Molecular biology for formyl peptide receptors in human diseases

Journal of Molecular Medicine

Volumn 91, Issue 7, 2013, Pages 781-789

  Li, Yongsheng ^a,b   Ye, Duyun ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Chemoattractants; Formyl peptides; G protein coupled receptors; Inflammation

Indexed keywords

FORMYLPEPTIDE RECEPTOR;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; AMYLOIDOSIS; DEGENERATIVE DISEASE; DIABETES MELLITUS; HOST RESISTANCE; HUMAN; INFLAMMATION; MOLECULAR BIOLOGY; NEOPLASM; OBESITY; PATHOGENESIS; PROTEIN PHOSPHORYLATION; REVIEW;

ACQUIRED IMMUNODEFICIENCY SYNDROME; ANIMALS; DIABETES MELLITUS; HUMANS; INFLAMMATION; NEOPLASMS; NEURODEGENERATIVE DISEASES; OBESITY; RECEPTORS, FORMYL PEPTIDE;

EID: 84879845082     PISSN: 09462716     EISSN: 14321440     Source Type: Journal    
DOI: 10.1007/s00109-013-1005-5     Document Type: Review

References (101)

1. Schiffmann E, Showell HV, Corcoran BA, Ward PA, Smith E, Becker EL (1975) The isolation and partial characterization of neutrophil chemotactic factors from Escherichia coli. J Immunol 114:1831-1837
2. Schiffmann E, Corcoran BA, Wahl SM (1975) N-formylmethionyl peptides as chemoattractants for leucocytes. Proc Natl Acad Sci U S A 72:1059-1062
3. Marasco WA, Phan SH, Krutzsch H, Showell HJ, Feltner DE, Nairn R, Becker EL, Ward PA (1984) Purification and identification of formyl-methionyl-leucyl- phenylalanine as the major peptide neutrophil chemotactic factor produced by Escherichia coli. J Biol Chem 259:5430-5439
4. Showell HJ, Freer RJ, Zigmond SH, Schiffmann E, Aswanikumar S, Corcoran B, Becker EL (1976) The structure-activity relations of synthetic peptides as chemotactic factors and inducers of lysosomal secretion for neutrophils. J Exp Med 143:1154-1169
5. Bao L, Gerard NP, Eddy RL Jr, Shows TB, Gerard C (1992) Mapping of genes for the human C5a receptor (C5AR), human FMLP receptor (FPR), and two FMLP receptor homologue orphan receptors (FPRH1, FPRH2) to chromosome 19. Genomics 13:437-440
6. Ye RD, Cavanagh SL, Quehenberger O, Prossnitz ER, Cochrane CG (1992) Isolation of a cDNA that encodes a novel granulocyte N-formyl peptide receptor. Biochem Biophys Res Commun 184:582-589
7. Durstin M, Gao JL, Tiffany HL, McDermott D, Murphy PM (1994) Differential expression of members of the N-formylpeptide receptor gene cluster in human phagocytes. Biochem Biophys Res Commun 201:174-179
8. Yang D, Chen Q, Le Y, Wang JM, Oppenheim JJ (2001) Differential regulation of formyl peptide receptor-like 1 expression during the differentiation of monocytes to dendritic cells and macrophages. J Immunol 166:4092-4098
9. Betten A, Bylund J, Christophe T, Boulay F, Romero A, Hellstrand K, Dahlgren C (2001) A proinflammatory peptide from Helicobacter pylori activates monocytes to induce lymphocyte dysfunction and apoptosis. J Clin Invest 108:1221-1228
10. Christophe T, Karlsson A, Dugave C, Rabiet MJ, Boulay F, Dahlgren C (2001) The synthetic peptide Trp-Lys-Tyr-Met-Val-Met-NH2 specifically activates neutrophils through FPRL1/lipoxin A4 receptors and is an agonist for the orphan monocyte-expressed chemoattractant receptor FPRL2. J Biol Chem 276:21585-21593
