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Article: Fibroblast Activation Protein (FAP)-Mediated Cleavage of Type III Collagen Reveals Serum Biomarker Potential in Non-Small Cell Lung Cancer and Spondyloarthritis.

Pedersen, Rasmus S / Thorlacius-Ussing, Jeppe / Raimondo, Maria G / Langholm, Lasse L / Schett, Georg / Ramming, Andreas / Karsdal, Morten / Willumsen, Nicholas

Biomedicines

2024 Volume 12, Issue 3

Abstract: Fibroblast activation protein (FAP) is a known promoter of tumor development and is associated with poor clinical outcome for various cancer types. Being specifically expressed in pathological conditions including multiple types of fibrosis and cancers, ... ...

Abstract	Fibroblast activation protein (FAP) is a known promoter of tumor development and is associated with poor clinical outcome for various cancer types. Being specifically expressed in pathological conditions including multiple types of fibrosis and cancers, FAP is an optimal target for diagnostics and treatment. Treatment strategies utilizing the unique proteolytic activity of FAP are emerging, thus emphasizing the importance of biomarkers to directly assess FAP activity. FAP is a type II transmembrane serine protease that has been shown to cleave collagens and other ECM components. In this study, we developed an ELISA assay (C3F) targeting a circulating type III collagen fragment derived from FAP cleavage to reflect FAP activity. We demonstrated that C3F was specific to the neoepitope of the cleavage site and that the fragment was generated through FAP cleavage of type III collagen. We measured C3F in serum from a cohort of patients with non-small cell lung cancer (NSCLC) (
Language	English
Publishing date	2024-02-29
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2720867-9
ISSN	2227-9059
ISSN	2227-9059
DOI	10.3390/biomedicines12030545
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Article ; Online: Regulation of tumor immunity and immunotherapy by the tumor collagen extracellular matrix.

Flies, Dallas B / Langermann, Solomon / Jensen, Christina / Karsdal, Morten A / Willumsen, Nicholas

Frontiers in immunology

2023 Volume 14, Page(s) 1199513

Abstract: It has been known for decades that the tumor extracellular matrix (ECM) is dysfunctional leading to loss of tissue architecture and promotion of tumor growth. The altered ECM and tumor fibrogenesis leads to tissue stiffness that act as a physical barrier ...

Abstract	It has been known for decades that the tumor extracellular matrix (ECM) is dysfunctional leading to loss of tissue architecture and promotion of tumor growth. The altered ECM and tumor fibrogenesis leads to tissue stiffness that act as a physical barrier to immune cell infiltration into the tumor microenvironment (TME). It is becoming increasingly clear that the ECM plays important roles in tumor immune responses. A growing body of data now indicates that ECM components also play a more active role in immune regulation when dysregulated ECM components act as ligands to interact with receptors on immune cells to inhibit immune cell subpopulations in the TME. In addition, immunotherapies such as checkpoint inhibitors that are approved to treat cancer are often hindered by ECM changes. In this review we highlight the ways by which ECM alterations affect and regulate immunity in cancer. More specifically, how collagens and major ECM components, suppress immunity in the complex TME. Finally, we will review how our increased understanding of immune and immunotherapy regulation by the ECM is leading towards novel disruptive strategies to overcome immune suppression.
MeSH term(s)	Humans ; Collagen ; Extracellular Matrix ; Immunotherapy ; Immunosuppression Therapy ; Neoplasms/therapy ; Tumor Microenvironment
Chemical Substances	Collagen (9007-34-5)
Language	English
Publishing date	2023-08-17
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	2606827-8
ISSN	1664-3224 ; 1664-3224
ISSN (online)	1664-3224
ISSN	1664-3224
DOI	10.3389/fimmu.2023.1199513
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Article ; Online: Preliminary investigation of elevated collagen and blood-clotting markers as potential noninvasive biomarkers for small cell lung cancer.

