Skip to main content
PMC home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1994 Jun 1;125(5):1077–1093. doi: 10.1083/jcb.125.5.1077

Growth site localization of Rho1 small GTP-binding protein and its involvement in bud formation in Saccharomyces cerevisiae

PMCID: PMC2120056  PMID: 8195291

Abstract

The Rho small GTP-binding protein family regulates various actomyosin- dependent cell functions, such as cell morphology, locomotion, cytokinesis, membrane ruffling, and smooth muscle contraction. In the yeast Saccharomyces cerevisiae, there is a homologue of mammalian RhoA, RHO1, which is essential for vegetative growth of yeast cells. To explore the function of the RHO1 gene, we isolated a recessive temperature-sensitive mutation of RHO1, rho1-104. The rho1-104 mutation caused amino acid substitutions of Asp 72 to Asn and Cys 164 to Tyr of Rho1p. Strains bearing the rho1-104 mutation accumulated tiny- or small- budded cells in which cortical actin patches were clustered to buds at the restrictive temperature. Cell lysis and cell death were also seen with the rho1-104 mutant. Indirect immunofluorescence microscopic study demonstrated that Rho1p was concentrated to the periphery of the cells where cortical actin patches were clustered, including the site of bud emergence, the tip of the growing buds, and the mother-bud neck region of cells prior to cytokinesis. Indirect immunofluorescence study with cells overexpressing RHO1 suggested that the Rho1p-binding site was saturable. A mutant Rho1p with an amino acid substitution at the lipid modification site remained in the cytoplasm. These results suggest that Rho1 small GTP-binding protein binds to a specific site at the growth region of cells, where Rho1p exerts its function in controlling cell growth.

Full Text

The Full Text of this article is available as a PDF (4.4 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adams A. E., Johnson D. I., Longnecker R. M., Sloat B. F., Pringle J. R. CDC42 and CDC43, two additional genes involved in budding and the establishment of cell polarity in the yeast Saccharomyces cerevisiae. J Cell Biol. 1990 Jul;111(1):131–142. doi: 10.1083/jcb.111.1.131. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Adams A. E., Pringle J. R. Relationship of actin and tubulin distribution to bud growth in wild-type and morphogenetic-mutant Saccharomyces cerevisiae. J Cell Biol. 1984 Mar;98(3):934–945. doi: 10.1083/jcb.98.3.934. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Adams A. E., Pringle J. R. Staining of actin with fluorochrome-conjugated phalloidin. Methods Enzymol. 1991;194:729–731. doi: 10.1016/0076-6879(91)94054-g. [DOI] [PubMed] [Google Scholar]
  4. Adamson P., Paterson H. F., Hall A. Intracellular localization of the P21rho proteins. J Cell Biol. 1992 Nov;119(3):617–627. doi: 10.1083/jcb.119.3.617. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Aktories K., Rösener S., Blaschke U., Chhatwal G. S. Botulinum ADP-ribosyltransferase C3. Purification of the enzyme and characterization of the ADP-ribosylation reaction in platelet membranes. Eur J Biochem. 1988 Mar 1;172(2):445–450. doi: 10.1111/j.1432-1033.1988.tb13908.x. [DOI] [PubMed] [Google Scholar]
  6. Ando S., Kaibuchi K., Sasaki T., Hiraoka K., Nishiyama T., Mizuno T., Asada M., Nunoi H., Matsuda I., Matsuura Y. Post-translational processing of rac p21s is important both for their interaction with the GDP/GTP exchange proteins and for their activation of NADPH oxidase. J Biol Chem. 1992 Dec 25;267(36):25709–25713. [PubMed] [Google Scholar]
  7. Boeke J. D., LaCroute F., Fink G. R. A positive selection for mutants lacking orotidine-5'-phosphate decarboxylase activity in yeast: 5-fluoro-orotic acid resistance. Mol Gen Genet. 1984;197(2):345–346. doi: 10.1007/BF00330984. [DOI] [PubMed] [Google Scholar]
  8. Bourne H. R., Sanders D. A., McCormick F. The GTPase superfamily: conserved structure and molecular mechanism. Nature. 1991 Jan 10;349(6305):117–127. doi: 10.1038/349117a0. [DOI] [PubMed] [Google Scholar]
