title: Critical role of amino acid position 343 of surfactant protein-D in the selective binding of glycolipids from Mycobacterium tuberculosis.
abstract: 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.
authors.affiliation: Division of Infectious Diseases, Department of Internal Medicine, Center for Microbial Interface Biology, The Ohio State University, Columbus, OH 43210, USA.
authors.forename: Tracy K
authors.initials: TK
authors.lastname: Carlson
authors.forename: Jordi B
authors.initials: JB
authors.lastname: Torrelles
authors.forename: Kelly
authors.initials: K
authors.lastname: Smith
authors.forename: Tim
authors.initials: T
authors.lastname: Horlacher
authors.forename: Riccardo
authors.initials: R
authors.lastname: Castelli
authors.forename: Peter H
authors.initials: PH
authors.lastname: Seeberger
authors.forename: Erika C
authors.initials: EC
authors.lastname: Crouch
authors.forename: Larry S
authors.initials: LS
authors.lastname: Schlesinger
mesh_terms: 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
chemical_list: D000942:Antigens, Bacterial; D006017:Glycolipids; D050505:Mutant Proteins; D010716:Phosphatidylinositols; D037663:Pulmonary Surfactant-Associated Protein D; C054977:phosphatidylinositol dimannoside; C072681:Mycobacterium tuberculosis antigens
references.citation: Biochem J. 2002 Aug 15;366(Pt 1):87-96
references.pmid: 11971759
references.citation: J Lipid Res. 2005 Mar;46(3):475-83
references.pmid: 15576843
references.citation: Biochim Biophys Acta. 2002 Sep 19;1572(2-3):364-86
references.pmid: 12223280
references.citation: Biochimie. 2003 Jan-Feb;85(1-2):153-66
references.pmid: 12765785
references.citation: J Immunol. 2002 Feb 1;168(3):1309-14
references.pmid: 11801670
references.citation: Infect Immun. 2006 Dec;74(12):7005-9
references.pmid: 17030585
references.citation: J Biol Chem. 2005 Apr 29;280(17):17046-56
references.pmid: 15711012
references.citation: Chembiochem. 2004 Mar 5;5(3):379-82
references.pmid: 14997532
references.citation: J Biol Chem. 1995 May 26;270(21):12380-9
references.pmid: 7759478
references.citation: Structure. 1999 Mar 15;7(3):255-64
references.pmid: 10368295
references.citation: J Immunol. 1999 Jul 1;163(1):312-21
references.pmid: 10384130
references.citation: Glycobiology. 2009 Jul;19(7):743-55
references.pmid: 19318518
references.citation: Glycobiology. 1995 Feb;5(1):117-27
references.pmid: 7772860
references.citation: J Biol Chem. 2001 Aug 3;276(31):28939-45
references.pmid: 11384997
references.citation: J Immunol. 2003 Aug 15;171(4):2014-23
references.pmid: 12902506
references.citation: Methods Mol Biol. 1998;101:91-107
references.pmid: 9921472
references.citation: Mol Immunol. 2006 Mar;43(9):1293-315
references.pmid: 16213021
references.citation: Biochemistry. 2009 Apr 21;48(15):3335-45
references.pmid: 19249874
references.citation: J Biol Chem. 2003 Feb 21;278(8):5513-6
references.pmid: 12496255
references.citation: Am J Respir Cell Mol Biol. 2006 Jul;35(1):84-94
references.pmid: 16514117
references.citation: J Immunol. 1996 Nov 15;157(10):4568-75
references.pmid: 8906835
references.citation: J Biol Chem. 2004 Sep 24;279(39):41227-39
references.pmid: 15263002
references.citation: Biochim Biophys Acta. 1998 Nov 19;1408(2-3):278-89
references.pmid: 9813367
references.citation: Biochemistry. 2007 May 1;46(17):5160-9
references.pmid: 17417879
references.citation: J Immunol. 2006 Aug 1;177(3):1805-16
references.pmid: 16849491
references.citation: Mol Microbiol. 2004 Jul;53(2):391-403
references.pmid: 15228522
references.citation: Immunobiology. 2004;209(1-2):117-27
references.pmid: 15481146
references.citation: Mol Microbiol. 2005 Nov;58(3):774-90
references.pmid: 16238626
references.citation: J Exp Med. 2005 Oct 3;202(7):987-99
references.pmid: 16203868
references.citation: J Mol Biol. 2003 Aug 8;331(2):509-23
references.pmid: 12888356
references.citation: J Biol Chem. 1997 Sep 12;272(37):23094-103
references.pmid: 9287310
references.citation: J Immunol. 1990 Apr 1;144(7):2771-80
references.pmid: 2108212
references.citation: Front Biosci. 1998 Aug 06;3:e149-63
references.pmid: 9696885
references.citation: J Biol Chem. 1994 Jun 24;269(25):17311-9
references.pmid: 8006040
references.citation: J Immunol. 1994 Apr 15;152(8):4070-9
references.pmid: 8144972
references.citation: Tuberculosis (Edinb). 2008 Nov;88(6):560-5
references.pmid: 18539533
references.citation: Biochem J. 2005 Dec 15;392(Pt 3):615-24
references.pmid: 16092920
references.citation: Glycobiology. 2004 Aug;14(8):693-700
references.pmid: 15115749
references.citation: J Biol Chem. 2001 Feb 9;276(6):3863-71
references.pmid: 11073941
references.citation: Eur J Biochem. 1997 Feb 1;243(3):630-5
references.pmid: 9057825
references.citation: Biochemistry. 2008 Jan 15;47(2):710-20
references.pmid: 18092821
references.citation: Biochemistry. 2001 Jul 3;40(26):7789-98
references.pmid: 11425305
references.citation: Curr Opin Microbiol. 2004 Feb;7(1):71-7
references.pmid: 15036144
references.citation: J Biol Chem. 1990 Apr 5;265(10):5755-60
references.pmid: 2108147
references.citation: J Biol Chem. 1995 Aug 11;270(32):19052-8
references.pmid: 7642568
references.citation: Curr Opin Immunol. 2005 Feb;17(1):18-24
references.pmid: 15653305