Promotion of Expansion and Differentiation of Hematopoietic Stem Cells by Interleukin-27 into Myeloid Progenitors to Control Infection in Emergency Myelopoiesis

PLoS Pathogens

Volumn 12, Issue 3, 2016, Pages

  Furusawa, Jun Ichi ^a   Mizoguchi, Izuru ^a   Chiba, Yukino ^a   Hisada, Masayuki ^a   Kobayashi, Fumie ^b   Yoshida, Hiroki ^c   Nakae, Susumu ^d   Tsuchida, Akihiko ^a   Matsumoto, Tetsuya ^a   Ema, Hideo ^e   Mizuguchi, Junichiro ^a   Yoshimoto, Takayuki ^a  

^a TOKYO MEDICAL UNIVERSITY   (Japan)

^b KYORIN UNIVERSITY   (Japan)

^c SAGA UNIVERSITY   (Japan)

^d UNIVERSITY OF TOKYO   (Japan)

^e KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA1 INTERFERON; GAMMA INTERFERON; INTERLEUKIN 17 RECEPTOR; INTERLEUKIN 27; RETROVIRUS VECTOR; STAT1 PROTEIN; STAT3 PROTEIN; CYTOKINE; IL27 PROTEIN, MOUSE; INTERLEUKIN DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DIFFERENTIATION; CELL TRANSFER; COLONY FORMING UNIT GM; CONTROLLED STUDY; DOWNSTREAM PROCESSING; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENOTYPE PHENOTYPE CORRELATION; HEMATOPOIETIC STEM CELL; HYDRODYNAMICS; IN VITRO STUDY; INFECTION CONTROL; INFLAMMATION; MALARIA; MOUSE; MYELOID PROGENITOR CELL; MYELOPOIESIS; NEUTROPHIL COUNT; NONHUMAN; PARASITEMIA; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; ANIMAL; B LYMPHOCYTE; BONE MARROW; BONE MARROW CELL; C57BL MOUSE; CELL LINEAGE; DRUG EFFECTS; HEMATOPOIESIS; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION; SPLEEN;

ANIMALS; B-LYMPHOCYTES; BONE MARROW; CELL DIFFERENTIATION; CELL LINEAGE; CYTOKINES; HEMATOPOIESIS; HEMATOPOIETIC STEM CELLS; INTERLEUKINS; MICE; MICE, INBRED C57BL; MYELOID CELLS; MYELOID PROGENITOR CELLS; MYELOPOIESIS; SIGNAL TRANSDUCTION; SPLEEN;

EID: 84962374894     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005507     Document Type: Article

References (65)

