Skip to main content

Advertisement

SpringerLink
Log in

Tissue transglutaminase in tumour progression: friend or foe?

  • Review Article
  • Published:
Amino Acids Aims and scope Submit manuscript

Summary.

Basic biological processes in which tissue transglutaminase (TG2, tTG) is thought to be important including apoptosis, cell adhesion and migration, ECM homeostasis and angiogenesis are key stages in the multistage tumour progression cascade. Studies undertaken with primary tumours and experimental models suggest that TG2 expression and activity in the tumour body and surrounding matrix generally decreases with tumour progression, favouring matrix destabilisation, but supporting angiogenesis and tumour invasion. In contrast, in the secondary metastatic tumour TG2 is often highly expressed whereby its potential roles in cell survival both at the intra- and extracellular level become important. In the following review the underlying molecular basis for the selection of these different phenotypes in tumour types and the anomaly for the requirement of TG2 is discussed in relation to the complex events of tumour progression.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

bFGF:

basic fibroblast growth factor

EC:

endothelial cell

ECM:

extracellular matrix

EGF:

endothelial growth factor

FAK:

focal adhesion kinase

LTBP:

latent transforming growth factor-β binding protein

MMP:

matrix metalloproteinase

NF-kappa B :

nuclear factor-kappa B

NO:

nitric oxide

TG2:

tissue transglutaminase

TGF-β:

transforming growth factor β

TIMP:

tissue inhibitor of matrix metalloproteinases

uPA:

urokinase plasminogen activator

uPARAP:

urokinase plasminogen activator receptor associated protein

VEGF:

vascular endothelial growth factor

References

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

    PubMed  CAS  Google Scholar 

  • SS Akimov AM Belkin (2001) ArticleTitleCell surface tissue transglutaminase is involved in adhesion and migration of monocytic cells on fibronectin Blood 98 1567–1576 Occurrence Handle11520809 Occurrence Handle10.1182/blood.V98.5.1567 Occurrence Handle1:CAS:528:DC%2BD3MXmvFGjtbs%3D

    Article  PubMed  CAS  Google Scholar 

  • SS Akimov B Krylov LF Flaischlimann AM Belkin (2000) ArticleTitleTissue transglutaminase is an integrin binding adhesion co-receptor for fibronectin J Biol Chem 148 825–838 Occurrence Handle1:CAS:528:DC%2BD3cXhsVOqsLg%3D

    CAS  Google Scholar 

  • MA Antonyak JM Jansen AM Miller TK Ly M Endo RA Cerione (2006) ArticleTitleTwo isoforms of tissue transglutaminase mediate opposing cellular fates Proc Natl Acad Sci USA 103 18609–18614 Occurrence Handle17116873 Occurrence Handle10.1073/pnas.0604844103 Occurrence Handle1:CAS:528:DC%2BD28XhtlahtrzO

    Article  PubMed  CAS  Google Scholar 

  • MA Antonyak US Singh DA Lee JE Boehm C Combs MM Zgola RL Page RA Cerione (2001) ArticleTitleEffects of tissue transglutaminase on retinoic acid-induced cellular differentiation and protection against apoptosis J Biol Chem 276 33582–33587 Occurrence Handle11438548 Occurrence Handle10.1074/jbc.M105318200 Occurrence Handle1:CAS:528:DC%2BD3MXmslyls7c%3D

    Article  PubMed  CAS  Google Scholar 

  • GC Auld H Ritchie LA Robbie NA Booth (2001) ArticleTitleThrombin upregulates tissue transglutaminase in ECs: a potential role for tissue transglutaminase in stability of atherosclerotic plaque Arterioscler Thromb Vasc Biol 21 1689–1694 Occurrence Handle11597946 Occurrence Handle1:CAS:528:DC%2BD3MXnslKqs7g%3D

    PubMed  CAS  Google Scholar 

  • C Barsigian AM Stern J Martinez (1991) ArticleTitleTissue (type II) transglutaminase covalently incorporates itself, fibrinogen, or fibronectin into high molecular weight complexes on the extracellular surface of isolated hepatocytes J Biol Chem 266 22501–22509 Occurrence Handle1682320 Occurrence Handle1:CAS:528:DyaK3MXmt12iu74%3D

