Proteoglycans and neuronal migration in the cerebral cortex during development and disease

Frontiers in Neuroscience

Volumn 9, Issue MAR, 2015, Pages

  Maeda, Nobuaki ^a  

^a TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

Author keywords

Chondroitin sulfate; Extracellular matrix; Heparan sulfate; Neuronal migration; Proteoglycan

Indexed keywords

CHONDROITIN SULFATE; CORE PROTEIN; GLYCOSAMINOGLYCAN; HEPARAN SULFATE; NEUROCAN; PHOSPHACAN; PROTEOGLYCAN; UNCLASSIFIED DRUG; VERSICAN;

ARTICLE; BIOSYNTHESIS; BRAIN CORTEX; CELL MIGRATION; CORPUS STRIATUM; EXTRACELLULAR MATRIX; GLYCOSAMINOGLYCAN METABOLISM; HUMAN; INTELLECTUAL IMPAIRMENT; LIGAND BINDING; MENTAL DISEASE; NEOCORTEX; NERVE CELL; NERVE CELL DIFFERENTIATION; NONHUMAN; POLARIZATION; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN STRUCTURE; SUBVENTRICULAR ZONE;

EID: 84928041519     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2015.00098     Document Type: Article

References (123)

1. Ai, X., Do, A. T., Lozynska, O., Kusche-Gullberg, M., Lindahl, U., and Emerson, C. P. (2003). QSulf1 remodels the 6-O sulfation states of cell surface heparan sulfate proteoglycans to promote Wnt signaling. J. Cell Biol. 162, 341-351. doi: 10.1083/jcb.200212083
2. Ai, X., Kitazawa, T., Do, A. T., Kusche-Gullberg, M., Labosky, P. A., and Emerson, C. P. (2007). SULF1 and SULF2 regulate heparan sulfate-mediated GDNF signaling for esophageal innervation. Development 134, 3327-3338. doi: 10.1242/dev.007674
3. Aono, S., Tokita, Y., Shuo, T., Yamauchi, S., Matsui, F., Nakanishi, K., et al. (2004). Glycosylation site for chondroitin sulfate on the neural part-time proteoglycan, neuroglycan C. J. Biol. Chem. 279, 46536-46541. doi: 10.1074/jbc.M403263200
4. Aspberg, A., Miura, R., Bourdoulous, S., Shimonaka, M., Heinegard, D., Schachner, M., et al. (1997). The C-type lectin domains of lecticans, a family of aggregating chondroitin sulfate proteoglycans, bind tenascin-R by protein-protein interactions independent of carbohydrate moiety. Proc. Natl. Acad. Sci. U.S.A. 94, 10116-10121. doi: 10.1073/pnas.94.19.10116
5. Berretta, S. (2012). Extracellular matrix abnormalities in schizophrenia. Neuropharmacology 62, 1584-1597. doi: 10.1016/j.neuropharm.2011.08.010
6. Bespalov, M. M., Sidorova, Y. A., Tumova, S., Ahonen-Bishopp, A., Magalhaes, A. C., Kulesskiy, E., et al. (2011). Heparan sulfate proteoglycan syndecan-3 is a novel receptor for GDNF, neurturin, and artemin. J. Cell Biol. 192, 153-169. doi: 10.1083/jcb.201009136
7. Buxbaum, J. D., Georgieva, L., Young, J. J., Plescia, C., Kajiwara, Y., Jiang, Y., et al. (2008). Molecular dissection of NRG1-ERBB4 signaling implicates PTPRZ1 as a potential schizophrenia susceptibility gene. Mol. Psychiatry 13, 162-172. doi: 10.1038/sj.mp.4001991
8. Choi, S., Lee, E., Kwon, S., Park, H., Yi, J. Y., Kim, S., et al. (2005). Transmembrane domain-induced oligomerization is crucial for the functions of syndecan-2 and syndecan-4. J. Biol. Chem. 280, 42573-42579. doi: 10.1074/jbc.M509238200
9. Coles, C. H., Shen, Y., Tenney, A. P., Siebold, C., Sutton, G. C., Lu, W., et al. (2011). Proteoglycan-specific molecular switch for RPTP? clustering and neuronal extension. Science 332, 484-488. doi: 10.1126/science.1200840
10. Conrad, A. H., Zhang, Y., Tasheva, E. S., and Conrad, G. W. (2010). Proteomic analysis of potential keratan sulfate, chondroitin sulfate A, and hyaluronic acid molecular interactions. Invest. Ophthalmol. Vis. Sci. 51, 4500-4515. doi: 10.1167/iovs.09-4914
11. Conway, C. D., Howe, K. M., Nettleton, N. K., Price, D. J., Mason, J. O., and Pratt, T. (2011). Heparan sulfate sugar modifications mediate the functions of Slits and other factors needed for mouse forebrain commissure development. J. Neurosci. 31, 1955-1970. doi: 10.1523/JNEUROSCI.2579-10.2011
