Skip to main content
Log in

Functional role of proteins containing ankyrin repeats

  • Published:
Cell and Tissue Biology Aims and scope Submit manuscript

Abstract

This review describes and discusses new data on the structure and function of proteins that contain ankyrin-like repeats in their structure. These proteins were found in cells of different organisms, but they do not belong to the cytoskeletal proteins. Many important functions of such proteins are provided by ankyrin repeats, which maintain protein-protein interactions that are involved in the formation of transcription complexes, the initiation of immune responses, biogenesis and the assembly of cation channels in the membranes, the regulation of some cell-cycle stages, symbiotic interactions, and many other processes. Mutations in genes that encode ankyrin-like proteins can cause defects in gene expression leading to onset and progression of many human and animal diseases; therefore, the structure, dynamics, and function of these proteins are objects of intensive study in modern biology.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Almawi, W.Y. and Melemedjian, O.K., Negative Regulation of Nuclear Factor-kB Activation and Function by Glucocorticoids, J. Mol. Endocrinol., 2002, vol. 28, pp. 69–78.

    Article  PubMed  CAS  Google Scholar 

  • Andrade, Y.N., Fernandes, J., Vazquez, E., Fernandez-Fernandez, J.M., Arniges, M., and Sanchez, T.M., TRPV4 Channel Is Involved in the Coupling of Fluid Viscosity Changes to Epithelial Ciliary Activity, J. Cell Biol., 2005, vol. 168, pp. 869–874.

    Article  PubMed  CAS  Google Scholar 

  • Andrews, B.J., Gene Expression. Dialogue with the Cell Cycle, Nature, 1992, vol. 355, pp. 393–394.

    Article  PubMed  CAS  Google Scholar 

  • Artavanis-Tsakonas, S., Matsuno, K., and Fortini, M.E., Notch Signaling, Science, 1995, vol. 268, pp. 225–232.

    Article  PubMed  CAS  Google Scholar 

  • Axton, J.M., Shamanski, F.L., Young, L.M., Henderson, D.S., Boyd, J.B., and Orr-Weaver, T.L., The Inhibitor of DNA Replication Encoded by the Drosophila Gene Plutonium Is a Small, Ankyrin Repeat Protein, EMBO J., 1994, vol. 13, pp. 462–470.

    PubMed  CAS  Google Scholar 

  • Baer, R. and Ludwig, T., The BRCA1/BARD1 Heterodimer, a Tumor Suppressor Complex with Ubiquitin E3 Ligase Activity, Curr. Opin. Genet. Dev., 2002, vol. 12, pp. 86–91.

    Article  PubMed  CAS  Google Scholar 

  • Baker, B., Zambryski, P., Staskawicz, B., Dinesh-Kumar, S.P., Signaling in Plant-microbe Interactions, Science, 1997, vol. 276, pp. 726–733.

    Article  PubMed  CAS  Google Scholar 

  • Bandell, M., Story, G.M., Hwang, S.W., Viswanath, V., Eid, S.R., Petrus, M.J., Earley, T.J., and Patapoutian, A., Noxious Cold Ion Channel TRPA1 Is Activated by Pungent Compounds and Bradykinin, Neuron, 2004, vol. 41, pp. 849–857.

    Article  PubMed  CAS  Google Scholar 

  • Batrukova, M.A., Betin, V.L., Rubtsov, A.M., and Lopina, O.D., Ankyrin: Structure, Properties, and Functions, Biokhimiya, 2000, vol. 65, no. 4, pp. 469–484.

    Google Scholar 

  • Beyon, J., Li, J., Ericson, K., Selby, T., Tevelev, A., Kim H.-J., O’Maille, P., and Tsai, M.-D., Tumor Suppressor p16 INK4A: Determination of Solution Structure and Analyses of Its Interaction with Cyclin-dependent Kinase 4, Mol. Cell., 1998, vol. 1, pp. 421–431.

    Article  Google Scholar 

  • Boice, J.A. and Fairman, R., Structural Characterization of the Tumor Suppressor p16, an Ankyrin-like Repeat Protein, Protein Sci., 1996, vol. 5, 1776–1784.

