CoChat
Sign Up
Cited by 194Psoriasis: Treatment and PathogenesisT-cell and B-cell ImmunologyIL-33, ST2, and ILC Pathways

Heterogeneity of human effector CD4+ T cells

Open access
Annunziato, Francesco, Romagnani, Sergio·2009·Arthritis Research & Therapy
DOI 10.1186/ar2843PMC PMC3003504
Open this paper in CoChat — free accountOpen PDF

Abstract

For many years the heterogeneity of CD4+ T-helper (Th) cells has been limited to Th1 and Th2 cells, which have been considered not only to be responsible for different types of protective responses, but also for the pathogenesis of many disorders. Th1 cells are indeed protective against intracellular microbes and they are thought to play a pathogenic role in organ-specific autoimmune and other chronic inflammatory disorders. Th2 cells provide protection against helminths, but are also responsible for the pathogenesis of allergic diseases. The identification and cloning of new cytokines has allowed one to enlarge the series of functional subsets of CD4+ Th effector cells. In particular, CD4+ Th cells producing IL-17 and IL-22, named Th17, have been initially implicated in the pathogenesis of many chronic inflammatory disorders instead of Th1 cells. However, the more recent studies in both humans and mice suggest that Th17 cells exhibit a high plasticity toward Th1 cells and that both Th17 and Th1 cells may be pathogenic. More recently, another two subsets of effector CD4+ Th cells, named Th9 and Th22 cells, have been described, even if their pathophysiological meaning is still unclear. Despite the heterogeneity of CD4+ effector Th cells being higher than previously thought and some of their subsets exhibiting high plasticity, the Th1/Th2 paradigm still maintains a strong validity.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1186/ar2843

Cites

12 of 12 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Differences in the proportions of CD4+ effector memory T-cells producing combinations of TNF-a, IL-2 and IFN-g after TGN1412 stimulation may reflect the heterogeneous nature of this population, which contains multiple functional subsets with different cytokine repertoires.

    “Differences in the proportions of CD4 + effector memory T-cells producing TNF-a, IL-2 and IFN-g combinations following TGN1412 stimulation may reflect the heterogeneous nature of this population which contains multiple functional subsets with different cytokine repertoires (e.g.Th1, Th2, Th9, Th17 and Th22) (Annunziato and Romagnani, 2009;Sallusto and Lanzavecchia, 2009).”

    From Monoclonal antibody TGN1412 trial failure explained by species differences in CD28 expression on CD4 <sup>+</sup> effector memory T‐cells (2010) · cites this paper as Annunziato and Romagnani, 2009

