The galactocerebrosidase enzyme contributes to maintain a functional neurogenic niche during early post-natal CNS development

Human Molecular Genetics

Volumn 21, Issue 21, 2012, Pages 4732-4750

  Santambrogio, Sara ^a,b,g   Ricca, Alessandra ^a   Maderna, Claudio ^a   Ieraci, Alessandro ^a,c   Aureli, Massimo ^c   Sonnino, Sandro ^c   Kulik, Willem ^d   Aimar, Patrizia ^e   Bonfanti, Luca ^e   Martino, Sabata ^f   Gritti, Angela ^a  

^a SAN RAFFAELE SCIENTIFIC INSTITUTE   (Italy)

^b VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

^c UNIVERSITY OF MILAN   (Italy)

^d UNIVERSITY OF AMSTERDAM   (Netherlands)

^e UNIVERSITY OF TURIN   (Italy)

^f UNIVERSITY OF PERUGIA   (Italy)

^g UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

GALACTOSYLCERAMIDASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CELL SURVIVAL; CELL TRANSPLANTATION; CONTROLLED STUDY; GENE TRANSFER; GLOBOID CELL LEUKODYSTROPHY; INFLAMMATION; LIPID STORAGE; LYSOSOME; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; OLIGODENDROGLIA; PATHOGENESIS; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; PROTEIN FUNCTION; STEM CELL NICHE; STIMULUS; SUBVENTRICULAR ZONE; UPREGULATION;

ANIMALS; CELL PROLIFERATION; CELL TRANSPLANTATION; CENTRAL NERVOUS SYSTEM; CHILD; DISEASE MODELS, ANIMAL; GALACTOSYLCERAMIDASE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE TRANSFER TECHNIQUES; GENETIC THERAPY; HUMANS; LEUKODYSTROPHY, GLOBOID CELL; MICE; NEURAL STEM CELLS; NEURONS; OLIGODENDROGLIA;

EID: 84867753672     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/dds313     Document Type: Article

References (65)

