#306000
GLYCOGEN STORAGE DISEASE IXa1; GSD9A1

Alternative titles; symbols
GSD IXa1
LIVER GLYCOGENOSIS, X-LINKED, TYPE I; XLG1
GLYCOGEN STORAGE DISEASE VIII, FORMERLY
GSD VIII, FORMERLY; GSD8, FORMERLY

Other entities represented in this entry:
GLYCOGEN STORAGE DISEASE IXa2, INCLUDED
GSD IXa2, INCLUDED; GSD9A2, INCLUDED
LIVER GLYCOGENOSIS, X-LINKED, TYPE II, INCLUDED; XLG2, INCLUDED

Phenotype Gene Relationships
Location Phenotype Phenotype
MIM number
Gene/Locus Gene/Locus
MIM number
Xp22.13 Glycogen storage disease, type IXa1 306000 PHKA2 300798
Xp22.13 Glycogen storage disease, type IXa2 306000 PHKA2 300798


TEXT
A number sign (#) is used with this entry because glycogen storage disease type IXa (GSD9a) is caused by mutation in the gene encoding the alpha-2 subunit of hepatic phosphorylase kinase (PHKA2; 300798).

Description
Glycogen storage disease type IX is a metabolic disorder resulting from a deficiency of hepatic phosphorylase kinase, a hexadecameric enzyme comprising 4 copies each of 4 unique subunits encoded by 4 different genes: alpha (PHKA2), beta (PHKB; 172490), gamma (PHKG2; 172471), and delta (CALM1; 114180). Mutations within the PHKA2, PHKB, and PHKG2 genes result in GSD9a, GSD9b (261750), and GSD9c (613027), respectively. GSD9a is an X-linked recessive disorder, whereas the others are autosomal recessive.

See also X-linked muscle PHK deficiency (GSD9D; 300559), caused by mutation in the gene encoding the muscle-specific alpha PHK subunit (PHKA1; 311870).

GSD IXa has been further divided into types IXa1 (GSD9A1), with no PHK activity in liver or erythrocytes, and IXa2 (GSD9A2), with no PHK in liver, but normal activity in erythrocytes. The clinical presentation of both subtypes is the same, and both are caused by mutations in the PHKA2 gene. However, mutations that result in IXa2 are either missense or small in-frame deletions or insertions enabling residual enzyme expression in erythrocytes (Keating et al., 1985; Hendrickx et al., 1994; Beauchamp et al., 2007).

Clinical Features
Glycogen storage disease IXa is one of the mildest of the glycogenoses of man. Clinical symptoms include hepatomegaly, growth retardation, elevation of glutamate-pyruvate transaminase and glutamate-oxaloacetate transaminase, hypercholesterolemia, hypertriglyceridemia, and fasting hyperketosis These clinical and biochemical abnormalities gradually disappear with age, and most adult patients are asymptomatic (Schimke et al., 1973; Willems et al., 1990).

Hendrickx et al. (1998) presented clinical, biochemical, and molecular findings in a patient with GSD IXa2 who had been followed for 40 years. Although growth was retarded early in life, he achieved a height of 182 cm at the age of 33 years. Thyroid therapy appeared to be helpful in this patient. Five male relatives also had liver glycogenosis. Genetic analysis identified a mutation in the PHKA2 gene (R186H; 300798.0008)

Beauchamp et al. (2007) reported 10 patients from 8 families with GSD IXa confirmed by genetic analysis. Age at diagnosis ranged from 12 months to 7 years. Clinical features were variable, and included hepatomegaly, short stature, liver dysfunction, hypoglycemia, hyperuricemia, hyperlipidemia, fasting ketosis, and mild motor delay. Five of the 8 probands had a demonstrable reduction of PHK activity in erythrocytes, consistent with GSD IXa1. The majority of patients had private mutations. The authors emphasized that molecular analysis results in accurate diagnosis for GSD IX when enzymology is uninformative, and thus allows for proper genetic counseling.

Clinical Management
In 4 boys with X-linked PHK-deficient glycogenosis, aged 29 months to 43 months, Garibaldi et al. (1978) found that dextrothyroxine (D-T4) had dramatic effects: the liver, previously greatly enlarged, returned to normal size; serum GOT, GPT, and triglycerides fell to normal; and hypoglycemia was corrected.