  9. Drubin D. G. Development of cell polarity in budding yeast. Cell. 1991 Jun 28;65(7):1093–1096. doi: 10.1016/0092-8674(91)90001-f. [DOI] [PubMed] [Google Scholar]
  10. Field J., Nikawa J., Broek D., MacDonald B., Rodgers L., Wilson I. A., Lerner R. A., Wigler M. Purification of a RAS-responsive adenylyl cyclase complex from Saccharomyces cerevisiae by use of an epitope addition method. Mol Cell Biol. 1988 May;8(5):2159–2165. doi: 10.1128/mcb.8.5.2159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fukumoto Y., Kaibuchi K., Hori Y., Fujioka H., Araki S., Ueda T., Kikuchi A., Takai Y. Molecular cloning and characterization of a novel type of regulatory protein (GDI) for the rho proteins, ras p21-like small GTP-binding proteins. Oncogene. 1990 Sep;5(9):1321–1328. [PubMed] [Google Scholar]
  12. Gietz D., St Jean A., Woods R. A., Schiestl R. H. Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res. 1992 Mar 25;20(6):1425–1425. doi: 10.1093/nar/20.6.1425. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hall A. The cellular functions of small GTP-binding proteins. Science. 1990 Aug 10;249(4969):635–640. doi: 10.1126/science.2116664. [DOI] [PubMed] [Google Scholar]
  14. Hart M. J., Eva A., Evans T., Aaronson S. A., Cerione R. A. Catalysis of guanine nucleotide exchange on the CDC42Hs protein by the dbl oncogene product. Nature. 1991 Nov 28;354(6351):311–314. doi: 10.1038/354311a0. [DOI] [PubMed] [Google Scholar]
  15. Hartwell L. H., Culotti J., Pringle J. R., Reid B. J. Genetic control of the cell division cycle in yeast. Science. 1974 Jan 11;183(4120):46–51. doi: 10.1126/science.183.4120.46. [DOI] [PubMed] [Google Scholar]
  16. Hartwell L. H. Genetic control of the cell division cycle in yeast. IV. Genes controlling bud emergence and cytokinesis. Exp Cell Res. 1971 Dec;69(2):265–276. doi: 10.1016/0014-4827(71)90223-0. [DOI] [PubMed] [Google Scholar]
  17. Hill J. E., Myers A. M., Koerner T. J., Tzagoloff A. Yeast/E. coli shuttle vectors with multiple unique restriction sites. Yeast. 1986 Sep;2(3):163–167. doi: 10.1002/yea.320020304. [DOI] [PubMed] [Google Scholar]
  18. Hirata K., Kikuchi A., Sasaki T., Kuroda S., Kaibuchi K., Matsuura Y., Seki H., Saida K., Takai Y. Involvement of rho p21 in the GTP-enhanced calcium ion sensitivity of smooth muscle contraction. J Biol Chem. 1992 May 5;267(13):8719–8722. [PubMed] [Google Scholar]
  19. Hori Y., Kikuchi A., Isomura M., Katayama M., Miura Y., Fujioka H., Kaibuchi K., Takai Y. Post-translational modifications of the C-terminal region of the rho protein are important for its interaction with membranes and the stimulatory and inhibitory GDP/GTP exchange proteins. Oncogene. 1991 Apr;6(4):515–522. [PubMed] [Google Scholar]
  20. Horiuchi H., Kaibuchi K., Kawamura M., Matsuura Y., Suzuki N., Kuroda Y., Kataoka T., Takai Y. The posttranslational processing of ras p21 is critical for its stimulation of yeast adenylate cyclase. Mol Cell Biol. 1992 Oct;12(10):4515–4520. doi: 10.1128/mcb.12.10.4515. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Isomura M., Kaibuchi K., Yamamoto T., Kawamura S., Katayama M., Takai Y. Partial purification and characterization of GDP dissociation stimulator (GDS) for the rho proteins from bovine brain cytosol. Biochem Biophys Res Commun. 1990 Jun 15;169(2):652–659. doi: 10.1016/0006-291x(90)90380-6. [DOI] [PubMed] [Google Scholar]
  22. Ito H., Fukuda Y., Murata K., Kimura A. Transformation of intact yeast cells treated with alkali cations. J Bacteriol. 1983 Jan;153(1):163–168. doi: 10.1128/jb.153.1.163-168.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Itoh T., Kaibuchi K., Masuda T., Yamamoto T., Matsuura Y., Maeda A., Shimizu K., Takai Y. The post-translational processing of ras p21 is critical for its stimulation of mitogen-activated protein kinase. J Biol Chem. 1993 Feb 15;268(5):3025–3028. [PubMed] [Google Scholar]
