Arabidopsis calmodulin-binding protein iq67-domain 1 localizes to microtubules and interacts with kinesin light chain-related protein-1

Journal of Biological Chemistry

Volumn 288, Issue 3, 2013, Pages 1871-1882

  Bürstenbinder, Katharina ^a,d   Savchenko, Tatyana ^b,d,e   Müller, Jens ^a,d   Adamson, Aaron W ^b,d   Stamm, Gina ^a   Kwong, Raymond ^b,f   Zipp, Brandon J ^b   Dinesh, Dhurvas Chandrasekaran ^b   Abel, Steffen ^a,b,c  

^a LEIBNIZ INSTITUTE OF PLANT BIOCHEMISTRY   (Germany)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^d INSTITUTE OF BASIC BIOLOGICAL PROBLEMS   (Russian Federation)

^e Dept of Population Sciences ^*  (United States)

^f Siemens Healthcare Diagnostics   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS SEEDLINGS; ARABIDOPSIS THALIANA; BIOCHEMICAL FUNCTIONS; CDNA LIBRARIES; CELL NUCLEUS; CELLULAR PROCESS; CELLULAR TRANSPORT; DELETION MAPPING; DIRECT INTERACTIONS; GENES ENCODE; GENETIC SCREENS; IN-VITRO; KINESIN MOTOR PROTEINS; KINESIN MOTORS; KINESINS; MICRO-TUBULAR; MICROTUBULES; PLANT TISSUES; SCAFFOLD PROTEIN; SECOND MESSENGER; SUBCELLULAR LOCALIZATIONS; TOBACCO LEAVE; YEAST TWO HYBRID;

AMINO ACIDS; CALCIUM; CAMS; FREIGHT TRANSPORTATION; PLANTS (BOTANY); SCAFFOLDS (BIOLOGY); SEED; TISSUE; YEAST;

CALMODULIN;

CALMODULIN; CALMODULIN BINDING PROTEIN; GREEN FLUORESCENT PROTEIN; KINESIN LIGHT CHAIN RELATED PROTEIN 1; MEMBRANE PROTEIN; MOLECULAR MOTOR; PROTEIN IQ67 DOMAIN 1; PROTEIN KLCR1; PROTEIN RFP; UNCLASSIFIED DRUG;

ARABIDOPSIS; ARTICLE; BINDING AFFINITY; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GENE DELETION; GENE MAPPING; GENETIC SCREENING; GENETIC TRANSFORMATION; IN VITRO STUDY; INTRACELLULAR TRANSPORT; MICROTUBULE; NONHUMAN; PLANT LEAF; PLANT TISSUE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SEEDLING; TOBACCO; TWO HYBRID SYSTEM; YEAST;

AMINO ACID MOTIFS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BINDING SITES; CALCIUM; CALCIUM SIGNALING; CALMODULIN; CALMODULIN-BINDING PROTEINS; GENE EXPRESSION REGULATION, PLANT; GENE LIBRARY; KINETICS; MICROSCOPY, FLUORESCENCE; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; PROTEIN BINDING; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT FUSION PROTEINS; TWO-HYBRID SYSTEM TECHNIQUES;

ARABIDOPSIS; ARABIDOPSIS THALIANA; EUKARYOTA; NICOTIANA TABACUM;

EID: 84872732685     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.396200     Document Type: Article

References (62)

