1DUMMY Genome-wide transcriptional response of silkworm (Bombyx mori) to infection by the microsporidian Nosema bombycis

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Ma, Zhengang ^a   Li, Chunfeng ^a   Pan, Guoqing ^a   Li, Zhihong ^a   Han, Bing ^a   Xu, Jinshan ^b   Lan, Xiqian ^a   Chen, Jie ^a   Yang, Donglin ^a   Chen, Quanmei ^a   Sang, Qi ^a   Ji, Xiaocun ^a   Li, Tian ^a   Long, Mengxian ^a   Zhou, Zeyang ^a,b  

^a SOUTHWEST UNIVERSITY   (China)

^b CHONGQING NORMAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

JUVENILE HORMONE; MELANIN; MONOPHENOL MONOOXYGENASE;

ANIMAL; ARTICLE; BACTERIAL SPORE; BIOSYNTHESIS; BOMBYX; CELLULAR IMMUNITY; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; GENETICS; GENOMICS; HUMORAL IMMUNITY; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MYCOSIS; NOSEMA; PHYSIOLOGY; SPECIES DIFFERENCE; TIME;

ANIMALS; BOMBYX; GENE EXPRESSION PROFILING; GENOMICS; IMMUNITY, CELLULAR; IMMUNITY, HUMORAL; JUVENILE HORMONES; MELANINS; MONOPHENOL MONOOXYGENASE; MYCOSES; NOSEMA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SPECIES SPECIFICITY; SPORES; TIME FACTORS; TRANSCRIPTION, GENETIC;

EID: 84893634012     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0084137     Document Type: Article

References (73)