    PubMed  CAS  Google Scholar 

  • AM Belkin SS Akimov LS Zaritskaya BI Ratnikov EI Deryugina AY Strongin (2001) ArticleTitleMatrix dependent proteolysis of surface transglutaminase by membrane type metalloproteinase regulates cancer cell adhesion and locomotion J Biol Chem 276 18415–18422 Occurrence Handle11278623 Occurrence Handle10.1074/jbc.M010135200 Occurrence Handle1:CAS:528:DC%2BD3MXktFWmt7c%3D

    Article  PubMed  CAS  Google Scholar 

  • AM Belkin EA 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 

  • SE Bell A Mavila R Salazar KJ Bayless S Kanagala SA Maxwell GE Davis (2001) ArticleTitleDifferential gene expression during capillary morphogenesis in 3D collagen matrices: regulated expression of genes involved in basement membrane matrix assembly, cell cycle progression, cellular differentiation and G-protein signalling J Cell Sci 114 2755–2773 Occurrence Handle11683410 Occurrence Handle1:CAS:528:DC%2BD3MXmt1Wgu70%3D

    PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • JM Bowness AH Tarr T Wong (1988) ArticleTitleIncreased transglutaminase activity during skin wound healing in rats Biochem Biophys Acta 967 234–240 Occurrence Handle2903771 Occurrence Handle1:CAS:528:DyaL1MXls1Gm

    PubMed  CAS  Google Scholar 

  • DY Chau RJ Collighan EA Verderio VL Addy M Griffin (2005) ArticleTitleThe cellular response to transglutaminase-cross-linked collagen Biomaterials 26 6518–6529 Occurrence Handle15927250 Occurrence Handle10.1016/j.biomaterials.2005.04.017 Occurrence Handle1:CAS:528:DC%2BD2MXms1Okur8%3D

    Article  PubMed  CAS  Google Scholar 

  • V De Laurenzi G Melino (2001) ArticleTitleGene disruption of tissue transglutaminase Mol Cell Biol 21 148–155 Occurrence Handle11113189 Occurrence Handle10.1128/MCB.21.1.148-155.2001 Occurrence Handle1:CAS:528:DC%2BD3MXovFyk

    Article  PubMed  CAS  Google Scholar 

  • HF Dvorak (1986) ArticleTitleTumors: wounds that do not heal. Similarities between tumor stroma generation and wound healing N Engl J Med 315 1650–1659 Occurrence Handle3537791 Occurrence Handle1:STN:280:DyaL2s%2FmsV2mtw%3D%3D Occurrence Handle10.1056/NEJM198612253152606

    Article  PubMed  CAS  Google Scholar 

  • L Fesus Z Szondy (2005) ArticleTitleTransglutaminase 2 in the balance of cell death and survival FEBS Lett 579 3297–3302 Occurrence Handle15943974 Occurrence Handle10.1016/j.febslet.2005.03.063 Occurrence Handle1:CAS:528:DC%2BD2MXltFSqu70%3D

    Article  PubMed  CAS  Google Scholar 

  • L Fesus V Thomazy F Autuori MP Ceru E Tarcsa M Piancentini (1989) ArticleTitleApoptotic hepatocytes become insoluble in detergents and chaotropic agents as a result of transglutaminase action FEBS Lett 245 150–154 Occurrence Handle2564346 Occurrence Handle10.1016/0014-5793(89)80210-8 Occurrence Handle1:CAS:528:DyaL1MXhslSqtr4%3D

    Article  PubMed  CAS  Google Scholar 

  • JY Fok S Ekmekcioglu K Mehta (2006) ArticleTitleImplications of tissue transglutaminase expression in malignant melanoma Mol Cancer Ther 5 1493–1503 Occurrence Handle16818508 Occurrence Handle10.1158/1535-7163.MCT-06-0083 Occurrence Handle1:CAS:528:DC%2BD28XmsVams70%3D

