Skip to main content
Advertisement

Main menu

  • Home
  • Articles
    • Accepted manuscripts
    • Issue in progress
    • Latest complete issue
    • Issue archive
    • Archive by article type
    • Special issues
    • Subject collections
    • Sign up for alerts
  • About us
    • About Development
    • About the Node
    • Editors and Board
    • Editor biographies
    • Travelling Fellowships
    • Grants and funding
    • Journal Meetings
    • Workshops
    • The Company of Biologists
    • Journal news
  • For authors
    • Submit a manuscript
    • Aims and scope
    • Presubmission enquiries
    • Article types
    • Manuscript preparation
    • Cover suggestions
    • Editorial process
    • Promoting your paper
    • Open Access
    • Biology Open transfer
  • Journal info
    • Journal policies
    • Rights and permissions
    • Media policies
    • Reviewer guide
    • Sign up for alerts
  • Contacts
    • Contacts
    • Subscriptions
    • Feedback
  • COB
    • About The Company of Biologists
    • Development
    • Journal of Cell Science
    • Journal of Experimental Biology
    • Disease Models & Mechanisms
    • Biology Open

User menu

  • Log in
  • Log out

Search

  • Advanced search
Development
  • COB
    • About The Company of Biologists
    • Development
    • Journal of Cell Science
    • Journal of Experimental Biology
    • Disease Models & Mechanisms
    • Biology Open

supporting biologistsinspiring biology

Development

  • Log in
Advanced search

RSS  Twitter  Facebook  YouTube 

  • Home
  • Articles
    • Accepted manuscripts
    • Issue in progress
    • Latest complete issue
    • Issue archive
    • Archive by article type
    • Special issues
    • Subject collections
    • Sign up for alerts
  • About us
    • About Development
    • About the Node
    • Editors and Board
    • Editor biographies
    • Travelling Fellowships
    • Grants and funding
    • Journal Meetings
    • Workshops
    • The Company of Biologists
    • Journal news
  • For authors
    • Submit a manuscript
    • Aims and scope
    • Presubmission enquiries
    • Article types
    • Manuscript preparation
    • Cover suggestions
    • Editorial process
    • Promoting your paper
    • Open Access
    • Biology Open transfer
  • Journal info
    • Journal policies
    • Rights and permissions
    • Media policies
    • Reviewer guide
    • Sign up for alerts
  • Contacts
    • Contacts
    • Subscriptions
    • Feedback
JOURNAL ARTICLES
The C. elegans par-4 gene encodes a putative serine-threonine kinase required for establishing embryonic asymmetry
J.L. Watts, D.G. Morton, J. Bestman, K.J. Kemphues
Development 2000 127: 1467-1475;
J.L. Watts
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
D.G. Morton
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
J. Bestman
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
K.J. Kemphues
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • Article
  • Info & metrics
  • PDF
Loading

Summary

During the first cell cycle of Caenorhabditis elegans embryogenesis, asymmetries are established that are essential for determining the subsequent developmental fates of the daughter cells. The maternally expressed par genes are required for establishing this polarity. The products of several of the par genes have been found to be themselves asymmetrically distributed in the first cell cycle. We have identified the par-4 gene of C. elegans, and find that it encodes a putative serine-threonine kinase with similarity to a human kinase associated with Peutz-Jeghers Syndrome, LKB1 (STK11), and a Xenopus egg and embryo kinase, XEEK1. Several strong par-4 mutant alleles are missense mutations that alter conserved residues within the kinase domain, suggesting that kinase activity is essential for PAR-4 function. We find that the PAR-4 protein is present in the gonads, oocytes and early embryos of C. elegans, and is both cytoplasmically and cortically distributed. The cortical distribution begins at the late 1-cell stage, is more pronounced at the 2- and 4-cell stages and is reduced at late stages of embryonic development. We find no asymmetry in the distribution of PAR-4 protein in C. elegans embryos. The distribution of PAR-4 protein in early embryos is unaffected by mutations in the other par genes.

