Metabolic engineering of Salmonella vaccine bacteria to boost human Vγ2Vδ2 T cell immunity

Journal of Immunology

Volumn 193, Issue 2, 2014, Pages 708-721

  Workalemahu, Grefachew ^a,b   Wang, Hong ^a,b   Puan, Kia Joo ^a,c   Nada, Mohanad H ^a,b   Kuzuyama, Tomohisa ^d   Jones, Bradley D ^a   Jin, Chenggang ^a,b,e   Morita, Craig T ^a,b  

^a UNIVERSITY OF IOWA   (United States)

^b DEPARTMENT OF VETERANS AFFAIRS   (United States)

^c AGENCY FOR SCIENCE   (Singapore)

^d UNIVERSITY OF TOKYO   (Japan)

^e Pharmasan Labs Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 HYDROXY 3 METHYL BUT 2 ENYL PYROPHOSPHATE; MEVALONIC ACID; PYROPHOSPHORIC ACID DERIVATIVE; SALMONELLOSIS VACCINE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL SURVIVAL; CELL EXPANSION; CELLULAR IMMUNITY; CONTROLLED STUDY; EPITHELIUM CELL; EX VIVO STUDY; GENE DELETION; HUMAN; HUMAN CELL; LYTB GENE; METABOLIC ENGINEERING; MEVALONATE PATHWAY GENE; NONHUMAN; PLASMID; PRIORITY JOURNAL; RHESUS MONKEY; SALMONELLA TYPHIMURIUM; T LYMPHOCYTE; VACCINATION; WILD TYPE;

ANIMALS; BACTERIAL PROTEINS; CELL PROLIFERATION; CELLS, CULTURED; GENE DELETION; HUMANS; IMMUNIZATION; LYMPHOCYTE ACTIVATION; MACACA MULATTA; METABOLIC ENGINEERING; METABOLIC NETWORKS AND PATHWAYS; MEVALONIC ACID; ORGANOPHOSPHATES; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; SALMONELLA TYPHIMURIUM; SALMONELLA VACCINES; T-LYMPHOCYTES;

EID: 84904268850     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1302746     Document Type: Article

References (121)

1. Puan, K.-J., C. Jin, H. Wang, G. Sarikonda, A. M. Raker, H. K. Lee, M. I. Samuelson, E. Märker-Hermann, L. Pasa-Tolic, E. Nieves, et al. 2007. Preferential recognition of a microbial metabolite by human Vγ2Vδ2 T cells. Int. Immunol. 19: 657-673. (Pubitemid 47072209)
2. Hintz, M., A. Reichenberg, B. Altincicek, U. Bahr, R. M. Gschwind, A.-K. Kollas, E. Beck, J. Wiesner, M. Eberl, and H. Jomaa. 2001. Identification of (E)-4-hydroxy-3-methyl-but-2-enyl pyrophosphate as a major activator for human γδ T cells in Escherichia coli. FEBS Lett. 509: 317-322. (Pubitemid 34015963)
3. Tanaka, Y., C. T. Morita, Y. Tanaka, E. Nieves, M. B. Brenner, and B. R. Bloom. 1995. Natural and synthetic non-peptide antigens recognized by human γδ T cells. Nature 375: 155-158.
4. Kunzmann, V., E. Bauer, and M. Wilhelm. 1999. γ/δ T-cell stimulation by pamidronate. N. Engl. J. Med. 340: 737-738.
5. Sanders, J. M., S. Ghosh, J. M. W. Chan, G. Meints, H. Wang, A. M. Raker, Y. Song, A. Colantino, A. Burzynska, P. Kafarski, et al. 2004. Quantitative structure-activity relationships for γδ T cell activation by bisphosphonates. J. Med. Chem. 47: 375-384. (Pubitemid 38057881)
6. Bukowski, J. F., C. T. Morita, and M. B. Brenner. 1999. Human γδ T cells recognize alkylamines derived from microbes, edible plants, and tea: implications for innate immunity. Immunity 11: 57-65. (Pubitemid 29359957)
7. Gober, H.-J., M. Kistowska, L. Angman, P. Jenö, L. Mori, and G. De Libero. 2003. Human T cell receptor γδ cells recognize endogenous mevalonate metabolites in tumor cells. J. Exp. Med. 197: 163-168. (Pubitemid 36152311)
8. Thompson, K., and M. J. Rogers. 2004. Statins prevent bisphosphonate-induced γ,δ-T-cell proliferation and activation in vitro. J. Bone Miner. Res. 19: 278-288. (Pubitemid 38116742)
9. Thompson, K., J. Rojas-Navea, and M. J. Rogers. 2006. Alkylamines cause Vγ9Vδ2 T-cell activation and proliferation by inhibiting the mevalonate pathway. Blood 107: 651-654. (Pubitemid 43076390)
10. Wang, H., G. Sarikonda, K.-J. Puan, Y. Tanaka, J. Feng, J.-L. Giner, R. Cao, J. Mönkkönen, E. Oldfield, and C. T. Morita. 2011. Indirect stimulation of human Vγ2Vδ2 T cells through alterations in isoprenoid metabolism. J. Immunol. 187: 5099-5113.
