Crystal structure of human nicotinic acid phosphoribosyltransferase

FEBS Open Bio

Volumn 5, Issue , 2015, Pages 419-428

  Marletta, Ada Serena ^a   Massarotti, Alberto ^a   Orsomando, Giuseppe ^b   Magni, Giulio ^b   Rizzi, Menico ^a   Garavaglia, Silvia ^a  

^a UNIVERSITY OF EASTERN PIEDMONT   (Italy)

^b UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

Author keywords

FK866; NAD biosynthesis; Nicotinic Acid; Phosphoribosyltransferase; Preiss Handler pathway; Recycling NAD pathway

Indexed keywords

DAPORINAD; MONOMER; NICOTINAMIDE PHOSPHORIBOSYLTRANSFERASE; NICOTINATE PHOSPHORIBOSYLTRANSFERASE; NICOTINIC ACID; PHOSPHORIBOSYL PYROPHOSPHATE; PHOSPHORIBOSYLTRANSFERASE; PYROPHOSPHATE;

ARTICLE; BINDING SITE; CATALYSIS; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME SPECIFICITY; ENZYME STRUCTURE; HOMEOSTASIS; HUMAN; MOLECULAR DOCKING; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN EXPRESSION;

EUKARYOTA; MAMMALIA;

EID: 84930944269     PISSN: 22115463     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.fob.2015.05.002     Document Type: Article

References (60)

