Skip to main content
Top
Published in: Journal of Inherited Metabolic Disease 6/2018

01-11-2018 | Glycogen Storage Disease

Long-term complications of glycogen storage disease type Ia in the canine model treated with gene replacement therapy

Authors: Elizabeth D. Brooks, Dustin J. Landau, Jeffrey I. Everitt, Talmage T. Brown, Kylie M. Grady, Lauren Waskowicz, Cameron R. Bass, John D’Angelo, Yohannes G. Asfaw, Kyha Williams, Priya S. Kishnani, Dwight D. Koeberl

Published in: Journal of Inherited Metabolic Disease | Issue 6/2018

Login to get access

Abstract

Background

Glycogen storage disease type Ia (GSD Ia) in dogs closely resembles human GSD Ia. Untreated patients with GSD Ia develop complications associated with glucose-6-phosphatase (G6Pase) deficiency. Survival of human patients on intensive nutritional management has improved; however, long-term complications persist including renal failure, nephrolithiasis, hepatocellular adenomas (HCA), and a high risk for hepatocellular carcinoma (HCC). Affected dogs fail to thrive with dietary therapy alone. Treatment with gene replacement therapy using adeno-associated viral vectors (AAV) expressing G6Pase has greatly prolonged life and prevented hypoglycemia in affected dogs. However, long-term complications have not been described to date.

Methods

Five GSD Ia-affected dogs treated with AAV-G6Pase were evaluated. Dogs were euthanized due to reaching humane endpoints related to liver and/or kidney involvement, at 4 to 8 years of life. Necropsies were performed and tissues were analyzed.

Results

Four dogs had liver tumors consistent with HCA and HCC. Three dogs developed renal failure, but all dogs exhibited progressive kidney disease histologically. Urolithiasis was detected in two dogs; uroliths were composed of calcium oxalate and calcium phosphate. One affected and one carrier dog had polycystic ovarian disease. Bone mineral density was not significantly affected.

