Metabolic Crosstalk Between Host and Parasitic Pathogens

  • Diana Moreira
  • Jérôme Estaquier
  • Anabela Cordeiro-da-Silva
  • Ricardo Silvestre
Part of the Experientia Supplementum book series (EXS, volume 109)


A complex network that embraces parasite–host intrinsic factors and the microenvironment regulated the interaction between a parasite and its host. Nutritional pressures exerted by both elements of this duet thus dictate this host–parasite niche. To survive and proliferate inside a host and a harsh nutritional environment, the parasites modulate different nutrient sensing pathways to subvert host metabolic pathways. Such mechanism is able to change the flux of distinct nutrients/metabolites diverting them to be used by the parasites. Apart from this nutritional strategy, the scavenging of nutrients, particularly host fatty acids, constitutes a critical mechanism to fulfil parasite nutritional requirements, ultimately defining the host metabolic landscape. The host metabolic alterations that result from host–parasite metabolic coupling can certainly be considered important targets to improve diagnosis and also for the development of future therapies. Metabolism is in fact considered a key element within this complex interaction, its modulation being crucial to dictate the final infection outcome.


Nutrient sensing pathways Host–parasite interaction Host metabolic pathways Scavenging of nutrients Host metabolic landscape 


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 IF/00021/2014 to RS and INFECT-ERA (Project INLEISH).


  1. Albuquerque SS, Carret C, Grosso A, Tarun AS, Peng X, Kappe SH, Prudêncio M, Mota MM (2009) Host cell transcriptional profiling during malaria liver stage infection reveals a coordinated and sequential set of biological events. BMC Genomics 10:270PubMedPubMedCentralCrossRefGoogle Scholar
  2. Andrade ZA, Silva HRR (1995) Parasitism of adipocytes by Trypanosoma cruzi. Mem Inst Oswaldo Cruz 90:521–522PubMedCrossRefGoogle Scholar
  3. Anes E, Kühnel MP, Bos E, Moniz-Pereira J, Habermann A, Griffiths G (2003) Selected lipids activate phagosome actin assembly and maturation resulting in killing of pathogenic mycobacteria. Nat Cell Biol 5:793–802PubMedCrossRefGoogle Scholar
  4. Araújo-Santos T, Rodríguez NE, Moura-Pontes S, Dixt UG, Abánades DR, Bozza PT, Wilson ME, Borges VM (2014) Role of prostaglandin F2α production in lipid bodies from Leishmania infantum chagasi: insights on virulence. J Infect Dis 210:1951–1961PubMedCrossRefGoogle Scholar
  5. Bailey AP, Koster G, Guillermier C, Hirst EMA, MacRae JI, Lechene CP, Postle AD, Gould AP (2015) Antioxidant role for lipid droplets in a stem cell niche of Drosophila. Cell 163:340–353PubMedPubMedCentralCrossRefGoogle Scholar
  6. Banerjee S, Ghosh J, Sen S, Guha R, Dhar R, Ghosh M, Datta S, Raychaudhury B, Naskar K, Haldar AK, Lal CS, Pandey K, Das VN, Das P, Roy S (2009) Designing therapies against experimental visceral leishmaniasis by modulating the membrane fluidity of antigen-presenting cells. Infect Immun 77(6):2330–2342. Scholar
  7. Bano N, Romano JD, Jayabalasingham B, Coppens I (2007) Cellular interactions of Plasmodium liver stage with its host mammalian cell. Int J Parasitol 37:1329–1341PubMedCrossRefGoogle Scholar
  8. Bar-Peled L, Sabatini DM (2014) Regulation of mTORC1 by amino acids. Trends Cell Biol 24:400–406PubMedPubMedCentralCrossRefGoogle Scholar
  9. Bar-Peled L, Chantranupong L, Cherniack AD, Chen WW, Ottina KA, Grabiner BC, Spear ED, Carter SL, Meyerson M, Sabatini DM (2013) A tumor suppressor complex with GAP activity for the rag GTPases that signal amino acid sufficiency to mTORC1. Science 340:1100–1106PubMedPubMedCentralCrossRefGoogle Scholar
  10. Beaumelle BD, Vial HJ (1988) Uninfected red cells from malaria-infected blood: alteration of fatty acid composition involving a serum protein: an in vivo and in vitro study. Vitr Cell Dev Biol 24:711–718CrossRefGoogle Scholar
  11. Blader IJ, Manger ID, Boothroyd JC (2001) Microarray analysis reveals previously unknown changes in Toxoplasma gondii-infected human cells. J Biol Chem 276:24223–24231PubMedCrossRefGoogle Scholar
  12. Blume M, Rodriguez-Contreras D, Landfear S, Fleige T, Soldati-Favre D, Lucius R, Gupta N (2009) Host-derived glucose and its transporter in the obligate intracellular pathogen Toxoplasma gondii are dispensable by glutaminolysis. Proc Natl Acad Sci USA 106:12998–13003PubMedPubMedCentralCrossRefGoogle Scholar
  13. Bougnères L, Helft J, Tiwari S, Vargas P, Chang BHJ, Chan L, Campisi L, Lauvau G, Hugues S, Kumar P et al (2009) A role for lipid bodies in the cross-presentation of phagocytosed antigens by MHC Class I in dendritic cells. Immunity 31:232–244PubMedPubMedCentralCrossRefGoogle Scholar
  14. Bozza PT, Yu W, Penrose JF, Morgan ES, Dvorak AM, Weller PF (1997) Eosinophil lipid bodies: specific, inducible intracellular sites for enhanced eicosanoid formation. J Exp Med 186:909–920PubMedPubMedCentralCrossRefGoogle Scholar
  15. Bozza PT, Yu W, Cassara J, Weller PF (1998) Pathways for eosinophil lipid body induction: differing signal transduction in cells from normal and hypereosinophilic subjects. J Leukoc Biol 64:563–569PubMedCrossRefGoogle Scholar
  16. Brasaemle DL, Dolios G, Shapiro L, Wang R (2004) Proteomic analysis of proteins associated with lipid droplets of basal and lipolytically stimulated 3T3-L1 adipocytes. J Biol Chem 279:46835–46842PubMedCrossRefGoogle Scholar
  17. Budanov AV, Karin M (2008) p53 Target genes Sestrin1 and Sestrin2 connect genotoxic stress and mTOR signaling. Cell 134:451–460PubMedPubMedCentralCrossRefGoogle Scholar
  18. Cabalén ME, Cabral MF, Sanmarco LM, Andrada MC, Onofrio LI, Ponce NE, Aoki MP, Gea S, Cano RC (2016) Chronic Trypanosoma cruzi infection potentiates adipose tissue macrophage polarization toward an anti-inflammatory M2 phenotype and contributes to diabetes progression in a diet-induced obesity model. Oncotarget 7:13400–13415PubMedPubMedCentralCrossRefGoogle Scholar
  19. Caffaro CE, Boothroyd JC (2011) Evidence for host cells as the major contributor of lipids in the intravacuolar network of toxoplasma-infected cells. Eukaryot Cell 10:1095–1099PubMedPubMedCentralCrossRefGoogle Scholar
  20. Caljon G, Van Reet N, De Trez C, Vermeersch M, Pérez-Morga D, Van Den Abbeele J (2016) The dermis as a delivery site of Trypanosoma brucei for tsetse flies. PLoS Pathog 12.