    Article  PubMed  CAS  Google Scholar 

  • Bork, P., Hundreds of Ankyrin-Like Repeats in Functionally Diverse Proteins: Mobile Modules That Cross Phyla Horizontally?, Proteins, 1993, vol. 17, pp. 363–374.

    Article  PubMed  CAS  Google Scholar 

  • Breeden, L. and Nasmyth, K., Similarity between Cell-cycle Genes of Budding Yeast and Fission Yeast and the Notch Gene of Drosophila, Nature, 1987, vol. 329, pp. 651–654.

    Article  PubMed  CAS  Google Scholar 

  • Carlyon, J.A., Ryan, D., Archer, K., and Fikrig, E., Effects of Anaplasma phagocytophilum on Host Cell Ferritin mRNA and Protein Levels, Infect Immun., 2005, vol. 73, pp. 7629–7636.

    Article  PubMed  CAS  Google Scholar 

  • Caturegli, P., Asanovich, K.M., Walls, J.J., Bakken, J.S., Madigan, J.E., and Popov, S., AnkA: an Ehrlichia phagocytophila Group Gene Encoding a Protein Antigen with Ankyrin-like Repeats, Infect. Immun., 2000, vol. 68, pp. 5277–5283.

    Article  PubMed  CAS  Google Scholar 

  • Clapham, D.E., Runnels, L.W., and Strübing, C., The TRP Ion Channel Family, Nature Rev. Neurosci. 2001, vol. 2, pp. 386–396.

    Google Scholar 

  • Kucinich, S., Bulet, P., Hetru, C., and Hoffmann, J.A., Inducible Antibacterial Peptides of Insects, Parasitol. Today, 1994, vol. 10, pp. 132–139.

    Article  Google Scholar 

  • Colbert, H.A., Smith, T.L., and Bargmann, C.I., OSM-9, a Novel Protein with Structural Similarity to Channels, Is Required for Olfaction, Mechanosensation and Olfactory and Aptation in Caenorhabditis elegans, J. Neurosci., 1997, vol. 17, pp. 8259–8269.

    PubMed  CAS  Google Scholar 

  • Cozzone, A.J., Regulation of Acetate Metabolism by Protein Phosphorylation in Enteric Bacteria, Annu. Rev. Microbiol., 1998, vol. 52, pp. 127–164.

    Article  PubMed  CAS  Google Scholar 

  • Desikan, R., A-H-Mackerness, S., Hancock, J.T., and Neill, S.J., Regulation of the Arabidopsis transcriptome by Oxidative Stress, Plant Physiol., 2001, vol. 127, no. 1, pp. 159–172.

    Article  PubMed  CAS  Google Scholar 

  • Diaz-Guerra, M., Esteban, M., and Martinez, J.L., Growth of Escherichia coli in Acetate as a Sole Carbon Source Is Inhibited by Ankyrin-like Repeats Present in the 2′,5′-linked Oligoadenylate-dependent Human RNase L Enzyme, FEMS Microbiol. Lett., 1997, vol. 149, pp. 107–113.

    Article  PubMed  CAS  Google Scholar 

  • Draetta, G.F., Mammalian G-cyclins, Curr. Opin. Cell Biol., 1994, pp. 62 342–62 846.

    Google Scholar 

  • Dreyfus, D.H., Nagasawa, M., Gelfand, E.W., and Ghoda, L.Y., Modulation of p53 Activity by IkappaBalpha: Evidence Suggesting a Common Phylogeny between NF-kappaB and p53 Transcription Factors, BMC Immunol., 2005, vol. 21, pp. 6–12.

    Google Scholar 

  • Dumler, J.S., Barbet, A.F., Bekker, C.P., Dasch, G.A., Palmer, G.H., and Ray, S.C., Reorganization of Genera in the Families Rickettsiaceae and Anaplasmataceae in the Order Rickettsiales: Unification of Some Species of Ehrlichia with Anaplasma, Cowdria with Ehrlichia and Ehrlichia with Neorickettsia, Descriptions of Six New Species Combinations and Designation of Ehrlichia equi and ‘HGE Agent’ as Subjective Synonyms of Ehrlichia phagocytophila. Int. J. Syst. Evol. Microbiol., 2001, vol. 51, pp. 2145–2165.

