Gene expression during the generation and activation of mouse neutrophils: Implication of novel functional and regulatory pathways

PLoS ONE

Volumn 9, Issue 10, 2014, Pages

  Ericson, Jeffrey A ^a   Duffau, Pierre ^b   Yasuda, Kei ^b   Ortiz Lopez, Adriana ^a   Rothamel, Katherine ^a   Rifkin, Ian R ^b   Monach, Paul A ^b   Best, Adam J ^c   Knell, Jamie ^c   Goldrath, Ananda ^c   Jojic, Vladimir ^d   Koller, Daphne ^d   Shay, Tal ^e   Regev, Aviv ^e   Cohen, Nadia ^f   Brennan, Patrick ^f   Brenner, Michael ^f   Kim, Francis ^g   Rao, Tata Nageswara ^g   Wagers, Amy ^g   Heng, Tracy ^a   Mathis, Diane ^a   Benoist, Christophe ^a   Bezman, Natalie A ^h   Sun, Joseph C ^h   Min Oo, Gundula ^h   Kim, Charlie C ^h   Lanier, Lewis L ^h   Miller, Jennifer ⁱ   Brown, Brian ⁱ   Merad, Miriam ⁱ   Gautier, Emmanuel L ^i,j   Jakubzick, Claudia ⁱ   Randolph, Gwendalyn J ^i,j   Blair, David A ^k   Dustin, Michael L ^k   Shinton, Susan A ^l   Hardy, Richard R ^l   Laidlaw, David ^m   Collins, Jim ⁿ   Gazit, Roi ^o   Rossi, Derrick J ^o   Malhotra, Nidhi ^p   Sylvia, Katelyn ^p   Kang, Joonsoo ^p   Kreslavsky, Taras ^a   Fletcher, Anne ^a   Elpek, Kutlu ^a   Bellemare Pelletier, Angelique ^a   Malhotra, Deepali ^a   Turley, Shannon ^a   more..

^a HARVARD MEDICAL SCHOOL   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^d Stanford University   (United States)

^e BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^f BRIGHAM AND WOMEN S HOSPITAL   (United States)

^g JOSLIN DIABETES CENTER   (United States)

^h UNIVERSITY OF CALIFORNIA   (United States)

ⁱ MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^j WASHINGTON UNIVERSITY   (United States)

^k NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^l FOX CHASE CANCER CENTER   (United States)

^m Brown Univerity   (United States)

ⁿ Boston University   (United States)

^o BOSTON CHILDREN S HOSPITAL   (United States)

^p UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON INDUCIBLE PROTEIN 10; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; LEUKOTRIENE; LIPOPROTEIN; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PROSTAGLANDIN; THIOGLYCOLIC ACID; TOLL LIKE RECEPTOR 9; TUMOR NECROSIS FACTOR ALPHA; URIC ACID; CYTOKINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTHRITIS; ARTICLE; CELL POPULATION; CONTROLLED STUDY; CYTOKINE RELEASE; DOWN REGULATION; EXPERIMENTAL PERITONITIS; GENE; GENE EXPRESSION; GENE IDENTIFICATION; IN VITRO STUDY; IN VIVO STUDY; IRF5 GENE; LEUKOCYTE ACTIVATION; MALE; MOUSE; MRGPR2A GENE; MRGPR2B GENE; NF KAPPA B GENE; NONHUMAN; PROTEIN METABOLISM; RNA TRANSLATION; STFA2L1 GENE; THIOGLYCOLATE-INDUCED PERITONITIS; UPREGULATION; ANIMAL; GENETICS; METABOLISM; NEUTROPHIL; TRANSCRIPTION INITIATION;

ANIMALS; CYTOKINES; GENE EXPRESSION; MICE; NEUTROPHIL ACTIVATION; NEUTROPHILS; TRANSCRIPTIONAL ACTIVATION; UP-REGULATION;

EID: 84940988389     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0108553     Document Type: Article

References (92)

