Journal of Hepatology
Volume 51, Issue 5 , Pages 909-917 , November 2009

Normoglycemia alone is insufficient to prevent long-term complications of hepatocellular adenoma in glycogen storage disease type Ib mice

  • Wai Han Yiu

      Affiliations

    • Section on Cellular Differentiation, Program on Developmental Endocrinology and Genetics, National Institute of Child Health and Human Development, Building 10, Room 9D42, 10 Center Drive, Bethesda, MD 20892-1830, USA
  • ,
  • Chi-Jiunn Pan

      Affiliations

    • Section on Cellular Differentiation, Program on Developmental Endocrinology and Genetics, National Institute of Child Health and Human Development, Building 10, Room 9D42, 10 Center Drive, Bethesda, MD 20892-1830, USA
  • ,
  • Paul A. Mead

      Affiliations

    • Section on Cellular Differentiation, Program on Developmental Endocrinology and Genetics, National Institute of Child Health and Human Development, Building 10, Room 9D42, 10 Center Drive, Bethesda, MD 20892-1830, USA
  • ,
  • Matthew F. Starost

      Affiliations

    • Division of Veterinary Resources, National Institutes of Health, Bethesda, MD 20892, USA
  • ,
  • Brian C. Mansfield

      Affiliations

    • Section on Cellular Differentiation, Program on Developmental Endocrinology and Genetics, National Institute of Child Health and Human Development, Building 10, Room 9D42, 10 Center Drive, Bethesda, MD 20892-1830, USA
  • ,
  • Janice Y. Chou

      Affiliations

    • Section on Cellular Differentiation, Program on Developmental Endocrinology and Genetics, National Institute of Child Health and Human Development, Building 10, Room 9D42, 10 Center Drive, Bethesda, MD 20892-1830, USA
    • Corresponding Author InformationCorresponding author. Tel.: +301 496 1094; fax: +301 402 6035.

Received 12 September 2008 ,Revised 26 October 2008 ,Accepted 6 November 2008.

