Nuclear matrix, nuclear envelope and premature aging syndromes in a translational research perspective

Semin Cell Dev Biol. 2014 May:29:125-47. doi: 10.1016/j.semcdb.2014.03.021. Epub 2014 Mar 22.

Abstract

Lamin A-related progeroid syndromes are genetically determined, extremely rare and severe. In the past ten years, our knowledge and perspectives for these diseases has widely progressed, through the progressive dissection of their pathophysiological mechanisms leading to precocious and accelerated aging, from the genes mutations discovery until therapeutic trials in affected children. A-type lamins are major actors in several structural and functional activities at the nuclear periphery, as they are major components of the nuclear lamina. However, while this is usually poorly considered, they also play a key role within the rest of the nucleoplasm, whose defects are related to cell senescence. Although nuclear shape and nuclear envelope deformities are obvious and visible events, nuclear matrix disorganization and abnormal composition certainly represent the most important causes of cell defects with dramatic pathological consequences. Therefore, lamin-associated diseases should be better referred as laminopathies instead of envelopathies, this later being too restrictive, considering neither the key structural and functional roles of soluble lamins in the entire nucleoplasm, nor the nuclear matrix contribution to the pathophysiology of lamin-associated disorders and in particular in defective lamin A processing-associated aging diseases. Based on both our understanding of pathophysiological mechanisms and the biological and clinical consequences of progeria and related diseases, therapeutic trials have been conducted in patients and were terminated less than 10 years after the gene discovery, a quite fast issue for a genetic disease. Pharmacological drugs have been repurposed and used to decrease the toxicity of the accumulated, unprocessed and truncated prelaminA in progeria. To date, none of them may be considered as a cure for progeria and these clinical strategies were essentially designed toward reducing a subset of the most dramatic and morbid features associated to progeria. New therapeutic strategies under study, in particular targeting the protein expression pathway at the mRNA level, have shown a remarkable efficacy both in vitro in cells and in vivo in mice models. Strategies intending to clear the toxic accumulated proteins from the nucleus are also under evaluation. However, although exceedingly rare, improving our knowledge of genetic progeroid syndromes and searching for innovative and efficient therapies in these syndromes is of paramount importance as, even before they can be used to save lives, they may significantly (i) expand the affected childrens' lifespan and preserve their quality of life; (ii) improve our understanding of aging-related disorders and other more common diseases; and (iii) expand our fundamental knowledge of physiological aging and its links with major physiological processes such as those involved in oncogenesis.

Keywords: Aging; Aging diseases; Lamins; Nuclear matrix; Progeria.

Publication types

  • Research Support, Non-U.S. Gov't
  • Review

MeSH terms

  • Aging, Premature / genetics
  • Aging, Premature / pathology*
  • Animals
  • Ataxia Telangiectasia / genetics
  • Cellular Senescence / genetics
  • DNA Repair / genetics
  • Disease Models, Animal
  • Humans
  • Lamin Type A / genetics*
  • Mice
  • Nuclear Lamina / genetics*
  • Progeria / genetics
  • Progeria / pathology*
  • Protein Processing, Post-Translational
  • Translational Research, Biomedical

Substances

  • LMNA protein, human
  • Lamin Type A