Active Targeted Nanoformulations via Folate Receptors: State of the Art and Future Perspectives
Abstract
:1. Introduction
2. Folic Acid-Targeted Chemotherapy
2.1. Folic Acid Conjugated Nanomedicines
2.1.1. Folic Acid-Cytotoxic Drug Conjugates
2.1.2. Folic Acid-Functionalized Nanoparticles
2.2. Anti-FR-Monoclonal Antibody-Coupled Nanoformulations
2.2.1. Anti-FR-Monoclonal Antibody-Drug Conjugates
2.2.2. Anti-FR-Monoclonal Antibody-Functionalized Nanoparticles
Formulation | Cancer type/Activity | Stage | Reference | ||
---|---|---|---|---|---|
Folic acid conjugated nanomedicines | Folic acid-cytotoxic drug conjugates | Folic acid-maytansinoid conjugates | Marked antiproliferative effect in ovarian, colon, nasopharyngeal carcinoma, lung, and cervical cancer (FR positive). No-activity in melanoma and breast cancer (FR negative) | Pre-clinical | [27,28] |
Folic acid-5-fluorouracil conjugates | Antitumor effect in colon cancer that overexpresses FRs | Pre-clinical | [30] | ||
Folic acid-methotrexate-arabinogalactan conjugates | Cytotoxic effect in leukemia models | Pre-clinical | [31] | ||
Folic acid-SB-T-1214 conjugates | Cytotoxic effect in blood, breast, and ovarian carcinomas overexpressing FRs. | Pre-clinical | [32] | ||
Folic acid-mitomicyn conjugates | Cytotoxic activity in lung adenocarcinoma models that overexpress FR | Pre-clinical | [33] | ||
Folic acid-bleomicyn conjugates | Cytotoxic effect in ovarian cancer (FR positive) | Pre-clinical | [34] | ||
Folic acid-camptothecin conjugates | Cytotoxic effect in FR positive cancer cells of the mouth | Pre-clinical | [37] | ||
Folic acid-polyethylene glycol-rhaponticin conjugates | Potent cytotoxic effect in FR positive epithelial and KB cancer cells. No-activity in FR-negative breast cancer cells | Pre-clinical | [38] | ||
Folic acid conjugated to a vinca alkaloid | Potent effect in ovarian cancer models (FR positive). This formulation is under clinical research | Clinical trial | [39] | ||
Folic acid conjugated to solubilizing peptide moiety (BMS-753493) | Phase I clinical studies in ovarian, colorectal, lung, and mammary tumors overexpressing FRs. An objetive anticancer response was not detected. | Clinical trial | [76] | ||
Folic acid conjugated to tubulysin (EC-1456) | Potent cytotoxic effect in vintafolide resistant FR-positive KB cancer cells. Phase I clinical studies in non-small lung cancer and ovarian cancer | Clinical trial | [77] | ||
Folic acid-Paclitaxel conjugates | No higher effect compared with unconjugated drugs in colon cancer cells that overexpress FR | Pre-clinical | [40] | ||
Folic acid-polyethylene glycol-cisplatin conjugates | No higher effect compared with unconjugated drugs in lung cancer cells that overexpress FR. However, a higher uptake was detected | Pre-clinical | [41] | ||
Folic acidfunctionalized nanoparticles | Folic acid-coated pH-sensitive liposomes loaded with doxorubicin | Cytotoxic effect in breast cancer models (FR positive) | Pre-clinical | [45] | |
Folic acid-coated pH-sensitive liposomes loaded with paclitaxel | Pre-clinical | [46,47] | |||
Folic acid-coated non-pH-sensitive liposomes loaded with doxorubicin | Pre-clinical | [49] | |||
Folic acid-coated silica mesoporous nanoparticles loaded with topotecan | Cytotoxic effect in retina cancer models (FR positive) | Pre-clinical | [52] | ||
Folic acid-coated silica mesoporous nanoparticles loaded with cisplatin | Cytotoxic effect in cervical cancer models (FR positive) | Pre-clinical | [51] | ||
