Skip to main content
SpringerLink
Log in
Book cover

Transglutaminases pp 43–62Cite as

Control of TG Functions Depending on Their Localization

  • Chapter
  • First Online:

Abstract

One of the unique characteristics of the transglutaminase (TG) family enzymes is multiple distribution of the members. It is known that TGs exist in the cytosol, plasma membrane, nucleus, and mitochondria, as well as outside cells, being associated with the extracellular matrix and being secreted into tissue fluids or blood circulation. Depending on where TGs locate, their molecular conformation is altered, and they exert multiple biological activities. Furthermore, their localization and thus their activities are changed in pathological situations, which is highly associated with progression of many diseases, including thrombotic disease, immune diseases including celiac disease, skin diseases, neurodegenerative diseases, hepatic diseases, fibrotic diseases and cancers.

This chapter summarizes information on distribution of TGs in various intracellular compartments and extracellular milieus, control of the activity of TGs depending on where they are, and molecular mechanisms by which TGs localize to specific compartments.

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

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Aeschlimann D, Paulsson M (1991) Cross-linking of laminin-nidogen complexes by tissue transglutaminase. A novel mechanism for basement membrane stabilization. J Biol Chem 266(23):15308–15317

    CAS  PubMed  Google Scholar 

  • Agah A, Kyriakides TR, Bornstein P (2005) Proteolysis of cell-surface tissue transglutaminase by matrix metalloproteinase-2 contributes to the adhesive defect and matrix abnormalities in thrombospondin-2-null fibroblasts and mice. Am J Pathol 167(1):81–88. doi:10.1016/s0002-9440(10)62955-0

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Akimov SS, Belkin AM (2001) Cell surface tissue transglutaminase is involved in adhesion and migration of monocytic cells on fibronectin. Blood 98(5):1567–1576

    Article  CAS  PubMed  Google Scholar 

  • Akimov SS, Krylov D, Fleischman LF, Belkin AM (2000) Tissue transglutaminase is an integrin-binding adhesion coreceptor for fibronectin. J Cell Biol 148(4):825–838

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Al-Jallad HF, Myneni VD, Piercy-Kotb SA, Chabot N, Mulani A, Keillor JW, Kaartinen MT (2011) Plasma membrane factor XIIIA transglutaminase activity regulates osteoblast matrix secretion and deposition by affecting microtubule dynamics. PLoS One 6(1):e15893. doi:10.1371/journal.pone.0015893

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ando Y, Imamura S, Owada MK, Kannagi R (1991) Calcium-induced intracellular cross-linking of lipocortin I by tissue transglutaminase in A431 cells. Augmentation by membrane phospholipids. J Biol Chem 266(2):1101–1108

    CAS  PubMed  Google Scholar 

  • Balajthy Z, Csomos K, Vamosi G, Szanto A, Lanotte M, Fesus L (2006) Tissue-transglutaminase contributes to neutrophil granulocyte differentiation and functions. Blood 108(6):2045–2054. doi:10.1182/blood-2004-02-007948

    Article  CAS  PubMed  Google Scholar 

  • Ballestar E, Abad C, Franco L (1996) Core histones are glutaminyl substrates for tissue transglutaminase. J Biol Chem 271(31):18817–18824

    Article  CAS  PubMed  Google Scholar 

  • Baranger K, Zani ML, Labas V, Dallet-Choisy S, Moreau T (2011) Secretory leukocyte protease inhibitor (SLPI) is, like its homologue trappin-2 (pre-elafin), a transglutaminase substrate. PLoS One 6(6):e20976. doi:10.1371/journal.pone.0020976

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Baumgartner W, Weth A (2007) Transglutaminase 1 stabilizes beta-actin in endothelial cells correlating with a stabilization of intercellular junctions. J Vasc Res 44(3):234–240. doi:10.1159/000100422

    Article  CAS  PubMed  Google Scholar 

  • Baumgartner W, Golenhofen N, Weth A, Hiiragi T, Saint R, Griffin M, Drenckhahn D (2004) Role of transglutaminase 1 in stabilisation of intercellular junctions of the vascular endothelium. Histochem Cell Biol 122(1):17–25. doi:10.1007/s00418-004-0668-y

    Article  CAS  PubMed  Google Scholar 

  • Behrendt N, Ronne E, Dano K (1993) A novel, specific pro-urokinase complex on monocyte-like cells, detected by transglutaminase-catalyzed cross-linking. FEBS Lett 336(3):394–396