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 77

  1. Parish CR Liew FY Immune response to chemically modified flagellin. 3. Enhanced cell-mediated immunity during high and low zone antibody tolerance to flagellin J Exp Med 1972 135 298 311 10.1084/jem.135.2.298 5060292 PMC2180527 · DOI
  2. Mosmann TR Cherwinski H Bond MW Giedlin MA Coffman RL 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 2419430
  3. Parronchi P Macchia D Piccinni MP Biswas P Simonelli C Maggi E Ricci M Ansari AA Romagnani S Allergen- and bacterial antigen-specific T-cell clones established from atopic donors show a different profile of cytokine production Proc Natl Acad Sci USA 1991 88 4538 4542 10.1073/pnas.88.10.4538 1827920 PMC51696 · DOI
  4. Del Prete GF De Carli M Mastromauro C Biagiotti R Macchia D Falagiani P Ricci M Romagnani S Purified protein derivative of Mycobacterium tuberculosis and excretory-secretory antigen(s) of Toxocara canis expand in vitro human T cells with stable and opposite (type 1 T helper or type 2 T helper) profile of cytokine production J Clin Invest 1991 88 346 350 10.1172/JCI115300 1829097 PMC296040 · DOI
  5. Romagnani S Biology of human TH1 and TH2 cells [review] J Clin Immunol 1995 15 121 129 10.1007/BF01543103 7559914 · DOI
  6. Kopf M Le Gros G Bachmann M Lamers MC Bluethmann H Kohler G Disruption of the murine IL-4 gene blocks Th2 cytokine responses Nature 1993 362 245 248 10.1038/362245a0 8384701 · DOI
  7. Coffman RL Seymour BW Hudak S Jackson J Rennick D Antibody to interleukin-5 inhibits helminth-induced eosinophilia in mice Science 1989 245 308 310 10.1126/science.2787531 2787531 · DOI
  8. Faulkner H Renauld J Van Snick J Grencis RK Interleukin-9 enhances resistance to the intestinal nematode Trichuris muris Infect Immun 1998 66 3832 3840 9673269 PMC108429
  9. Longphre M Li D Gallup M Drori E Ordoñez CL Redman T Wenzel S Bice DE Fahy JV Basbaum C Allergen-induced IL-9 directly stimulates mucin transcription in respiratory epithelial cells J Clin Invest 1999 104 1375 1382 10.1172/JCI6097 10562299 PMC409835 · DOI
  10. Manetti R Parronchi P Giudizi MG Piccinni MP Maggi E Trinchieri G Romagnani S Natural killer cell stimulatory factor (interleukin 12 [IL-12]) induces T helper type 1 (Th1)-specific immune responses and inhibits the development of IL-4-producing Th cells J Exp Med 1993 177 1199 1204 10.1084/jem.177.4.1199 8096238 PMC2190961 · DOI
  11. Manetti R Annunziato F Tomasevic L Giannò V Parronchi P Romagnani S Maggi E Polyinosinic acid: polycytidylic acid promotes T helper type 1-specific immune responses by stimulating macrophage production of interferon-alpha and interleukin-12 Eur J Immunol 1995 25 2656 2660 10.1002/eji.1830250938 7589141 · DOI
  12. Parronchi P De Carli M Manetti R Simonelli C Sampognaro S Piccinni MP Macchia D Maggi E Del Prete G Romagnani S IL-4 and IFN (alpha and gamma) exert opposite regulatory effects on the development of cytolytic potential by Th1 or Th2 human T cell clones J Immunol 1992 149 2977 2983 1401925
  13. Romagnani S Induction of TH1 and TH2 responses: a key role for the 'natural' immune response? Immunol Today 1992 13 379 381 10.1016/0167-5699(92)90083-J 1418371 · DOI
  14. Akira S Takeda K Kaisho T Toll-like receptors: critical proteins linking innate and acquired immunity Nat Immunol 2001 2 675 680 10.1038/90609 11477402 · DOI · Paper page
  15. Szabo SJ Dighe AS Gubler U Murphy KM Regulation of the interleukin (IL)-12Rβ2 subunit expression in developing T helper 1 (Th1) and Th2 cells J Exp Med 1997 185 817 824 10.1084/jem.185.5.817 9120387 PMC2196166 · DOI
  16. Afkarian M Sedy JR Yang J Jacobson NG Cereb N Yang SY Murphy TL Murphy KM T-bet is a STAT1-induced regulator of IL-12R expression in naïve CD4+ T cells Nat Immunol 2002 3 549 557 10.1038/ni794 12006974 · DOI
