p, an miR-320b | Upregulated | Aryl hydrocarbon receptor (AHR) signaling pathway, survival, apoptosis, differentiation, angiogenesis, and invasion | [35] |
SK-N-BE(2)C, CHLA-255, and IMR-32 | Culture media | miR-21 | Upregulated | Pro-inflammatory effect through the activation of the NF-kb and TLR8 pathways | [38] |
Plasma | miR-199a-3p | Upregulated | Increased proliferation and migration | [43] | |
Hepatoblastoma | |||||
Serum | miR-34a, miR-34b, and miR-34c | Downregulated | Tumor promotion | [47] | |
Plasma | miR-21 | Upregulated | [50] | ||
Osteosarcoma | |||||
MG63, MG63.2, HOS, and 143B cells | Culture Media Plasma | miR-675 | Upregulated | Migration, proliferation, and survival | [56] |
SAOS2; MG63; HOS; 143B; U2OS, and hFOB1.19 cells | Culture media | miR143-3p, miR21-5p, miR181a-5p, and miR148-5p | Upregulated | Apoptosis, cell adhesion, and migration | [60] |
Serum | miR-135b, miR-148a, miR-27a, and miR-9 | Upregulated | [62] | ||
miR-124, miR-133a, miR 199a-3p, and miR-385 | Downregulated | ||||
U2OS, HOS, 143B, and SAOS2 cells | Culture media | miR-25-3p | Upregulated | Promotes capillary formation | [68] |
SAOS-2, MG-63, and U-2 OS cells | Culture media | hsa-let-7f-5p, hsa-miR-16-5p, hsa-miR-21-5p, hsa-miR-192-5p, hsa-miR-148a-3p, hsa-miR-182-5p, hsa-miR-128-3p, hsa-miR-126-5p, hsa-miR-186-5p, hsa-miR-301a-3p, and hsa-miR-151a-3p | Upregulated | [72] | |
hsa-let-7b-5p, hsa-let-7d-3p, hsa-let-7e-5p, hsa-miR-23a-5p, hsa-miR-214-3p, hsa-miR-125a-5p, hsa-miR-331-3p, hsa-miR-193b-3p, hsa-miR-941, and hsa-miR-1908-5p | Downregulated | ||||
Ewing Sarcoma (EWS) | |||||
EWS cells | Culture media | miR-34a | Upregulated | Downregulates NF-k B signaling | [74] |
CD99neg-EWS cells | Culture media | miR-199-3p | Upregulated | Suppression of tumor growth, migration, and invasion | [75] |
Rhabdomyosarcoma | |||||
RH30, RH41, RD, JR1, and RH36 cells | Culture Media | miR-1246 miR-1268 | Tumorigenesis, angiogenesis, and apoptosis | [22] | |
Synovial Sarcoma | |||||
SYO-1, HS-SYII, 1273/99, and YaFuSS cells | Culture Media | miR-761 | Upregulated | Positively correlated with treatment resistance | [87] |
SYO-1, HS-SY-II, and YaFuSS cells | Culture Media Serum | miR-92b-3p | Upregulated | [90] | |
Desmoplastic small round cell tumor (DSRCT) | |||||
Plasma | miR-34-5p miR-22-3p miR-324-3p | Upregulated | Cell growth, proliferation, migration, and invasion | [92] | |
miR-342-3p miR-150-5p | Downregulated | ||||
Brain tumors | |||||
GSCS cells | Culture Media | miR-1290 miR-1246 | Upregulated | Stemness and cancer progression | [94] |
© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Galardi, A.; Colletti, M.; Di Paolo, V.; Vitullo, P.; Antonetti, L.; Russo, I.; Di Giannatale, A. Exosomal MiRNAs in Pediatric Cancers. Int. J. Mol. Sci. 2019, 20, 4600. https://doi.org/10.3390/ijms20184600
Galardi A, Colletti M, Di Paolo V, Vitullo P, Antonetti L, Russo I, Di Giannatale A. Exosomal MiRNAs in Pediatric Cancers. International Journal of Molecular Sciences. 2019; 20(18):4600. https://doi.org/10.3390/ijms20184600
Chicago/Turabian StyleGalardi, Angela, Marta Colletti, Virginia Di Paolo, Patrizia Vitullo, Loretta Antonetti, Ida Russo, and Angela Di Giannatale. 2019. "Exosomal MiRNAs in Pediatric Cancers" International Journal of Molecular Sciences 20, no. 18: 4600. https://doi.org/10.3390/ijms20184600
APA StyleGalardi, A., Colletti, M., Di Paolo, V., Vitullo, P., Antonetti, L., Russo, I., & Di Giannatale, A. (2019). Exosomal MiRNAs in Pediatric Cancers. International Journal of Molecular Sciences, 20(18), 4600. https://doi.org/10.3390/ijms20184600