Extensive regulation of nicotinate phosphoribosyltransferase (NAPRT) expression in human tissues and tumors

Oncotarget

Volumn 7, Issue 2, 2016, Pages 1973-1983

  Duarte Pereira, Sara ^a   Pereira Castro, Isabel ^a,c   Silva, Sarah S ^a   Correia, Mariana Gonçalves ^a   Neto, Célia ^a   da Costa, Luís Teixeira ^a,b   Amorim, António ^a,c   Silva, Raquel M ^a,d  

^a UNIVERSITY OF PORTO   (Portugal)

^b UNIVERSITY OF ÉVORA   (Portugal)

^c UNIVERSITY OF PORTO   (Portugal)

^d UNIVERSITY OF AVEIRO   (Portugal)

Author keywords

Alternative transcripts; Anti cancer therapies; Human NAD salvage; NAMPT; NAPRT

Indexed keywords

MESSENGER RNA; NICOTINAMIDE PHOSPHORIBOSYLTRANSFERASE; NICOTINATE PHOSPHORIBOSYLTRANSFERASE; NICOTINIC ACID; CYTOKINE; GLYCOSYLTRANSFERASE; NICOTINAMIDE PHOSPHORIBOSYLTRANSFERASE, HUMAN;

786 O CELL LINE; A549 CELL LINE; ARTICLE; BIOINFORMATICS; C643 CELL LINE; CAKI 2 CELL LINE; CANCER CELL LINE; CARCINOMA CELL LINE; CONTROLLED STUDY; DNA METHYLATION; EXON; EXPRESSED SEQUENCE TAG; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC VARIABILITY; HCT116 CELL LINE; HEK293 CELL LINE; HISTOPATHOLOGY; HL 60 CELL LINE; HUMAN; HUMAN TISSUE; INTRON; LEUKEMIA CELL LINE; MELANOMA CELL LINE; MKN28 CELL LINE; ML2 CELL LINE; MOLECULAR CLONING; MUTATIONAL ANALYSIS; NAMPT GENE; NAPRT GENE; NB4 CELL LINE; PROMOTER REGION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; TRANSCRIPTION REGULATION; WESTERN BLOTTING; ALTERNATIVE RNA SPLICING; GENETICS; MUTATION; NEOPLASM; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; TUMOR CELL CULTURE;

ALTERNATIVE SPLICING; CYTOKINES; DNA METHYLATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MUTATION; NEOPLASMS; NICOTINAMIDE PHOSPHORIBOSYLTRANSFERASE; PENTOSYLTRANSFERASES; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TUMOR CELLS, CULTURED;

EID: 84957627325     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.6538     Document Type: Article

References (66)

