Neu3 sialidase-mediated ganglioside conversion is necessary for axon regeneration and is blocked in CNS axons

Journal of Neuroscience

Volumn 34, Issue 7, 2014, Pages 2477-2492

  Kappagantula, Sunil ^a   Andrews, Melissa R ^a,b   Cheah, Menghon ^a   Abad Rodriguez, José ^c   Dotti, Carlos G ^d   Fawcett, James W ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF ST ANDREWS   (United Kingdom)

^c HOSPITAL NACIONAL DE PARAPLÉJICOS   (Spain)

^d CENTRO DE BIOLOGÍA MOLECULAR SEVERO OCHOA   (Spain)

Author keywords

Axon regeneration; Axotomy; Gangliosides; Neu3 sialidase

Indexed keywords

AXON REGENERATION; AXOTOMY; GANGLIOSIDES; NEU3 SIALIDASE;

ANIMALS; AXONS; AXOTOMY; ENZYME ACTIVATION; GANGLIOSIDES; IMMUNOHISTOCHEMISTRY; MALE; NERVE REGENERATION; NEURAMINIDASE; RATS; RATS, SPRAGUE-DAWLEY; RETINAL NEURONS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; SENSORY RECEPTOR CELLS; SIGNAL TRANSDUCTION; TRANSFECTION;

EID: 84893665187     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4432-13.2014     Document Type: Article

References (86)

