Exploration of microRNAs in porcine milk exosomes

BMC Genomics

Volumn 15, Issue 1, 2014, Pages

  Chen, Ting ^a   Xi, Qian Yun ^a   Ye, Rui Song ^a   Cheng, Xiao ^a   Qi, Qi En ^a   Wang, Song Bo ^a   Shu, Gang ^a   Wang, Li Na ^a   Zhu, Xiao Tong ^a   Jiang, Qing Yan ^a   Zhang, Yong Liang ^a  

^a SOUTH CHINA AGRICULTURAL UNIVERSITY   (China)

Author keywords

miRNA; Porcine milk exosomes; Solexa sequencing

Indexed keywords

IMMUNOGLOBULIN A; MICRORNA; MICRORNA 138 3P; MICRORNA 138 5P; MICRORNA 150 5P; MICRORNA 181A; MICRORNA 181C; MICRORNA 181D; MICRORNA 182; MICRORNA 191; MICRORNA 193A 3P; MICRORNA 20B 3P; MICRORNA 219 3P; MICRORNA 2411 3P; MICRORNA 290 5P; MICRORNA 30A 3P; MICRORNA 30C; MICRORNA 30D; MICRORNA 31 3P; MICRORNA 31 5P; MICRORNA 32; MICRORNA 378; MICRORNA 378C; MICRORNA 5003 3P; MICRORNA 551A; MICRORNA 874 3P; MICRORNA 96 5P; RNA 5S; SOMATOMEDIN C RECEPTOR; UNCLASSIFIED DRUG; UNINDEXED DRUG; 3' UNTRANSLATED REGION;

3' UNTRANSLATED REGION; ARTICLE; BIOINFORMATICS; BREAST MILK; CONTROLLED STUDY; CORRELATIONAL STUDY; EXOSOME; FEMALE; GENE EXPRESSION; GENE FUNCTION; GENE LOCATION; GENE ONTOLOGY; IMMUNOGLOBULIN PRODUCTION; IMMUNOREGULATION; LUCIFERASE ASSAY; NEWBORN; NONHUMAN; PIGLET; POLYMERASE CHAIN REACTION; RNA ANALYSIS; RNA SEQUENCE; SOLEXA SEQUENCING; SWINE; TRANSMISSION ELECTRON MICROSCOPY; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOLOGY; CHEMISTRY; CLUSTER ANALYSIS; GENETICS; HIGH THROUGHPUT SEQUENCING; METABOLISM; MILK; NUCLEOTIDE SEQUENCE; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS;

BOVINAE; SUS;

3' UNTRANSLATED REGIONS; ANIMALS; BASE SEQUENCE; CLUSTER ANALYSIS; COMPUTATIONAL BIOLOGY; EXOSOMES; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; MICRORNAS; MILK; RECEPTOR, IGF TYPE 1; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, RNA; SWINE;

EID: 84893155701     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-15-100     Document Type: Article

References (86)