Inheritance
Williams and Field (1961) found low leukocyte phosphorylase activity in 2 affected brothers, and normal activity in an unaffected brother and in the father. An intermediately low level in the mother, together with affected males, suggested X-linked inheritance. Wallis et al. (1966) restudied the family and with new methods found support for X-linkage.

Huijing and Fernandez (1969) studied 2 kindreds, one of which had 6 affected males and 2 possibly affected males. The other had 20 affected males, 2 affected females, and 7 probably affected males. X-linked inheritance was suggested. Huijing and Fernandez (1970) suggested that affected females studied by Hug et al. (1969) were heterozygotes.

By cloning cells of an obligate heterozygous female with GSD due to phosphorylase kinase deficiency, Migeon and Huijing (1974) demonstrated that some fibroblasts had enzymatic levels similar to those of affected hemizygotes. This was presented as proof of X-linkage and X-inactivation of the phosphorylase kinase locus.

Mapping
Willems et al. (1991) performed linkage analysis with X-chromosomal polymorphic DNA markers in 2 families with X-linked liver glycogenosis. Multipoint linkage analysis indicated that the mutation responsible for X-linked liver glycogenosis was located on Xp22 between DXS143 and DXS41. Linkage to the muscle PHKA1 region on Xq12-q13 was excluded.

Hendrickx et al. (1992, 1993) found a combined multipoint lod score of 16.79 for linkage of X-linked liver glycogenosis to chromosome Xp22.

Hendrickx et al. (1994) performed linkage analysis in 4 families with GSD IXa2, who had residual PHK activity in erythrocytes, and showed that this form was also linked to Xp22. The authors concluded that this biochemical variant type was allelic to GSD IXa1, and that both diseases are likely caused by mutations in PHKA2. Hendrickx et al. (1994) proposed the classification of XLG into types I and II.

Molecular Genetics
In affected members of 4 unrelated families with GSD IXa1, Hendrickx et al. (1995) identified 4 different mutations in the PHKA2 gene (300798.0001-300798.0004). Clinical features were somewhat variable, but included growth retardation, hepatomegaly, elevated liver enzymes, and normalization of symptoms with age. PHK activity was decreased to less than 20% of control values in erythrocytes and in liver, when measured.

Van den Berg et al. (1995) identified mutations in the PHKA2 gene (300798.0005 and 300798.0006) in affected members of 2 Dutch families with GSD IXa1. One of the families had been reported by Huijing and Fernandez (1969).

Burwinkel et al. (1996) identified mutations in the PHKA2 gene in patients with GSD IXa2 (see 306000.0008-306000.0010). The mutations appeared to cluster in limited sequence regions. Burwinkel et al. (1996) stressed that the clustering of type II mutations would further facilitate analysis by RT-PCR of blood cell mRNA and thus help avoid liver biopsy in the diagnosis.

Genotype/Phenotype Correlations
In 4 unrelated patients with GSD IXa2, Hendrickx et al. (1996) identified 4 different mutations in the PHKA2 gene (306000.0011-306000.0014). The mutations resulted in minor abnormalities in the primary structure of the protein. These mutations are found in a conserved RXX(X)T motif, resembling known phosphorylation sites that may be involved in the regulation of PHK. Hendrickx et al. (1996) postulated that PHK activity may be regulated by phosphorylation of these sites and that type II GSD9a may be due to impaired activation of PHK activity. The findings may explain why the in vitro PHK enzymatic activity is not deficient in type II, whereas it is in type I.

Burwinkel et al. (1998) described 8 new mutations and phenotypic consequences in patients with X-linked liver glycogenosis. One of the patients reported by Burwinkel et al. (1998) had low PHK activity in the liver but elevated levels in erythrocytes, typical of XLG type II. This patient had a lys189-to-glu missense mutation (K189E; 306000.0015). The authors noted that this observation adds to the growing body of evidence that the XLG phenotype is associated with missense mutations clustering at a few sites in the PHKA2 gene.

