Progress and Challenges of Water-soluble NIR-II Organic Fluorophores for Fluorescence Imaging in vivo

Abstract

The small-molecule fluorophores for the second near-infrared (NIR-II, 1000–1700 nm) window have attracted increasing attention in basic scientific research and preclinical practice owing to their deep-photo penetration, minimal physiological toxicity and simplicity of chemical modification. However, most of the reported small-molecule NIR-II fluorophores suffered from poor water solubility, which can easily cause organ toxicity. In addition, the aggregation caused by their poor water solubility in the aqueous solution would also result in weak fluorescence of these NIR-II fluorophores. Thus, it is highly desirable and valuable to develop water-soluble small-molecule NIR-II fluorophores with excellent photophysical properties for high-contrast in vivo imaging. In this review, we summarize the recent research advances in water-soluble small-molecule NIR-II fluorophores and highlight the representative bioimaging applications. Moreover, the potential challenges and perspectives of water-soluble small-molecule NIR-II fluorophores are discussed as well. We anticipate this review can help researchers to grab the latest information of water-soluble small-molecule fluorophores for NIR-II imaging, sequentially boosting their further development.

Keywords

Organic fluorophore / Fluorescent imaging / Imaging reagent / Fluorescent probe / The second near-infrared (NIR-II) imaging

References

[1] Hu Z, Fang C, Li B, Zhang Z, Cao C, Cai M, Su S, Sun X, Shi X, Li C, Zhou T, Zhang Y, Chi C, He P, Xia X, Chen Y, Gambhir S S, Cheng Z, Tian J. Nat. Biomed. Eng., 2020, 4: 259.

[2] Thomas J A. Chem. Soc. Rev., 2015, 44: 4494.

[3] Li C, Pang Y, Xu Y, Lu M, Tu L, Li Q, Sharma A, Guo Z, Li X, Sun Y. Chem. Soc. Rev., 2023, 52: 4392.

[4] Pratt E C, Skubal M, McLarney B, Causa-Andrieu P, Das S, Sawan P, Araji A, Riedl C, Vyas K, Tuch D, Grimm J. Nat. Biomed. Eng., 2022, 6: 559.

[5] Chen L, Lyu Y, Zhang X, Zheng L, Li Q, Ding D, Chen F, Liu Y, Li W, Zhang Y, Huang Q, Wang Z, Xie T, Zhang Q, Sima Y, Li K, Xu S, Ren T, Xiong M, Wu Y, Song J, Yuan L, Yang H, Zhang X-B, Tan W. Sci. China Chem., 2023, 66: 1336.

[6] Ou Y-F, Ren T-B, Yuan L, Zhang X-B. Chem.Biomed.Imaging, 2023, 1: 220.

[7] Chen Y, Wang S, Zhang F. Nat. Rev. Bioeng., 2023, 1: 60.

[8] Xu Y, Li C, An J, Ma X, Yang J, Luo L, Deng Y, Kim J S, Sun Y. Sci. China Chem., 2023, 66: 155.

[9] Tu L, Li C, Xiong X, Kim H J, Li Q, Mei L, Li J, Liu S, Kim S J, Sun Y. Angew. Chem. Int. Edit., 2023, 62: e202301560.

[10] Welsher K, Liu Z, Sherlock S P, Robinson J T, Chen Z, Daranciang D, Dai H. Nat. Nanotechnol., 2009, 4: 773.

[11] Qin Z, Ren T-B, Zhou H, Zhang X, He L, Li Z, Zhang X-B, Yuan L. Angew. Chem. Int. Ed., 2022, 61: e202201541.

[12] Wan H, Du H, Wang F, Dai H. Adv. Funct. Mater., 2019, 29: 1900566.

[13] He S, Song J, Qu J, Cheng Z. Chem. Soc. Rev., 2018, 47: 4258.

[14] Soo Choi H, Liu W, Misra P, Tanaka E, Zimmer J P, Itty Ipe B, Bawendi M G, Frangioni J V. Nat. Biotechnol., 2007, 25: 1165.

