AccScience Publishing / GPD / Volume 1 / Issue 1 / DOI: 10.36922/gpd.v1i1.87
ORIGINAL RESEARCH ARTICLE

Fluorescence imaging-guided photothermal therapy of asymmetric water-soluble pentamethine cyanine for colorectal cancer

Kun Tang1† Shuangshuang Jia1† Yaxin Zou1† Jiaheng Dong1 Fangyan Liu2 Kunli Cui1 Xiao Shi3 Lei Zhang1*
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1 Henan International Joint Laboratory for Nuclear Protein Regulation, School of Basic Medical Sciences, Henan University, Kaifeng 475004, P. R. China
2 Department of Academician Shengshou Hu Workstation, Fuwai Central China Cardiovascular Hospital, Zhengzhou 450046, P. R. China
3 Department of Pharmacy, The First Affiliated Hospital of Henan University, Henan University, Kaifeng 475004, P. R. China
Submitted: 8 May 2022 | Accepted: 16 June 2022 | Published: 29 June 2022
© 2022 by the Authors. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution 4.0 International License ( https://creativecommons.org/licenses/by/4.0/ )
Abstract

The combination of advanced optical technology and tumor treatment has developed into a selectively targeted tumor therapy strategy. Near-infrared (NIR) cyanine derivative has recently received increasing attention in photothermal therapy (PTT) because of its excellent biocompatibility, non-immunogenicity, high fluorescence and photothermal conversion efficiency, photostability, and tumor-homing. In this study, an asymmetric and water-soluble pentamethine cyanine was designed and synthesized to investigate the photosensitive activity and to explore its potential applications as a NIR photosensitizer for the diagnosis and therapy of colorectal cancer (CRC). The results of fluorescence imaging analysis showed that CY5-664 preferentially accumulated in the tumor as time elapsed, and the maximum fluorescence intensity was obtained at 24 h. Cell viability and animal xenograft model experiments showed that CY5-664 significantly inhibited tumor growth in vivo with 0.8 W/cm2 of 660 nm red laser pointer for 2 min, and in vitro with 0.5 W/cm2 of 660 nm red laser pointer for 2 min. In vitro and in vivo photothermal conversion experiments showed that CY5-664 exhibited an anti-CRC activity mainly through the PTT effect. Therefore, this work provides experimental evidence that CY5-664 is a drug candidate for CRC treatment mainly through the PTT effect and an alternative treatment strategy to develop a pentamethine cyanine-based CRC theranostic photosensitizer for synergistic CRC targeting, imaging, and therapy.

Keywords
Pentamethine cyanine
Photothermal therapy
Fluorescence imaging
Near-infrared
Colorectal cancer
Funding
National Natural Science Foundation of China
China Postdoctoral Science Foundation
Key R&D and Promotion Projects in Henan Province
Conflict of interest
The authors declare no conflict of interest.
References
[1]

Fakih MG, 2015, Metastatic colorectal cancer: Current state and future directions. J Clin Oncol, 33: 1809–1824. https://doi.org/10.1200/JCO.2014.59.7633

[2]

Kuipers EJ, Grady WM, Lieberman D, et al., 2015, Colorectal cancer. Nat Rev Dis Primers, 1: 15065. https://doi.org/10.1038/nrdp.2015.65

[3]

Bray F, Ferlay J, Soerjomataram I, et al., 2018, Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 68: 394–424. https://doi.org/10.3322/caac.21492

[4]

Dekker E, Tanis PJ, Vleugels JL, et al., 2019, Colorectal cancer. Lancet, 394: 1467–1480. https://doi.org/10.1016/S0140-6736(19)32319-0

[5]

Tomasello G, Petrelli F, Ghidini M, et al., 2017, FOLFOXIRI plus bevacizumab as conversion therapy for patients with initially unresectable metastatic colorectal cancer: A systematic review and pooled analysis. JAMA Oncol, 3: e170278. https://doi.org/10.1001/jamaoncol.2017.0278

[6]

Jardim DL, Rodrigues CA, Novis YA, et al., 2012, Oxaliplatin-related thrombocytopenia. Ann Oncol, 23: 1937–1942. https://doi.org/10.1093/annonc/mds074 

[7]

Fan W, Yung B, Huang P, et al., 2017, Nanotechnology for multimodal synergistic cancer therapy. Chem Rev, 117: 13566–13638. https://doi.org/10.1021/acs.chemrev.7b00258

