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Review | Open Access

Modulating microRNAs in cancer: next-generation therapies

Nahid Arghiani1,2, Khalid Shah1,2,3 ( )
Center for Stem Cell and Translational Immunotherapy (CSTI), Harvard Medical School, Boston, MA 02115, USA
Department of Neurosurgery, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02115, USA
Harvard Stem Cell Institute, Harvard University, Cambridge, MA 02138, USA
Show Author Information

Abstract

MicroRNAs (miRNAs) are a class of endogenously expressed non-coding regulators of the genome with an ability to mediate a variety of biological and pathological processes. There is growing evidence demonstrating frequent dysregulation of microRNAs in cancer cells, which is associated with tumor initiation, development, migration, invasion, resisting cell death, and drug resistance. Studies have shown that modulation of these small RNAs is a novel and promising therapeutic tool in the treatment of a variety of diseases, especially cancer, due to their broad influence on multiple cellular processes. However, suboptimal delivery of the appropriate miRNA to the cancer sites, quick degradation by nucleases in the blood circulation, and off target effects have limited their research and clinical applications. Therefore, there is a pressing need to improve the therapeutic efficacy of miRNA modulators, while at the same time reducing their toxicities. Several delivery vehicles for miRNA modulators have been shown to be effective in vitro and in vivo. In this review, we will discuss the role and importance of miRNAs in cancer and provide perspectives on currently available carriers for miRNA modulation. We will also summarize the challenges and prospects for the clinical translation of miRNA-based therapeutic strategies.

Keywords

delivery systemscancer therapyMiRNAsclinical translationdysregulation

References

1

Anglicheau D, Muthukumar T, Suthanthiran M. MicroRNAs: small RNAs with big effects. Transplantation. 2010; 90: 105-12.
Crossref Google Scholar
2

Martinez VD, Cohn DE, Telkar N, Minatel BC, Pewarchuk ME, Marshall EA, et al. Profiling the small non-coding RNA transcriptome of the human placenta. Sci Data. 2021; 8: 166.
Crossref Google Scholar
3

Peng Y, Croce CM. The role of microRNAs in human cancer. Signal Transduct Target Ther. 2016; 1: 15004.
Crossref Google Scholar
4
Sharad S, Kapur S. Therapeutic implication of miRNA in human disease. In: Walayat A, Yang M, Xiao D, editors. Antisense Therapy. London: IntechOpen; 2018. p. 82738.
5

Hata A, Lieberman J. Dysregulation of microRNA biogenesis and gene silencing in cancer. Sci Signal. 2015; 8: re3.
Crossref Google Scholar
6

Iorio MV, Croce CM. Causes and consequences of microRNA dysregulation. Cancer J. 2012; 18: 215-22.
Crossref Google Scholar
7

Zeinali T, Mansoori B, Mohammadi A, Baradaran B. Regulatory mechanisms of miR-145 expression and the importance of its function in cancer metastasis. Biomed Pharmacother. 2019; 109: 195-207.
Crossref Google Scholar
8

Wang B, Hsu SH, Wang X, Kutay H, Bid HK, Yu J, et al. Reciprocal regulation of microRNA-122 and c-Myc in hepatocellular cancer: role of E2F1 and transcription factor dimerization partner 2. Hepatology. 2014; 59: 555-66.
Crossref Google Scholar
9

Misiewicz-Krzeminska I, Krzeminski P, Corchete LA, Quwainder D, Rojas EA, Herreero AB, et al. Factors regulating microRNA expression and function in multiple myeloma. Noncoding RNA. 2019; 5: 9.
Crossref Google Scholar
10

Xiao J, Lin H, Luo X, Luo X, Wang Z. MiR-605 joins p53 network to form a p53:miR-605:Mdm2 positive feedback loop in response to stress. EMBO J. 2011; 30: 5021.
Crossref Google Scholar
11

Hermeking H. The miR-34 family in cancer and apoptosis. Cell Death Differ. 2010; 17: 193-9.
Crossref Google Scholar
12

Ma J, Gong W, Liu S, Li Q, Guo M, Wang J, et al. Ibrutinib targets microRNA-21 in multiple myeloma cells by inhibiting NF-κB and STAT3. Tumour Biol. 2018; 40: 1010428317731369.
Crossref Google Scholar
13

Kent OA, Chivukula RR, Mullendore M, Wentzel EA, Feldmann G, Lee KL, et al. Repression of the miR-143/145 cluster by oncogenic Ras initiates a tumor-promoting feed-forward pathway. Genes Dev. 2010; 24: 2754-9.
Crossref Google Scholar
14

Bracken CP, Gregory PA, Kolesnikoff N, Bert AG, Wang J, Shannon MF, et al. A double-negative feedback loop between ZEB1-SIP1 and the microRNA-200 family regulates epithelial-mesenchymal transition. Cancer Res. 2008; 68: 7846-54.
Crossref Google Scholar
15

Jiang RL, Li Y. Regulation of miRNA pathway and roles of microRNAs in tumorigenesis and metastasis. Human Genet Embryol S. 2013; 2: 2161-436.
Crossref Google Scholar
16

Kim J, Yao F, Xiao Z, Sun Y, Ma L. MicroRNAs and metastasis: small RNAs play big roles. Cancer Metastasis Rev. 2018; 37: 5-15.
Crossref Google Scholar
17

Yoshida K, Yamamoto Y, Ochiya T. MiRNA signaling networks in cancer stem cells. Regen Ther. 2021; 17: 1-7.
Crossref Google Scholar
18

Diepenbruck M, Tiede S, Saxena M, Ivanek R, Kalathur RKR, Lüönd F, et al. MiR-1199-5p and Zeb1 function in a double-negative feedback loop potentially coordinating EMT and tumour metastasis. Nat Commun. 2017; 8: 1168.
Crossref Google Scholar
19

Zhu X, Pan H, Liu L. Long noncoding RNA network: Novel insight into hepatocellular carcinoma metastasis (Review). Int J Mol Med. 2021; 48: 1-12.
Crossref Google Scholar
20

Arghiani N, Matin MM. MiR-21: A key small molecule with great effects in combination cancer therapy. Nucleic Acid Ther. 2021; 31: 271-83.
Crossref Google Scholar
21

