Ataxia is the major neuropathological finding in arylsulfatase G-deficient mice: Similarities and dissimilarities to Sanfilippo disease (mucopolysaccharidosis type III)

Human Molecular Genetics

Volumn 24, Issue 7, 2014, Pages 1856-1868

  Kowalewski, Björn ^a   Heimann, Peter ^a   Ortkras, Theresa ^a   Lüllmann Rauch, Renate ^b   Sawada, Tomo ^c   Walkley, Steven U ^c   Dierks, Thomas ^a   Damme, Markus ^a,b  

^a BIELEFELD UNIVERSITY   (Germany)

^b UNIVERSITY OF KIEL   (Germany)

^c ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARYLSULFATASE; ARYLSULFATASE G; CHOLESTEROL; GANGLIOSIDE GM2; GANGLIOSIDE GM3; PROTEIN AGGREGATE; PROTEIN P62; UBIQUITIN; UNCLASSIFIED DRUG; ARYLSULFATASE G, MOUSE; GLYCOLIPID;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ARYLSULFATASE G DEFICIENCY; ASTROCYTOSIS; ATAXIA; AUTOPHAGY; BRAIN CORTEX; BRAIN NERVE CELL; CELL SURVIVAL; CELL VACUOLE; CENTRAL NERVOUS SYSTEM; CEREBELLUM; CONTROLLED STUDY; ENZYME DEFICIENCY; GLIOSIS; HUMAN VERSUS ANIMAL COMPARISON; KNOCKOUT MOUSE; LIPID STORAGE; LYSOSOME MEMBRANE; MACROAUTOPHAGY; MACROPHAGE; MOUSE; MOUSE MODEL; MYELINATION; NERVE CELL DEGENERATION; NEUROPATHOLOGY; NONHUMAN; OLIGODENDROGLIA; PHENOTYPIC VARIATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PURKINJE CELL; SANFILIPPO SYNDROME; ANIMAL; COMPARATIVE STUDY; CYTOLOGY; DEFICIENCY; DISEASE MODEL; ENZYMOLOGY; FEMALE; GENETICS; HUMAN; MALE; METABOLISM; PATHOLOGY;

MUS;

ANIMALS; ARYLSULFATASES; ATAXIA; CEREBELLUM; DISEASE MODELS, ANIMAL; FEMALE; GLIOSIS; GLYCOLIPIDS; HUMANS; MALE; MICE; MICE, KNOCKOUT; MUCOPOLYSACCHARIDOSIS III; PURKINJE CELLS;

EID: 84926451641     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddu603     Document Type: Article

References (45)

