Redundancy in tumor necrosis factor (TNF) and lymphotoxin (LT) signaling in vivo: Mice with inactivation of the entire TNF/LT locus versus single-knockout mice

Molecular and Cellular Biology

Volumn 22, Issue 24, 2002, Pages 8626-8634

  Kuprash, Dmitry V ^a,b   Alimzhanov, Marat B ^a,c,d   Tumanov, Alexei V ^a,b   Grivennikov, Sergei I ^a   Shakhov, Alexander N ^b   Drutskaya, Ludmila N ^b   Marino, Michael W ^e   Turetskaya, Regina L ^a,b   Anderson, Arthur O ^f   Rajewsky, Klaus ^d   Pfeffer, Klaus ^c   Nedospasov, Sergei A ^a,b  

^a MOSCOW STATE UNIVERSITY   (Russian Federation)

^b SAIC FREDERICK INC   (United States)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^d UNIVERSITY OF COLOGNE   (Germany)

^e MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^f US Army Medical Research   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LYMPHOTOXIN; TUMOR NECROSIS FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ARTICLE; B LYMPHOCYTE; CELL COMPARTMENTALIZATION; CONTROLLED STUDY; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; GENE INACTIVATION; GENE LOCUS; GENETIC RECOMBINATION; KNOCKOUT MOUSE; LEUKOCYTE COUNT; LYMPHOID CELL; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SPLEEN; T LYMPHOCYTE;

ANIMALS; B-LYMPHOCYTES; GENE EXPRESSION REGULATION; GENE TARGETING; LEUKOCYTES; LYMPHOID TISSUE; LYMPHOTOXIN-ALPHA; MICE; MICE, KNOCKOUT; MICE, MUTANT STRAINS; MULTIGENE FAMILY; SIGNAL TRANSDUCTION; SPLEEN; T-LYMPHOCYTES; TUMOR NECROSIS FACTOR-ALPHA;

ANIMALIA;

EID: 18744387205     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.22.24.8626-8634.2002     Document Type: Article

References (70)

