Advancement of Engineered Bacteria for Orally Delivered Therapeutics
Peilin Guo
State Key Laboratory of Biochemical Engineering, Institute of Process Engineering, Chinese Academy of Sciences, Beijing, 100190 P. R. China
School of Chemical Engineering, University of Chinese Academy of Sciences, Beijing, 100049 P. R. China
Search for more papers by this authorShuang Wang
State Key Laboratory of Biochemical Engineering, Institute of Process Engineering, Chinese Academy of Sciences, Beijing, 100190 P. R. China
Search for more papers by this authorHua Yue
State Key Laboratory of Biochemical Engineering, Institute of Process Engineering, Chinese Academy of Sciences, Beijing, 100190 P. R. China
School of Chemical Engineering, University of Chinese Academy of Sciences, Beijing, 100049 P. R. China
Search for more papers by this authorXiao Zhang
State Key Laboratory of Biochemical Engineering, Institute of Process Engineering, Chinese Academy of Sciences, Beijing, 100190 P. R. China
Search for more papers by this authorGuanghui Ma
State Key Laboratory of Biochemical Engineering, Institute of Process Engineering, Chinese Academy of Sciences, Beijing, 100190 P. R. China
School of Chemical Engineering, University of Chinese Academy of Sciences, Beijing, 100049 P. R. China
Search for more papers by this authorCorresponding Author
Xin Li
State Key Laboratory of Biochemical Engineering, Institute of Process Engineering, Chinese Academy of Sciences, Beijing, 100190 P. R. China
E-mail: [email protected]; [email protected]
Search for more papers by this authorCorresponding Author
Wei Wei
State Key Laboratory of Biochemical Engineering, Institute of Process Engineering, Chinese Academy of Sciences, Beijing, 100190 P. R. China
School of Chemical Engineering, University of Chinese Academy of Sciences, Beijing, 100049 P. R. China
E-mail: [email protected]; [email protected]
Search for more papers by this authorPeilin Guo
State Key Laboratory of Biochemical Engineering, Institute of Process Engineering, Chinese Academy of Sciences, Beijing, 100190 P. R. China
School of Chemical Engineering, University of Chinese Academy of Sciences, Beijing, 100049 P. R. China
Search for more papers by this authorShuang Wang
State Key Laboratory of Biochemical Engineering, Institute of Process Engineering, Chinese Academy of Sciences, Beijing, 100190 P. R. China
Search for more papers by this authorHua Yue
State Key Laboratory of Biochemical Engineering, Institute of Process Engineering, Chinese Academy of Sciences, Beijing, 100190 P. R. China
School of Chemical Engineering, University of Chinese Academy of Sciences, Beijing, 100049 P. R. China
Search for more papers by this authorXiao Zhang
State Key Laboratory of Biochemical Engineering, Institute of Process Engineering, Chinese Academy of Sciences, Beijing, 100190 P. R. China
Search for more papers by this authorGuanghui Ma
State Key Laboratory of Biochemical Engineering, Institute of Process Engineering, Chinese Academy of Sciences, Beijing, 100190 P. R. China
School of Chemical Engineering, University of Chinese Academy of Sciences, Beijing, 100049 P. R. China
Search for more papers by this authorCorresponding Author
Xin Li
State Key Laboratory of Biochemical Engineering, Institute of Process Engineering, Chinese Academy of Sciences, Beijing, 100190 P. R. China
E-mail: [email protected]; [email protected]
Search for more papers by this authorCorresponding Author
Wei Wei
State Key Laboratory of Biochemical Engineering, Institute of Process Engineering, Chinese Academy of Sciences, Beijing, 100190 P. R. China
School of Chemical Engineering, University of Chinese Academy of Sciences, Beijing, 100049 P. R. China
E-mail: [email protected]; [email protected]
Search for more papers by this authorAbstract
The use of bacteria and their biotic components as therapeutics has shown great potential in the treatment of diseases. Orally delivered bacteria improve patient compliance compared with injection-administered bacteria and are considered the preferred mode. However, due to the harsh gastrointestinal environment, the viability and therapeutic efficacy of orally delivered bacteria are significantly reduced in vivo. In recent years, with the rapid development of synthetic biology and nanotechnology, bacteria and biotic components have been engineered to achieve directed genetic reprogramming for construction and precise spatiotemporal control in the gastrointestinal tract, which can improve viability and therapeutic efficiency. Herein, a state-of-the-art review on the current progress of engineered bacterial systems for oral delivery is provided. The different types of bacterial and biotic components for oral administration are first summarized. The engineering strategies of these bacteria and biotic components and their treatment of diseases are next systematically summarized. Finally, the current challenges and prospects of these bacterial therapeutics are highlighted that will contribute to the development of next-generation orally delivered bacteriotherapy.
Conflict of Interest
The authors declare no conflict of interest.
References
- 1a) K. Hou, Z. X. Wu, X. Y. Chen, J. Q. Wang, D. Zhang, C. Xiao, D. Zhu, J. B. Koya, L. Wei, J. Li, Z. S. Chen, Signal Transduction Targeted Ther. 2022, 7, 135; b) L. Yang, L. Y. Hung, Y. Zhu, S. Ding, K. G. Margolis, K. W. Leong, Research 2022, 2022, 9804014.