Hendrickx et al. (1999) identified PHKA2 mutations in 10 patients with XLG types I and II. They proposed that mutations in XLG type I, in which PHK activity is decreased in both liver and erythrocytes, results from truncation or disruption of the PHKA2 protein. In contrast, all type II mutations, which result in residual activity in erythrocytes, were missense mutations or small in-frame deletions and insertions. These results suggested that the biochemical differences between the 2 types of XLG are due to the different nature of the disease-causing mutations in PHKA2. Type I mutations may lead to absence of the alpha subunit, which causes an unstable PHK holoenzyme and deficient enzyme activity, whereas type II mutations may lead to in vivo deregulation of PHK, which might be difficult to demonstrate in vitro.

Nomenclature
The classification, particularly the numbering, of the glycogenoses has long been a matter of dispute. For example, Huijing (1970) referred to this disorder as glycogen storage disease type VIA; Hug (1974) assigned number VIII to a presumedly recessive form of phosphorylase deficiency with brain involvement and number IX to phosphorylase kinase deficiency (see Schimke et al., 1973). McAdams et al. (1974) presented information on classification and morphology of the glycogenoses.

Animal Model
Schneider et al. (1993) reviewed the animal mutants that result in PHK-linked glycogenoses. Two different X-linked disorders are known, as well as an autosomal recessive PHK deficiency affecting the liver and most other tissues but not muscle, in the rat.

See Also:
Goji et al. (1985); Hers (1959); Huijing (1967); Huijing (1970); Varsanyi et al. (1980)

REFERENCES
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2. Burwinkel, B., Amat, L., Gray, R. G. F., Matsuo, N., Muroya, K., Narisawa, K., Sokol, R. J., Vilaseca, M. A., Kilimann, M. W. Variability of biochemical and clinical phenotype in X-linked liver glycogenosis with mutations in the phosphorylase kinase PHKA2 gene. Hum. Genet. 102: 423-429, 1998. [PubMed: 9600238, related citations] [Full Text: Springer, Pubget]

3. Burwinkel, B., Shin, Y. S., Bakker, H. D., Deutsch, J., Lozano, M. J., Maire, I., Kilimann, M. W. Mutation hotspots in the PHKA2 gene in X-linked liver glycogenosis due to phosphorylase kinase deficiency with atypical activity in blood cells (XLG2). Hum. Molec. Genet. 5: 653-658, 1996. [PubMed: 8733134, related citations] [Full Text: HighWire Press, Pubget]

4. Garibaldi, L. R., Borrone, C., De Martini, I., Battistini, E. Dextrothyroxine treatment of phosphorylase-kinase deficiency glycogenosis in four boys. Helv. Paediat. Acta 33: 435-444, 1978. [PubMed: 280544, related citations] [Full Text: Pubget]

5. Goji, K., Morishita, Y., Kodama, S., Takahashi, T., Matsuo, T. Lymphocyte phosphorylase kinase activities in the sex-linked form of liver phosphorylase kinase deficiency. Europ. J. Pediat. 143: 179-182, 1985. [PubMed: 3987709, related citations] [Full Text: Pubget]

6. Hendrickx, J., Bosshard, N. U., Willems, P., Gitzelmann, R. Clinical, biochemical and molecular findings in a patient with X-linked liver glycogenosis followed for 40 years. Europ. J. Pediat. 157: 919-923, 1998. [PubMed: 9835437, related citations] [Full Text: Springer, Pubget]

7. Hendrickx, J., Coucke, P., Bossuyt, P., Wauters, J., Raeymaekers, P., Marchau, F., Smit, G. P. A., Stolte, I., Sardharwalla, I. B., Berthelot, J., Van den Bergh, I., Berger, R., Van Broeckhoven, C., Baussan, C., Wapenaar, M., Fernandes, J., Willems, P. J. X-linked liver glycogenosis: localization and isolation of a candidate gene. Hum. Molec. Genet. 2: 583-589, 1993. [PubMed: 8518797, related citations] [Full Text: HighWire Press, Pubget]

8. Hendrickx, J., Coucke, P., Dams, E., Lee, P., Odievre, M., Corbeel, L., Fernandes, J. F., Willems, P. J. Mutations in the phosphorylase kinase gene PHKA2 are responsible for X-linked liver glycogen storage disease. Hum. Molec. Genet. 4: 77-83, 1995. [PubMed: 7711737, related citations] [Full Text: Pubget]

9. Hendrickx, J., Coucke, P., Hors-Cayla, M.-C., Smit, G. P. A., Shin, Y. S., Deutsch, J., Smeitink, J., Berger, R., Lee, P., Fernandes, J., Willems, P. J. Localization of a new type of X-linked liver glycogenosis to the chromosomal region Xp22 containing the liver alpha-subunit of phosphorylase kinase (PHKA2). Genomics 21: 620-625, 1994. [PubMed: 7959740, related citations] [Full Text: Elsevier Science, Pubget]

10. Hendrickx, J., Coucke, P., Raeymaekers, P., Willems, P. J. X-linked liver glycogenosis: localization and isolation of a strong candidate gene. (Abstract) Am. J. Hum. Genet. 51 (suppl.): A190 only, 1992.