1. Dodd, A. N., Kudla, J., and Sanders, D. (2010) The language of calcium signaling. Annu. Rev. Plant Biol. 61, 593-620
2. + sensors in plant signalling. Biochem. J. 425, 27-40
3. Reddy, A. S., Ali, G. S., Celesnik, H., and Day, I. S. (2011) Coping with stresses. Roles of calcium-and calcium/calmodulin-regulated gene expression. Plant Cell 23, 2010-2032
4. Day, I. S., Reddy, V. S., Shad Ali, G., and Reddy, A. S. (2002) Analysis of EF-hand-containing proteins in Arabidopsis. Genome Biol 3, RESEARCH0056
5. Sanders, D., Pelloux, J., Brownlee, C., and Harper, J. F. (2002) Calcium at the crossroads of signaling. Plant Cell 14, S401-S417 (Pubitemid 34609250)
6. Hrabak, E. M., Chan, C. W., Gribskov, M., Harper, J. F., Choi, J. H., Halford, N., Kudla, J., Luan, S., Nimmo, H. G., Sussman, M. R., Thomas, M., Walker-Simmons, K., Zhu, J. K., and Harmon, A. C. (2003) The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiol 132, 666-680 (Pubitemid 36725704)
7. Weinl, S., and Kudla, J. (2009) The CBL-CIPK Ca2+-decoding signaling network. Function and perspectives. New Phytol. 184, 517-528
8. Luan, S. (2009) The CBL-CIPK network in plant calcium signaling. Trends Plant Sci. 14, 37-42
9. Reddy, A. S., Ben-Hur, A., and Day, I. S. (2011) Experimental and computational approaches for the study of calmodulin interactions. Phytochemistry 72, 1007-1019
10. McCormack, E., Tsai, Y. C., and Braam, J. (2005) Handling calcium signaling. Arabidopsis CaMs and CMLs. Trends Plant Sci. 10, 383-389 (Pubitemid 41059666)
11. Reddy, V. S., and Reddy, A. S. (2004) Proteomics of calcium-signaling components in plants. Phytochemistry 65, 1745-1776 (Pubitemid 38969920)
12. Bouché, N., Yellin, A., Snedden, W. A., and Fromm, H. (2005) Plantspecific calmodulin-binding proteins. Annu. Rev. Plant Biol. 56, 435-466
13. Rhoads, A. R., and Friedberg, F. (1997) Sequence motifs for calmodulin recognition. FASEB J. 11, 331-340 (Pubitemid 27193937)
14. Bähler, M., and Rhoads, A. (2002) Calmodulin signaling via the IQ motif. FEBS Lett. 513, 107-113 (Pubitemid 34242986)
15. Hoeflich, K. P., and Ikura, M. (2002) Calmodulin in action. Diversity in target recognition and activation mechanisms. Cell 108, 739-742 (Pubitemid 34327526)
16. Levy, M., Wang, Q., Kaspi, R., Parrella, M. P., and Abel, S. (2005) Arabidopsis IQD1, a novel calmodulin-binding nuclear protein, stimulates glucosinolate accumulation and plant defense. Plant J. 43, 79-96 (Pubitemid 40962737)
17. Abel, S., Savchenko, T., and Levy, M. (2005) Genome-wide comparative analysis of the IQD gene families in Arabidopsis thaliana and Oryza sativa. BMC Evol Biol 5, 72
18. Grubb, C. D., and Abel, S. (2006) Glucosinolate metabolism and its control. Trends Plant Sci. 11, 89-100 (Pubitemid 43238420)
19. Halkier, B. A., and Gershenzon, J. (2006) Biology and biochemistry of glucosinolates. Annu. Rev. Plant Biol. 57, 303-333 (Pubitemid 44061027)
20. Zentella, R., Zhang, Z. L., Park, M., Thomas, S. G., Endo, A., Murase, K., Fleet, C. M., Jikumaru, Y., Nambara, E., Kamiya, Y., and Sun, T. P. (2007) Global analysis of della direct targets in early gibberellin signaling in Arabidopsis. Plant Cell 19, 3037-3057 (Pubitemid 350276710)
21. Xiao, H., Jiang, N., Schaffner, E., Stockinger, E. J., and van der Knaap, E. (2008) A retrotransposon-mediated gene duplication underlies morphological variation of tomato fruit. Science 319, 1527-1530 (Pubitemid 351398181)
22. Wu, S., Xiao, H., Cabrera, A., Meulia, T., and van der Knaap, E. (2011)SUN regulates vegetative and reproductive organ shape by changing cell division patterns. Plant Physiol. 157, 1175-1186
