Roles of peptidoglycan recognition protein (PGRP) in immunity and implications for novel Anti-infective measures

Critical Reviews in Eukaryotic Gene Expression

Volumn 22, Issue 3, 2012, Pages 259-268

  Zhang, Zhen ^a   Long, Quanxin ^a   Xie, Jianping ^a  

^a SOUTHWEST UNIVERSITY   (China)

Author keywords

Distribution; Evolution; Immunity function; PGRP; Structure; Transcript regulation

Indexed keywords

AMIDASE; CARBOXYPEPTIDASE; CASPASE RECRUITMENT DOMAIN PROTEIN 15; GAMMA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 12; INTERLEUKIN 12P35; INTERLEUKIN 6; INTERLEUKIN 8; LIPOPOLYSACCHARIDE; LIPOTEICHOIC ACID; MANNOSE; PATTERN RECOGNITION RECEPTOR; PEPTIDOGLYCAN RECOGNITION PROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROPHENOL OXIDASE; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANTIINFLAMMATORY ACTIVITY; ARTICLE; BACTERICIDAL ACTIVITY; BACTERIOSTASIS; BOMBYX MORI; CRYSTAL STRUCTURE; CYTOKINE PRODUCTION; DIMERIZATION; DROSOPHILA; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE STRUCTURE; HUMAN; HYDROLYSIS; HYDROPHILICITY; INNATE IMMUNITY; LIGAND BINDING; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

AMIDOHYDROLASES; ANIMALS; BACTERIA; CARRIER PROTEINS; CATECHOL OXIDASE; ENZYME PRECURSORS; GENE EXPRESSION REGULATION; HUMANS; IMMUNITY, INNATE; INSECTS; LIPOPOLYSACCHARIDES; MANNOSE; PEPTIDOGLYCAN; RECEPTORS, PATTERN RECOGNITION; SIGNAL TRANSDUCTION; TEICHOIC ACIDS;

HEXAPODA; MAMMALIA;

EID: 84868515323     PISSN: 10454403     EISSN: None     Source Type: Journal    
DOI: 10.1615/CritRevEukarGeneExpr.v22.i3.90     Document Type: Article

References (76)

