Missense mutation in mouse GALC mimics human gene defect and offers new insights into krabbe disease

Human Molecular Genetics

Volumn 22, Issue 17, 2013, Pages 3397-3414

  Potter, Gregory B ^a,b,e   Santos, Marta ^c,d   Davisson, Muriel T ^e   Rowitch, David H ^f   Marks, Dan L ^a,b   Bongarzone, Ernesto R ^c,d   Petryniak, Magdalena A ^a,b,f  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b Pediatric Cancer Biology Program   (United States)

^c UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^d The Myelin Regeneration Group   (United States)

^e JACKSON LABORATORY   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GALACTOSYLCERAMIDASE; PSYCHOSINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEMYELINATION; DISEASE SEVERITY; ENZYME ACTIVITY; FEMALE; GENETIC DISORDER; GLIOSIS; GLOBOID CELL LEUKODYSTROPHY; HOMOZYGOSITY; MALE; MISSENSE MUTATION; MOUSE; MYELIN DEFICIENCY; NEUROPATHOLOGY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; WHITE MATTER;

EID: 84881586406     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt190     Document Type: Article

References (70)

1. Igisu, H. and Suzuki, K. (1984) Progressive accumulation of toxic metabolite in a genetic leukodystrophy. Science, 224, 753-755.
2. Xu, Y.H., Barnes, S., Sun, Y, Grabowski, G.A. (2010) Multi-system disorders of glycosphingolipid and ganglioside metabolism. J. Lipid Res., 51, 1643-1675.
3. Jacobs, J.M., Scaravilli, F, De Aranda, F.T. (1982) The pathogenesis of globoid cell leucodystrophy in peripheral nerve of the mouse mutant twitcher. J. Neurol. Sci., 55, 285-304.
4. Suzuki, K, Taniike, M. (1995) Murine model of genetic demyelinating disease: the twitcher mouse. Microsc. Res. Tech., 32, 204-214.
5. Wenger, D.A. (1997) Krabbe disease. GeneReviews at GeneTests: Medical Genetics Information Resource (database online). Copyright, University of Washington, Seattle, 2010.
6. Rafi, M.A., Luzi, P., Chen, Y.Q, Wenger, D.A. (1995) A large deletion together with a point mutation in the GALC gene is a common mutant allele in patients with infantile Krabbe disease. Hum. Mol. Genet., 4, 1285-1289.
7. Lissens, W., Arena, A., Seneca, S., Rafi, M., Sorge, G., Liebaers, I., Wenger, D, Fiumara, A. (2007) A single mutation in the GALC gene is responsible for the majority of late onset Krabbe disease patients in the Catania (Sicily, Italy) region. Hum. Mutat., 28, 742.
8. Tappino, B., Biancheri, R., Mort, M., Regis, S., Corsolini, F., Rossi, A., Stroppiano, M., Lualdi, S., Fiumara, A., Bembi, B. et al. (2010) Identification and characterization of 15 novel GALC gene mutations causing Krabbe disease. Hum. Mutat., 31, E1894-E1914.
9. Duffner, P.K., Barczykowski, A., Jalal, K., Yan, L., Kay, D.M, Carter, R.L. (2011) Early infantile Krabbe disease: results of the World-Wide Krabbe Registry. Ped. Neurol., 45, 141-148.
10. Lee, W.C., Kang, D., Causevic, E., Herdt, A.R., Eckman, E.A, Eckman, C.B. (2010) Molecular Characterization of mutations that cause globoid cell leukodystrophy and pharmacological rescue using small molecule chemical chaperones. J. Neurosci., 30, 5489-5497.
11. Wenger, D.A., Rafi, M.A, Luzi, P. (1997) Molecular genetics of Krabbe disease (globoid cell leukodystrophy): diagnostic and clinical implications. Hum. Mutat., 10, 268-279.
12. Duffner, P.K., Caggana, M., Orsini, J.J., Wenger, D.A., Patterson, M.C., Crosley, C.J., Kurtzberg, J., Arnold, G.L., Escolar, M.L., Adams, D.J. et al. (2009) Newborn screening for Krabbe disease: the New York State model. Ped. Neurol., 40, 245-252.
