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Genetic diversity of HLA system in three populations from Guanajuato, Mexico: Guanajuato City, León and rural Guanajuato
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 three populations from Guanajuato, Mexico: Guanajuato City, León and rural Guanajuato Jorge Arturo Pantoja-Torresa,1, Rodrigo Barquerab,c,1, , Mónica Ballesteros-Romeroc,1, Alicia Bravo-Acevedod,1, Esteban Arrieta-Bolañose,1, Gustavo Daniel Montiel-Hernándezf,1, Stephen Claytonc,1, Lidia Iris Rodríguez-Rodríguezg,1, Diana Iraíz Hernández-Zaragozac,h, Isis Goné-Vázquezi, Araceli Escobedo-Ruízi, Víctor Eduardo García-Ariasj, Francia Paulina Arellano-Pradoj, Marla Estefanía Rodríguez-Lópezj, María Guadalupe de Jesús Sánchez-Fernándezk, Mario J. Sandoval-Sandovall, Benjamín Gómez-Navarrom, Joaquín Zúñigan,o, Edmond J. Yunisp, Carolina Bekker-Méndezq, ⁎ Julio Granadosr, ⁎
a
Immunology Division, Unidad Médica de Alta Especialidad (UMAE) # 1, Instituto Mexicano del Seguro Social (IMSS), León, Guanajuato, Mexico Department of Archaeogenetics, Max Planck Institute for the Science of Human History (MPI-SHH), Jena, Germany Molecular Genetics Laboratory, Escuela Nacional de Antropología e Historia (ENAH), Mexico City, Mexico d Blood Bank, Unidad Médica de Alta Especialidad (UMAE) Hospital de Gineco Obstetricia No. 4 “Luis Castelazo Ayala”, Instituto Mexicano del Seguro Social (IMSS), Mexico City, Mexico e Institute for Experimental Cellular Therapy, University Hospital Essen, Essen, Germany f Escuela Nacional de Antropología e Historia (ENAH), Mexico City, Mexico g Archaeology Section, Centro INAH Guanajuato, Instituto Nacional de Antropología e Historia (INAH), Guanajuato, Guanajuato, Mexico h Immunogenetics Unit, Técnicas Genéticas Aplicadas a la Clínica (TGAC), Mexico City, Mexico i Histocompatibility Laboratory, Hospital de Especialidades, Centro Médico Nacional de Occidente (CMNO), Instituto Mexicano del Seguro Social (IMSS), Guadalajara, Jalisco, Mexico j Pediatrics Hospital, Centro Médico Nacional de Occidente (CMNO), Instituto Mexicano del Seguro Social (IMSS), Guadalajara, Jalisco, Mexico k Department of Nephrology and Transplantation Unit, Centro Médico Nacional de Occidente (CMNO), Instituto Mexicano del Seguro Social (IMSS), Guadalajara, Jalisco, Mexico l Central Office of Transplantation, Centro Médico Nacional de Occidente (CMNO), Instituto Mexicano del Seguro Social (IMSS), Guadalajara, Jalisco, Mexico m Central Office of Nephrology, Centro Médico Nacional de Occidente (CMNO), Instituto Mexicano del Seguro Social (IMSS), Guadalajara, Jalisco, Mexico n Laboratory of Immunobiology and Genetics, Instituto Nacional de Enfermedades Respiratorias Ismael Cosío Villegas, Mexico City, Mexico o Tecnologico de Monterrey, Escuela de Medicina y Ciencias de la Salud, Mexico City, Mexico p Department of Cancer Immunology and Virology, Dana-Farber Cancer Institute, Boston, MA, USA q Immunology and Infectology Research Unit, Infectology Hospital, Centro Médico Nacional “La Raza”, Instituto Mexicano del Seguro Social (IMSS), Mexico City, Mexico r Department of Transplantation, Instituto Nacional de Ciencias Médicas y Nutrición “Salvador Zubirán” (INCMNSZ), Mexico City, Mexico b c
ARTICLE INFO
ABSTRACT
Keywords: HLA Immunogenetics Population genetics Guanajuato Admixture
We studied HLA class I (HLA-A, -B) and class II (HLA-DRB1, -DQB1) alleles by PCR-SSP based typing in 262 Mexicans from the state of Guanajuato living in the cities of Guanajuato (N = 78), León (N = 22) and rural communities (N = 162), to obtain information regarding allelic and haplotypic frequencies. We find that the most frequent haplotypes found in the state of Guanajuato include 12 Native American and three European haplotypes. Admixture estimates revealed that the main genetic components in the state of Guanajuato are Native American (50.64 ± 2.11% by ML, 43.35% of Native American haplotypes) and European (44.14 ± 1.14% by ML; 39.35% of European haplotypes), while African genetic component is less apparent (5.22 ± 2.08% by ML; 8.36% of African haplotypes).
