Non-coding RNAs in epithelial immunity to Cryptosporidium infection

Parasitology

Volumn 141, Issue 10, 2014, Pages 1233-1243

  Zhou, Rui ^a   Feng, Yaoyu ^b   Chen, Xian Ming ^c  

^a WUHAN UNIVERSITY   (China)

^b EAST CHINA UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^c CREIGHTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cryptosporidium; epithelial cells; immunity; lincRNAs; miRNAs; ncRNAs

Indexed keywords

CHEMOKINE; CYTOKINE; MICRORNA; UNTRANSLATED RNA; ADAPTOR PROTEIN; CASPASE; CCAAT ENHANCER BINDING PROTEIN BETA; FRACTALKINE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 8; LONG UNTRANSLATED RNA; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR; PATTERN RECOGNITION RECEPTOR; PIWI INTERACTING RNA; POLYPEPTIDE ANTIBIOTIC AGENT; PROSTAGLANDIN E2; RIBOSOME RNA; RNA BINDING PROTEIN; RNA INDUCED SILENCING COMPLEX; RNA POLYMERASE II; SMALL INTERFERING RNA; SMALL NUCLEAR RNA; TOLL LIKE RECEPTOR 4; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR REL; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION FACTOR RELB; TRANSFER RNA;

CELL INFILTRATION; CRYPTOSPORIDIOSIS; CRYPTOSPORIDIUM PARVUM; CYTOKINE PRODUCTION; EXOSOME; GENE EXPRESSION; HOST; HUMAN; IMMUNOREGULATION; INNATE IMMUNITY; INTESTINE EPITHELIUM CELL; INTESTINE MUCOSA; PRIORITY JOURNAL; REVIEW; 3' UNTRANSLATED REGION; ADAPTIVE IMMUNITY; ANTIGEN RECOGNITION; ANTIPROTOZOAL ACTIVITY; AU RICH ELEMENT; CRYPTOSPORIDIUM; EPITHELIUM CELL; FEEDBACK SYSTEM; HOMEOSTASIS; NONHUMAN; PROTEIN SYNTHESIS; RNA PROCESSING; SIGNAL TRANSDUCTION; TRANSACTIVATION; ANIMAL; DIARRHEA; GENETICS; IMMUNOLOGY; METABOLISM; PARASITOLOGY;

CRYPTOSPORIDIUM; MAMMALIA; PROTOZOA;

ADAPTIVE IMMUNITY; ANIMALS; CRYPTOSPORIDIOSIS; CRYPTOSPORIDIUM; CYTOKINES; DIARRHEA; EPITHELIAL CELLS; HUMANS; IMMUNITY, INNATE; MICRORNAS; RNA, UNTRANSLATED;

EID: 84938592524     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S0031182014000614     Document Type: Review

References (76)

