Syndecan promotes axon regeneration by stabilizing growth cone migration

Cell Reports

Volumn 8, Issue 1, 2014, Pages 272-283

  Edwards, Tyson J ^a   Hammarlund, Marc ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SYNDECAN 1; SYNDECAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CAENORHABDITIS ELEGANS; CELL GROWTH; CONTROLLED STUDY; ENHANCER REGION; GABAERGIC SYSTEM; GROWTH CONE; GROWTH RATE; IN VIVO STUDY; MALE; MOTONEURON; NERVE FIBER REGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STABILITY; TIME LAPSE IMAGING; ANIMAL; GENETICS; METABOLISM; NERVE REGENERATION; PHYSIOLOGY; ADULT; FEMALE; MUTANT; TARGET CELL;

ANIMALS; CAENORHABDITIS ELEGANS; GROWTH CONES; NERVE REGENERATION; SYNDECANS;

EID: 84904428586     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.06.008     Document Type: Article

References (77)

1. Asikainen S., Vartiainen S., Lakso M., Nass R., Wong G. Selective sensitivity of Caenorhabditis elegans neurons to RNA interference. Neuroreport 2005, 16:1995-1999.
2. Attreed M., Desbois M., van Kuppevelt T.H., Bülow H.E. Direct visualization of specifically modified extracellular glycans in living animals. Nat. Methods 2012, 9:477-479.
3. Bass M.D., Roach K.A., Morgan M.R., Mostafavi-Pour Z., Schoen T., Muramatsu T., Mayer U., Ballestrem C., Spatz J.P., Humphries M.J. Syndecan-4-dependent Rac1 regulation determines directional migration in response to the extracellular matrix. J.Cell Biol. 2007, 177:527-538.
4. Bass M.D., Williamson R.C., Nunan R.D., Humphries J.D., Byron A., Morgan M.R., Martin P., Humphries M.J. A syndecan-4 hair trigger initiates wound healing through caveolin- and RhoG-regulated integrin endocytosis. Dev. Cell 2011, 21:681-693.
5. Bernfield M., Götte M., Park P.W., Reizes O., Fitzgerald M.L., Lincecum J., Zako M. Functions of cell surface heparan sulfate proteoglycans. Annu. Rev. Biochem. 1999, 68:729-777.
6. Bradke F., Fawcett J.W., Spira M.E. Assembly of a new growth cone after axotomy: the precursor to axon regeneration. Nat. Rev. Neurosci. 2012, 13:183-193.
7. Bülow H.E., Hobert O. Differential sulfations and epimerization define heparan sulfate specificity in nervous system development. Neuron 2004, 41:723-736.
8. Byrne A.B., Edwards T.J., Hammarlund M. Invivo Laser Axotomy in C. elegans. J.Vis. Exp 2011.
9. Calixto A., Chelur D., Topalidou I., Chen X., Chalfie M. Enhanced neuronal RNAi in C.elegans using SID-1. Nat. Methods 2010, 7:554-559.
10. Chau C.H., Shum D.K.Y., Chan Y.S., So K.-F. Heparan sulphates upregulate regeneration of transected sciatic nerves of adult guinea-pigs. Eur. J. Neurosci. 1999, 11:1914-1926.
11. Chen L., Wang Z., Ghosh-Roy A., Hubert T., Yan D., O'Rourke S., Bowerman B., Wu Z., Jin Y., Chisholm A.D. Axon regeneration pathways identified by systematic genetic screening in C.elegans. Neuron 2011, 71:1043-1057.
12. Clines G.A., Ashley J.A., Shah S., Lovett M. The structure of the human multiple exostoses 2 gene and characterization of homologs in mouse and Caenorhabditis elegans. Genome Res. 1997, 7:359-367.
13. Deepa S.S., Yamada S., Zako M., Goldberger O., Sugahara K. 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. A novel function to control binding of midkine, pleiotrophin, and basic fibroblast growth factor. J.Biol. Chem. 2004, 279:37368-37376.
14. Dent E.W., Gertler F.B. Cytoskeletal dynamics and transport in growth cone motility and axon guidance. Neuron 2003, 40:209-227.
15. Echtermeyer F., Baciu P.C., Saoncella S., Ge Y., Goetinck P.F. Syndecan-4 core protein is sufficient for the assembly of focal adhesions and actin stress fibers. J.Cell Sci. 1999, 112:3433-3441.
16. Echtermeyer F., Streit M., Wilcox-Adelman S., Saoncella S., Denhez F., Detmar M., Goetinck P. Delayed wound repair and impaired angiogenesis in mice lacking syndecan-4. J.Clin. Invest. 2001, 107:R9-R14.
17. El Bejjani R., Hammarlund M. Notch signaling inhibits axon regeneration. Neuron 2012, 73:268-278.
18. Elenius K., Vainio S., Laato M., Salmivirta M., Thesleff I., Jalkanen M. Induced expression of syndecan in healing wounds. J.Cell Biol. 1991, 114:585-595.
19. Elenius K., Määttä A., Salmivirta M., Jalkanen M. Growth factors induce 3T3 cells to express bFGF-binding syndecan. J.Biol. Chem. 1992, 267:6435-6441.
20. Ertürk A., Hellal F., Enes J., Bradke F. Disorganized microtubules underlie the formation of retraction bulbs and the failure of axonal regeneration. J.Neurosci. 2007, 27:9169-9180.
21. Esko J.D., Selleck S.B. Order out of chaos: assembly of ligand binding sites in heparan sulfate. Annu. Rev. Biochem. 2002, 71:435-471.
22. Fang-Yen C., Gabel C.V., Samuel A.D.T., Bargmann C.I., Avery L. Laser microsurgery in Caenorhabditis elegans. Methods in Cell Biology 2012, 177-206. Academic Press, New York. J.H. Rothman, A. Singson (Eds.).
23. Francis R., Waterston R.H. Muscle cell attachment in Caenorhabditis elegans. J.Cell Biol. 1991, 114:465-479.
24. Frøkjaer-Jensen C., Davis M.W., Hopkins C.E., Newman B.J., Thummel J.M., Olesen S.-P., Grunnet M., Jorgensen E.M. Single-copy insertion of transgenes in Caenorhabditis elegans. Nat. Genet. 2008, 40:1375-1383.
25. Frøkjær-Jensen C., Davis M.W., Ailion M., Jorgensen E.M. Improved Mos1-mediated transgenesis in C.elegans. Nat. Methods 2012, 9:117-118.
26. Fujisawa K., Wrana J.L., Culotti J.G. The slit receptor EVA-1 coactivates a SAX-3/Robo mediated guidance signal in C.elegans. Science 2007, 317:1934-1938.
27. Groves M.L., McKeon R., Werner E., Nagarsheth M., Meador W., English A.W. Axon regeneration in peripheral nerves is enhanced by proteoglycan degradation. Exp. Neurol. 2005, 195:278-292.
28. Hao J.C., Yu T.W., Fujisawa K., Culotti J.G., Gengyo-Ando K., Mitani S., Moulder G., Barstead R., Tessier-Lavigne M., Bargmann C.I. C.elegans slit acts in midline, dorsal-ventral, and anterior-posterior guidance via the SAX-3/Robo receptor. Neuron 2001, 32:25-38.
29. Hsueh Y.-P., Yang F.-C., Kharazia V., Naisbitt S., Cohen A.R., Weinberg R.J., Sheng M. Direct interaction of CASK/LIN-2 and syndecan heparan sulfate proteoglycan and their overlapping distribution in neuronal synapses. J.Cell Biol. 1998, 142:139-151.
30. Hu Y., González-Martínez D., Kim S.-H., Bouloux P.M.G. Cross-talk of anosmin-1, the protein implicated in X-linked Kallmann's syndrome, with heparan sulphate and urokinase-type plasminogen activator. Biochem. J. 2004, 384:495-505.
31. Hudson M.L., Kinnunen T., Cinar H.N., Chisholm A.D. C.elegans Kallmann syndrome protein KAL-1 interacts with syndecan and glypican to regulate neuronal cell migrations. Dev. Biol. 2006, 294:352-365.
32. Hussain S.-A., Piper M., Fukuhara N., Strochlic L., Cho G., Howitt J.A., Ahmed Y., Powell A.K., Turnbull J.E., Holt C.E., Hohenester E. A molecular mechanism for the heparan sulfate dependence of slit-robo signaling. J.Biol. Chem. 2006, 281:39693-39698.
33. Hwang H.-Y., Olson S.K., Esko J.D., Horvitz H.R. Caenorhabditis elegans early embryogenesis and vulval morphogenesis require chondroitin biosynthesis. Nature 2003, 423:439-443.
34. Jaakkola P., Vihinen T., Määttä A., Jalkanen M. Activation of an enhancer on the syndecan-1 gene is restricted to fibroblast growth factor family members in mesenchymal cells. Mol. Cell. Biol. 1997, 17:3210-3219.
35. Jaakkola P., Määttä A., Jalkanen M. The activation and composition of FiRE (an FGF-inducible response element) differ in a cell type- and growth factor-specific manner. Oncogene 1998, 17:1279-1286.
36. Jaakkola P., Kontusaari S., Kauppi T., Määtä A., Jalkanen M. Wound reepithelialization activates a growth factor-responsive enhancer in migrating keratinocytes. FASEB J. 1998, 12:959-969.
37. Jin Y., Jorgensen E., Hartwieg E., Horvitz H.R. The Caenorhabditis elegans gene unc-25 encodes glutamic acid decarboxylase and is required for synaptic transmission but not synaptic development. J.Neurosci. 1999, 19:539-548.
38. Johnson K.G., Ghose A., Epstein E., Lincecum J., O'Connor M.B., Van Vactor D. Axonal heparan sulfate proteoglycans regulate the distribution and efficiency of the repellent slit during midline axon guidance. Curr. Biol. 2004, 14:499-504.
39. Kamath R.S., Fraser A.G., Dong Y., Poulin G., Durbin R., Gotta M., Kanapin A., Le Bot N., Moreno S., Sohrmann M., et al. Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 2003, 421:231-237.
40. Kerschensteiner M., Schwab M.E., Lichtman J.W., Misgeld T. Invivo imaging of axonal degeneration and regeneration in the injured spinal cord. Nat. Med. 2005, 11:572-577.
41. Kim C.W., Goldberger O.A., Gallo R.L., Bernfield M. Members of the syndecan family of heparan sulfate proteoglycans are expressed in distinct cell-, tissue-, and development-specific patterns. Mol. Biol. Cell 1994, 5:797-805.
42. Kinnunen T., Kaksonen M., Saarinen J., Kalkkinen N., Peng H.B., Rauvala H. Cortactin-Src kinase signaling pathway is involved in N-syndecan-dependent neurite outgrowth. J.Biol. Chem. 1998, 273:10702-10708.
43. Kitagawa H., Egusa N., Tamura J.I., Kusche-Gullberg M., Lindahl U., Sugahara K. rib-2, a Caenorhabditis elegans homolog of the human tumor suppressor EXT genes encodes a novel α1,4-N-acetylglucosaminyltransferase involved in the biosynthetic initiation and elongation of heparan sulfate. J.Biol. Chem. 2001, 276:4834-4838.
44. Knobel K.M., Jorgensen E.M., Bastiani M.J. Growth cones stall and collapse during axon outgrowth in Caenorhabditis elegans. Development 1999, 126:4489-4498.
45. Kramer K.L., Yost H.J. Heparan sulfate core proteins in cell-cell signaling. Annu. Rev. Genet. 2003, 37:461-484.
46. Lee J.-S., Chien C.-B. When sugars guide axons: insights from heparan sulphate proteoglycan mutants. Nat. Rev. Genet. 2004, 5:923-935.
47. McIntire S.L., Reimer R.J., Schuske K., Edwards R.H., Jorgensen E.M. Identification and characterization of the vesicular GABA transporter. Nature 1997, 389:870-876.
48. Minniti A.N., Labarca M., Hurtado C., Brandan E. Caenorhabditis elegans syndecan (SDN-1) is required for normal egg laying and associates with the nervous system and the vulva. J.Cell Sci. 2004, 117:5179-5190.
49. Mizuguchi S., Uyama T., Kitagawa H., Nomura K.H., Dejima K., Gengyo-Ando K., Mitani S., Sugahara K., Nomura K. Chondroitin proteoglycans are involved in cell division of Caenorhabditis elegans. Nature 2003, 423:443-448.
50. Morgan M.R., Humphries M.J., Bass M.D. Synergistic control of cell adhesion by integrins and syndecans. Nat. Rev. Mol. Cell Biol. 2007, 8:957-969.
51. Morio H., Honda Y., Toyoda H., Nakajima M., Kurosawa H., Shirasawa T. EXT gene family member rib-2 is essential for embryonic development and heparan sulfate biosynthesis in Caenorhabditis elegans. Biochem. Biophys. Res. Commun. 2003, 301:317-323.
52. Murakami K., Yoshida S. Nerve injury induces the expression of syndecan-1 heparan sulfate proteoglycan in peripheral motor neurons. Neurosci. Lett. 2012, 527:28-33.
53. Murakami K., Namikawa K., Shimizu T., Shirasawa T., Yoshida S., Kiyama H. Nerve injury induces the expression of EXT2, a glycosyltransferase required for heparan sulfate synthesis. Neuroscience 2006, 141:1961-1969.
54. Nix P., Hammarlund M., Hauth L., Lachnit M., Jorgensen E.M., Bastiani M. Axon regeneration genes identified by RNAi screening in C.elegans. J.Neurosci. 2014, 34:629-645.
55. Pan Y.A., Misgeld T., Lichtman J.W., Sanes J.R. Effects of neurotoxic and neuroprotective agents on peripheral nerve regeneration assayed by time-lapse imaging invivo. J.Neurosci. 2003, 23:11479-11488.
56. Properzi F., Lin R., Kwok J., Naidu M., van Kuppevelt T.H., Ten Dam G.B., Camargo L.M., Raha-Chowdhury R., Furukawa Y., Mikami T., et al. Heparan sulphate proteoglycans in glia and in the normal and injured CNS: expression of sulphotransferases and changes in sulphation. Eur. J. Neurosci. 2008, 27:593-604.
57. Rapraeger A., Jalkanen M., Endo E., Koda J., Bernfield M. The cell surface proteoglycan from mouse mammary epithelial cells bears chondroitin sulfate and heparan sulfate glycosaminoglycans. J.Biol. Chem. 1985, 260:11046-11052.
58. Rautava J., Soukka T., Heikinheimo K., Miettinen P.J., Happonen R.-P., Jaakkola P. Different mechanisms of syndecan-1 activation through a fibroblast-growth-factor-inducible response element (FiRE) in mucosal and cutaneous wounds. J.Dent. Res. 2003, 82:382-387.
59. Rhiner C., Gysi S., Fröhli E., Hengartner M.O., Hajnal A. Syndecan regulates cell migration and axon guidance in C.elegans. Development 2005, 132:4621-4633.
60. Saoncella S., Echtermeyer F., Denhez F., Nowlen J.K., Mosher D.F., Robinson S.D., Hynes R.O., Goetinck P.F. Syndecan-4 signals cooperatively with integrins in a Rho-dependent manner in the assembly of focal adhesions and actin stress fibers. Proc. Natl. Acad. Sci. USA 1999, 96:2805-2810.
61. Schlessinger J., Plotnikov A.N., Ibrahimi O.A., Eliseenkova A.V., Yeh B.K., Yayon A., Linhardt R.J., Mohammadi M. Crystal structure of a ternary FGF-FGFR-heparin complex reveals a dual role for heparin in FGFR binding and dimerization. Mol. Cell 2000, 6:743-750.
62. Schwabiuk M., Coudiere L., Merz D.C. SDN-1/syndecan regulates growth factor signaling in distal tip cell migrations in C.elegans. Dev. Biol. 2009, 334:235-242.
63. Shworak N.W., Shirakawa M., Mulligan R.C., Rosenberg R.D. Characterization of ryudocan glycosaminoglycan acceptor sites. J.Biol. Chem. 1994, 269:21204-21214.
64. Soussi-Yanicostas N., Hardelin J.P., Arroyo-Jimenez M.M., Ardouin O., Legouis R., Levilliers J., Traincard F., Betton J.M., Cabanié L., Petit C. Initial characterization of anosmin-1, a putative extracellular matrix protein synthesized by definite neuronal cell populations in the central nervous system. J.Cell Sci. 1996, 109:1749-1757.
65. Soussi-Yanicostas N., Faivre-Sarrailh C., Hardelin J.P., Levilliers J., Rougon G., Petit C. Anosmin-1 underlying the X chromosome-linked Kallmann syndrome is an adhesion molecule that can modulate neurite growth in a cell-type specific manner. J.Cell Sci. 1998, 111:2953-2965.
66. Soussi-Yanicostas N., de Castro F., Julliard A.K., Perfettini I., Chédotal A., Petit C. Anosmin-1, defective in the X-linked form of Kallmann syndrome, promotes axonal branch formation from olfactory bulb output neurons. Cell 2002, 109:217-228.
67. Steigemann P., Molitor A., Fellert S., Jäckle H., Vorbrüggen G. Heparan sulfate proteoglycan syndecan promotes axonal and myotube guidance by slit/robo signaling. Curr. Biol. 2004, 14:225-230.
68. Stepp M.A., Gibson H.E., Gala P.H., Iglesia D.D.S., Pajoohesh-Ganji A., Pal-Ghosh S., Brown M., Aquino C., Schwartz A.M., Goldberger O., et al. Defects in keratinocyte activation during wound healing in the syndecan-1-deficient mouse. J.Cell Sci. 2002, 115:4517-4531.
69. Timmons L., Court D.L., Fire A. Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene 2001, 263:103-112.
70. Townley R.A., Bülow H.E. Genetic analysis of the heparan modification network in Caenorhabditis elegans. J.Biol. Chem. 2011, 286:16824-16831.
71. Van Vactor D., Wall D.P., Johnson K.G. Heparan sulfate proteoglycans and the emergence of neuronal connectivity. Curr. Opin. Neurobiol. 2006, 16:40-51.
72. Vitriol E.A., Zheng J.Q. Growth cone travel in space and time: the cellular ensemble of cytoskeleton, adhesion, and membrane. Neuron 2012, 73:1068-1081.
73. Woods A., Couchman J.R., Johansson S., Höök M. Adhesion and cytoskeletal organisation of fibroblasts in response to fibronectin fragments. EMBO J. 1986, 5:665-670.
74. Yamada S., Van Die I., Van den Eijnden D.H., Yokota A., Kitagawa H., Sugahara K. Demonstration of glycosaminoglycans in Caenorhabditis elegans. FEBS Lett. 1999, 459:327-331.
75. Yayon A., Klagsbrun M., Esko J.D., Leder P., Ornitz D.M. Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor. Cell 1991, 64:841-848.
76. Ylera B., Ertürk A., Hellal F., Nadrigny F., Hurtado A., Tahirovic S., Oudega M., Kirchhoff F., Bradke F. Chronically CNS-injured adult sensory neurons gain regenerative competence upon a lesion of their peripheral axon. Curr. Biol. 2009, 19:930-936.
77. Yoneda A., Couchman J.R. Regulation of cytoskeletal organization by syndecan transmembrane proteoglycans. Matrix Biol. 2003, 22:25-33.