  21. Campanale N, Nickel C, Daubenberger CA, Wehlan DA, Gorman JJ, Klonis N, Becker K, Tilley L (2003) Identification and characterization of heme-interacting proteins in the malaria parasite, Plasmodium falciparum. J Biol Chem 278:27354–27361PubMedCrossRefGoogle Scholar
  22. Capewell P, Cren-Travaillé C, Marchesi F, Johnston P, Clucas C, Benson RA, Gorman TA, Calvo-Alvarez E, Crouzols A, Jouvion G et al (2016) The skin is a significant but overlooked anatomical reservoir for vector-borne African trypanosomes. Elife 5.
  23. Caradonna KL, Engel JC, Jacobi D, Lee CH, Burleigh BA (2013) Host metabolism regulates intracellular growth of Trypanosoma cruzi. Cell Host Microbe 13:108–117PubMedPubMedCentralCrossRefGoogle Scholar
  24. Castellano BM, Thelen AM, Moldavski O, Feltes M, van der Welle REN, Mydock-McGrane L, Jiang X, van Eijkeren RJ, Davis OB, Louie SM et al (2017) Lysosomal cholesterol activates mTORC1 via an SLC38A9–Niemann-Pick C1 signaling complex. Science 355:1306–1311PubMedPubMedCentralCrossRefGoogle Scholar
  25. Chakraborty D, Banerjee S, Sen A, Banerjee KK, Das P, Roy S (2005) Leishmania donovani affects antigen presentation of macrophage by disrupting lipid rafts. J Immunol 175(5):3214–3224PubMedCrossRefGoogle Scholar
  26. Chantranupong L, Scaria SM, Saxton RA, Gygi MP, Shen K, Wyant GA, Wang T, Harper JW, Gygi SP, Sabatini DM (2016) The CASTOR proteins are arginine sensors for the mTORC1 pathway. Cell 165:153–164PubMedPubMedCentralCrossRefGoogle Scholar
  27. Charron AJ, Sibley LD (2002) Host cells: mobilizable lipid resources for the intracellular parasite Toxoplasma gondii. J Cell Sci 115:3049–3059PubMedGoogle Scholar
  28. Combs TP, Nagajyothi, Mukherjee S, De Almeida CJG, Jelicks LA, Schubert W, Lin Y, Jayabalan DS, Zhao D, Braunstein VL et al (2005) The adipocyte as an important target cell for Trypanosoma cruzi infection. J Biol Chem 280:24085–24094PubMedCrossRefGoogle Scholar
  29. Coppens I, Joiner KA (2003) Host but not parasite cholesterol controls toxoplasma cell entry by modulating organelle discharge. Mol Biol Cell 14:3804–3820PubMedPubMedCentralCrossRefGoogle Scholar
  30. Coppens I, Sinai AP, Joiner KA (2000) Toxoplasma gondii exploits host low-density lipoprotein receptor-mediated endocytosis for cholesterol acquisition. J Cell Biol 149:167–180PubMedPubMedCentralCrossRefGoogle Scholar
  31. Coppens I, Dunn JD, Romano JD, Pypaert M, Zhang H, Boothroyd JC, Joiner KA (2006) Toxoplasma gondii sequesters lysosomes from mammalian hosts in the vacuolar space. Cell 125:261–274PubMedCrossRefGoogle Scholar
  32. Crawford MJ, Thomsen-Zieger N, Ray M, Schachtner J, Roos DS, Seeber F (2006) Toxoplasma gondii scavenges host-derived lipoic acid despite its de novo synthesis in the apicoplast. EMBO J 25:3214–3222PubMedPubMedCentralCrossRefGoogle Scholar
  33. D’Avila H, Freire-de-Lima CG, Roque NR, Teixeira L, Barja-Fidalgo C, Silva AR, Melo RCN, DosReis GA, Castro-Faria-Neto HC, Bozza PT (2011) Host cell lipid bodies triggered by Trypanosoma cruzi infection and enhanced by the uptake of apoptotic cells are associated with prostaglandin E2 generation and increased parasite growth. J Infect Dis 204:951–961PubMedCrossRefGoogle Scholar
  34. D’Avila H, Toledo DAM, Melo RCN (2012) Lipid bodies: inflammatory organelles implicated in host- Trypanosoma cruzi interplay during innate immune responses. Mediat Inflamm 2012:1–11CrossRefGoogle Scholar
  35. Da Cunha DF, Da Cunha SFDC, Nunes AG, Silva-Vergara ML (2009) Is an increased body mass index associated with a risk of cutaneous leishmaniasis? Rev Soc Bras Med Trop 42:494–495PubMedCrossRefGoogle Scholar
  36. De Cicco NNT, Pereira MG, Corrêa JR, Andrade-Neto VV, Saraiva FB, Chagas-Lima AC, Gondim KC, Torres-Santos EC, Folly E, Saraiva EM et al (2012) LDL uptake by leishmania amazonensis: involvement of membrane lipid microdomains. Exp Parasitol 130:330–340PubMedCrossRefGoogle Scholar
  37. Debierre-Grockiego F, Schwarz RT (2010) Immunological reactions in response to apicomplexan glycosylphosphatidylinositols. Glycobiology 20:801–811PubMedCrossRefGoogle Scholar
  38. den Brok MH, Büll C, Wassink M, de Graaf AM, Wagenaars JA, Minderman M, Thakur M, Amigorena S, Rijke EO, Schrier CC et al (2016) Saponin-based adjuvants induce cross-presentation in dendritic cells by intracellular lipid body formation. Nat Commun 7:13324CrossRefGoogle Scholar
  39. Dinesh N, Pallerla DSR, Kaur PK, Kishore Babu N, Singh S (2014) Exploring Leishmania donovani 3-hydroxy-3-methylglutaryl coenzyme A reductase (HMGR) as a potential drug target by biochemical, biophysical and inhibition studies. Microb Pathog 66:14–23PubMedCrossRefGoogle Scholar
  40. Dobson DE, Kamhawi S, Lawyer P, Turco SJ, Beverley SM, Sacks DL (2010) Leishmania major survival in selective Phlebotomus papatasi sand fly vector requires a specific SCG-encoded lipophosphoglycan galactosylation pattern. PLoS Pathog 6:e1001185. Scholar
  41. Dumont ME, Dei-Cas E, Maurois P, Slomianny C, Prensier G, Houcke-Lecomte M, Vernes A, Camus D (1988) Histopathology of the liver and kidney during malaria: relation to malaria-induced dyslipoproteinemia. Ann Parasitol Hum Comp 63:171–183PubMedCrossRefGoogle Scholar
  42. Düvel K, Yecies JL, Menon S, Raman P, Lipovsky AI, Souza AL, Triantafellow E, Ma Q, Gorski R, Cleaver S et al (2010) Activation of a metabolic gene regulatory network downstream of mTOR complex 1. Mol Cell 39:171–183PubMedPubMedCentralCrossRefGoogle Scholar
  43. Dvorak AM, Weller PF, Harvey VS, Morgan ES, Dvorak HF (1993) Ultrastructural localization of prostaglandin endoperoxide synthase (Cyclooxygenase) to isolated, purified fractions of guinea pig peritoneal macrophage and line 10 hepatocarcinoma cell lipid bodies. Int Arch Allergy Immunol 101:136–142PubMedCrossRefGoogle Scholar
