1. Environmental pollutants and cancer progression

The environment presents all the elements that surround us (Schmidt 2012). In the environment, humans are exposed to pollutants in many ways, including orally, by inhalation or by the dermal route. Pollution of the environment is suspected to be one of the main causes of cancer (Parsa 2012). The process of carcinogenesis is mainly divided into three stages: initiation, promotion and progression. The initiation step follows a repeated exposure to “initiators” such as oxidative stress, chemical pollutants, virus and X-rays that increase the frequency of genetic mutations. The promotion step requires a non-mutagenic stimulus known as “promoters” such as chronic inflammation, estrogens and xenoestrogens (natural or chemical compounds that imitates estrogens) that promote proliferation of the initiated cells. The progression step comprises the expression of the malignant phenotype characterised by angiogenesis and metastasis (Liu et al. 2015). Exposure to environmental compounds may interfere at all stages of carcinogenesis, in particular at the initiation and promotion stages. Several studies have evaluated the association between widespread environmental pollutants and carcinogenesis. Indeed, epidemiological studies and in vitro approaches suggest that a great number of cancers could be induced via exposure to chemicals that humans are likely to encounter in their environment (Antwi et al. 2015, Boffetta 2006, Braun et al. 2016, Rochefort 2017, Rodgers et al. 2018, Wilde et al. 2018).

The International Agency for Research on Cancer (IARC) evaluated the carcinogenic risks to humans and has classified around 120 agents as carcinogenic, where the chemical substances represent the majority (IARC 2018). There are many kinds of environmental pollutants: 1) agriculture chemicals including pesticides such as 1,1,1-trichloro-2,2-bis(4-chlorophenyl)ethane (DDT); 2) the industrial chemicals including dioxins such as 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD), metals such as arsenic compounds, plasticisers such as bisphenol A (BPA) and health care products such as phthalates; 3) the air pollutants including polycyclic aromatic hydrocarbons (PAH) such as benzo[a]pyrene (B[a]P), N-Nitrosamines such as N-Nitrosodimethylamine (NDMA), air microparticles such as sulphur dioxide and carbon monoxide; 4) drugs including exogenous hormones and 5) some natural compounds such as aflatoxines. Pollutants are characterised by their higher persistence and pervasive nature due to high lipid solubility that allows them to remain, bioaccumulate in fatty tissues and interact with the environment for a long period of time (Mathew et al. 2017). These molecules can have different mechanisms of action; they could be genotoxic or non-genotoxic which include molecules that are able to induce epigenetic modifications, to alter the endocrine system, to act as immunosuppressors or inducers of tissue-specific toxicity and inflammatory responses (Caldwell 2012, Hernández et al. 2009). In this review, we will be discussing mainly the genotoxic compounds and the endocrine disruptors.

A "genotoxic" agent is able to damage the genetic material by inducing DNA damage, mutation or both (Hayashi 1992). Genotoxicity is a key feature of carcinogenesis; it promotes chromosome changes that may be structural (such as translocations, deletions, insertions, inversions, micro-nuclei and changes in telomere length) or numerical, affecting the numbers of chromosomes as in the case of aneuploidy and polyploidy (Smith et al. 2016). Genotoxicity, due to environmental molecules, can alter the oncogenes and tumour suppressor genes that regulate processes such as cell proliferation, cell death, cell differentiation and genomic stability (Hanahan and Weinberg 2011).

Endocrine disruptors or endocrine disrupting chemicals (EDC) are pseudo-persistent compounds present in the environment at very low concentrations; however, these low levels are able to interfere with hormonal regulation pathways causing effects leading to a variety of health problems, such as cancer, specifically the hormone-dependent type (breast, ovarian, endometrial, prostate, testicular) (Abaci et al. 2009, Nohynek et al. 2013, Rachoń 2015, Rochefort 2017). Endocrine disruptors act directly with hormone receptors by imitating or preventing the action of natural hormones (Schug et al. 2016). Most of these compounds have structures similar to steroid hormones such as estrogen and could interfere with the action of this hormone through binding to estrogen receptors (ER) (Shanle and Xu 2011, Tilghman et al. 2010). It is important to mention that estrogens activate different signalling pathways known to play an important role in tumour development (Vrtačnik et al. 2014).

In Table 1, we listed some of the main environmental genotoxic molecules or endocrine disruptors that are known/thought to be implicated in the process of carcinogenesis.