- 2M. R. Charbonneau, V. M. Isabella, N. Li, C. B. Kurtz, Nat. Commun. 2020, 11, 1738.
- 3a) Y. He, L. Fu, Y. Li, W. Wang, M. Gong, J. Zhang, X. Dong, J. Huang, Q. Wang, C. R. Mackay, Y. X. Fu, Y. Chen, X. Guo, Cell Metab. 2021, 33, 988; b) C. Campbell, P. T. McKenney, D. Konstantinovsky, O. I. Isaeva, M. Schizas, J. Verter, C. Mai, W. B. Jin, C. J. Guo, S. Violante, R. J. Ramos, J. R. Cross, K. Kadaveru, J. Hambor, A. Y. Rudensky, Nature 2020, 581, 475; c) Q. Zhang, Q. Zhao, T. Li, L. Lu, F. Wang, H. Zhang, Z. Liu, H. Ma, Q. Zhu, J. Wang, X. Zhang, Y. Pei, Q. Liu, Y. Xu, J. Qie, X. Luan, Z. Hu, X. Liu, Cell Metab. 2023, 35, 943; d) M. J. Bender, A. C. McPherson, C. M. Phelps, S. P. Pandey, C. R. Laughlin, J. H. Shapira, L. M. Sanchez, M. Rana, T. G. Richie, T. S. Mims, A. M. Gocher-Demske, L. Cervantes-Barragan, S. J. Mullett, S. L. Gelhaus, T. C. Bruno, N. Cannon, J. A. McCulloch, D. A. A. Vignali, R. Hinterleitner, A. V. Joglekar, J. F. Pierre, S. T. M. Lee, D. Davar, H. M. Zarour, M. Meisel, Cell 2023, 186, 1846.
- 4a) Y. Litvak, M. X. Byndloss, A. J. Bäumler, Science 2018, 362; b) H. Kayama, R. Okumura, K. Takeda, Annu. Rev. Immunol. 2020, 38, 23.
- 5D. Chen, D. Jin, S. Huang, J. Wu, M. Xu, T. Liu, W. Dong, X. Liu, S. Wang, W. Zhong, Y. Liu, R. Jiang, M. Piao, B. Wang, H. Cao, Cancer Lett 2020, 469, 456.
- 6X. Huang, J. Pan, F. Xu, B. Shao, Y. Wang, X. Guo, S. Zhou, Adv. Sci. 2021, 8, 2003572.
- 7G. P. Donaldson, M. S. Ladinsky, K. B. Yu, J. G. Sanders, B. B. Yoo, W. C. Chou, M. E. Conner, A. M. Earl, R. Knight, P. J. Bjorkman, S. K. Mazmanian, Science 2018, 360, 795.
- 8S. Zhou, C. Gravekamp, D. Bermudes, K. Liu, Nat. Rev. Cancer 2018, 18, 727.
- 9C. Yang, M. Cui, Y. Zhang, H. Pan, J. Liu, S. Wang, N. Ma, J. Chang, T. Sun, H. Wang, Commun. Biol. 2020, 3, 561.
- 10G. Vighi, F. Marcucci, L. Sensi, G. Di Cara, F. Frati, Clin. Exp. Immunol. 2008, 153, 3.
- 11G. Gabutti, A. Rossanese, A. Tomasi, S. Giuffrida, V. Nicosia, J. Barriga, C. Florescu, F. Sandri, A. Stefanati, Vaccines 2020, 8, 606.
- 12Y. Yue, J. Xu, Y. Li, K. Cheng, Q. Feng, X. Ma, N. Ma, T. Zhang, X. Wang, X. Zhao, G. Nie, Nat. Biomed. Eng. 2022, 6, 898.
- 13R. Orel, T. K. Trop, World J. Gastroenterol. 2014, 20, 11505.
- 14M. Gurung, Z. Li, H. You, R. Rodrigues, D. B. Jump, A. Morgun, N. Shulzhenko, EBioMedicine 2020, 51, 102590.
- 15N. Kobyliak, C. Conte, G. Cammarota, A. P. Haley, I. Styriak, L. Gaspar, J. Fusek, L. Rodrigo, P. Kruzliak, Nutr. Metab. 2016, 13, 14.
10.1186/s12986-016-0067-0 Google Scholar
- 16L. Zaharuddin, N. M. Mokhtar, K. N. Muhammad Nawawi, R. A. R. Ali, BMC Gastroenterol. 2019, 19, 131.
- 17a) M. Vitiello, M. Evangelista, N. Di Lascio, C. Kusmic, A. Massa, F. Orso, S. Sarti, A. Marranci, K. Rodzik, L. Germelli, D. Chandra, A. Salvetti, A. Pucci, D. Taverna, F. Faita, C. Gravekamp, L. Poliseno, Oncogene 2019, 38, 3756; b) N. S. Forbes, Nat. Rev. Cancer 2010, 10, 785.
- 18L. Xiong, S. Wang, J. W. Dean, K. N. Oliff, C. Jobin, R. Curtiss 3rd, L. Zhou, Nat. Microbiol. 2022, 7, 1087.
- 19G. Losurdo, A. Iannone, A. Contaldo, E. Ierardi, A. Di Leo, M. Principi, J. Gastrointestin. Liver Dis. 2015, 24, 499.
