Is the European spatial distribution of the HIV-1-resistant CCR5-Δ32 allele formed by a breakdown of the pathocenosis due to the historical Roman expansion?

Infection, Genetics and Evolution

Volumn 8, Issue 6, 2008, Pages 864-874

  Faure, Eric ^a   Royer Carenzi, Manuela ^a  

^a LATP   (France)

Author keywords

32 allele; Ancient Mediterranean civilizations; Chemokine receptor CCR5; Geographic distribution; Roman Empire

Indexed keywords

CHEMOKINE RECEPTOR CCR5; DNA;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ALLELE; ARTICLE; ASIA; CAUCASIAN; CORRELATION ANALYSIS; DISEASE COURSE; EUROPE; GENE DELETION; GENE FREQUENCY; GENE MUTATION; GENETIC SELECTION; HISTORY; HOMOZYGOSITY; HOST RESISTANCE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; PRIORITY JOURNAL; VIRUS RESISTANCE; VIRUS TRANSMISSION; WEST NILE FLAVIVIRUS; ZOONOSIS;

ANALYSIS OF VARIANCE; DEMOGRAPHY; EUROPEAN CONTINENTAL ANCESTRY GROUP; EVOLUTION, MOLECULAR; GENE FLOW; GENE FREQUENCY; GEOGRAPHY; HISTORY, ANCIENT; HIV INFECTIONS; HIV-1; HUMANS; IMMUNITY, INNATE; LINEAR MODELS; MUTATION; RECEPTORS, CCR5; ROMAN WORLD; SELECTION (GENETICS);

HUMAN IMMUNODEFICIENCY VIRUS 1; WEST NILE VIRUS;

EID: 55649125036     PISSN: 15671348     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.meegid.2008.08.007     Document Type: Article

References (134)

1. Ajuebor M.N., Carey J.A., and Swain M.G. CCR5 in T cell-mediated liver diseases: what's going on?. J. Immun. 177 (2006) 2039-2045
2. Alvarez V., López-Larrea C., and Coto E. Mutational analysis of the CCR5 and CXCR4 genes (HIV-1 co-receptors) in resistance to HIV-1 infection and AIDS development among intravenous drug users. Hum. Genet. 102 (1998) 483-486
3. Apostolakis S., Baritaki S., Krambovitis E., and Spandidos D.A. Distribution of HIV/AIDS protective SDF1,CCR5 and CCR2 gene variants within Cretan population. J. Clin. Virol. 34 (2005) 310-314
4. Arenzana-Seisdedos F., and Parmentier M. Genetics of resistance to HIV infection: role of co-receptors and co-receptor ligands. Semin. Immunol. 18 (2006) 387-403
5. Balanovsky O., Pocheshkhova E., Pshenichnov A., Solovieva D., Kuznetsova M., Voronko O., Churnosov M., Tegako O., Atramentova L., Lavryashina M., Evseeva I., Borinska S., Boldyreva M., Dubova N., and Balanovska E. Is spatial distribution of the HIV-1-resistant CCR5Delta32 allele formed by ecological factors?. J. Physiol. Anthropol. Appl. Hum. Sci. 24 (2005) 375-382
6. Balanovsky, O.P., Shadrina, M.I., Limborska, S.A., Balanovska, E.V., 2001. Global distribution of the CCR5Δ 32 mutation, causing resistance to HIV-1 infection: does it depend on climate, or history, or diseases? (Materials of the first 380 CCR5 Geographic Distribution international young medics' conference "Young doctors on the threshold of the third millennium", Yerevan, Armenia) (in Russian).
