Inborn errors of metabolism: The flux from Mendelian to complex diseases

Nature Reviews Genetics

Volumn 7, Issue 6, 2006, Pages 449-460

  Lanpher, Brendan ^a   Brunetti Pierri, Nicola ^a   Lee, Brendan ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; ARYLBUTYRIC ACID DERIVATIVE; BENZOIC ACID; BIOTIN; CARNITINE; CHOLESTEROL; COPPER; GALACTOSE; GLUCOSE; HEMIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; LACTOSE; MIGLUSTAT; NITROGEN; PENICILLAMINE; PHENYLACETATE SODIUM; PHENYLACETIC ACID DERIVATIVE; PHENYLALANINE; SODIUM PHENYLBUTYRATE; UNCLASSIFIED DRUG;

BONE MARROW TRANSPLANTATION; CLINICAL FEATURE; CLINICAL TRIAL; DIAGNOSTIC PROCEDURE; DIET THERAPY; DISEASE CLASSIFICATION; ENZYME REPLACEMENT; GAUCHER DISEASE; GENETIC DISORDER; GENOTYPE; GENOTYPE PHENOTYPE CORRELATION; HOMEOSTASIS; HUMAN; INBORN ERROR OF METABOLISM; METABOLIC DISORDER; METABOLITE; METABOLOMICS; MOLECULAR GENETICS; PATHOPHYSIOLOGY; PHENOTYPE; PRIORITY JOURNAL; REVIEW; UREA CYCLE DISORDER;

FORECASTING; GENETIC PREDISPOSITION TO DISEASE; HUMANS; METABOLISM, INBORN ERRORS; MUTATION; PHENOTYPE; SIGNAL TRANSDUCTION;

EID: 33646893457     PISSN: 14710056     EISSN: 14710064     Source Type: Journal    
DOI: 10.1038/nrg1880     Document Type: Review

References (101)

1. Chou, J. Y., Matern, D., Mansfield, B. C. & Chen, Y. T. Type I glycogen storage diseases: disorders of the glucose-6-phosphatase complex. Curr. Mol. Med. 2, 121-143 (2002).
2. Garrod, A. The Croonian lectures on inborn errors of metabolism, lecture II: alkaptonuria. Lancet 2, 73-79 (1908).
3. Wilcken, B., Wiley, V., Hammond, J. & Carpenter, K. Screening newborns for inborn errors of metabolism by tandem mass spectrometry. N. Engl. J. Med. 348, 2304-2312 (2003).
4. Roe, C. R., Ding, J. in The Molecular and Metabolic Basis of Inherited Disease (eds Scriver, C. R., Beaudet, A. L., Sly, W. S. & Valle, D.) 2297-2326 (McGraw-Hill, New York, 1995).
5. Dipple, K. M. & McCabe, E. R. Modifier genes convert 'simple' Mendelian disorders to complex traits. Mol. Genet. Metab. 71, 43-50 (2000).
6. Dipple, K. M. & McCabe, E. R. Phenotypes of patients with 'simple' Mendelian disorders are complex traits: thresholds, modifiers, and systems dynamics. Am. J. Hum. Genet. 66, 1729-1735 (2000). Provides an excellent overview of the true complexity of classical Mendelian IEM.
7. Applegarth, D. A., Dimmick, J. E. & Toone, J. R. Laboratory detection of metabolic disease. Pediatr. Clin. North Am. 36, 49-65 (1989).
8. Dunn, W. B., Bailey, N. J. & Johnson, H. E. Measuring the metabolome: current analytical technologies. Analyst 130, 606-625 (2005). Provides an overview of the available techniques for analysing multiple metabolites.
9. Pandor, A., Eastham, J., Beverley, C., Chilcott, J. & Paisley, S. Clinical effectiveness and cost-effectiveness of neonatal screening for inborn errors of metabolism using tandem mass spectrometry: a systematic review. Health Technol. Assess. 8, 1-121 (2004).
10. Millington, D. S., Kodo N., Norwood, D. L., Roe, C. R. Tandem mass spectrometry: a new method for acylcarnitine profiling with potential for neonatal screening for inborn errors of metabolism. J. Inherit. Metab. Dis. 13, 321-324 (1990).
11. Poustie, V. J. & Rutherford, P. Dietary interventions for phenylketonuria. Cochrane Database Syst. Rev., CD001304 (1999).
12. Guthrie, R. & Susi, A. A simple phenylalanine method for detecting phenylketonuria in large populations of newborn infants. Pediatrics 32, 338-343 (1963).
