Transglutaminase 2 ablation leads to mitophagy impairment associated with a metabolic shift towards aerobic glycolysis

Cell Death and Differentiation

Volumn 22, Issue 3, 2015, Pages 408-418

  Rossin, F ^a   D'Eletto, M ^a   Falasca, L ^b   Sepe, S ^c   Cocco, S ^d   Fimia, G M ^b,e   Campanella, M ^d,f   Mastroberardino, P G ^c   Farrace, M G ^a   Piacentini, M ^a,b  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

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

^c ERASMUS MEDICAL CENTER   (Netherlands)

^d EUROPEAN BRAIN RESEARCH INSTITUTE   (Italy)

^e UNIVERSITY OF SALENTO   (Italy)

^f ROYAL VETERINARY COLLEGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 2;

AEROBIC METABOLISM; ANIMAL; AUTOPHAGY; DEFICIENCY; ENERGY METABOLISM; ENZYMOLOGY; GLYCOLYSIS; HEK293 CELL LINE; HUMAN; KNOCKOUT MOUSE; METABOLISM; MITOCHONDRION; MOUSE; PATHOLOGY; PHYSIOLOGY;

AEROBIOSIS; ANIMALS; AUTOPHAGY; ENERGY METABOLISM; GLYCOLYSIS; GTP-BINDING PROTEINS; HEK293 CELLS; HUMANS; MICE; MICE, KNOCKOUT; MITOCHONDRIA; TRANSGLUTAMINASES;

EID: 84922574474     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2014.106     Document Type: Article

References (51)

