Journal of Life Sciences Volume 5 Number (3)
J LS
Journal of Life Sciences
Volume 5, Number 9, September 2011 (Serial Number 41)
Contents
Research Papers
Statistical Analysis of Genetic Diversity in 15 STR Loci from Han, Miao and Yao Tribes in South China
Kuanheng Wu, Miao He, Yijing Wang, Jian Song, Liping Ling and Daniel Wai Tin Chan 682
CCR5-CCR2 Gene Polymorphisms in Ethiopian Jews: Population Divergence and Its Relevance to HIV-1 Infection Resistance
Michael Korostishevsky, Batsheva Bonne-Tamir, Zvi Bentwich, Alexander Kalinkovich and Alexander Tsimanis
690 First Record of Frankliniella Occidentalis and Impatiens Necrotic Spot Virus in Egypt
Abeer Salah El-Deen Abd El-Wahab, Mohamed Abdel-Kader El-Sheikh and Salah Elnagar
697 Investigation of the Optimum Condition and Antimicrobial Activities of Pigments from Four
Potent Pigment-Producing Fungal Species
Neveen S. Geweely
712 Effect of Ginger Powder (Zingiber Officinale) on Plasma Lipid Profile and Liver Enzyme Activities of Hypercholesterolemic Rats
Ajayi Olubunmi Bolanle 717
Parasitic Plants as a New Target Plant for Screening Rice Allelopathic Potential
Yiqing Guo, Kil-Ung Kim, John I. Yoder and Donghyun Shin 725
Effect of Graded Levels of Nitrogen on Growth and Yield of Eggplant (Solanum Melongena) in Kabba, Southern Guinea Savanna Ecological Zone of Nigeria
John Akintola Oloniruha
728 Alternative Technologies Used in Laying Hens Husbandry
Marius Giorgi Usturoi, Paul Corneliu Boi şteanu, Răzvan Mihail Radu-Rusu, Ioan Mircea Pop, Marius Gheorghe Doli ş and Alexandru Usturoi
733
Phylogenetic Study of Freshwater Bivalve Parreysia Corrugata from Maharashtra State, India by 18S rRNA Sequences
Madhav V. Upadhye, Rajesh C. Patil, Sonal M. Manohar and Ujwala Jadhav 739
Effect of Thermal Stress, Cistern Size and Milking Frequency on Plasma Mineral Concentrations in Holstein Dairy Cows
Rim Ben Younes, Moez Ayadi, Taha Najar, Margherita Caccamo, Iris Schadt and Moncef Ben M’Rad 747
Effect of Ageing Time on Meat Characteristics of Castrated and Uncastrated Brahman Cattle
José A. Miguel, Jesús Ciria, Begoña Asenjo, David Colmenarez and Hector Pargas 754
Effect of Climate Change on Phenology of Forage Grass Species
Żurek Grzegorz
759 Developing Adaptation Strategies Due to Climate Change: With Special Reference to the Vulnerable Java Fisheries, Indonesia
Indah Susilowati and Agus Hartoko 768
Fast Determination of Cd, Pb, and Cu in Grape Must and Wine
Jarmila Lastincova, Ernest Beinrohr and Lubica Pospísilova 772
Effect of the Chromatic Assimilation (Bezold Effect) in the Vision of the Content on a Dinner Plate
Ignacio Tortajada, Jorge Montalvá and Mariano Aguilar
Journal of Life Sciences 5 (2011) 677-681
Statistical Analysis of Genetic Diversity in 15 STR Loci from Han, Miao and Yao Tribes in South China
1 1 1 1 2 Kuanheng Wu 3 , Miao He , Yijing Wang , Jian Song , Liping Ling and Daniel Wai Tin Chan 1. Life Sciences School, Sun Yat-sen University, Guangzhou, Guangdong 510275, China
2. Education School, Sun Yat-sen University, Guangzhou, Guangdong 510275, China 3. Department of Building Services Engineering, The Hong Kong Polytechnic University, Hunghom, Hong Kong, China
Received: August 18, 2010 / Accepted: November 03, 2010 / Published: September 30, 2011.
Abstract: It is interesting to find the possible statistical characters of 15 STRs in Han, Miao and Yao, the three main tribal populations in South China, and the significant differences of allele frequencies by comparing STR loci in each cluster for applications of forensic science. Genetic diversity in 15 STR loci [D8S1179, D21S11, D7S820, CSF1PO, D3S1358, TH01, D13S317, D16S539, D2S1338, D19S433, vWA, TPOX, D18S51, D5S818, and FGA] from Han, Miao and Yao tribes in South China had been analyzed. The allele frequencies of 15 tetrameric STR loci were obtained from 1,530 unrelated individuals of three main tribal populations [Han, Yao and Miao] inhibiting in South China. Cluster analysis and LSD test had been used for data analysis. The high degree statistical differentia of genetic polymorphism has been found among three tribal populations.
Key words: STR, genetic diversity, statistics, Han, Miao, Yao.
Abbreviations: STR: short tandem repeats; The traditional STR loci applied in forensic science includes 15 STR loci [D8S1179, D21S11, D7S820, CSF1PO, D3S1358, TH01, D13S317, D16S539, D2S1338, D19S433, vWA, TPOX, D18S51, D5S818, and FGA]; LSD: a least significant difference test of one-way analysis of variance.
1. Introduction differences founded at specific STR loci among Chinese populations in different locations. For
15 STR loci from three tribal populations Han, example, the significant differences were found at Miao and Yao in South China were obtained in present three STR loci [D3S1358, D21S11, D8S1179] study. Whole DNA extracted from venous blood was between Sichuan and Beijing populations, [D3S1358, obtained from randomly unrelated 1,000 Han, 248 D21S11, TPOX] between Sichuan and East China Yao and 282 Miao individuals, Guangdong Province. populations, [D5S818, D13S317, CSF1PO] between Tribe Miao and Yao have over nine million people Sichuan and Hong Kong populations according to the inhabiting mainly in mountainous areas of Guizhou, study of Zhang et al. [1]. It is interesting to find the Guangxi and Hainan Province. possible statistical characters of 15 STRs in Han, Miao The traditional methods of Hardy-Weinberg and Yao, the three main tribal populations in South equilibrium, the power of discrimination, the China, and the significant differences of allele probability of paternity exclusion, and the frequencies by comparing STR loci in each cluster for polymorphic information content have already applications of forensic science. Statistical methods presented profound conclusions about the significant based on cluster analysis, as well as LSD test show the
significant differentiation among the three tribal Corresponding author: Miao He, Ph.D., associate professor, research fields: bioinformatics, biostatistics. E-mail: populations. The aims of this study are to approach: (1)
lsshem@mail.sysu.edu.cn.