    Article  CAS  PubMed  Google Scholar 

  • Belkin AM, Zemskov EA, Hang J, Akimov SS, Sikora S, Strongin AY (2004) Cell-surface-associated tissue transglutaminase is a target of MMP-2 proteolysis. Biochemistry 43(37):11760–11769. doi:10.1021/bi049266z

    Article  CAS  PubMed  Google Scholar 

  • Belkin AM, Tsurupa G, Zemskov E, Veklich Y, Weisel JW, Medved L (2005) Transglutaminase-mediated oligomerization of the fibrin(ogen) alphaC domains promotes integrin-dependent cell adhesion and signaling. Blood 105(9):3561–3568. doi:10.1182/blood-2004-10-4089

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bendixen E, Harpel PC, Sottrup-Jensen L (1995) Location of the major epsilon-(gamma-glutamyl)lysyl cross-linking site in transglutaminase-modified human plasminogen. J Biol Chem 270(30):17929–17933

    Article  CAS  PubMed  Google Scholar 

  • Boroughs LK, Antonyak MA, Johnson JL, Cerione RA (2011) A unique role for heat shock protein 70 and its binding partner tissue transglutaminase in cancer cell migration. J Biol Chem 286(43):37094–37107. doi:10.1074/jbc.M111.242438

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bruce SE, Peters TJ (1983) The subcellular localization of transglutaminase in normal liver and in glucagon-treated and partial hepatectomized rats. Biosci Rep 3(12):1085–1090

    Article  CAS  PubMed  Google Scholar 

  • Candi E, Oddi S, Terrinoni A, Paradisi A, Ranalli M, Finazzi-Agro A, Melino G (2001) Transglutaminase 5 cross-links loricrin, involucrin, and small proline-rich proteins in vitro. J Biol Chem 276(37):35014–35023. doi:10.1074/jbc.M010157200

    Article  CAS  PubMed  Google Scholar 

  • Cho SY, Lee JH, Bae HD, Jeong EM, Jang GY, Kim CW, Shin DM, Jeon JH, Kim IG (2010) Transglutaminase 2 inhibits apoptosis induced by calcium- overload through down-regulation of BAX. Exp Mol Med 42(9):639–650. doi:10.3858/emm.2010.42.9.063

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chou CY, Streets AJ, Watson PF, Huang L, Verderio EA, Johnson TS (2011) A crucial sequence for transglutaminase type 2 extracellular trafficking in renal tubular epithelial cells lies in its N-terminal beta-sandwich domain. J Biol Chem 286(31):27825–27835. doi:10.1074/jbc.M111.226340

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Clegg JS (1984) Properties and metabolism of the aqueous cytoplasm and its boundaries. Am J Physiol 246(2 Pt 2):R133–R151

    CAS  PubMed  Google Scholar 

  • D’Eletto M, Farrace MG, Falasca L, Reali V, Oliverio S, Melino G, Griffin M, Fimia GM, Piacentini M (2009) Transglutaminase 2 is involved in autophagosome maturation. Autophagy 5(8):1145–1154

    Article  PubMed  Google Scholar 

  • Dardik R, Inbal A (2006) Complex formation between tissue transglutaminase II (tTG) and vascular endothelial growth factor receptor 2 (VEGFR-2): proposed mechanism for modulation of endothelial cell response to VEGF. Exp Cell Res 312(16):2973–2982. doi:10.1016/j.yexcr.2006.05.019

    Article  CAS  PubMed  Google Scholar 

  • Davies PJ, Davies DR, Levitzki A, Maxfield FR, Milhaud P, Willingham MC, Pastan IH (1980) Transglutaminase is essential in receptor-mediated endocytosis of alpha 2-macroglobulin and polypeptide hormones. Nature 283(5743):162–167

    Article  CAS  PubMed  Google Scholar 

  • Deasey S, Nurminsky D, Shanmugasundaram S, Lima F, Nurminskaya M (2013) Transglutaminase 2 as a novel activator of LRP6/beta-catenin signaling. Cell Signal 25(12):2646–2651. doi:10.1016/j.cellsig.2013.08.016

    Article  CAS  PubMed  Google Scholar 

  • Dedeoglu A, Kubilus JK, Jeitner TM, Matson SA, Bogdanov M, Kowall NW, Matson WR, Cooper AJ, Ratan RR, Beal MF, Hersch SM, Ferrante RJ (2002) Therapeutic effects of cystamine in a murine model of Huntington’s disease. J Neurosci Off J Soc Neurosci 22(20):8942–8950

