Microtubule-dependent distribution of mRNA in adult cardiocytes

Am J Physiol Heart Circ Physiol. 2008 Mar;294(3):H1135-44. doi: 10.1152/ajpheart.01275.2007. Epub 2008 Jan 4.

Abstract

Synthesis of myofibrillar proteins in the diffusion-restricted adult cardiocyte requires microtubule-based active transport of mRNAs as part of messenger ribonucleoprotein particles (mRNPs) to translation sites adjacent to nascent myofibrils. This is especially important for compensatory hypertrophy in response to hemodynamic overloading. The hypothesis tested here is that excessive microtubule decoration by microtubule-associated protein 4 (MAP4) after cardiac pressure overloading could disrupt mRNP transport and thus hypertrophic growth. MAP4-overexpressing and pressure-overload hypertrophied adult feline cardiocytes were infected with an adenovirus encoding zipcode-binding protein 1-enhanced yellow fluorescent protein fusion protein, which is incorporated into mRNPs, to allow imaging of these particles. Speed and distance of particle movement were measured via time-lapse microscopy. Microtubule depolymerization was used to study microtubule-based transport and distribution of mRNPs. Protein synthesis was assessed as radioautographic incorporation of [3H]phenylalanine. After microtubule depolymerization, mRNPs persist only perinuclearly and apparent mRNP production and protein synthesis decrease. Reestablishing microtubules restores mRNP production and transport as well as protein synthesis. MAP4 overdecoration of microtubules via adenovirus infection in vitro or following pressure overloading in vivo reduces the speed and average distance of mRNP movement. Thus cardiocyte microtubules are required for mRNP transport and structural protein synthesis, and MAP4 decoration of microtubules, whether directly imposed or accompanying pressure-overload hypertrophy, causes disruption of mRNP transport and protein synthesis. The dense, highly MAP4-decorated microtubule network seen in severe pressure-overload hypertrophy both may cause contractile dysfunction and, perhaps even more importantly, may prevent a fully compensatory growth response to hemodynamic overloading.

Publication types

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

MeSH terms

  • Actins / biosynthesis
  • Adult
  • Autoradiography
  • Cardiomegaly / pathology
  • Cytoplasm / metabolism
  • DNA-Binding Proteins / metabolism
  • Fluorescent Antibody Technique
  • Humans
  • Kinetics
  • Microscopy, Electron
  • Microtubule-Associated Proteins / biosynthesis
  • Microtubule-Associated Proteins / genetics
  • Microtubules / metabolism*
  • Microtubules / ultrastructure
  • Muscle Proteins / biosynthesis
  • Myocytes, Cardiac / metabolism*
  • Myocytes, Cardiac / pathology
  • Myocytes, Cardiac / ultrastructure
  • Pulmonary Artery / cytology
  • Pulmonary Artery / metabolism
  • RNA, Messenger / biosynthesis
  • RNA, Messenger / metabolism*
  • RNA-Binding Proteins

Substances

  • Actins
  • DNA-Binding Proteins
  • Microtubule-Associated Proteins
  • Muscle Proteins
  • RNA, Messenger
  • RNA-Binding Proteins
  • ZBP1 protein, human