Syndecan-4 in Tumor Cell Motility
Abstract
:Simple Summary
Abstract
1. Introduction
2. Cytoskeletal System during Cell Migration
2.1. Rearrangement of the Actin Cytoskeleton during Migration
2.2. The Role of Intermediate Filaments in Cell Motility
2.3. The Complex Function of Microtubules in Cell Migration
2.4. The Role of Septins in Cell Migration
3. Multiple Functions of Rho GTPases in Cell Motility
4. Front-Rear Polarity of Migrating Cells
5. Syndecan Family of Transmembrane Proteoglycans
General Structure of Syndecans
6. Structure, Interacting Partners and Signaling of Syndecan-4
6.1. Syndecan-4 and the Regulation of Rac1/RhoA Activity
6.2. Syndecan-4 and Focal Adhesion Formation
7. SDC4 and Tumor Cell Migration
7.1. Melanoma
7.2. Breast Cancer
7.3. Lung Cancer
7.4. Other Tumor Types
Cell Type | Migration Assay | Signaling Pathway | Biological Effect | Citation |
---|---|---|---|---|
4T1 and MDA-MB-231 breast cancer cells | - | - | SDC4 has an anti-migratory, anti-invasive tumor suppressor role. | [161] |
Colon carcinoma cells | - | SDC4 expression | SDC4 is downregulated in colon carcinoma cells. | [162] |
Infiltrating breast carcinoma tissues | - | SDC4 expression | SDC4 is upregulated in normal breast tissue compared to malignant breast tissue | [202] |
Human ovarian carcinoma cell line NIH:OVCAR5 | Modified Boyden chamber chemotaxis, Matrigel invasion assay | Carbohydrate modifications | The migration, invasion and tumor growth of ovarian carcinoma is mediated by the carbohydrate modifications of proteoglycans.SDC4 is upregulated in ovarian carcinoma. | [164] |
Mesothelioma, fibrosarcoma | - | SDC4 expression | SDC4 is upregulated in mesothelioma and fibrosarcoma. | [165] |
Breast carcinoma samples from patients | - | SDC4 expression | SDC4 is associated with high histological grade and a negative estrogen receptor status in breast carcinoma. | [166] |
4T1 mouse breast cancer cells | - | bone metastasis formation | SDC4-silenced breast carcinoma cells have decreased ability to form bone metastasis in mice. | [102] |
JKT-1 human seminoma cell line, NTERA-2 human embryonal carcinoma cell line, NCCIT teratocarcinoma cell line | - | SDC4 expression—metastatic potential | Reduced SDC4 expression is associated with reduced metastatic potential in testicular germ cell tumors. | [167] |
Patients with primary high grade intramedullary osteosarcoma, with low grade central osteosarcoma, with osteoid osteoma and normal bone tissues | - | SDC4 expression—metastasis formation, tumor size | Increased SDC4 expression is associated with the formation of distant metastasis and increased tumor size in osteosarcoma. | [168] |
Renca (mouse), 786-O and Caki-2 (human) renal carcinoma cells | Wound scratch assay, Transwell assay | High SDC4 expression in renal cell carcinoma | High SDC4 expression determines increased patient survival in renal cell carcinoma. | [169] |
M5 human metastatic melanoma cells | Chemotaxis assay, wound scratch assay | FGF-2/SDC4 | FGF-2 regulates melanoma cell migration in a SDC4-dependent manner. | [177] |
MV3 human melanoma cell line | Wound scratch assay | Cyr61/SDC4 | Cyr61 is exocytosed by binding to SDC4. Cyr61 binds to and activates integrins, thus induce migration, metastasis formation and tumorigenicity. | [178] |
