Macrophage development and polarization in chronic inflammation

Seminars in Immunology

Volumn 27, Issue 4, 2015, Pages 257-266

  Motwani, Madhur P ^a   Gilroy, Derek W ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE;

ADAPTIVE IMMUNITY; CELL MATURATION; CELL POLARITY; CHRONIC INFLAMMATION; HUMAN; IN VITRO STUDY; INFLAMMATION; MACROPHAGE; MONOCYTE; NONHUMAN; PHAGOCYTOSIS; PHENOTYPE; POLARIZATION; REVIEW; SEPSIS; ANIMAL; CYTOLOGY; IMMUNOLOGY;

ANIMALS; HUMANS; INFLAMMATION; MACROPHAGES; MONOCYTES; SEPSIS;

EID: 84951908279     PISSN: 10445323     EISSN: 10963618     Source Type: Journal    
DOI: 10.1016/j.smim.2015.07.002     Document Type: Review

References (170)

1. Mantovani A., Sica A., Sozzani S., Allavena P., Vecchi A., Locati M. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 2004, 25:677-686.
2. Ziegler-Heitbrock L., Ancuta P., Crowe S., Dalod M., Grau V., Hart D.N., Leenen P.J., Liu Y.J., MacPherson G., Randolph G.J., Scherberich J., Schmitz J., Shortman K., Sozzani S., Strobl H., Zembala M., Austyn J.M., Lutz M.B. Nomenclature of monocytes and dendritic cells in blood. Blood 2010, 116:e74-e80.
3. Guilliams M., Ginhoux F., Jakubzick C., Naik S.H., Onai N., Schraml B.U., Segura E., Tussiwand R., Yona S. Dendritic cells, monocytes and macrophages: a unified nomenclature based on ontogeny. Nat. Rev. Immunol. 2014, 14:571-578.
4. Cros J., Cagnard N., Woollard K., Patey N., Zhang S.Y., Senechal B., Puel A., Biswas S.K., Moshous D., Picard C., Jais J.P., D'Cruz D., Casanova J.L., Trouillet C., Geissmann F. Human CD14dim monocytes patrol and sense nucleic acids and viruses via TLR7 and TLR8 receptors. Immunity 2010, 33:375-386.
5. Skrzeczynska-Moncznik J., Bzowska M., Loseke S., Grage-Griebenow E., Zembala M., Pryjma J. Peripheral blood CD14high CD16+ monocytes are main producers of IL-10. Scand. J. Immunol. 2008, 67:152-159.
6. Geissmann F., Jung S., Littman D.R. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 2003, 19:71-82.
7. Sunderkotter C., Nikolic T., Dillon M.J., Van Rooijen N., Stehling M., Drevets D.A., Leenen P.J. Subpopulations of mouse blood monocytes differ in maturation stage and inflammatory response. J. Immunol. 2004, 172:4410-4417.
8. Auffray C., Fogg D., Garfa M., Elain G., Join-Lambert O., Kayal S., Sarnacki S., Cumano A., Lauvau G., Geissmann F. Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior. Science 2007, 317:666-670.
9. Geissmann F., Auffray C., Palframan R., Wirrig C., Ciocca A., Campisi L., Narni-Mancinelli E., Lauvau G. Blood monocytes: distinct subsets, how they relate to dendritic cells, and their possible roles in the regulation of T-cell responses. Immunol. Cell Biol. 2008, 86:398-408.
10. Palframan R.T., Jung S., Cheng G., Weninger W., Luo Y., Dorf M., Littman D.R., Rollins B.J., Zweerink H., Rot A., von Andrian U.H. Inflammatory chemokine transport and presentation in HEV: a remote control mechanism for monocyte recruitment to lymph nodes in inflamed tissues. J. Exp. Med. 2001, 194:1361-1373.
11. Weiner L.M., Li W., Holmes M., Catalano R.B., Dovnarsky M., Padavic K., Alpaugh R.K., Phase I. trial of recombinant macrophage colony-stimulating factor and recombinant gamma-interferon: toxicity, monocytosis, and clinical effects. Cancer Res. 1994, 54:4084-4090.
12. Saleh M.N., Goldman S.J., LoBuglio A.F., Beall A.C., Sabio H., McCord M.C., Minasian L., Alpaugh R.K., Weiner L.M., Munn D.H. CD16+ monocytes in patients with cancer: spontaneous elevation and pharmacologic induction by recombinant human macrophage colony-stimulating factor. Blood 1995, 85:2910-2917.
13. Korkosz M., Bukowska-Strakova K., Sadis S., Grodzicki T., Siedlar M. Monoclonal antibodies against macrophage colony-stimulating factor diminish the number of circulating intermediate and nonclassical (CD14(++)CD16(+)/CD14(+)CD16(++)) monocytes in rheumatoid arthritis patient. Blood 2012, 119:5329-5330.
14. Varol C., Landsman L., Fogg D.K., Greenshtein L., Gildor B., Margalit R., Kalchenko V., Geissmann F., Jung S. Monocytes give rise to mucosal, but not splenic, conventional dendritic cells. J. Exp. Med. 2007, 204:171-180.
15. Yona S., Kim K.W., Wolf Y., Mildner A., Varol D., Breker M., Strauss-Ayali D., Viukov S., Guilliams M., Misharin A., Hume D.A., Perlman H., Malissen B., Zelzer E., Jung S. Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity 2013, 38:79-91.
16. Belge K.U., Dayyani F., Horelt A., Siedlar M., Frankenberger M., Frankenberger B., Espevik T., Ziegler-Heitbrock L. The proinflammatory CD14+CD16+DR++ monocytes are a major source of TNF. J. Immunol. 2002, 168:3536-3542.
17. Burke B., Ahmad R., Staples K.J., Snowden R., Kadioglu A., Frankenberger M., Hume D.A., Ziegler-Heitbrock L. Increased TNF expression in CD43++ murine blood monocytes. Immunol. Lett. 2008, 118:142-147.