Thorlacius-Ussing, Jeppe / Kristensen, Søren Risom / Karsdal, Morten Asser / Willumsen, Nicholas / Pedersen, Shona

Thoracic cancer

2023 Volume 14, Issue 28, Page(s) 2830–2838

Abstract: Background: Small cell lung cancer (SCLC) is highly aggressive with limited therapeutic options and a poor prognosis. Moreover, noninvasive biomarker tools for detecting disease and monitoring treatment response are lacking. To address this, we ... ...

Abstract	Background: Small cell lung cancer (SCLC) is highly aggressive with limited therapeutic options and a poor prognosis. Moreover, noninvasive biomarker tools for detecting disease and monitoring treatment response are lacking. To address this, we evaluated serum biomarkers of extracellular matrix proteins not previously explored in SCLC. Methods: We measured biomarkers in the serum of 16 patients with SCLC before and after chemotherapy as well as in the serum of 11 healthy individuals. Results: Our findings demonstrated that SCLC serum had higher levels of collagen type I degradation, collagen type III formation, and collagen type XI formation than healthy controls. In addition, we observed higher levels of type XIX and XXII collagens, fibrinogen, and von Willebrand factor A formation in SCLC serum. The formation of type I collagen did not exhibit any discernible variation. However, we observed a decrease in the degradation of type I collagen following chemotherapy. Conclusion: Overall, our findings revealed elevated levels of collagen and blood-clotting markers in the serum of SCLC patients, indicating the potential of ECM proteins as noninvasive biomarkers for SCLC.
MeSH term(s)	Humans ; Small Cell Lung Carcinoma/diagnosis ; Small Cell Lung Carcinoma/drug therapy ; Collagen Type I ; Prognosis ; Biomarkers ; Collagen ; Extracellular Matrix Proteins ; Lung Neoplasms/drug therapy ; Biomarkers, Tumor
Chemical Substances	Collagen Type I ; Biomarkers ; Collagen (9007-34-5) ; Extracellular Matrix Proteins ; Biomarkers, Tumor
Language	English
Publishing date	2023-08-19
Publishing country	Singapore
Document type	Journal Article
ZDB-ID	2625856-0
ISSN	1759-7714 ; 1759-7706
ISSN (online)	1759-7714
ISSN	1759-7706
DOI	10.1111/1759-7714.15066
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Article ; Online: Autoreactivity against Denatured Type III Collagen Is Significantly Decreased in Serum from Patients with Cancer Compared to Healthy Controls.

Jensen, Christina / Drobinski, Patryk / Thorlacius-Ussing, Jeppe / Karsdal, Morten A / Bay-Jensen, Anne-Christine / Willumsen, Nicholas

International journal of molecular sciences

2023 Volume 24, Issue 8

Abstract: Autoantibodies have the potential as cancer biomarkers as they may associate with the outcome and immune-related adverse events (irAEs) following immunotherapy. Cancer and other fibroinflammatory diseases, such as rheumatoid arthritis (RA), are ... ...

Abstract	Autoantibodies have the potential as cancer biomarkers as they may associate with the outcome and immune-related adverse events (irAEs) following immunotherapy. Cancer and other fibroinflammatory diseases, such as rheumatoid arthritis (RA), are associated with excessive collagen turnover leading to collagen triple helix unfolding and denaturation with exposure of immunodominant epitopes. In this study, we aimed to investigate the role of autoreactivity against denatured collagen in cancer. A technically robust assay to quantify autoantibodies against denatured type III collagen products (anti-dCol3) was developed and then measured in pretreatment serum from 223 cancer patients and 33 age-matched controls. Moreover, the association between anti-dCol3 levels and type III collagen degradation (C3M) and formation (PRO-C3) was investigated. Anti-dCol3 levels were significantly lower in patients with bladder (
MeSH term(s)	Male ; Humans ; Collagen Type III/metabolism ; Complement C3 ; Collagen/metabolism ; Biomarkers, Tumor ; Biomarkers ; Melanoma ; Autoantibodies
Chemical Substances	Collagen Type III ; Complement C3 ; Collagen (9007-34-5) ; Biomarkers, Tumor ; Biomarkers ; Autoantibodies
Language	English
Publishing date	2023-04-11
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2019364-6
ISSN	1422-0067 ; 1422-0067 ; 1661-6596
ISSN (online)	1422-0067
ISSN	1422-0067 ; 1661-6596
DOI	10.3390/ijms24087067
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Article ; Online: The collagen landscape in cancer: profiling collagens in tumors and in circulation reveals novel markers of cancer-associated fibroblast subtypes.