REFERENCES

    1. Altschul S. F.,
    2. Gish W.,
    3. Miller W.,
    4. Myers E. W.,
    5. Lipman D. J.
    (1990) Basic local alignment search tool. J. Mol. Biol 215, 403–410
    OpenUrlCrossRefPubMedWeb of Science
    1. Bowerman B.
    (1998) Maternal control of pattern formation in early Caenorhabditis elegan s embryos. Curr. Top. Dev. Biol 39, 73–117
    OpenUrlCrossRefPubMedWeb of Science
    1. Bowerman B.,
    2. Draper B. W.,
    3. Mello C. C.,
    4. Priess J. R.
    (1993) The maternal gene skn-1 encodes a protein that is distributed unequally in early C. elegans embryos. Cell 74, 443–452
    OpenUrlCrossRefPubMedWeb of Science
    1. Bowerman B.,
    2. Ingram M. K.,
    3. Hunter C. P.
    (1997) The maternal par genes and the segregation of cell fate specification activities in early Caenorhabditis elegans embryos. Development 124, 3815–3826
    OpenUrlAbstract
    1. Boyd L.,
    2. Guo S.,
    3. Levitan D.,
    4. Stinchcomb D. T.,
    5. Kemphues K. J.
    (1996) PAR-2 is asymmetrically distributed and promotes association of P granules and PAR-1 with the cortex in C. elegans embryos. Development 122, 3075–3084
    OpenUrlAbstract
    1. Brenner S.
    (1974) The genetics of Caenorhabditis elegans. Genetics 77, 71–94
    OpenUrlAbstract/FREE Full Text
    1. Cheng N. N.,
    2. Kirby C. M.,
    3. Kemphues K. J.
    (1995) Control of cleavage spindle orientation in Caenorhabditis elegans: the role of the genes par-2 and par-3. Genetics 139, 549–559
    OpenUrlAbstract/FREE Full Text
    1. Collins J.,
    2. Saari B.,
    3. Anderson P.
    (1987) Activation of a transposable element in the germ line but not the soma of Caenorhabditis elegans. Nature 328, 726–728
    OpenUrlCrossRefPubMed
  1. Consortium (1998) Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 282, 2012–2018The, C. elegans, Sequencing
    OpenUrlAbstract/FREE Full Text
    1. Crittenden S. L.,
    2. Rudel D.,
    3. Binder J.,
    4. Evans T. C.,
    5. Kimble J.
    (1997) Genes required for GLP-1 asymmetry in the early Caenorhabditis elegans embryo. Dev. Biol 181, 36–46
    OpenUrlCrossRefPubMedWeb of Science
    1. Draper B. W.,
    2. Mello C. C.,
    3. Bowerman B.,
    4. Hardin J.,
    5. Priess J. R.
    (1996) MEX-3 is a KH domain protein that regulates blastomere identity in early C. elegans embryos. Cell 87, 205–216
    OpenUrlCrossRefPubMedWeb of Science
    1. Etemad-Moghadam B.,
    2. Guo S.,
    3. Kemphues K. J.
    (1995) Asymmetrically distributed PAR-3 protein contributes to cell polarity and spindle alignment in early C. elegans embryos. Cell 83, 743–752
    OpenUrlCrossRefPubMedWeb of Science
    1. Evans T. C.,
    2. Crittenden S. L.,
    3. Kodoyianni V.,
    4. Kimble J.
    (1994) Translational control of maternal glp-1 mRNA establishes an asymmetry in the C. elegans embryo. Cell 77, 183–194
    OpenUrlCrossRefPubMedWeb of Science
    1. Fire A.,
    2. Xu S.,
    3. Montgomery M. K.,
    4. Kostas S. A.,
    5. Driver S. E.,
    6. Mello C. C.
    (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391, 806–811
    OpenUrlCrossRefPubMedWeb of Science
    1. Goldstein B.,
    2. Hird S. N.
    (1996) Specification of the anteroposterior axis in Caenorhabditis elegans. Development 122, 1467–1474
    OpenUrlAbstract
    1. Guo S.,
    2. Kemphues K. J.
    (1995) par-1, a gene required for establishing polarity in C. elegans embryos, encodes a putative Ser/Thr kinase that is asymmetrically distributed. Cell 81, 611–620
    OpenUrlCrossRefPubMedWeb of Science
    1. Guo S.,
    2. Kemphues K. J.
    (1996) A non-muscle myosin required for embryonic polarity in Caenorhabditis elegans. Nature 382, 455–458
    OpenUrlCrossRefPubMed
    1. Hanks S. K.,
    2. Hunter T.
    (1995) Protein kinases 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification. FASEB J 9, 576–596
    OpenUrlAbstract
    1. Hanks S. K.,
    2. Quinn A. M.,
