Abstract
Antibodies to smooth muscle and non-muscle myosin allow the development of smooth muscle and its capillary system in the embryonic chicken gizzard to be followed by immunofluorescent techniques. Although smooth muscle development proceeds in a serosal to luminal direction, angiogenetic cell clusters develop independently at the luminal side close to the epithelial layer, and the presumptive capillaries invade the developing muscle in a luminal to serosal direction. The smooth muscle and non-muscle myosin heavy chains in this avian system cannot be separated by SDS polyacrylamide gel electrophoresis and do not show isoform specificity in immunoblotting, unlike the system found in mammals. Only two myosin heavy chains with Mr of 200 and 196 kDa were separable and considerable immunological cross-reactivity was found between the denatured myosin isoform heavy chains.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Auerbach R, Alby L, Morrissey L, Tu M, Joseph J (1985) Expression of organ-specific antigens on capillary endothelial cells. Microvasc Res 29:401–411
Babij P, Periasamy M (1989) Myosin heavy chain isoform diversity in smooth muscle is produced by differential RNA processing. J Mol Biol 210:673–679
Bennett T, Cobb JLS (1969) Studies of the avian gizzard: the development of the gizzard and its innervation. Z Zellforsch 98:599–621
Borrione AC, Zanellota AMC, Scannapieco G, Pauletto P, Sartore S (1989) Myosin heavy chain isoforms in adult and developing rabbit vascular smooth muscle. Eur J Biochem 183:413–417
Citi S, Kendrick-Jones J (1987) Studies on the structure and conformation of brush border myosin using monoclonal antibodies. Eur J Biochem 165:315–325
Gabella G (1989) Development of the smooth muscle: ultrastructural study of the chick embryo gizzard. Anat Embryol 180:213–226
Giuriato L, Scatena M, Chiavegato A, Tonello M, Scannapieco G, Pauletto P, Sartore S (1992) Nonmuscle myosin isoforms and cell heterogeneity in developing rabbit vascular smooth muscle. J Cell Sci 101:233–246
Goodson HV, Spudich JA (1993) Molecular evolution of the myosin family: relationships derived from comparison of amino acid sequences. Proc Natl Acad Sci USA 90:659–663
Gröschel-Stewart U, Chamley JH, McConnel JD, Burnstock G (1975) Comparison of the reaction of cultured smooth and cardiac muscle cells and fibroblasts to specific antibodies to myosin. Histochemistry 43:215–224
Gröschel-Stewart U, Rakousky C, Franke R, Peleg I, Kahane I, Eldor A, Muhlrad A (1985) Immunohistochemical studies with antibodies to myosin from the cytoplasm and membrane fraction of human blood platelets. Cell Tissue Res 241:399–403
Gröschel-Stewart U, Magel E, Paul E, Neidlinger AC (1989) Pig brain homogenates contain smooth muscle myosin and cytoplasmic myosin isoforms. Cell Tissue Res 257:137–139
Hamada Y, Yanagisawa M, Katsuragawa Y, Coleman JR, Nagata S, Matsuda G, Masaki T (1990) Distinct vascular and intestinal smooth muscle myosin heavy chain mRNAs are encoded by a single-copy gene in the chicken. Biochem Biophys Res Commun 170:53–58
Harlow E, Lane E (1988) Antibodies, a laboratory manual. Cold Springer Harbor, Laboratory, Cold Spring Harbor, NY
Hirai S, Hirabayashi T (1983) Developmental change of protein constituents in chicken gizzards. Dev Biol 97:483–493
Hirai S, Hirabayashi T (1986) Development of myofibrils in the gizzard of chicken embryos: intracellular distribution of structural proteins and development of contractility. Cell Tissue Res 243:487–493
