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REVIEW ARTICLE
Year : 2014  |  Volume : 10  |  Issue : 4  |  Page : 853-858

An overview of doxorubicin formulations in cancer therapy


Department of Research and Development, Bharat Serums and Vaccines Limited, R and D Centre, Mumbai, Maharashtra, India

Date of Web Publication9-Jan-2015

Correspondence Address:
Sangeeta Rivankar
Bharat Serums and Vaccines Limited, R and D Centre, DIL Complex, Near Tatwagyan Vidyapeeth, Ghodbunder Road, Thane West, Mumbai - 400 610, Maharashtra
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0973-1482.139267

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 > Abstract 

The burden of cancer is continuously increasing, and is rapidly becoming a global pandemic. The first liposomal encapsulated anticancer drug which received clinical approval against malignancies including solid tumours, transplantable leukemias and lymphomas was Doxorubicin HCl. This review is aimed at providing an overview of doxorubicin in cancer therapy. Pegylated liposomal doxorubicin has a polyethylene glycol (PEG) layer around doxorubicin-containing liposome as the result of a process known as pegylation. Non-pegylated liposomal doxorubicin (NPLD) was developed to overcome the drawbacks associated with previous formulations. Nudoxa; (NPLD) with its unique drug delivery system offers the benefit of pegylated liposomal doxorubicin without hand foot syndrome as the major side effect. Future studies will be directed towards estimating the costs of treatment with the novel liposomal doxorubicin formulations in order to assess their widespread use and robustness in treating patients with cancer.

 > Abstract in Chinese 

阿霉素制剂对肿瘤治疗的综述
摘要
癌症负担不断增加,并迅速成为一个流行性疾病。第一个临床被批准临床应用的是阿霉素脂质体,治疗恶性肿瘤包括实体瘤,白血病和淋巴瘤。本文综述阿霉素对肿瘤的治疗。聚乙二醇脂质体阿霉素的聚乙二醇(PEG)层包裹脂质体阿霉素的过程称为聚乙二醇化。非聚乙二醇脂质体阿霉素(NPLD)的开发是为了克服以前的配方相关的缺陷。nudoxa®(NPLD)以其独特的药物传递系统使聚乙二醇化脂质体阿霉素克服了手足综合征的主要副作用。未来的研究应评估新型脂质体阿霉素制剂治疗的成本,以及在广泛应用中的安全性。
关键词:脂质体,非聚乙二醇化,非聚乙二醇脂质体阿霉素,聚乙二醇化

Keywords: Liposomal, nonpegylated, nudoxa, pegylated


How to cite this article:
Rivankar S. An overview of doxorubicin formulations in cancer therapy. J Can Res Ther 2014;10:853-8

How to cite this URL:
Rivankar S. An overview of doxorubicin formulations in cancer therapy. J Can Res Ther [serial online] 2014 [cited 2022 Jul 7];10:853-8. Available from: https://www.cancerjournal.net/text.asp?2014/10/4/853/139267


 > Introduction Top


Cancer is a leading cause of morbidity and mortality worldwide. It is estimated that there will be 13.1 million deaths due to cancer in 2030. [1] Anthracyclines, especially doxorubicin, have been the mainstay of cancer therapy since long. Despite its broad-spectrum antineoplastic activity [Table 1], adverse events [Table 2], particularly cardiotoxicity, has limited the use of conventional doxorubicin in clinical practice. [2] This was especially so in patients with advanced disease requiring dose escalation. [3]
Table 1: The rapeutic uses of doxorubicin

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Table 2: Adverse effects associated with doxorubicin

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Doxorubicin hydrochloride (HCl) liposomal injection was the first liposomal encapsulated anticancer drug to receive clinical approval and has activity against a number of malignancies including solid tumors, transplantable leukemias, and lymphomas. [4]

Previous clinical studies have focused on the lower toxicity and better tolerability of liposomal anticancer drugs. [4] However, in recent years, research has focused on developing novel liposomal formulations. This review is aimed at providing an overview of doxorubicin in cancer therapy.


 > History of doxorubicin Top


The quest for anticancer compounds from soil-based microorganisms began in the 1950s. A new strain of Streptomyces peucetius, which produced a bright red pigment, was isolated, and an antibiotic was produced from this bacterium that was found to have good activity against mouse tumors. The new compound was named daunorubicin and was used successfully in the treatment of acute leukemia and lymphoma [5],[6] . However, by 1967, it was recognized that daunorubicin could produce fatal cardiac toxicity. [7]

Researches made genetic modifications to the Streptomyces spp. to produce a compound, Adriamycin, which was later called doxorubicin. Though doxorubicin had a higher therapeutic index cardiotoxicity continued to be a major problem. These compounds have been prototypes for subsequent research and today there are approximately more than 2000 known analogs of doxorubicin.


