Storage vesicles in neurons are related to Golgi complex alterations in mucopolysaccharidosis IIIB

American Journal of Pathology

Volumn 177, Issue 6, 2010, Pages 2984-2999

  Vitry, Sandrine ^a   Bruyère, Julie ^a   Hocquemiller, Michaël ^a   Bigou, Stéphanie ^a   Ausseil, Jérôme ^a   Colle, Marie Anne ^b   Prévost, Marie Christine ^a   Heard, Jean Michel ^a  

^a INSTITUT PASTEUR   (France)

^b INRA UMR 703   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BREFELDIN A; CELL PROTEIN; GOLGI MATRIX PROTEIN 130; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; BRAIN NERVE CELL; CELL ULTRASTRUCTURE; CELL VACUOLE; CONTROLLED STUDY; EMBRYO; ENDOCYTOSIS; GOLGI COMPLEX; LYSOSOME; MOUSE; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; SANFILIPPO SYNDROME; SANFILIPPO SYNDROME TYPE B; SECRETORY PATHWAY;

EID: 78649739968     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2010.100447     Document Type: Article

References (63)

1. Walkley SU: Pathogenic cascades in lysosomal disease-Why so complex? J Inherit Metab Dis 2009, 32:181-189
2. Sardiello M, Palmieri M, di Ronza A, Medina DL, Valenza M, Gennarino VA, Di Malta C, Donaudy F, Embrione V, Polishchuk RS, Banfi S, Parenti G, Cattaneo E, Ballabio A: A gene network regulating lysosomal biogenesis and function. Science 2009, 325:473-477
3. Lebrand C, Corti M, Goodson H, Cosson P, Cavalli V, Mayran N, Faure J, Gruenberg J: Late endosome motility depends on lipids via the small GTPase Rab7. EMBO J 2002, 21:1289-1300 (Pubitemid 34246508)
4. Cao Y, Espinola JA, Fossale E, Massey AC, Cuervo AM, MacDonald ME, Cotman SL: Autophagy is disrupted in a knock-in mouse model of juvenile neuronal ceroid lipofuscinosis. J Biol Chem 2006, 281:20483-20493
5. Pacheco CD, Kunkel R, Lieberman AP: Autophagy in Niemann-Pick C disease is dependent upon Beclin-1 and responsive to lipid trafficking defects. Hum Mol Genet 2007, 16:1495-1503
6. Settembre C, Fraldi A, Jahreiss L, Spampanato C, Venturi C, Medina D, de Pablo R, Tacchetti C, Rubinsztein DC, Ballabio A: A block of autophagy in lysosomal storage disorders. Hum Mol Genet 2008, 17:119-129
7. Takamura A, Higaki K, Kajimaki K, Otsuka S, Ninomiya H, Matsuda J, Ohno K, Suzuki Y, Nanba E: Enhanced autophagy and mitochondrial aberrations in murine G(M1)-gangliosidosis. Biochem Biophys Res Commun 2008, 367:616-622
8. Woloszynek JC, Coleman T, Semenkovich CF, Sands MS: Lysosomal dysfunction results in altered energy balance. J Biol Chem 2007, 282:35765-35771 (Pubitemid 350277125)
9. Raben N, Baum R, Schreiner C, Takikita S, Mizushima N, Ralston E, Plotz P: When more is less: excess and deficiency of autophagy coexist in skeletal muscle in Pompe disease. Autophagy 2009, 5:111-113
10. Nixon RA, Yang DS, Lee JH: Neurodegenerative lysosomal disorders: a continuum from development to late age. Autophagy 2008, 4:590-599
11. Winslow AR, Rubinsztein DC: Autophagy in neurodegeneration and development. Biochim Biophys Acta 2008, 1782:723-729
12. Tooze SA, Schiavo G: Liaisons dangereuses: autophagy, neuronal survival and neurodegeneration. Curr Opin Neurobiol 2008, 18:504-515
13. Pelled D, Lloyd-Evans E, Riebeling C, Jeyakumar M, Platt FM, Futerman AH: Inhibition of calcium uptake via the sarco/endoplasmic reticulum Ca2+-ATPase in a mouse model of Sandhoff disease and prevention by treatment with N-butyldeoxynojirimycin. J Biol Chem 2003, 278:29496-29501
14. Lloyd-Evans E, Pelled D, Riebeling C, Bodennec J, de-Morgan A, Waller H, Schiffmann R, Futerman AH: Glucosylceramide and glucosylsphingosine modulate calcium mobilization from brain microsomes via different mechanisms. J Biol Chem 2003, 278:23594-23599
