Genetic polymorphisms in the TERT-CLPTM1L region and lung cancer susceptibility in Chinese males

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1 1588 Genetic polymorphisms in the TERT-CLPTM1L region nd lung cncer susceptibility in Chinese mles XUYANG XIAO 1 nd WUBIN HE 2 1 Deprtment of Thorcic Surgery nd 2 Biologicl Therpy Center Lbortory, The First Affilited Hospitl of Jinzhou Medicl University, Jinzhou, Lioning , P.R. Chin Received Jnury 25, 2017; Accepted My 18, 2017 DOI: /ol Abstrct. The objective of the present study ws to nlyze the reltionship between genetic polymorphisms of the rs locus of the telomerse reverse trnscriptse (TERT) gene nd the rs locus of the cleft lip nd plte trnsmembrne protein 1 (CLPTM1L) gene nd the risk of developing lung cncer in mles in Jinzhou. A totl of 214 lung cncer ptients who were dmitted in Jinzhou Medicl University were nlyzed, nd 216 helthy mles were selected s controls. Venous blood from ll subjects nd dt on relevnt risk fctors were collected. DNA ws extrcted from peripherl blood by the phenol-chloroform method. Rel-time fluorescent quntittive PCR (TqMn rel time PCR) ws used for DNA mplifiction. The genotyping results of the genetic polymorphisms of the TERT rs nd CLPTM1L rs loci were detected. The risk of developing lung cncer in the popultion with the TERT rs locus crrying the T llele ws times tht with the TERT rs locus crrying the C llele fter djustment of the ge fctor. The risk of developing lung cncer in the popultion crrying the TT mutnt genotype nd the CT genotype incresed significntly compred with tht crrying the CC wild genotype [odds rtio (OR)=1.815, 95% CI= ; OR=2.417, 95% CI= ]. Bsed on comprison between the combintion of the two mutnt genotypes (CT+TT) nd the wild homozygous genotype (CC), the mutnt genotype incresed the risk of developing lung cncer (OR=1.955, 95% CI= ). The risk of developing lung cncer in the popultion with the CLPTM1L rs locus crrying the T llele ws times tht crrying the C llele (OR=1.343, 95% CI= ). The popultion with the TERT rs locus crrying the mutnt genotype (CT+TT) ws ssocited with the number of tumors Correspondence to: Dr Wubin He, Biologicl Therpy Center Lbortory, The First Affilited Hospitl of Jinzhou Medicl University, 2 People's Street, Gut, Jinzhou, Lioning , P.R. Chin E-mil: w0f8v5@163.com Key words: telomerse reverse trnscriptse, cleft lip nd plte trnsmembrne protein 1, lung cncer, mononucleotide polymorphism, hereditry susceptibility (OR=0.553, 95% CI= ). In conclusion, in mles, the TERT rs nd CLPTM1L rs T lleles re the susceptibility fctors for developing lung cncer. Individuls, including the smoking popultion, who crry both the TERT rs nd CLPTM1L rs T lleles re more likely to develop lung cncer. Introduction Tumorigenesis is multi-fctor, multi-stge, nd multi-gene process. In ddition to environmentl fctors, dietry fctors, biologicl fctors, nd hereditry fctors ply importnt roles in tumor progression (1,2). Genetic susceptibility is determined by single nucleotide on the individul genome (3,4). During tumorigenesis, environmentl fctors ply n inititing role, while hereditry fctors determine the susceptibility of individuls to tumorigenesis. In recent yers, reserch on genetic susceptibility to tumors hs ttrcted much ttention. Recent reserch in moleculr epidemiology hs imed to identify nd determine the mutnt loci of tumor-relted genes, nd further study the interctions between the environment nd genes, nd the interctions between genes by studying mononucleotide polymorphisms (4). Within DNA sequence, polymorphisms rising from muttion of single nucleotide (A, T, C, nd G) re clled single nucleotide polymorphisms (SNPs) (5). SNPs re mjor form of genome polymorphism (6). The gene coding region of n SNP