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Impairment of the metastatic activity of melanoma cells by transglutaminase-catalyzed incorporation of polyamines into laminin and Matrigel

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Summary.

Previously published evidences highlighted the effect of transglutaminase (TG, EC 2.3.2.13) activation on the reduction of the in vitro adhesive and invasive behaviour of murine B16-F10 melanoma cells, as well as in vivo. Here, we investigated the influence of spermidine (SPD) incorporation by TG into basement membrane components i.e. laminin (LN) or Matrigel (MG), on the adhesion and invasion of B16-F10 melanoma cells by these TG/SPD-modified substrates. The adhesion assays showed that cell binding to the TG/SPD-modified LN was reduced by 30%, when compared to untreated LN, whereas the reduction obtained using TG/SPD-modified MG was 35%. Similarly, tumor cell invasion by the Boyden chamber system through TG/SPD modified LN or MG was respectively reduced by 45%, and by 69%. Evaluation of matrix metalloproteinase (gelatinases MMP-2 and MMP-9) activities by gel-zymography showed that MMP-2 activity was unaffected, while MMP-9 activity was reduced by about 32% using TG/SPD-modified substrate. These results strongly suggest that the observed antiinvasive effect of TG activation in the host may be ascribed to the covalent incorporation of polyamines, which led to the post-translational modification of some components of the cell basement membrane. This modification may interfere with the metastatic property of melanoma cells, affecting the proteolytic activity necessary for their migration and invasion activities.

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References

  • D Aeschlimann M Paulsson (1991) ArticleTitleCross-linking of laminin-nidogen complexes by tissue transglutaminase. A novel mechanism for basement membrane stabilization J Biol Chem 266 15308–15317 Occurrence Handle1678389 Occurrence Handle1:CAS:528:DyaK3MXmslChurw%3D

    PubMed  CAS  Google Scholar 

  • D Aeschlimann M Paulsson K Mann (1992) ArticleTitleIdentification of Gln726 in nidogen as the amine acceptor in transglutaminase-catalyzed cross-linking of laminin-nidogen complexes J Biol Chem 267 11316–11321 Occurrence Handle1350783 Occurrence Handle1:CAS:528:DyaK3sXkvV2ksrk%3D

    PubMed  CAS  Google Scholar 

  • D Aeschlimann V Thomazy (2000) ArticleTitleProtein crosslinking in assembly and remodelling of extracellular matrices: the role of transglutaminases Connect Tissue Res 41 1–27 Occurrence Handle10826705 Occurrence Handle1:CAS:528:DC%2BD3cXnvV2qurk%3D

    PubMed  CAS  Google Scholar 

  • SS Akimov D Krylov LF Fleischman AM Belkin (2000) ArticleTitleTissue transglutaminase is an integrin-binding adhesion coreceptor for fibronectin J Cell Biol 148 825–838 Occurrence Handle10684262 Occurrence Handle10.1083/jcb.148.4.825 Occurrence Handle1:CAS:528:DC%2BD3cXhsVOqsLg%3D

    Article  PubMed  CAS  Google Scholar 

  • A Albini Y Iwamoto HK Kleinman GR Martin SA Aaronson JM Kozlowski RN McEwan (1987) ArticleTitleA rapid in vitro assay for quantitating the invasive potential of tumor cells Cancer Res 47 3239–3245 Occurrence Handle2438036 Occurrence Handle1:STN:280:DyaL2s3hsFKhtQ%3D%3D

    PubMed  CAS  Google Scholar 

  • SH Barsky CN Rao JE Williams LA Liotta (1984) ArticleTitleLaminin molecular domains which alter metastasis in a murine model J Clin Invest 74 843–848 Occurrence Handle6088586 Occurrence Handle1:CAS:528:DyaL2cXlsV2isL4%3D Occurrence Handle10.1172/JCI111501

    Article  PubMed  CAS  Google Scholar 

  • AM Belkin E Zemskov J Hang SS Akimov S Sikora AY Strongin (2004) ArticleTitleCell-surface-associated tissue transglutaminase is a target of MMP-2 proteolysis Biochemistry 43 11760–11769 Occurrence Handle15362860 Occurrence Handle10.1021/bi049266z Occurrence Handle1:CAS:528:DC%2BD2cXmvVyqtL8%3D

    Article  PubMed  CAS  Google Scholar 

  • S Beninati A Abbruzzese M Cardinali (1993) ArticleTitleDifferences in the post-translational modification of proteins by polyamines between weakly and highly metastatic B16 melanoma cells Int J Cancer 53 792–797 Occurrence Handle8095490 Occurrence Handle10.1002/ijc.2910530515 Occurrence Handle1:CAS:528:DyaK3sXltFCmsr4%3D

