Skip to main content

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

  • Chapter
  • First Online:
Metabolic Interaction in Infection

Part of the book series: Experientia Supplementum ((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.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 99.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 129.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 159.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • 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:e01690-14

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 24:395–402

    Article  CAS  PubMed  Google Scholar 

  • 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 69:1096–1104

    Article  CAS  PubMed  Google Scholar 

  • 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 114:2619–2622

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 127:1243–1252

    Article  CAS  PubMed  Google Scholar 

  • 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 109:3351–3359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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:e2961

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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:e0131904

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 17:406–413

    Article  CAS  PubMed  Google Scholar 

  • 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:eaaj1789

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 89:9676–9682

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.e3

    Article  PubMed  Google Scholar 

  • 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 

  • Deffert C, Cachat J, Krause K-H (2014) Phagocyte NADPH oxidase, chronic granulomatous disease and mycobacterial infections. Cell Microbiol 16:1168–1178

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • 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 67:433–443

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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 193:807–816

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 341:1238858

    Article  PubMed  CAS  Google Scholar 

  • 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 33:661–668

    Article  CAS  PubMed  Google Scholar 

  • 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 176:6752–6761

    Article  CAS  PubMed  Google Scholar 

  • Fan J, Ye J, Kamphorst JJ, Shlomi T, Thompson CB, Rabinowitz JD (2014) Quantitative flux analysis reveals folate-dependent NADPH production. Nature 510:298–302

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 288:12967–12977

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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:e1006227

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Grez M, Reichenbach J, Schwäble J, Seger R, Dinauer MC, Thrasher AJ (2011) Gene therapy of chronic granulomatous disease: the engraftment dilemma. Mol Ther 19:28–35

    Article  CAS  PubMed  Google Scholar 

  • 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 125:1762–1773

    Article  CAS  PubMed  Google Scholar 

  • 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 97:1686–1692

    Article  CAS  PubMed  Google Scholar 

  • Ha E-M (2005) A direct role for dual oxidase in Drosophila gut immunity. Science 310:847–850

    Article  CAS  PubMed  Google Scholar 

  • 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 98:3364–3368

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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  PubMed Central  Google Scholar 

  • 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 334:412–417

    Article  CAS  PubMed  Google Scholar 

  • 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 3:116

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 

  • 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 

  • 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 285:18868–18876

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 606:90–98

    Article  CAS  PubMed  Google Scholar 

  • 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 55:253–263

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 79:3338–3347

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 88:6355–6367

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 81:4091–4099

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 287:25758–25769

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 88:6660–6671

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 290:396–408

    Article  CAS  PubMed  Google Scholar 

  • 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 12:345–352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 507:220–230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Magni G (2008) Enzymology of mammalian NAD metabolism in health and disease. Front Biosci 3:6135

    Article  Google Scholar 

  • Martin KA, Lupey LN, Tempera I (2016) Epstein-Barr Virus oncoprotein LMP1 mediates epigenetic changes in host gene expression through PARP1. J Virol 90:8520–8530

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 18:1241–1255

    Article  CAS  PubMed  Google Scholar 

  • 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 27:421–433

    Article  CAS  PubMed  Google Scholar 

  • 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 73:1225–1236

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 281:8216–8223

    Article  CAS  PubMed  Google Scholar 

  • Mittal M, Siddiqui MR, Tran K, Reddy SP, Malik AB (2014) Reactive oxygen species in inflammation and tissue injury. Antioxid Redox Signal 20:1126–1167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 11:1–24

    Article  CAS  Google Scholar 

  • 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 281:31419–31429

    Article  CAS  PubMed  Google Scholar 

  • 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:e113939

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Munn DH, Mellor AL (2013) Indoleamine 2,3 dioxygenase and metabolic control of immune responses. Trends Immunol 34:137–143

    Article  CAS  PubMed  Google Scholar 

  • Murray MF, Srinivasan A (1995) Nicotinamide inhibits HIV-1 in both acute and chronic in vitro infection. Biochem Biophys Res Commun 210:954–959

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • 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 7:41962

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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  PubMed Central  CAS  Google Scholar 

  • 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 5:191–199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 6:31–41

    Article  PubMed  PubMed Central  Google Scholar 

  • 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  CAS  PubMed  Google Scholar 

  • 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 7:1209–1216

    Article  PubMed  Google Scholar 

  • 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 590:171–183

    Article  PubMed  Google Scholar 

  • 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 342:1243417–1243417

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 19:651–663

    Article  CAS  PubMed  Google Scholar 

  • 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 285:34106–34114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pollak N, Dölle C, Ziegler M (2007) The power to reduce: pyridine nucleotides – small molecules with a multitude of functions. Biochem J 402:205–218

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 106:2382–2390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 88:2442–2451

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 6:363–375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 6:878

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Segal BH, Romani LR (2009) Invasive aspergillosis in chronic granulomatous disease. Med Mycol 47(Suppl 1):S282–S290

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Sharma O, O’Seaghdha M, Velarde JJ, Wessels MR (2016) NAD+-glycohydrolase promotes intracellular survival of group A Streptococcus. PLoS Pathog 12:e1005468

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 

  • 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  PubMed Central  CAS  Google Scholar 

  • 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 424:245–250

    Article  CAS  PubMed  Google Scholar 

  • Tibbetts AS, Appling DR (2010) Compartmentalization of mammalian folate-mediated one-carbon metabolism. Annu Rev Nutr 30:57–81

    Article  CAS  PubMed  Google Scholar 

  • 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–e444

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 51:337–351

    Article  PubMed  CAS  Google Scholar 

  • 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 7:53

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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.M115.654129

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 

  • 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 13:1589–1597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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:e1005954

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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:e79757

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 103:514–527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 108:19611–19616

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 16:16

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 130:1095–1107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 91:657–666

    Article  CAS  PubMed  Google Scholar 

  • 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 297:259–263

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • 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 85:484–489

    Article  CAS  PubMed  Google Scholar 

  • 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 110:1464–1470

    Article  CAS  PubMed  Google Scholar 

  • 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 229:1193–1201

    Article  CAS  PubMed  Google Scholar 

Download references

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).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ricardo Silvestre .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer International Publishing AG, part of Springer Nature

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Mesquita, I., Vergnes, B., Silvestre, R. (2018). Alterations on Cellular Redox States upon Infection and Implications for Host Cell Homeostasis. In: Silvestre, R., Torrado, E. (eds) Metabolic Interaction in Infection. Experientia Supplementum, vol 109. Springer, Cham. https://doi.org/10.1007/978-3-319-74932-7_4

Download citation

Publish with us

Policies and ethics