Conclusions

Here, we show that the canine GSD Ia model demonstrates similar long-term complications as GSD Ia patients in spite of gene replacement therapy. Further development of gene therapy is needed to develop a more effective treatment to prevent long-term complications of GSD Ia.
Appendix
Available only for authorised users
Literature
go back to reference Austin SL, El-Gharbawy AH, Kasturi VG, James A, Kishnani PS (2013) Menorrhagia in patients with type I glycogen storage disease. Obstet Gynecol 122:1246–1254CrossRefPubMed Austin SL, El-Gharbawy AH, Kasturi VG, James A, Kishnani PS (2013) Menorrhagia in patients with type I glycogen storage disease. Obstet Gynecol 122:1246–1254CrossRefPubMed
go back to reference Baheti AD, Yeh MM, O'Malley R, Lalwani N (2015) Malignant transformation of hepatic adenoma in glycogen storage disease type-1a: report of an exceptional case diagnosed on surveillance imaging. J Clin Imaging Sci 5:47CrossRefPubMedPubMedCentral Baheti AD, Yeh MM, O'Malley R, Lalwani N (2015) Malignant transformation of hepatic adenoma in glycogen storage disease type-1a: report of an exceptional case diagnosed on surveillance imaging. J Clin Imaging Sci 5:47CrossRefPubMedPubMedCentral
go back to reference Bali DS, Chen YT, Austin S, Goldstein JL (1993) In: Adam MP, Ardinger HH, Pagon RA et al (eds) Glycogen storage disease type I. GeneReviews((R)), Seattle Bali DS, Chen YT, Austin S, Goldstein JL (1993) In: Adam MP, Ardinger HH, Pagon RA et al (eds) Glycogen storage disease type I. GeneReviews((R)), Seattle
go back to reference Brooks ED, Little D, Arumugam R et al (2013) Pathogenesis of growth failure and partial reversal with gene therapy in murine and canine Glycogen Storage Disease type Ia. Mol Genet Metab 109:161–170CrossRefPubMedPubMedCentral Brooks ED, Little D, Arumugam R et al (2013) Pathogenesis of growth failure and partial reversal with gene therapy in murine and canine Glycogen Storage Disease type Ia. Mol Genet Metab 109:161–170CrossRefPubMedPubMedCentral
go back to reference Calderaro J, Labrune P, Morcrette G et al (2013) Molecular characterization of hepatocellular adenomas developed in patients with glycogen storage disease type I. J Hepatol 58:350–357CrossRefPubMed Calderaro J, Labrune P, Morcrette G et al (2013) Molecular characterization of hepatocellular adenomas developed in patients with glycogen storage disease type I. J Hepatol 58:350–357CrossRefPubMed
go back to reference Carreiro G, Villela-Nogueira CA, Coelho H et al (2007) Orthotopic liver transplantation in glucose-6-phosphatase deficiency—Von Gierke disease—with multiple hepatic adenomas and concomitant focal nodular hyperplasia. J Pediatr Endocrinol Metab 20:545–549CrossRefPubMed Carreiro G, Villela-Nogueira CA, Coelho H et al (2007) Orthotopic liver transplantation in glucose-6-phosphatase deficiency—Von Gierke disease—with multiple hepatic adenomas and concomitant focal nodular hyperplasia. J Pediatr Endocrinol Metab 20:545–549CrossRefPubMed
go back to reference Chang CY, Hernandez-Prera JC, Roayaie S, Schwartz M, Thung SN (2013) Changing epidemiology of hepatocellular adenoma in the United States: review of the literature. Int J Hepatol 2013:604860 Chang CY, Hernandez-Prera JC, Roayaie S, Schwartz M, Thung SN (2013) Changing epidemiology of hepatocellular adenoma in the United States: review of the literature. Int J Hepatol 2013:604860
go back to reference Chen YT (2001) Glycogen storage diseases. In: Scriver CR, Beaudet AL, Sly WS, Valle D (eds) The metabolic and molecular bases of inherited disease. McGraw-Hill, New York, pp 1521–1551 Chen YT (2001) Glycogen storage diseases. In: Scriver CR, Beaudet AL, Sly WS, Valle D (eds) The metabolic and molecular bases of inherited disease. McGraw-Hill, New York, pp 1521–1551
