Talin: A Potential Drug Target for Cancer Therapy

Author(s): Rama Rao Malla, Rahul Kumar Vempati*

Journal Name: Current Drug Metabolism

Volume 21 , Issue 1 , 2020

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Graphical Abstract:


Talin is an intracellular cytoskeletal protein and one of the major components of the focal adhesion complex. It mainly acts as an interlink between transmembrane integrin receptors and cytosolic F-actin. Apart from integrins and actin, it also interacts with various other proteins in the adhesion complex to regulate their functional dynamics. Talin undergoes a variety of post-translational modifications and they are implicated in the control of cell motility. There are two talin isoforms (talin1 and talin2) in mammals and they are encoded by TLN1 and TLN2 genes, respectively. Recent studies showed that both the isoforms have some mechanistic dissimilarities in terms of their interaction with membrane-bound integrins. Among the two isoforms, talin1 was well studied, and most of the information available till now comes from talin1. The present review is aimed to provide an updated overview on the cellular significance of talin in normal and cancerous cells.

Keywords: Cancer, extra cellular matrix, focal adhesions, post translational modifications, talin, knock out.

Friedl, P.; Wolf, K. Tumour-cell invasion and migration: diversity and escape mechanisms. Nat. Rev. Cancer, 2003, 3(5), 362-374.
[http://dx.doi.org/10.1038/nrc1075] [PMID: 12724734]
Stuelten, C.H.; Parent, C.A.; Montell, D.J. Cell motility in cancer invasion and metastasis: insights from simple model organisms. Nat. Rev. Cancer, 2018, 18(5), 296-312.
[http://dx.doi.org/10.1038/nrc.2018.15] [PMID: 29546880]
Yilmaz, M.; Christofori, G. Mechanisms of motility in metastasizing cells. Mol. Cancer Res., 2010, 8(5), 629-642.
[http://dx.doi.org/10.1158/1541-7786.MCR-10-0139] [PMID: 20460404]
Wu, C. Focal adhesion: a focal point in current cell biology and molecular medicine. Cell Adhes. Migr., 2007, 1(1), 13-18.
[http://dx.doi.org/10.4161/cam.4081] [PMID: 19262093]
Kim, D.H.; Wirtz, D. Predicting how cells spread and migrate: focal adhesion size does matter. Cell Adhes. Migr., 2013, 7(3), 293-296.
[http://dx.doi.org/10.4161/cam.24804] [PMID: 23628962]
Pelham, R.J., Jr; Wang, Yl. Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc. Natl. Acad. Sci. USA, 1997, 94(25), 13661-13665.
Webb, D.J.; Parsons, J.T.; Horwitz, A.F. Adhesion assembly, disassembly and turnover in migrating cells -- over and over and over again. Nat. Cell Biol., 2002, 4(4), E97-E100.
[http://dx.doi.org/10.1038/ncb0402-e97] [PMID: 11944043]
Nagano, M.; Hoshino, D.; Koshikawa, N.; Akizawa, T.; Seiki, M. Turnover of focal adhesions and cancer cell migration. Int. J. Cell Biol., 2012, 2012310616
[http://dx.doi.org/10.1155/2012/310616] [PMID: 22319531]
Liang, E.I.; Mah, E.J.; Yee, A.F.; Digman, M.A. Correlation of focal adhesion assembly and disassembly with cell migration on nanotopography. Integr. Biol., 2017, 9(2), 145-155.
[http://dx.doi.org/10.1039/C6IB00193A] [PMID: 28092391]
Yan, J.; Yao, M.; Goult, B.T.; Sheetz, M.P. Talin dependent mechanosensitivity of cell focal adhesions. Cell. Mol. Bioeng., 2015, 8(1), 151-159.
[http://dx.doi.org/10.1007/s12195-014-0364-5] [PMID: 26097520]
Klapholz, B.; Brown, N.H. Talin - the master of integrin adhesions. J. Cell Sci., 2017, 130(15), 2435-2446.