1. Takizawa H, Boettcher S, Manz MG, (2012) Demand-adapted regulation of early hematopoiesis in infection and inflammation. Blood119: 2991–3002. doi: 10.1182/blood-2011-12-38011322246037
2. King KY, Goodell MA, (2011) Inflammatory modulation of HSCs: viewing the HSC as a foundation for the immune response. Nat Rev Immunol11: 685–692. doi: 10.1038/nri306221904387
3. Sato T, Onai N, Yoshihara H, Arai F, Suda T, et al. (2009) Interferon regulatory factor-2 protects quiescent hematopoietic stem cells from type I interferon-dependent exhaustion. Nat Med15: 696–700. doi: 10.1038/nm.197319483695
4. Essers MA, Offner S, Blanco-Bose WE, Waibler Z, Kalinke U, et al. (2009) IFNalpha activates dormant haematopoietic stem cells in vivo. Nature458: 904–908. doi: 10.1038/nature0781519212321
5. Baldridge MT, King KY, Boles NC, Weksberg DC, Goodell MA, (2010) Quiescent haematopoietic stem cells are activated by IFN-gamma in response to chronic infection. Nature465: 793–797. doi: 10.1038/nature0913520535209
6. Belyaev NN, Brown DE, Diaz AI, Rae A, Jarra W, et al. (2010) Induction of an IL7-R(+)c-Kit(hi) myelolymphoid progenitor critically dependent on IFN-gamma signaling during acute malaria. Nat Immunol11: 477–485. doi: 10.1038/ni.186920431620
7. Broxmeyer HE, Cooper S, Rubin BY, Taylor MW, (1985) The synergistic influence of human interferon-gamma and interferon-alpha on suppression of hematopoietic progenitor cells is additive with the enhanced sensitivity of these cells to inhibition by interferons at low oxygen tension in vitro. J Immunol135: 2502–2506. 3928752
8. Chen J, Lipovsky K, Ellison FM, Calado RT, Young NS, (2004) Bystander destruction of hematopoietic progenitor and stem cells in a mouse model of infusion-induced bone marrow failure. Blood104: 1671–1678. 15166031
9. Murphy M, Loudon R, Kobayashi M, Trinchieri G, (1986) Gamma interferon and lymphotoxin, released by activated T cells, synergize to inhibit granulocyte/monocyte colony formation. J Exp Med164: 263–279. 3088195
10. de Bruin AM, Demirel O, Hooibrink B, Brandts CH, Nolte MA, (2013) Interferon-gamma impairs proliferation of hematopoietic stem cells in mice. Blood121: 3578–3585. doi: 10.1182/blood-2012-05-43290623487025
11. Pietras EM, Lakshminarasimhan R, Techner JM, Fong S, Flach J, et al. (2014) Re-entry into quiescence protects hematopoietic stem cells from the killing effect of chronic exposure to type I interferons. J Exp Med211: 245–262. doi: 10.1084/jem.2013104324493802
12. Schurch CM, Riether C, Ochsenbein AF, (2014) Cytotoxic CD8+ T cells stimulate hematopoietic progenitors by promoting cytokine release from bone marrow mesenchymal stromal cells. Cell Stem Cell14: 460–472. doi: 10.1016/j.stem.2014.01.00224561082
13. Guermonprez P, Helft J, Claser C, Deroubaix S, Karanje H, et al. (2013) Inflammatory Flt3l is essential to mobilize dendritic cells and for T cell responses during Plasmodium infection. Nat Med19: 730–738. doi: 10.1038/nm.319723685841
14. Hall AO, Silver JS, Hunter CA, (2012) The Immunobiology of IL-27. Adv Immunol115: 1–44. doi: 10.1016/B978-0-12-394299-9.00001-122608254
15. Mizoguchi I, Higuchi K, Mitobe K, Tsunoda R, Mizuguchi J, Yoshimoto T, Yoshimoto T, et al. (2013) Interleukin-27: Regulation of immune responses and disease development by a pleiotropic cytokine with pro- and anti-inflammatory properties. In: Cytokine frontiers: Regulation of immune responses in health and diseaseTokyo: Springer. pp. 353–375.
16. Yoshida H, Hunter CA, (2015) The immunobiology of interleukin-27. Annu Rev Immunol33: 417–443. doi: 10.1146/annurev-immunol-032414-11213425861977
17. Seita J, Asakawa M, Ooehara J, Takayanagi S, Morita Y, et al. (2008) Interleukin-27 directly induces differentiation in hematopoietic stem cells. Blood111: 1903–1912. 18042804
18. Osawa M, Hanada K, Hamada H, Nakauchi H, (1996) Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell. Science273: 242–245. 8662508
19. Yamamoto R, Morita Y, Ooehara J, Hamanaka S, Onodera M, et al. (2013) Clonal analysis unveils self-renewing lineage-restricted progenitors generated directly from hematopoietic stem cells. Cell154: 1112–1126. doi: 10.1016/j.cell.2013.08.00723993099
20. Kondo M, Weissman IL, Akashi K, (1997) Identification of clonogenic common lymphoid progenitors in mouse bone marrow. Cell91: 661–672. 9393859
21. Akashi K, Traver D, Miyamoto T, Weissman IL, (2000) A clonogenic common myeloid progenitor that gives rise to all myeloid lineages. Nature404: 193–197. 10724173
