The Role of WAVE2 Signaling in Cancer
Abstract
:1. Introduction
2. The WAVE Regulatory Complex
3. Role of WAVE2 in Cancer
3.1. WAVE2 in Colorectal Cancer
3.2. WAVE2 in Cervical Cancer
3.3. WAVE2 in Pancreatic Cancer
3.4. WAVE2 in Prostate Cancer
3.5. WAVE2 in Breast Cancer
4. WAVE2 Signaling Cascade
5. Activation of WAVE Regulatory Complex
6. WAVE2 Is Regulated by Several Phosphorylation Events
6.1. AbI Tyrosine Phosphorylation of WRC
6.2. SRC Tyrosine Phosphorylation of WRC
6.3. Serine/Threonine Phosphorylation of WRC
6.3.1. Cyclin-Dependent Kinases (CDKs)
6.3.2. Casein Kinase 2 (CK2)
6.3.3. ERK
6.3.4. Protein Kinase A
7. WAVE2 and MicroRNAs
8. Regulation of WAVE2 by Oncogenic Signals
8.1. Protein Kinase B (AKT)
8.2. TGF-β
8.3. VEGF
8.4. ERK-MAPK
9. Possible Targets for Drug Therapies for Preventing Metastasis and Invasion
10. Discussion
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Rana, P.S.; Kurokawa, M.; Model, M.A. Evidence for macromolecular crowding as a direct apoptotic stimulus. J. Cell Sci. 2020, 133. [Google Scholar] [CrossRef] [PubMed]
- Rana, P.S.; Model, M.A. A Reverse-Osmosis Model of Apoptotic Shrinkage. Front. Cell Dev. Biol. 2020, 8, 588721. [Google Scholar] [CrossRef] [PubMed]
- Martin, T.; Ye, L.; Sanders, A.; Lane, J.; Jiang, W. Cancer Invasion and Metastasis: Molecular and Cellular Perspective. In Madame Curie Bioscience Database [Internet]; Landes Bioscience: Austin, TX, USA, 2013. [Google Scholar]
- Tarin, D. Cell and tissue interactions in carcinogenesis and metastasis and their clinical significance. Semin. Cancer Biol. 2011, 21, 72–82. [Google Scholar] [CrossRef]
- Chambers, A.F.; Groom, A.C.; Macdonald, I.C. Dissemination and growth of cancer cells in metastatic sites. Nat. Rev. Cancer 2002, 2, 563–572. [Google Scholar] [CrossRef] [PubMed]
- Fidler, I.J. The pathogenesis of cancer metastasis: The “seed and soil” hypothesis revisited. Nat. Rev. Cancer 2003, 3, 453–458. [Google Scholar] [CrossRef]
- Welch, D.R.; Hurst, D.R. Defining the Hallmarks of Metastasis. Cancer Res. 2019, 79, 3011–3027. [Google Scholar] [CrossRef]
- Friedl, P.; Wolf, K. Plasticity of cell migration: A multiscale tuning model. J. Cell Biol. 2010, 188, 11–19. [Google Scholar] [CrossRef] [Green Version]
- Polacheck, W.J.; Zervantonakis, I.; Kamm, R.D. Tumor cell migration in complex microenvironments. Cell. Mol. Life Sci. 2012, 70, 1335–1356. [Google Scholar] [CrossRef] [Green Version]
- Yamaguchi, H.; Condeelis, J. Regulation of the actin cytoskeleton in cancer cell migration and invasion. Biochim. Biophys. Acta 2007, 1773, 642–652. [Google Scholar] [CrossRef] [Green Version]
- Mullins, R.D.; Kelleher, J.F.; Pollard, T.D. Actin’ like actin? Trends Cell Biol. 1996, 6, 208–212. [Google Scholar] [CrossRef]
- Welch, M.D.; DePace, A.H.; Verma, S.; Iwamatsu, A.; Mitchison, T.J. The human Arp2/3 complex is composed of evolutionarily conserved subunits and is localized to cellular regions of dynamic actin filament assembly. J. Cell Biol. 1997, 138, 375–384. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Blundell, M.P.; Worth, A.; Bouma, G.; Thrasher, A.J. The Wiskott-Aldrich syndrome: The actin cytoskeleton and immune cell function. Dis. Markers 2010, 29, 157–175. [Google Scholar] [CrossRef]
- Blanchoin, L.; Amann, K.J.; Higgs, H.; Marchand, J.-B.; Kaiser, D.A.; Pollard, T.D. Direct observation of dendritic actin filament networks nucleated by Arp2/3 complex and WASP/Scar proteins. Nat. Cell Biol. 2000, 404, 1007–1011. [Google Scholar] [CrossRef] [PubMed]
- Machesky, L.M.; Mullins, R.D.; Higgs, H.; Kaiser, D.A.; Blanchoin, L.; May, R.; Hall, M.E.; Pollard, T.D. Scar, a WASp-related protein, activates nucleation of actin filaments by the Arp2/3 complex. Proc. Natl. Acad. Sci. USA 1999, 96, 3739–3744. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mullins, R.D.; Heuser, J.A.; Pollard, T.D. The interaction of Arp2/3 complex with actin: Nucleation, high affinity pointed end capping, and formation of branching networks of filaments. Proc. Natl. Acad. Sci. USA 1998, 95, 6181–6186. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Welch, M.D.; Mullins, R.D. Cellular control of actin nucleation. Annu. Rev. Cell Dev. Biol. 2002, 18, 247–288. [Google Scholar] [CrossRef]
