Melanin and Melanin-Functionalized Nanoparticles as Promising Tools in Cancer Research—A Review
Abstract
:Simple Summary
Abstract
1. Introduction
2. Human Melanogenesis in a Nutshell
3. Therapeutic Properties
3.1. Antioxidant Effect
3.2. Photoprotective Capacity
3.3. Anti-Inflammatory Properties
3.4. Anticancer Activity
4. Melanin-Based Targeted Cancer Therapy
4.1. Melanin Targeting in Cancer Therapy
4.2. Melanin Nanoparticles (MEL-NPs) in Cancer Therapy
4.2.1. Synthesis of MEL-NPs
4.2.2. Applications of MEL-NPs in Cancer Therapy
Chemotherapy
Radio(pharmaceutical) Therapy
Phototherapy
Immunotherapy
Gene Therapy
Cancer Detection and Bio-Imaging
Nanotheranostics
4.2.3. Biosafety and Metabolism of MEL-NPs
5. Concluding Remarks and Future Perspectives
Author Contributions
Funding
Conflicts of Interest
References
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Source | Effect | Observations | Tested Concentrations | Reference |
---|---|---|---|---|
Fungal melanin from Aspergillus nidulans | Antioxidant | inhibition of 5-thio-2-nitrobenzoic acid (TNB) oxidation; scavenging activity on the tested oxidants (i.e., H2O2 and HOCl) | 25, 50, and 100 µg/mL (in vitro) | [46] |
Melanin from the muscles of Gallus domesticus Brisson | Antioxidant | concentration-dependent scavenging of DPPH and superoxide radicals; inhibition of lipid peroxidation | 20–3000 µg/mL (in vitro) | [47] |
Bacterial melanin from Streptomyces glaucescens NEAE-H | Antioxidant Anticancer Anti-hemolytic | scavenging and neutralization of ABTS radical; ↑ mortality and cytotoxicity in HFB4 skin cancer cells; neutralization of free radicals and protection of erythrocytes from membrane destruction/lysis | 1.56–100 µg/mL; IC50 = 16.34 ± 1.31 µg/mL (in vitro) | [48] |
Bacterial melanin from Pseudomonas maltophilia AT18 | Photoprotective | ↑ viability of normal fibroblasts (NL-FB) post-UVA irradiation; inhibition of UVA-induced apoptosis; suppression of intracellular ROS generated by UVA | 25–800 µg/mL (in vitro) | [49] |
Bacterial melanin from Pseudomonas otitidis DDB2 | Photoprotective | protection of NIH 3T3 mouse fibroblasts against UVB radiation; scavenging of ROS generated upon UVB irradiation | 15.625–500 µg/mL (in vitro) | [50] |
Herbal melanin from Nigella sativa seed coats | Immunomodulatory | ↑ TNF-α, IL-6, and VEGF mRNA expression in human monocytic THP-1 cells and peripheral blood mononuclear cells (PBMC) | 50 and 100 µg/mL (in vitro) | [51] |
Immunomodulatory | ↑ IL-8 expression and production in human monocytic THP-1 cells and peripheral blood mono- nuclear cells (PBMC) | 5–50 µg/mL (in vitro) | [52] | |
Anticancer | ↓ cell viability; ↑ generation of cellular ROS; apoptosis induction; ↓ Bcl-2 expression; ↑ Bad expression; ↑ cytochrome c expression; activation of caspase-3 and -7; ↑ JNK, cJun and ATF2 phosphorylation; ↓ ERK phosphorylation in HT-29 and SW620 colorectal adenocarcinoma cells | 5–200 µg/mL (in vitro) | [53] | |
Anticancer | ↓ cell viability; cell growth arrest in G0/G1 and G2 phases; ↑ TLR4 protein expression; apoptosis induction in human acute monocytic leukemia THP-1 and human embryonic kidney HEK293 cells | 7.8–500 µg/mL (in vitro) | [54] | |
