Class I MHC Polymorphisms Associated with Type 2 Diabetes in the Mexican Population
Abstract
:1. Introduction
2. Materials and Methods
2.1. Exploration of the SIGMA Database
2.1.1. Diabetes in Mexico Study (DMS)
2.1.2. Mexico City Diabetes Study (MCDS)
2.1.3. Multiethnic Cohort (MEC)
2.1.4. UNAM/INCMNSZ Diabetes Study (UIDS)
2.2. Analysis and Documentation of Variants Found
2.3. IPD-IMGT/HLA Analysis
2.4. Comparison with GEO Dataset
3. Results
3.1. HLA Found Variants
3.2. HLA-A*03:01:01:01 Allele
3.3. HLA-C*01:02:01:01 Allele
3.4. HLA-C*01:02:01:01 and HLA-C*01:02:01:01 Allelic Frequencies
3.5. Differential HLA-A and HLA-C Expression Using GEO
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care 2009, 32, S62–S67. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ali, O. Genetics of type 2 diabetes. World J. Diabetes 2013, 4, 114–123. [Google Scholar] [CrossRef] [PubMed]
- Prasad, R.B.; Groop, L. Genetics of type 2 diabetes-pitfalls and possibilities. Genes 2015, 6, 87–123. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- DiMeglio, L.A.; Evans-Molina, C.; Oram, R.A. Type 1 diabetes. Lancet 2018, 391, 2449–2462. [Google Scholar] [CrossRef]
- U.K. Prospective Diabetes Study Group. Prospective Diabetes Study 16: Overview of 6 Years’ Therapy of Type II Diabetes: A Progressive Disease. Diabetes 1995, 44, 1249–1258. [Google Scholar] [CrossRef]
- Levy, J.; Atkinson, A.B.; Bell, P.M.; McCance, D.R.; Hadden, D.R. β-cell deterioration determines the onset and rate of progression of secondary dietary failure in Type 2 diabetes mellitus: The 10-year follow-up of the Belfast Diet Study. Diabet. Med. 1998, 15, 290–296. [Google Scholar] [CrossRef]
- Kahn, S.E.; Haffner, S.M.; Heise, M.A.; Herman, W.H.; Hotoan, R.R.; Jones, N.P.; Kravitz, B.G.; Lachin, J.M.; O’Neill, M.C.; Zinman, B.; et al. Glycemic durability of rosiglitazone, metformin, or glyburide monotherapy. N. Engl. J. Med. 2006, 355, 2427–2443. [Google Scholar] [CrossRef] [Green Version]
- Grant, S.F.A. The TCF7L2 Locus: A Genetic Window Into the Pathogenesis of Type 1 and Type 2 Diabetes. Diabetes Care 2019, 42, 1624–1629. [Google Scholar] [CrossRef] [Green Version]
- Moin, A.S.M.; Butler, A.E. Alterations in β Cell Identity in Type 1 and Type 2 Diabetes. Curr. Diabetes Rep. 2019, 19, 83. [Google Scholar] [CrossRef] [Green Version]
- Wiebe, J.C.; Wägner, A.M.; Novoa Mogollón, F.J. Genética de la diabetes mellitus. Nefrología 2011, 2, 111–119. [Google Scholar] [CrossRef]
- Alberts, B.; Johnson, A.; Lewis, J.; Raff, M.; Roberts, K.; Walter, P. T Cells and MHC Proteins. In Book Molecular Biology of the Cell, 4th ed.; Garland Science: New York, NY, USA, 2002. Available online: https://www.ncbi.nlm.nih.gov/books/NBK26926/ (accessed on 15 March 2021).
