Abstract
In the present study, immunogold labeling of ultrathin sections of rat small intestine and liver has been used to obtain insights into the ultrastructural localization and possible functions of annexins. In enterocytes, annexins II, IV, and VI are found at the periphery of the core of each microvillus and of the rootlets, but are absent from the interrootlet space. Annexins II, IV, and VI are also observed close to the interdigitated plasma membrane. In hepatocytes, only annexin VI is found to be concentrated within the microvilli in the bile canaliculi, on the inner face of the sinusoidal cell surface, particularly in the space of Disse, and all along the plasma membrane. Annexin VI is also detected in mitochondria of enterocytes and hepatocytes. These localizations are in agreement with the concept of a close calcium-dependent association of annexins with membranes and cytoskeletal proteins, particularly with actin. Moreover, they support the hypothesis of an involvement of annexins in exocytotic and endocytotic processes, which take place in epithelial cells.
Similar content being viewed by others
References
Cheney RE, Willard MB (1989) Characterization of the interaction between calpactin I and fodrin (non-erythroid spectrin). J Biol Chem 264:18068–18075
Cheney RE, Riley MA, Mooseker MS (1993) Phylogenic analysis of the myosin superfamily. Cell Motil Cytoskeleton 24:215–223
Creutz CE (1992) The annexins and exocytosis. Science 258:924–931
Dedman JR, Welsh MJ, Means AR (1978) Ca2+-dependent regulator. Production and characterization of a monospecific antibody. J Biol Chem 253:7515–7521
Diaz-Munoz M, Hamilton SL, Kaetzel MA, Hazarika P, Dedman JR (1990): Modulation of Ca2+ release channel activity from sarcoplasmic reticulum by annexin VI (67-kDa calcimedin). J Biol Chem 265:15894–15899
Drenckhahn D, Bennett V (1987) Polarized distribution of Mr 210000 and 190000 analogs of erythrocyte ankyrin along the plasma membrane of transporting epithelia, neurons and photoreceptors. Eur J Cell Biol 43:479–486
Drenckhahn D, Dermietzel R (1988) Organization of the actin filament cytoskeleton in the intestinal brush border. A quantitative and qualitative immunoelectron microscope study. J Cell Biol 107:1037–1048
Drenckhahn D, Franz H (1986) Identification of actin-, α-actinin-, and vinculin-containing plaques at the lateral membrane of epithelial cells. J Cell Biol 102:1843–1852
Feinberg JM, Rainteau DP, Kaetzel MA, Dacheux J-L, Dedman JR, Weinman SJ (1991) Differential localization of annexins in ram germ cells: a biochemical and immunocytochemical study. J Histochem Cytochem 39:955–963
Gerke V, Weber K (1984) Identity of p36K phosphorylated upon Rous sarcoma virus transformation with a protein purified from brush borders; calcium-dependent binding to non-erythroid spectrin and F-actin. EMBO J 3:227–233
Glenney JR Jr (1986) Co-precipitation of intestinal p36 with a 73K protein and a high molecular weight factor. Exp Cell Res 162:183–190
Glenney JR Jr, Tack B, Powell MA (1987) Calpactins: two distinct Ca2+-regulated phospholipid- and actin-binding proteins isolated from lung and placenta. J Cell Biol 104:503–511
Goldberg M, Feinberg J, Lecolle S, Kaetzel MA, Rainteau D, Lessard JM, Dedman JR, Weinman S (1991) Co-distribution of annexin VI and actin in secretory ameloblasts and odontoblasts of rat incisor. Cell Tissue Res 263:81–89
Gould KL, Cooper JA, Hunter T (1984) The 46000-dalton tyrosine protein kinase substrate is widespread, whereas the 36000-dalton substrate is only expressed at high levels in certain rodent tissues. J Cell Biol 98:487–497
Hagen SJ, Trier JS (1988) Immunocytochemical localization of actin in epithelial cells of rat small intestine by light and electron microscopy. J Histochem Cytochem 36:717–727