13. Bodamer, O. A. et al. Utilization of cornstarch in glycogen storage disease type Ia. Eur. J. Gastroenterol. Hepatol. 14, 1251-1256 (2002).
14. Solis, J. O. & Singh, R. H. Management of fatty acid oxidation disorders: a survey of current treatment strategies. J. Am. Diet. Assoc. 102, 1800-1803 (2002).
15. Pastores, G. M. & Barnett, N. L. Current and emerging therapies for the lysosomal storage disorders. Expert Opin. Emerg. Drugs 10, 891-902 (2005). An overview of the therapeutic agents that are available for storage diseases. Includes a discussion of bone-marrow transplant, enzyme replacement and substrate reduction.
16. Klinge, L., Straub, V., Neudorf, U. & Voit, T. Enzyme replacement therapy in classical infantile Pompe disease: results of a ten-month follow-up study. Neuropediatrics 36, 6-11 (2005).
17. Pastores, G. M., Barnett, N. L. & Kolodny, E. H. An open-label, noncomparative study of miglustat in type I Gaucher disease: efficacy and tolerability over 24 months of treatment. Clin. Ther. 27, 1215-1227 (2005).
18. Mian, A. & Lee, B. Urea-cycle disorders as a paradigm for inborn errors of hepatocyte metabolism. Trends Mol. Med. 8, 583-589 (2002).
19. Saudubray, J. M. et al. Liver transplantation in urea cycle disorders. Eur. J. Pediatr. 158, S55-S59 (1999).
20. Brunetti-Pierri, N. & Lee, B. Gene therapy for inborn errors of liver metabolism. Mol. Genet. Metab. 86, 13-24 (2005).
21. Birkemeyer, C., Luedemann, A., Wagner, C., Erban, A. & Kopka, J. Metabolome analysis: the potential of in vivo labeling with stable isotopes for metabolite profiling. Trends Biotechnol. 23, 28-33 (2005). An excellent review of the use of stable isotope tracers for the in vivo assays of metabolite fluxes.
22. Wiechert, W. 13C metabolic flux analysis. Metab. Eng. 3, 195-206 (2001).
23. Wittmann, C. Metabolic flux analysis using mass spectrometry. Adv. Biochem. Eng. Biotechnol. 74, 39-64 (2002).
24. Leonard, J. V. & Heales, S. J. The investigation of inborn errors in vivo using stable isotopes. Eur. J. Pediatr. 153, S81-S83 (1994).
25. Dufner, D. & Previs, S. F. Measuring in vivo metabolism using heavy water. Curr. Opin. Clin. Nutr. Metab. Care 6, 511-517 (2003).
26. Kelleher, J. K. Flux estimation using isotopic tracers: common ground for metabolic physiology and metabolic engineering. Metab. Eng. 3, 100-110 (2001).
27. Lee, B. et al. In vivo urea cycle flux distinguishes and correlates with phenotypic severity in disorders of the urea cycle. Proc. Natl Acad. Sci. USA 97, 8021-8026 (2000).
28. Scaglia, F. et al. Differential utilization of systemic and enterai ammonia for urea synthesis in control subjects and ornithine transcarbamylase deficiency carriers. Am. J. Clin. Nutr. 78, 749-755 (2003).
29. Brady, R. O., Kanfer, J. N., Bradley, R. M. & Shapiro, D. Demonstration of a deficiency of glucocerebroside-cleaving enzyme in Gaucher's disease. J. Clin. Invest. 45, 1112-1115 (1966).
30. Charrow, J. et al. The Gaucher registry: demographics and disease characteristics of 1698 patients with Gaucher disease. Arch. Intern. Med. 160, 2835-2843 (2000).
31. Theophilus, B., Latham, T., Grabowski, G. A. & Smith, F. I. Gaucher disease: molecular heterogeneity and phenotype-genotype correlations. Am. J. Hum. Genet. 45, 212-225 (1989).
32. Koprivica, V. et al. Analysis and classification of 304 mutant alleles in patients with type 1 and type 3 Gaucher disease. Am. J. Hum. Genet. 66, 1777-1786 (2000).
33. Bonifacino, J. S. & Weissman, A. M. Ubiquitin and the control of protein fate in the secretory and endocytic pathways. Annu. Rev. Cell Dev. Biol. 14, 19-57 (1998).
34. Brodsky, J. L. & McCracken, A. A. ER protein quality control and proteasome-mediated protein degradation. Semin. Cell Dev. Biol. 10, 507-513 (1999).