go back to reference Crane B, Luo X, Demaster A et al (2012) Rescue administration of a helper-dependent adenovirus vector with long-term efficacy in dogs with glycogen storage disease type Ia. Gene Ther 19:443–452CrossRefPubMed Crane B, Luo X, Demaster A et al (2012) Rescue administration of a helper-dependent adenovirus vector with long-term efficacy in dogs with glycogen storage disease type Ia. Gene Ther 19:443–452CrossRefPubMed
go back to reference Cunningham SC, Dane AP, Spinoulas A, Logan GJ, Alexander IE (2008) Gene delivery to the juvenile mouse liver using AAV2/8 vectors. Mol Ther 16:1081–1088CrossRefPubMed Cunningham SC, Dane AP, Spinoulas A, Logan GJ, Alexander IE (2008) Gene delivery to the juvenile mouse liver using AAV2/8 vectors. Mol Ther 16:1081–1088CrossRefPubMed
go back to reference Demaster A, Luo X, Curtis S et al (2012) Long-term efficacy following readministration of an adeno-associated virus vector in dogs with glycogen storage disease type Ia. Hum Gene Ther 23:407–418CrossRefPubMed Demaster A, Luo X, Curtis S et al (2012) Long-term efficacy following readministration of an adeno-associated virus vector in dogs with glycogen storage disease type Ia. Hum Gene Ther 23:407–418CrossRefPubMed
go back to reference Derks TG, van Rijn M (2015) Lipids in hepatic glycogen storage diseases: pathophysiology, monitoring of dietary management and future directions. J Inherit Metab Dis 38:537–543CrossRefPubMedPubMedCentral Derks TG, van Rijn M (2015) Lipids in hepatic glycogen storage diseases: pathophysiology, monitoring of dietary management and future directions. J Inherit Metab Dis 38:537–543CrossRefPubMedPubMedCentral
go back to reference Di Rocco M, Calevo MG, Taro M, Melis D, Allegri AE, Parenti G (2008) Hepatocellular adenoma and metabolic balance in patients with type Ia glycogen storage disease. Mol Genet Metab 93:398–402CrossRefPubMed Di Rocco M, Calevo MG, Taro M, Melis D, Allegri AE, Parenti G (2008) Hepatocellular adenoma and metabolic balance in patients with type Ia glycogen storage disease. Mol Genet Metab 93:398–402CrossRefPubMed
go back to reference Dingemanse W, Muller-Gerbl M, Jonkers I, Sloten JV, van Bree H, Gielen I (2017) A prospective follow up of age related changes in the subchondral bone density of the talus of healthy Labrador Retrievers. BMC Vet Res 13:57CrossRefPubMedPubMedCentral Dingemanse W, Muller-Gerbl M, Jonkers I, Sloten JV, van Bree H, Gielen I (2017) A prospective follow up of age related changes in the subchondral bone density of the talus of healthy Labrador Retrievers. BMC Vet Res 13:57CrossRefPubMedPubMedCentral
go back to reference Evans HE, Miller ME (2013) Miller’s anatomy of the dog. Elsevier, St. Louis Evans HE, Miller ME (2013) Miller’s anatomy of the dog. Elsevier, St. Louis
go back to reference Fabry A, Benjamin SA, Angleton GM (1982) Nodular hyperplasia of the liver in the beagle dog. Vet Pathol 19:109–119CrossRefPubMed Fabry A, Benjamin SA, Angleton GM (1982) Nodular hyperplasia of the liver in the beagle dog. Vet Pathol 19:109–119CrossRefPubMed
go back to reference Farah BL, Landau DJ, Sinha RA et al (2016) Induction of autophagy improves hepatic lipid metabolism in glucose-6-phosphatase deficiency. J Hepatol 64:370–379CrossRefPubMed Farah BL, Landau DJ, Sinha RA et al (2016) Induction of autophagy improves hepatic lipid metabolism in glucose-6-phosphatase deficiency. J Hepatol 64:370–379CrossRefPubMed
go back to reference Franco LM, Krishnamurthy V, Bali D et al (2005) Hepatocellular carcinoma in glycogen storage disease type Ia: a case series. J Inherit Metab Dis 28:153–162CrossRefPubMed Franco LM, Krishnamurthy V, Bali D et al (2005) Hepatocellular carcinoma in glycogen storage disease type Ia: a case series. J Inherit Metab Dis 28:153–162CrossRefPubMed