7. Balistreri C.R., Caruso C., Grimaldi M.P., Listì F., Vasto S., Orlando V., Campagna A.M., Lio D., and Candore G. CCR5 receptor: biologic and genetic implications in age-related diseases. Ann. N.Y. Acad. Sci. 1100 (2007) 162-172
8. Barbouche R.M., Hong L., Dellagi K., and Kostrikis L.G. Contrasting frequencies of CCR5delta32 and CCR2-64I alleles in the Tunisian population. J. Acquir. Immune Defic. Syndr. 26 (2001) 289-298
9. Battiloro E., Andreoni M., Parisi S.G., Mura M.S., Sotgiu G., Aceti A., Cossu G., Concia E., Verna R., and D'Ambrosio E. Distribution of the CCR5 delta32 allele in Italian HIV type 1-infected and normal individuals. AIDS Res. Hum. Retroviruses 16 (2000) 181-182
10. Beaumont R.L. Greek Influence in the Adriatic Sea before the Fourth Century B.C. J. Hellen. Stud. 56 (1936) 159-204
11. Biti R., Ffrench R., Young J., Bennetts B., Stewart G., and Liang T. HIV-1 infection in an individual homozygous for the CCR5 deletion allele. Nat. Med. 2 (1996) 1240-1243
12. Black F.L. Measles endemicity in insular populations: critical community size and its evolutionary implication. J. Theor. Biol. 11 (1996) 207-211
13. In: Bunak V.V. (Ed). Origin and Ethnic History of Russian People: Anthropological Data (1965), Nauka, Moscow 414 pp. (in Russian).
14. Burnham K.P., and Anderson D.R. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach. second ed. (2002), Springer-Verlag, New York
15. Burns J.C., Shimizu C., Gonzalez E., Kulkarni H., Patel S., Shike H., Sundel R.S., Newburger J.W., and Ahuja S.K. Genetic variations in the receptor-ligand pair CCR5 and CCL3L1 are important determinants of susceptibility to Kawasaki disease. J. Infect. Dis. 192 (2005) 344-349
16. Capasso L., D'Anastasio R., Pierfelice L., Di Fabrizio A., and Gallenga P.E. Roman conquest, lifespan, and diseases in ancient Italy. Lancet 362 (2003) 668
17. In: Cavalli-Sforza L.L. (Ed). Genes, People, and Languages (2002), Harper Collins, Canada 227 pp.
18. Cavalli-Sforza L.L., Menozzi P., and Piazza A. The History and Geography of Human Genes (1994), Princeton University Press, Princeton, NJ 1088 pp.
19. Christensen P.E., Schmidt H., Bang H.O., Andersen V., Jordal B., and Jensen O. An epidemic of measles in Southern Greenland, 1951. Measles in Virgin Soil II. The epidemic proper. Acta Med. Scand. 144 (1953) 431-449
20. Christodoulou C., Poullikas M., Neumann A.U., and Kostrikis L.G. Low frequency of CCR5delta32 allele among Greeks in Cyprus. AIDS Res. Hum. Retroviruses 13 (1997) 1373-1374
21. Clutton-Brock J. Domesticated Animals From Early Times (1981), British Museum (Natural History) and William Heinemann, London 208 pp.
22. Clutton-Brock J. A Natural History of Domesticated Animals (1987), Cambridge University Press, London and Cambridge 208 pp.
23. Cohn Jr. S.K., and Weaver L.T. The Black Death and AIDS: CCR5-Delta32 in genetics and history. Q. J. Med. 99 (2006) 497-503
24. Comrie B. Farming dispersal in Europe and the spread of the Indo-European language family. In: Bellwood P., and Renfrew C. (Eds). Examining the Farming/Language Dispersal Hypothesis (2002), McDonald Institute Monographs, McDonald Institute for Archaeological Research, Cambridge 409-419
25. Cornell T., and Matthews J. Atlas of the Roman World (1991), Stonehenge Press, UK 240 pp. (reprint of Phaidon, 1982)
26. de Silva E., and Stumpf M.P. HIV and the CCR5-Delta32 resistance allele. FEMS Microbiol. Lett. 241 (2004) 1-12
27. Dean M., Carrington M., and O'Brien S.J. Balanced polymorphism selected by genetic versus infectious human disease. Annu. Rev. Genomics Hum. Genet. 3 (2002) 263-292
28. Dean, M., Carrington, M., Winkler, C., Huttley, G.A., Smith, M.W., Allikmets, R., Goedert, J.J., Buchbinder, S.P., Vittinghott, E., Gomperts, E., Donfield, S., Vlahov, D., Kaslow, R., Saah, A., Rinaldo, C., Detels, R., Hemophilia Growth and Development Study, Multicenter AIDS Cohort Study, Multicenter Hemophilia Cohort Study, San Francisco City Cohort, ALIVE Study, O'Brien, S.J., 1996. Genetic restriction of HIV-1 infection and progression to AIDS by a deletion allele of the CCR5 structural gene. Science 273, 1856-1862.