 > Mechanism of action of doxorubicin Top


The exact mechanism of action of doxorubicin is complex and still unclear. Doxorubicin interacts with the DNA by intercalation thus, inhibiting macromolecular biosynthesis. [8],[9] This further inhibits the progression of the enzyme topoisomerase II, and relaxes supercoils in DNA for transcription. Doxorubicin stabilizes the topoisomerase II complex after it has broken the DNA chain for replication, preventing the DNA double helix from being resealed and thereby stopping the process of replication [Figure 1]. Another mechanism of doxorubicin HCl is its ability to generate free radicals that induce DNA and cell membrane damage.
Figure 1: Mechanism of action of doxorubicin

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 > Doxorubicin in cancer therapy Top


Doxorubicin is most commonly used to treat cancers of the bladder, breast, stomach, lung, ovaries, thyroid, soft tissue sarcoma, multiple myeloma, and Hodgkin's lymphoma. The commonly used doxorubicin-containing regimens may include Adriamycin, cyclophosphamide (AC), Taxotere, AC, Adriamycin, bleomycin, vinblastine, dacarbazine, bleomycin, etoposide, AC, vincristine, procarbazine, and prednisone, cyclophosphamide, Adriamycin, vincristine, prednisone and 5-fluorouracil, AC. Doxil is mainly used for the treatment of ovarian cancer where it has progressed or recurred after platinum-based chemotherapy, or for the treatment of AIDS-related Kaposi's sarcoma. [10]


 > Cardiotoxicity associated with conventional doxorubicin Top


The cardiotoxicity associated with conventional doxorubicin is broadly classified as either acute or chronic. [11],[12],[13] It is a major concern during therapy as it may be dose-limiting. Risk factors that may increase the occurrence of cardiotoxicity include previous or current heart disease, extremes in age, race, exposure to irradiation in the mediastinal region and the cumulative dose of doxorubicin received. Patients with acute doxorubicin-induced cardiotoxicity usually present with rhythm disturbances, abnormal electrocardiographic changes, and acute, but reversible, reductions in left-ventricular ejection fraction. In general, these symptoms occur within 24 h of infusion, are self-limiting, and do not appear to increase the risk of future cardiac events. Cardiotoxicity, a consequence of conventional doxorubicin treatment manifests as a chronic complication, which ultimately results in congestive cardiomyopathy. Such toxicity has been shown to correlate with peak plasma doxorubicin concentrations, as well as with the lifetime cumulative dose administered. [14],[15] Historically, cardiomyopathy has rarely been observed with cumulative doses of conventional doxorubicin below 450 mg/m 2 ; however, studies suggest that doxorubicin-induced congestive heart failure (CHF) may occur at lower-doses and with greater frequency than previously noted. [16],[17] Von Hoff et al.[16] reported incidence of conventional doxorubicin-induced CHF of approximately 3% at cumulative dose of 400 mg/m 2 , increasing to 7% at 550 mg/m 2 and to 18% at 700 mg/m 2 .


 > Rationale for the development of novel doxorubicin formulations Top


Several efforts have been made to improve the toxicity profile of conventional anthracyclines, including the development of novel anthracycline analogs, the use of low-dose, prolonged, continuous infusion schedules; co-administration with the cardioprotective agent dexrazoxane; and the use of liposomal encapsulation technology. [12],[18],[19]

The therapy-limiting toxicity for this drug is cardiomyopathy, which may lead to CHF and death. An approach to ameliorating doxorubicin-related toxicity is to use drug carriers, which engender a change in the pharmacological distribution of the drug, resulting in reduced drug levels in the heart. Examples of these carrier systems include lipid-based (liposome) formulations that effect a beneficial change in doxorubicin. Liposomal encapsulation represents the most successful strategy to date for increasing the therapeutic index of conventional anthracyclines. Liposomal drug-delivery systems have been studied extensively to increase the therapeutic index of chemotherapy. The development of liposomal anthracyclines was based on the rationale that liposomes cannot escape the vascular space in areas with tight capillary junctions (heart muscle) but can leave the circulation in tissues and organs lined with cells that are not tightly joined (tumor cells). [20] Thus, liposomal encapsulation results in the preferential concentration of anthracyclines in tumor tissue, while limiting exposure in those sites most frequently associated with conventional anthracycline toxicity, such as the myocardium.


 > Liposomal formulations of doxorubicin Top


Due to the side-effects of conventional doxorubicin therapy, a need for development of liposomal formulation with equal efficacy and less side-effects arose. One of the main advantages of using liposomes as a delivery system is that the phospholipids used to form these vesicles are extracted from natural sources such as egg yolks or soybean and hence they are safe in the body. In addition, the degree of saturation of phospholipid bilayer can be modified to alter the drug release rate.

Liposomes, composed of natural phospholipids mixed with varying amounts of cholesterol are removed from circulation by the reticuloendothelial system (RES) within a few minutes to a few hours, subsequent to the acquisition of opsonins from plasma. Because of this short circulation half-life, the use of conventional liposomes has limited clinical applications.


 > Pegylated liposomal formulations of doxorubicin Top


The fact that some polymers, such as polyethylene glycol (PEG), ganglioside, and cerebroside sulfate are able to inhibit opsonization of the liposomes by plasma proteins and increase the half-life of liposomal drugs has renewed activity in the area of liposomal drug-delivery systems. Prolonged circulation of liposomes has been linked to better therapeutic efficacy of liposomal anthracyclines, possibly related to increased accumulation of drug loaded liposomes in tumor tissue.

A further advancement in this line of treatment was the pegylated-liposomal doxorubicin (such as Doxil® /Caelyx® ), a unique form of liposomal doxorubicin, in which the liposomes were coated with PEG in a process known as pegylation. This prevents drug uptake by the RES, thereby prolonging the circulation time (half-life: 3-4 days [21] vs. 30 h for conventional doxorubicin [22] ) beyond that of conventional liposomes and enabling the drug to remain encapsulated until it reaches the tumor site. [23],[24]

Doxil® is approved by the Food and Drug Administration (FDA) for treatment of ovarian cancer after failure of first line platinum-based chemotherapy and multiple myeloma. Outside the United States, Doxil® is known as Caelyx® and is marketed by Janssen. [25] However, there is some evidence that raises doubts on the benefits of pegylation in cancer treatment. PEG is a large molecule and its presence on the liposomal surface may decrease the interactions of liposomes with cells and impede the entry of liposomes into the tumor tissue. [26] This may possibly reduce the accumulation of liposomal drugs in the tumor tissue. A study assessing the accumulation of liposomal doxorubicin in murine Lewis lung carcinoma showed that benefits with PEG liposomal doxorubicin, such as increased blood levels and circulation time may be of little advantage when compared to maximizing drug accumulation in tumors. [27]

However, pegylated-liposomal doxorubicins cause dose-limiting hand-foot syndrome (HFS) (palmar-plantar erythrodysesthesia) characterized by skin eruptions on the palms of the hand and/or soles of the feet, leading to interruption in therapy by at least 2 weeks and decrease in subsequent dosage by 25% (Doxil Product Information Leaflet). The incidence of HFS has been observed in approximately 50% of patients dosed at 50 mg/m 2 (Doxil Product Information leaflet).

