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Article ; Online: Aligned forces: Origins and mechanisms of cancer dissemination guided by extracellular matrix architecture.

Ray, Arja / Provenzano, Paolo P

2021 Volume 72, Page(s) 63–71

Abstract: Organized extracellular matrix (ECM), in the form of aligned architectures, is a critical mediator of directed cancer cell migration by contact guidance, leading to metastasis in solid tumors. Current models suggest anisotropic force generation through ... ...

Abstract	Organized extracellular matrix (ECM), in the form of aligned architectures, is a critical mediator of directed cancer cell migration by contact guidance, leading to metastasis in solid tumors. Current models suggest anisotropic force generation through the engagement of key adhesion and cytoskeletal complexes drives contact-guided migration. Likewise, disrupting the balance between cell-cell and cell-ECM forces, driven by ECM engagement for cells at the tumor-stromal interface, initiates and drives local invasion. Furthermore, processes such as traction forces exerted by cancer and stromal cells, spontaneous reorientation of matrix-producing fibroblasts, and direct binding of ECM modifying proteins lead to the emergence of collagen alignment in tumors. Thus, as we obtain a deeper understanding of the origins of ECM alignment and the mechanisms by which it is maintained to direct invasion, we are poised to use the new paradigm of stroma-targeted therapies to disrupt this vital axis of disease progression in solid tumors.
MeSH term(s)	Cell Communication ; Cell Line, Tumor ; Cell Movement ; Collagen ; Extracellular Matrix ; Neoplasms
Chemical Substances	Collagen (9007-34-5)
Language	English
Publishing date	2021-06-27
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	1026381-0
ISSN	1879-0410 ; 0955-0674
ISSN (online)	1879-0410
ISSN	0955-0674
DOI	10.1016/j.ceb.2021.05.004
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Article: Critical role of CD206+ macrophages in organizing anti-tumor immunity.

Ray, Arja / Hu, Kenneth H / Kersten, Kelly / Kuhn, Nicholas F / Samad, Bushra / Combes, Alexis J / Krummel, Matthew F

bioRxiv : the preprint server for biology

2023

Abstract: Tumor-associated macrophages (TAMs) are frequently and simplistically categorized as immunosuppressive, and one molecule prominently used to highlight their so-called 'M2' state is the surface protein CD206. However, direct evidence of the impact of ... ...

Abstract	Tumor-associated macrophages (TAMs) are frequently and simplistically categorized as immunosuppressive, and one molecule prominently used to highlight their so-called 'M2' state is the surface protein CD206. However, direct evidence of the impact of macrophages remains impaired by the lack of sufficiently penetrant and specific tools to manipulate them in vivo. We thus made a novel conditional CD206 knock-in mouse to specifically visualize and/or deplete these TAMs. Early depletion of CD206+ macrophages and monocytes (here, 'MonoMacs') strikingly led to an indirect loss of a key anti-tumor network of NK cells, conventional type I dendritic cells (cDC1) and CD8 T cells. Among myeloid cells, we found that the CD206+ TAMs are the primary producers of CXCL9, the well-established chemoattractant for CXCR3-expressing NK and CD8 T cells. In contrast, a population of stress-responsive TAMs ("Hypoxic" or
Language	English
Publishing date	2023-11-02
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.10.31.560822
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Article: Multimodal identification of rare potent effector CD8 T cells in solid tumors.

Ray, Arja / Bassette, Molly / Hu, Kenneth H / Pass, Lomax F / Samad, Bushra / Combes, Alexis / Johri, Vrinda / Davidson, Brittany / Hernandez, Grace / Zaleta-Linares, Itzia / Krummel, Matthew F

bioRxiv : the preprint server for biology

2023

Abstract: Antitumor immunity is driven by CD8 T cells, yet we lack signatures for the exceptional effectors in tumors, amongst the vast majority of CD8 T cells undergoing exhaustion. By leveraging the measurement of a canonical T cell activation protein (CD69) ... ...

Abstract	Antitumor immunity is driven by CD8 T cells, yet we lack signatures for the exceptional effectors in tumors, amongst the vast majority of CD8 T cells undergoing exhaustion. By leveraging the measurement of a canonical T cell activation protein (CD69) together with its RNA (
Language	English
Publishing date	2023-09-28
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.09.26.559470
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Article ; Online: Visualizing Spatial and Stoichiometric Barriers to Bispecific T-Cell Engager Efficacy.

