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role in cancer susceptibility. In a case-control study done by Jiang et al. it was
reported that rs417309 in DGCR8 was consistently associated with breast cancer risk
in Chinese women with an odds ratio (OR) of 1.50 (95% confidence interval
(CI) ¼ 1.16–1.93) (Jiang et al. 2013a). Another report also shows Non-coding
RNA associated rs2291109 (A > T) in DROSHA with increased breast cancer
susceptibility [Odds ratio (OR) ¼ 0.81; 95% Confidence Interval (CI) 0.66–0.99]
in Chinese patients.
Exportin 5 Exportin 5(XPO5) is a nucleo-cytoplasmic transporter protein classified
as a member of the importin-β family of proteins. XPO5 is responsible for nuclear
pre-miRNA transport and stabilization in a RAN-GTP dependent manner
recognizing it to be a rate-limiting step in miRNA biogenesis. Leaderer et al. in
their study demonstrated that two missense SNPs in XPO5, rs34324334 (S241N)
and rs11544382 (M1115T), have significant associations with breast cancer risk
(OR ¼ 1.59, 95% CI: 1.06–2.39). They also reported that the variant alleles of both
rs11544382 (OR ¼ 1.82, 95% CI: 1.09–3.03) and rs34324334 (OR ¼ 1.76, 95% CI:
1.10–2.83) were ominously associated with breast cancer risk in post-menopausal
women (Leaderer et al. 2011).
RAS-Related Nuclear Protein (RAN) RAS-Related Nuclear Protein (RAN) is a
small G protein essential for the translocation of pre-miRNA and proteins through
the nuclear pore complex in a RAN-GTP dependent manner. Polymorphism in RAN
can alter miRNA transport and expression and may contribute to pathogenic
changes. RAN protein is also involved in downstream regulation of the PI3K
signaling pathway, which is further involved in cancer cell invasion and metastasis.
Cho et al. reported that RAN rs14035 along with CT + TT genotype was associated
with decreased colorectal cancer (CRC) risk in male patients without diabetes
mellitus (DM) as well as in patients with rectal cancer. Additionally, they reported
that RAN rs14035 CC genotype was related to a decreased risk of CRC with respect
to tumor size and metabolism of homocysteine and folate (Cho et al. 2015).
However, such studies revealing the association between RAN and breast cancer
risk are yet to be reported.
DICER DICER1 is an enzyme which is responsible for the cleavage of miRNA
precursors. It is known to be involved in the oncogenic process of different cancers.
Pre-miRNA processing is mediated by DICER1along with a TARBP2
(transactivation-responsive RNA-binding protein2). TARBP2 is a protein factor of
the miRNA loading complex (includes DICER1, AGO2, and TRBP2) that are
essential for the formation of RNA-induced silencing complex (RISC) (Osuch-
Wojcikiewicz et al. 2015). In a population-based case control study done in Korean
Women, Sung et al. reported that no association between rs1057035 (C > T), located
in the 3
0
-UTR of DICER and risk of breast cancer (OR ¼ 0.64, 95% CI: 0.23–1.77,
P ¼ 0.39), However, they reported that DICER1 rs1057035 was significantly
associated with both disease-free survival (DFS) and overall survival (OS). Conse-
quently, they reported that the genetic variants TC/CC of rs1057035 were found to
3 Impact of MicroRNA Polymorphisms on Breast Cancer Susceptibility 63
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be associated with disease progression by 1.72-fold increase (95% CI, 1.00–2.99)
and risk of death by2.08-fold increase (95% CI, 1.01–4.28) (Sung et al. 2011;
Bermisheva et al. 2018).
