Integrin α-3 ß-1’s central role in breast cancer, melanoma and glioblastoma cell aggregation revealed by antibodies with blocking activity

References

• Scherer A, Kuhl S, Wessels D, Lusche DF, Hanson B, Ambrose J, Voss, E., Fletcher, E., Goldman, C., Soll, D. R., et al. A computer-assisted 3D model for analyzing the aggregation of tumorigenic cells reveals specialized behaviors and unique cell types that facilitate aggregate coalescence. PLoS One. 2015;10:e0118628. doi:10.1371/journal.pone.0118628.
   PubMed Web of Science ®Google Scholar
• Ambrose J, Livitz M, Wessels D, Kuhl S, Lusche DF, Scherer A, Voss E, Soll DR. Mediated coalescence: a possible mechanism for tumor cellular heterogeneity. Am J Cancer Res. 2015;5:3485–504.
   PubMed Web of Science ®Google Scholar
• Wessels D, Lusche DF, Voss E, Kuhl S, Buchele EC, Klemme MR, Russell KB, Ambrose J, Soll BA, Bossler A, et al. Melanoma cells undergo aggressive coalescence in a 3D Matrigel model that is repressed by anti-CD44. PLoS One. 2017;12:e0173400. doi:10.1371/journal.pone.0173400.
   PubMed Web of Science ®Google Scholar
• Weaver VM, Petersen OW, Wang F, Larabell CA, Briand P, Damsky C, Bissell MJ. Reversion of the malignant phenotype of human breast cells in three-dimensional culture and in vivo by integrin blocking antibodies. J Cell Biol. 1997;137:231–45.
   PubMed Web of Science ®Google Scholar
• Mukhopadhyay R, Theriault RL, Price JE. Increased levels of alpha6 integrins are associated with the metastatic phenotype of human breast cancer cells. Clin Exp Mets. 1999;17:325–32.
   PubMed Web of Science ®Google Scholar
• Gehlsen KR, Dillner L, Engvall E, Ruoslahti E. The human laminin receptor is a member of the integrin family of cell adhesion receptors. Science. 1988;241:1228–29.
   PubMed Web of Science ®Google Scholar
• Chen WT, Hasegawa E, Hasegawa T, Weinstock C, Yamada KM. Development of cell surface linkage complexes in cultured fibroblasts. J Cell Biol. 1985;100:1103–14.
   PubMed Web of Science ®Google Scholar
• Horwitz A, Duggan K, Greggs R, Decker C, Buck C. The cell substrate attachment (CSAT) antigen has properties of a receptor for laminin and fibronectin. J Cell Biol. 1985;101:2134–44.
   PubMed Web of Science ®Google Scholar
• Pytela R, Pierschbacher MD, Ruoslahti E. Identification and isolation of a 140 kd cell surface glycoprotein with properties expected of a fibronectin receptor. Cell. 1985;40:191–98.
   PubMed Web of Science ®Google Scholar
• Wayner EA, Carter WG. Identification of multiple cell adhesion receptors for collagen and fibronectin in human fibrosarcoma cells possessing unique alpha and common beta subunits. J Cell Biol. 1987;105:1873–84.
   PubMed Web of Science ®Google Scholar
• Carter WG, Wayner EA, Bouchard TS, Kaur P. The role of integrins alpha 2 beta 1 and alpha 3 beta 1 in cell-cell and cell-substrate adhesion of human epidermal cells. J Cell Biol. 1990;110:1387–404.
   PubMed Web of Science ®Google Scholar
• Hall DE, Reichardt LF, Crowley E, Holley B, Moezzi H, Sonnenberg A, Damsky CH. The alpha 1/beta 1 and alpha 6/beta 1 integrin heterodimers mediate cell attachment to distinct sites on laminin. J Cell Biol. 1990;110:2175–84.
   PubMed Web of Science ®Google Scholar
• Dedhar S, Jewell K, Rojiani M, Gray V. The receptor for the basement membrane glycoprotein entactin is the integrin alpha 3/beta 1. J Biol Chem. 1992;267:18908–14.
