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Exploring NAD+ metabolism in host–pathogen interactions

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Abstract

Nicotinamide adenine dinucleotide (NAD+) is a vital molecule found in all living cells. NAD+ intracellular levels are dictated by its synthesis, using the de novo and/or salvage pathway, and through its catabolic use as co-enzyme or co-substrate. The regulation of NAD+ metabolism has proven to be an adequate drug target for several diseases, including cancer, neurodegenerative or inflammatory diseases. Increasing interest has been given to NAD+ metabolism during innate and adaptive immune responses suggesting that its modulation could also be relevant during host–pathogen interactions. While the maintenance of NAD+ homeostatic levels assures an adequate environment for host cell survival and proliferation, fluctuations in NAD+ or biosynthetic precursors bioavailability have been described during host–pathogen interactions, which will interfere with pathogen persistence or clearance. Here, we review the double-edged sword of NAD+ metabolism during host–pathogen interactions emphasizing its potential for treatment of infectious diseases.

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References

  1. Alano CC, Garnier P, Ying W, Higashi Y, Kauppinen TM, Swanson RA (2010) NAD+ depletion is necessary and sufficient for poly(ADP-ribose) polymerase-1-mediated neuronal death. J Neurosci 30:2967–2978

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  2. Ariumi Y, Turelli P, Masutani M, Trono D (2005) DNA damage sensors ATM, ATR, DNA-PKcs, and PARP-1 are dispensable for human immunodeficiency virus type 1 integration. J Virol 79:2973–2978

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  3. Bastiat-Sempe B, Love JF, Lomayesva N, Wessels MR (2014) Streptolysin O and NAD-glycohydrolase prevent phagolysosome acidification and promote group a streptococcus survival in macrophages. mBio 5:e01690-01614

    Article  CAS  Google Scholar 

  4. Boasso A (2011) Wounding the immune system with its own blade: HIV-induced tryptophan catabolism and pathogenesis. Curr Med Chem 18:2247–2256

    Article  CAS  PubMed  Google Scholar 

  5. Brown SA, Palmer KL, Whiteley M (2008) Revisiting the host as a growth medium. Nat Rev Microbiol 6:657–666

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  6. Bruzzone S, Parenti MD, Grozio A, Ballestrero A, Bauer I, Del Rio A, Nencioni A (2013) Rejuvenating sirtuins: the rise of a new family of cancer drug targets. Curr Pharm Des 19:614–623

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  7. Bueno MT, Reyes D, Valdes L, Saheba A, Urias E, Mendoza C et al (2013) Poly(ADP-ribose) polymerase 1 promotes transcriptional repression of integrated retroviruses. J Virol 87:2496–2507

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  8. Burkle A (2005) Poly(ADP-ribose). The most elaborate metabolite of NAD+. FEBS J 272:4576–4589

    Article  PubMed  CAS  Google Scholar 

  9. Cagnetta A, Soncini D, Caffa I, Acharya C, Acharya P, Adamia S et al (2015) Apo866 increases anti-tumor activity of cyclosporin-a by inducing mitochondrial and endoplasmic reticulum stress in leukemia cells. Clin Cancer Res 21(17):3934–3945

    Article  CAS  PubMed  Google Scholar 

  10. Cappellini MD, Fiorelli G (2008) Glucose-6-phosphate dehydrogenase deficiency. Lancet 371:64–74

    Article  CAS  PubMed  Google Scholar 

  11. Cardoso F, Castro F, Moreira-Teixeira L, Sousa J, Torrado E, Silvestre R et al (2015) Myeloid sirtuin 2 expression does not impact long-term Mycobacterium tuberculosis control. PLoS One 10:e0131904

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  12. Cervantes-Sandoval I, Serrano-Luna Jde J, Garcia-Latorre E, Tsutsumi V, Shibayama M (2008) Characterization of brain inflammation during primary amoebic meningoencephalitis. Parasitol Int 57:307–313

