AMPK directly inhibits NDPK through a phosphoserine switch to maintain cellular homeostasis

Molecular Biology of the Cell

Volumn 23, Issue 2, 2012, Pages 381-389

  Onyenwoke, Rob U ^a   Forsberg, Lawrence J ^a   Liu, Lucy ^a   Williams, Tyisha ^a   Alzate, Oscar ^a   Brenman, Jay E ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; ADENYLATE KINASE; MUTANT PROTEIN; NUCLEOSIDE DIPHOSPHATE KINASE; PHOSPHOSERINE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ENERGY; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; GEL ELECTROPHORESIS; MALE; MOUSE; NEUROBLASTOMA; NONHUMAN; PRIORITY JOURNAL;

ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; BRAIN; CELL LINE, TUMOR; DROSOPHILA MELANOGASTER; GENE KNOCKOUT TECHNIQUES; HEK293 CELLS; HOMEOSTASIS; HUMANS; MALE; MICE; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEOSIDE-DIPHOSPHATE KINASE; PHOSPHORYLATION; PHOSPHOSERINE; TWO-DIMENSIONAL DIFFERENCE GEL ELECTROPHORESIS;

EID: 84862948331     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E11-08-0699     Document Type: Article

References (73)

1. Almaula N, Lu Q, Delgado J, Belkin S, Inouye M (1995). Nucleoside diphosphate kinase from Escherichia coli. J Bacteriol 177, 2524-2529.
2. Annesley SJ, Bago R, Mehta A, Fisher PR (2011). A genetic interaction between NDPK and AMPK in Dictyostelium discoideum that affects motility, growth and development. Naunyn Schmiedebergs Arch Pharmacol 384, 341-349.
3. Barnes K, Ingram JC, Porras OH, Barros LF, Hudson ER, Fryer LG, Foufelle F, Carling D, Hardie DG, Baldwin SA (2002). Activation of GLUT1 by metabolic and osmotic stress: potential involvement of AMP-activated protein kinase (AMPK). J Cell Sci 115, 2433-2442. (Pubitemid 34752985)
4. Biondi RM, Engel M, Sauane M, Welter C, Issinger OG, Jimenez de Asua L, Passeron S (1996). Inhibition of nucleoside diphosphate kinase activity by in vitro phosphorylation by protein kinase CK2. Differential phosphorylation of NDP kinases in HeLa cells in culture. FEBS Lett 399, 183-187. (Pubitemid 27007981)
5. Bjorklund MA, Vaahtomeri K, Peltonen K, Viollet B, Makela TP, Band AM, Laiho M (2010). Non-CDK-bound p27 (p27(NCDK)) is a marker for cell stress and is regulated through the Akt/PKB and AMPK-kinase pathways. Exp Cell Res 316, 762-774.
6. Boissan M, Dabernat S, Peuchant E, Schlattner U, Lascu I, Lacombe ML (2009). The mammalian Nm23/NDPK family: from metastasis control to cilia movement. Mol Cell Biochem 329, 51-62.
7. Bungard D, Fuerth BJ, Zeng PY, Faubert B, Maas NL, Viollet B, Carling D, Thompson CB, Jones RG, Berger SL (2010). Signaling kinase AMPK activates stress-promoted transcription via histone H2B phosphorylation. Science 329, 1201-1205.
8. Chang CL, Zhu XX, Thoraval DH, Ungar D, Rawwas J, Hora N, Strahler JR, Hanash SM, Radany E (1994). Nm23-H1 mutation in neuroblastoma. Nature 370, 335-336.
9. Chartier NT, Salazar Ospina DP, Benkemoun L, Mayer M, Grill SW, Maddox AS, Labbe JC (2011). PAR-4/LKB1 mobilizes nonmuscle myosin through anillin to regulate C. elegans embryonic polarization and cytokinesis. Curr Biol 21, 259-269.