Though Caelyx® /Doxil® (pegylated liposomal doxorubicin) has high affinity for the skin and a very long circulation time, a major limitation is dose-limiting HFS (palmar-plantar erythrodysesthesia). [28]


 > Nonpegylated liposomal formulations of doxorubicin Top


There remains a need for stable, long circulating liposomes that do not cause such deleterious effects such as the HFS. The new variant of liposomal doxorubicin, nonpegylated liposomal doxorubicin (NPLD), has a unique drug-delivery system, and provides a breakthrough in cancer therapy by offering the benefits of pegylated-liposomal doxorubicin without its major side-effects such as HFS.

Nonpegylated liposomal doxorubicin injection provides a better safety profile than not only conventional doxorubicin, but also Doxil® /Caelyx® . NPLD not only reduces the cardiac toxicity associated with doxorubicin, but also the dose-limiting toxicity associated with the use of Doxil® /Caelyx® , such as HFS. This is achieved by a combination of (1) specific composition and (2) a unique manufacturing process (both which have been patented) of the NPLD's liposome, which gives it the desired physicochemical properties.

The NPLDs have an increased circulation time and less cardiotoxicity as compared with conventional doxorubicin. Since NPLDs do not have PEG coating, they are not associated with the painful HFS, which is a dose-limiting adverse event with PEG-doxorubicin.

Myocet® is a NPLD manufactured by Enzon Pharmaceuticals for Cephalon in Europe and for Sopherion Therapeutics in the United States and Canada. [29] Myocet® is approved in Europe and Canada for treatment of metastatic breast cancer in combination with cyclophosphamide. [30] However, it is under the process for the US FDA approval. Three Phase III trials in breast cancer evaluated Myocet® in comparison with standard doxorubicin and epirubicin. Compared to standard doxorubicin, Myocet® demonstrated less cardiotoxicity with no loss of efficacy. Equal doses of epirubicin and Myocet® were as effective with no significant difference in cardiotoxicity. Another limitation of Myocet® is related to its administration which is presented as a three-vial system; Myocet doxorubicin HCl, Myocet liposomes and Myocet buffer. In addition, a small amount of 0.9% sodium chloride for injection is needed, which is not provided in the package. The constituted product is a liposome-encapsulated doxorubicin-citrate complex. [31] Further, the high cost of Myocet® has been a hindrance in its widespread use. This has been a limitation in its robust assessment within the treatment pathway for advanced cancers.

Nudoxa® (NPLD) with its unique drug-delivery system is a breakthrough in cancer therapy as it offers the benefit of pegylated liposomal doxorubicin without its major side-effects like HFS. Further, it decreased the toxicity and other adverse events such as nausea, vomiting, and alopecia. Nudoxa® was jointly developed by Zydus and Bharat Serums and Vaccines Pvt. Limited Nudoxa® is being used as a chemotherapy drug to treat various cancers, such as breast cancer, ovarian cancer, and AIDS-related Kaposi sarcoma. The formulation uses distearoyl-phosphatidylcholine, a phospholipid with high phase transition temperature, which increases the retention of the liposomal content. This allows the doxorubicin HCl liposomes to circulate for prolonged periods in the bloodstream. Liposomes are small enough (average diameter of approximately 100 nm) to pass intact (extravasate) through the defective blood vessels present in the tumors. The liposomal covering helps the drug from escaping into the body's immune system thereby enabling the drug to reach malignant cells. This results in reduction of harmful side-effects owing to minimized distribution of the drug to nontargeted tissues. The preclinical studies were aimed at comparing Nudoxa® with PEG liposomal doxorubicin and conventional doxorubicin (data on file). Nudoxa® has demonstrated favorable toxicity profile in animal models. Further, it offers an advantage over pegylated liposomal doxorubicin due to the absence of HFS. Maximum tolerated dose for Nudoxa® has been established at 70 mg/m 2 in Phase I clinical trials (data on file).

Nudoxa® was launched in the Indian market in 2008 and is being used as a chemotherapy drug to treat various cancers, particularly, breast cancer, ovarian cancer and AIDS-related Kaposi sarcoma. A Phase II/III open label multicentric randomized trial determined the safety and efficacy of Nudoxa® at two different dose levels as compared to doxorubicin in patients with metastatic breast cancer. The trial reported that Nudoxa® at 70 mg/m 2 was as efficacious as conventional doxorubicin with a better safety profile (CTRI/2009/091/1000795).