Table 1. Download as CSV 

List of the most common environmental molecules (genotoxics and endocrine disruptors) and the different types of cancers developed following their exposure.

Class	Source	Compound	Mechanism of action	Target organs	References
N-Nitrosamines	Contaminated water, Preserved foods, Tobacco smoke	N-Nitrosodimethylamine (NDMA)	Genotoxic	Liver	Beebe et al. 1993, Tsutsumi et al. 1993
				Esophagus (squamous cell carcinoma)	Keszei et al. 2013
		N-Butyl-N-(4-hydroxybutyl)nitrosamine (BBN)	Genotoxic	Bladder	Chuang et al. 2014, Parada et al. 2012, Sagara et al. 2010
Polycyclic Aromatic Hydrocarbon (PAH)	Grilled meat, Tobacco smoke, Combustion of organic substances	2-Acetylaminofluorene (2-AAF)	Genotoxic	Liver	Gauttier et al. 2013, Pogribny et al. 2009, Sehrawat and Sultana 2006
		7,12-Dimethylbenz[a]anthracene (DMBA)	Genotoxic	Breast	Siddiqui et al. 2013, Wang et al. 2011
				Mouth (Buccal cheek pouch)	Mang et al. 2006
		Benzo[a]pyrene (B[a]P)	Genotoxic	Lung	Anandakumar et al. 2008a, Anandakumar et al. 2008b
				Stomach	Goyal et al. 2010
				Colon	Diggs et al. 2013
Compounds of natural origin	Aspergillus flavus, Aspergillus parasitus	Aflatoxines	Genotoxic	Liver	Johnson et al. 2014, Liu et al. 2011
	Aristolochia clematitis	Aristolochic acid	Genotoxic	Urethra	Gruia et al. 2015
Pesticides	Insecticides, Acaricides	1,1,1-trichloro-2,2-bis(4-chlorophenyl)ethane (DDT)	Endocrine disruptors	Breast	Cohn et al. 2007
				Liver	McGlynn et al. 2006
Plasticiser	Plastic products, Epoxy resin	Bisphenol A (BPA)	Endocrine disruptors	Breast	Castillo Sanchez et al. 2016, Lei et al. 2017, Mandrup et al. 2016, Xu et al. 2017, Zhang et al. 2015, Zhang et al. 2016
				Cervical	Ma et al. 2015
				Prostate	Prins et al. 2014
				Ovaries	Kim et al. 2015
				Lung	Zhang et al. 2014
				Larynx	Li et al. 2017
Dioxin	Formed during industrial process, present in dust, soil and water	2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD)	Endocrine disruptors	Lung	Chen et al. 2014
Phthalates	Plastics products, Perfumes, Cosmetics and Care products	Di-n-butyl phthalate (DBP)	Endocrine disruptors	Breast	Chen and Chien 2014, Hsieh et al. 2012
		Mono-2-ethylhexyl phthalate (MEHP)	Endocrine disruptors	Ovaries	Chang et al. 2017

2. Receptors targeted by environmental pollutants

3. The case of AhR, an established nuclear receptor in mediating environmental pollutants effects

3.2. AhR and cancer

Constitutive activation of AhR. Studies have shown that AhR can be constitutively active, presumably because of endogenous ligands and plays an important role in the biology of several cell types when exogenous ligands (environmental molecules) are absent. Schlezinger et al. (2006) reviewed the involvement of AhR in the mammary gland tumourigenesis by inhibiting apoptosis while promoting the transition to an invasive phenotype. Additionally, in a human hepatoblastoma cell line, Terashima et al. (2013) demonstrated that, under glucose deprivation, the AhR pathway induces vascular endothelial growth factor (VEGF) expression by activating transcription factor 4. In addition, knockdown or inhibition of AhR inhibits the invasion and migration of cancer cells, as well as downregulates the expression of metastasis-associated genes and tumour cells (Goode et al. 2014, Parks et al. 2014). In vivo and in vitro, D'Amato and his colleagues demonstrated that the tryptophan 2,3-dioxygenase (TDO2)-AhR pathway plays a crucial role in the anoikis resistance and metastasis of triple negatif breast cancer (TNBC) cell lines. TNBC cells regulate the enzyme TDO2, thereby causing AhR activation by this endogenous ligand kynurenine catalysed by TDO2 (D'Amato et al. 2015). Moreover, in a human breast cancer cell line MDA-MB-231, knockdown of AhR by RNAi decreased proliferation, anchorage-independent growth and migration of the cells, suggesting a pro-oncogenic function of AhR (Goode et al. 2013).