   PubMed Web of Science ®Google Scholar
• Gehlsen KR, Sriramarao P, Furcht LT, Skubitz AP. A synthetic peptide derived from the carboxy terminus of the laminin A chain represents a binding site for the alpha 3 beta 1 integrin. J Cell Biol. 1992;117:449–59.
   PubMed Web of Science ®Google Scholar
• DeFreitas MF, Yoshida CK, Frazier WA, Mendrick DL, Kypta RM, Reichardt LF. Identification of integrin alpha 3 beta 1 as a neuronal thrombospondin receptor mediating neurite outgrowth. Neuron. 1995;15:333–43.
   PubMed Web of Science ®Google Scholar
• Wu C, Chung AE, McDonald JA. A novel role for alpha 3 beta 1 integrins in extracellular matrix assembly. J Cell Sci. 1995;108:2511–23.
   PubMed Web of Science ®Google Scholar
• Fukushi J, Makagiansar IT, Stallcup WB. NG2 proteoglycan promotes endothelial cell motility and angiogenesis via engagement of galectin-3 and alpha3beta1 integrin. Mol Biol Cell. 2004;15:3580–90. doi:10.1091/mbc.e04-03-0236.
   PubMed Web of Science ®Google Scholar
• Tamkun JW, DeSimone DW, Fonda D, Patel RS, Buck C, Horwitz AF, Hynes RO. Structure of integrin, a glycoprotein involved in the transmembrane linkage between fibronectin and actin. Cell. 1986;46:271–82.
   PubMed Web of Science ®Google Scholar
• Yamaguchi A, Tanoue K, Yamazaki H. Secondary signals mediated by GPIIb/IIIa in thrombin-activated platelets. Biochim Biophys Acta. 1990;1054:8–13.
   PubMedGoogle Scholar
• Hughes PE, O’Toole TE, Ylanne J, Shattil SJ, Ginsberg MH. The conserved membrane-proximal region of an integrin cytoplasmic domain specifies ligand binding affinity. J Biol Chem. 1995;270:12411–17.
   PubMed Web of Science ®Google Scholar
• Kaufmann R, Frosch D, Westphal C, Weber L, Klein CE. Integrin VLA-3: ultrastructural localization at cell-cell contact sites of human cell cultures. J Cell Biol. 1989;109:1807–15.
   PubMed Web of Science ®Google Scholar
• Larjava H, Peltonen J, Akiyama SK, Yamada SS, Gralnick HR, Uitto J, Yamada KM. Novel function for beta 1 integrins in keratinocyte cell-cell interactions. J Cell Biol. 1990;110:803–15.
   PubMed Web of Science ®Google Scholar
• Nakamura K, Iwamoto R, Mekada E. Membrane-anchored heparin-binding EGF-like growth factor (HB-EGF) and diphtheria toxin receptor-associated protein (DRAP27)/CD9 form a complex with integrin alpha 3 beta 1 at cell-cell contact sites. J Cell Biol. 1995;129:1691–705.
   PubMed Web of Science ®Google Scholar
• Frolikova M, Sebkova N, Ded L, Dvorakova-Hortova K. Characterization of CD46 and beta1 integrin dynamics during sperm acrosome reaction. Sci Rep. 2016;6:33714. doi:10.1038/srep33714.
   PubMed Web of Science ®Google Scholar
• Gehlsen KR, Davis GE, Sriramarao P. Integrin expression in human melanoma cells with differing invasive and metastatic properties. Clin Exp Mets. 1992;10:111–20.
   PubMed Web of Science ®Google Scholar
• Sachs N, Secades P, van Hulst L, Kreft M, Song JY, Sonnenberg A. Loss of integrin alpha3 prevents skin tumor formation by promoting epidermal turnover and depletion of slow-cycling cells. Proc Natl Acad Sci USA. 2012;109:21468–73. doi:10.1073/pnas.1204614110.
   PubMed Web of Science ®Google Scholar
• Ganguly KK, Pal S, Moulik S, Chatterjee A. Integrins and metastasis. Cell Adh Migr. 2013;7:251–61. doi:10.4161/cam.23840.
