Molecular Dynamics simulations of proteins

Introduction to protein simulation

In the previous part we've learned what MD simulations are and how to simulate

a van der Waals gas. Now it is time to set up a simulation of a biological

macromolecule: a small protein. Proteins are nature's universal machines. For

example, they are used as building blocks (e.g. collagen in skin, bones and

teeth), transporters (e.g. hemoglobin as oxygen transporter in the blood), as

reaction catalysts (enzymes like lysozyme that catalyse the breakdown of

sugars), and as nano-machines (like myosin that is at the basis of muscle

contraction). The protein's structure or molecular architecture is sufficient

for some of these functions (like for example in the case of collagen), but for

most others the function is intimately linked to internal dynamics. In these

cases, evolution has optimised and fine-tuned the protein to exhibit exactly

that type of dynamics that is essential for its function. Therefore, if we want

to understand protein function, we often first need to understand its

dynamics. Unfortunately, there are no experimental techniques available to

study protein dynamics at the atomic resolution at the physiologically relevant

time resolution (that can range from seconds or milliseconds down to

nanoseconds or even picoseconds). Therefore, computer simulations are

employed to numerically simulate protein dynamics.


As before, we will use the GROMACS

simulation package for this.


Today, we will simulate the dynamics of a small, typical

protein domain: the B1 domain of protein G. B1 is one of the domains

of protein G, a member of an important class of proteins, which form

IgG binding receptors on the surface of certain Staphylococcal and

Streptococcal strains. These proteins allow the pathogenic bacterium

to evade the host immune response by coating the invading bacteria

with host antibodies, thereby contributing significantly to the

pathogenicity of these bacteria (click

here for further background information on this protein).


Before a simulation can be started, an initial structure of the

protein is required. Fortunately, the structure of the B1 domain of

protein G has been solved experimentally, both by x-ray

crystallography and NMR. Experimentally solved protein structures are

collected and distributed by the Protein Data Bank (PDB). Please open

this link in a new browser

window and enter "protein G B1" in the search field. Several entries

in the PDB should match this query. We will choose the x-ray structure

with the highest resolution (entry 1PGB) for this study. To download

the structure, click on the link "1PGB", and then, under "Download Files",

select "PDB File". When prompted, select "save to disk", and save the file

to the local hard disk. To have a look at the contents of the file, on the unix prompt, type:

more 1PGB.pdb

As we've learned in the protein structure practical,

the file starts with general information about the protein, about the

structure, and about the experimental techniques used to determine the

structure, as well as literature references where the structure is described in

detail. (in "more", press the spacebar to scroll). Especially critical to check before we use a structure for a simulation

are the resolution and the R-factor (or free-R factor), that contain

information on how well the deposited structure matches the measured data

(x-ray reflection intensities). After the general information in the header,

the atomic coordinates follow, with one line per atom, containing the atom

number, the atom name, the residue name, the residue number the cartesian x,y,

and z coordinates, followed by two other numbers: the so called occupancy and

B-factor (or temperature factor). The latter two also contain important hints

about the coordinates. The occupancy is a measure for the percentage of atoms

in the crystal that occupies the specified coordinates. As you will see, in

this case the only occupancies that are not equal to one are found for water

molecules near the end of the file. These water positions are apparently not

occupied in all protein copies in he crystal. The next column contains the

so-called B-factors, which are a measure for the disorder or mobility of an

atom. Low B-factors (< 30) therefore correspond to well-defined parts of the

structure, whereas high B-factors (> 80) might indicate highly disordered parts

of the structure or even mis-interpreted parts of the model.

(quit the "more" program by pressing "q").

Now we can have a look at the structure:

rasmol 1PGB.pdb

to visualise the structure.

We now see a so-called wireframe

representation of the protein structure: atoms (with different colors

for the different chemical elements: grey for carbon; red for oxygen

and blue for nitrogen) are not shown directly, but the

bonds between atoms are shown as lines. Under "display", also try

other representations such as "sticks", "spacefill", "ball & stick"

and "cartoons". Exit rasmol under "file" -> "exit".

We will now prepare the protein structure to be simulated in gromacs.

