The importance of the stem cell marker prominin-1/CD133 in the uptake of transferrin and in iron metabolism in human colon cancer caco-2 cells

PLoS ONE

Volumn 6, Issue 9, 2011, Pages

  Bourseau Guilmain, Erika ^a   Griveau, Audrey ^a   Benoit, Jean Pierre ^a   Garcion, Emmanuel ^a  

^a UNIVERSITÉ D'ANGERS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD133 ANTIGEN; ONCOPROTEIN; PROMININ 1; TRANSFERRIN; TRANSFERRIN RECEPTOR; UNCLASSIFIED DRUG; CHLORPROMAZINE; GLYCOPROTEIN; IRON; LEUKOCYTE ANTIGEN; NANOCAPSULE; PEPTIDE; SMALL INTERFERING RNA;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ARTICLE; CELL STRAIN CACO 2; COLON CANCER; CONTROLLED STUDY; DOWN REGULATION; ENDOCYTOSIS; EXOCYTOSIS; EXTRACELLULAR SPACE; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; INTERNALIZATION; IRON METABOLISM; PROTEIN BINDING; PROTEIN TRANSPORT; RNA INTERFERENCE; SEQUENCE HOMOLOGY; TRANSCRIPTION REGULATION; UPREGULATION; COLON TUMOR; DRUG EFFECT; FLOW CYTOMETRY; GENETICS; METABOLISM; TRANSPORT AT THE CELLULAR LEVEL;

ANTIGENS, CD; BIOLOGICAL TRANSPORT; CACO-2 CELLS; CHLORPROMAZINE; COLONIC NEOPLASMS; ENDOCYTOSIS; FLOW CYTOMETRY; GLYCOPROTEINS; HUMANS; IRON; NANOCAPSULES; PEPTIDES; RNA, SMALL INTERFERING; TRANSFERRIN;

EID: 80053214612     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0025515     Document Type: Article

References (88)

1. Corbeil D, Roper K, Weigmann A, Huttner WB, (1998) AC133 hematopoietic stem cell antigen: human homologue of mouse kidney prominin or distinct member of a novel protein family? Blood 91: 2625-2626.
2. Miraglia S, Godfrey W, Yin AH, Atkins K, Warnke R, et al. (1997) A novel five-transmembrane hematopoietic stem cell antigen: isolation, characterization, and molecular cloning. Blood 90: 5013-5021.
3. Weigmann A, Corbeil D, Hellwig A, Huttner WB, (1997) Prominin, a novel microvilli-specific polytopic membrane protein of the apical surface of epithelial cells, is targeted to plasmalemmal protrusions of non-epithelial cells. Proc Natl Acad Sci U S A 94: 12425-12430.
4. Shmelkov SV, Jun L, St Clair R, McGarrigle D, Derderian CA, et al. (2004) Alternative promoters regulate transcription of the gene that encodes stem cell surface protein AC133. Blood 103: 2055-2061.
5. Boivin D, Labbe D, Fontaine N, Lamy S, Beaulieu E, et al. (2009) The stem cell marker CD133 (prominin-1) is phosphorylated on cytoplasmic tyrosine-828 and tyrosine-852 by Src and Fyn tyrosine kinases. Biochemistry 48: 3998-4007.
6. Maw MA, Corbeil D, Koch J, Hellwig A, Wilson-Wheeler JC, et al. (2000) A frameshift mutation in prominin (mouse)-like 1 causes human retinal degeneration. Hum Mol Genet 9: 27-34.
7. Zacchigna S, Oh H, Wilsch-Brauninger M, Missol-Kolka E, Jaszai J, et al. (2009) Loss of the cholesterol-binding protein prominin-1/CD133 causes disk dysmorphogenesis and photoreceptor degeneration. J Neurosci 29: 2297-2308.
8. King FW, Ritner C, Liszewski W, Kwan HC, Pedersen A, et al. (2009) Subpopulations of human embryonic stem cells with distinct tissue-specific fates can be selected from pluripotent cultures. Stem Cells Dev 18: 1441-1450.
9. Ferrandina G, Petrillo M, Bonanno G, Scambia G, (2009) Targeting CD133 antigen in cancer. Expert Opin Ther Targets 13: 823-837.
