Interleukin-12-producing CD103+ CD11b- CD8+ dendritic cells are responsible for eliciting gut intraepithelial lymphocyte response against Encephalitozoon cuniculi

Infection and Immunity

Volumn 83, Issue 12, 2015, Pages 4719-4730

  Moretto, Magali M ^a   Harrow, Danielle I ^a   Hawley, Teresa S ^b   Khan, Imtiaz A ^a  

^a GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^b GEORGE WASHINGTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD103 ANTIGEN; CD11B ANTIGEN; CD8 ANTIGEN; INTERLEUKIN 12; RETINOIC ACID; ALPHA E INTEGRINS; ALPHA INTEGRIN; BACTERIAL PROTEIN; GREEN FLUORESCENT PROTEIN; LEUKOCYTE ANTIGEN; PHOTOPROTEIN; YELLOW FLUORESCENT PROTEIN, BACTERIA;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN SPECIFICITY; ARTICLE; CELL ACTIVATION; CELL ISOLATION; CONTROLLED STUDY; CYTOKINE RELEASE; DENDRITIC CELL; ENCEPHALITOZOON CUNICULI; FLOW CYTOMETRY; INTESTINE EPITHELIUM; LAMINA PROPRIA; LYMPHOCYTE; MESENTERY LYMPH NODE; MOUSE; NONHUMAN; PRIORITY JOURNAL; UPREGULATION; ANIMAL; C57BL MOUSE; CD8+ T LYMPHOCYTE; ENCEPHALITOZOONOSIS; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; IMMUNOPHENOTYPING; INTESTINE; INTESTINE MUCOSA; LYMPH NODE; MICROBIOLOGY; MUCOSAL IMMUNITY; PATHOGENICITY; PATHOLOGY; REPORTER GENE; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

ANIMALS; ANTIGENS, CD; ANTIGENS, CD11B; BACTERIAL PROTEINS; CD8-POSITIVE T-LYMPHOCYTES; DENDRITIC CELLS; ENCEPHALITOZOON CUNICULI; ENCEPHALITOZOONOSIS; GENE EXPRESSION REGULATION; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; HOST-PATHOGEN INTERACTIONS; IMMUNITY, MUCOSAL; IMMUNOPHENOTYPING; INTEGRIN ALPHA CHAINS; INTERLEUKIN-12; INTESTINAL MUCOSA; INTESTINES; LUMINESCENT PROTEINS; LYMPH NODES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; SIGNAL TRANSDUCTION;

EID: 84949668475     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00820-15     Document Type: Article

References (52)