    CAS  Google Scholar 

  • Dolge L, Aufenvenne K, Traupe H, Baumgartner W (2012) Beta-actin is a target for transglutaminase activity at synaptic endings in chicken telencephalic cell cultures. J Mol Neurosci MN 46(2):410–419. doi:10.1007/s12031-011-9601-8

    Article  CAS  PubMed  Google Scholar 

  • Dudek SM, Johnson GV (1994) Transglutaminase facilitates the formation of polymers of the beta-amyloid peptide. Brain Res 651(1–2):129–133

    Article  CAS  PubMed  Google Scholar 

  • Faverman L, Mikhaylova L, Malmquist J, Nurminskaya M (2008) Extracellular transglutaminase 2 activates beta-catenin signaling in calcifying vascular smooth muscle cells. FEBS Lett 582(10):1552–1557. doi:10.1016/j.febslet.2008.03.053

    Article  CAS  PubMed  Google Scholar 

  • Faye C, Inforzato A, Bignon M, Hartmann DJ, Muller L, Ballut L, Olsen BR, Day AJ, Ricard-Blum S (2010) Transglutaminase-2: a new endostatin partner in the extracellular matrix of endothelial cells. Biochem J 427(3):467–475. doi:10.1042/bj20091594

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Festoff BW, SantaCruz K, Arnold PM, Sebastian CT, Davies PJ, Citron BA (2002) Injury-induced “switch” from GTP-regulated to novel GTP-independent isoform of tissue transglutaminase in the rat spinal cord. J Neurochem 81(4):708–718

    Article  CAS  PubMed  Google Scholar 

  • Filiano AJ, Tucholski J, Dolan PJ, Colak G, Johnson GV (2010) Transglutaminase 2 protects against ischemic stroke. Neurobiol Dis 39(3):334–343. doi:10.1016/j.nbd.2010.04.018

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fischer J, Koblyakova Y, Latendorf T, Wu Z, Meyer-Hoffert U (2013) Cross-linking of SPINK6 by transglutaminases protects from epidermal proteases. J Invest Dermatol 133(5):1170–1177. doi:10.1038/jid.2012.482

    Article  CAS  PubMed  Google Scholar 

  • Fisher M, Jones RA, Huang L, Haylor JL, El Nahas M, Griffin M, Johnson TS (2009) Modulation of tissue transglutaminase in tubular epithelial cells alters extracellular matrix levels: a potential mechanism of tissue scarring. Matrix Biol J Int Soc Matrix Biol 28(1):20–31. doi:10.1016/j.matbio.2008.10.003

    Article  CAS  Google Scholar 

  • Folk JE, Park MH, Chung SI, Schrode J, Lester EP, Cooper HL (1980) Polyamines as physiological substrates for transglutaminases. J Biol Chem 255(8):3695–3700

    CAS  PubMed  Google Scholar 

  • Furutani Y, Kato A, Fibriani A, Hirata T, Kawai R, Jeon JH, Fujii Y, Kim IG, Kojima S, Hirose S (2005) Identification, evolution, and regulation of expression of Guinea pig trappin with an unusually long transglutaminase substrate domain. J Biol Chem 280(21):20204–20215. doi:10.1074/jbc.M501678200

    Article  CAS  PubMed  Google Scholar 

  • Grenard P, Bresson-Hadni S, El Alaoui S, Chevallier M, Vuitton DA, Ricard-Blum S (2001) Transglutaminase-mediated cross-linking is involved in the stabilization of extracellular matrix in human liver fibrosis. J Hepatol 35(3):367–375

    Article  CAS  PubMed  Google Scholar 

  • Haddox MK, Russell DH (1981) Increased nuclear conjugated polyamines and transglutaminase during liver regeneration. Proc Natl Acad Sci U S A 78(3):1712–1716

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hamada K, Terauchi A, Nakamura K, Higo T, Nukina N, Matsumoto N, Hisatsune C, Nakamura T, Mikoshiba K (2014) Aberrant calcium signaling by transglutaminase-mediated posttranslational modification of inositol 1,4,5-trisphosphate receptors. Proc Natl Acad Sci U S A 111(38):E3966–E3975. doi:10.1073/pnas.1409730111

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hasegawa G, Suwa M, Ichikawa Y, Ohtsuka T, Kumagai S, Kikuchi M, Sato Y, Saito Y (2003) A novel function of tissue-type transglutaminase: protein disulphide isomerase. Biochem J 373(Pt 3):793–803. doi:10.1042/bj20021084

