Pancreatic stellate cells exhibit adaptation to oxidative stress evoked by hypoxia.
Calcium
Glutathione
Hypoxia
Pancreatic stellate cells
Reactive oxygen species
Journal
Biology of the cell
ISSN: 1768-322X
Titre abrégé: Biol Cell
Pays: England
ID NLM: 8108529
Informations de publication
Date de publication:
Oct 2020
Oct 2020
Historique:
received:
15
02
2020
revised:
31
05
2020
accepted:
04
06
2020
pubmed:
8
7
2020
medline:
20
7
2021
entrez:
8
7
2020
Statut:
ppublish
Résumé
Pancreatic stellate cells play a key role in the fibrosis that develops in diseases such as pancreatic cancer. In the growing tumour, a hypoxia condition develops under which cancer cells are able to proliferate. The growth of fibrotic tissue contributes to hypoxia. In this study, the effect of hypoxia (1% O Hypoxia induced an increase in intracellular and mitochondrial free-Ca Hypoxia creates pro-oxidant conditions in pancreatic stellate cells to which cells adapt and leads to increased viability and proliferation.
Sections du résumé
BACKGROUND INFORMATION
BACKGROUND
Pancreatic stellate cells play a key role in the fibrosis that develops in diseases such as pancreatic cancer. In the growing tumour, a hypoxia condition develops under which cancer cells are able to proliferate. The growth of fibrotic tissue contributes to hypoxia. In this study, the effect of hypoxia (1% O
RESULTS
RESULTS
Hypoxia induced an increase in intracellular and mitochondrial free-Ca
CONCLUSIONS AND SIGNIFICANCE
CONCLUSIONS
Hypoxia creates pro-oxidant conditions in pancreatic stellate cells to which cells adapt and leads to increased viability and proliferation.
Identifiants
pubmed: 32632968
doi: 10.1111/boc.202000020
doi:
Substances chimiques
Calcium
SY7Q814VUP
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
280-299Subventions
Organisme : Ministerio de Economía y Competitividad
ID : BFU2016-79259-R
Organisme : Ministerio de Ciencia, Innovación y Universidades
ID : EQC2018-004646-P
Organisme : Junta de Extremadura-FEDER
ID : GR18070
Informations de copyright
© 2020 Société Française des Microscopies and Société de Biologie Cellulaire de France. Published by John Wiley & Sons Ltd.
Références
Balamurugan, M., Santharaman, P., Madasamy, T., Rajesh, S., Sethy, N.K., Bhargava, K., Kotamraju, S. and Karunakaran, C. (2018) Recent trends in electrochemical biosensors of superoxide dismutases. Biosens. Bioelectron. 116, 89-99
Bradford, M.M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254
Cao, X., Fang, X., Malik, W.S., He, Y., Li, X., Xie, M., Sun, W., Xu, Y. and Liu, X. (2020) TRB3 interacts with ERK and JNK and contributes to the proliferation, apoptosis, and migration of lung adenocarcinoma cells. J. Cell. Physiol. 235, 538-547
Capolongo, G., Suzumoto, Y., D'Acierno, M., Simeoni, M., Capasso, G. and Zacchia, M. (2019) ERK1,2 signalling pathway along the nephron and its role in acid-base and electrolytes balance. Int. J. Mol. Sci. 20(17), E4153
Chan, K.K., Leung, C.O., Wong, C.C., Ho, D.W., Chok, K.S., Lai, C.L., Ng, I.O. and Lo, R.C. (2017) Secretory stanniocalcin 1 promotes metastasis of hepatocellular carcinoma through activation of JNK signaling pathway. Cancer Lett. 403, 330-338
Choi, J.H., Ji, Y.G., Ko, J.J., Cho, H.J. and Lee, D.H. (2018) Activating P2 × 7 receptors increases proliferation of human pancreatic cancer cells via ERK1/2 and JNK. Pancreas 47, 643-651
