Ancient origin of reggie (flotillin), reggie-like, and other lipid-raft proteins: Convergent evolution of the SPFH domain

Cellular and Molecular Life Sciences

Volumn 63, Issue 3, 2006, Pages 343-357

  Rivera Milla, E ^a   Stuermer, C A O ^a   Malaga Trillo E ^a  

^a UNIVERSITY OF KONSTANZ   (Germany)

Author keywords

Evolution; Flotillin; Lipid raft; Oligomerization; Reggie; SPFH

Indexed keywords

FLOTILLIN; LIPID RAFT PROTEIN; PROHIBITIN; PROTEIN; PROTEIN HFLC K; REGGIE LIKE PROTEIN; REGGIE PROTEIN; STOMATIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIUM; DATA BASE; EVOLUTION; FUNGUS; LIPID RAFT; NONHUMAN; NUCLEOTIDE SEQUENCE; ORGANISM; PHYLOGENY; PLANT; PROTEIN DOMAIN; PROTEIN FAMILY;

AMINO ACID SEQUENCE; ANIMALS; CONSERVED SEQUENCE; EVOLUTION, MOLECULAR; HUMANS; MEMBRANE MICRODOMAINS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEIN CONFORMATION; SEQUENCE HOMOLOGY, AMINO ACID;

ANIMALIA; BACTERIA (MICROORGANISMS); FUNGI; METAZOA;

EID: 32044464800     PISSN: 1420682X     EISSN: 15691632     Source Type: Journal    
DOI: 10.1007/s00018-005-5434-3     Document Type: Article

References (68)