1. Rongvaux A, Andris F, Van Gool F and Leo O. Reconstructing eukaryotic NAD metabolism. Bioessays. 2003; 25:683-690.
2. Magni G, Amici A, Emanuelli M, Orsomando G, Raffaelli N and Ruggieri S. Enzymology of NAD+ homeostasis in man. Cell Mol Life Sci. 2004; 61:19-34.
3. Bogan KL and Brenner C. Nicotinic acid, nicotinamide, and nicotinamide riboside: a molecular evaluation of NAD+ precursor vitamins in human nutrition. Annu Rev Nutr. 2008; 28:115-130.
4. Galli M, Van Gool F, Rongvaux A, Andris F and Leo O. The nicotinamide phosphoribosyltransferase: a molecular link between metabolism, inflammation, and cancer. Cancer Res. 2010; 70:8-11.
5. Bowlby SC, Thomas MJ, D'Agostino RB, Jr. and Kridel SJ. Nicotinamide phosphoribosyl transferase (nampt) is required for de novo lipogenesis in tumor cells. PLoS One. 2012; 7:e40195.
6. Chiarugi A, Dolle C, Felici R and Ziegler M. The NAD metabolome-a key determinant of cancer cell biology. Nat Rev Cancer. 2012; 12:741-752.
7. Reddy PS, Umesh S, Thota B, Tandon A, Pandey P, Hegde AS, Balasubramaniam A, Chandramouli BA, Santosh V, Rao MR, Kondaiah P and Somasundaram K. PBEF1/NAmPRTase/Visfatin: a potential malignant astrocytoma/glioblastoma serum marker with prognostic value. Cancer Biol Ther. 2008; 7:663-668.
8. Zhang LQ, Heruth DP and Ye SQ. Nicotinamide Phosphoribosyltransferase in Human Diseases. J Bioanal Biomed. 2011; 3:13-25.
9. Bi TQ, Che XM, Liao XH, Zhang DJ, Long HL, Li HJ and Zhao W. Overexpression of Nampt in gastric cancer and chemopotentiating effects of the Nampt inhibitor FK866 in combination with fluorouracil. Oncol Rep. 2011; 26:1251-1257.
10. Shackelford RE, Bui MM, Coppola D and Hakam A. Overexpression of nicotinamide phosphoribosyltransferase in ovarian cancers. Int J Clin Exp Pathol. 2010; 3:522-527.
11. Van Beijnum JR, Moerkerk PT, Gerbers AJ, De Bruine AP, Arends JW, Hoogenboom HR and Hufton SE. Target validation for genomics using peptide-specific phage antibodies: a study of five gene products overexpressed in colorectal cancer. Int J Cancer. 2002; 101:118-127.
12. Wang B, Hasan MK, Alvarado E, Yuan H, Wu H and Chen WY. NAMPT overexpression in prostate cancer and its contribution to tumor cell survival and stress response. Oncogene. 2011; 30:907-921.
13. Khan JA, Tao X and Tong L. Molecular basis for the inhibition of human NMPRTase, a novel target for anticancer agents. Nat Struct Mol Biol. 2006; 13:582-588.
14. Nahimana A, Attinger A, Aubry D, Greaney P, Ireson C, Thougaard AV, Tjornelund J, Dawson KM, Dupuis M and Duchosal MA. The NAD biosynthesis inhibitor APO866 has potent antitumor activity against hematologic malignancies. Blood. 2009; 113:3276-3286.
15. Pittelli M, Formentini L, Faraco G, Lapucci A, Rapizzi E, Cialdai F, Romano G, Moneti G, Moroni F and Chiarugi A. Inhibition of nicotinamide phosphoribosyltransferase: cellular bioenergetics reveals a mitochondrial insensitive NAD pool. J Biol Chem. 2010; 285:34106-34114.
16. Olesen UH, Petersen JG, Garten A, Kiess W, Yoshino J, Imai S, Christensen MK, Fristrup P, Thougaard AV, Bjorkling F, Jensen PB, Nielsen SJ and Sehested M. Target enzyme mutations are the molecular basis for resistance towards pharmacological inhibition of nicotinamide phosphoribosyltransferase. BMC Cancer. 2010; 10:677.
17. Watson M, Roulston A, Belec L, Billot X, Marcellus R, Bedard D, Bernier C, Branchaud S, Chan H, Dairi K, Gilbert K, Goulet D, Gratton MO, et al. The small molecule GMX1778 is a potent inhibitor of NAD+ biosynthesis: strategy for enhanced therapy in nicotinic acid phosphoribosyltransferase 1-deficient tumors. Mol Cell Biol. 2009; 29:5872-5888.
