Endocytic pathway of exogenous iron-loaded ferritin in intestinal epithelial (Caco-2) cells

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 304, Issue 7, 2013, Pages

  Antileo, Elmer ^a   Garri, Carolina ^a   Tapia, Victoria ^a   Muñoz, Juan Pablo ^b   Chiong, Mario ^a   Nualart, Francisco ^c   Lavandero, Sergio ^a,d   Fernández, Juan ^a   Núñez, Marco T ^a,e  

^a UNIVERSITY OF CHILE   (Chile)

^b UNIVERSITY OF BARCELONA   (Spain)

^c UNIVERSITY OF CONCEPCIÓN   (Chile)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^e Centre for Biochemical Engineering and Biotechnology   (Chile)

Author keywords

Endocytosis; Ferritin; Intestinal iron absorption

Indexed keywords

3 METHYLADENINE; CHLOROQUINE; CLATHRIN; EARLY ENDOSOME ANTIGEN 1; FERRITIN; IODINE 131; IRON; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 2; MICROTUBULE ASSOCIATED PROTEIN 1; 3-METHYLADENINE; ADENINE; DRUG DERIVATIVE; VESICULAR TRANSPORT PROTEIN;

ARTICLE; AUTOLYSOSOME; AUTOPHAGOSOME; CELL MEMBRANE; CELL STRAIN CACO 2; CONFOCAL LASER MICROSCOPY; CYTOSOL; ENDOCYTOSIS; ENDOSOME; HUMAN; HUMAN CELL; INTESTINE EPITHELIUM; IRON TRANSPORT; PRIORITY JOURNAL; TRANSMISSION ELECTRON MICROSCOPY; AUTOPHAGY; COATED PIT; CONFOCAL MICROSCOPY; FLUORESCENCE MICROSCOPY; INTESTINE MUCOSA; LYSOSOME; METABOLISM;

ADENINE; AUTOPHAGY; CACO-2 CELLS; COATED PITS, CELL-MEMBRANE; ENDOCYTOSIS; FERRITINS; HUMANS; INTESTINAL MUCOSA; IRON; LYSOSOMES; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION; MICROSCOPY, FLUORESCENCE; VESICULAR TRANSPORT PROTEINS;

MLCS; MLOWN;

EID: 84878140196     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00472.2012     Document Type: Article

References (57)

