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Table 1 Functions of microRNAs in tumor metastasis

From: The roles of microRNAs in the regulation of 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]