10. Cheng SW, Fryer LG, Carling D, Shepherd PR (2004). Thr2446 is a novel mammalian target of rapamycin (mTOR) phosphorylation site regulated by nutrient status. J Biol Chem 279, 15719-15722. (Pubitemid 38509255)
11. Crawford RM, Treharne KJ, Arnaud-Dabernat S, Daniel JY, Foretz M, Viollet B, Mehta A (2006a). Understanding the molecular basis of the interaction between NDPK-A and AMPK alpha 1. Mol Cell Biol 26, 5921-5931. (Pubitemid 44134345)
12. Crawford RM, Treharne KJ, Arnaud-Dabernat S, Daniel JY, Foretz M, Viollet B, Mehta A (2007). Protein kinase CK2 acts as a signal molecule switching between the NDPK-A/AMPK 1 complex and NDPK-B. FASEB J 21, 3398.
13. Crawford RM, Treharne KJ, Best OG, Muimo R, Riemen CE, Mehta A (2005). A novel physical and functional association between nucleoside diphosphate kinase A and AMP-activated protein kinase alpha1 in liver and lung. Biochem J 392, 201-209. (Pubitemid 41689416)
14. Crawford RM, Treharne KJ, Best OG, Riemen CE, Muimo R, Gruenert DC, Arnaud-Dabernat S, Daniel JY, Mehta A (2006b). NDPK-A (but not NDPK-B) and AMPK alpha1 (but not AMPK alpha2) bind the cystic fibrosis transmembrane conductance regulator in epithelial cell membranes. Cell Signal 18, 1595-1603. (Pubitemid 44216117)
15. Dammai V, Adryan B, Lavenburg KR, Hsu T (2003). Drosophila awd, the homolog of human nm23, regulates FGF receptor levels and functions synergistically with shi/dynamin during tracheal development. Genes Dev 17, 2812-2824. (Pubitemid 37463290)
16. Davies SP, Carling D, Hardie DG (1989). Tissue distribution of the AMP-activated protein kinase, and lack of activation by cyclic-AMP-dependent protein kinase, studied using a specific and sensitive peptide assay. Eur J Biochem 186, 123-128. (Pubitemid 20015134)
17. Davies SP, Hawley SA, Woods A, Carling D, Haystead TA, Hardie DG (1994). Purification of the AMP-activated protein kinase on ATP-gamma-Sepharose and analysis of its subunit structure. Eur J Biochem 223, 351-357. (Pubitemid 24244180)
18. Dyck JR, Gao G, Widmer J, Stapleton D, Fernandez CS, Kemp BE, Witters LA (1996). Regulation of 5'-AMP-activated protein kinase activity by the noncatalytic beta and gamma subunits. J Biol Chem 271, 17798-17803. (Pubitemid 26250755)
19. Egan DF et al. (2011). Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy. Science 331, 456-461.
20. Engel M, Veron M, Theisinger B, Lacombe ML, Seib T, Dooley S, Welter C (1995). A novel serine/threonine-specific protein phosphotransferase activity of Nm23/nucleoside-diphosphate kinase. Eur J Biochem 234, 200-207.
21. Freije JM, Blay P, MacDonald NJ, Manrow RE, Steeg PS (1997). Site-directed mutation of Nm23-H1. Mutations lacking motility suppressive capacity upon transfection are deficient in histidine-dependent protein phosphotransferase pathways in vitro. J Biol Chem 272, 5525-5532. (Pubitemid 27102375)
22. Gao G, Fernandez CS, Stapleton D, Auster AS, Widmer J, Dyck JR, Kemp BE, Witters LA (1996). Non-catalytic beta- and gamma-subunit isoforms of the 5′-AMP-activated protein kinase. J Biol Chem 271, 8675-8681.
23. Giraud MF, Georgescauld F, Lascu I, Dautant A (2006). Crystal structures of S120G mutant and wild type of human nucleoside diphosphate kinase A in complex with ADP. J Bioenerg Biomembr 38, 261-264. (Pubitemid 44946233)
24. Green AS, Chapuis N, Lacombe C, Mayeux P, Bouscary D, Tamburini J (2011). LKB1/AMPK/mTOR signaling pathway in hematological malignancies: From metabolism to cancer cell biology. Cell Cycle 10, 2115-2120.
