Regulators at Every Step—How microRNAs Drive Tumor Cell Invasiveness and Metastasis
Abstract
:Simple Summary
Abstract
1. Introduction
2. Tumor Cell Migration and Local Invasion
2.1. Step 1: Polarization of the Cytoskeleton and Formation of the Leading Protrusion
2.2. Step 2: Formation of Focalized Clusters by Recruitment and Adhesion of Cell Surface Receptors to ECM
2.2.1. Integrins
2.2.2. Podoplanin
2.2.3. CD44
2.2.4. Syndecan-1
2.2.5. Focal Adhesion Kinase (FAK)
2.2.6. Production of ECM
2.2.7. Cadherins
2.2.8. JAM-A
2.3. Step 3: Local Proteolysis of ECM
2.4. Step 4: Cell Contraction by Actomyosin, Myosin II Activation by the Small GTPase Rho and Step 5: Rotation of the Adhesive Bonds on the Trailing Edge
3. Epithelial–Mesenchymal Transition (EMT)
4. Angiogenesis
4.1. Regulation of Angiogenesis by miRNA
4.2. Vascular Endothelial Growth Factor-A (VEGF-A)
4.3. Thrombospondin-1 (TSP-1)
4.4. Platelet-Derived Growth Factor (PDGF)
4.5. Hypoxia-Inducible Factor 1 Alpha (HIF1a)
5. Chemokines and Growth Factors
6. Intravasation, Systemic Circulation, and Extravasation
6.1. Intravasation
6.2. Systemic Circulation
6.3. Extravasation
7. Metastatic Colonization
8. Tumor–Stroma Interactions
8.1. Cancer-Associated Fibroblasts (CAFs– Tumor Cells Interactions
8.2. Immune Cells–Tumor Cells Interactions
9. miRNAs as Biomarkers in Cancer
10. Challenges for the Use of miRNAs in Clinical Oncology
11. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
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miRNA | Cancer Type | Target | Role in Vitro | Role in Vivo | Ref. | |
---|---|---|---|---|---|---|
OncomiRs | miR-9 | Breast cancer | CDH1 | ↑ cell migration and invasiveness | ↑ tumor invasion and metastasis ↑ angiogenesis | [24] |
miR-10b | Breast cancer | HOXD10 | ↑ cell migration and invasiveness | ↑ tumor invasion and metastasis | [25] | |
miR-17-5p | Colorectal cancer | PTEN, P130 | ↑ cell migration and invasiveness | ↑ tumor growth | [26,27] | |
miR-19b | Breast cancer | TP53 | ↑ cell migration and invasiveness, cell cycle progression | ↑ tumor growth and metastasis | [28] | |
miR-21 | Colorectal cancer | Pdcd4 | ↑ cell invasiveness | ↑ intravasation and metastasis | [29] | |
miR-135b | Lung cancer | LZTS1, Hippo pathway | ↑ cell migration and invasiveness | ↑ tumor growth and metastasis | [30] | |
miR-181a | Breast cancer | Bim | ↑ cell migration and invasiveness ↓ anoikis | ↑ tumor growth and metastasis | [31] | |
miR-214 | Melanoma | TFAP2C, ITGA3 | ↑ cell migration and invasiveness | ↑ extravasation and metastasis | [32] | |
miR-211 | Colorectal cancer | CHD5 | ↑ cells proliferation and migration | ↑ tumor growth | [33] | |
miR-223 | Gastric cancer | EPB41L3 | ↑ cells motility and invasiveness | ↑ metastasis | [34] | |
Tumor suppressor miRs | miR-34a | Neuroblastoma | MAP3K9 | ↑ induction of cell cycle arrest and apoptosis | ↓ tumor growth | [35] |
