Alterations on Cellular Redox States upon Infection and Implications for Host Cell Homeostasis

  • Inês Mesquita
  • Baptiste Vergnes
  • Ricardo Silvestre
Chapter
Part of the Experientia Supplementum book series (EXS, volume 109)

Abstract

The cofactors nicotinamide adenine dinucleotide (NAD+) and its phosphate form, NADP+, are crucial molecules present in all living cells. The delicate balance between the oxidized and reduced forms of these molecules is tightly regulated by intracellular metabolism assuring the maintenance of homeostatic conditions, which are essential for cell survival and proliferation. A recent cluster of data has highlighted the importance of the intracellular NAD+/NADH and NADP+/NADPH ratios during host–pathogen interactions, as fluctuations in the levels of these cofactors and in precursors’ bioavailability may condition host response and, therefore, pathogen persistence or elimination. Furthermore, an increasing interest has been given towards how pathogens are capable of hijacking host cell proteins in their own advantage and, consequently, alter cellular redox states and immune function. Here, we review the basic principles behind biosynthesis and subcellular compartmentalization of NAD+ and NADP+, as well as the importance of these cofactors during infection, with a special emphasis on pathogen-driven modulation of host NAD+/NADP+ levels and contribution to the associated immune response.

Keywords

Nicotinamide adenine dinucleotide (NAD+Host–pathogen interaction NAD+/NADH ratio NADPH Sirtuins L-Tryptophan 

Notes

Funding Statement

This work was supported by the Northern Portugal Regional Operational Programme (NORTE 2020), under the Portugal 2020 Partnership Agreement, through the European Regional Development Fund (FEDER) (NORTE-01-0145-FEDER-000013) and the Fundação para a Ciência e Tecnologia (FCT) (contracts SFRH/BD/120127/2016 to IM and IF/00021/2014 to RS), and Infect-Era (project INLEISH).

References

  1. 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:e01690-14PubMedPubMedCentralCrossRefGoogle Scholar
  2. Bellac CL, Coimbra RS, Christen S, Leib SL (2006) Pneumococcal meningitis causes accumulation of neurotoxic kynurenine metabolites in brain regions prone to injury. Neurobiol Dis 24:395–402PubMedCrossRefGoogle Scholar
  3. Bellac CL, Coimbra RS, Christen S, Leib SL (2010) Inhibition of the Kynurenine-NAD + pathway leads to energy failure and exacerbates apoptosis in pneumococcal meningitis. J Neuropathol Exp Neurol 69:1096–1104PubMedCrossRefGoogle Scholar
  4. Bianchi M, Hakkim A, Brinkmann V, Siler U, Seger RA, Zychlinsky A, Reichenbach J (2009) Restoration of NET formation by gene therapy in CGD controls aspergillosis. Blood 114:2619–2622PubMedPubMedCentralCrossRefGoogle Scholar
  5. Bianchi M, Niemiec MJ, Siler U, Urban CF, Reichenbach J (2011) Restoration of anti-Aspergillus defense by neutrophil extracellular traps in human chronic granulomatous disease after gene therapy is calprotectin-dependent. J Allergy Clin Immunol 127:1243–1252PubMedCrossRefGoogle Scholar
  6. Boasso A, Herbeuval JP, Hardy AW, Anderson SA, Dolan MJ, Fuchs D, Shearer GM (2007) HIV inhibits CD4+ T-cell proliferation by inducing indoleamine 2,3-dioxygenase in plasmacytoid dendritic cells. Blood 109:3351–3359PubMedPubMedCentralCrossRefGoogle Scholar