1. Alimzhanov, M. B., D. V. Kuprash, M. H. Kosco-Vilbois, A. Luz, R. L. Turetskaya, A. Tarakhovsky, K. Rajewsky, S. A. Nedospasov, and K. Pfeffer. 1997. Abnormal development of secondary lymphoid tissues in lymphotoxin beta-deficient mice. Proc. Natl. Acad. Sci. USA 94:9302-9307.
2. Amiot, F., Y. Bellkaid, M. Lebastard, P. Ave, F. Dautry, and G. Milon. 1996. Abnormal organisation of the splenic marginal zone and the correlated leukocytosis in lymphotoxin-alpha and tumor necrosis factor alpha double deficient mice. Eur. Cytokine Netw. 7:733-739.
3. Arbibe, L., D. Vial, I. Rosinski-Chupin, N. Havet, M. Huerre, B. B. Vargaftig, and L. Touqui. 1997. Endotoxin induces expression of type II phospholipase A2 in macrophages during acute lung injury in guinea pigs: Involvement of TNF-alpha in lipopolysaccharide-induced type II phospholipase A2 synthesis. J. Immunol. 159:391-400.
4. Badwey, J. A., and M. L. Karnovsky. 1980. Active oxygen species and the functions of phagocytic leukocytes. Annu. Rev. Biochem. 49:695-726.
5. Banks, T. A., B. T. Rouse, M. K. Kerley, P. J. Blair, V. L. Godfrey, N. A. Kuklin, D. M. Bouley, J. Thomas, S. Kanangat, and M. L. Mucenski. 1995. Lymphotoxin-alpha-deficient mice. Effects on secondary lymphoid organ development and humoral immune responsiveness. J. Immunol. 155:1685-1693.
6. Berger, D. P., D. Naniche, M. T. Crowley, P. A. Koni, R. A. Flavell, and M. B. Oldstone. 1999. Lymphotoxin-beta-deficient mice show defective antiviral immunity. Virology 260:136-147.
7. Browning, J. L., A. Ngam-ek, P. Lawton, J. DeMarinis, R. Tizard, E. P. Chow, C. Hession, B. O'Brine-Greco, S. F. Foley, and C. F. Ware. 1993. Lymphotoxin beta, a novel member of the TNF family that forms a heteromeric complex with lymphotoxin on the cell surface. Cell 72:847-856.
8. Carswell, E. A., L. J. Old, R. L. Kassel, S. Green, N. Fiore, and B. Williamson. 1975. An endotoxin-induced serum factor that causes necrosis of tumors. Proc. Natl. Acad. Sci. USA 72:3666-3670.
9. Crowe, P. D., T. L. VanArsdale, B. N. Walter, C. F. Ware, C. Hession, B. Ehrenfels, J. L. Browning, W. S. Din, R. G. Goodwin, and C. A. Smith. 1994. A lymphotoxin-beta-specific receptor. Science 264:707-710.
10. Cyster, J. G. 1999. Chemokines and cell migration in secondary lymphoid organs. Science 286:2098-2102.
11. Davis, I. A., and B. T. Rouse. 1998. Immune responsiveness of lymphotoxinalpha-deficient mice: Two reconstitution models. Cell. Immunol. 189:116-124.
12. De Togni, P., J. Goellner, N. H. Ruddle, P. R. Streeter, A. Fick, S. Mariathasan, S. C. Smith, R. Carlson, L. P. Shornick, J. Strauss-Schoenberger, J. H. Russell, R. Karr, and D. D. Chaplin. 1994. Abnormal development of peripheral lymphoid organs in mice deficient in lymphotoxin. Science 264:703-707.
13. Elomaa, O., M. Kangas, C. Sahlberg, J. Tuukkanen, R. Sormunen, A. Liakka, I. Thesleff, G. Kraal, and K. Tryggvason. 1995. Cloning of a novel bacteria-binding receptor structurally related to scavenger receptors and expressed in a subset of macrophages. Cell 80:603-609.
14. Endres, R., A. Luz, H. Schulze, H. Neubauer, A. Futterer, S. M. Holland, H. Wagner, and K. Pfeffer. 1997. Listeriosis in p47(phox-/-) and TRp55-/mice: Protection despite absence of ROI and susceptibility despite presence of RNI. Immunity 7:419-432.
15. Erickson, S. L., F. J. de Sauvage, K. Kikly, K. Carver-Moore, S. Pitts-Meek, N. Gillett, K. C. Sheehan, R. D. Schreiber, D. V. Goeddel, and M. W. Moore. 1994. Decreased sensitivity to tumour-necrosis factor but normal T-cell development in TNF receptor-2-deficient mice. Nature 372:560-563.
16. Eugster, H. P., M. Muller, U. Karrer, B. D. Car, B. Schnyder, V. M. Eng, G. Woerly, M. Le Hir, F. di Padova, M. Aguet, R. Zinkernagel, H. Bluethmann, and B. Ryffel. 1996. Multiple immune abnormalities in tumor necrosis factor and lymphotoxin-alpha double-deficient mice. Int. Immunol. 8:23-36.
