Cited by 305Pancreatic and Hepatic Oncology ResearchCancer Immunotherapy and BiomarkersTGF-β signaling in diseases

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Oncogenic collagen I homotrimers from cancer cells bind to α3β1 integrin and impact tumor microbiome and immunity to promote pancreatic cancer

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Chen, Yang, Yang, Sujuan, Tavormina, Jena, Tampe, Desiree, Zeisberg, Michael, Wang, Huamin, Mahadevan, Krishnan K., Wu, Chang-Jiun, Sugimoto, Hikaru, Chang, Chia-Chi, Jenq, Robert R., McAndrews, Kathleen M., Kalluri, Raghu·2022·Cancer Cell

DOI 10.1016/j.ccell.2022.06.011PMC PMC9831277

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Abstract

In contrast to normal type I collagen (Col1) heterotrimer (α1/α2/α1) produced by fibroblasts, pancreatic cancer cells specifically produce unique Col1 homotrimer (α1/α1/α1). Col1 homotrimer results from epigenetic suppression of the Col1a2 gene and promotes oncogenic signaling, cancer cell proliferation, tumor organoid formation, and growth via α3β1 integrin on cancer cells, associated with tumor microbiome enriched in anaerobic Bacteroidales in hypoxic and immunosuppressive tumors. Deletion of Col1 homotrimers increases overall survival of mice with pancreatic ductal adenocarcinoma (PDAC), associated with reprograming of the tumor microbiome with increased microaerophilic Campylobacterales, which can be reversed with broad-spectrum antibiotics. Deletion of Col1 homotrimers enhances T cell infiltration and enables efficacy of anti-PD-1 immunotherapy. This study identifies the functional impact of Col1 homotrimers on tumor microbiome and tumor immunity, implicating Col1 homotrimer-α3β1 integrin signaling axis as a cancer-specific therapeutic target.

