The power to reduce: Pyridine nucleotides - Small molecules with a multitude of functions

Biochemical Journal

Volumn 402, Issue 2, 2007, Pages 205-218

  Pollak, Nadine ^a   Dölle, Christian ^a   Ziegler, Mathias ^a  

^a UNIVERSITY OF BERGEN   (Norway)

Author keywords

ADP ribosylation; Calcium signalling; NAD kinase (NADK); NAD(P)(H); Oxidative stress

Indexed keywords

MECHANICAL ALLOYING; OXIDATIVE STRESS; PROTEINS; PYRIDINE; TRANSDUCERS;

ADP RIBOSYLATION; CALCIUM SIGNALING; NAD KINASE (NADK); NAD(P)(H);

NUCLEOTIDES;

CYCLIC ADENOSINE DIPHOSPHATE RIBOSE; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; NICOTINIC ACID DERIVATIVE; PYRIDINE NUCLEOTIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE KINASE; PHOSPHOTRANSFERASE; REACTIVE OXYGEN METABOLITE;

ADENOSINE DIPHOSPHATE RIBOSYLATION; BIOSYNTHESIS; CELL FUNCTION; ENZYME SYNTHESIS; EUKARYOTE; NONHUMAN; OXIDATIVE STRESS; PHOSPHORYLATION; PRIORITY JOURNAL; PROKARYOTE; REVIEW; YEAST; ANIMAL; CHEMISTRY; ENZYME SPECIFICITY; HUMAN; METABOLISM; SIGNAL TRANSDUCTION;

ANIMALS; HUMANS; NAD; NADP; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; SUBSTRATE SPECIFICITY;

EID: 33847711060     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20061638     Document Type: Review

References (170)

