A Targeted Glycan-Related Gene Screen Reveals Heparan Sulfate Proteoglycan Sulfation Regulates WNT and BMP Trans-Synaptic Signaling

PLoS Genetics

Volumn 8, Issue 11, 2012, Pages

  Dani, Neil ^a   Nahm, Minyeop ^b   Lee, Seungbok ^b   Broadie, Kendal ^a  

^a VANDERBILT UNIVERSITY   (United States)

^b Seoul National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; DALLY LIKE PROTEIN; GLUTAMATE RECEPTOR; GLUTAMIC ACID; HEPARAN SULFATE 6 O SULFOTRANSFERASE; PROTEOGLYCAN; PROTEOHEPARAN SULFATE; SULFATASE; SULFOTRANSFERASE; SYNDECAN; UNCLASSIFIED DRUG; WNT PROTEIN;

AMINO ACID SYNTHESIS; ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL MATURATION; CONTROLLED STUDY; FEMALE; GENE SILENCING; GENETIC CORRELATION; GENETIC SCREENING; INTRACELLULAR SIGNALING; NEUROMODULATION; NONHUMAN; NUCLEAR IMPORT; NULL ALLELE; POSTSYNAPTIC POTENTIAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RNA INTERFERENCE; SULFATION; SYNAPTIC MEMBRANE; SYNAPTIC TRANSMISSION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BONE MORPHOGENETIC PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETIC THERAPY; HEPARITIN SULFATE; POLYSACCHARIDES; PROTEOGLYCANS; SIGNAL TRANSDUCTION; SULFATASES; SULFOTRANSFERASES; SYNAPSES; SYNAPTIC TRANSMISSION; WNT SIGNALING PATHWAY;

EID: 84870690924     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003031     Document Type: Article

References (97)