25. Gwinn DM, Shackelford DB, Egan DF, Mihaylova MM, Mery A, Vasquez DS, Turk BE, Shaw RJ (2008). AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol Cell 30, 214-226. (Pubitemid 351626684)
26. Hardie DG (2004). The AMP-activated protein kinase pathway - new players upstream and downstream. J Cell Sci 117, 5479-5487.
27. Hardie DG (2007). AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy. Nat Rev Mol Cell Biol 8, 774-785.
28. Hardie DG, Hawley SA (2001). AMP-activated protein kinase: the energy charge hypothesis revisited. Bioessays 23, 1112-1119.
29. Hardie DG, Hawley SA, Scott JW (2006). AMP-activated protein kinase-development of the energy sensor concept. J Physiol 574, 7-15. (Pubitemid 43905792)
30. Hawley SA, Davison M, Woods A, Davies SP, Beri RK, Carling D, Hardie DG (1996). Characterization of the AMP-activated protein kinase kinase from rat liver and identification of threonine 172 as the major site at which it phosphorylates AMP-activated protein kinase. J Biol Chem 271, 27879-27887. (Pubitemid 26367365)
31. Hawley SA, Pan DA, Mustard KJ, Ross L, Bain J, Edelman AM, Frenguelli BG, Hardie DG (2005). Calmodulin-dependent protein kinase kinase-beta is an alternative upstream kinase for AMP-activated protein kinase. Cell Metab 2, 9-19. (Pubitemid 43239821)
32. Holmes B, Dohm GL (2004). Regulation of GLUT4 gene expression during exercise. Med Sci Sports Exerc 36, 1202-1206. (Pubitemid 38878996)
33. Horman S, Browne G, Krause U, Patel J, Vertommen D, Bertrand L, Lavoinne A, Hue L, Proud C, Rider M (2002). Activation of AMP-activated protein kinase leads to the phosphorylation of elongation factor 2 and an inhibition of protein synthesis. Curr Biol 12, 1419-1423.
34. Hurley RL, Anderson KA, Franzone JM, Kemp BE, Means AR, Witters LA (2005). The Ca2+/calmodulin-dependent protein kinase kinases are AMP-activated protein kinase kinases. J Biol Chem 280, 29060-29066.
35. Inoki K, Zhu T, Guan KL (2003). TSC2 mediates cellular energy response to control cell growth and survival. Cell 115, 577-590. (Pubitemid 37506046)
36. Johnson EC, Kazgan N, Bretz CA, Forsberg LJ, Hector CE, Worthen RJ, Onyenwoke R, Brenman JE (2010). Altered metabolism and persistent starvation behaviors caused by reduced AMPK function in Drosophila. PLoS One 5, piie12799.
37. Jones RG, Plas DR, Kubek S, Buzzai M, Mu J, Xu Y, Birnbaum MJ, Thompson CB (2005). AMP-activated protein kinase induces a p53-dependent metabolic checkpoint. Mol Cell 18, 283-293. (Pubitemid 41350534)
38. Kazgan N, Williams T, Forsberg LJ, Brenman JE (2010). Identification of a nuclear export signal in the catalytic subunit of AMP-activated protein kinase. Mol Biol Cell 21, 3433-3442.
39. Kim J, Kundu M, Viollet B, Guan KL (2011). AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol 13, 132-141.
40. Krishnan KS, Rikhy R, Rao S, Shivalkar M, Mosko M, Narayanan R, Etter P, Estes PS, Ramaswami M (2001). Nucleoside diphosphate kinase, a source of GTP, is required for dynamin-dependent synaptic vesicle recycling. Neuron 30, 197-210. (Pubitemid 32441687)
41. Lamia KA et al. (2009). AMPK regulates the circadian clock by cryptochrome phosphorylation and degradation. Science 326, 437-440.
