The molecular diversity of glycosaminoglycans shapes animal development

Annual Review of Cell and Developmental Biology

Volumn 22, Issue , 2006, Pages 375-407

  Bülow, Hannes E ^a   Hobert, Oliver ^b  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b NewYork Presbyterian Hospital   (United States)

Author keywords

Axon patterning; Chondroitin sulfate; Dermatan sulfate; Heparan sulfate; Keratan sulfate; Proteoglycans

Indexed keywords

CHONDROITIN SULFATE; DERMATAN SULFATE; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR RECEPTOR; GLYCOSAMINOGLYCAN; KERATAN SULFATE; PROTEOGLYCAN;

BIOSYNTHESIS; DEVELOPMENT; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; NERVE FIBER; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; GLYCOSAMINOGLYCANS; GROWTH AND DEVELOPMENT; HUMANS; POLYMERS; PROTEOGLYCANS;

ANIMALIA;

EID: 33751187897     PISSN: 10810706     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.cellbio.22.010605.093433     Document Type: Review

References (164)

1. Ackley BD, Crew JR, Elamaa H, Pihlajaniemi T, Kuo CJ, Kramer JM. 2001. The NC1/endostatin domain of Caenorhabditis elegans type XVIII collagen affects cell migration and axon guidance. J. Cell. Biol. 152:1219-32
2. Ahn J, Lüdecke HJ, Lindow S, Horton WA, Lee B, et al. 1995. Cloning of the putative tumor suppressor gene for hereditary multiple exostoses (EXT1). Nat. Genet. 11:137-43
3. Akama TO, Nishida K, Nakayama J, Watanabe H, Ozaki K, et al. 2000. Macular corneal dystrophy type I and type II are caused by distinct mutations in a new sulphotransferase gene. Nat. Genet. 26:237-41
4. Alexander CM, Reichsman F, Hinkes MT, Lincecum J, Becker KA, et al. 2000. Syndecan-1 is required for Wnt-1-induced mammary tumorigenesis in mice. Nat. Genet. 25:329-32
5. Allen BL, Rapraeger AC. 2003. Spatial and temporal expression of heparan sulfate in mouse development regulates FGF and FGF receptor assembly. J. Cell Biol. 163:637-48
6. Arikawa-Hirasawa E, Rossi SG, Rotundo RL, Yamada Y. 2002. Absence of acetylcholinesterase at the neuromuscular junctions of perlecan-null mice. Nat. Neurosci. 5:119-23
7. Arikawa-Hirasawa E, Watanabe H, Takami H, Hassell JR, Yamada Y. 1999. Perlecan is essential for cartilage and cephalic development. Nat. Genet. 23:354-58
8. Baeg GH, Lin X, 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
9. Bech-Hansen NT, Naylor MJ, Maybaum TA, Sparkes RL, Koop B, et al. 2000. Mutations in NYX, encoding the leucine-rich proteoglycan nyctalopin, cause X-linked complete congenital stationary night blindness. Nat. Genet. 26:319-23
10. Bellaiche Y, The I, Perrimon N. 1998. Tout-velu is a Drosophila homologue of the putative tumor suppressor EXT-1 and is needed for Hh diffusion. Nature 394:85-88
11. Bernfield M, Gotte M, Park PW, Reizes O, Fitzgerald ML, et al. 1999. Functions of cell surface heparan sulfate proteoglycans. Annu. Rev. Biochem. 68:729-77
12. Bezakova G, Ruegg MA. 2003. New insights into the roles of agrin. Nat. Rev. Mol. Cell Biol. 4:295-308
13. Bink RJ, Habuchi H, Lele Z, Dolk E, Joore J, et al. 2003. Heparan sulfate 6-O-sulfotransferase is essential for muscle development in zebrafish. J. Biol. Chem. 278:31118-27
14. Brakebusch C, Seidenbecher CI, Asztely F, Rauch U, Matthies H, et al. 2002. Brevican-deficient mice display impaired hippocampal CA1 long-term potentiation but show no obvious deficits in learning and memory. Mol. Cell Biol. 22:7417-27
15. Bullock SL, Fletcher JM, Beddington RS, Wilson VA. 1998. Renal agenesis in mice homozygous for a gene trap mutation in the gene encoding heparan sulfate 2-sulfotransferase. Genes Dev. 12:1894-906
16. Bülow HE, Berry KL, Topper LH, Peles E, Hobert O. 2002. Heparan sulfate proteoglycan-dependent induction of axon branching and axon misrouting by the Kallmann syndrome gene kal-1. Proc. Natl. Acad. Sci. USA 99:6346-51