18. Qu C., Edwards E.W., Tacke F., Angeli V., Llodra J., Sanchez-Schmitz G., Garin A., Haque N.S., Peters W., van Rooijen N., Sanchez-Torres C., Bromberg J., Charo I.F., Jung S., Lira S.A., Randolph G.J. Role of CCR8 and other chemokine pathways in the migration of monocyte-derived dendritic cells to lymph nodes. J. Exp. Med. 2004, 200:1231-1241.
19. Randolph G.J., Jakubzick C., Qu C. Antigen presentation by monocytes and monocyte-derived cells. Curr. Opin. Immunol. 2008, 20:52-60.
20. Ingersoll M.A., Spanbroek R., Lottaz C., Gautier E.L., Frankenberger M., Hoffmann R., Lang R., Haniffa M., Collin M., Tacke F., Habenicht A.J., Ziegler-Heitbrock L., Randolph G.J. Comparison of gene expression profiles between human and mouse monocyte subsets. Blood 2010, 115:e10-e19.
21. Kim J., Woods A., Becker-Dunn E., Bottomly K. Distinct functional phenotypes of cloned Ia-restricted helper T cells. J. Exp. Med. 1985, 162:188-201.
22. Melchers I., Fey K., Eichmann K. Quantitative studies on T cell diversity. III. Limiting dilution analysis of precursor cells for T helper cells reactive to xenogeneic erythrocytes. J. Exp. Med. 1982, 156:1587-1603.
23. Imperiale M.J., Faherty D.A., Sproviero J.F., Zauderer M. Functionally distinct helper T cells enriched under different culture conditions cooperate with different B cells. J. Immunol. 1982, 129:1843-1848.
24. Waldmann H. Conditions determining the generation and expression of T helper cells. Immunol. Rev. 1977, 35:121-145.
25. Swierkosz J.E., Marrack P., Kappler J.W. Functional analysis of T cells expressing Ia antigens. I. Demonstration of helper T-cell heterogeneity. J. Exp. Med. 1979, 150:1293-1309.
26. Tada T., Takemori T., Okumura K., Nonaka M., Tokuhisa T. Two distinct types of helper T cells involved in the secondary antibody response: independent and synergistic effects of Ia- and Ia+ helper T cells. J. Exp. Med. 1978, 147:446-458.
27. Mosmann T.R., Cherwinski H., Bond M.W., Giedlin M.A., Coffman R.L. Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. J. Immunol. 1986, 136:2348-2357.
28. Mackaness G.B. Cellular resistance to infection. J. Exp. Med. 1962, 116:381-406.
29. Nathan C.F., Murray H.W., Wiebe M.E., Rubin B.Y. Identification of interferon-gamma as the lymphokine that activates human macrophage oxidative metabolism and antimicrobial activity. J. Exp. Med. 1983, 158:670-689.
30. Pace J.L., Russell S.W., Schreiber R.D., Altman A., Katz D.H. Macrophage activation: priming activity from a T-cell hybridoma is attributable to interferon-gamma. Proc. Natl. Acad. Sci. USA 1983, 80:3782-3786.
31. Celada A., Gray P.W., Rinderknecht E., Schreiber R.D. Evidence for a gamma-interferon receptor that regulates macrophage tumoricidal activity. J. Exp. Med. 1984, 160:55-74.
32. Stein M., Keshav S., Harris N., Gordon S. Interleukin 4 potently enhances murine macrophage mannose receptor activity: a marker of alternative immunologic macrophage activation. J. Exp. Med. 1992, 176:287-292.
33. Doyle A.G., Herbein G., Montaner L.J., Minty A.J., Caput D., Ferrara P., Gordon S. Interleukin-13 alters the activation state of murine macrophages in vitro: comparison with interleukin-4 and interferon-gamma. Eur. J. Immunol. 1994, 24:1441-1445.
34. Mills C.D., Kincaid K., Alt J.M., Heilman M.J., Hill A.M. M-1/M-2 macrophages and the Th1/Th2 paradigm. J. Immunol. 2000, 164:6166-6173.
35. Mosser D.M., Edwards J.P. Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol. 2008, 8:958-969.
36. Verreck F.A., de Boer T., Langenberg D.M., Hoeve M.A., Kramer M., Vaisberg E., Kastelein R., Kolk A., de Waal-Malefyt R., Ottenhoff T.H. Human IL-23-producing type 1 macrophages promote but IL-10-producing type 2 macrophages subvert immunity to (myco)bacteria. Proc. Natl. Acad. Sci. USA 2004, 101:4560-4565.
37. Murray P.J., Allen J.E., Biswas S.K., Fisher E.A., Gilroy D.W., Goerdt S., Gordon S., Hamilton J.A., Ivashkiv L.B., Lawrence T., Locati M., Mantovani A., Martinez F.O., Mege J.L., Mosser D.M., Natoli G., Saeij J.P., Schultze J.L., Shirey K.A., Sica A., Suttles J., Udalova I., van Ginderachter J.A., Vogel S.N., Wynn T.A. Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity 2014, 41:14-20.
38. Lang R., Patel D., Morris J.J., Rutschman R.L., Murray P.J. Shaping gene expression in activated and resting primary macrophages by IL-10. J. Immunol. 2002, 169:2253-2263.
39. Gordon S. Alternative activation of macrophages. Nat. Rev. Immunol. 2003, 3:23-35.
40. Mantovani A., Sozzani S., Locati M., Allavena P., Sica A. Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol. 2002, 23:549-555.
41. Krausgruber T., Blazek K., Smallie T., Alzabin S., Lockstone H., Sahgal N., Hussell T., Feldmann M., Udalova I.A. IRF5 promotes inflammatory macrophage polarization and TH1-TH17 responses. Nat. Immunol. 2011, 12:231-238.