    PubMed  CAS  Google Scholar 

  • Dumler, J.S., Choi, K.S., Garcia-Garcia, J.C., and Barat, N.S., Human Granulocytic Anaplasmosis and Anaplasma phagocytophilum. Emerg. Infect. Dis., 2005, vol. 11, pp. 1828–1834.

    PubMed  Google Scholar 

  • Dushay, M.S., Asling, B., and Hultmark, D., Origins of Immunity: Relish, a Compound Rel-like Gene in the Antibacterial Defense of Drosophila, Proc. Natl. Acad. Sci. USA, 1996, vol. 17, pp. 10 343–10 347.

    Google Scholar 

  • Elfring, L.K., Axton, J.M., Fenger, D.D., Page, A.W., Carminati, J.L., and Orr-Weaver, T.L., Drosophila PLUTONIUM Protein Is a Specialized Cell Cycle Regulator Required at the Onset of Embryogenesis, Mol. Biol. Cell., 1997, vol. 8, pp. 583–593.

    PubMed  CAS  Google Scholar 

  • Gaffney, T., Friedrich, L., Vernooij, B., Negrotto, D., Nye, G., Uknes, S., Ward, E., Kessmann, H., and Ryals, J., Requirement for Salicylic Acid for the Induction of Systemic Acquired Resistance, Science, 1993, vol. 261, pp. 754–756.

    Article  PubMed  CAS  Google Scholar 

  • Galinier, A., Bleicher, F., Neégre, D., Perrieére, G., Duclos, B., Cozzone, A.J., and Cortay, J.C., Primary Structure of the Intergenic Region between aceK and iclR in the Escherichia coli Chromosome, Gene, 1991, vol. 97, pp. 149–150.

    Article  PubMed  CAS  Google Scholar 

  • Genoud, T., Trevino Santa Cruz, M.B., and Metraux, J.P., Numeric Simulation of Plant Signaling Networks, Plant Physiol., 2001, vol. 126, pp. 1430–1437.

    Article  PubMed  CAS  Google Scholar 

  • Givskov, M., Olsen, L., and Molin, S., Cloning and Expression in Escherichia coli of the Gene for Extracellular Phospholipase A1 from Serratia liquefaciens, J. Bacteriol., 1988, vol. 170, pp. 5855–5862.

    PubMed  CAS  Google Scholar 

  • Hermkes, R., Funke, S., Richter, C., Kuhlmann, J., and Schunemann, D., The Alpha-helix of the Second Chromodomain of the 43 kDa Subunit of the Chloroplast Signal Recognition Particle Facilitates Binding to the 54 kDa Subunit, FEBS Lett., 2006, vol. 580, pp. 3107–3111.

    Article  PubMed  CAS  Google Scholar 

  • Howard, J. and Bechstedt, S., Hypothesis: a Helix of Ankyrin Repeats of the NOMPC-TRP Ion Channel Is the Gating Spring of Mechanoreceptors, Curr. Biol., 2004, vol. 14, pp. R224–R226.

    Article  PubMed  CAS  Google Scholar 

  • Howell, M.L., Alsabbagh, E., Ma, J.-F., Ochsner, U.A., Klotz, M.G., Beveridge, T.J., Blumenthal, K.M., Niederhoffer, E.C., Morris, R.E., Needham, D., Dean, G.E., Wani, M.A., and Hassett, D.J., AnkB, a Periplasmic Ankyrin-like Protein in Pseudomonas aeruginosa, Is Required for Optimal Catalase B (KatB) Activity and Resistance to Hydrogen Peroxide, J. Bacteriol., 2000, vol. 182, pp. 4545–4556.