    Article  PubMed  CAS  Google Scholar 

  • S Beninati DR Senger E Cordella-Miele AB Mukherjee K Singh BB Mukherjee (1994) ArticleTitleOsteopontin: its transglutaminase-catalyzed postranslational modifications and cross-linking to fibronectin J Biochem 115 675–682 Occurrence Handle7916341 Occurrence Handle1:CAS:528:DyaK2cXkslKnsLo%3D

    PubMed  CAS  Google Scholar 

  • V Berno D Porrini F Castiglioni M Campiglio P Casalini SM Pupa A Balsari S Ménard E Tagliabue (2005) ArticleTitleThe 67 kDa laminin receptor increases tumor aggressiveness by remodeling laminin-1 Endocr Relat Cancer 12 393–406 Occurrence Handle15947111 Occurrence Handle10.1677/erc.1.00870 Occurrence Handle1:CAS:528:DC%2BD2MXnsl2nur4%3D

    Article  PubMed  CAS  Google Scholar 

  • PJ Birckbichler MK Patterson (1978) ArticleTitleCellular transglutaminase, growth, and transformation Ann NY Acad Sci 312 354–365 Occurrence Handle40517 Occurrence Handle10.1111/j.1749-6632.1978.tb16813.x Occurrence Handle1:CAS:528:DyaE1MXksFeksb8%3D

    Article  PubMed  CAS  Google Scholar 

  • JM Bowness JE Folk R Timpl (1987) ArticleTitleIdentification of a substrate site for liver transglutaminase on the aminopeptide of type III collagen J Biol Chem 262 1022–1024 Occurrence Handle2879837 Occurrence Handle1:CAS:528:DyaL2sXhtFGltrw%3D

    PubMed  CAS  Google Scholar 

  • TH Chang E Szabo (2000) ArticleTitleInduction of differentiation and apoptosis by ligands of peroxisome proliferator-activated receptor γ in non small cell lung cancer Cancer Res 60 1129–1138 Occurrence Handle10706135 Occurrence Handle1:CAS:528:DC%2BD3cXhs1Shsbk%3D

    PubMed  CAS  Google Scholar 

  • SI Chung JE Folk (1972) ArticleTitletransglutaminase from hair follicle of guinea pig Proc Natl Acad Sci USA 69 303–307 Occurrence Handle4501114 Occurrence Handle10.1073/pnas.69.2.303 Occurrence Handle1:CAS:528:DyaE38Xps1WhtQ%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • CY Dadabay LJ Pike (1989) ArticleTitlePurification and characterization of a cytosolic transglutaminase from a cultured human tumour-cell line Biochem J 264 679–685 Occurrence Handle2575900 Occurrence Handle1:CAS:528:DyaK3cXjt1Kl

    PubMed  CAS  Google Scholar 

  • IJ Fidler (1973) ArticleTitleSelection of successive tumor lines for metastases Nature 245 148–149 Occurrence Handle10.1038/245148a0

    Article  Google Scholar 

  • IJ Fidler (1990) ArticleTitleCritical factors in the biology of human cancer metastasis: Twenty-eight G.H.A. Clowes memorial award lecture Cancer Res 50 6130–6138 Occurrence Handle1698118 Occurrence Handle1:STN:280:DyaK3czotFKrsA%3D%3D

    PubMed  CAS  Google Scholar 

  • JE Folk (1980) ArticleTitleTranglutaminases Annu Rev Biochem 49 517–531 Occurrence Handle6105840 Occurrence Handle10.1146/annurev.bi.49.070180.002505 Occurrence Handle1:CAS:528:DyaL3cXks1ChtLw%3D

    Article  PubMed  CAS  Google Scholar 

  • DS Grant HK Kleinman CP Leblond S Inoue AE Chung GR Martin (1985) ArticleTitleThe basement membrane-like matrix of the mouse EHS tumor: II. Immunohistochemical quantitation of six of its components Am J Anat 174 387–398 Occurrence Handle4083259 Occurrence Handle10.1002/aja.1001740403 Occurrence Handle1:CAS:528:DyaL28XkvFelsw%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • ZA Haroon TS Lai JM Hettasch RA Lindberg MW Dewhirst CS Greenberg (1999) ArticleTitleTissue transglutaminase is expressed as a host response to tumor invasion and inhibits tumor growth Lab Invest 79 1679–1686 Occurrence Handle10616216 Occurrence Handle1:CAS:528:DC%2BD3cXlsVCrtQ%3D%3D

    PubMed  CAS  Google Scholar 

  • RA Jones P Kotsakis TS Johnson DY Chau S Ali G Melino M Griffin (2006) ArticleTitleMatrix changes induced by transglutaminase 2 lead to inhibition of angiogenesis and tumor growth Cell Death Differ 13 1442–1453 Occurrence Handle16294209 Occurrence Handle10.1038/sj.cdd.4401816 Occurrence Handle1:CAS:528:DC%2BD28XotVyltrg%3D

