EP4-induced mitochondrial localization and cell migration mediated by CALML6 in human oral squamous cell carcinoma.
Humans
Cell Movement
Mouth Neoplasms
/ pathology
Mitochondria
/ metabolism
Receptors, Prostaglandin E, EP4 Subtype
/ metabolism
Animals
Mice
Cell Line, Tumor
Carcinoma, Squamous Cell
/ metabolism
Calcium-Calmodulin-Dependent Protein Kinase Kinase
/ metabolism
Calmodulin
/ metabolism
Squamous Cell Carcinoma of Head and Neck
/ metabolism
Journal
Communications biology
ISSN: 2399-3642
Titre abrégé: Commun Biol
Pays: England
ID NLM: 101719179
Informations de publication
Date de publication:
14 May 2024
14 May 2024
Historique:
received:
03
10
2023
accepted:
22
04
2024
medline:
15
5
2024
pubmed:
15
5
2024
entrez:
14
5
2024
Statut:
epublish
Résumé
Lymph node metastasis, primarily caused by the migration of oral squamous cell carcinoma (OSCC) cells, stands as a crucial prognostic marker. We have previously demonstrated that EP4, a subtype of the prostaglandin E2 (PGE2) receptor, orchestrates OSCC cell migration via Ca
Identifiants
pubmed: 38745046
doi: 10.1038/s42003-024-06231-4
pii: 10.1038/s42003-024-06231-4
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
567Informations de copyright
© 2024. The Author(s).
Références
Saikia, P. J., Pathak, L., Mitra, S. & Das, B. The emerging role of oral microbiota in oral cancer initiation, progression, and stemness. Front. Immunol. (Review) 14, 1198269 (2023).
doi: 10.3389/fimmu.2023.1198269
Miyauchi, S. et al. Immune modulation of head and neck squamous cell carcinoma and the tumor microenvironment by conventional therapeutics. Clin. Cancer Res. 25, 4211–4223 (2019).
pubmed: 30814108
pmcid: 6635035
doi: 10.1158/1078-0432.CCR-18-0871
Yokoyama, U., Iwatsubo, K., Umemura, M., Fujita, T. & Ishikawa, Y. The Prostanoid EP4 receptor and its signaling pathway. Pharmacol. Rev. 65, 1010–1052 (2013).
pubmed: 23776144
doi: 10.1124/pr.112.007195
Hoshikawa, H., Goto, R., Mori, T., Mitani, T. & Mori, N. Expression of prostaglandin E2 receptors in oral squamous cell carcinomas and growth inhibitory effects of an EP3 selective antagonist, ONO-AE3-240. Int. J. Oncol. 34, 847–852 (2009).
pubmed: 19212690
doi: 10.3892/ijo_00000211
Feske, S. et al. A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature 441, 179–185 (2006).
pubmed: 16582901
doi: 10.1038/nature04702
Putney, J. W. Jr. Identification of cellular activation mechanisms associated with salivary secretion. Annu. Rev. Physiol. 48, 75–88 (1986).
pubmed: 3010833
doi: 10.1146/annurev.ph.48.030186.000451
Umemura, M. et al. Store-operated Ca2+ entry (SOCE) regulates melanoma proliferation and cell migration. PLoS One 9, e89292 (2014).
pubmed: 24586666
pmcid: 3931742
doi: 10.1371/journal.pone.0089292
Umemura, M., Nakakaji, R. & Ishikawa, Y. Physiological functions of calcium signaling via Orai1 in cancer. J. Physiol. Sci. 73, 21 (2023).
pubmed: 37759164
pmcid: 10717067
doi: 10.1186/s12576-023-00878-0
Osawa, K. et al. Prostaglandin E2 receptor EP4 regulates cell migration through Orai1. Cancer Sci. 111, 160–174 (2020).
pubmed: 31755615
doi: 10.1111/cas.14247
Berridge, M. J., Bootman, M. D. & Roderick, H. L. Calcium signalling: dynamics, homeostasis and remodelling. Nat. Rev Mol. Cell Biol. 4, 517–529 (2003).
