Interaction of the cell adhesion molecule CHL1 with vitronectin, Integrins, And the plasminogen activator inhibitor-2 promotes CHL1-induced neurite outgrowth and neuronal migration

Journal of Neuroscience

Volumn 34, Issue 44, 2014, Pages 14606-14623

  Katic, Jelena ^a   Loers, Gabriele ^a   Kleene, Ralf ^a   Karl, Nicole ^a   Schmidt, Carsten ^a   Buck, Friedrich ^a   Zmijewski, Jaroslaw W ^e   Jakovcevski, Igor ^a   Preissner, Klaus T ^b   Schachner, Melitta ^c,d  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

^c RUTGERS UNIVERSITY   (United States)

^d SHANTOU UNIVERSITY MEDICAL COLLEGE   (China)

^e University of Alabama at Birmingham   (United States)

Author keywords

Cerebellar development; CHL1; Integrins; Migration; Plasminogen system; Vitronectin

Indexed keywords

ALPHA1 INTEGRIN; ALPHA2 INTEGRIN; ALPHA3 INTEGRIN; ALPHA4 INTEGRIN; ALPHA5 INTEGRIN; ALPHA6 INTEGRIN; ALPHA7 INTEGRIN; BETA1 INTEGRIN; BETA3 INTEGRIN; CD18 ANTIGEN; CD51 ANTIGEN; CELL ADHESION MOLECULE; INTEGRIN; NERVE CELL ADHESION MOLECULE L1; PLASMINOGEN ACTIVATOR INHIBITOR 1; PLASMINOGEN ACTIVATOR INHIBITOR 2; UROKINASE RECEPTOR; VITRONECTIN; CHL1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN RETRIEVAL; ARTICLE; BINDING ASSAY; BRAIN HOMOGENATE; CELL MIGRATION; CELL PROLIFERATION; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; CROSS LINKING; ELECTROSPRAY MASS SPECTROMETRY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GRANULE CELL; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE TEST; IMMUNOPRECIPITATION; MALE; MOUSE; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NEWBORN; NONHUMAN; PHAGE DISPLAY; POLYMERASE CHAIN REACTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; SIGNAL TRANSDUCTION; STEREOMETRY; SYNAPTOSOME; WESTERN BLOTTING; ANIMAL; CELL CULTURE; CELL MOTION; CEREBELLUM; CYTOLOGY; DRUG EFFECTS; GENETICS; KNOCKOUT MOUSE; METABOLISM; NERVE CELL; NEURITE; PHYSIOLOGY;

ANIMALS; CELL ADHESION MOLECULES; CELL MOVEMENT; CELLS, CULTURED; CEREBELLUM; INTEGRINS; MICE; MICE, KNOCKOUT; NEURITES; NEURONS; PLASMINOGEN ACTIVATOR INHIBITOR 2; VITRONECTIN;

EID: 84908350461     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3280-13.2014     Document Type: Article

References (76)

1. Andreyeva A, Leshchyns’ka I, Knepper M, Betzel C, Redecke L, Sytnyk V, Schachner M (2010) CHL1 is a selective organizer of the presynaptic machinery chaperoning the SNARE complex. PLoS One 5:e12018. CrossRef Medline
2. Angeloni D, Lindor NM, Pack S, Latif F, Wei MH, Lerman MI (1999a) CALL gene is haploinsufficient in a 3psyndrome patient. Am J Med Genet 86:482-485. CrossRef Medline
3. Angeloni D, Wei MH, Lerman MI (1999b) Two single nucleotide polymorphisms (SNPs) in the CALL gene for association studies with IQ. Psychiatr Genet 9:165-167. CrossRef Medline
4. Ango F, Wu C, Van der Want JJ, Wu P, Schachner M, Huang ZJ (2008) Bergmann glia and the recognition molecule CHL1 organize GABAergic axons and direct innervation of Purkinje cell dendrites. PLoS Biol 6:e103. CrossRef Medline
5. Archinti M, Britto M, Eden G, Furlan F, Murphy R, Degryse B (2011) The urokinase receptor in the central nervous system. CNS Neurol Disord Drug Targets 10:271-294. CrossRef Medline
6. Bae HB, Tadie JM, Jiang S, Park DW, Bell CP, Thompson LC, Peterson CB, Thannickal VJ, Abraham E, Zmijewski JW (2013) Vitronectin inhibits efferocytosis through interactions with apoptotic cells as well as with macrophages. J Immunol 190:2273-2281. CrossRef Medline
7. Blaess S, Graus-Porta D, Belvindrah R, Radakovits R, Pons S, Littlewood-Evans A, Senften M, Guo H, Li Y, Miner JH, Reichardt LF, Müller U (2004) Beta1-integrins are critical for cerebellar granule cell precursor proliferation. J Neurosci 24:3402-3412. CrossRef Medline
8. Bodary SC, McLean JW (1990) The integrin beta 1 subunit associates with the vitronectin receptor alpha v subunit to form a novel vitronectin receptor in a human embryonic kidney cell line. J Biol Chem 265:5938-5941. Medline
9. Bolte S, Cordelières FP (2006) A guided tour into subcellular colocalization analysis in light microscopy. J Microsc 224:213-232. CrossRef Medline
10. Bruneau N, Szepetowski P (2011) The role of the urokinase receptor in epilepsy, in disorders of language, cognition, communication and behavior, and in the central nervous system. Curr Pharm Des 17:1914-1923. CrossRef Medline
11. Buhusi M, Midkiff BR, Gates AM, Richter M, Schachner M, Maness PF (2003) Close homolog of L1 is an enhancer of integrin-mediated cell migration. J Biol Chem 278:25024-25031. CrossRef Medline
12. Campbell DB, Li C, Sutcliffe JS, Persico AM, Levitt P (2008) Genetic evidence implicating multiple genes in the MET receptor tyrosine kinase pathway in autism spectrum disorder. Autism Res 1:159-168. CrossRef Medline
13. Chen QY, Chen Q, Feng GY, Lindpaintner K, Chen Y, Sun X, Chen Z, Gao Z, Tang J, He L (2005) Case-control association study of the close homologue of L1 (CHL1) gene and schizophrenia in the Chinese population. Schizophr Res 73:269-274. CrossRef Medline
14. Chen S, Mantei N, Dong L, Schachner M (1999) Prevention of neuronal cell death by neural adhesion molecules L1 and CHL1. J Neurobiol 38:428-439. CrossRef Medline
15. Cho E, Lee KJ, Seo JW, Byun CJ, Chung SJ, Suh DC, Carmeliet P, Koh JY, Kim JS, Lee JY (2012) Neuroprotection by urokinase plasminogen activator in the hippocampus. Neurobiol Dis 46:215-224. CrossRef Medline
16. Chu TT, Liu Y (2010) An integrated genomic analysis of gene-function correlation on schizophrenia susceptibility genes. J Hum Genet 55:285-292. CrossRef Medline
17. Cuoco C, Ronchetto P, Gimelli S, Béna F, Divizia MT, Lerone M, MirabelliBadenier M, Mascaretti M, Gimelli G (2011) Microarray based analysis of an inherited terminal 3p26.3 deletion, containing only the CHL1 gene, from a normal father to his two affected children. Orphanet J Rare Dis 6:12. CrossRef Medline
18. Dahme M, Bartsch U, Martini R, Anliker B, Schachner M, Mantei N (1997) Disruption of the mouse L1 gene leads to malformations of the nervous system. Nat Genet 17:346-349. CrossRef Medline
19. Demyanenko GP, Schachner M, Anton E, Schmid R, Feng G, Sanes J, Maness PF (2004) Close homolog of L1 modulates area-specific neuronal positioning and dendrite orientation in the cerebral cortex. Neuron 44:423-437. CrossRef Medline
20. Demyanenko GP, Siesser PF, Wright AG, Brennaman LH, Bartsch U, Schachner M, Maness PF (2011) L1 and CHL1 cooperate in thalamocortical axon targeting. Cereb Cortex 21:401-412. CrossRef Medline
21. Eagleson KL, Gravielle MC, Schlueter McFadyen-Ketchum LJ, Russek SJ, Farb DH, Levitt P (2010) Genetic disruption of the autism spectrum disorder risk gene PLAUR induces GABAA receptor subunit changes. Neuroscience 168:797-810. CrossRef Medline
22. Espinosa JS, Luo L (2008) Timing neurogenesis and differentiation: insights from quantitative clonal analyses of cerebellar granule cells. J Neurosci 28:2301-2312. CrossRef Medline
23. Frints SG, Marynen P, Hartmann D, Fryns JP, Steyaert J, Schachner M, Rolf B, Craessaerts K, Snellinx A, Hollanders K, D’Hooge R, De Deyn PP, Froyen G (2003) CALL interrupted in a patient with non-specific mental retardation: gene dosage-dependent alteration of murine brain development and behavior. Hum Mol Genet 12:1463-1474. CrossRef Medline
24. Hillenbrand R, Molthagen M, Montag D, Schachner M (1999) The close homologue of the neural adhesion molecule L1 (CHL1): patterns of expression and promotion of neurite outgrowth by heterophilic interactions. Eur J Neurosci 11:813-826. CrossRef Medline
25. Holm J, Hillenbrand R, Steuber V, Bartsch U, Moos M, Lubbert H, Montag D, Schachner M (1996) Structural features of a close homologue of L1 (CHL1) in the mouse: a new member of the L1 family of neural recognition molecules. Eur J Neurosci 8:1613-1629. CrossRef Medline
26. Horton MA (1997) The alpha v beta 3 integrin “vitronectin receptor.” Int J Biochem Cell Biol 29:721-725. CrossRef Medline
27. Huang X, Zhu LL, Zhao T, Wu LY, Wu KW, Schachner M, Xiao ZC, Fan M (2011) CHL1 negatively regulates the proliferation and neuronal differentiation of neural progenitor cells through activation of the ERK1/2 MAPK pathway. Mol Cell Neurosci 46:296-307. CrossRef Medline
28. Irintchev A, Koch M, Needham LK, Maness P, Schachner M (2004) Impairment of sensorimotor gating in micse deficient in the cell adhesion molecule L1 or its close homologue, CHL1. Brain Res 1029:131-134. CrossRef Medline
29. Iyer AM, Zurolo E, Boer K, Baayen JC, Giangaspero F, Arcella A, Di Gennaro GC, Esposito V, Spliet WG, van Rijen PC, Troost D, Gorter JA, Aronica E (2010) Tissue plasminogen activator and urokinase plasminogen activator in human epileptogenic pathologies. Neuroscience 167:929-945. CrossRef Medline
30. Jakovcevski I, Wu J, Karl N, Leshchyns’ka I, Sytnyk V, Chen J, Irintchev A, Schachner M (2007) Glial scar expression of CHL1, the close homolog of the adhesion molecule L1, limits recovery after spinal cord injury. J Neurosci 27:7222-7233. CrossRef Medline
31. Jakovcevski I, Siering J, Hargus G, Karl N, Hoelters L, Djogo N, Yin S, Zecevic N, Schachner M, Irintchev A (2009) Close homologue of adhesion molecule L1 promotes survival of Purkinje and granule cells and granule cell migration during murine cerebellar development. J Comp Neurol 513: 496-510. CrossRef Medline
32. Kalus I, Schnegelsberg B, Seidah NG, Kleene R, Schachner M (2003) The proprotein convertase PC5A and a metalloprotease are involved in the proteolytic processing of the neural adhesion molecule L1. J Biol Chem 278:10381-10388. CrossRef Medline
33. Kleene R, Loers G, Langer J, Frobert Y, Buck F, Schachner M (2007) Prion protein regulates glutamate-dependent lactate transport of astrocytes. J Neurosci 27:12331-12340. CrossRef Medline
34. Kolata S, Wu J, Light K, Schachner M, Matzel LD (2008) Impaired working memory duration but normal learning abilities found in mice that are conditionally deficient in the close homolog of L1. J Neurosci 28:13505-13510. CrossRef Medline
35. Lahtinen L, Huusko N, Myöhänen H, Lehtivarjo AK, Pellinen R, Turunen MP, Ylä-Herttuala S, Pirinen E, Pitkänen A (2009) Expression of urokinase-type plasminogen activator receptor is increased during epileptogenesis in the rat hippocampus. Neuroscience 163:316-328. CrossRef Medline
36. Lemkey-Johnston N, Larramendi LM (1968) Types and distribution of synapses upon basket and stellate cells of the mouse cerebellum: an electron microscopic study. J Comp Neurol 134:73-112. CrossRef Medline
37. Leshchyns’ka I, Sytnyk V, Richter M, Andreyeva A, Puchkov D, Schachner M (2006) The adhesion molecule CHL1 regulates uncoating of clathrincoated synaptic vesicles. Neuron 52:1011-1025. CrossRef Medline
38. Levitt P (2005) Disruption of interneuron development. Epilepsia 46 [Suppl 7]:22-28. CrossRef Medline
39. Liu B, Zhang B, Wang T, Liang QC, Jing XR, Zheng J, Wang C, Meng Q, Wang L, Wang W, Guo H, You Y, Zhang H, Gao GD (2010) Increased expression of urokinase-type plasminogen activator receptor in the frontal cortex of patients with intractable frontal lobe epilepsy. J Neurosci Res 88: 2747-2754. CrossRef Medline
40. Lobov S, Ranson M (2011) Molecular competition between plasminogen activator inhibitors type-1 and-2 for urokinase: implications for cellular proteolysis and adhesion in cancer. Cancer Lett 303:118-127. CrossRef Medline
41. Lobov S, Wilczynska M, Bergström F, Johansson LB, Ny T (2004) Structural bases of the redox-dependent conformational switch in the serpin PAI-2. J Mol Biol 344:1359-1368. CrossRef Medline
42. Loers G, Schachner M (2007) Recognition molecules and neural repair. J Neurochem 101:865-882. CrossRef Medline
43. Loers G, Makhina T, Bork U, Dörner A, Schachner M, Kleene R (2012) The interaction between cell adhesion molecule L1, matrix metalloproteinase 14, and adenine nucleotide translocator at the plasma membrane regulates L1-mediated neurite outgrowth of murine cerebellar neurons. J Neurosci 32:3917-3930. CrossRef Medline
44. Madsen CD, Ferraris GM, Andolfo A, Cunningham O, Sidenius N (2007) uPAR-induced cell adhesion and migration: vitronectin provides the key. J Cell Biol 177:927-939. CrossRef Medline
45. Makhina T, Loers G, Schulze C, Ueberle B, Schachner M, Kleene R (2009) Extracellular GAPDH binds to L1 and enhances neurite outgrowth. Mol Cell Neurosci 41:206-218. CrossRef Medline
46. 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. CrossRef Medline
47. Masos T, Miskin R (1997) mRNAs encoding urokinase-type plasminogen activator and plasminogen activator inhibitor-1 are elevated in the mouse brain following kainate-mediated excitation. Brain Res Mol Brain Res 47:157-169. CrossRef Medline
48. Mathisen GH, Yazdani M, Rakkestad KE, Aden PK, Bodin J, Samuelsen M, Nygaard UC, Goverud IL, Gaarder M, Løberg EM, Bølling AK, Becher R, Paulsen RE (2013) Prenatal exposure to bisphenol A interferes with the development of cerebellar granule neurons in mice and chicken. Int J Dev Neurosci 31:762-769. CrossRef Medline
49. Montag-Sallaz M, Schachner M, Montag D (2002) Misguided axonal projections, neural cell adhesion molecule 180 mRNA upregulation, and altered behavior in mice deficient for the close homolog of L1. Mol Cell Biol 22:7967-7981. CrossRef Medline
50. Morag A, Pasmanik-Chor M, Oron-Karni V, Rehavi M, Stingl JC, Gurwitz D (2011) Genome-wide expression profiling of human lymphoblastoid cell lines identifies CHL1 as a putative SSRI antidepressant response biomarker. Pharmacogenomics 12:171-184. CrossRef Medline
51. Morellini F, Lepsveridze E, Kähler B, Dityatev A, Schachner M (2007) Reduced reactivity to novelty, impaired social behavior, and enhanced basal synaptic excitatory activity in perforant path projections to the dentate gyrus in young adult mice deficient in the neural cell adhesion molecule CHL1. Mol Cell Neurosci 34:121-136. CrossRef Medline
52. Murase S, Hayashi Y (1998) Concomitant expression of genes encoding integrin alpha v beta 5 heterodimer and vitronectin in growing parallel fibers of postnatal rat cerebellum: a possible role as mediators of parallel fiber elongation. J Comp Neurol 397:199-212. Medline
53. Nagai N, Okada K, Kawao N, Ishida C, Ueshima S, Collen D, Matsuo O (2008) Urokinase-type plasminogen activator receptor (uPAR) augments brain damage in a murine model of ischemic stroke. Neurosci Lett 432:46-49. CrossRef Medline
54. Ndode-Ekane XE, Pitkänen A (2013) Urokinase-type plasminogen activator receptor modulates epileptogenesis in mouse model of temporal lobe epilepsy. Mol Neurobiol 47:914-937. CrossRef Medline
55. Nikonenko AG, Sun M, Lepsveridze E, Apostolova I, Petrova I, Irintchev A, Dityatev A, Schachner M (2006) Enhanced perisomatic inhibition and impaired long-term potentiation in the CA1 region of juvenile CHL1deficient mice. Eur J Neurosci 23:1839-1852. CrossRef Medline
56. Pons S, Trejo JL, Martínez-Morales JR, Martí E (2001) Vitronectin regulates Sonic hedgehog activity during cerebellum development through CREB phosphorylation. Development 128:1481-1492. Medline
57. Powell EM, Campbell DB, Stanwood GD, Davis C, Noebels JL, Levitt P (2003) Genetic disruption of cortical interneuron development causes regionand GABA cell type-specific deficits, epilepsy, and behavioral dysfunction. J Neurosci 23:622-631. Medline
58. Pratte M, Jamon M (2009) Impairment of novelty detection in mice targeted for the Chl1 gene. Physiol Behav 97:394-400. CrossRef Medline
59. Pratte M, Rougon G, Schachner M, Jamon M (2003) Mice deficient for the close homologue of the neural adhesion cell L1 (CHL1) display alterations in emotional reactivity and motor coordination. Behav Brain Res 147:31-39. CrossRef Medline
60. Preissner KT, Reuning U (2011) Vitronectin in vascular context: facets of a multitalented matricellular protein. Semin Thromb Hemost 37:408-424. CrossRef Medline
61. Preissner KT, Wassmuth R, Muller-Berghaus G (1985) Physicochemical characterization of human S-protein and its function in the blood coagulation system. Biochem J 231:349-355. Medline
62. Preissner KT, Holzhuter S, Justus C, Muller-Berghaus G (1989) Identification of and partial characterization of platelet vitronectin: evidence for complex formation with platelet-derived plasminogen activator inhibitor-1. Blood 74: 1989-1996. Medline
