Evolution of IL4 and pathogen antagonism

Growth Factors

Volumn 29, Issue 4, 2011, Pages 153-160

  Pillai, Meenu R ^a   Bix, Mark ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

Evolution; Gastrointestinal nematode; Interleukin 4; Pathogen antagonism

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 13; INTERLEUKIN 15; INTERLEUKIN 2; INTERLEUKIN 21; INTERLEUKIN 4; INTERLEUKIN 4 RECEPTOR ALPHA; INTERLEUKIN 7; INTERLEUKIN 9; PROTEIN KINASE R; STAT PROTEIN;

ARTICLE; CELL DIFFERENTIATION; CYTOKINE PRODUCTION; CYTOKINE RELEASE; CYTOKINE RESPONSE; ENZYME ACTIVATION; HOST PARASITE INTERACTION; HOST RESISTANCE; LIGAND BINDING; MACROPHAGE; MOLECULAR EVOLUTION; NATURAL KILLER T CELL; NEMATODE; NONHUMAN; PHYLOGENETIC TREE; PRIORITY JOURNAL; RESPIRATORY TRACT DISEASE; SEQUENCE ANALYSIS; TH2 CELL;

ANIMALS; BIOLOGICAL EVOLUTION; EVOLUTION, MOLECULAR; GASTROINTESTINAL TRACT; HOST-PARASITE INTERACTIONS; HUMANS; IMMUNOGLOBULIN CLASS SWITCHING; INTERLEUKIN-4; INTERLEUKIN-4 RECEPTOR ALPHA SUBUNIT; MACROPHAGES; NEMATODA; NEMATODE INFECTIONS; PROTEIN BINDING; SELECTION, GENETIC;

EUTHERIA; MAMMALIA; NEMATODA;

EID: 79960346953     PISSN: 08977194     EISSN: 10292292     Source Type: Journal    
DOI: 10.3109/08977194.2011.590138     Document Type: Article

References (75)