17. Bülow HE, Hobert O. 2004. Differential sulfations and epimerization define heparan sulfate specificity in nervous system development. Neuron 41:723-36
18. Cano-Gauci DF, Song HH, Yang H, McKerlie C, Choo B, et al. 1999. Glypican-3-deficient mice exhibit developmental overgrowth and some of the abnormalities typical of Simpson-Golabi-Behmel syndrome. J. Cell Biol. 146:255-64
19. Chakravarti S. 2003. Functions of lumican and fibromodulin: lessons from knockout mice. Glycoconj. J. 19:287-93
20. Chakravarti S, Magnuson T, Lass JH, Jepsen KJ, LaMantia C, Carroll H. 1998. Lumican regulates collagen fibril assembly: skin fragility and corneal opacity in the absence of lumican. J. Cell Biol. 141:1277-86
21. Chen E, Stringer SE, Rusch MA, Selleck SB, Ekker SC. 2005. A unique role for 6-O sulfation modification in zebrafish vascular development. Dev. Biol. 284:364-76
22. Chung KY, Taylor JS, Shum DK, Chan SO. 2000. Axon routing at the optic chiasm after enzymatic removal of chondroitin sulfate in mouse embryos. Development 127:2673-83
23. Cifuentes-Diaz C, Velasco E, Meunier FA, Goudou D, Belkadi L, et al. 1998. The peripheral nerve and the neuromuscular junction are affected in the tenascin-C-deficient mouse. Cell Mol. Biol. 44:357-79
24. Costell M, Gustafsson E, Aszodi A, Morgelin M, Bloch W, et al. 1999. Perlecan maintains the integrity of cartilage and some basement membranes. J. Cell Biol. 147:1109-22
25. Danielson KG, Baribault H, Holmes DF, Graham H, Kadler KE, Iozzo RV. 1997. Targeted disruption of decorin leads to abnormal collagen fibril morphology and skin fragility. J. Cell Biol. 136:729-43
26. Dennissen MA, Jenniskens GJ, Pieffers M, Versteeg EM, Petitou M, et al. 2002. Large, tissue-regulated domain diversity of heparan sulfates demonstrated by phage display antibodies. J. Biol. Chem. 277:10982-86
27. Dhoot GK, Gustafsson MK, Ai X, Sun W, Standiford DM, Emerson CPJ. 2001. Regulation of Wnt signaling and embryo patterning by an extracellular sulfatase. Science 293:1663-66
28. Echtermeyer F, Streit M, Wilcox-Adelman S, Saoncella S, Denhez F, et al. 2001. Delayed wound repair and impaired angiogenesis in mice lacking syndecan-4. J. Clin. Invest. 107:R9-14
29. Esko JD, Lindahl U. 2001. Molecular diversity of heparan sulfate. J. Clin. Invest. 108:169-73
30. Esko JD, Selleck SB. 2002. Order out of chaos: assembly of ligand binding sites in heparan sulfate. Annu. Rev. Biochem. 71:435-71
31. Esko JD, Zhang L. 1996. Influence of core protein sequence on glycosaminoglycan assembly. Curr. Opin. Struct. Biol. 6:663-70
32. Fan G, Xiao L, Cheng L, Wang X, Sun B, Hu G. 2000. Targeted disruption of NDST-1 gene leads to pulmonary hypoplasia and neonatal respiratory distress in mice. FEBS Lett. 467:7-11
33. Feyzi E, Saldeen T, Larsson E, Lindahl U, Salmivirta M. 1998. Age-dependent modulation of heparan sulfate structure and function. J. Biol. Chem. 273:13395-98
34. Forsberg E, Hirsch E, Frohlich L, Meyer M, Ekblom P, et al. 1996. Skin wounds and severed nerves heal normally in mice lacking tenascin-C. Proc. Natl. Acad. Sci. USA 93:6594-99
35. Forsberg E, Pejler G, Ringvall M, Lunderius C, Tbmasini-Johansson B, et al. 1999. Abnormal mast cells in mice deficient in a heparin-synthesizing enzyme. Nature 400:773-76
36. Fukai N, Eklund L, Marneros AG, Oh SP, Keene DR, et al. 2002. Lack of collagen XVIII/endostatin results in eye abnormalities. EMBO J. 21:1535-44
37. Funderburgh JL. 2000. Keratan sulfate: structure, biosynthesis, and function. Glycobiology 10:951-58
38. Funderburgh JL. 2002. Keratan sulfate biosynthesis. IUBMB Life 54:187-94
39. Gautam M, Noakes PG, Moscoso L, Rupp F, Scheller RH, et al. 1996. Defective neuromuscular synaptogenesis in agrin-deficient mutant mice. Cell 85:525-35
