Probes and nano-delivery systems targeting NAD(P)H:quinone oxidoreductase 1: a mini-review
Xuewen Mu1, Yun Xu2, Zheng Wang1(), Dunyun Shi3()
1. School of Pharmaceutical Science & Technology, Tianjin University, Tianjin 300072, China 2. Central Lab, Shenzhen Second People’s Hospital/the First Affiliated Hospital of Shenzhen University, Shenzhen 518035, China 3. Institute of Hematology, Shenzhen Second People’s Hospital/the First Affiliated Hospital of Shenzhen University, Shenzhen 518035, China
The two-electron cytoplasmic reductase NAD(P)H:quinone oxidoreductase 1 is expressed in many tissues. NAD(P)H:quinone oxidoreductase 1 is well-known for being highly expressed in most cancers. Therefore, it could be a target for cancer therapy. Because it is a quinone reductase, many bioimaging probes based on quinone structures target NAD(P)H:quinone oxidoreductase 1 to diagnose tumours. Its expression is higher in tumours than in normal tissues, and using target drugs such as β-lapachone to reduce side effects in normal tissues can help. However, the physicochemical properties of β-lapachone limit its application. The problem can be solved by using nanosystems to deliver β-lapachone. This mini-review summarizes quinone-based fluorescent, near-infrared and two-photon fluorescent probes, as well as nanosystems for delivering the NAD(P)H:quinone oxidoreductase 1-activating drug β-lapachone. This review provides valuable information for the future development of probes and nano-delivery systems that target NAD(P)H:quinone oxidoreductase 1.
G Tedeschi, S Chen, V Massey. DT-diaphorase. Redox potential, steady-state, and rapid reaction studies. Journal of Biological Chemistry, 1995, 270( 3): 11981204
2
D Ross, D Siegel. Functions of NQO1 in cellular protection and CoQ10 metabolism and its potential role as a redox sensitive molecular switch. Frontiers in Physiology, 2017, 8 : 595 https://doi.org/10.3389/fphys.2017.00595
3
S Hosoda, W Nakamura, K Hayashi. Properties and reaction mechanism of DT diaphorase from rat liver. Journal of Biological Chemistry, 1974, 249( 20): 6416– 6423 https://doi.org/10.1016/S0021-9258(19)42173-X
4
R Li, M A Bianchet, P Talalay, L M Amzel. The three-dimensional structure of NAD(P)H:quinone reductase, a flavoprotein involved in cancer chemoprotection and chemotherapy: mechanism of the two-electron reduction. Proceedings of the National Academy of Sciences of the United States of America, 1995, 92( 19): 8846– 8850 https://doi.org/10.1073/pnas.92.19.8846
5
D Ross, J K Kepa, S L Winski, H D Beall, A Anwar, D Siegel. NAD(P)H:quinone oxidoreductase 1 (NQO1): chemoprotection, bioactivation, gene regulation and genetic polymorphisms. Chemico-Biological Interactions, 2000, 129( 1–2): 77– 97 https://doi.org/10.1016/S0009-2797(00)00199-X
6
D Siegel, D L Gustafson, D L Dehn, J Y Han, P Boonchoong, L J Berliner, D Ross. NAD(P)H:quinone oxidoreductase 1: role as a superoxide scavenger. Molecular Pharmacology, 2004, 65( 5): 1238– 1247 https://doi.org/10.1124/mol.65.5.1238
7
R E Beyer, J Segura-Aguilar, S Di Bernardo, M Cavazzoni, R Fato, D Fiorentini, M C Galli, M Setti, L Landi, G Lenaz. The role of DT-diaphorase in the maintenance of the reduced antioxidant form of coenzyme Q in membrane systems. Proceedings of the National Academy of Sciences of the United States of America, 1996, 93( 6): 2528– 2532 https://doi.org/10.1073/pnas.93.6.2528
8
D C Liebler. The role of metabolism in the antioxidant function of vitamin E. Critical Reviews in Toxicology, 1993, 23( 2): 147– 169 https://doi.org/10.3109/10408449309117115
9
A Bindoli, M Valente, L Cavallini. Inhibition of lipid peroxidation by alpha-tocopherolquinone and α-tocopherol-hydroquinone. Biochemistry International, 1985, 10( 5): 753– 761
10
I Kohar M Baca C Suarna R Stocker P T Southwell-Keely. Is α-tocopherol a reservoir for α-tocopheryl hydroquinone? Free Radical Biology & Medicine, 1995, 19( 2): 197– 207
11
D Siegel, E M Bolton, J A Burr, D C Liebler, D Ross. The reduction of alpha-tocopherolquinone by human NAD(P)H:quinone oxidoreductase: the role of alpha-tocopherol hydroquinone as a cellular antioxidant. Molecular Pharmacology, 1997, 52( 2): 300– 305 https://doi.org/10.1124/mol.52.2.300
