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Myasthenia Gravis Patients Human Thymus and Thymomas from And Functional Expression of Receptors for Calcitonin Gene-Related Peptide, Calcitonin, and Vasoactive Intestinal Peptide in the Human Thymus and Thymomas from This information is current as Myasthenia Gravis Patients of September 29, 2021. J.-C. Marie, A. Wakkach, A.-M. Coudray, E. Chastre, S. Berrih-Aknin and C. Gespach J Immunol 1999; 162:2103-2112; ; http://www.jimmunol.org/content/162/4/2103 Downloaded from References This article cites 57 articles, 18 of which you can access for free at: http://www.jimmunol.org/content/162/4/2103.full#ref-list-1 http://www.jimmunol.org/ Why The JI? Submit online. • Rapid Reviews! 30 days* from submission to initial decision • No Triage! Every submission reviewed by practicing scientists • Fast Publication! 4 weeks from acceptance to publication by guest on September 29, 2021 *average Subscription Information about subscribing to The Journal of Immunology is online at: http://jimmunol.org/subscription Permissions Submit copyright permission requests at: http://www.aai.org/About/Publications/JI/copyright.html Email Alerts Receive free email-alerts when new articles cite this article. Sign up at: http://jimmunol.org/alerts The Journal of Immunology is published twice each month by The American Association of Immunologists, Inc., 1451 Rockville Pike, Suite 650, Rockville, MD 20852 Copyright © 1999 by The American Association of Immunologists All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. Functional Expression of Receptors for Calcitonin Gene-Related Peptide, Calcitonin, and Vasoactive Intestinal Peptide in the Human Thymus and Thymomas from Myasthenia Gravis Patients1 J.-C. Marie,2,3* A. Wakkach,2† A.-M. Coudray,* E. Chastre,* S. Berrih-Aknin,† and C. Gespach4* The molecular and functional expression of serpentine membrane receptors for vasoactive intestinal peptide (VIP), calcitonin gene-related peptide (CGRP), and calcitonin (CT) were characterized in human thymus and thymomas from myasthenia gravis (MG) patients and thymic epithelial cells either in primary culture (PTEC) or transformed by the siman virus 40 large T (SV40LT) Downloaded from oncogene (LT-TEC). Using RT-PCR combined with Southern analysis, we identified the PCR products corresponding to the receptor (-R) transcripts for VIP, CGRP, and CT in thymus from control subjects and MG patients with either hyperplasia or thymoma. Similar expressions of the VIP- and CGRP-R transcripts were observed in PTEC, whereas the CT-R message was not detected. In LT-TEC, the signals for VIP-R, CGRP-R, and CT-R transcripts were seen with a lower intensity than those in control and MG thymus. In agreement with our molecular analysis, 1) VIP was the most potent peptide among VIP-related peptides (VIP > PACAP > PHM > PHV) to stimulate cAMP production through specific type 1 VIP receptors in both PTEC and LT-TEC; http://www.jimmunol.org/ 2) cAMP generation was induced by CGRP in PTEC and by CT in LT-TEC; 3) in frozen thymic sections and by flow cytometry, type 1 VIP-R, CGRP-R, and CT-R were localized in epithelial cells; and 4) in parallel, the transcription of the acetylcholine receptor a subunit (the main autoantigen in MG) was induced by CGRP and CT in PTEC and LT-TEC, respectively. Our data suggest that the neuroendocrine peptides VIP, CGRP, and CT may exert functional roles during MG and malignant transfor- mation of the human thymus. The Journal of Immunology, 1999, 162: 2103–2112. he thymus is an essential organ in the differentiation and ment through the release of cytokines and inhibition of stromal maturation of lymphoid precursor cells into mature T epithelial cell proliferation (10). by guest on September 29, 2021 T lymphocytes (1–4). These precursors, derived from bone The cellular heterogeneity of the thymus and the cross-talk be- marrow stem cells, are subjected to positive and negative selec- tween the different cell types constitute the main limit in under- tions by thymic stromal cells, including dendritic cells, macro- standing the physiology and pathophysiology of the thymus. phages, and epithelial cells (5–7). In this context, thymic epithelial Pathological thymi, including thymic hyperplasia and thymoma, cells have been shown to protect thymocytes from apoptosis (8) are frequently found in myasthenia gravis (MG),5 and MG patients and to promote the maturation of the double-positive (CD41 and 1 1 2 are improved after thymectomy (11). Autosensitization to acetyl- CD8 ) thymocytes into single-positive cells CD4 CD8 , choline receptors (AChR), which is the main autoantigen impli- CD42CD81 (9). In turn, thymocytes also modulate their environ- cated in MG, is thought to take place in the thymus (12). AChR a subunit (a-AChR) transcripts have been shown to be up-regulated by the neuropeptide calcitonin gene-related peptide (CGRP) in *Institut National de la Sante´et de la Recherche Me´dicale, Unit 482, Signalisation et chicken myocytes in primary culture (13). Thus, such an effect Fonctions Cellulaires, Applications au Diabe`te et aux Cancers Digestifs, Hoˆpital