is clled coding region SNP (csnp), which my led to chnges in the mino cid sequence of proteins, nd chnges in protein function. csnps hve importnt biologicl significnce (7). Bsed on estimtion, 1 in 1,000 people hve one SNP in the genome. The 3 billion humn bsic groups hve totl of over 3 million SNPs (8). Different individuls hve different susceptibilities to crcinogenic fctors in the environment becuse of polymorphisms. Therefore, SNPs cn be used to screen popultions susceptible to tumors in rpid nd lrge-scle mnner. Reserch on SNPs relted to tumors hs lso been focus in moleculr epidemiology in recent yers. The chromosome 5p15.33 region hs two known genes, humn telomerse reverse trnscriptse (TERT) nd cleft lip nd plte trnsmembrne protein 1 (CLPTM1L) (9-11). These genes hve multiple cncer risk loci nd my be ssocited with tumorigenesis. TERT is the ctlytic subunit of telomerse, nd is locted on chromosome 5p It spns 35 kb, nd comprises 16 exons

2 XIAO nd HE: GENETIC POLYMORPHISMS IN THE TERT-CLPTM1L REGION AND LUNG CANCER SUSCEPTIBILITY 1589 nd 15 introns. It is rte-limiting fctor for synthesizing the telomerse holoenzyme (12). Its expression correltes with the expression of telomerse. Chnges in TERT cn lso reflect corresponding chnges in the ctivity of intrcellulr telomerse (13). TERT is n importnt trget site for inhibiting telomerse ctivity. TERT cn increse the risk of tumors by influencing telomerse ctivity nd telomere length. In ddition, telomerse prticiptes in processes such s poptosis, DNA dmge repir, nd regultion of gene expression, thus influencing tumorigenesis nd progression (14,15). The CLPTM1L gene encodes for trnsmembrne protein, which induces poptosis in cispltin-resistnt cell lines. It is expressed in multiple norml nd mlignnt tissues such s the skin, lung, ovry, cervix, nd thymus (16,17). However, the functions of CLPTM1L, nd its role in tumorigenesis remin uncler. At present, CLPTM1L hs been confirmed to be overexpressed in humn ovrin tumor cell lines nd is resistnt to cispltin. CLPTM1L overexpression in pulmonry tumor cells cn protect them from poptosis induced by genotoxic stress, indicting tht it my hve ntipoptotic function. CLPTM1L is lso highly expressed in other tumor tissues. The forementioned observtions suggest tht CLPTM1L my be ssocited with the genesis of multiple tumor types. The genome-wide ssocition study reported tht the SNPs, TERT rs nd CLPTM1L rs401681, re significntly correlted with cncer risk (18). Regrding reserch on the reltionship between genetic polymorphisms of specific loci nd lung cncer susceptibility, Zhng et l studied the reltionship between the genetic polymorphism t rs , nd the risk of developing lung cncer in 400 lung cncer ptients nd 400 helthy subjects (controls) in the Asin popultion in Their results showed tht genetic muttion t the rs locus increses the risk of developing lung cncer (19). Currently, there is no reserch on the reltionship between the rs locus nd the risk of developing lung cncer. Using cse-control design method, the im of the present study ws to nlyze the reltionship between the genetic polymorphism of the rs locus of the TERT gene nd the rs locus of the CLPTM1L gene nd the risk of developing lung cncer in mles in Jinzhou city. Ptients nd methods Selection of reserch subjects. Mle ptients definitely dignosed with lung cncer bsed on histopthology who received opertive tretment in Grde 3, Clss A hospitls in Jinzhou city were selected, with cse-control reserch method, nd ssigned to the cse group. Inclusion criteri for the cse group: i) mle; ii) primry lung cncer, excluding metsttic lung cncer nd iii) received no chemotherpy or rdioctive therpy. A totl of 201 lung cncer ptients ged from 30 to 87 yers who sought medicl dvice in