- 20R. Maltby, M. P. Leatham-Jensen, T. Gibson, P. S. Cohen, T. Conway, PLoS One 2013, 8, e53957.
- 21C. Z. Wang, R. A. Kazmierczak, A. Eisenstark, Int. J. Microbiol. 2016, 2016, 5678702.
- 22G. Chen, D. P. Wei, L. J. Jia, B. Tang, L. Shu, K. Zhang, Y. Xu, J. Gao, X. F. Huang, W. H. Jiang, Q. G. Hu, Y. Huang, Q. Wu, Z. H. Sun, J. F. Zhang, Z. C. Hua, Cancer Sci. 2009, 100, 2437.
- 23S. N. Jiang, S. H. Park, H. J. Lee, J. H. Zheng, H. S. Kim, H. S. Bom, Y. Hong, M. Szardenings, M. G. Shin, S. C. Kim, V. Ntziachristos, H. E. Choy, J. J. Min, Mol. Ther. 2013, 21, 1985.
- 24F. Friedlos, P. Lehouritis, L. Ogilvie, D. Hedley, L. Davies, D. Bermudes, I. King, J. Martin, R. Marais, C. J. Springer, Clin. Cancer Res. 2008, 14, 4259.
- 25B. S. Sorenson, K. L. Banton, N. L. Frykman, A. S. Leonard, D. A. Saltzman, Clin. Orthop. Relat. Res. 2008, 466, 1285.
- 26S. K. Kim, R. B. Guevarra, Y. T. Kim, J. Kwon, H. Kim, J. H. Cho, H. B. Kim, J. H. Lee, J. Microbiol. Biotechnol. 2019, 29, 1335.
- 27a) S. Parvez, K. A. Malik, S. Ah Kang, H. Y. Kim, J. Appl. Microbiol. 2006, 100, 1171; b) R. G. Kerry, J. K. Patra, S. Gouda, Y. Park, H. S. Shin, G. Das, J. Food Drug Anal. 2018, 26, 927.
- 28a) M. de Vrese, J. Schrezenmeir 2002, 88, S59; b) W. Habermann, K. Zimmermann, H. Skarabis, R. Kunze, V. Rusch, Arzneimittelforschung 2002, 52, 622; c) J. M. Hamilton-Miller, Int. J. Antimicrob. Agents 2003, 22, 360.
- 29K. Akutko, A. Stawarski, J. Clin. Med. 2021, 10, 5931.
- 30K. Matsuoka, Immunol. Med. 2021, 44, 30.
- 31M. L. Vidakovics, J. Jendholm, M. Mörgelin, A. Månsson, C. Larsson, L. O. Cardell, K. Riesbeck, PLoS Pathog. 2010, 6, e1000724.
- 32J. Lee, Y. J. Yoon, J. H. Kim, N. T. H. Dinh, G. Go, S. Tae, K. S. Park, H. T. Park, C. Lee, T. Y. Roh, D. Di Vizio, Y. S. Gho, Front. Microbiol. 2018, 9, 2268.
- 33N. J. Bitto, R. Chapman, S. Pidot, A. Costin, C. Lo, J. Choi, T. D'Cruze, E. C. Reynolds, S. G. Dashper, L. Turnbull, C. B. Whitchurch, T. P. Stinear, K. J. Stacey, R. L. Ferrero, Sci. Rep. 2017, 7, 7072.
- 34Y. Pastor, A. Camacho, A. G. Gil, R. Ramos, A. L. Ceráin, I. Peñuelas, J. M. Irache, C. Gamazo, J. Med. Microbiol. 2017, 66, 946.
- 35J. Nevermann, A. Silva, C. Otero, D. P. Oyarzún, B. Barrera, F. Gil, I. L. Calderón, J. A. Fuentes, Front. Microbiol. 2019, 10, 104.
- 36a) M. Kaparakis-Liaskos, R. L. Ferrero, Nat. Rev. Immunol. 2015, 15, 375; b) R. Stentz, A. L. Carvalho, E. J. Jones, S. R. Carding, Biochem. Soc. Trans. 2018, 46, 1021.
- 37X. Z. Liu, Z. J. Wen, Y. M. Li, W. R. Sun, X. Q. Hu, J. Z. Zhu, X. Y. Li, P. Y. Wang, J. L. Pedraz, J. H. Lee, H. W. Kim, M. Ramalingam, S. Xie, R. Wang, ACS Appl. Mater. Interfaces 2023, 15, 3744.
- 38J. A. Molina-Tijeras, J. Gálvez, M. E. Rodríguez-Cabezas, Nutrients 2019, 11, 1038.
- 39J. Hu, J. Zuo, Z. Chen, L. Fu, X. Lv, S. Hu, X. Shi, Y. Jing, Y. Wang, Z. Wang, R. Mi, Y. Huang, D. Liu, K. Qi, X. Han, Vet. Microbiol. 2019, 229, 48.
- 40W. Zhu, Y. Zhang, X. Liu, Microbiol. Res. 2015, 176, 7.
- 41H. Chen, H. Ji, X. Kong, P. Lei, Q. Yang, W. Wu, L. Jin, D. Sun, Pharmaceutics 2021, 13, 1892.