42. Xu H., Zhu J., Smith S., Foldi J., Zhao B., Chung A.Y., Outtz H., Kitajewski J., Shi C., Weber S., Saftig P., Li Y., Ozato K., Blobel C.P., Ivashkiv L.B., Hu X. Notch-RBP-J signaling regulates the transcription factor IRF8 to promote inflammatory macrophage polarization. Nat. Immunol. 2012, 13:642-650.
43. Satoh T., Takeuchi O., Vandenbon A., Yasuda K., Tanaka Y., Kumagai Y., Miyake T., Matsushita K., Okazaki T., Saitoh T., Honma K., Matsuyama T., Yui K., Tsujimura T., Standley D.M., Nakanishi K., Nakai K., Akira S. The Jmjd3-Irf4 axis regulates M2 macrophage polarization and host responses against helminth infection. Nat. Immunol. 2010, 11:936-944.
44. Banerjee S., Xie N., Cui H., Tan Z., Yang S., Icyuz M., Abraham E., Liu G. MicroRNA let-7c regulates macrophage polarization. J. Immunol. 2013, 190:6542-6549.
45. Diaz-Gandarilla J.A., Osorio-Trujillo C., Hernandez-Ramirez V.I., Talamas-Rohana P. PPAR activation induces M1 macrophage polarization via cPLA(2)-COX-2 inhibition, activating ROS production against Leishmania mexicana. Biomed. Res. Int. 2013, 2013:215283.
46. Hasegawa-Moriyama M., Ohnou T., Godai K., Kurimoto T., Nakama M., Kanmura Y. Peroxisome proliferator-activated receptor-gamma agonist rosiglitazone attenuates postincisional pain by regulating macrophage polarization. Biochem. Biophys. Res. Commun. 2012, 426:76-82.
47. Lawrence T., Natoli G. Transcriptional regulation of macrophage polarization: enabling diversity with identity. Nat. Rev. Immunol. 2011, 11:750-761.
48. Lefevre L., Gales A., Olagnier D., Bernad J., Perez L., Burcelin R., Valentin A., Auwerx J., Pipy B., Coste A. PPARgamma ligands switched high fat diet-induced macrophage M2b polarization toward M2a thereby improving intestinal Candida elimination. PLoS One 2010, 5:e12828.
49. Charo I.F. Macrophage polarization and insulin resistance: PPARgamma in control. Cell Metab. 2007, 6:96-98.
50. Porta C., Rimoldi M., Raes G., Brys L., Ghezzi P., Di Liberto D., Dieli F., Ghisletti S., Natoli G., De Baetselier P., Mantovani A., Sica A. Tolerance and M2 (alternative) macrophage polarization are related processes orchestrated by p50 nuclear factor kappaB. Proc. Natl. Acad. Sci. USA 2009, 106:14978-14983.
51. Han M.S., Jung D.Y., Morel C., Lakhani S.A., Kim J.K., Flavell R.A., Davis R.J. JNK expression by macrophages promotes obesity-induced insulin resistance and inflammation. Science 2013, 339:218-222.
52. Wang Y.C., He F., Feng F., Liu X.W., Dong G.Y., Qin H.Y., Hu X.B., Zheng M.H., Liang L., Feng L., Liang Y.M., Han H. Notch signaling determines the M1 versus M2 polarization of macrophages in antitumor immune responses. Cancer Res. 2010, 70:4840-4849.
53. Satoh T., Kidoya H., Naito H., Yamamoto M., Takemura N., Nakagawa K., Yoshioka Y., Morii E., Takakura N., Takeuchi O., Akira S. Critical role of Trib1 in differentiation of tissue-resident M2-like macrophages. Nature 2013, 495:524-528.
54. Monticelli S., Natoli G. Short-term memory of danger signals and environmental stimuli in immune cells. Nat. Immunol. 2013, 14:777-784.
55. Ishii M., Wen H., Corsa C.A., Liu T., Coelho A.L., Allen R.M., Carson WFt, Cavassani K.A., Li X., Lukacs N.W., Hogaboam C.M., Dou Y., Kunkel S.L. Epigenetic regulation of the alternatively activated macrophage phenotype. Blood 2009, 114:3244-3254.
56. Jung S., Huitinga I., Schmidt B., Zielasek J., Dijkstra C.D., Toyka K.V., Hartung H.P. Selective elimination of macrophages by dichlormethylene diphosphonate-containing liposomes suppresses experimental autoimmune neuritis. J. Neurol. Sci. 1993, 119:195-202.
57. Hikawa N., Takenaka T. Myelin-stimulated macrophages release neurotrophic factors for adult dorsal root ganglion neurons in culture. Cell. Mol. Neurobiol. 1996, 16:517-528.
58. Rapalino O., Lazarov-Spiegler O., Agranov E., Velan G.J., Yoles E., Fraidakis M., Solomon A., Gepstein R., Katz A., Belkin M., Hadani M., Schwartz M. Implantation of stimulated homologous macrophages results in partial recovery of paraplegic rats. Nat. Med. 1998, 4:814-821.
59. Luk H.W., Noble L.J., Werb Z. Macrophages contribute to the maintenance of stable regenerating neurites following peripheral nerve injury. J. Neurosci. Res. 2003, 73:644-658.
60. Shiratori Y., Hongo S., Hikiba Y., Ohmura K., Nagura T., Okano K., Kamii K., Tanaka T., Komatsu Y., Ochiai T., Tsubouchi H., Omata M. Role of macrophages in regeneration of liver. Dig. Dis. Sci. 1996, 41:1939-1946.
61. Arnold L., Henry A., Poron F., Baba-Amer Y., van Rooijen N., Plonquet A., Gherardi R.K., Chazaud B. Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis. J. Exp. Med. 2007, 204:1057-1069.
62. McLoughlin R.M., Witowski J., Robson R.L., Wilkinson T.S., Hurst S.M., Williams A.S., Williams J.D., Rose-John S., Jones S.A., Topley N. Interplay between IFN-gamma and IL-6 signaling governs neutrophil trafficking and apoptosis during acute inflammation. J. Clin. Invest. 2003, 112:598-607.