1. Johansen T, Lamark T. Selective autophagy mediated by autophagic adapter proteins. Autophagy 2011; 7: 279-296.
2. Monastyrska I, Rieter E, Klionsky DJ, Reggiori F. Multiple roles of the cytoskeleton in autophagy. Biol Rev Camb Philos Soc 2009; 84: 431-448.
3. Mizushima N. Autophagy: process and function. Genes Dev 2007; 21: 2861-2873.
4. Levine B, Klionsky DJ. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev Cell 2004; 6: 463-477.
5. Huang J, Klionsky DJ. Autophagy and human disease. Cell Cycle 2007; 6: 1837-1849.
6. Levine B, Kroemer G. Autophagy in the pathogenesis of disease. Cell 2008; 132: 27-42.
7. Sarkar NK, Clarke DD, Waelsh H. An enzymically catalyzed incorporation of amines into proteins. Biochim Biophys Acta 1957; 25: 451-452.
8. Csosz E, Bagossi P, Nagy Z, Dosztanyi Z, Simon I, Fesus L. Substrate preference of transglutaminase 2 revealed by logistic regression analysis and intrinsic disorder examination. J Mol Biol 2008; 383: 390-402.
9. Facchiano A, Facchiano F. Transglutaminases and their substrates in biology and human diseases: 50 years of growing. Amino Acids 2009; 36: 599-614.
10. Di Venere A, Rossi A, De Matteis F, Rosato N, Agrò AF, Mei G. Opposite effects of Ca(2+) and GTP binding on tissue transglutaminase tertiary structure. J Biol Chem 2000; 275: 3915-3921.
11. Gundemir S, Colak G, Feola J, Blouin R, Johnson GV. Transglutaminase 2 facilitates or ameliorates HIF signaling and ischemic cell death depending on its conformation and localization. Biochim Biophys Acta 2013; 1833: 1-10.
12. Nakaoka H, Perez DM, Baek KJ, Das T, Husain A, Misono K et al. Gh: a GTP-binding protein with transglutaminase activity and receptor signaling function. Science 1994; 264: 1593-1596.
13. Piacentini M, Farrace MG, Piredda L, Matarrese P, Ciccosanti F, Falasca L et al. Transglutaminase overexpression sensitizes neuronal cell lines to apoptosis by increasing mitochondrial membrane potential and cellular oxidative stress. J Neurochem 2002; 81: 1061-1072.
14. Malorni W, Farrace MG, Matarrese P, Tinari A, Ciarlo L, Mousavi-Shafaei P et al. The adenine nucleotide translocator 1 acts as a type 2 transglutaminase substrate: implications for mitochondrial-dependent apoptosis. Cell Death Differ 2009; 16: 1480-1492.
15. Lorand L, Graham RM. Transglutaminases: crosslinking enzymes with pleiotropic functions. Nat Rev Mol Cell Biol 2003; 4: 140-156.
16. Zemskov EA, Janiak A, Hang J, Waghray A, Belkin AM. The role of tissue transglutaminase in cell-matrix interactions. Front Biosci 2006; 11: 1057-1076.
17. Malorni W, Farrace MG, Rodolfo C, Piacentini M. Type 2 transglutaminase in neurodegenerative diseases: the mitochondrial connection. Curr Pharm Des 2008; 14: 278-288.
18. Gundemir S, Johnson GV. Intracellular localization and conformational state of transglutaminase 2: implications for cell death. PLoS One 2009; 4: 6123.
19. Park D, Choi SS, Ha KS. Transglutaminase 2: a multi-functional protein in multiple subcellular compartments. Amino Acids 2010; 39: 619-631.
20. Piacentini M, D'Eletto M, Falasca L, Farrace MG, Rodolfo C. Transglutaminase 2 at the crossroads between cell death and survival. Adv Enzymol Relat Areas Mol Biol 2011; 78: 197-246.
21. Akar U, Ozpolat B, Mehta K, Fok J, Kondo Y, Lopez-Berestein G. Tissue transglutaminase inhibits autophagy in pancreatic cancer cells. Mol Cancer Res 2007; 5: 241-249.
22. D'Eletto M, Farrace MG, Falasca L, Reali V, Oliverio S, Melino G et al. Transglutaminase 2 is involved in autophagosome maturation. Autophagy 2009; 5: 1145-1154.
23. D'Eletto M, Farrace MG, Rossin F, Strappazzon F, Giacomo GD, Cecconi F et al. Type 2 transglutaminase is involved in the autophagy-dependent clearance of ubiquitinated proteins. Cell Death Differ 2012; 19: 1228-1238.
24. Rossin F, D'Eletto M, Macdonald D, Farrace MG, Piacentini M. TG2 transamidating activity acts as a reostat controlling the interplay between apoptosis and autophagy. Amino Acids 2012; 42: 1793-1802.
25. Battaglia G, Farrace MG, Mastroberardino PG, Viti I, Fimia GM, Van Beeumen J et al. Transglutaminase 2 ablation leads to defective function of mitochondrial respiratory complex I affecting neuronal vulnerability in experimental models of extrapyramidal disorders. J Neurochem 2007; 100: 36-49.
26. Mastroberardino PG, Farrace MG, Viti I, Pavone F, Fimia GM et al. "Tissue" transglutaminase contributes to the formation of disulphide bridges in proteins of mitochondrial respiratory complexes. Biochim Biophys Acta 2006; 1757: 1357-1365.
