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Human Molecular Genetics Advance Access published online on March 19, 2009

Human Molecular Genetics, doi:10.1093/hmg/ddp128
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© The Author 2009. Published by Oxford University Press. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org

Distinct mutations in the glycogen debranching enzyme found in Glycogen Storage Disease Type III lead to impairment in diverse cellular functions

Alan Cheng1, Mei Zhang1,4, Minoru Okubo2, Kaoru Omichi3 and Alan R. Saltiel1,*

1 Departments of Internal Medicine and Physiology, Life Sciences Institute, University of Michigan Medical Center, Ann Arbor, Michigan 48109, USA 2 Okinaka Memorial Institute for Medical Research and Toranomon Hospital, 2-2-2 Toranomon, Minato-ku, Tokyo 105-8470, Japan 3 Department of Chemistry, Graduate School of Science, Osaka Prefecture University, 1-1 Gakuen-cho, Sakai, Osaka, Japan

* Address correspondence and reprint requests to: Alan R. Saltiel, Life Sciences Institute, University of Michigan, Ann Arbor, Michigan 48109, USA; (Tel) 734-615-9787; (Fax) 734-763-6492; email: saltiel{at}lsi.umich.edu

Received February 23, 2009; Revised March 13, 2009; Accepted March 13, 2009

Glycogen Storage Disease Type III (GSDIII) is a metabolic disorder characterized by a deficiency in the glycogen debranching enzyme, amylo-1,6-glucosidase,4-{alpha}-glucanotransferase (AGL). Patients with GSDIII commonly exhibit hypoglycemia, along with variable organ dysfunction of the liver, muscle or heart tissues. The AGL protein binds to glycogen through its C-terminal region, and possesses two separate domains for the transferase and glucosidase activities. Most causative mutations are nonsense, and how they affect the enzyme is not well understood. Here we investigated four rare missense mutations to determine the molecular basis of how they affect AGL function leading to GSDIII. The L620P mutant primarily abolishes transferase activity while the R1147G variant impairs glucosidase function. Interestingly, mutations in the carbohydrate binding domain (G1448R and Y1445ins) are more severe in nature, leading to significant loss of all enzymatic activities and carbohydrate binding ability, as well as enhancing targeting for proteasomal degradation. This region (Y1445-G1448R) displays virtual identity across human and bacterial species, suggesting an important role that has been conserved throughout evolution. Our results clearly indicate that inactivation of either enzymatic activity is sufficient to cause GSDIII disease and suggest that the carbohydrate binding domain of AGL plays a major role to coordinate its functions and regulation by the ubiquitin-proteasome system.


4 Present address: Wyeth Research, Cambridge, Massachusetts 02140, USA


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