Heparan sulphate proteoglycans fine-tune mammalian physiology (original) (raw)

• Bulow, H. E. & Hobert, O. The molecular diversity of glycosaminoglycans shapes animal development. Annu. Rev. Cell Dev. Biol. 22, 375–407 (2006).
  CAS PubMed Google Scholar
• Hacker, U., Nybakken, K. & Perrimon, N. Heparan sulphate proteoglycans: the sweet side of development. Nature Rev. Mol. Cell Biol. 6, 530–541 (2005).
  Google Scholar
• Haltiwanger, R. S. & Lowe, J. B. Role of glycosylation in development. Annu. Rev. Biochem. 73, 491–537 (2004).
  CAS PubMed Google Scholar
• Esko, J. D. & Selleck, S. B. Order out of chaos: assembly of ligand binding sites in heparan sulfate. Annu. Rev. Biochem. 71, 435–471 (2002).
  CAS PubMed Google Scholar
• Dhoot, G. K. et al. Regulation of Wnt signaling and embryo patterning by an extracellular sulfatase. Science 293, 1663–1666 (2001).
  ADS CAS Google Scholar
• Morimoto-Tomita, M., Uchimura, K., Werb, Z., Hemmerich, S. & Rosen, S. D. Cloning and characterization of two extracellular heparin-degrading endosulfatases in mice and humans. J. Biol. Chem. 277, 49175–49185 (2002).
  CAS PubMed PubMed Central Google Scholar
• Vlodavsky, I. et al. Mammalian heparanase: involvement in cancer metastasis, angiogenesis and normal development. Semin. Cancer Biol. 12, 121–129 (2002).
  CAS PubMed Google Scholar
• Fedarko, N. S. & Conrad, H. E. A unique heparan sulfate in the nuclei of hepatocytes: structural changes with the growth state of the cells. J.Cell Biol. 102, 587–599 (1986).
  CAS PubMed Google Scholar
• Huntington, J. A. Mechanisms of glycosaminoglycan activation of the serpins in hemostasis. J. Thromb. Haemost. 1, 1535–1549 (2003).
  CAS PubMed Google Scholar
• Mohammadi, M., Olsen, S. K. & Ibrahimi, O. A. Structural basis for fibroblast growth factor receptor activation. Cytokine Growth Factor Rev. 16, 107–137 (2005).
  CAS PubMed Google Scholar
• Forsten-Williams, K., Chua, C. C. & Nugent, M. A. The kinetics of FGF-2 binding to heparan sulfate proteoglycans and MAP kinase signaling. J. Theor. Biol. 233, 483–499 (2005).
  CAS PubMed Google Scholar
• Kreuger, J., Spillmann, D., Li, J. P. & Lindahl, U. Interactions between heparan sulfate and proteins: the concept of specificity. J. Cell Biol. 174, 323–327 (2006).
  CAS PubMed PubMed Central Google Scholar
• Alexopoulou, A. N., Multhaupt, H. A. & Couchman, J. R. Syndecans in wound healing, inflammation and vascular biology. Int. J. Biochem. Cell Biol. 39, 505–528 (2006).
  PubMed Google Scholar
• Couchman, J. R., Chen, L. G. & Woods, A. Syndecans and cell adhesion. Int. Rev. Cytol. 207, 113–150 (2001).
  CAS PubMed Google Scholar
• Kirkpatrick, C. A. et al. The function of a Drosophila glypican does not depend entirely on heparan sulfate modification. Dev. Biol. 300, 570–582 (2006).
  CAS PubMed Google Scholar
• Reizes, O. et al. Transgenic expression of syndecan-1 uncovers a physiological control of feeding behavior by syndecan-3. Cell 106, 105–116 (2001).
  CAS PubMed Google Scholar
• Strader, A. D., Reizes, O., Woods, S. C., Benoit, S. C. & Seeley, R. J. Mice lacking the syndecan-3 gene are resistant to diet-induced obesity. J. Clin. Invest. 114, 1354–1360 (2004).
