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Functional analysis of a survivin-like gene in Bombyx mori

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Abstract

The survivin (svv) gene is a newly discovered member of the inhibitors of apoptosis gene family. In recent years, svv has been confirmed to have an anti-apoptosis function and to play a critical role in cell division. We identified a survivin-like gene in the silkworm, Bombyx mori (Bm-svv). In this study, to gain insight into its function, a baculovirus expression system was used to express the Bm-svv gene in insect cell lines. The recombinant viruses were then used as a vector to transform insect cells, and cell activity was determined using the Cell Counting Kit-8 (CCK-8), which is usually employed for detecting mammalian cell number. The results indicated that the Bm-svv gene plays a role in the cell growth arrest or apoptosis induced by viruses. Furthermore, the CCK-8 kit is effective in determining the activity of insect cells.

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References

  • Adida C, Berrebi D, Peuchmaur M, Reyes-Mugica M, Altieri DC (1998) Anti-apoptosis gene, survivin, and prognosis of neuroblastoma. Lancet 351:882–883

    Article  CAS  Google Scholar 

  • Ambrosini G, Adida C, Altieri DC (1997) A novel anti-apoptosis gene, survivin, expressed in cancer and lymphoma. Nat Med 3:917–921

    Article  CAS  Google Scholar 

  • Ayres MD, Howard SC, Kuzio J, Lopez-Ferber M, Possee RD (1994) The complete DNA sequence of Autographa californica nuclear polyhedrosis virus. Virology 202:586–605

    Article  CAS  Google Scholar 

  • Chejanovsky N, Gershburg E (1995) The wild-type Autographa californica nuclear polyhedrosis virus induces apoptosis of Spodoptera littoralis cells. Virology 209:519–525

    Article  CAS  Google Scholar 

  • Colnaghi R, Connell CM, Barrett RM, Wheatley SP (2006) Separating the anti-apoptotic and mitotic roles of survivin. J Biol Chem 281:33450–33456

    Article  CAS  Google Scholar 

  • Deveraux QL, Reed JC (1999) IAP family proteins–suppressors of apoptosis. Genes Dev 13:239–252

    Article  CAS  Google Scholar 

  • Ding J, Huang S, Wu S, Zhao Y, Liang L, Yan M, Ge C, Yao J, Chen T, Wan D, Wang H, Gu J, Yao M, Li J, Tu H, He X (2010) Gain of miR-151 on chromosome 8q24.3 facilitates tumour cell migration and spreading through downregulating RhoGDIA. Nat Cell Biol 12:390–399

    Article  CAS  Google Scholar 

  • Emery VC (1992) Baculovirus expression vectors. Methods Mol Biol 8:309–318

    CAS  Google Scholar 

  • Fuchs LY, Woods MS, Weaver RF (1983) Viral transcription during Autographa californica nuclear polyhedrosis virus infection: a novel RNA polymerase induced in infected Spodoptera Frugiperda cells. J Virol 48:641–646

    CAS  Google Scholar 

  • Fukuda S, Pelus LM (2006) Survivin, a cancer target with an emerging role in normal adult tissues. Mol Cancer Ther 5:1087–1098

    Article  CAS  Google Scholar 

  • Glocker B, Hoopes RR Jr, Hodges L, Rohrmann GF (1993) In vitro transcription from baculovirus late gene promoters: accurate mRNA initiation by nuclear extracts prepared from infected Spodoptera frugiperda cells. J Virol 67:3771–3776

    CAS  Google Scholar 

  • Gomi S, Majima K, Maeda S (1999) Sequence analysis of the genome of Bombyx mori nucleopolyhedrovirus. J Gen Virol 80:1323–1337

    CAS  Google Scholar 

  • Guarino LA, Summers MD (1986) Functional mapping of a trans-activating gene required for expression of a baculovirus delayed-early gene. J Virol 57:563–571

    CAS  Google Scholar 

  • Habtemichael N, Wunsch D, Bier C, Tillmann S, Unruhe B, Frauenknecht K, Heinrich UR, Mann WJ, Stauber RH, Knauer SK (2010) Cloning and functional characterization of the guinea pig apoptosis inhibitor protein Survivin. Gene 469:9–17

    Article  CAS  Google Scholar 

  • Hink WF (1970) Established insect cell line from the cabbage looper Trichoplusia ni. Nature 226:466–467

    Article  CAS  Google Scholar 

  • Ito T, Shiraki K, Sugimoto K, Yamanaka T, Fujikawa K, Ito M, Takase K, Moriyama M, Kawano H, Hayashida M, Nakano T, Suzuki A (2000) Survivin promotes cell proliferation in human hepatocellular carcinoma. Hepatology 31:1080–1085

