Activated Src requires Cadherin-11, Rac, and gp130 for Stat3 activation and survival of mouse Balb/c3T3 fibroblasts.
Journal
Cancer gene therapy
ISSN: 1476-5500
Titre abrégé: Cancer Gene Ther
Pays: England
ID NLM: 9432230
Informations de publication
Date de publication:
10 2022
10 2022
Historique:
received:
11
11
2021
accepted:
18
03
2022
revised:
08
02
2022
pubmed:
13
4
2022
medline:
20
10
2022
entrez:
12
4
2022
Statut:
ppublish
Résumé
We previously demonstrated that engagement of cadherins, cell to cell adhesion molecules, triggers a dramatic increase in levels and activity of the Rac/Cdc42 small GTPases, which is followed by secretion of IL6 family cytokines and activation of their common receptor, gp130, in an autocrine manner. This results in phosphorylation of the Signal Transducer and Activator of Transcription-3 (Stat3) on tyrosine-705, which then dimerizes, migrates to the nucleus, and activates transcription of genes involved in cell division and survival. In the present report we demonstrate that, in mouse Balb/c3T3 fibroblasts, mutationally activated Src
Identifiants
pubmed: 35411090
doi: 10.1038/s41417-022-00462-5
pii: 10.1038/s41417-022-00462-5
pmc: PMC9576600
doi:
Substances chimiques
Cadherins
0
Cytokine Receptor gp130
133483-10-0
Cytokines
0
Interleukin-6
0
osteoblast cadherin
156621-71-5
STAT3 Transcription Factor
0
Tyrosine
42HK56048U
rac GTP-Binding Proteins
EC 3.6.5.2
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
1502-1513Subventions
Organisme : CIHR
Pays : Canada
Informations de copyright
© 2022. The Author(s).
Références
Ma JH, Qin L, Li X. Role of STAT3 signaling pathway in breast cancer. Cell Commun Signal. 2020;18:33.
pubmed: 32111215
pmcid: 7048131
doi: 10.1186/s12964-020-0527-z
Johnson DE, O’Keefe RA, Grandis JR. Targeting the IL-6/JAK/STAT3 signalling axis in cancer. Nat Rev Clin Oncol. 2018;15:234–48.
pubmed: 29405201
pmcid: 5858971
doi: 10.1038/nrclinonc.2018.8
Niu G, Wright KL, Ma Y, Wright GM, Huang M, Irby R, et al. Role of Stat3 in regulating p53 expression and function. Mol Cell Biol. 2005;25:7432–40.
pubmed: 16107692
pmcid: 1190305
doi: 10.1128/MCB.25.17.7432-7440.2005
Gritsko T, Williams A, Turkson J, Kaneko S, Bowman T, Huang M, et al. Persistent activation of stat3 signaling induces survivin gene expression and confers resistance to apoptosis in human breast cancer cells. Clin Cancer Res. 2006;12:11–9.
pubmed: 16397018
doi: 10.1158/1078-0432.CCR-04-1752
Yu H, Pardoll D, Jove R. STATs in cancer inflammation and immunity: a leading role for STAT3. Nat Rev Cancer. 2009;9:798–809.
pubmed: 19851315
pmcid: 4856025
doi: 10.1038/nrc2734
Bharadwaj U, Kasembeli MM, Robinson P, Tweardy DJ. Targeting janus kinases and signal transducer and activator of transcription 3 to treat inflammation, fibrosis, and cancer: rationale, progress, and caution. Pharm Rev. 2020;72:486–526.
pubmed: 32198236
pmcid: 7300325
doi: 10.1124/pr.119.018440
Bromberg JF, Wrzeszczynska MH, Devgan G, Zhao Y, Pestell RG, Albanese C, et al. Stat3 as an oncogene. Cell 1999;98:295–303.
pubmed: 10458605
doi: 10.1016/S0092-8674(00)81959-5
Arulanandam R, Vultur A, Cao J, Carefoot E, Elliott BE, Truesdell PF, et al. Cadherin-cadherin engagement promotes cell survival via Rac1/Cdc42 and signal transducer and activator of transcription-3. Mol Cancer Res. 2009;7:1310–27.
pubmed: 19671682
doi: 10.1158/1541-7786.MCR-08-0469
Vultur A, Cao J, Arulanandam R, Turkson J, Jove R, Greer P, et al. Cell-to-cell adhesion modulates Stat3 activity in normal and breast carcinoma cells. Oncogene 2004;23:2600–16.
pubmed: 15007380
doi: 10.1038/sj.onc.1207378
Raptis L, Arulanandam R, Vultur A, Geletu M, Chevalier S, Feracci H. Beyond structure, to survival: Stat3 activation by cadherin engagement. Biochem Cell Biol. 2009;87:835–43.
pubmed: 19935869
doi: 10.1139/O09-061
Arulanandam R, Geletu M, Feracci H, Raptis L. Activated Rac1 requires gp130 for Stat3 activation, cell proliferation and migration. Exp Cell Res. 2010;316:875–86.
pubmed: 19852956
doi: 10.1016/j.yexcr.2009.10.017
Geletu M, Arulanandam R, Chevalier S, Saez B, Larue L, Feracci H, et al. Classical cadherins control survival through the gp130/Stat3 axis. BBA-Molecular. Cell Res. 2013;1833:1947–59.