go back to reference Gjorgjieva M, Raffin M, Duchampt A et al (2016) Progressive development of renal cysts in glycogen storage disease type I. Hum Mol Genet 25:3784–3797CrossRefPubMed Gjorgjieva M, Raffin M, Duchampt A et al (2016) Progressive development of renal cysts in glycogen storage disease type I. Hum Mol Genet 25:3784–3797CrossRefPubMed
go back to reference Jonges GN, Van Noorden CJ, Gossrau R (1990) Quantitative histochemical analysis of glucose-6-phosphatase activity in rat liver using an optimized cerium-diaminobenzidine method. J Histochem Cytochem 38:1413–1419CrossRefPubMed Jonges GN, Van Noorden CJ, Gossrau R (1990) Quantitative histochemical analysis of glucose-6-phosphatase activity in rat liver using an optimized cerium-diaminobenzidine method. J Histochem Cytochem 38:1413–1419CrossRefPubMed
go back to reference Kelly PM, Poon FW (2001) Hepatic tumours in glycogen storage disease type 1 (von Gierke’s disease). Clin Radiol 56:505–508CrossRefPubMed Kelly PM, Poon FW (2001) Hepatic tumours in glycogen storage disease type 1 (von Gierke’s disease). Clin Radiol 56:505–508CrossRefPubMed
go back to reference Kishnani PS, Faulkner E, VanCamp S et al (2001) Canine model and genomic structural organization of glycogen storage disease type Ia (GSD Ia). Vet Pathol 38:83–91CrossRefPubMed Kishnani PS, Faulkner E, VanCamp S et al (2001) Canine model and genomic structural organization of glycogen storage disease type Ia (GSD Ia). Vet Pathol 38:83–91CrossRefPubMed
go back to reference Kishnani PS, Chuang TP, Bali D et al (2009) Chromosomal and genetic alterations in human hepatocellular adenomas associated with type Ia glycogen storage disease. Hum Mol Genet 18:4781–4790CrossRefPubMed Kishnani PS, Chuang TP, Bali D et al (2009) Chromosomal and genetic alterations in human hepatocellular adenomas associated with type Ia glycogen storage disease. Hum Mol Genet 18:4781–4790CrossRefPubMed
go back to reference Kishnani PS, Austin SL, Abdenur JE et al (2014) Diagnosis and management of glycogen storage disease type I: a practice guideline of the American College of Medical Genetics and Genomics. Genet Med 16:e1CrossRefPubMed Kishnani PS, Austin SL, Abdenur JE et al (2014) Diagnosis and management of glycogen storage disease type I: a practice guideline of the American College of Medical Genetics and Genomics. Genet Med 16:e1CrossRefPubMed
go back to reference Koeberl DD, Sun BD, Damodaran TV et al (2006) Early, sustained efficacy of adeno-associated virus vector-mediated gene therapy in glycogen storage disease type Ia. Gene Ther 13:1281–1289CrossRefPubMed Koeberl DD, Sun BD, Damodaran TV et al (2006) Early, sustained efficacy of adeno-associated virus vector-mediated gene therapy in glycogen storage disease type Ia. Gene Ther 13:1281–1289CrossRefPubMed
go back to reference Koeberl DD, Pinto C, Sun B et al (2008) AAV vector-mediated reversal of hypoglycemia in canine and murine glycogen storage disease type Ia. Mol Ther 16:665–672CrossRefPubMed Koeberl DD, Pinto C, Sun B et al (2008) AAV vector-mediated reversal of hypoglycemia in canine and murine glycogen storage disease type Ia. Mol Ther 16:665–672CrossRefPubMed
go back to reference Koeberl DD, Kishnani PS, Bali D, Chen YT (2009) Emerging therapies for glycogen storage disease type I. Trends Endocrinol Metab 20:252–258CrossRefPubMed Koeberl DD, Kishnani PS, Bali D, Chen YT (2009) Emerging therapies for glycogen storage disease type I. Trends Endocrinol Metab 20:252–258CrossRefPubMed
go back to reference Korljan Jelaska B, Ostojic SB, Berovic N, Kokic V (2013) Continuous glucose monitoring in the treatment of obesity in patients with glycogen storage disease type Ia. Endocrinol Diabetes Metab Case Rep 2013:130056PubMedPubMedCentral Korljan Jelaska B, Ostojic SB, Berovic N, Kokic V (2013) Continuous glucose monitoring in the treatment of obesity in patients with glycogen storage disease type Ia. Endocrinol Diabetes Metab Case Rep 2013:130056PubMedPubMedCentral