- 42J. Chen, N. Li, F. She, Vaccine 2014, 32, 6054.
- 43S. Gong, N. Nan, Y. Sun, Z. He, J. Li, F. Chen, T. Li, N. Ning, J. Wang, Z. Li, D. Luo, H. Wang, Vaccines 2020, 8, 61.
- 44M. P. Szostak, H. Mader, M. Truppe, M. Kamal, F. O. Eko, V. Huter, J. Marchart, W. Jechlinger, W. Haidinger, E. Brand, E. Denner, S. Resch, E. Dehlin, A. Katinger, B. Kuen, A. Haslberger, A. Hensel, W. Lubitz, Behring Inst. Mitt. 1997, Feb(98), 191.
- 45M. Holay, Z. Guo, J. Pihl, J. Heo, J. H. Park, R. H. Fang, L. Zhang, ACS Appl. Bio Mater. 2021, 4, 3830.
- 46N. P. Minton, Nat. Rev. Microbiol. 2003, 1, 237.
- 47P. Lin, H. Yuan, J. Du, K. Liu, H. Liu, T. Wang, Appl. Microbiol. Biotechnol. 2020, 104, 2319.
- 48L. Yan, H. Da, S. Zhang, V. M. López, W. Wang, Microbiol Res 2017, 203, 19.
- 49R. Uebe, D. Schüler, Nat. Rev. Microbiol. 2016, 14, 621.
- 50G. Vargas, J. Cypriano, T. Correa, P. Leão, D. A. Bazylinski, F. Abreu, Molecules 2018, 23, 2438.
- 51T. Briolay, T. Petithomme, M. Fouet, N. Nguyen-Pham, C. Blanquart, N. Boisgerault, Mol. Cancer 2021, 20, 55.
- 52T. J. Beveridge, L. L. Graham, Microbiol. Rev. 1991, 55, 684.
- 53J. M. S. de Barros, T. Scherer, D. Charalampopoulos, V. V. Khutoryanskiy, A. D. Edwards, J. Pharm. Sci. 2014, 103, 2022.
- 54P. Feng, Z. Cao, X. Wang, J. Li, J. Liu, Adv. Mater. 2020, 32, 2002406.
- 55Q. W. Chen, Q. R. Li, M. W. Cao, J. H. Yan, X. Z. Zhang, Adv. Sci. 2022, 9, 2200986.
- 56S. Xie, L. Zhao, X. Song, M. Tang, C. Mo, X. Li, J. Controlled Release 2017, 268, 390.
- 57S. Taherkhani, M. Mohammadi, J. Daoud, S. Martel, M. Tabrizian, ACS Nano 2014, 8, 5049.
- 58J. Liu, Y. Wang, W. J. Heelan, Y. Chen, Z. Li, Q. Hu, Sci. Adv. 2022, 8, eabp8798.
- 59J. X. Fan, M. Y. Peng, H. Wang, H. R. Zheng, Z. L. Liu, C. X. Li, X. N. Wang, X. H. Liu, S. X. Cheng, X. Z. Zhang, Adv. Mater. 2019, 31, 1808278.
- 60X. Hu, X. Zhao, B. He, Z. Zhao, Z. Zheng, P. Zhang, X. Shi, R. T. K. Kwok, J. W. Y. Lam, A. Qin, B. Z. Tang, Research 2018, 2018, 3152870.
- 61E. M. Sletten, C. R. Bertozzi, Angew. Chem., Int. Ed. Engl. 2009, 48, 6974.
- 62P. Pan, J. X. Fan, X. N. Wang, J. W. Wang, D. W. Zheng, H. Cheng, X. Z. Zhang, Adv. Sci. 2019, 6, 1902500.
- 63W. Wang, Q. Yang, Y. Du, X. Zhou, X. Du, Q. Wu, L. Lin, Y. Song, F. Li, C. Yang, W. Tan, Angew. Chem., Int. Ed. Engl. 2020, 59, 2628.
- 64Z. Geng, X. Wang, F. Wu, Z. Cao, J. Liu, Sci. Adv. 2023, 9, eade0997.
- 65S. Qing, C. Lyu, L. Zhu, C. Pan, S. Wang, F. Li, J. Wang, H. Yue, X. Gao, R. Jia, W. Wei, G. Ma, Adv. Mater. 2020, 32, 2002085.
- 66a) M. M. Farley, B. Hu, W. Margolin, J. Liu, J. Bacteriol. 2016, 198, 1186; b) P. Lubitz, U. B. Mayr, W. Lubitz, Adv. Exp. Med. Biol. 2009, 655, 159.
- 67V. Gujrati, J. Prakash, J. Malekzadeh-Najafabadi, A. Stiel, U. Klemm, G. Mettenleiter, M. Aichler, A. Walch, V. Ntziachristos, Nat. Commun. 2019, 10, 1114.
- 68S. Paukner, G. Kohl, W. Lubitz, J. Controlled Release 2004, 94, 63.
- 69P. Kudela, S. Paukner, U. B. Mayr, D. Cholujova, G. Kohl, Z. Schwarczova, J. Bizik, J. Sedlak, W. Lubitz, Cancer Lett. 2008, 262, 54.
