Allergy: TGFβ receptor mutations impose a strong predisposition for human allergic disease

Science Translational Medicine

Volumn 5, Issue 195, 2013, Pages

  Frischmeyer Guerrerio, Pamela A ^a   Guerrerio, Anthony L ^a   Oswald, Gretchen ^a   Chichester, Kristin ^a   Myers, Loretha ^a   Halushka, Marc K ^a   Oliva Hemker, Maria ^a   Wood, Robert A ^a   Dietz, Harry C ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN E; INTERLEUKIN 13; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 2; CYTOKINE; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, HUMAN; PROTEIN SERINE THREONINE KINASE; TRANSFORMING GROWTH FACTOR BETA TYPE II RECEPTOR; TRANSFORMING GROWTH FACTOR-BETA TYPE II RECEPTOR;

ADOLESCENT; ADULT; ALLERGIC DISEASE; ALLERGIC RHINITIS; ARTICLE; ASTHMA; CD4+ T LYMPHOCYTE; CHILD; CONTROLLED STUDY; CYTOKINE PRODUCTION; ECZEMA; EOSINOPHIL COUNT; EOSINOPHILIC GASTROINTESTINAL DISORDER; FEMALE; FOOD ALLERGY; GENE MUTATION; GENETIC PREDISPOSITION; HUMAN; HUMAN CELL; HUMAN TISSUE; INTRACELLULAR SIGNALING; LOEYS DIETZ SYNDROME; LYMPHOCYTE COUNT; LYMPHOCYTE PROLIFERATION; MAJOR CLINICAL STUDY; MALE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RECEPTOR GENE; REGULATORY T LYMPHOCYTE; SCHOOL CHILD; TH2 CELL; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1 GENE; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 2 GENE; TRANSFORMING GROWTH FACTOR BETA RECEPTOR GENE; BLOOD; FLOW CYTOMETRY; GENETICS; HYPERSENSITIVITY; IMMUNOLOGY; METABOLISM; MUTATION;

CD4-POSITIVE T-LYMPHOCYTES; CYTOKINES; FLOW CYTOMETRY; FORKHEAD TRANSCRIPTION FACTORS; GENETIC PREDISPOSITION TO DISEASE; HUMANS; HYPERSENSITIVITY; IMMUNOGLOBULIN E; INTERLEUKIN-13; LOEYS-DIETZ SYNDROME; MUTATION; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; T-LYMPHOCYTES, REGULATORY;

EID: 84883028120     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3006448     Document Type: Article

References (58)

1. J. E. Markowitz, J. M. Spergel, E. Ruchelli, C. A. Liacouras, Elemental diet is an effective treatment for eosinophilic esophagitis in children and adolescents. Am. J. Gastroenterol. 98, 777-782 (2003).
2. J. M. Spergel, J. L. Beausoleil, M. Mascarenhas, C. A. Liacouras, The use of skin prick tests and patch tests to identify causative foods in eosinophilic esophagitis. J. Allergy Clin. Immunol. 109, 363-368 (2002).
3. M. F. Moffatt, I. G. Gut, F. Demenais, D. P. Strachan, E. Bouzigon, S. Heath, E. von Mutius, M. Farrall, M. Lathrop, W. O. Cookson; GABRIEL Consortium, A large-scale, consortium-based genomewide association study of asthma. N. Engl. J. Med. 363, 1211-1221 (2010).
4. H. Wu, I. Romieu, M. Shi, D. B. Hancock, H. Li, J. J. Sienra-Monge, G. Y. Chiu, H. Xu, B. E. del Rio-Navarro, S. J. London, Evaluation of candidate genes in a genome-wide association study of childhood asthma in Mexicans. J. Allergy Clin. Immunol. 125, 321-327.e13 (2010).
5. S. S. Aceves, R. O. Newbury, D. Chen, J. Mueller, R. Dohil, H. Hoffman, J. F. Bastian, D. H. Broide, Resolution of remodeling in eosinophilic esophagitis correlates with epithelial response to topical corticosteroids. Allergy 65, 109-116 (2010).
