Abstract
A newly isolated Pacific white shrimp (Litopenaeus vannamei) beta-actin promoter SbaP and its derivative compact construct SbaP (ENX) have recently been demonstrated to promote ectopic gene expression in vitro and in vivo. To further explore the potential transduction application, this newly isolated shrimp promoter SbaP was comparatively tested with cytomegalovirus (CMV), simian virus 40 (SV40), polyhedrin (Polh), and white spot syndrome virus immediate early gene 1 (WSSV ie1) four constitutive promoters and a beta-actin promoter (TbaP) from tilapia fish to characterize its promoting function in eight different cell lines. Luciferase quantitation assays revealed that SbaP can drive luciferase gene expression in all eight cell lines including sf21 (insect), PAC2 (zebrafish), EPC (carp), CHSE-214 (chinook salmon), GSTEF (green sea turtle), MS-1 (monk seal), 293T (human), and HeLa (human), but at different levels. Comparative analysis revealed that the promoting activity of SbaP was lower (≤10-fold) than CMV but higher (2–20 folds) than Polh in most of these cell lines tested. Whereas, SbaP mediated luciferase expression in sf21 cells was over 20-fold higher than CMV, SV40, Polh, and TbaP promoter. Compared to the SbaP, SbaP (ENX), which was constructed on the basis of SbaP by deletion of two “negative” regulatory elements, exhibited no significant change of promoting activity in EPC and PAC2 cells, but a 5 and 16 % lower promoting effect in 293T and HeLa cells, respectively. Additionally, a recombinant baculovirus was constructed under the control of SbaP (ENX), and efficient promoter activity of newly generated baculoviral vector was detected both in vitro of infected sf21 cells and in vivo of injected indicator shrimp. These results warrant the potential application of SbaP, particularly SbaP (ENX) in ectopic gene expression in future.
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References
Al-Dosari M, Zhang G, Knapp JE, Liu D (2006) Evaluation of viral and mammalian promoters for driving transgene expression in mouse liver. Biochem Biophys Res Commun 339:673–678
Arenal A, Pimentel R, Pimentel E, Martín L, Santiesteban D, Franco R, Aleström P (2008) Growth enhancement of shrimp (Litopenaeus schmitti) after transfer of tilapia growth hormone gene. Biotechnol Lett 30:845–851
Biberman Y, Meyuhas O (1997) Substitution of just five nucleotides at and around the transcription start site of rat beta-actin promoter is sufficient to render the resulting transcript a subject for translational control. FEBS Lett 405:333–336
Cayer MP et al (2007) Comparison of promoter activities for efficient expression into human B cells and haematopoietic progenitors with adenovirus Ad5/F35. J Immunol Methods 322:118–127
Du HH, Xu ZR, Wu XF, Li WF, Dai W (2006) Increased resistance to white spot syndrome virus in Procambarus clarkii by injection of envelope protein VP28 expressed using recombinant baculovirus. Aquaculture 260:39–43
Gao H, Wang Y, Li N, Peng WP, Sun Y, Tong GZ, Qiu HJ (2007) Efficient gene delivery into mammalian cells mediated by a recombinant baculovirus containing a whispovirus ie1 promoter, a novel shuttle promoter between insect cells and mammalian cells. J Biotechnol 131:138–143
Ge J, Jin L, Tang X, Gao D, An Q, Ping W (2014) Optimization of eGFP expression using a modified baculovirus expression system. J Biotechnol 173:41–46
Hu YC (2005) Baculovirus as a highly efficient expression vector in insect and mammalian cells. Acta Pharmacol Sin 26:405–416
Huang XD et al (2010) Shrimp NF-kappa B binds to the immediate-early gene ie1 promoter of white spot syndrome virus and upregulates its activity. Virology 406:176–180
Huang FT et al (2011) Efficient gene delivery into fish cells by an improved recombinant baculovirus. J Virol Methods 173:294–299
Hwang GL et al (2003) Isolation and characterisation of tilapia beta-actin promoter and comparison of its activity with carp beta-actin promoter. Biochim Biophys Acta 1625:11–18
