Home LiteratureArticle Details
PMID: 2956268 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Assembly of the intestinal brush border: appearance and redistribution of microvillar core proteins in developing chick enterocytes.

The Journal of cell biology ·Vol. 105 ·No. 1 ·1987-07-00 ·Pages 335-44

Shibayama T, Carboni JM, Mooseker MS

Abstract

The assembly of the intestinal microvillus cytoskeleton during embryogenesis in the chick was examined by immunochemical and light microscopic immunolocalization techniques. For these studies, affinity-purified antibodies reactive with three major cytoskeletal proteins of the adult intestinal microvillus, fimbrin, villin, and the 110-kD subunit of the 110K-calmodulin protein complex were prepared. Immunocytochemical staining of frozen sections of embryonic duodena revealed that all three proteins were present at detectable levels at the earliest stages examined, day 7-8 of incubation (Hamilton/Hamburger stages 25-30). Although initially all three proteins were diffusely distributed throughout the cytoplasm, there was a marked asynchrony in the accumulation of these core proteins within the apical domain of the enterocyte. Villin displayed concentrated apical staining by embryonic day 8 (stage 28), while the apical concentration of fimbrin was first observed at embryonic day 10 (stage 37). Diffuse staining of the enterocyte cytoplasm with the anti-110K was observed throughout development until a few days before hatch. By embryonic day 19-21 110K staining was concentrated at the cell periphery (apical and basolateral). The restricted apical localization characteristic of 110K in the adult brush border was not observed until the day of hatching. Immunoblot analysis of whole, solubilized embryonic duodena confirmed the presence of 110K, villin, and fimbrin throughout development and indicated substantial increases in all three proteins, particularly late in development. Immunoblot staining with anti-110K also revealed the presence of a high molecular mass (200 kD) immunoreactive species in embryonic intestine. This 200-kD form was absent from isolated embryonic enterocytes and may be a component of intestinal smooth muscle.