miR-137 | Colorectal cancer | FMNL2 | ↓ cells proliferation and invasion | ↓ metastasis | [36] | |
miR-192 | Colon cancer | Bcl-2, ZEB2 | ↑ apoptosis | ↓ metastasis | [37] | |
miR-375 | Liver cancer | AEG-1 | ↓ cell growth and invasiveness | ↓ tumor growth | [38] | |
miR-874 | Non-small cell lung cancer | MMP-2, uPA | ↓ cells invasiveness | ↓ tumor growth | [39] | |
let-7 | Lung cancer | KRAS | ↓ cell proliferation | ↓ tumor growth | [40] |
Target | Role | miRNA | Role | Ref. |
---|---|---|---|---|
RhoC | Promotes reorganization of the actin cytoskeleton and regulates cell shape and motility. | miR-93, miR-106b, miR-138, miR-372, miR-493, miR-509 | Decreases migration and invasiveness, reorganization of the stress fibers. | [67,68,69,70,71,72,73] |
CDC42 | Transduces signals to the actin cytoskeleton, promotes the formation of filopodia. | miR-133, miR-137, miR-186, miR-195, miR-330 | Decreases cell migration and invasiveness. | [49,50,51,52,53,74] |
RAC1 | Regulates reorganization of the actin cytoskeleton, promotes the formation of lamellipodia. | miR-142-3p, miR-145 | Decreases cell migration and invasiveness. | [57,58] |
RHOA | Regulates cell adhesion and migration, provides contractile force by the formation of stress fibers. | miR-31, miR-122, miR-133a-3p, miR-146a, miR-200b, miR-340-5p | Decreases cell migration. | [75,76,77,78,79,80] |
PHACTR1 | Binds actin and regulates the reorganization of the actin cytoskeleton. | miR-584 | Decreases expression leads to the induction of migration. | [81] |
TKS5 | Regulates actin cytoskeleton and invadopodia formation. | miR-200c | Decreases invasiveness. | [82] |
MYLK | Regulates the phosphorylation of myosin light chains. | miR-155, miR-200c |
Decreases invasiveness and ability to form invadopodia. | [82,83] |
ROCK1 | Regulates actinomyosin cytoskeleton. | miR-124, miR-145, miR-148b, miR-199a, miR-335, miR-340, miR-584, miR-1280 | Decreases cells migration and invasiveness. | [63,84,85,86,87,88,89] |
ROCK2 | Regulates actinomyosin cytoskeleton. | miR-124, miR-130a, miR-135a, miR-138, miR-139, miR-144, miR-185, miR-4529-5p | Decreases cells migration and invasiveness. | [90,91,92,93,94,95,96,97] |
FHOD1 | Regulates actin cytoskeleton. | miR-200c | Decreases migration and invasiveness. | [98] |
PPM1F | Regulates actin cytoskeleton. | miR-149, miR-200c, miR-490, miR-590 | Decreases migration and invasiveness. | [98,99,100,101] |
WAVE3 | Regulates actin cytoskeleton. | miR-31, miR-200 | Decreases invasiveness. | [102,103] |
PAK1 | Regulates cell motility and cytoskeletal remodeling. | Let-7, miR-7, miR-26a, miR-26b, miR-98, miR-145, miR-485, miR-494, | Decreases migration and invasiveness. | [64,103,104,105,106,107,108,109] |
DIAPH2 | Regulates microtubule attachment to kinetochores. | Let-7, miR-10b | Decreases migration and invasiveness. | [64,110] |