Cai Z, Zhang F, Chen W, Zhang J, Li H. MiRNAs: A promising target in the chemoresistance of bladder cancer. Onco Targets Ther. 2019; 12: 11805-16.
Crossref Google Scholar
22

An X, Sarmiento C, Tan T, Zhu H. Regulation of multidrug resistance by microRNAs in anti-cancer therapy. Acta Pharm Sin B. 2017; 7: 38-51.
Crossref Google Scholar
23

Jamialahmadi K, Zahedipour F, Karimi G. The role of microRNAs on doxorubicin drug resistance in breast cancer. J Pharm Pharmacol. 2021; 73: 997-1006.
Crossref Google Scholar
24

Tian Y, Tang L, Yi P, Pan Q, Han Y, Shi Y, et al. MiRNAs in radiotherapy resistance of nasopharyngeal carcinoma. J Cancer. 2020; 11: 3976-85.
Crossref Google Scholar
25

Li D, Tolleson WH, Yu D, Chen S, Guo L, Xiao W, et al. Regulation of cytochrome P450 expression by microRNAs and long noncoding RNAs: Epigenetic mechanisms in environmental toxicology and carcinogenesis. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev. 2019; 37: 180-214.
Crossref Google Scholar
26

Lan H, Lu H, Wang X, Jin H. MicroRNAs as potential biomarkers in cancer: opportunities and challenges. Biomed Res Int. 2015; 2015: 125094.
Crossref Google Scholar
27

Arneth B. Tumor microenvironment. Medicina. 2019; 56: 15.
Crossref Google Scholar
28

Caner A, Asik E, Ozpolat B. SRC signaling in cancer and tumor microenvironment. Adv Exp Med Biol. 2021; 1270: 57-71.
Crossref Google Scholar
29

Antomarchi J, Ambrosetti D, Cohen C, Delotte J, Chevallier A, Karimdjee-Soilihi B, et al. Immunosuppressive tumor microenvironment status and histological grading of endometrial carcinoma. Cancer Microenviron. 2019; 12: 169-79.
Crossref Google Scholar
30

Avraham R, Yarden Y. Regulation of signalling by microRNAs. Biochem Soc Trans. 2012; 40: 26-30.
Crossref Google Scholar
31

Eichelmann AK, Matuszcak C, Hummel R, Haier J. Role of miRNAs in cell signaling of cancer associated fibroblasts. Int J Biochem Cell Biol. 2018; 101: 94-102.
Crossref Google Scholar
32

Boguslawska J, Kryst P, Poletajew S, Piekielko-Witkowska A. TGF-β and microRNA Interplay in genitourinary cancers. Cells. 2019; 8: 1619.
Crossref Google Scholar
33

Wang R, Sun Y, Yu W, Yan Y, Qiao M, Jiang R, et al. Downregulation of miRNA-214 in cancer-associated fibroblasts contributes to migration and invasion of gastric cancer cells through targeting FGF9 and inducing EMT. J Exp Clin Cancer Res. 2019; 38: 20.
Crossref Google Scholar
34

Musumeci M, Coppola V, Addario A, Patrizii M, Maugeri-Sacca M, Memeo L, et al. Control of tumor and microenvironment cross-talk by miR-15a and miR-16 in prostate cancer. Oncogene. 2011; 30: 4231-42.
Crossref Google Scholar
35

Loh HY, Norman BP, Lai KS, Rahman NM, Alitheen NB, Osman MA. The regulatory role of microRNAs in breast cancer. Int J Mol Sci. 2019; 20: 4940.
Crossref Google Scholar
36

Lou W, Liu J, Gao Y, Zhong G, Chen D, Shen J, et al. MicroRNAs in cancer metastasis and angiogenesis. Oncotarget. 2017; 8: 115787-802.
Crossref Google Scholar
37

Wang H, Li K, Mei Y, Huang X, Li Z, Yang Q, et al. Sp1 suppresses miR-3178 to promote the metastasis invasion cascade via upregulation of TRIOBP. Mol Ther Nucleic Acids. 2018; 12: 1-11.
Crossref Google Scholar
38

Yang H, Zhang H, Ge S, Nng T, Bai M, Li J, et al. Exosome-derived miR-130a activates angiogenesis in gastric cancer by targeting C-MYB in vascular endothelial cells. Mol Ther. 2018; 26: 2466-75.
Crossref Google Scholar
39

Liu LZ, Li C, Chen Q, Jing Y, Carpenter R, Jiang Y, et al. MiR-21 induced angiogenesis through AKT and ERK activation and HIF-1α expression. PLoS One. 2011; 6: e19139.
Crossref Google Scholar
40

Zhuang G, Wu X, Jiang Z, Kasman I, Yao J, Guan Y, et al. Tumour-secreted miR-9 promotes endothelial cell migration and angiogenesis by activating the JAK-STAT pathway. EMBO J. 2012; 31: 3513-23.
Crossref Google Scholar
41

Goradel NH, Mohammadi N, Haghi-Aminjan H, Farhood B, Negshdari B, Sahebkar A. Regulation of tumor angiogenesis by microRNAs: State of the art. J Cell Physiol. 2019; 234: 1099-110.
Crossref Google Scholar
42

Chung HJ, Choi YE, Kim ES, Han YH, Park MJ, Bae IH. miR-29b attenuates tumorigenicity and stemness maintenance in human glioblastoma multiforme by directly targeting BCL2L2. Oncotarget. 2015; 6: 18429-44.
Crossref Google Scholar
43

Chen S, Zhang Y, Kuzel TM, Zhang B. Regulating tumor myeloid-derived suppressor cells by microRNAs. Cancer Cell Microenviron. 2015; 2: 1-8.
Google Scholar
44

Marcinkowska M, Sobierajska E, Stanczyk M, Janaszewska A, Chworos A, Klajnert-Maculewicz B. Conjugate of PAMAM dendrimer, doxorubicin and monoclonal antibody-trastuzumab: the new approach of a well-known strategy. Polymers. 2018; 10: 187.
Crossref Google Scholar
45

Sirotkin AV, Alexa R, Kišová G, Harrath AH, Alwasel S, Ovcharenko D, et al. MicroRNAs control transcription factor NF-kB (p65) expression in human ovarian cells. Funct Integr Genomics. 2015; 15: 271-5.
Crossref Google Scholar
46