1. Berger, F., Ramirez-Hernandez, M. H. and Ziegler, M. (2004) The new life of a centenarian: signalling functions of NAD(P). Trends Biochem. Sci. 29, 111-118
2. + synthesis. Adv. Enzymol. Relat. Areas Mol. Biol. 73, 135-182
3. + homeostasis in man. Cell. Mol. Life Sci. 61, 19-34
4. Katoh, A., Uenohara, K., Akita, M. and Hashimoto, T. (2006) Early steps in the biosynthesis of NAD in Arabidopsis start with aspartate and occur in the plastid. Plant Physiol. 141, 851-857
5. Berger, F., Lau, C., Dahlmann, M. and Ziegler, M. (2005) Subcellular compartmentation and differential catalytic properties of the three human nicotinamide mononucleotide adenylyltransferase isoforms. J. Biol. Chem. 280, 36334-36341
6. + in fungi and humans. Cell 117, 495-502
7. Sasiak, K. and Saunders, P. P. (1996) Purification and properties of a human nicotinamide ribonucleoside kinase. Arch. Biochem. Biophys. 333, 414-418
8. Chambon, P., Weill, J. D. and Mandel, P. (1963) Nicotinamide mononucleotide activation of new DNA-dependent polyadenylic acid synthesizing nuclear enzyme. Biochem. Biophys. Res. Commun. 11, 39-43
9. Honjo, T., Nishizuka, Y. and Hayaishi, O. (1968) Diphtheria toxin-dependent adenosine diphosphate ribosylation of aminoacyl transferase II and inhibition of protein synthesis. J. Biol. Chem. 243, 3553-3555
10. Paone, G., Wada, A., Stevens, L. A., Matin, A., Hirayama, T., Levine, R. L. and Moss, J. (2002) ADP ribosylation of human neutrophil peptide-1 regulates its biological properties. Proc. Natl. Acad. Sci. U.S.A. 99, 8231-8235
11. Corda, D. and Di Girolamo, M. (2003) Functional aspects of protein mono-ADP-ribosylation. EMBO J. 22, 1953-1958
12. Takamura-Enya, T., Watanabe, M., Totsuka, Y., Kanazawa, T., Matsushima-Hibiya, Y., Koyama, K., Sugimura, T. and Wakabayashi, K. (2001) Mono(ADP-ribosyl)ation of 2′-deoxyguanosine residue in DNA by an apoptosis-inducing protein, pierisin-1, from cabbage butterfly. Proc. Natl. Acad. Sci. U.S.A. 98, 12414-12419
13. Di Girolamo, M., Dani, N., Stilla, A. and Corda, D. (2005) Physiological relevance of the endogenous mono(ADP-ribosyl)ation of cellular proteins. FEBS J. 272, 4565-4575
14. Haigis, M. C., Mostoslavsky, R., Haigis, K. M., Fahie, K., Christodoulou, D. C., Murphy, A. J., Valenzuela, D. M., Yancopoulos, G. D., Karow, M., Blander, G. et al. (2006) SIRT4 inhibits glutamate dehydrogenase and opposes the effects of calorie restriction in pancreatic β cells. Cell 126, 941-954
15. Herrero-Yraola, A., Bakhit, S. M., Franke, P., Weise, C., Schweiger, M., Jorcke, D. and Ziegler, M. (2001) Regulation of glutamate dehydrogenase by reversible ADP-ribosylation in mitochondria. EMBO J. 20, 2404-2412
16. Otto, H., Reche, P. A., Bazan, F., Dittmar, K., Haag, F. and Koch-Nolte, F. (2005) In silico characterization of the family of PARP-like poly(ADP-ribosyl)transferases (pARTs). BMC Genomics 6, 139
17. Schreiber, V., Dantzer, F., Ame, J. C. and de Murcia, G. (2006) Poly(ADP-ribose): novel functions for an old molecule. Nat. Rev. Mol. Cell Biol. 7, 517-528
18. +. FEBS J. 272, 4576-4589
19. d'Adda di Fagagna, F., Hande, M. P., Tong, W. M., Lansdorp, P. M., Wang, Z. Q. and Jackson, S. P. (1999) Functions of poly(ADP-ribose) polymerase in controlling telomere length and chromosomal stability. Nat. Genet. 23, 76-80
20. Kraus, W. L. and Lis, J. T. (2003) PARP goes transcription. Cell 113, 677-683
21. Kanai, M., Tong, W. M., Sugihara, E., Wang, Z. Q., Fukasawa, K. and Miwa, M. (2003) Involvement of poly(ADP-ribose) polymerase 1 and poly(ADP-ribosyl) ation in regulation of centrosome function. Mol. Cell. Biol. 23, 2451-2462
22. Chi, N. W. and Lodish, H. F. (2000) Tankyrase is a golgi-associated mitogen-activated protein kinase substrate that interacts with IRAP in GLUT4 vesicles. J. Biol. Chem. 275, 38437-38444
23. Culver, G. M., McCraith, S. M., Zillmann, M., Kierzek, R., Michaud, N., LaReau, R. D., Turner, D. H. and Phizicky, E. M. (1993) An NAD derivative produced during transfer RNA splicing: ADP-ribose 1″-2″ cyclic phosphate. Science 261, 206-208
24. Perraud, A. L., Fleig, A., Dunn, C. A., Bagley, L. A., Launay, P., Schmitz, C., Stokes, A. J., Zhu, Q., Bessman, M. J., Penner, R. et al. (2001) ADP-ribose gating of the calcium-permeable LTRPC2 channel revealed by Nudix motif homology. Nature 411, 595-599
