Plasma membrane-anchored fluorescent tracker based on boron-dipyrromethene

doi:10.1016/j.cjche.2024.06.002

Abstract

Abstract: The construction of a stable-membrane tracker has significant implications for the visualization of the membrane in live cells. However, most current plasma trackers are not suitable for tracking plasma membranes for a long time due to their limited retention time. Herein, Mem580-F-Sulfo is designed to target and anchor cell membranes and therefore track cell membranes for a longer time. This tracker is composed of a lipophilic boron-dipyrromethene (BODIPY) derivative and a hydrophilic zwitterion to form an amphiphilic structure, which enables its targeting ability toward cell membranes. Moreover, a reactive ester group is included to bind with proteins through covalent bonds in cell membranes non-specifically, which extends retention time in cell membranes. Mem580-F-Sulfo shows intense brightness (94600), with a high molar absorption coefficient of up to about 100000 L·mol^-1·cm^-1 and a fluorescence quantum yield of up to 0.97. It shows fast cell membrane targeting ability and long retention up to 90 min. In brief, this work has not only developed a tracker with good cell membrane targetability but also provided a new strategy for improving the targeting stability of cell membranes.

Key words: Plasma membrane, Protein, Tracker, Imaging, Microstructure

摘要： The construction of a stable-membrane tracker has significant implications for the visualization of the membrane in live cells. However, most current plasma trackers are not suitable for tracking plasma membranes for a long time due to their limited retention time. Herein, Mem580-F-Sulfo is designed to target and anchor cell membranes and therefore track cell membranes for a longer time. This tracker is composed of a lipophilic boron-dipyrromethene (BODIPY) derivative and a hydrophilic zwitterion to form an amphiphilic structure, which enables its targeting ability toward cell membranes. Moreover, a reactive ester group is included to bind with proteins through covalent bonds in cell membranes non-specifically, which extends retention time in cell membranes. Mem580-F-Sulfo shows intense brightness (94600), with a high molar absorption coefficient of up to about 100000 L·mol^-1·cm^-1 and a fluorescence quantum yield of up to 0.97. It shows fast cell membrane targeting ability and long retention up to 90 min. In brief, this work has not only developed a tracker with good cell membrane targetability but also provided a new strategy for improving the targeting stability of cell membranes.

关键词: Plasma membrane, Protein, Tracker, Imaging, Microstructure

Yucong Gong, Xiangli Li, Daqing Ma, Lai Wang, Lin Zhou, Caiwei Lu, Yi Xiao, Xinfu Zhang. Plasma membrane-anchored fluorescent tracker based on boron-dipyrromethene[J]. Chinese Journal of Chemical Engineering, 2024, 72(8): 220-225.

Yucong Gong, Xiangli Li, Daqing Ma, Lai Wang, Lin Zhou, Caiwei Lu, Yi Xiao, Xinfu Zhang. Plasma membrane-anchored fluorescent tracker based on boron-dipyrromethene[J]. 中国化学工程学报, 2024, 72(8): 220-225.