- 70J. A. MacDiarmid, N. B. Mugridge, J. C. Weiss, L. Phillips, A. L. Burn, R. P. Paulin, J. E. Haasdyk, K. A. Dickson, V. N. Brahmbhatt, S. T. Pattison, A. C. James, G. Al Bakri, R. C. Straw, B. Stillman, R. M. Graham, H. Brahmbhatt, Cancer Cell 2007, 11, 431.
- 71G. Reid, M. E. Pel, M. B. Kirschner, Y. Y. Cheng, N. Mugridge, J. Weiss, M. Williams, C. Wright, J. J. Edelman, M. P. Vallely, B. C. McCaughan, S. Klebe, H. Brahmbhatt, J. A. MacDiarmid, N. van Zandwijk, Ann. Oncol. 2013, 24, 3128.
- 72J. Liu, W. Li, Y. Wang, Y. Ding, A. Lee, Q. Hu, Nano Today 2021, 41, 101291.
- 73Z. Cao, S. Cheng, X. Wang, Y. Pang, J. Liu, Nat. Commun. 2019, 10, 3452.
- 74S. Lin, S. Mukherjee, J. Li, W. Hou, C. Pan, J. Liu, Sci. Adv. 2021, 7, eabf0677.
- 75R. Liu, Z. Cao, L. Wang, X. Wang, S. Lin, F. Wu, Y. Pang, J. Liu, Nano Today 2022, 45, 101537.
- 76a) W. Quispe-Tintaya, D. Chandra, A. Jahangir, M. Harris, A. Casadevall, E. Dadachova, C. Gravekamp, Proc. Natl. Acad. Sci. U. S. A. 2013, 110, 8668; b) R. Fernandes, M. Zuniga, F. R. Sassine, M. Karakoy, D. H. Gracias, Small 2011, 7, 588.
- 77a) D. Akin, J. Sturgis, K. Ragheb, D. Sherman, K. Burkholder, J. P. Robinson, A. K. Bhunia, S. Mohammed, R. Bashir, Nat. Nanotechnol. 2007, 2, 441; b) Y. Alapan, O. Yasa, O. Schauer, J. Giltinan, A. F. Tabak, V. Sourjik, M. Sitti, Sci. Rob. 2018, 3, eaar4423; c) K. Ektate, M. C. Munteanu, H. Ashar, J. Malayer, A. Ranjan, Sci. Rep. 2018, 8, 13062.
- 78A. M. Vargason, S. Santhosh, A. C. Anselmo, Small 2020, 16, 2001705.
- 79J. H. Kim, C. S. Lee, B. G. Kim, Biochem. Biophys. Res. Commun. 2005, 331, 210.
- 80M. O. Din, T. Danino, A. Prindle, M. Skalak, J. Selimkhanov, K. Allen, E. Julio, E. Atolia, L. S. Tsimring, S. N. Bhatia, J. Hasty, Nature 2016, 536, 81.
- 81S. Chowdhury, S. Castro, C. Coker, T. E. Hinchliffe, N. Arpaia, T. Danino, Nat. Med. 2019, 25, 1057.
- 82M. Zhao, M. Yang, X. M. Li, P. Jiang, E. Baranov, S. Li, M. Xu, S. Penman, R. M. Hoffman, Proc. Natl. Acad. Sci. U. S. A. 2005, 102, 755.
- 83a) V. Gujrati, S. Kim, S. H. Kim, J. J. Min, H. E. Choy, S. C. Kim, S. Jon, ACS Nano 2014, 8, 1525; b) C. Pinero-Lambea, G. Bodelon, R. Fernandez-Perianez, A. M. Cuesta, L. Alvarez-Vallina, L. A. Fernandez, ACS Synth. Biol. 2015, 4, 463.
- 84C. L. Ho, H. Q. Tan, K. J. Chua, A. Kang, K. H. Lim, K. L. Ling, W. S. Yew, Y. S. Lee, J. P. Thiery, M. W. Chang, Nat. Biomed. Eng. 2018, 2, 27.
- 85a) Y. F. Bueso, P. Lehouritis, M. Tangney, J. Controlled Release 2018, 275, 217; b) Z. Hosseinidoust, B. Mostaghaci, O. Yasa, B. W. Park, A. V. Singh, M. Sitti, Adv. Drug Deliv. Rev. 2016, 106, 27.
- 86a) S. Leschner, I. V. Deyneko, S. Lienenklaus, K. Wolf, H. Bloecker, D. Bumann, H. Loessner, S. Weiss, Nucleic Acids Res. 2012, 40, 2984; b) J. C. Anderson, E. J. Clarke, A. P. Arkin, C. A. Voigt, J. Mol. Biol. 2006, 355, 619.
- 87Y. Chen, M. Du, Z. Yuan, Z. Chen, F. Yan, Nat. Commun. 2022, 13, 4468.
- 88a) X. Jin, I. H. Riedel-Kruse, Proc. Natl. Acad. Sci. U. S. A. 2018, 115, 3698; b) R. Ohlendorf, R. R. Vidavski, A. Eldar, K. Moffat, A. Moglich, J. Mol. Biol. 2012, 416, 534.