  17. Murphy KM Reiner SL The lineage decisions of helper T cells Nat Rev Immunol 2002 2 933 944 10.1038/nri954 12461566 · DOI
  18. Hibbert L Pflanz S De Waal Malefyt R Kastelein RA IL-27 and IFN-α signal via Stat1 and Stat3 and induce T-Bet and IL-12Rβ2 in naive T cells J Interferon Cytokine Res 2003 23 513 522 10.1089/10799900360708632 14565860 · DOI
  19. Smeltz RB Chen J Ehrhardt R Shevach EM Role of IFN-gamma in Th1 differentiation: IFN-gamma regulates IL-18R alpha expression by preventing the negative effects of IL-4 and by inducing/maintaining IL-12 receptor beta 2 expression J Immunol 2002 168 6165 6172 12055229
  20. Okazawa A Kanai T Watanabe M Yamazaki M Inoue N Ikeda M Kurimoto M Ishii H Hibi T Th1-mediated intestinal inflammation in Crohn's disease may be induced by activation of lamina propria lymphocytes through synergistic stimulation of interleukin-12 and interleukin-18 without T cell receptor engagement Am J Gastroenterol 2002 97 3108 3117 10.1111/j.1572-0241.2002.07107.x 12492197 · DOI
  21. Amsen D Blander JM Lee GR Tanigaki K Honjo T Flavell RA Instruction of distinct CD4 T helper cell fates by different notch ligands on antigen-presenting cells Cell 2004 117 515 526 10.1016/S0092-8674(04)00451-9 15137944 · DOI
  22. Liotta F Frosali F Querci V Mantei A Filì L Maggi L Mazzinghi B Angeli R Ronconi E Santarlasci V Biagioli T Lasagni L Ballerini C Parronchi P Scheffold A Cosmi L Maggi E Romagnani S Annunziato F Human immature myeloid dendritic cells trigger a TH2-polarizing program via Jagged-1/Notch interaction J Allergy Clin Immunol 2008 121 1000 1005 10.1016/j.jaci.2008.01.004 18313135 · DOI
  23. Owyang AM Zaph C Wilson EH Guild KJ McClanahan T Miller HR Cua DJ Goldschmidt M Hunter CA Kastelein RA Artis D Interleukin 25 regulates type 2 cytokine-dependent immunity and limits chronic inflammation in the gastrointestinal tract J Exp Med 2006 203 843 849 10.1084/jem.20051496 16606667 PMC1800834 · DOI · Paper page
  24. Fallon PG Ballantyne SJ Mangan NE Barlow JL Dasvarma A Hewett DR McIlgorm A Jolin HE McKenzie AN Identification of an interleukin (IL)-25-dependent cell population that provides IL-4, IL-5, and IL-13 at the onset of helminth expulsion J Exp Med 2006 203 1105 1116 10.1084/jem.20051615 16606668 PMC2118283 · DOI
  25. Kurata H Lee HJ O'Garra A Arai N Ectopic expression of activated Stat6 induces the expression of Th2-specific cytokines and transcription factors in developing Th1 cells Immunity 1999 11 677 688 10.1016/S1074-7613(00)80142-9 10626890 · DOI
  26. Zhu J Guo L Watson CJ Hu-Li J Paul WE Stat6 is necessary and sufficient for IL-4's role in Th2 differentiation and cell expansion J Immunol 2001 166 7276 7281 11390477
  27. Zhu J Min B Hu-Li J Watson CJ Grinberg A Wang Q Killeen N Urban JF Jr Guo L Paul WE Conditional deletion of Gata3 shows its essential function in T(H)1-T(H)2 responses Nat Immunol 2004 5 1157 1165 10.1038/ni1128 15475959 · DOI
  28. Pai SY Truitt ML Ho IC GATA-3 deficiency abrogates the development and maintenance of T helper type 2 cells Proc Natl Acad Sci USA 2004 101 1993 1998 10.1073/pnas.0308697100 14769923 PMC357040 · DOI
  29. Kim JI Ho IC Grusby MJ Glimcher LH The transcription factor c-Maf controls the production of interleukin-4 but not other Th2 cytokines Immunity 1999 10 745 751 10.1016/S1074-7613(00)80073-4 10403649 · DOI
  30. Ouyang W Löhning M Gao Z Assenmacher M Ranganath S Radbruch A Murphy KM Stat6-independent GATA-3 auto-activation directs IL-4-independent Th2 development and commitment Immunity 2000 12 27 37 10.1016/S1074-7613(00)80156-9 10661403 · DOI
  31. Zhu J Cote-Sierra J Guo L Paul WE Stat5 activation plays a critical role in Th2 differentiation Immunity 2003 19 739 748 10.1016/S1074-7613(03)00292-9 14614860 · DOI