  7. Boasso A, Hardy AW, Anderson SA, Dolan MJ, Shearer GM (2008) HIV-induced type I interferon and tryptophan catabolism drive T cell dysfunction despite phenotypic activation. PLoS One 3:e2961PubMedPubMedCentralCrossRefGoogle Scholar
  8. Brown SA, Palmer KL, Whiteley M (2008) Revisiting the host as a growth medium. Nat Rev Microbiol 6:657–666PubMedPubMedCentralCrossRefGoogle Scholar
  9. Cardoso F, Castro F, Moreira-Teixeira L, Sousa J, Torrado E, Silvestre R, Castro AG, Saraiva M, Pais TF (2015) Myeloid sirtuin 2 expression does not impact long-term Mycobacterium tuberculosis control. PLoS One 10:e0131904PubMedPubMedCentralCrossRefGoogle Scholar
  10. Cheng SC, Scicluna BP, Arts RJW, Gresnigt MS, Lachmandas E, Giamarellos-Bourboulis EJ, Kox M, Manjeri GR, Wagenaars JAL, Cremer OL et al (2016) Broad defects in the energy metabolism of leukocytes underlie immunoparalysis in sepsis. Nat Immunol 17:406–413PubMedCrossRefGoogle Scholar
  11. Cheng CY, Gutierrez NM, Marzuki MB, Lu X, Foreman TW, Paleja B, Lee B, Balachander A, Chen J, Tsenova L et al (2017) Host sirtuin 1 regulates mycobacterial immunopathogenesis and represents a therapeutic target against tuberculosis. Sci Immunol 2:eaaj1789PubMedPubMedCentralCrossRefGoogle Scholar
  12. Cheong W-C, Park J-H, Kang H-R, Song MJ (2015) Down-regulation of poly (ADP-ribose) polymerase-1 by a viral processivity factor facilitates gammaherpesvirus lytic replication. J Virol 89:9676–9682PubMedPubMedCentralCrossRefGoogle Scholar
  13. Conti F, Lugo-Reyes SO, Blancas Galicia L, He J, Aksu G, Borges de Oliveira E, Deswarte C, Hubeau M, Karaca N, de Suremain M et al (2016) Mycobacterial disease in patients with chronic granulomatous disease: a retrospective analysis of 71 cases. J Allergy Clin Immunol 138:241–248.e3PubMedCrossRefGoogle Scholar
  14. 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 86:1153–1159PubMedCrossRefGoogle Scholar
  15. Deffert C, Cachat J, Krause K-H (2014) Phagocyte NADPH oxidase, chronic granulomatous disease and mycobacterial infections. Cell Microbiol 16:1168–1178PubMedCrossRefGoogle Scholar
  16. Di Stefano M, Conforti L (2013) Diversification of NAD biological role: the importance of location. FEBS J 280:4711–4728PubMedCrossRefGoogle Scholar
  17. Dölle 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 67:433–443PubMedCrossRefGoogle Scholar
  18. Dousa TP, Chini EN, Beers KW (1996) Adenine nucleotide diphosphates: emerging second messengers acting via intracellular Ca2+ release. Am J Physiol 271:C1007–C1024PubMedCrossRefGoogle Scholar
  19. El-Zaatari M, Chang Y-M, Zhang M, Franz M, Shreiner A, McDermott AJ, van der Sluijs KF, Lutter R, Grasberger H, Kamada N et al (2014) Tryptophan catabolism restricts IFN-γ–expressing neutrophils and Clostridium difficile immunopathology. J Immunol 193:807–816PubMedPubMedCentralCrossRefGoogle Scholar
  20. Eskandarian HA, Impens F, Nahori M-A, Soubigou G, Coppee J-Y, Cossart P, Hamon MA (2013) A role for SIRT2-dependent histone H3K18 deacetylation in bacterial infection. Science 341:1238858PubMedCrossRefGoogle Scholar
  21. Estrada-Figueroa LA, Ramírez-Jiménez Y, Osorio-Trujillo C, Shibayama M, Navarro-García F, García-Tovar C, Talamás-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 33:661–668PubMedCrossRefGoogle Scholar
