Advertisement
JOURNAL ARTICLES
Requirement of c-kit for development of intestinal pacemaker system
H. Maeda, A. Yamagata, S. Nishikawa, K. Yoshinaga, S. Kobayashi, K. Nishi, S. Nishikawa
Development 1992 116: 369-375;

Summary

A discovery that the protooncogene encoding the receptor tyrosine kinase, c-kit, is allelic with the Dominant white spotting (W) locus establishes that c-kit plays a functional role in the development of three cell lineages, melanocyte, germ cell, and hematopoietic cell which are defective in W mutant mice. Recent analyses of c-kit expression in various tissues of mouse, however, have demonstrated that c-kit is expressed in more diverse tissues which are phenotypically normal in W mutant mice. Thus, whether or not c-kit expressed outside the three known cell lineages plays a functional role is one of the important questions needing answering in order to fully elucidate the role of c-kit in the development of the mouse. Here, we report that some of the cells in smooth muscle layers of developing intestine express c-kit. Blockade of its function for a few days postnatally by an antagonistic anti-c-kit monoclonal antibody (mAb) results in a severe anomaly of gut movement, which in BALB/c mice produces a lethal paralytic ileus. Physiological analysis indicates that the mechanisms required for the autonomic pacing of contraction in an isolated gut segment are defective in the anti-c-kit mAb-treated mice, W/Wv mice and even W/+ mice. These findings suggest that c-kit plays a crucial role in the development of a component of the pacemaker system that is required for the generation of autonomic gut motility.

