3D-printed engineered bacteria-laden gelatin/sodium alginate composite hydrogels for biological detection of ionizing radiation

Ziyuan Chen1, Jintao Shen1, Meng Wei1, Wenrui Yan1, Qiucheng Yan1, Zhangyu Li1, Yaqiong Chen1, Feng Zhang1, Lina Du1, Bochuan Yuan1, Yiguang Jin1
1Department of Pharmaceutical Sciences, Beijing Institute of Radiation Medicine, Beijing, China

Tóm tắt

Nuclear safety is a global growing concern, where ionizing radiation (IR) is a major injury factor resulting in serious damage to organisms. The detection of IR is usually conducted with physical dosimeters; however, biological IR detection methods are deficient. Here, a living composite hydrogel consisting of engineered bacteria and gelatin/sodium alginate was 3D-printed for the biological detection of IR. Three strains of PrecA::egfp gene circuit-containing engineered Escherichia coli were constructed with IR-dependent fluorescence, and the DH5α strain was finally selected due to its highest radiation response and fluorescence. Engineered bacteria were loaded in a series of gelatin/sodium alginate matrix hydrogels with different rheology, 3D printability and bacterial applicability. A high-gelatin-content hydrogel containing 10% gelatin/1.25% sodium alginate was optimal. The optimal living composite hydrogel was 3D-printed with the special bioink, which reported significant green fluorescence under γ-ray radiation. The living composite hydrogel provides a biological strategy for the detection of environmental ionizing radiation.