1. Strobel S. Immunity induced after a feed of antigen during early life: oral tolerance v. sensitisation. Proc Nutr Soc 2001, 60(4):437-442. 10.1079/PNS2001119, 12069395.
2. Armogida SA, Yannaras NM, Melton AL, Srivastava MD. Identification and quantification of innate immune system mediators in human breast milk. Allergy Asthma Proc 2004, 25(5):297-304.
3. Kramer MS, Chalmers B, Hodnett ED, Sevkovskaya Z, Dzikovich I, Shapiro S, Collet JP, Vanilovich I, Mezen I, Ducruet T. Promotion of breastfeeding intervention trial (PROBIT). JAMA 2001, 285(4):413-420. 10.1001/jama.285.4.413, 11242425.
4. Høst A, Koletzko B, Dreborg S, Muraro A, Wahn U, Aggett P, Bresson J, Hernell O, Lafeber H, Michaelsen K. Dietary products used in infants for treatment and prevention of food allergy. Arch Dis Child 1999, 81(1):80-84. 10.1136/adc.81.1.80, 1717972, 10373144.
5. Van Niel G, Porto-Carreiro I, Simoes S, Raposo G. Exosomes: a common pathway for a specialized function. J Biochem 2006, 140(1):13-21. 10.1093/jb/mvj128, 16877764.
6. Pan BT, Johnstone RM. Fate of the transferrin receptor during maturation of sheep reticulocytes in vitro: selective externalization of the receptor. Cell 1983, 33(3):967-978. 10.1016/0092-8674(83)90040-5, 6307529.
7. Théry C, Regnault A, Garin J, Wolfers J, Zitvogel L, Ricciardi-Castagnoli P, Raposo G, Amigorena S. Molecular characterization of dendritic cell-derived exosomes. J Cell Biol 1999, 147(3):599-610. 10.1083/jcb.147.3.599, 2151184, 10545503.
8. Raposo G, Nijman HW, Stoorvogel W, Liejendekker R, Harding CV, Melief C, Geuze HJ. B lymphocytes secrete antigen-presenting vesicles. J Exp Med 1996, 183(3):1161-1172. 10.1084/jem.183.3.1161, 2192324, 8642258.
9. Blanchard N, Lankar D, Faure F, Regnault A, Dumont C, Raposo G, Hivroz C. TCR activation of human T cells induces the production of exosomes bearing the TCR/CD3/ζ complex. J Immunol 2002, 168(7):3235-3241.
10. Raposo G, Tenza D, Mecheri S, Peronet R, Bonnerot C, Desaymard C. Accumulation of major histocompatibility complex class II molecules in mast cell secretory granules and their release upon degranulation. Mol Biol Cell 1997, 8(12):2631-2645. 10.1091/mbc.8.12.2631, 25733, 9398681.
11. Van Niel G, Raposo G, Candalh C, Boussac M, Hershberg R, Cerf-Bensussan N, Heyman M. Intestinal epithelial cells secrete exosome-like vesicles. Gastroenterology 2001, 121(2):337-349. 10.1053/gast.2001.26263, 11487543.
12. Mears R, Craven RA, Hanrahan S, Totty N, Upton C, Young SL, Patel P, Selby PJ, Banks RE. Proteomic analysis of melanoma-derived exosomes by two-dimensional polyacrylamide gel electrophoresis and mass spectrometry. Proteomics 2004, 4(12):4019-4031. 10.1002/pmic.200400876, 15478216.
13. Gonzalez-Begne M, Lu B, Han X, Hagen FK, Hand AR, Melvin JE, Yates JR. Proteomic analysis of human parotid gland exosomes by multidimensional protein identification technology (MudPIT). J Proteome Res 2009, 8(3):1304-1314. 10.1021/pr800658c, 2693447, 19199708.
14. Ogawa Y, Kanai-Azuma M, Akimoto Y, Kawakami H, Yanoshita R. Exosome-like vesicles with dipeptidyl peptidase IV in human saliva. Biol Pharm Bull 2008, 31(6):1059-1062. 10.1248/bpb.31.1059, 18520029.