1. Yoshida H, Kinoshita K, Ashida M. Purification of a peptidoglycan recognition protein from hemolymph of the silkworm, Bombyx mori. J Biol Chem. 1996 Jun 7;271(23):13854-60.
2. Werner T, Liu G, Kang D, Ekengren S, Steiner H, Hultmark D. A family of peptidoglycan recognition proteins in the fruit fly Drosophila melanogaster. Proc Natl Acad Sci USA. 2000 Dec 5;97(25):13772-7.
3. Christophides GK, Zdobnov E, Barillas-Mury C, Birney E, Blandin S, Blass C, Brey PT, Collins FH, Danielli A, Dimopoulos G, Hetru C, Hoa NT, Hoffmann JA, Kanzok SM, Letunic I, Levashina EA, Loukeris TG, Lycett G, Meister S, Michel K, Moita LF, Muller HM, Osta MA, Paskewitz SM, Reichhart JM, Rzhetsky A, Troxler L, Vernick KD, Vlachou D, Volz J, von Mering C, Xu J, Zheng L, Bork P, Kafatos FC. Immunity-related genes and gene families in Anopheles gambiae. Science. 2002 Oct 4;298(5591):159-65.
4. Liu C, Xu Z, Gupta D, Dziarski R. Peptidoglycan recognition proteins: a novel family of four human innate immunity pattern recognition molecules. J Biol Chem. 2001 Sep 14;276(37):34686-94.
5. Hoffmann JA. The immune response of Drosophila. Nature. 2003;426(6962):33-8.
6. Michel T, Reichhart JM, Hoffmann JA, Royet J. Drosophila Toll is activated by gram-positive bacteria through a circulating peptidoglycan recognition protein. Nature. 2001;414(6865):756-9.
7. Lemaitre B, Kromer-Metzger E, Michaut L, Nicolas E, Meister M, Georgel P, Reichhart JM, Hoffmann JA. A recessive mutation, immune deficiency (Imd), defines two distinct control pathways in the Drosophila host defense. Proc Natl Acad Sci U S A. 1995 Oct 10;92(21):9465-9.
8. Royet J, Dziarski R. Peptidoglycan recognition proteins: pleiotropic sensors and effectors of antimicrobial defences. Nature Reviews Microbiology. 2007;5(4):264-77.
9. Royet J. Infectious non-self recognition in invertebrates: lessons from Drosophila and other insect models. Mol Immunol. 2004 Nov;41(11):1063-75.
10. Schmidt RL, Trejo TR, Plummer TB, Platt JL, Tang AH. Infection-induced proteolysis of PGRP-LC controls the IMD activation and melanization cascades in Drosophila. FASEB J. 2008 Mar;22(3):918-29.
11. Reiser JB, Teyton L, Wilson IA. Crystal structure of the Drosophila peptidoglycan recognition protein (PGRP)-SA at 1.56 A resolution. J Mol Biol. 2004 Jul 16;340(4):909-17.
12. Pili-Floury S, Leulier F, Takahashi K, Saigo K, Samain E, Ueda R, Lemaitre B. In vivo RNA interference analysis reveals an unexpected role for GNBP 1 in the defense against Gram-positive bacterial infection in Drosophila adults. J Biol Chem. 2004 Mar 26;279(13):12848-53.
13. Filipe SR, Tomasz A, Ligoxygakis P. Requirements of peptidoglycan structure that allow detection by the Dro-sophila Toll pathway. EMBO Rep. 2005 Apr;6(4):327-33.
14. Gobert V, Gottar M, Matskevich AA, Rutschmann S, Royet J, Belvin M, Hoffmann JA, Ferrandon D. Dual activation of the Drosophila toll pathway by two pattern recognition receptors. Science. 2003 Dec 19;302(5653):2126-30.
15. Mishima Y, Quintin J, Aimanianda V, Kellenberger C, Coste F, Clavaud C, Hetru C, Hoffmann JA, Latge JP, Ferrandon D, Roussel A. The N-terminal domain of Drosophila Gram-negative binding protein 3 (GNBP3) defines a novel family of fungal pattern recognition receptors. J Biol Chem. 2009 Oct 16;284(42):28687-97.