  44. Efeyan ACWCSDM (2015) Nutrient-sensing mechanisms and pathways. Nature 517:302–310PubMedPubMedCentralCrossRefGoogle Scholar
  45. Egan DF, Shackelford DB, Mihaylova MM, Gelino S, Kohnz RA, Mair W, Vasquez DS, Joshi A, Gwinn DM, Taylor R et al (2011) Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy. Science 331:456–461PubMedCrossRefGoogle Scholar
  46. Ferreira AVM, Segatto M, Menezes Z, Macedo AM, Gelape C, de Oliveira Andrade L, Nagajyothi F, Scherer PE, Teixeira MM, Tanowitz HB (2011) Evidence for Trypanosoma cruzi in adipose tissue in human chronic chagas disease. Microbes Infect 13:1002–1005PubMedPubMedCentralCrossRefGoogle Scholar
  47. Foretz M, Viollet B (2011) Regulation of hepatic metabolism by AMPK. J Hepatol 54:827–829PubMedCrossRefGoogle Scholar
  48. Francisco AF, Lewis MD, Jayawardhana S, Taylor MC, Chatelain E, Kelly JM (2015) Limited ability of posaconazole to cure both acute and chronic Trypanosoma cruzi infections revealed by highly sensitive in vivo imaging. Antimicrob Agents Chemother 59:4653–4661PubMedPubMedCentralCrossRefGoogle Scholar
  49. Frank B, Marcu A, de Oliveira Almeida Petersen AL, Weber H, Stigloher C, Mottram JC, Scholz CJ, Schurigt U (2015) Autophagic digestion of Leishmania major by host macrophages is associated with differential expression of BNIP3, CTSE, and the miRNAs miR-101c, miR-129, and miR-210. Parasit Vectors 8:404PubMedPubMedCentralCrossRefGoogle Scholar
  50. Franke-Fayard B, Janse CJ, Cunha-Rodrigues M, Ramesar J, Büscher P, Que I, Löwik C, Voshol PJ, den Boer MA, van Duinen SG et al (2005) Murine malaria parasite sequestration: CD36 is the major receptor, but cerebral pathology is unlinked to sequestration. Proc Natl Acad Sci USA 102:11468–11473PubMedPubMedCentralCrossRefGoogle Scholar
  51. Freire-de-Lima CG, Nascimento DO, Soares MB, Bozza PT, Castro-Faria-Neto HC, de Mello FG, DosReis G a, Lopes MF (2000) Uptake of apoptotic cells drives the growth of a pathogenic trypanosome in macrophages. Nature 403:199–203PubMedCrossRefGoogle Scholar
  52. Freire-de-lima G, Roque NR, Teixeira L, Barja-fidalgo C, Avila HD, Silva AR, Melo RCN, Dosreis GA, Castro-faria-neto HC (2011) Host cell lipid bodies triggered by Trypanosoma cruzi infection and enhanced by the uptake of apoptotic cells are associated with Prostaglandin E 2 generation and increased parasite growth. J Infect Dis 204:951–961PubMedCrossRefGoogle Scholar
  53. Ganley IG, Lam DH, Wang J, Ding X, Chen S, Jiang X (2009) ULK1·ATG13·FIP200 complex mediates mTOR signaling and is essential for autophagy. J Biol Chem 284:12297–12305PubMedPubMedCentralCrossRefGoogle Scholar
  54. Gao Q, Goodman JM (2015) The lipid droplet—a well-connected organelle. Front Cell Dev Biol 3:1–12CrossRefGoogle Scholar
  55. Ghosh J, Lal CS, Pandey K, Das VN, Das P, Roychoudhury K, Roy S (2011) Human visceral leishmaniasis: decrease in serum cholesterol as a function of splenic parasite load. Ann Trop Med Parasitol 105(3):267–271. Scholar
  56. Ghosh J, Bose M, Roy S, Bhattacharyya SN (2013) Leishmania donovani targets dicer1 to downregulate miR-122, lower serum cholesterol, and facilitate murine liver infection. Cell Host Microbe 13:277–288PubMedPubMedCentralCrossRefGoogle Scholar
  57. Ginger ML (2006) Niche metabolism in parasitic protozoa. Philos Trans R Soc B Biol Sci 361:101–118CrossRefGoogle Scholar
  58. Gomes AF, Magalhães KG, Rodrigues RM, de Carvalho L, Molinaro R, Bozza PT, Barbosa HS (2014) Toxoplasma gondii-skeletal muscle cells interaction increases lipid droplet biogenesis and positively modulates the production of IL-12, IFN-g and PGE2. Parasit Vectors 7:47PubMedPubMedCentralCrossRefGoogle Scholar
  59. Gordon EB, Hart GT, Tran TM, Waisberg M, Akkaya M, Skinner J, Zinöcker S, Pena M, Yazew T, Qi C et al (2015) Inhibiting the mammalian target of rapamycin blocks the development of experimental cerebral malaria. mBio 6:1–17CrossRefGoogle Scholar
  60. Gwinn DM, Shackelford DB, Egan DF, Mihaylova MM, Mery A, Vasquez DS, Turk BE, Shaw RJ (2008) AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol Cell 30:214–226PubMedPubMedCentralCrossRefGoogle Scholar
  61. Hanson KK, Ressurreicao AS, Buchholz K, Prudencio M, Herman-Ornelas JD, Rebelo M, Beatty WL, Wirth DF, Hanscheid T, Moreira R et al (2013) Torins are potent antimalarials that block replenishment of Plasmodium liver stage parasitophorous vacuole membrane proteins. Proc Natl Acad Sci 110:E2838–E2847PubMedPubMedCentralCrossRefGoogle Scholar
  62. Hara K, Maruki Y, Long X, Yoshino K, Oshiro N, Hidayat S, Tokunaga C, Avruch J, Yonezawa K (2002) Raptor, a binding partner of target of rapamycin (TOR), mediates TOR action. Cell 110:177–189PubMedCrossRefGoogle Scholar
  63. Hardie DG (2011) AMP-activated protein kinase-an energy sensor that regulates all aspects of cell function. Genes Dev 25:1895–1908PubMedPubMedCentralCrossRefGoogle Scholar
  64. Hardie DG, Ross FA, Hawley SA (2012) AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nat Rev Mol Cell Biol 13:251–262PubMedPubMedCentralCrossRefGoogle Scholar
  65. Hosokawa N, Hara T, Kaizuka T, Kishi C, Takamura A, Miura Y, Iemura S, Natsume T, Takehana K, Yamada N et al (2009) Nutrient-dependent mTORC1 association with the ULK1 – Atg13 – FIP200 complex required for autophagy. Mol Biol Cell 20:1981–1991PubMedPubMedCentralCrossRefGoogle Scholar
  66. Hu X, Binns D, Reese ML (2017) The coccidian parasites Toxoplasma and Neospora dysregulate mammalian lipid droplet biogenesis. J Biol Chem 292:11009–11020PubMedCrossRefGoogle Scholar
  67. Inoki K, Li Y, Zhu T, Wu J, Guan K-L (2002) TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signalling. Nat Cell Biol 4:648–657PubMedCrossRefGoogle Scholar
  68. Itani S, Torii M, Ishino T (2014) D-Glucose concentration is the key factor facilitating liver stage maturation of Plasmodium. Parasitol Int 63:584–590PubMedCrossRefGoogle Scholar