1. Suzuki, K. (2003) Globoid cell leukodystrophy (Krabbe's disease): update. J. Child Neurol., 18, 595-603.
2. Escolar, M.L., Poe, M.D., Provenzale, J.M., Richards, K.C., Allison, J., Wood, S., Wenger, D.A., Pietryga, D., Wall, D., Champagne, M. et al. (2005) Transplantation of umbilical-cord blood in babies with infantile Krabbe's disease. N. Engl. J. Med., 352, 2069-2081.
3. Biffi, A., De Palma, M., Quattrini, A., Del Carro, U., Amadio, S., Visigalli, I., Sessa, M., Fasano, S., Brambilla, R., Marchesini, S. et al. (2004) Correction of metachromatic leukodystrophy in the mouse model by transplantation of genetically modified hematopoietic stem cells. J. Clin. Invest., 113, 1118-1129.
4. Yagi, T., Matsuda, J., Tominaga, K. and Suzuki, K. (2005) Hematopoietic cell transplantation ameliorates clinical phenotype and progression of the CNS pathology in the mouse model of late onset Krabbe disease. J. Neuropathol. Exp. Neurol., 64, 565-575.
5. Lattanzi, A., Neri, M., Maderna, C., di Girolamo, I., Martino, S., Orlacchio, A., Amendola, M., Naldini, L. and 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.
6. Rafi, M.A., Zhi Rao, H., Passini, M.A., Curtis, M., Vanier, M.T., Zaka, M., Luzi, P., Wolfe, J.H. and Wenger, D.A. (2005) AAV-mediated expression of galactocerebrosidase in brain results in attenuated symptoms and extended life span in murine models of globoid cell leukodystrophy. Mol. Ther., 11, 734-744.
7. Galbiati, F., Givogri, M.I., Cantuti, L., Rosas, A.L., Cao, H., van Breemen, R. and Bongarzone, E.R. (2009) Combined hematopoietic and lentiviral gene-transfer therapies in newborn Twitcher mice reveal contemporaneous neurodegeneration and demyelination in Krabbe disease. J. Neurosci. Res., 87, 1748-1759.
8. 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.
9. Lin, D., Fantz, C.R., Levy, B., Rafi, M.A., Vogler, C., Wenger, D.A. and Sands, M.S. (2005) AAV2/5 vector expressing galactocerebrosidase ameliorates CNS disease in the murine model of globoid-cell leukodystrophy more efficiently than AAV2. Mol. Ther., 12, 422-430.
10. Peretto, P., Giachino, C., Aimar, P., Fasolo, A. and Bonfanti, L. (2005) Chain formation and glial tube assembly in the shift from neonatal to adult subventricular zone of the rodent forebrain. J. Comp. Neurol., 487, 407-427.
11. Lois, C., Garcia-Verdugo, J.M. and Alvarez-Buylla, A. (1996) Chain migration of neuronal precursors. Science, 271, 978-981.
12. Peretto, P., Merighi, A., Fasolo, A. and Bonfanti, L. (1997) Glial tubes in the rostral migratory stream of the adult rat. Brain Res. Bull., 42, 9-21.
13. Doetsch, F. (2003) A niche for adult neural stem cells. Curr. Opin. Genet. Dev., 13, 543-550.
14. Guerrero-Cazares, H., Gonzalez-Perez, O., Soriano-Navarro, M., Zamora-Berridi, G., Garcia-Verdugo, J.M. and Quinones-Hinojosa, A. (2011) Cytoarchitecture of the lateral ganglionic eminence and rostral extension of the lateral ventricle in the human fetal brain. J. Comp. Neurol., 519, 1165-1180.
15. Wang, C., Liu, F., Liu, Y.Y., Zhao, C.H., You, Y., Wang, L., Zhang, J., Wei, B., Ma, T., Zhang, Q. et al. (2011) Identification and characterization of neuroblasts in the subventricular zone and rostral migratory stream of the adult human brain. Cell. Res., 21, 1534-1550.
16. Sanai, N., Nguyen, T., Ihrie, R.A., Mirzadeh, Z., Tsai, H.H., Wong, M., Gupta, N., Berger, M.S., Huang, E., Garcia-Verdugo, J.M. et al. (2011) Corridors of migrating neurons in the human brain and their decline during infancy. Nature, 478, 382-386.
17. Inta, D., Alfonso, J., von Engelhardt, J., Kreuzberg, M.M., Meyer, A.H., van Hooft, J.A. and Monyer, H. (2008) Neurogenesis and widespread forebrain migration of distinct GABAergic neurons from the postnatal subventricular zone. Proc. Natl Acad. Sci. USA, 105, 20994-20999.
18. Cameron, H.A. and Dayer, A.G. (2008) New interneurons in the adult neocortex: small, sparse, but significant? Biol. Psychiatry, 63, 650-655.
19. Bonfanti, L. and Peretto, P. (2011) Adult neurogenesis in mammals-a theme with many variations. Eur. J. Neurosci., 34, 930-950.
20. Sanai, N., Tramontin, A.D., Quinones-Hinojosa, A., Barbaro, N.M., Gupta, N., Kunwar, S., Lawton, M.T., McDermott, M.W., Parsa, A.T., Manuel-Garcia Verdugo, J. et al. (2004) Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature, 427, 740-744.
21. Quinones-Hinojosa, A., Sanai, N., Soriano-Navarro, M., Gonzalez-Perez, O., Mirzadeh, Z., Gil-Perotin, S., Romero-Rodriguez, R., Berger, M.S., Garcia-Verdugo, J.M. and Alvarez-Buylla, A. (2006) Cellular composition and cytoarchitecture of the adult human subventricular zone: a niche of neural stem cells. J. Comp. Neurol., 494, 415-434.