63. Hurst S.M., Wilkinson T.S., McLoughlin R.M., Jones S., Horiuchi S., Yamamoto N., Rose-John S., Fuller G.M., Topley N., Jones S.A. Il-6 and its soluble receptor orchestrate a temporal switch in the pattern of leukocyte recruitment seen during acute inflammation. Immunity 2001, 14:705-714.
64. Serhan C.N. Pro-resolving lipid mediators are leads for resolution physiology. Nature 2014, 510:92-101.
65. Levy B.D., Clish C.B., Schmidt B., Gronert K., Serhan C.N. Lipid mediator class switching during acute inflammation: signals in resolution. Nat. Immunol. 2001, 2:612-619.
66. Papayianni A., Serhan C.N., Brady H.R. Lipoxin A4 and B4 inhibit leukotriene-stimulated interactions of human neutrophils and endothelial cells. J. Immunol. 1996, 156:2264-2272.
67. Vanden Berghe T., Linkermann A., Jouan-Lanhouet S., Walczak H., Vandenabeele P. Regulated necrosis: the expanding network of non-apoptotic cell death pathways. Nat. Rev. Mol. Cell. Biol. 2014, 15:135-147.
68. Remijsen Q., Kuijpers T.W., Wirawan E., Lippens S., Vandenabeele P., Vanden Berghe T. Dying for a cause: NETosis, mechanisms behind an antimicrobial cell death modality. Cell Death Differ. 2011, 18:581-588.
69. Heasman S.J., Giles K.M., Ward C., Rossi A.G., Haslett C., Dransfield I. Glucocorticoid-mediated regulation of granulocyte apoptosis and macrophage phagocytosis of apoptotic cells: implications for the resolution of inflammation. J. Endocrinol. 2003, 178:29-36.
70. Shao W.H., Cohen P.L. Disturbances of apoptotic cell clearance in systemic lupus erythematosus. Arthritis Res. Ther. 2011, 13:202.
71. Brown J.R., Goldblatt D., Buddle J., Morton L., Thrasher A.J. Diminished production of anti-inflammatory mediators during neutrophil apoptosis and macrophage phagocytosis in chronic granulomatous disease (CGD). J. Leukoc. Biol. 2003, 73:591-599.
72. Savill J. Apoptosis in resolution of inflammation. J. Leukoc. Biol. 1997, 61:375-380.
73. Elliott M.R., Chekeni F.B., Trampont P.C., Lazarowski E.R., Kadl A., Walk S.F., Park D., Woodson R.I., Ostankovich M., Sharma P., Lysiak J.J., Harden T.K., Leitinger N., Ravichandran K.S. Nucleotides released by apoptotic cells act as a find-me signal to promote phagocytic clearance. Nature 2009, 461:282-286.
74. Lauber K., Bohn E., Krober S.M., Xiao Y.J., Blumenthal S.G., Lindemann R.K., Marini P., Wiedig C., Zobywalski A., Baksh S., Xu Y., Autenrieth I.B., Schulze-Osthoff K., Belka C., Stuhler G., Wesselborg S. Apoptotic cells induce migration of phagocytes via caspase-3-mediated release of a lipid attraction signal. Cell 2003, 113:717-730.
75. Gude D.R., Alvarez S.E., Paugh S.W., Mitra P., Yu J., Griffiths R., Barbour S.E., Milstien S., Spiegel S. Apoptosis induces expression of sphingosine kinase 1 to release sphingosine-1-phosphate as a "come-and-get-me" signal. FASEB J. 2008, 22:2629-2638.
76. Knies U.E., Behrensdorf H.A., Mitchell C.A., Deutsch U., Risau W., Drexler H.C., Clauss M. Regulation of endothelial monocyte-activating polypeptide II release by apoptosis. Proc. Natl. Acad. Sci. USA 1998, 95:12322-12327.
77. Horino K., Nishiura H., Ohsako T., Shibuya Y., Hiraoka T., Kitamura N., Yamamoto T. A monocyte chemotactic factor S19 ribosomal protein dimer, in phagocytic clearance of apoptotic cells. Lab. Invest. 1998, 78:603-617.
78. Savill J., Hogg N., Ren Y., Haslett C. Thrombospondin cooperates with CD36 and the vitronectin receptor in macrophage recognition of neutrophils undergoing apoptosis. J. Clin. Invest. 1992, 90:1513-1522.
79. Schwab J.M., Chiang N., Arita M., Serhan C.N. Resolvin E1 and protectin D1 activate inflammation-resolution programmes. Nature 2007, 447:869-874.
80. Bournazou I., Mackenzie K.J., Duffin R., Rossi A.G., Gregory C.D. Inhibition of eosinophil migration by lactoferrin. Immunol. Cell Biol. 2010, 88:220-223.
81. Bournazou I., Pound J.D., Duffin R., Bournazos S., Melville L.A., Brown S.B., Rossi A.G., Gregory C.D. Apoptotic human cells inhibit migration of granulocytes via release of lactoferrin. J. Clin. Invest. 2009, 119:20-32.
82. Vago J.P., Nogueira C.R., Tavares L.P., Soriani F.M., Lopes F., Russo R.C., Pinho V., Teixeira M.M., Sousa L.P. Annexin A1 modulates natural and glucocorticoid-induced resolution of inflammation by enhancing neutrophil apoptosis. J. Leukoc. Biol. 2012, 92:249-258.
83. Brown S., Heinisch I., Ross E., Shaw K., Buckley C.D., Savill J. Apoptosis disables CD31-mediated cell detachment from phagocytes promoting binding and engulfment. Nature 2002, 418:200-203.
84. Gardai S.J., McPhillips K.A., Frasch S.C., Janssen W.J., Starefeldt A., Murphy-Ullrich J.E., Bratton D.L., Oldenborg P.A., Michalak M., Henson P.M. Cell-surface calreticulin initiates clearance of viable or apoptotic cells through trans-activation of LRP on the phagocyte. Cell 2005, 123:321-334.