25. Vu, C. Q., Lu, P. J., Chen, C. S. and Jacobson, M. K. (1996) 2′-Phospho-cyclic ADP-ribose, a calcium-mobilizing agent derived from NADP. J. Biol. Chem. 271, 4747-4754
26. Basile, G., Taglialatela-Scafati, O., Damonte, G., Armirotti, A., Bruzzone, S., Guida, L., Franco, L., Usai, C., Fattorusso, E., De Flora, A. and Zocchi, E. (2005) ADP-ribosyl cyclases generate two unusual adenine homodinucleotides with cytotoxic activity on mammalian cells. Proc. Natl. Acad. Sci. U.S.A. 102, 14509-14514
27. Hellmich, M. R. and Strumwasser, F. (1991) Purification and characterization of a molluscan egg-specific NADase, a second-messenger enzyme. Cell Regul. 2, 193-202
28. Lee, H. C. (1997) Mechanisms of calcium signaling by cyclic ADP-ribose and NAADP. Physiol. Rev. 77, 1133-1164
29. +/cyclic ADP-ribose system. Ann. N.Y. Acad. Sci. 1028, 176-191
30. +-glycohydrolase in brain from CD38-deficient mice. J. Biol. Chem. 278, 40670-40678
31. 2+ signals in pancreatic acinar and β cells. J. Biol. Chem. 279, 7234-7240
32. Chini, E. N. and De Toledo, F. G. (2002) Nicotinic acid adenine dinucleotide phosphate: a new intracellular second messenger? Am. J. Physiol. Cell Physiol. 282, C1191-C1198
33. 2+-dependent phosphatase. Biochem. J. 365, 295-301
34. Tanner, K. G., Landry, J., Sternglanz, R. and Denu, J. M. (2000) Silent information regulator 2 family of NAD-dependent histone/protein deacetylases generates a unique product, 1-O-acetyl-ADP-ribose. Proc. Natl. Acad. Sci. U.S.A. 97, 14178-14182
35. Blander, G. and Guarente, L. (2004) The Sir2 family of protein deacetylases. Annu. Rev. Biochem. 73, 417-435
36. Frye, R. A. (1999) Characterization of five human cDNAs with homology to the yeast SIR2 gene: Sir2-like proteins (sirtuins) metabolize NAD and may have protein ADP-ribosyltransferase activity. Biochem. Biophys. Res. Commun. 260, 273-279
37. +-dependent histone/protein deacetylases. J. Biol. Chem. 277, 18535-18544
38. Grubisha, O., Rafty, L. A., Takanishi, C. L., Xu, X., Tong, L., Perraud, A. L., Scharenberg, A. M. and Denu, J. M. (2006) Metabolite of SIR2 reaction modulates TRPM2 ion channel. J. Biol. Chem. 281, 14057-14065
39. Liou, G. G., Tanny, J. C., Kruger, R. G., Walz, T. and Moazed, D. (2005) Assembly of the SIR complex and its regulation by O-acetyl-ADP-ribose, a product of NAD-dependent histone deacetylation. Cell 121, 515-527
40. Zhang, Q., Piston, D. W. and Goodman, R. H. (2002) Regulation of corepressor function by nuclear NADH. Science 295, 1895-1897
41. Williamson, D. H., Lund, P. and Krebs, H. A. (1967) The redox state of free nicotinamide-adenine dinucleotide in the cytoplasm and mitochondria of rat liver. Biochem. J. 103, 514-527
42. Veech, R. L., Eggleston, L. V. and Krebs, H. A. (1969) The redox state of free nicotinamide-adenine dinucleotide phosphate in the cytoplasm of rat liver. Biochem. J. 115, 609-619
43. Finkel, T. and Holbrook, N. J. (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408, 239-247
44. Droge, W. (2003) Oxidative stress and aging. Adv. Exp. Med. Biol. 543, 191-200
45. Klaunig, J. E. and Kamendulis, L. M. (2004) The role of oxidative stress in carcinogenesis. Annu. Rev. Pharmacol. Toxicol. 44, 239-267
46. Valko, M., Izakovic, M., Mazur, M., Rhodes, C. J. and Telser, J. (2004) Role of oxygen radicals in DNA damage and cancer incidence. Mol. Cell. Biochem. 266, 37-56
47. Berg, D., Youdim, M. B. and Riederer, P. (2004) Redox imbalance. Cell Tissue Res. 318, 201-213
48. Zhu, X., Lee, H. G., Casadesus, G., Avila, J., Drew, K., Perry, G. and Smith, M. A. (2005) Oxidative imbalance in Alzheimer's disease. Mol. Neurobiol. 31, 205-217
49. Obrosova, I., Faller, A., Burgan, J., Ostrow, E. and Williamson, J. R. (1997) Glycolytic pathway, redox state of NAD(P)-couples and energy metabolism in lens in galactose-fed rats: effect of an aldose reductase inhibitor. Curr. Eye Res. 16, 34-43
50. Lakowicz, J. R., Szmacinski, H., Nowaczyk, K. and Johnson, M. L. (1992) Fluorescence lifetime imaging of free and protein-bound NADH. Proc. Natl. Acad. Sci. U.S.A. 89, 1271-1275
51. Lin, S. J. and Guarente, L. (2003) Nicotinamide adenine dinucleotide, a metabolic regulator of transcription, longevity and disease. Curr. Opin. Cell Biol. 15, 241-246
52. Canepa, L., Ferraris, A. M., Miglino, M. and Gaetani, G. F. (1991) Bound and unbound pyridine dinucleotides in normal and glucose-6-phosphate dehydrogenase-deficient erythrocytes. Biochim. Biophys. Acta 1074, 101-104
