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Article ; Online: Chorioallantoic Membrane Microtumor Model to Study the Mechanisms of Tumor Angiogenesis, Vascular Permeability, and Tumor Cell Intravasation.

Deryugina, Elena I

Methods in molecular biology (Clifton, N.J.)

2016 Volume 1430, Page(s) 283–298

Abstract: The mechanisms governing the development of angiogenic blood vessels, which not only deliver the nutrients to growing tumors but also provide the conduits for tumor cell dissemination, are still not fully resolved. The model systems based on the grafting ...

Abstract	The mechanisms governing the development of angiogenic blood vessels, which not only deliver the nutrients to growing tumors but also provide the conduits for tumor cell dissemination, are still not fully resolved. The model systems based on the grafting of human tumor cells onto the chorioallantoic membrane (CAM) of the chick embryo offer several advantages to study complex processes underlying tumor angiogenesis and tumor cell dissemination. In particular, the CAM model described here allows for investigation of multiple microtumors as independent entities, thereby greatly facilitating quantification and statistical analyses of tumor neovascularization and cancer spreading. This CAM microtumor system was designed specifically to measure the level of tumor cell intravasation in combination with quantitative analyses of the microarchitecture and permeability of the intratumoral angiogenic blood vessels. By using this newly established microtumor model we have demonstrated the functional involvement of tumor matrix metalloproteinase-1 (MMP-1) and epidermal growth factor receptor (EGFR) in regulating the development of a distinct angiogenic vasculature capable of sustaining tumor cell intravasation and metastasis.
Language	English
Publishing date	2016
Publishing country	United States
Document type	Journal Article
ISSN	1940-6029
ISSN (online)	1940-6029
DOI	10.1007/978-1-4939-3628-1_19
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Article ; Online: Intratumoral Cancer Cell Intravasation Can Occur Independent of Invasion into the Adjacent Stroma.

Deryugina, Elena I / Kiosses, William B

Cell reports

2017 Volume 19, Issue 3, Page(s) 601–616

Abstract: Intravasation, active entry of cancer cells into the circulation, is often considered to be a relatively late event in tumor development occurring after stromal invasion. Here, we provide evidence that intravasation can be initiated early during tumor ... ...

Abstract	Intravasation, active entry of cancer cells into the circulation, is often considered to be a relatively late event in tumor development occurring after stromal invasion. Here, we provide evidence that intravasation can be initiated early during tumor development and proceed in parallel to or independent of tumor invasion into surrounding stroma. By applying direct and unbiased intravasation-scoring methods to two histologically distinct human cancer types in live-animal models, we demonstrate that intravasation takes place almost exclusively within the tumor core, involves intratumoral vasculature, and does not involve vasculotropic cancer cells invading tumor-adjacent stroma and migrating along tumor-converging blood vessels. Highlighting an additional role for EGFR in cancer, we find that EGFR is required for the development of an intravasation-sustaining intratumoral vasculature. Intratumoral localization of intravasation supports the notion that overt metastases in cancer patients could be initiated much earlier during cancer progression than appreciated within conventional clinical tumor staging systems.
MeSH term(s)	Animals ; Cell Line, Tumor ; Cell Movement ; Chick Embryo ; Disease Models, Animal ; Ear/pathology ; Green Fluorescent Proteins/metabolism ; Humans ; Hypoxia/pathology ; Mice, Inbred C57BL ; Mice, Inbred NOD ; Mice, SCID ; Neoplasm Invasiveness ; Neoplasm Metastasis ; Neoplasms/pathology ; Neovascularization, Pathologic ; Permeability ; Receptor, Epidermal Growth Factor/metabolism ; Stromal Cells/pathology
Chemical Substances	Green Fluorescent Proteins (147336-22-9) ; Receptor, Epidermal Growth Factor (EC 2.7.10.1)
Language	English
Publishing date	2017-04-18
Publishing country	United States
Document type	Journal Article
ZDB-ID	2649101-1
ISSN	2211-1247 ; 2211-1247
ISSN (online)	2211-1247
ISSN	2211-1247
DOI	10.1016/j.celrep.2017.03.064
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Article ; Online: Tumor angiogenesis: MMP-mediated induction of intravasation- and metastasis-sustaining neovasculature.

Deryugina, Elena I / Quigley, James P

Matrix biology : journal of the International Society for Matrix Biology

2015 Volume 44-46, Page(s) 94–112

Abstract: Metastasis is a distinct stage of cancer progression that requires the development of angiogenic blood vessels serving as conduits for tumor cell dissemination. An accumulated body of evidence indicates that metastasis-supporting neovasculature should ... ...