11. Ye RD, Boulay F, Wang JM, Dahlgren C, Gerard C, Parmentier M, Serhan CN, Murphy PM (2009) International Union of Basic and Clinical Pharmacology. LXXIII. Nomenclature for the formyl peptide receptor (FPR) family. Pharmacol Rev 61:119-161
12. Chiang N, Serhan CN, Dahlen SE, Drazen JM, Hay DW, Rovati GE, Shimizu T, Yokomizo T, Brink C (2006) The lipoxin receptor ALX: potent ligand-specific and stereoselective actions in vivo. Pharmacol Rev 58:463-487
13. Gao JL, Murphy PM (1993) Species and subtype variants of the N-formyl peptide chemotactic receptor reveal multiple important functional domains. J Biol Chem 268:25395-25401
14. Maestes DC, Potter RM, Prossnitz ER (1999) Differential phosphorylation paradigms dictate desensitization and internalization of the N-formyl peptide receptor. J Biol Chem 274:29791-29795
15. Wenzel-Seifert K, Arthur JM, Liu HY, Seifert R (1999) Quantitative analysis of formyl peptide receptor coupling to g(i)alpha(1), g(i)alpha(2), and g(i)alpha(3). J Biol Chem 274:33259-33266
16. Perez HD, Holmes R, Vilander LR, Adams RR, Manzana W, Jolley D, Andrews WH (1993) Formyl peptide receptor chimeras define domains involved in ligand binding. J Biol Chem 268:2292-2295
17. Quehenberger O, Prossnitz ER, Cavanagh SL, Cochrane CG, Ye RD (1993) Multiple domains of the N-formyl peptide receptor are required for high-affinity ligand binding. Construction and analysis of chimeric N-formyl peptide receptors. J Biol Chem 268:18167-18175
18. Lala A, Gwinn M, De Nardin E (1999) Human formyl peptide receptor function role of conserved and nonconserved charged residues. Eur J Biochem 264:495-499
19. Villanueva MS, Beckers CJ, Pamer EG (1994) Infection with Listeria monocytogenes impairs sialic acid addition to host cell glycoproteins. J Exp Med 180:2137-2145
20. Kim JW, Cunningham JM (1993) N-linked glycosylation of the receptor for murine ecotropic retroviruses is altered in virus-infected cells. J Biol Chem 268:16316-16320
21. Chiang N, Fierro IM, Gronert K, Serhan CN (2000) Activation of lipoxin A(4) receptors by aspirin-triggered lipoxins and select peptides evokes ligand-specific responses in inflammation. J Exp Med 191:1197-1208
22. Li Y, Cai L, Wang H, Wu P, Gu W, Chen Y, Hao H, Tang K, Yi P, Liu M et al (2011) Pleiotropic regulation of macrophage polarization and tumorigenesis by formyl peptide receptor-2. Oncogene 30:3887-3899
23. Ali H, Richardson RM, Haribabu B, Snyderman R (1999) Chemoattractant receptor cross-desensitization. J Biol Chem 274:6027-6030
24. Ferguson SS, Barak LS, Zhang J, Caron MG (1996) G-protein-coupled receptor regulation: role of G-protein-coupled receptor kinases and arrestins. Can J Physiol Pharmacol 74:1095-1110
25. Luttrell LM, Daaka Y, Lefkowitz RJ (1999) Regulation of tyrosine kinase cascades by G-protein-coupled receptors. Curr Opin Cell Biol 11:177-183
26. Oakley RH, Laporte SA, Holt JA, Barak LS, Caron MG (1999) Association of beta-arrestin with G protein-coupled receptors during clathrin-mediated endocytosis dictates the profile of receptor resensitization. J Biol Chem 274:32248-32257
