Skip to main content
SpringerLink
Log in

Microarray analysis of the gene expression profile in the midgut of silkworm infected with cytoplasmic polyhedrosis virus

  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

In order to obtain an overall view on silkworm response to Bombyx mori cytoplasmic polyhedrosis virus (BmCPV) infection, a microarray system comprising 22,987 oligonucluotide 70-mer probes was employed to compare differentially expressed genes in the midguts of BmCPV-infected and normal silkworm larvae. At 72 h post-inoculation, 258 genes exhibited at least 2.0-fold differences in expression level. Out of these, 135 genes were up-regulated, while 123 genes were down-regulated. According to gene ontology (GO), 140 genes were classified into GO categories. Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis indicates that 35 genes were involved in 10 significant (P < 0.05) KEGG pathways. The expressions of genes related to valine, leucine, and isoleucine degradation, retinol metabolism, and vitamin B6 metabolism were all down-regulated. The expressions of genes involved in ribosome and proteasome pathway were all up-regulated. Quantitative real-time polymerase chain reaction was performed to validate the expression patterns of 13 selected genes of interest. The results suggest that BmCPV infection resulted in the disturbance of protein and amino acid metabolism and a series of major physiological and pathological changes in silkworm. Our results provide new insights into the molecular mechanism of BmCPV infection and host cell response.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Zhou ZH, Zhang H, Jakana J, Lu XY, Zhang JQ (2003) Cytoplasmic polyhedrosis virus structure at 8 Å by electron cryomicroscopy structural basis of capsid stability and mRNA processing regulation. Structure 11:651–663

    Article  CAS  PubMed  Google Scholar 

  2. Hill CL, Booth TF, Stuart DI, Mertens PPC (1999) Lipofectin increases the specific activity of cypovirus particles for cultured insect cells. J Virol Methods 78:177–189

    Article  CAS  PubMed  Google Scholar 

  3. Rubinstein R, Harley EH, Losman M, Lutton D (1976) The nucleic acids of viruses infecting Heliothis armigera. Virology 69:323–326

    Article  CAS  PubMed  Google Scholar 

  4. Kawase S, Kawamori I (1968) Chromatographic studies on RNA synthesis in the midgut of the silkworm, Bombyx mori, infected with a cytoplasmic-polyhedrosis virus. J Invertebr Pathol 12:395–404

    Article  CAS  PubMed  Google Scholar 

  5. Kawase S, Furusawa T (1971) Effect of actinomycin D on RNA synthesis in the midguts of healthy and CPV-infected silkworms. J Invertebr Pathol 18:33–39

    Article  CAS  PubMed  Google Scholar 

  6. Magnoler A (1974) Effects of a cytoplasmic polyhedrosis on larval and postlarval stages of the gypsy moth, Porthetria dispar. J Invertebr Pathol 23:263–274

    Article  CAS  PubMed  Google Scholar 

  7. Sikorowski PP, Lawrence AM (1994) Heliothis cytoplasmic polyhedrosis virus and its effect upon microbial contaminant-free Heliothis virescens. J Inverterb Pathol 63:56–62

    Article  Google Scholar 

  8. Sikorowski PP, Thompson AC (1979) Effects of cytoplasmic polyhedrosis virus on diapausing Heliothis virescens. J Inverterb Pathol 33:66–70

    Article  Google Scholar 

  9. Tanaka H, Sagisaka A, Fujita K, Kaneko Y, Imanishi S, Yamakawa M (2009) Lipopolysaccharide elicits expression of immune-related genes in the silkworm, Bombyx mori. Insect Mol Biol 18:71–75

    Article  CAS  PubMed  Google Scholar 

  10. Yun EY, Lee JK, Kwon OY, Hwang JS, Kim I, Kang SW, Lee WJ, Ding JL, You KH, Goo TW (2009) Bombyx mori transferrin: genomic structure, expression and antimicrobial activity of recombinant protein. Dev Comp Immunol 33:1064–1069

    Article  CAS  PubMed  Google Scholar 

  11. Cheng TC, Zhang YL, Liu C, Xu PZ, Gao ZH, Xia QY, Xiang ZH (2008) Identification and analysis of Toll-related genes in the domesticated silkworm, Bombyx mori. Dev Comp Immunol 32:464–475

    Article  CAS  PubMed  Google Scholar 

  12. Thompson GJ, Kucharski R, Maleszka R, Oldroyd BP (2008) Genome-wide analysis of genes related to ovary activation in worker honey bees Insect. Mol Biol 17:657–665

    CAS  Google Scholar 

  13. Liu WM, Laux H, Henry JY, Bolton TB, Dalgleish AG, Galustian C (2009) A microarray study of altered gene expression in colorectal cancer cells after treatment with immunomodulatory drugs: differences in action in vivo and in vitro. Mol Biol Rep 37:1801–1814