    Article  PubMed  CAS  Google Scholar 

  • MT Kaartineen A Pirhonen A Linnala-Kankkunen PH Maenpaa (1999) ArticleTitleCross-linking of osteopontin by tissue transglutaminase increases its collagen binding properties J Biol Chem 274 1729–1735 Occurrence Handle10.1074/jbc.274.3.1729

    Article  Google Scholar 

  • HK Kleinman ML McGarvey JR Hassel VL Star FB Cannon GW Laurie GR Martin (1986) ArticleTitleBasement membranes complexes with biological activity Biochemistry 25 312–318 Occurrence Handle2937447 Occurrence Handle10.1021/bi00350a005 Occurrence Handle1:CAS:528:DyaL28XosVSmsA%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • HK Kleinman R Fridman T Kanemoto TM Sweeney M Zain L Royce (1991) ArticleTitleRole of basement membrane and laminin in metastasis and tumor growth Proc Am Assoc Cancer Res 31 490–498

    Google Scholar 

  • A Lentini P Mattioli L Nicolini A Pietrini A Abbruzzese S Beninati (1997) ArticleTitleAnti-invasive effects of theophylline on experimental B16-F10 melanoma lung metastasis Cancer J 10 274–277 Occurrence Handle1:CAS:528:DyaK1cXht1Gntg%3D%3D

    CAS  Google Scholar 

  • A Lentini HK Kleinman P Mattioli V Autuori-Pezzoli L Nicolini A Pietrini A Abbruzzese M Cardinali S Beninati (1998) ArticleTitleInhibition of melanoma pulmonary metastasis by methylxanthines due to decreased invasion and proliferation Melanoma Res 8 131–137 Occurrence Handle9610865 Occurrence Handle10.1097/00008390-199804000-00005 Occurrence Handle1:CAS:528:DyaK1cXjt1Sns7k%3D

    Article  PubMed  CAS  Google Scholar 

  • A Lentini C Forni B Provenzano S Beninati (2007) ArticleTitleEnhancement of transglutaminase activity and polyamine depletion in B16-F10 melanoma cells by flavonoids naringenin and hesperitin correlate to reduction of the in vivo metastatic potential Amino Acids 32 95–100 Occurrence Handle16699821 Occurrence Handle10.1007/s00726-006-0304-3 Occurrence Handle1:CAS:528:DC%2BD28Xht1Ogs7rO

    Article  PubMed  CAS  Google Scholar 

  • LA Liotta CN Rao UM Wewer (1986) ArticleTitleBiochemical interactions of tumor cells with the basement membrane Annu Rev Biochem 55 1037–1057 Occurrence Handle3017189 Occurrence Handle10.1146/annurev.bi.55.070186.005133 Occurrence Handle1:CAS:528:DyaL28XkslKku7g%3D

    Article  PubMed  CAS  Google Scholar 

  • RB Maccioni J Arechaga (1986) ArticleTitleTransglutaminase (TG) involvement in early embryogenesis Exp Cell Res 167 266–270 Occurrence Handle2875896 Occurrence Handle10.1016/0014-4827(86)90224-7 Occurrence Handle1:CAS:528:DyaL28Xmt1entLc%3D

    Article  PubMed  CAS  Google Scholar 

  • A Maddox MK Haddox (1985) ArticleTitleTransglutaminase activity increases in HL60 cells induced to differentiate with retinoic acid and TPA but not with DMSO Exp Cell Biol 53 294–300 Occurrence Handle2864293 Occurrence Handle1:CAS:528:DyaL2MXlvFeqsr8%3D Occurrence Handle10.1159/000163325

    Article  PubMed  CAS  Google Scholar 

  • SL Mangala B Arun AA Sahin K Mehta (2005) ArticleTitleTissue transglutaminase-induced alterations in extracellular matrix inhibit tumor invasion Mol Cancer 4 33–40 Occurrence Handle16153302 Occurrence Handle10.1186/1476-4598-4-33 Occurrence Handle1:CAS:528:DC%2BD2MXhtV2ktbjO

    Article  PubMed  CAS  Google Scholar 

  • GR Martin R Timpl (1987) ArticleTitleLaminin and other basement membrane components Ann Rev Cell Biol 3 57–85 Occurrence Handle3318883 Occurrence Handle1:CAS:528:DyaL1cXltlWqsg%3D%3D

