Mechanisms of cytokine secretion: A portfolio of distinct pathways allows flexibility in cytokine activity

European Journal of Cell Biology

Volumn 90, Issue 6-7, 2011, Pages 476-483

  Duitman, Erwin Hans ^a   Orinska, Zane ^a   Bulfone Paus, Silvia ^a,b  

^a RESEARCH CENTER BORSTEL   (Germany)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

IL 1 ; IL 12; IL 15; IL 2; TNF

Indexed keywords

INTERLEUKIN 12; INTERLEUKIN 15; INTERLEUKIN 1BETA; INTERLEUKIN 2; MESSENGER RNA; TUMOR NECROSIS FACTOR ALPHA;

BINDING AFFINITY; CELL DIFFERENTIATION; CELL INTERACTION; CELL SURFACE; CYTOKINE RELEASE; ENDOPLASMIC RETICULUM; GOLGI COMPLEX; HUMAN; MACROPHAGE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN STABILITY; PROTEIN TRANSPORT; REGULATORY MECHANISM; SECRETORY PATHWAY; SHORT SURVEY; SIGNAL TRANSDUCTION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TH17 CELL;

ANIMALS; CYTOKINES; HUMANS;

EID: 79955466520     PISSN: 01719335     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejcb.2011.01.010     Document Type: Short Survey

References (92)