1. Adams PC, Powell LW, Halliday JW. Isolation of a human hepatic ferritin receptor. Hepatology 8: 719-721, 1988.
2. Ainsworth SK, Karnovsky MJ. An ultrastructural staining method for enhancing the size and electron opacity of ferritin in thin sections. J Histochem Cytochem 20: 225-229, 1972.
3. Asano M, Komiyama K. Polymeric immunoglobulin receptor. J Oral Sci 53: 147-156, 2011.
4. Blommaart EF, Krause U, Schellens JP, Vreeling-Sindelarova H, Meijer AJ. The phosphatidylinositol 3-kinase inhibitors wortmannin and LY294002 inhibit autophagy in isolated rat hepatocytes. Eur J Biochem 243: 240-246, 1997.
5. Chen TT, Li L, Chung DH, Allen CD, Torti SV, Torti FM, Cyster JG, Chen CY, Brodsky FM, Niemi EC, Nakamura MC, Seaman WE, Daws MR. TIM-2 is expressed on B cells and in liver and kidney and is a receptor for H-ferritin endocytosis. J Exp Med 202: 955-965, 2005.
6. Fernandez J, Valladares M, Fuentes R, Ubilla A. Reorganization of cytoplasm in the zebrafish oocyte and egg during early steps of ooplasmic segregation. Dev Dyn 235: 656-671, 2006.
7. Fisher J, Devraj K, Ingram J, Slagle-Webb B, Madhankumar AB, Liu X, Klinger M, Simpson IA, Connor JR. Ferritin: a novel mechanism for delivery of iron to the brain and other organs. Am J Physiol Cell Physiol 293: C641-C649, 2007.
8. Florey O, Overholtzer M. Autophagy proteins in macroendocytic engulfment. Trends Cell Biol 22: 374-380, 2012.
9. Glick D, Barth S, Macleod KF. Autophagy: cellular and molecular mechanisms. J Pathol 221: 3-12, 2010.
10. Goldstein JL, Brown MS. Binding and degradation of low density lipoproteins by cultured human fibroblasts. Comparison of cells from a normal subject and from a patient with homozygous familial hypercholesterolemia. J Biol Chem 249: 5153-5162, 1974.
11. Han J, Seaman WE, Di X, Wang W, Willingham M, Torti FM, Torti SV. Iron uptake mediated by binding of H-ferritin to the TIM-2 receptor in mouse cells. PLoS One 6: e23800, 2011.
12. Harrison PM, Arosio P. The ferritins: molecular properties, iron storage function and cellular regulation. Biochim Biophys Acta 1275: 161-203, 1996.
13. Hultcrantz R, Glaumann H. Intracellular fate of ferritin in HeLa cells following microinjection. Exp Cell Res 171: 203-212, 1987.
14. Hurrell R, Egli I. Iron bioavailability and dietary reference values. Am J Clin Nutr 91: 1461S-1467S, 2010.
15. Iancu TC. Ultrastructural aspects of iron storage, transport and metabolism. J Neural Transm 118: 329-335, 2011.
16. Jia L, Betters JL, Yu L. Niemann-pick C1-like 1 (NPC1L1) protein in intestinal and hepatic cholesterol transport. Annu Rev Physiol 73: 239-259, 2011.
17. Jiang Y, Oliver P, Davies KE, Platt N. Identification and characterization of murine SCARA5, a novel class A scavenger receptor that is expressed by populations of epithelial cells. J Biol Chem 281: 11834-11845, 2006.
18. Kalgaonkar S, Lonnerdal B. Receptor-mediated uptake of ferritin-bound iron by human intestinal Caco-2 cells. J Nutr Biochem 20: 304-311, 2009.
19. Karnovsky M. A formaldehyde-glutaraldehyde fixative of high osmomolarity for use in electron microscopy (Abstract). J Cell Biol 27: 137A, 1965.
20. Knight A, Hughson E, Hopkins CR, Cutler DF. Membrane protein trafficking through the common apical endosome compartment of polarized Caco-2 cells. Mol Biol Cell 6: 597-610, 1995.
21. Kolachala VL, Sesikeran B, Nair KM. Evidence for a sequential transfer of iron amongst ferritin, transferrin and transferrin receptor during duodenal absorption of iron in rat and human. World J Gastroenterol 13: 1042-1052, 2007.
22. Laftah AH, Latunde-Dada GO, Fakih S, Hider RC, Simpson RJ, McKie AT. Haem and folate transport by proton-coupled folate transporter/ haem carrier protein 1 (SLC46A1). Br J Nutr 101: 1150-1156, 2009.
23. Le Brun NE, Crow A, Murphy ME, Mauk AG, Moore GR. Iron core mineralisation in prokaryotic ferritins. Biochim Biophys Acta 1800: 732-744, 2010.
24. Li JY, Paragas N, Ned RM, Qiu A, Viltard M, Leete T, Drexler IR, Chen X, Sanna-Cherchi S, Mohammed F, Williams D, Lin CS, Schmidt-Ott KM, Andrews NC, Barasch J. Scara5 is a ferritin receptor mediating non-transferrin iron delivery. Dev Cell 16: 35-46, 2009.
25. Li L, Fang CJ, Ryan JC, Niemi EC, Lebron JA, Bjorkman PJ, Arase H, Torti FM, Torti SV, Nakamura MC, Seaman WE. Binding and uptake of H-ferritin are mediated by human transferrin receptor-1. Proc Natl Acad Sci USA 107: 3505-3510, 2010.
26. Lonnerdal B, Bryant A, Liu X, Theil EC. Iron absorption from soybean ferritin in nonanemic women. Am J Clin Nutr 83: 103-107, 2006.
27. Luzio JP, Parkinson MD, Gray SR, Bright NA. The delivery of endocytosed cargo to lysosomes. Biochem Soc Trans 37: 1019-1021, 2009.
28. Macara IG, Hoy TG, Harrison PM. The formation of ferritin from apoferritin. Inhibition and metal ion-binding studies. Biochem J 135: 785-789, 1973.