11. Hendrickx, J., Dams, E., Coucke, P., Lee, P., Fernandes, J., Willems, P. J. X-linked liver glycogenosis type II (XLG II) is caused by mutations in PHKA2, the gene encoding the liver alpha subunit of phosphorylase kinase. Hum. Molec. Genet. 5: 649-652, 1996. [PubMed: 8733133, related citations] [Full Text: HighWire Press, Pubget]

12. Hendrickx, J., Lee, P., Keating, J. P., Carton, D., Sardharwalla, I. B., Tuchman, M., Baussan, C., Willems, P. J. Complete genomic structure and mutational spectrum of PHKA2 in patients with X-linked liver glycogenosis type I and II. Am. J. Hum. Genet. 64: 1541-1549, 1999. [PubMed: 10330341, related citations] [Full Text: Elsevier Science, Pubget]

13. Hers, H. G. Etudes enzymatiques sur fragments hepatiques: application a la classification des glycogenoses. Rev. Int. Hepat. 9: 35-55, 1959. [PubMed: 13646331, related citations] [Full Text: Pubget]

14. Hug, G. Personal Communication. Cincinnati, Ohio 1974.

15. Hug, G., Schubert, W. K., Chuck, G. Deficient activity of dephosphophosphorylase kinase and accumulation of glycogen in the liver. J. Clin. Invest. 48: 704-715, 1969. [PubMed: 5774108, related citations] [Full Text: Journal of Clinical Investigation, Pubget]

16. Huijing, F. Glycogen-storage disease type VIa: low phosphorylase kinase activity caused by a low enzyme-substrate affinity. Biochim. Biophys. Acta 206: 199-201, 1970. [PubMed: 5266383, related citations] [Full Text: Pubget]

17. Huijing, F. Phosphorylase kinase in leucocytes of normal subjects and of patients with glycogen-storage disease. Biochim. Biophys. Acta 148: 601-603, 1967.

18. Huijing, F. Phosphorylase kinase deficiency. Biochem. Genet. 4: 187-194, 1970. [PubMed: 5444101, related citations] [Full Text: Pubget]

19. Huijing, F., Fernandez, J. X-chromosomal inheritance of liver glycogenosis with phosphorylase kinase deficiency. Am. J. Hum. Genet. 21: 275-284, 1969. [PubMed: 5306139, related citations] [Full Text: Pubget]

20. Huijing, F., Fernandez, J. Liver glycogenosis and phosphorylase kinase deficiency. (Letter) Am. J. Hum. Genet. 22: 484-485, 1970. [PubMed: 5270453, related citations] [Full Text: Pubget]

21. Keating, J. P., Brown, B. I., White, N. H., DiMauro, S. X-linked glycogen storage disease: a cause of hypotonia, hyperuricemia, and growth retardation. Am. J. Dis. Child. 139: 609-613, 1985. [PubMed: 3859203, related citations] [Full Text: HighWire Press, Pubget]

22. McAdams, A. J., Hug, G., Bove, K. E. Glycogen storage disease, type I to X: criteria for morphologic diagnosis. Hum. Path. 5: 463-487, 1974. [PubMed: 4525190, related citations] [Full Text: Pubget]

23. Migeon, B. R., Huijing, F. Glycogen-storage disease associated with phosphorylase kinase deficiency: evidence for X inactivation. Am. J. Hum. Genet. 26: 360-368, 1974. [PubMed: 4524311, related citations] [Full Text: Pubget]

24. Schimke, R. N., Zakheim, R. M., Corder, R. C., Hug, G. Glycogen storage disease type IX: benign glycogenosis of liver and hepatic phosphorylase kinase deficiency. J. Pediat. 83: 1031-1034, 1973. [PubMed: 4518931, related citations] [Full Text: Pubget]