Thorlacius-Ussing, Jeppe / Jensen, Christina / Nissen, Neel I / Cox, Thomas R / Kalluri, Raghu / Karsdal, Morten / Willumsen, Nicholas

The Journal of pathology

2023 Volume 262, Issue 1, Page(s) 22–36

Abstract: Cancer-associated fibroblasts (CAFs) deposit and remodel collagens in the tumor stroma, impacting cancer progression and efficacy of interventions. CAFs are the focus of new therapeutics with the aim of normalizing the tumor microenvironment. To do this, ...

Abstract	Cancer-associated fibroblasts (CAFs) deposit and remodel collagens in the tumor stroma, impacting cancer progression and efficacy of interventions. CAFs are the focus of new therapeutics with the aim of normalizing the tumor microenvironment. To do this, a better understanding of CAF heterogeneity and collagen composition in cancer is needed. In this study, we sought to profile the expression of collagens at multiple levels with the goal of identifying cancer biomarkers. We investigated the collagen expression pattern in various cell types and CAF subtypes in a publicly available single-cell RNA sequencing (RNA-seq) dataset of pancreatic ductal adenocarcinoma. Next, we investigated the collagen expression profile in tumor samples across cancer types from The Cancer Genome Atlas (TCGA) database and evaluated if specific patterns of collagen expression were associated with prognosis. Finally, we profiled circulating collagen peptides using a panel of immunoassays to measure collagen fragments in the serum of cancer patients. We found that pancreatic stellate cells and fibroblasts were the primary producers of collagens in the pancreas. COL1A1, COL3A1, COL5A1, COL6A1 were expressed in all CAF subtypes, whereas COL8A1, COL10A1, COL11A1, COL12A1 were specific to myofibroblast CAFs (myCAF) and COL14A1 specific to inflammatory CAFs (iCAF). In TCGA database, myCAF collagens COL10A1 and COL11A1 were elevated across solid tumor types, and multiple associations between high expression and worse survival were found. Finally, circulating collagen biomarkers were elevated in the serum of patients with cancer relative to healthy controls with COL11A1 (myCAF) having the best diagnostic accuracy of the markers measured. In conclusion, CAFs express a noncanonical collagen profile with specific collagen subtypes associated with iCAFs and myCAFs in PDAC. These collagens are deregulated at the cellular, tumor, and systemic levels across different solid tumors and associate with survival. These findings could lead to new discoveries such as novel biomarkers and therapeutic targets. © 2023 The Authors. The Journal of Pathology published by John Wiley & Sons Ltd on behalf of The Pathological Society of Great Britain and Ireland.
MeSH term(s)	Humans ; Cancer-Associated Fibroblasts/pathology ; Pancreatic Neoplasms/pathology ; Fibroblasts/pathology ; Carcinoma, Pancreatic Ductal/pathology ; Collagen/metabolism ; Biomarkers, Tumor/genetics ; Biomarkers, Tumor/metabolism ; Tumor Microenvironment
Chemical Substances	Collagen (9007-34-5) ; Biomarkers, Tumor
Language	English
Publishing date	2023-09-20
Publishing country	England
Document type	Journal Article
ZDB-ID	3119-7
ISSN	1096-9896 ; 0022-3417
ISSN (online)	1096-9896
ISSN	0022-3417
DOI	10.1002/path.6207
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Article ; Online: Post-translational modifications of vimentin reflect different pathological processes associated with non-small cell lung cancer and chronic obstructive pulmonary disease.

