Carcinogenesis is a sequence of steps that are usually accompanied by abnormal cellular proliferation due to either a faulty activation of proto-oncogenes or inactivation of tumor suppressor genes. P53 is a tumor suppressor gene that is considered as the guardian of human genome as it has an essential role in disrupting the growth of cancer cells and interfering with angiogenesis (
16). The success of chemotherapy or radiation therapy in killing cancer cells is hindered by obstacles. One of these obstacles is related to the numerous adverse effects caused by this type of therapy due to their cytotoxicity and apoptosis induction in normal cells such as bone marrow, lymphoid organs, hair follicles, and epithelium lining of the small intestine (
17). Thus, the discovery of an alternative therapy to the currently used anti-cancer drugs has been considered as one of the most essential concerns. This was mainly to overcome their induced side effects such as myelosuppression, anemia, hair loss and most importantly due to the existence of resistance to these treatments (
18).
Overcoming the adverse effects on normal cells could be carried out through targeting p53 activation in cancer cells either through transcription-dependent or transcription-independent, but mitochondria-dependent mechanisms (
19). However, the main problem in this type of therapy is that restoring the apoptotic stimulating activity of p53 gene is inhibited as a result of mutation in p53 gene which is considered as the most commonly mutated gene in human cancer (
20). It was also demonstrated that regression of mutant p53 depletes the malignant properties of cancer cells, while the existence of mutation in p53 resulted in appearance of exaggerated properties in cancer cells such as metastasis and drug resistance (
21). It was also reported that retaining the apoptotic stimulating activity of p53 gene could be carried out through the delivery of wild type p53 gene into cancer cells via viral targeted gene therapy (
22). Another study demonstrated that the use of certain residue peptides could stabilize the tumor suppressor gene through specific binding to it (
23). In the same context, a class of proteins known as mouse double minute 2 homolog (MDM2) are considered negative regulator of the p53 tumor suppressor gene (
24). Thus, reactivation of p53 could be carried out by designing inhibitors of MDM2-p53 interaction, where it was demonstrated that MDM2 inhibitors could induce apoptosis and sensitize lung cancer cells to chemotherapy (
25,
26). Therefore, current study aimed to evaluate captopril and BTxA as anti-cancer agents in relation to their p53 pro-apoptotic potential in cancer cells as the success of restoring the activity of p53 reported to be a miracle weapon against cancer (
27).
The decreased risk for the development of prostate cancer in patients treated with captopril as an antihypertensive drug attracted the attention of researchers to investigate the anti-cancer potential of captopril (28). In the current study, captopril was investigated for its anti-cancer activity as it is available in pure form with identified structure, FDA approved and with known side effects and its pharmacokinetics have been studied extensively (
9,
29). In the mean time, botulinum toxin type A is a commercially available pure pharmaceutical product with a known protein sequence (
30), side effects (
31) as well as toxicity and clinical studies (
32). Hence, evaluating the anti-cancer efficacy of captopril and BTX-A is of great value rather than the searching for completely new drugs. DU145 is androgen-independent prostate cancer cell line that is characterized by the presence of 2 mutations in p53 gene (
33). To the best of our knowledge, the
in-vitro anti-cancer potentials of captopril and BTX-A against colon cancer cell lines has not been previously reported, thus prostate and colon cancer cells were selected as cancer cell models.
The observed anti-cancer potential in the present study was matching other studies despite variable conditions among different studies, where
in-vivo efficacy of captopril was demonstrated in counteracting the development of azoxymethane induced colonic premalignant lesions in diabetic and hypertensive rats (
34). In addition, artesunate and captopril exhibited synergistic anti-angiogenic effect
in-vitro and
in-vivo (
2). In the mean context, the recorded anti-cancer activity of botulinum toxin was in agreement with other studies which demonstrated the anti-cancer potential of other bacterial toxins. It was found that Coley′s toxin, which is a mixture of supernatants of
Streptococcus pyogenes and
Serratia marcescens cultures, was supposed to exhibit anti-cancer activity due to its ability to induce the release of tumor necrosis factor-α (TNF-α). In addition, the low molecular weight and hydrophobicity of theses bacterial peptides are important factors in their penetration into cancer cells which showed surface characters differ from that of normal cells (
35). Another study observed the cytotoxic potential of recombinant diphtheria toxin (DT385) against 15 cancer cell lines due to its ability to stimulate apoptosis as well as its inhibitory effect on protein synthesis in cancer cells. Moreover, DT385 showed an anti-angiogenic effect and reduced the tumor development in chick chorioallantoic membrane. In the mean time, the subcutaneous growth of Lewis lung carcinoma tumors was significantly inhibited in animal models post DT385 treatment (
36).
Current findings revealed that BTX-A could induce cytotoxicity in cancer cell lines with an IC
50 values of 7.2 and 6.4 U/mL for HCT116 and DU145 cells, respectively, without any toxicity to normal vero cells. In agreement with the present study, cytotoxic activity of BTX-A was recorded against human breast cancer (T47D) cells, with an IC
50 value of 5.3 U post 24 h treatment, in a time and concentration dependent manner. However, no effect on cellular viability was reported upon treatment with lower concentrations of BTX-A as low as 0.1 U. In the same time, greater cytotoxicity to T47D cells was observed compared to normal MCF10A cells (
11). Differences in IC
50 values between both studies could be justified by the variation among cell lines in the response to BTX-A. Also, it is worth to point out that the success of the novel cancer therapy doesn’t rely only on the cytotoxicity to cancer cells, but the specific toxicity to cancer cells in association with lower toxicity to normal cells should be taken into consideration (
37). Therefore, the currently recorded low cytotoxicity as well as the safety of captopril and BTX-A to normal vero cells, respectively, highlights the significant potentials of both drugs in minimizing the undesirable side effects on normal cells. In addition, the marked differences in cytotoxicity between cancer and vero cells could be rationalized by the variation between cancer and normal cells in the surface antigenic structure (
35).
