Feline acute intermittent porphyria: A phenocopy masquerading as an erythropoietic porphyria due to dominant and recessive hydroxymethylbilane synthase mutations

Human Molecular Genetics

Volumn 19, Issue 4, 2009, Pages 584-596

  Clavero, Sonia ^a   Bishop, David F ^a   Haskins, Mark E ^b   Giger, Urs ^b   Kauppinen, Raili ^c   Desnick, Robert J ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOLEVULINIC ACID; MESSENGER RNA; PORPHOBILINOGEN; PORPHOBILINOGEN DEAMINASE; UROPORPHYRINOGEN III SYNTHASE; COPROPORPHYRIN; PORPHYRIN; UROPORPHYRIN;

ACUTE INTERMITTENT PORPHYRIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD ANALYSIS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME METABOLISM; ENZYMURIA; ERYTHROPOIETIC PROTOPORPHYRIA; EXON; EXPERIMENTAL CAT; GENE DELETION; GENE DUPLICATION; GENE EXPRESSION; GENE MUTATION; GENETIC DISORDER; HETEROZYGOSITY; HOUSEKEEPING GENE; MISSENSE MUTATION; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; ANIMAL; BONE; CAT; CAT DISEASE; CHEMICAL STRUCTURE; CHEMISTRY; CONGENITAL ERYTHROPOIETIC PORPHYRIA; DISEASE MODEL; ENZYMOLOGY; FEMALE; GENETICS; HUMAN; MALE; METABOLISM; MOLECULAR GENETICS; MUTATION; TOOTH; URINE;

ANIMALIA; FELIDAE; PROKARYOTA;

ANIMALS; BONE AND BONES; CAT DISEASES; CATS; COPROPORPHYRINS; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; HYDROXYMETHYLBILANE SYNTHASE; MALE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; PORPHYRIA, ACUTE INTERMITTENT; PORPHYRIA, ERYTHROPOIETIC; PORPHYRINS; TOOTH; UROPORPHYRINS;

EID: 77950353656     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddp525     Document Type: Article

References (44)

