Cytokine secretion in macrophages: SNAREs, Rabs, and membrane trafficking

Frontiers in Immunology

Volumn 5, Issue OCT, 2014, Pages

  Murray, Rachael Zoe ^a   Stow, Jennifer Lea ^b  

^a QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Cytokine secretion; IL 10; IL 6; Macrophages; Rabs; SNAREs; TNF

Indexed keywords

CHLOROTRIANISENE; CYTOKINE; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 15; INTERLEUKIN 1BETA; INTERLEUKIN 6; MEMBRANE PROTEIN; RAB PROTEIN; SNARE PROTEIN; SYNAPTOTAGMIN; TUMOR NECROSIS FACTOR;

CELL MIGRATION; CELL TRANSPORT; CYTOKINE RELEASE; ENDOPLASMIC RETICULUM; ENDOSOME; HUMAN; IMMUNE RESPONSE; MACROPHAGE; MEMBRANE FUSION; PHAGOCYTOSIS; REVIEW; SECRETORY PATHWAY; TRANS GOLGI NETWORK;

EID: 84918799200     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2014.00538     Document Type: Review

References (83)

1. Hume DA. The mononuclear phagocyte system. Curr Opin Immunol (2006) 18:49-53. doi: 10.1016/j.coi.2005.11.008
2. Tabas I, Glass CK. Anti-inflammatory therapy in chronic disease: challenges and opportunities. Science (2013) 339:166-72. doi:10.1126/science.1230720
3. Chawla A, Nguyen KD, Goh YP. Macrophage-mediated inflammation in metabolic disease. Nat Rev Immunol (2011) 11:738-49. doi:10.1038/nri3071
4. Neurath MF. Cytokines in inflammatory bowel disease. Nat Rev Immunol (2014) 14:329-42. doi:10.1038/nri3661
5. Foster SL, Medzhitov R. Gene-specific control of the TLR-induced inflammatory response. Clin Immunol (2009) 130:7-15. doi:10.1016/j.clim.2008.08.015
6. Schroder K, Sweet MJ, Hume DA. Signal integration between IFNgamma and TLR signalling pathways in macrophages. Immunobiology (2006) 211:511-24. doi:10.1016/j.imbio.2006.05.007
7. Rossol M, Heine H, Meusch U, Quandt D, Klein C, Sweet MJ, et al. LPS-induced cytokine production in human monocytes and macrophages. Crit Rev Immunol (2011) 31:379-446. doi:10.1615/CritRevImmunol.v31.i5.20
8. Marks MS, Heijnen HF, Raposo G. Lysosome-related organelles: unusual compartments become mainstream. Curr Opin Cell Biol (2013) 25:495-505. doi:10.1016/j.ceb.2013.04.008
9. Clark R, Griffiths GM. Lytic granules, secretory lysosomes and disease. Curr Opin Immunol (2003) 15:516-21. doi:10.1016/S0952-7915(03)00113-4
10. Manderson AP, Kay JG, Hammond LA, Brown DL, Stow JL. Subcompartments of the macrophage recycling endosome direct the differential secretion of IL-6 and TNFalpha. J Cell Biol (2007) 178:57-69. doi:10.1083/jcb.200612131
11. Murray RZ, Kay JG, Sangermani DG, Stow JL. A role for the phagosome in cytokine secretion. Science (2005) 310:1492-5. doi:10.1126/science.1120225
12. Murray RZ, Wylie FG, Khromykh T, Hume DA, Stow JL. Syntaxin 6 and Vti1b form a novel SNARE complex, which is up-regulated in activated macrophages to facilitate exocytosis of tumor necrosis Factor-alpha. J Biol Chem (2005) 280:10478-83. doi:10.1074/jbc.M414420200
13. Stanley AC, Lieu ZZ, Wall AA, Venturato J, Khromykh T, Hamilton NA, et al. Recycling endosome-dependent and -independent mechanisms for IL-10 secretion in LPS-activated macrophages. J Leukoc Biol (2012) 92:1227-39. doi:10.1189/jlb.0412191
14. Lieu ZZ, Lock JG, Hammond LA, La Gruta NL, Stow JL, Gleeson PA. A trans-Golgi network golgin is required for the regulated secretion of TNF in activated macrophages in vivo. Proc Natl Acad Sci U S A (2008) 105:3351-6. doi:10.1073/pnas.0800137105