1. Malaga-Trillo E., Laessing U., Lang D. M., Meyer A. and Stuermer C. A. (2002) Evolution of duplicated reggie genes in zebrafish and goldfish. J. Mol. Evol. 54: 235-245
2. Schulte T., Paschke K. A., Laessing U., Lottspeich F. and Stuermer C. A. (1997) Reggie-1 and reggie-2, two cell surface proteins expressed by retinal ganglion cells during axon regeneration. Development 124: 577-587
3. Lang D. M., Lommel S., Jung M., Ankerhold R., Petrausch B., Laessing U. et al. (1998) Identification of reggie-1 and reggie-2 as plasmamembrane- associated proteins which cocluster with activated GPI-anchored cell adhesion molecules in non-caveolar micropatches in neurons. J. Neurobiol. 37: 502-523
4. Bickel P. E., Scherer P. E., Schnitzer J. E., Oh P., Lisanti M.P. and Lodish H. F. (1997) Flotillin and epidermal surface antigen define a new family of caveolae-associated integral membrane proteins. J. Biol. Chem. 272: 13793-13802
5. Galbiati F., Volonte D., Goltz J. S., Steele Z., Sen J., Jurcsak J. et al. (1998) Identification, sequence and developmental expression of invertebrate flotillins from Drosophila melanogaster. Gene 210: 229-237
6. Stuermer C. A., Lang D. M., Kirsch F., Wiechers M., Deininger S. O. and Plattner H. (2001) Glycosylphosphatidyl inositol-anchored proteins and fyn kinase assemble in noncaveolar plasma membrane microdomains defined by reggie-1 and -2. Mol. Biol. Cell. 12: 3031-3045
7. Morrow I. C., Rea S., Martin S., Prior I. A., Prohaska R., Hancock J. F. et al. (2002) Flotillin-1/reggie-2 traffics to surface raft domains via a novel Golgi-independent pathway: identification of a novel membrane targeting domain and a role for palmitoylation. J. Biol. Chem. 277: 48834-48841
8. Neumann-Giesen C., Falkenbach B., Beicht P., Claasen S., Luers G., Stuermer C. A. et al. (2004) Membrane and raft association of reggie-1/flotillin-2: role of myristoylation, palmitoylation and oligomerization and induction of filopodia by overexpression. Biochem J. 378: 509-518
9. Liu J., Deyoung S. M., Zhang M., Dold L. H. and Saltiel A. R. (2005) The SPFH domain of flotillin-1 contains distinct sequences that direct plasma membrane localization and protein interactions in 3T3-L1 adipocytes. J. Biol. Chem. 280: 16125-16134
10. Stuermer C. A., Langhorst M. F., Wiechers M. F., Legler D. F., Von Hanwehr S. H., Guse A. H. et al. (2004) PrPc capping in T cells promotes its association with the lipid raft proteins reggie-1 and reggie-2 and leads to signal transduction. FASEB J. 18: 1731-1733
11. Rajendran L., Masilamani M., Solomon S., Tikkanen R., Stuermer C. A., Plattner H. et al. (2003) Asymmetric localization of flotillins/reggies/ flotillins in preassembled platforms confers inherent polarity to hematopoietic cells. Proc. Natl. Acad. Sci. USA 100: 8241-8246
12. Salzer U. and Prohaska R. (2001) Stomatin, flotillin-1, and flotillin-2 are major integral proteins of erythrocyte lipid rafts. Blood 97: 1141-1143
13. Baumann C. A., Ribon V., Kanzaki M., Thurmond D. C., Mora S., Shigematsu S. et al. (2000) CAP defines a second signalling pathway required for insulin-stimulated glucose transport. Nature 407: 202-207
14. Kokubo H., Helms J. B., Ohno-Iwashita Y., Shimada Y., Horikoshi Y. and Yamaguchi H. (2003) Ultrastructural localization of flotillin-1 to cholesterol-rich membrane microdomains, rafts, in rat brain tissue. Brain Res. 965: 83-90
15. Kioka N., Ueda K. and Amachi T. (2002) Vinexin, CAP/ponsin, ArgBP2: a novel adaptor protein family regulating cytoskeletal organization and signal transduction. Cell. Struct. Funct. 27: 1-7
16. Kimura A., Baumann C. A., Chiang S. H. and Saltiel A. R. (2001) The sorbin homology domain: a motif for the targeting of proteins to lipid rafts. Proc. Natl. Acad. Sci. USA 98: 9098-9103
17. Stuermer C. A. and Plattner H. (2005) The 'lipid raft' microdomain proteins reggie-1 and reggie-2 (flotillins) are scaffolds for protein interaction and signalling. Biochem. Soc. Symp. 72: 109-118
18. Langhorst M. F., Reuter A. and Stuermer C. A. O. (2005) Scaffolding microdomains and beyond - the function of reggie/ flotillin proteins. Cell. Mol Life Sci. 62: 2228-2240
19. von Philipsborn A. C., Ferrer-Vaquer A., Rivera-Milla E., Stuermer C. A. and Malaga-Trillo E. (2004) Restricted expression of reggie genes and proteins during early zebrafish development. J. Comp. Neurol. 482: 257-272
20. Hoehne M., DeCouet G., Stuermer C. A. O. and Fischbach K. F. (2005) Loss- and gain of function analysis of the lipid raft proteins Reggie/Flotillin in Drosophila: they are post-translationally regulated and misexpression interferes with wing and eye development. Mol. Cell. Neurosci. 30: 326-338
21. Jacobowitz D. M. and Kallarakal A. T. (2004) Flotillin-1 in the substantia nigra of the Parkinson brain and a predominant localization in catecholaminergic nerves in the rat brain. Neurotox. Res. 6: 245-257
22. Kokubo H., Lemere C. A. and Yamaguchi H. (2000) Localization of flotillins in human brain and their accumulation with the progression of Alzheimer's disease pathology. Neurosci. Lett. 290: 93-96
23. Girardot N., Allinquant B., Langui D., Laquerriere A., Dubois B., Hauw J. J. et al. (2003) Accumulation of flotillin-1 in tangle-bearing neurones of Alzheimer's disease. Neuropathol. Appl. Neurobiol. 29: 451-461
24. Hazarika P., McCarty M. F., Prieto V. G., George S., Babu D., Koul D. et al. (2004) Up-regulation of Flotillin-2 is associated with melanoma progression and modulates expression of the thrombin receptor protease activated receptor 1. Cancer Res. 64: 7361-7369
25. Murphy S. C., Samuel B. U., Harrison T., Speicher K. D., Speicher D. W., Reid M. E. et al. (2004) Erythrocyte detergent-resistant membrane proteins: their characterization and selective uptake during malarial infection. Blood 103: 1920-1928
26. Schroeder W. T., Stewart-Galetka S., Mandavilli S., Parry D. A., Goldsmith L. and Duvic M. (1994) Cloning and characterization of a novel epidermal cell surface antigen (ESA). J. Biol. Chem. 269: 19983-19991
27. Cho Y. J., Chema D., Moskow J. J., Cho M., Schroeder W. T., Overbeek P. et al. (1995) Epidermal surface antigen (MS17S1) is highly conserved between mouse and human. Genomics 27: 251-258
28. Edgar A. J. and Polak J. M. (2001) Flotillin-1: gene structure. cDNA cloning from human lung and the identification of alternative polyadenylation signals. Int. J. Biochem. Cell. Biol. 33: 53-64
29. Tavernarakis N., Driscoll M. and Kyrpides N. C. (1999) The SPFH domain: implicated in regulating targeted protein turnover in stomatins and other membrane-associated proteins. Trends Biochem. Sci. 24: 425-427
30. Altschul S. F., Madden T. L., Schaffer A. A., Zhang J., Zhang Z., Miller W. et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25: 3389-3402
31. Kumar S., Tamura K., Jakobsen I. and Nei M. (2001) MEGA2: Molecular Evolutionary Genetics Analysis software. Bioinformatics 17: 1244-1245
32. Rivera-Milla E., Stuermer C. A. and Malaga-Trillo E. (2003) An evolutionary basis for scrapie disease: identification of a fish prion mRNA. Trends Genet. 19: 72-75
33. Miyamoto K., Koshiba S., Inoue M., Kigawa T. and Yokoyama S. (2004) Solution structure of the band 7 domain of the mouse flotillin 2 protein. www.rcsb.org/pdb/cgi/explore.cgi?pdbId=1win
34. Dominguez R. (2004) Actin-binding proteins - a unifying hypothesis. Trends Biochem. Sci. 29: 572-578
35. Lupas A. (1996) Prediction and analysis of coiled-coil structures. Methods Enzymol. 266: 513-525
36. Kyte J. and Doolittle R. F. (1982) A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157: 105-132
37. Glenner H., Hansen A. J., Sorensen M. V., Ronquist F., Huelsenbeck J. P. and Willerslev E. (2004) Bayesian inference of the metazoan phylogeny: a combined molecular and morphological approach. Curr. Biol. 14: 1644-1649
38. Pandur P. D., Dirksen M. L., Moore K. B. and Moody S. A. (2004) Xenopus flotillin1, a novel gene highly expressed in the dorsal nervous system. Dev. Dyn. 231: 881-887
39. Huang X., Gaballa A., Cao M. and Helmann J. D. (1999) Identification of target promoters for the Bacillus subtilis extracytoplasmic function sigma factor, sigma W. Mol. Microbiol. 31: 361-371
40. Wolf E., Kim P. S. and Berger B. (1997) MultiCoil: a program for predicting two- and three-stranded coiled coils. Protein Sci. 6: 1179-1189
41. Snyers L., Umlauf E. and Prohaska R. (1998) Oligomeric nature of the integral membrane protein stomatin. J. Biol. Chem. 273: 17221-17226
42. Tatsuta T., Model K. and Langer T. (2005) Formation of membrane-bound ring complexes by prohibitins in mitochondria. Mol. Biol. Cell. 16: 248-259
43. Nijtmans L. G., Artal S. M., Grivell L. A. and Coates P. J. (2002) The mitochondrial PHB complex: roles in mitochondrial respiratory complex assembly, ageing and degenerative disease. Cell. Mol. Life Sci. 59: 143-155