10. Wu Y, Wu PY, (2009) CD133 as a marker for cancer stem cells: progresses and concerns. Stem Cells Dev 18: 1127-1134.
11. Yang C, Yang Y, Gupta N, Liu X, He A, et al. (2007) Pentaspan membrane glycoprotein, prominin-1, is involved in glucose metabolism and cytoskeleton alteration. Biochemistry (Mosc) 72: 854-862.
12. Griguer CE, Oliva CR, Gobin E, Marcorelles P, Benos DJ, et al. (2008) CD133 is a marker of bioenergetic stress in human glioma. PLoS ONE 3: e3655.
13. Corbeil D, Roper K, Fargeas CA, Joester A, Huttner WB, (2001) Prominin: a story of cholesterol, plasma membrane protrusions and human pathology. Traffic 2: 82-91.
14. Roper K, Corbeil D, Huttner WB, (2000) Retention of prominin in microvilli reveals distinct cholesterol-based lipid micro-domains in the apical plasma membrane. Nat Cell Biol 2: 582-592.
15. Taieb N, Maresca M, Guo XJ, Garmy N, Fantini J, et al. (2009) The first extracellular domain of the tumour stem cell marker CD133 contains an antigenic ganglioside-binding motif. Cancer Lett 278: 164-173.
16. Marzesco AM, Janich P, Wilsch-Brauninger M, Dubreuil V, Langenfeld K, et al. (2005) Release of extracellular membrane particles carrying the stem cell marker prominin-1 (CD133) from neural progenitors and other epithelial cells. J Cell Sci 118: 2849-2858.
17. Rothberg KG, Heuser JE, Donzell WC, Ying YS, Glenney JR, et al. (1992) Caveolin, a protein component of caveolae membrane coats. Cell 68: 673-682.
18. Singh RD, Marks DL, Holicky EL, Wheatley CL, Kaptzan T, et al. (2010) Gangliosides and beta1-integrin are required for caveolae and membrane domains. Traffic 11: 348-360.
19. Garcion E, Lamprecht A, Heurtault B, Paillard A, Aubert-Pouessel A, et al. (2006) A new generation of anticancer, drug-loaded, colloidal vectors reverses multidrug resistance in glioma and reduces tumor progression in rats. Mol Cancer Ther 5: 1710-1722.
20. Paillard A, Hindre F, Vignes-Colombeix C, Benoit JP, Garcion E, (2010) The importance of endo-lysosomal escape with lipid nanocapsules for drug subcellular bioavailability. Biomaterials 31: 7542-7554.
21. Roger E, Lagarce F, Garcion E, Benoit JP, (2009) Lipid nanocarriers improve paclitaxel transport throughout human intestinal epithelial cells by using vesicle-mediated transcytosis. J Control Release 140: 174-181.
22. Wang LH, Rothberg KG, Anderson RG, (1993) Mis-assembly of clathrin lattices on endosomes reveals a regulatory switch for coated pit formation. J Cell Biol 123: 1107-1117.
23. Orlandi PA, Fishman PH, (1998) Filipin-dependent inhibition of cholera toxin: evidence for toxin internalization and activation through caveolae-like domains. J Cell Biol 141: 905-915.
24. Liu NQ, Lossinsky AS, Popik W, Li X, Gujuluva C, et al. (2002) Human immunodeficiency virus type 1 enters brain microvascular endothelia by macropinocytosis dependent on lipid rafts and the mitogen-activated protein kinase signaling pathway. J Virol 76: 6689-6700.
25. Ohtani Y, Irie T, Uekama K, Fukunaga K, Pitha J, (1989) Differential effects of alpha-, beta- and gamma-cyclodextrins on human erythrocytes. Eur J Biochem 186: 17-22.
26. Rodal SK, Skretting G, Garred O, Vilhardt F, van Deurs B, et al. (1999) Extraction of cholesterol with methyl-beta-cyclodextrin perturbs formation of clathrin-coated endocytic vesicles. Mol Biol Cell 10: 961-974.
27. Zhang Z, Wei T, Hou J, Li G, Yu S, et al. (2003) Iron-induced oxidative damage and apoptosis in cerebellar granule cells: attenuation by tetramethylpyrazine and ferulic acid. Eur J Pharmacol 467: 41-47.
28. Zhu L, Glahn RP, Yeung CK, Miller DD, (2006) Iron uptake by Caco-2 cells from NaFeEDTA and FeSO4: Effects of ascorbic acid, pH, and a Fe(II) chelating agent. J Agric Food Chem 54: 7924-7928.