[15] Lorenzo I, Serra-Prat M, Yébenes J C. Nutrients, 2019, 11: 1857.

[16] Cheng Q, Tian Y, Dang H, Teng C, Xie K, Yin D, Yan L. Adv. Healthc. Mater., 2022, 11: 2101697.

[17] Li B, Lu L, Zhao M, Lei Z, Zhang F. Angew. Chem. Int. Edit., 2018, 57: 7483.

[18] Yao C, Chen Y, Zhao M, Wang S, Wu B, Yang Y, Yin D, Yu P, Zhang H, Zhang F. Angew. Chem. Int. Edit., 2022, 61: e202114273.

[19] Li B, Zhao M, Feng L, Dou C, Ding S, Zhou G, Lu L, Zhang H, Chen F, Li X, Li G, Zhao S, Jiang C, Wang Y, Zhao D, Cheng Y, Zhang F. Nat. Commun., 2020, 11: 3102.

[20] Antaris A L, Chen H, Diao S, Ma Z, Zhang Z, Zhu S, Wang J, Lozano A X, Fan Q, Chew L, Zhu M, Cheng K, Hong X, Dai H, Cheng Z. Nat. Commun., 2017, 8: 15269.

[21] Cheng P, Pu K. Nat. Rev. Mater., 2021, 6: 1095.

[22] Cosco E D, Caram J R, Bruns O T, Franke D, Day R A, Farr E P, Bawendi M G, Sletten E M. Angew. Chem. Int. Edit., 2017, 56: 13126.

[23] Cosco E D, Spearman A L, Ramakrishnan S, Lingg J G P, Saccomano M, Pengshung M, Arús B A, Wong K C Y, Glasl S, Ntziachristos V, Warmer M, McLaughlin R R, Bruns O T, Sletten E M. Nat. Chem., 2020, 12: 1123.

[24] Bhalani D V, Nutan B, Kumar A, Singh Chandel A K. Biomedicines, 2022, 10: 2055.

[25] Tenchov R, Bird R, Curtze A E, Zhou Q. ACS Nano, 2021, 15: 16982.

[26] Yang Y, Sun C, Wang S, Yan K, Zhao M, Wu B, Zhang F. Angew. Chem. Int. Edit., 2022, 61: e202117436.

[27] Zeng Z, Ouyang J, Sun L, Zeng C, Zeng F, Wu S. Anal. Chem., 2020, 92: 9257.

[28] Bai L, Hu Z, Han T, Wang Y, Xu J, Jiang G, Feng X, Sun B, Liu X, Tian R, Sun H, Zhang S, Chen X, Zhu S. Theranostics, 2022, 12: 4536.

[29] Zhang Y., Jia Y., Zhu S., SmartMat, 2023, DOI: https://doi.org/10.1002/smm2.1245

[30] Lei Z, Sun C, Pei P, Wang S, Li D, Zhang X, Zhang F. Angew. Chem. Int. Edit., 2019, 58: 8166.

[31] Tao Z, Hong G, Shinji C, Chen C, Diao S, Antaris A L, Zhang B, Zou Y, Dai H. Angew. Chem. Int. Edit., 2013, 52: 13002.

[32] Shi Y, Yuan W, Liu Q, Kong M, Li Z, Feng W, Hu K, Li F. ACS Mater. Lett., 2019, 1: 418.

[33] Zhao M, Wang J, Lei Z, Lu L, Wang S, Zhang H, Li B, Zhang F. Angew. Chem. Int. Edit., 2021, 60: 5091.

[34] Wang S, Fan Y, Li D, Sun C, Lei Z, Lu L, Wang T, Zhang F. Nat. Commun., 2019, 10: 1058.

[35] Lu X, Zhu Y, Bai R, Wu Z, Qian W, Yang L, Cai R, Yan H, Li T, Pandey V, Liu Y, Lobie P E, Chen C, Zhu T. Nat. Nanotechnol., 2019, 14: 719.