27. Ali H, Richardson RM, Tomhave ED, Didsbury JR, Snyderman R (1993) Differences in phosphorylation of formylpeptide and C5a chemoattractant receptors correlate with differences in desensitization. J Biol Chem 268:24247-24254
28. Tardif M, Mery L, Brouchon L, Boulay F (1993) Agonist-dependent phosphorylation of N-formylpeptide and activation peptide from the fifth component of C (C5a) chemoattractant receptors in differentiated HL60 cells. J Immunol 150:3534-3545
29. Pitcher JA, Freedman NJ, Lefkowitz RJ (1998) G protein-coupled receptor kinases. Annu Rev Biochem 67:653-692
30. Prossnitz ER, Gilbert TL, Chiang S, Campbell JJ, Qin S, Newman W, Sklar LA, Ye RD (1999) Multiple activation steps of the N-formyl peptide receptor. Biochemistry 38:2240-2247
31. Prossnitz ER (1997) Desensitization of N-formylpeptide receptor-mediated activation is dependent upon receptor phosphorylation. J Biol Chem 272:15213-15219
32. Li YS, Wu P, Zhou XY, Chen JG, Cai L, Wang F, Xu LM, Zhang XL, Chen Y, Liu SJ et al (2008) Formyl-peptide receptor like 1: a potent mediator of the Ca2+ release-activated Ca2+ current ICRAC. Arch Biochem Biophys 478:110-118
33. Liu M, Chen K, Yoshimura T, Liu Y, Gong W, Wang A, Gao JL, Murphy PM, Wang JM (2012) Formylpeptide receptors are critical for rapid neutrophil mobilization in host defense against Listeria monocytogenes. Sci Rep 2:786
34. Gao JL, Lee EJ, Murphy PM (1999) Impaired antibacterial host defense in mice lacking the N-formylpeptide receptor. J Exp Med 189:657-662
35. Kim SD, Kim YK, Lee HY, Kim YS, Jeon SG, Baek SH, Song DK, Ryu SH, Bae YS (2010) The agonists of formyl peptide receptors prevent development of severe sepsis after microbial infection. J Immunol 185:4302-4310
36. Yang D, Chen Q, Schmidt AP, Anderson GM, Wang JM, Wooters J, Oppenheim JJ, Chertov O (2000) LL-37, the neutrophil granule- and epithelial cell-derived cathelicidin, utilizes formyl peptide receptor-like 1 (FPRL1) as a receptor to chemoattract human peripheral blood neutrophils, monocytes, and T cells. J Exp Med 192:1069-1074
37. Dufton N, Hannon R, Brancaleone V, Dalli J, Patel HB, Gray M, D'Acquisto F, Buckingham JC, Perretti M, Flower RJ (2010) Anti-inflammatory role of the murine formyl-peptide receptor 2: ligand-specific effects on leukocyte responses and experimental inflammation. J Immunol 184:2611-2619
38. Ernst S, Lange C, Wilbers A, Goebeler V, Gerke V, Rescher U (2004) An annexin 1 N-terminal peptide activates leukocytes by triggering different members of the formyl peptide receptor family. J Immunol 172:7669-7676
39. Perretti M (2003) The annexin 1 receptor(s): is the plot unravelling? Trends Pharmacol Sci 24:574-579
40. McDonald B, Pittman K, Menezes GB, Hirota SA, Slaba I, Waterhouse CC, Beck PL, Muruve DA, Kubes P (2010) Intravascular danger signals guide neutrophils to sites of sterile inflammation. Science 330:362-366
41. Chen K, Le Y, Liu Y, Gong W, Ying G, Huang J, Yoshimura T, Tessarollo L, Wang JM (2010) A critical role for the g protein-coupled receptor mFPR2 in airway inflammation and immune responses. J Immunol 184:3331-3335
42. Krishnamoorthy S, Recchiuti A, Chiang N, Yacoubian S, Lee CH, Yang R, Petasis NA, Serhan CN (2010) Resolvin D1 binds human phagocytes with evidence for proresolving receptors. Proc Natl Acad Sci U S A 107:1660-1665