29. Mole DR, (2010) Iron homeostasis and its interaction with prolyl hydroxylases. Antioxid Redox Signal 12: 445-458.
30. Woo KJ, Lee TJ, Park JW, Kwon TK, (2006) Desferrioxamine, an iron chelator, enhances HIF-1alpha accumulation via cyclooxygenase-2 signaling pathway. Biochem Biophys Res Commun 343: 8-14.
31. Yuan Y, Hilliard G, Ferguson T, Millhorn DE, (2003) Cobalt inhibits the interaction between hypoxia-inducible factor-alpha and von Hippel-Lindau protein by direct binding to hypoxia-inducible factor-alpha. J Biol Chem 278: 15911-15916.
32. Campillos M, Cases I, Hentze MW, Sanchez M, (2010) SIREs: searching for iron-responsive elements. Nucleic Acids Res 38: W360-367.
33. Conner SD, Schmid SL, (2003) Regulated portals of entry into the cell. Nature 422: 37-44.
34. Qian ZM, Li H, Sun H, Ho K, (2002) Targeted drug delivery via the transferrin receptor-mediated endocytosis pathway. Pharmacol Rev 54: 561-587.
35. Yang Z, Vadlamudi RK, Kumar R, (2005) Dynein light chain 1 phosphorylation controls macropinocytosis. J Biol Chem 280: 654-659.
36. Torgersen ML, Skretting G, van Deurs B, Sandvig K, (2001) Internalization of cholera toxin by different endocytic mechanisms. J Cell Sci 114: 3737-3747.
37. Liu AP, Aguet F, Danuser G, Schmid SL, (2010) Local clustering of transferrin receptors promotes clathrin-coated pit initiation. J Cell Biol 191: 1381-1393.
38. Chang J, Jallouli Y, Kroubi M, Yuan XB, Feng W, et al. (2009) Characterization of endocytosis of transferrin-coated PLGA nanoparticles by the blood-brain barrier. Int J Pharm 379: 285-292.
39. Dehouck B, Fenart L, Dehouck MP, Pierce A, Torpier G, et al. (1997) A new function for the LDL receptor: transcytosis of LDL across the blood-brain barrier. J Cell Biol 138: 877-889.
40. Nabi IR, Le PU, (2003) Caveolae/raft-dependent endocytosis. J Cell Biol 161: 673-677.
41. Subtil A, Gaidarov I, Kobylarz K, Lampson MA, Keen JH, et al. (1999) Acute cholesterol depletion inhibits clathrin-coated pit budding. Proc Natl Acad Sci U S A 96: 6775-6780.
42. Garcion E, Faissner A, ffrench-Constant C, (2001) Knockout mice reveal a contribution of the extracellular matrix molecule tenascin-C to neural precursor proliferation and migration. Development 128: 2485-2496.
43. Kemper K, Sprick MR, de Bree M, Scopelliti A, Vermeulen L, et al. (2010) The AC133 epitope, but not the CD133 protein, is lost upon cancer stem cell differentiation. Cancer Res 70: 719-729.
44. Inman RS, Wessling-Resnick M, (1993) Characterization of transferrin-independent iron transport in K562 cells. Unique properties provide evidence for multiple pathways of iron uptake. J Biol Chem 268: 8521-8528.
45. Richardson DR, Ponka P, (1997) The molecular mechanisms of the metabolism and transport of iron in normal and neoplastic cells. Biochim Biophys Acta 1331: 1-40.
46. Hentze MW, Kuhn LC, (1996) Molecular control of vertebrate iron metabolism: mRNA-based regulatory circuits operated by iron, nitric oxide, and oxidative stress. Proc Natl Acad Sci U S A 93: 8175-8182.
47. Piccinelli P, Samuelsson T, (2007) Evolution of the iron-responsive element. RNA 13: 952-966.
48. Theil EC, (1994) Iron regulatory elements (IREs): a family of mRNA non-coding sequences. Biochem J 304 (Pt 1): 1-11.
49. Hentze MW, Rouault TA, Caughman SW, Dancis A, Harford JB, et al. (1987) A cis-acting element is necessary and sufficient for translational regulation of human ferritin expression in response to iron. Proc Natl Acad Sci U S A 84: 6730-6734.
50. Erlitzki R, Long JC, Theil EC, (2002) Multiple, conserved iron-responsive elements in the 3′-untranslated region of transferrin receptor mRNA enhance binding of iron regulatory protein 2. J Biol Chem 277: 42579-42587.