[http://dx.doi.org/10.1242/jcs.190991] [PMID: 28701514]
Priddle, H.; Hemmings, L.; Monkley, S.; Woods, A.; Patel, B.; Sutton, D.; Dunn, G.A.; Zicha, D.; Critchley, D.R. Disruption of the talin gene compromises focal adhesion assembly in undifferentiated but not differentiated embryonic stem cells. J. Cell Biol., 1998, 142(4), 1121-1133.
[http://dx.doi.org/10.1083/jcb.142.4.1121] [PMID: 9722622]
Molony, L.; McCaslin, D.; Abernethy, J.; Paschal, B.; Burridge, K. Properties of talin from chicken gizzard smooth muscle. J. Biol. Chem., 1987, 262(16), 7790-7795.
[PMID: 3108258]
Burridge, K.; Connell, L. A new protein of adhesion plaques and ruffling membranes. J. Cell Biol., 1983, 97(2), 359-367.
[http://dx.doi.org/10.1083/jcb.97.2.359] [PMID: 6684120]
Critchley, D.R.; Gingras, A.R. Talin at a glance. J. Cell Sci., 2008, 121(Pt 9), 1345-1347.
[http://dx.doi.org/10.1242/jcs.018085] [PMID: 18434644]
Critchley, D.R. Biochemical and structural properties of the integrin-associated cytoskeletal protein talin. Annu. Rev. Biophys., 2009, 38, 235-254.
[http://dx.doi.org/10.1146/annurev.biophys.050708.133744] [PMID: 19416068]
Calderwood, D.A.; Zent, R.; Grant, R.; Rees, D.J.; Hynes, R.O.; Ginsberg, M.H. The Talin head domain binds to integrin beta subunit cytoplasmic tails and regulates integrin activation. J. Biol. Chem., 1999, 274(40), 28071-28074.
[http://dx.doi.org/10.1074/jbc.274.40.28071] [PMID: 10497155]
Rahikainen, R.; Öhman, T.; Turkki, P.; Varjosalo, M.; Hytönen, V.P. Talin-mediated force transmission and talin rod domain unfolding independently regulate adhesion signaling. J. Cell Sci., 2019, 132(7)jcs226514
[http://dx.doi.org/10.1242/jcs.226514] [PMID: 30837291]
Haining, A.W.; von Essen, M.; Attwood, S.J.; Hytönen, V.P.; Del Río Hernández, A. All subdomains of the talin rod are mechanically vulnerable and may contribute to cellular mechanosensing. ACS Nano, 2016, 10(7), 6648-6658.
[http://dx.doi.org/10.1021/acsnano.6b01658] [PMID: 27380548]
Hytönen, V.P.; Vogel, V. How force might activate talin’s vinculin binding sites: SMD reveals a structural mechanism. PLOS Comput. Biol., 2008, 4(2)e24
[http://dx.doi.org/10.1371/journal.pcbi.0040024] [PMID: 18282082]
Yao, M.; Goult, B.T.; Chen, H.; Cong, P.; Sheetz, M.P.; Yan, J. Mechanical activation of vinculin binding to talin locks talin in an unfolded conformation. Sci. Rep., 2014, 4, 4610.
[http://dx.doi.org/10.1038/srep04610] [PMID: 24714394]
Atherton, P.; Stutchbury, B.; Wang, D.Y.; Jethwa, D.; Tsang, R.; Meiler-Rodriguez, E.; Wang, P.; Bate, N.; Zent, R.; Barsukov, I.L.; Goult, B.T.; Critchley, D.R.; Ballestrem, C. Vinculin controls talin engagement with the actomyosin machinery. Nat. Commun., 2015, 6, 10038.
[http://dx.doi.org/10.1038/ncomms10038] [PMID: 26634421]
Humphries, J.D.; Wang, P.; Streuli, C.; Geiger, B.; Humphries, M.J.; Ballestrem, C. Vinculin controls focal adhesion formation by direct interactions with talin and actin. J. Cell Biol., 2007, 179(5), 1043-1057.