Từ khóa


Tài liệu tham khảo

Hirose K (2020) Atmospheric effects of Fukushima nuclear accident: a review from a sight of atmospheric monitoring. J Environ Radioact 218:106240. https://doi.org/10.1016/j.jenvrad.2020.106240 Brumfiel G, Fuyuno I (2012) Japan’s nuclear crisis: Fukushima’s legacy of fear. Nature 483:138–140. https://doi.org/10.1038/483138a Gorobets A (2016) Chernobyl anniversary: Ukraine should cut back nuclear power. Nature 534:37. https://doi.org/10.1038/534037e Valentin J (2003) A framework for assessing the impact of ionising radiation on non-human species. Ann ICRP 33(3):207–266. https://doi.org/10.1016/S0146-6453(03)000 Pentreath RJ (1999) A system for radiological protection of the environment: some initial thoughts and ideas. J Radiol Prot 19:117–128. https://doi.org/10.1088/0952-4746/19/2/302 International Atomic Energy Agency (2002) Ethical considerations in protecting the environment from the effects of ionizing radiation: a report for discussion. IAEA, Vienna Oughton DH (2016) Ethical foundations of environmental radiological protection. Ann ICRP 45(1 Suppl):345–357. https://doi.org/10.1177/0146645316639836 International Commission on Radiological Protection (2007) The 2007 recommendations of the international commission on radiological protection. Ann ICRP, Oxford International Atomic Energy Agency (2014) Radiation protection and safety of radiation sources: international basic safety standards. IAEA, Vienna Martinez AR, Heil JR, Charles TC (2019) An engineered GFP fluorescent bacterial biosensor for detecting and quantifying silver and copper ions. Biometals 32:265–272. https://doi.org/10.1007/s10534-019-00179-3 Roy R, Ray S, Chowdhury A et al (2021) Tunable multiplexed whole-cell biosensors as environmental diagnostics for ppb-level detection of aromatic pollutants. ACS Sens 6:1933–1939. https://doi.org/10.1021/acssensors.1c00329 Xue H, Shi H, Yu Z et al (2014) Design, construction, and characterization of a set of biosensors for aromatic compounds. ACS Synth Biol 3:1011–1014. https://doi.org/10.1021/sb500023f Bereza-Malcolm LT, Mann G, Franks AE (2015) Environmental sensing of heavy metals through whole cell microbial biosensors: a synthetic biology approach. ACS Synth Biol 4:535–546. https://doi.org/10.1021/sb500286r Jia X, Zhao T, Liu Y et al (2018) Gene circuit engineering to improve the performance of a whole-cell lead biosensor. FEMS Microbiol Lett 365:fny157. https://doi.org/10.1093/femsle/fny157 Mendoza JI, Soncini FC, Checa SK (2020) Engineering of a Au-sensor to develop a Hg-specific, sensitive and robust whole-cell biosensor for on-site water monitoring. Chem Commun 56:6590–6593. https://doi.org/10.1039/d0cc01323d Wu Y, Wang C, Wang D et al (2021) A whole-cell biosensor for point-of-care detection of waterborne bacterial pathogens. ACS Synth Biol 10:333–344. https://doi.org/10.1021/acssynbio.0c00491 Struss A, Pasini P, Ensor CM et al (2010) Paper strip whole cell biosensors: a portable test for the semiquantitative detection of bacterial quorum signaling molecules. Anal Chem 82:4457–4463. https://doi.org/10.1021/ac100231a Vollmer AC, Belkin S, Smulski DR et al (1997) Detection of DNA damage by use of Escherichia coli carrying recA’::lux, uvrA’::lux, or alkA’::lux reporter plasmids. Appl Environ Microbiol 63:2566–2577. https://doi.org/10.1128/aem.63.7.2566-2571.1997 Gao G, Fan L, Lu H et al (2008) Engineering Deinococcus radiodurans into biosensor to monitor radioactivity and genotoxicity in environment. Sci Bull 53:1675–1681. https://doi.org/10.1007/s11434-008-0224-6 Gao Y, Wu K, Suo Z (2019) Photodetachable adhesion. Adv Mater 31:e1806948. https://doi.org/10.1002/adma.201806948 Porter GC, Schwass DR, Tompkins GR et al (2021) AgNP/Alginate nanocomposite hydrogel for antimicrobial and antibiofilm applications. Carbohydr Polym 251:117017. https://doi.org/10.1016/j.carbpol.2020.117017 Yuk H, Varela CE, Nabzdyk CS et al (2019) Dry double-sided tape for adhesion of wet tissues and devices. Nature 575:169–174. https://doi.org/10.1038/s41586-019-1710-5 Noor N, Shapira A, Edri R et al (2019) 3D printing of personalized thick and perfusable cardiac patches and hearts. Adv Sci 6:1900344. https://doi.org/10.1002/advs.201900344 Jang J, Lee J, Seol YJ et al (2013) Improving mechanical properties of alginate hydrogel by reinforcement with ethanol treated polycaprolactone nanofibers. Compos B Eng 45:1216–1221. https://doi.org/10.1016/j.compositesb.2012.09.059 Barakat A, Kamoun EA, El-Moslamy SH et al (2022) Photo-curable carboxymethylcellulose composite hydrogel as a promising biomaterial for biomedical applications. Int J Biol Macromol 207:1011–1021. https://doi.org/10.1016/j.ijbiomac.2022.03.201 Ye W, Li H, Yu K et al (2020) 3D printing of gelatin methacrylate-based nerve guidance conduits with multiple channels. Mater Des 192:108757. https://doi.org/10.1016/j.matdes.2020.108757 Liu J, Qu M, Wang C et al (2022) A dual-cross-linked hydrogel patch for promoting diabetic wound healing. Small 18:e2106172. https://doi.org/10.1002/smll.202106172 Tsai CH, Hoang LN, Lin