Evidence for LKB1/AMP-activated protein kinase/endothelial nitric oxide synthase cascade regulated by hepatocyte growth factor, S-adenosylmethionine, and nitric oxide in hepatocyte proliferation

Hepatology

Volumn 49, Issue 2, 2009, Pages 608-617

  Vázquez Chantada, Mercedes ^a   Ariz, Usue ^a   Varela Rey, Marta ^a   Embade, Nieves ^a   Martínez Lopez, Nuria ^a   Fernández Ramos, David ^a   Gómez Santos, Laura ^a   Lamas, Santiago ^b   Lu, Shelly C ^c   Martínez Chantar, M Luz ^a   Mato, José M ^a  

^a INSTITUTO DE SALUD CARLOS III   (Spain)

^b CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN A2; CYCLIN D1; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HUR PROTEIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MESSENGER RNA; NITRIC OXIDE; PHOSPHOPROTEIN PHOSPHATASE; PROTEIN KINASE LKB1; S ADENOSYLMETHIONINE; SCATTER FACTOR; PROTEIN SERINE THREONINE KINASE; STK11 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL CULTURE; CELL GROWTH; CELL ISOLATION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME REGULATION; LIVER CELL; LIVER REGENERATION; MALE; MOUSE; NONHUMAN; PARTIAL HEPATECTOMY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RNA INTERFERENCE; ANIMAL; C57BL MOUSE; CELL DIVISION; CONFOCAL MICROSCOPY; CYTOLOGY; DNA REPLICATION; ENZYMOLOGY; GENE SILENCING; HOMEOSTASIS; LIVER RESECTION; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; CELL DIVISION; DNA REPLICATION; GENE SILENCING; HEPATECTOMY; HEPATOCYTES; HOMEOSTASIS; LIVER REGENERATION; MALE; MICE; MICE, INBRED C57BL; MICROSCOPY, CONFOCAL; NITRIC OXIDE SYNTHASE TYPE III; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES;

EID: 61949292843     PISSN: 02709139     EISSN: None     Source Type: Journal    
DOI: 10.1002/hep.22660     Document Type: Article

References (51)