  CAS PubMed PubMed Central Google Scholar
• Zcharia, E. et al. Transgenic expression of mammalian heparanase uncovers physiological functions of heparan sulfate in tissue morphogenesis, vascularization, and feeding behavior. FASEB J. 18, 252–263 (2004).
  CAS PubMed Google Scholar
• Mahley, R. W. & Ji, Z. S. Remnant lipoprotein metabolism: key pathways involving cell-surface heparan sulfate proteoglycans and apolipoprotein E. J. Lipid Res. 40, 1–16 (1999).
  ADS CAS PubMed Google Scholar
• MacArthur, J. M. et al. Liver heparan sulfate proteoglycans mediate clearance of triglyceride-rich lipoproteins independently of LDL receptor family members. J. Clin. Invest. 117, 153–164 (2007).
  CAS PubMed PubMed Central Google Scholar
• Fuki, I. V. et al. The syndecan family of proteoglycans. Novel receptors mediating internalization of atherogenic lipoproteins in vitro. J. Clin. Invest. 100, 1611–1622 (1997).
  CAS PubMed PubMed Central Google Scholar
• Zeng, B. J., Mortimer, B. C., Martins, I. J., Seydel, U. & Redgrave, T. G. Chylomicron remnant uptake is regulated by the expression and function of heparan sulfate proteoglycan in hepatocytes. J. Lipid Res. 39, 845–860 (1998).
  CAS PubMed Google Scholar
• Iozzo, R. V. Basement membrane proteoglycans: from cellar to ceiling. Nature Rev. Mol. Cell Biol. 6, 646–656 (2005).
  CAS Google Scholar
• Raats, C. J. I., Van den Born, J. & Berden, J. H. M. Glomerular heparan sulfate alterations: mechanisms and relevance for proteinuria. Kidney Int. 57, 385–400 (2000).
  CAS PubMed Google Scholar
• Kanwar, Y. S., Linker, A. & Farquhar, M. G. Increased permeability of the glomerular basement membrane to ferritin after removal of glycosaminoglycans (heparan sulfate) by enzyme digestion. J. Cell Biol. 86, 688–693 (1980).
  CAS PubMed Google Scholar
• Groffen, A. J. et al. Agrin is a major heparan sulfate proteoglycan in the human glomerular basement membrane. J. Histochem. Cytochem. 46, 19–27 (1998).
  CAS PubMed Google Scholar
• Arikawa-Hirasawa, E., Watanabe, H., Takami, H., Hassell, J. R. & Yamada, Y. Perlecan is essential for cartilage and cephalic development. Nature Genet. 23, 354–358 (1999).
  CAS PubMed Google Scholar
• Rossi, M. et al. Heparan sulfate chains of perlecan are indispensable in the lens capsule but not in the kidney. EMBO J. 22, 236–245 (2003).
  CAS PubMed PubMed Central Google Scholar
• Morita, H. et al. Heparan sulfate of perlecan is involved in glomerular filtration. J. Am. Soc. Nephrol. 16, 1703–1710 (2005).
  CAS PubMed Google Scholar
• Utriainen, A. et al. Structurally altered basement membranes and hydrocephalus in a type XVIII collagen deficient mouse line. Hum. Mol. Genet. 13, 2089–2099 (2004).
  CAS PubMed Google Scholar
• Gautam, M. et al. Defective neuromuscular synaptogenesis in agrin-deficient mutant mice. Cell 85, 525–535 (1996).
  CAS PubMed Google Scholar
• Westphal, V. et al. Reduced heparan sulfate accumulation in enterocytes contributes to protein-losing enteropathy in a congenital disorder of glycosylation. Am. J. Pathol. 157, 1917–1925 (2000).
  CAS PubMed PubMed Central Google Scholar
• Bode, L., Eklund, E. A., Murch, S. & Freeze, H. H. Heparan sulfate depletion amplifies TNF-α-induced protein leakage in an in vitro model of protein-losing enteropathy. Am. J. Physiol. Gastrointest. Liver Physiol. 288, G1015–G1023 (2005).