Saint-Antoine, Paris, France; and †Laboratoire d’Immunologie, Centre National de la occurring in the thymus would represent an important neuroendo- Recherche Scientifique-Unite´Propre de Recherche et de l’Enseignement Supe´rieur crine control in MG and thymic neoplasia. CGRP is a 37-amino Associe´e, Hoˆpital Marie Lannelongue, Le Plessis-Robinson, France acid peptide generated by tissue-specific alternative processing of Received for publication February 23, 1998. Accepted for publication November the calcitonin/CGRP gene transcript in central and peripheral neu- 30, 1998. rons (14, 15). Several neuroendocrine peptides, such as vasoactive The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked advertisement in accordance intestinal peptide (VIP), are also involved in the regulation of im- with 18 U.S.C. Section 1734 solely to indicate this fact. mune responses (16, 17). VIP is a 28-amino acid neuropeptide 1 This work was supported by the Institut National de la Sante´et de la Recherche Me´dicale, the Centre National de la Recherche Scientifique, and research grants from Association Franc¸aise contre les Myopathies, la Ligue Contre le Cancer, and Caisse Nationale d’Assurance Maladie des Travailleurs Salarie´s. 2 J.-C.M. and A.W. contributed equally. 5 Abbreviations used in this paper: MG, myasthenia gravis; AChR, acetylcholine receptors; a-AChR, a subunit of AChR; CGRP, calcitonin gene-related peptide; VIP, 3 Current address: Laboratoire de Physiopathologie de la Nutrition, Centre National vasoactive intestinal polypeptide; PACAP-38, pituitary adenylate cyclase-activating de la Recherche Scientifique et de l’Enseignement Supe´rieur Associe´e 7059, Univer- polypeptide; CT, calcitonin; PTEC, thymic epithelial cells in primary culture; LT- site´Paris 7, 75251 Paris Cedex 05, France. TEC, thymic epithelial cells transformed by the simian virus 40 large T oncogene; 4 Address correspondence and reprint requests to Dr. C. Gespach, Institut National de PHM, peptide with NH2-terminal histidine and C-terminal methionine; PHV, peptide la Sante´et de la Recherche Me´dicale, Unit 482, Signalisation et Fonctions Cellulaires, with NH2-terminal histidine and C-terminal valine; TGLP-1, truncated glucagon-like Applications au Diabe`te et aux Cancers Digestifs, Hoˆpital Saint-Antoine, 75571 Paris peptide-1; IAPP, islet amyloid polypeptide; pAbs, polyclonal Abs; RAMPS, receptor Cedex 12, France. E-mail address: [email protected] activity-modifying proteins; RCP, receptor component protein. Copyright © 1999 by The American Association of Immunologists 0022-1767/99/$02.00 2104 NEUROENDOCRINE PEPTIDE RECEPTORS IN HUMAN THYMUS structurally related to glucagon, pituitary adenylate cyclase-acti- software. The percentage of contaminating macrophages in thymic epithe- vating peptide (PACAP), and secretin (18). These regulatory pep- lial cell cultures was determined using anti-HLA-DR Abs (Dako, Trappes, tides exert their biological activities through activation of specific France). Most contaminant fibroblasts were eliminated by selective trypsinization. They represent ,10% of the total cell population as as- membrane receptors (19). These receptors have seven transmem- sessed by FACS analysis using anti-collagen III Ab (ICN, Costa Mesa, brane domains and are positively coupled to adenylyl cyclase. Sub- CA). The thymic epithelial cell population (at least 90% enriched), ob- types of VIP and CGRP/calcitonin (CT) receptors were identified tained after selective resistance to trypsin, was then used for PTEC culture on the basis of pharmacological and molecular analysis. VIP- and and SV40-LT transformation (see below). To obtain evidence of VIP-R expression in PTEC and LT-TEC1 cells in CGRP-immunoreactive fibers were identified in the thymus, and culture, we used the rabbit polyclonal Ab (pAb) A directed against the first both neuropeptides were reported to inhibit IL-2 production and extracellular loop of this serpentine receptor (26) at a dilution of 1/100 in proliferation of thymocytes in vitro (20–22). Further, VIP has been PBS. Primary and SV40-LT-transformed thymic cells were then washed, shown to rescue the immature double-positive CD41CD81 thy- incubated with goat anti-rabbit bound to tetramethylrhodamine isothiocya- mocytes from the glucocorticoid-induced apoptosis (23, 24). Thus, nate (Immunotech, Marseille, France), and washed twice in PBS. To our knowledge, there is no available CGRP-R or CT-R Ab. We it can be postulated that VIP exerts its protective effects against therefore biotinylated the CGRP and CT peptides according to the immu- apoptosis in thymocytes through an indirect action on thymic ep- noprobe biotinylation kit, as described by the manufacturer (Sigma, Saint- ithelial cells. Quentin Fallavier, France). Biotinylated CGRP or CT was incubated for 60 In the current hypotheses that neuroendocrine peptides exert a min with PTEC and LT-TEC1 cells, then unbound probe was eliminated by three washes, and fluorescence was revealed by avidin-phycoerythrin (Im- regulatory role on the development of the thymus and its immune munotech).
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