Rat embryonic fibroblasts (REFs), A375 melanoma cells, B16F10 melanoma cells, C57BL/6 mice | Transwell migration assay, lung metastasis model | Syntenin-1/SDC4 SDC4—inhibition of cancer-associated melanoma migration | SDC4 overexpression decreases melanoma cell migration in vitro and reduces the metastatic potential of melanoma in vivo. Syntenin-1 negatively regulates SDC4-mediated inhibition of cell migration and SDC4-mediated tumor suppression in melanoma. | [179] |
B16.F10 murine melanoma cells | Wound scratch assay | LysoPC/PKCδ/SDC4/PKCα/FAK | LysoPC C18:0 decreases the metastatic spread of melanoma cells. LysoPC activates PKCδ to phosphorylate SDC4 thereby deactivating PKCα and reducing FAK activity. | [180] |
MDA-MB-231 and MCF7 human breast cancer cells | 2D: wound scratch assay 3D: Matrigel and Collagen Type I | ADAMTS-15/SDC4 | Inhibition of mammary cancer cell migration by ADAMTS-15 requires SDC4. | [184] |
Human HaCat keratinocytes, A431 (human squamous skin epithelial) carcinoma cells, MCF10A (human mammary gland epithelial) cells | Wound scratch assay | HER1(EGFR)/α6β4 integrin/SDC4 | HER1-dependent activation of α6β4 integrin and α6β4 integrin-mediated cell invasion require SDC4. | [185] |
MDA-MB-231 breast adenocarcinoma cells | Cell invasion into 3D collagen gel | Integrin α2β1/MT1-MMP/SDCs–K-Ras mutant cell invasion | K-Ras mutant cells show increased expression of SDC1 and SDC4. MT1-MMP and α2β1 integrin promote invasive phenotype, SDCs reduce invasion into collagen matrices. | [186] |
MCF7, MDA-MB-435s and MDA-MB-231 breast cancer cells | Migration chamber (insert with polyethylene filter with 8 µM pores) | LL-37/SDC4LL-37/TRPV2/ic. Ca2+ LL-37/PI3K/AKT/motility | SDC4 is a receptor for LL-37 increasing Ca2+ levels via TRPV2 channels and increasing the motility of breast cancer cells via PI3K/AKT signaling. | [187] |
Non-metastatic rat mammary R37 cells, highly metastatic KP1 cells (R37 cells transfected with S100A4) | Wound scratch assay | SDC4/α5β1 integrin/PKCα—TG2 and S100A4-mediated cell migration | S100A4 mediates migration of tumor cells via SDC4 and α5β1 integrin-mediated PKCα activation. | [188] |
PANC-1 human pancreas adenocarcinoma cells, HT-29 human colon adenocarcinoma cells, MCF-7 and MDA-MB-231 human breast adenocarcinoma cells | - | NT4—SDC4 | The branched peptide NT4 inhibits cancer cell migration and FGF-induced invasion. NT4 binds to SDC4, the expression of SDC4 is upregulated breast cancer cells. | [189] |
MCF-7 (low metastatic ERa+), MDA-MB-231 (highly invasive ERa-) breast cancer cells | Wound scratch assay | IGFR/SDC4 expression | IGFR regulates the expression of SDC4 both in the presence and in the absence of E2 in breast cancer cells.IGFR inhibitors reduced the migration of MCF-7 cells but did not have a significant effect on MDA-MB-231 cells. | [190] |
C57Bl/6 mouse primary lymphatic endothelial cells, Lewis lung carcinoma cells, bone marrow–derived DCs (BMDCs) | Transwell migration assay, in vivo migration assay (BMDCs migration into lymph node), tumor growth studies | SDC4—dendritic cell maturation | SDC4-deficient mice exhibit impaired tumor growth and increased infiltration by mature dendritic cells. SDC4 is the dominant proteoglycan on dendritic cells. | [193] |
Primary lung fibroblasts | Boyden chamber, chemotaxis assay | CXCL10—SDC4 | In response to lung injury, the expression of SDC4 is increased. SDC4 directly interacts with CXCL10 and they inhibit the migration of fibroblasts. SDC4 is required for the inhibitory effect of CXCL10 during fibrosis. | [194] |
Human blood–derived monocytes, primary pulmonary endothelial cells, Lewis lung carcinoma cells (LLC1) | Boyden chamber, Transwell assay, spontaneous metastasis in mice | - | Increased expression of SDC4 is observed in endothelial cells after tumor cell seeding to the lungs. | [195] |
