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PMID: 23420878 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Innate lymphoid type 2 cells sustain visceral adipose tissue eosinophils and alternatively activated macrophages.

The Journal of experimental medicine ·Vol. 210 ·No. 3 ·2013-03-11 ·Pages 535-49

Molofsky AB, Nussbaum JC, Liang HE, Van Dyken SJ, Cheng LE, Mohapatra A, Chawla A, Locksley RM

Abstract

Eosinophils in visceral adipose tissue (VAT) have been implicated in metabolic homeostasis and the maintenance of alternatively activated macrophages (AAMs). The absence of eosinophils can lead to adiposity and systemic insulin resistance in experimental animals, but what maintains eosinophils in adipose tissue is unknown. We show that interleukin-5 (IL-5) deficiency profoundly impairs VAT eosinophil accumulation and results in increased adiposity and insulin resistance when animals are placed on a high-fat diet. Innate lymphoid type 2 cells (ILC2s) are resident in VAT and are the major source of IL-5 and IL-13, which promote the accumulation of eosinophils and AAM. Deletion of ILC2s causes significant reductions in VAT eosinophils and AAMs, and also impairs the expansion of VAT eosinophils after infection with Nippostrongylus brasiliensis, an intestinal parasite associated with increased adipose ILC2 cytokine production and enhanced insulin sensitivity. Further, IL-33, a cytokine previously shown to promote cytokine production by ILC2s, leads to rapid ILC2-dependent increases in VAT eosinophils and AAMs. Thus, ILC2s are resident in VAT and promote eosinophils and AAM implicated in metabolic homeostasis, and this axis is enhanced during Th2-associated immune stimulation.

