Expression of elastin, smooth muscle alpha-actin, and c-Jun as a function of the embryonic lineage of vascular smooth muscle cells

  • Preston F. GadsonJr.
  • Candace Rossignol
  • Judy McCoy
  • Thomas H. Rosenquist
Cellular Models
  • 46 Downloads

Summary

In the avian embryo, vascular smooth muscle cells (VSMC) in the aortic arch (elastic) arteries originate in the neural crest, whereas other VSMC develop from local mesoderm. These two lineages have been shown previously to be significantly different in the timing and expression of the smooth muscle phenotype and in their respective abilities to produce an orderly elastic matrix. Two differing kinds of VSMC also have been shown in mammals. In the experimental absence of neural crest (NC) in the avian embryo, the matrix is spatially disordered. The molecular basis of the difference between the normal NC-VSMC and the surrogate mesodermal (MDM)-VSMC has not previously been investigated. In this study the expression of vascular smooth muscle alpha-actin, tropoelastin, c-fos and c-jun were examined via immunoblotting, immunohistochemistry, Northern blot, and/or transcription run-on assays. Control avian VSMC of NC origin were compared with experimental MDM-derived VSMC that populate the cardiac outflow after surgical ablation of the NC. The results show that, when they are grown under identical conditions in vitro or freshly removed from an embryonic vessel, surrogate MDM-VSMC express about 10 times more alpha-actin and tropoelastin than the normal NC-VSMC; and MDM-VSMC express up to 15 times more c-jun, whereas c-fos was not different. These results show profound heterogeneity in the regulation of VSMC-specific genes that is based in the embryonic lineage of the cells.

Key words

vascular smooth muscle alpha-actin elastin c-jun c-fos embryonic lineage neural crest 