  24. Johnson D. I., Pringle J. R. Molecular characterization of CDC42, a Saccharomyces cerevisiae gene involved in the development of cell polarity. J Cell Biol. 1990 Jul;111(1):143–152. doi: 10.1083/jcb.111.1.143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kaibuchi K., Mizuno T., Fujioka H., Yamamoto T., Kishi K., Fukumoto Y., Hori Y., Takai Y. Molecular cloning of the cDNA for stimulatory GDP/GTP exchange protein for smg p21s (ras p21-like small GTP-binding proteins) and characterization of stimulatory GDP/GTP exchange protein. Mol Cell Biol. 1991 May;11(5):2873–2880. doi: 10.1128/mcb.11.5.2873. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Katayama M., Kawata M., Yoshida Y., Horiuchi H., Yamamoto T., Matsuura Y., Takai Y. The posttranslationally modified C-terminal structure of bovine aortic smooth muscle rhoA p21. J Biol Chem. 1991 Jul 5;266(19):12639–12645. [PubMed] [Google Scholar]
  27. Kawahara Y., Kawata M., Sunako M., Araki S., Koide M., Tsuda T., Fukuzaki H., Takai Y. Identification of a major GTP-binding protein in bovine aortic smooth muscle cytosol as the rhoA gene product. Biochem Biophys Res Commun. 1990 Jul 31;170(2):673–683. doi: 10.1016/0006-291x(90)92144-o. [DOI] [PubMed] [Google Scholar]
  28. Kikuchi A., Kuroda S., Sasaki T., Kotani K., Hirata K., Katayama M., Takai Y. Functional interactions of stimulatory and inhibitory GDP/GTP exchange proteins and their common substrate small GTP-binding protein. J Biol Chem. 1992 Jul 25;267(21):14611–14615. [PubMed] [Google Scholar]
  29. Kikuchi A., Yamamoto K., Fujita T., Takai Y. ADP-ribosylation of the bovine brain rho protein by botulinum toxin type C1. J Biol Chem. 1988 Nov 5;263(31):16303–16308. [PubMed] [Google Scholar]
  30. Kilmartin J. V., Adams A. E. Structural rearrangements of tubulin and actin during the cell cycle of the yeast Saccharomyces. J Cell Biol. 1984 Mar;98(3):922–933. doi: 10.1083/jcb.98.3.922. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Kishi K., Sasaki T., Kuroda S., Itoh T., Takai Y. Regulation of cytoplasmic division of Xenopus embryo by rho p21 and its inhibitory GDP/GTP exchange protein (rho GDI). J Cell Biol. 1993 Mar;120(5):1187–1195. doi: 10.1083/jcb.120.5.1187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Kolodziej P. A., Young R. A. Epitope tagging and protein surveillance. Methods Enzymol. 1991;194:508–519. doi: 10.1016/0076-6879(91)94038-e. [DOI] [PubMed] [Google Scholar]
  33. Kuchler K., Dohlman H. G., Thorner J. The a-factor transporter (STE6 gene product) and cell polarity in the yeast Saccharomyces cerevisiae. J Cell Biol. 1993 Mar;120(5):1203–1215. doi: 10.1083/jcb.120.5.1203. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Kuroda S., Kikuchi A., Hirata K., Masuda T., Kishi K., Sasaki T., Takai Y. Cooperative function of rho GDS and rho GDI to regulate rho p21 activation in smooth muscle. Biochem Biophys Res Commun. 1992 May 29;185(1):473–480. doi: 10.1016/s0006-291x(05)81009-5. [DOI] [PubMed] [Google Scholar]
  35. Lang P., Guizani L., Vitté-Mony I., Stancou R., Dorseuil O., Gacon G., Bertoglio J. ADP-ribosylation of the ras-related, GTP-binding protein RhoA inhibits lymphocyte-mediated cytotoxicity. J Biol Chem. 1992 Jun 15;267(17):11677–11680. [PubMed] [Google Scholar]
  36. Lee K. S., Hines L. K., Levin D. E. A pair of functionally redundant yeast genes (PPZ1 and PPZ2) encoding type 1-related protein phosphatases function within the PKC1-mediated pathway. Mol Cell Biol. 1993 Sep;13(9):5843–5853. doi: 10.1128/mcb.13.9.5843. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Lelias J. M., Adra C. N., Wulf G. M., Guillemot J. C., Khagad M., Caput D., Lim B. cDNA cloning of a human mRNA preferentially expressed in hematopoietic cells and with homology to a GDP-dissociation inhibitor for the rho GTP-binding proteins. Proc Natl Acad Sci U S A. 1993 Feb 15;90(4):1479–1483. doi: 10.1073/pnas.90.4.1479. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Levin D. E., Bartlett-Heubusch E. Mutants in the S. cerevisiae PKC1 gene display a cell cycle-specific osmotic stability defect. J Cell Biol. 1992 Mar;116(5):1221–1229. doi: 10.1083/jcb.116.5.1221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Madaule P., Axel R., Myers A. M. Characterization of two members of the rho gene family from the yeast Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1987 Feb;84(3):779–783. doi: 10.1073/pnas.84.3.779. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Matsui Y., Toh-E A. Yeast RHO3 and RHO4 ras superfamily genes are necessary for bud growth, and their defect is suppressed by a high dose of bud formation genes CDC42 and BEM1. Mol Cell Biol. 1992 Dec;12(12):5690–5699. doi: 10.1128/mcb.12.12.5690. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. McCaffrey M., Johnson J. S., Goud B., Myers A. M., Rossier J., Popoff M. R., Madaule P., Boquet P. The small GTP-binding protein Rho1p is localized on the Golgi apparatus and post-Golgi vesicles in Saccharomyces cerevisiae. J Cell Biol. 1991 Oct;115(2):309–319. doi: 10.1083/jcb.115.2.309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Miura Y., Kikuchi A., Musha T., Kuroda S., Yaku H., Sasaki T., Takai Y. Regulation of morphology by rho p21 and its inhibitory GDP/GTP exchange protein (rho GDI) in Swiss 3T3 cells. J Biol Chem. 1993 Jan 5;268(1):510–515. [PubMed] [Google Scholar]
  43. Mizuno T., Kaibuchi K., Yamamoto T., Kawamura M., Sakoda T., Fujioka H., Matsuura Y., Takai Y. A stimulatory GDP/GTP exchange protein for smg p21 is active on the post-translationally processed form of c-Ki-ras p21 and rhoA p21. Proc Natl Acad Sci U S A. 1991 Aug 1;88(15):6442–6446. doi: 10.1073/pnas.88.15.6442. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Morii N., Teru-uchi T., Tominaga T., Kumagai N., Kozaki S., Ushikubi F., Narumiya S. A rho gene product in human blood platelets. II. Effects of the ADP-ribosylation by botulinum C3 ADP-ribosyltransferase on platelet aggregation. J Biol Chem. 1992 Oct 15;267(29):20921–20926. [PubMed] [Google Scholar]
  45. Narumiya S., Sekine A., Fujiwara M. Substrate for botulinum ADP-ribosyltransferase, Gb, has an amino acid sequence homologous to a putative rho gene product. J Biol Chem. 1988 Nov 25;263(33):17255–17257. [PubMed] [Google Scholar]
  46. Nelson W. J. Regulation of cell surface polarity from bacteria to mammals. Science. 1992 Nov 6;258(5084):948–955. doi: 10.1126/science.1439806. [DOI] [PubMed] [Google Scholar]
  47. Ninomiya-Tsuji J., Nomoto S., Yasuda H., Reed S. I., Matsumoto K. Cloning of a human cDNA encoding a CDC2-related kinase by complementation of a budding yeast cdc28 mutation. Proc Natl Acad Sci U S A. 1991 Oct 15;88(20):9006–9010. doi: 10.1073/pnas.88.20.9006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Nishiyama T., Sasaki T., Takaishi K., Kato M., Yaku H., Araki K., Matsuura Y., Takai Y. rac p21 is involved in insulin-induced membrane ruffling and rho p21 is involved in hepatocyte growth factor- and 12-O-tetradecanoylphorbol-13-acetate (TPA)-induced membrane ruffling in KB cells. Mol Cell Biol. 1994 Apr;14(4):2447–2456. doi: 10.1128/mcb.14.4.2447. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Novick P., Botstein D. Phenotypic analysis of temperature-sensitive yeast actin mutants. Cell. 1985 Feb;40(2):405–416. doi: 10.1016/0092-8674(85)90154-0. [DOI] [PubMed] [Google Scholar]
  50. Paravicini G., Cooper M., Friedli L., Smith D. J., Carpentier J. L., Klig L. S., Payton M. A. The osmotic integrity of the yeast cell requires a functional PKC1 gene product. Mol Cell Biol. 1992 Nov;12(11):4896–4905. doi: 10.1128/mcb.12.11.4896. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Paterson H. F., Self A. J., Garrett M. D., Just I., Aktories K., Hall A. Microinjection of recombinant p21rho induces rapid changes in cell morphology. J Cell Biol. 1990 Sep;111(3):1001–1007. doi: 10.1083/jcb.111.3.1001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Pringle J. R., Adams A. E., Drubin D. G., Haarer B. K. Immunofluorescence methods for yeast. Methods Enzymol. 1991;194:565–602. doi: 10.1016/0076-6879(91)94043-c. [DOI] [PubMed] [Google Scholar]