Environmental molecules that deregulate cell cycle control via AhR pathway. As cited previously, the TCDD and B[a]P represent high-affinity xenobiotic ligands for the AhR. Emerging evidence has demonstrated the role of the AhR and its ligands in cancer. A study showed that the treatment of rat liver normal cells with TCDD leads to the activation of the transcription factor JUN-D, via AhR, resulting in the transcriptional induction of the cell cycle regulator proto-oncogene Cyclin A, that provokes a release from contact inhibition (Weiss et al. 2008). Within the same cell lines, the B[a]P, also via AhR, disrupts the contact inhibition and enhances cell proliferation (Andrysík et al. 2007). Studies in a human adenocarcinoma cell line revealed that AhR agonist (TCDD) was able to stimulate the growth of cancer cells by inducing the expression of E2F/DP2 complex which is involved in cell cycle regulation and DNA synthesis (Shimba et al. 2002). Thus, the activation of AhR plays a significant role in cell cycle deregulation induced by environmental molecules.

Environmental molecules that influence apoptosis. Inhibition of apoptosis is also a factor for tumour promotion/progression. In a model for studying hepatocarcinogenesis, TCDD stimulates the clonal expansion of pre-neoplastic hepatocytes by inhibiting apoptosis (Bock and Köhle 2005). It was also demonstrated in vitro that the use of AhR antagonist abolishes resistance to TCDD-induced apoptosis in three different lymphoma cell lines. Indeed, the TCDD-mediated inhibition of apoptosis via AhR was associated with an increase in cyclooxygenase-2 (COX-2) and deregulation of genes of the B-cell lymphoma-2 (Bcl-2) family such as the anti-apoptotic proteins Bcl-xl and Mcl-1 (Vogel et al. 2007). In addition, the activation of AhR by TCDD in mouse fibroblasts represses the induction of the pro-apoptotic E2F1 target genes such as TP73 and Apoptotic protease activating factor 1 (Apaf1); however, the inhibition of AhR causes an increase in E2F1 protein that will promote apoptosis (Marlowe et al. 2008). Moreover, Bekki et al. explored the activation of AhR by TCDD and kynurenine (an endogenous ligand for AhR) and found that these compounds were able to suppress the apoptotic response induced by anti-cancer therapy in breast cancer cells and induce inflammatory genes, such as COX-2 and nuclear factor kappa-light-chain-enhancer of activated B cells subunit RelB (NF-κB) (Bekki et al. 2015). These studies showed an anti-apoptotic function of the AhR suggesting its tumour promoting role.

Environmental molecules that affect cellular plasticity. Deregulation of cell–cell contact and tumour malignancy is associated with increased AhR expression. For instance, Diry et al. (2006) highlighted the effect of TCDD and 3-methylcholanthrene via AhR on cellular motility. Dioxin stimulated cytoskeleton remodelling, resulting in an increased interaction with the extracellular matrix and loosening of the cell-cell contact. This pro-migratory activity was mediated by the activation of Jun NH2-terminal kinase (JNK) and reverted with a JNK inhibitor (Diry et al. 2006). Additionally, Andrysík et al. (2013) demonstrated that the AhR agonist TCDD was able to disrupt contact inhibition and reduce gap junctional intercellular communication via downregulation of connexin-43 in an AhR-dependent manner. In addition, activation of B[a]P-dependent signal transduction pathway, where AhR involvement is primordial in B[a]P-induced carcinogenesis, also interferes with biological processes involved in migration and invasion of breast cancer cells and Triple Negative Breast Cancer (TNBC) cells which represents the worse prognosis sub-type in breast cancer (Castillo-Sanchez et al. 2013, Guo et al. 2015, Novikov et al. 2016, Shimizu et al. 2000).

Environmental molecules that are able to induce DNA damage leading to genetic mutations. It is well known that the environmental molecule B[a]P induces, via AhR, the expression of CYP1A1, which is involved in the biotransformation of B[a]P, a procarcinogen, into B[a]P-diol-epoxide (BPDE), an ultimate mutagen with a strong electrophilic power that allows it to form DNA adducts that cause cytogenetic alterations, DNA breaks, DNA damage and mutations in oncogenes and tumour suppressor genes (Chiang and Tsou 2009, IARC 2012, Morris and Seifter 1992, Rundle et al. 2000, Tarantini et al. 2011). BPDE was demonstrated to induce K-ras mutations in normal human bronchial epithelial and fibroblast cells; these mutations have also been found in lung tumours of people exposed to the smoke of charcoal combustion during their work (Feng et al. 2002, IARC 2010).