53. Mack, T. G., Reiner, M., Beirowski, B., Mi, W., Emanuelli, M., Wagner, D., Thomson, D., Gillingwater, T., Court, F., Conforti, L. et al. (2001) Wallerian degeneration of injured axons and synapses is delayed by a Ube4b/Nmnat chimeric gene. Nat. Neurosci. 4, 1199-1206
54. + levels. J. Biol. Chem. 277, 18881-18890
55. Sims, J. L., Berger, S. J. and Berger, N. A. (1983) Poly(ADP-ribose) polymerase inhibitors preserve nicotinamide adenine dinucleotide and adenosine 5′-triphosphate pools in DNA-damaged cells: mechanism of stimulation of unscheduled DNA synthesis. Biochemistry 22, 5188-5194
56. + repletion prevents PARP-1-induced glycolytic blockade and cell death in cultured mouse astrocytes. Biochem. Biophys. Res. Commun. 308, 809-813
57. Rydstrom, J., Hoek, J. B. and Ernster, L. (1976) Nicotinamide nucleotide transhydrogenases. In The Enzymes (Boyer, P.D., ed.), pp. 51-88, Academic Press, New York
58. Kletzien, R. F., Harris, P. K. and Foellmi, L. A. (1994) Glucose-6-phosphate dehydrogenase: a "housekeeping" enzyme subject to tissue-specific regulation by hormones, nutrients, and oxidant stress. FASEB J. 8, 174-181
59. Stanton, R. C., Seifter, J. L., Boxer, D. C., Zimmerman, E. and Cantley, L. C. (1991) Rapid release of bound glucose-6-phosphate dehydrogenase by growth factors. Correlation with increased enzymatic activity. J. Biol. Chem. 266, 12442-12448
60. Tian, W. N., Pignatare, J. N. and Stanton, R. C. (1994) Signal transduction proteins that associate with the platelet-derived growth factor (PDGF) receptor mediate the PDGF-induced release of glucose-6-phosphate dehydrogenase from permeabilized cells. J. Biol. Chem. 269, 14798-14805
61. Beutler, E. and West, C. (1978) Glucose-6-phosphate dehydrogenase variants in the chimpanzee. Biochem. Med. 20, 364-370
62. Luzzatto, L. (1993) Glucose 6-phosphate dehydrogenase deficiency and hemolytic anemia. In Hematology of Infancy and Childhood. (Nathan, D. G. and Oski, D. F., eds), pp. 674-691, W. B. Saunders, Philadelphia
63. Weber, G. (1987), Strongly conserved segment of gene expression in cancer cells. In Modulation of Liver Cell Expression (W. Reutter, H. Popper, I. M. Arias, P. C. Heinrich, D. Keppler, and L. Landmann, eds), pp. 303-314, MTP, Lancaster
64. Nogae, I. and Johnston, M. (1990) Isolation and characterization of the ZWF1 gene of Saccharomyces cerevisiae, encoding glucose-6-phosphate dehydrogenase. Gene 96, 161-169
65. Pandolfi, P. P., Sonati, F., Rivi, R., Mason, P., Grosveld, F. and Luzzatto, L. (1995) Targeted disruption of the housekeeping gene encoding glucose 6-phosphate dehydrogenase (G6PD): G6PD is dispensable for pentose synthesis but essential for defense against oxidative stress. EMBO J. 14, 5209-5215
66. Longo, L., Vanegas, O. C., Patel, M., Rosti, V., Li, H., Waka, J., Merghoub, T., Pandolfi, P. P., Notaro, R., Manova, K. and Luzzatto, L. (2002) Maternally transmitted severe glucose 6-phosphate dehydrogenase deficiency is an embryonic lethal. EMBO J. 21, 4229-4239
67. Filosa, S., Fico, A., Paglialunga, F., Balestrieri, M., Crooke, A., Verde, P., Abrescia, P., Bautista, J. M. and Martini, G. (2003) Failure to increase glucose consumption through the pentose-phosphate pathway results in the death of glucose-6-phosphate dehydrogenase gene-deleted mouse embryonic stem cells subjected to oxidative stress. Biochem. J. 370, 935-943
68. Fico, A., Paglialunga, F., Cigliano, L., Abrescia, P., Verde, P., Martini, G., Iaccarino, I. and Filosa, S. (2004) Glucose-6-phosphate dehydrogenase plays a crucial role in protection from redox-stress-induced apoptosis. Cell Death Differ. 11, 823-831
69. Ursini, M. V., Parrella, A., Rosa, G., Salzano, S. and Martini, G. (1997) Enhanced expression of glucose-6-phosphate dehydrogenase in human cells sustaining oxidative stress. Biochem. J. 323, 801-806
70. Salvemini, F., Franze, A., Iervolino, A., Filosa, S., Salzano, S. and Ursini, M. V. (1999) Enhanced glutathione levels and oxidoresistance mediated by increased glucose-6-phosphate dehydrogenase expression. J. Biol. Chem. 274, 2750-2757
71. Tian, W. N., Braunstein, L. D., Apse, K., Pang, J., Rose, M., Tian, X. and Stanton, R. C. (1999) Importance of glucose-6-phosphate dehydrogenase activity in cell death. Am. J. Physiol. 276, C1121-C1131