Statistical Analysis of Genetic Diversity in 15 STR Loci from
Han, Miao and Yao Tribes in South China
the genetic polymorphism presented by cluster analysis tribes. Further variance analysis was applied on these especially the genetic diversity between Han and two
STR loci using LSD value, calculated from two sets of other tribes; (2) a region of allele frequencies selected
STR locus allele frequencies array or mean allele by LSD test revealing significant differences among
frequencies array of each allele from several STR loci STR loci in the same cluster could serve as a genetic
in the same cluster, to discriminate the significant marker for individual identification among three tribal
differences of allele frequencies between two STR loci populations; (3) collecting the genetic polymorphic
[12, 13]. To be specific, we calculated LSD (= 0.05) information from the three tribal populations and
value from two arrays {X 1 ,X 2 ,X 3 …} and {Y 1 ,Y 2 , retrospectively interpreting the demographic tribal
Y 3 …} which represented allele frequencies of STR migration and amalgamation in South China.
locus X and Y separately. If |X i -Y i | > LSD, the allele frequencies Y i is significantly different from X i .
2. Materials and Methods
Microsoft Office Excel 2007 and SPSS 15 were used to
2.1 DNA Analyzed
analyze these data.
The allele distributions of 15 STR loci were obtained
3. Result
from 1,530 unrelated individuals [2-6]. Genome DNA Cluster analysis preformed on correlation matrix was extracted from whole blood using Chelex-100 indicated several profound conclusions which were extraction method (Bio-lad Company). Those samples then further studied by using LSD test. The results of
failed in former method using standard phenol
hierarchical cluster analysis revealed highly chloroform methods or DNA IQ commercial kits
TM
(Promega Company) extract DNA again [7]. consistent clusters iv among three tribal populations and clusters [i, ii, iii] shared genetic diversity to
2.2 STR Typing variant extend. LSD test applied on three STR loci
All samples were PCR amplified using [D8S1179, D7S820, D13S317] of Han further AmpFlSTR® Identifiler™ commercial kits (Applied
corroborated the significant diversity of clusters [i, Biosystems Company) [8]. PCR amplifications were
iii] among Han, Miao and Yao.
carried out according to manufacturers (AmpF/STR
3.1 Cluster Analysis
Indetifi-ler PCR amplification kit, AB Applied Biosystems). Amplification products were run in an
The hierarchical cluster analysis based on ABIPRISM 3100 genetic analyzer (ABI Company)
correlation matrix revealed profound genetic diversity using Liz500 as internal standard label. Genescan 3.7
characteristic among three tribes. 15 STR loci from (ABI Company) software was used to collect the data,
each tribe were subdivided into two primary clusters [I, analyze fragment sizes and Genepop v3.4 to calculate
II] and four secondary clusters [i, ii, iii, iv] separately the allele frequencies of each STR locus in 3 tribes [9].
in Fig. 1. The members in each cluster [i, ii, iii, iv] were nearly exactly the same, except three locus
2.3 Statistical Analysis [D8S1179, D7S820, D13S317] drift or switch,
Cluster analysis was applied on 15 STR loci from however the topologic structures differed obviously each tribal population using the correlation matrix
among three tribes especially between clusters iii of Han calculated from 15 sets of STR loci allele frequencies
and Yao, Han and Miao. These dissimilarities found [10, 11]. By comparing each pair of three cluster results,
by cluster analysis were further performed on LSD three STR loci [D8S1179, D7S820, and D13S317]
test in order to systematically analyze the significant probably indicated the genetic diversity among three
differences of allele frequencies [14-17].
Statistical Analysis of Genetic Diversity in 15 STR Loci from
Han, Miao and Yao Tribes in South China
and Yao. A set of symbols “-”, “+--”, “+-”, “+”, “++”, “+++”, “++++” were used to represent the levels of significant difference (< 0], (0, 0.04], (0.04, 0.08], (0.08, 0.12], (0.12, 0.16], (0.16, 0.20], (> 0.20). The “++++” and “+++” symbols focused on allele 13, 16,
17, 18 of STR loci D3S1358 and vWA interpreted a genetic diversity in Han’s D8S1179 and STR loci
(a)
[D3S1358, vWA, D18S51, D19S433] from both Miao and Yao. By comparison, symbols in two columns of
each STR locus indicated the genetic diversity between Miao and Yao. The distinctness located on 5 allele of D19S433 and allele 13 of D3S1358 and vWA.
3.2.2 LSD Analysis between Han’s D7S820 and STR Loci [CSF1PO, D5S818, D16S539, D13S317] from both Miao and Yao
(b)
The levels of significant differences about allelic with Han, focused on allele 8. CSF1PO column contained different symbols in two allelic positions of Miao and Yao probably interpreted STR diversity though not significant. Frequencies analyzed in Table 2 were not as distinct as in Table 1.
Table 1 shows that a slot located on allele 8 and
(c)
several “+” separated in allele 9, 11 and 12 of four STR
Fig. 1 The cluster analysis of Han (a), Miao (b) and Yao (c).
loci represented the genetic diversity in Han’s D7S820 The dissimilarities focused mainly on clusters [i, ii, iii], rather
and four STR loci of Miao and Yao, which had similar than iv were exactly the same among three tribes. The
hierarchy of cluster analysis with Han, focused on topologic structures in cluster iii varied between Han and Miao,
Han and Yao. allele 8. CSF1PO column contained different symbols in two allelic positions of Miao and Yao probably
3.2 Variance Analysis interpreted STR diversity though not significant. LSD values were used to discriminate the significant
3.2.3 LSD Test between Han’s D13S317 and differences of allele frequencies from specific STR loci
[CSF1PO, D5S818, D16S539, D7S820] from both [D8S1179, D7S820, and D13S317] of Han selected by
Miao and Yao
cluster analysis above between each pair of tribes. The LSD test results illustrated in Table 3
3.2.1 LSD Test between Han D8S1179 and STR represented more significant differences compared Loci [D3S1358, vWA, D18S51, D19S433] from both
with Table 2. “++++” symbols mainly located on allele Miao and Yao
8 and 12 of four STR loci consolidated the similar Since Han’s D8S1179 had the similar hierarchy of
results found in Table 2. The deviation information cluster analysis to Miao and Yao’s STR loci [D3S1358,
combining Table 2 and Table 3 suggested the most vWA, D18S51, D19S433], the result in Table 1
distinctive genetic character between Han [D13S317, revealed the significant differences allele frequencies
D7S820] and [CSF1PO, D5S818, D16S539, D7S820] ranging from allele 10 to 18 in four STR loci of Miao
from Miao and Yao, focused on allele [8, 11, 12].
Statistical Analysis of Genetic Diversity in 15 STR Loci from
Han, Miao and Yao Tribes in South China
Table 1 Han’s D8S1179 with Miao and Yao [D3S1358,
4. Discussion
vWA, D18S51, D19S433] LSD test.