go back to reference Labrune P, Trioche P, Duvaltier I, Chevalier P, Odievre M (1997) Hepatocellular adenomas in glycogen storage disease type I and III: a series of 43 patients and review of the literature. J Pediatr Gastroenterol Nutr 24:276–279CrossRefPubMed Labrune P, Trioche P, Duvaltier I, Chevalier P, Odievre M (1997) Hepatocellular adenomas in glycogen storage disease type I and III: a series of 43 patients and review of the literature. J Pediatr Gastroenterol Nutr 24:276–279CrossRefPubMed
go back to reference Landau DJ, Brooks ED, Perez-Pinera P et al (2016) In vivo zinc finger nuclease-mediated targeted integration of a glucose-6-phosphatase transgene promotes survival in mice with glycogen storage disease type IA. Mol Ther 24:697–706CrossRefPubMedPubMedCentral Landau DJ, Brooks ED, Perez-Pinera P et al (2016) In vivo zinc finger nuclease-mediated targeted integration of a glucose-6-phosphatase transgene promotes survival in mice with glycogen storage disease type IA. Mol Ther 24:697–706CrossRefPubMedPubMedCentral
go back to reference Lawrence NT, Chengsupanimit T, Brown LM, Weinstein DA (2015) High incidence of serologic markers of inflammatory bowel disease in asymptomatic patients with glycogen storage disease type Ia. JIMD Rep 24:123–128CrossRefPubMedPubMedCentral Lawrence NT, Chengsupanimit T, Brown LM, Weinstein DA (2015) High incidence of serologic markers of inflammatory bowel disease in asymptomatic patients with glycogen storage disease type Ia. JIMD Rep 24:123–128CrossRefPubMedPubMedCentral
go back to reference Lee PJ, Patel A, Hindmarsh PC, Mowat AP, Leonard JV (1995) The prevalence of polycystic ovaries in the hepatic glycogen storage diseases: its association with hyperinsulinism. Clin Endocrinol 42:601–606CrossRef Lee PJ, Patel A, Hindmarsh PC, Mowat AP, Leonard JV (1995) The prevalence of polycystic ovaries in the hepatic glycogen storage diseases: its association with hyperinsulinism. Clin Endocrinol 42:601–606CrossRef
go back to reference Lee YM, Jun HS, Pan CJ et al (2012) Prevention of hepatocellular adenoma and correction of metabolic abnormalities in murine glycogen storage disease type Ia by gene therapy. Hepatology 56:1719–1729CrossRefPubMedPubMedCentral Lee YM, Jun HS, Pan CJ et al (2012) Prevention of hepatocellular adenoma and correction of metabolic abnormalities in murine glycogen storage disease type Ia by gene therapy. Hepatology 56:1719–1729CrossRefPubMedPubMedCentral
go back to reference Lee YM, Pan CJ, Koeberl DD, Mansfield BC, Chou JY (2013) The upstream enhancer elements of the G6PC promoter are critical for optimal G6PC expression in murine glycogen storage disease type Ia. Mol Genet Metab 110:275–280CrossRefPubMedPubMedCentral Lee YM, Pan CJ, Koeberl DD, Mansfield BC, Chou JY (2013) The upstream enhancer elements of the G6PC promoter are critical for optimal G6PC expression in murine glycogen storage disease type Ia. Mol Genet Metab 110:275–280CrossRefPubMedPubMedCentral
go back to reference Lennartson G, Lundblad A, Sjoblad S, Svensson S, Ockerman PA (1976) Quantitation of a urinary tetrasaccharide by gas chromatography and mass spectrometry. Biomed Mass Spectrom 3:51–54CrossRefPubMed Lennartson G, Lundblad A, Sjoblad S, Svensson S, Ockerman PA (1976) Quantitation of a urinary tetrasaccharide by gas chromatography and mass spectrometry. Biomed Mass Spectrom 3:51–54CrossRefPubMed
go back to reference Luo X, Hall G, Li S et al (2011) Hepatorenal correction in murine glycogen storage disease type I with a double-stranded adeno-associated virus vector. Mol Ther 19:1961–1970CrossRefPubMedPubMedCentral Luo X, Hall G, Li S et al (2011) Hepatorenal correction in murine glycogen storage disease type I with a double-stranded adeno-associated virus vector. Mol Ther 19:1961–1970CrossRefPubMedPubMedCentral