1. Iozzo RV, (1998) Matrix proteoglycans: From molecular design to cellular function. Annual Review of Biochemistry 67: 609-652.
2. Varki A, (2011) Evolutionary Forces Shaping the Golgi Glycosylation Machinery: Why Cell Surface Glycans Are Universal to Living Cells. Cold Spring Harbor Perspectives in Biology 3: a005462.
3. Kleene R, Schachner M, (2004) Glycans and neural cell interactions. Nature Reviews Neuroscience 5: 195-208.
4. Dityatev A, Schachner M, (2006) The extracellular matrix and synapses. Cell and Tissue Research 326: 647-654.
5. Varki A, Cummings RD, Esko JD, Freeze HH, Stanley P, et al. (2009) Essentials of glycobiology.
6. Hagen KGT, Zhang LP, Tian E, Zhang Y, (2009) Glycobiology on the fly: Developmental and mechanistic insights from Drosophila. Glycobiology 19: 102-111.
7. Barros CS, Franco SJ, Mueller U, (2011) Extracellular Matrix: Functions in the Nervous System. Cold Spring Harbor Perspectives in Biology 3.
8. Vautrin J, (2010) The synaptomatrix: A solid though dynamic contact disconnecting transmissions from exocytotic events. Neurochemistry International 57: 85-96.
9. Dani N, Broadie K, (2012) Glycosylated synaptomatrix regulation of trans-synaptic signaling. Developmental Neurobiology 72: 2-21.
10. Rupp F, Payan DG, Magillsolc C, Cowan DM, Scheller RH, (1991) Structure and expression of rat agrin. Neuron 6: 811-823.
11. Tsim KWK, Ruegg MA, Escher G, Kroger S, McMahan UJ, (1992) cDNA that encodes active agrin. Neuron 8: 677-689.
12. Tsen G, Halfter W, Kroger S, Cole GJ, (1995) Agrin is a heparan-sulfate proteoglycan. Journal of Biological Chemistry 270: 3392-3399.
13. McDonnell KMW, Grow WA, (2004) Reduced glycosaminoglycan sulfation diminishes the agrin signal transduction pathway. Developmental Neuroscience 26: 1-10.
14. Parkhomovskiy N, Kammesheidt A, Martin PT, (2000) N-acetyllactosamine and the CT carbohydrate antigen mediate agrin-dependent activation of MuSK and acetylcholine receptor clustering in skeletal muscle. Molecular and Cellular Neuroscience 15: 380-397.
15. Rohrbough J, Rushton E, Woodruff E, Fergestad T, Vigneswaran K, et al. (2007) Presynaptic establishment of the synaptic cleft extracellular matrix is required for post-synaptic differentiation. Genes & Development 21: 2607-2628.
16. Rushton E, Rohrbough J, Broadie K, (2009) Presynaptic Secretion of Mind-the-Gap Organizes the Synaptic Extracellular Matrix-Integrin Interface and Postsynaptic Environments. Developmental Dynamics 238: 554-571.
17. Rohrbough J, Broadie K, (2010) Anterograde Jelly belly ligand to Alk receptor signaling at developing synapses is regulated by Mind the gap. Development 137: 3523-3533.
18. Rushton E, Rohrbough J, Deutsch K, Broadie K, (2012) Structure-function analysis of endogenous lectin mind-the-gap in synaptogenesis. Developmental Neurobiology 72: 1161-1179.
19. Carey DJ, (1997) Syndecans: Multifunctional cell-surface co-receptors. Biochemical Journal 327: 1-16.
20. Dejima K, Kanai MI, Akiyama T, Levings DC, Nakato H, (2011) Novel Contact-dependent Bone Morphogenetic Protein (BMP) Signaling Mediated by Heparan Sulfate Proteoglycans. Journal of Biological Chemistry 286: 17103-17111.
21. Yan D, Lin X, (2009) Shaping Morphogen Gradients by Proteoglycans. Cold Spring Harbor Perspectives in Biology 1: a002493.
22. Kleinschmit A, Koyama T, Dejima K, Hayashi Y, Kamimura K, et al. (2010) Drosophila heparan sulfate 6-O endosulfatase regualtes Wingless morphogen gradient formation. Developmental biology 345: 204-214.
23. Packard M, Koo ES, Gorczyca M, Sharpe J, Cumberledge S, et al. (2002) The drosophila wnt, wingless, provides an essential signal for pre- and postsynaptic differentiation. Cell 111: 319-330.
24. Korkut C, Budnik V, (2009) WNTs tune up the neuromuscular junction. Nature Reviews Neuroscience 10: 627-634.
25. McCabe BD, Marques G, Haghighi AP, Fetter RD, Crotty ML, et al. (2003) The BMP homolog Gbb provides a retrograde signal that regulates synaptic growth at the Drosophila neuromuscular junction. Neuron 39: 241-254.
26. Keshishian H, Kim YS, (2004) Orchestrating development and function: retrograde BMP signaling in the Drosophila nervous system. Trends in Neurosciences 27: 143-147.
27. Holt CE, Dickson BJ, (2005) Sugar codes for axons? Neuron 46: 169-172.