- Clement, C.C.; Nanaware, P.P.; Yamazaki, T.; Negroni, M.P.; Ramesh, K.; Morozova, K.; Thangaswamy, S.; Graves, A.; Kim, H.J.; Li, T.W.; et al. Pleiotropic consequences of metabolic stress for the major histocompatibility complex class II molecule antigen processing and presentation machinery. Immunity 2021, 54, 721–736. [Google Scholar] [CrossRef] [PubMed]
- Perez-Luque, E.; Alaez, C.; Malacara, J.M.; Garay, M.E.; Fajardo, M.E.; Nava, L.E.; Gorodezky, C. Protective effect of DRB1 locus against type 2 diabetes mellitus in Mexican Mestizos. Hum. Immunol. 2003, 64, 110–118. [Google Scholar] [CrossRef]
- Tipu, H.N.; Ahmed, T.A.; Bashir, M.M. Human leukocyte antigen class II susceptibility conferring alleles among non-insulin dependent diabetes mellitus patients. J. Coll. Physicians Surg. Pak. 2011, 21, 26–29. [Google Scholar] [PubMed]
- Rich, S.S.; French, L.R.; Sprafka, J.M.; Clements, J.P.; Goetz, F.C. HLA-associated susceptibility to type 2 (non-insulin-dependent) diabetes mellitus: The Wadena City Health Study. Diabetologia 1993, 36, 234–238. [Google Scholar] [CrossRef] [Green Version]
- Groop, L.; Koskimies, S.; Pelkonen, R.; Tolppanen, E.M. Increased frequency of HLA-Cw4 in type 2 diabetes. Acta Endocrinol. 1983, 104, 475–478. [Google Scholar] [CrossRef]
- Jeck, W.R.; Siebold, A.P.; Sharpless, N.E. Review: A meta-analysis of GWAS and age-associated diseases. Aging Cell 2012, 11, 727–731. [Google Scholar] [CrossRef] [Green Version]
- Torres-García, D.; Barquera, R.; Zúñiga, J. Receptores de células NK (KIR): Estructura, función y relevancia en la susceptibilidad de enfermedades. Rev. Inst. Nal. Enf. Resp. Mex. 2008, 21, 57–65. [Google Scholar]
- Shapiro, M.R.; Thirawatananond, P.; Peters, L.; Sharp, R.C.; Ogundare, S.; Posgai, A.L.; Perry, D.J.; Brusko, T.M. De-coding genetic risk variants in type 1 diabetes. Immunol. Cell Biol. 2021, 99, 496–508. [Google Scholar] [CrossRef]
- Sharma, C.; Ali, B.R.; Osman, W.; Afandi, B.; Aburawi, E.H.; Beshyah, S.A.; Al-Mahayri, Z.; Al-Rifai, R.H.; Al Yafei, Z.; ElGhazali, G.; et al. Association of variants in PTPN22, CTLA-4, IL2-RA, and INS genes with type 1 diabetes in Emiratis. Ann. Hum. Genet. 2021, 85, 48–57. [Google Scholar] [CrossRef]
- Valta, M.; Gazali, A.M.; Viisanen, T.; Ihantola, E.L.; Ekman, I.; Toppari, J.; Knip, M.; Veijola, R.; Ilonen, J.; Lempainen, J.; et al. Type 1 diabetes linked PTPN22 gene polymorphism is associated with the frequency of circulating regulatory T cells. Eur. J. Immunol. 2020, 50, 581–588. [Google Scholar] [CrossRef]
- Bhatia, K.; Patel, M.; Gorogo, M. Type 2 (non-insulin-dependent) diabetes mellitus and HLA antigens in Papua New Guinea. Diabetologia 1984, 27, 370–372. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tuomilehto-Wolf, E.; Tuomilehto, J.; Hitman, G.A.; Nissinen, A.; Stengård, J.; Pekkanen, J.; Kivinen, P.; Kaarsalo, E.; Karvonen, M.J. Genetic susceptibility to non-insulin dependent diabetes mellitus and glucose intolerance are located in HLA region. BMJ 1993, 307, 155–159. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Diamantopoulos, E.J.; Andreadis, E.A.; Kakou, M.G.; Vassilopoulos, C.V.; Vlachonikolis, I.G.; Gianna-Kopoulos, N.A.; Tarassi, K.E.; Papasteriades, C.A.; Nicolaides, A.N. Association of the HLA antigens with early atheromatosis in subjects with type 2 diabetes mellitus. Int. Angiol. 2002, 21, 379–383. [Google Scholar] [PubMed]