42. Lee JH et al. (2007). Energy-dependent regulation of cell structure by AMP-activated protein kinase. Nature 447, 1017-1020. (Pubitemid 46975745)
43. Lee M, Hwang JT, Lee HJ, Jung SN, Kang I, Chi SG, Kim SS, Ha J (2003). AMP-activated protein kinase activity is critical for hypoxia-inducible factor-1 transcriptional activity and its target gene expression under hypoxic conditions in DU145 cells. J Biol Chem 278, 39653-39661. (Pubitemid 37248526)
44. Liang J et al. (2007). The energy sensing LKB1-AMPK pathway regulates p27(kip1) phosphorylation mediating the decision to enter autophagy or apoptosis. Nat Cell Biol 9, 218-224. (Pubitemid 46420865)
45. MacDonald NJ, De la Rosa A, Benedict MA, Freije JM, Krutsch H, Steeg PS (1993). A serine phosphorylation of Nm23, and not its nucleoside diphosphate kinase activity, correlates with suppression of tumor metastatic potential. J Biol Chem 268, 25780-25789. (Pubitemid 23358195)
46. Merrill GF, Kurth EJ, Hardie DG, Winder WW (1997). AICA riboside increases AMP-activated protein kinase, fatty acid oxidation, and glucose uptake in rat muscle. Am J Physiol 273, E1107-E1112.
47. Mirouse V, Swick LL, Kazgan N, St Johnston D, Brenman JE (2007). LKB1 and AMPK maintain epithelial cell polarity under energetic stress. J Cell Biol 177, 387-392. (Pubitemid 46718268)
48. Mitchelhill KI, Stapleton D, Gao G, House C, Michell B, Katsis F, Witters LA, Kemp BE (1994). Mammalian AMP-activated protein kinase shares structural and functional homology with the catalytic domain of yeast Snf1 protein kinase. J Biol Chem 269, 2361-2364. (Pubitemid 24235720)
49. Montagne J, Stewart MJ, Stocker H, Hafen E, Kozma SC, Thomas G (1999). Drosophila S6 kinase: a regulator of cell size. Science 285, 2126-2129. (Pubitemid 29451430)
50. Nallamothu G, Woolworth JA, Dammai V, Hsu T (2008). Awd, the homolog of metastasis suppressor gene Nm23, regulates Drosophila epithelial cell invasion. Mol Cell Biol 28, 1964-1973. (Pubitemid 351342627)
51. Nielsen JN, Mustard KJ, Graham DA, Yu H, MacDonald CS, Pilegaard H, Goodyear LJ, Hardie DG, Richter EA, Wojtaszewski JF (2003). 5′-AMP- activated protein kinase activity and subunit expression in exercise-trained human skeletal muscle. J Appl Physiol 94, 631-641. (Pubitemid 36158241)
52. Osorio C, Sullivan PM, He DN, Mace BE, Ervin JF, Strittmatter WJ, Alzate O (2007). Mortalin is regulated by APOE in hippocampus of AD patients and by human APOE in TR mice. Neurobiol Aging 28, 1853-1862. (Pubitemid 47539697)
53. Pinaud R, Osorio C, Alzate O, Jarvis ED (2008). Profiling of experience-regulated proteins in the songbird auditory forebrain using quantitative proteomics. Eur J Neurosci 27, 1409-1422. (Pubitemid 351406259)
54. Proud CG (2004). Role of mTOR signalling in the control of translation initiation and elongation by nutrients. Curr Top Microbiol Immunol 279, 215-244.
55. Randazzo PA, Northup JK, Kahn RA (1991). Activation of a small GTP-binding protein by nucleoside diphosphate kinase. Science 254, 850-853. (Pubitemid 21917411)
56. Rosengard AM, Krutzsch HC, Shearn A, Biggs JR, Barker E, Margulies IM, King CR, Liotta LA, Steeg PS (1989). Reduced Nm23/Awd protein in tumour metastasis and aberrant Drosophila development. Nature 342, 177-180.
