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  • 제16권4호
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  • Pages.201-210
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  • 2016
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  • 1598-2629(pISSN)
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  • 2092-6685(eISSN)
대한면역학회 (The Korean Association of Immunobiologists)
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STAT6 and PARP Family Members in the Development of T Cell-dependent Allergic Inflammation

  • Purna Krishnamurthy (Department of Pediatrics, Wells Center for Pediatric Research, Indiana University School of Medicine) ;
  • Mark H. Kaplan (Department of Pediatrics, Wells Center for Pediatric Research, Indiana University School of Medicine)
  • 투고 : 2016.05.04
  • 심사 : 2016.07.20
  • 발행 : 2016.08.31
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초록

Allergic inflammation requires the orchestration of altered gene expression in the target tissue and in the infiltrating immune cells. The transcription factor STAT6 is critical in activating cytokine gene expression and cytokine signaling both in the immune cells and in target tissue cells including airway epithelia, keratinocytes and esophageal epithelial cells. STAT6 is activated by the cytokines IL-4 and IL-13 to mediate the pathogenesis of allergic disorders such as asthma, atopic dermatitis, food allergy and eosinophilic esophagitis (EoE). In this review, we summarize the role of STAT6 in allergic diseases, its interaction with the co-factor PARP14 and the molecular mechanisms by which STAT6 and PARP14 regulate gene transcription.

키워드

과제정보

The authors dedicate this article to the memory of Shreevrat Goenka who began the PARP14/ARTD8/Coast6 field a decade ago.

참고문헌

  1. Levy, D. E., and J. E. Darnell. 2002. Stats: transcriptional control and biological impact. Nat. Rev. Mol. Cell Biol. 3: 651-662. 
  2. Galli, S. J., M. Tsai, and A. M. Piliponsky. 2008. The development of allergic inflammation. Nature 454: 445-454. 
  3. Quelle, F. W., K. Shimoda, W. Thierfelder, C. Fischer, A. Kim, S. M. Ruben, J. L. Cleveland, J. H. Pierce, A. D. Keegan, K. Nelms, W. E. Paul, and J. N. Ihle. 1995. Cloning of murine Stat6 and human Stat6, Stat proteins that are tyrosine phosphorylated in responses to IL-4 and IL-3 but are not required for mitogenesis. Mol. Cell. Biol. 15: 3336-3343. 
  4. Mikita, T., D. Campbell, P. Wu, K. Williamson, and U. Schindler. 1996. Requirements for interleukin-4-induced gene expression and functional characterization of Stat6. Mol. Cell. Biol. 16: 5811-5820. 
  5. Wurster, A. L., T. Tanaka, and M. J. Grusby. 2000. The biology of Stat4 and Stat6. Oncogene 19: 2577-2584. 
  6. Hebenstreit, D., G. Wirnsberger, J. Horejs-hoeck, and A. Duschl. 2006. Signaling mechanisms , interaction partners , and target genes of STAT6. Cytokine Growth Factor Rev. 17: 173-188. 
  7. Takeda, K., T. Tanaka, W. Shi, M. Matsumoto, M. Minami, S. Kashiwamura, K. Nakanishi, N. Yoshida, T. Kishimoto, and S. Akira. 1996. Essential role of Stat6 in IL-4 signalling. Nature 380: 627-630. 
  8. Shimoda, K., J. van Deursen, M. Y. Sangster, S. R. Sarawar, R. T. Carson, R. A. Tripp, C. Chu, F. W. Quelle, T. Nosaka, D. A. A. Vignali, P. C. Doherty, G. Grosveld, W. E. Paul, and J. N. Ihle. 1996. Lack of IL-4-induced Th2 response and IgE class switching in mice with disrupted Stat6 gene. Nature 380: 630-633. 
  9. Kaplan, M. H., U. Schindler, S. T. Smiley, and M. J. Grusby. 1996. Stat6 is required for mediating responses to IL-4 and for the development of Th2 cells. Immunity 4: 313-319. 