16. Bischoff V, Vignal C, Boneca IG, Michel T, Hoffmann JA, Royet J. Function of the drosophila pattern-recognition receptor PGRP-SD in the detection of Grampositive bacteria. Nat Immunol. 2004 Nov;5(11):1175-80.
17. Michel T, Reichhart JM, Hoffmann JA, Royet J. Drosophila Toll is activated by Gram-positive bacteria through a circulating peptidoglycan recognition protein. Nature. 2001 Dec 13;414(6865):756-9.
18. Jang IH, Chosa N, Kim SH, Nam HJ, Lemaitre B, Ochiai M, Kambris Z, Brun S, Hashimoto C, Ashida M, Brey PT, Lee WJ. A Spatzle-processing enzyme required for toll signaling activation in Drosophila innate immunity. Dev Cell. 2006 Jan;10(1):45-55.
19. Lemaitre B, KromerMetzger E, Michaut L, Nicolas E, Meister M, Georgel P, Reichhart JM, Hoffmann JA. A recessive mutation, immune deficiency (Imd), defines two distinct control pathways in the Drosophila host defense. Proc Natl Acad Sci U S A. 1995;92(21):9465-9.
20. Kaneko T, Goldman WE, Mellroth P, Steiner H, Fukase K, Kusumoto S, Harley W, Fox A, Golenbock D, Silver-man N. Monomeric and polymeric gram-negative peptidoglycan but not purified LPS stimulate the Drosophila Imd pathway. Immunity. 2004 May;20(5):637-49.
21. Ramet M, Manfruelli P, Pearson A, Mathey-Prevot B, Ezekowitz RA. Functional genomic analysis of phagocytosis and identification of a Drosophila receptor for E. coli. Nature. 2002 Apr 11;416(6881):644-8.
22. Choe KM, Lee H, Anderson KV. Drosophila peptidoglycan recognition protein LC (PGRP-LC) acts as a signal-transducing innate immune receptor. Proceedings of the National Academy of Sciences of the United States of America. 2005;102(4):1122-6.
23. Werner T, Borge-Renberg K, Mellroth P, Steiner H, Hultmark D. Functional diversity of the Drosophila PGRP-LC gene cluster in the response to lipopolysac-charide and peptidoglycan. J Biol Chem. 2003;278(29): 26319-22.
24. Lim JH, Kim MS, Kim HE, Yano T, Oshima Y, Aggarwal K, Goldman WE, Silverman N, Kurata S, Oh BH. Structural basis for preferential recognition of diaminopimelic acid-type peptidoglycan by a subset of peptidoglycan recognition proteins. J Biol Chem. 2006 Mar 24;281(12):8286-95.
25. Kaneko T, Yano T, Aggarwal K, Lim JH, Ueda K, Os-hima Y, Peach C, Erturk-Hasdemir D, Goldman WE, Oh BH, Kurata S, Silverman N. PGRP-LC and PGRP-LE have essential yet distinct functions in the drosophila immune response to monomeric DAP-type peptidoglycan. Nat Tmmunol. 2006 Jul(7):715-23.
26. Takehana A, Yano T, Mita S, Kotani A, Oshima Y, Kurata S. Peptidoglycan recognition protein (PGRP)-LE and PGRP-LC act synergistically in Drosophila immunity. EMBO J. 2004 Nov 24;23(23):4690-700.
27. Takehana A, Katsuyama T, Yano T, Oshima Y, Takada H, Aigaki T, Kurata S. Overexpression of a pattern-recognition receptor, peptidoglycan-recognition protein-LE, activates imd/relish-mediated antibacterial defense and the prophenoloxidase cascade in Drosophila larvae. Proc Natl Acad Sci U S A. 2002 Oct 15;99(21):13705-10.
28. Basbous N, Coste F, Leone P, Vincentelli R, Royet J, Kellenberger C, Roussel A. The Drosophila peptidoglycan-recognition protein LF interacts with peptidoglycan-recognition protein LC to downregulate the Imd pathway. EMBO Rep. 2011 Apr;12(4):327-33.
29. Persson C, Oldenvi S, Steiner H. Peptidoglycan recognition protein LF: a negative regulator of Drosophila immunity. Insect Biochem Mol Biol. 2007 Dec;37(12):1309-16.
