Modeling the Early Steps of Cytoplasmic Trafficking in Viral Infection and Gene Delivery

Delivery of nucleic acid to the cell nucleus is a fundamental step in gene therapy. In this review of modeling drug and gene delivery, we focus on the particular stage of plasmid DNA or virus cytoplasmic trafficking. A challenging problem is to quantify the success of this limiting stage. We present some models and simulations of plasmid trafficking and of the limiting phase of DNA-polycation escape from an endosome and discuss virus cytoplasmic trafficking. The models can be used to assess the success of viral escape from endosomes, to quantify the early step of viral-cell infection, and to propose new simulation tools for designing new hybrid-viruses as synthetic vectors.

[1]  G. G. Stokes "J." , 1890, The New Yale Book of Quotations.

[2]  N. Metropolis,et al.  Equation of State Calculations by Fast Computing Machines , 1953, Resonance.

[3]  V. Georgiev Virology , 1955, Nature.

[4]  L. C. Moore,et al.  Nuclear envelope permeability , 1975, Nature.

[5]  L. Deaven,et al.  Quantitative determination of nuclear pore complexes in cycling cells with differing DNA content , 1977, The Journal of cell biology.

[6]  E. Neumann,et al.  Gene transfer into mouse lyoma cells by electroporation in high electric fields. , 1982, The EMBO journal.

[7]  H. Berg Random Walks in Biology , 2018 .

[8]  H. Risken The Fokker-Planck equation : methods of solution and applications , 1985 .

[9]  C. Knessl,et al.  Asymptotic solution of the Kramers-Moyal equation and first-passage times for Markov jump processes , 1984 .

[10]  C. Knessl,et al.  Solution of Kramers–Moyal equations for problems in chemical physics , 1984 .

[11]  C. Knessl,et al.  An Asymptotic Theory of Large Deviations for Markov Jump Processes , 1985 .

[12]  R. Peters Fluorescence microphotolysis to measure nucleocytoplasmic transport and intracellular mobility. , 1986, Biochimica et biophysica acta.

[13]  J. Northrop,et al.  Lipofection: a highly efficient, lipid-mediated DNA-transfection procedure. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[14]  M. Nango,et al.  Low pH induced membrane fusion of lipid vesicles containing proton-sensitive polymer. , 1987, Biochemistry.

[15]  M. Toner,et al.  Kinetics and likelihood of membrane rupture during electroporation , 1990 .

[16]  P. Beroza,et al.  Protonation of interacting residues in a protein by a Monte Carlo method: application to lysozyme and the photosynthetic reaction center of Rhodobacter sphaeroides. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[17]  D. Zhelev,et al.  Tension-stabilized pores in giant vesicles: determination of pore size and pore line tension. , 1993, Biochimica et biophysica acta.

[18]  A. Herrmann,et al.  Kinetics of the low pH-induced conformational changes and fusogenic activity of influenza hemagglutinin. , 1994, Biophysical journal.

[19]  Devesh Srivastava,et al.  Interpenetration of Interacting Polyelectrolytes , 1994 .

[20]  D. Scherman,et al.  A versatile vector for gene and oligonucleotide transfer into cells in culture and in vivo: polyethylenimine. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[21]  W. Ebeling Stochastic Processes in Physics and Chemistry , 1995 .

[22]  Netz,et al.  Pore formation and rupture in fluid bilayers. , 1996, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[23]  J. Weaver,et al.  Theory of electroporation: A review , 1996 .

[24]  R. Lamb,et al.  Orthomyxoviridae: The Viruses and Their Replication. , 1996 .

[25]  Roland L. Dunbrack,et al.  The Proton Sponge: a Trick to Enter Cells the Viruses Did Not Exploit , 1997, CHIMIA.

[26]  H. Alakomi,et al.  Polyethyleneimine is an effective permeabilizer of gram-negative bacteria. , 1997, Microbiology.