Argonaute 1 (AGO1) and 2 (AGO2) Argonaute RISC Component 1 (AGO1) and
2 (AGO2), also identified as “Eukaryotic Translation Initiation Factors 2C 1 and
2 (EIF2C1/2),” belong to Argonaute protein family. These Argonaute proteins bind
to mature miRNA to form RNA-induced silencing complex (RISC), which carries
miRNAs to their target 3
0
UTR binding sites. Argonaute proteins have several key
roles, as in transcriptome silencing, immune system regulation, cell differentiation,
and angiogenesis. Fawzy et al. reported significant association between genetic
variants rs636832 and rs2977490 of AGO1 and AGO2 proteins, respectively, on
breast cancer (BC) risk in Mediterranean population. They proved that AGO1*G
variant showed a significant BC risk under recessive model [adjusted odds ratio
(95% confidence interval); 4.90 (1.03–23.39), P ¼ 0.024], and was also associated
with lymph node infiltration (P ¼ 0.037), distant metastasis (P ¼ 0.019), advanced
clinical stage (P < 0.001), recurrence (P ¼ 0.032), and shorter overall survival
(P ¼ 0.001). Furthermore, AGO2*G/G genotype exhibited association with poor
pathological grade (P ¼ 0.029) (Fawzy et al. 2020).
3.2.2 SNPs in miRNA 3
0
UTR Region and Breast Cancer
SNPs located in the 3
0
UTR of the target mRNAs are referred to as poly-miRs
responsible for alteration in polyadenylation, protein-mRNA interactions, which
can either facilitate or hinder miRNA–mRNA interactions (Slaby et al. 2012).
Consistent with the predominant role of miRNAs in gene regulation, some SNPs
in miRNA 3
0
UTR region of miRNA-bindi ng site are found to interfere with miRNA
function and lead to differential gene expression. Increased expression levels of
SET8 expression were observed in various cancer types. SNP locus rs16917496
(T > C) in the 3
0
-untranslated region (3
0
-UTR) of SET8 a polymorphism within
miR-502 binding site was reported to be associated with susceptibility to breast
cancer. SET8 can alter cancer prognosis by modifying its expression, which could be
suppressed by miR-502 (Liu et al. 2016). The SNPs rs1051424 and rs11704 were
observed in the putative target sites of miRNA within the 3’-UTR of RPS6KB1 and
ZNF839, respectively. RPS6KB1, is a ribosomal protein S6 kinase B1, that belongs
to S6 kinase family of serine/threonine kinases which are found to be regulated by
phosphatidylinositol 3-kinase (PI3K)/Akt/mammalian target of rapamycin (mTOR)-
pathway. It was reported that RPS6KB1 located on chromosome 17q23 is often
amplified and overexpressed in breast cancer, and this phenotype correlates with
poor prognosis (Yang et al. 2017). Current ly, it is reported that 27 single nucleotide
polymorphisms noticed in the 3
0
UTR zone of the miRNA genes are detected to be
associated with the increased risk of breast cancer as shown in (Table 3.2).
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Table 3.2 Association of miRSNPs and their respective genes with breast cancer susceptibility
Gene Gene function SNP
Genetic
variants Modified microRNA
Association with breast
cancer References
ESR 1 Nuclear hormone receptor
involved in the regulation of
eukaryotic gene expression
increase cellular proliferation in
breast tissue
rs2747648 C/ T miR-453 Increased breast cancer
risk
Tchatchou et al.
(2009)
rs1062577 T/ A miR-3636, miR-3662
And miR-186
Increased BC risk Dehghan et al.
(2017)
TGFBR1 Positive regulation of cell
proliferation
rs686 miR-let-7b TGFBR1 tumor-specific
mutation in breast
cancer
rs334348 G-- > A miR-628-5p Increased breast cancer
risk
Nicoloso et al.
(2010)
BRCA1 DNA repair rs799917 T ˃ C miR-638 Increased breast cancer
risk
Shi et al. (2017)
rs8176318 G > T miR-1182
miR-544
miR-639
miR-149 and
miR-345
Increased BC risk Ahmad et al.
(2019)
BRCA2 Promoting uncontrolled cellular
proliferation
rs11169571 C ˃ T miR-320 Increased breast cancer
risk by two folds
Kontorovich
et al. (2010)
RNF 115 Promote proliferation possibly
through downregulation of the
expression of the tumor
suppressor
p21
rs17354678 T/C miR-486-5p Increased breast cancer
risk
Jacinta-
Fernandes et al.