22. Onai N, Kurabayashi K, Hosoi-Amaike M, Toyama-Sorimachi N, Matsushima K, et al. (2013) A clonogenic progenitor with prominent plasmacytoid dendritic cell developmental potential. Immunity38: 943–957. doi: 10.1016/j.immuni.2013.04.00623623382
23. van de Laar L, Coffer PJ, Woltman AM, (2012) Regulation of dendritic cell development by GM-CSF: molecular control and implications for immune homeostasis and therapy. Blood119: 3383–3393. doi: 10.1182/blood-2011-11-37013022323450
24. Masuda K, Kubagawa H, Ikawa T, Chen CC, Kakugawa K, et al. (2005) Prethymic T-cell development defined by the expression of paired immunoglobulin-like receptors. EMBO J24: 4052–4060. 16292344
25. Rosenbauer F, Tenen DG, (2007) Transcription factors in myeloid development: balancing differentiation with transformation. Nat Rev Immunol7: 105–117. 17259967
26. Geissmann F, Manz MG, Jung S, Sieweke MH, Merad M, et al. (2010) Development of monocytes, macrophages, and dendritic cells. Science327: 656–661. doi: 10.1126/science.117833120133564
27. Belz GT, Nutt SL, (2012) Transcriptional programming of the dendritic cell network. Nat Rev Immunol12: 101–113. doi: 10.1038/nri314922273772
28. Medvedovic J, Ebert A, Tagoh H, Busslinger M, (2011) Pax5: a master regulator of B cell development and leukemogenesis. Adv Immunol111: 179–206. doi: 10.1016/B978-0-12-385991-4.00005-221970955
29. Kaneko H, Shimizu R, Yamamoto M, (2010) GATA factor switching during erythroid differentiation. Curr Opin Hematol17: 163–168. doi: 10.1097/MOH.0b013e32833800b820216212
30. Hirai H, Zhang P, Dayaram T, Hetherington CJ, Mizuno S, et al. (2006) C/EBPbeta is required for 'emergency' granulopoiesis. Nat Immunol7: 732–739. 16751774
31. Hirai H, Yokota A, Tamura A, Sato A, Maekawa T, (2015) Non-steady-state hematopoiesis regulated by the C/EBPbeta transcription factor. Cancer Sci.
32. Manz MG, Boettcher S, (2014) Emergency granulopoiesis. Nat Rev Immunol14: 302–314. doi: 10.1038/nri366024751955
33. Ronnstrand L, (2004) Signal transduction via the stem cell factor receptor/c-Kit. Cell Mol Life Sci61: 2535–2548. 15526160
34. Lee CK, Smith E, Gimeno R, Gertner R, Levy DE, (2000) STAT1 affects lymphocyte survival and proliferation partially independent of its role downstream of IFN-gamma. J Immunol164: 1286–1292. 10640742
35. Yoshimoto T, Yoneto T, Waki S, Nariuchi H, (1998) Interleukin-12-dependent mechanisms in the clearance of blood-stage murine malaria parasite Plasmodium berghei XAT, an attenuated variant of P. berghei NK65. J Infect Dis177: 1674–1681. 9607848
36. Yoneto T, Waki S, Takai T, Tagawa Y, Iwakura Y, et al. (2001) A critical role of Fc receptor-mediated antibody-dependent phagocytosis in the host resistance to blood-stage Plasmodium berghei XAT infection. J Immunol166: 6236–6241. 11342646
37. Belyaev NN, Biro J, Langhorne J, Potocnik AJ, (2013) Extramedullary myelopoiesis in malaria depends on mobilization of myeloid-restricted progenitors by IFN-gamma induced chemokines. PLoS Pathog9: e1003406. doi: 10.1371/journal.ppat.100340623762028
38. Yoneto T, Yoshimoto T, Wang CR, Takahama Y, Tsuji M, et al. (1999) Gamma interferon production is critical for protective immunity to infection with blood-stage Plasmodium berghei XAT but neither NO production nor NK cell activation is critical. Infect Immun67: 2349–2356. 10225894
39. Borner C, (2003) The Bcl-2 protein family: sensors and checkpoints for life-or-death decisions. Mol Immunol39: 615–647. 12493639
40. Chipuk JE, Moldoveanu T, Llambi F, Parsons MJ, Green DR, (2010) The BCL-2 family reunion. Mol Cell37: 299–310. doi: 10.1016/j.molcel.2010.01.02520159550
41. Cisse B, Caton ML, Lehner M, Maeda T, Scheu S, et al. (2008) Transcription factor E2-2 is an essential and specific regulator of plasmacytoid dendritic cell development. Cell135: 37–48. doi: 10.1016/j.cell.2008.09.01618854153
42. Liu Z, Liu JQ, Talebian F, Wu LC, Li S, et al. (2013) IL-27 enhances the survival of tumor antigen-specific CD8+ T cells and programs them into IL-10-producing, memory precursor-like effector cells. Eur J Immunol43: 468–479. doi: 10.1002/eji.20124293023225163
43. Waki S, (1994) Antibody-dependent neutrophil-mediated parasite killing in non-lethal rodent malaria. Parasite Immunol16: 587–591. 7532294
44. Nnalue NA, Friedman MJ, (1988) Evidence for a neutrophil-mediated protective response in malaria. Parasite Immunol10: 47–58. 3281102