go back to reference Manzia TM, Angelico R, Toti L et al (2011) Glycogen storage disease type Ia and VI associated with hepatocellular carcinoma: two case reports. Transplant Proc 43:1181–1183CrossRefPubMed Manzia TM, Angelico R, Toti L et al (2011) Glycogen storage disease type Ia and VI associated with hepatocellular carcinoma: two case reports. Transplant Proc 43:1181–1183CrossRefPubMed
go back to reference Melis D, Rossi A, Pivonello R et al (2015) Glycogen storage disease type Ia (GSDIa) but not glycogen storage disease type Ib (GSDIb) is associated to an increased risk of metabolic syndrome: possible role of microsomal glucose 6-phosphate accumulation. Orphanet J Rare Dis 10:91CrossRefPubMedPubMedCentral Melis D, Rossi A, Pivonello R et al (2015) Glycogen storage disease type Ia (GSDIa) but not glycogen storage disease type Ib (GSDIb) is associated to an increased risk of metabolic syndrome: possible role of microsomal glucose 6-phosphate accumulation. Orphanet J Rare Dis 10:91CrossRefPubMedPubMedCentral
go back to reference Minarich LA, Kirpich A, Fiske LM, Weinstein DA (2012) Bone mineral density in glycogen storage disease type Ia and Ib. Genet Med Minarich LA, Kirpich A, Fiske LM, Weinstein DA (2012) Bone mineral density in glycogen storage disease type Ia and Ib. Genet Med
go back to reference Moraru E, Cuvinciuc O, Antonesei L et al (2007) Glycogen storage disease type I—between chronic ambulatory follow-up and pediatric emergency. J Gastrointestin Liver Dis 16:47–51PubMed Moraru E, Cuvinciuc O, Antonesei L et al (2007) Glycogen storage disease type I—between chronic ambulatory follow-up and pediatric emergency. J Gastrointestin Liver Dis 16:47–51PubMed
go back to reference Mutel E, Abdul-Wahed A, Ramamonjisoa N et al (2011) Targeted deletion of liver glucose-6 phosphatase mimics glycogen storage disease type 1a including development of multiple adenomas. J Hepatol 54:529–537CrossRefPubMed Mutel E, Abdul-Wahed A, Ramamonjisoa N et al (2011) Targeted deletion of liver glucose-6 phosphatase mimics glycogen storage disease type 1a including development of multiple adenomas. J Hepatol 54:529–537CrossRefPubMed
go back to reference Nathwani AC, Tuddenham EG, Rangarajan S et al (2011) Adenovirus-associated virus vector-mediated gene transfer in hemophilia B. N Engl J Med 365:2357–2365CrossRefPubMedPubMedCentral Nathwani AC, Tuddenham EG, Rangarajan S et al (2011) Adenovirus-associated virus vector-mediated gene transfer in hemophilia B. N Engl J Med 365:2357–2365CrossRefPubMedPubMedCentral
go back to reference Oberholzer K, Sewell AC (1990) Unique oligosaccharide (apparently glucotetrasaccharide) in urine of patients with glycogen storage diseases. Clin Chem 36:1381PubMed Oberholzer K, Sewell AC (1990) Unique oligosaccharide (apparently glucotetrasaccharide) in urine of patients with glycogen storage diseases. Clin Chem 36:1381PubMed
go back to reference Okechuku GO, Shoemaker LR, Dambska M, Brown LM, Mathew J, Weinstein DA (2017) Tight metabolic control plus ACE inhibitor therapy improves GSD I nephropathy. J Inherit Metab Dis 40:703–708CrossRefPubMed Okechuku GO, Shoemaker LR, Dambska M, Brown LM, Mathew J, Weinstein DA (2017) Tight metabolic control plus ACE inhibitor therapy improves GSD I nephropathy. J Inherit Metab Dis 40:703–708CrossRefPubMed
go back to reference Patnaik AK, Hurvitz AI, Lieberman PH, Johnson GF (1981) Canine hepatocellular carcinoma. Vet Pathol 18:427–438CrossRefPubMed Patnaik AK, Hurvitz AI, Lieberman PH, Johnson GF (1981) Canine hepatocellular carcinoma. Vet Pathol 18:427–438CrossRefPubMed
go back to reference Penhoat A, Fayard L, Stefanutti A, Mithieux G, Rajas F (2014) Intestinal gluconeogenesis is crucial to maintain a physiological fasting glycemia in the absence of hepatic glucose production in mice. Metabolism 63:104–111CrossRefPubMed Penhoat A, Fayard L, Stefanutti A, Mithieux G, Rajas F (2014) Intestinal gluconeogenesis is crucial to maintain a physiological fasting glycemia in the absence of hepatic glucose production in mice. Metabolism 63:104–111CrossRefPubMed