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hebert SS, Daviau A, Grondin G, Latreille M, Aubin RA, Blouin R (2000) The mixed lineage kinase DLK is oligomerized by tissue transglutaminase during apoptosis. J Biol Chem 275(42):32482–32490. doi:10.1074/jbc.M006528200

    Article  CAS  PubMed  Google Scholar 

  • Hiiragi T, Sasaki H, Nagafuchi A, Sabe H, Shen SC, Matsuki M, Yamanishi K, Tsukita S (1999) Transglutaminase type 1 and its cross-linking activity are concentrated at adherens junctions in simple epithelial cells. J Biol Chem 274(48):34148–34154

    Article  CAS  PubMed  Google Scholar 

  • Hitomi K, Presland RB, Nakayama T, Fleckman P, Dale BA, Maki M (2003) Analysis of epidermal-type transglutaminase (transglutaminase 3) in human stratified epithelia and cultured keratinocytes using monoclonal antibodies. J Dermatol Sci 32(2):95–103

    Article  CAS  PubMed  Google Scholar 

  • Ichinose A (2005) Extracellular transglutaminase: factor XIII. Prog Exp Tumor Res 38:192–208. doi:10.1159/000084241

    Article  CAS  PubMed  Google Scholar 

  • Jaovisidha K, Etim A, Yamakawa K, Masuda I, Gohr CM, Wakim BT, Boonapatcharoen N, Ninomiya J, Rosenthal AK (2006) The serine protease inhibitor trappin-2 is present in cartilage and synovial fluid in osteoarthritis. J Rheumatol 33(2):318–325

    CAS  PubMed  Google Scholar 

  • Jensen PH, Lorand L, Ebbesen P, Gliemann J (1993) Type-2 plasminogen-activator inhibitor is a substrate for trophoblast transglutaminase and factor XIIIa. Transglutaminase-catalyzed cross-linking to cellular and extracellular structures. Eur J Biochem/FEBS 214(1):141–146

    Article  CAS  Google Scholar 

  • Jiang WG, Ye L, Sanders AJ, Ruge F, Kynaston HG, Ablin RJ, Mason MD (2013) Prostate transglutaminase (TGase-4, TGaseP) enhances the adhesion of prostate cancer cells to extracellular matrix, the potential role of TGase-core domain. J Transl Med 11:269. doi:10.1186/1479-5876-11-269

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Johnson KA, Terkeltaub RA (2005) External GTP-bound transglutaminase 2 is a molecular switch for chondrocyte hypertrophic differentiation and calcification. J Biol Chem 280(15):15004–15012. doi:10.1074/jbc.M500962200

    Article  CAS  PubMed  Google Scholar 

  • Kaartinen MT, El-Maadawy S, Rasanen NH, McKee MD (2002) Tissue transglutaminase and its substrates in bone. J Bone Miner Res Off J Am Soc Bone Miner Res 17(12):2161–2173. doi:10.1359/jbmr.2002.17.12.2161

    Article  CAS  Google Scholar 

  • Karpuj MV, Garren H, Slunt H, Price DL, Gusella J, Becher MW, Steinman L (1999) Transglutaminase aggregates huntingtin into nonamyloidogenic polymers, and its enzymatic activity increases in Huntington’s disease brain nuclei. Proc Natl Acad Sci U S A 96(13):7388–7393

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kim SY, Grant P, Lee JH, Pant HC, Steinert PM (1999) Differential expression of multiple transglutaminases in human brain. Increased expression and cross-linking by transglutaminases 1 and 2 in Alzheimer’s disease. J Biol Chem 274(43):30715–30721

    Article  CAS  PubMed  Google Scholar 

  • Kim DS, Park SS, Nam BH, Kim IH, Kim SY (2006) Reversal of drug resistance in breast cancer cells by transglutaminase 2 inhibition and nuclear factor-kappaB inactivation. Cancer Res 66(22):10936–10943. doi:10.1158/0008-5472.can-06-1521

    Article  CAS  PubMed  Google Scholar 

  • Kojima S, Muramatsu H, Amanuma H, Muramatsu T (1995) Midkine enhances fibrinolytic activity of bovine endothelial cells. J Biol Chem 270(16):9590–9596

    Article  CAS  PubMed  Google Scholar 

  • Kuo TF, Tatsukawa H, Kojima S (2011) New insights into the functions and localization of nuclear transglutaminase 2. FEBS J 278(24):4756–4767. doi:10.1111/j.1742-4658.2011.08409.x

