The Leishmania-macrophage interaction: A metabolic perspective

Cellular Microbiology

Volumn 10, Issue 2, 2008, Pages 301-308

  Naderer, Thomas ^a   McConville, Malcolm J ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CELL RECEPTOR; ESSENTIAL AMINO ACID; LIPOPHOSPHOGLYCAN; POLYAMINE;

CARBON SOURCE; CELL INTERACTION; CELL METABOLISM; GLYCOCALYX; HOST PATHOGEN INTERACTION; HOST RESISTANCE; LEISHMANIA; MACROPHAGE; NONHUMAN; NUTRIENT AVAILABILITY; NUTRIENT UPTAKE; PARASITE SURVIVAL; PHAGOCYTOSIS; PHOSPHOLIPID TRANSFER; PRIORITY JOURNAL; SHORT SURVEY;

ANIMALS; GLYCOCALYX; HOST-PARASITE INTERACTIONS; LEISHMANIA; MACROPHAGES; PHAGOSOMES;

MAMMALIA; PROTOZOA;

EID: 38049129044     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2007.01096.x     Document Type: Short Survey

References (64)

1. Antoine, J.C., Prina, E., Lang, T., and Courret, N. (1998) The biogenesis and properties of the parasitophorous vacuoles that harbour Leishmania in murine macrophages. Trends Microbiol 6: 392-401.
2. Barr, S.D., and Gedamu, L. (2003) Role of peroxidoxins in Leishmania chagasi survival. Evidence of an enzymatic defense against nitrosative stress. J Biol Chem 278: 10816-10823.
3. Besteiro, S., Williams, R.A., Coombs, G.H., and Mottram, J.C. (2007) Protein turnover and differentiation in Leishmania. Int J Parasitol 37: 1063-1075.
4. Blackwell, J.M., Searle, S., Mohamed, H., and White, J.K. (2003) Divalent cation transport and susceptibility to infectious and autoimmune disease: Continuation of the Ity/Lsh/Bcg/Nramp1/Slc11a1 gene story. Immunol Lett 85: 197-203.
5. Burchmore, R.J., and Barrett, M.P. (2001) Life in vacuoles-nutrient acquisition by Leishmania amastigotes. Int J Parasitol 31: 1311-1320.
6. Burchmore, R.J., Rodriguez-Contreras, D., McBride, K., Merkel, P., Barrett, M.P., Modi, G., etal. (2003) Genetic characterization of glucose transporter function in Leishmania mexicana. Proc Natl Acad Sci USA 100: 3901-3906.
7. Cameron, P., McGachy, A., Anderson, M., Paul, A., Coombs, G.H., Mottram, J.C., etal. (2004) Inhibition of lipopolysaccharide-induced macrophage IL-12 production by Leishmania mexicana amastigotes: The role of cysteine peptidases and the NF-kappaB signaling pathway. J Immunol 173: 3297-3304.
8. Capul, A.A., Hickerson, S., Barron, T., Turco, S.J., and Beverley, S.M. (2007) Comparisons of mutants lacking the Golgi UDP-galactose or GDP-mannose transporters establish that phosphoglycans are important for promastigote but not amastigote virulence in Leishmania major. Infect Immun 75: 4629-4637.
9. Croft, S.L., Sundar, S., and Fairlamb, A.H. (2006) Drug resistance in leishmaniasis. Clin Microbiol Rev 19: 111-126.
10. Dogra, N., Warburton, C., and McMaster, W.R. (2007) Leishmania major abrogates gamma interferon-induced gene expression in human macrophages from a global perspective. Infect Immun 75: 3506-3515.
11. Garami, A., and Ilg, T. (2001a) The role of phosphomannose isomerase in Leishmania mexicana glycoconjugate synthesis and virulence. J Biol Chem 276: 6566-6575.
12. Garami, A., and Ilg, T. (2001b) Disruption of mannose activation in Leishmania mexicana: GDP-mannose pyrophosphorylase is required for virulence, but not for viability. EMBO J 20: 3657-3666.
13. Geraldo, M.V., Silber, A.M., Pereira, C.A., and Uliana, S.R. (2005) Characterisation of a developmentally regulated amino acid transporter gene from Leishmania amazonensis. FEMS Microbiol Lett 242: 275-280.
14. Gordon, S. (2003) Alternative activation of macrophages. Nat Rev Immunol 3: 23-35.