35. Hammond, C. & Helenius, A. Quality control in the secretory pathway. Curr. Opin. Cell. Biol. 7, 523-529 (1995).
36. Kopito, R. R. ER quality control: the cytoplasmic connection. Cell 88, 427-430 (1997).
37. Ron, I. & Horowitz, M. ER retention and degradation as the molecular basis underlying Gaucher disease heterogeneity. Hum. Mol. Genet. 14, 2387-2398 (2005).
38. Sitia, R. & Braakman, I. Quality control in the endoplasmic reticulum protein factory. Nature 426, 891-894 (2003).
39. Berrebi, A., Wishnitzer, R. & Von-der-Walde, U. Gaucher's disease: unexpected diagnosis in three patients over seventy years old. Nouv. Rev. Fr. Hematol. 26, 201-203 (1984).
40. Bodennec, J., Pelled, D., Riebeling, C., Trajkovic, S. & Futerman, A. H. Phosphatidylcholine synthesis is elevated in neuronal models of Gaucher disease due to direct activation of CTP:phosphocholine cytidylyltransferase by glucosylceramide. FASEB J. 16, 1814-1816 (2002).
41. Weinhold, P. A. & Feldman, D. A. Choline-phosphate cytidylyltransferase. Methods Enzymol. 209, 248-258 (1992).
42. Kay, A. C. et al. Enzyme replacement therapy in type I Gaucher disease. Trans. Assoc. Am. Physicians 104, 258-264 (1991).
43. Beutler, E. et al. Enzyme replacement therapy for Gaucher disease. Blood 78, 1183-1189 (1991).
44. Barton, N. W. et al. Replacement therapy for inherited enzyme deficiency - macrophage-targeted glucocerebrosidase for Gaucher's disease. N. Engl. J. Med. 324, 1464-1470 (1991).
45. Weinreb, N. J., Charrow, J., Andersson, H. C., Kaplan P., Kolodny, E. H., Mistry, P., et al. Effectiveness of enzyme replacement therapy in 1028 patients with type 1 Gaucher disease after 2 to 5 years of treatment: a report from the Gaucher registry. Am. J. Med. 113, 112-119 (2002).
46. Damiano, A. M., Pastores, G. M., Ware, J. E. The health-related quality of life of adults with Gaucher's disease receiving enzyme replacement therapy: results from a retrospective study. Qual. Life Res. 7, 373-386 (1998).
47. Rosenberg, M., Kingma, W., Fitzpatrick, M. A., Richards, S. M. Immunosurveillance of alglucerase enzyme therapy for Gaucher patients: induction of humoral tolerance in sero-converted patients after repeat administration. Blood 99, 2081-2088 (1999).
48. Cox, T. M., Lachmann, R., Hollak, C. E., Aerts, H., van Weely, S., Hrebicek, M. et al. Novel oral treatment of Gaucher's disease with N-butyldeoxynojirimycin (OGT 918) to decrease substrate biosynthesis. Lancet 355, 1481-1485 (2000).
49. Barranger, J. A. et al. Gaucher's disease: studies of gene transfer to haematopoietic cells. Baillieres Clin. Haematol. 10, 765-778 (1997).
50. Clarke, J. T. & Iwanochko, R. M. Enzyme replacement therapy of Fabry disease. Mol. Neurobiol. 32, 43-50 (2005).
51. Brady, R. O. & Schiffmann, R. Enzyme-replacement therapy for metabolic storage disorders. Lancet Neurol. 3, 752-756 (2004).
52. Miebach, E. Enzyme replacement therapy in mucopolysaccharidosis type I. Acta. Paediatr. Suppl. 94, 58-60 discussion 57 (2005).
53. Aharon-Peretz, J., Rosenbaum, H. & Gershoni-Baruch, R. Mutations in the glucocerebrosidase gene and Parkinson's disease in Ashkenazi Jews. N. Engl. J. Med. 351, 1972-1977 (2004).
54. Tayebi, N. et al. Gaucher disease and parkinsonism: a phenotypic and genotypic characterization. Mol. Genet. Metab. 73, 313-321 (2001).
55. Wong, K. et al. Neuropathology provides clues to the pathophysiology of Gaucher disease. Mol. Genet. Metab. 82, 192-207 (2004).
56. Krebs, H. A., Henseleit, K. Untersuchungen über die harnstoffbildung im tierkörper. Z. Physiol. Chem. 210, 33-66 (1932).