1. Alcami A, Smith GL. 1992. A soluble receptor for interleukin-1 beta encoded by vaccinia virus: A novel mechanism of virus modulation of the host response to infection. Cell 71(1): 153-167.
2. Bancroft AJ, Artis D, Donaldson DD, Sypek JP, Grencis RK. 2000. Gastrointestinal nematode expulsion in IL-4 knockout mice is IL-13 dependent. Eur J Immunol 30(7):2083-2091. (Pubitemid 30456205)
3. Barner M, Mohrs M, Brombacher F, Kopf M. 1998. Differences between IL-4R alpha-deficient and IL-4-deficient mice reveal a role for IL-13 in the regulation of Th2 responses. Curr Biol 8(11):669-672. (Pubitemid 28257973)
4. Bergstrom CT, Lachmann M. 2003. The Red King effect: When the slowest runner wins the coevolutionary race. Proc Natl Acad Sci USA 100(2):593-598. (Pubitemid 36126097)
5. Bix M, Wang ZE, Thiel B, Schork NJ, Locksley RM. 1998. Genetic regulation of commitment to interleukin 4 production by a CD4(\+) T cell-intrinsic mechanism. J Exp Med 188(12): 2289-2299. (Pubitemid 29028501)
6. Chen H, Paul WE. 1997. Cultured NK1.1 + CD4 + T cells produce large amounts of IL-4 and IFN-gamma upon activation by anti-CD3 or CD1. J Immunol 159(5):2240-2249. (Pubitemid 127681014)
7. Chen L, Grabowski KA, Xin J-P, Coleman J, Huang Z, Espiritu B, Alkan S, Xie HB, Zhu Y, White FA, Clancy J, Jr, Huang H. 2004. IL-4 induces differentiation and expansion of Th2 cytokine-producing eosinophils. J Immunol 172(4):2059-2066. (Pubitemid 38182351)
8. Clemens MJ, Elia A. 1997. The double-stranded RNA-dependent protein kinase PKR: Structure and function. J Interferon Cytokine Res 17(9):503-524. (Pubitemid 27475916)
9. Coffman RL, Ohara J, Bond MW, Carty J, Zlotnik A, Paul WE. 1986. B cell stimulatory factor-1 enhances the IgE response of lipopolysaccharide-activated B cells. J Immunol 136(12): 4538-4541. (Pubitemid 16090673)
10. Elde NC, Child SJ, Geballe AP, Malik HS. 2009. Protein kinase R reveals an evolutionary model for defeating viral mimicry. Nature 457(7228):485-489.
11. Else KJ, Finkelman FD, Maliszewski CR, Grencis RK. 1994. Cytokine-mediated regulation of chronic intestinal helminth infection. J Exp Med 179(1):347-351. (Pubitemid 24013003)
12. Finkelman FD, Shea-Donohue T, Goldhill J, Sullivan CA, Morris SC, Madden KB, Gause WC, Urban JF, Jr. 1997. Cytokine regulation of host defense against parasitic gastrointestinal nematodes: Lessons from studies with rodent models. Annu Rev Immunol 15:505-533. (Pubitemid 27169291)
13. Gascan H, Gauchat J-F, de Waal Malefyt R, Schneider P, Yssel H, de Vries JE. 1991. Regulation of human IgE synthesis. Clin Exp Allergy 21(Suppl 1):162-166.
14. Gomez-Escobar N, Lewis E, Maizels RM. 1998. A novel member of the transforming growth factor-beta (TGF-beta) superfamily from the filarial nematodes Brugia malayi and B. pahangi. Exp Parasitol 88(3):200-209. (Pubitemid 28375787)
15. Gomez-Escobar N, Gregory WF, Maizels RM. 2000. Identification of tgh-2, a filarial nematode homolog of Caenorhabditis elegans daf-7 and human transforming growth factor beta, expressed in microfilarial and adult stages of Brugia malayi. Infect Immun 68(11):6402-6410.
16. Grencis RK, Entwistle GM. 1997. Production of an interferon-gamma homologue by an intestinal nematode: Functionally significant or interesting artefact? Parasitology 115 Suppl: S101-S106. (Pubitemid 28166138)
17. Grunig G, Warnock M, Wakil AE, Venkayya R, Brombacher F, Rennick DM, Sheppard D, Mohrs M, Donaldson DD, Locksley RM, Corry DB. 1998. Requirement for IL-13 independently of IL-4 in experimental asthma. Science 282(5397):2261-2263. (Pubitemid 29004075)
18. Hammad H, Plantinga M, Deswarte K, Pouliot P, Willart MA, Kool M, Muskens F, Lambrecht BN. 2010. Inflammatory dendritic cells\not basophils\are necessary and sufficient for induction of Th2 immunity to inhaled house dust mite allergen. J Exp Med 207(10):2097-2111.