Erkan, M., Kurtoglu, M. and Kleeff, J. (2016) The role of hypoxia in pancreatic cancer: a potential therapeutic target? Expert. Rev. Gastroenterol. Hepatol. 10, 301-316
Erkan, M., Reiser-Erkan, C., Michalski, C.W., Deucker, S., Sauliunaite, D., Streit, S., Esposito, I., Friess, H. and Kleeff, J. (2009) Cancer-stellate cell interactions perpetuate the hypoxia-fibrosis cycle in pancreatic ductal adenocarcinoma. Neoplasia 11, 497-508
Estaras, M., Ameur, F.Z., Roncero, V., Fernandez-Bermejo, M., Blanco, G., Lopez, D., Mateos, J.M., Salido, G.M. and Gonzalez, A. (2019a) The melatonin receptor antagonist luzindole induces Ca2+ mobilization, reactive oxygen species generation and impairs trypsin secretion in mouse pancreatic acinar cells. Biochim. Biophys. Acta Gen. Subj. 1863, 129407
Estaras, M., Moreno, N., Santofimia-Castaño, P., Martinez-Morcillo, S., Roncero, V., Blanco, G., Lopez, D., Fernandez-Bermejo, M., Mateos, J.M., Iovanna, J.L., Salido, G.M. and Gonzalez, A. (2019b) Melatonin induces reactive oxygen species generation and changes in glutathione levels and reduces viability in human pancreatic stellate cells. J. Physiol. Biochem. 75, 185-197
Ferdek, P.E. and Jakubowska, M.A. (2017) Biology of pancreatic stellate cells-more than just pancreatic cancer. Pflugers Arch. 469, 1039-1050
Gialeli, C., Theocharis, A.D. and Karamanos, N.K. (2011) Roles of matrix metalloproteinases in cancer progression and their pharmacological targeting. FEBS J. 278, 16-27
Gonzalez, A., del Castillo-Vaquero, A., Miro-Moran, A., Tapia, J.A. and Salido, G.M. (2011) Melatonin reduces pancreatic tumor cell viability by altering mitochondrial physiology. J. Pineal Res. 50, 250-260
Gonzalez, A., Granados, M.P., Salido, G.M. and Pariente, J.A. (2003) Changes in mitochondrial activity evoked by cholecystokinin in isolated mouse pancreatic acinar cells. Cell. Signal. 15, 1039-1048
Gonzalez, A. and Salido, G.M. (2016) Determination of reactive oxygen species production in pancreatic acinar cells. Pancreapedia. https://doi.org/10.3998/panc.2016.32
Gonzalez, A., Schulz, I. and Schmid, A. (2000) Agonist-evoked mitochondrial Ca2+ signals in mouse pancreatic acinar cells. J. Biol. Chem. 275, 38680-38686
Gryshchenko, O., Gerasimenko, J.V., Gerasimenko, O.V and Petersen, O.H. (2016) Ca(2+) signals mediated by bradykinin type 2 receptors in normal pancreatic stellate cells can be inhibited by specific Ca(2+) channel blockade. J. Physiol. 594, 281-293
Gryshchenko, O., Gerasimenko, J.V., Peng, S., Gerasimenko, O.V. and Petersen, O.H. (2018) Calcium signalling in the acinar environment of the exocrine pancreas: physiology and pathophysiology. J. Physiol. 596, 2663-2678
Gupta, N., Park, J.E., Tse, W., Low, J.K., Kon, O.L., McCarthy, N. and Sze, S.K. (2019) ERO1α promotes hypoxic tumor progression and is associated with poor prognosis in pancreatic cancer. Oncotarget 10, 5970-5982
Hadler-Olsen, E., Winberg, J.O. and Uhlin-Hansen, L. (2013) Matrix metalloproteinases in cancer: their value as diagnostic and prognostic markers and therapeutic targets. Tumour Biol. 34, 2041-2051
Ikenaga, N., Ohuchida, K., Mizumoto, K., Cui, L., Kayashima, T., Morimatsu, K., Moriyama, T., Nakata, K., Fujita, H. and Tanaka, M. (2010) CD10+ pancreatic stellate cells enhance the progression of pancreatic cancer. Gastroenterology 139, 1041-1051
Karatug Kacar, A. and Bolkent, S. (2019) Vitronectin, fibronectin and epidermal growth factor induce proliferation via the JNK and ERK pathways in insulinoma INS-1 cells. Cytotechnology 71, 209-217
