THBS1-producing tumor-infiltrating monocyte-like cells contribute to immunosuppression and metastasis in colorectal cancer.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
25 09 2023
Historique:
received: 11 01 2023
accepted: 23 08 2023
medline: 27 9 2023
pubmed: 26 9 2023
entrez: 25 9 2023
Statut: epublish

Résumé

Mesenchymal activation, characterized by dense stromal infiltration of immune and mesenchymal cells, fuels the aggressiveness of colorectal cancers (CRC), driving progression and metastasis. Targetable molecules in the tumor microenvironment (TME) need to be identified to improve the outcome in CRC patients with this aggressive phenotype. This study reports a positive link between high thrombospondin-1 (THBS1) expression and mesenchymal characteristics, immunosuppression, and unfavorable CRC prognosis. Bone marrow-derived monocyte-like cells recruited by CXCL12 are the primary source of THBS1, which contributes to the development of metastasis by inducing cytotoxic T-cell exhaustion and impairing vascularization. Furthermore, in orthotopically generated CRC models in male mice, THBS1 loss in the TME renders tumors partially sensitive to immune checkpoint inhibitors and anti-cancer drugs. Our study establishes THBS1 as a potential biomarker for identifying mesenchymal CRC and as a critical suppressor of antitumor immunity that contributes to the progression of this malignancy with a poor prognosis.

Identifiants

pubmed: 37749092
doi: 10.1038/s41467-023-41095-y
pii: 10.1038/s41467-023-41095-y
pmc: PMC10520015
doi:

Substances chimiques

Immune Checkpoint Inhibitors 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

5534

Informations de copyright

© 2023. Springer Nature Limited.

Références

Cancer Cell. 2023 Feb 13;41(2):252-271.e9
pubmed: 36525970
Am J Physiol Endocrinol Metab. 2018 Dec 1;315(6):E1194-E1203
pubmed: 30351986
Cell. 2018 Nov 1;175(4):1014-1030.e19
pubmed: 30343900
Cell. 2019 Feb 7;176(4):775-789.e18
pubmed: 30595452
Proc Natl Acad Sci U S A. 2017 Nov 21;114(47):E10151-E10160
pubmed: 29109283
Nat Med. 2013 May;19(5):614-8
pubmed: 23584090
Nat Genet. 2022 Jul;54(7):963-975
pubmed: 35773407
Nat Rev Immunol. 2023 Feb;23(2):106-120
pubmed: 35697799
Cell Metab. 2021 May 4;33(5):1001-1012.e5
pubmed: 33691090
Cell. 2020 Aug 20;182(4):1044-1061.e18
pubmed: 32795414
Clin Cancer Res. 2016 Aug 15;22(16):4057-66
pubmed: 26994146
Genome Biol. 2022 May 11;23(1):113
pubmed: 35538548
Nat Med. 2002 Apr;8(4):349-57
pubmed: 11927940
J Immunol. 2001 Feb 15;166(4):2427-36
pubmed: 11160302
J Biol Chem. 1995 Mar 31;270(13):7304-10
pubmed: 7706271
Nat Med. 2015 Nov;21(11):1350-6
pubmed: 26457759
Cell. 2011 Mar 4;144(5):646-74
pubmed: 21376230
Sci Immunol. 2021 Oct;6(64):eabg7836
pubmed: 34597124
N Engl J Med. 2015 Jun 25;372(26):2509-20
pubmed: 26028255
Sci Rep. 2017 Nov 30;7(1):16618
pubmed: 29192179
J Clin Oncol. 2008 Dec 1;26(34):5583-8
pubmed: 18981463
J Biol Chem. 1999 May 7;274(19):13586-93
pubmed: 10224129
Dev Cell. 2021 Jan 11;56(1):95-110.e10
pubmed: 33207226
Cell Commun Signal. 2019 Sep 10;17(1):119
pubmed: 31500630
Nat Rev Immunol. 2009 Mar;9(3):162-74
pubmed: 19197294
Biochem Biophys Res Commun. 1990 Jul 31;170(2):867-72
pubmed: 1696478
J Hepatol. 2013 Aug;59(2):318-26
pubmed: 23624001
Mucosal Immunol. 2014 Mar;7(2):440-8
pubmed: 24045574
Genome Biol. 2019 Dec 23;20(1):296
pubmed: 31870423
Nat Genet. 2015 Apr;47(4):320-9
pubmed: 25706628
Cell. 2021 Jun 24;184(13):3573-3587.e29
pubmed: 34062119
Immunity. 2018 Dec 18;49(6):1132-1147.e7
pubmed: 30552022
Nat Genet. 2020 Jun;52(6):594-603
pubmed: 32451460
Immunity. 2017 Aug 15;47(2):323-338.e6
pubmed: 28813661
Nat Methods. 2012 Jun 28;9(7):676-82
pubmed: 22743772
Nature. 2018 Feb 22;554(7693):538-543
pubmed: 29443964
Nat Commun. 2019 Mar 8;10(1):1146
pubmed: 30850588
Science. 2020 Dec 11;370(6522):1328-1334
pubmed: 33303615
Sci Rep. 2017 Dec 4;7(1):16878
pubmed: 29203879
J Immunol. 2007 May 1;178(9):5930-9
pubmed: 17442977
Nat Rev Cancer. 2016 Aug 23;16(9):582-98
pubmed: 27550820
J Cell Biol. 1997 Aug 11;138(3):707-17
pubmed: 9245797
Cell. 2020 Apr 16;181(2):442-459.e29
pubmed: 32302573
Annu Rev Med. 2015;66:97-110
pubmed: 25341012
J Immunol. 2012 Nov 1;189(9):4426-36
pubmed: 23018457
Nat Med. 2000 Jan;6(1):41-8
pubmed: 10613822
Clin Cancer Res. 2007 Nov 15;13(22 Pt 1):6689-95
pubmed: 18006769
Matrix Biol. 2012 Apr;31(3):178-86
pubmed: 22266026
Proc Natl Acad Sci U S A. 2010 Feb 2;107(5):2177-82
pubmed: 20080664
Cell. 2021 Sep 16;184(19):5031-5052.e26
pubmed: 34534465
Adv Exp Med Biol. 2020;1272:133-147
pubmed: 32845506
Am J Clin Oncol. 2007 Jun;30(3):303-9
pubmed: 17551310
Bioinformatics. 2014 Apr 1;30(7):1015-6
pubmed: 24371154
Arterioscler Thromb Vasc Biol. 2020 Dec;40(12):e350-e366
pubmed: 33028100