29. Distante S., Robson K.J., Graham-Campbell J., Arnaiz-Villena A., Brissot P., and Worwood M. The origin and spread of the HFE-C282Y haemochromatosis mutation. Hum. Genet. 115 (2004) 269-279
30. Duncan S.R., Scott S., and Duncan C.J. Reappraisal of the historical selective pressures for the CCR5-32 mutation. J. Med. Genet. 42 (2005) 206-208
31. Duncan C.J., and Scott S. What caused the Black Death?. Postgrad. Med. J. 81 (2005) 315-320
32. Elharti E., Elaouad R., Simons M.J., Messouak-Elhachimi Z., Gluckman J.C., Parmentier M., and Benjouad A. Frequency of the CCR5 Delta 32 allele in the Moroccan population. AIDS Res. Hum. Retroviruses 16 (2000) 87-89
33. Elvin S.J., Williamson E.D., Scott J.C., Smith J.N., Pérez De Lema G., Chilla S., Clapham P., Pfeffer K., Schlöndorff D., and Luckow B. Evolutionary genetics: ambiguous role of CCR5 in Y. pestis infection. Nature 430 (2004) 417
34. Eugen-Olsen J., Iversen A.K., Garred P., Koppelhus U., Pedersen C., Benfield T.L., Sorensen A.M., Katzenstein T., Dickmeiss E., Gerstoft J., Skinhoj P., Svejgaard A., Nielsen J.O., and Hofmann B. Heterozygosity for a deletion in the CKR-5 gene leads to prolonged AIDS-free survival and slower CD4 T-cell decline in a cohort of HIV-seropositive individuals. AIDS 11 (1997) 305-310
35. Freitas T., Brehm A., and Fernandes A. Frequency of the CCR5-Δ32 mutation in the Atlantic Island Populations of Madeira, the Azores, Cabo Verde, and São Tomé e Príncipe. Hum. Biol. 78 (2006) 697-703
36. Galvani A.P., and Novembre J. The evolutionary history of the CCR5-Delta32 HIV-resistance mutation. Microbes Infect. 7 (2005) 302-309
37. Galvani A.P., and Slatkin M. Evaluating plague and smallpox as historical selective pressures for the CCR5-delta 32 HIV-resistance allele. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 15276-15279
38. Glass W.G., Lim J.K., Cholera R., Pletnev A.G., Gao J.L., and Murphy P.M. Chemokine receptor CCR5 promotes leukocyte trafficking to the brain and survival in West Nile virus infection. J. Exp. Med. 202 (2005) 1087-1098
39. Glass W.G., McDermott D.H., Lim J.K., Lekhong S., Yu S.F., Frank W.A., Pape J., Cheshier R.C., and Murphy P.M. CCR5 deficiency increases risk of symptomatic West Nile virus infection. J. Exp. Med. 203 (2006) 35-40
40. Gourevitch D. The galenic plague: a breakdown of the imperial pathocoenosis. Pathocoenosis and longue duree. Hist. Philos. Life Sci. 27 (2005) 57-69