    Google Scholar 

  14. Luo Y, Lv GL, Wu WT, Chen SN, Cheng ZQ (2010) Analysis of genome expression in the response of Oryza granulata to Xanthomonas oryzae pv oryzae. Mol Biol Rep 37:875–892

    Article  CAS  PubMed  Google Scholar 

  15. Sun W, Margam VM, Sun L, Buczkowski G, Bennett GW, Schemerhorn B, Muir WM, Pittendrigh BR (2006) Genome-wide analysis of phenobarbital-inducible genes in Drosophila melanogaster insect. Mol Biol 15:455–464

    CAS  Google Scholar 

  16. Noji T, Ote M, Takeda M, Mita K, Shimada T, Kawasaki H (2003) Isolation and comparison of different ecdysone-responsive cuticle protein genes in wing discs of Bombyx mori. Insect Biochem Mol Biol 33:671–679

    Article  CAS  PubMed  Google Scholar 

  17. Huang FF, Chai CL, Zhang Z, Liu ZH, Dai FY, Lu C, Xiang ZH (2008) The UDP-glucosytransferase multigene family in Bombyx mori. BMC Genomics 27:563

    Article  Google Scholar 

  18. Duan J, Xia Q, Cheng D, Zha X, Zhao P, Xiang Z (2008) Species-specific expansion of C2H2 zinc-finger genes and their expression profiles in silkworm, Bombyx mori. Insect Biochem Mol Biol 38:1121–1129

    Article  CAS  PubMed  Google Scholar 

  19. He PA, Nie Z, Chen J, Chen J, Lv Z, Sheng Q, Zhou S, Gao X, Kong L, Wu X, Jin Y, Zhang Y (2008) Identification and characteristics of microRNAs from Bombyx mori. BMC Genomics 28:248

    Article  Google Scholar 

  20. Zhang Y, Zhou X, Ge X, Jiang J, Li M, Jia S, Yang X, Kan Y, Miao X, Zhao G, Li F, Huang Y (2009) Insect-specific microRNA involved in the development of the silkworm Bombyx mori. PLoS One 4:e4677

    Article  PubMed  Google Scholar 

  21. Xia Q, Cheng D, Duan J, Wang G, Cheng T, Zha X, Liu C, Zhao P, Dai F, Zhang Z, He N, Zhang L, Xiang Z (2007) Microarray-based gene expression profiles in multiple tissues of the domesticated silkworm, Bombyx mori. Genome Biol 8:162

    Article  Google Scholar 

  22. Tusher V, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to transcriptional responses to ionizing radiation. Proc Natl Acad Sci USA 98:5116–5121

    Article  CAS  PubMed  Google Scholar 

  23. Liew KJ, Chow VT (2006) Microarray and real-time RT-PCR analyses of a novel set of differentially expressed human genes in ECV304 endothelial-like cells infected with dengue virus type 2. J Virol Methods 131:47–57

    Article  CAS  PubMed  Google Scholar 

  24. Zheng J, Zhou XH, Zhang WM, Liu WT (2006) Ribosomal protein S24 gene differential depression in gastric cancer and its premalignant lesions. Carcinog, Teratog and Mutagen (Chinese) 18:306–310

    CAS  Google Scholar 

  25. Campbell CL, Wilson WC (2002) Differentially expressed midgut transcripts in Culicoides sonorensis (Diptera:Ceratopgonidae) following Orbivirus (Reoviridae) oral feeding. Insect Mol Biol 11:595–604

    Article  CAS  PubMed  Google Scholar 

  26. Dai MS, Arnold H, Sun XX, Sears R, Lu H (2007) Inhibition of c-Myc activity by ribosomal protein L11. EMBO J 26:3332–3345

    Article  CAS  PubMed  Google Scholar 

  27. Peters JM, Franke WW, Kleinschmidt JA (1994) Distinct 19 S and 20 S subcomplexes of the 26 S proteasome and their distribution in the nucleus and the cytoplasm. J Biol Chem 269:7709–7718

    CAS  PubMed  Google Scholar 

  28. William HM, Keisuke SI, Randi S, Milena P, Frank P (2003) The role of the ubiquitin/proteasome system in cellular responses to radiation. Oncogene 22:5755–5773

    Article  Google Scholar 

  29. Haas AL, Siepmann TJ (1997) Pathways of ubiquitin conjugation. FASEB J 11:1257–1268

    CAS  PubMed  Google Scholar 

  30. Narayan K (2004) Insect defence: its impact on microbial control of insect pests. Curr Sci 86:800–814

    Google Scholar 

  31. Clarke TE, Clem RJ (2002) Lack of involvement of haemocytes in the establishment and spread of infection in Spodoptera frugiperda larvae infected with the baculovirus Autographa californica M nucleopolyhedrovirus by intrahaemocoelic injection. J Gen Virol 83:1565–1572