    Article  CAS  PubMed  Google Scholar 

  • Kuo TF, Tatsukawa H, Matsuura T, Nagatsuma K, Hirose S, Kojima S (2012) Free fatty acids induce transglutaminase 2-dependent apoptosis in hepatocytes via ER stress-stimulated PERK pathways. J Cell Physiol 227(3):1130–1137. doi:10.1002/jcp.22833

    Article  CAS  PubMed  Google Scholar 

  • Le M, Gohr CM, Rosenthal AK (2001) Transglutaminase participates in the incorporation of latent TGFbeta into the extracellular matrix of aging articular chondrocytes. Connect Tissue Res 42(4):245–253

    Article  CAS  PubMed  Google Scholar 

  • Lee J, Kim YS, Choi DH, Bang MS, Han TR, Joh TH, Kim SY (2004) Transglutaminase 2 induces nuclear factor-kappaB activation via a novel pathway in BV-2 microglia. J Biol Chem 279(51):53725–53735. doi:10.1074/jbc.M407627200

    Article  CAS  PubMed  Google Scholar 

  • Mahoney SA, Wilkinson M, Smith S, Haynes LW (2000) Stabilization of neurites in cerebellar granule cells by transglutaminase activity: identification of midkine and galectin-3 as substrates. Neuroscience 101(1):141–155

    Article  CAS  PubMed  Google Scholar 

  • Milakovic T, Tucholski J, McCoy E, Johnson GV (2004) Intracellular localization and activity state of tissue transglutaminase differentially impacts cell death. J Biol Chem 279(10):8715–8722. doi:10.1074/jbc.M308479200

    Article  CAS  PubMed  Google Scholar 

  • Mishra S, Murphy LJ (2004) Tissue transglutaminase has intrinsic kinase activity: identification of transglutaminase 2 as an insulin-like growth factor-binding protein-3 kinase. J Biol Chem 279(23):23863–23868. doi:10.1074/jbc.M311919200

    Article  CAS  PubMed  Google Scholar 

  • Mishra S, Saleh A, Espino PS, Davie JR, Murphy LJ (2006) Phosphorylation of histones by tissue transglutaminase. J Biol Chem 281(9):5532–5538. doi:10.1074/jbc.M506864200

    Article  CAS  PubMed  Google Scholar 

  • Nadella V, Wang Z, Johnson TS, Griffin M, Devitt A (2015) Transglutaminase 2 interacts with syndecan-4 and CD44 at the surface of human macrophages to promote removal of apoptotic cells. Biochim Biophys Acta 1853(1):201–212. doi:10.1016/j.bbamcr.2014.09.020

    Article  CAS  PubMed  Google Scholar 

  • Nakaoka H, Perez DM, Baek KJ, Das T, Husain A, Misono K, Im MJ, Graham RM (1994) Gh: a GTP-binding protein with transglutaminase activity and receptor signaling function. Science (New York, NY) 264(5165):1593–1596

    Article  CAS  Google Scholar 

  • Nara K, Aoyama Y, Iwata T, Hagiwara H, Hirose S (1992) Cell cycle-dependent changes in tissue transglutaminase mRNA levels in bovine endothelial cells. Biochem Biophys Res Commun 187(1):14–17

    Article  CAS  PubMed  Google Scholar 

  • Nemes Z, Marekov LN, Fesus L, Steinert PM (1999a) A novel function for transglutaminase 1: attachment of long-chain omega-hydroxyceramides to involucrin by ester bond formation. Proc Natl Acad Sci U S A 96(15):8402–8407

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nemes Z, Marekov LN, Steinert PM (1999b) Involucrin cross-linking by transglutaminase 1. Binding to membranes directs residue specificity. J Biol Chem 274(16):11013–11021

    Article  CAS  PubMed  Google Scholar 

  • Nemes Z, Petrovski G, Aerts M, Sergeant K, Devreese B, Fesus L (2009) Transglutaminase-mediated intramolecular cross-linking of membrane-bound alpha-synuclein promotes amyloid formation in Lewy bodies. J Biol Chem 284(40):27252–27264. doi:10.1074/jbc.M109.033969

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nunes I, Gleizes PE, Metz CN, Rifkin DB (1997) Latent transforming growth factor-beta binding protein domains involved in activation and transglutaminase-dependent cross-linking of latent transforming growth factor-beta. J Cell Biol 136(5):1151–1163