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 (MPI-SHH), 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.2019.06.002 Received 3 June 2019; Accepted 6 June 2019 0198-8859/ © 2019 American Society for Histocompatibility and Immunogenetics. Published by Elsevier Inc. All rights reserved.
Please cite this article as: Jorge Arturo Pantoja-Torres, et al., Human Immunology, https://doi.org/10.1016/j.humimm.2019.06.002
Human Immunology xxx (xxxx) xxx–xxx
J.A. Pantoja-Torres, et al.
The state of Guanajuato is located in the Central region of Mexico, and is part of the western zone, bordered to the west by the state of Jalisco, to the northwest by Zacatecas, to the east by Querétaro and to the south by Michoacán. It is divided internally into three major geographical regions: the Northern region, the Bajío and the Southern region [1]. The zone of plains that extend along the rivers that feed the Lerma and that go into Querétaro and Jalisco is known as the Bajío area, a prosperous region that is dedicated to agriculture [2]. The orography of Guanajuato is determined by the Sierra Madre Occidental, the Transversal Volcanic Axis and the Sierra Madre del Sur, as well as the local mountain system. The Sierra de Guanajuato has been the center of the most important mining operations in the country since colonial times. Guanajuato’s location right in the center of the country brings it closer to its three most important cities (Mexico City, Guadalajara and Monterrey), plus the distance to both the northern and southern borders is roughly the same. The state of Guanajuato is one of the most populated in the country with a total of 5 853 677 people living there, in an area of 30 589 square kilometers, which represents 1.6% of the total area of the country, resulting in a population density of 191 inhabitants/Km2. The population is distributed in 46 municipalities of which 70% are localities considered urban, while 30% of the population lives in rural regions [3]. The capital of the state is the city of Guanajuato, although with 184 239 inhabitants it is not the most populated. León is the most populated city with 1 578 626 inhabitants, followed by the cities of Irapuato and Celaya. At least ten municipalities concentrate population numbering between 100 000 to 250 000 inhabitants, followed by 14 municipalities that have a population size between 50 000 and 100 000 inhabitants; and finally six municipalities with populations numbering between 25 000 and 50 000 inhabitants [4]. The current settlement pattern dates back to the Colonial period and revolved around economic activity, especially mining and agriculture. Speakers of indigenous languages are few: 3 239 Otomí speakers, followed by Chichimeca jonaz with 2 142 speakers, Náhuatl (1 246 speakers), and finally 818 speakers of Mazahua [3]. However, this pattern was different and fluctuating during the pre-Hispanic era. The history of Guanajuato is intimately linked to the history of the northern region of the country, western Mexico and the Valley of Mexico basin. During the pre-Hispanic era it constituted the border zone between Mesoamerica and the northern region, a fluctuating frontier that allowed the interchange between these two regions [1]. Data on early human occupation of the current state of Guanajuato are scarce and resemble that of lithic age hunter-gatherer groups that have been found in other areas of the country. It is assumed that the transition of these small groups of hunter-gatherers to semi-sedentary
agricultural villages was a process similar to what happened in other areas of Mesoamerica. In the region of Guanajuato there is archaeological evidence of human occupation over three periods: settlement (represented by the Chupícuaro cultural tradition between 400 and 100 BCE [2]), a period of depopulation (abandonment of the important sedentary sites that occurred between 800 and 1300 AD), and finally a period of repopulation (event that began in the second half of the 14th century) [1]. Undoubtedly, the influence of the Chupícuaro cultural tradition on the diverse cultures of the West, as well as on the emergence of the great urban centers of the center and valley of Mexico was lasting and extensive, so that it is possible to find its characteristic ceramics in places such as Tula and Teotihuacán, as well as in Cuicuilco [5]. The lands north of the Lerma River were not always arid and these were populated by sedentary agricultural groups that founded complex urban centers with a notable Toltec and central Mesoamerica influence, but also of the large urban centers of northern Mexico. [1]. However, between the 10th and 11th centuries AD, the abandonment of this area gradually began, either because an abrupt climate change produced intense aridity that took agricultural peoples to abandon their settlements or due to the fall and collapse of Tula and Teotihuacán, leading to a massive population rearrangement during the Classic period [2]. The archaeological record accounts for an important historical moment: all the sites were abandoned and diverse nomadic groups (hunter-gatherers practicing agriculture at a small scale) arrived to the same regions. However, these groups had cultural features considered as Mesoamerican, built important centers, belonged to socially stratified societies and celebrated elaborate rites. During the late post Classic, in the last moments of Pre-Columbian America, the Tarascans were the hegemonic group. They formed an empire that extended its limits throughout the state and became the opposition to the dominant power of the Mexicas that established control in the central lands of the country [1,2]. With the conquest of Mexico-Tenochtitlan the Spanish began exploration and colonization of the territory called New Spain. One of the first explorations to the state of Guanajuato was lead by Nuño de Guzmán, but it was the religious orders, especially the Franciscans, who established the Indian villages, concentrating the dispersed population [1]. The need to control the rebel groups of the north (i.e. the Chichimeca) and the need to exploit the silver deposits and to make use of the lands for agriculture and settling cattle ranches led them to start a war against the indigenous groups of the north, which resulted in the annihilation and subjugation of most of the peoples living there [1,6]. Currently the state of Guanajuato maintains a remarkable population density, its economic sector continues to focus on mining and agriculture as main engines, although it also presents a considerable flow of national and international migration, especially to the USA, it is Fig. 1. Geographic situation of Guanajuato and admixture proportions for the state of Guanajuato [composed by the following populations: Mexico Guanajuato, Guanajuato city, N = 22, Allele Frequencies Net Database Identifier (AFND-ID): 3498; Mexico Guanajuato, León, N = 78, AFND-ID: 3497; Mexico Guanajuato Rural, N = 162, AFND-ID: 3581]. Admixture proportions were estimated by 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 [15].