1. Abad-Rodriguez J, Robotti A (2007) Regulation of axonal development by plasma membrane gangliosides. J Neurochem 103:47-55. CrossRef Medline
2. Abe N, Borson SH, Gambello MJ, Wang F, Cavalli V (2010) Mammalian target of rapamycin (m TOR) activation increases axonal growth capacity of injured peripheral nerves. J Biol Chem 285:28034-28043. CrossRef Medline
3. Afshari FT, Kappagantula S, Fawcett JW (2009) Extrinsic and intrinsic factors controlling axonal regeneration after spinal cord injury. Expert Rev Mol Med 11:e37. CrossRef Medline
4. Agthong S, Koonam J, Kaewsema A, Chentanez V (2009) Inhibition of MAPK ERK impairs axonal regeneration without an effect on neuronal loss after nerve injury. Neurol Res 31:1068-1074. CrossRef Medline
5. Agthong S, Kaewsema A, Chentanez V (2012) Inhibition of P38 MAPK reduces loss of primary sensory neurons after nerve transection. Neurol Res 34:714-720. CrossRef Medline
6. Bähr M, Vanselow J, Thanos S (1989) Ability of adult rat ganglion cells to regrow axons in vitro can be influenced by fibroblast growth factor and gangliosides. Neurosci Lett 96:197-201. CrossRef Medline
7. Bradke F, Dotti CG (1999) The role of local actin instability in axon formation. Science 283:1931-1934. CrossRef Medline
8. Bradke F, Fawcett JW, Spira ME (2012) Assembly of a new growth cone after axotomy: the precursor to axon regeneration. Nat Rev Neurosci 13:183-193. CrossRef Medline
9. Chew DJ, Fawcett JW, Andrews MR (2012) The challenges of long-distance axon regeneration in the injured CNS. Prog Brain Res 201:253-294. CrossRef Medline
10. Chierzi S, Ratto GM, Verma P, Fawcett JW (2005) The ability of axons to regenerate their growth cones depends on axonal type and age, and is regulated by calcium, c AMP and ERK. Eur J Neurosci 21:2051-2062. CrossRef Medline
11. Cho Y, Cavalli V (2012) HDAC5is a novel injury-regulated tubulin deacetylase controlling axon regeneration. EMBO J 31:3063-3078. CrossRef Medline
12. Cho Y, Sloutsky R, Naegle KM, Cavalli V (2013) Injury-induced HDAC5 nuclear export is essential for axon regeneration. J Neurosci 155:894-908. CrossRef
13. Collins BE, Yang LJ, Mukhopadhyay G, Filbin MT, Kiso M, Hasegawa A, Schnaar RL (1997) Sialic acid specificity of myelin-associated glycoprotein binding. J Biol Chem 272:1248-1255. CrossRef Medline
14. Coulthard LR, White DE, Jones DL, McDermott MF, Burchill SA (2009) P38(MAPK): stress responses from molecular mechanisms to therapeutics. Trends Mol Med 15:369-379. CrossRef Medline
15. Cuello AC, Garofalo L, Liberini P, Maysinger D (1994) Cooperative effects of gangliosides on trophic factor-induced neuronal cell recovery and synaptogenesis: studies in rodents and subhuman primates. Prog Brain Res 101:337-355. CrossRef Medline
16. Da Silva JS, Hasegawa T, Miyagi T, Dotti CG, Abad-Rodriguez J (2005) Asymmetric membrane ganglioside sialidase activity specifies axonal fate. Nat Neurosci 8:606-615. CrossRef Medline
17. Erez H, Malkinson G, Prager-Khoutorsky M, De Zeeuw CI, Hoogenraad CC, Spira ME (2007) Formation of microtubule-based traps controls the sorting and concentration of vesicles to restricted sites of regenerating neurons after axotomy. J Cell Biol 176:497-507. CrossRef Medline
18. Ertürk A, Hellal F, Enes J, Bradke F (2007) Disorganized microtubules underlie the formation of retraction bulbs and the failure of axonal regeneration. J Neurosci 27:9169-9180. CrossRef Medline
19. Facci L, Leon A, Toffano G, Sonnino S, Ghidoni R, Tettamanti G (1984) Promotion of neuritogenesis in mouse neuroblastoma cells by exogenous gangliosides: relationship between the effect and the cell association of ganglioside GM1. J Neurochem 42:299-305. CrossRef Medline
20. Furukawa K, Ohmi Y, Ohkawa Y, Tokuda N, Kondo Y, Tajima O, Furukawa K (2011) Regulatory mechanisms of nervous systems with glycosphingolipids. Neurochem Res 36:1578-1586. CrossRef Medline
21. Gao X, Lowry PR, Zhou X, Depry C, Wei Z, Wong GW, Zhang J (2011) PI3K/Akt signaling requires spatial compartmentalization in plasma membrane microdomains. Proc Natl Acad Sci U S A 108:14509-14514. CrossRef Medline
22. Geisler FH, Coleman WP, Grieco G, Poonian D (2001) The Sygen multicenter acute spinal cord injury study. Spine 26:S87-S98. CrossRef Medline
23. Grider MH, Park D, Spencer DM, Shine HD (2009) Lipid raft-targeted Akt promotes axonal branching and growth cone expansion via m TOR and Rac1, respectively. J Neurosci Res 87:3033-3042. CrossRef Medline
24. Guirland C, Zheng JQ (2007) Membrane lipid rafts and their role in axon guidance. Adv Exp Med Biol 621:144-155. CrossRef Medline
25. Guirland C, Suzuki S, Kojima M, Lu B, Zheng JQ (2004) Lipid rafts mediate chemotropic guidance of nerve growth cones. Neuron 42:51-62. CrossRef Medline
26. Hanz S, Perlson E, Willis D, Zheng JQ, Massarwa R, Huerta JJ, Koltzenburg M, Kohler M, van-Minnen J, Twiss JL, Fainzilber M (2003) Axoplasmic importins enable retrograde injury signaling in lesioned nerve. Neuron 40:1095-1104. CrossRef Medline
27. Ichikawa N, Iwabuchi K, Kurihara H, Ishii K, Kobayashi T, Sasaki T, Hattori N, Mizuno Y, Hozumi K, Yamada Y, Arikawa-Hirasawa E (2009) Binding of laminin-1 to monosialoganglioside GM1 in lipid rafts is crucial for neurite outgrowth. J Cell Sci 122:289-299. CrossRef Medline
28. Jung H, Yoon BC, Holt CE (2012) Axonal m RNA localization and local protein synthesis in nervous system assembly, maintenance and repair. Nat Rev Neurosci 13:308-324. CrossRef Medline
29. Kalka D, von Reitzenstein C, Kopitz J, Cantz M (2001) The plasma membrane ganglioside sialidase cofractionates with markers of lipid rafts. Biochem Biophys Res Commun 283:989-993. CrossRef Medline
30. Kamber D, Erez H, Spira ME (2009) Local calcium-dependent mechanisms determine whether a cut axonal end assembles a retarded endbulb or competent growth cone. Exp Neurol 219:112-125. CrossRef Medline
31. Kamiguchi H (2006) The region-specific activities of lipid rafts during axon growth and guidance. J Neurochem 98:330-335. CrossRef Medline
32. Kato K, Shiga K, Yamaguchi K, Hata K, Kobayashi T, Miyazaki K, Saijo S, Miyagi T (2006) Plasma-membrane-associated sialidase (Neu3) differentially regulates integrin-mediated cell proliferation through lamininand fibronectin-derived signalling. Biochem J 394:647-656. CrossRef Medline
33. Kato N, Matsumoto M, Kogawa M, Atkins GJ, Findlay DM, Fujikawa T, Oda H, Ogata M (2013) Critical role of P38 MAPK for regeneration of the sciatic nerve following crush injury in vivo. J Neuroinflammation 10:1. CrossRef Medline
34. Katoh-Semba R, Kaneko R, Kitajima S, Tsuzuki M, Ichisaka S, Hata Y, Yamada H, Miyazaki N, Takahashi Y, Kato K (2009) Activation of P38 mitogen-activated protein kinase is required for in vivo brain-derived neurotrophic factor production in the rat hippocampus. Neuroscience 163:352-361. CrossRef Medline
35. Kilic E, El Ali A, Kilic U, Guo Z, Ugur M, Uslu U, Bassetti CL, Schwab ME, Hermann DM (2010) Role of Nogo-A in neuronal survival in the reperfused ischemic brain. J Cereb Blood Flow Metab 30:969-984. CrossRef Medline
36. Kittaka D, Itoh M, Ohmi Y, Kondo Y, Fukumoto S, Urano T, Tajima O, Furukawa K (2008) Impaired hypoglossal nerve regeneration in mutant mice lacking complex gangliosides: down-regulation of neurotrophic factors and receptors as possible mechanisms. Glycobiology 18:509-516. CrossRef Medline
37. Kopitz J, von Reitzenstein C, Sinz K, Cantz M (1996) Selective ganglioside desialylation in the plasma membrane of human neuroblastoma cells. Glycobiology 6:367-376. CrossRef Medline
38. Lehmann HC, Lopez PH, Zhang G, Ngyuen T, Zhang J, Kieseier BC, Mori S, Sheikh KA (2007) Passive immunization with anti-ganglioside antibodies directly inhibits axon regeneration in an animal model. J Neurosci 27:27-34. CrossRef Medline
39. Liu RY, Snider WD (2001) Different signaling pathways mediate regenerative versus developmental sensory axon growth. J Neurosci 21:RC164. Medline
40. Long KE, Lemmon V (2000) Dynamic regulation of cell adhesion molecules during axon outgrowth. J Neurobiol 44:230-245. CrossRef Medline
41. Lopez PH, Zhang G, Zhang J, Lehmann HC, Griffin JW, Schnaar RL, Sheikh KA (2010) Passive transfer of Ig G anti-GM1 antibodies impairs peripheral nerve repair. J Neurosci 30:9533-9541. CrossRef Medline
42. Mandolesi G, Madeddu F, Bozzi Y, Maffei L, Ratto GM (2004) Acute physiological response of mammalian central neurons to axotomy: ionic regulation and electrical activity. FASEB J 18:1934-1936. CrossRef Medline
43. Mei S, Gu H, Ward A, Yang X, Guo H, He K, Liu Z, Cao W (2012) P38 mitogen-activated kinase (MAPK) promotes cholesterol ester formation accumulation in macrophages through inhibition of macroautophagy. J Biol Chem 15:11761-11768. CrossRef Medline
44. Miyagi T, Wada T, Iwamatsu A, Hata K, Yoshikawa Y, Tokuyama S, Sawada M (1999) Molecular cloning and characterization of a plasma membrane-associated sialidase specific for gangliosides. J Biol Chem 274: 5004-5011. CrossRef Medline
45. Miyagi T, Wada T, Yamaguchi K (2008a) Roles of plasma membraneassociated sialidase Neu3 in human cancers. Biochim Biophys Acta 1780: 532-537. CrossRef Medline
46. Miyagi T, Wada T, Yamaguchi K, Hata K, Shiozaki K (2008b) Plasma membrane-associated sialidase as a crucial regulator of transmembrane signalling. J Biochem 144:279-285. CrossRef Medline
47. Miyata M, Kambe M, Tajima O, Moriya S, Sawaki H, Hotta H, Kondo Y, Narimatsu H, Miyagi T, Furukawa K, Furukawa K (2011) Membrane sialidase Neu3 is highly expressed in human melanoma cells promoting cell growth with minimal changes in the composition of gangliosides. Cancer Sci 102:2139-2149. CrossRef Medline
48. Monti E, Miyagi T (2012) Structure and function of mammalian sialidases. Top Curr Chem. Advance online publication. Retrieved May 26, 2012. doi: 10.1007/128_2012_328. CrossRef Medline
49. Moore DL, Goldberg JL (2011) Multiple transcription factor families regulate axon growth and regeneration. Dev Neurobiol 71:1186-1211. CrossRef Medline
50. Mountney A, Zahner MR, Lorenzini I, Oudega M, Schramm LP, Schnaar RL (2010) Sialidase enhances recovery from spinal cord contusion injury. Proc Natl Acad Sci U S A 107:11561-11566. CrossRef Medline
51. Mountney A, Zahner MR, Sturgill ER, Riley CJ, Aston JW, Oudega M, Schramm LP, Hurtado A, Schnaar RL (2013) Sialidase, chondroitinase ABC, and combination therapy after spinal cord contusion injury. J Neurotrauma 30:181-190. CrossRef Medline
52. Myers RR, Sekiguchi Y, Kikuchi S, Scott B, Medicherla S, Protter A, Campana WM (2003) Inhibition of P38 MAP kinase activity enhances axonal regeneration. Exp Neurol 184:606-614. CrossRef Medline
53. Neumann H, Schweigreiter R, Yamashita T, Rosenkranz K, Wekerle H, Barde YA (2002) Tumor necrosis factor inhibits neurite outgrowth and branching of hippocampal neurons by a ρ-dependent mechanism. J Neurosci 22:854-862. Medline
54. Nix P, Hisamoto N, Matsumoto K, Bastiani M (2011) Axon regeneration requires coordinate activation of P38 and JNK MAPK pathways. Proc Natl Acad Sci U S A 108:10738-10743. CrossRef Medline
55. Norambuena A, Schwartz MA (2011) Effects of integrin-mediated cell adhesion on plasma membrane lipid raft components and signaling. Mol Biol Cell 22:3456-3464. CrossRef Medline
56. Nozaki K, Nishimura M, Hashimoto N (2001) Mitogen-activated protein kinases and cerebral ischemia. Mol Neurobiol 23:1-19. CrossRef Medline
57. Oehler C, Kopitz J, Cantz M (2002) Substrate specificity and inhibitor studies of a membrane-bound ganglioside sialidase isolated from human brain tissue. Biol Chem 383:1735-1742. CrossRef Medline
58. Ohkawa Y, Miyazaki S, Hamamura K, Kambe M, Miyata M, Tajima O, Ohmi Y, Yamauchi Y, Furukawa K, Furukawa K (2010) Ganglioside GD3 enhances adhesion signals and augments malignant properties of melanoma cells by recruiting integrins to glycolipid-enriched microdomains. J Biol Chem 285:27213-27223. CrossRef Medline
59. Okada M, Itoh Mi M, Haraguchi M, Okajima T, Inoue M, Oishi H, Matsuda Y, Iwamoto T, Kawano T, Fukumoto S, Miyazaki H, Furukawa K, Aizawa S, Furukawa K (2002) b-Series ganglioside deficiency exhibits no definite changes in the neurogenesis and the sensitivity to Fas-mediated apoptosis but impairs regeneration of the lesioned hypoglossal nerve. J Biol Chem 277:1633-1636. CrossRef Medline
60. 2+ mobilisation and stress kinases in cultured sensory neurones. Neuropharmacology 42:93-106. CrossRef Medline
61. Rabin SJ, Mocchetti I (1995) GM1 ganglioside activates the high-affinity nerve growth factor receptor trk A. J Neurochem 65:347-354. CrossRef Medline
62. Rabin SJ, Bachis A, Mocchetti I (2002) Gangliosides activate Trk receptors by inducing the release of neurotrophins. J Biol Chem 277:49466-49472. CrossRef Medline
63. Roche PH, Figarella-Branger D, Daniel L, Bianco N, Pellet W, Pellissier JF (1997) Expression of cell adhesion molecules in normal nerves, chronic axonal neuropathies and Schwann cell tumors. J Neurol Sci 151:127-133. CrossRef Medline
64. Rodriguez JA, Piddini E, Hasegawa T, Miyagi T, Dotti CG (2001) Plasma membrane ganglioside sialidase regulates axonal growth and regeneration in hippocampal neurons in culture. J Neurosci 21:8387-8395. Medline
65. Sheikh KA, Sun J, Liu Y, Kawai H, Crawford TO, Proia RL, Griffin JW, Schnaar RL (1999) Mice lacking complex gangliosides develop Wallerian degeneration and myelination defects. Proc Natl Acad Sci U S A 96:7532-7537. CrossRef Medline
66. Singh RD, Marks DL, Holicky EL, Wheatley CL, Kaptzan T, Sato SB, Kobayashi T, Ling K, Pagano RE (2010) Gangliosides and beta1-integrin are required for caveolae and membrane domains. Traffic 11:348-360. CrossRef Medline
67. Skaper SD, Katoh-Semba R, Varon S (1985) GM1 ganglioside accelerates neurite outgrowth from primary peripheral and central neurons under selected culture conditions. Brain Res 355:19-26. Medline
68. Spira ME, Oren R, Dormann A, Gitler D (2003) Critical calpain-dependent ultrastructural alterations underlie the transformation of an axonal segment into a growth cone after axotomy of cultured Aplysia neurons. J Comp Neurol 457:293-312. CrossRef Medline
69. Stuermer CA (2010) The reggie/flotillin connection to growth. Trends Cell Biol 20:6-13. CrossRef Medline
70. Sun F, He Z (2010) Neuronal intrinsic barriers for axon regeneration in the adult CNS. Curr Opin Neurobiol 20:510-518. CrossRef Medline
