Novel markers to delineate murine M1 and M2 macrophages

PLoS ONE

Volumn 10, Issue 12, 2015, Pages

  Jablonski, Kyle A ^a   Amici, Stephanie A ^a   Webb, Lindsay M ^a   Ruiz Rosado, Juan De Dios ^b   Popovich, Phillip G ^c   Partida Sanchez, Santiago ^b   Guerau De arellano, Mireia ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b THE RESEARCH INSTITUTE AT NATIONWIDE CHILDREN S HOSPITAL   (United States)

^c THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGINASE 1; BIOLOGICAL MARKER; CD38 ANTIGEN; EARLY GROWTH RESPONSE FACTOR 2; FORMYLPEPTIDE RECEPTOR; FORMYLPEPTIDE RECEPTOR 2; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 18; MYC PROTEIN; UNCLASSIFIED DRUG; LIPOPOLYSACCHARIDE; MESSENGER RNA; TRANSCRIPTOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; CONTROLLED STUDY; FLOW CYTOMETRY; GENE IDENTIFICATION; IN VITRO STUDY; IN VIVO STUDY; MACROPHAGE; MOUSE; NONHUMAN; PHENOTYPE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; ANIMAL; C57BL MOUSE; CHEMICALLY INDUCED; CYTOLOGY; ENZYME IMMUNOASSAY; GENETICS; HIGH THROUGHPUT SEQUENCING; INFLAMMATION; MACROPHAGE ACTIVATION; METABOLISM; PHYSIOLOGY; PROCEDURES; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; BIOMARKERS; FLOW CYTOMETRY; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; IMMUNOENZYME TECHNIQUES; INFLAMMATION; LIPOPOLYSACCHARIDES; MACROPHAGE ACTIVATION; MACROPHAGES; MICE; MICE, INBRED C57BL; PHENOTYPE; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TRANSCRIPTOME;

EID: 84956883431     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0145342     Document Type: Article

References (69)

1. Gow DJ, Sester DP, Hume DA. CSF-1, IGF-1, and the control of postnatal growth and development. J Leukoc Biol. Society for Leukocyte Biology; 2010; 88: 475-481. doi:10.1189/jlb.0310158 PMID: 20519640.
2. Pollard JW. Trophic macrophages in development and disease. Nature Reviews Immunology. 2009; 9: 259-270. doi:10.1038/nri2528 PMID: 19282852.
3. Sica A, Mantovani A. Macrophage plasticity and polarization: in vivo veritas. J Clin Invest. 2012; 122: 787-795. doi:10.1172/JCI59643 PMID: 22378047.
4. Wynn TA, Chawla A, Pollard JW. Macrophage biology in development, homeostasis and disease. Nature. 2013; 496: 445-455. doi:10.1038/nature12034 PMID: 23619691.
5. Benoit M, Desnues B, Mege J- L. Macrophage polarization in bacterial infections. J Immunol. 2008; 181: 3733-3739. PMID: 18768823.
6. Andersson U, Wang H, Palmblad K, Aveberger AC, Bloom O, Erlandsson-Harris H, et al. High mobility group 1 protein (HMG-1) stimulates proinflammatory cytokine synthesis in human monocytes. J Exp Med. 2000; 192: 565-570. Available: http://eutils.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&id=10952726&retmode=ref&cmd=prlinksPMID:10952726.
7. Xue J, Schmidt SV, Sander J, Draffehn A, Krebs W, Quester I, et al. Transcriptome-based network analysis reveals a spectrum model of human macrophage activation. Immunity. 2014; 40: 274-288. doi:10.1016/j.immuni.2014.01.006 PMID: 24530056.
8. Mosser DM, Edwards JP. Exploring the full spectrum of macrophage activation. Nat Rev Immunol. 2008; 8: 958-969. doi:10.1038/nri2448 PMID: 19029990.
9. Martinez FO, Helming L, Gordon S. Alternative activation of macrophages: An immunologic functional perspective. Annu Rev Immunol. 2009; 27: 451-483. doi:10.1146/annurev.immunol.021908.132532 PMID: 19105661.
10. Bronte V, Murray PJ. Understanding local macrophage phenotypes in disease: modulating macrophage function to treat cancer. Nat Med. 2015; 21: 117-119. doi:10.1038/nm.3794 PMID: 25654601.
