Heparan sulfate saccharides modify focal adhesions: Implication in mucopolysaccharidosis neuropathophysiology

Journal of Molecular Biology

Volumn 427, Issue 4, 2015, Pages 775-791

  Bruyère, Julie ^a,d   Roy, Elise ^a   Ausseil, Jérôme ^b   Lemonnier, Thomas ^a   Teyre, Guillaume ^a   Bohl, Delphine ^a   Etienne Manneville, Sandrine ^a   Lortat Jacob, Hugues ^c   Heard, Jean Michel ^a   Vitry, Sandrine ^a  

^a INSTITUT PASTEUR   (France)

^b INSERM   (France)

^c CEA GRENOBLE   (France)

^d INSERM U1005   (France)

Author keywords

Cell polarisation; Focal adhesion; Glycosaminoglycans; Mucopolysaccharidosis; Neural cell migration

Indexed keywords

CARBOHYDRATE; HEPARAN SULFATE; FOCAL ADHESION KINASE 1; PAXILLIN; PTK2 PROTEIN, HUMAN; PXN PROTEIN, MOUSE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; CELL ACTIVATION; CELL MIGRATION; CHEMICAL MODIFICATION; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FOCAL ADHESION; INTRACELLULAR SIGNALING; MOUSE; MUCOPOLYSACCHARIDOSIS; NERVE CELL; NEURAL STEM CELL; NEUROBLAST; NEUROPATHOLOGY; NONHUMAN; POLARIZATION; PRIORITY JOURNAL; WILD TYPE; ANIMAL; BIOSYNTHESIS; BRAIN; C57BL MOUSE; CELL CULTURE; CELL MOTION; CELL POLARITY; CYTOLOGY; ENZYME ACTIVATION; GENETICS; HUMAN; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PHOSPHORYLATION; PLURIPOTENT STEM CELL; SANFILIPPO SYNDROME; SWINE;

MUS;

ANIMALS; ASTROCYTES; BRAIN; CELL MOVEMENT; CELL POLARITY; CELLS, CULTURED; ENZYME ACTIVATION; FOCAL ADHESION KINASE 1; FOCAL ADHESIONS; HEPARITIN SULFATE; HUMANS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUCOPOLYSACCHARIDOSIS III; NEURAL STEM CELLS; PAXILLIN; PHOSPHORYLATION; PLURIPOTENT STEM CELLS; SWINE;

EID: 84922357984     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2014.09.012     Document Type: Article

References (54)

