Light-induced release of DNA from plasmon-resonant nanoparticles: Towards light-controlled gene therapy

Surface-plasmon driven DNA dehybridization is a topic of intense current interest due to its highly promising potential for enabling light-controlled gene therapy: it is also of inherent interest as a light-driven nanoscale actuation process. In this study we formulate an Au nanoshell-based complex designed to release single-stranded DNA (ssDNA) from its surface when illuminated with plasmon-resonant light. This system allows us to examine DNA dehybridization induced by excitation of localized surface plasmons on the nanoparticle, relative to the thermal DNA dehybridization (melting). The dehybridization temperatures, and the percentage of DNA released per nanoparticle, differ markedly between the two processes.

[1]  Park,et al.  Optical reflectance and scattering studies of nucleation and growth of bubbles at a liquid-solid interface induced by pulsed laser heating. , 1993, Physical review letters.

[2]  A. Stephens,et al.  Antisense oligonucleotide therapy in cancer. , 2003, Current opinion in molecular therapeutics.

[3]  J. Nam,et al.  Lipid-gold-nanoparticle hybrid-based gene delivery. , 2008, Small.

[4]  R. Blake,et al.  Stacking energies in DNA. , 1991, The Journal of biological chemistry.

[5]  Mostafa A. El-Sayed,et al.  Preparation and Growth Mechanism of Gold Nanorods (NRs) Using Seed-Mediated Growth Method , 2003 .

[6]  V. Rotello,et al.  Glutathione-mediated delivery and release using monolayer protected nanoparticle carriers. , 2006, Journal of the American Chemical Society.

[7]  Mostafa A. El-Sayed,et al.  How long does it take to melt a gold nanorod?: A femtosecond pump–probe absorption spectroscopic study , 1999 .

[8]  Mark H Schoenfisch,et al.  Water-soluble nitric oxide-releasing gold nanoparticles. , 2007, Langmuir : the ACS journal of surfaces and colloids.

[9]  J. SantaLucia,et al.  Improved nearest-neighbor parameters for predicting DNA duplex stability. , 1996, Biochemistry.

[10]  Albert S. Benight,et al.  Electrical detection of the temperature induced melting transition of a DNA hairpin covalently attached to gold interdigitated microelectrodes , 2008, Nucleic acids research.

[11]  H. Blöcker,et al.  Predicting DNA duplex stability from the base sequence. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[12]  Chad A. Mirkin,et al.  Oligonucleotide-Modified Gold Nanoparticles for Intracellular Gene Regulation , 2006, Science.

[13]  Wah Chiu,et al.  Remotely triggered liposome release by near-infrared light absorption via hollow gold nanoshells. , 2008, Journal of the American Chemical Society.

[14]  L. Seymour,et al.  Key issues in non-viral gene delivery. , 1998, Advanced drug delivery reviews.

[15]  R. Stafford,et al.  Nanoshell-mediated near-infrared thermal therapy of tumors under magnetic resonance guidance , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[16]  Vincent M Rotello,et al.  Gold nanoparticles in delivery applications. , 2008, Advanced drug delivery reviews.

[17]  Chad A. Mirkin,et al.  Gene regulation with polyvalent siRNA-nanoparticle conjugates. , 2009, Journal of the American Chemical Society.

[18]  Gregory V. Hartland,et al.  Heat Dissipation for Au Particles in Aqueous Solution: Relaxation Time versus Size , 2002 .

[19]  Hidekazu Kumano,et al.  Effect of indium doping on the transient optical properties of GaN films , 1999 .

[20]  R. Samulski,et al.  Adeno-associated viral vectors as gene delivery vehicles. , 2000, International journal of molecular medicine.

[21]  N. Sugimoto,et al.  Improved thermodynamic parameters and helix initiation factor to predict stability of DNA duplexes. , 1996, Nucleic acids research.

[22]  Naomi J. Halas,et al.  Surface enhanced Raman scattering in the near infrared using metal nanoshell substrates , 1999 .