D3S1358 vWA D18S51 D19S433 Huge number of STR loci in unrelated three tribal Allele Miao Yao Miao Yao Miao Yao Miao Yao
populations of South China has been typed in order to 10 + + + + + + + +
obtain genetic characteristics of these three tribes. 11 +- +- +- +- +- +- +- +-
12 + + + + +-- +-- +- +- Cluster analysis and LSD test have been applied to
13 +++ ++ +++ ++ +-- +-- + + discover several genetic hypotheses about the tribal
differentiation. The most distinctive feature of present 14 ++ + ++ +- - - - +--
13.2 +--
study is the genetic diversity among three tribes and
15 +-- +- + + +-- - ++ several regions of allelic significant [17-20].
The profound conclusions obtained from present 16 ++++ ++++ +-- + +- +- +-- +-
study include several points below.
The cluster analysis indicates an exactly identical 17 ++++ ++++ ++++ +++ - +- --
16.2 +--
+--
cluster ⅳ of each tribal population in both members 18 +- +- +++ +++ +-- +--
and topological structure. Four STR loci [D2S1138, 19 - - - +- +-- -
FGA, D21S11, TH01] included in cluster ⅳ indicate 20 - - - - +-- -
“-”, “+--”, “+-”, “+”, “++”, “+++”, “++++” represent the levels high consistent genetic characters.
of significant difference (- ∞, 0], (0, 0.04], (0.04, 0.08], (0.08, Members in clusters [iii, i] vary in three tribal 0.12], (0.12, 0.16], (0.16, 0.20], (0.20, ∞+), LSD (Han and
populations, also have the same of topological structure. Miao) = 0.032820, LSD (Han and Yao) = 0.032858.
The hierarchical positions of the three STR loci
Table 2 Han’s D7S820 with Miao and Yao [CSF1PO,
[D8S1179, D7S820, and D13S317] vary among three
D5S818, D16S539 and D7S820].
tribes according to cluster analysis. CSF1PO D5S818 D16S539 D13S317 Allele
The statistical analysis reveals the variance between Miao Yao Miao Yao Miao Yao Miao Yao
Han’s D8S1179 and clusters ⅲ [D3S1358, vWA, 7 --------
D18S51, D19S433] in Miao and Yao focuses on allele 8 +- +- +- +- +- +- +- +- [13, 16, 17, 18] of D3S1358 and vWA. 9 - - - - +- +- --
10 - - - - - - - - The variance between Han’s [D13S317, D7S820]
11 +- - - - - - - +-- and cluster i [CSF1PO, D5S818, D16S539, D7S820] in 12 ++ +- - - - - +-- +--
Miao and Yao focuses on allele [8, 11, 12]. 13 - - - - - - - -
The weightiness of STR loci in cluster ⅳ could be LSD (Han and Miao) = 0.0882, LSD (Han and Yao) = 0.0969.
omitted or reduced since the indistinguishable genetic diversity was in paternity testing or personal identify
Table 3 Han D13S317 with Miao and Yao [CSF1PO, D5S818, D16S539 and D7S820].
among these three tribes.
CSF1PO D5S818 D16S539 D7S820 The weightiness of cluster [iii, i] supposes to be Allele
Miao Yao Miao Yao Miao Yao Miao Yao aggravated because of the high degree of genetic 7--------
Acknowledgment
10 -------- 11 - - - +-- --+-
The authors appreciate all blood donors in this study. 12 ++++ ++ +- +-- +- - - +--
Without their cooperation, the study could not be 13 - - +-- -----
accomplished. This work was supported by National LSD (Han and Miao) = 0.0908, LSD (Han and Yao) = 0.0937.
Natural Science Foundation of China (No. 60736028)
Statistical Analysis of Genetic Diversity in 15 STR Loci from
Han, Miao and Yao Tribes in South China
and Science and Technology Planning Project of of debris from fingemails, Int. J. Legal. Med. 106 (1993) 81-84.
Guangdong Province of China (No. 2003A3080503). [10] M. Raymond, F. Rousset, GENEPOP: Populations
References genetics software for exact tests and ecumenicism,
Journal of Heredity 86 (1995) 248-249. [1] H.J. Zhuang, Y.B. Li, J.P. Jiang, J. Zhang, J. Wu, H. Du,
C.C. Cockerham, Analyses of gene frequencies, Genetics et al., Analysis of 15 STR loci in Chinese population
74 (1973) 679-700.
from Sichuan in West China, Forensic Science [12] D.J. Balding, R.A. Nichols, DNA profile match International 171 (2007) 222-225.
probability calculation: How to allow for population [2]
C. Liu, C.H. Liu, H.J. Wang, Genetic diversity at 15 STR stratification relatedness, database selection and single loci in two tribal populations in Southern China, Forensic
bands, Forensic Sci. International 64 (1994) 125-140. Science international 162 (2006) 28-32.
[13] S. Schneider, J.M. Kueffer, D. Roessli, L. Excoffier, A [3] J.G. Hirschfeld, M.J. Farfan, V. Prieto, M.L. Soto, Y.
Softerware for Population Genetic Data Analysis, Torres, P. Sanz, Allele distribution of 15 STRs in a
Genetics and Biometry Laboratory, University of Geneva, population from Extremadura (Central-Western Spain),
Switzerland, 1997.
International Congress Series 1239 (2003) 165-169. [14] J. Goudet, M. Raymond, T.D. Meeus, F. Rousset, Test [4] L.A. Zhivotovsky, S. Ahmed, W. Wang, A.H. Bittles,
differentiation in diploid populations, Genetics 144 (1996) The forensic DNA implications of genetic differentiation
1993-1940.
between endogamous communities, Forensic Science [15] S.W. Guo, E.A. Thompson, Performing the exact test of International 119 (2001) 269-272.
Hardy-Weinberg proportions for multiple alleles, [5] M.S. Shi, J.P. Tang, R.F. Bai, X.J. Yu, J.Y. Lv, B. Hu,
Biometrics 48 (1992) 361-372.
Haplotypes of 20 Y-chromosomal STRs in a population [16] J.B.S. Haldane, An exact test for randomness of mating, sample from southeast China (Chaoshan area), Int. J.
Journal of Genetics 52 (1954) 631-635. Legal. Med. 121 (2007) 455-462.
[17] E.J. Louis, E.R. Dempster, An exact test for Hardy-Weinberg [6] L.A. Zhivotovsky, V.M. Veremeichyk, A.I. Mikulich, I.G.
and multiple alleles, Biometrics 43 (1987) 805-811. Udina, L.A. Atramentova, S.A. Kotova, et al., A
E. Bosch, F. Calafell, A.P. Lezaun, J. Clarimon, D. comprehensive population survey on the distribution of
Comas, E. Mateu, et al., Genetic structure of north-west STR frequencies in Belarus, Forensic Science Interational
Africa revealed by STR analysis, European Jouranl of 172 (2007) 156-160.
Human Genetics 8 (2000) 360-366. [7] U.D. Immel, M. Krawczak, J. Udolph, A. Richter, H.
