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Chemistry 1951

The Structure of Proteins: Two Hydrogen-Bonded Helical Configurations of the Polypeptide Chain

Linus Pauling, Robert Corey & Herman Branson

Fold a protein chain by the rules of the chemical bond, and one shape falls out: the α-helix.

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In depth · the introduction

Before anyone had ever seen a protein clearly, Linus Pauling folded one in his head — using nothing but the rules of the chemical bond.

The big idea

Proteins are long chains of amino acids, and to work they must fold into precise shapes. In 1951 Pauling and his colleagues asked a daring question: what shapes can the chain take if you obey, exactly, the rules chemistry already knew — how long each bond is, how stiff each link is, and where the tiny attractions called hydrogen bonds can form? The answer was almost forced. One especially neat shape kept appearing: a right-handed coil, like a spiral staircase, which they named the α-helix. Each turn of the coil is stitched to the next by hydrogen bonds, which makes it sturdy and self-supporting.

How it came about

Pauling had the crucial clue years earlier: the link between two amino acids — the peptide bond — is flat and rigid, not free to twist, because of the way its electrons are shared. With the exact shapes of amino acids measured in his Caltech lab by Robert Corey, and the geometry worked out in detail by the physicist Herman Branson, Pauling looked for coils in which every hydrogen bond came out straight and the right length.

A rival team in Cambridge had searched the year before and failed, because they had assumed each turn must hold a whole number of amino acids. Pauling let go of that assumption — his helix has about three and a half per turn — and the structure clicked into place. He is said to have worked part of it out while ill in bed, folding a paper chain by hand until the bonds met.

Why it mattered

It was the first time anyone had correctly predicted a piece of a protein's shape, and it was confirmed almost at once when Max Perutz spotted exactly the X-ray signal the α-helix demanded. It showed that the shapes of life's molecules follow from plain chemistry — and it pioneered the model-building method that, just two years later, cracked the structure of DNA.

A way to picture it

Think of a spiral staircase made of paper links, where a point on the rail sits directly above the matching point one turn below. Now imagine tiny magnets that only click when two links sit squarely above each other, four steps apart. The only way to build the staircase so every magnet clicks is to give each turn about three and a half steps — not three, not four. Those magnets are the hydrogen bonds, and that clicked-together staircase is the α-helix. Once it is zipped up the whole length, it holds its own shape.

A coil you grow with a slider; dashed lines show each hydrogen bond reaching four beads ahead, holding the spiral together. A toggle compares it with a tighter coil whose bonds reach three beads ahead.

Where it sits

Pauling's α-helix and his model-building style directly shaped the DNA double helix two years later (see watson-crick-1953); both are right-handed coils held together by hydrogen bonds. The α-helix is one of the basic alphabet-letters of protein shape — and predicting how a chain of amino acids arranges those letters into a whole fold is exactly the problem that AlphaFold (see alphafold-2021) finally solved seventy years on.

The original document
Original source text
L. Pauling, R. B. Corey & H. R. Branson · Proc. Natl. Acad. Sci. USA 37 (1951): 205–211 · communicated February 28, 1951
The approach
The paper builds protein structures from the ground up — from the established geometry of the chemical bond, rather than from low-resolution X-ray pictures. The peptide group is taken as rigid and planar, a consequence of the partial double-bond character of the C–N bond in Pauling's resonance theory, with bond lengths and angles fixed by the crystal structures of amino acids and small peptides determined in Corey's laboratory.
The hydrogen-bond rule
Every backbone N–H and C=O is required to take part in a nearly straight hydrogen bond of about 2.72 Å. Imposing this on a regularly coiled chain leaves only a few possible helices — and, crucially, they need not repeat after a whole number of residues per turn, the restriction that had defeated the earlier Cambridge survey.
Two helices
Two configurations satisfy the rules: a tightly wound helix with about 3.7 residues per turn — the α-helix, in which each carbonyl is hydrogen-bonded to the amide of the residue four along — and a wider helix with about 5.1 residues per turn. The α-helix rises about 1.5 Å per residue and repeats every 5.4 Å along its axis.
[ … ]
The prediction and its test
Companion papers in the same 1951 issue extend the scheme to the pleated sheet and further chain configurations. The decisive test was the α-helix's predicted 1.5 Å axial repeat, which Max Perutz soon found as a strong X-ray reflection in hair keratin and in haemoglobin.
Gates and Crellin Laboratories of Chemistry, California Institute of Technology · 1951