15. Ginzburg L, Futerman AH: Defective calcium homeostasis in the cerebellum in a mouse model of Niemann-Pick A disease. J Neurochem 2005, 95:1619-1628
16. Bodennec J, Pelled D, Riebeling C, Trajkovic S, Futerman AH: Phosphatidylcholine synthesis is elevated in neuronal models of Gaucher disease due to direct activation of CTP:phosphocholine cytidylyl-transferase by glucosylceramide. FASEB J 2002, 16:1814-1816
17. Walkley SU: Secondary accumulation of gangliosides in lysosomal storage disorders. Semin Cell Dev Biol 2004, 15:433-444 (Pubitemid 38781905)
18. Tessitore A, del PMM, Sano R, Ma Y, Mann L, Ingrassia A, Laywell ED, Steindler DA, Hendershot LM, d'Azzo A: GM1-ganglioside-mediated activation of the unfolded protein response causes neuronal death in a neurodegenerative gangliosidosis. Mol Cell 2004, 15:753-766
19. Wei H, Kim SJ, Zhang Z, Tsai PC, Wisniewski KE, Mukherjee AB: ER and oxidative stresses are common mediators of apoptosis in both neurodegenerative and non-neurodegenerative lysosomal storage disorders and are alleviated by chemical chaperones. Hum Mol Genet 2008, 17:469-477
20. Sano R, Annunziata I, Patterson A, Moshiach S, Gomero E, Opferman J, Forte M, d'Azzo A: GM1-ganglioside accumulation at the mitochondria-associated ER membranes links ER stress to Ca(2+)-dependent mitochondrial apoptosis. Mol Cell 2009, 36:500-511
21. Li HH, Yu WH, Rozengurt N, Zhao HZ, Lyons KM, Anagnostaras S, Fanselow MS, Suzuki K, Vanier MT, Neufeld EF: Mouse model of Sanfilippo syndrome type B produced by targeted disruption of the gene encoding alpha-N- acetylglucosaminidase. Proc Natl Acad Sci USA 1999, 96:14505-14510
22. Ryazantsev S, Yu WH, Zhao HZ, Neufeld EF, Ohmi K: Lysosomal accumulation of SCMAS (subunit c of mitochondrial ATP synthase) in neurons of the mouse model of mucopolysaccharidosis III B. Mol Genet Metab 2007, 90:393-401 (Pubitemid 46484425)
23. Ohmi K, Kudo LC, Ryazantsev S, Zhao HZ, Karsten SL, Neufeld EF: Sanfilippo syndrome type B, a lysosomal storage disease, is also a tauopathy. Proc Natl Acad Sci USA 2009, 106:8332-8337
24. Ausseil J, Desmaris N, Bigou S, Attali R, Corbineau S, Vitry S, Parent M, Cheillan D, Fuller M, Maire I, Vanier M, Heard JM: Early neurodegeneration progresses independently of microglial activation by heparan sulfate in the brain of mucopolysaccharidosis IIIB mice. PloSONE 2008, 3:e2296
25. Vitry S, Ausseil J, Hocquemiller M, NBigou S, Coura R, Heard JM: Synaptophysin expression defect in cortical neurons of the mouse model of mucopolysaccharidosis type IIIB. Mol Cell Neurosci 2009, 41:8-18
26. Neufeld EF, Muenzer J: The mucopolysaccharidoses. Edited by C.R. Scriver ALB, W. S. Sly, D. Valle. New York, McGraw-Hill, 2001, p. pp. 3421-3452
27. Hadfield MG, Ghatak NR, Nakoneczna I, Lippman HR, Myer EC, Constantopoulos G, Bradley RM: Pathologic findings in mucopolysaccharidosis type IIIB (Sanfilippo's sydnrome B). Arch Neurol 1980, 37:645-650
28. Tamagawa K, Morimatsu Y, Fujisawa K, Hara A, Taketomi T: Neuropathological study and chemico-pathological correlation in sibling cases of Sanfilippo syndrome type B. Brain Dev 1985, 7:599-609
29. Cressant A, Desmaris N, Verot L, Brejot T, Froissart R, Vanier MT, Maire I, Heard JM: Improved behavior and neuropathology in the mouse model of Sanfilippo type IIIB disease after adeno-associated virus-mediated gene transfer in the striatum. J Neurosci 2004, 24:10229-10239 (Pubitemid 39492050)
30. Palmer DN, Bayliss SL, Westlake VJ: Batten disease and the ATP synthase subunit c turnover pathway: raising antibodies to subunit c. Am J Med Genet 1995, 57:260-265
31. Chen F, Vitry S, Hocquemiller M, Desmaris N, Ausseil J, Heard JM: alpha-l-Iduronidase transport in neurites. Mol Genet Metab 2006, 87:349-358 32.