[19] L. Garofano, M. Pizzamiglio, C. Vecchio, Italian Rodig, M. Kleiber, et al., Y-chromosomal STR haplotype
population data in thirteen short tandem repeat loci: analysis reveals surname-associated strata in the
HUMTHO1, D21S11, D18S51, HUMVWFA31, East-German population, European Journal of Human
HUMFIBRA, D8S1179, HUMTPOX, HUMCSF1PO, Genetics 14 (2006) 577-582.
D16S539, D7S820, D13S317, D5S818, D3S1358, [8] P.S. Walsh, D.A. Metzger, R. Higuchi, Chelex 100 as a
Forensic Science International 97 (1998) 53-60. medium for simple extration of DNA for PCR-based
[20] K.M. Chan, C.T. Chiu, P. Tsui, D.M. Wong, W.K. Fung, typing from forensic material, Biotechniques 10 (1991)
Population data for the Identifier 15 STR loci in Hong 506-513.
Kong Chinese, Forensic Science International 152 (2005) [9] P. Wiegand, T. bajanowski, B. Brinkmann, PCR typing
307-309 .
Journal of Life Sciences 5 (2011) 682-689
CCR5-CCR2 Gene Polymorphisms in Ethiopian Jews: Population Divergence and Its Relevance to HIV-1 Infection Resistance
1 2 3 Michael Korostishevsky 4 , Batsheva Bonne-Tamir , Zvi Bentwich , Alexander Kalinkovich and Alexander Tsimanis 5
1. Department of Anatomy and Anthropology, Tel Aviv University, Tel Aviv 69978, Israel 2. Department of Human Molecular Genetics & Biochemistry, Tel Aviv University, Tel Aviv 69978, Israel 3. Rosetta Genomics, Rehovot 76706, Israel 4. Department of Immunology, Weizmann Institute of Science, Rehovot 76100, Israel 5. Biona Ltd, Rehovot 76120, Israel
Received: January 25, 2011 / Accepted: May 18, 2011 / Published: September 30, 2011.
Abstract: CCR5 and CCR2 genes have been implicated in HIV disease progression and HIV resistance in various human populations but not in the Ethiopian Jews. The authors examined polymorphisms in the CCR5-CCR2 gene region in two groups of Ethiopian Jews,
29 non-exposed and 13 exposed but uninfected individuals. Prevalence of the CCR2-V64I and CCR5-32 mutations as well as genetic variations in the CCR5 promoter region at positions 208, 627, 676 and 927 has been studied. The authors confirmed the absence of CCR5-32 mutation in all individuals studied. Three CCR5 single-nucleotide polymorphisms (SNPs) G208T, T627C and A676G were in tight linkage disequilibrium (LD) with each other. In contrast, a lack of LD was observed across the above-mentioned SNPs and proximal SNPs C927T and distal CCR2-G190A. Only four CCR5 haplotypes - HHA, HHC, HHE and HHF*2 were identified in both
groups. Using multi-SNP analysis, no significant differences in the genotype frequencies between the groups were found ( 2 χ 3df = 4.66, P = 0.198). Observed deviation in a single SNP allele frequency (T627C SNP: 2 χ 1df = 4.14, P = 0.042) was not preserved after the Bonferroni correction. Allelic frequencies were compared to other geographically targeted worldwide populations, where clear distinction between Ethiopian Jews and Africans has been found. These data were reflected in the phylogenetic tree, in which Ethiopian Jews branch with Asians.
Key words: CCR5 and CCR2 polymorphism, Ethiopian Jews, HIV-1 infection resistance.
1. Introduction of CCR5 (CCR5-32) and a single conservative valine-to-isoleucine (V64I) mutation in CCR2 coding
The observation that chemokine receptors are used region (CCR2-G190A) have been identified. These by HIV as coreceptor for the cellular entry led to the highly specific polymorphisms are distributed through discovery of genetic factors that can affect susceptibility the world population with differing frequencies to infection with HIV or the rate of progression to dependent on ethnic groups and any particular disease once infection is established [1, 2]. Functionally population group contains a distinctive set of haplotype important polymorphisms in the regulatory region of pair combinations. The finding that polymorphisms in CCR5 gene, a 32-base pair deletion in the coding part the promoter region of CCR5 gene are associated with
differential HIV-1 disease progression suggests that Corresponding author: Michael Korostishevsky, Ph.D., senior scientist, research field: genetic epidemiology. E-mail:
these haplotypes are not functionally similar [3-7]. korost@post.tau.ac.il.
CCR5-CCR2 Gene Polymorphisms in Ethiopian Jews:
Population Divergence and Its Relevance to HIV-1 Infection Resistance
CCR5-32 deletion is the best characterized genetic of CCR2 gene. The authors estimated the magnitude of trait. In the epidemiological studies, the allelic frequency
linkage disequilibrium between the SNPs and of the deletion was 10%-20% among Caucasians,
performed multi-SNP analysis between the samples. particularly amongst those of Northen European descent
Using the CCR5 haplotype distribution data for with 1% homozygosity. This mutation is extremely rare
different ethnic groups, the authors investigated the in African and Asian population [8, 9]. Individuals
phylogenetic relationships for Ethiopian Jews. homozygous for CCR5-32 mutation are almost
2. Materials and Methods
completely resistant to HIV infection most probably due to lack of CCR5 receptor on their cell surfaces [10].
2.1 Subjects
Studies of CCR5-32 mutation in exposed but uninfected
A total of 29 HIV-1-negative (control) and 13 individuals have revealed that only a small proportion of exposed but uninfected seronegative (ESN) Ethiopian them were homozygous for this mutation [11]. Jews were sampled for this study. The evaluation of Heterozygosity for CCR5-32 mutation is associated
clinical status of individuals including the presence of with delayed progression to AIDS in infected
antibodies to HIV-1 and HIV-1 viral particles has been individuals. Moreover, frequency of heterozygosity is
performed in the Kaplan Medical Center, Rehovot, significantly higher in long term non-progressors than in
Israel, as described [17]. Samples were coded and progressors and rapid progressors [8-10, 12, 13]. The
mechanism of protection is not clear and it is believed tested blind. Informed consent was obtained for the that CCR5 expression may be altered in these
collected samples.
individuals. CCR2-V64I mutation is associated with
2.2 Genotyping
delay in progression to AIDS, probably due to the heterodimerization and sequestration of the CCR5
The authors verified the presence of CCR5- Δ32 receptor [14, 15].
deletion and genotyped sequence variations for the Our research focused on CCR5 genetics of Ethiopian
single-nucleotide polymorphism (SNP) G208T, T627C, Jews currently living in Israel. This population
A676G and C927T in the CCR5 promoter region as originated in the north of Lake Tana in Gondar,
well as G190A mutation in the coding part of CCR2 Ethiopia, and several thousands of them were airlifted
gene. The authors used genomic DNA obtained from to Israel first during the Ethiopian civil war (1984-1985)
peripheral blood lymphocytes. The DNA samples were and then in 1989.