[http://dx.doi.org/10.1083/jcb.200703036] [PMID: 18056416]
Gingras, A.R.; Bate, N.; Goult, B.T.; Hazelwood, L.; Canestrelli, I.; Grossmann, J.G.; Liu, H.; Putz, N.S.; Roberts, G.C.; Volkmann, N.; Hanein, D.; Barsukov, I.L.; Critchley, D.R. The structure of the C-terminal actin-binding domain of talin. EMBO J., 2008, 27(2), 458-469.
[http://dx.doi.org/10.1038/sj.emboj.7601965] [PMID: 18157087]
Gough, R.E.; Goult, B.T. The tale of two talins - two isoforms to fine-tune integrin signalling. FEBS Lett., 2018, 592(12), 2108-2125.
[http://dx.doi.org/10.1002/1873-3468.13081] [PMID: 29723415]
Lee, H.S.; Lim, C.J.; Puzon-McLaughlin, W.; Shattil, S.J.; Ginsberg, M.H. RIAM activates integrins by linking talin to ras GTPase membrane-targeting sequences. J. Biol. Chem., 2009, 284(8), 5119-5127.
[http://dx.doi.org/10.1074/jbc.M807117200] [PMID: 19098287]
Kalli, A.C.; Campbell, I.D.; Sansom, M.S. Conformational changes in talin on binding to anionic phospholipid membranes facilitate signaling by integrin transmembrane helices. PLOS Comput. Biol., 2013, 9(10), e1003316
[http://dx.doi.org/10.1371/journal.pcbi.1003316] [PMID: 24204243]
Chinthalapudi, K.; Rangarajan, E.S.; Izard, T. The interaction of talin with the cell membrane is essential for integrin activation and focal adhesion formation. Proc. Natl. Acad. Sci. USA, 2018, 115(41), 10339-10344.
[http://dx.doi.org/10.1073/pnas.1806275115] [PMID: 30254158]
Wegener, K.L.; Partridge, A.W.; Han, J.; Pickford, A.R.; Liddington, R.C.; Ginsberg, M.H.; Campbell, I.D. Structural basis of integrin activation by talin. Cell, 2007, 128(1), 171-182.
[http://dx.doi.org/10.1016/j.cell.2006.10.048] [PMID: 17218263]
Calderwood, D.A.; Yan, B.; de Pereda, J.M.; Alvarez, B.G.; Fujioka, Y.; Liddington, R.C.; Ginsberg, M.H. The phosphotyrosine binding-like domain of talin activates integrins. J. Biol. Chem., 2002, 277(24), 21749-21758.
[http://dx.doi.org/10.1074/jbc.M111996200] [PMID: 11932255]
Calderwood, D.A. Talin controls integrin activation. Biochem. Soc. Trans., 2004, 32(Pt3), 434-437.
[http://dx.doi.org/10.1042/bst0320434] [PMID: 15157154]
Ratnikov, B.I.; Partridge, A.W.; Ginsberg, M.H. Integrin activation by talin. J. Thromb. Haemost., 2005, 3, 1783-1790.
Ellis, S.J.; Lostchuck, E.; Goult, B.T.; Bouaouina, M.; Fairchild, M.J.; López-Ceballos, P.; Calderwood, D.A.; Tanentzapf, G. The talin head domain reinforces integrin-mediated adhesion by promoting adhesion complex stability and clustering. PLoS Genet., 2014, 10(11)e1004756
[http://dx.doi.org/10.1371/journal.pgen.1004756] [PMID: 25393120]
Ellis, S.J.; Pines, M.; Fairchild, M.J.; Tanentzapf, G. In vivo functional analysis reveals specific roles for the integrin-binding sites of talin. J. Cell Sci., 2011, 124(Pt 11), 1844-1856.
