Advertisement

Transgenic Research

, Volume 19, Issue 5, pp 903–913 | Cite as

Impaired plant growth and development caused by human immunodeficiency virus type 1 Tat

  • Marni E. Cueno
  • Yurina Hibi
  • Kenichi Imai
  • Antonio C. Laurena
  • Takashi OkamotoEmail author
Brief Communication

Abstract

Previous attempts to express the human immunodeficiency virus 1 (HIV-1) Tat (trans-activator of transcription) protein in plants resulted in a number of physiological abnormalities, such as stunted growth and absence of seed formation, that could not be explained. In the study reported here, we expressed Tat in tomato and observed phenotypic abnormalities, including stunted growth, absence of root formation, chlorosis, and plant death, as a result of reduced cytokinin levels. These reduced levels were ascribed to a differentially expressed CKO35 in Tat-bombarded tomato. Of the two CKO isoforms that are naturally expressed in tomato, CKO43 and CKO37, only the expression of CKO37 was affected by Tat. Our analysis of the Tat confirmed that the Arg-rich and RGD motifs of Tat have functional relevance in tomato and that independent mutations at these motifs caused inhibition of the differentially expressed CKO isoform and the extracellular secretion of the Tat protein, respectively, in our Tat-bombarded tomato samples.

Keywords

Cytokinin Cytokinin oxidase HIV-1 Tat Tomato Transient expression 

Notes

Acknowledgments

This work was supported by the Ministries of Health, Labor and Welfare and Education, Culture, Sports, Science and Technology.