    Article  PubMed  CAS  Google Scholar 

  • J Folkman (1990) ArticleTitleWhat is the evidence that tumors are angiogenesis dependent J Natl Cancer Inst 82 4–6 Occurrence Handle1688381 Occurrence Handle10.1093/jnci/82.1.4 Occurrence Handle1:STN:280:DyaK3c%2FnvF2qug%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • L Foulds (1954) The experimental study of tumour progressions NumberInSeriesI–III Academic Press London

    Google Scholar 

  • CA Gaudry E Verderio D Aeschlimann A Cox C Smith M Griffin (1999) ArticleTitleCell surface localization of tissue transglutaminase is dependent on a fibronectin-binding site in its N-terminal beta-sandwich domain J Biol Chem 22 30707–30714 Occurrence Handle10.1074/jbc.274.43.30707

    Article  Google Scholar 

  • M Griffin R Casadio CM Bergamini (2002) ArticleTitleTransglutaminases: nature’s biological glues Biochem J 368 377–396 Occurrence Handle12366374 Occurrence Handle10.1042/BJ20021234 Occurrence Handle1:CAS:528:DC%2BD38XovF2jt78%3D

    Article  PubMed  CAS  Google Scholar 

  • MY Grigoriev EN Suspitsin AV Togo KM Pozharisski OA Ivanova R Nardacci L Falasca M Piacentini EN Imyanitov KP Hanson (2001) ArticleTitleTissue transglutaminase expression in breast carcinomas J Exp Clin Cancer Res 20 265–268 Occurrence Handle11484985 Occurrence Handle1:STN:280:DC%2BD38%2FislCltg%3D%3D

    PubMed  CAS  Google Scholar 

  • JL Guan (1997) ArticleTitleRole of focal adhesion kinase in integrin signaling Int J Biochem Cell Biol 29 1085–1096 Occurrence Handle9416004 Occurrence Handle10.1016/S1357-2725(97)00051-4 Occurrence Handle1:CAS:528:DyaK2sXotVGhs74%3D

    Article  PubMed  CAS  Google Scholar 

  • WC Hahn CM Counter AS Lunberg RL Beijersbern MW Brooks RA Weinberg (1999) ArticleTitleCreation of human tumour cells with defined genetic elements Nature 400 464–468 Occurrence Handle10440377 Occurrence Handle10.1038/22780 Occurrence Handle1:CAS:528:DyaK1MXltVGmtLc%3D

    Article  PubMed  CAS  Google Scholar 

  • D Hanahan RA Weinberg (2000) ArticleTitleThe hallmarks of cancer Cell 100 57–70 Occurrence Handle10647931 Occurrence Handle10.1016/S0092-8674(00)81683-9 Occurrence Handle1:CAS:528:DC%2BD3cXks1CktA%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • D Hand BM Elliott M Griffin (1988) ArticleTitleExpression of the cytosolic and particulate forms of transglutaminase during chemically induced rat liver carcinogenesis Biochem Biophys Acta 970 137–145 Occurrence Handle2898262 Occurrence Handle10.1016/0167-4889(88)90172-3 Occurrence Handle1:CAS:528:DyaL1cXkslWhurY%3D

    Article  PubMed  CAS  Google Scholar 

  • ZA Haroon JM Hettasch TS Lai MW Dewhirst CS Greenberg (1999a) ArticleTitleTissue transglutaminase is expressed, active, and directly involved in rat dermal wound healing and angiogenesis FASEB J 13 1787–1795 Occurrence Handle1:CAS:528:DyaK1MXms1Ohsrk%3D

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • JF Herman LS Mangala K Mehta (2006) ArticleTitleImplications of increased tissue transglutaminase (TG2) expression in drug-resistant breast cancer (MCF-7) cells Oncogene 25 3049–3058 Occurrence Handle16449978 Occurrence Handle10.1038/sj.onc.1209324 Occurrence Handle1:CAS:528:DC%2BD28Xks1OrsLw%3D

    Article  PubMed  CAS  Google Scholar 

  • JM Hettasch N Bandarenko JL Burchette TS Lai JR Marks ZA Haroon K Peters MW Dewhirst JD Iglehart CS Greenberg (1996) ArticleTitleTissue transglutaminase expression in human breast cancer Lab Invest 75 637–645 Occurrence Handle8941210 Occurrence Handle1:STN:280:DyaK2s%2Fps1WrtA%3D%3D