Li, J., Zhou, R., Zhang, J. and Li, Z.F. (2014) Calcium signaling of pancreatic acinar cells in the pathogenesis of pancreatitis. World J. Gastroenterol. 20, 16146-16152
Mahadevan, D. and Von Hoff, D.D. (2007) Tumor-stroma interactions in pancreatic ductal adenocarcinoma. Mol. Cancer Ther. 6, 1186-1197
Martinez-Morcillo, S., Perez-Lopez, M., Soler-Rodriguez, F. and Gonzalez, A. (2019) The organophosphorus pesticide dimethoate decreases cell viability and induces changes in different biochemical parameters of rat pancreatic stellate cells. Toxicol. In Vitro 54, 89-97
McCarroll, J.A., Naim, S., Sharbeen, G., Russia, N., Lee, J., Kavallaris, M., Goldstein, D. and Phillips, P.A. (2014) Role of pancreatic stellate cells in chemoresistance in pancreatic cancer. Front. Physiol. 5, 141
Masamune, A., Kikuta, K., Watanabe, T., Satoh, K., Hirota, M. and Shimosegawa, T. (2008) Hypoxia stimulates pancreatic stellate cells to induce fibrosis and angiogenesis in pancreatic cancer. Am. J. Physiol. Gastrointest. Liver Physiol. 295, G709-G717
Mateo, F., Vidal-Laliena, M., Pujol, M.J. and Bachs, O. (2010) Acetylation of cyclin A: a new cell cycle regulatory mechanism. Biochem. Soc. Trans. 38, 83-86
Milani, P., Gagliardi, S., Cova, E. and Cereda, C. (2011) SOD1 transcriptional and posttranscriptional regulation and its potential implications in ALS. Neurol. Res. Int. 2011, 458427
Moir, J.A., Mann, J. and White, S.A. (2015) The role of pancreatic stellate cells in pancreatic cancer. Surg. Oncol. 24, 232-238
Nielsen, N., Kondratska, K., Ruck, T., Hild, B., Kovalenko, I., Schimmelpfennig, S., Welzig, J., Sargin, S., Lindemann, O., Christian, S., Meuth, S.G., Prevarskaya, N. and Schwab, A. (2017) TRPC6 channels modulate the response of pancreatic stellate cells to hypoxia. Pflugers Arch. 469, 1567-1577
Policastro, L.L., Ibañez, I.L., Notcovich, C., Duran, H.A. and Podhajcer, O.L. (2013) The tumor microenvironment: characterization, redox considerations, and novel approaches for reactive oxygen species-targeted gene therapy. Antioxid. Redox Signal. 19, 854-895
Popov, Y., Patsenker, E., Bauer, M., Niedobitek, E., Schulze-Krebs, A. and Schuppan, D. (2006) Halofuginone induces matrix metalloproteinases in rat hepatic stellate cells via activation of p38 and NFkappaB. J. Biol. Chem. 281, 15090-15098
Pothula, S.P., Xu, Z., Goldstein, D., Pirola, R.C., Wilson, J.S. and Apte, M.V. (2016) Key role of pancreatic stellate cells in pancreatic cancer. Cancer Lett. 381, 194-200
Rebours, V., Albuquerque, M., Sauvanet, A., Ruszniewski, P., Levy, P., Paradis, V., Bedossa, P. and Couvelard, A. (2013) Hypoxia pathways and cellular stress activate pancreatic stellate cells: development of an organotypic culture model of thick slices of normal human pancreas. PLoS One 8, e76229
Roskoski, R. Jr. (2016) Cyclin-dependent protein kinase inhibitors including palbociclib as anticancer drugs. Pharmacol. Res. 107, 249-275
Santofimia-Castaño, P., Garcia-Sanchez, L., Ruy, D.C., Fernandez-Bermejo, M., Salido, G.M. and Gonzalez, A. (2014) The seleno-organic compound ebselen impairs mitochondrial physiology and induces cell death in AR42J cells. Toxicol. Lett. 229, 465-473
Santofimia-Castaño, P., Garcia-Sanchez, L., Ruy, D.C., Sanchez-Correa, B., Fernandez-Bermejo, M., Tarazona, R., Salido, G.M. and Gonzalez, A. (2015) Melatonin induces calcium mobilization and influences cell proliferation independently of MT1/MT2 receptor activation in rat pancreatic stellate cells. Cell Biol. Toxicol. 31, 95-110