(2020)
(continued)
3 Impact of MicroRNA Polymorphisms on Breast Cancer Susceptibility 65
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Table 3.2 (continued)
Gene Gene function SNP
Genetic
variants Modified microRNA
Association with breast
cancer References
ErbB4 Cell cycle arrest rs13423759 C ˃ A miR-548 Bidkani et al.
(2018)
rs12471583 (c.
*3622A > G)
miR-511-5p,
miR-4659a-5p,
miR-4659b-5p, and
miR-6830-3p
Associated with ER/PR
negativity and advanced
breast cancer
Tabatabian et al.
(2020)
RAD 52 DNA repair and meiotic and
mitotic recombination
rs7963551 A > C Let-7 Reduced breast cancer
risk
Jiang et al.
(2013b)
IQgap 1 Negative regulation of rs1042538 A/T miR-124 Increased breast cancer
risk
Zheng et al.
(2011)
Itgb4 Intracellular signaling pathways
that control growth,
differentiation, apoptosis, cell
motility, migration, and survival
rs743554 G/A miR-34a Increased breast cancer
associated risk
Brendle et al.
(2008)
MMP9 Tumor invasion and metastasis
cellular differentiation
rs1056628 A > C miR-491-5p Increased breast cancer
menace
Pirooz et al.
(2018)
SET 8 Transcriptional activation of the
p53 protein; cell cycle
progression; apoptosis
rs16917496 T/C miR-502 Increased breast cancer
risk at an early age
Song et al.
(2009);Wei et al.
(2018)
KRAS Abnormal changes of normal
cells, and to accelerate the
formation of the tumor solid
rs61764370 T˃G Let-7 Increase the BC risk Sanaei et al.
(2017);
Mohthash et al.
(2020)
rs712 G/T Let-7 No association on BC
risk
Huang et al.
(2011), Du et al.
(2017)
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3.2.3 SNPs in Pri-, Pre-, Mature miRNA and Breast Cancer
Susceptibility
Breast cancer has a genetic predisposition attached to its occurrence. SNPs are
commonly observed in the mature miRNA, pre- and pri-forms of the miRNA
sequence with a potential towards altering the processing and their binding of
miRNAs to their target genes. Polymorphisms occurring in the seed region of a
microRNA gene may contribute to its oncogenic or tumor suppressive functions and
subsequently affect cancer risk or susceptibility.
Hu et al. investigated the associations of SNPs (rs2910164, rs2292832,
rs11614913, and rs3746444) linked to the pre-miRNAs transcript types (hsa-mir-
146a, hsa-mir-149, hsa-mir-196a2, and hsa-mir-499) with breast cancer susceptibil-
ity in Chinese female population and reported that hsa-mir-196a2 rs11614913:T > C
and hsa-mir-499 rs3746444:A > G variant genotypes were significantly associated
with increased risks of breast cancer (odds ratio, 1.23; 95% confidence interval,
1.02–1.48 for rs11614913:T > C; also OR, 1.25; 95% CI, 1.02–1.51 for rs3746444:
A > G in a dominant genetic model (Hu et al. 2009). Zhao et al. in their study
reported that SNP rs6505162 in pre-miR-423 affects the mature miR expression, and
miR-423 has definitely an oncogenic role in breast tumorigenesis (Zhao et al. 2015).
Aberrant expression of miR-146a was reported in breast cancer tissues. A G > C
polymorphism (rs2910164) was identified in the miR-146a precursor, that can lead
to mismatch in base pair sequence from a G: U pair to a C: U particularly in its stem
region (Lian et al. 2012).
Shen et al. identified that rs2910164 can lead to the pathogenesis of breast cancer,
this is because BRCA1 and BRCA2 key breast cancer genes are the target genes of
miR-146a.miRNAs due to their multitudinous functions might also be used as
biomarkers for the early diagnosis of cancer. Consequen tly, patients susceptible to
breast cancer possessing at least one miR-146a-variant allele could be diagnosed
earlier than the patients with no corresponding variant allele (Shen et al. 2008).
Bahreini et al. found a link between SNP in miR-559 and breast cancer susceptibil-
ity. They reported that the miR-559 SNP rs5845 0758 that is located in the coding
region of the pre-miR-559 hairpin stem-loop structure was associated with increase
in risk of breast cancer incidence. According to their reports, the non-dominant
genotypes (CT + TT) were found to be associated with breast cancer in patients
(OR 3.62; 95% CI, 1.95–6.69; p < 0.0001) (Bahreini et al. 2020).