 > Other novel formulations of doxorubicin Top


Stealth liposomes have gained an important place in cancer chemotherapy, but still these liposomes are modulated in terms of their selectivity for tumors by attachment of ligands. [32] Antibody coated liposome (immunoliposomes) are extensively studied where either an antibody is attached directly to liposome phospholipid head group or to the terminus of PEG polymer. [33] Temperature sensitive liposomes are also fabricated for tumor targeting. Similarly, acid triggered, enzyme triggered and light triggered release are being studied for delivery of doxorubicin. Other case of active targeting are sulfatide-mediated liposome [34] and folate receptor targeting. [35] Block co-polymers of poly (ethylene oxide)-poly (propylene oxide) block copolymers (pluronics) have also being developed for doxorubicin. Hydroxyapatite implants containing doxorubicin have been developed and tested in in vivo model for osteogenic sarcoma. [36] Thermosensitive poly (organophosphazenes) hydrogels containing doxorubicin have also been studied. The release of loaded doxorubicin from the polymer hydrogel was significantly sustained over 20 days. Oral delivery of microgels composed of pluronics was found to be active against Caco-2 cells. [37] Biological particles like resealed erythrocytes and bacterial ghosts are being explored for the delivery of doxorubicin are also proving to be quite effective. [38] Nanoparticles prepared using polybutylcyanoacrylate as delivery system for doxorubicin to target liver cancer have been studied. [39] The findings suggested that drug was released slowly in liver during detection period in treatment groups. Nanoparticles in range of 100-150 nm diameter range had the best liver targeting characteristics. It also decreased doxorubicin distribution in other tissues such as heart, kidney, and lung. Poly (butylcyanoacrylate) nanoparticles coated with polysorbate 80 considerably enhance the antitumor effect of doxorubicin against an intracranial glioblastoma in rats. [40]

Doxorubicin-loaded polymer-lipid hybrid nanoparticles were formulated and evaluated in a murine solid tumor model. [41] A new bioadhesive drug-delivery system, poly (d, l-lactide-co-glycolide/montmorillonite nanoparticles were developed for oral delivery of paclitaxel. Such a novel formulation is expected to possess extended residence time in the gastrointestinal tract, which promotes oral delivery of paclitaxel. [42]

Among the novel formulations, only the liposomal doxorubicin formulations have been extensively studied and explored in clinical trials in patients with different stages of cancer.


 > Conclusion Top


Conventional doxorubicin has been a mainstay of treatment for breast and ovarian cancers. Although the use of conventional doxorubicin has been somewhat limited by its adverse effects, recent efforts have markedly improved its safety and tolerability. Until date, the most successful strategy for improving the therapeutic index of conventional doxorubicin formulations has been liposomal encapsulation, which results in preferential accumulation of drug within the tumor site to maximize efficacy and minimize toxicity. Pegylated liposomal doxorubicin has demonstrated efficacy in ovarian cancer patients who have failed platinum and paclitaxel therapies, as well as in metastatic breast cancer. However, dose-limiting HFS limits its usage. Nudoxa® is a NPLD, in which doxorubicin is confined in nonpegylated liposomes. Safety and efficacy of Nudoxa® has been established in several preclinical studies (data on file). Currently Nudoxa® is being studied in clinical trials to establish its safety and efficacy in different types of cancers. The early results show that Nudoxa® is as efficacious as conventional doxorubicin with a better safety profile. This may present an improved treatment regimen for late stage cancer patients.

With established efficacy and safety profiles, future studies will hopefully be directed toward estimating the costs of treatment with the novel liposomal doxorubicin formulations in order to assess their widespread use and robustness in treating patients with cancer.

 
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    Figures

  [Figure 1]
 
 
    Tables

  [Table 1], [Table 2]