    Article  CAS  Google Scholar 

  • Jehle JA, Lange M, Wang H, Hu Z, Wang Y, Hauschild R (2006) Molecular identification and phylogenetic analysis of baculoviruses from Lepidoptera. Virology 346:180–193

    Article  CAS  Google Scholar 

  • Johnson EA, Svetlov SI, Wang KK, Hayes RL, Pineda JA (2005) Cell-specific DNA fragmentation may be attenuated by a survivin-dependent mechanism after traumatic brain injury in rats. Exp Brain Res 167:17–26

    Article  CAS  Google Scholar 

  • Katsuma S, Deng DX, Zhou CL, Iwanaga M, Noguchi Y, Kobayashi M, Maeda S (2000) Identification of novel residues involved in nuclear localization of a baculovirus polyhedrin protein. Virus Genes 21:233–240

    Article  CAS  Google Scholar 

  • Kawasaki H, Altieri DC, Lu CD, Toyoda M, Tenjo T, Tanigawa N (1998) Inhibition of apoptosis by survivin predicts shorter survival rates in colorectal cancer. Cancer Res 58:5071–5074

    CAS  Google Scholar 

  • Keerthivasan G, Liu H, Gump JM, Dowdy SF, Wickrema A, Crispino JD (2012) A novel role for survivin in erythroblast enucleation. Haematologica 97:1471–1479

    Article  CAS  Google Scholar 

  • Kindt N, Menzebach A, Van de Wouwer M, Betz I, De Vriese A, Conway EM (2008) Protective role of the inhibitor of apoptosis protein, survivin, in toxin-induced acute renal failure. FASEB J 22:510–521

    Article  CAS  Google Scholar 

  • Knauer SK, Bier C, Schlag P, Fritzmann J, Dietmaier W, Rodel F, Klein-Hitpass L, Kovacs AF, Doring C, Hansmann ML, Hofmann WK, Kunkel M, Brochhausen C, Engels K, Lippert BM, Mann W, Stauber RH (2007a) The survivin isoform survivin-3B is cytoprotective and can function as a chromosomal passenger complex protein. Cell Cycle 6:1502–1509

    CAS  Google Scholar 

  • Knauer SK, Kramer OH, Knosel T, Engels K, Rodel F, Kovacs AF, Dietmaier W, Klein-Hitpass L, Habtemichael N, Schweitzer A, Brieger J, Rodel C, Mann W, Petersen I, Heinzel T, Stauber RH (2007b) Nuclear export is essential for the tumor-promoting activity of survivin. FASEB J 21:207–216

    Article  CAS  Google Scholar 

  • Kondo A, Maeda S (1991) Host range expansion by recombination of the baculoviruses Bombyx mori nuclear polyhedrosis virus and Autographa californica nuclear polyhedrosis virus. J Virol 65:3625–3632

    CAS  Google Scholar 

  • Kost TA, Condreay JP, Jarvis DL (2005) Baculovirus as versatile vectors for protein expression in insect and mammalian cells. Nat Biotechnol 23:567–575

    Article  CAS  Google Scholar 

  • Kunz C, Focke F, Saito Y, Schuermann D, Lettieri T, Selfridge J, Schar P (2009) Base excision by thymine DNA glycosylase mediates DNA-directed cytotoxicity of 5-fluorouracil. PLoS Biol 7:e91

    Article  Google Scholar 

  • Lens SM, Vader G, Medema RH (2006) The case for Survivin as mitotic regulator. Curr Opin Cell Biol 18:616–622

    Article  CAS  Google Scholar 

  • Li F, Ambrosini G, Chu EY, Plescia J, Tognin S, Marchisio PC, Altieri DC (1998) Control of apoptosis and mitotic spindle checkpoint by survivin. Nature 396:580–584

    Article  CAS  Google Scholar 

  • Licari P, Bailey JE (1991) Factors influencing recombinant protein yields in an insect cell-bacuiovirus expression system: multiplicity of infection and intracellular protein degradation. Biotechnol Bioeng 37:238–246

    Article  CAS  Google Scholar 

  • Lu CD, Altieri DC, Tanigawa N (1998) Expression of a novel antiapoptosis gene, survivin, correlated with tumor cell apoptosis and p53 accumulation in gastric carcinomas. Cancer Res 58:1808–1812

    CAS  Google Scholar 

  • Luque T, Finch R, Crook N, O’Reilly DR, Winstanley D (2001) The complete sequence of the Cydia pomonella granulovirus genome. J Gen Virol 82:2531–2547

    CAS  Google Scholar 

  • Martin O, Croizier G (1997) Infection of a Spodoptera frugiperda cell line with Bombyx mori nucleopolyhedrovirus. Virus Res 47:179–185

