Critical role of amino acid position 343 of surfactant protein-D in the selective binding of glycolipids from Mycobacterium tuberculosis.
Surfactant protein D (SP-D), a lectin that recognizes carbohydrates via its C-type carbohydrate recognition domains (CRDs), regulates Mycobacterium tuberculosis (M.tb)-macrophage interactions via recognition of M.tb mannosylated cell wall components. SP-D binds to, agglutinates, and reduces phagocytosis and intracellular growth of M.tb. Species-specific variations in the CRD amino acid sequence contribute to carbohydrate recognition preferences and have been exploited to enhance the antimicrobial properties of SP-D in vitro. Here, we characterized the binding interaction between several wild-type and mutant SP-D neck + CRD trimeric subunits (NCRDs) and pathogenic and nonpathogenic mycobacterial species. Specific amino acid substitutions (i.e., the 343-amino-acid position) that flank the carbohydrate binding groove led to significant increases in binding of only virulent and attenuated M.tb strains and to a lesser extent M. marinum, whereas there was negligible binding to M. avium complex and M. smegmatis. Moreover, a nonconserved mutation at the critical 321-amino-acid position (involved in Ca(2+) coordination) abrogated binding to M.tb and M. marinum. We further characterized the binding of NCRDs to the predominant surface-exposed mannosylated lipoglycans of the M.tb cell envelope. Results showed a binding pattern that is dependent on the nature of the side chain of the 343-amino-acid position flanking the SP-D CRD binding groove and the nature of the terminal mannosyl sugar linkages of the mycobacterial lipoglycans. We conclude that the 343 position is critical in defining the binding pattern of SP-D proteins to M.tb and its mannosylated cell envelope components.
Carlson
Tracy K
TK
Division of Infectious Diseases, Department of Internal Medicine, Center for Microbial Interface Biology, The Ohio State University, Columbus, OH 43210, USA.
Torrelles
Jordi B
JB
Smith
Kelly
K
Horlacher
Tim
T
Castelli
Riccardo
R
Seeberger
Peter H
PH
Crouch
Erika C
EC
Schlesinger
Larry S
LS
D000595:Amino Acid Sequence; D000942:Antigens, Bacterial / Q000737:chemistry / Q000378:metabolism*; D001665:Binding Sites / Q000235:genetics; D002240:Carbohydrate Sequence; D006017:Glycolipids / Q000737:chemistry / Q000378:metabolism*; D006801:Humans; D008954:Models, Biological; D008969:Molecular Sequence Data; D050505:Mutant Proteins / Q000737:chemistry / Q000378:metabolism; D009169:Mycobacterium tuberculosis / Q000737:chemistry / Q000378:metabolism; D010716:Phosphatidylinositols / Q000737:chemistry / Q000378:metabolism; D011485:Protein Binding / Q000235:genetics; D054730:Protein Interaction Domains and Motifs / Q000235:genetics; D055503:Protein Multimerization / Q000502:physiology; D037663:Pulmonary Surfactant-Associated Protein D / Q000737:chemistry* / Q000235:genetics / Q000378:metabolism*; D013379:Substrate Specificity
D000942:Antigens, Bacterial; D006017:Glycolipids; D050505:Mutant Proteins; D010716:Phosphatidylinositols; D037663:Pulmonary Surfactant-Associated Protein D; C054977:phosphatidylinositol dimannoside; C072681:Mycobacterium tuberculosis antigens
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