Scp160-Dependent mRNA Trafficking Mediates Pheromone Gradient Sensing and Chemotropism in Yeast

Cell Reports

Volumn 1, Issue 5, 2012, Pages 483-494

  Gelin Licht, Rita ^a,b   Paliwal, Saurabh ^b   Conlon, Patrick ^b   Levchenko, Andre ^b   Gerst, Jeffrey E ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b Johns Hopkins University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; MESSENGER RNA; MYOSIN IV; PHEROMONE RECEPTOR; PROTEIN SCP160; PROTEIN SHE2; PROTEIN SHE3; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CHEMICAL PHENOMENA; CHEMOTROPISM; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; FUNGUS GROWTH; MATING; NONHUMAN; PHEROMONE GRADIENT SENSING; PROTEIN RNA BINDING; RNA TRANSLATION; RNA TRANSPORT; YEAST;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CELL DIVISION; CELL POLARITY; CHEMOTAXIS; GTP-BINDING PROTEIN ALPHA SUBUNITS; MYOSIN HEAVY CHAINS; MYOSIN TYPE V; PHEROMONES; RNA, MESSENGER; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TROPISM;

EUKARYOTA;

EID: 84861702462     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2012.03.004     Document Type: Article

References (49)

1. Affolter M., Weijer C.J. Signaling to cytoskeletal dynamics during chemotaxis. Dev. Cell 2005, 9:19-34.
2. Aronov S., Gelin-Licht R., Zipor G., Haim L., Safran E., Gerst J.E. mRNAs encoding polarity and exocytosis factors are cotransported with the cortical endoplasmic reticulum to the incipient bud in Saccharomyces cerevisiae. Mol. Cell. Biol. 2007, 27:3441-3455.
3. Bassell G.J., Taneja K.L., Kislauskis E.H., Sundell C.L., Powers C.M., Ross A., Singer R.H. Actin filaments and the spatial positioning of mRNAS. Adv. Exp. Med. Biol. 1994, 358:183-189.
4. Baum S., Bittins M., Frey S., Seedorf M. Asc1p, a WD40-domain containing adaptor protein, is required for the interaction of the RNA-binding protein Scp160p with polysomes. Biochem. J. 2004, 380:823-830.
5. Betschinger J., Knoblich J.A. Dare to be different: asymmetric cell division in Drosophila, C. elegans and vertebrates. Curr. Biol. 2004, 14:R674-R685.
6. Blumer K.J., Thorner J. Receptor-G protein signaling in yeast. Annu. Rev. Physiol. 1991, 53:37-57.
7. Bramham C.R., Wells D.G. Dendritic mRNA: transport, translation and function. Nat. Rev. Neurosci. 2007, 8:776-789.
8. Bretscher A. Polarized growth and organelle segregation in yeast: the tracks, motors, and receptors. J. Cell Biol. 2003, 160:811-816.
9. Brykailo M.A., Corbett A.H., Fridovich-Keil J.L. Functional overlap between conserved and diverged KH domains in Saccharomyces cerevisiae SCP160. Nucleic Acids Res. 2007, 35:1108-1118.
10. Casamayor A., Snyder M. Bud-site selection and cell polarity in budding yeast. Curr. Opin. Microbiol. 2002, 5:179-186.
11. Dodson R.E., Shapiro D.J. An estrogen-inducible protein binds specifically to a sequence in the 3' untranslated region of estrogen-stabilized vitellogenin mRNA. Mol. Cell. Biol. 1994, 14:3130-3138.
12. Dohlman H.G. G proteins and pheromone signaling. Annu. Rev. Physiol. 2002, 64:129-152.
13. Drubin D.G., Nelson W.J. Origins of cell polarity. Cell 1996, 84:335-344.