32. Franceschini I, Vitry S, Padilla F, Casanova P, Tham TN, Fukuda M, Rougon G, Durbec P, Dubois-Dalcq M: Migrating and myelinating potential of neural precursors engineered to overexpress PSA-NCAM. Mol Cell Neurosci 2004, 27:151-162
33. Presley JF, Cole NB, Schroer TA, Hirschberg K, Zaal KJ, Lippincott-Schwartz J: ER-to-Golgi transport visualized in living cells [see comments]. Nature 1997, 389:81-85
34. Heldermon CD, Hennig AK, Ohlemiller KK, Ogilvie JM, Herzog ED, Breidenbach A, Vogler C, Wozniak DF, Sands MS: Development of sensory, motor and behavioral deficits in the murine model of Sanfilippo syndrome type B. PLoS ONE 2007, 2:e772
35. Hocquemiller M, Vitry S, Bigou S, Bruyere J, Ausseil J, Heard JM: GAP43 overexpression and enhanced neurite outgrowth in mucopolysaccharidosis type IIIB cortical neuron cultures. J Neurosci Res 2010, 88:202-213
36. Klionsky DJ, Abeliovich H, Agostinis P, Agrawal DK, Aliev G, Askew DS, Baba M, Baehrecke EH, Bahr BA, Ballabio A, Bamber BA, Bassham DC, Bergamini E, Bi X, Biard-Piechaczyk M, Blum JS, Bredesen DE, Brodsky JL, Brumell JH, Brunk UT, Bursch W, Camougrand N, Cebollero E, Cecconi F, Chen Y, Chin LS, Choi A, Chu CT, Chung J, Clarke PG, Clark RS, Clarke SG, Clave C, Cleveland JL, Codogno P, Colombo MI, Coto-Montes A, Cregg JM, Cuervo AM, Debnath J, Demarchi F, Dennis PB, Dennis PA, Deretic V, Devenish RJ, Di Sano F, Dice JF, Difiglia M, Dinesh-Kumar S, Distelhorst CW, Djavaheri-Mergny M, Dorsey FC, Droge W, Dron M, Dunn WA Jr, Duszenko M, Eissa NT, Elazar Z, Esclatine A, Eskelinen EL, Fesus L, Finley KD, Fuentes JM, Fueyo J, Fujisaki K, Galliot B, Gao FB, Gewirtz DA, Gibson SB, Gohla A, Goldberg AL, Gonzalez R, Gonzalez-Estevez C, Gorski S, Gottlieb RA, Haussinger D, He YW, Heidenreich K, Hill JA, Hoyer-Hansen M, Hu X, Huang WP, Iwasaki A, Jaattela M, Jackson WT, Jiang X, Jin S, Johansen T, Jung JU, Kadowaki M, Kang C, Kelekar A, Kessel DH, Kiel JA, Kim HP, Kimchi A, Kinsella TJ, Kiselyov K, Kitamoto K, Knecht E, Komatsu M, Kominami E, Kondo S, Kovacs AL, Kroemer G, Kuan CY, Kumar R, Kundu M, Landry J, Laporte M, Le W, Lei HY, Lenardo MJ, Levine B, Lieberman A, Lim KL, Lin FC, Liou W, Liu LF, Lopez-Berestein G, Lopez-Otin C, Lu B, Macleod KF, Malorni W, Martinet W, Matsuoka K, Mautner J, Meijer AJ, Melendez A, Michels P, Miotto G, Mistiaen WP, Mizushima N, Mograbi B, Monastyrska I, Moore MN, Moreira PI, Moriyasu Y, Motyl T, Munz C, Murphy LO, Naqvi NI, Neufeld TP, Nishino I, Nixon RA, Noda T, Nurnberg B, Ogawa M, Oleinick NL, Olsen LJ, Ozpolat B, Paglin S, Palmer GE, Papassideri I, Parkes M, Perlmutter DH, Perry G, Piacentini M, Pinkas-Kramarski R, Prescott M, Proikas-Cezanne T, Raben N, Rami A, Reggiori F, Rohrer B, Rubinsztein DC, Ryan KM, Sadoshima J, Sakagami H, Sakai Y, Sandri