1. Belenky P., Bogan K.L., Brenner C. NAD+ metabolism in health and disease. Trends Biochem. Sci. 2007, 32:12-19.
2. Magni G., Amici A., Emanuelli M., Orsomando G., Raffaelli N., et al. Enzymology of NAD+ homeostasis in man. Cell. Mol. Life Sci. 2004, 61:19-34.
3. Berger F., Ramirez-Hernandez M.H., Ziegler M. The new life of a centenarian: signalling functions of NAD(P). Trends Biochem. Sci. 2004, 29:111-118.
4. Ziegler M. New functions of a long-known molecule. Emerging roles of NAD in cellular signaling. Eur. J. Biochem. 2000, 267:1550-1564.
5. Guse A.H. Second messenger function and the structure-activity relationship of cyclic adenosine diphosphoribose (cADPR). FEBS J. 2005, 272:4590-4597.
6. Marmorstein R. Structure and chemistry of the Sir2 family of NAD+-dependent histone/protein deacetylases. Biochem. Soc. Trans. 2004, 32:904-909.
7. Magni G., Orsomando G., Raffelli N., Ruggieri S. Enzymology of mammalian NAD metabolism in health and disease. Front. Biosci. 2008, 13:6135-6154.
8. Araki T., Sasaki Y., Milbrandt J. Increased nuclear NAD biosynthesis and SIRT1 activation prevent axonal degeneration. Science 2004, 305:1010-1013.
9. Di Stefano M., Conforti L. Diversification of NAD biological role: the importance of location. FEBS J. 2013, 280:4711-4728.
10. Guarente L., Picard F. Calorie restriction - the SIR2 connection. Cell 2005, 120:473-482.
11. Bieganowski P., Brenner C. Discoveries of nicotinamide riboside as a nutrient and conserved NRK genes establish a Preiss-Handler independent route to NAD+ in fungi and humans. Cell 2004, 117:495-502.
12. Magni G., Amici A., Emanuelli M., Raffaelli N., Ruggieri S. Enzymology of NAD+ synthesis. Adv. Enzymol. Relat. Areas Mol. Biol. 1999, 73:135-182.
13. Garavaglia S., D'Angelo I., Emanuelli M., Carnevali F., Pierella F., et al. Structure of human NMN adenylyltransferase. A key nuclear enzyme for NAD homeostasis. J. Biol. Chem. 2002, 277:8524-8530.
14. Zhai R.G., Rizzi M., Garavaglia S. Nicotinamide/nicotinic acid mononucleotide adenylyltransferase, new insights into an ancient enzyme. Cell. Mol. Life Sci. 2009, 66(17):2805-2818.
15. Rizzi M., Bolognesi M., Coda A. A novel deamido-NAD+-binding site revealed by the trapped NAD-adenylate intermediate in the NAD+ synthetase structure. Structure 1998, 6(9):1129-1140.
16. Revollo J.R., Grimm A.A., Imai S. The NAD biosynthesis pathway mediated by nicotinamide phosphoribosyltransferase regulates Sir2 activity in mammalian cells. J. Biol. Chem. 2004, 279:50754-50763.
17. Rongvaux A., Andris F., Van Gool F., Leo O. Reconstructing eukaryotic NAD metabolism. BioEssays 2003, 25:683-690.
18. Mori V.A.A., Mazzola F., Di Stefano M., Conforti L., Magni G., Ruggieri S., Raffaelli N., Orsomando G. Metabolic profiling of alternative NAD biosynthetic routes in mouse tissues. PloSOne 2014, 9(11):1-27.
19. Jackson T.M., Rawling J.M., Roebuck B.D., Kirkland J.B. Large supplements of nicotinic acid and nicotinamide increase tissue NAD+ and poly(ADP-ribose) levels but do not affect diethylnitrosamine-induced altered hepatic foci in Fischer-344 rats. J. Nutr. 1995, 125:1455-1461.
20. Handler P., Kohn H.I. The mechanisms of cozymase synthesis in the human erythrocyte: a comparison of the roles of nicotinic acid and nicotinamide. J. Biol. Chem. 1943, 150:447-452.
21. Henderson L.M. Niacin. Annu. Rev. Nutr. 1983, 3:289-307.
22. Hara N., Yamada K., Shibata T., Osago H., Hashimoto T., et al. Elevation of cellular NAD levels by nicotinic acid and involvement of nicotinic acid phosphoribosyltransferase in human cells. J. Biol. Chem. 2007, 282:24574-24582.
23. Jacobson E.L., Kim H., Kim M., Williams J.D., Coyle D.L., et al. A topical lipophilic niacin derivative increases NAD, epidermal differentiation and barrier function in photodamaged skin. Exp. Dermatol. 2007, 16:490-499.
24. Bodor E.T., Offermanns S. Nicotinic acid: an old drug with a promising future. Br. J. Pharmacol. 2008, 153(Suppl. 1):68-75.
25. Wise A., Foord S.M., Fraser N.J., Barnes A.A., Elshourbagy N., et al. Molecular identification of high and low affinity receptors for nicotinic acid. J. Biol. Chem. 2003, 278:9869-9874.
26. Soga T., Kamohara M., Takasaki J., Matsumoto S., Saito T., et al. Molecular identification of nicotinic acid receptor. Biochem. Biophys. Res. Commun. 2003, 303:364-369.
27. Zamporlini F., Ruggieri S., Mazzola F., Amici A., Orsomando G., Raffaelli N. Novel assay for simultaneous measurement of pyridine mononucleotides synthesizing activities allows dissection of the NAD biosynthetic machinery in mammalian cells. FEBS J. 2014, 281(22):5104-5119.
28. Galassi L., Di Stefano M., Brunetti L., Orsomando G., Amici A., et al. Characterization of human nicotinate phosphoribosyltransferase: kinetic studies, structure prediction and functional analysis by site-directed mutagenesis. Biochimie 2012, 94:300-309.
29. Gross J., Rajavel M., Segura E., Grubmeyer C. Energy coupling in Salmonella typhimurium nicotinic acid phosphoribosyltransferase: identification of His-219 as site of phosphorylation. Biochemistry 1996, 35:3917-3924.
30. Kosaka A., Spivey H.O., Gholson R.K. Nicotinate phosphoribosyltransferase of yeast. Purification and properties. J. Biol. Chem. 1971, 246:3277-3283.
31. Khan J.A., Tao X., Tong L. Molecular basis for the inhibition of human NMPRTase, a novel target for anticancer agents. Nat. Struct. Mol. Biol. 2006, 13:582-588.
32. Kabsch W. XDS. Acta Crystallogr. D Biol. Crystallogr. 2010, 66(Pt 2):125-132.