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still an attractor of population from other areas of the country and from other countries [4,7]. For the present work, we analyzed HLA class I (HLA-A, -B) and class II (HLA-DRB1, -DQB1) PCR-SSP based typings in 262 Mexicans from the state of Guanajuato [composed by the following populations: Mexico Guanajuato, Guanajuato city, N = 22, Allele Frequencies Net Database Identifier (AFND-ID): 3498; Mexico Guanajuato, León, N = 78, AFNDID: 3497; Mexico Guanajuato Rural, N = 162, AFND-ID: 3581]. In addition to the individual populations we also show data for these combined populations. The latter are not held on AFND to prevent duplication of data. Maximum-likelihood (ML) frequencies for alleles and four-locus haplotypes were estimated using an ExpectationMaximization algorithm. For a comprehensive review on the methods, such as sample collection, HLA typing and statistical analyses, please refer to [8] in this same issue. For the frequencies of HLA-A, -B, -DRB1 and -DQB1 and haplotypic data for the sample sets of the state of Guanajuato please refer to the Supplementary Information: Supplementary Tables 1–8. For data on Hardy-Weinberg equilibrium (HWE) please see Supplementary Information: Supplementary Table 9 of this work and Supplementary Information: Supplementary Table 9 in [8] in this same issue. We find that the most frequent haplotypes for the state (haplotypic frequency, H.F. > 1.0%, arbitrarily; Supplementary Table 5) include 12 Native American (HLA ∼ A*02 ∼ B*35 ∼ DRB1*08 ∼ DQB1*04, A*02 ∼ B*39 ∼ DRB1*04 ∼ DQB1*03:02, A*68 ∼ B*39 ∼ DRB1*04 ∼ DQB1*03:02, A*24 ∼ B*39 ∼ DRB1*04 ∼ DQB1*03:02, A*24 ∼ B*35 ∼ DRB1*04 ∼ DQB1*03:02, A*02 ∼ B*35 ∼ DRB1*04 ∼ DQB1*03:02, A*02 ∼ B*39 ∼ DRB1*08 ∼ DQB1*04, A*02 ∼ B*15:01 ∼ DRB1*08 ∼ DQB1*04, A*31 ∼ B*35 ∼ DRB1*04 ∼ DQB1*03:02, A*31 ∼ B*35 ∼ DRB1*08 ∼ DQB1*04, A*68 ∼ B*39 ∼ DRB1*08 ∼ DQB1*04 and A*24 ∼ B*35 ∼ DRB1*16 ∼ DQB1*03:01) and three European (HLA ∼ A*29 ∼ B*44 ∼ DRB1*07 ∼ DQB1*02, A*01 ∼ B*08 ∼ DRB1*03:01 ∼ DQB1*02 and A*68 ∼ B*14:02 ∼ DRB1*01 ∼ DQB1*05) haplotypes. Admixture estimates (Fig. 1) revealed that the main genetic components in the state of Guanajuato are Native American (50.64 ± 2.11% by the ML method and 43.35% by estimating the proportion of Native American haplotypes) and European (44.14 ± 1.14% by the ML method and 39.35% by estimating the proportion of European haplotypes), while African genetic component is less apparent (5.22 ± 2.08% by the ML method and 8.36% by estimating the proportion of African haplotypes). Previous reports on admixture estimations for the state of Guanajuato using genome-wide SNP data show similar proportions of Native American (57.6% ± 9.6% [9]; 59.17% [10]) and European (39.9 ± 10.0% [9]; 36.78% [10]) ancestral contributions, with a less prominent African component (1.1 ± 1.8% [9]; 4.05% [10]). In line with previous reports [11], we find a higher contribution of African ancestry in rural areas when compared with urban settlements both by ML estimations [7.63 ± 0.54% vs. 0.00 ± 5.20% (Guanajuato) vs. 2.18 ± 5.26% (León), respectively] and by the proportion of African haplotypes present in the sample sets [9.51% vs. 6.81% (Guanajuato) vs. 6.41% (León), respectively]. However, the Native American component follows a different pattern with higher proportion of Native American ancestry in the cities than in the rural areas both by ML estimations [47.91 ± 1.58% vs. 75.23 ± 4.01% (Guanajuato) vs.