You, Ran / Artichoker, Jordan / Ray, Arja / Gonzalez Velozo, Hugo / Rock, Dan A / Conner, Kip P / Krummel, Matthew F

Cancer immunology research

2022 Volume 10, Issue 6, Page(s) 698–712

Abstract: Bispecific T-cell engager (BiTE) molecules are biologic T cell-directing immunotherapies. Blinatumomab is approved for treatment of B-cell malignancies, but BiTE molecule development in solid tumors has been more challenging. Here, we employed intravital ...

Abstract	Bispecific T-cell engager (BiTE) molecules are biologic T cell-directing immunotherapies. Blinatumomab is approved for treatment of B-cell malignancies, but BiTE molecule development in solid tumors has been more challenging. Here, we employed intravital imaging to characterize exposure and pharmacodynamic response of an anti-muCD3/anti-huEGFRvIII mouse surrogate BiTE molecule in EGFR variant III (EGFRvIII)-positive breast tumors implanted within immunocompetent mice. Our study revealed heterogeneous temporal and spatial dynamics of BiTE molecule extravasation into solid tumors, highlighting physical barriers to BiTE molecule function. We also discovered that high, homogeneous EGFRvIII expression on cancer cells was necessary for a BiTE molecule to efficiently clear tumors. In addition, we found that resident tumor-infiltrating lymphocytes (TIL) were sufficient for optimal tumor killing only at high BiTE molecule dosage, whereas inclusion of peripheral T-cell recruitment was synergistic at moderate to low dosages. We report that deletion of stimulatory conventional type I DCs (cDC1) diminished BiTE molecule-induced T-cell activation and tumor clearance, suggesting that in situ antigen-presenting cell (APC) engagements modulate the extent of BiTE molecule efficacy. In summary, our work identified multiple requirements for optimal BiTE molecule efficacy in solid tumors, providing insights that could be harnessed for solid cancer immunotherapy development.
MeSH term(s)	Animals ; Antibodies, Bispecific/pharmacology ; Antibodies, Bispecific/therapeutic use ; B-Lymphocytes ; Immunotherapy/methods ; Lymphocyte Activation ; Mice ; Neoplasms/pathology ; T-Lymphocytes
Chemical Substances	Antibodies, Bispecific
Language	English
Publishing date	2022-04-11
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	2732489-8
ISSN	2326-6074 ; 2326-6066
ISSN (online)	2326-6074
ISSN	2326-6066
DOI	10.1158/2326-6066.CIR-21-0594
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Zs.A 7022: Show issues

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Article ; Online: Cancer Stem Cell Migration in Three-Dimensional Aligned Collagen Matrices.

Ray, Arja / Morford, Rachel K / Provenzano, Paolo P

Current protocols in stem cell biology

2018 Volume 46, Issue 1, Page(s) e57

Abstract: Cell migration is strongly influenced by the organization of the surrounding 3-D extracellular matrix. In particular, within fibrous solid tumors, carcinoma cell invasion may be directed by patterns of aligned collagen in the extra-epithelial space. Thus, ...

Abstract	Cell migration is strongly influenced by the organization of the surrounding 3-D extracellular matrix. In particular, within fibrous solid tumors, carcinoma cell invasion may be directed by patterns of aligned collagen in the extra-epithelial space. Thus, studying the interactions of heterogeneous populations of cancer cells that include the stem/progenitor-like cancer stem cell subpopulation and aligned collagen networks is critical to our understanding of carcinoma dissemination. Here, we describe a robust method to generate aligned collagen matrices in vitro that mimic in vivo fiber organization. Subsequently, a protocol is presented for seeding aligned matrices with distinct carcinoma cell subpopulations and performing live cell imaging and quantitative analysis of cell migration. Together, the engineered constructs and the imaging techniques laid out here provide a platform to study cancer stem cell migration in 3-D anisotropic collagen with real-time visualization of cellular interactions with the fibrous matrix. © 2018 by John Wiley & Sons, Inc.
MeSH term(s)	Animals ; Cell Culture Techniques/methods ; Cell Line, Tumor ; Cell Movement/drug effects ; Cell Tracking ; Collagen/pharmacology ; Extracellular Matrix/drug effects ; Extracellular Matrix/metabolism ; Fibroblasts/cytology ; Fibroblasts/drug effects ; Neoplastic Stem Cells/pathology ; Rats ; Time-Lapse Imaging
Chemical Substances	Collagen (9007-34-5)
Language	English
Publishing date	2018-05-24
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ISSN	1938-8969
ISSN (online)	1938-8969
DOI	10.1002/cpsc.57
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Spatiotemporal co-dependency between macrophages and exhausted CD8

