sign in sign up
<<
Home , Ciudad Victoria, Monterrey, Nuevo Santander, Tamaulipas

Human Immunology xxx (xxxx) xxx–xxx

Contents lists available at ScienceDirect

Human Immunology

journal homepage: www.elsevier.com/locate/humimm

Genetic diversity of HLA system in two from , : and rural Tamaulipas ⁎ Tirzo Jesús Rodríguez-Munguíaa,1, Rodrigo Barquerab,c, ,1, Carmen Adalid-Sáinzd,1, Diana Iraíz Hernández-Zaragozac,e,1, Esteban Arrieta-Bolañosf,1, Stephen Claytonb,1, Guadalupe Aquino-Rubioa, Marisela del Rocío González-Martínezg, Hanna Pacheco-Ubaldoc, Liliana González-Medinac, Abraham Lona-Sánchezc, Alicia Bravo-Acevedoh, Héctor Delgado-Aguirred, Néstor Escareño-Montieli, Yolanda Jaramillo-Rodríguezj, Antonio Salgado-Adamej, Federico Juárez-de la Cruzi, Joaquín Zúñigak,l, Edmond J. Yunism, ⁎ Carolina Bekker-Méndezn, Julio Granadoso, a Molecular Biology , Hospital General “Norberto Treviño Zapata”, Dirección de Servicios de Salud de Tamaulipas, Ciudad Victoria, Tamaulipas, Mexico b Department of Archaeogenetics, Max Planck Institute for the of Human History (MPI-SHH), Jena, Germany c Molecular Genetics Laboratory, Escuela Nacional de Antropología e Historia (ENAH), , Mexico d Laboratory of Histocompatibility, Unidad Médica de Alta Especialidad (UMAE) # 71, Instituto Mexicano del Seguro Social (IMSS), Torreón, , Mexico e Immunogenetics Unit, Técnicas Genéticas Aplicadas a la Clínica (TGAC), Mexico City, Mexico f Institute for Experimental Cellular Therapy, Hospital Essen, Essen, Germany g Microbiology Department, Faculty of Medicine, Universidad Autónoma de Coahuila, Torreón, Coahuila, Mexico h Blood Bank, UMAE Hospital de Gineco Obstetricia No. 4 “Luis Castelazo Ayala”, Instituto Mexicano del Seguro Social (IMSS), Mexico City, Mexico i Department of Transplantation, Unidad Médica de Alta Especialidad (UMAE) # 71, Instituto Mexicano del Seguro Social (IMSS), Torreón, Coahuila, Mexico j Direction of and , Unidad Médica de Alta Especialidad (UMAE) # 71, Instituto Mexicano del Seguro Social (IMSS), Torreón, Coahuila, Mexico k Laboratory of Immunobiology and Genetics, Instituto Nacional de Enfermedades Respiratorias Ismael Cosío Villegas, Mexico City, Mexico l Tecnologico de , Escuela de Medicina y Ciencias de la Salud, Mexico City, Mexico m Department of Cancer Immunology and Virology, Dana-Farber Cancer Institute, Boston, MA, USA n Immunology and Infectology Research Unit, Infectology Hospital, Centro Médico Nacional “La Raza”, Instituto Mexicano del Seguro Social (IMSS), Mexico City, Mexico o Department of Transplantation, Instituto Nacional de Ciencias Médicas y Nutrición “Salvador Zubirán” (INCMNSZ), Mexico City, Mexico

ARTICLE INFO ABSTRACT

Keywords: We studied HLA class I (HLA-A, -B) and class II (HLA-DRB1, -DQB1) alleles by PCR-SSP based typing in 148 HLA from the state of Tamaulipas living in Ciudad Victoria (N = 23) and rural communities (N = 125), to Immunogenetics obtain information regarding allelic and haplotypic frequencies. We found that the most frequent haplotypes in genetics the state of Tamaulipas include ten Native American, three European and one African haplotypes. Admixture Tamaulipas estimates revealed that the main genetic components in the state of Tamaulipas are Native American Admixture (54.69 ± 0.93% by ML; 47.65% of Native American haplotypes) and European (34.66 ± 5.62% by ML; 33.56% of European haplotypes), and a relatively high African genetic component (10.65 ± 5.05% by ML; 12.42% of African haplotypes).

