Macrophage-Derived Human Resistin Is Induced in Multiple Helminth Infections and Promotes Inflammatory Monocytes and Increased Parasite Burden

PLoS Pathogens

Volumn 11, Issue 1, 2015, Pages 1-14

  Jang, Jessica C ^a   Chen, Gang ^a   Wang, Spencer H ^a   Barnes, Mark A ^a   Chung, Josiah I ^a   Camberis, Mali ^b   Le Gros, Graham ^b   Cooper, Philip J ^c,d,e   Steel, Cathy ^f   Nutman, Thomas B ^f   Lazar, Mitchell A ^g   Nair, Meera G ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MALAGHAN INSTITUTE OF MEDICAL RESEARCH   (New Zealand)

^c Laboratorio de Investigaciones FEPIS   (Ecuador)

^d PONTIFICIA UNIVERSIDAD CATÓLICA DEL ECUADOR   (Ecuador)

^e ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

^f NATIONAL INSTITUTES OF HEALTH   (United States)

^g UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; CHEMOKINE RECEPTOR CCR2; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERFERON REGULATORY FACTOR 7; INTERLEUKIN 1ALPHA; INTERLEUKIN 6; LEPTIN; MONOCYTE CHEMOTACTIC PROTEIN 1; MONOCYTE CHEMOTACTIC PROTEIN 2; RESISTIN; TOLL LIKE RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; VASCULAR CELL ADHESION MOLECULE 1; AUTACOID; CYTOKINE; RETN PROTEIN, HUMAN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INFILTRATION; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HELMINTHIASIS; HISTOLOGY; HUMAN; INFLAMMATION; MONOCYTE; MOUSE; NEUTROPHIL; NIPPOSTRONGYLUS BRASILIENSIS; NONHUMAN; PARASITE LOAD; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TH2 CELL; TRANSCRIPTION REGULATION; UPREGULATION; WUCHERERIA BANCROFTI; ANIMAL; C57BL MOUSE; FEMALE; GENETICS; IMMUNOLOGY; MACROPHAGE; MALE; METABOLISM; NIPPOSTRONGYLUS; PARASITEMIA; PARASITOLOGY; RAT; SPRAGUE DAWLEY RAT; STRONGYLE INFECTION; TRANSGENIC MOUSE;

MURINAE; MUS; MUS MUSCULUS; NIPPOSTRONGYLUS BRASILIENSIS; VERMES; WUCHERERIA BANCROFTI;

ANIMALS; CYTOKINES; FEMALE; HELMINTHIASIS; HUMANS; INFLAMMATION; INFLAMMATION MEDIATORS; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MONOCYTES; NIPPOSTRONGYLUS; PARASITEMIA; RATS; RATS, SPRAGUE-DAWLEY; RESISTIN; STRONGYLIDA INFECTIONS; UP-REGULATION;

EID: 84923826412     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004579     Document Type: Article

References (58)