RDX | Regulates of membrane domains through interaction with the cytoskeleton and transmembrane proteins. | Let-7, miR-31, mir-200b, miR-409 | Decreases migration and invasiveness. | [64,111,112] |
PAK2 | Regulates of cell motility and cytoskeletal remodeling. | miR-7, miR-23b, miR-137, miR-216a, miR-455, miR-4779, | Decreases migration and invasiveness, cytoskelet remodeling. | [113,114,115,116,117] |
CFL1 | Binds actin and regulates cell proliferation and migration. | miR-342 | Decreases invasion and migration. | [118] |
TWF1 | Binds actin and promotes EMT. | miR-30c, miR-142, miR-486 | Decreases stress fibers F-actin formation. | [119,120,121] |
PFN1 | Binds actin and inhibits cells proliferation, migration, invasion and EMT. | miR-19a-3p, miR-182, miR-299-3p, miR-330-3p, | Increases migration and invasiveness. | [122,123,124,125,126] |
FSCN1 | Stabilizes actin filaments in invadopodia. | miR-24, miR-133a, miR-133b, miR-145, miR-200b, miR-326, miR-429, miR-539, miR-663 | Decreases invasiveness. | [127,128,129,130,131,132,133,134,135] |
WASL | Regulates actin polymerization. | miR-142-3p, miR-148a | Decreases invasiveness, reduced number of membrane protrusions. | [65,136] |
Integrin | Protein Name | Synonyms [146] | miRNA | Ref. |
---|---|---|---|---|
ITGA1 | α1 | CD49a | miR-375 | [145] |
ITGA2 | α2 | CD49b, α2 subunit of very late antigen 2 (VLA-2) | miR-31 | [144] |
ITGA2B | αIIb | GTA, CD41, GP2B, HPA3, CD41b, GPIIb | miR-122 | [147] |
ITGA3 | α3 | CD49c, α3 subunit of VLA-3 | miR-199 family | [148] |
ITGA4 | α4 | CD49d, α4 subunit of VLA-4 | miR-30a | [149] |
ITGA5 | α5 | CD49e, fibronectin receptor alpha | miR-25-3p, miR-26a, miR-31, miR-92, miR-142-3p, miR-148b, miR-149 | [65,84,138,144,150] |
ITGA6 | α6 | CD49f, ITGA6B | miR-25, miR-29s, miR-143-3p | [151,152,153] |
ITGA7 | α7 | nd | ||
ITGA8 | α8 | nd | ||
ITGA9 | α9 | miR-296-3p | [154] | |
ITGA10 | α10 | miR-34a | [155] | |
ITGA11 | α11 | miR-148a | [136] | |
ITGAD | αD | nd | ||
ITGAE | αE | CD103, human mucosal lymphocyte antigen 1α | nd | |
ITGAL | αL | CD11a (p180), lymphocyte function-associated antigen 1 (LFA-1) α subunit | miR-126 | [156] |
ITGAM | αM | Mac-1, CD11b, complement receptor 3 (CR3) subunit | miR-124 miR-223 | [157,158] |
ITGAV | αV | CD51, MSK8, vitronectin receptor α (VNRα) | miR-25, miR-31, miR-92, miR-142-3p | [65,144,151,159] |
ITGAX | αX | CD11c, CR4 subunit | miR-142 | [160] |
ITGB1 | β1 | Fibronectin receptor β, CD29, MDF2, MSK12 | miR-29b, miR-29c miR-31, miR-124 miR-130b, miR-149 miR-183, miR-338-3p, miR-451 | [144,161,162,163,164,165,166,167] |
ITGB2 | β2 | Leukocyte cell adhesion molecule, CD18, CR3 subunit, CR4 subunit | miR-1, miR-133a | [168] |
ITGB3 | β3 | CD61; GP3A; GPIIIa, platelet glycoprotein IIIa | miR-31, mir-150 | [144,169] |
ITGB4 | β4 | CD104 | miR-29a, miR-184 | [170] |
ITGB5 | β5 | miR-185 | [171] | |
ITGB6 | β6 | miR-17/20a | [172] | |
ITGB7 | β7 | nd | ||
ITGB8 | β8 | let-7, miR-93 miR-145, miR-148a | [64,136,173] |
