Evidence of an asymmetrical endophenotype in congenital fibrosis of extraocular muscles type 3 resulting from TUBB3 mutations

Invest Ophthalmol Vis Sci. 2010 Sep;51(9):4600-11. doi: 10.1167/iovs.10-5438. Epub 2010 Apr 14.

Abstract

Purpose: Orbital magnetic resonance imaging (MRI) was used to investigate the structural basis of motility abnormalities in congenital fibrosis of the extraocular muscles type 3 (CFEOM3), a disorder resulting from missense mutations in TUBB3, which encodes neuron-specific beta-tubulin isotype III.

Methods: Ophthalmic examinations in 13 volunteers from four CFEOM3 pedigrees and normal control subjects, were correlated with TUBB3 mutation and MRI findings that demonstrated extraocular muscle (EOM) size, location, contractility, and innervation.

Results: Volunteers included clinically affected and clinically unaffected carriers of R262C and D417N TUBB3 amino acid substitutions and one unaffected, mutation-negative family member. Subjects with CFEOM3 frequently had asymmetrical blepharoptosis, limited vertical duction, variable ophthalmoplegia, exotropia, and paradoxical abduction in infraduction. MRI demonstrated variable, asymmetrical levator palpebrae superioris and superior rectus EOM atrophy that correlated with blepharoptosis, deficient supraduction, and small orbital motor nerves. Additional EOMs exhibited variable hypoplasia that correlated with duction deficit, but the superior oblique muscle was spared. Ophthalmoplegia occurred only when the subarachnoid width of CN3 was <1.9 mm. A-pattern exotropia was frequent, correlating with apparent lateral rectus (LR) muscle misinnervation by CN3. Optic nerve (ON) cross sections were subnormal, but rectus pulley locations were normal.

Conclusions: CFEOM3 caused by TUBB3 R262C and D417N amino acid substitutions features abnormalities of EOM innervation and function that correlate with subarachnoid CN3 hypoplasia, occasional abducens nerve hypoplasia, and subclinical ON hypoplasia that can resemble CFEOM1. Clinical and MRI findings in CFEOM3 are more variable than those in CFEOM1 and are often asymmetrical. Apparent LR innervation by the inferior rectus motor nerve is an overlapping feature of Duane retraction syndrome and CFEOM1. These findings suggest that CFEOM3 is an asymmetrical, variably penetrant, congenital cranial dysinnervation disorder leading to secondary EOM atrophy.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Abducens Nerve / abnormalities
  • Abducens Nerve / pathology
  • Adolescent
  • Adult
  • Amino Acid Substitution
  • Family Health
  • Female
  • Fibrosis
  • Humans
  • Magnetic Resonance Imaging
  • Male
  • Middle Aged
  • Muscular Atrophy / congenital
  • Muscular Atrophy / genetics
  • Muscular Atrophy / pathology
  • Mutation, Missense
  • Oculomotor Muscles / abnormalities*
  • Oculomotor Muscles / pathology*
  • Oculomotor Nerve / abnormalities
  • Oculomotor Nerve / pathology
  • Oculomotor Nerve Diseases / congenital
  • Oculomotor Nerve Diseases / genetics*
  • Oculomotor Nerve Diseases / pathology*
  • Optic Nerve / abnormalities
  • Optic Nerve / pathology
  • Pedigree
  • Phenotype
  • Tubulin / genetics*
  • Visual Acuity
  • Young Adult

Substances

  • TUBB3 protein, human
  • Tubulin