Abstract
Immunohistochemistry of α-smooth muscle actin and desmin, two markers of smooth muscle cell differentiation, and electron-microscopic observation of thick filaments of myosin were performed on the media of the developing rat hepatic portal vein to gain insights into the chronology of differentiation of its longitudinal and circular smooth muscles. In accordance with the ultrastructural distribution of thin filaments, staining of α-smooth muscle actin is lightly positive in the myoblasts at postnatal day 1 and then extends in probably all muscle cells of the developing vessel. Desmin, which appears later than α-smooth muscle actin in the two muscles, is distributed throughout the longitudinal layer at day 8, whereas the first arrangements of thick filaments are detectable in most longitudinal muscle cells; at this stage, desmin and thick filaments are absent from the poorly differentiated circular muscle cells. The longitudinal muscle cells differentiate in a strikingly synchronized way from day 8 onwards, conferring a homogeneous structure to the developing and mature longitudinal layer. Several desmin-positive cells and a heterogeneous distribution of thick filaments occur in the circular muscle at day 14; the subsequent extension of these filaments in this layer results in a persisting heterogeneous distribution in the young 7-week-old adult. Many features of the mature smooth muscle cells are established within the third week in the longitudinal muscle, approximately one week before those of the circular layer. These results are consistent with the function of the longitudinal muscle as a spontaneously contractile smooth muscle unit, and emphasize the need for its fast maturation to fulfil its major role in the control of portal blood flow.
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References
Bagby RM (1990) Ultrastructure, cytochemistry, and organization of myofilaments in vertebrate smooth muscle cells In: Motta PM (ed) Ultrastructure of smooth muscle. Kluwer, Norwell, pp 23–61
Bennett T, Cobb JLS (1969) Studies on the avian gizzard: the development of the gizzard and its innervation. Z Zellforsch 98:599–621
Bochaton-Piallat ML, Gabbiani F, Ropraz P, Gabbiani G (1992) Cultured aortic smooth muscle cells from newborn and adult rats show distinct cytoskeletal features. Differentiation 49:175–185
Bohr DF, Funaki S (1964) Electrical and mechanical activity of isolated vascular smooth muscle of the rat. Nature 203:192–194
Campbell GR, Chamley-Campbell J, Gröschel-Stewart U, Small JV, anderson P (1979) Antibody staining of 10 nm (100 Å) filaments in cultured smooth, cardiac and skeletal muscle cells. Exp Cell Res 66:417–425
Clowes AW, Clowes MM, Kocher O, Ropraz P, Chaponnier C, Gabbiani G (1988) Arterial smooth muscle cells in vivo: relationship between actin isoform expression, and mitogenesis and their modulation by heparin. J Cell Biol 107:1939–1945
Fatigati V, Murphy RA (1984) Actin and tropomyosin variants in smooth muscle: dependence on tissue type. J Biol Chem 259:14383–14388
Frank ED, Tuszynski GP, Warren L (1982) Localization of vimentin and desmin in BHK 21/C13 cells and in baby hamster kidney. Exp Cell Res 139:235–247
Gabbiani G, Schmid E, Winter S, Chaponnier C, De Chastonay C, Vandekerckhove J, Weber K, Franke WW (1981) Vascular smooth muscle cells differ from other smooth muscle cells: predominance of vimentin filaments and a specific α-type actin. Proc Natl Acad Sci USA 78:298–302
Gabella G (1989) Development of smooth muscle: an ultrastructural study of the gizzard of the chick embryo. Anat Embryol 180:213–226
Garfield RE (1979) Regeneration of smooth muscle: ultrastructure and multipotential properties of smooth muscle. In: Mauro A (ed) Muscle regeneration. Raven Press, New York, pp 383–404
Giuriato L, Scatena M, Chiavegato A, Tonello M, Scannapieco G, Pauletto P, Sartore S (1992) Non-muscle myosin and cell heterogeneity in developing rabbit vascular smooth muscle. J Cell Sci 101:233–246
Golenhofen K (1972) Electrophysiological studies on spontaneous activity of vascular smooth muscle. In: Betz E (ed) Vascular smooth muscle. Proceedings of the 25th International Congress of Physiological Sciences and Annual Meeting of the German Angiological Society. Springer, Berlin Heidelberg New York, pp 1–2
Golenhofen K (1981) Differentiation of calcium activation processes in smooth muscle using selective antagonists. In: Bülbring E, Brading AF, Jones AW, Tomita T (eds) Smooth muscle: an assessment of current knowledge. Arnold, London, pp 157–170
Gröschel-Stewart U, Chamley JH, Campbell GR, Burnstock G (1975) Changes in myosin distribution in dedifferentiating and redifferentiating smooth muscle cells in tissue culture. Cell Tissue Res 165:13–22
Hammersen F (1972) On the fine structure of the portal vein in different rodents. In: Betz E (ed) Vascular smooth muscle. Proceedings of the 25th International Congress of Physiological Sciences and Annual Meeting of the German Angiological Society. Springer, Berlin Heidelberg New York, pp 113–115