An Y, Yang Q. MiR-21 modulates the polarization of macrophages and increases the effects of M2 macrophages on promoting the chemoresistance of ovarian cancer. Life Sci. 2020; 242: 117162.
Crossref Google Scholar
47

Afshar AS, Xu J, Goutsias J. Integrative identification of deregulated miRNA/TF-mediated gene regulatory loops and networks in prostate cancer. PLoS One. 2014; 9: e100806.
Crossref Google Scholar
48

Shoeibi S. Diagnostic and theranostic microRNAs in the pathogenesis of atherosclerosis. Acta Physiol. 2020; 228: e13353.
Crossref Google Scholar
49

Nakano T, Chen IH, Wang CC, Chen PJ, Tseng HP, Huang KT, et al. Circulating exosomal miR-92b: Its role for cancer immunoediting and clinical value for prediction of posttransplant hepatocellular carcinoma recurrence. Am J Transplant. 2019; 19: 3250-62.
Crossref Google Scholar
50

Kogure A, Kosaka N, Ochiya T. Cross-talk between cancer cells and their neighbors via miRNA in extracellular vesicles: an emerging player in cancer metastasis. J Biomed Sci. 2019; 26: 7.
Crossref Google Scholar
51

Dai X, Huang R, Hu S, Zhou Y, Sun X, Gui P, et al. A novel miR-0308-3p revealed by miRNA-seq of HBV-positive hepatocellular carcinoma suppresses cell proliferation and promotes G1/S arrest by targeting double CDK6/Cyclin D1 genes. Cell Biosci. 2020; 10: 24.
Crossref Google Scholar
52

Lee WH, Chen KP, Wang K, Huang HC, Juan HF. Characterizing the cancer-associated microbiome with small RNA sequencing data. Biochem Biophys Res Commun. 2020; 522: 776-82.
Crossref Google Scholar
53

Hanna J, Hossain GS, Kocerha J. The potential for microRNA therapeutics and clinical research. Front Genet. 2019; 10: 478.
Crossref Google Scholar
54

Kim H, Kim J, Kim K, Chang H, You K, Kim VN. Bias-minimized quantification of microRNA reveals widespread alternative processing and 3’ end modification. Nucleic Acids Res. 2019; 47: 2630-40.
Crossref Google Scholar
55

Wang N, Zheng J, Chen Z, Liu Y, Dura B, Kwak M, et al. Single-cell microRNA-mRNA co-sequencing reveals non-genetic heterogeneity and mechanisms of microRNA regulation. Nat Commun. 2019; 10: 95.
Crossref Google Scholar
56

Bhere D, Arghiani N, Lechtich ER, Yao Y, Alsaab S, Bei F, et al. Simultaneous downregulation of miR-21 and upregulation of miR-7 has anti-tumor efficacy. Sci Rep. 2020; 10: 1779.
Crossref Google Scholar
57

Corsten MF, Miranda R, Kasmieh R, Krichevsky AM, Weissleder R, Shah K. MicroRNA-21 knockdown disrupts glioma growth in vivo and displays synergistic cytotoxicity with neural precursor cell delivered S-TRAIL in human gliomas. Cancer Res. 2007; 67: 8994-9000.
Crossref Google Scholar
58

Lima JF, Cerqueira L, Figueiredo C, Oliveira C, Azevedo NF. Anti-miRNA oligonucleotides: A comprehensive guide for design. RNA Biol. 2018; 15: 338-52.
Crossref Google Scholar
59
Sharad S, Kapur S. MiRNA-based therapeutics in oncology, realities, and challenges. In: Balacescu O, Visan S, Baldasici O, Balacescu L, editors. Antisense Therapy. London: IntechOpen. 2018; 31.
60

Zhong S, Jeong JH, Chen Z, Chen Z, Luo JL. Targeting tumor microenvironment by small-molecule inhibitors. Transl Oncol. 2020; 13: 57-69.
Crossref Google Scholar
61

Aquino-Jarquin G. Emerging role of CRISPR/Cas9 technology for microRNAs editing in cancer research. Cancer Res. 2017; 77: 6812-7.
Crossref Google Scholar
62

Nam L, Coll C, Erthal LCS, de la Torre C, Serrano D, Martínez-Máñez R, et al. Drug delivery nanosystems for the localized treatment of glioblastoma multiforme. Materials (Basel). 2018; 11: 779.
Crossref Google Scholar
63

Chen Y, Gao DY, Huang L. In vivo delivery of miRNAs for cancer therapy: challenges and strategies. Adv Drug Deliv Rev. 2015; 81: 128-41.
Crossref Google Scholar
64
Ladame S, Cheng JY. Nanotechnology and drug delivery. In: Delcassian D, Patel AK, editors. Bioengineering innovative solutions for cancer. Cambridge: Academic Press; 2020. p. 197-219.
Crossref
65

Rietwyk S, Peer D. Next-generation lipids in RNA interference therapeutics. ACS Nano. 2017; 11: 7572-86.
Crossref Google Scholar
66

Chen Y, Zhu X, Zhang X, Liu B, Huang L. Nanoparticles modified with tumor-targeting scFv deliver siRNA and miRNA for cancer therapy. Mol Ther. 2010; 18: 1650-6.
Crossref Google Scholar
67

Zhang JS, Liu F, Huang L. Implications of pharmacokinetic behavior of lipoplex for its inflammatory toxicity. Adv Drug Deliv Rev. 2005; 57: 689-98.
Crossref Google Scholar
68

Trang P, Wiggins JF, Daige CL, Cho C, Omotola M, Brown D, et al. Systemic delivery of tumor suppressor microRNA mimics using a neutral lipid emulsion inhibits lung tumors in mice. Mol Ther. 2011; 19: 1116-22.
Crossref Google Scholar
69
Peplow PV, Martinez B, Calin GA, Esquela-Kerscher A. Strategies for safe and targeted delivery of microRNA therapeutics. In: Myoung SS, Kasinski AL, editors. MicroRNAs in diseases and disorders. London: Royal Society of Chemistry; 2019. p. 386-415.
Crossref
70
Malik B. Small non-coding RNAs as a tool for personalized therapy in familial cancers. In: Malik SS, Masood N, Sherrard A, Bishop PN, editors. AGO-driven non-coding RNAs. Cambridge: Academic Press; 2019. p. 179-208.
Crossref
71