22. van Echten-Deckert, G. and Herget, T. (2006) Sphingolipid metabolism in neural cells. Biochim. Biophys. Acta, 1758, 1978-1994.
23. Hannun, Y.A. and Obeid, L.M. (2008) Principles of bioactive lipid signalling: lessons from sphingolipids. Nat. Rev. Mol. Cell Biol., 9, 139-150.
24. Yu, R.K., Nakatani, Y. and Yanagisawa, M. (2009) The role of glycosphingolipid metabolism in the developing brain. J. Lipid. Res., 50(suppl), S440-S445.
25. Li, H.H., Zhao, H.Z., Neufeld, E.F., Cai, Y. and Gomez-Pinilla, F. (2002) Attenuated plasticity in neurons and astrocytes in the mouse model of Sanfilippo syndrome type B. J. Neurosci. Res., 69, 30-38.
26. Walton, R.M. and Wolfe, J.H. (2007) Abnormalities in neural progenitor cells in a dog model of lysosomal storage disease. J. Neuropathol. Exp. Neurol., 66, 760-769.
27. Kim, S.J., Park, J.S. and Kang, K.S. (2008) Stem cells in Niemann-Pick disease. Dis. Markers, 24, 231-238.
28. Visigalli, I., Ungari, S., Martino, S., Park, H., Cesani, M., Gentner, B., Sergi Sergi, L., Orlacchio, A., Naldini, L. and Biffi, A. (2010) The galactocerebrosidase enzyme contributes to the maintenance of a functional hematopoietic stem cell niche. Blood, 116, 1857-1866.
29. Escolar, M.L., Poe, M.D., Smith, J.K., Gilmore, J.H., Kurtzberg, J., Lin, W. and Styner, M. (2009) Diffusion tensor imaging detects abnormalities in the corticospinal tracts of neonates with infantile Krabbe disease. AJNR, 30, 1017-1021.
30. Castelvetri, L.C., Givogri, M.I., Zhu, H., Smith, B., Lopez-Rosas, A., Qiu, X., van Breemen, R. and Bongarzone, E.R. (2011) Axonopathy is a compounding factor in the pathogenesis of Krabbe disease. Acta Neuropathol., 122, 35-48.
31. White, A.B., Galbiati, F., Givogri, M.I., Lopez Rosas, A., Qiu, X., van Breemen, R. and 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.
32. Mirzadeh, Z., Doetsch, F., Sawamoto, K., Wichterle, H. and Alvarez-Buylla, A. (2010) The subventricular zone en-face: wholemount staining and ependymal flow. J. Vis. Exp., 39, pii: 1938.
33. Gritti, A., Dal Molin, M., Foroni, C. and Bonfanti, L. (2009) Effects of developmental age, brain region, and time in culture on long-term proliferation and multipotency of neural stem cell populations. J. Comp. Neurol., 517, 333-349.
34. Lois, C. and Alvarez-Buylla, A. (1993) Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc. Natl Acad. Sci. USA, 90, 2074-2077.
35. Reynolds, B.A. and Rietze, R.L. (2005) Neural stem cells and neurospheres-re-evaluating the relationship. Nat. Methods, 2, 333-336.
36. Pastrana, E., Silva-Vargas, V. and Doetsch, F. (2011) Eyes wide open: a critical review of sphere-formation as an assay for stem cells. Cell Stem Cell, 8, 486-498.
37. Louis, S.A., Rietze, R.L., Deleyrolle, L., Wagey, R.E., Thomas, T.E., Eaves, A.C. and Reynolds, B.A. (2008) Enumeration of neural stem and progenitor cells in the neural colony-forming cell assay. Stem Cells, 26, 988-996.
38. Ekdahl, C.T., Claasen, J.H., Bonde, S., Kokaia, Z. and Lindvall, O. (2003) Inflammation is detrimental for neurogenesis in adult brain. Proc. Natl Acad. Sci. USA, 100, 13632-13637.
39. Gritti, A. (2011) Gene therapy for lysosomal storage disorders. Expert Opin. Biol. Ther., 11, 1153-1167.
40. Neri, M., Ricca, A., di Girolamo, I., Alcala'-Franco, B., Cavazzin, C., Orlacchio, A., Martino, S., Naldini, L. and 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.
41. Luo, J., Daniels, S.B., Lennington, J.B., Notti, R.Q. and Conover, J.C. (2006) The aging neurogenic subventricular zone. Aging Cell, 5, 139-152.
42. Luzi, P., Abraham, R.M., Rafi, M.A., Curtis, M., Hooper, D.C. and 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.
43. Borda, J.T., Alvarez, X., Mohan, M., Ratterree, M.S., Phillippi-Falkenstein, K., Lackner, A.A. and Bunnell, B.A. (2008) Clinical and immunopathologic alterations in rhesus macaques affected with globoid cell leukodystrophy. Am. J. Pathol., 172, 98-111.
44. Martino, G., Pluchino, S., Bonfanti, L. and Schwartz, M. (2011) Brain regeneration in physiology and pathology: the immune signature driving therapeutic plasticity of neural stem cells. Physiol. Rev., 91, 1281-1304.
45. Hofling, A.A., Kim, J.H., Fantz, C.R., Sands, M.S. and Song, S.K. (2009) Diffusion tensor imaging detects axonal injury and demyelination in the spinal cord and cranial nerves of a murine model of globoid cell leukodystrophy. NMR Biomed., 22, 1100-1106.
