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Article ; Online: Necrotic debris and STING exert therapeutically relevant effects on tumor cholesterol homeostasis.

Katakam, Sampath / Anand, Santosh / Martin, Patricia / Riggi, Nicolo / Stamenkovic, Ivan

Life science alliance

2022 Volume 5, Issue 3

Abstract: Malignant tumors commonly display necrosis, which invariably triggers an inflammatory response that supports tumor growth. However, the effect on tumor cells of necrotic debris, or damage-associated molecular patterns (DAMPs) released by dying cells is ... ...

Abstract	Malignant tumors commonly display necrosis, which invariably triggers an inflammatory response that supports tumor growth. However, the effect on tumor cells of necrotic debris, or damage-associated molecular patterns (DAMPs) released by dying cells is unknown. Here, we addressed the effect of DAMPs on primary Ewing sarcoma (EwS) cells and cell lines grown in 3D (spheroids) and 2D culture. We show that DAMPs promote the growth of EwS spheroids but not 2D cultures and that the underlying mechanism implicates an increase in cholesterol load in spheroids. In contrast, stimulation of the nucleic acid sensor signaling platform STING by its ligand cyclic GMP-AMP decreases the tumor cell cholesterol load and reduces their tumor initiating ability. Overexpression of STING or stimulation with cyclic GMP-AMP opposes the growth stimulatory effect of DAMPs and synergizes with the cholesterol synthesis inhibitor simvastatin to inhibit tumor growth. Our observations show that modulation of cholesterol homeostasis is a major effect of necrotic cell debris and STING and suggest that combining STING agonists with statins may help control tumor growth.
MeSH term(s)	Alarmins/metabolism ; Apoptosis ; Biomarkers ; Cell Line, Tumor ; Cholesterol/metabolism ; Disease Management ; Disease Susceptibility ; Gene Expression Regulation, Neoplastic ; Homeostasis ; Humans ; Lipid Metabolism ; Membrane Proteins/metabolism ; Necrosis/metabolism ; Neoplasms/etiology ; Neoplasms/metabolism ; Neoplasms/pathology ; Neoplasms/therapy ; Spheroids, Cellular ; Tumor Cells, Cultured
Chemical Substances	Alarmins ; Biomarkers ; Membrane Proteins ; STING1 protein, human ; Cholesterol (97C5T2UQ7J)
Language	English
Publishing date	2022-01-04
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	2575-1077
ISSN (online)	2575-1077
DOI	10.26508/lsa.202101256
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Article ; Online: Ewing's Sarcoma.

Riggi, Nicolò / Suvà, Mario L / Stamenkovic, Ivan

The New England journal of medicine

2021 Volume 384, Issue 2, Page(s) 154–164

MeSH term(s)	Antineoplastic Agents/therapeutic use ; Bone Neoplasms/genetics ; Bone Neoplasms/therapy ; Combined Modality Therapy ; DNA Methylation ; DNA, Neoplasm/metabolism ; Gene Expression Regulation ; Humans ; Mutation ; Oncogene Proteins, Fusion/metabolism ; Polymorphism, Genetic ; Prognosis ; Proto-Oncogene Protein c-fli-1/metabolism ; RNA-Binding Protein EWS/metabolism ; Sarcoma, Ewing/genetics ; Sarcoma, Ewing/therapy ; Suppression, Genetic ; Translocation, Genetic
Chemical Substances	Antineoplastic Agents ; DNA, Neoplasm ; EWS-FLI fusion protein ; Oncogene Proteins, Fusion ; Proto-Oncogene Protein c-fli-1 ; RNA-Binding Protein EWS
Language	English
Publishing date	2021-01-26
Publishing country	United States
Document type	Journal Article ; Review
ZDB-ID	207154-x
ISSN	1533-4406 ; 0028-4793
ISSN (online)	1533-4406
ISSN	0028-4793
DOI	10.1056/NEJMra2028910
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Article ; Online: Mesenchymal stromal cells in cancer: a review of their immunomodulatory functions and dual effects on tumor progression.

Galland, Sabine / Stamenkovic, Ivan

The Journal of pathology

2019 Volume 250, Issue 5, Page(s) 555–572

Abstract: Mesenchymal stem or stromal cells (MSCs) are pluripotent cells implicated in a broad range of physiological events, including organogenesis and maintenance of tissue homeostasis as well as tissue regeneration and repair. Because their current definition ... ...