Daige CL, Wiggins JF, Priddy L, Nelligan-Davis T, Zhao J, Brown D. Systemic delivery of a miR34a mimic as a potential therapeutic for liver cancer. Mol Cancer Ther. 2014; 13: 2352-60.
Crossref Google Scholar
72

Bai Z, Wei J, Yu C, Han X, Qin X, Zhanf C, et al. Non-viral nanocarriers for intracellular delivery of microRNA therapeutics. J Mater Chem B. 2019; 7: 1209-25.
Crossref Google Scholar
73

Garg U, Chauhan S, Nagaich U, Jain N. Current advances in chitosan nanoparticles based drug delivery and targeting. Adv Pharm Bull. 2019; 9: 195-204.
Crossref Google Scholar
74

Palmerston Mendes L, Pan J, Torchilin VP. Dendrimers as nanocarriers for nucleic acid and drug delivery in cancer therapy. Molecules. 2017; 22: 1404.
Crossref Google Scholar
75

Ren L, Huang C, Liu YH, Yu Y, Lin L, Wen LJ. The effect and mechanism of microRNA-21 on cis-dichlorodiamineplatinum resistance in lung cancer cell strain. Zhonghua Yi Xue Za Zhi. 2016; 96: 1454-8.
Google Scholar
76

Mir M, Ahmed N, Rehman AU. Recent applications of PLGA based nanostructures in drug delivery. Colloid Surface B Biointerfaces. 2017; 159: 217-31.
Crossref Google Scholar
77

Navarro SM, Morgan TW, Astete CE, Stout RW, Coulon D, Mottram P, et al. Biodistribution and toxicity of orally administered poly (lactic-co-glycolic) acid nanoparticles to F344 rats for 21 days. Nanomedicine. 2016; 11: 1653-69.
Crossref Google Scholar
78

Sharma S, Parmar A, Kori S, Sandhir R. PLGA-based nanoparticles: a new paradigm in biomedical applications. Trac-Trend Anal Chem. 2016; 80: 30-40.
Crossref Google Scholar
79

Fernandez-Piñeiro I, Badiola I, Sanchez A. Nanocarriers for microRNA delivery in cancer medicine. Biotechnol Adv. 2017; 35: 350-60.
Crossref Google Scholar
80

Zhang T, Xue X, He D, Hsieh JT. A prostate cancer-targeted polyarginine-disulfide linked PEI nanocarrier for delivery of microRNA. Cancer Lett. 2015; 365: 156-65.
Crossref Google Scholar
81

Debnath S, Karan S, Debnath M, Dash J, Chatterjee TK. Poly-L-lysine inhibits tumor angiogenesis and induces apoptosis in ehrlich ascites carcinoma and in sarcoma S-180 tumor. Asian Pac J Cancer Prev. 2017; 18: 2255-68.
Google Scholar
82

Shukla RS, Qin B, Cheng K. Peptides used in the delivery of small noncoding RNA. Mol Pharm. 2014; 11: 3395-408.
Crossref Google Scholar
83

Jin H, Yu Y, Chrisler WB, Xiong Y, Hu D, Lei C. Delivery of microRNA-10b with polylysine nanoparticles for inhibition of breast cancer cell wound healing. Breast Cancer. 2012; 6: 9-19.
Crossref Google Scholar
84

Li T, Meng Z, Zhu X, Gan H, Gu R, Wu Z, et al. New synthetic peptide with efficacy for heparin reversal and low toxicity and immunogenicity in comparison to protamine sulfate. Biochem Biophys Res Commun. 2015; 467: 497-502.
Crossref Google Scholar
85

Yoo H, Mok H. Evaluation of multimeric siRNA conjugates for efficient protamine-based delivery into breast cancer cells. Arch Pharm Res. 2015; 38: 129-36.
Crossref Google Scholar
86

Silva S, Almeida AJ, Vale N. Combination of cell-penetrating peptides with nanoparticles for therapeutic application: A review. Biomolecules. 2019; 9: 22.
Crossref Google Scholar
87

Mcclorey G, Banerjee S. Cell-penetrating peptides to enhance delivery of oligonucleotide-based therapeutics. Biomedicines. 2018; 6: 51.
Crossref Google Scholar
88

Oh B, Song H, Lee D, Oh J, Kim G, Ihm SH, et al. Anti-cancer effect of R3V6 peptide-mediated delivery of an anti-microRNA-21 antisense-oligodeoxynucleotide in a glioblastoma animal model. J Drug Target. 2017; 25: 132-9.
Crossref Google Scholar
89

Song H, Oh B, Choi M, Oh J, Lee M. Delivery of anti-microRNA-21 antisense-oligodeoxynucleotide using amphiphilic peptides for glioblastoma gene therapy. J Drug Target. 2015; 23: 360-70.
Crossref Google Scholar
90

Takei Y, Takigahira M, Mihara K, Tarumi Y, Yanagihara K. The metastasis-associated microRNA miR-516a-3p is a novel therapeutic target for inhibiting peritoneal dissemination of human scirrhous gastric cancer. Cancer Res. 2011; 71: 1442-53.
Crossref Google Scholar
91

Takeshita F, Patrawala L, Osaki M, Takahashi RU, Yamamoto Y, Kosaka N, et al. Systemic delivery of synthetic microRNA-16 inhibits the growth of metastatic prostate tumors via downregulation of multiple cell-cycle genes. Mol Ther. 2010; 18: 181-7.
Crossref Google Scholar
92

Tazawa H, Tsuchiya N, Izumiya M, Nakagama H. Tumor-suppressive miR-34a induces senescence-like growth arrest through modulation of the E2F pathway in human colon cancer cells. Proc Natl Acad Sci U S A. 2007; 104: 15472-7.
Crossref Google Scholar
93

Ben-Shushan D, Markovsky E, Gibori H, Triam G, Scomparin A, Satchi-Fainaro R. Overcoming obstacles in microRNA delivery towards improved cancer therapy. Drug Deliv Transl Res. 2014; 4: 38-49.
Crossref Google Scholar
94

