* Special issue dedicated to Dr. Guido Tettamanti. 1 Department of Neurology, The Johns Hopkins University School of Medicine, Baltimore, Maryland 21205; present address: Meikai University, School of Dentistry, Saitama 350-0283, Japan. 2 Departments of Pharmacology and Neuroscience, The Johns Hop- kins University School of Medicine, Baltimore, Maryland 21205. 3 Department of Neurogenetics Research, Kennedy Krieger Insti- tute, and Departments of Neurology and Pediatrics, Johns Hopkins University School of Medicine, Baltimore, Maryland 21205. 4 Address reprint requests to: Ronald L. Schnaar, Department of Pharmacology, The Johns Hopkins School of Medicine, 725 N. Wolfe Street, Baltimore, Maryland 21205. Tel: (410) 955-8392; Fax: (410) 955-4900; E-mail: schnaar@jhu.edu Anti-Ganglioside Antibodies Bind with Enhanced Affinity to Gangliosides Containing Very Long Chain Fatty Acids* Yumi Tagawa, 1 Wouter Laroy, 2 Leonardo Nimrichter, 2 Susan E. Fromholt, 2 Ann B. Moser, 3 Hugo W. Moser, 3 and Ronald L. Schnaar 2,4 (Accepted April 5, 2002) Gangliosides function in both physiological and pathological molecular recognition. Although much research has focused on the role of ganglioside glycans in recognition, fewer studies have addressed the role of the ceramide moiety. Ceramides of major brain gangliosides are composed predominantly of monounsaturated 18-carbon and 20-carbon long chain bases with a saturated 18-carbon fatty acid amide. In contrast, gangliosides of X-linked adrenoleukodystrophy patients are characterized by abnormal very long chain fatty acids that are proposed to be associated with autoimmune inflammation. In the current study we synthesized and characterized derivatives of the major brain ganglioside GD1a bearing defined very long chain fatty acid amides (C24:0, C24:1, and C26:0). When tested in a solid phase binding assay in the presence of auxiliary mem- brane lipids, GD1a species with long chain fatty acids were up to 8-fold more potent than nor- mal brain GD1a in binding four different anti-GD1a monoclonal antibodies. These data support the hypothesis that gangliosides bearing very long chain fatty acids are differentially displayed on membranes, which may lead to altered antigenicity. KEY WORDS: GD1a; adrenoleukodystrophy; autoimmune disease; ceramide. Neurochemical Research, Vol. 27, Nos. 7/8, August 2002 (© 2002), pp. 847–855 847 0364-3190/02/0800–0847/0 © 2002 Plenum Publishing Corporation nervous system gangliosides act as both physiological and pathological recognition molecules, binding to en- dogenous lectins (3), toxins (4), and autoimmune anti- bodies (5,6). Brain gangliosides comprise a highly varied family of molecules sharing a sialylated oligosac- charide moiety and a ceramide lipid moiety (2,7,8). Although many studies have evaluated the role of oligosaccharide structure in the recognition of gan- gliosides, fewer have addressed the role of the ceramide, which may impact the physical presentation, and there- fore recognition, of gangliosides at the cell surface (9,10). In normal adult human brain, the ceramide moieties of major gangliosides (GM1, GD1a, GD1b, and GT1b) have predominantly monounsaturated 18- or 20-carbon long chain bases (d18:1, d20:1) and an 18-carbon saturated fatty acid amide (C18:0), although 10% of each species carries a C20:0 and 1% a INTRODUCTION Gangliosides are broadly distributed in vertebrate tissues, but are expressed in especially high abundance in the nervous system (1,2). Among other functions,