Function and expression study uncovered hepatocyte plasma membrane ecto-ATP synthase as a novel player in liver regeneration

Biochemical Journal

Volumn 473, Issue 16, 2016, Pages 2519-2530

  Taurino, Federica ^a   Giannoccaro, Caterina ^a   Sardanelli, Anna Maria ^a,b   Cavallo, Alessandro ^c   De Luca, Elisa ^d   Santacroce, Salvatore ^a   Papa, Sergio ^e   Zanotti, Franco ^a   Gnoni, Antonio ^a,b  

^a UNIVERSITY OF BARI   (Italy)

^b University of Rome   (Italy)

^c UNIVERSITY OF SALENTO   (Italy)

^d ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^e CNR   (Italy)

Author keywords

ATP synthase; Ecto ATP synthase; Extracellular ATP ADP; Hepatocytes; Liver regeneration; Proton trafficking

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; HYDROLASE; PROTON; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; ADENOSINE TRIPHOSPHATASE; ECTOATPASE; F1F0-ATP SYNTHASE; MEMBRANE PROTEIN;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; ENZYME ACTIVITY; LIVER CELL; LIVER REGENERATION; LIVER RESECTION; MALE; MITOCHONDRION; NONHUMAN; PARTIAL HEPATECTOMY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REGENERATION; VISUAL EVOKED POTENTIAL; ANIMAL; BIOCATALYSIS; ENZYMOLOGY; LIVER MITOCHONDRION; METABOLISM; WISTAR RAT;

ADENOSINE TRIPHOSPHATASES; ANIMALS; BIOCATALYSIS; HEPATECTOMY; LIVER REGENERATION; MALE; MEMBRANE PROTEINS; MITOCHONDRIA, LIVER; MITOCHONDRIAL PROTON-TRANSLOCATING ATPASES; RATS; RATS, WISTAR;

EID: 84994585610     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BCJ20160065     Document Type: Article

References (52)