30. Maillet F, Bischoff V, Vignal C, Hoffmann J, Royet J. The Drosophila peptidoglycan recognition protein PGRP-LF blocks PGRP-LC and IMD/JNK pathway activation. Cell Host Microbe. 2008 May 15;3(5):293-303.
31. Sumathipala N, Jiang H. Involvement of Manduca sexta peptidoglycan recognition protein-1 in the recognition of bacteria and activation of prophenoloxidase system. Insect Biochem Mol Biol. 2010 Jun;40(6):487-95.
32. Takehana A, Yano T, Mita S, Kotani A, Oshima Y, Kurata S. Peptidoglycan recognition protein (PGRP)-LE and PGRP-LC act synergistically in Drosophila immunity. EMBO J. 2004;23(23):4690-700.
33. Cerenius L, Liang Z, Duvic B, Keyser P, Hellman U, Palva ET, Iwanaga S, Soderhall K. Structure and biological activity of a 1,3-beta-D-glucan-binding protein in crustacean blood. J Biol Chem. 1994 Nov 25;269(47):29462-7.
34. Lee MH, Osaki T, Lee JY, Baek MJ, Zhang R, Park JW, Kawabata S, Soderhall K, Lee BL. Peptidoglycan recognition proteins involved in 1,3-beta-D-glucan-dependent prophenoloxidase activation system of insect. J Biol Chem. 2004 Jan 30;279(5):3218-27.
35. Bischoff V, Vignal C, Duvic B, Boneca IG, Hoffmann JA, Royet J. Downregulation of the Drosophila immune response by peptidoglycan-recognition proteins SC1 and SC2. PLoS Pathog. 2006 Feb;2(2):e14.
36. Zaidman-Rémy A, Hervé M, Poidevin M, Pili-Floury S, Kim M-S, Blanot D, Oh B-H, Ueda R, Mengin-Lecreulx D, Lemaitre B. The Drosophila amidase PGRP-LB modulates the immune response to bacterial infection. Immunity. 2006;24(4):463-73.
37. Mellroth P, Steiner H. PGRP-SB1: An N-acetylmuramoyl 1-alanine amidase with antibacterial activity. Biochem Biophys Res Commun. 2006;350(4):994-9.
38. Mellroth P, Karlsson J, Steiner H. A scavenger function for a Drosophila peptidoglycan recognition protein. J Biol Chem. 2003 Feb 28;278(9):7059-64.
39. Zaidman-Remy A, Poidevin M, Herve M, Welchman DP, Paredes JC, Fahlander C, Steiner H, Mengin-Lecreulx D, Lemaitre B. Drosophila immunity: analysis of PGRP-SB 1 expression, enzymatic activity and function. PLoS One. 2011;6(2):e17231.
40. Chang CI, Pili-Floury S, Herve M, Parquet C, Chelliah Y, Lemaitre B, Mengin-Lecreulx D, Deisenhofer J. A Drosophila pattern recognition receptor contains a peptidoglycan docking groove and unusual L,D-carboxypeptidase activity. PLoS Biol. 2004 Sep;2(9):e277.
41. Guan R, Malchiodi EL, Wang Q, Schuck P, Mariuzza RA. Crystal structure of the C-terminal peptidoglycan-binding domain of human peptidoglycan recognition protein Ia. J Biol Chem. 2004;279(30):31873-82.
42. Wang ZM. Human peptidoglycan recognition protein-L Is an N-acetylmuramoyl-L-alanine amidase. J Biol Chem. 2003;278(49):49044-52.
43. Gelius E, Persson C, Karlsson J, Steiner H. A mammalian peptidoglycan recognition protein with N-acetylmuramoyl-L-alanine amidase activity. Biochem Biophys Res Commun. 2003 Jul 11;306(4):988-94.
44. Saha S, Qi J, Wang S, Wang M, Li X, Kim YG, Nunez G, Gupta D, Dziarski R. PGLYRP-2 and Nod2 are both required for peptidoglycan-induced arthritis and local inflammation. Cell Host Microbe. 2009 Feb 19;5(2):137-50.
45. Dziarski R, Platt KA, Gelius E, Steiner H, Gupta D. Defect in neutrophil killing and increased susceptibility to infection with nonpathogenic gram-positive bacteria in peptidoglycan recognition protein-S (PGRP-S)-deficient mice. Blood. 2003 Jul 15;102(2):689-97.