11. Wang, H., O. Henry, M. D. Distefano, Y. C. Wang, J. Räikkönen, J. Mönkkönen, Y. Tanaka, and C. T. Morita. 2013. Butyrophilin 3A1 plays an essential role in prenyl pyrophosphate stimulation of human Vγ2Vδ2 T cells. J. Immunol. 191: 1029-1042.
12. Palakodeti, A., A. Sandstrom, L. Sundaresan, C. Harly, S. Nedellec, D. Olive, E. Scotet, M. Bonneville, and E. J. Adams. 2012. The molecular basis for modulation of human Vγ9Vδ2 T cell responses by CD277/butyrophilin-3 (BTN3A)-specific antibodies. J. Biol. Chem. 287: 32780-32790.
13. Harly, C., Y. Guillaume, S. Nedellec, C.-M. Peigné, H. Mönkkönen, J. Mönkkönen, J. Li, J. Kuball, E. J. Adams, S. Netzer, et al. 2012. Key implication of CD277/butyrophilin-3 (BTN3A) in cellular stress sensing by a major human γδ T-cell subset. Blood 120: 2269-2279.
14. Vavassori, S., A. Kumar, G. S. Wan, G. S. Ramanjaneyulu, M. Cavallari, S. El Daker, T. Beddoe, A. Theodossis, N. K. Williams, E. Gostick, et al. 2013. Butyrophilin 3A1 binds phosphorylated antigens and stimulates human γδ T cells. Nat. Immunol. 14: 908-916.
15. Morita, C. T., C. Jin, G. Sarikonda, and H. Wang. 2007. Nonpeptide antigens, presentation mechanisms, and immunological memory of human Vγ2Vδ2 T cells: discriminating friend from foe through the recognition of prenyl pyrophosphate antigens. Immunol. Rev. 215: 59-76. (Pubitemid 46212230)
16. Huang, D., Y. Shen, L. Qiu, C. Y. Chen, L. Shen, J. Estep, R. Hunt, D. Vasconcelos, G. Du, P. Aye, et al. 2008. Immune distribution and localization of phosphoantigen-specific Vγ2VδT cells in lymphoid and nonlymphoid tissues in Mycobacterium tuberculosis infection. Infect. Immun. 76: 426-436.
17. Ali, Z., L. Shao, L. Halliday, A. Reichenberg, M. Hintz, H. Jomaa, and Z. W. Chen. 2007. Prolonged (E)-4-hydroxy-3-methyl-but-2-enyl pyrophosphate-driven antimicrobial and cytotoxic responses of pulmonary and systemic Vγ2Vδ2 T cells in macaques. J. Immunol. 179: 8287-8296.
18. Workalemahu, G., M. Foerster, and C. Kroegel. 2004. Expression and synthesis of fibroblast growth factor-9 in human γδ T-lymphocytes. Response to isopentenyl pyrophosphate and TGF-β1/IL-15. J. Leukoc. Biol. 75: 657-663. (Pubitemid 38405657)
19. Gertner-Dardenne, J., C. Bonnafous, C. Bezombes, A.-H. Capietto, V. Scaglione, S. Ingoure, D. Cendron, E. Gross, J.-F. Lepage, A. Quillet-Mary, et al. 2009. Bromohydrin pyrophosphate enhances antibody-dependent cell-mediated cytotoxicity induced by therapeutic antibodies. Blood 113: 4875-4884.
20. Malkovska, V., F. Cigel, and B. E. Storer. 1994. Human T cells in hu-PBL-SCID mice proliferate in response to Daudi lymphoma and confer anti-tumour immunity. Clin. Exp. Immunol. 96: 158-165. (Pubitemid 24213814)
21. Kabelitz, D., D. Wesch, E. Pitters, and M. Zöller. 2004. Characterization of tumor reactivity of human Vγ9Vδ2 γδ T cells in vitro and in SCID mice in vivo. J. Immunol. 173: 6767-6776. (Pubitemid 39541063)
22. Benzaïd, I., H. Mönkkönen, V. Stresing, E. Bonnelye, J. Green, J. Mönkkönen, J. L. Touraine, and P. Clézardin. 2011. High phosphoantigen levels in bisphosphonate-treated human breast tumors promote Vγ9Vδ2 T-cell chemotaxis and cytotoxicity in vivo. Cancer Res. 71: 4562-4572.
23. D'Asaro, M., C. La Mendola, D. Di Liberto, V. Orlando, M. Todaro, M. Spina, G. Guggino, S. Meraviglia, N. Caccamo, A. Messina, et al. 2010. Vγ9Vδ2 T lymphocytes efficiently recognize and kill zoledronate-sensitized, imatinib-sensitive, and imatinib-resistant chronic myelogenous leukemia cells. J. Immunol. 184: 3260-3268.
24. Wilhelm, M., V. Kunzmann, S. Eckstein, P. Reimer, F. Weissinger, T. Ruediger, and H.-P. Tony. 2003. γδ T cells for immune therapy of patients with lymphoid malignancies. Blood 102: 200-206.
