expression in the lesioned CNS, regulation by bfgf, and their role during brain development two members of the L1 family
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1 Research Collection Doctoral Thesis expression in the lesioned CNS, regulation by bfgf, and their role during brain development two members of the L1 family Author(s): Lang, Doris Publication Date: 2000 Permanent Link: Rights / License: In Copyright - Non-Commercial Use Permitted This page was generated automatically upon download from the ETH Zurich Research Collection. For more information please consult the Terms of use. ETH Library
2 Diss. ETFI No LI AND CHL1 Two Members of the LI Family: Expression in the Lesioned CNS, Regulationby bfgf, and their Role during Brain Development A dissertation submitted to the Swiss Federal Instituteof TechnologyZürich for the degree of Doctorof Natural Scifncfs presentedby Doris Lang M.A., University of Colorado,USA born Mav 15, 1964 Citizen of ObererlinsbachSO, Switzerland accepted on the recommendationof Prof. M.E. Schwab,referee Prof. M. Schachner, co-referee Prof. H.-P. Lipp, co-referee 2000
3 Summary vi Summary LI and the close homologof LI (CHL'l) are two members of the LI family of cell recognition molecules believedto play critical roles in the developing,adult, and lesioned nervous tissue. LI is implicated in such diverse processes as migration of nerve cells, elongation, fasciculation and pathfinding of axons, myelination in the peripheral nervous system (PNS), and synaptic plasticity. Although a detailed functional characterization of CE1L1 has still to be performed, CHL1 has been demonstrated to support neurite elongation in vitro. Experimentally manipulated and geneticallv modified mouse mutants were analyzed to obtain further insights into the functional roles of both proteins in vivo. Lack of axonal regeneration in the mammalian central nervous system (CNS) has been related to inhibitory molecules which are expressed by glial cells and which prevent axonal regrowth. The paucitv of molecules with neurite-growth promoting properties on cell surfaces of differentiatedcns glial cells may also explain the inability of the adult mammalian CNS to regen.era.te injured axons. To test the latter hypothesis, axonal regeneration was studied in the optic nerve of a transgenic mouse ectopically expressing LI in astrocytes under regulatory sequences of the gene for the glial fibrillary acidic protein (GFAP). Different transgenic mouse lines were cross-bred to increase levels of transgene expression. Exogeneous basic fibroblast growth factor (bfgf),known to increase GFAP expression, was applied to further increase transgene expression. Increased expression of transgenic LI mrna and protein was found in retinal Müller cells. Despite the fact that glial cells expressed high levels of the LI transgene, regrowthof injured retinal ganglion cell axons in transgenic mice was not improved when compared with wild-type animals. Thus, high levels of the Li transgene present on CNS glial inhibitory properties of adult CNS tissue. cells are not sufficient to override the A critical role of LI for normal brain development Is indicated by the fact that mutations in the LI gene cause a severe neurological disease, termed CRASH. Mutations in the LI gene lead to severe malformations of the brain. The phenotype of CRASH patients is complex and variable, both within and between families. Typical defects associated with CRASH Syndrome include: corpus callosum hypoplasia, mental retardation, adducted thumbs, spastic paraplegia, and/or hydrocephalus. Ll-deficient mice have been generated to establish an animal model for CRASH Syndrome. Mutant mice revealed a
4 Summary vü phenotype reminiscent to that of CRASH patients. The variability of the phenotype was low, with the only exception of hydrocephalus. Depending on the genetic background,mice either developed an apparentlynormal ventricular system, significantlyenlarged lateral ventricles, or severe macrocephalus. In contrast to affected male patients, heterozygous females are eonsidered to be healthy. The LI gene is located on the X-chromosome, and in females one X- chromosome is inactivated at random early during neural development. The nervous system of carrier females should thus consist of a mosaic of cells expressing either wild-type or mutated 1.1. Analysis of heterozygous female mice revealed an apparently normal development of the brain, and a mosaic of cells expressing either wild-type or mutant LI. Observations demonstrate that, on average, 50% of all normally LI-positive cells have to expresswild-type LI to allow normal brain development. CELLI (dose homolog of El) is a recently identified cell recognition molecule of the LI family expressed in nervous tissue. CEIL1 mediales adhesion by heterophilic interactions,and supports neurite elongationin vitro. To obtain first insights into possible functions of CHL1 in vivo, its expressionwas studied in the lesioned optic nerve. Expression of CHL1 was strongly upregulated by optic nerve glial cells in response to an optic nerve crush, both at the mrnaand the protein level. Furthermore, application of exogeneousbfgf also induced. upregulation of CHL1 by CNS glial cells. Observations demonstrate that CHL1 is a novel marker for reactive astrogliosis, and suggest important functional roles of CHL1 in the lesioned CNS.
5 Zusammenfassung Vlll Zusammenfassung LI und CHL1 ("close homolog of LI") gehören zu der Ll-Familie der Zeilerkennungsmoleküle und es wird vermutet, dass beide Proteine eine wichtige Rolle während der Entwicklungdes Nervensystemsund im adulten und lädierten Nervengewebespielen. LI beeinflusst verschiedene Prozesse wie Migration von Nervenzellen, Auswachsen, Bündelung und.richtungsabhängigeswachsen von Axonen, Myelinisierung im peripheren Nervensystem (PNS) und synaptische Plastizität. Obwohl eine detaillierte, funktionelle Charakterisierung von CHE! noch aussteht, ist gezeigt worden, dass CHL1 das Auswachsen von Neuriten in vitro unterstützt. Experimentell manipulierte und genetisch veränderte Maus-Mutanten wurden analysiert, um weitere Erkenntnisse in die funktionellen Rollen beider Proteine in vivo zu gewinnen. Die Unfähigkeit zur axonalen Regeneration im zentralen Nervensystem (ZNS) der Säuger konnte auf inhibitorischemolekülezurückgeführt werden, die von glialen Zellen exprimiert werden und die die Regeneration von Axonen verhindern. Die geringe Zahl von Oberflächen-Molekülen auf differenzierten Gliazellen im ZNS mit Eigenschaften, die das Neuritenwachstum fördern, könnte ebenfalls die Unfähigkeit zur Regeneration im adulten Säuger-ZNS erklären. Um diese Hypothese zu testen, wurde die axonale Regeneration im optischen Nerv von transgenen Mäusen studiert, welche LI ektopisch in Astrozyten unter regulatorischen Sequenzen des "glial fibrillary acidic protein" (GFAP) exprimieren.verschiedene transgenemauslinien wurden untereinander gekreuzt, um die Expression des transgenen LI zu erhöhen. Exogener "basic fibroblastgrowth factor" (bfgf), welcher die GFAP Expression erhöht, wurde appliziert, um die Expression des Transgenes weiter zu erhöhen. Eine erhöhte Expression des Transgens auf mrna- und Protein-Niveau konnte in den retinalen Müller-Zellengefundenwerden. Trotz der Tatsache, dass eine erhöhte Menge an transgenemli in Gliazellen des ZNS exprimiertwurde, regenerierten die Axone der retinaler Ganglienzellen in den transgenen Mäusen nicht besser als in Wildtyp-Mäusen.Folglich sind erhöhte Mengen an transgenem LI auf Gliazellen im ZNS nicht ausreichend,um die inhibitorischen Eigenschaftendes adulten ZNS Gewebes zu überwiegen. -fco Dass LI eine bedeutenderolle bei der Entwicklungdes Gehirns spielt, wird durch die Tatsache deutlich, dass Mutationen im Ll-Gen gravierende.missbildungen im Gehirn verursachen.diese Missbildungen werden unter der
6 Zusammenfassung IX Bezeichnung CRASEI zusammengefasst. CRASFI-Patienten zeigen eine komplexe und unterschiedliche Ausprägung der Krankheit, sowohl innerhalb verschiedenerfamilien aber auch innerhalb derselbenfamilie. Typische Defekte im Zusammenhang mit dem CRASH Syndrom beinhalten: Corpus Callosum Hypoplasie, Retardierung, angewinkelte Daumen (adducted fhumbs), Spastische Paraplegie und/oder Hydrozeph.al.us. Um ein Mausmodell für CRASH zu etablieren, wurde eine Mutante generiert, welche LI vermindert exprimiert. Diese Ll-mutanten Mäuse zeigten einen ähnlichen Phänotyp CRASH-Patienten.Abgesehen wie von der Ausprägung eines Elydrozephalus war die Variabilität des Phänotypsgering. Abhangend vom genetischenhintergrund entwickelten die Mäuse entweder ein normales ventrikuläres System, eine signifikante Vergrösserung der lateralen Ventrikel oder massiven Makrozephalus. Im Gegensatz zu den erkrankten männlichenpatienten scheinen heterozygote Frauen gesund zu sein. Das Ll-Gen ist auf dem X-Chromosom lokalisiert. Von den beiden X-Chromosomen einer Zelle wird ein beliebiges, zufällig ausgewähltes X-Chromosom bei Frauen während der frühen Entwicklung des Gehirns inaktiviert. Das Nervensystem von heterozygoten Frauen sollte daher aus einem Mosaik von Zellen bestehen, die entweder normalesoder mutiertes LI exprimieren. Die Untersuchungen zeigen, dass durchschnittlich 50% aller normalerweisell-positivenzellen Wildtyp-Ll exprimieren müssen, um eine normale Entwicklung des Gehirns zu gewährleisten. CHL1 (close homolog of Li) ist ein kürzlich identifiziertes Zeilerkennungsmolekül der Ll-Familie, welches im Nervengewebeexprimiert wird. CHL1 fördert die Adhäsion durchheterophile Interaktion und unterstützt in vitro das Neuritenwachstum.Um erste Einblicke in mögliche Funktionen von CHL'l in vivo zu gewinnen, wurde die Expression von CHL1 im lädierten optischen Nerv untersucht. Die Expression von CEIL1 war in Gliazellen des optischen Nervs stark erhöht. Diese Beobachtungen zeigen, dass CHL1 eine neuer Marker für reaktive Astrozyten ist, und deuten auf eine wichtige, funktionelle Rolle von CHL1 im lädierten ZNS hin.
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