12
D Ross. Quinone reductases multitasking in the metabolic world. Drug Metabolism Reviews, 2004, 36( 3–4): 639– 654 https://doi.org/10.1081/DMR-200033465
13
H Zhu, Y Li. NAD(P)H:quinone oxidoreductase 1 and its potential protective role in cardiovascular diseases and related conditions. Cardiovascular Toxicology, 2012, 12( 1): 39– 45 https://doi.org/10.1007/s12012-011-9136-9
14
H Zhu, Z Jia, J E Mahaney, D Ross, H P Misra, M A Trush, Y Li. The highly expressed and inducible endogenous NAD(P)H:quinone oxidoreductase 1 in cardiovascular cells acts as a potential superoxide scavenger. Cardiovascular Toxicology, 2007, 7( 3): 202– 211 https://doi.org/10.1007/s12012-007-9001-z
15
J M Mccord, I Fridovich. Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). Journal of Biological Chemistry, 1969, 244( 22): 6049– 6055 https://doi.org/10.1016/S0021-9258(18)63504-5
16
D Siegel, D Ross. Immunodetection of NAD(P)H:quinone oxidoreductase 1 (NQO1) in human tissues. Free Radical Biology & Medicine, 2000, 29( 3–4): 246– 253 https://doi.org/10.1016/S0891-5849(00)00310-5
K Zhang, D Chen, K Ma, X Wu, H Hao, S Jiang. NAD(P)H:quinone oxidoreductase 1 (NQO1) as a therapeutic and diagnostic target in cancer. Journal of Medicinal Chemistry, 2018, 61( 16): 6983– 7003 https://doi.org/10.1021/acs.jmedchem.8b00124
G Asher, J Lotem, B Cohen, L Sachs, Y Shaul. Regulation of p53 stability and p53-dependent apoptosis by NADH quinone oxidoreductase 1. Proceedings of the National Academy of Sciences of the United States of America, 2001, 98( 3): 1188– 1193 https://doi.org/10.1073/pnas.98.3.1188
21
G Asher, J Lotem, R Kama, L Sachs, Y Shaul. NQO1 stabilizes p53 through a distinct pathway. Proceedings of the National Academy of Sciences of the United States of America, 2002, 99( 5): 3099– 3104 https://doi.org/10.1073/pnas.052706799
22
G Asher, J Lotem, L Sachs, C Kahana, Y Shaul. MDM-2 and ubiquitin-independent p53 proteasomal degradation regulated by NQO1. Proceedings of the National Academy of Sciences of the United States of America, 2002, 99( 20): 13125– 13130 https://doi.org/10.1073/pnas.202480499
23
G Asher, Z Bercovich, P Tsvetkov, Y Shaul, C Kahana. 20s proteasomal degradation of ornithine decarboxylase is regulated by NQO1. Molecular Cell, 2005, 17( 5): 645– 655 https://doi.org/10.1016/j.molcel.2005.01.020
24
B S Cornblatt, L Ye, A T Dinkova-Kostova, M Erb, J W Fahey, N K Singh, M S Chen, T Stierer, E Garrett-Mayer, P Argani, N E Davidson, P Talalay, T W Kensler, K Visvanathan. Preclinical and clinical evaluation of sulforaphane for chemoprevention in the breast. Carcinogenesis, 2007, 28( 7): 1485– 1490 https://doi.org/10.1093/carcin/bgm049
25
Y J Surh. Cancer chemoprevention with dietary phytochemicals. Nature Reviews Cancer, 2003, 3( 10): 768– 780 https://doi.org/10.1038/nrc1189
26
J J Schlager, G Powis. Cytosolic NAD(P)H:(quinone-acceptor)oxidoreductase in human normal and tumor tissue: effects of cigarette smoking and alcohol. International Journal of Cancer, 1990, 45( 3): 403– 409 https://doi.org/10.1002/ijc.2910450304
27
Y Ma, J Kong, G Yan, X Ren, D Jin, T Jin, L Lin, Z Lin. NQO1 overexpression is associated with poor prognosis in squamous cell carcinoma of the uterine cervix. BMC Cancer, 2014, 14( 1): 414 https://doi.org/10.1186/1471-2407-14-414
28
Y Yang, Y Zhang, Q Wu, X Cui, Z Lin, S Liu, L Chen. Clinical implications of high NQO1 expression in breast cancers. Journal of Experimental & Clinical Cancer Research, 2014, 33( 1): 14 https://doi.org/10.1186/1756-9966-33-14
29
A M Lewis, M Ough, J Du, M S Tsao, L W Oberley, J J Cullen. Targeting NAD(P)H:quinone oxidoreductase (NQO1) in pancreatic cancer. Molecular Carcinogenesis, 2017, 56( 7): 1825– 1834 https://doi.org/10.1002/mc.20199
30
B Madajewski, M A Boatman, G Chakrabarti, D A Boothman, E A Bey. Depleting tumor-NQO1 potentiates anoikis and inhibits growth of NSCLC. Molecular Cancer Research, 2016, 14( 1): 14– 25 https://doi.org/10.1158/1541-7786.MCR-15-0207-T