go back to reference Rake JP, Visser G, Labrune P, Leonard JV, Ullrich K, Smit GP (2002) Glycogen storage disease type I: diagnosis, management, clinical course and outcome. Results of the European Study on Glycogen Storage Disease Type I (ESGSD I). Eur J Pediatr 161(Suppl 1):S20–S34CrossRefPubMed Rake JP, Visser G, Labrune P, Leonard JV, Ullrich K, Smit GP (2002) Glycogen storage disease type I: diagnosis, management, clinical course and outcome. Results of the European Study on Glycogen Storage Disease Type I (ESGSD I). Eur J Pediatr 161(Suppl 1):S20–S34CrossRefPubMed
go back to reference Reddy SK, Kishnani PS, Sullivan JA et al (2007) Resection of hepatocellular adenoma in patients with glycogen storage disease type Ia. J Hepatol 47:658–663CrossRefPubMed Reddy SK, Kishnani PS, Sullivan JA et al (2007) Resection of hepatocellular adenoma in patients with glycogen storage disease type Ia. J Hepatol 47:658–663CrossRefPubMed
go back to reference Sakellariou S, Al-Hussaini H, Scalori A et al (2012) Hepatocellular adenoma in glycogen storage disorder type I: a clinicopathological and molecular study. Histopathology 60:E58–E65CrossRefPubMed Sakellariou S, Al-Hussaini H, Scalori A et al (2012) Hepatocellular adenoma in glycogen storage disorder type I: a clinicopathological and molecular study. Histopathology 60:E58–E65CrossRefPubMed
go back to reference Schneider S, Breit SM, Grampp S et al (2004) Comparative assessment of bone mineral measurements obtained by use of dual-energy x-ray absorptiometry, peripheral quantitative computed tomography, and chemical-physical analyses in femurs of juvenile and adult dogs. Am J Vet Res 65:891–900CrossRefPubMed Schneider S, Breit SM, Grampp S et al (2004) Comparative assessment of bone mineral measurements obtained by use of dual-energy x-ray absorptiometry, peripheral quantitative computed tomography, and chemical-physical analyses in femurs of juvenile and adult dogs. Am J Vet Res 65:891–900CrossRefPubMed
go back to reference Sechi A, Deroma L, Lapolla A et al (2013) Fertility and pregnancy in women affected by glycogen storage disease type I, results of a multicenter Italian study. J Inherit Metab Dis 36:83–89CrossRefPubMed Sechi A, Deroma L, Lapolla A et al (2013) Fertility and pregnancy in women affected by glycogen storage disease type I, results of a multicenter Italian study. J Inherit Metab Dis 36:83–89CrossRefPubMed
go back to reference Sever S, Weinstein DA, Wolfsdorf JI, Gedik R, Schaefer EJ (2012) Glycogen storage disease type Ia: linkage of glucose, glycogen, lactic acid, triglyceride, and uric acid metabolism. J Clin Lipidol 6:596–600CrossRefPubMed Sever S, Weinstein DA, Wolfsdorf JI, Gedik R, Schaefer EJ (2012) Glycogen storage disease type Ia: linkage of glucose, glycogen, lactic acid, triglyceride, and uric acid metabolism. J Clin Lipidol 6:596–600CrossRefPubMed
go back to reference Shestopaloff YK (2014) Method for finding metabolic properties based on the general growth law. Liver examples. A general framework for biological modeling. PLoS One 9:e99836CrossRefPubMedPubMedCentral Shestopaloff YK (2014) Method for finding metabolic properties based on the general growth law. Liver examples. A general framework for biological modeling. PLoS One 9:e99836CrossRefPubMedPubMedCentral
go back to reference Sluiter W, van den Bosch JC, Goudriaan DA et al (2012) Rapid ultraperformance liquid chromatography-tandem mass spectrometry assay for a characteristic glycogen-derived tetrasaccharide in Pompe disease and other glycogen storage diseases. Clin Chem 58:1139–1147CrossRefPubMed Sluiter W, van den Bosch JC, Goudriaan DA et al (2012) Rapid ultraperformance liquid chromatography-tandem mass spectrometry assay for a characteristic glycogen-derived tetrasaccharide in Pompe disease and other glycogen storage diseases. Clin Chem 58:1139–1147CrossRefPubMed