72. Haselbeck, R. J. and McAlister-Henn, L. (1991) Isolation, nucleotide sequence, and disruption of the Saccharomyces cerevisiae gene encoding mitochondrial NADP(H)-specific isocitrate dehydrogenase. J. Biol. Chem. 266, 2339-2345
73. Loftus, T. M., Hall, L. V., Anderson, S. L. and McAlister-Henn, L. (1994) Isolation, characterization, and disruption of the yeast gene encoding cytosolic NADP-specific isocitrate dehydrogenase. Biochemistry 33, 9661-9667
74. Henke, B., Girzalsky, W., Berteaux-Lecellier, V. and Erdmann, R. (1998) IDP3 encodes a peroxisomal NADP-dependent isocitrate dehydrogenase required for the β-oxidation of unsaturated fatty acids. J. Biol. Chem. 273, 3702-3711
75. +-specific isocitrate dehydrogenases in Saccharomyces cerevisiae. J. Biol. Chem. 273, 31486-31493
76. Boles, E., de Jong-Gubbels, P. and Pronk, J. T. (1998) Identification and characterization of MAE1, the Saccharomyces cerevisiae structural gene encoding mitochondrial malic enzyme. J. Bacteriol. 180, 2875-2882
77. Grabowska, D. and Chelstowska, A. (2003) The ALD6 gene product is indispensable for providing NADPH in yeast cells lacking glucose-6-phosphate dehydrogenase activity. J. Biol. Chem. 278, 13984-13988
78. Minard, K. I. and McAlister-Henn, L. (2005) Sources of NADPH in yeast vary with carbon source. J. Biol. Chem. 280, 39890-39896
79. Plaut, G. W., Cook, M. and Aogaichi, T. (1983) The subcellular location of isozymes of NADP-isocitrate dehydrogenase in tissues from pig, ox and rat. Biochim. Biophys. Acta 760, 300-308
80. Yoshihara, T., Hamamoto, T., Munakata, R., Tajiri, R., Ohsumi, M. and Yokota, S. (2001) Localization of cytosolic NADP-dependent isocitrate dehydrogenase in the peroxisomes of rat liver cells: biochemical and immunocytochemical studies. J. Histochem. Cytochem. 49, 1123-1131
81. +-dependent isocitrate dehydrogenase. J. Biol. Chem. 276, 16168-16176
82. +-ICDH) on cellular defence against oxidative injury by γ-rays. Int. J. Radiat. Biol. 80, 635-642
83. +-dependent isocitrate dehydrogenase plays a key role in lipid metabolism. J. Biol. Chem. 279, 39968-39974
84. + -dependent isocitrate dehydrogenase. Free Radical Res. 39, 441-448
85. Lee, S. M., Koh, H. J., Park, D. C., Song, B. J., Huh, T. L. and Park, J. W. (2002) Cytosolic NADP(+)-dependent isocitrate dehydrogenase status modulates oxidative damage to cells. Free Radical Biol. Med. 32, 1185-1196
86. Bukato, G., Kochan, Z. and Swierczynski, J. (1995) Purification and properties of cytosolic and mitochondrial malic enzyme isolated from human brain. Int. J. Biochem. Cell Biol. 27, 47-54
87. Frenkel, R. (1971) Bovine heart malic enzyme. I. Isolation and partial purification of a cytoplasmic and a mitochondrial enzyme. J. Biol. Chem. 246, 3069-3074
88. Sanz, N., Diez-Fernandez, C., Valverde, A. M., Lorenzo, M., Benito, M. and Cascales, M. (1997) Malic enzyme and glucose 6-phosphate dehydrogenase gene expression increases in rat liver cirrhogenesis. Br. J. Cancer. 75, 487-492
89. Diez-Fernandez, C., Sanz, N. and Cascales, M. (1996) Changes in glucose-6-phosphate dehydrogenase and malic enzyme gene expression in acute hepatic injury induced by thioacetamide. Biochem. Pharmacol. 51, 1159-1163
90. McKenna, M. C., Stevenson, J. H., Huang, X., Tildon, J. T., Zielke, C. L. and Hopkins, I. B. (2000) Mitochondrial malic enzyme activity is much higher in mitochondria from cortical synaptic terminals compared with mitochondria from primary cultures of cortical neurons or cerebellar granule cells. Neurochem. Int. 36, 451-459
91. MacDonald, M. J. (1995) Feasibility of a mitochondrial pyruvate malate shuttle in pancreatic islets. Further implication of cytosolic NADPH in insulin secretion. J. Biol. Chem. 270, 20051-20058
92. Vasiliou, V. and Nebert, D. W. (2005) Analysis and update of the human aldehyde dehydrogenase (ALDH) gene family. Hum. Genomics 2, 138-143
93. Pappa, A., Sophos, N. A. and Vasiliou, V. (2001) Corneal and stomach expression of aldehyde dehydrogenases: from fish to mammals. Chem. Biol. Interact. 130-132, 181-191
94. Pappa, A., Chen, C., Koutalos, Y., Townsend, A. J. and Vasiliou, V. (2003) Aldh3a1 protects human corneal epithelial cells from ultraviolet- and 4-hydroxy-2-nonenal-induced oxidative damage. Free Radical Biol. Med. 34, 1178-1189
95. Fisher, R. R. and Kaplan, N. O. (1973) Studies on the mitochondrial energy-linked pyridine nucleotide transhydrogenase. Biochemistry 12, 1182-1188
