Hepatic metal ion transporter ZIP8 regulates manganese homeostasis and manganese-dependent enzyme activity

Journal of Clinical Investigation

Volumn 127, Issue 6, 2017, Pages 2407-2417

  Lin, Wen ^a   Vann, David R ^b   Doulias, Paschalis Thomas ^c   Wang, Tao ^a   Landesberg, Gavin ^d   Li, Xueli ^c   Ricciotti, Emanuela ^e   Scalia, Rosario ^d   He, Miao ^c,f   Hand, Nicholas J ^f   Rader, Daniel J ^a,e,f  

^a Institute for Translational Medicine and Therapeutics   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^d TEMPLE UNIVERSITY   (United States)

^e Institute of Translational Medicine and Therapeutics   (United States)

^f UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGINASE; BETA 1,4 GALACTOSYLTRANSFERASE; MANGANESE; MESSENGER RNA; MULTIDRUG RESISTANCE PROTEIN 1; REGULATOR PROTEIN; SOLUTE CARRIER FAMILY 39 MEMBER 8; SOLUTE CARRIER PROTEIN; UNCLASSIFIED DRUG; CATION TRANSPORT PROTEIN; N ACETYLLACTOSAMINE SYNTHASE; SLC39A8 PROTEIN, MOUSE;

ADENO ASSOCIATED VIRUS; ALLELE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BILIARY EXCRETION; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; GENE OVEREXPRESSION; HOMEOSTASIS; HOMOZYGOSITY; LIVER CELL; MALE; MANGANESE BLOOD LEVEL; METABOLISM; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; ANIMAL; BILE; C57BL MOUSE; ENZYMOLOGY; GLYCOSYLATION; HEK293 CELL LINE; HUMAN; KNOCKOUT MOUSE; LIVER; PHYSIOLOGY; PROTEIN PROCESSING;

ANIMALS; ARGINASE; BILE; CATION TRANSPORT PROTEINS; FEMALE; GLYCOSYLATION; HEK293 CELLS; HOMEOSTASIS; HUMANS; LIVER; MALE; MANGANESE; MICE, INBRED C57BL; MICE, KNOCKOUT; N-ACETYLLACTOSAMINE SYNTHASE; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 85020211303     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI90896     Document Type: Article

References (55)