1. Wittner M, Weiss LM (1999) The microsporidia and microsporidiosis. In: Becnel JJ, Andreadis GA, editors. Microsporidia in Insects. Washington, DC: American Society for Microbiology. 447-458.
2. Didier ES, Snowden KF, Shadduck JA (1998) Biology of microsporidian species infecting mammals. Advances in parasitology 40: 283-320. (Pubitemid 30411813)
3. Xu Y, Weiss LM (2005) The microsporidian polar tube: a highly specialised invasion organelle. Int J Parasitol 35: 941-953. (Pubitemid 41074072)
4. Bigliardi E, Sacchi L (2001) Cell biology and invasion of the microsporidia. Microbes Infect 3: 373-379. (Pubitemid 32441660)
5. Weidner E, Byrd W (1982) The microsporidian spore invasion tube. II. Role of calcium in the activation of invasion tube discharge. J Cell Biol 93: 970-975.
6. Li Z, Pan G, Li T, Huang W, Chen J, et al. (2012) SWP5, a spore wall protein, interacts with polar tube proteins in the parasitic microsporidian Nosema bombycis. Eukaryot Cell 11: 229-237.
7. Bouzahzah B, Nagajyothi F, Ghosh K, Takvorian PM, Cali A, et al. (2010) Interactions of Encephalitozoon cuniculi polar tube proteins. Infect Immun 78: 2745-2753.
8. Xu Y, Takvorian P, Cali A, Wang F, Zhang H, et al. (2006) Identification of a new spore wall protein from Encephalitozoon cuniculi. Infect Immun 74: 239-247. (Pubitemid 43023078)
9. 2+ suggests dependence of water influx upon membrane hydration and specific transmembrane pathways. J Eukaryot Microbiol 44: 109-116.
10. Li Y, Wu Z, Pan G, He W, Zhang R, et al. (2009) Identification of a novel spore wall protein (SWP26) from microsporidia Nosema bombycis. Int J Parasitol 39: 391-398.
11. Dang X, Pan G, Li T, Lin L, Ma Q, et al. (2012) Characterization of a subtilisin-like protease with apical localization from microsporidian Nosema bombycis. J Invertebr Pathol 112: 166-174.
12. Ellis J, Sinclair D, Morrison D, Al-Qassab S, Springett K, et al. (2010) Microarray analyses of mouse responses to infection by Neospora caninum identifies disease associated cellular pathways in the host response. Mol Biochem Parasit 174: 117-127.
13. Rosenblum EB, Poorten TJ, Settles M, Murdoch GK, Robert J, et al. (2009) Genome-wide transcriptional response of Silurana (Xenopus) tropicalis to infection with the deadly chytrid fungus. PloS one 4: e6494.
14. Yang YL, Buck GA, Widmer G (2010) Cell sorting-assisted microarray profiling of host cell response to Cryptosporidium parvum infection. Infect Immun 78: 1040-1048.
15. Dussaubat C, Brunet JL, Higes M, Colbourne JK, Lopez J, et al. (2012) Gut Pathology and Responses to the Microsporidium Nosema ceranae in the Honey Bee Apis mellifera. PloS one 7: e37017.
16. Pan G, Xu J, Li T, Xia Q, Liu S, et al. (2013) Comparative genomics of parasitic silkworm microsporidia reveal an association between genome expansion and host adaptation. BMC Genomics 14: 186.
17. Xia Q, Zhou Z, Lu C, Cheng D, Dai F, et al. (2004) A draft sequence for the genome of the domesticated silkworm (Bombyx mori). Science 306: 1937-1940. (Pubitemid 39627858)
18. Xia Q, Cheng D, Duan J, Wang G, Cheng T, et al. (2007) Microarray-based gene expression profiles in multiple tissues of the domesticated silkworm, Bombyx mori. Genome Biol 8: R162.
19. Huang L, Cheng T, Xu P, Cheng D, Fang T, et al. (2009) A genome-wide survey for host response of silkworm, Bombyx mori during pathogen Bacillus bombyseptieus infection. PloS one 4: e8098.
20. Liu H, Pan G, Song S, Xu J, Li T, et al. (2008) Multiple rDNA units distributed on all chromosomes of Nosema bombycis. J Invertebr Pathol 99: 235-238.
21. Gatehouse HS, Malone LA (1998) The ribosomal RNA gene region of Nosema apis (Microspora): DNA sequence for small and large subunit rRNA genes and evidence of a large tandem repeat unit size. J Invertebr Pathol 71: 97-105. (Pubitemid 128349171)
22. Yang YH, Dudoit S, Luu P, Lin DM, Peng V, et al. (2002) Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res 30: e15.
23. Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. P Natl Acad Sci USA 98: 5116-5121. (Pubitemid 32397092)
24. Wang F, Yang LR, Tang XD, Mo JC, Yang WJ, et al. (2006) The translational and transcriptional initiation sites of BmNPV lef-7 gene. Virus Genes 33: 351-357. (Pubitemid 44440193)
25. Riddiford LM (1994) Cellular and Molecular Actions of Juvenile Hormone I. General Considerations and Premetamorphic Actions. Adv Insect Physiol 24: 213-274.
