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Crosstalk Between Cell Adhesion Molecules and the Semaphorin/Neuropilin/Plexin Signalling

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The Neuropilins: Role and Function in Health and Disease

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Abstract

Signalling by cell adhesion molecules (IgCAMs) plays diverse and fundamental roles in the formation, maturation and function of the nervous system. Investigations of their mechanisms of action during early steps of the wiring of neuronal circuits uncovered a contribution of the L1CAM subgroup of IgCAMs in axonal responses to Class 3 Semaphorins (Sema3s), which are secreted in vertebrates. L1CAMs were found to interact with Neuropilins (NRPs), the ligand-binding moiety of Sema3 receptor complexes. As such, L1-NRP cis interactions were shown to be required for some Sema3s to elicit a neuronal guidance response, while trans interactions were found to regulate the nature of the response. From these initial findings, additional contributions and molecular interplay with the Semaphorin signalling have been characterized, which expand the physiological and pathological contexts in which IgCAM/Semaphorin crosstalk might contribute.

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References

  1. Jongbloets BC, Pasterkamp RJ (2014) Semaphorin signalling during development. Development 141:3292–3297

    Article  CAS  PubMed  Google Scholar 

  2. Drabkin H, Nasarre P, Gemmill R (2014) The emerging role of class-3 semaphorins and their neuropilin receptors in oncology. Onco Targets Ther 7:1663

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  3. Perälä N, Sariola H, Immonen T (2012) More than nervous: the emerging roles of plexins. Differ Res Biol Divers 83:77–91

    Article  CAS  Google Scholar 

  4. Fujisawa H (2002) From the discovery of neuropilin to the determination of its adhesion sites. Adv Exp Med Biol 515:1–12

    Article  CAS  PubMed  Google Scholar 

  5. Nakamura F, Tanaka M, Takahashi T, Kalb RG, Strittmatter SM (1998) Neuropilin-1 extracellular domains mediate semaphorin D/lll-induced growth cone collapse. Neuron 21:1093–1100

    Article  CAS  PubMed  Google Scholar 

  6. Takahashi T, Fournier A, Nakamura F, Wang LH, Murakami Y, Kalb RG, Fujisawa H, Strittmatter SM (1999) Plexin-neuropilin-1 complexes form functional semaphorin-3A receptors. Cell 99:59–69

    Article  CAS  PubMed  Google Scholar 

  7. Tamagnone L, Artigiani S, Chen H, He Z, Gl M, Song H, Chedotal A, Winberg ML, Goodman CS, Poo M, Tessier-Lavigne M, Comoglio PM (1999) Plexins are a large family of receptors for transmembrane, secreted, and GPI-anchored semaphorins in vertebrates. Cell 99:71–80

    Article  CAS  PubMed  Google Scholar 

  8. Rohm B, Ottemeyer A, Lohrum M, Puschel AW (2000) Plexin/neuropilin complexes mediate repulsion by the axonal guidance signal semaphorin 3A. Mech Dev 93:95–104

    Article  CAS  PubMed  Google Scholar 

  9. Burden-Gulley SM, Pendergast M, Lemmon V (1997) The role of cell adhesion molecule L1 in axonal extension, growth cone motility, and signal transduction. Cell Tissue Res 290:415–422

    Article  CAS  PubMed  Google Scholar 

  10. Hortsch M (2000) Structural and functional evolution of the L1 family: are four adhesion molecules better than one? Mol Cell Neurosci 15:1–10

    Article  CAS  PubMed  Google Scholar 

  11. Castellani V, Chédotal A, Schachner M, Faivre-Sarrailh C, Rougon G (2000a) Analysis of the L1-deficient mouse phenotype reveals cross-talk between Sema3A and L1 signaling pathways in axonal guidance. Neuron 27:237–249

    Article  CAS  PubMed  Google Scholar 

  12. Law CO, Kirby RJ, Aghamohammadzadeh S, Furley AJW (2008a) The neural adhesion molecule TAG-1 modulates responses of sensory axons to diffusible guidance signals. Development 135:2361–2371

    Article  CAS  PubMed  Google Scholar 

  13. Itoh K, Cheng L, Kamei Y, Fushiki S, Kamiguchi H, Gutwein P, Stoeck A, Arnold B, Altevogt P, Lemmon V (2004) Brain development in mice lacking L1-L1 homophilic adhesion. J Cell Biol 165:145–154

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Wright AG, Demyanenko GP, Powell A, Schachner M, Enriquez-Barreto L, Tran TS, Polleux F, Maness PF (2007) Close homolog of L1 and neuropilin 1 mediate guidance of thalamocortical axons at the ventral telencephalon. J Neurosci 27:13667–13679

    Article  CAS  PubMed  Google Scholar 

  15. Falk J, Bechara A, Fiore R, Nawabi H, Zhou H, Hoyo-Becerra C, Bozon M, Rougon G, Grumet M, Puschel AW, Sanes JR, Castellani V (2005) Dual functional activity of semaphorin 3B is required for positioning the anterior commissure. Neuron 48:63–75

    Article  PubMed  Google Scholar 

  16. Demyanenko GP, Mohan V, Zhang X, Brennaman LH, Dharbal KES, Tran TS, Manis PB, Maness PF (2014) Neural cell adhesion molecule NrCAM regulates Semaphorin 3F-induced dendritic spine remodeling. J Neurosci 34:11274–11287

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Demyanenko GP, Riday TT, Tran TS, Dalal J, Darnell EP, Brennaman LH, Sakurai T, Grumet M, Philpot BD, Maness PF (2011a) NrCAM deletion causes topographic mistargeting of thalamocortical axons to the visual cortex and disrupts visual acuity. J Neurosci 31:1545–1558

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Castellani V, De Angelis E, Kenwrick S, Rougon G (2002) Cis and trans interactions of L1 with neuropilin-1 control axonal responses to semaphorin 3A. EMBO J 21:6348–6357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Dang P, Smythe E, Furley AJW (2012a) TAG1 regulates the endocytic trafficking and signaling of the Semaphorin3A receptor complex. J Neurosci 32:10370–10382

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Wang X, Zhang W, Cheever T, Schwarz V, Opperman K, Hutter H, Koepp D, Chen L (2008) The C. elegans L1CAM homologue LAD-2 functions as a coreceptor in MAB-20/Sema2 mediated axon guidance. J Cell Biol 180:233–246

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Cohen NR, Taylor JS, Scott LB, Guillery RW, Soriano P, Furley AJ (1998) Errors in corticospinal axon guidance in mice lacking the neural cell adhesion molecule L1. Curr Biol 8:26–33

    Article  CAS  PubMed  Google Scholar 

  22. Kamiguchi H, Hlavin ML, Lemmon V (1998a) Role of L1 in neural development: what the knockouts tell us. Mol Cell Neurosci 12:48–55

    Article  CAS  PubMed  Google Scholar 

  23. Kawakami A, Kitsukawa T, Takagi S, Fujisawa H (1996) Developmental^ regulated expression of a cell surface protein, neuropilin, in the mouse nervous system. J Neurobiol 29:1–17

    Article  CAS  PubMed  Google Scholar 

  24. Sibbe M, Taniguchi M, Schachner M, Bartsch U (2007) Development of the corticospinal tract in Semaphorin3A- and CD24-deficient mice. Neuroscience 150:898–904

    Article  CAS  PubMed  Google Scholar 

  25. Faulkner RL, Low LK, Liu XB, Coble J, Jones EG, Cheng HJ (2008) Dorsal turning of motor corticospinal axons at the pyramidal decussation requires plexin signaling. Neural Dev 3:21

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Canty AJ, Murphy M (2008) Molecular mechanisms of axon guidance in the developing corticospinal tract. Prog Neurobiol 85:214–235

    Article  CAS  PubMed  Google Scholar 

  27. Rünker AE, Little GE, Suto F, Fujisawa H, Mitchell KJ (2008) Semaphorin-6A controls guidance of corticospinal tract axons at multiple choice points. Neural Dev 3:34

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. Pires-Neto MA, Lent R (1993) The prenatal development of the anterior commissure in hamsters: pioneer fibers lead the way. Brain Res Dev Brain Res 72:59–66

    Article  CAS  PubMed  Google Scholar 

  29. Cummings DM, Malun D, Brunjes PC (1997) Development of the anterior commissure in the opossum: midline extracellular space and glia coincide with early axon decussation. J Neurobiol 32:403–414

    Article  CAS  PubMed  Google Scholar 

  30. Klingler E, Martin P-M, Garcia M, Moreau-Fauvarque C, Falk J, Chareyre F, Giovannini M, Chédotal A, Girault J-A, Goutebroze L (2015) The cytoskeleton-associated protein SCHIP1 is involved in axon guidance, and is required for piriform cortex and anterior commissure development. Dev Camb Engl 142:2026–2036

    CAS  Google Scholar 

  31. Giger RJ, Cloutier JF, Sahay A, Prinjha RK, Levengood DV, Moore SE, Pickering S, Simmons D, Rastan S, Walsh FS, Kolodkin AL, Ginty DD, Geppert M (2000) Neuropilin-2 is required in vivo for selective axon guidance responses to secreted semaphorins. Neuron 25:29–41

    Article  CAS  PubMed  Google Scholar 

  32. Sahay A, Molliver ME, Ginty DD, Kolodkin AL (2003) Semaphorin 3F is critical for development of limbic system circuitry and is required in neurons for selective CNS axon guidance events. J Neurosci 23:6671–6680

    CAS  PubMed  Google Scholar 

  33. Dufour A, Seibt J, Passante L, Depaepe V, Ciossek T, Frisén J, Kullander K, Flanagan JG, Polleux F, Vanderhaeghen P (2003) Area specificity and topography of thalamocortical projections are controlled by ephrin/Eph genes. Neuron 39:453–465

    Article  CAS  PubMed  Google Scholar 

  34. López-Bendito G, Cautinat A, Sánchez JA, Bielle F, Flames N, Garratt AN, Talmage DA, Role LW, Charnay P, Marín O, Garel S (2006) Tangential neuronal migration controls axon guidance: a role for neuregulin-1 in thalamocortical axon navigation. Cell 125:127–142

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Skaliora I, Singer W, Betz H, Püschel AW (1998) Differential patterns of semaphorin expression in the developing rat brain. Eur J Neurosci 10:1215–1229

    Article  CAS  PubMed  Google Scholar 

  36. Tamamaki N, Fujimori K, Nojyo Y, Kaneko T, Takauji R (2003) Evidence that Sema3A and Sema3F regulate the migration of GABAergic neurons in the developing neocortex. J Comp Neurol 455:238–248

    Article  CAS  PubMed  Google Scholar 

  37. Demyanenko GP, Siesser PF, Wright AG, Brennaman LH, Bartsch U, Schachner M, Maness PF (2011b) L1 and CHL1 cooperate in thalamocortical axon targeting. Cereb Cortex 21:401–412

    Article  PubMed  Google Scholar 

  38. Ohyama K, Tan-Takeuchi K, Kutsche M, Schachner M, Uyemura K, Kawamura K (2004) Neural cell adhesion molecule L1 is required for fasciculation and routing of thalamocortical fibres and corticothalamic fibres. Neurosci Res 48:471–475

    Article  CAS  PubMed  Google Scholar 

  39. Wiencken-Barger AE (2004) The role of L1 in axon pathfinding and fasciculation. Cereb Cortex 14:121–131

    Article  CAS  PubMed  Google Scholar 

  40. Davis BM, Frank E, Johnson FA, Scott SA (1989) Development of central projections of lumbosacral sensory neurons in the chick. J Comp Neurol 279:556–566

    Article  CAS  PubMed  Google Scholar 

  41. Eide AL, Glover JC (1997) Developmental dynamics of functionally specific primary sensory afferent projections in the chicken embryo. Anat Embryol (Berl) 195:237–250

    Article  CAS  Google Scholar 

  42. Snider WD (1994) Functions of the neurotrophins during nervous system development: what the knockouts are teaching us. Cell 77:627–638

    Article  PubMed  Google Scholar 

  43. Fu SY, Sharma K, Luo Y, Raper JA, Frank E (2000) SEMA3A regulates developing sensory projections in the chicken spinal cord. J Neurobiol 45:227–236

    Article  CAS  PubMed  Google Scholar 

  44. Wright DE, White FA, Gerfen RW, Silos-Santiago I, Snider WD (1995) The guidance molecule semaphorin III is expressed in regions of spinal cord and periphery avoided by growing sensory axons. J Comp Neurol 361:321–333

    Article  CAS  PubMed  Google Scholar 

  45. Behar O, Golden JA, Mashimo H, Schoen FJ, Fishman MC (1996) Semaphorin III is needed for normal patterning and growth of nerves, bones and heart. Nature 383:525–528

    Article  CAS  PubMed  Google Scholar 

  46. Gu C, Rodriguez ER, Reimert DV, Shu T, Fritzsch B, Richards U, Kolodkin AL, Ginty DD (2003) Neuropilin-1 conveys semaphorin and VEGF signaling during neural and cardiovascular development. Dev Cell 5:45–57

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Liu RQ, Wang W, Legg A, Abramyan J, O’Connor TP (2014) Semaphorin 5B is a repellent cue for sensory afferents projecting into the developing spinal cord. Development 141:1940–1949

    Article  CAS  PubMed  Google Scholar 

  48. Browne K, Wang W, Liu RQ, Piva M, O’Connor TP (2012) Transmembrane semaphorin5B is proteolytically processed into a repulsive neural guidance cue. J Neurochem 123(1):135–146

    Article  CAS  PubMed  Google Scholar 

  49. Saghatelyan AK, Nikonenko AG, Sun M, Rolf B, Putthoff P, Kutsche M, Bartsch U, Dityatev A, Schachner M (2004) Reduced GABAergic transmission and number of hippocampal perisomatic inhibitory synapses in juvenile mice deficient in the neural cell adhesion molecule L1. Mol Cell Neurosci 26:191–203

    Article  CAS  PubMed  Google Scholar 

  50. Triana-Baltzer GB, Liu Z, Berg DK (2006) Pre- and postsynaptic actions of L1-CAM in nicotinic pathways. Mol Cell Neurosci 33:214–226

    Article  CAS  PubMed  Google Scholar 

  51. Huang ZJ (2006) Subcellular organization of GABAergic synapses: role of ankyrins and L1 cell adhesion molecules. Nat Neurosci 9:163–166

    Article  CAS  PubMed  Google Scholar 

  52. Bouzioukh F, Daoudal G, Falk J, Debanne D, Rougon G, Castellani V (2006) Semaphorin3A regulates synaptic function of differentiated hippocampal neurons. Eur J Neurosci 23:2247–2254

    Article  PubMed  Google Scholar 

  53. Morita A, Yamashita N, Sasaki Y, Uchida Y, Nakajima O, Nakamura F, Yagi T, Taniguchi M, Usui H, Katoh-Semba R, Takei K, Goshima Y (2006) Regulation of dendritic branching and spine maturation by semaphorin3A-Fyn signaling. J Neurosci 26:2971–2980

    Article  CAS  PubMed  Google Scholar 

  54. Sahay A, Kim CH, Sepkuty JP, Cho E, Huganir RL, Ginty DD, Kolodkin AL (2005) Secreted semaphorins modulate synaptic transmission in the adult hippocampus. J Neurosci 25:3613–3620

    Article  CAS  PubMed  Google Scholar 

  55. Tran TS, Rubio ME, Clem RL, Johnson D, Case L, Tessier-Lavigne M, Huganir RL, Ginty DD, Kolodkin AL (2009) Secreted semaphorins control spine distribution and morphogenesis in the postnatal CNS. Nature 462:1065–1069

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Castellani V, Falk J, Rougon G (2004a) Semaphorin3A-induced receptor endocytosis during axon guidance responses is mediated by L1 CAM. Mol Cell Neurosci 26:89–100

    Article  CAS  PubMed  Google Scholar 

  57. Bechara A, Nawabi H, Moret F, Yaron A, Weaver E, Bozon M, Abouzid K, Guan JL, Tessier-Lavigne M, Lemmon V, Castellani V (2008) FAK-MAPK-dependent adhesion disassembly downstream of L1 contributes to semaphorin3A-induced collapse. EMBO J 27:1549–1562

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Kamiguchi H (2007) The role of cell adhesion molecules in axon growth and guidance. Adv Exp Med Biol 621:95–103

    Article  PubMed  Google Scholar 

  59. Maness PF, Schachner M (2007) Neural recognition molecules of the immunoglobulin superfamily: signaling transducers of axon guidance and neuronal migration. Nat Neurosci 10:19–26

    Article  CAS  PubMed  Google Scholar 

  60. Herron LR, Hill M, Davey F, Gunn-Moore FJ (2009) The intracellular interactions of the L1 family of cell adhesion molecules. Biochem J 419:519–531

    Article  CAS  PubMed  Google Scholar 

  61. Suter DM, Errante LD, Belotserkovsky V, Forscher P (1998) The Ig superfamily cell adhesion molecule, apCAM, mediates growth cone steering by substrate-cytoskeletal coupling. J Cell Biol 141:227–240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Suter DM, Forscher P (2000) Substrate-cytoskeletal coupling as a mechanism for the regulation of growth cone motility and guidance. J Neurobiol 44:97–113

    Article  CAS  PubMed  Google Scholar 

  63. Faivre-Sarrailh C, Falk J, Pollerberg E, Schachner M, Rougon G (1999) NrCAM, cerebellar granule cell receptor for the neuronal adhesion molecule F3, displays an actin-dependent mobility in growth cones. J Cell Sci 112(Pt 18):3015–3027

    CAS  PubMed  Google Scholar 

  64. Falk J, Thoumine O, Dequidt C, Choquet D, Faivre-Sarrailh C (2004) NrCAM coupling to the cytoskeleton depends on multiple protein domains and partitioning into lipid rafts. Mol Biol Cell 15:4695–4709

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Gil OD (2003) Ankyrin binding mediates L1CAM interactions with static components of the cytoskeleton and inhibits retrograde movement of L1CAM on the cell surface. J Cell Biol 162:719–730

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Nishimura K, Yoshihara F, Tojima T, Ooashi N, Yoon W, Mikoshiba K, Bennett V, Kamiguchi H (2003) L1-dependent neuritogenesis involves ankyrinB that mediates L1-CAM coupling with retrograde actin flow. J Cell Biol 163:1077–1088

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Shimada T, Toriyama M, Uemura K, Kamiguchi H, Sugiura T, Watanabe N, Inagaki N (2008) Shootin1 interacts with actin retrograde flow and L1-CAM to promote axon outgrowth. J Cell Biol 181:817–829

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Dirks P, Thomas U, Montag D (2006) The cytoplasmic domain of NrCAM binds to PDZ domains of synapse-associated proteins SAP90/PSD95 and SAP97. Eur J Neurosci 24:25–31

    Article  PubMed  Google Scholar 

  69. Davey F, Hill M, Falk J, Sans N, Gunn-Moore FJ (2005) Synapse associated protein 102 is a novel binding partner to the cytoplasmic terminus of neurone-glial related cell adhesion molecule. J Neurochem 94:1243–1253

    Article  CAS  PubMed  Google Scholar 

  70. Zheng C-Y, Seabold GK, Horak M, Petralia RS (2011) MAGUKs, synaptic development, and synaptic plasticity. Neuroscientist 17:493–512

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Elias GM, Apostolides PF, Kriegstein AR, Nicoll RA, others (2008) Differential trafficking of AMPA and NMDA receptors by SAP102 and PSD-95 underlies synapse development. Proc Natl Acad Sci 105:20953–20958

    Google Scholar 

  72. Bennett V, Healy J (2009) Membrane domains based on ankyrin and spectrin associated with cell-cell interactions. Cold Spring Harb Perspect Biol 1:a003012–a003012

    Article  PubMed  PubMed Central  Google Scholar 

  73. Davis JQ, Bennett V (1994) Ankyrin binding activity shared by the neurofascin/Ll/NrCAM family of nervous system cell adhesion molecules. J Biol Chem 269:27163–27166

    CAS  PubMed  Google Scholar 

  74. Tuvia S, Garver TD, Bennett V (1997) The phosphorylation state of the FIGQY tyrosine of neurofascin determines ankyrin-binding activity and patterns of cell segregation. Proc Natl Acad Sci U S A 94:12957–12962

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Garver TD, Ren Q, Tuvia S, Bennett V (1997) Tyrosine phosphorylation at a site highly conserved in the L1 family of cell adhesion molecules abolishes ankyrin binding and increases lateral mobility of neurofascin. J Cell Biol 137:703–714

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Hortsch M, Nagaraj K, Godenschwege T (2009) The interaction between L1-type proteins and ankyrins – a master switch for L1-type CAM function. Cell Mol Biol Lett 14:57–69

    Article  CAS  PubMed  Google Scholar 

  77. Boiko T, Vakulenko M, Ewers H, Yap CC, Norden C, Winckler B (2007) Ankyrin-dependent and -independent mechanisms orchestrate axonal compartmentalization of L1 family members neurofascin and Ll/neuron-glia cell adhesion molecule. J Neurosci 27:590–603

    Article  CAS  PubMed  Google Scholar 

  78. Scotland P, Zhou D, Benveniste H, Bennett V (1998) Nervous system defects of AnkyrinB (−/−) mice suggest functional overlap between the cell adhesion molecule L1 and 440-kD AnkyrinB in premyelinated axons. J Cell Biol 143:1305–1315

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Buhusi M, Schlatter MC, Demyanenko GP, Thresher R, Maness PF (2008) L1 interaction with ankyrin regulates mediolateral topography in the retinocollicular projection. J Neurosci 28:177–188

    Article  CAS  PubMed  Google Scholar 

  80. Cheng L, Itoh K, Lemmon V (2005a) L1-mediated branching is regulated by two ezrin-radixin-moesin (ERM)-binding sites, the RSLE region and a novel juxtamembrane ERM-binding region. J Neurosci 25:395–403

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Dickson TC (2002) Functional binding interaction identified between the axonal CAM L1 and members of the ERM family. J Cell Biol 157:1105–1112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Sakurai T, Gil OD, Whittard JD, Gazdoiu M, Joseph T, Wu J, Waksman A, Benson DL, Salton SR, Felsenfeld DP (2008) Interactions between the L1 cell adhesion molecule and ezrin support traction-force generation and can be regulated by tyrosine phosphorylation. J Neurosci Res 86:2602–2614

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Gunn-Moore FJ, Hill M, Davey F, Herron LR, Tait S, Sherman D, Brophy PJ (2006) A functional FERM domain binding motif in neurofascin. Mol Cell Neurosci 33:441–446

    Article  CAS  PubMed  Google Scholar 

  84. Schlatter MC, Buhusi M, Wright AG, Maness PF (2008) CHL1 promotes Sema3A-induced growth cone collapse and neurite elaboration through a motif required for recruitment of ERM proteins to the plasma membrane. J Neurochem 104:731–744

    CAS  PubMed  Google Scholar 

  85. Bretscher A, Chambers D, Nguyen R, Reczek D (2000) ERM-Merlin and EBP50 protein families in plasma membrane organization and function. Annu Rev Cell Dev Biol 16:113–143

    Article  CAS  PubMed  Google Scholar 

  86. Mintz CD, Carcea I, McNickle DG, Dickson TC, Ge Y, Salton SRJ, Benson DL (2008) ERM proteins regulate growth cone responses to Sema3A. J Comp Neurol 510:351–366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Tojima T, Itofusa R, Kamiguchi H (2010) Asymmetric clathrin-mediated endocytosis drives repulsive growth cone guidance. Neuron 66:370–377

    Article  CAS  PubMed  Google Scholar 

  88. Piper M, Plachez C, Zalucki O, Fothergill T, Goudreau G, Erzurumlu R, Gu C, Richards U (2009) Neuropilin 1-Sema signaling regulates crossing of cingulate pioneering axons during development of the corpus callosum. Cereb Cortex 19 Suppl l:i11–i21

    Article  Google Scholar 

  89. Fournier AE, Nakamura F, Kawamoto S, Goshima Y, Kalb RG, Strittmatter SM (2000) Semaphorin3A enhances endocytosis at sites of receptor-F-actin colocalization during growth cone collapse. J Cell Biol 149:411–422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Jurney WM, Gallo G, Letourneau PC, McLoon SC (2002) Rac1-mediated endocytosis during ephrin-A2- and semaphorin 3A-induced growth cone collapse. J Neurosci 22:6019–6028

    CAS  PubMed  Google Scholar 

  91. Carcea I, Ma’ayan A, Mesias R, Sepulveda B, Salton SR, Benson DL (2010) Flotillin-mediated endocytic events dictate cell type-specific responses to semaphorin 3A. J Neurosci 30:15317–15329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Kamiguchi H, Long KE, Pendergast M, Schaefer AW, Rapoport I, Kirchhausen T, Lemmon V (1998b) The neural cell adhesion molecule L1 interacts with the AP-2 adaptor and is endocytosed via the clathrin-mediated pathway. J Neurosci 18:5311–5321

    CAS  PubMed  PubMed Central  Google Scholar 

  93. Kamiguchi H, Lemmon V (2000) Recycling of the cell adhesion molecule L1 in axonal growth cones. J Neurosci 20:3676–3686

    CAS  PubMed  PubMed Central  Google Scholar 

  94. Schaefer AW, Kamiguchi H, Wong EV, Beach CM, Landreth G, Lemmon V (1999) Activation of the MAPK signal cascade by the neural cell adhesion molecule L1 requires L1 internalization. J Biol Chem 274:37965–37973

    Article  CAS  PubMed  Google Scholar 

  95. Schaefer AW (2002) L1 endocytosis is controlled by a phosphorylation-dephosphorylation cycle stimulated by outside-in signaling by L1. J Cell Biol 157:1223–1232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Aikawa Y (2013) Ubiquitination within the membrane-proximal ezrin-radixin-moesin (ERM)-binding region of the L1 cell adhesion molecule. Commun Integr Biol 6:e24750

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  97. Aikawa Y (2012) Rabex-5 regulates the endocytic trafficking pathway of ubiquitinated neural cell adhesion molecule L1. J Biol Chem 287(39):32312–32323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Thelen K, Kedar V, Panicker AK, Schmid R-S, Midkiff BR, Maness PF (2002) The neural cell adhesion molecule L1 potentiates integrin-dependent cell migration to extracellular matrix proteins. J Neurosci 22:4918–4931

    CAS  PubMed  Google Scholar 

  99. Sadowski L, Pilecka I, Miaczynska M (2009) Signaling from endosomes: location makes a difference. Exp Cell Res 315:1601–1609

    Article  CAS  PubMed  Google Scholar 

  100. Schmid RS, Pruitt WM, Maness PF (2000) A MAP kinase-signaling pathway mediates neurite outgrowth on L1 and requires Src-dependent endocytosis. J Neurosci 20:4177–4188

    CAS  PubMed  Google Scholar 

  101. Campbell DS, Holt CE (2003) Apoptotic pathway and MAPKs differentially regulate chemotropic responses of retinal growth cones. Neuron 37:939–952

    Article  CAS  PubMed  Google Scholar 

  102. Kabayama H, Nakamura T, Takeuchi M, Iwasaki H, Taniguchi M, Tokushige N, Mikoshiba K (2009) Ca2+ induces macropinocytosis via F-actin depolymerization during growth cone collapse. Mol Cell Neurosci 40:27–38

    Article  CAS  PubMed  Google Scholar 

  103. Kabayama H, Takeuchi M, Taniguchi M, Tokushige N, Kozaki S, Mizutani A, Nakamura T, Mikoshiba K (2011) Syntaxin IB suppresses macropinocytosis and semaphorin 3A-induced growth cone collapse. J Neurosci 31:7357–7364

    Article  CAS  PubMed  Google Scholar 

  104. Sigismund S, Woelk T, Puri C, Maspero E, Tacchetti C, Transidico P, Di Fiore PP, Polo S (2005) Clathrin-independent endocytosis of ubiquitinated cargos. Proc Natl Acad Sci U S A 102:2760–2765

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Long KE, Asou H, Snider MD, Lemmon V (2001) The role of endocytosis in regulating L1-mediated adhesion. J Biol Chem 276:1285–1290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Stenmark H (2012) The Rabs: a family at the root of metazoan evolution. BMC Biol 10:68

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Stenmark H (2009) Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 10:513–525

    Article  CAS  PubMed  Google Scholar 

  108. Feliciano WD, Yoshida S, Straight SW, Swanson JA (2011) Coordination of the Rab5 cycle on macropinosomes. Traffic 12:1911–1922

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Roberts RL, Barbieri MA, Ullrich J, Stahl PD (2000) Dynamics of rab5 activation in endocytosis and phagocytosis. J Leukoc Biol 68:627–632

    CAS  PubMed  Google Scholar 

  110. Horiuchi H, Giner A, Hoflack B, Zerial M (1995) A GDP/GTP exchange-stimulatory activity for the Rab5-RabGDI complex on clathrin-coated vesicles from bovine brain. J Biol Chem 270:11257–11262

    Article  CAS  PubMed  Google Scholar 

  111. Falk J, Konopacki FA, Zivraj KH, Holt CE (2014) Rab5 and Rab4 regulate axon elongation in the Xenopus visual system. J Neurosci 34:373–391

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Wu K-Y, He M, Hou Q-Q, Sheng A-L, Yuan L, Liu F, Liu W-W, Li GP, Jiang X-Y, Luo Z-G, others (2014) Semaphorin 3A activates the guanosine triphosphatase Rab5 to promote growth cone collapse and organize callosal axon projections. Sci Signal 7(340):ra81

    Google Scholar 

  113. Ren Q, Bennett V (1998) Palmitoylation of neurofascin at a site in the membrane-spanning domain highly conserved among the L1 family of cell adhesion molecules. J Neurochem 70:1839–1849

    Article  CAS  PubMed  Google Scholar 

  114. Schmid RS, Midkiff BR, Kedar VP, Maness PF (2004) Adhesion molecule L1 stimulates neuronal migration through Vav2-Pakl signaling. Neuroreport 15:2791–2794

    CAS  PubMed  Google Scholar 

  115. Tian N, Leshchyns’ka I, Welch JH, Diakowski W, Yang H, Schachner M, Sytnyk V (2012) Lipid raft-dependent endocytosis of close homolog of adhesion molecule L1 (CHL1) promotes neuritogenesis. J Biol Chem 287:44447–44463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Kozik P, Francis RW, Seaman MNJ, Robinson MS (2010) A screen for endocytic motifs. Traffic 11:843–855

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Kamiguchi H, Lemmon V (1997) Neural cell adhesion molecule LI: signaling pathways and growth cone motility. J Neurosci Res 49:1–8

    Article  CAS  PubMed  Google Scholar 

  118. Hines JH, Abu-Rub M, Henley JR (2010) Asymmetric endocytosis and remodeling of betal-integrin adhesions during growth cone chemorepulsion by MAG. Nat Neurosci 13:829–837

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Woo S, Gomez TM (2006) Rac1 and RhoA promote neurite outgrowth through formation and stabilization of growth cone point contacts. J Neurosci 26:1418–1428

    Article  CAS  PubMed  Google Scholar 

  120. Cheng L, Lemmon S, Lemmon V (2005b) RanBPM is an L1-interacting protein that regulates L1-mediated mitogen-activated protein kinase activation: L1 interacts with RanBPM. J Neurochem 94:1102–1110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Wang D, Li Z, Messing EM, Wu G (2002) Activation of Ras/Erk pathway by a novel MET-interacting protein RanBPM. J Biol Chem 277:36216–36222

    Article  CAS  PubMed  Google Scholar 

  122. Ben-Zvi A, Manor O, Schachner M, Yaron A, Tessier-Lavigne M, Behar O (2008) The semaphorin receptor PlexinA3 mediates neuronal apoptosis during dorsal root ganglia development. J Neurosci 28:12427–12432

    Article  CAS  PubMed  Google Scholar 

  123. Togashi H, Schmidt EF, Strittmatter SM (2006) RanBPM contributes to Semaphorin3A signaling through plexin-A receptors. J Neurosci 26:4961–4969

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Toyofuku T, Yoshida J, Sugimoto T, Zhang H, Kumanogoh A, Hori M, Kikutani H (2005) FARP2 triggers signals for Sema3A-mediated axonal repulsion. Nat Neurosci 8:1712–1719

    Article  CAS  PubMed  Google Scholar 

  125. Stenmark H, Vitale G, Ullrich O, Zerial M (1995) Rabaptin-5 is a direct effector of the small GTPase Rab5 in endocytic membrane fusion. Cell 83:423–432

    Article  CAS  PubMed  Google Scholar 

  126. Uchida Y, Ohshima T, Sasaki Y, Suzuki H, Yanai S, Yamashita N, Nakamura F, Takei K, lhara Y, Mikoshiba K, Kolattukudy P, Honnorat J, Goshima Y (2005) Semaphorin3A signalling is mediated via sequential Cdk5 and GSK3beta phosphorylation of CRMP2: implication of common phosphorylating mechanism underlying axon guidance and Alzheimer’s disease. Genes Cells 10:165–179

    Article  CAS  PubMed  Google Scholar 

  127. Schmidt EF, Shim S-O, Strittmatter SM (2008) Release of MICAL autoinhibition by semaphorin-plexin signaling promotes interaction with collapsin response mediator protein. J Neurosci 28:2287–2297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Schmidt EF, Strittmatter SM (2007) The CRMP family of proteins and their role in Sema3A signaling. In: Pasterkamp RJ (ed) Semaphorins: receptor and intracellular signaling mechanisms. Springer, New York, pp 1–11

    Chapter  Google Scholar 

  129. Adle-Biassette H, Saugier-Veber P, Fallet-Bianco C, Delezoide A-L, Razavi F, Drouot N, Bazin A, Beaufrère A-M, Bessières B, Blesson S, Bucourt M, Carles D, Devisme L, Dijoud F, Fabre B, Fernandez C, Gaillard D, Gonzales M, Jossic F, Joubert M, Laurent N, Leroy B, Loeuillet L, Loget P, Marcorelles P, Martinovic J, Perez M-J, Satge D, Sinico M, Tosi M, Benichou J, Gressens P, Frebourg T, Laquerrière A (2013) Neuropathological review of 138 cases genetically tested for X-linked hydrocephalus: evidence for closely related clinical entities of unknown molecular bases. Acta Neuropathol (Berl) 126:427–442

    Article  CAS  Google Scholar 

  130. Nawabi H, Briancon-Marjollet A, Clark C, Sanyas I, Takamatsu H, Okuno T, Kumanogoh A, Bozon M, Takeshima K, Yoshida Y, Moret F, Abouzid K, Castellani V (2010) A midline switch of receptor processing regulates commissural axon guidance in vertebrates. Genes Dev 24:396–410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Zou Y, Stoeckli E, Chen H, Tessier-Lavigne M (2000) Squeezing axons out of the gray matter: a role for slit and semaphorin proteins from midline and ventral spinal cord. Cell 102:363–375

    Article  CAS  PubMed  Google Scholar 

  132. Evans TA, Bashaw GJ (2010) Axon guidance at the midline: of mice and flies. Curr Opin Neurobiol 20:79–85

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Evans TA, Santiago C, Arbeille E, Bashaw GJ (2015) Robo2 acts in trans to inhibit Slit-Robol repulsion in pre-crossing commissural axons. eLife 4:e08407

    PubMed  PubMed Central  Google Scholar 

  134. Neuhaus-Follini A, Bashaw GJ (2015) Crossing the embryonic midline: molecular mechanisms regulating axon responsiveness at an intermediate target. Wiley Interdiscip Rev Dev Biol 4:377–389

    Article  PubMed  PubMed Central  Google Scholar 

  135. Charoy C, Nawabi H, Reynaud F, Derrington E, Bozon M, Wright K, Falk J, Helmbacher F, Kindbeiter K, Castellani V (2012) gdnf activates midline repulsion by Semaphorin3B via NCAM during commissural axon guidance. Neuron 75:1051–1066

    Article  CAS  PubMed  Google Scholar 

  136. Bonanomi D, Pfaff SL (2010) Motor axon pathfinding. Cold Spring Harb Perspect Biol 2:a001735

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  137. Dudanova I, Gatto G, Klein R (2010) GDNF acts as a chemoattractant to support ephrinA-induced repulsion of limb motor axons. Curr Biol CB 20:2150–2156

    Article  CAS  PubMed  Google Scholar 

  138. Sanyas I, Bozon M, Moret F, Castellani V (2012) Motoneuronal Sema3C is essential for setting stereotyped motor tract positioning in limb-derived chemotropic semaphorins. Dev Camb Engl 139:3633–3643

    CAS  Google Scholar 

  139. Hanson MG, Landmesser LT (2004) Normal patterns of spontaneous activity are required for correct motor axon guidance and the expression of specific guidance molecules. Neuron 43:687–701

    Article  CAS  PubMed  Google Scholar 

  140. Worzfeld T, Offermanns S (2014) Semaphorins and plexins as therapeutic targets. Nat Rev Drug Discov 13:603–621

    Article  CAS  PubMed  Google Scholar 

  141. Huber AB, Kania A, Tran TS, Gu C, De Marco GN, Lieberam I, Johnson D, Jessell TM, Ginty DD, Kolodkin AL (2005) Distinct roles for secreted semaphorin signaling in spinal motor axon guidance. Neuron 48:949–964

    Article  CAS  PubMed  Google Scholar 

  142. Haupt C, Kloos K, Faus-Kessler T, Huber AB (2010) Semaphorin 3A-Neuropilin-l signaling regulates peripheral axon fasciculation and pathfinding but not developmental cell death patterns. Eur J Neurosci 31:1164–1172

    Article  PubMed  Google Scholar 

  143. Sasselli V, Pachnis V, Burns AJ (2012) The enteric nervous system. Dev Biol 366:64–73

    Article  CAS  PubMed  Google Scholar 

  144. Kuwajima T, Yoshida Y, Takegahara N, Petros TJ, Kumanogoh A, Jessell TM, Sakurai T, Mason C (2012) Optic Chiasm Presentation of Semaphorin6D in the Context of Plexin-Al and Nr-CAM Promotes Retinal Axon Midline Crossing. Neuron 74:676–690

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Stoeckli ET, Landmesser LT (1995) Axonin-1, Nr-CAM, and Ng-CAM play different roles in the in vivo guidance of chick commissural neurons. Neuron 14:1165–1179

    Article  CAS  PubMed  Google Scholar 

  146. Codina-Solà M, Rodríguez-Santiago B, Horns A, Santoyo J, Rigau M, Aznar-Lafn G, Del Campo M, Gener B, Gabau E, Botella MP, Gutiérrez-Arumf A, Antiñolo G, Pérez-Jurado LA, Cuscó I (2015) Integrated analysis of whole-exome sequencing and transcriptome profiling in males with autism spectrum disorders. Mol Autism 6:21

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  147. Gilabert-Juan J, Sáez AR, Lopez-Campos G, Sebastiá-Ortega N, González-Martínez R, Costa J, Haro JM, Callado LF, Meana JJ, Nacher J, Sanjuán J, Moltó MD (2015) Semaphorin and plexin gene expression is altered in the prefrontal cortex of schizophrenia patients with and without auditory hallucinations. Psychiatry Res 229:850–857

    Article  CAS  PubMed  Google Scholar 

  148. Arbeille E, Reynaud F, Sanyas I, Bozon M, Kindbeiter K, Causeret F, Pierani A, Falk J, Moret F, Castellani V (2015) Cerebrospinal fluid-derived Semaphorin3B orients neuroepithelial cell divisions in the apicobasal axis. Nat Commun 6:6366

