Evidence for a structural role for acid-fast lipids in oocyst walls of cryptosporidium, Toxoplasma, and Eimeria

mBio

Volumn 4, Issue 5, 2013, Pages

  Bushkin, G Guy ^a,b,d   Motari, Edwin ^a   Carpentieri, Andrea ^a,e   Dubey, Jitender P ^c   Costello, Catherine E ^b   Robbins, Phillips W ^a   Samuelson, John ^a,b  

^a BOSTON UNIVERSITY   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c AGRICULTURAL RESEARCH SERVICE   (United States)

^d WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^e UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ACYLTRANSFERASE; CELLULOSE; CUTINE; GLUCAN; LIPID; MYCOLIC ACID; ORGANIC SOLVENT; PEPTIDOGLYCAN; POLYKETIDE SYNTHASE; TRIACYLGLYCEROL; UNCLASSIFIED DRUG;

ACID FAST BACTERIUM; ACID FAST STAIN; ARTICLE; BACTERIAL CELL WALL; CELL COMPOSITION; CELL INTERACTION; CELL LABELING; COMPLEX FORMATION; CONTROLLED STUDY; CRYPTOSPORIDIUM; EIMERIA; LIPID ANALYSIS; LIPID BILAYER; LIPID COMPOSITION; LIPOGENESIS; MASS SPECTROMETRY; MYCOBACTERIUM; NONHUMAN; OOCYST; PLANT STRUCTURES; PRIORITY JOURNAL; STAINING; TOXOPLASMA;

ANIMALS; CELL WALL; CHICKENS; CRYPTOSPORIDIUM; EIMERIA; LIPID METABOLISM; LIPIDS; OOCYSTS; POULTRY DISEASES; PROTOZOAN INFECTIONS, ANIMAL; PROTOZOAN PROTEINS; STAINING AND LABELING; TOXOPLASMA;

EID: 84887163359     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00387-13     Document Type: Article

References (33)

1. Belli SI, Smith NC, Ferguson DJ. 2006. The coccidian oocyst: a tough nut to crack! Trends Parasitol. 22:416-423.
2. Dubey JP, Lindsay DS, Speer CA. 1998. Structures of Toxoplasma gondii tachyzoites, bradyzoites, and sporozoites and biology and development of tissue cysts. Clin. Microbiol. Rev. 11:267-299.
3. Weiss LM, Dubey JP. 2009. Toxoplasmosis: a history of clinical observations. Int. J. Parasitol. 39:895-901.
4. Ferguson DJ, Belli SI, Smith NC, Wallach MG. 2003. The development of the macrogamete and oocyst wall in Eimeria maxima: immuno-light and electron microscopy. Int. J. Parasitol. 33:1329-1340.
5. Chapman HD, Jeffers TK, Williams RB. 2010. Forty years of monensin for the control of coccidiosis in poultry. Poult. Sci. 89:1788-1801.
6. Kotloff KL, Nataro JP, Blackwelder WC, Nasrin D, Farag TH, Panchalingam S, Wu Y, Sow SO, Sur D, Breiman RF, Faruque AS, Zaidi AK, Saha D, Alonso PL, Tamboura B, Sanogo D, Onwuchekwa U, Manna B, Ramamurthy T, Kanungo S, Ochieng JB, Omore R, Oundo JO, Hossain A, Das SK, Ahmed S, Qureshi S, Quadri F, Adegbola RA, Antonio M, Hossain MJ, Akinsola A, Mandomando I, Nhampossa T, Acácio S, Biswas K, O'Reilly CE, Mintz ED, Berkeley LY, Muhsen K, Sommerfelt H, Robins-Browne RM, Levine MM. 2013. Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case-control study. Lancet 382:209-222.
7. Chatterjee A, Banerjee S, Steffen M, O'Connor RM, Ward HD, Robbins PW, Samuelson J. 2010. Evidence for mucin-like glycoproteins that tether sporozoites of Cryptosporidium parvum to the inner surface of the oocyst wall. Eukaryot. Cell 9:84-96.
8. Bushkin GG, Motari E, Magnelli P, Gubbels MJ, Dubey JP, Miska KB, Bullitt E, Costello CE, Robbins PW, Samuelson J. 2012. 1,3-Glucan, which can be targeted by drugs, forms a trabecular scaffold in the oocyst walls of Toxoplasma and Eimeria. mBio 3(5):e00258-12. doi:10.1128/ mBio.00258-12.
9. Mai K, Smith NC, Feng ZP, Katrib M, Slapeta J, Slapetova I, Wallach MG, Luxford C, Davies MJ, Zhang X, Norton RS, Belli SI. 2011. Peroxidase catalysed cross-linking of an intrinsically unstructured protein via dityrosine bonds in the oocyst wall of the apicomplexan parasite, Eimeria maxima. Int. J. Parasitol. 41:1157-1164.
10. Aurrecoechea C, Heiges M, Wang H, Wang Z, Fischer S, Rhodes P, Miller J, Kraemer E, Stoeckert CJ, Jr, Roos DS, Kissinger JC. 2007. ApiDB: integrated resources for the apicomplexan bioinformatics resource center. Nucleic Acids Res. 35:D427-D430.
11. Garcia LS, Bruckner DA, Brewer TC, Shimizu RY. 1983. Techniques for the recovery and identification of Cryptosporidium oocysts from stool specimens. J. Clin. Microbiol. 18:185-190.
12. Layre E, Sweet L, Hong S, Madigan CA, Desjardins D, Young DC, Cheng TY, Annand JW, Kim K, Shamputa IC, McConnell MJ, Debono CA, Behar SM, Minnaard AJ, Murray M, Barry CE, III, Matsunaga I, Moody DB. 2011. A comparative lipidomics platform for chemotaxonomic analysis of Mycobacterium tuberculosis. Chem. Biol. 18:1537-1549.
13. Yamada H, Bhatt A, Danev R, Fujiwara N, Maeda S, Mitarai S, Chikamatsu K, Aono A, Nitta K, Jacobs WR, Jr, Nagayama K. 2012. Nonacid-fastness in Mycobacterium tuberculosis DeltakasB mutant correlates with the cell envelope electron density. Tuberculosis (Edinb) 92:351-357.
14. Portevin D, De Sousa-D'Auria C, Houssin C, Grimaldi C, Chami M, Daffé M, Guilhot C. 2004. A polyketide synthase catalyzes the last condensation step of mycolic acid biosynthesis in mycobacteria and related organisms. Proc. Natl. Acad. Sci. U. S. A. 101:314-319.
15. Beisson F, Li-Beisson Y, Pollard M. 2012. Solving the puzzles of cutin and suberin polymer biosynthesis. Curr. Opin. Plant Biol. 15:329-337.
16. Hendry C, Dionne K, Hedgepeth A, Carroll K, Parrish N. 2009. Evaluation of a rapid fluorescent staining method for detection of mycobacteria in clinical specimens. J. Clin. Microbiol. 47:1206-1208.
17. Buda GJ, Isaacson T, Matas AJ, Paolillo DJ, Rose JK. 2009. Three dimensional imaging of plant cuticle architecture using confocal scanning laser microscopy. Plant J. 60:378-385.
18. Gulder TA, Freeman MF, Piel J. 1 March 2011. The catalytic diversity of multimodular polyketide synthases: natural product biosynthesis beyond textbook assembly rules. Top. Curr. Chem. [Epub ahead of print
19. Zhu G, LaGier MJ, Stejskal F, Millership JJ, Cai X, Keithly JS. 2002. Cryptosporidium parvum: the first protist known to encode a putative polyketide synthase. Gene 298:79-89.
20. Chiang YM, Oakley BR, Keller NP, Wang CC. 2010. Unraveling polyketide synthesis in members of the genus Aspergillus. Appl. Microbiol. Biotechnol. 86:1719-1736.
21. Mauzy MJ, Enomoto S, Lancto CA, Abrahamsen MS, Rutherford MS. 2012. The Cryptosporidium parvum transcriptome during in vitro development. PLoS One 7:e31715. doi:10.1371/journal.pone.0031715.
22. Cai X, Herschap D, Zhu G. 2005. Functional characterization of an evolutionarily distinct phosphopantetheinyl transferase in the apicomplexan Cryptosporidium parvum. Eukaryot. Cell 4:1211-1220.
23. Lesage G, Bussey H. 2006. Cell wall assembly in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 70:317-343.
24. Drummond RA, Brown GD. 2011. The role of Dectin-1 in the host defence against fungal infections. Curr. Opin. Microbiol. 14:392-399.
25. Possenti A, Cherchi S, Bertuccini L, Pozio E, Dubey JP, Spano F. 2010. Molecular characterisation of a novel family of cysteine-rich proteins of Toxoplasma gondii and ultrastructural evidence of oocyst wall localisation. Int. J. Parasitol. 40:1639-1649.
26. Hein EM, Blank LM, Heyland J, Baumbach JI, Schmid A, Hayen H. 2009. Glycerophospholipid profiling by high-performance liquid chromatography/mass spectrometry using exact mass measurements and multi-stage mass spectrometric fragmentation experiments in parallel. Rapid Commun. Mass Spectrom. 23:1636-1646.
27. Quittnat F, Nishikawa Y, Stedman TT, Voelker DR, Choi JY, Zahn MM, Murphy RC, Barkley RM, Pypaert M, Joiner KA, Coppens I. 2004. On the biogenesis of lipid bodies in ancient eukaryotes: synthesis of triacylglycerols by a Toxoplasma DGAT1-related enzyme. Mol. Biochem. Parasitol. 138:107-122.
28. Ramakrishnan S, Docampo MD, Macrae JI, Pujol FM, Brooks CF, van Dooren GG, Hiltunen JK, Kastaniotis AJ, McConville MJ, Striepen B. 2012. Apicoplast and endoplasmic reticulum cooperate in fatty acid biosynthesis in apicomplexan parasite Toxoplasma gondii. J. Biol. Chem. 287: 4957-4971.
29. Striepen B, Soldati D. 2007. Genetic manipulation of Toxoplasma gondii, p 391-418. In Kim LM, Kim K (ed), Toxoplasma gondii, the model apicomplexan: perspectives and methods. Academic Press, London, United Kingdom.
30. Johnston WL, Dennis JW. 2012. The eggshell in the C. elegans oocyte-to-embryo transition. Genesis 50:333-349.
31. Samuelson J, Robbins P. 2011. A simple fibril and lectin model for cyst walls of Entamoeba and perhaps Giardia. Trends Parasitol. 27:17-22.
32. Remmal A, Achahbar S, Bouddine L, Chami N, Chami F. 2011. In vitro destruction of Eimeria oocysts by essential oils. Vet. Parasitol. 182: 121-126.
33. Mohanty D, Sankaranarayanan R, Gokhale RS. 2011. Fatty acyl-AMP ligases and polyketide synthases are unique enzymes of lipid biosynthetic machinery in Mycobacterium tuberculosis. Tuberculosis (Edinb) 91: 448-455.