Filarial Infection or Antigen Administration Improves Glucose Tolerance in Diet-Induced Obese Mice

Journal of Innate Immunity

Volumn 8, Issue 6, 2016, Pages 601-616

  Berbudi, Afiat ^a,c   Surendar, Jayagopi ^a   Ajendra, Jesuthas ^a   Gondorf, Fabian ^a   Schmidt, David ^a   Neumann, Anna Lena ^a   Wardani, Ajeng P F ^a,c   Layland, Laura E ^a   Hoffmann, Linda S ^a   Pfeifer, Alexander ^a   Hoerauf, Achim ^a,b   Hübner, Marc P ^a  

^a UNIVERSITY HOSPITAL BONN   (Germany)

^b UNIVERSITY OF BONN   (Germany)

^c PADJADJARAN UNIVERSITY   (Indonesia)

Author keywords

Adipose tissue; Alternatively activated macrophages; Eosinophils; Filariae; Glucose tolerance; Helminths; Immunomodulation; Inflammation; Insulin resistance; Litomosoides sigmodontis; Regulatory T cells; Type 2 diabetes

Indexed keywords

INSULIN; LITOMOSOIDES SIGMODONTIS ANTIGEN; PARASITE ANTIGEN; UNCLASSIFIED DRUG;

ADIPOCYTE; ADIPOSE TISSUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; DIET INDUCED OBESITY; EOSINOPHIL; EPIDIDYMIS FAT; FATTY ACID TRANSPORT; FILARIASIS; GENE EXPRESSION; GLUCOSE TOLERANCE; HELMINTH; IMMUNE RESPONSE; INFLAMMATION; LITOMOSOIDES SIGMODONTIS; LYMPHOID CELL; MACROPHAGE; MALE; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; DIET; DISEASE MODEL; FILARIOIDEA; GENETICS; HUMAN; IMMUNOLOGY; INSULIN RESISTANCE; KNOCKOUT MOUSE; LIPID METABOLISM; NON INSULIN DEPENDENT DIABETES MELLITUS; OBESITY; SIGNAL TRANSDUCTION; TH2 CELL;

ANIMALS; ANTIGENS, HELMINTH; DIABETES MELLITUS, TYPE 2; DIET; DISEASE MODELS, ANIMAL; EOSINOPHILS; FILARIASIS; FILARIOIDEA; HUMANS; INSULIN RESISTANCE; LIPID METABOLISM; MACROPHAGES; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; OBESITY; SIGNAL TRANSDUCTION; TH2 CELLS;

EID: 84983742556     PISSN: 1662811X     EISSN: 16628128     Source Type: Journal    
DOI: 10.1159/000448401     Document Type: Article

References (55)