   PubMed Web of Science ®Google Scholar
• Weber GF, Ashkar S, Glimcher MJ, Cantor H. Receptor-ligand interaction between CD44 and osteopontin (Eta-1). Science. 1996;271:509–12.
   PubMed Web of Science ®Google Scholar
• Naor D, Sionov RV, Ish-Shalom D. CD44: structure, function, and association with the malignant process. Adv Cancer Res. 1997;71:241–319.
   PubMed Web of Science ®Google Scholar
• Goodison S, Urquidi V, Tarin D. CD44 cell adhesion molecules. Mol Pathol. 1999;52:189–96.
   PubMedGoogle Scholar
• Piotrowicz RS, Damaj BB, Hachicha M, Incardona F, Howell SB, Finlayson M. A6 peptide activates CD44 adhesive activity, induces FAK and MEK phosphorylation, and inhibits the migration and metastasis of CD44-expressing cells. Mol Cancer Ther. 2011;10:2072–82. doi:10.1158/1535-7163.MCT-11-0351.
   PubMed Web of Science ®Google Scholar
• Senbanjo LT, Chellaiah MA. CD44: a multifunctional cell surface adhesion receptor is a regulator of progression and metastasis of cancer cells. Front Cell Dev Biol. 2017;5:18. doi:10.3389/fcell.2017.00018.
   PubMed Web of Science ®Google Scholar
• Katagiri YU, Sleeman J, Fujii H, Herrlich P, Hotta H, Tanaka K, Chikuma S, Yagita H, Okumura K, Murakami M, et al. CD44 variants but not CD44s cooperate with beta1-containing integrins to permit cells to bind to osteopontin independently of arginine-glycine-aspartic acid, thereby stimulating cell motility and chemotaxis. Cancer Res. 1999;59:219–26.
   PubMed Web of Science ®Google Scholar
• Kurtis MS, Tu BP, Gaya OA, Mollenhauer J, Knudson W, Loeser RF, Knudson CB, Sah RL. Mechanisms of chondrocyte adhesion to cartilage: role of beta1-integrins, CD44, and annexin V. J Orthop Res. 2001;19:1122–30. doi:10.1016/S0736-0266(01)00051-1.
   PubMed Web of Science ®Google Scholar
• Knudson W, Loeser RF. CD44 and integrin matrix receptors participate in cartilage homeostasis. Cell Mol Life Sci. 2002;59:36–44.
   PubMed Web of Science ®Google Scholar
• Kren A, Baeriswyl V, Lehembre F, Wunderlin C, Strittmatter K, Antoniadis H, Fässler R, Cavallaro U, Christofori G. Increased tumor cell dissemination and cellular senescence in the absence of beta1-integrin function. Embo J. 2007;26:2832–42. doi:10.1038/sj.emboj.7601738.
   PubMed Web of Science ®Google Scholar
• Lee JL, Wang MJ, Sudhir PR, Chen JY. CD44 engagement promotes matrix-derived survival through the CD44-SRC-integrin axis in lipid rafts. Mol Cell Biol. 2008;28:5710–23. doi:10.1128/MCB.00186-08.
   PubMed Web of Science ®Google Scholar
• Hughes CS, Postovit LM, Lajoie GA. Matrigel: a complex protein mixture required for optimal growth of cell culture. Proteomics. 2010;10:1886–90. doi:10.1002/pmic.200900758.
   PubMed Web of Science ®Google Scholar
• Soule HD, Maloney TM, Wolman SR, Peterson WD Jr., Brenz R, McGrath CM, Russo J, Pauley RJ, Jones RF, Brooks SC. Isolation and characterization of a spontaneously immortalized human breast epithelial cell line, MCF-10. Cancer Res. 1990;50:6075–86.
   PubMed Web of Science ®Google Scholar
• Clark MJ, Homer N, O’Connor BD, Chen Z, Eskin A, Lee H, Merriman B, Nelson SF, Horwitz MS. U87MG decoded: the genomic sequence of a cytogenetically aberrant human cancer cell line. PLoS Genet. 2010;6:e1000832. doi:10.1371/journal.pgen.1000832.
   PubMed Web of Science ®Google Scholar
• Takada Y, Puzon W. Identification of a regulatory region of integrin beta 1 subunit using activating and inhibiting antibodies. J Biol Chem. 1993;268:17597–601.