85. Fadok V.A., Bratton D.L., Henson P.M. Phagocyte receptors for apoptotic cells: recognition, uptake, and consequences. J. Clin. Invest. 2001, 108:957-962.
86. Gregory C.D., Pound J.D. Microenvironmental influences of apoptosis in vivo and in vitro. Apoptosis 2010, 15:1029-1049.
87. Park D., Tosello-Trampont A.C., Elliott M.R., Lu M., Haney L.B., Ma Z., Klibanov A.L., Mandell J.W., Ravichandran K.S. BAI1 is an engulfment receptor for apoptotic cells upstream of the ELMO/Dock180/Rac module. Nature 2007, 450:430-434.
88. Devitt A., Moffatt O.D., Raykundalia C., Capra J.D., Simmons D.L., Gregory C.D. Human CD14 mediates recognition and phagocytosis of apoptotic cells. Nature 1998, 392:505-509.
89. Fadok V.A., Henson P.M., Apoptosis: giving phosphatidylserine recognition an assist--with a twist. Curr. Biol. 2003, 13:R655-R657.
90. Bystrom J., Evans I., Newson J., Stables M., Toor I., van Rooijen N., Crawford M., Colville-Nash P., Farrow S., Gilroy D.W. Resolution-phase macrophages possess a unique inflammatory phenotype that is controlled by cAMP. Blood 2008, 112:4117-4127.
91. Bystrom J., Wynn T.A., Domachowske J.B., Rosenberg H.F. Gene microarray analysis reveals interleukin-5-dependent transcriptional targets in mouse bone marrow. Blood 2004, 103:868-877.
92. Bellingan G.J., Xu P., Cooksley H., Cauldwell H., Shock A., Bottoms S., Haslett C., Mutsaers S.E., Laurent G.J. Adhesion molecule-dependent mechanisms regulate the rate of macrophage clearance during the resolution of peritoneal inflammation. J. Exp. Med. 2002, 196:1515-1521.
93. Ariel A., Serhan C.N. New lives given by cell death: macrophage differentiation following their encounter with apoptotic leukocytes during the resolution of inflammation. Front. Immunol. 2012, 3:4.
94. Newson J., Stables M., Karra E., Arce-Vargas F., Quezada S., Motwani M., Mack M., Yona S., Audzevich T., Gilroy D.W. Resolution of acute inflammation bridges the gap between innate and adaptive immunity. Blood 2014, 124:1748-1764.
95. Schif-Zuck S., Gross N., Assi S., Rostoker R., Serhan C.N., Ariel A. Saturated-efferocytosis generates pro-resolving CD11b low macrophages: modulation by resolvins and glucocorticoids. Eur. J. Immunol. 2011, 41:366-379.
96. Fadok V.A., Warner M.L., Bratton D.L., Henson P.M. CD36 is required for phagocytosis of apoptotic cells by human macrophages that use either a phosphatidylserine receptor or the vitronectin receptor (alpha v beta 3). J. Immunol. 1998, 161:6250-6257.
97. Fadok V.A., Henson P.M., Apoptosis: getting rid of the bodies. Curr. Biol. 1998, 8:R693-R695.
98. Fadok V.A., Bratton D.L., Konowal A., Freed P.W., Westcott J.Y., Henson P.M. Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-beta PGE2, and PAF. J. Clin. Invest. 1998, 101:890-898.
99. Serhan C.N., Dalli J., Karamnov S., Choi A., Park C.K., Xu Z.Z., Ji R.R., Zhu M., Petasis N.A. Macrophage proresolving mediator maresin 1 stimulates tissue regeneration and controls pain. FASEB J. 2012, 26:1755-1765.
100. McCutcheon J.C., Hart S.P., Canning M., Ross K., Humphries M.J., Dransfield I. Regulation of macrophage phagocytosis of apoptotic neutrophils by adhesion to fibronectin. J. Leukoc. Biol. 1998, 64:600-607.
101. Godson C., Mitchell S., Harvey K., Petasis N.A., Hogg N., Brady H.R. Cutting edge: lipoxins rapidly stimulate nonphlogistic phagocytosis of apoptotic neutrophils by monocyte-derived macrophages. J. Immunol. 2000, 164:1663-1667.
102. Giles K.M., Ross K., Rossi A.G., Hotchin N.A., Haslett C., Dransfield I. Glucocorticoid augmentation of macrophage capacity for phagocytosis of apoptotic cells is associated with reduced p130Cas expression, loss of paxillin/pyk2 phosphorylation, and high levels of active Rac. J. Immunol. 2001, 167:976-986.
103. Philippidis P., Mason J.C., Evans B.J., Nadra I., Taylor K.M., Haskard D.O., Landis R.C. Hemoglobin scavenger receptor CD163 mediates interleukin-10 release and heme oxygenase-1 synthesis: antiinflammatory monocyte-macrophage responses in vitro, in resolving skin blisters in vivo, and after cardiopulmonary bypass surgery. Circ. Res. 2004, 94:119-126.
104. Willis D., Moore A.R., Frederick R., Willoughby D.A. Heme oxygenase: a novel target for the modulation of the inflammatory response. Nat. Med. 1996, 2:87-90.
105. Koedel U., Frankenberg T., Kirschnek S., Obermaier B., Hacker H., Paul R., Hacker G. Apoptosis is essential for neutrophil functional shutdown and determines tissue damage in experimental pneumococcal meningitis. PLoS Pathog 2009, 5:e1000461.
106. Ramachandran P., Pellicoro A., Vernon M.A., Boulter L., Aucott R.L., Ali A., Hartland S.N., Snowdon V.K., Cappon A., Gordon-Walker T.T., Williams M.J., Dunbar D.R., Manning J.R., van Rooijen N., Fallowfield J.A., Forbes S.J., Iredale J.P. Differential Ly-6C expression identifies the recruited macrophage phenotype, which orchestrates the regression of murine liver fibrosis. Proc. Natl. Acad. Sci. USA 2012, 109:E3186-E3195.