19. Herbert DR, Hölscher C, Mohrs M, Arendse B, Schwegmann A, Radwanska M, Leeto M, Kirsch R, Hall P, Mossmann H, Claussen B, Förster I, Brombacher F. 2004. Alternative macrophage activation is essential for survival during schistoso-miasis and downmodulates T helper 1 responses and immuno-pathology. Immunity 20(5):623-635. (Pubitemid 38659504)
20. Howard M, Farrar J, Hilfiker M, Johnson B, Takatsu K, Hamaoka T, Paul WE. 1982. Identification of a T cell-derived B cell growth factor distinct from interleukin 2. J Exp Med 155: 914-923. (Pubitemid 12187863)
21. Hu FQ, Smith CA, Pickup DJ. 1994. Cowpox virus contains two copies of an early gene encoding a soluble secreted form of the type II TNF receptor. Virology 204(1):343-356. (Pubitemid 24305347)
22. Hughes AL, Nei M. 1988. Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals over-dominant selection. Nature 335(6186):167-170.
23. Junttila IS, Mizukami K, Dickensheets H, Meier-Schellersheim M, Yamane H, Donnelly RP, Paul WE. 2008. Tuning sensitivity to IL-4 and IL-13: Differential expression of IL-4Ralpha, IL-13Ralpha1, and gammac regulates relative cytokine sensitivity. J Exp Med 205(11):2595-2608.
24. Kashiwada M, Levy DM, McKeag L, Murray K, Schröder AJ, Canfield SM, Traver G, Rothman PB. 2010. IL-4-induced transcription factor NFIL3/E4BP4 controls IgE class switching. Proc Natl Acad Sci USA 107(2):821-826.
25. Kimura M. 1979. The neutral theory of molecular evolution. Sci Am 241(5):98-100, 102, 108 passim.
26. Koyanagi M, Kerns JA, Chung L, Zhang Y, Brown S, Moldoveanu T, Malik HS, Bix M. 2010. Diversifying selection and functional analysis of interleukin-4 suggests antagonism-driven evolution at receptor-binding interfaces. BMC Evol Biol 10:223-236.
27. Kraich M, Klein M, Patiño E, Harrer H, Nickel J, Sebald W, Mueller TD. 2006. A modular interface of IL-4 allows for scalable affinity without affecting specificity for the IL-4 receptor. BMC Biol 4:13-31.
28. Kronenberg M, Gapin L. 2002. The unconventional lifestyle of NKT cells. Nat Rev Immunol 2(8):557-568. (Pubitemid 37328731)
29. Langland JO, Cameron JM, Heck MC, Jancovich JK, Jacobs BL. 2006. Inhibition of PKR by RNA and DNA viruses. Virus Res 119(1):100-110. (Pubitemid 43765973)
30. LaPorte SL, Juo ZS, Vaclavikova J, Colf LA, Qi X, Heller NM, Keegan AD, Garcia KC. 2008. Molecular and structural basis of cytokine receptor pleiotropy in the interleukin-4/13 system. Cell 132(2):259-272. (Pubitemid 351172435)
31. Le Gros G, Ben-Sasson SZ, Seder R, Finkelman FD, Paul WE. 1990. Generation of interleukin 4 (IL-4)-producing cells in vivo and in vitro: IL-2 and IL-4 are required for in vitro generation of IL-4-producing cells. J Exp Med 172(3):921-929. (Pubitemid 20301238)
32. Li WH, Wu CI, Luo CC. 1985. A new method for estimating synonymous and nonsynonymous rates of nucleotide substitution considering the relative likelihood of nucleotide and codon changes. Mol Biol Evol 2(2):150-174. (Pubitemid 15239737)
33. Liu Z, Liu Q, Pesce J, Anthony RM, Lamb E, Whitmire J, Hamed H, Morimoto M, Urban JF, Jr, Gause WC. 2004. Requirements for the development of IL-4-producing T cells during intestinal nematode infections: What it takes to make a Th2 cell in vivo. Immunol Rev 201:57-74. (Pubitemid 39318444)
34. Maizels RM, Holland MJ. 1998. Parasite immunology: Pathways for expelling intestinal helminths. Curr Biol 8(20):R711-R714. (Pubitemid 28501364)
35. Maizels RM, Yazdanbakhsh M. 2003. Immune regulation by helminth parasites: Cellular and molecular mechanisms. Nat Rev Immunol 3(9):733-744. (Pubitemid 41070814)
36. Martinez FO, Helming L, Gordon S. 2009. Alternative activation of macrophages: An immunologic functional perspective. Annu Rev Immunol 27:451-483.
37. McKenzie GJ, Bancroft A, Grencis RK, McKenzie AN. 1998. A distinct role for interleukin-13 in Th2-cell-mediated immune responses. Curr Biol 8(6):339-342. (Pubitemid 28159120)