17. Everest, P., M. Roberts, and G. Dougan. 1998. Susceptibility to Salmonella typhimurium infection and effectiveness of vaccination in mice deficient in the tumor necrosis factor alpha p55 receptor. Infect. Immun. 66:3355-3364.
18. Fu, Y. X., H. Molina, M. Matsumoto, G. Huang, J. Min, and D. D. Chaplin. 1997. Lymphotoxin-alpha (LTalpha) supports development of splenic follicular structure that is required for IgG responses. J. Exp. Med. 185:2111-2120.
19. Futterer, A., K. Mink, A. Luz, M. H. Kosco-Vilbois, and K. Pfeffer. 1998. The lymphotoxin beta receptor controls organogenesis and affinity maturation in peripheral lymphoid tissues. Immunity 9:59-70.
20. Giroir, B. P., T. Brown, and B. Beutler. 1992. Constitutive synthesis of tumor necrosis factor in the thymus. Proc. Natl. Acad. Sci. USA 89:4864-4868.
21. Gough, P. J., and S. Gordon. 2000. The role of scavenger receptors in the innate immune system. Microbes Infect. 2:305-311.
22. Granger, G. A., and T. W. Williams. 1968. Lymphocyte cytotoxicity in vitro: Activation and release of a cytotoxic factor. Nature 218:1253-1254.
23. Gray, P. W., B. B. Aggarwal, C. V. Benton, T. S. Bringman, W. J. Henzel, J. A. Jarrett, D. W. Leung, B. Moffat, P. Ng, and L. P. Svedersky. 1984. Cloning and expression of cDNA for human lymphotoxin, a lymphokine with tumour necrosis activity. Nature 312:721-724.
24. Gu, H., Y. R. Zou, and K. Rajewsky. 1993. Independent control of immunoglobulin switch recombination at individual switch regions evidenced through Cre-loxP-mediated gene targeting. Cell 73:1155-1164.
25. Hughes, E. A., and J. E. Galan. 2002. Immune response to Salmonella: Location, location, location? Immunity 16:325-328.
26. Ito, D., T. C. Back, A. N. Shakhov, R. H. Wiltrout, and S. A. Nedospasov. 1999. Mice with a targeted mutation in lymphotoxin-alpha exhibit enhanced tumor growth and metastasis: Impaired NK cell development and recruitment. J. Immunol. 163:2809-2815.
27. Jones, B. D., and S. Falkow. 1996. Salmonellosis: Host immune responses and bacterial virulence determinants. Annu. Rev. Immunol. 14:533-561.
28. Jones, B. D., N. Ghori, and S. Falkow. 1994. Salmonella typhimurium initiates murine infection by penetrating and destroying the specialized epithelial M cells of the Peyer's patches. J. Exp. Med. 180:15-23.
29. Joyner, A. L. 1993. Gene Targeting: A Practical Approach. IRL Press, New York, N.Y.
30. Karrer, U., A. Althage, B. Odermatt, C. W. M. Roberts, S. J. Korsmeyer, S. Miyawaki, H. Hengartner, and R. M. Zinkernagel. 1997. On the key role of secondary lymphoid organs in antiviral immune responses studied in alymphoplastic (aly/aly) and spleenless (Hox11-/-) mutant mice. J. Exp. Med. 185:2157-2170.
31. Kaufmann, S. H. 1993. Immunity to intracellular bacteria. Annu. Rev. Immunol. 11:129-163.
32. Koni, P. A., R. Sacca, P. Lawton, J. L. Browning, N. H. Ruddle, and R. A. Flavell. 1997. Distinct roles in lymphoid organogenesis for lymphotoxins alpha and beta revealed in lymphotoxin beta-deficient mice. Immunity 6:491-500.
33. Korner, H., M. Cook, D. S. Riminton, F. A. Lemckert, R. M. Hoek, B. Ledermann, F. Kontgen, B. Fazekas de St. Groth, and J. D. Sedgwick. 1997. Distinct roles for lymphotoxin-alpha and tumor necrosis factor in organogenesis and spatial organization of lymphoid tissue. Eur J. Immunol. 27:2600-2609.
34. Kuprash, D. V., M. B. Alimzhanov, D. K. Pokholok, S. V. Kozlov, T. I. Novobrantseva, R. L. Turetskaia, and S. A. Nedospasov. 1994. Characteristics of murine chromosome 17 containing three tumor necrosis factor family genes, including the gene of the transmembrane subunit of lymphotoxin. Dokl. Akad. Nauk 337:683-686. (In Russian.)
35. Kuprash, D. V., M. B. Alimzhanov, A. Tumanov, A. O. Anderson, K. Pfeffer, and S. A. Nedospasov. 1999. TNF and lymphotoxin beta cooperate in the maintenance of secondary lymphoid tissue microarchitecture but not in the development of lymph nodes. J. Immunol. 163:6575-6580.
36. Lawton, P., J. Nelson, R. Tizard, and J. L. Browning. 1995. Characterization of the mouse lymphotoxin-beta gene. J. Immunol. 154:239-246.