1. Andrei C., Dazzi C., Lotti L., Torrisi M.R., Chimini G., Rubartelli A. The secretory route of the leaderless protein interleukin1beta involves exocytosis of endolysosome-related vesicles. Mol. Biol. Cell 1999, 10:1463-1475.
2. Andrei C., Margiocco P., Poggi A., Lotti L.V., Torrisi M.R., Rubartelli A. Phospholipases C and A2 control lysosome-mediated IL-1 beta secretion: implications for inflammatory processes. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:9745-9750.
3. Benado A., Nasagi-Atiya Y., Sagi-Eisenberg R. Protein trafficking in immune cells. Immunobiology 2009, 214:507-525.
4. Bergamaschi C., Rosati M., Jalah R., Valentin A., Kulkarni V., Alicea C., Zhang G.M., Patel V., Felber B.K., Pavlakis G.N. Intracellular interaction of interleukin-15 with its receptor alpha during production leads to mutual stabilization and increased bioactivity. J. Biol. Chem. 2008, 283:4189-4199.
5. Bergamaschi C., Jalah R., Kulkarni V., Rosati M., Zhang G.M., Alicea C., Zolotukhin A.S., Felber B.K., Pavlakis G.N. Secretion and biological activity of short signal peptide IL-15 is chaperoned by IL-15 receptor alpha in vivo. J. Immunol. 2009, 183:3064-3072.
6. Bianco F., Pravettoni E., Colombo A., Schenk U., Möller T., Matteoli M., Verderio C. Astrocyte-derived ATP induces vesicle shedding and IL-1 beta release from microglia. J. Immunol. 2005, 174:7268-7277.
7. Black R.A., Rauch C.T., Kozlosky C.J., Peschon J.J., Slack J.L., Wolfson M.F., Castner B.J., Stocking K.L., Reddy P., Srinivasan S., Nelson N., Boiani N., Schooley K.A., Gerhart M., Davis R., Fitzner J.N., Johnson R.S., Paxton R.J., March C.J., Cerretti D.P. A metalloproteinase disintegrin that releases tumour-necrosis factor-alpha from cells. Nature 1997, 385:729-733.
8. Bosenberg M.W., Massagué J. Juxtacrine cell signaling molecules. Curr. Opin. Cell Biol. 1993, 5:832-838.
9. Brough D., Rothwell N.J. Caspase-1-dependent processing of pro-interleukin-1b is cytosolic and precedes cell death. J. Cell Sci. 2007, 120:772-781.
10. Carra G., Gerosa F., Trinchieri G. Biosynthesis and posttranslational regulation of human IL-12. J. Immunol. 2000, 164:4752-4761.
11. Carriere V., Roussel L., Ortega N., Lacorre D.A., Americh L., Aguilar L., Bouche G., Girard J.P. IL-33, the IL-1-like cytokine ligand for ST2 receptor, is a chromatin-associated nuclear factor in vivo. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:282-287.
12. Carta S., Tassi S., Semino C., Fossati G., Mascagni P., Dinarello C.A., Rubartelli A. Histone deacetylase inhibitors prevent exocytosis of interleukin-1beta-containing secretory lysosomes: role of microtubules. Blood 2006, 108:1618-1626.
13. Collison L.W., Workman C.J., Kuo T.T., Boyd K., Wang Y., Vignali K.M., Cross R., Sehy D., Blumberg R.S., Vignali D.A. The inhibitory cytokine IL-35 contributes to regulatory T-cell function. Nature 2007, 450:566-569.
14. Conradt H.S., Ausmeier M., Dittmar K.E., Hauser H., Lindenmaier W. Secretion of glycosylated human interleukin-2 by recombinant mammalian cell lines. Carbohydr. Res. 1986, 149:443-450.
15. Crispín J.C., Tsokos G.C. Transcriptional regulation of IL-2 in health and autoimmunity. Autoimmun. Rev. 2009, 8:190-195.
16. Crivellato E., Nico B., Mallardi F., Beltrami C.A., Ribatti D. Piecemeal degranulation as a general secretory mechanism?. Anat. Rec. A: Discov. Mol. Cell. Evol. Biol. 2003, 274:778-784.
17. Curnow S.J., Pryce K., Modi N., Knight B., Graham E.M., Stewart J.E., Fortune F., Stanford M.R., Murray P.I., Wallace G.R. Serum cytokine profiles in Behçet's disease: is there a role for IL-15 in pathogenesis?. Immunol. Lett. 2008, 121:7-12.