- Imura, H.; Kuzuya, H.; Seino, Y. MHC class II antigen and other genes in NIDDM. Nihon Rinsho 1991, 49, 531–536. [Google Scholar] [PubMed]
- Banerji, M.A.; Norin, A.J.; Chaiken, R.L.; Lebovitz, H.E. HLA-DQ associations distinguish insulin-resistant and insulin-sensitive variants of NIDDM in black Americans. Diabetes Care 1993, 16, 429–433. [Google Scholar] [CrossRef]
- Romano-Carratelli, C.; Galdiero, M.; Bentivoglio, C.; Nuzzo, I.; Cozzolino, D.; Torella, R. HLA class II antigens and interleukin-1 in patients affected by type-II diabetes mellitus and hyperlipemia. J. Med. 1993, 24, 28–34. [Google Scholar]
- Pandey, J.P.; Zamani, M.; Cassiman, J.-J. Epistatic effects of genes encoding tumor necrosis factor-α, immunoglobulin allotypes, and HLA antigens on susceptibility to non-insulin-dependent (type 2) diabetes mellitus. Immunogenetics 1999, 49, 860–864. [Google Scholar] [CrossRef]
- Motala, A.A.; Busson, M.; Al-Harbi, E.M.; Khuzam, M.A.A.; Al-Omari, E.M.D.; Arekat, M.R.; Almawi, W.Y. Susceptible and protective human leukocyte antigen class II alleles and haplotypes in bahraini type 2 (non-insulin-dependent) diabetes mellitus patients. Clin. Diagn. Lab. Immunol. 2005, 12, 213–217. [Google Scholar] [CrossRef] [Green Version]
- Jacobi, T.; Massier, L.; Klöting, N.; Horn, K.; Schuch, A.; Ahnert, P.; Engel, C.; Löffler, M.; Burkhardt, R.; Thiery, J.; et al. HLA Class II Allele Analyses Implicate Common Genetic Components in Type 1 and Non-Insulin-Treated Type 2 Diabetes. J. Clin. Endocrinol. Metab. 2020, 105, e245–e254. [Google Scholar] [CrossRef]
- Chinniah, R.; Sevak, V.; Pandi, S.; Ravi, P.M.; Vijayan, M.; Kannan, A.; Karuppiah, B. HLA-DRB1 genes and the expression dynamics of HLA CIITA determine the susceptibility to T2DM. Immunogenetics 2021, 73, 291–305. [Google Scholar] [CrossRef]
- Shin, S.; Hyun, B.; Lee, A.; Kong, H.; Han, S.; Lee, C.K.; Ha, N.J.; Kim, K. Metformin Suppresses MHC-Restricted Antigen Presentation by Inhibiting Co-Stimulatory Factors and MHC Molecules in APCs. Biomol. Ther. 2013, 21, 35–41. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Williams, A.L.; Jacobs, S.B.; Moreno-Macías, H.; Huerta-Chagoya, A.; Churchhouse, C.; Márquez-Luna, C.; García-Ortíz, H.; Gómez-Vázquez, M.J.; Burtt, N.P.; Aguilar-Salinas, C.A.; et al. Sequence variants in SLC16A11 are a common risk factor for type 2 diabetes in Mexico. Nature 2014, 506, 97. [Google Scholar] [CrossRef] [PubMed]