15. Gueirard, P., Laplante, A., Rondeau, C., Milon, G., and Desjardins, M. (2007) Trafficking of Leishmania donovani promastigotes in non-lytic compartments in neutrophils enables the subsequent transfer of parasites to macrophages. Cell Microbiol 10: 100-111.
16. Hart, D.T., and Coombs, G.H. (1982) Leishmania mexicana: Energy metabolism of amastigotes and promastigotes. Exp Parasitol 54: 397-409.
17. Hoyer, C., Zander, D., Fleischer, S., Schilhabel, M., Kroener, M., Platzer, M., and Clos, J. (2004) A Leishmania donovani gene that confers accelerated recovery from stationary phase growth arrest. Int J Parasitol 34: 803-811.
18. Huynh, C., Sacks, D.L., and Andrews, N.W. (2006) A Leishmania amazonensis ZIP family iron transporter is essential for parasite replication within macrophage phagolysosomes. J Exp Med 203: 2363-2375.
19. Ilg, T. (2000) Lipophosphoglycan is not required for infection of macrophages or mice by Leishmania mexicana. EMBO J 19: 1953-1962.
20. Ilg, T. (2002) Generation of myo-inositol-auxotrophic Leishmania mexicana mutants by targeted replacement of the myo-inositol-1-phosphate synthase gene. Mol Biochem Parasitol 120: 151-156.
21. Iniesta, V., Gomez-Nieto, L.C., and Corraliza, I. (2001) The inhibition of arginase by N(omega)-hydroxy-1-arginine controls the growth of Leishmania inside macrophages. J Exp Med 193: 777-784.
22. Iniesta, V., Carcelen, J., Molano, I., Peixoto, P.M., Redondo, E., Parra, P., etal. (2005) Arginase I induction during Leishmania major infection mediates the development of disease. Infect Immun 73: 6085-6090.
23. Ivens, A.C., Peacock, C.S., Worthey, E.A., Murphy, L., Aggarwal, G., Berriman, M., etal. (2005) The Genome of the Kinetoplastid Parasite, Leishmania major. Science 309: 436-442.
24. Johann, A.M., Barra, V., Kuhn, A.M., Weigert, A., von Knethen, A., and Brune, B. (2007) Apoptotic cells induce arginase II in macrophages, thereby attenuating NO production. FASEB J 21: 2704-2712.
25. Kane, M.M., and Mosser, D.M. (2001) The role of IL-10 in promoting disease progression in leishmaniasis. J Immunol 166: 1141-1147.
26. Kima, P.E. (2007) The amastigote forms of Leishmania are experts at exploiting host cell processes to establish infection and persist. Int J Parasitol 37: 1087-1096.
27. Kropf, P., Herath, S., Weber, V., Modolell, M., and Muller, I. (2003) Factors influencing Leishmania major infection in IL-4-deficient BALB/c mice. Parasite Immunol 25: 439-447.
28. Kropf, P., Fuentes, J.M., Fahnrich, E., Arpa, L., Herath, S., Weber, V., etal. (2005) Arginase and polyamine synthesis are key factors in the regulation of experimental leishmaniasis in vivo. FASEB J 19: 1000-1002.
29. Landfear, S.M. (2001) Molecular genetics of nucleoside transporters in Leishmania and African trypanosomes. Biochem Pharmacol 62: 149-155.
30. Lodge, R., Diallo, T.O., and Descoteaux, A. (2006) Leishmania donovani lipophosphoglycan blocks NADPH oxidase assembly at the phagosome membrane. Cell Microbiol 8: 1922-1931.
31. McConville, M.J., and Blackwell, J.M. (1991) Developmental changes in the glycosylated phosphatidylinositols of Leishmania donovani. Characterization of the promastigote and amastigote glycolipids. J Biol Chem 266: 15170-15179.
32. McConville, M.J., de Souza, D., Saunders, E., Likic, V.A., and Naderer, T. (2007) Living in a phagolysosome; metabolism of Leishmania amastigotes. Trends Parasitol 23: 368-375.
33. Maugeri, D.A., Cazzulo, J.J., Burchmore, R.J., Barrett, M.P., and Ogbunude, P.O. (2003) Pentose phosphate metabolism in Leishmania mexicana. Mol Biochem Parasitol 130: 117-125.