Folic acid-coated silica mesoporous nanoparticles loaded with doxorubicin | Pre-clinical | [50] | |||
Folic acid-coated Poly(lactic-co-glycolic acid) nanoparticles loaded with cisplatin | Pre-clinical | [53] | |||
Folic acid-Alendronate-coated Poly(lactic-co-glycolic acid) nanoparticles loaded with paclitaxel | Cytotoxic effect in non-small lung cancer overexpressing FR | Pre-clinical | [54] | ||
Folic acid-coated Poly(lactic-co-glycolic acid) nanoparticles loaded with paclitaxel and cisplatin | Non-coated and folic acid coated nanoparticles showed a similar tumor growth inhibition in FR-positive lung tumo models developed in mice | Pre-clinical | [55] | ||
Folic acid-functionalized iron oxide condensed colloidal magnetic clusters containing doxorubicin | Cytotoxic activity in FR-positive triple-negative breast cancer | Pre-clinical | [56] | ||
Folic acid-functionalized iron oxide nanoparticles | Cytotoxic activity in FR-positive cervical cancer | Pre-clinical | [57] | ||
Folic acid-coated liposomes loaded with BIM-S plasmid | Anticancer effect in non-small lung cancer. The formulations were designed for tumor associated macrophages | Pre-clinical | [61] | ||
Folic acid-functionalized-liposomes loaded with doxycycline | Pre-clinical | [63] | |||
Folic acid-coated chitosan nanoparticles loaded with signaling transducers and activators of transcription 3 | Anticancer effect in Lewis lung adenocarcinoma. The formulations were designed for tumor associated macrophages | Pre-clinical | [64] | ||
Anti-FR-monoclonal antibodies coupled nanoformulations | Antibody- drugconjugates | Farletuzumab conjugated with eribulin | Anticancer effect in non-small lung cancer overexpressing FR | Clinical trial | [68] |
Anti-FRα-monoclonal antibody-maytansinoid conjugate (mirvetuximab soravtansine) | Higher anticancer activity in ovarian and non-small lung carcinomas overexpressing FRα. Several clinical trials are ongoing to evaluate its efficacy as monotherapy or in combination with chemo and other immmunotherapeutic drugs in ovarian cancer patients | Clinical trial | [69,70,71,72,73,74] | ||
FR-targeted-nanoparticles | Antibody-conjugated gold-coated magnetite nanoparticles | Anticancer effect in triple-negative breast cancer overexpressing FR | Pre -clinical | [75] |
3. Folic Acid-Targeted Nanoformulations in Inflammatory Diseases
3.1. FR-Targeted Nanoformulations in Rheumatoid Arthritis
3.1.1. Folic Acid-Coated Nanoparticles
Formulation | Disease | Stage | References | |
---|---|---|---|---|
Folic acid coated nanoparticles | Folic acid-functionalized liposomes loaded with methotrexate | Rheumatoid arthritis | Pre-clinical | [81] |
Folic acid-functionalized lipid—polymeric nanoparticles loaded with methotrexate | Pre-clinical | [82] | ||
Folic acid-coated double liposomes loaded with both methrotrexate and prednisolone | Pre-clinical | [83] | ||
Folic acid-conjugated dendrimers loaded with methotrexate | Pre-clinical | [84] | ||
Folic acid-functionalized mesoporous silica-coated-gold nanoparticles loaded with methotrexate | Pre-clinical | [86] | ||
Folic acid-coated albumin nanoparticles loaded with etoricoxib | Pre-clinical | [87] | ||
Folic acid-coated pH-sensitive polyethylene glycol-chitosan-based nanoparticles loaded with methotrexate | Pre-clinical | [88] | ||
Anti FRβ monoclonal antibody coated formulations | Anti-FRβ antibody-functionalized Cholesterol grafted chitosan nanoparticles loaded with methotrexate | Pre-clinical | [89] | |
