Developmentally regulated sphingolipid degradation in Leishmania major

PLoS ONE

Volumn 7, Issue 1, 2012, Pages

  Zhang, Ou ^a   Xu, Wei ^a   Pillai, Agiesh ^a   Zhang, Kai ^a  

^a TEXAS TECH UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INOSITOL PHOSPHOSPHINGOLIPID PHOSPHOLIPASE C LIKE ENZYME; PHOSPHODIESTERASE; SPHINGOLIPID; UNCLASSIFIED DRUG; GLYCOSPHINGOLIPID; INOSITOLPHOSPHORYLCERAMIDE; PHOSPHOLIPASE C; SPHINGOMYELIN PHOSPHODIESTERASE;

ACID TOLERANCE; AMASTIGOTE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; ENZYME ACTIVITY; FEMALE; HOST PARASITE INTERACTION; LEISHMANIA MAJOR; LIPID DEGRADATION; MACROPHAGE; MAMMAL; MOUSE; NONHUMAN; PARASITE DEVELOPMENT; PARASITE SURVIVAL; PARASITE VIRULENCE; PROMASTIGOTE; PROTEIN EXPRESSION; ANIMAL; BAGG ALBINO MOUSE; CELL SHAPE; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTAGENESIS; PARASITOLOGY; PHYSIOLOGY; SKIN LEISHMANIASIS; TRANSGENIC ANIMAL;

LEISHMANIA MAJOR; MAMMALIA; MUS; PHLEBOTOMINAE; PROTOZOA;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL SHAPE; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLYCOSPHINGOLIPIDS; HOST-PARASITE INTERACTIONS; LEISHMANIA MAJOR; LEISHMANIASIS, CUTANEOUS; MICE; MICE, INBRED BALB C; MUTAGENESIS; SPHINGOLIPIDS; SPHINGOMYELIN PHOSPHODIESTERASE; TYPE C PHOSPHOLIPASES;

EID: 84863407848     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0031059     Document Type: Article

References (57)