31
E T Oh, J W Kim, J M Kim, S J Kim, J S Lee, S S Hong, J Goodwin, R J Ruthenborg, M G Jung, H J Lee, C H Lee, E S Park, C Kim, H J Park. NQO1 inhibits proteasome-mediated degradation of HIF-1α. Nature Communications, 2016, 7( 1): 13593 https://doi.org/10.1038/ncomms13593
H Wagner. Image-guided conformal radiation therapy planning and delivery for non-small-cell lung cancer. Cancer Control, 2003, 10( 4): 277– 288 https://doi.org/10.1177/107327480301000402
34
B J Altman, Z E Stine, C V Dang. From Krebs to clinic: glutamine metabolism to cancer therapy. Nature Reviews. Cancer, 2016, 16( 11): 749 https://doi.org/10.1038/nrc.2016.114
N S Awadallah, D Dehn, R J Shah, S Russell Nash, Y K Chen, D Ross, J S Bentz, K R Shroyer. NQO1 expression in pancreatic cancer and its potential use as a biomarker. Applied Immunohistochemistry & Molecular Morphology, 2008, 16( 1): 24– 31 https://doi.org/10.1097/PAI.0b013e31802e91d0
37
A Razgulin, N Ma, J Rao. Strategies for in vivo imaging of enzyme activity: an overview and recent advances. Chemical Society Reviews, 2011, 40( 7): 4186– 4216 https://doi.org/10.1039/c1cs15035a
38
R Siegel, D Naishadham, A Jemal. Cancer statistics, 2012. CA: a Cancer Journal for Clinicians, 2012, 62( 1): 10– 29 https://doi.org/10.3322/caac.20138
39
Q T Nguyen, E S Olson, T A Aguilera, T Jiang, M Scadeng, L G Ellies, R Y Tsien. Surgery with molecular fluorescence imaging using activatable cell-penetrating peptides decreases residual cancer and improves survival. Proceedings of the National Academy of Sciences of the United States of America, 2010, 107( 9): 4317– 4322 https://doi.org/10.1073/pnas.0910261107
40
W C Silvers, B Prasai, D H Burk, M L Brown, R L Mccarley. Profluorogenic reductase substrate for rapid, selective, and sensitive visualization and detection of human cancer cells that overexpress nqo1. Journal of the American Chemical Society, 2013, 135( 1): 309– 314 https://doi.org/10.1021/ja309346f
41
R M Duke, E B Veale, F M Pfeffer, P E Kruger, T Gunnlaugsson. Colorimetric and fluorescent anion sensors: an overview of recent developments in the use of 1,8-naphthalimide-based chemosensors. Chemical Society Reviews, 2010, 39( 10): 3936– 3953 https://doi.org/10.1039/b910560n
42
X Qian, Y Xiao, Y Xu, X Guo, J Qian, W Zhu. “Alive” dyes as fluorescent sensors: fluorophore, mechanism, receptor and images in living cells. Chemical Communications (Cambridge), 2010, 46( 35): 6418– 6436 https://doi.org/10.1039/c0cc00686f
43
K M Mcmahon, M Volpato, H Y Chi, P Musiwaro, K Poterlowicz, Y Peng, A J Scally, L H Patterson, R M Phillips, C W Sutton. Characterization of changes in the proteome in different regions of 3D multicell tumor spheroids. Journal of Proteome Research, 2012, 11( 5): 2863– 2875 https://doi.org/10.1021/pr2012472
44
M C Cox, L M Reese, L R Bickford, S S Verbridge. Toward the broad adoption of 3D tumor models in the cancer drug pipeline. ACS Biomaterials Science & Engineering, 2015, 1( 10): 877– 894 https://doi.org/10.1021/acsbiomaterials.5b00172
45
J Friedrich, C Seidel, R Ebner, L A Kunz-Schughart. Spheroid-based drug screen: considerations and practical approach. Nature Protocols, 2009, 4( 3): 309– 324 https://doi.org/10.1038/nprot.2008.226
46
M Vinci, S Gowan, F Boxall, L Patterson, M Zimmermann, W Court, C Lomas, M Mendiola, D Hardisson, S A Eccles. Advances in establishment and analysis of three-dimensional tumor spheroid-based functional assays for target validation and drug evaluation. BMC Biology, 2012, 10( 1): 29 https://doi.org/10.1186/1741-7007-10-29
47
A L Vahrmeijer, M Hutteman, J R van der Vorst, C J van de Velde, J V Frangioni. Image-guided cancer surgery using near-infrared fluorescence. Nature Reviews. Clinical Oncology, 2013, 10( 9): 507– 518 https://doi.org/10.1038/nrclinonc.2013.123
48
Q T Nguyen, R Y Tsien. Fluorescence-guided surgery with live molecular navigation—a new cutting edge. Nature Reviews Cancer, 2013, 13( 9): 653– 662 https://doi.org/10.1038/nrc3566
49