  10. Ouyang, W., M. Lohning, Z. Gao, M. Assenmacher, S. Ranganath, a Radbruch, and K. M. Murphy. 2000. Stat6-independent GATA-3 autoactivation directs IL-4-independent Th2 development and commitment. Immunity 12: 27-37. 
  11. Kuperman, D., B. Schofield, M. Wills-Karp, and M. J. Grusby. 1998. Signal transducer and activator of transcription factor 6 (Stat6)-deficient mice are protected from antigen-induced airway hyperresponsiveness and mucus production. J. Exp. Med. 187: 939-948. 
  12. Akimoto, T., F. Numata, M. Tamura, Y. Takata, N. Higashida, T. Takashi, K. Takeda, and S. Akira. 1998. Abrogation of bronchial eosinophilic inflammation and airway hyperreactivity in signal transducers and activators of transcription (STAT)6-deficient mice. J. Exp. Med. 187: 1537-1542. 
  13. Tomkinson, A., A. Kanehiro, N. Rabinovitch, A. Joetham, G. Cieslewicz, and E. W. Gelfand. 1999. The failure of STAT6-deficient mice to develop airway eosinophilia and airway hyperresponsiveness is overcome by interleukin-5. Am. J. Respir. Crit. Care Med. 160: 1283-1291. 
  14. Webb, D. C., A. N. J. McKenzie, A. M. L. Koskinen, M. Yang, J. Mattes, and P. S. Foster. 2000. Integrated signals between IL-13, IL-4, and IL-5 regulate airways hyperreactivity. J. Immunol. 165: 108-113. 
  15. Hoshino, A., T. Tsuji, J. Matsuzaki, T. Jinushi, S. Ashino, T. Teramura, K. Chamoto, Y. Tanaka, Y. Asakura, T. Sakurai, Y. Mita, A. Takaoka, S. Nakaike, T. Takeshima, H. Ikeda, and T. Nishimura. 2004. STAT6-mediated signaling in Th2-dependent allergic asthma: Critical role for the development of eosinophilia, airway hyper-responsiveness and mucus hypersecretion, distinct from its role in Th2 differentiation. Int. Immunol. 16: 1497-1505. 
  16. Elias, J. A., Z. Zhu, G. Chupp, and R. J. Homer. 1999. Airway remodeling in asthma. J. Clin. Invest. 104: 1001-1006. 
  17. Kuperman, D. A., X. Huang, L. L. Koth, G. H. Chang, G. M. Dolganov, Z. Zhu, J. A. Elias, D. Sheppard, and D. J. Erle. 2002. Direct effects of interleukin-13 on epithelial cells cause airway hyperreactivity and mucus overproduction in asthma. Nat. Med. 8: 885-889. 
  18. McCusker, C. T., Y. Wang, J. Shan, M. W. Kinyanjui, A. Villeneuve, H. Michael, and E. D. Fixman. 2007. Inhibition of experimental allergic airways disease by local application of a cell-penetrating dominant-negative STAT-6 peptide. J. Immunol. 179: 2556-2564. 
  19. Chiba, Y., M. Todoroki, Y. Nishida, M. Tanabe, and M. Misawa. 2009. A novel STAT6 inhibitor AS1517499 ameliorates antigen-induced bronchial hypercontractility in mice. Am. J. Respir. Cell Mol. Biol. 41: 516-524. 
  20. Hamid, Q., M. Boguniewicz, and D. Y. M. Leung. 1994. Differential in situ cytokine gene expression in acute versus chronic atopic dermatitis. J. Clin. Invest. 94: 870-6. 
  21. Palmer, C. N. A., A. D. Irvine, A. Terron-Kwiatkowski, Y. Zhao, H. Liao, S. P. Lee, D. R. Goudie, A. Sandilands, L. E. Campbell, F. J. D. Smith, G. M. O'Regan, R. M. Watson, J. E. Cecil, S. J. Bale, J. G. Compton, J. J. DiGiovanna, P. Fleckman, S. Lewis-Jones, G. Arseculeratne, A. Sergeant, C. S. Munro, B. El Houate, K. McElreavey, L. B. Halkjaer, H. Bisgaard, S. Mukhopadhyay, and W. H. I. McLean. 2006. Common loss-of-function variants of the epidermal barrier protein filaggrin are a major predisposing factor for atopic dermatitis. Nat. Genet. 38: 441-446. 
