Association between field liming and the epidemic of Type 1 diabetes

Abstract

Zinc is an essential nutrient for mammals. Zinc has only one oxidation state Zn²⁺ but it has many coordination states, which can alter without demanding energy. Coordination states depend on prevailing pH. In soils the coordination state changes from octahedral (nonphysiologic) form to tetrahedral (physiologic) form when pH rises to about 6.5. Weathering processes of common soil mineral mica are also pH dependent. Large scale argricultural field liming began from 1950’s onward in the Western Countries and since that time the incidence of Type 1 diabetes (T1D) began to increase in the Western Countries. Liming elevates soil pH often near 6.5 and favours mosaic mica-vermiculite nanoparticle formation in which vermiculite corner binds zinc in tetrahedral (physiological) coordination state. In this pH mica corner remains in native form and offers the plane for soluble pMHC molecule (binded with antigenic beta-cell specific self peptide) to adhere on mica and as a consequence to trigger the activation of autoreactive CD4 and/or CD8 T cells. Beta-cell specific autoantigens are released because abundant zinc derived from endocytosed zinc-mica-vermiculite particles in lysosomes leads to incresed beta-cell apoptosis, also the physiological neonatal beta-cell mass remodeling enhance beta-cell specific auto-antigen release. Furthermore enterovirusinfections during first years of life are common and can release beta-cell specific auto-antigens. The probable disease mechanism is dealt with this review article.

Keywords

Soil liming / Zinc coordination states / Non-conventional T cell activation / Natural nanoparticles

References

[1] Knip M, Veijola R, Virtanen SM, et al. Environmental triggers and determinants of type 1 diabetes. Diabetes. 2005; 54: 125-36. https://doi.org/10.2337/diabetes.54.suppl_2.S125

[2] Honkanen H, Oikarinen S, Nurminen N, et al. Detection of enteroviruses in stools precedes islet autoimmunity by several months: possible evidence for slowly operating mechanism in virus-induced autoimmunity. Diabetologia. 2017; 60: 424-431. PMid:28070615. https://doi.org/10.1007/s00125-016-4177-z

[3] Gale EAM. The rise of childhood type 1 diabetes in the 20th century. Diabetes. 2002; 51: 3353-61. https://doi.org/10.2337/diabetes.51.12.3353

[4] Harjutsalo V, Sund R, Knip M, et al. Incidence of type1 diabetes in Finland. JAMA. 2013; 310(4): 427-28. PMid:23917294. https://doi.org/10.1001/jama.2013.8399

[5] Kondrashova A, Reunanen A, Romanov A, et al. A six-fold gradient in the incidence of type 1 diabetes at the eastern border of Finland. Ann Med. 2005; 37(1): 67-72. PMid:15902849. https://doi.org/10.1080/07853890410018952

[6] Uusitalo R, Salo R. Investigated soil-safe food (article in finnish). 2002; ISBN 951-729-695-9.

[7] Myyrä S. Decreasing trend in agricultural field liming (article in finnish). Koetoiminta ja käytäntö. 2004; 61(4): 11-12.

[8] The miracle of the cerrado. The Economist. 2010.

[9] Bernoux M, Volkoff B, da Conceicao M, et al. CO₂ emissions from liming of agricultural soils in Brazil. Global Biogeochemical Cycles. 2003; 17: 1049.

[10] Negrato CA, Dias JP, Teixeira MF, et al. Temporal trends in incidence of type 1 diabetes between 1986 and 2006 in Brazil. J Endocrinol Invest. 2010; 33: 373-7. PMid:19620822. https://doi.org/10.1007/BF03346606

[11] Newhook LA, Penney S, Fiander J, et al. Recent incidence of type 1 diabetes mellitus in children 0-14 years in Newfoundland and Labrador, Canada climbs to over 45/100,000: a retrospective time trend study. BMC Res Notes. 2012; 5: 628. PMid:23146327. https://doi.org/10.1186/1756-0500-5-628

[12] Dorff E, Beaulieu MS. Feeding the soil puts food on your plate. Statistics Canada, Census of Agriculture. 2015.

[13] Hoffmann SR, Shafer MM, Armstrong DE. Strong colloidal and dissolved organic ligands binding copper and zinc in rivers. Environ Sci Technol. 2007; 15: 6996-7002.

[14] Roberts DR, Ford RG, Sparks DL. Kinetics and mechanisms of Zn complexation on metal oxides using EXAFS spectroscopy. Journal of Colloid and Interface Science. 2003; 263: 364-376. https://doi.org/10.1016/S0021-9797(03)00281-9

[15] Krezel A, Maret W. The biological inorganic chemistry of zinc ions. Arch Biochem Biophys. 2016; 611: 3-19. PMid:27117234. https://doi.org/10.1016/j.abb.2016.04.010

[16] Voegelin A, Jacquat O, Barmettler K, et al. Time-dependent changes of zinc speciation in four soils contaminated with zincite or sphalerite. Environ Sci Technol. 2011; 45: 255-261. PMid:21142002. https://doi.org/10.1021/es101189d

[17] Covelo EF, Vega FA, Andrade ML. Competitive sorption and desorption of heavy metals by individual soil components. J Hazard Mater. 2007: 140: 308-15. PMid:17049729. https://doi.org/10.1016/j.jhazmat.2006.09.018

[18] Junnila SK. Type 1 diabetes epidemic in Finland is triggered by zinc-containig amorphous silica nanoparticles. Medical Hypotheses. 2015; 84: 336-340. PMid:25659493. https://doi.org/10.1016/j.mehy.2015.01.021

[19] Hillier S, Marwa EMM, Rice CM. On the mechanism of exfoliation of “vermiculite”. Clay Minerals. 2013; 48: 563-82. https://doi.org/10.1180/claymin.2013.048.4.01

[20] Jung M, Shin MK, Jung YK, et al. Modulation of macrophage activities in proliferation, lysosome and phagosome by the nonspecific immunostimulator, mica. PloS One. 2015; 10(2): e0117838. PMid:25668030. https://doi.org/10.1371/journal.pone.0117838

[21] Li YV. Zinc and insulin in pancreatic beta-cells. Endocrine. 2014; 45: 178-89. PMid:23979673. https://doi.org/10.1007/s12020-013-0032-x

[22] Kang TW, Kim HS, Lee BNC, et al. Mica nanoparticle, STB-HO eliminates the human breast carcinoma cells by regulating the interaction of tumor with its immune microenvironment. Scientific Reports. 2015; 5: article number 17515.