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Additional file 5 of Identification of fibronectin type III domain containing 3B as a potential prognostic and therapeutic target for pancreatic cancer: a preliminary analysis
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Additional file 7 of Identification of fibronectin type III domain containing 3B as a potential prognostic and therapeutic target for pancreatic cancer: a preliminary analysis
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Additional file 6 of Cirrhotic-extracellular matrix attenuates aPD-1 treatment response by initiating immunosuppressive neutrophil extracellular traps formation in hepatocellular carcinoma
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Additional file 8 of Identification of fibronectin type III domain containing 3B as a potential prognostic and therapeutic target for pancreatic cancer: a preliminary analysis
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Additional file 3 of Cirrhotic-extracellular matrix attenuates aPD-1 treatment response by initiating immunosuppressive neutrophil extracellular traps formation in hepatocellular carcinoma
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Additional file 14 of Cirrhotic-extracellular matrix attenuates aPD-1 treatment response by initiating immunosuppressive neutrophil extracellular traps formation in hepatocellular carcinoma
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Additional file 10 of Cirrhotic-extracellular matrix attenuates aPD-1 treatment response by initiating immunosuppressive neutrophil extracellular traps formation in hepatocellular carcinoma
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Additional file 12 of Weighted gene coexpression network analysis and machine learning reveal oncogenome associated microbiome plays an important role in tumor immunity and prognosis in pan-cancer
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Additional file 1 of Identification of fibronectin type III domain containing 3B as a potential prognostic and therapeutic target for pancreatic cancer: a preliminary analysis
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Additional file 2 of Identification of fibronectin type III domain containing 3B as a potential prognostic and therapeutic target for pancreatic cancer: a preliminary analysis
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Additional file 12 of Cirrhotic-extracellular matrix attenuates aPD-1 treatment response by initiating immunosuppressive neutrophil extracellular traps formation in hepatocellular carcinoma
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Additional file 6 of Identification of fibronectin type III domain containing 3B as a potential prognostic and therapeutic target for pancreatic cancer: a preliminary analysis
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Additional file 4 of Cirrhotic-extracellular matrix attenuates aPD-1 treatment response by initiating immunosuppressive neutrophil extracellular traps formation in hepatocellular carcinoma
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Additional file 7 of Cirrhotic-extracellular matrix attenuates aPD-1 treatment response by initiating immunosuppressive neutrophil extracellular traps formation in hepatocellular carcinoma
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Additional file 2 of Cirrhotic-extracellular matrix attenuates aPD-1 treatment response by initiating immunosuppressive neutrophil extracellular traps formation in hepatocellular carcinoma
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Additional file 10 of Weighted gene coexpression network analysis and machine learning reveal oncogenome associated microbiome plays an important role in tumor immunity and prognosis in pan-cancer
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Additional file 1 of Weighted gene coexpression network analysis and machine learning reveal oncogenome associated microbiome plays an important role in tumor immunity and prognosis in pan-cancer
Guan, S., Lin, Q., Wu, X.-D., & Yu, H.-B. (2024) · Figshare · doi:10.6084/m9.figshare.26610069
Additional file 4 of Weighted gene coexpression network analysis and machine learning reveal oncogenome associated microbiome plays an important role in tumor immunity and prognosis in pan-cancer
Guan, S., Lin, Q., Wu, X.-D., & Yu, H.-B. (2024) · Figshare · doi:10.6084/m9.figshare.26610093
Additional file 2 of Alterations of the bile microbiome is associated with progression-free survival in pancreatic ductal adenocarcinoma patients
Jiang, H., Tian, Y., Xu, L., Chen, X., Huang, Y., Wu, J., Wang, T., Liu, T., Wu, X., Ye, C., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26741486
Additional file 6 of Weighted gene coexpression network analysis and machine learning reveal oncogenome associated microbiome plays an important role in tumor immunity and prognosis in pan-cancer
Guan, S.-W., Lin, Q., Wu, X.-D., & Yu, H.-B. (2024) · Figshare · doi:10.6084/m9.figshare.26610108
Additional file 8 of Weighted gene coexpression network analysis and machine learning reveal oncogenome associated microbiome plays an important role in tumor immunity and prognosis in pan-cancer
Guan, S.-W., Lin, Q., Wu, X.-D., & Yu, H.-B. (2024) · Figshare · doi:10.6084/m9.figshare.26610114
Additional file 2 of Weighted gene coexpression network analysis and machine learning reveal oncogenome associated microbiome plays an important role in tumor immunity and prognosis in pan-cancer