1. Abrahamsen, M. S., Templeton, T. J., Enomoto, S., Abrahante, J. E., Zhu, G., Lancto, C. A., Deng, M., Liu, C., Widmer, G., Tzipori, S., Buck, G. A., Xu, P., Bankier, A. T., Dear, P. H., Konfortov, B. A., Spriggs, H. F., Iyer, L., Anantharaman, V., Aravind, L. and Kapur, V. (2004). Complete genome sequence of the apicomplexan. Cryptosporidium parvum. Science 304, 441-445. doi: 10.1126/science.1094786.
2. Asirvatham, A. J., Gregorie, C. J., Hu, Z., Magner, W.J. and Tomasi, T.B. (2008). MicroRNA targets in immune genes and the Dicer/Argonaute and ARE machinery components. Molecular Immunology 45, 1995-2006. doi: 10.1016/j.molimm.2007.10.035.
3. Bartel, D. P. (2004). MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281-297. doi: 10.1016/S0092-8674(04)00045-5.
4. Bhatnagar, S. and Schorey, J. S. (2007). Exosomes released from infected macrophages contain Mycobacterium avium glycopeptidolipids and are proinflammatory. Journal of Biological Chemistry 282, 25779-25789. doi: 10.1074/jbc.M702277200.
5. Blikslager, A. T., Moeser, A. J., Gookin, J. L., Jones, S.L. and Odle, J. (2007). Restoration of barrier function in injured intestinal mucosa. Physiological Reviews 87, 545-564. doi: 10.1152/physrev.00012.2006.
6. Borad, A. and Ward, H. (2010). Human immune responses in cryptospor-idiosis. Future Microbiology 5, 507-519. doi: 10.2217/fmb.09.128.
7. Carpenter, S., Aiello, D., Atianand, M. K., Ricci, E. P., Gandhi, P., Hall, L. L., Byron, M., Monks, B., Henry-Bezy, M., Lawrence, J. B., O'Neill, L. A., Moore, M. J., Caffrey, D. R. and Fitzgerald, K. A. (2013). A long noncoding RNA mediates both activation and repression of immune response genes. Science 341, 789-792. doi: 10.1126/science. 1240925.
8. Chakravorty, S.J., Cockwell, P., Girdlestone, J., Brooks, C. J. and Savage, C. O. (2002). Fractalkine expression on human renal tubular epithelial cells: potential role in mononuclear cell adhesion. Clinical and Experimental Immunology 129, 150-159. doi: 10.1046/j.1365-2249.2002. 01906-x.
9. Chaumeil, J., Le Baccon, P., Wutz, A. and Heard, E. (2006). A novel role for Xist RNA in the formation of a repressive nuclear compartment into which genes are recruited when silenced. Genes and Development 20, 2223-2237. doi: 10.1101/gad.380906.
10. Chen, X. M., Keithly, J. S., Paya, C. V. and LaRusso, N.F. (2002). Cryptosporidiosis. New England Journal of Medicine 346, 1723-1731. doi: 10.1056/NEJMra013170.
11. Chen, X. M., O'Hara, S. P., Nelson, J. B., Splinter, P. L., Small, A. J., Tietz, P. S., Limper, A. H. and LaRusso, N. F. (2005). Multiple TLRs are expressed in human cholangiocytes and mediate host epithelial defense responses to Cryptosporidium parvum via activation of NF-kappaB. Journal of Immunology 175, 7447-7456.
12. Chen, X. M., Splinter, P.L., O'Hara, S. P. and LaRusso, N.F. (2007). A cellular micro-RNA, let-7i, regulates toll-like receptor 4 expression and contributes to cholangiocyte immune responses against Cryptosporidium parvum infection. Journal of Biological Chemistry 282, 28929-28938. doi: 10.1074/jbc.M702633200.
13. Choi, S.M., McAleer, J. P., Zheng, M., Pociask, D. A., Kaplan, M. H., Qin, S., Reinhart, T. A. and Kolls, J. K. (2013). Innate Stat3-mediated induction of the antimicrobial protein Reg3gamma is required for host defense against MRSA pneumonia. Journal of Experimental Medicine 210, 551-561. doi: 10.1084/jem.20120260.
14. Dommett, R., Zilbauer, M., George, J. T. and Bajaj-Elliott, M. (2005). Innate immune defence in the human gastrointestinal tract. Molecular Immunology 42, 903-912. doi: 10.1016/j.molimm.2004.12.004.