1. Valstar, M.J., Ruijter, G.J., van Diggelen, O.P., Poorthuis, B.J. and Wijburg, F.A. (2008) Sanfilippo syndrome: a mini-review. J. Inherit. Metab. Dis., 31, 240-252.
2. Neufeld, E.F. and Muenzer, J. (2001) The Mucopolysaccharidoses. In Scriver, C.R. (ed), The Metabolic and Molecular Bases of Inherited Diseases. McGraw-Hill, New York, NY, pp. 3421-3452.
3. Muenzer, J. (1986) Mucopolysaccharidoses. Adv. Pediatr., 33, 269-302.
4. Wijburg, F.A.,Wegrzyn, G., Burton, B.K. and Tylki-Szymanska, A. (2013) Mucopolysaccharidosis type III (Sanfilippo syndrome) and misdiagnosis of idiopathic developmental delay, attention deficit/hyperactivity disorder or autism spectrum disorder. Acta Paediatr. Suppl., 102, 462-470.
5. Martin, J.J., Ceuterick, C., Van Dessel, G., Lagrou, A. and Dierick, W. (1979) Two cases of mucopolysaccharidosis type III (Sanfilippo). An anatomopathological study. Acta Neuropathol., 46, 185-190.
6. Jones, M.Z., Alroy, J., Rutledge, J.C., Taylor, J.W., Alvord, E.C. Jr, Toone, J., Applegarth, D., Hopwood, J.J., Skutelsky, E., Ianelli, C. et al. (1997) Human mucopolysaccharidosis IIID: clinical, biochemical, morphological and immunohistochemical characteristics. J. Neuropath. Exp. Neur., 56, 1158-1167.
7. Elleder, M., Sokolova, J. and Hrebicek, M. (1997) Follow-up study of subunit c of mitochondrial ATP synthase (SCMAS) in Batten disease and in unrelated lysosomal disorders. Acta Neuropathol., 93, 379-390.
8. Oldfors, A. and Sourander, P. (1981) Storage of lipofuscin in neurons in mucopolysaccharidosis. Report on a case of Sanfilippo's syndrome with histochemical and electronmicroscopic findings. Acta Neuropathol., 54, 287-292.
9. Wisniewski, K., Rudelli, R., Laure-Kamionowska, M., Sklower, S., Houck, G.E. Jr, Kieras, F., Ramos, P., Wisniewski, H.M. and Braak, H. (1985) Sanfilippo disease, type Awith some features of ceroid lipofuscinosis. Neuropediatrics, 16, 98-105.
10. Ryazantsev, S., Yu, W.H., Zhao, H.Z., Neufeld, E.F. and Ohmi, K. (2007) Lysosomal accumulation of SCMAS (subunit c of mitochondrial ATP synthase) in neurons of the mouse model of mucopolysaccharidosis III B. Mol. Genet. Metab., 90, 393-401.
11. Clarke, L.A., Russell, C.S., Pownall, S., Warrington, C.L., Borowski, A., Dimmick, J.E., Toone, J. and Jirik, F.R. (1997) Murine mucopolysaccharidosis type I: targeted disruption of the murine alpha-L-iduronidase gene. Hum. Mol. Genet., 6, 503-511.
12. Li, H.H., Yu,W.H., Rozengurt, N., Zhao, H.Z., Lyons, K.M., Anagnostaras, S., Fanselow, M.S., Suzuki, K., Vanier, M.T. and Neufeld, E.F. (1999) Mouse model of Sanfilippo syndrome type B produced by targeted disruption of the gene encoding alpha-N-acetylglucosaminidase. Proc. Natl Acad. Sci. USA, 96, 14505-14510.
13. Heldermon, C.D., Qin, E.Y., Ohlemiller, K.K., Herzog, E.D., Brown, J.R., Vogler, C., Hou, W., Orrock, J.L., Crawford, B.E. and Sands, M.S. (2013) Disease correction by combined neonatal intracranial AAV and systemic lentiviral gene therapy in Sanfilippo Syndrome type B mice. Gene Ther., 20, 913-921.
14. Heldermon, C.D., Ohlemiller, K.K., Herzog, E.D., Vogler, C., Qin, E., Wozniak, D.F., Tan, Y., Orrock, J.L. and Sands, M.S. (2010) Therapeutic efficacy of bone marrow transplant, intracranial AAV-mediated gene therapy, or both in the mouse model of MPS IIIB. Mol. Ther., 18, 873-880.