  69. Itoe MA, Sampaio JL, Cabal GG, Real E, Zuzarte-Luis V, March S, Bhatia SN, Frischknecht F, Thiele C, Shevchenko A et al (2014) Host cell phosphatidylcholine is a key mediator of malaria parasite survival during liver stage infection. Cell Host Microbe 16:778–786PubMedPubMedCentralCrossRefGoogle Scholar
  70. Jacinto E, Loewith R, Schmidt A, Lin S, Rüegg MA, Hall A, Hall MN (2004) Mammalian TOR complex 2 controls the actin cytoskeleton and is rapamycin insensitive. Nat Cell Biol 6:1122–1128PubMedCrossRefGoogle Scholar
  71. Jackson KE, Klonis N, Ferguson DJP, Adisa A, Dogovski C, Tilley L (2004) Food vacuole-associated lipid bodies and heterogeneous lipid environments in the malaria parasite, Plasmodium falciparum. Mol Microbiol 54:109–122PubMedCrossRefGoogle Scholar
  72. Jäger SS, Handschin CC, St-Pierre JJ, Spiegelman BMBM (2007) AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1alpha. PNAS 104:12017–12022PubMedPubMedCentralCrossRefGoogle Scholar
  73. Jaramillo M, Gomez MA, Larsson O, Shio MT, Topisirovic I, Contreras I, Luxenburg R, Rosenfeld A, Colina R, McMaster RW et al (2011) Leishmania repression of host translation through mTOR cleavage is required for parasite survival and infection. Cell Host Microbe 9:331–341PubMedCrossRefGoogle Scholar
  74. Jayabalasingham B, Bano N, Coppens I (2010) Metamorphosis of the malaria parasite in the liver is associated with organelle clearance. Cell Res 20:1043–1059PubMedPubMedCentralCrossRefGoogle Scholar
  75. Johndrow C, Nelson R, Tanowitz H, Weiss LM, Nagajyothi F (2014) Trypanosoma cruzi infection results in an increase in intracellular cholesterol. Microbes Infect 16:337–344PubMedPubMedCentralCrossRefGoogle Scholar
  76. Kaizuka T, Hara T, Oshiro N, Kikkawa U, Yonezawa K, Takehana K, Iemura SI, Natsume T, Mizushima N (2010) Tti1 and Tel2 are critical factors in mammalian target of rapamycin complex assembly. J Biol Chem 285:20109–20116PubMedPubMedCentralCrossRefGoogle Scholar
  77. Kalender A, Selvaraj A, Kim SY, Gulati P, Brûlé S, Viollet B, Kemp BE, Bardeesy N, Dennis P, Schlager JJ et al (2010) Metformin, independent of AMPK, inhibits mTORC1 in a rag GTPase-dependent manner. Cell Metab 11:390–401PubMedPubMedCentralCrossRefGoogle Scholar
  78. Kaushansky A, Ye AS, Austin LS, Mikolajczak SA, Vaughan AM, Camargo N, Metzger PG, Douglass AN, MacBeath G, Kappe SHI (2013) Suppression of host p53 is critical for plasmodium liver-stage infection. Cell Rep 3:630–637PubMedPubMedCentralCrossRefGoogle Scholar
  79. Kim D, Sarbassov DD, Ali SM, Latek RR, Guntur KVP, Erdjument-bromage H, Tempst P, Sabatini DM (2003) GbetaL, a positive regulator of the rapamycin- sensitive pathway required for the nutrient- sensitive interaction between raptor and mTOR. Mol Cell 11:895–904PubMedCrossRefGoogle Scholar
  80. Kim J, Kundu M, Viollet B, Guan K-L (2011) AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol 13:132–141PubMedPubMedCentralCrossRefGoogle Scholar
  81. Kirk K, Horner HA, Kirk J (1996) Glucose uptake in Plasmodium falciparum-infected erythrocytes is an equilibrative not an active process. Mol Biochem Parasitol 82:195–205PubMedCrossRefGoogle Scholar
  82. Kumar GA, Roy S, Jafurulla M, Mandal C, Chattopadhyay A (2016) Statin-induced chronic cholesterol depletion inhibits Leishmania donovani infection: relevance of optimum host membrane cholesterol. Biochim Biophys Acta—Biomembr 1858:2088–2096CrossRefGoogle Scholar
  83. Labaied M, Jayabalasingham B, Bano N, Cha SJ, Sandoval J, Guan G, Coppens I (2011) Plasmodium salvages cholesterol internalized by LDL and synthesized de novo in the liver. Cell Microbiol 13:569–586PubMedCrossRefGoogle Scholar
  84. Lal CS, Verma N, Rabidas VN, Ranjan A, Pandey K, Verma RB, Singh D, Kumar S, Das P (2010) Total serum cholesterol determination can provide understanding of parasite burden in patients with visceral leishmaniasis infection. Clin Chim Acta 411(23–24):2112–2113. Scholar
  85. Laplante M, Sabatini DM (2009) An emerging role of mTOR in lipid biosynthesis. Curr Biol 19:R1046–R1052PubMedPubMedCentralCrossRefGoogle Scholar
  86. Laplante M, Sabatini DM (2012) MTOR signaling in growth control and disease. Cell 149:274–293PubMedPubMedCentralCrossRefGoogle Scholar
  87. Lecoeur H, Giraud E, Prévost M-C, Milon G, Lang T (2013) Reprogramming neutral lipid metabolism in mouse dendritic leucocytes hosting live leishmania amazonensis amastigotes. PLoS Negl Trop Dis 7:e2276PubMedPubMedCentralCrossRefGoogle Scholar
  88. Lingelbach K, Joiner K (1998) The parasitophorous vacuole membrane surrounding Plasmodium and Toxoplasma: an unusual compartment in infected cells. J Cell Sci 111(Pt 1):1467–1475PubMedGoogle Scholar
  89. Long AP, Manneschmidt AK, Verbrugge B, Dortch MR, Minkin SC, Prater KE, Biggerstaff JP, Dunlap JR, Dalhaimer P (2012) Lipid droplet de novo formation and fission are linked to the cell cycle in fission yeast. Traffic 13:705–714PubMedCrossRefGoogle Scholar
  90. Loria P, Miller S, Foley M, Tilley L (1999) Inhibition of the peroxidative degradation of haem as the basis of action of chloroquine and other quinoline antimalarials. Biochem J 339:363PubMedPubMedCentralCrossRefGoogle Scholar
  91. MacRae JI, Sheiner L, Nahid A, Tonkin C, Striepen B, McConville MJ (2012) Mitochondrial metabolism of glucose and glutamine is required for intracellular growth of Toxoplasma gondii. Cell Host Microbe 12:682–692PubMedPubMedCentralCrossRefGoogle Scholar
  92. Martins RM, Alves RM, Macedo S, Yoshida N (2011) Starvation and rapamycin differentially regulate host cell lysosome exocytosis and invasion by Trypanosoma cruzi metacyclic forms. Cell Microbiol 13:943–954PubMedCrossRefGoogle Scholar
  93. Meireles P, Sales-dias J, Andrade CM, Mello-vieira J, Mancio-silva L, Simas JP, Staines HM, Prudêncio M (2017) GLUT1-mediated glucose uptake plays a crucial role during plasmodium hepatic infection. Cell Biol 19.