15. Dong, H. and Chen, X. (2006). Immunoregulatory role of B7-H1 in chronicity of inflammatory responses. Cellular and Molecular Immunology 3, 179-187.
16. Gong, A. Y., Zhou, R., Hu, G., Liu, J., Sosnowska, D., Drescher, K. M., Dong, H. and Chen, X. M. (2010). Cryptosporidium parvum induces B7-H1 expression in cholangiocytes by down-regulating microRNA-513. Journal of Infectious Diseases 201, 160-169. doi: 10.1086/648589.
17. Gong, A. Y., Hu, G., Zhou, R., Liu, J., Feng, Y., Soukup, G. A. and Chen, X. M. (2011). MicroRNA-221 controls expression of intercellular adhesion molecule-1 in epithelial cells in response to Cryptosporidium parvum infection. International Journal for Parasitology 41, 397-403. doi: 10.1016/j.ijpara.2010.11.011.
18. Goodgame, R. W. (1996). Understanding intestinal spore-forming protozoa: cryptosporidia, microsporidia, isospora, and cyclospora. Annals of Internal Medicine 124, 429-441. doi: 10.7326/0003-4819-124-4-199602150-00008.
19. Gookin, J. L., Chiang, S., Allen, J., Armstrong, M. U., Stauffer, S.H., Finnegan, C. and Murtaugh, M. P. (2006). NF-kappaB-mediated expression of iNOS promotes epithelial defense against infection by Cryptosporidium parvum in neonatal piglets. American Journal of Physiology-Gastrointestinal and Liver Physiology 290, G164-G174. doi: 10.1152/ajpgi.00460.2004.
20. Guttman, M., Amit, I., Garber, M., French, C., Lin, M. F., Feldser, D., Huarte, M., Zuk, O., Carey, B. W., Cassady, J.P., Cabili, M. N., Jaenisch, R., Mikkelsen, T.S., Jacks, T., Hacohen, N., Bernstein, B. E., Kellis, M., Regev, A., Rinn, J. L. and Lander, E.S. (2009). Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 458, 223-227. doi: 10.1038/nature07672.
21. Hayden, M. S. and Ghosh, S. (2008). Shared principles in NF-kappaB signaling. Cell 132, 344-362. doi: 10.1016/j.cell.2008.01.020.
22. Hayward, A. R., Chmura, K. and Cosyns, M. (2000). Interferon-gamma is required for innate immunity to Cryptosporidium parvum in mice. Journal of Infectious Diseases 182, 1001-1004. doi: 10.1086/315802.
23. Hu, G., Zhou, R., Liu, J., Gong, A. Y., Eischeid, A. N., Dittman, J. W. and Chen, X. M. (2009). MicroRNA-98 and let-7 confer cholangiocyte expression of cytokine-inducible Src homology 2-containing protein in response to microbial challenge. Journal of Immunology 183, 1617-1624. doi: 10.4049/jimmunol.0804362.
24. Hu, G., Zhou, R., Liu, J., Gong, A. Y. and Chen, X.M. (2010). MicroRNA-98 and let-7 regulate expression of suppressor of cytokine signaling 4 in biliary epithelial cells in response to Cryptosporidium parvum infection. Journal of Infectious Diseases 202, 125-135. doi: 10.1086/653212.
25. Hu, G., Gong, A. Y., Roth, A. L., Huang, B. Q., Ward, H. D., Zhu, G., Larusso, N.F., Hanson, N. D. and Chen, X. M. (2013). Release of luminal exosomes contributes to TLR4-mediated epithelial antimicrobial defense. PLoS Pathogens 9, e1003261. doi: 10.1371/journal.ppat.1003261.
26. Huarte, M., Guttman, M., Feldser, D., Garber, M., Koziol, M. J., Kenzelmann-Broz, D., Khalil, A. M., Zuk, O., Amit, I., Rabani, M., Attardi, L. D., Regev, A., Lander, E. S., Jacks, T. and Rinn, J. L. (2010). A large intergenic noncoding RNA induced by p53 mediates global gene repression in the p53 response. Cell 142, 409-419. doi: 10.1016/j. cell.2010.06.040.
27. Kawai, T. and Akira, S. (2010). The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nature Immunology 11, 373-384. doi: 10.1038/ni.1863.
28. Kincaid, R. P. and Sullivan, C.S. (2012). Virus-encoded microRNAs: an overview and a look to the future. PLoS Pathogens 8, e1003018. doi: 10.1371/journal.ppat.1003018.