46. Chan, W.Y., Kohsaka, S. and Rezaie, P. (2007) The origin and cell lineage of microglia: new concepts. Brain Res. Rev., 53, 344-354.
47. Rossi, D. and Volterra, A. (2009) Astrocytic dysfunction: insights on the role in neurodegeneration. Brain Res. Bull., 80, 224-232.
48. Kielar, C., Wishart, T.M., Palmer, A., Dihanich, S., Wong, A.M., Macauley, S.L., Chan, C.H., Sands, M.S., Pearce, D.A., Cooper, J.D. et al. (2009) Molecular correlates of axonal and synaptic pathology in mouse models of Batten disease. Hum. Mol. Genet., 18, 4066-4080.
49. Robel, S., Berninger, B. and Gotz, M. (2011) The stem cell potential of glia: lessons from reactive gliosis. Nat. Rev. Neurosci., 12, 88-104.
50. Igisu, H. and Suzuki, K. (1984) Glycolipids of the spinal cord, sciatic nerve, and systemic organs of the twitcher mouse. J. Neuropathol. Exp. Neurol., 43, 22-36.
51. Kobayashi, T., Goto, I., Yamanaka, T., Suzuki, Y., Nakano, T. and Suzuki, K. (1988) Infantile and fetal globoid cell leukodystrophy: analysis of galactosylceramide and galactosylsphingosine. Ann. Neurol., 24, 517-522.
52. Taylor, R.M., Lee, J.P., Palacino, J.J., Bower, K.A., Li, J., Vanier, M.T., Wenger, D.A., Sidman, R.L. and Snyder, E.Y. (2006) Intrinsic resistance of neural stem cells to toxic metabolites may make them well suited for cell non-autonomous disorders: evidence from a mouse model of Krabbe leukodystrophy. J. Neurochem., 97, 1585-1599.
53. White, A.B., Givogri, M.I., Lopez-Rosas, A., Cao, H., van Breemen, R., Thinakaran, G. and Bongarzone, E.R. (2009) Psychosine accumulates in membrane microdomains in the brain of krabbe patients, disrupting the raft architecture. J. Neurosci., 29, 6068-6077.
54. Lloyd-Evans, E., Pelled, D., Riebeling, C., Bodennec, J., de-Morgan, A., Waller, H., Schiffmann, R. and Futerman, A.H. (2003) Glucosylceramide and glucosylsphingosine modulate calcium mobilization from brain microsomes via different mechanisms. J. Biol. Chem., 278, 23594-23599.
55. Hans, M., Pusch, A., Dai, L., Racke, K., Swandulla, D., Gieselmann, V. and Kappler, J. (2009) Lysosulfatide regulates the motility of a neural precursor cell line via calcium-mediated process collapse. Neurochem. Res., 34, 508-517.
56. Pelled, D., Trajkovic-Bodennec, S., Lloyd-Evans, E., Sidransky, E., Schiffmann, R. and Futerman, A.H. (2005) Enhanced calcium release in the acute neuronopathic form of Gaucher disease. Neurobiol. Dis., 18, 83-88.
57. Kamiguchi, H. (2006) The region-specific activities of lipid rafts during axon growth and guidance. J. Neurochem., 98, 330-335.
58. Cearley, C.N. and Wolfe, J.H. (2007) A single injection of an adeno-associated virus vector into nuclei with divergent connections results in widespread vector distribution in the brain and global correction of a neurogenetic disease. J. Neurosci., 27, 9928-9940.
59. Passini, M.A., Macauley, S.L., Huff, M.R., Taksir, T.V., Bu, J., Wu, I.H., Piepenhagen, P.A., Dodge, J.C., Shihabuddin, L.S., O'Riordan, C.R. et al. (2005) AAV vector-mediated correction of brain pathology in a mouse model of Niemann-Pick A disease. Mol. Ther., 11, 754-762.
60. Givogri, M.I., Bottai, D., Zhu, H.L., Fasano, S., Lamorte, G., Brambilla, R., Vescovi, A., Wrabetz, L. and Bongarzone, E. (2008) Multipotential neural precursors transplanted into the metachromatic leukodystrophy brain fail to generate oligodendrocytes but contribute to limit brain dysfunction. Dev. Neurosci., 30, 340-357.
61. Braulke, T. and Bonifacino, J.S. (2009) Sorting of lysosomal proteins. Biochim. Biophys. Acta, 1793, 605-614.
62. Suzuki, K. (1995) The twitcher mouse: a model for Krabbe disease and for experimental therapies. Brain Pathol., 5, 249-258.
63. Prinetti, A., Chigorno, V., Tettamanti, G. and Sonnino, S. (2000) Sphingolipid-enriched membrane domains from rat cerebellar granule cells differentiated in culture. A compositional study. J. Biol. Chem., 275, 11658-11665.
64. Dolcetta, D., Perani, L., Givogri, M.I., Galbiati, F., Orlacchio, A., Martino, S., Roncarolo, M.G. and Bongarzone, E. (2004) Analysis of galactocerebrosidase activity in the mouse brain by a new histological staining method. J. Neurosci. Res., 77, 462-464.
65. Martino, S., Tiribuzi, R., Tortori, A., Conti, D., Visigalli, I., Lattanzi, A., Biffi, A., Gritti, A. and Orlacchio, A. (2009) Specific determination of beta-galactocerebrosidase activity via competitive inhibition of beta-galactosidase. Clin. Chem., 55, 541-548.