Kersten, Kelly / Hu, Kenneth H / Combes, Alexis J / Samad, Bushra / Harwin, Tory / Ray, Arja / Rao, Arjun Arkal / Cai, En / Marchuk, Kyle / Artichoker, Jordan / Courau, Tristan / Shi, Quanming / Belk, Julia / Satpathy, Ansuman T / Krummel, Matthew F

Cancer cell

2022 Volume 40, Issue 6, Page(s) 624–638.e9

Abstract: T cell exhaustion is a major impediment to antitumor immunity. However, it remains elusive how other immune cells in the tumor microenvironment (TME) contribute to this dysfunctional state. Here, we show that the biology of tumor-associated macrophages ( ... ...

Abstract	T cell exhaustion is a major impediment to antitumor immunity. However, it remains elusive how other immune cells in the tumor microenvironment (TME) contribute to this dysfunctional state. Here, we show that the biology of tumor-associated macrophages (TAMs) and exhausted T cells (T
MeSH term(s)	CD8-Positive T-Lymphocytes ; Cell Differentiation ; Humans ; Macrophages ; Neoplasms/genetics ; Tumor Microenvironment
Language	English
Publishing date	2022-05-26
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2078448-X
ISSN	1878-3686 ; 1535-6108
ISSN (online)	1878-3686
ISSN	1535-6108
DOI	10.1016/j.ccell.2022.05.004
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Zs.A 5650: Show issues			Location: Je nach Verfügbarkeit (siehe Angabe bei Bestand) bis Jg. 1994: Bestellungen von Artikeln über das Online-Bestellformular Jg. 1995 - 2021: Lesesall (2.OG) ab Jg. 2022: Lesesaal (EG)
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Article: Dynamics of 3D carcinoma cell invasion into aligned collagen

Ray, Arja / Morford, Rachel K / Ghaderi, Nima / Odde, David J / Provenzano, Paolo. P

Integrative biology. 2018 Feb. 19, v. 10, no. 2

2018

Abstract: Carcinoma cells frequently expand and invade from a confined lesion, or multicellular clusters, into and through the stroma on the path to metastasis, often with an efficiency dictated by the architecture and composition of the microenvironment. ... ...

Abstract	Carcinoma cells frequently expand and invade from a confined lesion, or multicellular clusters, into and through the stroma on the path to metastasis, often with an efficiency dictated by the architecture and composition of the microenvironment. Specifically, in desmoplastic carcinomas such as those of the breast, aligned collagen tracks provide contact guidance cues for directed cancer cell invasion. Yet, the evolving dynamics of this process of invasion remains poorly understood, in part due to difficulties in continuously capturing both spatial and temporal heterogeneity and progression to invasion in experimental systems. Therefore, to study the local invasion process from cell dense clusters into aligned collagen architectures found in solid tumors, we developed a novel engineered 3D invasion platform that integrates an aligned collagen matrix with a cell dense tumor-like plug. Using multiphoton microscopy and quantitative analysis of cell motility, we track the invasion of cancer cells from cell-dense bulk clusters into the pre-aligned 3D matrix, and define the temporal evolution of the advancing invasion fronts over several days. This enables us to identify and probe cell dynamics in key regions of interest: behind, at, and beyond the edge of the invading lesion at distinct time points. Analysis of single cell migration identifies significant spatial heterogeneity in migration behavior between cells in the highly cell-dense region behind the leading edge of the invasion front and cells at and beyond the leading edge. Moreover, temporal variations in motility and directionality are also observed between cells within the cell-dense tumor-like plug and the leading invasive edge as its boundary extends into the anisotropic collagen over time. Furthermore, experimental results combined with mathematical modeling demonstrate that in addition to contact guidance, physical crowding of cells is a key regulating factor orchestrating variability in single cell migration during invasion into anisotropic ECM. Thus, our novel platform enables us to capture spatio-temporal dynamics of cell behavior behind, at, and beyond the invasive front and reveals heterogeneous, local interactions that lead to the emergence and maintenance of the advancing front.
Keywords	anisotropy ; breasts ; carcinoma ; cell movement ; collagen ; mathematical models ; metastasis ; microscopy ; neoplasm cells ; quantitative analysis ; spatial variation ; temporal variation
Language	English
Dates of publication	2018-0219
Size	p. 100-112.
Publishing place	The Royal Society of Chemistry
Document type	Article
ZDB-ID	2480063-6
ISSN	1757-9708 ; 1757-9694
ISSN (online)	1757-9708
ISSN	1757-9694
DOI	10.1039/c7ib00152e
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Stromal architecture directs early dissemination in pancreatic ductal adenocarcinoma

