Review
. 2018 Jul; 6(1):65.
doi: 10.1186/s40425-018-0376-0.

Tumor matrix remodeling and novel immunotherapies: the promise of matrix-derived immune biomarkers

Muhammad Umair Mushtaq 1 Athanasios Papadas 1 Adam Pagenkopf 1 Evan Flietner 1 Zachary Morrow 1 Sibgha Gull Chaudhary 1 Fotis Asimakopoulos 2 
Affiliations
  • PMID: 29970158
  •     195 References
  •     52 citations

Abstract

Recent advances in our understanding of the dynamics of cellular cross-talk have highlighted the significance of host-versus-tumor effect that can be harnessed with immune therapies. Tumors exploit immune checkpoints to evade adaptive immune responses. Cancer immunotherapy has witnessed a revolution in the past decade with the development of immune checkpoint inhibitors (ICIs), monoclonal antibodies against cytotoxic T lymphocyte antigen 4 (CTLA-4) and programmed cell death protein 1 (PD-1) or their ligands, such as PD1 ligand 1 (PD-L1). ICIs have been reported to have activity against a broad range of tumor types, in both solid organ and hematologic malignancy contexts. However, less than one-third of the patients achieve a durable and meaningful treatment response. Expression of immune checkpoint ligands (e.g., PD-L1), mutational burden and tumor-infiltrating lymphocytes are currently used as biomarkers for predicting response to ICIs. However, they do not reliably predict which patients will benefit from these therapies. There is dire need to discover novel biomarkers to predict treatment efficacy and to identify areas for development of combination strategies to improve response rates. Emerging evidence suggests key roles of tumor extracellular matrix (ECM) components and their proteolytic remodeling products in regulating each step of the cancer-immunity cycle. Here we review tumor matrix dynamics and matrix remodeling in context of anti-tumor immune responses and immunotherapy and propose the exploration of matrix-based biomarkers to identify candidates for immune therapy.

Keywords: Adaptive immune response; Immune biomarkers; Immune checkpoint inhibitors; Immunotherapy; Matrix remodeling; Tumor microenvironment.

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Highly Cited.
Influence of Immune Myeloid Cells on the Extracellular Matrix During Cancer Metastasis.
David Jiang, Su Yin Lim.
Cancer Microenviron, 2016 Mar 10; 9(1). PMID: 26956475    Free PMC article.
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Moving targets: Emerging roles for MMPs in cancer progression and metastasis.
Gemma Shay, Conor C Lynch, Barbara Fingleton.
Matrix Biol, 2015 Feb 06; 44-46. PMID: 25652204    Free PMC article.
Highly Cited. Review.
Nivolumab in previously untreated melanoma without BRAF mutation.
Caroline Robert, Georgina V Long, +25 authors, Paolo A Ascierto.
N Engl J Med, 2014 Nov 18; 372(4). PMID: 25399552
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Clinical significance of PD-L1 and PD-L2 copy number gains in non-small-cell lung cancer.
Yusuke Inoue, Katsuhiro Yoshimura, +12 authors, Haruhiko Sugimura.
Oncotarget, 2016 Apr 07; 7(22). PMID: 27050074    Free PMC article.
Role of lymphatic vessels in tumor immunity: passive conduits or active participants?
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J Mammary Gland Biol Neoplasia, 2010 Sep 14; 15(3). PMID: 20835756
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The matrisome: in silico definition and in vivo characterization by proteomics of normal and tumor extracellular matrices.
Alexandra Naba, Karl R Clauser, +3 authors, Richard O Hynes.
Mol Cell Proteomics, 2011 Dec 14; 11(4). PMID: 22159717    Free PMC article.
Highly Cited.
Activated monocytes in peritumoral stroma of hepatocellular carcinoma foster immune privilege and disease progression through PD-L1.
Dong-Ming Kuang, Qiyi Zhao, +4 authors, Limin Zheng.
J Exp Med, 2009 May 20; 206(6). PMID: 19451266    Free PMC article.
Highly Cited.
Depletion of carcinoma-associated fibroblasts and fibrosis induces immunosuppression and accelerates pancreas cancer with reduced survival.
Berna C Özdemir, Tsvetelina Pentcheva-Hoang, +18 authors, Raghu Kalluri.
Cancer Cell, 2014 May 27; 25(6). PMID: 24856586    Free PMC article.
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Inflammation amplification by Versican: the first mediator.
Zhenwei Zhang, Lei Miao, Lianghua Wang.
Int J Mol Sci, 2012 Jul 28; 13(6). PMID: 22837669    Free PMC article.
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P S Linsley, J L Greene, +3 authors, R Peach.
Immunity, 1994 Dec 01; 1(9). PMID: 7534620
Highly Cited.
Targeting Matrix Metalloproteinases in Cancer: Bringing New Life to Old Ideas.
Jillian Cathcart, Ashleigh Pulkoski-Gross, Jian Cao.
Genes Dis, 2015 Jun 23; 2(`1). PMID: 26097889    Free PMC article.
Highly Cited.
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Shannon J Turley, Viviana Cremasco, Jillian L Astarita.