Di Pietro P, Strano G, Zuccarello L, Satriano C. Gold and silver nanoparticles for applications in theranostics. Curr Top Med Chem. 2016; 16: 3069-102.
Crossref Google Scholar
95

Vallet-Regí M, Colilla M, Izquierdo-Barba I, Manzano M. Mesoporous silica nanoparticles for drug delivery: current insights. Molecules. 2017; 23: 47.
Crossref Google Scholar
96

El-Boubbou K. Magnetic iron oxide nanoparticles as drug carriers: clinical relevance. Nanomedicine. 2018; 13: 953-71.
Crossref Google Scholar
97

Zhao MX, Zhu BJ. The research and applications of quantum dots as nano-carriers for targeted drug delivery and cancer therapy. Nanoscale Res Lett. 2016; 11: 207.
Crossref Google Scholar
98

Li JM, Zhao MX, Su H, Wang YY, Tan CP, Ji LN, et al. Multifunctional quantum-dot-based siRNA delivery for HPV18 E6 gene silence and intracellular imaging. Biomaterials. 2011; 32: 7978-87.
Crossref Google Scholar
99

Choi AO, Brown SE, Szyf M, Maysinger D. Quantum dot-induced epigenetic and genotoxic changes in human breast cancer cells. J Mol Med (Berl). 2008; 86: 291-302.
Crossref Google Scholar
100

Dobrovolskaia MA, Mcneil SE. Immunological properties of engineered nanomaterials. Nat Nanotechnol. 2007; 2: 469-78.
Crossref Google Scholar
101

Valentini F, Mari E, Zicari A, Calcaterra A, Talano M, Scioli MG, et al. Metal free graphene oxide (GO) nanosheets and pristine-single wall carbon nanotubes (p-SWCNTs) biocompatibility investigation: A comparative study in different human cell lines. Int J Mol Sci. 2018; 19: 1316.
Crossref Google Scholar
102

Yang HW, Huang CY, Lin CW, Liu HL, Huang CW, Liao SS, et al. Gadolinium-functionalized nanographene oxide for combined drug and microRNA delivery and magnetic resonance imaging. Biomaterials. 2014; 35: 6534-42.
Crossref Google Scholar
103

Dahlin RL, Kasper FK, Mikos AG. Polymeric nanofibers in tissue engineering. Tissue Eng Part B Rev. 2011; 17: 349-64.
Crossref Google Scholar
104
Grumezescu AM. Delivering miRNA modulators for cancer treatment. In: Estanqueiro MVH, Lobo JMS, Amaral H. Drug targeting and stimuli sensitive drug delivery systems. London: William Andrew Publishing. 2018: 517-65.
Crossref
105
Mitra AK, Cholkar K, Mandal A. Electrospun Nanofibers in Drug Delivery: Fabrication, Advances, and Biomedical Applications. In: Agrahari V, Agrahari V, Meng J, Mitra AK, editors. Emerging nanotechnologies for diagnostics, drug delivery and medical devices. Amsterdam: Elsevier; 2017. p. 189-215.
Crossref
106

Shi X, Zhou W, Ma D, Ma Q, Bridges D, Ma Y, et al. Ectrospinning of nanofibers and their applications for energy devices. J Nanomat. 2015; 16: 1-21.
Crossref Google Scholar
107

Sasikanth K, Nama S, Suresh S, Brahmaiah B. Nanofibers-a new trend in nano drug delivery systems. Pharma Innovation. 2013; 2: 118.
Google Scholar
108

Orellana EA, Tenneti S, Rangasamy L, Lyle LT, Low PS, Kasinski AL. FolamiRs: ligand-targeted, vehicle-free delivery of microRNAs for the treatment of cancer. Sci Transl Med. 2017; 9: 1-10.
Crossref Google Scholar
109

He F, Wen N, Xiao D, Yan J, Xiong H, Cai S, et al. Aptamer-based targeted drug deliverysystems: Current potential and challenges. Curr Med Chem. 2020; 27: 2189-219.
Crossref Google Scholar
110

Esposito CL, Catuogno S, de Franciscis V. Aptamer-mediated selective delivery of short RNA therapeutics in cancer cells. J RNAi Gene Silencing. 2014; 10: 500-6.
Google Scholar
111

Yin H, Xiong G, Guo S, Xu C, Xu R, Guo P, et al. Delivery of anti-miRNA for triple-negative breast cancer therapy using RNA nanoparticles targeting sem cell marker CD133. Mol Ther. 2019; 27: 1252-61.
Crossref Google Scholar
112

Guo S, Huang F, Guo P. Construction of folate-conjugated pRNA of bacteriophage phi29 DNA packaging motor for delivery of chimeric siRNA to nasopharyngeal carcinoma cells. Gene Ther. 2006; 13: 814-20.
Crossref Google Scholar
113

Ye X, Liu Z, Hemida MG, Yang D. Targeted delivery of mutant tolerant anti-coxsackievirus artificial microRNAs using folate conjugated bacteriophage Phi29 pRNA. PLoS One. 2011; 6: e21215.
Crossref Google Scholar
114
Shegokar R. Lipid nanocarriers for delivery of poorly soluble and poorly permeable drugs. In: Kovacevic AB, editor. Nanopharmaceuticals. Amsterdam: Elsevier; 2020. p. 151-74.
Crossref
115

Khalil IA, Younis MA, Kimura S, Harashima H. Lipid nanoparticles for cell-specific in vivo targeted delivery of nucleic acids. Biol Pharm Bull. 2020; 43: 584-95.
Crossref Google Scholar
116

Costa PM, Cardoso AL, Custódia C, Cunha P, de Almedia LP, de Lima MC. MiRNA-21 silencing mediated by tumor-targeted nanoparticles combined with sunitinib: A new multimodal gene therapy approach for glioblastoma. J Control Release. 2015; 207: 31-9.
Crossref Google Scholar
117

Schlich M, Palomba R, Costabile G, Mizrahy S, Pannuzzo M, Peer D, et al. Cytosolic delivery of nucleic acids: the case of ionizable lipid nanoparticles. Bioeng Transl Med. 2021; 6: e10213.
Crossref Google Scholar
118

