Lymphotoxin Beta Receptor Signaling in Intestinal Epithelial Cells Orchestrates Innate Immune Responses against Mucosal Bacterial Infection

Immunity

Volumn 32, Issue 3, 2010, Pages 403-413

  Wang, Yugang ^a   Koroleva, Ekaterina P ^a   Kruglov, Andrei A ^b   Kuprash, Dmitry V ^c   Nedospasov, Sergei A ^b,c   Fu, Yang Xin ^a   Tumanov, Alexei V ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b DEUTSCHES RHEUMA FORSCHUNGSZENTRUM   (Germany)

^c ENGELHARDT INSTITUTE OF MOLECULAR BIOLOGY   (Russian Federation)

Author keywords

Cellimmuno; Molimmuno

Indexed keywords

CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; LYMPHOTOXIN BETA RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL INFECTION; CONTROLLED STUDY; HEMATOPOIETIC CELL; IMMUNOREGULATION; INFECTION PREVENTION; INNATE IMMUNITY; INTESTINE EPITHELIUM CELL; INTESTINE INFECTION; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

ADAPTIVE IMMUNITY; ANIMALS; BONE MARROW CELLS; CITROBACTER RODENTIUM; ENTEROBACTERIACEAE INFECTIONS; EPITHELIAL CELLS; IMMUNITY, INNATE; INTESTINAL MUCOSA; LYMPHOTOXIN BETA RECEPTOR; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; SIGNAL TRANSDUCTION;

EID: 77950022870     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.immuni.2010.02.011     Document Type: Article

References (45)