96. Hoek, J. B. and Rydstrom, J. (1988) Physiological roles of nicotinamide nucleotide transhydrogenase. Biochem. J. 254, 1-10
97. Rydstrom, J. (2006) Mitochondrial NADPH, transhydrogenase and disease. Biochim. Biophys. Acta 1757, 721-726
98. Gerdes, S. Y., Scholle, M. D., D'Souza, M., Bernal, A., Baev, M. V., Farrell, M., Kurnasov, O. V., Daugherty, M. D., Mseeh, F., Polanuyer, B. M. et al. (2002) From genetic footprinting to antimicrobial drug targets: examples in cofactor biosynthetic pathways. J. Bacteriol. 184, 4555-4572
99. Grose, J. H., Joss, L., Velick, S. F. and Roth, J. R. (2006) Evidence that feedback inhibition of NAD kinase controls responses to oxidative stress. Proc. Natl. Acad. Sci. U.S.A. 103, 7601-7606
100. Kobayashi, K., Ehrlich, S. D., Albertini, A., Amati, G., Andersen, K. K., Arnaud, M., Asai, K., Ashikaga, S., Aymerich, S., Bessieres, P. et al. (2003) Essential Bacillus subtilis genes. Proc. Natl. Acad. Sci. U.S.A. 100, 4678-4683
101. Sassetti, C. M., Boyd, D. H. and Rubin, E. J. (2003) Genes required for mycobacterial growth defined by high density mutagenesis. Mol. Microbiol. 48, 77-84
102. Bieganowski, P., Seidle, H. F., Wojcik, M. and Brenner, C. (2006) Synthetic lethal and biochemical analyses of NAD and NADH kinases in Saccharomyces cerevisiae establish separation of cellular functions. J. Biol. Chem. 281, 22439-22445
103. Shianna, K. V., Marchuk, D. A. and Strand, M. K. (2006) Genomic characterization of POS5, the Saccharomyces cerevisiae mitochondrial NADH kinase. Mitochondrion 6, 94-101
104. Vestin, R. (1937) Enzymic change from codehydrogenase I to codehydrogenase II. Naturwissenschaften 25, 667-668
105. von Euler, H. and Adler, E. (1938) Enzymic intertransformation of codehydrogenase I and cohydrogenase II. Z. Physiol. Chem. 252, 41-48
106. Kornberg, A. (1950) Enzymatic synthesis of triphosphopyridine nucleotide. J. Biol. Chem. 182, 805-813
107. Apps, D. K. (1968) Kinetic Studies of pigeon liver NAD kinase. Eur. J. Biochem. 5, 444-450
108. Fernandes, M. (1970) Properties of rat brain NAD-kinase. J. Neurochem. 17, 503-509
109. Nemchinskaia, V. L. and Smirnova, T. B. (1967) Isolation and properties of NAD kinase from rat liver. Biokhimiia 32, 854-858
110. + kinase: purification, properties and affinity gel studies. Int. J. Biochem. 14, 839-844
111. Tseng, Y. M., Harris, B. G. and Jacobson, M. K. (1979) Isolation and characterization of yeast nicotinamide adenine dinucleotide kinase. Biochim. Biophys. Acta 568, 205-214
112. Yamamoto, Y. (1966) NAD kinase in higher plants. Plant Physiol. 41, 523-528
113. Kawai, S., Mori, S., Mukai, T., Suzuki, S., Yamada, T., Hashimoto, W. and Murata, K. (2000) Inorganic polyphosphate/ATP-NAD kinase of Micrococcus flavus and Mycobacterium tuberculosis H37Rv. Biochem. Biophys. Res. Commun. 276, 57-63
114. Magni, G., Orsomando, G. and Raffaelli, N. (2006) Structural and functional properties of NAD kinase, a key enzyme in NADP biosynthesis. Mini Rev. Med. Chem. 6, 739-746
115. Labesse, G., Douguet, D., Assairi, L. and Gilles, A. M. (2002) Diacylglyceride kinases, sphingosine kinases and NAD kinases: distant relatives of 6-phosphofructokinases. Trends Biochem. Sci. 27, 273-275
116. Mori, S., Yamasaki, M., Maruyama, Y., Momma, K., Kawai, S., Hashimoto, W., Mikami, B. and Murata, K. (2005) NAD-binding mode and the significance of intersubunit contact revealed by the crystal structure of Mycobacterium tuberculosis NAD kinase-NAD complex. Biochem. Biophys. Res. Commun. 327, 500-508
117. Raffaelli, N., Finaurini, L., Mazzola, F., Pucci, L., Sorci, L., Amici, A. and Magni, G. (2004) Characterization of Mycobacterium tuberculosis NAD kinase: functional analysis of the full-length enzyme by site-directed mutagenesis. Biochemistry 43, 7610-7617
118. Garavaglia, S., Raffaelli, N., Finaurini, L., Magni, G. and Rizzi, M. (2004) A novel fold revealed by Mycobacterium tuberculosis NAD kinase, a key allosteric enzyme in NADP biosynthesis. J. Biol. Chem. 279, 40980-40986
119. Liu, J., Lou, Y., Yokota, H., Adams, P. D., Kim, R. and Kim, S. H. (2005) Crystal structures of an NAD kinase from Archaeoglobus fulgidus in complex with ATP, NAD, or NADP. J. Mol. Biol. 354, 289-303
120. Oganesyan, V., Huang, C., Adams, P. D., Jancarik, J., Yokota, H. A., Kim, R. and Kim, S. H. (2005) Structure of a NAD kinase from Thermotoga maritima at 2.3 Å resolution. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 61, 640-646