1. Myler PJ, (2008) Searching the Tritryp genomes for drug targets. Adv Exp Med Biol 625: 133-140.
2. Croft SL, Coombs GH, (2003) Leishmaniasis-current chemotherapy and recent advances in the search for novel drugs. Trends Parasitol 19: 502-508.
3. Castillo E, Dea-Ayuela MA, Bolas-Fernandez F, Rangel M, Gonzalez-Rosende ME, (2010) The kinetoplastid chemotherapy revisited: current drugs, recent advances and future perspectives. Curr Med Chem 17: 4027-4051.
4. Bartke N, Hannun YA, (2009) Bioactive sphingolipids: metabolism and function. J Lipid Res 50 (Suppl): S91-96.
5. Gault CR, Obeid LM, Hannun YA, (2010) An overview of sphingolipid metabolism: from synthesis to breakdown. Adv Exp Med Biol 688: 1-23.
6. Marchesini N, Hannun YA, (2004) Acid and neutral sphingomyelinases: roles and mechanisms of regulation. Biochem Cell Biol 82: 27-44.
7. Duan RD, (2006) Alkaline sphingomyelinase: an old enzyme with novel implications. Biochim Biophys Acta 1761: 281-291.
8. Clarke CJ, Wu BX, Hannun YA, (2011) The neutral sphingomyelinase family: identifying biochemical connections. Adv Enzyme Regul 51: 51-58.
9. Dickson RC, Lester RL, (1999) Yeast sphingolipids. Biochim Biophys Acta 1426: 347-357.
10. Sperling P, Heinz E, (2003) Plant sphingolipids: structural diversity, biosynthesis, first genes and functions. Biochim Biophys Acta 1632: 1-15.
11. Zhang K, Beverley SM, (2010) Phospholipid and sphingolipid metabolism in Leishmania. Mol Biochem Parasitol 170: 55-64.
12. Sawai H, Okamoto Y, Luberto C, Mao C, Bielawska A, et al. (2000) Identification of ISC1 (YER019w) as inositol phosphosphingolipid phospholipase C in Saccharomyces cerevisiae. J Biol Chem 275: 39793-39798.
13. Vaena de Avalos S, Okamoto Y, Hannun YA, (2004) Activation and localization of inositol phosphosphingolipid phospholipase C, Isc1p, to the mitochondria during growth of Saccharomyces cerevisiae. J Biol Chem 279: 11537-11545.
14. Vaena de Avalos S, Su X, Zhang M, Okamoto Y, Dowhan W, et al. (2005) The phosphatidylglycerol/cardiolipin biosynthetic pathway is required for the activation of inositol phosphosphingolipid phospholipase C, Isc1p, during growth of Saccharomyces cerevisiae. J Biol Chem 280: 7170-7177.
15. Cowart LA, Hannun YA, (2005) Using genomic and lipidomic strategies to investigate sphingolipid function in the yeast heat-stress response. Biochem Soc Trans 33: 1166-1169.
16. Kitagaki H, Cowart LA, Matmati N, Montefusco D, Gandy J, et al. (2009) ISC1-dependent metabolic adaptation reveals an indispensable role for mitochondria in induction of nuclear genes during the diauxic shift in Saccharomyces cerevisiae. J Biol Chem 284: 10818-10830.
17. Shea JM, Kechichian TB, Luberto C, Del Poeta M, (2006) The cryptococcal enzyme inositol phosphosphingolipid-phospholipase C confers resistance to the antifungal effects of macrophages and promotes fungal dissemination to the central nervous system. Infect Immun 74: 5977-5988.
18. Henry J, Guillotte A, Luberto C, Del Poeta M, (2011) Characterization of inositol phospho-sphingolipid-phospholipase C 1 (Isc1) in Cryptococcus neoformans reveals unique biochemical features. FEBS Lett 585: 635-640.
19. Kaneshiro ES, Jayasimhulu K, Lester RL, (1986) Characterization of inositol lipids from Leishmania donovani promastigotes: identification of an inositol sphingophospholipid. J Lipid Res 27: 1294-1303.
20. Zhang K, Showalter M, Revollo J, Hsu FF, Turk J, et al. (2003) Sphingolipids are essential for differentiation but not growth in Leishmania. EMBO J 22: 6016-6026.
21. Zhang O, Wilson MC, Xu W, Hsu FF, Turk J, et al. (2009) Degradation of host sphingomyelin is essential for Leishmania virulence. PLoS Pathog 5 (12): e1000692.
22. Xu W, Xin L, Soong L, Zhang K, (2011) Sphingolipid degradation by Leishmania is required for its resistance to acidic pH in the mammalian host. Infection and Immunity in press.
23. Young SA, Smith TK, The essential neutral sphingomyelinase is involved in the trafficking of the variant surface glycoprotein in the bloodstream form of Trypanosoma brucei. Mol Microbiol 76: 1461-1482.
24. Sacks DL, Perkins PV, (1984) Identification of an infective stage of Leishmania promastigotes. Science 223: 1417-1419.
25. Matmati N, Hannun YA, (2008) Thematic Review Series: Sphingolipids. ISC1 (inositol phosphosphingolipid-phospholipase C), the yeast homologue of neutral sphingomyelinases. J Lipid Res 49: 922-928.
26. Okamoto Y, Vaena De Avalos S, Hannun YA, (2002) Structural requirements for selective binding of ISC1 to anionic phospholipids. J Biol Chem 277: 46470-46477.
27. Clarke CJ, Snook CF, Tani M, Matmati N, Marchesini N, et al. (2006) The extended family of neutral sphingomyelinases. Biochemistry 45: 11247-11256.
28. Okamoto Y, Vaena de Avalos S, Hannun YA, (2003) Functional analysis of ISC1 by site-directed mutagenesis. Biochemistry 42: 7855-7862.
29. Tamura H, Tameishi K, Yamada A, Tomita M, Matsuo Y, et al. (1995) Mutation in aspartic acid residues modifies catalytic and haemolytic activities of Bacillus cereus sphingomyelinase. Biochem J 309 (Pt 3): 757-764.
30. Ha DS, Schwarz JK, Turco SJ, Beverley SM, (1996) Use of the green fluorescent protein as a marker in transfected Leishmania. Mol Biochem Parasitol 77: 57-64.
31. Denny PW, Gokool S, Russell DG, Field MC, Smith DF, (2000) Acylation-dependent protein export in Leishmania. J Biol Chem 275: 11017-11025.
32. Bates PA, (2008) Leishmania sand fly interaction: progress and challenges. Curr Opin Microbiol 11: 340-344.
33. Sacks DL, Perkins PV, (1985) Development of infective stage Leishmania promastigotes within phlebotomine sand flies. Am J Trop Med Hyg 34: 456-459.
34. Saunders EC, DP DES, Naderer T, Sernee MF, Ralton JE, et al. (2010) Central carbon metabolism of Leishmania parasites. Parasitology 137: 1303-1313.
35. Bringaud F, Riviere L, Coustou V, (2006) Energy metabolism of trypanosomatids: adaptation to available carbon sources. Mol Biochem Parasitol 149: 1-9.
36. Marchesini N, Docampo R, (2002) A plasma membrane P-type H(+)-ATPase regulates intracellular pH in Leishmania mexicana amazonensis. Mol Biochem Parasitol 119: 225-236.
37. Vieira L, Slotki I, Cabantchik ZI, (1995) Chloride conductive pathways which support electrogenic H+ pumping by Leishmania major promastigotes. J Biol Chem 270: 5299-5304.
38. Nikolova-Karakashian MN, Rozenova KA, (2010) Ceramide in stress response. Adv Exp Med Biol 688: 86-108.
39. Goni FM, Alonso A, (2002) Sphingomyelinases: enzymology and membrane activity. FEBS Lett 531: 38-46.
40. Almeida T, Marques M, Mojzita D, Amorim MA, Silva RD, et al. (2007) Isc1p Plays a Key Role in Hydrogen Peroxide Resistance and Chronological Lifespan through Modulation of Iron Levels and Apoptosis. Mol Biol Cell.
41. Almeida T, Marques M, Mojzita D, Amorim MA, Silva RD, et al. (2008) Isc1p plays a key role in hydrogen peroxide resistance and chronological lifespan through modulation of iron levels and apoptosis. Mol Biol Cell 19: 865-876.
42. Barbosa AD, Osorio H, Sims KJ, Almeida T, Alves M, et al. (2011) Role for Sit4p-dependent mitochondrial dysfunction in mediating the shortened chronological lifespan and oxidative stress sensitivity of Isc1p-deficient cells. Mol Microbiol 81: 515-527.
43. Schulze H, Sandhoff K, (2011) Lysosomal lipid storage diseases. Cold Spring Harb Perspect Biol 3.
44. Schuchman EH, (2010) Acid sphingomyelinase, cell membranes and human disease: lessons from Niemann-Pick disease. FEBS Lett 584: 1895-1900.
45. Levran O, Desnick RJ, Schuchman EH, (1991) Niemann-Pick disease: a frequent missense mutation in the acid sphingomyelinase gene of Ashkenazi Jewish type A and B patients. Proc Natl Acad Sci U S A 88: 3748-3752.
46. Smith EL, Schuchman EH, (2008) The unexpected role of acid sphingomyelinase in cell death and the pathophysiology of common diseases. Faseb J 22: 3419-3431.
47. Kapler GM, Coburn CM, Beverley SM, (1990) Stable transfection of the human parasite Leishmania major delineates a 30-kilobase region sufficient for extrachromosomal replication and expression. Mol Cell Biol 10: 1084-1094.
48. Akopyants NS, Matlib RS, Bukanova EN, Smeds MR, Brownstein BH, et al. (2004) Expression profiling using random genomic DNA microarrays identifies differentially expressed genes associated with three major developmental stages of the protozoan parasite Leishmania major. Mol Biochem Parasitol 136: 71-86.
49. Ouakad M, Bahi-Jaber N, Chenik M, Dellagi K, Louzir H, (2007) Selection of endogenous reference genes for gene expression analysis in Leishmania major developmental stages. Parasitol Res 101: 473-477.
50. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
51. Ranasinghe S, Rogers ME, Hamilton JG, Bates PA, Maingon RD, (2008) A real-time PCR assay to estimate Leishmania chagasi load in its natural sand fly vector Lutzomyia longipalpis. Trans R Soc Trop Med Hyg 102: 875-882.
52. Zhang K, Hsu FF, Scott DA, Docampo R, Turk J, et al. (2005) Leishmania salvage and remodelling of host sphingolipids in amastigote survival and acidocalcisome biogenesis. Mol Microbiol 55: 1566-1578.
53. Zhang K, Pompey JM, Hsu FF, Key P, Bandhuvula P, et al. (2007) Redirection of sphingolipid metabolism toward de novo synthesis of ethanolamine in Leishmania. EMBO J 26: 1094-1104.
54. Racoosin EL, Beverley SM, (1997) Leishmania major: promastigotes induce expression of a subset of chemokine genes in murine macrophages. Exp Parasitol 85: 283-295.
55. Glaser TA, Wells SJ, Spithill TW, Pettitt JM, Humphris DC, et al. (1990) Leishmania major and L. donovani: a method for rapid purification of amastigotes. Exp Parasitol 71: 343-345.
56. Titus RG, Marchand M, Boon T, Louis JA, (1985) A limiting dilution assay for quantifying Leishmania major in tissues of infected mice. Parasite Immunol 7: 545-555.
57. Titus RG, Muller I, Kimsey P, Cerny A, Behin R, et al. (1991) Exacerbation of experimental murine cutaneous leishmaniasis with CD4+ Leishmania major-specific T cell lines or clones which secrete interferon-gamma and mediate parasite-specific delayed-type hypersensitivity. Eur J Immunol 21: 559-567.