25. Dieli, F., D. Vermijlen, F. Fulfaro, N. Caccamo, S. Meraviglia, G. Cicero, A. Roberts, S. Buccheri, M. D'Asaro, N. Gebbia, et al. 2007. Targeting human γδ T cells with zoledronate and interleukin-2 for immunotherapy of hormone-refractory prostate cancer. Cancer Res. 67: 7450-7457. (Pubitemid 47206575)
26. Lang, J. M., M. R. Kaikobad, M. Wallace, M. J. Staab, D. L. Horvath, G. Wilding, G. Liu, J. C. Eickhoff, D. G. McNeel, and M. Malkovsky. 2011. Pilot trial of interleukin-2 and zoledronic acid to augment γδ T cells as treatment for patients with refractory renal cell carcinoma. Cancer Immunol. Immunother. 60: 1447-1460.
27. Bennouna, J., V. Levy, H. Sicard, H. Senellart, M. Audrain, S. Hiret, F. Rolland, H. Bruzzoni-Giovanelli, M. Rimbert, C. Galéa, et al. 2010. Phase I study of bromohydrin pyrophosphate (BrHPP, IPH 1101), a Vγ9Vδ2 T lymphocyte agonist in patients with solid tumors. Cancer Immunol. Immunother. 59: 1521-1530.
28. Sugie, T., K. Murata-Hirai, M. Iwasaki, C. T. Morita, W. Li, H. Okamura, N. Minato, M. Toi, and Y. Tanaka. 2013. Zoledronic acid-induced expansion of γδ T cells from early-stage breast cancer patients: effect of IL-18 on helper NK cells. Cancer Immunol. Immunother. 62: 677-687.
29. Shen, Y., D. Zhou, L. Qiu, X. Lai, M. Simon, L. Shen, Z. Kou, Q. Wang, L. Jiang, J. Estep, et al. 2002. Adaptive immune response of Vγ2Vδ2+ T cells during mycobacterial infections. Science 295: 2255-2258. (Pubitemid 34258837)
30. Ryan-Payseur, B., J. Frencher, L. Shen, C. Y. Chen, D. Huang, and Z. W. Chen. 2012. Multieffector-functional immune responses of HMBPP-specific Vγ2Vδ2 T cells in nonhuman primates inoculated with Listeria monocytogenes ΔactA prfA&z.ast;. J. Immunol. 189: 1285-1293.
31. Keasling, J. D. 2012. Synthetic biology and the development of tools for metabolic engineering. Metab. Eng. 14: 189-195.
32. Immethun, C. M., A. G. Hoynes-O'Connor, A. Balassy, and T. S. Moon. 2013. Microbial production of isoprenoids enabled by synthetic biology. Front. Microbiol. 4: 75.
33. Ajikumar, P. K., K. Tyo, S. Carlsen, O.Mucha, T. H. Phon, and G. Stephanopoulos. 2008. Terpenoids: opportunities for biosynthesis of natural product drugs using engineered microorganisms. Mol. Pharm. 5: 167-190. (Pubitemid 351579123)
34. Cryz, S. J., Jr., E. Fürer, and M. M. Levine. 1988. [Effectiveness of oral, attenuated live Salmonella typhi Ty 21a vaccine in controlled field trials]. Schweiz. Med. Wochenschr. 118: 467-470.
35. Wahdan, M. H., C. Sérié, Y. Cerisier, S. Sallam, and R. Germanier. 1982. A controlled field trial of live Salmonella typhi strain Ty 21a oral vaccine against typhoid: three-year results. J. Infect. Dis. 145: 292-295.
36. Anwar, E., E. Goldberg, A. Fraser, C. J. Acosta, M. Paul, and L. Leibovici. 2014. Vaccines for preventing typhoid fever. Cochrane Database Syst. Rev. 1: CD001261.
37. Majowicz, S. E., J. Musto, E. Scallan, F. J. Angulo, M. Kirk, S. J. O'Brien, T. F. Jones, A. Fazil, and R. M. Hoekstra; International Collaboration on Enteric Disease 'Burden of Illness' Studies. 2010. The global burden of nontyphoidal Salmonella gastroenteritis. Clin. Infect. Dis. 50: 882-889.
38. MacLennan, C. A., and M. M. Levine. 2013. Invasive nontyphoidal Salmonella disease in Africa: current status. Expert Rev. Anti Infect. Ther. 11: 443-446.
39. Feasey, N. A., G. Dougan, R. A. Kingsley, R. S. Heyderman, and M. A. Gordon. 2012. Invasive non-typhoidal salmonella disease: an emerging and neglected tropical disease in Africa. Lancet 379: 2489-2499.