Hartshorne DJ, Gorecka A (1980) Biochemistry of the contractile proteins of smooth muscle. In: Bohr DF, Somlyo AP, Sparks HV Jr (eds) Handbook of physiology. The cardiovascular system, Vascular smooth muscle. American Physiological Society, Bethesda, pp 93–120
Holman ME, Kasby CB, Suthers MB, Wilson JAF (1968) Some properties of the smooth muscle of rabbit portal vein. J Physiol 196:111–132
Johansson B (1976) Structural and functional changes in rat portal veins after experimental portal hypertension. Acta Physiol Scand 98:381–383
Kocher O, Gabbiani G (1986) Expression of actin mRNAs in rat aortic smooth muscle cells during development, experimental intimal thickening, and culture. Differentiation 32:245–251
Kocher O, Skalli O, Cerutti D, Gabbiani F, Gabbiani G (1985) Cytoskeletal features of rat aortic cells during development. An electron microscopic, immunohistochemical, and biochemical study. Circ Res 56:829–838
Komuro T, Burnstock G (1980) The fine structure of smooth muscle cells and their relationship to connective tissue in the rabbit portal vein. Cell Tissue Res 210:257–267
Lazarides E, Balzer DR (1978) Specificity of desmin to avian and mammalian muscle cells. Cell 14:429–438
Lennette DA (1978) An improved medium for immunofluorescence microscopy. Am J Clin Pathol 69:647–648
Ljung B, Stage (McMurphy) D (1975) Posthatal ontogenetic development of neurogenic and myogenic control in the rat portal vein. Acta Physiol Scand 94:112–127
Ljung B, Lundberg JM, Dahlström A, Kjellstedt A (1979) Structural and functional ontogenetic development of the rat portal vein after neonatal 6-hydroxydopamine treatment. Acta Physiol Scand 106:271–279
Lundberg J, Ljung B, Stage (McMurphy) D, Dahlström A (1976) Postnatal ontogenic development of the adrenergic innervation pattern in the rat portal vein. Cell Tissue Res 172:15–27
Malmqvist U, Arner A (1988) Contractile properties during development of hypertrophy of the smooth muscle in the rat portal vein. Acta Physiol Scand 133:49–61
Malmqvist U, Arner A (1990) Isoform distribution and tissue contents of contractile and cytoskeletal proteins in hypertrophied smooth muscle from rat portal vein. Circ Res 66:832–845
Mathison R (1983) Actions of neurotransmitters and peptides on longitudinal and circular muscle of the rat portal vein. J Pharm Pharmacol 35:34–37
Ody M, Thiévent A, Millet M, Connat J-L (1993) Postnatal development of the rat portal vein: correlation with occurrence of peptidergic innervation. Cell Tissue Res 272:303–314
Osborn M, Weber K (1983) Tumor diagnosis by intermediate filament typing: a novel tool for surgical pathology. Lab Invest 48:372–394
Owens GK, Thompson MM (1986) Developmental changes in isoactin expression in rat aortic smooth muscle cells in vivo. J Biol Chem 261:13373–13380
Schmid E, Osborn M, Rungger-Brändle E, Gabbiani G, Weber K, Franke WW (1982) Distribution of vimentin and desmin filaments in smooth muscle tissue of mammalian and avian aorta. Exp Cell Res 137:329–340
Skalli O, Ropraz P, Trzeciak A, Benzonana G, Gillessen D, Gabbiani G (1986) A monoclonal antibody against α-smooth muscle actin: a new probe for smooth muscle differentiation. J Cell Biol 103:2787–2796
Skalli O, Vandekerckhove J, Gabbiani G (1987) Actin-isoform pattern as a marker of normal or pathological smooth-muscle and fibroblastic tissues. Differentiation 33:232–238
Somlyo AP, Devine CE, Somlyo AV, Rice RV (1973) Filament organization in vertebrate smooth muscle. Philos Trans R Soc Lond [Biol] 265:223–229
Sutter MC, Ljung B (1977) Contractility, muscle mass, and agonist sensitivity of isolated portal veins from normo- and hypertensive rats. Acta Physiol Scand 99:484–495
Ts'ao CH, Glagov S, Kelsey BF (1970) Special structural features of the rat portal vein. Anat Rec 166:529–540
Ts'ao CH, Glagov S, Kelsey BF (1971) Structure of the mammalian portal vein: postnatal establishment of two mutually perpendicular medial muscle zones in the rat. Anat Rec 171:457–470
Vandekerckhove J, Weber K (1978) At least six different actins are expressed in a higher mammal: an analysis based on the amino acid sequence of the amino-terminal tryptic peptide. J Mol Biol 126:783–802
Woolgar JR, Scott TM (1989) The relationship between innervation and arterial structure in late prenatal and early postnatal development of the rat jejunal artery. J Anat 167:57–70
Yamauchi A, Burnstock G (1969) Post-natal development of smooth muscle cells in the mouse vas deferens. A fine structural study. J Anat 104:1–15
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Thiévent, A., Connat, JL. Cytoskeletal features in longitudinal and circular smooth muscles during development of the rat portal vein. Cell Tissue Res 279, 199–208 (1995). https://doi.org/10.1007/BF00300704
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DOI: https://doi.org/10.1007/BF00300704