Espada J, Martin-Perez J. An update on Src family of nonreceptor tyrosine kinases biology. Int Rev Cell Mol Biol. 2017;331:83–122.
pubmed: 28325216
doi: 10.1016/bs.ircmb.2016.09.009
Elsberger B, Tan BA, Mitchell TJ, Brown SB, Mallon EA, Tovey SM, et al. Is expression or activation of Src kinase associated with cancer-specific survival in ER-, PR- and HER2-negative breast cancer patients? Am J Pathol. 2009;175:1389–97.
pubmed: 19762712
pmcid: 2751536
doi: 10.2353/ajpath.2009.090273
Turkson J, Bowman T, Garcia R, Caldenhoven E, De Groot RP, Jove R. Stat3 activation by Src induces specific gene regulation and is required for cell transformation. Mol Cell Biol. 1998;18:2545–52.
pubmed: 9566874
pmcid: 110634
doi: 10.1128/MCB.18.5.2545
Bromberg JF, Horvath CM, Besser D, Lathem WW, Darnell JE Jr. Stat3 activation is required for cellular transformation by v-src. Mol Cell Biol. 1998;18:2553–8.
pubmed: 9566875
pmcid: 110635
doi: 10.1128/MCB.18.5.2553
Orlandini M, Oliviero S. In fibroblasts Vegf-D expression is induced by cell-cell contact mediated by cadherin-11. J Biol Chem. 2001;276:6576–81.
pubmed: 11108717
doi: 10.1074/jbc.M009573200
Raptis L, Lamfrom H, Benjamin TL. Regulation of cellular phenotype and expression of polyomavirus middle T antigen in rat fibroblasts. Mol Cell Biol. 1985;5:2476–86.
pubmed: 2426583
pmcid: 366975
van Kuppeveld FJ, Johansson KE, Galama JM, Kissing J, Bolske G, van der Logt JT, et al. Detection of mycoplasma contamination in cell cultures by a mycoplasma group-specific PCR. Appl Environ Microbiol. 1994;60:149–52.
pubmed: 7509584
pmcid: 201282
doi: 10.1128/aem.60.1.149-152.1994
Geletu M, Mohan R, Arulanandam R, Berger-Becvar A, Nabi IR, Gunning PT, et al. Reciprocal regulation of the Cadherin-11/Stat3 axis by caveolin-1 in mouse fibroblasts and lung carcinoma cells. Biochim Biophys Acta. 2018;1865:794–802.
doi: 10.1016/j.bbamcr.2018.02.004
Wadhawan A, Smith C, Nicholson RI, Barrett-Lee P, Hiscox S. Src-mediated regulation of homotypic cell adhesion: implications for cancer progression and opportunities for therapeutic intervention. Cancer Treat Rev. 2011;37:234–41.
pubmed: 20888696
doi: 10.1016/j.ctrv.2010.08.003
Geletu M, Guy S, Arulanandam R, Feracci H, Raptis L. Engaged for survival; from cadherin ligation to Stat3 activation. Jaks-Stat 2013;2:e27363.
doi: 10.4161/jkst.27363
Narimatsu M, Maeda H, Itoh S, Atsumi T, Ohtani T, Nishida K, et al. Tissue-specific autoregulation of the stat3 gene and its role in interleukin-6-induced survival signals in T cells. Mol Cell Biol. 2001;21:6615–25.
pubmed: 11533249
pmcid: 99807
doi: 10.1128/MCB.21.19.6615-6625.2001
Lynch EA, Stall J, Schmidt G, Chavrier P, D’Souza-Schorey C. Proteasome-mediated degradation of Rac1-GTP during epithelial cell scattering. Mol Biol Cell. 2006;17:2236–42.
pubmed: 16481404
pmcid: 1446081
doi: 10.1091/mbc.e05-08-0779
Servitja JM, Marinissen MJ, Sodhi A, Bustelo XR, Gutkind JS. Rac1 function is required for Src-induced transformation. Evidence of a role for Tiam1 and Vav2 in Rac activation by Src. J Biol Chem. 2003;278:34339–46.
pubmed: 12810717
doi: 10.1074/jbc.M302960200
Rose-John S. Interleukin-6 signalling in health and disease. F1000Res. 2020;9.