  22. Fallarino F, Grohmann U, You S, McGrath BC, Cavener DR, Vacca C, Orabona C, Bianchi R, Belladonna ML, Volpi C et al (2006) The combined effects of tryptophan starvation and tryptophan catabolites down-regulate T Cell receptor-chain and induce a regulatory phenotype in naive T cells. J Immunol 176:6752–6761PubMedCrossRefGoogle Scholar
  23. Fan J, Ye J, Kamphorst JJ, Shlomi T, Thompson CB, Rabinowitz JD (2014) Quantitative flux analysis reveals folate-dependent NADPH production. Nature 510:298–302PubMedPubMedCentralCrossRefGoogle Scholar
  24. Gameiro PA, Laviolette LA, Kelleher JK, Iliopoulos O, Stephanopoulos G (2013) Cofactor balance by nicotinamide nucleotide transhydrogenase (NNT) coordinates reductive carboxylation and glucose catabolism in the tricarboxylic acid (TCA) cycle. J Biol Chem 288:12967–12977PubMedPubMedCentralCrossRefGoogle Scholar
  25. Ganesan R, Hos NJ, Gutierrez S, Fischer J, Stepek JM, Daglidu E, Krönke M, Robinson N (2017) Salmonella Typhimurium disrupts Sirt1/AMPK checkpoint control of mTOR to impair autophagy. PLoS Pathog 13:e1006227PubMedPubMedCentralCrossRefGoogle Scholar
  26. Grez M, Reichenbach J, Schwäble J, Seger R, Dinauer MC, Thrasher AJ (2011) Gene therapy of chronic granulomatous disease: the engraftment dilemma. Mol Ther 19:28–35PubMedCrossRefGoogle Scholar
  27. Gurtner GJ, Newberry RD, Schloemann SR, McDonald KG, Stenson WF (2003) Inhibition of indoleamine 2,3-dioxygenase augments trinitrobenzene sulfonic acid colitis in mice. Gastroenterology 125:1762–1773PubMedCrossRefGoogle Scholar
  28. Gutierrez DA, Valdes L, Serguera C, Llano M (2016) Poly(ADP-ribose) polymerase-1 silences retroviruses independently of viral DNA integration or heterochromatin formation. J Gen Virol 97:1686–1692PubMedCrossRefGoogle Scholar
  29. Ha E-M (2005) A direct role for dual oxidase in Drosophila gut immunity. Science 310:847–850PubMedCrossRefGoogle 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 U S A 98:3364–3368PubMedPubMedCentralCrossRefGoogle Scholar
  31. He M, Gao SJ (2014) A novel role of SIRT1 in gammaherpesvirus latency and replication. Cell Cycle 13:3328–3330PubMedPubMedCentralCrossRefGoogle Scholar
  32. Hogan D, Wheeler RT (2014) The complex roles of NADPH oxidases in fungal infection. Cell Microbiol 16:1156–1167PubMedPubMedCentralCrossRefGoogle Scholar
  33. Houtkooper RH, Pirinen E, Auwerx J (2012) Sirtuins as regulators of metabolism and healthspan. Nat Rev Mol Cell Biol 13:225–238PubMedPubMedCentralCrossRefGoogle Scholar
  34. Kameoka M, Nukuzuma S, Itaya A, Tanaka Y, Ota K, Inada Y, Ikuta K, Yoshihara K (2005) Poly(ADP-ribose)polymerase-1 is required for integration of the human immunodeficiency virus type 1 genome near centromeric alphoid DNA in human and murine cells. Biochem Biophys Res Commun 334:412–417PubMedCrossRefGoogle Scholar
  35. Kim S-H, Lee W-J (2014) Role of DUOX in gut inflammation: lessons from Drosophila model of gut-microbiota interactions. Front Cell Infect Microbiol 3:116PubMedPubMedCentralCrossRefGoogle Scholar
  36. 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 305:147–152PubMedCrossRefGoogle Scholar
  37. 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 22:39–49PubMedCrossRefGoogle Scholar
  38. Lau C, Dölle C, Gossmann TI, Agledal L, Niere M, Ziegler M (2010) Isoform-specific targeting and interaction domains in human nicotinamide mononucleotide adenylyltransferases. J Biol Chem 285:18868–18876PubMedPubMedCentralCrossRefGoogle Scholar