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Parisa Maleki Dana, Fatemeh Sadoughi, Russel J. Reiter, Sotoudeh Mohammadi, Zahra Heidar, Masoumeh Mirzamoradi, Zatollah Asemi
Biochimie. 2022;
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9 Dosimetric assessment of antitumor treatment by enhanced bleomycin delivery via electroporation and sonoporation
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10 Targeted liposomes for combined delivery of artesunate and temozolomide to resistant glioblastoma
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12 Establishment of childhood hepatoblastoma xenografts and evaluation of the anti-tumour effects of anlotinib, oxaliplatin and sorafenib
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13 Doxorubicin delivery systems with an acetylacetone-based block in cholesterol-terminated copolymers: diverse activity against estrogen-dependent and estrogen-independent breast cancer cells
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14 Characterization of Caerulomycin A as a dual-targeting anticancer agent
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15 Bioequivalence of a hybrid pegylated liposomal doxorubicin hydrochloride injection and Caelyx®: A single-dose, randomized, multicenter, open-label, two-period crossover study in patients with advanced ovarian cancer
S.S. Prakash, Rajnish Vasant Nagarkar, Krishna Chaitanya Puligundla, K.N. Lokesh, Rakesh Reddy Boya, Ankit Baldevbhai Patel, Lovenish Goyal, Aniket Thoke, Jigar Gordhanbhai Patel, Ajay Omprakash Mehta, Ghanshyam Nanubhai Patel, Mujtaba A. Khan, Imran Ahmad
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16 Oleanolic Acid-conjugated human serum albumin nanoparticles encapsulating doxorubicin as synergistic combination chemotherapy in oropharyngeal carcinoma and melanoma
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17 Dual-targeted and controlled release delivery of doxorubicin to breast adenocarcinoma: In vitro and in vivo studies
Zahra Jamshidi, Taraneh Sadat Zavvar, Mohammad Ramezani, Mona Alibolandi, Farzin Hadizadeh, Khalil Abnous, Seyed Mohammad Taghdisi
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18 Design and optimization of PEGylated silver nanoparticles for efficient delivery of doxorubicin to cancer cells
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20 Hydrazone modified nanoscale metal-organic frameworks as pH responsive nanoplatforms for cancer therapy
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21 Protective effects of berberine on various kidney diseases: Emphasis on the promising effects and the underlined molecular mechanisms
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22 Doxorubicin-induced senescence in normal fibroblasts promotes in vitro tumour cell growth and invasiveness: the role of Quercetin in modulating these processes
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23 Apocynum venetum leaf extract alleviated doxorubicin-induced cardiotoxicity through the AKT/Bcl-2 signaling pathway
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24 Greenness estimation of chromatographic assay for the determination of anthracycline-based antitumor drug in bacterial ghost matrix of Salmonella typhimurium
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26 Engineering Chemotherapeutic-Augmented Calcium Phosphate Nanoparticles for Treatment of Intraperitoneal Disseminated Ovarian Cancer
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28 Current Insights into Cellular Senescence and Myotoxicity Induced by Doxorubicin: The Role of Exercise and Growth Factors
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29 Bixin Prevents Colorectal Cancer Development through AMPK-Activated Endoplasmic Reticulum Stress
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31 A Review of Pharmacology, Toxicity and Pharmacokinetics of 2,3,5,4'-Tetrahydroxystilbene-2-O-ß-D-Glucoside
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32 Thioredoxin-1 Activation by Pterostilbene Protects Against Doxorubicin-Induced Hepatotoxicity via Inhibiting the NLRP3 Inflammasome
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33 Cariporide Attenuates Doxorubicin-Induced Cardiotoxicity in Rats by Inhibiting Oxidative Stress, Inflammation and Apoptosis Partly Through Regulation of Akt/GSK-3ß and Sirt1 Signaling Pathway
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34 Long Non-Coding RNA in Gastric Cancer: Mechanisms and Clinical Implications for Drug Resistance
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35 Smart Lipid–Polysaccharide Nanoparticles for Targeted Delivery of Doxorubicin to Breast Cancer Cells
Manuela Curcio, Matteo Brindisi, Giuseppe Cirillo, Luca Frattaruolo, Antonella Leggio, Vittoria Rago, Fiore Pasquale Nicoletta, Anna Rita Cappello, Francesca Iemma
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36 Nanoliposomes in Cancer Therapy: Marketed Products and Current Clinical Trials
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38 Design and Synthesis of Menthol and Thymol Derived Ciprofloxacin: Influence of Structural Modifications on the Antibacterial Activity and Anticancer Properties
Tomasz Szostek, Daniel Szulczyk, Jolanta Szymanska-Majchrzak, Michal Kolinski, Sebastian Kmiecik, Dagmara Otto-Slusarczyk, Aleksandra Zawodnik, Eliza Rajkowska, Kinga Chaniewicz, Marta Struga, Piotr Roszkowski
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39 The Mechanism of Dynamic Interaction between Doxorubicin and Calf Thymus DNA at the Single-Molecule Level Based on Confocal Raman Spectroscopy
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40 Targeted Drug Delivery Biopolymers Effectively Inhibit Breast Tumor Growth and Prevent Doxorubicin-Induced Cardiotoxicity
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41 Synthesis of a new water-soluble hexacarboxylated tribenzotriquinacene derivative and its competitive host–guest interaction for drug delivery
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44 Role of Creatine in the Heart: Health and Disease
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45 The Effects of Bergamot Polyphenolic Fraction, Cynara cardunculus, and Olea europea L. Extract on Doxorubicin-Induced Cardiotoxicity
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48 Hyperthermia Enhances Doxorubicin Therapeutic Efficacy against A375 and MNT-1 Melanoma Cells
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49 Cold Atmospheric Plasma: A New Strategy Based Primarily on Oxidative Stress for Osteosarcoma Therapy
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52 Chemotherapeutic Regimens and Chemotherapy-Free Intervals Influence the Survival of Patients with Recurrent Advanced Epithelial Ovarian Carcinoma: A Retrospective Population-Based Study
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57 Evaluation of Anti-Cancer Effects of Caspian Cobra (Naja naja oxiana) Snake Venom in Comparison with Doxorubicin in HeLa Cancer Cell Line and Normal HFF Fibroblast
