Identifying domains of EFHC1 involved in ciliary localization, ciliogenesis, and the regulation of Wnt signaling

Developmental Biology

Volumn 411, Issue 2, 2016, Pages 257-265

  Zhao, Ying ^a   Shi, Jianli ^a   Winey, Mark ^a   Klymkowsky, Michael W ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

Biological science: Cell biology; Ciliogenesis; Developmental biology; Myoclonic epilepsy; Wnt signaling; Xenopus embryo

Indexed keywords

BETA CATENIN; CALCIUM BINDING PROTEIN; EFHC1 PROTEIN; EFHC1B PROTEIN; UNCLASSIFIED DRUG; WNT8A PROTEIN; EFHC1 PROTEIN, XENOPUS; GREEN FLUORESCENT PROTEIN; RNA; WNT PROTEIN; WNT8A PROTEIN, XENOPUS; XENOPUS PROTEIN;

ANIMAL TISSUE; ARTICLE; AUTOCRINE EFFECT; AXONEME; CILIATED EPITHELIUM CELL; CILIOGENESIS; CONTROLLED STUDY; DOWN REGULATION; ECTODERM; EMBRYO; EMBRYO PATTERN FORMATION; EUKARYOTIC FLAGELLUM; NEURAL CREST; NEURAL TUBE; NONHUMAN; ORGANELLE BIOGENESIS; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; WNT SIGNALING PATHWAY; XENOPUS LAEVIS; ANIMAL; CONFOCAL MICROSCOPY; CYTOLOGY; EMBRYOLOGY; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; METABOLISM; MORPHOGENESIS; MUTATION; PHENOTYPE; PROTEIN TERTIARY STRUCTURE; REPORTER GENE; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; BETA CATENIN; CALCIUM-BINDING PROTEINS; CILIA; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MICROSCOPY, CONFOCAL; MORPHOGENESIS; MUTATION; NEURAL CREST; NEURAL TUBE; PHENOTYPE; PROTEIN STRUCTURE, TERTIARY; RNA; SIGNAL TRANSDUCTION; UP-REGULATION; WNT PROTEINS; WNT SIGNALING PATHWAY; XENOPUS LAEVIS; XENOPUS PROTEINS;

EID: 84959572539     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2016.01.004     Document Type: Article

References (54)

