Bicc1 Polymerization Regulates the Localization and Silencing of Bound mRNA

REFERENCES

• Marchand V, Gaspar I, Ephrussi A. 2012. An intracellular transmission control protocol: assembly and transport of ribonucleoprotein complexes. Curr Opin Cell Biol 24:202–210. http://dx.doi.org/10.1016/j.ceb.2011.12.014.
   PubMedGoogle Scholar
• Kim-Ha J, Smith JL, Macdonald PM. 1991. oskar mRNA is localized to the posterior pole of the Drosophila oocyte. Cell 66:23–35. http://dx.doi.org/10.1016/0092-8674(91)90136-M.
   PubMed Web of Science ®Google Scholar
• Ephrussi A, Dickinson LK, Lehmann R. 1991. oskar organizes the germ plasm and directs localization of the posterior determinant nanos. Cell 66:37–50. http://dx.doi.org/10.1016/0092-8674(91)90137-N.
   PubMed Web of Science ®Google Scholar
• Ephrussi A, Lehmann R. 1992. Induction of germ cell formation by oskar. Nature 358:387–392. http://dx.doi.org/10.1038/358387a0.
   PubMed Web of Science ®Google Scholar
• Kim-Ha J, Kerr K, Macdonald PM. 1995. Translational regulation of oskar mRNA by bruno, an ovarian RNA-binding protein, is essential. Cell 81:403–412. http://dx.doi.org/10.1016/0092-8674(95)90393-3.
   PubMed Web of Science ®Google Scholar
• Markussen FH, Michon AM, Breitwieser W, Ephrussi A. 1995. Translational control of oskar generates short OSK, the isoform that induces pole plasma assembly. Development 121:3723–3732.
   PubMed Web of Science ®Google Scholar
• St Johnston D. 2005. Moving messages: the intracellular localization of mRNAs. Nat Rev Mol Cell Biol 6:363–375. http://dx.doi.org/10.1038/nrm1643.
   PubMed Web of Science ®Google Scholar
• Ghosh S, Marchand V, Gaspar I, Ephrussi A. 2012. Control of RNP motility and localization by a splicing-dependent structure in oskar mRNA. Nat Struct Mol Biol 19:441–449. http://dx.doi.org/10.1038/nsmb.2257.
   PubMed Web of Science ®Google Scholar
• Kim G, Pai CI, Sato K, Person MD, Nakamura A, Macdonald PM. 2015. Region-specific activation of oskar mRNA translation by inhibition of Bruno-mediated repression. PLoS Genet 11:e1004992. http://dx.doi.org/10.1371/journal.pgen.1004992.
   PubMedGoogle Scholar
• Kugler JM, Lasko P. 2009. Localization, anchoring and translational control of oskar, gurken, bicoid and nanos mRNA during Drosophila oogenesis. Fly 3:15–28. http://dx.doi.org/10.4161/fly.3.1.7751.
   PubMed Web of Science ®Google Scholar
• Bouvrette DJ, Price SJ, Bryda EC. 2008. K homology domains of the mouse polycystic kidney disease-related protein, Bicaudal-C (Bicc1), mediate RNA binding in vitro. Nephron Exp Nephrol 108:e27–e34. http://dx.doi.org/10.1159/000112913.
   PubMedGoogle Scholar
• Hollingworth D, Candel AM, Nicastro G, Martin SR, Briata P, Gherzi R, Ramos A. 2012. KH domains with impaired nucleic acid binding as a tool for functional analysis. Nucleic Acids Res 40:6873–6886. http://dx.doi.org/10.1093/nar/gks368.
   PubMed Web of Science ®Google Scholar
• Mahone M, Saffman EE, Lasko PF. 1995. Localized Bicaudal-C RNA encodes a protein containing a KH domain, the RNA binding motif of FMR1. EMBO J 14:2043–2055.
