Lysosomal dysfunction causes neurodegeneration in mucolipidosis II 'knock-in' mice

Brain

Volumn 135, Issue 9, 2012, Pages 2661-2675

  Kollmann, K ^a   Damme, M ^b   Markmann, S ^a   Morelle, W ^c   Schweizer, M ^a   Hermans Borgmeyer, I ^a   Rochert A K ^a   Pohl, S ^a   Lubke T ^d   Michalski, J C ^c   Kakela R ^e   Walkley, S U ^f   Braulke, T ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

^c UNIVERSITÉ DES SCIENCES ET TECHNOLOGIES DE LILLE   (France)

^d BIELEFELD UNIVERSITY   (Germany)

^e UNIVERSITY OF HELSINKI   (Finland)

^f ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

ganglioside; impaired autophagy; lysosomal storage disease; mucolipidosis; trafficking of lysosomal proteins

Indexed keywords

ALPHA LEVO FUCOSIDASE; ALPHA MANNOSIDASE; BETA N ACETYLHEXOSAMINIDASE; BIOLOGICAL MARKER; BIS(MONOACYLGLYCERO)PHOSPHATE; CHOLESTEROL; GANGLIOSIDE GM2; GANGLIOSIDE GM3; GLYCAN; LYSOSOME ENZYME; MANNOSE 6 PHOSPHATE; MICROTUBULE ASSOCIATED PROTEIN 1 LIGHT CHAIN 3; NIEMANN PICK C2 PROTEIN; PROTEIN P62; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTOSIS; AUTOPHAGY; BRAIN ATROPHY; CELL AGGREGATION; CELL LOSS; CELL SWELLING; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME BLOOD LEVEL; FEMALE; GROWTH RETARDATION; HUMAN; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MALE; MASS SPECTROMETRY; MOUSE; MUCOLIPIDOSIS TYPE 2; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN TARGETING; PURKINJE CELL; SKELETON MALFORMATION; ULTRASTRUCTURE;

EID: 84866402050     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/aws209     Document Type: Article

References (58)