  39. Lee WP, Hou MC, Lan KH, Li CP, Chao Y, Lin HC, Lee SD (2016) Helicobacter pylori-induced chronic inflammation causes telomere shortening of gastric mucosa by promoting PARP-1-mediated non-homologous end joining of DNA. Arch Biochem Biophys 606:90–98PubMedCrossRefGoogle Scholar
  40. Lewis CA, Parker SJ, Fiske BP, McCloskey D, Gui DY, Green CR, Vokes NI, Feist AM, Vander Heiden MG, Metallo CM (2014) Tracing compartmentalized NADPH metabolism in the cytosol and mitochondria of mammalian cells. Mol Cell 55:253–263PubMedPubMedCentralCrossRefGoogle Scholar
  41. Li W, Katz BP, Spinola SM (2011) Haemophilus ducreyi lipooligosaccharides induce expression of the immunosuppressive enzyme indoleamine 2,3-dioxygenase via type I interferons and tumor necrosis factor alpha in human dendritic cells. Infect Immun 79:3338–3347PubMedPubMedCentralCrossRefGoogle Scholar
  42. Li Q, He M, Zhou F, Ye F, Gao S-J (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 88:6355–6367PubMedPubMedCentralCrossRefGoogle Scholar
  43. Lischke T, Heesch K, Schumacher V, Schneider M, Haag F, Koch-Nolte F, Mittrücker HW (2013) CD38 controls the innate immune response against listeria monocytogenes. Infect Immun 81:4091–4099PubMedPubMedCentralCrossRefGoogle Scholar
  44. Liu TF, Vachharajani VT, Yoza BK, McCall CE (2012) NAD+-dependent sirtuin 1 and 6 proteins coordinate a switch from glucose to fatty acid oxidation during the acute inflammatory response. J Biol Chem 287:25758–25769PubMedPubMedCentralCrossRefGoogle Scholar
  45. Liu W, Lin Y, Xiao H, Xing S, Chen H, Chi P, Zhang G (2014) Epstein-Barr virus infection induces indoleamine 2,3-dioxygenase expression in human monocyte-derived macrophages through p38/mitogen-activated protein kinase and NF-κB pathways: impairment in T cell functions. J Virol 88:6660–6671PubMedPubMedCentralCrossRefGoogle Scholar
  46. Liu TF, Vachharajani V, Millet P, Bharadwaj MS, Molina AJ, McCall CE (2015) Sequential actions of SIRT1-RELB-SIRT3 coordinate nuclear-mitochondrial communication during immunometabolic adaptation to acute inflammation and sepsis. J Biol Chem 290:396–408PubMedCrossRefGoogle Scholar
  47. Liu L, Shah S, Fan J, Park JO, Wellen KE, Rabinowitz JD (2016) Malic enzyme tracers reveal hypoxia-induced switch in adipocyte NADPH pathway usage. Nat Chem Biol 12:345–352PubMedPubMedCentralCrossRefGoogle Scholar
  48. Lupey-Green LN, Moquin SA, Martin KA, McDevitt SM, Hulse M, Caruso LB, Pomerantz RT, Miranda JL, Tempera I (2017) PARP1 restricts Epstein Barr Virus lytic reactivation by binding the BZLF1 promoter. Virology 507:220–230PubMedPubMedCentralCrossRefGoogle Scholar
  49. Magni G (2008) Enzymology of mammalian NAD metabolism in health and disease. Front Biosci 3:6135CrossRefGoogle Scholar
  50. Martin KA, Lupey LN, Tempera I (2016) Epstein-Barr Virus oncoprotein LMP1 mediates epigenetic changes in host gene expression through PARP1. J Virol 90:8520–8530PubMedPubMedCentralCrossRefGoogle Scholar
  51. Matalonga J, Glaria E, Bresque M, Escande C, Carbó JM, Kiefer K, Vicente R, León TE, Beceiro S, Pascual-García M et al (2017) The nuclear receptor LXR limits bacterial infection of host macrophages through a mechanism that impacts cellular NAD metabolism. Cell Rep 18:1241–1255PubMedCrossRefGoogle Scholar