Jha RK, Xu ZR, Shen J, Bai SJ, Sun JY, Li WF (2006) The efficacy of recombinant vaccines against white spot syndrome virus in Procambarus clarkii. Immunol Lett 105:68–76
Kawamoto T et al (1988) Identification of the human beta-actin enhancer and its binding factor. Mol Cell Biol 8:267–272
Khimmakthong U, Deachamag P, Phongdara A, Chotigeat W (2011) Stimulating the immune response of Litopenaeus vannamei using the phagocytosis activating protein (PAP) gene. Fish Shellfish Immunol 31:415–422
Kono T, Sonoda K, Kitao Y, Mekata T, Itami T, Sakai M (2009) The expression analysis of innate immune-related genes in Kuruma shrimp Penaeus japonicus after DNA vaccination against Penaeid rod-shaped DNA virus. Fish Pathol 44:94–97
Laimins LA, Khoury G, Gorman C, Howard B, Gruss P (1982) Host-specific activation of transcription by tandem repeats from simian virus 40 and Moloney murine sarcoma virus. Proc Natl Acad Sci U S A 79:6453–6457
Lanford RE, Luckow V, Kennedy RC, Dreesman GR, Notvall L, Summers MD (1989) Expression and characterization of hepatitis B virus surface antigen polypeptides in insect cells with a baculovirus expression system. J Virol 63:1549–1557
Li F, Ke W, Yan XM, Xu LM (2011) Gene transfection and expression in the primary culture of crayfish hemocytes. Fish Shellfish Immunol 31:161–163
Li S, Zhang QN, Zhang XT, Zheng XY, Lv YF, Hao ZM (2014) Cytomegalovirus immediate-early promoter efficiently drives heterogeneous gene expression in Spodoptera frugiperda (Sf9) insect cells. Cell Mol Biol 60:6–11
Liang C-Y, Wang H, Li T, Hu Z, Chen X (2003) High efficiency gene transfer into mammalian kidney cells using baculovirus vectors. Arch Virol 149:51–60
Lin YH, Lee LH, Shih WL, Hu YC, Liu HJ (2008) Baculovirus surface display of sigmaC and sigmaB proteins of avian reovirus and immunogenicity of the displayed proteins in a mouse model. Vaccine 26:6361–6367
Liu WJ, Chang YS, Wang CH, Kou GH, Lo CF (2005) Microarray and RT-PCR screening for white spot syndrome virus immediate-early genes in cycloheximide-treated shrimp. Virology 334:327–341
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(−Delta Delta C) method. Methods 25:402–408
Lu LQ, Wang H, Manopo I, Yu L, Kwang J (2005) Baculovirus-mediated promoter assay and transcriptional analysis of white spot syndrome virus orf427 gene. Virol J 2:71
Lu L, Yu L, Kwang J (2007) Baculovirus surface-displayed hemagglutinin of H5N1 influenza virus sustains its authentic cleavage, hemagglutination activity, and antigenicity. Biochem Biophys Res Commun 358:404–409
Madhan S, Prabakaran M, Kwang J (2010) Baculovirus as vaccine vectors. Curr Gene Ther 10:201–213
Mori H et al (1994) Expression of the Newcastle disease virus (NDV) fusion glycoprotein and vaccination against NDV challenge with a recombinant baculovirus. Avian Dis 38:772–777
Mu Y, Lan JF, Zhang XW, Wang XW, Zhao XF, Wang JX (2012) A vector that expresses VP28 of WSSV can protect red swamp crayfish from white spot disease. Dev Comp Immunol 36:442–449
Musthaq SS, Kwang J (2011) Oral vaccination of baculovirus-expressed VP28 displays enhanced protection against white spot syndrome virus in Penaeus monodon. PLoS One 6:e26428
Musthaq SS, Madhan S, Hameed ASS, Kwang J (2009) Localization of VP28 on the baculovirus envelope and its immunogenicity against white spot syndrome virus in Penaeus monodon. Virology 391:315–324
Ng S-Y, Gunning P, Eddy R, Ponte P, Leavitt J, Shows T, Kedes L (1985) Evolution of the functional human beta-actin gene and its multi-pseudogene family: conservation of noncoding regions and chromosomal dispersion of pseudogenes. Mol Cell Biol 5:2720–2732
Pan Y, Zhao Q, Fang L, Luo R, Chen H, Xiao S (2009) Efficient gene delivery into mammalian cells by recombinant baculovirus containing a hybrid cytomegalovirus promoter/Semliki Forest virus replicon. J Gene Med 11:1030–1038
Paul A, Jardin BA, Kulamarva A, Malhotra M, Elias CB, Prakash S (2010) Recombinant baculovirus as a highly potent vector for gene therapy of human colorectal carcinoma: molecular cloning, expression, and in vitro characterization. Mol Biotechnol 45:129–139