1. Heng TS, Painter MW (2008) The Immunological Genome Project: networks of gene expression in immune cells. Nat Immunol 9: 1091-1094.
2. Narayan K, Sylvia KE, Malhotra N, Yin CC, Martens G, et al. (2012) Intrathymic programming of effector fates in three molecularly distinct gammadelta T cell subtypes. Nat Immunol 13: 511-518.
3. Malhotra D, Fletcher AL, Astarita J, Lukacs-Kornek V, Tayalia P, et al. (2012) Transcriptional profiling of stroma from inflamed and resting lymph nodes defines immunological hallmarks. Nat Immunol 13: 499-510.
4. Miller JC, Brown BD, Shay T, Gautier EL, Jojic V, et al. (2012) Deciphering the transcriptional network of the dendritic cell lineage. Nat Immunol 13: 888-899.
5. Bezman NA, Kim CC, Sun JC, Min-Oo G, Hendricks DW, et al. (2012) Molecular definition of the identity and activation of natural killer cells. Nat Immunol 13: 1000-1009.
6. Gautier EL, Shay T, Miller J, Greter M, Jakubzick C, et al. (2012) Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nat Immunol 13: 1118-1128.
7. Cohen NR, Brennan PJ, Shay T, Watts GF, Brigl M, et al. (2013) Shared and distinct transcriptional programs underlie the hybrid nature of iNKT cells. Nat Immunol 14: 90-99.
8. Best JA, Blair DA, Knell J, Yang E, Mayya V, et al. (2013) Transcriptional insights into the CD8(+) T cell response to infection and memory T cell formation. Nat Immunol 14: 404-412.
9. Malhotra N, Narayan K, Cho OH, Sylvia KE, Yin C, et al. (2013) A network of high-mobility group box transcription factors programs innate interleukin-17 production. Immunity 38: 681-693.
10. Jojic V, Shay T, Sylvia K, Zuk O, Sun X, et al. (2013) Identification of transcriptional regulators in the mouse immune system. Nat Immunol 14: 633-643.
11. Mingueneau M, Kreslavsky T, Gray D, Heng T, Cruse R, et al. (2013) The transcriptional landscape of alphabeta T cell differentiation. Nat Immunol 14: 619-632.
12. Jack RM, Fearon DT (1988) Selective synthesis of mRNA and proteins by human peripheral blood neutrophils. J Immunol 140: 4286-4293.
13. Cassatella MA (1999) Neutrophil-derived proteins: selling cytokines by the pound. Adv Immunol 73: 369-509.
14. Mantovani A, Cassatella MA, Costantini C, Jaillon S (2011) Neutrophils in the activation and regulation of innate and adaptive immunity. Nat Rev Immunol 11: 519-531.
15. Wright HL, Moots RJ, Bucknall RC, Edwards SW (2010) Neutrophil function in inflammation and inflammatory diseases. Rheumatology (Oxford) 49: 1618-1631.
16. Jarvis JN, Jiang K, Frank MB, Knowlton N, Aggarwal A, et al. (2009) Gene expression profiling in neutrophils from children with polyarticular juvenile idiopathic arthritis. Arthritis Rheum 60: 1488-1495.
17. Theilgaard-Monch K, Knudsen S, Follin P, Borregaard N (2004) The transcriptional activation program of human neutrophils in skin lesions supports their important role in wound healing. J Immunol 172: 7684-7693.
18. Radom-Aizik S, Zaldivar F Jr., Leu SY, Galassetti P, Cooper DM (2008) Effects of 30 min of aerobic exercise on gene expression in human neutrophils. J Appl Physiol 104: 236-243.
19. Kotz KT, Xiao W, Miller-Graziano C, Qian WJ, Russom A, et al. (2010) Clinical microfluidics for neutrophil genomics and proteomics. Nat Med 16: 1042-1047.
