Extra-mitochondrial localisation of frataxin and its association with IscU1 during enterocyte-like differentiation of the human colon adenocarcinoma cell line Caco-2

Journal of Cell Science

Volumn 118, Issue 17, 2005, Pages 3917-3924

  Acquaviva, Fabio ^a   De Biase, Irene ^a   Nezi, Luigi ^a   Ruggiero, Giuseppina ^a   Tatangelo, Fabiana ^b   Pisano, Carmela ^b   Monticelli, Antonella ^a   Garbi, Corrado ^a   Acquaviva, Angela Maria ^a   Cocozza, Sergio ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b NATIONAL CANCER INSTITUTE   (Italy)

Author keywords

Caco 2 cells; Differentiation; Frataxin; Mitochondrial mass; Subcellular localisation

Indexed keywords

FRATAXIN; IRON SULFUR PROTEIN; ISOPROTEIN; MESSENGER RNA; PROTEIN ISCU1; UNCLASSIFIED DRUG;

ARTICLE; CANCER CELL CULTURE; CELL DIFFERENTIATION; COLON ADENOCARCINOMA; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOPLASM; FRIEDREICH ATAXIA; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; INTESTINE CELL; INTESTINE CRYPT; INTESTINE EPITHELIUM CELL; INTESTINE VILLUS; IRON METABOLISM; MITOCHONDRION; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS;

CACO-2 CELLS; CELL DIFFERENTIATION; CELL FRACTIONATION; ENTEROCYTES; FRIEDREICH ATAXIA; HUMANS; INTESTINAL MUCOSA; IRON-BINDING PROTEINS; IRON-SULFUR PROTEINS; ISOENZYMES; MITOCHONDRIA; SUPEROXIDE DISMUTASE;

ATAXIA;

EID: 26244448912     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.02516     Document Type: Article

References (45)