41. Grmek M.D. Préliminaires d'une étude des maladies. Ann. Econ. Soc. Civil. 24 (1969) 1437-1483
42. Grmek M.D. Diseases in the Ancient Greek World (1991), Johns Hopkins University Press, Baltimore and London 476 pp.
43. Gross L. A well-studied disease-resistance gene shows no signs of selection. PLoS Biol. 3 (2005) e400
44. Guglielmino C.R., Piazza A., Menozzi P., and Cavalli-Sforza L.L. Uralic genes in Europe. Am. J. Phys. Anthropol. 83 (1990) 57-68
45. Haldane J.B.S. Disease and evolution. Ric. Sci. 19 Suppl. (1949) 333-334
46. Hamblin M.T., Thompson E.E., and Di Rienzo A. Complex signatures of natural selection at the Duffy blood group locus. Am. J. Hum. Genet. 70 (2000) 369-383
47. Hedrick P.W., and Verrelli B.C. "Ground truth" for selection on CCR5-Delta32. Trends Genet. 22 (2006) 293-296
48. Helgason A., Sigur{eth}ardóttir S., Gulcher J.R., Ward R., and Stefánsson K. MtDNA and the origin of the Icelanders: deciphering signals of recent population history. Am. J. Hum. Genet. 66 (2000) 999-1016
49. Helgason A., Sigureth Ardóttir S., Nicholson J., Sykes B., Hill E.W., Bradley D.G., Bosnes V., Gulcher J.R., Ward R., and Stefánsson K. Estimating Scandinavian and Gaelic ancestry in the male settlers of Iceland. Am. J. Hum. Genet. 67 (2000) 697-717
50. Hoffman T.L., MacGregor R.R., Burger H., Mick R., Doms R.W., and Collman R.G. CCR5 genotypes in sexually active couples discordant for human immunodeficiency virus type 1 infection status. J. Infect. Dis. 176 (1997) 1093-1096
51. Huang Y., Paxton W.A., Wolinsky S.M., Neumann A.U., Zhang L., He T., Kang S., Ceradini D., Jin Z., Yazdanbakhsh K., Kunstman K., Erickson D., Dragon E., Landau N.R., Phair J., Ho D.D., and Koup R.A. The role of a mutant CCR5 allele in HIV-1 transmission and disease progression. Nat. Med. 2 (1996) 1240-1243
52. Hummel S., Schmidt D., Kremeyer B., Herrmann B., and Oppermann M. Detection of the CCR5-Δ32 HIV resistance gene in Bronze Age skeletons. Genes Immun. 6 (2005) 371-374
53. Jagodzinski P.P., Lecybyl R., Ignacak M., Juszczyk J., and Trzeciak W.H. Distribution of 32 alelle of the CCR5 gene in the population of Poland. J. Hum. Genet. 45 (2000) 271-274
54. Jennison G. Animals for Show and Pleasure in ancient Rome (1937), Manchester University Press, Manchester 209 pp.
55. Kalev I., Mikelsaar A.V., Beckman L., Tasa G., and Parlist P. High frequency of the HIV-1 protective CCR5 delta32 deletion in native Estonians. Eur. J. Epidemiol. 16 (2000) 1107-1109
56. Kantor R., and Gershoni J.M. Distribution of the CCR5 gene 32-base pair deletion in Israeli ethnic groups. J. Acquir. Immune Defic. Syndr. Hum. Retrovirol. 20 (1999) 81-84
57. Karam W., Jurjus R., Khoury N., Khansa H., Assad C., Zalloua P., and Jurjus A. Frequency of the CCR5-delta 32 chemokine receptor gene mutation in the Lebanese population. East. Mediterranean Health J. 10 (2004) 671-675
58. Klitz W., Brautbar C., Schito A.M., Barcellos L.F., and Oksenberg J.R. Evolution of the CCR5 delta 32 mutation based on haplotype variation in Jewish and Northern European population samples. Hum. Immunol. 62 (2001) 530-538
59. Kremeyer B., Hummel S., and Herrmann B. Frequency analysis of the delta32ccr5 HIV resistance allele in a medieval plague mass grave. Anthropol. Anz. 63 (2005) 13-22
60. Lalani A.S., Masters J., Zeng W., Barrett J., Pannu R., Everett H., Arendt C.W., and McFadden G. Use of chemokine receptors by poxviruses. Science 286 (1999) 1968-1971
61. Libert F., Cochaux P., Beckman G., Samson M., Aksenova M., Cao A., Czeizel A., Claustres M., Rua C., Ferrari M., Ferrec C., Glover G., Grinde B., Guran S., Kucinskas V., Lavinha J., Mercier B., Ogur G., Peltonen L., Rosatelli C., Schwartz M., Spitsyn V., Timar L., Beckman L., Parmentier M., and Vassart G. The Δ CCR5 mutation conferring protection against HIV-1 in Caucasian populations has a single and recent origin in Northeastern Europe. Hum. Mol. Genet. 7 (1998) 399-406
62. Lidén, K., Linderholm, A., Götherström, A., 2006. Pushing it back. Dating the CCR5-Δ32 bp deletion to the Mesolithic in Sweden and its implications for the Meso/Neo transition. Documenta Praehistorica XXXIII, 2006 (Neolithic Studies 13), vol. 633, p. 577.2.