6. W.H. Oddy, M.Halonen, F.D. Martinez, I. C. Lohman, D. A. Stern, M. Kurzius-Spencer, S. Guerra, A. L. Wright, TGF-β in human milk is associated with wheeze in infancy. J. Allergy Clin. Immunol. 112, 723-728 (2003).
7. M. O. Li, S. Sanjabi, R. A. Flavell, Transforming growth factor-β controls development, homeostasis, and tolerance of T cells by regulatory T cell-dependent and -independent mechanisms. Immunity 25, 455-471 (2006).
8. P. R. Mangan, L. E. Harrington, D. B. O'Quinn, W. S. Helms, D. C. Bullard, C. O. Elson, R. D. Hatton, S. M. Wahl, T. R. Schoeb, C. T. Weaver, Transforming growth factor-β induces development of the TH17 lineage. Nature 441, 231-234 (2006).
9. M. Veldhoen, C. Uyttenhove, J. van Snick, H. Helmby, A. Westendorf, J. Buer, B. Martin, C. Wilhelm, B. Stockinger, Transforming growth factor-β 'reprograms' the differentiation of T helper 2 cells and promotes an interleukin 9-producing subset. Nat. Immunol. 9, 1341-1346 (2008).
10. - effector T cells. Nat. Immunol. 9, 1347-1355 (2008).
11. S. Sanjabi, L. A. Zenewicz, M. Kamanaka, R. A. Flavell, Anti-inflammatory and pro-inflammatory roles of TGF-β, IL-10, and IL-22 in immunity and autoimmunity. Curr. Opin. Pharmacol. 9, 447-453 (2009).
12. M. O. Li, R. A. Flavell, TGF-β: A master of all T cell trades. Cell 134, 392-404 (2008).
13. B. L. Loeys, J. Chen, E. R. Neptune, D. P. Judge, M. Podowski, T. Holm, J. Meyers, C. C. Leitch, N. Katsanis, N. Sharifi, F. L. Xu, L. A. Myers, P. J. Spevak, D. E. Cameron, J. De Backer, J. Hellemans, Y. Chen, E. C. Davis, C. L. Webb, W. Kress, P. Coucke, D. B. Rifkin, A. M. De Paepe, H. C. Dietz, A syndrome of altered cardiovascular, craniofacial, neurocognitive and skeletal development caused by mutations in TGFBR1 or TGFBR2. Nat. Genet. 37, 275-281 (2005).
14. S. A. Bock, Prospective appraisal of complaints of adverse reactions to foods in children during the first 3 years of life. Pediatrics 79, 683-688 (1987).
15. H. A. Sampson, Update on food allergy. J. Allergy Clin. Immunol. 113, 805-819 (2004).
16. A. H. Liu, R. Jaramillo, S. H. Sicherer, R. A. Wood, S. A. Bock, A. W. Burks, M. Massing, R. D. Cohn, D. C. Zeldin, National prevalence and risk factors for food allergy and relationship to asthma: Results from the National Health and Nutrition Examination Survey 2005-2006. J. Allergy Clin. Immunol. 126, 798-806.e14 (2010).
17. Trends in Asthma Morbidity and Mortality (American Lung Association, Epidemiology and Statistics Unit, Research and Program Services, Washington, DC, 2011).
18. Vital Statistics (Centers for Disease Control and Prevention, Atlanta, GA, 2011).
19. B. Bloom, R. A. Cohen, G. Freeman, Summary health statistics for U.S. children: National Health Interview Survey, 2010. Vital Health Stat. 10 250, 1-80 (2011).
20. J. R. Pleis, B. W. Ward, J. W. Lucas, Summary health statistics for U.S. adults: National Health Interview Survey, 2009. Vital Health Stat. 10 249, 1-207 (2010).