49.17 ± 3.84% (León), respectively] and by the proportion of Native American haplotypes present in the sample sets [41.72% vs. 56.82% (Guanajuato) vs. 42.95% (León), respectively]. The proportion of Asian haplotypes appears relatively constant in all sample sets analyzed (7.03% for the whole state, 6.81% for Guanajuato, 6.41% for León and 7.36% for the rural areas), which is slightly different to previous reports using genome-wide SNP data (1.3 ± 2.1% [9]). This component may be present due to the large numbers of Southeast Asians arriving via the Manila Galleon trade route and settling in the Central Region of the Vice-Royalty of New Spain during the first two centuries of the Colonial Period [12] but also with the East Asian migration events happening during the last part of the 19th century and the beginning of the 20th century [13]. All data from our sample sets, both frequencies and individual genotypes, can be found at The Allele Frequency Net Database website (www.allelefrequencies.netwww.allelefrequencies.net) [14]. Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.humimm.2019.06.002. References [1] M. Blanco, Alma Parra, Ethelia Ruiz Medrano, Guanajuato. Historia breve, FCE/ COLMEX/FHA, Mexico City, 2011. [2] E. Nalda, La arqueología de Guanajuato. Trabajos recientes, Arqueol. Mex. (2008) 36–43. [3] Instituto Nacional de Estadística y Geografía (INEGI), Conociendo Guanajuato, 6th Ed, Instituto Nacional de Estadística y Geografía, Mexico, 2016. [4] Instituto Nacional de Estadística y Geografía, Tabulados del cuestionario ampliado, Censo de Población y Vivienda 2010. (2011). http://www.beta.inegi.org.mx/ proyectos/ccpv/2010/ (accessed 06.09.18). [5] B. Braniff, Guanajuato en la historia, Arqueol. Mex. 28–35 (2008). [6] D. Frye, The native peoples of northeastern Mexico, in: R.E.W. Adams, M.J. MacLeod (Eds.), The Cambridge History of the Native Peoples of the Americas, Mesoamerica, Vol. II Cambridge University Press, Cambridge, 2008, pp. 89–135. [7] J. Sobrino, Migración interna en México durante el siglo XX, 1st Ed., Consejo Nacional de Población, Mexico City, 2010. [8] 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 in Mexico correlates with underlying population genetic structure, Hum. Immunol. (2019). [9] I. Silva-Zolezzi, A. Hidalgo-Miranda, J. Estrada-Gil, J.C. Fernandez-Lopez, L. UribeFigueroa, A. Contreras, et al., Analysis of genomic diversity in Mexican Mestizo populations to develop genomic medicine in Mexico, Proc. Natl. Acad. Sci. U.S.A. 106 (2009) 8611–8616. [10] A. Moreno-Estrada, C.R. Gignoux, J.C. Fernández-López, F. Zakharia, M. Sikora, A.V. Contreras, et al., The genetics of Mexico recapitulates Native American substructure and affects biomedical traits, Science 344 (2014) 1280–1285, https://doi. org/10.1126/science.1251688. [11] B.Z. González-Sobrino, A.P. Pintado-Cortina, L. Sebastián-Medina, F. MoralesMandujano, A.V. Contreras, Y.E. Aguilar, et al., Genetic diversity and differentiation in urban and indigenous populations of mexico: patterns of mitochondrial DNA and Y-chromosome lineages, Biodemogr. Soc. Biol. 62 (2016) 53–72, https://doi.org/ 10.1080/19485565.2015.1117938. [12] D. Oropeza, La migración asiática libre al centro del virreinato novohispano, 1565–1700, Relaciones Estudios de Historia y Sociedad. 37 (2017) 347, https://doi. org/10.24901/rehs.v37i147.181. [13] J.J. Gómez Izquierdo, El movimiento antichino en México (1871–1934) : problemas del racismo y del nacionalismo durante la Revolución Mexicana, Instituto Nacional de Antropología e Historia, Mexico City, 1992. [14] E.J.M. dos Santos, A. McCabe, F.F. Gonzalez-Galarza, A.R. Jones, D. Middleton, Allele frequencies net database: improvements for storage of individual genotypes and analysis of existing data, Hum. Immunol. 77 (2016) 238–248, https://doi.org/ 10.1016/j.humimm.2015.11.013. [15] Google, Google Earth Pro ©, (2019). earth.google.com.