    PubMed  CAS  Google Scholar 

  • I Hunter K Sigmundsson N Beauchemin B Obrink (1998) ArticleTitleThe cell adhesion molecule C-CAM is a substrate for tissue transglutaminase FEBS Lett 425 141–144 Occurrence Handle9541024 Occurrence Handle10.1016/S0014-5793(98)00223-3 Occurrence Handle1:CAS:528:DyaK1cXhs1Gis70%3D

    Article  PubMed  CAS  Google Scholar 

  • DE Ingber (2002) ArticleTitleMechanical signaling and the cellular response to extracellular matrix in angiogenesis and cardiovascular physiology Circ Res 91 877–887 Occurrence Handle12433832 Occurrence Handle10.1161/01.RES.0000039537.73816.E5 Occurrence Handle1:CAS:528:DC%2BD38XosFWgu7s%3D

    Article  PubMed  CAS  Google Scholar 

  • D Jiang W Ying Y Lu J Wan W Liu Y Zhu Z Qiu F Qian (2003) ArticleTitleIdentification of metastasis associated proteins by proteomic analysis and functional exploration of interleukin-18 in metastasis Proteomics 3 724–737 Occurrence Handle12748951 Occurrence Handle10.1002/pmic.200300411 Occurrence Handle1:CAS:528:DC%2BD3sXjvFGisb8%3D

    Article  PubMed  CAS  Google Scholar 

  • TS Johnson CR Knight S el-Alaoui S Mian RC Rees V Gentile PJ Davies M Griffin (1994) ArticleTitleTransfection of tissue transglutaminase into a highly malignant hamster fibrosarcoma leads to a reduced incidence of primary tumor growth Oncogene 9 2935–2942 Occurrence Handle7916148 Occurrence Handle1:CAS:528:DyaK2cXmt1Olsbk%3D

    PubMed  CAS  Google Scholar 

  • TS Johnson CI Scholfield J Parry M Griffin (1998) ArticleTitleInduction of tissue transglutaminase by dexamethasone: its correlation to receptor number and transglutaminase-mediated cell death in a series of malignant hamster fibrosarcomas Biochem J 331 105–112 Occurrence Handle9512467 Occurrence Handle1:CAS:528:DyaK1cXisVWksbg%3D

    PubMed  CAS  Google Scholar 

  • TS Johnson NJ Skill AM Nahas SD Oldroyd GL Thomas JA Douthwaite JL Haylor M Griffin (1999) ArticleTitleTransglutaminase translocation and antigen translocation in experimental renal scarring J Am Soc Nephrol 10 2146–2157 Occurrence Handle10505691 Occurrence Handle1:CAS:528:DyaK1MXms1ylsrg%3D

    PubMed  CAS  Google Scholar 

  • RA Jones P Kotsakis TS Johnson DY Chau S Ali G Melino M Griffin (2005) ArticleTitleMatrix changes induced by transglutaminase 2 lead to inhibition of angiogenesis and tumour 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 

  • RA Jones B Nicholas S Mian PJA Davis M Griffin (1997) ArticleTitleReduced expression of tissue transglutaminase in a human EC line leads to changes in cell spreading, cell adhesion and reduced polymerisation of fibronectin J Cell Sci 110 2461–2472 Occurrence Handle9410884 Occurrence Handle1:CAS:528:DyaK2sXnt1Giurg%3D

    PubMed  CAS  Google Scholar 

  • L Kong RJ Korthuis (1997) ArticleTitleMelanoma cell adhesion to injured arterioles: mechanisms of stabilised tethering Clin Exp Metastasis 15 426–431 Occurrence Handle9219731 Occurrence Handle10.1023/A:1018406422727 Occurrence Handle1:STN:280:DyaK2szmtlCgug%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • G Korner DE Schneider MA Purdon TD Bjornsson (1989) ArticleTitleBovine aortic EC transglutaminase. Enzyme characterization and regulation of activity Biochem J 262 633–641 Occurrence Handle2572221 Occurrence Handle1:CAS:528:DyaL1MXls12rsbk%3D