    3. Hunter T.
    (1988) The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241, 42–52
    OpenUrlAbstract/FREE Full Text
    1. Hemminki A.,
    2. Markie D.,
    3. Tomlinson I.,
    4. Avizienyte E.,
    5. Roth S.,
    6. Loukola A.,
    7. Bignell G.,
    8. Warren W.,
    9. Aminoff M.,
    10. Hoglund P.,
    11. et al.
    (1998) A serine/threonine kinase gene defective in Peutz-Jeghers syndrome. Nature 391, 184–187
    OpenUrlCrossRefPubMedWeb of Science
    1. Higgins D. G.,
    2. Bleasby A. J.,
    3. Fuchs R.
    (1992) CLUSTAL V: improved software for multiple sequence alignment. Comput. Appl. Biosci 8, 189–191
    OpenUrlAbstract/FREE Full Text
    1. Hird S. N.,
    2. Paulsen J. E.,
    3. Strome S.
    (1996) Segregation of germ granules in living Caenorhabditis elegans embryos: cell-type-specific mechanisms for cytoplasmic localisation. Development 122, 1303–1312
    OpenUrlAbstract
    1. Hung T. J.,
    2. Kemphues K. J.
    (1999) PAR-6 is a conserved PDZ domain-containing protein that colocalizes with PAR-3 in Caenorhabditis elegans embryos. Development 126, 127–135
    OpenUrlAbstract
    1. Hunter C. P.,
    2. Kenyon C.
    (1996) Spatial and temporal controls target pal-1 blastomere-specification activity to a single blastomere lineage in C. elegans embryos. Cell 87, 217–226
    OpenUrlCrossRefPubMedWeb of Science
    1. Jenne D. E.,
    2. Reimann H.,
    3. Nezu J.,
    4. Friedel W.,
    5. Loff S.,
    6. Jeschke R.,
    7. Muller O.,
    8. Back W.,
    9. Zimmer M.
    (1998) Peutz-Jeghers syndrome is caused by mutations in a novel serine threonine kinase. Nat. Genet 18, 38–43
    OpenUrlCrossRefPubMedWeb of Science
    1. Kemphues K. J.,
    2. Priess J. R.,
    3. Morton D. G.,
    4. Cheng N. S.
    (1988) Identification of genes required for cytoplasmic localization in early C. elegans embryos. Cell 52, 311–320
    OpenUrlCrossRefPubMedWeb of Science
    1. Kirby C.,
    2. Kusch M.,
    3. Kemphues K.
    (1990) Mutations in the par genes of Caenorhabditis elegans affect cytoplasmic reorganization during the first cell cycle. Dev. Biol 142, 203–215
    OpenUrlCrossRefPubMed
    1. Knighton D. R.,
    2. Zheng J. H.,
    3. Ten,
    4. Eyck L. F.,
    5. Ashford V. A.,
    6. Xuong N. H.,
    7. Taylor S. S.,
    8. Sowadski J. M.
    (1991) Crystal structure of the catalytic subunit of cyclic adenosine monophosphate-dependent protein kinase [see comments]. Science 253, 407–414
    OpenUrlAbstract/FREE Full Text
    1. Kuwabara P. E.,
    2. Shah S.
    (1994). Cloning by synteny: identifying C.briggsae homologues of C. elegans genes. Nucleic Acids Res 22, 4414–4418
    OpenUrlAbstract/FREE Full Text
    1. Lee R. C.,
    2. Feinbaum R. L.,
    3. Ambros V.
    (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75, 843–854
    OpenUrlCrossRefPubMedWeb of Science
    1. Levitan D. J.,
    2. Boyd L.,
    3. Mello C. C.,
    4. Kemphues K. J.,
    5. Stinchcomb D. T.
    (1994) par-2, a gene required for blastomere asymmetry in Caenorhabditis elegans, encodes zinc-finger and ATP-binding motifs. Proc. Natl. Acad. Sci. USA 91, 6108–6112
    OpenUrlAbstract/FREE Full Text
    1. Luukko K.,
    2. Ylikorkala A.,
    3. Tiainen M.,
    4. Makela T. P.
    (1999) Expression of LKB1 and PTEN tumor suppressor genes during mouse embryonic development. Mech. Dev 83, 187–190
    OpenUrlCrossRefPubMedWeb of Science
    1. Mehenni H.,
    2. Gehrig C.,
    3. Nezu J.,
    4. Oku A.,
    5. Shimane M.,
    6. Rossier C.,
    7. Guex N.,
    8. Blouin J. L.,
    9. Scott H. S.,
    10. Antonarakis S. E.
    (1998) Loss of LKB1 kinase activity in Peutz-Jeghers syndrome, and evidence for allelic and locus heterogeneity. Am. J. Hum. Genet 63, 1641–1650
    OpenUrlCrossRefPubMedWeb of Science
    1. Mello C. C.,
    2. Draper B. W.,
    3. Priess J. R.
    (1994) The maternal genes apx-1 and glp-1 and establishment of dorsal-ventral polarity in the early C. elegans embryo. Cell 77, 95–106