[http://dx.doi.org/10.1242/jcs.083337] [PMID: 21558413]
de Pereda, J.M.; Wegener, K.L.; Santelli, E.; Bate, N.; Ginsberg, M.H.; Critchley, D.R.; Campbell, I.D.; Liddington, R.C. Structural basis for phosphatidylinositol phosphate kinase type Igamma binding to talin at focal adhesions. J. Biol. Chem., 2005, 280(9), 8381-8386.
[http://dx.doi.org/10.1074/jbc.M413180200] [PMID: 15623515]
Ye, X.; McLean, M.A.; Sligar, S.G. Phosphatidylinositol 4,5-bisphosphate modulates the affinity of talin-1 for phospholipid bilayers and activates its autoinhibited form. Biochemistry, 2016, 55(36), 5038-5048.
[http://dx.doi.org/10.1021/acs.biochem.6b00497] [PMID: 27548281]
Lee, S.Y.; Voronov, S.; Letinic, K.; Nairn, A.C.; Di Paolo, G.; De Camilli, P. Regulation of the interaction between PIPKI gamma and talin by proline-directed protein kinases. J. Cell Biol., 2005, 168(5), 789-799.
[http://dx.doi.org/10.1083/jcb.200409028] [PMID: 15738269]
Ling, K.; Doughman, R.L.; Iyer, V.V.; Firestone, A.J.; Bairstow, S.F.; Mosher, D.F.; Schaller, M.D.; Anderson, R.A. Tyrosine phosphorylation of type Igamma phosphatidylinositol phosphate kinase by Src regulates an integrin-talin switch. J. Cell Biol., 2003, 163(6), 1339-1349.
[http://dx.doi.org/10.1083/jcb.200310067] [PMID: 14691141]
Le, O.T.; Cho, O.Y.; Tran, M.H.; Kim, J.A.; Chang, S.; Jou, I.; Lee, S.Y. Phosphorylation of phosphatidylinositol 4-phosphate 5-kinase γ by Akt regulates its interaction with talin and focal adhesion dynamics. Biochim. Biophys. Acta, 2015, 1853(10 Pt A), 2432-2443.
[http://dx.doi.org/10.1016/j.bbamcr.2015.07.001] [PMID: 26149501]
Li, X.; Zhou, Q.; Sunkara, M.; Kutys, M.L.; Wu, Z.; Rychahou, P.; Morris, A.J.; Zhu, H.; Evers, B.M.; Huang, C. Ubiquitylation of phosphatidylinositol 4-phosphate 5-kinase type I γ by HECTD1 regulates focal adhesion dynamics and cell migration. J. Cell Sci., 2013, 126(Pt 12), 2617-2628.
[http://dx.doi.org/10.1242/jcs.117044] [PMID: 23572508]
Jafari, N.; Zheng, Q.; Li, L.; Li, W.; Qi, L.; Xiao, J.; Gao, T.; Huang, C. p70S6K1 (S6K1)-mediated phosphorylation regulates phosphatidylinositol 4-phosphate 5-kinase type I γ degradation and cell invasion. J. Biol. Chem., 2016, 291(49), 25729-25741.
[http://dx.doi.org/10.1074/jbc.M116.742742] [PMID: 27780861]
Bouaouina, M.; Goult, B.T.; Huet-Calderwood, C.; Bate, N.; Brahme, N.N.; Barsukov, I.L.; Critchley, D.R.; Calderwood, D.A. A conserved lipid-binding loop in the kindlin FERM F1 domain is required for kindlin-mediated αIIbβ3 integrin coactivation. J. Biol. Chem., 2012, 287(10), 6979-6990.
[http://dx.doi.org/10.1074/jbc.M111.330845] [PMID: 22235127]
Yates, L.A.; Füzéry, A.K.; Bonet, R.; Campbell, I.D.; Gilbert, R.J. Biophysical analysis of Kindlin-3 reveals an elongated conformation and maps integrin binding to the membrane-distal β-subunit NPXY motif. J. Biol. Chem., 2012, 287(45), 37715-37731.