63. Rolf B, Lang D, Hillenbrand R, Richter M, Schachner M, Bartsch U (2003) Altered expression of CHL1 by glial cells in response to optic nerve injury and intravitreal application of fibroblast growth factor-2. J Neurosci Res 71:835-843. CrossRef Medline
64. Royer-Zemmour B, Ponsole-Lenfant M, Gara H, Roll P, Lévêque C, Massacrier A, Ferracci G, Cillario J, Robaglia-Schlupp A, Vincentelli R, Cau P, Szepetowski P (2008) Epileptic and developmental disorders of the speech cortex: ligand/receptor interaction of wild-type and mutant SRPX2 with the plasminogen activator receptor uPAR. Hum Mol Genet 17:3617-3630. CrossRef Medline
65. Sakurai K, Migita O, Toru M, Arinami T (2002) An association between a missense polymorphism in the close homologue of L1 (CHL1, CALL) gene and schizophrenia. Mol Psychiatry 7:412-415. CrossRef Medline
66. Salyakina D, Cukier HN, Lee JM, Sacharow S, Nations LD, Ma D, Jaworski JM, Konidari I, Whitehead PL, Wright HH, Abramson RK, Williams SM, Menon R, Haines JL, Gilbert JR, Cuccaro ML, Pericak-Vance MA (2011) Copy number variants in extended autism spectrum disorder families reveal candidates potentially involved in autism risk. PLoS One 6:e26049. CrossRef Medline
67. Schmidt C, Lepsverdize E, Chi SL, Das AM, Pizzo SV, Dityatev A, Schachner M (2008) Amyloid precursor protein and amyloid beta-peptide bind to ATP synthase and regulate its activity at the surface of neural cells. Mol Psychiatry 13:953-969. CrossRef Medline
68. Sharon R, Abramovitz R, Miskin R (2002) Plasminogen mRNA induction in the mouse brain after kainate excitation: codistribution with plasminogen activator inhibitor-2 (PAI-2) mRNA. Brain Res Mol Brain Res 104: 170-175. CrossRef Medline
69. Shoukier M, Fuchs S, Schwaibold E, Lingen M, Gärtner J, Brockmann K, Zirn B (2013) Microduplication of 3p26.3 in nonsyndromic intellectual disability indicates an important role of CHL1 for normal cognitive function. Neuropediatrics 44:268-271 CrossRef Medline
70. Smith HW, Marshall CJ (2010) Regulation of cell signaling by uPAR. Nat Rev Mol Cell Biol 11:23-36. CrossRef Medline
71. Tam GW, van de Lagemaat LN, Redon R, Strathdee KE, Croning MD, Malloy MP, Muir WJ, Pickard BS, Deary IJ, Blackwood DH, Carter NP, Grant SG (2010) Confirmed rare copy number variants implicate novel genes in schizophrenia. Biochem Soc Trans 38:445-451. CrossRef Medline
72. Wang S, Cesca F, Loers G, Schweizer M, Buck F, Benfenati F, Schachner M, Kleene R (2011) Synapsin I is an oligomannose-carrying glycoprotein, acts as an oligomannose-binding lectin, and promotes neurite outgrowth and neuronal survival when released via glia-derived exosomes. J Neurosci 31:7275-7290. CrossRef Medline
73. Wei Y, Eble JA, Wang Z, Kreidberg JA, Chapman HA (2001) Urokinase receptors promote beta1 integrin function through interactions with integrin alpha3beta1. Mol Biol Cell 12:2975-2986. CrossRef Medline
74. 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. CrossRef Medline
75. Yamasaki T, Kawaji K, Ono K, Bito H, Hirano T, Osumi N, Kengaku M (2001) Pax6 regulates granule cell polarization during parallel fiber formation in the developing cerebellum. Development 128:3133-3144. Medline
76. Zhang SJ, Zou M, Lu L, Lau D, Ditzel DA, Delucinge-Vivier C, Aso Y, Descombes P, Bading H (2009) Nuclear calcium signaling controls expression of a large gene pool: identification of a gene program for acquired neuroprotection induced by synaptic activity. PLoS Genet 5:e1000604. CrossRef Medline