    PubMed  CAS  Google Scholar 

  • N LeBrasseur (2005) ArticleTitleTumours feed on collagen J Chem Biol 169 835

    Google Scholar 

  • J Lee YS Kim DH Choi MS Bang TR Han TH Joh SY Kim (2004) ArticleTitleTransglutaminase 2 induces nuclear factor-kappa B activation via a novel pathway in BV-2 microglia J Biol Chem 279 53725–53735 Occurrence Handle15471861 Occurrence Handle10.1074/jbc.M407627200 Occurrence Handle1:CAS:528:DC%2BD2cXhtVKqu73F

    Article  PubMed  CAS  Google Scholar 

  • LA Liotta CE Kohn (2001) ArticleTitleThe microenvironment of the tumour-host interface Nature 411 375–379 Occurrence Handle11357145 Occurrence Handle10.1038/35077241 Occurrence Handle1:CAS:528:DC%2BD3MXktVSjs78%3D

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • AP Mann A Verma G Sethi B Manavathi H Wang JY Fok AB Kunnumakkara R Kumar BB Aggarwal K Mehta (2000) ArticleTitleOverexpression of tissue transglutaminase leads to constitutive activation of nuclear factor-{kappa}B in cancer cells: delineation of a novel pathway Cancer Res 66 8788–8795 Occurrence Handle10.1158/0008-5472.CAN-06-1457 Occurrence Handle1:CAS:528:DC%2BD28XovF2hsbg%3D

    Article  CAS  Google Scholar 

  • J Martinez DG Chalupowitz RK Roush A Sheth C Barsigian (1994) ArticleTitleTransglutaminase mediated processing of fibronectin by EC monolayers Biochemistry 33 2538–2545 Occurrence Handle7906954 Occurrence Handle10.1021/bi00175a024 Occurrence Handle1:CAS:528:DyaK2cXhsF2rsbo%3D

    Article  PubMed  CAS  Google Scholar 

  • K Mehta (1994) ArticleTitleHigh levels of transglutaminase expression in doxorubicin-resistant human breast carcinoma cells Int J Cancer 58 400–406 Occurrence Handle7914183 Occurrence Handle10.1002/ijc.2910580316 Occurrence Handle1:CAS:528:DyaK2cXlslKgtLc%3D

    Article  PubMed  CAS  Google Scholar 

  • K Mehta J Fok FR Miller D Koul AA Sahin (2004) ArticleTitlePrognostic significance of tissue transglutaminase in drug resistant and metastatic breast cancer Clin Cancer Res 10 8068–8076 Occurrence Handle15585642 Occurrence Handle10.1158/1078-0432.CCR-04-1107 Occurrence Handle1:CAS:528:DC%2BD2cXhtVCrs7vO

    Article  PubMed  CAS  Google Scholar 

  • G Melino M Annicchiarico-Putruzzelli L Piredda E Candi V Gentile PJA Davies M Piacentini (1994) ArticleTitleTissue transglutaminase and apoptosis: sence and antisensse transfection studies with human neuroblastoma cells Mol Cell Biol 14 6584–6596 Occurrence Handle7935379 Occurrence Handle1:CAS:528:DyaK2cXmtVajtLw%3D

    PubMed  CAS  Google Scholar 

  • S Mian S EI Alaoui J Lawry V Gentile PJA Davies M Griffin (1995) ArticleTitleThe importance of the GTP-binding protein tissue transglutaminase in the regulation of cell cycle progression FEBS Lett 370 27–31 Occurrence Handle7649299 Occurrence Handle10.1016/0014-5793(95)00782-5 Occurrence Handle1:CAS:528:DyaK2MXns1Cqs70%3D

    Article  PubMed  CAS  Google Scholar 

  • A Mirza S Liu E Frizell J Zhu J Maddukuri P Davis R Schwarting P Norton MA Zern (1997) ArticleTitleA role of tissue transglutaminase in hepatic injury and fibrogenesis and its regulation by NF kapa beta Am Physiol Soc 35 281–288