    Article  PubMed  Google Scholar 

  13. Chandrasekaran S, Caparon MG (2015) The Streptococcus pyogenes NAD glycohydrolase modulates epithelial cell PARylation and HMGB1 release. Cell Microbiol 17(9):1376–1390

    Article  CAS  PubMed  Google Scholar 

  14. Chen XY, Zhang HS, Wu TC, Sang WW, Ruan Z (2013) Down-regulation of NAMPT expression by miR-182 is involved in Tat-induced HIV-1 long terminal repeat (LTR) transactivation. Int J Biochem Cell Biol 45:292–298

    Article  CAS  PubMed  Google Scholar 

  15. Choi J, Corder NL, Koduru B, Wang Y (2014) Oxidative stress and hepatic Nox proteins in chronic hepatitis C and hepatocellular carcinoma. Free Radic Biol Med 72:267–284

    Article  CAS  PubMed  Google Scholar 

  16. Cumont MC, Monceaux V, Viollet L, Lay S, Parker R, Hurtrel B, Estaquier J (2007) TGF-beta in intestinal lymphoid organs contributes to the death of armed effector CD8 T cells and is associated with the absence of virus containment in rhesus macaques infected with the simian immunodeficiency virus. Cell Death Differ 14:1747–1758

    Article  CAS  PubMed  Google Scholar 

  17. de Toledo FG, Cheng J, Liang M, Chini EN, Dousa TP (2000) ADP-Ribosyl cyclase in rat vascular smooth muscle cells: properties and regulation. Circ Res 86:1153–1159

    Article  PubMed  Google Scholar 

  18. Di Stefano M, Conforti L (2013) Diversification of NAD biological role: the importance of location. FEBS J 280:4711–4728

    Article  PubMed  CAS  Google Scholar 

  19. Dolle C, Niere M, Lohndal E, Ziegler M (2010) Visualization of subcellular NAD pools and intra-organellar protein localization by poly-ADP-ribose formation. Cell Mol Life Sci 67:433–443

    Article  PubMed  CAS  Google Scholar 

  20. Domergue R, Castano I, De Las Penas A, Zupancic M, Lockatell V, Hebel JR et al (2005) Nicotinic acid limitation regulates silencing of Candida adhesins during UTI. Science 308:866–870

    Article  CAS  PubMed  Google Scholar 

  21. Dousa TP, Chini EN, Beers KW (1996) Adenine nucleotide diphosphates: emerging second messengers acting via intracellular Ca2+ release. Am J Physiol 271:C1007–C1024

    CAS  PubMed  Google Scholar 

  22. El-Zaatari M, Chang YM, Zhang M, Franz M, Shreiner A, McDermott AJ et al (2014) Tryptophan catabolism restricts IFN-gamma-expressing neutrophils and Clostridium difficile immunopathology. J Immunol 193:807–816

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  23. Eskandarian HA, Impens F, Nahori MA, Soubigou G, Coppee JY, Cossart P, Hamon MA (2013) A role for SIRT2-dependent histone H3K18 deacetylation in bacterial infection. Science 341:1238858

    Article  PubMed  CAS  Google Scholar 

  24. Estrada-Figueroa LA, Ramirez-Jimenez Y, Osorio-Trujillo C, Shibayama M, Navarro-Garcia F, Garcia-Tovar C, Talamas-Rohana P (2011) Absence of CD38 delays arrival of neutrophils to the liver and innate immune response development during hepatic amoebiasis by Entamoeba histolytica. Parasite Immunol 33:661–668

    Article  CAS  PubMed  Google Scholar 

  25. Fouquerel E, Sobol RW (2014) ARTD1 (PARP1) activation and NAD(+) in DNA repair and cell death. DNA Repair (Amst) 23:27–32

    Article  CAS  Google Scholar 

  26. Gazanion E, Garcia D, Silvestre R, Gerard C, Guichou JF, Labesse G et al (2011) The Leishmania nicotinamidase is essential for NAD+ production and parasite proliferation. Mol Microbiol 82:21–38