MMP | Role | Role in Cancer | miRNA | Ref. |
---|---|---|---|---|
Collagenases | ||||
MMP-1 | Degradation of collagen types I, II, III, V, IX and fibrillary collagen | Initial invasion, metastasis | miR-222, miR-361-5p | [212,213] |
MMP-8 | Degradation of collagen types I, II, III, V, IX and fibrillary collagen | Inhibits invasion and metastasis | miR-539, miR-2682-3p | [214] |
MMP-13 | Degradation of collagens types I, II, III, V, IX and fibrillary collagen | Tumor growth, invasion | miR-125b,miR-148a, miR-188-5p | [215,216] |
Matrilysins | ||||
MMP-7 | Proteolysis of fibronectin, collagen type IV, laminin, elastin, entactin, osteopontin, and cartilage proteoglycan aggregates | Invasive potential, proliferation, anti-apoptotic | miR-143, miR-489, miR-543 | [217,218] |
MMP-26 | Degradation of collagen type IV, fibronectin, fibrinogen, casein, vitronectin, and others | Activates MMP-9 | nd | |
Metalloelastase | ||||
MMP-12 | Degradation of elastin | Protective inhibition of tumor growth | nd | |
Stromelysins | ||||
MMP-3 | Degradation of collagen types II, III, IV, IX, and X, proteoglycans, fibronectin, laminin, and elastin | Invasion, metastasis, EMT, angiogenesis | miR-17, miR-152 | [219,220] |
MMP-10 | Degradation of proteoglycans and fibronectin | Invasion, migration, tumor growth | nd | |
MMP-11 | Degradation of alpha-1 antitrypsin | Early tumor invasion | miR-125a-5p, miR-145, miR-192 | [221,222,223] |
Gelatinases | ||||
MMP-2 | Degradation of type IV collagen | Degradation of ECM | miR-29b, miR-29c, miR-106b, miR-874 | [39,203,224,225] |
MMP-9 | Degradation of type IV collagen | Degradation of ECM | miR-29b, miR-183, miR-491-5p | [226,227,228] |
Enamelysin | ||||
MMP-20 | Tooth-specific MMP | nd | ||
Membrane-Type | ||||
MMP-14 | Degradation of fibronectin, collagen, and gelatin | Activation of other MMPs | miR-9, miR-22, miR-337-3p | [229,230,231] |
MMP-15 | EMT, angiogenesis | miR-608 | [232] | |
MMP-16 | Invasion, metastasis | miR-132, miR-146a, miR-146b, miR-215, miR-328-3p | [233,234,235,236,237] | |
MMP-17 | Angiogenesis, metastasis | nd | ||
MMP-24 | Migration, metastasis | nd | ||
MMP-25 | Tumor growth | nd | ||
Others | ||||
MMP-19 | Tumor growth, adhesion, metastasis | miR-16, miR-193b-3p, miR-637 | [238,239,240] | |
Inhibitors of metalloproteinase | ||||
TIMP1 | Inhibition of MMP-14 -16, -19, -24 and ADAM10 | Inhibition of cancer growth and metastasis | miR-182, miR-1293 | [241,242] |
TIMP2 | Inhibition of all MMPs and ADAM12 | Inhibition of cancer growth and metastasis | miR-205-5p | [243] |
TIMP3 | Inhibition of all MMPs and ADAM10, 12, 17, 28 and 33; ADAMTS-1, -4, and -5, ADAMTS-2 | Inhibition of tumor growth, angiogenesis, and invasion | miR-21, miR-103, miR-181b, miR-191 | [244,245,246,247] |
TIMP4 | Inhibition of most MMPs and ADAM17d, -28, and -33 | Inhibition of angiogenesis, and invasion, promotion of apoptosis | miR-558 | [248] |