29. + T cells are not essential for control of early acute Cryptosporidium parvum infection in neonatal mice. Infection and Immunity 79, 1647-1653. doi: 10.1128/IAI.00922-10.
30. Kotloff, K. L., Nataro, J. P., Blackwelder, W. C., Nasrin, D., Farag, T.H., Panchalingam, S., Wu, Y., Sow, S. O., Sur, D., Breiman, R. F., Faruque, A. S., Zaidi, A. K., Saha, D., Alonso, P. L., Tamboura, B., Sanogo, D., Onwuchekwa, U., Manna, B., Ramamurthy, T., Kanungo, S., Ochieng, J. B., Omore, R., Oundo, J. O., Hossain, A., Das, S. K., Ahmed, S., Qureshi, S., Quadri, F., Adegbola, R. A., Antonio, M., Hossain, M. J., Akinsola, A., Mandomando, I., Nhampossa, T., Acácio, S., Biswas, K., O'Reilly, C. E., Mintz, E. D., Berkeley, L. Y., Muhsen, K., Sommerfelt, H., Robins-Browne, R. M. and Levine, M. M. (2013). Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case-control study. Lancet 382, 209-222. doi: 10.1016/S0140-6736(13)60844-2.
31. Kozomara, A. and Griffiths-Jones, S. (2011). miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Research 39, D152-D157. doi: 10.1093/nar/gkq1027.
32. Lean, I. S., McDonald, S. A., Bajaj-Elliott, M., Pollok, R. C., Farthing, M. J. and McDonald, V. (2003). Interleukin-4 and transforming growth factor beta have opposing regulatory effects on gamma interferon-mediated inhibition of Cryptosporidium parvum reproduction. Infection and Immunity 71, 4580-4585. doi: 10.1128/IAI.71.8.4580-4585.2003.
33. Lee, J. T. (2012). Epigenetic regulation by long noncoding RNAs. Science 338, 1435-1439. doi: 10.1126/science.1231776.
34. Lee, Y., Kim, M., Han, J., Yeom, K. H., Lee, S., Baek, S. H. and Kim, V. N. (2004). MicroRNA genes are transcribed by RNA polymerase II. EMBO Journal 23, 4051-4060. doi: 10.1038/sj.emboj. 7600385.
35. Leitch, G. J.and He, Q.(1994). Arginine-derived nitric oxide reduces fecal oocyst shedding in nude mice infected with Cryptosporidium parvum. Infection and Immunity 62, 5173-5176.
36. Leung, A.K., Young, A.G., Bhutkar, A., Zheng, G. X., Bosson, A. D., Nielsen, C. B. and Sharp, P. A. (2011). Genome-wide identification of Ago2 binding sites from mouse embryonic stem cells with and without mature microRNAs. Nature Structural and Molecular Biology 18, 237-244. doi: 10.1038/nsmb.1991.
37. Linker, K., Pautz, A., Fechir, M., Hubrich, T., Greeve, J. and Kleinert, H. (2005). Involvement of KSRP in the post-transcriptional regulation of human iNOS expression-complex interplay of KSRP with TTP and HuR. Nucleic Acids Research 33, 4813-4827. doi: 10.1093/nar/gki797.
38. Liu, N. and Olson, E. N. (2010). MicroRNA regulatory networks in cardiovascular development. Developmental Cell 18, 510-525. doi: 10.1016/j.devcel.2010.03.010.
39. Mallegol, J., Van Niel, G., Lebreton, C., Lepelletier, Y., Candalh, C., Dugave, C., Heath, J. K., Raposo, G., Cerf-Bensussan, N. and Heyman, M. (2007). T84-intestinal epithelial exosomes bear MHC class II/peptide complexes potentiating antigen presentation by dendritic cells. Gastroenterology 132, 1866-1876. doi: 10.1053/j.gastro.2007. 02.043.
40. Mansell, A., Smith, R., Doyle, S. L., Gray, P., Fenner, J.E., Crack, P. J., Nicholson, S. E., Hilton, D. J., O'Neill, L. A. and Hertzog, P. J. (2006). Suppressor of cytokine signaling 1 negatively regulates toll-like receptor signaling by mediating Mal degradation. Nature Immunology 7, 148-155. doi: 10.1038/ni1299.
41. McDonald, V., Korbel, D. S., Barakat, F. M., Choudhry, N. and Petry, F. (2013). Innate immune responses against Cryptosporidium parvum infection. Parasite Immunology 35, 55-64. doi: 10.1111/pim.12020.
42. Mercer, T. R., Dinger, M. E. and Mattick, J. S. (2009). Long non-coding RNAs: insights into functions. Nature Reviews Genetics 10, 155-159. doi: 10.1038/nrg2521.