40. Takagi, M., T. Kuzuyama, S. Takahashi, and H. Seto. 2000. A gene cluster for the mevalonate pathway from Streptomyces sp. strain CL190. J. Bacteriol. 182: 4153-4157. (Pubitemid 30463776)
41. Kaneda, K., T. Kuzuyama, M. Takagi, Y. Hayakawa, and H. Seto. 2001. An unusual isopentenyl diphosphate isomerase found in the mevalonate pathway gene cluster from Streptomyces sp. strain CL190. Proc. Natl. Acad. Sci. USA 98: 932-937. (Pubitemid 32121165)
42. Stark, M. J. R. 1987. Multicopy expression vectors carrying the lac repressor gene for regulated high-level expression of genes in Escherichia coli. Gene 51: 255-267. (Pubitemid 17061191)
43. Cohen, S. N., A. C. Chang, H. W. Boyer, and R. B. Helling. 1973. Construction of biologically functional bacterial plasmids in vitro. Proc. Natl. Acad. Sci. USA 70: 3240-3244.
44. Datsenko, K. A., and B. L. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 97: 6640-6645. (Pubitemid 30412767)
45. Puan, K.-J., H. Wang, T. Dairi, T. Kuzuyama, and C. T. Morita. 2005. fldA is an essential gene required in the 2-C-methyl-D-erythritol 4-phosphate pathway for isoprenoid biosynthesis. FEBS Lett. 579: 3802-3806. (Pubitemid 40897728)
46. Elsinghorst, E. A. 1994. Measurement of invasion by gentamicin resistance. Methods Enzymol. 236: 405-420. (Pubitemid 24283627)
47. Sarikonda, G., H. Wang, K.-J. Puan, X.-H. Liu, H. K. Lee, Y. Song, M. D. Distefano, E. Oldfield, G. D. Prestwich, and C. T. Morita. 2008. Photoaffinity antigens for human γδ T cells. J. Immunol. 181: 7738-7750.
48. Martin, V. J., D. J. Pitera, S. T. Withers, J. D. Newman, and J. D. Keasling. 2003. Engineering a mevalonate pathway in Escherichia coli for production of terpenoids. Nat. Biotechnol. 21: 796-802. (Pubitemid 36791399)
49. Kizer, L., D. J. Pitera, B. F. Pfleger, and J. D. Keasling. 2008. Application of functional genomics to pathway optimization for increased isoprenoid production. Appl. Environ. Microbiol. 74: 3229-3241. (Pubitemid 351747029)
50. Pitera, D. J., C. J. Paddon, J. D. Newman, and J. D. Keasling. 2007. Balancing a heterologous mevalonate pathway for improved isoprenoid production in Escherichia coli. Metab. Eng. 9: 193-207. (Pubitemid 46329511)
51. Jones, K. L., S. W. Kim, and J. D. Keasling. 2000. Low-copy plasmids can perform as well as or better than high-copy plasmids for metabolic engineering of bacteria. Metab. Eng. 2: 328-338. (Pubitemid 32122506)
52. Steinbacher, S., J. Kaiser, W. Eisenreich, R. Huber, A. Bacher, and F. Rohdich. 2003. Structural basis of fosmidomycin action revealed by the complex with 2-C-methyl-D-erythritol 4-phosphate synthase (IspC). Implications for the catalytic mechanism and anti-malaria drug development. J. Biol. Chem. 278: 18401-18407. (Pubitemid 36799462)
53. Morita, C. T., E. M. Beckman, J. F. Bukowski, Y. Tanaka, H. Band, B. R. Bloom, D. E. Golan, and M. B. Brenner. 1995. Direct presentation of nonpeptide prenyl pyrophosphate antigens to human γδ T cells. Immunity 3: 495-507.
54. Poquet, Y., P. Constant, F. Halary, M.-A. Peyrat, M. Gilleron, F. Davodeau, M. Bonneville, and J.-J. Fournié. 1996. A novel nucleotide-containing antigen for human blood γδ T lymphocytes. Eur. J. Immunol. 26: 2344-2349. (Pubitemid 26340933)
55. Wang, H., H. K. Lee, J. F. Bukowski, H. Li, R. A. Mariuzza, Z. W. Chen, K.-H. Nam, and C. T. Morita. 2003. Conservation of nonpeptide antigen recognition by rhesus monkey Vγ2Vδ2 T cells. J. Immunol. 170: 3696-3706. (Pubitemid 36359240)
56. Wang, H., Z. Fang, and C. T. Morita. 2010. Vγ2Vδ2 T cell receptor recognition of prenyl pyrophosphates is dependent on all CDRs. J. Immunol. 184: 6209-6222.
57. Puan, K. J., J. S. H. Low, T. W. K. Tan, J. T. S. Wee, E. H. Tan, K. W. Fong, E. T. Chua, C. Jin, J.-L. Giner, C. T. Morita, et al. 2009. Phenotypic and functional alterations of Vγ2Vδ2 T cell subsets in patients with active nasopharyngeal carcinoma. Cancer Immunol. Immunother. 58: 1095-1107.
58. Appay, V., R. A. W. van Lier, F. Sallusto, and M. Roederer. 2008. Phenotype and function of human T lymphocyte subsets: consensus and issues. Cytometry A 73: 975-983.
59. Berger, C., M. C. Jensen, P. M. Lansdorp, M. Gough, C. Elliott, and S. R. Riddell. 2008. Adoptive transfer of effector CD8+ T cells derived from central memory cells establishes persistent T cell memory in primates. J. Clin. Invest. 118: 294-305.