1. Lee SC, Corradi N, Doan S, Dietrich FS, Keeling PJ, Heitman J. 2010. Evolution of the sex-related locus and genomic features shared in microsporidia and fungi. PLoS One 5:e10539. http://dx.doi.org/10.1371/journal.pone.0010539.
2. Didier ES, Weiss LM. 2006. Microsporidiosis: current status. Curr Opin Infect Dis 19:485-492. http://dx.doi.org/10.1097/01.qco.0000244055.46382.23.
3. Chacin-Bonilla L, Panunzio AP, Monsalve-Castillo FM, Parra-Cepeda IE, Martinez R. 2006. Microsporidiosis in Venezuela: prevalence of intestinal microsporidiosis and its contribution to diarrhea in a group of human immunodeficiency virus-infected patients from Zulia State. Am J Trop Med Hyg 74:482-486.
4. Sokolova OI, Demyanov AV, Bowers LC, Didier ES, Yakovlev AV, Skarlato SO, Sokolova YY. 2011. Emerging microsporidian infections in Russian HIV-infected patients. J Clin Microbiol 49:2102-2108. http://dx.doi.org/10.1128/JCM.02624-10.
5. Viriyavejakul P, Nintasen R, Punsawad C, Chaisri U, Punpoowong B, Riganti M. 2009. High prevalence of Microsporidium infection in HIVinfected patients. Southeast Asian J Trop Med Public Health 40:223-228.
6. Orenstein JM, Russo P, Didier ES, Bowers C, Bunin N, Teachey DT. 2005. Fatal pulmonary microsporidiosis due to Encephalitozoon cuniculi following allogeneic bone marrow transplantation for acute myelogenous leukemia. Ultrastruct Pathol 29:269-276. http://dx.doi.org/10.1080/01913120590951257.
7. Sivgin S, Eser B, Kaynar L, Kurnaz F, Sivgin H, Yazar S, Cetin M, Unal A. 2013. Encephalitozoon intestinalis: a rare cause of diarrhea in an allogeneic hematopoietic stem cell transplantation (HSCT) recipient complicated by albendazole-related hepatotoxicity. Turk J Haematol 30:204-208. http://dx.doi.org/10.4274/Tjh.90692.
8. Kicia M, Wesolowska M, Jakuszko K, Kopacz Z, Sak B, Kvetonova D, Krajewska M, Kvac M. 2014. Concurrent infection of the urinary tract with Encephalitozoon cuniculi and Enterocytozoon bieneusi in a renal transplant recipient. J Clin Microbiol 52:1780-1782. http://dx.doi.org/10.1128/JCM.03328-13.
9. Hocevar SN, Paddock CD, Spak CW, Rosenblatt R, Diaz-Luna H, Castillo I, Luna S, Friedman GC, Antony S, Stoddard RA, Tiller RV, Peterson T, Blau DM, Sriram RR, da Silva A, de Almeida M, Benedict T, Goldsmith CS, Zaki SR, Visvesvara GS, Kuehnert MJ. 2014. Microsporidiosis acquired through solid organ transplantation: a public health investigation. Ann Intern Med 160:213-220. http://dx.doi.org/10.7326/M13-2226.
10. Kotkova M, Sak B, Kvetonova D, Kvac M. 2013. Latent microsporidiosis caused by Encephalitozoon cuniculi in immunocompetent hosts: a murine model demonstrating the ineffectiveness of the immune system and treatment with albendazole. PLoS One 8:e60941. http://dx.doi.org/10.1371/journal.pone.0060941.
11. Snowden KF, Didier ES, Orenstein JM, Shadduck JA. 1998. Animal models of human microsporidial infections. Lab Anim Sci 48:589-592.
12. Hayday A, Theodoridis E, Ramsburg E, Shires J. 2001. Intraepithelial lymphocytes: exploring the third way in immunology. Nat Immunol 2:997-1003. http://dx.doi.org/10.1038/ni1101-997.
13. Li Z, Zhang C, Zhou Z, Zhang J, Tian Z. 2012. Small intestinal intraepithelial lymphocytes expressing CD8 and T cell receptor γδ are involved in bacterial clearance during Salmonella enterica serovar Typhimurium infection. Infect Immun 80:565-574. http://dx.doi.org/10.1128/IAI.05078-11.
14. Culshaw RJ, Bancroft GJ, McDonald V. 1997. Gut intraepithelial lymphocytes induce immunity against Cryptosporidium infection through a mechanism involving gamma interferon production. Infect Immun 65: 3074-3079.
15. Buzoni-Gatel D, Lepage AC, Dimier-Poisson IH, Bout DT, Kasper LH. 1997. Adoptive transfer of gut intraepithelial lymphocytes protects against murine infection with Toxoplasma gondii. J Immunol 158:5883-5889.