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Contents lists available at ScienceDirect
Human Immunology journal homepage: www.elsevier.com/locate/humimm
Genetic diversity of HLA system in three populations from Guanajuato, Mexico: Guanajuato City, León and rural Guanajuato Jorge Arturo Pantoja-Torresa,1, Rodrigo Barquerab,c,1, , Mónica Ballesteros-Romeroc,1, Alicia Bravo-Acevedod,1, Esteban Arrieta-Bolañose,1, Gustavo Daniel Montiel-Hernándezf,1, Stephen Claytonc,1, Lidia Iris Rodríguez-Rodríguezg,1, Diana Iraíz Hernández-Zaragozac,h, Isis Goné-Vázquezi, Araceli Escobedo-Ruízi, Víctor Eduardo García-Ariasj, Francia Paulina Arellano-Pradoj, Marla Estefanía Rodríguez-Lópezj, María Guadalupe de Jesús Sánchez-Fernándezk, Mario J. Sandoval-Sandovall, Benjamín Gómez-Navarrom, Joaquín Zúñigan,o, Edmond J. Yunisp, Carolina Bekker-Méndezq, ⁎ Julio Granadosr, ⁎
a
Immunology Division, Unidad Médica de Alta Especialidad (UMAE) # 1, Instituto Mexicano del Seguro Social (IMSS), León, Guanajuato, Mexico Department of Archaeogenetics, Max Planck Institute for the Science of Human History (MPI-SHH), Jena, Germany Molecular Genetics Laboratory, Escuela Nacional de Antropología e Historia (ENAH), Mexico City, Mexico d Blood Bank, Unidad Médica de Alta Especialidad (UMAE) Hospital de Gineco Obstetricia No. 4 “Luis Castelazo Ayala”, Instituto Mexicano del Seguro Social (IMSS), Mexico City, Mexico e Institute for Experimental Cellular Therapy, University Hospital Essen, Essen, Germany f Escuela Nacional de Antropología e Historia (ENAH), Mexico City, Mexico g Archaeology Section, Centro INAH Guanajuato, Instituto Nacional de Antropología e Historia (INAH), Guanajuato, Guanajuato, Mexico h Immunogenetics Unit, Técnicas Genéticas Aplicadas a la Clínica (TGAC), Mexico City, Mexico i Histocompatibility Laboratory, Hospital de Especialidades, Centro Médico Nacional de Occidente (CMNO), Instituto Mexicano del Seguro Social (IMSS), Guadalajara, Jalisco, Mexico j Pediatrics Hospital, Centro Médico Nacional de Occidente (CMNO), Instituto Mexicano del Seguro Social (IMSS), Guadalajara, Jalisco, Mexico k Department of Nephrology and Transplantation Unit, Centro Médico Nacional de Occidente (CMNO), Instituto Mexicano del Seguro Social (IMSS), Guadalajara, Jalisco, Mexico l Central Office of Transplantation, Centro Médico Nacional de Occidente (CMNO), Instituto Mexicano del Seguro Social (IMSS), Guadalajara, Jalisco, Mexico m Central Office of Nephrology, Centro Médico Nacional de Occidente (CMNO), Instituto Mexicano del Seguro Social (IMSS), Guadalajara, Jalisco, Mexico n Laboratory of Immunobiology and Genetics, Instituto Nacional de Enfermedades Respiratorias Ismael Cosío Villegas, Mexico City, Mexico o Tecnologico de Monterrey, Escuela de Medicina y Ciencias de la Salud, Mexico City, Mexico p Department of Cancer Immunology and Virology, Dana-Farber Cancer Institute, Boston, MA, USA q Immunology and Infectology Research Unit, Infectology Hospital, Centro Médico Nacional “La Raza”, Instituto Mexicano del Seguro Social (IMSS), Mexico City, Mexico r Department of Transplantation, Instituto Nacional de Ciencias Médicas y Nutrición “Salvador Zubirán” (INCMNSZ), Mexico City, Mexico b c
ARTICLE INFO
ABSTRACT
Keywords: HLA Immunogenetics Population genetics Guanajuato Admixture
We studied HLA class I (HLA-A, -B) and class II (HLA-DRB1, -DQB1) alleles by PCR-SSP based typing in 262 Mexicans from the state of Guanajuato living in the cities of Guanajuato (N = 78), León (N = 22) and rural communities (N = 162), to obtain information regarding allelic and haplotypic frequencies. We find that the most frequent haplotypes found in the state of Guanajuato include 12 Native American and three European haplotypes. Admixture estimates revealed that the main genetic components in the state of Guanajuato are Native American (50.64 ± 2.11% by ML, 43.35% of Native American haplotypes) and European (44.14 ± 1.14% by ML; 39.35% of European haplotypes), while African genetic component is less apparent (5.22 ± 2.08% by ML; 8.36% of African haplotypes).
