Transepithelial heme-iron transport: Effect of heme oxygenase overexpression

European Journal of Nutrition

Volumn 50, Issue 5, 2011, Pages 363-371

  Mendiburo, M J ^a   Le Blanc, S ^a   Espinoza, A ^a   Pizarro, F ^a   Arredondo, M ^a  

^a UNIVERSITY OF CHILE   (Chile)

Author keywords

Caco 2 cells; Heme oxygenase; Heme Fe; Transepithelial transport

Indexed keywords

BILIVERDIN; CARBON MONOXIDE; COMPLEMENTARY DNA; FERRITIN; FERROUS ION; HEME OXYGENASE 1; HEMOGLOBIN; IRON; MYOGLOBIN;

ARTICLE; BASOLATERAL MEMBRANE; CELL MEMBRANE; CELL STRAIN CACO 2; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME LOCALIZATION; HUMAN; HUMAN CELL; IMMUNOLOCALIZATION; INTESTINE CELL; IRON ABSORPTION; IRON METABOLISM; IRON TRANSPORT; PROTEIN EXPRESSION; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION;

ANTIBODIES; BIOLOGICAL AVAILABILITY; BIOLOGICAL TRANSPORT; BLOTTING, WESTERN; CACO-2 CELLS; FERRITINS; GENE EXPRESSION REGULATION; HEME; HEME OXYGENASE-1; HEMOGLOBINS; HUMANS; INTESTINES; IRON; OXIDOREDUCTASES ACTING ON CH-CH GROUP DONORS;

EID: 80053614430     PISSN: 14366207     EISSN: 14366215     Source Type: Journal    
DOI: 10.1007/s00394-010-0144-5     Document Type: Article

References (42)

