Analysis of Unfolded Protein Response Activation in Colon Adenocarcinoma Epithelial Cells: A Proteomic Study.
LC‐MS/MS
colorectal cancer
endoplasmic reticulum stress
epithelial cells
unfolded protein response
Journal
Proteomics. Clinical applications
ISSN: 1862-8354
Titre abrégé: Proteomics Clin Appl
Pays: Germany
ID NLM: 101298608
Informations de publication
Date de publication:
03 Sep 2024
03 Sep 2024
Historique:
revised:
26
07
2024
received:
02
02
2024
accepted:
22
08
2024
medline:
3
9
2024
pubmed:
3
9
2024
entrez:
3
9
2024
Statut:
aheadofprint
Résumé
High throughput technologies have identified molecular patterns in colorectal cancer (CRC) cells, aiding in modeling responses to anti-cancer treatments. The different responses observed depend on the type of cancer, the tumour grade and the functional programme of the cancer cells. Recent studies suggest that the unfolded protein response (UPR), autophagy and apoptosis could be involved in treatment resistance mechanisms by interacting with the tumour microenvironment (TME). We analysed by LC-MS/MS the proteome of two representative colon adenocarcinoma epithelial cell lines from different tumour grades (CCL-233 and CCL-221) at the basal state or after the UPR induction. Cell lines expressed a different proteome on about 10% of their total proteins identified, especially on UPR, autophagy and apoptosis pathways proteins at basal state. After UPR induction, the proteome of the cells was modified with a greater adaptive response to cellular stress in CCL-221 cells where the UPR was strongly activated at the basal state. CRC cell lines at different tumour grades expressed different functional programmes at the proteomic level and were characterised by different responses to the UPR induction. This study suggests that baseline cancer cell stress status could have an impact on the efficiency of cancer therapies.
Identifiants
pubmed: 39226110
doi: 10.1002/prca.202400008
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e202400008Subventions
Organisme : Infrastructures en Biologie Santé et Agronomie
Organisme : Programme Investissement d'Avenir
ID : I-SITEULNE/ANR-16-IDEX-0004ULNE
Organisme : Région Hauts-de-France
Organisme : Centre National de la Recherche Scientifique
Organisme : European Regional Development Fund
Organisme : Université de Lille
Organisme : CHU Lille - Fonds d'aide à l'émergence
ID : SOBV01F1813C1066
Informations de copyright
© 2024 The Author(s). PROTEOMICS ‐ Clinical Applications published by Wiley‐VCH GmbH.
Références
M. S. Hossain, H. Karuniawati, and A. A. Jairoun, “Colorectal Cancer: A Review of Carcinogenesis, Global Epidemiology, Current Challenges, Risk Factors, Preventive and Treatment Strategies,” Cancers (Basel) 14 (2022): 1732.
J. Ferlay, M. Colombet, I. Soerjomataram, et al., “Cancer Statistics for the Year 2020: An Overview,” International Journal of Cancer 149 (2021): 778–789.
H. Sung, J. Ferlay, R. L. Siegel, et al., “Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries,” CA: A Cancer Journal for Clinicians 71 (2021): 209–249.
E. Dekker, P. J. Tanis, J. L. A. Vleugels, P. M. Kasi, and M. B. Wallace, “Colorectal Cancer,” Lancet 394 (2019): 1467–1480.
I. Martínez‐Reyes and N. S. Chandel, “Cancer Metabolism: Looking Forward,” Nature Reviews Cancer 21 (2021): 669–680.
S. A. Oakes, “Endoplasmic Reticulum Stress Signaling in Cancer Cells,” American Journal of Pathology 190 (2020): 934–946.
Y. Lin, M. Jiang, W. Chen, T. Zhao, and Y. Wei, “Cancer and ER Stress: Mutual Crosstalk Between Autophagy, Oxidative Stress and Inflammatory Response,” Biomedicine & Pharmacotherapy 118 (2019): 109249.
X. Chen and J. R. Cubillos‐Ruiz, “Endoplasmic Reticulum Stress Signals in the Tumour and Its Microenvironment,” Nature Reviews Cancer 21 (2021): 71–88.
J. S. Redzic, J. D. Gomez, J. E. Hellwinkel, T. J. Anchordoquy, and M. W. Graner, “Proteomic Analyses of Brain Tumor Cell Lines Amidst the Unfolded Protein Response,” Oncotarget 7 (2016): 47831–47847.