12. Deepa, S. S., Umehara, Y., Higashiyama, S., Itoh, N., and Sugahara, K. (2002). Specific molecular interactions of oversulfated chondroitin sulfate E with various heparin-binding growth factors. J. Biol. Chem. 277, 43707-43716. doi: 10.1074/jbc.M207105200
13. Deepa, S. S., Yamada, S., Zako, M., Goldberger, O., and Sugahara, K. (2004). Chondroitin sulfate chains on Syndecan-1 and Syndecan-4 from normal murine mammary gland epithelial cells are structurally and functionally distinct and cooperate with heparan sulfate chains to bind growth factors. J. Biol. Chem. 279, 37368-37376. doi: 10.1074/jbc.M403031200
14. Dhamija, R., Graham, J. M., Smaoui, N., Thorland, E., and Kirmani, S. (2014). Novel de novo SPOCK1 mutation in a proband with developmental delay, microcephaly and agenesis of corpus callosum. Eur. J. Med. Genet. 57, 181-184. doi: 10.1016/j.ejmg.2014.02.009
15. Dick, G., Tan, C. L., Alves, J. N., Ehlert, E. M., Miller, G. M., Hsieh-Wilson, L. C., et al. (2013). Semaphorin 3A binds to the perineuronal nets via chondroitin sulfate type E motifs in rodent brains. J. Biol. Chem. 288, 27384-27395. doi: 10.1074/jbc.M111.310029
16. Dotti, C. G., Sullivan, C. A., and Banker, G. A. (1988). The establishment of polarity by hippocampal neurons in culture. J. Neurosci. 8, 1454-1468.
17. Evsyukova, I., Plestant, C., and Anton, E. S. (2013). Integrative mechanism of oriented neuronal migration in the developing brain. Annu. Rev. Cell Dev. Biol. 29, 299-353. doi: 10.1146/annurev-cellbio-101512-122400
18. Feng, Z. J., Gao, S. B., Wu, Y., Xu, X. F., Hua, X., and Jin, G. H. (2010). Lung cancer cell migration is regulated via repressing growth factor PTN/RPTP ß/? signaling by menin. Oncogene 29, 5416-5426. doi: 10.1038/onc.2010.282
19. Filmus, J., and Capurro, M. (2014). The role of glypicans in Hedgehog signaling. Matrix Biol. 35, 248-252. doi: 10.1016/j.matbio.2013.12.007
20. Filmus, J., Capurro, M., and Rast, J. (2008). Glypicans. Genome Biol. 9:224. doi: 10.1186/gb-2008-9-5-224
21. Fisher, D., Xing, B., Dill, J., Li, H., Hoang, H. H., Zhao, Z., et al. (2011). Leukocyte common antigen-related phosphatase is a functional receptor for chondroitin sulfate proteoglycan axon growth inhibitors. J. Neurosci. 31, 14051-14066. doi: 10.1523/JNEUROSCI.1737-11.2011
22. Flames, N., Long, J. E., Garratt, A. N., Fischer, T. M., Gassmann, M., Birchmeier, C., et al. (2004). Short- and long-range attraction of cortical GABAergic interneurons by neuregulin-1. Neuron 44, 251-261. doi: 10.1016/j.neuron.2004.09.028
23. Franco, S. J., and Muller, U. (2011). Extracellular matrix functions during neuronal migration and lamination in the mammalian central nervous system. Dev. Neurobiol. 71, 889-900. doi: 10.1002/dneu.20946
24. Fukada, M., Fujikawa, A., Chow, J. P., Ikematsu, S., Sakuma, S., and Noda, M. (2006). Protein tyrosine phosphatase receptor type Z is inactivated by ligand-induced oligomerization. FEBS Lett. 580, 4051-4056. doi: 10.1016/j.febslet.2006.06.041
25. Goossens, D., Gestel, S., Claes, S., Rijk, P. D., Souery, D., Massat, I., et al. (2003). A novel CpG-associated brain-expressed candidate gene for chromosome 18q-linked bipolar disorder. Mol. Psychiatry 8, 83-89. doi: 10.1038/sj.mp.4001190
26. Herndon, M. E., Stipp, C. S., and Lander, A. D. (1999). Interactions of neural glycosaminoglycans and proteoglycans with protein ligands: assessment of selectivity, heterogeneity and the participation of core proteins in binding. Glycobiology 9, 143-155. doi: 10.1093/glycob/9.2.143
27. Hienola, A., Tumova, S., Kulesskiy, E., and Rauvala, H. (2006). N-syndecan deficiency impairs neural migration in brain. J. Cell Biol. 174, 569-580. doi: 10.1083/jcb.200602043
28. Hirose, J., Kawashima, H., Yoshie, O., Tashiro, K., and Miyasaka, M. (2001). Versican interacts with chemokines and modulates cellular responses. J. Biol. Chem. 276, 5228-5234. doi: 10.1074/jbc.M007542200
29. Hu, H. (2001). Cell surface heparan sulfate is involved in the repulsive guidance activities of Slit2 protein. Nat. Neurosci. 4, 695-701. doi: 10.1038/89482
