Source: CORNELL UNIVERSITY submitted to
ASYMMETRIC CELL DIVISION IN C. ELEGANS EMBRYOS
Sponsoring Institution
State Agricultural Experiment Station
Project Status
TERMINATED
Funding Source
STATE
Reporting Frequency
Annual
Accession No.
0177885
Grant No.
(N/A)
Project No.
NYC-165302
Proposal No.
(N/A)
Multistate No.
(N/A)
Program Code
(N/A)
Project Start Date
Apr 1, 1998
Project End Date
Sep 30, 2009
Grant Year
(N/A)
Project Director
Kemphues, K. J.
Recipient Organization
CORNELL UNIVERSITY
(N/A)
ITHACA,NY 14853
Performing Department
MOLECULAR BIOLOGY AND GENETICS
Non Technical Summary
(N/A)
Animal Health Component
(N/A)
Research Effort Categories
Basic
100%
Applied
(N/A)
Developmental
(N/A)
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
30431991080100%
Knowledge Area
304 - Animal Genome;

Subject Of Investigation
3199 - Invertebrates, general/other;

Field Of Science
1080 - Genetics;
Goals / Objectives
Asymmetric cell division, in which the two daughter cells adopt different fates, plays a key role in embryonic development and in tissue regeneration in adult life. This goal of this project is to obtain detailed molecular information about intrinsically asymmetric cell divisions using the nematode C. elegans as a model system. The research addresses two general questions: How are the intracellular asymmetries established. 2) How are mitotic spindles aligned along the axis of asymmetry. The research focuses on the six par genes, which are required for a series of reproducible asymmetric divisions in the lineage leading to the C. elegans germ line. Mutations in these genes disrupt both polarized distributions of cellular components and proper alignment of mitotic spindles in the early embryo. The proposed experiments address three broad and overlapping questions: How do the PAR proteins contribute to intracellular asymmetry. How are the PAR proteins localized. With what other cellular components do the PAR proteins interact to control asymmetric cell divisions. The recent discovery of yeast and human homologues of par-1 suggests conservation of mechanisms to establish intracellular asymmetries. Because of this we expect our analysis to provide basic information that will be applicable to studies of human growth and development.
Project Methods
Molecular cloning of par-4, par-5 and par-6 and the determination of the distribution of their protein products in the early embryo. For cloning, we will use a variety of techniques including transposon tagging, germline transformation rescue, and production of antisense RNA phenocopies. Protein distributions will be determined by immunofluorescence microscopy using antibodies raised against fusion proteins made in bacteria. Determination of the functional relationships among the par genes. We will compare PAR protein distributions by double label immunofluroescence microscopy in wild type and par mutant embryos. Investigations of the mechanisms of PAR protein localization and action. We will assay the distribution par mRNAs, ectopically expressed PAR proteins, and tagged PAR protein fragments to test hypotheses about localization. Identification of proteins that interact with the PAR proteins. This will be achieved by a combination of genetic screens for enhancers and suppressors of par mutations and "interaction cloning" using filter binding assays and the yeast two-hybrid system.

Progress 10/01/08 to 09/30/09

Outputs
OUTPUTS: This year, I presented a seminar at Syracuse University to the Cell Biology Department entitled "Establishing embryonic polarity in C. elegans", and two of my graduate students presented posters at the international C. elegans meeting in L.A. California and also presented talks at the New York C. elegans meeting. PARTICIPANTS: Not relevant to this project. TARGET AUDIENCES: Our work is basic biomedically related research. As such our target audience is the entire human race. PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.

Impacts
Our research has led to changes in knowledge about cell polarity. In particular we have identified and studied new genes with roles in establishing or maintaining cell polarity. Work in the lab focuses on a group of proteins called PAR proteins. This reporting period we made progress in three areas: 1) We completed our analysis of the PAR-3 and PAR-6 proteins, identifying which parts of the proteins are essential for function and learning that the requirements differ in different tissues and among different animals (e.g. fruit fly and mammals) 2) We have identified a new ubiquitin hydrolase,USP-47, that functions redundantly with MATH-33, a ubiquitin hydrolase that we had discovered earlier. The two proteins acting together play a key role in polarity establishment in the early embryo 3) We have identified a role for members of the small GTPas family (rab proteins) in early embryonic polarity.

