TG2 transamidating activity acts as a reostat controlling the interplay between apoptosis and autophagy

Amino Acids

Volumn 42, Issue 5, 2012, Pages 1793-1802

  Rossin, Federica ^a   D'Eletto, Manuela ^a   MacDonald, Douglas ^c   Farrace, Maria Grazia ^a   Piacentini, Mauro ^a,b  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

^b NATIONAL INSTITUTE FOR INFECTIOUS DISEASES L SPALLANZANI   (Italy)

^c CHDI MANAGEMENT CHDI FOUNDATION   (United States)

Author keywords

Apoptosis; Autophagy; Transamidating activity; Transglutaminase 2

Indexed keywords

CASPASE 3; ISOENZYME; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 2;

ANIMAL CELL; APOPTOSIS; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CATALYSIS; CELL IMMORTALIZATION; CELL PROTECTION; EMBRYO; ENZYME ACTIVITY; FIBROBLAST; GENE INACTIVATION; MOUSE; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; WILD TYPE;

ANIMALS; APOPTOSIS; AUTOPHAGY; CASPASE 3; CELLS, CULTURED; FIBROBLASTS; GENE EXPRESSION; MICE; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS; MUTANT PROTEINS; POLY(ADP-RIBOSE) POLYMERASES; TRANSFECTION; TRANSGLUTAMINASES;

MUS;

EID: 84862771829     PISSN: 09394451     EISSN: 14382199     Source Type: Journal    
DOI: 10.1007/s00726-011-0899-x     Document Type: Article

References (47)