Nat Rev Immunol, 2015 Oct 17; 15(11). PMID: 26471778
Highly Cited. Review.
Hyaluronan: A modulator of the tumor microenvironment.
Theerawut Chanmee, Pawared Ontong, Naoki Itano.
Cancer Lett, 2016 Feb 28; 375(1). PMID: 26921785
Highly Cited. Review.
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Kurt A Schalper, Vamsidhar Velcheti, +4 authors, David L Rimm.
Clin Cancer Res, 2014 Mar 22; 20(10). PMID: 24647569
Highly Cited.
PD-L2 is a second ligand for PD-1 and inhibits T cell activation.
Y Latchman, C R Wood, +18 authors, G J Freeman.
Nat Immunol, 2001 Feb 27; 2(3). PMID: 11224527
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Biomarkers for Response of Melanoma Patients to Immune Checkpoint Inhibitors: A Systematic Review.
Charissa A C Jessurun, Julien A M Vos, Jacqueline Limpens, Rosalie M Luiten.
Front Oncol, 2017 Oct 17; 7. PMID: 29034210    Free PMC article.
Pembrolizumab versus docetaxel for previously treated, PD-L1-positive, advanced non-small-cell lung cancer (KEYNOTE-010): a randomised controlled trial.
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Lancet, 2015 Dec 30; 387(10027). PMID: 26712084
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Laminin-511: a multi-functional adhesion protein regulating cell migration, tumor invasion and metastasis.
Normand Pouliot, Nicole Kusuma.
Cell Adh Migr, 2012 Oct 19; 7(1). PMID: 23076212    Free PMC article.
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Yide Huang, Shu-Dong Zhang, +3 authors, Hang-Fai Kwok.
Oncol Rep, 2015 May 13; 33(6). PMID: 25963805
Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation.
G J Freeman, A J Long, +16 authors, T Honjo.
J Exp Med, 2000 Oct 04; 192(7). PMID: 11015443    Free PMC article.
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Baseline gut microbiota predicts clinical response and colitis in metastatic melanoma patients treated with ipilimumab.
N Chaput, P Lepage, +15 authors, F Carbonnel.
Ann Oncol, 2017 Apr 04; 28(6). PMID: 28368458
Highly Cited.
Versican and the control of inflammation.
Thomas N Wight, Inkyung Kang, Mervyn J Merrilees.
Matrix Biol, 2014 Feb 12; 35. PMID: 24513039    Free PMC article.
Highly Cited. Review.
ADAMTS proteases and cancer.
Santiago Cal, Carlos López-Otín.
Matrix Biol, 2015 Feb 01; 44-46. PMID: 25636539
Review.
Versican-Derived Matrikines Regulate Batf3-Dendritic Cell Differentiation and Promote T Cell Infiltration in Colorectal Cancer.
Chelsea Hope, Philip B Emmerich, +11 authors, Fotis Asimakopoulos.
J Immunol, 2017 Jul 30; 199(5). PMID: 28754680    Free PMC article.
Matrix metalloproteinase inhibitors (MMPIs): the beginning of phase I or the termination of phase III clinical trials.
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Axitinib in combination with pembrolizumab in patients with advanced renal cell cancer: a non-randomised, open-label, dose-finding, and dose-expansion phase 1b trial.
Michael B Atkins, Elizabeth R Plimack, +11 authors, Toni K Choueiri.
Lancet Oncol, 2018 Feb 15; 19(3). PMID: 29439857    Free PMC article.
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Marc G Achen, Bradley K McColl, Steven A Stacker.
Cancer Cell, 2005 Feb 16; 7(2). PMID: 15710325
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Sunhwa Kim, Michael Karin.
Ann N Y Acad Sci, 2011 Feb 01; 1217. PMID: 21276007    Free PMC article.
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Atezolizumab versus docetaxel in patients with previously treated non-small-cell lung cancer (OAK): a phase 3, open-label, multicentre randomised controlled trial.
Achim Rittmeyer, Fabrice Barlesi, +23 authors, OAK Study Group.
Lancet, 2016 Dec 17; 389(10066). PMID: 27979383    Free PMC article.
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Laminin-5 (laminin-332): Unique biological activity and role in tumor growth and invasion.
Kaoru Miyazaki.
Cancer Sci, 2006 Jan 31; 97(2). PMID: 16441418
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Chemokine expression in melanoma metastases associated with CD8+ T-cell recruitment.
Helena Harlin, Yuru Meng, +5 authors, Thomas F Gajewski.
Cancer Res, 2009 Mar 19; 69(7). PMID: 19293190    Free PMC article.
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In colorectal cancer mast cells contribute to systemic regulatory T-cell dysfunction.
Nichole R Blatner, Andreas Bonertz, +8 authors, Khashayarsha Khazaie.
Proc Natl Acad Sci U S A, 2010 Mar 24; 107(14). PMID: 20308560    Free PMC article.
Myeloid suppressor lines inhibit T cell responses by an NO-dependent mechanism.
Alessandra Mazzoni, Vincenzo Bronte, +5 authors, David M Segal.