   PubMed Web of Science ®Google Scholar
• Belkin VM, Kozlova NI, Bychkova VV, Shekhonin BV. Beta 1 integrin subunit dimerization via disulfide bonds. Biochem Mol Biol Int. 1996;40:53–60.
   PubMedGoogle Scholar
• Goodpaster T, Randolph-Habecker J. A flexible mouse-on-mouse immunohistochemical staining technique adaptable to biotin-free reagents, immunofluorescence, and multiple antibody staining. J Histochem Cytochem. 2014;62:197–204. doi:10.1369/0022155413511620.
   PubMed Web of Science ®Google Scholar
• Lusche DF, Buchele EC, Russell KB, Soll BA, Vitolo MI, Klemme MR, Wessels DJ, Soll DR. Overexpressing TPTE2 (TPIP), a homolog of the human tumor suppressor gene PTEN, rescues the abnormal phenotype of the PTEN(-/-) mutant. Oncotarget. 2018;9:21100–21. doi:10.18632/oncotarget.24941.
   PubMedGoogle Scholar
• Slater TF, Sawyer B, Straeuli U. Studies on succinate-tetrazolium reductase systems. Iii. Points of coupling of four different tetrazolium salts. Biochim Biophys Acta. 1963;77:383–93.
   PubMed Web of Science ®Google Scholar
• Yazlovitskaya EM, Viquez OM, Tu T, De Arcangelis A, Georges-Labouesse E, Sonnenberg A, Pozzi A, Zent R. The laminin binding alpha3 and alpha6 integrins cooperate to promote epithelial cell adhesion and growth. Matrix Biol. 2018. doi:10.1016/j.matbio.2018.08.010.
   PubMed Web of Science ®Google Scholar
• Das L, Anderson TA, Gard JM, Sroka IC, Strautman SR, Nagle RB, Morrissey C, Knudsen BS, Cress AE. Characterization of laminin binding integrin internalization in prostate cancer cells. J Cell Biochem. 2017;118:1038–49. doi:10.1002/jcb.25673.
   PubMed Web of Science ®Google Scholar
• Wayner EA, Hoffstrom BG. Development of monoclonal antibodies to integrin receptors. Methods Enzymol. 2007;426:117–53. doi:10.1016/S0076-6879(07)26007-0.
   PubMed Web of Science ®Google Scholar
• Carter WG, Kaur P, Gil SG, Gahr PJ, Wayner EA. Distinct functions for integrins alpha 3 beta 1 in focal adhesions and alpha 6 beta 4/bullous pemphigoid antigen in a new stable anchoring contact (SAC) of keratinocytes: relation to hemidesmosomes. J Cell Biol. 1990;111:3141–54.
   PubMed Web of Science ®Google Scholar
• Sonnenberg A, Modderman PW, Hogervorst F. Laminin receptor on platelets is the integrin VLA-6. Nature. 1988;336:487–89. doi:10.1038/336487a0.
   PubMed Web of Science ®Google Scholar
• Heider KH, Dammrich J, Skroch-Angel P, Muller-Hermelink HK, Vollmers HP, Herrlich P, Ponta H. Differential expression of CD44 splice variants in intestinal- and diffuse-type human gastric carcinomas and normal gastric mucosa. Cancer Res. 1993;53:4197–203.
   PubMed Web of Science ®Google Scholar
• Olsson E, Honeth G, Bendahl PO, Saal LH, Gruvberger-Saal S, Ringner M, Vallon-Christersson J, Jönsson G, Holm K, Lövgren K, et al. CD44 isoforms are heterogeneously expressed in breast cancer and correlate with tumor subtypes and cancer stem cell markers. BMC Cancer. 2011;11:418. doi:10.1186/1471-2407-11-418.
   PubMed Web of Science ®Google Scholar
• Basakran NS. CD44 as a potential diagnostic tumor marker. Saudi Med J. 2015;36:273–79. doi:10.15537/smj.2015.3.9622.