107. Buckley C.D., Gilroy D.W., Serhan C.N., Stockinger B., Tak P.P. The resolution of inflammation. Nat. Rev. Immunol. 2013, 13:59-66.
108. Serhan C.N., Brain S.D., Buckley C.D., Gilroy D.W., Haslett C., O'Neill L.A., Perretti M., Rossi A.G., Wallace J.L. Resolution of inflammation: state of the art, definitions and terms. FASEB J. 2007, 21:325-332.
109. Uderhardt S., Herrmann M., Oskolkova O.V., Aschermann S., Bicker W., Ipseiz N., Sarter K., Frey B., Rothe T., Voll R., Nimmerjahn F., Bochkov V.N., Schett G., Kronke G. 12/15-Lipoxygenase orchestrates the clearance of apoptotic cells and maintains immunologic tolerance. Immunity 2012.
110. Newson J., Stables M., Karra E., Arce-Vargas F., Quezada S., Motwani M., Mack M., Yona S., Audzevich T., Gilroy D.W. Resolution of acute inflammation bridges the gap between innate and adaptive immunity. Blood 2014.
111. van Rijt L.S., Vos N., Willart M., Muskens F., Tak P.P., van der Horst C., Hoogsteden H.C., Lambrecht B.N. Persistent activation of dendritic cells after resolution of allergic airway inflammation breaks tolerance to inhaled allergens in mice. Am. J. Respir. Crit. Care Med. 2011, 184:303-311.
112. Rosas M., Davies L.C., Giles P.J., Liao C.T., Kharfan B., Stone T.C., O'Donnell V.B., Fraser D.J., Jones S.A., Taylor P.R. The transcription factor Gata6 links tissue macrophage phenotype and proliferative renewal. Science 2014, 344:645-648.
113. Okabe Y., Medzhitov R. Tissue-specific signals control reversible program of localization and functional polarization of macrophages. Cell 2014, 157:832-844.
114. Anders H.J., Ryu M. Renal microenvironments and macrophage phenotypes determine progression or resolution of renal inflammation and fibrosis. Kidney Int. 2011, 80:915-925.
115. Tani Y., Isobe Y., Imoto Y., Segi-Nishida E., Arai H., Arita M. Eosinophils control the resolution of inflammation and draining lymph node hypertrophy through the proresolving mediators and CXCL13 pathway in mice. FASEB J. 2014, 28(September (9)):4036-4043.
116. Yamada T., Tani Y., Nakanishi H., Taguchi R., Arita M., Arai H. Eosinophils promote resolution of acute peritonitis by producing proresolving mediators in mice. FASEB J. 2011, 25:561-568.
117. Jenner W., Motwani M., Veighey K., Newson J., Audzevich T., Nicolaou A., Murphy S., Macallister R., Gilroy D.W. Characterisation of leukocytes in a human skin blister model of acute inflammation and resolution. PloS One 2014, 9:e89375.
118. Fang Y., Chen K., Jackson D.A., Sharp G.C., Braley-Mullen H. Eosinophils infiltrate thyroids, but have no apparent role in induction or resolution of experimental autoimmune thyroiditis in interferon-gamma(-/-) mice. Immunology 2010, 129:329-337.
119. Fingerle G., Pforte A., Passlick B., Blumenstein M., Strobel M., Ziegler-Heitbrock H.W. The novel subset of CD14+/CD16+ blood monocytes is expanded in sepsis patients. Blood 1993, 82:3170-3176.
120. Blumenstein M., Boekstegers P., Fraunberger P., Andreesen R., Ziegler-Heitbrock H.W., Fingerle-Rowson G. Cytokine production precedes the expansion of CD14+CD16+ monocytes in human sepsis: a case report of a patient with self-induced septicemia. Shock 1997, 8:73-75.
121. Tang B.M., Huang S.J., McLean A.S. Genome-wide transcription profiling of human sepsis: a systematic review. Crit. Care 2010, 14:R237.
122. Xiao W., Mindrinos M.N., Seok J., Cuschieri J., Cuenca A.G., Gao H., Hayden D.L., Hennessy L., Moore E.E., Minei J.P., Bankey P.E., Johnson J.L., Sperry J., Nathens A.B., Billiar T.R., West M.A., Brownstein B.H., Mason P.H., Baker H.V., Finnerty C.C., Jeschke M.G., Lopez M.C., Klein M.B., Gamelli R.L., Gibran N.S., Arnoldo B., Xu W., Zhang Y., Calvano S.E., McDonald-Smith G.P., Schoenfeld D.A., Storey J.D., Cobb J.P., Warren H.S., Moldawer L.L., Herndon D.N., Lowry S.F., Maier R.V., Davis R.W., Tompkins R.G. A genomic storm in critically injured humans. J. Exp. Med. 2011, 208:2581-2590.
123. Tang B.M., McLean A.S., Dawes I.W., Huang S.J., Cowley M.J., Lin R.C. Gene-expression profiling of gram-positive and gram-negative sepsis in critically ill patients. Crit. Care Med. 2008, 36:1125-1128.
124. Shalova I.N., Lim J.Y., Chittezhath M., Zinkernagel A.S., Beasley F., Hernandez-Jimenez E., Toledano V., Cubillos-Zapata C., Rapisarda A., Chen J., Duan K., Yang H., Poidinger M., Melillo G., Nizet V., Arnalich F., Lopez-Collazo E., Biswas S.K. Human monocytes undergo functional re-programming during sepsis mediated by hypoxia-inducible factor-1alpha. Immunity 2015, 42:484-498.
125. Kawanaka N., Yamamura M., Aita T., Morita Y., Okamoto A., Kawashima M., Iwahashi M., Ueno A., Ohmoto Y., Makino H. CD14+ CD16+ blood monocytes and joint inflammation in rheumatoid arthritis. Arthritis Rheum. 2002, 46:2578-2586.
