1,122
Views
13
CrossRef citations to date
0
Altmetric
Research Papers

CD151 promotes α3β1 integrin-dependent organization of carcinoma cell junctions and restrains collective cell invasion

, , , , , & show all
Pages 1626-1640 | Received 19 Feb 2015, Accepted 12 Sep 2015, Published online: 30 Oct 2015

References

  • Bjerke MA, Dzamba BJ, Wang C, DeSimone DW. FAK is required for tension-dependent organization of collective cell movements in Xenopus mesendoderm. Dev Biol 2014; 394:340-56; PMID:25127991; http://dx.doi.org/10.1016/j.ydbio.2014.07.023
  • Cai D, Chen SC, Prasad M, He L, Wang X, Choesmel-Cadamuro V, Sawyer JK, Danuser G, Montell DJ. Mechanical feedback through E-cadherin promotes direction sensing during collective cell migration. Cell 2014; 157:1146-59; PMID:24855950; http://dx.doi.org/10.1016/j.cell.2014.03.045
  • Aman A, Piotrowski T. Cell-cell signaling interactions coordinate multiple cell behaviors that drive morphogenesis of the lateral line. Cell Adh Migr 2011; 5:499-508; PMID:22274715; http://dx.doi.org/10.4161/cam.5.6.19113
  • Arima S, Nishiyama K, Ko T, Arima Y, Hakozaki Y, Sugihara K, Koseki H, Uchijima Y, Kurihara Y, Kurihara H. Angiogenic morphogenesis driven by dynamic and heterogeneous collective endothelial cell movement. Development 2011; 138:4763-76; PMID:21965612; http://dx.doi.org/10.1242/dev.068023
  • Theveneau E, Mayor R. Neural crest delamination and migration: from epithelium-to-mesenchyme transition to collective cell migration. Dev Biol 2012; 366:34-54; PMID:22261150; http://dx.doi.org/10.1016/j.ydbio.2011.12.041
  • Einenkel J, Braumann U-D, Horn L-C, Kuska J-P, Höckel M. Three-D analysis of the invasion front in squamous cell carcinoma of the uterine cervix: histopathologic evidence for collective invasion per continuitatem. Anal Quant Cytol Histol 2007; 29:279-90; PMID:17987808
  • Patsialou A, Bravo-Cordero JJ, Wang Y, Entenberg D, Liu H, Clarke M, Condeelis JS. Intravital multiphoton imaging reveals multicellular streaming as a crucial component of in vivo cell migration in human breast tumors. Intravital 2013; 2:e25294; PMID:25013744; http://dx.doi.org/10.4161/intv.25294
  • Cheung KJ, Gabrielson E, Werb Z, Ewald AJ. Collective invasion in breast cancer requires a conserved basal epithelial program. Cell 2013; 155:1639-51; PMID:24332913; http://dx.doi.org/10.1016/j.cell.2013.11.029
  • Nguyen-Ngoc KV, Cheung KJ, Brenot A, Shamir ER, Gray RS, Hines WC, Yaswen P, Werb Z, Ewald AJ. ECM microenvironment regulates collective migration and local dissemination in normal and malignant mammary epithelium. Proc Natl Acad Sci USA 2012; 109:E2595-604; PMID:22923691; http://dx.doi.org/10.1073/pnas.1212834109
  • Friedl P, Locker J, Sahai E, Segall JE. Classifying collective cancer cell invasion. Nat Cell Biol 2012; 14:777-83; PMID:22854810; http://dx.doi.org/10.1038/ncb2548
  • Cheung KJ, Ewald AJ. Illuminating breast cancer invasion: diverse roles for cell-cell interactions. Curr Opin Cell Biol 2014; 30C:99-111; ; http://dx.doi.org/10.1016/j.ceb.2014.07.003
  • Macpherson IR, Hooper S, Serrels A, McGarry L, Ozanne BW, Harrington K, Frame MC, Sahai E, Brunton VG. p120-catenin is required for the collective invasion of squamous cell carcinoma cells via a phosphorylation-independent mechanism. Oncogene 2007; 26:5214-28; PMID:17334396; http://dx.doi.org/10.1038/sj.onc.1210334