Guan, S.-W., Lin, Q., Wu, X.-D., & Yu, H.-B. (2024) · Figshare · doi:10.6084/m9.figshare.26610072
Additional file 9 of Identification of fibronectin type III domain containing 3B as a potential prognostic and therapeutic target for pancreatic cancer: a preliminary analysis
Wang, Y., Kong, Y., Yang, Q., Zhong, C., & Zhou, D. (2024) · Figshare · doi:10.6084/m9.figshare.26702533
Additional file 1 of Cirrhotic-extracellular matrix attenuates aPD-1 treatment response by initiating immunosuppressive neutrophil extracellular traps formation in hepatocellular carcinoma
Shen, X., Xie, S.-Z., Zheng, X., Zou, T., Hu, B., Xu, J., Liu, L., Xu, Y.-F., Wang, X., Wang, H., et al. (2024) · Figshare · doi:10.6084/m9.figshare.25271793
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Additional file 3 of Identification of fibronectin type III domain containing 3B as a potential prognostic and therapeutic target for pancreatic cancer: a preliminary analysis
Wang, Y., Kong, Y., Yang, Q., Zhong, C., & Zhou, D. (2024) · Figshare · doi:10.6084/m9.figshare.26702512
Additional file 5 of Cirrhotic-extracellular matrix attenuates aPD-1 treatment response by initiating immunosuppressive neutrophil extracellular traps formation in hepatocellular carcinoma
Shen, X.-T., Xie, S.-Z., Zheng, X., Zou, T., Hu, B., Xu, J., Liu, L., Xu, Y.-F., Wang, X., Wang, H., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26684379
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Additional file 11 of Weighted gene coexpression network analysis and machine learning reveal oncogenome associated microbiome plays an important role in tumor immunity and prognosis in pan-cancer
Guan, S., Lin, Q., Wu, X.-D., & Yu, H.-B. (2024) · Figshare · doi:10.6084/m9.figshare.26610123
Additional file 13 of Cirrhotic-extracellular matrix attenuates aPD-1 treatment response by initiating immunosuppressive neutrophil extracellular traps formation in hepatocellular carcinoma
Shen, X., Xie, S.-Z., Zheng, X., Zou, T., Hu, B.-Y., Xu, J., Liu, L., Xu, Y.-F., Wang, X.-F., Wang, H., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26684403
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Additional file 15 of Cirrhotic-extracellular matrix attenuates aPD-1 treatment response by initiating immunosuppressive neutrophil extracellular traps formation in hepatocellular carcinoma
Shen, X.-T., Xie, S.-Z., Zheng, X., Zou, T., Hu, B.-Y., Xu, J., Liu, L., Xu, Y.-F., Wang, X.-F., Wang, H., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26684409
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Additional file 9 of Cirrhotic-extracellular matrix attenuates aPD-1 treatment response by initiating immunosuppressive neutrophil extracellular traps formation in hepatocellular carcinoma
Shen, X., Xie, S.-Z., Zheng, X., Zou, T., Hu, B.-Y., Xu, J., Liu, L., Xu, Y.-F., Wang, X., Wang, H., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26684391
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Additional file 9 of Weighted gene coexpression network analysis and machine learning reveal oncogenome associated microbiome plays an important role in tumor immunity and prognosis in pan-cancer
Guan, S., Lin, Q., Wu, X.-D., & Yu, H.-B. (2024) · Figshare · doi:10.6084/m9.figshare.26610117
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Authors: Chen, Y., Yang, S., Tavormina, J., Tampe, D., Zeisberg, M., Wang, H., Mahadevan, K. K., Wu, C.-J., Sugimoto, H., Chang, C.-C., Jenq, R. R., McAndrews, K. M., & Kalluri, R.
Affiliations: The University of Texas MD Anderson Cancer Center (US)
Universitätsmedizin Göttingen (DE)
Corresponding author: Kalluri, Raghu
ORCID: Chen, Yang
Yang, Sujuan
Tavormina, Jena
Zeisberg, Michael
Wang, Huamin
Mahadevan, Krishnan K.
Wu, Chang-Jiun
Sugimoto, Hikaru
Chang, Chia-Chi
Jenq, Robert R.
McAndrews, Kathleen M.
Kalluri, Raghu
Venue: Cancer Cell
Publisher: Elsevier BV
Published: 2022-08
Volume: 40
Issue: 8
Pages: 818-834.e9
ISSN: 1535-6108 (ISSN-L)
DOI: 10.1016/j.ccell.2022.06.011
PMC: PMC9831277
OpenAlex: W4286267917
Cited by: 289
References: 69
Citations by year: 2026: 48 · 2025: 82 · 2024: 100 · 2023: 49 · 2022: 10
FWCI: 26.79
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 372 d)
doi.org/10.15223/policy-017 (stm-asf)
doi.org/10.15223/policy-037 (stm-asf)
doi.org/10.15223/policy-012 (stm-asf)
doi.org/10.15223/policy-029 (stm-asf)
doi.org/10.15223/policy-004 (stm-asf)
Locations: Cancer Cell (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Digital Commons-TMC (Texas Medical Center) (submittedVersion)
Funders: Sid W. Richardson Foundation (P30CA016672)
National Cancer Institute (P01CA117969, P30CA16672)
Topics: Health Sciences › Medicine › Oncology › Pancreatic and Hepatic Oncology Research
Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › TGF-β signaling in diseases
Keywords: alpha3beta1 integrin, pancreatic ductal adenocarcinoma, tumor microbiome, Bacteroidales, Campylobacterales, tumor hypoxia, immunosuppression, T cell infiltration, anti-PD-1 therapy, antitumor immunity, tumor organoids, tumor cell proliferation
MeSH terms: Animals, Collagen, Pancreatic Neoplasms, Carcinoma, Pancreatic Ductal, Collagen Type I, Integrin alpha3beta1, Mice, Carcinogenesis, Microbiota

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Oncogenic collagen I homotrimers from cancer cells bind to α3β1 integrin and impact tumor microbiome and immunity to promote pancreatic cancer

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