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Research Paper

Deletion of caveolin scaffolding domain alters cancer cell migration

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Pages 1268-1280 | Received 03 May 2018, Accepted 08 May 2019, Published online: 22 May 2019

References

  • Kathuria H, Cao YX, Ramirez MI, et al. Transcription of the caveolin-1 gene is differentially regulated in lung type I epithelial and endothelial cell lines. A role for ETS proteins in epithelial cell expression. J Biol Chem. 2004;279:30028–30036.
  • Eberspacher E, Werner C, Engelhard K, et al. Long-term effects of hypothermia on neuronal cell death and the concentration of apoptotic proteins after incomplete cerebral ischemia and reperfusion in rats. Acta Anaesthesiol Scand. 2005;49:477–487.
  • Smart EJ, Ying Y, Donzell WC, et al. A role for caveolin in transport of cholesterol from endoplasmic reticulum to plasma membrane. J Biol Chem. 1996;271:29427–29435.
  • Busija AR, Patel HH, Insel PA. Caveolins and Cavins in the trafficking, maturation, and degradation of Caveolae: implications for cell physiology. Am J Physiol Cell Physiol. 2017;312:C459–C477.
  • Williams TM, Lisanti MP. The caveolin genes: from cell biology to medicine. Ann Med. 2004;36:584–595.
  • Patel HH, Insel PA. Lipid rafts and Caveolae and their role in compartmentation of redox signaling. Antioxid Redox Signal. 2009;11:1357–1372.
  • Patel HH, Murray F, Insel PA. G-protein-coupled receptor-signaling components in membrane raft and Caveolae microdomains. Handb Exp Pharmacol. 2008;186:167–184.
  • Patel HH, Murray F, Insel PA. Caveolae as organizers of pharmacologically relevant signal transduction molecules. Annu Rev Pharmacol Toxicol. 2008;48:359–391.
  • Bosch M, Marí M, Herms A, et al. Caveolin-1 deficiency causes cholesterol-dependent mitochondrial dysfunction and apoptotic susceptibility. Curr Biol. 2011;21:681-686.
  • Pol A, Martin S, Fernandez MA, et al. Dynamic and regulated association of caveolin with lipid bodies: modulation of lipid body motility and function by a dominant negative mutant. Mol Biology Cell. 2004;15:99–110.
  • Kuo CY, Lin YC, Yang JJ, et al. Interaction abolishment between mutant caveolin-1(Delta62-100) and ABCA1 reduces HDL-mediated cellular cholesterol efflux. Biochem Biophys Res Comm. 2011;414:337–343.
  • Lacroix-Triki M, Geyer FC, Reis-Filho JS. Caveolin-1 P132L mutation in human cancers: 1 Caveat to be voiced. J Mol Diag: JMD. 2010;12:562–565.
  • Schrauwen I, Szelinger S, Siniard AL, et al. A Frame-shift mutation in CAV1 is associated with a severe neonatal progeroid and lipodystrophy syndrome. PLoS One. 2015;10:e0131797.
  • Chanvorachote P, Chunhacha P. Caveolin-1 regulates endothelial adhesion of lung cancer cells via reactive oxygen species-dependent mechanism. PLoS One. 2013;8:e57466.
  • Bender F, Montoya M, Monardes V, et al. Caveolae and Caveolae-like membrane domains in cellular signaling and disease: identification of downstream targets for the tumor suppressor protein caveolin-1. Biol Res. 2002;35:151–167.
  • Burgermeister E, Liscovitch M, Röcken C, et al. Caveats of caveolin-1 in cancer progression. Cancer Lett.  2008;268:187–201.
  • Shatz M, Liscovitch M. Caveolin-1: a tumor-promoting role in human cancer. Int J Radiat Biol. 2008;84:177–189.
  • Senetta R, Stella G, Pozzi E, et al. Caveolin-1 as a promoter of tumour spreading: when, how, where and why. J Cell Mol Med. 2013;17:325–336.