28. Matani P, Sharrow M, Tiemeyer M, (2007) Ligand, modulatory, and co-receptor functions of neural glycans. Frontiers in Bioscience 12: 3852-3879.
29. Yamaguchi Y, (2002) Glycobiology of the synapse: the role of glycans in the formation, maturation, and modulation of synapses. Biochimica Et Biophysica Acta-General Subjects 1573: 369-376.
30. Martin PT, (2002) Glycobiology of the synapse. Glycobiology 12: 1R-7R.
31. Martin PT, (2003) Glycobiology of the neuromuscular junction. Journal of Neurocytology 32: 915.
32. Keshishian H, Broadie K, Chiba A, Bate M, (1996) The Drosophila neuromuscular junction: A model system for studying synaptic development and function. Annual Review of Neuroscience 19: 545-575.
33. Gramates LS, Budnik V, (1999) Assembly and maturation of the Drosophila larval neuromuscular junction. Neuromuscular Junctions in Drosophila 43: 93-+.
34. Ruiz-Canada C, Budnik V, (2006) Introduction on the use of the Drosophila embryonic/larval neuromuscular junction as a model system to study synapse development and function, and a brief summary of pathfinding and target recognition. Fly Neuromuscular Junction: Structure and Function, Second Edition 75: 1-31.
35. Dietzl G, Chen D, Schnorrer F, Su KC, Barinova Y, et al. (2007) A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448: 151-U151.
36. Wodarz A, Hinz U, Engelbert M, Knust E, (1995) Expression of crumbs confers apical character on plasma-membrane domains of ectodermal epithelia of Drosophila. Cell 82: 67-76.
37. Kanehisa M, Goto S, (2000) KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Research 28: 27-30.
38. Hoffmann R, Valencia A, (2004) A gene network for navigating the literature. Nature Genetics 36: 664-664.
39. Tweedie S, Ashburner M, Falls K, Leyland P, McQuilton P, et al. (2009) FlyBase: enhancing Drosophila Gene Ontology annotations. Nucleic Acids Research 37: D555-D559.
40. Gatto CL, Broadie K, (2008) Temporal requirements of the fragile X mental retardation protein in the regulation of synaptic structure. Development 135: 2637-2648.
41. Beumer KJ, Rohrbough J, Prokop A, Broadie K, (1999) A role for PS integrins in morphological growth and synaptic function at the postembryonic neuromuscular junction of Drosophila. Development 126: 5833-5846.
42. You J, Belenkaya T, Lin X, (2011) Sulfated Is a Negative Feedback Regulator of Wingless in Drosophila. Developmental Dynamics 240: 640-648.
43. Kamimura K, Fujise M, Villa F, Izumi S, Habuchi H, et al. (2001) Drosophila heparan sulfate 6-O-sulfotransferase (dHS6ST) gene- Structure, expression, and function in the formation of the tracheal system. Journal of Biological Chemistry 276: 17014-17021.
44. Ai XB, Do AT, Lozynska O, Kusche-Gullberg M, Lindahl U, et al. (2003) QSulf1 remodels the 6-O sulfation states of cell surface heparan sulfate proteoglycans to promote Wnt signaling. Journal of Cell Biology 162: 341-351.
45. Johnson KG, Tenney AP, Ghose A, Duckworth AM, Higashi ME, et al. (2006) The HSPGs syndecan and dallylike bind the receptor phosphatase LAR and exert distinct effects on synaptic development. Neuron 49: 517-531.
46. Lin XH, Perrimon N, (2000) Role of heparan sulfate proteoglycans in cell-cell signaling in Drosophila. Matrix Biology 19: 303-307.
47. Hacker U, Nybakken K, Perrimon N, (2005) Heparan sulphate proteoglycans: The sweet side of development. Nature Reviews Molecular Cell Biology 6: 530-541.
48. Yan D, Wu Y, Feng Y, Lin S-C, Lin X, (2009) The Core Protein of Glypican Daily-Like Determines Its Biphasic Activity in Wingless Morphogen Signaling. Developmental Cell 17: 470-481.
49. Salinas PC, (2003) Synaptogenesis: Wnt and TGF-beta take centre stage. Current Biology 13: R60-R62.
50. Marques G, (2005) Morphogens and synaptogenesis in Drosophila. Journal of Neurobiology 64: 417-434.
51. Packard M, Mathew D, Budnik V, (2003) Wnts and TGF beta in synaptogenesis: Old friends signalling at new places. Nature Reviews Neuroscience 4: 113-120.
52. Rawson JM, Lee M, Kennedy EL, Selleck SB, (2003) Drosophila neuromuscular synapse assembly and function require the TGF-beta type I receptor saxophone and the transcription factor mad. Journal of Neurobiology 55: 134-150.
53. Cox M, Nelson D (2004) Lehninger, Principles of Biochemistry. 1100.