43. Goh J, Baird AW, O'Keane C, Watson RW, Cottell D, Bernasconi G, Petasis NA, Godson C, Brady HR, MacMathuna P (2001) Lipoxin A(4) and aspirin-triggered 15-epi-lipoxin A(4) antagonize TNF-alpha-stimulated neutrophil-enterocyte interactions in vitro and attenuate TNF-alpha-induced chemokine release and colonocyte apoptosis in human intestinal mucosa ex vivo. J Immunol 167:2772-2780
44. Sodin-Semrl S, Taddeo B, Tseng D, Varga J, Fiore S (2000) Lipoxin A4 inhibits IL-1 beta-induced IL-6, IL-8, and matrix metalloproteinase-3 production in human synovial fibroblasts and enhances synthesis of tissue inhibitors of metalloproteinases. J Immunol 164:2660-2666
45. Wu SH, Lu C, Dong L, Zhou GP, He ZG, Chen ZQ (2005) Lipoxin A4 inhibits TNF-alpha-induced production of interleukins and proliferation of rat mesangial cells. Kidney Int 68:35-46
46. Sun YP, Oh SF, Uddin J, Yang R, Gotlinger K, Campbell E, Colgan SP, Petasis NA, Serhan CN (2007) Resolvin D1 and its aspirin-triggered 17R epimer. Stereochemical assignments, anti-inflammatory properties, and enzymatic inactivation. J Biol Chem 282:9323-9334
47. Chiang N, Fredman G, Backhed F, Oh SF, Vickery T, Schmidt BA, Serhan CN (2012) Infection regulates pro-resolving mediators that lower antibiotic requirements. Nature 484:524-528
48. Aliberti J, Hieny S, Reis e Sousa C, Serhan CN, Sher A (2002) Lipoxin-mediated inhibition of IL-12 production by DCs: a mechanism for regulation of microbial immunity. Nat Immunol 3:76-82
49. Levy BD, De Sanctis GT, Devchand PR, Kim E, Ackerman K, Schmidt BA, Szczeklik W, Drazen JM, Serhan CN (2002) Multi-pronged inhibition of airway hyper-responsiveness and inflammation by lipoxin A(4). Nat Med 8:1018-1023
50. Jozsef L, Zouki C, Petasis NA, Serhan CN, Filep JG (2002) Lipoxin A4 and aspirin-triggered 15-epi-lipoxin A4 inhibit peroxynitrite formation, NF-kappa B and AP-1 activation, and IL-8 gene expression in human leukocytes. Proc Natl Acad Sci U S A 99:13266-13271
51. Nascimento-Silva V, Arruda MA, Barja-Fidalgo C, Villela CG, Fierro IM (2005) Novel lipid mediator aspirin-triggered lipoxin A4 induces heme oxygenase-1 in endothelial cells. Am J Physiol Cell Physiol 289:C557-C563
52. Souza DG, Fagundes CT, Amaral FA, Cisalpino D, Sousa LP, Vieira AT, Pinho V, Nicoli JR, Vieira LQ, Fierro IM et al (2007) The required role of endogenously produced lipoxin A4 and annexin-1 for the production of IL-10 and inflammatory hyporesponsiveness in mice. J Immunol 179:8533-8543
53. Rodgers K, McMahon B, Mitchell D, Sadlier D, Godson C (2005) Lipoxin A4 modifies platelet-derived growth factor-induced pro-fibrotic gene expression in human renal mesangial cells. Am J Pathol 167:683-694
54. El Kebir D, Jozsef L, Khreiss T, Pan W, Petasis NA, Serhan CN, Filep JG (2007) Aspirin-triggered lipoxins override the apoptosis-delaying action of serum amyloid A in human neutrophils: a novel mechanism for resolution of inflammation. J Immunol 179:616-622
55. Serhan CN (2007) Resolution phase of inflammation: novel endogenous anti-inflammatory and proresolving lipid mediators and pathways. Annu Rev Immunol 25:101-137