  53. Qadota H., Ishii I., Fujiyama A., Ohya Y., Anraku Y. RHO gene products, putative small GTP-binding proteins, are important for activation of the CAL1/CDC43 gene product, a protein geranylgeranyltransferase in Saccharomyces cerevisiae. Yeast. 1992 Sep;8(9):735–741. doi: 10.1002/yea.320080906. [DOI] [PubMed] [Google Scholar]
  54. Regazzi R., Kikuchi A., Takai Y., Wollheim C. B. The small GTP-binding proteins in the cytosol of insulin-secreting cells are complexed to GDP dissociation inhibitor proteins. J Biol Chem. 1992 Sep 5;267(25):17512–17519. [PubMed] [Google Scholar]
  55. Ridley A. J., Hall A. The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell. 1992 Aug 7;70(3):389–399. doi: 10.1016/0092-8674(92)90163-7. [DOI] [PubMed] [Google Scholar]
  56. Rose M. D., Fink G. R. KAR1, a gene required for function of both intranuclear and extranuclear microtubules in yeast. Cell. 1987 Mar 27;48(6):1047–1060. doi: 10.1016/0092-8674(87)90712-4. [DOI] [PubMed] [Google Scholar]
  57. Rothstein R. Targeting, disruption, replacement, and allele rescue: integrative DNA transformation in yeast. Methods Enzymol. 1991;194:281–301. doi: 10.1016/0076-6879(91)94022-5. [DOI] [PubMed] [Google Scholar]
  58. Rubin E. J., Gill D. M., Boquet P., Popoff M. R. Functional modification of a 21-kilodalton G protein when ADP-ribosylated by exoenzyme C3 of Clostridium botulinum. Mol Cell Biol. 1988 Jan;8(1):418–426. doi: 10.1128/mcb.8.1.418. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Sikorski R. S., Boeke J. D. In vitro mutagenesis and plasmid shuffling: from cloned gene to mutant yeast. Methods Enzymol. 1991;194:302–318. doi: 10.1016/0076-6879(91)94023-6. [DOI] [PubMed] [Google Scholar]
  60. Sikorski R. S., Hieter P. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics. 1989 May;122(1):19–27. doi: 10.1093/genetics/122.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Sloat B. F., Adams A., Pringle J. R. Roles of the CDC24 gene product in cellular morphogenesis during the Saccharomyces cerevisiae cell cycle. J Cell Biol. 1981 Jun;89(3):395–405. doi: 10.1083/jcb.89.3.395. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Takai Y., Kaibuchi K., Kikuchi A., Kawata M. Small GTP-binding proteins. Int Rev Cytol. 1992;133:187–230. doi: 10.1016/s0074-7696(08)61861-6. [DOI] [PubMed] [Google Scholar]
  63. Takaishi K., Kikuchi A., Kuroda S., Kotani K., Sasaki T., Takai Y. Involvement of rho p21 and its inhibitory GDP/GTP exchange protein (rho GDI) in cell motility. Mol Cell Biol. 1993 Jan;13(1):72–79. doi: 10.1128/mcb.13.1.72. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Takaishi K., Sasaki T., Kato M., Yamochi W., Kuroda S., Nakamura T., Takeichi M., Takai Y. Involvement of Rho p21 small GTP-binding protein and its regulator in the HGF-induced cell motility. Oncogene. 1994 Jan;9(1):273–279. [PubMed] [Google Scholar]
  65. Tominaga T., Sugie K., Hirata M., Morii N., Fukata J., Uchida A., Imura H., Narumiya S. Inhibition of PMA-induced, LFA-1-dependent lymphocyte aggregation by ADP ribosylation of the small molecular weight GTP binding protein, rho. J Cell Biol. 1993 Mar;120(6):1529–1537. doi: 10.1083/jcb.120.6.1529. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Valencia A., Chardin P., Wittinghofer A., Sander C. The ras protein family: evolutionary tree and role of conserved amino acids. Biochemistry. 1991 May 14;30(19):4637–4648. doi: 10.1021/bi00233a001. [DOI] [PubMed] [Google Scholar]
  67. Wilson I. A., Niman H. L., Houghten R. A., Cherenson A. R., Connolly M. L., Lerner R. A. The structure of an antigenic determinant in a protein. Cell. 1984 Jul;37(3):767–778. doi: 10.1016/0092-8674(84)90412-4. [DOI] [PubMed] [Google Scholar]
  68. Yaku H., Sasaki T., Takai Y. The Dbl oncogene product as a GDP/GTP exchange protein for the Rho family: its properties in comparison with those of Smg GDS. Biochem Biophys Res Commun. 1994 Jan 28;198(2):811–817. doi: 10.1006/bbrc.1994.1116. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES