The cryptosporidium parvum transcriptome during in vitro development

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Mauzy, Mary J ^a   Enomoto, Shinichiro ^a   Lancto, Cheryl A ^a   Abrahamsen, Mitchell S ^a   Rutherford, Mark S ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTOZOAL RNA; RNA 18S; TRANSCRIPTOME;

ARTICLE; CONTROLLED STUDY; CRYPTOSPORIDIOSIS; CRYPTOSPORIDIUM PARVUM; DEVELOPMENTAL GENE; DEVELOPMENTAL STAGE; DISEASE DURATION; EPITHELIUM CELL; GENE CLUSTER; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE IDENTIFICATION; HUMAN; HUMAN CELL; IN VITRO STUDY; INTRACELLULAR SPACE; NONHUMAN; PARASITE DEVELOPMENT; RNA TRANSLATION; TRANSCRIPTION REGULATION; CELL LINE; CLUSTER ANALYSIS; GENE EXPRESSION PROFILING; GENETICS; GENOME; GROWTH, DEVELOPMENT AND AGING; HOST PARASITE INTERACTION; INTESTINE; MEROZOITE; NUCLEOTIDE SEQUENCE; PARASITOLOGY; PATHOGENICITY; REAL TIME POLYMERASE CHAIN REACTION; SPOROZOITE; TROPHOZOITE;

CRYPTOSPORIDIUM PARVUM;

BASE SEQUENCE; CELL LINE; CLUSTER ANALYSIS; CRYPTOSPORIDIOSIS; CRYPTOSPORIDIUM PARVUM; EPITHELIAL CELLS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOME, PROTOZOAN; HOST-PARASITE INTERACTIONS; HUMANS; INTESTINES; MEROZOITES; REAL-TIME POLYMERASE CHAIN REACTION; RNA, PROTOZOAN; RNA, RIBOSOMAL, 18S; SPOROZOITES; TRANSCRIPTOME; TROPHOZOITES;

EID: 84858197464     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0031715     Document Type: Article

References (72)

1. Frost FJ, Muller TB, Calderon RL, Craun GF, (2004) Analysis of serological responses to Cryptosporidium antigen among NHANES III participants. Ann Epidemiol 14: 473-478.
2. Centers for Disease Control and Prevention (2010) Cryptosporidiosis surveillance-united states, 2006-2008 and giardiasis surveillance- United States, 2006-2008. MMWR 59 (No. SS-6): 1-12.
3. Chappell CL, Okhuysen PC, Langer-Curry R, Widmer G, Akiyoshi DE, et al. (2006) Cryptosporidium hominis: Experimental challenge of healthy adults. Am J Trop Med Hyg 75: 851-857.
4. Thompson RC, Olson ME, Zhu G, Enomoto S, Abrahamsen MS, et al. (2005) Cryptosporidium and cryptosporidiosis. Adv Parasitol 59: 77-158.
5. Xu P, Widmer G, Wang Y, Ozaki LS, Alves JM, et al. (2004) The genome of Cryptosporidium hominis. Nature 431: 1107-1112.
6. Abrahamsen MS, Templeton TJ, Enomoto S, Abrahante JE, Zhu G, et al. (2004) Complete genome sequence of the apicomplexan, Cryptosporidium parvum. Science 304: 441-445.
7. Abrahamsen MS, Schroeder AA, (1999) Characterization of intracellular Cryptosporidium parvum gene expression. Mol Biochem Parasitol 104: 141-146.
8. Cai X, Woods KM, Upton SJ, Zhu G, (2005) Application of quantitative real-time reverse transcription-PCR in assessing drug efficacy against the intracellular pathogen Cryptosporidium parvum in vitro. Antimicrob Agents Chemother 49: 4437-4442.
9. Sanderson SJ, Xia D, Prieto H, Yates J, Heiges M, et al. (2008) Determining the protein repertoire of Cryptosporidium parvum sporozoites. Proteomics 8: 1398-1414.
10. Snelling WJ, Lin Q, Moore JE, Millar BC, Tosini F, et al. (2007) Proteomics analysis and protein expression during sporozoite excystation of Cryptosporidium parvum (coccidia, apicomplexa). Mol Cell Proteomics 6: 346-355.
11. Strong WB, Nelson RG, (2000) Gene discovery in Cryptosporidium parvum: Expressed sequence tags and genome survey sequences. Contrib Microbiol 6: 92-115.
12. Yamagishi J, Wakaguri H, Sugano S, Kawano S, Fujisaki K, et al. (2011) Construction and analysis of full-length cDNA library of Cryptosporidium parvum. Parasitol Int 60: 199-202.
13. Upton SJ, Tilley M, Brillhart DB, (1995) Effects of select medium supplements on in vitro development of Cryptosporidium parvum in HCT-8 cells. J Clin Microbiol 33: 371-375.
14. Deng M, Templeton TJ, London NR, Bauer C, Schroeder AA, et al. (2002) Cryptosporidium parvum genes containing thrombospondin type 1 domains. Infect Immun 70: 6987-6995.
15. Kubista M, Andrade JM, Bengtsson M, Forootan A, Jonak J, et al. (2006) The real-time polymerase chain reaction. Mol Aspects Med 27: 95-125.
16. Stahlberg A, Hakansson J, Xian X, Semb H, Kubista M, (2004) Properties of the reverse transcription reaction in mRNA quantification. Clin Chem 50: 509-515.
17. Wakaguri H, Suzuki Y, Sasaki M, Sugano S, Watanabe J, (2009) Inconsistencies of genome annotations in apicomplexan parasites revealed by 5′-end-one-pass and full-length sequences of oligo-capped cDNAs. BMC Genomics 10: 312.
18. Schroeder AA, Brown AM, Abrahamsen MS, (1998) Identification and cloning of a developmentally regulated Cryptosporidium parvum gene by differential mRNA display PCR. Gene 216: 327-334.
19. Fontaine M, Guillot E, (2003) Study of 18S rRNA and rDNA stability by real-time RT-PCR in heat-inactivated Cryptosporidium parvum oocysts. FEMS Microbiol Lett 226: 237-243.
20. Jensen BC, Sivam D, Kifer CT, Myler PJ, Parsons M, (2009) Widespread variation in transcript abundance within and across developmental stages of Trypanosoma brucei. BMC Genomics 10: 482.
21. R Development Core Team (2009) R: A language and environment for statistical computing. 2.10.1. Available: http://www.R-project.org. Accessed July 1, 2011.
22. Maechler M, Rousseeuw P, Struyf A, Hubert M, Hornick K, (2011) Cluster analysis basics and extensions. R package version 1.14.1.
23. Eisen MB, Spellman PT, Brown PO, Botstein D, (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 95: 14863-14868.
24. Warnes GR, (2009) Includes R source code and/or documentation contributed by (in alphabetical order): In: Bolker B, Bonebakker L, Gentleman R, Huber W, Liaw A, Lumley T, Maechler M, Magnusson A, Moeller S, Schwartz M, Venables W, editors. (2009) Gplots: Various R programming tools for plotting data. 2.7.4. Available: http://CRAN.R-project.org/package=gplots via the Internet. Accessed July 1, 2011.