30. Huegel, J., Sgariglia, F., Enomoto-Iwamoto, M., Koyama, E., Dormans, J. P., and Pacifici, M. (2013). Heparan sulfate in skeletal development, growth, and pathology: the case of hereditary multiple exostoses. Dev. Dyn. 242, 1021-1032. doi: 10.1002/dvdy.24010
31. Ichihara-Tanaka, K., Oohira, A., Rumsby, M., and Muramatsu, T. (2006). Neuroglycan C is a novel midkine receptor involved in process elongation of oligodendroglial precursor-like cells. J. Biol. Chem. 281, 30857-30864. doi: 10.1074/jbc.M602228200
32. Irie, F., Okuno, M., Matsumoto, K., Pasquale, E. B., and Yamaguchi, Y. (2008). Heparan sulfate regulates ephrin-A3/EphA receptor signaling. Proc. Natl. Acad. Sci. U.S.A. 105, 12307-12312. doi: 10.1073/pnas.0801302105
33. Ishii, M., and Maeda, N. (2008a). Oversulfated chondroitin sulfate plays critical roles in the neuronal migration in the cerebral cortex. J. Biol. Chem. 283, 32610-32620. doi: 10.1074/jbc.M806331200
34. Ishii, M., and Maeda, N. (2008b). Spatiotemporal expression of chondroitin sulfate sulfotransferases in the postnatal developing mouse cerebellum. Glycobiology 18, 602-614. doi: 10.1093/glycob/cwn040
35. Ito, Y., Yamada, S., Takahashi, N., Saito, S., Yoshimi, A., Inada, T., et al. (2008). No association between the protein tyrosine phosphatase, receptor-type, Z polypeptide 1 (PTPRZ1) gene and schizophrenia in the Japanese population. Am. J. Med. Genet. B Neuropsychiatr. Genet. 147B, 1013-1018. doi: 10.1002/ajmg.b.30692
36. Kantor, D. B., Chivatakarn, O., Peer, K. L., Oster, S. F., Inatani, M., Hansen, M. J., et al. (2004). Semaphorin 5A is a bifunctional axon guidance cue regulated by heparan and chondroitin sulfate proteoglycans. Neuron 44, 961-975. doi: 10.1016/j.neuron.2004.12.002
37. Kawashima, H., Atarashi, K., Hirose, M., Hirose, J., Yamada, S., Sugahara, K., et al. (2002). Oversulfated chondroitin/dermatan sulfates containing GlcAß1/IdoAa1-3GalNAc(4,6-O-disulfate) interact with L- and P-selectin and chemokines. J. Biol. Chem. 277, 12921-12930. doi: 10.1074/jbc.M200396200
38. Kinnunen, T., Raulo, E., Nolo, R., Maccarana, M., Lindahl, U., and Rauvala, H. (1996). Neurite outgrowth in brain neurons induced by heparin-binding growth-associated molecule (HB-GAM) depends on the specific interaction of HB-GAM with heparan sulfate at the cell surface. J. Biol. Chem. 271, 2243-2248. doi: 10.1074/jbc.271.4.2243
39. Kinugasa, Y., Ishiguro, H., Tokita, Y., Oohira, A., Ohmoto, H., and Higashiyama, S. (2004). Neuroglycan C, a novel member of the neuregulin family. Biochem. Biophys. Res. Commun. 321, 1045-1049. doi: 10.1016/j.bbrc.2004.07.066
40. Koutsioumpa, M., Polytarchou, C., Courty, J., Zhang, Y., Kieffer, N., Mikelis, C., et al. (2013). Interplay between avß3 integrin and nucleolin regulates human endothelial and glioma cell migration. J. Biol. Chem. 288, 343-354. doi: 10.1074/jbc.M112.387076
41. Krueger, N. X., and Saito, H. (1992). A human transmembrane protein- tyrosine-phosphatase, PTP?, is expressed in brain and has an N-terminal receptor domain homologous to carbonic anhydrases. Proc. Natl. Acad. Sci. U.S.A. 89, 7417-7421. doi: 10.1073/pnas.89.16.7417
42. Kuschert, G. S., Coulin, F., Power, C. A., Proudfoot, A. E. I., Hubbard, R. E., Hoogewerf, A. J., et al. (1999). Glycosaminoglycans interact selectively with chemokines and modulate receptor binding and cellular responses. Biochemistry 38, 12959-12968. doi: 10.1021/bi990711d
43. Lambaerts, K., Wilcox-Adelman, S. A., and Zimmermann, P. (2009). The signaling mechanism of Syndecan heparan sulfate proteoglycans. Curr. Opin. Cell Biol. 21, 662-669. doi: 10.1016/j.ceb.2009.05.002
44. Lencz, T., Guha, S., Liu, C., Rosenfeld, J., Mukherjee, S., DeRosse, P., et al. (2013). Genome-wide association study implicates NDST3 in schizophrenia and bipolar disorder. Nat. Commun. 4:2739. doi: 10.1038/ncomms3739
