Microtubule-associated protein 1 light chain 3 is a fibronectin mRNA- binding protein linked to mrna translation in lamb vascular smooth muscle cells

Journal of Clinical Investigation

Volumn 100, Issue 12, 1997, Pages 3070-3082

  Zhou, Bin ^a,b,c   Boudreau, Nancy ^a,b,c,f   Coulber, Claire ^a,b,c   Hammarback, James ^d   Rabinovitch, Marlene ^a,b,c,e  

^a HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d WAKE FOREST SCHOOL OF MEDICINE   (United States)

^e HOSPITAL FOR SICK CHILDREN   (Canada)

^f VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cell migration; Ductus arteriosus; Extracellular matrix protein; Protein purification; Transfection

Indexed keywords

BINDING PROTEIN; FIBRONECTIN; MESSENGER RNA; MICROTUBULE ASSOCIATED PROTEIN 1; MICROTUBULE ASSOCIATED PROTEIN 1 LIGHT CHAIN 3; RNA BINDING PROTEIN; SCLEROPROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL MIGRATION; DUCTUS ARTERIOSUS; GENE OVEREXPRESSION; GENETIC TRANSFECTION; LAMB; NONHUMAN; PHENOTYPE; PLASMID; PRIORITY JOURNAL; PROTEIN PURIFICATION; RNA TRANSLATION; SMOOTH MUSCLE FIBER; VASCULAR SMOOTH MUSCLE;

EID: 0031438648     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI119862     Document Type: Article

References (54)