51. Jacolot S, Ferec C, Mura C, (2008) Iron responses in hepatic, intestinal and macrophage/monocyte cell lines under different culture conditions. Blood Cells Mol Dis 41: 100-108.
52. Teichmann R, Stremmel W, (1990) Iron uptake by human upper small intestine microvillous membrane vesicles. Indication for a facilitated transport mechanism mediated by a membrane iron-binding protein. J Clin Invest 86: 2145-2153.
53. He WL, Feng Y, Li XL, Wei YY, Yang XE, (2008) Availability and toxicity of Fe(II) and Fe(III) in Caco-2 cells. J Zhejiang Univ Sci B 9: 707-712.
54. Cmejla R, Petrak J, Cmejlova J, (2006) A novel iron responsive element in the 3′UTR of human MRCKalpha. Biochem Biophys Res Commun 341: 158-166.
55. Martini LA, Tchack L, Wood RJ, (2002) Iron treatment downregulates DMT1 and IREG1 mRNA expression in Caco-2 cells. J Nutr 132: 693-696.
56. Sanchez M, Galy B, Muckenthaler MU, Hentze MW, (2007) Iron-regulatory proteins limit hypoxia-inducible factor-2alpha expression in iron deficiency. Nat Struct Mol Biol 14: 420-426.
57. Lin E, Graziano JH, Freyer GA, (2001) Regulation of the 75-kDa subunit of mitochondrial complex I by iron. J Biol Chem 276: 27685-27692.
58. Cho HH, Cahill CM, Vanderburg CR, Scherzer CR, Wang B, et al. (2010) Selective translational control of the Alzheimer amyloid precursor protein transcript by iron regulatory protein-1. J Biol Chem 285: 31217-31232.
59. Giebel B, Corbeil D, Beckmann J, Hohn J, Freund D, et al. (2004) Segregation of lipid raft markers including CD133 in polarized human hematopoietic stem and progenitor cells. Blood 104: 2332-2338.
60. Corbeil D, Roper K, Hellwig A, Tavian M, Miraglia S, et al. (2000) The human AC133 hematopoietic stem cell antigen is also expressed in epithelial cells and targeted to plasma membrane protrusions. J Biol Chem 275: 5512-5520.
61. Corbeil D, Marzesco AM, Wilsch-Brauninger M, Huttner WB, (2010) The intriguing links between prominin-1 (CD133), cholesterol-based membrane microdomains, remodeling of apical plasma membrane protrusions, extracellular membrane particles, and (neuro)epithelial cell differentiation. FEBS Lett 584: 1659-1664.
62. Huttner HB, Janich P, Kohrmann M, Jaszai J, Siebzehnrubl F, et al. (2008) The stem cell marker prominin-1/CD133 on membrane particles in human cerebrospinal fluid offers novel approaches for studying central nervous system disease. Stem Cells 26: 698-705.
63. Nunez MT, Glass J, (1982) Reconstitution of the transferrin receptor in lipid vesicles. Effect of cholesterol on the binding of transferrin. Biochemistry 21: 4139-4143.
64. Davis RJ, Corvera S, Czech MP, (1986) Insulin stimulates cellular iron uptake and causes the redistribution of intracellular transferrin receptors to the plasma membrane. J Biol Chem 261: 8708-8711.
65. Enns CA, (2001) Pumping iron: the strange partnership of the hemochromatosis protein, a class I MHC homolog, with the transferrin receptor. Traffic 2: 167-174.
66. Galvez T, Teruel MN, Heo WD, Jones JT, Kim ML, et al. (2007) siRNA screen of the human signaling proteome identifies the PtdIns(3,4,5)P3-mTOR signaling pathway as a primary regulator of transferrin uptake. Genome Biol 8: R142.
67. Bhatt L, Murphy C, O'Driscoll LS, Carmo-Fonseca M, McCaffrey MW, et al. (2010) N-glycosylation is important for the correct intracellular localization of HFE and its ability to decrease cell surface transferrin binding. FEBS J 277: 3219-3234.
68. Warburg O, (1956) On respiratory impairment in cancer cells. Science 124: 269-270.
69. Antonescu CN, Diaz M, Femia G, Planas JV, Klip A, (2008) Clathrin-dependent and independent endocytosis of glucose transporter 4 (GLUT4) in myoblasts: regulation by mitochondrial uncoupling. Traffic 9: 1173-1190.