45. Li, D., Feng, G., and He, L. (2009). Case-control study of association between the functional candidate gene ERBB3 and schizophrenia in Caucasian population. Wold J. Biol. Psychiatry 10, 595-598. doi: 10.1080/15622970903304442
46. Li, F., Shi, W., Capurro, M., and Filmus, J. (2011). Glypican-5 stimulates rhabdomyosarcoma cell proliferation by activating Hedgehog signaling. J. Cell Biol. 192, 691-704. doi: 10.1083/jcb.201008087
47. Li, G., Adesnik, H., Li, J., Long, J., Nicoll, R. A., Rubenstein, J. L. R., et al. (2008). Regional distribution of cortical interneurons and development of inhibitory tone are regulated by Cxcl12/Cxcr4 signaling. J. Neurosci. 28, 1085-1098. doi: 10.1523/JNEUROSCI.4602-07.2008
48. Li, H., Yamagata, T., Mori, M., and Momoi, M. Y. (2002). Association of autism in two patients with hereditary multiple exostoses caused by novel deletion mutation of EXT1. J. Hum. Genet. 47, 262-265. doi: 10.1007/s100380200036
49. Li, Y., Laue, K., Temtamy, S., Aglan, M., Kotan, L. D., Yigit, G., et al. (2010). Temtamy preaxial brachydactyly syndrome is caused by loss-of-function mutations in chondroitin synthase 1, a protein target of BMP signaling. Am. J. Hum. Genet. 87, 757-767. doi: 10.1016/j.ajhg.2010.10.003
50. Liu, Z., Li, F., Ruan, K., Zhang, J., Mei, Y., Wu, J., et al. (2014). Structural and functional insights into the human Borjeson-Forssman-Lehmann syndrome-associated protein PHF6. J. Biol. Chem. 289, 10069-10083. doi: 10.1074/jbc.M113.535351
51. Lopez-Bendito, G., Sanchez-Alcaniz, J. A., Borrell, V., Pico, E., Valdeolmillos, V., and Marin, O. (2008). Chemokine signaling controls intracortical migration and final distribution of GABAergic interneurons. J. Neurosci. 28, 1613-1624. doi: 10.1523/JNEUROSCI.4651-07.2008
52. Maeda, N., Fukazawa, N., and Hata, T. (2006). The binding of chondroitin sulfate to pleiotrophin/heparin-binding growth-associated molecule is regulated by chain length and oversulfated structures. J. Biol. Chem. 281, 4894-4902. doi: 10.1074/jbc.M507750200
53. Maeda, N., Hamanaka, H., Oohira, A., and Noda, M. (1995). Purification, characterization and developmental expression of a brain-specific chondroitin sulfate proteoglycan, 6B4 proteoglycan/phosphacan. Neuroscience 67, 23-35. doi: 10.1016/0306-4522(94)00069-H
54. Maeda, N., Hamanaka, H., Shintani, T., Nishiwaki, T., and Noda, M. (1994). Multiple receptor-like protein tyrosine phosphatases in the form of chondroitin sulfate proteoglycan. FEBS Lett. 354, 67-70. doi: 10.1016/0014-5793(94)01093-5
55. Maeda, N., He, J., Yajima, Y., Mikami, T., Sugahara, K., and Yabe, T. (2003). Heterogeneity of the chondroitin sulfate portion of phosphacan/6B4 proteoglycan regulates its binding affinity for pleiotrophin/heparin-binding growth-associated molecule. J. Biol. Chem. 278, 35805-35811. doi: 10.1074/jbc.M305530200
56. Maeda, N., Ichihara-Tanaka, K., Kimura, T., Kadomatsu, K., Muramatsu, T., and Noda, M. (1999). A receptor-like protein-tyrosine phosphatase PTP?/RPTPß binds a heparin-binding growth factor midkine. J. Biol. Chem. 274, 12474-12479. doi: 10.1074/jbc.274.18.12474
57. Maeda, N., Ishii, M., Nishimura, K., and Kamimura, K. (2011). Functions of chondroitin sulfate and heparan sulfate in the developing brain. Neurochem. Res. 36, 1228-1240. doi: 10.1007/s11064-010-0324-y
58. Maeda, N., Matsui, F., and Oohira, A. (1992). A chondroitin sulfate proteoglycan that is developmentally regulated in the cerebellar mossy fiber system. Dev. Biol. 151, 564-574. doi: 10.1016/0012-1606(92)90194-L
59. Maeda, N., Nishiwaki, T., Shintani, T., Hamanaka, H., and Noda, M. (1996). 6B4 proteoglycan/phosphacan, an extracellular variant of receptor-like protein-tyrosine phosphatase?/RPTPß, binds pleiotrophin/heparin-binding growth-associated molecule (HB-GAM). J. Biol. Chem. 271, 21446-21452. doi: 10.1074/jbc.271.35.21446