  94. Mejia P, Treviño-Villarreal JH, Hine C, Harputlugil E, Lang S, Calay E, Rogers R, Wirth D, Duraisingh MT, Mitchell JR (2015) Dietary restriction protects against experimental cerebral malaria via leptin modulation and T-cell mTORC1 suppression. Nat Commun 6:6050PubMedPubMedCentralCrossRefGoogle Scholar
  95. Melo RC (1999) Depletion of immune effector cells induces myocardial damage in the acute experimental Trypanosoma cruzi infection: ultrastructural study in rats. Tissue Cell 31:281–290PubMedCrossRefGoogle Scholar
  96. Melo RCN, Dvorak AM (2012) Lipid body–phagosome interaction in macrophages during infectious diseases: host defense or pathogen survival strategy? PLoS Pathog 8:e1002729PubMedPubMedCentralCrossRefGoogle Scholar
  97. Melo RCN, Ávila HD, Fabrino DL, Almeida PE, Bozza PT (2003) Macrophage lipid body induction by Chagas disease in vivo: putative intracellular domains for eicosanoid formation during infection. Tissue Cell 35:59–67PubMedCrossRefGoogle Scholar
  98. Miao Q, Ndao M (2014) Trypanosoma cruzi infection and host lipid metabolism. Mediators Inflamm 2014:902038. Scholar
  99. Mikolajczak SA, Jacobs-Lorena V, MacKellar DC, Camargo N, Kappe SHI (2007) L-FABP is a critical host factor for successful malaria liver stage development. Int J Parasitol 37:483–489PubMedCrossRefGoogle Scholar
  100. Miller LH (1969) Distribution of mature trophozoites and schizonts of Plasmodium falciparum in the organs of Aotus trivirgatus, the night monkey. Am J Trop Med Hyg 18:860–865PubMedCrossRefGoogle Scholar
  101. Ming M, Ewen ME, Pereira ME (1995) Trypanosome invasion of mammalian cells requires activation of the TGF beta signaling pathway. Cell 82:287–296PubMedCrossRefGoogle Scholar
  102. Moreira D, Silvestre R, Cordeiro da Silva A, Estaquier J, Foretz M, Viollet B (2015a) AMP-activated protein kinase as a target for pathogens: friends or foes? Curr Drug Targets 17:163–166Google Scholar
  103. Moreira D, Rodrigues V, Abengozar M, Rivas L, Rial E, Laforge M, Li X, Foretz M, Viollet B, Estaquier J et al (2015b) Leishmania infantum Modulates Host Macrophage Mitochondrial Metabolism by Hijacking the SIRT1-AMPK Axis. PLoS Pathog. 11:1–24CrossRefGoogle Scholar
  104. Mota LAM, Roberto Neto J, Monteiro VG, Lobato CSS, de Oliveira MA, da Cunha M, D’Ávila H, Seabra SH, Bozza PT, DaMatta RA (2014) Culture of mouse peritoneal macrophages with mouse serum induces lipid bodies that associate with the parasitophorous vacuole and decrease their microbicidal capacity against Toxoplasma gondii. Mem Inst Oswaldo Cruz 109:767–774PubMedPubMedCentralCrossRefGoogle Scholar
  105. Mueller A-K, Camargo N, Kaiser K, Andorfer C, Frevert U, Matuschewski K, Kappe SHI (2005) Plasmodium liver stage developmental arrest by depletion of a protein at the parasite-host interface. Proc Natl Acad Sci USA 102:3022–3027PubMedPubMedCentralCrossRefGoogle Scholar
  106. Mukherjee M, Basu Ball W, Das PK (2014) Leishmania donovani activates SREBP2 to modulate macrophage membrane cholesterol and mitochondrial oxidants for establishment of infection. Int J Biochem Cell Biol 55:196–208PubMedCrossRefGoogle Scholar
  107. Murphy DJ (2001) The biogenesis and functions of lipid bodies in animals, plants and microorganisms. Prog Lipid Res 40:325–438PubMedCrossRefGoogle Scholar
  108. Naderer T, McConville MJ (2011) Intracellular growth and pathogenesis of Leishmania parasites. Essays Biochem 51:81–95PubMedCrossRefGoogle Scholar
  109. Nagajyothi F, Desruisseaux MS, Thiruvur N, Weiss LM, Braunstein VL, Albanese C, Teixeira MM, de Almeida CJ, Lisanti MP, Scherer PE et al (2008) Trypanosoma cruzi infection of cultured adipocytes results in an inflammatory phenotype. Obesity (Silver Spring) 16:1992–1997CrossRefGoogle Scholar
  110. Nagajyothi F, Weiss LM, Silver DL, Desruisseaux MS, Scherer PE, Herz J, Tanowitz HB (2011) Trypanosoma cruzi utilizes the host low density lipoprotein receptor in invasion. PLoS Negl Trop Dis 5:e953PubMedPubMedCentralCrossRefGoogle Scholar
  111. Nagajyothi F, Weiss LM, Zhao D, Koba W, Jelicks LA, Cui M, Factor SM, Scherer PE, Tanowitz HB (2014) High fat diet modulates Trypanosoma cruzi infection associated myocarditis. PLoS Negl Trop Dis 8:e3118PubMedPubMedCentralCrossRefGoogle Scholar
  112. Ndao M, Spithill TW, Caffrey R, Li H, Podust VN, Perichon R, Santamaria C, Ache A, Duncan M, Powell MR et al (2010) Identification of novel diagnostic serum biomarkers for chagas’ disease in asymptomatic subjects by mass spectrometric profiling. J Clin Microbiol 48:1139–1149PubMedPubMedCentralCrossRefGoogle Scholar
  113. Nebl T, De Veer MJ, Schofield L (2005) Stimulation of innate immune responses by malarial glycosylphosphatidylinositol via pattern recognition receptors. Parasitology 130(Suppl):S45–S62PubMedCrossRefGoogle Scholar
  114. Nievelstein-Post P, Mottino G, Fogelman A, Frank J (1994) An ultrastructural study of lipoprotein accumulation in cardiac valves of the rabbit. Arterioscler Thromb 14:1151–1161PubMedCrossRefGoogle Scholar
  115. Nolan SJ, Romano JD, Coppens I (2017) Host lipid droplets: an important source of lipids salvaged by the intracellular parasite Toxoplasma gondii. PLOS Pathog 13:e1006362PubMedPubMedCentralCrossRefGoogle Scholar
  116. Omsland A, Hackstadt T, Heinzen RA (2013) Bringing culture to the uncultured: Coxiella burnetii and lessons for obligate intracellular bacterial pathogens. PLoS Pathog 9:e1003540PubMedPubMedCentralCrossRefGoogle Scholar
  117. Orlofsky A (2009) Toxoplasma-induced autophagy: a window into nutritional futile cycles in mammalian cells? Autophagy 5:404–406PubMedPubMedCentralCrossRefGoogle Scholar
  118. Palacpac NMQ, Hiramine Y, Mi-ichi F, Torii M, Kita K, Hiramatsu R, Horii T, Mitamura T (2004) Developmental-stage-specific triacylglycerol biosynthesis, degradation and trafficking as lipid bodies in Plasmodium falciparum-infected erythrocytes. J Cell Sci 117:1469–1480PubMedCrossRefGoogle Scholar
  119. Pereira MG, Nakayasu ES, Sant’Anna C, de Cicco NNT, Atella GC, de Souza W, Almeida IC, Cunha-e-Silva N (2011) Trypanosoma cruzi epimastigotes are able to store and mobilize high amounts of cholesterol in reservosome lipid inclusions. PLoS One 6.