    CAS  PubMed  Google Scholar 

  32. Yao HP, Wu XF, Gokulamma K (2006) Antiviral activity in the mulberry silkworm, Bombyx mori. J Zhejiang Univ Sci A (China) 7(Suppl II):350–356

    Article  Google Scholar 

  33. Bell MR, Kanavel RF (1976) Effect of dose of cytoplasmic polyhedrosis virus on infection, mortality, development rate, and larval and pupal weights of the pink bollworm. J Invertebr Pathol 28:121–126

    Article  Google Scholar 

  34. Rubinstein R (1983) Characterization of the proteins and serological relationships of cytoplasmic polyhedrosis virus of Heliothis armigera. J Inverterb Pathol 42:292–294

    Article  CAS  Google Scholar 

  35. Le Floc’h N, Melchior D, Obled C (2004) Modifications of protein and amino acid metabolism during inflammation and immune system activation. Livest Prod Sci 87:37–45

    Google Scholar 

  36. Kanost MR (1999) Serine proteinase inhibitors in arthropod immunity. Dev Comp Immunol 23:291–301

    Article  CAS  PubMed  Google Scholar 

  37. Ahmad ST, Sweeney ST, Lee JA, Sweeney NT, Gao FB (2009) Genetic screen identifies serpin5 as a regulator of the toll pathway and CHMP2B toxicity associated with frontotemporal dementia. Proc Natl Acad Sci USA 106:12168–12173

    Article  PubMed  Google Scholar 

  38. Tanaka H, Ishibashi J, Fujita K, Nakajima Y, Sagisaka A, Tomimoto K, Suzuki N, Yoshiyama M, Kaneko Y, Iwasaki T, Sunagawa T, Yamaji K, Asaoka A, Mita K, Yamakawa M (2008) A genome-wide analysis of genes and gene families involved in innate immunity of Bombyx mori. Insect Biochem Mol Biol 38:1087–1110

    Article  CAS  PubMed  Google Scholar 

  39. Bao YY, Tang XD, Lv ZY, Wang XY, Tian CH, Xu YP, Zhang CX (2009) Gene expression profiling of resistant and susceptible Bombyx mori strains reveals nucleopolyhedrovirus-associated variations in host gene transcript levels. Genomics 94:138–145

    Article  CAS  PubMed  Google Scholar 

  40. Ponnuvel KM, Nakazawa H, Furukawa S, Asaoka A, Ishibashi J, Tanaka H, Yamakawa M (2003) A lipase isolated from the silkworm shows antiviral activity against NPV. J Virol 77:10725–10729

    Article  CAS  PubMed  Google Scholar 

  41. Isaacs CE, Litov RE, Marie P, Thormar H (1992) Addition of lipases to infant formulas produces antiviral and antibacterial activity. J Nutr Biochem 3:304–308

    Article  CAS  Google Scholar 

  42. Wallin RPA, Lundqvist A, Moré SH, Bonin A, Kiessling R, Ljunggren H (2002) Heat-shock proteins as activators of the innate immune system. Trends Immunol 23:130–135

    Article  CAS  PubMed  Google Scholar 

  43. George J, Afek A, Gilburd B, Shoenfeld Y, Harats D (2001) Cellular and humoral immune responses to heat shock protein 65 are both involved in promoting fatty-streak formation in LDL-receptor deficient mice. J Am Coll Cardiol 38:900–905

    Article  CAS  PubMed  Google Scholar 

  44. Tezel G, Yang JJ, Wax MB (2004) Heat shock proteins, immunity and glaucoma. Brain Res Bull 62:473–480

    Article  CAS  PubMed  Google Scholar 

  45. Merril AH Jr, Nikolova-Karakashian M, Schmelz EM, Morgan ET, Stewart J (1999) Regulation of cytochrome P450 expression by sphingolipids. Chem Phys Lipids 102:131–139

    Article  PubMed  Google Scholar 

  46. Ai J, Yu Q, Cheng T, Dai F, Zhang X, Zhu Y, Xiang Z (2010) Characterization of multiple CYP9A genes in the silkworm, Bombyx mori. Mol Biol Rep 37:1657–1664

    Article  CAS  PubMed  Google Scholar 

  47. Guengerich FP (2008) Cytochrome p450 and chemical toxicology. Chem Res Toxicol 21:70–83

    Article  CAS  PubMed  Google Scholar 

  48. Shen B, Dong HQ, Tian HS, Ma L, Li XL, Wu GL, Zhu CL (2003) Cytochrome P450 genes expressed in the deltamethrin-susceptible and -resistant strains of Culex pipiens pallens. Pestic Biochem Physiol 75:19–26

