Global transcriptional response to Hfe deficiency and dietary iron overload in mouse liver and duodenum

PLoS ONE

Volumn 4, Issue 9, 2009, Pages

  Rodriguez, Alejandra ^a   Luukkaala, Tiina ^b   Fleming, Robert E ^c,d   Britton, Robert S ^c,d   Bacon, Bruce R ^c,d   Parkkila, Seppo ^a,e  

^a UNIVERSITY OF TAMPERE   (Finland)

^b UNIVERSITY OF TAMPERE   (Finland)

^c SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d Saint Louis University   (United States)

^e TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

ACUTE PHASE PROTEIN; HFE PROTEIN; INTESTINE ENZYME; IRON; TRANSCRIPTOME; ANTIMICROBIAL CATIONIC PEPTIDE; HEPCIDIN; HFE PROTEIN, MOUSE; HLA ANTIGEN CLASS 1; MEMBRANE PROTEIN;

ANALYTICAL EQUIPMENT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DUODENUM; ENZYME INDUCTION; GENE OVEREXPRESSION; GENETIC DIFFERENCE; GENETIC TRANSCRIPTION; GENOTYPE; IRON OVERLOAD; LIVER; MALE; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PROTEIN DEFICIENCY; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UNINDEXED SEQUENCE; ANIMAL; ANIMAL FOOD; C57BL MOUSE; DNA MICROARRAY; GENETIC ASSOCIATION; GENETICS; HUMAN; METABOLISM; TRANSGENIC MOUSE;

MURINAE; MUS;

ANIMAL FEED; ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; DUODENUM; GENOME-WIDE ASSOCIATION STUDY; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; IRON OVERLOAD; LIVER; MALE; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OXIDATIVE STRESS; TRANSCRIPTION, GENETIC;

EID: 70349644493     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0007212     Document Type: Article

References (47)

