12
J. Mol Biol. (1987) 196, 641-6.56
Interior and Surface of Monomeric Proteins
Susan Miller^ Joel Janin^, Arthur M. Lesk^ * f
and Cyrus Chothia^ ^
' Christopher Ingold Laboratories, University College London
20 Gordon Street. London WCIG OA.l, England
^ Laboratoire de Biologic Physicochimique, Universite Paris-Sud
Bat. 433, 91405 Orsay, France
^ Medical Research Council, Laboratory of Molecular Biology
Hills Road, Cambridge CB2 2QH, England
'^ Biocomputing Programme, EMBL, Meyerhofstr. 1, Postfach 1022.09
D-6900 Heidelberg, Federal Republic of Germany
(Received 6 October 1986, and in revised form 13 March 1987)
The solvent-accessible surface area (AJ of 46 monomeric proteins is calculated using
atomic co-ordinates from high-resolution and well-refined crystal structures. The .4^ of
these proteins can be determined to within 1 to 2 % and that of their individual residues to
within 10 to 20%.
The A^ values of proteins are correlated with their molecular weight (M,) in the range 4000
to 35,000: the power law A^ = d-Z M"^^ predicts protein A^ values to within 4% on
average. The average water-accessible surface is found to be 57% non-polar, 24% polar and
19% charged, with 5% root-mean-square variations. The molecular surface buried inside
the protein is 58% non-polar, 39% polar and 4% charged. The buried surface contains
more uncharged polar groups (mostly peptides) than the surface that remains accessible,
but many fewer charged groups.
On average, 15% of residues in small proteins and 32% in larger ones may be classed as
"buried residues", having less than 5% of their surface accessible to the solvent. The
accessibilities of most other residues are evenly distributed in the range 5 to 50%. Although
the fraction of buried residues increases with molecular weight, the amino acid compositions
of the protein interior and surface show no systematic variation with molecular weight,
except for small proteins that are often very rich in buried cysteines.
From amino acid compositions of protein surfaces and interiors we calculate an effective
coefficient of partition for each type of residue, and derive an implied set of transfer free
energy values. This is compared with other sets of partition coefficients derived directly
from experimental data. The extent to which groups of residues (charged, polar and non-
polar) are buried within proteins correlates well with their hydrophobicity derived from
amino acid transfer experiments. Within these three groups, the correlation is low.
1. Introduction
The polypeptide chains of globular proteins fold
into compact shapes, in which large parts of the
chain are shielded from contact with the solvent. It
is believed that this shielding is the primary source
of free energy stabilizing the native conformation.
Kauzmann (1959) reviewed the forces that maintain
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the structure of globular proteins: covalent bonds,
dispersion forces (van der Waals' forces), salt
bridges, hydrogen bonds and "hydrophobic bonds",
which arise from the preference of non-polar
compounds for non-aqueous solvents, Kauzmann
estimated the strength of hydrophobic bonds and
pointed out that they are largely entropic in nature,
in contrast to other bonds, which are mostly
enthalpic. The contribution of hydrophobic bonds
to the free energy of folding of a protein in water
should be related to the partition coefficient of
model organic compounds between water and
© 1987 Academic Press Inc. (London) Ltd.