    Article  CAS  PubMed  Google Scholar 

  27. Grandvaux N, Mariani M, Fink K (2015) Lung epithelial NOX/DUOX and respiratory virus infections. Clin Sci (Lond) 128:337–347

    Article  CAS  Google Scholar 

  28. Ha EM, Lee KA, Seo YY, Kim SH, Lim JH, Oh BH et al (2009) Coordination of multiple dual oxidase-regulatory pathways in responses to commensal and infectious microbes in Drosophila gut. Nat Immunol 10:949–957

    Article  CAS  PubMed  Google Scholar 

  29. Ha EM, Oh CT, Bae YS, Lee WJ (2005) A direct role for dual oxidase in Drosophila gut immunity. Science 310:847–850

    Article  CAS  PubMed  Google Scholar 

  30. Ha HC, Juluri K, Zhou Y, Leung S, Hermankova M, Snyder SH (2001) Poly(ADP-ribose) polymerase-1 is required for efficient HIV-1 integration. Proc Natl Acad Sci USA 98:3364–3368

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  31. Hassa PO, Haenni SS, Elser M, Hottiger MO (2006) Nuclear ADP-ribosylation reactions in mammalian cells: Where are we today and where are we going? Microbiol Mol Biol Rev 70:789–829

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  32. He M, Gao SJ (2014) A novel role of SIRT1 in gammaherpesvirus latency and replication. Cell Cycle 13:3328–3330

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  33. Hill T 3rd, Xu C, Harper RW (2010) IFNgamma mediates DUOX2 expression via a STAT-independent signaling pathway. Biochem Biophys Res Commun 395:270–274

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  34. Hogan D, Wheeler RT (2014) The complex roles of NADPH oxidases in fungal infection. Cell Microbiol 16:1156–1167

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  35. Hoshi M, Saito K, Hara A, Taguchi A, Ohtaki H, Tanaka R et al (2010) The absence of IDO upregulates type I IFN production, resulting in suppression of viral replication in the retrovirus-infected mouse. J Immunol 185:3305–3312

    Article  CAS  PubMed  Google Scholar 

  36. Houtkooper RH, Pirinen E, Auwerx J (2012) Sirtuins as regulators of metabolism and healthspan. Nat Rev Mol Cell Biol 13:225–238

    Article  CAS  PubMed  Google Scholar 

  37. Joo JH, Ryu JH, Kim CH, Kim HJ, Suh MS, Kim JO et al (2012) Dual oxidase 2 is essential for the toll-like receptor 5-mediated inflammatory response in airway mucosa. Antioxid Redox Signal 16:57–70

    Article  CAS  PubMed  Google Scholar 

  38. Kemmer G, Reilly TJ, Schmidt-Brauns J, Zlotnik GW, Green BA, Fiske MJ et al (2001) NadN and e (P4) are essential for utilization of NAD and nicotinamide mononucleotide but not nicotinamide riboside in Haemophilus influenzae. J Bacteriol 183:3974–3981

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  39. Kim HJ, Kim CH, Kim MJ, Ryu JH, Seong SY, Kim S et al (2015) The Induction of pattern-recognition receptor expression against influenza A virus through Duox2-derived reactive oxygen species in Nasal Mucosa. Am J Respir Cell Mol Biol 53:525–535

    Article  CAS  PubMed  Google Scholar 

  40. Kim S, Kurokawa D, Watanabe K, Makino S, Shirahata T, Watarai M (2004) Brucella abortus nicotinamidase (PncA) contributes to its intracellular replication and infectivity in mice. FEMS Microbiol Lett 234:289–295

    Article  CAS  PubMed  Google Scholar 

  41. Kim SH, Lee WJ (2014) Role of DUOX in gut inflammation: lessons from Drosophila model of gut–microbiota interactions. Front Cell Infect Microbiol 3:116