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References

  1. 1.
    Angel, P.; Karin, M. The role ofJun, Fos and the AP1 complex in cell-proliferation and transformation. Biochem. Biophys. Acta 1072:129–157; 1991.PubMedGoogle Scholar
  2. 2.
    Barone, L. M.; Wolfe, B. L.; Faris, B., et al. Elastin mRNA levels and insoluble elastin accumulation in neonatal rat smooth muscle cell cultures. Biochemistry 27:3175–3182; 1988.PubMedCrossRefGoogle Scholar
  3. 3.
    Baule, V. J.; Foster, J. A. Multiple chick tropoelastin mRNAs. Biochem. Biophys. Res. Commun. 154:1054–1060; 1988.PubMedCrossRefGoogle Scholar
  4. 4.
    Beall, A. C.; Rosenquist, T. H. Smooth muscle cells of neural crest origin form the aorticopulmonary septum in the avian embryo. Anat. Rec. 226:360–366; 1990.PubMedCrossRefGoogle Scholar
  5. 5.
    Blank, R. S.; Owens, G. K. Platelet-derived growth factor regulates actin isoform expression and growth state in cultured rat aortic smooth muscle cells. J. Cell Physiol. 142:635–645; 1990.PubMedCrossRefGoogle Scholar
  6. 6.
    Bohmann, D.; Bos, T. J.; Admon, A., et al. Human proto-oncogene c-jun encodes a DNA-binding protein with structural and functional properties of transcription factor AP1. Science 238:1386–1392; 1987.PubMedCrossRefGoogle Scholar
  7. 7.
    Campbell, G. R.; Campbell, J. H.; Manderson, J. A., et al. Arterial smooth muscle: a multifunctional mesenchymal cell. Arch. Pathol. Lab. Med. 112:977–986; 1988.PubMedGoogle Scholar
  8. 8.
    Carter, K.; Bryan, S.; Gadson, P., et al. Deadenlylation of alphal-acid glycoprotein mRNA in cultured hepatic cells during stimulation by dexamethasone. J. Biol. Chem. 264:4112–4119; 1989.PubMedGoogle Scholar
  9. 9.
    Chirgwin, J. M.; Przybala, H. E.; MacDonald, R. J., et al. Isolation of biologically active ribonucleic acid. Biochemistry 18:5294–5299; 1979.PubMedCrossRefGoogle Scholar
  10. 10.
    Clarkson, T. B.; Prichard, R. W.; Netsky, M. G., et al. Atherosclerosis in pigeons: its spontaneous occurrence and resemblance to human atherosclerosis. Arch. Pathol. 68:143; 1959.Google Scholar
  11. 11.
    Curran, T. M.; Gordon, B.; Robino, K. L., et al. Isolation and characterization of the c-Fos (rat) cDNA and analysis of post-translational modification in vitro. Oncogene 2:79–84; 1987.PubMedGoogle Scholar
  12. 12.
    Franz, T. Persistent truncus arteriosus in the Splotch mutant mouse. Anat. Embryol. 180:457; 1989.PubMedCrossRefGoogle Scholar
  13. 13.
    Gadson, P.; McCoy, J.; Wikstrom, A. C., et al. Suppression of protein kinase C and the stimulation of glucocorticoid receptor synthesis by dexamethasone in human fibroblasts derived from tumor tissue. J. Cell Biochem. 43:185–198; 1990.PubMedCrossRefGoogle Scholar
  14. 14.
    Giachelli, C.; Bae, N.; Lombardi, D., et al. Molecular cloning and characterization of 2B7, a rat mRNA which distinguishes smooth muscle phenotypes in vitro and is identical to osteopontin (secreted phosphoprotein I, 2aR). Biochem. Biophys. Res. Commun. 177:867–873; 1991.PubMedCrossRefGoogle Scholar
  15. 15.
    Giachelli, C. M.; Majesky, M. W.; Schwartz, S. M. Developmentally regulated cytochrome P-450Ia1 expression in cultured rat smooth muscle cells. J. Biol. Chem. 266:3981–3986; 1991.PubMedGoogle Scholar
  16. 16.
    Gordon, D.; Mohai, L. G.; Schwartz, S. M. Induction of polyploidy in cultures of neonatal rat aortic smooth muscle cells. Circ. Res. 59:633–644; 1986.PubMedGoogle Scholar
  17. 17.
    Hood, L. C.; Rosenquist, T. H. Coronary artery development in the chick: origin and deployment of smooth muscle cells, and the effects of neural crest ablation. Anat. Rec 234:291–300; 1992.PubMedCrossRefGoogle Scholar
  18. 18.
    Hultgardh-Nilsson, A.; Larsson, S. H.; Jin, P., et al. Neurokinin A induces expression of the c-fos, c-jun and c-myc genes in rat smooth muscle cells. Eur. J. Biochem. 194:527–532; 1990.PubMedCrossRefGoogle Scholar
  19. 19.