  52. Medana IM, Mai NTH, Day NPJ, Hien TT, Bethell D, Phu NH, Farrar J, White NJ, Turner GDH (2001) Cellular stress and injury responses in the brains of adult Vietnamese patients with fatal Plasmodium falciparum malaria. Neuropathol Appl Neurobiol 27:421–433PubMedCrossRefGoogle Scholar
  53. Mesquita I, Varela P, Belinha A, Gaifem J, Laforge M, Vergnes B, Estaquier J, Silvestre R (2016) Exploring NAD+ metabolism in host-pathogen interactions. Cell Mol Life Sci 73:1225–1236PubMedCrossRefGoogle Scholar
  54. Michan S, Sinclair D (2007) Sirtuins in mammals: insights into their biological function. Biochem J 404:1–13PubMedPubMedCentralCrossRefGoogle Scholar
  55. Michos A, Gryllos I, Håkansson 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 281:8216–8223PubMedCrossRefGoogle Scholar
  56. Mittal M, Siddiqui MR, Tran K, Reddy SP, Malik AB (2014) Reactive oxygen species in inflammation and tissue injury. Antioxid Redox Signal 20:1126–1167PubMedPubMedCentralCrossRefGoogle Scholar
  57. Moreira D, Rodrigues V, Abengozar M, Rivas L, Rial E, Laforge M, Li X, Foretz M, Viollet B, Estaquier J et al (2015) Leishmania infantum modulates host macrophage mitochondrial metabolism by hijacking the SIRT1-AMPK axis. PLoS Pathog 11:1–24CrossRefGoogle Scholar
  58. Moreschi I, Bruzzone S, Nicholas RA, Fruscione F, Sturla L, Benvenuto F, Usai C, Meis S, Kassack MU, Zocchi E et al (2006) Extracellular NAD+ is an agonist of the human P2Y 11 purinergic receptor in human granulocytes. J Biol Chem 281:31419–31429PubMedCrossRefGoogle Scholar
  59. Mori V, Amici A, Mazzola F, Di Stefano M, Conforti L, Magni G, Ruggieri S, Raffaelli N, Orsomando G (2014) Metabolic profiling of alternative NAD biosynthetic routes in mouse tissues. PLoS One 9:e113939PubMedPubMedCentralCrossRefGoogle Scholar
  60. Müller S (2004) Redox and antioxidant systems of the malaria parasite Plasmodium falciparum. Mol Microbiol 53:1291–1305PubMedCrossRefGoogle Scholar
  61. Munn DH, Mellor AL (2013) Indoleamine 2,3 dioxygenase and metabolic control of immune responses. Trends Immunol 34:137–143PubMedCrossRefGoogle Scholar
  62. Murray MF, Srinivasan A (1995) Nicotinamide inhibits HIV-1 in both acute and chronic in vitro infection. Biochem Biophys Res Commun 210:954–959PubMedCrossRefGoogle Scholar
  63. Murray MF, Nghiem M, Srinivasan A (1995) HIV infection decreases intracellular nicotinamide adenine dinucleotide [NAD]. Biochem Biophys Res Commun 212:126–131PubMedCrossRefGoogle Scholar
  64. Navarro J, Gozalbo-López B, Méndez AC, Dantzer F, Schreiber V, Martínez C, Arana DM, Farrés J, Revilla-Nuin B, Bueno MF et al (2017) PARP-1/PARP-2 double deficiency in mouse T cells results in faulty immune responses and T lymphomas. Sci Rep 7:41962PubMedPubMedCentralCrossRefGoogle Scholar
  65. O’Seaghdha M, Wessels MR (2013) Streptolysin O and its co-toxin NAD-glycohydrolase protect group A Streptococcus from xenophagic killing. PLoS Pathog 9:e1003394PubMedPubMedCentralCrossRefGoogle Scholar
  66. Olszewski KL, Morrisey JM, Wilinski D, Burns JM, Vaidya AB, Rabinowitz JD, Llinás M (2009) Host-parasite interactions revealed by Plasmodium falciparum metabolomics. Cell Host Microbe 5:191–199PubMedPubMedCentralCrossRefGoogle Scholar
  67. Paiva CN, Bozza MT (2014) Are reactive oxygen species always detrimental to pathogens? Antioxid Redox Signal 20:1000–1037PubMedPubMedCentralCrossRefGoogle Scholar
  68. Palmer CS, Cherry CL, Sada-Ovalle I, Singh A, Crowe SM (2016) Glucose metabolism in T cells and monocytes: new perspectives in HIV pathogenesis. EBioMedicine 6:31–41PubMedPubMedCentralCrossRefGoogle Scholar
  69. Panday A, Sahoo MK, Osorio D, Batra S (2015) NADPH oxidases: an overview from structure to innate immunity-associated pathologies. Cell Mol Immunol 12:5–23PubMedCrossRefGoogle Scholar
  70. Partida-Sánchez S, Cockayne DA, Monard S, Jacobson EL, Oppenheimer N, Garvy B, Kusser K, Goodrich S, Howard M, Harmsen A 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 7:1209–1216PubMedCrossRefGoogle Scholar
  71. Partidá-Sánchez 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 590:171–183PubMedCrossRefGoogle Scholar
  72. Peek CB, Affinati AH, Ramsey KM, Kuo H-Y, Yu W, Sena LA, Ilkayeva O, Marcheva B, Kobayashi Y, Omura C et al (2013) Circadian clock NAD+ cycle drives mitochondrial oxidative metabolism in mice. Science 342:1243417–1243417PubMedPubMedCentralCrossRefGoogle Scholar
  73. Pircalabioru G, Aviello G, Kubica M, Zhdanov A, Paclet MH, Brennan L, Hertzberger R, Papkovsky D, Bourke B, Knaus UG (2016) Defensive mutualism rescues NADPH oxidase inactivation in gut infection. Cell Host Microbe 19:651–663PubMedCrossRefGoogle Scholar
  74. Pittelli M, Formentini L, Faraco G, Lapucci A, Rapizzi E, Cialdai F, Romano G, Moneti G, Moroni F, Chiarugi A (2010) Inhibition of nicotinamide phosphoribosyltransferase: cellular bioenergetics reveals a mitochondrial insensitive NAD pool. J Biol Chem 285:34106–34114PubMedPubMedCentralCrossRefGoogle Scholar
  75. Pollak N, Dölle C, Ziegler M (2007) The power to reduce: pyridine nucleotides – small molecules with a multitude of functions. Biochem J 402:205–218PubMedPubMedCentralCrossRefGoogle Scholar
  76. Potula R, Poluektova L, Knipe B, Chrastil J, Heilman D, Dou H, Takikawa O, Munn DH, Gendelman HE, Persidsky Y (2005) Inhibition of indoleamine 2,3-dioxygenase (IDO) enhances elimination of virus-infected macrophages in an animal model of HIV-1 encephalitis. Blood 106:2382–2390PubMedPubMedCentralCrossRefGoogle Scholar
  77. 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 63:721–735PubMedPubMedCentralCrossRefGoogle Scholar
  78. Rada B, Leto T (2008) Oxidative innate immune defenses by Nox/Duox family NADPH oxidases. Contrib Microbiol 15:164–187PubMedPubMedCentralCrossRefGoogle Scholar
  79. Ren J-H, Tao Y, Zhang Z-Z, Chen W-X, Cai X-F, Chen K, Ko BCB, Song C-L, Ran L-K, Li W-Y et al (2014) Sirtuin 1 regulates hepatitis B virus transcription and replication by targeting transcription factor AP-1. J Virol 88:2442–2451PubMedPubMedCentralCrossRefGoogle Scholar
  80. Revollo JR, Körner A, Mills KF, Satoh A, Wang T, Garten A, Dasgupta B, Sasaki Y, Wolberger C, Townsend RR et al (2007) Nampt/PBEF/Visfatin regulates insulin secretion in beta cells as a systemic NAD biosynthetic enzyme. Cell Metab 6:363–375PubMedPubMedCentralCrossRefGoogle Scholar
  81. Rom S, Reichenbach NL, Dykstra H, Persidsky Y (2015) The dual action of poly(ADP-ribose) polymerase-1 (PARP-1) inhibition in HIV-1 infection: HIV-1 ltr inhibition and diminution in Rho GTPase activity. Front Microbiol 6:878PubMedPubMedCentralCrossRefGoogle Scholar
  82. Schmidt SV, Schultze JL (2014) New insights into IDO biology in bacterial and viral infections. Front Immunol 5:384PubMedPubMedCentralCrossRefGoogle Scholar