1. International Diabetes Federation: IDF Diabetes Atlas, ed 6, 2014. Brussels, International Diabetes Federation, 2014, http://www.idf. org/sites/default/files/Atlas-poster-2014- EN.pdf.
2. Cipolletta D, Kolodin D, Benoist C, Mathis D: Tissular T(regs): a unique population of adipose-tissue-resident Foxp3+CD4+ T cells that impacts organismal metabolism. Semin Immunol 2011; 23: 431-437.
3. Wu D, Molofsky AB, Liang H-E, Ricardo-Gonzalez RR, Jouihan HA, Bando JK, Chawla A, Locksley RM: Eosinophils sustain adipose alternatively activated macrophages associated with glucose homeostasis. Science 2011; 332: 243-247.
4. Molofsky AB, Nussbaum JC, Liang H, Van Dyken SJ, Cheng LE, Mohapatra A, et al: Innate lymphoid type 2 cells sustain visceral adipose tissue eosinophils and alternatively activated macrophages. J Exp Med 2013; 210: 535-549.
5. Winer DA, Winer S, Shen L, Wadia PP, Yantha J, Paltser G, et al: B cells promote insulin resistance through modulation of T cells and production of pathogenic IgG antibodies. Nat Med 2011; 17: 610-617.
6. Olefsky JM, Glass CK: Macrophages, inflammation, and insulin resistance. Annu Rev Physiol 2010; 72: 219-246.
7. Spranger J, Kroke A, Mohlig M, Hoffmann K, Bergmann MM, Ristow M, et al: Inflammatory cytokines and the risk to develop type 2 diabetes: results of the prospective population-based European Prospective Investigation into Cancer and Nutrition (EPIC)-Potsdam Study. Diabetes 2003; 52: 812-817.
8. McSorley HJ, Hewitson JP, Maizels RM: Immunomodulation by helminth parasites: defining mechanisms and mediators. Int J Parasitol 2013; 43: 301-310.
9. Kreider T, Anthony RM, Urban JF, Gause WC: Alternatively activated macrophages in helminth infections. Curr Opin Immunol 2007; 19: 448-453.
10. Wammes LJ, Mpairwe H, Elliott AM, Yazdanbakhsh M, Hoeppli R, Bundy D, et al: Helminth therapy or elimination: epidemiological, immunological, and clinical considerations. Lancet Infect Dis 2014; 14: 1150-1162.
11. Berbudi A, Ajendra J, Wardani APF, Hoerauf A, Hubner MP: Parasitic helminths and their beneficial impact on type 1 and type 2 diabetes. Diabetes Metab Res Rev 2016; 32: 238-250.
12. Maizels RM, Maizels RM, Yazdanbakhsh M, Asher MI, Montefort S, Bjorksten B, et al: Parasitic helminth infections and the control of human allergic and autoimmune disorders. Clin Microbiol Infect 2016; 22: 481-486.
13. Hubner MP, Stocker JT, Mitre E: Inhibition of type 1 diabetes in filaria-infected non-obese diabetic mice is associated with a T helper type 2 shift and induction of FoxP3+ regulatory T cells. Immunology 2009; 127: 512-522.
14. Hubner MP, Shi Y, Torrero MN, Mueller E, Larson D, Soloviova K, et al: Helminth protection against autoimmune diabetes in nonobese diabetic mice is independent of a type 2 immune shift and requires TGF-β J Immunol 2012; 188: 559-568.
15. Aravindhan V, Mohan V, Surendar J, Muralidhara Rao M, Pavankumar N, Deepa M, et al: Decreased prevalence of lymphatic filariasis among diabetic subjects associated with a diminished pro-inflammatory cytokine response (CURES 83). PLoS Negl Trop Dis 2010; 4:e707.
16. Chen Y, Lu J, Huang Y, Wang T, Xu Y, Xu M, et al: Association of previous schistosome infection with diabetes and metabolic syndrome: a cross-sectional study in rural China. J Clin Endocrinol Metab 2013; 98:E283-E287.
17. Wiria AE, Hamid F, Wammes LJ, Prasetyani MA, Dekkers OM, May L, et al: Infection with soil-transmitted helminths is associated with increased insulin sensitivity. PLoS One 2015; 10:e0127746.