P. Mokarram, M. Albokashy, M. Zarghooni, et al., “New Frontiers in the Treatment of Colorectal Cancer: Autophagy and the Unfolded Protein Response as Promising Targets,” Autophagy 13 (2017): 781–819.
R. Mora‐Molina, D. Stöhr, M. Rehm, and A. López‐Rivas, “cFLIP Downregulation is an Early Event Required for Endoplasmic Reticulum Stress‐Induced Apoptosis in Tumor Cells,” Cell Death & Disease 13 (2022): 1–12.
E. A. V. Beilankouhi, M. A. Sajadi, I. Alipourfard, P. Hassani, M. Valilo, and R. Safaralizadeh, “Role of the ER‐Induced UPR Pathway, Apoptosis, and Autophagy in Colorectal Cancer,” Pathology—Research and Practice 248 (2023): 154706.
M. Kusaczuk, E. T. Ambel, M. Naumowicz, and G. Velasco, “Cellular Stress Responses as Modulators of Drug Cytotoxicity in Pharmacotherapy of Glioblastoma,” Biochimica Et Biophysica Acta (BBA)—Reviews on Cancer 1879 (2024): 189054.
F. Iorio, T. A. Knijnenburg, D. J. Vis, et al., “A Landscape of Pharmacogenomic Interactions in Cancer,” Cell 166 (2016): 740–754.
M. Frejno, R. Zenezini Chiozzi, M. Wilhelm, et al., “Pharmacoproteomic Characterisation of Human Colon and Rectal Cancer,” Molecular Systems Biology 13 (2017): 951.
R. Mukherji, C. Yin, R. Hameed, et al., “The Current State of Molecular Profiling in Gastrointestinal Malignancies,” Biology Direct 17 (2022): 15.
J. Erde, R. R. O. Loo, and J. A. Loo, “Enhanced FASP (eFASP) to Increase Proteome Coverage and Sample Recovery for Quantitative Proteomic Experiments,” Journal of Proteome Research 13 (2014): 1885–1895.
C. Barbé, F. Bray, M. Gueugneau, et al., “Comparative Proteomic and Transcriptomic Analysis of Follistatin‐Induced Skeletal Muscle Hypertrophy,” Journal of Proteome Research 16 (2017): 3477–3490.
S. Vivier, A. Chepy, F. Bray, et al., “Passages in Culture and Stimulation Conditions Influence Protein Expression of Primary Fibroblasts,” Proteomics 22 (2022): 2100116.
J. Cox and M. Mann, “MaxQuant Enables High Peptide Identification Rates, Individualized p.p.b.‐Range Mass Accuracies and Proteome‐Wide Protein Quantification,” Nature Biotechnology 26 (2008): 1367–1372.
J. Cox, N. Neuhauser, A. Michalski, R. A. Scheltema, J. V. Olsen, and M. Mann, “Andromeda: A Peptide Search Engine Integrated Into the MaxQuant Environment,” Journal of Proteome Research 10 (2011): 1794–1805.
J. Cox, M. Y. Hein, C. A. Luber, I. Paron, N. Nagaraj, and M. Mann, “Accurate Proteome‐Wide Label‐Free Quantification by Delayed Normalization and Maximal Peptide Ratio Extraction, Termed MaxLFQ,” Molecular & Cellular Proteomics 13 (2014): 2513–2526.
S. Tyanova, T. Temu, P. Sinitcyn, et al., “The Perseus Computational Platform for Comprehensive Analysis of (Prote)Omics Data,” Nature Methods 13 (2016): 731–740.
M. Ashburner, C. A. Ball, J. A. Blake, et al., “Gene Ontology: Tool for the Unification of Biology,” Nature Genetics 25 (2000): 25–29.
The Gene Onthology Consortium. “The Gene Ontology Resource: 20 Years and Still Going Strong,” Nucleic Acids Research 47 (2019): D330–D338.
H. Mi, A. Muruganujan, D. Ebert, X. Huang, and P. D. Thomas, “PANTHER Version 14: More Genomes, a New PANTHER GO‐Slim and Improvements in Enrichment Analysis Tools,” Nucleic Acids Research 47 (2019): D419–D426.