   PubMedGoogle Scholar
• Saffman EE, Styhler S, Rother K, Li W, Richard S, Lasko P. 1998. Premature translation of oskar in oocytes lacking the RNA-binding protein Bicaudal-C. Mol Cell Biol 18:4855–4862.
   PubMedGoogle Scholar
• Kugler JM, Chicoine J, Lasko P. 2009. Bicaudal-C associates with a Trailer Hitch/Me31B complex and is required for efficient Gurken secretion. Dev Biol 328:160–172. http://dx.doi.org/10.1016/j.ydbio.2009.01.024.
   PubMed Web of Science ®Google Scholar
• Chicoine J, Benoit P, Gamberi C, Paliouras M, Simonelig M, Lasko P. 2007. Bicaudal-C recruits CCR4-NOT deadenylase to target mRNAs and regulates oogenesis, cytoskeletal organization, and its own expression. Dev Cell 13:691–704. http://dx.doi.org/10.1016/j.devcel.2007.10.002.
   PubMed Web of Science ®Google Scholar
• Cogswell C, Price SJ, Hou X, Guay-Woodford LM, Flaherty L, Bryda EC. 2003. Positional cloning of jcpk/bpk locus of the mouse. Mamm Genome 14:242–249. http://dx.doi.org/10.1007/s00335-002-2241-0.
   PubMed Web of Science ®Google Scholar
• Tran U, Pickney LM, Ozpolat BD, Wessely O. 2007. Xenopus Bicaudal-C is required for the differentiation of the amphibian pronephros. Dev Biol 307:152–164. http://dx.doi.org/10.1016/j.ydbio.2007.04.030.
   PubMed Web of Science ®Google Scholar
• Kraus MR, Clauin S, Pfister Y, Di Maio M, Ulinski T, Constam D, Bellanne-Chantelot C, Grapin-Botton A. 2012. Two mutations in human BICC1 resulting in Wnt pathway hyperactivity associated with cystic renal dysplasia. Hum Mutat 33:86–90. http://dx.doi.org/10.1002/humu.21610.
   PubMed Web of Science ®Google Scholar
• Flaherty L, Messer A, Russell LB, Rinchik EM. 1992. Chlorambucil-induced mutations in mice recovered in homozygotes. Proc Natl Acad Sci U S A 89:2859–2863. http://dx.doi.org/10.1073/pnas.89.7.2859.
   PubMedGoogle Scholar
• Nauta J, Ozawa Y, Sweeney WE, Jr, Rutledge JC, Avner ED. 1993. Renal and biliary abnormalities in a new murine model of autosomal recessive polycystic kidney disease. Pediatr Nephrol 7:163–172. http://dx.doi.org/10.1007/BF00864387.
   PubMedGoogle Scholar
• Ryan S, Verghese S, Cianciola NL, Cotton CU, Carlin CR. 2010. Autosomal recessive polycystic kidney disease epithelial cell model reveals multiple basolateral epidermal growth factor receptor sorting pathways. Mol Biol Cell 21:2732–2745. http://dx.doi.org/10.1091/mbc.E09-12-1059.
   PubMedGoogle Scholar
• Kotsis F, Boehlke C, Kuehn EW. 2013. The ciliary flow sensor and polycystic kidney disease. Nephrol Dial Transplant 28:518–526. http://dx.doi.org/10.1093/ndt/gfs524.
   PubMedGoogle Scholar
• Wang S, Zhang J, Nauli SM, Li X, Starremans PG, Luo Y, Roberts KA, Zhou J. 2007. Fibrocystin/polyductin, found in the same protein complex with polycystin-2, regulates calcium responses in kidney epithelia. Mol Cell Biol 27:3241–3252. http://dx.doi.org/10.1128/MCB.00072-07.
   PubMed Web of Science ®Google Scholar
• Lian P, Li A, Li Y, Liu H, Liang D, Hu B, Lin D, Jiang T, Moeckel G, Qin D, Wu G. 2014. Loss of polycystin-1 inhibits Bicc1 expression during mouse development. PLoS One 9:e88816. http://dx.doi.org/10.1371/journal.pone.0088816.