15. Micaroni M, Stanley AC, Khromykh T, Venturato J, Wong CX, Lim JP, et al. Rab6a/a' are important Golgi regulators of pro-inflammatory TNF secretion in macrophages. PLoS One (2013) 8:e57034. doi:10.1371/journal.pone.0057034
16. Mori R, Ikematsu K, Kitaguchi T, Kim SE, Okamoto M, Chiba T, et al. Release of TNF-alpha from macrophages is mediated by small GTPase Rab37. Eur J Immunol (2011) 41:3230-9. doi:10.1002/eji.201141640
17. De Matteis MA, Luini A. Exiting the Golgi complex. Nat Rev Mol Cell Biol (2008) 9:273-84. doi:10.1038/nrm2378
18. Hsu VW, Prekeris R. Transport at the recycling endosome. Curr Opin Cell Biol (2010) 22:528-34. doi:10.1016/j.ceb.2010.05.008
19. Adrain C, Zettl M, Christova Y, Taylor N, Freeman M. Tumor necrosis factor signaling requires iRhom2 to promote trafficking and activation of TACE. Science (2012) 335:225-8. doi:10.1126/science.1214400
20. Tian Y, Pate C, Andreolotti A, Wang L, Tuomanen E, Boyd K, et al. Cytokine secretion requires phosphatidylcholine synthesis. J Cell Biol (2008) 181:945-57. doi:10.1083/jcb.200706152
21. Han C, Chen T, Yang M, Li N, Liu H, Cao X. Human SCAMP5, a novel secretory carrier membrane protein, facilitates calcium-triggered cytokine secretion by interaction with SNARE machinery. J Immunol (2009) 182:2986-96. doi:10.4049/jimmunol.0802002
22. Pagan JK, Wylie FG, Joseph S, Widberg C, Bryant NJ, James DE, et al. The t-SNARE syntaxin 4 is regulated during macrophage activation to function in membrane traffic and cytokine secretion. Curr Biol (2003) 13:156-60. doi:10.1016/S0960-9822(03)00006-X
23. Low PC, Misaki R, Schroder K, Stanley AC, Sweet MJ, Teasdale RD, et al. Phosphoinositide 3-kinase delta regulates membrane fission of Golgi carriers for selective cytokine secretion. J Cell Biol (2010) 190:1053-65. doi:10.1083/jcb.201001028
24. Braun V, Deschamps C, Raposo G, Benaroch P, Benmerah A, Chavrier P, et al. AP-1 and ARF1 control endosomal dynamics at sites of FcR mediated phagocytosis. Mol Biol Cell (2007) 18:4921-31. doi:10.1091/mbc.E07-04-0392
25. Arango Duque G, Fukuda M, Descoteaux A. Synaptotagmin XI regulates phagocytosis and cytokine secretion in macrophages. J Immunol (2013) 190:1737-45. doi:10.4049/jimmunol.1202500
26. Stanley AC, Wong CX, Micaroni M, Venturato J, Khromykh T, Stow JL, et al. The Rho GTPase Rac1 is required for recycling endosome-mediated secretion of TNF in macrophages. Immunol Cell Biol (2014) 92:275-86. doi:10.1038/icb.2013.90
27. Sudhof TC, Rothman JE. Membrane fusion: grappling with SNARE and SM proteins. Science (2009) 323:474-7. doi:10.1126/science.1161748
28. Offenhauser C, Lei N, Roy S, Collins BM, Stow JL, Murray RZ. Syntaxin 11 binds Vti1b and regulates late endosome to lysosome fusion in macrophages. Traffic (2011) 12:762-73. doi:10.1111/j.1600-0854.2011.01189.x
29. Risselada HJ, Grubmuller H. How SNARE molecules mediate membrane fusion: recent insights from molecular simulations. Curr Opin Struct Biol (2012) 22:187-96. doi:10.1016/j.sbi.2012.01.007
30. Jahn R, Fasshauer D. Molecular machines governing exocytosis of synaptic vesicles. Nature (2012) 490:201-7. doi:10.1038/nature11320
31. Veale KJ, Offenhauser C, Lei N, Stanley AC, Stow JL, Murray RZ. VAMP3 regulates podosome organisation in macrophages and together with Stx4/SNAP23 mediates adhesion, cell spreading and persistent migration. Exp Cell Res (2011) 317:1817-29. doi:10.1016/j.yexcr.2011.04.016