go back to reference Sun B, Li S, Yang L et al (2009) Activation of glycolysis and apoptosis in glycogen storage disease type Ia. Mol Genet Metab 97:267–271CrossRefPubMed Sun B, Li S, Yang L et al (2009) Activation of glycolysis and apoptosis in glycogen storage disease type Ia. Mol Genet Metab 97:267–271CrossRefPubMed
go back to reference Talente GM, Coleman RA, Alter C et al (1994) Glycogen storage disease in adults. Ann Intern Med 120:218–226CrossRefPubMed Talente GM, Coleman RA, Alter C et al (1994) Glycogen storage disease in adults. Ann Intern Med 120:218–226CrossRefPubMed
go back to reference van Dijk TH, Laskewitz AJ, Grefhorst A et al (2013) A novel approach to monitor glucose metabolism using stable isotopically labelled glucose in longitudinal studies in mice. Lab Anim 47:79–88CrossRefPubMed van Dijk TH, Laskewitz AJ, Grefhorst A et al (2013) A novel approach to monitor glucose metabolism using stable isotopically labelled glucose in longitudinal studies in mice. Lab Anim 47:79–88CrossRefPubMed
go back to reference Visser G, Rake JP, Kokke FT, Nikkels PG, Sauer PJ, Smit GP (2002) Intestinal function in glycogen storage disease type I. J Inherit Metab Dis 25:261–267CrossRefPubMed Visser G, Rake JP, Kokke FT, Nikkels PG, Sauer PJ, Smit GP (2002) Intestinal function in glycogen storage disease type I. J Inherit Metab Dis 25:261–267CrossRefPubMed
go back to reference Volmar KE, Burchette JL, Creager AJ (2003) Hepatic adenomatosis in glycogen storage disease type Ia: report of a case with unusual histology. Arch Pathol Lab Med 127:e402–e405PubMed Volmar KE, Burchette JL, Creager AJ (2003) Hepatic adenomatosis in glycogen storage disease type Ia: report of a case with unusual histology. Arch Pathol Lab Med 127:e402–e405PubMed
go back to reference Wang DQ, Carreras CT, Fiske LM et al (2012) Characterization and pathogenesis of anemia in glycogen storage disease type Ia and Ib. Genet Med 14:795–799CrossRefPubMed Wang DQ, Carreras CT, Fiske LM et al (2012) Characterization and pathogenesis of anemia in glycogen storage disease type Ia and Ib. Genet Med 14:795–799CrossRefPubMed
go back to reference Weinstein DA, Correia CE, Conlon T et al (2010) Adeno-associated virus-mediated correction of a canine model of glycogen storage disease type Ia. Hum Gene Ther 21:903–910CrossRefPubMedPubMedCentral Weinstein DA, Correia CE, Conlon T et al (2010) Adeno-associated virus-mediated correction of a canine model of glycogen storage disease type Ia. Hum Gene Ther 21:903–910CrossRefPubMedPubMedCentral
go back to reference Yiu WH, Lee YM, Peng WT et al (2010) Complete normalization of hepatic G6PC deficiency in murine glycogen storage disease type Ia using gene therapy. Mol Ther 18:1076–1084CrossRefPubMedPubMedCentral Yiu WH, Lee YM, Peng WT et al (2010) Complete normalization of hepatic G6PC deficiency in murine glycogen storage disease type Ia using gene therapy. Mol Ther 18:1076–1084CrossRefPubMedPubMedCentral
Metadata
Title
Long-term complications of glycogen storage disease type Ia in the canine model treated with gene replacement therapy
Authors
Elizabeth D. Brooks
Dustin J. Landau
Jeffrey I. Everitt
Talmage T. Brown
Kylie M. Grady
Lauren Waskowicz
Cameron R. Bass
John D’Angelo
Yohannes G. Asfaw
Kyha Williams
Priya S. Kishnani
Dwight D. Koeberl
Publication date
01-11-2018
Publisher
Springer Netherlands
Published in
Journal of Inherited Metabolic Disease / Issue 6/2018
Print ISSN: 0141-8955
Electronic ISSN: 1573-2665
DOI
https://doi.org/10.1007/s10545-018-0223-y

Other articles of this Issue 6/2018

Journal of Inherited Metabolic Disease 6/2018 Go to the issue