63. Limborska S.A., Balanovsky O.P., Balanovskaya E.V., Slominsky P.A., Schadrina M.I., Livshits L.A., Kravchenko S.A., Pampuha V.M., Khusnutdinova E.K., and Spitsyn V.A. Analysis of CCR5Δ32 geographic distribution and its correlation with some climatic and geographic factors. Hum. Hered. 53 (2002) 49-54
64. Liu R., Paxton W.A., Choe S., Ceradini D., Martin S.R., Horuk R., MacDonald M.E., Stuhlmann H., Koup R.A., and Landau N.R. Homozygous defect in HIV-1 coreceptor accounts for resistance of some multiply-exposed individuals to HIV-1 infection. Cell 86 (1996) 367-377
65. Lucotte G., and Dieterlen F. More about the Viking hypothesis of origin of the delta32 mutation in the CCR5 gene conferring resistance to HIV-1 infection. Infect. Genet. Evol. 3 (2003) 293-295
66. Lucotte G., and Smets P. CCR5-Delta32 allele frequencies in Ashkenazi Jews. Genet. Test. 7 (2003) 333-337
67. Lucotte G. Frequencies of the CC chemokine receptor 5 delta 32 allele in various populations of defined racial background. Biomed. Pharmacother. 51 (1997) 469-473
68. Lucotte G. Distribution of the CCR5 gene 32-basepair deletion in West Europe. A hypothesis about the possible dispersion of the mutation by the Vikings in historical times. Hum. Immunol. 62 (2001) 933-936
69. Lucotte G. Frequency analysis and allele map in favor of the Celtic origin of the C282Y mutation of hemochromatosis. Blood Cells Mol. Dis. 27 (2001) 549-556
70. Lucotte G. Frequencies of 32 base pair deletion of the (Delta 32) allele of the CCR5 HIV-1 co-receptor gene in Caucasians: a comparative analysis. Infect. Genet. Evol. 1 (2002) 201-205
71. Lucotte G. High prevalences of carriers of the 35delG mutation of connexin 26 in the Mediterranean area. Int. J. Pediatr. Otorhinolaryngol. 71 (2007) 741-746
72. Lucotte G., and Dieterlen F. A European allele map of the C282Y mutation of hemochromatosis: Celtic versus Viking origin of the mutation?. Blood Cells Mol. Dis. 31 (2003) 262-267
73. Lucotte G., and Mercier G. Frequency of the coreceptor CCR5 gene delta 32 mutation in different French regions. C. R. Acad. Sci. III 321 (1998) 409-413
74. Lucotte G., and Mercier G. Distribution of the CCR5 gene 32-bp deletion in Europe. J. Acquir. Immune Def. Syndr. Hum. Retrovirol. 19 (1998) 174-177
75. Lucotte G., Mercier G., and Smets P. Elevated frequencies of the mutant allele delta32 at the CCR5 gene in Ashkenazic Jews. AIDS Res. Hum. Retroviruses 15 (1999) 1-2
76. Lusso P. HIV and the chemokine system: 10 years later. EMBO J. 25 (2006) 447-456
77. Maayan S., Zhang L., Shinar E., Ho J., He T., Manni N., Kostrikis L.G., and Neumann A.U. Evidence for recent selection of the CCR5-delta 32 deletion from differences in its frequency between Ashkenazi and Sephardi Jews. Genes Immun. 1 (2000) 358-361
78. Magierowska M., Lepage V., Boubnova L., Carcassi C., de Juan D., Djoulah S., El Chenawi F., Grunnet N., Halle L., Ivanova R., Jungerman M., Naumova E., Petrany G., Sonnerborg A., Stavropoulos C., Thorsby E., Vu-Trieu A., Debre P., Theodorou I., and Charron D. Distribution of the CCR5 gene 32 base pair deletion and SDF1-3′A variant in healthy individuals from different populations. Immunogenetics 48 (1998) 417-419
79. Manzano C., de la Rua C., Iriondo M., Mazon L.I., Vicario A., and Aguirre A. Structuring the genetic heterogeneity of the Basque population: a view from classical polymorphisms. Hum. Biol. 74 (2002) 51-74
80. Martinson J.J., Chapman N.H., Rees D.C., Liu Y.T., and Clegg J.B. Global distribution of the CCR5 gene 32-base pair deletion. Nat. Genet. 16 (1997) 100-102
81. Martinson J.J., Hong L., Karanicolas R., Moore J.P., and Kostrikis L.G. Global distribution of the CCR2-64I/CCR5-59653T HIV-1 disease-protective haplotype. AIDS 14 (2000) 483-489
82. McMichael A.J. Environmental and social influences on emerging infectious diseases: past, present and future. Philos. Trans. R. Soc. Lond. B Biol. Sci. 359 (2004) 1049-1058