[http://dx.doi.org/10.1074/jbc.M112.415208] [PMID: 22989875]
Calderwood, D.A.; Campbell, I.D.; Critchley, D.R. Talins and kindlins: partners in integrin-mediated adhesion. Nat. Rev. Mol. Cell Biol., 2013, 14(8), 503-517.
[http://dx.doi.org/10.1038/nrm3624] [PMID: 23860236]
Kahner, B.N.; Kato, H.; Banno, A.; Ginsberg, M.H.; Shattil, S.J.; Ye, F. Kindlins, integrin activation and the regulation of talin recruitment to αIIbβ3. PLoS One, 2012, 7(3)e34056
[http://dx.doi.org/10.1371/journal.pone.0034056] [PMID: 22457811]
Theodosiou, M.; Widmaier, M.; Böttcher, R.T.; Rognoni, E.; Veelders, M.; Bharadwaj, M.; Lambacher, A.; Austen, K.; Müller, D.J.; Zent, R.; Fässler, R. Kindlin-2 cooperates with talin to activate integrins and induces cell spreading by directly binding paxillin. eLife, 2016., 5e10130
[http://dx.doi.org/10.7554/eLife.10130] [PMID: 26821125]
Yuan, Y.; Li, L.; Zhu, Y.; Qi, L.; Azizi, L.; Hytönen, V.P.; Zhan, C.G.; Huang, C. The molecular basis of talin2's high affinity toward β1-integrin. Sci. Rep., 2017, 7, 41989.
[http://dx.doi.org/10.1038/srep41989] [PMID: 28155884]
Yao, M.; Goult, B.T.; Klapholz, B.; Hu, X.; Toseland, C.P.; Guo, Y.; Cong, P.; Sheetz, M.P.; Yan, J. The mechanical response of talin. Nat. Commun., 2016, 7, 11966.
[http://dx.doi.org/10.1038/ncomms11966] [PMID: 27384267]
Mykuliak, V.V.; Haining, A.W.M.; von Essen, M.; Del Río Hernández, A.; Hytönen, V.P. Mechanical unfolding reveals stable 3-helix intermediates in talin and α-catenin. PLOS Comput. Biol., 2018, 14(4)e1006126
[http://dx.doi.org/10.1371/journal.pcbi.1006126] [PMID: 29698481]
Hirata, H.; Tatsumi, H.; Lim, C.T.; Sokabe, M. Force-dependent vinculin binding to talin in live cells: a crucial step in anchoring the actin cytoskeleton to focal adhesions. Am. J. Physiol. Cell Physiol., 2014, 306(6), C607-C620.
[http://dx.doi.org/10.1152/ajpcell.00122.2013] [PMID: 24452377]
Carisey, A.; Tsang, R.; Greiner, A.M.; Nijenhuis, N.; Heath, N.; Nazgiewicz, A.; Kemkemer, R.; Derby, B.; Spatz, J.; Ballestrem, C. Vinculin regulates the recruitment and release of core focal adhesion proteins in a force-dependent manner. Curr. Biol., 2013, 23(4), 271-281.
[http://dx.doi.org/10.1016/j.cub.2013.01.009] [PMID: 23375895]
DeClue, J.E.; Martin, G.S. Phosphorylation of talin at tyrosine in Rous sarcoma virus-transformed cells. Mol. Cell. Biol., 1987, 7(1), 371-378.
[http://dx.doi.org/10.1128/MCB.7.1.371] [PMID: 3031468]
Pasquale, E.B.; Maher, P.A.; Singer, S.J. Talin is phosphorylated on tyrosine in chicken embryo fibroblasts transformed by Rous sarcoma virus. Proc. Natl. Acad. Sci. USA, 1986, 83(15), 5507-5511.