1. Araki M., Masutani C., Takemura M., Uchida A., Sugasawa K., Kondoh J., Ohkuma Y., Hanaoka F. Centrosome protein centrin 2/caltractin 1 is part of the xeroderma pigmentosum group C complex that initiates global genome nucleotide excision repair. J. Biol. Chem. 2001, 276:18665-18672.
2. Bai D., Bailey J.N., Duron R.M., Alonso M.E., Medina M.T., Martinez-Juarez I.E., Suzuki T., Machado-Salas J., Ramos-Ramirez R., Tanaka M., et al. DNA variants in coding region of EFHC1: SNPs do not associate with juvenile myoclonic epilepsy. Epilepsia 2009, 50:1184-1190.
3. Blaya C., Moorjani P., Salum G.A., Gonçalves L., Weiss L.A., Leistner-Segal S., Manfro G.G., Smoller J.W. Preliminary evidence of association between EFHC2, a gene implicated in fear recognition, and harm avoidance. Neurosci. Lett. 2009, 452:84-86.
4. Bradley L., Sun B., Collins-Racie L., LaVallie E., McCoy J., Sive H. Different activities of the frizzled-related proteins frzb2 and sizzled2 during Xenopus anteroposterior patterning. Dev. Biol. 2000, 227:118-132.
5. Brooks E.R., Wallingford J.B. In vivo investigation of cilia structure and function using Xenopus. Methods Cell. Biol. 2015, 127:131-159.
6. Brown J., Witman G. Cilia and diseases. BioScience 2014, 64:1126-1137.
7. Chu D.T.W., Klymkowsky M.W. The appearance of acetylated alpha-tubulin during early development and cellular differentiation in Xenopus. Dev. Biol. 1989, 136:104-117.
8. Cunningham C.N., Schmidt C.A., Schramm N.J., Gaylord M.R., Resendes K.K. Human TREX2 components PCID2 and centrin 2, but not ENY2, have distinct functions in protein export and co-localize to the centrosome. Exp. Cell. Res. 2014, 320:209-218.
9. de Nijs L., Wolkoff N., Grisar T., Lakaye B. Juvenile myoclonic epilepsy as a possible neurodevelopmental disease: Role of EFHC1 or Myoclonin1. Epilepsy Behav. 2013, 28:S58-S60.
10. Dent J.A., Polson A.G., Klymkowsky M.W. A whole-mount immunocytochemical analysis of the expression of the intermediate filament protein vimentin in Xenopus. Development 1989, 105:61-74.
11. Dubaissi E., Papalopulu N. Embryonic frog epidermis: a model for the study of cell-cell interactions in the development of mucociliary disease. Dis. Model. Mech. 2011, 4:179-192.
12. Ferkol T.W., Leigh M.W. Ciliopathies: the central role of cilia in a spectrum of pediatric disorders. J. Pediatr. 2012, 160:366-371.
13. Gerdes J.M., Liu Y., Zaghloul N.A., Leitch C.C., Lawson S.S., Kato M., Beachy P.A., Beales P.L., DeMartino G.N., Fisher S. Disruption of the basal body compromises proteasomal function and perturbs intracellular Wnt response. Nat. Genet. 2007, 39:1350-1360.
14. Glinka A., Wu W., Delius H., Monaghan A.P., Blumenstock C., Niehrs C. Dickkopf-1 is a member of a new family of secreted proteins and functions in head induction. Nature 1998, 391:357-362.
15. Gu W., Sander T.L., Heils A., Lenzen K.P., Steinlein O.K. A new EF-hand containing gene EFHC2 on Xp11. 4: Tentative evidence for association with juvenile myoclonic epilepsy. Epilepsy Res. 2005, 66:91-98.
16. Hildebrandt F., Benzing T., Katsanis N. Ciliopathies. N. Engl. J. Med. 2011, 364:1533-1543.
17. Ikeda K., Brown J.A., Yagi T., Norrander J.M., Hirono M., Eccleston E., Kamiya R., Linck R.W. Rib72, a conserved protein associated with the ribbon compartment of flagellar A-microtubules and potentially involved in the linkage between outer doublet microtubules. J. Biol. Chem. 2003, 278:7725-7734.
18. Ikeda T., Ikeda K., Enomoto M., Park M.K., Hirono M., Kamiya R. The mouse ortholog of EFHC1 implicated in juvenile myoclonic epilepsy is an axonemal protein widely conserved among organisms with motile cilia and flagella. FEBS Lett. 2005, 579:819-822.
