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Polymorphisms in Toll-Like Receptor Genes and Risk of Cancer

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Polymorphisms in Toll-Like Receptor Genes and Risk of Cancer Oncogene (2008) 27, 244–252 & 2008 Nature Publishing Group All rights reserved 0950-9232/08 $30.00 www.nature.com/onc REVIEW Polymorphisms in Toll-like receptor genes and risk of cancer EM El-Omar, MT Ng and GL Hold Department of Medicine and Therapeutics, Institute of Medical Sciences, Aberdeen University, Foresterhill, Aberdeen, UK Host genetic factors are emerging as key determinants of majority of polymorphisms studied are single nucleotide disease risk for many cancers. Identifying candidate genes polymorphisms (SNPs) that occur with a frequency of is a major challenge that has to stem from a profound >1% in the normal population (in contrast to ‘muta- understanding of the pathophysiology of the disease. The tions’ that occur with a frequency of o1%). It is Toll-like receptors are important members of the host’s estimated that up to 10 million SNPs are probably innate immune response and their genes have been found to present in the human genome though not all have thus be polymorphic. This genetic variation allows for a more far been identified. Naturally, most of these SNPs do intricate repertoire that enables the host to withstand not occur in coding sequences, and even those that do, microbial challenges. While this may be advantageous on a are not associated with any alteration in the amino acid population level, there may be less favourable outcomes for sequence and are therefore of no functional conse- individuals that harbour certain genotypes associated with quence. A more useful definition of the variability of excessive immune activation and inflammatory drive. The these SNPs involves haplotype analysis. Haplotypes are damage is often collateral and is manifest in organs where a combination of alleles at different markers along the this chronic inflammation alters normal physiology. A same chromosome that are inherited as a unit. The classic example of this paradigm is the Helicobacter pylori- HapMap project was set up to address this (www. induced gastric cancer model. Another emerging model is hapmap.org) and is a valuable tool that will facilitate prostate cancer where Toll-like receptor polymorphisms the study of genetic polymorphisms relevant to human have also been found to play a role. In this review, we health and disease. Other types of genetic variation discuss polymorphisms in Toll-like receptors and give an include deletion and insertion polymorphisms and insight into how they may influence risk of cancer. microsatellite repeat polymorphisms. Oncogene (2008) 27, 244–252; doi:10.1038/sj.onc.1210912 There has been an exponential rise in the number of published genetic association studies. Quite often, a Keywords: gastric cancer; Helicobacter pylori; genetic report of a single genetic marker is published with great polymorphisms; single nucleotide polymorphisms; promise only to be followed by several negative studies Toll-like receptors; prostate cancer that fail to reproduce the original observation. There is no doubt that the strategy of genetic association studies could be a powerful tool for dissecting human diseases, provided certain principles are observed to minimize the chances of false positive, and negative, reports. The most Introduction important of these principles are (1) rigorous definition of disease phenotype, (2) choice of candidate genes that The completion of the human genome project was a are plausibly linked to the pathophysiology of the disease momentous occasion for humanity. It opened up the under study, (3) selection of polymorphisms with known opportunity to dissect complex human traits and to (or at least potentially) functional consequences, (4) understand basic pathways of health and disease. The choice of genetic markers that are reasonably frequent in strategies for looking at host genetic factors are varied the population under study (variant allele frequency of at and include linkage analysis studies that are suitable for least 5%), (5) appropriate selection of controls that are pursuing rare high-risk alleles in conditions that have a matched for ethnicity, age, gender and environmental hereditary basis. Equally, population-based association exposures, (6) design of studies that are adequately studies are very useful for examining genes with a role in powered to produce a valid result. Even then, the commoner multifactorial diseases that have a strong statistical analyses of such studies have to take into environmental component (Risch, 2000). These associa- account the real problem of false positive results by tion studies often estimate the risk of developing a multiple testing. Appropriate corrections for multiple certain disease in carriers and non-carriers of a testing