Regarding anti-proliferative effect of captopril and BTX-A, the results showed suppression in cellular proliferation of cancer cells which was directly proportional to the increase in the concentrations of the tested drugs. In the mean context, a study reported that BTX-A reduces cellular growth and proliferation of both LNCaP and PC-3 prostate cell lines as well as in cells transformed by phospholipase C-Gamma 1 overexpression (
38,
39). While another study demonstrated that BTX-A inhibits the proliferation and showed an apoptotic effect to prostate cancer (LNCaP) but not to PC-3 cells (
40). On the contrary to the previously recorded findings, captopril didn’t show anti-proliferative effect on human mammary ductal carcinoma cells except in presence of sub-physiologic concentrations of copper salts (
41). In another study, captopril showed no anti-proliferative effect on breast tumor (MDA-MB-361), melanoma (Fem-x), cervical carcinoma (HeLa), and human myelogenous leukemia (K562) cell lines (
42). This was also justified by the reported clinical evidence of the differences in frequencies of polymorphisms within many of cancer drug-related genes which subsequently lead to variable response to anti-cancer agents (
43).
One of the major problems in treatment of cancer is the metastasis of cancer cells. Metastasis is defined as the ability of cancer cells to invade other tissues and divide inside it in uncontrolled manner. Thus, searching an effective alternative therapy to manage the problem of metastasis is of great concern, especially that conventional therapies were unsuccessful (
38). Captopril anti-metastatic potential that was recorded in the current study against colon and prostate cancer cell lines was in consistence with another study which reported that captopril could reduce the growth of colorectal cancer liver metastases
in-vivo (
44). Moreover, the anti-metastatic activity of captopril was recorded against human lung cancer (LNM35) cells which were injected in mice (
45). However, the anti-metastatic activity of BTxA was seldom reported.
P53 is a tumor suppressor gene that is activated in response to cellular stress or DNA damage and directed to induce cellular arrest in cancer cells. As a consequence to this cellular stress, p53 stimulates apoptosis via two major apoptosis-initiating pathways, designated as death receptor (extrinsic) and mitochondria-dependent (intrinsic) apoptotic pathways. The extrinsic signaling pathway that initiates apoptosis involves transmembrane receptor-mediated interactions. These involve death receptors that were members of the tumor necrosis factor (TNF) receptor. Members of TNF receptor have a cytoplasmic domain called the “death domain”. This death domain plays a critical role in transmitting the death signal from the cell surface to the intracellular signaling pathways resulting in apoptosis (
46).
The intrinsic signaling pathway that initiates apoptosis involves non-receptor-mediated stimuli releasing intracellular signals that act directly on targets within the cell. These stimuli cause changes in the inner mitochondrial membrane resulting in an opening of the mitochondrial permeability transition (MPT) pore and loss of the mitochondrial transmembrane potential accompanied with release of two main groups of pro-apoptotic proteins from the intermembrane space into the cytosol. The first group of pro-apoptotic proteins is proteins that activate the caspase dependent mitochondrial pathway including cytochrome c, Smac/DIABLO, and the serine protease HtrA2/Omi. While, the second group of pro-apoptotic proteins, namely, AIF (Apoptosis Inducing Factor), endonuclease G (Endo G) and caspase-activated DNase (CAD), are released from the mitochondria during apoptosis causing DNA fragmentation and condensation of peripheral nuclear chromatin. It is essential to focus on that the control and regulation of these apoptotic mitochondrial events occurs through members of Bcl-2 family proteins. In addition, the tumor suppressor protein, p53, has a critical role in the regulation of these proteins (
47).
Depending on the fact that p53 plays an essential role in the determining the fate of cancer cells, the therapeutic strategies that target the activation of p53-mediated apoptotic pathway could present a novel and effective pathway to destruct cancer cells (
48). Consequently, quantitation of the effect of captopril and BTxA on the expression level of a pro-apoptotic (p53) gene was performed in the present study to find out the relation between the recorded anti-cancer activities of tested drugs and their apoptotic stimulating potentials. Moreover, real time PCR was selected for evaluating the expression level as it is the most reliable and accurate method (
49). Current results revealed that the anti-cancer activity of tested drugs is related to their up-regulation potential of p53 gene which resulted in apoptosis induction. In consistence with these findings, it was reported that the cytotoxic effect of BTX-A on breast cancer cells was associated with apoptosis induction (
11). Moreover, the efficacy of injecting botulinum neurotoxin Type A was recently demonstrated in reducing the lower urinary tract symptoms accompanied by benign prostatic hyperplasia due to enhancement of apoptosis (50). Also, captopril exhibited an
in-vivo apoptotic stimulating activity against human lung cancer (LNM35) cells post injection in mice (
45).
Accordingly, the use of captopril in regulating the blood pressure in cancer patients could be beneficial in preventing the progress of their cases. Hypertension was also recorded to be a common risk factor for chemotherapy, thus captopril could be combined with chemotherapeutic agents to make use of its anticancer and antihypertensive effects (
51). In addition, there is no fear from development of cancer associated with the use of BTX-A either in cosmetic or therapeutic applications. The cytotoxic and anti-proliferative as well as the anti-metastatic efficacy of captopril and BTX-A indicated that both drugs could present a novel and potential therapeutic strategy in cancer therapy through stimulating the intrinsic pathway of apoptosis. Also, restoring p53 apoptotic potential by the effect of captopril and BTX-A may play a role in overcoming the problem of resistance to anti-cancer drugs through directing cancer cells to self-destruction with minimal effect on the neighboring normal tissues.