Grde 3, Clss A hospitls in Jinzhou city from 2008 to 2013 were included s reserch subjects. In ddition, 211 helthy mles who underwent physicl exmintions in the physicl exmintion center during the corresponding period were selected s controls using the frequency mtching method. All reserch subjects signed n informed consent form. Next, blood smples from ll reserch subjects were collected. Dt on demogrphic chrcteristics, relevnt clinicl indexes, nd exposure to environmentl fctors were obtined by questionnires. This study ws pproved by the Ethics Committee of the First Affilited Hospitl of Jinzhou Medicl University. Signed written informed consents were obtined from ll prticipnts before the study. Epidemiologicl investigtion. Uniformly prepred questionnires were used. An epidemiologicl investigtion into the reserch subjects ws mde by two trined investigtors. The content of the investigtion included demogrphic dt (nmes nd ges), smoking history, nd clinicl indexes. Non-smokers referred to individuls who smoked <100 cigrettes in their lives. The relevnt clinicl indexes were grouped ccording to the rnge of stndrd reference vlues. All investigtion dt were checked repetedly nd coded. A dtbse ws estblished with the EpiDt softwre version 3.5 (Tree str Inc., Ashlnd, OR, USA), nd dt were entered. DNA extrction. Frozen nticogulted blood from lung cncer ptients ws thwed in wter bth t 37 C. A totl of 1 ml of whole blood ws tken, nd 4 ml of erythrocyte lysis buffer (Sigm-Aldrich, St. Louis, MO, USA) ws dded. Smples were shken sufficiently, mixed well, nd llowed to stnd for 30 min. Smples were centrifuged t x g, nd the superntnt ws discrded. A totl of 1 ml of the buffer + 11 ml protese K (Qigen, Vlenci, CA, USA) were dded nd shken in wter bth for 20 h t 37 C until the leukocyte blocks disppered. An equl volume of blnce phenol (Qigen) ws dded. Smples were inverted gently for 10 min, nd centrifuged t 1,006.2 x g. The superntnt ws pipetted into 5 ml EP tubes. This step ws repeted once. An equl mount of 24:1 chloroform-isomylol (Promeg Corportion, Mdison, WI, USA) ws dded. Smples were shken gently for 10 min, nd centrifuged t 1,006.2 x g. The superntnt ws then pipetted. This step ws repeted once. The superntnt ws pipetted into 2 ml EP tubes. Cold nhydrous ethnol ws dded (Beijing Chemicl Regent Co., Ltd., Beijing, Chin). Smples were centrifuged t 10,500 x g for 10 min. The superntnt ws discrded. A totl of 200 ml of 70% ethnol ws dded. Smples were wshed twice. Smples were then inverted slowly for 1 min, nd centrifuged t 10,500 x g for 10 min. The superntnt ws discrded. Smples were ir dried t room temperture. A totl of 100 ml of TE ws dded to dissolve the DNA. The OD vlue (Thermo Fisher Scientific, Wlthm, MA, USA) ws mesured. Smples were plced t -20 C. Rel-time PCR genotyping. The TqMn genotyping technique ws used for the detection of TERT rs nd CLPTM1L rs polymorphisms. The PCR TqMn probe nd primers were designed nd synthesized by ABI PE Applied Biosystems (Foster City, CA, USA). TqMn Mster mix ws from ABI PE Applied Biosystems. PCR rection system: 2.50 µl of 2x TqMn Mster mix, 0.25 µl of 20x primer nd probe mixture, 1.25 µl of H 2 O, nd 1.00 µl of DNA, for totl of 5.00 µl. PCR mplifiction conditions: PCR rections nd fluorescence signl reding were performed on n ABI 7500 fluorescent quntittion PCR mplifier (ABI PE Applied Biosystems). The mplifiction conditions were s