15. Langford-Smith, A., Wilkinson, F.L., Langford-Smith, K.J., Holley, R.J., Sergijenko, A., Howe, S.J., Bennett,W.R., Jones, S.A., Wraith, J., Merry, C.L. et al. (2012) Hematopoietic stem cell and gene therapy corrects primary neuropathology and behavior in mucopolysaccharidosis IIIA mice. Mol. Ther., 20, 1610-1621.
16. Malinowska, M., Wilkinson, F.L., Langford-Smith, K.J., Langford-Smith, A., Brown, J.R., Crawford, B.E., Vanier, M.T., Grynkiewicz, G., Wynn, R.F., Wraith, J.E. et al. (2010) Genistein improves neuropathology and corrects behaviour in a mouse model of neurodegenerative metabolic disease. PLoS ONE, 5, e14192.
17. Kowalewski, B., Lamanna, W.C., Lawrence, R., Damme, M., Stroobants, S., Padva, M., Kalus, I., Frese, M.A., Lubke, T., Lullmann-Rauch, R. et al. (2012) Arylsulfatase G inactivation causes loss of heparan sulfate 3-O-sulfatase activity and mucopolysaccharidosis in mice. Proc. Natl Acad. Sci. USA, 109, 10310-10315.
18. Abitbol, M., Thibaud, J.L., Olby, N.J., Hitte, C., Puech, J.P., Maurer, M., Pilot-Storck, F., Hedan, B., Dreano, S., Brahimi, S. et al. (2010) A canine Arylsulfatase G (ARSG) mutation leading to a sulfatase deficiency is associated with neuronal ceroid lipofuscinosis. Proc. Natl Acad. Sci. USA, 107, 14775-14780.
19. Ko, D.C., Milenkovic, L., Beier, S.M., Manuel, H., Buchanan, J. and Scott, M.P. (2005) Cell-autonomous death of cerebellar purkinje neurons with autophagy in Niemann-Pick type C disease. PLoS Genet., 1, 81-95.
20. Sarna, J.R., Larouche, M., Marzban, H., Sillitoe, R.V., Rancourt, D.E. and Hawkes, R. (2003) Patterned Purkinje cell degeneration in mouse models of Niemann-Pick type C disease. J. Comp. Neurol., 456, 279-291.
21. Walkley, S.U. and Vanier, M.T. (2009) Secondary lipid accumulation in lysosomal disease. Biochim. Biophys. Acta, 1793, 726-736.
22. McGlynn, R., Dobrenis, K. andWalkley, S.U. (2004) Differential subcellular localization of cholesterol, gangliosides, and glycosaminoglycans in murine models of mucopolysaccharide storage disorders. J. Comp. Neurol., 480, 415-426.
23. Walkley, S.U. (2004) Secondary accumulation of gangliosides in lysosomal storage disorders. Semin. CellDev. Biol., 15, 433-444.
24. Lieberman, A.P., Puertollano, R., Raben, N., Slaugenhaupt, S., Walkley, S.U. and Ballabio, A. (2012) Autophagy in lysosomal storage disorders. Autophagy, 8, 719-730.
25. Micsenyi, M.C., Sikora, J., Stephney, G., Dobrenis, K. andWalkley, S.U. (2013) Lysosomal membrane permeability stimulates protein aggregate formation in neurons of a lysosomal disease. J. Neurosci., 33, 10815-10827.
26. Bjorkoy, G., Lamark, T., Brech, A., Outzen, H., Perander, M., Overvatn, A., Stenmark, H. and Johansen, T. (2005) p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J. Cell Biol., 171, 603-614.
27. Wilkinson, F.L., Holley, R.J., Langford-Smith, K.J., Badrinath, S., Liao, A., Langford-Smith, A., Cooper, J.D., Jones, S.A.,Wraith, J. E.,Wynn, R.F. et al. (2012) Neuropathology inmousemodels of mucopolysaccharidosis type I, IIIA and IIIB. PLoSONE, 7, e35787.
28. Bhaumik, M.,Muller, V.J., Rozaklis, T., Johnson, L., Dobrenis, K., Bhattacharyya, R.,Wurzelmann, S., Finamore, P., Hopwood, J.J., Walkley, S.U. et al. (1999) A mouse model for mucopolysaccharidosis type III A (Sanfilippo syndrome). Glycobiology, 9, 1389-1396.
29. Mato, M., Ookawara, S., Sakamoto, A., Aikawa, E., Ogawa, T., Mitsuhashi, U., Masuzawa, T., Suzuki, H., Honda, M., Yazaki, Y. et al. (1996) Involvement of specific macrophage-lineage cells surrounding arterioles in barrier and scavenger function in brain cortex. Proc. Natl Acad. Sci. USA, 93, 3269-3274.
