A worm of one's own: How helminths modulate host adipose tissue function and metabolism

Trends in Parasitology

Volumn 31, Issue 9, 2015, Pages 435-441

  Guigas, Bruno ^a   Molofsky, Ari B ^b  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Adipose tissue; Diabetes; Helminth; Metabolism; Type 2 immunity

Indexed keywords

ADIPOSE TISSUE; HELMINTHIASIS; HOMEOSTASIS; HOST PATHOGEN INTERACTION; HUMAN; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; IMMUNOREGULATION; INFLAMMATION; METABOLIC DISORDER; NONHUMAN; OBESITY; PARASITE IMMUNITY; REVIEW; TH2 CELL; TISSUE METABOLISM; ANIMAL; EVOLUTION; HELMINTH; HOST PARASITE INTERACTION; IMMUNOLOGY; METABOLIC SYNDROME X; METABOLISM; MOUSE; PARASITOLOGY; PHYSIOLOGY;

ADIPOSE TISSUE; ANIMALS; BIOLOGICAL EVOLUTION; HELMINTHIASIS; HELMINTHS; HOST-PARASITE INTERACTIONS; METABOLIC SYNDROME X; MICE;

EID: 84940611205     PISSN: 14714922     EISSN: 14715007     Source Type: Journal    
DOI: 10.1016/j.pt.2015.04.008     Document Type: Review

References (90)