    PubMed  CAS  Google Scholar 

  • DF Mosher (1984) ArticleTitleCross-linking of fibronectin to collagenous proteins Mol Cell Biochem 58 63–68 Occurrence Handle6143254 Occurrence Handle10.1007/BF00240605 Occurrence Handle1:CAS:528:DyaL2cXpvVKjuw%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • GL Nicolson (1989) ArticleTitleMetastatic tumor cell interactions with endothelium, basement membrane and tissue Curr Opin Cell Biol 1 1009–1019 Occurrence Handle2697287 Occurrence Handle10.1016/0955-0674(89)90073-2 Occurrence Handle1:STN:280:DyaK3c7otVOjsA%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • DC Sane TL Moser AM Pippen CJ Parker KE Achyuthan CS Greenberg (1988) ArticleTitleVitronectin is a substrate for transglutaminases Biochem Biophys Res Commun 157 115–120 Occurrence Handle2461707 Occurrence Handle10.1016/S0006-291X(88)80020-2 Occurrence Handle1:CAS:528:DyaL1MXltlGrtg%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • DG Tang KV Honn (1994) ArticleTitleAdhesion molecules and tumor metastasis: an update Invas Metast 14 109–122 Occurrence Handle1:CAS:528:DyaK2MXovF2mtr4%3D

    CAS  Google Scholar 

  • VP Terranova JE Williams LA Liotta GR Martin (1984) ArticleTitleModulation of the metastatic activity of melanoma cells by laminin and fibronectin Science 226 982–985 Occurrence Handle6505678 Occurrence Handle10.1126/science.6505678 Occurrence Handle1:CAS:528:DyaL2MXjvF2h

    Article  PubMed  CAS  Google Scholar 

  • R Timpl S Fujiwara M Dziadek M Aumailley S Weber J Engel (1984) ArticleTitleLaminin, proteoglycan, nidogen and collagen IV: structural models and molecular interactions Ciba Found Symp 108 25–43 Occurrence Handle6440757 Occurrence Handle1:CAS:528:DyaL2MXnsVantg%3D%3D

    PubMed  CAS  Google Scholar 

  • T Turpeenniemi-Hujanen (2005) ArticleTitleGelatinases (MMP-2 and MMP-9) and their natural inhibitors as prognostic indicators in solid cancers Biochimie 87 287–297 Occurrence Handle15781315 Occurrence Handle10.1016/j.biochi.2005.01.014 Occurrence Handle1:CAS:528:DC%2BD2MXisVWqt7k%3D

    Article  PubMed  CAS  Google Scholar 

  • UM Wewer LA Liotta M Jaye GA Ricca WN Drohan AP Claysmith CN Rao et al. (1986) ArticleTitleAltered levels of laminin receptor mRNA in various human carcinoma cells that have different abilities to bind laminin Proc Natl Acad Sci USA 83 7137–7141 Occurrence Handle2429301 Occurrence Handle10.1073/pnas.83.19.7137 Occurrence Handle1:CAS:528:DyaL28XmtVKltLg%3D

    Article  PubMed  CAS  Google Scholar 

  • HK Yow JM Wong HS Chen CG Lee S Davis GD Steele SuffixJr LB Chen (1988) ArticleTitleIncreased mRNA expression of a laminin binding protein in human colon carcinoma. Complete sequence of a full-length cDNA encoding the protein Proc Natl Acad Sci USA 85 6394–6398 Occurrence Handle2970639 Occurrence Handle10.1073/pnas.85.17.6394 Occurrence Handle1:CAS:528:DyaL1MXhsVyqtLw%3D

    Article  PubMed  CAS  Google Scholar 

  • EA Zemskov A Janiak J Hang A Waghray AM Belkin (2006) ArticleTitleThe role of tissue transglutaminase in cell-matrix interactions Front Biosci 11 1057–1076 Occurrence Handle16146797 Occurrence Handle10.2741/1863 Occurrence Handle1:CAS:528:DC%2BD2MXhtlSrurfK

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Biology, University of Rome “Tor Vergata”, Rome, Italy

    A. Lentini, B. Provenzano & S. Beninati

  2. Experimental Oncology Department, National Institute of Tumours, Fondazione G. Pascale, Naples, Italy

    M. Caraglia

  3. Department of Biochemistry, Russian People’s Friendship University, Moscow, Russia

    A. Shevchenko

  4. Department of Biochemistry and Biophysics, University of Naples, Naples, Italy

    A. Abbruzzese

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  1. A. Lentini
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  2. B. Provenzano
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  3. M. Caraglia
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  4. A. Shevchenko
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  5. A. Abbruzzese
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  6. S. Beninati
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Authors’ address: Simone Beninati, Department of Biology, University of Rome “Tor Vergata”, Via della Ricerca Scientifica, I-00133 Rome, Italy

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Lentini, A., Provenzano, B., Caraglia, M. et al. Impairment of the metastatic activity of melanoma cells by transglutaminase-catalyzed incorporation of polyamines into laminin and Matrigel. Amino Acids 34, 251–256 (2008). https://doi.org/10.1007/s00726-007-0505-4

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