Publications

  • Nathaniel Peters, Dahlia E. Perez, Mi Hye Song, Yan Liu, Thomas Muller-Reichert, Cathy Caron, Kenneth J Kemphues, and Kevin F OConnell 2010. Control of Mitotic and Meiotic Centriole Duplication by the Plk4- Related Kinase ZYG-1. J Cell Sci (in press)


Progress 10/01/07 to 09/30/08

Outputs
OUTPUTS: As this project is basic research, there are no outputs. PARTICIPANTS: Not relevant to this project. TARGET AUDIENCES: Because our work is basic biomedical science, our target audience is all humans. PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.

Impacts
Our research has led to changes in knowledge about cell polarity. In particular we have identified and studied new genes with roles in establishing or maintaining cell polarity. Work in the lab focuses on a group of proteins called PAR proteins. This reporting period we made progress in four areas: 1) We have learned that a serine/threonine kinase called PIG-1 acts redundantly with PAR-1 and PAR-4 to control the distribution of other polarity proteins in the one-cell C. elegans embryo. 2) We have identified an ubiquitin hydrolase called MATH-33 as having a role in supporting the function of the PAR-2 protein. 3) We have determined which protein domains of the PAR-3 protein are essential or non-essential for the function of the protein in living animals. 4) We have determined that the protein LGL-1 functions redundantly with the PAR-2 protein to restrict another set of proteins to the anterior end of the cell.

Publications

  • No publications reported this period


Progress 10/01/06 to 09/30/07

Outputs
OUTPUTS: Cell polarity is essential for many aspects of embryogenesis and homeostasis. Work in my lab focuses on understanding the mechanistic basis for polarity establishment in early embryonic cells of the nematode Caenorhabitis elegans, with particular emphasis on the roles of six genes we identified called par genes. The proteins made by these genes are required for polarized distributions of critical cell fate determinants in the early embryo, and for polarity in postembryonic tissues. Consistent with their role in polarity, the PAR proteins are distributed at the cell periphery in an asymmetric fashion and our data indicate they affect polarity by signaling differentially at the poles of the embryos. During the past year we have focused on 1) continuing an analysis of the roles of specific parts of the PAR-3 protein in living embryos 2) beginning the analysis of the proteins pig-1, lgl-1 and math-33, three proteins that can enhance par mutant phenotypes 3) testing the roles of specific parts of the par-6 protein in living animals. PARTICIPANTS: Diane Morton, Ph.D. Research Associate Wendy Hoose, M.S. Technician II Mona Hassab, Technician I Jin Li, Graduate Student (received Ph.D. during reporting period) Heon Kim, Graduate Student Bingsi Li, Graduate Student Alex Beatty, Graduate Student Rich McCloskey, Graduate Student TARGET AUDIENCES: National and International Basic Research and Medical Community

Impacts
This project is basic biomedical research that addresses animal development and cell function. In general, our work has provided insight into how the PAR proteins work to establish cell polarity in the C. elegans model system. Work in other labs has built on our discoveries and gone in new directions, showing that these same proteins act in a conserved way to regulate cell and organismal polarity in many animals. Athough the long-term impact of our work is expected to be in the area of human health, in particular understanding cancer, the discovery of RNA interference in my lab has made an impact on biotechnology research throughout the world. (Follow-up research elucidating the mechanism of RNA interference was awarded the 2006 Nobel Prize in physiology and medicine.)

Publications

  • No publications reported this period


Progress 01/01/06 to 12/31/06

Outputs
Cell polarity is essential for many aspects of embryogenesis and homeostasis. Work in my lab focuses on understanding the mechanistic basis for polarity establishment in early embryonic cells of the nematode Caenorhabitis elegans, with particular emphasis on the roles of six genes we identified called par genes. The proteins made by these genes are required for polarized distributions of critical cell fate determinants in the early embryo, and for polarity in postembryonic tissues. Consistent with their role in polarity, the PAR proteins are distributed at the cell periphery in an asymmetric fashion and our data indicate they affect polarity by signaling differentially at the poles of the embryos. During the past year we have focused on 1) continuing an analysis of the roles of specific parts of the PAR-3 protein in living embryos 2) completing an RNAi-based enhancer screen for proteins that function in polarity, and beginning the analysis of the most promising of these proteins 3)showing that the proteins ECT-2 and RHO-1 play an essential role in transducing the polarity signal from the sperm centrosome. In general our work has provided insight into how the PAR proteins work to establish cell polarity in the C. elegans model system. Work in other labs has built on our discoveries and gone in new directions, showing that these same proteins act in a conserved way to regulate cell and organismal polarity in many animals.