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nunomura K, Kawakami S, Shimizu T, Hara T, Nakamura K, Terakawa Y, Yamasaki A, Ikegami S (2003) In vivo cross-linking of nucleosomal histones catalyzed by nuclear transglutaminase in starfish sperm and its induction by egg jelly triggering the acrosome reaction. Eur J Biochem/FEBS 270(18):3750–3759

    Article  CAS  Google Scholar 

  • Ohba H, Harano T, Omura T (1981) Intracellular and intramembranous localization of a protein disulfide isomerase in rat liver. J Biochem 89(3):889–900

    CAS  PubMed  Google Scholar 

  • Pavlyukov MS, Antipova NV, Balashova MV, Shakhparonov MI (2012) Detection of Transglutaminase 2 conformational changes in living cell. Biochem Biophys Res Commun 421(4):773–779. doi:10.1016/j.bbrc.2012.04.082

    Article  CAS  PubMed  Google Scholar 

  • Pfundt R, van Ruissen F, van Vlijmen-Willems IM, Alkemade HA, Zeeuwen PL, Jap PH, Dijkman H, Fransen J, Croes H, van Erp PE, Schalkwijk J (1996) Constitutive and inducible expression of SKALP/elafin provides anti-elastase defense in human epithelia. J Clin Invest 98(6):1389–1399. doi:10.1172/jci118926

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Piacentini M, Farrace MG, Piredda L, Matarrese P, Ciccosanti F, Falasca L, Rodolfo C, Giammarioli AM, Verderio E, Griffin M, Malorni W (2002) Transglutaminase overexpression sensitizes neuronal cell lines to apoptosis by increasing mitochondrial membrane potential and cellular oxidative stress. J Neurochem 81(5):1061–1072

    Article  CAS  PubMed  Google Scholar 

  • Pinkas DM, Strop P, Brunger AT, Khosla C (2007) Transglutaminase 2 undergoes a large conformational change upon activation. PLoS Biol 5(12):e327. doi:10.1371/journal.pbio.0050327

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Ponnusamy M, Pang M, Annamaraju PK, Zhang Z, Gong R, Chin YE, Zhuang S (2009) Transglutaminase-1 protects renal epithelial cells from hydrogen peroxide-induced apoptosis through activation of STAT3 and AKT signaling pathways. Am J Physiol Renal Physiol 297(5):F1361–F1370. doi:10.1152/ajprenal.00251.2009

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Popov Y, Sverdlov DY, Sharma AK, Bhaskar KR, Li S, Freitag TL, Lee J, Dieterich W, Melino G, Schuppan D (2011) Tissue transglutaminase does not affect fibrotic matrix stability or regression of liver fibrosis in mice. Gastroenterology 140(5):1642–1652. doi:10.1053/j.gastro.2011.01.040

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Priglinger SG, Alge CS, Neubauer AS, Kristin N, Hirneiss C, Eibl K, Kampik A, Welge-Lussen U (2004) TGF-beta2-induced cell surface tissue transglutaminase increases adhesion and migration of RPE cells on fibronectin through the gelatin-binding domain. Invest Ophthalmol Vis Sci 45(3):955–963

    Article  PubMed  Google Scholar 

  • Robinson NA, Eckert RL (1998) Identification of transglutaminase-reactive residues in S100A11. J Biol Chem 273(5):2721–2728

    Article  CAS  PubMed  Google Scholar 

  • Robinson NJ, Baker PN, Jones CJ, Aplin JD (2007) A role for tissue transglutaminase in stabilization of membrane-cytoskeletal particles shed from the human placenta. Biol Reprod 77(4):648–657. doi:10.1095/biolreprod.107.061747

    Article  CAS  PubMed  Google Scholar 

  • Rodolfo C, Mormone E, Matarrese P, Ciccosanti F, Farrace MG, Garofano E, Piredda L, Fimia GM, Malorni W, Piacentini M (2004) Tissue transglutaminase is a multifunctional BH3-only protein. J Biol Chem 279(52):54783–54792. doi:10.1074/jbc.M410938200

    Article  CAS  PubMed  Google Scholar 

  • Rossin F, D’Eletto M, Falasca L, Sepe S, Cocco S, Fimia GM, Campanella M, Mastroberardino PG, Farrace MG, Piacentini M (2015) Transglutaminase 2 ablation leads to mitophagy impairment associated with a metabolic shift towards aerobic glycolysis. Cell Death Differ 22(3):408–418. doi:10.1038/cdd.2014.106