MeSH Terms
Animals Ca(2+) Mg(2+)-ATPase/analysis Calmodulin/analysis Carrier Proteins/analysis Chick Embryo Cytoskeletal Proteins/metabolism Cytoskeleton/metabolism,ultrastructure Duodenum/cytology,embryology Fluorescent Antibody Technique Membrane Glycoproteins Membrane Proteins/analysis Microfilament Proteins/analysis Microvilli/metabolism,ultrastructure Morphogenesis
Chemicals
Calmodulin Carrier Proteins Cytoskeletal Proteins Membrane Glycoproteins Membrane Proteins Microfilament Proteins plastin villin Ca(2+) Mg(2+)-ATPase
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Shibayama T
Carboni J M
Mooseker M S
References (28)
28 references, click to expand
  1. Spectrin, fodrin, and TW260/240: a family of related proteins lining the plasma membrane.
    Cell Motil. 1983;3(5-6):671-82 PMID: 6661770
  2. Characterization of the 110-kdalton actin-calmodulin-, and membrane-binding protein from microvilli of intestinal epithelial cells.
    J Cell Biol. 1983 Oct;97(4):974-85 PMID: 6311843
  3. Studies on the spectrin-like protein from the intestinal brush border, TW 260/240, and characterization of its interaction with the cytoskeleton and actin.
    J Cell Biol. 1984 Jan;98(1):66-78 PMID: 6538573
  4. The microvillus 110K cytoskeletal protein is an integral membrane protein.
    Cell. 1984 Jul;37(3):743-51 PMID: 6744412
  5. The 110,000-dalton actin- and calmodulin-binding protein from intestinal brush border is a myosin-like ATPase.
    J Biol Chem. 1984 Nov 25;259(22):14128-35 PMID: 6094541
  6. Ligand-induced changes in the location of actin, myosin, 95K (alpha-actinin), and 120K protein in amebae of Dictyostelium discoideum.
    J Cell Biol. 1985 Jun;100(6):1884-93 PMID: 3889011
  7. Effects of actin filament cross-linking and filament length on actin-myosin interaction.
    J Cell Biol. 1985 Nov;101(5 Pt 1):1850-7 PMID: 2932451
  8. Regulation of intestinal brush border microvillus length during development by the G- to F-actin ratio.
    Dev Biol. 1986 Apr;114(2):381-8 PMID: 3956872
  9. Calcium and the regulation of cytoskeletal assembly, structure and contractility.
    Ciba Found Symp. 1986;122:232-49 PMID: 3792141
  10. Organization, chemistry, and assembly of the cytoskeletal apparatus of the intestinal brush border.
    Annu Rev Cell Biol. 1985;1:209-41 PMID: 3916317
  11. The 110-kD protein-calmodulin complex of the intestinal microvillus is an actin-activated MgATPase.
    J Cell Biol. 1987 Jul;105(1):313-24 PMID: 2956266
  12. FINE STRUCTURE OF CELL SURFACE SPECIALIZATIONS IN THE MATURING DUODENAL MUCOSA OF THE CHICK.
    J Cell Biol. 1964 Apr;21:75-85 PMID: 14154497
  13. Characterization of an integral membrane glycoprotein associated with the microfilaments of pig intestinal microvilli.
    EMBO J. 1983;2(3):469-75 PMID: 11894965
  14. Morphogenesis of intestinal villi. I. Scanning electron microscopy of the duodenal epithelium of the developing chick embryo.
    J Morphol. 1972 Jun;137(2):193-213 PMID: 4555575
  15. Morphogenesis of intestinal villi. II. Mechanism of formation of previllous ridges.
    J Embryol Exp Morphol. 1975 Dec;34(3):723-40 PMID: 1214115
  16. Fluorescent antibody localization of myosin in the cytoplasm, cleavage furrow, and mitotic spindle of human cells.
    J Cell Biol. 1976 Dec;71(3):848-75 PMID: 62755
  17. A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples.
    Anal Biochem. 1978 Jun 15;87(1):206-10 PMID: 98070
  18. SDS microslab linear gradient polyacrylamide gel electrophoresis.
    Anal Biochem. 1978 Jul 1;87(2):386-96 PMID: 686359
  19. Development of the structural components of the brush border in absorptive cells of the chick intestine.
    Cell Tissue Res. 1979;204(3):387-405 PMID: 118806
  20. Brush-border alpha-actinin? Comparison of two proteins of the microvillus core with alpha-actinin by two-dimensional peptide mapping.
    J Cell Biol. 1980 Aug;86(2):466-74 PMID: 7400215
  21. Fimbrin, a new microfilament-associated protein present in microvilli and other cell surface structures.
    J Cell Biol. 1980 Jul;86(1):335-40 PMID: 6998986
  22. Calcium control of the intestinal microvillus cytoskeleton: its implications for the regulation of microfilament organizations.
    Proc Natl Acad Sci U S A. 1980 Nov;77(11):6458-62 PMID: 6935660
  23. Regulation of microvillus structure: calcium-dependent solation and cross-linking of actin filaments in the microvilli of intestinal epithelial cells.
    J Cell Biol. 1980 Dec;87(3 Pt 1):809-22 PMID: 6893989
  24. F-actin binding and bundling properties of fimbrin, a major cytoskeletal protein of microvillus core filaments.
    J Biol Chem. 1981 Sep 10;256(17):9283-8 PMID: 6894925
  25. Ca++-calmodulin-dependent phosphorylation of myosin, and its role in brush border contraction in vitro.
    J Cell Biol. 1982 Dec;95(3):943-59 PMID: 6897550
  26. Role of fimbrin and villin in determining the interfilament distances of actin bundles.
    Nature. 1983 Jan 20;301(5897):209-14 PMID: 6823301
  27. Fodrin is the general spectrin-like protein found in most cells whereas spectrin and the TW protein have a restricted distribution.
    Cell. 1983 Sep;34(2):503-12 PMID: 6352052
  28. Development of nutrient transport systems in chick jejunum.
    Am J Physiol. 1984 Feb;246(2 Pt 1):G101-7 PMID: 6141739
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1987-07-00
Pages
335-44
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2114914
Subset
IM
Grants
NIADDK NIH HHS · AM 25387 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]