    Article  PubMed  CAS  Google Scholar 

  • Hsieh, T.-C., Aguero-Rosenfeld, M., Wu, J.M., Ng, C., Papanikolou, N.K., Varde, S.A., Schwartz, I., Pizzolo, J.G., Melamed, M., Horowitz, H.W., Nadelman, R.B., and Wormser, G.P., Cellular Changes and Induction of Apoptosis in Human Promyelocytic HL60 Cells Infected with the Agent of Human Granulocytic Ehrlichiosis (HGE), Biochem. Biophys. Res. Commun., 1997, vol. 232, pp. 298–303.

    Article  PubMed  CAS  Google Scholar 

  • Hultmark, D., Insect Immunology. Ancient Relationships, Nature, 1994, vol. 367, pp. 116–117.

    Article  PubMed  CAS  Google Scholar 

  • Hurst, G.D. and Jiggins, F.M., Male-killing Bacteria in Insects: Mechanisms, Incidence, and Implications, Emerg. Infect. Dis., 2000, vol. 6, pp. 329–336.

    PubMed  CAS  Google Scholar 

  • Ishikawa, H., Claudio, E., Dambach, D., Raventós-Suárez, C., Ryan, C., and Bravo, R.. Chronic Inflammation and Susceptibility to Bacterial Infections in Mice Lacking the Polypeptide (p)105 Precursor (NFk-B1) but Expressing p50, J. Exp. Med., 1998, vol. 187, pp. 985–996.

    Article  PubMed  CAS  Google Scholar 

  • Iturbe-Ormaetxe, I., Burke, G.R., Riegler, M., and O’Neill, S.L., Distribution, Expression, and Motif Variability of Ankyrin Domain Genes in Wolbachia pipientis, J. Bacteriol., 2005, vol. 187, pp. 5136–5145.

    Article  PubMed  CAS  Google Scholar 

  • Iwabushi, K., Bartel, P.L, Li, B., Marraccino, R., and Fields, S., Two Cellular Proteins that Bind to Wild-type but not Mutant p53, Proc. Natl. Acad. Sci. USA, 1994, vol. 91, pp. 6098–6102.

    Article  Google Scholar 

  • Jonas-Straube, E., Hutin, C., Hoffman, N.E., and Schunemann, D., Functional Analysis of the Protein-interacting Domains of Chloroplast SRP43, J. Biol. Chem., 2001, vol. 276, pp. 24 654–24 660.

    CAS  Google Scholar 

  • Jordt, S.E., Bautista, D.M., Chuang, H.H., McKemy, D.D., Zygmunt, P.M., Hogestatt, E.D., Meng, I.D., and Julius, D., Mustard Oils and Cannabinoids Excite Sensory Nerve Fibres through the TRP Channel ANKTM1, Nature, 2004, vol. 427, pp. 260–265.

    Article  PubMed  CAS  Google Scholar 

  • Karppinen, S-M., Heikkinen, K., Rapakko, K., and Winqvist, R., Mutation Screening of the BARD1 Gene: Evidence for Involvement of the Cys557Ser Allele in Hereditary Susceptibility to Breast Cancer, J. Med. Genet., 2004, vol. 41, pp. 1–5.

    Article  Google Scholar 

  • Kobayashi, S., Kajino, S., Takahashi, N., Kanazawa, S., Imai, K., Hibi, Y., Ohara, H., Itoh, M., and Okamoto, T., 53BP2 Induces Apoptosis through the Mitochondrial Death Pathway Genes to Cells, 2005, vol. 10, pp. 253–260.

    CAS  Google Scholar 

  • Krawczyk, M., and Reith, W., Regulation of MHC Class II Expression, a Unique Regulatory System Identified by the Study of a Primary Immunodeficiency Disease, J. Compilat., 2006, vol. 67, pp. 183–197.

    CAS  Google Scholar 

  • Liedtke, W. and Kim, C., Functionality of the TRPV Subfamily of TRP Ion Channels: Add Mechano-TRP and Osmo-TRP to the Lexicon, Cell. Mol. Life Sci., 2005, vol. 1, pp. 2–18.