126. Hepburn A.L., Mason J.C., Davies K.A. Expression of Fcgamma and complement receptors on peripheral blood monocytes in systemic lupus erythematosus and rheumatoid arthritis. Rheumatology (Oxford) 2004, 43:547-554.
127. Wijngaarden S., van Roon J.A., Bijlsma J.W., van de Winkel J.G., Lafeber F.P. Fcgamma receptor expression levels on monocytes are elevated in rheumatoid arthritis patients with high erythrocyte sedimentation rate who do not use anti-rheumatic drugs. Rheumatology (Oxford) 2003, 42:681-688.
128. Fingerle-Rowson G., Angstwurm M., Andreesen R., Ziegler-Heitbrock H.W. Selective depletion of CD14+ CD16+ monocytes by glucocorticoid therapy. Clin. Exp. Immunol. 1998, 112:501-506.
129. Dayyani F., Belge K.U., Frankenberger M., Mack M., Berki T., Ziegler-Heitbrock L. Mechanism of glucocorticoid-induced depletion of human CD14+CD16+ monocytes. J. Leukoc. Biol. 2003, 74:33-39.
130. Cairns A.P., Crockard A.D., Bell A.L. The CD14+ CD16+ monocyte subset in rheumatoid arthritis and systemic lupus erythematosus. Rheumatol. Int. 2002, 21:189-192.
131. Bruhl H., Cihak J., Plachy J., Kunz-Schughart L., Niedermeier M., Denzel A., Rodriguez Gomez M., Talke Y., Luckow B., Stangassinger M., Mack M. Targeting of Gr-1+ CCR2+ monocytes in collagen-induced arthritis. Arthritis Rheum. 2007, 56:2975-2985.
132. Weber C., Zernecke A., Libby P. The multifaceted contributions of leukocyte subsets to atherosclerosis: lessons from mouse models. Nat. Rev. Immunol. 2008, 8:802-815.
133. Moore K.J., Tabas I. Macrophages in the pathogenesis of atherosclerosis. Cell 2011, 145:341-355.
134. Zernecke A., Shagdarsuren E., Weber C. Chemokines in atherosclerosis: an update. Arterioscler. Thromb. Vasc. Biol. 2008, 28:1897-1908.
135. Stoger J.L., Gijbels M.J., van der Velden S., Manca M., van der Loos C.M., Biessen E.A., Daemen M.J., Lutgens E., de Winther M.P. Distribution of macrophage polarization markers in human atherosclerosis. Atherosclerosis 2012, 225:461-468.
136. Hakkinen T., Karkola K., Yla-Herttuala S. Macrophages, smooth muscle cells, endothelial cells, and T-cells express CD40 and CD40L in fatty streaks and more advanced human atherosclerotic lesions. Colocalization with epitopes of oxidized low-density lipoprotein, scavenger receptor, and CD16 (Fc gammaRIII). Virchows Arch. 2000, 437:396-405.
137. Rothe G., Gabriel H., Kovacs E., Klucken J., Stohr J., Kindermann W., Schmitz G. Peripheral blood mononuclear phagocyte subpopulations as cellular markers in hypercholesterolemia. Arterioscler. Thromb. Vasc. Biol. 1996, 16:1437-1447.
138. Schlitt A., Heine G.H., Blankenberg S., Espinola-Klein C., Dopheide J.F., Bickel C., Lackner K.J., Iz M., Meyer J., Darius H., Rupprecht H.J. CD14+CD16+ monocytes in coronary artery disease and their relationship to serum TNF-alpha levels. Thromb. Haemost. 2004, 92:419-424.
139. Llodra J., Angeli V., Liu J., Trogan E., Fisher E.A., Randolph G.J. Emigration of monocyte-derived cells from atherosclerotic lesions characterizes regressive, but not progressive, plaques. Proc. Natl. Acad. Sci. USA 2004, 101:11779-11784.
140. Fadini G.P., Simoni F., Cappellari R., Vitturi N., Galasso S., Vigili de Kreutzenberg S., Previato L., Avogaro A. Pro-inflammatory monocyte-macrophage polarization imbalance in human hypercholesterolemia and atherosclerosis. Atherosclerosis 2014, 237:805-808.
141. Nikolic T., Bouma G., Drexhage H.A., Leenen P.J., Diabetes-prone N.O.D. mice show an expanded subpopulation of mature circulating monocytes, which preferentially develop into macrophage-like cells in vitro. J. Leukoc. Biol. 2005, 78:70-79.
142. Bouma G., Lam-Tse W.K., Wierenga-Wolf A.F., Drexhage H.A., Versnel M.A. Increased serum levels of MRP-8/14 in type 1 diabetes induce an increased expression of CD11b and an enhanced adhesion of circulating monocytes to fibronectin. Diabetes 2004, 53:1979-1986.
143. Patino R., Ibarra J., Rodriguez A., Yague M.R., Pintor E., Fernandez-Cruz A., Figueredo A. Circulating monocytes in patients with diabetes mellitus, arterial disease, and increased CD14 expression. Am. J. Cardiol. 2000, 85:1288-1291.
144. Mizuno K., Toma T., Tsukiji H., Okamoto H., Yamazaki H., Ohta K., Ohta K., Kasahara Y., Koizumi S., Yachie A. Selective expansion of CD16highCCR2- subpopulation of circulating monocytes with preferential production of haem oxygenase (HO)-1 in response to acute inflammation. Clin. Exp. Immunol. 2005, 142:461-470.
145. Nakatani K., Takeshita S., Tsujimoto H., Kawamura Y., Kawase H., Sekine I. Regulation of the expression of Fc gamma receptor on circulating neutrophils and monocytes in Kawasaki disease. Clin. Exp. Immunol. 1999, 117:418-422.