1. Wiria A.E., et al. Helminth infection in populations undergoing epidemiological transition: a friend or foe?. Semin. Immunopathol. 2012, 34:889-901.
2. DiAngelo J.R., et al. The immune response attenuates growth and nutrient storage in Drosophila by reducing insulin signaling. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:20853-20858.
3. Odegaard J.I., Chawla A. Alternative macrophage activation and metabolism. Annu. Rev. Pathol. Mech. Dis. 2011, 6:275-297.
4. Hotez P.J., et al. Helminth infections: the great neglected tropical diseases. J. Clin. Invest. 2008, 118:1311-1321.
5. Allen J.E., Maizels R.M. Diversity and dialogue in immunity to helminths. Nat. Rev. Immunol. 2011, 11:375-388.
6. Zaph C., et al. Mucosal immune responses following intestinal nematode infection. Parasit. Immunol. 2014, 36:439-452.
7. Saz H.J. Energy metabolisms of parasitic helminths: adaptations to parasitism. Annu. Rev. Physiol. 1981, 43:323-341.
8. Stephenson L.S., et al. Malnutrition and parasitic helminth infections. Parasitology 2000, 121:S23-S38.
9. King C.H., Dangerfield-Cha M. The unacknowledged impact of chronic schistosomiasis. Chronic Illn. 2008, 4:65-79.
10. Colley D.G., et al. Human schistosomiasis. Lancet 2014, 383:2253-2264.
11. Wammes L.J., et al. Helminth therapy or elimination: epidemiological, immunological, and clinical considerations. Lancet Infect. Dis. 2014, 14:1150-1162.
12. Tahapary, D.L. (2015) Helminth infections and type 2 diabetes: a cluster-randomized placebo controlled SUGARSPIN trial in Nangapanda, Flores, Indonesia. http://dx.doi.org/10.1186/s12879-015-0873-4.
13. Wiria A.E., et al. Helminth infections, type-2 immune response, and metabolic syndrome. PLoS Pathog. 2014, 10:e1004140.
14. Hussaarts L., et al. Priming dendritic cells for th2 polarization: lessons learned from helminths and implications for metabolic disorders. Front. Immunol. 2014, 5:499.
15. Alberti K.G.M.M., et al. Harmonizing the metabolic syndrome a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation 2009, 120:1640-1645.
16. Guariguata L., et al. Global estimates of diabetes prevalence for 2013 and projections for 2035. Diabetes Res. Clin. Pract. 2014, 103:137-149.
17. Donath M.Y., Shoelson S.E. Type 2 diabetes as an inflammatory disease. Nat. Rev. Immunol. 2011, 11:98-107.
18. Hotamisligil G.S., et al. Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science 1993, 259:87-91.
19. Uysal K.T., et al. Protection from obesity-induced insulin resistance in mice lacking TNF-alpha function. Nature 1997, 389:610-614.
20. Pradhan A.D., et al. C-reactive protein, interleukin 6, and risk of developing type 2 diabetes mellitus. JAMA 2001, 286:327-334.
21. Xu H., et al. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J. Clin. Invest. 2003, 112:1821-1830.
22. Lumeng C.N., et al. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J. Clin. Invest. 2007, 117:175-184.
23. Lumeng C.N., et al. Increased inflammatory properties of adipose tissue macrophages recruited during diet-induced obesity. Diabetes 2007, 56:16-23.
24. Nishimura S., et al. CD8+ effector T cells contribute to macrophage recruitment and adipose tissue inflammation in obesity. Nat. Med. 2009, 15:914-920.
25. Mathis D. Immunological goings-on in visceral adipose tissue. Cell Metab. 2013, 17:851-859.
26. Osborn O., Olefsky J.M. The cellular and signaling networks linking the immune system and metabolism in disease. Nat. Med. 2012, 18:363-374.
27. Winer S., et al. Normalization of obesity-associated insulin resistance through immunotherapy. Nat. Med. 2009, 15:921-929.
28. Feuerer M., et al. Lean, but not obese, fat is enriched for a unique population of regulatory T cells that affect metabolic parameters. Nat. Med. 2009, 15:930-939.
29. Liu J., et al. Genetic deficiency and pharmacological stabilization of mast cells reduce diet-induced obesity and diabetes in mice. Nat. Med. 2009, 15:940-945.
30. Talukdar S., et al. Neutrophils mediate insulin resistance in mice fed a high-fat diet through secreted elastase. Nat. Med. 2012, 18:1407-1412.
31. Wensveen, F.M. et al. (2015) NK cells link obesity-induced adipose stress to inflammation and insulin resistance. Nat Immunol. 16, 376-385.