1. Gittenberger-de-Groot, A.C., J.L.M. Strengers, M. Mentink, R.E. Poelmann, and D.F. Patterson. 1985. Histologic studies on normal and persistent ductus arteriosus in the dog. J. Am. Coll. Cardiol. 6:394-404.
2. Gittenberger-de-Groot, A.C., A.J.M. Moulaert, and J.F. Hitchcock. 1980. Histology of the persistent arteriosus in cases of congenital rubella. Circulation. 62:183-186.
3. Gittenberger-de-Groot, A.C., I. Ertbruggen, A.J.M. Moulaert, and E. Harinck. 1980. The ductus arteriosus in the preterm infant: histologic and clinical observations. J. Pediatr. 96:88-93.
4. Boudreau, N., and M. Rabinovitch. 1991. Developmentally regulated changes in extracellular matrix in endothelial and smooth muscle cells in the ductus arteriosus may be related to intimai proliferation. Lab. Invest. 64:187-199.
5. Boudreau, N., E.A. Turley, and M. Rabinovitch. 1991. Fibronectin, hyaluronan and a hyaluronan binding protein contribute to increased ductus arteriosus smooth muscle migration. Dev. Biol. 143:235-247.
6. Boudreau, N., N. Clausell, J. Boyle, and M. Rabinovitch. 1992. Transforming growth factor-beta regulates increased ductus arteriosus endothelial glycosaminoglycan synthesis and a post-transcriptional mechanism controls increased smooth muscle fibronectin, features associated with intimai proliferation. Lab. Invest. 67:350-359.
7. Hynes, R.O., and A.D. Lander. 1992. Contact and adhesive specificities in the associations, migration, and targeting of cells and axons. Cell. 68:303-322.
8. Dean, D.C., M.S. Blakeley, R.F. Newby, P. Ghazal, L. Hennighausen, and S. Bourgeois. 1989. Forskolin inducibility and tissue-specific expression of the fibronectin promoter. Mol. Cell. Biol. 9:1498-1506.
9. Penttinen, R., S. Kobayashi, and P. Bornstein. 1988. Transforming growth factor β increases mRNA for matrix proteins both in the presence and in the absence of changes in mRNA stability. Proc. Natl. Acad. Sci. USA. 85: 1105-1108.
10. Ffrench-Constant, C., L. Van De Water, H.F. Dvorak, and R.O. Hynes. 1989. Reappearance of an embryonic pattern of fibronectin splicing during wound healing in the adult rat. J. Cell Biol. 109:903-914.
11. Glukhova, M.A., M.G. Frid, B.V. Shekhonin, T.D. Vasilevskaya, J. Grunwald, M. Saginati, and V.E. Koteliansky. 1989. Expression of extra domain A fibronectin sequence in vascular smooth muscle cells is phenotype dependent. J. Cell Biol. 109:357-366.
12. Rasoamanantena, P., R. Thweatt, J. Labat-Robert, and S. Goldstein. 1994. Altered regulation of fibronectin gene expression in Werner syndrome fibroblasts. Exp. Cell Res. 213:121-127.
13. Chou, L., J.D. Firth, V.-J. Uitto, and D.M. Brunette. 1995. Substratum surface topography alters cell shape and regulates fibronectin mRNA level, mRNA stability, secretion and assembly in human fibroblasts. J. Cell Sci. 108: 1563-1573.
14. Dean, D.C., R.F. Newby, and S. Bourgeois. 1988. Regulation of fibronectin biosynthesis by dexamethasone, transforming growth factor β, and cAMP in human cell lines. J. Cell. Biol. 106:2159-2170.
15. Chandler, L.A., and S. Bourgeois. 1991. Posttranscriptional down-regulation of fibronectin in N-ras-transformed cells. Cell Growth Differ. 2:379-384.
16. Klausner, R.D., and J.B. Harford. 1989. cis-trans models for posttranscriptional gene regulation. Science. 246:870-873.
17. Caput, D., B. Beuller, K. Hartog, S. Brown-Shimer, and A. Cerami. 1986. Identification of a common nucleotide sequence in the 3′ -untranslated region of mRNA molecules specifying inflammatory mediators. Proc. Natl. Acad. Sci. USA. 83:1670-1675.
18. Kornblihtt, A.R., K. Vibe-Pedersen, and F.E. Baralle. 1983. Isolation and characterization of cDNA clones for human and bovine fibronectins. Proc. Natl. Acad. Sci. USA. 80:3218-3222.
19. Schwarbauer, J.E., J.W. Tamkun, I.R. Lemischka, and R.O. Hynes. 1983. Three different fibronectin mRNAs arise by alternative splicing within the coding region. Cell. 35:421-431.
20. Jones, T.R., and M.D. Cole. 1987. Rapid cytoplasmic turnover of c-myc mRNA: requirement of 3′ untranslated sequences. Mol. Cell. Biol. 7:4513-4519.
21. Shaw, G., and R. Kamen. 1986. A conserved AU sequence from the 3′ untranslated region of GM-CSF mRNA mediates selective mRNA degradation. Cell. 46:659-667.
22. Shyu, A.-B., J.G. Belasco, and M.E. Greenberg. 1991. Two distinct destabilizing elements in the c-fos message trigger deadenylation as a first step in rapid mRNA decay. Genes Dev. 5:221-231.
23. Wilson, T., and R. Treisman. 1988. Removal of poly(A) and consequent degradation of c-fos mRNA facilitated by AU-rich sequences. Nature. 336:396-399.
24. Kruys, V., O. Marinx, G. Shaw, J. Deschamps, and G. Huez. 1989. Translational blockade imposed by cytokine-derived UA-rich sequences. Science. 245:85-88.
25. Kruys, V., M. Wathelet, P. Poupart, R. Contreras, W. Fiers, J. Content, and G. Huez. 1987. The 3′ untranslated region of the human interferon-β mRNA has an inhibitory effect on translation. Proc. Natl. Acad. Sci. USA. 84: 6030-6034.
26. Grafi, G., I. Sela, and G. Galili. 1993. Translational regulation of human beta interferon mRNA: association of the 3′ AU-rich sequence with the poly(A) tail reduces translation efficiency in vitro. Mol. Cell. Biol. 13:3487-3493.
27. Han, J., T. Brown, and B. Beutler. 1990. Endotoxin-responsive sequences control cachectin/tumor necrosis factor biosynthesis at the translational level. J. Exp. Med. 171:465-475.