  32. Zhu J Yamane H Cote-Sierra J Guo L Paul WE GATA-3 promotes Th2 responses through three different mechanisms: induction of Th2 cytokine production, selective growth of Th2 cells and inhibition of Th1 cell-specific factors Cell Res 2006 16 3 10 10.1038/sj.cr.7310002 16467870 · DOI
  33. Usui T Nishikomori R Kitani A Strober W GATA-3 suppresses Th1 development by downregulation of Stat4 and not through effects on IL-12Rβ2 chain or T-bet Immunity 2003 18 415 428 10.1016/S1074-7613(03)00057-8 12648458 · DOI
  34. Usui T Preiss JC Kanno Y Yao ZJ Bream JH O'Shea JJ Strober W T-bet regulates Th1 responses through essential effects on GATA-3 function rather than on IFNG gene acetylation and transcription J Exp Med 2006 203 755 766 10.1084/jem.20052165 16520391 PMC2118252 · DOI
  35. Mosmann TR Sad S The expanding universe of T-cell subsets: Th1, Th2 and more Immunol Today 1996 17 138 146 10.1016/0167-5699(96)80606-2 8820272 · DOI
  36. Romagnani S The Th1/Th2 paradigm Immunol Today 1997 18 263 266 10.1016/S0167-5699(97)80019-9 9190109 · DOI
  37. Romagnani S The role of lymphocytes in allergic disease J Allergy Clin Immunol 2000 105 399 408 10.1067/mai.2000.104575 10719286 · DOI
  38. Oppmann B Lesley R Blom B Timans JC Xu Y Hunte B Vega F Yu N Wang J Singh K Zonin F Vaisberg E Churakova T Liu M Gorman D Wagner J Zurawski S Liu Y Abrams JS Moore KW Rennick D de Waal-Malefyt R Hannum C Bazan JF Kastelein RA 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 10.1016/S1074-7613(00)00070-4 11114383 · DOI
  39. Gately MK Renzetti LM Magram J Stern AS Adorini L Gubler U Presky DH The interleukin-12/interleukin-12-receptor system: role in normal and pathologic immune responses Annu Rev Immunol 1998 16 495 521 10.1146/annurev.immunol.16.1.495 9597139 · DOI
  40. Krakowski M Owens T Interferon-gamma confers resistance to experimental allergic encephalomyelitis Eur J Immunol 1996 26 1641 1646 10.1002/eji.1830260735 8766573 · DOI
  41. Willenborg DO Fordham S Bernard CC Cowden WB Ramshaw IA IFN-gamma plays a critical down-regulatory role in the induction and effector phase of myelin oligodendrocyte glycoprotein-induced autoimmune encephalomyelitis J Immunol 1996 157 3223 3227 8871615
  42. Willenborg DO Fordham SA Staykova MA Ramshaw IA Cowden WB IFN-gamma is critical to the control of murine autoimmune encephalomyelitis and regulates both in the periphery and in the target tissue: a possible role for nitric oxide J Immunol 1999 163 5278 5286 10553050
  43. McGeachy MJ Chen Y Tato CM Laurence A Joyce-Shaikh B Blumenschein WM McClanahan TK O'Shea JJ Cua DJ The interleukin 23 receptor is essential for the terminal differentiation of interleukin 17-producing effector T helper cells in vivo Nat Immunol 2009 10 314 324 10.1038/ni.1698 19182808 PMC2945605 · DOI · Paper page
  44. Mangan PR Harrington LE O'Quinn DB Helms WS Bullard DC Elson CO Hatton RD Wahl SM Schoeb TR Weaver CT Transforming growth factor-beta induces development of the T(H)17 lineage Nature 2006 441 231 234 10.1038/nature04754 16648837 · DOI · Paper page
  45. Yang XO Pappu BP Nurieva R Akimzhanov A Kang HS Chung Y Ma L Shah B Panopoulos AD Schluns KS Watowich SS Tian Q Jetten AM Dong C T helper 17 lineage differentiation is programmed by orphan nuclear receptors ROR alpha and ROR gamma Immunity 2008 28 29 39 10.1016/j.immuni.2007.11.016 18164222 PMC2587175 · DOI · Paper page
  46. Chen Z Laurence A O'Shea JJ Signal transduction pathways and transcriptional regulation in the control of Th17 differentiation Semin Immunol 2007 19 400 408 10.1016/j.smim.2007.10.015 18166487 PMC2323678 · DOI · Paper page
  47. Ouyang W Koli JK Zheng Y The biological functions of T helper 17 cell effector cytokines in inflammation Immunity 2008 28 454 467 10.1016/j.immuni.2008.03.004 18400188 PMC3424508 · DOI