60. Klebanoff, C. A., L. Gattinoni, P. Torabi-Parizi, K. Kerstann, A. R. Cardones, S. E. Finkelstein, D. C. Palmer, P. A. Antony, S. T. Hwang, S. A. Rosenberg, et al. 2005. Central memory self/tumor-reactive CD8+ T cells confer superior antitumor immunity compared with effector memory T cells. Proc. Natl. Acad. Sci. USA 102: 9571-9576. (Pubitemid 40981722)
61. Klebanoff, C. A., L. Gattinoni, D. C. Palmer, P. Muranski, Y. Ji, C. S. Hinrichs, Z. A. Borman, S. P. Kerkar, C. D. Scott, S. E. Finkelstein, et al. 2011. Determinants of successful CD8+ T-cell adoptive immunotherapy for large established tumors in mice. Clin. Cancer Res. 17: 5343-5352.
62. Hara, T., Y. Mizuno, K. Takaki, H. Takada, H. Akeda, T. Aoki, M. Nagata, K. Ueda, G. Matsuzaki, Y. Yoshikai, and K. Nomoto. 1992. Predominant activation and expansion of Vγ9-bearing γδ T cells in vivo as well as in vitro in Salmonella infection. J. Clin. Invest. 90: 204-210.
63. Hoshina, T., K. Kusuhara, M. Saito, Y. Mizuno, and T. Hara. 2012. NKRP1A+ γδ and αβ T cells are preferentially induced in patients with Salmonella infection. Hum. Immunol. 73: 623-628.
64. Sicard, H., S. Ingoure, B. Luciani, C. Serraz, J.-J. Fournié, M. Bonneville, J. Tiollier, and F. Romagné. 2005. In vivo immunomanipulation of Vγ9Vδ2 T cells with a synthetic phosphoantigen in a preclinical nonhuman primate model. J. Immunol. 175: 5471-5480. (Pubitemid 41456434)
65. Laurent, G. 2009 A phase I/II open label study of IPH1101 (with low dose of IL-2) in combination with rituximab re-treatment in patients with follicular lymphoma. In European Cancer Organization/European Society for Medical Oncology Congress, September 20-24, Berlin, Germany.
66. Meraviglia, S., M. Eberl, D. Vermijlen, M. Todaro, S. Buccheri, G. Cicero, C. La Mendola, G. Guggino, M. D'Asaro, V. Orlando, et al. 2010. In vivo manipulation of Vγ9Vδ2 T cells with zoledronate and low-dose interleukin-2 for immunotherapy of advanced breast cancer patients. Clin. Exp. Immunol. 161: 290-297.
67. Jouen-Beades, F., E. Paris, C. Dieulois, J.-F. Lemeland, V. Barre-Dezelus, S. Marret, G. Humbert, J. Leroy, and F. Tron. 1997. In vivo and in vitro activation and expansion of γδ T cells during Listeria monocytogenes infection in humans. Infect. Immun. 65: 4267-4272. (Pubitemid 27422087)
68. Bertotto, A., F. Spinozzi, R. Gerli, G. Bassotti, N. Forenza, C. Vagliasindi, and R. Vaccaro. 1995. Peripheral blood γδ T cells in human listeriosis. Acta Paediatr. 84: 1434-1435. (Pubitemid 26029967)
69. Bertotto, A., R. Gerli, F. Spinozzi, C. Muscat, F. Scalise, G. Castellucci, M. Sposito, F. Candio, and R. Vaccaro. 1993. Lymphocytes bearing the γδ T cell receptor in acute Brucella melitensis infection. Eur. J. Immunol. 23: 1177-1180. (Pubitemid 23120185)
70. Poquet, Y., M. Kroca, F. Halary, S. Stenmark, M.-A. Peyrat, M. Bonneville, J. J. Fournié, and A. Sjöstedt. 1998. Expansion of Vγ9Vδ2 T cells is triggered by Francisella tularensis-derived phosphoantigens in tularemia but not after tularemia vaccination. Infect. Immun. 66: 2107-2114. (Pubitemid 28194109)
71. Cairo, C., A. M. Hebbeler, N. Propp, J. L. Bryant, V. Colizzi, and C. D. Pauza. 2007. Innate-like γδ T cell responses to mycobacterium Bacille Calmette-Guerin using the public Vγ2 repertoire in Macaca fascicularis. Tuberculosis (Edinb.) 87: 373-383. (Pubitemid 46936237)
72. Balbi, B., M. T. Valle, S. Oddera, D. Giunti, F. Manca, G. A. Rossi, and L. Allegra. 1993. T-lymphocytes with γδ+ Vδ2+ antigen receptors are present in increased proportions in a fraction of patients with tuberculosis or with sarcoidosis. Am. Rev. Respir. Dis. 148: 1685-1690. (Pubitemid 24002510)
73. Hoft, D. F., R. M. Brown, and S. T. Roodman. 1998. Bacille Calmette-Guérin vaccination enhances human γδ T cell responsiveness to mycobacteria suggestive of a memory-like phenotype. J. Immunol. 161: 1045-1054. (Pubitemid 28323573)
74. Mazzola, T. N., M. T. N. Da Silva, Y. M. F. Moreno, S. C. B. S. Lima, E. F. Carniel, A. M. Morcillo, M. A. R. G. M. Antonio, M. L. Zanolli, A. A. Netto, M. H. Blotta, et al. 2007. Robust γδ+ T cell expansion in infants immunized at birth with BCG vaccine. Vaccine 25: 6313-6320. (Pubitemid 47088760)
75. Constant, P., Y. Poquet, M.-A. Peyrat, F. Davodeau,M. Bonneville, and J.-J. Fournié. 1995. The antituberculous Mycobacterium bovis BCG vaccine is an attenuated mycobacterial producer of phosphorylated nonpeptidic antigens for human γδ T cells. Infect. Immun. 63: 4628-4633.