    Google Scholar 

  • M Mizoguchi T Iwaki M Fukui (1998) ArticleTitleA comparative immunohistochemical study of tissue transglutaminase and factor XIIIa in hemangioblastoma Neuropathology 18 199–205 Occurrence Handle10.1111/j.1440-1789.1998.tb00100.x

    Article  Google Scholar 

  • H Nakahara (1997) ArticleTitleTransmembrane/cytoplasmic domain mediated membrane type 1-matrix metalloproteinase docking to invadopodia is required for cell invasion Proc Natl Acad Sci USA 94 7959–7964 Occurrence Handle9223295 Occurrence Handle10.1073/pnas.94.15.7959 Occurrence Handle1:CAS:528:DyaK2sXksl2nurs%3D

    Article  PubMed  CAS  Google Scholar 

  • B Nicholas P Smethurst E Verderio R Jones M Griffin (2003) ArticleTitleCross-linking of cellular proteins by tissue transglutaminase during necrotic cell death: a mechanism for maintaining tissue integrity Biochem J 371 413–422 Occurrence Handle12533191 Occurrence Handle10.1042/BJ20021949 Occurrence Handle1:CAS:528:DC%2BD3sXisleqsrw%3D

    Article  PubMed  CAS  Google Scholar 

  • S Oliverio A Amendola F Di Sano MG Farrace L Fesus Z Nemes L Piredda A Spinedi M Piacentini (1997) ArticleTitleTissue transglutaminase-dependent posttranslational modification of the retinoblastoma gene product in promonocytic cells undergoing apoptosis Mol Cell Biol 17 6040–6048 Occurrence Handle9315663 Occurrence Handle1:CAS:528:DyaK2sXmtlOhtrc%3D

    PubMed  CAS  Google Scholar 

  • CC Park MJ Bissell MH Barcellos-Hoffm (2000) ArticleTitleThe influence of the microenvironment on the malignant phenotype Mol Med Today 6 324–329 Occurrence Handle10904250 Occurrence Handle10.1016/S1357-4310(00)01756-1 Occurrence Handle1:CAS:528:DC%2BD3cXls1ansrc%3D

    Article  PubMed  CAS  Google Scholar 

  • M Piacentini MG Farrace L Piredda P Matarrese F Ciccosanti L Falasca C Rodolfo AM Giammarioli E Verderio M Griffin W Malorni (2002) ArticleTitleTransglutaminase overexpression sensitizes neuronal cell lines to apoptosis by increasing mitochondrial membrane potential and cellular oxidative stress J Neurochem 81 1061–1072 Occurrence Handle12065619 Occurrence Handle10.1046/j.1471-4159.2002.00898.x Occurrence Handle1:CAS:528:DC%2BD38XksV2hs7s%3D

    Article  PubMed  CAS  Google Scholar 

  • M Piacentini L Piredda DT Starace M Annicchiarico-Petruzzelli M Mattei S Oliverio MG Farrace G Melino (1996) ArticleTitleDifferential growth of N- and S-type human neuroblastoma cells xenografted into scid mice: correlation with apoptosis J Pathol 180 415–422 Occurrence Handle9014863 Occurrence Handle10.1002/(SICI)1096-9896(199612)180:4<415::AID-PATH684>3.0.CO;2-A Occurrence Handle1:STN:280:DyaK2s7mslWktg%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • DH Russell JR Womble (1982) ArticleTitleTransglutaminase may mediate certain physiological effects of endogenous amines and of amine-containing therapeutic agents Life Sci 30 1499–1508 Occurrence Handle6123059 Occurrence Handle10.1016/0024-3205(82)90236-3 Occurrence Handle1:CAS:528:DyaL38XhvFaksLk%3D

    Article  PubMed  CAS  Google Scholar 

  • PA Smethurst M Griffin (1996) ArticleTitleMeasurement of tissue transglutaminase activity in a permeabilized cell system: its regulation by Ca2+ and nucleotides Biochem J 313 803–808 Occurrence Handle8611158 Occurrence Handle1:CAS:528:DyaK28XhtV2it7g%3D