70. Tanner LI, Lienhard GE, (1989) Localization of transferrin receptors and insulin-like growth factor II receptors in vesicles from 3T3-L1 adipocytes that contain intracellular glucose transporters. J Cell Biol 108: 1537-1545.
71. Livingstone C, James DE, Rice JE, Hanpeter D, Gould GW, (1996) Compartment ablation analysis of the insulin-responsive glucose transporter (GLUT4) in 3T3-L1 adipocytes. Biochem J 315 (Pt 2): 487-495.
72. Stehling O, Sheftel AD, Lill R, (2009) Chapter 12 Controlled expression of iron-sulfur cluster assembly components for respiratory chain complexes in mammalian cells. Methods Enzymol 456: 209-231.
73. Alirol E, Martinou JC, (2006) Mitochondria and cancer: is there a morphological connection? Oncogene 25: 4706-4716.
74. Platet N, Liu SY, Atifi ME, Oliver L, Vallette FM, et al. (2007) Influence of oxygen tension on CD133 phenotype in human glioma cell cultures. Cancer Lett 258: 286-290.
75. Soeda A, Park M, Lee D, Mintz A, Androutsellis-Theotokis A, et al. (2009) Hypoxia promotes expansion of the CD133-positive glioma stem cells through activation of HIF-1alpha. Oncogene 28: 3949-3959.
76. Matsumoto K, Arao T, Tanaka K, Kaneda H, Kudo K, et al. (2009) mTOR signal and hypoxia-inducible factor-1 alpha regulate CD133 expression in cancer cells. Cancer Res 69: 7160-7164.
77. Eckard J, Dai J, Wu J, Jian J, Yang Q, et al. (2010) Effects of cellular iron deficiency on the formation of vascular endothelial growth factor and angiogenesis. Iron deficiency and angiogenesis. Cancer Cell Int 10: 28.
78. Knowles HJ, Mole DR, Ratcliffe PJ, Harris AL, (2006) Normoxic stabilization of hypoxia-inducible factor-1alpha by modulation of the labile iron pool in differentiating U937 macrophages: effect of natural resistance-associated macrophage protein 1. Cancer Res 66: 2600-2607.
79. Guzy RD, Hoyos B, Robin E, Chen H, Liu L, et al. (2005) Mitochondrial complex III is required for hypoxia-induced ROS production and cellular oxygen sensing. Cell Metab 1: 401-408.
80. Dery MA, Michaud MD, Richard DE, (2005) Hypoxia-inducible factor 1: regulation by hypoxic and non-hypoxic activators. Int J Biochem Cell Biol 37: 535-540.
81. Bedrine-Ferran H, Le Meur N, Gicquel I, Le Cunff M, Soriano N, et al. (2004) Transcriptome variations in human CaCo-2 cells: a model for enterocyte differentiation and its link to iron absorption. Genomics 83: 772-789.
82. Piccirillo SG, Reynolds BA, Zanetti N, Lamorte G, Binda E, et al. (2006) Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells. Nature 444: 761-765.
83. Campos B, Wan F, Farhadi M, Ernst A, Zeppernick F, et al. (2010) Differentiation therapy exerts antitumor effects on stem-like glioma cells. Clin Cancer Res 16: 2715-2728.
84. Kondo T, Setoguchi T, Taga T, (2004) Persistence of a small subpopulation of cancer stem-like cells in the C6 glioma cell line. Proc Natl Acad Sci U S A 101: 781-786.
85. Toyokuni S, (1996) Iron-induced carcinogenesis: the role of redox regulation. Free Radic Biol Med 20: 553-566.
86. Mastroberardino PG, Hoffman EK, Horowitz MP, Betarbet R, Taylor G, et al. (2009) A novel transferrin/TfR2-mediated mitochondrial iron transport system is disrupted in Parkinson's disease. Neurobiol Dis 34: 417-431.
87. Jiang D, Li X, Williams R, Patel S, Men L, et al. (2009) Ternary complexes of iron, amyloid-beta, and nitrilotriacetic acid: binding affinities, redox properties, and relevance to iron-induced oxidative stress in Alzheimer's disease. Biochemistry 48: 7939-7947.
88. He X, Hahn P, Iacovelli J, Wong R, King C, et al. (2007) Iron homeostasis and toxicity in retinal degeneration. Prog Retin Eye Res 26: 649-673.