76. Eberl, M., B. Altincicek, A.-K. Kollas, S. Sanderbrand, U. Bahr, A. Reichenberg, E. Beck, D. Foster, J. Wiesner, M. Hintz, and H. Jomaa. 2002. Accumulation of a potent γδ T-cell stimulator after deletion of the lytB gene in Escherichia coli. Immunology 106: 200-211. (Pubitemid 34621828)
77. Wang, S., Q. Kong, and R. Curtiss, III. 2013. New technologies in developing recombinant attenuated Salmonella vaccine vectors. Microb. Pathog. 58: 17-28.
78. Kong, W., J. Clark-Curtiss, and R. Curtiss, III. 2013. Utilizing Salmonella for antigen delivery: the aims and benefits of bacterial delivered vaccination. Expert Rev. Vaccines 12: 345-347.
79. Tennant, S. M., J. Y. Wang, J. E. Galen, R. Simon, M. F. Pasetti, O. Gat, and M. M. Levine. 2011. Engineering and preclinical evaluation of attenuated nontyphoidal Salmonella strains serving as live oral vaccines and as reagent strains. Infect. Immun. 79: 4175-4185.
80. Galen, J. E., J. Y. Wang, M. Chinchilla, C. Vindurampulle, J. E. Vogel, H. Levy, W. C. Blackwelder, M. F. Pasetti, and M. M. Levine. 2010. A new generation of stable, nonantibiotic, low-copy-number plasmids improves immune responses to foreign antigens in Salmonella enterica serovar Typhi live vectors. Infect. Immun. 78: 337-347.
81. Hoiseth, S. K., and B. A. Stocker. 1981. Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 291: 238-239. (Pubitemid 11081517)
82. Hindle, Z., S. N. Chatfield, J. Phillimore, M. Bentley, J. Johnson, C. A. Cosgrove, M. Ghaem-Maghami, A. Sexton, M. Khan, F. R. Brennan, et al. 2002. Characterization of Salmonella enterica derivatives harboring defined aroC and Salmonella pathogenicity island 2 type III secretion system (ssaV) mutations by immunization of healthy volunteers. Infect. Immun. 70: 3457-3467. (Pubitemid 34665982)
83. Steger, K. K., and C. D. Pauza. 1997. Immunization of Macaca mulatta with aroA attenuated Salmonella typhimurium expressing the SIVp27 antigen. J. Med. Primatol. 26: 44-50. (Pubitemid 127515864)
84. Tacket, C. O., D. M. Hone, R. Curtiss, III, S. M. Kelly, G. Losonsky, L. Guers, A. M. Harris, R. Edelman, and M. M. Levine. 1992. Comparison of the safety and immunogenicity of ΔaroC ΔaroD and Δcya Δcrp Salmonella typhi strains in adult volunteers. Infect. Immun. 60: 536-541.
85. Cornish, R. M., J. R. Roth, and C. D. Poulter. 2006. Lethal mutations in the isoprenoid pathway of Salmonella enterica. J. Bacteriol. 188: 1444-1450. (Pubitemid 43228677)
86. Altincicek, B., A. Kollas, M. Eberl, J. Wiesner, S. Sanderbrand, M. Hintz, E. Beck, and H. Jomaa. 2001. LytB, a novel gene of the 2-C-methyl-D-erythritol 4-phosphate pathway of isoprenoid biosynthesis in Escherichia coli. FEBS Lett. 499: 37-40. (Pubitemid 32539316)
87. McAteer, S., A. Coulson, N. McLennan, and M. Masters. 2001. The lytB gene of Escherichia coli is essential and specifies a product needed for isoprenoid biosynthesis. J. Bacteriol. 183: 7403-7407. (Pubitemid 33121876)
88. Sauret-Güeto, S., E. M. Urós, E. Ibáñez, A. Boronat, and M. Rodríguez-Concepción. 2006. A mutant pyruvate dehydrogenase E1 subunit allows survival of Escherichia coli strains defective in 1-deoxy-D-xylulose 5-phosphate synthase. FEBS Lett. 580: 736-740.