  48. Dubin PJ Kolls JK Th17 cytokines and mucosal immunity Immunol Rev 2008 226 160 171 10.1111/j.1600-065X.2008.00703.x 19161423 · DOI
  49. Fouser LA Wright JF Dunussi-Joannopoulos K Collins M Th17 cytokines and their emerging roles in inflammation and autoimmunity Immunol Rev 2008 226 87 102 10.1111/j.1600-065X.2008.00712.x 19161418 · DOI
  50. van Beelen AJ Teunissen MB Kapsenberg ML de Jong EC Interleukin-17 in inflammatory skin disorders Curr Opin Allergy Clin Immunol 2007 7 374 381 10.1097/ACI.0b013e3282ef869e 17873575 · DOI
  51. Chen Z O'Shea JJ Th17 cells: a new fate for differentiating helper T cells Immunol Res 2008 41 87 102 10.1007/s12026-007-8014-9 18172584 · DOI
  52. Cosmi L De Palma R Santarlasci V Maggi L Capone M Frosali F Rodolico G Querci V Abbate G Angeli R Berrino L Fambrini M Caproni M Tonelli F Lazzeri E Parronchi P Liotta F Maggi E Romagnani S Annunziato F Human interleukin 17-producing cells originate from a CD161+CD4+ T cell precursor J Exp Med 2008 205 1903 1916 10.1084/jem.20080397 18663128 PMC2525581 · DOI
  53. Lanier LL Chang C Philips JH Human NKR-P1A. A disulphide-linked homodimer of the C-type lectin superfamily expressed by a subset of NK and T lymphocytes J Immunol 1994 153 2417 2428 8077657
  54. Acosta-Rodriguez EV Rivino L Geginat J Jarrossay D Gattorno M Lanzavecchia A Sallusto F Napolitani G Surface phenotype and antigenic specificity of human interleukin 17-producing T helper memory cells Nat Immunol 2007 8 639 646 10.1038/ni1467 17486092 · DOI · Paper page
  55. Annunziato F Cosmi L Santarlasci V Maggi L Liotta F Mazzinghi B Parente E Filì L Ferri S Frosali F Giudici F Romagnani P Parronchi P Tonelli F Maggi E Romagnani S Phenotypic and functional features of human Th17 cells J Exp Med 2007 204 1849 1861 10.1084/jem.20070663 17635957 PMC2118657 · DOI · Paper page
  56. Wilson NJ Boniface K Chan JR McKenzie BS Blumenschein WM Mattson JD Basham B Smith K Chen T Morel F Lecron JC Kastelein RA Cua DJ McClanahan TK Bowman EP de Waal Malefyt R Development, cytokine profile and function of human interleukin 17-producing helper T cells Nat Immunol 2007 8 950 957 10.1038/ni1497 17676044 · DOI · Paper page
  57. Chen Z Tato CM Muul L Laurence A O'Shea JJ Distinct regulation of interleukin-17 in human T helper lymphocytes Arthritis Rheum 2007 56 2936 2946 10.1002/art.22866 17763419 PMC2323677 · DOI
  58. Manel N Unutmaz D Littman DR The differentiation of human Th17 cells requires transforming growth factor-β and induction of the nuclear receptor RORγt Nat Immunol 2008 9 641 649 10.1038/ni.1610 18454151 PMC2597394 · DOI
  59. Yang L Anderson DE Baecher-Allan C Hastings WD Bettelli E Oukka M Kuchroo VK Hafler DA IL-21 and TGF-β are required for differentiation of human T(H)17 cells Nature 2008 454 350 352 10.1038/nature07021 18469800 PMC2760130 · DOI
  60. Santarlasci V Maggi L Capone M Frosali F Querci V De Palma R Liotta F Cosmi L Maggi E Romagnani S Annunziato F TGF-beta indirectly favors the development of human Th17 cells by inhibiting Th1 cells Eur J Immunol 2009 39 207 215 10.1002/eji.200838748 19130583 · DOI
  61. Kleinschek MA Boniface K Sadekova S Grein J Murphy EE Turner SP Raskin L Desai B Faubion WA de Waal Malefyt R Pierce RH McClanahan T Kastelein RA Circulating and gut-resident human Th17 cells express CD161 and promote intestinal inflammation J Exp Med 2009 206 525 534 10.1084/jem.20081712 19273624 PMC2699125 · DOI · Paper page
  62. Boniface K Bak-Jensen KS Li Y Blumenschein WM McGeachy MJ McClanahan TK McKenzie BS Kastelein RA Cua DJ de Waal Malefyt R Prostaglandin E2 regulates Th17 cell differentiation and function through cyclic AMP and EP2/EP4 receptor signaling J Exp Med 2009 206 535 548 10.1084/jem.20082293 19273625 PMC2699124 · DOI