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 (MPI-SHH), 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.2019.06.002 Received 3 June 2019; Accepted 6 June 2019 0198-8859/ © 2019 American Society for Histocompatibility and Immunogenetics. Published by Elsevier Inc. All rights reserved.
Please cite this article as: Jorge Arturo Pantoja-Torres, et al., Human Immunology, https://doi.org/10.1016/j.humimm.2019.06.002
Human Immunology xxx (xxxx) xxx–xxx
J.A. Pantoja-Torres, et al.
The state of Guanajuato is located in the Central region of Mexico, and is part of the western zone, bordered to the west by the state of Jalisco, to the northwest by Zacatecas, to the east by Querétaro and to the south by Michoacán. It is divided internally into three major geographical regions: the Northern region, the Bajío and the Southern region [1]. The zone of plains that extend along the rivers that feed the Lerma and that go into Querétaro and Jalisco is known as the Bajío area, a prosperous region that is dedicated to agriculture [2]. The orography of Guanajuato is determined by the Sierra Madre Occidental, the Transversal Volcanic Axis and the Sierra Madre del Sur, as well as the local mountain system. The Sierra de Guanajuato has been the center of the most important mining operations in the country since colonial times. Guanajuato’s location right in the center of the country brings it closer to its three most important cities (Mexico City, Guadalajara and Monterrey), plus the distance to both the northern and southern borders is roughly the same. The state of Guanajuato is one of the most populated in the country with a total of 5 853 677 people living there, in an area of 30 589 square kilometers, which represents 1.6% of the total area of the country, resulting in a population density of 191 inhabitants/Km2. The population is distributed in 46 municipalities of which 70% are localities considered urban, while 30% of the population lives in rural regions [3]. The capital of the state is the city of Guanajuato, although with 184 239 inhabitants it is not the most populated. León is the most populated city with 1 578 626 inhabitants, followed by the cities of Irapuato and Celaya. At least ten municipalities concentrate population numbering between 100 000 to 250 000 inhabitants, followed by 14 municipalities that have a population size between 50 000 and 100 000 inhabitants; and finally six municipalities with populations numbering between 25 000 and 50 000 inhabitants [4]. The current settlement pattern dates back to the Colonial period and revolved around economic activity, especially mining and agriculture. Speakers of indigenous languages are few: 3 239 Otomí speakers, followed by Chichimeca jonaz with 2 142 speakers, Náhuatl (1 246 speakers), and finally 818 speakers of Mazahua [3]. However, this pattern was different and fluctuating during the pre-Hispanic era. The history of Guanajuato is intimately linked to the history of the northern region of the country, western Mexico and the Valley of Mexico basin. During the pre-Hispanic era it constituted the border zone between Mesoamerica and the northern region, a fluctuating frontier that allowed the interchange between these two regions [1]. Data on early human occupation of the current state of Guanajuato are scarce and resemble that of lithic age hunter-gatherer groups that have been found in other areas of the country. It is assumed that the transition of these small groups of hunter-gatherers to semi-sedentary
agricultural villages was a process similar to what happened in other areas of Mesoamerica. In the region of Guanajuato there is archaeological evidence of human occupation over three periods: settlement (represented by the Chupícuaro cultural tradition between 400 and 100 BCE [2]), a period of depopulation (abandonment of the important sedentary sites that occurred between 800 and 1300 AD), and finally a period of repopulation (event that began in the second half of the 14th century) [1]. Undoubtedly, the influence of the Chupícuaro cultural tradition on the diverse cultures of the West, as well as on the emergence of the great urban centers of the center and valley of Mexico was lasting and extensive, so that it is possible to find its characteristic ceramics in places such as Tula and Teotihuacán, as well as in Cuicuilco [5]. The lands north of the Lerma River were not always arid and these were populated by sedentary agricultural groups that founded complex urban centers with a notable Toltec and central Mesoamerica influence, but also of the large urban centers of northern Mexico. [1]. However, between the 10th and 11th centuries AD, the abandonment of this area gradually began, either because an abrupt climate change produced intense aridity that took agricultural peoples to abandon their settlements or due to the fall and collapse of Tula and Teotihuacán, leading to a massive population rearrangement during the Classic period [2]. The archaeological record accounts for an important historical moment: all the sites were abandoned and diverse nomadic groups (hunter-gatherers practicing agriculture at a small scale) arrived to the same regions. However, these groups had cultural features considered as Mesoamerican, built important centers, belonged to socially stratified societies and celebrated elaborate rites. During the late post Classic, in the last moments of Pre-Columbian America, the Tarascans were the hegemonic group. They formed an empire that extended its limits throughout the state and became the opposition to the dominant power of the Mexicas that established control in the central lands of the country [1,2]. With the conquest of Mexico-Tenochtitlan the Spanish began exploration and colonization of the territory called New Spain. One of the first explorations to the state of Guanajuato was lead by Nuño de Guzmán, but it was the religious orders, especially the Franciscans, who established the Indian villages, concentrating the dispersed population [1]. The need to control the rebel groups of the north (i.e. the Chichimeca) and the need to exploit the silver deposits and to make use of the lands for agriculture and settling cattle ranches led them to start a war against the indigenous groups of the north, which resulted in the annihilation and subjugation of most of the peoples living there [1,6]. Currently the state of Guanajuato maintains a remarkable population density, its economic sector continues to focus on mining and agriculture as main engines, although it also presents a considerable flow of national and international migration, especially to the USA, it is Fig. 1. Geographic situation of Guanajuato and admixture proportions for the state of Guanajuato [composed by the following populations: Mexico Guanajuato, Guanajuato city, N = 22, Allele Frequencies Net Database Identifier (AFND-ID): 3498; Mexico Guanajuato, León, N = 78, AFND-ID: 3497; Mexico Guanajuato Rural, N = 162, AFND-ID: 3581]. Admixture proportions were estimated by 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 [15].