Located in the Gulf Coast lowlands, the state of Tamaulipas borders and to the west with and the state of Nuevo León [1,2]. As of 2015, to the north with the of America; to the east with the Gulf Tamaulipas has a population of 3 441 698 inhabitants, which represents of Mexico; to the south with the states of and San Luis Potosí, 2.9% of the population of Mexico. In Tamaulipas one of every 100

Abbreviations: HLA, human leukocyte antigen; MPA, most-probable ancestry; LD, linkage disequilibrium ⁎ Corresponding authors at: Department of Archaeogenetics, Max Planck Institute for the Science of Human History, Kahlaische Strasse 10, 07745 Jena, Germany (R. Barquera). Department of Transplantation, Instituto Nacional de Ciencias Médicas y Nutrición “Salvador Zubirán” (INCMNSZ), Vasco de Quiroga 15, Belisario Domínguez Sección XVI, 14080 Tlalpan, CDMX, Mexico (J. Granados). E-mail addresses: [email protected] (R. Barquera), [email protected] (J. Granados). URLs: http://www.shh.mpg.de/en (R. Barquera), http://www.innsz.mx (J. Granados). 1 These authors contributed equally to the present work. https://doi.org/10.1016/j.humimm.2019.07.288 Received 8 July 2019; Accepted 13 July 2019 0198-8859/ © 2019 American Society for Histocompatibility and Immunogenetics. Published by Elsevier Inc. All rights reserved.

Please cite this article as: Tirzo Jesús Rodríguez-Munguía, et al., Human Immunology, https://doi.org/10.1016/j.humimm.2019.07.288 T.J. Rodríguez-Munguía, et al. Human Immunology xxx (xxxx) xxx–xxx

Fig. 1. Location of Tamaulipas and admixture proportions for the state of Tamaulipas [composed by the following populations: Mexico Tamaulipas, Ciudad Victoria, N = 23, Allele Frequencies Net Database Identifier (AFND-ID): 3489; Mexico Tamaulipas Rural, N = 125, AFND-ID: 3585]. Admixture proportions were estimatedby ML using HLA-A, -B and -DRB1 frequencies as genetic estimators. Green refers to the proportion of European contribution, purple to Native American contribution and yellow depicts African contribution. Map modified from Google Maps Pro [17]. inhabitants of 3 years and over is a speaker of an indigenous language. II (HLA-DRB1, -DQB1) PCR-SSP based typings in 148 Mexicans from the The most common indigenous languages in the state are: Nahuatl state of Tamaulipas [composed by the following populations: Mexico (46.7%) and Huastec (19.5%). About 6.3% of the population of the Tamaulipas, Ciudad Victoria, N = 23, Allele Frequencies Net Database state considers themselves indigenous and 0.3% as Afro-descendant Identifier (AFND-ID): 3489; Mexico Tamaulipas Rural, N = 125, AFND- [1,3]. ID: 3585]. In addition to the individual populations we also show data According to the archaeological data, the presence of sedentary for these combined populations. The latter are not held on AFND to groups in the northern part of the region (like the one found prevent duplication of data. Maximum-likelihood (ML) frequencies for in Lomas del Real located in Altamira, Tamaulipas) during the pre- alleles and four-locus haplotypes were estimated using an Expectation- Columbian era goes back to 1700–1400 BCE (Formative period), when Maximization algorithm. For a comprehensive review on the methods, the first micro-villages of farmers were established that complemented such as sample collection, HLA typing and statistical analyses, please their diet with hunting, fishing and gathering through the exploitation refer to [9] in this same issue. For the frequencies of HLA-A, -B, -DRB1 of