23. Köhler, C., and Neuhaus, G. (2000) Characterisation of calmodulin binding to cyclic nucleotide-gated ion channels from Arabidopsis thaliana. FEBS Lett. 471, 133-136 (Pubitemid 30190051)
24. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685
25. Kim, J., Harter, K., and Theologis, A. (1997) Protein-protein interactions among the Aux/IAA proteins. Proc. Natl. Acad. Sci. U.S.A. 94, 11786-11791 (Pubitemid 127658017)
26. Karimi, M., Inzé, D., and Depicker, A. (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7, 193-195 (Pubitemid 36725938)
27. Nakagawa, T., Suzuki, T., Murata, S., Nakamura, S., Hino, T., Maeo, K., Tabata, R., Kawai, T., Tanaka, K., Niwa, Y., Watanabe, Y., Nakamura, K., Kimura, T., and Ishiguro, S. (2007) Improved Gateway binary vectors. High performance vectors for creation of fusion constructs in transgenic analysis of plants. Biosci. Biotechnol. Biochem. 71, 2095-2100 (Pubitemid 350113146)
28. Voinnet, O., Rivas, S., Mestre, P., and Baulcombe, D. (2003) An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J 33, 949-956 (Pubitemid 36339384)
29. Clough, S. J. (2005) Floral dip, Agrobacterium-mediated germ line transformation. Methods Mol. Biol. 286, 91-102
30. Müller, J., Beck, M., Mettbach, U., Komis, G., Hause, G., Menzel, D., and Samaj, J. (2010) Arabidopsis MPK6 is involved in cell division plane control during early root development and localizes to the pre-prophase band, phragmoplast, trans-Golgi network, and plasma membrane. Plant J 61, 234-248
31. Choi, M. S., Kim, M. C., Yoo, J. H., Moon, B. C., Koo, S. C., Park, B. O., Lee, J. H., Koo, Y. D., Han, H. J., Lee, S. Y., Chung, W. S., Lim, C. O., and Cho, M. J. (2005) Isolation of a calmodulin-binding transcription factor from rice (Oryza sativa L.). J. Biol. Chem. 280, 40820-40831 (Pubitemid 41780574)
32. Kang, C. H., Jung, W. Y., Kang, Y. H., Kim, J. Y., Kim, D. G., Jeong, J. C., Baek, D. W., Jin, J. B., Lee, J. Y., Kim, M. O., Chung, W. S., Mengiste, T., Koiwa, H., Kwak, S. S., Bahk, J. D., Lee, S. Y., Nam, J. S., Yun, D. J., and Cho, M. J. (2006) AtBAG6, a novel calmodulin-binding protein, induces programmed cell death in yeast and plants. Cell Death Differ. 13, 84-95
33. McCormack, E., and Braam, J. (2003) Calmodulin and related potential calcium sensors of Arabidopsis. New Phytol. 159, 585-598 (Pubitemid 37024063)
34. Verhey, K. J., Kaul, N., and Soppina, V. (2011) Kinesin assembly and movement in cells. Annu. Rev. Biophys. 40, 267-288
35. Houdusse, A., Gaucher, J. F., Krementsova, E., Mui, S., Trybus, K. M., and Cohen, C. (2006) Crystal structure of apocalmodulin bound to the first two IQ motifs of myosin V reveals essential recognition features. Proc. Natl. Acad. Sci. U.S.A. 103, 19326-19331 (Pubitemid 46026031)
36. Houdusse, A., and Cohen, C. (1995) Target sequence recognition by the calmodulin superfamily. Implications from light chain binding to the regulatory domain of scallop myosin. Proc. Natl. Acad. Sci. U.S.A. 92, 10644-10647
37. + regulates calmodulin binding to IQ motifs in IRS-1. Biochemistry 35, 15883-15889 (Pubitemid 26422327)
38. DeFalco, T. A., Chiasson, D., Munro, K., Kaiser, B. N., and Snedden, W. A. (2010) Characterization of GmCaMK1, a member of a soybean calmodulin-binding receptor-like kinase family. FEBS Lett. 584, 4717-4724
39. Bouché, N., Scharlat, A., Snedden, W., Bouchez, D., and Fromm, H. (2002) A novel family of calmodulin binding transcription activators in multicellular organisms. J. Biol. Chem. 277, 21851-21861 (Pubitemid 34952338)
40. Yang, T., and Poovaiah, B. W. (2000) An early ethylene up-regulated gene encoding a calmodulin-binding protein involved in plant senescence and death. J. Biol. Chem. 275, 38467-38473 (Pubitemid 32009172)