- Padrick, S.B.; Rosen, M.K. Physical mechanisms of signal integration by WASP family proteins. Annu. Rev. Biochem. 2010, 79, 707–735. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Paunola, E.; Mattila, P.; Lappalainen, P. WH2 domain: A small, versatile adapter for actin monomers. FEBS Lett. 2002, 513, 92–97. [Google Scholar] [CrossRef] [Green Version]
- Miki, H.; Suetsugu, S.; Takenawa, T. WAVE, a novel WASP-family protein involved in actin reorganization induced by Rac. EMBO J. 1998, 17, 6932–6941. [Google Scholar] [CrossRef] [Green Version]
- Kelly, A.E.; Kranitz, H.; Dotsch, V.; Mullins, R.D. Actin binding to the central domain of WASP/Scar proteins plays a critical role in the activation of the Arp2/3 complex. J. Biol. Chem. 2006, 281, 10589–10597. [Google Scholar] [CrossRef] [Green Version]
- Marchand, J.-B.; Kaiser, D.A.; Pollard, T.D.; Higgs, H. Interaction of WASP/Scar proteins with actin and vertebrate Arp2/3 complex. Nat. Cell Biol. 2000, 3, 76–82. [Google Scholar] [CrossRef] [PubMed]
- Kurisu, S.; Takenawa, T. The WASP and WAVE family proteins. Genome Biol. 2009, 10, 226. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Takenawa, T.; Miki, H. WASP and WAVE family proteins: Key molecules for rapid rearrangement of cortical actin filaments and cell movement. J. Cell Sci. 2001, 114, 1801–1809. [Google Scholar] [CrossRef] [PubMed]
- Stradal, T.; Rottner, K.; Disanza, A.; Confalonieri, S.; Innocenti, M.; Scita, G. Regulation of actin dynamics by WASP and WAVE family proteins. Trends Cell Biol. 2004, 14, 303–311. [Google Scholar] [CrossRef]
- Millard, T.H.; Sharp, S.J.; Machesky, L.M. Signalling to actin assembly via the WASP (Wiskott-Aldrich syndrome protein)-family proteins and the Arp2/3 complex. Biochem. J. 2004, 380 Pt 1, 1–17. [Google Scholar] [CrossRef] [Green Version]
- Miki, H.; Miura, K.; Takenawa, T. N-WASP, a novel actin-depolymerizing protein, regulates the cortical cytoskeletal rearrangement in a PIP2-dependent manner downstream of tyrosine kinases. EMBO J. 1996, 15, 5326–5335. [Google Scholar] [CrossRef]
- Massaad, M.J.; Ramesh, N.; Geha, R.S. Wiskott-Aldrich syndrome: A comprehensive review. Ann. N. Y. Acad. Sci. 2013, 1285, 26–43. [Google Scholar] [CrossRef]
- Tsuboi, S.; Nonoyama, S.; Ochs, H.D. Wiskott–Aldrich syndrome protein is involved in αIIbβ3-mediated cell adhesion. EMBO Rep. 2006, 7, 506–511. [Google Scholar] [CrossRef] [Green Version]
- Semple, J.W.; Siminovitch, K.A.; Mody, M.; Milev, Y.; Lazarus, A.H.; Wright, J.F.; Freedman, J. Flow cytometric analysis of platelets from childrenwith the Wiskott-Aldrich syndrome reveals defects in platelet development, activation and structure. Br. J. Haematol. 1997, 97, 747–754. [Google Scholar] [CrossRef]
- Baldini, M.G. Nature of the platelet DEFECT in the Wiskott-Aldrich Syndrome. Ann. N. Y. Acad. Sci. 1972, 201, 437–444. [Google Scholar] [CrossRef]
- Gröttum, K.A.; Hovig, T.; Holmsen, H.; Abrahamsen, A.F.; Jeremic, M.; Seip, M. Wiskott—Aldrich Syndrome: Qualitative Platelet Defects and Short Platelet Survival. Br. J. Haematol. 1969, 17, 373–388. [Google Scholar] [CrossRef] [PubMed]
- Shcherbina, A.; Rosen, F.S.; Remold-O’Donnell, E. WASP levels in platelets and lymphocytes of wiskott-aldrich syndrome patients correlate with cell dysfunction. J. Immunol. 1999, 163, 6314–6320. [Google Scholar] [PubMed]
- Prislovsky, A.; Zeng, X.; Sokolic, R.A.; Garabedian, E.N.; Anur, P.; Candotti, F.; Strom, T.S. Platelets from WAS patients show an increased susceptibility toex vivophagocytosis. Platelets 2013, 24, 288–296. [Google Scholar] [CrossRef] [Green Version]