- 89M. Cui, T. Sun, S. Li, H. Pan, J. Liu, X. Zhang, L. Li, S. Li, C. Wei, C. Yu, C. Yang, N. Ma, B. Ma, S. Lu, J. Chang, W. Zhang, H. Wang, Cell Rep. 2021, 36, 109690.
- 90H. Suzuki, Y. Saito, T. Hibi, Gut Liver 2009, 3, 81.
- 91K. Schütze, E. Hentschel, B. Dragosics, A. M. Hirschl, Gut 1995, 36, 831.
- 92E. Mohit, S. Rafati, Mol. Immunol. 2013, 56, 599.
- 93Y. Talebkhan, M. Bababeik, M. Esmaeili, A. Oghalaei, S. Saberi, Z. Karimi, N. Afkhami, M. Mohammadi, J. Microbiol. Methods 2010, 82, 334.
- 94a) D. van der Lelie, A. Oka, S. Taghavi, J. Umeno, T. J. Fan, K. E. Merrell, S. D. Watson, L. Ouellette, B. Liu, M. Awoniyi, Y. Lai, L. Chi, K. Lu, C. S. Henry, R. B. Sartor, Nat. Commun. 2021, 12, 3105; b) L. Xu, B. Liu, L. Huang, Z. Li, Y. Cheng, Y. Tian, G. Pan, H. Li, Y. Xu, W. Wu, Z. Cui, L. Xie, Microbiol Spectr 2022, 10, e0065722; c) C. Zhou, Y. Wang, C. Li, Z. Xie, L. Dai, Microbiol. Spectr. 2023, 11, e0333022; d) K. Atarashi, T. Tanoue, K. Oshima, W. Suda, Y. Nagano, H. Nishikawa, S. Fukuda, T. Saito, S. Narushima, K. Hase, S. Kim, J. V. Fritz, P. Wilmes, S. Ueha, K. Matsushima, H. Ohno, B. Olle, S. Sakaguchi, T. Taniguchi, H. Morita, M. Hattori, K. Honda, Nature 2013, 500, 232.
- 95L. Steidler, W. Hans, L. Schotte, S. Neirynck, F. Obermeier, W. Falk, W. Fiers, E. Remaut, Science 2000, 289, 1352.
- 96M. L. Hanson, J. A. Hixon, W. Li, B. K. Felber, M. R. Anver, C. A. Stewart, B. M. Janelsins, S. K. Datta, W. Shen, M. H. McLean, S. K. Durum, Gastroenterology 2014, 146, 210.
- 97J. Zhou, M. Li, Q. Chen, X. Li, L. Chen, Z. Dong, W. Zhu, Y. Yang, Z. Liu, Q. Chen, Nat. Commun. 2022, 13, 3432.
- 98J. Xu, J. Xu, T. Shi, Y. Zhang, F. Chen, C. Yang, X. Guo, G. Liu, D. Shao, K. W. Leong, G. Nie, Adv. Mater. 2023, 35, 2207890.
- 99K. Vandenbroucke, W. Hans, J. Van Huysse, S. Neirynck, P. Demetter, E. Remaut, P. Rottiers, L. Steidler, Gastroenterology 2004, 127, 502.
- 100J. P. Motta, L. G. Bermúdez-Humarán, C. Deraison, L. Martin, C. Rolland, P. Rousset, J. Boue, G. Dietrich, K. Chapman, P. Kharrat, J. P. Vinel, L. Alric, E. Mas, J. M. Sallenave, P. Langella, N. Vergnolle, Sci. Transl. Med. 2012, 4, 158ra144.
- 101Z. Z. Hamady, Ann. R. Coll. Surg. Engl. 2013, 95, 235.
- 102K. Vandenbroucke, H. de Haard, E. Beirnaert, T. Dreier, M. Lauwereys, L. Huyck, J. Van Huysse, P. Demetter, L. Steidler, E. Remaut, C. Cuvelier, P. Rottiers, Mucosal Immunol. 2010, 3, 49.
- 103N. M. Breyner, C. Michon, C. S. de Sousa, P. B. Vilas Boas, F. Chain, V. A. Azevedo, P. Langella, J. M. Chatel, Front. Microbiol. 2017, 8, 114.
- 104B. Foligne, R. Dessein, M. Marceau, S. Poiret, M. Chamaillard, B. Pot, M. Simonet, C. Daniel, Gastroenterology 2007, 133, 862.
- 105S. Shigemori, T. Watanabe, K. Kudoh, M. Ihara, S. Nigar, Y. Yamamoto, Y. Suda, T. Sato, H. Kitazawa, T. Shimosato, Microb. Cell Fact. 2015, 14, 189.
- 106S. del Carmen, R. M. Rosique, T. Saraiva, M. Zurita-Turk, A. Miyoshi, V. Azevedo, A. de Moreno de LeBlanc, P. Langella, L. G. Bermúdez-Humarán, J. G. LeBlanc, J Clin Gastroenterol 2014, 48, S12.
- 107I. M. Carroll, J. M. Andrus, J. M. Bruno-Bárcena, T. R. Klaenhammer, H. M. Hassan, D. S. Threadgill, Am. J. Physiol. Gastrointest. Liver Physiol. 2007, 293, G729.