MeSH Terms
Animals Eosinophils/physiology Helminthiasis/immunology Immunity, Innate Insulin Resistance Interleukin-13/physiology Interleukin-33 Interleukin-5/physiology Interleukins/pharmacology Intestinal Diseases, Parasitic/immunology Intra-Abdominal Fat/cytology Lymphocyte Activation Macrophage Activation Macrophages/physiology Mice Mice, Inbred BALB C Mice, Inbred C57BL T-Lymphocytes, Helper-Inducer/immunology
Chemicals
IL33 protein, human Interleukin-13 Interleukin-33 Interleukin-5 Interleukins
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Molofsky Ari B
Howard Hughes Medical Institute, University of California, San Francisco, San Francisco 94143, USA.
Nussbaum Jesse C
Liang Hong-Erh
Van Dyken Steven J
Cheng Laurence E
Mohapatra Alexander
Chawla Ajay
Locksley Richard M
References (55)
55 references, click to expand
  1. Fundamental signals that regulate eosinophil homing to the gastrointestinal tract.
    J Clin Invest. 1999 Jun;103(12):1719-27 PMID: 10377178
  2. Adipose tissue invariant NKT cells protect against diet-induced obesity and metabolic disorder through regulatory cytokine production.
    Immunity. 2012 Sep 21;37(3):574-87 PMID: 22981538
  3. Identification of innate IL-5-producing cells and their role in lung eosinophil regulation and antitumor immunity.
    J Immunol. 2012 Jan 15;188(2):703-13 PMID: 22174445
  4. Systemically dispersed innate IL-13-expressing cells in type 2 immunity.
    Proc Natl Acad Sci U S A. 2010 Jun 22;107(25):11489-94 PMID: 20534524
  5. IL-4/STAT6 immune axis regulates peripheral nutrient metabolism and insulin sensitivity.
    Proc Natl Acad Sci U S A. 2010 Dec 28;107(52):22617-22 PMID: 21149710
  6. IL-33 expands suppressive CD11b+ Gr-1(int) and regulatory T cells, including ST2L+ Foxp3+ cells, and mediates regulatory T cell-dependent promotion of cardiac allograft survival.
    J Immunol. 2011 Nov 1;187(9):4598-610 PMID: 21949025
  7. Macrophage-mediated inflammation in metabolic disease.
    Nat Rev Immunol. 2011 Oct 10;11(11):738-49 PMID: 21984069
  8. Innate lymphoid cells mediate influenza-induced airway hyper-reactivity independently of adaptive immunity.
    Nat Immunol. 2011 May 29;12(7):631-8 PMID: 21623379
  9. Short term high fat diet challenge promotes alternative macrophage polarization in adipose tissue via natural killer T cells and interleukin-4.
    J Biol Chem. 2012 Jul 13;287(29):24378-86 PMID: 22645141
  10. IL-5-deficient mice have a developmental defect in CD5+ B-1 cells and lack eosinophilia but have normal antibody and cytotoxic T cell responses.
    Immunity. 1996 Jan;4(1):15-24 PMID: 8574848
  11. A two-step process for cytokine production revealed by IL-4 dual-reporter mice.
    Immunity. 2005 Oct;23(4):419-29 PMID: 16226507
  12. Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity.
    Nature. 2010 Apr 29;464(7293):1367-70 PMID: 20200518
  13. Lean, but not obese, fat is enriched for a unique population of regulatory T cells that affect metabolic parameters.
    Nat Med. 2009 Aug;15(8):930-9 PMID: 19633656
  14. Pulmonary innate lymphoid cells are major producers of IL-5 and IL-13 in murine models of allergic asthma.
    Eur J Immunol. 2012 May;42(5):1106-16 PMID: 22539286
  15. Interleukin-33 prolongs allograft survival during chronic cardiac rejection.
    Transpl Int. 2011 Oct;24(10):1027-39 PMID: 21797940
  16. The expanding family of innate lymphoid cells: regulators and effectors of immunity and tissue remodeling.
    Nat Immunol. 2011 Jan;12(1):21-7 PMID: 21113163
  17. Severe obesity increases adipose tissue expression of interleukin-33 and its receptor ST2, both predominantly detectable in endothelial cells of human adipose tissue.
    Int J Obes (Lond). 2013 May;37(5):658-65 PMID: 22828942
  18. Early lymphocyte expansion is severely impaired in interleukin 7 receptor-deficient mice.
    J Exp Med. 1994 Nov 1;180(5):1955-60 PMID: 7964471
  19. Biology of the eosinophil.
    Adv Immunol. 2009;101:81-121 PMID: 19231593
  20. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain.
    Nat Neurosci. 2010 Jan;13(1):133-40 PMID: 20023653
  21. Human IL-25- and IL-33-responsive type 2 innate lymphoid cells are defined by expression of CRTH2 and CD161.
    Nat Immunol. 2011 Sep 11;12(11):1055-62 PMID: 21909091
  22. Stat6 is required for mediating responses to IL-4 and for development of Th2 cells.
    Immunity. 1996 Mar;4(3):313-9 PMID: 8624821
  23. Innate lymphoid cells promote lung-tissue homeostasis after infection with influenza virus.
    Nat Immunol. 2011 Nov;12(11):1045-54 PMID: 21946417
  24. Interleukin-33 induces protective effects in adipose tissue inflammation during obesity in mice.
    Circ Res. 2010 Sep 3;107(5):650-8 PMID: 20634488
  25. Lung natural helper cells are a critical source of Th2 cell-type cytokines in protease allergen-induced airway inflammation.
    Immunity. 2012 Mar 23;36(3):451-63 PMID: 22425247
  26. The eosinophil.
    Annu Rev Immunol. 2006;24:147-74 PMID: 16551246
  27. Activation of natural killer T cells promotes M2 Macrophage polarization in adipose tissue and improves systemic glucose tolerance via interleukin-4 (IL-4)/STAT6 protein signaling axis in obesity.
    J Biol Chem. 2012 Apr 20;287(17):13561-71 PMID: 22396530
  28. Alternative activation of macrophages: an immunologic functional perspective.
    Annu Rev Immunol. 2009;27:451-83 PMID: 19105661