Mouse lung endothelial cells | Random migration assay; ex vivo C57BL/6 mice aortic ring assay | ADAMTS-1—MMP9—SDC4 | ADAMTS-1 modulates the cell surface expression of SDC4 via MMP9. ADAMTS-1 and SDC4 inhibit cell migration, whilst their inhibition increase angiogenesis. | [126] |
A549 human lung adenocarcinoma cells | Wound scratch assay, transwell chemotaxis assay | SDC4/Snail/TGFβ1-induced EMT | SDC4 promotes migration and invasion of lung adenocarcinoma cells. SDC4 positively regulates TGFβ1-induced EMT (via Snail), consequently promoting a more motile phenotype. | [174] |
A549 lung tumor epithelial cells | Wound scratch assay, matrigel invasion assay, in vivo lung tumor metastasis | ADAM17–SDC4 cleavage;SDC1—in vivo lung tumor metastasis | SDC1 tCFT was sufficient to induce lung metastasis formation in SCID mice, whilst SDC4 tCFT achieved as efficient wound closure as SDC1 tCFT. (tCTF = transmembrane C-terminal fragment) | [196] |
JAR choriocarcinoma cells | Modified Boyden-chamber chemotactic assay | CXCL12/SDC4 | SDC4 binds to CXCL12 and regulates CXCL12-mediated cell migration and invasion. SDC4 plays a role in the invasiveness of extravillous cytotrophoblast in moles. | [197] |
Huh7 human hepatoma cells | Bio-coat cell migration chambers, Matrigel invasion assay | SDF-1 (CXCL12)/ CXCR4/SDC4 | SDC4 is essential for SDF-1 (CXCL12) induced migration and invasion of hepatoma cells. | [198] |
Human cervix epitheloid carcinoma (HeLa) cells | Bio-coat cell migration chambers, Matrigel invasion assay | SDC4–SDF-1/CXCL12– PKCδ, JNK/SAPK | SDC4 plays a role in SDF-1/CXCL12-mediated cell invasion and chemotaxis. PKCδ and c-jun NH2-terminal kinase/stress-activated protein kinase (JNK/SAPK) are involved in the SDF-1/CXCL12-induced cell invasion. | [199] |
Human cervix epitheloid carcinoma (HeLa) cells | Wound scratch assay, Transwell assays | Calumenin–FN, SDC4, α5β1 integrin–ERK1/2 | Calumenin inhibits cell migration and tumor metastasis through FN, SDC4 and α5β1-integrin by the suppression of ERK1/2 signaling. | [200] |
Papillary thyroid cancer cells K1, BCPAP, TPC-1 and IHH-4, normal thyroid Nthy-ori3-1 cells | Transwell assay, wound scratch assay | SDC4—Wnt/β-catenin signaling pathway | SDC4-silencing decreased papillary thyroid cancer cell migration and invasion and represses EMT. Furthermore, SDC4-silencing suppresses Wnt/βcatenin signaling, thus promoting apoptosis. | [176] |
Huh7, HepG2and Hep3B human hepatoma cells | Bio-coat migration chambers, Matrigel invasion assay | RANTES/CCL5—SDC4 | SDC4 is essential in RANTES/CCL5-mediated hepatoma cell invasion and migration and its binding to the cell plasma membrane. | [201] |
8. Syndecan-4 and Non-Cancer Cell Migration
9. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
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Keller-Pinter, A.; Gyulai-Nagy, S.; Becsky, D.; Dux, L.; Rovo, L. Syndecan-4 in Tumor Cell Motility. Cancers 2021, 13, 3322. https://doi.org/10.3390/cancers13133322
Keller-Pinter A, Gyulai-Nagy S, Becsky D, Dux L, Rovo L. Syndecan-4 in Tumor Cell Motility. Cancers. 2021; 13(13):3322. https://doi.org/10.3390/cancers13133322
Chicago/Turabian StyleKeller-Pinter, Aniko, Szuzina Gyulai-Nagy, Daniel Becsky, Laszlo Dux, and Laszlo Rovo. 2021. "Syndecan-4 in Tumor Cell Motility" Cancers 13, no. 13: 3322. https://doi.org/10.3390/cancers13133322