60. Maeda, N., and Noda, M. (1998). Involvement of receptor-like protein tyrosine phosphatase ?/RPTPß and its ligand pleiotrophin/heparin-binding growth-associated molecule (HB-GAM) in neuronal migration. J. Cell Biol. 142, 203-216. doi: 10.1083/jcb.142.1.203
61. Malfait, F., Kariminejad, A., Damme, T. V., Gauche, C., Syx, D., Merhi-Soussi, F., et al. (2013). Defective initiation of glycosaminoglycan synthesis due to B3GALT6 mutations causes a pleiotropic Ehlers-Danlos-syndrome-like connective tissue disorder. Am. J. Hum. Genet. 92, 935-945. doi: 10.1016/j.ajhg.2013.04.016
62. Margolis, R. U., Lalley, K., Kiang, W. L., Crockett, C., and Margolis, R. K. (1976). Isolation and properties of a soluble chondroitin sulfate proteoglycan from brain. Biochem. Biophys. Res. Commun. 73, 1018-1024. doi: 10.1016/0006-291X(76)90224-2
63. Margolis, R. U., Margolis, R. K., Chang, L. B., and Preti, C. (1975). Glycosaminoglycans of brain during development. Biochemistry 14, 85-88. doi: 10.1021/bi00672a014
64. Marin, O. (2013). Cellular and molecular mechanisms controlling the migration of neocortical interneurons. Eur. J. Neurosci. 38, 2019-2029. doi: 10.1111/ejn.12225
65. Maurel, P., Rauch, U., Flad, M., Margolis, R. K., and Margolis, R. U. (1994). Phosphacan, a chondroitin sulfate proteoglycan of brain that interacts with neurons and neural cell-adhesion molecules, is an extracellular variant of a receptor-type protein tyrosine phosphatase. Proc. Natl. Acad. Sci. U.S.A. 91, 2512-2516. doi: 10.1073/pnas.91.7.2512
66. Mbemba, E., Gluckman, J. C., and Gattegno, L. (2000). Glycan and glycosaminoglycan binding properties of stromal cell-derived factor (SDF)-1a. Glycobiology 10, 21-29. doi: 10.1093/glycob/10.1.21
67. Mei, L., and Nave, K.-A. (2014). Neuregulin-ERBB signaling in the nervous system and neuropsychiatric diseases. Neuron 83, 27-49. doi: 10.1016/j.neuron.2014.06.007
68. Meng, K., Rodriguez-Pena, A., Dimitrov, T., Chen, W., Yamin, M., Noda, M., et al. (2000). Pleiotrophin signals increased tyrosine phosphorylation of ß-catenin through inactivation of the intrinsic catalytic activity of the receptor-type protein tyrosine phosphatase ß/?. Proc. Natl. Acad. Sci. U.S.A. 97, 2603-2608. doi: 10.1073/pnas.020487997
69. Meyer-Puttlitz, B., Junker, E., Margolis, R. U., and Margolis, R. K. (1996). Chondroitin sulfate proteoglycans in the developing central nervous system. II. Immunocytochemical localization of neurocan and phosphacan. J. Comp. Neurol. 366, 44-54.
70. Mikami, T., and Kitagawa, H. (2013). Biosynthesis and function of chondroitin sulfate. Biochim. Biophys. Acta 1830, 4719-4733. doi: 10.1016/j.bbagen.2013.06.006
71. Mitsunaga, C., Mikami, T., Mizumoto, S., Fukuda, J., and Sugahara, K. (2006). Chondroitin sulfate/dermatan sulfate hybrid chains in the development of cerebellum: spatiotemporal regulation of the expression of critical disulfated disaccharides by specific sulfotransferases. J. Biol. Chem. 281, 18942-18952. doi: 10.1074/jbc.M510870200
72. Mizumoto, S., Fongmoon, D., and Sugahara, K. (2013b). Interaction of chondroitin sulfate and dermatan sulfate from various biological sources with heparin-binding growth factors and cytokines. Glycoconj. J. 30, 619-632. doi: 10.1007/s10719-012-9463-5
73. Mizumoto, S., Ikegawa, S., and Sugahara, K. (2013a). Human genetic disorders caused by mutations in genes encoding biosynthetic enzymes for sulfated glycosaminoglycans. J. Biol. Chem. 288, 10953-10961. doi: 10.1074/jbc.R112.437038
74. Mouw, J. K., Ou, G., and Weaver, V. M. (2014). Extracellular matrix assembly: a multiscale deconstruction. Nat. Rev. Mol. Cell Biol. 15, 771-785. doi: 10.1038/nrm3902
75. Muhleisen, T. W., Mattheisen, M., Strohmaier, J., Degenhardt, F., Priebe, L., Schultz, C. C., et al. (2012). Association between schizophrenia and common variation in neurocan (NCAN), a genetic risk factor for bipolar disorder. Schizophr. Res. 138, 69-73. doi: 10.1016/j.schres.2012.03.007