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59 Mechanisms and Potential Treatment Options of Heart Failure in Patients With Multiple Myeloma
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68 Isoliquiritigenin ameliorates doxorubicin-induced acute pancreatitis by inhibiting ROS production via modulation of Nrf2/HO-1 oxidative stress pathway
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71 Thymoquinone and Costunolide Induce Apoptosis of Both Proliferative and Doxorubicin-Induced-Senescent Colon and Breast Cancer Cells
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72 Platelet-rich plasma inhibits Adriamycin-induced inflammation via blocking the NF-?B pathway in articular chondrocytes
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73 A novel formulation of theranostic nanomedicine for targeting drug delivery to gastrointestinal tract cancer
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74 Development of an engineered peptide antagonist against periostin to overcome doxorubicin resistance in breast cancer
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75 Doxorubicin treatment modulates chemoresistance and affects the cell cycle in two canine mammary tumour cell lines
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77 miR-520b Inhibits IGF-1R to Increase Doxorubicin Sensitivity and Promote Cell Apoptosis in Breast Cancer
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78 Evaluation of Cytotoxicity Induced by the Anti-Cancerous Drugs Doxorubicin and Erlotinib in Allium cepa Assay for Eco-Safety Monitoring
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79 Circ-SKA3 Enhances Doxorubicin Toxicity in AC16 Cells Through miR-1303/TLR4 Axis
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80 Enhanced antitumour efficacy of functionalized doxorubicin plus schisandrin B co-delivery liposomes via inhibiting epithelial-mesenchymal transition
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81 Loading of doxorubicin on poly(methyl methacrylate-co-methacrylic acid) nanoparticles and release study
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82 Role of miRNAs in regulating responses to radiotherapy in human breast cancer
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85 Dual covalent functionalization of single-walled carbon nanotubes for effective targeted cancer therapy
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86 Engineering the early bone metastatic niche through human vascularized immuno bone minitissues
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88 The application of aluminium phthalocyanine AlPs-4-mediated photodynamic therapy against human soft tissue sarcoma (RMS) cell line
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91 Chemotherapeutic drugs: Cell death- and resistance-related signaling pathways. Are they really as smart as the tumor cells?
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92 AIE-Based Fluorescent Triblock Copolymer Micelles for Simultaneous Drug Delivery and Intracellular Imaging
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93 Miniatured Fluidics-Mediated Modular Self-Assembly of Anticancer Drug–Amino Acid Composite Microbowls for Combined Chemo-Photodynamic Therapy in Glioma
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94 ?-Ray-Triggered Drug Release of Reactive Oxygen Species-Sensitive Nanomedicine for Enhanced Concurrent Chemoradiation Therapy
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95 Two-dimensional materials in biomedical, biosensing and sensing applications
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96 Aptamers: an emerging navigation tool of therapeutic agents for targeted cancer therapy
Chang Yang, Yu Jiang, Sai Heng Hao, Xing Yi Yan, De Fei Hong, Hua Naranmandura
Journal of Materials Chemistry B. 2021;
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97 Irisin ameliorates doxorubicin-induced cardiac perivascular fibrosis through inhibiting endothelial-to-mesenchymal transition by regulating ROS accumulation and autophagy disorder in endothelial cells
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98 Enhanced therapeutic index of liposomal doxorubicin Myocet locally delivered by fibrin gels in immunodeficient mice bearing human neuroblastoma
Maurizio Viale, Vittorio Bertone, Irena Maric, Michele Cilli, Laura Emionite, Vittorio Bocchini, Mirco Ponzoni, Vincenzo Fontana, Fabrizio De Luca, Mattia Rocco
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99 Evidences for the mechanism of Shenmai injection antagonizing doxorubicin-induced cardiotoxicity
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100 Treatment outcome of doxorubicin versus idarubicin in adult acute myeloid leukemia
Hemat Afifi Sherif, Ahmed Magdy, Heba Anees Elshesheni, Sherein Mahmoud Ramadan, Reham A. Rashed
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101 Tumor targeting antibody-conjugated nanocarrier with pH/thermo dual-responsive macromolecular film layer for enhanced cancer chemotherapy
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Materials Science and Engineering: C. 2021; 118: 111361
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102 Doxorubicin nanoformulations on therapy against cancer: An overview from the last 10?years
Natália A. D'Angelo, Mariana A. Noronha, Mayra C.C. Câmara, Isabelle S. Kurnik, Chuying Feng, Victor H.S. Araujo, João H.P.M. Santos, Valker Feitosa, João V.D. Molino, Carlota O. Rangel-Yagui, Marlus Chorilli, Emmanuel Ho, André M. Lopes
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103 Cellulose acetate encapsulated upconversion nanoparticles – A novel theranostic platform
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104 Nano-immunotherapy: Unique mechanisms of nanomaterials in synergizing cancer immunotherapy
Quan Liu, Yanhong Duo, Jianye Fu, Meng Qiu, Zhe Sun, Dickson Adah, Jianlong Kang, Zhongjian Xie, Taojian Fan, Shiyun Bao, Han Zhang, Li-Ping Liu, Yihai Cao
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105 Synergetic effect of adsorption-photocatalysis by GO-CeO2nanocomposites for photodegradation of doxorubicin
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106 Liposomal doxorubicin as targeted delivery platform: Current trends in surface functionalization
Vivek Makwana, Jasmine Karanjia, Thomas Haselhorst, Shailendra Anoopkumar-Dukie, Santosh Rudrawar
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107 Construction and antitumor properties of a targeted nano-drug carrier system responsive to the tumor microenvironment
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108 Preparation and characterization of PEGylated liposomal Doxorubicin targeted with leptin-derived peptide and evaluation of their anti-tumor effects, in vitro and in vivo in mice bearing C26 colon carcinoma
Naghmeh Shahraki, Amin Mehrabian, Shahrazad Amiri-Darban, Seyedeh Alia Moosavian, Mahmoud Reza Jaafari
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109 Identification and validation of a prognostic signature and combination drug therapy for immunotherapy of head and neck squamous cell carcinoma