Auteurs

Mayuki Omatsu (M)

Department of Gastroenterology and Hepatology, Kyoto University Graduate School of Medicine, Kyoto, Japan.

Yuki Nakanishi (Y)

Department of Gastroenterology and Hepatology, Kyoto University Graduate School of Medicine, Kyoto, Japan. yuki@kuhp.kyoto-u.ac.jp.

Kosuke Iwane (K)

Department of Gastroenterology and Hepatology, Kyoto University Graduate School of Medicine, Kyoto, Japan.

Naoki Aoyama (N)

Department of Gastroenterology and Hepatology, Kyoto University Graduate School of Medicine, Kyoto, Japan.

Angeles Duran (A)

Department of Pathology and Laboratory Medicine, Weill Cornell Medicine, New York, USA.

Yu Muta (Y)

Department of Pathology and Laboratory Medicine, Weill Cornell Medicine, New York, USA.
Department of Gastroenterology and Hepatology, Kyoto University Graduate School of Medicine, Kyoto, Japan.

Anxo Martinez-Ordoñez (A)

Department of Pathology and Laboratory Medicine, Weill Cornell Medicine, New York, USA.

Qixiu Han (Q)

Department of Pathology and Laboratory Medicine, Weill Cornell Medicine, New York, USA.

Nobukazu Agatsuma (N)

Department of Gastroenterology and Hepatology, Kyoto University Graduate School of Medicine, Kyoto, Japan.

Kenta Mizukoshi (K)

Department of Gastroenterology and Hepatology, Kyoto University Graduate School of Medicine, Kyoto, Japan.

Munenori Kawai (M)

Department of Gastroenterology and Hepatology, Kyoto University Graduate School of Medicine, Kyoto, Japan.

Go Yamakawa (G)

Department of Gastroenterology and Hepatology, Kyoto University Graduate School of Medicine, Kyoto, Japan.

Mio Namikawa (M)

Department of Gastroenterology and Hepatology, Kyoto University Graduate School of Medicine, Kyoto, Japan.

Kensuke Hamada (K)

Department of Gastroenterology and Hepatology, Kyoto University Graduate School of Medicine, Kyoto, Japan.