Through a meta-analysis Tan et al. reported statistically significant association
between mir-499a rs3746444 polymorphism and an increased breast cancer suscep-
tibility under all genetic models (homozygous, OR ¼ 1.33, 95% CI ¼ 1.03–1.71,
P ¼ 0.03; heterozygous, OR ¼ 1.08, 95%CI ¼ 1.00–1.16, P ¼ 0.04; dominant,
OR ¼ 1.15, 95% CI ¼ 1.02–1.30; P ¼ 0.03; recessive, OR ¼ 1.35, 95%
CI ¼ 1.06–1.72, P ¼ 0.01; allele, OR ¼ 1.12, 95% CI ¼ 1.00–
1.26, P ¼ 0.04)
(Tan et al. 2020).
3 Impact of MicroRNA Polymorphisms on Breast Cancer Susceptibility 67
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3.2.4 SNPs in miRNA-Coding Genes
miR-let 7 Du et al. explored the effects of polymorphism on miR-let-7-related
genes (mirSNPs) on breast cancer risk and clinical outcomes. They reported that
rs1042713 in the ADRB2 gene was associated with the susceptibility to both
HR-positive and HR-negative breast cancer. This association was attributed to the
conformational change in the protein, induced by rs1042713 in the ADRB2 gene
which might have led to changes in the interaction within the signaling pathways,
advancing to carcinogenesis in both HR-positive and HR-negative breast cancer.
Additionally, they demonstrated that HIF1AN rs11292, a let-7 miRNA-related SNP
(mirSNP), was associated with breast cancer risk. Moreover, they proved that
rs1017105 CLDN12 expression can be regarded as an independent predictor of
poor disease-free survival rate in ER-negative breast cancer patients (Du et al. 2019).
miR-27a The miRNA-27 family consists of miR-27a and miR-27b, and the former
plays a vital role in tumor development. The G-allele of rs895819 (A > G), located
in the terminal loop of the pre-miR27a oncogene, was reported to be significantly
associated with reduced familial breast cancer risk (OR ¼ 0.88;95% CI: 0.78–0.99)
study done in German population (Li et al. 2019).
miR-34 SNP rs4938723 CC of miR-34b/34c genotype was reported to be
associated with decreased breast cancer mortality. Bensen et al. reported no signifi-
cant association between the pri-miR-34b/c rs4938723 variant and susceptibility to
BC, and found that this polymorphism was in fact associated with BC survival
(CC vs. TT + TC: hazard ratio, 0.57; 95% CI, 0.37–0.89; P ¼ 0.01) (Sanaei et al.
2016).
miR-146a The functional microRNA polymorphisms miR-146a rs2910164 G > C
is reported to be associated with breast cancer (BC) risk. A meta-analysis done by
Zhang et al. 2017 testified that rs2910164 polymorphism has no association with
breast cancer risk (Zhang et al. 2017).
miR-196a2 miR 196a2 is a miRNA gene that is aberrantly expressed in BC in
comparison with normal tissues. Its over expression was reported to be a biomarker
for the prognosis of BC patients. The variant rs11614913 in pre-miR-196a2
represents a miRNA variant that can extend in the mature miR-196a2 sequence. This
SNP rs11614913 not only affects the maturation of mir-196a but also the regulation
of the target mRNA. Moreover, it is reported that the SNP rs11614913 is associated
with augmented susceptibility to BC. The predicted targets for miR-196a2 are
DHFR and Thymidylate synthase. A recent meta-analysis substantiated that the
rs11614913 CC genotype of miR-196a2 was known to be linked with an increased
breast cancer risk compared with the TT + CT genotypes (Zhang et al. 2014).
miR-423 microRNA-423 is an oncogenic factor which is frequently upregulated in
cancer. This gene has coding sequences for miR- 423-3p and miR-423-5p. The
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polymorphism rs6505162 at the 3
0
non-coding sequence located within hsa-mir-423
miRNA gene was reported to be associated with breast cancer (Kontorovich et al.