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110 Sensitive analysis of doxorubicin and curcumin by micellar electromagnetic chromatography with a double wavelength excitation source
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111 Folic acid-appended galactoxyloglucan-capped iron oxide nanoparticles as a biocompatible nanotheranostic agent for tumor-targeted delivery of doxorubicin
B.S. Unnikrishnan, Anitha Sen, G.U. Preethi, Manu M. Joseph, S. Maya, R. Shiji, K.S. Anusree, T.T. Sreelekha
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112 Doxorubicin delivery by magnetic nanotheranostics enhances the cell death in chemoresistant colorectal cancer-derived cells
María Julia Martín, Pamela Azcona, Verónica Lassalle, Claudia Gentili
European Journal of Pharmaceutical Sciences. 2021; 158: 105681
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113 Folic acid-doxorubicin polymeric nanocapsules: A promising formulation for the treatment of triple-negative breast cancer
Rodrigo Cé, Gabriela Klein Couto, Barbara Zoche Pacheco, Danieli Rosane Dallemole, Júlia Damé Paschoal, Bruna Silveira Pacheco, Silvia Stanisçuaski Guterres, Fabiana Seixas, Tiago Collares, Adriana Raffin Pohlmann
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114 Doxorubicin suppresses chondrocyte differentiation by stimulating ROS production
Cheng Wu, Jiayi Luo, Yuanxin Liu, Jiannan Fan, Xianwen Shang, Riguang Liu, Chuan Ye, Jihong Yang, Hong Cao
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115 Effective drug delivery system based on hydrophobin and halloysite clay nanotubes for sustained release of doxorubicin
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116 Incidence and risk factors for oral mucositis in pediatric patients receiving chemotherapy
Marina Curra, Amanda F. Gabriel, Maria Beatriz C. Ferreira, Marco Antonio T. Martins, André T. Brunetto, Lauro J. Gregianin, Manoela Domingues Martins
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117 The role of miRNAs in colorectal cancer progression and chemoradiotherapy
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118 The nephroprotective effects and mechanisms of rehmapicrogenin include ROS inhibition via an oestrogen-like pathway both in vivo and in vitro
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119 DNA damaging agents and DNA repair: From carcinogenesis to cancer therapy
Larissa Costa de Almeida, Felipe Antunes Calil, João Agostinho Machado-Neto, Leticia Veras Costa-Lotufo
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120 Intracellular RNA and nuclear DNA-dual-targeted tumor therapy via upconversion nanoplatforms with UCL/MR dual-mode bioimaging
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121 A bioimaging system combining human cultured reporter cells and planar chromatography to identify novel bioactive molecules
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122 Sustained and controlled delivery of doxorubicin from an in-situ setting biphasic hydroxyapatite carrier for local treatment of a highly proliferative human osteosarcoma
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123 Optical properties of natural small molecules and their applications in imaging and nanomedicine
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124 Application of new multicomponent nanosystems for overcoming doxorubicin resistance in breast cancer therapy
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125 Cyclodextrin-based delivery systems for in vivo-tested anticancer therapies
Ana Cláudia Santos, Diana Costa, Laura Ferreira, Catarina Guerra, Miguel Pereira-Silva, Irina Pereira, Diana Peixoto, Nuno R. Ferreira, Francisco Veiga
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126 Matrix Metalloproteinase-9-Responsive Surface Charge-Reversible Nanocarrier to Enhance Endocytosis as Efficient Targeted Delivery System for Cancer Diagnosis and Therapy
Qiu-Ju Han, Xiao-Tong Lan, Ying Wen, Chuan-Zeng Zhang, Michael Cleary, Yasra Sayyed, Guangdong Huang, Xiaoling Tuo, Long Yi, Zhen Xi, Lu-Yuan Li, Qiang-Zhe Zhang
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127 Multi-Functional Liposome: A Powerful Theranostic Nano-Platform Enhancing Photodynamic Therapy
Xiamin Cheng, Jing Gao, Yang Ding, Yao Lu, Qiancheng Wei, Dezhi Cui, Jiali Fan, Xiaoman Li, Ershu Zhu, Yongna Lu, Qiong Wu, Lin Li, Wei Huang
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128 Perspectives and controversies regarding the use of natural products for the treatment of lung cancer
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129 The Use of Phospholipids to Make Pharmaceutical Form Line Extensions
Peter Hoogevest, Harry Tiemessen, Josbert M. Metselaar, Simon Drescher, Alfred Fahr
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130 Thymoquinone attenuates doxorubicin-cardiotoxicity in rats
Derya Karabulut, Emel Ozturk, Emin Kaymak, Ali Tugrul Akin, Birkan Yakan
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131 Thymoquinone has a neuroprotective effect against inflammation, oxidative stress, and endoplasmic reticulum stress in the brain cortex, medulla, and hippocampus due to doxorubicin
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132 A quantitative systems pharmacology approach to predict the safe-equivalent dose of doxorubicin in patients with cardiovascular comorbidity
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133 Ribosomal protein L5 mediated inhibition of c-Myc is critically involved in sanggenon G induced apoptosis in non-small lung cancer cells
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134 Advances in engineering local drug delivery systems for cancer immunotherapy
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135 2D Germanane Derivative as a Vector for Overcoming Doxorubicin Resistance in Cancer Cells
Michaela Fojtu, Jan Balvan, Martina Raudenská, Tomáš Vicar, Jirí Šturala, Zdenek Sofer, Jan Luxa, Jan Plutnar, Michal Masarík, Martin Pumera
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136 Protein phosphatase 1 in tumorigenesis: is it worth a closer look?
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137 Preparation and in vitro/in vivo evaluation of doxorubicin-loaded poly[lactic-co-glycol acid] microspheres using electrospray method for sustained drug delivery and potential intratumoral injection
Ming-Yi Hsu, Yu-Ting Huang, Chun-Jui Weng, Chien-Ming Chen, Yong-Fong Su, Sung-Yu Chu, Jeng-Hwei Tseng, Ren-Chin Wu, Shih-Jung Liu
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138 Hypoxia-sensitive micellar nanoparticles for co-delivery of siRNA and chemotherapeutics to overcome multi-drug resistance in tumor cells
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139 Alginate microbeads with internal microvoids for the sustained release of drugs
Stefania Boi, Nadia Rouatbi, Elena Dellacasa, Donatella Di Lisa, Paolo Bianchini, Orietta Monticelli, Laura Pastorino
International Journal of Biological Macromolecules. 2020; 156: 454