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J.A. Pantoja-Torres, et al.
still an attractor of population from other areas of the country and from other countries [4,7]. For the present work, we analyzed HLA class I (HLA-A, -B) and class II (HLA-DRB1, -DQB1) PCR-SSP based typings in 262 Mexicans from the state of Guanajuato [composed by the following populations: Mexico Guanajuato, Guanajuato city, N = 22, Allele Frequencies Net Database Identifier (AFND-ID): 3498; Mexico Guanajuato, León, N = 78, AFNDID: 3497; Mexico Guanajuato Rural, N = 162, AFND-ID: 3581]. In addition to the individual populations we also show data for these combined populations. The latter are not held on AFND to prevent duplication of data. Maximum-likelihood (ML) frequencies for alleles and four-locus haplotypes were estimated using an ExpectationMaximization algorithm. For a comprehensive review on the methods, such as sample collection, HLA typing and statistical analyses, please refer to [8] in this same issue. For the frequencies of HLA-A, -B, -DRB1 and -DQB1 and haplotypic data for the sample sets of the state of Guanajuato please refer to the Supplementary Information: Supplementary Tables 1–8. For data on Hardy-Weinberg equilibrium (HWE) please see Supplementary Information: Supplementary Table 9 of this work and Supplementary Information: Supplementary Table 9 in [8] in this same issue. We find that the most frequent haplotypes for the state (haplotypic frequency, H.F. > 1.0%, arbitrarily; Supplementary Table 5) include 12 Native American (HLA ∼ A*02 ∼ B*35 ∼ DRB1*08 ∼ DQB1*04, A*02 ∼ B*39 ∼ DRB1*04 ∼ DQB1*03:02, A*68 ∼ B*39 ∼ DRB1*04 ∼ DQB1*03:02, A*24 ∼ B*39 ∼ DRB1*04 ∼ DQB1*03:02, A*24 ∼ B*35 ∼ DRB1*04 ∼ DQB1*03:02, A*02 ∼ B*35 ∼ DRB1*04 ∼ DQB1*03:02, A*02 ∼ B*39 ∼ DRB1*08 ∼ DQB1*04, A*02 ∼ B*15:01 ∼ DRB1*08 ∼ DQB1*04, A*31 ∼ B*35 ∼ DRB1*04 ∼ DQB1*03:02, A*31 ∼ B*35 ∼ DRB1*08 ∼ DQB1*04, A*68 ∼ B*39 ∼ DRB1*08 ∼ DQB1*04 and A*24 ∼ B*35 ∼ DRB1*16 ∼ DQB1*03:01) and three European (HLA ∼ A*29 ∼ B*44 ∼ DRB1*07 ∼ DQB1*02, A*01 ∼ B*08 ∼ DRB1*03:01 ∼ DQB1*02 and A*68 ∼ B*14:02 ∼ DRB1*01 ∼ DQB1*05) haplotypes. Admixture estimates (Fig. 1) revealed that the main genetic components in the state of Guanajuato are Native American (50.64 ± 2.11% by the ML method and 43.35% by estimating the proportion of Native American haplotypes) and European (44.14 ± 1.14% by the ML method and 39.35% by estimating the proportion of European haplotypes), while African genetic component is less apparent (5.22 ± 2.08% by the ML method and 8.36% by estimating the proportion of African haplotypes). Previous reports on admixture estimations for the state of Guanajuato using genome-wide SNP data show similar proportions of Native American (57.6% ± 9.6% [9]; 59.17% [10]) and European (39.9 ± 10.0% [9]; 36.78% [10]) ancestral contributions, with a less prominent African component (1.1 ± 1.8% [9]; 4.05% [10]). In line with previous reports [11], we find a higher contribution of African ancestry in rural areas when compared with urban settlements both by ML estimations [7.63 ± 0.54% vs. 0.00 ± 5.20% (Guanajuato) vs. 2.18 ± 5.26% (León), respectively] and by the proportion of African haplotypes present in the sample sets [9.51% vs. 6.81% (Guanajuato) vs. 6.41% (León), respectively]. However, the Native American component follows a different pattern with higher proportion of Native American ancestry in the cities than in the rural areas both by ML estimations [47.91 ± 1.58% vs. 75.23 ± 4.01% (Guanajuato) vs.