40. Ghiselli G, Farber SA. 2005. D-glucuronyl C5-epimerase acts in dorso-ventral axis formation in zebrafish. BMC Dev. Biol. 5:19
41. Gleghorn L, Ramesar R, Beighton P, Wallis G. 2005. A mutation in the variable repeat region of the aggrecan gene (AGC1) causes a form of spondyloepiphyseal dysplasia associated with severe, premature osteoarthritis. Am. J. Hum. Genet. 77:484-90
42. Grako KA, Ochiya T, Barritt D, Nishiyama A, Stallcup WB. 1999. PDGFα-receptor is unresponsive to PDGF-AA in aortic smooth muscle cells from the NG2 knockout mouse. J. Cell Sci. 112(Pt. 6):905-15
43. Gregg RG, Mukhopadhyay S, Candille SI, Ball SL, Pardue MT, et al. 2003. Identification of the gene and the mutation responsible for the mouse nob phenotype. Invest. Ophthalmol. Vis. Sci. 44:378-84
44. Grobe K, Inatani M, Pallerla SR, Castagnola J, Yamaguchi Y, Esko JD. 2005. Cerebral hypoplasia and craniofacial defects in mice lacking heparan sulfate Ndst1 gene function. Development 132:3777-86
45. Häcker U, Lin X, Perrimon N. 1997. The Drosophila sugarless gene modulates Wingless signaling and encodes an enzyme involved in polysaccharide biosynthesis. Development 124:3565-73
46. Häcker U, Nybakken K, Perrimon N. 2005. Heparan sulphate proteoglycans: the sweet side of development. Nat. Rev. Mol. Cell Biol. 6:530-41
47. HajMohammadi S, Enjyoji K, Princivalle M, Christi P, Lech M, et al. 2003. Normal levels of anticoagulant heparan sulfate are not essential for normal hemostasis. J. Clin. Invest. 111:989-99
48. Han C, Belenkaya TY, Khodoun M, Tauchi M, Lin X. 2004. Distinct and collaborative roles of Drosophila EXT family proteins in morphogen signaling and gradient formation. Development 131:1563-75
49. Hao JC, Yu TW, Fujisawa K, Culotti JG, Gengyo-Ando K, et al. 2001. C. elegans Slit acts in midline, dorsal-ventral, and anterior-posterior guidance via the SAX-3/Robo receptor. Neuron 32:25-38
50. Harroch S, Furtado GC, Brueck W, Rosenbluth J, Lafaille J, et al. 2002. A critical role for the protein tyrosine phosphatase receptor type Z in functional recovery from demyelinating lesions. Nat. Genet. 32:411-14
51. Harroch S, Palmeri M, Rosenbluth J, Custer A, Okigaki M, et al. 2000. No obvious abnormality in mice deficient in receptor protein tyrosine phosphatase β. Mol. Cell Biol. 20:7706-15
52. Herman T, Hartwieg E, Horvitz HR. 1999. sqv mutants of Caenorhabditis elegans are defective in vulval epithelial invagination. Proc. Natl. Acad. Sci. USA 96:968-73
53. Herman T, Horvitz HR. 1999. Three proteins involved in Caenorhabditis elegans vulval invagination are similar to components of a glycosylation pathway. Proc. Natl. Acad. Sci. USA 96:974-79
54. Hobert O, Bülow H. 2003. Development and maintenance of neuronal architecture at the ventral midline of C. elegans. Curr. Opin. Neurobiol. 13:70-78
55. Hu H. 2001. Cell-surface heparan sulfate is involved in the repulsive guidance activities of Slit2 protein. Nat. Neurosci. 4:695-701
56. Humphries DE, Wong GW, Friend DS, Gurish MF, Qiu WT, et al. 1999. Heparin is essential for the storage of specific granule proteases in mast cells. Nature 400:769-72
57. Hwang HY, Olson SK, Brown JR, Esko JD, Horvitz HR. 2003a. The Caenorhabditis elegans genes sqv-2 and sqv-6, which are required for vulval morphogenesis, encode glycosaminoglycan galactosyltransferase II and xylosyltransferase. J. Biol. Chem. 278:11735-38
58. Hwang HY, Horvitz HR. 2002. The SQV-1 UDP-glucuronic acid decarboxylase and the SQV-7 nucleotide-sugar transporter may act in the Golgi apparatus to affect Caenorhabditis elegans vulval morphogenesis and embryonic development. Proc. Natl. Acad. Sci. USA 99:14218-23
59. Hwang HY, Olson SK, Esko JD, Horvitz HR. 2003b. Caenorhabditis elegans early embryogenesis and vulval morphogenesis require chondroitin biosynthesis. Nature 423:439-43