subjected to a polymerase chain reaction-restriction The purpose of this study was to examine whether
fragment length polymorphism (PCR-RFLP) assay as the DNA polymorphisms at the loci that encode CCR5
previously described [12, 18, 19]. PCR amplification and CCR2 receptors, can potentially explain the
was performed to amplify CCR5 promoter and CCR5 persistent seronegativity in a group of exposed
and CCR2 genes fragments covering the polymorphic seronegative (ESN) individuals. Using sites (Table 1). evolutionary-based CCR5 haplotype classification [3,
For CCR2-V64I mutation, the PCR products were 16], the authors have characterized this polymorphism
digested with FokI. After digestion, the products of in two groups of Ethiopian Jews: Healthy individuals
digestion for CCR2 and the PCR products for delta-32 without any history of HIV infection or ESN
CCR5 were loaded on a 4% agarose gel in 0.5 × TBE individuals. The authors assessed of CCR5-32 deletion
and electrophoresed at 85 V for 2 hours. as well as several single nucleotide polymorphisms
CCR5 promoter polymorphism was also detected by (SNPs) in the CCR5 promoter region and coding part
PCR amplification using [- 32 P]-dATP. PCR products
CCR5-CCR2 Gene Polymorphisms in Ethiopian Jews: Population Divergence and Its Relevance to HIV-1 Infection Resistance
Table 1 SNPs and primer to PCR-amplify the CCR5 and CCR2 genes.
G190A, CCR2 ORF
5’GAC AGA AGC AAA CAC AGC CA3’ G208T, CCR5 Exon1
F 5’ACG GTG CTC CCT GTC ATA AA3’
F9 5’GAT TCT GTG TAG TGG GAT GAG C3’
5’GAG TTT CTT GTA GGG GAA CGG3’ T627C, CCR5 Exon2
A676G, CCR5 Exon2
F8 5’CTC ATC TGG CCA GAA GAG CTG3’ C927T, CCR5 Exon3
5’ACT GTG ACC CTT TCC TTA TC3’
CCR5- Δ32 ORF
62,036-62,067
5A 5’AGG TCT TCA TTA CAC CTG CAG C3’ 5B 5’CCT CTC ATT TCG ACA CCG AAG C3’
*The numbering of nucleotide positions is based on GenBank sequence U95626.
were resolved by electrophoresis in 6.5% that amplified the region encoding the 32-bp deletion. polyacrylamide gel.
CCR5-32 deletion was not detected in either the control or ESN groups, indicating that this mutant allele is
2.3 Statistical Analysis probably rare or absent in the Ethiopian Jewish
Genotype and allele frequencies of the SNPs were population. CCR5-32 allele is very common in white calculated by direct counting. Possible differences in
populations, yet this allele is rare in people of African the frequencies of each of the SNP genotypes and
and Asian descent including Ethiopian Jews [30]. alleles between the samples were estimated using the 2 χ The results of LD tests between pairs of SNP markers
test, as described elsewhere [20, 21]. The Arlequin for ESN and control groups are depicted in Fig. 1. As software package [22] was used for: 1) Evaluation of
can be seen, three internal SNPs, CCR5-G208T, genetic distances between different populations [23]; 2)
CCR5-T627C and CCR5-A676G, demonstrated Estimation of pairwise LD between the SNP markers
significant linkage disequilibrium (P < 0.05). Distal [24, 25]; 3) Detection of departure from SNP CCR2-G190A and proximal CCR5-C927T were Hardy-Weinberg equilibrium (HWE) [26]; and 4)
found in strong linkage disequilibrium (P < 0.0005), Calculation of the maximum likelihood (ML) of
while a lack of linkage disequilibrium between them haplotype frequencies [27].
and the internal SNPs was observed. Our results Based on the ML haplotype frequency estimates, the
confirmed the strong linkage disequilibrium between likelihood ratio test (LRT) for sample differentiation
CCR2-64I and CCR5-927T, which had been reported was evaluated as previously described [28]. PHYLIP
previously [31].
software package [29] was used for phylogeny Allelic and genotype frequencies for the CCR2-G190A and four CCR5 promoter
inferences based on the CCR2-CCR5 region genetic polymorphisms among the control and ESN
distances. The Bonferroni corrections were performed
individuals are shown in Table 2.
by the SISA online procedure
A discrepancy in allelic frequency between the (http://home.clara.net/sisa/bonfer.htm).
control and ESN individuals was found for the
3. Results and Discussion 2 CCR5-A676G SNP ( χ
1df = 4.14, P = 0.042). The association suggests that this mutation may be tracking
3.1 Genotype and Allele Frequencies the same effect on HIV-1 disease progression.
Both the control and ESN groups were genotyped for However, this deviation of one from five SNPs typed in the CCR5-32, CCR2-G190A and CCR5 promoter
this study is not preserved after the Bonferroni alleles constituting the CCR5 human haplotypes.
correction, which takes into account multiple-test The authors performed DNA PCR by use of primers
problem.
CCR5-CCR2 Gene Polymorphisms in Ethiopian Jews:
Population Divergence and Its Relevance to HIV-1 Infection Resistance
SNP
V64I G208T T627C A676G C927T
V64I G208T T627C
A676G C927T
Fig. 1 Significance level for pairwise LD in the ESN and control samples. LD significance above the diagonal corresponds to the ESN sample and below the diagonal to the control sample (white: P > 0.05; gray: 0.005 < P < 0.05; dark gray: 0.0005 < P < 0.005; black: P < 0.0005).
Table 2 Genotype and allele frequencies of each SNP 1 in ESN and control samples.
SNPs Genotype distribution Allele distribution
2 χ 2 test Allele ESN Control χ test CCR2-64I
ID 2 Position 3 Genotype ESN
Control
0.40 (G190A)
CCR5-G208T 58,934 GG 7 8 3.87 3.09 G 20 33
GT 6 17 TT 0 4
T6 25
CCR5-T627C 59,353 TT 1 8 4.57 4.14 T9 34
CT 7 18 CC 5 3
C 17 24
CCR5-A676G 59,402 AA 7 8 3.87 3.09 A6 33
AG 6 17 GG 0
G 20 25
CCR5-C927T 59,653 TT 1 0 2.29 0.40 C 19 46
CT 5 12 CC 7 17
T7 12
1 SNPs that were non-polymorphic in both samples are not presented in the table: CCR5-A29G (100% A) and CCR5-630 (100% C). 2 SNP designations are according to Ref. [32]. 3 The numbering of nucleotide positions is based on GenBank sequence U95626.