References

  1. Addo MM, Altfeld M, Rosenberg ES, Eldridge RL, Philips MN, Habeeb K, Khatri A, Brander C, Robbins GK, Mazzara GP, Goulder PJ, Walker BD (2001) The HIV-1 regulatory proteins Tat and Rev are frequently targeted by cytotoxic T lymphocytes derived from HIV-1-infected individuals. Proc Natl Acad Sci USA 98:1781–1786CrossRefPubMedGoogle Scholar
  2. Albini A, Benelli R, Giunciuglio D, Cai T, Mariani G, Ferrini S, Noonan DM (1998) Identification of a novel domain of HIV tat involved in monocyte chemotaxis. J Biol Chem 273:15895–15900CrossRefPubMedGoogle Scholar
  3. Brugiere N, Jiao S, Hantke S, Zinselmeier C, Roessler JA, Niu X, Jones RJ, Habben JE (2003) Cytokinin oxidase gene expression in maize is localized to the vasculature, and is induced by cytokinins, abscisic acid, and abiotic stress. Plant Physiol 132:1228–1240CrossRefPubMedGoogle Scholar
  4. Calnan BJ, Biancalana S, Hudson D, Frankel AD (1991) Analysis of arginine-rich peptides from the HIV Tat protein reveals unusual features of RNA-protein recognition. Genes Dev 5:201–210CrossRefPubMedGoogle Scholar
  5. Clark JP III, Sampair CS, Kofuji P, Nath A, Ding JM (2005) HIV protein, transactivator of transcription, alters circadian rhythms through the light entrainment pathway. Am J Physiol Regul Integr Comp Physiol 289:R656–R662PubMedGoogle Scholar
  6. Di Cola A, Robinson C (2005) Large-scale translocation reversal within the thylakoid Tat system in vivo. J Cell Biol 171:281–289CrossRefPubMedGoogle Scholar
  7. Evans DA, Sharp WR (1983) Single gene mutations in tomato plants regenerated from tissue culture. Science 221:949–951CrossRefPubMedGoogle Scholar
  8. Fisher AG, Ratner L, Mitsuya H, Marselle LM, Harper ME, Broder S, Gallo RC, Wong-Staal F (1986) Infectious mutants of HTLV-III with changes in the 3′ region and markedly reduced cytopathic effects. Science 233:655–659CrossRefPubMedGoogle Scholar
  9. Goldstein G, Tribbick G, Manson K (2001) Two B cell epitopes of HIV-1 Tat protein have limited antigenic polymorphism in geographically diverse HIV-1 strains. Vaccine 19:1738–1746CrossRefPubMedGoogle Scholar
  10. Imai K, Nakata K, Kawai K, Hamano T, Mei N, Kasai H, Okamoto T (2005) Induction of OGG1 gene expression by HIV-1 Tat. J Biol Chem 280:26701–26713CrossRefPubMedGoogle Scholar
  11. Kakimoto T (2003) Perception and signal transduction of cytokinins. Annu Rev Plant Biol 54:605–627CrossRefPubMedGoogle Scholar
  12. Kanazawa S, Okamoto T, Peterlin BM (2000) Tat competes with CIITA for the binding to P-TEFb and blocks the expression of MHC class II genes in HIV infection. Immunity 12:61–70CrossRefPubMedGoogle Scholar
  13. Karasev AV, Foulke S, Wellens C, Rich A, Shon KJ, Zwierzynski I, Hone D, Koprowski H, Reitz M (2005) Plant based HIV-1 vaccine candidate: Tat protein produced in spinach. Vaccine 23:1875–1880CrossRefPubMedGoogle Scholar
  14. Kim BO, Liu Y, Ruan Y, Xu ZC, Schantz L, He JJ (2003) Neuropathologies in transgenic mice expressing human immunodeficiency virus type 1 Tat protein under the regulation of the astrocyte-specific glial fibrillary acidic protein promoter and doxycycline. Am J Pathol 162:1693–1707PubMedGoogle Scholar
  15. Kohl TO, Hitzeroth II, Christensen ND, Rybicki EP (2007) Expression of HPV-11 L1 protein in transgenic Arabidopsis thaliana and Nicotiana tabacum. BMC Biotechnol 7:56CrossRefPubMedGoogle Scholar
  16. Meinhardt SW, Cheng W, Kwon CY, Donohue CM, Rasmussen JB (2002) Role of the arginyl-glycyl-aspartic motif in the action of Ptr ToxA produced by Pyrenophora tritici-repentis. Plant Physiol 130:1545–1551CrossRefPubMedGoogle Scholar
  17. Muller WE, Okamoto T, Reuter P, Ugarkovic D, Schroder HC (1990) Functional characterization of Tat protein from human immunodeficiency virus. Evidence that Tat links viral RNAs to nuclear matrix. J Biol Chem 265:3803–3808PubMedGoogle Scholar
  18. Oey M, Lohse M, Kreikemeyer B, Bock R (2009) Exhaustion of the chloroplast protein synthesis capacity by massive expression of a highly stable protein antibiotic. Plant J 57:436–445CrossRefPubMedGoogle Scholar
  19. Okamoto T, Wong-Staal F (1986) Demonstration of virus-specific transcriptional activator(s) in cells infected with HTLV-III by an in vitro cell-free system. Cell 47:29–35CrossRefPubMedGoogle Scholar
  20. Okamoto H, Asamitsu K, Nishimura H, Kamatani N, Okamoto T (2000) Reciprocal modulation of transcriptional activities between HIV-1 Tat and MHC class II transactivator CIITA. Biochem Biophys Res Commun 279:494–499CrossRefPubMedGoogle Scholar
  21. Polanska L, Vicankova A, Novakova M, Malbeck J, Dobrev PI, Brzobohaty B, Vankova R, Machackova I (2007) Altered cytokinin metabolism affects cytokinin, auxin, and abscisic acid contents in leaves and chloroplasts, and chloroplast ultrastructure in transgenic tobacco. J Exp Bot 58:637–649CrossRefPubMedGoogle Scholar
  22. Ramirez YJ, Tasciotti E, Gutierrez-Ortega A, Donayre Torres AJ, Olivera Flores MT, Giacca M, Gomez Lim MA (2007) Fruit-specific expression of the human immunodeficiency virus type 1 tat gene in tomato plants and its immunogenic potential in mice. Clin Vaccine Immunol 14:685–692CrossRefPubMedGoogle Scholar
  23. Sakakibara H (2006) Cytokinins: activity, biosynthesis, and translocation. Annu Rev Plant Biol 57:431–449CrossRefPubMedGoogle Scholar
  24. Santi L, Huang Z, Mason H (2006) Virus-like particles production in green plants. Methods 40:66–76CrossRefPubMedGoogle Scholar
  25. Schmulling T, Werner T, Riefler M, Krupkova E, Bartrina y Manns I (2003) Structure and function of cytokinin oxidase/dehydrogenase genes of maize, rice, Arabidopsis and other species. J Plant Res 116:241–252CrossRefPubMedGoogle Scholar
  26. Senchou V, Weide R, Carrasco A, Bouyssou H, Pont-Lezica R, Govers F, Canut H (2004) High affinity recognition of a Phytophthora protein by Arabidopsis via an RGD motif. Cell Mol Life Sci 61:502–509CrossRefPubMedGoogle Scholar
  27. Shchelkunov SN, Salyaev RK, Pozdnyakov SG, Rekoslavskaya NI, Nesterov AE, Ryzhova TS, Sumtsova VM, Pakova NV, Mishutina UO, Kopytina TV, Hammond RW (2006) Immunogenicity of a novel, bivalent, plant-based oral vaccine against hepatitis B and human immunodeficiency viruses. Biotechnol Lett 28:959–967CrossRefPubMedGoogle Scholar
  28. Webster DE, Thomas MC, Pickering R, Whyte A, Dry IB, Gorry PR, Wesselingh SL (2005) Is there a role for plant-made vaccines in the prevention of HIV/AIDS? Immunol Cell Biol 83:239–247CrossRefPubMedGoogle Scholar
  29. Werner T, Motyka V, Strnad M, Schmulling T (2001) Regulation of plant growth by cytokinin. Proc Natl Acad Sci USA 98:10487–10492CrossRefPubMedGoogle Scholar
  30. Yang SH, Yu H, Goh CJ (2003) Functional characterisation of a cytokinin oxidase gene DSCKX1 in Dendrobium orchid. Plant Mol Biol 51:237–248CrossRefPubMedGoogle Scholar
  31. Zahn LM, Hines PJ, Pennisi E, Travis J (2008) Green genes. Plant genomes. Introduction. Science 320:465CrossRefPubMedGoogle Scholar
  32. Zhou F, Badillo-Corona JA, Karcher D, Gonzalez-Rabade N, Piepenburg K, Borchers AM, Maloney AP, Kavanagh TA, Gray JC, Bock R (2008) High-level expression of human immunodeficiency virus antigens from the tobacco and tomato plastid genomes. Plant Biotechnol J 6:897–913CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Marni E. Cueno
    • 1
  • Yurina Hibi
    • 1
  • Kenichi Imai
    • 1
  • Antonio C. Laurena
    • 2
  • Takashi Okamoto
    • 1
    Email author
  1. 1.Department of Molecular and Cellular Biology Laboratory, Graduate School of Medical SciencesNagoya City UniversityMizuho-ku, NagoyaJapan
  2. 2.Biochemistry Laboratory, Institute of Plant BreedingUniversity of the PhilippinesLos BanosPhilippines

Personalised recommendations