[36] de Castro C E, Panico K, Stangherlin L M, Ribeiro C A S, da Silva M C C, Carneiro-Ramos M S, Dal-Bó A G, Giacomelli F C. Bioconjugate Chem., 2020, 31: 2638.

[37] Huang J, Xie C, Zhang X, Jiang Y, Li J, Fan Q, Pu K. Angew. Chem. Int. Edit., 2019, 58: 15120.

[38] Ouyang J, Sun L, Zeng F, Wu S. Analyst, 2022, 147: 410.

[39] Chen Y, Pei P, Lei Z, Zhang X, Yin D, Zhang F. Angew. Chem. Int. Edit., 2021, 60: 15809.

[40] Yan D, Li T, Yang Y, Niu N, Wang D, Ge J, Wang L, Zhang R, Wang D, Tang B Z. Adv. Mater., 2022, 34: 2206643.

[41] Sun Y, Qu C, Chen H, He M, Tang C, Shou K, Hong S, Yang M, Jiang Y, Ding B, Xiao Y, Xing L, Hong X, Cheng Z. Chem. Sci., 201, 7: 6203.

[42] Bandi V G, Luciano M P, Saccomano M, Patel N L, Bischof T S, Lingg J G P, Tsrunchev P T, Nix M N, Ruehle B, Sanders C, Riffle L, Robinson C M, Difilippantonio S, Kalen J D, Resch-Genger U, Ivanic J, Bruns O T, Schnermann M J. Nat. Methods, 2022, 19: 353.

[43] Li D-H, Gamage R S, Oliver A G, Patel N L, Muhammad Usama S, Kalen J D, Schnermann M J, Smith B D. Angew. Chem. Int. Edit., 2023, 62: e202305062.

[44] Choi H S, Nasr K, Alyabyev S, Feith D, Lee J H, Kim S H, Ashitate Y, Hyun H, Patonay G, Strekowski L, Henary M, Frangioni J V. Angew. Chem. Int. Edit., 2011, 50: 6258.

[45] Jia S, Lin E Y, Mobley E B, Lim I, Guo L, Kallepu S, Low P S, Sletten E M. Chem, 2023, 9: 3648.

[46] Ding B, Xiao Y, Zhou H, Zhang X, Qu C, Xu F, Deng Z, Cheng Z, Hong X. J. Med. Chem., 2019, 62: 2049.

[47] de Valk K S, Handgraaf H J, Deken M M, Sibinga Mulder B G, Valentijn A R, Terwisscha van Scheltinga A G, Kuil J, van Esdonk M J, Vuijk J, Bevers R F, Peeters K C, Holman F A, Frangioni J V, Burggraaf J, Vahrmeijer A L. Nat. Commun., 2019, 10: 3118.

[48] Choi H S, Gibbs S L, Lee J H, Kim S H, Ashitate Y, Liu F, Hyun H, Park G, Xie Y, Bae S, Henary M, Frangioni J V. Nat. Biotechnol., 2013, 31: 148.

[49] Wang H, Kang H, Dinh J, Yokomizo S, Stiles WR, Tully M, Cardenas K, Srinivas S, Ingerick J, Ahn S, Bao K, Choi H S. Biomater. Res., 2022, 26: 51.

[50] Chen S, Brunskill E W, Potter S S, Dexheimer P J, Salomonis N, Aronow B J, Hong C I, Zhang T, Kopan R. Dev. Cell, 2015, 35: 49.

[51] Perazella M A, Coca S G. Nat. Rev. Nephrol., 2013, 9: 484.

[52] Chen C, Tian R, Zeng Y, Chu C, Liu G. Bioconjugate Chem., 2020, 31: 276.

[53] Chen Z, Zhang Z, Zeng F, Wu S. Chem. Biomed. Imaging, 2023, 1: 716.

[54] Zeng C, Tan Y, Sun L, Long Y, Zeng F, Wu S. ACS Appl. Mater. Interfaces, 2023, 15: 17664.

[55] Ridker P M, Cook N R. Lancet, 2013, 382: 1762.