Impacts
This project is basic biomedical research that addresses animal development and cell function. Athough the long-term impact of our work is expected to be in the area of human health, the discovery of RNA interference in my lab has made an impact on biotechnology research throughout the world. (Follow-up research elucidating the mechanism of RNA interference was awarded the 2006 Nobel Prize in physiology and medicine.)

Publications

  • Beers M. and Kemphues K. 2006. Depletion of the co-chaperone CDC-37 reveals two modes of PAR-6 cortical association in C. elegans embryos. Development 133:3745-54.
  • Aceto D., Beers M. and Kemphues K.J. 2006. Interaction of PAR-6 with CDC-42 is required for maintenance but not establishment of PAR asymmetry in C. elegans. Dev Biol. 299:386-97.
  • Schetter, A., Askjaer, P., Piano, F., Mattaj, I. and Kemphues, K. 2006. Nucleoporins NPP-1, NPP-3, NPP-4, NPP-11 and NPP-13 are required for properspindle orientation in C.elegans. Developmental Biology 289:360-71.


Progress 01/01/05 to 12/31/05

Outputs
Cell polarity is essential for many aspects of embryogenesis and homeostasis. Work in my lab focuses on understanding the mechanistic basis for polarity establishment in early embryonic cells of the nematode Caenorhabitis elegans, with particular emphasis on the roles of six genes we identified called par genes. The proteins made by these genes are required for polarized distributions of critical cell fate determinants in the early embryo, and for polarity in postembryonic tissues. Consistent with their role in polarity, the PAR proteins are distributed at the cell periphery in an asymmetric fashion and our data indicate they affect polarity by signaling differentially at the poles of the embryos. During the past year we have focused on 1) continuing an analysis of the role of the roles of specific parts of the PAR-3 protein in living embryos 2) completing our analysis of the role of nuclear envelope in oriented cell divisions in the early embryo, 3) continuing to identify additional proteins that interact with PAR-1 using RNAi 4) investigating the role of fatty acid metabolism and protein stability in polarity, 5) testing the role of the actin cytoskeleton in transducing the polarity signal from the sperm centrosome. In general our work has provided insight into how these proteins work to establish cell polarity in the C. elegans model system. Work in other labs has built on our discoveries and gone in new directions, showing that these same proteins act in a conserved way to regulate cell and organismal polarity in many animals.

Impacts
This project is basic biomedical research that addresses animal development and cell function. Athough the long-term impact of our work is expected to be in the area of human health, the discovery of RNA interference in my lab has made an impact on biotechnology research throughout the world.

Publications

  • Kemphues K. 2005. Essential Genes (December 24, 2005), WormBook, ed. The C. elegans Research Community, WormBook, doi/10.1895/wormbook.1.57.1, http://www.wormbook.org.


Progress 01/01/04 to 12/31/04

Outputs
Cell polarity is essential for many aspects of embryogenesis and homeostasis. Work in my lab focuses on understanding the mechanistic basis for polarity establishment in early embryonic cells of the nematode Caenorhabitis elegans, with particular emphasis on the roles of six genes we identified called par genes. The proteins made by these genes are required for polarized distributions of critical cell fate determinants in the early embryo, and for polarity in postembryonic tissues. Consistent with their role in polarity, the PAR proteins are distributed at the cell periphery in an asymmetric fashion and our data indicate they affect polarity by signaling differentially at the poles of the embryos. During the past year we have focused on 1) testing the biological role of biochemical interactions between the PAR-6 and a conserved signaling molecule CDC-42, extending our previous studies with new reagents that report on the distribution of CDC-42 protein in the cell, 2) completing our analysis of a role for PAR-3 in postembryonic development, 3) analyzing the role of nuclear envelope in oriented cell divisions in the early embryo, 4) continuing to identify additional proteins that interact with PAR-1, 5) beginning an analysis of the roles of specific parts of the PAR-3 protein in living embryos and 6) investigating the role of fatty acid metabolism and protein stability in polarity. In general our work has provided insight into how these proteins work to establish cell polarity in the C. elegans model system. Work in other labs has built on our discoveries and gone in new directions, showing that these same proteins act in a conserved way to regulate cell and organismal polarity in many animals.