  63. Napolitani G Acosta-Rodriguez EV Lanzavecchia A Sallusto F Prostaglandin E2 enhances Th17 responses via modulation of IL-17 and IFN-gamma production by memory CD4+ T cells Eur J Immunol 2009 39 1301 1312 10.1002/eji.200838969 19384872 · DOI
  64. Chung Y Chang SH Martinez GJ Yang XO Nurieva R Kang HS Ma L Watowich SS Jetten AM Tian Q Dong C Critical regulation of early Th17 cell differentiation by interleukin-1 signaling Immunity 2009 30 576 587 10.1016/j.immuni.2009.02.007 19362022 PMC2705871 · DOI
  65. Koenen HJ Smeets RL Vink PM van Rijssen E Boots AM Joosten I Human CD25highFoxp3pos regulatory T cells differentiate into IL-17-producing cells Blood 2008 112 2340 2352 10.1182/blood-2008-01-133967 18617638 · DOI
  66. Deknuydt F Bioley G Valmori D Ayyoub M IL-1β and IL-2 convert human Treg into T(H)17 cells Clin Immunol 2009 131 298 307 10.1016/j.clim.2008.12.008 19211307 · DOI
  67. Beriou G Costantino CM Ashley CW Yang L Kuchroo VK Baecher-Allan C Hafler DA IL-17-producing human peripheral regulatory T cells retain suppressive function Blood 2009 113 4240 4249 10.1182/blood-2008-10-183251 19171879 PMC2676084 · DOI
  68. Voo KS Wang YH Santori FR Boggiano C Wang YH Arima K Bover L Hanabuchi S Khalili J Marinova E Zheng B Littman DR Liu YJ Identification of IL-17-producing FOXP3+ regulatory T cells in humans Proc Natl Acad Sci USA 2009 106 4793 4798 10.1073/pnas.0900408106 19273860 PMC2653560 · DOI
  69. Wei G Wei L Zhu J Zang C Hu-Li J Yao Z Cui K Kanno Y Roh TY Watford WT Schones DE Peng W Sun HW Paul WE O'Shea JJ Zhao K Global mapping of H3K4me3 and H3K27me3 reveals specificity and plasticity in lineage fate determination of differentiating CD4+T cells Immunity 2009 30 155 167 10.1016/j.immuni.2008.12.009 19144320 PMC2722509 · DOI · Paper page
  70. Martin-Orozco N Chung Y Chang SH Wang YH Dong C Th17 cells promote pancreatic inflammation but only induce diabetes efficiently in lymphopenic hosts after conversion into Th1 cells Eur J Immunol 2009 39 216 224 10.1002/eji.200838475 19130584 PMC2755057 · DOI
  71. Bending D De La Peña H Veldhoen M Phillips JM Uyttenhove C Stockinger B Cooke A Highly purified Th17 cells from BDC2.5NOD mice convert into Th1-like cells in NOD/SCID recipient mice J Clin Invest 2009 in press 19188681 PMC2648686
  72. Veldhoen M Uyttenhove C van Snick J Helmby H Westendorf A Buer J Martin B Wilhelm C Stockinger B Transforming growth factor-beta 'reprograms' the differentiation of T helper 2 cells and promotes an interleukin 9-producing subset Nat Immunol 2008 9 1341 1346 10.1038/ni.1659 18931678 · DOI · Paper page
  73. Gessner A Blum H Röllinghoff M Differential regulation of IL-9-expression after infection with Leishmania major in susceptible and resistant mice Immunobiology 1993 189 419 435 8125519
  74. Louahed J Toda M Jen J Hamid Q Renauld JC Levitt RC Nicolaides NC Interleukin-9 upregulates mucus expression in the airways Am J Respir Cell Mol Biol 2000 22 649 656 10837360
  75. Wu B Huang C Kato-Maeda M Hopewell PC Daley CL Krensky AM Clayberger C IL-9 is associated with an impaired Th1 immune response in patients with tuberculosis Clin Immunol 2008 126 202 210 10.1016/j.clim.2007.09.009 18032114 · DOI
  76. Nowak EC Weaver CT Turner H Begum-Haque S Becher B Schreiner B Coyle AJ Kasper LH Noelle RJ IL-9 as a mediator of Th17-driven inflammatory disease J Exp Med 2009 206 1653 1660 10.1084/jem.20090246 19596803 PMC2722185 · DOI · Paper page
  77. Elyaman W Bradshaw EM Uyttenhove C Dardalhon V Awasthi A Imitola J Bettelli E Oukka M van Snick J Renauld JC Kuchroo VK Khoury SJ IL-9 induces differentiation of TH17 cells and enhances function of FoxP3+ natural regulatory T cells Proc Natl Acad Sci USA 2009 106 12885 12890 10.1073/pnas.0812530106 19433802 PMC2722314 · DOI · Paper page

