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Mtdna Evidence: Genetic Background Associated with Related Populations at High Risk for Esophageal Cancer Between Chaoshan and T View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Genomics 90 (2007) 474–481 www.elsevier.com/locate/ygeno mtDNA evidence: Genetic background associated with related populations at high risk for esophageal cancer between Chaoshan and Taihang Mountain areas in China ⁎ Xiao-Yun Li a,1, Min Su a, ,1, Hai-Hua Huang a, Hui Li b, Dong-Ping Tian a, Yu-Xia Gao a a Department of Pathology, Key Immunopathology Laboratory of Guangdong Province, Shantou University Medical College, Shantou, Guangdong 515031, China b State Key Laboratory of Genetic Engineering and Center for Anthropological Studies, School of Life Sciences, Fudan University, Shanghai, Jiangsu 200433, China Received 4 April 2007; accepted 20 June 2007 Available online 9 August 2007 Abstract There are three major geographic regions in China known for their high incidences of esophageal cancer (EC): the Taihang Mountain range of north-central China, the Minnan area of Fujian province, and the Chaoshan plain of Guangdong province. Historically, waves of great population migrations from north-central China through coastal Fujian to the Chaoshan plain were recorded. To study the genetic relationship among the related EC high-risk populations, we analyzed mitochondrial DNA (mtDNA) haplogroups based on 30 EC patients from Chaoshan and used control samples from the high-risk populations, including 48, 73, and 89 subjects from the Taihang, Fujian, and Chaoshan areas, respectively. The principal component of all haplogroups, correlation analysis of haplogroup frequency distributions between populations, and haplogroup D network analysis showed that compared with other Chinese populations, populations in the three studied areas are genetically related. The highest haplogroup frequency shared by all studied populations was haplogroup D, with much higher frequency in the Chaoshan area EC patients. The majority of haplogroup D individuals among the Chaoshan area EC patients belonged to subhaplogroups D4a and D5a, with the total frequency of these two haplogroups significantly higher than that in the high-risk population in the same area (χ2 =9.017, pb0.01). In conclusion, EC high-risk populations in these three areas share a similar matrilineal genetic background, and D4a and D5a might be candidate genetic markers for screening populations susceptible to EC in the Chaoshan area. Ours is the first report to show the association between mtDNA haplogroups (D4a and D5a) and esophageal cancer. © 2007 Elsevier Inc. All rights reserved. Keywords: mtDNA haplogroup; Esophageal cancer high-risk population; Genetic background; Candidate genetic markers Esophageal cancer (EC) is one of the most common fatal eastern littoral of China, including the Chaoshan plain in cancers worldwide. There are particular geographical hot spots Guangdong province and the southern part of Fujian province with high EC incidences. Most EC patients live in the so-called (Minnan area), are less known to the world. The Chaoshan area, “esophageal cancer belt,” which stretches from central China next to the Minnan area, is surrounded by the Lianhua westward through Central Asia to northern Iran [1,2]. In north- Mountains and South China Sea and is thus relatively geo- central China, the Taihang Mountain area between Henan, graphically isolated from the inner part of China. Our previous Hebei, and Shanxi provinces is a well-known high-risk region study [3] reported an annual average crude incidence rate for EC for EC. In contrast, EC high-risk areas located in the south- to be 71.07/100,000 from 1995 to 2003 on Nanao Island, which represents a relatively isolated district within the Chaoshan area. We and others have reported familial aggregation of EC Abbreviations: EC, esophageal cancer; mtDNA, mitochondrial DNA; patients and increased EC risk in family members in north- HVS-I, hypervariable segment I; PC, principal component. – ⁎ Corresponding author. Fax: +86 754 8900429. central China and the Chaoshan area [4 7]. These findings E-mail address: [email protected] (M. Su). support the potentially important role of genetic susceptibility 1 These authors are co-first authors of this article. in EC etiology in high-risk populations. Ascertaining genetic 0888-7543/$ - see front matter © 2007 Elsevier Inc. All rights reserved. doi:10.1016/j.ygeno.2007.06.006 X.