Arja Ray / Mackenzie K. Callaway / Nelson J. Rodríguez-Merced / Alexandra L. Crampton / Marjorie Carlson / Kenneth B. Emme / Ethan A. Ensminger / Alexander A. Kinne / Jonathan H. Schrope / Haley R. Rasmussen / Hong Jiang / David G. DeNardo / David K. Wood / Paolo P. Provenzano

JCI Insight, Vol 7, Iss

2022 Volume 3

Abstract: Pancreatic ductal adenocarcinoma (PDA) is an extremely metastatic and lethal disease. Here, in both murine and human PDA, we demonstrate that extracellular matrix architecture regulates cell extrusion and subsequent invasion from intact ductal structures ...

Abstract	Pancreatic ductal adenocarcinoma (PDA) is an extremely metastatic and lethal disease. Here, in both murine and human PDA, we demonstrate that extracellular matrix architecture regulates cell extrusion and subsequent invasion from intact ductal structures through tumor-associated collagen signatures (TACS). This results in early dissemination from histologically premalignant lesions and continual invasion from well-differentiated disease, and it suggests TACS as a biomarker to aid in the pathologic assessment of early disease. Furthermore, we show that pancreatitis results in invasion-conducive architectures, thus priming the stroma prior to malignant disease. Analysis in potentially novel microfluidic-derived microtissues and in vivo demonstrates decreased extrusion and invasion following focal adhesion kinase (FAK) inhibition, consistent with decreased metastasis. Thus, data suggest that targeting FAK or strategies to reengineer and normalize tumor microenvironments may have roles not only in very early disease, but also for limiting continued dissemination from unresectable disease. Likewise, it may be beneficial to employ stroma-targeting strategies to resolve precursor diseases such as pancreatitis in order to remove stromal architectures that increase risk for early dissemination.
Keywords	Cell biology ; Oncology ; Medicine ; R
Subject code	610
Language	English
Publishing date	2022-02-01T00:00:00Z
Publisher	American Society for Clinical investigation
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: Stromal architecture directs early dissemination in pancreatic ductal adenocarcinoma.

Ray, Arja / Callaway, Mackenzie K / Rodríguez-Merced, Nelson J / Crampton, Alexandra L / Carlson, Marjorie / Emme, Kenneth B / Ensminger, Ethan A / Kinne, Alexander A / Schrope, Jonathan H / Rasmussen, Haley R / Jiang, Hong / DeNardo, David G / Wood, David K / Provenzano, Paolo P