56. Glenner GG (1980) Amyloid deposits and amyloidosis. The beta-fibrilloses (first of two parts). N Engl J Med 302:1283-1292
57. Stone MJ (1990) Amyloidosis: a final common pathway for protein deposition in tissues. Blood 75:531-545
58. Selkoe DJ (1999) Translating cell biology into therapeutic advances in Alzheimer's disease. Nature 399:A23-A31
59. Akiyama H, Barger S, Barnum S, Bradt B, Bauer J, Cole GM, Cooper NR, Eikelenboom P, Emmerling M, Fiebich BL et al (2000) Inflammation and Alzheimer's disease. Neurobiol Aging 21:383-421
60. Rogers J (1995) Inflammation as a pathogenic mechanism in Alzheimer's disease. Arzneimittelforschung 45:439-442
61. Lim GP, Yang F, Chu T, Chen P, Beech W, Teter B, Tran T, Ubeda O, Ashe KH, Frautschy SA et al (2000) Ibuprofen suppresses plaque pathology and inflammation in a mouse model for Alzheimer's disease. J Neurosci 20:5709-5714
62. Yazawa H, Yu ZX, Le Takeda Y, Gong W, Ferrans VJ, Oppenheim JJ, Li CC, Wang JM (2001) Beta amyloid peptide (Abeta42) is internalized via the G-protein-coupled receptor FPRL1 and forms fibrillar aggregates in macrophages. FASEB J 15:2454-2462
63. Iribarren P, Chen K, Hu J, Gong W, Cho EH, Lockett S, Uranchimeg B, Wang JM (2005) CpG-containing oligodeoxynucleotide promotes microglial cell uptake of amyloid beta 1-42 peptide by up-regulating the expression of the G-protein- coupled receptor mFPR2. FASEB J 19:2032-2034
64. Chen K, Iribarren P, Hu J, Chen J, Gong W, Cho EH, Lockett S, Dunlop NM, Wang JM (2006) Activation of Toll-like receptor 2 on microglia promotes cell uptake of Alzheimer disease-associated amyloid beta peptide. J Biol Chem 281:3651-3659
65. Kong Y, Ruan L, Qian L, Liu X, Le Y (2010) Norepinephrine promotes microglia to uptake and degrade amyloid beta peptide through upregulation of mouse formyl peptide receptor 2 and induction of insulin-degrading enzyme. J Neurosci 30:11848-11857
66. Maderna P, Cottell DC, Toivonen T, Dufton N, Dalli J, Perretti M, Godson C (2010) FPR2/ALX receptor expression and internalization are critical for lipoxin A4 and annexin-derived peptide-stimulated phagocytosis. FASEB J 24:4240-4249
67. Hashimoto Y, Niikura T, Ito Y, Sudo H, Hata M, Arakawa E, Abe Y, Kita Y, Nishimoto I (2001) Detailed characterization of neuroprotection by a rescue factor humanin against various Alzheimer's disease-relevant insults. J Neurosci 21:9235-9245
68. Harada M, Habata Y, Hosoya M, Nishi K, Fujii R, Kobayashi M, Hinuma S (2004) N-Formylated humanin activates both formyl peptide receptor-like 1 and 2. Biochem Biophys Res Commun 324:255-261
69. Ying G, Iribarren P, Zhou Y, Gong W, Zhang N, Yu ZX, Le Y, Cui Y, Wang JM (2004) Humanin, a newly identified neuroprotective factor, uses the G protein-coupled formylpeptide receptor-like-1 as a functional receptor. J Immunol 172:7078-7085
70. Prusiner SB (1998) Prions. Proc Natl Acad Sci U S A 95:13363-13383
71. Perry VH, Bolton SJ, Anthony DC, Betmouni S (1998) The contribution of inflammation to acute and chronic neurodegeneration. Res Immunol 149:721-725
72. Brown DR, Kretzschmar HA (1997) Microglia and prion disease: a review. Histol Histopathol 12:883-892