18. Olesen UH, Thougaard AV, Jensen PB and Sehested M. A preclinical study on the rescue of normal tissue by nicotinic acid in high-dose treatment with APO866, a specific nicotinamide phosphoribosyltransferase inhibitor. Mol Cancer Ther. 2010; 9:1609-1617.
19. Shames DS, Elkins K, Walter K, Holcomb T, Du P, Mohl D, Xiao Y, Pham T, Haverty PM, Liederer B, Liang X, Yauch RL, O'Brien T, et al. Loss of NAPRT1 Expression by Tumor-Specific Promoter Methylation Provides a Novel Predictive Biomarker for NAMPT Inhibitors. Clinical cancer research: an official journal of the American Association for Cancer Research. 2013; 19:6912-6923.
20. O'Brien T, Oeh J, Xiao Y, Liang X, Vanderbilt A, Qin A, Yang L, Lee LB, Ly J, Cosino E, LaCap JA, Ogasawara A, Williams S, et al. Supplementation of nicotinic acid with NAMPT inhibitors results in loss of in vivo efficacy in NAPRT1-deficient tumor models. Neoplasia. 2013; 15:1314-1329.
21. Hara N, Yamada K, Shibata T, Osago H, Hashimoto T and Tsuchiya M. Elevation of cellular NAD levels by nicotinic acid and involvement of nicotinic acid phosphoribosyltransferase in human cells. J Biol Chem. 2007; 282:24574-24582.
22. Olesen UH, Hastrup N and Sehested M. Expression patterns of nicotinamide phosphoribosyltransferase and nicotinic acid phosphoribosyltransferase in human malignant lymphomas. APMIS. 2011; 119:296-303.
23. Cerna D, Li H, Flaherty S, Takebe N, Coleman CN and Yoo SS. 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; 287:22408-22417.
24. Galassi L, Di Stefano M, Brunetti L, Orsomando G, Amici A, Ruggieri S and Magni G. Characterization of human nicotinate phosphoribosyltransferase: Kinetic studies, structure prediction and functional analysis by site-directed mutagenesis. Biochimie. 2012; 94:300-309.
25. Wheeler DL, Barrett T, Benson DA, Bryant SH, Canese K, Chetvernin V, Church DM, Dicuccio M, Edgar R, Federhen S, Feolo M, Geer LY, Helmberg W, et al. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res. 2008; 36:D13-21.
26. Uhlen M, Fagerberg L, Hallstrom BM, Lindskog C, Oksvold P, Mardinoglu A, Sivertsson A, Kampf C, Sjostedt E, Asplund A, Olsson I, Edlund K, Lundberg E, et al. Proteomics. Tissue-based map of the human proteome. Science. 2015; 347:1260419.
27. Marletta AS, Massarotti A, Orsomando G, Magni G, Rizzi M and Garavaglia S. Crystal structure of human nicotinic acid phosphoribosyltransferase. FEBS Open Bio. 2015; 5:419-428.
28. Duarte-Pereira S, Silva SS, Azevedo L, Castro L, Amorim A and Silva RM. NAMPT and NAPRT1: novel polymorphisms and distribution of variants between normal tissues and tumor samples. Scientific reports. 2014; 4:6311.
29. Boyle AP, Hong EL, Hariharan M, Cheng Y, Schaub MA, Kasowski M, Karczewski KJ, Park J, Hitz BC, Weng S, Cherry JM and Snyder M. Annotation of functional variation in personal genomes using RegulomeDB. Genome Res. 2012; 22:1790-1797.
30. Forbes SA, Beare D, Gunasekaran P, Leung K, Bindal N, Boutselakis H, Ding M, Bamford S, Cole C, Ward S, Kok CY, Jia M, De T, et al. COSMIC: exploring the world's knowledge of somatic mutations in human cancer. Nucleic Acids Res. 2014; 43:D805-811.
31. Chen R, Davydov EV, Sirota M and Butte AJ. Nonsynonymous and synonymous coding SNPs show similar likelihood and effect size of human disease association. PLoS One. 2010; 5:e13574.