Yuichi Fukunaga (Y)

Department of Gastroenterology and Hepatology, Kyoto University Graduate School of Medicine, Kyoto, Japan.
Cancer Research Unit, Sumitomo Pharma Co., Ltd, Osaka, Japan.

Takahiro Utsumi (T)

Department of Gastroenterology and Hepatology, Kyoto University Graduate School of Medicine, Kyoto, Japan.

Makoto Sono (M)

Department of Gastroenterology and Hepatology, Kyoto University Graduate School of Medicine, Kyoto, Japan.

Tomonori Masuda (T)

Department of Gastroenterology and Hepatology, Kyoto University Graduate School of Medicine, Kyoto, Japan.

Akitaka Hata (A)

Department of Dermatology, Kyoto University Graduate School of Medicine, Kyoto, Japan.

Osamu Araki (O)

Department of Gastroenterology and Hepatology, Kyoto University Graduate School of Medicine, Kyoto, Japan.

Munemasa Nagao (M)

Department of Gastroenterology and Hepatology, Kyoto University Graduate School of Medicine, Kyoto, Japan.

Takaaki Yoshikawa (T)

Department of Gastroenterology and Hepatology, Kyoto University Graduate School of Medicine, Kyoto, Japan.

Satoshi Ogawa (S)

Department of Gastroenterology and Hepatology, Kyoto University Graduate School of Medicine, Kyoto, Japan.

Yukiko Hiramatsu (Y)

Department of Gastroenterology and Hepatology, Kyoto University Graduate School of Medicine, Kyoto, Japan.

Motoyuki Tsuda (M)

Department of Gastroenterology and Hepatology, Kyoto University Graduate School of Medicine, Kyoto, Japan.

Takahisa Maruno (T)

Department of Gastroenterology and Hepatology, Kyoto University Graduate School of Medicine, Kyoto, Japan.

Toshiaki Kogame (T)

Department of Dermatology, Kyoto University Graduate School of Medicine, Kyoto, Japan.

Hiroaki Kasashima (H)

Department of Gastroenterological Surgery, Osaka Metropolitan University, Osaka, Japan.

Nobuyuki Kakiuchi (N)

Department of Gastroenterology and Hepatology, Kyoto University Graduate School of Medicine, Kyoto, Japan.
The Hakubi Center for Advanced Research, Kyoto University, Kyoto, Japan.

Masahiro M Nakagawa (MM)

Department of Pathology and Tumor Biology, Kyoto University, Kyoto, Japan.

Kenji Kawada (K)

Department of Gastrointestinal Surgery, Kyoto University, Graduate School of Medicine, Kyoto, Japan.

Masakazu Yashiro (M)

Department of Gastroenterological Surgery, Osaka Metropolitan University, Osaka, Japan.

Kiyoshi Maeda (K)

Department of Gastroenterological Surgery, Osaka Metropolitan University, Osaka, Japan.

Yasuyuki Saito (Y)

Division of Molecular and Cellular Signaling, Department of Biochemistry and Molecular Biology, Kobe University Graduate School of Medicine, Kobe, Japan.

Takashi Matozaki (T)

Division of Molecular and Cellular Signaling, Department of Biochemistry and Molecular Biology, Kobe University Graduate School of Medicine, Kobe, Japan.
Division of Biosignal Regulation, Department of Biochemistry and Molecular Biology, Kobe University Graduate School of Medicine, Kobe, Japan.

Akihisa Fukuda (A)

Department of Gastroenterology and Hepatology, Kyoto University Graduate School of Medicine, Kyoto, Japan.

Kenji Kabashima (K)

Department of Dermatology, Kyoto University Graduate School of Medicine, Kyoto, Japan.

Kazutaka Obama (K)

Department of Gastrointestinal Surgery, Kyoto University, Graduate School of Medicine, Kyoto, Japan.

Seishi Ogawa (S)

Department of Pathology and Tumor Biology, Kyoto University, Kyoto, Japan.

Nader Sheibani (N)

Department of Ophthalmology and Visual Sciences, University of Wisconsin-, Madison, Wisconsin, USA.

Maria T Diaz-Meco (MT)

Department of Pathology and Laboratory Medicine, Weill Cornell Medicine, New York, USA.

Jorge Moscat (J)

Department of Pathology and Laboratory Medicine, Weill Cornell Medicine, New York, USA.

Hiroshi Seno (H)

Department of Gastroenterology and Hepatology, Kyoto University Graduate School of Medicine, Kyoto, Japan.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH