presented by Dipl. accepted Reprints from: Immunobiology (1992) 186:160 (Abstract) CLONING AND CHARACTERIZATION OF TRAP (CD40 LIGAND)
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1 Diss ETH No CLONING AND CHARACTERIZATION OF TRAP (CD40 LIGAND) AND ITS ROLE IN THE PRIMARY IMMUNODEFICIENCY X-LINKED IMMUNODEFICIENCY WITH HYPER-IGM' A dissertation submitted to the SWISS FEDERAL INSTITUTE OF TECHNOLOGY ZURICH for the degree of Doctor of Natural Sciences presented by Daniel Graf Dipl. Natw. ETH born November 22,1965 citizen of Luzern (LU) accepted on the recommendation of Prof. Dr. H. Hengartner, examiner PD Dr. R.A. Kroczek, coexaminer 1994 Reprints from: Immunobiology (1992) 186:160 (Abstract) Eur. J. Immunol. (1992) 22: Nature (1992) 361:
2 -6-1. SUMMARY T cell activation, which is critical for most specific immune responses, requires two sets of signals. The first signal is delivered through the TCR/CD3 complex and accounts for the clonality of activation. The second or accessory signal is delivered by antigen presenting cells (APC) and is not clearly defined. Subsequent to this initial activation a complex process is started which leads to T cell differentiation and proliferation. On the molecular level this process induces the up regulation and de novo transcription of more than 100 genes. However, only some of these genes require the synergistic action of both signals. Because of this characteristic these genes are likely to encode proteins critical for T cell fate and function. Based on a collection of 100 T cell activation genes, a multigene analysis system was established which links distinct activation signals to subsequent gene expression. T cells were stimulated with the phorbol ester PMA + the Ca++-ionophore A23187, which replace both physiologic stimuli and induce T cell proliferation, or with either compound alone, which is not sufficient for proliferation, to identify those genes whose expression is dependent on both signals. One particular cdna clone identified by this system was exclusively expressed in activated T cells. The polypeptide encoded by a mrna of approximately 2.3 kb is 261 amino acids long with a molecular weight of 33 kda. The structural features predict a type II transmembrane protein, but are also compatible with a secreted form. The protein belongs to the tumor necrosis factor/lymphotoxin cytokine family, hence its name TRAP (TNF related activation protein). TRAP is highly similar to an identified murine ligand for CD40 both at the protein level (77.4%) and the nucleotide level (82.8%). Expressed on the surface of a murine myeloma cell line, TRAP was identified as a physiological human ligand for CD40 by its ability to bind to a soluble CD40 molecule. Signaling for the B cell immunoglobulin isotype switch requires T cell derived cytokines and T/T3 cell interaction, which operates primarily through the CD40 molecule on B cells. The primary immunodeficiency X-linked immunodeficiency with hyper-igm (HIGM1) is characterized by an immunoglobulin isotype switch defect and has been assigned to the q26 region of the X-chromosome. An isolated genomic clone for TRAP was used to map its gene to the q region of the X-chromosome, suggesting a causal relationship between TRAP and HIGM1. Peripheral blood T cells of three individuals with HIGM1 were analyzed and found to be unable to bind a soluble CD40 molecule. Subsequent genetic analysis revealed for all three patients single point mutations within the coding region of TRAP incompatible
3 -7- with functional cell surface expression. Thus the failure of TRAP to interact with CD40 on functionally intact B cells is responsible for the observed immunoglobulin defect in HIGM1. This finding reveals the critical role of TRAP for the immunoglobulin isotype switch. Subsequently the induction requirements for TRAP expression were further analyzed in vitro. To this end two monoclonal antibodies were generated against TRAP and initially characterized. TRAP mrna is expressed rapidly and independent of de novo protein synthesis. Its expression is highly sensitive to CsA both on the mrna and on the protein levels. Doses of 100 ng/ml CsA suppress its expression to 95%. The CsA dose/response curve found for TRAP is similar to the one for the IL-2 gene. Like the IL-2 gene, TRAP requires the synergistic stimulus of PMA and Ca++-ionophore for expression. Neither PMA, Ca++-ionophore, PHA or anti-cd3 alone are sufficient to induce TRAP cell surface expression to more than 2-5% of the induction obtained with PMA + A The early expression and the need for a synergistic stimulus define TRAP as the first so far described T-cell surface protein with a two-signal dependence. Its expression can therefore be used as a measure for 'complete't cell activation.