  22. Baurecht, H., A. D. Irvine, N. Novak, T. Illig, B. Buhler, J. Ring, S. Wagenpfeil, and S. Weidinger. 2007. Toward a major risk factor for atopic eczema: meta-analysis of filaggrin polymorphism data. J. Allergy Clin. Immunol. 120: 1406-1412. 
  23. Howell, M. D., B. E. Kim, P. Gao, A. V. Grant, M. Boguniewicz, A. DeBenedetto, L. Schneider, L. A. Beck, K. C. Barnes, and D. Y. M. Leung. 2007. Cytokine modulation of atopic dermatitis filaggrin skin expression. J. Allergy Clin. Immunol. 120: 150-155. 
  24. Kim, B. E., D. Y. M. Leung, M. Boguniewicz, and M. D. Howell. 2008. Loricrin and involucrin expression is downregulated by Th2 cytokines through STAT-6. Clin. Immunol. 126: 332-337. 
  25. Nomura, I., E. Goleva, M. D. Howell, Q. A. Hamid, P. Y. Ong, C. F. Hall, M. A. Darst, B. Gao, M. Boguniewicz, J. B. Travers, and D. Y. M. Leung. 2003. Cytokine milieu of atopic dermatitis, as compared to psoriasis, skin prevents induction of innate immune response genes. J. Immunol. 171: 3262-3269. 
  26. Bruns, H. A., U. Schindler, and M. H. Kaplan. 2003. Expression of a constitutively active Stat6 in vivo alters lymphocyte homeostasis with distinct effects in T and B cells. J. Immunol. Immunol. 170: 3478-3487. 
  27. Sehra, S., H. A. Bruns, A.-N. N. Ahyi, E. T. Nguyen, N. W. Schmidt, E. G. Michels, G.-U. von Bulow, and M. H. Kaplan. 2008. IL-4 is a critical determinant in the generation of allergic inflammation initiated by a constitutively active Stat6. J. Immunol. 180: 3551-3559. 
  28. Sehra, S., Y. Yao, M. D. Howell, E. T. Nguyen, G. S. Kansas, D. Y. M. Leung, J. B. Travers, and M. H. Kaplan. 2010. IL-4 regulates skin homeostasis and the predisposition toward allergic skin inflammation. J. Immunol. 184: 3186-3190. 
  29. Turner, M. J., S. Dasilva-arnold, N. Luo, X. Hu, C. C. West, L. Sun, C. Hall, J. Bradish, M. H. Kaplan, J. B. Travers, and Y. Sun. 2014. STAT6-mediated keratitis and blepharitis: a novel murine model of ocular atopic dermatitis. Invest. Ophthalmol. Vis. Sci. 55: 3803-3808. 
  30. Chan, L. S., N. Robinson, and L. Xu. 2001. Expression of interleukin-4 in the epidermis of transgenic mice results in a pruritic inflammatory skin disease: an experimental animal model to study atopic dermatitis. J. Invest. Dermatol. 117: 977-983. 
  31. Zheng, T., M. H. Oh, S. Y. Oh, J. T. Schroeder, A. B. Glick, and Z. Zhu. 2009. Transgenic expression of interleukin-13 in the skin induces a pruritic dermatitis and skin remodeling. J. Invest. Dermatol. 129: 742-751. 
  32. Sicherer, S. H., and D. Y. M. Leung. 2015. Advances in allergic skin disease, anaphylaxis, and hypersensitivity reactions to foods, drugs, and insects in 2014. J. Allergy Clin. Immunol. 135: 357-367. 
  33. Amoli, M., S. Hand, A. Hajeer, K. Jones, S. Rolf, C. Sting, B. Davies, and W. Ollier. 2002. Polymorphism in the Stat6 gene encodes risk for nut allergy. Genes Immun. 3: 220-224. 