References

[1] G. Enkavi, M. Javanainen, W. Kulig, T. Rog, I. Vattulainen, Multiscale simulations of biological membranes: the challenge to understand biological phenomena in a living substance, Chem. Rev. 119 (9) (2019) 5607-5774.
[2] M. Riggi, K. Niewola-Staszkowska, N. Chiaruttini, A. Colom, B. Kusmider, V. Mercier, S. Soleimanpour, M. Stahl, S. Matile, A. Roux, R. Loewith, Decrease in plasma membrane tension triggers PtdIns(4, 5)P₂ phase separation to inactivate TORC2, Nat. Cell Biol. 20 (9) (2018) 1043-1051.
[3] C. Jin, J.X. He, J.M. Zou, W.J. Xuan, T. Fu, R.W. Wang, W.H. Tan, Phosphorylated lipid-conjugated oligonucleotide selectively anchors on cell membranes with high alkaline phosphatase expression, Nat. Commun. 10 (1) (2019) 2704.
[4] V.V. Shynkar, A.S. Klymchenko, C. Kunzelmann, G. Duportail, C.D. Muller, A.P. Demchenko, J.M. Freyssinet, Y. Mely, Fluorescent biomembrane probe for ratiometric detection of apoptosis, J. Am. Chem. Soc. 129 (7) (2007) 2187-2193.
[5] S. Xu, W.J. Pan, Z.L. Song, L. Yuan, Molecular engineering of near-infrared fluorescent probes for cell membrane imaging, Molecules 28 (4) (2023) 1906.
[6] J. Mu, F. Liu, M.S. Rajab, M. Shi, S. Li, C. Goh, L. Lu, Q.H. Xu, B. Liu, L.G. Ng, B. Xing, A small-molecule FRET reporter for the real-time visualization of cell-surface proteolytic enzyme functions, Angew Chem. Int. Ed. Engl. 53 (52) (2014) 14357-14362.
[7] M.M. Ali, D.K. Kang, K. Tsang, M. Fu, J.M. Karp, W. Zhao, Cell-surface sensors: lighting the cellular environment, Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 4 (5) (2012) 547-561.
[8] X.L. Li, M.T. Fan, Z.H. Wang, D.X. Li, S.Y. Wu, X.Y. Cui, Y. Xiao, X.F. Zhang, BODIPY-based NIR trackers with acidity-driven amphiphilicity for STED super-resolution imaging of lysosomal membranes, Anal. Chem. (2024) 2958-2967.
[9] Z.Y. Shang, X.Y. Yang, Q.T. Meng, S.Y. Tian, Z.Q. Zhang, A ratiometric near-infrared fluorescent probe for the detection and monitoring of hypochlorous acid in rheumatoid arthritis model and real water samples, Smart Mol. 1 (2) (2023) e20220007.
[10] M. Schaferling, The art of fluorescence imaging with chemical sensors, Angew Chem. Int. Ed. Engl. 51 (15) (2012) 3532-3554.
[11] K. Li, T.B. Ren, S.Y. Huan, L. Yuan, X.B. Zhang, Progress and perspective of solid-state organic fluorophores for biomedical applications, J. Am. Chem. Soc. 143 (50) (2021) 21143-21160.
[12] Y.F. Huang, Y.B. Zhang, F.J. Huo, Y. Wen, C.X. Yin, Design strategy and bioimaging of small organic molecule multicolor fluorescent probes, Sci. China Chem. 63 (12) (2020) 1742-1755.
[13] W. Xu, Z.B. Zeng, J.H. Jiang, Y.T. Chang, L. Yuan, Discerning the chemistry in individual organelles with small-molecule fluorescent probes, Angew Chem. Int. Ed. Engl. 55 (44) (2016) 13658-13699.
[14] X.F. Zhang, C. Wang, L.J. Jin, Z. Han, Y. Xiao, Photostable bipolar fluorescent probe for video tracking plasma membranes related cellular processes, ACS Appl. Mater. Interfaces 6 (15) (2014) 12372-12379.
[15] D.I. Danylchuk, S. Moon, K. Xu, A.S. Klymchenko, Switchable solvatochromic probes for live-cell super-resolution imaging of plasma membrane organization, Angew Chem. Int. Ed. Engl. 58 (42) (2019) 14920-14924.
[16] K.N. Wang, G.B. Qi, H.Y. Chu, X.J. Chao, L.Y. Liu, G.H. Li, Q. Cao, Z.W. Mao, B. Liu, Probing cell membrane damage using a molecular rotor probe with membrane-to-nucleus translocation, Mater. Horiz. 7 (12) (2020) 3226-3233.
[17] Y.N. Wang, B. Xu, L.H. Qiu, Y.J. Xu, R. Sun, J.F. Ge, A series of novel cell membrane fluorescent probes based on oxazolopyridine unit, Dyes Pigments. 185 (2021) 108883.
[18] Q.H. Li, J.X. Hong, S.M. Feng, S.Y. Gong, G.Q. Feng, Polarity-sensitive cell membrane probe reveals lower polarity of tumor cell membrane and its application for tumor diagnosis, Anal. Chem. 94 (31) (2022) 11089-11095.