  • Canel M, Serrels A, Miller D, Timpson P, Serrels B, Frame MC, Brunton VG. Quantitative in vivo imaging of the effects of inhibiting integrin signaling via Src and FAK on cancer cell movement: effects on E-cadherin dynamics. Cancer Res 2010; 70:9413-22; PMID:21045155; http://dx.doi.org/10.1158/0008-5472.CAN-10-1454
  • Ng MR, Besser A, Danuser G, Brugge JS. Substrate stiffness regulates cadherin-dependent collective migration through myosin-II contractility. J Cell Biol 2012; 199:545-63; PMID:23091067; http://dx.doi.org/10.1083/jcb.201207148
  • Martinez-Rico C, Pincet F, Thiery JP, Dufour S. Integrins stimulate E-cadherin-mediated intercellular adhesion by regulating Src-kinase activation and actomyosin contractility. J Cell Sci 2010; 123:712-22; PMID:20144995; http://dx.doi.org/10.1242/jcs.047878
  • Pirraglia C, Walters J, Ahn N, Myat MM. Rac1 GTPase acts downstream of αPS1βPS integrin to control collective migration and lumen size in the Drosophila salivary gland. Dev Biol 2013; 377:21-32; PMID:23500171; http://dx.doi.org/10.1016/j.ydbio.2013.02.020
  • Canel M, Serrels A, Frame MC, Brunton VG. E-cadherin-integrin crosstalk in cancer invasion and metastasis. J Cell Sci 2013; 126:393-401; PMID:23525005; http://dx.doi.org/10.1242/jcs.100115
  • Stipp CS. Laminin-binding integrins and their tetraspanin partners as potential antimetastatic targets. Expert Rev Mol Med 2010; 12:e3; PMID:20078909; http://dx.doi.org/10.1017/S1462399409001355
  • Romanska HM, Berditchevski F. Tetraspanins in human epithelial malignancies. J Pathol 2011; 223:4-14; PMID:20938929; http://dx.doi.org/10.1002/path.2779
  • Charrin S, Jouannet S, Boucheix C, Rubinstein E. Tetraspanins at a glance. J Cell Sci 2014; 127:3641-8; PMID:25128561; http://dx.doi.org/10.1242/jcs.154906
  • Hemler ME. Tetraspanin proteins promote multiple cancer stages. Nat Rev Cancer 2014; 14:49-60; PMID:24505619; http://dx.doi.org/10.1038/nrc3640
  • Wang HX, Li Q, Sharma C, Knoblich K, Hemler ME. Tetraspanin protein contributions to cancer. Biochem Soc Trans 2011; 39:547-52; PMID:21428937; http://dx.doi.org/10.1042/BST0390547
  • Zöller M. Tetraspanins: push and pull in suppressing and promoting metastasis. Nat Rev Cancer 2009; 9:40-55; PMID:19078974; http://dx.doi.org/10.1038/nrc2543
  • Sadej R, Grudowska A, Turczyk L, Kordek R, Romanska HM. CD151 in cancer progression and metastasis: a complex scenario. Lab Invest 2013; 94(1):41-51; PMID:24247563
  • Roselli S, Kahl RGS, Copeland BT, Naylor MJ, Weidenhofer J, Muller WJ, Ashman LK. Deletion of Cd151 reduces mammary tumorigenesis in the MMTV/PyMT mouse model. BMC Cancer 2014; 14:509; PMID:25012362; http://dx.doi.org/10.1186/1471-2407-14-509
  • Deng X, Li Q, Hoff J, Novak M, Yang H, Jin H, Erfani SF, Sharma C, Zhou P, Rabinovitz I, et al. Integrin-Associated CD151 Drives ErbB2-Evoked Mammary Tumor Onset and Metastasis. Neoplasia 2012; 14:678-89; PMID:22952421; http://dx.doi.org/10.1593/neo.12922