[23]  Dakrong Pissuwan,et al.  Therapeutic possibilities of plasmonically heated gold nanoparticles. , 2006, Trends in biotechnology.

[24]  A. Govorov,et al.  Experimental and theoretical studies of light-to-heat conversion and collective heating effects in metal nanoparticle solutions. , 2009, Nano letters.

[25]  M. Stephenson,et al.  Inhibition of Rous sarcoma viral RNA translation by a specific oligodeoxyribonucleotide. , 1978, Proceedings of the National Academy of Sciences of the United States of America.

[26]  A. Domb,et al.  Polymers in gene therapy: antisense delivery systems , 1998 .

[27]  Alexander O. Govorov,et al.  Generating heat with metal nanoparticles , 2007 .

[28]  C. Mirkin,et al.  A fluorescence-based method for determining the surface coverage and hybridization efficiency of thiol-capped oligonucleotides bound to gold thin films and nanoparticles. , 2000, Analytical chemistry.

[29]  R. Weissleder A clearer vision for in vivo imaging , 2001, Nature Biotechnology.

[30]  D. Burgess,et al.  DNA-based therapeutics and DNA delivery systems: A comprehensive review , 2005, The AAPS Journal.

[31]  R. Langer,et al.  Designing materials for biology and medicine , 2004, Nature.

[32]  Younan Xia,et al.  Gold nanostructures: engineering their plasmonic properties for biomedical applications. , 2006, Chemical Society reviews.

[33]  J. West,et al.  Near-infrared resonant nanoshells for combined optical imaging and photothermal cancer therapy. , 2007, Nano letters.

[34]  K. Baek,et al.  Enhanced cellular delivery and transfection efficiency of plasmid DNA using positively charged biocompatible colloidal gold nanoparticles. , 2007, Biochimica et biophysica acta.

[35]  Naomi J. Halas,et al.  Nanoengineering of optical resonances , 1998 .

[36]  Emil Prodan,et al.  Electronic structure and polarizability of metallic nanoshells , 2002 .

[37]  J. SantaLucia,et al.  A unified view of polymer, dumbbell, and oligonucleotide DNA nearest-neighbor thermodynamics. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[38]  C. Keating,et al.  Curvature effects in DNA:Au nanoparticle conjugates. , 2009, ACS nano.

[39]  Matthew Tirrell,et al.  Laser-Activated Gene Silencing via Gold Nanoshell-siRNA Conjugates. , 2009, ACS nano.

[40]  K. Hamad-Schifferli,et al.  Selective release of multiple DNA oligonucleotides from gold nanorods. , 2009, ACS nano.

[41]  V. Rotello,et al.  Stability of Gold Nanoparticle‐Bound DNA toward Biological, Physical, and Chemical Agents , 2006, Chemical biology & drug design.

[42]  Tammy Y. Olson,et al.  Synthesis, characterization, and tunable optical properties of hollow gold nanospheres. , 2006, The journal of physical chemistry. B.

[43]  R. S. Quartin,et al.  Effect of ionic strength on the hybridization of oligodeoxynucleotides with reduced charge due to methylphosphonate linkages to unmodified oligodeoxynucleotides containing the complementary sequence. , 1989, Biochemistry.

[44]  Hironobu Takahashi,et al.  Controlled release of plasmid DNA from gold nanorods induced by pulsed near-infrared light. , 2005, Chemical communications.

[45]  Lingyan Huang,et al.  Effects of sodium ions on DNA duplex oligomers: improved predictions of melting temperatures. , 2004, Biochemistry.

[46]  Wei Qian,et al.  The potential use of the enhanced nonlinear properties of gold nanospheres in photothermal cancer therapy , 2007, Lasers in surgery and medicine.

[47]  Reginald Birngruber,et al.  On the possibility of high-precision photothermal microeffects and the measurement of fast thermal denaturation of proteins , 1999 .