41. Reddy, V. S., Safadi, F., Zielinski, R. E., and Reddy, A. S. (1999) Interaction of a kinesin-like protein with calmodulin isoforms from Arabidopsis. J. Biol. Chem. 274, 31727-31733
42. Black, D. J., LaMartina, D., and Persechini, A. (2009) The IQ domains in neuromodulin and PEP19 represent two major functional classes. Biochemistry 48, 11766-11772
43. Arabidopsis Interactome Mapping Consortium (2011) Evidence for network evolution in an Arabidopsis interactome map. Science 333, 601-607
44. Dixon, D. P., Lapthorn, A., and Edwards, R. (2002) Plant glutathione transferases. Genome Biol. 3, REVIEWS3004
45. Wagner, U., Edwards, R., Dixon, D. P., and Mauch, F. (2002) Probing the diversity of the Arabidopsis glutathione S-transferase gene family. Plant Mol. Biol. 49, 515-532 (Pubitemid 34623001)
46. Dixon, D. P., Skipsey, M., and Edwards, R. (2010) Roles for glutathione transferases in plant secondary metabolism. Phytochemistry 71, 338-350
47. Dixon, D. P., and Edwards, R. (2009) Selective binding of glutathione conjugates of fatty acid derivatives by plant glutathione transferases. J. Biol. Chem. 284, 21249-21256
48. Soønderby, I. E., Geu-Flores, F., and Halkier, B. A. (2010) Biosynthesis of glucosinolates. Gene discovery and beyond. Trends Plant Sci. 15, 283-290
49. Nutricati, E., Miceli, A., Blando, F., and De Bellis, L. (2006) Characterization of two Arabidopsis thaliana glutathione S-transferases. Plant Cell Rep. 25, 997-1005 (Pubitemid 44252685)
50. Akhmanova, A., and Hammer, J. A., 3rd. (2010) Linking molecular motors to membrane cargo. Curr. Opin. Cell Biol. 22, 479-487
51. Hirokawa, N., Noda, Y., Tanaka, Y., and Niwa, S. (2009) Kinesin superfamily motor proteins and intracellular transport. Nat. Rev. Mol. Cell Biol. 10, 682-696
52. Schnapp, B. J. (2003) Trafficking of signaling modules by kinesin motors. J. Cell Sci. 116, 2125-2135 (Pubitemid 36722359)
53. Brown, M. D., and Sacks, D. B. (2009) Protein scaffolds in MAP kinase signalling. Cell Signal 21, 462-469
54. White, C. D., Brown, M. D., and Sacks, D. B. (2009) IQGAPs in cancer. A family of scaffold proteins underlying tumorigenesis. FEBS Lett. 583, 1817-1824
55. Zhu, C., and Dixit, R. (2012) Functions of the Arabidopsis kinesin superfamily of microtubule-based motor proteins. Protoplasma 249, 887-899
56. Reddy, A. S., and Day, I. S. (2001) Kinesins in the Arabidopsis genome. A comparative analysis among eukaryotes. BMC Genomics 2, 2
57. + binding protein with one EF-hand motif, interacts with a microtubule motor protein and regulates trichome morphogenesis. Plant Cell 16, 185-200 (Pubitemid 38162362)
58. Kanai, Y., Dohmae, N., and Hirokawa, N. (2004) Kinesin transports RNA. Isolation and characterization of an RNA-transporting granule. Neuron 43, 513-525 (Pubitemid 39094678)
59. Kindler, S., Wang, H., Richter, D., and Tiedge, H. (2005) RNA transport and local control of translation. Annu. Rev. Cell Dev. Biol. 21, 223-245 (Pubitemid 41740634)
60. Koroleva, O. A., Gibson, T. M., Cramer, R., and Stain, C. (2010) Glucosinolate-accumulating S-cells in Arabidopsis leaves and flower stalks undergo programmed cell death at early stages of differentiation. Plant J 64, 456-469
61. Clay, N. K., Adio, A. M., Denoux, C., Jander, G., and Ausubel, F. M. (2009) Glucosinolate metabolites required for an Arabidopsis innate immune response. Science 323, 95-101
62. Bednarek, P., Pislewska-Bednarek, M., Svatos, A., Schneider, B., Doubsky, J., Mansurova, M., Humphry, M., Consonni, C., Panstruga, R., Sanchez-Vallet, A., Molina, A., and Schulze-Lefert, P. (2009) A glucosinolate metabolism pathway in living plant cells mediates broad-spectrum antifungal defense. Science 323, 101-106