References 

  1. Chou JY, Matern D, Mansfield BC, Chen Y-T. Type I glycogen storage diseases: disorders of the glucose-6-phosphatase complex. Curr Mol Med. 2002;2:121–143
  2. Chou JY, Mansfield BC. Glucose-6-phosphate transporter: the key to glycogen storage disease type Ib. In:  Broer S,  Wagner CA editor. Membrane transporter diseases. New York: Springer; 2003;p. 91–205
  3. Shieh J-J, Pan C-J, Mansfield BC, Chou JY. Glucose-6-phosphate hydrolase, widely expressed outside the liver, can explain age-dependent resolution of hypoglycemia in glycogen storage disease type Ia. J Biol Chem. 2003;278:47098–47103
  4. Ghosh A, Shieh J-J, Pan C-J, Chou JY. Histidine-167 is the phosphate acceptor in glucose-6-phosphatase-β forming a phosphohistidine-enzyme intermediate during catalysis. J Biol Chem. 2004;279:12479–12483
  5. Kim SY, Nguyen ATD, Gao J-L, Murphy PM, Mansfield BC, Chou JY. Bone-marrow derived cells require a functional glucose-6-phosphate transporter for normal myeloid functions. J Biol Chem. 2006;281:28794–28801
  6. Cheung YY, Kim SY, Yiu WH, Pan CJ, Jun HS, Ruef RA, et al. Impaired neutrophil activity and increased susceptibility to bacterial infection in mice lacking glucose-6-phosphatase-beta. J Clin Invest. 2007;117:784–793
  7. Kim SY, Jun HS, Mansfield BC, Chou JY. Neutrophil stress and apoptosis underlie myeloid dysfunction in glycogen storage disease type Ib. Blood. 2008;111:5704–5711
  8. Gitzelmann R, Bosshard NU. Defective neutrophil and monocyte functions in glycogen storage disease type 1b: a literature review. Eur J Pediatr. 1993;152:S33–S38
  9. Chen L-Y, Shieh J-J, Lin B, Pan C-J, Gao J-L, Murphy PM, et al. Impaired glucose homeostasis, neutrophil rafficking and function in mice lacking the glucose-6-phosphate transporter. Hum Mol Genet. 2003;12:2547–2558
  10. Greene HL, Slonim AE, O’Neill JA, Burr IM. Continuous nocturnal intragastric feeding for management of type 1 glycogen-storage disease. N Engl J Med. 1776;294:423–425
  11. Chen YT, Cornblath M, Sidbury JB. Cornstarch therapy in type I glycogen storage disease. N Engl J Med. 1984;310:171–175
  12. Schroten H, Roesler J, Breidenbach T, Wendel U, Elsner J, Schweitzer S, et al. Granulocyte and granulocyte-macrophage colony-stimulating factors for treatment of neutropenia in glycogen storage disease type Ib. J Pediatr. 1991;119:748–754
  13. Roe TF, Coates TD, Thomas DW, Miller JH, Gilsanz V. Brief report: treatment of chronic inflammatory bowel disease in glycogen storage disease type Ib with colony-stimulating factors. N Engl J Med. 1992;326:1666–1669
  14. Bianchi L. Glycogen storage disease I and hepatocellular tumours. Eur J Pediatr. 1993;52:S63–S70
  15. Labrune P, Trioche P, Duvaltier I, Chevalier P, Odievre M. Hepatocellular adenomas in glycogen storage disease type I and III: a series of 43 patients and review of the literature. J Pediatr Gastroenterol Nutr. 1997;24:276–279
  16. Lee PJ. Glycogen storage disease type I: pathophysiology of liver adenomas. Eur J Pediatr. 2002;161:S46–S49
  17. Rake JP, Visser G, Labrune P, Leonard JV, Ullrich K, Smit GP. 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. 2002;161(Suppl 1):S20–S34
  18. Pan C-J, Lin B, Chou JY. Transmembrane topology of human Glucose-6-phosphate transporter. J Biol Chem. 1999;274:13865–13869
  19. Yiu WH, Pan C-J, Allamarvdasht A, Kim SY, Chou JY. Glucose-6-phosphate transporter gene therapy corrects metabolic and myeloid abnormalities in glycogen storage disease type Ib mice. Gene Ther. 2007;14:219–226
  20. Wilson JM. Adenovirus-mediated gene transfer to liver. Adv Drug Deliv Rev. 2001;46:205–209
  21. Gao GP, Alvira MR, Wang L, Calcedo R, Johnston J, Wilson JM. Novel adeno-associated viruses from rhesus monkeys as vectors for human gene therapy. Proc Natl Acad Sci USA. 2002;99:11854–11859
  22. Thomas CE, Storm TA, Huang Z, Kay MA. Rapid uncoating of vector genomes is the key to efficient liver transduction with pseudotyped adeno-associated virus vectors. J Virol. 2004;78:3110–3122