Abstract	Metastasis is a distinct stage of cancer progression that requires the development of angiogenic blood vessels serving as conduits for tumor cell dissemination. An accumulated body of evidence indicates that metastasis-supporting neovasculature should possess certain structural characteristics allowing for the process of tumor cell intravasation, an active entry of cancer cells into the vessel interior. It appears that the development of tumor vessels with lumens of a distinctive size and support of these vessels by a discontinuous pericyte coverage constitute critical microarchitectural requirements to: (a) provide accessible points for vessel wall penetration by primary tumor cells; (b) provide enough lumen space for a tumor cell or cell aggregate upon intravasation; and (c) allow for sufficient rate of blood flow to carry away intravasated cells from the primary tumor to the next, proximal or distal site. This review will primarily focus on the functional roles of matrix metalloproteinases (MMPs), which catalytically trigger the development of an intravasation-sustaining neovasculature at the early stages of tumor growth and are also required for the maintenance of a metastasis-supporting state of blood vessels at later stages of cancer progression.
MeSH term(s)	Animals ; Humans ; Matrix Metalloproteinases/metabolism ; Neoplasm Metastasis ; Neoplasms/blood supply ; Neoplasms/metabolism ; Neoplasms/pathology ; Neovascularization, Pathologic/enzymology ; Vascular Endothelial Growth Factor A/metabolism
Chemical Substances	Vascular Endothelial Growth Factor A ; Matrix Metalloproteinases (EC 3.4.24.-)
Language	English
Publishing date	2015-05
Publishing country	Netherlands
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	1183793-7
ISSN	1569-1802 ; 0945-053X
ISSN (online)	1569-1802
ISSN	0945-053X
DOI	10.1016/j.matbio.2015.04.004
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Article ; Online: Combating angiogenesis early: potential of targeting tumor-recruited neutrophils in cancer therapy.

Quigley, James P / Deryugina, Elena I

Future oncology (London, England)

2012 Volume 8, Issue 1, Page(s) 5–8

MeSH term(s)	Angiogenesis Inhibitors/pharmacology ; Angiogenesis Inhibitors/therapeutic use ; Animals ; Humans ; Interleukin-8/metabolism ; Neoplasms/blood supply ; Neoplasms/drug therapy ; Neoplasms/pathology ; Neovascularization, Pathologic/drug therapy ; Neutrophils/drug effects ; Neutrophils/metabolism ; Receptors, Interleukin-8A/antagonists & inhibitors ; Receptors, Interleukin-8A/metabolism ; Receptors, Interleukin-8B/antagonists & inhibitors ; Receptors, Interleukin-8B/metabolism
Chemical Substances	Angiogenesis Inhibitors ; CXCL8 protein, human ; Interleukin-8 ; Receptors, Interleukin-8A ; Receptors, Interleukin-8B
Language	English
Publishing date	2012-01-10
Publishing country	England
Document type	Editorial
ZDB-ID	2274956-1
ISSN	1744-8301 ; 1479-6694
ISSN (online)	1744-8301
ISSN	1479-6694
DOI	10.2217/fon.11.133
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Zs.A 6478: Show issues

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Article ; Online: Intratumoral Cancer Cell Intravasation Can Occur Independent of Invasion into the Adjacent Stroma

Elena I. Deryugina / William B. Kiosses

Cell Reports, Vol 19, Iss 3, Pp 601-

2017 Volume 616

Abstract: ... Deryugina and Kiosses investigate the localization of intravasation within primary tumors. They find ...

Abstract	Summary: Intravasation, active entry of cancer cells into the circulation, is often considered to be a relatively late event in tumor development occurring after stromal invasion. Here, we provide evidence that intravasation can be initiated early during tumor development and proceed in parallel to or independent of tumor invasion into surrounding stroma. By applying direct and unbiased intravasation-scoring methods to two histologically distinct human cancer types in live-animal models, we demonstrate that intravasation takes place almost exclusively within the tumor core, involves intratumoral vasculature, and does not involve vasculotropic cancer cells invading tumor-adjacent stroma and migrating along tumor-converging blood vessels. Highlighting an additional role for EGFR in cancer, we find that EGFR is required for the development of an intravasation-sustaining intratumoral vasculature. Intratumoral localization of intravasation supports the notion that overt metastases in cancer patients could be initiated much earlier during cancer progression than appreciated within conventional clinical tumor staging systems. : Deryugina and Kiosses investigate the localization of intravasation within primary tumors. They find that the majority of intravasation events occur within the tumor core and not at the invasive edge within tumor outgrowths into adjacent stroma in the models examined. Mechanistically, EGFR appears to impact intratumoral intravasation by regulating development of a fully interconnected angiogenic vasculature. Keywords: cancer metastasis, cell intravasation, tumor invasion, stromal invasion, tumor cell migration, tumor angiogenesis, EGFR, animal models of cancer, mouse ear tumor model, chorioallantoic membrane model
Keywords	Biology (General) ; QH301-705.5
Subject code	610
Language	English
Publishing date	2017-04-01T00:00:00Z
Publisher	Elsevier
Document type	Article ; Online
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Article ; Online: Cell surface remodeling by plasmin: a new function for an old enzyme.