2010).
miR-499 Afsharzadeh et al. in their study reported that rs11614913 (T to C)
together with miRSNP A to G (rs3746444) in mir-499 is significantly associated
with increased breast cancer susceptibility. In addition to this a miRSNP C to T
(rs93410170) in the 3
0
UTR of the estrogen receptor-α (ER-α) was implicated in
breast cancer susceptibility by modulating miR-206. Moreover, an integrin, β-4
SNP, was predicted to influence breast cancer survival and tumor aggressiveness.
Here a chromosomal translocation was responsible for alteration in the let-7 miRNA
mediated regulation of group A2 with high mobility leading to oncogenic transfor-
mation) (Afsharzadeh et al. 2017).
miR-520f Meshkat et al. in their study demonstrated that the GA genoty pe of the
rs75598818 SNP, on stem-loop region of the mir-520f reduced risk of BC develop-
ment (GA versus GG, OR ¼ 0.50, 95% CI: 0.25–0.98, P ¼ 0.041). Moreover, they
even reported that A allele mir-520f rs75598818 might lead to reduced production of
miR520f-3p, a tumor suppressor miRNA with a role in pathogenesis of BC. They
showed that the GA genotype might be associated with HER-2 positivi ty. Their
findings suggest a possibility of varied functional aspects attributed to miR-520f-3p
in normal and breast cancer cells.
Similarly, SNPs in miR-559 (rs58450758) and miR-618 (rs2682818) were reported
to be associated wi th incre ase breast cancer susceptibility. SNPs in the microRNA
genes which were studied until recently are discussed in (Table 3.3).
3.3 Therapeutic Implications of miRNA
There is enormous research done in the discovery of miRNA and its association with
diseases. Rendering the therapeutic usefulness of miRNAs into clinical setting has
been improvised by the utilization of novel high-throughput technologies on a
variety of patient samples, like blood, tissue, serum, cerebrospina l fluid and (fresh
and formalin-fixed paraffin-embedded [FFPE]). These technologies are not only
known to lower the laboratory costs, enhance operational productivity, and the
yield but also to decipher smaller molecules. Albeit, there are enormous therapeutic
implications associated with miRNAs, yet the emergence of miRNA drug candidates
has not taken a lead to be translated into FDA approved drug molecules, they are
dormant either in Phase I or Phase II clinical trials. miRNA therapeutics is the most
widely evolving treatment modality with its clinical applications not limited to
cancer malignancies alone but involve a wide array of diseases like cardiac
disorders, sepsis, neurological ailments, hepatic disorders, etc. (Sethi et al. 2018).
However, miRNAs targeting is most prominently used in onco-therapeutics opening
a new genre of cancer treatment. For example, miR-17 family is currently being
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Table 3.3 SNPs in miRNA-coding region
MicroRNA
type Gene target
Genetic
variants
Associated
polymiR
Association
with breast
cancer References
miR-10b HOXD10,
TBX5, KLF4,
PTEN, and
syndecan-1
AG/GG rs4078756 Increased BC
risk
Chen et al. (2017)
miR-27a SPRY 2;
TMEM170B;
BAK; SET8
C˃T;
A > G
rs895819 Decreased
risk of breast
cancer
Mashayekhi et al.
(2018), Barjui
et al. (2017),
Morales et al.
(2018), Li et al.
(2019), Dai et al.
(2020)
miR-34a p53 GA/AA rs72631823 Increased risk
of TNBC
Kalapanida et al.
(2018)
miR-34 b/c p53 T/C rs4938723 Debatable Sanaei et al.
(2016)
miR-101 SOX2 and
NRF2
C > G rs1053872 Increased risk
of BC
Yi et al. (2019)
C˃T rs462480 Increased risk
of BC
C > G rs7536540 No
association
miR-146a ERBB2 G/C rs2910164 Dubious Bodal et al.
(2017), Zhang
et al. (2017),
Meshkat et al.
(2018)
miR-185 RhoA and
Cdc42
C/T rs2008591 Reduced risk
of BC
Bensen et al.