13. Sakai, N., Inui, K., Tatsumi, N., Fukushima, H., Nishigaki, T., Taniike, M., Nishimoto, J., Tsukamoto, H., Yanagihara, I., Ozono, K. et al. (1996) Molecular cloning and expression ofcDNAfor murine galactocerebrosidase and mutation analysis of the twitcher mouse, a model of Krabbe's disease. J. Neurochem., 66, 1118-1124.
14. Lee, W.C., Tsoi, Y.K., Dickey, C.A., DeLucia, M.W., Dickson, D.W, Eckman, C.B. (2006) Suppression of galactosylceramidase (GALC) expression in the twitcher mouse model of globoid cell leukodystrophy (GLD) is caused by nonsense-mediated mRNA decay (NMD). Neurobiol. Disease, 23, 273-280.
15. Duchen, L.W., Eicher, E.M., Jacobs, J.M., Scaravilli, F, Teixeira, F. (1980) Hereditary leucodystrophy in the mouse: the new mutant twitcher. Brain, 103, 695-710.
16. Kobayashi, T., Yamanaka, T., Jacobs, J.M., Teixeira, F, Suzuki, K. (1980) The Twitcher mouse: an enzymatically authentic model of human globoid cell leukodystrophy (Krabbe disease). Brain Res., 202, 479-483.
17. Luzi, P., Rafi, M.A., Zaka, M., Curtis, M., Vanier, M.T, Wenger, D.A. (2001) Generation of a mouse with low galactocerebrosidase activity by gene targeting: a new model of globoid cell leukodystrophy (Krabbe disease). Mol. Genet. Metab., 73, 211-223.
18. Dolcetta, D., Perani, L., Givogri, M.I., Galbiati, F., Orlacchio, A., Martino, S., Roncarolo, M.G, Bongarzone, E. (2004) Analysis of galactocerebrosidase activity in the mouse brain by a new histological staining method. J. Neurosci. Res., 77, 462-464.
19. Martino, S., Tiribuzi, R., Tortori, A., Conti, D., Visigalli, I., Lattanzi, A., Biffi, A., Gritti, A, Orlacchio, A. (2009) Specific determination of -galactocerebrosidase activity via competitive inhibition of -galactosidase. Clin. Chem., 55, 541-548.
20. Chen, Y.Q., Rafi, M.A., de Gala, G, Wenger, D.A. (1993) Cloning and expression of cDNA encoding human galactocerebrosidase, the enzyme deficient in globoid cell leukodystrophy. Hum. Mol. Genet., 2, 1841-1845.
21. Nagano, S., Yamada, T., Shinnoh, N., Furuya, H., Taniwaki, T, Kira, J. (1998) Expression and processing of recombinant human galactosylceramidase. Clin. Chim. Acta, 276, 53-61.
22. Strazza, M., Luddi, A., Carbone, M., Rafi, M.A., Costantino-Ceccarini, E, Wenger, D.A. (2009) Significant correction of pathology in brains of twitcher mice following injection of genetically modified mouse neural progenitor cells. Mol. Genet. Metab., 97, 27-34.
23. Suzuki, K. (2003) Globoid cell leukodystrophy (Krabbe's disease): update. J. Child Neurol., 18, 595-603.
24. Ohno, M., Komiyama, A., Martin, P.M, Suzuki, K. (1993) Proliferation of microglia/macrophages in the demyelinating CNS and PNS of twitcher mouse. Brain Res., 602, 268-274.
25. Takahashi, H., Igisu, H, Suzuki, K. (1983) The twitcher mouse: an ultrastructural study on the oligodendroglia. Acta Neuropath., 59, 159-166.
26. Siddiqi, Z.A., Sanders, D.B, Massey, J.M. (2006) Peripheral neuropathy in Krabbe disease: electrodiagnostic findings. Neurology, 67, 263-267.