26. Wyatt GR, Davey KG (1996) Cellular and molecular actions of juvenile hormone. II. Roles of juvenile hormone in adult insects. Adv Insect Physiol 26: 1-155.
27. Bede JC, Teal PEA, Goodman WG, Tobe SS (2001) Biosynthetic pathway of insect juvenile hormone III in cell suspension cultures of the sedge Cyperus iria. Plant Physiol 127: 584-593. (Pubitemid 32996760)
28. Shinoda T, Itoyama K (2003) Juvenile hormone acid methyltransferase: a key regulatory enzyme for insect metamorphosis. P Natl Acad Sci USA 100: 11986-11991. (Pubitemid 37271502)
29. Vieira CU, Bonetti AM, Simões ZLP, Maranhão AQ, Costa CS, et al. (2007) Farnesoic acid O-methyl transferase (FAMeT) isoforms: Conserved traits and gene expression patterns related to caste differentiation in the stingless bee, Melipona scutellaris. Arch Insect Biochem 67: 97-106. (Pubitemid 351220130)
30. Seleznev KV (2003) The role of microsporidia in the disturbance of the hormonal balance in the infected insects. Parazitologiia 37: 428-435.
31. Zhang QR, Xu WH, Chen FS, Li S (2005) Molecular and biochemical characterization of juvenile hormone epoxide hydrolase from the silkworm, Bombyx mori. Insect Biochem Molec 35: 153-164.
32. Finlayson LH, Walters VA (1957) Abnormal metamorphosis in saturniid moths infected by a microsporidian. Nature 180: 713-714.
33. Fisher FM, Sanborn RC (1964) Nosema as a source of juvenile hormone in parasitized insects. The Biological Bulletin 126: 235-252.
34. Zhou Y, Xiao Q, Zhang Z, He J, Zhang Y (2002) Foreign insect hormones stimulating the transcription of the ie-1 promoter of Bombyx mori nuclear polyhedrosis virus in vivo and in vitro. Biosci Biotech Bioch 66: 1488-1494. (Pubitemid 39246854)
35. Blalock JE (1984) The immune system as a sensory organ. J Immunol 132: 1067-1070.
36. Borghetti P, Saleri R, Mocchegiani E, Corradi A, Martelli P (2009) Infection, immunity and the neuroendocrine response. Vet Immunol Immunop 130: 141-162.
37. Flatt T, Heyland A, Rus F, Porpiglia E, Sherlock C, et al. (2008) Hormonal regulation of the humoral innate immune response in Drosophila melanogaster. J Exp Biol 211: 2712-2724.
38. Tian L, Guo E, Wang S, Liu S, Jiang RJ, et al. (2010) Developmental regulation of glycolysis by 20-hydroxyecdysone and juvenile hormone in fat body tissues of the silkworm, Bombyx mori. J Mol Cell Biol 2: 255-263.
39. Ogata H, Goto S, Sato K, Fujibuchi W, Bono H, et al. (1999) KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res 27: 29-34. (Pubitemid 29209394)
40. Neill JD, Ridpath JF (2003) Gene expression changes in BVDV2-infected MDBK cells. Biologicals 31: 97-102. (Pubitemid 36593343)
41. Freitak D, Ots I, Vanatoa A, Hörak P (2003) Immune response is energetically costly in white cabbage butterfly pupae. Proc. R. Soc. Lond. B 270: S220-S222. (Pubitemid 37430861)
42. Hetru C, Troxler L, Hoffmann JA (2003) Drosophila melanogaster antimicrobial defense. J Infect Dis 187: S327-S334. (Pubitemid 36724504)
43. Bulet P, Hetru C, Dimarcq JL, Hoffmann D (1999) Antimicrobial peptides in insects; structure and function. Dev Comp Immunol 23: 329-344. (Pubitemid 29309611)
44. Lemaitre B, Hoffmann J (2007) The host defense of Drosophila melanogaster. Annu Rev Immunol 25: 697-743. (Pubitemid 46697922)
45. Muniz CA, Jaillard D, Lemaitre B, Boccard F (2007) Erwinia carotovora Evf antagonizes the elimination of bacteria in the gut of Drosophila larvae. Cell Microbiol 9: 106-119. (Pubitemid 44910085)
46. Hinnebusch BJ, Rudolph AE, Cherepanov P, Dixon JE, Schwan TG, et al. (2002) Role of Yersinia murine toxin in survival of Yersinia pestis in the midgut of the flea vector. Science 296: 733-735. (Pubitemid 34442000)
47. Muniz CA, Jaillard D, Lemaitre B, Boccard F (2007) Erwinia carotovora Evf antagonizes the elimination of bacteria in the gut of Drosophila larvae. Cell Microbiol 9: 106-119. (Pubitemid 44910085)
48. Brey PT, Lee WJ, Yamakawa M, Koizumi Y, Perrot S, et al. (1993) Role of the integument in insect immunity: epicuticular abrasion and induction of cecropin synthesis in cuticular epithelial cells. P Natl Acad Sci USA 90: 6275-6279. (Pubitemid 23191498)
49. Hara S, Yamakawa M (1995) Moricin, a novel type of antibacterial peptide isolated from the silkworm, Bombyx mori. J Biol Chem 270: 29923-29927. (Pubitemid 26002154)