1. Ng E, et al. Genome-wide association study of toxic metals and trace elements reveals novel associations. Hum Mol Genet. 2015;24(16):4739-4745.
2. International Consortium for Blood Pressure Genome-Wide Association Studies, et al. Genetic variants in novel pathways influence blood pressure and cardiovascular disease risk. Nature. 2011;478(7367):103-109.
3. Ehret GB, et al. The genetics of blood pressure regulation and its target organs from association studies in 342, 415 individuals. Nat Genet. 2016;48(10):1171-1184.
4. Teslovich TM, et al. Biological, clinical and population relevance of 95 loci for blood lipids. Nature. 2010;466(7307):707-713.
5. Global Lipids Genetics Consortium, et al. Discovery and refinement of loci associated with lipid levels. Nat Genet. 2013;45(11):1274-1283.
6. Speliotes EK, et al. Association analyses of 249, 796 individuals reveal 18 new loci associated with body mass index. Nat Genet. 2010;42(11):937-948.
7. Carrera N, et al. Association study of nonsynonymous single nucleotide polymorphisms in schizophrenia. Biol Psychiatry. 2012;71(2):169-177.
8. Schizophrenia Working Group of the Psychiatric Genomics Consortium. Biological insights from 108 schizophrenia-associated genetic loci. Nature. 2014;511(7510):421-427.
9. Reference SNP (refSNP) Cluster Report: rs13107325. NCBI. https://www.ncbi.nlm.nih. gov/projects/SNP/snp
10. Zhang R, et al. A blood pressure-associated variant of the SLC39A8 gene influences cellular cadmium accumulation and toxicity. Hum Mol Genet. 2016;25(18):4117-4126.
11. Marger L, Bertrand D, Singec I, Xi HS, Wendland JR, Schubert CR. Functional characterization of ZiP8, a zinc transporter with potential relevance for neuropsychiatric disorders. HiQScreen. http://www.hiqscreen.com/Posters/Poster Zip8%20CRS.pdf. Accessed March 24, 2017.
12. Begum NA, Kobayashi M, Moriwaki Y, Matsumoto M, Toyoshima K, Seya T. Mycobacterium bovis BCG cell wall and lipopolysaccharide induce a novel gene, BIGM103, encoding a 7-TM protein: identification of a new protein family having Zn-transporter and Zn-metalloprotease signatures. Genomics. 2002;80(6):630-645.
13. He L, et al. ZIP8, member of the solute-carrier-39 (SLC39) metal-transporter family: characterization of transporter properties. Mol Pharmacol. 2006;70(1):171-180.
14. Wang CY, et al. ZIP8 is an iron and zinc transporter whose cell-surface expression is upregulated by cellular iron loading. J Biol Chem. 2012;287(41):34032-34043.
15. Gálvez-Peralta M, et al. ZIP8 zinc transporter: indispensable role for both multiple-organ organogenesis and hematopoiesis in utero. PLoS One. 2012;7(5):e36055.
16. Boycott KM, et al. Autosomal-Recessive Intellectual Disability with Cerebellar Atrophy Syndrome Caused by Mutation of the Manganese and Zinc Transporter Gene SLC39A8. Am J Hum Genet. 2015;97(6):886-893.
17. Park JH, et al. SLC39A8 Deficiency: A Disorder of Manganese Transport and Glycosylation. Am J Hum Genet. 2015;97(6):894-903.
18. Riley LG, et al. A SLC39A8 variant causes manganese deficiency, and glycosylation and mitochondrial disorders. J Inherit Metab Dis. 2017;40(2):261-269.
19. Scott K, Gadomski T, Kozicz T, Morava E. Congenital disorders of glycosylation: new defects and still counting. J Inherit Metab Dis. 2014;37(4):609-617.
20. Wedler FC. Biochemical and nutritional role of manganese: an overview. In: Klimis-Tavntzis DJ, ed. Manganese in health and disease. Boca Raton, FL: CRC Press, Inc. 1994;1-37.
21. Kanyo ZF, Scolnick LR, Ash DE, Christianson DW. Structure of a unique binuclear manganese cluster in arginase. Nature. 1996;383(6600):554-557.
22. Ramakrishnan B, Ramasamy V, Qasba PK. Structural snapshots of beta-1, 4-galactosyltransferase-I along the kinetic pathway. J Mol Biol. 2006;357(5):1619-1633.
23. Keen CL, et al. Nutritional aspects of manganese from experimental studies. Neurotoxicology. 1999;20(2-3):213-223.
24. Chua AC, Morgan EH. Manganese metabolism is impaired in the Belgrade laboratory rat. J Comp Physiol B, Biochem Syst Environ Physiol. 1997;167(5):361-369.
25. Chen P, Parmalee N, Aschner M. Genetic factors and manganese-induced neurotoxicity. Front Genet. 2014;5:265.
26. Quadri M, et al. Mutations in SLC30A10 cause parkinsonism and dystonia with hypermanganesemia, polycythemia, and chronic liver disease. Am J Hum Genet. 2012;90(3):467-477.
27. Roth JA. Homeostatic and toxic mechanisms regulating manganese uptake, retention, and elimination. Biol Res. 2006;39(1):45-57.
28. Fujishiro H, Yano Y, Takada Y, Tanihara M, Himeno S. Roles of ZIP8, ZIP14, and DMT1 in transport of cadmium and manganese in mouse kidney proximal tubule cells. Metallomics. 2012;4(7):700-708.
29. Davis CD, Zech L, Greger JL. Manganese metabolism in rats: an improved methodology for assessing gut endogenous losses. Proc Soc Exp Biol Med. 1993;202(1):103-108.