60. Inatani M, Irie F, Plump AS, Tessier-Lavigne M, Yamaguchi Y. 2003. Mammalian brain morphogenesis and midline axon guidance require heparan sulfate. Science 302:1044-46
61. Iozzo RV. 1999. The biology of the small leucine-rich proteoglycans. Functional network of interactive proteins. J. Biol. Chem. 274:18843-46
62. Ishiguro K, Kadomatsu K, Kojima T, Muramatsu H, Matsuo S, et al. 2001. Syndecan-4 deficiency increases susceptibility to κ-carrageenan-induced renal damage. Lab. Invest. 81:509-16
63. Ishiguro K, Kadomatsu K, Kojima T, Muramatsu H, Nakamura E, et al. 2000a. Syndecan-4 deficiency impairs the fetal vessels in the placental labyrinth. Dev. Dyn. 219:539-44
64. Ishiguro K, Kadomatsu K, Kojima T, Muramatsu H, Tsuzuki S, et al. 2000b. Syndecan-4 deficiency impairs focal adhesion formation only under restricted conditions. J. Biol. Chem. 275:5249-52
65. Jepsen KJ, Wu F, Peragallo JH, Paul J, Roberts L, et al. 2002. A syndrome of joint laxity and impaired tendon integrity in lumican- and fibromodulin-deficient mice. J. Biol. Chem. 277:35532-40
66. Johnson KG, Ghose A, Epstein E, Lincecum J, O'Connor MB, Van Vactor D. 2004. Axonal heparan sulfate proteoglycans regulate the distribution and efficiency of the repellent slit during midline axon guidance. Curr. Biol. 14:499-504
67. Jüttner R, More MI, Das D, Babich A, Meier J, et al. 2005. Impaired synapse function during postnatal development in the absence of CALEB, an EGF-like protein processed by neuronal activity. Neuron 46:233-45
68. 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. J. Biol. Chem. 276:17014-21
69. Kamimura K, Rhodes JM, Ueda R, McNeely M, Shukla D, et al. 2004. Regulation of Notch signaling by Drosophila heparan sulfate 3-O sulfotransferase. J. Cell Biol. 166:1069-79
70. Kantor DB, Chivatakarn O, Peer KL, Oster SF, Inatani M, et al. 2004. Semaphorin 5A is a bifunctional axon guidance cue regulated by heparan and chondroitin sulfate proteoglycans. Neuron 44:961-75
71. Khan AA, Bose C, Yam LS, Soloski MJ, Rupp F. 2001. Physiological regulation of the immunological synapse by agrin. Science 292:1681-86
72. Kiernan BW, Garcion E, Ferguson J, Frost EE, Torres EM, et al. 1999. Myelination and behavior of tenascin-C null transgenic mice. Eur. J. Neurosci. 11:3082-92
73. Kinnunen T, Huang Z, Townsend J, Gatdula MM, Brown JR, et al. 2005. Heparan 2-O-sulfotransferase, hst-2, is essential for normal cell migration in Caenorbabditis elegans. Proc. Natl. Acad. Sci. USA 102:1507-12
74. Kirkpatrick CA, Dimitroff BD, Rawson JM, Selleck SB. 2004. Spatial regulation of Wingless morphogen distribution and signaling by Dally-like protein. Dev. Cell 7:513-23
75. Kizawa H, Kou I, Iida A, Sudo A, Miyamoto Y, et al. 2005. An aspartic acid repeat polymorphism in asporin inhibits chondrogenesis and increases susceptibility to osteoarthritis. Nat. Genet. 37:138-44
76. Klüppel M, Wight TN, Chan C, Hinek A, Wrana JL. 2005. Maintenance of chondroitin sulfation balance by chondroitin-4-sulfotransferase 1 is required for chondrocyte development and growth factor signaling during cartilage morphogenesis. Development 132:3989-4003
77. Kramer KL, Yost HJ. 2002. Ectodermal syndecan-2 mediates left-right axis formation in migrating mesoderm as a cell-nonautonomous Vg1 cofactor. Dev. Cell 2:115-24
78. Kramer KL, Yost HJ. 2003. Heparan sulfate core proteins in cell-cell signaling. Annu. Rev. Genet. 37:461-84
79. Kreuger J, Perez L, Giraldez AJ, Cohen SM. 2004. Opposing activities of Dally-like glypican at high and low levels of Wingless morphogen activity. Dev. Cell 7:503-12
80. Kruse K, Pantazis P, Bollenbach T, Julicher F, Gonzalez-Gaitan M. 2004. Dpp gradient formation by dynamin-dependent endocytosis: receptor trafficking and the diffusion model. Development 131:4843-56
81. Kusche-Gullberg M, Kjellen L. 2003. Sulfotransferases in glycosaminoglycan biosynthesis. Curr. Opin. Struct. Biol. 13:605-11