Abstract	Mesenchymal stem or stromal cells (MSCs) are pluripotent cells implicated in a broad range of physiological events, including organogenesis and maintenance of tissue homeostasis as well as tissue regeneration and repair. Because their current definition is somewhat loose - based primarily on their ability to differentiate into a variety of mesenchymal tissues, adhere to plastic, and express, or lack, a handful of cell surface markers - MSCs likely encompass several subpopulations, which may have diverse properties. Their diversity may explain, at least in part, the pleiotropic functions that they display in different physiological and pathological settings. In the context of tissue injury, MSCs can respectively promote and attenuate inflammation during the early and late phases of tissue repair. They may thereby act as sensors of the inflammatory response and secrete mediators that boost or temper the response as required by the stage of the reparatory and regenerative process. MSCs are also implicated in regulating tumor development, in which they are increasingly recognized to play a complex role. Thus, MSCs can both promote and constrain tumor progression by directly affecting tumor cells via secreted mediators and cell-cell interactions and by modulating the innate and adaptive immune response. This review summarizes our current understanding of MSC involvement in tumor development and highlights the mechanistic underpinnings of their implication in tumor growth and progression. © 2020 Authors. Journal of Pathology published by John Wiley & Sons Ltd on behalf of Pathological Society of Great Britain and Ireland.
MeSH term(s)	Cell Communication/physiology ; Disease Progression ; Humans ; Inflammation/pathology ; Mesenchymal Stem Cell Transplantation/methods ; Mesenchymal Stem Cells/immunology ; Mesenchymal Stem Cells/pathology ; Neoplasms/pathology
Language	English
Publishing date	2019-12-18
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	3119-7
ISSN	1096-9896 ; 0022-3417
ISSN (online)	1096-9896
ISSN	0022-3417
DOI	10.1002/path.5357
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Article ; Online: Ewing's Sarcoma. Reply.

Riggi, Nicolò / Suvà, Mario L / Stamenkovic, Ivan

The New England journal of medicine

2021 Volume 384, Issue 15, Page(s) 1477–1478

MeSH term(s)	Bone Neoplasms ; Humans ; Sarcoma, Ewing/therapy ; Tumor Cells, Cultured
Language	English
Publishing date	2021-04-14
Publishing country	United States
Document type	Letter ; Comment
ZDB-ID	207154-x
ISSN	1533-4406 ; 0028-4793
ISSN (online)	1533-4406
ISSN	0028-4793
DOI	10.1056/NEJMc2102423
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Article ; Online: Attenuation of the pro-inflammatory signature of lung cancer-derived mesenchymal stromal cells by statins.

Galland, Sabine / Martin, Patricia / Fregni, Giulia / Letovanec, Igor / Stamenkovic, Ivan

Cancer letters

2020 Volume 484, Page(s) 50–64

Abstract: Solid tumor growth triggers a dynamic host response, which recapitulates wound healing and defines the tumor microenvironment (TME). In addition to the action of the tumor cells themselves, the TME is maintained by a myriad of immune and stromal cell- ... ...