1. Agarwal A, Shiraishi F, Visner GA, Nick HS (1998) Linoleyl hydroperoxide transcriptionally upregulates heme oxygenase-1 gene expression in human renal epithelial and aortic endothelial cells. J Am Soc Nephrol 9:1990-1997 (Pubitemid 28482146)
2. Arredondo M, Orellana A, Núñez MT (1997) Intracellular iron regulates iron regulatory protein activity and iron absorption in intestinal epithelial (Caco-2) cells. Am J Physiol 273(36):G275-G280
3. Arredondo M, KIoosterman J, Núñez S, Segovia F, Candia V, Flores S, Le Blanc S, Olivares M, Pizarro P (2008) Heme iron uptake by Caco-2 cells is a saturable, temperature sensitive and modulated by extracellular pH and potassium. Biol Trace Elem Res 125:109-119
4. Beard JL, Dawson H, Pinero DJ (1996) Iron metabolism: a comprehensive review. Nutr Rev 54:295-317 (Pubitemid 27129673)
5. Camhi SL, Alam J, Otterbein L, Sylvester SL, Choi AM (1995) Induction of heme oxygenase-1 gene expression by lipopolysaccharide is mediated by AP-1 activation. Am J Respir Cell Mol Biol 130:387-398
6. Carraway MS, Ghio AJ, Taylor JL, Piantadosi CA (1998) Induction of ferritin and heme oxygenase-1 by endotoxin in the lung. Am J Physiol Lung Cell Mol Physiol 275:L583-L592
7. Carraway MS, Ghio AJ, Carter JD, Piantadosi CA (2000) Expression of heme oxygenase-1 in the lung in chronic hypoxia. Am J Respir Cell Mol Biol 278:L806-L812 (Pubitemid 30220042)
8. Cermak J, Baila J, Jacob HS, Baila G, Enright H, Nath K, Vercellotti GM (1993) Tumor cell heme uptake induces ferritin synthesis resulting in altered oxidant sensibility: possible role in chemotherapy efficacy. Cancer Res 53:5308-5313 (Pubitemid 23333404)
9. Choi AMK, Alam J (1996) Heme oxygenase-1: function, regulation, and implication of a novel stress-inducible protein in oxidant-induced lung injury. Am J Respir Cell Mol Biol 15:9-19 (Pubitemid 126439851)
10. Conrad ME, Umbreit JN (2000) Iron absorption and transport- an update. Am J Hematol 64:287-298
11. Durante W, Kroll MH, Christodoulides N, Peyton KJ, Schafer AI (1997) Nitric oxide induces heme oxygenase-1 gene expression and carbon monoxide production in vascular smooth muscle cells. Circ Res 80:557-564 (Pubitemid 27137293)
12. Eisenstein RS, Garcia-Mayolt D, Pettingellt W, Munro HM (1991) Regulation of ferritin and heme oxygenase synthesis in rat fibroblasts by different forms of iron translational control/ironregulated proteins/metabolic regulation/iron regulatory elementbinding protein/chelatable iron). Proc Nat Acad Sci USA 88:688-692
13. Ewing JF, Maines MD (1991) Rapid induction of heme oxygenase- 1 mRNA and protein by hyperthermia in rat brain: heme oxygenase 2 is not a heat shock protein. Proc Natl Acad Sci USA 88:5364-5368 (Pubitemid 21914745)
14. Eyssen-Hernandez R, Ladoux A, Frelin C (1996) Differential regulation of cardiac heme oxygenase-1 and vascular endothelial growth factor mRNA expressions by hemin, heavy metals, heat shock and anoxia. FEBS Lett 382:229-233 (Pubitemid 26091437)
15. Fogg S, Agarwal A, Nick HS, Visner GA (1999) Iron regulates hyperoxia-dependent human heme oxygenase-1 gene expression in pulmonary endothelial cells. Am J Respir Cell Mol Biol 20:797-804 (Pubitemid 129495668)
16. Grasbeck R, Majuri R, Kouvonen I, Tenhunen R (1982) Spectral and other studies on the intestinal haem receptor of the pig. Biochem Biophys Acta 700:137-142
17. Hayashi S, Omata Y, Sakamoto H, Higashimoto Y, Hara T, Sagara Y, Noguchi M (2004) Characterization of rat heme oxygenase- 3 gene Implication of processed pseudogenes derived from heme oxygenase-2 gene. Gene 336(2):241-250 (Pubitemid 38891741)
18. Keel SB, Doty RT, Yang Z, Quigley JG, Chen J, Knoblaugh S, Kingsley PD, De Domenico I, Vaughn MB, Kaplan J, Palis J, Abkowitz JL (2008)Aheme export protein is required for red blood cell differentiation and iron homeostasis. Science 319:825-828 (Pubitemid 351225875)
19. Keyse SM, Tyrrell RM (1987) Both near ultraviolet radiation and the oxidizing agent hydrogen peroxide induce a 32-kDa stress protein in normal human skin fibroblasts. J Biol Chem 262:14821-14825 (Pubitemid 17157372)