20. Fessler MB, Malcolm KC, Duncan MW, Worthen GS (2002) A genomic and proteomic analysis of activation of the human neutrophil by lipopolysaccharide and its mediation by p38 mitogen-activated protein kinase. J Biol Chem 277: 31291-31302.
21. Malcolm KC, Arndt PG, Manos EJ, Jones DA, Worthen GS (2003) Microarray analysis of lipopolysaccharide-treated human neutrophils. Am J Physiol Lung Cell Mol Physiol 284: L663-670.
22. Zhang X, Kluger Y, Nakayama Y, Poddar R, Whitney C, et al. (2004) Gene expression in mature neutrophils: early responses to inflammatory stimuli. J Leukoc Biol 75: 358-372.
23. Kobayashi SD, Voyich JM, Whitney AR, DeLeo FR (2005) Spontaneous neutrophil apoptosis and regulation of cell survival by granulocyte macrophage-colony stimulating factor. J Leukoc Biol 78: 1408-1418.
24. Subrahmanyam YV, Yamaga S, Prashar Y, Lee HH, Hoe NP, et al. (2001) RNA expression patterns change dramatically in human neutrophils exposed to bacteria. Blood 97: 2457-2468.
25. Sasmono RT, Ehrnsperger A, Cronau SL, Ravasi T, Kandane R, et al. (2007) Mouse neutrophilic granulocytes express mRNA encoding the macrophage colony-stimulating factor receptor (CSF-1R) as well as many other macrophage-specific transcripts and can transdifferentiate into macrophages in vitro in response to CSF-1. J Leukoc Biol 82: 111-123.
26. McDonald PP (2004) Transcriptional regulation in neutrophils: teaching old cells new tricks. Adv Immunol 82: 1-48.
27. Halene S, Gaines P, Sun H, Zibello T, Lin S, et al. (2010) C/EBPepsilon directs granulocytic-vs-monocytic lineage determination and confers chemotactic function via Hlx. Exp Hematol 38: 90-103.
28. Friedman AD (2007) Transcriptional control of granulocyte and monocyte development. Oncogene 26: 6816-6828.
29. Hock H, Hamblen MJ, Rooke HM, Traver D, Bronson RT, et al. (2003) Intrinsic requirement for zinc finger transcription factor Gfi-1 in neutrophil differentiation. Immunity 18: 109-120.
30. McDonald PP, Bald A, Cassatella MA (1997) Activation of the NF-kappaB pathway by inflammatory stimuli in human neutrophils. Blood 89: 3421-3433.
31. Martinon F, Petrilli V, Mayor A, Tardivel A, Tschopp J (2006) Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature 440: 237-241.
32. Matsumoto I, Staub A, Benoist C, Mathis D (1999) Arthritis provoked by linked T and B cell recognition of a glycolytic enzyme. Science 286: 1732-1735.
33. Korganow AS, Ji H, Mangialaio S, Duchatelle V, Pelanda R, et al. (1999) From systemic T cell self-reactivity to organ-specific autoimmune disease via immunoglobulins. Immunity 10: 451-461.
34. Takaoka A, Yanai H, Kondo S, Duncan G, Negishi H, et al. (2005) Integral role of IRF-5 in the gene induction programme activated by Toll-like receptors. Nature 434: 243-249.
35. Itou T, Collins LV, Thoren FB, Dahlgren C, Karlsson A (2006) Changes in activation states of murine polymorphonuclear leukocytes (PMN) during inflammation: a comparison of bone marrow and peritoneal exudate PMN. Clin Vaccine Immunol 13: 575-583.
36. Painter MW, Davis S, Hardy RR, Mathis D, Benoist C, et al. (2011) Transcriptomes of the B and T lineages compared by multiplatform microarray profiling. J Immunol 186: 3047-3057.
37. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Royal Stat Soc B 57: 289-300.