1. Antonyak MA, Jansen JM, Miller AM, Ly TK, Endo M, Cerione RA (2006) Two isoforms of tissue transglutaminase mediate opposing cellular fates. Proc Natl Acad Sci USA 103:18609-18614 (Pubitemid 44913458)
2. Cao L, Petrusca DN, Satpathy M, Nakshatri H, Petrache I et al (2008) Tissue transglutaminase protects epithelial ovarian cancer cells from cisplatin-induced apoptosis by promoting cell survival signaling. Carcinogenesis 29:1893-1900
3. Collighan RJ, Griffin M (2009) Transglutaminase 2 cross-linking of matrix proteins: biological significance and medical applications. Amino Acids 36:659-670
4. 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 5:1145-1154
5. Datta S, Antonyak MA, Cerione RA (2007) GTP-binding-defective forms of tissue transglutaminase trigger cell death. Biochemistry 46:14819-14829 (Pubitemid 350308873)
6. 2+) and GTP binding on tissue transglutaminase tertiary structure. J Biol Chem 275:3915-3921 (Pubitemid 30094616)
7. Eisenberg-Lerner A, Bialik S, Simon HU, Kimchi A (2009) Life and death partners: apoptosis, autophagy and the cross-talk between them. Cell Death Differ 16:966-975
8. Facchiano F, Facchiano A, Facchiano AM (2006) The role of transglutaminase-2 and its substrates in human diseases. Front Biosci 11:1758-1773 (Pubitemid 43253392)
9. Fesus L, Piacentini M (2002) Transglutaminase 2: an enigmatic enzyme with diverse functions. Trends Biochem Sci 27:534-539 (Pubitemid 35279599)
10. Fesus L, Szondy Z (2005) Transglutaminase 2 in the balance of cell death and survival. FEBS Lett 579:3297-3302 (Pubitemid 40804677)
11. Fesus L, Thomazy V, Autuori F, Ceru MP, Tarcsa E, Piacentini M (1989) Apoptotic hepatocytes become insoluble in detergents and chaotropic agents as a result of transglutaminase action. FEBS Lett 245:150-154 (Pubitemid 19076220)
12. Fimia GM, Piacentini M (2010) Regulation of autophagy in mammals and its interplay with apoptosis. Cell Mol Life Sci 67:1581-1588
13. Folk JE, Finlayson JS (1977) The epsilon-(gamma-glutamyl)lysine crosslink and the catalytic role of transglutaminases. Adv Protein Chem 31:1-133
14. Gaudry CA, Verderio E, Aeschlimann D, Cox A, Smith C, Griffin M (1999) Cell surface localization of tissue transglutaminase is dependent on a fibronectin-binding site in its N-terminal betasandwich domain. J Biol Chem 274:30707-30714
15. 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 373:793-803 (Pubitemid 36981089)
16. Kahlem P, Green H, Djian P (1998) Transglutaminase as the agent of neurodegenerative diseases due to polyglutamine expansion. Pathol Biol (Paris) 46:681-682 (Pubitemid 29018198)
17. Klionsky DJ (2007) Autophagy: from phenomenology to molecular understanding in less than a decade. Nat Rev Mol Cell Biol 8:931-937 (Pubitemid 47622558)
18. Levine B, Kroemer G (2008) Autophagy in the pathogenesis of disease. Cell 132:27-42
19. Liu S, Cerione RA, Clardy J (2002) Structural basis for the guanine nucleotide-binding activity of tissue transglutaminase and its regulation of transamidation activity. Proc Natl Acad Sci USA 99:2743-2747 (Pubitemid 34240531)
20. Lorand L, Graham RM (2003) Transglutaminases: crosslinking enzymes with pleiotropic functions. Nat Rev Mol Cell Biol 4:140-156 (Pubitemid 36172696)
21. Luciani A, Villella VR, Esposito S, Brunetti-Pierri N, Medina DL, Settembre C, Gavina M, Raia V, Ballabio A, Maiuri L (2011) Cystic fibrosis: a disorder with defective autophagy. Autophagy 7:92-94
22. Maiuri MC, Le Toumelin G, Criollo A, Rain JC, Gautier F, Juin P, Tasdemir E, Pierron G, Troulinaki K, Tavernarakis N, Hickman JA, Geneste O, Kroemer G (2007a) Functional and physical interaction between Bcl-XL and a BH3-like domain in Beclin-1. EMBO J 26:2527-2539 (Pubitemid 46788315)
23. Maiuri MC, Zalckvar E, Kimchi A, Kroemer G (2007b) Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat Rev Mol Cell Biol 8:741-752 (Pubitemid 47312826)
24. Malorni W, Farrace MG, Rodolfo C, Piacentini M (2008) Type 2 transglutaminase in neurodegenerative diseases: the mitochondrial connection. Curr Pharm Des 14:278-288 (Pubitemid 351516872)
25. Malorni W, Farrace MG, Matarrese P, Tinari A, Ciarlo L, Mousavi- Shafaei P, D'Eletto M, Di Giacomo G, Melino G, Palmieri L, Rodolfo C, Piacentini M (2009) The adenine nucleotide translocator 1 acts as a type 2 transglutaminase substrate: implications for mitochondrial-dependent apoptosis. Cell Death Differ 16:1480-1492