  83. Schreiber V, Dantzer F, Amé JC, De Murcia G (2006) Poly(ADP-ribose): novel functions for an old molecule. Nat Rev Mol Cell Biol 7:517–528PubMedCrossRefGoogle Scholar
  84. Segal BH, Romani LR (2009) Invasive aspergillosis in chronic granulomatous disease. Med Mycol 47(Suppl 1):S282–S290PubMedCrossRefGoogle Scholar
  85. Seman M, Adriouch S, Haag F, Koch-Nolte F (2004) Ecto-ADP-ribosyltransferases (ARTs): emerging actors in cell communication and signaling. Curr Med Chem 11:857–872PubMedCrossRefGoogle Scholar
  86. Sharma O, O’Seaghdha M, Velarde JJ, Wessels MR (2016) NAD+-glycohydrolase promotes intracellular survival of group A Streptococcus. PLoS Pathog 12:e1005468PubMedPubMedCentralCrossRefGoogle Scholar
  87. Siva AC, Bushman F (2002) Poly(ADP-ribose) polymerase 1 is not strictly required for infection of murine cells by retroviruses. J Virol 76:11904–11910PubMedPubMedCentralCrossRefGoogle Scholar
  88. Sodhi RK, Singh N, Jaggi AS (2010) Poly(ADP-ribose) polymerase-1 (PARP-1) and its therapeutic implications. Vascul Pharmacol 53:77–87PubMedCrossRefGoogle Scholar
  89. 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 10:144PubMedPubMedCentralCrossRefGoogle Scholar
  90. Thakur BK, Chandra A, Dittrich T, Welte K, Chandra P (2012) Inhibition of SIRT1 by HIV-1 viral protein Tat results in activation of p53 pathway. Biochem Biophys Res Commun 424:245–250PubMedCrossRefGoogle Scholar
  91. Tibbetts AS, Appling DR (2010) Compartmentalization of mammalian folate-mediated one-carbon metabolism. Annu Rev Nutr 30:57–81PubMedCrossRefGoogle Scholar
  92. Uyoga S, Ndila CM, Macharia AW, Nyutu G, Shah S, Peshu N, Clarke GM, Kwiatkowski DP, Rockett KA, Williams TN (2015) Glucose-6-phosphate dehydrogenase deficiency and the risk of malaria and other diseases in children in Kenya: a case-control and a cohort study. Lancet Haematol 2:e437–e444PubMedPubMedCentralCrossRefGoogle Scholar
  93. Van Assche T, Deschacht M, Da Luz RAI, Maes L, Cos P (2011) Leishmania-macrophage interactions: insights into the redox biology. Free Radic Biol Med 51:337–351PubMedCrossRefGoogle Scholar
  94. Van den Bergh R, Florence E, Vlieghe E, Boonefaes T, Grooten J, Houthuys E, Tran H, Gali Y, De Baetselier P, Vanham G et al (2010) Transcriptome analysis of monocyte-HIV interactions. Retrovirology 7:53PubMedPubMedCentralCrossRefGoogle Scholar
  95. VanLinden MR, Dölle C, Pettersen IK, Kulikova VA, Niere M, Agrimi G, Dyrstad SE, Palmieri F, Nikiforov AA, Tronstad KJ, Ziegler M (2015) Subcellular distribution of NAD+ between cytosol and mitochondria determines the metabolic profile of human cells. J Biol Chem 290(46):27644–27659.  https://doi.org/10.1074/jbc.M115.654129PubMedPubMedCentralCrossRefGoogle Scholar
  96. 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 9:847–854PubMedCrossRefGoogle Scholar
  97. Vujkovic-Cvijin I, Swainson LA, Chu SN, Ortiz AM, Santee CA, Petriello A, Dunham RM, Fadrosh DW, Lin DL, Faruqi AA et al (2015) Gut-resident Lactobacillus abundance associates with IDO1 inhibition and Th17 dynamics in SIV-infected macaques. Cell Rep 13:1589–1597PubMedPubMedCentralCrossRefGoogle Scholar
  98. Wan X, Wen JJ, Koo SJ, Liang LY, Garg NJ (2016) SIRT1-PGC1α-NFκB pathway of oxidative and inflammatory stress during Trypanosoma cruzi infection: benefits of SIRT1-targeted therapy in improving heart function in Chagas disease. PLoS Pathog. 12:e1005954PubMedPubMedCentralCrossRefGoogle Scholar