    Google Scholar 

  • Lin, J.-H., Makris, A., McMahon, C., Bear, S.E., Patriotis, C., Prasad, V.R., Brent, R., Golemis, E.A., and Tsichlis, P.N., The Ankyrin Repeat Containing Adaptor Protein Tvl-1 Is a Novel Substrate and Regulator of Raf-1, J. Biol. Chem., 1999, vol. 274, pp. 14 706–14 715.

    CAS  Google Scholar 

  • Loon, L.C., Bakker, P.A., and Pieterse, C.M., Systemic Resistance Induced by Rhizosphere Bacteria, Annu. Rev. Phytopathol., 1998, vol. 36, pp. 453–483.

    Article  PubMed  Google Scholar 

  • Lux, S.E., John, K.M., and Bennett, V., Analysis of cDNA for Human Erythrocyte Ankyrin Indicates a Repeated Structure with Homology to Tissue Differentiation and Cell-cycle Control Proteins, Nature, 1990, vol. 344, pp. 36–42.

    Article  PubMed  CAS  Google Scholar 

  • Malek, S., Huang, D., Huxford, T., Ghosh, S., and Ghosh, G., X-ray Crystal Structure of an IkB/NF-kB p65 Homodimer Complex, J. Biol. Chem., 2003, vol. 278, pp. 23 094–23 100.

    Article  CAS  Google Scholar 

  • Masternak, K., Barras, E., Zufferey, M., Conrad, B., Corthals, G., Aebersold, R., Sanchez, J.C., Hochstrasser, D.F., Mach, B., and Reith, W., A Gene Encoding a Novel RFX-associated Transactivator Is Mutated in the Majority of MHC Class II Deficiency Patients, Nat. Genet., 1998, vol. 20, pp. 273–277.

    Article  PubMed  CAS  Google Scholar 

  • Mitchell, T.C., Hildeman, D., and Kedl, R.M., Immunological Adjuvant Promote Activated T Cell Survival via Induction of Bcl-3, Nat. Immunol., 2001, vol. 2, pp. 397–402.

    PubMed  CAS  Google Scholar 

  • Mitchell, T.C., Thompson, B.S., Trent, J.O., and Casella, C.R., A Short Domain within Bcl-3 Is Responsible for Its Lymphocyte Survival Activity, Ann. N.Y. Acad. Sci., 2002, vol. 975, pp. 132–147.

    PubMed  CAS  Google Scholar 

  • Mosavi, L.K., Cammett, T.J., Desrosiers, D.C., and Peng, Z.Y., The Ankyrin Repeat as Molecular Architecture for Protein Recognition, Protein Sci., 2004, vol. 13, pp. 1435–1448.

    Article  PubMed  CAS  Google Scholar 

  • Nasmyth, K., and Dirick, L., The Role of SWI4 and SWI6 in the Activity of G1 Cyclins in Yeast, Cell, 1991, vol. 66, pp. 995–1013.

    Article  PubMed  CAS  Google Scholar 

  • Negre, D., Cortay, J.-C., Galinier, A., Sauve, P., and Cozzone, A.J., Specific Interactions between the IclR Repressor of the Acetate Operon of Escherichia coli and Its Operator, J. Mol. Biol., 1992, vol. 228, pp. 23–29.

    Article  PubMed  CAS  Google Scholar 

  • Nekrep, N., Geyer, M., Jabrane-Ferrat, N., and Peterlin, B.M., Analysis of Ankyrin Repeats Reveals How a Single Point Mutation in RFXANK Results in Bare Lymphocyte Syndrome, Mol. Cell. Biol., 2001, vol. 21, pp. 5566–5576.

    Article  PubMed  CAS  Google Scholar 

  • Neuwald, A.F. and Green, P., Detecting Patterns in Protein Sequences, J. Mol. Biol., 1994, vol. 239, pp. 698–712.