1. Hotez PJ, Brindley PJ, Bethony JM, King CH, Pearce EJ, et al. (2008) Helminth infections: the great neglected tropical diseases. J Clin Invest 118: 1311–1321.
2. MacDonald TT, Choy MY, Spencer J, Richman PI, Diss T, et al. (1991) Histopathology and immunohistochemistry of the caecum in children with the Trichuris dysentery syndrome. J Clin Pathol 44: 194–199.
3. Min B, Prout M, Hu-Li J, Zhu J, Jankovic D, et al. (2004) Basophils produce IL-4 and accumulate in tissues after infection with a Th2-inducing parasite. J Exp Med 200: 507–517.
4. Neill DR, Wong SH, Bellosi A, Flynn RJ, Daly M, et al. (2010) Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature 464: 1367–1370.
5. Voehringer D, Shinkai K, Locksley RM, (2004) Type 2 immunity reflects orchestrated recruitment of cells committed to IL-4 production. Immunity 20: 267–277.
6. Le Goff L, Lamb TJ, Graham AL, Harcus Y, Allen JE, (2002) IL-4 is required to prevent filarial nematode development in resistant but not susceptible strains of mice. Int J Parasitol 32: 1277–1284.
7. Urban JF, JrNoben-Trauth N, Donaldson DD, Madden KB, Morris SC, et al. (1998) IL-13, IL-4Ralpha, and Stat6 are required for the expulsion of the gastrointestinal nematode parasite Nippostrongylus brasiliensis. Immunity 8: 255–264.
8. Chen F, Liu Z, Wu W, Rozo C, Bowdridge S, et al. (2012) An essential role for TH2-type responses in limiting acute tissue damage during experimental helminth infection. Nat Med 18: 260–266.
9. Herbert DR, Holscher C, Mohrs M, Arendse B, Schwegmann A, et al. (2004) Alternative macrophage activation is essential for survival during schistosomiasis and downmodulates T helper 1 responses and immunopathology. Immunity 20: 623–635.
10. Urban J, Fang H, Liu Q, Ekkens MJ, Chen SJ, et al. (2000) IL-13-mediated worm expulsion is B7 independent and IFN-gamma sensitive. J Immunol 164: 4250–4256.
11. Babu S, Bhat SQ, Pavan Kumar N, Lipira AB, Kumar S, et al. (2009) Filarial lymphedema is characterized by antigen-specific Th1 and th17 proinflammatory responses and a lack of regulatory T cells. PLoS Negl Trop Dis 3: e420.
12. Babu S, Anuradha R, Kumar NP, George PJ, Kumaraswami V, et al. (2012) Toll-like receptor- and filarial antigen-mediated, mitogen-activated protein kinase- and NF-kappaB-dependent regulation of angiogenic growth factors in filarial lymphatic pathology. Infect Immun 80: 2509–2518.
13. Helmby H, Grencis RK, (2003) Essential role for TLR4 and MyD88 in the development of chronic intestinal nematode infection. Eur J Immunol 33: 2974–2979.
14. Yang RZ, Huang Q, Xu A, McLenithan JC, Eisen JA, et al. (2003) Comparative studies of resistin expression and phylogenomics in human and mouse. Biochem Biophys Res Commun 310: 927–935.
15. Nair MG, Du Y, Perrigoue JG, Zaph C, Taylor JJ, et al. (2009) Alternatively activated macrophage-derived RELM-{alpha} is a negative regulator of type 2 inflammation in the lung. J Exp Med 206: 937–952.
16. Pesce JT, Ramalingam TR, Wilson MS, Mentink-Kane MM, Thompson RW, et al. (2009) Retnla (relmalpha/fizz1) suppresses helminth-induced Th2-type immunity. PLoS Pathog 5: e1000393.
17. Nair MG, Guild KJ, Du Y, Zaph C, Yancopoulos GD, et al. (2008) Goblet cell-derived resistin-like molecule beta augments CD4+ T cell production of IFN-gamma and infection-induced intestinal inflammation. J Immunol 181: 4709–4715.
18. Artis D, Wang ML, Keilbaugh SA, He W, Brenes M, et al. (2004) RELMbeta/FIZZ2 is a goblet cell-specific immune-effector molecule in the gastrointestinal tract. Proc Natl Acad Sci U S A 101: 13596–13600.
19. Steppan CM, Bailey ST, Bhat S, Brown EJ, Banerjee RR, et al. (2001) The hormone resistin links obesity to diabetes. Nature 409: 307–312.
20. Jung HS, Park KH, Cho YM, Chung SS, Cho HJ, et al. (2006) Resistin is secreted from macrophages in atheromas and promotes atherosclerosis. Cardiovasc Res 69: 76–85.