15. García JM, García V, Peña C, Domínguez G, Silva J, Diaz R, Espinosa P, Citores MJ, Collado M, Bonilla F. Extracellular plasma RNA from colon cancer patients is confined in a vesicle-like structure and is mRNA-enriched. RNA 2008, 14(7):1424-1432. 10.1261/rna.755908, 2441977, 18456845.
16. Pisitkun T, Shen RF, Knepper MA. Identification and proteomic profiling of exosomes in human urine. Proc Natl Acad Sci USA 2004, 101(36):13368. 10.1073/pnas.0403453101, 516573, 15326289.
17. Keller S, Rupp C, Stoeck A, Runz S, Fogel M, Lugert S, Hager H, Abdel-Bakky M, Gutwein P, Altevogt P. CD24 is a marker of exosomes secreted into urine and amniotic fluid. Kidney Int 2007, 72(9):1095-1102. 10.1038/sj.ki.5002486, 17700640.
18. Runz S, Keller S, Rupp C, Stoeck A, Issa Y, Koensgen D, Mustea A, Sehouli J, Kristiansen G, Altevogt P. Malignant ascites-derived exosomes of ovarian carcinoma patients contain CD24 and EpCAM. Gynecol Oncol 2007, 107(3):563-571. 10.1016/j.ygyno.2007.08.064, 17900673.
19. Prado N, Marazuela EG, Segura E, Fernández-García H, Villalba M, Théry C, Rodríguez R, Batanero E. Exosomes from bronchoalveolar fluid of tolerized mice prevent allergic reaction. J Immunol 2008, 181(2):1519-1525.
20. Simpson RJ, Jensen SS, Lim JWE. Proteomic profiling of exosomes: current perspectives. Proteomics 2008, 8(19):4083-4099. 10.1002/pmic.200800109, 18780348.
21. Deregibus MC, Cantaluppi V, Calogero R, Iacono ML, Tetta C, Biancone L, Bruno S, Bussolati B, Camussi G. Endothelial progenitor cell-derived microvesicles activate an angiogenic program in endothelial cells by a horizontal transfer of mRNA. Blood 2007, 110(7):2440-2448. 10.1182/blood-2007-03-078709, 17536014.
22. Lakkaraju A, Rodriguez-Boulan E. Itinerant exosomes: emerging roles in cell and tissue polarity. Trends Cell Biol 2008, 18(5):199-209. 10.1016/j.tcb.2008.03.002, 3754907, 18396047.
23. Schorey JS, Bhatnagar S. Exosome function: from tumor immunology to pathogen biology. Traffic 2008, 9(6):871-881. 10.1111/j.1600-0854.2008.00734.x, 3636814, 18331451.
24. Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ, Lötvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 2007, 9(6):654-659. 10.1038/ncb1596, 17486113.
25. Nakatani H, Aoki N, Nakagawa Y, Jin-No S, Aoyama K, Oshima K, Ohira S, Sato C, Nadano D, Matsuda T. Weaning-induced expression of a milk-fat globule protein, MFG-E8, in mouse mammary glands, as demonstrated by the analyses of its mRNA, protein and phosphatidylserine-binding activity. Biochem J 2006, 395(Pt 1):21. 1409693, 16401186.
26. Admyre C, Johansson SM, Qazi KR, Filén JJ, Lahesmaa R, Norman M, Neve EPA, Scheynius A, Gabrielsson S. Exosomes with immune modulatory features are present in human breast milk. J Immunol 2007, 179(3):1969-1978.
27. Hata T, Murakami K, Nakatani H, Yamamoto Y, Matsuda T, Aoki N. Isolation of bovine milk-derived microvesicles carrying mRNAs and microRNAs. Biochem Biophys Res Commun 2010, 396(2):528-533. 10.1016/j.bbrc.2010.04.135, 20434431.
28. Zhou Q, Li M, Wang X, Li Q, Wang T, Zhu Q, Zhou X, Gao X, Li X. Immune-related microRNAs are abundant in breast milk exosomes. Int J Biol Sci 2012, 8(1):118. 3248653, 22211110.