(2013)
A/G rs887205 Reduced risk
of BC
Bensen et al.
(2013)
miR-196a2 BRCA1 C
˃T rs11614913 Controversial Bodal et al.
(2017), Dai et al.
(2016), Morales
et al. (2018)
miR-218-2 SLIT2 G/A rs11134527 Increased risk
of BC
Danesh et al.
(2018)
miR-301b CDKN2A,
LMNB1
rs384262 Danesh et al.
(2018)
miR-423 NSRP1 C/A rs6505162 Debatable Smith et al.
(2012); Moazeni-
Roodi et al.
(2019),
Pourmoshir et al.
(2020)
(continued)
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scrutinized as a therapeutic option for the treatment of vulvar carcinoma. Treatment
of cancer is made possible by two methods; one is to inhibit the overtly expressed
miRNA using antisense miRNA derivatives called antisense oligonucleotides,
antagomiRs, miR sponges or LNA constructs. Second method is called “miRNA
replacement therapy” which helps in restoration of tumor suppressive miRNAs’
using miRNA mimetics like siRNA-like duplex or chemically modified
oligoribonucleotide. Anti-miRNAs are used to target diseases causing miRs.
Miravirsen is the only miRNA-based drug until now that has reached clinical trials.
Miravirsen is locked nucleic acid (LNA) antisense oligonucleo tide inhibitor which
targets miR-122 (Kwok et al. 2017). Furthermore, Hepatitis C virus (HCV) infected
patients were tested with Anti-miR-122. Anti-miR-10b was shown to reduce metas-
tasis of breast cancer in animal studies. In spite of the wide therapeutic applications
and inevi table role of miRs in treatment of variety of diseases, further studies related
to their precise mechanism of action and identifying their targets are warranted
(Seven et al. 2014).
Table 3.3 (continued)
MicroRNA
type Gene target
Genetic
variants
Associated
polymiR
Association
with breast
cancer References
miR-499 FOXO4,
PDCD4,Sox6
and rod 1
AG/GG rs3746444 Increased risk
of BC
Dai et al. (2016),
Tan et al. (2020)
miR-520f ERBB2 G/A rs75598818 Decreased
susceptibility
to BC
Meshkat et al.
(2018)
miR-559 ERBB2,
MTA1,
MTA2,
CCND1 and
ULK1
C > T rs58450758 Increase
breast cancer
susceptibility
Bahreini et al.
(2020)
miR-605 ABL2,
KRAS,
RAF1, CBL,
ELK1, ETS1
and MDM2
A > G rs2043556 Increase
breast cancer
susceptibility
Kazemi and
Vallian (2020)
miR-618 LPR12 C > A rs2682818 Increased BC
risk in
non-familial
early-onset
BC
Morales et al.
(2016)
3 Impact of MicroRNA Polymorphisms on Breast Cancer Susceptibility 71
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3.4 Conclusion and Future Prospects
Over the past decade, the number of experimental studies on miRNAs has increased
exponentially, but the data gathered, and the novice miRNA being discovered
advocates that we are still at the beginning. Consequently, microRNAs (miRNAs)
gene regulators are being considered as of paramount clinical importance due to their
involvement in wide array of processes such as cancer diagnosis and predicting their
usefulness as prognostic biomarkers and novel anticancer therapeutic agents that can
be used alone or in combination with current targeted therapies. The discovery of
single nucleotide polymorphisms (SNPs) in the miRNA regions or transcripts along
with binding sites or target genes could provide insights about the link between
associations of various miRSNPs and susceptibility of cancer. Single nucleotide
polymorphisms (SNPs) are benign genetic variants that are extensively studied in
several diseases to know their exact mechanism. However, changes or SNPs in miRs
can alter various activities of protein formation and function like expression, binding
affinity folding, etc. Moreover, elaborate knowledge of miRSNP their potential
mechanisms can be used to identify several cancer subtypes and classify cancer
patients accordingly. Not only this, it can be used to provide better treatment options
with accuracy and efficacy. Therefore, further characterization of miRSNPs along
with more association studies with larger sample sizes is warranted to make accurate
predictions of cancer risk and can provided better diagnostic tests.
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