38. Utomo A, Cullere X, Glogauer M, Swat W, Mayadas TN (2006) Vav proteins in neutrophils are required for FcgammaR-mediated signaling to Rac GTPases and nicotinamide adenine dinucleotide phosphate oxidase component p40(phox). J Immunol 177: 6388-6397.
39. Zhang X, Majlessi L, Deriaud E, Leclerc C, Lo-Man R (2009) Coactivation of Syk kinase and MyD88 adaptor protein pathways by bacteria promotes regulatory properties of neutrophils. Immunity 31: 761-771.
40. Wen T, Mingler MK, Blanchard C, Wahl B, Pabst O, et al. (2012) The pan-B cell marker CD22 is expressed on gastrointestinal eosinophils and negatively regulates tissue eosinophilia. J Immunol 188: 1075-1082.
41. Ringsholt M, Hogdall EV, Johansen JS, Price PA, Christensen LH (2007) YKL-40 protein expression in normal adult human tissues-an immunohistochemical study. J Mol Histol 38: 33-43.
42. Aoki N, Kimura Y, Kimura S, Nagato T, Azumi M, et al. (2009) Expression and functional role of MDL-1 (CLEC5A) in mouse myeloid lineage cells. J Leukoc Biol 85: 508-517.
43. Ortiz de Apodaca MA, Fernandez E, de la Fuente G (1992) Tris discriminates between the different alpha-glucosidase activities from extracts of human neutrophils. J Inherit Metab Dis 15: 213-219.
44. Diaz-Sotomayor M, Quezada-Calvillo R, Avery SE, Chacko SK, Yan LK, et al. (2013) Maltase-glucoamylase Modulates Gluconeogenesis; Sucrase-isomaltase Dominates Starch Digestion Glucogenesis. J Pediatr Gastroenterol Nutr 57: 704-712.
45. Qureshi A, Subathra M, Grey A, Schey K, Del Poeta M, et al. (2010) Role of sphingomyelin synthase in controlling the antimicrobial activity of neutrophils against Cryptococcus neoformans. PLoS One 5: e15587.
46. Gowda S, Yeang C, Wadgaonkar S, Anjum F, Grinkina N, et al. (2011) Sphingomyelin synthase 2 (SMS2) deficiency attenuates LPS-induced lung injury. Am J Physiol Lung Cell Mol Physiol 300: L430-440.
47. Hume DA, Summers KM, Raza S, Baillie JK, Freeman TC (2010) Functional clustering and lineage markers: insights into cellular differentiation and gene function from large-scale microarray studies of purified primary cell populations. Genomics 95: 328-338.
48. Theilgaard-Monch K, Jacobsen LC, Borup R, Rasmussen T, Bjerregaard MD, et al. (2005) The transcriptional program of terminal granulocytic differentiation. Blood 105: 1785-1796.
49. Borregaard N (2010) Neutrophils, from marrow to microbes. Immunity 33: 657-670.
50. Amulic B, Cazalet C, Hayes GL, Metzler KD, Zychlinsky A (2012) Neutrophil function: from mechanisms to disease. Annu Rev Immunol 30: 459-489.
51. Mabbott NA, Kenneth Baillie J, Hume DA, Freeman TC (2010) Meta-analysis of lineage-specific gene expression signatures in mouse leukocyte populations. Immunobiology 215: 724-736.
52. Elliott ER, Van Ziffle JA, Scapini P, Sullivan BM, Locksley RM, et al. (2011) Deletion of Syk in neutrophils prevents immune complex arthritis. J Immunol 187: 4319-4330.
53. Bainton DF, Ullyot JL, Farquhar MG (1971) The development of neutrophilic polymorphonuclear leukocytes in human bone marrow. J Exp Med 134: 907-934.
54. McLaren JE, Michael DR, Ashlin TG, Ramji DP (2011) Cytokines, macrophage lipid metabolism and foam cells: implications for cardiovascular disease therapy. Prog Lipid Res 50: 331-347.
55. de Villiers WJ, Smart EJ (1999) Macrophage scavenger receptors and foam cell formation. J Leukoc Biol 66: 740-746.