pubmed: 12838335
doi: 10.1038/nrm1155
Marcelo, K. L., Means, A. R. & York, B. The Ca(2+)/Calmodulin/CaMKK2 Axis: Nature’s Metabolic CaMshaft. Trends Endocrinol. Metab. 27, 706–718 (2016).
pubmed: 27449752
pmcid: 5035586
doi: 10.1016/j.tem.2016.06.001
Pulliam, T. L. et al. Regulation and role of CAMKK2 in prostate cancer. Nat. Rev. Urol. 19, 367–380 (2022).
pubmed: 35474107
doi: 10.1038/s41585-022-00588-z
Lin, C. et al. Inhibition of CAMKK2 impairs autophagy and castration-resistant prostate cancer via suppression of AMPK-ULK1 signaling. Oncogene 40, 1690–1705 (2021).
pubmed: 33531625
pmcid: 7935762
doi: 10.1038/s41388-021-01658-z
Najar, M. A. et al. Molecular profiling associated with Calcium/Calmodulin-dependent protein Kinase Kinase 2 (CAMKK2)-Mediated carcinogenesis in gastric cancer. J. Proteome Res. 20, 2687–2703 (2021).
pubmed: 33844560
doi: 10.1021/acs.jproteome.1c00008
Long, Y. C. & Zierath, J. R. AMP-activated protein kinase signaling in metabolic regulation. J. Clin. Invest. 116, 1776–1783 (2006).
pubmed: 16823475
pmcid: 1483147
doi: 10.1172/JCI29044
Wang, Z. et al. The EF-Hand Protein CALML6 Suppresses Antiviral Innate Immunity by Impairing IRF3 Dimerization. Cell Rep. 26, 1273–1285.e1275 (2019).
pubmed: 30699354
doi: 10.1016/j.celrep.2019.01.030
Scheid, A. D., Beadnell, T. C. & Welch, D. R. Roles of mitochondria in the hallmarks of metastasis. Br. J. Cancer 124, 124–135 (2021).
pubmed: 33144695
doi: 10.1038/s41416-020-01125-8
Pelicano, H. et al. Mitochondrial dysfunction and reactive oxygen species imbalance promote breast cancer cell motility through a CXCL14-mediated mechanism. Cancer Res. 69, 2375–2383 (2009).
pubmed: 19276362
pmcid: 2760349
doi: 10.1158/0008-5472.CAN-08-3359
Luanpitpong, S. et al. Regulation of lung cancer cell migration and invasion by reactive oxygen species and caveolin-1. J. Biol. Chem. 285, 38832–38840 (2010).
pubmed: 20923773
pmcid: 2998081
doi: 10.1074/jbc.M110.124958
Macleod, K. F. Mitophagy and mitochondrial dysfunction in cancer. Ann. Rev. Cancer Biol. 4, 41–60 (2020).
doi: 10.1146/annurev-cancerbio-030419-033405
Wu, Z. et al. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98, 115–124 (1999).
pubmed: 10412986
doi: 10.1016/S0092-8674(00)80611-X
Nii, M. et al. Suppression of metastasis by tissue inhibitor of metalloproteinase-1 in a newly established human oral squamous cell carcinoma cell line. Int. J. Oncol. 16, 119–143 (2000).
pubmed: 10601556
Momose, F. et al. Variant sublines with different metastatic potentials selected in nude mice from human oral squamous cell carcinomas. J. Oral Pathol. Med. 18, 391–395 (1989).
pubmed: 2585303
doi: 10.1111/j.1600-0714.1989.tb01570.x
Sugiura, K. et al. Hypoxia and CD11b+ cell influx are strongly associated with lymph node metastasis of oral cancer. Anticancer Res. 40, 6845–6852 (2020).