- 108Y. Xie, Q. Guo, S. Li, M. Liu, Q. Zhang, Z. Xu, H. Sun, J. Microbiol. Biotechnol. 2017, 27.
- 109P. Wei, Y. Yang, Q. Ding, X. Li, H. Sun, Z. Liu, J. Huang, Y. Gong, J. Med. Microbiol. 2016, 65, 160.
- 110E. Spisni, M. C. Valerii, L. De Fazio, E. Cavazza, F. Borsetti, A. Sgromo, M. Candela, M. Centanni, F. Rizello, A. Strillacci, Mol. Ther. 2015, 23, 278.
- 111P. Praveschotinunt, A. M. Duraj-Thatte, I. Gelfat, F. Bahl, D. B. Chou, N. S. Joshi, Nat. Commun. 2019, 10, 5580.
- 112X. Yan, X. Y. Liu, D. Zhang, Y. D. Zhang, Z. H. Li, X. Liu, F. Wu, G. Q. Chen, Cell Mol. Immunol. 2021, 18, 2344.
- 113Y. Chung, Y. Ryu, B. C. An, Y. S. Yoon, O. Choi, T. Y. Kim, J. Yoon, J. Y. Ahn, H. J. Park, S. K. Kwon, J. F. Kim, M. J. Chung, Microbiome 2021, 9, 122.
- 114D. W. Zheng, R. Q. Li, J. X. An, T. Q. Xie, Z. Y. Han, R. Xu, Y. Fang, X. Z. Zhang, Adv. Mater. 2020, 32, 2004529.
- 115T. M. Savage, R. L. Vincent, S. S. Rae, L. H. Huang, A. Ahn, K. Pu, F. Li, K. de Los Santos-Alexis, C. Coker, T. Danino, N. Arpaia, Sci. Adv. 2023, 9, eadc9436.
- 116T. Tanoue, S. Morita, D. R. Plichta, A. N. Skelly, W. Suda, Y. Sugiura, S. Narushima, H. Vlamakis, I. Motoo, K. Sugita, A. Shiota, K. Takeshita, K. Yasuma-Mitobe, D. Riethmacher, T. Kaisho, J. M. Norman, D. Mucida, M. Suematsu, T. Yaguchi, V. Bucci, T. Inoue, Y. Kawakami, B. Olle, B. Roberts, M. Hattori, R. J. Xavier, K. Atarashi, K. Honda, Nature 2019, 565, 600.
- 117N. Saeidi, C. K. Wong, T. M. Lo, H. X. Nguyen, H. Ling, S. S. Leong, C. L. Poh, M. W. Chang, Mol. Syst. Biol. 2011, 7, 521.
- 118E. Koh, I. Y. Hwang, H. L. Lee, R. De Sotto, J. W. J. Lee, Y. S. Lee, J. C. March, M. W. Chang, Nat. Commun. 2022, 13, 3834.
- 119E. van Nood, A. Vrieze, M. Nieuwdorp, S. Fuentes, E. G. Zoetendal, W. M. de Vos, C. E. Visser, E. J. Kuijper, J. F. Bartelsman, J. G. Tijssen, P. Speelman, M. G. Dijkgraaf, J. J. Keller, N. Engl. J. Med. 2013, 368, 407.
- 120K. Cai, W. Tu, Y. Liu, T. Li, H. Wang, Sci. Rep. 2015, 5, 17479.
- 121D. W. Zheng, P. Pan, K. W. Chen, J. X. Fan, C. X. Li, H. Cheng, X. Z. Zhang, Nat. Biomed. Eng. 2020, 4, 853.
- 122T. Takiishi, H. Korf, T. L. Van Belle, S. Robert, F. A. Grieco, S. Caluwaerts, L. Galleri, I. Spagnuolo, L. Steidler, K. Van Huynegem, P. Demetter, C. Wasserfall, M. A. Atkinson, F. Dotta, P. Rottiers, C. Gysemans, C. Mathieu, J. Clin. Invest. 2012, 122, 1717.
- 123Z. Chen, L. Guo, Y. Zhang, R. L. Walzem, J. S. Pendergast, R. L. Printz, L. C. Morris, E. Matafonova, X. Stien, L. Kang, D. Coulon, O. P. McGuinness, K. D. Niswender, S. S. Davies, J. Clin. Invest. 2014, 124, 3391.
- 124K. J. Adolfsen, I. Callihan, C. E. Monahan, P. J. Greisen, J. Spoonamore, M. Momin, L. E. Fitch, M. J. Castillo, L. Weng, L. Renaud, C. J. Weile, J. H. Konieczka, T. Mirabella, A. Abin-Fuentes, A. G. Lawrence, V. M. Isabella, Nat. Commun. 2021, 12, 6215.
- 125C. B. Kurtz, Y. A. Millet, M. K. Puurunen, M. Perreault, M. R. Charbonneau, V. M. Isabella, J. W. Kotula, E. Antipov, Y. Dagon, W. S. Denney, D. A. Wagner, K. A. West, A. J. Degar, A. M. Brennan, P. F. Miller, Sci. Transl. Med. 2019, 11, eaau7975.
- 126F. P. Canale, C. Basso, G. Antonini, M. Perotti, N. Li, A. Sokolovska, J. Neumann, M. J. James, S. Geiger, W. Jin, J. P. Theurillat, K. A. West, D. S. Leventhal, J. M. Lora, F. Sallusto, R. Geiger, Nature 2021, 598, 662.