21. Patel L, Buckels AC, Kinghorn IJ, Murdock PR, Holbrook JD, et al. (2003) Resistin is expressed in human macrophages and directly regulated by PPAR gamma activators. Biochem Biophys Res Commun 300: 472–476.
22. Migita K, Maeda Y, Miyashita T, Kimura H, Nakamura M, et al. (2006) The serum levels of resistin in rheumatoid arthritis patients. Clin Exp Rheumatol 24: 698–701.
23. Reilly MP, Lehrke M, Wolfe ML, Rohatgi A, Lazar MA, et al. (2005) Resistin is an inflammatory marker of atherosclerosis in humans. Circulation 111: 932–939.
24. Jiang S, Park DW, Tadie JM, Gregoire M, Deshane J, et al. (2014) Human resistin promotes neutrophil proinflammatory activation and neutrophil extracellular trap formation and increases severity of acute lung injury. J Immunol 192: 4795–4803.
25. Lehrke M, Reilly MP, Millington SC, Iqbal N, Rader DJ, et al. (2004) An inflammatory cascade leading to hyperresistinemia in humans. PLoS Med 1: e45.
26. Park HK, Qatanani M, Briggs ER, Ahima RS, Lazar MA, (2011) Inflammatory induction of human resistin causes insulin resistance in endotoxemic mice. Diabetes 60: 775–783.
27. Kuo CH, Chen KF, Chou SH, Huang YF, Wu CY, et al. (2013) Lung tumor-associated dendritic cell-derived resistin promoted cancer progression by increasing Wolf-Hirschhorn syndrome candidate 1/Twist pathway. Carcinogenesis 34: 2600–2609.
28. Hsieh YY, Shen CH, Huang WS, Chin CC, Kuo YH, et al. (2014) Resistin-induced stromal cell-derived factor-1 expression through Toll-like receptor 4 and activation of p38 MAPK/NFkappaB signaling pathway in gastric cancer cells. J Biomed Sci 21: 59.
29. Benomar Y, Gertler A, De Lacy P, Crepin D, Ould Hamouda H, et al. (2013) Central resistin overexposure induces insulin resistance through Toll-like receptor 4. Diabetes 62: 102–114.
30. Reece JJ, Siracusa MC, Scott AL, (2006) Innate immune responses to lung-stage helminth infection induce alternatively activated alveolar macrophages. Infect Immun 74: 4970–4981.
31. Boring L, Gosling J, Chensue SW, Kunkel SL, Farese RV, Jret al. (1997) Impaired monocyte migration and reduced type 1 (Th1) cytokine responses in C-C chemokine receptor 2 knockout mice. J Clin Invest 100: 2552–2561.
32. Taub DD, Lloyd AR, Conlon K, Wang JM, Ortaldo JR, et al. (1993) Recombinant human interferon-inducible protein 10 is a chemoattractant for human monocytes and T lymphocytes and promotes T cell adhesion to endothelial cells. J Exp Med 177: 1809–1814.
33. Odegaard JI, Chawla A, (2011) Alternative macrophage activation and metabolism. Annu Rev Pathol 6: 275–297.
34. Thomas GD, Ruckerl D, Maskrey BH, Whitfield PD, Blaxter ML, et al. (2012) The biology of nematode- and IL4Ralpha-dependent murine macrophage polarization in vivo as defined by RNA-Seq and targeted lipidomics. Blood 120: e93–e104.
35. Lehrke M, Lazar MA, (2004) Inflamed about obesity. Nat Med 10: 126–127.
36. Jackson JA, Turner JD, Kamal M, Wright V, Bickle Q, et al. (2006) Gastrointestinal nematode infection is associated with variation in innate immune responsiveness. Microbes Infect 8: 487–492.
37. Bethony J, Brooker S, Albonico M, Geiger SM, Loukas A, et al. (2006) Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet 367: 1521–1532.
38. Moncayo AL, Vaca M, Oviedo G, Workman LJ, Chico ME, et al. (2013) Effects of geohelminth infection and age on the associations between allergen-specific IgE, skin test reactivity and wheeze: a case-control study. Clin Exp Allergy 43: 60–72.
39. Loke P, Nair MG, Parkinson J, Guiliano D, Blaxter M, et al. (2002) IL-4 dependent alternatively-activated macrophages have a distinctive in vivo gene expression phenotype. BMC Immunol 3: 7.
40. Nair MG, Gallagher IJ, Taylor MD, Loke P, Coulson PS, et al. (2005) Chitinase and Fizz family members are a generalized feature of nematode infection with selective upregulation of Ym1 and Fizz1 by antigen-presenting cells. Infect Immun 73: 385–394.