  34. Hancock, D. B., I. Romieu, G. Y. Chiu, J.-J. Sienra-Monge, H. Li, B. E. del Rio-Navarro, and S. J. London. 2012. STAT6 and LRP1 polymorphisms are associated with food allergen sensitization in Mexican children. J. Allergy Clin. Immunol. 129: 1673-1676. 
  35. Kweon, M., M. Yamamoto, M. Kajiki, I. Takahashi, and H. Kiyono. 2000. Systemically derived large intestinal CD4+ Th2 cells play a central role in STAT6-mediated allergic diarrhea. J. Clin. Invest. 106: 199-206. 
  36. Brandt, E. B., A. Munitz, T. Orekov, M. K. Mingler, M. Mcbride, F. D. Finkelman, and M. E. Rothenberg. 2009. Targeting IL-4 / IL-13 signaling to alleviate oral allergen - induced diarrhea. J. Allergy Clin. Immunol. 123: 53-58. 
  37. Burton, O. T., A. R. Darling, J. S. Zhou, M. Noval-Rivas, T. G. Jones, M. F. Gurish, T. A. Chatila, and H. C. Oettgen. 2013. Direct effects of IL-4 on mast cells drive their intestinal expansion and increase susceptibility to anaphylaxis in a murine model of food allergy. Mucosal Immunol. 6: 740-750. 
  38. Forbes, E. E., K. Groschwitz, J. P. Abonia, E. B. Brandt, E. Cohen, C. Blanchard, R. Ahrens, L. Seidu, A. Mckenzie, R. Strait, F. D. Finkelman, P. S. Foster, K. I. Matthaei, M. E. Rothenberg, and S. P. Hogan. 2008. IL-9 - and mast cell - mediated intestinal permeability predisposes to oral antigen hypersensitivity. J. Exp. Med. 205: 897-913. 
  39. Chen, C., J. Lee, B. Liu, S. Ohta, P. Wang, A. V Kartashov, L. Mugge, J. P. Abonia, A. Barski, K. Izuhara, M. E. Rothenberg, F. D. Finkelman, and S. P. Hogan. 2015. Induction of interleukin-9-producing mucosal mast cells promotes susceptibility to IgE-mediated article induction of interleukin-9-producing mucosal mast cells promotes susceptibility to IgE-mediated experimental food allergy. Immunity 43: 1-15. 
  40. Mathias, C. B., S. A. Hobson, M. Garcia-lloret, G. Lawson, D. Poddighe, E.-J. Freyschmidt, W. Xing, M. F. Gurish, T. A. Chatila, and H. C. Oettgen. 2011. Mechanisms of allergy and clinical immunology IgE-mediated systemic anaphylaxis and impaired tolerance to food antigens in mice with enhanced IL-4 receptor signaling. J. Allergy Clin. Immunol. 127: 795-805. 
  41. Rivas, M. N., O. T. Burton, P. Wise, L. Charbonnier, P. Georgiev, H. C. Oettgen, R. Rachid, and T. A. Chatila. 2015. Regulatory T cell reprogramming toward a Th2-cell- like lineage impairs oral tolerance and promotes regulatory T cell reprogramming toward a Th2-cell-like lineage impairs oral tolerance and promotes food allergy. Immunity 42: 512-523. 
  42. Blanchard, C., S. Durual, M. Estienne, S. Emami, S. Vasseur, and J. C. Cuber. 2005. Eotaxin-3/CCL26 gene expression in intestinal epithelial cells is up-regulated by interleukin-4 and interleukin-13 via the signal transducer and activator of transcription 6. Int. J. Biochem. Cell Biol. 37: 2559-2573. 
  43. Furuta, G. T., and D. A. Katzka. 2015. Eosinophilic Esophagitis. N. Engl. J. Med. 373: 1640-1648. 
  44. Hoeck, J., and M. Woisetschlager. 2001. Activation of eotaxin-3/CCLl26 gene expression in human dermal fibroblasts is mediated by STAT6. J. Immunol. 167: 3216-3222. 