25. Schneider, A., Davidson, J. J., Wullrich, A., Kilimann, M. W. Phosphorylase kinase deficiency in I-strain mice is associated with a frameshift mutation in the alpha-subunit muscle isoform. Nature Genet. 5: 381-385, 1993. [PubMed: 8298647, related citations] [Full Text: Nature Publishing Group, Pubget]

26. van den Berg, I. E. T., van Beurden, E. A. C. M., Malingre, H. E. M., Ploos van Amstel, H. K., Poll-The, B. T., Smeitink, J. A. M., Lamers, W. H., Berger, R. X-linked liver phosphorylase kinase deficiency is associated with mutations in the human liver phosphorylase kinase alpha subunit. Am. J. Hum. Genet. 56: 381-387, 1995. [PubMed: 7847371, related citations] [Full Text: Pubget]

27. Varsanyi, M., Vrbica, A., Heilmeyer, L. M. G., Jr. X-linked dominant inheritance of partial phosphorylase kinase deficiency in mice. Biochem. Genet. 18: 247-261, 1980. [PubMed: 7447922, related citations] [Full Text: Pubget]

28. Wallis, P. G., Sidbury, J. B., Jr., Harris, R. C. Hepatic phosphorylase defect. Studies on peripheral blood. Am. J. Dis. Child. 111: 278-282, 1966. [PubMed: 5904467, related citations] [Full Text: HighWire Press, Pubget]

29. Willems, P. J., Gerver, W. J. M., Berger, R., Fernandes, J. The natural history of liver glycogenosis due to phosphorylase kinase deficiency: a longitudinal study of 41 patients. Europ. J. Pediat. 149: 268-271, 1990. [PubMed: 2303074, related citations] [Full Text: Pubget]

30. Willems, P. J., Hendrickx, J., Van der Auwera, B. J., Vits, L., Raeymaekers, P., Coucke, P. J., Van den Bergh, I., Berger, R., Smit, G. P. A., Van Broeckhoven, C., Kilimann, M. W., Van Elsen, A. F., Fernandes, J. F. Mapping of the gene for X-linked liver glycogenosis due to phosphorylase kinase deficiency to human chromosome region Xp22. Genomics 9: 565-569, 1991. [PubMed: 1674721, related citations] [Full Text: Pubget]

31. Williams, H. E., Field, J. B. Low leukocyte phosphorylase in hepatic phosphorylase deficient glycogen storage disease. J. Clin. Invest. 40: 1841-1845, 1961. [PubMed: 14007166, related citations] [Full Text: Journal of Clinical Investigation, Pubget]

Contributors: Cassandra L. Kniffin - reorganized : 10/1/2009
Cassandra L. Kniffin - updated : 9/24/2009
Victor A. McKusick - updated : 5/28/1999
Victor A. McKusick - updated : 2/3/1999
Victor A. McKusick - updated : 1/25/1999
Clair A. Francomano - updated : 5/27/1998
Victor A. McKusick - updated : 11/17/1997
Moyra Smith - updated : 6/12/1996
Creation Date: Victor A. McKusick : 6/4/1986
Edit History: carol : 12/01/2010
carol : 10/1/2009
ckniffin : 9/24/2009
carol : 1/6/2009
carol : 4/17/2007
carol : 4/17/2007
carol : 4/17/2007
alopez : 2/3/2006
terry : 4/6/2005
carol : 3/17/2004
mgross : 6/14/1999
mgross : 6/3/1999
terry : 5/28/1999
carol : 2/12/1999
terry : 2/3/1999
carol : 2/1/1999
terry : 1/25/1999
carol : 6/19/1998
terry : 6/16/1998
terry : 6/16/1998
dholmes : 5/28/1998
dholmes : 5/27/1998
dholmes : 5/21/1998
alopez : 5/8/1998
jenny : 11/20/1997
jenny : 11/19/1997
terry : 11/17/1997
alopez : 7/8/1997
mark : 3/27/1997
terry : 10/31/1996
carol : 6/12/1996
carol : 2/27/1995
davew : 8/22/1994
jason : 7/13/1994
warfield : 4/20/1994
mimadm : 4/13/1994
carol : 12/17/1993