- Marathe, B.M.; Prislovsky, A.; Astrakhan, A.; Rawlings, D.J.; Wan, J.Y.; Strom, T.S. Antiplatelet antibodies in WASP (-) mice correlate with evidence of increased in vivo platelet consumption. Exp. Hematol. 2009, 37, 1353–1363. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Prislovsky, A.; Marathe, B.; Hosni, A.; Bolen, A.L.; Nimmerjahn, F.; Jackson, C.W.; Weiman, D.; Strom, T.S. Rapid platelet turnover in WASP (-) mice correlates with increased ex vivo phagocytosis of opsonized WASP (-) platelets. Exp. Hematol. 2008, 36, 609–623. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rottner, K.; Faix, J.; Bogdan, S.; Linder, S.; Kerkhoff, E. Actin assembly mechanisms at a glance. J. Cell Sci. 2017, 130, 3427–3435. [Google Scholar] [CrossRef] [Green Version]
- Lebensohn, A.M.; Kirschner, M.W. Activation of the WAVE Complex by Coincident Signals Controls Actin Assembly. Mol. Cell 2009, 36, 512–524. [Google Scholar] [CrossRef] [Green Version]
- Suetsugu, S.; Kurisu, S.; Oikawa, T.; Yamazaki, D.; Oda, A.; Takenawa, T. Optimization of WAVE2 complex–induced actin polymerization by membrane-bound IRSp53, PIP3, and Rac. J. Cell Biol. 2006, 173, 571–585. [Google Scholar] [CrossRef]
- Miki, H.; Yamaguchi, H.; Suetsugu, S.; Takenawa, T. IRSp53 is an essential intermediate between Rac and WAVE in the regulation of membrane ruffling. Nat. Cell Biol. 2000, 408, 732–735. [Google Scholar] [CrossRef]
- Dahl, J.P.; Wang-Dunlop, J.; Gonzales, C.; Goad, M.E.P.; Mark, R.J.; Kwak, S.P. Characterization of the WAVE1 Knock-Out Mouse: Implications for CNS Development. J. Neurosci. 2003, 23, 3343–3352. [Google Scholar] [CrossRef] [Green Version]
- Yan, C.; Martinez-Quiles, N.; Eden, S.; Shibata, T.; Takeshima, F.; Shinkura, R.; Fujiwara, Y.; Bronson, R.; Snapper, S.B.; Kirschner, M.W.; et al. WAVE2 deficiency reveals distinct roles in embryogenesis and Rac-mediated actin-based motility. EMBO J. 2003, 22, 3602–3612. [Google Scholar] [CrossRef] [Green Version]
- Qin, H.; Lu, S.; Thangaraju, M.; Cowell, J.K. Wasf3 Deficiency Reveals Involvement in Metastasis in a Mouse Model of Breast Cancer. Am. J. Pathol. 2019, 189, 2450–2458. [Google Scholar] [CrossRef]
- Innocenti, M.; Zucconi, A.; Disanza, A.; Frittoli, E.; Areces, L.B.; Steffen, A.; Stradal, T.; Di Fiore, P.P.; Carlier, M.-F.; Scita, G. Abi1 is essential for the formation and activation of a WAVE2 signalling complex. Nat. Cell Biol. 2004, 6, 319–327. [Google Scholar] [CrossRef]
- Eden, S.; Rohatgi, R.; Podtelejnikov, A.V.; Mann, M.; Kirschner, M.W. Mechanism of regulation of WAVE1-induced actin nucleation by Rac1 and Nck. Nat. Cell Biol. 2002, 418, 790–793. [Google Scholar] [CrossRef] [PubMed]
- Chen, Z.; Borek, D.; Padrick, S.; Gomez, T.S.; Metlagel, Z.; Ismail, A.M.; Umetani, J.; Billadeau, D.D.; Otwinowski, Z.; Rosen, M.K. Structure and control of the actin regulatory WAVE complex. Nat. Cell Biol. 2010, 468, 533–538. [Google Scholar] [CrossRef] [PubMed]
- Mendoza, M.C. Phosphoregulation of the WAVE regulatory complex and signal integration. In Seminars in Cell & Developmental Biology; Academic Press: Cambridge, MA, USA, 2013. [Google Scholar]
- Campellone, K.G.; Welch, M.D. A nucleator arms race: Cellular control of actin assembly. Nat. Rev. Mol. Cell Biol. 2010, 11, 237–251. [Google Scholar] [CrossRef] [Green Version]
- Pollard, T.D. Regulation of actin filament assembly by Arp2/3 complex and formins. Annu. Rev. Biophys. Biomol. Struct. 2007, 36, 451–477. [Google Scholar] [CrossRef] [PubMed]
- Chen, B.; Chou, H.-T.; Brautigam, C.A.; Xing, W.; Yang, S.; Henry, L.; Doolittle, L.K.; Walz, T.; Rosen, M.K. Rac1 GTPase activates the WAVE regulatory complex through two distinct binding sites. eLife 2017, 6, e29795. [Google Scholar] [CrossRef]
- Takahashi, K.; Suzuki, K. WAVE2 targeting to phosphatidylinositol 3,4,5-triphosphate mediated by insulin receptor substrate p53 through a complex with WAVE. Cell. Signal. 2010, 22, 1708–1716. [Google Scholar] [CrossRef]
- Oikawa, T.; Yamaguchi, H.; Itoh, T.; Kato, M.; Ijuin, T.; Yamazaki, D.; Suetsugu, S.; Takenawa, T. PtdIns(3,4,5)P3 binding is necessary for WAVE2-induced formation of lamellipodia. Nat. Cell Biol. 2004, 6, 420–426. [Google Scholar] [CrossRef]
- Sossey-Alaoui, K.; Head, K.; Nowak, N.; Cowell, J. Genomic organization and expression profile of the human and mouse WAVE gene family. Mamm. Genome 2003, 14, 314–322. [Google Scholar] [CrossRef]