89. Perez-Gil, J., E. M. Uros, S. Sauret-Güeto, L. M. Lois, J. Kirby, M. Nishimoto, E. E. Baidoo, J. D. Keasling, A. Boronat, and M. Rodriguez-Concepcion. 2012. Mutations in Escherichia coli aceE and ribB genes allow survival of strains defective in the first step of the isoprenoid biosynthesis pathway. PLoS ONE 7: e43775.
90. Sauret-Güeto, S., A. Ramos-Valdivia, E. Ibáñez, A. Boronat, and M. Rodríguez-Concepción. 2003. Identification of lethal mutations in Escherichia coli genes encoding enzymes of the methylerythritol phosphate pathway. Biochem. Biophys. Res. Commun. 307: 408-415.
91. Pérez-Gil, J., and M. Rodríguez-Concepción. 2013. Metabolic plasticity for isoprenoid biosynthesis in bacteria. Biochem. J. 452: 19-25.
92. Yoon, S.-H., S.-H. Lee, A. Das, H.-K. Ryu, H.-J. Jang, J.-Y. Kim, D.-K. Oh, J. D. Keasling, and S.-W. Kim. 2009. Combinatorial expression of bacterial whole mevalonate pathway for the production of β-carotene in E. coli. J. Biotechnol. 140: 218-226.
93. Ajikumar, P. K., W.-H. Xiao, K. E. J. Tyo, Y. Wang, F. Simeon, E. Leonard, O. Mucha, T. H. Phon, B. Pfeifer, and G. Stephanopoulos. 2010. Isoprenoid pathway optimization for Taxol precursor overproduction in Escherichia coli. Science 330: 70-74.
94. Hamano, Y., T. Dairi, M. Yamamoto, T. Kawasaki, K. Kaneda, T. Kuzuyama, N. Itoh, and H. Seto. 2001. Cloning of a gene cluster encoding enzymes responsible for the mevalonate pathway from a terpenoid-antibiotic-producing Streptomyces strain. Biosci. Biotechnol. Biochem. 65: 1627-1635. (Pubitemid 33617630)
95. Wall, D. M., C. V. Srikanth, and B. A. McCormick. 2010. Targeting tumors with Salmonella Typhimurium: potential for therapy. Oncotarget 1: 721-728.
96. Hoffman, R. M. 2012. Bugging tumors. Cancer Discov 2: 588-590.
97. Low, K. B., M. Ittensohn, T. Le, J. Platt, S. Sodi, M. Amoss, O. Ash, E. Carmichael, A. Chakraborty, J. Fischer, et al. 1999. Lipid A mutant Salmonella with suppressed virulence and TNFα induction retain tumor-targeting in vivo. Nat. Biotechnol. 17: 37-41. (Pubitemid 29037207)
98. Chorobik, P., D. Czaplicki, K. Ossysek, and J. Bereta. 2013. Salmonella and cancer: from pathogens to therapeutics. Acta Biochim. Pol. 60: 285-297.
99. Massa, P. E., A. Paniccia, A. Monegal, A. de Marco, and M. Rescigno. 2013. Salmonella engineered to express CD20-targeting antibodies and a drug-converting enzyme can eradicate human lymphomas. Blood 122: 705-714.
100. Chen, C. Y., S. Yao, D. Huang, H. Wei, H. Sicard, G. Zeng, H. Jomaa, M. H. Larsen, W. R. Jacobs, Jr., R. Wang, et al. 2013. Phosphoantigen/IL2 expansion and differentiation of Vγ2Vδ2 T cells increase resistance to tuberculosis in nonhuman primates. PLoS Pathog. 9: e1003501.
101. Dieli, F., M. Troye-Blomberg, J. Ivanyi, J. J. Fournié, A. M. Krensky, M. Bonneville, M. A. Peyrat, N. Caccamo, G. Sireci, and A. Salerno. 2001. Granulysin-dependent killing of intracellular and extracellular Mycobacterium tuberculosis by Vγ9/Vδ2 T lymphocytes. J. Infect. Dis. 184: 1082-1085. (Pubitemid 32955129)
102. Spencer, C. T., G. Abate, A. Blazevic, and D. F. Hoft. 2008. Only a subset of phosphoantigen-responsive γ9δ2 T cells mediate protective tuberculosis immunity. J. Immunol. 181: 4471-4484.
103. Spencer, C. T., G. Abate, I. G. Sakala, M. Xia, S. M. Truscott, C. S. Eickhoff, R. Linn, A. Blazevic, S. S. Metkar, G. Peng, et al. 2013. Granzyme A produced by γ9δ2 T cells induces human macrophages to inhibit growth of an intracellular pathogen. PLoS Pathog. 9: e1003119.