[23] Hojyo S, Fukada T. Roles of zinc sinaling in the immune system. Journal of Immunological Research. 2016; Article ID 6762343.

[24] Yu M, Lee WW, Tomar D, et al. Regulation of T cell receptor sinaling by activation-induced zinc influx. J Exp Med. 2011; 208: 775-85. PMid:21422171. https://doi.org/10.1084/jem.20100031

[25] Costello LC, Fenselau CC, Franklin RB. Evidence for operation of the direct zinc ligand exhange mechanism for trafficking, transport and reactivity of zinc in mammalian cells. J Inorg Biochem. 2011; 105: 589-99. PMid:21440525. https://doi.org/10.1016/j.jinorgbio.2011.02.002

[26] Danke NA, Koelle DM, Yee C, et al. Autorective T cells in healthy individuals. J Immunol. 2004; 172: 5967-72. https://doi.org/10.4049/jimmunol.172.10.5967

[27] Skowera A, Ladell K, McLaren JE, et al. Beta-cell-specific CD8 T cell phenotype in type 1 diabetes reflects chronic autoantigen exposure. Diabetes. 2015; 64: 916-925. PMid:25249579. https://doi.org/10.2337/db14-0332

[28] Phillips JM, Parish NM, Raine T, et al. Type 1 diabetes development requires both CD4+ and CD8+ T cells and can be reversed by non-depleting antibodies targeting both T cell populations. Rev Diabet Stud. 2009; 6: 97-103. PMid:19806239. https://doi.org/10.1900/RDS.2009.6.97

[29] Bourgeous C, Tanchot C. CD4 T cells are required for CD8 T cell memory generation. Eur J Immunol. 2003; 33: 3225-3231. PMid:14635030. https://doi.org/10.1002/eji.200324576

[30] Nicolau DV, Watson GS, Cahill C, et al. Actin adsorbed on HOPG and mica substrates: characterization and manipulation by atomic force microscopy. NSTI-Nanotech. 2004; 1: 103-105.

[31] Ma Z, Sharp KA, Janmey PA, et al. Surface-anchored monomeric agonist pMHCs alone trigger TCR with high sensitivity. PloSBiol. 2008; 6: e43. PMid:18303949. https://doi.org/10.1371/journal.pbio.0060043

[32] Frauwirth KA, Riley JL, Harris MH, et al. The CD28 signaling pathway regulates glucose metabolism. Immunity. 2002; 16: 769-77. https://doi.org/10.1016/S1074-7613(02)00323-0

[33] Arora G, Sajid A, Arulanandh MD, et al. Zinc regulates the activity of kinase-phosphatase pair (BasPrkC/BasPrpC) in Basillus anthracis. Biometals. 2013; 26: 715-30. PMid:23793375. https://doi.org/10.1007/s10534-013-9646-y

[34] Trudeau JD, Dutz JP, Arany E, et al. Neonatal beta-cell apoptosis: a trigger for autoimmune diabetes? Diabetes. 2000; 49: 1-7.

[35] Bach JM, Otto H, Nepom GT, et al. High affinity presentation of an autoantigenic peptide in type 1 diabetes by an HLA class II protein encoded in a haplotype protecting from disease. J Autoimmun. 1997; 10: 375-86. PMid:9237801. https://doi.org/10.1006/jaut.1997.0143

[36] Jung M, Lee J, Seo HY, et al. Cathepsin inhibition-induced lysosomal dysfunction enhances pancreatic beta-cell apoptosis in high glucose. PloS One. 2015; 10: e0116972.

[37] Lockwood TD. Lysosomal metal, redox and proton cycles influencing the CysHis cathepsin reaction. Metallomics. 2013; 5: 110-124. PMid:23302864. https://doi.org/10.1039/c2mt20156a

[38] Acker JG, Bricker OP. The influence of pH on biotite dissolution and alteration kinetics at low temperature. Geochimica et Cosmochimica Acta. 1992; 56: 3073-92. https://doi.org/10.1016/0016-7037(92)90290-Y

[39] Li T, Jianjun C. Nonporous silica nanoparticles for nanomedicine application. Nano Today. 2013; 8: 290-312. PMid:23997809. https://doi.org/10.1016/j.nantod.2013.04.007

[40] Tiede K, Boxall ABAB, Tear SP, et al. Detection and characterization of engineered nanoparticles in food and the environment. Food Additives & Contaminants: Part A. 2008; 25: 795-821. PMid:18569000. https://doi.org/10.1080/02652030802007553

[41] Sverdrup HU, Warfvinge PG. What is left for researchers in liming? A critical review of state-of-art acidification miotigation. Lake an Reservoir Management. 1988; 4: 87-97. https://doi.org/10.1080/07438148809354383

[42] Samuelsson U, Löfman O. Geographical mapping of type 1 diabetes in children and adolescents in south east Sweden. J Epidemiol Community Health. 2004; 58: 388-392. https://doi.org/10.1136/jech.2002.004135