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Ganglioside/protein kinase signals triggering cytoskeletal actin reorganization

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Abstract

Exposure of neuronal cells to nanomolar concentrations of oligosaccharide portions of ganglioside GM2 and GT1b stimulates cAMP-dependent protein kinase (PKA) Ca2+/calmodulin-dependent protein kinase II (CaMKII), respectively, in a few seconds suggesting the presence of glyco-receptor-like molecules on the surface of the cells. Both GM2/PKA (GalNAc/PKA) and GT1b/CaMKII signaling cascades induced cytoskeletal actin reorganization through Cdc42 activation leading to filopodia formation within 2 min. Long-term effects of these glyco-signals were facilitation of dendritic differentiation of primary cultured hippocampal neurons and cerebellar Purkinje neurons indicating physiological roles of the signals in neuronal differentiation and maturation. Published in 2004.

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References

  1. Hakomori S, Igarashi Y, Functional role of glycosphingolipids in cell recognition and signaling, J Biochem 118, 1091–103 (1995).

    PubMed  CAS  Google Scholar 

  2. Basu SC, The serendipity of ganglioside biosynthesis: Pathway to CARS and HY-CARS glycosyltransferases, Glycobiology 1, 469–75 (1991).

    PubMed  CAS  Google Scholar 

  3. Sheikh K, Sun J, Liu Y, Kawai H, Crawford T, Proia R, Griffin J, Schnaar R, Mice lacking complex gangliosides developWallerian degeneration and myelination defects, Proc Natl Acad Sci USA 96, 7532–7 (1999).

    Article  PubMed  CAS  Google Scholar 

  4. Wu G, Xie X, Lu Z-H, Ledeen RW, Cerebellar neurons lacking complex gangliosides degenerate in the presence of depolarizing levels of potassium, Proc Natl Acad Sci USA 98, 307–12 (2001).

    Article  PubMed  CAS  Google Scholar 

  5. Ghosh S, Kyle JW, Dastgheib S, Daussin F, Li Z, Basu S, Purification, properties, and immunological characterization of GalT-3 (UDP-galactose: GM2 ganglioside, β 1-3 galactosyltransferase) from embryonic chicken brain, Glycoconjugate J 12, 838–47 (1995).

    Article  CAS  Google Scholar 

  6. Miyazaki H, Fukumoto S, Okada M, Hasegawa T, Furukawa K, Expression cloning of rat cDNA encoding UDP-galactose: GD2 β 1,3-galactosyltransferase that determines the expression of GD1b/GM1/GA1, J Biol Chem 272, 24794–9 (1997).

    Article  PubMed  CAS  Google Scholar 

  7. Higashi H, Basu M, Basu S, Biosynthesis in vitro of disialosylneolactotetraosylceramide by a solubilized sialyltransferase from embryonic chicken brain, J Biol Chem 260, 824–8 (1985).

    PubMed  CAS  Google Scholar 

  8. Nara K, Watanabe Y, Maruyama K, Kasahara K, Nagai Y, Sanai Y, Expression cloning of a CMP-NeuAc: NeuAc α 2-3Gal β 1-4Glc β 1-1'-Cer α 2,8-sialyltransferase (GD3 synthase) from human melanoma cells, Proc Natl Acad Sci USA 91, 7952–6 (1994).

    Article  PubMed  CAS  Google Scholar 

  9. Kawai H, Allende ML, Wada R, Kono M, Sango K, Deng C, Miyakawa T, Crawley JN, Werth N, Bierfreund U, Sandhoff K, Proia RL, Mice expressing only monosialoganglioside GM3 exhibit lethal audiogenic seizures, J Biol Chem 276, 6885–8 (2001).

    Article  PubMed  CAS  Google Scholar 

  10. Ramirez OA, Gomez RA, Carrer HF, Gangliosides improve synaptic transmission in dentate gyrus of hippocampal rat slices, Brain Res 506, 291–3 (1990).

    Article  PubMed  CAS  Google Scholar 

  11. Hwang HM, Wang JT, Chiu TH, Effects of exogenous GM1 ganglioside on LTP in rat hippocampal slices perfused with different concentrations of calcium, Neurosci Lett 141, 227–30 (1992).

    Article  PubMed  CAS  Google Scholar 

  12. Li YX, Mei ZT, The role of monosialoganglioside GM1 in LTPinduction in rat hippocampal slices, Science in China Series B— Chemistry Life Sciences & Earth Sciences, 37, 581–9 (1994).

    CAS  Google Scholar 

  13. Inokuchi J, Mizutani A, Jimbo M, Usuki S, Yamagishi K, Mochizuki H, Muramoto K, Kobayashi K, Kuroda Y, Iwasaki K, Ohgami Y, Fujiwara M, Up-regulation of ganglioside biosynthesis, functional synapse formation, and memory retention by a synthetic ceramide analog (L-PDMP), Biochem Biophys Res Commun 237, 595–600 (1997).

    Article  PubMed  CAS  Google Scholar 

  14. Furuse H, Waki H, Kaneko K, Fujii S, Miura M, Sasaki H, Ito KI, Kato H, Ando S, Effect of the mono-and tetra-sialogangliosides, GM1 and GQ1b, on long-term potentiation in the CA1 hippocampal neurons of the guinea pig, Exp Brain Res 123, 307–14 (1998).

    Article  PubMed  CAS  Google Scholar 

  15. Mutoh T, Tokuda A, Miyadai T, Hamaguchi M, Fujiki N, Ganglioside GM1 binds to the Trk protein and regulates receptor function, Proc Natl Acad Sci USA 92, 5087–91 (1995).

    Article  PubMed  CAS  Google Scholar 

  16. Li R, Liu Y, Ladisch S, Enhancement of epidermal growth factor signaling and activation of SRC kinase by gangliosides, J Biol Chem 276, 42782–92 (2001).

    Article  PubMed  CAS  Google Scholar 

  17. Miljan EA, Meuillet EJ, Mania-Farnell B, George D, Yamamoto H, Simon HG, Bremer EG, Interaction of the extracellular domain of the epidermal growth factor receptor with gangliosides, J Biol Chem 277, 10108–13 (2002).

    Article  PubMed  CAS  Google Scholar 

  18. Goldenring JR, Otis LC, Yu RK, DeLorenzo RJ, Calcium ganglioside-dependent protein kinase activity in rat brain membrane, J Neurochem 44, 1229-34 (1985)

    PubMed  CAS  Google Scholar 

  19. Tsuji S, Nakajima J, Sasaki T, Nagai Y, Bioactive gangliosides. IV. Ganglioside GQ1b/Ca2+ dependent protein kinase activity exists in the plasma membrane fraction of neuroblastoma cell line, GOTO, J Biochem 97, 969–72 (1985).

    PubMed  CAS  Google Scholar 

  20. Kreutter D, Kim JY, Goldenring JR, Rasmussen H, Ukomadu C, DeLorenzo RJ, Yu RK, Regulation of protein kinase C activity by gangliosides, J Biol Chem 262, 1633–7 (1987).

    PubMed  CAS  Google Scholar 

  21. Momoi T, Activation of protein kinaseCby gangliosideGM3in the presence of calcium and 12-O-tetradecanoylphorbol-13-acetate, Biochem Biophys Res Commun 138, 865–71 (1986).

    Article  PubMed  CAS  Google Scholar 

  22. Arakane F, Fukunaga k, Satake M, Miyazaki K, Okamura H, Miyamoto E, Stimulation of cyclic adenosine 3',5'-monophosphate-dependent protein kinase with brain gangliosides, Neurochem Intnatl 26, 187–93 (1995).

    Article  CAS  Google Scholar 

  23. Yates AJ, Walters JD, Wood CL, Johnson JD, Ganglioside modulation of cyclic AMP-dependent protein kinase and cyclic nucleotide phosphodiesterase in vitro, J Neurochem 53, 162–7 (1989).

    PubMed  CAS  Google Scholar 

  24. Fukunaga K, Miyamoto E, Soderling TR, Regulation of Ca2+/calmodulin-dependent protein kinase II by brain gangliosides, J Neurochem 54, 102–9 (1990).

    CAS  Google Scholar 

  25. Higashi H, Omori A, Yamagata T, Calmodulin, a gangliosidebinding protein. Binding of gangliosides to calmodulin in the presence of calcium, J Biol Chem 267, 9831–8 (1992).

    PubMed  CAS  Google Scholar 

  26. Higashi H, Yamagata T, Mechanism for ganglioside-mediated modulation of calmodulin-dependent enzyme. Modulation of calmodulin-dependent cyclic nucleotide phosphodiesterase activity through the binding of gangliosides to calmodulin and the enzyme, J Biol Chem 267, 9839–43 (1992).

    PubMed  CAS  Google Scholar 

  27. Roisen F, Bartfeld H, Nagele R, Yorke G, Ganglioside stimulation of axonal sprouting in vitro, Science 214, 577–8 (1981).

    PubMed  CAS  Google Scholar 

  28. Prinetti A, Iwabuchi K, Hakomori S, Glycosphingolipid-enriched signaling domain in mouse neuroblastoma Neuro2a cells. Mechanism of ganglioside-dependent neuritogenesis, J Biol Chem 274, 20916–24 (1999).

    Article  PubMed  CAS  Google Scholar 

  29. Tsuji S, Yamashita T, Nagai Y, A novel, carbohydrate signalmediated cell surface protein phosphorylation: Ganglioside GQ1b stimulates ecto-protein kinase activity on the cell surface of a human neuroblastoma cell line, GOTO, J Biochem 104, 498–503 (1988).

    PubMed  CAS  Google Scholar 

  30. Van Brocklyn JR, Vandenheede JR, Fertel R, Yates AJ, Rampersaud AA, Ganglioside GM1 activates the mitogenactivated protein kinase Erk2 and p70 S6 kinase in U-1242 MG human glioma cells, J Neurochem 69, 116–25 (1997).

    Article  PubMed  CAS  Google Scholar 

  31. Kojima N, Hakomori S, Cell adhesion, spreading and motility of GM3-expressing calls based on glycolipid-glycolipid interaction, J Biol Chem 266, 17552-8 (1991).

    Google Scholar 

  32. Kojima N, Hakomori S, Cell adhesion, spreading, and motility of GM3-expressing cells based on glycolipid-glycolipid interaction, J Biol Chem 266, 17552–8 (1991).

    PubMed  CAS  Google Scholar 

  33. Iwabuchi K, Yamamura S, Prinetti A, Handa K, Hakomori S, GM3-enriched microdomain involved in cell adhesion and signal transduction through carbohydrate-carbohydrate interaction in mouse melanoma B16 cells, J Biol Chem 273, 9130-8 (1998).

    Article  PubMed  CAS  Google Scholar 

  34. Vyas AA, Patel HV, Fromholt SE, Heffer-Lauc M, Vyas KA, Dang J, Schachner M, Schnaar RL, Gangliosides are functional nerve cell ligands for myelin-associated glycoprotein (MAG), an inhibitor of nerve regeneration, Proc Natl Acad Sci USA 99, 8412–7 (2002).

    Article  PubMed  CAS  Google Scholar 

  35. Neumann S, Bradke F, Tessier-Lavigne M, Basbaum AI, Regeneration of sensory axons within the injured spinal cord induced by intraganglionic cAMP elevation, Neuron 34, 885–93 (2002).

    Article  PubMed  CAS  Google Scholar 

  36. Qiu J, Cai D, Dai H, McAtee M, Hoffman PN, Bregman BS, Filbin MT, Spinal axon regeneration induced by elevation of cyclic AMP, Neuron 34, 895–903 (2002).

    Article  PubMed  CAS  Google Scholar 

  37. Kotani M, Kawashima I, Ozawa H, Terashima T, Tai T, Differential distribution of major gangliosides in rat central nervous system detected by specific monoclonal antibodies, Glycobiology 3, 137–46 (1993).

    PubMed  CAS  Google Scholar 

  38. Wu G-Y, Cline HT, Stabilization of dendritic arbor structure in vivo by CaMKII, Science 279, 222–6 (1998).

    Article  PubMed  CAS  Google Scholar 

  39. Higashi H, Sato K, Omori A, Sekiguchi M, Ohtake A, Kudo Y, Imaging of Ca2+/calmodulin-dependent protein kinase II activity in hippocampal neurons, NeuroReport 7, 2695–700 (1996).

    PubMed  CAS  Google Scholar 

  40. Higashi H, Kudo Y, Regulation by gangliosides of calcium/ calmodulin-dependent protein phosphorylation and dephosphorylation in living cells, Glycoconjugate J 12, 554 (1995).

    Google Scholar 

  41. Chen N, Furuya S, Doi H, Hashimoto Y, Kudo Y, Higashi H, Ganglioside/Calmodulin kinase II signal inducing cdc42-mediated neuronal actin-reorganization, Neuroscience 120, 163–76 (2003).

    Article  PubMed  CAS  Google Scholar 

  42. Nobes CD, Hall A, Rho Rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia, Cell 81, 53–62 (1995).

    Article  PubMed  CAS  Google Scholar 

  43. Threadgill R, Bobb K, Ghosh A, Regulation of dendritic growth and remodeling by Rho, Rac, and Cdc42, Neuron 19, 625–34 (1997).

    Article  PubMed  CAS  Google Scholar 

  44. Ruchhoeft ML, Ohnuma S, McNeill L, Holt CE, Harris WA, The neuronal architecture of Xenopus retinal ganglion cells is sculpted by rho-family GTPases in vivo, J Neurosci 19, 8454–63 (1999).

    PubMed  CAS  Google Scholar 

  45. Gao FB, Brenman JE, Jan LY, Jan YN, Genes regulating dendritic outgrowth, branching, and routing in Drosophila, Genes Dev 13, 2549–61 (1999).

    Article  PubMed  CAS  Google Scholar 

  46. Furuya S, Mitoma J, Makino A, Hirabayashi Y, Ceramide and its interconvertible metabolite sphingosine function as indispensable lipid factors involved in survival and dendritic differentiation of cerebellar Purkinje cells, J Neurochem 71, 366–77 (1998).

    Article  PubMed  CAS  Google Scholar 

  47. Furuya S, Tabata T, Mitoma J, Yamada K, Yamasaki M, Makino A, Yamamoto T, Watanabe M, Kano M, Hirabayashi Y, L-Serine and glycine serve as major astroglia-derived trophic factors for cerebellar Purkinje neurons, Proc Natl Acad Sci USA 97, 11528–533 (2000).

    Article  PubMed  CAS  Google Scholar 

  48. Kawashima I, Nagata I, Tai T, Immunocytochemical analysis of gangliosides in rat primary cerebellar cultures using specific monoclonal antibodies, Brain Res 732, 75–86 (1996).

    Article  PubMed  CAS  Google Scholar 

  49. Kotani M, Terashima T, Tai T, Developmental changes of ganglioside expressions in postnatal rat cerebellar cortex, Brain Res 700, 40–58 (1995).

    Article  PubMed  CAS  Google Scholar 

  50. Wu G, Lu Z, Alfinito P, L edeen R, Opioid receptor and calcium channel regulation of adenylyl cyclase, modulated by GM1, in NG108-15 cells: Competitive interactions, Neurosci Res 22, 1281–9 (1997).

    CAS  Google Scholar 

  51. Malenka RC, Synaptic plasticity in the hippocampus: LTP and LTD, Cell 78, 535–8 (1994).

    Article  PubMed  CAS  Google Scholar 

  52. Mukherji S, Soderling TR, Regulation of Ca2+/calmodulindependent protein kinase II by inter-and intrasubunit-catalyzed autophosphorylations, J Biol Chem 269, 13744–7 (1994).

    PubMed  CAS  Google Scholar 

  53. Soderling TR, CaM-kinases: Modulators of synaptic plasticity, Curr Opin Neurobiol 10, 375–80 (2000).

    Article  PubMed  CAS  Google Scholar 

  54. Shen K, Teruel M, Subramanian K, Meyer T, CaMKIIb functions as an F-actin targeting module that localizes CaMKIIa/b heterooligomers to dendritic spines, Neuron 21, 593–606 (1998).

    Article  PubMed  CAS  Google Scholar 

  55. Landis D, Reese T, Cytoplasmic organization in cerebellar dendritic spines, J Cell Biol 97, 1169–78 (1983).

    Article  PubMed  CAS  Google Scholar 

  56. Caceres A, Payne MR, Binder LI, Steward O, Immunocytochemical localization of actin and microtubule-associated protein MAP2 in dendritic spines, Proc Natl Acad Sci USA 80, 1738–42 (1983).

    Article  PubMed  CAS  Google Scholar 

  57. Purpura DP, Suzuki K, Distortion of neuronal geometry and formation of aberrant synapses in neuronal storage disease, Brain Res 116, 1–21 (1976).

    Article  PubMed  CAS  Google Scholar 

  58. Siegel DA, Walkley SU, Growth of ectopic dendrites on cortical pyramidal neurons in neuronal storage diseases correlates with abnormal accumulation of GM2 ganglioside, J Neurochem 62, 1852–62 (1994).

    Article  PubMed  CAS  Google Scholar 

  59. Goodman LA, Walkley SU, Elevated GM2 ganglioside is associated with dendritic proliferation in normal developing neocortex, Dev. Brain Res 93, 162–171 (1996).

    Article  CAS  Google Scholar 

  60. Walkley SU, Siegel DA, Dobrenis K, Zervas M, GM2 ganglioside as a regulator of pyramidal neuron dendritogenesis, Ann NY Acad Sci 845, 188–99 (1998).

    Article  PubMed  CAS  Google Scholar 

  61. Blitzer RD, Wong T, Nouranifar R, Iyengar R, Landau EM, Postsynaptic cAMP pathway gates early LTP in hippocampal CA1 region, Neuron 15, 1403–414 (1995).

    Article  PubMed  CAS  Google Scholar 

  62. Frey U, Huang Y-Y, Kandel ER, Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons, Science 260, 1661–4 (1993).

    PubMed  CAS  Google Scholar 

  63. Nayak A, Zastrow DJ, Lickteig R, Zahniser NR, Bowning MD, Maintenance of late-phase LTP is accompanied by PKAdependent increase inAMPAreceptor synthesis, Nature 394, 680–3 (1998).

    Article  PubMed  CAS  Google Scholar 

  64. Kao HT, Song HJ, Porton B, Ming GL, Hoh J, Abraham M, Czernik AJ, Pieribone VA, Poo MM, Greengard P, A protein kinase Adependent molecular switch in synapsins regulates neurite outgrowth, Nat Neurosci 5, 431–7 (2002).

    PubMed  CAS  Google Scholar 

  65. Higashi H, Sato K, Ohtake A, Omori A, Yoshida S, Kudo Y, Imaging of cAMP-dependent protein kinase activity in living neural cells using a novel fluorescent substrate, FEBS Lett 414, 55–60 (1997).

    Article  PubMed  CAS  Google Scholar 

  66. Higashi H, Sato K, Ohtake A, Omori A, Yoshida S, Kudo Y, Nagai Y, Saccharide specificity and mechanism for glycoconjugatemediated activation of cyclic AMP-dependent protein kinase in neural cells, Glycoconjugate J 14, S10 (1997).

    Google Scholar 

  67. Chen N, Furuya S, Shinoda Y, Yumoto M, Ohtake A, Sato K, Doi H, Hashimoto Y, Kudo Y, Higashi H, Extracellular carbohydratesignal triggering cAMP-dependent protein kinase-dependent neuronal actin-reorganization, Neuroscience 122, 985–95 (2003).

    Article  PubMed  CAS  Google Scholar 

  68. Higashi H, Chen N, Hashimoto Y, Neuronal actin-spike formation under local PKA activation by glyco-signal through cell-surface N-acetylgalactosamine receptor, J Neurochem 78, 34 (2001).

    Google Scholar 

  69. Sanes J, Cheney J, Lectin binding reveals a synapse-specific carbohydrate in skeletal muscle, Nature 300, 646–7 (1982).

    Article  PubMed  CAS  Google Scholar 

  70. Scott L, Bacou F, Sanes J, A synapse-specific carbohydrate at the neuromuscular junction: Association with both acetylcholinesterase and a glycolipid, J Neurosci 8, 932–44 (1988).

    PubMed  CAS  Google Scholar 

  71. Inoue A, Sanes J, Lamina-specific connectivity in the brain: Regulation by N-cadherin, neurotrophins, and glycoconjugates, Science 276, 1428–31 (1997).

    Article  PubMed  CAS  Google Scholar 

  72. Vijayaraghavan S, Goueli SA, Davey MP, Carr DW, Protein kinase A-anchoring inhibitor peptides arrest mammalian sperm motility, J Biol Chem 272, 4747–52 (1997).

    Article  PubMed  CAS  Google Scholar 

  73. Glantz S, Amat J, Rubin C, cAMP signaling in neurons: Patterns of neuronal expression and intracellular localization for a novel protein, AKAP 150, that anchors the regulatory subunit of cAMP-dependent protein kinase II b, Mol Biol Cell 3, 1215–28 (1992).

    PubMed  CAS  Google Scholar 

  74. Li Y, Ndubuka C, Rubin C, A kinase anchor protein 75 targets regulatory (RII) subunits of cAMP-dependent protein kinase II to the cortical actin cytoskeleton in non-neuronal cells, J Biol Chem 271, 16862–9 (1996).

    Article  PubMed  CAS  Google Scholar 

  75. Tsuji S, Arita M, Nagai Y, GQ1b, a bioactive ganglioside that exhibits novel nerve growth factor (NGF)-like activities in the two neuroblastoma cell lines, J Biochem 94, 303–6 (1983).

    PubMed  CAS  Google Scholar 

  76. Wang L, Colella R, Roisen F, Ganglioside GM1 alters neuronal morphology by modulating the association of MAP2 with microtubules and actin filaments, Dev Brain Res 105, 227–39 (1998).

    Article  CAS  Google Scholar 

  77. Simons K, Ikonen E, Functional rafts in cell membranes, Nature 387, 569–72 (1997).

    Article  PubMed  CAS  Google Scholar 

  78. Simons M, Friedrichson T, Schulz JB, Pitto M, Masserini M, Kurzchalia TV, Exogenous administration of gangliosides displaces GPI-anchored proteins from lipid microdomains in living cells, Mol Biol Cell 10, 3187–96 (1999).

    PubMed  CAS  Google Scholar 

  79. Hakomori S, Yamamura S, Handa AK, Signal transduction through glyco(sphingo)lipids. Introduction and recent studies on glyco(sphingo)lipid-enriched microdomains, Ann NY Acad Sci 845, 1–10 (1998).

    Article  PubMed  CAS  Google Scholar 

  80. Fischer M, Kaech S, Knutti D, Matus A, Rapid actin-based plasticity in dendritic spines, Neuron 20, 847–54 (1998).

    Article  PubMed  CAS  Google Scholar 

  81. Ziv N, Smith S, Evidence for a role of dendritic filopodia in synaptogenesis and spine formation, Neuron 17, 91–102 (1996).

    Article  PubMed  CAS  Google Scholar 

  82. Moshkov DA, Mukhtasimova NF, Pavlik LL, Tiras NR, Pakhotina ID, In vitro long-term potentiation of electrotonic responses of goldfish mauthner cells is accompanied by ultrastructural changes at afferent mixed synapses, Neuroscience 87, 591–605 (1998).

    Article  PubMed  CAS  Google Scholar 

  83. Engert F, Bonhoeffer T, Dendritic spine changes associated with hippocampal long-term synaptic plasticity, Nature 399, 66–70 (1999).

    Article  PubMed  CAS  Google Scholar 

  84. Toni N, Buchs PA, Nikonenko I, Bron CR, Muller D, LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite, Nature 402, 421–5 (1999).

    Article  PubMed  CAS  Google Scholar 

  85. Maletic-Savatic M, Malinow R, Svoboda K, Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity, Science 283, 1923–7 (1999).

    Article  PubMed  CAS  Google Scholar 

  86. Forman D, Ledeen R, Axonal transport of gangliosides in the gold-fish optic nerve, Science 177, 630–3 (1972).

    PubMed  CAS  Google Scholar 

  87. Feoktistov I, Goldstein AE, Biaggioni I, lic AMP and protein inase a stimulate Cdc42: Role ofA2adenosine receptors in human mast cells, Mol Pharmacol 58, 903–10 (2000).

    PubMed  CAS  Google Scholar 

  88. Takagi H, Kadowaki K, Purification and chemical properties of a flocculant produced by Paecilomyces, Agric Biol Chem 49, 3159–64 (1985).

    CAS  Google Scholar 

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  1. Mitsubishi Kagaku Institute of Life Sciences, 11-Go Minamioya, Machida, Tokyo, 194-8511, Japan

    Hideyoshi Higashi

  2. Institute of Materia Medica, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, 100050, China

    Nai Hong Chen

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Higashi, H., Chen, N.H. Ganglioside/protein kinase signals triggering cytoskeletal actin reorganization. Glycoconj J 20, 49–58 (2003). https://doi.org/10.1023/B:GLYC.0000016742.88750.1a

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