3 1590 Tble I. Bsic informtion on the cse group nd control group. Chrcteristics Cse group (%) Control group (%) P-vlue Mles Averge ge 56.36± ± Smokers 130 (60.7) 82 (34.1) Non-smokers 84 (39.3) 134 (64.4) CRP 161 (75.23) SCCA (mg/l) 56 (26.1) CEA (mg/l) 78 (36.4) TNM stge I+II 90 (42.0) TNM stge III+IV 124 (58.0) No lymphtic metstsis 182 (85.0) Lymphtic metstsis 32 (15.0) No. of tumors =1 105 (49.0) 2 99 (51.0) Two-sided test; the differences were considered sttisticlly significnt when P<0.05. CRP, C-rective protein; SCCA, squmous cell crcinom ntigen; CEA, crcinoembryonic ntigen; TNM, tumor-node-metstsis. follows: pre-denturtion for 10 min t 95 C; denturtion for 30 sec t 92 C, nneling nd extension for 1 min t 60 C, for 47 cycles in totl. SDS softwre version 4.0 (ABI PE Applied Biosystems) ws used for genotype nlysis. The genotypes of smples were judged by detecting FAM nd VIC fluorescence intensity mrked by different lleles of the sme gene. Sttisticl nlysis. SPSS 19.0 softwre (SPSS, Inc., Chicgo, IL, USA) ws used for dt nlysis. A two-sided test ws conducted to detect the differences in distribution of demogrphic chrcteristics, relevnt risk fctors, nd SNP genotype between the cse group nd control group. P<0.05 ws considered sttisticlly significnt. The logistic regression model ws used to compute the odds rtio (OR) of vrious fctors nd their 95% confidence intervl (95% CI), nd nlyze the reltionship between genetic polymorphisms nd the risk of developing lung cncer. Results Generl conditions of reserch subjects. The bsic conditions of the cse group nd control group re shown in Tble I. A totl of 214 mle lung cncer ptients nd 216 helthy mles were included s reserch subjects. The ges of the cse group nd control group rnged from 30 to 86 yers. The verge ge of the cse group ws 56.36±10.43 yers, nd the verge ge of the control group ws 57.27±12.32 yers. There were no significnt differences in ge between the two groups (P=0.513). Bsed on sttisticl nlysis, there were no significnt differences in distribution of ptients with or without history of smoking between the cse group nd control group (P=0.256). The distribution of relevnt clinicl indexes of the lung cncer ptients [crcinoembryonic ntigen, tumor-nodemetstsis (TNM) stging, lymphtic metstsis, nd number of tumors] is shown in Tble I. Figure 1. Detection of the genotype of the TERT rs locus. The red points represent CC homozygous individuls. The blue points represent TT homozygous individuls. The green points represent CT heterozygous individuls. TERT, telomerse reverse trnscriptse. Distribution of TERT nd CLPTMlL polymorphism genotypes nd the reltionship between the distribution nd risk of developing lung cncer in mles. The genotypes of the TERT rs nd CLPTM1L rs loci re shown in Fig. 1. The verticl coordintes represent the C lleles, nd the horizontl coordintes represent the T lleles.

4 XIAO nd HE: GENETIC POLYMORPHISMS IN THE TERT-CLPTM1L REGION AND LUNG CANCER SUSCEPTIBILITY 1591 Tble II. Reltionship between the genetic polymorphism of TERT nd CLPM1L nd lung cncer susceptibility in mles. Genotype Cse group Control group P-vlue OR (95% CI) TERT rs CC CT ( ) TT ( ) CT+TT ( ) T llele ( ) CLPTM1L rs CC CT ( ) TT ( ) CT+TT ( ) T llele ( ) The OR vlue ws subjected to ge correction. The differences were considered sttisticlly significnt t P<0.05. TERT, telomerse reverse trnscriptse; CLPTM1L, cleft lip nd plte trnsmembrne protein 1; OR, odds rtio. Tble III. Reltionship between the joint ction of the genetic polymorphism of TERT nd CLPTM1L nd lung cncer susceptibility in mles. TERT rs CLPTM1L rs Cse group Control group P-vlue OR (95% CI) CC CC 23 6 CC CT+TT ( ) CT+TT CC ( ) CT+TT CT+TT < ( ) The OR vlue ws subjected to ge correction. The differences were considered sttisticlly significnt t P<0.05. TERT, telomerse reverse trnscriptse; CLPTM1L, cleft lip nd plte trnsmembrne protein 1; OR, odds rtio. Reltionship between the genetic polymorphisms of TERT nd CLPTM1L nd lung cncer susceptibility in mles. The genotype frequencies of the two genetic loci, TERT rs nd CLPTM1L rs401681, in both the cse group nd