B16F10 melanoma tumor lysates containing melanin (microneedle patch) | Anticancer | Melanin-mediated heat generation; promotion of tumor-antigen uptake by dendritic cells; ↑ antitumor vaccination against B16F10 tumors; complete tumor remission in BRAFV600E-mutated BP melanoma- and 4T1 breast carcinoma-bearing mice | around 50 µg of melanin/patch (in vivo) | [55] |
Synthetic melanin | Immunomodulatory | ↑ CD8+ T-cell responses and inhibition of tumor growth in BALB/c mice; ↑ efficiency of melanin as adjuvant in anticancer vaccines | 0.5 μg of melanin bound to the gp100 epitope (gp100-melanin) (in vivo) | [56] |
Application | Melanin Nanoplatform Type | Cancer Type | Observations | Concentration/Dosage | Reference |
---|---|---|---|---|---|
Chemotherapy | Doxorubicin-loaded MEL-NPs | Thyroid cancer | Chelating of doxorubicin (DOX) through π-π stacking and hydrogen bonding; ↓ viability of HTh74 and HTh74R thyroid cancer cells; ↑ therapeutic efficacy and cell internalization compared to free doxorubicin. | 10, 20, 40, 80, 160 mg/L (in vitro) | [98] |
PDA-coated and alendronate-grafted paclitaxel (PTX) nanoparticles | Osteosarcoma | Targeted cancer treatment; sustained drug release; ↑ cytotoxicity against K7M2 wt osteosarcoma cells; ↑ accumulation in tumor, and ↓ side effects of PTX in K7M2 wt tumor-bearing mice | 1, 5, 10, 50, 100 µg/mL (in vitro) 8 mg/kg equivalent concentrations of PTX (in vivo) | [99] | |
PTX-loaded trastuzumab-decorated PDA-NPs (PDA NPs•Tmab@PTX) | Breast cancer | ↓ viability of BT474, SKBR3, and HS5 cells HER2+ breast cancer cells; ↑ number of early apoptotic HER2+ breast cancer cells BT474; disintegration and ↓ viability BT474 spheroids | 0.035, and 0.042 mg/mL (2D in vitro model) 0.035 mg/mL (3D in vitro model) | [100] | |
RGD-modified polydopamine-paclitaxel-loaded poly (3-hydroxybutyrate-co-3-hydroxyvalerate) nanoparticles | Hepatocellular carcinoma | ↓ cytotoxicity against L02 of PTX-free NPs; ↓ viability of HepG2 and SMMC-7721 cells; ↑ inhibitory effect on HepG2 and SMMC-7721 cell proliferation compared to free PTX; ↑ cellular uptake in HepG2 cells; ↑ PTX release at pH values of 5.0–6.5; ↓ tumor volume and weight in HepG2 tumor-bearing mice | 0.1, 0.5, 1, 2.5, 5, 10 µg/mL (in vitro) 4 mg/kg (in vivo) | [101] | |
Doxorubicin-loaded polyethylene glycol functionalized MEL-NPs | Breast cancer | Sustained and extended release of doxorubicin; ↓ proliferation of MDA-MB-231 breast cancer cells; | 0.125, 0.250, 0.500 mg (in vitro) | [102] | |
Curcumin-loaded silver-decorated melanin-like polydopamine/mesoporous silica composites | Cervical and Taxol-resistant non-small cell lung cancers | ↓ hemolytic activity and biocompatibility; pH- and ROS-responsive release of curcumin; prolonged inhibition of Escherichia coli and Staphylococcus aureus bacterial growth; ↑ chemotherapeutic efficiency against HeLa (human cervical) and A549/TAX (Taxol-resistant non-small cell lung) cancer cells compared to free curcumin. | ≤ 500 µg/mL (in vitro) | [103] | |