S Keereweer, P B van Driel, T J Snoeks, J D Kerrebijn, R J Baatenburg De Jong, A L Vahrmeijer, H J Sterenborg, C W Lowik. Optical image-guided cancer surgery: challenges and limitations. Clinical Cancer Research, 2013, 19( 14): 3745– 3754 https://doi.org/10.1158/1078-0432.CCR-12-3598
50
G M Van Dam, G Themelis, L M Crane, N J Harlaar, R G Pleijhuis, W Kelder, A Sarantopoulos, J S De Jong, H J Arts, A G Van Der Zee, J Bart, P S Low, V Ntziachristos. Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-alpha targeting: first in-human results. Nature Medicine, 2011, 17( 10): 1315– 1319 https://doi.org/10.1038/nm.2472
51
H Kobayashi, P L Choyke. Target-cancer-cell-specific activatable fluorescence imaging probes: rational design and in vivo applications. Accounts of Chemical Research, 2011, 44( 2): 83– 90 https://doi.org/10.1021/ar1000633
52
F De Moliner, I Biazruchka, K Konsewicz, S Benson, S Singh, J S Lee, M Vendrell. Near-infrared benzodiazoles as small molecule environmentally-sensitive fluorophores. Frontiers of Chemical Science and Engineering, 2022, 16( 1): 128– 135 https://doi.org/10.1007/s11705-021-2080-8
53
Z Shen, B Prasai, Y Nakamura, H Kobayashi, M S Jackson, R L Mccarley. A near-infrared, wavelength-shiftable, turn-on fluorescent probe for the detection and imaging of cancer tumor cells. ACS Chemical Biology, 2017, 12( 4): 1121– 1132 https://doi.org/10.1021/acschembio.6b01094
54
Q Gong, F Yang, J Hu, T Li, P Wang, X Li, X Zhang. Rational designed highly sensitive NQO1-activated near-infrared fluorescent probe combined with nqo1 substrates in vivo: an innovative strategy for NQO1-overexpressing cancer theranostics. European Journal of Medicinal Chemistry, 2021, 224 : 113707 https://doi.org/10.1016/j.ejmech.2021.113707
55
M F Mendoza, N M Hollabaugh, S U Hettiarachchi, R L Mccarley. Human NAD(P)H:quinone oxidoreductase type I (hNQO1) activation of quinone propionic acid trigger groups. Biochemistry, 2012, 51( 40): 8014– 8026 https://doi.org/10.1021/bi300760u
56
S R Punganuru, H R Madala, V Arutla, R Zhang, K S Srivenugopal. Characterization of a highly specific NQO1-activated near-infrared fluorescent probe and its application for in vivo tumor imaging. Scientific Reports, 2019, 9( 1): 8577 https://doi.org/10.1038/s41598-019-44111-8
57
Z Cheng, W O Valença, G G Dias, J Scott, N D Barth, Moliner F de, G B P Souza, R J Mellanby, M Vendrell, Silva Júnior E N da. Natural product-inspired profluorophores for imaging NQO1 activity in tumour tissues. Bioorganic & Medicinal Chemistry, 2019, 27( 17): 3938– 3946 https://doi.org/10.1016/j.bmc.2019.07.017
58
Z Yuan, M Xu, T Wu, X Zhang, Y Shen, U Ernest, L Gui, F Wang, Q He, H Chen. Design and synthesis of NQO1 responsive fluorescence probe and its application in bio-imaging for cancer diagnosis. Talanta, 2019, 198 : 323– 329 https://doi.org/10.1016/j.talanta.2019.02.009
59
J Zhang, H W Liu, X X Hu, J Li, L H Liang, X B Zhang, W Tan. Efficient two-photon fluorescent probe for nitroreductase detection and hypoxia imaging in tumor cells and tissues. Analytical Chemistry, 2015, 87( 23): 11832– 11839 https://doi.org/10.1021/acs.analchem.5b03336
60
W S Shin, M G Lee, P Verwilst, J H Lee, S G Chi, J S Kim. Mitochondria-targeted aggregation induced emission theranostics: crucial importance of in situ activation. Chemical Science, 2016, 7( 9): 6050– 6059
61
Q Xu, C H Heo, J A Kim, H S Lee, Y Hu, D Kim, K M Swamy, G Kim, S J Nam, H M Kim, J Yoon. A selective imidazoline-2-thione-bearing two-photon fluorescent probe for hypochlorous acid in mitochondria. Analytical Chemistry, 2016, 88( 12): 6615– 6620 https://doi.org/10.1021/acs.analchem.6b01738
62
Q Xu, C H Heo, G Kim, H W Lee, H M Kim, J Yoon. Development of imidazoline-2-thiones based two-photon fluorescence probes for imaging hypochlorite generation in a co-culture system. Angewandte Chemie International Edition, 2015, 54( 16): 4890– 4894 https://doi.org/10.1002/anie.201500537
63
H M Kim, B R Cho. Small-molecule two-photon probes for bioimaging applications. Chemical Reviews, 2015, 115( 11): 5014– 5055 https://doi.org/10.1021/cr5004425
64