56. Zhao Y, Bruemmer D (2010) NR4A orphan nuclear receptors: transcriptional regulators of gene expression in metabolism and vascular biology. Arterioscler Thromb Vasc Biol 30: 1535-1541.
57. Maxwell MA, Muscat GE (2006) The NR4A subgroup: immediate early response genes with pleiotropic physiological roles. Nucl Recept Signal 4: e002.
58. Pei L, Castrillo A, Chen M, Hoffmann A, Tontonoz P (2005) Induction of NR4A orphan nuclear receptor expression in macrophages in response to inflammatory stimuli. J Biol Chem 280: 29256-29262.
59. Lundequist A, Calounova G, Wensman H, Ronnberg E, Pejler G (2011) Differential regulation of Nr4a subfamily nuclear receptors following mast cell activation. Mol Immunol 48: 1753-1761.
60. Griffith OW (1999) Biologic and pharmacologic regulation of mammalian glutathione synthesis. Free Radic Biol Med 27: 922-935.
61. Borgeat P (1989) Biochemistry of the lipoxygenase pathways in neutrophils. Can J Physiol Pharmacol 67: 936-942.
62. Baehner RL, Boxer LA (1979) Role of membrane vitamin E and cytoplasmic glutathione in the regulation of phagocytic functions of neutrophils and monocytes. Am J Pediatr Hematol Oncol 1: 71-76.
63. Gilbert C, Poubelle PE, Borgeat P, Pouliot M, Naccache PH (2003) Crystal-induced neutrophil activation: VIII. Immediate production of prostaglandin E2 mediated by constitutive cyclooxygenase 2 in human neutrophils stimulated by urate crystals. Arthritis Rheum 48: 1137-1148.
64. Serhan CN, Lundberg U, Weissmann G, Samuelsson B (1984) Formation of leukotrienes and hydroxy acids by human neutrophils and platelets exposed to monosodium urate. Prostaglandins 27: 563-581.
65. Weissmann G, Serhan C, Korchak HM, Smolen JE (1984) Mechanisms of mediator release from neutrophils. Adv Exp Med Biol 172: 527-552.
66. Coffey MJ, Phare SM, Peters-Golden M (2004) Role of leukotrienes in killing of Mycobacterium bovis by neutrophils. Prostaglandins Leukot Essent Fatty Acids 71: 185-190.
67. Kim JS, Kim JM, Jung HC, Song IS (2001) Expression of cyclooxygenase-2 in human neutrophils activated by Helicobacter pylori water-soluble proteins: possible involvement of NF-kappaB and MAP kinase signaling pathway. Dig Dis Sci 46: 2277-2284.
68. Chen M, Boilard E, Nigrovic PA, Clark P, Xu D, et al. (2008) Predominance of cyclooxygenase 1 over cyclooxygenase 2 in the generation of proinflammatory prostaglandins in autoantibody-driven K/BxN serum-transfer arthritis. Arthritis Rheum 58: 1354-1365.
69. Abi Abdallah DS, Egan CE, Butcher BA, Denkers EY (2011) Mouse neutrophils are professional antigen-presenting cells programmed to instruct Th1 and Th17 T-cell differentiation. Int Immunol 23: 317-326.
70. Luo HR, Loison F (2008) Constitutive neutrophil apoptosis: mechanisms and regulation. Am J Hematol 83: 288-295.
71. Filep JG, El Kebir D (2009) Neutrophil apoptosis: a target for enhancing the resolution of inflammation. J Cell Biochem 108: 1039-1046.
72. Shah D, Sah S, Nath SK (2013) Interaction between glutathione and apoptosis in systemic lupus erythematosus. Autoimmun Rev 12: 741-751.
73. Tansho-Nagakawa S, Ubagai T, Kikuchi-Ueda T, Koshio O, Koshibu Y, et al. (2012) Analysis of membrane antigens on neutrophils from patients with sepsis. J Infect Chemother 18: 646-651.
74. Lindau D, Mussard J, Wagner BJ, Ribon M, Ronnefarth VM, et al. (2013) Primary blood neutrophils express a functional cell surface Toll-like receptor 9. Eur J Immunol 43: 2101-2113.