Joyce NC, Haire MF, Palade GE (1985) Contractile proteins in pericytes. II. Immunocytochemical evidence for the presence of two isomyosins in graded concentrations. J Cell Biol 100:1387–1395
Kawamoto S, Adelstein RS (1987) Characterization of myosin heavy chains in cultured aorta smooth muscle cells. J Biol Chem 262:7282–7288
Kawamoto S, Adelstein RS (1991) Characterization of myosin heavy chains: differential expression of two mRNAs and evidence for two different polypeptides. J Cell Biol 112:915–924
Kuro-o M, Nagai R, Tsuchimochi H, Katoh H, Yazaki Y, Ohkubo A, Takaku F (1989) Developmentally regulated expression of vascular smooth muscle myosin heavy chain isoforms. J Biol Chem 264:18272–18275
Kuro-o M, Ryozo N, Nakahara K, Katoh H, Tsai RC, Tsuchimochi H, Yazaki Y, Ohkubo A, Takaku F (1991) cDNA cloning of a myosin heavy chain isoform in embryonic smooth muscle and its expression during vascular development and in arterio-sclerosis. J Biol Chem 266:3768–3773
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
Mohammad MA, Sparrow MP (1988) Changes in myosin heavy chain stoichiometry in pig tracheal smooth muscle during development. FEBS Lett 228:109–112
Mooseker M (1993) A multitude of myosins. Curr Biol 3:245–248
Murakami N, Elzinga M (1992) Immunohistochemical studies on the distribution of cellular myosin II isoforms in brain and aorta. Cell Motil Cytoskeleton 22:281–295
Paul ER, Vo TL, Meyer A, Gröschel-Stewart U (1992) Embryonic chicken gizzard: immunolocalization of collagen and smooth muscle myosin. Cell Tissue Res 270:377–382
Rovner AS, Thompson MM, Murphy RA (1986a) Two different heavy chains are found in smooth muscle myosin. Am J Physiol 250:C861-C870
Rovner AS, Murphy RA, Owens GK (1986b) Expression of smooth muscle and nonmuscle myosin heavy chains in cultured vascular smooth muscle cells. J Biol Chem 261:14740–14745
Saborio JL, Segure M, Flores M, Garca R, Palmer E (1979) Differential expression of gizzard actin genes during chick embryogenesis. J Biol Chem 254:11119–11125
Saez CG, Myers JC, Shows TB, Leinwand LA (1990) Human nonmuscle myosin heavy chain mRNA: generation of diversity through alternative polyadenylation. Proc Natl Acad Sci USA 87:1164–1168
Shohet RV, Conti MA, Kawamoto S, Preston Y, Brill DA, Adelstein RS (1989) Cloning of the cDNA encoding the myosin heavy chain of a vertebrate cellular myosin. Proc Natl Acad Sci USA 86:7726–7730
Simons M, Wang M, McBride OW, Kawamoto S, Yamakawa K, Gdula D, Adelstein RS, Weir L (1991) Human nonmuscle myosin heavy chains are encoded by two genes located on different chromosomes. Circ Res 69:530–539
Stuewer D, Gröschel-Stewart U (1985) Expression of immunoreactive myosin and myoglobin in the developing chicken gizzard. Roux's Arch Dev Biol 194:417–424
Stuewer D, Gröschel-Stewart U (1990) Immune response of rabbits to native G-actins. Biochim Biophys Acta 1039:5–11
Takahashi M, Kawamoto S, Adelstein RS (1992) Evidence for inserted sequences in the head region of nonmuscle myosin specific to the nervous system. J Biol Chem 267:17864–17871
Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 84:9049–9050
Zanellato AMC, Borrione AC, Tonello M, Scannapieco G, Pauletto P, Sartore S (1990) Myosin isoform expression and smooth muscle cell heterogeneity in normal and arteriosclerotic rabbit aorta. Arteriosclerosis 10:996–1009
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Paul, E.R., Christian, AL., Franke, R. et al. Embryonic chicken gizzard: smooth muscle and non-muscle myosin isoforms. Cell Tissue Res 276, 381–386 (1994). https://doi.org/10.1007/BF00306123
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00306123