1. Birchmeier C, Birchmeier W, Gherardi E, Vande Woude GF. Met, metastasis, motility and more. Nat Rev Mol Cell Biol 2003;4:915-925.
2. Borowiak M, Garratt AN, Wüstefeld T, Strehle M, Trautwein C, Birchmeier C. Met provides essential signals for liver regeneration. Proc Natl Acad Sci U S A 2004;101:10608-10613.
3. Ponzetto C, Bardelli A, Zhen Z, Maina F, dalla Zonca P, Giordano S, et al. A multifunctional docking site mediates signaling and transformation by the hepatocyte growth factor/scatter factor receptor family. Cell 1994;77: 261-277.
4. Paumelle R, Tulasne D, Kherrouche Z, Plaza S, Leroy C, Reveneau S, et al. Hepatocyte growth factor/scatter factor activates the ETS1 transcription factor by a RAS-RAF-MEK-ERK signaling pathway. Oncogene 2002;21: 2309-2319.
5. Fausto N, Campbell JS, Riehle KJ. Liver regeneration. HEPATOLOGY 2006; 43:S45-S53.
6. Michalopoulos GM. Liver regeneration. J Cell Physiol 2007;213:286-300.
7. Martínez-Chantar ML, Vázquez-Chantada M, Garnacho M, Latasa MU, Varela-Rey M, Dotor J, et al. S-adenosylmethionine regulates cytoplasmic HuR via AMPK-activated kinase. Gastroenterology 2006; 131:223-232.
8. Hardie DG, Hawley SA, Scott JW. AMP-activated protein kinase-development of the energy sensory concept. J Physiol 2006;574:7-15.
9. Hawley SA, Boudeau J, Reid JL, Mustard KJ, Udd L, Makela TP, et al. Complexes between the LKB1 tumor suppressor, STRADα/βare upstream kinases in the AMP-activated protein kinase cascade. J Biol 2003;2:28.
10. Hawley SA, Pan DA, Mustard KJ, Ross L, Bain J, Edelman AM, et al. Calmodulin-dependent protein kinase-beta is an alternative upstream kinase for AMP-activated protein kinase. Cell Metab 2005;2:9-19.
11. Woods A, Dickerson K, Heath R, Hong SP, Momcilovic M, Johnstone SR, et al. Ca2+/calmodulin-dependent protein kinase kinase-beta acts upstream of AMP-activated protein kinase in mammalian cells. Cell Metab 2005;2:21-33.
12. Brennan CM, Steitz JA. HuR and mRNA stability. Cell Mol Life Sci 2001;58:266-277.
13. Wang W, Yang X, Cristofalo VJ, Holbrook NJ, Gorospe M. Loss of HuR is linked to reduced expression of proliferative genes during replicative senescence. Mol Cell Biol 2001;21:5889-5898.
14. Mato JM, Lu SC. Role of S-adenosyl-L-methionine in liver health and injury. HEPATOLOGY 2007;45:1306-1312.
15. Mato JM, Martínez-Chantar ML, Lu SC. Methionine metabolism and liver disease. Ann Rev Nutr 2008;28:273-293.
16. Lu SC, Alvarez L, Huang ZZ, Chen L, An W, Corrales FJ, et al. Methionine adenosyltransferase 1A knockout mice are predisposed to liver injury and exhibit increased expression of genes involved in proliferation. Proc Natl Acad Sci U S A 2001;98:5560-5565.
17. Martínez-Chantar ML, Corrales FJ, Martínez-Cruz A, García-Trevijano ER, Huang ZZ, Chen L, et al. Spontaneous oxidative stress and liver tumors in mice lacking methionine adenosyltransferase 1A. FASEB J 2002; 16:1292-1294.
18. Cai J, Mao Z, Hwang J, Lu SC. Differential expression of methionine adenosyltransferase genes influences the rate of growth of human hepatocellular carcinoma cells. Cancer Res 1998;58:1444-1450.
19. Garcea R, Daino L, Pascale R, Simile MM, Puddu M, Ruggiu ME, et al. Protooncogene methylation and expression in regenerating liver and preneoplastic liver nodules induced in the rat by diethylnitrosamine: effect of variations of S-adenosylmethionine:S-adenosylhomocysteine ratio. Carcinogenesis 1989;10:1183-1192.
20. Huang ZZ, Mao Z, Cai J, Lu SC. Changes in methionine adenosyltransferase during liver regeneration in the rat. Am J Physiol 1998;275:G14-G21.
21. Pascale RM, Simile MM, Daino L, Pinna G, Bennati S, Carta M, et al. Chemoprevention of rat liver carcinogenesis by S-adenosyl-L-lmethionine: a long term study. Cancer Res 1995;16:427-430.
22. Hortelano S, Dewez B, Genaro AM, Díaz-Guerra MJ, Boscá L. Nitric oxide is raised in regenerating liver after partial hepatectomy. HEPATOLOGY 1995;21:776-786.
23. Díaz-Guerra MJ, Velasco M, Martín-Sanz P, Boscá L. Nuclear factor kappaB is required for the transcriptional control of type II NO synthase in regenerating liver. Biochem J 1997;326:791-797.
24. Rai RM, Lee FY, Rosen A, Tang SQ, Lin HZ, Koteish A, et al. Impaired liver regeneration in inducible nitric oxide synthase deficient mice. Proc Natl Acad Sci U S A 1998;95:1329-1334.
25. Ruiz F, Corrales FJ, Miqueo C, Mato JM. Nitric oxide inactivates rat hepatic methionine adenosyltransferase In vivo by S-nitrosylation. HEPATOLOGY 1998;28:1051-1057.
26. Pérez-Mato I, Castro C, Ruiz FA, Corrales FJ, Mato JM. Methionine adenosyltransferase S-nitrosylation is regulated by the basic and acidic amino acids surrounding the target thiol. J Biol Chem 1999;274:17075-17079.
27. Chen ZP, Mitchelhill KI, Michel BJ, Stapleton D, Rodríguez-Crespo I, Witters LA, et al. AMP-activated protein kinase phosphorylation of endothelial NO synthase. FEBS Lett 1999;443:285-289.
28. Morrow VA, Foufelle F, Connell JM, Petrie JR, Gould GW, Salt IP. Direct activation of AMP-activated protein kinase stimulates nitric-oxide synthesis in human aortic endothelial cells. J Biol Chem 2003;278:31629-31639.