20. Kim HP, Wang X, Galbiati F, Ryter SW, Choi AM (2004) Caveolae compartmentalization of heme oxygenase-1 in endothelial cells. FASEB J 18:1080-1089 (Pubitemid 38859216)
21. Krishnamurthy P, Xie T, Schuetz JD (2007) The role of transporters in cellular heme and porphyrin homeostasis. Pharmacol Ther 114:345-358 (Pubitemid 46843250)
22. Latunde-Dada GO, Simpson RJ, McKie AT (2006) Recent advances in mammalian haem transport. Trends Biochem Sci 31:182-188 (Pubitemid 43357998)
23. Lautier D, Luscher P, Tyrrell RM (1992) Endogenous glutathione levels modulate both constitutive and UVA radiation/hydrogen peroxide inducible expression of the human heme oxygenase gene. Carcinogenesis 13:227-232
24. Lee PJ, Alam J, Wiegand GW, Choi AM (1996) Overexpression of heme oxygenase-1 expression in human pulmonary epithelial cells results in cell growth arrest and increased resistance to hyperoxia. Proc Natl Acad Sci USA 93:10393-10398 (Pubitemid 26314633)
25. Lee PJ, Jiang BH, Chin BY, Iyer NV, Alam J, Semenza GL, Choi AM (1997) Hypoxia-inducible factor-1 mediates transcriptional activation of the heme oxygenase-1 gene in response to hypoxia. J Biol Chem 272:5375-5381 (Pubitemid 27102353)
26. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265-275
27. Mendiburo MJ, Flores S, Pizarro F, Arredondo M (2006) Heme oxygenase-1 overexpression increases iron fluxes in Caco-2 cells. Biol Res 39:195-197 (Pubitemid 44027662)
28. Morse D, Choi MAK (2002) Heme oxygenase-1 the "emerging molecule" has arrived. Am J Respir Cell Mol Biol 27:8-16 (Pubitemid 34657385)
29. Parmley RT, Barton JC, Conrad ME, Austin RL, Holland RM (1981) Ultraestructural cytochemistry and radioautography of hemoglobin-iron absorption. Exp Mol Pathol 34:131-134
30. Philpott CC (2002) Molecular aspects of iron absorption: insights into the role of HFE in hemochromatosis. Hepatology 35:993-1001 (Pubitemid 34453996)
31. Pizarro F, Olivares M, Hertrampf E, Mazariegos DI, Arredondo M (2003) Heme-iron absorption is saturable by heme-iron dose in women. J Nutr 133:2214-2217 (Pubitemid 36841542)
32. Quigley JG, Yang Z, Worthington MT, Phillips JD, Sabo KM, Sabath DE, Berg CL, Sassa S, Wood BL, Abkowitz JL (2004) Identification of a human heme exporter that is essential for erythropoiesis. Cell 118:757-766 (Pubitemid 39221734)
33. Raffin SB, Woo CH, Roost KT, Price DC, Schmid R (1974) Intestinal absorption of hemoglobin heme iron cleavage by mucosal heme oxygenase. J Clin Invest 54:1344-1352
34. Roy CN, Enns CA (2000) Iron homeostasis: new tales from the crypt. Blood 96:4020-4027
35. Stocker R (1990) Induction of heme oxygenase as a defense against oxidative stress. Free Radic Res Commun 9:101-112 (Pubitemid 20177138)
36. Sun Y, Rotenberg MO, Maines MD (1990) Developmental expression of heme oxygenase isozymes in rat brain. Two HO-2 mRNAs are detected. J Biol Chem 265:8212-8217
37. Takeda A, Perry G, Abraham NG, Dwyer BE, Kuttyi RK, Laitinen JT, Petersen RB, Smith MA (2000) Overexpression of heme oxygenase in neuronal cells, the possible interaction with tau. J Biol Chem 275:5395-5399 (Pubitemid 30115170)
38. Tapia N, Arredondo M, Núñez MT (1996) Regulation of Fe absorption by cultured intestinal epithelia (Caco-2) cell monolayers with varied Fe status. Am J Physiol 1271:G443-G447
39. Trakshel GM, Kutty RK, Maines MD (1986) Purification and characterization of the major constitutive form of testicular heme oxygenase. The noninducible isoform. J Biol Chem 261:11131-11137 (Pubitemid 17216715)
40. Weintraub LR, Weinstein MB, Huser HJ, Rafal S (1968) Absorption of hemoglobin iron: the role of a heme-splitting substance in the intestinal mucosa. J Clin Invest 47:531-539
41. Wheby MS, Spyker DA (1981) Hemoglobin iron absorption kinetics in the iron-deficient dog. Am J Clin Nutr 34:1686-1693 (Pubitemid 12245262)
42. Wyllie JC, Kaufman MD (1982) An electron microscopy study of heme uptake by rat duodenum. Lab Invest 47:471-476 (Pubitemid 13229685)