   PubMedGoogle Scholar
• Tran U, Zakin L, Schweickert A, Agrawal R, Doger R, Blum M, De Robertis EM, Wessely O. 2010. The RNA-binding protein bicaudal C regulates polycystin 2 in the kidney by antagonizing miR-17 activity. Development 137:1107–1116. http://dx.doi.org/10.1242/dev.046045.
   PubMed Web of Science ®Google Scholar
• Piazzon N, Maisonneuve C, Guilleret I, Rotman S, Constam DB. 2012. Bicc1 links the regulation of cAMP signaling in polycystic kidneys to microRNA-induced gene silencing. J Mol Cell Biol 4:398–408. http://dx.doi.org/10.1093/jmcb/mjs027.
   PubMedGoogle Scholar
• Gattone VH, II, Wang X, Harris PC, Torres VE. 2003. Inhibition of renal cystic disease development and progression by a vasopressin V2 receptor antagonist. Nat Med 9:1323–1326. http://dx.doi.org/10.1038/nm935.
   PubMed Web of Science ®Google Scholar
• Rees S, Kittikulsuth W, Roos K, Strait KA, Van Hoek A, Kohan DE. 2014. Adenylyl cyclase 6 deficiency ameliorates polycystic kidney disease. J Am Soc Nephrol 25:232–237. http://dx.doi.org/10.1681/ASN.2013010077.
   PubMed Web of Science ®Google Scholar
• Harris PC, Torres VE. 2014. Genetic mechanisms and signaling pathways in autosomal dominant polycystic kidney disease. J Clin Invest 124:2315–2324. http://dx.doi.org/10.1172/JCI72272.
   PubMed Web of Science ®Google Scholar
• Lee DC, Chan KW, Chan SY. 1998. Expression of transforming growth factor alpha and epidermal growth factor receptor in adult polycystic kidney disease. J Urol 159:291–296. http://dx.doi.org/10.1016/S0022-5347(01)64084-9.
   PubMed Web of Science ®Google Scholar
• Sweeney WE, Jr, Avner ED. 1998. Functional activity of epidermal growth factor receptors in autosomal recessive polycystic kidney disease. Am J Physiol 275:F387–F394.
   PubMed Web of Science ®Google Scholar
• Dell KM, Nemo R, Sweeney WE, Jr, Levin JI, Frost P, Avner ED. 2001. A novel inhibitor of tumor necrosis factor-alpha converting enzyme ameliorates polycystic kidney disease. Kidney Int 60:1240–1248. http://dx.doi.org/10.1046/j.1523-1755.2001.00963.x.
   PubMed Web of Science ®Google Scholar
• Shillingford JM, Murcia NS, Larson CH, Low SH, Hedgepeth R, Brown N, Flask CA, Novick AC, Goldfarb DA, Kramer-Zucker A, Walz G, Piontek KB, Germino GG, Weimbs T. 2006. The mTOR pathway is regulated by polycystin-1, and its inhibition reverses renal cystogenesis in polycystic kidney disease. Proc Natl Acad Sci U S A 103:5466–5471. http://dx.doi.org/10.1073/pnas.0509694103.
   PubMed Web of Science ®Google Scholar
• Maisonneuve C, Guilleret I, Vick P, Weber T, Andre P, Beyer T, Blum M, Constam DB. 2009. Bicaudal C, a novel regulator of Dvl signaling abutting RNA-processing bodies, controls cilia orientation and leftward flow. Development 136:3019–3030. http://dx.doi.org/10.1242/dev.038174.
   PubMedGoogle Scholar
• Pennekamp P, Menchen T, Dworniczak B, Hamada H. 2015. Situs inversus and ciliary abnormalities: 20 years later, what is the connection? Cilia 4:1. http://dx.doi.org/10.1186/s13630-014-0010-9.