H W Liu, S Xu, P Wang, X X Hu, J Zhang, L Yuan, X B Zhang, W Tan. An efficient two-photon fluorescent probe for monitoring mitochondrial singlet oxygen in tissues during photodynamic therapy. Chemical Communications (Cambridge), 2016, 52( 83): 12330– 12333 https://doi.org/10.1039/C6CC05880A
65
Y Liu, F Meng, L He, X Yu, W Lin. Fluorescence behavior of a unique two-photon fluorescent probe in aggregate and solution states and highly sensitive detection of RNA in water solution and living systems. Chemical Communications (Cambridge), 2016, 52( 57): 8838– 8841 https://doi.org/10.1039/C6CC03746A
66
Z Mao, W Feng, Z Li, L Zeng, W Lv, Z Liu. Nir in, far-red out: developing a two-photon fluorescent probe for tracking nitric oxide in deep tissue. Chemical Science, 2016, 7( 8): 5230– 5235
67
N Kwon, M K Cho, S J Park, D Kim, S J Nam, L Cui, H M Kim, J Yoon. An efficient two-photon fluorescent probe for human NAD(P)H:quinone oxidoreductase (hNQO1) detection and imaging in tumor cells. Chemical Communications, 2017, 53( 3): 525– 528 https://doi.org/10.1039/C6CC08971B
68
W S Shin, J Han, P Verwilst, R Kumar, J H Kim, J S Kim. Cancer targeted enzymatic theranostic prodrug: precise diagnosis and chemotherapy. Bioconjugate Chemistry, 2016, 27( 5): 1419– 1426 https://doi.org/10.1021/acs.bioconjchem.6b00184
69
N Kaneda, H Nagata, T Furuta, T Yokokura. Metabolism and pharmacokinetics of the camptothecin analogue CPT-11 in the mouse. Cancer Research, 1990, 50( 6): 1715– 1720
70
M S Bentle, E A Bey, Y Dong, K E Reinicke, D A Boothman. New tricks for old drugs: the anticarcinogenic potential of DNA repair inhibitors. Journal of Molecular Histology, 2006, 37( 5–7): 203– 218 https://doi.org/10.1007/s10735-006-9043-8
71
D A Boothman, D K Trask, A B Pardee. Inhibition of potentially lethal DNA damage repair in human tumor cells by beta-lapachone, an activator of topoisomerase I. Cancer Research, 1989, 49( 3): 605– 612
72
J J Pink, S M Planchon, C Tagliarino, M E Varnes, D Siegel, D A Boothman. NAD(P)H:quinone oxidoreductase activity is the principal determinant of β-lapachone cytotoxicity. Journal of Biological Chemistry, 2000, 275( 8): 5416– 5424 https://doi.org/10.1074/jbc.275.8.5416
73
S M Planchon, J J Pink, C Tagliarino, W G Bornmann, M E Varnes, D A Boothman. β-Lapachone-induced apoptosis in human prostate cancer cells: involvement of NQO1/xip3. Experimental Cell Research, 2001, 267( 1): 95– 106 https://doi.org/10.1006/excr.2001.5234
74
M Ough, A Lewis, E A Bey, J Gao, J M Ritchie, W Bornmann, D A Boothman, L W Oberley, J J Cullen. Efficacy of β-lapachone in pancreatic cancer treatment: exploiting the novel, therapeutic target NQO1. Cancer Biology & Therapy, 2005, 4( 1): 95– 102 https://doi.org/10.4161/cbt.4.1.1382
75
M S Beg, X Huang, M A Silvers, D E Gerber, J Bolluyt, V Sarode, F Fattah, R J Deberardinis, M E Merritt, X J Xie, R Leff, D Laheru, D A Boothman. Using a novel NQO1 bioactivatable drug, beta-lapachone (ARQ761), to enhance chemotherapeutic effects by metabolic modulation in pancreatic cancer. Journal of Surgical Oncology, 2017, 116( 1): 83– 88 https://doi.org/10.1002/jso.24624
76
S Zada, J S Hwang, M Ahmed, T H Lai, T M Pham, D H Kim, D R Kim. Protein kinase a activation by beta-lapachone is associated with apoptotic cell death in NQO1overexpressing breast cancer cells. Oncology Reports, 2019, 42( 4): 1621– 1630
77
C W Song, J J Chae, E K Choi, T S Hwang, C Kim, B U Lim, H J Park. Anti-cancer effect of bio-reductive drug β-lapachon is enhanced by activating NQO1 with heat shock. International Journal of Hyperthermia, 2008, 24( 2): 161– 169 https://doi.org/10.1080/02656730701781895
78
H J Park E K Choi J Choi K J Ahn E J Kim I M Ji Y H Kook S D Ahn B Williams R Griffin D A Boothman C K Lee C W Song. Heat-induced up-regulation of NAD(P)H:quinone oxidoreductase potentiates anticancer effects of β-lapachone . Clinical Cancer Research, 2005, 11(24 Pt 1): 8866- 8871
79
M Suzuki, M Amano, J Choi, H J Park, B W Williams, K Ono, C W Song. Synergistic effects of radiation and β-lapachone in DU-145 human prostate cancer cells in vitro. Radiation Research, 2006, 165( 5): 525– 531 https://doi.org/10.1667/RR3554.1