121. Rossmann, M. G., Moras, D. and Olsen, K. W. (1974) Chemical and biological evolution of nucleotide-binding protein. Nature 250, 194-199
122. Turner, W. L., Waller, J. C., Vanderbeld, B. and Snedden, W. A. (2004) Cloning and characterization of two NAD kinases from Arabidopsis. Identification of a calmodulin binding isoform. Plant Physiol. 135, 1243-1255
123. Kornberg, A. (1999) Inorganic polyphosphate: a molecule of many functions. Prog. Mol. Subcell. Biol. 23, 1-18
124. Bark, K., Kampfer, P., Sponner, A. and Dott, W. (1993) Polyphosphate-dependent enzymes in some coryneform bacteria isolated from sewage sludge. FEMS Microbiol. Lett. 107, 133-138
125. Berrin, J. G., Pierrugues, O., Brutesco, C., Alonso, B., Montillet, J. L., Roby, D. and Kazmaier, M. (2005) Stress induces the expression of AtNADK-1, a gene encoding a NAD(H) kinase in Arabidopsis thaliana. Mol. Genet. Genomics 273, 10-19
126. Mori, S., Kawai, S., Shi, F., Mikami, B. and Murata, K. (2005) Molecular conversion of NAD kinase to NADH kinase through single amino acid residue substitution. J. Biol. Chem. 280, 24104-24112
127. Lerner, F., Niere, M., Ludwig, A. and Ziegler, M. (2001) Structural and functional characterization of human NAD kinase. Biochem. Biophys. Res. Commun. 288, 69-74
128. Kawai, S., Mori, S., Mukai, T., Hashimoto, W. and Murata, K. (2001) Molecular characterization of Escherichia coli NAD kinase. Eur. J. Biochem. 268, 4359-4365
129. Shi, F., Kawai, S., Mori, S., Kono, E. and Murata, K. (2005) Identification of ATP-NADH kinase isozymes and their contribution to supply of NADP(H) in Saccharomyces cerevisiae. FEBS J. 272, 3337-3349
130. Garavaglia, S., Galizzi, A. and Rizzi, M. (2003) Allosteric regulation of Bacillus subtilis NAD kinase by quinolinic acid. J. Bacteriol. 185, 4844-4850
131. Cheng, W. and Roth, J. R. (1994) Evidence for two NAD kinases in Salmonella typhimurium. J. Bacteriol. 176, 4260-4268
132. Anderson, J. M., Charbonneau, H., Jones, H. P., McCann, R. O. and Cormier, M. J. (1980) Characterization of the plant nicotinamide adenine dinucleotide kinase activator protein and its identification as calmodulin. Biochemistry 19, 3113-3120
133. Epel, D., Patton, C., Wallace, R. W. and Cheung, W. Y. (1981) Calmodulin activates NAD kinase of sea urchin eggs: an early event of fertilization. Cell 23, 543-549
134. Williams, M. B. and Jones, H. P. (1985) Calmodulin-dependent NAD kinase of human neutrophils. Arch. Biochem. Biophys. 237, 80-87
135. Anderson, J. M. and Cormier, M. J. (1978) Calcium-dependent regulation of NAD kinase. Biochem. Biophys. Res. Commun. 84, 595-602
136. Muto, S. and Miyachi, S. (1977) Properties of a protein activator of NAD kinase from plants. Plant Physiol. 59, 55-60
137. Stinemetz, C. L., Kuzmanoff, K. M., Evans, M. L. and Jarrett, H. W. (1987) Correlation between calmodulin activity and gravitropic sensitivity in primary roots of maize. Plant Physiol. 84, 1337-1342
138. 2+, calmodulin-dependent NAD kinase from corn is located in the outer mitochondrial membrane. J. Biol. Chem. 259, 184-189
139. 2+, calmodulin-independent activity in the stroma of pea chloroplasts. FEBS Lett. 167, 332-338
140. Simon, P., Dieter, P., Bonzon, M., Greppin, H. and Marme, D. (1982) Calmodulin-dependent and independent NAD kinase activities from cytoplasmic fractions of spinach (Spinacia oleracea L.). Plant Cell Rep. 1, 119-122
141. Swezey, R. R. and Epel, D. (1995) The in vivo rate of glucose-6-phosphate dehydrogenase activity in sea urchin eggs determined with a photolabile caged substrate. Dev. Biol. 169, 733-744
142. Standart, N. M., Bray, S. J., George, E. L., Hunt, T. and Ruderman, J. V. (1985) The small subunit of ribonucleotide reductase is encoded by one of the most abundant translationally regulated maternal RNAs in clam and sea urchin eggs. J. Cell Biol. 100, 1968-1976
143. Akkaraju, G. R., Hansen, L. J. and Jagus, R. (1991) Increase in eukaryotic initiation factor 2B activity following fertilization reflects changes in redox potential. J. Biol. Chem. 266, 24451-24459
144. Foerder, C. A., Klebanoff, S. J. and Shapiro, B. M. (1978) Hydrogen peroxide production, chemiluminescence, and the respiratory burst of fertilization: interrelated events in early sea urchin development. Proc. Natl. Acad. Sci. U.S.A. 75, 3183-3187