1. Alimzhanov M.B., Kuprash D.V., Kosco-Vilbois M.H., Luz A., Turetskaya R.L., Tarakhovsky A., Rajewsky K., Nedospasov S.A., Pfeffer K. Abnormal development of secondary lymphoid tissues in lymphotoxin beta-deficient mice. Proc. Natl. Acad. Sci. USA 1997, 94:9302-9307.
2. Anders R.A., Subudhi S.K., Wang J., Pfeffer K., Fu Y.X. Contribution of the lymphotoxin beta receptor to liver regeneration. J. Immunol. 2005, 175:1295-1300.
3. Appelberg R. Neutrophils and intracellular pathogens: Beyond phagocytosis and killing. Trends Microbiol. 2007, 15:87-92.
4. Browning J.L. Inhibition of the lymphotoxin pathway as a therapy for autoimmune disease. Immunol. Rev. 2008, 223:202-220.
5. Browning J.L., French L.E. Visualization of lymphotoxin-beta and lymphotoxin-beta receptor expression in mouse embryos. J. Immunol. 2002, 168:5079-5087.
6. Bry L., Brenner M.B. Critical role of T cell-dependent serum antibody, but not the gut-associated lymphoid tissue, for surviving acute mucosal infection with Citrobacter rodentium, an attaching and effacing pathogen. J. Immunol. 2004, 172:433-441.
7. Cella M., Fuchs A., Vermi W., Facchetti F., Otero K., Lennerz J.K., Doherty J.M., Mills J.C., Colonna M. A human natural killer cell subset provides an innate source of IL-22 for mucosal immunity. Nature 2009, 457:722-725.
8. Chiang E.Y., Kolumam G.A., Yu X., Francesco M., Ivelja S., Peng I., Gribling P., Shu J., Lee W.P., Refino C.J., et al. Targeted depletion of lymphotoxin-alpha-expressing TH1 and TH17 cells inhibits autoimmune disease. Nat. Med. 2009, 15:766-773.
9. Clausen B.E., Burkhardt C., Reith W., Renkawitz R., Forster I. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res. 1999, 8:265.
10. Cupedo T., Crellin N.K., Papazian N., Rombouts E.J., Weijer K., Grogan J.L., Fibbe W.E., Cornelissen J.J., Spits H. Human fetal lymphoid tissue-inducer cells are interleukin 17-producing precursors to RORC+ CD127+ natural killer-like cells. Nat. Immunol. 2009, 10:66-74.
11. Eberl G., Littman D.R. Thymic origin of intestinal alphabeta T cells revealed by fate mapping of RORgammat+ cells. Science 2004, 305:248-251.
12. Eberl G., Marmon S., Sunshine M.J., Rennert P.D., Choi Y., Littman D.R. An essential function for the nuclear receptor RORgamma(t) in the generation of fetal lymphoid tissue inducer cells. Nat. Immunol. 2004, 5:64.
13. Fu Y.X., Chaplin D.D. Development and maturation of secondary lymphoid tissues. Annu. Rev. Immunol. 1999, 17:399-433.
14. Fu Y.X., Huang G., Wang Y., Chaplin D.D. B lymphocytes induce the formation of follicular dendritic cell clusters in a lymphotoxin alpha-dependent fashion. J. Exp. Med. 1998, 187:1009-1018.
15. Futterer A., Mink K., Luz A., Kosco-Vilbois M.H., Pfeffer K. The lymphotoxin beta receptor controls organogenesis and affinity maturation in peripheral lymphoid tissues. Immunity 1998, 9:59-70.
16. Gibson D.L., Ma C., Rosenberger C.M., Bergstrom K.S., Valdez Y., Huang J.T., Khan M.A., Vallance B.A. Toll-like receptor 2 plays a critical role in maintaining mucosal integrity during Citrobacter rodentium-induced colitis. Cell. Microbiol. 2008, 10:388-403.
17. Gonzalez M., Mackay F., Browning J.L., Kosco-Vilbois M.H., Noelle R.J. The sequential role of lymphotoxin and B cells in the development of splenic follicles. J. Exp. Med. 1998, 187:997-1007.
18. Ivanov I.I., McKenzie B.S., Zhou L., Tadokoro C.E., Lepelley A., Lafaille J.J., Cua D.J., Littman D.R. The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 2006, 126:1121-1133.
19. Junt T., Tumanov A.V., Harris N., Heikenwalder M., Zeller N., Kuprash D.V., Aguzzi A., Ludewig B., Nedospasov S.A., Zinkernagel R.M. Expression of lymphotoxin beta governs immunity at two distinct levels. Eur. J. Immunol. 2006, 36:2061-2075.
20. Lebeis S.L., Bommarius B., Parkos C.A., Sherman M.A., Kalman D. TLR signaling mediated by MyD88 is required for a protective innate immune response by neutrophils to Citrobacter rodentium. J. Immunol. 2007, 179:566-577.
21. Luci C., Reynders A., Ivanov I.I., Cognet C., Chiche L., Chasson L., Hardwigsen J., Anguiano E., Banchereau J., Chaussabel D., et al. Influence of the transcription factor RORgammat on the development of NKp46+ cell populations in gut and skin. Nat. Immunol. 2009, 10:75-82.
22. Maaser C., Housley M.P., Iimura M., Smith J.R., Vallance B.A., Finlay B.B., Schreiber J.R., Varki N.M., Kagnoff M.F., Eckmann L. Clearance of Citrobacter rodentium requires B cells but not secretory immunoglobulin A (IgA) or IgM antibodies. Infect. Immun. 2004, 72:3315-3324.
23. MacDonald T.T., Frankel G., Dougan G., Goncalves N.S., Simmons C. Host defences to Citrobacter rodentium. Int. J. Med. Microbiol. 2003, 293:87-93.