  45. Kagami, S., H. Saeki, M. Komine, T. Kakinuma, Y. Tsunemi, K. Nakamura, K. Sasaki, A. Asahina, and K. Tamaki. 2005. Interleukin-4 and interleukin-13 enhance CCL26 production in a human keratinocyte cell line, HaCaT cells. Clin. Exp. Immunol. 141: 459-466. 
  46. Mishra, A., and M. E. Rothenberg. 2003. Intratracheal IL-13 induces eosinophilic esophagitis by an IL-5, eotaxin-1, and STAT6-dependent mechanism. Gastroenterology 125: 1419-1427. 
  47. Zhang, X., E. Cheng, X. Huo, C. Yu, Q. Zhang, T. H. Pham, D. H. Wang, S. J. Spechler, and R. F. Souza. 2012. Omeprazole blocks STAT6 binding to the eotaxin-3 promoter in eosinophilic esophagitis cells. PLoS One 7: e50037. 
  48. Niranjan, R., M. Rayapudi, A. Mishra, P. Dutt, S. Dynda, and A. Mishra. 2013. Pathogenesis of allergen-induced eosinophilic esophagitis is independent of interleukin (IL)-13. Immunol. Cell Biol. 91: 408-415. 
  49. Krishnamurthy, P., J. D. Sherrill, K. Parashette, S. Goenka, M. E. Rothenberg, S. Gupta, and M. H. Kaplan. 2014. Correlation of increased PARP14 and CCL26 expression in biopsies from children with eosinophilic esophagitis. J. Allergy Clin. Immunol. 133: 577-580. 
  50. Blanchard, C., E. M. Stucke, K. Burwinkel, J. M. Caldwell, M. H. Collins, A. Ahrens, B. K. Buckmeier, S. C. Jameson, A. Greenberg, A. Kaul, J. P. Franciosi, J. P. Kushner, L. J. Martin, P. E. Putnam, J. P. Abonia, S. I. Wells, and M. E. Rothenberg. 2010. Coordinate interaction between IL-13 and epithelial differentiation cluster genes in eosinophilic esophagitis. J. Immunol. 184: 4033-4041. 
  51. Sherrill, J. D., K. Kc, D. Wu, Z. Djukic, J. M. Caldwell, E. M. Stucke, K. A. Kemme, M. S. Costello, M. K. Mingler, C. Blanchard, M. H. Collins, J. P. Abonia, P. E. Putnam, E. S. Dellon, R. C. Orlando, S. P. Hogan, and M. E. Rothenberg. 2014. Desmoglein-1 regulates esophageal epithelial barrier function and immune responses in eosinophilic esophagitis. Mucosal Immunol. 7: 718-729. 
  52. Hottiger, M. O., P. O. Hassa, B. Luscher, H. Schuler, and F. Koch-Nolte. 2010. Toward a unified nomenclature for mammalian ADP-ribosyltransferases. Trends Biochem. Sci. 35: 208-219. 
  53. Schreiber, V., F. Dantzer, J.-C. Ame, and G. de Murcia. 2006. Poly(ADP-ribose): novel functions for an old molecule. Nat. Rev. Mol. Cell Biol. 7: 517-528. 
  54. Yelamos, J., Y. Monreal, L. Saenz, E. Aguado, V. Schreiber, R. Mota, T. Fuente, A. Minguela, P. Parrilla, G. de Murcia, E. Almarza, P. Aparicio, and J. Menissier-de Murcia. 2006. PARP-2 deficiency affects the survival of CD4+CD8+ double-positive thymocytes. EMBO J. 25: 4350-4360. 
  55. Rosado, M. M., E. Bennici, F. Novelli, and C. Pioli. 2013. Beyond DNA repair, the immunological role of PARP-1 and its siblings. Immunology 139: 428-437. 
  56. Saenz, L., J. J. Lozano, R. Valdor, A. Baroja-Mazo, P. Ramirez, P. Parrilla, P. Aparicio, L. Sumoy, and J. Yelamos. 2008. Transcriptional regulation by poly(ADP-ribose) polymerase-1 during T cell activation. BMC Genomics 9: 171. 