REFERENCES

    1. Chabot B.,
    2. Stephenson D. A.,
    3. Chapman V. M.,
    4. Besmer P.,
    5. Bernstein A.
    (1988) The proto-oncogene c- kit encoding a transmembrane tyrosine kinase receptor maps to the mouse W locus. Nature 335, 88–89
    OpenUrlCrossRefPubMed
    1. Copeland N. G.,
    2. Gilbert D. J.,
    3. Cho B. C.,
    4. Donovan P. J.,
    5. Jenkins N. A.,
    6. Cosman D.,
    7. Anderson D.,
    8. Lyman S. D.,
    9. Williams D. E.
    (1990) Mast cell growth factor maps near the Steel locus on mouse chromosome 10 and is deleted in a number of Steel alleles. Cell 63, 175–183
    OpenUrlCrossRefPubMedWeb of Science
    1. Faussone-Pellegrini M. S.
    (1984) Morphogenesis of the special circular muscle layer and the interstitial cells of Cajal related to the plexus muscularis profundus of mouse intestinal muscle coat. Anat. Embryol 169, 151–158
    OpenUrlCrossRefPubMed
    1. Geissler E. N.,
    2. McFarland E. C.,
    3. Russel E. S.
    (1981) Analysis of pleiotropism at the dominat white spotting (W) locus of the house mouse: A description of ten new W alleles. Genetics 97, 337–361
    OpenUrlAbstract/FREE Full Text
    1. Geissler E. N.,
    2. Ryan M. A.,
    3. Housman D. E.
    (1988) The dominant white spotting (W) locus of the mouse encodes the c- kit protooncogene. Cell 55, 185–192
    OpenUrlCrossRefPubMedWeb of Science
    1. Giebel L. B.,
    2. Spritz R. A.
    (1991) Mutation of the KIT (mast/stem cell growth factor receptor) protooncogene in human piebaldism. Proc.Natl.Acad.Sci. USA 88, 8696–8699
    OpenUrlAbstract/FREE Full Text
    1. Hayashi S. I.,
    2. Kunisada M.,
    3. Ogawa M.,
    4. Yamaguchi K.,
    5. Nishikawa S. I.
    (1991) Exon skipping by mutation of an authentic splice site of c- kit gene in W/W mouse. Nucleic Acids Res 19, 1267–1271
    OpenUrlAbstract/FREE Full Text
    1. Huang E.,
    2. Nocka K.,
    3. Beier D. R.,
    4. Chu T. Y.,
    5. Buck J.,
    6. Lahm H. W.,
    7. Wellner D.,
    8. Leder P.,
    9. Besmer P.
    (1990) The hematopoietic growth factor KL is encoded by the Sl locus and is the ligand of the c- kit receptor, the gene product of the W locus. Cell 63, 225–233
    OpenUrlCrossRefPubMedWeb of Science
    1. Keshet E.,
    2. Lyman S.D.,
    3. Williams D. E.,
    4. Anderson D. M.,
    5. Jenkins N. A.,
    6. Copeland N. G.,
    7. Parada L. F.
    (1991) Embryonic RNA expression patterns of the c- kit receptor and its cognate ligand suggest multiple functional roles in mouse development. EMBO J 10, 2425–2435
    OpenUrlPubMedWeb of Science
    1. Kobayashi S.
    (1990) The structure of the autonomic end apparatus in the guinea-pig small intestine and the problem of the interstitial cells of Cajal. Acta. Med. Biol 38, 103–127
    OpenUrl
    1. Lane P. W.
    (1966) Association of megacolon with two recessive spotting genes in the mouse. J. Hered 57, 29–31
    OpenUrlFREE Full Text
    1. Lane P. W.,
    2. Liu H. M.
    (1984) Association of megacolon with a new dominant spotting gene (Dom) in the mouse. J. Hered 75, 435–439
    OpenUrlAbstract/FREE Full Text
    1. Langton P. D.,
    2. Ward S. M.,
    3. Carl A.,
    4. Norell M.,
    5. Sanders K. M.
    (1990) Spontaneous electrical activity of interstitial cell of Cajal isolated from canine proximal colon. Proc.Natl.Acad.Sci. USA 86, 103–127
    OpenUrl
    1. Maillet M.
    (1963) Le reactif au tetraoxyde de osmiumiodure du zinc. Z. Mikrosk. Anat. Forsch 70, 397–425
    OpenUrlPubMed
    1. Manova K.,
    2. Nocka K.,
    3. Besmer P.,
    4. Bachvarova R. F.
    (1990) Gonadal expression of c- kit encoded at the W locus of the mouse. Development 110, 1057–1069
    OpenUrlAbstract/FREE Full Text
    1. Matsui Y.,
    2. Zsebo M.,
    3. Hogan B. L. M.
    (1990) Embryonic expression of a haematopoietic growth factor encoded by Sl locus and the ligand for c- kit. Nature 347, 667–669
    OpenUrlCrossRefPubMed
    1. Motro B.,
    2. Van Der Kooy D.,
    3. Rossant J.,
    4. Reith A.,
    5. Bernstein A.
    (1991) Contiguous patterns of c- kit and steel expression: analysis of mutation at the W and Sl loci. Development 113, 1207–1221
    OpenUrlAbstract
    1. Nishikawa S.,
    2. Kusakabe M.,
    3. Yoshinaga K.,
    4. Ogawa M.,
    5. Hayashi S. I.,
    6. Kunisada T.,
    7. Era T.,
    8. Sakakura T.,
    9. Nishikawa S. I.
    (1991) In utero manipulation of coat color formation by a monoclonal anti-c- kit antibody: two distinct waves of c- kit- dependency during melanocyte development. EMBO J 10, 2111–2118
    OpenUrlPubMedWeb of Science
    1. Nocka K.,
    2. Tan J. C.,
    3. Chiu E.,
    4. Chu T. Y.,
    5. Ray P.,
    6. Trakman P.,
    7. Besmer P.
    (1990). Molecular bases of dominant negative and loss of function mutation at the murine c- kit/white spotting locus: W37, Wv, W41 and W. EMBO J 9, 1805–1813
    OpenUrlPubMedWeb of Science
    1. Ogawa M.,
    2. Mtsuzaki Y.,
    3. Nishikawa S.,
    4. Hayashi S. I.,
    5. Kunisada T.,
    6. Sudo T.,
    7. Kina T.,
    8. Nakauchi H.,
    9. Nishikawa S. I.
    (1991) Expression and function of c- kit in hemopoietic progenitor cells. J.Exp.Med 174, 63–71
    OpenUrlAbstract/FREE Full Text
    1. Orr-Urtreger A.,
    2. Avivi A.,
    3. Zimmer Y.,
    4. Givol D.,
    5. Yarden Y.,
    6. Lonai P.
    (1990) Developmental expression of c- kit, a proto-oncogene encoded by the W locus. Development 109, 911–923
    OpenUrlAbstract/FREE Full Text
    1. Papayannopoulou T.,
    2. Brice M.,
    3. Broudy V. C.,
    4. Zsebo K. M.
    (1991) Isolation of c- kit receptor expressing cells from bone marrow, peripheral blood, and fetal liver: Functional properties and composite antigenic profile. Blood 78, 1403–1412
    OpenUrlAbstract/FREE Full Text
    1. Qui F.,
    2. Ray P.,
    3. Brown K.,
    4. Barker P. E.,
    5. Jhanwar S.,
    6. Riddle F. H.,
    7. Besmer P.
    (1988) Primary structure of c- kit: relationship with the CSF-1/PDGF receptor kinase family-oncogenic activation of v- kit involves deletion of extracellular domain and C-terminus. EMBO J 7, 1003–1011
    OpenUrlPubMedWeb of Science
    1. Reith A. D.,
    2. Rottapel R.,
    3. Giddens E.,
    4. Brady C.,
    5. Forrester L.,
    6. Bernstein A.
    (1990) W mutant mice with mild or severe developmental defects contain distinct point mutations in the kinase domain of the c- kit transmembrane receptor. Genes Dev 4, 390–400
    OpenUrlAbstract/FREE Full Text
    1. Russell E. S.
    (1979) Hereditary anemias of the mouse: a review for geneticists. Adv. Genetics 20, 357–459
    OpenUrlPubMed
    1. Shimada M.,
    2. Kitamura Y.,
    3. Yokoyama M.,
    4. Miyano Y.,
    5. Maeyama K.,
    6. Yamamotodai A.,
    7. Takahashi Y.,
    8. Tatsuta M.
    (1980) Spontaneous stomach ulcer in genetically mast-cell depleted W/Wv mice. Nature 283, 662–664
    OpenUrlCrossRefPubMed
    1. Springer T.,
    2. Galfre G.,
    3. Secher D. S.,
    4. Milstein C.
    (1979) Mac-1: a macrophage differentiation antigen indentified by monoclonal antibody. Eur.J.Immunol 9, 301–306
    OpenUrlPubMedWeb of Science
    1. Tan J. C.,
    2. Nocka K.,
    3. Ray P.,
    4. Traktman P.,
    5. Besmer P.
    (1990). The dominant W42 spotting phenotype results from a missense mutation in the c- kit kinase receptor.. Science 247, 209–212
    OpenUrlAbstract/FREE Full Text
    1. Thuneberg L.
    (1982) Interstitial cells of Cajal: intestinal pacemaker cells?. Adv. Anat. Embryol. Cell. Biol 71, 1–130
    OpenUrlPubMed
    1. Yarden Y.,
    2. Kuang W.J.,
    3. Yang-Feng T.,
    4. Coussens L.,
    5. Munemitsu S.,
    6. Dull T.J.,
    7. Chen E.,
    8. Schlessinger J.,
    9. Francke U.,
    10. Ullrich A.
    (1987) Human proto-oncogene c- kit: a new cell surface receptor tyrosine kinase for an unidentified ligand. EMBO J 6, 3341–3351
    OpenUrlPubMedWeb of Science
    1. Yokoyama M.,
    2. Kitamura Y.,
    3. Kohrogi T.,
    4. Miyoshi I.
    (1982) Necessity of bile for and lack of inhibitory effect of retinoid on development of forestomach papillomas in nontreated mutant mice of the W/Wv genotype. Cancer Res 42, 3806–3809
    OpenUrlAbstract/FREE Full Text
    1. Yoshinaga K.,
    2. Nishikawa S.,
    3. Ogawa M.,
    4. Hayashi S. I.,
    5. Kunisada T.,
    6. Fujimoto T.,
    7. Nishikawa S. I.
    (1991) Role of c- kit in mouse spermatogenesis: identification of spermatogonia as a specific site of c- kit expression and function. Development 113, 689–699
    OpenUrlAbstract
    1. Voller E.,
    2. Roessner A.,
    3. Lipecki K.H.,
    4. Zwadlo G.,
    5. Hagemeier H.H.,
    6. Grundmann E.
    (1987) Biologic characterization of human bone tumors. Virchow Arch. B 53, 58–65
    OpenUrlPubMed
    1. Zsebo K. M.,
    2. Williams D. A.,
    3. Geissler E. N.,
    4. Broudy V. C.,
    5. Martin F. H.,
    6. Atkins H. L.,
    7. Hsu R. Y.,
    8. Birkett N. C.,
    9. Okino K. H.,
    10. Murdock D. C.,
    11. Jacobsen F. W.,
    12. Langley K. E.,
    13. Smith K. A.,
    14. Takeishi T.,
    15. Cattanach B. M.,
    16. Galli S. J.,
    17. Suggs S. V.
    (1990) Stem cell factor is encoded at the Sl locus of the mouse and is the ligand for the c- kit tyrosine kinase receptor. Cell 63, 213–224
    OpenUrlCrossRefPubMedWeb of Science
Back to top