  • Tse EY, Ko FC, Tung EK, et al. Caveolin-1 overexpression is associated with hepatocellular carcinoma tumourigenesis and metastasis. J Pathol. 2012;226:645–653.
  • Patani N, Martin LA, Reis-Filho JS, et al. The role of caveolin-1 in human breast cancer. Breast Cancer Res Treat. 2012;131:1–15.
  • Byrne DP, Dart C, Rigden DJ. Evaluating caveolin interactions: do proteins interact with the caveolin scaffolding domain through a widespread aromatic residue-rich motif? PLoS One. 2012;7:e44879.
  • Hoop CL, Sivanandam VN, Kodali R, et al. Structural characterization of the caveolin scaffolding domain in association with cholesterol-rich membranes. Biochemistry. 2012;51:90–99.
  • Tagawa A, Mezzacasa A, Hayer A, et al. Assembly and trafficking of Caveolar domains in the cell: Caveolae as stable, cargo-triggered, vesicular transporters. J Cell Biol. 2005;170:769–779.
  • Bucci M, Gratton JP, Rudic RD, et al. In vivo delivery of the caveolin-1 scaffolding domain inhibits nitric oxide synthesis and reduces inflammation. Nat Med. 2000;6:1362–1367.
  • Hehlgans S, Eke I, Storch K, et al. Caveolin-1 mediated radioresistance of 3D grown pancreatic cancer cells. Radiother Oncol. 2009;92:362–370.
  • Li L, Ren CH, Tahir SA, et al. Caveolin-1 maintains activated Akt in prostate cancer cells through scaffolding domain binding site interactions with and inhibition of serine/threonine protein phosphatases PP1 and PP2A. Mol Cell Biol. 2003;23:9389–9404.
  • Razani B, Woodman SE, Lisanti MP. Caveolae: from cell biology to animal physiology. Pharmacol Rev. 2002;54:431–467.
  • Razani B, Lisanti MP. Two distinct caveolin-1 domains mediate the functional interaction of caveolin-1 with protein kinase A. Am J Physiol Cell Physiol. 2001;281:C1241–50.
  • Schmitz M, Kloppner S, Klopfleisch S, et al. Mutual effects of caveolin and nerve growth factor signaling in pig oligodendrocytes. J Neurosci Res. 2010;88:572–588.
  • Schmitz M, Zerr I, Althaus HH. Effect of Cavtratin, a caveolin-1 scaffolding domain peptide, on oligodendroglial signaling cascades. Cell Molecular Neurobiol. 2011;31:991–997.
  • Capiod T. Extracellular calcium has multiple targets to control cell proliferation. Adv Exp Med Biol. 2016;898:133–156.
  • Kwiatek AM, Minshall RD, Cool DR, et al. Caveolin-1 regulates store-operated Ca2+ influx by binding of its scaffolding domain to transient receptor potential channel-1 in endothelial cells. Mol Pharmacol. 2006;70:1174–1183.
  • Pani B, Ong HL, Brazer SC, et al. Activation of TRPC1 by STIM1 in ER-PM microdomains involves release of the channel from its scaffold caveolin-1. Proc Nat Acad Sci USA. 2009;106:20087–20092.
  • Sundivakkam PC, Kwiatek AM, Sharma TT, et al. Caveolin-1 scaffold domain interacts with TRPC1 and IP3R3 to regulate Ca2+ store release-induced Ca2+ entry in endothelial cells. Am J Physiol Cell Physiol. 2009;296:C403–13.
  • Perez-Verdaguer M, Capera J, Martinez-Marmol R, et al. Caveolin interaction governs Kv1.3 lipid raft targeting. Sci Rep. 2016;6:22453.