    Article  PubMed Central  PubMed  Google Scholar 

  42. Kim UH, Kim MK, Kim JS, Han MK, Park BH, Kim HR (1993) Purification and characterization of NAD glycohydrolase from rabbit erythrocytes. Arch Biochem Biophys 305:147–152

    Article  CAS  PubMed  Google Scholar 

  43. Koedel U, Winkler F, Angele B, Fontana A, Pfister HW (2002) Meningitis-associated central nervous system complications are mediated by the activation of poly(ADP-ribose) polymerase. J Cereb Blood Flow Metab 22:39–49

    Article  CAS  PubMed  Google Scholar 

  44. Kurnasov OV, Polanuyer BM, Ananta S, Sloutsky R, Tam A, Gerdes SY, Osterman AL (2002) Ribosylnicotinamide kinase domain of NadR protein: identification and implications in NAD biosynthesis. J Bacteriol 184:6906–6917

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  45. Lau C, Dolle C, Gossmann TI, Agledal L, Niere M, Ziegler M (2010) Isoform-specific targeting and interaction domains in human nicotinamide mononucleotide adenylyltransferases. J Biol Chem 285:18868–18876

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  46. Lau C, Niere M, Ziegler M (2009) The NMN/NaMN adenylyltransferase (NMNAT) protein family. Front Biosci (Landmark Ed) 14:410–431

    Article  CAS  Google Scholar 

  47. Lee HC (2006) Structure and enzymatic functions of human CD38. Mol Med 12:317–323

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  48. Li Q, He M, Zhou F, Ye F, Gao SJ (2014) Activation of Kaposi’s sarcoma-associated herpesvirus (KSHV) by inhibitors of class III histone deacetylases: identification of sirtuin 1 as a regulator of the KSHV life cycle. J Virol 88:6355–6367

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  49. Lu H, Wu Q, Yang H (2015) DUOX2 promotes the elimination of the Klebsiella pneumoniae strain K5 from T24 cells through the reactive oxygen species pathway. Int J Mol Med 36:551–558

    PubMed  Google Scholar 

  50. Magni G, Orsomando G, Raffelli N, Ruggieri S (2008) Enzymology of mammalian NAD metabolism in health and disease. Front Biosci 13:6135–6154

    Article  CAS  PubMed  Google Scholar 

  51. Mantis NJ, Sansonetti PJ (1996) The nadB gene of Salmonella typhimurium complements the nicotinic acid auxotrophy of Shigella flexneri. Mol Gen Genet 252:626–629

    CAS  PubMed  Google Scholar 

  52. Medana IM, Mai NT, Day NP, Hien TT, Bethell D, Phu NH et al (2001) Cellular stress and injury responses in the brains of adult Vietnamese patients with fatal Plasmodium falciparum malaria. Neuropathol Appl Neurobiol 27:421–433

    Article  CAS  PubMed  Google Scholar 

  53. Michan S, Sinclair D (2007) Sirtuins in mammals: insights into their biological function. Biochem J 404:1–13

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  54. Michos A, Gryllos I, Hakansson A, Srivastava A, Kokkotou E, Wessels MR (2006) Enhancement of streptolysin O activity and intrinsic cytotoxic effects of the group A streptococcal toxin, NAD-glycohydrolase. J Biol Chem 281:8216–8223

    Article  CAS  PubMed  Google Scholar 

  55. Mocarski ES, Guo H, Kaiser WJ (2015) Necroptosis: the Trojan horse in cell autonomous antiviral host defense. Virology 479–480:160–166

    Article  PubMed  CAS  Google Scholar 

  56. Moreira D, Rodrigues V, Abengozar M, Rivas L, Rial E, Laforge M et al (2015) Leishmania infantum modulates host macrophage mitochondrial metabolism by hijacking the SIRT1-AMPK axis. PLoS Pathog 11:e1004684

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  57. Moreno-Vinasco L, Quijada H, Sammani S, Siegler J, Letsiou E, Deaton R et al (2014) Nicotinamide phosphoribosyltransferase inhibitor is a novel therapeutic candidate in murine models of inflammatory lung injury. Am J Respir Cell Mol Biol 51:223–228