pubmed: 33288576
doi: 10.21873/anticanres.14706
Chen, S. et al. Cloning and characterization of human CAGLP gene encoding a novel EF-hand protein. DNA Seq 15, 365–368 (2004).
pubmed: 15621662
doi: 10.1080/10425170400012933
Szklarczyk, D. et al. The STRING database in 2023: protein–protein association networks and functional enrichment analyses for any sequenced genome of interest. Nucleic Acids Res. 51, D638–D646 (2022).
pmcid: 9825434
doi: 10.1093/nar/gkac1000
Lin, F. et al. The camKK2/camKIV relay is an essential regulator of hepatic cancer. Hepatology 62, 505–520 (2015).
pubmed: 25847065
doi: 10.1002/hep.27832
Zuo, X. et al. Metastasis regulation by PPARD expression in cancer cells. JCI Insight 2, e91419 (2017).
pubmed: 28097239
pmcid: 5214933
doi: 10.1172/jci.insight.91419
Morita, Y. et al. Cellular fibronectin 1 promotes VEGF-C expression, lymphangiogenesis and lymph node metastasis associated with human oral squamous cell carcinoma. Clin. Exp. Metastasis 32, 739–753 (2015).
pubmed: 26319373
doi: 10.1007/s10585-015-9741-2
Chaube, B. & Bhat, M. K. AMPK, a key regulator of metabolic/energy homeostasis and mitochondrial biogenesis in cancer cells. Cell Death Dis. 7, e2044 (2016).
pubmed: 26775698
pmcid: 4816182
doi: 10.1038/cddis.2015.404
Denisenko, T. V., Gorbunova, A. S. & Zhivotovsky, B. Mitochondrial Involvement in Migration, Invasion and Metastasis. Front. Cell Dev. Biol. 7, 355 (2019).
pubmed: 31921862
pmcid: 6932960
doi: 10.3389/fcell.2019.00355
Tan, Z. et al. The Role of PGC1α in cancer metabolism and its therapeutic implications. Mol. Cancer Ther. 15, 774–782 (2016).
pubmed: 27197257
doi: 10.1158/1535-7163.MCT-15-0621
Zhang, J. & Zhang, Q. Using Seahorse machine to measure OCR and ECAR in cancer cells. Methods Mol. Biol. 1928, 353–363 (2019).
pubmed: 30725464
doi: 10.1007/978-1-4939-9027-6_18
Marchetti, P., Fovez, Q., Germain, N., Khamari, R. & Kluza, J. Mitochondrial spare respiratory capacity: Mechanisms, regulation, and significance in non-transformed and cancer cells. FASEB J. 34, 13106–13124 (2020).
pubmed: 32808332
doi: 10.1096/fj.202000767R
Nakamura, H. & Takada, K. Reactive oxygen species in cancer: Current findings and future directions. Cancer Sci. 112, 3945–3952 (2021).
pubmed: 34286881
pmcid: 8486193
doi: 10.1111/cas.15068
Junqueira-de-Azevedo Ide, L. et al. Cloning and expression of calglandulin, a new EF-hand protein from the venom glands of Bothrops insularis snake in E. coli. Biochim. Biophys. Acta 1648, 90–98 (2003).
pubmed: 12758151
doi: 10.1016/S1570-9639(03)00111-0
Chattopadhyay, E. & Roy, B. Altered mitochondrial signalling and metabolism in cancer. Front. Oncol. 7, 43 (2017).
pubmed: 28373964
pmcid: 5357656
doi: 10.3389/fonc.2017.00043
Madan, S., Uttekar, B., Chowdhary, S. & Rikhy, R. Mitochondria lead the way: mitochondrial dynamics and function in cellular movements in development and disease. Front. Cell Dev. Biol. 9, 781933 (2021).
pubmed: 35186947
doi: 10.3389/fcell.2021.781933
Ying, F. et al. Prostaglandin E receptor subtype 4 protects against diabetic cardiomyopathy by modulating cardiac fatty acid metabolism via FOXO1/CD36 signalling. Biochem. Biophys. Res. Commun. 548, 196–203 (2021).