11. Murray PJ, Allen JE, Biswas SK, Fisher EA, Gilroy DW, Goerdt S, et al. Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity. 2014; 41: 14-20. doi:10.1016/j.immuni.2014.06.008 PMID: 25035950.
12. Porta C, Rimoldi M, Raes G, Brys L, Ghezzi P, Di Liberto D, et al. Tolerance and M2 (alternative) macrophage polarization are related processes orchestrated by p50 nuclear factor kappaB. Proc Natl Acad Sci USA. 2009; 106: 14978-14983. doi:10.1073/pnas.0809784106 PMID: 19706447.
13. Mokarram N, Bellamkonda RV. A Perspective on Immunomodulation and Tissue Repair. Ann Biomed Eng. 2013. doi:10.1007/s10439-013-0941-0.
14. Mantovani A, Biswas SK, Galdiero MR, Sica A, Locati M. Macrophage plasticity and polarization in tissue repair and remodelling. J Pathol. 2013; 229: 176-185. doi:10.1002/path.4133 PMID: 23096265.
15. Jouanguy E, Döffinger R, Dupuis S, Pallier A, Altare F, Casanova JL. IL-12 and IFN-gamma in host defense against mycobacteria and salmonella in mice and men. Curr Opin Immunol. 1999; 11: 346- 351. PMID: 10375558.
16. Pfeffer K, Matsuyama T, Kündig TM, Wakeham A, Kishihara K, Shahinian A, et al. Mice deficient for the 55 kd tumor necrosis factor receptor are resistant to endotoxic shock, yet succumb to L. monocytogenes infection. Cell. 1993; 73: 457-467. PMID: 8387893.
17. Ordway D, Harton M, Henao-Tamayo M, Montoya R, Orme IM, Gonzalez-Juarrero M. Enhanced macrophage activity in granulomatous lesions of immune mice challenged with Mycobacterium tuberculosis. The Journal of Immunology. 2006; 176: 4931-4939. PMID: 16585589.
18. Vazquez-Torres A, Xu Y, Jones-Carson J, Holden DW, Lucia SM, Dinauer MC, et al. Salmonella pathogenicity island 2-dependent evasion of the phagocyte NADPH oxidase. Science. 2000; 287: 1655- 1658. PMID: 10698741.
19. Bost KL, Clements JD. Intracellular Salmonella dublin induces substantial secretion of the 40-kilodalton subunit of interleukin-12 (IL-12) but minimal secretion of IL-12 as a 70-kilodalton protein in murine macrophages. Infect Immun. 1997; 65: 3186-3192. PMID: 9234773.
20. Dornand J, Gross A, Lafont V, Liautard J, Oliaro J, Liautard J- P. The innate immune response against Brucella in humans. Vet Microbiol. 2002; 90: 383-394. PMID: 12414158.
21. Miller BH, Fratti RA, Poschet JF, Timmins GS, Master SS, Burgos M, et al. Mycobacteria inhibit nitric oxide synthase recruitment to phagosomes during macrophage infection. Infect Immun. 2004; 72: 2872-2878. PMID: 15102799.
22. Kahnert A, Seiler P, Stein M, Bandermann S, Hahnke K, Mollenkopf H, et al. Alternative activation deprives macrophages of a coordinated defense program to Mycobacterium tuberculosis. Eur J Immunol. 2006; 36: 631-647. doi:10.1002/eji.200535496 PMID: 16479545.
23. Valledor AF, Comalada M, Santamaría-Babi LF, Lloberas J, Celada A. Macrophage proinflammatory activation and deactivation: A question of balance. Adv Immunol. 2010; 108: 1-20. doi:10.1016/B978-0-12-380995-7.00001-X PMID: 21056727.
24. Vogel DY, Vereyken EJ, Glim JE, Heijnen PD, Moeton M, van der Valk P, et al. Macrophages in inflammatory multiple sclerosis lesions have an intermediate activation status. Journal of Neuroinflammation. BioMed Central Ltd; 2013; 10: 35. doi:10.1186/1742-2094-10-35.
25. Butovsky O, Siddiqui S, Gabriely G, Lanser AJ, Dake B, Murugaiyan G, et al. Modulating inflammatory monocytes with a unique microRNA gene signature ameliorates murine ALS. Journal of Clinical Investigation. American Society for Clinical Investigation; 2012; 122: 3063-3087. doi:10.1172/JCI62636 PMID: 22863620.
