Skip to main content

Advertisement

Log in

Cell Membrane Diversity in Noncovalent Protein Transduction

  • Published:
Journal of Membrane Biology Aims and scope Submit manuscript

Abstract

Crossing of the plasma membrane for all macromolecules without energy, receptors or any artificial methods was thought to be difficult. Our previous studies demonstrated that arginine-rich intracellular delivery (AID) peptides are able to deliver macromolecules, such as proteins, RNAs and DNAs, into either animal or plant cells. Cellular internalization could be mediated by effective and nontoxic AID peptides in either a covalent or noncovalent protein transduction (NPT) manner. AID peptides were so versatile that the procedure seemed to replace the current artificial transfection methods. However, the utilization of AID peptides has been limited to animal or plant systems so far. None has proposed that AID peptides could work in other species. Here, we select some representative organisms to screen whether NPT mediated by AID peptides works in them. They include cyanobacteria, bacteria, archaea, algae, fungi and yeasts. The results reveal that not all living beings possess this capability of protein transduction. Interestingly, all species of prokaryotes tested, which were thought to be highly diverse from the animal and plant systems, appear to be capable of NPT. The mechanism of AID-mediated NPT in cyanobacteria is in a classical endocytosis- and energy-independent pathway and may involve macropinocytosis. In contrast, green algae and multicellular fungi of the eukaryotes are impermeable to protein passage. Our results bring an interesting clue to the reexamination of the phylogeny of both algae and fungi.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12

Similar content being viewed by others

References

  • Cai SR, Xu G, Becker-Hapak M, Ma M, Dowdy SF, McLeod HL (2006) The kinetics and tissue distribution of protein transduction in mice. Eur J Pharm Sci 27:311–319

    Article  PubMed  CAS  Google Scholar 

  • Chang M, Chou JC, Lee HJ (2005a) Cellular internalization of fluorescent proteins via arginine-rich intracellular delivery peptide in plant cells. Plant Cell Physiol 46:482–488

    Google Scholar 

  • Chang M, Hsu HY, Lee HJ (2005b) Dye-free protein molecular weight markers. Electrophoresis 26:3062–3068

    Google Scholar 

  • Chang M, Lee HJ (2005) Gradient polymerase chain reaction performance using regular thermal cycle machine. Anal Biochem 340:174–177

    Article  PubMed  CAS  Google Scholar 

  • Chang M, Chou JC, Chen CP, Liu BR, Lee HJ (2007) Noncovalent protein transduction in plant cells by macropinocytosis. New Phytol 174:46–56

    Article  PubMed  CAS  Google Scholar 

  • Chen CP, Chou JC, Liu BR, Chang M, Lee HJ (2007) Transfection and expression of plasmid DNA in plant cells by an arginine-rich intracellular delivery peptide without protoplast preparation. FEBS Lett 581:1891–1897

    PubMed  CAS  Google Scholar 

  • Chou JC, Huang YB (2005) Induction and characterization of an indole-3-acetyl-l-alanine hydrolase from Arthrobacter ilicis. J Plant Growth Regul 24:11–18

    Article  CAS  Google Scholar 

  • Conner SD, Schmid SL (2003) Regulated portals of entry into the cell. Nature 422:37–44

    Article  PubMed  CAS  Google Scholar 

  • Console S, Marty C, Garcia-Echeverria C, Schwendener R, Ballmer-Hofer K (2003) Antennapedia and HIV trans-activator of transcription (Tat) “protein transduction domains” promote endocytosis of high molecular weight cargo upon binding to cell surface glycosaminoglycans. J Biol Chem 278:35109–35114

    Article  PubMed  CAS  Google Scholar 

  • Dietz GP, Bahr M (2004) Delivery of bioactive molecules into the cell: the Trojan horse approach. Mol Cell Neurosci 27:85–131

    Article  PubMed  CAS  Google Scholar 

  • Dowdy SF, Snyder EL (2005) Recent advances in the use of protein transduction domains for the delivery of peptides, proteins and nucleic acids in vivo. Expert Opin Drug Deliv 2:43–51