JCI insight

2022 Volume 7, Issue 3

Abstract	Pancreatic ductal adenocarcinoma (PDA) is an extremely metastatic and lethal disease. Here, in both murine and human PDA, we demonstrate that extracellular matrix architecture regulates cell extrusion and subsequent invasion from intact ductal structures through tumor-associated collagen signatures (TACS). This results in early dissemination from histologically premalignant lesions and continual invasion from well-differentiated disease, and it suggests TACS as a biomarker to aid in the pathologic assessment of early disease. Furthermore, we show that pancreatitis results in invasion-conducive architectures, thus priming the stroma prior to malignant disease. Analysis in potentially novel microfluidic-derived microtissues and in vivo demonstrates decreased extrusion and invasion following focal adhesion kinase (FAK) inhibition, consistent with decreased metastasis. Thus, data suggest that targeting FAK or strategies to reengineer and normalize tumor microenvironments may have roles not only in very early disease, but also for limiting continued dissemination from unresectable disease. Likewise, it may be beneficial to employ stroma-targeting strategies to resolve precursor diseases such as pancreatitis in order to remove stromal architectures that increase risk for early dissemination.
MeSH term(s)	Animals ; Apoptosis ; Carcinoma, Pancreatic Ductal/genetics ; Carcinoma, Pancreatic Ductal/pathology ; Carcinoma, Pancreatic Ductal/therapy ; Cell Line, Tumor ; Cell Movement ; Focal Adhesion Kinase 1/antagonists & inhibitors ; Focal Adhesion Kinase 1/biosynthesis ; Focal Adhesion Kinase 1/genetics ; Gene Expression Regulation, Neoplastic ; Humans ; Mice ; Mice, Transgenic ; Neoplasms, Experimental ; Pancreatic Neoplasms/genetics ; Pancreatic Neoplasms/pathology ; Pancreatic Neoplasms/therapy ; RNA, Small Interfering/genetics ; Tumor Microenvironment/genetics
Chemical Substances	RNA, Small Interfering ; Focal Adhesion Kinase 1 (EC 2.7.10.2) ; Ptk2 protein, mouse (EC 2.7.10.2)
Language	English
Publishing date	2022-02-08
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ISSN	2379-3708
ISSN (online)	2379-3708
DOI	10.1172/jci.insight.150330
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Article ; Online: Dynamics of 3D carcinoma cell invasion into aligned collagen.

Ray, Arja / Morford, Rachel K / Ghaderi, Nima / Odde, David J / Provenzano, Paolo P

Integrative biology : quantitative biosciences from nano to macro

2018 Volume 10, Issue 2, Page(s) 100–112

Abstract	Carcinoma cells frequently expand and invade from a confined lesion, or multicellular clusters, into and through the stroma on the path to metastasis, often with an efficiency dictated by the architecture and composition of the microenvironment. Specifically, in desmoplastic carcinomas such as those of the breast, aligned collagen tracks provide contact guidance cues for directed cancer cell invasion. Yet, the evolving dynamics of this process of invasion remains poorly understood, in part due to difficulties in continuously capturing both spatial and temporal heterogeneity and progression to invasion in experimental systems. Therefore, to study the local invasion process from cell dense clusters into aligned collagen architectures found in solid tumors, we developed a novel engineered 3D invasion platform that integrates an aligned collagen matrix with a cell dense tumor-like plug. Using multiphoton microscopy and quantitative analysis of cell motility, we track the invasion of cancer cells from cell-dense bulk clusters into the pre-aligned 3D matrix, and define the temporal evolution of the advancing invasion fronts over several days. This enables us to identify and probe cell dynamics in key regions of interest: behind, at, and beyond the edge of the invading lesion at distinct time points. Analysis of single cell migration identifies significant spatial heterogeneity in migration behavior between cells in the highly cell-dense region behind the leading edge of the invasion front and cells at and beyond the leading edge. Moreover, temporal variations in motility and directionality are also observed between cells within the cell-dense tumor-like plug and the leading invasive edge as its boundary extends into the anisotropic collagen over time. Furthermore, experimental results combined with mathematical modeling demonstrate that in addition to contact guidance, physical crowding of cells is a key regulating factor orchestrating variability in single cell migration during invasion into anisotropic ECM. Thus, our novel platform enables us to capture spatio-temporal dynamics of cell behavior behind, at, and beyond the invasive front and reveals heterogeneous, local interactions that lead to the emergence and maintenance of the advancing front.
MeSH term(s)	Breast Neoplasms/metabolism ; Breast Neoplasms/pathology ; Carcinoma/metabolism ; Carcinoma/pathology ; Cell Line, Tumor ; Cell Movement/physiology ; Collagen/metabolism ; Extracellular Matrix/metabolism ; Extracellular Matrix/pathology ; Female ; Humans ; Imaging, Three-Dimensional ; Microscopy, Fluorescence, Multiphoton ; Models, Biological ; Neoplasm Invasiveness/pathology ; Neoplasm Invasiveness/physiopathology ; Systems Biology
Chemical Substances	Collagen (9007-34-5)
Language	English
Publishing date	2018-01-17
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2480063-6
ISSN	1757-9708 ; 1757-9694
ISSN (online)	1757-9708
ISSN	1757-9694
DOI	10.1039/c7ib00152e
Database	MEDical Literature Analysis and Retrieval System OnLINE

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