1. Ballabio A, Gieselmann V. Lysosomal disorders: from storage to cellular damage. Biochim Biophys Acta 2009; 1793: 684-96.
2. Blanz J, Stroobants S, Lü llmann-Rauch R, Morelle W, Ludemann M, D'Hooge R, et al. Reversal of peripheral and central neural storage and ataxia after recombinant enzyme replacement therapy in alpha-mannosidosis mice. Hum Mol Genet 2008; 17: 3437-45.
3. Boonen M, van Meel E, Oorsschot V, Klumperman J, Kornfeld S. Vacuolization of mucolipidosis type II mouse exocrine gland cells represents accumulation of autolysosomes. Mol Biol Cell 2011; 22: 1135-47.
4. Bosshard NU, Hubler M, Arnold S, Briner J, Spycher MA, Sommerlade HJ, et al. Spontaneous mucolipidosis in a cat: an animal model of human I-cell disease. Vet Pathol 1996; 33: 1-13.
5. Braulke T, Bonifacino JS. Sorting of lysosomal proteins. Biochim Biophys Acta 2009; 1793: 605-14.
6. Cathey SS, Leroy JG, Wood T, Eaves K, Simensen RJ, Kudo M, et al. Phenotype and genotype in mucolipidosis II and III alpha/beta: a study of 61 probands. J Med Genet 2010; 47: 38-48.
7. Claussen M, Kü bler B, Wendland M, Neifer K, Schmidt B, Zapf J, et al. Proteolysis of insulin-like growth factors (IGF) and IGF binding proteins by cathepsin D. Endocrinology 1997; 138: 3797-803.
8. Cox TM, Cachon-Gonzalez MB. The cellular pathology of lysosomal diseases. J Pathol 2012; 226: 241-54.
9. Damme M, Stroobants S, Walkley SU, Lü llmann-Rauch R, D'Hooge R, Fogh J, et al. Cerebellar alterations and gait defects as therapeutic outcome measures for enzyme replacement therapy in alpha-mannosidosis. J Neuropathol Exp Neurol 2011; 70: 83-94.
10. Deffieu MS, Pfeffer SR. Niemann-Pick type C 1 function requires lumenal domain residues that mediate cholesterol-dependent NPC2 binding. Proc Natl Acad Sci USA 2011; 108: 18932-6.
11. Flanagan-Steet H, Sias C, Steet R. Altered chondrocyte differentiation and extracellular matrix homeostasis in a zebrafish model for mucoli-pidosis II. Am J Pathol 2009; 175: 2063-75.
12. Gallala HD, Sandhoff K. Biological function of the cellular lipid BMP-BMP as a key activator for cholesterol sorting and membrane digestion. Neurochem Res 2011; 36: 1594-600.
13. Gelfman CM, Vogel P, Issa TM, Turner CA, Lee WS, Kornfeld S, et al. Mice lacking alpha/beta subunits of GlcNAc-1-phosphotransferase exhibit growth retardation, retinal degeneration, and secretory cell lesions. Invest Ophthalmol Vis Sci 2007; 48: 5221-8.
14. Hickman S, Neufeld EF. A hypothesis for I-cell disease: defective hydrolases that do not enter lysosomes. Biochem Biophys Res Commun 1972; 49: 992-9.
15. Hiesberger T, Huttler S, Rohlmann A, Schneider W, Sandhoff K, Herz J. Cellular uptake of saposin (SAP) precursor and lysosomal delivery by the low density lipoprotein receptor-related protein (LRP). EMBO J. 1998; 17: 4617-25.
16. Jabs S, Quitsch A, Käkelä R, Koch B, Tyynelä J, Brade H, et al. Accumulation of bis(monoacylglycero)phosphate and gangliosides in mouse models of neuronal ceroid lipofuscinosis. J Neurochem 2008; 106: 1415-25.
17. Jansen P, Giehl K, Nyengaard JR, Teng K, Lioubinski O, Sjoegaard SS, et al. Roles for the pro-neurotrophin receptor sortilin in neuronal development, aging and brain injury. Nat Neurosci 2007; 10: 1449-57.
18. Käkelä R, Somerharju P, Tyynelä J. Analysis of phospholipid molecular species in brains from patients with infantile and juvenile neuronal-ceroid lipofuscinosis using liquid chromatography-electrospray ionization mass spectrometry. J Neurochem 2003; 84: 1051-65.
19. Kaplan A, Fischer D, Achord D, Sly W. Phosphohexosyl recognition is a general characteristic of pinocytosis of lysosomal glycosidases by human fibroblasts. J Clin Invest 1977; 60: 1088-93.
20. Karageorgos LE, Isaac EL, Brooks DA, Ravenscroft EM, Davey R, Hopwood JJ, et al. Lysosomal biogenesis in lysosomal storage disorders. Exp Cell Res 1997; 234: 85-97.