41. Cuenco KT, Ottesen EA, Williams SA, Nutman TB, Steel C, (2009) Heritable factors play a major role in determining host responses to Wuchereria bancrofti infection in an isolated South Pacific island population. J Infect Dis 200: 1271–1278.
42. Weller PF, Ottesen EA, Heck L, Tere T, Neva FA, (1982) Endemic filariasis on a Pacific island. I. Clinical, epidemiologic, and parasitologic aspects. Am J Trop Med Hyg 31: 942–952.
43. Anthony RM, Rutitzky LI, Urban JF, JrStadecker MJ, Gause WC, (2007) Protective immune mechanisms in helminth infection. Nat Rev Immunol 7: 975–987.
44. Herbert DR, Yang JQ, Hogan SP, Groschwitz K, Khodoun M, et al. (2009) Intestinal epithelial cell secretion of RELM-beta protects against gastrointestinal worm infection. J Exp Med 206: 2947–2957.
45. He W, Wang ML, Jiang HQ, Steppan CM, Shin ME, et al. (2003) Bacterial colonization leads to the colonic secretion of RELMbeta/FIZZ2, a novel goblet cell-specific protein. Gastroenterology 125: 1388–1397.
46. Osborne LC, Joyce KL, Alenghat T, Sonnenberg GF, Giacomin PR, et al. (2013) Resistin-like molecule alpha promotes pathogenic Th17 cell responses and bacterial-induced intestinal inflammation. J Immunol 190: 2292–2300.
47. Qatanani M, Szwergold NR, Greaves DR, Ahima RS, Lazar MA, (2009) Macrophage-derived human resistin exacerbates adipose tissue inflammation and insulin resistance in mice. J Clin Invest 119: 531–539.
48. Babu S, Kumaraswami V, Nutman TB, (2009) Alternatively activated and immunoregulatory monocytes in human filarial infections. J Infect Dis 199: 1827–1837.
49. Semnani RT, Mahapatra L, Moore V, Sanprasert V, Nutman TB, (2011) Functional and phenotypic characteristics of alternative activation induced in human monocytes by interleukin-4 or the parasitic nematode Brugia malayi. Infect Immun 79: 3957–3965.
50. Gan AM, Butoi ED, Manea A, Simion V, Stan D, et al. (2013) Inflammatory effects of resistin on human smooth muscle cells: up-regulation of fractalkine and its receptor, CX3CR1 expression by TLR4 and Gi-protein pathways. Cell Tissue Res 351: 161–174.
51. Silswal N, Singh AK, Aruna B, Mukhopadhyay S, Ghosh S, et al. (2005) Human resistin stimulates the pro-inflammatory cytokines TNF-alpha and IL-12 in macrophages by NF-kappaB-dependent pathway. Biochem Biophys Res Commun 334: 1092–1101.
52. Tarkowski A, Bjersing J, Shestakov A, Bokarewa MI, (2010) Resistin competes with lipopolysaccharide for binding to toll-like receptor 4. J Cell Mol Med 14: 1419–1431.
53. Pirvulescu MM, Gan AM, Stan D, Simion V, Calin M, et al. (2014) Subendothelial resistin enhances monocyte transmigration in a co-culture of human endothelial and smooth muscle cells by mechanisms involving fractalkine, MCP-1 and activation of TLR4 and Gi/o proteins signaling. Int J Biochem Cell Biol 50: 29–37.
54. Lee S, Lee HC, Kwon YW, Lee SE, Cho Y, et al. (2014) Adenylyl cyclase-associated protein 1 is a receptor for human resistin and mediates inflammatory actions of human monocytes. Cell Metab 19: 484–497.
55. Anuradha R, George PJ, Pavan Kumar N, Fay MP, Kumaraswami V, et al. (2012) Circulating microbial products and acute phase proteins as markers of pathogenesis in lymphatic filarial disease. PLoS Pathog 8: e1002749.
56. George PJ, Anuradha R, Kumar NP, Kumaraswami V, Nutman TB, et al. (2012) Evidence of microbial translocation associated with perturbations in T cell and antigen-presenting cell homeostasis in hookworm infections. PLoS Negl Trop Dis 6: e1830.
57. Babu S, Nutman TB, (2012) Immunopathogenesis of lymphatic filarial disease. Semin Immunopathol 34: 847–861.
58. Wang J, Gusti V, Saraswati A, Lo DD, (2011) Convergent and divergent development among M cell lineages in mouse mucosal epithelium. J Immunol 187: 5277–5285.