Cell wall glycopolymers of Firmicutes and their role as nonprotein adhesins

FEBS Letters

Volumn 590, Issue 21, 2016, Pages 3758-3771

  Schade, Jessica ^a   Weidenmaier, Christopher ^a,b  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b German Center for Research in Infectious Disease (DZIF)   (Germany)

Author keywords

cell wall; Firmicutes; glycopolymers; gram positive; nonprotein adhesin; scavenger receptors; Staphylococcus aureus; wall teichoic acid

Indexed keywords

BACTERIAL PROTEIN; CELL WALL GLYCOPOLYMER; CLASS A SCAVENGER RECEPTOR; CLASS B SCAVENGER RECEPTOR; CLASS F SCAVENGER RECEPTOR; MICROBIAL PRODUCTS NOT CLASSIFIED ELSEWHERE; SREC I PROTEIN; UNCLASSIFIED DRUG; ADHESIN; BACTERIAL POLYSACCHARIDE; SCARF1 PROTEIN, HUMAN; SCAVENGER RECEPTOR F;

BACTERIAL CELL WALL; BACTERIAL COLONIZATION; BIOSYNTHESIS; CHEMICAL STRUCTURE; CONTROLLED STUDY; COVALENT BOND; FIRMICUTES; HOMEOSTASIS; HORIZONTAL GENE TRANSFER; HOST PATHOGEN INTERACTION; MICROBIAL ACTIVITY; MICROFLORA; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS AUREUS; CELL WALL; CHEMISTRY; GRAM POSITIVE INFECTION; HUMAN; METABOLISM; MICROBIOLOGY; NOSE CAVITY;

ADHESINS, BACTERIAL; CELL WALL; FIRMICUTES; GRAM-POSITIVE BACTERIAL INFECTIONS; HOST-PATHOGEN INTERACTIONS; HUMANS; NASAL CAVITY; POLYSACCHARIDES, BACTERIAL; SCAVENGER RECEPTORS, CLASS F;

EID: 84994608334     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1002/1873-3468.12288     Document Type: Review

References (103)

1. Fischer W (1997) Pneumococcal lipoteichoic and teichoic acid. Microb Drug Resist 3, 309–325.
2. Baddiley J (1972) Teichoic acids in cell walls and membranes of bacteria. Essays Biochem 8, 35–77.
3. Ward JB (1981) Teichoic and teichuronic acids: biosynthesis, assembly, and location. Microbiol Rev 45, 211–243.
4. Brown S, Santa Maria Jr JP and Walker S (2013) Wall teichoic acids of gram-positive bacteria. Annu Rev Microbiol 67, 313–336.
5. Schneewind O and Missiakas D (2014) Lipoteichoic acids, phosphate-containing polymers in the envelope of gram-positive bacteria. J Bacteriol 196, 1133–1142.
6. Weidenmaier C and Peschel A (2008) Teichoic acids and related cell-wall glycopolymers in Gram-positive physiology and host interactions. Nat Rev Microbiol 6, 276–287.
7. Neuhaus FC and Baddiley J (2003) A continuum of anionic charge: structures and functions of D-alanyl-teichoic acids in gram-positive bacteria. Microbiol Mol Biol Rev 67, 686–723.
8. Weidenmaier C and Lee JC (2016) Structure and function of surface polysaccharides of Staphylococcus aureus. Curr Top Microbiol Immunol, doi: 10.1007/82_2015_5018.
9. Mistou MY, Sutcliffe IC and van Sorge NM (2016) Bacterial glycobiology: rhamnose-containing cell wall polysaccharides in Gram-positive bacteria. FEMS Microbiol Rev 40, 464–479.
10. Fritz G and Mascher T (2014) A balancing act times two: sensing and regulating cell envelope homeostasis in Bacillus subtilis. Mol Microbiol 94, 1201–1207.