21. Kobayashi T, Beuchat MH, Lindsay M, Frias S, Palmiter RD, Sakuraba H, et al. Late endosomal membranes rich in lysobisphosphatidic acid regulate cholesterol transport. Nat Cell Biol. 1999; 1: 113-18.
22. Kollmann K, Pohl S, Marschner K, Encarnacao M, Sakwa I, Tiede S, et al. Mannose phosphorylation in health and disease. Eur J Cell Biol 2010; 89: 117-23.
23. Komatsu M, Wang QJ, Holstein GR, Friedrich VL Jr, Iwata J, Kominami E, et al. Essential role for autophagy protein Atg7 in the maintenance of axonal homeostasis and the prevention of axonal degeneration. Proc Natl Acad Sci. USA 2007; 104: 14489-94.
24. Köster A, von Figura K, Pohlmann R. Mistargeting of lysosomal enzymes in Mr 46000 mannose 6-phosphate receptor-deficient mice is compensated by carbohydrate-specific endocytotic receptors. Eur J Biochem 1994; 224: 685-9.
25. Kornfeld S, Sly WS. I-cell disease and pseudo-Hurler polydystrophy: disorders of lysosomal enzyme phosphorylation and localization. In: Scriver CR, Beaudet AL, Sly WS, Valle D, Childs B, Kinzler KW, Vogelstein B, editors. The metabolic and molecular bases of inherited disease. New York: McGraw-Hill Inc.; 2001. p. 3421-52.
26. Kudo M, Bao M, D'Souza A, Ying F, Pan H, Roe BA, et al. The alpha-and beta-subunits of the human UDP-N-acetylglucosamine:lysosomal enzyme N-acetylglucosamine-1-phosphotransferase [corrected] are encoded by a single cDNA. J Biol Chem 2005; 280: 36141-9.
27. Kudo M, Brem MS, Canfield WM. Mucolipidosis II (I-cell disease) and mucolipidosis IIIA (classical pseudo-Hurler polydystrophy) are caused by mutations in the GlcNAc-phosphotransferase a/b-subunits precursor gene. Am J Hum Genet 2006; 78: 451-63.
28. Kudo M, Canfield WM. Structural requirements for efficient processing and activation of recombinant human UDP-N-acetylglucosamine: lysosomal-enzyme-N- acetylglucosamine-1-phosphotransferase. J Biol Chem 2006; 281: 11761-8.
29. Lefrancois S, Zeng J, Hassan AJ, Canuel M, Morales CR. The lysosomal trafficking of sphingolipid activator proteins (SAPs) is mediated by sortilin. EMBO J 2003; 22: 6430-7.
30. Leroy JG, Demars RI. Mutant enzymatic and cytological phenotypes in cultured human fibroblasts. Science 1967; 157: 804-6.
31. Lübke T, Lobel P, Sleat DE. Proteomics of the lysosome. Biochim Biophys Acta 2009; 1793: 625-35.
32. Marschner K, Kollmann K, Schweizer M, Braulke T, Pohl S. A key enzyme in the biogenesis of lysosomes is a protease that regulates cholesterol metabolism. Science 2011; 333: 87-90.
33. Martin JJ, Leroy JG, van Eygen M, Ceuterick C. I-cell disease. A further report on its pathology. Acta Neuropathol 1984; 64: 234-42.
34. Mazrier H, Van Hoeven M, Wang P, Knox VW, Aguirre GD, Holt E, et al. Inheritance, biochemical abnormalities, and clinical features of feline mucolipidosis II: the first animal model of human I-cell disease. J Hered 2003; 94: 363-73.
35. Micsenyi MC, Dobrenis K, Stephney G, Pickel J, Vanier MT, Slaugenhaupt SA, et al. Neuropathology of the Mcoln1(-/-) knockout mouse model of mucolipidosis type IV. J Neuropathol Exp Neurol 2009; 68: 125-35.
36. Morelle W, Jimenez JC, Cieniewski-Bernard C, Dei-Cas E, Michalski JC. Characterization of the N-linked glycans of Giardia intestinalis. Glycobiology 2005a; 15: 549-59.
37. Morelle W, Page A, Michalski JC. Electrospray ionization ion trap mass spectrometry for structural characterization of oligosaccharides deriva-tized with 2-aminobenzamide. Rapid Commun Mass Spectrom 2005b; 19: 1145-58.
38. Mü ller-Loennies S, Galliciotti G, Kollmann K, Glatzel M, Braulke T. A novel single-chain antibody fragment for detection of mannose 6-phosphate-containing proteins: application in mucolipidosis type II patients and mice. Am J Pathol 2010; 177: 240-7.