Gambogenic acid-loaded functional polydopamine nanoparticles (GNA@PDA-FA SA NPs) | Breast cancer | ↓ 4T1 (breast cancer cells) cell viability; ↓ IC50 value compared to raw GNA; ↑ targeting effect of GNA against 4T1 cells; inhibition of tumor growth in 4T1 xenograft-bearing BALB/C mice | 0.78–310 µM (in vitro) 24 mg/kg (in vivo) | [104] | |
Iron-chelated doxorubicin-loaded folic acid-conjugated polyethylene glycol (PEG)-coated polydopamine nanoparticles (DOX@Fe-PDA/FA-PEG NPs) | Breast cancer | ↑ pH responsiveness of the PDA-modified NPs and pH-dependent release of DOX; ↑ DOX release under acidic conditions; sustained DOX release; ↑ cell uptake compared to free DOX; ↓ MCF7 (breast cancer cells) cell viability; ↑ intracellular ROS in MCF7 cells | 0.1093–3.5 µg/mL (in vitro) | [105] | |
Doxorubicin-loaded polyethylene glycol-modified polydopamine nanoparticles (PDA-PEG-DOX) | Breast cancer | ↓ MDA-MB-231 (breast cancer cells) cell viability; ↓ pro-caspase 3 expression level; accumulation within the MDA-MB-231 cell nucleus and lysosomes; ↓ mitochondrial membrane potential | 0.5, 1, and 5 µg/mL (in vitro) | [106] | |
Doxorubicin-loaded triphenylphosphonium- functionalized polyethylene glycol-modified polydopamine nanoparticles (PDA-PEG-TPP-DOX) | Breast cancer | ↓ MDA-MB-231 cell viability; ↓ pro-caspase 3 expression level; ↓ mitochondrial membrane potential; mitochondria-targeted anticancer effect; ↓ long-term drug resistance. | 0.5, 1, and 5 µg/mL (in vitro) | [106] | |
Radio (pharmaceutical) Therapy | Melanin-covered silica nanoparticles (MNs) | - | ↓ hematologic toxicity in mice exposed to external gamma radiation and radioimmunotherapy | 50 mg/kg (in vivo) | [107] |
Melanin nanoparticles (MNPs) | - | ↓ gamma radiation-induced cytotoxicity in Chinese hamster ovary cells | 6.25, 12.5, 25 and 50 µg/mL (in vitro) | [108] | |
131I-labeled PEGylated polydopamine nanoparticles loaded with sanguinarine and metformin (131I-PDA- PEG-SAN-MET) | Breast cancer | ↓ 4T1 cell viability; induction of 4T1 cell apoptosis; relieved tumor hypoxia in 4T1 tumor-bearing nude mice. | NPs containing 4 mg/kg of SAN, 8 mg/kg of MET, 200 mCi of 131I (in vivo) | [109] | |
PEGylated polydopamine nanoparticles loaded with 131I and DOX (131I-PDA-PEG/DOX) | Breast cancer | ↓ 4T1 cell viability; ↑ cellular 131I uptake delivered by PDA-PEG; inhibited tumor growth, reduced tumor size, and prolonged survival rate in BALB/c mice bearing 4T1 xenografts. | 10 mg/kg of PDA-PEG, 20 mCi of 131I (in vivo) | [110] | |
Phototherapy | Arginine-doped synthetic melanin nanoparticles (SMNPs) | Breast cancer | ↑ photothermal efficiency following arginine introduction within the PDA structures of SMNPs; ↓ 4T1 cell viability; ↓ tumor volume and weight in 4T1 xenograft-bearing female BALB/c nude mice. | 12.5, 25, 50, 100, 200 μg/mL (in vitro) 10.0 and 20.0 mg/kg (in vivo) | [111] |
RGD- and beclin 1-modified and PEGylated MEL-NPs | Anticancer | Induced autophagy and cytotoxicity; ↓ cell viability upon NIR irradiation in cancer cells; tumor regression in BALB/c nude mice at 43 °C | 50 μg/mL (in vitro) 34 mg/kg (in vivo) | [112] | |