- Patti, M.E.; Butte, A.J.; Crunkhorn, S.; Cusi, K.; Berria, R.; Kashyap, S.; Miyazaki, Y.; Kohane, I.; Costello, M.; Saccone, R.; et al. Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: Potential role of PGC1 and NRF1. Proc. Natl. Acad. Sci. USA 2003, 100, 8466–8471. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Marselli, L.; Thorne, J.; Dahiya, S.; Sgroi, D.C.; Sharma, A.; Bonner-Weir, S.; Marchetti, P.; Weir, G.C. Gene expression profiles of β-cell enriched tissue obtained by laser capture microdissection from subjects with type 2 diabetes. PLoS ONE 2010, 5, e11499. [Google Scholar] [CrossRef] [Green Version]
- Itariu, B.K.; Stulnig, T.M. Autoimmune aspects of type 2 diabetes mellitus—A mini-review. Gerontology 2014, 60, 189–196. [Google Scholar] [CrossRef]
- Napolitano, G.; Bucci, I.; Giuliani, C.; Massafra, C.; Di Petta, C.; Devangelio, E.; Singer, D.S.; Monaco, F.; Kohn, L.D. High glucose levels increase major histocompatibility complex class I gene expression in thyroid cells and amplify interferon-γ action. Endocrinology 2002, 143, 1008–1017. [Google Scholar] [CrossRef]
- Nam, H.W.; Cho, Y.J.; Lim, J.A.; Kim, S.J.; Kim, H.; Sim, S.Y.; Lim, D.G. Functional status of immune cells in patients with long-lasting type 2 diabetes mellitus. Clin. Exp. Immunol. 2018, 194, 125–136. [Google Scholar] [CrossRef] [Green Version]
- Sarikonda, G.; Pettus, J.; Phatak, S.; Sachithanantham, S.; Miller, J.F.; Wesley, J.D.; Cadag, E.; Chae, J.; Ganesan, L.; Mallios, R.; et al. CD8 T-cell reactivity to islet antigens is unique to type 1 while CD4 T-cell reactivity exists in both type 1 and type 2 diabetes. J. Autoimmun. 2014, 50, 77–82. [Google Scholar] [CrossRef]
- Nakamura, M.; Nishida, W.; Yamada, Y.; Chujo, D.; Watanabe, Y.; Imagawa, A.; Hanafusa, T.; Kawasaki, E.; Onuma, H.; Osawa, H.; et al. Insulin administration may trigger pancreatic β-cell destruction in patients with type 2 diabetes. Diabetes Res. Clin. Pract. 2008, 79, 220–229. [Google Scholar] [CrossRef]
- Cucak, H.; Grunnet, L.G.; Rosendahl, A. Accumulation of M1-like macrophages in type 2 diabetic islets is followed by a systemic shift in macrophage polarization. J. Leukoc. Biol. 2014, 95, 149–160. [Google Scholar] [CrossRef]
- Dittmer, I.; Woodfield, G.; Simpson, I. Non-insulin-dependent diabetes mellitus in New Zealand Maori: A relationship with Class I but not Class II histocompatibility locus antigens. N. Z. Med. J. 1998, 111, 294–296. [Google Scholar] [PubMed]
- Berzina, L.; Shtauvere-Brameus, A.; Rumba, I.; Sanjeevi, C.B. Microsatellite allele A5.1 of MHC class I chain-related gene A is associated with latent autoimmune diabetes in adults in Latvia. Ann. N. Y. Acad. Sci. 2002, 958, 353–356. [Google Scholar] [CrossRef]
- Sanjeevi, C.B.; Kanungo, A.; Berzina, L.; Shtauvere-Brameus, A.; Ghaderi, M.; Samal, K.C. MHC class I chain-related gene alleles distinguish malnutrition-modulated diabetes, insulin-dependent diabetes, and non-insulin-dependent diabetes mellitus patients from eastern India. Ann. N. Y. Acad. Sci. 2002, 958, 341–344. [Google Scholar] [CrossRef] [PubMed]
- Pozzilli, P.; Pieralice, S. Latent Autoimmune Diabetes in Adults: Current Status and New Horizons. Endocrinol. Metab. 2018, 33, 147–159. [Google Scholar] [CrossRef] [PubMed]
