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The extracellular matrix in tumor progression and metastasis

  • Johannes A. EbleEmail author
  • Stephan Niland
Review

Abstract

The extracellular matrix (ECM) constitutes the scaffold of tissues and organs. It is a complex network of extracellular proteins, proteoglycans and glycoproteins, which form supramolecular aggregates, such as fibrils and sheet-like networks. In addition to its biochemical composition, including the covalent intermolecular cross-linkages, the ECM is also characterized by its biophysical parameters, such as topography, molecular density, stiffness/rigidity and tension. Taking these biochemical and biophysical parameters into consideration, the ECM is very versatile and undergoes constant remodeling. This review focusses on this remodeling of the ECM under the influence of a primary solid tumor mass. Within this tumor stroma, not only the cancer cells but also the resident fibroblasts, which differentiate into cancer-associated fibroblasts (CAFs), modify the ECM. Growth factors and chemokines, which are tethered to and released from the ECM, as well as metabolic changes of the cells within the tumor bulk, add to the tumor-supporting tumor microenvironment. Metastasizing cancer cells from a primary tumor mass infiltrate into the ECM, which variably may facilitate cancer cell migration or act as barrier, which has to be proteolytically breached by the infiltrating tumor cell. The biochemical and biophysical properties therefore determine the rates and routes of metastatic dissemination. Moreover, primed by soluble factors of the primary tumor, the ECM of distant organs may be remodeled in a way to facilitate the engraftment of metastasizing cancer cells. Such premetastatic niches are responsible for the organotropic preference of certain cancer entities to colonize at certain sites in distant organs and to establish a metastasis. Translational application of our knowledge about the cancer-primed ECM is sparse with respect to therapeutic approaches, whereas tumor-induced ECM alterations such as increased tissue stiffness and desmoplasia, as well as breaching the basement membrane are hallmark of malignancy and diagnostically and histologically harnessed.

Keywords

Extracellular matrix Tumor progression Tumor microenvironment Cancer-associated fibroblast Metastatic cascade Cell migration Cell infiltration Invadopodia Metastatic niche Metastasis 

Abbreviations

ADAMTS

A disintegrin and metalloproteinase with thrombospondin motifs

CAF

Cancer-associated fibroblast

CCN

CTGF, Cyr61, and NOV

CTGF

Connective tissue growth

CXCL12 = SDF.1

C-X-X chemokine 12 = stroma cell-derived factor-1

Cyr61

Cysteine-rich angiogenic protein 61

DDR

Discoidin domain receptor

ECM

Extracellular matrix

ED-A, -B

Extra domain-A, -B

EGF-L

Epidermal growth factor-like

EGFR

Epidermal growth factor receptor

Ela-2

Neutrophil elastase

ERC

Elastin receptor complex

Endo180

Endocytic receptor 180 = C-type mannose receptor 2

FNFr

Fibronectin fragment

GAG

Glycosaminoglycan

GPVI

Glycoprotein VI

HGF

Hepatocyte growth factor

IGF-1R

Insulin-like growth factor 1 receptor

IL

Interleukin

KRAS

Kirsten rat sarcoma oncogene

LAIR-1

Leukocyte-associated immunoglobulin-like receptor 1

LG3, 4

Laminin globular domain 3, 4

LOX/LOXL

Lysyl oxidase/lysyl oxidase-like

LRP6

Low-density lipoprotein receptor-related protein 6

LY75

Lymphocyte antigen 75 (CD205, DEC-205)

MET

Mesenchymal-epithelial transition factor proto-oncogene, hepatocyte growth factor receptor, HGFR

MMP

Matrix metalloproteinase

MR

Mannose receptor

MuSK

Muscle-specific kinase

NC1

Non-collagenous domain 1

NCAM-L1

Neural cell adhesion molecule L1

NOV

Nephroblastoma overexpressed gene

NrCAM

Neuron-glial related cell adhesion molecule

PAR

Protease-activated receptor

PD-1/PD-L1

Programmed death-1/programmed death ligand-1

PDGF

Platelet-derived growth factor

PLA2R

Phospholipase-A2-receptor

Sema3F

Semaphorin 3F

SIBLING

Small integrin-binding ligand-N-linked glycoprotein

SLRP

Small leucine-rich proteoglycan

SPARC

Secreted protein, acid and rich in cysteine

TAM

Tumor-associated macrophage

TF

Tissue factor

TLR-2, -4

Toll-like receptor-2, -4

TME

Tumor microenvironment

TGF-β

Transforming growth factor-β

Treg

Regulatory T cell

VEGF

Vascular endothelial growth factor

VEGFR2

Vascular endothelial growth factor receptor 2

VM

Vasculogenic mimicry

Notes

Funding

To study different aspect of tumor biology, J.A.E. receives financial support from Deutsche Forschungsgemeinschaft (SFB1009 A09) (MMP14 in invadopodia), from the People Programme (Marie Curie Actions) of the European Union’s Seventh Framework Programme FP7/2007-2013/under the REA Grant agreement n° [316610] (CAF differentiation in tumor stroma), and from the Wilhelm Sander Stiftung (grant:2016.113.1 to J.A.E.) (Interactions between tumor and endothelial cells).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

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© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Institute of Physiological Chemistry and PathobiochemistryUniversity of MünsterMünsterGermany

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