   PubMedGoogle Scholar
• Ponting CP. 1995. SAM: a novel motif in yeast sterile and Drosophila polyhomeotic proteins. Protein Sci 4:1928–1930. http://dx.doi.org/10.1002/pro.5560040927.
   PubMed Web of Science ®Google Scholar
• Carroll M, Tomasson MH, Barker GF, Golub TR, Gilliland DG. 1996. The TEL/platelet-derived growth factor beta receptor (PDGF beta R) fusion in chronic myelomonocytic leukemia is a transforming protein that self-associates and activates PDGF beta R kinase-dependent signaling pathways. Proc Natl Acad Sci U S A 93:14845–14850. http://dx.doi.org/10.1073/pnas.93.25.14845.
   PubMed Web of Science ®Google Scholar
• Meruelo AD, Bowie JU. 2009. Identifying polymer-forming SAM domains. Proteins 74:1–5. http://dx.doi.org/10.1002/prot.22232.
   PubMedGoogle Scholar
• Kim CA, Gingery M, Pilpa RM, Bowie JU. 2002. The SAM domain of polyhomeotic forms a helical polymer. Nat Struct Biol 9:453–457.
   PubMedGoogle Scholar
• Tran HH, Kim CA, Faham S, Siddall MC, Bowie JU. 2002. Native interface of the SAM domain polymer of TEL. BMC Struct Biol 2:5. http://dx.doi.org/10.1186/1472-6807-2-5.
   PubMedGoogle Scholar
• Knight MJ, Leettola C, Gingery M, Li H, Bowie JU. 2011. A human sterile alpha motif domain polymerizome. Protein Sci 20:1697–1706. http://dx.doi.org/10.1002/pro.703.
   PubMedGoogle Scholar
• Korinek V, Barker N, Morin PJ, van Wichen D, de Weger R, Kinzler KW, Vogelstein B, Clevers H. 1997. Constitutive transcriptional activation by a beta-catenin-Tcf complex in APC−/− colon carcinoma. Science 275:1784–1787. http://dx.doi.org/10.1126/science.275.5307.1784.
   PubMed Web of Science ®Google Scholar
• Schwarz-Romond T, Metcalfe C, Bienz M. 2007. Dynamic recruitment of axin by Dishevelled protein assemblies. J Cell Sci 120:2402–2412. http://dx.doi.org/10.1242/jcs.002956.
   PubMed Web of Science ®Google Scholar
• Cougot N, Babajko S, Seraphin B. 2004. Cytoplasmic foci are sites of mRNA decay in human cells. J Cell Biol 165:31–40. http://dx.doi.org/10.1083/jcb.200309008.
   PubMed Web of Science ®Google Scholar
• National Research Council. 2011. Guide for the care and use of laboratory animals, 8th ed. National Academies Press, Washington, DC.
   Google Scholar
• Harada BT, Knight MJ, Imai S, Qiao F, Ramachander R, Sawaya MR, Gingery M, Sakane F, Bowie JU. 2008. Regulation of enzyme localization by polymerization: polymer formation by the SAM domain of diacylglycerol kinase delta1. Structure 16:380–387. http://dx.doi.org/10.1016/j.str.2007.12.017.
   PubMedGoogle Scholar
• Arnold K, Bordoli L, Kopp J, Schwede T. 2006. The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22:195–201. http://dx.doi.org/10.1093/bioinformatics/bti770.
   PubMed Web of Science ®Google Scholar
• Eswar N, Webb B, Marti-Renom MA, Madhusudhan MS, Eramian D, Shen MY, Pieper U, Sali A. 2006. Comparative protein structure modeling using Modeller. Curr Protoc Bioinformatics Chapter 5:Unit 5.6. http://dx.doi.org/10.1002/0471250953.bi0506s15.
   PubMedGoogle Scholar
• Shen MY, Sali A. 2006. Statistical potential for assessment and prediction of protein structures. Protein Sci 15:2507–2524. http://dx.doi.org/10.1110/ps.062416606.
