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Examining further the cellular mechanism involved in CBD-induced cell death, they found that CBD reduced mitochondrial membrane potential, triggered the translocation of the Beclin2 interacting protein Bid to the mitochondria and the release of cytochrome C to the cytosol and, ultimately, the activation of the intrinsic apoptotic pathway. Finally, the relationship between CBD-induced apoptosis and autophagic cell death was explored by blocking each form of cell death with specific inhibitors.
CBD treatment induced the cleavage of Beclin1 and the subsequent translocation of the cleavage product to the mitochondria where it may induce apoptosis through the enhancement of cytochrome C release [ 34 , 35 ].
As a whole this work highlights the presence of a complex balance between autophagy and mitochondria-mediated apoptosis in CBD-induced breast cancer cell death and strengthens the idea that CBD can be considered as an alternative agent for breast cancer therapy.
Figure 3 shows a schematic representation of the signalling pathways associated with the effect of CBD in breast cancer cell proliferation and invasion. Schematic representation of the signalling pathways associated with CBD effects on breast cancer. CBD also possesses anti-tumoural properties in gliomas, tumours of glial origin characterized by a high morphological and genetic heterogeneity and considered one of the most devastating neoplasms, showing high proliferative rate, aggressive invasiveness and insensitivity to radio- and chemotherapy.
After the seminal paper of Jacobsson et al. Interestingly, CBD did not affect viability of non-transformed primary glial cells [ 38 ]. When tumour xenografts were generated in immune-deficient mice, in vivo intratumoural treatment with CBD significantly reduced tumour growth [ 37 ]. The anti-proliferative effect of CBD was cannabinoid and vanilloid receptors independent. More importantly, this paper demonstrated for the first time that the anti-tumour effect of CBD involved the induction of oxidative stress, through increased early production of ROS, depletion of intracellular glutathione and increased GSH-associated enzymatic activity.
Accordingly, the CBD anti-proliferative effect was reversed by the anti-oxidant , tocopherol. In line with this, more recently Torres et al. These effects were not observed with either compound individually, indicating them as a prerogative of combination treatment.
Differently from Marcu's data [ 39 ], our recent results Dr. Valenti, University of Insubria, Varese, pers.
Thus, inhibition of these three molecules appears as part of the multiple molecular targets for CBD anti-neoplastic activity [ 41 ]. Further biochemical analysis of glioma tumour tissues excised from nude mice treated in vivo with CBD indicated a significant decrease of activity and content of 5-LOX, as well as a marked stimulation of FAAH and a decrease of AEA content [ 42 ]. Besides cell growth, CBD reduced glioma cell migration [ 43 ] and invasiveness in a Boyden chamber test [ 39 ], at concentrations lower than those required to inhibit cell proliferation.
CBD seems to counteract glioma cell proliferation and invasion through multiple mechanisms, as summarized in Figure 4. Schematic representation of the signalling pathways associated with CBD effects on glioma. They demonstrated that CBD treatment induced apoptosis, through caspase-3 activation in human acute myeloid leukaemia HL cell line, whereas it had no effect on human monocytes from normal individuals.
Later on, McKallip et al. In Jurkat cells, CBD exposure resulted in the activation of caspase-8, -9, and -3, the cleavage of poly ADPribose polymerase and the decrease in full-length Bid, suggesting a possible cross-talk between the intrinsic and extrinsic apoptotic pathways.
Moreover, exposure to CBD led to the loss of mitochondrial membrane potential and subsequent release of cytochrome C. Finally, CBD decreased the levels of phospho-p38 mitogen-activated protein kinase [ 45 ], and this effect was blocked by treatment with a CB 2 -selective antagonist or ROS scavenger.
In addition, CBD treatment caused a significant reduction in tumour burden and increased the level of apoptotic tumours in ELbearing mice [ 45 ]. Together, the results suggest that CBD, acting through CB 2 receptors and ROS production, may represent a novel and highly selective treatment for leukaemia.
Moreover, previous evidence indicated that human leukaemias and lymphomas expressed significantly higher levels of CB 2 receptors compared with other tumour cell lines, suggesting that tumours of immune origin may be highly sensitive to the CB 2 -mediated effects of CBD [ 46 ]. Given the poor response of lung cancer to available therapy and its aggressive biological nature, a series of targets and new therapeutic strategies for their treatment are currently being investigated [ 47 — 50 ].
Recently, Ramer et al. Interestingly all these cellular events were blocked by cannabinoids or TRPV1 receptor antagonists. The significant inhibition of A cell invasion following CBD treatment was also accompanied by the downregulation of another important factor involved in the regulation of cell spreading, the plasminogen activator inhibitor PAI-1 [ 52 ]. Additionally , in vivo studies in thymic aplastic nude mice revealed a significant inhibition of A lung metastases following CBD treatment [ 51 ] and a significant downregulation of PAI-1 protein was demonstrated in A xenografts of CBD-treated rats [ 52 ].