  23. Xu L, Daly T, Gao C, Flotte TR, Song S, Byrne BJ, et al. CMV-beta-actin promoter directs higher expression from an adeno-associated viral vector in the liver than the cytomegalovirus or elongation factor 1 alpha promoter and results in therapeutic levels of human factor X in mice. Hum Gene Ther. 2001;12:563–573
  24. Grimm D, Kern A, Rittner K, Kleinschmidt JA. Novel tools for production and purification of recombinant adenoassociated virus vectors. Hum Gene Ther. 1998;10:2745–2760
  25. Hauswirth WW, Lewin AS, Zolotukhin S, Muzyczka N. Production and purification of recombinant adeno-associated virus. Methods Enzymol. 2000;316:743–761
  26. Nakai H, Yant SR, Storm TA, Fuess S, Meuse L, Kay MA. Extrachromosomal recombinant adeno-associated virus vector genomes are primarily responsible for stable liver transduction in vivo. J Virol. 2001;75:6969–6976
  27. Cunningham SC, Dane AP, Spinoulas A, Alexander IE. Gene delivery to the juvenile mouse liver using AAV2/8 vectors. Mol Ther. 2008;16:1081–1088
  28. Conlon TJ, Cossette T, Erger K, Choi YK, Clarke T, Scott-Jorgensen M, et al. Efficient hepatic delivery and expression from a recombinant adeno-associated virus 8 pseudotyped α1-antitrypsin vector. Mol Ther. 2005;12:867–875
  29. Nakai H, Fuess S, Storm TA, Muramatsu S, Nara Y, Kay M. Unrestricted hepatocyte transduction with adeno-associated virus serotype 8 vectors in mice. J Virol. 2005;79:214–224
  30. Seppen J, Bakker C, de Jong B, Kunne C, van den Oever K, Vandenberghe K, et al. Adeno-associated virus vector serotypes mediate sustained correction of bilirubin UDP glucuronosyltransferase deficiency in rats. Mol Ther. 2006;13:1085–1092
  31. Cumano A, Godin I. Ontogeny of the hematopoietic system. Annu Rev Immunol. 2007;25:745–785
  32. Iwasaki H, Akashi K. Myeloid lineage commitment from the hematopoietic stem cell. Immunity. 2007;26:726–740
  33. Maina N, Han Z, Li X, Hu Z, Zhong L, Bischof D, et al. Recombinant self-complementary adeno-associated virus serotype vector-mediated hematopoietic stem cell transduction and lineage-restricted, long-term transgene expression in a murine serial bone marrow transplantation model. Hum Gene Ther. 2008;19:376–383
  34. Marra F, Gastaldelli A, Svegliati Baroni G, Tell G, Tiribelli C. Molecular basis and mechanisms of progression of non-alcoholic steatohepatitis. Trends Mol Med. 2008;14:72–81
  35. Yamashita T, Ishibashi Y, Nagaoka I, Kasuya K, Masuda K, Warabi H, et al. Studies of glycogen-induced inflammation of mice. Dynamics of inflammatory responses and influence of antiinflammatory drugs and protease inhibitors. Inflammation. 1982;6:87–101
  36. Mulligan MS, Lentsch AB, Miyasaka M, Ward PA. Cytokine and adhesion molecule requirements for neutrophil recruitment during glycogen-induced peritonitis. Inflamm Res. 1998;47:251–255
  37. Zucman-Rossi J, Jeannot E, Nhieu JT, Scoazec JY, Guettier C, Rebouissou S, et al. Genotype-phenotype correlation in hepatocellular adenoma: new classification and relationship with HCC. Hepatology. 2006;43:515–524
  38. Bioulac-Sage P, Rebouissou S, Thomas C, Blanc JF, Saric J, Sa Cunha A, et al. Hepatocellular adenoma subtype classification using molecular markers and immunohistochemistry. Hepatology. 2007;46:740–748
  39. Poe R, Snover DC. Adenomas in glycogen storage disease type 1. Two cases with unusual histologic features. Am J Surg Pathol. 1988;12:477–483
  40. Volmar KE, Burchette JL, Creager AJ. Hepatic adenomatosis in glycogen storage disease type Ia: report of a case with unusual histology. Arch Pathol Lab Med. 2003;127:e402–e405
  41. Carter PJ, Samulski RJ. Adeno-associated viral vectors as gene delivery vehicles. Int J Mol Med. 2000;6:17–27
  42. Flotte TR. Gene therapy progress and prospects: recombinant adeno-associated virus (rAAV) vectors. Gene Ther. 2004;11:805–810
  43. Donsante A, Miller DG, Li Y, Vogler C, Brunt EM, Russell DW, et al. AAV vector integration sites in mouse hepatocellular carcinoma. Science. 2007;317:477

 The authors declare that they do not have anything to disclose regarding funding from industries or conflict of interest with respect to this manuscript. This is a NIH funded study.

PII: S0168-8278(09)00009-9

doi: 10.1016/j.jhep.2008.11.026

Journal of Hepatology
Volume 51, Issue 5 , Pages 909-917 , November 2009