    Article  PubMed  CAS  Google Scholar 

  • Ogas, J., Andrews, B.J, and Herskowitz, I., Transcriptional Activation of CLN1, CLN2, and a Putative New G1 Cyclin (HCS26) by SWI4, a Positive Regulator of G1-specific Transcription, Cell, 1991, vol. 66, pp. 1015–1026.

    Article  PubMed  CAS  Google Scholar 

  • O’Neill, S.L., Giordano, R., Colbert, A.M., Karr, T.L., and Robertson, H.M., 16S rRNA Phylogenetic Analysis of the Bacterial Endosymbionts Associated with Cytoplasmic Incompatibility in Insects, Proc. Natl. Acad. Sci. USA, 1992, vol. 89, pp. 2699–2702.

    Article  PubMed  CAS  Google Scholar 

  • Orian, A., Schwartz, A.L., Israe, A., Whiteside, S., Kahana, C., and Ciechanover, A., Structural Motifs Involved in Ubiquitin-mediated Processing of the NF-kB Precursor p105: Roles of the Glycine-rich Region and a Downstream Ubiquitination, Domain Molec. Cell. Biol., 1999, vol. 19, pp. 3664–3673.

    CAS  Google Scholar 

  • Park, J., Kim, K.J., Choi, K.S., Grab, D.J., and Dumler, J.S., Anaplasma phagocytophilum AnkA Binds to Granulocyte DNA and Nuclear Proteins, Cell Microbiol., 2004, vol. 6, pp. 743–751.

    Article  PubMed  CAS  Google Scholar 

  • Petcherski, A., and Kimble, J., LAG-3 is a Putative Transcriptional Activator in the C. elegans Notch Pathway, Nature, 2000, vol. 405, pp. 364–368.

    Article  PubMed  CAS  Google Scholar 

  • Pieterse, C.M., van Wees, C.M., van Pelt, J.A., Knoester, M., Laan, R., Gerrits, H., Weisbeek, P.J., and Loon, L.C., A Novel Signaling Pathway Controlling Induced Systemic Resistance in Arabidopsis, Plant Cell, 1998, vol. 10, 1571–1580.

    Article  PubMed  CAS  Google Scholar 

  • Pieterse, C.M., van Wees, S.C., Ton, J., van Pelt, J.A., and Loon, L.C., Signaling in Rhizobacteria-induced Systemic Resistance in Arabidopsis thanliana, Plant Biol., 2002, vol. 4, pp. 535–544.

    Article  CAS  Google Scholar 

  • Rapp, U.R., Role of Raf-1 Serine/Threonine Protein Kinase in Growth Factor Signal Transduction, Oncogene, 1991, vol. 6, pp. 495–500.

    PubMed  CAS  Google Scholar 

  • Salzberg, S.L., Hotopp, J.C., Delcher, A.L., Pop, M., Smith, D.R., Eisen, M.B., and Nelson, W.C., Serendipitous Discovery of Wolbachia Genomes in Multiple Drosophila Species, Genome Biol., 2005, vol. 6, pp. R23–R23.8.

    Article  PubMed  Google Scholar 

  • Schunemann, D., Structure and Function of the Chloroplast Signal Recognition Particle, Curr. Genet., 2004, vol. 44, pp. 295–304.

    Article  PubMed  CAS  Google Scholar 

  • Schweizer, H.P. and Hoang, T.T., An Improved System for Gene Replacement and xylE Fusion Analysis in Pseudomonas aeruginosa, Gene, 1995, vol. 158, pp. 15–22.

    Article  PubMed  CAS  Google Scholar 

  • Sedgwick, S.G. and Smerdon, S.J., The Ankyrin Repeat: a Diversity of Interactions on a Common Structural Framework, Trends Biochem. Sci., 1999, vol. 24, pp. 311–316.

    Article  PubMed  CAS  Google Scholar 

  • Shaw, K.L., Grimsley, G.R., Yakovlev, G.I., Makarov, A.A., and Pace, C.N., The Effect of Net Charge on the Solubility, Activity, and Stability of Ribonuclease Sa, Protein Sci., 2001, vol. 10, pp. 1206–1215.