1. Anderson, K.E., Sassa, S., Bishop, D.F. and Desnick, R.J. (2001) Disorders of heme biosynthesis: X-Linked sideroblastic anemia and the porphyrias. Scriver, C.S., Beaudet, A.L., Sly, W.S. and Valle, D. (eds), The Metabolic and Molecular Bases of Inherited Disease., 8th edn. McGraw-Hill, New York, Vol. 2, pp.2991-3062.
2. Amoroso, E.C., Loosmore, R.M., Rimington, C. and Tooth, B.E. (1957) Congenital porphyria in bovines: first living case in Britain. Nature, 180, 230-231.
3. Clare, N.T.S. and Stephens, E.H. (1944) Congenital porphyria in pigs. Nature, 153, 252-253.
4. Jenkins, M.M., LeBoeuf, R.D., Ruth, G.R. and Bloomer, J.R. (1998) A novel stop codon mutation (X417L) of the ferrochelatase gene in bovine protoporphyria, a natural animal model of the human disease. Biochim. Biophys. Acta, 1408, 18-24.
5. Jorgensen, S.K. (1959) Congenital porphyria in pigs. Br. Vet. J., 115, 160-175.
6. Levin, E.Y. and Flyger, V. (1973) Erythropoietic porphyria of the fox squirrel Sciurus niger. J. Clin. Invest., 52, 96-105.
7. Nezamzadeh, R., Seubert, A., Pohlenz, J. and Brenig, B. (2005) Identification of a mutation in the ovine uroporphyrinogen decarboxylase (UROD) gene associated with a type of porphyria. Anim. Genet., 36, 297-302.
8. Ruth, G.R., Schwartz, S. and Stephenson, B. (1977) Bovine protoporphyria: the first nonhuman model of this hereditary photosensitizing disease. Science, 198, 199-201.
9. Shiozawa, M., Miyazawa, T., Koeda, T., Takahashi, M. and Fujiwara, H. (1995) Protoporphyric disorder in livers of broiler chickens. J. Vet. Med. Sci., 57, 549-551.
10. Tobias, G. (1964) Congenital Porphyria in a Cat. J. Am. Vet. Med. Assoc., 145, 462-463.
11. Giddens, W.E. Jr, Labbe, R.F., Swango, L.J. and Padgett, G.A. (1975) Feline congenital erythropoietic porphyria associated with severe anemia and renal disease. Clinical, morphologic, and biochemical studies. Am. J. Pathol., 80, 367-386.
12. Jorgensen, S.K. and With, T.K. (1955) Congenital porphyria in swine and cattle in Denmark. Nature, 176, 156-158.
13. Jorgensen, S.K. and With, T.K. (1963) Porphyria in domestic animals: Danish observations in pigs and cattle and comparison with human porphyria. Ann. NY Acad. Sci., 104, 701-709.
14. Glenn, B.L., Glenn, H.G. and Omtvedt, I.T. (1968) Congenital porphyria in the domestic cat (Felis catus): preliminary investigations on inheritance pattern. Am. J. Vet. Res., 29, 1653-1657.
15. Glenn, B.L. (1970) Feline porphyria: comparative aspects with porphyria of other domestic animals and man. Animal Models in Biomedical Research III, National Academy of Sciences, Washington DC, Vol. 4, pp.135-148.
16. Kauppinen, R., Mustajoki, S., Pihlaja, H., Peltonen, L. and Mustajoki, P. (1995) Acute intermittent porphyria in Finland: 19 mutations in the porphobilinogen deaminase gene. Hum. Mol. Genet., 4, 215-222.
17. Grandchamp, B., De Verneuil, H., Beaumont, C., Chretien, S., Walter, O. and Nordmann, Y. (1987) Tissue-specific expression of porphobilinogen deaminase. Two isoenzymes from a single gene. Eur. J. Biochem., 162, 105-110.
18. Cunha, L., Kuti, M., Bishop, D.F., Mezei, M., Zeng, L., Zhou, M.M. and Desnick, R.J. (2008) Human uroporphyrinogen III synthase: NMR-based mapping of the active site. Proteins, 71, 855-873.
19. Louie, G.V., Brownlie, P.D., Lambert, R., Cooper, J.B., Blundell, T.L., Wood, S.P., Warren, M.J., Woodcock, S.C. and Jordan, P.M. (1992) Structure of porphobilinogen deaminase reveals a flexible multidomain polymerase with a single catalytic site. Nature, 359, 33-39.
20. Song, G., Li, Y., Cheng, C., Zhao, Y., Gao, A., Zhang, R., Joachimiak, A., Shaw, N. and Liu, Z.J. (2009) Structural insight into acute intermittent porphyria. FASEB J., 23, 396-404.
21. Traas, A.M., Wang, P., Ma, X., Tittiger, M., Schaller, L., O'Donnell, P., Sleeper, M.M., Vite, C., Herati, R., Aguirre, G.D. et al. (2007) Correction of clinical manifestations of canine mucopolysaccharidosis I with neonatal retroviral vector gene therapy. Mol. Ther., 15, 1423-1431.
22. Sewell, A.C., Haskins, M.E. and Giger, U. (2007) Inherited metabolic disease in companion animals: searching for nature's mistakes. Vet. J., 174, 252-259.
23. Tessitore, A., Faella, A., O'Malley, T., Cotugno, G., Doria, M., Kunieda, T., Matarese, G., Haskins, M. and Auricchio, A. (2008) Biochemical, pathological, and skeletal improvement of mucopolysaccharidosis VI after gene transfer to liver but not to muscle. Mol. Ther., 16, 30-37.
24. Lindberg, R.L., Porcher, C., Grandchamp, B., Ledermann, B., Burki, K., Brandner, S., Aguzzi, A. and Meyer, U.A. (1996) Porphobilinogen deaminase deficiency in mice causes a neuropathy resembling that of human hepatic porphyria. Nat. Genet., 12, 195-199.