45. Pierrot C, Adam E, Hot D, Lafitte S, Capron M, et al. (2007) Contribution of T cells and neutrophils in protection of young susceptible rats from fatal experimental malaria. J Immunol178: 1713–1722. 17237421
46. Yoshimoto T, Takahama Y, Wang CR, Yoneto T, Waki S, et al. (1998) A pathogenic role of IL-12 in blood-stage murine malaria lethal strain Plasmodium berghei NK65 infection. J Immunol160: 5500–5505. 9605153
47. Findlay EG, Greig R, Stumhofer JS, Hafalla JC, de Souza JB, et al. (2010) Essential role for IL-27 receptor signaling in prevention of Th1-mediated immunopathology during malaria infection. J Immunol185: 2482–2492. doi: 10.4049/jimmunol.090401920631310
48. Villegas-Mendez A, de Souza JB, Lavelle SW, Gwyer Findlay E, Shaw TN, et al. (2013) IL-27 receptor signalling restricts the formation of pathogenic, terminally differentiated Th1 cells during malaria infection by repressing IL-12 dependent signals. PLoS Pathog9: e1003293. doi: 10.1371/journal.ppat.100329323593003
49. Gwyer Findlay E, Villegas-Mendez A, de Souza JB, Inkson CA, Shaw TN, et al. (2013) IL-27 receptor signaling regulates CD4+ T cell chemotactic responses during infection. J Immunol190: 4553–4561. doi: 10.4049/jimmunol.120291623536628
50. Liu FD, Kenngott EE, Schroter MF, Kuhl A, Jennrich S, et al. (2014) Timed action of IL-27 protects from immunopathology while preserving defense in influenza. PLoS Pathog10: e1004110. doi: 10.1371/journal.ppat.100411024809349
51. Wirtz S, Tubbe I, Galle PR, Schild HJ, Birkenbach M, et al. (2006) Protection from lethal septic peritonitis by neutralizing the biological function of interleukin 27. J Exp Med203: 1875–1881. 16880260
52. Li JP, Wu H, Xing W, Yang SG, Lu SH, et al. (2010) Interleukin-27 as a negative regulator of human neutrophil function. Scand J Immunol72: 284–292. doi: 10.1111/j.1365-3083.2010.02422.x20883313
53. Liu J, Guan X, Ma X, (2007) Regulation of IL-27 p28 gene expression in macrophages through MyD88- and interferon-gamma-mediated pathways. J Exp Med204: 141–152. 17227910
54. Murugaiyan G, Mittal A, Weiner HL, (2010) Identification of an IL-27/osteopontin axis in dendritic cells and its modulation by IFN-gamma limits IL-17-mediated autoimmune inflammation. Proc Natl Acad Sci U S A107: 11495–11500. doi: 10.1073/pnas.100209910720534530
55. Murugaiyan G, Beynon V, Pires Da Cunha A, Joller N, Weiner HL, (2012) IFN-gamma limits Th9-mediated autoimmune inflammation through dendritic cell modulation of IL-27. J Immunol189: 5277–5283. doi: 10.4049/jimmunol.120080823125412
56. Tormo AJ, Beaupre LA, Elson G, Crabe S, Gauchat JF, (2013) A polyglutamic acid motif confers IL-27 hydroxyapatite and bone-binding properties. J Immunol190: 2931–2937. doi: 10.4049/jimmunol.120146023390294
57. Morrison SJ, Scadden DT, (2014) The bone marrow niche for haematopoietic stem cells. Nature505: 327–334. doi: 10.1038/nature1298424429631
58. Heinrich PC, Behrmann I, Haan S, Hermanns HM, Muller-Newen G, et al. (2003) Principles of interleukin (IL)-6-type cytokine signalling and its regulation. Biochem J374: 1–20. 12773095
59. Drucker C, Gewiese J, Malchow S, Scheller J, Rose-John S, (2010) Impact of interleukin-6 classic- and trans-signaling on liver damage and regeneration. J Autoimmun34: 29–37. doi: 10.1016/j.jaut.2009.08.00319717281
60. Wunderlich CM, Delic D, Behnke K, Meryk A, Strohle P, et al. (2012) Cutting edge: Inhibition of IL-6 trans-signaling protects from malaria-induced lethality in mice. J Immunol188: 4141–4144. doi: 10.4049/jimmunol.110213722467660
61. Okabe M, Ikawa M, Kominami K, Nakanishi T, Nishimune Y, (1997) 'Green mice' as a source of ubiquitous green cells. FEBS Lett407: 313–319. 9175875
62. Yoshida H, Hamano S, Senaldi G, Covey T, Faggioni R, et al. (2001) WSX-1 is required for the initiation of Th1 responses and resistance to L. major infection. Immunity15: 569–578. 11672539
63. Morishima N, Mizoguchi I, Takeda K, Mizuguchi J, Yoshimoto T, (2009) TGF-beta is necessary for induction of IL-23R and Th17 differentiation by IL-6 and IL-23. Biochem Biophys Res Commun386: 105–110. doi: 10.1016/j.bbrc.2009.05.14019501566
64. Yoshimoto T, Okada K, Morishima N, Kamiya S, Owaki T, et al. (2004) Induction of IgG2a class switching in B cells by IL-27. J Immunol173: 2479–2485. 15294962
65. Morita S, Kojima T, Kitamura T, (2000) Plat-E: an efficient and stable system for transient packaging of retroviruses. Gene Ther7: 1063–1066. 10871756