  CAS PubMed Google Scholar
• Donnelly, J. P., Rosenthal, A., Castle, V. P. & Holmes, R. D. Reversal of protein-losing enteropathy with heparin therapy in three patients with univentricular hearts and Fontan palliation. J. Pediatr. 130, 474–478 (1997).
  CAS PubMed Google Scholar
• Kronenberg, H. M. Developmental regulation of the growth plate. Nature 423, 332–336 (2003).
  ADS CAS Google Scholar
• Koziel, L., Kunath, M., Kelly, O. G. & Vortkamp, A. Ext1-dependent heparan sulfate regulates the range of Ihh signaling during endochondral ossification. Dev. Cell 6, 801–813 (2004).
  CAS PubMed Google Scholar
• Lander, A. D., Nie, Q. & Wan, F. Y. Do morphogen gradients arise by diffusion? Dev. Cell 2, 785–796 (2002).
  CAS PubMed Google Scholar
• Arikawa-Hirasawa, E. et al. Dyssegmental dysplasia, Silverman–Handmaker type, is caused by functional null mutations of the perlecan gene. Nature Genet. 27, 431–434 (2001).
  CAS PubMed Google Scholar
• Stickens, D., Zak, B. M., Rougier, N., Esko, J. D. & Werb, Z. Mice deficient in Ext2 lack heparan sulfate and develop exostoses. Development 132, 5055–5068 (2005).
  CAS PubMed PubMed Central Google Scholar
• Hovey, R. C., Trott, J. F. & Vonderhaar, B. K. Establishing a framework for the functional mammary gland: from endocrinology to morphology. J. Mammary Gland Biol. Neoplasia 7, 17–38 (2002).
  PubMed Google Scholar
• Liu, B. Y., McDermott, S. P., Khwaja, S. S. & Alexander, C. M. The transforming activity of Wnt effectors correlates with their ability to induce the accumulation of mammary progenitor cells. Proc. Natl Acad. Sci. USA 101, 4158–4163 (2004).
  ADS CAS PubMed Google Scholar
• Gautam, M., DeChiara, T. M., Glass, D. J., Yancopoulos, G. D. & Sanes, J. R. Distinct phenotypes of mutant mice lacking agrin, MuSK, or rapsyn. Brain Res. Dev. Brain Res. 114, 171–178 (1999).
  CAS PubMed Google Scholar
• Jenniskens, G. J. et al. Phenotypic knockout of heparan sulfates in myotubes impairs excitation-induced calcium spiking. FASEB J. 17, NIL606–NIL629 (2003).
  Google Scholar
• Mook-Jung, I. & Gordon, H. Acetylcholine receptor clustering in C2 muscle cells requires chondroitin sulfate. J.Neurobiol. 28, 482–492 (1995).
  CAS PubMed Google Scholar
• McDonnell, K. M. & Grow, W. A. Reduced glycosaminoglycan sulfation diminishes the agrin signal transduction pathway. Dev. Neurosci. 26, 1–10 (2004).
  CAS PubMed Google Scholar
• Kramer, K. L. & Yost, H. J. Ectodermal syndecan-2 mediates left–right axis formation in migrating mesoderm as a cell-nonautonomous Vg1 cofactor. Dev. Cell 2, 115–124 (2002).
  CAS PubMed Google Scholar
• Jakobsson, L. et al. Heparan sulfate in trans potentiates VEGFR-mediated angiogenesis. Dev. Cell 10, 625–634 (2006).
  CAS PubMed Google Scholar
• Parish, C. R. The role of heparan sulphate in inflammation. Nature Rev. Immunol. 6, 633–643 (2006).
  MathSciNet CAS Google Scholar
• Wang, L., Fuster, M., Sriramarao, P. & Esko, J. D. Endothelial heparan sulfate deficiency impairs L-selectin- and chemokine-mediated neutrophil trafficking during inflammatory responses. Nature Immunol. 6, 902–910 (2005).
  CAS Google Scholar
• Abrink, M., Grujic, M. & Pejler, G. Serglycin is essential for maturation of mast cell secretory granule. J. Biol. Chem. 279, 40897–40905 (2004).
  PubMed Google Scholar
• Humphries, D. E. et al. Heparin is essential for the storage of specific granule proteases in mast cells. Nature 400, 769–772 (1999).