82. Lander AD, Nie Q, Wan FY. 2002. Do morphogen gradients arise by diffusion? Dev. Cell 2:785-96
83. Lee JS, von der Hardt S, Rusch MA, Stringer SE, Stickney HL, et al. 2004. Axon sorting in the optic tract requires HSPG synthesis by ext2 (dackel) and extl3 (boxer). Neuron 44:947-60
84. Li JP, Gong F, Hagner-McWhirter A, Forsberg E, Abrink M, et al. 2003. Targeted disruption of a murine glucuronyl C5-epimerase gene results in heparan sulfate lacking L-iduronic acid and in neonatal lethality. J. Biol. Chem. 278:28363-66
85. Li Q, Park PW, Wilson CL, Parks WC. 2002. Matrilysin shedding of syndecan-1 regulates chemokine mobilization and transepithelial efflux of neutrophils in acute lung injury. Cell 111:635-46
86. Lin X. 2004. Functions of heparan sulfate proteoglycans in cell signaling during development. Development 131:6009-21
87. Lin X, Buff EM, Perrimon N, Michelson AM. 1999. Heparan sulfate proteoglycans are essential for FGF receptor signaling during Drosophila embryonic development. Development 126:3715-23
88. Lin X, Perrimon N. 1999. Dally cooperates with Drosophila Frizzled 2 to transduce Wingless signaling. Nature 400:281-84
89. Lin X, Wei G, Shi Z, Dryer L, Esko JD, et al. 2000. Disruption of gastrulation and heparan sulfate biosynthesis in EXT1-deficient mice. Dev. Biol. 224:299-311
90. Lindahl U, Kusche-Gullberg M, Kjellen L. 1998. Regulated diversity of heparan sulfate. J. Biol. Chem. 273:24979-82
91. Liu CY, Birk DE, Hassell JR, Kane B, Kao WW. 2003. Keratocan-deficient mice display alterations in corneal structure. J. Biol. Chem. 278:21672-77
92. Maccarana M, Olander B, Malmstrom J, Tiedemann K, Aebersold R, et al. 2006. Biosynthesis of dermatan sulfate: Chondroitin glucuronate C5-epimerase is identical to SART2. J. Biol. Chem. 281:11560-68
93. Marneros AG, Olsen BR. 2005. Physiological role of collagen XVIII and endostatin. FASEB J. 19:716-28
94. McLaughlin D, Karlsson F, Tian N, Pratt T, Bullock SL, et al. 2003. Specific modification of heparan sulphate is required for normal cerebral cortical development. Mech. Dev. 120:1481-88
95. Merz DC, Alves G, Kawano T, Zheng H, Culotti JG. 2003. UNC-52/perlecan affects gonadal leader cell migrations in C. elegans hermaphrodites through alterations in growth factor signaling. Dev. Biol. 256:173-86
96. Minniti AN, Labarca M, Hurtado C, Brandan E. 2004. Caenorhabditis elegans syndecan (SDN-1) is required for normal egg laying and associates with the nervous system and the vulva. J. Cell Sci. 117:5179-90
97. Mitchell KJ, Pinson KI, Kelly OG, Brennan J, Zupicich J, et al. 2001. Functional analysis of secreted and transmembrane proteins critical to mouse development. Nat. Genet. 28:241-49
98. Mizuguchi S, Uyama T, Kitagawa H, Nomura KH, Dejima K, et al. 2003. Chondroitin proteoglycans are involved in cell division of Caenorhabditis elegans. Nature 423:443-48
99. Mjaatvedt CH, Yamamura H, Capehart AA, Turner D, Markwald RR. 1998. The Cspg2 gene, disrupted in the hdf mutant, is required for right cardiac chamber and endocardial cushion formation. Dev. Biol. 202:56-66
100. Morio H, Honda Y, Toyoda H, Nakajima M, Kurosawa H, Shirasawa T. 2003. EXT gene family member rib-2 is essential for embryonic development and heparan sulfate biosynthesis in Caenorhabditis elegans. Biochem. Biophys. Res. Commun. 301:317-23
101. Muñoz R, Moreno M, Oliva C, Orbenes C, Larraín J. 2006. Syndecan-4 regulates non-canonical Wnt signalling and is essential for convergent and extension movements in Xenopus embryos. Nat. Cell Biol. 8(5):492-500
102. Nakato H, Futch TA, Selleck SB. 1995. The division abnormally delayed (dally) gene: a putative integral membrane proteoglycan required for cell division patterning during postembryonic development of the nervous system in Drosophila. Development 121:3687-702