32. Wu D., et al. Eosinophils sustain adipose alternatively activated macrophages associated with glucose homeostasis. Science 2011, 332:243-247.
33. Yang Z., et al. Parasitic nematode-induced modulation of body weight and associated metabolic dysfunction in mouse models of obesity. Infect. Immun. 2013, 81:1905-1914.
34. Molofsky A.B., et al. Innate lymphoid type 2 cells sustain visceral adipose tissue eosinophils and alternatively activated macrophages. J. Exp. Med. 2013, 210:535-549.
35. Hussaarts L., 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, 10.1096/fj.14-266239.
36. Van Dyken S.J., Locksley R.M. Interleukin-4- and interleukin-13-mediated alternatively activated macrophages: roles in homeostasis and disease. Annu. Rev. Immunol. 2013, 31:317-343.
37. Kita H. Eosinophils: multifaceted biological properties and roles in health and disease. Immunol. Rev. 2011, 242:161-177.
38. Hams E., et al. Cutting edge: IL-25 elicits innate lymphoid type 2 and type II NKT cells that regulate obesity in mice. J. Immunol. 2013, 191:5349-5353.
39. Moro K., et al. Innate production of T(H)2 cytokines by adipose tissue-associated c-Kit(+)Sca-1(+) lymphoid cells. Nature 2010, 463:540-544.
40. Diefenbach A. Innate lymphoid cells in the defense against infections. Eur. J. Microbiol. Immunol. (Bp) 2013, 3:143-151.
41. Nussbaum J.C., et al. Type 2 innate lymphoid cells control eosinophil homeostasis. Nature 2013, 502:245-248.
42. Walker J.A., McKenzie A.N. Development and function of group 2 innate lymphoid cells. Curr. Opin. Immunol. 2013, 25:148-155.
43. Cipolletta D., et al. PPAR-γ is a major driver of the accumulation and phenotype of adipose tissue Treg cells. Nature 2012, 486:549-553.
44. Vasanthakumar A., et al. The transcriptional regulators IRF4, BATF and IL-33 orchestrate development and maintenance of adipose tissue-resident regulatory T cells. Nat. Immunol. 2015, 16:276-285.
45. Schiering C., et al. The alarmin IL-33 promotes regulatory T-cell function in the intestine. Nature 2014, 513:564-568.
46. Burzyn D., et al. Regulatory T cells in nonlymphoid tissues. Nat. Immunol. 2013, 14:1007-1013.
47. McSorley H.J., Maizels R.M. Helminth infections and host immune regulation. Clin. Microbiol. Rev. 2012, 25:585-608.
48. Gause W.C., et al. Type 2 immunity and wound healing: evolutionary refinement of adaptive immunity by helminths. Nat. Rev. Immunol. 2013, 13:607-614.
49. Moltke, et al. I-L-C-2 it: type 2 immunity and group 2 innate lymphoid cells in homeostasis. Curr. Opin. Immunol. 2014, 31:58-65.
50. Stanya K.J., et al. Direct control of hepatic glucose production by interleukin-13 in mice. J. Clin. Invest. 2013, 123:261-271.
51. Ricardo-Gonzalez R.R., et al. IL-4/STAT6 immune axis regulates peripheral nutrient metabolism and insulin sensitivity. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:22617-22622.
52. Wolfs I.M.J., et al. Reprogramming macrophages to an anti-inflammatory phenotype by helminth antigens reduces murine atherosclerosis. FASEB J. 2014, 28:288-299.
53. Doenhoff M.J., et al. An anti-atherogenic effect of Schistosoma mansoni infections in mice associated with a parasite-induced lowering of blood total cholesterol. Parasitology 2002, 125:415-421.
54. Neill D.R., et al. Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature 2010, 464:1367-1370.
55. Luck H., et al. Regulation of obesity-related insulin resistance with gut anti-inflammatory agents. Cell Metab. 2015, 21:527-542.
56. Walk S.T., et al. Alteration of the murine gut microbiota during infection with the parasitic helminth Heligmosomoides polygyrus. Inflamm. Bowel Dis. 2010, 16:1841-1849.
57. Lee S.C., et al. Helminth colonization is associated with increased diversity of the gut microbiota. PLoS Negl. Trop. Dis. 2014, 8:e2880.
58. Cayrol C., Girard J-P. IL-33: an alarmin cytokine with crucial roles in innate immunity, inflammation and allergy. Curr. Opin. Immunol. 2014, 31:31-37.
59. Endo Y., et al. The Interleukin-33-p38 kinase axis confers memory T helper 2 cell pathogenicity in the airway. Immunity 2015, 42:294-308.
60. Miller A.M., et al. Interleukin-33 induces protective effects in adipose tissue inflammation during obesity in mice. Circ. Res. 2010, 107:650-658.
61. Lee M-W., et al. Activated type 2 innate lymphoid cells regulate beige fat biogenesis. Cell 2015, 160:74-87.