11. Araki Y and Ito E (1989) Linkage units in cell walls of gram-positive bacteria. Crit Rev Microbiol 17, 121–135.
12. Armstrong JJ, Baddiley J, Buchanan JG, Davision AL, Kelemen MV and Neuhaus FC (1959) Composition of teichoic acids from a number of bacterial walls. Nature 184, 247–248.
13. Weidenmaier C, Kokai-Kun JF, Kristian SA, Chanturiya T, Kalbacher H, Gross M, Nicholson G, Neumeister B, Mond JJ and Peschel A (2004) Role of teichoic acids in Staphylococcus aureus nasal colonization, a major risk factor in nosocomial infections. Nat Med 10, 243–245.
14. Peschel A, Otto M, Jack RW, Kalbacher H, Jung G and Gotz F (1999) Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins, and other antimicrobial peptides. J Biol Chem 274, 8405–8410.
15. Peschel A, Vuong C, Otto M and Gotz F (2000) The D-alanine residues of Staphylococcus aureus teichoic acids alter the susceptibility to vancomycin and the activity of autolytic enzymes. Antimicrob Agents Chemother 44, 2845–2847.
16. Doran KS, Engelson EJ, Khosravi A, Maisey HC, Fedtke I, Equils O, Michelsen KS, Arditi M, Peschel A and Nizet V (2005) Blood–brain barrier invasion by group B Streptococcus depends upon proper cell-surface anchoring of lipoteichoic acid. J Clin Invest 115, 2499–2507.
17. Xia G, Maier L, Sanchez-Carballo P, Li M, Otto M, Holst O and Peschel A (2010) Glycosylation of wall teichoic acid in Staphylococcus aureus by TarM. J Biol Chem 285, 13405–13415.
18. Winstel V, Liang C, Sanchez-Carballo P, Steglich M, Munar M, Broker BM, Penades JR, Nubel U, Holst O, Dandekar T et al. (2013) Wall teichoic acid structure governs horizontal gene transfer between major bacterial pathogens. Nat Commun 4, 2345.
19. Winstel V, Kuhner P, Salomon F, Larsen J, Skov R, Hoffmann W, Peschel A and Weidenmaier C (2015) Wall teichoic acid glycosylation governs Staphylococcus aureus nasal colonization. MBio 6, e00632–15.
20. Brown S, Xia G, Luhachack LG, Campbell J, Meredith TC, Chen C, Winstel V, Gekeler C, Irazoqui JE, Peschel A et al. (2012) Methicillin resistance in Staphylococcus aureus requires glycosylated wall teichoic acids. Proc Natl Acad Sci USA 109, 18909–18914.
21. Percy MG and Grundling A (2014) Lipoteichoic acid synthesis and function in gram-positive bacteria. Annu Rev Microbiol 68, 81–100.
22. Geiss-Liebisch S, Rooijakkers SH, Beczala A, Sanchez-Carballo P, Kruszynska K, Repp C, Sakinc T, Vinogradov E, Holst O, Huebner J et al. (2012) Secondary cell wall polymers of Enterococcus faecalis are critical for resistance to complement activation via mannose-binding lectin. J Biol Chem 287, 37769–37777.
23. Cole JN and Nizet V (2016) Bacterial evasion of host antimicrobial peptide defenses. Microbiol Spectr, doi: 10.1128/microbiolspec.VMBF-0006-2015.
24. Wartha F, Beiter K, Albiger B, Fernebro J, Zychlinsky A, Normark S and Henriques-Normark B (2007) Capsule and D-alanylated lipoteichoic acids protect Streptococcus pneumoniae against neutrophil extracellular traps. Cell Microbiol 9, 1162–1171.
25. Baur S, Rautenberg M, Faulstich M, Grau T, Severin Y, Unger C, Hoffmann WH, Rudel T, Autenrieth IB and Weidenmaier C (2014) A nasal epithelial receptor for Staphylococcus aureus WTA governs adhesion to epithelial cells and modulates nasal colonization. PLoS Pathog 10, e1004089.