21. K. Singh, S. Axelrod, L. Bielory, The epidemiology of ocular and nasal allergy in the United States, 1988-1994. J. Allergy Clin. Immunol. 126, 778-783.e776 (2010).
22. E. O. Meltzer, M. S. Blaiss, M. J. Derebery, T. A. Mahr, B. R. Gordon, K. K. Sheth, A. L. Simmons, M. A. Wingertzahn, J. M. Boyle, Burden of allergic rhinitis: Results from the Pediatric Allergies in America survey. J. Allergy Clin. Immunol. 124, S43-S70 (2009).
23. T. E. Shaw, G. P. Currie, C. W. Koudelka, E. L. Simpson, Eczema prevalence in the United States: Data from the 2003 National Survey of Children's Health. J. Invest. Dermatol. 131, 67-73 (2011).
24. J. M. Hanifin, M. L. Reed; Eczema Prevalence and Impact Working Group, A population-based survey of eczema prevalence in the United States. Dermatitis 18, 82-91 (2007).
25. D. Laughter, J. A. Istvan, S. J. Tofte, J. M. Hanifin, The prevalence of atopic dermatitis in Oregon schoolchildren. J. Am. Acad. Dermatol. 43, 649-655 (2000).
26. R. J. Noel, P. E. Putnam, M. E. Rothenberg, Eosinophilic esophagitis. N. Engl. J. Med. 351, 940-941 (2004).
27. J. M. Spergel, W. M. Book, E. Mays, L. Song, S. S. Shah, N. J. Talley, P. A. Bonis, Variation in prevalence, diagnostic criteria, and initial management options for eosinophilic gastrointestinal diseases in the United States. J. Pediatr. Gastroenterol. Nutr. 52, 300-306 (2011).
28. W. C. Huang, F. C. Yen, F. S. Shie, C. M. Pan, Y. J. Shiao, C. N. Yang, F. L. Huang, Y. J. Sung, H. J. Tsay, TGF-β1 blockade of microglial chemotaxis toward Aβ aggregates involves SMAD signaling and down-regulation of CCL5. J. Neuroinflammation 7, 28 (2010).
29. + T cells expressing the FoxP3 transcription factor. Immunity 30, 899-911 (2009).
30. Y. Wang, A. Souabni, R. A. Flavell, Y. Y. Wan, An intrinsic mechanism predisposes Foxp3- expressing regulatory T cells to Th2 conversion in vivo. J. Immunol. 185, 5983-5992 (2010).
31. + T cell transcription factors. Nat. Rev. Immunol. 12, 799-804 (2012).
32. + regulatory T cells. PLoS One 7, e34547 (2012).
33. D. S. Lim, S. Lutucuta, P. Bachireddy, K. Youker, A. Evans, M. Entman, R. Roberts, A. J. Marian, Angiotensin II blockade reverses myocardial fibrosis in a transgenic mouse model of human hypertrophic cardiomyopathy. Circulation 103, 789-791 (2001).
34. P. Lavoie, G. Robitaille, M. Agharazii, S. Ledbetter, M. Lebel, R. Larivière, Neutralization of transforming growth factor-β attenuates hypertension and prevents renal injury in uremic rats. J. Hypertens. 23, 1895-1903 (2005).
35. J. P. Habashi, D. P. Judge, T. M. Holm, R. D. Cohn, B. L. Loeys, T. K. Cooper, L. Myers, E. C. Klein, G. Liu, C. Calvi, M. Podowski, E. R. Neptune, M. K. Halushka, D. Bedja, K. Gabrielson, D. B. Rifkin, L. Carta, F. Ramirez, D. L. Huso, H. C. Dietz, Losartan, an AT1 antagonist, prevents aortic aneurysm in a mouse model of Marfan syndrome. Science 312, 117-121 (2006).
36. S. H. Sicherer, T. J. Furlong, H. H. Maes, R. J. Desnick, H. A. Sampson, B. D. Gelb, Genetics of peanut allergy: A twin study. J. Allergy Clin. Immunol. 106, 53-56 (2000).