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140 Doxorubicin-loaded composite nanogels for cancer treatment
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141 In vitro irradiation of doxorubicin with 18F-FDG Cerenkov radiation and its potential application as a theragnostic system.
Hilda Angeline Quintos-Meneses, Liliana Aranda-Lara, Enrique Morales-Ávila, Eugenio Torres-García, Miguel Ángel Camacho-López, Mariana Sánchez-Holguín, Myrna A. Luna-Gutiérrez, Ninfa Ramírez-Durán, Keila Isaac-Olivé
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142 Arctigenin, a novel TMEM16A inhibitor for lung adenocarcinoma therapy
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143 New molecular and biochemical insights of doxorubicin-induced hepatotoxicity
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144 Graphene oxide as a potential drug carrier – Chemical carrier activation, drug attachment and its enzymatic controlled release
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145 Extracellular vesicles as natural therapeutic agents and innate drug delivery systems for cancer treatment: Recent advances, current obstacles, and challenges for clinical translation
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146 Reversing P-Glycoprotein-Associated Multidrug Resistance of Breast Cancer by Targeted Acid-Cleavable Polysaccharide Nanoparticles with Lapatinib Sensitization
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ACS Applied Materials & Interfaces. 2020; 12(46): 51198
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147 Facile Fabrication Route of Janus Gold-Mesoporous Silica Nanocarriers with Dual-Drug Delivery for Tumor Therapy
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148 Effect of TAT-DOX-PEG irradiated gold nanoparticles conjugates on human osteosarcoma cells
Raoul V. Lupusoru, Daniela A. Pricop, Cristina M. Uritu, Adina Arvinte, Adina Coroaba, Irina Esanu, Mirela F. Zaltariov, Mihaela Silion, Cipriana Stefanescu, Mariana Pinteala
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149 Co-delivery of Doxorubicin and Curcumin with Polypeptide Nanocarrier for Synergistic Lymphoma Therapy
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150 The implications of mitochondria in doxorubicin treatment of cancer in the context of traditional and modern medicine
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151 Dexrazoxane Protects Cardiomyocyte from Doxorubicin-Induced Apoptosis by Modulating miR-17-5p
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152 Protective Effect of miR-204 on Doxorubicin-Induced Cardiomyocyte Injury via HMGB1
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153 Genomic instability and cancer: lessons from Drosophila
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154 Doxorubicin delivery by polymer nanocarrier based on N-methylglucamine resorcinarene
Tatiana Yu. Sergeeva, Rezeda K. Mukhitova, Leysan R. Bakhtiozina, Irek R. Nizameev, Marsil K. Kadirov, Anastasia S. Sapunova, Alexandra D. Voloshina, Albina Y. Ziganshina, Igor S. Antipin
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155 Development of stimuli-responsive intelligent polymer micelles for the delivery of doxorubicin
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156 Reticulocalbin-1 knockdown increases the sensitivity of cells to Adriamycin in nasopharyngeal carcinoma and promotes endoplasmic reticulum stress-induced cell apoptosis
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157 Differential changes in the pharmacokinetics of doxorubicin in diethylnitrosamine-induced hepatocarcinoma model rats
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158 Pluronic P123 modified nano micelles loaded with doxorubicin enhanced tumor-suppressing effect on drug-resistant breast cancer cells
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159 Modification of graphene oxide by angiopep-2 enhances anti-glioma efficiency of the nanoscaled delivery system for doxorubicin
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160 Preparation, characterization, and in vitro evaluation of amphiphilic peptide P12 and P12-DOX nanomicelles as antitumor drug carriers
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161 Anthracycline-related cardiotoxicity in older patients with acute myeloid leukemia: a Young SIOG review paper
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162 Protective role of black seed oil in doxorubicin-induced cardiac toxicity in children with acute lymphoblastic leukemia
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163 Galectin-3 inhibition attenuates doxorubicin-induced cardiac dysfunction by upregulating the expression of peroxiredoxin-4
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164 Tumor in 3D: In Vitro Complex Cellular Models to Improve Nanodrugs Cancer Therapy
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165 Key Signaling Pathways Engaged in Cancer Management: Current Update
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166 Drug Delivery Approaches for Doxorubicin in the Management of Cancers
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167 Ditelluride-Bridged PEG-PCL Copolymer as Folic Acid-Targeted and Redox-Responsive Nanoparticles for Enhanced Cancer Therapy
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168 Human Pluripotent Stem Cell-Derived Cardiomyocytes for Assessment of Anticancer Drug-Induced Cardiotoxicity
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169 Krebs Cycle Intermediate-Modified Carbonate Apatite Nanoparticles Drastically Reduce Mouse Tumor Burden and Toxicity by Restricting Broad Tissue Distribution of Anticancer Drugs
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170 Signal transducer and activator of transcription 6 as a target in colon cancer therapy (Review)
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171 Assessing Advantages and Drawbacks of Rapidly Generated Ultra-Large 3D Breast Cancer Spheroids: Studies with Chemotherapeutics and Nanoparticles
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172 Liposomes for Intra-Articular Analgesic Drug Delivery in Orthopedics: State-of-Art and Future Perspectives. Insights from a Systematic Mini-Review of the Literature
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173 Liquid Chromatography–Tandem Mass Spectrometry for the Simultaneous Determination of Doxorubicin and its Metabolites Doxorubicinol, Doxorubicinone, Doxorubicinolone, and 7-Deoxydoxorubicinone in Mouse Plasma
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174 Doxorubicin Loaded Poloxamer Thermosensitive Hydrogels: Chemical, Pharmacological and Biological Evaluation
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175 Antitumor Features of Vegetal Protein-Based Nanotherapeutics
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176 The Basement Membrane in a 3D Breast Acini Model Modulates Delivery and Anti-Proliferative Effects of Liposomal Anthracyclines
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