104. Ottones, F., J. Dornand, A. Naroeni, J. P. Liautard, and J. Favero. 2000. Vγ9Vδ2 T cells impair intracellular multiplication of Brucella suis in autologous monocytes through soluble factor release and contact-dependent cytotoxic effect. J. Immunol. 165: 7133-7139. (Pubitemid 32001189)
105. Dudal, S., C. Turriere, S. Bessoles, P. Fontes, F. Sanchez, J. Liautard, J. P. Liautard, and V. Lafont. 2006. Release of LL-37 by activated human Vγ9Vδ2 T cells: a microbicidal weapon against Brucella suis. J. Immunol. 177: 5533-5539. (Pubitemid 44527627)
106. Oliaro, J., S. Dudal, J. Liautard, J. B. Andrault, J. P. Liautard, and V. Lafont. 2005. Vγ9Vδ2 T cells use a combination of mechanisms to limit the spread of the pathogenic bacteria Brucella. J. Leukoc. Biol. 77: 652-660. (Pubitemid 40628745)
107. Marischen, L., D. Wesch, J. M. Schröder, O. Wiedow, and D. Kabelitz. 2009. Human γδ T cells produce the protease inhibitor and antimicrobial peptide elafin. Scand. J. Immunol. 70: 547-552.
108. Chen, Z. W. 2013. Multifunctional immune responses of HMBPP-specific Vγ2Vδ2 T cells in M. tuberculosis and other infections. Cell. Mol. Immunol. 10: 58-64.
109. Chen, Z. W. 2011. Immune biology of Ag-specific γδ T cells in infections. Cell. Mol. Life Sci. 68: 2409-2417.
110. Morita, C. T., C. M. Parker, M. B. Brenner, and H. Band. 1994. TCR usage and functional capabilities of human γδ T cells at birth. J. Immunol. 153: 3979-3988. (Pubitemid 24322565)
111. Parker, C. M., V. Groh, H. Band, S. A. Porcelli, C. Morita, M. Fabbi, D. Glass, J. L. Strominger, and M. B. Brenner. 1990. Evidence for extrathymic changes in the T cell receptor γ/δ repertoire. J. Exp. Med. 171: 1597-1612. (Pubitemid 20167553)
112. Cairo, C., B. Sagnia, G. Cappelli, V. Colizzi, R. G. Leke, R. J. Leke, and C. D. Pauza. 2013. Human cord blood γδ T cells expressing public Vγ2 chains dominate the response to bisphosphonate plus interleukin-15. Immunology 138: 346-360.
113. Davodeau, F., M. A. Peyrat, M. M. Hallet, I. Houde, H. Vie, and M. Bonneville. 1993. Peripheral selection of antigen receptor junctional features in a major human γδ subset. Eur. J. Immunol. 23: 804-808. (Pubitemid 23101061)
114. Groh, V., S. Porcelli, M. Fabbi, L. L. Lanier, L. J. Picker, T. Anderson, R. A. Warnke, A. K. Bhan, J. L. Strominger, and M. B. Brenner. 1989. Human lymphocytes bearing T cell receptor γ/δ are phenotypically diverse and evenly distributed throughout the lymphoid system. J. Exp. Med. 169: 1277-1294. (Pubitemid 19104962)
115. Kinjo, Y., D. Wu, G. Kim, G. W. Xing, M. A. Poles, D. D. Ho, M. Tsuji, K. Kawahara, C. H. Wong, and M. Kronenberg. 2005. Recognition of bacterial glycosphingolipids by natural killer T cells. Nature 434: 520-525. (Pubitemid 40477061)
116. Kinjo, Y., E. Tupin, D. Wu, M. Fujio, R. Garcia-Navarro, M. R. Benhnia, D. M. Zajonc, G. Ben-Menachem, G. D. Ainge, G. F. Painter, et al. 2006. Natural killer T cells recognize diacylglycerol antigens from pathogenic bacteria. Nat. Immunol. 7: 978-986. (Pubitemid 44263912)
117. Kjer-Nielsen, L., O. Patel, A. J. Corbett, J. Le Nours, B. Meehan, L. Liu, M. Bhati, Z. Chen, L. Kostenko, R. Reantragoon, et al. 2012. MR1 presents microbial vitamin B metabolites to MAIT cells. Nature 491: 717-723.
118. Corbett, A. J., S. B. G. Eckle, R. W. Birkinshaw, L. Liu, O. Patel, J. Mahony, Z. Chen, R. Reantragoon, B. Meehan, H. Cao, et al. 2014. T-cell activation by transitory neo-antigens derived from distinct microbial pathways. Nature 10.1038/nature.13160.
119. López-Sagaseta, J., C. L. Dulberger, J. E. Crooks, C. D. Parks, A. M. Luoma, A. McFedries, I. Van Rhijn, A. Saghatelian, and E. J. Adams. 2013. The molecular basis for mucosal-associated invariant T cell recognition of MR1 proteins. Proc. Natl. Acad. Sci. USA 110: E1771-E1778.
120. Patel, O., L. Kjer-Nielsen, J. Le Nours, S. B. G. Eckle, R. Birkinshaw, T. Beddoe, A. J. Corbett, L. Liu, J. J. Miles, B. Meehan, et al. 2013. Recognition of vitamin B metabolites by mucosal-associated invariant T cells. Nat. Commun. 4: 2142.
121. Yi, W., X. Liu, Y. Li, J. Li, C. Xia, G. Zhou, W. Zhang, W. Zhao, X. Chen, and P. G. Wang. 2009. Remodeling bacterial polysaccharides by metabolic pathway engineering. Proc. Natl. Acad. Sci. USA 106: 4207-4212.