- Sossey-Alaoui, K. Surfing the big WAVE: Insights into the role of WAVE3 as a driving force in cancer progression and metastasis. Semin. Cell Dev. Biol. 2012, 24, 287–297. [Google Scholar] [CrossRef] [Green Version]
- Kurisu, S.; Suetsugu, S.; Yamazaki, D.; Yamaguchi, H.; Takenawa, T. Rac-WAVE2 signaling is involved in the invasive and metastatic phenotypes of murine melanoma cells. Oncogene 2004, 24, 1309–1319. [Google Scholar] [CrossRef] [Green Version]
- Sossey-Alaoui, K.; Ranalli, T.A.; Li, X.; Bakin, A.; Cowell, J. WAVE3 promotes cell motility and invasion through the regulation of MMP-1, MMP-3, and MMP-9 expression. Exp. Cell Res. 2005, 308, 135–145. [Google Scholar] [CrossRef] [PubMed]
- Wang, W.; Kansakar, U.; Markovic, V.; Wang, B.; Sossey-Alaoui, K. WAVE3 phosphorylation regulates the interplay between PI3K, TGF-β, and EGF signaling pathways in breast cancer. Oncogenesis 2020, 9, 1–13. [Google Scholar] [CrossRef] [PubMed]
- Siegel, R.L.; Miller, K.D.; Fuchs, H.E.; Jemal, A. Cancer Statistics. CA Cancer J. Clin. 2021, 71, 7–33. [Google Scholar] [CrossRef]
- Park, B.V.; Freeman, Z.; Ghasemzadeh, A.; Chattergoon, M.A.; Rutebemberwa, A.; Steigner, J.; Winter, M.E.; Huynh, T.V.; Sebald, S.M.; Lee, S.-J.; et al. TGFβ1-Mediated SMAD3 Enhances PD-1 Expression on Antigen-Specific T Cells in Cancer. Cancer Discov. 2016, 6, 1366–1381. [Google Scholar] [CrossRef] [Green Version]
- Na Sun, L.; Xing, C.; Zhi, Z.; Liu, Y.; Chen, L.-Y.; Shen, T.; Zhou, Q.; Liu, Y.H.; Gan, W.J.; Wang, J.-R.; et al. Dicer suppresses cytoskeleton remodeling and tumorigenesis of colorectal epithelium by miR-324-5p mediated suppression of HMGXB3 and WASF-2. Oncotarget 2017, 8, 55776–55789. [Google Scholar] [CrossRef] [PubMed]
- Iwaya, K.; Oikawa, K.; Semba, S.; Tsuchiya, B.; Mukai, Y.; Otsubo, T.; Nagao, T.; Izumi, M.; Kuroda, M.; Domoto, H.; et al. Correlation between liver metastasis of the colocalization of actin-related protein 2 and 3 complex and WAVE2 in colorectal carcinoma. Cancer Sci. 2007, 98, 992–999. [Google Scholar] [CrossRef]
- Tan, F.; He, D.; Hu, K.; Wang, D.; Zhang, S.; Li, J.; Wang, Z.; Tao, Y. WAVE2 Enhanced Hepatic Stellate Cells Activity in Colorectal Liver Metastases. Cancer Manag. Res. 2020, 12, 7671–7680. [Google Scholar] [CrossRef] [PubMed]
- Li, K.; Peng, Y.-F.; Guo, J.-Z.; Li, M.; Zhang, Y.; Chen, J.-Y.; Lin, T.-R.; Yu, X.; Yu, W.-D. Abelson interactor 1 splice isoform-L plays an anti-oncogenic role in colorectal carcinoma through interactions with WAVE2 and full-length Abelson interactor 1. World J. Gastroenterol. 2021, 27, 1595–1615. [Google Scholar] [CrossRef]
- Wang, J.; Feng, Y.; Chen, X.; Du, Z.; Jiang, S.; Ma, S.; Zou, W. SH3BP1-induced Rac-Wave2 pathway activation regulates cervical cancer cell migration, invasion, and chemoresistance to cisplatin. J. Cell. Biochem. 2018, 119, 1733–1745. [Google Scholar] [CrossRef] [PubMed]
- Taniuchi, K.; Furihata, M.; Naganuma, S.; Saibara, T. WAVE2 is associated with poor prognosis in pancreatic cancers and promotes cell motility and invasiveness via binding to ACTN4. Cancer Med. 2018, 7, 5733–5751. [Google Scholar] [CrossRef] [PubMed]
- Taniuchi, K.; Yawata, T.; Tsuboi, M.; Ueba, T.; Saibara, T. Efficient delivery of small interfering RNAs targeting particular mRNAs into pancreatic cancer cells inhibits invasiveness and metastasis of pancreatic tumors. Oncotarget 2019, 10, 2869–2886. [Google Scholar] [CrossRef] [Green Version]
- Kitagawa, T.; Taniuchi, K.; Tsuboi, M.; Sakaguchi, M.; Kohsaki, T.; Okabayashi, T.; Saibara, T. Circulating pancreatic cancer exosomal RNA s for detection of pancreatic cancer. Mol. Oncol. 2019, 13, 212–227. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kato, T.; Kawai, K.; Egami, Y.; Kakehi, Y.; Araki, N. Rac1-dependent lamellipodial motility in prostate cancer PC-3 cells revealed by Optogenetic control of rac1 activity. PLoS ONE 2014, 9, e97749. [Google Scholar] [CrossRef] [Green Version]
- Sung, H.; Ferlay, J.; Siegel, R.L.; Laversanne, M.; Soerjomataram, I.; Jemal, A.; Bray, F. Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries. CA Cancer J. Clin. 2021, 71, 209–249. [Google Scholar] [CrossRef]