Cited by

Sorted by citations

Authors
Annunziato, F., & Romagnani, S.
Affiliations
University of Florence (IT)
Corresponding author
Romagnani, Sergio
ORCID
Annunziato, Francesco
Venue
Arthritis Research & Therapy
Publisher
Springer Science and Business Media LLC
Published
2009
Volume
11
Issue
6
Pages
257
ISSN
1478-6354 (ISSN-L)
DOI
10.1186/ar2843
PMC
PMC3003504
OpenAlex
W2008783725
Cited by
194
References
12
Citations by year
2026: 2 · 2025: 4 · 2024: 2 · 2023: 4 · 2022: 9 · 2021: 10 · 2020: 9 · 2019: 14 · 2018: 11 · 2017: 9 · 2016: 11 · 2015: 10 · 2014: 28 · 2013: 17 · 2012: 27
FWCI
1.41
Type
journal article
Language
en
Open access
Locations
  • Arthritis Research & Therapy (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • Florence Research (University of Florence) (submittedVersion, other-oa)
Funders
  • European Commission (LSHB-CT-2005-518167)
  • Associazione Italiana per la Ricerca sul Cancro
Topics
  • Life Sciences › Immunology and Microbiology › Immunology › Psoriasis: Treatment and Pathogenesis
  • Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
  • Life Sciences › Immunology and Microbiology › Immunology › IL-33, ST2, and ILC Pathways
Keywords
CD4+ T cells, Th1 cells, Th2 cells, Th17 cells, Th9 cells, Th22 cells, IL-17, IL-22, T cell plasticity, chronic inflammatory diseases, autoimmune disease, allergic diseases, Th1/Th2 paradigm
MeSH terms
Animals, Humans, CD4-Positive T-Lymphocytes, T-Lymphocyte Subsets, Mice

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review