28. Aharon, T., and R.J. Schneider. 1993. Selective destabilization of shortlived mRNAs with the granulocyte-macrophage colony-stimulating factor AU-rich 3′ noncoding region is mediated by a cotranslational mechanism. Mol. Cell. Biol. 13:1971-1980.
29. Savant-Bhonsale, S., and D.W. Cleveland. 1992. Evidence for instability of mRNAs containing AUUUA motifs mediated through translation-dependent assembly of a > 20S degradation complex. Genes Dev. 6:1927-1939.
30. Winstall, E., M. Gamache, and V. Raymond. 1995. Rapid mRNA degradation mediated by the c-fos 3′ AU-rich element and that mediated by the granulocyte-macrophage colony-stimulating factor 3′ AU-rich element occur through similar polysome-associated mechanisms. Mol. Cell. Biol. 12:2931-2940.
31. Malter, J.S. 1989. Identification of an AUUUA-specific messenger RNA binding protein. Science. 246:664-666.
32. Bohjanen, P.R., B. Petryniak, C.H. June, C.B. Thompson, and T. Lindsten. 1992. AU RNA-binding factors differ in their binding specificities and affinities. J. Biol. Chem. 267:6302-6309.
33. Levine, T.D., F. Gao, P.H. King, L.G. Andrews, and J.D. Keene. 1993. Hel-N1: an autoimmune RNA-binding protein with specificity for 3′ uridylaterich untranslated regions of growth factor mRNAs. Mol. Cell. Biol. 13:3494-3504.
34. Ma, W.-J., S. Cheng, C. Campbell, A. Wright, and H. Furneaux. 1996. Cloning and characterization of HuR, a ubiquitously expressed Elav-like protein. J. Biol. Chem. 271:8144-8151.
35. Nakagawa, J., H. Waldner, S. Meyer-Monard, J. Hofsteenge, P. Jeno, and C. Moroni. 1995. AUH, a gene encoding an AU-specific RNA binding protein with intrinsic enoyl-CoA hydratase activity. Proc. Acad. Natl. Sci. USA. 92: 2051-2055.
36. Zhang, W., B.J. Wagner, K. Ehrenman, A.W. Schaefer, C.T. DeMaria, D. Crater, K. DeHaven, L. Long, and G. Brewer. 1993. Purification, characterization, and cDNA cloning of an AU-rich element RNA-binding protein, AUF1. Mol. Cell. Biol. 13:7652-7665.
37. Mann, S.S., and J.A. Hammarback. 1994. Molecular characterization of light chain 3: a microtubule binding subunit of MAP1A and MAP1B. J. Biol. Chem. 269:11492-11497.
38. Rabinovitch, M., S. Beharry, T. Bothwell, and G. Jackowski. 1988. Qualitative and quantitative differences in protein synthesis comparing fetal lamb ductus arteriosus endothelium and smooth muscle with cells from adjacent vascular sites. Dev. Biol. 130:250-258.
39. Luckow, B., and G. Schütz. 1987. CAT constructions with multiple unique restriction sites for the functional analysis of eukaryotic promoters and regulatory elements. Nucleic Acids Res. 15:5490.
40. Ellis, L., E. Clauser, D.O. Morgan, M. Edery, R.A. Roth, and W.J. Rutter. 1986. Replacement of insulin receptor tyrosine residues 1162 and 1163 compromises insulin-stimulated kinase activity and uptake of 2-deoxyglucose. Cell. 45:721-732.
41. Milligan, J.F., D.R. Groebe, G.W. Witherell, and O.C. Uhlenbeck. 1987. Oligoribonucleotide synthesis using T7 RNA polymerase and synthetic DNA templates. Nucleic Acids Res. 15:8783-8797.
42. Sambrook, J., E.F. Frisch, and T. Maniatis. 1989. Molecular Cloning: A Laboratory Manual. Vol. 3. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
43. Kohout, T.A., J.J. O'Brian, S.T. Gaa, W.J. Lederer, and T.B. Rogers. 1996. Novel adenovirus component system that transfects cultured cardiac cells with high efficiency. Circ. Res. 78:971-977.
44. Bassell, G.J., C.M. Powers, K.L. Taneja, and R.H. Singer. 1994. Single mRNAs visualized by ultrastructural in situ hybridization are principally localized at actin filament intersections in fibroblasts. J. Cell Biol. 126:863-876.
45. Malter, J.S., and Y. Hong. 1991. A redox switch and phosphorylation are involved in the post-translational up-regulation of the adenosine-uridine binding factor by phorbol ester and ionophore. J. Biol. Chem. 266:3167-3171.
46. Burd, C.G., E.L. Matunis, and G. Dreyfuss. 1991. The multiple RNA-binding domains of the mRNA poly(A)-binding protein have different RNA-binding activities. Mol. Cell. Biol. 11:3419-3424.
47. Singer, R.H. 1992. The cytoskeleton and mRNA localization. Curr. Opin. Cell Biol. 3:719-721.
48. St. Johnston, D. 1995. The intracellular localization of messenger RNAs. Cell. 81:161-170.
49. Suprenant, K.A. 1993. Microtubules, ribosomes, and RNA: evidence for cytoplasmic localization and translational regulation. Cell Motil. Cytoskeleton. 25:1-9.
50. Kislauskis, E.H., X. Zhu, and R.H. Singer. 1994. Sequence responsible for intracellular localization of β-actin messenger RNA also affects cell phenotype. J. Cell Biol. 127:441-451.
51. Kim-Ha, J., K. Kerr, and P.M. Macdonald. 1995. Translational regulation of oskar mRNA by Bruno, an ovarian RNA-binding protein, is essential. Cell. 81:403-412.
52. Ferrandon, D., L. Elphick, C. Nusslein-Volhard, and D. St. Johnston. 1994. Staufen protein associates with the 3′UTR of bicoid mRNA to form particles that move in a microtubule-dependent manner. Cell. 79:1221-1232.
53. Schumacher, J.M., K. Lee, S. Edelhoff, and R.E. Braun. 1995. Spnr. a murine RNA-binding protein that is localized to cytoplasmic microtubules. J. Cell Biol. 129:1023-1032.
54. Han, J.R., G.K. Yiu, and N.O. Hecht. 1995. Testis/brain RNA-binding protein attaches translationally repressed and transported mRNAs to microtubules. Proc. Natl. Acad. Sci. USA. 92:9550-9554.