- Thike, A.A.; Cheok, P.Y.; Jara-Lazaro, A.R.; Tan, B.; Tan, P.; Tan, P.H. Triple-negative breast cancer: Clinicopathological characteristics and relationship with basal-like breast cancer. Mod. Pathol. 2009, 23, 123–133. [Google Scholar] [CrossRef] [Green Version]
- Welch, M.D.; Iwamatsu, A.; Mitchison, T.J. Actin polymerization is induced by Arp 2/3 protein complex at the surface of Listeria monocytogenes. Nat. Cell Biol. 1997, 385, 265–269. [Google Scholar] [CrossRef] [PubMed]
- Machesky, L.; Atkinson, S.J.; Ampe, C.; Vandekerckhove, J.; Pollard, T.D. Purification of a cortical complex containing two unconventional actins from Acanthamoeba by affinity chromatography on profilin-agarose. J. Cell Biol. 1994, 127, 107–115. [Google Scholar] [CrossRef] [PubMed]
- Ko, H.S.; Kim, J.S.; Cho, S.M.; Lee, H.-J.; Ahn, K.S.; Kim, S.-H.; Lee, E.-O. Urokinase-type plasminogen activator expression and Rac1/WAVE-2/Arp2/3 pathway are blocked by pterostilbene to suppress cell migration and invasion in MDA-MB-231 cells. Bioorg. Med. Chem. Lett. 2014, 24, 1176–1179. [Google Scholar] [CrossRef] [Green Version]
- Bryce, N.S.; Reynolds, A.B.; Koleske, A.J.; Weaver, A.M. WAVE2 Regulates Epithelial Morphology and Cadherin Isoform Switching through Regulation of Twist and Abl. PLoS ONE 2013, 8, e64533. [Google Scholar] [CrossRef]
- Takahashi, K.; Suzuki, K. WAVE2, N-WASP, and mena facilitate cell invasion via phosphatidylinositol 3-kinase-dependent local accumulation of actin filaments. J. Cell. Biochem. 2011, 112, 3421–3429. [Google Scholar] [CrossRef] [PubMed]
- Yokotsuka, M.; Iwaya, K.; Saito, T.; Pandiella, A.; Tsuboi, R.; Kohno, N.; Matsubara, O.; Mukai, K. Overexpression of HER2 signaling to WAVE2–Arp2/3 complex activates MMP-independent migration in breast cancer. Breast Cancer Res. Treat. 2010, 126, 311–318. [Google Scholar] [CrossRef] [PubMed]
- Yamazaki, D.; Suetsugu, S.; Miki, H.; Kataoka, Y.; Nishikawa, S.-I.; Fujiwara, T.; Yoshida, N.; Takenawa, T. WAVE2 is required for directed cell migration and cardiovascular development. Nat. Cell Biol. 2003, 424, 452–456. [Google Scholar] [CrossRef] [PubMed]
- Suetsugu, S.; Yamazaki, D.; Kurisu, S.; Takenawa, T. Differential roles of WAVE1 and WAVE2 in dorsal and peripheral ruffle formation for fibroblast cell migration. Dev. Cell 2003, 5, 595–609. [Google Scholar] [CrossRef] [Green Version]
- Kunda, P.; Craig, G.; Dominguez, V.; Baum, B. Abi, Sra1, and Kette Control the Stability and Localization of SCAR/WAVE to Regulate the Formation of Actin-Based Protrusions. Curr. Biol. 2003, 13, 1867–1875. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yeh, T.C.; Ogawa, W.; Danielsen, A.G.; Roth, R.A. Characterization and cloning of a 58/53-kDa substrate of the insulin receptor tyrosine kinase. J. Biol. Chem. 1996, 271, 2921–2928. [Google Scholar] [CrossRef] [Green Version]
- Zhao, H.; Pykäläinen, A.; Lappalainen, P. I-BAR domain proteins: Linking actin and plasma membrane dynamics. Curr. Opin. Cell Biol. 2011, 23, 14–21. [Google Scholar] [CrossRef]
- Mattila, P.; Pykalainen, A.; Saarikangas, J.; Paavilainen, V.; Vihinen, H.; Jokitalo, E.; Lappalainen, P. Missing-in-metastasis and IRSp53 deform PI(4,5)P2-rich membranes by an inverse BAR domain–like mechanism. J. Cell Biol. 2007, 176, 953–964. [Google Scholar] [CrossRef] [PubMed]
- Ismail, A.M.; Padrick, S.; Chen, B.; Umetani, J.; Rosen, M.K. The WAVE regulatory complex is inhibited. Nat. Struct. Mol. Biol. 2009, 16, 561–563. [Google Scholar] [CrossRef]
- Takahashi, K. WAVE2 protein complex coupled to membrane and microtubules. J. Oncol. 2012, 2012, 1–11. [Google Scholar] [CrossRef] [Green Version]
- Yuan, T.L.; Cantley, L.C. PI3K pathway alterations in cancer: Variations on a theme. Oncogene 2008, 27, 5497–5510. [Google Scholar] [CrossRef] [Green Version]
- Côté, J.-F.; Vuori, K. GEF what? Dock180 and related proteins help Rac to polarize cells in new ways. Trends Cell Biol. 2007, 17, 383–393. [Google Scholar] [CrossRef] [Green Version]
- Rossman, K.L.; Der, C.; Sondek, J. GEF means go: Turning on RHO GTPases with guanine nucleotide-exchange factors. Nat. Rev. Mol. Cell Biol. 2005, 6, 167–180. [Google Scholar] [CrossRef] [PubMed]