J Immunol, 2002 Jan 05; 168(2). PMID: 11777962
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A decrease of regulatory T cells correlates with overall survival after sunitinib-based antiangiogenic therapy in metastatic renal cancer patients.
Olivier Adotevi, Helene Pere, +11 authors, Eric Tartour.
J Immunother, 2010 Oct 16; 33(9). PMID: 20948437
The prognostic landscape of genes and infiltrating immune cells across human cancers.
Andrew J Gentles, Aaron M Newman, +11 authors, Ash A Alizadeh.
Nat Med, 2015 Jul 21; 21(8). PMID: 26193342    Free PMC article.
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PD-L1 expression in the Merkel cell carcinoma microenvironment: association with inflammation, Merkel cell polyomavirus and overall survival.
Evan J Lipson, Jeremy G Vincent, +10 authors, Janis M Taube.
Cancer Immunol Res, 2014 Jan 15; 1(1). PMID: 24416729    Free PMC article.
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Proteolytic and non-proteolytic migration of tumour cells and leucocytes.
Peter Friedl, Katarina Wolf.
Biochem Soc Symp, 2003 Nov 01; (70). PMID: 14587300
Review.
Roles of versican in cancer biology--tumorigenesis, progression and metastasis.
William Weidong Du, Weining Yang, Albert J Yee.
Histol Histopathol, 2013 Mar 23; 28(6). PMID: 23519970
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Cancer microenvironment and inflammation: role of hyaluronan.
Dragana Nikitovic, Maria Tzardi, +2 authors, George N Tzanakakis.
Front Immunol, 2015 May 01; 6. PMID: 25926834    Free PMC article.
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Nivolumab for Recurrent Squamous-Cell Carcinoma of the Head and Neck.
Robert L Ferris, George Blumenschein, +20 authors, Maura L Gillison.
N Engl J Med, 2016 Oct 11; 375(19). PMID: 27718784    Free PMC article.
Highly Cited.
Genomic correlates of response to CTLA-4 blockade in metastatic melanoma.
Eliezer M Van Allen, Diana Miao, +19 authors, Levi A Garraway.
Science, 2015 Sep 12; 350(6257). PMID: 26359337    Free PMC article.
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In vitro and in vivo evidence for shear-induced activation of latent transforming growth factor-beta1.
Jasimuddin Ahamed, Nathalie Burg, +3 authors, Barry S Coller.
Blood, 2008 Jun 12; 112(9). PMID: 18544680    Free PMC article.
Tumor-associated macrophages as major players in the tumor microenvironment.
Theerawut Chanmee, Pawared Ontong, Kenjiro Konno, Naoki Itano.
Cancers (Basel), 2014 Aug 16; 6(3). PMID: 25125485    Free PMC article.
Highly Cited. Review.
Myeloid-derived suppressor cells in cancer: recent progress and prospects.
Yazan S Khaled, Basil J Ammori, Eyad Elkord.
Immunol Cell Biol, 2013 Jun 26; 91(8). PMID: 23797066
Highly Cited. Review.
Tumor angiogenesis is accompanied by a decreased inflammatory response of tumor-associated endothelium.
A W Griffioen, C A Damen, G H Blijham, G Groenewegen.
Blood, 1996 Jul 15; 88(2). PMID: 8695814
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H Dong, G Zhu, K Tamada, L Chen.
Nat Med, 1999 Dec 02; 5(12). PMID: 10581077
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Spatial distribution of B cells predicts prognosis in human pancreatic adenocarcinoma.
Giovanni Francesco Castino, Nina Cortese, +14 authors, Federica Marchesi.
Oncoimmunology, 2016 May 04; 5(4). PMID: 27141376    Free PMC article.
Nivolumab versus Docetaxel in Advanced Squamous-Cell Non-Small-Cell Lung Cancer.
Julie Brahmer, Karen L Reckamp, +22 authors, David R Spigel.
N Engl J Med, 2015 Jun 02; 373(2). PMID: 26028407    Free PMC article.
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STAT3 regulates arginase-I in myeloid-derived suppressor cells from cancer patients.
David Vasquez-Dunddel, Fan Pan, +9 authors, Young Kim.
J Clin Invest, 2013 Mar 05; 123(4). PMID: 23454751    Free PMC article.
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The matricellular functions of small leucine-rich proteoglycans (SLRPs).
Rosetta Merline, Roland M Schaefer, Liliana Schaefer.
J Cell Commun Signal, 2009 Oct 08; 3(3-4). PMID: 19809894    Free PMC article.
Fibroblast Activation Protein-α-Positive Fibroblasts Promote Gastric Cancer Progression and Resistance to Immune Checkpoint Blockade.
Xuyang Wen, Xiaoping He, +4 authors, Qianwen Li.
Oncol Res, 2016 Dec 17; 25(4). PMID: 27983931    Free PMC article.
Pembrolizumab for the treatment of non-small-cell lung cancer.
Edward B Garon, Naiyer A Rizvi, +25 authors, KEYNOTE-001 Investigators.