Kaetzel MA, Hazarika P, Dedman JR (1989) Differential tissue expression of three 35-kDa annexin calcium-dependent phospholipid-binding proteins. J Biol Chem 264:14463–14470
Karasik A, Pepinsky RB, Shoelson SE, Kahn CR (1988) Lipocortins 1 and 2 as substrates for the insulin receptor kinase in rat liver. J Biol Chem 263:11862–11867
Koob R, Zimmermann M, Schoner W, Drenckhahn D (1987) Colocalization and precipitation of ankyrin and Na+, K+-ATPase in kidney epithelial cells. Eur J Cell Biol 45:230–237
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
Lessard JL (1988) Two monoclonal antibodies to actin: One muscle selective and one generally reactive. Cell Motil Cytoskeleton 10:349–362
Massey D, Traverso V, Maroux S (1991) Lipocortin IV is a basolateral cytoskeleton constituent of rabbit enterocytes. J Biol Chem 266:3125–3130
Mathew JK, Krolak JM, Dedman JR (1986) Calcimedins: purification and characterization from chicken gizzard and rat and bovine livers. J Cell Biochem 32:223–234
Mooseker MS (1985) Organization, chemistry and assembly of the cytoskeletal apparatus of the intestinal brush-border. Annu Rev Cell Biol 1:209–241
Moss SE (1992) The annexins. Portland, London, Chapel Hill
Newman R, Tucker A, Ferguson C, Tsernoglou D, Leonhard K, Crumpton MJ (1989) Crystallization of p68 on lipid monolayers and as three-dimensional single crystals. J Mol Biol 206:213–219
Pepinsky RB, Tizard R, Mattaliano RJ, Sinclair LK, Miller GT, Browning JL, Chow EP, Burne C, Huang KS, Pratt D, Wachter L, Hession C, Frey AZ, Wallner BP (1988) Five distinct calcium and phospholipid binding proteins share homology with lipocortin I. J Biol Chem 263:10799–10811
Pollard HB, Guy HR, Arispe N, De la Fuente M, Lee G, Rojas EM, Pollard JR, Srivastava M, Zhang-Keck ZY, Merezhinskaya N, Caohuy H, Burns AL, Rojas E (1992) Calcium channel and membrane fusion activity of synexin and other members of the annexin gene family. Biophys J 62:15–18
Sawtell NM, Hartman AL, Lessard JL (1988) Unique isoactins in the brush border of rat intestinal epithelial cells. Cell Motil Cytoskeleton 11:318–325
Shadle PJ, Gerke V, Weber K (1985) Three Ca2+-binding proteins from porcine liver and intestine differ immunologically and physicochemically and are distinct in Ca2+ affinities. J Biol Chem 260:16354–16360
Smith VL, Dedman JR (1986) An immunological comparison of several novel calcium-binding proteins. J Biol Chem 261:15815–15818
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 76:4350–4354
Weinman S, Ores-Carton C, Rainteau D, Puszkin S (1986) Immunoelectron microscopic localization of calmodulin and phospholipase A2 in spermatozoa. J Histochem Cytochem 34:1171–1177
Weinman S, Weinman J, Rainteau D (1994) Calmodulin in rat enterocyte: an immunogold electron microscope study. Cell Tissue Res 276:353–357
Wice BM, Gordon JI (1992) A strategy for isolation of cDNAs encoding proteins affecting human intestinal epithelial cell growth and differentiation: characterization of a novel gutspecific N-myristoylated annexin. J Cell Biol 116:405–422
Wolenski JS, Hayden SM, Forscher P, Mooseker MS (1993) Calcium-calmodulin and regulation of brush border myosin-I MgATPase and mechanochemistry. J Cell Biol 122:613–621
Zot HG, Doberstein SK, Pollard TD (1992) Myosin-I moves actin filaments on a phospholipid substrate: implication for membrane targeting. J Cell Biol 116:367–376
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Weinman, J.S., Feinberg, J.M., Rainteau, D.P. et al. Annexins in rat enterocyte and hepatocyte: an immunogold electron-microscope study. Cell Tissue Res. 278, 389–397 (1994). https://doi.org/10.1007/BF00414181
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00414181