25. Liu J, Enomoto S, Lancto CA, Abrahamsen MS, Rutherford MS, (2008) Inhibition of apoptosis in Cryptosporidium parvum infected intestinal epithelial cells is dependent on survivin. Infect Immun 76: 3784-3792.
26. Templeton TJ, Iyer LM, Anantharaman V, Enomoto S, Abrahante JE, et al. (2004) Comparative analysis of apicomplexa and genomic diversity in eukaryotes. Genome Res 14: 1686-1695.
27. Kaufman L, Rousseeuw PJ, (1990) Finding groups in data: An introduction to cluster analysis New York John Wiley & Sons, Inc.
28. Borowski H, Thompson RC, Armstrong T, Clode PL, (2010) Morphological characterization of Cryptosporidium parvum life-cycle stages in an in vitro model system. Parasitology 137: 13-26.
29. Chatterjee A, Banerjee S, Steffen M, O'Connor RM, Ward HD, et al. (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.
30. Dubey JP, Speer CA, Fayer R, (1990) Cryptosporidiosis of man and animals Boca Raton, FL CRC Press.
31. SGD Project. Saccharomyces genome database (2010) Available: http://www.yeastgenome.org/cache/genomeSnapshot.html. Accessed January 20, 2011.
32. Joe A, Verdon R, Tzipori S, Keusch GT, Ward HD, (1998) Attachment of Cryptosporidium parvum sporozoites to human intestinal epithelial cells. Infect Immun 66: 3429-3432.
33. Jenkins MC, O'Brien C, Miska K, Schwarz RS, Karns J, et al. (2011) Gene expression during excystation of Cryptosporidium parvum oocysts. Parasitol Res 109: 509-513.
34. Behnke MS, Wootton JC, Lehmann MM, Radke JB, Lucas O, et al. (2010) Coordinated progression through two subtranscriptomes underlies the tachyzoite cycle of Toxoplasma gondii. PLoS One 5: e12354.
35. Gritzmacher CA, Reese RT, (1984) Protein and nucleic acid synthesis during synchronized growth of Plasmodium falciparum. J Bacteriol 160: 1165-1167.
36. de Rojas MO, Wasserman M, (1985) Temporal relationships on macromolecular synthesis during the asexual cell cycle of Plasmodium falciparum. Trans R Soc Trop Med Hyg 79: 792-796.
37. Le Roch KG, Zhou Y, Blair PL, Grainger M, Moch JK, et al. (2003) Discovery of gene function by expression profiling of the malaria parasite life cycle. Science 301: 1503-1508.
38. Putignani L, Possenti A, Cherchi S, Pozio E, Crisanti A, et al. (2008) The thrombospondin-related protein CpMIC1 (CpTSP8) belongs to the repertoire of micronemal proteins of Cryptosporidium parvum. Mol Biochem Parasitol 157: 98-101.
39. Tosini F, Agnoli A, Mele R, Gomez Morales MA, Pozio E, (2004) A new modular protein of Cryptosporidium parvum, with ricin B and LCCL domains, expressed in the sporozoite invasive stage. Mol Biochem Parasitol 134: 137-147.
40. Fayer R, (1997) Cryptosporidium and cryptosporidiosis Boca Raton, FL CRC Press.
41. Jorgensen P, Rupes I, Sharom JR, Schneper L, Broach JR, et al. (2004) A dynamic transcriptional network communicates growth potential to ribosome synthesis and critical cell size. Genes Dev 18: 2491-2505.
42. Bernstein KA, Bleichert F, Bean JM, Cross FR, Baserga SJ, (2007) Ribosome biogenesis is sensed at the start cell cycle checkpoint. Mol Biol Cell 18: 953-964.
43. Moore SA, (1988) Kinetic evidence for a critical rate of protein synthesis in the saccharomyces cerevisiae yeast cell cycle. J Biol Chem 263: 9674-9681.
44. Li JL, Cox LS, (2003) Characterisation of a sexual stage-specific gene encoding ORC1 homologue in the human malaria parasite Plasmodium falciparum. Parasitol Int 52 (1): 41-52.
45. Mehra P, Biswas AK, Gupta A, Gourinath S, Chitnis CE, et al. (2005) Expression and characterization of human malaria parasite Plasmodium falciparum origin recognition complex subunit 1. Biochem Biophys Res Commun 337: 955-966.
46. Chen F, Mackey AJ, Stoeckert CJ Jr, Roos DS, (2006) OrthoMCL-DB: Querying a comprehensive multi-species collection of ortholog groups 34 (Database issue) Nucleic Acids Res: D363-8.
47. Agop-Nersesian C, Naissant B, Ben Rached F, Rauch M, Kretzschmar A, et al. (2009) Rab11A-controlled assembly of the inner membrane complex is required for completion of apicomplexan cytokinesis. PLoS Pathog 5 (1): e1000270.
48. Maiorano D, Lutzmann M, Mechali M, (2006) MCM proteins and DNA replication. Curr Opin Cell Biol 18: 130-136.