M, Sasakawa C, Sass M, Schneider C, Seglen PO, Seleverstov O, Settleman J, Shacka JJ, Shapiro IM, Sibirny A, Silva-Zacarin EC, Simon HU, Simone C, Simonsen A, Smith MA, Spanel-Borowski K, Srinivas V, Steeves M, Stenmark H, Stromhaug PE, Subauste CS, Sugimoto S, Sulzer D, Suzuki T, Swanson MS, Tabas I, Takeshita F, Talbot NJ, Talloczy Z, Tanaka K, Tanaka K, Tanida I, Taylor GS, Taylor JP, Terman A, Tettamanti G, Thompson CB, Thumm M, Tolkovsky AM, Tooze SA, Truant R, Tumanovska LV, Uchiyama Y, Ueno T, Uzcategui NL, van der Klei I, Vaquero EC, Vellai T, Vogel MW, Wang HG, Webster P, Wiley JW, Xi Z, Xiao G, Yahalom J, Yang JM, Yap G, Yin XM, Yoshimori T, Yu L, Yue Z, Yuzaki M, Zabirnyk O, Zheng X, Zhu X, Deter RL: Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 2008, 4:151-175
37. Hughes H, Stephens DJ: Assembly, organization, and function of the COPII coat. Histochem Cell Biol 2008, 129:129-151
38. Lu L, Tai G, Hong W: Autoantigen Golgin-97, an effector of Arl1 GTPase, participates in traffic from the endosome to the trans-golgi network. Mol Biol Cell 2004, 15:4426-4443 (Pubitemid 39299093)
39. Ward TH, Polishchuk RS, Caplan S, Hirschberg K, Lippincott-Schwartz J: Maintenance of Golgi structure and function depends on the integrity of ER export. J Cell Biol 2001, 155:557-570
40. Altan-Bonnet N, Sougrat R, Lippincott-Schwartz J: Molecular basis for Golgi maintenance and biogenesis. Curr Opin Cell Biol 2004, 16:364-372
41. Hirschberg K, Lippincott-Schwartz J: Secretory pathway kinetics and in vivo analysis of protein traffic from the Golgi complex to the cell surface. FASEB J 1999, 13 Suppl 2:S251-S256
42. Puri S, Linstedt AD: Capacity of the golgi apparatus for biogenesis from the endoplasmic reticulum. Mol Biol Cell 2003, 14:5011-5018
43. Horton AC, Ehlers MD: Dual modes of endoplasmic reticulum-to-Golgi transport in dendrites revealed by live-cell imaging. J Neurosci 2003, 23:6188-6199
44. Coleman M: Axon degeneration mechanisms: commonality amid diversity. Nat Rev Neurosci 2005, 6:889-898
45. Walkley SU, Baker HJ, Rattazzi MC, Haskins ME, Wu JY: Neuroaxonal dystrophy in neuronal storage disorders: evidence for major GABAergic neuron involvement. J Neurol Sci 1991, 104:1-8
46. McGlynn R, Dobrenis K, Walkley SU: Differential subcellular localization of cholesterol, gangliosides, and glycosaminoglycans in murine models of mucopolysaccharide storage disorders. J Comp Neurol 2004, 480:415-426 (Pubitemid 39587233)
47. Lachmann RH, te Vruchte D, Lloyd-Evans E, Reinkensmeier G, Sillence DJ, Fernandez-Guillen L, Dwek RA, Butters TD, Cox TM, Platt FM: Treatment with miglustat reverses the lipid-trafficking defect in Niemann-Pick disease type C. Neurobiol Dis 2004, 16:654-658
