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Pulp Border in L1-Deficient Mice Selective Malformation of the Splenic White Selective Malformation of the Splenic White Pulp Border in L1-Deficient Mice Shih-Lien Wang, Michael Kutsche, Gino DiSciullo, Melitta Schachner and Steven A. Bogen This information is current as of September 27, 2021. J Immunol 2000; 165:2465-2473; ; doi: 10.4049/jimmunol.165.5.2465 http://www.jimmunol.org/content/165/5/2465 Downloaded from References This article cites 45 articles, 12 of which you can access for free at: http://www.jimmunol.org/content/165/5/2465.full#ref-list-1 Why The JI? Submit online. http://www.jimmunol.org/ • 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 *average by guest on September 27, 2021 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 © 2000 by The American Association of Immunologists All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. Selective Malformation of the Splenic White Pulp Border in L1-Deficient Mice1 Shih-Lien Wang,* Michael Kutsche,† Gino DiSciullo,* Melitta Schachner,† and Steven A. Bogen2* Lymphocytes enter the splenic white pulp by crossing the poorly characterized boundary of the marginal sinus. In this study, we describe the importance of L1, an adhesion molecule of the Ig superfamily, for marginal sinus integrity. We find that germline insertional mutation of L1 is associated with a selective malformation of the splenic marginal sinus. Other splenic structures remain intact. Immunofluorescence analysis of the extracellular framework of the spleen, using an Ab to laminin, reveals that L1 knockout mice have an irregularly shaped, discontinuous white pulp margin. Electron microscopic analysis shows that it is associated with bizarrely shaped marginal sinus lining cells at the periphery of the white pulp. These abnormalities correlate with the localization of L1 in normal mice in that L1 is normally expressed on marginal sinus lining cells at the white pulp border. These Downloaded from L1-immunopositive lining cells coexpress high levels of mucosal addressin cell adhesion molecule-1 and vimentin, indicating that they are of fibroblastic lineage and express a well-characterized addressin. Our findings are the first to implicate L1 in splenic lymphoid architectural development. Moreover, these findings help define the poorly characterized sinusoidal boundary across which mononuclear cells cross to enter the splenic white pulp. The Journal of Immunology, 2000, 165: 2465–2473. ononuclear cells enter lymphoid organs via two dis- nicates, directly or indirectly, with the blood vascular system (4– http://www.jimmunol.org/ tinct routes. Although the blood vascular route has 6). Ultrastructurally, the marginal sinus wall is more analogous to M been a major focus of interest over the last decade, the LN sinusoidal lining cells than blood vascular endothelium. there is a paucity of information about mononuclear cell passage Namely, both types of sinusoidal lining cells associate with a sim- across sinusoidal walls. Specifically, mononuclear cells, such as ilar type of protein matrix, do not assume the tall morphology often macrophages, lymphocytes, and dendritic cells, travel from the site associated with postcapillary venules, and do not have a known of Ag contact to a draining lymphoid organ. In the context of a intercellular junction capable of regulating fluid and solute flow. It 3 lymph node (LN), mononuclear cells drain into the subcapsular is across this boundary that mononuclear cells must cross to enter sinus, enter the cortical sinusoids, and then migrate into the lym- the splenic white pulp. by guest on September 27, 2021 phoid parenchyma by crossing the relatively poorly defined bound- We are particularly interested in identifying the underlying ad- ary of the sinusoidal lining. This lining comprises a single layer of hesion molecules that mediate structural features of sinusoidal lin- flattened cells associated with collagen fibrils and extracellular ma- ings. To this end, we have focused our attention on the L1 adhe- trix proteins, such as laminin (1, 2). Comparatively little is known sion molecule. L1 is a 1260-aa-long Ig superfamily adhesion about the physiological properties of this lining, such as the ex- molecule (7). It has been implicated in several important neurobi- pression of adhesion molecules, mechanisms of locomotion of ological processes, including neurite outgrowth, neurite fascicula- mononuclear cells along the lining surface, or whether the sinu- tion, axon-Schwann