26. Weidenmaier C, Kokai-Kun JF, Kulauzovic E, Kohler T, Thumm G, Stoll H, Gotz F and Peschel A (2008) Differential roles of sortase-anchored surface proteins and wall teichoic acid in Staphylococcus aureus nasal colonization. Int J Med Microbiol 298, 505–513.
27. Weidenmaier C, Peschel A and Xiong YQ (2005) Lack of wall teichoic acids in Staphylococcus aureus leads to reduced interactions with endothelial cells and to attenuated virulence in a rabbit model of endocarditis. J Infect Dis 191, 1771–1777.
28. Reichmann NT, Picarra Cassona C, Monteiro JM, Bottomley AL, Corrigan RM, Foster SJ, Pinho MG and Grundling A (2014) Differential localization of LTA synthesis proteins and their interaction with the cell division machinery in Staphylococcus aureus. Mol Microbiol 92, 273–286.
29. Reichmann NT and Grundling A (2011) Location, synthesis and function of glycolipids and polyglycerolphosphate lipoteichoic acid in Gram-positive bacteria of the phylum Firmicutes. FEMS Microbiol Lett 319, 97–105.
30. Kojima N, Araki Y and Ito E (1985) Structure of the linkage units between ribitol teichoic acids and peptidoglycan. J Bacteriol 161, 299–306.
31. Armstrong JJ, Baddiley J and Buchanan JG (1960) Structure of the ribitol teichoic acid from the walls of Bacillus subtilis. Biochem J 76, 610–621.
32. Winstel V, Sanchez-Carballo P, Holst O, Xia G and Peschel A (2014) Biosynthesis of the unique wall teichoic acid of Staphylococcus aureus lineage ST395. MBio, 5, e00869.
33. Denapaite D, Bruckner R, Hakenbeck R and Vollmer W (2012) Biosynthesis of teichoic acids in Streptococcus pneumoniae and closely related species: lessons from genomes. Microb Drug Resist 18, 344–358.
34. Fischer W (2000) Phosphocholine of pneumococcal teichoic acids: role in bacterial physiology and pneumococcal infection. Res Microbiol 151, 421–427.
35. Fischer W, Behr T, Hartmann R, Peter-Katalinic J and Egge H (1993) Teichoic acid and lipoteichoic acid of Streptococcus pneumoniae possess identical chain structures. A reinvestigation of teichoid acid (C polysaccharide). Eur J Biochem 215, 851–857.
36. Hakenbeck R, Madhour A, Denapaite D and Bruckner R (2009) Versatility of choline metabolism and choline-binding proteins in Streptococcus pneumoniae and commensal streptococci. FEMS Microbiol Rev 33, 572–586.
37. Horne DS and Tomasz A (1993) Possible role of a choline-containing teichoic acid in the maintenance of normal cell shape and physiology in Streptococcus oralis. J Bacteriol 175, 1717–1722.
38. Theilacker C, Holst O, Lindner B, Huebner J and Kaczynski Z (2012) The structure of the wall teichoic acid isolated from Enterococcus faecalis strain 12030. Carbohydr Res 354, 106–109.
39. Bychowska A, Theilacker C, Czerwicka M, Marszewska K, Huebner J, Holst O, Stepnowski P and Kaczynski Z (2011) Chemical structure of wall teichoic acid isolated from Enterococcus faecium strain U0317. Carbohydr Res 346, 2816–2819.
40. Brown S, Zhang YH and Walker S (2008) A revised pathway proposed for Staphylococcus aureus wall teichoic acid biosynthesis based on in vitro reconstitution of the intracellular steps. Chem Biol 15, 12–21.
41. Brown S, Meredith T, Swoboda J and Walker S (2010) Staphylococcus aureus and Bacillus subtilis W23 make polyribitol wall teichoic acids using different enzymatic pathways. Chem Biol 17, 1101–1110.