103. Nicole S, Davoine CS, Topaloglu H, Cattolico L, Barral D, et al. 2000. Perlecan, the major proteoglycan of basement membranes, is altered in patients with Schwartz-Jampel syndrome (chondrodystrophic myotonia). Nat. Genet. 26:480-83
104. Ohta M, Sakai T, Saga Y, Aizawa S, Saito M. 1998. Suppression of hematopoietic activity in tenascin-C-deficient mice. Blood 91:4074-83
105. Okajima T, Fukumoto S, Furukawa K, Urano T. 1999. Molecular basis for the progeroid variant of Ehlers-Danlos syndrome. Identification and characterization of two mutations in galactosyltransferase I gene. J. Biol. Chem. 274:28841-44
106. Ortega S, Ittmann M, Tsang SH, Ehrlich M, Basilico C. 1998. Neuronal defects and delayed wound healing in mice lacking fibroblast growth factor 2. Proc. Natl. Acad. Sci. USA 95:5672-77
107. Park PW, Pier GB, Hinkes MT, Bernfield M. 2001. Exploitation of syndecan-1 shedding by Pseudomonas aeruginosa enhances virulence. Nature 411:98-102
108. Park Y, Rangel C, Reynolds MM, Caldwell MC, Johns M, et al. 2003. Drosophila perlecan modulates FGF and hedgehog signals to activate neural stem cell division. Dev. Biol. 253:247-57
109. Pellegata NS, Dieguez-Lucena JL, Joensuu T, Lau S, Montgomery KT, et al. 2000. Mutations in KERA, encoding keratocan, cause cornea plana. Nat. Genet. 25:91-95
110. Pellegrini L. 2001. Role of heparan sulfate in fibroblast growth factor signaling: a structural view. Curr. Opin. Struct. Biol. 11:629-34
111. Perrimon N, Lanjuin A, Arnold C, Noll E. 1996. Zygotic lethal mutations with maternal effect phenotypes in Drosophila melanogaster. II. Loci on the second and third chromosomes identified by P-element-induced mutations. Genetics 144:1681-92
112. Pilia G, Hughes-Benzie RM, MacKenzie A, Baybayan P, Chen EY, et al. 1996. Mutations in GPC3, a glypican gene, cause the Simpson-Golabi-Behmel overgrowth syndrome. Nat. Genet. 12:241-47
113. Pusch CM, Zeitz C, Brandau O, Pesch K, Achatz H, et al. 2000. The complete form of X-linked congenital stationary night blindness is caused by mutations in a gene encoding a leucine-rich repeat protein. Nat. Genet. 26:324-27
114. Quentin E, Gladen A, Roden L, Kresse H. 1990. A genetic defect in the biosynthesis of dermatan sulfate proteoglycan: galactosyltransferase I deficiency in fibroblasts from a patient with a progeroid syndrome. Proc. Natl. Acad. Sci. USA 87:1342-46
115. Rauch U, Zhou XH, Roos G. 2005. Extracellular matrix alterations in brains lacking four of its components. Biochem. Biophys. Res. Commun. 328:608-17
116. Rawson JM, Dimitroff B, Johnson KG, Rawson JM, Ge X, et al. 2005. The heparan sulfate proteoglycans Dally-like and Syndecan have distinct functions in axon guidance and visual-system assembly in Drosophila. Curr. Biol. 15:833-38
117. Reizes O, Lincecum J, Wang Z, Goldberger O, Huang L, et al. 2001. Transgenic expression of syndecan-1 uncovers a physiological control of feeding behavior by syndecan-3. Cell 106:105-16
118. Rhiner C, Gysi S, Frohli E, Hengartner MO, Hajnal A. 2005. Syndecan regulates cell migration and axon guidance in C. elegans. Development 132:4621-33
119. Rhodes KE, Fawcett JW. 2004. Chondroitin sulphate proteoglycans: preventing plasticity or protecting the CNS? J. Anat. 204:33-48
120. Ringvall M, Ledin J, Holmborn K, van Kuppevelt T, Ellin F, et al. 2000. Defective heparan sulfate biosynthesis and neonatal lethality in mice lacking N-deacetylase/N-sulfotransferase-1. J. Biol. Chem. 275:25926-30
121. Rogalski TM, Williams BD, Mullen GP, Moerman DG. 1993. Products of the unc-52 gene in Caenorhabditis elegans are homologous to the core protein of the mammalian basement membrane heparan sulfate proteoglycan. Genes Dev. 7:1471-84