32. Fields IC, Shteyn E, Pypaert M, Proux-Gillardeaux V, Kang RS, Galli T, et al. v-SNARE cellubrevin is required for basolateral sorting of AP-1B-dependent cargo in polarized epithelial cells. J Cell Biol (2007) 177:477-88. doi:10.1083/jcb.200610047
33. Hernandez JM, Stein A, Behrmann E, Riedel D, Cypionka A, Farsi Z, et al. Membrane fusion intermediates via directional and full assembly of the SNARE complex. Science (2012) 336:1581-4. doi:10.1126/science.1221976
34. Alabi AA, Tsien RW. Perspectives on kiss-and-run: role in exocytosis, endocytosis, and neurotransmission. Annu Rev Physiol (2013) 75:393-422. doi:10.1146/annurev-physiol-020911-153305
35. Vardjan N, Jorgacevski J, Zorec R. Fusion pores, SNAREs, and exocytosis. Neuroscientist (2013) 19:160-74. doi:10.1177/1073858412461691
36. Hong W. SNAREs and traffic. Biochim Biophys Acta (2005) 1744:120-44. doi:10.1016/j.bbamcr.2005.03.014
37. Stow JL, Manderson AP, Murray RZ. SNAREing immunity: the role of SNAREs in the immune system. Nat Rev Immunol (2006) 6:919-29. doi:10.1038/nri1980
38. Zhao C, Smith EC, Whiteheart SW. Requirements for the catalytic cycle of the N-ethylmaleimide-sensitive factor (NSF). Biochim Biophys Acta (2012) 1823:159-71. doi:10.1016/j.bbamcr.2011.06.003
39. Hutagalung AH, Novick PJ. Role of Rab GTPases in membrane traffic and cell physiology. Physiol Rev (2011) 91:119-49. doi:10.1152/physrev.00059.2009
40. Mizuno-Yamasaki E, Rivera-Molina F, Novick P. GTPase networks in membrane traffic. Annu Rev Biochem (2012) 81:637-59. doi:10.1146/annurev-biochem-052810-093700
41. Wickner W. Membrane fusion: five lipids, four SNAREs, three chaperones, two nucleotides, and a Rab, all dancing in a ring on yeast vacuoles. Annu Rev Cell Dev Biol (2010) 26:115-36. doi:10.1146/annurev-cellbio-100109-104131
42. Kurowska M, Goudin N, Nehme NT, Court M, Garin J, Fischer A, et al. Terminal transport of lytic granules to the immune synapse is mediated by the kinesin-1/Slp3/Rab27a complex. Blood (2012) 119:3879-89. doi:10.1182/blood-2011-09-382556
43. Zhang XM, Ellis S, Sriratana A, Mitchell CA, Rowe T. Sec15 is an effector for the Rab11 GTPase in mammalian cells. J Biol Chem (2004) 279:43027-34. doi:10.1074/jbc.M402264200
44. Rajendran L, Knolker HJ, Simons K. Subcellular targeting strategies for drug design and delivery. Nat Rev Drug Discov (2010) 9:29-42. doi:10.1038/nrd2897
45. Masuyer G, Chaddock JA, Foster KA, Acharya KR. Engineered botulinum neurotoxins as new therapeutics. Annu Rev Pharmacol Toxicol (2014) 54:27-51. doi:10.1146/annurev-pharmtox-011613-135935
46. Stigter EA, Guo Z, Bon RS, Wu YW, Choidas A, Wolf A, et al. Development of selective, potent RabGGTase inhibitors. J Med Chem (2012) 55:8330-40. doi:10.1021/jm300624s
47. Shurety W, Merino-Trigo A, Brown D, Hume DA, Stow JL. Localization and post-Golgi trafficking of tumor necrosis factor-alpha in macrophages. J Interferon Cytokine Res (2000) 20:427-38. doi:10.1089/107999000312379
48. Munro S. The golgin coiled-coil proteins of the Golgi apparatus. Cold Spring Harbor Perspect Biol (2011) 3:a005256. doi:10.1101/cshperspect.a005256
49. Miserey-Lenkei S, Chalancon G, Bardin S, Formstecher E, Goud B, Echard A. Rab and actomyosin-dependent fission of transport vesicles at the Golgi complex. Nat Cell Biol (2010) 12:645-54. doi:10.1038/ncb2067