75. Oh SJ, Kim JH, Chung DH (2013) NOD2-mediated suppression of CD55 on neutrophils enhances C5a generation during polymicrobial sepsis. PLoS Pathog 9: e1003351.
76. Choe JY, Crain B, Wu SR, Corr M (2003) Interleukin 1 receptor dependence of serum transferred arthritis can be circumvented by toll-like receptor 4 signaling. J Exp Med 197: 537-542.
77. Marzluff WF, Gongidi P, Woods KR, Jin J, Maltais LJ (2002) The human and mouse replication-dependent histone genes. Genomics 80: 487-498.
78. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, et al. (2004) Neutrophil extracellular traps kill bacteria. Science 303: 1532-1535.
79. Papayannopoulos V, Zychlinsky A (2009) NETs: a new strategy for using old weapons. Trends Immunol 30: 513-521.
80. Xu J, Zhang X, Monestier M, Esmon NL, Esmon CT (2011) Extracellular histones are mediators of death through TLR2 and TLR4 in mouse fatal liver injury. J Immunol 187: 2626-2631.
81. Friggeri A, Banerjee S, Xie N, Cui H, De Freitas A, et al. (2012) Extracellular histones inhibit efferocytosis. Mol Med 18: 825-833.
82. Ning S, Pagano JS, Barber GN (2011) IRF7: activation, regulation, modification and function. Genes Immun 12: 399-414.
83. Barnes BJ, Kellum MJ, Field AE, Pitha PM (2002) Multiple regulatory domains of IRF-5 control activation, cellular localization, and induction of chemokines that mediate recruitment of T lymphocytes. Mol Cell Biol 22: 5721-5740.
84. Barnes BJ, Moore PA, Pitha PM (2001) Virus-specific activation of a novel interferon regulatory factor, IRF-5, results in the induction of distinct interferon alpha genes. J Biol Chem 276: 23382-23390.
85. Pandey AK, Yang Y, Jiang Z, Fortune SM, Coulombe F, et al. (2009) NOD2, RIP2 and IRF5 play a critical role in the type I interferon response to Mycobacterium tuberculosis. PLoS Pathog 5: e1000500.
86. Yanai H, Chen HM, Inuzuka T, Kondo S, Mak TW, et al. (2007) Role of IFN regulatory factor 5 transcription factor in antiviral immunity and tumor suppression. Proc Natl Acad Sci U S A 104: 3402-3407.
87. Yasuda K, Richez C, Maciaszek JW, Agrawal N, Akira S, et al. (2007) Murine dendritic cell type I IFN production induced by human IgG-RNA immune complexes is IFN regulatory factor (IRF)5 and IRF7 dependent and is required for IL-6 production. J Immunol 178: 6876-6885.
88. Couzinet A, Tamura K, Chen HM, Nishimura K, Wang Z, et al. (2008) A cell-type-specific requirement for IFN regulatory factor 5 (IRF5) in Fas-induced apoptosis. Proc Natl Acad Sci U S A 105: 2556-2561.
89. Hu G, Barnes BJ (2009) IRF-5 is a mediator of the death receptor-induced apoptotic signaling pathway. J Biol Chem 284: 2767-2777.
90. Negishi H, Ohba Y, Yanai H, Takaoka A, Honma K, et al. (2005) Negative regulation of Toll-like-receptor signaling by IRF-4. Proc Natl Acad Sci U S A 102: 15989-15994.
91. Paun A, Reinert JT, Jiang Z, Medin C, Balkhi MY, et al. (2008) Functional characterization of murine interferon regulatory factor 5 (IRF-5) and its role in the innate antiviral response. J Biol Chem 283: 14295-14308.
92. Krausgruber T, Blazek K, Smallie T, Alzabin S, Lockstone H, et al. (2011) IRF5 promotes inflammatory macrophage polarization and TH1-TH17 responses. Nat Immunol 12: 231-238.