Phosphorylase kinase (EC 2.7.1.38) plays a key role
in the neuronal and hormonal regulation of glycogenoly-
sis in skeletal muscle. The enzyme has a complex molec-
ular organization and forms a hexadecamer consisting of
four different subunits with stoichiometry (αβγδ)
4
and
molecular mass 1320 kD [1-3]. It was shown that the γ-
subunit (44.7 kD) has a catalytic function [4], whereas
the α- (138.4 kD), β- (125.2 kD), and δ-subunits
(16.7 kD) are regulatory ones [5, 6], with the δ-subunit
being identical to the Ca
2+
-binding protein calmodulin
[7].
The oligomeric state of phosphorylase kinase
depends on the concentration of Ca
2+
and Mg
2+
. Ca
2+
and Mg
2+
stimulate the enzymatic activity by inducing
changes in the tertiary and quaternary structure of the
phosphorylase kinase molecule [8, 9]. In the absence of
Ca
2+
and Mg
2+
the enzyme exists as a monomer and a
dimer with sedimentation coefficients s
20,w
= 23 S (which
corresponds to the molecular mass 1320 kD) and s
20,w
=
36.5 S, respectively [1, 10]. It should be noted that in this
case the monomer of phosphorylase kinase is assumed to
be a hexadecamer (αβγδ)
4
. Upon addition of 0.1 mM
Ca
2+
and 10 mM Mg
2+
, higher-order oligomers are
formed [10, 11].
In skeletal muscle, about 40% of phosphorylase
kinase together with other enzymes of glycogen metabo-
lism is localized on the surface of glycogen granules [12].
It is known that glycogen increases 2-3-fold the affinity of
phosphorylase kinase to its protein substrate, glycogen
phosphorylase b [13, 14]. The α-subunit of the enzyme
plays an important role in the contact of phosphorylase
kinase with glycogen [15]. In addition, the regulatory α-
subunit together with the catalytic γ-subunit can interact
with the phosphorylase kinase substrate, glycogen phos-
phorylase b [16]. Previously we proposed a model of an
ordered binding of glycogen phosphorylase b and phos-
phorylase kinase on the glycogen particle, which explains
the increase in the tightness of the binding of phosphory-
lase kinase with glycogen in the presence of glycogen
phosphorylase b [17].
It is known that some enzymes of the
protein–glycogen complex in skeletal muscle have affin-
ity to flavins. The flavin-binding sites in glycogen phos-
phorylase a were discovered by Sprang et al. [18].
Localization of the FMN-binding sites in the molecule
of glycogen phosphorylase a was determined by X-ray
analysis. We have studied in detail the interaction of
flavins (riboflavin, FMN, and FAD) with glycogen phos-
phorylase b [19-23]. All flavins studied have inhibitory
effect on the enzyme, with FMN having the strongest
ISSN 0006-2979, Biochemistry (Moscow), 2006, Vol. 71, No. 6, pp. 652-657. © Pleiades Publishing, Inc., 2006.
Original Russian Text © V. F. Makeeva, N. A. Chebotareva, I. E. Andreeva, N. B. Livanova, B. I. Kurganov, 2006, published in Biokhimiya, 2006, Vol. 71, No. 6, pp. 808-814.
652
* To whom correspondence should be addressed.
Interaction of Phosphorylase Kinase from Rabbit Skeletal Muscle
with Flavin Adenine Dinucleotide
V. F. Makeeva*, N. A. Chebotareva, I. E. Andreeva, N. B. Livanova, and B. I. Kurganov
Bach Institute of Biochemistry, Russian Academy of Sciences, Leninsky pr. 33,
119071 Moscow, Russia; fax: (495) 954-2732; E-mail: makeeva@inbi.ras.ru
Received August 18, 2005
Abstract—The interaction of flavin adenine dinucleotide (FAD) with rabbit skeletal muscle phosphorylase kinase has been
studied. Direct evidence of binding of phosphorylase kinase with FAD has been obtained using analytical ultracentrifuga-
tion. It has been shown that FAD prevents the formation of the enzyme–glycogen complex, but exerts practically no effect
on the phosphorylase kinase activity. The dependence of the relative rate of phosphorylase kinase–glycogen complex for-
mation on the concentration of FAD has cooperative character (the Hill coefficient is 1.3). Under crowding conditions in
the presence of 1 M trimethylamine-N-oxide (TMAO), FAD has an inhibitory effect on self-association of phosphorylase
kinase. The data suggest that the complex of glycogen metabolism enzymes in protein–glycogen particles may function as a
flavin depot in skeletal muscle.
DOI: 10.1134/S0006297906060095
Key words: phosphorylase kinase, FAD, glycogen, trimethylamine-N-oxide, turbidimetry, sedimentation, association