    PubMed Central  PubMed  Google Scholar 

  58. Mori V, Amici A, Mazzola F, Di Stefano M, Conforti L, Magni G et al (2014) Metabolic profiling of alternative NAD biosynthetic routes in mouse tissues. PLoS One 9:e113939

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  59. Muller S (2004) Redox and antioxidant systems of the malaria parasite Plasmodium falciparum. Mol Microbiol 53:1291–1305

    Article  PubMed  CAS  Google Scholar 

  60. Murakami Y, Hoshi M, Hara A, Takemura M, Arioka Y, Yamamoto Y et al (2012) Inhibition of increased indoleamine 2,3-dioxygenase activity attenuates Toxoplasma gondii replication in the lung during acute infection. Cytokine 59:245–251

    Article  CAS  PubMed  Google Scholar 

  61. Murray MF (2003) Nicotinamide: an oral antimicrobial agent with activity against both Mycobacterium tuberculosis and human immunodeficiency virus. Clin Infect Dis 36:453–460

    Article  CAS  PubMed  Google Scholar 

  62. Murray MF, Nghiem M, Srinivasan A (1995) HIV infection decreases intracellular nicotinamide adenine dinucleotide [NAD]. Biochem Biophys Res Commun 212:126–131

    Article  CAS  PubMed  Google Scholar 

  63. O’Hara JK, Kerwin LJ, Cobbold SA, Tai J, Bedell TA, Reider PJ, Llinas M (2014) Targeting NAD+ metabolism in the human malaria parasite Plasmodium falciparum. PLoS One 9:e94061

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  64. O’Seaghdha M, Wessels MR (2013) Streptolysin O and its co-toxin NAD-glycohydrolase protect group A Streptococcus from Xenophagic killing. PLoS Pathog 9:e1003394

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  65. Olesen UH, Thougaard AV, Jensen PB, Sehested M (2010) 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 9:1609–1617

    Article  CAS  PubMed  Google Scholar 

  66. Paiva CN, Bozza MT (2014) Are reactive oxygen species always detrimental to pathogens? Antioxid Redox Signal 20:1000–1037

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  67. Panday A, Sahoo MK, Osorio D, Batra S (2015) NADPH oxidases: an overview from structure to innate immunity-associated pathologies. Cell Mol Immunol 12:5–23

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  68. Partida-Sanchez S, Cockayne DA, Monard S, Jacobson EL, Oppenheimer N, Garvy B et al (2001) Cyclic ADP-ribose production by CD38 regulates intracellular calcium release, extracellular calcium influx and chemotaxis in neutrophils and is required for bacterial clearance in vivo. Nat Med 7:1209–1216

    Article  CAS  PubMed  Google Scholar 

  69. Partida-Sanchez S, Rivero-Nava L, Shi G, Lund FE (2007) CD38: an ecto-enzyme at the crossroads of innate and adaptive immune responses. Adv Exp Med Biol 590:171–183

    Article  PubMed  Google Scholar 

  70. Pittelli M, Formentini L, Faraco G, Lapucci A, Rapizzi E, Cialdai F et al (2010) Inhibition of nicotinamide phosphoribosyltransferase: cellular bioenergetics reveals a mitochondrial insensitive NAD pool. J Biol Chem 285:34106–34114

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  71. Prendergast GC, Smith C, Thomas S, Mandik-Nayak L, Laury-Kleintop L, Metz R, Muller AJ (2014) Indoleamine 2,3-dioxygenase pathways of pathogenic inflammation and immune escape in cancer. Cancer Immunol Immunother 63:721–735

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  72. Prunier AL, Schuch R, Fernandez RE, Maurelli AT (2007) Genetic structure of the nadA and nadB antivirulence loci in Shigella spp. J Bacteriol 189:6482–6486

