Transduction of skeletal muscles with common reporter genes can promote muscle fiber degeneration and inflammation

PLoS One. 2012;7(12):e51627. doi: 10.1371/journal.pone.0051627. Epub 2012 Dec 12.

Abstract

Recombinant adeno-associated viral vectors (rAAV vectors) are promising tools for delivering transgenes to skeletal muscle, in order to study the mechanisms that control the muscle phenotype, and to ameliorate diseases that perturb muscle homeostasis. Many studies have employed rAAV vectors carrying reporter genes encoding for β-galactosidase (β-gal), human placental alkaline phosphatase (hPLAP), and green fluorescent protein (GFP) as experimental controls when studying the effects of manipulating other genes. However, it is not clear to what extent these reporter genes can influence signaling and gene expression signatures in skeletal muscle, which may confound the interpretation of results obtained in experimentally manipulated muscles. Herein, we report a strong pro-inflammatory effect of expressing reporter genes in skeletal muscle. Specifically, we show that the administration of rAAV6:hPLAP vectors to the hind limb muscles of mice is associated with dose- and time-dependent macrophage recruitment, and skeletal muscle damage. Dose-dependent expression of hPLAP also led to marked activity of established pro-inflammatory IL-6/Stat3, TNFα, IKKβ and JNK signaling in lysates obtained from homogenized muscles. These effects were independent of promoter type, as expression cassettes featuring hPLAP under the control of constitutive CMV and muscle-specific CK6 promoters both drove cellular responses when matched for vector dose. Importantly, the administration of rAAV6:GFP vectors did not induce muscle damage or inflammation except at the highest doses we examined, and administration of a transgene-null vector (rAAV6:MCS) did not cause damage or inflammation at any of the doses tested, demonstrating that GFP-expressing, or transgene-null vectors may be more suitable as experimental controls. The studies highlight the importance of considering the potential effects of reporter genes when designing experiments that examine gene manipulation in vivo.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alkaline Phosphatase / administration & dosage
  • Alkaline Phosphatase / genetics
  • Animals
  • Cytomegalovirus / genetics
  • Dependovirus / genetics
  • GPI-Linked Proteins / administration & dosage
  • GPI-Linked Proteins / genetics
  • Genes, Reporter / genetics*
  • Genetic Vectors / administration & dosage
  • Genetic Vectors / genetics
  • Green Fluorescent Proteins / metabolism
  • HEK293 Cells
  • Humans
  • Inflammation / pathology*
  • Injections, Intramuscular
  • Isoenzymes / administration & dosage
  • Isoenzymes / genetics
  • Macrophages / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Muscle Fibers, Skeletal / metabolism*
  • Muscle Fibers, Skeletal / pathology*
  • Organ Specificity / genetics
  • Promoter Regions, Genetic / genetics
  • Signal Transduction
  • T-Lymphocytes / metabolism
  • Time Factors
  • Transduction, Genetic*

Substances

  • GPI-Linked Proteins
  • Isoenzymes
  • Green Fluorescent Proteins
  • Alkaline Phosphatase
  • alkaline phosphatase, placental

Grants and funding

This work was supported by funding from the National Health & Medical Research Council, Australia (grants# 526648 and 586649, http://www.nhmrc.gov.au/) and from the Muscular Dystrophy Association, United States of America (grant# 69684, http://mdausa.org/) awarded to PG. PG is supported by a Senior Research Fellowship sponsored by Pfizer Australia (http://www.pfizer.com.au/sites/au/research_and_development/Pages/default.aspx). The Baker IDI Heart & Diabetes Institute is supported in part by the Operational Infrastructure Support Program of the Victorian Government. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.