80
E K Choi, K Terai, I M Ji, Y H Kook, K H Park, E T Oh, R J Griffin, B U Lim, J S Kim, D S Lee, D A Boothman, M Loren, C W Song, H J Park. Upregulation of NAD(P)H:Quinone oxidoreductase by radiation potentiates the effect of bioreductive β-lapachone on cancer cells. Neoplasia, 2007, 9( 8): 634– 642 https://doi.org/10.1593/neo.07397
81
L S Li, S Reddy, Z H Lin, S Liu, H Park, S G Chun, W G Bornmann, J Thibodeaux, J Yan, G Chakrabarti, X J Xie, B D Sumer, D A Boothman, J S Yordy. NQO1-mediated tumor-selective lethality and radiosensitization for head and neck cancer. Molecular Cancer Therapeutics, 2016, 15( 7): 1757– 1767 https://doi.org/10.1158/1535-7163.MCT-15-0765
82
M J Lamberti, N B Vittar, C Da Silva Fde, V F Ferreira, V A Rivarola. Synergistic enhancement of antitumor effect of β-lapachone by photodynamic induction of quinone oxidoreductase (NQO1). Phytomedicine, 2013, 20( 11): 1007– 1012 https://doi.org/10.1016/j.phymed.2013.04.018
83
M J Lamberti, A B Morales Vasconsuelo, M Chiaramello, V F Ferreira, M Macedo Oliveira, S Baptista Ferreira, V A Rivarola, N B Rumie Vittar. NQO1 induction mediated by photodynamic therapy synergizes with β-lapachone-halogenated derivative against melanoma. Biomedicine and Pharmacotherapy, 2018, 108 : 1553– 1564 https://doi.org/10.1016/j.biopha.2018.09.159
84
N Nasongkla, A F Wiedmann, A Bruening, M Beman, D Ray, W G Bornmann, D A Boothman, J Gao. Enhancement of solubility and bioavailability of β-lapachone using cyclodextrin inclusion complexes. Pharmaceutical Research, 2003, 20( 10): 1626– 1633 https://doi.org/10.1023/A:1026143519395
85
E Blanco, E A Bey, C Khemtong, S G Yang, J Setti-Guthi, H Chen, C W Kessinger, K A Carnevale, W G Bornmann, D A Boothman, J Gao. β-Lapachone micellar nanotherapeutics for non-small cell lung cancer therapy. Cancer Research, 2010, 70( 10): 3896– 3904 https://doi.org/10.1158/0008-5472.CAN-09-3995
86
D Zhang, J Yang, J Guan, B Yang, S Zhang, M Sun, R Yang, T Zhang, R Zhang, Q Kan, H Zhang, Z He, L Shang, J Sun. In vivo tailor-made protein corona of a prodrug-based nanoassembly fabricated by redox dual-sensitive paclitaxel prodrug for the superselective treatment of breast cancer. Biomaterials Science, 2018, 6( 9): 2360– 2374 https://doi.org/10.1039/C8BM00548F
87
M Li, L Zhao, T Zhang, Y Shu, Z He, Y Ma, D Liu, Y Wang. Redox-sensitive prodrug nanoassemblies based on linoleic acid-modified docetaxel to resist breast cancers. Acta Pharmaceutica Sinica. B, 2019, 9( 2): 421– 432 https://doi.org/10.1016/j.apsb.2018.08.008
88
K Wang, B Yang, H Ye, X Zhang, H Song, X Wang, N Li, L Wei, Y Wang, H Zhang, Q Kan, Z He, D Wang, J Sun. Self-strengthened oxidation-responsive bioactivating prodrug nanosystem with sequential and synergistically facilitated drug release for treatment of breast cancer. ACS Applied Materials & Interfaces, 2019, 11( 21): 18914– 18922 https://doi.org/10.1021/acsami.9b03056
89
M Ganesan, G Kanimozhi, B Pradhapsingh, H A Khan, A S Alhomida, A Ekhzaimy, G R Brindha, N R Prasad. Phytochemicals reverse P-glycoprotein mediated multidrug resistance via signal transduction pathways. Biomedicine and Pharmacotherapy, 2021, 139 : 111632 https://doi.org/10.1016/j.biopha.2021.111632
90
Y Yan, C J Ochs, G K Such, J K Heath, E C Nice, F Caruso. Bypassing multidrug resistance in cancer cells with biodegradable polymer capsules. Advanced Materials, 2010, 22( 47): 5398– 5403 https://doi.org/10.1002/adma.201003162
91
L Che, Z Liu, D Wang, C Xu, C Zhang, J Meng, J Zheng, H Yuan, G Zhao, X Zhou. Computer-assisted engineering of programmed drug releasing multilayer nanomedicine via indomethacin-mediated ternary complex for therapy against a multidrug resistant tumor. Acta Biomaterialia, 2019, 97 : 461– 473 https://doi.org/10.1016/j.actbio.2019.07.033
92
N Chang, Y Zhao, N Ge, L Qian. A pH/ROS cascade-responsive and self-accelerating drug release nanosystem for the targeted treatment of multi-drug-resistant colon cancer. Drug Delivery, 2020, 27( 1): 1073– 1086 https://doi.org/10.1080/10717544.2020.1797238
93