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  73. Prunier AL, Schuch R, Fernandez RE, Mumy KL, Kohler H, McCormick BA, Maurelli AT (2007) nadA and nadB of Shigella flexneri 5a are antivirulence loci responsible for the synthesis of quinolinate, a small molecule inhibitor of Shigella pathogenicity. Microbiology 153:2363–2372

    Article  CAS  PubMed  Google Scholar 

  74. Pulla VK, Sriram DS, Soni V, Viswanadha S, Sriram D, Yogeeswari P (2015) Targeting NAMPT for therapeutic intervention in cancer and inflammation: structure-based drug design and biological screening. Chem Biol Drug Des 86(4):881–894

    Article  CAS  PubMed  Google Scholar 

  75. Rada B, Leto TL (2008) Oxidative innate immune defenses by Nox/Duox family NADPH oxidases. Contrib Microbiol 15:164–187

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  76. Ren JH, Tao Y, Zhang ZZ, Chen WX, Cai XF, Chen K et al (2014) Sirtuin 1 regulates hepatitis B virus transcription and replication by targeting transcription factor AP-1. J Virol 88:2442–2451

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  77. Revollo JR, Korner A, Mills KF, Satoh A, Wang T, Garten A et al (2007) Nampt/PBEF/Visfatin regulates insulin secretion in beta cells as a systemic NAD biosynthetic enzyme. Cell Metab 6:363–375

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  78. Roberts KJ, Cross A, Vasieva O, Moots RJ, Edwards SW (2013) Inhibition of pre-B cell colony-enhancing factor (PBEF/NAMPT/visfatin) decreases the ability of human neutrophils to generate reactive oxidants but does not impair bacterial killing. J Leukoc Biol 94:481–492

    Article  CAS  PubMed  Google Scholar 

  79. Rodrigues V, Cordeiro-da-Silva A, Laforge M, Ouaissi A, Silvestre R, Estaquier J (2012) Modulation of mammalian apoptotic pathways by intracellular protozoan parasites. Cell Microbiol 14:325–333

    Article  CAS  PubMed  Google Scholar 

  80. Sampath D, Zabka TS, Misner DL, O’Brien T, Dragovich PS (2015) Inhibition of nicotinamide phosphoribosyltransferase (NAMPT) as a therapeutic strategy in cancer. Pharmacol Ther 151:16–31

    Article  CAS  PubMed  Google Scholar 

  81. Schmidt SV, Schultze JL (2014) New insights into IDO biology in bacterial and viral infections. Front Immunol 5:384

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  82. Schreiber V, Dantzer F, Ame JC, de Murcia G (2006) Poly(ADP-ribose): novel functions for an old molecule. Nat Rev Mol Cell Biol 7:517–528

    Article  CAS  PubMed  Google Scholar 

  83. Schroten H, Spors B, Hucke C, Stins M, Kim KS, Adam R, Daubener W (2001) Potential role of human brain microvascular endothelial cells in the pathogenesis of brain abscess: inhibition of Staphylococcus aureus by activation of indoleamine 2,3-dioxygenase. Neuropediatrics 32:206–210

    Article  CAS  PubMed  Google Scholar 

  84. Seman M, Adriouch S, Haag F, Koch-Nolte F (2004) Ecto-ADP-ribosyltransferases (ARTs): emerging actors in cell communication and signaling. Curr Med Chem 11:857–872

    Article  CAS  PubMed  Google Scholar 

  85. Sereno D, Alegre AM, Silvestre R, Vergnes B, Ouaissi A (2005) In vitro antileishmanial activity of nicotinamide. Antimicrob Agents Chemother 49:808–812

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  86. Shigemura T, Shiohara M, Kato M, Furuta S, Kaneda K, Morishita K et al (2015) Superoxide-generating Nox5alpha is functionally required for the human T-cell leukemia virus Type 1-induced cell transformation phenotype. J Virol 89:9080–9089