Wei P, Cornel EJ, Du J. Ultrasound-responsive polymer-based drug delivery systems. Drug Deliv Transl Res. 2021; 11: 1323-39.
Crossref Google Scholar
119

Dzmitruk V, Apartsin E, Ihnatsyeu-Kachan A, Abashkin V, Scharbin D, Bryszewska M. Dendrimers show promise for siRNA and microRNA therapeutics. Pharmaceutics. 2018; 10: 126.
Crossref Google Scholar
120

Yazdian-Robati R, Ramezani M, Jalalian SH, Abnous K, Taghdisi SM. Targeted delivery of epirubicin to cancer cells by polyvalent aptamer system in vitro and in vivo. Pharm Res. 2016; 33: 2289-97.
Crossref Google Scholar
121

Hao Y, Kieft JS. Three-way junction conformation dictates self-association of phage packaging RNAs. RNA Biol. 2016; 13: 635-45.
Crossref Google Scholar
122

Hao C, Li X, Tian C, Jiang W, Wang G, Mao C. Construction of RNA nanocages by re-engineering the packaging RNA of Phi29 bacteriophage. Nat Commun. 2014; 5: 3890.
Crossref Google Scholar
123

Binzel DW, Shu Y, Li H, Sun M, Zhang Q, Shu D, et al. Specific delivery of miRNA for high efficient inhibition of prostate cancer by RNA nanotechnology. Mol Ther. 2016; 24: 1267-77.
Crossref Google Scholar
124
Jayandharan GR. Viral-and non-viral-based hybrid vectors for gene therapy. In: Mahato M, Jayandharan GR, Vemula PK, editors. Gene and cell therapy: biology and applications. New York: Springer; 2018. p. 111-30.
Crossref
125

Dasgupta I, Chatterjee A. Recent advances in miRNA delivery systems. Methods Protoc. 2021; 4: 10.
Crossref Google Scholar
126

Frank AM, Weidner T, Brynza J, Uckert W, Buchholz CJ, Hartmann J. CD8-Specific designed ankyrin repeat proteins improve selective gene delivery into human and primate T lymphocytes. Hum Gene Ther. 2020; 31: 679-91.
Crossref Google Scholar
127

Stein S, Ott MG, Schultze-Strasser S, Jauch A, Burwinkel B, Kinner A, et al. Genomic instability and myelodysplasia with monosomy 7 consequent to EVI1 activation after gene therapy for chronic granulomatous disease. Nat Med. 2010; 16: 198-204.
Crossref Google Scholar
128

Hacein-Bey-Abina S, von Kalle C, Schmidt M, Le Deist F, Wulffraat N, Mclntyre E, et al. A serious adverse event after successful gene therapy for X-linked severe combined immunodeficiency. N Engl J Med. 2003; 348: 255-6.
Crossref Google Scholar
129

Cavazzana-Calvo M, Payen E, Negre O, Wang G, Hehir K, Fusil F, et al. Transfusion independence and HMGA2 activation after gene therapy of human β-thalassaemia. Nature. 2010; 467: 318-22.
Crossref Google Scholar
130

Zhang JH, Du AL, Wang L, Wang XY, Gao JH, Wang TY. Episomal lentiviral vector-mediated miR-145 overexpression inhibits proliferation and induces apoptosis of human esophageal carcinomas cells. Recent Pat Anticancer Drug Discov. 2016; 11: 453-60.
Crossref Google Scholar
131

Aravalli RN. Development of microRNA therapeutics for hepatocellular carcinoma. Diagnostics (Basel). 2013; 3: 170-91.
Crossref Google Scholar
132

Bofill-De Ros X, Gironella M, Fillat C. MiR-148a- and miR-216a-regulated oncolytic adenoviruses targeting pancreatic tumors attenuate tissue damage without perturbation of miRNA activity. Mol Ther. 2014; 22: 1665-77.
Crossref Google Scholar
133

Kim J, Kim PH, Kim SW, Yun CO. Enhancing the therapeutic efficacy of adenovirus in combination with biomaterials. Biomaterials. 2012; 33: 1838-50.
Crossref Google Scholar
134
Fernandes TG, Diogo MM, Cabral JMS. Bioengineering strategies for gene delivery. In: Shams S, Silva EA, editors. Engineering strategies for regenerative medicine. Academic Press; 2020. p. 107-48.
Crossref
135

Aponte-Ubillus JJ, Barajas D, Peltier J, Bardliving C, Shamlou P, Gold D. Molecular design for recombinant adeno-associated virus (rAAV) vector production. Appl Microbiol Biotechnol. 2018; 102: 1045-54.
Crossref Google Scholar
136

Latronico MV, Condorelli G. Therapeutic use of microRNAs in myocardial diseases. Curr Heart Fail Rep. 2011; 8: 193-7.
Crossref Google Scholar
137
Brunetti-Pierri N. AAV vector-based gene therapy, progress and current challenges. In Safety and Efficacy of Gene-Based Therapeutics for Inherited Disorders. New York: Springer; 2017. p. 77-112.
Crossref
138

Vannucci L, Lai M, Chiuppesi F, Ceccherini-Nelli L, Pistello M. Viral vectors: a look back and ahead on gene transfer technology. New Microbiol. 2013; 36: 1-22.
Google Scholar
139

Bhere D, Tamura K, Wakimoto H, Choi SH, Purow B, Debatisse J, et al. MicroRNA-7 upregulates death receptor 5 and primes resistant brain tumors to caspase-mediated apoptosis. Neuro Oncol. 2018; 20: 215-24.
Crossref Google Scholar
140
Sonawane SH, Bhanvase BA, Sivakumar M. Virus-like particles: nano-carriers in targeted therapeutics. In: Saha G, Saudagar P, Dubey VK, editors. Encapsulation of active molecules and their delivery system. Amsterdam: Elsevier; 2020. p. 197.
Crossref
141

Yao Y, Jia T, Pan Y, Gou H, Li Y, Sun Y, et al. Using a novel microRNA delivery system to inhibit osteoclastogenesis. Int J Mol Sci. 2015; 16: 8337-50.
Crossref Google Scholar
142