Although we now have a starting structure for our protein, one might

have noticed that hydrogen atoms (which would appear white) are still missing from the

structure. This is because hydrogen atoms contain too few electrons to

be observed by x-ray crystallography at moderate resolutions. Also,

gromacs requires a molecular description (or topology) of the

molecules to be simulated before we can start, containing information

on e.g. which atoms are covalently bonded and other physical information. Both the generation of

hydrogen atoms and writing of the topology can be done with the

gromacs program pdb2gmx:

pdb2gmx -f 1PGB.pdb -o conf.pdb

when prompted for the force-field to be used, choose "6" (OPLS-AA/L

all-atom force field). View the result with:

rasmol conf.pdb

See the added hydrogens? The topology file written by pdb2gmx is called "topol.top". Have a

look at the contents of the file using:

more topol.top

you will see a list of all the atoms (with masses, charges), followed

by bonds (covalent bonds connecting the atoms), angles, dihedral

angles etc. Near the very end of the topology (in the "[molecules]"

section) there is a summary of the simulation system, including the

protein and 24 crystallographic water molecules.

The topology file thus contains all the physical information about all

interactions between the atoms of the protein (bonds, angles, torsion

angles, Lennard-Jones interactions and electrostatic interactions).

The next step in setting up the simulation system is to solvate the

protein in a water box, to mimick a physiological environment. For that, we first need to define a

simulation box. In this case we will generate a rectangular box with

the box-edges at least 7 Angstroms apart from the protein surface:


editconf -f conf.pdb -o box.pdb -d 0.7

(note that gromacs uses units of nanometers). View the result

with

rasmol box.pdb
and, in rasmol, type:

unitcell true

Now we fill the simulation box with SPC water using genbox:

genbox -cp box.pdb -cs spc216 -o water.pdb -p topol.top

Again, view the output (water.pdb) with rasmol. Now the simulation

system is almost ready. Before we can start the dynamics, we must

perform an energy minimisation, to alleviate any bad contacts (atoms

overlapping such that a significant repulsion would result, causing

numerical problems in the simulation) that

might be present in the system. For this we need a parameter file,

specifying which type of minimisation should be carried out, the

number of steps, etc. For your convenience a file called "em.mdp" has

already been prepared and can be downloaded from here. View the file

with "more" to see its contents. We use the gromacs preprocessor to

prepare our energy minimisation:

grompp -f em.mdp -c water.pdb -p topol.top -o em.tpr

This collects all the information from em.mdp, the coordinates from

water.pdb and the topology from topol.top, checks if the contents are

consistent and writes a unified output file: em.tpr, which will be

used to carry out the minimisation:

mdrun -v -s em.tpr -c em.pdb

The output shows that already the initial energy was rather low, so

in this case there were hardly any bad contacts. Having a look at

"em.pdb" shows that the structure hardly changed during

minimisation.


The careful user may have noticed that grompp gave a warning:

System has non-zero total charge: -4.

Before we continue with the dynamics, we should neutralise

this net charge of the simulation system. This

is to prevent artefacts that would arise as a side effect caused by

the periodic boundary conditions used in the simulation. A net charge

would result in an electrostatic repulsion between neighbouring

periodic images. Therefore, 4 sodium ions will be added to the system:

/usr/global/whatif/genion -s em.tpr -o ions.pdb -np 4

Type "12" to select the water group (SOL) from which 4 water molecules

will be replaced by sodium ions.

The output (ions.pdb) can be checked with rasmol. To better see the

ions, type (in rasmol):

select na

cpk

Since we now changed the topology of the system (4 water molecules

were replaced by sodium ions), we have to manually adapt the topology:

xedit topol.top

browse towards the end of the file, and change the number of SOL

(water) molecules (from 2183 to 2179). Then, add a line with "NA+ 4",

(note the space between "+" and "4") and do a "save" (twice!) followed by

"quit". Just to be on the safe side, we

repeat the energy minimisation, now with the ions included

(remember to (re)run grompp to create a new run input file whenever

changes to the topology, or coordinates have been made):

grompp -f em.mdp -c ions.pdb -p topol.top -o em.tpr

mdrun -v -s em.tpr -c em.pdb

Now we have all that is required to start the dynamics. Again, a

parameter file has been prepared for the simulation, and can be

downloaded here. Please browse

through the file "md.mdp" (using "more") to get an idea of the

simulation parameters. The gromacs online manual describes all

parameters in detail here.

Please don't worry in this stage about all individual parameters,

we've chosen common values typical for protein simulations.

Again, we use the gromacs preprocessor to prepare the simulation:

grompp -f md.mdp -c em.pdb -p topol.top -o md.tpr

and start the simulation!

mdrun -v -s md.tpr -c md.pdb -nice 0

The simulation is running now, and depending on the speed and load of

the computer, the simulation will run for a number of minutes. Until

the simulation is finished, relax, lean back or drink a coffee, before

clicking here to continue with the analysis of the simulation.


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