N Engl J Med, 2015 Apr 22; 372(21). PMID: 25891174
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Cutting edge: mast cells critically augment myeloid-derived suppressor cell activity.
Sheinei J Saleem, Rebecca K Martin, +7 authors, Daniel H Conrad.
J Immunol, 2012 Jun 19; 189(2). PMID: 22706087    Free PMC article.
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Mark A Travis, Dean Sheppard.
Annu Rev Immunol, 2013 Dec 10; 32. PMID: 24313777    Free PMC article.
Highly Cited. Review.
Programmed death ligand-1 expression in non-small cell lung cancer.
Vamsidhar Velcheti, Kurt A Schalper, +7 authors, David L Rimm.
Lab Invest, 2013 Nov 13; 94(1). PMID: 24217091    Free PMC article.
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Heparan Sulfate Proteoglycans May Promote or Inhibit Cancer Progression by Interacting with Integrins and Affecting Cell Migration.
Mariana A Soares, Felipe C O B Teixeira, +4 authors, Mariana P Stelling.
Biomed Res Int, 2015 Nov 12; 2015. PMID: 26558271    Free PMC article.
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Morgan Huse.
Nat Rev Immunol, 2017 Aug 02; 17(11). PMID: 28757604    Free PMC article.
Highly Cited. Review.
Sunitinib mediates reversal of myeloid-derived suppressor cell accumulation in renal cell carcinoma patients.
Jennifer S Ko, Arnold H Zea, +10 authors, James H Finke.
Clin Cancer Res, 2009 Mar 12; 15(6). PMID: 19276286
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Matrix architecture defines the preferential localization and migration of T cells into the stroma of human lung tumors.
Hélène Salmon, Katarzyna Franciszkiewicz, +5 authors, Emmanuel Donnadieu.
J Clin Invest, 2012 Feb 02; 122(3). PMID: 22293174    Free PMC article.
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Regulatory T Cells in the Tumor Microenvironment and Cancer Progression: Role and Therapeutic Targeting.
Belal Chaudhary, Eyad Elkord.
Vaccines (Basel), 2016 Aug 12; 4(3). PMID: 27509527    Free PMC article.
Highly Cited. Review.
Prognostic significance of Versican expression in gastric adenocarcinoma.
X-H Shen, W-R Lin, +12 authors, X Du.
Oncogenesis, 2015 Dec 01; 4. PMID: 26619403    Free PMC article.
Oncology meets immunology: the cancer-immunity cycle.
Daniel S Chen, Ira Mellman.
Immunity, 2013 Jul 31; 39(1). PMID: 23890059
Highly Cited. Review.
TGF-beta: a master of all T cell trades.
Ming O Li, Richard A Flavell.
Cell, 2008 Aug 12; 134(3). PMID: 18692464    Free PMC article.
Highly Cited. Review.
Glycosaminoglycans: key players in cancer cell biology and treatment.
Nikos Afratis, Chrisostomi Gialeli, +6 authors, Nikos K Karamanos.
FEBS J, 2012 Feb 16; 279(7). PMID: 22333131
Highly Cited. Review.
Programmed death-1 blockade enhances expansion and functional capacity of human melanoma antigen-specific CTLs.
Raymond M Wong, Ron R Scotland, +4 authors, Jeffrey S Weber.
Int Immunol, 2007 Sep 28; 19(10). PMID: 17898045
Genomic and Transcriptomic Features of Response to Anti-PD-1 Therapy in Metastatic Melanoma.
Willy Hugo, Jesse M Zaretsky, +15 authors, Roger S Lo.
Cell, 2016 Mar 22; 165(1). PMID: 26997480    Free PMC article.
Highly Cited.
Combined Nivolumab and Ipilimumab or Monotherapy in Untreated Melanoma.
James Larkin, Vanna Chiarion-Sileni, +28 authors, Jedd D Wolchok.
N Engl J Med, 2015 Jun 02; 373(1). PMID: 26027431    Free PMC article.
Highly Cited.
Prospective identification of neoantigen-specific lymphocytes in the peripheral blood of melanoma patients.
Alena Gros, Maria R Parkhurst, +11 authors, Steven A Rosenberg.
Nat Med, 2016 Feb 24; 22(4). PMID: 26901407    Free PMC article.
Highly Cited.
Endothelial and nonendothelial sources of PDGF-B regulate pericyte recruitment and influence vascular pattern formation in tumors.
Alexandra Abramsson, Per Lindblom, Christer Betsholtz.
J Clin Invest, 2003 Oct 17; 112(8). PMID: 14561699    Free PMC article.
Highly Cited.
Deconstruction of a Metastatic Tumor Microenvironment Reveals a Common Matrix Response in Human Cancers.
Oliver M T Pearce, Robin M Delaine-Smith, +22 authors, Frances R Balkwill.
Cancer Discov, 2017 Dec 03; 8(3). PMID: 29196464    Free PMC article.
Highly Cited.
Melanoma-educated CD14+ cells acquire a myeloid-derived suppressor cell phenotype through COX-2-dependent mechanisms.
Yumeng Mao, Isabel Poschke, +7 authors, Rolf Kiessling.