[56] Dong Y, Lu X, Li Y, Chen W, Yin L, Zhao J, Hu X, Li X, Lei Z, Wu Y, Chen H, Luo X, Qian X, Yang Y. Chin. Chem. Lett., 2023, 34: 108154.

[57] Antaris A L, Chen H, Cheng K, Sun Y, Hong G, Qu C, Diao S, Deng Z, Hu X, Zhang B, Zhang X, Yaghi O K, Alamparambil Z R, Hong X, Cheng Z, Dai H. Nat. Mater., 201, 15: 235.

[58] Luo X, Li J, Zhao J, Gu L, Qian X, Yang Y. Chin. Chem. Lett., 2019, 30: 839.

[59] Li D-H, Smith B D. J. Org. Chem., 2022, 87: 5893.

[60] Xu W, Leary E, Sangtarash S, Jirasek M, González M T, Christensen K E, Abellán Vicente L, Agraít N, Higgins S J, Nichols R J, Lambert C J, Erson H L. J. Am. Chem. Soc., 2021, 143: 20472.

[61] Tolbert L M, Zhao X. J. Am. Chem. Soc., 1997, 119: 3253.

[62] Grüneboom A, Hawwari I, Weidner D, Culemann S, Müller S, Henneberg S, Brenzel A, Merz S, Bornemann L, Zec K, Wuelling M, Kling L, Hasenberg M, Voortmann S, Lang S, Baum W, Ohs A, Kraff O, Quick H H, Jäger M, Landgraeber S, Dudda M, Danuser R, Stein J V, Rohde M, Gelse K, Garbe A I, Adamczyk A, Westendorf A M, Hoffmann D, Christiansen S, Engel D R, Vortkamp A, Krönke G, Herrmann M, Kamradt T, Schett G, Hasenberg A, Gunzer M. Nat. Metab., 2019, 1: 236.

[63] Sivaraj K K, Adams R H. Development, 201, 143: 2706.

[64] Mi C, Zhang X, Yang C, Wu J, Chen X, Ma C, Wu S, Yang Z, Qiao P, Liu Y, Wu W, Guo Z, Liao J, Zhou J, Guan M, Liang C, Liu C, Jin D. Nat. Commun., 2023, 14: 6287.

[65] Chen P, Qu F, He L, Li M, Sun P, Fan Q, Zhang C, Li D. J. Nanobiotechnol., 2023, 21: 230.

[66] Yan R, Guo Y, Wang X, Liang G, Yang A, Li J. ACS Nano, 2022, 16: 8399.

[67] Zaheer A, Lenkinski R E, Mahmood A, Jones A G, Cantley L C, Frangioni J V. Nat. Biotechnol., 2001, 19: 1148.

[68] Bhushan K R, Misra P, Liu F, Mathur S, Lenkinski R E, Frangioni J V. J. Am. Chem. Soc., 2008, 130: 17648.

[69] Hyun H, Wada H, Bao K, Gravier J, Yadav Y, Laramie M, Henary M, Frangioni J V, Choi H S. Angew. Chem. Int. Edit., 2014, 53: 10668.

[70] Feng Y, Zhu S, Antaris A L, Chen H, Xiao Y, Lu X, Jiang L, Diao S, Yu K, Wang Y, Herraiz S, Yue J, Hong X, Hong G, Cheng Z, Dai H, Hsueh A J. Chem. Sci., 2017, 8: 3703.

[71] Lin J, Li Q, Zeng X, Chen Z, Ding Q, Li Y, Zhou H, Meng X, Chen D, Deng Z, Hong X, Xiao Y. Sci. China: Chem., 2020, 63: 766.

[72] Zhang X, Ji A, Wang Z, Lou H, Li J, Zheng L, Zhou Y, Qu C, Liu X, Chen H, Cheng Z. J. Med. Chem., 2021, 64: 11543.

[73] Terenziani F, Przhonska O V, Webster S, Padilha L A, Slominsky Y L, Davydenko I G, Gerasov A O, Kovtun Y P, Shandura M P, Kachkovski A D, Hagan D J, Van Stryland E W, Painelli A. J. Phys. Chem. Lett., 2010, 1: 1800.