43. Muller, W.A. (2009). Mechanisms of transendothelial migration of leukocytes. Circulation Research 105, 223-230. doi: 10.1161/CIRCRESAHA. 109.200717.
44. Nordone, S. K. and Gookin, J. L. (2010). Lymphocytes and not IFN-gamma mediate expression of iNOS by intestinal epithelium in murine cryptosporidiosis. Parasitology Research 106, 1507-1511. doi: 10.1007/s00436-010-1837-7.
45. O'Hara, S. P., Splinter, P. L., Gajdos, G.B., Trussoni, C.E., Fernandez-Zapico, M. E., Chen, X. M. and LaRusso, N. F. (2010). NFkappaB p50-CCAAT/enhancer-binding protein beta (C/EBPbeta)-mediated transcriptional repression of microRNA let-7i following microbial infection. Journal of Biological Chemistry 285, 216-225. doi: 10.1074/jbc. M109.041640.
46. Ørom, U. A. and Lund, A. H. (2010). Experimental identification of microRNA targets. Gene 451, 1-5. doi: 10.1016/j.gene.2009.11.008.
47. Pantenburg, B., Dann, S. M., Wang, H.C., Robinson, P., Castellanos-Gonzalez, A., Lewis, D. E. and White, A. C., Jr. (2008). Intestinal immune response to human Cryptosporidium sp. infection. Infection and Immunity 76, 23-29. doi: 10.1128/IAI.00960-07.
48. Pautz, A., Art, J., Hahn, S., Nowag, S., Voss, C.and Kleinert, H.(2010). Regulation of the expression of inducible nitric oxide synthase. Nitric Oxide 23, 75-93. doi: 10.1016/j.niox.2010.04.007.
49. Petry, F., Jakobi, V. and Tessema, T. S. (2010). Host immune response to Cryptosporidium parvum infection. Experimental Parasitology 126, 304-309. doi: 10.1016/j.exppara.2010.05.022.
50. Pierce, K. K. and Kirkpatrick, B.D. (2009). Update on human infections caused by intestinal protozoa. Current Opinion in Gastroenterology 25, 12-17. doi: 10.1097/MOG.0b013e32831da7dd.
51. Poppelmann, B., Klimmek, K., Strozyk, E., Voss, R., Schwarz, T. and Kulms, D. (2005). NF{kappa}B-dependent down-regulation of tumor necrosis factor receptor-associated proteins contributes to inter-leukin-1-mediated enhancement of ultraviolet B-induced apoptosis. Journal of Biological Chemistry 280, 15635-15643. doi: 10.1074/jbc.M413006200.
52. Putignani, L. and Menichella, D. (2010). Global distribution, public health and clinical impact of the protozoan pathogen cryptosporidium. Interdisciplinary Perspectives on Infectious Diseases 2010, 1-39. doi: 10.1155/2010/753512.
53. Reigstad, C. S., Lunden, G. O., Felin, J. and Backhed, F. (2009). Regulation of serum amyloid A3 (SAA3) in mouse colonic epithelium and adipose tissue by the intestinal microbiota. PLoS One 4, e5842. doi: 10.1371/journal.pone.0005842.
54. Rinn, J. L., Kertesz, M., Wang, J. K., Squazzo, S. L., Xu, X., Brugmann, S. A., Goodnough, L. H., Helms, J. A., Farnham, P. J., Segal, E. and Chang, H. Y. (2007). Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 129, 1311-1323. doi: 10.1016/j.cell.2007.05.022.
55. Robbins, P. D. and Morelli, A.E. (2014). Regulation of immune responses by extracellular vesicles. Nature Review in Immunology 105, 195-208. doi: 10.1038/nri3622.
56. Saini, H. K., Griffiths-Jones, S. and Enright, A. J. (2007). Genomic analysis of human microRNA transcripts. Proceedings of the National Academy of Sciences USA 104, 17719-17724. doi: 10.1073/pnas.0703890104.
57. Schonrock, N., Harvey, R.P. and Mattick, J. S. (2012). Long noncoding RNAs in cardiac development and pathophysiology. Circulation Research 111, 1349-1362. doi: 10.1161/CIRCRESAHA.112.268953.
58. Smalheiser, N. R. (2007). Exosomal transfer of proteins and RNAs at synapses in the nervous system. Biology Direct 2, 35. doi: 10.1186/1745-6150-2-35.
59. Stievano, L., Piovan, E. and Amadori, A. (2004). C and CX3C chemokines: cell sources and physiopathological implications. Critical Reviews in Immunology 24, 205-228. doi: 10.1615/CritRevImmunol. v24.i3.40.