145. Heinecke, J. W. and Shapiro, B. M. (1989) Respiratory burst oxidase of fertilization. Proc. Natl. Acad. Sci. U.S.A. 86, 1259-1263
146. Foerder, C. A. and Shapiro, B. M. (1977) Release of ovoperoxidase from sea urchin eggs hardens the fertilization membrane with tyrosine crosslinks. Proc. Natl. Acad. Sci. U.S.A. 74, 4214-4218
147. + kinase, NADPH reoxidation, and peroxidase activities by physiological concentrations of thyroid stimulating hormone acting in vitro: a quantitative cytochemical study. Endocrinology 123, 2499-2505
148. Harding, S. A., Oh, S. H. and Roberts, D. M. (1997) Transgenic tobacco expressing a foreign calmodulin gene shows an enhanced production of active oxygen species. EMBO J. 16, 1137-1144
149. Zielinski, R. E. (1998) Calmodulin and calmodulin-binding proteins in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49, 697-725
150. Butcher, R. A. and Schreiber, S. L. (2004) Identification of Ald6p as the target of a class of small-molecule suppressors of FK506 and their use in network dissection. Proc. Natl. Acad. Sci. U.S.A. 101, 7868-7873
151. Outten, C. E. and Culotta, V. C. (2003) A novel NADH kinase is the mitochondrial source of NADPH in Saccharomyces cerevisiae. EMBO J. 22, 2015-2024
152. Kawai, S., Suzuki, S., Mori, S. and Murata, K. (2001) Molecular cloning and identification of UTR1 of a yeast Saccharomyces cerevisiae as a gene encoding an NAD kinase. FEMS Microbiol. Lett. 200, 181-184
153. Ghaemmaghami, S., Huh, W. K., Bower, K., Howson, R. W., Belle, A., Dephoure, N., O'Shea, E. K. and Weissman, J. S. (2003) Global analysis of protein expression in yeast. Nature 425, 737-741
154. Krems, B., Charizanis, C. and Entian, K. D. (1995) Mutants of Saccharomyces cerevisiae sensitive to oxidative and osmotic stress. Curr. Genet. 27, 427-434
155. Strand, M. K., Stuart, G. R., Longley, M. J., Graziewicz, M. A., Dominick, O. C. and Copeland, W. C. (2003) POS5 gene of Saccharomyces cerevisiae encodes a mitocliondrial NADH kinase required for stability of mitochondrial DNA. Eukaryotic Cell 2, 809-820
156. + transporter in Saccharomyces cerevisiae. J. Biol. Chem. 281, 1524-1531
157. Douce, R. and Neuburger, M. (1989) The uniqueness of plant mitochondria. Annu. Rev. Plant Physiol. Plant Mol. Biol. 40, 371-414
158. Muto, S. and Miyachi, S. (1981) Light-induced conversion of nicotinamide adenine dinucleotide to nicotinamide adenine dinucleotide phosphate in higher plant leaves. Plant Physiol. 68, 324-328
159. Chai, M. F., Chen, Q. J., An, R., Chen, Y. M., Chen, J. and Wang, X. C. (2005) NADK2, an Arabidopsis chloroplastic NAD kinase, plays a vital role in both chlorophyll synthesis and chloroplast protection. Plant Mol. Biol. 59, 553-564
160. Turner, W. L., Waller, J. C. and Snedden, W. A. (2005) Identification, molecular cloning and functional characterization of a novel NADH kinase from Arabidopsis thaliana (thale cress). Biochem. J. 385, 217-223
161. + kinase in the rat conceptus. Toxicol. Appl. Pharmacol. 170, 124-129
162. Navas, P., Minnifield, N., Sun, I. and Morre, D. J. (1986) NADP phosphatase as a marker in free-flow electrophoretic separations for cisternae of the Golgi apparatus midregion. Biochim. Biophys. Acta 881, 1-9
163. + phosphatase: a novel mitochondrial enzyme. Biochem. Biophys. Res. Commun. 146, 253-257
164. Gallais, S., de Crescenzo, M. A. and Laval-Martin, D. L. (2000) Evidence of active NADP(+) phosphatase in dormant seeds of Avena sativa L. J. Exp. Bot. 51, 1389-1394
165. Reidl, J., Schlor, S., Kraiss, A., Schmidt-Brauns, J., Kemmer, G. and Soleva, E. (2000) NADP and NAD utilization in Haemophilus influenzae. Mol. Microbiol. 35, 1573-1581
166. Goto, K., Laval-Martin, D. L. and Edmunds, Jr, L. N. (1985) Biochemical modeling of an autonomously oscillatory circadian clock in Euglena. Science 228, 1284-1288
167. Laval-Martin, D. L., Carre, I. A., Barbera, S. J. and Edmunds, Jr, L. N. (1990) Rhythmic changes in the activities of NAD kinase and NADP phosphatase in the achlorophyllous ZC mutant of Euglena gracilis Klebs (strain Z). Arch.
168. + balance. J. Basic Microbiol. 44, 185-196
169. Kawai, S., Fukuda, C., Mukai, T. and Murata, K. (2005) MJ0917 in archaeon Methanococcus jannaschii is a novel NADP phosphatase/NAD kinase. J. Biol. Chem. 280, 39200-39207
170. Thompson, J. D., Higgins, D. G. and Gibson, T. J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680