  • Sadej R, Romanska H, Kavanagh D, Baldwin G, Takahashi T, Kalia N, Berditchevski F. Tetraspanin CD151 regulates transforming growth factor β signaling: implication in tumor metastasis. Cancer Res 2010; 70:6059-70; PMID:20570898; http://dx.doi.org/10.1158/0008-5472.CAN-09-3497
  • Sadej R, Romanska H, Baldwin G, Gkirtzimanaki K, Novitskaya V, Filer AD, Krcova Z, Kusinska R, Ehrmann J, Buckley CD, et al. CD151 regulates tumorigenesis by modulating the communication between tumor cells and endothelium. Mol Cancer Res 2009; 7:787-98; PMID:19531562; http://dx.doi.org/10.1158/1541-7786.MCR-08-0574
  • Yang XH, Richardson AL, Torres-Arzayus MI, Zhou P, Sharma C, Kazarov AR, Andzelm MM, Strominger JL, Brown M, Hemler ME. CD151 accelerates breast cancer by regulating α 6 integrin function, signaling, and molecular organization. Cancer Res 2008; 68:3204-13; PMID:18451146; http://dx.doi.org/10.1158/0008-5472.CAN-07-2949
  • Li Q, Yang XH, Xu F, Sharma C, Wang HX, Knoblich K, Rabinovitz I, Granter SR, Hemler ME. Tetraspanin CD151 plays a key role in skin squamous cell carcinoma. Oncogene 2012; 32(14):1772-83
  • Copeland BT, Bowman MJ, Ashman LK. Genetic ablation of the tetraspanin CD151 reduces spontaneous metastatic spread of prostate cancer in the TRAMP model. Mol Cancer Res 2013; 11:95-105; PMID:23131993; http://dx.doi.org/10.1158/1541-7786.MCR-12-0468
  • Yue S, Mu W, Zöller M. Tspan8 and CD151 promote metastasis by distinct mechanisms. Eur J Cancer 2013; 49:2934-48; PMID:23683890; http://dx.doi.org/10.1016/j.ejca.2013.03.032
  • Novitskaya V, Romanska H, Kordek R, Potemski P, Kusińska R, Parsons M, Odintsova E, Berditchevski F. Integrin α3β1-CD151 complex regulates dimerization of ErbB2 via RhoA. Oncogene 2013; 33(21):2779-89; PMID:23792450
  • Palmer TD, Martinez CH, Vasquez C, Hebron K, Jones-Paris C, Arnold SA, Chan SM, Chalasani V, Gomez-Lemus JA, Williams AK, et al. Integrin-free tetraspanin CD151 can inhibit tumor cell motility upon clustering and is a clinical indicator of prostate cancer progression. Cancer Res 2013; 74(1):173-87
  • Baldwin LA, Hoff JT, Lefringhouse J, Zhang M, Jia C, Liu Z, Erfani S, Jin H, Xu M, She QB, et al. CD151-α3β1 integrin complexes suppress ovarian tumor growth by repressing slug-mediated EMT and canonical wnt signaling. Oncotarget 2014; 5(23):12203-17; PMID:25356755
  • Voss MA, Gordon N, Maloney S, Ganesan R, Ludeman L, McCarthy K, Gornall R, Schaller G, Wei W, Berditchevski F, et al. Tetraspanin CD151 is a novel prognostic marker in poor outcome endometrial cancer. Br J Cancer 2011; 104:1611-8; PMID:21505452; http://dx.doi.org/10.1038/bjc.2011.80
  • Romanska HM, Potemski P, Collins SI, Williams H, Parmar S, Berditchevski F. Loss of CD151/Tspan24 from the complex with integrin α3β1 in invasive front of the tumour is a negative predictor of disease-free survival in oral squamous cell carcinoma. Oral Oncol 2013; 49:224-9; PMID:23099281; http://dx.doi.org/10.1016/j.oraloncology.2012.09.013
  • Chien CW, Lin SC, Lai YY, Lin BW, Lin SC, Lee JC, Tsai SJ. Regulation of CD151 by hypoxia controls cell adhesion and metastasis in colorectal cancer. Clin Cancer Res 2008; 14:8043-51; PMID:19073968; http://dx.doi.org/10.1158/1078-0432.CCR-08-1651
  • Sawada S, Yoshimoto M, Odintsova E, Hotchin NA, Berditchevski F. The tetraspanin CD151 functions as a negative regulator in the adhesion-dependent activation of Ras. J Biol Chem 2003; 278:26323-6; PMID:12782641; http://dx.doi.org/10.1074/jbc.C300210200
  • Winterwood NE, Varzavand A, Meland MN, Ashman LK, Stipp CS. A critical role for tetraspanin CD151 in alpha3beta1 and alpha6beta4 integrin-dependent tumor cell functions on laminin-5. Mol Biol Cell 2006; 17:2707-21; PMID:16571677; http://dx.doi.org/10.1091/mbc.E05-11-1042
  • Zevian S, Winterwood NE, Stipp CS. Structure-function analysis of tetraspanin CD151 reveals distinct requirements for tumor cell behaviors mediated by α3β1 versus α6β4 integrin. J Biol Chem 2011; 286:7496-506; PMID:21193415; http://dx.doi.org/10.1074/jbc.M110.173583
  • Johnson JL, Winterwood N, DeMali KA, Stipp CS. Tetraspanin CD151 regulates RhoA activation and the dynamic stability of carcinoma cell-cell contacts. J Cell Sci 2009; 122:2263-73; PMID:19509057; http://dx.doi.org/10.1242/jcs.045997
  • Marinkovich MP, Verrando P, Keene DR, Meneguzzi G, Lunstrum GP, Ortonne JP, Burgeson RE. Basement membrane proteins kalinin and nicein are structurally and immunologically identical. Lab Invest 1993; 69:295-9; PMID:8377472
  • Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods 2012; 9:671-5; PMID:22930834; http://dx.doi.org/10.1038/nmeth.2089
  • Cerami E, Gao J, Dogrusoz U, Gross BE, Sumer SO, Aksoy BA, Jacobsen A, Byrne CJ, Heuer ML, Larsson E, et al. The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov 2012; 2:401-4; PMID:22588877; http://dx.doi.org/10.1158/2159-8290.CD-12-0095
  • Gao J, Aksoy BA, Dogrusoz U, Dresdner G, Gross B, Sumer SO, Sun Y, Jacobsen A, Sinha R, Larsson E, et al. Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci Signal 2013; 6:pl1
  • Cancer Genome Atlas Research Network. Comprehensive genomic characterization of squamous cell lung cancers. Nature 2012; 489:519-25; PMID:22960745; http://dx.doi.org/10.1038/nature11404
  • Eeckhoute J, Keeton EK, Lupien M, Krum SA, Carroll JS, Brown M. Positive cross-regulatory loop ties GATA-3 to estrogen receptor α expression in breast cancer. Cancer Res 2007; 67:6477-83; PMID:17616709; http://dx.doi.org/10.1158/0008-5472.CAN-07-0746
  • Győrffy B, Lánczky A, Eklund AC, Denkert C, Budczies J, Li Q, Szallasi Z. An online survival analysis tool to rapidly assess the effect of 22,277 genes on breast cancer prognosis using microarray data of 1,809 patients. Breast Cancer Res Treat 2010; 123:725-31; PMID:20020197; http://dx.doi.org/10.1007/s10549-009-0674-9
  • Shang M, Koshikawa N, Schenk S, Quaranta V. The LG3 module of laminin-5 harbors a binding site for integrin alpha3beta1 that promotes cell adhesion, spreading, and migration. J Biol Chem 2001; 276:33045-53; PMID:11395486; http://dx.doi.org/10.1074/jbc.M100798200
  • Falk DL, Wessels D, Jenkins L, Pham T, Kuhl S, Titus MA, Soll DR. Shared, unique and redundant functions of three members of the class I myosins (MyoA, MyoB and MyoF) in motility and chemotaxis in Dictyostelium. J Cell Sci 2003; 116:3985-99; PMID:12953059; http://dx.doi.org/10.1242/jcs.00696
  • Lee SH, Oh SY, Do SI, Lee HJ, Kang HJ, Rho YS, Bae WJ, Lim YC. SOX2 regulates self-renewal and tumorigenicity of stem-like cells of head and neck squamous cell carcinoma. Br J Cancer 2014; 111:2122-30; PMID:25321191; http://dx.doi.org/10.1038/bjc.2014.528
  • Chen C, Wei Y, Hummel M, Hoffmann TK, Gross M, Kaufmann AM, Albers AE. Evidence for epithelial-mesenchymal transition in cancer stem cells of head and neck squamous cell carcinoma. PLoS One 2011; 6:e16466; PMID:21304586; http://dx.doi.org/10.1371/journal.pone.0016466
  • Ribeiro AS, Paredes J. P-Cadherin Linking Breast Cancer Stem Cells and Invasion: A promising marker to Identify an “Intermediate/Metastable” EMT State. Front Oncol 2014; 4:371; PMID:25601904; http://dx.doi.org/10.3389/fonc.2014.00045
  • Shigeta M, Sanzen N, Ozawa M, Gu J, Hasegawa H, Sekiguchi K. CD151 regulates epithelial cell-cell adhesion through PKC- and Cdc42-dependent actin cytoskeletal reorganization. J Cell Biol 2003; 163:165-76; PMID:14557253; http://dx.doi.org/10.1083/jcb.200301075
  • Chometon G, Zhang ZG, Rubinstein E, Boucheix C, Mauch C, Aumailley M. Dissociation of the complex between CD151 and laminin-binding integrins permits migration of epithelial cells. Exp Cell Res 2006; 312:983-95; PMID:16490193; http://dx.doi.org/10.1016/j.yexcr.2005.12.034
  • Zhang F, Michaelson JE, Moshiach S, Sachs N, Zhao W, Sun Y, Sonnenberg A, Lahti JM, Huang H, Zhang XA. Tetraspanin CD151 maintains vascular stability by balancing the forces of cell adhesion and cytoskeletal tension. Blood 2011; 118:4274-84; PMID:21832275; http://dx.doi.org/10.1182/blood-2011-03-339531
  • Chattopadhyay N, Wang Z, Ashman LK, Brady-Kalnay SM, Kreidberg JA. alpha3beta1 integrin-CD151, a component of the cadherin-catenin complex, regulates PTPmu expression and cell-cell adhesion. J Cell Biol 2003; 163:1351-62; PMID:14691142; http://dx.doi.org/10.1083/jcb.200306067
  • Kim KK, Wei Y, Szekeres C, Kugler MC, Wolters PJ, Hill ML, Frank JA, Brumwell AN, Wheeler SE, Kreidberg JA, et al. Epithelial cell alpha3beta1 integrin links β-catenin and Smad signaling to promote myofibroblast formation and pulmonary fibrosis. J Clin Invest 2009; 119:213-24; PMID:19104148
  • Kim Y, Kugler MC, Wei Y, Kim KK, Li X, Brumwell AN, Chapman HA. Integrin alpha3beta1-dependent β-catenin phosphorylation links epithelial Smad signaling to cell contacts. J Cell Biol 2009; 184:309-22; PMID:19171760; http://dx.doi.org/10.1083/jcb.200806067
  • Raymond K, Cagnet S, Kreft M, Janssen H, Sonnenberg A, Glukhova MA. Control of mammary myoepithelial cell contractile function by α3β1 integrin signalling. EMBO J 2011; 30:1896-906; PMID:21487391; http://dx.doi.org/10.1038/emboj.2011.113
  • Kerrisk ME, Greer CA, Koleske AJ. Integrin α3 is required for late postnatal stability of dendrite arbors, dendritic spines and synapses, and mouse behavior. J Neurosci 2013; 33:6742-52; PMID:23595732; http://dx.doi.org/10.1523/JNEUROSCI.0528-13.2013
  • Palecek SP, Loftus JC, Ginsberg MH, Lauffenburger DA, Horwitz AF. Integrin-ligand binding properties govern cell migration speed through cell-substratum adhesiveness. Nature 1997; 385:537-40; PMID:9020360; http://dx.doi.org/10.1038/385537a0
  • Zaman MH, Trapani LM, Sieminski AL, Siemeski A, Mackellar D, Gong H, Kamm RD, Wells A, Lauffenburger DA, Matsudaira P. Migration of tumor cells in 3D matrices is governed by matrix stiffness along with cell-matrix adhesion and proteolysis. Proc Natl Acad Sci USA 2006; 103:10889-94; PMID:16832052; http://dx.doi.org/10.1073/pnas.0604460103