Abstract	Solid tumor growth triggers a dynamic host response, which recapitulates wound healing and defines the tumor microenvironment (TME). In addition to the action of the tumor cells themselves, the TME is maintained by a myriad of immune and stromal cell-derived soluble mediators and extracellular matrix components whose combined action supports tumor progression. However, therapeutic targeting of the TME has proven challenging because of incomplete understanding of the tumor-host crosstalk at the molecular level. Here, we investigated the crosstalk between mesenchymal stromal cells (MSCs) and primary cancer cells (PCCs) from human squamous cell lung carcinoma (SCC). We discovered that PCCs secrete CCL3 and stimulate IL-6, CCL2, ICAM-1 and VCAM-1 expression in MSCs and that the MSC-PCC crosstalk can be disrupted by the lipid-lowering drug simvastatin, which displays pleiotropic effects on cell metabolism and suppresses IL-6 and CCL2 production by MSCs and CCL3 secretion by PCCs. In addition, simvastatin inhibited spheroid formation by PCCs and negatively affected PCC survival. Our observations demonstrate that commonly used statins may be repurposed to target the TME in lung carcinoma.
MeSH term(s)	Aged ; Aged, 80 and over ; Carcinoma, Squamous Cell/genetics ; Carcinoma, Squamous Cell/metabolism ; Carcinoma, Squamous Cell/pathology ; Cells, Cultured ; Chemokine CCL2/genetics ; Chemokine CCL2/metabolism ; Chemokine CCL3/genetics ; Chemokine CCL3/metabolism ; Cytokines/genetics ; Cytokines/metabolism ; Female ; Gene Expression/drug effects ; Humans ; Inflammation Mediators/metabolism ; Interleukin-6/genetics ; Interleukin-6/metabolism ; Lung Neoplasms/genetics ; Lung Neoplasms/metabolism ; Lung Neoplasms/pathology ; Male ; Mesenchymal Stem Cells/cytology ; Mesenchymal Stem Cells/drug effects ; Mesenchymal Stem Cells/metabolism ; Middle Aged ; Simvastatin/pharmacology ; Tumor Cells, Cultured ; Tumor Microenvironment/drug effects ; Tumor Microenvironment/genetics
Chemical Substances	Chemokine CCL2 ; Chemokine CCL3 ; Cytokines ; Inflammation Mediators ; Interleukin-6 ; Simvastatin (AGG2FN16EV)
Language	English
Publishing date	2020-05-08
Publishing country	Ireland
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	195674-7
ISSN	1872-7980 ; 0304-3835
ISSN (online)	1872-7980
ISSN	0304-3835
DOI	10.1016/j.canlet.2020.05.005
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Article ; Online: Synovial sarcoma: when epigenetic changes dictate tumour development.

Riggi, Nicolo / Cironi, Luisa / Stamenkovic, Ivan

Swiss medical weekly

2018 Volume 148, Page(s) w14667

Abstract: Synovial sarcoma is a highly aggressive soft tissue malignancy that often affects adolescents and young adults. It is associated with a unique chromosomal translocation that results in the formation and expression of the fusion gene SS18-SSX, which ... ...

Abstract	Synovial sarcoma is a highly aggressive soft tissue malignancy that often affects adolescents and young adults. It is associated with a unique chromosomal translocation that results in the formation and expression of the fusion gene SS18-SSX, which underlies its pathogenesis. Although SS18-SSX provides a potentially unique therapeutic target, all attempts to neutralise it have been unsuccessful thus far. When complete surgical removal of the tumour fails, therapy is limited to largely ineffective cytotoxic drug regimens. Nevertheless, recent discoveries about the mechanisms of SS18-SSX protein function have provided insight into potential alternative therapeutic strategies. SS18-SSX displays oncogenic activity through protein-protein interactions and participation in chromatin remodelling complexes. This review summarises our current understanding of the function of SS18-SSX and the mechanisms by which it alters the epigenetic landscape of permissive cells to induce transformation and the subsequent development of synovial sarcoma.
MeSH term(s)	Cell Transformation, Neoplastic/genetics ; Chromatin/genetics ; Epigenesis, Genetic ; Humans ; Neoplasm Proteins/genetics ; Proto-Oncogene Proteins/genetics ; Repressor Proteins/genetics ; Sarcoma, Synovial/genetics ; Sarcoma, Synovial/pathology ; Translocation, Genetic/genetics
Chemical Substances	Chromatin ; Neoplasm Proteins ; Proto-Oncogene Proteins ; Repressor Proteins ; SS18 protein, human ; synovial sarcoma X breakpoint proteins (164289-47-8)
Language	English
Publishing date	2018-12-02
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	2036179-8
ISSN	1424-3997 ; 1424-7860
ISSN (online)	1424-3997
ISSN	1424-7860
DOI	10.4414/smw.2018.14667
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Article ; Online: Recruitment of Matrix Metalloproteinase-9 (MMP-9) to the Fibroblast Cell Surface by Lysyl Hydroxylase 3 (LH3) Triggers Transforming Growth Factor-β (TGF-β) Activation and Fibroblast Differentiation.

Dayer, Cynthia / Stamenkovic, Ivan

The Journal of biological chemistry

2015 Volume 290, Issue 22, Page(s) 13763–13778

Abstract: Solid tumor growth triggers a wound healing response. Similar to wound healing, fibroblasts in the tumor stroma differentiate into myofibroblasts (also referred to as cancer-associated fibroblasts) primarily, but not exclusively, in response to ... ...