39. Nielsen R, Courtoy PJ, Jacobsen C, Dom G, Lima WR, Jadot M, et al. Endocytosis provides a major alternative pathway for lysosomal biogenesis in kidney proximal tubular cells. Proc Natl Acad Sci USA 2007; 104: 5407-12.
40. Ong WY, Sundaram RK, Huang E, Ghoshal S, Kumar U, Pentchev PG, et al. Neuronal localization and association of Niemann Pick C2 protein (HE1/NPC2) with the postsynaptic density. Neuroscience 2004; 128: 561-70.
41. Owada M, Neufeld EF. Is there a mechanism for introducing acid hydro-lases into liver lysosomes that is independent of mannose 6-phosphate recognition? Evidence from I-cell disease. Biochem Biophys Res Commun 1982; 105: 814-20.
42. Petrey AC, Flanagan-Steet H, Johnson S, Fan X, De la Rosa M, Haskins ME, et al. Excessive activity of cathepsin K is associated with cartilage defects in a zebrafish model of mucolipidosis II. Dis Model Mech 2012; 5: 177-90.
43. Raas-Rothschild A, Cormier-Daire V, Bao M, Genin E, Salomon R, Brewer K, et al. Molecular basis of variant pseudo-hurler polydystro-phy (mucolipidosis IIIC). J Clin Invest 2000; 105: 673-81.
44. Reczek D, Schwake M, Schrö der J, Hughes H, Blanz J, Jin X, et al. LIMP-2 is a receptor for lysosomal mannose-6-phosphate-independent targeting of beta-glucocerebrosidase. Cell 2007; 131: 770-83.
45. Roces DP, Lü llmann-Rauch R, Peng J, Balducci C, Andersson C, Tollersrud O, et al. Efficacy of enzyme replacement therapy in alpha-mannosidosis mice: a preclinical animal study. Hum Mol Genet 2004; 13: 1979-88.
46. Rodriguez CI, Buchholz F, Galloway J, Sequerra R, Kasper J, Ayala R, et al. High-efficiency deleter mice show that FLPe is an alternative to Cre-loxP. Nat Genet 2000; 25: 139-40.
47. Schulze H, Kolter T, Sandhoff K. Principles of lysosomal membrane degradation: cellular topology and biochemistry of lysosomal lipid degradation. Biochim Biophys Acta 2009; 1793: 674-83.
48. Sleat DE, Zheng H, Qian M, Lobel P. Identification of sites of mannose 6-phosphorylation on lysosomal proteins. Mol Cell Proteomics 2006; 5: 686-701.
49. Spranger JW, Wiedemann HR. The genetic mucolipidoses. Diagnosis and differential diagnosis. Humangenetik 1970; 9: 113-39.
50. Tiede S, Storch S, Lü bke T, Henrissat B, Bargal R, Raas-Rothschild A, et al. Mucolipidosis II is caused by mutations in GNPTA encoding the alpha/beta GlcNAc-1-phosphotransferase. Nat Med 2005a; 11: 1109-12.
51. Tiede S, Muschol N, Reutter G, Cantz M, Ullrich K, Braulke T. Missense mutations in N-acetylglucosamine-1-phosphotransferase alpha/beta subunit gene in a patient with mucolipidosis III and a mild clinical phenotype. Am J Med Genet A 2005b; 137A: 235-40.
52. Tondeur M, Vamos-Hurwitz E, Mockel-Pohl S, Dereume JP, Cremer N, Loeb H. Clinical, biochemical, and ultrastructural studies in a case of chondrodystrophy presenting the I-cell phenotype in tissue culture. J Pediatr 1971; 79: 366-78.
53. Vogel P, Payne BJ, Read R, Lee WS, Gelfman CM, Kornfeld S. Comparative pathology of murine mucolipidosis types II and IIIC. Vet Pathol. 2009; 46: 313-24.
54. Waheed A, Pohlmann R, Hasilik A, von Figura K, van Elsen A, Leroy JG. Deficiency of UDP-N-acetylglucosamine: lysosomal enzyme N-acetylglucosamine-1- phosphotransferase in organs of I-cell patients. Biochem Biophys Res Commun 1982; 105: 1052-8.
55. Walkley SU, Sikora J, Micsenyi M, Davidson C, Dobrenis K. Lysosomal compromise and brain dysfunction: examining the role of neuroaxonal dystrophy. Biochem Soc Trans 2010; 38: 1436-41.
56. Walkley SU, Vanier MT. Secondary lipid accumulation in lysosomal disease. Biochim Biophys Acta 2009; 1793: 726-36.
57. Weinert S, Jabs S, Supanchart C, Schweizer M, Gimber N, Richter M, et al. Lysosomal pathology and osteopetrosis upon loss of H+-driven lysosomal Cl-accumulation. Science 2010; 328: 1401-3.
58. Winchester B. Lysosomal metabolism of glycoproteins. Glycobiology 2005; 15: 1R-15R.