Deryugina, Elena I / Quigley, James P

Journal of biomedicine & biotechnology

2012 Volume 2012, Page(s) 564259

Abstract: Plasmin, one of the most potent and reactive serine proteases, is involved in various physiological processes, including embryo development, thrombolysis, wound healing and cancer progression. The proteolytic activity of plasmin is tightly regulated ... ...

Abstract	Plasmin, one of the most potent and reactive serine proteases, is involved in various physiological processes, including embryo development, thrombolysis, wound healing and cancer progression. The proteolytic activity of plasmin is tightly regulated through activation of its precursor, plasminogen, only at specific times and in defined locales as well as through inhibition of active plasmin by its abundant natural inhibitors. By exploiting the plasminogen activating system and overexpressing distinct components of the plasminogen activation cascade, such as pro-uPA, uPAR and plasminogen receptors, malignant cells can enhance the generation of plasmin which in turn, modifies the tumor microenvironment to sustain cancer progression. While plasmin-mediated degradation and modification of extracellular matrix proteins, release of growth factors and cytokines from the stroma as well as activation of several matrix metalloproteinase zymogens, all have been a focus of cancer research studies for decades, the ability of plasmin to cleave transmembrane molecules and thereby to generate functionally important cleaved products which induce outside-in signal transduction, has just begun to receive sufficient attention. Herein, we highlight this relatively understudied, but important function of the plasmin enzyme as it is generated de novo at the interface between cross-talking cancer and host cells.
MeSH term(s)	Animals ; Cell Communication/physiology ; Cell Membrane/metabolism ; Fibrinolysin/metabolism ; Humans ; Models, Biological
Chemical Substances	Fibrinolysin (EC 3.4.21.7)
Language	English
Publishing date	2012-10-14
Publishing country	United States
Document type	Journal Article ; Review
ZDB-ID	2052552-7
ISSN	1110-7251 ; 1110-7243
ISSN (online)	1110-7251
ISSN	1110-7243
DOI	10.1155/2012/564259
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Zs.A 5540: Show issues

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Article ; Online: EGFR regulates the development and microarchitecture of intratumoral angiogenic vasculature capable of sustaining cancer cell intravasation.

Minder, Petra / Zajac, Ewa / Quigley, James P / Deryugina, Elena I

Neoplasia (New York, N.Y.)

2015 Volume 17, Issue 8, Page(s) 634–649

Abstract: Many malignant characteristics of cancer cells are regulated through pathways induced by the tyrosine kinase activity of the epidermal growth factor receptor (EGFR). Herein, we show that besides directly affecting the biology of cancer cells per se, EGFR ...