    Article  CAS  PubMed  Google Scholar 

  • Saber-Lichtenberg Y, Brix K, Schmitz A, Heuser JE, Wilson JH, Lorand L, Herzog V (2000) Covalent cross-linking of secreted bovine thyroglobulin by transglutaminase. FASEB J Off Publ Fed Am Soc Exp Biol 14(7):1005–1014

    CAS  Google Scholar 

  • Sane DC, Moser TL, Pippen AM, Parker CJ, Achyuthan KE, Greenberg CS (1988) Vitronectin is a substrate for transglutaminases. Biochem Biophys Res Commun 157(1):115–120

    Article  CAS  PubMed  Google Scholar 

  • Serrano K, Devine DV (2002) Intracellular factor XIII crosslinks platelet cytoskeletal elements upon platelet activation. Thromb Haemost 88(2):315–320

    CAS  PubMed  Google Scholar 

  • Shibata T, Sekihara S, Fujikawa T, Miyaji R, Maki K, Ishihara T, Koshiba T, Kawabata S (2013) Transglutaminase-catalyzed protein-protein cross-linking suppresses the activity of the NF-kappaB-like transcription factor relish. Sci Signal 6(285):ra61. doi:10.1126/scisignal.2003970

    Article  PubMed  CAS  Google Scholar 

  • Shrestha R, Tatsukawa H, Shrestha R, Ishibashi N, Matsuura T, Kagechika H, Kose S, Hitomi K, Imamoto N, Kojima S (2015) Molecular mechanism by which acyclic retinoid induces nuclear localization of transglutaminase 2 in human hepatocellular carcinoma cells. Cell Death Dis. doi:10.1038/cddis.2015.339 (in press)

  • Shweke N, Boulos N, Jouanneau C, Vandermeersch S, Melino G, Dussaule JC, Chatziantoniou C, Ronco P, Boffa JJ (2008) Tissue transglutaminase contributes to interstitial renal fibrosis by favoring accumulation of fibrillar collagen through TGF-beta activation and cell infiltration. Am J Pathol 173(3):631–642. doi:10.2353/ajpath.2008.080025

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Siegel M, Strnad P, Watts RE, Choi K, Jabri B, Omary MB, Khosla C (2008) Extracellular transglutaminase 2 is catalytically inactive, but is transiently activated upon tissue injury. PLoS One 3(3):e1861. doi:10.1371/journal.pone.0001861

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Singh US, Erickson JW, Cerione RA (1995) Identification and biochemical characterization of an 80 kilodalton GTP-binding/transglutaminase from rabbit liver nuclei. Biochemistry 34(48):15863–15871

    Article  CAS  PubMed  Google Scholar 

  • Song Y, Kirkpatrick LL, Schilling AB, Helseth DL, Chabot N, Keillor JW, Johnson GV, Brady ST (2013) Transglutaminase and polyamination of tubulin: posttranslational modification for stabilizing axonal microtubules. Neuron 78(1):109–123. doi:10.1016/j.neuron.2013.01.036

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Staab JF, Bradway SD, Fidel PL, Sundstrom P (1999) Adhesive and mammalian transglutaminase substrate properties of Candida albicans Hwp1. Science 283(5407):1535–1538

    Article  CAS  PubMed  Google Scholar 

  • Steinert PM, Marekov LN (1995) The proteins elafin, filaggrin, keratin intermediate filaments, loricrin, and small proline-rich proteins 1 and 2 are isodipeptide cross-linked components of the human epidermal cornified cell envelope. J Biol Chem 270(30):17702–17711

    Article  CAS  PubMed  Google Scholar 

  • Tatsukawa H, Fukaya Y, Frampton G, Martinez-Fuentes A, Suzuki K, Kuo TF, Nagatsuma K, Shimokado K, Okuno M, Wu J, Iismaa S, Matsuura T, Tsukamoto H, Zern MA, Graham RM, Kojima S (2009) Role of transglutaminase 2 in liver injury via cross-linking and silencing of transcription factor Sp1. Gastroenterology 136(5):1783–1795, e1710. doi:10.1053/j.gastro.2009.01.007

    Article  CAS  PubMed  Google Scholar 

  • Tseng HC, Tang JB, Gandhi PS, Luo CW, Ou CM, Tseng CJ, Lin HJ, Chen YH (2012) Mutual adaptation between mouse transglutaminase 4 and its native substrates in the formation of copulatory plug. Amino Acids 42(2–3):951–960. doi:10.1007/s00726-011-1009-9