Impacts
This project is basic biomedical research. Athough the long-term impact of our work is expected to be in the area of human health, the discovery of RNA interference in my lab has made an impact on biotechnology research throughout the world.

Publications

  • Aono S, Legouis R, Hoose WA, Kemphues KJ. 2004. PAR-3 is required for epithelial cell polarity in the distal spermatheca of C. elegans Development. 131: 2865-74.


Progress 01/01/03 to 12/31/03

Outputs
Cell polarity is essential for many aspects of embryogenesis and homeostasis. Work in my lab focuses on understanding the mechanistic basis for polarity establishment in early embryonic cells of the nematode Caenorhabitis elegans, with particular emphasis on the roles of six genes we identified called par genes. The proteins made by these genes are required for polarized distributions of critical cell fate determinants in the early embryo, and for polarity in postembryonic tissues. Consistent with their role in polarity, the PAR proteins are distributed at the cell periphery in an asymmetric fashion and our data indicate they affect polarity by signaling differentially at the poles of the embryos. During the past year we have focused on 1) testing the biological role of biochemical interactions between the PAR-6 and a conserved signaling molecule CDC-42, 2) Analyzing a role for PAR-3 in postembryonic development, 3) analyzing the role of nuclear envelope in oriented cell divisions in the early embryo, and 4)seeking to identify additional proteins that interact with PAR-1 and PAR-4. In general our work has provided insight into how these proteins work in the nematode. Work in other labs has built on our discoveries and gone in new directions, showing that these same proteins act in a conserved way to regulate cell and organismal polarity in many animals.

Impacts
This project is basic biomedical research. Athough the long-term impact of our work is expected to be in the area of human health, the discovery of RNA interference in my lab has made an impact on biotechnology research throughout the world.

Publications

  • Hurd, D. D. and Kemphues, K. J. 2003. PAR-1 is required for morphogenesis of the Caenorhabditis elegans vulva. Developmental Biology 253: 54-65.
  • Cuenca, A. A., Schetter A., Aceto D., Kemphues, K., Seydoux, G. 2003. Polarization of the C. elegans zygote proceeds via distinct establishment and maintenance phases. Development 130: 1255-65.


Progress 01/01/02 to 12/31/02

Outputs
Cell polarity is essential for many aspects of embryogenesis and homeostasis. Work in my lab focuses on understanding the mechanistic basis for polarity establishment in early embryonic cells of the nematode Caenorhabitis elegans, with particular emphasis on the roles of six genes we identified called par genes. The proteins made by these genes are required for polarized distributions of critical cell fate determinants in the early embryo, and as we've discovered this year, for polarity in postembryonic tissues. Consistent with their role in polarity, the PAR proteins are distributed at the cell periphery in an asymmetric fashion and our data indicate they affect polarity by signaling differentially at the poles of the embryos. During the past year we have focused on 1) testing the biological role of biochemical interactions between the PAR-6.PAR-3 and PKC-3 proteins 2) demonstrating the role of CDC-42/PAR-6 interaction 3) completing our functional genomics analysis of a set of ovary-enriched genes, 4) completing an analysis of PAR-1 function during postembryonic development and 5) discovering and analyzing a role for PAR-3 in postembryonic development. In general our work has provided insight into how these proteins work in the nematode. Work in other labs has built on our discoveries and gone in new directions, showing that these same proteins act in a conserved way to regulate cell and organismal polarity in many animals.

Impacts
This project is basic biomedical research. Athough the long-term impact of our work is expected to be in the area of human health, the discovery of RNA interference in my lab has made an impact on biotechnology research throughout the world.

Publications

  • Morton, D.G., Shakes, D.C., Nugent, S., Dichoso, D., Wang, W., Golden A., and Kemphues, K. J. 2002. The C. elegans par-5 gene encodes a 14-3-3 protein required for cellular asymmetry in the early embryo. Developmental Biology 241: 47-58.
  • Piano F, Schetter AJ, Morton DG, Gunsalus KC, Reinke V, Kim SK, Kemphues KJ. 2002. Gene Clustering Based on RNAi Phenotypes of Ovary-Enriched Genes in C. elegans. Current Biology 12: 1959-1964.
  • Walhout AJ, Reboul J, Shtanko O, Bertin N, Vaglio P, Ge H, Lee H, Doucette-Stamm L, Gunsalus KC, Schetter AJ, Morton DG, Kemphues KJ, Reinke V, Kim SK, Piano F, Vidal M. 2002. Integrating Interactome, Phenome, and Transcriptome Mapping Data for the C. elegans Germline. Current Biology 12: 1952-1958.