marine, lacustrine and riparian resources [4]. The Pre Classic period and -DQB1 and haplotypic data for the sample sets of the state of Ta- in Tamaulipas is important as it yields, together with Tehuacán maulipas, please refer to the Supplementary Information: (), the first evidence of domesticated plants that would become Supplementary Tables 1–7. For data on Hardy-Weinberg equilibrium the basis of Mesoamerican diet from that moment until present times (HWE) please see Supplementary Information: Supplementary Table 8: [2,5]. At the time of contact with , about 25 000–115 000 of this work and Supplementary Information: Supplementary Table 9 in Native Americans lived in northern Tamaulipas and probably even [9] in this same issue. We found that the most frequent haplotypes for more Huastecs in the southern part of the state. By the mid-eighteenth the state (haplotypic frequency, H.F. > 1.0%, arbitrarily; century, the Native American population has been estimated to be only Supplementary Table 5) include eight Native American (HLA ~ 2500 individuals [6]. A*68 ~ B*48 ~ DRB1*04 ~ DQB1*03:02, A*02 ~ B*35 ~ DRB1*04 ~ During the 18th century Franciscan monks followed José de DQB1*03:02, A*02 ~ B*40:02 ~ DRB1*04 ~ DQB1*03:02, A*24 ~ Escandón’s military expedition, which led to the conquest of B*40:02 ~ DRB1*04 ~ DQB1*03:02, A*02 ~ B*15:01 ~ DRB1*04 ~ Tamaulipas, the last area of the northeast to come under Spanish con- DQB1*03:02, A*02 ~ B*51 ~ DRB1*04 ~ DQB1*03:02, A*68 ~ trol [6]. The first Spanish permanent settlement in the area wasTam- B*35 ~ DRB1*04 ~ DQB1*03:02 and A*68 ~ B*40:02 ~ DRB1*04 ~ pico in 1554. What is now Tamaulipas was incorporated as a province DQB1*03:02), two European (HLA ~ A*29 ~ B*44 ~ DRB1*07 ~ of New in 1746 with the name of . Once the DQB1*02 and A*24 ~ B*35 ~ DRB1*03:01 ~ DQB1*02), and one Spanish Crown in Mexico had been defeated, Tamaulipas African (HLA ~ A*30 ~ B*53 ~ DRB1*13 ~ DQB1*06) haplotypes. Ad- became one of the 19 founding states of the United Mexican States. mixture estimates (Fig. 1) revealed that the main genetic components in During the 20th century, the main migratory influx to the state came the state of Tamaulipas are Native American (54.69 ± 0.93% by the from the neighboring states of San Luis Potosí and Veracruz which, ML method and 47.65% by estimating the proportion of Native Amer- together with the development of and industrial complexes, ican haplotypes) and European (34.66 ± 5.62% by the ML method and led to a 10-fold growth of the population of the state, going from ap- 33.56% by estimating the proportion of European haplotypes), and a proximately 200 000 in the 1900′s to over two million by the end of the relatively high African genetic component (10.65 ± 5.05% by the ML century [7]. Given the combined effect of the development of industry method and 12.42% by estimating the proportion of African haplo- in the state and its condition of being a state bordering with the United types). Admixture proportions using genome-wide approaches (an- States, Tamaulipas has traditionally been an immigration attractor, cestry-informative markers (AIMs) for the northeastern region of even for foreign population, with a vast majority of it being born in the Mexico [10] and single nucleotide polymorphisms (SNPs) for the state USA [8]. of Tamaulipas [11]) from previous reports show similar results with the For the present work, we analyzed HLA class I (HLA-A, -B) and class Native American component as the most prominent one (56% AIMs,