48. Fares H, Greenwald I: Regulation of endocytosis by CUP-5, the Caenorhabditis elegans mucolipin-1 homolog. Nat Genet 2001, 28:64-68
49. Puthenveedu MA, Bachert C, Puri S, Lanni F, Linstedt AD: GM130 and GRASP65-dependent lateral cisternal fusion allows uniform Golgi-enzyme distribution. Nat Cell Biol 2006, 8:238-248
50. Mitrovic S, Ben-Tekaya H, Koegler E, Gruenberg J, Hauri HP: The cargo receptors Surf4, endoplasmic reticulum-Golgi intermediate compartment (ERGIC)-53, and p25 are required to maintain the architecture of ERGIC and Golgi. Mol Biol Cell 2008, 19:1976-1990
51. Alvarez C, Garcia-Mata R, Hauri HP, Sztul E: The p115-interactive proteins GM130 and giantin participate in endoplasmic reticulum-Golgi traffic. J Biol Chem 2001, 276:2693-2700 (Pubitemid 33649127)
52. Seemann J, Jokitalo EJ, Warren G: The role of the tethering proteins p115 and GM130 in transport through the Golgi apparatus in vivo. Mol Biol Cell 2000, 11:635-645
53. Marra P, Salvatore L, Mironov A Jr, Di Campli A, Di Tullio G, Trucco A, Beznoussenko G, Mironov A, De Matteis MA: The biogenesis of the Golgi ribbon: the roles of membrane input from the ER and of GM130. Mol Biol Cell 2007, 18:1595-1608
54. Strating JR, Martens GJ: The p24 family and selective transport processes at the ER-Golgi interface. Biol Cell 2009, 101:495-509
55. Moyer BD, Allan BB, Balch WE: Rab1 interaction with a GM130 effector complex regulates COPII vesicle cis-Golgi tethering. Traffic 2001, 2:268-276
56. Preisinger C, Short B, De Corte V, Bruyneel E, Haas A, Kopajtich R, Gettemans J, Barr FA: YSK1 is activated by the Golgi matrix protein GM130 and plays a role in cell migration through its substrate 14-3-3zeta. J Cell Biol 2004, 164:1009-1020
57. Chiu CF, Ghanekar Y, Frost L, Diao A, Morrison D, McKenzie E, Lowe M: ZFPL1, a novel ring finger protein required for cis-Golgi integrity and efficient ER-to-Golgi transport. EMBO J 2008, 27:934-947 (Pubitemid 351508150)
58. Grace EA, Rabiner CA, Busciglio J: Characterization of neuronal dystrophy induced by fibrillar amyloid beta: implications for Alzheimer's disease. Neuroscience 2002, 114:265-273
59. Walkley SU, Vanier MT: Secondary lipid accumulation in lysosomal disease. Biochim Biophys Acta 2009, 1793:726-736
60. Jackson CL: Mechanisms of transport through the Golgi complex. J Cell Sci 2009, 122:443-452
61. Sutterlin C, Polishchuk R, Pecot M, Malhotra V: The Golgi-associated protein GRASP65 regulates spindle dynamics and is essential for cell division. Mol Biol Cell 2005, 16:3211-3222
62. Kodani A, Sutterlin C: The Golgi protein GM130 regulates centrosome morphology and function. Mol Biol Cell 2008, 19:745-753
63. Rivero S, Cardenas J, Bornens M, Rios RM: Microtubule nucleation at the cis-side of the Golgi apparatus requires AKAP450 and GM130. EMBO J 2009, 28:1016-1028