33. Collaborative Computational Project, Number 4 The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 1994, 50(5):760-763.
34. Bunkóczi G., Read R.J. Improvement of molecular-replacement models with Sculptor. Acta Crystallogr. D Biol. Crystallogr. 2011, 67(P4):303-312.
35. Terwilliger T.C., Dimaio F., Read R.J., Baker D., Bunkóczi G., Adams P.D., Grosse-Kunstleve R.W., Afonine P.V., Echols N. Phenix.mr_rosetta: molecular replacement and model rebuilding with Phenix and Rosetta. J. Struct. Funct. Genomics 2012, 13(2):81-90.
36. Murshudov G.N., Vagin A.A., Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. 1997, D53:240-255.
37. Emsley P., Lohkamp B., Scott W.G., Cowtan K. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 2010, 66(4):486-501.
38. Brunger A.T. Free R value: a novel statistic quantity for assessing the accuracy of crystal structures. Nature 1992, 355(6359):472-475.
39. Perrakis A., Harkiolaki M., Wilson K.S., Lamzin V.S. ARP/wARP and molecular replacement. Acta Crystallogr. D Biol. Crystallogr. 2001, 57(10):1445-1450.
40. Berendsen H.J., Spoel V.D., Drunen R.V. GROMACS: a message-passing parallel molecular dynamics implementation. Comput. Phys. Commun. 1995, 95:43-56.
41. Laskowsky R.A., Moss D.S., Thornton J.M. Main-chain bond lengths and bond angles in protein structures. J. Mol. Biol. 1993, 231(4):1049-1067.
42. N.M. Santa Fe, OpenEye Scientific Software, http://www.eyesopen.com.
43. Hawkins P.C.D., Skillman A.G., Warren G.L., Ellingson B.A., Stahl M.T. Conformer generation with OMEGA: algorithm and validation using high quality structures from the Protein Databank and Cambridge Structural Database. J. Chem. Inf. Model. 2010, 50:572-584.
44. Hawkins P.C.D., Nicholls A. Conformer generation with OMEGA: learning from the data set and the analysis of failures. J. Chem. Inf. Model. 2012, 52:2919-2936.
45. N.M. Santa Fe, FRED, version 3.0.0; OpenEye Scientific Software, http://www.eyesopen.com.
46. McGann M. FRED pose prediction and virtual screening accuracy. J. Chem. Inf. Model. 2011, 51:578-596.
47. N.M. Santa Fe, SZYBKI, version 1.7.0; OpenEye Scientific Software, http://www.eyesopen.com.
48. 45Schrödinger LLC, The PyMOL Molecular Graphics System, version 1.3, 2010.
49. Niedel J., Dietrich L.S. Nicotinate phosphoribosyltransferase of human erythrocytes. Purification and properties. J. Biol. Chem. 1973, 248(10):3500.
50. Shin D.H., Oganesyan N., Jancarik J., Yokota H., Kim R., Kim S.H. Crystal structure of a nicotinate phosphoribosyltransferase from Thermoplasma acidophilum. J. Biol. Chem. 2005, 280(18):18326-18335.
51. Wang T., Zhang X., Bheda P., Revollo J.R., Imai S., Wolberger C. Structure of Nampt/PBEF/visfatin, a mammalian NAD+ biosynthetic enzyme. Nat. Struct. Mol. Biol. 2006, 13(7):661-662.
52. Liu H., Woznica K., Catton G., Crawford A., Botting N., Naismith J.H. Structural and kinetic characterization of quinolinate phosphoribosyltransferase (hQPRTase) from homo sapiens. J. Mol. Biol. 2007, 373(3):755-763.
53. Chappie J.S., Cànaves J.M., Han G.W., Rife C.L., Xu Q., Stevens R.C. The structure of a eukaryotic nicotinic acid phosphoribosyltransferase reveals structural heterogeneity among type II PRTases. Structure 2005, 13(9):1385-1396.
54. Audrito V., Serra S., Brusa D., Mazzola F., Arruga F., Vaisitti T., Coscia M., Maffei R., Rossi D., Wang T., Inghirami G., Rizzi M., Gaidano G., Garcia J.G., Wolberger C., Raffaelli N., Deaglio S. Extracellular nicotinamide phosphoribosyltransferase (NAMPT) promotes M2 macrophage polarization in chronic lymphocytic leukemia. Blood 2015, 125(1):111-123. 10.1182/blood-2014-07-589069.
55. Garavaglia S., Perozzi S., Galeazzi L., Raffaelli N., Rizzi M. The crystal structure of human a-amino-b-carboxymuconate-e-semialdehyde decarboxylase in complex with 1,3-dihydroxyacetonephosphate suggests a regulatory link between NAD synthesis and glycolysis. FEBS J. 2009, 276(22):6615-6623.
56. Ganji S.H., Qin S., Zhang L., Kamanna V.S., Kashyap M.L. Niacin inhibits vascular oxidative stress, redox-sensitive genes, and monocyte adhesion to human aortic endothelial cells. Atherosclerosis 2009, 202(1):68-75.
57. Duarte-Pereira S., Silva S.S., Azevedo L., Castro L., Amorim A., Silva R.M. NAMPT and NAPRT1: novel polymorphisms and distribution of variants between normal tissues and tumor samples. Sci. Rep. 2014, 4:6311.
58. Shames D.S., Elkins K., Walter K., Holcomb T., Du P., Mohl D., Xiao Y., Pham T., Haverty P.M., Liederer B., Liang X., Yauch R.L., O'Brien T., Bourgon R., Koeppen H., Belmont L.D. Loss of NAPRT1 expression by tumor-specific promoter methylation provides a novel predictive biomarker for NAMPT inhibitors. Clin. Cancer Res. 2013, 9(24):6912-6923.
59. Lasky-Su J., Anney R.J., Neale B.M., Franke B., Zhou K., Maller J.B., Vasquez A.A., Chen W., Asherson P., Buitelaar J., Banaschewski T., Ebstein R., Gill M., Miranda A., Mulas F., Oades R.D., Roeyers H., Rothenberger A., Sergeant J., Sonuga-Barke E., Steinhausen H.C., Taylor E., Daly M., Laird N., Lange C., Faraone S.V. Genome-wide association scan of the time to onset of attention deficit hyperactivity disorder. Am. J. Med. Genet. B Neuropsychiatr. Genet. 2008, 147B(8):1355-1358.
60. Cerna D., Li H., Flaherty S., Takebe N., Coleman C.N., Yoo S.S. Inhibition of nicotinamide phosphoribosyltransferase (NAMPT) activity by small molecule GMX1778 regulates reactive oxygen species (ROS)-mediated cytotoxicity in a p53- and nicotinic acid phosphoribosyltransferase1 (NAPRT1)-dependent manner. J. Biol. Chem. 2012, 287(26):22408-22417.