RECK | Inhibition of MMP-9 | Inhibition of metastasis | miR-7, miR-21, miR-222 | [207,249,250,251] |
miRNAs Promoting Invasiveness | miRNAs Suppressing Invasiveness | ||||
---|---|---|---|---|---|
miRNA | Targets | Ref. | miRNA | Targets | Ref. |
miR-9 | SOX7, CDH1, α-catenin | [24,256,257,258] | miR-10b | IGF-1R, HOXA-3, FGF13 | [259,260,261] |
miR-10b | TP53, PAX6, NOTCH1, HOXD10, TIP30, KLF4, HOXB3 | [259,262,263,264,265] | miR-29c | CDK6, ITGB1, TIAM1, Collagens, Laminin γ1 | [193,266,267,268] |
miR-21 | PDCD4, maspin, HBP1, LZTFL1, KLF5 | [185,269,270,271,272] | miR-34a | SATB2, BCL-2, HNF4α, Snail, MMP9, MMP14, Notch1 | [273,274,275,276,277,278] |
miR-103 | DAPK, KLF4, OLFM4, LATS2, PTEN | [279,280,281,282] | miR-135a | ROCK1, Smo, ERRα | [283,284,285] |
miR-107 | TPM1, DAPK, KLF4 | [279,286] | miR-145 | PAK4, ROCK1, MMP11, Rab27a, MUC1, MMP16, N-cadherin, ZEB2, Ets1, KLF4 | [88,287,288,289,290,291,292,293] |
miR-135b | NR3C2, LZTS1, APC, FOXO1, ST6GALNAC2, RECK, EVI5 | [30,71,294,295,296,297] | miR-148b | WNT1, MTA2, ROCK1, Dock6 | [298,299,300,301] |
miR-155 | DOCK-1, SDCBP, ANXA-2, CLDN-1, NDFIP1, SOCS1, TP53INP1, BCL6 | [302,303,304,305,306] | miR-200 | Foxf2, Flt1, BMP4, Onecut2, LIMK1, BMI-1, E2F3 | [307,308,309,310,311] |
miR-223 | PAX6, hFBXW7, EPB41L3 | [34,312,313] | miR-214 | JAG1, ROCK1, CDC25B, ARL2, GALNT7, MKK3, JAK1 | [314,315,316,317,318,319,320] |
miR-424 | CADM1, SMAD7 | [321,322] | miR-340 | NT5E, EphA3, SIRT7, NF-κB1, RhoA, ROCK1, JAK1 | [85,323,324,325,326,327,328] |
Target | miRNAs | Ref. |
---|---|---|
TGF-β1 | miR-99a, miR-99b, miR-744 | [359,360] |
TGFBR2 | miR-17 family, miR-21, miR-204, miR-211, miR-373, miR-520 | [361,362,363,364,365] |
ZEB1 | miR-200 family, miR-205 | [366,367] |
ZEB2 | miR-132, miR-138, miR-154, miR-200 family, miR-205, miR-215 | [367,368,369,370,371] |
Twist1 | let-7d, miR-33a, miR-145a-5p, miR-151-5p, miR-214, miR-580 | [372,373,374,375] |
Twist2 | miR-138, miR-215 | [376,377] |
Notch | miR-23b, miR-30a, miR-34a, miR-206 | [131,378,379,380] |
Snail1 | miR-22, miR-34a, miR-137, miR-182 | [231,276,381] |
Snail2 | miR-30a, miR-124, miR-203, miR-204, miR-211 | [362,382,383,384] |
EZH2 | miR-138 | [368] |
Slug | miR-1, miR-30a, miR-124, miR-506, miR-630, miR-590-3p | [385,386,387,388,389,390] |
N-cadherin | miR-145, miR-194 | [391,392] |
Vimentin | miR-30c | [393] |
Fibronectin | miR-1, miR-139, miR-200c, miR-432 | [394,395,396,397] |
E-Cadherin | miR-10b, miR-22, miR-23b, miR-25, miR-92a, miR-221, miR-720, | [196,398,399,400,401,402,403] |
ZO-1 | miR-103 | [404] |
Claudins | miR-98 (claudin-1), miR-146-5p (claudin-12), miR-421 (claudin-11), miR-488 (claudin-2), miR-155 (claudin-1) | [405,406,407,408,409] |
Target | miRNA | Ref. |
---|---|---|
VEGF | miR-20b, miR-27b, miR-29b, miR-93, miR-126, miR-128, miR-140-5p, miR-195, miR-203, miR-205, miR-497, miR-503, miR-638, | [51,245,413,414,415,416,417,418,419,420,421,422,423,424] |