Cancer Res, 2013 May 02; 73(13). PMID: 23633486
Regulation of the Immune System by Laminins.
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Trends Immunol, 2017 Jul 08; 38(11). PMID: 28684207    Free PMC article.
Review.
Current status and perspectives in translational biomarker research for PD-1/PD-L1 immune checkpoint blockade therapy.
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J Hematol Oncol, 2016 May 29; 9(1). PMID: 27234522    Free PMC article.
Highly Cited. Review.
PD-1 Blockade in Tumors with Mismatch-Repair Deficiency.
Dung T Le, Jennifer N Uram, +32 authors, Luis A Diaz.
N Engl J Med, 2015 Jun 02; 372(26). PMID: 26028255    Free PMC article.
Highly Cited.
The commensal microbiome is associated with anti-PD-1 efficacy in metastatic melanoma patients.
Vyara Matson, Jessica Fessler, +5 authors, Thomas F Gajewski.
Science, 2018 Jan 06; 359(6371). PMID: 29302014    Free PMC article.
Highly Cited.
RhoGDI2 suppresses lung metastasis in mice by reducing tumor versican expression and macrophage infiltration.
Neveen Said, Marta Sanchez-Carbayo, Steven C Smith, Dan Theodorescu.
J Clin Invest, 2012 Mar 13; 122(4). PMID: 22406535    Free PMC article.
Transcriptome-based network analysis reveals a spectrum model of human macrophage activation.
Jia Xue, Susanne V Schmidt, +18 authors, Joachim L Schultze.
Immunity, 2014 Feb 18; 40(2). PMID: 24530056    Free PMC article.
Highly Cited.
The ADAMTS (A Disintegrin and Metalloproteinase with Thrombospondin motifs) family.
Richard Kelwick, Ines Desanlis, Grant N Wheeler, Dylan R Edwards.
Genome Biol, 2015 May 31; 16. PMID: 26025392    Free PMC article.
Highly Cited. Review.
Hyperproduction of hyaluronan in neu-induced mammary tumor accelerates angiogenesis through stromal cell recruitment: possible involvement of versican/PG-M.
Hiroshi Koyama, Terumasa Hibi, +8 authors, Naoki Itano.
Am J Pathol, 2007 Feb 27; 170(3). PMID: 17322391    Free PMC article.
Involvement of PD-L1 on tumor cells in the escape from host immune system and tumor immunotherapy by PD-L1 blockade.
Yoshiko Iwai, Masayoshi Ishida, +3 authors, Nagahiro Minato.
Proc Natl Acad Sci U S A, 2002 Sep 10; 99(19). PMID: 12218188    Free PMC article.
Highly Cited.
Endothelial Basement Membrane Laminin 511 Contributes to Endothelial Junctional Tightness and Thereby Inhibits Leukocyte Transmigration.
Jian Song, Xueli Zhang, +14 authors, Lydia Sorokin.
Cell Rep, 2017 Feb 02; 18(5). PMID: 28147279
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Review.
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Richard O Hynes.
Science, 2009 Dec 08; 326(5957). PMID: 19965464    Free PMC article.
Highly Cited. Review.
Genetic basis for clinical response to CTLA-4 blockade in melanoma.
Alexandra Snyder, Vladimir Makarov, +18 authors, Timothy A Chan.
N Engl J Med, 2014 Nov 20; 371(23). PMID: 25409260    Free PMC article.
Highly Cited.
Fc-dependent depletion of tumor-infiltrating regulatory T cells co-defines the efficacy of anti-CTLA-4 therapy against melanoma.
Tyler R Simpson, Fubin Li, +11 authors, Sergio A Quezada.
J Exp Med, 2013 Jul 31; 210(9). PMID: 23897981    Free PMC article.
Highly Cited.
Association of Somatic Mutations of ADAMTS Genes With Chemotherapy Sensitivity and Survival in High-Grade Serous Ovarian Carcinoma.
Yuexin Liu, Maya Yasukawa, +10 authors, Wei Zhang.
JAMA Oncol, 2015 Jul 17; 1(4). PMID: 26181259    Free PMC article.
B7-DC, a new dendritic cell molecule with potent costimulatory properties for T cells.
S Y Tseng, M Otsuji, +7 authors, H Tsuchiya.
J Exp Med, 2001 Apr 03; 193(7). PMID: 11283156    Free PMC article.
Highly Cited.
CTLA-4 blockade increases IFNgamma-producing CD4+ICOShi cells to shift the ratio of effector to regulatory T cells in cancer patients.
Chrysoula I Liakou, Ashish Kamat, +5 authors, Padmanee Sharma.
Proc Natl Acad Sci U S A, 2008 Sep 27; 105(39). PMID: 18818309    Free PMC article.
Highly Cited.
Intact extracellular matrix and the maintenance of immune tolerance: high molecular weight hyaluronan promotes persistence of induced CD4+CD25+ regulatory T cells.
Paul L Bollyky, Ben A Falk, +3 authors, Gerald T Nepom.
J Leukoc Biol, 2009 Apr 30; 86(3). PMID: 19401397    Free PMC article.