cell interaction, myelination, neuronal cell mi- soidal wall is porous or relatively impermeable to the free flow of gration, and synaptic plasticity (8–12). L1 acts homophilically and macromolecules and cells (3). heterophilically (8, 13, 14). The importance of L1 in neuronal de- In the spleen, the most analogous structure to the LN sinusoid is velopment is reflected by the fact that mutations in the human L1 the marginal sinus. The marginal sinus lining cells are a thin layer gene lead to a group of neurological syndromes (15, 16). of flattened cells that envelop the white pulp. These flattened cells Although L1 was initially identified in the nervous system, L1 is form the inner layer of the marginal sinus, a space that commu- also expressed in nonneuronal tissues. Specifically, L1 is ex- pressed by cells of hematopoietic origin (17, 18), intestinal epi- *Department of Pathology and Laboratory Medicine, Boston University School of thelial cells (19), epithelium of the male urogenital tract (20), and Medicine, Boston, MA 02118; and †Zentrum fu¨r Molekulare Neurobiologie, Univer- sita¨t Hamburg, Hamburg, Germany other cells of epithelial origin (21). The functional role of L1 on Received for publication December 22, 1999. Accepted for publication June 13, 2000. these cells is largely unexplored. L1 has been implicated in an in vitro cell binding assay between lymphocytes and bend 3 endo- 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 thelioma cells, raising the possibility of a potential role in lym- with 18 U.S.C. Section 1734 solely to indicate this fact. phocyte-endothelial cell interactions (22). It is also involved in 1 This work was supported by National Institutes of Health Grant 1R29AI34562 to kidney morphogenesis (23). S.A.B. Previous data from our laboratory implicated the Ig superfamily 2 Address correspondence and reprint requests to Dr. Steven A. Bogen, Department of adhesion molecule L1 in maintaining normal sinusoidal structure Pathology and Laboratory Medicine, Boston University School of Medicine, Boston, MA 02118. E-mail address: [email protected] in LNs during immune hypertrophy (24). Specifically, we found 3 Abbreviations used in this paper: LN, lymph node; FDC, follicular dendritic cell; that in vivo administration of an L1 mAb disrupted the normal KO, knockout; MMM, marginal metallophilic macrophage; NRIgG, normal nonim- remodeling of the cortical sinusoidal lining cells of LNs during an mune rat IgG; RT, room temperature; DAB, 3,3Ј-diaminobenzidine; SLC, sinus lining cell; RC, reticular cell; MAdCAM-1, mucosal addressin cell adhesion molecule-1; immune response. The L1 mAb did not disrupt static, quiescent PECAM-1, platelet endothelial cell adhesion molecule-1. sinusoidal lining cells. Rather, it interfered only with sinsusoidal Copyright © 2000 by The American Association of Immunologists 0022-1767/00/$02.00 2466 MALFORMATION OF THE WHITE PULP BORDER IN L1 KO MICE lining cells mediating the process of matrix remodeling induced by was no opportunity for confusion to arise. The brown DAB precipitate immune stimulation. A limitation with the in vivo L1 Ab study was denoting endogenous peroxidase is easily distinguished on bright-field op- that it required a xenogenic rat anti-mouse L1 mAb. Consequently, tics from the fluorescent signal identifying the location of Ags of interest. The 324 (anti-L1) mAb or NRIgG control were applied at 0.1 ␮g/ml, a mouse (host) anti-rat IgG immune response developed 10–14 Ј followed by donkey anti-rat IgG (Fab )2-biotin at a 1/1000 dilution. All days after L1 mAb administration. This model was therefore useful incubations were performed at RT for 40 min. Subsequently, streptavidin- only in short term studies, such as acute hypertrophic responses to peroxidase and tyramide-FITC were applied and incubated as per the man- immune stimulation. ufacturer’s recommendations. Between each step, the sections were washed three times for 5 min in PBS, 0.1% Tween 20. Because of the structural similarities between the splenic mar- For two-color staining of L1 and MAdCAM-1, we modified the proce- ginal sinus and LN cortical sinusoids, we hypothesize that the dure to distinguish the two rat mAbs with two distinct fluorochromes (flu- splenic marginal sinus may also be reliant on the L1 adhesion orescein and Texas Red). L1 was first detected as described above, except molecule for structural integrity. To elucidate the role of L1 in the that the 324 mAb was applied
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