1. Adamec, J., Rusnak, F., Owen, W. G., Naylor, S., Benson, L. M., Gacy, A. M. and Isaya, G. (2000). Iron-dependent self-assembly of recombinant yeast frataxin: implications for Friedreich's ataxia. Am. J. Hum. Genet. 67, 549-562.
2. Alvarez-Hernandez, X., Nichols, G. M. and Glass, J. (1991). Caco-2 cell line: a system for studying intestinal iron transport across epithelial cell monolayers. Biochim. Biophys. Acta 1070, 205-208.
3. Babcock, M., de Silva, D., Oaks, R., Davis-Kaplan, S., Jiralerspong, S., Montermini, L., Pandolfo, M. and Kaplan, J. (1997). Regulation of mitochondrial iron accumulation by Yfh1p, a putative homolog of frataxin. Science 276, 1709-1712.
4. Babyatsky, M. W. and Podolsky, D. K. (1999). Growth and development of the gastrointestinal tract. In Textbook of Gastroenterology. 3rd edn (ed. T. Yamada), pp. 547-584. Philadelphia: J. B. Lippincott.
5. Becker, E. M., Greer, J. M., Ponka, P. and Richardson, D. R. (2002). Erythroid differentiation and protoporphyrin IX down-regulate frataxin expression in Friend cells: characterization of frataxin expression compared with molecules involved in iron metabolism and hemoglobinization. Blood 99, 3813-3822.
6. Beinert, H. and Kiley, P. J. (1999). Fe-S proteins in sensing and regulatory functions. Curr. Opin. Chem. Biol. 3, 152-157.
7. Bidichandani, S. I., Ashizawa, T. and Patel, I. (1998). The GAA triplet-repeat expansion in Friedreich ataxia interferes with transcription and may be associated with an unusual DNA structure. Am. J. Hum. Genet. 62, 111-121.
8. Branda, S. S., Cavadini, P., Adamec, J., Kalousek, F., Throni, F. and Isaya, G. (1999). Yeast and human frataxin are processed to mature form in two sequential steps by the mitochondrial processing peptidase. J. Biol. Chem. 274, 22763-22769.
9. Cammack, R. (1992). In Iron-Sulfur Proteins (ed. R. Cammack), Vol. 38, pp. 281-322. San Diego: Academic Press.
10. Campuzano, V., Montermini, L., Moltò. M. D., Pianese, L., Cossee, M., Cavalcanti. F., Monros, E., Rodius, F., Duclos, F., Monticelli, A. et al. (1996). Friedreich's ataxia: autosomal recessive disease caused by an intronic GAA triplet repeat expansion. Science 271, 1423-1427.
11. Campuzano, V., Montermini, L., Lutz, Y., Cova, L., Hindelang, C., Jiralerspong, S., Trottier, Y., Kish, S. J., Faucheux, B., Trouillas, P. et al. (1997). Frataxin is reduced in Friedreich ataxia patients and is associated with mitochondrial membranes. Hum. Mol. Genet. 6, 1771-1780.
12. Cavadini, P., Gellera, C., Patel, P. I. and Isaya, G. (2000). Human frataxin maintains mitochondrial iron homeostasis in Saccharomyces cerevisiae. Hum. Mol. Genet. 9, 2523-2530.
13. Cavadini, P., O'Neill, H. A., Benda, O. and Isaya, G. (2002). Assembly and iron-binding properties of human frataxin, the protein deficient in Friedreich ataxia. Hum. Mol. Genet. 11, 217-227.
14. Duby, G., Foury, F., Ramazzotti, A., Herrmann, J. and Lutz, T. (2002). A non-essential function for yeast frataxin in iron-sulphur cluster assembly. Hum. Mol. Genet. 11, 2635-2643.
15. Dutkiewicz, R., Schilke, B., Kneiszner, H., Walter, W., Craig, E. A. and Marszalek, J. (2003). Ssq1, a mitochondrial Hsp70 involved in iron-sulphur (Fe/S) centre biogenesis: Similarities to and differences from its bacterial counterpart. J. Biol. Chem. 278, 29719-29727.
16. Ekmekcioglu, C., Strauss-Blasche, G. and Marktl, W. (1998). The plasma membrane Fe(3+)-reductase activity of Caco-2 cells is modulated during differentiation. Biochem. Mol. Biol. Int. 46, 951-961.
17. Foury, F. and Talibi, D. (2001). Mitochondrial control of iron homeostasis. A genome wide analysis of gene expression in a yeast frataxin-deficient strain. J. Biol. Chem. 276, 7762-7768.
18. Gerber, J., Muhlenhoff, U. and Lill, R. (2003). An interaction between frataxin and Isu1/Nfs1 that is crucial for Fe/S cluster synthesis on Isu1. EMBO Rep. 4, 906-911.
19. Griffiths, W. J., Kelly, A. L., Smith, S. J. and Cox, T. M. (2000). Localisation of iron transport and regulatory proteins in human cells. Q. J. Med. 93, 575-587.
20. Halleux, C. and Schneider, Y. J. (1991). Iron absorption by intestinal epithelial cells: Caco2 cells cultivated in serum-free medium, on polyethyleneterephthalate microporous membranes, as an in vitro model. In vitro Cell Dev. Biol. 27, 293-302.
21. Harding, A. E. (1981). Friedreich's ataxia: a clinical and genetic study of 90 families with an analysis of early diagnostic criteria and intrafamilial clustering of clinical features. Brain 104, 589-620.
22. Huynen, M. A., Snel, B., Bork, P. and Gibson, T. J. (2001). The phylogenetic distribution of frataxin indicates a role in iron-sulphur cluster protein assembly. Hum. Mol. Genet. 10, 2463-2468.