Pushko P, Pumpens P, Grens E. Development of virus-like particle technology from small highly symmetric to large complex virus-like particle structures. Intervirology. 2013; 56: 141-65.
Crossref Google Scholar
143

Callanan J, Stockdale SR, Shkoporov A, Draper LA, Ross RP, Hill C. RNA phage biology in a metagenomic era. Viruses. 2018; 10: 386.
Crossref Google Scholar
144
Pinto AM, Silva MD, Pastrana LM, Bañobre-López M, Sillankorva S. The clinical path to deliver encapsulated phages and lysins. FEMS Microbiol Rev. Published online first: March 30, 2021. DOI: 10.1093/femsre/fuab019.
Crossref
145
Gerrard JA, Domigan LJ. Virus-derived nanoparticles. In: Dashti NH, Sainsbury F, editors. Protein nanotechnology. New York: Springer; 2020. p. 149-62.
Crossref
146

Pan Y, Zhang Y, Jia T, Zhang K, Li J, Wang L. Development of a microRNA delivery system based on bacteriophage MS2 virus-like particles. FEBS J. 2012; 279: 1198-208.
Crossref Google Scholar
147

Sun Y, Sun Y, Zhao R. Establishment of microRNA delivery system by PP7 bacteriophage-like particles carrying cell-penetrating peptide. J Biosci Bioeng. 2017; 124: 242-9.
Crossref Google Scholar
148

Hoffmann DB, Böker KO, Schneider S, Eckermann-Felkl E, Schuder A, Komrakova M, et al. In vivo siRNA delivery using JC virus-like particles decreases the expression of RANKL in rats. Mol Ther Nucleic Acids. 2016; 5: e298.
Crossref Google Scholar
149

Chao CN, Yang YH, Wu MS, Chou MC, Fang CY, Lin MC, et al. Gene therapy for human glioblastoma using neurotropic JC virus-like particles as a gene delivery vector. Sci Rep. 2018; 8: 2213.
Crossref Google Scholar
150

Chen W, Kang T, Yuan R, Shao C, Jing S. Immunogenicity and protective potency of Norovirus GII.17 virus-like particle-based vaccine. Biotechnol Lett. 2020; 42: 1211-8.
Crossref Google Scholar
151

Armstrong JK, Hempel G, Koling S, Chan LS, Fisher T, Meiselman HJ, et al. Antibody against poly(ethylene glycol) adversely affects PEG-asparaginase therapy in acute lymphoblastic leukemia patients. Cancer. 2007; 110: 103-11.
Crossref Google Scholar
152

Galaway FA, Stockley PG. MS2 viruslike particles: a robust, semisynthetic targeted drug delivery platform. Mol Pharm. 2013; 10: 59-68.
Crossref Google Scholar
153

Lin Y, Lu Y, Li X. Biological characteristics of exosomes and genetically engineered exosomes for the targeted delivery of therapeutic agents. J Drug Target. 2020; 28: 129-41.
Crossref Google Scholar
154

Sun Z, Shi K, Yang S, Liu J, Zhou Q, Wang G, et al. Effect of exosomal miRNA on cancer biology and clinical applications. Mol Cancer. 2018; 17: 147.
Crossref Google Scholar
155

del Pozo-Acebo L, Hazas MLL, Tomé-Carneiro J, Gil-Cabrerizo P, San-Cristobal R, Busto R, et al. Bovine milk-derived exosomes as a drug delivery vehicle for miRNA-based therapy. Int J Mol Sci. 2021; 22: 1105.
Crossref Google Scholar
156

Shimbo K, Miyaki S, Ishitobi H, Kato Y, Kubo T, Shimose S, et al. Exosome-formed synthetic microRNA-143 is transferred to osteosarcoma cells and inhibits their migration. Biochem Biophys Res Commun. 2014; 445: 381-7.
Crossref Google Scholar
157

Ohno S, Takanashi M, Sudo K, Ueda S, Ishikawa A, Matsuyama N, et al. Systemically injected exosomes targeted to EGFR deliver antitumor microRNA to breast cancer cells. Mol Ther. 2013; 21: 185-91.
Crossref Google Scholar
158

Wang Y, Chen X, Tian B, Liu J, Yang L, Zeng L, et al. Nucleolin-targeted extracellular vesicles as a versatile platform for biologics delivery to breast cancer. Theranostics. 2017; 7: 1360-72.
Crossref Google Scholar
159

Lu M, Xing H, Xun Z, Yang T, Ding P, Cai C, et al. Exosome-based small RNA delivery: progress and prospects. Asian J Pharm Sci. 2018; 13: 1-11.
Crossref Google Scholar
160

Morishita M, Takahashi Y, Nishikawa M, Sano K, Kato K, Yamashita T, et al. Quantitative analysis of tissue distribution of the B16BL6-derived exosomes using a streptavidin-lactadherin fusion protein and iodine-125-labeled biotin derivative after intravenous injection in mice. J Pharm Sci. 2015; 104: 705-13.
Crossref Google Scholar
161

Takahashi Y, Nishikawa M, Shinotsuka H, Matsui Y, Ohara S, Imai T, et al. Visualization and in vivo tracking of the exosomes of murine melanoma B16-BL6 cells in mice after intravenous injection. J Biotechnol. 2013; 165: 77-84.
Crossref Google Scholar
162

Pittenger MF, Discher DE, Péault BM, Phinney DG, Hare JM, Caplan AI. Mesenchymal stem cell perspective: cell biology to clinical progress. NPJ Regen Med. 2019; 4: 22.
Crossref Google Scholar
163
Orlando G, Piemonti L, Ricordi C, Stratta RJ, eds. Cellular therapies in preclinical and clinical islet transplantation: Mesenchymal stem cells. In: Korsgren O, Scholz H, editors. Transplantation, Bioengineering, and Regeneration of the Endocrine Pancreas. Cambridge: Academic Press; 2020. p. 821-31.
Crossref
164

Su Y, Zhang T, Huang T, Gao J. Current advances and challenges of mesenchymal stem cells-based drug delivery system and their improvements. Int J Pharm. 2021; 600: 120477.
Crossref Google Scholar
165