  ADS CAS PubMed Google Scholar
• Forsberg, E. et al. Abnormal mast cells in mice deficient in a heparin-synthesizing enzyme. Nature 400, 773–776 (1999).
  ADS CAS PubMed Google Scholar
• Grujic, M. et al. Serglycin-deficient cytotoxic T lymphocytes display defective secretory granule maturation and granzyme B storage. J. Biol. Chem. 280, 33411–33418 (2005).
  CAS PubMed Google Scholar
• Zernichow, L. et al. Serglycin is the major secreted proteoglycan in macrophages and has a role in the regulation of macrophage tumor necrosis factor-α secretion in response to lipopolysaccharide. J. Biol. Chem. 281, 26792–26801 (2006).
  CAS PubMed Google Scholar
• Sher, I. et al. Targeting perlecan in human keratinocytes reveals novel roles for perlecan in epidermal formation. J. Biol. Chem. 281, 5178–5187 (2006).
  CAS PubMed Google Scholar
• Zhou, Z. et al. Impaired angiogenesis, delayed wound healing and retarded tumor growth in perlecan heparan sulfate-deficient mice. Cancer Res. 64, 4699–4702 (2004).
  CAS PubMed Google Scholar
• Echtermeyer, F. et al. Delayed wound repair and impaired angiogenesis in mice lacking syndecan-4. J. Clin. Invest. 107, 9–14 (2001).
  Google Scholar
• Stepp, M. A. et al. Defects in keratinocyte activation during wound healing in the syndecan-1-deficient mouse. J. Cell Sci. 115, 4517–4531 (2002).
  CAS PubMed Google Scholar
• Kainulainen, V., Wang, H. M., Schick, C. & Bernfield, M. Syndecans, heparan sulfate proteoglycans, maintain the proteolytic balance of acute wound fluids. J. Biol. Chem. 273, 11563–11569 (1998).
  CAS PubMed Google Scholar
• Midwood, K. S., Valenick, L. V., Hsia, H. C. & Schwarzbauer, J. E. Coregulation of fibronectin signaling and matrix contraction by tenascin-C and syndecan-4. Mol. Biol. Cell 15, 5670–5677 (2004).
  CAS PubMed PubMed Central Google Scholar
• Cool, S. M. & Nurcombe, V. Heparan sulfate regulation of progenitor cell fate. J. Cell Biochem. 99, 1040–1051 (2006).
  CAS PubMed Google Scholar
• Cornelison, D. D. et al. Essential and separable roles for syndecan-3 and syndecan-4 in skeletal muscle development and regeneration. Genes Dev. 18, 2231–2236 (2004).
  CAS PubMed PubMed Central Google Scholar
• Zcharia, E. et al. Heparanase regulates murine hair growth. Am. J. Pathol. 166, 999–1008 (2005).
  CAS PubMed PubMed Central Google Scholar
• De Agostini, A., Watkins, S. C., Slayter, H. S., Youssoufian, H. & Rosenberg, R. D. Localization of anticoagulantly active heparan sulfate proteoglycans in vascular endothelium: antithrombin binding on cultured endothelial cells and perfused rat aorta. J. Cell Biol. 111, 1293–1304 (1990).
  CAS PubMed Google Scholar
• Marcum, J. A., Fritze, L., Galli, S. J., Karp, G. & Rosenberg, R. D. Microvascular heparin-like species with anticoagulant activity. Am. J. Physiol. 245, H725–H733 (1983).
  CAS PubMed Google Scholar
• HajMohammadi, S. et al. Normal levels of anticoagulant heparan sulfate are not essential for normal hemostasis. J. Clin. Invest. 111, 989–999 (2003).
  CAS PubMed PubMed Central Google Scholar
• Shworak, N. W., HajMohammadi, S., De Agostini, A. I. & Rosenberg, R. D. Mice deficient in heparan sulfate 3-_O_-sulfotransferase-1: normal hemostasis with unexpected perinatal phenotypes. Glycoconj. J. 19, 355–361 (2002).