    Article  PubMed  Google Scholar 

  • Elowitz MB, Surette MG, Wolf PE, Stock JB, Leibler S (1999) Protein mobility in the cytoplasm of Escherichia coli. J Bacteriol 181:197–203

    PubMed  CAS  Google Scholar 

  • Fawell S, Seery J, Daikh Y, Moore C, Chen LL, Pepinsky B, Barsoum J (1994) Tat-mediated delivery of heterologous proteins into cells. Proc Natl Acad Sci USA 91:664–668

    Article  PubMed  CAS  Google Scholar 

  • Frankel AD, Pabo CO (1988) Cellular uptake of the Tat protein from human immunodeficiency virus. Cell 55:1189–1193

    Article  PubMed  CAS  Google Scholar 

  • Futaki S (2005) Membrane-permeable arginine-rich peptides and the translocation mechanisms. Adv Drug Deliv Rev 57:547–558

    Article  PubMed  CAS  Google Scholar 

  • Green M, Loewenstein PM (1988) Autonomous functional domains of chemically synthesized human immunodeficiency virus Tat trans-activator protein. Cell 55:1179–1188

    Article  PubMed  CAS  Google Scholar 

  • Henar Valdivieso M, Duran A, Roncero C (1999) Chitin synthases in yeast and fungi. EXS 87:55–69

    PubMed  CAS  Google Scholar 

  • Hou YW, Chan MH, Hsu HR, Liu BR, Chen CP, Chen HH, Lee HJ (2007) Transdermal delivery of proteins mediated by noncovalently associated arginine-rich intracellular delivery peptides. Exp Dermatol 16:999–1006

    Article  PubMed  CAS  Google Scholar 

  • Kaplan IM, Wadia JS, Dowdy SF (2005) Cationic TAT peptide transduction domain enters cells by macropinocytosis. J Control Release 102:247–253

    Article  PubMed  CAS  Google Scholar 

  • Kessels MM, Qualmann B (2004) The syndapin protein family: linking membrane trafficking with the cytoskeleton. J Cell Sci 117:3077–3086

    Article  PubMed  CAS  Google Scholar 

  • Kroth PG (2002) Protein transport into secondary plastids and the evolution of primary and secondary plastids. Int Rev Cytol 221:191–255

    Article  PubMed  CAS  Google Scholar 

  • Lewis LA, Muller-Parker G (2004) Phylogenetic placement of “zoochlorellae” (Chlorophyta), algal symbiont of the temperate sea anemone Anthopleura elegantissima. Biol Bull 207:87–92

    Article  PubMed  CAS  Google Scholar 

  • Lin JY, Wu TZ, Chou JC (2006) In vitro induction of fruiting body in Antrodia cinnamomea—a medicinally important fungus. Bot Stud 47:267–272

    Google Scholar 

  • Lindsay MA (2002) Peptide-mediated cell delivery: application in protein target validation. Curr Opin Pharmacol 2:587–594

    Article  PubMed  CAS  Google Scholar 

  • Liu K, Lee HJ, Leong SS, Liu CL, Chou CJ (2007) A bacterial indole-3-acetyl-l-aspartic acid hydrolase inhibits mungbean 2 (Vigna radiata L.) seed germination through arginine-rich intracellular delivery. J Plant Growth Regul 26:278–284

    Article  CAS  Google Scholar 

  • Nakase I, Niwa M, Takeuchi T, Sonomura K, Kawabata N, Koike Y, Takehashi M, Tanaka S, Ueda K, Simpson JC, Jones AT, Sugiura Y, Futaki S (2004) Cellular uptake of arginine-rich peptides: roles for macropinocytosis and actin rearrangement. Mol Ther 10:1011–1022

    Article  PubMed  CAS  Google Scholar 

  • Pearlmutter NL, Lembi CA (1978) Localization of chitin in algal and fungal cell walls by light and electron microscopy. J Histochem Cytochem 26:782–791

    PubMed  CAS  Google Scholar 

  • Romeike J, Friedl T, Helms G, Ott S (2002) Genetic diversity of algal and fungal partners in four species of Umbilicaria (lichenized Ascomycetes) along a transect of the Antarctic peninsula. Mol Biol Evol 19:1209–1217