 Download PDF

Email
JOURNAL ARTICLES
Requirement of c-kit for development of intestinal pacemaker system
H. Maeda, A. Yamagata, S. Nishikawa, K. Yoshinaga, S. Kobayashi, K. Nishi, S. Nishikawa
Development 1992 116: 369-375;
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
Alerts

Article navigation

Other journals from The Company of Biologists

Advertisement

Kathryn Virginia Anderson (1952-2020)

Developmental geneticist Kathryn Anderson passed away at home on 30 November 2020. Tamara Caspary, a former postdoc and friend, remembers Kathryn and her remarkable contribution to developmental biology.

Zooming into 2021

In a new Editorial, Editor-in-Chief James Briscoe and Executive Editor Katherine Brown reflect on the triumphs and tribulations of the last 12 months, and look towards a hopefully calmer and more predictable year.

Read & Publish participation extends worldwide

Over 60 institutions in 12 countries are now participating in our Read & Publish initiative. Here, James Briscoe explains what this means for his institution, The Francis Crick Institute. Find out more and view our full list of participating institutions.

Upcoming special issues

Imaging Development, Stem Cells and Regeneration
Submission deadline: 30 March 2021
Publication: mid-2021

The Immune System in Development and Regeneration
Guest editors: Florent Ginhoux and Paul Martin
Submission deadline: 1 September 2021
Publication: Spring 2022

Both special issues welcome Review articles as well as Research articles, and will be widely promoted online and at key global conferences.

Development presents...

Our successful webinar series continues into 2021, with early-career researchers presenting their papers and a chance to virtually network with the developmental biology community afterwards. Sign up to join our next session:

10 February
Time: 13:00 (GMT)
Chaired by: preLights