83. McNeill W.H. Plagues and People (1976), Anchor Books, New York 365 pp.
84. McNicholl J.M., Smith D.K., Qari S.H., and Hodge T. Host genes and HIV: the role of the chemokine receptor gene CCR5 and its allele. Emerg. Infect. Dis. 3 (1997) 261-271
85. Mecsas J., Franklin G., Kuziel W.A., Brubaker R.R., Falkow S., and Mosier D.E. Evolutionary genetics: CCR5 mutation and plague protection. Nature 427 (2004) 606
86. Michael N.L., Chang G., Louie L.G., Mascola J.R., Dondero D., Birx D.L., and Sheppard H.W. The role of viral phenotype and CCR-5 gene defects in HIV-1 transmission and disease progression. Nat. Med. 3 (1997) 338-340
87. Milman N., and Pedersen P. Evidence that the Cys282Tyr mutation of the HFE gene originated from a population in Southern Scandinavia and spread with the Vikings. Clin. Genet. 64 (2003) 36-47
88. Morkot, R., 1999. Atlas de la Grèce antique, 6500 à 30 av. J.-C. Éditions Autrement, Paris, 144 pp.
89. Novembre J., Galvani A.P., and Slatkin M. The geographic spread of the CCR5 Delta32 HIV-resistance allele. PLoS Biol. 3 (2005) e339
90. Noymer A. Contesting the cause and severity of the black death: a review essay. Popul. Dev. Rev. 33 (2007) 616-627
91. Otaegui D., Ruíz-Martínez J., Olaskoaga J., Emparanza J.I., and de Munain A.L. Influence of CCR5-Delta32 genotype in Spanish population with multiple sclerosis. Neurogenetics 8 (2007) 201-205
92. Papa A., Papadimitriou E., Adwan G., Clewley J.P., Malissiovas N., Ntoutsos I., Alexiou S., and Antoniadis A. HIV-1 co-receptor CCR5 and CCR2 mutations among Greeks. FEMS Immunol. Med. Microbiol. 28 (2000) 87-89
93. Paxton W.A., Martin S.R., Tse D., O'Brien T.R., Skurnick J., VanDevanter N.L., Padian N., Braun J.F., Kotler D.P., Wolinsky S.M., and Koup R.A. Relative resistance to HIV-1 infection of CD4 lymphocytes from persons who remain uninfected despite multiple high-risk sexual exposure. Nat. Med. 2 (1996) 412-417
94. Petrek M., Cermáková Z., Hutyrová B., Miceková D., Drábek J., Rovensky J., and Bosák V. CC chemokine receptor 5 and interleukin-1 receptor antagonist gene polymorphisms in patients with primary Sjogren's syndrome. Clin. Exp. Rheumatol. 20 (2002) 701-703
95. Piras I.S., Vacca L., Calò C.M., Falchi A., Ghiani M.E., Varesi L., and Vona G. Distribuzione delle varianti Δ32 e 64I dei geni per il CCR5 e il CCR2 in alcune popolazioni del Mediterraneo. Antropo 9 (2005) 29-39
96. Poljak M., Tomažic J., Seme K., Maticic M., and Vidmar L. Prevalence of mutant CCR5 allele in Slovenian HIV-1-infected and non-infected individuals. Acta Virol. 42 (1998) 23-26
97. Prahalad S. Negative association between the chemokine receptor CCR5-Delta32 polymorphism and rheumatoid arthritis: a meta-analysis. Genes Immun. 7 (2006) 264-268
98. Ristić S., Starcević-Cizmarević N., Brajenović-Milić B., Crnić-Martinović M., and Kapović M. Frequency of CCR5 gene 32-basepair deletion in Croatian normal population. Croat. Med. J. 46 (2005) 693-694
99. Romano-Spica V., Ianni A., Arzani D., Cattarini L., Majore S., and Dean M. Allelic distribution of CCR5 and CCR2 genes in an Italian population sample. AIDS Res. Hum. Retroviruses 16 (2000) 99-101
100. Ruiz A., Royo J.L., Rubio A., Borrego S., Leal M., Sánchez B., Nuñez-Roldán A., and Antiñolo G. Spectrofluorimetric analysis of CCR5-delta 32 allele using real-time polymerase chain reaction: prevalence in southern Spanish HIV(+) patients and noninfected population. AIDS Res. Hum. Retroviruses 17 (2001) 191-193
101. Sabeti P.C., Walsh E., Schaffner S.F., Varilly P., Fry B., Hutcheson H.B., Cullen M., Mikkelsen T.S., Roy J., Patterson N., Cooper R., Reich D., Altshuler D., O'Brien S., and Lander E.S. The case for selection at CCR5-Δ32. PLoS Biol. 3 (2005) e378