Nissen, Neel Ingemann / Karsdal, Morten / Willumsen, Nicholas

Oncotarget

2019 Volume 10, Issue 63, Page(s) 6829–6841

Abstract: Introduction: Vimentin has shown to be highly implicated in cancer initiation and progression. Vimentin is often a target of post-translational modifications (PTMs) which can be disease specific, thus targeting these specific modifications can be of ... ...

Abstract	Introduction: Vimentin has shown to be highly implicated in cancer initiation and progression. Vimentin is often a target of post-translational modifications (PTMs) which can be disease specific, thus targeting these specific modifications can be of high biomarker potential. In this study we set out to evaluate the biological relevance and serum biomarker potential of citrullinated vimentin (VICM) and non-citrullinated vimentin (VIM) in non-small cell lung cancer (NSCLC) and chronic obstructive pulmonary disease (COPD). Methods: A competitive ELISA targeting VIM was developed and quantified in serum from patients with NSCLC and COPD. VIM was compared with levels of VICM in the same indications. Results: VIM was significantly increased in NSCLC ( Conclusions: These findings suggest a biomarker potential of VIM in NSCLC. Our findings also indicate that PTMs of vimentin are highly relevant and that targeting these modifications can have differential biomarker potential.
Language	English
Publishing date	2019-11-26
Publishing country	United States
Document type	Journal Article
ZDB-ID	2560162-3
ISSN	1949-2553 ; 1949-2553
ISSN (online)	1949-2553
ISSN	1949-2553
DOI	10.18632/oncotarget.27332
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Article ; Online: Collagens and Cancer associated fibroblasts in the reactive stroma and its relation to Cancer biology.

Nissen, Neel I / Karsdal, Morten / Willumsen, Nicholas

Journal of experimental & clinical cancer research : CR

2019 Volume 38, Issue 1, Page(s) 115

Abstract: The extracellular matrix (ECM) plays an important role in cancer progression. It can be divided into the basement membrane (BM) that supports epithelial/endothelial cell behavior and the interstitial matrix (IM) that supports the underlying stromal ... ...

Abstract	The extracellular matrix (ECM) plays an important role in cancer progression. It can be divided into the basement membrane (BM) that supports epithelial/endothelial cell behavior and the interstitial matrix (IM) that supports the underlying stromal compartment. The major components of the ECM are the collagens. While breaching of the BM and turnover of e.g. type IV collagen, is a well described part of tumorigenesis, less is known regarding the impact on tumorigenesis from the collagens residing in the stroma. Here we give an introduction and overview to the link between tumorigenesis and stromal collagens, with focus on the fibrillar collagens type I, II, III, V, XI, XXIV and XXVII as well as type VI collagen. Moreover, we discuss the impact of the cells responsible for this altered stromal collagen remodeling, the cancer associated fibroblasts (CAFs), and how these cells are key players in orchestrating the tumor microenvironment composition and tissue microarchitecture, hence also driving tumorigenesis and affecting response to treatment. Lastly, we discuss how specific collagen-derived biomarkers reflecting the turnover of stromal collagens and CAF activity may be used as tools to non-invasively interrogate stromal reactivity in the tumor microenvironment and predict response to treatment.
MeSH term(s)	Cancer-Associated Fibroblasts/metabolism ; Cancer-Associated Fibroblasts/pathology ; Carcinogenesis/genetics ; Collagen Type I/genetics ; Collagen Type I/metabolism ; Fibroblasts/metabolism ; Gene Expression Regulation, Neoplastic ; Humans ; Neoplasms/genetics ; Neoplasms/metabolism ; Neoplasms/pathology ; Stromal Cells/metabolism ; Stromal Cells/pathology ; Tumor Microenvironment/genetics
Chemical Substances	Collagen Type I
Language	English
Publishing date	2019-03-06
Publishing country	England
Document type	Journal Article ; Review
ZDB-ID	803138-1
ISSN	1756-9966 ; 0392-9078
ISSN (online)	1756-9966
ISSN	0392-9078
DOI	10.1186/s13046-019-1110-6
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Zs.A 2065: Show issues

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Article: Matrix Metalloprotease Generated Fragments of Type VI Collagen Have Serum Biomarker Potential in Cancer - A Proof of Concept Study.