Abstract	Many malignant characteristics of cancer cells are regulated through pathways induced by the tyrosine kinase activity of the epidermal growth factor receptor (EGFR). Herein, we show that besides directly affecting the biology of cancer cells per se, EGFR also regulates the primary tumor microenvironment. Specifically, our findings demonstrate that both the expression and signaling activity of EGFR are required for the induction of a distinct intratumoral vasculature capable of sustaining tumor cell intravasation, a critical rate-limiting step in the metastatic cascade. An intravasation-sustaining mode of intratumoral angiogenic vessels depends on high levels of tumor cell EGFR and the interplay between EGFR-regulated production of interleukin 8 by tumor cells, interleukin-8-induced influx of tumor-infiltrating neutrophils delivering their unique matrix metalloproteinase-9, and neutrophil matrix metalloproteinase-9-dependent release of the vascular permeability and endothelial growth factor, VEGF. Our data indicate that through VEGF-mediated disruption of endothelial layer integrity and increase of intratumoral vasculature permeability, EGFR activity significantly facilitates active intravasation of cancer cells. Therefore, this study unraveled an important but overlooked function of EGFR in cancer, namely, its ability to create an intravasation-sustaining microenvironment within the developing primary tumor by orchestrating several interrelated processes required for the initial steps of cancer metastasis through vascular routes. Our findings also suggest that EGFR-targeted therapies might be more effective when implemented in cancer patients with early-staged primary tumors containing a VEGF-dependent angiogenic vasculature. Accordingly, early EGFR inhibition combined with various anti-VEGF approaches could synergistically suppress tumor cell intravasation through inhibiting the highly permeable angiogenic vasculature induced by EGFR-overexpressing aggressive cancer cells.
MeSH term(s)	Animals ; Blotting, Western ; Cell Line, Tumor ; Chick Embryo ; Chorioallantoic Membrane/blood supply ; Chorioallantoic Membrane/metabolism ; Chorioallantoic Membrane/pathology ; ErbB Receptors/genetics ; ErbB Receptors/metabolism ; Gene Expression Regulation, Neoplastic ; Humans ; Matrix Metalloproteinase 9/metabolism ; Microscopy, Fluorescence ; Neoplasm Invasiveness ; Neoplasm Metastasis ; Neoplasm Transplantation ; Neoplasms/blood supply ; Neoplasms/genetics ; Neoplasms/metabolism ; Neovascularization, Pathologic/genetics ; Neovascularization, Pathologic/metabolism ; RNA Interference ; Reverse Transcriptase Polymerase Chain Reaction ; Tumor Microenvironment/genetics ; Vascular Endothelial Growth Factor A/genetics ; Vascular Endothelial Growth Factor A/metabolism
Chemical Substances	Vascular Endothelial Growth Factor A ; EGFR protein, human (EC 2.7.10.1) ; ErbB Receptors (EC 2.7.10.1) ; Matrix Metalloproteinase 9 (EC 3.4.24.35)
Language	English
Publishing date	2015-09-28
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	1483840-0
ISSN	1476-5586 ; 1522-8002
ISSN (online)	1476-5586
ISSN	1522-8002
DOI	10.1016/j.neo.2015.08.002
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Zs.A 5203: Show issues

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Article: Pleiotropic roles of matrix metalloproteinases in tumor angiogenesis: contrasting, overlapping and compensatory functions.

Deryugina, Elena I / Quigley, James P

Biochimica et biophysica acta

2009 Volume 1803, Issue 1, Page(s) 103–120

Abstract: A number of extensive reviews are available discussing the roles of MMPs in various aspects of cancer progression from benign tumor formation to overt cancer present with deadly metastases. This review will focus specifically on the evidence functionally ...

Abstract	A number of extensive reviews are available discussing the roles of MMPs in various aspects of cancer progression from benign tumor formation to overt cancer present with deadly metastases. This review will focus specifically on the evidence functionally linking the MMPs and tumor-induced angiogenesis in various in vivo models. Emphasis has been placed on the cellular origin of the MMPs in tumor tissue, the requirement of proMMP activation and the resulting proteolytic activity for the induction and progression of tumor angiogenesis, and the pleiotropic roles for some of the MMPs. The functional mechanisms of the angiogenic MMPs are discussed as well as their catalytic detection in complex biological systems. In addition, the contribution of active MMPs to metastatic spread and establishment of secondary metastasis will be discussed in view of the findings indicating that MMPs are involved in the preparation of pre-metastatic niches. Finally, the most recent evidence, indicating the pro-metastatic consequences of anti-angiogenic therapies employing MMP inhibitors will be presented as examples highlighting possible outcomes of interfering with the pleiotropic nature of the MMP functionality.
MeSH term(s)	Animals ; Enzyme Activation ; Humans ; Matrix Metalloproteinases/metabolism ; Neoplasms/blood supply ; Neoplasms/enzymology ; Neoplasms/pathology ; Neovascularization, Pathologic/enzymology ; Neovascularization, Pathologic/therapy ; Protein Processing, Post-Translational ; Stem Cells/cytology
Chemical Substances	Matrix Metalloproteinases (EC 3.4.24.-)
Language	English
Publishing date	2009-10-02
Publishing country	Netherlands
Document type	Journal Article ; Review
ZDB-ID	60-7
ISSN	1879-2596 ; 1879-260X ; 1872-8006 ; 1879-2642 ; 1879-2618 ; 1879-2650 ; 0006-3002 ; 0005-2728 ; 0005-2736 ; 0304-4165 ; 0167-4838 ; 1388-1981 ; 0167-4889 ; 0167-4781 ; 0304-419X ; 1570-9639 ; 0925-4439 ; 1874-9399
ISSN (online)	1879-2596 ; 1879-260X ; 1872-8006 ; 1879-2642 ; 1879-2618 ; 1879-2650
ISSN	0006-3002 ; 0005-2728 ; 0005-2736 ; 0304-4165 ; 0167-4838 ; 1388-1981 ; 0167-4889 ; 0167-4781 ; 0304-419X ; 1570-9639 ; 0925-4439 ; 1874-9399
DOI	10.1016/j.bbamcr.2009.09.017
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Article ; Online: Chapter 2. Chick embryo chorioallantoic membrane models to quantify angiogenesis induced by inflammatory and tumor cells or purified effector molecules.