  57. Kim, M. Y., T. Zhang, and W. L. Kraus. 2005. Poly (ADP-ribosyl) ation by PARP-1 : " PAR-laying " NAD+ into a nuclear signal. Genes Dev 19: 1951-1967. 
  58. Oumouna, M., R. Datta, K. Oumouna-Benachour, Y. Suzuki, C. Hans, K. Matthews, K. Fallon, and H. Boulares. 2006. Poly(ADP-ribose) polymerase-1 inhibition prevents eosinophil recruitment by modulating Th2 cytokines in a murine model of allergic airway inflammation: a potential specific effect on IL-5. J. Immunol. 177: 6489-6496. 
  59. Boulares, A. H., A. J. Zoltoski, Z. A. Sherif, P. Jolly, D. Massaro, and M. E. Smulson. 2003. Gene knockout or pharmacological inhibition of poly(ADP-ribose) polymerase-1 prevents lung inflammation in a murine model of asthma. Am. J. Respir. Cell Mol. Biol. 28: 322-329. 
  60. Suzuki, Y., E. Masini, C. Mazzocca, S. Cuzzocrea, A. Ciampa, H. Suzuki, and D. Bani. 2004. Inhibition of Poly (ADP-Ribose) polymerase prevents allergen- induced asthma-like reaction in sensitized guinea pigs. Pharmacology 311: 1241-1248. 
  61. Virag, L., P. Bai, I. Bak, P. Pacher, J. G. Mabley, L. Liaudet, E. Bakondi, P. Gergely, M. Kollai, and C. Szabo. 2004. Effects of poly(ADP-ribose) polymerase inhibition on inflammatory cell migration in a murine model of asthma. Med. Sci. Monit. 10: BR77-R83. 
  62. Naura, A. S., C. P. Hans, M. Zerfaoui, D. You, S. a Cormier, M. Oumouna, and A. H. Boulares. 2008. Post-allergen challenge inhibition of poly(ADP-ribose) polymerase harbors therapeutic potential for treatment of allergic airway inflammation. Clin. Exp. Allergy 38: 839-846. 
  63. Olabisi, O. A., N. Soto-Nieves, E. Nieves, T. T. C. Yang, X. Yang, R. Y. L. Yu, H. Y. Suk, F. Macian, and C.-W. Chow. 2008. Regulation of transcription factor NFAT by ADP-ribosylation. Mol. Cell. Biol. 28: 2860-2871. 
  64. Datta, R., A. S. Naura, M. Zerfaoui, Y. Errami, M. Oumouna, H. Kim, J. Ju, V. P. Ronchi, A. L. Haas, and A. H. Boulares. 2011. PARP-1 deficiency blocks IL-5 expression through calpain-dependent degradation of STAT-6 in a murine asthma model. Allergy Eur. J. Allergy Clin. Immunol. 66: 853-861. 
  65. Pehrson, J.R., V. A. Fried. 1992. MacroH2A, a core histone containing a large nonhistone region. Science 5075:1398-400 
  66. Ladurner, A. G. 2003. Inactivating chromosomes: A macro domain that minimizes transcription. Mol. Cell 12: 1-4. 
  67. Vyas, S., I. Matic, L. Uchima, J. Rood, R. Zaja, R. T. Hay, I. Ahel, and P. Chang. 2014. Family-wide analysis of poly(ADP-ribose) polymerase activity. Nat. Commun. 5: 4426. 
  68. Goenka, S., and M. Boothby. 2006. Selective potentiation of Stat-dependent gene expression by collaborator of Stat6 (CoaSt6), a transcriptional cofactor. Proc. Natl. Acad. Sci. U. S. A. 103: 4210-4215. 
  69. Goenka, S., H. C. Sung, and M. Boothby. 2007. Collaborator of Stat6 (CoaSt6)-associated poly(ADP-ribose) polymerase activity modulates Stat6-dependent gene transcription. J. Biol. Chem. 282: 18732-18739. 