24. Madison B.B., Dunbar L., Qiao X.T., Braunstein K., Braunstein E., Gumucio D.L. Cis elements of the villin gene control expression in restricted domains of the vertical (crypt) and horizontal (duodenum, cecum) axes of the intestine. J. Biol. Chem. 2002, 277:33275.
25. Mundy R., MacDonald T.T., Dougan G., Frankel G., Wiles S. Citrobacter rodentium of mice and man. Cell. Microbiol. 2005, 7:1697-1706.
26. Ohtsuka Y., Lee J., Stamm D.S., Sanderson I.R. MIP-2 secreted by epithelial cells increases neutrophil and lymphocyte recruitment in the mouse intestine. Gut 2001, 49:526-533.
27. Rakoff-Nahoum S., Paglino J., Eslami-Varzaneh F., Edberg S., Medzhitov R. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 2004, 118:229-241.
28. Satoh-Takayama N., Vosshenrich C.A., Lesjean-Pottier S., Sawa S., Lochner M., Rattis F., Mention J.J., Thiam K., Cerf-Bensussan N., Mandelboim O., et al. Microbial flora drives interleukin 22 production in intestinal NKp46+ cells that provide innate mucosal immune defense. Immunity 2008, 29:958-970.
29. Shakhov A.N., Lyakhov I.G., Tumanov A.V., Rubtsov A.V., Drutskaya L.N., Marino M.W., Nedospasov S.A. Gene profiling approach in the analysis of lymphotoxin and TNF deficiencies. J. Leukoc. Biol. 2000, 68:151.
30. Spahn T.W., Maaser C., Eckmann L., Heidemann J., Lugering A., Newberry R., Domschke W., Herbst H., Kucharzik T. The lymphotoxin-beta receptor is critical for control of murine Citrobacter rodentium-induced colitis. Gastroenterology 2004, 127:1463.
31. Spehlmann M.E., Dann S.M., Hruz P., Hanson E., McCole D.F., Eckmann L. CXCR2-dependent mucosal neutrophil influx protects against colitis-associated diarrhea caused by an attaching/effacing lesion-forming bacterial pathogen. J. Immunol. 2009, 183:3332-3343.
32. Summers-DeLuca L.E., McCarthy D.D., Cosovic B., Ward L.A., Lo C.C., Scheu S., Pfeffer K., Gommerman J.L. Expression of lymphotoxin-alphabeta on antigen-specific T cells is required for DC function. J. Exp. Med. 2007, 204:1071-1081.
33. Sun Z., Unutmaz D., Zou Y.R., Sunshine M.J., Pierani A., Brenner-Morton S., Mebius R.E., Littman D.R. Requirement for RORgamma in thymocyte survival and lymphoid organ development. Science 2000, 288:2369-2373.
34. Takatori H., Kanno Y., Watford W.T., Tato C.M., Weiss G., Ivanov I.I., Littman D.R., O'Shea J.J. Lymphoid tissue inducer-like cells are an innate source of IL-17 and IL-22. J. Exp. Med. 2009, 206:35-41.
35. Tamada K., Ni J., Zhu G., Fiscella M., Teng B., van Deursen J.M., Chen L. Cutting edge: Selective impairment of CD8+ T cell function in mice lacking the TNF superfamily member LIGHT. J. Immunol. 2002, 168:4832-4835.
36. Tsuji M., Suzuki K., Kitamura H., Maruya M., Kinoshita K., Ivanov I.I., Itoh K., Littman D.R., Fagarasan S. Requirement for lymphoid tissue-inducer cells in isolated follicle formation and T cell-independent immunoglobulin A generation in the gut. Immunity 2008, 29:261-271.
37. Tumanov A., Kuprash D., Lagarkova M., Grivennikov S., Abe K., Shakhov A., Drutskaya L., Stewart C., Chervonsky A., Nedospasov S. Distinct role of surface lymphotoxin expressed by B cells in the organization of secondary lymphoid tissues. Immunity 2002, 17:239-250.
38. Tumanov A.V., Grivennikov S.I., Shakhov A.N., Rybtsov S.A., Koroleva E.P., Takeda J., Nedospasov S.A., Kuprash D.V. Dissecting the role of lymphotoxin in lymphoid organs by conditional targeting. Immunol. Rev. 2003, 195:106-116.
39. Uren T.K., Wijburg O.L., Simmons C., Johansen F.E., Brandtzaeg P., Strugnell R.A. Vaccine-induced protection against gastrointestinal bacterial infections in the absence of secretory antibodies. Eur. J. Immunol. 2005, 35:180-188.
40. Vallance B.A., Deng W., Jacobson K., Finlay B.B. Host susceptibility to the attaching and effacing bacterial pathogen Citrobacter rodentium. Infect. Immun. 2003, 71:3443-3453.
41. Vivier E., Spits H., Cupedo T. Interleukin-22-producing innate immune cells: New players in mucosal immunity and tissue repair?. Nat. Rev. Immunol. 2009, 9:229-234.
42. Wang J., Anders R.A., Wu Q., Peng D., Cho J.H., Sun Y., Karaliukas R., Kang H.S., Turner J.R., Fu Y.X. Dysregulated LIGHT expression on T cells mediates intestinal inflammation and contributes to IgA nephropathy. J. Clin. Invest. 2004, 113:826-835.
43. Wang Y., Zhu M., Miller M., Fu Y.X. Immunoregulation by tumor necrosis factor superfamily member LIGHT. Immunol. Rev. 2009, 229:232-243.
44. Ware C.F. Network communications: Lymphotoxins, LIGHT, and TNF. Annu. Rev. Immunol. 2005, 23:787-819.
45. Zheng Y., Valdez P.A., Danilenko D.M., Hu Y., Sa S.M., Gong Q., Abbas A.R., Modrusan Z., Ghilardi N., de Sauvage F.J., Ouyang W. Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat. Med. 2008, 14:282-289.