    Article  CAS  PubMed  Google Scholar 

  87. Singh SK, Kurnasov OV, Chen B, Robinson H, Grishin NV, Osterman AL, Zhang H (2002) Crystal structure of Haemophilus influenzae NadR protein. A bifunctional enzyme endowed with NMN adenyltransferase and ribosylnicotinimide kinase activities. J Biol Chem 277:33291–33299

    Article  CAS  PubMed  Google Scholar 

  88. Siva AC, Bushman F (2002) Poly(ADP-ribose) polymerase 1 is not strictly required for infection of murine cells by retroviruses. J Virol 76:11904–11910

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  89. Sodhi RK, Singh N, Jaggi AS (2010) Poly(ADP-ribose) polymerase-1 (PARP-1) and its therapeutic implications. Vascul Pharmacol 53:77–87

    Article  CAS  PubMed  Google Scholar 

  90. Sommer F, Backhed F (2015) The gut microbiota engages different signaling pathways to induce Duox2 expression in the ileum and colon epithelium. Mucosal Immunol 8:372–379

    Article  CAS  PubMed  Google Scholar 

  91. Sorci L, Kurnasov O, Rodionov D, Osterman A (2010) Genomics and enzymology of NAD biosynthesis. In: Mander L, Liu H-W (eds) Comprehensive natural products II. Elsevier, Oxford, pp 213–257

    Chapter  Google Scholar 

  92. Strengert M, Jennings R, Davanture S, Hayes P, Gabriel G, Knaus UG (2014) Mucosal reactive oxygen species are required for antiviral response: role of Duox in influenza a virus infection. Antioxid Redox Signal 20:2695–2709

    Article  CAS  PubMed  Google Scholar 

  93. Sun K, Metzger DW (2014) Influenza infection suppresses NADPH oxidase-dependent phagocytic bacterial clearance and enhances susceptibility to secondary methicillin-resistant Staphylococcus aureus infection. J Immunol 192:3301–3307

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  94. Takeuchi M, Niimi T, Masumoto M, Orita M, Yokota H, Yamamoto T (2014) Discovery of a novel nicotinamide phosphoribosyl transferase (NAMPT) inhibitor via in silico screening. Biol Pharm Bull 37:31–36

    Article  CAS  PubMed  Google Scholar 

  95. Tatsuno I, Isaka M, Minami M, Hasegawa T (2010) NADase as a target molecule of in vivo suppression of the toxicity in the invasive M-1 group A Streptococcal isolates. BMC Microbiol 10:144

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  96. Van Assche T, Deschacht M, da Luz RA, Maes L, Cos P (2011) Leishmania-macrophage interactions: insights into the redox biology. Free Radic Biol Med 51:337–351

    Article  PubMed  CAS  Google Scholar 

  97. Van den Bergh R, Florence E, Vlieghe E, Boonefaes T, Grooten J, Houthuys E et al (2010) Transcriptome analysis of monocyte-HIV interactions. Retrovirology 7:53

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  98. Viegas MS, do Carmo A, Silva T, Seco F, Serra V, Lacerda M, Martins TC (2007) CD38 plays a role in effective containment of mycobacteria within granulomata and polarization of Th1 immune responses against Mycobacterium avium. Microbes Infect 9:847–854

    Article  CAS  PubMed  Google Scholar 

  99. Vilcheze C, Weinrick B, Wong KW, Chen B, Jacobs WR Jr (2010) NAD+ auxotrophy is bacteriocidal for the tubercle bacilli. Mol Microbiol 76:365–377

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  100. Williamson DH, Lund P, Krebs HA (1967) The redox state of free nicotinamide-adenine dinucleotide in the cytoplasm and mitochondria of rat liver. Biochem J 103:514–527

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  101. Xie H, Lei N, Gong AY, Chen XM, Hu G (2014) Cryptosporidium parvum induces SIRT1 expression in host epithelial cells through downregulating let-7i. Hum Immunol 75:760–765

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  102. Yamahira A, Narita M, Iwabuchi M, Uchiyama T, Iwaya S, Ohiwa R et al (2014) Activation of the leukemia plasmacytoid dendritic cell line PMDC05 by Toho-1, a novel IDO inhibitor. Anticancer Res 34:4021–4028