Qin JY, Zhang L, Clift KL, Hulur I, Xiang AP, Ren BZ, Lahn BT (2010) Systematic comparison of constitutive promoters and the doxycycline-inducible promoter. PLoS One 5:e10611
Rajesh Kumar S, Ishaq Ahamed VP, Sarathi M, Nazeer Basha A, Sahul Hameed AS (2008) Immunological responses of Penaeus monodon to DNA vaccine and its efficacy to protect shrimp against white spot syndrome virus (WSSV). Fish Shellfish Immunol 24:467–478
Rout N, Kumar S, Jaganmohan S, Murugan V (2007) DNA vaccines encoding viral envelope proteins confer protective immunity against WSSV in black tiger shrimp. Vaccine 25:2778–2786
Sapkota A, Sapkota AR, Kucharski M, Burke J, McKenzie S, Walker P, Lawrence R (2008) Aquaculture practices and potential human health risks: current knowledge and future priorities. Environ Int 34:1215–1226
Shi YL, Soderlund M, Xiang JH, Lu YN (2015) Function and regulation domains of a newly isolated putative beta-actin promoter from pacific white shrimp. PLoS One 10:e0122262
Sun PS, Soderlund M, Venzon NC, Ye D, Lu Y (2007) Isolation and characterization of two actins of the pacific white shrimp, Litopenaeus vannamei. Mar Biol 151:2145–2151
Sun YM, Li FH, Chi YH, Xiang JH (2013) Enhanced resistance of marine shrimp Exopalamon carincauda Holthuis to WSSV by injecting live VP28-recombinant bacteria. Acta Oceanol Sin 32:52–58
Syed Musthaq SK, Kwang J (2014) Evolution of specific immunity in shrimp—a vaccination perspective against white spot syndrome virus. Dev Comp Immunol 46:279–290
Tseng F, Tsai H, Liao I, Song Y (2000) Introducing foreign DNA into tiger shrimp (Penaeusmonodon) by electroporation. Theriogenology 54:1421–1432
Wang H-C, Chang Y-S, Kou G-H, Lo C-F (2004) White spot syndrome virus: molecular characterization of a major structural protein in a baculovirus expression system and shrimp hemocytes. Mar Biotechnol 6:S95–S99
Wang S et al (2007) Construction and immunogenicity of pseudotype baculovirus expressing GP5 and M protein of porcine reproductive and respiratory syndrome virus. Vaccine 25:8220–8227
Witteveldt J, Vlak JM, van Hulten MC (2004) Protection of Penaeus monodon against white spot syndrome virus using a WSSV subunit vaccine. Fish Shellfish Immunol 16:571–579
Wu C, Lu Y (2010) High-titre retroviral vector system for efficient gene delivery into human and mouse cells of haematopoietic and lymphocytic lineages. J Gen Virol 91:1909–1918
Xu ZL, Mizuguchi H, Ishii-Watabe A, Uchida E, Mayumi T, Hayakawa T (2001) Optimization of transcriptional regulatory elements for constructing plasmid vectors. Gene 272:149–156
Xu Z, Du H, Xu Y, Sun J, Shen J (2006) Crayfish Procambarus clarkii protected against white spot syndrome virus by oral administration of viral proteins expressed in silkworms. Aquaculture 253:179–183
Yu W et al (2012) The screening and functional study of proteins binding with the BmNPV polyhedrin promoter. Virol J 9:90
Zhao C, Zhang XJ, Li F, Huan P, Xiang JH (2013) Functional analysis of the promoter of the heat shock cognate 70 gene of the Pacific white shrimp, Litopenaeus vannamei. Fish Shellfish Immunol 34:397–401
Zhou X, Li B, Wang J, Yin H, Zhang Y (2010) The feasibility of using a baculovirus vector to deliver the sodium-iodide symporter gene as a reporter. Nucl Med Biol 37:299–308
Acknowledgments
Authors would like to thank Dr. Dustin Moss and Shaun Moss (Oceanic Institute) for providing experimental shrimp for this study. This study was supported in parts from University of Hawaii at Manoa OVCRGE grant (No. 399767), University of Hawaii Sea Grant (661160), and China National Hightech Research and Development Program (863 Program 2012AA10A404). However, the funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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Shi, Y., Xiang, J., Zhou, G. et al. The Pacific White Shrimp β-actin Promoter: Functional Properties and the Potential Application for Transduction System Using Recombinant Baculovirus. Mar Biotechnol 18, 349–358 (2016). https://doi.org/10.1007/s10126-016-9700-1
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DOI: https://doi.org/10.1007/s10126-016-9700-1