Prevention of hepatocellular adenoma and correction of metabolic abnormalities in murine glycogen storage disease type Ia by gene therapy

Hepatology. 2012 Nov;56(5):1719-29. doi: 10.1002/hep.25717. Epub 2012 Aug 27.

Abstract

Glycogen storage disease type Ia (GSD-Ia), which is characterized by impaired glucose homeostasis and chronic risk of hepatocellular adenoma (HCA), is caused by deficiencies in the endoplasmic reticulum (ER)-associated glucose-6-phosphatase-α (G6Pase-α or G6PC) that hydrolyzes glucose-6-phosphate (G6P) to glucose. G6Pase-α activity depends on the G6P transporter (G6PT) that translocates G6P from the cytoplasm into the ER lumen. The functional coupling of G6Pase-α and G6PT maintains interprandial glucose homeostasis. We have shown previously that gene therapy mediated by AAV-GPE, an adeno-associated virus (AAV) vector expressing G6Pase-α directed by the human G6PC promoter/enhancer (GPE), completely normalizes hepatic G6Pase-α deficiency in GSD-Ia (G6pc(-/-) ) mice for at least 24 weeks. However, a recent study showed that within 78 weeks of gene deletion, all mice lacking G6Pase-α in the liver develop HCA. We now show that gene therapy mediated by AAV-GPE maintains efficacy for at least 70-90 weeks for mice expressing more than 3% of wild-type hepatic G6Pase-α activity. The treated mice displayed normal hepatic fat storage, had normal blood metabolite and glucose tolerance profiles, had reduced fasting blood insulin levels, maintained normoglycemia over a 24-hour fast, and had no evidence of hepatic abnormalities. After a 24-hour fast, hepatic G6PT messenger RNA levels in G6pc(-/-) mice receiving gene therapy were markedly increased. Because G6PT transport is the rate-limiting step in microsomal G6P metabolism, this may explain why the treated G6pc(-/-) mice could sustain prolonged fasts. The low fasting blood insulin levels and lack of hepatic steatosis may explain the absence of HCA.

Conclusion: These results confirm that AAV-GPE-mediated gene transfer corrects hepatic G6Pase-α deficiency in murine GSD-Ia and prevents chronic HCA formation.

Publication types

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

MeSH terms

  • Adenoma / prevention & control*
  • Animals
  • Antiporters / genetics
  • Antiporters / metabolism
  • Blood Glucose
  • Body Mass Index
  • Body Weight
  • Dependovirus / genetics
  • Disease Models, Animal
  • Female
  • Genetic Therapy* / adverse effects
  • Genetic Vectors
  • Glucose Tolerance Test
  • Glucose-6-Phosphatase / genetics*
  • Glucose-6-Phosphatase / metabolism
  • Glycogen Storage Disease Type I / enzymology*
  • Glycogen Storage Disease Type I / genetics
  • Glycogen Storage Disease Type I / therapy*
  • Homeostasis
  • Insulin / blood
  • Liver / enzymology
  • Liver / metabolism*
  • Liver / pathology
  • Liver Neoplasms / prevention & control*
  • Male
  • Mice
  • Mice, Knockout
  • Monosaccharide Transport Proteins / genetics
  • Monosaccharide Transport Proteins / metabolism
  • Promoter Regions, Genetic
  • RNA, Messenger / metabolism

Substances

  • Antiporters
  • Blood Glucose
  • Insulin
  • Monosaccharide Transport Proteins
  • RNA, Messenger
  • glucose 6-phosphate(transporter)
  • Glucose-6-Phosphatase