26. Mastroberardino PG, Iannicola C, Nardacci R, Bernassola F, De Laurenzi V, Melino G, Moreno S, Pavone F, Oliverio S, Fesus L, Piacentini M (2002) Tissue' transglutaminase ablation reduces neuronal death and prolongs survival in a mouse model of Huntington's disease. Cell Death Differ 9:873-880 (Pubitemid 35023603)
27. Mastroberardino PG, Farrace MG, Viti I, Pavone F, Fimia GM, Melino G, Rodolfo C, Piacentini M (2006) "Tissue" transglutaminase contributes to the formation of disulphide bridges in proteins of mitochondrial respiratory complexes. Biochim Biophys Acta 1757:1357-1365 (Pubitemid 44442141)
28. Mehta K, Fok JY, Mangala LS (2006) Tissue transglutaminase: from biological glue to cell survival cues. Front Biosci 11:173-185 (Pubitemid 43253484)
29. Melino G, Piacentini M (1998) 'Tissue' transglutaminase in cell death: a downstream or a multifunctional upstream effector? FEBS Lett 430:59-63 (Pubitemid 28307032)
30. Mishra S, Murphy LJ (2004) Tissue transglutaminase has intrinsic kinase activity: identification of transglutaminase 2 as an insulinlike growth factor-binding protein-3 kinase. J Biol Chem 279:23863-23868 (Pubitemid 38725242)
31. 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 264:1593-1596
32. Oliverio S, Amendola A, Rodolfo C, Spinedi A, Piacentini M (1999) Inhibition of "tissue" transglutaminase increases cell survival by preventing apoptosis. J Biol Chem 274:34123-34128 (Pubitemid 129511748)
33. Park ES, Won JH, Han KJ, Suh PG, Ryu SH, Lee HS, Yun HY, Kwon NS, Baek KJ (1998) Phospholipase C-delta1 and oxytocin receptor signalling: evidence of its role as an effector. Biochem J 331:283-289 (Pubitemid 28163986)
34. Pedersen LC, Yee VC, Bishop PD, Le Trong I, Teller DC, Stenkamp RE (1994) Transglutaminase factor XIII uses proteinase-like catalytic triad to crosslink macromolecules. Protein Sci 3:1131-1135 (Pubitemid 24209910)
35. Piacentini M, Colizzi V (1999) Tissue transglutaminase: apoptosis versus autoimmunity. Immunol Today 20:130-134 (Pubitemid 29130342)
36. Piacentini M, Autuori F, Dini L, Farrace MG, Ghibelli L, Piredda L, Fesus L (1991) "Tissue" transglutaminase is specifically expressed in neonatal rat liver cells undergoing apoptosis upon epidermal growth factor-stimulation. Cell Tissue Res 263:227-235
37. 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 81:1061-1072 (Pubitemid 34809289)
38. 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 279:54783-54792 (Pubitemid 40053223)
39. Rubinsztein DC, Gestwicki JE, Murphy LO, Klionsky DJ (2007) Potential therapeutic applications of autophagy. Nat Rev Drug Discov 6:304-312 (Pubitemid 46505881)
40. Szondy Z, Mastroberardino PG, Varadi J, Farrace MG, Nagy N et al (2006) Tissue transglutaminase (TG2) protects cardiomyocytes against ischemia/reperfusion injury by regulating ATP synthesis. Cell Death Differ 13:1827-1829 (Pubitemid 44390867)
41. 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 crosslinking and silencing of transcription factor Sp1. Gastroenterology 136:1783-1795
42. Tucholski J, Johnson GV (2002) Tissue transglutaminase differentially modulates apoptosis in a stimuli-dependent manner. J Neurochem 81:780-791 (Pubitemid 34809306)
43. Vezza R, Habib A, FitzGerald GA (1999) Differential signaling by the thromboxane receptor isoforms via the novel GTP-binding protein, Gh. J Biol Chem 274:12774-12779
44. Yamaguchi H, Wang HG (2006) Tissue transglutaminase serves as an inhibitor of apoptosis by cross-linking caspase 3 in thapsigargintreated cells. Mol Cell Biol 26:569-579 (Pubitemid 43089769)
45. Yee VC, Pedersen LC, Le Trong I, Bishop PD, Stenkamp RE, Teller DC (1994) Three-dimensional structure of a transglutaminase: human blood coagulation factor XIII. Proc Natl Acad Sci USA 91:7296-7300 (Pubitemid 24226850)
46. Yousefi S, Perozzo R, Schmid I, Ziemiecki A, Schaffner T, Scapozza L, Brunner T, Simon HU (2006) Calpain-mediated cleavage of Atg5 switches autophagy to apoptosis. Nat Cell Biol 8:1124-1132 (Pubitemid 44473608)
47. Zhang J, Ney PA (2009) Role of BNIP3 and NIX in cell death, autophagy, and mitophagy. Cell Death Differ 7:939-946