42. D'Elia MA, Henderson JA, Beveridge TJ, Heinrichs DE and Brown ED (2009) The N-acetylmannosamine transferase catalyzes the first committed step of teichoic acid assembly in Bacillus subtilis and Staphylococcus aureus. J Bacteriol 191, 4030–4034.
43. Chaudhuri RR, Allen AG, Owen PJ, Shalom G, Stone K, Harrison M, Burgis TA, Lockyer M, Garcia-Lara J, Foster SJ et al. (2009) Comprehensive identification of essential Staphylococcus aureus genes using Transposon-Mediated Differential Hybridisation (TMDH). BMC Genom 10, 291.
44. D'Elia MA, Millar KE, Beveridge TJ and Brown ED (2006) Wall teichoic acid polymers are dispensable for cell viability in Bacillus subtilis. J Bacteriol 188, 8313–8316.
45. Pasquina LW, Santa Maria JP and Walker S (2013) Teichoic acid biosynthesis as an antibiotic target. Curr Opin Microbiol 16, 531–537.
46. Rajagopal M and Walker S (2016) Envelope structures of gram-positive bacteria. Curr Top Microbiol Immunol, doi: 10.1007/82_2015_5021.
47. Pereira MP, Schertzer JW, D'Elia MA, Koteva KP, Hughes DW, Wright GD and Brown ED (2008) The wall teichoic acid polymerase TagF efficiently synthesizes poly(glycerol phosphate) on the TagB product lipid III. ChemBioChem 9, 1385–1390.
48. Ginsberg C, Zhang YH, Yuan Y and Walker S (2006) In vitro reconstitution of two essential steps in wall teichoic acid biosynthesis. ACS Chem Biol 1, 25–28.
49. Pereira MP, D'Elia MA, Troczynska J and Brown ED (2008) Duplication of teichoic acid biosynthetic genes in Staphylococcus aureus leads to functionally redundant poly(ribitol phosphate) polymerases. J Bacteriol 190, 5642–5649.
50. Meredith TC, Swoboda JG and Walker S (2008) Late-stage polyribitol phosphate wall teichoic acid biosynthesis in Staphylococcus aureus. J Bacteriol 190, 3046–3056.
51. Kawai Y, Marles-Wright J, Cleverley RM, Emmins R, Ishikawa S, Kuwano M, Heinz N, Bui NK, Hoyland CN, Ogasawara N et al. (2011) A widespread family of bacterial cell wall assembly proteins. EMBO J 30, 4931–4941.
52. Chan YG, Frankel MB, Dengler V, Schneewind O and Missiakas D (2013) Staphylococcus aureus mutants lacking the LytR-CpsA-Psr family of enzymes release cell wall teichoic acids into the extracellular medium. J Bacteriol 195, 4650–4659.
53. Reichmann NT, Cassona CP and Grundling A (2013) Revised mechanism of D-alanine incorporation into cell wall polymers in Gram-positive bacteria. Microbiology 159, 1868–1877.
54. Lu D, Wormann ME, Zhang X, Schneewind O, Grundling A and Freemont PS (2009) Structure-based mechanism of lipoteichoic acid synthesis by Staphylococcus aureus LtaS. Proc Natl Acad Sci USA 106, 1584–1589.
55. Hanson BR and Neely MN (2012) Coordinate regulation of Gram-positive cell surface components. Curr Opin Microbiol 15, 204–210.
56. Atilano ML, Pereira PM, Yates J, Reed P, Veiga H, Pinho MG and Filipe SR (2010) Teichoic acids are temporal and spatial regulators of peptidoglycan cross-linking in Staphylococcus aureus. Proc Natl Acad Sci USA 107, 18991–18996.
57. Qamar A and Golemi-Kotra D (2012) Dual roles of FmtA in Staphylococcus aureus cell wall biosynthesis and autolysis. Antimicrob Agents Chemother 56, 3797–3805.