37. M. E. Rothenberg, J. M. Spergel, J. D. Sherrill, K. Annaiah, L. J. Martin, A. Cianferoni, L. Gober, C. Kim, J. Glessner, E. Frackelton, K. Thomas, C. Blanchard, C. Liacouras, R. Verma, S. Aceves, M. H. Collins, T. Brown-Whitehorn, P. E. Putnam, J. P. Franciosi, R. M. Chiavacci, S. F. Grant, J. P. Abonia, P. M. Sleiman, H. Hakonarson, Common variants at 5q22 associate with pediatric eosinophilic esophagitis. Nat. Genet. 42, 289-291 (2010).
38. C. Ober, T. C. Yao, The genetics of asthma and allergic disease: A 21st century perspective. Immunol. Rev. 242, 10-30 (2011).
39. W. M. Grady, L. L. Myeroff, S. E. Swinler, A. Rajput, S. Thiagalingam, J. D. Lutterbaugh, A. Neumann, M. G. Brattain, J. Chang, S. J. Kim, K. W. Kinzler, B. Vogelstein, J. K. Willson, S. Markowitz, Mutational inactivation of transforming growth factor b receptor type II in microsatellite stable colon cancers. Cancer Res. 59, 320-324 (1999).
40. T. Mizuguchi, G. Collod-Beroud, T. Akiyama, M. Abifadel, N. Harada, T. Morisaki, D. Allard, M. Varret, M. Claustres, H. Morisaki, M. Ihara, A. Kinoshita, K. Yoshiura, C. Junien, T. Kajii, G. Jondeau, T. Ohta, T. Kishino, Y. Furukawa, Y. Nakamura, N. Niikawa, C. Boileau, N. Matsumoto, Heterozygous TGFBR2 mutations in Marfan syndrome. Nat. Genet. 36, 855-860 (2004).
41. R. Wieser, J. L. Wrana, J. Massagué, GS domain mutations that constitutively activate TbR-I, the downstream signaling component in the TGF-β receptor complex. EMBO J. 14, 2199-2208 (1995).
42. C. Dai, X. Wen, W. He, Y. Liu, Inhibition of proinflammatory RANTES expression by TGF-β1 is mediated by glycogen synthase kinase-3β- dependent β-catenin signaling. J. Biol. Chem. 286, 7052-7059 (2011).
43. + regulatory T cells in human autoimmune disease. Nat. Med. 17, 673-675 (2011).
44. Q. Zhang, J. C. Davis, I. T. Lamborn, A. F. Freeman, H. Jing, A. J. Favreau, H. F. Matthews, J. Davis, M. L. Turner, G. Uzel, S. M. Holland, H. C. Su, Combined immunodeficiency associated with DOCK8 mutations. N. Engl. J. Med. 361, 2046-2055 (2009).
45. Y. Minegishi, M. Saito, T. Morio, K. Watanabe, K. Agematsu, S. Tsuchiya, H. Takada, T. Hara, N. Kawamura, T. Ariga, H. Kaneko, N. Kondo, I. Tsuge, A. Yachie, Y. Sakiyama, T. Iwata, F. Bessho, T. Ohishi, K. Joh, K. Imai, K. Kogawa, M. Shinohara, M. Fujieda, H. Wakiguchi, S. Pasic, M. Abinun, H. D. Ochs, E. D. Renner, A. Jansson, B. H. Belohradsky, A. Metin, N. Shimizu, S.Mizutani, T.Miyawaki, S. Nonoyama, H. Karasuyama, Human tyrosine kinase 2 deficiency reveals its requisite roles in multiple cytokine signals involved in innate and acquired immunity. Immunity 25, 745-755 (2006).