[19] Y.H. Li, Y.Q. Wu, J. Chang, M. Chen, R. Liu, F.Y. Li, A bioprobe based on aggregation induced emission (AIE) for cell membrane tracking, Chem. Commun. 49 (96) (2013) 11335-11337.
[20] I.O. Aparin, R. Yan, R. Pelletier, A.A. Choi, D.I. Danylchuk, K. Xu, A.S. Klymchenko, Fluorogenic dimers as bright switchable probes for enhanced super-resolution imaging of cell membranes, J. Am. Chem. Soc. 144 (39) (2022) 18043-18053.
[21] L. Shi, K. Li, Y.H. Liu, X. Liu, Q. Zhou, Q. Xu, S.Y. Chen, X.Q. Yu, Bio-inspired assembly in a phospholipid bilayer: effective regulation of electrostatic and hydrophobic interactions for plasma membrane specific probes, Chem. Commun. 56 (25) (2020) 3661-3664.
[22] L. Shi, Y.H. Liu, K. Li, A. Sharma, K.K. Yu, M.S. Ji, L.L. Li, Q. Zhou, H. Zhang, J.S. Kim, X.Q. Yu, An AIE-based probe for rapid and ultrasensitive imaging of plasma membranes in biosystems, Angew Chem. Int. Ed. Engl. 59 (25) (2020) 9962-9966.
[23] Q.H. Li, W.L. Zhu, S.Y. Gong, S.Y. Jiang, G.Q. Feng, Selective visualization of tumor cell membranes and tumors with a viscosity-sensitive plasma membrane probe, Anal. Chem. 95 (18) (2023) 7254-7261.
[24] W.L. Zhu, Q.H. Li, S.Y. Gong, G.Q. Feng, Cell membrane targetable NIR fluorescent polarity probe for selective visualization of cancer cells and early tumor, Anal. Chim. Acta 1278 (2023) 341748.
[25] S.M. Feng, Z.P. Zheng, S.Y. Gong, G.Q. Feng, A unique probe enables labeling cell membrane and Golgi apparatus and tracking peroxynitrite in Golgi oxidative stress and drug-induced liver injury, Sensor. Actuator. B Chem. 361 (2022) 131751.
[26] S.M. Feng, Y.J. Liu, Q.H. Li, Z.S. Gui, G.Q. Feng, Two water-soluble and wash-free fluorogenic probes for specific lighting up cancer cell membranes and tumors, Anal. Chem. 94 (3) (2022) 1601-1607.
[27] D.K. Zhang, V. Martin, I. Garcia-Moreno, A. Costela, M.E. Perez-Ojeda, Y. Xiao, Development of excellent long-wavelength BODIPY laser dyes with a strategy that combines extending π-conjugation and tuning ICT effect, Phys. Chem. Chem. Phys. 13 (28) (2011) 13026-13033.
[28] X.F. Zhang, Y. Xiao, J. Qi, J.L. Qu, B. Kim, X.L. Yue, K.D. Belfield, Long-wavelength, photostable, two-photon excitable BODIPY fluorophores readily modifiable for molecular probes, J. Org. Chem. 78 (18) (2013) 9153-9160.
[29] H. Wang, W.W. Zhao, X.Y. Liu, S. Wang, Y.L. Wang, BODIPY-based fluorescent surfactant for cell membrane imaging and photodynamic therapy, ACS Appl. Bio Mater. 3 (1) (2020) 593-601.
[30] A. Polita, M. Stancikaite, R. Zvirblis, K. Maleckaite, J. Dodonova-Vaitkuniene, S. Tumkevicius, A.P. Shivabalan, G. Valincius, Designing a green-emitting viscosity-sensitive 4, 4-difluoro-4-bora-3a, 4a-diaza- s-indacene (BODIPY) probe for plasma membrane viscosity imaging, RSC Adv. 13 (28) (2023) 19257-19264.
[31] S. Serrano-Buitrago, M. Munoz-Ubeda, V.G. Almendro-Vedia, J. Sanchez-Camacho, B.L. Maroto, F. Moreno, J. Banuelos, I. Garcia-Moreno, I. Lopez-Montero, S. de la Moya, Polar ammoniostyryls easily converting a clickable lipophilic BODIPY in an advanced plasma membrane probe, J. Mater. Chem. B 11 (10) (2023) 2108-2114.
[32] S.H. Huang, B.C. Huang, L. Chao, Development of cell membrane electrophoresis to measure the diffusivity of a native transmembrane protein, Anal. Chem. 94 (10) (2022) 4531-4537.
[33] M. Kaur, A. Janaagal, N. Balsukuri, I. Gupta, Evolution of Aza-BODIPY dyes-a hot topic, Coord. Chem. Rev. 498 (2024) 215428.
[34] Y.J. Reo, S. Sarkar, M. Dai, Y.J. Yang, K.H. Ahn, Structurally compact, blue-green-red fluorescence trackers for the outer cell membrane: zwitterionic (naphthylvinyl)pyridinium dyes, ACS Appl. Bio Mater. 4 (3) (2021) 2089-2096.