    OpenUrlCrossRefPubMedWeb of Science
    1. Mello C. C.,
    2. Schubert C.,
    3. Draper B.,
    4. Zhang W.,
    5. Lobel R.,
    6. Priess J. R.
    (1996) The PIE-1 protein and germline specification in C. elegans embryos. Nature 382, 710–712
    OpenUrlCrossRefPubMed
    1. Morton D. G.,
    2. Roos J. M.,
    3. Kemphues K. J.
    (1992) par-4, a gene required for cytoplasmic localization and determination of specific cell types in Caenorhabditis elegans embryogenesis. Genetics 130, 771–790
    OpenUrlAbstract/FREE Full Text
    1. Nezu J.,
    2. Oku A.,
    3. Shimane M.
    (1999) Loss of cytoplasmic retention ability of mutant LKB1 found in Peutz-Jeghers syndrome patients. Biochem. Biophys. Res. Commun 261, 750–755
    OpenUrlCrossRefPubMedWeb of Science
    1. Olmsted J. B.
    (1986) Analysis of cytoskeletal structures using blot-purified monospecific antibodies. Methods Enzymol 134, 467–472
    OpenUrlCrossRefPubMedWeb of Science
    1. Rose L. S.,
    2. Kemphues K. J.
    (1998) Early patterning of the C. elegans embryo. Annu. Rev. Genet 32, 521–545
    OpenUrlCrossRefPubMedWeb of Science
    1. Ross L. H.,
    2. Freedman J. H.,
    3. Rubin C. S.
    (1995) Structure and expression of novel spliced leader RNA genes in Caenorhabditis elegans. J. Biol. Chem 270, 22066–22075
    OpenUrlAbstract/FREE Full Text
    1. Smith D. B.,
    2. Johnson K. S.
    (1988) Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene 67, 31–40
    OpenUrlCrossRefPubMedWeb of Science
    1. Smith D. P.,
    2. Spicer J.,
    3. Smith A.,
    4. Swift S.,
    5. Ashworth A.
    (1999) The mouse Peutz-Jeghers syndrome gene Lkb1 encodes a nuclear protein kinase. Hum. Mol. Genet 8, 1479–1485
    OpenUrlAbstract/FREE Full Text
    1. Spieth J.,
    2. Brooke G.,
    3. Kuersten S.,
    4. Lea K.,
    5. Blumenthal T.
    (1993) Operons in C. elegans: polycistronic mRNA precursors are processed by trans-splicing of SL2 to downstream coding regions. Cell 73, 521–532
    OpenUrlCrossRefPubMedWeb of Science
    1. Strome S.
    (1986) Fluorescence visualization of the distribution of microfilaments in gonads and early embryos of the nematode Caenorhabditis elegans. J. Cell. Biol 103, 2241–2252
    OpenUrlAbstract/FREE Full Text
    1. Strome S.,
    2. Wood W. B.
    (1982) Immunofluorescence visualization of germ-line-specific cytoplasmic granules in embryos, larvae, and adults of Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 79, 1558–1562
    OpenUrlAbstract/FREE Full Text
    1. Strome S.,
    2. Wood W. B.
    (1983) Generation of asymmetry and segregation of germ-line granules in early C. elegans embryos. Cell 35, 15–25
    OpenUrlCrossRefPubMedWeb of Science
    1. Su J. Y.,
    2. Erikson E.,
    3. Maller J. L.
    (1996) Cloning and characterization of a novel serine/threonine protein kinase expressed in early Xenopus embryos. J. Biol. Chem 271, 14430–14437
    OpenUrlAbstract/FREE Full Text
    1. Sulston J. E.,
    2. Schierenberg E.,
    3. White J. G.,
    4. Thomson J. N.
    (1983) The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev. Biol 100, 64–119
    OpenUrlCrossRefPubMedWeb of Science
    1. Tabuse Y.,
    2. Izumi Y.,
    3. Piano F.,
    4. Kemphues K. J.,
    5. Miwa J.,
    6. Ohno S.
    (1998) Atypical protein kinase C cooperates with PAR-3 to establish embryonic polarity in Caenorhabditis elegans. Development 125, 3607–3614
    OpenUrlAbstract
    1. Watts J. L.,
    2. Etemad-Moghadam B.,
    3. Guo S.,
    4. Boyd L.,
    5. Draper B. W.,
    6. Mello C. C.,
    7. Priess J. R.,
    8. Kemphues K. J.
    (1996) par-6, a gene involved in the establishment of asymmetry in early C. elegans embryos, mediates the asymmetric localization of PAR-3. Development 122, 3133–3140
    OpenUrlAbstract
Previous ArticleNext Article
Back to top
Previous ArticleNext Article

