Collagen structure: The molecular source of the tendon magic angle effect

Gary D. Fullerton, Andres Rahal

Research output: Contribution to journalArticle

78 Citations (Scopus)

Abstract

This review of tendon/collagen structure shows that the orientational variation in MRI signals from tendon, which is referred to as the "magic angle" (MA) effect, is caused by irreducible separation of charges on the main chain of the collagen molecule. These charges are held apart in a vacuum by stereotactic restriction of protein folding due in large part to a high concentration of hydroxyproline ring residues in the amino acids of mammalian collagen. The elevated protein electrostatic energy is reduced in water by the large dielectric constant of the highly polar solvent (κ ∼ 80). The water molecules serve as dielectric molecules that are bound by an energy that is nearly equivalent to the electrostatic energy between the neighboring positive and negative charge pairs in a vacuum. These highly immobilized water molecules and secondary molecules in the hydrogen-bonded water network are confined to the transverse plane of the tendon. Orientational restriction causes residual dipole coupling, which is directly responsible for the frequency and phase shifts observed in orientational MRI (OMRI) described by the MA effect. Reference to a wide range of biophysical measurements shows that native hydration is a monolayer on collagen hm = 1.6 g/g, which divides into two components consisting of primary hydration on polar surfaces hpp = 0.8 g/g and secondary hydration hs = 0.8 g/g bridging over hydrophobic surface regions. Primary hydration further divides into side-chain hydration hpsc = 0.54 g/g and main-chain hydration hpmc = 0.263 g/g. The main-chain fraction consists of water that bridges between charges on the main chain and is responsible for almost all of the enthalpy of melting ΔH = 70 J/g-dry mass. Main-chain water bridges consist of one extremely immobilized Ramachandran water bridge per tripeptide hRa = 0.0658 g/g and one double water bridge per tripeptide hdwb = 0.1974 g/g, with three water molecules that are sufficiently slowed to act as the spin-lattice relaxation sink for the entire tendon.

Original languageEnglish (US)
Pages (from-to)345-361
Number of pages17
JournalJournal of Magnetic Resonance Imaging
Volume25
Issue number2
DOIs
StatePublished - Feb 2007

Fingerprint

Molecular Structure
Tendons
Collagen
Water
Vacuum
Static Electricity
Protein Folding
Hydroxyproline
Freezing
Hydrogen
Amino Acids

Keywords

  • Bound water
  • Collagen
  • Collagen hydration
  • Double water bridges
  • Hydration
  • Magic angle effect
  • MRI contrast phenomena
  • Protein hydration
  • T1 relaxation
  • T2 relaxation
  • Tendon
  • Water binding
  • Water bridges

ASJC Scopus subject areas

  • Radiology Nuclear Medicine and imaging
  • Radiological and Ultrasound Technology

Cite this

Collagen structure : The molecular source of the tendon magic angle effect. / Fullerton, Gary D.; Rahal, Andres.

In: Journal of Magnetic Resonance Imaging, Vol. 25, No. 2, 02.2007, p. 345-361.

Research output: Contribution to journalArticle

Fullerton, Gary D. ; Rahal, Andres. / Collagen structure : The molecular source of the tendon magic angle effect. In: Journal of Magnetic Resonance Imaging. 2007 ; Vol. 25, No. 2. pp. 345-361.
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