    Jackson, W. F.; Gauldin, H. E.; Tomita, H., et al. Neural crest ablation does not alter ventricular pressure or estimated cardiac output despite altered morphology. Ann. NY Acad. Sci. 588:389–392; 1990.CrossRefGoogle Scholar
  20. 20.
    Kirby, M. L.; Gale, T. F.; Stewart, D. E. Neural crest cells contribute to aorticopulmonary septation. Science 220:1059; 1983.PubMedCrossRefGoogle Scholar
  21. 21.
    Kirby, M. L. Cardiac morphogenesis—recent research advances. Pediatr. Res. 21:219; 1988.CrossRefGoogle Scholar
  22. 22.
    Kirby, M. L.; Waldo, K. L. Role of neural crest in congenital heart disease. Circulation 82:332; 1990.PubMedGoogle Scholar
  23. 23.
    Kocher, O.; Skalli, O.; Bloom, W. S., et al. Cytoskeleton of rat aortic smooth muscle cells. Normal and experimental intimal thickening. Lab. Invest. 50:645–651; 1984.PubMedGoogle Scholar
  24. 24.
    Lauper, N. T.; Unni, K. K.; Kottke, B. A., et al. Anatomy and histology of aorta of White Carneau pigeon. Lab. Invest. 32:536; 1975.PubMedGoogle Scholar
  25. 25.
    LeLievre, C. S.; LeDouarin, N. M. Mesenchymal derivatives of the neural crest: analysis of chimaeric quail and chick embryos. J. Embryol. Exp. Morphol. 34:125; 1975.Google Scholar
  26. 26.
    Majesky, M. W.; Benditt, E. P.; Schwartz, S. M. Expression and developmental control of platelet-derived growth factor A-chain and B-chain/Sis genes in rat aortic smooth muscle cells. Proc. Natl. Acad. Sci. USA 85:1524–1528; 1988.PubMedCrossRefGoogle Scholar
  27. 27.
    Majesky, M. W.; Schwartz, S. M. Smooth muscle diversity in arterial wound repair. Toxicol. Pathol. 18:554–559; 1990.PubMedGoogle Scholar
  28. 28.
    Miano, J. M.; Tota, R. R.; Vlasic, N., et al. Early proto-oncogene expression in rat aortic smooth muscle cells following endothelial removal. Am. J. Pathol. 137:761–765; 1990.PubMedGoogle Scholar
  29. 29.
    Morrison-Graham, K.; Weston, J. A. Mouse mutants provide new insights into the role of extracellular matrix in cell migration and differentiation. Trends Genet. 5:116–121; 1989.PubMedCrossRefGoogle Scholar
  30. 30.
    Naftilan, A. J.; Gilliland, G. K.; Eldridge, C. S., et al. Induction of the proto-oncogene c-jun by angiotensin II. Mol. Cell. Biol. 10:5536–5540; 1990.PubMedGoogle Scholar
  31. 31.
    Nishibatake, M.; Kirby, M. L.; Forbes, G. Pathogenesis of persistent truncus arteriosus and dextroposed aorta in the chick embryo after neural crest ablation. Lab. Invest. 75:255; 1987.Google Scholar
  32. 32.
    Owens, G. K.; Loeb, A.; Gordon, D., et al. Expression of smooth muscle-specific alpha-isoactin in cultured vascular smooth muscle cells: relationship between growth and cyto-differentiation. J. Cell Biol. 102:343–352; 1986.PubMedCrossRefGoogle Scholar
  33. 33.
    Pratt, R. M.; Goulding, E. H.; Abbott, B. D. Retinoic acid inhibits migration of cranial neural crest cells in the cultured mouse embryo. J. Craniofacial Genet. Dev. Biol. 7:205; 1987.Google Scholar
  34. 34.
    Rein, A. J. J. T.; Dollberg, S.; Gale, R. Genetics of conotruncal malformation: review of the literature and report of a consanguinous kindred with various conotruncal malformations. Am. J. Med. Genet. 36:353; 1990.PubMedCrossRefGoogle Scholar
  35. 35.
    Roberts, J. C.; Strauss, R. Comparative atherosclerosis. New York: Harper and Row; 1965.Google Scholar
  36. 36.
    Rosenberg, H. G.; Williams, W. G.; Trusler, G. A., et al. Structural composition of central pulmonary arteries. Growth potential after surgical shunts. Surgury 94:498–503; 1987.Google Scholar
  37. 37.
    Rosenquist, T. H.; McCoy, J. R.; Waldo, K., et al. Origin and propagation of elastogenesis in the cardiovascular system. Anat. Rec. 221:860–871; 1988.PubMedCrossRefGoogle Scholar
  38. 38.
    Rosenquist, T. H.; Beall, A. C.; Modis, L., et al. Impaired elastic matrix development in the great arteries after ablation of the cardiac neural crest. Anat. Rec. 226:347–359; 1990.PubMedCrossRefGoogle Scholar