58. Farha MA, Leung A, Sewell EW, D'Elia MA, Allison SE, Ejim L, Pereira PM, Pinho MG, Wright GD and Brown ED (2013) Inhibition of WTA synthesis blocks the cooperative action of PBPs and sensitizes MRSA to beta-lactams. ACS Chem Biol 8, 226–233.
59. Bierbaum G and Sahl HG (1985) Induction of autolysis of staphylococci by the basic peptide antibiotics Pep 5 and nisin and their influence on the activity of autolytic enzymes. Arch Microbiol 141, 249–254.
60. Frankel MB and Schneewind O (2012) Determinants of murein hydrolase targeting to cross-wall of Staphylococcus aureus peptidoglycan. J Biol Chem 287, 10460–10471.
61. Winstel V, Xia G and Peschel A (2014) Pathways and roles of wall teichoic acid glycosylation in Staphylococcus aureus. Int J Med Microbiol 304, 215–221.
62. Xia G, Corrigan RM, Winstel V, Goerke C, Grundling A and Peschel A (2011) Wall teichoic Acid-dependent adsorption of staphylococcal siphovirus and myovirus. J Bacteriol 193, 4006–4009.
63. Greenberg JW, Fischer W and Joiner KA (1996) Influence of lipoteichoic acid structure on recognition by the macrophage scavenger receptor. Infect Immun 64, 3318–3325.
64. Peiser L, Mukhopadhyay S and Gordon S (2002) Scavenger receptors in innate immunity. Curr Opin Immunol 14, 123–128.
65. Canton J, Neculai D and Grinstein S (2013) Scavenger receptors in homeostasis and immunity. Nat Rev Immunol 13, 621–634.
66. Pluddemann A, Mukhopadhyay S and Gordon S (2006) The interaction of macrophage receptors with bacterial ligands. Expert Rev Mol Med 8, 1–25.
67. Hashimoto M, Tawaratsumida K, Kariya H, Kiyohara A, Suda Y, Krikae F, Kirikae T and Gotz F (2006) Not lipoteichoic acid but lipoproteins appear to be the dominant immunobiologically active compounds in Staphylococcus aureus. J Immunol 177, 3162–3169.
68. Gisch N, Kohler T, Ulmer AJ, Muthing J, Pribyl T, Fischer K, Lindner B, Hammerschmidt S and Zahringer U (2013) Structural reevaluation of Streptococcus pneumoniae Lipoteichoic acid and new insights into its immunostimulatory potency. J Biol Chem 288, 15654–15667.
69. Goldstein JL, Ho YK, Brown MS, Innerarity TL and Mahley RW (1980) Cholesteryl ester accumulation in macrophages resulting from receptor-mediated uptake and degradation of hypercholesterolemic canine beta-very low density lipoproteins. J Biol Chem 255, 1839–1848.
70. Prabhudas M, Bowdish D, Drickamer K, Febbraio M, Herz J, Kobzik L, Krieger M, Loike J, Means TK, Moestrup SK et al. (2014) Standardizing scavenger receptor nomenclature. J Immunol 192, 1997–2006.
71. Zani IA, Stephen SL, Mughal NA, Russell D, Homer-Vanniasinkam S, Wheatcroft SB and Ponnambalam S (2015) Scavenger receptor structure and function in health and disease. Cells 4, 178–201.
72. Gowen BB, Borg TK, Ghaffar A and Mayer EP (2001) The collagenous domain of class A scavenger receptors is involved in macrophage adhesion to collagens. J Leukoc Biol 69, 575–582.
73. Dunne DW, Resnick D, Greenberg J, Krieger M and Joiner KA (1994) The type I macrophage scavenger receptor binds to gram-positive bacteria and recognizes lipoteichoic acid. Proc Natl Acad Sci USA 91, 1863–1867.
74. Mietus-Snyder M, Friera A, Glass CK and Pitas RE (1997) Regulation of scavenger receptor expression in smooth muscle cells by protein kinase C: a role for oxidative stress. Arterioscler Thromb Vasc Biol 17, 969–978.
