Abstract
Proof that plants possess homologs of animal adhesion proteins is lacking. In this paper we describe the generation of monoclonal antibodies that interfere with cell-cell contacts in the 4-cell embryo of the multicellular alga Volvox carteri, resulting in a hole between the cells. The number of following cell divisions is reduced and the cell division pattern is altered drastically. Antibodies given at a later stage of embryogenesis specifically inhibit inversion of the embryo, a morphogenetic movement that turns the embryo inside out. Immunofluorescence microscopy localizes the antigen (Algal-CAM) at cell contact sites of the developing embryo. Algal-CAM is a protein with a three-domain structure: an N-terminal extensin-like domain characteristic for plant cell walls and two repeats with homology to fasciclin I, a cell adhesion molecule involved in the neuronal development of Drosophila. Alternatively spliced variants of Algal-CAM mRNA were detected that are produced under developmental control. Thus, Algal-CAM is the first plant homolog of animal adhesion proteins.
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- Adair W. S., Steinmetz S. A., Mattson D. M., Goodenough U. W., Heuser J. E. Nucleated assembly of Chlamydomonas and Volvox cell walls. J Cell Biol. 1987 Nov;105(5):2373–2382. doi: 10.1083/jcb.105.5.2373. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
- Chen C. G., Cornish E. C., Clarke A. E. Specific expression of an extensin-like gene in the style of Nicotiana alata. Plant Cell. 1992 Sep;4(9):1053–1062. doi: 10.1105/tpc.4.9.1053. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Edelman G. M., Crossin K. L. Cell adhesion molecules: implications for a molecular histology. Annu Rev Biochem. 1991;60:155–190. doi: 10.1146/annurev.bi.60.070191.001103. [DOI] [PubMed] [Google Scholar]
- Edelman G. M. Morphoregulatory molecules. Biochemistry. 1988 May 17;27(10):3533–3543. doi: 10.1021/bi00410a001. [DOI] [PubMed] [Google Scholar]
- Ekblom P., Vestweber D., Kemler R. Cell-matrix interactions and cell adhesion during development. Annu Rev Cell Biol. 1986;2:27–47. doi: 10.1146/annurev.cb.02.110186.000331. [DOI] [PubMed] [Google Scholar]
- Elkins T., Hortsch M., Bieber A. J., Snow P. M., Goodman C. S. Drosophila fasciclin I is a novel homophilic adhesion molecule that along with fasciclin III can mediate cell sorting. J Cell Biol. 1990 May;110(5):1825–1832. doi: 10.1083/jcb.110.5.1825. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Elkins T., Zinn K., McAllister L., Hoffmann F. M., Goodman C. S. Genetic analysis of a Drosophila neural cell adhesion molecule: interaction of fasciclin I and Abelson tyrosine kinase mutations. Cell. 1990 Feb 23;60(4):565–575. doi: 10.1016/0092-8674(90)90660-7. [DOI] [PubMed] [Google Scholar]
- Englund P. T. The structure and biosynthesis of glycosyl phosphatidylinositol protein anchors. Annu Rev Biochem. 1993;62:121–138. doi: 10.1146/annurev.bi.62.070193.001005. [DOI] [PubMed] [Google Scholar]
- Ertl H., Hallmann A., Wenzl S., Sumper M. A novel extensin that may organize extracellular matrix biogenesis in Volvox carteri. EMBO J. 1992 Jun;11(6):2055–2062. doi: 10.1002/j.1460-2075.1992.tb05263.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ertl H., Mengele R., Wenzl S., Engel J., Sumper M. The extracellular matrix of Volvox carteri: molecular structure of the cellular compartment. J Cell Biol. 1989 Dec;109(6 Pt 2):3493–3501. doi: 10.1083/jcb.109.6.3493. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Frischauf A. M., Lehrach H., Poustka A., Murray N. Lambda replacement vectors carrying polylinker sequences. J Mol Biol. 1983 Nov 15;170(4):827–842. doi: 10.1016/s0022-2836(83)80190-9. [DOI] [PubMed] [Google Scholar]
- Frohman M. A., Dush M. K., Martin G. R. Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci U S A. 1988 Dec;85(23):8998–9002. doi: 10.1073/pnas.85.23.8998. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fry S. C. Isodityrosine, a new cross-linking amino acid from plant cell-wall glycoprotein. Biochem J. 1982 May 15;204(2):449–455. doi: 10.1042/bj2040449. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Goldman M. H., Pezzotti M., Seurinck J., Mariani C. Developmental expression of tobacco pistil-specific genes encoding novel extensin-like proteins. Plant Cell. 1992 Sep;4(9):1041–1051. doi: 10.1105/tpc.4.9.1041. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Green K. J., Kirk D. L. Cleavage patterns, cell lineages, and development of a cytoplasmic bridge system in Volvox embryos. J Cell Biol. 1981 Dec;91(3 Pt 1):743–755. doi: 10.1083/jcb.91.3.743. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Green K. J., Viamontes G. I., Kirk D. L. Mechanism of formation, ultrastructure, and function of the cytoplasmic bridge system during morphogenesis in Volvox. J Cell Biol. 1981 Dec;91(3 Pt 1):756–769. doi: 10.1083/jcb.91.3.756. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hallmann A., Sumper M. An inducible arylsulfatase of Volvox carteri with properties suitable for a reporter-gene system. Purification, characterization and molecular cloning. Eur J Biochem. 1994 Apr 1;221(1):143–150. doi: 10.1111/j.1432-1033.1994.tb18723.x. [DOI] [PubMed] [Google Scholar]
- Hortsch M., Goodman C. S. Drosophila fasciclin I, a neural cell adhesion molecule, has a phosphatidylinositol lipid membrane anchor that is developmentally regulated. J Biol Chem. 1990 Sep 5;265(25):15104–15109. [PubMed] [Google Scholar]
- Kirk D. L., Birchem R., King N. The extracellular matrix of Volvox: a comparative study and proposed system of nomenclature. J Cell Sci. 1986 Feb;80:207–231. doi: 10.1242/jcs.80.1.207. [DOI] [PubMed] [Google Scholar]
- Kirk D. L., Harper J. F. Genetic, biochemical, and molecular approaches to Volvox development and evolution. Int Rev Cytol. 1986;99:217–293. doi: 10.1016/s0074-7696(08)61428-x. [DOI] [PubMed] [Google Scholar]
- Kirk M. M., Kirk D. L. Translational regulation of protein synthesis, in response to light, at a critical stage of Volvox development. Cell. 1985 Jun;41(2):419–428. doi: 10.1016/s0092-8674(85)80015-5. [DOI] [PubMed] [Google Scholar]
- Kyte J., Doolittle R. F. A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982 May 5;157(1):105–132. doi: 10.1016/0022-2836(82)90515-0. [DOI] [PubMed] [Google Scholar]
- McAllister L., Rehm E. J., Goodman G. S., Zinn K. Alternative splicing of micro-exons creates multiple forms of the insect cell adhesion molecule fasciclin I. J Neurosci. 1992 Mar;12(3):895–905. doi: 10.1523/JNEUROSCI.12-03-00895.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ochiai H., Schwarz H., Merkl R., Wagle G., Gerisch G. Stage-specific antigens reacting with monoclonal antibodies against contact site A, a cell-surface glycoprotein of Dictyostelium discoideum. Cell Differ. 1982 Jan;11(1):1–13. doi: 10.1016/0045-6039(82)90011-2. [DOI] [PubMed] [Google Scholar]
- Perlman D., Halvorson H. O. A putative signal peptidase recognition site and sequence in eukaryotic and prokaryotic signal peptides. J Mol Biol. 1983 Jun 25;167(2):391–409. doi: 10.1016/s0022-2836(83)80341-6. [DOI] [PubMed] [Google Scholar]
- Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schiedlmeier B., Schmitt R., Müller W., Kirk M. M., Gruber H., Mages W., Kirk D. L. Nuclear transformation of Volvox carteri. Proc Natl Acad Sci U S A. 1994 May 24;91(11):5080–5084. doi: 10.1073/pnas.91.11.5080. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Showalter A. M., Bell J. N., Cramer C. L., Bailey J. A., Varner J. E., Lamb C. J. Accumulation of hydroxyproline-rich glycoprotein mRNAs in response to fungal elicitor and infection. Proc Natl Acad Sci U S A. 1985 Oct;82(19):6551–6555. doi: 10.1073/pnas.82.19.6551. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Skonier J., Neubauer M., Madisen L., Bennett K., Plowman G. D., Purchio A. F. cDNA cloning and sequence analysis of beta ig-h3, a novel gene induced in a human adenocarcinoma cell line after treatment with transforming growth factor-beta. DNA Cell Biol. 1992 Sep;11(7):511–522. doi: 10.1089/dna.1992.11.511. [DOI] [PubMed] [Google Scholar]
- Starr R. C. Control of differentiation in Volvox. Symp Soc Dev Biol. 1970;29:59–100. doi: 10.1016/b978-0-12-395534-0.50009-1. [DOI] [PubMed] [Google Scholar]
- Starr R. C., Jaenicke L. Purification and characterization of the hormone initiating sexual morphogenesis in Volvox carteri f. nagariensis Iyengar. Proc Natl Acad Sci U S A. 1974 Apr;71(4):1050–1054. doi: 10.1073/pnas.71.4.1050. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Studier F. W., Rosenberg A. H., Dunn J. J., Dubendorff J. W. Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol. 1990;185:60–89. doi: 10.1016/0076-6879(90)85008-c. [DOI] [PubMed] [Google Scholar]
- Sumper M. Control of differentiation in volvox carteri: a model explaining pattern formation during embryogenesis. FEBS Lett. 1979 Nov 1;107(1):241–246. doi: 10.1016/0014-5793(79)80505-0. [DOI] [PubMed] [Google Scholar]
- 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]
- Takeichi M. The cadherins: cell-cell adhesion molecules controlling animal morphogenesis. Development. 1988 Apr;102(4):639–655. doi: 10.1242/dev.102.4.639. [DOI] [PubMed] [Google Scholar]
- Takeshita S., Kikuno R., Tezuka K., Amann E. Osteoblast-specific factor 2: cloning of a putative bone adhesion protein with homology with the insect protein fasciclin I. Biochem J. 1993 Aug 15;294(Pt 1):271–278. doi: 10.1042/bj2940271. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Viamontes G. I., Fochtmann L. J., Kirk D. L. Morphogenesis in Volvox: analysis of critical variables. Cell. 1979 Jul;17(3):537–550. doi: 10.1016/0092-8674(79)90262-9. [DOI] [PubMed] [Google Scholar]
- Viamontes G. I., Kirk D. L. Cell shape changes and the mechanism of inversion in Volvox. J Cell Biol. 1977 Dec;75(3):719–730. doi: 10.1083/jcb.75.3.719. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wenzl S., Sumper M. A novel glycosphingolipid that may participate in embryo inversion in Volvox carteri. Cell. 1986 Aug 15;46(4):633–639. doi: 10.1016/0092-8674(86)90889-5. [DOI] [PubMed] [Google Scholar]
- Woessner J. P., Goodenough U. W. Molecular characterization of a zygote wall protein: an extensin-like molecule in Chlamydomonas reinhardtii. Plant Cell. 1989 Sep;1(9):901–911. doi: 10.1105/tpc.1.9.901. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zinn K., McAllister L., Goodman C. S. Sequence analysis and neuronal expression of fasciclin I in grasshopper and Drosophila. Cell. 1988 May 20;53(4):577–587. doi: 10.1016/0092-8674(88)90574-0. [DOI] [PubMed] [Google Scholar]
- von Heijne G. A new method for predicting signal sequence cleavage sites. Nucleic Acids Res. 1986 Jun 11;14(11):4683–4690. doi: 10.1093/nar/14.11.4683. [DOI] [PMC free article] [PubMed] [Google Scholar]
- von Heijne G. Patterns of amino acids near signal-sequence cleavage sites. Eur J Biochem. 1983 Jun 1;133(1):17–21. doi: 10.1111/j.1432-1033.1983.tb07424.x. [DOI] [PubMed] [Google Scholar]