have to be applied, or alternatively, the positive particular genetic polymorphism. The overwhelming findings should be regarded as preliminary and should be validated in an independent set of cases and controls. Finally, the genetic epidemiology has to involve basic Correspondence: Professor EM El-Omar, Department of Medicine and Therapeutics, Aberdeen University, Institute of Medical Sciences, science in order to unravel and validate the molecular Foresterhill, Aberdeen, Scotland, AB25 2ZD, UK. mechanisms involved. Adherence to these basic princi- E-mail: [email protected] ples will ensure that false positive trails are minimized Toll-like receptor genes and risk of cancer EM El-Omar et al 245 and will offer a true opportunity to understand complex interact with MyD88, which subsequently lowers the multifactorial human diseases. There has never been a production of cytokines especially IL-2 (Kang and more stressing time for adherence to these principles, as Chae, 2001). The polymorphism, which causes an amino the advancement in genotyping technology has made acid change from arginine to tryptophan, has been possible the annotation of the entire human genome. reported to be associated with lepromatous leprosy in a Current technology allows us to genotype up to 500 000 Korean population (Kang and Chae, 2001) and SNPs in one run. We have witnessed a shift towards recurrent bacterial infections in Turkish children these so-called whole genome association studies where (Kutukculer et al., 2007). large multi-centre consortia attempt to examine a very The other well-described TLR2 SNP is also located in the large number of cases and controls for a particular coding region, which is at amino acid position 753 disease. The power of these studies allows for an substituting an arginine residue to a glutamine residue exploratory phase where thousands of SNPs are (Schroder et al., 2003). The polymorphism has been reported examined and a validation phase that attempts to to increase the risk of gram-negative sepsis in a Caucasian replicate positive associations independently. More population (Schroder et al., 2003). Recently, Hamann et al. awesome is the future prospect of replacing genotyping (2005) showed that carriage of the Arg753Gln SNP was also and haplotyping with direct low-cost sequencing of the a risk factor for coronary restenosis, a chronic inflammatory entire genome, the so-called ‘$1000 genome’ (Collins disease, for patients undergoing percutaneous transluminal et al., 2003). coronary angioplasty. In this review, we attempt to shed some light on the In addition to these two SNPs, Jelavic et al. (2006) role of genetic polymorphisms in the Toll-like receptor reported that the allele frequency of a TLR2 guanine- (TLR) genes and how this influences the risk of cancer. thymine (GT) microsatellite repeat polymorphism in the The basic pathobiology of these TLRs in relation to second intron has an impact on the susceptibility to cancer has been discussed extensively in the accompany- sporadic colorectal cancer. Individuals who developed ing reviews and we will concentrate on the role of sporadic colorectal cancer tended to have decreased variations in their genes. We will start by summarizing frequency of alleles 20 and 21 GT repeats and increased some of the published literature on relevant polymorph- frequency of alleles with 31 GT repeats (Jelavic et al., isms in some of the TLRs. We will then discuss specific 2006). Another single polymorphism within TLR2 examples of polymorphisms in TLRs that have been promoter region has been identified to be associated implicated in gastric and prostate cancer. with asthma in children (Yang et al., 2004). The result was supported by a larger study investigating the functionality of TLR2/16934 polymorphism with asth- ma in children of European farmers (Eder et al., 2004). Genetic polymorphisms in Toll-like receptors TLRs play an essential role in innate immunity, being involved in regulation of inflammatory reactions and Toll-like receptor 4 activation of the adaptive immune response to eliminate harmful pathogens. Hundreds of SNPs have been TLR4 is required for innate immunity to gram-negative identified in TLRs but the functional consequences of bacteria. Arbour et al. screened the entire coding region these have not been uncovered in the overwhelming of TLR4 in 82 subjects using single-strand conformation majority. Many associations have been reported be- polymorphism and direct DNA sequencing, and identi- tween TLR polymorphisms and infectious disease or fied a common SNP, an A–G substitution at nucleotide cancers and as we will see later, it is the interaction position þ 896, downstream of the cDNA start codon between infection and chronic inflammation that most (Arbour et al., 2000). This missense mutation leads to an likely mediates the increased risk of cancer
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