102. Saftić V., Rudan D., and Zgaga L. Mendelian diseases and conditions in Croatian island populations: historic records and new insights. Croat. Med. J. 47 (2006) 543-552
103. Salem A.H., and Batzer M.A. Distribution of the HIV resistance CCR5-Delta32 allele among Egyptians and Syrians. Mutat. Res. 616 (2007) 175-180
104. Sallares R., and Gomzi S. Biomolecular archaeology of malaria. Ancient Biomol. 3 (2001) 195-213
105. Samson M., Libert F., Doranz B.J., Rucker J., Liesnard C., Farber C.M., Saragosti S., Lapoumeroulie C., Cognaux J., Forceille C., Muyldermans G., Verhofstede C., Burtonboy G., Georges M., Imai T., Rana S., Yi Y., Smyth R.J., Collman R.G., Doms R.W., Vassart G., and Parmentier M. Resistance to HIV-1 infection in caucasian individuals bearing mutant alleles of the CCR-5 chemokine receptor gene. Nature 382 (1996) 722-725
106. Scarre, C., 1995. Atlas de la Rome antique, 800 av. J.-C. - 540 ap. J.-C. De la naissance de la République à la chute de l'Empire. Éditions Autrement, Paris, 144 pp.
107. Schliekelman P., Garner C., and Slatkin M. Natural selection and resistance to HIV. Nature 411 (2001) 545-546
108. Scott S., and Duncan C.J. Biology of Plagues: Evidence from Historical Populations (2001), Cambridge University Press, Cambridge 434 pp.
109. Scott S., and Duncan C.J. Return of the Black Death: The World's Greatest Serial Killer (2004), Wiley, J. and Sons, New York 318 pp.
110. Shumway R.H., and Stoffer D.S. Time Series Analysis and its Applications (1999), Springer-Verlag, New York
111. Sidoti A., D'Angelo R., Rinaldi C., De Luca G., Pino F., Salpietro C., Giunta D.E., Saltalamacchia F., and Amato A. Distribution of the mutated Δ32 allele of the CCR5 gene in a Sicilian population. Int. J. Immunogenet. 32 (2005) 193-198
112. Slatkin M. Simulating genealogies of selected alleles in a population of variable size. Genet. Res. 78 (2001) 49-57
113. Slominsky P.A., Shadrina M.I., Spitsyn V.A., Mikulich A.I., Khusnutdinova E.K., and Limborska S.A. A simple and rapid method for determining a 32-bp deletion in the gene for the chemokine receptor CCR5. Russian J. Genet. 33 (1997) 1596-1598
114. Smoljanović M., Ristic S., and Hayward C. Historic exposure to plague and present-day frequency of CCR5del32 in two isolated island communities of Dalmatia, Croatia. Croat. Med. J. 47 (2006) 579-584
115. Sonoda S., Li H.C., Cartier L., Nunez L., and Tajima K. Ancient HTLV type 1 provirus DNA of Andean mummy. AIDS Res. Hum. Retroviruses 16 (2000) 1753-1756
116. Stephens J.C., Reich D.E., Goldstein D.B., Shin H.D., Smith M.W., Carrington M., Winkler C., Huttley G., Allikmets R., Schriml L., Gerrard B., Malasky M., Ramos M.D., Morlo t.S., Tzetis M., Oddoux C., Giovine F.S., Nasioulas G., Chandler D., Aseev M., Hanson M., Kalaydjieva L., Glavac D., Gasparini P., Kanavakis E., Claustres M., Kambouris M., Ostrer H., Duff G., Baranov V., Sibul H., Metspalu A., Goldman D., Martin N., Duffy D., Schmidtke J., Estivill X., O'Brien S.J., and Dean M. Dating the origin of the CCR5-Δ32 AIDS-resistance allele by the coalescence of haplotypes. Am. J. Hum. Genet. 62 (1998) 1507-1515
117. Struyf F., Thoelen I., Charlier N., Keyaerts E., Van der Donck I., Wuu J., and Van Ranst M. Prevalence of CCR5 and CCR2 HIV-coreceptor gene polymorphisms in Belgium. Hum. Hered. 50 (2000) 304-307
118. Stumpf M.P., and Wilkinson-Herbots H.M. Allelic histories: positive selection on a HIV-resistance allele. Trends Ecol. Evol. 19 (2004) 166-168
119. Su B., Sun G., Lu D., Xiao J., Hu F., Chakraborty R., Deka R., and Jin L. Distribution of three HIV-1 resistance-conferring polymorphisms (SDF1-3′A, CCR2-64I, and CCR5-delta32) in global populations. Eur. J. Hum. Genet. 8 (2000) 975-979
120. Szalai C., Császár A., Czinner A., Szabó T., and Falus A. High. frequency of the CCR5 deletion allele in Gypsies living in Hungary. Immunol. Lett. 63 (1998) 57-58