[http://dx.doi.org/10.1073/pnas.83.15.5507] [PMID: 2426700]
Tidball, J.G.; Spencer, M.J. PDGF stimulation induces phosphorylation of talin and cytoskeletal reorganization in skeletal muscle. J. Cell Biol., 1993, 123(3), 627-635.
[http://dx.doi.org/10.1083/jcb.123.3.627] [PMID: 7693714]
Ratnikov, B.; Ptak, C.; Han, J.; Shabanowitz, J.; Hunt, D.F.; Ginsberg, M.H. Talin phosphorylation sites mapped by mass spectrometry. J. Cell Sci., 2005, 118(Pt 21), 4921-4923.
[http://dx.doi.org/10.1242/jcs.02682] [PMID: 16254238]
Jin, J.K.; Tien, P.C.; Cheng, C.J.; Song, J.H.; Huang, C.; Lin, S.H.; Gallick, G.E. Talin1 phosphorylation activates β1 integrins: a novel mechanism to promote prostate cancer bone metastasis. Oncogene, 2015, 34(14), 1811-1821.
[http://dx.doi.org/10.1038/onc.2014.116] [PMID: 24793790]
Huang, C.; Rajfur, Z.; Yousefi, N.; Chen, Z.; Jacobson, K.; Ginsberg, M.H. Talin phosphorylation by Cdk5 regulates Smurf1-mediated talin head ubiquitylation and cell migration. Nat. Cell Biol., 2009, 11(5), 624-630.
[http://dx.doi.org/10.1038/ncb1868] [PMID: 19363486]
Huang, Z.; Barker, D.; Gibbins, J.M.; Dash, P.R. Talin is a substrate for SUMOylation in migrating cancer cells. Exp. Cell Res., 2018, 370(2), 417-425.
[http://dx.doi.org/10.1016/j.yexcr.2018.07.005] [PMID: 30003879]
Gunawan, M.; Venkatesan, N.; Loh, J.T.; Wong, J.F.; Berger, H.; Neo, W.H.; Li, L.Y.; La Win, M.K.; Yau, Y.H.; Guo, T.; See, P.C.; Yamazaki, S.; Chin, K.C.; Gingras, A.R.; Shochat, S.G.; Ng, L.G.; Sze, S.K.; Ginhoux, F.; Su, I.H. The methyltransferase Ezh2 controls cell adhesion and migration through direct methylation of the extranuclear regulatory protein talin. Nat. Immunol., 2015, 16(5), 505-516.
[http://dx.doi.org/10.1038/ni.3125] [PMID: 25751747]
Slater, M.; Cooper, M.; Murphy, C.R. The cytoskeletal proteins alpha-actinin, Ezrin, and talin are De-expressed in endometriosis and endometrioid carcinoma compared with normal uterine epithelium. Appl. Immunohistochem. Mol. Morphol., 2007, 15(2), 170-174.
[http://dx.doi.org/10.1097/01.pai.0000194762.78889.26] [PMID: 17525629]
Xu, N.; Chen, H.J.; Chen, S.H.; Xue, X.Y.; Chen, H.; Zheng, Q.S.; Wei, Y.; Li, X.D.; Huang, J.B.; Cai, H.; Sun, X.L. Upregulation of Talin-1 expression associates with advanced pathological features and predicts lymph node metastases and biochemical recurrence of prostate cancer. Medicine (Baltimore), 2016, 95(29)e4326
[http://dx.doi.org/10.1097/MD.0000000000004326] [PMID: 27442684]
Jevnikar, Z.; Rojnik, M.; Jamnik, P.; Doljak, B.; Fonovic, U.P.; Kos, J. Cathepsin H mediates the processing of talin and regulates migration of prostate cancer cells. J. Biol. Chem., 2013, 288(4), 2201-2209.