1. Boyer, P.D. (1997) The ATP synthase: a splendid molecular machine. Annu. Rev. Biochem. 66, 717-749
2. 0 ATP synthases. Annu. Rev. Biochem. 78, 649-672
3. Yoshida, M., Muneyuki, E. and Hisabori, T (2001) ATP synthase: a marvellous rotary engine of the cell. Nat. Rev. Mol. Cell Biol. 2, 669-677
4. Panfoli, I., Ravera, S., Bruschi, M., Candiano, G. and Morelli, A. (2011) Proteomics unravels the exportability of mitochondrial respiratory chains. Expert Rev. Proteomics 8, 231-239
5. Martinez, L.O., Jacquet, S., Esteve, J.P., Rolland, C, Cabezón, E., Champagne, E., Pineau, T., Georgeaud, V., Walker, J.E., Tercé, F. et al. (2003) Ectopic β-chain of ATP synthase is an apolipoprotein A-I receptor in hepatic HDL endocytosis. Nature 421, 75-79
6. Xing, S.L., Yan, J., Yu, Z.H. and Zhu, C.Q. (2011) Neuronal cell surface ATP synthase mediates synthesis of extracellular ATP and regulation of intracellular pH. Cell Biol. Int. 35, 81-86 PubMed
7. 1 ATPase: metabolic and immunological functions. Curr. Opin. Lipidol. 17, 279-284
8. Chi, S.L. and Pizzo, S.V. (2006) Angiostatin is directly cytotoxic to tumor cells at low extracellular pH: a mechanism dependent on cell surface-associated ATP synthase. Cancer Res. 66, 875-882
9. 0-ATPase, F-type proton-translocating ATPase, at the plasma membrane is critical for efficient influenza virus budding. Proc. Natl. Acad. Sci. U.S.A. 109, 4615-4620
10. Vacirca, D., Delunardo, F., Matarrese, P., Colasanti, T., Margutti, P., Siracusano, A., Pontecorvo, S., Capozzi, A, Sorice, M., Francia, A. et al. (2012) Autoantibodies to the adenosine triphosphate synthase play a pathogenetic role in Alzheimer's disease. Neurobiol. Aging 33, 753-766
11. Chang, H.Y., Huang, H.C., Huang, T.C., Yang, P.C., Wang, YC. and Juan, H.F. (2012) Ectopic ATP synthase blockade suppresses lung adenocarcinoma growth by activating the unfolded protein response. Cancer Res. 72, 4696-4706
12. Zhang, LH, Kamanna, VS, Zhang, M.C. and Kashyap, MI. (2008) Niacin inhibits surface expression of ATP synthase βchain in HepG2 cells: implications for raising HDL. J. Lipid Res. 49, 1195-1201
13. Si-Tayeb, K., Lemaigre, F.R and Duncan, S.A. (2010) Organogenesis and development of the liver. Dev. Cell 1, 175-189
14. Higgins, G.M. and Anderson, R.M. (1931) Experimental pathology of the liver: restoration of the liver of the white rat following partial removal. Arch. Pathol. 12, 186-202
15. DeFrances, M.C. and Michalopoulos, G.K. (2011) Liver regeneration and partial hepatectomy: process and prototype. In Liver Regeneration (Hiissinger, D., ed.), pp. 1-16
16. Michalopoulos, G.K. (2007) Liver regeneration. J. Cell. Physiol. 213, 286-300
17. Guerrieri, F, Vendemiale, G., Grattagliano, I., Cocco, T, Pellecchia, G. and Altomare, E. (1999) Mitochondrial oxidative alterations following partial hepatectomy. Free Radie. Biol. Med. 26, 34-41
18. Guerrieri, F, Muolo, L, Cocco, T, Capozza, G., Turturro, N., Cantatore, P. and Papa, S. (1995) Correlation between rat liver regeneration and mitochondrial energy metabolism. Biochim. Biophys. Acta 1272, 95-100
19. 0-ATP synthase on the extracellular surface of rat hepatocytes. Biochim. Biophys. Acta 1777, 1326-1335
20. Cavallo, A, Priore, P., Gnoni, G.V, Papa, S., Zanotti, F and Gnoni, A. (2013) 3, 5-Diiodo-L-thyronine administration to hypothyroid rats rapidly enhances fatty acid oxidation rate and bioenergetic parameters in liver cells. PLoS One 8, e52328
21. Hubbard, A.L., Wall, D.A. and Ma, A. (1983) Isolation of rat hepatocyte plasma membranes. I. Presence of the three major domains. J. Cell Biol. 96, 217-229
22. Seglen, P.O. (1973) Preparation of rat liver cells. 3. Enzymatic requirements for tissue dispersion. Exp. Cell Res. 82, 391-398
23. Gnoni, G.V., Geelen, M.J.H., Bijleveld, C, Quagliariello, E. and van den Bergh, S.G. (1985) Short term stimulation of lipogenesis by triiodothyronine in maintenance cultures of rat hepatocytes. Biochem. Biophys. Res. Commun. 128, 525-530
24. 0-ATP synthase activity and cardiolipin level in liver mitochondria of hypothyroid rats. J. Bioenerg. Biomembr. 43, 349-357
25. Symersky, J., Osowski, D., Walters, D.E. and Mueller, D.M. (2012) Oligomycin frames a common drug-binding site in the ATP synthase. Proc. Natl. Acad. Sci. U.S.A. 109, 13961-13965