29. Majeski AE, Dice JF. Mechanisms of chaperone-mediated autophagy. Int J Biochem Cell Biol 36: 2435-2444, 2004.
30. Mann S, Williams JM, Treffry A, Harrison PM. Reconstituted and native iron-cores of bacterioferritin and ferritin. J Mol Biol 198: 405-416, 1987.
31. Massey A, Kiffin R, Cuervo AM. Pathophysiology of chaperone-mediated autophagy. Int J Biochem Cell Biol 36: 2420-2434, 2004.
32. Mehrpour M, Esclatine A, Beau I, Codogno P. Autophagy in health and disease. I. Regulation and significance of autophagy: an overview. Am J Physiol Cell Physiol 298: C776-C785, 2010.
33. Mizushima N. Methods for monitoring autophagy. Int J Biochem Cell Biol 36: 2491-2502, 2004.
34. Mortimore GE, Poso AR. Intracellular protein catabolism and its control during nutrient deprivation and supply. Annu Rev Nutr 7: 539-564, 1987.
35. Moss D, Fargion S, Fracanzani AL, Levi S, Cappellini MD, Arosio P, Powell LW, Halliday JW. Functional roles of the ferritin receptors of human liver, hepatoma, lymphoid and erythroid cells. J Inorg Biochem 47: 219-227, 1992.
36. Núñez MT. Regulatory mechanisms of intestinal iron absorption-uncovering of a fast-response mechanism based on DMT1 and ferroportin endocytosis. Biofactors 36: 88-97, 2010.
37. Núñez MT, Tapia V, Arredondo M. Intestinal epithelia (Caco-2) cells acquire iron through the basolateral endocytosis of transferrin. J Nutr 126: 2151-2158, 1996.
38. Petiot A, Ogier-Denis E, Blommaart EF, Meijer AJ, Codogno P. Distinct classes of phosphatidylinositol 3=-kinases are involved in signaling pathways that control macroautophagy in HT-29 cells. J Biol Chem 275: 992-998, 2000.
39. Ponka P, Beaumont C, Richardson DR. Function and regulation of transferrin and ferritin. Semin Hematol 35: 35-54, 1998.
40. Qiu A, Jansen M, Sakaris A, Min SH, Chattopadhyay S, Tsai E, Sandoval C, Zhao R, Akabas MH, Goldman ID. Identification of an intestinal folate transporter and the molecular basis for hereditary folate malabsorption. Cell 127: 917-928, 2006.
41. Ramm GA, Britton RS, O'Neill R, Bacon BR. Identification and characterization of a receptor for tissue ferritin on activated rat lipocytes. J Clin Invest 94: 9-15, 1994.
42. Richter GW. A study of hemosiderosis with the aid of electron microscopy; with observations on the relationship between hemosiderin and ferritin. J Exp Med 106: 203-218, 1957.
43. Rodriguez-Boulan E, Kreitzer G, Musch A. Organization of vesicular trafficking in epithelia. Nat Rev Mol Cell Biol 6: 233-247, 2005.
44. Rodriguez-Manzanet R, DeKruyff R, Kuchroo VK, Umetsu DT. The costimulatory role of TIM molecules. Immunol Rev 229: 259-270, 2009.
45. San Martin CD, Garri C, Pizarro F, Walter T, Theil EC, Núñez MT. Caco-2 intestinal epithelial cells absorb soybean ferritin by mu2 (AP2)-dependent endocytosis. J Nutr 138: 659-666, 2008.
46. Shayeghi M, Latunde-Dada GO, Oakhill JS, Laftah AH, Takeuchi K, Halliday N, Khan Y, Warley A, McCann FE, Hider RC, Frazer DM, Anderson GJ, Vulpe CD, Simpson RJ, McKie AT. Identification of an intestinal heme transporter. Cell 122: 789-801, 2005.
47. Stromhaug PE, Berg TO, Fengsrud M, Seglen PO. Purification and characterization of autophagosomes from rat hepatocytes. Biochem J 335: 217-224, 1998.
48. Takami M, Mizumoto K, Kasuya I, Kino K, Sussman HH, Tsunoo H. Human placental ferritin receptor. Biochim Biophys Acta 884: 31-38, 1986.
49. Takatsuka C, Inoue Y, Matsuoka K, Moriyasu Y. 3-methyladenine inhibits autophagy in tobacco culture cells under sucrose starvation conditions. Plant Cell Physiol 45: 265-274, 2004.
50. Tanida I, Ueno T, Kominami E. LC3 conjugation system in mammalian autophagy. Int J Biochem Cell Biol 36: 2503-2518, 2004.
51. Tapia V, Arredondo M, Núñez MT. Regulation of Fe absorption by cultured intestinal epithelia (Caco-2) cell monolayers with varied Fe status. Am J Physiol Gastrointest Liver Physiol 271: G443-G447, 1996.
52. Theil EC. Ferritin protein nanocages use ion channels, catalytic sites, and nucleation channels to manage iron/oxygen chemistry. Curr Opin Chem Biol 15: 304-311, 2011.
53. Theil EC. Iron, ferritin, nutrition. Annu Rev Nutr 24: 327-343, 2004.
54. Theil EC, Chen H, Miranda C, Janser H, Elsenhans B, Núñez MT, Pizarro F, Schumann K. Absorption of iron from ferritin is independent of heme iron and ferrous salts in women and rat intestinal segments. J Nutr 142: 478-483, 2012.
55. Todorich B, Zhang X, Slagle-Webb B, Seaman WE, Connor JR. Tim-2 is the receptor for H-ferritin on oligodendrocytes. J Neurochem 107: 1495-1505, 2008.
56. Vincent RA Jr, Spicer SS. Giant dense bodies in fibroblasts cultured from beige mice with the Chediak-Higashi syndrome. Am J Pathol 105: 270-278, 1981.
57. Wibo M, Poole B. Protein degradation in cultured cells. II. The uptake of chloroquine by rat fibroblasts and the inhibition of cellular protein degradation and cathepsin B1. J Cell Biol 63: 430-440, 1974.