Deryugina, Elena I / Quigley, James P

Methods in enzymology

2008 Volume 444, Page(s) 21–41

Abstract: Angiogenesis plays a critical role in many normal physiological processes as well as in tumor neovascularization associated with cancer progression. Among various animal model systems designed to study the mechanisms underlying angiogenesis, chick embryo ...

Abstract	Angiogenesis plays a critical role in many normal physiological processes as well as in tumor neovascularization associated with cancer progression. Among various animal model systems designed to study the mechanisms underlying angiogenesis, chick embryo models have been useful tools in analyzing the angiogenic potential of purified factors and intact cells. The chorioallantoic membrane (CAM), a specialized, highly vascularized tissue of the avian embryo, serves as an ideal indicator of the anti- or pro-angiogenic properties of test compounds. In this chapter, we describe a number basic chick embryo CAM models of angiogenesis. A special emphasis is on the model system employing three-dimensional (3D) collagen grafts planted on the CAM, referred herein as onplants. This collagen onplant model allows for unambiguous quantification of angiogenesis and also for in-depth analysis of the cellular and biochemical mechanisms by which specific cells of different origin or purified effector molecules induce or inhibit the angiogenic process.
MeSH term(s)	Animals ; Chick Embryo ; Chorioallantoic Membrane/blood supply ; Chorioallantoic Membrane/metabolism ; Collagen/metabolism ; Disease Models, Animal ; Humans ; Inflammation/metabolism ; Neoplasms/blood supply ; Neoplasms/metabolism ; Neovascularization, Pathologic/metabolism
Chemical Substances	Collagen (9007-34-5)
Language	English
Publishing date	2008-11-14
Publishing country	United States
Document type	Journal Article
ISSN	1557-7988
ISSN (online)	1557-7988
DOI	10.1016/S0076-6879(08)02802-4
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Article: Chick embryo chorioallantoic membrane model systems to study and visualize human tumor cell metastasis.

Deryugina, Elena I / Quigley, James P

Histochemistry and cell biology

2008 Volume 130, Issue 6, Page(s) 1119–1130

Abstract: Since their introduction almost a century ago, chick embryo model systems involving the technique of chorioallantoic grafting have proved invaluable in the in vivo studies of tumor development and angiogenesis and tumor cell dissemination. The ability of ...

Abstract	Since their introduction almost a century ago, chick embryo model systems involving the technique of chorioallantoic grafting have proved invaluable in the in vivo studies of tumor development and angiogenesis and tumor cell dissemination. The ability of the chick embryo's chorioallantoic membrane (CAM) to efficiently support the growth of inoculated xenogenic tumor cells greatly facilitates analysis of human tumor cell metastasis. During spontaneous metastasis, the highly vascularized CAM sustains rapid tumor formation within several days following cell grafting. The dense capillary network of the CAM also serves as a repository of aggressive tumor cells that escaped from the primary tumor and intravasated into the host vasculature. This spontaneous metastasis setting provides a unique experimental model to study in vivo the intravasation step of the metastatic cascade. During experimental metastasis when tumor cells are inoculated intravenously, the CAM capillary system serves as a place for initial arrest and then, for tumor cell extravasation and colonization. The tissue composition and accessibility of the CAM for experimental interventions makes chick embryo CAM systems attractive models to follow the fate and visualize microscopically the behavior of grafted tumor cells in both spontaneous and experimental metastasis settings.
MeSH term(s)	Animals ; Cell Line, Tumor ; Cell Movement ; Cell Proliferation ; Chick Embryo ; Chorioallantoic Membrane/blood supply ; Chorioallantoic Membrane/immunology ; Humans ; Microscopy/methods ; Models, Animal ; Monocytes/immunology ; Neoplasm Invasiveness ; Neoplasm Metastasis ; Neoplasms/blood supply ; Neoplasms/immunology ; Neoplasms/pathology ; Neoplastic Cells, Circulating/pathology ; Neovascularization, Physiologic
Language	English
Publishing date	2008-11-13
Publishing country	Germany
Document type	Journal Article ; Review
ZDB-ID	1222930-1
ISSN	1432-119X ; 0948-6143 ; 0301-5564
ISSN (online)	1432-119X
ISSN	0948-6143 ; 0301-5564
DOI	10.1007/s00418-008-0536-2
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