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Cold Spring Harb Perspect Biol, 2011 Sep 23; 4(1). PMID: 21937732    Free PMC article.
Highly Cited. Review.
Heparanase promotes tumor infiltration and antitumor activity of CAR-redirected T lymphocytes.
Ignazio Caruana, Barbara Savoldo, +6 authors, Gianpietro Dotti.
Nat Med, 2015 Apr 08; 21(5). PMID: 25849134    Free PMC article.
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YAP/TAZ Related BioMechano Signal Transduction and Cancer Metastasis.
Bridget Martinez, Yongchao Yang, +4 authors, David Mascareñas.
Front Cell Dev Biol, 2019 Oct 23; 7. PMID: 31637239    Free PMC article.
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Expression of TIM3/VISTA checkpoints and the CD68 macrophage-associated marker correlates with anti-PD1/PDL1 resistance: implications of immunogram heterogeneity.
Shumei Kato, Ryosuke Okamura, +11 authors, Razelle Kurzrock.
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Extracellular Matrix in the Tumor Microenvironment and Its Impact on Cancer Therapy.
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Review.
Non-invasive biomarkers derived from the extracellular matrix associate with response to immune checkpoint blockade (anti-CTLA-4) in metastatic melanoma patients.
Christina Jensen, Daniel Hargbøl Madsen, +4 authors, Nicholas Willumsen.
J Immunother Cancer, 2018 Dec 21; 6(1). PMID: 30567561    Free PMC article.
Increased intratumoral mast cells foster immune suppression and gastric cancer progression through TNF-α-PD-L1 pathway.
Yipin Lv, Yongliang Zhao, +16 authors, Yuan Zhuang.
J Immunother Cancer, 2019 Feb 28; 7(1). PMID: 30808413    Free PMC article.
Collagen density regulates the activity of tumor-infiltrating T cells.
Dorota E Kuczek, Anne Mette H Larsen, +12 authors, Daniel H Madsen.
J Immunother Cancer, 2019 Mar 15; 7(1). PMID: 30867051    Free PMC article.
Immunotherapy: breaching the barriers for cancer treatment.
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Mass Spectrometry-Based Multivariate Proteomic Tests for Prediction of Outcomes on Immune Checkpoint Blockade Therapy: The Modern Analytical Approach.
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Review.
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Elife, 2020 Mar 04; 9. PMID: 32122466    Free PMC article.
Cancer Immunotherapy Based on Natural Killer Cells: Current Progress and New Opportunities.
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Front Immunol, 2019 Jun 20; 10. PMID: 31214177    Free PMC article.
Highly Cited. Review.
miR-448 targets IDO1 and regulates CD8+ T cell response in human colon cancer.
Qiong Lou, Ruixian Liu, +8 authors, Huanliang Liu.
J Immunother Cancer, 2019 Aug 09; 7(1). PMID: 31391111    Free PMC article.
Extracellular Protease ADAMTS1 Is Required at Early Stages of Human Uveal Melanoma Development by Inducing Stemness and Endothelial-Like Features on Tumor Cells.
Carlos Peris-Torres, María Del Carmen Plaza-Calonge, +4 authors, Juan Carlos Rodríguez-Manzaneque.
Cancers (Basel), 2020 Apr 02; 12(4). PMID: 32230715    Free PMC article.
Integrating the Tumor Microenvironment into Cancer Therapy.
Sabina Sanegre, Federico Lucantoni, +3 authors, Tomás Álvaro Naranjo.
Cancers (Basel), 2020 Jul 01; 12(6). PMID: 32599891    Free PMC article.
Review.
Systematic Analysis of Aberrant Biochemical Networks and Potential Drug Vulnerabilities Induced by Tumor Suppressor Loss in Malignant Pleural Mesothelioma.
Haitang Yang, Duo Xu, +4 authors, Ren-Wang Peng.
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Concepts of extracellular matrix remodelling in tumour progression and metastasis.
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The nine ADAMs family members serve as potential biomarkers for immune infiltration in pancreatic adenocarcinoma.
Bing Qi, Han Liu, +8 authors, Shilin Xia.
PeerJ, 2020 Oct 17; 8. PMID: 33062410    Free PMC article.
Blood-based extracellular matrix biomarkers are correlated with clinical outcome after PD-1 inhibition in patients with metastatic melanoma.
Daan P Hurkmans, Christina Jensen, +4 authors, Nicholas Willumsen.
J Immunother Cancer, 2020 Oct 24; 8(2). PMID: 33093157    Free PMC article.
Granzyme B Degraded Type IV Collagen Products in Serum Identify Melanoma Patients Responding to Immune Checkpoint Blockade.
Christina Jensen, Dovile Sinkeviciute, +6 authors, Nicholas Willumsen.
Cancers (Basel), 2020 Oct 02; 12(10). PMID: 32998446    Free PMC article.
Cancer Extracellular Matrix Proteins Regulate Tumour Immunity.
Alex Gordon-Weeks, Arseniy E Yuzhalin.