    Article  CAS  Google Scholar 

  • Ruchaud S, Carmena M, Earnshaw WC (2007) Chromosomal passengers: conducting cell division. Nat Rev Mol Cell Biol 8:798–812

    Article  CAS  Google Scholar 

  • Sah NK, Khan Z, Khan GJ, Bisen PS (2006) Structural, functional and therapeutic biology of survivin. Cancer Lett 244:164–171

    Article  CAS  Google Scholar 

  • Smith GE, Summers MD, Fraser MJ (1983) Production of human beta interferon in insect cells infected with a baculovirus expression vector. Mol Cell Biol 3:2156–2165

    CAS  Google Scholar 

  • Stauber RH, Rabenhorst U, Rekik A, Engels K, Bier C, Knauer SK (2006) Nucleocytoplasmic shuttling and the biological activity of mouse survivin are regulated by an active nuclear export signal. Traffic 7:1461–1472

    Article  CAS  Google Scholar 

  • Su WJ, Wu Y, Wu HL, Zhu SY, Wang WB (2008) Expression of Bombyx mori nucleopolyhedrovirus ORF76 in permissive and non-permissive cell lines by a novel Bac-to-Bac/BmNPV baculovirus expression system. Pol J Microbiol 57:271–274

    CAS  Google Scholar 

  • Summers MD (2006) Milestones leading to the genetic engineering of baculoviruses as expression vector systems and viral pesticides. Adv Virus Res 68:3–73

    CAS  Google Scholar 

  • Sun C, Nettesheim D, Liu Z, Olejniczak ET (2005) Solution structure of human survivin and its binding interface with Smac/Diablo. Biochemistry 44:11–17

    Article  CAS  Google Scholar 

  • Swana HS, Grossman D, Anthony JN, Weiss RM, Altieri DC (1999) Tumor content of the antiapoptosis molecule survivin and recurrence of bladder cancer. N Engl J Med 341:452–453

    Article  CAS  Google Scholar 

  • Tamura K, Mawaribuchi S, Yoshimoto S, Shiba T, Takamatsu N, Ito M (2010) Tumor necrosis factor-related apoptosis-inducing ligand 1 (TRAIL1) enhances the transition of red blood cells from the larval to adult type during metamorphosis in Xenopus. Blood 115:850–859

    Article  CAS  Google Scholar 

  • Wang YY, Zhou GB, Yin T, Chen B, Shi JY, Liang WX, Jin XL, You JH, Yang G, Shen ZX, Chen J, Xiong SM, Chen GQ, Xu F, Liu YW, Chen Z, Chen SJ (2005) AML1-ETO and C-KIT mutation/overexpression in t(8;21) leukemia: implication in stepwise leukemogenesis and response to Gleevec. Proc Natl Acad Sci U S A 102:1104–1109

    Article  CAS  Google Scholar 

  • Wang XJ, Chen J, Lv ZB, Nie ZM, Wang D, Shen HD, Wang XD, Wu XF, Zhang YZ (2007) Expression and functional analysis of the cellular retinoic acid binding protein from silkworm pupae (Bombyx mori). J Cell Biochem 102:970–979

    Article  CAS  Google Scholar 

  • Weldon JE, Xiang L, Chertov O, Margulies I, Kreitman RJ, FitzGerald DJ, Pastan I (2009) A protease-resistant immunotoxin against CD22 with greatly increased activity against CLL and diminished animal toxicity. Blood 113:3792–3800

    Article  CAS  Google Scholar 

  • Zhang JY, Pan MH, Sun ZY, Huang SJ, Yu ZS, Liu D, Zhao DH, Lu C (2010) The genomic underpinnings of apoptosis in the silkworm Bombyx mori. BMC Genomics 11:611

    Article  Google Scholar 

  • Zhang LJ, Xue YQ, Yang C, Yang WH, Chen L, Zhang QJ, Qu TY, Huang S, Zhao LR, Wang XM, Duan WM (2012) Human albumin prevents 6-hydroxydopamine-induced loss of tyrosine hydroxylase in in vitro and in vivo. PLoS One 7:e41226

    Article  CAS  Google Scholar 

  • Zhou X, Dai LL, Jia LP, Zheng YY, Wang WB (2005) Study on the inhibitive effect of Astragalus Injection solution on hepatic fibrosis in rats. Zhonghua Gan Zang Bing Za Zhi 13:575–578

    Google Scholar 

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Acknowledgments

We thank Professor Jiang Zhu from Soochow University for providing the Spli cells.

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There is no conflict of interest in this paper.

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Correspondence to Wenbing Wang.

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Tang, H., Wu, Y., Wu, H. et al. Functional analysis of a survivin-like gene in Bombyx mori. Cytotechnology 66, 181–191 (2014). https://doi.org/10.1007/s10616-013-9551-9

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