122. Rossi M, Morita H, Sormunen R, Airenne S, Kreivi M, et al. 2003. Heparan sulfate chains of perlecan are indispensable in the lens capsule but not in the kidney. EMBO J. 22:236-45
123. Rugarli EI, Ballabio A. 1993. Kallmann syndrome. From genetics to neurobiology. JAMA 270:2713-16
124. Rugarli EI, Di Schiavi E, Hilliard MA, Arbucci S, Ghezzi C, et al. 2002. The Kallmann syndrome gene homolog in C. elegans is involved in epidermal morphogenesis and neurite branching. Development 129:1283-94
125. Saga Y, Yagi T, Ikawa Y, Sakakura T, Aizawa S. 1992. Mice develop normally without tenascin. Genes Dev. 6:1821-31
126. Sedita J, Izvolsky K, Cardoso WV. 2004. Differential expression of heparan sulfate 6-O-sulfotransferase isoforms in the mouse embryo suggests distinctive roles during organogenesis. Dev. Dyn. 231:782-94
127. Seidler DG, Faiyaz-Ul-Haque M, Hansen U, Yip GW, Zaidi SH, et al. 2006. Defective glycosylation of decorin and biglycan, altered collagen structure, and abnormal phenotype of the skin fibroblasts of an Ehlers-Danlos syndrome patient carrying the novel Arg270Cys substitution in galactosyltransferase I (β4GalT-7). J. Mol. Med. Published online April 1, 2006; doi: 10.1007/s00109-006-0046-4
128. Sen J, Goltz JS, Stevens L, Stein D. 1998. Spatially restricted expression of pipe in the Drosophila egg chamber defines embryonic dorsal-ventral polarity. Cell 95:471-81
129. Sertie AL, Sossi V, Camargo AA, Zatz M, Brahe C, Passos-Bueno MR. 2000. Collagen XVIII, containing an endogenous inhibitor of angiogenesis and tumor growth, plays a critical role in the maintenance of retinal structure and in neural tube closure (Knobloch syndrome). Hum. Mol. Genet. 9:2051-58
130. Shworak NW, HajMohammadi S, De Agostini AI, Rosenberg RD. 2003. Mice deficient in heparan sulfate 3-O-sulfotransferase-1: normal hemostasis with unexpected perinatal phenotypes. Glycoconj. J. 19:355-61
131. Song HH, Shi W, Xiang YY, Filmus J. 2005. The loss of glypican-3 induces alterations in Wnt signaling. J. Biol. Chem. 280:2116-25
132. Spicer AP, Tien JL, Joo A, Bowling RA Jr. 2002. Investigation of hyaluronan function in the mouse through targeted mutagenesis. Glycoconj. J. 19:341-45
133. Steigemann P, Molitor A, Fellert S, Jackle H, Vorbruggen G. 2004. Heparan sulfate proteoglycan syndecan promotes axonal and myotube guidance by slit/robo signaling. Curr. Biol. 14:225-30
134. Stickens D, Clines G, Burbee D, Ramos P, Thomas S, et al. 1996. The EXT2 multiple exostoses gene defines a family of putative tumor suppressor genes. Nat. Genet. 14:25-32
135. Stickens D, Zak BM, Rougier N, Esko JD, Werb Z. 2005. Mice deficient in Ext2 lack heparan sulfate and develop exostoses. Development 132:5055-68
136. Sugahara K, Kitagawa H. 2002. Heparin and heparan sulfate biosynthesis. IUBMB Life 54:163-75
137. Sugahara K, Mikami T, Uyama T, Mizuguchi S, Nomura K, Kitagawa H. 2003. Recent advances in the structural biology of chondroitin sulfate and dermatan sulfate. Curr. Opin. Struct. Biol. 13:612-20
138. Svensson L, Aszodi A, Reinholt FP, Fassler R, Heinegard D, Oldberg A. 1999. Fibromodulin-null mice have abnormal collagen fibrils, tissue organization, and altered lumican deposition in tendon. J. Biol. Chem. 274:9636-47
139. Takei Y, Ozawa Y, Sato M, Watanabe A, Tabata T. 2004. Three Drosophila EXT genes shape morphogen gradients through synthesis of heparan sulfate proteoglycans. Development 131:73-82
140. Tasheva ES, Koester A, Paulsen AQ, Garrett AS, Boyle DL, et al. 2002. Mimecan/osteoglycin-deficient mice have collagen fibril abnormalities. Mol. Vis. 8:407-15
141. Thiele H, Sakano M, Kitagawa H, Sugahara K, Rajab A, et al. 2004. Loss of chondroitin 6-O-sulfotransferase-1 function results in severe human chondrodysplasia with progressive spinal involvement. Proc. Natl. Acad. Sci. USA 101:10155-60
142. Toole BP. 2001. Hyaluronan in morphogenesis. Semin. Cell Dev. Biol. 12:79-87