  120. Peterson TR, Laplante M, Thoreen CC, Sancak Y, Kang SA, Kuehl WM, Gray NS, Sabatini DM (2009) DEPTOR is an mTOR inhibitor frequently overexpressed in multiple myeloma cells and required for their survival. Cell 137:873–886PubMedPubMedCentralCrossRefGoogle Scholar
  121. Peterson TR, Sengupta SS, Harris TE, Carmack AE, Kang SA, Balderas E, Guertin DA, Madden KL, Carpenter AE, Finck BN et al (2011) MTOR complex 1 regulates lipin 1 localization to control the srebp pathway. Cell 146:408–420PubMedPubMedCentralCrossRefGoogle Scholar
  122. Pfaller MA, Krogstad DJ, Parquette AR, Nguyen-Dinh P (1982) Plasmodium falciparum: stage-specific lactate production in synchronized cultures. Exp Parasitol 54:391–396PubMedCrossRefGoogle Scholar
  123. Pinheiro RO, Nunes MP, Pinheiro CS, D’Avila H, Bozza PT, Takiya CM, Côrte-Real S, Freire-de-Lima CG, DosReis GA (2009) Induction of autophagy correlates with increased parasite load of Leishmania amazonensis in BALB/c but not C57BL/6 macrophages. Microbes Infect 11:181–190PubMedCrossRefGoogle Scholar
  124. Pol A, Gross SP, Parton RG (2014) Biogenesis of the multifunctional lipid droplet: lipids, proteins, and sites. J Cell Biol 204:635–646PubMedPubMedCentralCrossRefGoogle Scholar
  125. Portugal LR, Fernandes LR, Pietra Pedroso VS, Santiago HC, Gazzinelli RT, Alvarez-Leite JI (2008) Influence of low-density lipoprotein (LDL) receptor on lipid composition, inflammation and parasitism during Toxoplasma gondii infection. Microbes Infect 10:276–284PubMedCrossRefGoogle Scholar
  126. Potter CJ, Pedraza LG, Xu T (2002) Akt regulates growth by directly phosphorylating Tsc2. Nat Cell Biol 4:658–665PubMedCrossRefGoogle Scholar
  127. Prioli P, Rosenberg I (1990) High- and low-density lipoproteins enhance infection of Trypanosoma cruzi in vitro. Mol Biochem Parasitol 38:191–198PubMedCrossRefGoogle Scholar
  128. Pulido-Mendez M, Finol HJ, Giron ME, Aguilar I (2006) Ultrastructural pathological changes in mice kidney caused by Plasmodium berghei infection. J Submicrosc Cytol Pathol 38:143–148PubMedGoogle Scholar
  129. Rabhi I, Rabhi S, Ben-Othman R, Rasche A, Consortium S, Daskalaki A, Trentin B, Piquemal D, Regnault B, Descoteaux A et al (2012) Transcriptomic signature of leishmania infected mice macrophages: a metabolic point of view. PLoS Negl Trop Dis 6:e1763PubMedPubMedCentralCrossRefGoogle Scholar
  130. Rabhi S, Rabhi I, Trentin B, Piquemal D, Regnault B, Goyard S, Lang T, Descoteaux A, Enninga J, Guizani-Tabbane L (2016) Lipid droplet formation, their localization and dynamics during leishmania major macrophage infection. PLoS One 11:1–19CrossRefGoogle Scholar
  131. Ramakrishnan S, Serricchio M, Striepen B, Bütikofer P (2013) Lipid synthesis in protozoan parasites: a comparison between kinetoplastids and apicomplexans. Prog Lipid Res 52:488–512PubMedCrossRefGoogle Scholar
  132. Reeves GM, Mazaheri S, Snitker S, Langenberg P, Giegling I, Hartmann AM, Konte B, Friedl M, Okusaga O, Groer MW et al (2013) A positive association between T. gondii seropositivity and obesity. Front Public Heal 1:73CrossRefGoogle Scholar
  133. Robert V, Bourgouin C, Depoix D, Thouvenot C, Lombard M-N, Grellier P (2008) Malaria and obesity: obese mice are resistant to cerebral malaria. Malar J 7:81PubMedPubMedCentralCrossRefGoogle Scholar
  134. Rodrigues CD, Hannus M, Prudêncio M, Martin C, Gonçalves LA, Portugal S, Epiphanio S, Akinc A, Hadwiger P, Jahn-Hofmann K et al (2008) Host scavenger receptor SR-BI plays a dual role in the establishment of malaria parasite liver infection. Cell Host Microbe 4:271–282PubMedCrossRefGoogle Scholar
  135. Rodriguez A, Samoff E, Rioult MG, Chung A (1996) Host cell invasion by trypanosomes requires lysosomes and microtubule/kinesin-mediated transport. J Cell Biol 134:349–362PubMedCrossRefGoogle Scholar
  136. Rodriguez-Acosta A, Finol HJ, Pulido-Mendez M, Marquez A, Andrade G, Gonzalez N, Aguilar I, Giron ME, Pinto A (1998) Liver ultrastructural pathology in mice infected with Plasmodium berghei. J Submicrosc Cytol Pathol 30:299–307PubMedGoogle Scholar
  137. Romano JD, Coppens I (2013) Host Organelle Hijackers: a similar modus operandi for Toxoplasma gondii and Chlamydia trachomatis: co-infection model as a tool to investigate pathogenesis. Pathog Dis 69:72–86PubMedCrossRefGoogle Scholar
  138. Romano PS, Arboit MA, Vázquez CL, Colombo MI (2009) The autophagic pathway is a key component in the lysosomal dependent entry of Trypanosoma cruzi into the host cell. Autophagy 5:6–18PubMedCrossRefGoogle Scholar
  139. Rosenthal PJ, Meshnick SR (1996) Hemoglobin catabolism and iron utilization by malaria parasites. Mol Biochem Parasitol 83:131–139PubMedCrossRefGoogle Scholar
  140. Roux PP, Ballif BA, Anjum R, Gygi SP, Blenis J (2004) Tumor-promoting phorbol esters and activated Ras inactivate the tuberous sclerosis tumor suppressor complex via p90 ribosomal S6 kinase. Proc Natl Acad Sci USA 101:13489–13494PubMedPubMedCentralCrossRefGoogle Scholar
  141. Rubin-de-celis SSC, Uemura H, Yoshida N, Schenkman S (2006) Expression of trypomastigote trans -sialidase in metacyclic forms of Trypanosoma cruzi increases parasite escape from its parasitophorous vacuole. Cell Microbiol 8:1888–1898PubMedCrossRefGoogle Scholar
  142. Ruivo MTG, Vera IM, Sales-Dias J, Meireles P, Gural N, Bhatia SN, Mota MM, Mancio-Silva L (2016) Host AMPK is a modulator of plasmodium liver infection. Cell Rep 16:2539–2545PubMedPubMedCentralCrossRefGoogle Scholar
  143. Sacks DL (2001) Leishmania-sand fly interactions controlling species-specific vector competence. Cell Microbiol 3:189–196PubMedCrossRefGoogle Scholar