71. Tringali C, Lupo B, Silvestri I, Papini N, Anastasia L, Tettamanti G, Venerando B (2012) The plasma membrane sialidase Neu3 regulates the malignancy of renal carcinoma cells by controlling β1 integrin internalization and recycling. J Biol Chem 287:42835-42845. CrossRef Medline
72. Verma P, Chierzi S, Codd AM, Campbell DS, Meyer RL, Holt CE, Fawcett JW (2005) Axonal protein synthesis and degradation are necessary for efficient growth cone regeneration. J Neurosci 25:331-342. CrossRef Medline
73. Vogelaar CF, Gervasi NM, Gumy LF, Story DJ, Raha-Chowdhury R, Leung KM, Holt CE, Fawcett JW (2009) Axonal m RNAs: characterisation and role in the growth and regeneration of dorsal root ganglion axons and growth cones. Mol Cell Neurosci 42:102-115. CrossRef Medline
74. Vyas AA, Patel HV, Fromholt SE, Heffer-Lauc M, Vyas KA, Dang J, Schachner M, Schnaar RL (2002) Gangliosides are functional nerve cell ligands for myelin-associated glycoprotein (MAG), an inhibitor of nerve regeneration. Proc Natl Acad Sci U S A 99:8412-8417. CrossRef Medline
75. Waetzig V, Herdegen T (2005) MEKK1 controls neurite regrowth after experimental injury by balancing ERK1/2 and JNK2 signaling. Mol Cell Neurosci 30:67-78. CrossRef Medline
76. Wang Z, Jin Y (2011) Genetic dissection of axon regeneration. Curr Opin Neurobiol 21:189-196. CrossRef Medline
77. Williams G, Wood A, Williams EJ, Gao Y, Mercado ML, Katz A, Joseph-McCarthy D, Bates B, Ling HP, Aulabaugh A, Zaccardi J, Xie Y, Pangalos MN, Walsh FS, Doherty P (2008) Ganglioside inhibition of neurite outgrowth requires Nogo receptor function: identification of interaction sites and development of novel antagonists. J Biol Chem 283:16641-16652. CrossRef Medline
78. Willis D, Li KW, Zheng JQ, Chang JH, Smit AB, Kelly T, Merianda TT, Sylvester J, van Minnen J, Twiss JL (2005) Differential transport and local translation of cytoskeletal, injury-response, and neurodegeneration protein m RNAs in axons. J Neurosci 25:778-791. CrossRef Medline
79. Witte H, Neukirchen D, Bradke F (2008) Microtubule stabilization specifies initial neuronal polarization. J Cell Biol 180:619-632. CrossRef Medline
80. Wu G, Lu ZH, Obukhov AG, Nowycky MC, Ledeen RW (2007) Induction of calcium influx through TRPC5 channels by cross-linking of GM1 ganglioside associated with alpha5beta1 integrin initiates neurite outgrowth. J Neurosci 27:7447-7458. CrossRef Medline
81. Yamaguchi K, Hata K, Wada T, Moriya S, Miyagi T (2006) Epidermal growth factor-induced mobilization of a ganglioside-specific sialidase (Neu3) to membrane ruffles. Biochem Biophys Res Commun 346:484-490. CrossRef Medline
82. Yang LJ, Lorenzini I, Vajn K, Mountney A, Schramm LP, Schnaar RL (2006) Sialidase enhances spinal axon outgrowth in vivo. Proc Natl Acad Sci U S A 103:11057-11062. CrossRef Medline
83. Yoo S, van Niekerk EA, Merianda TT, Twiss JL (2010) Dynamics of axonal m RNA transport and implications for peripheral nerve regeneration. Exp Neurol 223:19-27. CrossRef Medline
84. Zhang G, Lehmann HC, Manoharan S, Hashmi M, Shim S, Ming GL, Schnaar RL, Lopez PH, Bogdanova N, Sheikh KA (2011) Anti-ganglioside antibody-mediated activation of Rho A induces inhibition of neurite outgrowth. J Neurosci 31:1664-1675. CrossRef Medline
85. Zheng JQ, Kelly TK, Chang B, Ryazantsev S, Rajasekaran AK, Martin KC, Twiss JL (2001) A functional role for intra-axonal protein synthesis during axonal regeneration from adult sensory neurons. J Neurosci 21:9291-9303. Medline
86. 2+ induce the dedifferentiation of axonal segments into growth cones. J Neurosci 17:3568-3579. Medline