[8]

de Boer E, Harlaar NJ, Taruttis A, et al., 2015, Optical innovations in surgery. Br J Surg, 102: e56–72. https://doi.org/10.1002/bjs.9713

[9]

Liang C, Xu L, Song G, et al., 2016, Emerging nanomedicine approaches fighting tumor metastasis: Animal models, metastasis-targeted drug delivery, phototherapy, and immunotherapy. Chem Soc Rev, 45: 6250–6269. https://doi.org/10.1039/c6cs00458j

[10]

Zhen X, Cheng P, Pu K, 2019, Recent advances in cell membrane-camouflaged nanoparticles for cancer phototherapy. Small, 15: e1804105. https://doi.org/10.1002/smll.201804105

[11]

Jung HS, Verwilst P, Sharma A, et al., 2018, Organic molecule-based photothermal agents: An expanding photothermal therapy universe. Chem Soc Rev, 47: 2280–2297. https://doi.org/10.1039/c7cs00522a

[12]

Lovell JF, Jin CS, Huynh E, et al., 2011, Porphysome nanovesicles generated by porphyrin bilayers for use as multimodal biophotonic contrast agents. Nat Mater, 10: 324–332. https://doi.org/10.1038/nmat2986

[13]

Luo S, Tan X, Fang S, et al., 2016, Mitochondria-targeted small-molecule fluorophores for dual modal cancer phototherapy. Adv Funct Mater, 26: 2826–2835. https://doi.org/10.1002/adfm.201600159

[14]

Mu X, Lu Y, Wu F, et al., 2020, Supramolecular nanodiscs self-assembled from non-ionic heptamethine cyanine for imaging-guided cancer photothermal therapy. Adv Mater, 32: e1906711. https://doi.org/10.1002/adma.201906711

[15]

Wang Y, Yang T, Ke H, et al., 2015, Smart albumin-biomineralized nanocomposites for multimodal imaging and photothermal tumor ablation. Adv Mater, 27: 3874–3882. https://doi.org/10.1002/adma.201500229

[16]

Deng L, Cai X, Sheng D, et al., 2017, A laser-activated biocompatible theranostic nanoagent for targeted multimodal imaging and photothermal therapy. Theranostics, 7: 4410–4423. https://doi.org/10.7150/thno.21283

[17]

Lu W, Melancon MP, Xiong C, et al., 2011, Effects of photoacoustic imaging and photothermal ablation therapy mediated by targeted hollow gold nanospheres in an orthotopic mouse xenograft model of glioma. Cancer Res, 71: 6116–6121. https://doi.org/10.1158/0008-5472.CAN-10-4557

[18]

Gao W, Sun Y, Cai M, et al., 2018, Copper sulfide nanoparticles as a photothermal switch for TRPV1 signaling to attenuate atherosclerosis. Nat Commun, 9: 231. https://doi.org/10.1038/s41467-017-02657-z

[19]

de Melo-Diogo D, Pais-Silva C, Dias DR, et al., 2017, Strategies to improve cancer photothermal therapy mediated by nanomaterials. Adv Healthc Mater, 6: 1700073. https://doi.org/10.1002/adhm.201700073

[20]

Yu H, Cui Z, Yu P, et al., 2015, pH- and NIR light-responsive micelles with hyperthermia-triggered tumor penetration and cytoplasm drug release to reverse doxorubicin resistance in breast cancer. Adv Funct Mater, 25: 2489–2500. https://doi.org/10.1002/adfm.201404484

[21]

Lee S, Jung JS, Jo G, et al., 2019, Near-infrared fluorescent sorbitol probe for targeted photothermal cancer therapy. Cancers, 11: 1286. https://doi.org/10.3390/cancers11091286

[22]

Shafirstein G, Baumler W, Hennings LJ, et al., 2012, Indocyanine green enhanced near-infrared laser treatment of murine mammary carcinoma. Int J Cancer, 130: 1208–1215. https://doi.org/10.1002/ijc.26126

[23]

Wang L, Li H, Zhang J, et al., 2013, Phosphatidylethanolamine binding protein 1 in vacular endothelial cell autophagy and atherosclerosis. J Physiol, 591: 5005–5015. https://doi.org/10.1113/jphysiol.2013.262667

[24]