38. McKenzie GJ, Fallon PG, Emson CL, Grencis RK, McKenzie AN. 1999. Simultaneous disruption of interleukin (IL)-4 and IL-13 defines individual roles in T helper cell type 2-mediated responses. J Exp Med 189(10):1565-1572. (Pubitemid 29240881)
39. Min B, Prout M, Hu-Li J, Zhu J, Jankovic D, Morgan ES, Urban JF, Jr, Dvorak AM, Finkelman FD, LeGros G, Paul WE. 2004. Basophils produce IL-4 and accumulate in tissues after infection with a Th2-inducing parasite. J Exp Med 200(4):507-517. (Pubitemid 39121907)
40. Moore KW, Vieira P, Fiorentino DF, Trounstine ML, Khan TA, Mosmann TR. 1990. Homology of cytokine synthesis inhibitory factor (IL-10) to the Epstein-Barr virus gene BCRFI. Science 248:1230-1234.
41. Moore PS, Boshoff C, Weiss RA, Chang Y. 1996. Molecular mimicry of human cytokine and cytokine response pathway genes by KSHV. Science 274(5293):1739-1744. (Pubitemid 26414912)
42. Mueller TD, Zhang JL, Sebald W, Duschl A. 2002. Structure, binding, and antagonists in the IL-4/IL-13 receptor system. Biochim Biophys Acta 1592(3):237-250. (Pubitemid 35284881)
43. Nelms K, Huang H, Ryan J, Keegan A, Paul WE. 1999. The IL-4 receptor: Signaling mechanisms and biologic functions. Annu Rev Immunol 17:701-738. (Pubitemid 29241138)
44. Noben-Trauth N, Hu-Li J, Paul WE. 2002. IL-4 secreted from individual naive CD4\+ T cells acts in an autocrine manner to induce Th2 differentiation. Eur J Immunol 32(5):1428-1433. (Pubitemid 34546271)
45. Noelle R, Krammer PH, Ohara J, Uhr JW, Vitetta ES. 1984. Increased expression of Ia antigens on resting B cells: An additional role for B-cell growth factor. Proc Natl Acad Sci USA 81(19):6149-6153. (Pubitemid 15220797)
46. O'Connell MJ, McInerney JO. 2005. Gamma chain receptor interleukins: Evidence for positive selection driving the evolution of cell-to-cell communicators in the mammalian immune system. J Mol Evol 61(5):608-619. (Pubitemid 41598607)
47. Ohnmacht C, Schwartz C, Panzer M, Schiedewitz I, Naumann R, Voehringer D. 2010. Basophils orchestrate chronic allergic dermatitis and protective immunity against helminths. Immunity 33(3):364-374.
48. Okamoto M, Van Stry M, Chung L, Koyanagi M, Sun X, Suzuki Y, Ohara O, Kitamura H, Hijikata A, Kubo M, Bix M. 2009. Mina, an Il4 repressor, controls T helper type 2 bias. Nat Immunol 10(8):872-879.
49. Pastrana DV, Raghavan N, FitzGerald P, Eisinger SW, Metz C, Bucala R, Schleimer RP, Bickel C, Scott AL. 1998. Filarial nematode parasites secrete a homologue of the human cytokine macrophage migration inhibitory factor. Infect Immun 66(12): 5955-5963. (Pubitemid 28531858)
50. Paul WE, Zhu J. 2010. How are T(H)2-type immune responses initiated and amplified? Nat Rev Immunol 10(4):225-235.
51. Perkins C, Wills-Karp M, Finkelman FD. 2006. IL-4 induces IL-13-independent allergic airway inflammation. J Allergy Clin Immunol 118(2):410-419. (Pubitemid 44142729)
52. Richter G, Blankenstein T, Diamantstein T. 1990. Evolutionary aspects, structure, and expression of the rat interleukin 4 gene. Cytokine 2(3):221-228.
53. Richter G, Hein G, Blankenstein T, Diamantstein T. 1995. The rat interleukin 4 receptor: Coevolution of ligand and receptor. Cytokine 7(3):237-241.
54. Rockman MV, Hahn MW, Soranzo N, Goldstein DB, Wray GA. 2003. Positive selection on a human-specific transcription factor binding site regulating IL4 expression. Curr Biol 13(23): 2118-2123. (Pubitemid 37502530)
55. Roehm NW, Leibson HJ, Zlotnik A, Kappler J, Marrack P, Cambier JC. 1984. Interleukin-induced increase in Ia expression by normal mouse B cells. J Exp Med 160(3):679-694. (Pubitemid 14074770)
56. Shen BJ, Hage T, Sebald W. 1996. Global and local determinants for the kinetics of interleukin-4/interleukin-4 receptor alpha chain interaction. A biosensor study employing recombinant inter-leukin-4-binding protein. Eur J Biochem 240(1):252-261. (Pubitemid 26276779)