37. Locksley, R. M., N. Killeen, and M. J. Lenardo. 2001. The TNF and TNF receptor superfamilies: Integrating mammalian biology. Cell 104:487-501.
38. Marino, M. W., A. Dunn, D. Grail, M. Inglese, Y. Noguchi, E. Richards, A. Jungbluth, H. Wada, M. Moore, B. Williamson, S. Basu, and L. J. Old. 1997. Characterization of tumor necrosis factor-deficient mice. Proc. Natl. Acad. Sci. USA 94:8093-8098.
39. Mastroeni, P., J. N. Skepper, and C. E. Hormaeche. 1995. Effect of antitumor necrosis factor alpha antibodies on histopathology of primary Salmonella infections. Infect. Immun. 63:3674-3682.
40. Matsumoto, M., S. Mariathasan, M. H. Nahm, F. Baranyay, J. J. Peschon, and D. D. Chaplin. 1996. Role of lymphotoxin and the type I TNF receptor in the formation of germinal centers. Science 271:1289-1291.
41. McSorley, S. J., S. Asch, M, Costalonga, R. L. Reinhardt, and M. K. Jenkins. 2002. Tracking salmonella-specific CD4 T cells in vivo reveals a local mucosal response to a disseminated infection. Immunity 16:365-377.
42. Mebius, R. E., P. Rennert, and I. L. Weissman. 1997. Developing lymph nodes collect CD4+CD3- LTbeta+ cells that can differentiate to APC, NK cells, and follicular cells but not T or B cells. Immunity 7:493-504.
43. Morrissey, P. J., K. Charrier, and S. N. Vogel. 1995. Exogenous tumor necrosis factor alpha and interleukin-1α increase resistance to Salmonella typhimurium: Efficacy is influenced by the Ity and Lps loci. Infect. Immun. 63:3196-3198.
44. Muller, U., C. V. Jongeneel, S. A. Nedospasov, K. F. Lindahl, and M. Steinmetz. 1987. Tumour necrosis factor and lymphotoxin genes map close to H-2D in the mouse major histocompatibility complex. Nature 325:265-267.
45. Nedospasov, S. A., B. Hirt, A. N. Shakhov, V. N. Dobrynin, E. Kawashima, R. S. Accolla, and C. V. Jongeneel. 1986. The genes for tumor necrosis factor (TNF-alpha) and lymphotoxin (TNF-beta) are tandemly arranged on chromosome 17 of the mouse. Nucleic Acids Res. 14:7713-7725.
46. Nedospasov, S. A., A. N. Shakhov, R. L. Turetskaya, V. A. Mett, M. M. Azizov, G. P. Georgiev, V. G. Korobko, V. N. Dobrynin, S. A. Filippov, N. S. Bystrov, E. F. Boldyreva, S. A. Chuvpilo, A. M. Chumakov, L. N. Shingarova, and Y. A. Ovchinnikov. 1986. Tandem arrangement of genes coding for tumor necrosis factor (TNF-alpha) and lymphotoxin (TNF-beta) in the human genome. Cold Spring Harbor Symp. Quant. Biol. 51:611-624.
47. Neumann, B., A. Luz, K. Pfeffer, and B. Holzmann. 1996. Defective Peyer's patch organogenesis in mice lacking the 55-kD receptor for tumor necrosis factor. J. Exp. Med. 184:259-264.
48. Ngo, V. N., H. Korner, M. D. Gunn, K. N. Schmidt, R. D. Sean, M. D. Cooper, J. L. Browning, J. D. Sedgwick, and J. G. Cyster. 1999. Lymphotoxin alpha/beta and tumor necrosis factor are required for stromal cell expression of homing chemokines in B and T cell areas of the spleen. J. Exp. Med. 189:403-412.
49. Pasparakis, M., L. Alexopoulou, V. Episkopou, and G. Kollias. 1996. Immune and inflammatory responses in TNF alpha-deficient mice: A critical requirement for TNF alpha in the formation of primary B cell follicles, follicular dendritic cell networks and germinal centers, and in the maturation of the humoral immune response. J. Exp. Med. 184:1397-1411.
50. Pennica, D., G. E. Nedwin, J. S. Hayflick, P. H. Seeburg, R. Derynck, M. A. Palladino, W. J. Kohr, B. B. Aggarwal, and D. V. Goeddel. 1984. Human tumour necrosis factor: Precursor structure, expression and homology to lymphotoxin. Nature 312:724-729.
51. Pfeffer, K., T. Matsuyama, T. M. Kundig, A. Wakeham, K. Kishihara, A. Shahinian, K. Wiegmann, P. S. Ohashi, M. Kronke, and T. W. Mak. 1993. Mice deficient for the 55 kd tumor necrosis factor receptor are resistant to endotoxic shock, yet succumb to L. monocytogenes infection. Cell 73:457-467.
52. Pokholok, D. K., I. G. Maroulakou, D. V. Kuprash, M. B. Alimzhanov, S. V. Kozlov, T. I. Novobrantseva, R. L. Turetskaya, J. E. Green, and S. A. Nedospasov. 1995. Cloning and expression analysis of the murine lymphotoxin beta gene. Proc. Natl. Acad. Sci. USA 92:674-678.