62. Brestoff J.R., et al. Group 2 innate lymphoid cells promote beiging of white adipose tissue and limit obesity. Nature 2014, 519:242-246.
63. Zeyda M., et al. 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, 37:658-665.
64. Wood I.S., et al. IL-33, a recently identified interleukin-1 gene family member, is expressed in human adipocytes. Biochem. Biophys. Res. Commun. 2009, 384:105-109.
65. Sutherland A.P.R., et al. Linking obesity with type 2 diabetes: the role of T-bet. Diabetes Metab. Syndr. Obes. 2014, 7:331-340.
66. Rocha V.Z., et al. Interferon-gamma, a Th1 cytokine, regulates fat inflammation: a role for adaptive immunity in obesity. Circ. Res. 2008, 103:467-476.
67. Wong N., et al. Deficiency in interferon-gamma results in reduced body weight and better glucose tolerance in mice. Endocrinology 2011, 152:3690-3699.
68. Franceschi C., Campisi J. Chronic inflammation (inflammaging) and its potential contribution to age-associated diseases. J. Gerontol A: Biol. Sci. Med. Sci. 2014, 69:S4-S9.
69. Macaulay R., et al. The role of the T cell in age-related inflammation. AGE 2012, 35:563-572.
70. Cipolletta D., et al. Appearance and disappearance of the mRNA signature characteristic of Treg cells in visceral adipose tissue: age, diet, and PPARγ effects. Proc. Natl. Acad. Sci. U.S.A. 2015, 112:482-487.
71. Everts B., et al. Omega-1, a glycoprotein secreted by Schistosoma mansoni eggs, drives Th2 responses. J. Exp. Med. 2009, 206:1673-1680.
72. Everts B., et al. Schistosome-derived omega-1 drives Th2 polarization by suppressing protein synthesis following internalization by the mannose receptor. J. Exp. Med. 2012, 209:1753-1767.
73. Schramm G., et al. IPSE/alpha-1: a major immunogenic component secreted from Schistosoma mansoni eggs. Mol. Biochem. Parasitol. 2006, 147:9-19.
74. Bhargava P., et al. Immunomodulatory glycan LNFPIII alleviates hepatosteatosis and insulin resistance through direct and indirect control of metabolic pathways. Nat. Med. 2012, 18:1665-1672.
75. Meevissen M.H.J., et al. Schistosoma mansoni egg glycoproteins and C-type lectins of host immune cells: molecular partners that shape immune responses. Exp. Parasitol. 2012, 132:14-21.
76. Pearce E.L., Pearce E.J. Metabolic pathways in immune cell activation and quiescence. Immunity 2013, 38:633-643.
77. Huang S.C-C., et al. Fatty acid oxidation is essential for egg production by the parasitic flatworm Schistosoma mansoni. PLoS Pathog. 2012, 8:e1002996.
78. Tam C.S., et al. Brown adipose tissue mechanisms and potential therapeutic targets. Circulation 2012, 125:2782-2791.
79. Vosselman M.J., et al. Energy dissipation in brown adipose tissue: From mice to men. Mol. Cell. Endocrinol. 2013, 379:43-50.
80. Frontini A., Cinti S. Distribution and development of brown adipocytes in the murine and human adipose organ. Cell Metab. 2010, 11:253-256.
81. Bartelt A., et al. Brown adipose tissue activity controls triglyceride clearance. Nat. Med. 2011, 17:200-205.
82. Chondronikola M., et al. Brown adipose tissue improves whole-body glucose homeostasis and insulin sensitivity in humans. Diabetes 2014, 63:4089-4099.
83. Bartelt A., Heeren J. Adipose tissue browning and metabolic health. Nat. Rev. Endocrinol. 2014, 10:24-36.
84. Harms M., Seale P. Brown and beige fat: development, function and therapeutic potential. Nat. Med. 2013, 19:1252-1263.
85. Daniel H., Derry D.M. Criteria for differentiation of brown and white fat in the rat. Can. J. Physiol. Pharmacol. 2011, 10.1139/y69-154.
86. Slavin B.G., Ballard K.W. Morphological studies on the adrenergic innervation of white adipose tissue. Anat. Rec. 1978, 191:377-389.
87. Brestoff J.R., Artis D. Immune regulation of metabolic homeostasis in health and disease. Cell 2015, 161:146-160.
88. Nguyen K.D., et al. Alternatively activated macrophages produce catecholamines to sustain adaptive thermogenesis. Nature 2011, 480:104-108.
89. Qiu Y., et al. Eosinophils and type 2 cytokine signaling in macrophages orchestrate development of functional beige fat. Cell 2014, 157:1292-1308.
90. Rao R.R., et al. Meteorin-like is a hormone that regulates immune-adipose interactions to increase beige fat thermogenesis. Cell 2014, 157:1279-1291.