Willumsen, Nicholas / Bager, Cecilie / Karsdal, Morten A

Translational oncology

2019 Volume 12, Issue 5, Page(s) 693–698

Abstract: Background: Type VI collagen (COL6) is associated with several pro-tumorigenic events. COL6 is primarily composed of three alpha-chains (a1-a3) forming a specialized microfibrillar network to support tissue architecture. COL6 homeostasis is lost in the ... ...

Abstract	Background: Type VI collagen (COL6) is associated with several pro-tumorigenic events. COL6 is primarily composed of three alpha-chains (a1-a3) forming a specialized microfibrillar network to support tissue architecture. COL6 homeostasis is lost in the tumor due to increased COL6 synthesis by activated fibroblast and altered proteolytic degradation by matrix metalloproteases (MMPs). Consequently, pathology-specific COL6 fragments are released to the circulation. This study evaluates four COL6 fragments measured in serum as potential biomarkers for cancer. Methods: C6Ma1 (MMP-generated neo-epitope on the a1 chain), C6Ma3 (MMP-generated neo-epitope on the a3 chain), PRO-C6 (C-terminal of the a3 chain) and IC-6 (internal epitope on the a1 chain) were measured by ELISA in serum from patients with various stage 1-4 cancer indications (n = 4-11 per indication, total n = 65) and healthy controls (n = 13). Results: C6Ma1 and C6Ma3 were significantly elevated in most cancer types compared to controls; PRO-C6 and IC6 were not. No significant differences were seen according to age, gender and TNM stage. Comparing cancer patients to controls, the AUROC was 0.90 (P < .0001), 0.87 (P < .0001), 0.59 (P = .311) and 0.53 (P = .747) for C6Ma1, C6Ma3, PRO-C6 and IC-6, respectively. Only C6M and C6Ma3 correlated significantly (Spearman, r = 0.74, P < .0001). Conclusions: MMP-generated COL6 fragments (C6Ma1, C6Ma3) were elevated in serum from cancer patients compared to controls and had promising diagnostic accuracy. This supports that MMP-mediated COL6 remodeling is important in tumorigenesis and indicate cancer biomarker potential of quantifying COL-6 fragments in serum. Future studies should determine biological and clinical applicability of the COL-6 serum biomarkers in relation to cancer.
Language	English
Publishing date	2019-03-09
Publishing country	United States
Document type	Journal Article
ZDB-ID	2443840-6
ISSN	1936-5233 ; 1936-5233 ; 1944-7124
ISSN (online)	1936-5233
ISSN	1936-5233 ; 1944-7124
DOI	10.1016/j.tranon.2019.02.004
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Article ; Online: Vastatin (the NC1 domain of human type VIII collagen a1 chain) is linked to stromal reactivity and elevated in serum from patients with colorectal cancer.

Willumsen, Nicholas / Jorgensen, Lars Nannestad / Karsdal, Morten Asser

Cancer biology & therapy

2019 Volume 20, Issue 5, Page(s) 692–699

Abstract: Vastatin, a fragment derived from type VIII collagen, is one of the least studied collagen-derived matrikines. Vastatin can be detected in serum but little is known regarding the relevance of serum vastatin in colorectal cancer (CRC). In this study, ... ...