Cisplatin prodrug Pt (IV) MEL-NPs | Prostate cancer | ↓ viability of PC3, DU145, and LNCaP prostate cancer cells; induction of mitochondrial membrane depolarization in PC3 cells; ↑ cell uptake ability; synergistic photothermal therapy and chemotherapy properties; potent photothermal conversion efficiency (29.6%); biocompatibility; prolonged the blood circulation time and ↓ tumor growth in BALB/c mice. | 10, 20, 30 µM (in vitro) 200 µL (in vivo) | [113] | |
Gemcitabine-loaded dual-functional melanin-based nanoliposomes | Pancreatic cancer | Synergistic antitumor effect between melanin and gemcitabine; ↑ therapeutic efficiency; potent conversion of NIR light into thermal energy in the presence of MEL; photothermal conversion efficiency of MEL uninfluenced by liposomal encapsulation and drug loading; ↓ cell viability of BxPC-3 pancreatic cancer cells; controlled and enhanced drug release to the tumor sites via hyperthermia; no systemic toxicity to BxPC-3 tumor-bearing mice | 50 mg/kg (in vivo) | [114] | |
Docetaxel-loaded polydopamine-functionalized CA-(PCL-ran-PLA) nanoparticles | Breast cancer | ↑ drug loading content, and encapsulation efficiency; effective target delivery of drugs to tumor sites by incorporating AS1411 aptamers; synergistic chemo-photothermal effect; ↓ proliferation of MCF-7 breast cancer cells; ↑ survival time, and ↓ side effects in mice; ↓ tumor volume in vivo | 0.25–25 μg/mL (in vitro) 10 mg/kg (in vivo) | [115] | |
PDA/transferrin hybrid NPs | Malignant melanoma | ↑ apoptosis when associated with UV irradiation in B16F10 mouse melanoma cells, J774A.1 mouse macrophages, and in an organotypic melanoma spheroid model; lack of cytotoxicity or proliferation impairment of PDA-NPs in B16F10 and J774A.1; | 5–160 µg/mL (in vitro) | [116] | |
Hyaluronic acid-decorated polydopamine nanoparticles with conjugated chlorin e6 (HA–PDA–Ce6) | Colorectal carcinoma | ↓ dark toxicity; ↑ photodynamic and photothermal activities upon laser illumination; ↑ uptake and penetration in vitro and in vivo; ↑ cytotoxicity and apoptosis in HCT-116 cells following the combined laser treatment; inhibited tumor growth in HCT-116 tumor-bearing mice. | IC50 = 33.07 ± 12.92 μg/mL (in vitro) 0.65 mg/kg (in vivo) | [117] | |
Epirubicin-hybrid polydopamine nanoparticles (E/PCF-NPs) | Breast cancer | pH sensitive drug release; ↑ cytotoxicity against 4T1 cells; inhibited survival rate and induced cell apoptosis 4T1 cells; ↑ ROS generation; ↓ NAD+/NADH; complete tumor regression in 4T1 tumor-bearing mice | IC50 = 1.3 ± 0.2 μg/mL (in vitro) 5 mg/kg drug dose (in vivo) | [118] | |
Folate-modified PDA nanoparticles loaded with a cationic phthalocyanine-type photosensitizer (PDA-FA-Pc) | Breast cancer Cervical cancer | Non-measurable toxicity of PDA-FA-Pc without illumination; ↓ dose-dependent survival rate of MCF-7, HeLa, HELF, and L02 cells following illumination; ↑ cytotoxicity against tumor cells (MCF-7, HeLa) compared to healthy cells (HELF, L02); ↓ tumor volume and weight in MCF-7 and HeLa xenograft-bearing female Kunming mice. | 0.15, 0.3, 0.6, 1.2 and 2.4 mg/mL (in vitro) 43.5 mg/kg (in vivo) | [119] | |