  29. Targeted deletion of a high-affinity GATA-binding site in the GATA-1 promoter leads to selective loss of the eosinophil lineage in vivo.
    J Exp Med. 2002 Jun 3;195(11):1387-95 PMID: 12045237
  30. Homeostasis and effector function of lymphopenia-induced "memory-like" T cells in constitutively T cell-depleted mice.
    J Immunol. 2008 Apr 1;180(7):4742-53 PMID: 18354198
  31. Type 2 immunity is controlled by IL-4/IL-13 expression in hematopoietic non-eosinophil cells of the innate immune system.
    J Exp Med. 2006 Jun 12;203(6):1435-46 PMID: 16702603
  32. Adipocyte-derived Th2 cytokines and myeloid PPARdelta regulate macrophage polarization and insulin sensitivity.
    Cell Metab. 2008 Jun;7(6):485-95 PMID: 18522830
  33. Alternatively activated macrophages produce catecholamines to sustain adaptive thermogenesis.
    Nature. 2011 Nov 20;480(7375):104-8 PMID: 22101429
  34. IL-25 induces IL-4, IL-5, and IL-13 and Th2-associated pathologies in vivo.
    Immunity. 2001 Dec;15(6):985-95 PMID: 11754819
  35. Simultaneous disruption of interleukin (IL)-4 and IL-13 defines individual roles in T helper cell type 2-mediated responses.
    J Exp Med. 1999 May 17;189(10):1565-72 PMID: 10330435
  36. RAG-1-deficient mice have no mature B and T lymphocytes.
    Cell. 1992 Mar 6;68(5):869-77 PMID: 1547488
  37. The transcription factor GATA-3 controls cell fate and maintenance of type 2 innate lymphoid cells.
    Immunity. 2012 Oct 19;37(4):634-48 PMID: 23063333
  38. New IL-17 family members promote Th1 or Th2 responses in the lung: in vivo function of the novel cytokine IL-25.
    J Immunol. 2002 Jul 1;169(1):443-53 PMID: 12077275
  39. Eosinophils develop in distinct stages and are recruited to peripheral sites by alternatively activated macrophages.
    J Leukoc Biol. 2007 Jun;81(6):1434-44 PMID: 17339609
  40. Chitin induces accumulation in tissue of innate immune cells associated with allergy.
    Nature. 2007 May 3;447(7140):92-6 PMID: 17450126
  41. Adipose tissue-resident immune cells: key players in immunometabolism.
    Trends Endocrinol Metab. 2012 Aug;23(8):407-15 PMID: 22795937
  42. Eotaxin and obesity.
    J Clin Endocrinol Metab. 2006 Jan;91(1):256-61 PMID: 16263831
  43. Analysis of type 2 immunity in vivo with a bicistronic IL-4 reporter.
    Immunity. 2001 Aug;15(2):303-11 PMID: 11520464
  44. Innate production of T(H)2 cytokines by adipose tissue-associated c-Kit(+)Sca-1(+) lymphoid cells.
    Nature. 2010 Jan 28;463(7280):540-4 PMID: 20023630
  45. Divergent expression patterns of IL-4 and IL-13 define unique functions in allergic immunity.
    Nat Immunol. 2011 Dec 04;13(1):58-66 PMID: 22138715
  46. An essential role for TH2-type responses in limiting acute tissue damage during experimental helminth infection.
    Nat Med. 2012 Jan 15;18(2):260-6 PMID: 22245779
  47. Eosinophils sustain adipose alternatively activated macrophages associated with glucose homeostasis.
    Science. 2011 Apr 8;332(6026):243-7 PMID: 21436399
  48. The absence of interleukin 1 receptor-related T1/ST2 does not affect T helper cell type 2 development and its effector function.
    J Exp Med. 1999 Nov 15;190(10):1541-8 PMID: 10562328
  49. Interleukin 5 deficiency abolishes eosinophilia, airways hyperreactivity, and lung damage in a mouse asthma model.
    J Exp Med. 1996 Jan 1;183(1):195-201 PMID: 8551223
  50. Thymic stromal lymphopoietin: an immune cytokine gene associated with the metabolic syndrome and blood pressure in severe obesity.
    Clin Sci (Lond). 2012 Jul;123(2):99-109 PMID: 22304237
  51. IL-33-responsive lineage- CD25+ CD44(hi) lymphoid cells mediate innate type 2 immunity and allergic inflammation in the lungs.
    J Immunol. 2012 Feb 1;188(3):1503-13 PMID: 22198948
  52. Lineage(-)Sca1+c-Kit(-)CD25+ cells are IL-33-responsive type 2 innate cells in the mouse bone marrow.
    J Immunol. 2011 Dec 1;187(11):5795-804 PMID: 22048767
  53. Interleukin-7 regulates adipose tissue mass and insulin sensitivity in high-fat diet-fed mice through lymphocyte-dependent and independent mechanisms.
    PLoS One. 2012;7(6):e40351 PMID: 22768283
  54. IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines.
    Immunity. 2005 Nov;23(5):479-90 PMID: 16286016
  55. Relationship between interleukin-5 and eotaxin in regulating blood and tissue eosinophilia in mice.
    J Clin Invest. 1997 Mar 1;99(5):1064-71 PMID: 9062365
Article Info
Journal
The Journal of experimental medicine
Abbr.
J Exp Med
ISSN
1540-9538
Published
2013-03-11
Epub
2013-00-18
Pages
535-49
Language
English
Region
United States
NLM ID
2985109R
PMCID
PMC3600903
Subset
IM
Grants
NIAID NIH HHS · P01 AI078869 · United States
NIDDK NIH HHS · P30 DK063720 · United States
NIAID NIH HHS · AI026918 · United States
NIGMS NIH HHS · T32 GM007618 · United States
NHLBI NIH HHS · P01 HL107202 · United States
NIAID NIH HHS · R01 AI026918 · United States
NIAID NIH HHS · K08 AI095319 · United States
Howard Hughes Medical Institute · United States
NIAID NIH HHS · T32 AI007641 · United States
NICHD NIH HHS · T32 HD044331 · United States
NIDDK NIH HHS · R01 DK094641 · United States
NIAID NIH HHS · R37 AI026918 · United States
NIAID NIH HHS · R01 AI030663 · United States
NIAID NIH HHS · AI030663 · United States
NHLBI NIH HHS · R01 HL076746 · United States
NIAID NIH HHS · AI078869 · United States
NHLBI NIH HHS · HL107202 · United States
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