73. Le Y, Yazawa H, Gong W, Yu Z, Ferrans VJ, Murphy PM, Wang JM (2001) The neurotoxic prion peptide fragment PrP(106-126) is a chemotactic agonist for the G protein-coupled receptor formyl peptide receptor-like 1. J Immunol 166:1448-1451
74. Ueda H, Howard OM, Grimm MC, Su SB, Gong W, Evans G, Ruscetti FW, Oppenheim JJ, Wang JM (1998) HIV-1 envelope gp41 is a potent inhibitor of chemoattractant receptor expression and function in monocytes. J Clin Invest 102:804-812
75. Wang JM, Ueda H, Howard OM, Grimm MC, Chertov O, Gong X, Gong W, Resau JH, Broder CC, Evans G et al (1998) HIV-1 envelope gp120 inhibits the monocyte response to chemokines through CD4 signal-dependent chemokine receptor down-regulation. J Immunol 161:4309-4317
76. Dragic T (2001) An overview of the determinants of CCR5 and CXCR4 co-receptor function. J Gen Virol 82:1807-1814
77. Nara PL, Garrity RR, Goudsmit J (1991) Neutralization of HIV-1: a paradox of humoral proportions. FASEB J 5:2437-2455
78. Shen W, Li B, Wetzel MA, Rogers TJ, Henderson EE, Su SB, Gong W, Le Y, Sargeant R, Dimitrov DS et al (2000) Down-regulation of the chemokine receptor CCR5 by activation of chemotactic formyl peptide receptor in human monocytes. Blood 96:2887-2894
79. Deng X, Ueda H, Su SB, Gong W, Dunlop NM, Gao JL, Murphy PM, Wang JM (1999) A synthetic peptide derived from human immunodeficiency virus type 1 gp120 downregulates the expression and function of chemokine receptors CCR5 and CXCR4 in monocytes by activating the 7-transmembrane G-protein-coupled receptor FPRL1/LXA4R. Blood 94:1165-1173
80. Shen W, Proost P, Li B, Gong W, Le Y, Sargeant R, Murphy PM, Van Damme J, Wang JM (2000) Activation of the chemotactic peptide receptor FPRL1 in monocytes phosphorylates the chemokine receptor CCR5 and attenuates cell responses to selected chemokines. Biochem Biophys Res Commun 272:276-283
81. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW Jr (2003) Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 112:1796-1808
82. Arkan MC, Hevener AL, Greten FR, Maeda S, Li ZW, Long JM, Wynshaw-Boris A, Poli G, Olefsky J, Karin M (2005) IKK-beta links inflammation to obesity-induced insulin resistance. Nat Med 11:191-198
83. Gonzalez-Periz A, Horrillo R, Ferre N, Gronert K, Dong B, Moran-Salvador E, Titos E, Martinez-Clemente M, Lopez-Parra M, Arroyo V et al (2009) Obesity-induced insulin resistance and hepatic steatosis are alleviated by omega-3 fatty acids: a role for resolvins and protectins. FASEB J 23:1946-1957
84. White PJ, Arita M, Taguchi R, Kang JX, Marette A (2010) Transgenic restoration of long-chain n-3 fatty acids in insulin target tissues improves resolution capacity and alleviates obesity-linked inflammation and insulin resistance in high-fat-fed mice. Diabetes 59:3066-3073
85. Hellmann J, Tang Y, Kosuri M, Bhatnagar A, Spite M (2011) Resolvin D1 decreases adipose tissue macrophage accumulation and improves insulin sensitivity in obese-diabetic mice. FASEB J 25:2399-2407
86. Balkwill F, Mantovani A (2010) Cancer and inflammation: implications for pharmacology and therapeutics. Clin Pharmacol Ther 87:401-406
87. Mantovani A, Allavena P, Sica A, Balkwill F (2008) Cancer-related inflammation. Nature 454:436-444
