Water at the Macromolecular Surface - Advances in Chemistry (ACS

May 5, 1994 - 3 Laboratory of Biochemistry and Metabolism, National Institute of Diabetes, ... Physics, IBILCE-UNESP, Sao Jose de Rio Preto, Sao Paulo...
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9 Water at the Macromolecular Surface

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Solvation Energy and Functional Control V. Adrian Parsegian , R. Peter Rand , Marcio Colombo , and Donald C. Rau 1

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3,4

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Laboratory of Structural Biology, Division of Computer Research and Technology, National Institutes of Health, Bethesda, MD 20892 Biological Sciences, Brock University, St. Catharines, Ontario L2S 3A1, Canada Laboratory of Biochemistry and Metabolism, National Institute of Diabetes, Digestive, and Kidney Disease National Institutes of Health, Bethesda, MD 20892 1

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The contribution of hydration to the energetics of molecular conformation and assembly has been recognized for a long time, but has been difficult to measure. We use osmotic stress to measure the forces and energies in molecular assemblies. The same strategy can be used to measure the contribution of water to the chemical free energy change of individually functioning molecules. We describe, as examples, the contribution of water to the gating of membrane channels to the binding of oxygen to hemoglobin; and to the forces between bilayer membranes, within nonbilayer lipid assemblies, and on macromolecular surfaces. From the magnitude of their energies we conclude that hydration-dehydration reactions play an important but neglected role in molecular function.

TTHE

M E A S U R E M E N T O F I N T E R M O L E C U L A R F O R C E S a n d o f the solvation o f

biomolecules c a n give n e w physical insight into the control o f cellular processes. O u r a i m i n this chapter is to illustrate the role o f such measure­ ments i n molecular function. It has b e e n k n o w n f o r some time that the forces encountered w h e n macromolecules o r membranes approach contact are Current address: Department of Physics, I B I L C E - U N E S P , Sao Jose de Rio Preto, Sao Paulo, Brazil 15054

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0065-2393/94/0235-0177$08.00/0 © 1994 American Chemical Society

Blank and Vodyanoy; Biomembrane Electrochemistry Advances in Chemistry; American Chemical Society: Washington, DC, 1994.

178

BIOMEMBRANE ELECTROCHEMISTRY

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generally exponentially varying " h y d r a t i o n forces" c o m i n g f r o m the energy n e e d e d to remove water f r o m between membranes or between macromolecular surfaces. Q u i t e recently, it became apparent that "allosterism", changes i n the functioning f o r m o f proteins, might entail substantial changes i n the n u m b e r o f water molecules devoted to solvating the p r o t e i n surface. If data f r o m the systems examined so far are typical, that is, i f molecular h y d r a t i o n - d e h y d r a t i o n is a part o f functional control, t h e n measured h y d r a ­ tion energies can b e an important but neglected part o f molecular f u n c t i o n . O u r first task is hnguistic: to present i n tandem the mathematical forms that describe interaction forces together w i t h the expressions for the c h e m i c a l free energies acting to change macromolecular conformation. W i t h this vocabulary w e then review several examples o f measured forces a n d confor­ mation reactions. W e conclude b y c o m p a r i n g the magnitude o f energies derived f r o m forces w i t h the energies n e e d e d to change properties o f proteins or o f l i p i d assemblies.

The Language of Hydration Forces T h e hydration pressure, F ( i n dynes p e r centimeter squared or force p e r unit area), acts between parallel membranes a n d varies exponentially w i t h a decay distance λ ( I - J O ) so that one may write F =

F exp(-d /X) 0

w

T h e base 10 logarithm o f the fitted coefficient F can be f r o m 9 to 12 w i t h F i n dynes p e r centimeter squared, λ can b e f r o m 1 to 2.5 Â (6), a n d d is membrane separation. W h e n pressure F is integrated, it becomes an energy p e r unit area, E, a n d 0

0

w

Ε = \P w i t h respect to infinite separation, an energy that can be o n the o r d e r o f 100 e r g / c m for polar surfaces brought to anhydrous contact. It is instructive to convert these hydration energies o f contact into c h e m i c a l units. F o r example, over a 1 X 1-nm patch o f m e m b r a n e the energy o f 100 e r g / c m becomes 2

2

100 e r g / c m

2

Χ 10"

1 4

cm

2

= 10~

1 2

erg/nm

I f w e divide b y t h e r m a l energy units kT = 4 X 1 0 " becomes 25fcT/nm

1 4

2

erg, this energy

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Blank and Vodyanoy; Biomembrane Electrochemistry Advances in Chemistry; American Chemical Society: Washington, DC, 1994.

9.

PARSEGIAN ET AL.

R e c a l l i n g that kT have

Water at the Macromolecular Surface

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p e r particle is equivalent to 0.6 k c a l / m o l o f particles, w e

15 k c a l / ( m o l · n m patch o f m e m b r a n e ) 2

T h e area 1 n m is o n the order o f the area o c c u p i e d b y one or two p h o s p h o l i p i d molecules i n membranes. T h e energy, 15 k c a l / m o l , is already o n the order o f the high-energy bonds i n v o l v e d i n the p r o d u c t i o n - u t i l i z a t i o n o f adenosine triphosphate.

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B e t w e e n parallel linear molecules i n w e l l - d e f i n e d arrays, exponential variation is again observed (11-13). T h e w o r k o f transfer o f water f r o m such an array is expressed i n terms o f a c h e m i c a l potential o f water or, equivalently, o f an osmotic stress I I o n the lattice as a f u n c t i o n o f a lattice parameter such as lattice interaxial distance d : o s m

{

n When

there

osm

=n exp(-d A) o

1

is p u r e l y repulsive interaction between

parallel linear

molecules, the decay distance λ can range f r o m 2.5 to 3.5 Â. U s u a l l y the molecules pack into a hexagonal array. T h e osmotic stress o n the lattice can be converted to a force p e r unit length /

between parallel molecules.

Specifically ( I I ) ,

/K) = n

osm

K)(4/^3)

Because i n most cases λ