    PubMed  CAS  Google Scholar 

  • D Telci M Griffin (2006) ArticleTitleTissue transglutaminase (TG2) – a wound response enzyme Front Biosci 11 867–882 Occurrence Handle16146777 Occurrence Handle10.2741/1843 Occurrence Handle1:CAS:528:DC%2BD2MXhtlSrurnJ

    Article  PubMed  CAS  Google Scholar 

  • EA Verderio C Gaudry S Gross C Smith S Downes M Griffin (1999) ArticleTitleRegulation of cell surface tissue transglutaminase: effects on matrix storage of latent transforming growth factor-beta binding protein-1 J Histochem Cytochem 47 1417–1432 Occurrence Handle10544215 Occurrence Handle1:CAS:528:DyaK1MXntlyktbo%3D

    PubMed  CAS  Google Scholar 

  • EA Verderio B Nicholas S Gross M Griffin (1998) ArticleTitleRegulated expression of tissue transglutaminase in Swiss 3t3 fibroblasts: effects on the processing of fibronectin cell attachment and cell death Exp Cell Res 239 119–138 Occurrence Handle9511731 Occurrence Handle10.1006/excr.1997.3874 Occurrence Handle1:CAS:528:DyaK1cXhs1yqt70%3D

    Article  PubMed  CAS  Google Scholar 

  • EA Verderio D Telci A Okoye G Melino M Griffin (2003) ArticleTitleA novel RGD-independent cell adhesion pathway mediated by fibronectin-bound tissue transglutaminase rescues cells from anoikis J Biol Chem 278 42604–42614 Occurrence Handle12732629 Occurrence Handle10.1074/jbc.M303303200 Occurrence Handle1:CAS:528:DC%2BD3sXot1alsLw%3D

    Article  PubMed  CAS  Google Scholar 

  • L Xu S Begun JD Heran RO Hynes (2006) ArticleTitleGPR 56, an atypical G protein receptor, binds tissue transglutaminase, TG2, and inhibits melanoma tumor growth and metastasis Proc Natl Acad Sci USA 103 9023–9028 Occurrence Handle16757564 Occurrence Handle10.1073/pnas.0602681103 Occurrence Handle1:CAS:528:DC%2BD28XmsVWjs78%3D

    Article  PubMed  CAS  Google Scholar 

  • L Yuan K Choi C Khosla X Zheng R Higashikubo MR Chicoine KM Rich (2005) ArticleTitleTissue transglutaminase 2 inhibition promotes cell death and chemosensitivity in glioblastomas Mol Cancer Ther 4 1293–1302 Occurrence Handle16170020 Occurrence Handle10.1158/1535-7163.MCT-04-0328 Occurrence Handle1:CAS:528:DC%2BD2MXhtVKnt7jJ

    Article  PubMed  CAS  Google Scholar 

  • M Ziche L Morbidelli R Choudhuri HT Zhang S Donnini HJ Granger R Bicknell (1997) ArticleTitleNitric oxide synthase lies downstream from vascular endothelial growth factor-induced but not basic growth factor-induced angiogenesis J Clin Invest 99 2625–2634 Occurrence Handle9169492 Occurrence Handle1:CAS:528:DyaK2sXjs1Knurs%3D Occurrence Handle10.1172/JCI119451

    Article  PubMed  CAS  Google Scholar 

  • KA Zirvi JP Keogh A Slomiany (1993) ArticleTitleEffects of exogenous transglutaminase on spreading of human colorectal-carcinoma cells Cancer Biochem Biophys 13 283–294 Occurrence Handle8521378 Occurrence Handle1:CAS:528:DyaK2cXitFeqsbo%3D

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Unilever R&D Port Sunlight, Bebington, Wirral, U.K.

    P. Kotsakis

  2. School of Life and Health Sciences, Aston University, Aston Triangle, Birmingham, U.K.

    M. Griffin

Authors
  1. P. Kotsakis
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. Griffin
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kotsakis, P., Griffin, M. Tissue transglutaminase in tumour progression: friend or foe?. Amino Acids 33, 373–384 (2007). https://doi.org/10.1007/s00726-007-0516-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00726-007-0516-1

Search

Navigation