JB Review J. Biochem. 117, 1-6 (1995)

Birth of the Sliding Filament Concept in Muscle Contraction

Koscak Maruyama

Office of the President, Chiba University, Inage-ku, Chiba 263

Received for publication, September 12, 1994

Why were the two classical papers by A.F. Huxley and R. Niedergerke and by H.E. Huxley

and J. Hanson on the sliding filament concept in muscle contraction published in the same

issue (May 22, 1954) of Nature? This historical survey reveals the background of the two

groups' monumental work.

Key words: Andrew Huxley, Hugh Huxley, Jean Hanson, muscle contraction, Rolf

Niedergerke, sliding filament concept.

In the 1954 May 22 issue of Nature, two classical papers

appeared: "Structural changes in muscle during contrac

tion" by A.F. Huxley and R. Niedergerke (1) and "Changes

in the cross-striations of muscle during contraction and

stretch and their structural interpretation" by H.E. Huxley

and J. Hanson (2). It is generally accepted that these two

short papers presented the first evidence for the sliding

filament concept in muscle contraction (3, 4).

By that time it was a prevailing opinion under the

influence of English biophysicist William Astbury (1898-

1961) and Swiss chemist Kurt H. Meyer (1883-1953) that

muscle contracted as a consequence of conformational

changes of the filamentous proteins (5). For example,

wide-angle X-ray diffraction work by Astbury and Dickin

son had suggested that the changes of the structures of

muscle contractile proteins from the ƒÀ form (ƒÀ sheet) to the

a form (a helix) occurred during muscle contraction (6),

although this change was later denied by Astbury himself in

1947 (7). Morales presented a primitive type of the sliding

concept in 1948 (8).

The sliding filament concept was revolutionary at the

time, and is now regarded as a major universal mechanism

of biomotility, not only in myosin/actin-based motility but

also in the kinesin, dynein/microtubule-based motility of

cells. A molecular motor (myosin, kinesin, and dynein)

slides along a rail (actin filament or microtubule) in a

definite direction dictated by the polarity of the rail,

utilizing the energy derived from the splitting of ATP (Fig.

la). When the motors are appropriately immobilized, then

the rail is moved in a definite direction leading to the

changes in length of the muscle filaments (sarcomere

length) (Fig. lb). One can regard this sliding filament

concept as a paradigm in biological sciences as Thomas

Kuhn has defined.

This article is mainly concerned with the events leading

to the simultaneous publication of the two Nature papers.

Attention will be especially directed to the roles played by

both Huxleys and Hanson, and to their mutual relationship

at that time.

The Huxley-Niedergerke work

Andrew Fielding Huxley, born at Hampstead, London, in

1917, was educated as a physiologist at Trinity College,

Cambridge, and was an assistant director of research at the

Department of Physiology, Cambridge, from 1951 to 1959.

In 1951 he changed his research subject from nerve to

muscle after completing the monumental papers with Alan

Hodgkin on the excitation mechanism of squid giant axon

(Nobel Prize for Physiology or Medicine, 1963) (10, 11).

Huxley had become interested in the structure and function

of striated muscle through the stimulating lectures of David

Hill, a muscle physiologist [son of a great muscle physiolo

gist, Archibald V. Hill (1886-1977), Nobel laureate

(1922)], while he was asked to take over Hill's lectures in

1948 (10).

Huxley started his muscle work by developing a new

interference microscope suitable for the observation of

striation changes during muscle contraction. Assisted by

the firm of R. & J. Beck, he undertook to construct a

high-power interference microscope, and his hand-made

microscope was successfully in use (12) by the end of 1952

(10).

In the autumn of 1952, Rolf Niedergerke, born at

Mulheim-Ruhr, Germany, in 1921, joined Huxley's labora

tory (13). He had worked on isolated nerve fibers in

Alexander von Muralt's Institute in Berne. Robert

Stampfli, who taught Niedergerke nerve fiber dissection,

recommended him to Huxley as a collaborator for isolation

of single muscle fibers (13). Niedergerke had been a

demonstrator in physiology at Gottingen (13).

Huxley and Niedergerke quickly reached a preliminary

conclusion that the A band width in a sarcomere was fairly

constant during passive stretch, isometric contraction and

also isotonic contraction, to a certain extent. The force was

generated while the A band remainded invariant during

isometric contraction. These results were obtained by early

1953 (11). However, completion of the work was delayed

due to Huxley's duties as the editor of the Journal of

Physiology and the secretary of the Council of Trinity

College (11).

Niedergerke, who had read a number of papers on the

myofibrillar structure by 19th century German workers,

pointed out to Huxley the idea by Wilhelm Krause (1869)

(14) that the A band (width, 1.5ƒÊm) in mammalian muscle

consisted of longitudinally parallel rodlets (filaments) and

the rodlets did not change in length during contraction, but

attracted "fluid" from the adjacent I bands. This is a

prototype of the sliding concept, if "fluid" is read as

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