32. Sauna ZE and Kimchi-Sarfaty C. Understanding the contribution of synonymous mutations to human disease. Nat Rev Genet. 2011; 12:683-691.
33. Rice GI, Reijns MA, Coffin SR, Forte GM, Anderson BH, Szynkiewicz M, Gornall H, Gent D, Leitch A, Botella MP, Fazzi E, Gener B, Lagae L, et al. Synonymous Mutations in RNASEH2A Create Cryptic Splice Sites Impairing RNase H2 Enzyme Function in Aicardi-Goutieres Syndrome. Human mutation. 2013; 34:1066-70. doi: 10.1002/humu.22336.
34. Belenky P, Bogan KL and Brenner C. NAD+ metabolism in health and disease. Trends Biochem Sci. 2007; 32:12-19.
35. Matheny CJ, Wei MC, Bassik MC, Donnelly AJ, Kampmann M, Iwasaki M, Piloto O, Solow-Cordero DE, Bouley DM, Rau R, Brown P, McManus MT, Weissman JS, et al. Next-generation NAMPT inhibitors identified by sequential high-throughput phenotypic chemical and functional genomic screens. Chemistry & biology. 2013; 20:1352-1363.
36. Tan B, Young DA, Lu ZH, Wang T, Meier TI, Shepard RL, Roth K, Zhai Y, Huss K, Kuo MS, Gillig J, Parthasarathy S, Burkholder TP, et al. Pharmacological inhibition of nicotinamide phosphoribosyltransferase (NAMPT), an enzyme essential for NAD+ biosynthesis, in human cancer cells: metabolic basis and potential clinical implications. J Biol Chem. 2013; 288:3500-3511.
37. Revollo JR, Korner A, Mills KF, Satoh A, Wang T, Garten A, Dasgupta B, Sasaki Y, Wolberger C, Townsend RR, Milbrandt J, Kiess W and Imai S. Nampt/PBEF/Visfatin regulates insulin secretion in beta cells as a systemic NAD biosynthetic enzyme. Cell Metab. 2007; 6:363-375.
38. Houtkooper RH, Canto C, Wanders RJ and Auwerx J. The secret life of NAD+: an old metabolite controlling new metabolic signaling pathways. Endocr Rev. 2010; 31:194-223.
39. Roulston A and Shore GC. New Strategies to Maximize Therapeutic Opportunities for NAMPT Inhibitors in Oncology. Molecular & Cellular Oncology. 2015:00-00.
40. Shackelford R, Hirsh S, Henry K, Abdel-Mageed A, Kandil E and Coppola D. Nicotinamide phosphoribosyltransferase and SIRT3 expression are increased in well-differentiated thyroid carcinomas. Anticancer research. 2013; 33:3047-3052.
41. Xiao Y, Elkins K, Durieux JK, Lee L, Oeh J, Yang LX, Liang X, DelNagro C, Tremayne J, Kwong M, Liederer BM, Jackson PK, Belmont LD, et al. Dependence of tumor cell lines and patient-derived tumors on the NAD salvage pathway renders them sensitive to NAMPT inhibition with GNE-618. Neoplasia. 2013; 15:1151-1160.
42. Beaudoing E, Freier S, Wyatt JR, Claverie JM and Gautheret D. Patterns of variant polyadenylation signal usage in human genes. Genome Res. 2000; 10:1001-1010.
43. Xu Q, Modrek B and Lee C. Genome-wide detection of tissue-specific alternative splicing in the human transcriptome. Nucleic Acids Res. 2002; 30:3754-3766.
44. Yeo G, Holste D, Kreiman G and Burge CB. Variation in alternative splicing across human tissues. Genome Biol. 2004; 5.
45. Anders G, Mackowiak SD, Jens M, Maaskola J, Kuntzagk A, Rajewsky N, Landthaler M and Dieterich C. doRiNA: a database of RNA interactions in post-transcriptional regulation. Nucleic Acids Res. 2012; 40:D180-186.
46. Peters L and Meister G. Argonaute proteins: mediators of RNA silencing. Mol Cell. 2007; 26:611-623.
47. Ameyar-Zazoua M, Rachez C, Souidi M, Robin P, Fritsch L, Young R, Morozova N, Fenouil R, Descostes N, Andrau JC, Mathieu J, Hamiche A, Ait-Si-Ali S, et al. Argonaute proteins couple chromatin silencing to alternative splicing. Nat Struct Mol Biol. 2012; 19:998-1004.
