Oral delivery of Acid Alpha Glucosidase epitopes expressed in plant chloroplasts suppresses antibody formation in treatment of Pompe mice

Plant Biotechnol J. 2015 Oct;13(8):1023-32. doi: 10.1111/pbi.12413. Epub 2015 Jun 5.

Abstract

Deficiency of acid alpha glucosidase (GAA) causes Pompe disease in which the patients systemically accumulate lysosomal glycogen in muscles and nervous systems, often resulting in infant mortality. Although enzyme replacement therapy (ERT) is effective in treating patients with Pompe disease, formation of antibodies against rhGAA complicates treatment. In this report, we investigated induction of tolerance by oral administration of GAA expressed in chloroplasts. Because full-length GAA could not be expressed, N-terminal 410-amino acids of GAA (as determined by T-cell epitope mapping) were fused with the transmucosal carrier CTB. Tobacco transplastomic lines expressing CTB-GAA were generated through site-specific integration of transgenes into the chloroplast genome. Homoplasmic lines were confirmed by Southern blot analysis. Despite low-level expression of CTB-GAA in chloroplasts, yellow or albino phenotype of transplastomic lines was observed due to binding of GAA to a chloroplast protein that has homology to mannose-6 phosphate receptor. Oral administration of the plant-made CTB-GAA fusion protein even at 330-fold lower dose (1.5 μg) significantly suppressed immunoglobulin formation against GAA in Pompe mice injected with 500 μg rhGAA per dose, with several-fold lower titre of GAA-specific IgG1 and IgG2a. Lyophilization increased CTB-GAA concentration by 30-fold (up to 190 μg per g of freeze-dried leaf material), facilitating long-term storage at room temperature and higher dosage in future investigations. This study provides the first evidence that oral delivery of plant cells is effective in reducing antibody responses in ERT for lysosomal storage disorders facilitating further advances in clinical investigations using plant cell culture system or in vitro propagation.

Keywords: Pompe disease; bioencapsulation; enzyme replacement therapy; lysosomal storage disorder; molecular farming; oral tolerance.

Publication types

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

MeSH terms

  • Administration, Oral
  • Animals
  • Antibody Formation*
  • Chloroplasts / metabolism*
  • Cholera Toxin / metabolism
  • Disease Models, Animal
  • Enzyme Replacement Therapy
  • Epitopes / administration & dosage*
  • Epitopes / immunology
  • Gene Expression
  • Genetic Vectors / metabolism
  • Glycogen Storage Disease Type II / drug therapy*
  • Humans
  • Mice
  • Nicotiana / genetics*
  • Phenotype
  • Plants, Genetically Modified
  • Recombinant Fusion Proteins / metabolism
  • alpha-Glucosidases / administration & dosage*
  • alpha-Glucosidases / therapeutic use*

Substances

  • Epitopes
  • Recombinant Fusion Proteins
  • Cholera Toxin
  • GAA protein, human
  • alpha-Glucosidases