60. Striepen, B. (2013). Parasitic infections: time to tackle cryptosporidiosis. Nature 503, 189-191. doi: 10.1038/503189a.
61. Südhof, T. C. and Rothman, J. E. (2009). Membrane fusion: grappling with SNARE and SM proteins. Science 323, 474-477. doi: 10.1126/science.1161748.
62. Taganov, K. D., Boldin, M. P., Chang, K. J. and Baltimore, D. (2006). NF-kappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proceedings of the National Academy of Sciences USA 103, 12481-12486. doi: 10.1073/pnas.0605298103.
63. Tang, B., Xiao, B., Liu, Z., Li, N., Zhu, E. D., Li, B. S., Xie, Q. H., Zhuang, Y., Zou, Q. M. and Mao, X. H. (2010). Identification of MyD88 as a novel target of miR-155, involved in negative regulation of Helicobacter pylori-induced inflammation. FEBS Letters 584, 1481-1486. doi: 10.1016/j.febslet.2010.02.063.
64. Théry, C. (2011). Exosomes: secreted vesicles and intercellular communications. F1000 Biology Reports 3, 15. doi: 10.3410/B3-15.
65. Tzipori, S. and Griffiths, J. K. (1998). Natural history and biology of Cryptosporidium parvum. Advances in Parasitology 40, 5-36.
66. Ulitsky, I. and Bartel, D. P. (2013). LincRNAs: genomics, evolution, and mechanisms. Cell 154, 26-46. doi: 10.1016/j.cell.2013.06.020.
67. Valadi, H., Ekstrom, K., Bossios, A., Sjostrand, M., Lee, J. J. and Lötvall, J.O. (2007). Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nature Cell Biology 9, 654-659. doi: 10.1038/ncb1596.
68. van Niel, G., Porto-Carreiro, I., Simoes, S. and Raposo, G. (2006). Exosomes: a common pathway for a specialized function. Journal of Biochemistry 140, 13-21. doi: 10.1093/jb/mvj128.
69. Winter, J., Jung, S., Keller, S., Gregory, R. I. and Diederichs, S. (2009). Many roads to maturity: microRNA biogenesis pathways and their regulation. Nature Cell Biology 11, 228-234. doi: 10.1038/ncb0309-228.
70. Winzen, R., Thakur, B. K., Dittrich-Breiholz, O., Shah, M., Redich, N., Dhamija, S., Kracht, M. and Holtmann, H. (2007). Functional analysis of KSRP interaction with the AU-rich element of interleukin-8 and identification of inflammatory mRNA targets. Molecular and Cellular Biology 27, 8388-8400. doi: 10.1128/MCB.01493-07.
71. Yoshimura, A., Naka, T. and Kubo, M. (2007). SOCS proteins, cytokine signalling and immune regulation. Nature Reviews Immunology 7, 454-465. doi: 10.1038/nri2093.
72. Yu, X., Harris, S. L. and Levine, A. J. (2006). The regulation of exosome secretion: a novel function of the p53 protein. Cancer Research 66, 4795-4801. doi: 10.1158/0008-5472.CAN-05-4579.
73. Zhou, R., Hu, G., Liu, J., Gong, A.Y., Drescher, K. M. and Chen, X. M. (2009). NF-kappaB p65-dependent transactivation of miRNA genes following Cryptosporidium parvum infection stimulates epithelial cell immune responses. PLoS Pathogens 5, e1000681. doi: 10.1371/journal. ppat.1000681.
74. Zhou, R., O'Hara, S. P. and Chen, X. M. (2011). MicroRNA regulation of innate immune responses in epithelial cells. Cellular and Molecular Immunology 8, 371-379. doi: 10.1038/cmi.2011.19.
75. Zhou, R., Gong, A. Y., Eischeid, A. N. and Chen, X.M.(2012). miR-27b targets KSRP to coordinate TLR4-mediated epithelial defense against Cryptosporidium parvum infection. PLoS Pathogens 8, e1002702. doi: 10.1371/journal.ppat.1002702.
76. Zhou, R., Gong, A. Y., Chen, D., Miller, R. E., Eischeid, A. N. and Chen, X. M. (2013). Histone deacetylases and NF-kB signaling coordinate expression of CX3CL1 in epithelial cells in response to microbial challenge by suppressing miR-424 and miR-503. PLoS One 8, e65153. doi: 10.1371/journal.pone.0065153.