  • Ohman E, Nilsson A, Madeira A, et al. Use of surface plasmon resonance coupled with mass spectrometry reveals an interaction between the voltage-gated sodium channel type X alpha-subunit and caveolin-1. J Prot Res. 2008;7:5333–5338.
  • Scanlon CS, Van Tubergen EA, Inglehart RC, et al. Biomarkers of epithelial-mesenchymal transition in squamous cell carcinoma. J Dent Res. 2013;92:114–121.
  • Schilling JM, Head BP, Patel HH. Caveolins as Regulators of Stress Adaptation. Mol Pharmacol. 2018;93:277–285.
  • Lamaze C, Tardif N, Dewulf M, et al. The Caveolae dress code: structure and signaling. Curr Opin Cell Biol. 2017;47:117–125.
  • Chen D, Che G. Value of caveolin-1 in cancer progression and prognosis: emphasis on cancer-associated fibroblasts, human cancer cells and mechanism of caveolin-1 expression (Review). Oncol Lett. 2014;8:1409–1421.
  • Han F, Zhu HG. Caveolin-1 regulating the invasion and expression of matrix metalloproteinase (MMPs) in pancreatic carcinoma cells. J Surg Res. 2010;159:443–450.
  • Chen CL, Hsieh FC, Lieblein JC, et al. Stat3 activation in human endometrial and cervical cancers. Br J Cancer. 2007;96:591–599.
  • Chatterjee M, Ben-Josef E, Thomas DG, et al. Caveolin-1 is associated with tumor progression and confers a multi-modality resistance phenotype in pancreatic cancer. Sci Rep. 2015;5:10867.
  • Chiu WT, Lee HT, Huang FJ, et al. Caveolin-1 upregulation mediates suppression of primary breast tumor growth and brain metastases by stat3 inhibition. Cancer Res. 2011;71:4932–4943.
  • Zhang HF, Lai R. STAT3 in Cancer-Friend or Foe? Cancers (Basel). 2014;6:1408–1440.
  • Jasmin JF, Mercier I, Sotgia F, et al. SOCS proteins and caveolin-1 as negative regulators of endocrine signaling. Trends Endocrinol Metabol. 2006;17:150–158.
  • Geletu M, Mohan R, Arulanandam R, 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.
  • Avalle L, Camporeale A, Camperi A, et al. STAT3 in cancer: A double edged sword. Cytokine. 2017;98:42–50.
  • Xiao F, Dc C. FAK mediates STAT3 activation, migration and invasion in ovarian carcinoma cells. Cancer Res. 2014;74(19 Suppl):Abstractnr 3095.
  • Parat MO, Riggins GJ. Caveolin-1, Caveolae, and glioblastoma. Neuro Oncol. 2012;14:679–688.
  • Nunez-Wehinger S, Ortiz RJ, Diaz N, et al. Caveolin-1 in cell migration and metastasis. Curr Mol Med. 2014;14:255–274.
  • Urra H, Torres VA, Ortiz RJ, et al. Caveolin-1-enhanced motility and focal adhesion turnover require tyrosine-14 but not accumulation to the rear in metastatic cancer cells. PLoS One. 2012;7:e33085.
  • Hernandez-Deviez DJ, Howes MT, Laval SH, et al. Caveolin regulates endocytosis of the muscle repair protein, dysferlin. J Biol Chem. 2008;283:6476–6488.
  • Shivshankar P, Halade GV, Calhoun C, et al. Caveolin-1 deletion exacerbates cardiac interstitial fibrosis by promoting M2 macrophage activation in mice after myocardial infarction. J Mol Cell Cardiol. 2014;76:84–93.
  • Yang J, Zhu T, Zhao R, et al. Caveolin-1 inhibits proliferation, migration, and invasion of human colorectal cancer cells by suppressing phosphorylation of epidermal growth factor receptor. Med Sci Monit. 2018;24:332–341.
  • Luanpitpong S, Talbott SJ, Rojanasakul Y, et al. Regulation of lung cancer cell migration and invasion by reactive oxygen species and caveolin-1. J Biol Chem. 2010;285:38832–38840.