27. Mikoshiba, K., Fujishiro, M., Kohsaka, S., Okano, H., Takamatsu, K, Tsukada, Y. (1985) Disorders in myelination in the twitcher mutant: immunohistochemical and biochemical studies. Neurochem. Res., 10, 1129-1141.
28. Castelvetri, L.C., Givogri, M.I., Zhu, H., Smith, B., Lopez-Rosas, A., Qiu, X., van Breemen, R, Bongarzone, E.R. (2011) Axonopathy is a compounding factor in the pathogenesis of Krabbe disease. Acta Neuropath., 122, 35-48.
29. Smith, B., Galbiati, F., Castelvetri, L.C., Givogri, M.I., Lopez-Rosas, A, Bongarzone, E.R. (2011) Peripheral neuropathy in the Twitcher mouse involves the activation of axonal caspase 3. ASN Neuro., 3, 213-222.
30. White, A.B., Galbiati, F., Givogri, M.I., Lopez Rosas, A., Qiu, X., van Breemen, R, Bongarzone, E.R. (2011) Persistence of psychosine in brain lipid rafts is a limiting factor in the therapeutic recovery of a mouse model for Krabbe disease. J. Neurosci. Res., 89, 352-364.
31. Stenson, P.D., Mort, M., Ball, E.V., Howells, K., Phillips, A.D., Thomas, N.S, Cooper, D.N. (2009) The Human Gene Mutation Database: 2008 update. Genome Med., 1, 13.
32. Morana, G., Biancheri, R., Dirocco, M., Filocamo, M., Marazzi, M.G., Pessagno, A, Rossi, A. (2009) Enhancing cranial nerves and cauda equina: an emerging magnetic resonance imaging pattern in metachromatic leukodystrophy and krabbe disease. Neuropediatrics, 40, 291-294.
33. Deane, J.E., Graham, S.C., Kim, N.N., Stein, P.E., McNair, R., Cachon-Gonzalez, M.B., Cox, T.M, Read, R.J. (2011) Insights into Krabbe disease from structures of galactocerebrosidase. Proc. Natl Acad. Sci. USA, 108, 15169-15173.
34. Valenzano, K.J., Khanna, R., Powe, A.C., Boyd, R., Lee, G., Flanagan, J.J, Benjamin, E.R. (2011) Identification and characterization of pharmacological chaperones to correct enzyme deficiencies in lysosomal storage disorders. Assay Drug Dev. Technol., 9, 213-235.
35. Suzuki, K. (1998) Twenty five years of the "psychosine hypothesis": a personal perspective of its history and present status. Neurochem. Res., 23, 251-259.
36. Miyatake, T, Suzuki, K. (1972) Globoid cell leukodystrophy: additional deficiency of psychosine galactosidase. Biochem. Biophys. Res. Commun., 48, 539-543.
37. LeVine, S.M., Wetzel, D.L, Eilert, A.J. (1994) Neuropathology of twitcher mice: examination by histochemistry, immunohistochemistry, lectin histochemistry and Fourier transform infrared microspectroscopy. Int. J. Dev. Neurosci., 12, 275-288.
38. Giri, S., Khan, M., Rattan, R., Singh, I, Singh, A.K. (2006) Krabbe disease: psychosine-mediated activation of phospholipase A2 in oligodendrocyte cell death. J. Lipid Res., 47, 1478-1492.
39. Suzuki, K, Tanaka, H. (1976) Studies on the pathogenesis of Krabbe's leukodystrophy: cellular reaction of the brain to exogenous galactosylsphingosine, monogalactosyl diglyceride, and lactosylceramide. Adv. Exp. Med. Biol., 68, 99-114.
40. Shinoda, H., Kobayashi, T., Katayama, M., Goto, I, Nagara, H. (1987) Accumulation of galactosylsphingosine (psychosine) in the twitcher mouse: determination by HPLC. J. Neurochem., 49, 92-99.
41. Tanaka, K., Nagara, H., Kobayashi, T, Goto, I. (1988) The twitcher mouse: accumulation of galactosylsphingosine and pathology of the sciatic nerve. Brain Res., 454, 340-346.