76. Muramatsu, T. (2014). Structure and function of midkine as the basis of its pharmacological effects. Br. J. Pharmacol. 171, 814-826. doi: 10.1111/bph.12353
77. Murphy, K. J., Merry, C. L., Lyon, M., Thompson, J. E., Roberts, I. S., and Gallagher, J. T. (2004). A new model for the domain structure of heparan sulfate based on the novel specificity of K5 lyase. J. Biol. Chem. 279, 27239-27245. doi: 10.1074/jbc.M401774200
78. Nadanaka, S., and Kitagawa, H. (2008). Heparan sulfate biosynthesis and disease. J. Biochem. 144, 7-14. doi: 10.1093/jb/mvn040
79. Nagamine, S., Tamba, M., Ishimine, H., Araki, K., Shiomi, K., Okada, T., et al. (2012). Organ-specific sulfation patterns of heparan sulfate generated by extracellular sulfatases Sulf1 and Sulf2 in mice. J. Biol. Chem. 287, 9579-9590. doi: 10.1074/jbc.M111.290262
80. Nakanishi, K., Tokita, Y., Aono, S., Ida, M., Matsui, F., Higashi, Y., et al. (2010). Neuroglycan C, a brain-specific chondroitin sulfate proteoglycan, interacts with pleiotrophin, a heparin-binding growth factor. Neurochem. Res. 35, 1131-1137. doi: 10.1007/s11064-010-0164-9
81. Nakanishi, S. (1983). Extracellular matrix during laminar pattern formation of neocortex in normal and reeler mutant mice. Dev. Biol. 95, 305-316. doi: 10.1016/0012-1606(83)90031-3
82. Nishimura, K., Ishii, M., Kuraoka, M., Kamimura, K., and Maeda, N. (2010). Opposing functions of chondroitin sulfate and heparan sulfate during early neuronal polarization. Neuroscience 169, 1535-1547. doi: 10.1016/j.neuroscience.2010.06.027
83. Ohtaka-Maruyama, C., Hirai, S., Miwa, A., Heng, J. I., Shitara, H., Ishii, R., et al. (2013). RP58 regulates the multipolar-bipolar transition of newborn neurons in the developing cerebral cortex. Cell Rep. 3, 458-471. doi: 10.1016/j.celrep.2013.01.012
84. Oohira, A., Matsui, F., Watanabe, E., Kushima, Y., and Maeda, N. (1994). Developmentally regulated expression of a brain specific species of chondroitin sulfate proteoglycan, neurocan, identified with a monoclonal antibody 1G2 in the rat cerebrum. Neuroscience 60, 145-157. doi: 10.1016/0306-4522(94)90210-0
85. Pankonin, M. S., Gallagher, J. T., and Loeb, J. A. (2005). Specific structural features of heparan sulfate proteoglycans potentiate neuregulin-1 signaling. J. Biol. Chem. 280, 383-388. doi: 10.1074/jbc.M402645200
86. Peles, E., Schlessinger, J., and Grumet, M. (1998). Multi-ligand interactions with receptor-like protein tyrosine phosphatase ß: implications for intercellular signaling. Trends Biochem. Sci. 23, 121-124. doi: 10.1016/S0968-0004(98)01195-5
87. Perez-Pinera, P., Chang, Y., and Deuel, T. F. (2007). Pleiotrophin, a multifunctional tumor promoter through induction of tumor angiogenesis, remodeling of the tumor microenvironment, and activation of stromal fibroblast. Cell Cycle 6, 2877-2883. doi: 10.4161/cc.6.23.5090
88. Polleux, F., Whitford, K. L., Dijkhuizen, P. A., Vitalis, T., and Ghosh, A. (2002). Control of cortical interneuron migration by neurotrophins and PI3-knase signaling. Development 129, 3147-3160.
89. Polykratis, A., Katsoris, P., Courty, J., and Papadimitriou, E. (2005). Characterization of heparin affin regulatory peptide signaling in human endothelial cells. J. Biol. Chem. 280, 22454-22461. doi: 10.1074/jbc.M414407200
90. Popp, S., Andersen, J. S., Maurel, P., and Margolis, R. U. (2003). Localization of aggrecan and versican in the developing rat central nervous system. Dev. Dyn. 227, 143-149. doi: 10.1002/dvdy.10282
91. Raftery, L. A., and Umulis, D. M. (2012). Regulation of BMP activity and range in Drosophila wing development. Curr. Opin. Cell Biol. 24, 158-165. doi: 10.1016/j.ceb.2011.11.004
92. Rauch, U., Gao, P., Janetzko, A., Flaccus, A., Hilgenberg, L., Tekotte, H., et al. (1991). Isolation and characterization of developmentally regulated chondroitin sulfate and chondroitin/keratin sulfate proteoglycans of brain identified with monoclonal antibodies. J. Biol. Chem. 266, 14785-14801.