19. Karpinka J.B., Fortriede J.D., Burns K.A., James-Zorn C., Ponferrada V.G., Lee J., Karimi K., Zorn A.M., Vize P.D. Xenbase, the Xenopus model organism database; new virtualized system, data types and genomes. Nucleic acids research 2015, 43:D756-D763.
20. Katano M., Numata T., Aguan K., Hara Y., Kiyonaka S., Yamamoto S., Miki T., Sawamura S., Suzuki T., Yamakawa K., et al. The juvenile myoclonic epilepsy-related protein EFHC1 interacts with the redox-sensitive TRPM2 channel linked to cell death. Cell. Calcium 2012, 51:179-185.
21. Kilburn C.L., Pearson C.G., Romijn E.P., Meehl J.B., Giddings T.H., Culver B.P., Yates J.R., Winey M. New Tetrahymena basal body protein components identify basal body domain structure. J. Cell. Biol. 2007, 178:905-912.
22. Kim K.D., Lake B.B., Haremaki T., Weinstein D.C., Sokol S.Y. Rab11 regulates planar polarity and migratory behavior of multiciliated cells in Xenopus embryonic epidermis. Dev. Dyn. 2012, 241:1385-1395.
23. King S.M. Axonemal protofilament ribbons, DM10 domains, and the link to juvenile myoclonic epilepsy. Cell. Motil. Cytoskelet. 2006, 63:245-253.
24. Li F.-Q., Mofunanya A., Harris K., Takemaru K.-I. Chibby cooperates with 14-3-3 to regulate β-catenin subcellular distribution and signaling activity. J. Cell. Biol. 2008, 181:1141-1154.
25. Liu Y.P., Tsai I.-C., Morleo M., Oh E.C., Leitch C.C., Massa F., Lee B.-H., Parker D.S., Finley D., Zaghloul N.A. Ciliopathy proteins regulate paracrine signaling by modulating proteasomal degradation of mediators. The Journal of clinical investigation 2014, 124:2059.
26. Merriam J.M., Rubenstein A.B., Klymkowsky M.W. Cytoplasmically anchored plakoglobin induces a WNT-like phenotype in Xenopus. Dev. Biol. 1997, 185:67-81.
27. Nieuwkoop P.D., Faber J. Normal table of Xenopus laevis (Daudin): A Systematical and Chronological Survey of the Development from the Fertilized Egg till the end of Metamorphosis 1967, Amsterdam Publishing Company, Amsterdam, New York, republished in 1994 by Garland Publishing.
28. Pal Deb, Helbig Ingo Commentary: Pathogenic EFHC1 mutations are tolerated in healthy individuals dependent on reported ancestry. Epilepsia 2015, 56:195-196.
29. Park L., Wang G., Moore J., Girouard H., Zhou P., Anrather J., Iadecola C. The key role of transient receptor potential melastatin-2 channels in amyloid-β-induced neurovascular dysfunction. Nature communications 2014, 5:5318.
30. Rossetto M.G., Zanarella E., Orso G., Scorzeto M., Megighian A., Kumar V., Delgado-Escueta A.V., Daga A. Defhc1.1, a homologue of the juvenile myoclonic gene EFHC1, modulates architecture and basal activity of the neuromuscular junction in Drosophila. Hum. Mol. Genet. 2011, 20:4248-4257.
31. Rossi A., Kontarakis Z., Gerri C., Nolte H., Hölper S., Krüger M., Stainier D.Y. Genetic compensation induced by deleterious mutations but not gene knockdowns. Nature 2015, 524:230-233.
32. Sahni N., Yi S., Taipale M., Bass J., Coulombe-Huntington J., Yang F., Peng J., Weile J., Karras G.I., Wang Y. Widespread macromolecular interaction perturbations in human genetic disorders. Cell 2015, 161:647-660.
33. Setter P., Malvey-Dorn E., Steffen W., Stephens R., Linck R. Tektin interactions and a model for molecular functions. Exp. Cell. Res. 2006, 312:2880-2896.
34. Shi J., Severson C., Yang J., Wedlich D., Klymkowsky M.W. Snail2 controls BMP/Wnt mesodermal induction of neural crest. Development 2011, 138:3135-3145.
