Zebrafish model of amyloid light chain cardiotoxicity: regeneration versus degeneration

Am J Physiol Heart Circ Physiol. 2019 May 1;316(5):H1158-H1166. doi: 10.1152/ajpheart.00788.2018. Epub 2019 Mar 15.

Abstract

Cardiac dysfunction is the most frequent cause of morbidity and mortality in amyloid light chain (AL) amyloidosis caused by a clonal immunoglobulin light chain (LC). Previously published transgenic animal models of AL amyloidosis have not recapitulated the key phenotype of cardiac dysfunction seen in AL amyloidosis, which has limited our understanding of the disease mechanisms in vivo, as well as the development of targeted AL therapeutics. We have developed a transgenic zebrafish model in which a λ LC derived from a patient with AL amyloidosis is conditionally expressed in the liver under the control of the Gal4 upstream activation sequence enhancer system. Circulating LC levels of 125 µg/ml in these transgenic zebrafish are comparable to median pathological serum LC levels. Functional analysis links abnormal contractile function with evidence of cellular and molecular proteotoxicity in the heart, including increased cell death and autophagy. However, despite pathological and functional phenotypes analogous to human AL, the lifespan of the transgenic fish is comparable to control fish without the expressed AL-LC transgene. Nuclear labeling experiments suggest increased cardiac proliferation in the transgenic fish, which can be counteracted by treatment with a small molecule proliferation inhibitor leading to increased zebrafish mortality because of cardiac apoptosis and functional deterioration. This transgenic zebrafish model provides a platform to study underlying AL disease mechanisms in vivo further. NEW & NOTEWORTHY Heart failure is a major cause of mortality in amyloid light (AL) amyloidosis, yet it has been difficult to model in animals. We report the generation of a transgenic zebrafish model for AL amyloidosis with pathological concentration of circulating human light chain protein that results in cardiac dysfunction. The light chain toxicity triggers regeneration in the zebrafish heart resulting in functional compensation early in life, but with age develops into cardiac dysfunction.

Keywords: amyloidosis; in vivo model cardiovascular disease; proteotoxicity; transgenic zebrafish.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Amyloidosis / embryology
  • Amyloidosis / genetics
  • Amyloidosis / metabolism*
  • Amyloidosis / physiopathology
  • Animals
  • Animals, Genetically Modified
  • Apoptosis*
  • Cardiomyopathies / embryology
  • Cardiomyopathies / genetics
  • Cardiomyopathies / metabolism*
  • Cardiomyopathies / physiopathology
  • Cardiotoxicity
  • Cell Proliferation*
  • Disease Models, Animal
  • Humans
  • Immunoglobulin lambda-Chains / genetics
  • Immunoglobulin lambda-Chains / metabolism*
  • Myocardium / metabolism*
  • Myocardium / pathology
  • Regeneration*
  • Zebrafish

Substances

  • Immunoglobulin lambda-Chains