50. De Matteis MA, Di Campli A, Godi A. The role of the phosphoinositides at the Golgi complex. Biochim Biophys Acta (2005) 1744:396-405. doi:10.1016/j.bbamcr.2005.04.013
51. Gonzalez-Jamett AM, Momboisse F, Haro-Acuna V, Bevilacqua JA, Caviedes P, Cardenas AM. Dynamin-2 function and dysfunction along the secretory pathway. Front Endocrinol (2013) 4:126. doi:10.3389/fendo.2013.00126
52. Kay JG, Murray RZ, Pagan JK, Stow JL. Cytokine secretion via cholesterol-rich lipid raft-associated SNAREs at the phagocytic cup. J Biol Chem (2006) 281:11949-54. doi:10.1074/jbc.M600857200
53. Mattila PK, Lappalainen P. Filopodia: molecular architecture and cellular functions. Nat Rev Mol Cell Biol (2008) 9:446-54. doi:10.1038/nrm2406
54. Niedergang F, Colucci-Guyon E, Dubois T, Raposo G, Chavrier P. ADP ribosylation factor 6 is activated and controls membrane delivery during phagocytosis in macrophages. J Cell Biol (2003) 161:1143-50. doi:10.1083/jcb.200210069
55. Beemiller P, Hoppe AD, Swanson JA. A phosphatidylinositol-3-kinase-dependent signal transition regulates ARF1 and ARF6 during Fcgamma receptor-mediated phagocytosis. PLoS Biol (2006) 4:e162. doi:10.1371/journal.pbio.0040162
56. Vinet AF, Fukuda M, Descoteaux A. The exocytosis regulator synaptotagmin V controls phagocytosis in macrophages. J Immunol (2008) 181:5289-95. doi:10.4049/jimmunol.181.8.5289
57. Heasman SJ, Ridley AJ. Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat Rev Mol Cell Biol (2008) 9:690-701. doi:10.1038/nrm2476
58. Bokoch GM. Regulation of innate immunity by Rho GTPases. Trends Cell Biol (2005) 15:163-71. doi:10.1016/j.tcb.2005.01.002
59. Tellier E, Canault M, Rebsomen L, Bonardo B, Juhan-Vague I, Nalbone G, et al. The shedding activity of ADAM17 is sequestered in lipid rafts. Exp Cell Res (2006) 312:3969-80. doi:10.1016/j.yexcr.2006.08.027
60. McIlwain DR, Lang PA, Maretzky T, Hamada K, Ohishi K, Maney SK, et al. iRhom2 regulation of TACE controls TNF-mediated protection against Listeria and responses to LPS. Science (2012) 335:229-32. doi:10.1126/science.1214448
61. Siggs OM, Xiao N, Wang Y, Shi H, Tomisato W, Li X, et al. iRhom2 is required for the secretion of mouse TNFalpha. Blood (2012) 119:5769-71. doi:10.1182/blood-2012-03-417949
62. Dinarello CA. Immunological and inflammatory functions of the interleukin-1 family. Annu Rev Immunol (2009) 27:519-50. doi:10.1146/annurev.immunol.021908.132612
63. Dubyak GR. P2X7 receptor regulation of non-classical secretion from immune effector cells. Cell Microbiol (2012) 14:1697-706. doi:10.1111/cmi.12001
64. Hamon Y, Luciani MF, Becq F, Verrier B, Rubartelli A, Chimini G. Interleukin-1beta secretion is impaired by inhibitors of the Atp binding cassette transporter, ABC1. Blood (1997) 90:2911-5.
65. Flieger O, Engling A, Bucala R, Lue H, Nickel W, Bernhagen J. Regulated secretion of macrophage migration inhibitory factor is mediated by a non-classical pathway involving an ABC transporter. FEBS Lett (2003) 551:78-86. doi:10.1016/S0014-5793(03)00900-1
66. Bergsbaken T, Fink SL, Cookson BT. Pyroptosis: host cell death and inflammation. Nat Rev Microbiol (2009) 7:99-109. doi:10.1038/nrmicro2070
67. Eder C. Mechanisms of interleukin-1beta release. Immunobiology (2009) 214:543-53. doi:10.1016/j.imbio.2008.11.007