[48]  C. E. Moran,et al.  Laser-Induced Reshaping of Metallodielectric Nanoshells under Femtosecond and Nanosecond Plasmon Resonant Illumination , 2004 .

[49]  Peter Nordlander,et al.  Plasmonic nanostructures: artificial molecules. , 2007, Accounts of chemical research.

[50]  I. Tinoco,et al.  The stability of helical polynucleotides: base contributions. , 1962, Journal of molecular biology.

[51]  Luke P. Lee,et al.  Remote optical switch for localized and selective control of gene interference. , 2009, Nano letters.

[52]  Naomi J Halas,et al.  Nanoshell-enabled photothermal cancer therapy: impending clinical impact. , 2008, Accounts of chemical research.

[53]  D. Turner,et al.  Improved free-energy parameters for predictions of RNA duplex stability. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[54]  P. Jain,et al.  Review of Some Interesting Surface Plasmon Resonance-enhanced Properties of Noble Metal Nanoparticles and Their Applications to Biosystems , 2007 .

[55]  Chad A Mirkin,et al.  Polyvalent DNA nanoparticle conjugates stabilize nucleic acids. , 2020, Nano letters.

[56]  D. Crothers,et al.  THEORY OF THE MELTING TRANSITION OF SYNTHETIC POLYNUCLEOTIDES: EVALUATION OF THE STACKING FREE ENERGY. , 1964, Journal of molecular biology.

[57]  Wei Zhang,et al.  Gold nanoparticle ensembles as heaters and actuators: melting and collective plasmon resonances , 2006, Nanoscale Research Letters.

[58]  Chad A Mirkin,et al.  The role radius of curvature plays in thiolated oligonucleotide loading on gold nanoparticles. , 2009, ACS nano.

[59]  K. Leong,et al.  Multifunctional nanorods for gene delivery , 2003, Nature materials.

[60]  Yi-Cheng Chen,et al.  DNA-gold nanorod conjugates for remote control of localized gene expression by near infrared irradiation. , 2006, Journal of the American Chemical Society.

[61]  S. Crooke,et al.  Molecular mechanisms of action of antisense drugs. , 1999, Biochimica et biophysica acta.

[62]  M J Doktycz,et al.  Studies of DNA dumbbells. I. Melting curves of 17 DNA dumbbells with different duplex stem sequences linked by T4 endloops: Evaluation of the nearest‐neighbor stacking interactions in DNA , 1992, Biopolymers.

[63]  Melting transition of directly linked gold nanoparticle DNA assembly , 2005, physics/0503090.

[64]  W. Wels,et al.  DNA-carrier proteins for targeted gene delivery. , 2000, Advanced drug delivery reviews.

[65]  Albert S. Benight,et al.  Thermal denaturation of DNA molecules: A comparison of theory with experiment , 1985 .

[66]  Stephan Link,et al.  Optical properties and ultrafast dynamics of metallic nanocrystals. , 2003, Annual review of physical chemistry.

[67]  Vincent M Rotello,et al.  Efficient gene delivery vectors by tuning the surface charge density of amino acid-functionalized gold nanoparticles. , 2008, ACS nano.

[68]  A Paul Alivisatos,et al.  Discrete nanostructures of quantum dots/Au with DNA. , 2004, Journal of the American Chemical Society.

[69]  Yusaku Tagashira,et al.  Stabilities of nearest‐neighbor doublets in double‐helical DNA determined by fitting calculated melting profiles to observed profiles , 1981 .

[70]  P. Nordlander,et al.  A Hybridization Model for the Plasmon Response of Complex Nanostructures , 2003, Science.

[71]  Seymour,et al.  Key issues in non-viral gene delivery. , 2001, Advanced drug delivery reviews.

[72]  Erika Check,et al.  Gene therapy: A tragic setback , 2002, Nature.

[73]  E. Finot,et al.  Direct measurement of the melting temperature of supported DNA by electrochemical method. , 2003, Nucleic acids research.