1. Britton RS (1996) Metal-induced hepatotoxicity. Semin Liver Dis 16: 3-12.
2. Parkkila S, Niemela O, Britton RS, Fleming RE, Waheed A, et al. (2001) Molecular aspects of iron absorption and HFE expression. Gastroenterology 121: 1489-1496.
3. Feder JN, Gnirke A, Thomas W, Tsuchihashi Z, Ruddy DA, et al. (1996) A novel MHC class I-like gene is mutated in patients with hereditary haemochromatosis. Nat Genet 13: 399-408.
4. Fleming RE, Britton RS, Waheed A, Sly WS, Bacon BR (2005) Pathophysiology of hereditary hemochromatosis. Semin Liver Dis 25: 411-419.
5. Papanikolaou G, Samuels ME, Ludwig EH, MacDonald ML, Franchini PL, et al. (2004) Mutations in HFE2 cause iron overload in chromosome 1q-linked juvenile hemochromatosis. Nat Genet 36: 77-82.
6. Nemeth E, Ganz T (2006) Regulation of iron metabolism by hepcidin. Annu Rev Nutr 26: 323-342.
7. Abboud S, Haile DJ (2000) A novel mammalian iron-regulated protein involved in intracellular iron metabolism. J Biol Chem 275: 19906-19912.
8. McKie AT, Marciani P, Rolfs A, Brennan K, Wehr K, et al. (2000) A novel duodenal iron-regulated transporter, IREG1, implicated in the basolateral transfer of iron to the circulation. Mol Cell 5: 299-309.
9. Gunshin H, Mackenzie B, Berger UV, Gunshin Y, Romero MF, et al. (1997) Cloning and characterization of a mammalian proton-coupled metal-ion transporter. Nature 388: 482-488.
10. Nemeth E, Tuttle MS, Powelson J, Vaughn MB, Donovan A, et al. (2004) Hepcidin regulates cellular iron efflux by binding to ferroportin and inducing its internalization. Science 306: 2090-2093.
11. Nicolas G, Chauvet C, Viatte L, Danan JL, Bigard X, et al. (2002) The gene encoding the iron regulatory peptide hepcidin is regulated by anemia, hypoxia, and inflammation. J Clin Invest 110: 1037-1044.
12. Pigeon C, Ilyin G, Courselaud B, Leroyer P, Turlin B, et al. (2001) A new mouse liver-specific gene, encoding a protein homologous to human antimicrobial peptide hepcidin, is overexpressed during iron overload. J Biol Chem 276: 7811-7819.
13. Zhou XY, Tomatsu S, Fleming RE, Parkkila S, Waheed A, et al. (1998) HFE gene knockout produces mouse model of hereditary hemochromatosis. Proc Natl Acad Sci U S A 95: 2492-2497.
14. Ramm GA (2000) Animal models of iron overload based on excess exogenous iron. In: Barton JC, Edwards CQ, eds. Hemochromatosis: Genetics, Pathophysiology, Diagnosis and Treatment. New York: Cambridge University Press. pp 494-507.
15. Bridle KR, Frazer DM, Wilkins SJ, Dixon JL, Purdie DM, et al. (2003) Disrupted hepcidin regulation in HFE-associated haemochromatosis and the liver as a regulator of body iron homoeostasis. Lancet 361: 669-673.
16. Ahmad KA, Ahmann JR, Migas MC, Waheed A, Britton RS, et al. (2002) Decreased liver hepcidin expression in the Hfe knockout mouse. Blood Cells Mol Dis 29: 361-366.
17. Coppin H, Darnaud V, Kautz L, Meynard D, Aubry M, et al. (2007) Gene expression profiling of Hfe-/- liver and duodenum in mouse strains with differing susceptibilities to iron loading: identification of transcriptional regulatory targets of Hfe and potential hemochromatosis modifiers. Genome Biol 8: R221.
18. Morey JS, Ryan JC, Van Dolah FM (2006) Microarray validation: factors influencing correlation between oligonucleotide microarrays and real-time PCR. Biol Proced Online 8: 175-193.
19. Muckenthaler M, Roy CN, Custodio AO, Minana B, deGraaf J, et al. (2003) Regulatory defects in liver and intestine implicate abnormal hepcidin and Cybrd1 expression in mouse hemochromatosis. Nat Genet 34: 102-107.
20. Abgueguen E, Toutain B, Bedrine H, Chicault C, Orhant M, et al. (2006) Differential expression of genes related to HFE and iron status in mouse duodenal epithelium. Mamm Genome 17: 430-450.
21. Goetz DH, Holmes MA, Borregaard N, Bluhm ME, Raymond KN, et al. (2002) The neutrophil lipocalin NGAL is a bacteriostatic agent that interferes with siderophore-mediated iron acquisition. Mol Cell 10: 1033-1043.
22. Yang J, Mori K, Li JY, Barasch J (2003) Iron, lipocalin, and kidney epithelia. Am J Physiol Renal Physiol 285: F9-18.
23. Devireddy LR, Gazin C, Zhu X, Green MR (2005) A cell-surface receptor for lipocalin 24p3 selectively mediates apoptosis and iron uptake. Cell 123: 1293-1305.
24. Mori K, Lee HT, Rapoport D, Drexler IR, Foster K, et al. (2005) Endocytic delivery of lipocalin-siderophore-iron complex rescues the kidney from ischemia-reperfusion injury. J Clin Invest 115: 610-621.
25. Yan QW, Yang Q, Mody N, Graham TE, Hsu CH, et al. (2007) The adipokine lipocalin 2 is regulated by obesity and promotes insulin resistance. Diabetes 56: 2533-2540.
26. Ilyin G, Courselaud B, Troadec MB, Pigeon C, Alizadeh M, et al. (2003) Comparative analysis of mouse hepcidin 1 and 2 genes: evidence for different patterns of expression and co-inducibility during iron overload. FEBS Lett 542: 22-26.
27. Rodriguez A, Hilvo M, Kytomaki L, Fleming RE, Britton RS, et al. (2007) Effects of iron loading on muscle: genome-wide mRNA expression profiling in the mouse. BMC Genomics 8: 379.
28. Norton JD (2000) ID helix-loop-helix proteins in cell growth, differentiation and tumorigenesis. J Cell Sci 113 (Pt 22): 3897-3905.
29. Damdinsuren B, Nagano H, Kondo M, Yamamoto H, Hiraoka N, et al. (2005) Expression of Id proteins in human hepatocellular carcinoma: relevance to tumor dedifferentiation. Int J Oncol 26: 319-327.
30. Kautz L, Meynard D, Monnier A, Darnaud V, Bouvet R, et al. (2008) Iron regulates phosphorylation of Smad1/5/8 and gene expression of Bmp6, Smad7, Id1, and Atoh8 in the mouse liver. Blood 112: 1503-1509.
31. Andriopoulos B Jr, Corradini E, Xia Y, Faasse SA, Chen S, et al. (2009) BMP6 is a key endogenous regulator of hepcidin expression and iron metabolism. Nat Genet 41: 482-487.
32. Brown KE, Broadhurst KA, Mathahs MM, Weydert J (2007) Differential expression of stress-inducible proteins in chronic hepatic iron overload. Toxicol Appl Pharmacol 223: 180-186.
33. Shayeghi M, Latunde-Dada GO, Oakhill JS, Laftah AH, Takeuchi K, et al (2005) Identification of an intestinal heme transporter. Cell 122: 789-801.
34. Qiu A, Jansen M, Sakaris A, Min SH, Chattopadhyay S, et al. (2006) Identification of an intestinal folate transporter and the molecular basis for hereditary folate malabsorption. Cell 127: 917-928.
35. Fleming RE, Sly WS (2002) Mechanisms of iron accumulation in hereditary hemochromatosis. Annu Rev Physiol 64: 663-680.
36. Trinder D, Olynyk JK, Sly WS, Morgan EH (2002) Iron uptake from plasma transferrin by the duodenum is impaired in the Hfe knockout mouse. Proc Natl Acad Sci U S A 99: 5622-5626.
37. Zoller H, Pietrangelo A, Vogel W, Weiss G (1999) Duodenal metal-transporter (DMT-1, NRAMP-2) expression in patients with hereditary haemochromatosis. Lancet 353: 2120-2123.
38. Fleming RE, Migas MC, Zhou X, Jiang J, Britton RS, et al. (1999) Mechanism of increased iron absorption in murine model of hereditary hemochromatosis: increased duodenal expression of the iron transporter DMT1. Proc Natl Acad Sci U S A 96: 3143-3148.
39. Owen D, Kuhn LC (1987) Noncoding 3′ sequences of the transferrin receptor gene are required for mRNA regulation by iron. Embo J 6: 1287-1293.
40. Dupic F, Fruchon S, Bensaid M, Loreal O, Brissot P, et al. (2002) Duodenal mRNA expression of iron related genes in response to iron loading and iron deficiency in four strains of mice. Gut 51: 648-653.
41. Edgar R, Domrachev M, Lash AE (2002) Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30: 207-210.
42. GEO. Gene Expression Omnibus. http://www.ncbi.nlm.nih.gov/geo/.
43. The DAVID Bioinformatic Resources. http://david.abcc.ncifcrf.gov.
44. Dennis G Jr, Sherman BT, Hosack DA, Yang J, Gao W, et al. (2003) DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol 4: P3.
45. Primer3. http://frodo.wi.mit.edu/.
46. BLAST. Basic Local Alignment and Search Tool. http://blast.ncbi.nlm.nih.gov/Blast.cgi.
47. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, et al. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3: RESEARCH0034.