146. Katayama K., Matsubara T., Fujiwara M., Koga M., Furukawa S. CD14+CD16+ monocyte subpopulation in Kawasaki disease. Clin. Exp. Immunol. 2000, 121:566-570.
147. Jin F., Balthasar J.P. Mechanisms of intravenous immunoglobulin action in immune thrombocytopenic purpura. Hum. Immunol. 2005, 66:403-410.
148. Emminger W., Zlabinger G.J., Fritsch G., Urbanek R. CD14(dim)/CD16(bright) monocytes in hemophagocytic lymphohistiocytosis. Eur. J. Immunol. 2001, 31:1716-1719.
149. Rivier A., Pene J., Rabesandratana H., Chanez P., Bousquet J., Campbell A.M. Blood monocytes of untreated asthmatics exhibit some features of tissue macrophages. Clin. Exp. Immunol. 1995, 100:314-318.
150. Okamoto H., Mizuno K., Horio T. Circulating CD14+ CD16+ monocytes are expanded in sarcoidosis patients. J. Dermatol. 2003, 30:503-509.
151. Nagasawa T., Kobayashi H., Aramaki M., Kiji M., Oda S., Izumi Y. Expression of CD14 CD16 and CD45RA on monocytes from periodontitis patients. J. Periodontal. Res. 2004, 39:72-78.
152. Novak N., Allam P., Geiger E., Bieber T. Characterization of monocyte subtypes in the allergic form of atopic eczema/dermatitis syndrome. Allergy 2002, 57:931-935.
153. Rahman S.H., Salter G., Holmfield J.H., Larvin M., McMahon M.J. Soluble CD14 receptor expression and monocyte heterogeneity but not the C-260T CD14 genotype are associated with severe acute pancreatitis. Crit. Care Med. 2004, 32:2457-2463.
154. Yoshioka Y., Ohwada A., Harada N., Satoh N., Sakuraba S., Dambara T., Fukuchi Y. Increased circulating CD16+ CD14dim monocytes in a patient with pulmonary alveolar proteinosis. Respirology 2002, 7:273-279.
155. Scherberich J.E., Estner H., Segerer W. Impact of different immunosuppressive regimens on antigen-presenting blood cells in kidney transplant patients. Kidney Blood Press Res. 2004, 27:177-180.
156. Brauner A., Lu Y., Hallden G., Hylander B., Lundahl J. Difference in the blood monocyte phenotype between uremic patients and healthy controls: its relation to monocyte differentiation into macrophages in the peritoneal cavity. Inflammation 1998, 22:55-66.
157. Cottam D.R., Gorecki P.J., Curvelo M., Weltman D., Angus L.D., Shaftan G. Preperitoneal herniation into a laparoscopic port site without a fascial defect. Obes. Surg. 2002, 12:121-123.
158. Tidball J.G., Villalta S.A. Regulatory interactions between muscle and the immune system during muscle regeneration. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2010, 298:R1173-R1187.
159. Zhang L., Ran L., Garcia G.E., Wang X.H., Han S., Du J., Mitch W.E. Chemokine CXCL16 regulates neutrophil and macrophage infiltration into injured muscle, promoting muscle regeneration. Am. J. Pathol. 2009, 175:2518-2527.
160. Marino J.S., Tausch B.J., Dearth C.L., Manacci M.V., McLoughlin T.J., Rakyta S.J., Linsenmayer M.P., Pizza F.X. Beta2-integrins contribute to skeletal muscle hypertrophy in mice. Am. J. Physiol. Cell Physiol. 2008, 295:C1026-C1036.
161. Liu H., Niu A., Chen S.E., Li Y.P. Beta3-integrin mediates satellite cell differentiation in regenerating mouse muscle. FASEB J. 2011, 25:1914-1921.
162. Mayer U., Saher G., Fassler R., Bornemann A., Echtermeyer F., von der Mark H., Miosge N., Poschl E., von der Mark K. Absence of integrin alpha 7 causes a novel form of muscular dystrophy. Nat. Genet. 1997, 17:318-323.
163. Vidal B., Serrano A.L., Tjwa M., Suelves M., Ardite E., De Mori R., Baeza-Raja B., Martinez de Lagran M., Lafuste P., Ruiz-Bonilla V., Jardi M., Gherardi R., Christov C., Dierssen M., Carmeliet P., Degen J.L., Dewerchin M., Munoz-Canoves P. Fibrinogen drives dystrophic muscle fibrosis via a TGFbeta/alternative macrophage activation pathway. Genes Dev. 2008, 22:1747-1752.
164. Wynn T.A. Cellular and molecular mechanisms of fibrosis. J. Pathol. 2008, 214:199-210.
165. Desguerre I., Mayer M., Leturcq F., Barbet J.P., Gherardi R.K., Christov C. Endomysial fibrosis in Duchenne muscular dystrophy: a marker of poor outcome associated with macrophage alternative activation. J. Neuropathol. Exp. Neurol. 2009, 68:762-773.
166. Gray M., Palispis W., Popovich P.G., van Rooijen N., Gupta R. Macrophage depletion alters the blood-nerve barrier without affecting Schwann cell function after neural injury. J. Neurosci. Res. 2007, 85:766-777.
167. Laskin D.L., Laskin J.D. Role of macrophages and inflammatory mediators in chemically induced toxicity. Toxicology 2001, 160:111-118.
168. Craggs R.I., King R.H., Thomas P.K. The effect of suppression of macrophage activity on the development of experimental allergic neuritis. Acta Neuropathol. 1984, 62:316-323.
169. Bruck W., Bruck Y., Diederich U., Friede R.L. Dorsal root ganglia cocultured with macrophages: an in vitro model to study experimental demyelination. Acta Neuropathol. 1994, 88:459-464.
170. Duffield J.S., Forbes S.J., Constandinou C.M., Clay S., Partolina M., Vuthoori S., Wu S., Lang R., Iredale J.P. Selective depletion of macrophages reveals distinct, opposing roles during liver injury and repair. J. Clin. Invest. 2005, 115:56-65.