Transglutaminase 2 contributes to apoptosis induction in jurkat t cells by modulating Ca2+ homeostasis via cross-linking RAP1GDS1

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Hsieh, Yu Fan ^a   Liu, Guang Yaw ^a   Lee, Yi Ju ^a   Yang, Jiann Jou ^a   Sándor, Katalin ^b   Sarang, Zsolt ^b   Bononi, Angela ^c   Pinton, Paolo ^c   Tretter, László ^d   Szondy, Zsuzsa ^b   Tsay, Gregory J ^a,e  

^a CHUNG SHAN MEDICAL UNIVERSITY   (Taiwan)

^b UNIVERSITY OF DEBRECEN   (Hungary)

^c UNIVERSITY OF FERRARA   (Italy)

^d SEMMELWEIS UNIVERSITY   (Hungary)

^e CHUNG SHAN MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANOSINE TRIPHOSPHATASE; INOSITOL TRISPHOSPHATE; MUTANT PROTEIN; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 2; RAP1,GTP GDP DISSOCIATION STIMULATOR 1; RYANODINE RECEPTOR; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CALCIUM HOMEOSTASIS; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL TYPE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENZYME LOCALIZATION; HUMAN; HUMAN CELL; LEUKEMIA CELL LINE; MITOCHONDRION; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; CALCIUM; CALCIUM SIGNALING; CELL LINE; ENDOPLASMIC RETICULUM; FIBROBLASTS; GENE EXPRESSION REGULATION; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HOMEOSTASIS; HUMANS; INOSITOL PHOSPHATES; ION TRANSPORT; JURKAT CELLS; MICE; MITOCHONDRIA; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; TRANSGLUTAMINASES;

EID: 84892624512     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0081516     Document Type: Article

References (44)