Q Li, W Hou, M Li, H Ye, H Li, Z Wang. Ultrasound combined with core cross-linked nanosystem for enhancing penetration of doxorubicin prodrug/beta-lapachone into tumors. International Journal of Nanomedicine, 2020, 15 : 4825– 4845 https://doi.org/10.2147/IJN.S251277
94
M Ye, Y Han, J Tang, Y Piao, X Liu, Z Zhou, J Gao, J Rao, Y Shen. A tumor-specific cascade amplification drug release nanoparticle for overcoming multidrug resistance in cancers. Advanced Materials, 2017, 29( 38): 1702342 https://doi.org/10.1002/adma.201702342
95
Z Tang, H Zhang, Y Liu, D Ni, H Zhang, J Zhang, Z Yao, M He, J Shi, W Bu. Antiferromagnetic pyrite as the tumor microenvironment-mediated nanoplatform for self-enhanced tumor imaging and therapy. Advanced Materials, 2017, 29( 47): 1701683 https://doi.org/10.1002/adma.201701683
96
Y Dai, Z Yang, S Cheng, Z Wang, R Zhang, G Zhu, Z Wang, B C Yung, R Tian, O Jacobson, C Xu, Q Ni, J Song, X Sun, G Niu, X Chen. Toxic reactive oxygen species enhanced synergistic combination therapy by self-assembled metal-phenolic network nanoparticles. Advanced Materials, 2018, 30( 8): 1704877 https://doi.org/10.1002/adma.201704877
97
M Huo, L Wang, Y Chen, J Shi. Tumor-selective catalytic nanomedicine by nanocatalyst delivery. Nature Communications, 2017, 8( 1): 357 https://doi.org/10.1038/s41467-017-00424-8
98
M Liu, Y Xu, Y Zhao, Z Wang, D Shi. Hydroxyl radical-involved cancer therapy via fenton reactions. Frontiers of Chemical Science and Engineering, 2022, 16( 3): 345– 363 https://doi.org/10.1007/s11705-021-2077-3
99
M Zhang, X Qin, Z Zhao, Q Du, Q Li, Y Jiang, Y Luan. A self-amplifying nanodrug to manipulate the janus-faced nature of ferroptosis for tumor therapy. Nanoscale Horizons, 2022, 7( 2): 198– 210 https://doi.org/10.1039/D1NH00506E
100
Z Chen, J J Yin, Y T Zhou, Y Zhang, L Song, M Song, S Hu, N Gu. Dual enzyme-like activities of iron oxide nanoparticles and their implication for diminishing cytotoxicity. ACS Nano, 2012, 6( 5): 4001– 4012 https://doi.org/10.1021/nn300291r
101
L Gao, J Zhuang, L Nie, J Zhang, Y Zhang, N Gu, T Wang, J Feng, D Yang, S Perrett, X Yan. Intrinsic peroxidase-like activity of ferromagnetic nanoparticles. Nature Nanotechnology, 2007, 2( 9): 577– 583 https://doi.org/10.1038/nnano.2007.260
102
Q Chen, J Zhou, Z Chen, Q Luo, J Xu, G Song. Tumor-specific expansion of oxidative stress by glutathione depletion and use of a fenton nanoagent for enhanced chemodynamic therapy. ACS Applied Materials & Interfaces, 2019, 11( 34): 30551– 30565 https://doi.org/10.1021/acsami.9b09323
103
H Tian, M Zhang, G Jin, Y Jiang, Y Luan. Cu-MOF chemodynamic nanoplatform via modulating glutathione and H2O2 in tumor microenvironment for amplified cancer therapy. Journal of Colloid and Interface Science, 2021, 587 : 358– 366 https://doi.org/10.1016/j.jcis.2020.12.028
104
D Peer, J M Karp, S Hong, O C Farokhzad, R Margalit, R Langer. Nanocarriers as an emerging platform for cancer therapy. Nature Nanotechnology, 2007, 2( 12): 751– 760 https://doi.org/10.1038/nnano.2007.387
105
E E Connor, J Mwamuka, A Gole, C J Murphy, M D Wyatt. Gold nanoparticles are taken up by human cells but do not cause acute cytotoxicity. Small, 2005, 1( 3): 325– 327 https://doi.org/10.1002/smll.200400093
S Y Jeong, S J Park, S M Yoon, J Jung, H N Woo, S L Yi, S Y Song, H J Park, C Kim, J S Lee, J S Lee, E K Choi. Systemic delivery and preclinical evaluation of Au nanoparticle containing beta-lapachone for radiosensitization. Journal of Controlled Release, 2009, 139( 3): 239– 245 https://doi.org/10.1016/j.jconrel.2009.07.007
108
E A Bey, M S Bentle, K E Reinicke, Y Dong, C R Yang, L Girard, J D Minna, W G Bornmann, J Gao, D A Boothman. An NQO1- and PARP-1-mediated cell death pathway induced in non-small-cell lung cancer cells by β-lapachone. Proceedings of the National Academy of Sciences of the United States of America, 2007, 104( 28): 11832– 11837 https://doi.org/10.1073/pnas.0702176104
109