[http://dx.doi.org/10.1074/jbc.M112.436394] [PMID: 23204516]
Bostanci, O.; Kemik, O.; Kemik, A.; Battal, M.; Demir, U.; Purisa, S.; Mihmanli, M. A novel screening test for colon cancer: Talin-1. Eur. Rev. Med. Pharmacol. Sci., 2014, 18(17), 2533-2537.
[PMID: 25268101]
Chen, P.; Lei, L.; Wang, J.; Zou, X.; Zhang, D.; Deng, L.; Wu, D. Downregulation of Talin1 promotes hepatocellular carcinoma progression through activation of the ERK1/2 pathway. Cancer Sci., 2017, 108(6), 1157-1168.
[http://dx.doi.org/10.1111/cas.13247] [PMID: 28375585]
Chen, P.; Zheng, X.; Zhou, Y.; Xu, Y.; Zhu, L.; Qian, Y. Talin-1 interaction network promotes hepatocellular carcinoma progression. Oncotarget, 2017, 8(8), 13003-13014.
[http://dx.doi.org/10.18632/oncotarget.14674] [PMID: 28099903]
Kanamori, H.; Kawakami, T.; Effendi, K.; Yamazaki, K.; Mori, T.; Ebinuma, H.; Masugi, Y.; Du, W.; Nagasaka, K.; Ogiwara, A.; Kyono, Y.; Tanabe, M.; Saito, H.; Hibi, T.; Sakamoto, M. Identification by differential tissue proteome analysis of talin-1 as a novel molecular marker of progression of hepatocellular carcinoma. Oncology, 2011, 80(5-6), 406-415.
[http://dx.doi.org/10.1159/000330734] [PMID: 21846996]
Fang, K.P.; Dai, W.; Ren, Y.H.; Xu, Y.C.; Zhang, S.M.; Qian, Y.B. Both Talin-1 and Talin-2 correlate with malignancy potential of the human hepatocellular carcinoma MHCC-97 L cell. BMC Cancer, 2016, 16, 45.
[http://dx.doi.org/10.1186/s12885-016-2076-9] [PMID: 26822056]
Liang, Y.; Chen, H.; Ji, L.; Du, J.; Xie, X.; Li, X.; Lou, Y. Talin2 regulates breast cancer cell migration and invasion by apoptosis. Oncol. Lett., 2018, 16(1), 285-293.
[http://dx.doi.org/10.3892/ol.2018.8641] [PMID: 29928413]
Li, L.; Li, X.; Qi, L.; Rychahou, P.; Jafari, N.; Huang, C. The role of talin2 in breast cancer tumorigenesis and metastasis. Oncotarget, 2017, 8(63), 106876-106887.
[http://dx.doi.org/10.18632/oncotarget.22449] [PMID: 29290996]
Wen, Z.; Liang, Y.; Deng, S.; Zou, L.; Xie, X.; Yang, J.; Wu, Y. Talin2 regulates invasion of human breast cancer MDA-MB-231 cells via alteration of the tumor microenvironment. Oncol. Lett., 2019, 17(6), 4835-4842.
[http://dx.doi.org/10.3892/ol.2019.10175] [PMID: 31186690]
Sen, S.; Ng, W.P.; Kumar, S. Contributions of talin-1 to glioma cell-matrix tensional homeostasis. J. R. Soc. Interface, 2012, 9(71), 1311-1317.
[http://dx.doi.org/10.1098/rsif.2011.0567] [PMID: 22158841]
Lai, M.T.; Hua, C.H.; Tsai, M.H.; Wan, L.; Lin, Y.J.; Chen, C.M.; Chiu, I.W.; Chan, C.; Tsai, F.J.; Jinn-Chyuan Sheu, J. Talin-1 overexpression defines high risk for aggressive oral squamous cell carcinoma and promotes cancer metastasis. J. Pathol., 2011, 224(3), 367-376.
[http://dx.doi.org/10.1002/path.2867] [PMID: 21547905]

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Year: 2020
Published on: 13 February, 2020
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DOI: 10.2174/1389200221666200214114018
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