It is worth noting that CBD decreased invasiveness in a range of therapeutically relevant concentrations 0. Together, these findings provide a novel mechanism underlying the anti-invasive action of CBD on human lung cancer cells and imply its use as a therapeutic option for the treatment of highly invasive cancers. Thyroid cancer is the most common endocrine malignancy and Ligresti et al. Later on, Lee et al. The presence of N-acetyl-L-cysteine NAC , a precursor of glutathione, markedly attenuated the induction of apoptosis and restored the diminished levels of cellular thiols.
The observation that CBD induced oxidative stress in thymocytes, EL-4 cells and splenocytes [ 56 ] substantiates the notion that, unlike monocytes, T cells both primary and immortalized, are all sensitive and respond similarly to CBD, with a central role of ROS generation.
Colon cancer is a major cause of morbidity and mortality in Western countries. A recent paper from Izzo's group [ 57 ] demonstrated the chemopreventive effect of CBD in a preclinical animal model of colon cancer based on azoxymethane AOM administration in mice. In vitro studies, supported the beneficial effect of CBD. In the light of its safety records, these results suggest that CBD might be worthy of clinical consideration in colon cancer prevention.
Angiogenesis consists of the formation of new blood vessels from pre-existing ones and represents another promising therapeutic target for cancer therapy. Surprisingly, so far no study has investigated the effect of CBD on angiogenesis. Our data currently awaiting publication [ 58 ] demonstrated that CBD potently inhibited HUVE cells proliferation, migration and invasion through the induction of endothelial cell cytostasis without triggering apoptosis.
Interestingly, CBD also affected endothelial cell differentiation into tubular capillaries as well as the outgrowth of capillary-like structures from HUVEC spheroids in vitro. In addition, the anti-angiogenic properties of CBD were demonstrated also in vivo , using a matrigel sponge model. Collectively , these preliminary data demonstrate that, besides its well known pro-apoptotic anti-proliferative and anti-invasive actions, CBD may also exert anti-angiogenic effects, thus further strengthening its potential application in cancer therapy.
Collectively, the non-psychoactive plant-derived cannabinoid CBD exhibits pro-apoptotic and anti-proliferative actions in different types of tumours and may also exert anti-migratory, anti-invasive, anti-metastatic and perhaps anti-angiogenic properties.
On the basis of these results, evidence is emerging to suggest that CBD is a potent inhibitor of both cancer growth and spread. Interestingly , the anticancer effect of this compound seems to be selective for cancer cells, at least in vitro , since it does not affect normal cell lines. The efficacy of CBD is linked to its ability to target multiple cellular pathways that control tumourigenesis through the modulation of different intracellular signalling depending on the cancer type considered.
The most common effect of CBD is the increase in ROS production that seems to be determinant for triggering its beneficial action in all the considered cancer cell types. In some cases lung, leukaemia, colon a clear contribution of these receptors has been demonstrated through the use of specific antagonists, but in other cancer types glioma and breast their relevance appears only marginal or absent. Besides the in vitro data, the efficacy of CBD in reducing tumour growth and, in some cases, metastasization was confirmed in experimental animal models.
However, the potential clinical application of CBD for cancer therapy needs some consideration. Its low toxicity is certainly a good starting point. The route of administration appears more problematic since CBD oral absorption is slow and unpredictable. Interestingly, this range of concentration was demonstrated to be active in inhibiting lung cancer cell invasion [ 52 , 53 ], thus suggesting that in some cases the oral route could be the appropriate choice.
Moreover, oromucosal administration may represent a first choice in the presence of nausea and vomiting. In the light of its safety record and considering that CBD is already currently used in patients with multiple sclerosis, the findings here summarized suggest that CBD might be worthy of clinical consideration for cancer therapy. National Center for Biotechnology Information , U. Br J Clin Pharmacol. Published online Apr Author information Article notes Copyright and License information Disclaimer.
Received Jan 30; Accepted Apr This article has been cited by other articles in PMC. Open in a separate window. Cannabinoids in the treatment of cancer Cannabinoids are currently used in cancer patients to palliate wasting, emesis and pain that often accompany cancer.
Table 1 Effects of cannabidiol on different types of cancer. CBD and breast cancer In Ligresti et al. CBD and glioma CBD also possesses anti-tumoural properties in gliomas, tumours of glial origin characterized by a high morphological and genetic heterogeneity and considered one of the most devastating neoplasms, showing high proliferative rate, aggressive invasiveness and insensitivity to radio- and chemotherapy.
CBD and lung cancer Given the poor response of lung cancer to available therapy and its aggressive biological nature, a series of targets and new therapeutic strategies for their treatment are currently being investigated [ 47 — 50 ].
CBD and endocrine tumours Thyroid cancer is the most common endocrine malignancy and Ligresti et al. CBD and colon cancer Colon cancer is a major cause of morbidity and mortality in Western countries. CBD and angiogenesis Angiogenesis consists of the formation of new blood vessels from pre-existing ones and represents another promising therapeutic target for cancer therapy.
Conclusion and future directions Collectively, the non-psychoactive plant-derived cannabinoid CBD exhibits pro-apoptotic and anti-proliferative actions in different types of tumours and may also exert anti-migratory, anti-invasive, anti-metastatic and perhaps anti-angiogenic properties.
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