  CAS PubMed Google Scholar
• Hasan, S. et al. Coordinate expression of anticoagulant heparan sulfate proteoglycans and serine protease inhibitors in the rat ovary: a potent system of proteolysis control. Biol.Reprod. 66, 144–158 (2002).
  CAS PubMed Google Scholar
• Hosseini, G., Liu, J. & De Agostini, A. I. Characterization and hormonal modulation of anticoagulant heparan sulfate proteoglycans synthesized by rat ovarian granulosa cells. J. Biol. Chem. 271, 22090–22099 (1996).
  CAS PubMed Google Scholar
• Fuster, M. M. & Esko, J. D. The sweet and sour of cancer: glycans as novel therapeutic targets. Nature Rev. Cancer 5, 526–542 (2005).
  CAS Google Scholar
• van Horssen, J., Wesseling, P., van den Heuvel, L. P., de Waal, R. M. & Verbeek, M. M. Heparan sulphate proteoglycans in Alzheimer's disease and amyloid-related disorders. Lancet Neurol. 2, 482–492 (2003).
  CAS PubMed Google Scholar
• Li, J. P. et al. In vivo fragmentation of heparan sulfate by heparanase overexpression renders mice resistant to amyloid protein A amyloidosis. Proc. Natl Acad. Sci. USA 102, 6473–6477 (2005).
  ADS CAS PubMed Google Scholar
• Li, Q., Park, P. W., Wilson, C. L. & Parks, W. C. Matrilysin shedding of syndecan-1 regulates chemokine mobilization and transepithelial efflux of neutrophils in acute lung injury. Cell 111, 635–646 (2002).
  CAS PubMed Google Scholar
• Park, P. W., Pier, G. B., Hinkes, M. T. & Bernfield, M. Exploitation of syndecan-1 shedding by Pseudomonas aeruginosa enhances virulence. Nature 411, 98–102 (2001).
  ADS CAS PubMed Google Scholar
• Haynes, A. et al. Syndecan 1 shedding contributes to Pseudomonas aeruginosa sepsis. Infect. Immun. 73, 7914–7921 (2005).
  CAS PubMed PubMed Central Google Scholar
• Xu, J., Park, P. W., Kheradmand, F. & Corry, D. B. Endogenous attenuation of allergic lung inflammation by syndecan-1. J. Immunol. 174, 5758–5765 (2005).
  CAS PubMed Google Scholar
• Dinglasan, R. R. & Jacobs-Lorena, M. Insight into a conserved lifestyle: protein–carbohydrate adhesion strategies of vector-borne pathogens. Infect. Immun. 73, 7797–7807 (2005).
  CAS PubMed PubMed Central Google Scholar
• Bishop, J. R. & Esko, J. D. The elusive role of heparan sulfate in Toxoplasma gondii infection. Mol. Biochem. Parasitol. 139, 267–269 (2005).
  CAS PubMed Google Scholar
• Bishop, J. R., Crawford, B. E. & Esko, J. D. Cell surface heparan sulfate promotes replication of Toxoplasma gondii. Infect. Immun. 73, 5395–5401 (2005).
  CAS PubMed PubMed Central Google Scholar
• Cano-Gauci, D. F. et al. Glypican-3-deficient mice exhibit developmental overgrowth and some of the abnormalities typical of Simpson-Golabi-Behmel syndrome. J. Cell Biol. 146, 255–264 (1999).
  CAS PubMed PubMed Central Google Scholar
• Chiao, E. et al. Overgrowth of a mouse model of the Simpson–Golabi–Behmel syndrome is independent of IGF signaling. Dev. Biol. 243, 185–206 (2002).
  CAS PubMed Google Scholar
• Kaksonen, M. et al. Syndecan-3-deficient mice exhibit enhanced LTP and impaired hippocampus-dependent memory. Mol. Cell. Neurosci. 21, 158–172 (2002).
  CAS PubMed Google Scholar
• Grobe, K. et al. Cerebral hypoplasia and craniofacial defects in mice lacking heparan sulfate Ndst1 gene function. Development 132, 3777–3786 (2005).