18. Dejgaard S., Nicolay J., Taheri M., Thomas D.Y., Bergeron J.J. The ER glycoprotein quality control system. Curr. Issues Mol. Biol. 2004, 6:29-42.
19. Denef C. Paracrinicity: the story of 30 years of cellular pituitary crosstalk. J. Neuroendocrinol. 2008, 20:1-70.
20. Dinarello C.A. Immunological and inflammatory functions of the interleukin-1 family. Annu. Rev. Immunol. 2009, 27:519-550.
21. Dinarello C.A. IL-1: discoveries, controversies and future directions. Eur. J. Immunol. 2010, 40:599-606.
22. Domonkos A., Udvardy A., Laszlo L., Nagy T., Duda E. Receptor-like properties of the 26kDa transmembrane form of TNF. Eur. Cytokine Netw. 2001, 12:411-419.
23. Duitman E.H., 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 α. Mol. Cell. Biol. 2008, 15:4851-4861.
24. Eder C. Mechanisms of interleukin-1β release. Immunobiology 2009, 214:543-553.
25. Eisenberg S.P., Brewer M.T., Verderber E., Heimdal P., Brandhuber B.J., Thompson R.C. Interleukin 1 receptor antagonist is a member of the interleukin 1 gene family: evolution of a cytokine control mechanism. Proc. Natl. Acad. Sci. U. S. A. 1991, 88:5232-5236.
26. Ferrari D., Pizzirani C., Adinolfi E., Lemoli R.M., Curti A., Idzko M., Panther E., Di Virgilio F. The P2X7 receptor: a key player in IL-1 processing and release. J. Immunol. 2006, 176:3877-3883. (Erratum in: J. Immunol. 179 (2007) 8569).
27. Franchi L., Eigenbrod T., Muñoz-Planillo R., Nuñez G. The inflammasome: a caspase-1-activation platform that regulates immune responses and disease pathogenesis. Nat. Immunol. 2009, 10:241-247.
28. Gaggero A., Azzarone B., Andrei C., Mishal Z., Meazza R., Zappia E., Rubartelli A., Ferrini F. Differential intracellular trafficking, secretion and endosomal localization of two IL-15 isoforms. Eur. J. Immunol. 1999, 29:1265-1274.
29. Giron-Michel J., Giuliani M., Fogli M., Brouty-Boyé D., Ferrini S., Baychelier F., Eid P., Lebousse-Kerdilès C., Durali D., Biassoni R., Charpentier B., Vasquez A., Chouaib S., Caignard A., Moretta L., Azzarone B. Membrane-bound and soluble IL-15/IL-15Ralpha complexes display differential signaling and functions on human hematopoietic progenitors. Blood 2005, 106:2302-2310.
30. Goodwin R.G., Lupton S., Schmierer A., Hjerrild K.J., Jerzy R., Clevenger W., Gillis S., Cosman D., Namen A.E. Human interleukin 7: molecular cloning and growth factor activity on human and murine B-lineage cells. Proc. Natl. Acad. Sci. U. S. A. 1989, 86:302-306.
31. Grell M., Douni E., Wajant H., Löhden M., Clauss M., Maxeiner B., Georgopoulos S., Lesslauer W., Kollias G., Pfizenmaier K., Scheurich P. The transmembrane form of tumor necrosis factor is the prime activating ligand of the 80kDa tumor necrosis factor receptor. Cell 1995, 83:793-802.
32. Griffiths G.M., Tsun A., Stinchcombe J.C. The immunological synapse: a focal point for endocytosis and exocytosis. J. Cell Biol. 2010, 189:399-406.
33. Halban P.A., Irminger J.C. Sorting and processing of secretory proteins. Biochem. J. 1994, 299:1-18.
34. Hamon Y., Luciani M.F., Becq F., Verrier B., Rubartelli A., Chimini G. Interleukin-1beta secretion is impaired by inhibitors of the Atp binding cassette transporter, ABC1. Blood 1997, 90:2911-2915.
35. Harrington L.E., Hatton R.D., Mangan P.R., Turner H., Murphy T.L., Murphy K.M., Weaver C.T. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat. Immunol. 2005, 6:1123-1132.
36. Hehlgans T., Pfeffer K. The intriguing biology of the tumour necrosis factor/tumour necrosis factor receptor superfamily: players, rules and the games. Immunology 2005, 115:1-20.
37. Horiuchi T., Mitoma H., Harashima S., Tsukamoto H., Shimoda T. Transmembrane TNF-alpha: structure, function and interaction with anti-TNF agents. Rheumatology (Oxford) 2010, 49:1215-1228.
38. Huse M., Lillemeier B.F., Kuhns M.S., Chen D.S., Davis M.M. T cells use two directionally distinct pathways for cytokine secretion. Nat. Immunol. 2006, 7:247-255.
39. Huse M., Quann E.J., Davis M.M. Shouts, whispers and the kiss of death: directional secretion in T cells. Nat. Immunol. 2008, 9:1105-1111.
40. Jang G.C., Kim H.Y., Ahn S.Y., Kim D.S. Raised serum interleukin 15 levels in Kawasaki disease. Ann. Rheum. Dis. 2003, 62:264-266.
41. Kallen K.J. The role of transsignalling via the agonistic soluble IL-6 receptor in human diseases. Biochim. Biophys. Acta 2002, 1592:323-343.
42. Kuczyński S., Winiarska H., Abramczyk M., Szczawińska K., Wierusz-Wysocka B., Dworacka M. IL-15 is elevated in serum patients with type 1 diabetes mellitus. Diabetes Res. Clin. Pract. 2005, 69:231-236.
43. Kurys G., Tagaya Y., Bamford R., Hanover J.A., Waldmann T.A. The long signal peptide isoform and its alternative processing direct the intracellular trafficking of interleukin-15. J. Biol. Chem. 2000, 275:30653-30659.
44. McGraw-Hill Concise Encyclopedia of Science and Technology 2005, McGraw-Hill, New York. 5th edition. M. Licker (Ed.).
45. Lieu Z.Z., Lock J.G., Hammond L.A., La Gruta N.L., Stow J.L., Gleeson P.A. A trans-golgi network golgin is required for the regulated secretion of TNFa in activated macrophages in vivo. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:3351-3356.
46. Losy J., Niezgoda A., Zaremba J. IL-15 is elevated in sera of patients with relapsing-remitting multiple sclerosis. Folia Neuropathol. 2002, 40:151-153.
47. Luheshi N.M., Rothwell N.J., Brough D. Dual functionality of interleukin-1 family cytokines: implications for anti-interleukin-1 therapy. Br. J. Pharmacol. 2009, 157:1318-1329.
48. Ma A., Koka R., Burkett P. Diverse functions of IL-2, IL-15, and IL-7 in lymphoid homeostasis. Annu. Rev. Immunol. 2006, 24:657-679.
49. MacKenzie A., Wilson H.L., Kiss-Toth E., Dower S.K., North R.A., Surprenant A. Rapid secretion of interleukin-1beta by microvesicle shedding. Immunity 2001, 15:825-835.
50. Malek T.R. The biology of interleukin-2. Annu. Rev. Immunol. 2008, 26:453-479.
51. Manderson A.P., Kay J.G., Hammond L.A., Brown D.L., Stow J.L. Subcompartments of the macrophage recycling endosome direct the differential secretion of IL-6 and TNFa. J. Cell Biol. 2007, 178:57-69.
52. Martins G.A., Cimmino L., Liao J., Magnusdottir E., Calame K. Blimp-1 directly represses Il2 and the Il2 activator Fos, attenuating T cell proliferation and survival. J. Exp. Med. 2008, 205:1959-1965.
53. Marty V., Medina C., Combe C., Parnet P., Amedee T. ATP-binding cassette transporter ABC1 is required for the release of interleukin-1b by P2X7-stimulated and lipopolysaccharide-primed mouse Schwann cells. Glia 2005, 49:511-519.
54. Moqbel R., Coughlin J.J. Differential secretion of cytokines. Sci. STKE 2006, 338:26.
55. Morandi B., Mortara L., Carrega P., Cantoni C., Costa G., Accolla R.S., Mingari M.C., Ferrini S., Moretta L., Ferlazzo G. NK cells provide helper signal for CD8+ T cells by inducing the expression of membrane-bound IL-15 on DCs. Int. Immunol. 2009, 21:599-606.
56. Mortier E., Woo T., Advincula R., Gozalo S., Ma A. IL-15Ralpha chaperones IL-15 to stable dendritic cell membrane complexes that activate NK cells via trans presentation. J. Exp. Med. 2008, 205:1213-1225.