46. Osanai A, Sashinami H, Asano K, Li SJ, Hu DL, Nakane A. Mouse peptidoglycan recognition protein PGLYRP-1 plays a role in the host innate immune response against Listeria monocytogenes Infection. Infection and Immunity. 2010;79(2):858-66.
47. Tydell CC, Yuan J, Tran P, Selsted ME. Bovine peptidoglycan recognition protein-S: antimicrobial activity, localization, secretion, and binding properties. J Immunol. 2006 Jan 15;176(2):1154-62.
48. Lu X, Wang M, Qi J, Wang H, Li X, Gupta D, Dziarski R. Peptidoglycan recognition proteins are a new class of human bactericidal proteins. J Biol Chem. 2006;281(9):5895-907.
49. Park SY, Gupta D, Hurwich R, Kim CH, Dziarski R. Peptidoglycan recognition protein Pglyrp2 protects mice from psoriasis-like skin inflammation by promoting regulatory T cells and limiting Th17 responses. J Immunol. 2011 Dec 1;187(11):5813-23.
50. Zenhom M, Hyder A, de Vrese M, Heller KJ, Roeder T, Schrezenmeir J. Peptidoglycan recognition protein 3 (Pg-lyRP3) has an anti-inflammatory role in intestinal epithelial cells. Immunobiology. 2012 Apr;217(4):412-9.
51. Sharma P, Dube D, Singh A, Mishra B, Singh N, Sinha M, Dey S, Kaur P, Mitra DK, Sharma S, Singh TP. Structural basis of recognition of pathogen-associated molecular patterns and inhibition of proinflammatory cytokines by camel peptidoglycan recognition protein. J Biol Chem. 2011 May 6;286(18):16208-17.
52. Zenhom M, Hyder A, Kraus-Stojanowic I, Auinger A, Roeder T, Schrezenmeir J. PPARgamma-dependent peptidoglycan recognition protein 3 (PG1yRP3) expression regulates proinflammatory cytokines by microbial and dietary fatty acids. Immunobiology. 2011 Jun;216(6):715-24.
53. Zenhom M, Hyder A, de Vrese M, Heller KJ, Roeder T, Schrezenmeir J. Prebiotic oligosaccharides reduce proinflammatory cytokines in intestinal Caco-2 cells via activation of PPARgamma and peptidoglycan recognition protein 3. JNutr. 2011 May;141(5):971-7.
54. Kim MS, Byun M, Oh BH. Crystal structure of peptidoglycan recognition protein LB from Drosophila melano-gaster. Nat Immunol. 2003 Aug;4(8):787-93.
55. Gottar M, Gobert V, Michel T, Belvin M, Duyk G, Hoffmann JA, Ferrandon D, Royet J. The Drosophila immune response against Gram-negative bacteria is mediated by a peptidoglycan recognition protein. Nature. 2002;416(6881):640-4.
56. Leulier F, Parquet C, Pili-Floury S, Ryu JH, CaroffM, Lee WJ, Mengin-Lecreulx D, Lemaitre B. The Drosophila immune system detects bacteria through specific peptidogly-can recognition. Nature Immunol. 2003;4(5):478-84.
57. Wang M, Liu LH, Wang S, Li X, Lu X, Gupta D, Dzi-arski R. Human peptidoglycan recognition proteins require zinc to kill both gram-positive and gram-negative bacteria and are synergistic with antibacterial peptides. J Immunol. 2007 Mar 1;178(5):3116-25.
58. Zhang Y, van der Fits L, Voerman JS, Melief MJ, Laman JD, Wang M, Wang H, Li X, Walls CD. Identification of serum N-acetylmuramoyl-L-alanine amidase as liver peptidoglycan recognition protein 2. Biochim Biophys Acta. 2005;1752(1):34-46.
59. Wang ZM, Li X, Cocklin RR, Wang M, Fukase K, Inamura S, Kusumoto S, Gupta D, Dziarski R. Human peptidoglycan recognition protein-L is an N-acetylmuramoyl-L-alanine amidase. J Biol Chem. 2003 Dec 5;278(49):49044-52.
