One-dimensional Brownian motion of charged nanoparticles along microtubules: a model system for weak binding interactions.
Various proteins are known to exhibit one-dimensional Brownian motion along charged rodlike polymers, such as microtubules (MTs), actin, and DNA. The electrostatic interaction between the proteins and the rodlike polymers appears to be crucial for one-dimensional Brownian motion, although the underlying mechanism has not been fully clarified. We examined the interactions of positively-charged nanoparticles composed of polyacrylamide gels with MTs. These hydrophilic nanoparticles bound to MTs and displayed one-dimensional Brownian motion in a charge-dependent manner, which indicates that nonspecific electrostatic interaction is sufficient for one-dimensional Brownian motion. The diffusion coefficient decreased exponentially with an increasing particle charge (with the exponent being 0.10 kBT per charge), whereas the duration of the interaction increased exponentially (exponent of 0.22 kBT per charge). These results can be explained semiquantitatively if one assumes that a particle repeats a cycle of binding to and movement along an MT until it finally dissociates from the MT. During the movement, a particle is still electrostatically constrained in the potential valley surrounding the MT. This entire process can be described by a three-state model analogous to the Michaelis-Menten scheme, in which the two parameters of the equilibrium constant between binding and movement, and the rate of dissociation from the MT, are derived as a function of the particle charge density. This study highlights the possibility that the weak binding interactions between proteins and rodlike polymers, e.g., MTs, are mediated by a similar, nonspecific charge-dependent mechanism.
Minoura
Itsushi
I
Laboratory for Molecular Biophysics, Brain Science Institute, RIKEN, Wako, Saitama, Japan. minoura@brain.riken.jp
Katayama
Eisaku
E
Sekimoto
Ken
K
Muto
Etsuko
E
D000180:Acrylic Resins / Q000737:chemistry; D000818:Animals; D004058:Diffusion; D016547:Kinesins / Q000378:metabolism; D008870:Microtubules / Q000378:metabolism*; D008954:Models, Biological; D009038:Motion; D053758:Nanoparticles / Q000737:chemistry*; D034421:Sus scrofa; D000099166:Polyacrylamides
D000180:Acrylic Resins; D016547:Kinesins; D000099166:Polyacrylamides
Annu Rev Phys Chem. 1995;46:657-700
7495482
Biochem Biophys Res Commun. 2007 Mar 9;354(2):379-84
17241612
Biochem Biophys Res Commun. 2006 Feb 3;340(1):23-8
16343429
Nat Cell Biol. 2008 Apr;10(4):407-14
18364702
Proc Natl Acad Sci U S A. 2008 Aug 5;105(31):10721-6
18658237
Proc Natl Acad Sci U S A. 2006 Apr 11;103(15):5752-7
16585517
J Mol Biol. 1970 Nov 14;53(3):401-17
4924006
Proc Natl Acad Sci U S A. 2007 Mar 13;104(11):4332-6
17360524
Proc Natl Acad Sci U S A. 2000 Jan 18;97(2):640-5
10639132
EMBO J. 1996 Sep 16;15(18):5104-11
8890184
Nucleic Acids Res. 2004 Jun 03;32(10):3040-52
15178741
J Biol Chem. 1999 May 28;274(22):15293-6
10336412
Cell. 1989 Dec 1;59(5):915-25
2531633
J Cell Biol. 2005 Feb 28;168(5):691-6
15738263
J Cell Sci. 1993 Mar;104 ( Pt 3):899-906
8314880
Science. 1999 Feb 19;283(5405):1152-7
10024239
Proc Natl Acad Sci U S A. 2004 Oct 12;101(41):14731-5
15469913
Nat Cell Biol. 2006 Jun;8(6):562-70
16715075
J Biochem. 1996 Jun;119(6):1024-32
8827433
Trends Biochem Sci. 2004 Jun;29(6):301-9
15276184
Biophys J. 2001 Nov;81(5):2838-50
11606295
Nature. 2005 May 19;435(7040):308-12
15902249
Biophys J. 2009 Jan;96(2):609-20
19167308
J Chem Phys. 2006 Apr 21;124(15):154902
16674260
Proc Natl Acad Sci U S A. 2001 Aug 28;98(18):10037-41
11517324
Nature. 2006 May 4;441(7089):115-9
16672973
Cell Struct Funct. 1999 Oct;24(5):373-83
15216895
Biophys J. 1999 Oct;77(4):2284-94
10512846
Q Rev Biophys. 1978 May;11(2):179-246
353876
Biosystems. 2003 Sep;71(1-2):145-56
14568215
J Biol Chem. 1989 Jan 15;264(2):675-8
2642903
Methods Enzymol. 1972;25:464-8
23014427
Nat Chem Biol. 2005 Nov;1(6):342-7
16408074
Phys Rev Lett. 2006 Jul 28;97(4):048302
16907618
Biophys J. 2006 May 15;90(10):3739-48
16500962
Annu Rev Biophys Biophys Chem. 1990;19:423-65
2194482
Proc Natl Acad Sci U S A. 2007 Sep 25;104(39):15328-33
17878301
Biophys J. 2006 May 15;90(10):3643-52
16500969
Curr Opin Cell Biol. 2009 Feb;21(1):68-73
19185482