    Article  CAS  Google Scholar 

  49. Juri Ayub M, Levin MJ, Aguilar CF (2001) Overexpression and refolding of the hydrophobic ribosomal P0 protein from Trypanosoma cruzi: a component of the P1/P2/P0 complex. Protein Expr Purif 22:225–233

    Article  CAS  PubMed  Google Scholar 

  50. Santos C, Ballesta JPG (1994) Ribosomal protein P0, contrary to phosphoproteins P1 and P2, is required for ribosome activity and Saccharomyces cerevisiae viability. J Biol Chem 269:15689–15696

    CAS  PubMed  Google Scholar 

  51. Gomez-Lorenzo MG, Garcia-Bustos JF (1998) Ribosomal P-protein stalk function is targeted by sordarin antifungals. J Biol Chem 273:25041–25044

    Article  CAS  PubMed  Google Scholar 

  52. Justice MC, Ku T, Hsu MJ, Carniol K, Schmatz D, Nielsen J (1999) Mutations in ribosomal L10e confer resistance to the fungal specific eukaryotic elongation factor 2 inhibitor sordarin. J Biol Chem 274:4869–4875

    Article  CAS  PubMed  Google Scholar 

  53. Bei R, Masuelli L, Trono P, Orvietani PL, Losito S, Marzocchella L, Vitolo D, Albonici L, Mrozek MA, Di Gennaro E, Lista F, Faggioni G, Ionna F, Binaglia L, Manzari V, Budillon A, Modesti A (2007) The ribosomal P0 protein induces a spontaneous immune response in patients with head and neck advanced stage carcinoma that is not dependent on its overexpression in carcinomas. Int J Oncol 31:1301–1308

    CAS  PubMed  Google Scholar 

  54. Cygler M, Schrag JD, Sussman JL, Harel M, Silman L, Gentry MK, Doctor BP (1993) Relationship between sequence conservation and three-dimensional structure in a large family of esterases, lipases, and related proteins. Protein Sci 2:366–382

    Article  CAS  PubMed  Google Scholar 

  55. Satoh T, Hosokawa M (2006) Structure, function and regulation of carboxylesterases. Chem Biol Interact 162:195–211

    Article  CAS  PubMed  Google Scholar 

  56. Cao CW, Zhang J, Gao XW, Liang P, Guo HL (2008) Overexpression of carboxylesterase gene associated with organophosphorous insecticide resistance in cotton aphids, Aphis gossypii (Glover). Pestic Biochem Physiol 90:175–180

    Article  CAS  Google Scholar 

  57. Gao GT, Cheng KP, Yao Q, Chen HQ, Wang LL, Xu JP, Zhao Y, Wang YJ (2007) A study on the activity of carboxylesterase and the differential expression of its gene in the midguts of Bombyx mori resistant to BmDNV-Z. Agric Sci Chin 6:1018–1026

    CAS  Google Scholar 

  58. Ngoka LC (2008) Dramatic down-regulation of oxidoreductases in human hepatocellular carcinoma hepG2 cells: proteomics and gene ontology unveiling new frontiers in cancer enzymology. Proteome Sci 6:29

    Article  PubMed  Google Scholar 

  59. Sharma MR, Polavarapu R, Roseman D, Patel V, Eaton E, Kishor PB, Nanji AA (2008) Increased severity of alcoholic liver injury in female verses male rats: a microarray analysis. Exp Mol Pathol 84:46–58

    Article  CAS  PubMed  Google Scholar 

  60. Luo M, Liang XQ, Dang P, Holbrook CC, Bausher MG, Lee RD, Guo BZ (2005) Microarray-based screening of differentially expressed genes in peanut in response to Aspergillus parasiticus infection and drought stress. Plant Sci 169:695–703

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This project was supported by the National Natural Science Foundation of China (Grant No. 30972143).

Author information

Authors and Affiliations

  1. School of Biotechnology and Environmental Engineering, Jiangsu University of Science and Technology, Zhenjiang, 212018, China

    Ping Wu, Xiu Wang, Yun-Feng Jiang & Xi-Jie Guo

  2. Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture of The People’s Republic of China, Sericultural Research Institute, Chinese Academy of Agricultural Sciences, Zhenjiang, 212018, China

    Ping Wu, Guang-xing Qin, Ting Liu, Mu-Wang Li & Xi-Jie Guo

Authors
  1. Ping Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiu Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Guang-xing Qin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ting Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yun-Feng Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mu-Wang Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xi-Jie Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xi-Jie Guo.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 381 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wu, P., Wang, X., Qin, Gx. et al. Microarray analysis of the gene expression profile in the midgut of silkworm infected with cytoplasmic polyhedrosis virus. Mol Biol Rep 38, 333–341 (2011). https://doi.org/10.1007/s11033-010-0112-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-010-0112-4

Keywords

Search

Navigation