49.17 ± 3.84% (León), respectively] and by the proportion of Native American haplotypes present in the sample sets [41.72% vs. 56.82% (Guanajuato) vs. 42.95% (León), respectively]. The proportion of Asian haplotypes appears relatively constant in all sample sets analyzed (7.03% for the whole state, 6.81% for Guanajuato, 6.41% for León and 7.36% for the rural areas), which is slightly different to previous reports using genome-wide SNP data (1.3 ± 2.1% [9]). This component may be present due to the large numbers of Southeast Asians arriving via the Manila Galleon trade route and settling in the Central Region of the Vice-Royalty of New Spain during the first two centuries of the Colonial Period [12] but also with the East Asian migration events happening during the last part of the 19th century and the beginning of the 20th century [13]. All data from our sample sets, both frequencies and individual genotypes, can be found at The Allele Frequency Net Database website (www.allelefrequencies.netwww.allelefrequencies.net) [14]. Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.humimm.2019.06.002. References [1] M. Blanco, Alma Parra, Ethelia Ruiz Medrano, Guanajuato. Historia breve, FCE/ COLMEX/FHA, Mexico City, 2011. [2] E. Nalda, La arqueología de Guanajuato. Trabajos recientes, Arqueol. Mex. (2008) 36–43. [3] Instituto Nacional de Estadística y Geografía (INEGI), Conociendo Guanajuato, 6th Ed, Instituto Nacional de Estadística y Geografía, Mexico, 2016. [4] Instituto Nacional de Estadística y Geografía, Tabulados del cuestionario ampliado, Censo de Población y Vivienda 2010. (2011). http://www.beta.inegi.org.mx/ proyectos/ccpv/2010/ (accessed 06.09.18). [5] B. Braniff, Guanajuato en la historia, Arqueol. Mex. 28–35 (2008). [6] D. Frye, The native peoples of northeastern Mexico, in: R.E.W. Adams, M.J. MacLeod (Eds.), The Cambridge History of the Native Peoples of the Americas, Mesoamerica, Vol. II Cambridge University Press, Cambridge, 2008, pp. 89–135. [7] J. Sobrino, Migración interna en México durante el siglo XX, 1st Ed., Consejo Nacional de Población, Mexico City, 2010. [8] 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 in Mexico correlates with underlying population genetic structure, Hum. Immunol. (2019). [9] I. Silva-Zolezzi, A. Hidalgo-Miranda, J. Estrada-Gil, J.C. Fernandez-Lopez, L. UribeFigueroa, A. Contreras, et al., Analysis of genomic diversity in Mexican Mestizo populations to develop genomic medicine in Mexico, Proc. Natl. Acad. Sci. U.S.A. 106 (2009) 8611–8616. [10] A. Moreno-Estrada, C.R. Gignoux, J.C. Fernández-López, F. Zakharia, M. Sikora, A.V. Contreras, et al., The genetics of Mexico recapitulates Native American substructure and affects biomedical traits, Science 344 (2014) 1280–1285, https://doi. org/10.1126/science.1251688. [11] B.Z. González-Sobrino, A.P. Pintado-Cortina, L. Sebastián-Medina, F. MoralesMandujano, A.V. Contreras, Y.E. Aguilar, et al., Genetic diversity and differentiation in urban and indigenous populations of mexico: patterns of mitochondrial DNA and Y-chromosome lineages, Biodemogr. Soc. Biol. 62 (2016) 53–72, https://doi.org/ 10.1080/19485565.2015.1117938. [12] D. Oropeza, La migración asiática libre al centro del virreinato novohispano, 1565–1700, Relaciones Estudios de Historia y Sociedad. 37 (2017) 347, https://doi. org/10.24901/rehs.v37i147.181. [13] J.J. Gómez Izquierdo, El movimiento antichino en México (1871–1934) : problemas del racismo y del nacionalismo durante la Revolución Mexicana, Instituto Nacional de Antropología e Historia, Mexico City, 1992. [14] E.J.M. dos Santos, A. McCabe, F.F. Gonzalez-Galarza, A.R. Jones, D. Middleton, Allele frequencies net database: improvements for storage of individual genotypes and analysis of existing data, Hum. Immunol. 77 (2016) 238–248, https://doi.org/ 10.1016/j.humimm.2015.11.013. [15] Google, Google Earth Pro ©, (2019). earth.google.com.
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