CCR5-CCR2 Gene Polymorphisms in Ethiopian Jews: Population Divergence and Its Relevance to HIV-1 Infection Resistance
3.2 Haplotype Polymorphism pairs was HHC/HHE (23.1%), followed by HHC/HHF*2, HHE/HHE and HHE/HHF*2, the
Only four haplotypes among known CCR5 haplotypes that were the most common pairs. Such haplotypes were detected in ESN and control distribution of haplotype pairs, both in the control and individuals (Table 3). ESN groups are typical of Caucasians, whereas two The haplotypes are notated according to the pairs, HHA/HHA and HHA/HHF*2 haplotypes, evolutionary-based classification of the CCR5 [3, 16]. typical of Africans [32] were rare in Ethiopian Jews. The HHF*2 frequency in the ESN individuals is It has been previously shown that polymorphism in slightly higher than that in the control group (26.9% vs. the CCR5 promoter region is involved in HIV-1 20.7%), although the difference did not attain statistical infection, disease progression, and disease transmission significance. In the control group, the most common [12, 14, 33, 34]. However, comparative analysis of CCR5 haplotype was HHC (43.1%), whereas among CCR5 polymorphisms undertaken in ESN individuals ESN individuals, the most common haplotype was for three ethnic groups (Caucasian, Asian and African) HHE (38.6%). Of note, both haplotypes have significantly revealed the controversial results. Mangano et al. higher frequencies in Caucasians [3]. The minor examined 649 HIV-1-exposed Argentinean children at haplotype in both studied groups was HHA (15.5% and risk for parental infection, and found that the frequency 11.5%, respectively), which is more frequent in of HHE-containing haplotypes was higher in the
Africans. However, the multi-SNP likelihood ratio test HIV-positive children. Moreover, homozygosity and
did not find significant differences between the studied
heterozygosity of HHE haplotype have been suggested groups ( χ 3df = 4.66, P = 0.198). Interestingly, as major factors associated with an increased risk of
genotyping of samples from both studied groups failed parental infection whereas delay in progression to AIDS
to detect presence of HHD and/or HHB haplotypes, which are specific to African population [3, 16].
is associated with HHF*2 haplotype [35]. Gonzalez et al. have found that HHE haplotype influenced the
Eight different genotypes were found in the control outcome of European Americans adults [3]. Although
group: HHA/HHA, HHA/HHC, HHA/HHF*2, HHF*2 and HHE haplotypes are associated with the
HHA/HHE, HHC/HHC, HHC/HHE, HHC/HHF*2, opposite effects, both haplotypes are carriers of
HHE/HHF*2. In the ESN group seven haplotype pair “non-protective” 303-a allele and in the luciferase assay
combinations, namely HHA/HHC, HHA/HHF*2, exhibit the highest transcriptional activity [16]. HHF*2
HHA/HHE, HHC/HHE, HHC/HHF*2, HHE/HHE and homozygosity was also associated with HIV-1
HHF*2/HHF*2 were detected. In the control group, the resistance in discordant couple cohort from Thailand. most prevalent haplotype pairs were HHC/HHF2 Furthermore, in vitro infection experiments showed that (27.6%), followed by HHC/HHC and HHC/HHE. On PBMC isolated from the HIV-1-exposed and the other hand, in the ESN group the leading haplotype unexposed seronegative women carrying different
Table 3 ML estimates of haplotype frequencies in ESN and
CCR5 haplogroups (including HHF*2/HHF*2) had no
control samples.
differences in susceptibility to HIV-1 infection [36, 37]. Haplotype HH ESN Control OR LRT*(P-value)
A cohort study of Ugandan population showed no G-G-C-A-C HHE 0.385 0.207 1.859 association between CCR5 polymorphisms and the rate G-T-T-G-C HHC 0.231 0.431 0.535
A-G-C-A-T HHF*2 0.269 0.207 1.301 of disease progression [38]. Polymorphisms in the
G-G-T-A-C HHA 0.115 0.155 0.744 CCR5 promoter region may influence cell surface * The likelihood ratio test (LRT) for sample differentiation was
expression and consequently could influence individual evaluated as previously described [28].
susceptibility to HIV [39]. However, similar expression
CCR5-CCR2 Gene Polymorphisms in Ethiopian Jews:
Population Divergence and Its Relevance to HIV-1 Infection Resistance
level of CCR5 was found in HIV-exposed uninfected
3.3 Population Divergence
females and unexposed controls from Kenya and Using the CCR5-CCR2 haplotype frequency Ethiopia [40, 41]. Taken together, these data suggest estimates, the genetic distances (Corrected Average that the distribution of polymorphisms in CCR5 Pairwise Difference: ARLEQUIN software package) promoter region varies significantly across between Ethiopian Jews and other 7 populations were race/ethnicity groups, so that the same mutation in
evaluated (Table 4).
different race groups may have various or even opposite The population relationship reconstructed by using
functional effects. these distances (the UPGMA algorithm: PHYLIP
Study of the genetic structure of Ethiopian Jews by software package) was also undertaken and the results
using mtDNA and some nonrecombinant Y-chromosome markers and 5’-globin haplotypes
are depicted in Fig. 2.
elements clearly demonstrated that Ethiopian Jews are As can be seen, the dendrogram shows two
a mixture of African and Caucasian (Asian) population well-defined population groups: The first one and are significantly different from other Jewish
containing two populations, namely Non-Pygmy and communities [42-46]. Several authors argued that
American Africans, and the second one containing the Ethiopian Jews derive mostly from Africans [47];
remaining six populations, which are further divided. however, both cultural and historic evidence shows
Within these groups, Ethiopian Jews are “sisters” to tight relationship between populations of Ethiopia and
Asian populations (non-Indians and Indians), while Asia (Near East and southern Arabia).
Thai population is found to be the most distant.
Table 4 Population average pairwise differences*.
Population Non-pygmy Afr. Amer European Non-indian Indian Eth. Jews Thai Argentina Non-pygmy # 0.78 0.79 0.83 0.85 0.83 0.85 0.87 0.83 Afr. Amer # 0.21 0.79 0.82 0.81 0.82 0.83 0.81 0.81 European # 11.04 7.26 0.66 0.71 0.71 0.72 0.7 0.73 Non-indian # 11.07 7.72 3.14 0.7
0.73 0.71 0.66 0.73 Indian # 7.44 4.55 1.49 1.56 0.73 0.73 0.7 0.75 Eth. Jews
10 6.92 3.64 0.16 0.41 0.72 0.66 0.74 Thai ##
19.36 15.17 8.03 2.75 4.91 1.77 0.57 0.7 Argentina # 6.5 3.94 2.45 0.88 0.99 1.09 4.27 0.75 *Above diagonal: Average number of pairwise differences between populations, d(ij).
Diagonal elements: Average number of pairwise differences within population, d(i). Below diagonal: Corrected average pairwise difference, d(i, j)-(d(i)+d(j))/2. Row data of CCR5 haplotypes distribution was taken from: # - [32] and ## - [37].
NON-PYGMY
4. Conclusion
AFR. AMER.