  • Zhao X, Guan JL. Focal adhesion kinase and its signaling pathways in cell migration and angiogenesis. Adv Drug Deliv Rev. 2011;63:610–615.
  • Bolos V, Gasent JM, Lopez-Tarruella S, et al. The dual kinase complex FAK-Src as a promising therapeutic target in cancer. Onco Targets Ther. 2010;3:83–97.
  • Scheel J, Srinivasan J, Honnert U, et al. Involvement of caveolin-1 in meiotic cell-cycle progression in Caenorhabditis elegans. Nat Cell Biol. 1999;1:127–129.
  • Liu P, Rudick M, Anderson RG. Multiple functions of caveolin-1. J Biol Chem. 2002;277:41295–41298.
  • Galbiati F, Volonte D, Liu J, et al. Caveolin-1 expression negatively regulates cell cycle progression by inducing G(0)/G(1) arrest via a p53/p21(WAF1/Cip1)-dependent mechanism. Mol Biol Cell. 2001;12:2229–2244.
  • Fang K, Fu W, Beardsley AR, et al. Overexpression of caveolin-1 inhibits endothelial cell proliferation by arresting the cell cycle at G0/G1 phase. Cell Cycle (Georgetown, Tex). 2007;6:199–204.
  • Torres VA, Tapia JC, Rodriguez DA, et al. caveolin-1 controls cell proliferation and cell death by suppressing expression of the inhibitor of apoptosis protein survivin. J Cell Sci. 2006;119:1812–1823.
  • Feng Y, Venema VJ, Venema RC, et al. VEGF induces nuclear translocation of Flk-1/KDR, endothelial nitric oxide synthase, and caveolin-1 in vascular endothelial cells. Biochem Biophys Res Comm. 1999;256:192–197.
  • Sanna E, Miotti S, Mazzi M, et al. Binding of nuclear caveolin-1 to promoter elements of growth-associated genes in ovarian carcinoma cells. Exp Cell Res. 2007;313:1307–1317.
  • Joo JC, Hwang JH, Jo E, et al. Cordycepin induces apoptosis by caveolin-1-mediated JNK regulation of Foxo3a in human lung adenocarcinoma. Oncotarget. 2017;8:12211–12224.
  • Wang R, Zhang Q, Peng X, et al. Stellettin B induces G1 arrest, apoptosis and autophagy in human non-small cell lung cancer A549 cells via blocking PI3K/Akt/mTOR pathway. Sci Rep. 2016;6:27071.
  • Smits VA, Medema RH. Checking out the G(2)/M transition. Biochim Biophys Acta. 2001;1519:1–12.
  • Kang D, Chen J, Wong J, et al. The checkpoint protein Chfr is a ligase that ubiquitinates Plk1 and inhibits Cdc2 at the G2 to M transition. J Cell Biol. 2002;156:249–260.
  • Kawamoto H, Koizumi H, Uchikoshi T. Expression of the G2-M checkpoint regulators cyclin B1 and cdc2 in nonmalignant and malignant human breast lesions: immunocytochemical and quantitative image analyses. Am J Pathol. 1997;150:15–23.
  • Canela N, Rodriguez-Vilarrupla A, Estanyol JM, et al. The SET protein regulates G2/M transition by modulating cyclin B-cyclin-dependent kinase 1 activity. J Biol Chem. 2003;278:1158–1164.
  • Huang Y, Sramkoski RM, Jacobberger JW. The kinetics of G2 and M transitions regulated by B cyclins. PLoS One. 2013;8:e80861.
  • Head BP, Patel HH, Roth DM, et al. G-protein-coupled receptor signaling components localize in both sarcolemmal and intracellular caveolin-3-associated microdomains in adult cardiac myocytes. J Biol Chem. 2005;280:31036–31044.

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