4 ZUSAMMENFASSUNG T-Zell Aktivierung ist fur die meisten spezifischen Immunantworten wichtig und wird durch zwei unabhangige Signale induziert. Das erste Signal wird vom T-Zell Rezeptor/CD3 Komplex vermittelt und steuert die Klonalitat der Aktivierung. Das zweite, akzessorische und noch nicht eindeutig identifizierte Signal wird von Antigen-prSsentierenden Zellen vermittelt. Auf die initiale Aktivierung folgt ein komplexer Prozess, der zu T-Zell Differenzierung und Proliferation fuhrt. Dabei werden auf molekularer Ebene mehr als 100 Gene neu oder verstitrkt transkribiert. Nur einige dieser Gene brauchen daftir aber das gemeinsame Eintreffen von Signal eins und zwei. Deswegen sind auf solchen Genen wahrscheinlich Schliisselproteine fiir Schicksal und Funktion der T-Zelle kodiert. Basierend auf einer einer Kollektion von 100 T-Zell Aktivierungsgenen wurde ein Multi-Gen Analyse' System entwickelt, um einzelne Signal-Transduktionswege mit darauffolgender Genexpression zu verkntipfen. T-Zellen wurden mit dem Phorbol Ester PMA, mit dem Ca++-Ionophor A23187, oder mit beiden Reagenzien gemeinsam stimuliert, um Gene zu identizifieren, deren Expression beide Substanzen braucht. PMA + A23187 zusammen eingesetzt ersetzen nsmlich die physiologischen Signale und regen T-Zellen zur Proliferation an, einzeln eingesetzt sind sie dazu nicht in der Lage. Eines der so identifizierten Gene war zusatzlich ausschliesslich in aktivierten T-Zellen zu finden. Seine etwa 2.3 kb lange mrna kodiert ein 261 Aminosauren langes und 33 kda schweres Protein mit strukturellen Eigenschaften, die sowohl mit einem Typ n Transmembran-protein als auch mit einem sezernierten Protein vereinbar sind. Das Protein gehort zur Familie des Tumor Nekrose Faktors und wurde deswegen TRAP genannt, was fiir Tumor Nekrose Faktor verwandtes Aktivierungsprotein (TNF related activation protein) steht. TRAP ist zu 77.4% auf der Proteinebene und zu 82.8% auf der NukleinsSureebene mit dem Maus CD40-Liganden verwandl Auf der Oberflache einer Maus Myelom Linie exprimiert kann TRAP an losliches CD40 binden und ist somit ein physiologischer humaner Ligand fur CD40. Die Induktion des B-Zell Immunglobulin-Isotyp Klassenwechsels braucht T-Zell Zytokine und eine T/B-Zell Interaktion. Bei letzterer spielt das CD40-Molektil der B-Zelle eine wichtige Rolle. Die primsre X-gebundene Immundefizienz mit Hyper-IgM (HIGM1) weist einen Defekt in diesem Klassenwechsel auf und wurde der q26 Region des X-Chromosomes zugeordnet. Ein genomischer Klon ftir TRAP wurde isoliert. Damit wurde das TRAP Gen der q Region des X- Chromosomes zugeordnet. Dies fuhrte zu der Vermutung, dass ein kausaler Zusammenhang zwischen TRAP und HIGM1 besteht T-Zellen aus dem peripheren Blut dreier Personen mit HIGM1 wurden analysiert. Es zeigte sich, dass sie kein losliches CD40 binden konnten. Darauffolgende genetische Analysen ergaben, dass alle drei Patienten einzelne Punkt-Mutationen im kodierenden Bereich des TRAP-Genes hatten,
5 -9- die unvereinbar mit einer funktionellen Expression des Molektiles sind. Die B-Zellen per funktionell intakt Demzufolge ist bei Personen mit HIGM1 die unterbrochene TRAP/CD40 Interaktion der Grand fiir die beobachtete defekte Immunglobulinsynthese. TRAP besetzt demzufolge beim Immunglobulin-Isotyp Klassenwechsel eine Schltisselposition. se waren Zusatzlich wurden die Bedingungen der TRAP-Expression zwei monoklonale AntikOrper gegen TRAP generiert in vitro weiter untersucht. Es wurden und initial charakterisiert TRAP mrna wird schnell und unabhsngig einer Protein-Neusynthese exprimiert. Seine Expression ist sowohl auf der mrna wie auch auf der Protein-Ebene hoch empfindlich auf das Immunsuppressivum Cyclosporin A, denn Dosen von 100 ng/ml verringern seine Expression zu 95%. Die Dosis/Wirkungs-Kurve fiir TRAP ist ahnlich der des Interleukin-2 (IL-2) Genes. Wie die IL-2 Induktion benotigt auch die TRAP Induktion ein gemeinsames Wirken von PMA + A Weder PMA, Ca++-Ionophor, Phytohaemagglutinin (PHA) oder anti-cd3 AntikOrper alleine k5nnen TRAP, im Vergleich zur synergistischen PMA + Ca++-Ionophor Stimulation, zu mehr als 2-5% auf der Zelloberflache induzieren. Die friihe Expression und ein zwingender synergistischer Stimulus definieren TRAP als das erste, bisher beschriebene T-Zelloberflachen-Protein mit einer 'Zwei-Signal-AbhSngigkeit'. Seine Expression kann demzufolge als Mass fiir eine 'vollstsndige' T- Zell Aktivierung eingesetzt werden.
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