1. Bonneh-Barkay D, Wiley CA. Brain extracellular matrix in neurodegeneration. Brain Pathol 2009;19:573-85.
2. Maeda N, Ishii M, Nishimura K, Kamimura K. Functions of chondroitin sulfate and heparan sulfate in the developing brain. Neurochem Res 2011;36:1228-40.
3. Sarrazin S, Lamanna WC, Esko JD. Heparan sulfate proteoglycans. Cold Spring Harbor Perspect Biol 2011;3:a004952.
4. Stringer SE, Gallagher JT. Heparan sulphate. Int J Biochem Cell Biol 1997;29:709-14.
5. de Wit J, Verhaagen J. Proteoglycans as modulators of axon guidance cue function. Adv Exp Med Biol 2007;600:73-89.
6. Xian X, Gopal S, Couchman JR. Syndecans as receptors and organizers of the extracellular matrix. Cell Tissue Res 2010;339:31-46.
7. Barczyk M, Carracedo S, Gullberg D. Integrins. Cell Tissue Res 2010;339:269-80.
8. Morgan MR, Humphries MJ, Bass MD. Synergistic control of cell adhesion by integrins and syndecans. Nat Rev Mol Cell Biol 2007;8:957-69.
9. Legate KR, Wickstrom SA, Fassler R. Genetic and cell biological analysis of integrin outside-in signaling. Genes Dev 2009;23:397-418.
10. Moissoglu K, Schwartz MA. Integrin signalling in directed cell migration. Biol Cell 2006;98:547-55.
11. Mahalingam Y, Gallagher JT, Couchman JR. Cellular adhesion responses to the heparin-binding (HepII) domain of fibronectin require heparan sulfate with specific properties. J Biol Chem 2007;282:3221-30.
12. Sardiello M, Ballabio A. Lysosomal enhancement: a CLEAR answer to cellular degradative needs. Cell Cycle 2009;8:4021-2.
13. Medina DL, Fraldi A, Bouche V, Annunziata F, Mansueto G, Spampanato C, et al. Transcriptional activation of lysosomal exocytosis promotes cellular clearance. Dev Cell 2011;21:421-30.
14. Li HH, Yu WH, Rozengurt N, Zhao HZ, Lyons KM, Anagnostaras S, et al. Mouse model of Sanfilippo syndrome type B produced by targeted disruption of the gene encoding alpha-N-acetylglucosaminidase. Proc Natl Acad Sci U S A 1999;96:14505-10.
15. Ausseil J, Desmaris N, Bigou S, Attali R, Corbineau S, Vitry S, et al. Early neurodegeneration progresses independently of microglial activation by heparan sulfate in the brain of mucopolysaccharidosis IIIB mice. PLoS One 2008;3:e2296.
16. Li HH, Zhao HZ, Neufeld EF, Cai Y, Gomez-Pinilla F. Attenuated plasticity in neurons and astrocytes in the mouse model of Sanfilippo syndrome type B. J Neurosci Res 2002;69:30-8.
17. 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;88:202-13.
18. Lemonnier T, Blanchard S, Toli D, Roy E, Bigou S, Froissart R, et al. Modeling neuronal defects associated with a lysosomal disorder using patient-derived induced pluripotent stem cells. Hum Mol Genet 2011;20:3653-66.
19. Coppa GV, Buzzega D, Zampini L, Maccari F, Galeazzi T, Padella L, et al. Agarose-gel electrophoresis for the diagnosis of mucopolysaccharidoses. Clin Chem Lab Med 2011;50:589-92.
20. Etienne-Manneville S, Hall A. Integrin-mediated activation of Cdc42 controls cell polarity in migrating astrocytes through PKCzeta. Cell 2001;106:489-98.
21. Peng H, Shah W, Holland P, Carbonetto S. Integrins and dystroglycan regulate astrocyte wound healing: the integrin beta1 subunit is necessary for process extension and orienting the microtubular network. Dev Neurobiol 2008;68:559-74.
22. Osmani N, Vitale N, Borg JP, Etienne-Manneville S. Scrib controls Cdc42 localization and activity to promote cell polarization during astrocyte migration. Curr Biol 2006;16:2395-405.
23. DerMardirossian C, Bokoch GM. GDIs: central regulatory molecules in Rho GTPase activation. Trends Cell Biol 2005;15:356-63.
24. Faure J, Dagher MC. Interactions between Rho GTPases and Rho GDP dissociation inhibitor (Rho-GDI). Biochimie 2001;83:409-14.
25. Jaffe AB, Hall A. Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol 2005;21:247-69.
26. Vitry S, Bruyere J, Hocquemiller M, Bigou S, Ausseil J, Colle MA, et al. Storage vesicles in neurons are related to Golgi complex alterations in mucopolysaccharidosis IIIB. Am J Pathol 2010;177:2984-99.
27. Wilkinson FL, Holley RJ, Langford-Smith KJ, Badrinath S, Liao A, Langford-Smith A, et al. Neuropathology in mouse models of mucopolysaccharidosis type I, IIIA and IIIB. PLoS One 2012;7:e35787.
28. Belvindrah R, Hankel S, Walker J, Patton BL, Muller U. Beta1 integrins control the formation of cell chains in the adult rostral migratory stream. J Neurosci 2007;27:2704-17.