M. Kanehisa, “Toward Understanding the Origin and Evolution of Cellular Organisms,” Protein Science 28 (2019): 1947–1951.
D. Liang, M. Khoonkari, T. Avril, E. Chevet, and F. A. E. Kruyt, “The Unfolded Protein Response as Regulator of Cancer Stemness and Differentiation: Mechanisms and Implications for Cancer Therapy,” Biochemical Pharmacology 192 (2021): 114737.
J. Huang, H. Pan, J. Wang, et al., “Unfolded Protein Response in Colorectal Cancer,” Cell & Bioscience 11 (2021): 26.
L. Fang, S. Chen, H. Gong, et al., “Identification of an Unfolded Protein Response‐Related Signature for Predicting the Prognosis of Pancreatic Ductal Adenocarcinoma,” Frontiers in Oncology 12 (2023): 1060508.
Q. Wan, L. Jin, and Z. Wang, “Comprehensive Analysis of Cancer Hallmarks in Cutaneous Melanoma and Identification of a Novel Unfolded Protein Response as a Prognostic Signature,” Aging (Albany NY) 12 (2020): 20684–20701.
C. Hetz, K. Zhang, and R. J. Kaufman, “Mechanisms, Regulation and Functions of the Unfolded Protein Response,” Nature Reviews Molecular Cell Biology 21 (2020): 421–438.
S. Harada and D. Morlote, “Molecular Pathology of Colorectal Cancer,” Advances in Anatomic Pathology 27 (2020): 20.
A. Aranda‐Anzaldo and M. A. R. Dent, “Is Cancer a Disease Set up by Cellular Stress Responses?,” Cell Stress & Chaperones 26 (2021): 597–609.
A. C. Kimmelman and E. White, “Autophagy and Tumor Metabolism,” Cell Metabolism 25 (2017): 1037–1043.
H. Rodriguez, J. C. Zenklusen, L. M. Staudt, J. H. Doroshow, and D. R. Lowy, “The Next Horizon in Precision Oncology—Proteogenomics to Inform Cancer Diagnosis and Treatment,” Cell 184 (2021): 1661–1670.
V. W. Xue, S. C. C. Wong, and W. C. Cho, “From Proteomic Landscape to Single‐Cell Oncoproteomics,” Expert Review of Proteomics 18 (2021): 1–6.
M. Ludvigsen, L. Thorlacius‐Ussing, H. Vorum, M. T. Stender, O. Thorlacius‐Ussing, and B. Honoré, “Proteomic Characterization of Colorectal Cancer Tissue From Patients Identifies Novel Putative Protein Biomarkers,” Current Issues in Molecular Biology 43 (2021): 1043–1056.
L. Sisinni, M. Pietrafesa, S. Lepore, et al., “Endoplasmic Reticulum Stress and Unfolded Protein Response in Breast Cancer: The Balance Between Apoptosis and Autophagy and Its Role in Drug Resistance,” International Journal of Molecular Sciences 20, no. 4 (2019): 857.
R. M. Mohammad, I. Muqbil, L. Lowe, et al., “Broad Targeting of Resistance to Apoptosis in Cancer,” Seminars in Cancer Biology 35 (2015): S78–S103.
S. Tabrez, N. R. Jabir, M. I. Khan, et al., “Association of Autoimmunity and Cancer: An Emphasis on Proteolytic Enzymes,” Seminars in Cancer Biology 64 (2020): 19–28.
M. Zanetti, S. Xian, M. Dosset, and H. Carter, “The Unfolded Protein Response at the Tumor‐Immune Interface,” Frontiers in Immunology 13 (2022): 823157.
M. Songane, M. Khair, and M. Saleh, “An Updated View on the Functions of Caspases in Inflammation and Immunity,” Seminars in Cell & Developmental Biology 82 (2018): 137–149.
S. Conus and H.‐U. Simon, “Cathepsins: Key Modulators of Cell Death and Inflammatory Responses,” Biochemical Pharmacology 76 (2008): 1374–1382.
Z. Jiang, G. Zhang, L. Huang, Y. Yuan, C. Wu, and Y. Li, “Transmissible Endoplasmic Reticulum Stress: A Novel Perspective on Tumor Immunity,” Frontiers in Cell and Developmental Biology 8 (2020): 846.