Folic acid coated nanoparticles | Folic acid-coated poly(lactic-co-glycolic acid) nanoparticles loaded with resveratrol | Ulcerative Colitis | Pre-clinical | [90] |
3.1.2. Anti-FRβ Monoclonal Antibody-Coated Nanoformulations
3.2. FR-Targeted-Nanoformulations in Inflammatory Bowel Disorders
4. FR-Targeted Nanoparticles to Cross the Blood–Brain Barrier
5. FR-Targeted Formulations as Imaging Strategy
5.1. Cancer Disease
5.2. Inflammatory Diseases
Formulation Type | Composition | Indication | Imaging Technique | Stage | Reference | |
---|---|---|---|---|---|---|
Cancer | Radiolabeled FR ligands | Etarfolatide® [99mTc]Tc-EC20 | Identification of tumors overexpressing FRs to predict when treatment with FR-targeted therapies is a good strategy This formulation is under clinical research. | PET | Clinical trial | [100,101] |
3′-aza-2′-[18F]F-fluorofolic acid | Visualization of FR-positive tumor masses, evaluated in vivo in KB-derived tumors developed in mice. | PET | Pre-clinical | [102] | ||
[18F]F-folic acid derivative | PET | Pre-clinical | [103] | |||
[18F]F-fluorodeoxyglucose-folate | PET | Pre-clinical | [104] | |||
[⁶⁸Ga]Ga-DOTA-folate | Visualization of FR-positive tumor masses, evaluated in vivo in KB-derived tumors developed in mice. No accumulation in HT1080-derived tumors (FR negative). | PET | Pre-clinical | [105] | ||
[⁶⁸Ga]Ga -NODAGA-folate | Visualization of FR-positive tumor masses, evaluated in vivo in KB-derived tumors developed in mice. | PET | Pre-clinical | [106] | ||
[⁶⁸Ga]Ga -NOTA-folate | Visualization of FR-positive tumor masses, evaluated in vivo in KB-derived tumors developed in mice. Better in vivo performance than 99mTc-EC20. | PET | Pre-clinical | [107] | ||
177Lu-labeled folate conjugates containing an albumin binder | Visualization of FR-positive tumor masses, evaluated in vivo in KB-derived tumors developed in mice. Better than conjugates without albumin binder. Anticancer activity in KB-derived tumors, ovarian cancer cell line overexpressing FR and in vivo breast cancer model. | PET | Pre-clinical | [108,116] | ||
[18F]F-fluorodeoxyglucose-folate with albumin-binding capacity | Visualization of FR-positive Kidney tumor masses. Better than conjugates without albumin binder. | PET | Pre-clinical | [109] | ||
47Sc-labeled folate conjugates containing an albumin binder | Visualization of FR-positive Kidney tumor masses. Better than conjugates without albumin binder. Anticancer activity in KB-derived tumors and ovarian cancer cell line overexpressing FR. | PET | Pre-clinical | [110] | ||
152Tb-labeled folate conjugates containing an albumin binder | Visualization of KB-derived tumors. | PET | Pre-clinical | [111] | ||
155Tb-labeled folate conjugates containing an albumin binder | Visualization of KB-derived tumors. | SPECT | Pre-clinical | [111] | ||
64Cu-labeled folate conjugates containing an albumin binder | visualization of FR-positive tumors. Lower tumor-to-kidney ratio compared with other radiolabelled conjugates. | PET | Pre-clinical | [112] | ||
55Co-labeled folate conjugates containing an albumin binder | Visualization of FR-positive tumors. Lower tumor-to-kidney ratio compared with other radiolabelled conjugates. | PET | Pre-clinical | [113] | ||
177Lu-labeled MTHF conjugates containing an albumin binder | Visualization of FR-positive tumor masses due to selective targeting to FRα. | PET | Pre-clinical | [114] | ||
[161Tb]Tb-albumin binding folate conjugate | Theracnostic purpose. Tumor visualization and anticancer activity in KB-derived tumors. | PET | Pre-clinical | [111] | ||