   PubMed Web of Science ®Google Scholar
• Belitsos PC, Hildreth JE, August JT. Homotypic cell aggregation induced by anti-CD44(Pgp-1) monoclonal antibodies and related to CD44(Pgp-1) expression. J Immunol. 1990;144:1661–70.
   PubMed Web of Science ®Google Scholar
• Peach RJ, Hollenbaugh D, Stamenkovic I, Aruffo A. Identification of hyaluronic acid binding sites in the extracellular domain of CD44. J Cell Biol. 1993;122:257–64.
   PubMed Web of Science ®Google Scholar
• Bajorath J, Greenfield B, Munro SB, Day AJ, Aruffo A. Identification of CD44 residues important for hyaluronan binding and delineation of the binding site. J Biol Chem. 1998;273:338–43.
   PubMed Web of Science ®Google Scholar
• Gardner MJ, Catterall JB, Jones LM, Turner GA. Human ovarian tumour cells can bind hyaluronic acid via membrane CD44: a possible step in peritoneal metastasis. Clin Exp Mets. 1996;14:325–34.
   PubMed Web of Science ®Google Scholar
• Brown PJ, Juliano RL. Monoclonal antibodies to distinctive epitopes on the alpha and beta subunits of the fibronectin receptor. Exp Cell Res. 1988;177:303–18.
   PubMed Web of Science ®Google Scholar
• Hayashi Y, Haimovich B, Reszka A, Boettiger D, Horwitz A. Expression and function of chicken integrin beta 1 subunit and its cytoplasmic domain mutants in mouse NIH 3T3 cells. J Cell Biol. 1990;110:175–84.
   PubMed Web of Science ®Google Scholar
• Zhang XP, Puzon-McLaughlin W, Irie A, Kovach N, Prokopishyn NL, Laferte S, Takeuchi K, Tsuji T, Takada Y. Alpha 3 beta 1 adhesion to laminin-5 and invasin: critical and differential role of integrin residues clustered at the boundary between alpha 3 N-terminal repeats 2 and 3. Biochem. 1999;38:14424–31.
   PubMed Web of Science ®Google Scholar
• Byron A, Humphries JD, Askari JA, Craig SE, Mould AP, Humphries MJ. Anti-integrin monoclonal antibodies. J Cell Sci. 2009;122:4009–11. doi:10.1242/jcs.056770.
   PubMed Web of Science ®Google Scholar
• Pytela R, Pierschbacher MD, Ruoslahti E. A 125/115-kDa cell surface receptor specific for vitronectin interacts with the arginine-glycine-aspartic acid adhesion sequence derived from fibronectin. Proc Natl Acad Sci USA. 1985;82:5766–70.
   PubMed Web of Science ®Google Scholar
• Hynes RO. Integrins: a family of cell surface receptors. Cell. 1987;48:549–54.
   PubMed Web of Science ®Google Scholar
• Petersen OW, Ronnov-Jessen L, Howlett AR, Bissell MJ. Interaction with basement membrane serves to rapidly distinguish growth and differentiation pattern of normal and malignant human breast epithelial cells. Proc Natl Acad Sci USA. 1992;89:9064–68.
   PubMed Web of Science ®Google Scholar
• Vinci M, Gowan S, Boxall F, Patterson L, Zimmermann M, Court W, Lomas C, Mendiola M, Hardisson D, Eccles SA. Advances in establishment and analysis of three-dimensional tumor spheroid-based functional assays for target validation and drug evaluation. BMC Biol. 2012;10:29. doi:10.1186/1741-7007-10-29.
   PubMed Web of Science ®Google Scholar
• Pardee AB. G1 events and regulation of cell proliferation. Science. 1989;246:603–08.
   PubMed Web of Science ®Google Scholar
• Hanahan D, Weinberg RA. The hallmarks of cancer. Cell. 2000;100:57–70.
   PubMed Web of Science ®Google Scholar
• Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144:646–74. doi:10.1016/j.cell.2011.02.013.
   PubMed Web of Science ®Google Scholar
• Wyllie AH, Kerr JF, Currie AR. Cell death: the significance of apoptosis. Int Rev Cytol. 1980;68:251–306.