26. Friedl, P., Friedl, C. and Schairer, H.U. (1979) The ATP synthetase of Escherichia coli K12: purification of the enzyme and reconstitution of energy-transducing activities Eur. J. Biochem. 100, 175-180
27. Carlsen, S.A., Schmell, E., Weigel, P.H. and Roseman, S. (1981) The effect of the method of isolation on the surface properties of isolated rat hepatocytes. J. Biol. Chem. 256, 8058-8062
28. + translocation in the mitochondrial ATP synthase complex. Biochem. Biophys. Res. Commun. 384, 43-48
29. Woods, H.F. and Krebs, H.A. (1971) Lactate production in the perfused rat liver. Biochem. J. 125, 129-139
30. +-ATP synthase in the extracellular ATP synthesis and proliferation of human umbilical vein endothelial cells. Mol. Cancer Res. 1, 931-939
31. Fausto, N. (2000) Liver regeneration. J. Hepatol. 3, 19-31
32. Taub, R. (2004) Liver regeneration: from myth to mechanism. Nat. Rev. Mol. Cell Biol. 5, 836-847
33. 1-ATPase: a moonlighting protein complex and an unexpected apoA-l receptor. World J. Gastroenterol. 16, 5925-5935
34. 0-ATP synthase translocates to cell surface in hepatocytes and has high activity in tumor-like acidic and hypoxic environment. Acta Biochim. Biophys. Sin. 42, 530-537
35. +-ATPase in regenerating rat liver. FEBS Lett. 188, 345-351 CrossRef
36. 0 complex of rat-liver mitochondria during early hepatic regeneration. FEBS Lett. 209, 197-202
37. Crumm, S., Cofan, M., Juskeviciute, E. and Hoek, J.B. (2008) Adenine nucleotide changes in the remnant liver: an early signal for regeneration after partial hepatectomy. Hepatology 48, 898-908
38. Gonzales, E., Julien, B., Serrière-Lanneau, V, Nicou, A., Doignon, I., Lagoudakis, L, Garcin, I., Azoulay, D., Duclos-Vallée, J.C., Castaing, D. et al. (2010) ATP release after partial hepatectomy regulates liver regeneration in the rat. J. Hepatol. 52, 54-62
39. 2 purinergic receptor activation is essential for efficient hepatocyte proliferation in response to partial hepatectomy. Am. J. Physiol. Gastrointest. Liver Physiol. 307, 1073-1087
40. Graubardt, N., Fahrner, R., Trochsler, M., Keogh, A., Breu, K., Furer, C, Stroka, D., Robson, S.C., Slack, E., Candinas, D. et al. (2013) Promotion of liver regeneration by natural killer cells in a murine model is dependent on extracellular adenosine triphosphate phosphohydrolysis. Hepatology 57, 1969-1979
41. Casey, J.R., Grinstein, S. and Orlowski, J. (2010) Sensors and regulators of intracellular pH. Nat. Rev. Mol. Cell Biol. 11, 50-61
42. Parks, S.K., Chiche, J. and Pouysségur, J. (2013) Disrupting proton dynamics and energy metabolism for cancer therapy. Nat. Rev. Cancer 13, 611-623
43. Lagadic-Gossmann, D., Hue, L. and Lecureur, V (2004) Alterations of intracellular pH homeostasis in apoptosis: origins and roles. Cell Death Differ. 11, 953-961
44. Koch, K.S. and Leffert, Hi. (1979) Increased sodium ion influx is necessary to initiate rat hepatocyte proliferation. Cell 18, 153-163
45. Moule, S.K. and McGivan, J.D. (1990) Regulation of the plasma membrane potential in hepatocytes: mechanism and physiological significance. Biochim. Biophys. Acta 1031, 383-397
46. Paloheimo, M., Linkola, J., Lempinen, M. and Folke, M. (1984) Time-courses of hepatocellular hyperpolarization and cyclic adenosine 3', 5'-monophosphate accumulation after partial hepatectomy in the rat: effects of fasting for 48 hours and intravenous injection of glucose. Gastroenterology 87, 639-646
47. Wondergem, R. and Harder, D.R. (1980) Membrane potential measurements during rat liver regeneration. J. Cell. Physiol. 102, 193-197
48. Kang, LI, Mars, W.M. and Michalopoulos, G.K. (2012) Signals and cells involved in regulating liver regeneration. Cells 1, 1261-1292
49. Uriel, J. (1976) Cancer, retrodifferentiation, and the myth of Faust. Cancer Res. 36, 4269-4275
50. 0-ATP synthase. Trends Biochem. Sci. 34, 343-350
51. McKenzie, M., Liolitsa, D., Akinshina, N., Campanella, M., Sisodiya, S., Hargreaves, l., Nirmalananthan, N, Sweeney, M.G., Abou-Sleiman, P.M., Wood, N.W. et al. (2007) Mitochondrial ND5 gene variation associated with encephalomyopathy and mitochondrial ATP consumption. J. Biol. Chem. 282, 36845-36852
52. Hong, S. and Pedersen, PL. (2008) ATP synthase and the actions of inhibitors utilized to study its roles in human health, disease, and other scientific areas. Microbiol. Mol. Biol. Rev. 72, 590-641