48. Grosso AR, Gomes AQ, Barbosa-Morais NL, Caldeira S, Thorne NP, Grech G, von Lindern M and Carmo-Fonseca M. Tissue-specific splicing factor gene expression signatures. Nucleic Acids Res. 2008; 36:4823-4832.
49. Buckanovich RJ, Yang YY and Darnell RB. The onconeural antigen Nova-1 is a neuron-specific RNA-binding protein, the activity of which is inhibited by paraneoplastic antibodies. J Neurosci. 1996; 16:1114-1122.
50. Valverde R, Edwards L and Regan L. Structure and function of KH domains. FEBS J. 2008; 275:2712-2726.
51. Teplova M, Malinina L, Darnell JC, Song J, Lu M, Abagyan R, Musunuru K, Teplov A, Burley SK, Darnell RB and Patel DJ. Protein-RNA and protein-protein recognition by dual KH1/2 domains of the neuronal splicing factor Nova-1. Structure. 2011; 19:930-944.
52. Paz I, Akerman M, Dror I, Kosti I and Mandel-Gutfreund Y. SFmap: a web server for motif analysis and prediction of splicing factor binding sites. Nucleic Acids Res. 2010; 38:W281-285.
53. Heinemeyer T, Wingender E, Reuter I, Hermjakob H, Kel AE, Kel OV, Ignatieva EV, Ananko EA, Podkolodnaya OA, Kolpakov FA, Podkolodny NL and Kolchanov NA. Databases on transcriptional regulation: TRANSFAC, TRRD and COMPEL. Nucleic Acids Res. 1998; 26:362-367.
54. Koutsodontis G, Moustakas A and Kardassis D. The role of Sp1 family members, the proximal GC-rich motifs, and the upstream enhancer region in the regulation of the human cell cycle inhibitor p21WAF-1/Cip1 gene promoter. Biochemistry. 2002; 41:12771-12784.
55. Pavlidis P and Noble WS. Matrix2png: a utility for visualizing matrix data. Bioinformatics. 2003; 19:295-296.
56. Castro LF, Lopes-Marques M, Wilson JM, Rocha E, Reis-Henriques MA, Santos MM and Cunha I. A novel Acetyl-CoA synthetase short-chain subfamily member 1 (Acss1) gene indicates a dynamic history of paralogue retention and loss in vertebrates. Gene. 2012; 497:249-255.
57. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004; 32:1792-1797.
58. Drummond A, Ashton B, Buxton S, Cheung M, Cooper A, Duran C, Field M, Heled J, Kearse M, Markowitz S, Moir R, Stones-Havas S, Sturrock S, et al. (2011). Geneious. http://www.geneious.com).
59. Cunningham F, Amode MR, Barrell D, Beal K, Billis K, Brent S, Carvalho-Silva D, Clapham P, Coates G, Fitzgerald S, Gil L, Giron CG, Gordon L, et al. Ensembl 2015. Nucleic Acids Res. 2015; 43:D662-669.
60. Chen PW, Murray TG, Uno T, Salgaller ML, Reddy R and Ksander BR. Expression of MAGE genes in ocular melanoma during progression from primary to metastatic disease. Clin Exp Metastasis. 1997; 15:509-518.
61. Ksander BR, Rubsamen PE, Olsen KR, Cousins SW and Streilein JW. Studies of tumor-infiltrating lymphocytes from a human choroidal melanoma. Invest Ophthalmol Vis Sci. 1991; 32:3198-3208.
62. Pereira-Castro I, Quental R, da Costa LT, Amorim A and Azevedo L. Successful COG8 and PDF overlap is mediated by alterations in splicing and polyadenylation signals. Hum Genet. 2012; 131:265-274.
63. Pereira-Castro I, Costa LT, Amorim A and Azevedo L. Transcriptional regulation of the human mitochondrial peptide deformylase (PDF). Biochem Biophys Res Commun. 2012; 421:825-831.
64. Burgos ES, Ho MC, Almo SC and Schramm VL. A phosphoenzyme mimic, overlapping catalytic sites and reaction coordinate motion for human NAMPT. Proc Natl Acad Sci U S A. 2009; 106:13748-13753.
65. Sali A, Potterton L, Yuan F, van Vlijmen H and Karplus M. Evaluation of comparative protein modeling by MODELLER. Proteins. 1995; 23:318-326.
66. Schrodinger, LLC. (2010). The PyMOL Molecular Graphics System, Version 1.3r1.