Fan XL, Zhang Y, Li X, Fu QL. Mechanisms underlying the protective effects of mesenchymal stem cell-based therapy. Cell Mol Life Sci. 2020; 77: 2771-94.
Crossref Google Scholar
166

Shah K. Mesenchymal stem cells engineered for cancer therapy. Adv Drug Deliv Rev. 2012; 64: 739-48.
Crossref Google Scholar
167

Munoz JL, Bliss SA, Greco SJ, Ramkissoon SH, Ligon KL, Rameshwar P. Delivery of functional anti-miR-9 by mesenchymal stem cell-derived exosomes to glioblastoma multiforme cells conferred chemosensitivity. Mol Ther Nucleic Acids. 2013; 2: e126.
Crossref Google Scholar
168

Lee HK, Finniss S, Cazacu S, Bucris E, Ziv-Av A, Xiang C, et al. Mesenchymal stem cells deliver synthetic microRNA mimics to glioma cells and glioma stem cells and inhibit their cell migration and self-renewal. Oncotarget. 2013; 4: 346-61.
Crossref Google Scholar
169

Zhang CL, Huang T, Wu BL, He WX, Liu D. Stem cells in cancer therapy: opportunities and challenges. Oncotarget. 2017; 8: 75756-66.
Crossref Google Scholar
170

Chu DT, Nguyen TT, Tien NLB, Tran DK, Jeong JH, Anh PG, et al. Recent progress of stem cell therapy in cancer treatment: molecular mechanisms and potential applications. Cells. 2020; 9: 563.
Crossref Google Scholar
171

Bonneau E, Neveu B, Kostantin E, Tsongalis GJ, de Guire V. How close are miRNAs from clinical practice? A perspective on the diagnostic and therapeutic market. EJIFCC. 2019; 30: 114-27.
Google Scholar
172

Baumann V, Winkler J. miRNA-based therapies: strategies and delivery platforms for oligonucleotide and non-oligonucleotide agents. Future Med Chem. 2014; 6: 1967-84.
Crossref Google Scholar
173

Beg MS, Brenner AJ, Sachdev J, Borad M, Kang YK, Stoudemire J, et al. Phase Ⅰ study of MRX34, a liposomal miR-34a mimic, administered twice weekly in patients with advanced solid tumors. Invest New Drugs. 2017; 35: 180-8.
Crossref Google Scholar
174

Hong DS, Kang YK, Borad M, Sachdev J, Ejadi S, Lim HY, et al. Phase Ⅰ study of MRX34, a liposomal miR-34a mimic, in patients with advanced solid tumours. Br J Cancer. 2020; 122: 1630-7.
Crossref Google Scholar
175

Titze-De-Almeida R, David C, Titze-De-Almeida SS. The race of 10 synthetic RNAi-based drugs to the pharmaceutical market. Pharm Res. 2017; 34: 1339-63.
Crossref Google Scholar
176

Kreth S, Hübner M, Hinske LC. MicroRNAs as clinical biomarkers and therapeutic tools in perioperative medicine. Anesth Analg. 2018; 126: 670-81.
Crossref Google Scholar
177

Reid G, Johnson TG, van Zandwijk N. Manipulating microRNAs for the treatment of malignant pleural mesothelioma: Past, present and future. Front Oncol. 2020; 10: 105.
Crossref Google Scholar
178

van Zandwijk N, Pavlakis N, Kao SC, Linton A, Boyer MJ, Clarke S, et al. Safety and activity of microRNA-loaded minicells in patients with recurrent malignant pleural mesothelioma: a first-in-man, phase Ⅰ, open-label, dose-escalation study. Lancet Oncol. 2017; 18: 1386-96.
Crossref Google Scholar
179

Bajan S, Hutvagner G. RNA-based therapeutics: From antisense oligonucleotides to miRNAs. Cells. 2020; 9: 137.
Crossref Google Scholar
180

Shah MY, Ferrajoli A, Sood AK, Lopez-Berestein G, Calin GA. MicroRNA therapeutics in cancer - an emerging concept. EBioMedicine. 2016; 12: 34-42.
Crossref Google Scholar
181
Faintuch J, Faintuch S. Non-coding RNA therapy in cancer. In: Souckova K, Ivkovic TC, Slaby O, editors. Precision medicine for investigators, practitioners and providers. Cambridge: Academic Press; 2020. p. 211-20.
Crossref
182

Segal M, Biscans A, Gilles ME, Anastasiadou E, de Luca R, Lim J, et al. Hydrophobically modified let-7b miRNA enhances biodistribution to NSCLC and downregulates HMGA2 in vivo. Mol Ther Nucleic Acids. 2020; 19: 267-77.
Crossref Google Scholar
183

Hossian A, Mackenzie GG. Mattheolabakis G. MiRNAs in gastrointestinal diseases: can we effectively deliver RNA-based therapeutics orally? Nanomedicine (Lond). 2019; 14: 2873-89.
Crossref Google Scholar
184

Tao H, Zhao J, Liu T, Cai Y, Zhou X, Xing H, et al. Intranasal delivery of miR-146a mimics delayed seizure onset in the lithium-pilocarpine mouse model. Mediators Inflamm. 2017; 2017: 6512620.
Crossref Google Scholar
185

Topcu B, Gultekinoglu M, Timur SS, Eroglu I, Ulubayram K, Eroglu H. Current approaches and future prospects of nanofibers: a special focus on antimicrobial drug delivery. J Drug Target. 2021; 29: 563-75.
Crossref Google Scholar
186

Wang G, Hu W, Chen H, Shou X, Ye T, Xu Y. Cocktail strategy based on NK cell-derived exosomes and their biomimetic nanoparticles for dual tumor therapy. Cancers (Basel). 2019; 11: 1560.
Crossref Google Scholar
Cancer Biology & Medicine
Volume 19 Issue 3,
March 2022
Pages 289-304
DOI: 10.20892/j.issn.2095-3941.2021.0294
Cite this article:
Arghiani N, Shah K. Modulating microRNAs in cancer: next-generation therapies. Cancer Biology & Medicine, 2022, 19(3): 289-304. https://doi.org/10.20892/j.issn.2095-3941.2021.0294

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Received: 13 May 2021
Accepted: 27 July 2021
Published: 15 March 2022
©2022 Cancer Biology & Medicine.

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