57. 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.
58. Mosmann T.R., Coffman R.L. TH1 and TH2 cells: different patterns of lymphokine secretion lead to different functional properties. Annu. Rev. Immunol. 1989, 7:145-173.
59. Murphy C.A., Langrish C.L., Chen Y., Blumenschein W., McClanahan T., Kastelein R.A., Sedgwick J.D., Cua D.J. Divergent pro- and antiinflammatory roles for IL-23 and IL-12 in joint autoimmune inflammation. J. Exp. Med. 2003, 198:1951-1957.
60. Murphy F.J., Hayes M.P., Burd P.R. Disparate intracellular processing of human IL-12 preprotein subunits: atypical processing of the P35 signal peptide. J. Immunol. 2000, 164:839-847.
61. Murray R.Z., Kay J.G., Sangermani D.G., Stow J.L. A role of the phagosome in cytokine secretion. Science 2005, 310:1492-1495.
62. Musso T., Calosso L., Zucca M., Millesimo M., Ravarino D., Giovarelli M., Malavasi F., Ponzi A.N., Paus R., Bulfone-Paus S. Human monocytes constitutively express membrane-bound, biologically active, and interferon-gamma-upregulated interleukin-15. Blood 1999, 93:3531-3539.
63. Neely G.G., Epelman S., Ma L.L., Colarusso P., Howlett C.J., Amankwah E.K., McIntyre A.C., Robbins S.M., Mody C.H. Monocyte surface-bound IL-15 can function as an activating receptor and participate in reverse signaling. J. Immunol. 2004, 172:4225-4234.
64. Neill D.R., Wong S.H., Bellosi A., Flynn R.J., Daly M., Langford T.K., Bucks C., Kane C.M., Fallon P.G., Pannell R., Jolin H.E., McKenzie A.N. Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature 2010, 464:1367-1370.
65. Nickel W. The mystery of nonclassical protein secretion. A current view on cargo proteins and potential export routes. Eur. J. Biochem. 2003, 270:2109-2119.
66. Onu A., Pohl T., Krause H., Bulfone-Paus S. Regulation of IL-15 secretion via the leader peptide of two IL-15 isoforms. J. Immunol. 1997, 158:255-262.
67. Oppmann B., Lesley R., Blom B., Timans J.C., Xu Y., Hunte B., Vega F., Yu N., Wang J., Singh K., Vaisberg E., Churakova T., Liu M., Gorman D., Wagner J., Zurawski S., Liu Y., Abrams J.S., Moore K.W., Rennick D., de Waal-Malefyt R., Hannum C., Bazan J.F., Kastelein R.A. Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity 2000, 13:715-725.
68. O'Reilly L.A., Tai L., Lee L., Kruse E.A., Grabow S., Fairlie W.D., Haynes N.M., Tarlinton D.M., Zhang J.G., Belz G.T., Smyth M.J., Bouillet P., Robb L., Strasser A. Membrane-bound Fas ligand only is essential for Fas-induced apoptosis. Nature 2009, 461:659-663.
69. Park H., Li Z., Yang X.O., Chang S.H., Nurieva R., Wang Y.H., Wang Y., Hood L., Zhu Z., Tian Q., Dong C. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat. Immunol. 2005, 6:1133-1141.
70. Park J.J., Loh Y.P. How peptide hormone vesicles are transported to the secretion site for exocytosis. Mol. Endocrinol. 2008, 22:2583-2595.
71. Pflanz S., Timans J.C., Cheung J., Rosales R., Kanzler H., Gilbert J., Hibbert L., Churakova T., Travis M., Vaisberg E., Blumenschein W.M., Mattson J.D., Wagner J.L., To W., Zurawski S., McClanahan T.K., Gorman D.M., Bazan J.F., de Waal Malefyt R., Rennick D., Kastelein R.A. IL-27, a heterodimeric cytokine composed of EBI3 and p28 protein, induces proliferation of naive CD4(+) T cells. Immunity 2002, 16:779-790.
72. Pickett J.A., Edwardson J.M. Compound exocytosis: mechanisms and functional significance. Traffic 2006, 7:109-116.
73. Pizzirani C., Ferrari D., Chiozzi P., Adinolfi E., Sandonà D., Savaglio E., Di Virgilio F. Stimulation of P2 receptors causes release of IL-1beta-loaded microvesicles from human dendritic cells. Blood 2007, 109:3856-3864.