-Y. Li et al. / Genomics 90 (2007) 474–481 475 background of EC patients will facilitate the clarification of Table 1 molecular genetic mechanisms in esophageal carcinogenesis, mtDNA haplogroup distribution among all populations in three studied areas the risk evaluation of individuals from high-risk populations, Haplogroup Taihang Fujian EC Chaoshan EC Chaoshan and the establishment of effective screening to identify EC- Mountain EC high-risk high-risk area EC susceptible individuals and preventive measures. high-risk population (%) population (%) patients (%) population (%) (n=73) (n=89) (n=30) According to historical records [8], Han inhabitants of north- (n=48) central China (Henan and Shanxi Hans) continuously migrated A 6.25 8.22 7.87 0.00 into the Chaoshan area via Fujian due to warfare and famines B4 0.00 2.74 0.00 0.00 and gradually became the predominant inhabitants of the B4a 4.17 5.48 3.37 0.00 Chaoshan area. Although the Taihang Mountain, Fujian, and B4b1 2.08 2.74 3.37 0.00 B4c1 0.00 1.37 5.62 6.67 Chaoshan EC high-risk areas are geographically distant, we a hypothesize that these EC high-risk populations could share B5 0.00 0.00 2.25 0.00 B5a 2.08 0.00 2.25 0.00 common genetic traits. mtDNA is characterized by a strictly B5b 10.42 1.37 1.12 6.67 maternal mode of inheritance, absence of recombination, rapid C 6.25 5.48 3.37 3.33 rate of mutation, and high level of population-specific poly- D a 16.67 10.96 5.62 3.33 morphisms. These make mtDNA widely applicable for studying D4a 0.00 4.11 6.74 20.00 evolutionary relationships among human ethnic groups [9–11]. D4b 0.00 1.37 1.12 0.00 D5 2.08 2.74 2.25 0.00 Because mtDNA is strictly maternally inherited, the mtDNA D5a 6.25 4.11 3.37 13.33 sequence has evolved by the sequential accumulation of base F a 2.08 0.00 3.37 0.00 substitutions along radiating maternal lineages [12]. Therefore, F1a 6.25 10.96 3.37 3.33 the characteristics of mtDNA enable researchers to trace related F1b 2.08 1.37 2.25 0.00 lineages back through time, highlighting the maternal ancestry F1 0.00 1.37 0.00 0.00 F1c 2.08 0.00 0.00 0.00 of a population, without the confounding effects of biparental F2a 0.00 1.37 1.12 0.00 inheritance and recombination inherent in nuclear DNA [13]. F2 a 0.00 0.00 0.00 0.00 The common methods used in these studies are restriction G a 10.42 1.37 5.62 6.67 M a 0.00 1.37 0.00 0.00 enzyme analysis of mtDNA coding regions in conjunction with a sequence analysis of the mtDNA D-loop region, which has M7 0.00 0.00 1.12 0.00 M7b 0.00 4.11 5.62 6.67 apparently evolved several times faster than other regions M7b1 0.00 6.85 2.25 0.00 [9–11,14–16]. The combined information from coding region M7b2 2.08 0.00 1.12 3.33 and D-loop region contributes to the phylogenetic analysis of M7c 0.00 1.37 0.00 6.67 mtDNA. M8a 6.25 4.11 4.49 10.00 In this study, we investigated the mtDNA polymorphism M9a 2.08 2.74 3.37 0.00 N a 0.00 1.37 1.12 0.00 distribution among populations from the Taihang Mountain, N9a 4.17 4.11 3.37 0.00 Fujian, and Chaoshan EC high-risk areas. Our data suggested a M10 2.08 0.00 0.00 0.00 close genetic relationship between the Chaoshan and the R9a 0.00 2.74 4.49 0.00 Taihang Mountain EC high-risk populations. Compared with R9b 0.00 1.37 1.12 0.00 the other mtDNA haplogroups, the D4a and D5a haplogroups R11 2.08 1.37 1.12 0.00 Y 2.08 0.00 3.37 0.00 were found to be closely associated with EC in the Chaoshan Z 0.00 1.37 3.37 10.00 area. a Haplogroup status cannot be further specified into subhaplogroups. Results mtDNA haplogroup frequencies frequencies in northern Hans than in their southern counterparts and thus were northern Han dominant haplogroups, whereas Our primary goal was to investigate the genetic affinity B, F, R9a, R9b, N9a, M7b, and M7b1 constituted the southern between the EC high-risk populations and the potential asso- native dominant haplogroups and showed much higher overall ciation between mtDNA haplogroup variations and EC frequencies in southern Hans than in northern Hans. Thus, we occurrence. mtDNA haplogroups identified in 30 unrelated EC further summarized the haplogroup distribution in the Chaoshan patients from the Chaoshan area and 210 unrelated EC high-risk area EC patients and EC high-risk populations from the Taihang individuals from the Taihang Mountain, Fujian, and Chaoshan Mountain, Fujian, and Chaoshan areas according to southern areas are presented in Table 1. A total of 38 haplogroups were and northern haplogroup distributions among the general studied. We estimated haplogroup diversity of each population Chinese population (Table 3). (Table 2). Compared with the EC high-risk populations from the Table 3 shows, in the Taihang Mountain area EC high-risk Taihang Mountain, Fujian, and Chaoshan areas, the mtDNA populations, that the overall frequency of the northern Han haplogroups in EC patients from the Chaoshan area was the least dominant haplogroups (A, C, D, G, M8a, Y, and Z) was 56.25%.
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