   PubMed Web of Science ®Google Scholar
• Pronk S, Pall S, Schulz R, Larsson P, Bjelkmar P, Apostolov R, Shirts MR, Smith JC, Kasson PM, van der Spoel D, Hess B, Lindahl E. 2013. GROMACS 4.5: a high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics 29:845–854. http://dx.doi.org/10.1093/bioinformatics/btt055.
   PubMed Web of Science ®Google Scholar
• Morse PM, Feshbach H. 1953. Asymptotic series; method of steepest descent, p 434–443. Methods of theoretical physics, part I. McGraw-Hill, New York, NY.
   Google Scholar
• Mackerell AD, Jr, Feig M, Brooks CL, III. 2004. Extending the treatment of backbone energetics in protein force fields: limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations. J Comput Chem 25:1400–1415. http://dx.doi.org/10.1002/jcc.20065.
   PubMed Web of Science ®Google Scholar
• Flaherty L, Bryda EC, Collins D, Rudofsky U, Montgomery JC. 1995. New mouse model for polycystic kidney disease with both recessive and dominant gene effects. Kidney Int 47:552–558. http://dx.doi.org/10.1038/ki.1995.69.
   PubMedGoogle Scholar
• Bertrand E, Chartrand P, Schaefer M, Shenoy SM, Singer RH, Long RM. 1998. Localization of ASH1 mRNA particles in living yeast. Mol Cell 2:437–445. http://dx.doi.org/10.1016/S1097-2765(00)80143-4.
   PubMed Web of Science ®Google Scholar
• Fu Y, Kim I, Lian P, Li A, Zhou L, Li C, Liang D, Coffey RJ, Ma J, Zhao P, Zhan Q, Wu G. 2010. Loss of Bicc1 impairs tubulomorphogenesis of cultured IMCD cells by disrupting E-cadherin-based cell-cell adhesion. Eur J Cell Biol 89:428–436. http://dx.doi.org/10.1016/j.ejcb.2010.01.002.
   PubMedGoogle Scholar
• Qiao F, Bowie JU. 2005. The many faces of SAM. Sci STKE 2005:re7.
   PubMedGoogle Scholar
• Nakel K, Hartung SA, Bonneau F, Eckmann CR, Conti E. 2010. Four KH domains of the C. elegans Bicaudal-C ortholog GLD-3 form a globular structural platform. RNA 16:2058–2067. http://dx.doi.org/10.1261/rna.2315010.
   PubMedGoogle Scholar
• Hofmann I, Casella M, Schnolzer M, Schlechter T, Spring H, Franke WW. 2006. Identification of the junctional plaque protein plakophilin 3 in cytoplasmic particles containing RNA-binding proteins and the recruitment of plakophilins 1 and 3 to stress granules. Mol Biol Cell 17:1388–1398.
   PubMed Web of Science ®Google Scholar
• Stagner EE, Bouvrette DJ, Cheng J, Bryda EC. 2009. The polycystic kidney disease-related proteins Bicc1 and SamCystin interact. Biochem Biophys Res Commun 383:16–21. http://dx.doi.org/10.1016/j.bbrc.2009.03.113.
   PubMedGoogle Scholar
• Hoff S, Halbritter J, Epting D, Frank V, Nguyen TM, van Reeuwijk J, Boehlke C, Schell C, Yasunaga T, Helmstadter M, Mergen M, Filhol E, Boldt K, Horn N, Ueffing M, Otto EA, Eisenberger T, Elting MW, van Wijk JA, Bockenhauer D, Sebire NJ, Rittig S, Vyberg M, Ring T, Pohl M, Pape L, Neuhaus TJ, Elshakhs NA, Koon SJ, Harris PC, Grahammer F, Huber TB, Kuehn EW, Kramer-Zucker A, Bolz HJ, Roepman R, Saunier S, Walz G, Hildebrandt F, Bergmann C, Lienkamp SS. 2013. ANKS6 is a central component of a nephronophthisis module linking NEK8 to INVS and NPHP3. Nat Genet 45:951–956. http://dx.doi.org/10.1038/ng.2681.