29. Gu Y, Li M, Wang T, Liang Y, Zhong Z, Wang X, Zhou Q, Chen L, Lang Q, He Z, et al. Lactation-related microRNA expression profiles of porcine breast milk exosomes. PLoS One 2012, 7(8):e43691. 10.1371/journal.pone.0043691, 3427246, 22937080.
30. Cullen BR. RNA interference: antiviral defense and genetic tool. Nat Immunol 2002, 3(7):597-599. 10.1038/ni0702-597, 12087412.
31. Hutvágner G, Zamore PD. A microRNA in a multiple-turnover RNAi enzyme complex. Science 2002, 297(5589):2056-2060. 10.1126/science.1073827, 12154197.
32. Carrington JC, Ambros V. Role of microRNAs in plant and animal development. Science 2003, 301(5631):336-338. 10.1126/science.1085242, 12869753.
33. Cerutti H. RNA interference: traveling in the cell and gaining functions?. Trends Genet 2003, 19(1):39-46. 10.1016/S0168-9525(02)00010-0, 12493247.
34. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136(2):215-233. 10.1016/j.cell.2009.01.002, 3794896, 19167326.
35. Friedman RC, Farh KKH, Burge CB, Bartel DP. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 2009, 19(1):92-105. 2612969, 18955434.
36. Rodriguez A, Vigorito E, Clare S, Warren MV, Couttet P, Soond DR, van Dongen S, Grocock RJ, Das PP, Miska EA. Requirement of bic/microRNA-155 for normal immune function. Science 2007, 316(5824):608-611. 10.1126/science.1139253, 2610435, 17463290.
37. Hyun S, Lee JH, Jin H, Nam J, Namkoong B, Lee G, Chung J, Kim VN. Conserved MicroRNA miR-8/miR-200 and its target USH/FOG2 control growth by regulating PI3K. Cell 2009, 139(6):1096-1108. 10.1016/j.cell.2009.11.020, 20005803.
38. Lal A, Navarro F, Maher CA, Maliszewski LE, Yan N, O'Day E, Chowdhury D, Dykxhoorn DM, Tsai P, Hofmann O. miR-24 Inhibits cell proliferation by targeting E2F2, MYC, and other cell-cycle genes via binding to " seedless" 3' UTR microRNA recognition elements. Mol Cell 2009, 35(5):610-625. 10.1016/j.molcel.2009.08.020, 2757794, 19748357.
39. Chen CZ, Li L, Lodish HF, Bartel DP. MicroRNAs modulate hematopoietic lineage differentiation. Science 2004, 303(5654):83-86. 10.1126/science.1091903, 14657504.
40. Lässer C, Alikhani VS, Ekström K, Eldh M, Paredes PT, Bossios A, Sjöstrand M, Gabrielsson S, Lötvall J, Valadi H. Human saliva, plasma and breast milk exosomes contain RNA: uptake by macrophages. J Transl Med 2011, 9(1):9. 10.1186/1479-5876-9-9, 3033821, 21235781.
41. Ji Z, Wang G, Xie Z, Wang J, Zhang C, Dong F, Chen C. Identification of novel and differentially expressed microRNAs of dairy goat mammary gland tissues using Solexa sequencing and bioinformatics. PLoS ONE 2012, 7(11):e49463. 10.1371/journal.pone.0049463, 3498112, 23166677.
42. Li R, Li Y, Kristiansen K, Wang J. SOAP: short oligonucleotide alignment program. Bioinformatics 2008, 24(5):713-714. 10.1093/bioinformatics/btn025, 18227114.
43. Li Y, Zhang Z, Liu F, Vongsangnak W, Jing Q, Shen B. Performance comparison and evaluation of software tools for microRNA deep-sequencing data analysis. Nucleic Acids Res 2012, 40(10):4298-4305. 10.1093/nar/gks043, 3378883, 22287634.
44. Jiang P, Wu H, Wang W, Ma W, Sun X, Lu Z. MiPred: classification of real and pseudo microRNA precursors using random forest prediction model with combined features. Nucleic Acids Res 2007, 35(suppl 2):W339-W344. 1933124, 17553836.
45. Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 2003, 31(13):3406-3415. 10.1093/nar/gkg595, 169194, 12824337.
46. Fu H, Tie Y, Xu C, Zhang Z, Zhu J, Shi Y, Jiang H, Sun Z, Zheng X. Identification of human fetal liver miRNAs by a novel method. FEBS Lett 2005, 579(17):3849-3854. 10.1016/j.febslet.2005.05.064, 15978578.
47. Kosaka N, Izumi H, Sekine K, Ochiya T. microRNA as a new immune-regulatory agent in breast milk. Silence 2010, 1(1):7. 10.1186/1758-907X-1-7, 2847997, 20226005.
48. Ebhardt HA, Fedynak A, Fahlman RP. Naturally occurring variations in sequence length creates microRNA isoforms that differ in argonaute effector complex specificity. Silence 2010, 1(1):12. 10.1186/1758-907X-1-12, 2901367, 20534119.
49. Guo L, Lu Z. Global expression analysis of miRNA gene cluster and family based on isomiRs from deep sequencing data. Comput Biol Chem 2010, 34(3):165-171. 10.1016/j.compbiolchem.2010.06.001, 20619743.
50. Naya L, Khan GA, Sorin C, Hartmann C, Crespi M, Lelandais-Brière C. Cleavage of a non-conserved target by a specific miR156 isoform in root apexes of Medicago truncatula. Plant Signal Behav 2010, 5(3):328-331. 10.4161/psb.5.3.11190, 2881292, 20200496.
51. Li M, Xia Y, Gu Y, Zhang K, Lang Q, Chen L, Guan J, Luo Z, Chen H, Li Y. MicroRNAome of porcine pre-and postnatal development. PLoS One 2010, 5(7):e11541. 10.1371/journal.pone.0011541, 2902522, 20634961.
52. He L, Hannon GJ. MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet 2004, 5(7):522-531. 10.1038/nrg1379, 15211354.
53. Lagos-Quintana M, Rauhut R, Yalcin A, Meyer J, Lendeckel W, Tuschl T. Identification of tissue-specific microRNAs from mouse. Curr Biol 2002, 12(9):735-739. 10.1016/S0960-9822(02)00809-6, 12007417.
54. Tran N, O'Brien CJ, Clark J, Rose B. Potential role of micro-RNAs in head and neck tumorigenesis. Head Neck 2010, 32(8):1099-1111. 10.1002/hed.21356, 20213828.
55. Morales Prieto DM, Markert UR. MicroRNAs in pregnancy. J Reprod Immunol 2011, 88(2):106-111. 10.1016/j.jri.2011.01.004, 21353310.
56. Xie S, Huang T, Shen Y, Li X, Zhang X, Zhu M, Qin H, Zhao S. Identification and characterization of microRNAs from porcine skeletal muscle. Anim Genet 2010, 41(2):179-190. 10.1111/j.1365-2052.2009.01991.x, 19968636.
57. Chen X, Gao C, Li H, Huang L, Sun Q, Dong Y, Tian C, Gao S, Dong H, Guan D. Identification and characterization of microRNAs in raw milk during different periods of lactation, commercial fluid, and powdered milk products. Cell Res 2010, 20(10):1128-1137. 10.1038/cr.2010.80, 20548333.
58. Ye R-S, Xi Q-Y, Qi Q, Cheng X, Chen T, Li H, Kallon S, Shu G, Wang S-B, Jiang Q-Y. Differentially Expressed miRNAs after GnRH Treatment and Their Potential Roles in FSH Regulation in Porcine Anterior Pituitary Cell. PLoS ONE 2013, 8(2):e57156. 10.1371/journal.pone.0057156, 3579806, 23451171.
59. Zheng B, Liang L, Wang C, Huang S, Cao X, Zha R, Liu L, Jia D, Tian Q, Wu J. MicroRNA-148a suppresses tumor cell invasion and metastasis by downregulating ROCK1 in gastric cancer. Clin Cancer Res 2011, 17(24):7574-7583. 10.1158/1078-0432.CCR-11-1714, 21994419.