42. Yoshimura, T., Kobayashi, T., Shinnoh, N, Goto, I. (1990) Accumulation of galactosylsphingosine (psychosine) does not interfere with phosphorylation and methylation of myelin basic protein in the twitcher mouse. Neurochem. Res., 15, 963-967.
43. Kobayashi, T., Goto, I., Yamanaka, T., Suzuki, Y., Nakano, T, Suzuki, K. (1988) Infantile and fetal globoid cell leukodystrophy: analysis of galactosylceramide and galactosylsphingosine. Ann. Neurol., 24, 517-522.
44. Korn-Lubetzki, I., Dor-Wollman, T., Soffer, D., Raas-Rothschild, A., Hurvitz, H, Nevo, Y. (2003) Early peripheral nervous system manifestations of infantile Krabbe disease. Ped. Neurol., 28, 115-118.
45. Kobayashi, S., Katayama, M., Satoh, J., Suzuki, K, Suzuki, K. (1988) The twitcher mouse.Analteration of the unmyelinated fibers in the PNS.Am. J. Pathol., 131, 308-319.
46. Santambrogio, S., Ricca, A., Maderna, C., Ieraci, A., Aureli, M., Sonnino, S., Kulik, W., Aimar, P., Bonfanti, L., Martino, S, et al.. (2012) The galactocerebrosidase enzyme contributes to maintain a functional neurogenic niche during early post-natal CNS development. Hum. Mol. Genet., 21, 4732-4750.
47. Luzi, P., Abraham, R.M., Rafi, M.A., Curtis, M., Hooper, D.C, Wenger, D.A. (2009) Effects of treatments on inflammatory and apoptotic markers in the CNS of mice with globoid cell leukodystrophy. Brain Res., 1300, 146-158.
48. Suzuki, K. (1990) Myelin pathology in the twitcher mouse. Ann. NY Acad. Sci., 605, 313-324.
49. Gresle, M.M., Alexandrou, E., Wu, Q., Egan, G., Jokubaitis, V., Ayers, M., Jonas, A., Doherty, W., Friedhuber, A., Shaw, G, et al.. (2012) Leukemia inhibitory factor protects axons in experimental autoimmune encephalomyelitis via an oligodendrocyte-independent mechanism. PLoS One, 7, e47379.
50. Grossberg, A.J., Scarlett, J.M, Marks, D.L. (2010) Hypothalamic mechanisms in cachexia. Physiol. Behav., 100, 478-489.
51. Karst, S.Y., Ward-Bailey, P.F., Samples, R., Johnson, K.R., Donahue, L.R, Davisson, M.T. (2008) In MGI Direct Data Submission to Mouse Genome Database. The Jackson Laboratory, Bar Harbor, Maine. http ://mousemutant.jax.org/articles/mmrmutanttwi5j.html.
52. Ye, S., Dhillon, S., Ke, X., Collins, A.R, Day, I.N. (2001) An efficient procedure for genotyping single nucleotide polymorphisms. Nucleic Acids Res., 29, E88-88.
53. You, F.M., Huo, N., Gu, Y., Luo, M.-C., Ma, Y., Hane, D., Lazo, G.R., Dvorak, J, Anderson, O.D. (2008) BatchPrimer3: A high throughput web application for PCR and sequencing primer design. BMC Bioinformatics, 9, 253.
54. Galbiati, F., Basso, V., Cantuti, L., Givogri, M.I., Lopez-Rosas, A., Perez, N., Vasu, C., Cao, H., van Breemen, R., Mondino, A, et al.. (2007) Autonomic denervation of lymphoid organs leads to epigenetic immune atrophy in a mouse model of Krabbe disease. J. Neurosci., 27, 13730-13738.
55. Krasnow, S.M., Nguyen, M.L, Marks, D.L. (2011) Increased maternal fat consumption during pregnancy alters body composition in neonatal mice. Am. J. Physiol. Endocrinol. Metab., 301, E1243-E1253.