AhR activity maintains cancer stem cells (CSC) capacity. AhR has also been reported to affect CSC, a subtype of cancerous cells and to lead to the initiation, progression and development of metastases in the carcinogenesis (Gasiewicz et al. 2017). One hypothesis assumes that tumours are maintained by a self-renewing CSC population, which is also able to differentiate into non-self-renewing cells populations that make the mass of the tumour (McDermott and Wicha 2010). Stanford et al. (2016) have shown that activation of AhR increases the development of CSC and their characteristics in TNBC cells. Furthermore, hyperactivation of AhR by B[a]P increases the activity of the stem cells specific marker, the aldehyde dehydrogenase (ALDH) and the expression of migration/invasion-associated genes such as Snai1, Twist 1, Twist2, Tgfb1 and Vim. In addition, AhR ligands increase the translocation of the sex-determining region Y-box 2, a master regulator of self-renewal, to the nucleus (Stanford et al. 2016). These data highlight the role of AhR in the development of cells with cancer stem cell-like properties and mostly the role of environmental AhR ligands in intensifying breast cancer progression. A recent study demonstrated that the AhR/CYP1A1 signalling pathway, activated by TCDD and 2,4-dimethoxybenzaldehyde, appears to be involved in the regulation (development, maintenance and self-renewal) of breast CSC via PTEN/Akt and β-catenin pathways by inhibiting the expression of PTEN and activating the expression of Akt and β-catenin (Al-Dhfyan et al. 2017).

The possible AhR biomarker value in cancer. Few studies investigated the prognosis value of AhR in cancer. In upper urinary tract tumours, the high levels of nuclear AhR expression predicted a higher tumour grade (Ishida et al. 2010). Later, it has been explored that nuclear translocation of AhR was associated with a poor prognosis in squamous cell carcinoma (Su et al. 2013). Moreover, ERα negative breast cancers exhibited a high expression of AhR, coupled with hypermethylation of the CpG islands of the BRCA1 gene promoter (or in other words with BRCA1 inactivation), suggesting that it could serve as a predictive biomarker for tumour development (Romagnolo et al. 2015). Finally, a recent study suggested the use of Memo-1, an important effector of cell migration mediated by AhR activation, as a new prognostic factor of aggressive disease in colorectal cancer patients (Bogoevska et al. 2017). Finally, Roth et al. (2009) demonstrated that AhR expression was higher in patients with a family history of upper gastrointestinal cancer exposed to PAH, revealing the deleterious effects of PAH exposure, including PAH-induced cancer.

The molecular mechanisms affected by the activation of AhR by environmental pollutants, discussed above, are represented in Fig. 1.

Figure 1.

Schematic resume representing the main effects of environmental pollutants in carcinogenesis mediated by the AhR receptor. Exogenous ligands activate AhR and affect several molecular mechanisms resulting in various genes expression that cooperate to promote carcinogenesis.