Chlorin e6-conjugated PDA nanospheres | Hepatocellular carcinoma | Simultaneous PTT and PDT therapy; ↑ internalization within HepG2 cells; ↓ cell viability of HepG2 cells; tumor regression in HepG2 tumor-bearing male BALB/c-nude mice | Ce6 concentration 0.1–8 μg/mL (in vitro) 20 μg/mL PDA and 5 μg/mL Ce6 (in vivo) | [120] | |
PDA nanoparticles carrying tumor cell lysate (TLC) (TCL@PDA NPs) | Delayed cancer progression in tumor-bearing mice; ↑ antigen uptake, BMDCs (bone-marrow-derived dendritic cells) maturation, and Th1-related cytokines secretion; ↑ CD4+ and CD8+ T cells; delayed tumor development by empty PDA-NPs | 300 μg TLC | [121] | ||
Immunotherapy | Polydopamine-coated mesoporous silica nanoparticles containing thiolated ovalbumin and ammonium bicarbonate (MSNs-ABC@PDA-OVA) | Malignant melanoma | Rapid antigen release and endosome escape under laser illumination; ↑ activation and maturation of dendritic cells; antigen specific CD8+ and Th1 CD4+ T cell responses; melanoma eradication with a cure rate of 75%; strong immunological memory; inhibition of tumor recurrence and metastasis in C57BL/6 mice. | 25 µg OVA/mouse (in vivo) | [122] |
Antigen-ovalbumin-loaded polydopamine nanoparticles (OVA@Pdop-NPs) | Colon cancer | Lack of cytotoxicity and ↑ cellular uptake in bone marrow-derived dendritic cells (BMDCs); ↑ maturation of dendritic cells; ↑ expression of major histocompatibility complex, costimulatory molecules, and cytokines; activation of OVA-specific cytotoxic CD8+ T cells; ↑ production of memory CD4+ and CD8+ T cells; ↓ tumor growth in OVA-MC38 colon tumor-bearing mice | 0.5–100 μg/mL (in vitro) 100 μg/mice OVA content (in vivo) | [123] | |
Natural melanin nanoparticles coated with cancer cell membrane (M@C NPs) | Breast cancer | ↑ antitumor activity; ↑ levels of CD8+ T cells and cytokines; ↑ 4T1 cell cytotoxicity and ↓ cell invasion under laser radiation; ↑ expression of calreticulin proteins under irradiation suggesting immunogenic cell death of 4T1 cells; ↑ tumor targeting ability, ↓ levels of IL- 12 and IL-6, and synergistic effect with immunoblocking inhibitors (IDOi) leading to ↓ tumor volume and growth in mice. | ≤ 1000 μg/mL (in vitro) | [124] | |
Gene Therapy | pH-responsive polydopamine nanoparticles modified with polyethylenimine and polyethylene glycol-phenylboronic acid (PDANP-PEI-rPEG) | Hepatocellular carcinoma (in vitro) Malignant melanoma (in vivo) | Stability to physiological pH (7.4); ↑ gene transfection levels; ↑ photothermal conversion ability; quick endosomal escape; | 0.4–1.5 mass ratio PDANP to DNA (in vitro) 50 μL (in vivo) | [125] |
DNA-polydopamine-MnO2 nanocomplex (DP-PM) | Breast cancer | ↓ viability of MCF7 cells; ↓ tumor volume and weight in MCF7 xenograft-bearing BALB/c nude mice; glutathione-triggered release of Mn2+ to activate intracytoplasmic DNAzyme ↑ Egr-1 mRNA cleavage activity of DNAzyme and ↓ of Egr-1 protein in tumor cells; synergistic tumor ablation upon NIR irradiation. | 5–50 μg/mL (in vitro) | [126] | |
Polyethylenimine-modified polydopamine nanoparticles (PPNPs) | Hepatocellular carcinoma | ↓ cytotoxicity to HepG2 cells; ↑ gene transfection levels compared to Lipofectamine 2000 at mass ratios of 23 and 30; tripled gene transfection levels following NIR irradiation; lack of hemolytic effect. | 10–30 mass ratio PPNPs to DNA (in vitro) | [127] | |