del Valle I, Rudloff S, Carles A, Li Y, Liszewska E, Vogt R, et al. E-cadherin is required for the proper activation of the Lifr/Gp130 signaling pathway in mouse embryonic stem cells. Development 2013;140:1684–92.
pubmed: 23487312
doi: 10.1242/dev.088690
Creedon H, Brunton VG. Src kinase inhibitors: promising cancer therapeutics? Crit Rev Oncog. 2012;17:145–59.
pubmed: 22471705
doi: 10.1615/CritRevOncog.v17.i2.20
Zhang S, Yu D. Targeting Src family kinases in anti-cancer therapies: turning promise into triumph. Trends Pharm Sci. 2012;33:122–8.
pubmed: 22153719
doi: 10.1016/j.tips.2011.11.002
Grandis JR, Drenning SD, Zeng Q, Watkins SC, Melhem MF, Endo S, et al. Constitutive activation of Stat3 signaling abrogates apoptosis in squamous cell carcinogenesis in vivo. Proc Nat Acad Sci USA. 2000;97:4227–32.
pubmed: 10760290
pmcid: 18206
doi: 10.1073/pnas.97.8.4227
Epling-Burnette PK, Liu JH, Catlett-Falcone R, Turkson J, Oshiro M, Kothapalli R, et al. Inhibition of STAT3 signaling leads to apoptosis of leukemic large granular lymphocytes and decreased Mcl-1 expression. J Clin Invest. 2001;107:351–62.
pubmed: 11160159
pmcid: 199188
doi: 10.1172/JCI9940
Wegrzyn J, Potla R, Chwae YJ, Sepuri NB, Zhang Q, Koeck T, et al. Function of mitochondrial Stat3 in cellular respiration. Science 2009;323:793–7.
pubmed: 19131594
pmcid: 2758306
doi: 10.1126/science.1164551
Gough DJ, Corlett A, Schlessinger K, Wegrzyn J, Larner AC, Levy DE. Mitochondrial STAT3 supports Ras-dependent oncogenic transformation. Science 2009;324:1713–6.
pubmed: 19556508
pmcid: 2840701
doi: 10.1126/science.1171721
Demaria M, Poli V. From the nucleus to the mitochondria and back: the odyssey of a multitask STAT3. Cell Cycle. 2011;10:3221–2.
pubmed: 21926478
doi: 10.4161/cc.10.19.17379
Sears RC, Nevins JR. Signaling networks that link cell proliferation and cell fate. J Biol Chem. 2002;277:11617–20.
pubmed: 11805123
doi: 10.1074/jbc.R100063200
Feltes CM, Kudo A, Blaschuk O, Byers SW. An alternatively spliced cadherin-11 enhances human breast cancer cell invasion. Cancer Res. 2002;62:6688–97.
pubmed: 12438268
Chu K, Cheng CJ, Ye X, Lee YC, Zurita AJ, Chen DT, et al. Cadherin-11 promotes the metastasis of prostate cancer cells to bone. Mol Cancer Res. 2008;6:1259–67.
pubmed: 18708358
pmcid: 2643879
doi: 10.1158/1541-7786.MCR-08-0077
Carmona FJ, Villanueva A, Vidal A, Munoz C, Puertas S, Penin RM, et al. Epigenetic disruption of cadherin-11 in human cancer metastasis. J Pathol. 2012;228:230–40.
pubmed: 22374749
pmcid: 3467766
doi: 10.1002/path.4011
Niit M, Hoskin V, Geletu M, Arulanandam R, BE E, Raptis L. Cell-cell and cell-matrix adhesion in survival and metastasis: Stat3 vs Akt. Biomolecular Concepts. 2015;6:383–99.
pubmed: 26565555
doi: 10.1515/bmc-2015-0022
Pohlodek K, Tan YY, Singer CF, Gschwantler-Kaulich D. Cadherin-11 expression is upregulated in invasive human breast cancer. Oncol Lett. 2016;12:4393–8.
pubmed: 28101202
pmcid: 5228198
doi: 10.3892/ol.2016.5236
Wang Q, Jia Y, Peng X, Li C. Clinical and prognostic association of oncogene cadherin 11 in gastric cancer. Oncol Lett. 2020;19:4011–23.
pubmed: 32391104
pmcid: 7204628
Irby RB, Yeatman TJ. Increased Src activity disrupts cadherin/catenin-mediated homotypic adhesion in human colon cancer and transformed rodent cells. Cancer Res. 2002;62:2669–74.
pubmed: 11980666
Pishvaian MJ, Feltes CM, Thompson P, Bussemakers MJ, Schalken JA, Byers SW. Cadherin-11 is expressed in invasive breast cancer cell lines. Cancer Res. 1999;59:947–52.
pubmed: 10029089
Tamura D, Hiraga T, Myoui A, Yoshikawa H, Yoneda T. Cadherin-11-mediated interactions with bone marrow stromal/osteoblastic cells support selective colonization of breast cancer cells in bone. Int J Oncol. 2008;33:17–24.
pubmed: 18575746
Garcia R, Bowman TL, Niu G, Yu H, Minton S, Muro-Cacho CA, et al. Constitutive activation of Stat3 by the Src and JAK tyrosine kinases participates in growth regulation of human breast carcinoma cells. Oncogene 2001;20:2499–513.
pubmed: 11420660
doi: 10.1038/sj.onc.1204349
D’Abreo C. Role of Cadherin-11 and gp130 in transformation by activated Src. MSc thesis, Queen’s University. 2011.