18. Hays R, Esterman A, Giacomin P, Loukas A, McDermott R, Krolewiecki AJ, et al: Does Strongyloides stercoralis infection protect against type 2 diabetes in humans? Evidence from Australian aboriginal adults. Diabetes Res Clin Pract 2015; 107: 355-361.
19. Malozowski S, Sahlroot JT: Interleukin-1-receptor antagonist in type 2 diabetes mellitus. N Engl J Med 2007; 357: 302-303.
20. Moller DE: Potential role of TNF-alpha in the pathogenesis of insulin resistance and type 2 diabetes. Trends Endocrinol Metab 2000; 11: 212-217.
21. Santomauro AT, Boden G, Silva ME, Rocha DM, Santos RF, Ursich MJ, et al: Overnight lowering of free fatty acids with Acipimox improves insulin resistance and glucose tolerance in obese diabetic and nondiabetic subjects. Diabetes 1999; 48: 1836-1841.
22. Frayn KN: Adipose tissue as a buffer for daily lipid flux. Diabetologia 2002; 45: 1201-1210.
23. Volkmann L, Bain O, Saeftel M, Specht S, Fischer K, Brombacher F, et al: Murine filariasis: interleukin 4 and interleukin 5 lead to containment of different worm developmental stages. Med Microbiol Immunol 2003; 192: 23-31.
24. Ajendra J, Specht S, Neumann A-L, Gondorf F, Schmidt D, Gentil K, et al: ST2 deficiency does not impair type 2 immune responses during chronic filarial infection but leads to an increased microfilaremia due to an impaired splenic microfilarial clearance. PLoS One 2014; 9:e93072.
25. Lahl K, Loddenkemper C, Drouin C, Freyer J, Arnason J, Eberl G, et al: Selective depletion of Foxp3 + regulatory T cells induces a scurfylike disease. J Exp Med 2007; 204: 57-63.
26. Lahl K, Sparwasser T: In vivo depletion of FoxP3+ Tregs using the DEREG mouse model. Methods Mol Biol 2011; 707: 157-172.
27. Lumeng CN, Deyoung SM, Bodzin JL, Saltiel AR: Increased inflammatory properties of adipose tissue macrophages recruited during diet-induced obesity. Diabetes 2007; 56: 16-23.
28. Fujisaka S, Usui I, Bukhari A, Ikutani M, Oya T, Kanatani Y, et al: Regulatory mechanisms for adipose tissue M1 and M2 macrophages in diet-induced obese mice. Diabetes 2009; 58: 2574-2582.
29. Vaughan DE: PAI-1 and atherothrombosis. J Thromb Haemost 2005; 3: 1879-1883.
30. Jeoung NH, Harris RA: Knocking out PDK2 and PDK4 lowers fasting blood glucose levels, increases insulin sensitivity, and greatly improves glucose tolerance. FASEB J 2007; 21: LB35-LB36.
31. Layland LE, Ajendra J, Ritter M, Wiszniewsky A, Hoerauf A, Hubner MP: Development of patent Litomosoides sigmodontis infections in semi-susceptible C57BL/6 mice in the absence of adaptive immune responses. Parasit Vectors 2015; 8: 396.
32. Lumeng CN, Bodzin JL, Saltiel AR: Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest 2007; 117: 175-184.
33. Odegaard JI, Ricardo-Gonzalez RR, Goforth MH, Morel CR, Subramanian V, Mukundan L, et al: Macrophage-specific PPARγ controls alternative activation and improves insulin resistance. Nature 2007; 447: 1116-1120.
34. Odegaard JI, Ricardo-Gonzalez RR, Red Eagle A, Vats D, Morel CR, Goforth MH, et al: Alternative M2 activation of Kupffer cells by PPAR? ameliorates obesity-induced insulin resistance. Cell Metab 2008; 7: 496-507.
35. Bhargava P, Li C, Stanya KJ, Jacobi D, Dai L, Liu S, et al: Immunomodulatory glycan LNFPIII alleviates hepatosteatosis and insulin resistance through direct and indirect control of metabolic pathways. Nat Med 2012; 28: 1-9.