    Article  PubMed  CAS  Google Scholar 

  • Sidi, S., Friedrich, R.W., and Nicolson, T., NompC TRP-channel Required for Vertebrate Sensory Hair Cell Mechanotransduction, Science, 2003, vol. 301, pp. 96–99.

    Article  PubMed  CAS  Google Scholar 

  • Stange, C., Plant-virus Interactions during the Infective Process, Cien. Inv. Agr., 2006, vol. 33, no. 1, pp. 1–18.

    Google Scholar 

  • Stevens, L., Giordano, R., and Fialho, R.F., Male-Killing, Nematode Infections, Bacteriophage Infection, and Virulence of Cytoplasmic Bacteria in the Genus Wolbachia, Annu. Rev. Ecol. Syst., 2001, vol. 32, pp. 519–545.

    Article  Google Scholar 

  • Stouthamer, R., Breeuwer, J.A., Luck, R.F., and Werren, J.H., Molecular Identification of Microorganisms Associated with Parthenogenesis, Nature, 1999, vol. 361, pp. 66–68.

    Article  Google Scholar 

  • Subramaniam, R., Desveaux, D., Spickler, C., Michnick, S.W., and Brisson, N., Direct Visualization of Protein Interactions in Plant Cells, Nat. Biotechnol., 2000, vol. 19, pp. 769–772.

    Article  CAS  Google Scholar 

  • Tobin D., Madsen D.M., Kahn-Kirby A., Peckol E., Moulder G., and Barstead R., Combinatorial Expression of TRPV Channel Proteins Defines Their Sensory Functions and Subcellular Localization in C. elegans Neurons, Neuron, 2002, vol. 35, pp. 307–318.

    Article  PubMed  CAS  Google Scholar 

  • Tracey, W.D., Wilson, R.I., Laurent, G., and Benzer, S., Painless, a Drosophila Gene Essential for Nociception, Cell, 2003, vol. 113, pp. 261–273.

    Article  PubMed  CAS  Google Scholar 

  • Vazquez, G., Wedel, B.J., Aziz, O., Trebak, M., and Putney, J.W., The Mammalian TRPC Cation Channels, Biochim. Biophys. Acta, 2004, vol. 1742, pp. 21–36.

    Article  PubMed  CAS  Google Scholar 

  • Vriens, J., Owsianik, G., Voets, T., Droogmans, G., and Nilius, B., Invertebrate TRP Proteins as Functional Models for Mammalian Channels, Eur. J. Physiol., 2004, vol. 449, pp. 213–226.

    CAS  Google Scholar 

  • Walker, R.G., Willingham, A.T., and Zuker C.S., A Drosophila Mechanosensory Transduction Channel, Science, 2000, vol. 287, pp. 2229–2234.

    Article  PubMed  CAS  Google Scholar 

  • Wedel, B.J., Vazquez, G., McKay, R.R., Bird, G., Putney, J.W., Acalmodulin/Inositol 1,4,5-Trisphosphate (IP3) Receptor-binding Region Targets TRPC3 to the Plasma Membrane in a Calmodulin/IP3 Receptor-independent Process, J. Biol. Chem., 2003, vol. 278, pp. 25 758–25 765.

    Article  CAS  Google Scholar 

  • Zhou, S., Fujimuro, M., Hsieh, J.J.-D., Chen, L., Miyamoto, A., Weinmaster, G., and Hayward, S.D., SKIP, a CBF1-associated Protein, Interacts with the Ankyrin Repeat Domain of NotchIC to Facilitate NotchIC Function, Mol. Cell. Biol., 2000, vol. 20, pp. 2400–2410.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to E. V. Kiseleva.

Additional information

Original Russian Text © D.A. Voronin, E.V. Kiseleva, 2008, published in Tsitologiya, Vol. 50, No. 1, 2008.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Voronin, D.A., Kiseleva, E.V. Functional role of proteins containing ankyrin repeats. Cell Tiss. Biol. 2, 1–12 (2008). https://doi.org/10.1134/S1990519X0801001X

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1990519X0801001X

Key words

Navigation