Zhang Y, Turkson J, Carter-Su C, Smithgall T, Levitzki A, Kraker A, et al. Activation of Stat3 in v-Src transformed fibroblasts requires cooperation of Jak1 kinase activity. J Biol Chem. 2000;275:24935–44.
pubmed: 10823829
doi: 10.1074/jbc.M002383200
Geletu M, Adan H, Niit M, Arulanandam R, Carefoot E, Hoskin V, et al. Modulation of Akt vs Stat3 activity by the focal adhesion kinase in non-neoplastic mouse fibroblasts. Exp Cell Res. 2021;404:112601.
pubmed: 33957118
doi: 10.1016/j.yexcr.2021.112601
Wong JV, Dong P, Nevins JR, Mathey-Prevot B, You L. Network calisthenics: control of E2F dynamics in cell cycle entry. Cell Cycle. 2011;10:3086–94.
pubmed: 21900750
pmcid: 3218619
doi: 10.4161/cc.10.18.17350
Young AP, Nagarajan R, Longmore GD. Mechanisms of transcriptional regulation by Rb-E2F segregate by biological pathway. Oncogene 2003;22:7209–17.
pubmed: 14562049
doi: 10.1038/sj.onc.1206804
Tsai KY, Hu Y, Macleod KF, Crowley D, Yamasaki L, Jacks T. Mutation of E2f-1 suppresses apoptosis and inappropriate S phase entry and extends survival of Rb-deficient mouse embryos. Mol Cell. 1998;2:293–304.
pubmed: 9774968
doi: 10.1016/S1097-2765(00)80274-9
Moroni MC, Hickman ES, Lazzerini Denchi E, Caprara G, Colli E, Cecconi F, et al. Apaf-1 is a transcriptional target for E2F and p53. Nat Cell Biol. 2001;3:552–8.
pubmed: 11389439
doi: 10.1038/35078527
Leone G, DeGregori J, Sears R, Jakoi L, Nevins JR. Myc and Ras collaborate in inducing accumulation of active cyclin E/Cdk2 and E2F. Nature 1997;387:422–6.
pubmed: 9163430
doi: 10.1038/387422a0
Irwin M, Marin MC, Phillips AC, Seelan RS, Smith DI, Liu W, et al. Role for the p53 homologue p73 in E2F-1-induced apoptosis. Nature 2000;407:645–8.
pubmed: 11034215
doi: 10.1038/35036614
Vultur A, Arulanandam R, Turkson J, Niu G, Jove R, Raptis L. Stat3 is required for full neoplastic transformation by the Simian Virus 40 large tumor antigen. Mol Biol Cell. 2005;16:3832–46.
pubmed: 15917293
pmcid: 1182320
doi: 10.1091/mbc.e04-12-1104
Herold CI, Chadaram V, Peterson BL, Marcom PK, Hopkins J, Kimmick GG, et al. Phase II trial of dasatinib in patients with metastatic breast cancer using real-time pharmacodynamic tissue biomarkers of Src inhibition to escalate dosing. Clin Cancer Res. 2011;17:6061–70.
pubmed: 21810917
doi: 10.1158/1078-0432.CCR-11-1071
Finn RS, Bengala C, Ibrahim N, Roche H, Sparano J, Strauss LC, et al. Dasatinib as a single agent in triple-negative breast cancer: results of an open-label phase 2 study. Clin Cancer Res. 2011;17:6905–13.
pubmed: 22028489
doi: 10.1158/1078-0432.CCR-11-0288
Mayer EL, Baurain JF, Sparano J, Strauss L, Campone M, Fumoleau P, et al. A phase 2 trial of dasatinib in patients with advanced HER2-positive and/or hormone receptor-positive breast cancer. Clin Cancer Res. 2011;17:6897–904.
pubmed: 21903773
doi: 10.1158/1078-0432.CCR-11-0070
Tian J, Raffa FA, Dai M, Moamer A, Khadang B, Hachim IY, et al. Dasatinib sensitises triple negative breast cancer cells to chemotherapy by targeting breast cancer stem cells. Br J Cancer. 2018;119:1495–507.
pubmed: 30482914
pmcid: 6288167
doi: 10.1038/s41416-018-0287-3