57. Brusilow, S. W. & Horwich, A. L. in The Molecular and Metabolic Basis of Inherited Disease (eds Scriver, C. R., Beaudet, A. L., Sly, W. S. & Valle, D.) 1187-1232 (McGraw-Hill, New York, 1995).
58. Bachmann, C. Long-term outcome of patients with urea cycle disorders and the question of neonatal screening. Eur. J. Pediatr. 162, S29-S33 (2003).
59. Bachmann, C. Outcome and survival of 88 patients with urea cycle disorders: a retrospective evaluation. Eur. J. Pediatr. 162, 410-416 (2003).
60. Msall, M., Batshaw, M. L., Suss, R., Brusilow, S. W. & Mellits, E. D. Neurologic outcome in children with inborn errors of urea synthesis. Outcome of urea-cycle enzymopathies. N. Engl. J. Med. 310, 1500-1505 (1984).
61. Msall, M., Monahan, P. S., Chapanis, N. & Batshaw, M. L. Cognitive development in children with inborn errors of urea synthesis. Acta. Paediatr. Jpn. 30, 435-441 (1988).
62. Christopher, R., Rajivnath, V. & Shetty, K. T. Arginase deficiency. Indian J. Pediatr. 64, 266-269 (1997).
63. Crombez, E. A. & Cederbaum, S. D. Hyperargininemia due to liver arginase deficiency. Mol. Genet. Metab. 84, 243-251 (2005).
64. Gerrits, G. P. et al. Argininosuccinic aciduria: clinical and biochemical findings in three children with the late onset form, with special emphasis on cerebrospinal fluid findings of amino acids and pyrimidines. Neuropediatrics 24, 15-18 (1993).
65. Linnebank, M. et al. Argininosuccinate lyase (ASL) deficiency: mutation analysis in 27 patients and a completed structure of the human ASL gene. Hum. Genet. 111, 350-359 (2002).
66. Parsons, H. G., Scott, R. B., Pinto, A., Carter, R. J. & Snyder, F. F. Argininosuccinic aciduria: long-term treatment with arginine. J. Inherit. Metab. Dis. 10, 152-161 (1987).
67. Prasad, A. N., Breen, J. C., Ampola, M. G. & Rosman, N. P. Argininemia: a treatable genetic cause of progressive spastic diplegia simulating cerebral palsy: case reports and literature review. J. Child Neurol. 12, 301-309 (1997).
68. Reid Sutton, V., Pan, Y., Davis, E. C. & Craigen, W. J. A mouse model of argininosuccinic aciduria: biochemical characterization. Mol. Genet. Metab. 78, 11-16 (2003).
69. Maher, A. D. et al. Mathematical modelling of the urea cycle. A numerical investigation into substrate channelling. Eur. J. Biochem. 270, 3953-3961 (2003). An example of the power of computerized modelling of metabolic pathways.
70. Palacios, R., Huitron, C. & Soberon, G. Preferential hydrolysis of endogenous arginine by rat liver arginase. Biochem. Biophys. Res. Commun. 38, 438-443 (1970).
71. Hill, H. Z. & Goodman, S. I. Detection of inborn errors of metabolism. III. Defects in urea cycle metabolism. Clin. Genet. 6, 79-81 (1974).
72. Tuchman, M., Jaleel, N., Morizono, H., Sheehy, L. & Lynch, M. G. Mutations and polymorphisms in the human ornithine transcarbamylase gene. Hum. Mutat. 19, 93-107 (2002).
73. Burlina, A. B. et al. Allopurinol challenge test in children. J. Inherit. Metab. Dis. 15, 707-712 (1992).
74. Ricciuti, F. C., Gelehrter, T. D., Rosenberg, L. E. X-chromosome inactivation in human liver: confirmation of X-linkage of ornithine transcarbamylase. Am. J. Hum. Genet. 28, 332-338 (1976).
75. Hauser, E. R., Finkelstein, J. E., Valle, D. & Brusilow, S. W. Allopurinol-induced orotidinuria. A test for mutations at the ornithine carbamoyltransferase locus in women. N. Engl. J. Med. 322, 1641-1645 (1990).
76. Yudkoff, M. et al. In vivo nitrogen metabolism in ornithine transcarbamylase deficiency. J. Clin. Invest. 98, 2167-2173 (1996).
77. Scaglia, F. et al. An integrated approach to the diagnosis and prospective management of partial ornithine transcarbamylase deficiency. Pediatrics 109, 150-152 (2002).