Cancers (Basel), 2020 Nov 15; 12(11). PMID: 33187209    Free PMC article.
Review.
Versican and Versican-matrikines in Cancer Progression, Inflammation, and Immunity.
Athanasios Papadas, Garrett Arauz, +2 authors, Fotis Asimakopoulos.
J Histochem Cytochem, 2020 Jul 07; 68(12). PMID: 32623942    Free PMC article.
Review.
The Extracellular Matrix-Derived Biomarkers for Diagnosis, Prognosis, and Personalized Therapy of Malignant Tumors.
Elena V Petersen, Daria A Chudakova, +3 authors, Ospan A Mynbaev.
Front Oncol, 2021 Jan 12; 10. PMID: 33425730    Free PMC article.
Review.
Harnessing Extracellular Matrix Biology for Tumor Drug Delivery.
Nithya Subrahmanyam, Hamidreza Ghandehari.
J Pers Med, 2021 Feb 13; 11(2). PMID: 33572559    Free PMC article.
Review.
Identification of a 14-Gene Prognostic Signature for Diffuse Large B Cell Lymphoma (DLBCL).
Pengcheng Feng, Hongxia Li, +2 authors, Guixia Li.
Front Genet, 2021 Mar 02; 12. PMID: 33643388    Free PMC article.
ADAMTS proteases and the tumor immune microenvironment: Lessons from substrates and pathologies.
Silvia Redondo-García, Carlos Peris-Torres, Rita Caracuel-Peramos, Juan Carlos Rodríguez-Manzaneque.
Matrix Biol Plus, 2021 Mar 16; 9. PMID: 33718860    Free PMC article.
Review.
Prognostic and therapeutic implications of extracellular matrix associated gene signature in renal clear cell carcinoma.
Pankaj Ahluwalia, Meenakshi Ahluwalia, +5 authors, Ravindra Kolhe.
Sci Rep, 2021 Apr 09; 11(1). PMID: 33828127    Free PMC article.
An Extracellular Matrix-Based Signature Associated With Immune Microenvironment Predicts the Prognosis and Therapeutic Responses of Patients With Oesophageal Squamous Cell Carcinoma.
Hongpan Zhang, Qi Shi, +5 authors, Feng Li.
Front Mol Biosci, 2021 Apr 20; 8. PMID: 33869274    Free PMC article.
Identification of NTRK3 as a potential prognostic biomarker associated with tumor mutation burden and immune infiltration in bladder cancer.
Zhao Zhang, Yongbo Yu, +5 authors, Haitao Niu.
BMC Cancer, 2021 Apr 26; 21(1). PMID: 33894748    Free PMC article.
Potential Therapeutic Significance of Laminin in Head and Neck Squamous Carcinomas.
Nathalia Meireles Da Costa, Fábio A Mendes, +3 authors, Antonio Palumbo Júnior.
Cancers (Basel), 2021 May 01; 13(8). PMID: 33920762    Free PMC article.
Review.
Extracellular Vesicle Mediated Tumor-Stromal Crosstalk Within an Engineered Lung Cancer Model.
Kayla F Goliwas, Hannah M Ashraf, +8 authors, Jessy S Deshane.
Front Oncol, 2021 May 11; 11. PMID: 33968758    Free PMC article.
Identification of Prognostic Glycolysis-Related lncRNA Signature in Tumor Immune Microenvironment of Hepatocellular Carcinoma.
Yang Bai, Haiping Lin, +2 authors, Shi'an Yu.
Front Mol Biosci, 2021 May 11; 8. PMID: 33968985    Free PMC article.
Combined with interventional therapy, immunotherapy can create a new outlook for tumor treatment.
Tonglei Fang, Junyuan Xiao, +3 authors, Yingsheng Cheng.
Quant Imaging Med Surg, 2021 Jun 04; 11(6). PMID: 34079746    Free PMC article.
Review.
Immunological Significance of Prognostic DNA Methylation Sites in Hepatocellular Carcinoma.
Qianhui Xu, Yuanbo Hu, +8 authors, Wen Huang.
Front Mol Biosci, 2021 Jun 15; 8. PMID: 34124163    Free PMC article.
Identification of Genes Related to Immune Infiltration in the Tumor Microenvironment of Cutaneous Melanoma.
Rujia Qin, Wen Peng, +4 authors, Chuanzheng Sun.
Front Oncol, 2021 Jun 18; 11. PMID: 34136377    Free PMC article.
Development and validation of ferroptosis-related lncRNAs signature for hepatocellular carcinoma.
Jiaying Liang, Yaofeng Zhi, +13 authors, Jin Zhang.
PeerJ, 2021 Jun 29; 9. PMID: 34178478    Free PMC article.
The Cancer-Immunity Cycle in Multiple Myeloma.
Mika Casey, Kyohei Nakamura.
Immunotargets Ther, 2021 Jul 24; 10. PMID: 34295843    Free PMC article.
Review.
Comprehensive analysis of an immune-related ceRNA network in identifying a novel lncRNA signature as a prognostic biomarker for hepatocellular carcinoma.
Rui Chen, Yunlong Chen, +5 authors, Jian Yang.