75. Pitas RE (1990) Expression of the acetyl low density lipoprotein receptor by rabbit fibroblasts and smooth muscle cells. Up-regulation by phorbol esters. J Biol Chem 265, 12722–12727.
76. Thomas CA, Li Y, Kodama T, Suzuki H, Silverstein SC and El Khoury J (2000) Protection from lethal gram-positive infection by macrophage scavenger receptor-dependent phagocytosis. J Exp Med 191, 147–156.
77. Elomaa O, Kangas M, Sahlberg C, Tuukkanen J, Sormunen R, Liakka A, Thesleff I, Kraal G and Tryggvason K (1995) Cloning of a novel bacteria-binding receptor structurally related to scavenger receptors and expressed in a subset of macrophages. Cell 80, 603–609.
78. van der Laan LJ, Dopp EA, Haworth R, Pikkarainen T, Kangas M, Elomaa O, Dijkstra CD, Gordon S, Tryggvason K and Kraal G (1999) Regulation and functional involvement of macrophage scavenger receptor MARCO in clearance of bacteria in vivo. J Immunol 162, 939–947.
79. Ojala JR, Pikkarainen T, Tuuttila A, Sandalova T and Tryggvason K (2007) Crystal structure of the cysteine-rich domain of scavenger receptor MARCO reveals the presence of a basic and an acidic cluster that both contribute to ligand recognition. J Biol Chem 282, 16654–16666.
80. Jiang Y, Oliver P, Davies KE and Platt N (2006) Identification and characterization of murine SCARA5, a novel class A scavenger receptor that is expressed by populations of epithelial cells. J Biol Chem 281, 11834–11845.
81. Silverstein RL, Li W, Park YM and Rahaman SO (2010) Mechanisms of cell signaling by the scavenger receptor CD36: implications in atherosclerosis and thrombosis. Trans Am Clin Climatol Assoc 121, 206–220.
82. Hoebe K, Georgel P, Rutschmann S, Du X, Mudd S, Crozat K, Sovath S, Shamel L, Hartung T, Zahringer U et al. (2005) CD36 is a sensor of diacylglycerides. Nature 433, 523–527.
83. Adachi H and Tsujimoto M (2002) Characterization of the human gene encoding the scavenger receptor expressed by endothelial cell and its regulation by a novel transcription factor, endothelial zinc finger protein-2. J Biol Chem 277, 24014–24021.
84. Kumari M, Sunoj RB and Balaji PV (2012) Exploration of CH.pi mediated stacking interactions in saccharide: aromatic residue complexes through conformational sampling. Carbohydr Res 361, 133–140.
85. Wimmerova M, Kozmon S, Necasova I, Mishra SK, Komarek J and Koca J (2012) Stacking interactions between carbohydrate and protein quantified by combination of theoretical and experimental methods. PLoS One 7, e46032.
86. Abachin E, Poyart C, Pellegrini E, Milohanic E, Fiedler F, Berche P and Trieu-Cuot P (2002) Formation of D-alanyl-lipoteichoic acid is required for adhesion and virulence of Listeria monocytogenes. Mol Microbiol 43, 1–14.
87. Kristian SA, Datta V, Weidenmaier C, Kansal R, Fedtke I, Peschel A, Gallo RL and Nizet V (2005) D-alanylation of teichoic acids promotes group a streptococcus antimicrobial peptide resistance, neutrophil survival, and epithelial cell invasion. J Bacteriol 187, 6719–6725.
88. Cundell DR (2002) Development of a microbiology course for diverse majors; longitudinal survey of the use of various active, problem-based learning assignments. Microbiol Educ 3, 12–17.
89. Weidenmaier C, Goerke C and Wolz C (2012) Staphylococcus aureus determinants for nasal colonization. Trends Microbiol 20, 243–250.
90. Misawa Y, Kelley KA, Wang X, Wang L, Park WB, Birtel J, Saslowsky D and Lee JC (2015) Staphylococcus aureus colonization of the mouse gastrointestinal tract is modulated by wall teichoic acid, capsule, and surface proteins. PLoS Pathog 11, e1005061.