Cancer Detection and Bio-Imaging | Mesoporous polydopamine carrying sorafenib and SPIO nanoparticles (SRF@MPDA-SPIO NPs) | Hepatocellular carcinoma | ↑ MRI contrast; ↑ R2 (1/T2) values; MRI-guided ferroptosis; responsive release of ferric ions and sorafenib to stimuli (pH, temperature); effectively conversion ability of NIR light; reduced tumor volume and weight in HCT-116 tumor-bearing mice | 100 μL (in vivo) | [128] |
Ions (Fe3+, Bi3+, I+)-doped melanin nanoparticles conjugated with EGFR antibody (iMNPs) | Hepatocellular carcinoma | ↑ contrast intensity in T1-w MRI and CT; specific targeting of EGFR-overexpressed HepG2 cells observed by MRI and CT imaging; ↑ contrast of MRI/CT/SPECT images in xenograft-bearing-mice | 200 μL (in vivo) | [129] | |
Nanotheranostics | PDA-based theranostic nanoprobe loaded with fluorescein isothiocyanate (FITC)-labeled hairpin DNA (hpDNA) and doxorubicin | Breast cancer | ↓ viability of 4T1 breast cancer cells; real-time detection of the dynamic expression of specific miRNAs; ↓ tumor volume in 4T1 xenograft-bearing male BALB/c-nu mice | 2.5, 5, 10, 20 μg/mL of doxorubicin (in vitro) | [130] |
Cu (II)-doped polydopamine-coated gold nanorods | Squamous cell carcinoma | ↑ physiological stability, biocompatibility, photothermal performance, and blood circulation time; computer tomography imaging and magnetic resonance imaging functions; ↓ tumor volume and weight; lack of short-term toxicity against liver and renal functions in BALB/c mice | 25–500 µg/mL (in vitro) 50 μL of 5 mg/mL (in vivo) | [131] | |
Mn2+ -coordinated PDA-modified doxorubicin-loaded poly (lactic- co-glycolic acid) (PLGA) NPs | Colon cancer | ↑ permeability and retention; ↑ ability of NIR photothermal transduction in vitro and in vivo; chemo-photothermal synergistic effect; ↑ DOX release; ↓ viability of CT26 murine colorectal carcinoma cells; stronger efficacy in killing cancer cells under NIR irradiation; efficient cellular uptake; ↓ tumor growth in CT26 tumor-bearing mice; no acute side effects in vivo | ≤ 200 µg/mL (in vitro) 20 mg/kg (in vivo) | [132] |
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Marcovici, I.; Coricovac, D.; Pinzaru, I.; Macasoi, I.G.; Popescu, R.; Chioibas, R.; Zupko, I.; Dehelean, C.A. Melanin and Melanin-Functionalized Nanoparticles as Promising Tools in Cancer Research—A Review. Cancers 2022, 14, 1838. https://doi.org/10.3390/cancers14071838
Marcovici I, Coricovac D, Pinzaru I, Macasoi IG, Popescu R, Chioibas R, Zupko I, Dehelean CA. Melanin and Melanin-Functionalized Nanoparticles as Promising Tools in Cancer Research—A Review. Cancers. 2022; 14(7):1838. https://doi.org/10.3390/cancers14071838
Chicago/Turabian StyleMarcovici, Iasmina, Dorina Coricovac, Iulia Pinzaru, Ioana Gabriela Macasoi, Roxana Popescu, Raul Chioibas, Istvan Zupko, and Cristina Adriana Dehelean. 2022. "Melanin and Melanin-Functionalized Nanoparticles as Promising Tools in Cancer Research—A Review" Cancers 14, no. 7: 1838. https://doi.org/10.3390/cancers14071838