14. Estrada P., Kim J., Coleman J., Walker L., Dunn B., Takizawa P., Novick P., Ferro-Novick S. Myo4p and She3p are required for cortical ER inheritance in Saccharomyces cerevisiae. J. Cell Biol. 2003, 163:1255-1266.
15. Frey S., Pool M., Seedorf M. Scp160p, an RNA-binding, polysome-associated protein, localizes to the endoplasmic reticulum of Saccharomyces cerevisiae in a microtubule-dependent manner. J. Biol. Chem. 2001, 276:15905-15912.
16. Gerst J.E. Message on the web: mRNA and ER co-trafficking. Trends Cell Biol. 2008, 18:68-76.
17. Grote E. Cell fusion assays for yeast mating pairs. Methods Mol. Biol. 2008, 475:165-196.
18. Guo M., Aston C., Burchett S.A., Dyke C., Fields S., Rajarao S.J., Uetz P., Wang Y., Young K., Dohlman H.G. The yeast G protein alpha subunit Gpa1 transmits a signal through an RNA binding effector protein Scp160. Mol. Cell 2003, 12:517-524.
19. Haim L., Zipor G., Aronov S., Gerst J.E. A genomic integration method to visualize localization of endogenous mRNAs in living yeast. Nat. Methods 2007, 4:409-412.
20. Huh W.K., Falvo J.V., Gerke L.C., Carroll A.S., Howson R.W., Weissman J.S., O'Shea E.K. Global analysis of protein localization in budding yeast. Nature 2003, 425:686-691.
21. Irie K., Tadauchi T., Takizawa P.A., Vale R.D., Matsumoto K., Herskowitz I. The Khd1 protein, which has three KH RNA-binding motifs, is required for proper localization of ASH1 mRNA in yeast. EMBO J. 2002, 21:1158-1167.
22. Jansen R.P., Dowzer C., Michaelis C., Galova M., Nasmyth K. Mother cell-specific HO expression in budding yeast depends on the unconventional myosin myo4p and other cytoplasmic proteins. Cell 1996, 84:687-697.
23. Lang B.D., Fridovich-Keil J.L. Scp160p, a multiple KH-domain protein, is a component of mRNP complexes in yeast. Nucleic Acids Res. 2000, 28:1576-1584.
24. Lange S., Katayama Y., Schmid M., Burkacky O., Bräuchle C., Lamb D.C., Jansen R.P. Simultaneous transport of different localized mRNA species revealed by live-cell imaging. Traffic 2008, 9:1256-1267.
25. Li A.M., Watson A., Fridovich-Keil J.L. Scp160p associates with specific mRNAs in yeast. Nucleic Acids Res. 2003, 31:1830-1837.
26. Lin A.C., Holt C.E. Function and regulation of local axonal translation. Curr. Opin. Neurobiol. 2008, 18:60-68.
27. Long R.M., Singer R.H., Meng X., Gonzalez I., Nasmyth K., Jansen R.P. Mating type switching in yeast controlled by asymmetric localization of ASH1 mRNA. Science 1997, 277:383-387.
28. Martin K.C., Ephrussi A. mRNA localization: gene expression in the spatial dimension. Cell 2009, 136:719-730.
29. Narayanaswamy R., Moradi E.K., Niu W., Hart G.T., Davis M., McGary K.L., Ellington A.D., Marcotte E.M. Systematic definition of protein constituents along the major polarization axis reveals an adaptive reuse of the polarization machinery in pheromone-treated budding yeast. J. Proteome Res. 2009, 8:6-19.
30. Paliwal S., Iglesias P.A., Campbell K., Hilioti Z., Groisman A., Levchenko A. MAPK-mediated bimodal gene expression and adaptive gradient sensing in yeast. Nature 2007, 446:46-51.
31. Park H.O., Bi E. Central roles of small GTPases in the development of cell polarity in yeast and beyond. Microbiol. Mol. Biol. Rev. 2007, 71:48-96.