143. Toole BP. 2004. Hyaluronan: from extracellular glue to pericellular cue. Nat. Rev. Cancer 4:528-39
144. Topczewski J, Sepich DS, Myers DC, Walker C, Amores A, et al. 2001. The zebrafish glypican knypek controls cell polarity during gastrulation movements of convergent extension. Dev. Cell 1:251-64
145. Toyoda H, Kinoshita-Toyoda A, Selleck SB. 2000. Structural analysis of glycosaminoglycans in Drosophila and Caenorhabditis elegans and demonstration that tout-velu, a Drosophila gene related to EXT tumor suppressors, affects heparan sulfate in vivo. J. Biol. Chem. 275:2269-75
146. Turnbull J, Powell A, Guimond S. 2001. Heparan sulfate: decoding a dynamic multifunctional cell regulator. Trends Cell Biol. 11:75-82
147. Turnbull JE. 2001. Integral glycan sequencing of heparan sulfate and heparin saccharides. Methods Mol. Biol. 171:129-39
148. Uchimura K, Kadomatsu K, Nishimura H, Muramatsu H, Nakamura E, et al. 2002. Functional analysis of the chondroitin 6-sulfotransferase gene in relation to lymphocyte subpopulations, brain development, and oversulfated chondroitin sulfates. J. Biol. Chem. 277:1443-50
149. Uchimura K, Kadomatsu K, El-Fasakhany FM, Singer MS, Izawa M, et al. 2004. N-acetylglucosamine 6-O-sulfotransferase-1 regulates expression of L-selectin ligands and lymphocyte homing. J. Biol. Chem. 279:35001-8
150. Van Vactor D, Wall DP, Johnson KG. 2006. Heparan sulfate proteoglycans and the emergence of neuronal connectivity. Curr. Opin. Neurobiol. 16:40-51
151. Varki A, Cummings R, Esko J, Freeze H, Hart G, Marth J, eds. 2006. Essentials of Glycobiology. Cold Spring Harbor, New York: Cold Spring Harb. Lab. 2nd ed.
152. Venkataraman G, Shriver Z, Raman R, Sasisekharan R. 1999. Sequencing complex polysaccharides. Science 286:537-42
153. Wang L, Fuster M, Sriramarao P, Esko JD. 2005. Endothelial heparan sulfate deficiency impairs L-selectin- and chemokine-mediated neutrophil trafficking during inflammatory responses. Nat. Immunol. 6:902-10
154. Watanabe H, Kimata K, Line S, Strong D, Gao LY, et al. 1994. Mouse cartilage matrix deficiency (cmd) caused by a 7 bp deletion in the aggrecan gene. Nat. Genet. 7:154-57
155. Weber P, Bartsch U, Rasband MN, Czaniera R, Lang Y, et al. 1999. Mice deficient for tenascin-R display alterations of the extracellular matrix and decreased axonal conduction velocities in the CNS. J. Neurosci. 19:4245-62
156. Xu T, Bianco P, Fisher LW, Longenecker G, Smith E, et al. 1998. Targeted disruption of the biglycan gene leads to an osteoporosis-like phenotype in mice. Nat. Genet. 20:78-82
157. Yamaguchi Y. 2000. Lecticans: organizers of the brain extracellular matrix. Cell Mol. Life Sci. 57:276-89
158. Young MF, Bi Y, Ameye L, Chen XD. 2003. Biglycan knockout mice: new models for musculoskeletal diseases. Glycoconj. J. 19:257-62
159. Yu TW, Bargmann CI. 2001. Dynamic regulation of axon guidance. Nat. Neurosci. 4:1169-76
160. Zallen JA, Yi BA, Bargmann CI. 1998. The conserved immunoglobulin superfamily member SAX-3/Robo directs multiple aspects of axon guidance in C. elegans. Cell 92:217-27
161. Zhang H, Muramatsu T, Murase A, Yuasa S, Uchimura K, Kadomatsu K. 2006. N-acetylglucosamine 6-O-sulfotransferase-1 is required for brain keratan sulfate biosynthesis and glial scar formation after brain injury. Glycobiology 16:702-10
162. Zhou M, Sutliff RL, Paul RJ, Lorenz JN, Hoying JB, et al. 1998. Fibroblast growth factor 2 control of vascular tone. Nat. Med. 4:201-7
163. Zhou XH, Brakebusch C, Matthies H, Oohashi T, Hirsch E, et al. 2001. Neurocan is dispensable for brain development. Mol. Cell Biol. 21:5970-78
164. Zhu X, Sen J, Stevens L, Goltz JS, Stein D. 2005. Drosophila pipe protein activity in the ovary and the embryonic salivary gland does not require heparan sulfate glycosaminoglycans. Development 132:3813-22