    Article  CAS  PubMed  Google Scholar 

  • van den Akker J, VanBavel E, van Geel R, Matlung HL, Guvenc Tuna B, Janssen GM, van Veelen PA, Boelens WC, De Mey JG, Bakker EN (2011) The redox state of transglutaminase 2 controls arterial remodeling. PLoS One 6(8):e23067. doi:10.1371/journal.pone.0023067

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Verderio E, Gaudry C, Gross S, Smith C, Downes S, Griffin M (1999) Regulation of cell surface tissue transglutaminase: effects on matrix storage of latent transforming growth factor-beta binding protein-1. J Histochem Cytochem Off J Histochem Soc 47(11):1417–1432

    Article  CAS  Google Scholar 

  • Verderio EA, Telci D, Okoye A, Melino G, Griffin M (2003) A novel RGD-independent cel adhesion pathway mediated by fibronectin-bound tissue transglutaminase rescues cells from anoikis. J Biol Chem 278(43):42604–42614. doi:10.1074/jbc.M303303200

    Article  CAS  PubMed  Google Scholar 

  • Vig PJ, Wei J, Shao Q, Hebert MD, Subramony SH, Sutton LT (2007) Role of tissue transglutaminase type 2 in calbindin-D28k interaction with ataxin-1. Neurosci Lett 420(1):53–57. doi:10.1016/j.neulet.2007.04.005

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang Z, Telci D, Griffin M (2011) Importance of syndecan-4 and syndecan −2 in osteoblast cell adhesion and survival mediated by a tissue transglutaminase-fibronectin complex. Exp Cell Res 317(3):367–381. doi:10.1016/j.yexcr.2010.10.015

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Collighan RJ, Pytel K, Rathbone DL, Li X, Griffin M (2012) Characterization of heparin-binding site of tissue transglutaminase: its importance in cell surface targeting, matrix deposition, and cell signaling. J Biol Chem 287(16):13063–13083. doi:10.1074/jbc.M111.294819

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang Z, Perez M, Caja S, Melino G, Johnson TS, Lindfors K, Griffin M (2013) A novel extracellular role for tissue transglutaminase in matrix-bound VEGF-mediated angiogenesis. Cell Death Dis 4:e808. doi:10.1038/cddis.2013.318

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang L, Uhlig PC, Eikenberry EF, Robenek H, Bruckner P, Hansen U (2014) Lateral growth limitation of corneal fibrils and their lamellar stacking depend on covalent collagen cross-linking by transglutaminase-2 and lysyl oxidases, respectively. J Biol Chem 289(2):921–929. doi:10.1074/jbc.M113.496364

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yoo JO, Lim YC, Kim YM, Ha KS (2012) Transglutaminase 2 promotes both caspase-dependent and caspase-independent apoptotic cell death via the calpain/BAX protein signaling pathway. J Biol Chem 287(18):14377–14388. doi:10.1074/jbc.M111.326074

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zemskov EA, Mikhailenko I, Hsia RC, Zaritskaya L, Belkin AM (2011) Unconventional secretion of tissue transglutaminase involves phospholipid-dependent delivery into recycling endosomes. PLoS One 6(4):e19414. doi:10.1371/journal.pone.0019414

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Micro-Signaling Regulation Technology Unit, RIKEN Center for Life Science Technologies, 2-1 Hirosawa, Wako, Saitama, 351-0198, Japan

    Yutaka Furutani Ph.D. & Soichi Kojima Ph.D.

Authors
  1. Yutaka Furutani Ph.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Soichi Kojima Ph.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Soichi Kojima Ph.D. .

Editor information

Editors and Affiliations

  1. Grad Sch of Pharmaceutical Sciences, Nagoya University, Nagoya, Aichi, Japan

    Kiyotaka Hitomi

  2. Micro-Signaling Regulation Technol. Unit, RIKEN Center for Life Sci. Technologies, Wako, Saitama, Japan

    Soichi Kojima

  3. Dept. Biochemistry and Molecular Biology, University of Debrecen, Debrecen, Hungary

    Laszlo Fesus

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer Japan

About this chapter

Cite this chapter

Furutani, Y., Kojima, S. (2015). Control of TG Functions Depending on Their Localization. In: Hitomi, K., Kojima, S., Fesus, L. (eds) Transglutaminases. Springer, Tokyo. https://doi.org/10.1007/978-4-431-55825-5_2

Download citation

Publish with us

Policies and ethics

Search

Navigation