29. Sagne C, Gasnier B. Molecular physiology and pathophysiology of lysosomal membrane transporters. J Inherit Metab Dis 2008;31:258-66.
30. Roy E, Bruyere J, Flamant P, Bigou S, Ausseil J, Vitry S, et al. GM130 gain-of-function induces cell pathology in a model of lysosomal storage disease. Hum Mol Genet 2012;21:1481-95.
31. 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;480:415-26.
32. Myers JP, Robles E, Ducharme-Smith A, Gomez TM. Focal adhesion kinase modulates Cdc42 activity downstream of positive and negative axon guidance cues. J Cell Sci 2012;125:2918-29.
33. Tomar A, Lim ST, Lim Y, Schlaepfer DD. A FAK-p120Ras-GAP-p190RhoGAP complex regulates polarity in migrating cells. J Cell Sci 2009;122:1852-62.
34. Chacon MR, Fernandez G, Rico B. Focal adhesion kinase functions downstream of Sema3A signaling during axonal remodeling. Mol Cell Neurosci 2010;44:30-42.
35. Rico B, Beggs HE, Schahin-Reed D, Kimes N, Schmidt A, Reichardt LF. Control of axonal branching and synapse formation by focal adhesion kinase. Nat Neurosci 2004;7:1059-69.
36. Faye C, Moreau C, Chautard E, Jetne R, Fukai N, Ruggiero F, et al. Molecular interplay between endostatin, integrins, and heparan sulfate. J Biol Chem 2009;284:22029-40.
37. Gopal S, Bober A, Whiteford JR, Multhaupt HA, Yoneda A, Couchman JR. Heparan sulfate chain valency controls syndecan-4 function in cell adhesion. J Biol Chem 2010;285:14247-58.
38. Stehbens S, Wittmann T. Targeting and transport: how microtubules control focal adhesion dynamics. J Cell Biol 2012;198:481-9.
39. Miller PM, Folkmann AW, Maia AR, Efimova N, Efimov A, Kaverina I. Golgi-derived CLASP-dependent microtubules control Golgi organization and polarized trafficking in motile cells. Nat Cell Biol 2009;11:1069-80.
40. 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;28:1016-28.
41. Vinogradova T, Miller PM, Kaverina I. Microtubule network asymmetry in motile cells: role of Golgi-derived array. Cell Cycle 2009;8:2168-74.
42. Efimov A, Kharitonov A, Efimova N, Loncarek J, Miller PM, Andreyeva N, et al. Asymmetric CLASP-dependent nucleation of noncentrosomal microtubules at the trans-Golgi network. Dev Cell 2007;12:917-30.
43. Ohmi K, Greenberg DS, Rajavel KS, Ryazantsev S, Li HH, Neufeld EF. Activated microglia in cortex of mouse models of mucopolysaccharidoses I and IIIB. Proc Natl Acad Sci U S A 2003;100:1902-7.
44. Villani GR, Gargiulo N, Faraonio R, Castaldo S, Gonzalez YRE, Di Natale P. Cytokines, neurotrophins, and oxidative stress in brain disease from mucopolysaccharidosis IIIB. J Neurosci Res 2007;85:612-22.
45. Harper PS, Laurence KM, Parkes A, Wusteman FS, Kresse H, von Figura K, et al. Sanfilippo A disease in the fetus. J Med Genet 1974;11:123-32.
46. Lafont F, Rouget M, Triller A, Prochiantz A, Rousselet A. In vitro control of neuronal polarity by glycosaminoglycans. Development 1992;114:17-29.
47. Nishimura K, Ishii M, Kuraoka M, Kamimura K, Maeda N. Opposing functions of chondroitin sulfate and heparan sulfate during early neuronal polarization. Neuroscience 2010;169:1535-47.
48. Ronca F, Andersen JS, Paech V, Margolis RU. Characterization of Slit protein interactions with glypican-1. J Biol Chem 2001;276:29141-7.
49. Ellinwood NM, Ausseil J, Desmaris N, Bigou S, Liu S, Jens JK, et al. Safe, efficient, and reproducible gene therapy of the brain in the dog models of Sanfilippo and Hurler syndromes. Mol Ther 2010;19:251-9.
50. Crawley AC, Marshall N, Beard H, Hassiotis S, Walsh V, King B, et al. Enzyme replacement reduces neuropathology in MPS IIIA dogs. Neurobiol Dis 2011;43:422-34.
51. Etienne-Manneville S. In vitro assay of primary astrocyte migration as a tool to study Rho GTPase function in cell polarization. Methods Enzymol 2006;406:565-78.
52. Vitry S, Bertrand JY, Cumano A, Dubois-Dalcq M. Primordial hematopoietic stem cells generate microglia but not myelinforming cells in a neural environment. J Neurosci 2003;23:10724-31.
53. Brennand KJ, Simone A, Jou J, Gelboin-Burkhart C, Tran N, Sangar S, et al. Modelling schizophrenia using human induced pluripotent stem cells. Nature 2011;473:221-5.
54. Kim DS, Lee JS, Leem JW, Huh YJ, Kim JY, Kim HS, et al. Robust enhancement of neural differentiation from human ES and iPS cells regardless of their innate difference in differentiation propensity. Stem Cell Rev 2010;6:270-81.