78. Batshaw, M. L., MacArthur, R. B. & Tuchman, M. Alternative pathway therapy for urea cycle disorders: twenty years later. J. Pediatr. 138, S46-S54 discussion S54-S55 (2001).
79. Brusilow, S. W., Valle, D. L. & Batshaw, M. New pathways of nitrogen excretion in inborn errors of urea synthesis. Lancet 2, 452-454 (1979).
80. Pearson, D. L. et al. Neonatal pulmonary hypertension - urea-cycle intermediates, nitric oxide production, and carbamoyl-phosphate synthetase function. N. Engl. J. Med. 344, 1832-1838 (2001). An example of genetic variation in a metabolic pathway - the study reveals a phenotype that is not associated with classical Mendelian IEM.
81. Summar, M. L., Scott, N., Cummings, E., Hutcheson, H., Dawling, S., Christman, B. Analysis of 200 patients undergoing bone marrow transplant shows allelic disequilibrium between drug related toxicity and a common exonic polymorphism in the CPSI gene and correlates with disruption of urea cycle intermediates. Am. J. Hum. Genet. 65 (Suppl.), A25 (1999).
82. Summar, M. L. et al. Relationship between carbamoyl-phosphate synthetase genotype and systemic vascular function. Hypertension 43, 186-191 (2004).
83. Summar, M. L. et al. Environmentally determined genetic expression: clinical correlates with molecular variants of carbamyl phosphate synthetase I. Mol. Genet. Metab. 81, S12-S19 (2004).
84. Scaglia, F. et al. Clinical consequences of urea cycle enzyme deficiencies and potential links to arginine and nitric oxide metabolism. J. Nutr. 134, 2775S-2782S discussion 2796S-2797S (2004).
85. Altmuller, J., Palmer, L. J., Fischer, G., Scherb, H. & Wjst, M. Genomewide scans of complex human diseases: true linkage is hard to find. Am. J. Hum. Genet. 69, 936-950 (2001).
86. Hirschhorn, J. N., Lohmueller, K., Byrne, E. & Hirschhorn, K. A comprehensive review of genetic association studies. Genet. Med. 4, 45-61 (2002).
87. Vockley, J., Rinaldo, P., Bennett, M. J., Matern, D. & Vladutiu, G. D. Synergistic heterozygosity: disease resulting from multiple partial defects in one or more metabolic pathways. Mol. Genet. Metab. 71, 10-18 (2000).
88. Bains, W. The parts list of life. Nature Biotechnol. 19, 401-402 (2001).
89. Scriver, C. R. & Waters, P. J. Monogenic traits are not simple: lessons from phenylketonuria. Trends Genet. 15, 267-272 (1999). A further example of monogenic disorders that reveal more complex phenotypes.
90. Ideker, T. et al. Integrated genomic and proteomic analyses of a systematically perturbed metabolic network. Science 292, 929-934 (2001).
91. 13C]galactose oxidation studies in patients with galactosemia. Mol. Genet. Metab. 82, 130-136 (2004).
92. Halliday, D. & Bodamer, O. A. Measurement of glucose turnover - implications for the study of inborn errors of metabolism. Eur. J. Pediatr. 156, S35-S38 (1997).
93. Schadewaldt, P. & Wendel, U. Metabolism of branched-chain amino acids in maple syrup urine disease. Eur. J. Pediatr. 156, S62-S66 (1997).
94. Bearn, A. G. Archibald Edward Garrod, the reluctant geneticist. Genetics 137, 1-4 (1994).
95. Pauling, L., Itano, H., Singer, S. J., Wells, I. Sickle cell anemia, a molecular disease. Science 110, 543-548 (1949).
96. Ingram, V. M. A specific chemical difference between the globins of normal human and sickle-cell anaemia haemoglobin. Nature 178, 792-794 (1956).
97. Ingram, V. M. Gene mutations in human haemoglobin: the chemical difference between normal and sickle cell haemoglobin. Nature 180, 326-328 (1957).
98. McKusick, V. Human Genetics 1-148 (Prentice-Hall, Englewood Cliffs, New Jersey, 1969).
99. McKusick, V. A. On lumpers and splitters, or the nosology of genetic disease. Perspect. Biol. Med. 12, 298-312 (1969).
100. Lander, E. S. et al. Initial sequencing and analysis of the human genome. Nature 409, 860-921 (2001).
101. Nezu, J. et al. Primary systemic carnitine deficiency is caused by mutations in a gene encoding sodium ion-dependent carnitine transporter. Nature Genet. 21, 91-94 (1999).