88. Le Y, Murphy PM, Wang JM (2002) Formyl-peptide receptors revisited. Trends Immunol 23:541-548
89. Zhou Y, Bian X, Le Y, Gong W, Hu J, Zhang X, Wang L, Iribarren P, Salcedo R, Howard OM et al (2005) Formylpeptide receptor FPR and the rapid growth of malignant human gliomas. J Natl Cancer Inst 97:823-835
90. Yang Y, Liu Y, Yao X, Ping Y, Jiang T, Liu Q, Xu S, Huang J, Mou H, Gong W et al (2011) Annexin 1 released by necrotic human glioblastoma cells stimulates tumor cell growth through the formyl peptide receptor 1. Am J Pathol 179:1504-1512
91. Huang J, Hu J, Bian X, Chen K, Gong W, Dunlop NM, Howard OM, Wang JM (2007) Transactivation of the epidermal growth factor receptor by formylpeptide receptor exacerbates the malignant behavior of human glioblastoma cells. Cancer Res 67:5906-5913
92. Kim JE, Kim HJ, Choi JM, Lee KH, Kim TY, Cho BK, Jung JY, Chung KY, Cho D, Park HJ (2010) The antimicrobial peptide human cationic antimicrobial protein-18/cathelicidin LL-37 as a putative growth factor for malignant melanoma. Br J Dermatol 163:959-967
93. Malle E, Sodin-Semrl S, Kovacevic A (2009) Serum amyloid A: an acute-phase protein involved in tumour pathogenesis. Cell Mol Life Sci 66:9-26
94. Zonder JA, Barlogie B, Durie BG, McCoy J, Crowley J, Hussein MA (2006) Thrombotic complications in patients with newly diagnosed multiple myeloma treated with lenalidomide and dexamethasone: benefit of aspirin prophylaxis. Blood 108:403, author reply 404
95. Perretti M, Chiang N, La M, Fierro IM, Marullo S, Getting SJ, Solito E, Serhan CN (2002) Endogenous lipid- and peptide-derived anti-inflammatory pathways generated with glucocorticoid and aspirin treatment activate the lipoxin A4 receptor. Nat Med 8:1296-1302
96. Serhan CN, Takano T, Clish CB, Gronert K, Petasis N (1999) Aspirin-triggered 15-epi-lipoxin A4 and novel lipoxin B4 stable analogs inhibit neutrophil-mediated changes in vascular permeability. Adv Exp Med Biol 469:287-293
97. Chen Y, Hao H, He S, Cai L, Li Y, Hu S, Ye D, Hoidal J, Wu P, Chen X (2010) Lipoxin A4 and its analogue suppress the tumor growth of transplanted H22 in mice: the role of antiangiogenesis. Mol Cancer Ther 9:2164-2174
98. Liu S, Wu P, Ye D, Huang Y, Zhou X, Li Y, Cai L (2009) Effects of lipoxin A(4) on CoCl(2)-induced angiogenesis and its possible mechanisms in human umbilical vein endothelial cells. Pharmacology 84:17-23
99. Liu Y, Chen K, Wang C, Gong W, Yoshimura T, Liu M, Wang JM (2013) Cell surface receptor FPR2 promotes antitumor host defense by limiting m2 polarization of macrophages. Cancer Res 73:550-560
100. Coffelt SB, Marini FC, Watson K, Zwezdaryk KJ, Dembinski JL, LaMarca HL, Tomchuck SL, Honer zu Bentrup K, Danka ES, Henkle SL et al (2009) The pro-inflammatory peptide LL-37 promotes ovarian tumor progression through recruitment of multipotent mesenchymal stromal cells. Proc Natl Acad Sci U S A 106:3806-3811
101. De Santo C, Arscott R, Booth S, Karydis I, Jones M, Asher R, Salio M, Middleton M, Cerundolo V (2010) Invariant NKT cells modulate the suppressive activity of IL-10-secreting neutrophils differentiated with serum amyloid A. Nat Immunol 11:1039-1046