26. Wang G, Zhang J, Hu X, Zhang L, Mao L, Jiang X, et al. Microglia/macrophage polarization dynamics in white matter after traumatic brain injury. J Cereb Blood Flow Metab. 2013; 33: 1864-1874. doi:10.1038/jcbfm.2013.146 PMID: 23942366.
27. Hu X, Li P, Guo Y, Wang H, Leak RK, Chen S, et al. Microglia/macrophage polarization dynamics reveal novel mechanism of injury expansion after focal cerebral ischemia. Stroke; a journal of cerebral circulation. Lippincott Williams & Wilkins; 2012; 43: 3063-3070. doi:10.1161/STROKEAHA.112.659656.
28. Kigerl KA, Gensel JC, Ankeny DP, Alexander JK, Donnelly DJ, Popovich PG. Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J Neurosci. 2009; 29: 13435-13444. doi:10.1523/JNEUROSCI.3257-09.2009 PMID: 19864556.
29. Moreira AP, Hogaboam CM. Macrophages in allergic asthma: fine-tuning their pro- And anti-inflammatory actions for disease resolution. J Interferon Cytokine Res. 2011; 31: 485-491. doi:10.1089/jir.2011.0027 PMID: 21631355.
30. Raes G, De Baetselier P, Noël W, Beschin A, Brombacher F, Hassanzadeh Gh G. Differential expression of FIZZ1 and Ym1 in alternatively versus classically activated macrophages. J Leukoc Biol. 2002; 71: 597-602. PMID: 11927645.
31. Kasmi El KC, Qualls JE, Pesce JT, Smith AM, Thompson RW, Henao-Tamayo M, et al. Toll-like receptor- induced arginase 1 in macrophages thwarts effective immunity against intracellular pathogens. Nat Immunol. 2008; 9: 1399-1406. doi:10.1038/ni.1671 PMID: 18978793.
32. Antonios JK, Yao Z, Li C, Rao AJ, Goodman SB. Macrophage polarization in response to wear particles in vitro. Cell Mol Immunol. 2013; 10: 471-482. doi:10.1038/cmi.2013.39 PMID: 24013843.
33. Scotton CJ, Martinez FO, Smelt MJ, Sironi M, Locati M, Mantovani A, et al. Transcriptional profiling reveals complex regulation of the monocyte IL-1 beta system by IL-13. The Journal of Immunology. 2005; 174: 834-845. PMID: 15634905.
34. Martinez FO, Gordon S, Locati M, Mantovani A. Transcriptional profiling of the human monocyte-tomacrophage differentiation and polarization: new molecules and patterns of gene expression. The Journal of Immunology. 2006; 177: 7303-7311. PMID: 17082649.
35. Martinez FO, Helming L, Milde R, Varin A, Melgert BN, Draijer C, et al. Genetic programs expressed in resting and IL-4 alternatively activated mouse and human macrophages: similarities and differences. Blood. 2013; 121: 57-69. doi:10.1182/blood-2012-06-436212 PMID: 23293084.
36. Chartouni El C, Rehli M. Comprehensive analysis of TLR4-induced transcriptional responses in interleukin 4-primed mouse macrophages. Immunobiology. 2010; 215: 780-787. doi:10.1016/j.imbio.2010.05.032 PMID: 20692533.
37. Mabbott NA, Kenneth Baillie J, Hume DA, Freeman TC. Meta-analysis of lineage-specific gene expression signatures in mouse leukocyte populations. Immunobiology. 2010; 215: 724-736. doi:10.1016/j.imbio.2010.05.012 PMID: 20580463.
38. Reich M, Liefeld T, Gould J, Lerner J, Tamayo P, Mesirov JP. GenePattern 2.0. Nat Genet. 2006; 38: 500-501. doi:10.1038/ng0506-500 PMID: 16642009.
39. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001; 25: 402-408. doi:10.1006/meth.2001.1262 PMID: 11846609.
40. Larionov A, Krause A, Miller W. A standard curve based method for relative real time PCR data processing. BMC Bioinformatics. BioMed Central Ltd; 2005; 6: 62. doi:10.1186/1471-2105-6-62 PMID: 15780134.
41. Gordon S, Martinez FO. Alternative activation of macrophages: mechanism and functions. Immunity. 2010; 32: 593-604. doi:10.1016/j.immuni.2010.05.007 PMID: 20510870.