control group complied with Hrdy-Weinberg equilibrium. The polymorphisms of the two genetic loci nd the distribution of the lleles in both groups re shown in Tble II. The results showed tht the risk of developing lung cncer in the popultion with the TERT rs locus crrying the T llele ws times the risk of developing lung cncer in the popultion crrying the C llele (OR=1.614, 95% CI= ) following djustment of the ge fctor. Furthermore, the risk of developing lung cncer in the popultion crrying the TT mutnt gene nd the CT genotype incresed significntly compred with tht in the popultion crrying the CC wild genotype. The differences were sttisticlly significnt (OR=1.815, 95% CI= ); (OR=2.417, 95% CI= ). In ddition, bsed on comprison between the combintion of two mutnt genotypes (CT+TT) nd the wild homozygous genotype (CC), the mutnt genotype incresed the risk of developing lung cncer. The differences were sttisticlly significnt (OR=1.955, 95% CI= ). The risk of developing lung cncer in the popultion crrying the T llele t the CLPTM1L rs locus ws times the risk of developing lung cncer in the popultion crrying the C llele (OR=1.343, 95% CI= ). Bsed on comprison between the combintion of two mutnt genotypes (CT+TT) nd the wild homozygous (CC) genotype, the mutnt genotype incresed the risk of developing lung cncer. The differences were sttisticlly significnt (OR=1.744, 95% CI= ). Next, the genetic polymorphisms of the TERT rs nd CLPTM1L rs loci were combined to nlyze the joint ction of the two genes. The results of nlysis re shown in Tble III. The risk of developing lung cncer in individuls with mutnt genotypes of the TERT rs nd CLPTM1L rs loci incresed significntly (OR=4.457, 95% CI= ). The differences were sttisticlly significnt. The results in Tble IV show tht individuls crrying the mutnt genotypes (CT+TT), CC of TERT rs , nd mutnt genotype (CT+TT) of CLPTMlL rs in the smoking popultion hd significntly higher risk of developing lung cncer compred with those crrying the wild homozygous genotype (CC) in the non-smoking popultion (OR=2.348, 95% CI= ; OR=2.785, 95% CI= ). The differences were sttisticlly significnt.

5 1592 Tble IV. Reltionship between the joint ction of genetic polymorphism of TERT nd CLPTM1L nd smoking, nd lung cncer susceptibility in mles. Smokers Genotype Cse group Control group P-vlue OR (95% CI) TERT rs CC CT+TT ( ) + CC ( ) + CT+TT ( ) CLPTM1L rs CC CT+TT ( ) + CC ( ) + CT+TT ( ) The OR vlue ws subjected to ge correction. The differences were considered sttisticlly significnt t P<0.05. TERT, telomerse reverse trnscriptse; CLPTM1L, cleft lip nd plte trnsmembrne protein 1; OR, odds rtio. Tble V. Anlysis of the correltion between the genetic polymorphism of the TERT rs locus nd the progression of course of disese of the mle lung cncer ptients. Indexes of progression of course of disese Genotype I+II III+IV P-vlue OR (95% CI) CC CT ( ) TT ( ) CT+TT ( ) Lymphtic metstsis (-) Lymphtic metstsis (+) CC CT ( ) TT ( ) CT+TT ( ) One tumor More thn two tumors CC CT ( ) TT ( ) CT+TT ( ) The OR vlue ws subjected to ge correction. The differences were considered sttisticlly significnt t P<0.05. TERT, telomerse reverse trnscriptse; OR, odds rtio. Anlysis of the correltion between the genetic polymorphism of TERT nd CLPTM1L nd progression of lung cncer. The results in Tbles V nd VI show tht in lung cncer ptients, crrying the mutnt genotype (CT+TT) t the TERT rs locus is ssocited with the number of tumors (OR=0.553, 95% CI= ). The differences were sttisticlly significnt. The indexes relted to progression of other lung cncers (TNM stging nd lymphtic metstsis) were not correlted with the genetic polymorphism. Discussion The incidence of lung cncer is multi-fctor nd multi-stge process cused by genetic nd environmentl fctors (1). In recent yers, numerous studies hve focused on the