    PubMed  CAS  Google Scholar 

  • Schwarze SR, Ho A, Vocero-Akbani A, Dowdy SF (1999) In vivo protein transduction: delivery of a biologically active protein into the mouse. Science 285:1569–1572

    Article  PubMed  CAS  Google Scholar 

  • Schwarze SR, Hruska KA, Dowdy SF (2000) Protein transduction: unrestricted delivery into all cells. Trends Cell Biol 10:290–295

    Article  PubMed  CAS  Google Scholar 

  • Stork T, Michel KP, Pistorius EK, Dietz KJ (2005) Bioinformatic analysis of the genomes of the cyanobacteria Synechocystis sp. PCC 6803 and Synechococcus elongates PCC 7942 for the presence of peroxiredoxins and their transcript regulation under stress. J Exp Bot 56:3193–3206

    Article  PubMed  CAS  Google Scholar 

  • Tartar A, Boucias DG, Adams BJ, Becnel JJ (2002) Phylogenetic analysis identifies the invertebrate pathogen Helicosporidium sp. as a green alga (Chlorophyta). Int J Syst Evol Microbiol 52:273–279

    PubMed  CAS  Google Scholar 

  • Vives E, Brodin P, Lebleu B (1997) A truncated HIV-1 tat protein basic domain rapidly translocates through the plasma membrane and accumulates in the cell nucleus. J Biol Chem 272:16010–16017

    Article  PubMed  CAS  Google Scholar 

  • Wadia JS, Dowdy SF (2002) Protein transduction technology. Curr Opin Biotechnol 13:52–56

    Article  PubMed  CAS  Google Scholar 

  • Wadia JS, Stan RV, Dowdy SF (2004) Transducible TAT-HA fusogenic peptide enhances escape of TAT-fusion proteins after lipid raft macropinocytosis. Nat Med 10:310–315

    Article  PubMed  CAS  Google Scholar 

  • Wadia JS, Dowdy SF (2005) Transmembrane delivery of protein and peptide drugs by TAT-mediated transduction in the treatment of cancer. Adv Drug Deliv Rev 57:579–596

    Article  PubMed  CAS  Google Scholar 

  • Wang YH, Chen CP, Chan MH, Chang M, Hou YW, Chen HH, Hsu HR, Liu K, Lee HJ (2006) Arginine-rich intracellular delivery peptides noncovalently transport protein into living cells. Biochem Biophys Res Commun 346:758–767

    Article  PubMed  CAS  Google Scholar 

  • Wang YH, Hou YW, Lee HJ (2007) An intracellular delivery method for siRNA by an arginine-rich peptide. J Biochem Biophys Methods 70:579–586

    Article  PubMed  CAS  Google Scholar 

  • Weng JH, Shieh YJ (2004) Salicylhydroxamic acid (SHAM) inhibits O2 photoreduction which protects nitrogenase activity in the cyanobacterium Synechococcus sp. RF-1. Photosyn Res 82:151–164

    Article  PubMed  CAS  Google Scholar 

  • Woese CR, Fox GE (1977) Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci USA 74:5088–5090

    Article  PubMed  CAS  Google Scholar 

  • Woese CR, Kandler O, Wheelis ML (1990) Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci USA 87:4576–4579

    Article  PubMed  CAS  Google Scholar 

  • Wu JT, Chiang YR, Huang WY, Jane WN (2006) Cytotoxic effects of free fatty acids on phytoplankton algae and cyanobacteria. Aqua Toxicol 80:338–345

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Drs. Yuh-Jang Shieh and Jiunn-Tzong Wu from Academia Sinica (Taipei, Taiwan) for providing cyanobacteria and chlorophytes, respectively. We are grateful to Mr. Jeffrey Picard for critical reading and editing of the manuscript. This work was supported by the National Science Council, Taiwan.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Han-Jung Lee.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Liu, B.R., Chou, JC. & Lee, HJ. Cell Membrane Diversity in Noncovalent Protein Transduction. J Membrane Biol 222, 1–15 (2008). https://doi.org/10.1007/s00232-008-9096-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00232-008-9096-6

Keywords

Navigation