60. Wang H, Gupta D, Li X, Dziarski R. Peptidoglycan recognition protein 2 (N-acetylmuramoyl-L-Ala amidase) is induced in keratinocytes by bacteria through the p38 kinase pathway. Infect Immun. 2005;73(11):7216-25.
61. Dziarski R, Gupta D. Mammalian PGRPs: novel antibacterial proteins. Cell Microbiol. 2006;8(7):1059-69.
62. Guan R, Wang Q, Sundberg EJ, Mariuzza RA. Crystal structure of human peptidoglycan recognition protein S (PGRP-S) at 1.70 A resolution. J Mol Biol. 2005 Apr 8;347(4):683-91.
63. Guan R, Brown PH, Swaminathan CP, Roychowdhury A, Boons GJ, Mariuzza RA. Crystal structure of human peptidoglycan recognition protein I alpha bound to a muramyl pentapeptide from Gram-positive bacteria. Protein Sci. 2006 May:15(15):1199-206.
64. Cho S, Wang Q, Swaminathan CP, Hesek D, Lee M, Boons GJ, Mobashery S, Mariuzza RA. Structural insights into the bactericidal mechanism of human peptidoglycan recognition proteins. Proc Natl Acad Sci U S A. 2007 May 22;104(21):8761-6.
65. Chang CI, Chelliah Y, Borek D, Mengin-Lecreulx D, Deisenhofer J. Structure of tracheal cytotoxin in complex with a heterodimeric pattern-recognition receptor. Science. 2006 Mar 24;311(5768):1761-4.
66. Sharma P, Dube D, Sinha M, Mishra B, Dey S, Mal G, Pathak KM, Kaur P, Sharma S, Singh TP. Multiligand specificity of pathogen-associated molecular pattern-binding site in peptidoglycan recognition protein. J Biol Chem. 2011 Sep 9;286(36):31723-30.
67. Leone P, Bischoff V, Kellenberger C, Hetru C, Royet J, Roussel A. Crystal structure of Drosophila PGRP-SD suggests binding to DAP-type but not lysine-type peptidoglycan. Mol Immunol. 2008 May;45(9):2521-30.
68. Guan R, Roychowdhury A, Ember B, Kumar S, Boons GJ, Mariuzza RA. Structural basis for peptidoglycan binding by peptidoglycan recognition proteins. Proc Natl Acad Sci U S A. 2004 Dec 7;101(49):17168-73.
69. Mellroth P, Karlsson J, Hakansson J, Schultz N, Goldman WE, Steiner H. Ligand-induced dimerization of Drosophila peptidoglycan recognition proteins in vitro. Proc Natl Acad Sci U S A. 2005 May 3;102(18):6455-60.
70. Li X, Wang S, Wang H, Gupta D. Differential expression of peptidoglycan recognition protein 2 in the skin and liver requires different transcription factors. J Biol Chem. 2006 Jul 28;281(30):20738-48.
71. Montañño AM, Tsujino F, Takahata N, Satta Y. Evolutionary origin of peptidoglycan recognition proteins in vertebrate innate immune system. BMC Evolut Biol. 2011;11(1):79.
72. Kashyap DR, Wang M, Liu LH, Boons GJ, Gupta D, Dziarski R. Peptidoglycan recognition proteins kill bacteria by activating protein-sensing two-component systems. Nat Med. 2011 Jun;17(6):676-83.
73. Kietzman C, Tuomanen E. PGRPs kill with an ancient weapon. Nat Med. 2011;17(6):665-6.
74. Kurata S. Extracellular and intracellular pathogen recognition by Drosophila PGRP-LE and PGRP-LC. Int Immunol. 2010;22(3):143-8.
75. Yano T, Mita S, Ohmori H, Oshima Y, Fujimoto Y, Ueda R, Takada H, Goldman WE, Fukase K, Silverman N, Yoshimori T, Kurata S. Autophagic control of listeria through intracellular innate immune recognition in drosophila. Nat Immunol. 2008;9(8):908-16.
76. Goto A, Yano T, Terashima J, Iwashita S, Oshima Y, Kurata S. Cooperative regulation of the induction of the novel antibacterial Listericin by peptidoglycan recognition protein LE and the JAK-STAT pathway. J Biol Chem. 2010 May 21;285(21):15731-8.