35. Shi J., Zhao Y., Galati N., Winey M., Klymkowsky M.W. Chibby functions in Xenopus ciliary assembly, embryonic development, and the regulation of gene expression. Dev. Biol. 2014, 395:287-298.
36. Shi, J., Zhou, Y., Vonderfecht, T., Winey, M. and Klymkowsky, M.W. (2015). Centrin-2 (Cetn2) mediated regulation of FGF/FGFR gene expression in Xenopus. Scientific Reports 5:10283.
37. Sive H.L., Grainger R.M., Harland R.M. Early development of Xenopus laevis: a laboratory manual. Cold Spring Harbor 2000, Cold Spring Harbor Laboratory Press.
38. Steinman R.M. An electron microscopic study of ciliogenesis in developing epidermis and trachea in the embryo of Xenopus laevis. Am. J. Anat. 1968, 122:19-55.
39. Stogmann E., Lichtner P., Baumgartner C., Bonelli S., Assem-Hilger E., Leutmezer F., Schmied M., Hotzy C., Strom T.M., Meitinger T., et al. Idiopathic generalized epilepsy phenotypes associated with different EFHC1 mutations. Neurology 2006, 67:2029-2031.
40. Subaran Ryan, L., Conte Juliette, M., Stewart William, C.L., Greenberg David, A. Pathogenic EFHC1 mutations are tolerated in healthy individuals dependent on reported ancestry. Epilepsia 2015, 56:188-194.
41. Suzuki T., Delgado-Escueta A.V., Aguan K., Alonso M.E., Shi J., Hara Y., Nishida M., Numata T., Medina M.T., Takeuchi T., et al. Mutations in EFHC1 cause juvenile myoclonic epilepsy. Nat. Genet. 2004, 36:842-849.
42. Suzuki T., Inoue I., Yamagata T., Morita N., Furuichi T., Yamakawa K. Sequential expression of Efhc1/myoclonin1 in choroid plexus and ependymal cell cilia. Biochem. Biophys. Res. Commun. 2008, 367:226-233.
43. Suzuki T., Miyamoto H., Nakahari T., Inoue I., Suemoto T., Jiang B., Hirota Y., Itohara S., Saido T.C., Tsumoto T., et al. Efhc1 deficiency causes spontaneous myoclonus and increased seizure susceptibility. Hum. Mol. Genet. 2009, 18:1099-1109.
44. Takemaru K., Yamaguchi S., Lee Y.S., Zhang Y., Carthew R.W., Moon R.T. Chibby, a nuclear beta-catenin-associated antagonist of the Wnt/Wingless pathway. Nature 2003, 422:905-909.
45. Takemaru K.-I., Fischer V., Li F.-Q. Fine-tuning of nuclear β-catenin by Chibby and 14-3-3. Cell. Cycle 2009, 8:210-213.
46. von Podewils F., Kowoll V., Schroeder W., Geithner J., Wang Z., Gaida B., Bombach P., Kessler C., Felbor U., Runge U. Predictive value of EFHC1 variants for the long-term seizure outcome in juvenile myoclonic epilepsy. Epilepsy Behav. 2015, 44:61-66.
47. Wallingford J.B., Mitchell B. Strange as it may seem: the many links between Wnt signaling, planar cell polarity, and cilia. Genes. Dev. 2011, 25:201-213.
48. Weiss L.A., Purcell S., Waggoner S., Lawrence K., Spektor D., Daly M.J., Sklar P., Skuse D. Identification of EFHC2 as a quantitative trait locus for fear recognition in Turner syndrome. Hum. Mol. Genet. 2007, 16:107-113.
49. Werner M.E., Mitchell B.J. Understanding ciliated epithelia: the power of Xenopus. Genesis 2012, 50:176-185.
50. Yamakawa K., Suzuki T. Re-evaluation of myoclonin1 immunosignals in neuron, mitotic spindle, and midbody-Nonspecific?. Epilepsy Behav. 2013, 28:S61-S62.
51. Yanai I., Peshkin L., Jorgensen P., Kirschner M.W. Mapping gene expression in two Xenopus species: evolutionary constraints and developmental flexibility. Dev. Cell. 2011, 20:483-496.
52. 3 regulation. Development 2003, 130:5609-5624.
53. Zhang C., Carl T.F., Trudeau E.D., Simmet T., Klymkowsky M.W. An NF-kappaB and slug regulatory loop active in early vertebrate mesoderm. PLoS ONE 2006, 1:e106.
54. Zhang C., Klymkowsky M.W. Unexpected functional redundancy between Twist and Slug (Snail2) and their feedback regulation of NF-kappaB via Nodal and Cerberus. Dev. Biol. 2009, 331:340-349.