  CAS PubMed Google Scholar
• Ringvall, M. et al. Defective heparan sulfate biosynthesis and neonatal lethality in mice lacking _N_-deacetylase/_N_-sulfotransferase-1. J. Biol. Chem. 275, 25926–25930 (2000).
  CAS PubMed Google Scholar
• Pan, Y., Woodbury, A., Esko, J. D., Grobe, K. & Zhang, X. Heparan sulfate biosynthetic gene Ndst1 is required for FGF signaling in early lens development. Development 133, 4933–4944 (2006).
  CAS PubMed Google Scholar
• Bullock, S. L., Fletcher, J. M., Beddington, R. S. & Wilson, V. A. Renal agenesis in mice homozygous for a gene trap mutation in the gene encoding heparan sulfate 2-sulfotransferase. Genes Dev. 12, 1894–1906 (1998).
  CAS PubMed PubMed Central Google Scholar
• Li, J. P. et al. 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, 28363–28366 (2003).
  CAS PubMed Google Scholar
• Serpinskaya, A. S., Feng, G., Sanes, J. R. & Craig, A. M. Synapse formation by hippocampal neurons from agrin-deficient mice. Dev. Biol. 205, 65–78 (1999).
  CAS PubMed Google Scholar
• Arikawa-Hirasawa, E., Rossi, S. G., Rotundo, R. L. & Yamada, Y. Absence of acetylcholinesterase at the neuromuscular junctions of perlecan-null mice. Nature Neurosci. 5, 119–123 (2002).
  CAS PubMed Google Scholar
• Viviano, B. L. et al. Altered hematopoiesis in glypican-3-deficient mice results in decreased osteoclast differentiation and a delay in endochondral ossification. Dev. Biol. 282, 152–162 (2005).
  CAS PubMed Google Scholar
• Paine-Saunders, S., Viviano, B. L., Zupicich, J., Skarnes, W. C. & Saunders, S. glypican-3 controls cellular responses to Bmp4 in limb patterning and skeletal development. Dev. Biol. 225, 179–187 (2000).
  CAS PubMed Google Scholar
• Pallerla, S. R., Pan, Y., Zhang, X., Esko, J. D. & Grobe, K. Heparan sulfate Ndst1 gene function variably regulates multiple signaling pathways during mouse development. Dev. Dyn. 236, 556–563 (2007).
  CAS PubMed Google Scholar
• Kram, V. et al. Heparanase is expressed in osteoblastic cells and stimulates bone formation and bone mass. J. Cell Physiol. 207, 784–792 (2006).
  CAS PubMed Google Scholar
• Zcharia, E. et al. Heparanase accelerates wound angiogenesis and wound healing in mouse and rat models. FASEB J. 19, 211–221 (2005).
  CAS PubMed Google Scholar
• Li, Q. & Olsen, B. R. Increased angiogenic response in aortic explants of collagen XVIII/endostatin-null mice. Am. J. Pathol. 165, 415–424 (2004).
  CAS PubMed PubMed Central Google Scholar
• Moulton, K. S. et al. Loss of collagen XVIII enhances neovascularization and vascular permeability in atherosclerosis. Circulation 110, 1330–1336 (2004).
  CAS PubMed Google Scholar
• Gotte, M. et al. Role of syndecan-1 in leukocyte–endothelial interactions in the ocular vasculature. Invest. Ophthalmol. Vis. Sci. 43, 1135–1141 (2002).
  PubMed Google Scholar
• Ishiguro, K. et al. Syndecan-4 deficiency impairs the fetal vessels in the placental labyrinth. Dev. Dyn. 219, 539–544 (2000).
  CAS PubMed Google Scholar
• Fan, G. et al. Targeted disruption of NDST-1 gene leads to pulmonary hypoplasia and neonatal respiratory distress in mice. FEBS Lett. 467, 7–11 (2000).
  ADS CAS PubMed Google Scholar
• Ishiguro, K. et al. Syndecan-4 deficiency increases susceptibility to κ-carrageenan-induced renal damage. Lab. Invest. 81, 509–516 (2001).
  CAS PubMed Google Scholar