68. Blott EJ, Griffiths GM. Secretory lysosomes. Nat Rev Mol Cell Biol (2002) 3:122-31. doi:10.1038/nrm732
69. Andrei C, Dazzi C, Lotti L, Torrisi MR, Chimini G, Rubartelli A. The secretory route of the leaderless protein interleukin 1beta involves exocytosis of endolysosome-related vesicles. Mol Biol Cell (1999) 10:1463-75. doi:10.1091/mbc.10.5.1463
70. Bruns C, McCaffery JM, Curwin AJ, Duran JM, Malhotra V. Biogenesis of a novel compartment for autophagosome-mediated unconventional protein secretion. J Cell Biol (2011) 195:979-92. doi:10.1083/jcb.201106098
71. Jiang S, Dupont N, Castillo EF, Deretic V. Secretory versus degradative autophagy: unconventional secretion of inflammatory mediators. J Innate Immun (2013) 5:471-9. doi:10.1159/000346707
72. Dupont N, Jiang S, Pilli M, Ornatowski W, Bhattacharya D, Deretic V. Autophagy-based unconventional secretory pathway for extracellular delivery of IL-1beta. EMBO J (2011) 30:4701-11. doi:10.1038/emboj.2011.398
73. Croxford AL, Kulig P, Becher B. IL-12-and IL-23 in health and disease. Cytokine Growth Factor Rev (2014) 25:415-21. doi:10.1016/j.cytogfr.2014.07.017
74. Snijders A, Hilkens CM, van der Pouw Kraan TC, Engel M, Aarden LA, Kapsenberg ML. Regulation of bioactive IL-12 production in lipopolysaccharide-stimulated human monocytes is determined by the expression of the p35 subunit. J Immunol (1996) 156:1207-12.
75. Murphy FJ, Hayes MP, Burd PR. Disparate intracellular processing of human IL-12 preprotein subunits: atypical processing of the P35 signal peptide. J Immunol (2000) 164:839-47. doi:10.4049/jimmunol.164.2.839
76. Vaidyanathan H, Zhou Y, Petro TM, Schwartzbach SD. Intracellular localization of the p35 subunit of murine IL-12. Cytokine (2003) 21:120-8. doi:10.1016/S1043-4666(03)00016-4
77. Duitman EH, Orinska Z, Bulanova E, Paus R, Bulfone-Paus S. How a cytokine is chaperoned through the secretory pathway by complexing with its own receptor: lessons from interleukin-15 (IL-15)/IL-15 receptor alpha. Mol Cell Biol (2008) 28:4851-61. doi:10.1128/MCB.02178-07
78. Ouyang S, Hsuchou H, Kastin AJ, Pan W. TNF stimulates nuclear export and secretion of IL-15 by acting on CRM1 and ARF6. PLoS One (2013) 8:e69356. doi:10.1371/journal.pone.0069356
79. Erlandsson Harris H, Andersson U. Mini-review: the nuclear protein HMGB1 as a proinflammatory mediator. Eur J Immunol (2004) 34:1503-12. doi:10.1002/eji.200424916
80. Scaffidi P, Misteli T, Bianchi ME. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature (2002) 418:191-5. doi:10.1038/nature00858
81. Gardella S, Andrei C, Ferrera D, Lotti LV, Torrisi MR, Bianchi ME, et al. The nuclear protein HMGB1 is secreted by monocytes via a non-classical, vesicle-mediated secretory pathway. EMBO Rep (2002) 3:995-1001. doi:10.1093/embo-reports/kvf198
82. Bonaldi T, Talamo F, Scaffidi P, Ferrera D, Porto A, Bachi A, et al. Monocytic cells hyperacetylate chromatin protein HMGB1 to redirect it towards secretion. EMBO J (2003) 22:5551-60. doi:10.1093/emboj/cdg516
83. Lee H, Shin N, Song M, Kang UB, Yeom J, Lee C, et al. Analysis of nuclear high mobility group box 1 (HMGB1)-binding proteins in colon cancer cells: clustering with proteins involved in secretion and extranuclear function. J Proteome Res (2010) 9:4661-70. doi:10.1021/pr100386r