32. Prinz W.A., Grzyb L., Veenhuis M., Kahana J.A., Silver P.A., Rapoport T.A. Mutants affecting the structure of the cortical endoplasmic reticulum in Saccharomyces cerevisiae. J. Cell Biol. 2000, 150:461-474.
33. Pruyne D., Bretscher A. Polarization of cell growth in yeast. I. Establishment and maintenance of polarity states. J. Cell Sci. 2000, 113:365-375.
34. Reinke C.A., Kozik P., Glick B.S. Golgi inheritance in small buds of Saccharomyces cerevisiae is linked to endoplasmic reticulum inheritance. Proc. Natl. Acad. Sci. USA 2004, 101:18018-18023.
35. Rose M.D., Winston F., Hieter P. Methods in Yeast Genetics 1990, Cold Spring Harbor Laboratory Press, New York.
36. Rosoff W.J., Urbach J.S., Esrick M.A., McAllister R.G., Richards L.J., Goodhill G.J. A new chemotaxis assay shows the extreme sensitivity of axons to molecular gradients. Nat. Neurosci. 2004, 7:678-682.
37. Segall J.E. Polarization of yeast cells in spatial gradients of alpha mating factor. Proc. Natl. Acad. Sci. USA 1993, 90:8332-8336.
38. Shepard K.A., Gerber A.P., Jambhekar A., Takizawa P.A., Brown P.O., Herschlag D., DeRisi J.L., Vale R.D. Widespread cytoplasmic mRNA transport in yeast: identification of 22 bud-localized transcripts using DNA microarray analysis. Proc. Natl. Acad. Sci. USA 2003, 100:11429-11434.
39. Slessareva J.E., Routt S.M., Temple B., Bankaitis V.A., Dohlman H.G. Activation of the phosphatidylinositol 3-kinase Vps34 by a G protein alpha subunit at the endosome. Cell 2006, 126:191-203.
40. Takahashi T., Shimoi H., Ito K. Identification of genes required for growth under ethanol stress using transposon mutagenesis in Saccharomyces cerevisiae. Mol. Genet. Genomics 2001, 265:1112-1119.
41. Takizawa P.A., Vale R.D. The myosin motor, Myo4p, binds Ash1 mRNA via the adapter protein, She3p. Proc. Natl. Acad. Sci. USA 2000, 97:5273-5278.
42. Takizawa P.A., Sil A., Swedlow J.R., Herskowitz I., Vale R.D. Actin-dependent localization of an RNA encoding a cell-fate determinant in yeast. Nature 1997, 389:90-93.
43. Weber V., Wernitznig A., Hager G., Harata M., Frank P., Wintersberger U. Purification and nucleic-acid-binding properties of a Saccharomyces cerevisiae protein involved in the control of ploidy. Eur. J. Biochem. 1997, 249:309-317.
44. Wiederkehr A., Du Y., Pypaert M., Ferro-Novick S., Novick P. Sec3p is needed for the spatial regulation of secretion and for the inheritance of the cortical endoplasmic reticulum. Mol. Biol. Cell 2003, 14:4770-4782.
45. Wodarz A. Establishing cell polarity in development. Nat. Cell Biol. 2002, 4:E39-E44.
46. Yao J., Sasaki Y., Wen Z., Bassell G.J., Zheng J.Q. An essential role for beta-actin mRNA localization and translation in Ca2+-dependent growth cone guidance. Nat. Neurosci. 2006, 9:1265-1273.
47. Yoon B.C., Zivraj K.H., Holt C.E. Local translation and mRNA trafficking in axon pathfinding. Results Probl. Cell Differ. 2009, 48:269-288.
48. Zhang H.L., Singer R.H., Bassell G.J. Neurotrophin regulation of beta-actin mRNA and protein localization within growth cones. J. Cell Biol. 1999, 147:59-70.
49. Zhang N.N., Dudgeon D.D., Paliwal S., Levchenko A., Grote E., Cunningham K.W. Multiple signaling pathways regulate yeast cell death during the response to mating pheromones. Mol. Biol. Cell 2006, 17:3409-3422.