Skip to main content
PMC home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1994 Oct 2;127(2):521–535. doi: 10.1083/jcb.127.2.521

Differential perturbations in the morphogenesis of anterior structures induced by overexpression of truncated XB- and N-cadherins in Xenopus embryos

PMCID: PMC2120208  PMID: 7929592

Abstract

Cadherins, a family of Ca-dependent adhesion molecules, have been proposed to act as regulators of morphogenetic processes and to be major effectors in the maintenance of tissue integrity. In this study, we have compared the effects of the expression of two truncated cadherins during early neurogenesis in Xenopus laevis. mRNA encoding deleted forms of XB- and N-cadherin lacking most of the extracellular domain were injected into the four animal dorsal blastomeres of 32-cell stage Xenopus embryos. These truncated cadherins altered the cohesion of cells derived from the injected blastomeres and induced morphogenetic defects in the anterior neural tissue to which they chiefly contributed. Truncated XB-cadherin was more efficient than N- cadherin in inducing these perturbations. Moreover, the coexpression of both truncated cadherins had additive perturbation effects on neural development. The two truncated cadherins can interact with the three known catenins, but with distinct affinities. These results suggest that the adhesive signal mediated by cadherins can be perturbed by overexpressing their cytoplasmic domains by competing with different affinity with catenins and/or a common anchor structure. Therefore, the correct regulation of cadherin function through the cytoplasmic domain appears to be a crucial step in the formation of the neural tissue.

Full Text

The Full Text of this article is available as a PDF (6.0 MB).

Selected References

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

  1. Amaya E., Musci T. J., Kirschner M. W. Expression of a dominant negative mutant of the FGF receptor disrupts mesoderm formation in Xenopus embryos. Cell. 1991 Jul 26;66(2):257–270. doi: 10.1016/0092-8674(91)90616-7. [DOI] [PubMed] [Google Scholar]
  2. Chan B. M., Kassner P. D., Schiro J. A., Byers H. R., Kupper T. S., Hemler M. E. Distinct cellular functions mediated by different VLA integrin alpha subunit cytoplasmic domains. Cell. 1992 Mar 20;68(6):1051–1060. doi: 10.1016/0092-8674(92)90077-p. [DOI] [PubMed] [Google Scholar]
  3. Choi Y. S., Gumbiner B. Expression of cell adhesion molecule E-cadherin in Xenopus embryos begins at gastrulation and predominates in the ectoderm. J Cell Biol. 1989 Jun;108(6):2449–2458. doi: 10.1083/jcb.108.6.2449. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  5. Dale L., Slack J. M. Fate map for the 32-cell stage of Xenopus laevis. Development. 1987 Apr;99(4):527–551. doi: 10.1242/dev.99.4.527. [DOI] [PubMed] [Google Scholar]
  6. 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 Jan;105(1):61–74. doi: 10.1242/dev.105.1.61. [DOI] [PubMed] [Google Scholar]
  7. Detrick R. J., Dickey D., Kintner C. R. The effects of N-cadherin misexpression on morphogenesis in Xenopus embryos. Neuron. 1990 Apr;4(4):493–506. doi: 10.1016/0896-6273(90)90108-r. [DOI] [PubMed] [Google Scholar]
  8. Doherty P., Ashton S. V., Moore S. E., Walsh F. S. Morphoregulatory activities of NCAM and N-cadherin can be accounted for by G protein-dependent activation of L- and N-type neuronal Ca2+ channels. Cell. 1991 Oct 4;67(1):21–33. doi: 10.1016/0092-8674(91)90569-k. [DOI] [PubMed] [Google Scholar]
  9. Donalies M., Cramer M., Ringwald M., Starzinski-Powitz A. Expression of M-cadherin, a member of the cadherin multigene family, correlates with differentiation of skeletal muscle cells. Proc Natl Acad Sci U S A. 1991 Sep 15;88(18):8024–8028. doi: 10.1073/pnas.88.18.8024. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Duband J. L., Dufour S., Hatta K., Takeichi M., Edelman G. M., Thiery J. P. Adhesion molecules during somitogenesis in the avian embryo. J Cell Biol. 1987 May;104(5):1361–1374. doi: 10.1083/jcb.104.5.1361. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Edelman G. M. Morphoregulation. Dev Dyn. 1992 Jan;193(1):2–10. doi: 10.1002/aja.1001930103. [DOI] [PubMed] [Google Scholar]
  12. Edelman G. M., Murray B. A., Mege R. M., Cunningham B. A., Gallin W. J. Cellular expression of liver and neural cell adhesion molecules after transfection with their cDNAs results in specific cell-cell binding. Proc Natl Acad Sci U S A. 1987 Dec;84(23):8502–8506. doi: 10.1073/pnas.84.23.8502. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Friedlander D. R., Mège R. M., Cunningham B. A., Edelman G. M. Cell sorting-out is modulated by both the specificity and amount of different cell adhesion molecules (CAMs) expressed on cell surfaces. Proc Natl Acad Sci U S A. 1989 Sep;86(18):7043–7047. doi: 10.1073/pnas.86.18.7043. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Fujimori T., Miyatani S., Takeichi M. Ectopic expression of N-cadherin perturbs histogenesis in Xenopus embryos. Development. 1990 Sep;110(1):97–104. doi: 10.1242/dev.110.1.97. [DOI] [PubMed] [Google Scholar]
  15. Fujimori T., Takeichi M. Disruption of epithelial cell-cell adhesion by exogenous expression of a mutated nonfunctional N-cadherin. Mol Biol Cell. 1993 Jan;4(1):37–47. doi: 10.1091/mbc.4.1.37. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Geiger B., Ayalon O. Cadherins. Annu Rev Cell Biol. 1992;8:307–332. doi: 10.1146/annurev.cb.08.110192.001515. [DOI] [PubMed] [Google Scholar]
  17. Ginsberg D., DeSimone D., Geiger B. Expression of a novel cadherin (EP-cadherin) in unfertilized eggs and early Xenopus embryos. Development. 1991 Feb;111(2):315–325. doi: 10.1242/dev.111.2.315. [DOI] [PubMed] [Google Scholar]
  18. Harris W. A., Hartenstein V. Neuronal determination without cell division in Xenopus embryos. Neuron. 1991 Apr;6(4):499–515. doi: 10.1016/0896-6273(91)90053-3. [DOI] [PubMed] [Google Scholar]
  19. Hatta K., Takagi S., Fujisawa H., Takeichi M. Spatial and temporal expression pattern of N-cadherin cell adhesion molecules correlated with morphogenetic processes of chicken embryos. Dev Biol. 1987 Mar;120(1):215–227. doi: 10.1016/0012-1606(87)90119-9. [DOI] [PubMed] [Google Scholar]
  20. Herrenknecht K., Ozawa M., Eckerskorn C., Lottspeich F., Lenter M., Kemler R. The uvomorulin-anchorage protein alpha catenin is a vinculin homologue. Proc Natl Acad Sci U S A. 1991 Oct 15;88(20):9156–9160. doi: 10.1073/pnas.88.20.9156. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Herzberg F., Wildermuth V., Wedlich D. Expression of XBcad, a novel cadherin, during oogenesis and early development of Xenopus. Mech Dev. 1991 Aug;35(1):33–42. doi: 10.1016/0925-4773(91)90039-9. [DOI] [PubMed] [Google Scholar]
  22. Hirano S., Kimoto N., Shimoyama Y., Hirohashi S., Takeichi M. Identification of a neural alpha-catenin as a key regulator of cadherin function and multicellular organization. Cell. 1992 Jul 24;70(2):293–301. doi: 10.1016/0092-8674(92)90103-j. [DOI] [PubMed] [Google Scholar]
  23. Huang S., Moody S. A. The retinal fate of Xenopus cleavage stage progenitors is dependent upon blastomere position and competence: studies of normal and regulated clones. J Neurosci. 1993 Aug;13(8):3193–3210. doi: 10.1523/JNEUROSCI.13-08-03193.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Inuzuka H., Redies C., Takeichi M. Differential expression of R- and N-cadherin in neural and mesodermal tissues during early chicken development. Development. 1991 Nov;113(3):959–967. doi: 10.1242/dev.113.3.959. [DOI] [PubMed] [Google Scholar]
  25. Jacobson M., Hirose G. Clonal organization of the central nervous system of the frog. II. Clones stemming from individual blastomeres of the 32- and 64-cell stages. J Neurosci. 1981 Mar;1(3):271–284. doi: 10.1523/JNEUROSCI.01-03-00271.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Kemler R. From cadherins to catenins: cytoplasmic protein interactions and regulation of cell adhesion. Trends Genet. 1993 Sep;9(9):317–321. doi: 10.1016/0168-9525(93)90250-l. [DOI] [PubMed] [Google Scholar]
  27. Kemler R., Ozawa M., Ringwald M. Calcium-dependent cell adhesion molecules. Curr Opin Cell Biol. 1989 Oct;1(5):892–897. doi: 10.1016/0955-0674(89)90055-0. [DOI] [PubMed] [Google Scholar]
  28. Kintner C. R., Brockes J. P. Monoclonal antibodies to the cells of a regenerating limb. J Embryol Exp Morphol. 1985 Oct;89:37–55. [PubMed] [Google Scholar]
  29. Kintner C. Regulation of embryonic cell adhesion by the cadherin cytoplasmic domain. Cell. 1992 Apr 17;69(2):225–236. doi: 10.1016/0092-8674(92)90404-z. [DOI] [PubMed] [Google Scholar]
  30. Koch P. J., Goldschmidt M. D., Zimbelmann R., Troyanovsky R., Franke W. W. Complexity and expression patterns of the desmosomal cadherins. Proc Natl Acad Sci U S A. 1992 Jan 1;89(1):353–357. doi: 10.1073/pnas.89.1.353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Kreis T. E. Microinjected antibodies against the cytoplasmic domain of vesicular stomatitis virus glycoprotein block its transport to the cell surface. EMBO J. 1986 May;5(5):931–941. doi: 10.1002/j.1460-2075.1986.tb04306.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Krieg P. A., Melton D. A. Functional messenger RNAs are produced by SP6 in vitro transcription of cloned cDNAs. Nucleic Acids Res. 1984 Sep 25;12(18):7057–7070. doi: 10.1093/nar/12.18.7057. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Krieg P. A., Sakaguchi D. S., Kintner C. R. Primary structure and developmental expression of a large cytoplasmic domain form of Xenopus laevis neural cell adhesion molecule (NCAM). Nucleic Acids Res. 1989 Dec 25;17(24):10321–10335. doi: 10.1093/nar/17.24.10321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Levi G., Broders F., Dunon D., Edelman G. M., Thiery J. P. Thyroxine-dependent modulations of the expression of the neural cell adhesion molecule N-CAM during Xenopus laevis metamorphosis. Development. 1990 Apr;108(4):681–692. doi: 10.1242/dev.108.4.681. [DOI] [PubMed] [Google Scholar]
  35. Levi G., Crossin K. L., Edelman G. M. Expression sequences and distribution of two primary cell adhesion molecules during embryonic development of Xenopus laevis. J Cell Biol. 1987 Nov;105(5):2359–2372. doi: 10.1083/jcb.105.5.2359. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Levi G., Ginsberg D., Girault J. M., Sabanay I., Thiery J. P., Geiger B. EP-cadherin in muscles and epithelia of Xenopus laevis embryos. Development. 1991 Dec;113(4):1335–1344. doi: 10.1242/dev.113.4.1335. [DOI] [PubMed] [Google Scholar]
  37. Levi G., Gumbiner B., Thiery J. P. The distribution of E-cadherin during Xenopus laevis development. Development. 1991 Jan;111(1):159–169. doi: 10.1242/dev.111.1.159. [DOI] [PubMed] [Google Scholar]
  38. Levine E., Lee C. H., Kintner C., Gumbiner B. M. Selective disruption of E-cadherin function in early Xenopus embryos by a dominant negative mutant. Development. 1994 Apr;120(4):901–909. doi: 10.1242/dev.120.4.901. [DOI] [PubMed] [Google Scholar]
  39. Magee A. I., Buxton R. S. Transmembrane molecular assemblies regulated by the greater cadherin family. Curr Opin Cell Biol. 1991 Oct;3(5):854–861. doi: 10.1016/0955-0674(91)90060-c. [DOI] [PubMed] [Google Scholar]
  40. Matsuzaki F., Mège R. M., Jaffe S. H., Friedlander D. R., Gallin W. J., Goldberg J. I., Cunningham B. A., Edelman G. M. cDNAs of cell adhesion molecules of different specificity induce changes in cell shape and border formation in cultured S180 cells. J Cell Biol. 1990 Apr;110(4):1239–1252. doi: 10.1083/jcb.110.4.1239. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. McCrea P. D., Brieher W. M., Gumbiner B. M. Induction of a secondary body axis in Xenopus by antibodies to beta-catenin. J Cell Biol. 1993 Oct;123(2):477–484. doi: 10.1083/jcb.123.2.477. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. McCrea P. D., Gumbiner B. M. Purification of a 92-kDa cytoplasmic protein tightly associated with the cell-cell adhesion molecule E-cadherin (uvomorulin). Characterization and extractability of the protein complex from the cell cytostructure. J Biol Chem. 1991 Mar 5;266(7):4514–4520. [PubMed] [Google Scholar]
  43. Melton D. A., Krieg P. A., Rebagliati M. R., Maniatis T., Zinn K., Green M. R. Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter. Nucleic Acids Res. 1984 Sep 25;12(18):7035–7056. doi: 10.1093/nar/12.18.7035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Moody S. A. Fates of the blastomeres of the 32-cell-stage Xenopus embryo. Dev Biol. 1987 Aug;122(2):300–319. doi: 10.1016/0012-1606(87)90296-x. [DOI] [PubMed] [Google Scholar]
  45. Moore R., Walsh F. S. The cell adhesion molecule M-cadherin is specifically expressed in developing and regenerating, but not denervated skeletal muscle. Development. 1993 Apr;117(4):1409–1420. doi: 10.1242/dev.117.4.1409. [DOI] [PubMed] [Google Scholar]
  46. Nagafuchi A., Takeichi M. Cell binding function of E-cadherin is regulated by the cytoplasmic domain. EMBO J. 1988 Dec 1;7(12):3679–3684. doi: 10.1002/j.1460-2075.1988.tb03249.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Nagafuchi A., Takeichi M., Tsukita S. The 102 kd cadherin-associated protein: similarity to vinculin and posttranscriptional regulation of expression. Cell. 1991 May 31;65(5):849–857. doi: 10.1016/0092-8674(91)90392-c. [DOI] [PubMed] [Google Scholar]
  48. Napolitano E. W., Venstrom K., Wheeler E. F., Reichardt L. F. Molecular cloning and characterization of B-cadherin, a novel chick cadherin. J Cell Biol. 1991 May;113(4):893–905. doi: 10.1083/jcb.113.4.893. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Nose A., Nagafuchi A., Takeichi M. Expressed recombinant cadherins mediate cell sorting in model systems. Cell. 1988 Sep 23;54(7):993–1001. doi: 10.1016/0092-8674(88)90114-6. [DOI] [PubMed] [Google Scholar]
  50. Nose A., Nagafuchi A., Takeichi M. Isolation of placental cadherin cDNA: identification of a novel gene family of cell-cell adhesion molecules. EMBO J. 1987 Dec 1;6(12):3655–3661. doi: 10.1002/j.1460-2075.1987.tb02698.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Nose A., Tsuji K., Takeichi M. Localization of specificity determining sites in cadherin cell adhesion molecules. Cell. 1990 Apr 6;61(1):147–155. doi: 10.1016/0092-8674(90)90222-z. [DOI] [PubMed] [Google Scholar]
  52. Ozawa M., Baribault H., Kemler R. The cytoplasmic domain of the cell adhesion molecule uvomorulin associates with three independent proteins structurally related in different species. EMBO J. 1989 Jun;8(6):1711–1717. doi: 10.1002/j.1460-2075.1989.tb03563.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Ozawa M., Engel J., Kemler R. Single amino acid substitutions in one Ca2+ binding site of uvomorulin abolish the adhesive function. Cell. 1990 Nov 30;63(5):1033–1038. doi: 10.1016/0092-8674(90)90506-a. [DOI] [PubMed] [Google Scholar]
  54. Ozawa M., Hoschützky H., Herrenknecht K., Kemler R. A possible new adhesive site in the cell-adhesion molecule uvomorulin. Mech Dev. 1990 Dec;33(1):49–56. doi: 10.1016/0925-4773(90)90134-8. [DOI] [PubMed] [Google Scholar]
  55. Ozawa M., Kemler R. Molecular organization of the uvomorulin-catenin complex. J Cell Biol. 1992 Feb;116(4):989–996. doi: 10.1083/jcb.116.4.989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Ozawa M., Ringwald M., Kemler R. Uvomorulin-catenin complex formation is regulated by a specific domain in the cytoplasmic region of the cell adhesion molecule. Proc Natl Acad Sci U S A. 1990 Jun;87(11):4246–4250. doi: 10.1073/pnas.87.11.4246. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Pasqualini R., Hemler M. E. Contrasting roles for integrin beta 1 and beta 5 cytoplasmic domains in subcellular localization, cell proliferation, and cell migration. J Cell Biol. 1994 Apr;125(2):447–460. doi: 10.1083/jcb.125.2.447. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Peifer M., Orsulic S., Sweeton D., Wieschaus E. A role for the Drosophila segment polarity gene armadillo in cell adhesion and cytoskeletal integrity during oogenesis. Development. 1993 Aug;118(4):1191–1207. doi: 10.1242/dev.118.4.1191. [DOI] [PubMed] [Google Scholar]
  59. Pollerberg G. E., Burridge K., Krebs K. E., Goodman S. R., Schachner M. The 180-kD component of the neural cell adhesion molecule N-CAM is involved in cell-cell contacts and cytoskeleton-membrane interactions. Cell Tissue Res. 1987 Oct;250(1):227–236. doi: 10.1007/BF00214676. [DOI] [PubMed] [Google Scholar]
  60. Pollerberg G. E., Schachner M., Davoust J. Differentiation state-dependent surface mobilities of two forms of the neural cell adhesion molecule. Nature. 1986 Dec 4;324(6096):462–465. doi: 10.1038/324462a0. [DOI] [PubMed] [Google Scholar]
  61. Ranscht B., Dours-Zimmermann M. T. T-cadherin, a novel cadherin cell adhesion molecule in the nervous system lacks the conserved cytoplasmic region. Neuron. 1991 Sep;7(3):391–402. doi: 10.1016/0896-6273(91)90291-7. [DOI] [PubMed] [Google Scholar]
  62. Sacristán M. P., Vestal D. J., Dours-Zimmermann M. T., Ranscht B. T-cadherin 2: molecular characterization, function in cell adhesion, and coexpression with T-cadherin and N-cadherin. J Neurosci Res. 1993 Apr 15;34(6):664–680. doi: 10.1002/jnr.490340610. [DOI] [PubMed] [Google Scholar]
  63. Saint-Jeannet J. P., Levi G., Girault J. M., Koteliansky V., Thiery J. P. Ventrolateral regionalization of Xenopus laevis mesoderm is characterized by the expression of alpha-smooth muscle actin. Development. 1992 Aug;115(4):1165–1173. doi: 10.1242/dev.115.4.1165. [DOI] [PubMed] [Google Scholar]
  64. Schneider S., Herrenknecht K., Butz S., Kemler R., Hausen P. Catenins in Xenopus embryogenesis and their relation to the cadherin-mediated cell-cell adhesion system. Development. 1993 Jun;118(2):629–640. doi: 10.1242/dev.118.2.629. [DOI] [PubMed] [Google Scholar]
  65. Schwarz M. A., Owaribe K., Kartenbeck J., Franke W. W. Desmosomes and hemidesmosomes: constitutive molecular components. Annu Rev Cell Biol. 1990;6:461–491. doi: 10.1146/annurev.cb.06.110190.002333. [DOI] [PubMed] [Google Scholar]
  66. Simonneau L., Broders F., Thiery J. P. N-cadherin transcripts in Xenopus laevis from early tailbud to tadpole. Dev Dyn. 1992 Aug;194(4):247–260. doi: 10.1002/aja.1001940402. [DOI] [PubMed] [Google Scholar]
  67. Slack J. M. Peanut lectin receptors in the early amphibian embryo: regional markers for the study of embryonic induction. Cell. 1985 May;41(1):237–247. doi: 10.1016/0092-8674(85)90077-7. [DOI] [PubMed] [Google Scholar]
  68. Springer T. A. Adhesion receptors of the immune system. Nature. 1990 Aug 2;346(6283):425–434. doi: 10.1038/346425a0. [DOI] [PubMed] [Google Scholar]
  69. Suzuki S., Sano K., Tanihara H. Diversity of the cadherin family: evidence for eight new cadherins in nervous tissue. Cell Regul. 1991 Apr;2(4):261–270. doi: 10.1091/mbc.2.4.261. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Takeichi M. Cadherins: a molecular family important in selective cell-cell adhesion. Annu Rev Biochem. 1990;59:237–252. doi: 10.1146/annurev.bi.59.070190.001321. [DOI] [PubMed] [Google Scholar]
  71. Thiery J. P., Delouvée A., Gallin W. J., Cunningham B. A., Edelman G. M. Ontogenetic expression of cell adhesion molecules: L-CAM is found in epithelia derived from the three primary germ layers. Dev Biol. 1984 Mar;102(1):61–78. doi: 10.1016/0012-1606(84)90175-1. [DOI] [PubMed] [Google Scholar]
  72. Troyanovsky S. M., Eshkind L. G., Troyanovsky R. B., Leube R. E., Franke W. W. Contributions of cytoplasmic domains of desmosomal cadherins to desmosome assembly and intermediate filament anchorage. Cell. 1993 Feb 26;72(4):561–574. doi: 10.1016/0092-8674(93)90075-2. [DOI] [PubMed] [Google Scholar]
  73. Watanabe M., Frelinger A. L., 3rd, Rutishauser U. Topography of N-CAM structural and functional determinants. I. Classification of monoclonal antibody epitopes. J Cell Biol. 1986 Nov;103(5):1721–1727. doi: 10.1083/jcb.103.5.1721. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Wetts R., Kook J. H., Fraser S. E. Proportion of proliferative cells in the tadpole retina is increased after embryonic lesion. Dev Dyn. 1993 Sep;198(1):54–64. doi: 10.1002/aja.1001980106. [DOI] [PubMed] [Google Scholar]

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

RESOURCES