60. Zhang H, Li Y, Huang Q, Ren X, Hu H, Sheng H, Lai M. MiR-148a promotes apoptosis by targeting Bcl-2 in colorectal cancer. Cell Death Differ 2011, 18(11):1702-1710. 10.1038/cdd.2011.28, 3190106, 21455217.
61. He L, Thomson JM, Hemann MT, Hernando-Monge E, Mu D, Goodson S, Powers S, Cordon-Cardo C, Lowe SW, Hannon GJ. A microRNA polycistron as a potential human oncogene. Nature 2005, 435(7043):828-833. 10.1038/nature03552, 15944707.
62. Li L, Shi JY, Zhu GQ, Shi B. MiR-17-92 cluster regulates cell proliferation and collagen synthesis by targeting TGFB pathway in mouse palatal mesenchymal cells. J Cell Biochem 2012, 113(4):1235-1244. 10.1002/jcb.23457, 22095742.
63. Mendell JT. miRiad roles for the miR-17-92 cluster in development and disease. Cell 2008, 133(2):217-222. 10.1016/j.cell.2008.04.001, 2732113, 18423194.
64. Mavrakis KJ, Wolfe AL, Oricchio E, Palomero T, De Keersmaecker K, McJunkin K, Zuber J, James T, Khan AA, Leslie CS. Genome-wide RNA-mediated interference screen identifies miR-19 targets in Notch-induced T-cell acute lymphoblastic leukaemia. Nat Cell Biol 2010, 12(4):372-379. 10.1038/ncb2037, 2989719, 20190740.
65. Río P, Agirre X, Garate L, Baños R, Álvarez L, San José-Enériz E, Badell I, Casado JA, Garín M, Prósper F. Down-regulated expression of hsa-miR-181c in Fanconi anemia patients: implications in TNFα regulation and proliferation of hematopoietic progenitor cells. Blood 2012, 119(13):3042-3049. 10.1182/blood-2011-01-331017, 22310912.
66. Agrawal R, Tran U, Wessely O. The miR-30 miRNA family regulates Xenopus pronephros development and targets the transcription factor Xlim1/Lhx1. Development 2009, 136(23):3927-3936. 10.1242/dev.037432, 2778741, 19906860.
67. Akao Y, Nakagawa Y, Naoe T. let-7 microRNA functions as a potential growth suppressor in human colon cancer cells. Biol Pharm Bull 2006, 29(5):903-906. 10.1248/bpb.29.903, 16651716.
68. Shell S, Park SM, Radjabi AR, Schickel R, Kistner EO, Jewell DA, Feig C, Lengyel E, Peter ME. Let-7 expression defines two differentiation stages of cancer. Proc Natl Acad Sci 2007, 104(27):11400-11405. 10.1073/pnas.0704372104, 2040910, 17600087.
69. Ma K, He Y, Zhang H, Fei Q, Niu D, Wang D, Ding X, Xu H, Chen X, Zhu J. DNA methylation-regulated miR-193a-3p dictates resistance of hepatocellular carcinoma to 5-fluorouracil via repression of SRSF2 expression. J Biol Chem 2012, 287(8):5639-5649. 10.1074/jbc.M111.291229, 3285337, 22117060.
70. Kahai S, Lee SC, Lee DY, Yang J, Li M, Wang CH, Jiang Z, Zhang Y, Peng C, Yang BB. MicroRNA miR-378 regulates nephronectin expression modulating osteoblast differentiation by targeting GalNT-7. PLoS One 2009, 4(10):e7535. 10.1371/journal.pone.0007535, 2760121, 19844573.
71. Zhang L, Flygare J, Wong P, Lim B, Lodish HF. miR-191 regulates mouse erythroblast enucleation by down-regulating Riok3 and Mxi1. Genes Dev 2011, 25(2):119-124. 10.1101/gad.1998711, 3022257, 21196494.
72. Schaar DG, Medina DJ, Moore DF, Strair RK, Ting Y. miR-320 targets transferrin receptor 1 (CD71) and inhibits cell proliferation. Exp Hematol 2009, 37(2):245-255. 10.1016/j.exphem.2008.10.002, 19135902.