25. Medlock, A.E., Meissner, P.N., Davidson, B.P., Corrigall, A.V. and Dailey, H.A. (2002) A mouse model for South African (R59W) variegate porphyria: construction and initial characterization. Cell. Mol. Biol., 48, 71-78.
26. Bonkovsky, H.L. and Barnard, G. (1998) Diagnosis of porphyric syndromes: a practical approach in the era of molecular biology. Berk, P.D. and Schmid, R. (eds), Seminars in Liver Disease, Thieme Medical Publishers, Inc., New York, Vol. 18, pp.57-65.
27. Kauppinen, R. and von und zu Fraunberg, M. (2002) Molecular and biochemical studies of acute intermittent porphyria in 196 patients and their families. Clin. Chem., 48, 1891-1900.
28. De Siervi, A., Weiss Cadiz, D.E., Parera, V.E., del C Batlle, A.M. and Rossetti, M.V. (2000) Identification and characterization of two novel mutations that produce acute intermittent porphyria: a 3-base deletion (841-843delGGA) and a missense mutation (T35M). Hum. Mutat., 16, 373-377.
29. Chang, Y.F., Imam, J.S. and Wilkinson, M.F. (2007) The nonsense-mediated decay RNA surveillance pathway. Annu. Rev. Biochem., 76, 51-74.
30. Brownlie, P.D., Lambert, R., Louie, G.V., Jordan, P.M., Blundell, T.L., Warren, M.J., Cooper, J.B. and Wood, S.P. (1994) The three-dimensional structures of mutants of porphobilinogen deaminase: toward an understanding of the structural basis of acute intermittent porphyria. Protein Sci., 3, 1644-1650.
31. Delfau, M.H., Picat, C., De Rooij, F., Voortman, G., Deybach, J.C., Nordmann, Y. and Grandchamp, B. (1991) Molecular heterogeneity of acute intermittent porphyria: identification of four additional mutations resulting in the CRIM-negative subtype of the disease. Am. J. Hum. Genet., 49, 421-428.
32. Beukeveld, G.J., Wolthers, B.G., Nordmann, Y., Deybach, J.C., Grandchamp, B. and Wadman, S.K. (1990) A retrospective study of a patient with homozygous form of acute intermittent porphyria. J. Inherited Metab. Dis., 13, 673-683.
33. Llewellyn, D.H., Smyth, S.J., Elder, G.H., Hutchesson, A.C., Rattenbury, J.M. and Smith, M.F. (1992) Homozygous acute intermittent porphyria: compound heterozygosity for adjacent base transitions in the same codon of the porphobilinogen deaminase gene. Hum. Genet., 89, 97-98.
34. Solis, C., Martinez-Bermejo, A., Naidich, T.P., Kaufmann, W.E., Astrin, K.H., Bishop, D.F. and Desnick, R.J. (2004) Acute intermittent porphyria: studies of the severe homozygous dominant disease provides insights into the neurologic attacks in acute porphyrias. Arch. Neurol., 61, 1764-1770.
35. Hessels, J., Voortman, G., van der Wagen, A., van der Elzen, C., Scheffer, H. and Zuijderhoudt, F.M. (2004) Homozygous acute intermittent porphyria in a 7-year-old boy with massive excretions of porphyrins and porphyrin precursors. J. Inherited Metab. Dis., 27, 19-27.
36. Ong, P.M., Lanyon, W.G., Moore, M.R. and Connor, J.M. (1998) Acute intermittent porphyria: alternative splicing of hydroxymethylbilane synthase mRNA excludes exons 3 and 12. Mol. Cell. Probes, 12, 63-70.
37. Whatley, S.D., Woolf, J.R. and Elder, G.H. (1999) Comparison of complementary and genomic DNA sequencing for the detection of mutations in the HMBS gene in British patients with acute intermittent porphyria: identification of 25 novel mutations. Hum. Genet., 104, 505-510.
38. Unzu, C., Sampedro, A., Mauléon, I., Vanrell, L., Dubrot, J., de Salamanca, R.E., González-Aseguinolaza, G., Melero, I., Prieto, J. and Fontanellas, A. Porphobilinogen deaminase over-expression in hepatocytes, but not in erythrocytes, prevents accumulation of toxic porphyrin precursors in a mouse model of acute intermittent porphyria. J. Hepatol. doi: 10.1016/j.jhep.2009.09.003.
39. Anderson, P.M. and Desnick, R.J. (1980) Purification and properties of uroporphyrinogen I synthase from human erythrocytes. Identification of stable enzyme-substrate intermediates. J. Biol. Chem., 255, 1993-1999.
40. Bishop, D.F. and Desnick, R.J. (1986) Porphobilinogen synthase: a specific and sensitive coupled-enzyme assay. Methods Enzymol., 123, 339-345.
41. Tsai, S.F., Bishop, D.F. and Desnick, R.J. (1987) Coupled-enzyme and direct assays for uroporphyrinogen III synthase activity in human erythrocytes and cultured lymphoblasts. Enzymatic diagnosis of heterozygotes and homozygotes with congenital erythropoietic porphyria. Anal. Biochem., 166, 120-133.
42. Lim, C.K., Li, F.M. and Peters, T.J. (1988) High-performance liquid chromatography of porphyrins. J. Chromatogr., 429, 123-153.
43. Haliassos, A., Chomel, J.C., Tesson, L., Baudis, M., Kruh, J., Kaplan, J.C. and Kitzis, A. (1989) Modification of enzymatically amplified DNA for the detection of point mutations. Nucleic Acids Res., 17, 3606.
44. Tyagi, R., Lai, R. and Duggleby, R.G. (2004) A new approach to 'megaprimer' polymerase chain reaction mutagenesis without an intermediate gel purification step. BMC Biotechnol., 4,2-7.