93. Rauch, U., Karthikeyan, L., Maurel, P., Margolis, R. U., and Margolis, R. K. (1992). Cloning and primary structure of neurocan, a developmentally regulated, aggregating chondroitin sulfate proteoglycan of brain. J. Biol. Chem. 267, 19536-19547.
94. Raulo, E., Chernousov, M. A., Carey, D. J., Nolo, R., and Rauvala, H. (1994). Isolation of a neuronal cell surface receptor of heparin binding growth-associated molecule (HB-GAM). Identification as N-syndecan (Syndecan-3). J. Biol. Chem. 269, 12999-13004.
95. Reuter, M. S., Musante, L., Hu, H., Diederich, S., Sticht, H., Ekici, A. B., et al. (2014). NDST1 missense mutations in autosomal recessive intellectual disability. Am. J. Med. Genet. A 164A, 2753-2763. doi: 10.1002/ajmg.a.36723
96. Rickard, S. M., Mummery, R. S., Mulloy, B., and Rider, C. C. (2003). The binding of human glial cell line-derived neurotrophic factor to heparin and heparan sulfate: importance of 2-O-sulfate groups and effect on its interaction with its receptor, GFRa1. Glycobiology 13, 419-426. doi: 10.1093/glycob/cwg046
97. Rogers, C. J., Clark, P. M., Tully, S. E., Abrol, R., Garcia, K. C., Goddard, W. A., et al. (2011). Elucidating glycosaminoglycan-protein-protein interactions using carbohydrate microarray and computational approaches. Proc. Natl. Acad. Sci. U.S.A. 108, 9747-9752. doi: 10.1073/pnas.1102962108
98. Rudolph, J., Zimmer, G., Steinecke, A., Barchmann, S., and Bolz, J. (2010). Ephrins guide migrating cortical interneurons in the basal telencephalon. Cell Adh. Migr. 4, 400-408. doi: 10.4161/cam.4.3.11640
99. Schnepp, A., KompLindgen, P., Hulsmann, H., Kroger, S., Paulsson, M., and Hartmann, U. (2005). Mouse testican-2. Expression, glycosylation, and effects on neurite outgrowth. J. Biol. Chem. 280, 11274-11280. doi: 10.1074/jbc.M414276200
100. Schreml, J., Durmaz, B., Cogulu, O., Keupp, K., Beleggia, F., Pohl, E., et al. (2014). The missing "link": an autosomal recessive short stature syndrome caused by a hypofunctional XYLT1 mutation. Hum. Genet. 133, 29-39. doi: 10.1007/s00439-013-1351-y
101. Schultz, C. C., Muhleisen, T. W., Nenadic, I., Koch, K., Wagner, G., Schachtzabel, C., et al. (2014). Common variation in NCAN, a risk factor for bipolar disorder and schizophrenia, influences local cortical folding in schizophrenia. Psychol. Med. 44, 811-820. doi: 10.1017/S0033291713001414
102. Shi, J., Potash, J. B., Knowles, J. A., Weissman, M. M., Coryell, W., Scheftner, W. A., et al. (2011). Genome-wide association study of recurrent early-onset major depressive disorder. Mol. Psychiatry 16, 193-201. doi: 10.1038/mp.2009.124
103. Shipp, E. L., and Hsieh-Wilson, L. C. (2007). Profiling the sulfation specificities of glycosaminoglycan interactions with growth factors and chemotactic proteins using microarrays. Chem. Biol. 14, 195-208. doi: 10.1016/j.chembiol.2006.12.009
104. Silver, D. J., and Silver, J. (2014). Contribution of chondroitin sulfate proteoglycans to neurodevelopment, injury, and cancer. Curr. Opin. Neurobiol. 27, 171-178. doi: 10.1016/j.conb.2014.03.016
105. So, H. C., Fong, P. Y., Chen, R. Y., Hui, T. C., Ng, M. Y., Cherny, S. S., et al. (2010). Identification of neuroglycan C and interacting partners as potential susceptibility genes for schizophrenia in a Southern Chinese population. Am. J. Med. Genet. B Neuropsychiatr. Genet. 153B, 103-113. doi: 10.1002/ajmg.b.30961
106. Soleman, S., Filippov, M. A., Dityatev, A., and Fawcett, J. W. (2013). Targeting the neural extracellular matrix in neurological disorders. Neuroscience 253, 194-213. doi: 10.1016/j.neuroscience.2013.08.050
107. Steinecke, A., Gampe, C., Zimmer, G., Rudolph, J., and Bolz, J. (2014). EphA/ephrin A reverse signaling promotes the migration of cortical interneurons from the medial ganglionic eminence. Development 141, 460-471. doi: 10.1242/dev.101691