46. D. V. Wallace, M. S. Dykewicz, D. I. Bernstein, J. Blessing-Moore, L. Cox, D. A. Khan, D. M. Lang, R. A. Nicklas, J. Oppenheimer, J. M. Portnoy, C. C. Randolph, D. Schuller, S. L. Spector, S. A. Tilles; Joint Task Force on Practice; American Academy of Allergy; Asthma & Immunology; American College of Allergy; Asthma and Immunology; Joint Council of Allergy, Asthma and Immunology, The diagnosis and management of rhinitis: An updated practice parameter. J. Allergy Clin. Immunol. 122, S1-S84 (2008).
47. D. Y. Leung, R. A. Nicklas, J. T. Li, I. L. Bernstein, J. Blessing-Moore, M. Boguniewicz, J. A. Chapman, D. A. Khan, D. Lang, R. E. Lee, J. M. Portnoy, D. E. Schuller, S. L. Spector, S. A. Tilles, Disease management of atopic dermatitis: An updated practice parameter. Joint Task Force on Practice Parameters. Ann. Allergy Asthma Immunol. 93, S1-S21 (2004).
48. S. Roy-Ghanta, D. F. Larosa, D. A. Katzka, Atopic characteristics of adult patients with eosinophilic esophagitis. Clin. Gastroenterol. Hepatol. 6, 531-535 (2008).
49. C. Blanchard, M. E. Rothenberg, Basic pathogenesis of eosinophilic esophagitis. Gastrointest. Endosc. Clin. N. Am. 18, 133-143 (2008).
50. T. F. Brown-Whitehorn, J. M. Spergel, The link between allergies and eosinophilic esophagitis: Implications for management strategies. Expert Rev. Clin. Immunol. 6, 101-109 (2010).
51. A. Mishra, S. P. Hogan, E. B. Brandt, M. E. Rothenberg, IL-5 promotes eosinophil trafficking to the esophagus. J. Immunol. 168, 2464-2469 (2002).
52. M. Toda, D. Y. Leung, S. Molet, M. Boguniewicz, R. Taha, P. Christodoulopoulos, T. Fukuda, J. A. Elias, Q. A. Hamid, Polarized in vivo expression of IL-11 and IL-17 between acute and chronic skin lesions. J. Allergy Clin. Immunol. 111, 875-881 (2003).
53. R. Halwani, S. Al-Muhsen, H. Al-Jahdali, Q. Hamid, Role of transforming growth factor-β in airway remodeling in asthma. Am. J. Respir. Cell Mol. Biol. 44, 127-133 (2011).
54. L. G. Gregory, S. A. Mathie, S. A. Walker, S. Pegorier, C. P. Jones, C. M. Lloyd, Overexpression of Smad2 drives house dust mite-mediated airway remodeling and airway hyperresponsiveness via activin and IL-25. Am. J. Respir. Crit. Care Med. 182, 143-154 (2010).
55. L. Zuo, P. C. Fulkerson, F. D. Finkelman, M. Mingler, C. A. Fischetti, C. Blanchard, M. E. Rothenberg, IL-13 induces esophageal remodeling and gene expression by an eosinophil-independent, IL-13Rα2-inhibited pathway. J. Immunol. 185, 660-669 (2010).
56. P. A. Frischmeyer-Guerrerio, A. L. Guerrerio, K. L. Chichester, A. P. Bieneman, R. A. Hamilton, R. A. Wood, J. T. Schroeder, Dendritic cell and T cell responses in children with food allergy. Clin. Exp. Allergy 41, 61-71 (2011).
57. N. M. Kjellman, S. G. Johansson, A. Roth, Serum IgE levels in healthy children quantified by a sandwich technique (PRIST). Clin. Allergy 6, 51-59 (1976).
58. C. R. Jolliff, K. M. Cost, P. C. Stivrins, P. P. Grossman, C. R. Nolte, S. M. Franco, K. J. Fijan, L. L. Fletcher, H. C. Shriner, Reference intervals for serum IgG, IgA, IgM, C3, and C4 as determined by rate nephelometry. Clin. Chem. 28, 126-128 (1982).