73. Li QJ, Chau J, Ebert PJR, Sylvester G, Min H, Liu G, Braich R, Manoharan M, Soutschek J, Skare P. miR-181a is an intrinsic modulator of T cell sensitivity and selection. Cell 2007, 129(1):147-161. 10.1016/j.cell.2007.03.008, 17382377.
74. Aslam MI, Patel M, Singh B, Jameson JS, Pringle JH. MicroRNAs are Novel Biomarkers for Detection of Colorectal Cancer. Biomarker 2012, 1-18. Croatia, Rijeka: In Tech, Khan TK.
75. Curtis J, Bourne F. Immunoglobulin quantitation in sow serum, colostrum and milk and the serum of young pigs. Biochimica et Biophysica Acta (BBA)-Protein Structure 1971, 236(1):319-332.
76. Kumura H, Sone T, Shimazaki K, Kobayashi E. Sequence analysis of porcine polymeric immunoglobulin receptor from mammary epithelial cells present in colostrum. J Dairy Res 2000, 67(04):631-636. 10.1017/S0022029900004404, 11131076.
77. Castigli E, Alt FW, Davidson L, Bottaro A, Mizoguchi E, Bhan AK, Geha RS. CD40-deficient mice generated by recombination-activating gene-2-deficient blastocyst complementation. Proc Natl Acad Sci 1994, 91(25):12135-12139. 10.1073/pnas.91.25.12135, 45391, 7527552.
78. Kawabe T, Naka T, Yoshida K, Tanaka T, Fujiwara H, Suematsu S, Yoshida N, Kishimoto T, Kikutani H. The immune responses in CD40-deficient mice: impaired immunoglobulin class switching and germinal center formation. Immunity 1994, 1(3):167. 10.1016/1074-7613(94)90095-7, 7534202.
79. Durandy A, Schiff C, Bonnefoy JY, Forveille M, Rousset F, Mazzei G, Milili M, Fischer A. Induction by anti-CD40 antibody or soluble CD40 ligand and cytokines of IgG, IgA and IgE production by B cells from patients with X-linked hyper IgM syndrome. Eur J Immunol 2005, 23(9):2294-2299.
80. Le Jan C, Chevaleyre C. Reduced expression of SLA Class 1 antigens by intestinal epithelium of newborn piglets. Vet Immunol Immunopathol 1996, 50(1):167-172.
81. Van Vlasselaer P, Punnonen J, De Vries J. Transforming growth factor-beta directs IgA switching in human B cells. J Immunol 1992, 148(7):2062-2067.
82. 2 Class Switching by Inducing Epithelial-Cell Secretion of the Cytokine APRIL. Immunity 2007, 26(6):812-826. 10.1016/j.immuni.2007.04.014, 17570691.
83. Bowman EP, Kuklin NA, Youngman KR, Lazarus NH, Kunkel EJ, Pan J, Greenberg HB, Butcher EC. The intestinal chemokine thymus-expressed chemokine (CCL25) attracts IgA antibody-secreting cells. J Exp Med 2002, 195(2):269-275. 10.1084/jem.20010670, 2193602, 11805153.
84. Svensson M, Marsal J, Ericsson A, Carramolino L, Brodén T, Márquez G, Agace WW. CCL25 mediates the localization of recently activated CD8alphabeta^+ lymphocytes to the small-intestinal mucosa. J Clin Investig 2002, 110(8):1113-1122. 10.1172/JCI0215988, 150799, 12393847.
85. Lanier LL, O'Fallon S, Somoza C, Phillips JH, Linsley PS, Okumura K, Ito D, Azuma M. CD80 (B7) and CD86 (B70) provide similar costimulatory signals for T cell proliferation, cytokine production, and generation of CTL. J Immunol 1995, 154(1):97-105.
86. Hutloff A, Dittrich AM, Beier KC, Eljaschewitsch B, Kraft R, Anagnostopoulos I, Kroczek RA. ICOS is an inducible T-cell co-stimulator structurally and functionally related to CD28. Nature 1999, 402:21-24.