Table 1.

Functions of microRNAs in tumor metastasis

microRNA	Function in tumor metastasis	Targets and putative targets	References
miR-10b	Promotes cell migration, invasion and metastasis	TP53, PAX6, NOTCH1, HOXD10	[11, 12]
miR-19a/b	Promotes gastric cancer cell migration, invasion and metastasis	MXD1	[13]
miR-135b	Promotes cell migration, invasion and metastasis	LATS2, β-TrCP, NDR2, LZTS1	[14]
miR-362-5p	Promotes cell proliferation, migration and invasion in vitro and tumor growth and metastasis in vivo	CYLD	[15]
miR-34a	Inhibits cell migration, invasion and lung metastasis of breast cancer cells; suppresses prostate CSCs and metastasis; decreases the production of the chemokine CCL22; disturbs the bone metastatic niche	Fra-1, CD44, CCL22, Tgif2	[16, 68, 72, 73]
miR-34c	Inhibits cell migration, invasion and lung metastasis of breast cancer cells	Fra-1	[16]
miR-135a	Inhibits prostate cancer cell migration and invasion	ROCK1, ROCK2	[17]
miR-137	Reduces the invasiveness of colorectal cancer cells	FMNL2	[18]
miR-145	Attenuates gastric cancer cell migratory and invasive abilities in vitro and suppresses the metastatic cascade in vivo; inhibits the invasion and metastasis of neuroblastoma cells	N-cadherin, HIF-2α	[19, 20]
miR-1	Affects the cellular organization of F-actin and impairs tumor cell invasion and filopodia formation	FN1, LASP1, XPO6	[21]
miR-335	Suppresses cell migration, invasion and metastasis	Tenascin C, SOX4	[24]
miR-29c	Inhibits tumor invasion and metastasis	Collagens, Laminin γ1	[25]
miR-21	Promotes epithelial collective cell migration, invasion and lung metastasis; enhances colorectal cancer cell intravasation	TPM1, PDCD4, Maspin, PDCD4	[27, 30, 31]
miR-124	Modulates the intercellular adhesion of leading cells; inhibits EMT in vitro and suppresses intrahepatic and pulmonary metastasis in vivo	Integrin β1, ROCK2, EZH2	[28, 55]
miR-105	Destroys the integrity of vascular endothelial barriers to promote metastasis	ZO-1	[29]
miR-182	Promotes cancer cell intravasation into the circulation	Mtss1, Pai1, Rsu1, Timp1	[32]
miR-520c/373	Inhibits cell invasion in vitro and the intravasation of breast cancer cells in vivo	RELA, TGFBR2	[33]
let-7	Inhibits bone metastasis of breast cancer cells	HMGA2, Snail	[34]
miR-296-3p	Promotes prostate cancer cell survival	ICAM-1	[35]
miR-148b	Inhibits multiple steps of tumor progression via the regulation of invasion, resistance to anoikis, extravasation, lung metastasis colonization and chemotherapeutic response	ITGA5, ROCK1, PIK3CA/p110α, NRAS, CSF1	[36]
miR-155	Negatively regulates the function of the brain endothelial barrier; promotes TGF-β-induced EMT, tight junction dissolution, cell migration and invasion. Suppresses tumor growth via the regulation of the tumor microenvironment	Annexin-2, Claudin-1, DOCK-1, Syntenin-1, c-Maf, Pu.1, Ship1, C/EBPβ, HIF-1α	[38, 50, 76–78]
miR-214	Suppresses cell migration and invasion in vitro and inhibits liver metastasis of colorectal cancer cells in vivo but promotes migration, invasion and resistance to anoikis of melanoma cells in vitro and the extravasation and lung metastasis formation in vivo	FGFR1, TFAP2C	[39–41]
miR-31	Represses local invasion, extravasation and initial survival in distant tissues and distant metastatic colonization	ITGA5, RDX, RhoA	[42]
miR-25	Inhibits extravasation of prostate cancer cells in vivo	αv- and α6-integrins	[43]
miR-200s	Inhibits EMT but promotes metastatic colonization	Sec23a, ZEB1, ZEB2	[44, 52, 53]
miR-122	Promotes metastatic colonization of breast cancer cells	PKM2	[45]
miR-149	Inhibits basal-like breast cancer cell migration and invasion in vitro and impairs lung colonization in vivo	Rap1a, Rap1b	[46]
miR-493	Inhibits the settlement of metastasized colon cancer cells in the liver; promotes the death of colon cancer cells	IGF1R	[47]
miR-148a	Inhibits hepatoma cell migration in vitro and pulmonary metastatic colonization in vivo	Met	[48]
miR-9	Promotes breast cancer cell motility and invasiveness; enhances squamous cell carcinoma CSC expansion and metastasis	CDH1, α-catenin	[49, 66]
miR-20a	Induces EMT and promotes metastasis	Smad7	[51]
miR-203	Suppresses cell invasion and EMT in vitro and lung metastatic colonization in vivo	SNAI2	[54]
miR-612	Inhibits local invasion and distant metastatic colonization	Akt2	[56]
miR-125a	Inhibits EMT of ovarian cancer cells	ARID3B	[58]
miR-424	Promotes EMT	TGFBR3	[60]
miR-22	Promotes EMT, invasiveness, stemness and metastasis	TET1, TET2, TET3	[64]
miR-199a	Endows breast cancer cells with enhanced CSC properties; promotes invasion, angiogenesis and colonization in the case of melanoma	FOXP2, ApoE	[65, 92]
miR-133a	Promotes invasion of CSCs that express high levels of CD133	SGMS2, UBA2, SNX30, ANXA2	[67]
miR-7	Suppresses cell invasion and metastasis; inhibits the ability of breast CSCs to metastasize to the brain	SETDB1, KLF4	[69, 70]
miR-33b	Inhibits the stemness and lung metastasis of breast cancer cells	HMGA2, SALL4, Twist1	[71]
miR-494	Promotes the accumulation of MDSCs in tumor tissues	PTEN	[81]
miR-101	Augments cancer cell stemness and enhances the tumorigenic and metastatic potential of cancer cells; inhibits HCC growth, intrahepatic metastasis and distant metastasis	CtBP2, ROCK2	[82, 94]
miR-126	Inhibits endothelial recruitment, metastatic angiogenesis and metastatic colonization at distant sites	IGFBP2, PITPNC1, MERTK, SDF-1α	[83, 84]
miR-126*	Suppresses breast cancer metastasis via the inhibition of the recruitment of mesenchymal stem cells and inflammatory monocytes	SDF-1α	[84]
miR-23b	Promotes breast cancer cell dormancy in a metastatic niche	MARCKS	[87]
miR-127/197/222/223	Promotes breast cancer cell quiescence	CXCL12	[88]
miR-103/107	Promotes local invasion and liver metastasis	DAPK, KLF4	[89]