36. Ricardo-Gonzalez RR, Red Eagle A, Odegaard JI, Jouihan H, Morel CR, Heredia JE, et al: IL-4/STAT6 immune axis regulates peripheral nutrient metabolism and insulin sensitivity. Proc Natl Acad Sci USA 2010; 107: 22617-22622.
37. O'Garra A, Chang R, Go N, Hastings R, Haughton G, Howard M: Ly-1 B (B-1) cells are the main source of B cell-derived interleukin 10. Eur J Immunol 1992; 22: 711-717.
38. Zhou L: Striking similarity: GATA-3 regulates ILC2 and Th2 cells. Immunity 2012; 37: 589-591.
39. Lee M-W, Odegaard JI, Mukundan L, Qiu Y, Molofsky AB, Nussbaum JC, et al: Activated type 2 innate lymphoid cells regulate beige fat biogenesis. Cell 2015; 160: 74-87.
40. Brestoff JR, Kim BS, Saenz SA, Stine RR, Monticelli LA, Sonnenberg GF, et al: Group 2 innate lymphoid cells promote beiging of white adipose tissue and limit obesity. Nature 2015; 519: 242-246.
41. Wohlfert EA, Grainger JR, Bouladoux N, Konkel JE, Oldenhove G, Ribeiro CH, et al: GATA3 controls Foxp3+ regulatory T cell fate during inflammation in mice. J Clin Invest 2011; 121: 4503-4515.
42. Wang Y, Su MA, Wan YY: An essential role of the transcription factor GATA-3 for the function of regulatory T cells. Immunity 2011; 35: 337-48.
43. Barbi J, Pardoll D, Pan F: Treg functional stability and its responsiveness to the microenvironment. Immunol Rev 2014; 259: 115-139.
44. Thauvin-Robinet C, Auclair M, Duplomb L, Caron-Debarle M, Avila M, St-Onge J, et al: PIK3R1 mutations cause syndromic insulin resistance with lipoatrophy. Am J Hum Genet 2013; 93: 141-149.
45. Zmuda-Trzebiatowska E, Oknianska A, Manganiello V, Degerman E: Role of PDE3B in insulin-induced glucose uptake, GLUT-4 translocation and lipogenesis in primary rat adipocytes. Cell Signal 2006; 18: 382-390.
46. Aronoff SL, Berkowitz K, Shreiner B: Glucose metabolism and regulation: beyond insulin and glucagon. Diabetes Spectr 2004; 17: 183-190.
47. Hussaarts L, Garcia-Tardon N, van Beek L, Heemskerk MM, Haeberlein S, van der Zon GC, et al: Chronic helminth infection and helminth-derived egg antigens promote adipose tissue M2 macrophages and improve insulin sensitivity in obese mice. FASEB J 2015; 7: 3027-3039.
48. Hise AG, Daehnel K, Gillette-Ferguson I, Cho E, McGarry HF, Taylor MJ, et al: Innate immune responses to endosymbiotic Wolbachia bacteria in Brugia malayi and Onchocerca volvulus are dependent on TLR2, TLR6, MyD88, and Mal, but not TLR4, TRIF, or TRAM. J Immunol 2007; 178: 1068-1076.
49. Lehrke M, Lazar MA: The many faces of PPARγ. Cell 2005; 123: 993-999.
50. Rangwala SM, Rhoades B, Shapiro JS, Rich AS, Kim JK, Shulman GI, et al: Genetic modulation of PPARγ phosphorylation regulates insulin sensitivity. Dev Cell 2003; 5: 657-663.
51. Nolan JJ, Ludvik B, Beerdsen P, Joyce M, Olefsky J: Improvement in glucose tolerance and insulin resistance in obese subjects treated with troglitazone. N Engl J Med 1994; 331: 1188-1193.
52. Welch JS, Ricote M, Akiyama TE, Gonzalez FJ, Glass CK: PPARγ and PPARδ negatively regulate specific subsets of lipopolysaccharide and IFN-γ target genes in macrophages. Proc Natl Acad Sci USA 2003; 100: 6712-6717.
53. Cipolletta D, Feuerer M, Li A, Kamei N, Lee J, Shoelson SE, et al: PPAR-γ is a major driver of the accumulation and phenotype of adipose tissue T reg cells. Nature 2012; 486: 549-553.
54. Wen H, Gris D, Lei Y, Jha S, Zhang L, Huang MT-H, et al: Fatty acid-induced NLRP3-ASC inflammasome activation interferes with insulin signaling. Nat Immunol 2011; 12: 408-415.
55. Hoerauf A, Satoguina J, Saeftel M, Specht S: Immunomodulation by filarial nematodes. Parasite Immunol 2005; 27: 417-429.