1. Folk JE, Chung SI (1985) Transglutaminases. Methods Enzymol 113: 358-375.
2. Fesus L, Piacentini M (2002) Transglutaminase 2: an enigmatic enzyme with diverse functions. Trends Biochem Sci 27: 534-539.
3. Rodolfo C, Mormone E, Matarrese P, Ciccosanti F, Farrace MG, et al. (2004) Tissue transglutaminase is a multifunctional BH3-only protein. J Biol Chem 279: 54783-54792.
4. Kerr JF, Wyllie AH, Currie AR (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26: 239-257.
5. Vaux DL (2011) Apoptogenic factors released from mitochondria. Biochem Biophys Acta 1813: 546-550.
6. Rizzuto R, Pinton P, Carrington W, Fay FS, Fogarty KE, et al. (1998) Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2+ responses. Science 280: 1763-1766.
7. Pinton P, Giorgi C, Siviero R, Zecchini E, Rizzuto R (2008) Calcium and apoptosis: ER-mitochondria Ca2+ transfer in the control of apoptosis. Oncogene 27: 6407-6418.
8. Szalai G, Krishnamurthy R, Hajnóczky G (1999) Apoptosis driven by IP(3)-linked mitochondrial calcium signals. EMBO J 18: 6349-6361.
9. 2+ concentration of the endoplasmic reticulum is a key determinant of ceramideinduced apoptosis: significance for the molecular mechanism of Bcl-2 action. EMBO J 20: 2690-2701.
10. Mendes CC, Gomes DA, Thompson M, Souto NC, Goes TS, et al. (2005) The type III inositol 1,4,5-trisphosphate receptor preferentially transmits apoptotic Ca2+ signals into mitochondria. J Biol Chem 280: 40892-40900.
11. Khan AA, Soloski MJ, Sharp AH, Schilling G, Sabatini DM, et al. (1996) Lymphocyte apoptosis: mediation by increased type 3 inositol 1,4,5-trisphosphate receptor. Science 273: 503-507.
12. Fesus L, Szondy Z (2005) Transglutaminase 2 in the balance of cell death and survival. FEBS Lett 579: 3297-3302.
13. Chhabra A, Verma A, Mehta K (2009) Tissue transglutaminase promotes or suppresses tumors depending on cell context. Anticancer Res 29: 1909-1919.
14. Szondy Z, Molnar P, Nemes Z, Boyiadzis M, Kedei N, et al. (1997) Differential expression of tissue transglutaminase during in vivo apoptosis of thymocytes induced via distinct signalling pathways. FEBS Lett 404: 307-313.
15. Garabuczi É, Kiss B, Felszeghy S, Tsay GJ, Fésüs L, et al. (2013) Retinoids produced by macrophages engulfing apoptotic cells contribute to the appearance of transglutaminase 2 in apoptotic thymocytes. Amino Acids 44: 235-244.
16. Amendola A, Gougeon ML, Poccia F, Bondurand A, Fesus L, et al. (1996) Induction of "tissue" transglutaminase in HIV pathogenesis: evidence for high rate of apoptosis of CD4+ T lymphocytes and accessory cells in lymphoid tissues. Proc Natl Acad Sci USA 93: 11057-11062.
17. Oliverio S, Amendola A, Di Sano F, Farrace MG, Fesus L, et al. (1997) Tissue transglutaminase-dependent posttranslational modification of the retinoblastoma gene product in promonocytic cells undergoing apoptosis. Mol Cell Biol 17: 6040-6048.
18. Mishra S, Murphy LJ (2006) The p53 oncoprotein is a substrate for tissue transglutaminase kinase activity. Biochem Biophys Res Commun 339: 726-730.
19. Hutchinson JP, Rittinger K, Eccleston JF (2000) Purification and characterization of guanine nucleotide dissociation stimulator protein. Methods Enzymol 325: 71-82.
20. Lee KN, Arnold SA, Birckbichler PJ, Patterson MK, Fraij BM, et al. (1993) Sitedirected mutagenesis of human tissue transglutaminase: Cys-277 is essential for transglutaminase activity but not for GTPase activity. Biochim Biophys Acta 1202: 1-6.
21. Wyllie AH (1980) Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature 284: 555-556.
22. Hoth M, Fanger CM, Lewis RS (1997) Mitochondrial regulation of storeoperated calcium signaling in T lymphocytes. J Cell Biol 137: 633-648.
23. Rogers TB, Inesi G, Wade R, Lederer WJ (1995) Use of thapsigargin to study Ca2+ homeostasis in cardiac cells. Biosci Rep 15: 341-349.
24. Taylor CW, Dale P (2012) Intracellular Ca(2+) channels - a growing community. Mol Cell Endocrinol 353: 21-28.
25. Boyer JL, Downes CP, Harden TK (1989) Kinetics of activation of phospholipase C by P2Y purinergic receptor agonists and guanine nucleotides. J Biol Chem 264:884-890.
26. Palade P, Dettbarn C, Alderson B, Volpe P (1989) Pharmacologic differentiation between inositol-1,4,5-trisphosphate-induced Ca2+ release and Ca2+ - or caffeine-induced Ca2+ release from intracellular membrane systems. Mol Pharmacol 36: 673-680.
27. Magnier C, Bredoux R, Kovacs T, Quarck R, Papp B, et al. (1994) Correlated expression of the 97 kDa sarcoendoplasmic reticulum Ca(2+)-ATPase and Rap1B in platelets and various cell lines. Biochem J 297: 343-350.
28. Holz GG (2004) Epac: A new cAMP-binding protein in support of glucagon-like peptide-1 receptor-mediated signal transduction in the pancreatic b-Cell. Diabetes 53: 5-13.
29. Schmidt M, Evellin S, Weernink PA, von Dorp F, Rehmann H, et al. (2001) A new phospholipase-C-calcium signalling pathway mediated by cyclic AMP and a Rap GTPase. Nat Cell Biol 3: 1020-1024.
30. Begg GE, Carrington L, Stokes PH, Matthews JM, Wouters MA, et al. (2006) Mechanism of allosteric regulation of transglutaminase 2 by GTP. Proc Natl Acad Sci USA 103: 19683-19688.
31. Csordás G, Renken C, Várnai P, Walter L, Weaver D, et al. (2006) Structural and functional features and significance of the physical linkage between ER and mitochondria. J Cell Biol 174: 915-921.
32. Patergnani S, Suski JM, Agnoletto C, Bononi A, Bonora M, et al. (2011) Calcium signaling around Mitochondria Associated Membranes (MAMs). Cell Commun Signal 9: 19.
33. Joseph SK, Hajnoczky G (2007) IP3 receptors in cell survival and apoptosis: Ca2+ release and beyond. Apoptosis 12: 951-968.
34. Melino G, Annicchiarico-Petruzzelli M, Piredda L, Candi E, Gentile V, et al. (1994) Tissue transglutaminase and apoptosis: sense and antisense transfection studies with human neuroblastoma cells. Mol Cell Biol 14: 6584-6596.
35. Flourakis M, Van Coppenolle F, Lehen'kyi V, Beck B, Skryma R, et al. (2006) Passive calcium leak via translocon is a first step for iPLA2-pathway regulated store operated channels activation. FASEB J 20: E409-416.
36. Singh US, Pan J, Kao YL, Joshi S, Young KL, et al. (2003) Tissue transglutaminase mediates activation of RhoA and MAP kinase pathways during retinoic acid-induced neuronal differentiation of SH-SY5Y cells. J Biol Chem 278: 391-399.
37. Yi SJ, Groffen J, Heisterkamp N (2009) Transglutaminase 2 regulates the GTPase-activating activity of Bcr. J Biol Chem 284: 35645-35651.
38. Király R, Demény M, Fésüs L (2011) Protein transamidation by transglutaminase 2 in cells: a disputed Ca2+-dependent action of a multifunctional protein. FEBS J 278:4717-4739.
39. Szondy Z, Mastroberardino PG, Váradi 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.
40. Bernassola F, Federici M, Corazzari M, Terrinoni A, Hribal ML, et al. (2002) Role of transglutaminase 2 in glucose tolerance: knockout mice studies and a putative mutation in a MODY patient. FASEB J 16: 1371-1378.
41. Maechler P, Wollheim CB (2001) Mitochondrial function in normal and diabetic beta-cells. Nature 414: 807-812.
42. D'Eletto M, Farrace MG, Falasca L, Reali V, Oliverio S, et al. (2009) Transglutaminase 2 is involved in autophagosome maturation. Autophagy 8: 1145-1154.
43. Smaili SS, Hsu YT, Carvalho AC, Rosenstock TR, Sharpe JC, et al. (2003) Mitochondria, calcium and pro-apoptotic proteins as mediators in cell death signaling. Braz J Med Biol Res 36: 183-190.
44. Wieckowski MR, Giorgi C, Lebiedzinska M, Duszynski J, Pinton P (2009) Isolation of mitochondria-associated membranes and mitochondria from animal tissues and cells. Naure Protoc 4: 1582-1590.