[27]  P. Nelson,et al.  Dynamically stabilized pores in bilayer membranes. , 1996, Biophysical journal.

[28]  A. Verkman,et al.  Translational Diffusion of Macromolecule-sized Solutes in Cytoplasm and Nucleus , 1997, The Journal of cell biology.

[29]  A. R. Klemm,et al.  Effects of polyethyleneimine on endocytosis and lysosome stability. , 1998, Biochemical pharmacology.

[30]  I. Helander,et al.  Permeabilizing action of polyethyleneimine on Salmonella typhimurium involves disruption of the outer membrane and interactions with lipopolysaccharide. , 1998, Microbiology.

[31]  P. Sens,et al.  Pore formation and area exchange in tense membranes , 1998 .

[32]  T. Friedmann,et al.  Enhanced Gene Transfer with Fusogenic Liposomes Containing Vesicular Stomatitis Virus G Glycoprotein , 1998, Journal of Virology.

[33]  S. J. Flint,et al.  Principles of Virology: Molecular Biology, Pathogenesis, and Control , 1999 .

[34]  F. Booy,et al.  Conformational Intermediates and Fusion Activity of Influenza Virus Hemagglutinin , 1999, Journal of Virology.

[35]  Olivier Sandre,et al.  Dynamics of transient pores in stretched vesicles. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[36]  I. Verma A tumultuous year for gene therapy. , 2000, Molecular therapy : the journal of the American Society of Gene Therapy.

[37]  J. Skehel,et al.  Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. , 2000, Annual review of biochemistry.

[38]  P. Gennes,et al.  Transient pores in stretched vesicles: role of leak-out , 2000, Physica A: Statistical Mechanics and its Applications.

[39]  B. Sodeik,et al.  Mechanisms of viral transport in the cytoplasm. , 2000, Trends in microbiology.

[40]  M. Hallek,et al.  Real-Time Single-Molecule Imaging of the Infection Pathway of an Adeno-Associated Virus , 2001, Science.

[41]  M. Fornerod,et al.  Import of adenovirus DNA involves the nuclear pore complex receptor CAN/Nup214 and histone H1 , 2001, Nature Cell Biology.

[42]  J. Hansen,et al.  Infection of purified nuclei by adeno-associated virus 2. , 2001, Molecular therapy : the journal of the American Society of Gene Therapy.

[43]  F. Grosveld,et al.  Baculovirus Infection of Nondividing Mammalian Cells: Mechanisms of Entry and Nuclear Transport of Capsids , 2001, Journal of Virology.

[44]  L. Chernomordik,et al.  Voltage-induced nonconductive pre-pores and metastable single pores in unmodified planar lipid bilayer. , 2001, Biophysical journal.

[45]  M. Stevens Simple simulations of DNA condensation. , 2001, Biophysical journal.

[46]  G. Zuber,et al.  Towards synthetic viruses. , 2001, Advanced drug delivery reviews.

[47]  D. Lauffenburger,et al.  Quantitative analysis of synthetic gene delivery vector design properties. , 2001, Molecular therapy : the journal of the American Society of Gene Therapy.

[48]  N. Pante,et al.  Nuclear pore complex is able to transport macromolecules with diameters of about 39 nm. , 2002, Molecular biology of the cell.

[49]  E. Knapp,et al.  Protonation and stability of the globular domain of influenza virus hemagglutinin. , 2002, Biophysical journal.

[50]  A. Verkman Solute and macromolecule diffusion in cellular aqueous compartments. , 2002, Trends in biochemical sciences.

[51]  R. Winkler,et al.  Complex formation in systems of oppositely charged polyelectrolytes: a molecular dynamics simulation study. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

[52]  T. Bieber,et al.  Intracellular route and transcriptional competence of polyethylenimine-DNA complexes. , 2002, Journal of controlled release : official journal of the Controlled Release Society.

[53]  C. R. Middaugh,et al.  Biophysical characterization of PEI/DNA complexes. , 2003, Journal of pharmaceutical sciences.