Sarcar, B., Li, X. and Fleming, J.B. (2019) Hypoxia-induced autophagy degrades stromal lumican into tumor microenvironment of pancreatic ductal adenocarcinoma: a mini review. J. Cancer Treatment. Diagn. 3, 22-27
Sasaki, T., Shimizu, T., Koyama, T., Sakai, M., Uchiyama, S., Kawakami, S., Noda, Y., Shirasawa, T. and Kojima, S. (2011) Superoxide dismutase deficiency enhances superoxide levels in brain tissues during oxygenation and hypoxia-reoxygenation. J. Neurosci. Res. 89, 601-610
Sies, H. (1999) Glutathione and its role in cellular functions. Free Radical Biol. Med. 27, 916-921
Sherman, M.H. (2018) Stellate cells in tissue repair, inflammation, and cancer. Annu. Rev. Cell Dev. Biol. 34, 333-355
Tang, D., Wu, Q., Zhang, J., Zhang, H., Yuan, Z., Xu, J., Chong, Y., Huang, Y., Xiong, Q., Wang, S., Tian, Y., Lu, Y., Ge, X., Shen, W. and Wang, D. (2018) Galectin-1 expression in activated pancreatic satellite cells promotes fibrosis in chronic pancreatitis/pancreatic cancer via the TGF-β1/Smad pathway. Oncol. Rep. 39, 1347-1355
Thakur, N., Kumari, S. and Mehrotra, R. (2018) Association between Cyclin D1 G870A (rs9344) polymorphism and cancer risk in Indian population: meta-analysis and trial sequential analysis. Biosci. Rep. 38, BSR20180694
Tian, W., Rojo de la Vega, M., Schmidlin, C.J., Ooi, A. and Zhang, D.D. (2018) Kelch-like ECH-associated protein 1 (KEAP1) differentially regulates nuclear factor erythroid-2-related factors 1 and 2 (NRF1 and NRF2). J. Biol. Chem. 293, 2029-2040
Villaverde, A., Parra, V. and Estevez, M. (2014). Oxidative and nitrosative stress induced in myofibrillar proteins by a hydroxyl-radical-generating system: impact of nitrite and ascorbate. J. Agric. Food Chem. 62, 2158-2164
Wang, J.L., Quan, Q., Ji, R., Guo, X.Y., Zhang, J.M., Li, X. and Liu, Y.G. (2018) Isorhamnetin suppresses PANC-1 pancreatic cancer cell proliferation through S phase arrest. Biomed. Pharmacother. 108, 925-933
Wu, L., Huang, X., Kuang, Y., Xing, Z., Deng, X. and Luo, Z. (2019) Thapsigargin induces apoptosis in adrenocortical carcinoma by activating endoplasmic reticulum stress and the JNK signaling pathway: an in vitro and in vivo study. Drug Des. Devel. Ther. 13, 2787-2798
Xiao, B., Chen, D., Luo, S., Hao, W., Jing, F., Liu, T., Wang, S., Geng, Y., Li, L., Xu, W., Zhang, Y., Liao, X., Zuo, D., Wu, Y., Li, M. and Ma, Q. (2016) Extracellular translationally controlled tumor protein promotes colorectal cancer invasion and metastasis through Cdc42/JNK/ MMP9 signaling. Oncotarget 7, 50057-50073
Xiao, Y., Zhang, H., Ma, Q., Huang, R., Lu, J., Liang, X., Liu, X., Zhang, Z., Yu, L., Pang, J., Zhou, L., Liu, T., Wu, H. and Liang, Z. (2019) YAP1-mediated pancreatic stellate cell activation inhibits pancreatic cancer cell proliferation. Cancer Lett. 462, 51-56
Xu, P., Xia, X., Yang, Z., Tian, Y., Di, J. and Guo, M. (2017) Silencing of TCTN1 inhibits proliferation, induces cell cycle arrest and apoptosis in human thyroid cancer. Exp. Ther. Med. 14, 3720-3726
Yu, L., Li, J.J., Liang, X.L., Wu, H. and Liang, Z. (2019) PSME3 promotes TGFB1 secretion by pancreatic cancer cells to induce pancreatic stellate cell proliferation. J. Cancer 10, 2128-2138
Zou, X., Ratti, B.A., O'Brien, J.G., Lautenschlager, S.O., Gius, D.R., Bonini, M.G. and Zhu, Y. (2017) Manganese superoxide dismutase (SOD2): is there a center in the universe of mitochondrial redox signaling? J. Bioenerg. Biomembr. 49, 325-333