42. Schattgen SA, Fitzgerald KA. The PYHIN protein family as mediators of host defenses. Immunol Rev. 2011; 243: 109-118. doi:10.1111/j.1600-065X.2011.01053.x PMID: 21884171.
43. Kato H, Sato S, Yoneyama M, Yamamoto M, Uematsu S, Matsui K, et al. Cell type-specific involvement of RIG-I in antiviral response. Immunity. 2005; 23: 19-28. doi:10.1016/j.immuni.2005.04.010 PMID: 16039576.
44. Link JM, Hurlin PJ. The activities of MYC, MNT and the MAX-interactome in lymphocyte proliferation and oncogenesis. Biochim Biophys Acta. 2015; 1849: 554-562. doi:10.1016/j.bbagrm.2014.04.004 PMID: 24731854.
45. Safford M, Collins S, Lutz MA, Allen A, Huang C-T, Kowalski J, et al. Egr-2 and Egr-3 are negative regulators of T cell activation. Nat Immunol. 2005; 6: 472-480. doi:10.1038/ni1193 PMID: 15834410.
46. Chamberlain LM, Holt-Casper D, Gonzalez-Juarrero M, Grainger DW. Extended culture of macrophages from different sources and maturation results in a common M2 phenotype. J Biomed Mater Res A. 2015. doi:10.1002/jbm.a.35415.
47. Rose S, Misharin A, Perlman H. A novel Ly6C/Ly6G-based strategy to analyze the mouse splenic myeloid compartment. Cytometry. 2012; 81: 343-350. doi:10.1002/cyto.a.22012 PMID: 22213571.
48. Alder JK, Georgantas RW, Hildreth RL, Kaplan IM, Morisot S, Yu X, et al. Kruppel-like factor 4 is essential for inflammatory monocyte differentiation in vivo. The Journal of Immunology. 2008; 180: 5645- 5652. PMID: 18390749.
49. Feinberg MW, Cao Z, Wara AK, Lebedeva MA, Senbanerjee S, Jain MK. Kruppel-like factor 4 is a mediator of proinflammatory signaling in macrophages. J Biol Chem. 2005; 280: 38247-38258. doi:10.1074/jbc.M509378200 PMID: 16169848.
50. Liao X, Sharma N, Kapadia F, Zhou G, Lu Y, Hong H, et al. Krüppel-like factor 4 regulates macrophage polarization. J Clin Invest. 2011; 121: 2736-2749. doi:10.1172/JCI45444 PMID: 21670502.
51. Zhang C, Bai N, Chang A, Zhang Z, Yin J, Shen W, et al. ATF4 is directly recruited by TLR4 signaling and positively regulates TLR4-trigged cytokine production in human monocytes. Cell Mol Immunol. 2013; 10: 84-94. doi:10.1038/cmi.2012.57 PMID: 23241898.
52. Kobayashi T, Matsuoka K, Sheikh SZ, Elloumi HZ, Kamada N, Hisamatsu T, et al. NFIL3 is a regulator of IL-12 p40 in macrophages and mucosal immunity. J Immunol. 2011; 186: 4649-4655. doi:10.4049/jimmunol.1003888 PMID: 21383239.
53. Oukka M, Kim ST, Lugo G, Sun J, Wu L-C, Glimcher LH. A mammalian homolog of Drosophila schnurri, KRC, regulates TNF receptor-driven responses and interacts with TRAF2. Mol Cell. 2002; 9: 121-131. PMID: 11804591.
54. Lin C-C, Bradstreet TR, Schwarzkopf EA, Sim J, Carrero JA, Chou C, et al. Bhlhe40 controls cytokine production by T cells and is essential for pathogenicity in autoimmune neuroinflammation. Nat Commun. 2014; 5: 3551. doi:10.1038/ncomms4551 PMID: 24699451.
55. O'Carroll C, Fagan A, Shanahan F, Carmody RJ. Identification of a unique hybrid macrophage-polarization state following recovery from lipopolysaccharide tolerance. J Immunol. 2014; 192: 427-436. doi:10.4049/jimmunol.1301722 PMID: 24337373.
56. Bae Y-S, Yi HJ, Lee H-Y, Jo EJ, Kim JI, Lee TG, et al. Differential activation of formyl peptide receptorlike 1 by peptide ligands. The Journal of Immunology. 2003; 171: 6807-6813. PMID: 14662886.