6 XIAO nd HE: GENETIC POLYMORPHISMS IN THE TERT-CLPTM1L REGION AND LUNG CANCER SUSCEPTIBILITY 1593 Tble VI. Anlysis of the correltion between the genetic polymorphism of the CLPTM1L rs locus nd the progression of the course of disese of mle lung cncer ptients. Indexes of progression of course of disese Genotype I+II III+IV P-vlue OR (95% CI) CC CT ( ) TT ( ) CT+TT ( ) Lymphtic metstsis ( ) Lymphtic metstsis (+) CC CT ( ) TT ( ) CT+TT ( ) One tumor More thn two tumors CC CT ( ) TT ( ) CT+TT ( ) The OR vlue ws subjected to ge correction. The differences were considered sttisticlly significnt t P<0.05. CLPTM1L, cleft lip nd plte trnsmembrne protein 1; OR, odds rtio. reltionship between relevnt genetic polymorphisms nd lung cncer susceptibility. Studying mles from Jinzhou city s reserch subjects, we investigted the reltionship between the risk of developing lung cncer nd polymorphisms of TERT nd CLPTM1L s well s exposure to risk fctors. Both SNPs t the TERT rs locus nd CLPTM1L rs locus cn increse the risk of developing lung cncer. The interctions between the two fctors nd genetic nd environmentl fctors significntly increse the risk of developing lung cncer. TERT is the ctlytic subunit of telomerse, nd is locted on chromosome 5p It spns 35 kb, nd comprises 16 exons nd 15 introns. It is rte-limiting fctor for synthesizing the telomerse holoenzyme. The rs locus is locted on the second exon of the gene. The moleculr weight of the TERT protein is pproximtely 127 kd, nd is primrily distributed in the nucleus. Muttion of its non-ctive structurl domin, DAT, influences the binding between TERT nd telomere DNA, thus ffecting the ctivity of telomerse in extending telomeres. Moreover, it hs higher tumor specificity (19). Our results showed tht there were significnt differences in genotype frequencies between the cse group nd control group. The risk of developing lung cncer in the popultion crrying the T llele is incresed significntly compred with the popultion crrying the C llele. The risk of developing lung cncer in the popultion crrying the mutnt genotype nd the CT genotype is incresed significntly compred with the popultion crrying the CC wild genotype. The differences were sttisticlly significnt. These results indicte tht genetic polymorphism of the TERT rs locus my be n independent risk fctor for the incidence of lung cncer in mles. CLPTM1L is locted on the chromosome 5p15.33 region, nd encodes for trnsmembrne protein. It cn induce cell poptosis in cispltin-resistnt cell lines. It is expressed in multiple norml nd mlignnt tissues such s the skin, lung, ovry, cervix, nd thymus (20,21). Currently, CLPTM1L is confirmed to be overexpressed nd resistnt to cispltin in humn ovrin tumor cell lines. Its overexpression in pulmonry tumor cells cn protect ginst poptosis induced by genotoxic stress (22-24), indicting tht it hs nti-poptotic function. However, the functions of CLPTM1L, nd its role in tumorigenesis remin uncler. We studied the reltionship between the genetic polymorphism of the CLPTM1L rs locus nd lung cncer in mles. The risk of developing lung cncer in the popultion crrying the T llele is incresed significntly compred with those crrying the C llele. Bsed on comprison between the combintion of the two mutnt genotypes (CT+TT) nd the wild homozygous genotype (CC), the mutnt genotype increses the risk of developing lung cncer. There is no reserch on the reltionship between the genetic polymorphism nd lung cncer, wheres gret del on lung cncer, but there re differences mong the results. This study hd limittions. The smple-size ws reltively smll. The nlysis only involved SNPs of two genes in the chromosome 5p15.33 region. Future studies require n expnded popultion rnge nd incresed smple-size. Furthermore, the nlysis should involve multiple genetic loci. The reltionship between genetic polymorphisms of the