  70. Mehrotra, P., J. P. Riley, R. Patel, F. Li, L. Voss, and S. Goenka. 2011. PARP-14 functions as a transcriptional switch for Stat6-dependent gene activation. J. Biol. Chem. 286: 1767-1776. 
  71. Mehrotra, P., A. Hollenbeck, J. P. Riley, F. Li, R. J. Patel, N. Akhtar, and S. Goenka. 2013. Poly (ADP-ribose) polymerase 14 and its enzyme activity regulates TH2 differentiation and allergic airway disease. J. Allergy Clin. Immunol. 131: 521-531. 
  72. Bettelli, E., T. Korn, and V. K. Kuchroo. 2007. Th17 : the third member of the effector T cell trilogy. Curr. Opin. Immunol. 19: 652-657. 
  73. Alcorn, J. F., C. R. Crowe, and J. K. Kolls. 2010. TH17 cells in asthma and COPD. Annu. Rev. Physiol. 72: 495-516. 
  74. Kemeny, D. M. 2012. The role of the T follicular helper cells in allergic disease. Cell. Mol. Immunol. 9: 386-389. 
  75. Crotty, S. 2014. Review T follicular helper cell differentiation , function , and roles in disease. Immunity 41: 529-542. 
  76. Riley, J. P., A. Kulkarni, P. Mehrotra, B. Koh, N. B. Perumal, M. H. Kaplan, and S. Goenka. 2013. PARP-14 binds specific DNA sequences to promote Th2 cell gene expression. PLoS One 8: e83127. 
  77. Mehrotra, P., P. Krishnamurthy, J. Sun, S. Goenka, and M. H. Kaplan. 2015. Poly-ADP-ribosyl polymerase-14 promotes T helper 17 and follicular T helper development. Immunology 146: 537-546. 
  78. Cho, S. H., S. Goenka, T. Henttinen, P. Gudapati, A. Reinikainen, C. M. Eischen, R. Lahesmaa, and M. Boothby. 2009. PARP-14, a member of the B aggressive lymphoma family, transduces survival signals in primary B cells. Blood 113: 2416-2425. 
  79. Blanchard, C., N. Wang, K. F. Stringer, A. Mishra, P. C. Fulkerson, J. P. Abonia, S. C. Jameson, C. Kirby, M. R. Konikoff, M. H. Collins, M. B. Cohen, R. Akers, S. P. Hogan, A. H. Assa'ad, P. E. Putnam, B. J. Aronow, and M. E. Rothenberg. 2006. Eotaxin-3 and a uniquely conserved gene expression profile in eosinophilic esophagitis. J. Clin. Invest. 116: 536-547. 
  80. Gupta, S. K., J. F. Fitzgerald, T. Kondratyuk, and H. HogenEsch. 2006. Cytokine expression in normal and inflamed esophageal mucosa: a study into the pathogenesis of allergic eosinophilic esophagitis. J. Pediatr. Gastroenterol. Nutr. 42: 22-26. 
  81. Nasta, F., F. Laudisi, M. Sambucci, M. M. Rosado and C. Pioli. 2010. Increased Foxp3+ regulatory T cells in poly (ADP-ribose) polymerase -1 deficiency. J. Immunol. 184: 3470-3477. 
  82. Bai, P., C. Hegedus, E. Szabo, L. Gyure, E. Bakondi, A. Brunyanszki, S. Gergely, C. Szabo, and L. Virag. 2009. Poly (ADP-Ribose ) polymerase mediates inflammation in a mouse model of contact hypersensitivity. J. Invest. Dermatol. 129: 234-238. 
  83. Brunyanszki, A., C. Hegedus, M. Szanto, K. Erdelyi, K. Kovacs, V. Schreiber, S. Gergely, B. Kiss, E. Szabo, L. Virag, and P. Bai. 2010. Genetic ablation of PARP-1 protects against oxazolone-induced contact hypersensitivity by modulating oxidative stress. J. Invest. Dermatol. 130: 2629-2637.