pubmed: 33647796
doi: 10.1016/j.bbrc.2021.01.038
Ying, F., Cai, Y., Cai, Y., Wang, Y. & Tang, E. H. C. Prostaglandin E receptor subtype 4 regulates lipid droplet size and mitochondrial activity in murine subcutaneous white adipose tissue. FASEB J. 31, 4023–4036 (2017).
pubmed: 28533326
doi: 10.1096/fj.201700191R
Tochhawng, L., Deng, S., Pervaiz, S. & Yap, C. T. Redox regulation of cancer cell migration and invasion. Mitochondrion 13, 246–253 (2013).
pubmed: 22960576
doi: 10.1016/j.mito.2012.08.002
Chae, I. G. et al. Generation of ROS by CAY10598 leads to inactivation of STAT3 signaling and induction of apoptosis in human colon cancer HCT116 cells. Free Radic. Res. 48, 1311–1321 (2014).
pubmed: 25096910
doi: 10.3109/10715762.2014.951838
Buchholz, A. et al. EP4 as a negative prognostic factor in patients with vulvar cancer. Cancers 13, 1410 (2021).
pubmed: 33808776
pmcid: 8003514
doi: 10.3390/cancers13061410
Mukherjee, D. et al. Targeting CaMKK2 inhibits actin cytoskeletal assembly to suppress cancer metastasis. Cancer Res. 83, 2889–2907 (2023).
pubmed: 37335130
pmcid: 10472110
doi: 10.1158/0008-5472.CAN-22-1622
Anaya, J. OncoLnc: linking TCGA survival data to mRNAs, miRNAs, and lncRNAs. PeerJ Comput. Sci. 2, e67 (2016).
doi: 10.7717/peerj-cs.67
Nemoto, H. et al. Store-operated calcium entry via ORAI1 regulates doxorubicin-induced apoptosis and prevents cardiotoxicity in cardiac fibroblasts. PLoS One 17, e0278613 (2022).
pubmed: 36472998
pmcid: 9725120
doi: 10.1371/journal.pone.0278613
Baljinnyam, E. et al. Epac1 increases migration of endothelial cells and melanoma cells via FGF2-mediated paracrine signaling. Pigment Cell Melanoma Res. 27, 611–620 (2014).
pubmed: 24725364
pmcid: 4283731
doi: 10.1111/pcmr.12250
Kioi, M. et al. IL-13 cytotoxin has potent antitumor activity and synergizes with paclitaxel in a mouse model of oral squamous cell carcinoma. Int. J. Cancer 124, 1440–1448 (2009).
pubmed: 19065664
doi: 10.1002/ijc.24067
Baljinnyam, E. et al. Exchange protein directly activated by cyclic AMp increases melanoma cell migration by a Ca2+-dependent mechanism. Cancer Res. 70, 5607–5617 (2010).
pubmed: 20551063
doi: 10.1158/0008-5472.CAN-10-0056
Caneba, C. A., Bellance, N., Yang, L., Pabst, L. & Nagrath, D. Pyruvate uptake is increased in highly invasive ovarian cancer cells under anoikis conditions for anaplerosis, mitochondrial function, and migration. Am. J. Physiol. Endocrinol. Metab. 303, E1036–E1052 (2012).
pubmed: 22895781
doi: 10.1152/ajpendo.00151.2012
Xu, Z. et al. SQLE mediates metabolic reprogramming to promote LN metastasis in castration-resistant prostate cancer. Onco. Targets Ther. 14, 4285–4295 (2021).
pubmed: 34335030
pmcid: 8318010
doi: 10.2147/OTT.S315813
Eguchi, H. et al. A magnetic anti-cancer compound for magnet-guided delivery and magnetic resonance imaging. Sci. Rep. 5, 9194 (2015).
pubmed: 25779357
pmcid: 4361848
doi: 10.1038/srep09194