30. Aschner JL, Aschner M. Nutritional aspects of manganese homeostasis. Mol Aspects Med. 2005;26(4-5):353-362.
31. Ramakrishnan B, Boeggeman E, Ramasamy V, Qasba PK. Structure and catalytic cycle of beta-1, 4-galactosyltransferase. Curr Opin Struct Biol. 2004;14(5):593-600.
32. Potelle S, et al. Glycosylation abnormalities in Gdt1p/TMEM165 deficient cells result from a defect in Golgi manganese homeostasis. Hum Mol Genet. 2016;25(8):1489-1500.
33. Bendiak B, Schachter H. Control of glycoprotein synthesis. Kinetic mechanism, substrate specificity, and inhibition characteristics of UDPN- acetylglucosamine:alpha-D-mannoside beta 1-2 N-acetylglucosaminyltransferase II from rat liver. J Biol Chem. 1987;262(12):5784-5790.
34. Shawki A, et al. Intestinal DMT1 is critical for iron absorption in the mouse but is not required for the absorption of copper or manganese. Am J Physiol Gastrointest Liver Physiol. 2015;309(8):G635-G647.
35. Nam H, et al. ZIP14 and DMT1 in the liver, pancreas, and heart are differentially regulated by iron deficiency and overload: implications for tissue iron uptake in iron-related disorders. Haematologica. 2013;98(7):1049-1057.
36. Girijashanker K, et al. Slc39a14 gene encodes ZIP14, a metal/bicarbonate symporter: similarities to the ZIP8 transporter. Mol Pharmacol. 2008;73(5):1413-1423.
37. Tuschl K, et al. Mutations in SLC39A14 disrupt manganese homeostasis and cause childhood- onset parkinsonism-dystonia. Nat Commun. 2016;7:11601.
38. Roels H, et al. Epidemiological survey among workers exposed to manganese: effects on lung, central nervous system, and some biological indices. Am J Ind Med. 1987;11(3):307-327.
39. Reimund JM, Dietemann JL, Warter JM, Baumann R, Duclos B. Factors associated to hypermanganesemia in patients receiving home parenteral nutrition. Clin Nutr. 2000;19(5):343-348.
40. Hauser RA, Zesiewicz TA, Rosemurgy AS, Martinez C, Olanow CW. Manganese intoxication and chronic liver failure. Ann Neurol. 1994;36(6):871-875.
41. Chen P, Chakraborty S, Peres TV, Bowman AB, Aschner M. Manganese-induced Neurotoxicity: From C. elegans to Humans. Toxicol Res (Camb). 2015;4(2):191-202.
42. Chicoine LG, Paffett ML, Young TL, Nelin LD. Arginase inhibition increases nitric oxide production in bovine pulmonary arterial endothelial cells. Am J Physiol Lung Cell Mol Physiol. 2004;287(1):L60-L68.
43. Shatanawi A, et al. Angiotensin II-induced vascular endothelial dysfunction through RhoA/Rho kinase/p38 mitogen-activated protein kinase/ arginase pathway. Am J Physiol, Cell Physiol. 2011;300(5):C1181-C1192.
44. Holowatz LA, Kenney WL. Up-regulation of arginase activity contributes to attenuated reflex cutaneous vasodilatation in hypertensive humans. J Physiol (Lond). 2007;581(Pt 2):863-872.
45. Xia B, et al. Serum N-glycan and O-glycan analysis by mass spectrometry for diagnosis of congenital disorders of glycosylation. Anal Biochem. 2013;442(2):178-185.
46. Moremen KW, Tiemeyer M, Nairn AV. Vertebrate protein glycosylation: diversity, synthesis and function. Nat Rev Mol Cell Biol. 2012;13(7):448-462.
47. Skropeta D, et al. N-Glycosylation regulates endothelial lipase-mediated phospholipid hydrolysis in apoE- and apoA-I-containing high density lipoproteins. J Lipid Res. 2007;48(9):2047-2057.
48. van den Boogert MA, et al. Genetic defects inprotein glycosylation as a cause of dyslipidemia [abstract 14741]. Circulation. 2013;128(Suppl 22): A14741.
49. Albers JJ, Day JR, Wolfbauer G, Kennedy H, Vuletic S, Cheung MC. Impact of site-specific N-glycosylation on cellular secretion, activity and specific activity of the plasma phospholipid transfer protein. Biochim Biophys Acta. 2011;1814(7):908-911.
50. Viñals M, Xu S, Vasile E, Krieger M. Identification of the N-linked glycosylation sites on the high density lipoprotein (HDL) receptor SR-BI and assessment of their effects on HDL binding and selective lipid uptake. J Biol Chem. 2003;278(7):5325-5332.
51. Singaraja RR, et al. Specific mutations in ABCA1 have discrete effects on ABCA1 function and lipid phenotypes both in vivo and in vitro. Circ Res. 2006;99(4):389-397.
52. Stout JD, Brinker DF, Driscoll CP, Davison S, Murphy LA. Serum biochemistry values, plasma mineral levels, and whole blood heavy metal measurements in wild northern goshawks (Accipiter gentilis). J Zoo Wildl Med. 2010;41(4):649-655.
53. Murty S, et al. Nanoparticles functionalized with collagenase exhibit improved tumor accumulation in a murine xenograft model. Part Part Syst Charact. 2014;31(12):1307-1312.
54. Corraliza IM, Campo ML, Soler G, Modolell M. Determination of arginase activity in macrophages: a micromethod. J Immunol Methods. 1994;174(1-2):231-235.
55. Li X, Raihan MA, Reynoso FJ, He M. Glycosylation analysis for congenital disorders of glycosylation. Curr Protoc Hum Genet. 2015;86:17.18.1-17.18.22.