16. Müller S, Buhler-Jungo M, Mueller C. 2000. Intestinal intraepithelial lymphocytes exert potent protective cytotoxic activity during an acute virus infection. J Immunol 164:1986-1994. http://dx.doi.org/10.4049/jimmunol.164.4.1986.
17. Moretto M, Weiss LM, Khan IA. 2004. Induction of a rapid and strong antigen-specific intraepithelial lymphocyte response during oral Encephalitozoon cuniculi infection. J Immunol 172:4402-4409. http://dx.doi.org/10.4049/jimmunol.172.7.4402.
18. Moretto MM, Weiss LM, Combe CL, Khan IA. 2007. IFN-γ-producing dendritic cells are important for priming of gut intraepithelial lymphocyte response against intracellular parasitic infection. J Immunol 179:2485-2492. http://dx.doi.org/10.4049/jimmunol.179.4.2485.
19. Mellman I, Steinman RM. 2001. Dendritic cells: specialized and regulated antigen processing machines. Cell 106:255-258. http://dx.doi.org/10.1016/S0092-8674(01)00449-4.
20. + dendritic cells in the regulation of tissue-selective T cell homing. J Exp Med 202:1063-1073. http://dx.doi.org/10.1084/jem.20051100.
21. + regulatory T cells via a TGF-β and retinoic acid-dependent mechanism. J Exp Med 204:1757-1764. http://dx.doi.org/10.1084/jem.20070590.
22. Guan H, Moretto M, Bzik DJ, Gigley J, Khan IA. 2007. NK cells enhance dendritic cell response against parasite antigens via NKG2D pathway. J Immunol 179:590-596. http://dx.doi.org/10.4049/jimmunol.179.1.590.
23. Lefrançois L, Lycke N. 2001. Isolation of mouse small intestinal intraepithelial lymphocytes, Peyer's patch, and lamina propria cells. Curr Protoc Immunol Chapter 3:Unit 3.19. http://dx.doi.org/10.1002/0471142735.im0319s17.
24. Lutz MB, Kukutsch N, Ogilvie AL, Rossner S, Koch F, Romani N, Schuler G. 1999. An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J Immunol Methods 223:77-92. http://dx.doi.org/10.1016/S0022-1759(98)00204-X.
25. Montufar-Solis D, Klein JR. 2006. An improved method for isolating intraepithelial lymphocytes (IELs) from the murine small intestine with consistently high purity. J Immunol Methods 308:251-254. http://dx.doi.org/10.1016/j.jim.2005.10.008.
26. Orenstein JM, Gaetz HP, Yachnis AT, Frankel SS, Mertens RB, Didier ES. 1997. Disseminated microsporidiosis in AIDS: are any organs spared? AIDS 11:385-386.
27. - dendritic cells migrate in lymph and prime effector T cells. Mucosal Immunol 6:104-113. http://dx.doi.org/10.1038/mi.2012.53.
28. + dendritic cells into the intestinal epithelium to sample bacterial antigens for presentation. Immunity 38:581-595. http://dx.doi.org/10.1016/j.immuni.2013.01.009.
29. Courret N, Darche S, Sonigo P, Milon G, Buzoni-Gatel D, Tardieux I. 2006. CD11c-and CD11b-expressing mouse leukocytes transport single Toxoplasma gondii tachyzoites to the brain. Blood 107:309-316. http://dx.doi.org/10.1182/blood-2005-02-0666.
30. Pron B, Boumaila C, Jaubert F, Berche P, Milon G, Geissmann F, Gaillard JL. 2001. Dendritic cells are early cellular targets of Listeria monocytogenes after intestinal delivery and are involved in bacterial spread in the host. Cell Microbiol 3:331-340. http://dx.doi.org/10.1046/j.1462-5822.2001.00120.x.
31. Matloubian M, Lo CG, Cinamon G, Lesneski MJ, Xu Y, Brinkmann V, Allende ML, Proia RL, Cyster JG. 2004. Lymphocyte egress from thymus and peripheral lymphoid organs is dependent on S1P receptor 1. Nature 427:355-360. http://dx.doi.org/10.1038/nature02284.
32. Czeloth N, Bernhardt G, Hofmann F, Genth H, Forster R. 2005. Sphingosine-1-phosphate mediates migration of mature dendritic cells. J Immunol 175:2960-2967. http://dx.doi.org/10.4049/jimmunol.175.5.2960.
33. Lan YY, De Creus A, Colvin BL, Abe M, Brinkmann V, Coates PT, Thomson AW. 2005. The sphingosine-1-phosphate receptor agonist FTY720 modulates dendritic cell trafficking in vivo. Am J Transplant 5:2649-2659. http://dx.doi.org/10.1111/j.1600-6143.2005.01085.x.