CC et al (2022) Evaluation of topical and subconjunctival injection of hyaluronic acid-coated nanoparticles for drug delivery to posterior eye. Pharmaceutics 14:1253–1269. https://doi.org/10.3390/pharmaceutics14061253 Yue K, Trujillo-de Santiago G, Alvarez MM et al (2015) Synthesis, properties, and biomedical applications of gelatin methacryloyl (GelMA) hydrogels. Biomaterials 73:254–271. https://doi.org/10.1016/j.biomaterials.2015.08.045 Chen S, Jang TS, Pan HM et al (2020) 3D freeform printing of nanocomposite hydrogels through in situ precipitation in reactive viscous fluid. Int J Bioprint 6:258–278. https://doi.org/10.18063/ijb.v6i2.258 Rastogi P, Kandasubramanian B (2019) Review of alginate-based hydrogel bioprinting for application in tissue engineering. Biofabrication 11:042001. https://doi.org/10.1088/1758-5090/ab331e Stubbe B, Mignon A, Declercq H et al (2019) Development of gelatin-alginate hydrogels for burn wound treatment. Macromol Biosci 19:e1900123. https://doi.org/10.1002/mabi.201900123 Ye W, Xie C, Liu Y et al (2021) 3D printed high-resolution scaffold with hydrogel microfibers for providing excellent biocompatibility. J Biomater Appl 35:633–642. https://doi.org/10.1177/0885328220962606 Dubbin K, Dong Z, Park DM et al (2021) Projection microstereolithographic microbial bioprinting for engineered biofilms. Nano Lett 21:1352–1359. https://doi.org/10.1021/acs.nanolett.0c04100 Cai Y, Chang SY, Gan SW et al (2022) Nanocomposite bioinks for 3D bioprinting. Acta Biomater 151:45–69. https://doi.org/10.1016/j.actbio.2022.08.014 Kim SY, Han G, Hwang DB et al (2021) Design and usability evaluations of a 3D-printed implantable drug delivery device for acute liver failure in preclinical settings. Adv Healthc Mater 10:e2100497. https://doi.org/10.1002/adhm.202100497 Jang TS, Park SJ, Lee JE et al (2022) Topography-supported nanoarchitectonics of hybrid scaffold for systematically modulated bone regeneration and remodeling. Adv Funct Mater 32(51):2206863. https://doi.org/10.1002/adfm.202206863 Muskan, Gupta D, Negi NP (2022) 3D bioprinting: printing the future and recent advances. Bioprinting 27:e00211. https://doi.org/10.1016/j.bprint.2022.e00211 Yang X, Li S, Ren Y et al (2022) 3D printed hydrogel for articular cartilage regeneration. Compos B Eng 237:109863. https://doi.org/10.1016/j.compositesb.2022.109863 Han WT, Jang T, Chen S et al (2019) Improved cell viability for large-scale biofabrication with photo-crosslinkable hydrogel systems through a dual-photoinitiator approach. Biomater Sci 8:450–461. https://doi.org/10.1039/c9bm01347d Kyle S (2018) 3D printing of bacteria: the next frontier in biofabrication. Trends Biotechnol 36:340–341. https://doi.org/10.1016/j.tibtech.2018.01.010 Freyman MC, Kou T, Wang S et al (2020) 3D printing of living bacteria electrode. Nano Res 13:1318–1323. https://doi.org/10.1007/s12274-019-2534-1 Shen J, Liu J, Yu S et al (2021) Diaminodiacid bridge improves enzymatic and in vivo inhibitory activity of peptide CPI-1 against botulinum toxin serotype A. Chin Chem Lett 32:4049–4052. https://doi.org/10.1016/j.cclet.2021.03.055 Ning W, Shang P, Wu J et al (2018) Novel amphiphilic, biodegradable, biocompatible, thermo-responsive ABA triblock copolymers based on PCL and PEG analogues via a combination of ROP and RAFT: synthesis, characterization, and sustained drug release from self-assembled micelles. Polymers 10:214–231. https://doi.org/10.3390/polym10020214 Blanchard L, de Groot A (2021) Coexistence of SOS-dependent and SOS-independent regulation of DNA repair genes in radiation-resistant Deinococcus bacteria. Cells 10:924–936. https://doi.org/10.3390/cells10040924 Prada Medina CA, Aristizabal Tessmer ET, Quintero Ruiz N et al (2016) Survival and SOS response induction in ultraviolet B irradiated Escherichia coli cells with defective repair mechanisms. Int J Radiat Biol 92:321–328. https://doi.org/10.3109/09553002.2016.1152412 Maslowska KH, Makiela-Dzbenska K, Fijalkowska IJ (2019) The SOS system: a complex and tightly regulated response to DNA damage. Environ Mol Mutagen 60:368–384. https://doi.org/10.1002/em.22267 Lippincott-Schwartz J, Snapp E, Kenworthy A (2001) Studying protein dynamics in living cells. Nat Rev Mol Cell Biol 2:444–456. https://doi.org/10.1038/35073068 Schaffner M, Rühs P, Coulter F et al (2017) 3D printing of bacteria into functional complex materials. Sci Adv 3:6804. https://doi.org/10.1126/sciadv.aao6804 Song K, Compaan AM, Chai W et al (2020) Injectable gelatin microgel-based composite ink for 3D bioprinting in air. ACS Appl Mater Interfaces 12:22453–22466. https://doi.org/10.1021/acsami.0c01497 Asohan AW, Hashim R, Ku Ishak KM et al (2022) Preparation and characterisation of cellulose nanocrystal/alginate/polyethylene glycol diacrylate (CNC/Alg/PEGDA) hydrogel using double network crosslinking technique for bioprinting application. Appl Sci 12:771–786. https://doi.org/10.3390/app12020771 He Y, Yang F, Zhao H et al (2016) Research on the printability of hydrogels in 3D bioprinting. Sci Rep 6:29977. https://doi.org/10.1038/srep29977