23. Jumarie, C. and Malo, C. (1991). Caco-2 cells cultured in serum-free medium as a model for the study of enterocytic differentiation in vitro. J. Cell Physiol. 149, 24-33.
24. Knight, S. A., Sepuri, N. B., Pain, D. and Dancis, A. (1998). Mt-Hsp70 homolog, Ssc2p, required for maturation of yeast frataxin and mitochondrial iron homeostasis. J. Biol. Chem. 273, 18389-18393.
25. Knox, C., Sass, E., Neupert, W. and Pines, O. (1998). Import into mitochondria, folding and retrograde movement of fumarase in yeast. J. Biol. Chem. 273, 25587-25593.
26. Koutnikova, H., Campuzano, V. and Koenig, M. (1998). Matration of wild-type and mutated frataxin by the mitochondrial processing peptidase. Hum. Mol. Genet. 7, 1485-1489.
27. Lanier, L. L. and Recktenwald, D. (1991). Multicolor immunofluorescence and flow cytometry. Methods 2, 192-198.
28. Livak, K. J. and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 25, 402-408.
29. Lutz, T., Westermann, B., Neupert, W. and Herrmann, J. M. (2001). The mitochondrial proteins Ssq1 and Jac1 are required for the assembly of iron sulphur clusters in mitochondria. J. Mol. Biol. 307, 815-825. Erratum in: J. Mol. Biol. 308, 1091.
30. Morgan, E. H. and Oates, P. S. (2002). Mechanisms and regulation of intestinal iron absorption. Blood Cells Mol. Dis. 29, 384-399.
31. Muhlenhoff, U. and Lill, R. (2000). Biogenesis of iron-sulphur proteins in eukaryotes: a novel task of mitochondria that is inherited from bacteria. Biochem. Biophys. Acta. 1459, 370-382.
32. Muhlenhoff, U., Richhardt, N., Ristow, M., Kispal, G. and Lill, R. (2002). The yeast frataxin homolog Yfh1p plays a specific role in the maturation of cellular Fe/S proteins. Hum. Mol. Genet. 11, 2025-2036.
33. Park, S., Gakh, O., Mooney, S. M. and Isaya, G. (2002). The ferroxidase activity of yeast frataxin. J. Biol. Chem. 277, 38589-38595.
34. Pignata, S., Maggini, L., Zarrilli, R., Rea, A. and Acquaviva, A. M. (1994). The enterocyte-like differentiation of the Caco-2 tumour cell line strongly correlates with responsiveness to cAMP and activation of kinase A pathway. Cell Growth Differ. 5, 967-973.
35. Pinto, M., Robine-Leon, S., Appay, M. D., Kedinger, M., Triadou, N., Dussaulx, E., Lacroix, B., Simon-Assmann, P., Haffen, K., Fogh, J. et al. (1983). Enterocyte-like differentiation and polarization of the human colon carcinoma cell line Caco-2 in culture. Biol. Cell. 47, 323-330.
36. Puccio, H., Simon, D., Cossee, M., Criqui-Filipe, P., Tiziano, F., Melki, J., Hindelang, C., Matyas, R., Rustin, P. and Koenig, M. (2001). Mouse models for Friedreich ataxia exhibit cardiomyopathy, sensory nerve defect and Fe-S enzyme deficiency followed by intramitochondrial iron deposits. Nat. Genet. 27, 181-186.
37. Ran, Q., Wadhwa, R., Kawai, R., Kaul, S. C., Sifers, R. N., Bick, R. J., Smith, J. R. and Pereira-Smith, O. M. (2000). Extramitochondrial localisation of mortalin/mthsp70/PBP74/GRP75. Biochem. Biophys. Res. Commun. 275, 174-179.
38. Rotig, A., de Lonlay, P., Chretien, D., Foury, E, Koenig, M., Sidi, D., Munnich, A. and Rustin, P. (1997). Aconitase and mitochondrial iron-sulphur protein deficiency in Friedreich ataxia. Nat. Genet. 17, 215-217.
39. Santos, M. M., Ohshima, K. and Pandolfo, M. (2001). Frataxin deficiency enhances apoptosis in cells differentiating into neuroectoderm. Hum. Mol. Genet 10, 1935-1944.
40. Schumann, K., Moret, R., Kunzle, H. and Kuhn, L. C. (1999). Iron regulatory protein as an endogenous sensor of iron in rat intestinal mucosa. Possible implications for the regulation of iron absorption. Eur. J. Biochem. 260, 362-372.
41. Soltys, B. J. and Gupta, R. S. (1999). Mitochondrial-matrix proteins at unexpected locations: are they exported? Trends Biochem. Sci. 24, 174-177.
42. Stehling, O., Elsasser, H. P., Bruckel, B., Muhlenhoff, U. and Lill, R. (2004). Iron-sulphur protein maturation in human cell: evidence for a function of frataxin Hum. Mol. Genet. 13, 3007-3015.
43. Tong, W. H. and Rouault, T. (2000). Distinct iron-sulphur cluster assembly complexes exist in the cytosol and mitochondria of human cells. EMBO J. 19, 5692-5700.
44. Voisine, C., Schilke, B., Ohlson, M., Beinert, H., Marszalek, J. and Craig, E. A. (2000). Role of the mitochondrial Hsp70s, Ssc1 and Ssq1, in the maturation of Yfh1 Mol. Cell. Biol. 20, 3677-3684.
45. Yoon, T. and Cowan, J. A. (2003). Iron-sulphur cluster biosynthesis. Characterization of frataxin as an iron donor for assembly of [2Fe-2S] clusters in ISU-type proteins. J. Am. Chem. Soc. 125, 6078-6084.