74. Prudovsky I., Mandinova A., Soldi R., Bagala C., Graziani I., Landriscina M., Tarantini F., Duarte M., Bellum S., Doherty H., Maciag T. The non-classical export routes: FGF1 and IL-1alpha point the way. J. Cell Sci. 2003, 116(Pt 24):4871-4881.
75. Qu Y., Franchi L., Nunez G., Dubyak G.R. Nonclassical IL-1 beta secretion stimulated by P2X7 receptors is dependent on inflammasome activation and correlated with exosome release in murine macrophages. J. Immunol. 2007, 179:1913-1925.
76. Re R.N. Toward a theory of intracrine hormone action. Regul. Pept. 2002, 106:1-6.
77. Reis e Sousa C., Hieny S., Scharton-Kersten T., Jankovic D., Charest H., Germain R.N., Sher A. In vivo microbial stimulation induces rapid CD40 ligand-independent production of interleukin 12 by dendritic cells and their redistribution to T cell areas. J. Exp. Med. 1997, 186:1819-1829.
78. Rennick D., Kastelein R.A. IL-27, a heterodimeric cytokine composed of EBI3 and p28 protein, induces proliferation of naive CD4(+) T cells. Immunity 2002, 16:779-790.
79. Rose-John S., Waetzig G.H., Scheller J., Grötzinger J., Seegert D. The IL-6/sIL-6R complex as a novel target for therapeutic approaches. Expert Opin. Ther. Targets 2007, 11:613-624.
80. Schluns K.S., Stoklasek T., Lefrançois L. The roles of interleukin-15 receptor alpha: trans-presentation, receptor component, or both?. Int. J. Biochem. Cell Biol. 2005, 37:1567-1571.
81. Simpson J.C. Screening the secretion machinery: high throughput imaging approaches to elucidate the secretory pathway. Semin. Cell Dev. Biol. 2009, 20:903-909.
82. Sojka D.K., Bruniquel D., Schwartz R.H., Singh N.J. IL-2 secretion by CD4+ T cells in vivo is rapid, transient, and influenced by TCR-specific competition. J. Immunol. 2004, 172:6136-6143.
83. Stanley A.C., Lacy P. Pathways for cytokine secretion. Physiology 2010, 25:218-229.
84. Staudt V., Bothur E., Klein M., Lingnau K., Reuter S., Grebe N., Gerlitzki B., Hoffmann M., Ulges A., Taube C., Dehzad N., Becker M., Stassen M., Steinborn A., Lohoff M., Schild H., Schmitt E., Bopp T. Interferon-regulatory factor 4 is essential for the developmental program of T helper 9 cells. Immunity 2010, 33:192-202.
85. Stow J.L., Low P.C., Offenhäuser C., Sangermani D. Cytokine secretion in macrophages and other cells: pathways and mediators. Immunobiology 2009, 214:601-612.
86. Tang P., Hung M.C., Klostergaard J. Human pro-tumor necrosis factor is a homotrimer. Biochemistry 1996, 35:8216-8225.
87. Trinchieri G. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat. Rev. Immunol. 2003, 3:133-146.
88. Trinchieri G., Pflanz S., Kastelein R.A. The IL-12 family of heterodimeric cytokines: new players in the regulation of T cell responses. Immunity 2003, 19:641-644.
89. Villarino A.V., Tato C.M., Stumhofer J.S., Yao Z., Cui Y.K., Hennighausen L., O'Shea J.J., Hunter C.A. Helper T cell IL-2 production is limited by negative feedback and STAT-dependent cytokine signals. J. Exp. Med. 2007, 204:65-71.
90. Waldmann T.A. The biology of interleukin-2 and interleukin-15: implications for cancer therapy and vaccine design. Nat. Rev. Immunol. 2006, 6:595-601.
91. Yang Y.C., Ciarletta A.B., Temple P.A., Chung M.P., Kovacic S., Witek-Giannotti J.S., Leary A.C., Kriz R., Donahue R.E., Wong G.G., Clark S.C. Human IL-3 (multi-CSF): identification by expression cloning of a novel hematopoietic growth factor related to murine IL-3. Cell 1986, 47:3-10.
92. Zimmerman G.A., Lorant D.E., McIntyre T.M., Prescott S.M. Juxtacrine intercellular signaling: another way to do it. Am. J. Respir. Cell Mol. Biol. 1993, 9:573-577.