Aging (Albany NY), 2021 Jul 09; 13(13). PMID: 34237706    Free PMC article.
The Efficacy of Anti-PD-L1 Treatment in Melanoma Is Associated with the Expression of the ECM Molecule EMILIN2.
Albina Fejza, Maurizio Polano, +5 authors, Eva Andreuzzi.
Int J Mol Sci, 2021 Jul 25; 22(14). PMID: 34299131    Free PMC article.
Human Hyaluronidase PH20 Potentiates the Antitumor Activities of Mesothelin-Specific CAR-T Cells Against Gastric Cancer.
Ruocong Zhao, Yuanbin Cui, +13 authors, Peng Li.
Front Immunol, 2021 Jul 31; 12. PMID: 34326835    Free PMC article.
Endogenous and Therapeutic Estrogens: Maestro Conductors of the Microenvironment of ER+ Breast Cancers.
Linda A Schuler, Fern E Murdoch.
Cancers (Basel), 2021 Aug 08; 13(15). PMID: 34359625    Free PMC article.
Review.
Landscape of Prognostic m6A RNA Methylation Regulators in Hepatocellular Carcinoma to Aid Immunotherapy.
Qianhui Xu, Hao Xu, +9 authors, Wen Huang.
Front Cell Dev Biol, 2021 Aug 24; 9. PMID: 34422799    Free PMC article.
Targeting Versican as a Potential Immunotherapeutic Strategy in the Treatment of Cancer.
Priyanka Hirani, Valentine Gauthier, +2 authors, Oliver M T Pearce.
Front Oncol, 2021 Sep 17; 11. PMID: 34527586    Free PMC article.
Review.
Extracellular Matrix Enzymes and Immune Cell Biology.
Meagan McMahon, Siying Ye, +2 authors, John Stambas.
Front Mol Biosci, 2021 Sep 17; 8. PMID: 34527702    Free PMC article.
Review.
Role of Toll-like receptors in natural killer cell function in acute lymphoblastic leukemia.
Janet Gallardo-Zapata, Carmen Maldonado-Bernal.
Oncol Lett, 2021 Sep 21; 22(5). PMID: 34539852    Free PMC article.
Review.
Prognostic Role of ceRNA Network in Immune Infiltration of Hepatocellular Carcinoma.
Qianhui Xu, Shaohuai Chen, Yuanbo Hu, Wen Huang.
Front Genet, 2021 Oct 01; 12. PMID: 34589117    Free PMC article.
Serological assessment of collagen fragments and tumor fibrosis may guide immune checkpoint inhibitor therapy.
Christina Jensen, Neel I Nissen, +2 authors, Nicholas Willumsen.
J Exp Clin Cancer Res, 2021 Oct 18; 40(1). PMID: 34656158    Free PMC article.
Review.
Clinical M2 macrophages-related genes to aid therapy in pancreatic ductal adenocarcinoma.
Qianhui Xu, Shaohuai Chen, Yuanbo Hu, Wen Huang.
Cancer Cell Int, 2021 Nov 01; 21(1). PMID: 34717651    Free PMC article.
Interrogation of the Microenvironmental Landscape in Brain Tumors Reveals Disease-Specific Alterations of Immune Cells.
Florian Klemm, Roeltje R Maas, +11 authors, Johanna A Joyce.
Cell, 2020 May 30; 181(7). PMID: 32470396    Free PMC article.
The BRD9/7 Inhibitor TP-472 Blocks Melanoma Tumor Growth by Suppressing ECM-Mediated Oncogenic Signaling and Inducing Apoptosis.
Lawrence David Mason, Suresh Chava, Kiran Kumar Reddi, Romi Gupta.
Cancers (Basel), 2021 Nov 14; 13(21). PMID: 34771678    Free PMC article.
Stromal Characteristics and Impact on New Therapies for Metastatic Triple-Negative Breast Cancer.
Shelby A Fertal, Johanna E Poterala, Suzanne M Ponik, Kari B Wisinski.
Cancers (Basel), 2022 Mar 11; 14(5). PMID: 35267548    Free PMC article.
Review.
Is an Immunosuppressive Microenvironment a Characteristic of Both Intra- and Extraparenchymal Central Nervous Tumors?
Amina Soltani, Bela Kajtar, +5 authors, Judit E Pongracz.
Pathophysiology, 2021 Jan 08; 28(1). PMID: 35366268    Free PMC article.
Fibrotic activity quantified in serum by measurements of type III collagen pro-peptides can be used for prognosis across different solid tumor types.
Nicholas Willumsen, Christina Jensen, +22 authors, Morten A Karsdal.
Cell Mol Life Sci, 2022 Mar 26; 79(4). PMID: 35332383    Free PMC article.
Review.
Extracellular Matrix-Based Gene Expression Signature Defines Two Prognostic Subtypes of Hepatocellular Carcinoma With Different Immune Microenvironment Characteristics.
Hui Tang, Tingting You, +2 authors, Yingyi Wang.
Front Mol Biosci, 2022 Apr 12; 9. PMID: 35402515    Free PMC article.