Rio Y, Nicoud JF, Rehspringer JL, et al., 2000, Fullerodendrimers with peripheral triethyleneglycol chains. Tetrahedron Lett, 41: 10207–10210. https://doi.org/10.1016/S0040-4039(00)01837-2

[25]

Gao Y, Zheng QC, Xu S, et al., 2019, Theranostic nanodots with aggregation-induced emission characteristic for targeted and image-guided photodynamic therapy of hepatocellular carcinoma. Theranostics, 9: 1264–1279. https://doi.org/10.7150/thno.29101

[26]

Zhang L, Liu W, Liu F, et al., 2020, IMCA induces ferroptosis mediated by SLC7A11 through the AMPK/mTOR pathway in colorectal cancer. Oxid Med Cell Longev, 2020: 1675613. https://doi.org/10.1155/2020/1675613

[27]

James NS, Joshi P, Ohulchanskyy TY, et al., 2016, Photosensitizer (PS)-cyanine dye (CD) conjugates: Impact of the linkers joining the PS and CD moieties and their orientation in tumor-uptake and photodynamic therapy (PDT). Eur J Med Chem, 122: 770–785. https://doi.org/10.1016/j.ejmech.2016.06.045

[28]

Liu T, Liu W, Zhang M, et al., 2018, Ferrous-supply-regeneration nanoengineering for cancer-cell-specific ferroptosis in combination with imaging-guided photodynamic therapy. ACS Nano, 12: 12181–12192. https://doi.org/10.1021/acsnano.8b05860

[29]

Bhattarai P, Dai ZF. Cyanine based nanoprobes for cancer theranostics. Adv Healthc Mater, 6: 1700262. https://doi.org/10.1002/adhm.201700262

[30]

Zhang Q, Guo Q, Chen Q, et al., 2020, Highly efficient 2D NIR-II photothermal agent with fenton catalytic activity for cancer synergistic photothermal-chemodynamic therapy. Adv Sci (Weinh), 7: 1902576. https://doi.org/10.1002/advs.201902576

[31]

Garbuz DG, 2017, Regulation of heat shock gene expression in response to stress. Mol Biol (Mosk), 51: 400–417. https://doi.org/10.7868/S0026898417020100

[32]

Lo PC, Rodriguez-Morgade MS, Pandey RK, et al., 2020, The unique features and promises of phthalocyanines as advanced photosensitisers for photodynamic therapy of cancer. Chem Soc Rev, 49: 1041–1056. https://doi.org/10.1039/c9cs00129h

[33]

Qi JS, Song CP, Wang BS, et al., 2018, Reactive oxygen species signaling and stomatal movement in plant responses to drought stress and pathogen attack. J Integr Plant Biol, 60: 805–826. https://doi.org/10.1111/jipb.12654

[34]

Song Y, Miao Y, Song CP, 2014, Behind the scenes: The roles of reactive oxygen species in guard cells. New Phytol, 201: 1121–1140. https://doi.org/10.1111/nph.12565

[35]

Zhang L, Liu W, Wang Q, et al., 2018, New drug candidate targeting the 4A1 orphan nuclear receptor for medullary thyroid cancer therapy. Molecules, 23: 565. https://doi.org/10.3390/molecules23030565 

[36]

Yu HB, Li DY, Zhang HF, et al., 2010, Resveratrol inhibits invasion and metastasis of hepatocellular carcinoma cells. J Anim Vet Adv, 9: 3117–3124.

[37]

Chai LQ, Meng JH, Gao J, et al., 2018, Identification of a crustacean beta-1,3-glucanase related protein as a pattern recognition protein in antibacterial response. Fish Shellfish Immunol, 80: 155–164. https://doi.org/10.1016/j.fsi.2018.06.004

[38]

Cheng XS, Li MS, Du J, et al., 2011, Neuronal apoptosis in the developing cerebellum. Anat Histol Embryol, 40: 21–27. https://doi.org/10.1111/j.1439-0264.2010.01033.x

[39]

Guo ZK, Lin JT, Chang LS, et al., 2011, Features of cardiomyocyte division during rat heart development. Pak J Zool, 43: 321–330.

[40]

Chen M, Li K, Li H, et al., 2017, The glutathione peroxidase gene family in Gossypium hirsutum: Genome-wide identification, classification, gene expression and functional analysis. Sci Rep, 7: 44743. https://doi.org/10.1038/srep44743

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Gene & Protein in Disease, Electronic ISSN: 2811-003X Published by AccScience Publishing