54. Shimokawa K, Kimura-Yoshida C, Nagai N, Mukai K, Matsubara K, et al. (2011) Cell Surface Heparan Sulfate Chains Regulate Local Reception of FGF Signaling in the Mouse Embryo. Developmental Cell 21: 257-272.
55. Sen A, Yokokura T, Kankel MW, Dimlich DN, Manent J, et al. (2011) Modeling spinal muscular atrophy in Drosophila links Smn to FGF signaling. Journal of Cell Biology 192: 481-495.
56. Shishido E, Ono N, Kojima T, Saigo K, (1997) Requirements of DFR1/heartless, a mesoderm-specific Drosophila FGF-receptor, for the formation of heart, visceral and somatic muscles, and ensheathing of longitudinal axon tracts in CNS. Development 124: 2119-2128.
57. Mathew D, Ataman B, Chen JY, Zhang YL, Cumberledge S, et al. (2005) Wingless signaling at synapses is through cleavage and nuclear import of receptor DFrizzled2. Science 310: 1344-1347.
58. Kim NMG, (2010) Identification of downstream targets of the Bone Morphogenetic Protein pathway in the Drosophila nervous system. Developmental Dynamics 239: 2413-2425.
59. Mosca TJ, Schwarz TL, (2010) The nuclear import of Frizzled2-C by Importins-beta 11 and alpha 2 promotes postsynaptic development. Nature Neuroscience 13: 935-U950.
60. Persson U, Izumi H, Souchelnytskyi S, Itoh S, Grimsby S, et al. (1998) The L45 loop in type I receptors for TGF-beta family members is a critical determinant in specifying Smad isoform activation. Febs Letters 434: 83-87.
61. Nahm M, Long AA, Paik SK, Kim S, Bae YC, et al. (2010) The Cdc42-selective GAP Rich regulates postsynaptic development and retrograde BMP transsynaptic signaling. Journal of Cell Biology 191: 661-675.
62. Higashi-Kovtun ME, Mosca TJ, Dickman DK, Meinertzhagen IA, Schwarz TL, (2010) Importin-beta 11 Regulates Synaptic Phosphorylated Mothers Against Decapentaplegic, and Thereby Influences Synaptic Development and Function at the Drosophila Neuromuscular Junction. Journal of Neuroscience 30: 5253-5268.
63. Wagh DA, Rasse TM, Asan E, Hofbauer A, Schwenkert I, et al. (2006) Bruchpilot, a protein with homology to ELKS/CAST, is required for structural integrity and function of synaptic active zones in Drosophila (vol 49, pg 833, 2006). Neuron 51: 275-275.
64. Featherstone DE, Rushton E, Rohrbough J, Liebl F, Karr J, et al. (2005) An essential Drosophila glutamate receptor subunit that functions in both central neuropil and neuromuscular junction. Journal of Neuroscience 25: 3199-3208.
65. Inlow JK, Restifo LL, (2004) Molecular and comparative genetics of mental retardation. Genetics 166: 835-881.
66. Muntoni F, Torelli S, Brockington M, (2008) Muscular dystrophies due to glycosylation defects. Neurotherapeutics 5: 627-632.
67. Schachter H, Freeze HH, (2009) Glycosylation diseases: Quo vadis? Biochimica Et Biophysica Acta-Molecular Basis of Disease 1792: 925-930.
68. Belmonte MK, Allen G, Beckel-Mitchener A, Boulanger LM, Carper RA, et al. (2004) Autism and abnormal development of brain connectivity. Journal of Neuroscience 24: 9228-9231.
69. Gatto CL, Broadie K, (2011) Drosophila modeling of heritable neurodevelopmental disorders. Current Opinion in Neurobiology 21 (6) (): 834-41.
70. Zhang LP, Zhang Y, Ten Hagen KG, (2008) A Mucin-type O-Glycosyltransferase Modulates Cell Adhesion during Drosophila Development. Journal of Biological Chemistry 283: 34076-34086.
71. Zhang LP, Tran DT, Ten Hagen KG, (2010) An O-Glycosyltransferase Promotes Cell Adhesion during Development by Influencing Secretion of an Extracellular Matrix Integrin Ligand. Journal of Biological Chemistry 285: 19491-19501.
72. Rohrbough J, Grotewiel MS, Davis RL, Broadie K, (2000) Integrin-mediated regulation of synaptic morphology, transmission, and plasticity. Journal of Neuroscience 20: 6868-6878.
73. Beumer K, Matthies HJG, Bradshaw A, Broadie K, (2002) Integrins regulate DLG/FAS2 via a CaM kinase II-dependent pathway to mediate synapse elaboration and stabilization during postembryonic development. Development 129: 3381-3391.
74. Prokopenko SN, He YC, Lu Y, Bellen HJ, (2000) Mutations affecting the development of the peripheral nervous system in drosophila: A molecular screen for novel proteins. Genetics 156: 1691-1715.
75. Dhoot GK, Gustafsson MK, Ai XB, Sun WT, Standiford DM, et al. (2001) Regulation of Wnt signaling and embryo patterning by an extracellular sulfatase. Science 293: 1663-1666.