57. Liu Y, Chen K, Wang C, Gong W, Yoshimura T, Liu M, et al. Cell surface receptor FPR2 promotes antitumor host defense by limiting M2 polarization of macrophages. Cancer Res. 2013; 73: 550-560. doi:10.1158/0008-5472.CAN-12-2290 PMID: 23139214.
58. Partida-Sánchez S, Iribarren P, Moreno-García ME, Gao J-L, Murphy PM, Oppenheimer N, et al. Chemotaxis and calcium responses of phagocytes to formyl peptide receptor ligands is differentially regulated by cyclic ADP ribose. The Journal of Immunology. 2004; 172: 1896-1906. PMID: 14734775.
59. Malavasi F, Deaglio S, Funaro A, Ferrero E, Horenstein AL, Ortolan E, et al. Evolution and function of the ADP ribosyl cyclase/CD38 gene family in physiology and pathology. Physiol Rev. 2008; 88: 841- 886. doi:10.1152/physrev.00035.2007 PMID: 18626062.
60. Musso T, Deaglio S, Franco L, Calosso L, Badolato R, Garbarino G, et al. CD38 expression and functional activities are up-regulated by IFN-gamma on human monocytes and monocytic cell lines. J Leukoc Biol. 2001; 69: 605-612. PMID: 11310847.
61. Partida-Sánchez S, Cockayne DA, Monard S, Jacobson EL, Oppenheimer N, Garvy B, et al. Cyclic ADP-ribose production by CD38 regulates intracellular calcium release, extracellular calcium influx and chemotaxis in neutrophils and is required for bacterial clearance in vivo. Nat Med. 2001; 7: 1209-1216. doi:10.1038/nm1101-1209 PMID: 11689885.
62. Partida-Sánchez S, Randall TD, Lund FE. Innate immunity is regulated by CD38, an ecto-enzyme with ADP-ribosyl cyclase activity. Microbes Infect. 2003; 5: 49-58. PMID: 12593973.
63. Viegas MS, do Carmo A, Silva T, Seco F, Serra V, Lacerda M, et al. CD38 plays a role in effective containment of mycobacteria within granulomata and polarization of Th1 immune responses against Mycobacterium avium. Microbes Infect. 2007; 9: 847-854. doi:10.1016/j.micinf.2007.03.003 PMID: 17533152.
64. Takenouchi R, Inoue K, Kambe Y, Miyata A. N-arachidonoyl glycine induces macrophage apoptosis via GPR18. Biochem Biophys Res Commun. 2012; 418: 366-371. doi:10.1016/j.bbrc.2012.01.027 PMID: 22266325.
65. Arpa L, Valledor AF, Lloberas J, Celada A. IL-4 blocks M-CSF-dependent macrophage proliferation by inducing p21Waf1 in a STAT6-dependent way. Eur J Immunol. 2009; 39: 514-526. doi:10.1002/eji.200838283 PMID: 19130475.
66. Schroder AJ, Pavlidis P, Arimura A, Capece D, Rothman PB. Cutting edge: STAT6 serves as a positive and negative regulator of gene expression in IL-4-stimulated B lymphocytes. The Journal of Immunology. 2002; 168: 996-1000. PMID: 11801631.
67. Gabet Y, Baniwal SK, Leclerc N, Shi Y, Kohn-Gabet AE, Cogan J, et al. Krox20/EGR2 deficiency accelerates cell growth and differentiation in the monocytic lineage and decreases bone mass. Blood. 2010; 116: 3964-3971. doi:10.1182/blood-2010-01-263830 PMID: 20716776.
68. Weilemann A, Grau M, Erdmann T, Merkel O, Sobhiafshar U, Anagnostopoulos I, et al. Essential role of IRF4 and MYC signaling for survival of anaplastic large cell lymphoma. Blood. 2015; 125: 124-132. doi:10.1182/blood-2014-08-594507 PMID: 25359993.
69. Pello OM, De Pizzol M, Mirolo M, Soucek L, Zammataro L, Amabile A, et al. Role of c-MYC in alternative activation of human macrophages and tumor-associated macrophage biology. Blood. 2012; 119: 411- 421. doi:10.1182/blood-2011-02-339911 PMID: 22067385.