Skip to main content

Advertisement

SpringerLink
Log in

The Pacific White Shrimp β-actin Promoter: Functional Properties and the Potential Application for Transduction System Using Recombinant Baculovirus

  • Original Article
  • Published:
Marine Biotechnology Aims and scope Submit manuscript

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.

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
Fig. 3
Fig. 4

Similar content being viewed by others

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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Hu YC (2005) Baculovirus as a highly efficient expression vector in insect and mammalian cells. Acta Pharmacol Sin 26:405–416

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Huang FT et al (2011) Efficient gene delivery into fish cells by an improved recombinant baculovirus. J Virol Methods 173:294–299

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Kawamoto T et al (1988) Identification of the human beta-actin enhancer and its binding factor. Mol Cell Biol 8:267–272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Madhan S, Prabakaran M, Kwang J (2010) Baculovirus as vaccine vectors. Curr Gene Ther 10:201–213

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Tseng F, Tsai H, Liao I, Song Y (2000) Introducing foreign DNA into tiger shrimp (Penaeusmonodon) by electroporation. Theriogenology 54:1421–1432

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Yu W et al (2012) The screening and functional study of proteins binding with the BmNPV polyhedrin promoter. Virol J 9:90

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

  1. Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, 266071, China

    Yingli Shi & Jianhai Xiang

  2. University of Chinese Academy of Sciences, Beijing, 100049, China

    Yingli Shi

  3. Department of Public Health Sciences, University of Hawaii at Manoa, Honolulu, HI, 96822, USA

    Yingli Shi, Guangzhou Zhou, Hsin-I Tong, Wen Kang, Si Sun & Yuanan Lu

  4. College of Bioengineering, Henan University of Technology, Zhengzhou, 450001, China

    Guangzhou Zhou

  5. Department of Human Nutrition, Food and Animal Sciences, University of Hawaii at Manoa, Honolulu, HI, 96822, USA

    Tetsuzan Benny Ron

Authors
  1. Yingli Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jianhai Xiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Guangzhou Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tetsuzan Benny Ron
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hsin-I Tong
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Wen Kang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Si Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yuanan Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Jianhai Xiang or Yuanan Lu.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-016-9700-1

Keywords

Search

Navigation