EUROPEAN
No statistically significant differences between HIV-
NON-INDIAN
unexposed and exposed uninfected Ethiopian Jews at
ETH. JEWS
the allele, genotype, or haplotype level have been found.
INDIAN ARGENTINA
The pattern of CCR5-CCR2 genetic variations in Eth-
iopian Jews resembles the one found in Asian populations
THAI
Fig. 2 UPGMA tree based on CCR5 haplotype frequencies.
and is distinguished from that found in Africans.
CCR5-CCR2 Gene Polymorphisms in Ethiopian Jews: Population Divergence and Its Relevance to HIV-1 Infection Resistance
Acknoledgments
HIV-1 infection of CD4 lymphocytes from persons who remain uninfected despite multiple high-risk sexual
The authors thank M.Malasky for dedicated exposure, Nature Medicine 2 (4) (1996) 412-417. technical assistance. [12] M.P. Martin, M. Dean, M.W. Smith, C. Winkler, B. Gerrard, N.L. Michael, et al., Genetic acceleration of
References
AIDS progression by a promoter variant of CCR5, Science 282 (5395) (1998) 1907-1911.
[1] J.P. Moore, A. Trkola, T. Dragic, Co-receptors for HIV-1 [13] A.M. de Roda Husman, M. Koot, M. Cornelissen, I.P. entry, Curr. Opin. Immunol. 9 (4) (1997) 551-562.
Keet, M. Brouwer, S.M. Broersen, et al., Association [2] O.J. Cohen, A. Kinter, A.S. Fauci, Host factors in the
between CCR5 genotype and the clinical course of HIV-1 pathogenesis of HIV disease, Immunol. Rev. 159 (1997)
infection, Ann. Intern. Med. 127 (10) (1997) 882-890. 31-48.
[14] L.G. Kostrikis, Y. Huang, J.P. Moore, S.M. Wolinsky, L. [3]
E. Gonzalez, M. Bamshad, N. Sato, S. Mummidi, R. Zhang, Y. Guo, et al., A chemokine receptor CCR2 allele Dhanda, G. Catano, et al., Race-specific HIV-1
delays HIV-1 disease progression and is associated with a disease-modifying effects associated with CCR5
CCR5 promoter mutation, Nature Medicine 4 (3) (1998) haplotypes, Proc. Natl. Acad. Sci. 96 (21) (1999)
350-353.
12004-12009. [15] M. Mellado, J.M. Rodriguez-Frade, A.J. Vila-Coro, A.M. [4] S.J. O’Brien, J.P. Moore, The effect of genetic variation in
de Ana, A.C. Martinez, Chemokine control of HIV-1 chemokines and their receptors on HIV transmission and
infection, Nature 400 (6746) (1999) 723-724. progression to AIDS, Immunol. Rev. 177 (2000) 99-111.
[16] S. Mummidi, M. Bamshad, S.S. Ahuja, E. Gonzalez, P.M. [5] J. Tang, B. Shelton, N.J. Makhatadze, Distribution of
Feuillet, K. Begum, et al., Evolution of human and chemokine receptor CCR2 and CCR5 genotypes and their
non-human primate CC chemokine receptor 5 gene and relative contribution to human immunodeficiency virus
mRNA: Potential roles for haplotype and mRNA diversity, type 1 (HIV-1) seroconversion, early HIV-1 RNA
differential haplotype-specific transcriptional activity, and concentration in plasma, and later disease progression, J.
altered transcrition factor binding to polymorphic Virol. 76 (2) (2002) 662-672.
nucleotides in the pathogenesis of HIV-1 and simian [6] P.S. Kulkarni, S.T. Butera, A.C. Duerr, Resistance to
immunodeficiency virus, J. Biol. Chem. 275 (25) (2000) HIV-1 infection: Lessons learned from studies of highly
18946-18961.
exposed persistently seronegative (HEPS) individuals, [17] Z. Weisman, A. Kalinkovich, G. Borkow, M. Stein, Z. AIDS Rev. 5 (2) (2003) 87-103.
Greenberg, Z. Bentwich, Infection by different HIV-1 [7] M. Li, R. Song, S. Masciotra, V. Soriano, T.J. Spira, R.B.
subtypes (B and C) results in a similar immune activation Lal, et al., Association of CCR5 human haplogroup E with
profile despite distinct immune backgrounds, J. Acquir. rapid HIV type 1 disease progression, AIDS Res. Hum.
Immune Defic. Syndr. 21 (2) (1999) 157-163. Retroviruses 21 (2) (2005) 111-115.
[18] M. Carrington, M. Dean, M.P. Martin, S.J. O’Brien, [8] M. Dean, M. Carrington, C. Winkler, G.A. Huttley, M.W.
Genetics of HIV-1 infection: Chemokine receptor CCR5 Smith, R. Allikmets, et al., Genetic restriction of HIV-1
polymorphism and its consequences, Hum. Mol. Genet. 8 infection and progression to AIDS by a deletion allele of
(10) (1999) 1939-1945.
the CKR5 structural gene, Science 273 (5283) (1996) [19] M.W. Smith, M. Dean, M. Carrington, C. Winkler, G.A. 1856-1862.
Huttley, D.A. Lomb, et al., Contrasting genetic influence [9] P.A. Zimmerman, A. Buckler-White, G. Alkhatib, T.
of CCR2 and CCR5 variants on HIV-1 infection and Spalding, J. Kubofcik, C. Combadiere, et al., Inherited
disease progression, Science 277 (5328) (1997) 959-965. resistance to HIV-1 conferred by an inactivating mutation
[20] J.H. Abramson, P.M. Gahlinger, Computer Program for in CC chemokine receptor 5: Studies in populations with
Epidemiologists, PEPI version 3, Brixton Books, London, contrasting clinical phenotypes, defined racial background,
and quantified risk, Mol. Med. 3 (1) (1997) 23-36. [21] L. Komlos, M. Korostishevsky, I. Halbrecht, D. Vardimon, [10] R. Liu, W.A. Paxton, S. Choe, D. Ceradini, S.R. Martin, R.
Z. Ben-Rafael, T. Klein, Possible sex-correlated Horuk, et al., Homozygous defect in HIV-1 coreceptor
transmission of maternal class I HLA haplotypes, Eur. J. accounts for resistance of some multiply-exposed
Immunogenet. 24 (3) (1997) 169-177. individuals to HIV-1 infection, Cell 86 (3) (1996)
[22] S. Schneider, D. Roessli, L. Excoffer, M. Arlequin, A 367-377.
software for population genetic data analysis, version 2.00, [11] W.A. Paxton, S.R. Martin, D. Tse, T.R. O’Brien, J.
University of Geneva, Switzerland, 2000. Skurnick, N.L. VanDevanter, et al., Relative resistance to
http://Lgb.unige.ch/arlequin.