Abstract	Solid tumor growth triggers a wound healing response. Similar to wound healing, fibroblasts in the tumor stroma differentiate into myofibroblasts (also referred to as cancer-associated fibroblasts) primarily, but not exclusively, in response to transforming growth factor-β (TGF-β). Myofibroblasts in turn enhance tumor progression by remodeling the stroma. Among proteases implicated in stroma remodeling, matrix metalloproteinases (MMPs), including MMP-9, play a prominent role. Recent evidence indicates that MMP-9 recruitment to the tumor cell surface enhances tumor growth and invasion. In the present work, we addressed the potential relevance of MMP-9 recruitment to and activity at the surface of fibroblasts. We show that recruitment of MMP-9 to the fibroblast cell surface occurs through its fibronectin-like (FN) domain and that the molecule responsible for the recruitment is lysyl hydroxylase 3 (LH3). Functional assays suggest that both pro- and active MMP-9 trigger α-smooth muscle actin expression in cultured fibroblasts, reflecting myofibroblast differentiation, possibly as a result of TGF-β activation. Moreover, the recombinant FN domain inhibited both MMP-9-induced TGF-β activation and α-smooth muscle actin expression by displacing MMP-9 from the fibroblast cell surface. Together our results uncover LH3 as a new docking receptor of MMP-9 on the fibroblast cell surface and demonstrate that the MMP-9 FN domain is essential for the interaction. They also show that the recombinant FN domain inhibits MMP-9-induced TGF-β activation and fibroblast differentiation, providing a potentially attractive therapeutic reagent toward attenuating tumor progression where MMP-9 activity is strongly implicated.
MeSH term(s)	Animals ; CHO Cells ; Cell Differentiation ; Cell Line, Tumor ; Cell Membrane/metabolism ; Cell Separation ; Cricetinae ; Cricetulus ; Fibroblasts/metabolism ; Flow Cytometry ; HEK293 Cells ; Humans ; Liver/metabolism ; Matrix Metalloproteinase 9/metabolism ; Microscopy, Fluorescence ; Myofibroblasts/cytology ; Procollagen-Lysine, 2-Oxoglutarate 5-Dioxygenase/metabolism ; Recombinant Proteins/metabolism ; Transforming Growth Factor beta/metabolism ; Tumor Microenvironment
Chemical Substances	Recombinant Proteins ; Transforming Growth Factor beta ; PLOD3 protein, human (EC 1.14.11.-) ; Procollagen-Lysine, 2-Oxoglutarate 5-Dioxygenase (EC 1.14.11.4) ; MMP9 protein, human (EC 3.4.24.35) ; Matrix Metalloproteinase 9 (EC 3.4.24.35)
Language	English
Publishing date	2015-03-30
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2997-x
ISSN	1083-351X ; 0021-9258
ISSN (online)	1083-351X
ISSN	0021-9258
DOI	10.1074/jbc.M114.622274
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Article: CIC-DUX4 Chromatin Profiling Reveals New Epigenetic Dependencies and Actionable Therapeutic Targets in CIC-Rearranged Sarcomas.

Bakaric, Arnaud / Cironi, Luisa / Praz, Viviane / Sanalkumar, Rajendran / Broye, Liliane C / Favre-Bulle, Kerria / Letovanec, Igor / Digklia, Antonia / Renella, Raffaele / Stamenkovic, Ivan / Ott, Christopher J / Nakamura, Takuro / Antonescu, Cristina R / Rivera, Miguel N / Riggi, Nicolò

Cancers

2024 Volume 16, Issue 2

Abstract: CIC-DUX4-rearranged sarcoma (CDS) is a rare and aggressive soft tissue tumor that occurs most frequently in young adults. The key oncogenic driver of this disease is the expression of the CIC-DUX4 fusion protein as a result of chromosomal rearrangements. ...

Abstract	CIC-DUX4-rearranged sarcoma (CDS) is a rare and aggressive soft tissue tumor that occurs most frequently in young adults. The key oncogenic driver of this disease is the expression of the CIC-DUX4 fusion protein as a result of chromosomal rearrangements. CIC-DUX4 displays chromatin binding properties, and is therefore believed to function as an aberrant transcription factor. However, the chromatin remodeling events induced by CIC-DUX4 are not well understood, limiting our ability to identify new mechanism-based therapeutic strategies for these patients. Here, we generated a genome-wide profile of CIC-DUX4 DNA occupancy and associated chromatin states in human CDS cell models and primary tumors. Combining chromatin profiling, proximity ligation assays, as well as genetic and pharmacological perturbations, we show that CIC-DUX4 operates as a potent transcriptional activator at its binding sites. This property is in contrast with the repressive function of the wild-type CIC protein, and is mainly mediated through the direct interaction of CIC-DUX4 with the acetyltransferase p300. In keeping with this, we show p300 to be essential for CDS tumor cell proliferation; additionally, we find its pharmacological inhibition to significantly impact tumor growth in vitro and in vivo. Taken together, our study elucidates the mechanisms underpinning CIC-DUX4-mediated transcriptional regulation.
Language	English
Publishing date	2024-01-21
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2527080-1
ISSN	2072-6694
ISSN	2072-6694
DOI	10.3390/cancers16020457
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Article ; Online: Cancer Metastasis: A Reappraisal of Its Underlying Mechanisms and Their Relevance to Treatment.