29. Levine YC, Li GK, Michel T. Agonist-modulated regulation of AMP activated protein kinase (AMPK) in endothelial cells. Evidence for an AMPK>Rac1>Akt>endothelial nitric-oxide synthase pathway. J Biol Chem 2007;282:20351-20364.
30. Reihill JA, Ewart MA, Hardie DG, Salt IP. AMP-activated protein kinase mediates VEGF-stimulated endothelial NO production. Biochem Biophys Res Commun 2007;354:1084-1088.
31. Makondo K, Kimura K, Kitamura T, Yamaji D, Jung BD, Saito M. Hepatocyte growth factor activates endothelial nitric oxide synthase by Ca(2+)- and phosphoinositide 3-kinase/Akt-dependent phosphorylation in aortic endothelial cells. Biochem J 2003;374:63-69.
32. Uruno A, Sugawara A, Kanatsuka H, Arima S, Taniyama Y, Kudo M, et al. Hepatocyte growth factor stimulates nitric oxide production through endothelial nitric oxide synthase activation by the phosphoinositide 3-kinase/Akt pathway and possibly by mitogen-activated protein kinase kinase in vascular endothelial cells. Hypertens Res 2004;27:887-895.
33. Wang HH, Lautt WW. Evidence of nitric oxide, a flow-dependent factor, being a trigger of liver regeneration in rats. Can J Physiol Pharmacol 1998;76:1072-1079.
34. García-Trevijano ER, Martínez-Chantar ML, Latasa MU, Mato JM, Avila MA. NO sensitizes rat hepatocytes to proliferation by modifying S-adenosylmethionine levels. Gastroenterology 2002;122:1355-1363.
35. Gobeil F, Zhu T, Brault S, Geha A, Vazquez-Tello A, Fortier A, et al. Nitric oxide signaling via nuclearized endothelial nitric-oxide synthase expression of the immediate early genes iNOS and mPGES-1. J Biol Chem 2006;281:16058-16067.
36. Leffert HL, Koch KS, Moran T, Williams M. Liver cells. Methods Enzymol 1979;58:536-544.
37. Medico E, Mongiovi AM, Huff J, Jelinek MA, Follenzi A, Gaudino G, et al. The tyrosine kinase receptors Ron and Sea control scattering and morphogenesis of liver progenitor cells in vitro. Mol Biol Cell 1966;7:495-504.
38. López-Rivera E, Lizarbe TR, Martínez-Moreno M, López-Novoa JM, Rodríguez-Barbero A, Rodrigo J, et al. Matrix metalloproteinase 13 mediates nitric oxide activation of endothelial cell migration. Proc Natl Acad Sci U S A 2005;102:3685-3690.
39. Higgins BC, Andersen RM. Experimental pathology of liver: Restoration of liver of the white rat following partial surgical removal. Arch Pathol 1931; 12:186-202.
40. Martínez-Chantar ML, Vazquez-Chantada M, Ariz U, Martinez N, Varela M, Capdevila A, et al. Loss of the glycine N-methyltransferase gene leads to steatosis and hepatocellular carcinoma in mice. HEPATOLOGY 2008;28:273-293.
41. Sapkota GP, Kieloch A, Lizcano JM, Lain S, Arthur JS, Williams MR, et al. Phosphorylation of the protein kinase mutated in Peutz-Jeghers cancer syndrome, LKB1/STK11, at Ser431 by p90(RSK) and cAMP-dependent protein kinase, but not its farnesylation at Cys(433), is essential for LKB1 to suppress cell growth. J Biol Chem 2001;276:19469-19482.
42. Frémin C, Ezan F, Boisselier P, Bessard A, Page's G, Pouysségur J, et al. ERK2 but not ERK1 plays a key role in hepatocyte replication: An RNA imediated ERK2 knockdown approach in wild-type and ERK1 null hepatocytes. HEPATOLOGY 2007;45:1035-1045.
43. Majano PL, García-Monzón C, García-Trevijano ER, Corrales FJ, Cámara J, Ortiz P, et al. S-adenosylmethionine modulates inducible nitric oxide synthase gene expression in rat liver and isolated hepatocytes. J Hepatol 2001;35:692-699.
44. McCall TB, Feelisch M, Palmer RM, Moncada S. Identification of Niminoethyl-L-ornithine as an irreversible inhibitor of nitric oxide synthase in phagocytic cells. Br J Pharmacol 1991;102:234-238.
45. Chen L, Zeng Y, Yang H, Le TD, French SW, Corrales FJ, et al. Impaired liver regeneration in mice lacking methionine adenosyltransferase 1A. FASEB J 2004;18:914-916.
46. Latasa MU, Boukaba A, García-Trevijano ER, Torres L, Rodríguez JL, Caballería J, et al. Hepatocyte growth factor induces MAT2A expression and histone acetylation in rat hepatocytes: Role in liver regeneration. FASEB J 2001;15:1248-1250.
47. Rodríguez-Pascual F, Hausding M, Ihrig-Biedert I, Furneaux H, Levy AP, Förstermann U, et al. Complex contribution of the 3'-untranslated region to the expressional regulation of the human inducible nitric-oxide gene. Involvement of the RNA-binding protein HuR. J Biol Chem 2000;275: 26040-26049.
48. Matsui K, Nishizawa M, Ozaki T, Kimura T, Hashimoto I, Yamada M, et al. Natural antisense transcript stabilizes inducible nitric oxide synthase messenger RNA in rat hepatocytes. HEPATOLOGY 2008;47:686-697.
49. Choi HC, Song P, Xie Z, Wu Y, Xu J, Zhang M, et al. Reactive nitrogen species is required for the activation of the AMP-activated protein kinase by statin in vivo. J Biol Chem 2008;283:20186-20197.
50. Nakashima S, Saji S, Nakamura T, Nozawa Y. Activated protein kinase activation in hepatocyte growth factor-stimulated rat hepatocytes: involvement of protein tyrosine kinase and protein kinase C. HEPATOLOGY 1996; 23:1244-1253.
51. Hashigasako A, Machide M, Nakamura T, Matsumoto K, Nakamura T. Bi-directional regulation of Ser-985 phosphrylation of c-Met via protein kinaseCand protein phosphatase 2A involves c-Met activation and cellular responsiveness to hepatocyte growth factor. J Biol Chem 2004;279:26445-26452.