  39. 39.
    Rosenquist, T. H.; Beall, A. C. Elastogenic cells in the developing cardiovascular system: smooth muscle, non-muscle and cardiac neural crest. Ann. NY Acad. Sci. 588:106–119; 1990.PubMedCrossRefGoogle Scholar
  40. 40.
    Rosenquist, T. H.; Fray-Gavalas, C. A.; Waldo, K. L., et al. Development of the musculoelastic septation complex in the avian truncus arteriosus. Am. J. Anat. 189:339; 1990.PubMedCrossRefGoogle Scholar
  41. 41.
    Rosenquist, T. H.; Modis, L. Spatial order of collagens in the great vessels, associated with congenital heart defects. Anat. Rec. 229:116–124; 1991.PubMedCrossRefGoogle Scholar
  42. 42.
    Ruzica, D. L.; Schwartz, R. J. Sequential activation of alpha-actin genes during avian cardiogenesis: vascular smooth muscle alpha-actin gene transcripts mark the onset of cardiomyocyte differentiation. J. Cell Biol. 107:2575–2586; 1988.CrossRefGoogle Scholar
  43. 43.
    Sambrook, J.; Fritsch, E. F.; Maniatis, T. Molecular cloning: a laboratory manual. New York: Cold Spring Harbor Press; 1989:7.2–7.83.Google Scholar
  44. 44.
    Schwartz, S. M.; Campbell, G. H.; Campbell, J. H. Replication of smooth muscle cells in vascular disease. Circ. Res. 58:427; 1986.PubMedGoogle Scholar
  45. 45.
    Schwartz, S. M.; Heimark, R. L.; Majesky, M. W. Developmental mechanisms underlying pathology of arteries. Physiol. Rev. 70:1177–1209; 1990.PubMedGoogle Scholar
  46. 46.
    Seifert, R. A.; Schwartz, S. M.; Bowen-Pope, D. F. Developmentally regulated production of platelet-derived growth factor-like molecules. Nature 311:669–671; 1984.PubMedCrossRefGoogle Scholar
  47. 47.
    Siebert, J. R.; Graham, J. M.; MacDonald, C. Pathological features of the CHARGE association: support for involvement of the neural crest. Teratology 31:331; 1985.PubMedCrossRefGoogle Scholar
  48. 48.
    Skalli, O.; Ropaz, P.; Trzeciak, A., et al. A monoclonal antibody against alpha-smooth muscle actin: a new probe for smooth muscle differentiation. J. Cell Biol. 103:2787–2796; 1986.PubMedCrossRefGoogle Scholar
  49. 49.
    Smith-Thomas, L.; Lott, I.; Bronner-Fraser, M. Effects of isoretinoin on the behavior of neural crest cells in vitro. Dev. Biol. 123:276; 1987.PubMedCrossRefGoogle Scholar
  50. 50.
    Sumida, H.; Akimoto, N.; Nakamura, H. Distribution of the neural crest cells in the heart of birds: a three dimensional analysis. Anat. Embryol. 180:29–35; 1989.PubMedCrossRefGoogle Scholar
  51. 51.
    Topouzis, S.; Catravas, J. D.; Ryan, J., et al. Influence of embryonic development, origin and anatomic location of smooth muscle on angiotensin converting enzyme activity in chicken aorta. Circ. Res. 71:923–931; 1992.PubMedGoogle Scholar
  52. 52.
    Turla, M. B.; Thompson, M. M.; Corjay, M. H., et al. Mechanisms of angiotensin II- and arginine vasopressin-induced increases in protein synthesis and content in cultured rat aortic smooth muscle cells: evidence for selective increases in smooth muscle isoactin expression. Circ. Res. 68:288–299; 1991.PubMedGoogle Scholar
  53. 53.
    Ussry, T. W.; Arensman, F. W.; Leatherbury, L., et al. Non-cardiac defects associated with conotruncal abnormalities—further implications of neural crest influence. J. Am. Coll. Cardiol. 13:118A; 1989.Google Scholar
  54. 54.
    Wrenn, R. W.; Raeuber, C. L.; Herman, L. E., et al. Transforming growth factor beta: signal transduction via protein kinase C in cultures of embryonic smooth muscle cells. In Vitro Cell Dev. Biol. 29A:73–78; 1993.PubMedGoogle Scholar

Copyright information

© Tissue Culture Association 1993

Authors and Affiliations

  • Preston F. GadsonJr.
    • 1
  • Candace Rossignol
    • 2
  • Judy McCoy
    • 2
  • Thomas H. Rosenquist
    • 1
  1. 1.Department of Cell Biology and AnatomyUniversity of Nebraska Medical CenterOmaha
  2. 2.Department of Cellular Biology and AnatomyMedical College of GeorgiaAugusta

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