56. Lattanzi, A., Neri, M., Maderna, C., di Girolamo, I., Martino, S., Orlacchio, A., Amendola, M., Naldini, L, Gritti, A. (2010) Widespread enzymatic correction of CNS tissues by a single intracerebral injection of therapeutic lentiviral vector in leukodystrophy mouse models. Hum. Mol. Genet., 19, 2208-2227.
57. Visigalli, I., Ungari, S., Martino, S., Park, H., Cesani, M., Gentner, B., Sergi Sergi, L., Orlacchio, A., Naldini, L, Biffi, A. (2010) The galactocerebrosidase enzyme contributes to the maintenance of a functional hematopoietic stem cell niche. Blood, 116, 1857-1866.
58. Neri, M., Ricca, A., di Girolamo, I., Alcala'-Franco, B., Cavazzin, C., Orlacchio, A., Martino, S., Naldini, L, Gritti, A. (2011) Neural stem cell gene therapy ameliorates pathology and function in a mouse model of globoid cell leukodystrophy. Stem Cells, 29, 1559-1571.
59. Suzuki, K. (1983) The twitcher mouse. A model of human globoid cell leukodystrophy (krabbe's disease). Am. J. Path., 111, 394-397.
60. Tanaka, K., Nagara, H., Kobayashi, T, Goto, I. (1989) The twitcher mouse: accumulation of galactosylsphingosine and pathology of the central nervous system. Brain Res., 482, 347-350.
61. Gentner, B., Visigalli, I., Hiramatsu, H., Lechman, E., Ungari, S., Giustacchini, A., Schira, G., Amendola, M., Quattrini, A., Martino, S, et al.. (2010) Identification of hematopoietic stem cell-specific miRNAs enables gene therapy of globoid cell leukodystrophy. Sci. Transl. Med., 2, 58ra84.
62. Pellegatta, S., Tunici, P., Poliani, P.L., Dolcetta, D., Cajola, L., Colombelli, C., Ciusani, E., Di Donato, S, Finocchiaro, G. (2006) The therapeutic potential of neural stem/progenitor cells in murine globoid cell leukodystrophy is conditioned by macrophage/microglia activation. Neurobiol. Disease, 21, 314-323.
63. Wu, Y.P., McMahon, E.J., Matsuda, J., Suzuki, K, Matsushima, G.K. (2001) Expression of immune-related molecules is downregulated in twitcher mice following bone marrow transplantation. J. Neuropathol. Exp. Neurol., 60, 1062-1074.
64. Kagitani-Shimono, K., Mohri, I., Fujitani, Y., Suzuki, K., Ozono, K., Urade, Y, Taniike, M. (2005) Anti-inflammatory therapy by ibudilast, a phosphodiesterase inhibitor, in demyelination of twitcher, a genetic demyelination model. J. Neuroinflammation, 2, 10.
65. Taniike, M, Suzuki, K. (1994) Spacio-temporal progression of demyelination in twitcher mouse: with clinico-pathological correlation. Acta Neuropath., 88, 228-236.
66. Kobayashi, S., Chiu, F.C., Katayama, M., Sacchi, R.S, Suzuki, K. (1986) Expression of glial fibrillary acidic protein in the CNS and PNS of murine globoid cell leukodystrophy, the twitcher. Am. J. Path., 125, 227-243.
67. Suzuki, K, Ohno, M. (1995) Expression of immune-related molecules in a murine genetic demyelinating disease. Prog. Brain Res., 105, 289-294.
68. Taniike, M., Mohri, I., Eguchi, N., Irikura, D., Urade, Y., Okada, S, Suzuki, K. (1999) An apoptotic depletion of oligodendrocytes in the twitcher, a murine model of globoid cell leukodystrophy. J. Neuropathol. Exp. Neurol., 58, 644-653.
69. Nagara, H., Kobayashi, T, Suzuki, K. (1982) The twitcher mouse: normal pattern of early myelination in the spinal cord. Brain Res., 244, 289-294.
70. Takahashi, H, Suzuki, K. (1984) Demyelination in the spinal cord of murine globoid cell leukodystrophy (the twitcher mouse). Acta Neuropath., 62, 298-308.