49. Kolodner RD, Marsischky GT, (1999) Eukaryotic DNA mismatch repair. Curr Opin Genet Dev 9: 89-96.
50. Striepen B, Jordan CN, Reiff S, van Dooren GG, (2007) Building the perfect parasite: Cell division in apicomplexa. PLoS Pathog 3 (6): e78.
51. Gordon JL, Beatty WL, Sibley LD, (2008) A novel actin-related protein is associated with daughter cell formation in Toxoplasma gondii. Eukaryot Cell 7: 1500-1512.
52. Santos JM, Lebrun M, Daher W, Soldati D, Dubremetz JF, (2009) Apicomplexan cytoskeleton and motors: Key regulators in morphogenesis, cell division, transport and motility. Int J Parasitol 39: 153-162.
53. Hall N, Carlton J, (2005) Comparative genomics of malaria parasites. Curr Opin Genet Dev 15: 609-613.
54. Cleary MD, Singh U, Blader IJ, Brewer JL, Boothroyd JC, (2002) Toxoplasma gondii asexual development: Identification of developmentally regulated genes and distinct patterns of gene expression. Eukaryot Cell 1: 329-340.
55. Denton H, Roberts CW, Alexander J, Thong KW, Coombs GH, (1996) Enzymes of energy metabolism in the bradyzoites and tachyzoites of Toxoplasma gondii. FEMS Microbiol Lett 137: 103-108.
56. Yang S, Parmley SF, (1995) A bradyzoite stage-specifically expressed gene of Toxoplasma gondii encodes a polypeptide homologous to lactate dehydrogenase. Mol Biochem Parasitol 73: 291-294.
57. Deng M, Lancto CA, Abrahamsen MS, (2004) Cryptosporidium parvum regulation of human epithelial cell gene expression. Int J Parasitol 34: 73-82.
58. Xu T, Ping J, Yu Y, Yu F, Yu Y, et al. (2010) Revealing parasite influence in metabolic pathways in apicomplexa infected patients. BMC Bioinformatics 11 (Suppl 11): S13.
59. Hirano T, Mitchison TJ, (1994) A heterodimeric coiled-coil protein required for mitotic chromosome condensation in vitro. Cell 79: 449-458.
60. Sutani T, Yuasa T, Tomonaga T, Dohmae N, Takio K, et al. (1999) Fission yeast condensin complex: Essential roles of non-SMC subunits for condensation and Cdc2 phosphorylation of Cut3/SMC4. Genes Dev 13: 2271-2283.
61. Bell SP, Dutta A, (2002) DNA replication in eukaryotic cells. Annu Rev Biochem 71: 333-374.
62. Patterson S, Robert C, Whittle C, Chakrabarti R, Doerig C, et al. (2006) Pre-replication complex organization in the atypical DNA replication cycle of Plasmodium falciparum: Characterization of the mini-chromosome maintenance (MCM) complex formation. Mol Biochem Parasitol 145: 50-59 10.1016/j.molbiopara.2005.09.006.
63. Balaji S, Babu MM, Iyer LM, Aravind L, (2005) Discovery of the principal specific transcription factors of apicomplexa and their implication for the evolution of the AP2-integrase DNA binding domains. Nucleic Acids Res 33: 3994-4006.
64. Yuda M, Iwanaga S, Shigenobu S, Kato T, Kaneko I, (2010) Transcription factor AP2-sp and its target genes in malarial sporozoites. Mol Microbiol 75: 854-863 10.1111/j.1365-2958.2009.07005.x.
65. Heiges M, Wang H, Robinson E, Aurrecoechea C, Gao X, et al. (2006) CryptoDB: A Cryptosporidium bioinformatics resource update 34 (Database issue) Nucleic Acids Res: D419-22.
66. Duncker BP, Chesnokov IN, McConkey BJ, (2009) The origin recognition complex protein family. Genome Biol 10 (3): 214.
67. Dueber EC, Costa A, Corn JE, Bell SD, Berger JM, (2011) Molecular determinants of origin discrimination by Orc1 initiators in archaea. Nucleic Acids Res 39: 3621-3631.
68. Grainge I, Gaudier M, Schuwirth BS, Westcott SL, Sandall J, et al. (2006) Biochemical analysis of a DNA replication origin in the archaeon Aeropyrum pernix. J Mol Biol 363: 355-369
69. Bishop R, Shah T, Pelle R, Hoyle D, Pearson T, et al. (2005) Analysis of the transcriptome of the protozoan Theileria parva using MPSS reveals that the majority of genes are transcriptionally active in the schizont stage. Nucleic Acids Res 33: 5503-5511.
70. Bozdech Z, Llinas M, Pulliam BL, Wong ED, Zhu J, et al. (2003) The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum. PLoS Biol 1 (1): E5.
71. Behnke MS, Radke JB, Smith AT, Sullivan WJ Jr, White MW, (2008) The transcription of bradyzoite genes in Toxoplasma gondii is controlled by autonomous promoter elements. Mol Microbiol 68: 1502-1518.
72. Oliveros JC, (2007) VENNY. an interactive tool for comparing lists with venn diagrams. May 1, 2011.