- 127S. Moradi-Kalbolandi, A. K. Majidzadeh, M. H. Abdolvahab, N. Jalili, L. Farahmand, Probiotics Antimicrob. Proteins 2021, 13, 1239.
- 128a) W. T. Yang, G. L. Yang, X. Yang, S. M. Shonyela, L. Zhao, Y. L. Jiang, H. B. Huang, C. W. Shi, J. Z. Wang, G. Wang, J. H. Zhao, C. F. Wang, Appl. Microbiol. Biotechnol. 2017, 101, 8475; b) D. T. Ho, T. Hatabu, Y. Sunada, Y. Kondo, Biosci. Microbiota Food Health 2020, 39, 117.
- 129M. Wang, T. Fu, J. Hao, L. Li, M. Tian, N. Jin, L. Ren, C. Li, Int. J. Biol. Macromol. 2020, 160, 736.
- 130R. Keikha, S. M. Hashemi-Shahri, A. Jebali, Sci. Rep. 2021, 11, 21308.
- 131a) J. E. Clark-Curtiss, R. Curtiss 3rd, J. Immunol. 2018, 200, 39; b) N. Chin'ombe, Viruses 2013, 5, 2062.
- 132a) V. Jawalagatti, P. Kirthika, C. Hewawaduge, J. Y. Park, M. S. Yang, B. Oh, M. Y. So, B. Kim, J. H. Lee, Front. Immunol. 2022, 13, 811802; b) V. Jawalagatti, P. Kirthika, J. Y. Park, C. Hewawaduge, J. H. Lee, J. Adv. Res. 2022, 36, 211.
- 133V. Jawalagatti, P. Kirthika, C. Hewawaduge, M. S. Yang, J. Y. Park, B. Oh, J. H. Lee, Mol. Ther. 2022, 30, 1926.
- 134J. C. Sung, Y. Liu, K. C. Wu, M. C. Choi, C. H. Ma, J. Lin, E. I. C. He, D. Y. Leung, E. T. Sze, Y. K. Hamied, D. M. Lam, K. W. Kwong, Vaccines 2022, 10, 1852.
10.3390/vaccines10111852 Google Scholar
- 135https://clinicaltrials.gov/ct2/show/study/NCT05057923.
- 136a) S. Wang, Q. Kong, R. Curtiss 3rd, Microb. Pathog. 2013, 58, 17; b) S. M. Tennant, M. M. Levine, Vaccine 2015, 33, C36.
- 137H. Su, Q. Liu, X. Bian, S. Wang, R. Curtiss 3rd, Q. Kong, Proc. Natl. Acad. Sci. U. S. A. 2021, 118, e2013350118.
- 138H. Su, Q. Liu, S. Wang, R. Curtiss 3rd, Q. Kong, Theranostics 2019, 9, 3565.
- 139N. Pan, B. Liu, X. Bao, H. Zhang, S. Sheng, Y. Liang, H. Pan, X. Wang, Vaccines 2021, 9, 984.
- 140G. Szabo, Gastroenterology 2015, 148, 30.
- 141M. Llopis, A. M. Cassard, L. Wrzosek, L. Boschat, A. Bruneau, G. Ferrere, V. Puchois, J. C. Martin, P. Lepage, T. L. Roy, L. Lefèvre, B. Langelier, F. Cailleux, A. M. González-Castro, S. Rabot, F. Gaudin, H. Agostini, S. Prévot, D. Berrebi, D. Ciocan, C. Jousse, S. Naveau, P. Gérard, G. Perlemuter, Gut 2016, 65, 830.
- 142T. Hendrikx, Y. Duan, Y. Wang, J. H. Oh, L. M. Alexander, W. Huang, P. Stärkel, S. B. Ho, B. Gao, O. Fiehn, P. Emond, H. Sokol, J. P. van Pijkeren, B. Schnabl, Gut 2019, 68, 1504.
- 143H. Pan, T. Sun, M. Cui, N. Ma, C. Yang, J. Liu, G. Pang, B. Liu, L. Li, X. Zhang, W. Zhang, J. Chang, H. Wang, ACS Nano 2022, 16, 6049.
- 144Y. Yu, S. Lin, Z. Chen, B. Qin, Z. He, M. Cheng, M. Sun, J. Sun, Nano Today 2023, 48, 101731.
- 145M. J. Liao, M. O. Din, L. Tsimring, J. Hasty, Science 2019, 365, 1045.
- 146a) V. M. Isabella, B. N. Ha, M. J. Castillo, D. J. Lubkowicz, S. E. Rowe, Y. A. Millet, C. L. Anderson, N. Li, A. B. Fisher, K. A. West, P. J. Reeder, M. M. Momin, C. G. Bergeron, S. E. Guilmain, P. F. Miller, C. B. Kurtz, D. Falb, Nat. Biotechnol. 2018, 36, 857; b) D. B. Pedrolli, N. V. Ribeiro, P. N. Squizato, V. N. de Jesus, D. A. Cozetto, Team AQA Unesp at iGEM 2017, Trends Biotechnol. 2019, 37, 100.