27. Rodriguez-Enriquez S, Kim I, Currin RT, Lemasters JJ. Tracker dyes to probe mitochondrial autophagy (mitophagy) in rat hepatocytes. Autophagy 2006; 2: 39-46.
28. Gegg ME, Cooper JM, Chau KY, Rojo M, Schapira AH, Taanman JW. Mitofusin 1 and mitofusin 2 are ubiquitinated in a PINK1/parkin-dependent manner upon induction of mitophagy. Hum Mol Genet 2010; 19: 4861-4870.
29. Ziviani E, Whitworth AJ. How could Parkin-mediated ubiquitination of mitofusin promote mitophagy? Autophagy 2010; 6: 660-662.
30. Springer W, Kahle PJ. Regulation of PINK1-Parkin-mediated mitophagy. Autophagy 2011; 7: 266-278.
31. Rimessi A, Bonora M, Marchi S, Patergnani S, Marobbio CM, Lasorsa FM et al. Perturbed mitochondrial Ca2+ signals as causes or consequences of mitophagy induction. Autophagy 2013; 9: 1677-1686.
32. Zhang C, Yuan XR, Li HY, Zhao ZJ, Liao YW, Wang XY et al. Downregualtion of dynamin-related protein 1 attenuates glutamate-induced excitotoxicity via regulating mitochondrial function in a calcium dependent manner in HT22 cells. Biochem Biophys 2014; 443: 138-143.
33. Chen H, Chan DC. Mitochondrial dynamics - fusion, fission, movement, and mitophagy - in neurodegenerative diseases. Hum Mol Genet 2009; 18: R169-R176.
34. Pi H, Xu S, Zhang L, Guo P, Li Y, Xie J et al. Dynamin 1-like-dependent mitochondrial fission initiates overactive mitophagy in the hepatotoxicity of cadmium. Autophagy 2013; 9: 1780-1800.
35. Twig G, Hyde B, Shirihai OS. Mitochondrial fusion, fission and autophagy as a quality control axis: the bioenergetic view. Biochim Biophys Acta 2008; 1777: 1092-1097.
36. Campanella M, Casswell E, Chong S, Farah Z, Wieckowski MR, Abramov AY et al. Regulation of mitochondrial structure and function by the F1Fo-ATPase inhibitor protein, IF1. Cell Metab 2008; 8: 13-25.
37. Faccenda D, Tan CH, Duchen MR, Campanella M. Mitochondrial IF1 preserves cristae structure to limit apoptotic cell death signaling. Cell Cycle 2013; 12: 2530-1532.
38. Lefebvre V, Du Q, Baird S, Ng AC, Nascimento M, Campanella M et al. Genome-wide RNAi screen identifies ATPase inhibitory factor 1 (ATPIF1) as essential for PARK2 recruitment and mitophagy. Autophagy 2013; 9: 1770-1779.
39. Tarze A, Deniaud A, Le Bras M, Maillier E, Molle D, Larochette N et al. GAPDH, a novel regulator of the pro-apoptotic mitochondrial membrane permeabilization. Oncogene 2007; 26: 2606-2620.
40. Kathiria AS, Butcher LD, Feagins LA, Souza RF, Boland CR, Theiss AL. Prohibitin 1 modulates mitochondrial stress-related autophagy in human colonic epithelial cells. PLoS One 2012; 7: e31231.
41. Kim NC, Tresse E, Kolaitis RM, Molliex A, Thomas RE, Alami NH et al. VCP is essential for mitochondrial quality control by PINK1/Parkin and this function is impaired by VCP mutations. Neuron 2013; 78: 65-80.
42. Orru S, Ruoppolo M, Francese S, Vitagliano L, Marino G, Esposito C. Identification of tissue transglutaminase-reactive lysine residues in glyceraldehyde-3-phosphate dehydrogenase. Protein Sci 2002; 11: 137-146.
43. Filiano AJ, Bailey CD, Tucholski J, Gundemir S, Johnson GV. Transglutaminase 2 protects against ischemic insult, interacts with HIF1beta, and attenuates HIF1 signaling. FASEB J 2008; 22: 2662-2675.
44. Frank S, Gaume B, Bergmann-Leitner ES, Leitner WW, Robert EG, Catez F et al. The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. Dev Cell 2001; 1: 515-525.
45. Lackner LL, Nunnari JM. The molecular mechanism and cellular functions of mitochondrial division. Biochim Biophys Acta 2009; 1792: 1138-1144.
46. Ong SB, Subrayan S, Lim SY, Yellon DM, Davidson SM, Hausenloy DJ. Inhibiting mitochondrial fission protects the heart against ischemia/reperfusion injury. Circulation 2010; 121: 2012-2022.
47. Tanaka A, Youle RJ. A chemical inhibitor of DRP1 uncouples mitochondrial fission and apoptosis. Mol Cell 2008; 29: 409-410.
48. Cassidy-Stone A, Chipuk JE, Ingerman E, Song C, Yoo C, Kuwana T et al. Chemical inhibition of the mitochondrial division dynamin reveals its role in Bax/Bak-dependent mitochondrial outer membrane permeabilization. Dev Cell 2008; 14: 193-204.
49. Park SW, Kim KY, Lindsey JD, Dai Y, Heo H, Nguyen DH et al. A selective inhibitor of drp1, mdivi-1, increases retinal ganglion cell survival in acute ischemic mouse retina. Invest Ophthalmol Vis Sci 2011; 52: 2837-2843.
50. Strnad P, Zatloukal K, Stumptner C, Kulaksiz H, Denk H. Mallory-Denk-bodies: lessons from keratin-containing hepatic inclusion bodies. Biochim Biophys Acta 2008; 1782: 764-774.
51. Høyer-Hansen M, Jäättelä M. Connecting endoplasmic reticulum stress to autophagy by unfolded protein response and calcium. Cell Death Differ 2007; 14: 1576-1582.