4. The case of GPER1, an emerging receptor in mediating environmental pollutants impact

4.2. GPER1 and cancer

GPER1 may promote carcinogenesis. The chemical structure of BPA that looks like E2 provides estrogenic properties to BPA (Brzozowski et al. 1997). It was demonstrated that, besides its activity through ER, BPA induces cell proliferation and migration via the GPER1/EGFR/ERK pathway in breast cancer cells (Pupo et al. 2012). In addition, the fact that BPA is able to bind GPER1 and to activate non-genomic pathways could explain these fast effects on the activation of signalling pathways, even at low doses (Richter et al. 2007, Talsness et al. 2009). For instance, at doses of 10^-9 M to 10^-12 M, BPA showed a proliferative effect on testicular cancer cells JKT-1 by activating the signalling pathways involving the protein kinase A and protein kinase G via GPER1 (Bouskine et al. 2009). Moreover, in seminoma cells, BPA was also able to promote proliferation through GPER1 (Chevalier et al. 2011). By binding to GPER1, BPA induced activation of ERK1/2 and transcriptional regulation of c-fos in human breast cancer cells via the AP1-mediated pathway (Dong et al. 2011). Additionally in breast cancer cells and through GPER1, BPA activated signal transduction pathways; it mediated migration and invasion by inducing the expression of kinases such as FAK, Src and ERK2 and by increasing AP-1 and NFκB-DNA binding activity through a Src- and ERK2-dependent pathway (Castillo Sanchez et al. 2016). Interestingly, in non-hormonal cancers, BPA binds to GPER1 and induces cancer progression in laryngeal squamous cell carcinoma and lung cancer cells (Li et al. 2017, Zhang et al. 2014). In a hypoxic microenvironment, BPA stimulated cell proliferation and migration of vascular endothelial cells and breast cancer cells in vitro by up-regulating the hypoxia inducible factor-1 alpha and VEGF expressions in a GPER1-dependent manner; and enhanced tumour growth in vivo (Xu et al. 2017). A recent study showed that one of the BPA derivatives, 4,4'-thiodiphenol, displaying more powerful estrogenic activity than BPA, was able to stimulate cell proliferation in ERα positive cancer cells by activating the GPER1-PI3K/AKT and ERK1/2 pathways (Lei et al. 2017). Therefore, more attention should be paid to BPA exposure. In addition, lower concentrations of phthalates were able to promote human breast cancer progression by inducing a proliferative effect through the PI3K/AKT signalling pathway (Chen and Chien 2014). Recent data showed that the MEHP, an environmental xenoestrogen, triggered the proliferation of cervical cancer cells within a GPER1/Akt-dependent-manner by directly binding to GPER1 (Yang et al. 2018). As for DDT, in 2006 Thomas and Dong showed that the derivative compounds of DDT displayed affinity for GPER1, but to date, data lack studies for testing the effect of DDT on carcinogenesis via the GPER1-dependent manner (Thomas and Dong 2006).

GPER1 is implicated in pathways that lead to the activation of the transcriptional machinery. Studies have demonstrated the involvement of GPER1 in cell proliferation, cell survival and cell migration mechanisms by inducing the transcription of genes such as cyclin D2, Bcl-2, connective tissue growth factor (CTGF) and the oncogene c-fos etc. (Kanda and Watanabe 2003, Kanda and Watanabe 2004, Maggiolini et al. 2004, Pandey et al. 2009). These data suggest possible roles for GPER1 in the development of metastases and in the resistance to anti-estrogens. The role of GPER1 in promoting cancer is also reinforced with the presence of a cross talk between GPER1 and the insulin-like growth factor receptor-1 which is associated with multiple tumour progression characteristics, such as the development of metastases and resistance to chemotherapy by triggering downstream pathways, such as ERK and AKT (De Marco et al. 2013, Knowlden et al. 2008, Lappano et al. 2013).

The possible GPER1 biomarker value in cancer. Several studies have highlighted the use of GPER1 as a cancer biomarker. The results of a clinical study showed that the expression of GPER-1 might correlate with clinical and pathological-poor outcome biomarkers, by showing an association with metastasis, human epidermal growth factor receptor 2 (HER2) expression and tumour size (Filardo et al. 2006). GPER1 has also been shown to be an important prognostic factor in high-risk endometrial cancer patients with lower survival rates (Smith et al. 2007). High expression levels of GPER1 have been correlated with low survival rates in breast cancer patients treated with tamoxifen and in patients with the aggressive epithelial ovarian cancer (Ignatov et al. 2011, Smith et al. 2009). In silico, a bad prognostic value for high levels of expression of GPER1 in HER2+ breast cancers subtype was obtained (Yang and Shao 2016). As well, Fahlén et al. (2016) have found that malignant breast tumours showed a high expression of GPER1 compared to benign tumours. Interestingly, a recent study showed that GPR30 expression was observed in both the cytoplasm and nucleus of cells from ovarian cancer tissues where the nuclear GPER1 expression predicts poor survival in patients with ovarian cancer, especially in those with a high grade malignancy (Zhu et al. 2018). To date, there is no study showing a correlation between the environmental carcinogen exposure and GPER1 expression to be used as a biomarker.

The molecular mechanisms affected by the activation of GPER1 by environmental pollutants, discussed above, are represented in Fig. 2 .

Figure 2.

Schematic resume representing the main effects of environmental pollutants in carcinogenesis mediated by GPER1 receptor. Exogenous ligands activate GPER1 and affect several molecular mechanisms resulting in various genes expression that cooperate to promote carcinogenesis.

5. Conclusion

Acknowledgements

Funding program

Grant title

Hosting institution

Ethics and security

Author contributions

Conflicts of interest

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