108. Stolp, H., Neuhaus, A., Sundramoorthi, R., and Molnar, Z. (2012). The long and the short of it: gene and environment interactions during early cortical development and consequences for long-term neurological diseases. Front. Psychiatry 3:50. doi: 10.3389/fpsyt.2012.00050
109. Sulkava, S., Ollila, H. M., Ahola, K., Partonen, T., Viitasalo, K., Kettunen, J., et al. (2013). Genome-wide scan of job-related exhaustion with three replication studies implicate a susceptibility variant at the UST gene locus. Hum. Mol. Genet. 22, 3363-3372. doi: 10.1093/hmg/ddt185
110. Svensson, G., Awad, W., Hakansson, M., Mani, K., and Logan, D. T. (2012). Crystal structure of N-glycosylated human glypican-1 core protein. J. Biol. Chem. 287, 14040-14051. doi: 10.1074/jbc.M111.322487
111. Takahashi, N., Sakurai, T., Bozdagi-Gunal, O., Dorr, N. P., Moy, J., Krug, L., et al. (2011). Increased expression of receptor phosphotyrosine phosphatase-ß/? is associated with molecular, cellular, behavioral and cognitive schizophrenia phenotypes. Transl. Psychiatry 1:e8. doi: 10.1038/tp.2011.8
112. Tenorio, J., Arias, P., Martinez-Glez, V., Santos, F., Garcia-Minaur, S., Nevado, J., et al. (2014). Simpson-Golabi-Behmel syndrome types I and II. Orphanet J. Rare Dis. 9, 138. doi: 10.1186/s13023-014-0138-0
113. Theocharidis, U., Long, K., ffrench-Constant, C., and Faissner, A. (2014). Regulation of the neural stem cell compartment by extracellular matrix constituents. Prog. Brain Res. 214, 13-28. doi: 10.1016/B978-0-444-63486-3.00001-3
114. Uher, R., Perroud, N., Ng, M. Y., Hauser, J., Henigsberg, N., Maier, W., et al. (2010). Genome-wide pharmacogenetics of antidepressant response in the GENDEP project. Am. J. Psychiatry 167, 555-564. doi: 10.1176/appi.ajp.2009.09070932
115. Wang, Q., Yang, L., Alexander, C., and Temple, S. (2012). The niche factor sydecan-1 regulates the maintenance and proliferation of neural progenitor cells during mammalian cortical development. PLoS ONE 7:e42883. doi: 10.1371/journal.pone.0042883
116. Wang, S., Ai, X., Freeman, S. D., Pownall, M. E., Lu, Q., Kessler, D. S., et al. (2004). QSulf1, heparan sulfate 6-O-endosulfatase, inhibits fibroblast growth factor signaling in mesoderm induction and angiogenesis. Proc. Natl. Acad. Sci. U.S.A. 101, 4833-4838. doi: 10.1073/pnas.0401028101
117. Watanabe, E., Maeda, N., Matsui, F., Kushima, Y., Noda, M., and Oohira, A. (1995). Neuroglycan C, a novel membrane-spanning chondroitin sulfate proteoglycan that is restricted to the brain. J. Biol. Chem. 270, 26876-26882. doi: 10.1074/jbc.270.45.26876
118. Wu, Y., Belenkaya, T. Y., and Lin, X. (2010). Dual roles of Drosophila glypican Dally-like in Wingless/Wnt signaling and distribution. Methods Enzymol. 480, 33-50. doi: 10.1016/S0076-6879(10)80002-3
119. 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. doi: 10.1093/glycob/cwi090
120. Zhang, C., Mejia, L. A., Huang, J., Valnegri, P., Bennett, E. J., Anckar, J., et al. (2013). The X-linked intellectual disability protein PHF6 associates with the PAF1 complex and regulates neuronal migration in the mammalian brain. Neuron 78, 986-993. doi: 10.1016/j.neuron.2013.04.021
121. Zhu, Y., Li, H., Zhou, L., Wu, J. Y., and Rao, Y. (1999). Cellular and molecular guidance of GABAergic neuronal migration from an extracortical origin to the neocortex. Neuron 23, 473-485. doi: 10.1016/S0896-6273(00)80801-6
122. Zimmer, G., Schanuel, S. M., Burger, S., Weth, F., Steinecke, A., Bolz, J., et al. (2010). Chondroitin sulfate acts in concert with semaphoring 3A to guide tangential migration of cortical interneurons in the ventral telencephalon. Cereb. Cortex 20, 2411-2422. doi: 10.1093/cercor/bhp309
123. Zou, P., Zou, K., Muramatsu, H., Ichihara-Tanaka, K., Habuchi, O., Ohtake, S., et al. (2003). Glycosaminoglycan structures required for strong binding to midkine, a heparin-binding growth factor. Glycobiology 13, 35-42. doi: 10.1093/glycob/cwg001