30. Garbuzova-Davis, S., Louis, M.K., Haller, E.M., Derasari, H.M., Rawls, A.E. and Sanberg, P.R. (2011) Blood-brain barrier impairment in an animal model of MPS III B. PLoS ONE, 6, e16601.
31. Vogler, C., Levy, B., Galvin, N., Lessard, M., Soper, B. and Barker, J. (2005) Early onset of lysosomal storage disease in a murine model of mucopolysaccharidosis type VII: undegraded substrate accumulates in many tissues in the fetus and very young MPS VII mouse. Pediatr. Dev. Pathol., 8, 453-462.
32. Jones, M.Z., Alroy, J., Downs-Kelly, E., Lucas, R.E., Kraemer, S. A., Cavanagh, K.T., King, B. and Hopwood, J.J. (2004) Caprine mucopolysaccharidosis IIID: fetal and neonatal brain and liver glycosaminoglycan and morphological perturbations. J. Mol. Neurosci., 24, 277-291.
33. Thacker, B.E., Xu, D., Lawrence, R. and Esko, J.D. (2014) Heparan sulfate 3-O-sulfation: a rare modification in search of a function. Matrix Biol., 35, 60-72.
34. Eckhardt, M. (2008) The role and metabolism of sulfatide in the nervous system. Mol. Neurobiol., 37, 93-103.
35. Dekaban, A.S. and Constantopoulos, G. (1977) Mucopolysaccharidosis type I, II, IIIA and V. Pathological and biochemical abnormalities in the neural and mesenchymal elements of the brain. Acta Neuropathol., 39, 1-7.
36. Van Dessel, G., Lagrou, A., Martin, J.J., Ceuterick, C. and Dierick, W. (1979) Two cases of mucopolysaccharidosis type III (Sanfilippo). A biochemical study. J. Neurol. Sci., 40, 77-86.
37. Jones, M.Z., Alroy, J., Boyer, P.J., Cavanagh, K.T., Johnson, K., Gage, D., Vorro, J., Render, J.A., Common, R.S., Leedle, R.A. et al. (1998) Caprine mucopolysaccharidosis-IIID: clinical, biochemical, morphological and immunohistochemical characteristics. J. Neuropath. Exp. Neur., 57, 148-157.
38. Gondre-Lewis, M.C., McGlynn, R. and Walkley, S.U. (2003) Cholesterol accumulation in NPC1-deficient neurons is ganglioside dependent. Curr. Biol., 13, 1324-1329.
39. Zhou, S., Davidson, C., McGlynn, R., Stephney, G., Dobrenis, K., Vanier, M.T. and Walkley, S.U. (2011) Endosomal/lysosomal processing of gangliosides affects neuronal cholesterol sequestration in Niemann-Pick disease type C. Am. J. Pathol., 179, 890-902.
40. Maejima, I., Takahashi, A., Omori, H., Kimura, T., Takabatake, Y., Saitoh, T., Yamamoto, A., Hamasaki, M., Noda, T., Isaka, Y. et al. (2013) Autophagy sequesters damaged lysosomes to control lysosomal biogenesis and kidney injury. Embo. J., 32, 2336-2347.
41. Hung, Y.H., Chen, L.M., Yang, J.Y. and Yang, W.Y. (2013) Spatiotemporally controlled induction of autophagy-mediated lysosome turnover. Nat. Commun., 4, 2111.
42. Meyer, A., Kossow, K., Gal, A., Muhlhausen, C., Ullrich, K., Braulke, T. and Muschol, N. (2007) Scoring evaluation of the natural course of mucopolysaccharidosis type IIIA (Sanfilippo syndrome type A). Pediatrics, 120, e1255-e1261.
43. van de Kamp, J.J., Niermeijer, M.F., von Figura, K. and Giesberts, M.A. (1981) Genetic heterogeneity and clinical variability in the Sanfilippo syndrome (types A, B, and C). Clin. Genet., 20, 152-160.
44. Thacker, B.E., Xu, D., Lawrence, R. and Esko, J.D. (2013) Heparan sulfate 3-O-sulfation: a rare modification in search of a function. Matrix Biol., 35:60-72.
45. Yabe, T., Hata, T., He, J. and Maeda, N. (2005) Developmental and regional expression of heparan sulfate sulfotransferase genes in the mouse brain. Glycobiology, 15, 982-993.