[54]  F. Szoka,et al.  Chloride Accumulation and Swelling in Endosomes Enhances DNA Transfer by Polyamine-DNA Polyplexes* , 2003, Journal of Biological Chemistry.

[55]  D. Hammer,et al.  Pore stability and dynamics in polymer membranes , 2002, cond-mat/0211501.

[56]  O. Farago “Water-free” computer model for fluid bilayer membranes , 2003, cond-mat/0304203.

[57]  Y. Mély,et al.  Monitoring of the formation and dissociation of polyethylenimine/DNA complexes by two photon fluorescence correlation spectroscopy. , 2003, Biophysical journal.

[58]  V. Talanquer,et al.  Nucleation of pores in amphiphile bilayers , 2003 .

[59]  Michael J Rust,et al.  Visualizing infection of individual influenza viruses , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[60]  Olivier Sandre,et al.  Transient pores in vesicles , 2003 .

[61]  L. Fournier,et al.  Lattice model for the kinetics of rupture of fluid bilayer membranes. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

[62]  Y. Levin,et al.  Pore dynamics of osmotically stressed vesicles , 2003, cond-mat/0311350.

[63]  L. Pelkmans,et al.  Caveolin-Stabilized Membrane Domains as Multifunctional Transport and Sorting Devices in Endocytic Membrane Traffic , 2004, Cell.

[64]  Michael J Rust,et al.  Endocytosis of influenza viruses. , 2004, Microbes and infection.

[65]  M. Kozlov,et al.  Influenza Hemagglutinins Outside of the Contact Zone Are Necessary for Fusion Pore Expansion* , 2004, Journal of Biological Chemistry.

[66]  C. Culmsee,et al.  Purification of polyethylenimine polyplexes highlights the role of free polycations in gene transfer , 2004, The journal of gene medicine.

[67]  G. Farr,et al.  Parvoviral virions deploy a capsid-tethered lipolytic enzyme to breach the endosomal membrane during cell entry. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[68]  C. Santangelo,et al.  Pore formation in fluctuating membranes. , 2004, The Journal of chemical physics.

[69]  A. Verkman,et al.  Actin Cytoskeleton as the Principal Determinant of Size-dependent DNA Mobility in Cytoplasm , 2005, Journal of Biological Chemistry.

[70]  S. Whelan,et al.  Endosomal Proteolysis of the Ebola Virus Glycoprotein Is Necessary for Infection , 2005, Science.

[71]  S. Shorte,et al.  Quantitative four-dimensional tracking of cytoplasmic and nuclear HIV-1 complexes , 2006, Nature Methods.

[72]  M. Imai,et al.  Membrane Fusion by Single Influenza Hemagglutinin Trimers , 2006, Journal of Biological Chemistry.

[73]  Yi Han,et al.  Cultivation of recombinant Chinese hamster ovary cells grown as suspended aggregates in stirred vessels. , 2006, Journal of bioscience and bioengineering.

[74]  Michael J Rust,et al.  Ligands for Clathrin-Mediated Endocytosis Are Differentially Sorted into Distinct Populations of Early Endosomes , 2006, Cell.

[75]  M. Imai,et al.  Dual Wavelength Imaging Allows Analysis of Membrane Fusion of Influenza Virus inside Cells , 2006, Journal of Virology.

[76]  M. Stewart Molecular mechanism of the nuclear protein import cycle , 2007, Nature Reviews Molecular Cell Biology.

[77]  S. Roche,et al.  Structure of the Prefusion Form of the Vesicular Stomatitis Virus Glycoprotein G , 2007, Science.

[78]  Z. Schuss,et al.  The narrow escape problem for diffusion in cellular microdomains , 2007, Proceedings of the National Academy of Sciences.

[79]  P. S. Rachakonda,et al.  The relevance of salt bridges for the stability of the influenza virus hemagglutinin , 2007, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[80]  X. Zhuang,et al.  Virus trafficking – learning from single-virus tracking , 2007, Nature Reviews Microbiology.