53. Rennert, P. D., J. L. Browning, R. Mebius, F. Mackay, and P. S. Hochman. 1996. Surface lymphotoxin alpha/beta complex is required for the development of peripheral lymphoid organs. J. Exp. Med. 184:1999-2006.
54. Rescigno, M., M. Urbano, B. Valzasina, M. Francolini, G. Rotta, R. Bonasio, F. Granucci, J. P. Kraehenbuhl, and P. Ricciardi-Castagnoli. 2001. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat. Immunol. 2:361-367.
55. Roach, D. R., H. Briscoe, B. Saunders, M. P. France, S. Riminton, and W. J. Britton. 2001. Secreted lymphotoxin-alpha is essential for the control of an intracellular bacterial infection. J. Exp. Med. 193:239-246.
56. Rothe, J., W. Lesslauer, H. Lotscher, Y. Lang, P. Koebel, F. Kontgen, A. Althage, R. Zinkernagel, M. Steinmetz, and H. Bluethmann. 1993. Mice lacking the tumour necrosis factor receptor 1 are resistant to TNF-mediated toxicity but highly susceptible to infection by Listeria monocytogenes. Nature 364:798-802.
57. Ruddle, N. H., and B. H. Waksman. 1967. Cytotoxic effect of lymphocyteantigen interaction in delayed hypersensitivity. Science 157:1060-1062.
58. Sauer, B. 1993. Manipulation of transgenes by site-specific recombination: Use of Cre recombinase. Methods Enzymol. 225:890-900.
59. Scheu, S., J. Alferink, T. Potzel, W. Barchet, U. Kalinke, and K. Pfeffer. 2002. Targeted disruption of LIGHT causes defects in costimulatory T cell activation and reveals cooperation with lymphotoxin beta in mesenteric lymph node genesis. J. Exp. Med. 195:1613-1624.
60. Shakhov, A. N., I. G. Lyakhov, A. V. Tumanov, A. V. Rubtsov, L. N. Drutskaya, M. W. Marino, and S. A. Nedospasov. 2000. Gene profiling approach in the analysis of lymphotoxin and TNF deficiencies. J. Leukoc. Biol. 68:151-157.
61. Shakhov, A. N., and S. A. Nedospasov. 2001. Expression profiling in knockout mice: Lymphotoxin versus tumor necrosis factor in the maintenance of splenic microarchitecture. Cytokine Growth Factor Rev. 12:107-119.
62. 2 family, is associated with lymphotoxin deficiency. Genes Immunity 1:191-199.
63. Unanue, E. R. 1997. Inter-relationship among macrophages, natural killer cells and neutrophils in early stages of Listeria resistance. Curr. Opin. Immunol. 9:35-43.
64. Valentin, E., R. S. Koduri, J. C. Scimeca, G. Carle, M. H. Gelb, M. Lazdunski, and G. Lambeau. 1999. Cloning and recombinant expression of a novel mouse-secreted phospholipase A2. J. Biol. Chem. 274:19152-19160.
65. Van Vliet, E., M. Melis, J. M. Foidart, and W. van Ewijk. 1986. Reticular fibroblasts in peripheral lymphoid organs identified by a monoclonal antibody. J. Histochem. Cytochem. 34:883-890.
66. Wang, J., A. Foster, R. Chin, P. Yu, Y. Sun, Y. Wang, K. Pfeffer, and Y. X. Fu. 2002. The complementation of lymphotoxin deficiency with LIGHT, a newly discovered TNF family member, for the restoration of secondary lymphoid structure and function. Eur. J. Immunol. 32:1969-1979.
67. Ware, C. F., P. D. Crowe, M. H. Grayson, M. J. Androlewicz, and J. L. Browning. 1992. Expression of surface lymphotoxin and tumor necrosis factor on activated T, B, and natural killer cells. J. Immunol. 149:3881-3888.
68. Wilhelm, P., D. S. Riminton, U. Ritter, F. A. Lemckert, C. Scheidig, R. Hoek, J. D. Sedgwick, and H. Korner. 2002. Membrane lymphotoxin contributes to anti-leishmanial immunity by controlling structural integrity of lymphoid organs. Eur. J. Immunol. 32:1993-2003.
69. Wu, Q., Y. Wang, J. Wang, E. O. Hedgeman, J. L. Browning, and Y. X. Fu. 1999. The requirement of membrane lymphotoxin for the presence of dendritic cells in lymphoid tissues. J. Exp. Med. 190:629-638.
70. Yoshida, H., H. Kawamoto, S. M. Santee, H. Hashi, K. Honda, S. Nishikawa, C. F. Ware, Y. Katsura, and S. I. Nishikawa. 2001. Expression of alpha(4)beta(7) integrin defines a distinct pathway of lymphoid progenitors committed to T cells, fetal intestinal lymphotoxin producer, NK, and dendritic cells. J. Immunol. 167:2511-2521.