57. Rubenstein EM, McCartney RR, Zhang C, Shokat KM, Shirra MK, Arndt KM, Schmidt MC (2008). Access denied: Snf1 activation loop phosphorylation is controlled by availability of the phosphorylated threonine 210 to the PP1 phosphatase. J Biol Chem 283, 222-230.
58. Sanders MJ, Grondin PO, Hegarty BD, Snowden MA, Carling D (2007). Investigating the mechanism for AMP activation of the AMP-activated protein kinase cascade. Biochem J 403, 139-148. (Pubitemid 46569875)
59. Shackelford DB, Shaw RJ (2009). The LKB1-AMPK pathway: metabolism and growth control in tumour suppression. Nat Rev Cancer 9, 563-575.
60. Shaw RJ (2006). Glucose metabolism and cancer. Curr Opin Cell Biol 18, 598-608.
61. Shaw RJ (2009). LKB1 and AMP-activated protein kinase control of mTOR signalling and growth. Acta Physiol (Oxf) 196, 65-80.
62. Shaw RJ, Kosmatka M, Bardeesy N, Hurley RL, Witters LA, DePinho RA, Cantley LC (2004). The tumor suppressor LKB1 kinase directly activates AMP-activated kinase and regulates apoptosis in response to energy stress. Proc Natl Acad Sci USA 101, 3329-3335. (Pubitemid 38338195)
63. Stapleton D et al. (1996). Mammalian AMP-activated protein kinase subfamily. J Biol Chem 271, 611-614. (Pubitemid 26034902)
64. Tepper AD, Dammann H, Bominaar AA, Veron M (1994). Investigation of the active site and the conformational stability of nucleoside diphosphate kinase by site-directed mutagenesis. J Biol Chem 269, 32175-32180.
65. Timmons L, Hersperger E, Woodhouse E, Xu J, Liu LZ, Shearn A (1993). The expression of the Drosophila awd gene during normal development and in neoplastic brain tumors caused by lgl mutations. Dev Biol 158, 364-379. (Pubitemid 23243894)
66. Timmons L, Xu J, Hersperger G, Deng XF, Shearn A (1995). Point mutations in awdKpn which revert the prune/Killer of prune lethal interaction affect conserved residues that are involved in nucleoside diphosphate kinase substrate binding and catalysis. J Biol Chem 270, 23021-23030.
67. Treharne KJ, Best OG, Mehta A (2009). The phosphorylation status of membrane-bound nucleoside diphosphate kinase in epithelia and the role of AMP. Mol Cell Biochem 329, 107-114.
68. Venerando A, Pagano MA, Tosoni K, Meggio F, Cassidy D, Stobbart M, Pinna LA, Mehta A (2011). Understanding protein kinase CK2 mis-regulation upon F508del CFTR expression. Naunyn Schmiedebergs Arch Pharmacol 384, 473-488.
69. Watts JL, Morton DG, Bestman J, Kemphues KJ (2000). The C. elegans par-4 gene encodes a putative serine-threonine kinase required for establishing embryonic asymmetry. Development 127, 1467-1475. (Pubitemid 30232597)
70. Williams T, Brenman JE (2008). LKB1 and AMPK in cell polarity and division. Trends Cell Biol 18, 193-198.
71. Williams T, Courchet J, Viollet B, Brenman JE, Polleux F (2011). AMP-activated protein kinase (AMPK) activity is not required for neuronal development but regulates axogenesis during metabolic stress. Proc Natl Acad Sci USA 108, 5849-5854.
72. Winder WW, Wilson HA, Hardie DG, Rasmussen BB, Hutber CA, Call GB, Clayton RD, Conley LM, Yoon S, Zhou B (1997). Phosphorylation of rat muscle acetyl-CoA carboxylase by AMP-activated protein kinase and protein kinase A. J Appl Physiol 82, 219-225. (Pubitemid 27052064)
73. Zhai B, Villen J, Beausoleil SA, Mintseris J, Gygi SP (2008). Phosphoproteome analysis of Drosophila melanogaster embryos. J Proteome Res 7, 1675-1682.