   PubMed Web of Science ®Google Scholar
• Taskiran EZ, Korkmaz E, Gucer S, Kosukcu C, Kaymaz F, Koyunlar C, Bryda EC, Chaki M, Lu D, Vadnagara K, Candan C, Topaloglu R, Schaefer F, Attanasio M, Bergmann C, Ozaltin F. 2014. Mutations in ANKS6 cause a nephronophthisis-like phenotype with ESRD. J Am Soc Nephrol 25:1653–1661. http://dx.doi.org/10.1681/ASN.2013060646.
   PubMedGoogle Scholar
• Leettola CN, Knight MJ, Cascio D, Hoffman S, Bowie JU. 2014. Characterization of the SAM domain of the PKD-related protein ANKS6 and its interaction with ANKS3. BMC Struct Biol 14:17. http://dx.doi.org/10.1186/1472-6807-14-17.
   PubMedGoogle Scholar
• Yakulov TA, Yasunaga T, Ramachandran H, Engel C, Muller B, Hoff S, Dengjel J, Lienkamp SS, Walz G. 2015. Anks3 interacts with nephronophthisis proteins and is required for normal renal development. Kidney Int 87:1191–1200. http://dx.doi.org/10.1038/ki.2015.17.
   PubMedGoogle Scholar
• Zhang Y, Cooke A, Park S, Dewey CN, Wickens M, Sheets MD. 2013. Bicaudal-C spatially controls translation of vertebrate maternal mRNAs. RNA 19:1575–1582. http://dx.doi.org/10.1261/rna.041665.113.
   PubMedGoogle Scholar
• Zhou HX, Rivas G, Minton AP. 2008. Macromolecular crowding and confinement: biochemical, biophysical, and potential physiological consequences. Annu Rev Biophys 37:375–397. http://dx.doi.org/10.1146/annurev.biophys.37.032807.125817.
   PubMed Web of Science ®Google Scholar
• Kertesz M, Iovino N, Unnerstall U, Gaul U, Segal E. 2007. The role of site accessibility in microRNA target recognition. Nat Genet 39:1278–1284. http://dx.doi.org/10.1038/ng2135.
   PubMed Web of Science ®Google Scholar
• Kedde M, van Kouwenhove M, Zwart W, Oude Vrielink JA, Elkon R, Agami R. 2010. A Pumilio-induced RNA structure switch in p27-3′ UTR controls miR-221 and miR-222 accessibility. Nat Cell Biol 12:1014–1020. http://dx.doi.org/10.1038/ncb2105.
   PubMed Web of Science ®Google Scholar
• Miles WO, Tschop K, Herr A, Ji JY, Dyson NJ. 2012. Pumilio facilitates miRNA regulation of the E2F3 oncogene. Genes Dev 26:356–368. http://dx.doi.org/10.1101/gad.182568.111.
   PubMedGoogle Scholar
• Isono K, Endo TA, Ku M, Yamada D, Suzuki R, Sharif J, Ishikura T, Toyoda T, Bernstein BE, Koseki H. 2013. SAM domain polymerization links subnuclear clustering of PRC1 to gene silencing. Dev Cell 26:565–577. http://dx.doi.org/10.1016/j.devcel.2013.08.016.
   PubMed Web of Science ®Google Scholar
• Qiao F, Song H, Kim CA, Sawaya MR, Hunter JB, Gingery M, Rebay I, Courey AJ, Bowie JU. 2004. Derepression by depolymerization; structural insights into the regulation of Yan by Mae. Cell 118:163–173. http://dx.doi.org/10.1016/j.cell.2004.07.010.
   PubMedGoogle Scholar