- Leng, Y.; Zhang, J.; Badour, K.; Arpaia, E.; Freeman, S.; Cheung, P.; Siu, M.; Siminovitch, K. Abelson-interactor-1 promotes WAVE2 membrane translocation and Abelson-mediated tyrosine phosphorylation required for WAVE2 activation. Proc. Natl. Acad. Sci. USA 2005, 102, 1098–1103. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Salgia, R.; Li, J.-L.; Ewaniuk, D.S.; Pear, W.; Pisick, E.; Burky, S.A.; Ernst, T.; Sattler, M.; Chen, L.B.; Griffin, J.D. BCR/ABL induces multiple abnormalities of cytoskeletal function. J. Clin. Investig. 1997, 100, 46–57. [Google Scholar] [CrossRef]
- Huang, Y.; Comiskey, E.O.; DuPree, R.S.; Li, S.; Koleske, A.J.; Burkhardt, J. The c-Abl tyrosine kinase regulates actin remodeling at the immune synapse. Blood 2008, 112, 111–119. [Google Scholar] [CrossRef] [PubMed]
- Van Etten, R.A. Cycling, stressed-out and nervous: Cellular functions of c-Abl. Trends Cell Biol. 1999, 9, 179–186. [Google Scholar] [CrossRef] [Green Version]
- Zhuang, C.; Tang, H.; Dissanaike, S.; Cobos, E.; Tao, Y.; Dai, Z. CDK1-mediated phosphorylation of abi1 attenuates Bcr-Abl-induced F-actin assembly and tyrosine phosphorylation of WAVE complex during mitosis. J. Biol. Chem. 2011, 286, 38614–38626. [Google Scholar] [CrossRef] [Green Version]
- Stuart, J.R.; Gonzalez, F.H.; Kawai, H.; Yuan, Z.-M. c-Abl interacts with the WAVE2 signaling complex to induce membrane ruffling and cell spreading. J. Biol. Chem. 2006, 281, 31290–31297. [Google Scholar] [CrossRef]
- Li, Y.; Clough, N.; Sun, X.; Yu, W.; Abbott, B.L.; Hogan, C.J.; Dai, Z. Bcr-Abl induces abnormal cytoskeleton remodeling, β1 integrin clustering and increased cell adhesion to fibronectin through the Abl interactor 1 pathway. J. Cell Sci. 2007, 120, 1436–1446. [Google Scholar] [CrossRef] [Green Version]
- Ardern, H.; Sandilands, E.; Machesky, L.M.; Timpson, P.; Frame, M.C.; Brunton, V.G. Src-dependent phosphorylation of Scar1 promotes its association with the Arp2/3 complex. Cell Motil. Cytoskelet. 2006, 63, 6–13. [Google Scholar] [CrossRef]
- Frame, M.C. Src in cancer: Deregulation and consequences for cell behaviour. Biochim. Biophys. Acta 2002, 1602, 114–130. [Google Scholar] [CrossRef]
- Yeatman, T.J. A renaissance for SRC. Nat. Rev. Cancer 2004, 4, 470–480. [Google Scholar] [CrossRef]
- Guarino, M. Src signaling in cancer invasion. J. Cell. Physiol. 2010, 223, 14–26. [Google Scholar] [CrossRef]
- Miyamoto, Y.; Yamauchi, J.; Tanoue, A. Cdk5 phosphorylation of WAVE2 regulates oligodendrocyte precursor cell migration through nonreceptor tyrosine kinase fyn. J. Neurosci. 2008, 28, 8326–8337. [Google Scholar] [CrossRef] [Green Version]
- Ortega, C.E.; Seidner, Y.; Dominguez, I. Mining CK2 in cancer. PLoS ONE 2014, 9, e115609. [Google Scholar] [CrossRef] [PubMed]
- Pocha, S.M.; Cory, G.O. WAVE2 is regulated by multiple phosphorylation events within its VCA domain. Cell Motil. Cytoskelet. 2009, 66, 36–47. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ura, S.; Pollitt, A.Y.; Veltman, D.M.; Morrice, N.A.; Machesky, L.; Insall, R.H. Pseudopod growth and evolution during cell movement is controlled through SCAR/WAVE dephosphorylation. Curr. Biol. 2012, 22, 553–561. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Danson, C.M.; Pocha, S.M.; Bloomberg, G.B.; Cory, G.O. Phosphorylation of WAVE2 by MAP kinases regulates persistent cell migration and polarity. J. Cell Sci. 2007, 120, 4144–4154. [Google Scholar] [CrossRef] [Green Version]
- Mendoza, M.C.; Er, E.E.; Zhang, W.; Ballif, B.A.; Elliott, H.L.; Danuser, G.; Blenis, J. ERK-MAPK Drives Lamellipodia Protrusion by Activating the WAVE2 Regulatory Complex. Mol. Cell 2011, 41, 661–671. [Google Scholar] [CrossRef] [Green Version]
- Nakanishi, O.; Suetsugu, S.; Yamazaki, D.; Takenawa, T. Effect of WAVE2 phosphorylation on activation of the Arp2/3 complex. J. Biochem. 2006, 141, 319–325. [Google Scholar] [CrossRef]
- Ceglia, I.; Kim, Y.; Nairn, A.C.; Greengard, P. Signaling pathways controlling the phosphorylation state of WAVE1, a regulator of actin polymerization. J. Neurochem. 2010, 114, 182–190. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yamashita, H.; Ueda, K.; Kioka, N. WAVE2 forms a complex with PKA and is involved in PKA enhancement of membrane protrusions. J. Biol. Chem. 2011, 286, 3907–3914. [Google Scholar] [CrossRef] [Green Version]
- Westphal, R.S.; Soderling, S.H.; Alto, N.M.; Langeberg, L.K.; Scott, J.D. Scar/WAVE-1, a Wiskott-Aldrich syndrome protein, assembles an actin-associated multi-kinase scaffold. EMBO J. 2000, 19, 4589–4600. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hao, J.; Lai, M.; Liu, C. Expression of miR-335 in triple-negative breast cancer and its effect on chemosensitivity. J. Buon 2019, 24, 1526–1531. [Google Scholar] [PubMed]
- Wang, J.; Tsouko, E.; Jonsson, P.; Bergh, J.; Hartman, J.; Aydogdu, E.; Williams, C. miR-206 inhibits cell migration through direct targeting of the actin-binding protein Coronin 1C in triple-negative breast cancer. Mol. Oncol. 2014, 8, 1690–1702. [Google Scholar] [CrossRef] [PubMed]
- Damiano, V.; Brisotto, G.; Borgna, S.; di Gennaro, A.; Armellin, M.; Perin, T.; Guardascione, M.; Maestro, R.; Santarosa, M. Epigenetic silencing of miR-200c in breast cancer is associated with aggressiveness and is modulated by ZEB1. Genes Chromosom. Cancer 2017, 56, 147–158. [Google Scholar] [CrossRef]
- Meng, Z.; Zhang, R.; Wang, Y.; Zhu, G.; Jin, T.; Li, C.; Zhang, S. miR-200c/PAI-2 promotes the progression of triple negative breast cancer via M1/M2 polarization induction of macrophage. Int. Immunopharmacol. 2020, 81, 106028. [Google Scholar] [CrossRef] [PubMed]
- Han, B.; Huang, J.; Han, Y.; Hao, J.; Wu, X.; Song, H.; Chen, X.; Shen, Q.; Dong, X.; Pang, H.; et al. The microRNA miR-181c enhances chemosensitivity and reduces chemoresistance in breast cancer cells via down-regulating osteopontin. Int. J. Biol. Macromol. 2019, 125, 544–556. [Google Scholar] [CrossRef]
- Hong, Z.; Hong, C.; Ma, B.; Wang, Q.; Zhang, X.; Li, L.; Wang, C.; Chen, D. MicroRNA-126-3p inhibits the proliferation, migration, invasion, and angiogenesis of triple-negative breast cancer cells by targeting RGS3. Oncol. Rep. 2019, 42, 1569–1579. [Google Scholar] [CrossRef] [PubMed]
- Yu, B.; You, W.; Chen, G.; Yu, Y.; Yang, Q. MiR-140-5p inhibits cell proliferation and metastasis by regulating MUC1 via BCL2A1/MAPK pathway in triple negative breast cancer. Cell Cycle 2019, 18, 2641–2650. [Google Scholar] [CrossRef] [PubMed]
- Weihua, Z.; GuoRong, Z.; Xiaolong, C.; Weizhan, L. MiR-33a functions as a tumor suppressor in triple-negative breast cancer by targeting EZH2. Cancer Cell Int. 2020, 20, 1–12. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kawaguchi, T.; Yan, L.; Qi, Q.; Peng, X.; Gabriel, E.M.; Young, J.; Liu, S.; Takabe, K. Overexpression of suppressive microRNAs, miR-30a and miR-200c are associated with improved survival of breast cancer patients. Sci. Rep. 2017, 7, 15945. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Derivery, E.; Fink, J.; Martin, D.; Houdusse, A.; Piel, M.; Stradal, T.E.; Louvard, D.; Gautreau, A. Free Brick1 is a trimeric precursor in the assembly of a functional wave complex. PLoS ONE 2008, 3, e2462. [Google Scholar] [CrossRef] [PubMed]
- Escobar, B.; de Cárcer, G.; Fernández-Miranda, G.; Cascon, A.; Bravo-Cordero, J.J.; Montoya, M.; Robledo, M.; Cañamero, M.; Malumbres, M. Brick1 is an essential regulator of actin cytoskeleton required for embryonic development and cell transformation. Cancer Res. 2010, 70, 9349–9359. [Google Scholar] [CrossRef] [Green Version]
- Cai, X.; Xiao, T.; James, S.Y.; Da, J.; Lin, N.; Liu, Y.; Zheng, Y.; Zou, S.; Di, X.; Guo, S.; et al. Metastatic potential of lung squamous cell carcinoma associated with HSPC300 through its interaction with WAVE2. Lung Cancer 2009, 65, 299–305. [Google Scholar] [CrossRef]
- Wang, Q.-Y.; Zhou, C.-X.; Zhan, M.-N.; Tang, J.; Wang, C.-L.; Ma, C.-N.; He, M.; Chen, G.-Q.; He, J.-R.; Zhao, Q. MiR-133b targets Sox9 to control pathogenesis and metastasis of breast cancer. Cell Death Dis. 2018, 9, 752. [Google Scholar] [CrossRef]
- Takenawa, T.; Suetsugu, S. The WASP-WAVE protein network: Connecting the membrane to the cytoskeleton. Nat. Rev. Mol. Cell. Biol. 2007, 8, 37–48. [Google Scholar] [CrossRef]
- Insall, R.H.; Machesky, L.M. Actin Dynamics at the Leading Edge: From Simple Machinery to Complex Networks. Dev. Cell 2009, 17, 310–322. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Derivery, E.; Gautreau, A. Generation of branched actin networks: Assembly and regulation of the N-WASP and WAVE molecular machines. Bioessays 2010, 32, 119–131. [Google Scholar] [CrossRef] [PubMed]
- Bellacosa, A.; Kumar, C.C.; Di Cristofano, A.; Testa, J.R. Activation of AKT kinases in cancer: Implications for therapeutic targeting. Adv. Cancer Res. 2005, 94, 29–86. [Google Scholar] [PubMed]
- Liu, H.-W.; Bi, W.-T.; Huang, H.-T.; Li, R.-X.; Xi, Q.; Feng, L.; Bo, W.; Hu, M.; Wen, W.-S. Satb1 promotes Schwann cell viability and migration via activation of PI3K/AKT pathway. Eur. Rev. Med. Pharmacol. Sci. 2018, 22, 4268–4277. [Google Scholar] [CrossRef] [PubMed]
- Moraes, L.; Zanchin, N.I.; Cerutti, J.M. ABI3, a component of the WAVE2 complex, is potentially regulated by PI3K/AKT pathway. Oncotarget 2017, 8, 67769–67781. [Google Scholar] [CrossRef] [Green Version]
- Tian, M.; Schiemann, W.P. The TGFβ paradox in human cancer: An update. Future Oncol. 2009, 5, 259–271. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ferrari, G.; Cook, B.D.; Terushkin, V.; Pintucci, G.; Mignatti, P. Transforming growth factor-beta 1 (TGF-β1) induces angiogenesis through vascular endothelial growth factor (VEGF)-mediated apoptosis. J. Cell. Physiol. 2009, 219, 449–458. [Google Scholar] [CrossRef] [Green Version]
- Carmeliet, P. VEGF as a key mediator of angiogenesis in cancer. Oncology 2005, 69, 4–10. [Google Scholar] [CrossRef]
- Tao, Y.; Hu, K.; Tan, F.; Zhang, S.; Zhou, M.; Luo, J.; Wang, Z. SH3-domain binding protein 1 in the tumor microenvironment promotes hepatocellular carcinoma metastasis through WAVE2 pathway. Oncotarget 2016, 7, 18356–18370. [Google Scholar] [CrossRef]
- Holmqvist, K.; Cross, M.; Rolny, C.; Hägerkvist, R.; Rahimi, N.; Matsumoto, T.; Claesson-Welsh, L.; Welsh, M. The adaptor protein Shb binds to tyrosine 1175 in vascular endothelial growth factor (VEGF) receptor-2 and regulates VEGF-dependent cellular migration. J. Biol. Chem. 2004, 279, 22267–22275. [Google Scholar] [CrossRef] [Green Version]
- Kim, J.S.; Kang, C.G.; Kim, S.-H.; Lee, E.-O. Rhapontigenin suppresses cell migration and invasion by inhibiting the PI3K-dependent Rac1 signaling pathway in MDA-MB-231 human breast cancer cells. J. Nat. Prod. 2014, 77, 1135–1139. [Google Scholar] [CrossRef] [PubMed]
- Morgan-Fisher, M.; Wewer, U.M.; Yoneda, A. Regulation of ROCK Activity in Cancer. J. Histochem. Cytochem. 2012, 61, 185–198. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sanz-Moreno, V.; Gadea, G.; Ahn, J.; Paterson, H.; Marra, P.; Pinner, S.; Sahai, E.; Marshall, C.J. Rac Activation and Inactivation Control Plasticity of Tumor Cell Movement. Cell 2008, 135, 510–523. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Uehata, M.; Ishizaki, T.; Satoh, H.; Ono, T.; Kawahara, T.; Morishita, T.; Tamakawa, H.; Yamagami, K.; Inui, J.; Maekawa, M.; et al. Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nat. Cell Biol. 1997, 389, 990–994. [Google Scholar] [CrossRef] [PubMed]
- Asano, T.; Ikegaki, I.; Satoh, S.; Suzuki, Y.; Shibuya, M.; Takayasu, M.; Hidaka, H. Mechanism of action of a novel antivasospasm drug, HA1077. J. Pharmacol. Exp. Ther. 1987, 241, 1033–1040. [Google Scholar]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Rana, P.S.; Alkrekshi, A.; Wang, W.; Markovic, V.; Sossey-Alaoui, K. The Role of WAVE2 Signaling in Cancer. Biomedicines 2021, 9, 1217. https://doi.org/10.3390/biomedicines9091217
Rana PS, Alkrekshi A, Wang W, Markovic V, Sossey-Alaoui K. The Role of WAVE2 Signaling in Cancer. Biomedicines. 2021; 9(9):1217. https://doi.org/10.3390/biomedicines9091217
Chicago/Turabian StyleRana, Priyanka Shailendra, Akram Alkrekshi, Wei Wang, Vesna Markovic, and Khalid Sossey-Alaoui. 2021. "The Role of WAVE2 Signaling in Cancer" Biomedicines 9, no. 9: 1217. https://doi.org/10.3390/biomedicines9091217