121. Talbert R.J.A. Atlas of Classical History (1988), Crom Helm, Londres 217 pp.
122. Talbert R.J.A. Barrington Atlas of the Greek and Roman World. 3 vol. and one CD-ROM (2000), Princeton University Press, Princeton 1772 pp.
123. Theilmann J.M., and Cate F. A plague of plagues: the problem of plague diagnosis in Medieval England. J. Interdiscipl. Hist. 37 (2007) 371-393
124. Vitart V., Biloglav Z., Hayward C., Janicijevic B., Smolej-Narancic N., Barac L., Pericic M., Klaric I.M., Skaric-Juric T., Barbalic M., Polasek O., Kolcic I., Carothers A., Rudan P., Hastie N., Wright A., Campbell H., and Rudan I. 3000 years of solitude: extreme differentiation in the island isolates of Dalmatia, Croatia. Eur. J. Hum. Genet. 14 (2006) 478-487
125. Voevodin A., Samilchuk E., and Dashti S. Frequencies of SDF-1 chemokine, CCR-5, and CCR-2 chemokine receptor gene alleles conferring resistance to human immunodeficiency virus type 1 and AIDS in Kuwaitis. J. Med. Virol. 58 (1999) 54-58
126. Walker J.K., Ahumada A., Frank B., Gaspard R., Berman K., Quackenbush J., and Schwartz D.A. Multistrain genetic comparisons reveal CCR5 as a receptor involved in airway hyperresponsiveness. Am. J. Respir. Cell. Mol. Biol. 34 (2006) 711-718
127. Wang X., Grus W.E., and Zhang J. Gene losses during human origins. PLoS Biol. 4 (2006) e52
128. Watterson G.A., and Guess H.A. Is the most frequent allele the oldest?. Theor. Popul. Biol. 11 (1997) 141-160
129. Willis M.F., and Warburton M.F. Measles susceptibility in two Pacific atoll populations. Epidemiological factors and response to live attenuated measles virus. Med. J. Aust. 1 (1974) 789-793
130. Witas H.W., and Zawicki P. Allele protecting against HIV (CCR5-Δ32) identified in early medieval specimens from Central Poland. Preliminary results. Prz. Antropol. Anthropol. Rev. 69 (2006) 49-53
131. Youngkin C.K., Nunemaker M.E., Battey L.L., and Glenn C.A. Measles epidemic on Guam. US Nav. Med. Bull. 49 (1949) 950-955
132. Zamarchi R., Indraccolo S., Minuzzo S., Coppola V., Gringeri A., Santagostino E., Vicenzi E., De Silvestro G., Biagiotti R., Baldassarre C., Chieco-Bianchi L., and Amadori A. Frequency of a mutated CCR-5 allele (delta32) among Italian healthy donors and individuals at risk of parenteral HIV infection. AIDS Res. Hum. Retroviruses 15 (1999) 337-344
133. Zawicki P., and Witas H.W. HIV-1 protecting CCR5-Delta32 allele in medieval Poland. Infect. Genet. Evol. 8 (2008) 146-151
134. Zimmerman P.A., Buckler-White A., Alkhatib G., Spalding T., Kubofcik J., Combadiere C., Weissman D., Cohen O., Rubbert A., Lam G., Vaccarezza M., Kennedy P.E., Kumaraswami V., Giorgi J.V., Detels R., Hunter J., Chopek M., Berger E.A., Fauci A.S., Nutman T.B., and Murphy P.M. Inherited resistance to HIV-1 conferred by an inactivating mutation in CC chemokine receptor 5: studies in populations with contrasting clinical phenotypes, defined racial background, and quantified risk. Mol. Med. J. 3 (1997) 23-36