76. Morin X, Daneman R, Zavortink M, Chia W, (2001) A protein trap strategy to detect GFP-tagged proteins expressed from their endogenous loci in Drosophila. Proceedings of the National Academy of Sciences of the United States of America 98: 15050-15055.
77. Lai J-P, Sandhu DS, Yu C, Han T, Moser CD, et al. (2008) Sulfatase 2 up-regulates glypican 3, promotes fibroblast growth factor signaling, and decreases survival in hepatocellular carcinoma. Hepatology 47: 1211-1222.
78. Han C, Yan D, Belenkaya TY, Lin XJ, (2005) Drosophila glypicans Dally and Dally-like shape the extracellular Wingless morphogen gradient in the wing disc. Development 132: 667-679.
79. Pfeiffer S, Ricardo S, Manneville JB, Alexandre C, Vincent JP, (2002) Producing cells retain and recycle wingless in Drosophila embryos. Current Biology 12: 957-962.
80. Gorsi B, Stringer SE, (2007) Tinkering with heparan sulfate sulfation to steer development. Trends in Cell Biology 17: 173-177.
81. Otsuki S, Hanson SR, Miyaki S, Grogan SP, Kinoshita M, et al. (2010) Extracellular sulfatases support cartilage homeostasis by regulating BMP and FGF signaling pathways. Proceedings of the National Academy of Sciences of the United States of America 107: 10202-10207.
82. Baeg GH, Perrimon N, (2000) Functional binding of secreted molecules to heparan sulfate proteoglycans in Drosophila. Current Opinion in Cell Biology 12: 575-580.
83. Baeg GH, Lin XH, Khare N, Baumgartner S, Perrimon N, (2001) Heparan sulfate proteoglycans are critical for the organization of the extracellular distribution of Wingless. Development 128: 87-94.
84. Mohammadi M, Olsen SK, Goetz R, (2005) A protein canyon in the FGF-FGF receptor dimer selects from an a la carte menu of heparan sulfate motifs. Current Opinion in Structural Biology 15: 506-516.
85. Ataman B, Ashley J, Gorczyca D, Gorczyca M, Mathew D, et al. (2006) Nuclear trafficking of Drosophila Frizzled-2 during synapse development requires the PDZ protein dGRIP. Proceedings of the National Academy of Sciences of the United States of America 103: 7841-7846.
86. Marques G, Bao H, Haerry TE, Shimell MJ, Duchek P, et al. (2002) The Drosophila BMP type II receptor wishful thinking regulates neuromuscular synapse morphology and function. Neuron 33: 529-543.
87. Wharton KA, Cook JM, Torres-Schumann S, de Castro K, Borod E, et al. (1999) Genetic analysis of the bone morphogenetic protein-related gene, gbb, identifies multiple requirements during Drosophila development. Genetics 152: 629-640.
88. McCabe BD, Hom S, Aberle H, Fetter RD, Marques G, et al. (2004) Highwire regulates presynaptic BMP signaling essential for synaptic growth. Neuron 41: 891-905.
89. Aberle H, Haghighi AP, Fetter RD, McCabe BD, Magalhaes TR, et al. (2002) wishful thinking encodes a BMP type II receptor that regulates synaptic growth in Drosophila. Neuron 33: 545-558.
90. Lin DM, Goodman CS, (1994) Ectopic and increased expression of Fasciclin-II alters motoneuron growth cone guidance. Neuron 13: 507-523.
91. Brand AH, Perrimon N, (1993) Targeted gene-expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415.
92. Sepp KJ, Schulte J, Auld VJ, (2001) Peripheral glia direct axon guidance across the CNS/PNS transition zone. Developmental Biology 238: 47-63.
93. Kamimura K, Koyama T, Habuchi H, Ueda R, Masu M, et al. (2006) Specific and flexible roles of heparan sulfate modifications in Drosophila FGF signaling. Journal of Cell Biology 174: 773-778.
94. Marie B, Pym E, Bergquist S, Davis GW, (2010) Synaptic Homeostasis Is Consolidated by the Cell Fate Gene gooseberry, a Drosophila pax3/7 Homolog. Journal of Neuroscience 30: 8071-8082.
95. Goold CP, Davis GW, (2007) The BMP ligand Gbb gates the expression of synaptic horneostasis independent of synaptic growth control. Neuron 56: 109-123.
96. Spring J, Painesaunders SE, Hynes RO, Bernfield M, (1994) Drosophila Syndecan- conservation of a cell-surface heparan-sulfate proteoglycan. Proceedings of the National Academy of Sciences of the United States of America 91: 3334-3338.
97. Friedrich MVK, Schneider M, Timpl R, Baumgartner S, (2000) Perlecan domain V of Drosophila melanogaster- Sequence, recombinant analysis and tissue expression. European Journal of Biochemistry 267: 3149-3159.