   PubMedGoogle Scholar
• Lowe SW, Bodis S, Bardeesy N, McClatchey A, Remington L, Ruley HE, Fisher DE, Jacks T, Pelletier J, Housman DE. Apoptosis and the prognostic significance of p53 mutation. Cold Spring Harb Symp Quant Biol. 1994;59:419–26.
   PubMedGoogle Scholar
• Sporn MB, Todaro GJ. Autocrine secretion and malignant transformation of cells. N Engl J Med. 1980;303:878–80. doi:10.1056/NEJM198010093031511.
   PubMed Web of Science ®Google Scholar
• Ertao Z, Jianhui C, Chuangqi C, Changjiang Q, Sile C, Yulong H, Hui, W., Shirong, C. Autocrine Sonic hedgehog signaling promotes gastric cancer proliferation through induction of phospholipase Cgamma1 and the ERK1/2 pathway. J Exp Clin Cancer Res. 2016;35:63. doi:10.1186/s13046-016-0444-6.
   PubMed Web of Science ®Google Scholar
• Woodhouse EC, Chuaqui RF, Liotta LA. General mechanisms of metastasis. Cancer. 1997;80:1529–37.
   PubMed Web of Science ®Google Scholar
• Rl B, Hy C, Messing A, van Dyke T, Aj L, Palmiter RD. Transgenic mice harboring SV40 T-antigen genes develop characteristic brain tumors. Cell. 1984;37:367–79.
   PubMed Web of Science ®Google Scholar
• Abercrombie M, Heaysman JE. Observations on the social behaviour of cells in tissue culture. II. Monolayering of fibroblasts. Exp Cell Res. 1954;6:293–306.
   PubMed Web of Science ®Google Scholar
• Abercrombie M. Contact inhibition and malignancy. Nature. 1979;281:259–62.
   PubMed Web of Science ®Google Scholar
• Slaughter DP, Southwick HW, Smejkal W. Field cancerization in oral stratified squamous epithelium; clinical implications of multicentric origin. Cancer. 1953;6:963–68.
   PubMed Web of Science ®Google Scholar
• Lochhead P, Chan AT, Nishihara R, Fuchs CS, Beck AH, Giovannucci E, Ogino S. Etiologic field effect: reappraisal of the field effect concept in cancer predisposition and progression. Mod Pathol. 2015;28:14–29. doi:10.1038/modpathol.2014.81.
   PubMed Web of Science ®Google Scholar
• Smoller BR. Histologic criteria for diagnosing primary cutaneous malignant melanoma. Mod Pathol. 2006;19(Suppl 2):S34–40. doi:10.1038/modpathol.3800508.
   PubMedGoogle Scholar
• Cailleau R, Young R, Olive M, Reeves WJ Jr. Breast tumor cell lines from pleural effusions. J Natl Cancer Inst. 1974;53:661–74.
   PubMed Web of Science ®Google Scholar
• Moore GE, Gerner RE. Malignant melanoma. Surg Gynecol Obstet. 1971;132:427–36.
   PubMedGoogle Scholar
• Sanchez P, Daniels KJ, Park YN, Soll DR. Generating a battery of monoclonal antibodies against native green fluorescent protein for immunostaining, FACS, IP, and ChIP using a unique adjuvant. Monoclon Antib Immunodiagn Immunother. 2014;33:80–88. doi:10.1089/mab.2013.0089.
   PubMedGoogle Scholar
• Park YN, Glover RA, Daniels KJ, Soll DR. Generation and validation of monoclonal antibodies against the maltose binding protein. Monoclon Antib Immunodiagn Immunother. 2016;35:104–08. doi:10.1089/mab.2015.0072.
   PubMedGoogle Scholar
• Conway TP, Daniels KJ, Park YN, Soll DR. Generating a battery of monoclonal antibodies against firefly luciferase for dot blot analysis, western blot analysis, and immunostaining of cells in culture and paraffin sections. Monoclon Antib Immunodiagn Immunother. 2018;37:45–51. doi:10.1089/mab.2017.0057.
   PubMedGoogle Scholar
• Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012;9:676–82. doi:10.1038/nmeth.2019.
   PubMed Web of Science ®Google Scholar