Riggi, Nicolo / Aguet, Michel / Stamenkovic, Ivan

Annual review of pathology

2017 Volume 13, Page(s) 117–140

Abstract: Metastases are responsible for the vast majority of cancer-related deaths, but, despite intense efforts to understand their underlying mechanisms with the goal of uncovering effective therapeutic targets, treatment of metastatic cancer has progressed ... ...

Abstract	Metastases are responsible for the vast majority of cancer-related deaths, but, despite intense efforts to understand their underlying mechanisms with the goal of uncovering effective therapeutic targets, treatment of metastatic cancer has progressed minimally. In this review, we examine the biological programs currently proposed to be key drivers of metastasis. On the basis of evidence from a growing body of research, we discuss to what extent the cellular and molecular mechanisms that are suggested to underlie cancer cell dissemination are specific to the metastatic process, as opposed to representing natural primary tumor progression. Our review highlights the contrast between the abundance of insight gained into the events that constitute the metastatic cascade and the paucity of therapeutic options.
MeSH term(s)	Humans ; Neoplasm Invasiveness/pathology ; Neoplasm Metastasis/pathology ; Neoplasms/pathology ; Neoplastic Stem Cells/pathology
Language	English
Publishing date	2017-10-25
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	2227429-7
ISSN	1553-4014 ; 1553-4006
ISSN (online)	1553-4014
ISSN	1553-4006
DOI	10.1146/annurev-pathol-020117-044127
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Article: Extracellular matrix remodelling: the role of matrix metalloproteinases.

Stamenkovic, Ivan

The Journal of pathology

2003 Volume 200, Issue 4, Page(s) 448–464

Abstract: Matrix metalloproteinases (MMPs) are a growing family of metalloendopeptidases that cleave the protein components of the extracellular matrix and thereby play a central role in tissue remodelling. For many years following their discovery, MMPs were ... ...

Abstract	Matrix metalloproteinases (MMPs) are a growing family of metalloendopeptidases that cleave the protein components of the extracellular matrix and thereby play a central role in tissue remodelling. For many years following their discovery, MMPs were believed to function primarily as regulators of ECM composition and to facilitate cell migration simply by removing barriers such as collagen. It is becoming increasingly clear, however, that MMPs are implicated in the functional regulation of a host of non-ECM molecules that include growth factors and their receptors, cytokines and chemokines, adhesion receptors and cell surface proteoglycans, and a variety of enzymes. MMPs therefore play an important role in the control of cellular interactions with and response to their environment in conditions that promote tissue turnover, be they physiological, such as normal development, or pathological, such as inflammation and cancer. This review summarizes some of the recent discoveries that have shed new light on the role of MMPs in physiology and disease.
MeSH term(s)	Bone Development/physiology ; Cadherins/metabolism ; Cytokines/metabolism ; Enzyme Activation ; Enzyme Inhibitors/therapeutic use ; Extracellular Matrix/enzymology ; Extracellular Matrix/pathology ; Growth Substances/metabolism ; Humans ; Matrix Metalloproteinase Inhibitors ; Matrix Metalloproteinases/physiology ; Neoplasm Invasiveness ; Neoplasm Metastasis ; Neoplasms/drug therapy ; Neoplasms/enzymology ; Wound Healing/physiology
Chemical Substances	Cadherins ; Cytokines ; Enzyme Inhibitors ; Growth Substances ; Matrix Metalloproteinase Inhibitors ; Matrix Metalloproteinases (EC 3.4.24.-)
Language	English
Publishing date	2003-07
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	3119-7
ISSN	1096-9896 ; 0022-3417
ISSN (online)	1096-9896
ISSN	0022-3417
DOI	10.1002/path.1400
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