X Huang, E A Motea, Z R Moore, J Yao, Y Dong, G Chakrabarti, J A Kilgore, M A Silvers, P L Patidar, A Cholka, F Fattah, Y Cha, G G Anderson, R Kusko, M Peyton, J Yan, X J Xie, V Sarode, N S Williams, J D Minna, M Beg, D E Gerber, E A Bey, D A Boothman. Leveraging an NQO1 bioactivatable drug for tumor-selective use of poly(ADP-ribose) polymerase inhibitors. Cancer Cell, 2016, 30( 6): 940– 952 https://doi.org/10.1016/j.ccell.2016.11.006
110
L Zhou, J Chen, Y Sun, K Chai, Z Zhu, C Wang, M Chen, W Han, X Hu, R Li, T Yao, H Li, C Dong, S Shi. A self-amplified nanocatalytic system for achieving “1 + 1 + 1 > 3” chemodynamic therapy on triple negative breast cancer. Journal of Nanobiotechnology, 2021, 19( 1): 261 https://doi.org/10.1186/s12951-021-00998-y
111
L Zhang, Z Chen, K Yang, C Liu, J Gao, F Qian. β-Lapachone and paclitaxel combination micelles with improved drug encapsulation and therapeutic synergy as novel nanotherapeutics for NQO1-targeted cancer therapy. Molecular Pharmaceutics, 2015, 12( 11): 3999– 4010 https://doi.org/10.1021/acs.molpharmaceut.5b00448
112
X Li, X Jia, H Niu. Nanostructured lipid carriers co-delivering lapachone and doxorubicin for overcoming multidrug resistance in breast cancer therapy. International Journal of Nanomedicine, 2018, 13 : 4107– 4119 https://doi.org/10.2147/IJN.S163929
113
X Dong, H J Liu, H Y Feng, S C Yang, X L Liu, X Lai, Q Lu, J F Lovell, H Z Chen, C Fang. Enhanced drug delivery by nanoscale integration of a nitric oxide donor to induce tumor collagen depletion. Nano Letters, 2019, 19( 2): 997– 1008 https://doi.org/10.1021/acs.nanolett.8b04236
114
C Chu, X Lyu, Z Wang, H Jin, S Lu, D Xing, X Hu. Cocktail polyprodrug nanoparticles concurrently release cisplatin and peroxynitrite-generating nitric oxide in cisplatin-resistant cancers. Chemical Engineering Journal, 2020, 402 : 126125 https://doi.org/10.1016/j.cej.2020.126125
115
K Zhang, H Xu, X Jia, Y Chen, M Ma, L Sun, H Chen. Ultrasound-triggered nitric oxide release platform based on energy transformation for targeted inhibition of pancreatic tumor. ACS Nano, 2016, 10( 12): 10816– 10828 https://doi.org/10.1021/acsnano.6b04921
116
M Wan, H Chen, Q Wang, Q Niu, P Xu, Y Yu, T Zhu, C Mao, J Shen. Bio-inspired nitric-oxide-driven nanomotor. Nature Communications, 2019, 10( 1): 966 https://doi.org/10.1038/s41467-019-08670-8
117
L Qin, H Gao. The application of nitric oxide delivery in nanoparticle-based tumor targeting drug delivery and treatment. Asian Journal of Pharmaceutical Sciences, 2019, 14( 4): 380– 390 https://doi.org/10.1016/j.ajps.2018.10.005
118
L B Vong, Y Nagasaki. Nitric oxide nano-delivery systems for cancer therapeutics: advances and challenges. Antioxidants, 2020, 9( 9): 791 https://doi.org/10.3390/antiox9090791
119
J An, Y G Hu, C Li, X L Hou, K Cheng, B Zhang, R Y Zhang, D Y Li, S J Liu, B Liu, D Zhu, Y D Zhao. A pH/ultrasound dual-response biomimetic nanoplatform for nitric oxide gas-sonodynamic combined therapy and repeated ultrasound for relieving hypoxia. Biomaterials, 2020, 230 : 119636 https://doi.org/10.1016/j.biomaterials.2019.119636
120
Z Yuan, C Lin, Y He, B Tao, M Chen, J Zhang, P Liu, K Cai. Near-infrared light-triggered nitric-oxide-enhanced photodynamic therapy and low-temperature photothermal therapy for biofilm elimination. ACS Nano, 2020, 14( 3): 3546– 3562 https://doi.org/10.1021/acsnano.9b09871
121
M Shi, J Zhang, Y Wang, C Peng, H Hu, M Qiao, X Zhao, D Chen. Tumor-specific nitric oxide generator to amplify peroxynitrite based on highly penetrable nanoparticles for metastasis inhibition and enhanced cancer therapy. Biomaterials, 2022, 283 : 121448 https://doi.org/10.1016/j.biomaterials.2022.121448
122
J Lee, E T Oh, H Yoon, C W Kim, Y Han, J Song, H Jang, H J Park, C Kim. Mesoporous nanocarriers with a stimulus-responsive cyclodextrin gatekeeper for targeting tumor hypoxia. Nanoscale, 2017, 9( 20): 6901– 6909 https://doi.org/10.1039/C7NR00808B
123
S R Gayam, P Venkatesan, Y M Sung, S Y Sung, S H Hu, H Y Hsu, S P Wu. An NAD(P)H:quinone oxidoreductase 1 (NQO1) enzyme responsive nanocarrier based on mesoporous silica nanoparticles for tumor targeted drug delivery in vitro and in vivo. Nanoscale, 2016, 8( 24): 12307– 12317 https://doi.org/10.1039/C6NR03525F