34. Rothkötter HJ, Pabst R, Bailey M. 1999. Lymphocyte migration in the intestinal mucosa: entry, transit and emigration of lymphoid cells and the influence of antigen. Vet Immunol Immunopathol 72:157-165. http://dx.doi.org/10.1016/S0165-2427(99)00128-2.
35. Shortman K, Caux C. 1997. Dendritic cell development: multiple pathways to nature's adjuvants. Stem Cells 15:409-419. http://dx.doi.org/10.1002/stem.150409.
36. Pabst O, Bernhardt G. 2010. The puzzle of intestinal lamina propria dendritic cells and macrophages. Eur J Immunol 40:2107-2111. http://dx.doi.org/10.1002/eji.201040557.
37. +, antigen sampling cells migrate in lymph and serve classical dendritic cell functions. J Exp Med 206:3101-3114. http://dx.doi.org/10.1084/jem.20091925.
38. Trinchieri G. 1998. Interleukin-12: a cytokine at the interface of inflammation and immunity. Adv Immunol 70:83-243. http://dx.doi.org/10.1016/S0065-2776(08)60387-9.
39. Liu CH, Fan YT, Dias A, Esper L, Corn RA, Bafica A, Machado FS, Aliberti J. 2006. Dendritic cells are essential for in vivo IL-12 production and developmentof resistance against Toxoplasma gondii infection in mice. JImmunol 177:31-35. http://dx.doi.org/10.4049/jimmunol.177.1.31.
40. Berberich C, Ramirez-Pineda JR, Hambrecht C, Alber G, Skeiky YA, Moll H. 2003. Dendritic cell (DC)-based protection against an intracellular pathogen is dependent upon DC-derived IL-12 and can be induced by molecularly defined antigens. J Immunol 170:3171-3179. http://dx.doi.org/10.4049/jimmunol.170.6.3171.
41. + DC, with a plasmacytoid phenotype, induce differentiation and support function of T cells with regulatory properties. Immunology 108:481-492. http://dx.doi.org/10.1046/j.1365-2567.2003.01606.x.
42. + dendritic cells in the small intestine expresses TLR3, TLR7, and TLR9 and induces Th1 response and CTL activity. J Immunol 186:6287-6295. http://dx.doi.org/10.4049/jimmunol.1004036.
43. Gately MK, Wolitzky AG, Quinn PM, Chizzonite R. 1992. Regulation of human cytolytic lymphocyte responses by interleukin-12. Cell Immunol 143:127-142. http://dx.doi.org/10.1016/0008-8749(92)90011-D.
44. Johansson-Lindbom B, Svensson M, Wurbel MA, Malissen B, Marquez G, Agace W. 2003. Selective generation of gut tropic T cells in gutassociated lymphoid tissue (GALT): requirement for GALT dendritic cells and adjuvant. J Exp Med 198:963-969. http://dx.doi.org/10.1084/jem.20031244.
45. Mora JR, Bono MR, Manjunath N, Weninger W, Cavanagh LL, Rosemblatt M, Von Andrian UH. 2003. Selective imprinting of gut-homing T cells by Peyer's patch dendritic cells. Nature 424:88-93. http://dx.doi.org/10.1038/nature01726.
46. Iwata M, Hirakiyama A, Eshima Y, Kagechika H, Kato C, Song SY. 2004. Retinoic acid imprints gut-homing specificity on T cells. Immunity 21:527-538. http://dx.doi.org/10.1016/j.immuni.2004.08.011.
47. Montufar-Solis D, Garza T, Klein JR. 2007. T-cell activation in the intestinal mucosa. Immunol Rev 215:189-201. http://dx.doi.org/10.1111/j.1600-065X.2006.00471.x.
48. Lefrançois L, Parker CM, Olson S, Muller W, Wagner N, Schon MP, Puddington L. 1999. The role of β7 integrins in CD8 T cell trafficking during an antiviral immune response. J Exp Med 189:1631-1638. http://dx.doi.org/10.1084/jem.189.10.1631.
49. + conventional dendritic cells. J Exp Med 207:823-836. http://dx.doi.org/10.1084/jem.20091627.
50. + dendritic cells are key players in the innate immune control of Cryptosporidium parvum infection in neonatal mice. PLoS Pathog 9:e1003801. http://dx.doi.org/10.1371/journal.ppat.1003801.
51. Chirdo FG, Millington OR, Beacock-Sharp H, Mowat AM. 2005. Immunomodulatory dendritic cells in intestinal lamina propria. Eur J Immunol 35:1831-1840. http://dx.doi.org/10.1002/eji.200425882.
52. Bogunovic M, Ginhoux F, Helft J, Shang L, Hashimoto D, Greter M, Liu K, Jakubzick C, Ingersoll MA, Leboeuf M, Stanley ER, Nussenzweig M, Lira SA, Randolph GJ, Merad M. 2009. Origin of the lamina propria dendritic cell network. Immunity 31:513-525. http://dx.doi.org/10.1016/j.immuni.2009.08.010.