34. Murray, H.W., Szuro-Sudol, A., Wellner, D., Oca, M.J., Granger, A.M., Libby, D.M., etal. (1989) Role of tryptophan degradation in respiratory burst-independent antimicrobial activity of gamma interferon-stimulated human macrophages. Infect Immun 57: 845-849.
35. Naderer, T., Vince, J.E., and McConville, M.J. (2004) Surface determinants of Leishmania parasites and their role in infectivity in the mammalian host. Curr Mol Med 4: 649-665.
36. Naderer, T., Ellis, M.A., Sernee, M.F., De Souza, D.P., Curtis, J., Handman, E., and McConville, M.J. (2006) Virulence of Leishmania major in macrophages and mice requires the gluconeogenic enzyme fructose-1,6-bisphosphatase. Proc Natl Acad Sci USA 103: 5502-5507.
37. Opperdoes, F., and Coombs, G.H. (2007) Metabolism of Leishmania; proven and predicted. Trends Parasitology 23: 149-158.
38. Ortiz, D., Sanchez, M.A., Pierce, S., Herrmann, T., Kimblin, N., Archie Bouwer, H.G., and Landfear, S.M. (2007) Molecular genetic analysis of purine nucleobase transport in Leishmania major. Mol Microbiol 64: 1228-1243.
39. Ouellette, M., Drummelsmith, J., El-Fadili, A., Kundig, C., Richard, D., and Roy, G. (2002) Pterin transport and metabolism in Leishmania and related trypanosomatid parasites. Int J Parasitol 32: 385-398.
40. Plewes, K.A., Barr, S.D., and Gedamu, L. (2003) Iron superoxide dismutases targeted to the glycosomes of Leishmania chagasi are important for survival. Infect Immun 71: 5910-5920.
41. Qi, H., Ji, J., Wanasen, N., and Soong, L. (2004) Enhanced replication of Leishmania amazonensis amastigotes in gamma interferon-stimulated murine macrophages: Implications for the pathogenesis of cutaneous leishmaniasis. Infect Immun 72: 988-995.
42. Ralton, J.E., Naderer, T., Piraino, H.L., Bashtannyk, T.A., Callaghan, J.M., and McConville, M.J. (2003) Evidence that intracellular β1-2 mannan is a virulence factor in Leishmania parasites. J Biol Chem 278: 40757-40763.
43. Roberts, S.C., Tancer, M.J., Polinsky, M.R., Gibson, K.M., Heby, O., and Ullman, B. (2004) Arginase plays a pivotal role in polyamine precursor metabolism in Leishmania. Characterization of gene deletion mutants. J Biol Chem 279: 23668-23678.
44. Rochette, A., McNicoll, F., Girard, J., Breton, M., Leblanc, E., Bergeron, M.G., and Papadopoulou, B. (2005) Characterization and developmental gene regulation of a large gene family encoding amastin surface proteins in Leishmania spp. Mol Biochem Parasitol 140: 205-220.
45. Rosenzweig, D., Smith, D., Opperdoes, F., Stern, S., Olafson, R.W., and Zilberstein, D. (2007) Retooling Leishmania metabolism: From sand fly gut to human macrophage. FASEB J (in press) doi: 10.1096/fj.07-9254com.
46. Rubin-Bejerano, I., Fraser, I., Grisafi, P., and Fink, G.R. (2003) Phagocytosis by neutrophils induces an amino acid deprivation response in Saccharomyces cerevisiae and Candida albicans. Proc Natl Acad Sci USA 100: 11007-11012.
47. Sacks, D., and Anderson, C. (2004) Re-examination of the immunosuppressive mechanisms mediating non-cure of Leishmania infection in mice. Immunol Rev 201: 225-238.
48. Schaible, U.E., and Kaufmann, S.H. (2005) A nutritive view on the host-pathogen interplay. Trends Microbiol 13: 373-380.
49. Schaible, U.E., Schlesinger, P.H., Steinberg, T.H., Mangel, W.F., Kobayashi, T., and Russell, D.G. (1999) Parasitophorous vacuoles of Leishmania mexicana acquire macromolecules from the host cell cytosol via two independent routes. J Cell Sci 112: 681-693.
50. Sernee, M.F., Ralton, J.E., Dinev, Z., Khairallah, G.N., O'Hair, R.A., Williams, S.J., and McConville, M.J. (2006) Leishmania β-1,2-mannan is assembled on a mannose-cyclic phosphate primer. Proc Natl Acad Sci USA 103: 9458-9463.
51. Shaked-Mishan, P., Suter-Grotemeyer, M., Yoel-Almagor, T., Holland, N., Zilberstein, D., and Rentsch, D. (2006) A novel high-affinity arginine transporter from the human parasitic protozoan Leishmania donovani. Mol Microbiol 60: 30-38.
52. Spath, G.F., Garraway, L.A., Turco, S.J., and Beverley, S.M. (2003) The role (s) of lipophosphoglycan (LPG) in the establishment of Leishmania major infections in mammalian hosts. Proc Natl Acad Sci USA 100: 9536-9541.
53. Tovar, J., Cunningham, M.L., Smith, A.C., Croft, S.L., and Fairlamb, A.H. (1998) Down-regulation of Leishmania donovani trypanothione reductase by heterologous expression of a trans-dominant mutant homologue: Effect on parasite intracellular survival. Proc Natl Acad Sci USA 95: 5311-5316.
54. Vickers, T.J., Orsomando, G., de la Garza, R.D., Scott, D.A., Kang, S.O., Hanson, A.D., and Beverley, S.M. (2006) Biochemical and genetic analysis of methylenetetrahydrofolate reductase in Leishmania metabolism and virulence. J Biol Chem 281: 38150-38158.
55. Voth, D.E., and Heinzen, R.A. (2007) Lounging in a lysosome: The intracellular lifestyle of Coxiella burnetii. Cell Microbiol 9: 829-840.
56. Wanasen, N., MacLeod, C.L., Ellies, L.G., and Soong, L. (2007) 1-arginine and cationic amino acid transporter 2B regulate growth and survival of Leishmania amazonensis amastigotes in macrophages. Infect Immun 75: 2802-2810.
57. Wanderley, J.L., Moreira, M.E., Benjamin, A., Bonomo, A.C., and Barcinski, M.A. (2006) Mimicry of apoptotic cells by exposing phosphatidylserine participates in the establishment of amastigotes of Leishmania (L) amazonensis in mammalian hosts. J Immunol 176: 1834-1839.
58. Winter, G., Fuchs, M., McConville, M.J., Stierhof, Y.D., and Overath, P. (1994) Surface antigens of Leishmania mexicana amastigotes: characterization of glycoinositol phospholipids and a macrophage-derived glycosphingolipid. J Cell Sci 107: 2471-2482.
59. van Zandbergen, G., Klinger, M., Mueller, A., Dannenberg, S., Gebert, A., Solbach, W., and Laskay, T. (2004) Cutting edge: Neutrophil granulocyte serves as a vector for Leishmania entry into macrophages. J Immunol 173: 6521-6525.
60. van Zandbergen, G., Bollinger, A., Wenzel, A., Kamhawi, S., Voll, R., Klinger, M., etal. (2006) Leishmania disease development depends on the presence of apoptotic promastigotes in the virulent inoculum. Proc Natl Acad Sci USA 103: 13837-13842.
61. van Zandbergen, G., Solbach, W., and Laskay, T. (2007) Apoptosis driven infection. Autoimmunity 40: 349-352.
62. Zhang, K., Hsu, F.F., Scott, D.A., Docampo, R., Turk, J., and Beverley, S.M. (2005) Leishmania salvage and remodelling of host sphingolipids in amastigote survival and acidocalcisome biogenesis. Mol Microbiol 55: 1566-1578.
63. Zhang, K., Pompey, J.M., Hsu, F.F., Key, P., Bandhuvula, P., Saba, J.D., etal. (2007) Redirection of sphingolipid metabolism toward de novo synthesis of ethanolamine in Leishmania. EMBO J 26: 1094-1104.
64. Zufferey, R., Allen, S., Barron, T., Sullivan, D.R., Denny, P.W., Almeida, I.C., etal. (2003) Ether phospholipids and glycosylinositolphospholipids are not required for amastigote virulence or for inhibition of macrophage activation by Leishmania major. J Biol Chem 278: 44708-44718.