  144. Sancak Y, Bar-Peled L, Zoncu R, Markhard AL, Nada S, Sabatini DM (2010) Ragulator-rag complex targets mTORC1 to the lysosomal surface and is necessary for its activation by amino acids. Cell 141:290–303PubMedPubMedCentralCrossRefGoogle Scholar
  145. Sarbassov DD, Ali SM, Kim D-H, Guertin DA, Latek RR, Erdjument-Bromage H, Tempst P, Sabatini DM (2004) Rictor, a novel binding partner of mTOR, defines a rapamycin-insensitive and raptor-independent pathway that regulates the cytoskeleton. Curr Biol 14:1296–1302PubMedCrossRefGoogle Scholar
  146. Sarnáglia G, Covre L, Pereira F, DE Matos Guedes H, Faria A, Dietza R, Rodrigues R, Maioli T, Gomes D (2016) Diet-induced obesity promotes systemic inflammation and increased susceptibility to murine visceral leishmaniasis. Parasitology 143:1647–1655PubMedCrossRefGoogle Scholar
  147. Saunders EC, Ng WW, Kloehn J, Chambers JM, Ng M, McConville MJ (2014) Induction of a stringent metabolic response in intracellular stages of Leishmania mexicana leads to increased dependence on mitochondrial metabolism. PLoS Pathog 10:e1003888PubMedPubMedCentralCrossRefGoogle Scholar
  148. Schofield L, Hewitt MC, Evans K, Siomos M-A, Seeberger PH (2002) Synthetic GPI as a candidate anti-toxic vaccine in a model of malaria. Nature 418:785–789PubMedCrossRefGoogle Scholar
  149. Schwab JC, Beckers CJ, Joiner KA (1994) The parasitophorous vacuole membrane surrounding intracellular Toxoplasma gondii functions as a molecular sieve. Proc Natl Acad Sci USA 91:509–513PubMedPubMedCentralCrossRefGoogle Scholar
  150. Semini G, Paape D, Paterou A, Schroeder J, Barrios-Llerena M, Aebischer T (2017) Changes to cholesterol trafficking in macrophages by Leishmania parasites infection. Microbiologyopen 6:1–13CrossRefGoogle Scholar
  151. Shang L, Chen S, Du F, Li S, Zhao L, Wang X (2011) Nutrient starvation elicits an acute autophagic response mediated by Ulk1 dephosphorylation and its subsequent dissociation from AMPK. Proc Natl Acad Sci 108:4788–4793PubMedPubMedCentralCrossRefGoogle Scholar
  152. Shoemaker JP, Hoffman RV, Huffman DG (1970) Trypanosoma cruzi: preference for brown adipose tissue in mice by the Tulahuen strain. Exp Parasitol 27:403–407PubMedCrossRefGoogle Scholar
  153. Sibley LD, Niesman IR, Parmley SF (1995) Regulated secretion of multi-lamellar vesicles leads to formation of a tubulo- vesicular network in host-cell vacuoles occupied by Toxoplasma gondii. J Cell Sci 1677:1669–1677Google Scholar
  154. Silva JS, Twardzik DR, Reed SG (1991) Regulation of Trypanosoma cruzi infections in vitro and in vivo by transforming growth factor beta (TGF-beta). J Exp Med 174:539–545PubMedCrossRefGoogle Scholar
  155. Simões AP, Roelofsen B, Op den Kamp J (1992) Incorporation of free fatty acids can explain alterations in the molecular species composition of phosphatidylcholine and phosphatidyethanolamine in human erythrocytes as induced by Plasmodium falciparum. Cell Biol Int Rep 16:533–545PubMedCrossRefGoogle Scholar
  156. Sinai AP, Webster P, Joiner KA (1997) Association of host cell endoplasmic reticulum and mitochondria with the Toxoplasma gondii parasitophorous vacuole membrane: a high affinity interaction. J Cell Sci 2128:2117–2128Google Scholar
  157. Slavic K, Delves MJ, Prudêncio M, Talman AM, Straschil U, Derbyshire ET, Xu Z, Sinden RE, Mota MM, Morin C et al (2011) Use of a selective inhibitor to define the chemotherapeutic potential of the plasmodial hexose transporter in different stages of the parasite’s life cycle. Antimicrob Agents Chemother 55:2824–2830PubMedPubMedCentralCrossRefGoogle Scholar
  158. Soares MJ, De Souza W (1988) Cytoplasmic organelles of trypanosomatids: a cytochemical and stereological study. J Submicrosc Cytol Pathol 20:349–361PubMedGoogle Scholar
  159. Soares MJ, Souto-Padrón T, Bonaldo MC, Goldenberg S, de Souza W (1989) A stereological study of the differentiation process in Trypanosoma cruzi. Parasitol Res 75:522–527PubMedCrossRefGoogle Scholar
  160. Spalding KL, Arner E, Westermark PO, Bernard S, Buchholz BA, Bergmann O, Blomqvist L, Hoffstedt J, Näslund E, Britton T et al (2008) Dynamics of fat cell turnover in humans. Obstet Gynecol Surv 63:577–578CrossRefGoogle Scholar
  161. Stambolic V, MacPherson D, Sas D, Lin Y, Snow B, Jang Y, Benchimol S, Mak TW (2001) Regulation of PTEN transcription by p53. Mol Cell 8:317–325PubMedCrossRefGoogle Scholar
  162. Steinberg GR, Kemp BE (2009) AMPK in health and disease. Physiol Rev 89(3):1025–1078. Scholar
  163. Suh C-I, Stull ND, Li XJ, Tian W, Price MO, Grinstein S, Yaffe MB, Atkinson S, Dinauer MC (2006) The phosphoinositide-binding protein p40phox activates the NADPH oxidase during FcgammaIIA receptor-induced phagocytosis. J Exp Med 203:1915–1925PubMedPubMedCentralCrossRefGoogle Scholar
  164. Sunnemark D, Harris RA, Frostega J, Anders O (2000) Induction of early atherosclerosis in CBA/J mice by combination of Trypanosoma cruzi infection and a high cholesterol diet. Atherosclerosis 153:273–282PubMedCrossRefGoogle Scholar
  165. Tanowitz HB, Amole B, Hewlett D, Wittner M (1988) Trypanosoma cruzi infection in diabetic mice. Trans R Soc Trop Med Hyg 82:90–93PubMedCrossRefGoogle Scholar
  166. Tauchi-Sato K, Ozeki S, Houjou T, Taguchi R, Fujimoto T (2002) The surface of lipid droplets is a phospholipid monolayer with a unique fatty acid composition. J Biol Chem 277:44507–44512PubMedCrossRefGoogle Scholar
  167. Tee AR, Manning BD, Roux PP, Cantley LC, Blenis J (2003) Tuberous sclerosis complex gene products, Tuberin and Hamartin, control mTOR signaling by acting as a GTPase-activating protein complex toward Rheb. Curr Biol 13:1259–1268PubMedCrossRefGoogle Scholar