  99. Wang G, Huang X, Li Y, Guo K, Ning P, Zhang Y (2013) PARP-1 inhibitor, DPQ, attenuates LPS-induced acute lung injury through inhibiting NF-κB-mediated inflammatory response. PLoS One 8:e79757PubMedPubMedCentralCrossRefGoogle Scholar
  100. Williamson D, Lund P, Krebs H (1967) The redox state of free nicotinamide-adenine dinucleotide in the cytoplasm and mitochondria of rat liver. Biochem J 103:514–527PubMedPubMedCentralCrossRefGoogle Scholar
  101. Wise DR, Ward PS, Shay JES, Cross JR, Gruber JJ, Sachdeva UM, Platt JM, DeMatteo RG, Simon MC, Thompson CB (2011) Hypoxia promotes isocitrate dehydrogenase-dependent carboxylation of -ketoglutarate to citrate to support cell growth and viability. Proc Natl Acad Sci 108:19611–19616PubMedPubMedCentralCrossRefGoogle Scholar
  102. Wu X, Deng G, Li M, Li Y, Ma C, Wang Y, Liu X (2015) Wnt/β-Catenin signaling reduces Bacillus Calmette-Guerin-induced macrophage necrosis through a ROS-mediated PARP/AIF-dependent pathway. BMC Immunol 16:16PubMedPubMedCentralCrossRefGoogle Scholar
  103. 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 75:760–765PubMedPubMedCentralCrossRefGoogle Scholar
  104. Yang H, Yang T, Baur JA, Perez E, Matsui T, Carmona JJ, Lamming DWW, Souza-Pinto NC, Bohr VA, Rosenzweig A et al (2007) Nutrient-sensitive mitochondrial NAD+ levels dictate cell survival. Cell 130:1095–1107PubMedPubMedCentralCrossRefGoogle Scholar
  105. Yeung AWS, Wu W, Freewan M, Stocker R, King NJC, Thomas SR (2012) Flavivirus infection induces indoleamine 2,3-dioxygenase in human monocyte-derived macrophages via tumor necrosis factor and NF-κB. J Leukoc Biol 91:657–666PubMedCrossRefGoogle Scholar
  106. Yu SW, Wang H, Poitras MF, Coombs C, Bowers WJ, Federoff HJ, Poirier GG, Dawson TM, Dawson VL (2002) Mediation of poly(ADP-ribose) polymerase-1 – dependent cell death by apoptosis-inducing factor. Science 297:259–263PubMedCrossRefGoogle Scholar
  107. Zerez CR, Roth EF, Schulman S, Tanaka KR (1990) Increased nicotinamide adenine dinucleotide content and synthesis in Plasmodium falciparum-infected human erythrocytes. Blood 75:1705–1710PubMedGoogle Scholar
  108. Zhang HS, Zhou Y, Wu MR, Zhou HS, Xu F (2009) Resveratrol inhibited Tat-induced HIV-1 LTR transactivation via NAD+-dependent SIRT1 activity. Life Sci 85:484–489PubMedCrossRefGoogle Scholar
  109. Zhang H-S, Sang W-W, Wang Y-O, Liu W (2010) Nicotinamide phosphoribosyltransferase/sirtuin 1 pathway is involved in human immunodeficiency virus type 1 Tat-mediated long terminal repeat transactivation. J Cell Biochem 110:1464–1470PubMedCrossRefGoogle Scholar
  110. Zhang HS, Chen XY, Wu TC, Zhang FJ (2014) Tanshinone II A inhibits tat-induced HIV-1 transactivation through redox-regulated AMPK/Nampt pathway. J Cell Physiol 229:1193–1201PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Inês Mesquita
    • 1
    • 2
  • Baptiste Vergnes
    • 3
  • Ricardo Silvestre
    • 1
    • 2
  1. 1.Life and Health Sciences Research Institute (ICVS), School of Health Sciences, University of MinhoBragaPortugal
  2. 2.ICVS/3B’s-PT Government Associate LaboratoryBraga/GuimarãesPortugal
  3. 3.MIVEGEC (IRD 224-CNRS 5290-Université Montpellier), Institut de Recherche pour le Développement (IRD)MontpellierFrance

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