  • Friedl P, Alexander S. Cancer invasion and the microenvironment: plasticity and reciprocity. Cell 2011; 147:992-1009; PMID:22118458; http://dx.doi.org/10.1016/j.cell.2011.11.016
  • Yang XH, Flores LM, Li Q, Zhou P, Xu F, Krop IE, Hemler ME. Disruption of laminin-integrin-CD151-focal adhesion kinase axis sensitizes breast cancer cells to ErbB2 antagonists. Cancer Res 2010; 70:2256-63; PMID:20197472; http://dx.doi.org/10.1158/0008-5472.CAN-09-4032
  • Kaplan-Lefko PJ, Chen TM, Ittmann MM, Barrios RJ, Ayala GE, Huss WJ, Maddison LA, Foster BA, Greenberg NM. Pathobiology of autochthonous prostate cancer in a pre-clinical transgenic mouse model. Prostate 2003; 55:219-37; PMID:12692788; http://dx.doi.org/10.1002/pros.10215
  • Sarrió D, Rodriguez-Pinilla SM, Hardisson D, Cano A, Moreno-Bueno G, Palacios J. Epithelial-mesenchymal transition in breast cancer relates to the basal-like phenotype. Cancer Res 2008; 68:989-97; http://dx.doi.org/10.1158/0008-5472.CAN-07-2017
  • Giordano A, Gao H, Anfossi S, Cohen E, Mego M, Lee BN, Tin S, De Laurentiis M, Parker CA, Alvarez RH, et al. Epithelial-mesenchymal transition and stem cell markers in patients with HER2-positive metastatic breast cancer. Mol Cancer Ther 2012; 11:2526-34; PMID:22973057; http://dx.doi.org/10.1158/1535-7163.MCT-12-0460
  • Chung SS, Giehl N, Wu Y, Vadgama JV. STAT3 activation in HER2-overexpressing breast cancer promotes epithelial-mesenchymal transition and cancer stem cell traits. Int J Oncol 2014; 44:403-11; PMID:24297508
  • Yan W, Cao QJ, Arenas RB, Bentley B, Shao R. GATA3 inhibits breast cancer metastasis through the reversal of epithelial-mesenchymal transition. J Biol Chem 2010; 285:14042-51; PMID:20189993; http://dx.doi.org/10.1074/jbc.M110.105262
  • Sachs N, Claessen N, Aten J, Kreft M, Teske GJD, Koeman A, Zuurbier CJ, Janssen H, Sonnenberg A. Blood pressure influences end-stage renal disease of Cd151 knockout mice. J Clin Invest 2012; 122:348-58; PMID:22201679; http://dx.doi.org/10.1172/JCI58878
  • Sachs N, Kreft M, van den Bergh Weerman MA, Beynon AJ, Peters TA, Weening JJ, Sonnenberg A. Kidney failure in mice lacking the tetraspanin CD151. J Cell Biol 2006; 175:33-9; PMID:17015618; http://dx.doi.org/10.1083/jcb.200603073
  • Baleato RM, Guthrie PL, Gubler MC, Ashman LK, Roselli S. Deletion of CD151 results in a strain-dependent glomerular disease due to severe alterations of the glomerular basement membrane. Am J Pathol 2008; 173:927-37; PMID:18787104; http://dx.doi.org/10.2353/ajpath.2008.071149
  • Tsujino K, Takeda Y, Arai T, Shintani Y, Inagaki R, Saiga H, Iwasaki T, Tetsumoto S, Jin Y, Ihara S, et al. Tetraspanin CD151 Protects against Pulmonary Fibrosis by maintaining epithelial integrity. Am J Respir Crit Care Med 2012; 186:170-80; PMID:22592804; http://dx.doi.org/10.1164/rccm.201201-0117OC
  • Marusyk A, Almendro V, Polyak K. Intra-tumour heterogeneity: a looking glass for cancer? Nat Rev Cancer 2012; 12:323-34; PMID:22513401; http://dx.doi.org/10.1038/nrc3261

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.