CCR5-CCR2 Gene Polymorphisms in Ethiopian Jews:
Population Divergence and Its Relevance to HIV-1 Infection Resistance
[23] M. Nei, Molecular Evolutionary Genetics, Columbia of HIV-1 discordant couples in Thailand: Association of University Press, New York, 1987.
CCR2 64I homozygosity with HIV-1-negative status, J. [24] M. Slatkin, Linkage disequilibrium in growing and stable
Acquir. Immune Defic. Syndr. 29 (3) (2002) 314-315. population, Genetics 137 (4) (1994) 331-336.
C. Yang, M. Li, K. Limpakarnjanarat, N.L. Young, T. [25] M. Slatkin, L. Excoffier, Testing for linkage
Hodge, S.T. Butera, et al., Polymorphisms in the CCR5 disequilibrium in genotypic data using the EM algorithm,
coding and noncoding regions among HIV type 1-exposed, Heredity 76 (4) (1996) 377-383.
persistently seronegative female sex-workers from [26] S.W. Guo, E.A. Thompson, Performing the exact test of
Thailand, AIDS Res. Hum. Retroviruses 19 (8) (2003) Hardy-Weinberg proportion for multiple alleles,
661-665.
Biometrics 48 (2) (1992) 361-372. [38] P.A. Ramaley, N. French, P. Kaleebu, C. Gilks, J. [27] L. Excoffier, M. Slatkin, Maximum-likelihood estimation
Whitworth, A.V. Hill, Chemokine-receptor genes and of molecular haplotype frequencies in a diploid population,
AIDS risk, Nature 417 (6885) (2002) 140. Mol. Biol. Evol. 12 (5) (1995) 921-927.
[39] J.R. Salkowitz, S.E. Bruse, H. Meyerson, H. Valdez, D.E. [28] M. Korostishevsky, I. Kremer, M. Kaganovich, A.
Mosier, C.V. Harding, et al., CCR5 promoter Cholostoy, I. Murad, M. Muhaheed, et al., Transmission
polymorphism determines macrophage CCR5 density and disequilibrium and haplotype analysis of the G72/G30
magnitude of HIV-1 propagation in vitro, Clin. Immunol. locus: suggestive linkage to schizophrenia in Palestinian
108 (3) (2003) 234-240.
Arabs living in North of Israel, Am. J. Med. Genet. Part B: [40] K.R. Fowke, T. Dong, S.L. Rowland-Jones, J. Oyugi, W.J. Neuropsychiatr. Genet. 141 (1) (2006) 91-95.
Rutherford, J. Kimani, et al., HIV type 1 resistance in [29] PHYLIP Phylogeny Inference Package, Release 3.57c,
Kenyan sex workers is not associated with altered cellular University of Washington, USA, available online at:
susceptibility to HIV type 1 infection or enhanced http://evolution.genetics.washington.edu/phylip.html, 1995.
β-chemokine production, AIDS Res. Hum. Retroviruses [30] R. Kantor, J.M. Gershoni, Distribution of the CCR5 gene
14 (17) (1998) 1521-1530.
32-base pair deletion in Israeli ethnic groups, J. Acquir. [41] T. Messele, T.F. Rinke de Wit, M. Brouwer, M. Aklilu, T. Immune Defic. Syndr. Hum. Retrovirol. 20 (1) (1999)
Birru, A.L. Fontanet, et al., No difference in in vitro 81-84.
susceptibility to HIV type 1 between high-risk [31] J.J. Martinson, L. Hong, R. Karanicolas, J.P. Moore, L.G.
HIV-negative Ethiopian commercial sex workers and Kostrikis, Global distribution of the
low-risk control subjects, AIDS Res. Hum. Retroviruses CCR2-64I/CCR5-59653T HIV-1 disease-protective
17 (5) (2001) 433-441.
A. Zoossmann-Diskin, A. Ticher, I. Hakim, Z. Goldwitch, [32]
haplotype, AIDS 14 (5) (2000) 483-489.
E. Gonzalez, R. Dhanda, M. Bamshad, S. Mummidi, R. A. Rubinstein, B. Bonne-Tamir, Genetic affinities of Geevarghese, G. Catano, et al., Global survey of genetic
Ethiopian Jews, Isr. J. Med. Sci. 27 (5) (1991) 245-251. variation in CCR5, RANTES, and MIP-1: Impact on the
[43] U. Ritte, E. Neufeld, M. Broit, D. Shavit, U. Motro, The epidemiology of the HIV-1 pandemic, Proc. Natl. Acad.
differences among Jewish communities-maternal and Sci. USA 98 (9) (2001) 5199-5204.
paternal contributions, J. Mol. Evol. 37 (4) (1993) [33]
D.H. McDermott, P.A. Zimmerman, F. Guignard, C.A.
435-440.
Kleeberger, S.F. Leitman, Multicenter AIDS Cohort Study
G. Lucotte, P. Smets, Origins of Falasha Jews studied by (MACS), CCR5 promoter polymorphism and HIV-1
haplotypes of the Y chromosome, Hum. Biol. 71 (6) (1999) disease progression, Lancet 352 (9131) (1998) 866-870.
989-993.
[34] S. Mummidi, S. Ahuja, E. Gonzalez, S.A. Anderson, E.N. [45] M.F. Hammer, A.J. Redd, E.T. Wood, M.R. Bonner, H. Santiago, K.T. Stephan, et al., Geneology of the CCR5
Jarjanazi, T. Karafet, et al., Jewish and Middle Eastern locus and chemokine system gene variants associated with
non-Jewish populations share a common pool of altered rates of HIV-1 disease progression, Nature
Y-chromosome biallelic haplotypes, Proc. Natl. Acad. Sci. Medicine 4 (7) (1998) 786-793.
97 (12) (2000) 6769-6774.
[35] A. Mangano, E. Gonzalez, R. Dhanda, G. Catano, M. [46] N. Rosenberg, E. Woolf, J.K. Pritchard, T. Schaap, D. Bamshad, A. Bock, et al., Concordance between the CC
Gefel, I. Shpirer, et al., Distinctive genetic signatures in chemokine receptor 5 genetic determinants that alter risks
the Libyan Jews, Proc. Natl. Acad. Sci. 98 (3) (2001) of transmission and disease progression in children
858-863.
exposed perinatally to human immunodeficiency virus, J. [47] T. Kivisild, M. Reidla, E. Metspalu, A. Rosa, A. Brehm, E. Infect. Dis. 183 (11) (2001) 1574-1585.
Pennarun, et al., Ethiopian mitochondrial heritage: [36] S. Louisirirotchanakul, H. Liu, A. Roongpisuthipong, E.E.
Tracking gene flow across and around the gate of tears, Nakayama, Y. Takebe, T. Shioda, et al., Genetic analysis
Am. J. Hum. Genet. 75 (5) (2004) 752-770.
Journal of Life Sciences 5 (2011) 690-696
First Record of Frankliniella Occidentalis and Impatiens Necrotic Spot Virus in Egypt