- Acton, R.T.; Roseman, J.M.; Bell, D.S.; Goldenberg, R.L.; Tseng, M.L.; Vanichanan, C.; Harman, L.A.; Go, R.C. Genes within the major histocompatibility complex predict NIDDM in African-American women in Alabama. Diabetes Care 1994, 17, 1491–1494. [Google Scholar] [CrossRef]
- Groop, L.; Groop, P.H.; Koskimies, S. Relationship between B-cell function and HLA antigens in patients with type 2 (non-insulin-dependent) diabetes. Diabetologia 1986, 29, 757–760. [Google Scholar] [CrossRef]
- Jabbar, A.A.; Mezaal, T.J.; Dawood, F.H. Association of HLA antigens with diabetes mellitus in an Iraqi population. Dis. Markers 1989, 7, 79–85. [Google Scholar]
- Li, H.; Lindholm, E.; Almgren, P.; Gustafsson, å.; Forsblom, C.; Groop, L.; Tuomi, T. Possible Human Leukocyte Antigen-Mediated Genetic Interaction between Type 1 and Type 2 Diabetes. J. Clin. Endocrinol. Metab. 2001, 86, 574–582. [Google Scholar] [CrossRef] [Green Version]
- Patel, K.M. The Association of Human Leukocyte Antigen (HLA) Alleles and Type 2 Diabetes Mellitus (T2DM) among Mexican Americans (MA). ETD Collection University of Texas at El Paso. AAI3390623. Doctor Dissertation, ProQuest Dissertations Publishing, Ann Arbor, MI, USA, 2009. Available online: https://scholarworks.utep.edu/dissertations/AAI3390623 (accessed on 30 October 2020).
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Mendoza-Ramírez, P.; López-Olaiz, M.A.; Morales-Fernández, A.L.; Flores-Echiveste, M.I.; de Jesus Casillas-Navarro, A.; Pérez-Rodríguez, M.A.; de Jesús Orozco-Luna, F.; Cortés-Romero, C.; Zuñiga, L.Y.; Sanchez Parada, M.G.; et al. Class I MHC Polymorphisms Associated with Type 2 Diabetes in the Mexican Population. Genes 2022, 13, 772. https://doi.org/10.3390/genes13050772
Mendoza-Ramírez P, López-Olaiz MA, Morales-Fernández AL, Flores-Echiveste MI, de Jesus Casillas-Navarro A, Pérez-Rodríguez MA, de Jesús Orozco-Luna F, Cortés-Romero C, Zuñiga LY, Sanchez Parada MG, et al. Class I MHC Polymorphisms Associated with Type 2 Diabetes in the Mexican Population. Genes. 2022; 13(5):772. https://doi.org/10.3390/genes13050772
Chicago/Turabian StyleMendoza-Ramírez, Paola, Mildred Alejandra López-Olaiz, Adriana Lizeth Morales-Fernández, María Isabel Flores-Echiveste, Antonio de Jesus Casillas-Navarro, Marco Andrés Pérez-Rodríguez, Felipe de Jesús Orozco-Luna, Celso Cortés-Romero, Laura Yareni Zuñiga, María Guadalupe Sanchez Parada, and et al. 2022. "Class I MHC Polymorphisms Associated with Type 2 Diabetes in the Mexican Population" Genes 13, no. 5: 772. https://doi.org/10.3390/genes13050772
APA StyleMendoza-Ramírez, P., López-Olaiz, M. A., Morales-Fernández, A. L., Flores-Echiveste, M. I., de Jesus Casillas-Navarro, A., Pérez-Rodríguez, M. A., de Jesús Orozco-Luna, F., Cortés-Romero, C., Zuñiga, L. Y., Sanchez Parada, M. G., Hernandez-Ortega, L. D., Mercado-Sesma, A. R., & Baptista-Rosas, R. C. (2022). Class I MHC Polymorphisms Associated with Type 2 Diabetes in the Mexican Population. Genes, 13(5), 772. https://doi.org/10.3390/genes13050772