57. Sokol CL, Chu NQ, Yu S, Nish SA, Laufer TM, Medzhitov R. 2009. Basophils function as antigen-presenting cells for an allergen-induced T helper type 2 response. Nat Immunol 10(7): 713-720.
58. Song HM, Jang AS, Ahn MH, Takizawa H, Lee SH, Kwon JH, Lee YM, Rhim TY, Park CS. 2008. Ym1 and Ym2 expression in a mouse model exposed to diesel exhaust particles. Environ Toxicol 23(1):110-116. (Pubitemid 351272446)
59. Swain SL, Weinberg AD, English M, Huston G. 1990. IL-4 directs the development of Th2-like helper effectors. J Immunol 145(11):3796-3806.
60. Upton C, Mossman K, McFadden G. 1992. Encoding of a homolog of the IFN-gamma receptor by myxoma virus. Science 258(5086):1369-1372. (Pubitemid 23007791)
61. Urban JF, Katona IM, Paul WE, Finkelman FD. 1991. Interleukin 4 is important in protective immunity to a gastrointestinal nematode infection in mice. Proc Natl Acad Sci USA 88(13): 5513-5517. (Pubitemid 21914775)
62. Urban JF, Jr, Noben-Trauth N, Donaldson DD, Madden KB, Morris SC, Collins M, Finkelman FD. 1998. IL-13, IL-4Ralpha, and Stat6 are required for the expulsion of the gastrointestinal nematode parasite Nippostrongylus brasiliensis. Immunity 8(2):255-264. (Pubitemid 28123752)
63. Urban JF, Jr, Noben-Trauth N, Schopf L, Madden KB, Finkelman FD. 2001. Cutting edge: IL-4 receptor expression by non-bone marrow-derived cells is required to expel gastrointestinal nematode parasites. J Immunol 167(11):6078-6081. (Pubitemid 33081531)
64. Vallance BA, Collins SM. 1998. The effect of nematode infection upon intestinal smooth muscle function. Parasite Immunol 20(5):249-253. (Pubitemid 28255398)
65. van Panhuys N, Tang S-C, Prout M, Camberis M, Scarlett D, Roberts J, Hu-Li J, Paul WE, Le Gros G. 2008. In vivo studies fail to reveal a role for IL-4 or STAT6 signaling in Th2 lymphocyte differentiation. Proc Natl Acad Sci USA 105(34): 12423-12428.
66. Van Valen L. 1973. A new evolutionary law. Evol Theory 1:1-30.
67. Voehringer D, Shinkai K, Locksley RM. 2004. Type 2 immunity reflects orchestrated recruitment of cells committed to IL-4 production. Immunity 20(3):267-277. (Pubitemid 38388229)
68. Wang Y, Shen BJ, Sebald W. 1997. A mixed-charge pair in human interleukin 4 dominates high-affinity interaction with the receptor alpha chain. Proc Natl Acad Sci USA 94(5): 1657-1662. (Pubitemid 27113891)
69. Weiss DL, Brown MA. 2001. Regulation of IL-4 production in mast cells: A paradigm for cell-type-specific gene expression. Immunol Rev 179:35-47. (Pubitemid 32175084)
70. Wills-Karp M. 1999. Immunologic basis of antigen-induced airway hyperresponsiveness. Annu Rev Immunol 17:255-281. (Pubitemid 29241125)
71. Wills-Karp M, Luyimbazi J, Xu X, Schofield B, Neben TY, Karp CL, Donaldson DD. 1998. Interleukin-13: Central mediator of allergic asthma. Science 282(5397):2258-2261. (Pubitemid 29004074)
72. Wu X, Di Rienzo A, Ober C. 2001. A population genetics study of single nucleotide polymorphisms in the interleukin 4 receptor alpha (IL4RA) gene. Genes Immun 2(3):128-134. (Pubitemid 33674877)
73. Yagi R, Suzuki W, Seki N, Kohyama M, Inoue T, Arai T, Kubo M. 2002. The IL-4 production capability of different strains of naive CD4(\+) T cells controls the direction of the T(h) cell response. Int Immunol 14(1):1-11. (Pubitemid 34083392)
74. Zhang JL, Simeonowa I, Wang Y, Sebald W. 2002. The high-affinity interaction of human IL-4 and the receptor alpha chain is constituted by two independent binding clusters. J Mol Biol 315(3):399-407. (Pubitemid 34729348)
75. Zhou B, Headley MB, Aye T, Tocker J, Comeau MR, Ziegler SF. 2008. Reversal of thymic stromal lymphopoietin-induced airway inflammation through inhibition of Th2 responses. J Immunol 181(9):6557-6562.