[81]  D. Holcman Modeling DNA and Virus Trafficking in the Cell Cytoplasm , 2007 .

[82]  Youichi Suzuki,et al.  The road to chromatin — nuclear entry of retroviruses , 2007, Nature Reviews Microbiology.

[83]  J. Birchall,et al.  Nuclear localisation and pDNA condensation in non‐viral gene delivery , 2007, The journal of gene medicine.

[84]  Kristen N. Duthie,et al.  Wide varieties of cationic nanoparticles induce defects in supported lipid bilayers. , 2008, Nano letters.

[85]  K. Stiasny,et al.  Identification of specific histidines as pH sensors in flavivirus membrane fusion , 2008, The Journal of cell biology.

[86]  Thibault Lagache,et al.  Effective Motion of a Virus Trafficking Inside a Biological Cell , 2007, SIAM J. Appl. Math..

[87]  Z. Schuss,et al.  Diffusion escape through a cluster of small absorbing windows , 2008 .

[88]  Ying Tu,et al.  A fusogenic segment of glycoprotein H from herpes simplex virus enhances transfection efficiency of cationic liposomes , 2008, The journal of gene medicine.

[89]  T. Lagache,et al.  Quantifying intermittent transport in cell cytoplasm. , 2008, Physical review. E, Statistical, nonlinear, and soft matter physics.

[90]  Amit Singer,et al.  Partially Reflected Diffusion , 2008, SIAM J. Appl. Math..

[91]  Shuang Yang,et al.  Release of cationic polymer-DNA complexes from the endosome: A theoretical investigation of the proton sponge hypothesis. , 2008, The Journal of chemical physics.

[92]  K. Leong,et al.  Quantitative comparison of intracellular unpacking kinetics of polyplexes by a model constructed from quantum dot-FRET. , 2008, Molecular therapy : the journal of the American Society of Gene Therapy.

[93]  O. Farago Membrane fluctuations near a plane rigid surface. , 2008, Physical review. E, Statistical, nonlinear, and soft matter physics.

[94]  T. Lagache,et al.  Quantitative analysis of virus and plasmid trafficking in cells. , 2007, Physical review. E, Statistical, nonlinear, and soft matter physics.

[95]  M. Kokaia,et al.  Epilepsy and Gene Therapy: Resculpturing Synaptic Transmission with Neuropeptides , 2009 .

[96]  G. Whittaker,et al.  Activation of the SARS coronavirus spike protein via sequential proteolytic cleavage at two distinct sites , 2009, Proceedings of the National Academy of Sciences.

[97]  R. Peters Functionalization of a nanopore: the nuclear pore complex paradigm. , 2009, Biochimica et biophysica acta.

[98]  Daniel Coombs,et al.  Diffusion on a Sphere with Localized Traps: Mean First Passage Time, Eigenvalue Asymptotics, and Fekete Points , 2009, SIAM J. Appl. Math..

[99]  E. Abad,et al.  Narrow escape time to a structured target located on the boundary of a microdomain. , 2009, The Journal of chemical physics.

[100]  Z. Schuss Theory and Applications of Stochastic Processes: An Analytical Approach , 2009 .

[101]  D. Dykxhoorn,et al.  Breaking down the barriers: siRNA delivery and endosome escape , 2010, Journal of Cell Science.

[102]  Z. Schuss Theory and Applications of Stochastic Processes , 2010 .

[103]  S. Sharma,et al.  The Fokker-Planck Equation , 2010 .

[104]  Alan R. Lowe,et al.  Selectivity Mechanism of the Nuclear Pore Complex Characterized by Single Cargo Tracking , 2010, Nature.

[105]  M. Rout,et al.  The nuclear pore complex and nuclear transport. , 2010, Cold Spring Harbor perspectives in biology.

[106]  Y. George Receptor-mediated in Vitro Gene Transformation by a Soluble DNA Carrier System , 2022 .