  168. Tewary P, Veena K, Pucadyil TJ, Chattopadhyay A, Madhubala R (2006) The sterol-binding antibiotic nystatin inhibits entry of non-opsonized Leishmania donovani into macrophages. Biochem Biophys Res Commun 339:661–666PubMedCrossRefGoogle Scholar
  169. Toledo DAM, D’Avila H, Melo RCN (2016) Host lipid bodies as platforms for intracellular survival of protozoan parasites. Front Immunol 7:1–6CrossRefGoogle Scholar
  170. Triggiani M, Oriente A, Seeds MC, Bass DA, Marone G, Chilton FH (1995) Migration of human inflammatory cells into the lung results in the remodeling of arachidonic acid into a triglyceride pool. J Exp Med 182:1181–1190PubMedCrossRefGoogle Scholar
  171. Trindade S, Rijo-Ferreira F, Carvalho T, Pinto-Neves D, Guegan F, Aresta-Branco F, Bento F, Young SA, Pinto A, Van Den Abbeele J et al (2016) Trypanosoma brucei parasites occupy and functionally adapt to the adipose tissue in mice. Cell Host Microbe 19:837–848PubMedPubMedCentralCrossRefGoogle Scholar
  172. Vial HJ, Eldin P, Tielens AGM, Van Hellemond JJ (2003) Phospholipids in parasitic protozoa. Mol Biochem Parasitol 126:143–154PubMedCrossRefGoogle Scholar
  173. Vilar-Pereira G, Carneiro VC, Mata-Santos H, Vicentino ARR, Ramos IP, Giarola NLL, Feijó DF, Meyer-Fernandes JR, Paula-Neto HA, Medei E et al (2016) Resveratrol reverses functional chagas heart disease in mice. PLOS Pathog 12:e1005947PubMedPubMedCentralCrossRefGoogle Scholar
  174. Wan H-C, Melo RCN, Jin Z, Dvorak AM, Weller PF (2007) Roles and origins of leukocyte lipid bodies: proteomic and ultrastructural studies. FASEB J 21:167–178PubMedCrossRefGoogle Scholar
  175. Wang Z, Wilson WA, Fujino MA, Roach PJ (2001) Antagonistic controls of autophagy and glycogen accumulation by Snf1p, the yeast homolog of AMP-activated protein kinase, and the cyclin-dependent kinase Pho85p. Mol Cell Biol 21:5742–5752PubMedPubMedCentralCrossRefGoogle Scholar
  176. Wang Y, Weiss LM, Orlofsky A (2009a) Intracellular parasitism with Toxoplasma gondii stimulates mammalian-target-of-rapamycin-dependent host cell growth despite impaired signalling to S6K1 and 4E-BP1. Cell Microbiol 11:983–1000PubMedPubMedCentralCrossRefGoogle Scholar
  177. Wang Y, Weiss LM, Orlofsky A (2009b) Host cell autophagy is induced by Toxoplasma gondii and contributes to parasite growth. J Biol Chem 284:1694–1701PubMedPubMedCentralCrossRefGoogle Scholar
  178. Wang Y, Weiss LM, Orlofsky A (2010) Coordinate control of host centrosome position, organelle distribution, and migratory response by Toxoplasma gondii via host mTORC2. J Biol Chem 285:15611–15618PubMedPubMedCentralCrossRefGoogle Scholar
  179. Wang QA, Tao C, Gupta RK, Scherer PE (2013) Tracking adipogenesis during white adipose tissue development, expansion and regeneration. Nat Med 19:1338–1344PubMedPubMedCentralCrossRefGoogle Scholar
  180. Wilairatana P, Riganti M, Puchadapirom P, Punpoowong B, Vannaphan S, Udomsangpetch R, Krudsood S, Brittenham GM, Looareesuwan S (2000) Prognostic significance of skin and subcutaneous fat sequestration of parasites in severe falciparum malaria. Southeast Asian J Trop Med Public Health 31:203–212PubMedGoogle Scholar
  181. Wilkowsky SE, Barbieri MA, Stahl P, Isola ELD (2001) Trypanosoma cruzi: phosphatidylinositol 3-kinase and protein kinase B activation is associated with parasite invasion. Exp Cell Res 218:211–218CrossRefGoogle Scholar
  182. Wolfson RL, Chantranupong L, Saxton RA, Shen K, Scaria SM, Cantor JR, Sabatini DM (2016) Sestrin2 is a leucine sensor for the mTORC1 pathway. Science 351:43–48PubMedCrossRefGoogle Scholar
  183. Wolins NE, Rubin B, Brasaemle DL (2001) TIP47 associates with lipid droplets. J Biol Chem 276:5101–5108PubMedCrossRefGoogle Scholar
  184. Yalaoui S, Huby T, Gego A, Rametti A, Moreau M, Collet X, Siau A, Van Gemert G, Sauerwein RW, Luty AJF et al (2008) Article scavenger receptor BI boosts hepatocyte permissiveness to plasmodium infection. Cell Host Microbe 4:283–292PubMedCrossRefGoogle Scholar
  185. Zhang HH, Huang J, Düvel K, Boback B, Wu S, Squillance RM, Wu CL, Manning BD (2009) Insulin stimulates adipogenesis through the Akt-TSC2-mTORC1 pathway. PLoS One 4:e6189PubMedPubMedCentralCrossRefGoogle Scholar
  186. Zhang CS, Jiang B, Li M, Zhu M, Peng Y, Zhang YL, Wu YQ, Li TY, Liang Y, Lu Z et al (2014) The lysosomal v-ATPase-ragulator complex is a common activator for AMPK and mTORC1, acting as a switch between catabolism and anabolism. Cell Metab 20:526–540PubMedCrossRefGoogle Scholar
  187. Zuzarte-Luis V, Mello-Vieira J, Marreiros IM, Liehl P, Chora AF, Carret C, Carvalho T, Mota MM (2017) Dietary alterations modulate susceptibility to Plasmodium infection. Nat Microbiol 2(12):1600–1607PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Diana Moreira
    • 1
    • 2
    • 3
    • 4
    • 5
  • Jérôme Estaquier
    • 6
    • 7
  • Anabela Cordeiro-da-Silva
    • 3
    • 4
    • 5
  • Ricardo Silvestre
    • 1
    • 2
  1. 1.Life and Health Sciences Research Institute (ICVS), School of MedicineUniversity of MinhoBragaPortugal
  2. 2.ICVS/3B’s-PT Government Associate LaboratoryBraga/GuimarãesPortugal
  3. 3.i3S-Instituto de Investigacão e Inovação em SaúdeUniversidade do PortoPortoPortugal
  4. 4.IBMC-Instituto de Biologia Molecular e CelularUniversidade do PortoPortoPortugal
  5. 5.Departamento de Ciências Bioloógicas, Faculdade de FarmaáciaUniversidade do PortoPortoPortugal
  6. 6.CNRS FR 3636, Université Paris DescartesParisFrance
  7. 7.Centre de Recherche du CHU de QuébecUniversité LavalQuébecCanada

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