44. Kihara A., Akiyama Y. and Ito K. (1997) Host regulation of lysogenic decision in bacteriophage lambda: transmembrane modulation of FtsH (HflB), the cII degrading protease, by HflKC (HflA). Proc. Natl. Acad. Sci. USA 94: 5544-5549
45. Roselli S., Gribouval O., Boute N., Sich M., Benessy F., Attie T. et al. (2002) Podocin localizes in the kidney to the slit diaphragm area. Am. J. Pathol. 160: 131-139
46. Huber T. B. and Benzing T. (2005) The slit diaphragm: a signaling platform to regulate podocyte function. Curr. Opin. Nephrol. Hypertens. 14: 211-216
47. Chervitz S. A., Aravind L., Sherlock G., Ball C. A., Koonin E. V., Dwight S. S. et al. (1998) Comparison of the complete protein sets of worm and yeast: orthology and divergence. Science 282: 2022-2028
48. Winzer T., Bairl A., Linder M., Linder D., Werner D. and Müller P. (1999) A novel 53-kDa nodulin of the symbiosome membrane of soybean nodules, controlled by Bradyrhizobium japonicum. Mol. Plant Microbe Interact. 12: 218-226
49. Owczarek C. M., Treutlein H. R., Portbury K. J., Gulluyan L. M., Kola I. and Hertzog P. J. (2001) A novel member of the STOMATIN/EPB72/mec-2 family, stomatin-like 2 (STOML2), is ubiquitously expressed and localizes to HSA chromosome 9p13.1. Cytogenet. Cell Genet. 92: 196-203
50. Ruvkun G. and Hobert O. (1998) The taxonomy of developmental control in Caenorhabditis elegans. Science 282: 2033-2041
51. Danchin E. G. and Pontarotti P. (2004) Statistical evidence for a more than 800-million-year-old evolutionarily conserved genomic region in our genome. J. Mol. Evol. 59: 587-597
52. Lupas A. (1997) Predicting coiled-coil regions in proteins. Curr. Opin. Struct. Biol. 7: 388-393
53. Kohn W. D., Mant C. T. and Hodges R. S. (1997) Alpha-helical protein assembly motifs. J. Biol. Chem. 272: 2583-2586
54. Hung A. Y. and Sheng M. (2002) PDZ domains: structural modules for protein complex assembly. J. Biol. Chem. 277: 5699-5702
55. Santamaria A., Castellanos E., Gomez V., Benedit P., Renau-Piqueras J., Morote J. et al. (2005) PTOV1 enables the nuclear translocation and mitogenic activity of flotillin-1, a major protein of lipid rafts. Mol. Cell. Biol. 25: 1900-1911
56. Magnuson K., Jackowski S., Rock C. O. and Cronan J. E. Jr. (1993) Regulation of fatty acid biosynthesis in Escherichia coli. Microbiol. Rev. 57: 522-542
57. Wilson B. S., Steinberg S. L., Liederman K., Pfeiffer J. R., Surviladze Z., Zhang J. et al. (2004) Markers for detergent-resistant lipid rafts occupy distinct and dynamic domains in native membranes. Mol. Biol. Cell. 15: 2580-2592
58. Stewart G. W. (1997) Stomatin. Int. J. Biochem. Cell. Biol. 29: 271-274
59. Huang M., Gu G., Ferguson E. L. and Chalfie M. (1995) A stomatin-like protein necessary for mechanosensation in C. elegans. Nature 378: 292-295
60. Barnes T. M., Jin Y., Horvitz H. R., Ruvkun G. and Hekimi S. (1996) The Caenorhabditis elegans behavioral gene unc-24 encodes a novel bipartite protein similar to both erythrocyte band 7.2 (stomatin) and nonspecific lipid transfer protein. J. Neurochem. 67: 46-57
61. Eveleth D. D. and Marsh J. L. (1986) Evidence for evolutionary duplication of genes in the dopa decarboxylase region of Drosophila. Genetics 114: 469-483
62. Huber T. B., Simons M., Hartleben B., Sernetz L., Schmidts M., Gundlach E. et al. (2003) Molecular basis of the functional podocin-nephrin complex: mutations in the NPHS2 gene disrupt nephrin targeting to lipid raft microdomains. Hum. Mol. Genet. 12: 3397-3405
63. Goodman M. B., Ernstrom G. G., Chelur D. S., O'Hagan R., Yao C. A. and Chalfie M. (2002) MEC-2 regulates C. elegans DEG/ ENaC channels needed for mechanosensation. Nature 415: 1039-1042
64. Cohen A. W., Hnasko R., Schubert W. and Lisanti M. P. (2004) Role of caveolae and caveolins in health and disease. Physiol. Rev. 84: 1341-1379
65. Dietzen D. J., Hastings W. R. and Lublin D. M. (1995) Caveolin is palmitoylated on multiple cysteine residues: palmitoylation is not necessary for localization of caveolin to caveolae. J. Biol. Chem. 270: 6838-6842
66. Monier S., Parton R. G., Vogel F., Behlke J., Henske A. and Kurzchalia T. V. (1995) VIP21-caveolin, a membrane protein constituent of the caveolar coat, oligomerizes in vivo and in vitro. Mol. Biol. Cell. 6: 911-927
67. Gupta R. S. and Griffiths E. (2002) Critical issues in bacterial phylogeny. Theor. Popul. Biol. 61: 423-434
68. Daubin V., Gouy M. and Perriere G. (2002) A phylogenomic approach to bacterial phylogeny: evidence of a core of genes sharing a common history. Genome Res. 12: 1080-1090