91. Shimaoka T, Kume N, Minami M, Hayashida K, Sawamura T, Kita T and Yonehara S (2001) LOX-1 supports adhesion of Gram-positive and Gram-negative bacteria. J Immunol 166, 5108–5114.
92. Shimaoka T, Nakayama T, Kume N, Takahashi S, Yamaguchi J, Minami M, Hayashida K, Kita T, Ohsumi J, Yoshie O et al. (2003) Cutting edge: SR-PSOX/CXC chemokine ligand 16 mediates bacterial phagocytosis by APCs through its chemokine domain. J Immunol 171, 1647–1651.
93. Gutwein P, Abdel-Bakky MS, Schramme A, Doberstein K, Kampfer-Kolb N, Amann K, Hauser IA, Obermuller N, Bartel C, Abdel-Aziz AA et al. (2009) CXCL16 is expressed in podocytes and acts as a scavenger receptor for oxidized low-density lipoprotein. Am J Pathol 174, 2061–2072.
94. Adachi H and Tsujimoto M (2002) FEEL-1, a novel scavenger receptor with in vitro bacteria-binding and angiogenesis-modulating activities. J Biol Chem 277, 34264–34270.
95. Amiel E, Nicholson-Dykstra S, Walters JJ, Higgs H and Berwin B (2007) Scavenger receptor-A functions in phagocytosis of E. coli by bone marrow dendritic cells. Exp Cell Res 313, 1438–1448.
96. Ricci R, Sumara G, Sumara I, Rozenberg I, Kurrer M, Akhmedov A, Hersberger M, Eriksson U, Eberli FR, Becher B et al. (2004) Requirement of JNK2 for scavenger receptor A-mediated foam cell formation in atherogenesis. Science 306, 1558–1561.
97. Ohnishi K, Komohara Y, Fujiwara Y, Takemura K, Lei X, Nakagawa T, Sakashita N and Takeya M (2011) Suppression of TLR4-mediated inflammatory response by macrophage class A scavenger receptor (CD204). Biochem Biophys Res Commun 411, 516–522.
98. Stuart LM, Deng J, Silver JM, Takahashi K, Tseng AA, Hennessy EJ, Ezekowitz RA and Moore KJ (2005) Response to Staphylococcus aureus requires CD36-mediated phagocytosis triggered by the COOH-terminal cytoplasmic domain. J Cell Biol 170, 477–485.
99. Biocca S, Falconi M, Filesi I, Baldini F, Vecchione L, Mango R, Romeo F, Federici G, Desideri A and Novelli G (2009) Functional analysis and molecular dynamics simulation of LOX-1 K167N polymorphism reveal alteration of receptor activity. PLoS One 4, e4648.
100. Khaidakov M, Wang X and Mehta JL (2011) Potential involvement of LOX-1 in functional consequences of endothelial senescence. PLoS One 6, e20964.
101. Sano M, Korekane H, Ohtsubo K, Yamaguchi Y, Kato M, Shibukawa Y, Tajiri M, Adachi H, Wada Y, Asahi M et al. (2012) N-glycans of SREC-I (scavenger receptor expressed by endothelial cells): essential role for ligand binding, trafficking and stability. Glycobiology 22, 714–724.
102. Shetty S, Weston CJ, Oo YH, Westerlund N, Stamataki Z, Youster J, Hubscher SG, Salmi M, Jalkanen S, Lalor PF et al. (2011) Common lymphatic endothelial and vascular endothelial receptor-1 mediates the transmigration of regulatory T cells across human hepatic sinusoidal endothelium. J Immunol 186, 4147–4155.
103. Nassir F, Wilson B, Han X, Gross RW and Abumrad NA (2007) CD36 is important for fatty acid and cholesterol uptake by the proximal but not distal intestine. J Biol Chem 282, 19493–19501.