Abstract	Vastatin, a fragment derived from type VIII collagen, is one of the least studied collagen-derived matrikines. Vastatin can be detected in serum but little is known regarding the relevance of serum vastatin in colorectal cancer (CRC). In this study, serum vastatin was measured (ELISA) in 67 healthy controls and 48 CRC patients prior to resection and compared to clinicopathological parameters and serum biomarkers of stromal reactivity (C3M, VICM). Impact of resection and chemotherapy were evaluated by comparing baseline values with a 3-month follow-up sample (n = 23). Serum vastatin was detectable in 114 of 115 subjects. At baseline vastatin was elevated in CRC compared to controls (P < 0.001) with a diagnostic accuracy (AUROC) of 0.865, p < 0.0001. Vastatin correlated with age in controls but not in patients with CRC; no association was seen with clinicopathological parameters. Vastatin was independently associated with C3M (stepwise linear regression coefficient 0.25, p = 0.046). Overall, no difference was seen in vastatin levels between baseline and follow-up. In conclusion, vastatin is elevated in serum from patients with CRC and correlate with interstitial matrix degradation (C3M). This indicates that vastatin is linked to stromal reactivity and suggests that vastatin has biomarker potential in CRC. The association with clinicopathological parameters and treatment effect needs further evaluation.
MeSH term(s)	Adult ; Age Factors ; Aged ; Aged, 80 and over ; Biomarkers, Tumor/blood ; Biomarkers, Tumor/metabolism ; Case-Control Studies ; Chemotherapy, Adjuvant ; Collagen Type VIII/blood ; Collagen Type VIII/metabolism ; Colorectal Neoplasms/blood ; Colorectal Neoplasms/diagnosis ; Colorectal Neoplasms/pathology ; Colorectal Neoplasms/therapy ; Extracellular Matrix/pathology ; Female ; Follow-Up Studies ; Healthy Volunteers ; Humans ; Male ; Middle Aged ; Young Adult
Chemical Substances	Biomarkers, Tumor ; Col8A1 protein, human ; Collagen Type VIII ; vastatin
Language	English
Publishing date	2019-01-09
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2146305-0
ISSN	1555-8576 ; 1538-4047
ISSN (online)	1555-8576
ISSN	1538-4047
DOI	10.1080/15384047.2018.1550571
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Zs.A 5887: Show issues

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Article ; Online: MCT4 and CD147 co-localize with MMP14 in invadopodia and support matrix degradation and invasion by breast cancer cells.

Meng, Signe / Sørensen, Ester E / Ponniah, Muthulakshmi / Thorlacius-Ussing, Jeppe / Crouigneau, Roxane / Larsen, Tanja / Borre, Magnus T / Willumsen, Nicholas / Flinck, Mette / Pedersen, Stine F

Journal of cell science

2024

Abstract: The lactate-proton cotransporter MCT4 and its chaperone CD147 are upregulated in breast cancers, correlating with decreased patient survival. Here, we test the hypothesis that MCT4 and CD147 favor breast cancer invasion through interdependent effects on ... ...

Abstract	The lactate-proton cotransporter MCT4 and its chaperone CD147 are upregulated in breast cancers, correlating with decreased patient survival. Here, we test the hypothesis that MCT4 and CD147 favor breast cancer invasion through interdependent effects on extracellular matrix (ECM) degradation. MCT4 and CD147 expression and membrane localization were strongly reciprocally interdependent in MDA-MB-231 breast cancer cells. Knockdown (KD) and overexpression (OE) of MCT4 and/or CD174 in- and decreased, respectively, migration, invasion, and fluorescent gelatin degradation. OE of both proteins increased gelatin degradation and appearance of the matrix metalloprotease (MMP)-generated collagen-I cleavage product reC1M more than each protein alone, suggesting a concerted role in ECM degradation. MCT4 and CD147 co-localized with invadopodia markers at the plasma membrane and with MMP14, the lysosomal marker LAMP-1, and partially with the autophagosome marker LC3, in F-actin-decorated intracellular vesicles. We conclude that MCT4 and CD147 reciprocally regulate each other and interdependently support migration and invasiveness of MDA-MB-231 breast cancer cells. Mechanistically, this involves MCT4-CD147-dependent stimulation of ECM degradation and specifically of MMP-mediated collagen-I degradation. We suggest that the MCT4-CD147 complex is co-delivered to invadopodia with MMP14.
Language	English
Publishing date	2024-04-25
Publishing country	England
Document type	Journal Article
ZDB-ID	2993-2
ISSN	1477-9137 ; 0021-9533
ISSN (online)	1477-9137
ISSN	0021-9533
DOI	10.1242/jcs.261608
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