7 1594 rs nd rs loci nd the progression of the disese requires further vlidtion in future studies. In conclusion, there is correltion between genetic polymorphisms of TERT nd CLPTM1L nd lung cncer in mles. The TERT rs nd CLPTMlL rs401681t lleles increse the risk of developing lung cncer in mles. They ply role in understnding the pthogenesis of lung cncer nd screening for the high-risk popultion. Acknowledgements The present study ws funded by Jinzhou Medicl University specil fund XZJJ References 1. Yin J, Li Y, Yin M, Sun J, Liu L, Qin Q, Li X, Long L, Nie S nd Wei S: TERT-CLPTM1L polymorphism rs contributes to cncers risk: evidence from met-nlysis bsed on 29 publictions. PLoS One 7: e50650, Mocellin S, Verdi D, Pooley KA, Lndi MT, Egn KM, Bird DM, Prescott J, De Vivo I nd Nitti D: Telomerse reverse trnscriptse locus polymorphisms nd cncer risk: field synopsis nd met-nlysis. J Ntl Cncer Inst 104: , Chen XF, Ci S, Chen QG, Ni ZH, Tng JH, Xu DW nd Wng XB: Multiple vrints of TERT nd CLPTM1L constitute risk fctors for lung denocrcinom. Genet Mol Res 11: , Jing M, Wu H nd Qin C: Genetic vrint rs t 5p15.33 modifies susceptibility to lung cncer but not esophgel squmous cell crcinom. PLoS One 8: e84277, Yng IA, Hollowy JW nd Fong KM: Genetic susceptibility to lung cncer nd co-morbidities. J Thorc Dis 5 (Suppl 5): , Zhong R, Liu L, Zou L, Zhu Y, Chen W, Zhu B, Shen N, Rui R, Long L, Ke J, et l: Genetic vritions in TERT-CLPTM1L locus re ssocited with risk of lung cncer in Chinese popultion. Mol Crcinog 52 (Suppl 1): E118-E126, Li C, Yin Z, Wu W, Li X, Ren Y nd Zhou B: Genetic vritions in TERT-CLPTM1L genes nd risk of lung cncer in Chinese women nonsmokers. PLoS One 8: e64988, Ln Q, Cwthon R, Go Y, Hu W, Hosgood HD III, Brone-Adesi F, Ji BT, Bssig B, Chow WH, Shu X, et l: Longer telomere length in peripherl white blood cells is ssocited with risk of lung cncer nd the rs (CLPTM1L-TERT) polymorphism in prospective cohort study mong women in Chin. PLoS One 8: e59230, Myneni AA, Chng SC, Niu R, Liu L, Ochs-Blcom HM, Li Y, Zhng C, Zho B, Shi J, Hn X, et l: Genetic polymorphisms of TERT nd CLPTM1L nd risk of lung cncer - cse-control study in Chinese popultion. Lung Cncer 80: , Zho Z, Li C, Yng L, Zhng X, Zho X, Song X, Li X, Wng J, Qin J, Yng Y, et l: Significnt ssocition of 5p15.33 (TERT CLPTM1L genes) with lung cncer in Chinese Hn popultion. Exp Lung Res 39: 91-98, Wng H, Zho Y, M J, Zhng G, Mu Y, Qi G, Fng Z, Wng L, Fn Q nd M Z: The genetic vrint rs401681c/t is ssocited with the risk of non-smll cell lung cncer in Chinese minlnd popultion. Genet Mol Res 12: 67-73, Tseng TS, Prk JY, Zblet J, Moody-Thoms S, Sothern MS, Chen T, Evns DE nd Lin HY: Role of nicotine dependence on the reltionship between vrints in the nicotinic receptor genes nd risk of lung denocrcinom. PLoS One 9: e107268, Yin Z, Cui Z, Ren Y, Zhng H, Yn Y, Zho Y, M R, Wng Q, He Q nd Zhou B: Genetic polymorphisms of TERT nd CLPTM1L, cooking oil fume exposure, nd risk of lung cncer: cse-control study in Chinese non-smoking femle popultion. Med Oncol 31: 114, Wng Z, Zhu B, Zhng M, Prikh H, Ji J, Chung CC, Smpson JN, Hoskins JW, Hutchinson A, Burdette L, et l: Imputtion nd subset-bsed ssocition nlysis cross different cncer types identifies multiple independent risk loci in the TERT-CLPTM1L region on chromosome 5p Hum Mol Genet 23: , Zhng Y, Zho M, Shen L, Ren Y, Su L, Li X, Yin Z nd Zhou B: Genetic polymorphisms of TERT nd CLPTM1L nd risk of lung cncer: cse-control study in northest Chinese mle popultion. 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