VEGFR | miR-378a, miR-497 | [425] |
NRP1 | miR-141, miR-338 | [426,427] |
TSP-1 | miR-19a, miR-182, miR-467 | [428,429,430] |
FGF | miR-503, miR-5582-5p | [421,431] |
HDGF | miR-139, miR-195, miR-214, miR-497, miR-511, miR-873, miR-939 | [432,433,434,435,436,437,438] |
Angiogenin | miR-204 | [363] |
PDGF | miR-29a | [439] |
HIF1a | miR-20b, miR-33a, miR-107, miR-135b, miR-519c | [440,441,442,443] |
HIF2a | miR-145 | [58] |
VHL | miR-21, miR-155, miR-222 | [444,445,446] |
STAT3 | miR-125a, miR-411, miR-544, miR-874, miR-1299 | [447,448,449,450,451] |
Bmi-1 | miR-16, miR-132, miR-183, miR-200c, miR-203, miR-218 | [452,453,454,455,456,457] |
E2F3 | miR-194-5p, miR-200c, miR-217, miR-432, miR-449a | [311,458,459,460,461] |
NF90 | miR-590-5p | [462] |
miRNA | Cancer | Type of Tissue | Mirna Level | Lymph Node Metastasis | Distant Metastasis | Ref. |
---|---|---|---|---|---|---|
miR-203 | Colorectal | Serum | High | OR 2.9; 95%CI 1.4–6.1; p = 0.0035 | OR 5.3; 95%CI 2.4–11.5; p < 0.0001 | [549] |
miR-885-5p | Colorectal | Serum | High | OR 3.0; 95%CI 1.3–7.2; p = 0.0116 | OR 3.1; 95%CI 1.0–10.0; p = 0.0456 | [547] |
miR-19a | Various carcinomas | Serum and tissue | High | OR 0.564; 95%CI 0.346–0.921 | nd | [550] |
miR-20a | Cervical | Serum | High | OR 1.552; 95%CI 1.137–2.118 | nd | [551] |
miR-21 | Breast | Serum and tissue | High | OR 2.36; 95%CI 1.04–4.78; p = 0.03 | nd | [545] |
miR-21 | Pancreatic ductal adenocarcinoma | Serum and tissue | High | OR 1.45; 95%CI 1.02–2.06; p = 0.038 | [546] | |
miR-122-5p | Colorectal | Serum | High | OR 1.621; 95%CI 1.255–2.092; p = 0.0002 | nd | [552] |
miR-146b-5p | Colorectal | Serum | High | OR 2.096; 95%CI 1.594–2.756; p < 0.0001 | nd | [552] |
miR-186-5 | Colorectal | Serum | High | OR 2.910; 95%CI 1.810–4.678; p < 0.0001 | nd | [552] |
miR-193a-5p | Colorectal | Serum | High | OR 0.656; 95%CI 0.577–0.774; p < 0.0001 | nd | [552] |
let-7i | Colorectal | Tissue | Low | nd | OR 5.5; 95%CI 1.1–26.8; p = 0.0334 | [547] |
miR-10b | Colorectal | Tissue | High | nd | OR 4.9; 95%CI 1.2–19.7; p = 0.0248 | [547] |
miR-29a | Colorectal | Serum | High | nd | OR 3.500; 95%CI 1.274–9.617; p < 0.05 | [553] |
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Grzywa, T.M.; Klicka, K.; Włodarski, P.K. Regulators at Every Step—How microRNAs Drive Tumor Cell Invasiveness and Metastasis. Cancers 2020, 12, 3709. https://doi.org/10.3390/cancers12123709
Grzywa TM, Klicka K, Włodarski PK. Regulators at Every Step—How microRNAs Drive Tumor Cell Invasiveness and Metastasis. Cancers. 2020; 12(12):3709. https://doi.org/10.3390/cancers12123709
Chicago/Turabian StyleGrzywa, Tomasz M., Klaudia Klicka, and Paweł K. Włodarski. 2020. "Regulators at Every Step—How microRNAs Drive Tumor Cell Invasiveness and Metastasis" Cancers 12, no. 12: 3709. https://doi.org/10.3390/cancers12123709