    CAS  PubMed  Google Scholar 

  103. Yang H, Yang T, Baur JA, Perez E, Matsui T, Carmona JJ et al (2007) Nutrient-sensitive mitochondrial NAD+ levels dictate cell survival. Cell 130:1095–1107

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  104. Yu H, Schwarzer K, Forster M, Kniemeyer O, Forsbach-Birk V, Straube E, Rodel J (2010) Role of high-mobility group box 1 protein and poly(ADP-ribose) polymerase 1 degradation in Chlamydia trachomatis-induced cytopathicity. Infect Immun 78:3288–3297

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  105. Yu JW, Sun LJ, Liu W, Zhao YH, Kang P, Yan BZ (2013) Hepatitis C virus core protein induces hepatic metabolism disorders through down-regulation of the SIRT1-AMPK signaling pathway. Int J Infect Dis 17:e539–e545

    Article  CAS  PubMed  Google Scholar 

  106. Yu SW, Wang H, Poitras MF, Coombs C, Bowers WJ, Federoff HJ et al (2002) Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science 297:259–263

    Article  CAS  PubMed  Google Scholar 

  107. Zerez CR, Roth EF Jr, Schulman S, Tanaka KR (1990) Increased nicotinamide adenine dinucleotide content and synthesis in Plasmodium falciparum-infected human erythrocytes. Blood 75:1705–1710

    CAS  PubMed  Google Scholar 

  108. Zhang YJ, Reddy MC, Ioerger TR, Rothchild AC, Dartois V, Schuster BM et al (2013) Tryptophan biosynthesis protects mycobacteria from CD4 T-cell-mediated killing. Cell 155:1296–1308

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

JG was supported by PD/BD/106053/2015. BV was supported by IRD (Institut de Recherche pour le Développement) institutional funding. JE was supported by a European Community’s Seventh Framework Program under grant agreement No. 602773 (Project KINDRED), an ANR grant (LEISH-APO, France) and a Partenariat Hubert Curien (PHC) (program Volubilis, MA/11/262). JE also thanks the Canada Research Chair program for his support. RS thank FCT—Foundation for Science and Technology—for their Investigator FCT Grant (IF/00021/2014)

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Authors and Affiliations

  1. Microbiology and Infection Research Domain, Life and Health Sciences Research Institute (ICVS), School of Health Sciences, University of Minho, Braga, Portugal

    Inês Mesquita, Patrícia Varela, Ana Belinha, Joana Gaifem & Ricardo Silvestre

  2. ICVS/3B’s-PT Government Associate Laboratory, Braga/Guimarães, Portugal

    Inês Mesquita, Patrícia Varela, Ana Belinha, Joana Gaifem & Ricardo Silvestre

  3. MIVEGEC (IRD 224-CNRS 5290-Université Montpellier), Institut de Recherche pour le Développement (IRD), Montpellier, France

    Baptiste Vergnes

  4. CNRS FR 3636, Université Paris Descartes, 75006, Paris, France

    Mireille Laforge & Jérôme Estaquier

  5. Centre de Recherche du CHU de Québec, Université Laval, Quebec, G1V 4G2, Canada

    Jérôme Estaquier

Authors
  1. Inês Mesquita
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  2. Patrícia Varela
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  3. Ana Belinha
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  4. Joana Gaifem
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  5. Mireille Laforge
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  6. Baptiste Vergnes
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  7. Jérôme Estaquier
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  8. Ricardo Silvestre
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Correspondence to Jérôme Estaquier or Ricardo Silvestre.

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Mesquita, I., Varela, P., Belinha, A. et al. Exploring NAD+ metabolism in host–pathogen interactions. Cell. Mol. Life Sci. 73, 1225–1236 (2016). https://doi.org/10.1007/s00018-015-2119-4

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  • DOI: https://doi.org/10.1007/s00018-015-2119-4

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