[149Tb]Tb-albumin binding folate conjugate | Theranostic purpose. Tumor visualization and anticancer activity in KB-derived tumors. | PET | Pre-clinical | [111] | ||
[90Y]Y-albumin binding folate conjugate | Theranostic purpose Anticancer activity in ovarian cancer cell line overexpressing FR. | PET | Pre-clinical | [115] | ||
Radiolabeled anti FR-monoclonal antibodies | [111In]In-farteluzumab(anti-FRα- monoclonal antibody) and [131I]I- farteluzumab | Radioimmunoscintigraphy and possibly radioimmunotherapy of ovarian carcinomas. | SPECT | Pre-clinical | [108] | |
Fluorescent conjugates | Folic acid-fluorescein isothiocyanate conjugates (EC17) | Visualization of tumor masses in ovarian cancer patients during the cytoreductive surgery. | NIFI | Clinical trail | [118] | |
FR targeted nanoparticles | Mesoporous Silica nanoparticles coated with folic acid and loaded with a fluorescent agent | Visualization of pancreatic tumors overexpressing FR. | NIFI | Pre-clinical | [119] | |
Silica nanoparticles coated with folic acid and loaded with a phosphorescent agent | In vitro evaluation of FR expression in cervical cancer cells. | Phosphorescence Lifetime Imaging | Pre-clinical | [120] | ||
Gold nanostars covered with a silica shell that is functionalized with anti-FRα-monoclonal antibodies | Visualization of ovarian tumors | Raman imaging | Pre-clinical | [121] | ||
Mesoporous silica nanoparticles loaded with perfluorohexane and coated with indocyanine green and folic acid | Treatment and imaging or breast carcinomas | NIFI | Pre-clinical | [123] | ||
Folic acid-coated nanoparticles loaded with perfluorohexane and paclitaxel green indocyanine | Ultrasound imaging | Pre-clinical | [124] | |||
Gold-albumin nanoparticles coupled with folic acid and loaded with doxorubicin | Treatment and imaging or FR-positive gastric cancer cells | Tomography imaging | Pre-clinical | [125] | ||
Arthritis | FR targeted nanoparticles for imaging | Folic acid-coated iron oxide nanoparticles | Inflammation site visualization | MRI | Pre-clinical | [126] |
Ulcerative colitis | FR targeted nanoparticles for theragnosis | Liposomes coated with folic acid and loaded with betamethasone and a fluorescent dye | Inflammation site visualization and anti-inflammatory effect | NIFI | Pre-clinical | [127] |
6. Advanced Folate Receptor Targeted Nanomedicines in Clinic
6.1. Etarfolide
6.2. Vintafolide
6.3. Mirvetuximab Soravtansine
6.4. EC17 Conjugate
6.5. BMS-753493 Conjugate
6.6. EC1456 Conjugate
7. Current and Future Perspectives
8. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Martín-Sabroso, C.; Torres-Suárez, A.I.; Alonso-González, M.; Fernández-Carballido, A.; Fraguas-Sánchez, A.I. Active Targeted Nanoformulations via Folate Receptors: State of the Art and Future Perspectives. Pharmaceutics 2022, 14, 14. https://doi.org/10.3390/pharmaceutics14010014
Martín-Sabroso C, Torres-Suárez AI, Alonso-González M, Fernández-Carballido A, Fraguas-Sánchez AI. Active Targeted Nanoformulations via Folate Receptors: State of the Art and Future Perspectives. Pharmaceutics. 2022; 14(1):14. https://doi.org/10.3390/pharmaceutics14010014
Chicago/Turabian StyleMartín-Sabroso, Cristina, Ana Isabel Torres-Suárez, Mario Alonso-González, Ana Fernández-Carballido, and Ana Isabel Fraguas-Sánchez. 2022. "Active Targeted Nanoformulations via Folate Receptors: State of the Art and Future Perspectives" Pharmaceutics 14, no. 1: 14. https://doi.org/10.3390/pharmaceutics14010014