This Issue

 Download PDF

Email

Thank you for your interest in spreading the word on Development.

NOTE: We only request your email address so that the person you are recommending the page to knows that you wanted them to see it, and that it is not junk mail. We do not capture any email address.

Enter multiple addresses on separate lines or separate them with commas.
The C. elegans par-4 gene encodes a putative serine-threonine kinase required for establishing embryonic asymmetry
(Your Name) has sent you a message from Development
(Your Name) thought you would like to see the Development web site.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Share
JOURNAL ARTICLES
The C. elegans par-4 gene encodes a putative serine-threonine kinase required for establishing embryonic asymmetry
J.L. Watts, D.G. Morton, J. Bestman, K.J. Kemphues
Development 2000 127: 1467-1475;
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
JOURNAL ARTICLES
The C. elegans par-4 gene encodes a putative serine-threonine kinase required for establishing embryonic asymmetry
J.L. Watts, D.G. Morton, J. Bestman, K.J. Kemphues
Development 2000 127: 1467-1475;

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Alerts

Please log in to add an alert for this article.

Sign in to email alerts with your email address

Article navigation

  • Top
  • Article
  • Info & metrics
  • PDF

Related articles

Cited by...

More in this TOC section

  • Morphogenetic cell movements in the middle region of the dermomyotome dorsomedial lip associated with patterning and growth of the primary epaxial myotome
  • Germline and developmental roles of the nuclear transport factor importin (α)3 in C. elegans
  • Monofocal origin of telencephalic oligodendrocytes in the anterior entopeduncular area of the chick embryo
Show more JOURNAL ARTICLES

Similar articles

Other journals from The Company of Biologists

Journal of Cell Science

Journal of Experimental Biology

Disease Models & Mechanisms

Biology Open

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

Articles

  • Accepted manuscripts
  • Issue in progress
  • Latest complete issue
  • Issue archive
  • Archive by article type
  • Special issues
  • Subject collections
  • Sign up for alerts

About us

  • About Development
  • About the Node
  • Editors and board
  • Editor biographies
  • Travelling Fellowships
  • Grants and funding
  • Journal Meetings
  • Workshops
  • The Company of Biologists

For authors

  • Submit a manuscript
  • Aims and scope
  • Presubmission enquiries
  • Article types
  • Manuscript preparation
  • Cover suggestions
  • Editorial process
  • Promoting your paper
  • Open Access
  • Biology Open transfer

Journal info

  • Journal policies
  • Rights and permissions
  • Media policies
  • Reviewer guide
  • Sign up for alerts

Contact

  • Contact Development
  • Subscriptions
  • Advertising
  • Feedback

 Twitter   YouTube   LinkedIn

© 2021   The Company of Biologists Ltd   Registered Charity 277992