50. Yang W, Cheng T, Ye M, Deng X, Yi H, et al. (2011) Functional divergence among silkworm antimicrobial peptide paralogs by the activities of recombinant proteins and the induced expression profiles. PloS one 6: e18109.
51. Wang Y, Cheng T, Rayaprolu S, Zou Z, Xia Q, et al. (2007) Proteolytic activation of pro-spätzle is required for the induced transcription of antimicrobial peptide genes in lepidopteran insects. Dev Comp Immunol 31: 1002-1012. (Pubitemid 47095006)
52. Luo H, Dearolf CR (2001) The JAK/STAT pathway and Drosophila development. Bioessays 23: 1138-1147.
53. Agaisse H, Perrimon N (2004) The roles of JAK/STAT signaling in Drosophila immune responses. Immunol Rev 198: 72-82. (Pubitemid 38406936)
54. O'Shea JJ, Gadina M, Schreiber RD (2002) Cytokine Signaling in 2002-New Surprises in the Jak/Stat Pathway. Cell 109: S121-S131.
55. Grace MJ, Cutler D (2004) Pegylating IFNs at His-34 improves the in vitro antiviral activity through the JAK/STAT pathway. Antivir Chem Chemoth 15: 287-297. (Pubitemid 39656965)
56. Chaudhuri A, Yang B, Gendelman HE, Persidsky Y, Kanmogne GD (2008) STAT1 signaling modulates HIV-1-induced inflammatory responses and leukocyte transmigration across the blood-brain barrier. Blood 111: 2062-2072. (Pubitemid 351451518)
57. Lemaitre B, Hoffmann J (2007) The host defense of Drosophila melanogaster. Annu Rev Immunol 25: 697-743. (Pubitemid 46697922)
58. Chaimanee V, Chantawannakul P, Chen Y, Evans JD, Pettis JS (2012) Differential expression of immune genes of adult honey bee (Apis mellifera) after inoculated by Nosema ceranae. J Insect Physiol 58: 1090-1095.
59. Nappi AJ, Vass E (2006) Melanogenesis and the generation of cytotoxic molecules during insect cellular immune reactions. Pigm Cell Res 6: 117-126.
60. Ashida M (1990) The prophenoloxidase cascade in insect immunity. Res Immunol 141: 908-910.
61. Lavine MD, Strand MR (2002) Insect hemocytes and their role in immunity. Insect Biochem Molec 32: 1295-1309.
62. Takase H, Watanabe A, Yoshizawa Y, Kitami M, Sato R (2009) Identification and comparative analysis of three novel C-type lectins from the silkworm with functional implications in pathogen recognition. Dev Comp Immunol 33: 789-800.
63. Law RH, Zhang Q, McGowan S, Buckle AM, Silverman GA, et al. (2006) An overview of the serpin superfamily. Genome Biol 7: 216.
64. Bao Y, Xue J, Wu W, Wang Y, Lv Z, et al. (2011) An immune-induced Reeler protein is involved in the Bombyx mori melanization cascade. Insect Biochem Molec 41: 696-706.
65. Gliński Z, Jarosz J (1997) Molluscan immune defenses. Arch Immunol Ther Ex 45: 149.
66. Roxstróm-Lindquist K, Terenius O, Faye I (2004) Parasite-specific immune response in adult Drosophila melanogaster: a genomic study. Embo Rep 5: 207-212. (Pubitemid 38401203)
67. Huang L, Cheng T, Xu P, Duan J, Fang T, et al. (2009) Immunoglobulin superfamily is conserved but evolved rapidly and is active in the silkworm, Bombyx mori. Insect Mol Biol 18: 517-530.
68. Zouali M (2001) B cell tolerance to self in systemic autoimmunity. Arch Immunol Ther Ex 49: 361-366.
69. Watanabe A, Miyazawa S, Kitami M, Tabunoki H, Ueda K, et al. (2006) Characterization of a novel C-type lectin, Bombyx mori multibinding protein, from the B. mori hemolymph: mechanism of wide-range microorganism recognition and role in immunity. J Immunol 177: 4594-4604. (Pubitemid 44469791)
70. Herve C, Dabos P, Galaud J, Rouge P, Lescure B (1996) Characterization of an Arabidopsis thaliana Gene that Defines a New Class of Putative Plant Receptor Kinases with an Extracellular Lectin-like Domain. J Mol Biol 258: 778-788. (Pubitemid 26150880)
71. Nishiguchi M, Yoshida K, Sumizono T, Tazaki K (2002) A receptor-like protein kinase with a lectin-like domain from lombardy poplar: gene expression in response to wounding and characterization of phosphorylation activity. Mol Genet Genomics 267: 506-514. (Pubitemid 34671345)
72. Huang L (2010) A Genome-wide Analysis of the Silkworm Host Responses to Bacillus Bombyseptieus (Bb) and Other Pathogens (Ph.D Thesis), Chongqing: Southwest University. PP.43-72.
73. Tanaka H, Ishibashi J, Fujita K, Nakajima Y, Sagisaka A, et al. (2008) A genome-wide analysis of genes and gene families involved in innate immunity of Bombyx mori. Insect Biochem Molec 38: 1087-1110.