    Article  CAS  PubMed  Google Scholar 

  149. Martins-de-Souza D, Cassoli JS, Nascimento JM, Hensley K, Guest PC, Pinzon-Velasco AM, Turck CW (2015) The protein interactome of collapsin response mediator protein-2 (CRMP2/DPYSL2) reveals novel partner proteins in brain tissue. Proteomics Clin Appl 9:817–831

    Article  CAS  PubMed  Google Scholar 

  150. Williams HJ, Norton N, Peirce T, Dwyer S, Williams NM, Moskvina V, Owen MJ, O’Donovan MC (2007) Association analysis of the glial cell line-derived neurotrophic factor (GDNF) gene in schizophrenia. Schizophr Res 97:271–276

    Article  CAS  PubMed  Google Scholar 

  151. Tunca Z, Kıvırcık Akdede B, Özerdem A, Alkın T, Polat S, Ceylan D, Bayın M, Cengizçetin Kocuk N, Şimşek S, Resmi H, Akan P (2015) Diverse glial cell line-derived neurotrophic factor (GDNF) support between mania and schizophrenia: a comparative study in four major psychiatric disorders. Eur Psychiatry J Assoc Eur Psychiatr 30:198–204

    Article  CAS  Google Scholar 

  152. Rich JIM, Hans C, Jones B, Iversen ES, McLendon RE, Rasheed BKA, Dobra A, Dressman HK, Bigner DD, Nevins JR, West M (2005) Gene expression profiling and genetic markers in glioblastoma survival. Cancer Res 65:4051–4058

    Article  CAS  PubMed  Google Scholar 

  153. Karayan-Tapon L, Wager M, Guilhot J, Levillain P, Marquant C, Clarhaut J, Potiron V, Roche J (2008) Semaphorin, neuropilin and VEGF expression in glial tumours: SEMA3G, a prognostic marker? Br J Cancer 99:1153–1160

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. Cai G, Qiao S, Chen K (2015) Suppression of miR-221 inhibits glioma cells proliferation and invasion via targeting SEMA3B. Biol Res 48:37

    Article  PubMed  PubMed Central  Google Scholar 

  155. Sehgal A, Ricks S, Warrick J, Boynton AL, Murphy GP (1999) Antisense human neuroglia related cell adhesion molecule hNr-CAM, reduces the tumorigenic properties of human glioblastoma cells. Anticancer Res 19:4947–4953

    CAS  PubMed  Google Scholar 

  156. Sehgal A, Boynton AL, Young RF, Vermeulen SS, Yonemura KS, Kohler EP, Aldape HC, Simrell CR, Murphy GP (1998) Cell adhesion molecule Nr-CAM is over-expressed in human brain tumors. Int J Cancer J Int Cancer 76:451–458

    Article  CAS  Google Scholar 

  157. Wan G, Too H-P (2010) A specific isoform of glial cell line-derived neurotrophic factor family receptor alpha 1 regulates RhoA expression and glioma cell migration. J Neurochem 115:759–770

    Article  CAS  PubMed  Google Scholar 

  158. Yu Z-Q, Zhang B-L, Ren Q-X, Wang J-C, Yu R-T, Qu D-W, Liu Z-H, Xiong Y, Gao D-S (2013) Changes in transcriptional factor binding capacity resulting from promoter region methylation induce aberrantly high GDNF expression in human glioma. Mol Neurobiol 48:571–580

    Article  CAS  PubMed  Google Scholar 

  159. Song H, Moon A (2006) Glial cell-derived neurotrophic factor (GDNF) promotes low-grade Hs683 glioma cell migration through JNK, ERK-1/2 and p38 MAPK signaling pathways. Neurosci Res 56:29–38

    Article  CAS  PubMed  Google Scholar 

  160. Ku M-C, Wolf SA, Respondek D, Matyash V, Pohlmann A, Waiczies S, Waiczies H, Niendorf T, Synowitz M, Glass R, Kettenmann H (2013) GDNF mediates glioblastoma-induced microglia attraction but not astrogliosis. Acta Neuropathol (Berl) 125:609–620

    Article  CAS  Google Scholar 

  161. Correa RG, Sasahara RM, Bengtson MH, Katayama ML, Salim AC, Brentani MM, Sogayar MC, de Souza SJ, Simpson AJ (2001) Human semaphorin 6B [(HSA)SEMA6B], a novel human class 6 semaphorin gene: alternative splicing and all-trans-retinoic acid-dependent downregulation in glioblastoma cell lines. Genomics 73:343–348

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank Pr E. Derrington for constructive reading and comments on the manuscript.

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  1. Institut NeuroMyoGene (INMG), UMR CNRS 5310 – INSERM U1217-Université Claude, Bernard -Lyon I, Bâtiment Mendel 16 rue Raphaël Dubois, F-69622, Villeurbanne Cedex, France

    Leila Boubakar, Julien FaIk & Valérie Castellani

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  1. Leila Boubakar
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  2. Julien FaIk
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  3. Valérie Castellani
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Correspondence to Valérie Castellani .

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  1. Department Anatomy and Cell Biology, Israel Institute of Technology Technion, Haifa, Israel

    Gera Neufeld

  2. Department Anatomy and Cell Biology, Israel Institute of Technology Technion, Haifa, Israel

    Ofra Kessler

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Boubakar, L., FaIk, J., Castellani, V. (2017). Crosstalk Between Cell Adhesion Molecules and the Semaphorin/Neuropilin/Plexin Signalling. In: Neufeld, G., Kessler, O. (eds) The Neuropilins: Role and Function in Health and Disease. Springer, Cham. https://doi.org/10.1007/978-3-319-48824-0_4

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