2 T.J. Rodríguez-Munguía, et al. Human Immunology xxx (xxxx) xxx–xxx

52.54% SNPs), followed by European ancestry (38% AIMs, 42.77% doi.org/10.1016/j.humimm.2019.07.288. SNPs) and a modest African contribution (6% AIMs, 4.69% SNPs). However, a higher proportion of African ancestry (15.4%) has been References previously reported for Tamaulipas using Y-chromosome SNPs [12], showing the asymmetric contribution of African genetic components [1] Instituto Nacional de Estadística y Geografía (INEGI), Conociendo Tamaulipas, sixth into the region. The relatively high African proportion found in the ed., Instituto Nacional de Estadística y Geografía, Mexico, 2016. [2] R.A. Diehl, The precolumbian of the gulf coast, in: R.E.W. Adams, state could be explained partly because of the recent immigration from M.J. Madeod (Eds.), The Cambridge History of the Native Peoples of the Americas, Veracruz (a state with a relatively high proportion of African ancestry) Vol. II, Cambridge University Press, Cambridge, 2008, pp. 156–196. and its closeness to the ports and settlements where African enslaved [3] INEGI (instituto Nacional de Estadistica y Geografia), Perfil sociodemográfico dela población afrodescendiente en México, INEGI (instituto Nacional de Estadistica y individuals were brought into the during the Colonial period Geografia), Mexico City, 2017. [13], but also due to the fact that during the 19th century, northeastern [4] J.E. Velasco González, G.A. Ramírez Castilla, C. Serrano-Sánchez, Bioarqueología Mexico became a destination for fugitive slaves and African American en la cuenca baja del Río Pánuco. Estudio de restos óseos en Altamira, Tamaulipas, freemen migrating from the and [14]. The Anales de Antropología 45 (2011) 51–78. [5] R.N. Zeitlin, J.F. Zeitlin, The paleoindian and archaic cultures of Mesoamerica, in: differences between the estimation of the African component couldbe R.E.W. Adams, M.J. MacLeod (Eds.), The Cambridge History of the Native Peoples due to differences in the admixture estimation methods (three lociof of the Americas, Vol. II, Mesoamerica Cambridge University Press, Cambridge, HLA vs. whole genome SNP data and uniparental markers), or differ- 2008, pp. 45–121. [6] D. Frye, The Native Peoples of northeastern Mexico, in: R.E.W. Adams, ences in local genomic ancestry: there is an apparent increase in African M.J. MacLeod (Eds.), The Cambridge History of the Native Peoples of the Americas, ancestry in Latin American mixed ancestry populations that could be Vol. II, Mesoamerica Cambridge University Press, Cambridge, 2008, pp. 89–135. due to selection of such variants after the conquest and during the co- [7] J. Sobrino, Migración interna en México durante el siglo XX, 1st Ed., Consejo Nacional de Población, Mexico City, 2010. lonial period (discussed in [9] in this issue). [8] INEGI, Los extranjeros en México, Mexico City, 2014. doi:10.1016/0306-4522(87) For Ciudad Victoria, the main genetic components are Native 92980-0. American (47.22 ± 8.34% by the ML method and 30.44% by esti- [9] R. Barquera, D.I. Hernández Zaragoza, A. Bravo Acevedo, E. Arrieta Bolaños, S. Clayton, V. Acuña Alonzo, et al., The immunogenetic diversity of the HLA system mating the proportion of Native American haplotypes) and European in Mexico correlates with underlying population genetic structure, Hum. Immunol. (36.70 ± 7.90% by the ML method and 41.30% by estimating the (2019). proportion of European haplotypes), and a very prominent African [10] M.L. Martinez-Fierro, J. Beuten, R.J. Leach, E.J. Parra, M. Cruz-Lopez, H. Rangel- Villalobos, et al., Ancestry informative markers and admixture proportions in genetic component (16.08 ± 3.51% by the ML method and 19.57% by northeastern Mexico, J. Hum. Genet. 54 (2009) 504–509, https://doi.org/10.1038/ estimating the proportion of African haplotypes), although due to the jhg.2009.65. sample size these results may be biased. The rural areas follow a similar [11] A. Moreno-Estrada, C.R. Gignoux, J.C. Fernández-López, F. Zakharia, M. Sikora, pattern with the main genetic components being Native American A.V. Contreras, et al., The genetics of Mexico recapitulates Native American sub- structure and affects biomedical traits, Science 344 (2014) 1280–1285, https://doi. (56.16 ± 2.14% by the ML method and 50.80% by estimating the org/10.1126/science.1251688. proportion of Native American haplotypes) and European [12] B.Z. González-Sobrino, A.P. Pintado-Cortina, L. Sebastián-Medina, F. Morales- (34.26 ± 8.12% by the ML method and 32.14% by estimating the Mandujano, A.V. Contreras, Y.E. Aguilar, et al., Genetic diversity and differentiation in urban and indigenous populations of Mexico: patterns of mitochondrial DNA and proportion of European haplotypes), and an important African genetic Y-chromosome lineages, Biodemography Social Biol. 62 (2016) 53–72, https://doi. contribution (9.58 ± 6.20% by the ML method and 11.11% by esti- org/10.1080/19485565.2015.1117938. mating the proportion of African haplotypes), although not as high as [13] G. Aguirre Beltrán, La población negra en México: Estudio etnohistórico, second ed., Fondo de Cultura Económica (FCE), Mexico City, 1972. the one for Ciudad Victoria. The proportion of Asian haplotypes re- [14] J.C. Gassner, African American fugitive slaves and freemen in Matamoros, mains relatively constant (state of Tamaulipas 4.03%, Ciudad Victoria Tamaulipas, 1820–1865, The University of Texas – Pan American (2004). 6.52%, and the rural areas 3.57%). This Asian genetic presence can be [15] J.J. Gómez Izquierdo, El movimiento antichino en México (1871-1934) : problemas del racismo y del nacionalismo durante la Revolución Mexicana, Instituto Nacional explained by the important presence of Asian (mainly Chinese) im- de Antropología e Historia, Mexico City, 1992. migrants settling there by the end of the 19th century and the beginning [16] E.J.M. dos Santos, A. McCabe, F.F. Gonzalez-Galarza, A.R. Jones, D. Middleton, of the 20th century [15]. All data from our sample sets, both fre- Allele Frequencies Net Database: Improvements for storage of individual genotypes and analysis of existing data, Hum. Immunol. 77 (2016) 238–248, https://doi.org/ quencies and individual genotypes, can be found at The Allele Fre- 10.1016/j.humimm.2015.11.013. quency Net Database website (www.allelefrequencies.net) [16]. [17] Google, Google Earth Pro ©, (2019). earth.google.com.

Appendix A. Supplementary data

Supplementary data to this article can be found online at https://

3