1067
Acta Crvst. (1996). D52, 1067-1074
An X-ray Analysis of Native Monoclinic Lysozyme. A Case Study on the Reliability of
Refined Protein Structures and a Comparison with the Low-Humidity Form in Relation to
Mobility and Enzyme Action
H. G. NAGENDRA, C. SUDARSANAKUMAR AND M. VIJAYAN
Molecular Biophysics Unit, Indian Institute of Science, Bangalore-560 012, India. E-mail: mv@mbu.iisc, ernet, in
(Received 8 April 1995: accepted 12 Februao" 1996)
Abstract
The atomic models of native monoclinic lysozyme
obtained by refinement at Bangalore and elsewhere
[Young, Dewan, Nave & Tilton (1993). J. Appl. Co'st.
26, 309-319] differed significantly in the flexible
regions of the protein molecule. The two models were
reconciled starting from regions where they were in
reasonable agreement to produce an improved model
which yielded an R value of 0.169 for 12 816 observed
reflections in the 10-2,~, resolution range. The recon-
ciled model was compared with the structure of the 88 %
relative humidity form obtained through a water-
mediated transformation [Madhusudan, Kodandapani
& Vijayan (1993). Acta Co, st. D49, 234-245]. Parts of
the flexible regions of the molecule register significant
movements during the transformation. The changes
resulting from the transformation from the native to the
low-humidity forms are pronounced in many of the side
chains in the active-site region, thus indicating the
relationship between hydration, mobility and enzyme
action. The fact that the overall changes in molecular
geometry resulting from water-mediated transformation
are similar to those which occur during enzyme action,
further emphasizes this relationship.
1. Introduction
We have been exploring the variability in protein
hydration and its structural consequences, including its
implication to enzyme action, using an approach
involving water-mediated transformations induced by
changes in the solvent content in protein crystals
resulting from systematic changes in environmental
humidity (Salunke, Veerapandian & Vijayan, 1984;
Salunke, Veerapandian, Kodandapani & Vijayan, 1985;
Kodandapani, Suresh & Vijayan, 1990; Madhusudan &
Vijayan, 1991; Madhusudan, Kodandapani & Vijayan,
1993; Radhakishan, Chandra, Sudarsanakumar, Suguna
& Vijayan, 1995; Nagendra, Sudarsanakumar &
Vijayan, 1995). This exploration has also led to the
elucidation of the nature of mobility in hen egg-white
lysozyme and bovine ribonuclease A and the identifica-
tion of the relatively invariant features in their hydration
© 1996 International Union of Crystallography
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shell (Madhusudan & Vijayan, 1991; Radhakishan et
al., 1995). Among the water-mediated transformations,
the one exhibited by monoclinic lysozyme was the most
impressive. During the transformation which occurs
around a relative humidity of 90% and is accompanied
by substantial loss of water, the two crystallographically
independent protein molecules in the native form
become equivalent. The solvent content of the low-
humidity 88% form is as low as 22% which is perhaps
the lowest observed in any protein crystal until now.
This form diffracts substantially better than the native
form and its X-ray analysis has also led to useful
information on the water structure associated with
proteins (Madhusudan et al., 1993). A detailed
comparison of this structure with that of the native
form could not be carried out as the available structure
of native monoclinic lysozyme was only incompletely
refined (Rao, Hogle & Sundaralingam, 1983). There-
fore, we undertook a thorough refinement of the
structure of the native crystals using data collected on
an area detector with the partially refined structure
available in the Protein Data Bank (Bernstein et al.,
1977) as the starting model. By the time this refinement
was completed, another independent refinement of the
structure using diffractometer data with the same
starting model became available (Young, Dewan,
Nave & Triton, 1993). A comparison of these two
refined structures and the procedures adopted for the
reconciliation of the differences between them form the
subject matter of the first part of this paper.
Problems associated with the refinement of protein
structures especially the possibility of arriving at a
crystallographically acceptable, but erroneous, refined
structure, have been a matter of concern from the
early days of protein structure refinement (Chambers
& Stroud, 1977; Vijayan, 1980). Several investiga-
tions have been carried out to explore these problems
through comparisons of the parameters of the same
structure obtained through refinement by different
groups, different data sets or both. The results of
three of the most recent of these investigations
(Daopin, Davies, Schlunegger & Grutter, 1994;
Harata, 1994; Fields et al., 1994) underline the
reliability of refined structures. The results of a fourth
Acta Crystallographica Section D
ISSN 0907-4449 © 1996