Progress 01/01/01 to 12/31/01

Outputs
Cell polarity is essential for many aspects of embryogenesis and homeostasis. Work in my lab focuses on understanding the mechanistic basis for polarity establishment in early embryonic cells of the nematode Caenorhabditis elegans, with particular emphasis on the roles of six genes we identified called par genes. The proteins made by these genes are required for polarized distributions of critical cell fate determinants in the one-cell stage embryo. Consistent with their role in polarity, the PAR proteins are distributed at the cell periphery in an asymmetric fashion and our data indicate that they affect polarity by signaling differentially at the poles of the embryo. During the past year we have focused on 1) establishing the existence of biochemical interactions between PAR-6, PAR-3 and PKC-3 proteins, 2) testing the hypothesis that PAR-6 can bind to the CDC-42 protein 3) completing our molecular analysis of the par-5 gene, 4) finishing up a functional genomics analysis of a set of 750 genes that are expressed in the C. elegans ovary. All of these projects have moved forward. In general our work has provided insight into how cell polarity is established in this nematode. Recent work in other labs during the past two years has extended analysis of PAR-1, PAR-3, PAR-6 and PKC-3 to mammals and fruit flies, and frogs showing that these proteins are evolutionarily conserved and play a role in cell polarity in many animals.

Impacts
This project is basic biomedical research. Although the long term impact of our work is expected to be in the area of human health, the discovery of RNA interference in my lab and our recent application of it has had an impact on biotechnology research throughout the world.

Publications

  • O'Connell, K.F., Caron, C., Kopish, K.R., Hurd, D.D., Kemphues, K.J., Li, Yongjing, and White, J. G. 2001. The C. elegans zyg-1 Gene Encodes a Novel Regulator of Centrosome Duplication with Distinct Maternal and Paternal Roles in the Embryo. Cell 105: 547-558.


Progress 01/01/00 to 12/31/00

Outputs
Asymmetric cell division is essential for many aspects of embryogenesis and homeostasis. Work in my lab focuses on understanding the mechanistic basis for polarity establishment in early embryonic cells of the nematode Caenorhabditis elegans, with particular emphasis on the roles of six genes we identified called par genes. The proteins made by these genes are required for polarized distributions of critical cell fate determinants in the one-cell stage embryo. Consistent with their role in polarity, the PAR proteins are distributed at the cell periphery in an asymmetric fashion and our data indicate that they affect polarity by signaling differentially at the poles of the embryo. During the past year we have focused on 1) establishing the existence of biochemical interactions between PAR-6, PAR-3 and PKC-3 proteins, 2) testing the hypothesis that PAR-6 can bind to the CDC-42 protein 3) completing our molecular analysis of the par-4 gene 4) carrying out a functional genomics analysis of a set of about 1000 genes that are expressed in the C. elegans ovary. All of these projects have moved forward. In general our work has provided insight into how cell polarity is established. Recent work in other labs during the past year has extended analysis of PAR-3, PAR-6 and PKC-3 to mammals and fruit flies showing that these proteins are evolutionarily conserved and probably play a role in cell polarity in most animals. Our functional genomics analysis has provided proof of concept for using RNA interference on a large scale to assign functions to uncharacterized genes.

Impacts
This project is basic biomedical research. Although the long term impact of our work is expected to be in the area of human health, the discovery of RNA interference in my lab and our recent application of it has had an impact on biotechnology research throughout the world.

Publications

  • Watts, J. L., Morton, D.G., Bestman, J. and Kemphues, K. J. (2000) The C. elegans par-4 gene encodes a putative serine-threonine kinase required for establishing embryonic asymmetry. Development 127:1467-1475.
  • Tomancak, P.,Piano, F.,Riechmann, V., Gunsalus, K., Kemphues, K.J. and Ephrussi, A.(2000) A D. melanogaster homologue of C. elegans par-1 acts at an early step in embryonic axis formation. Nature Cell Biology 2: 458-460.
  • Piano, F., Schetter, A. J., Mangone, M., Stien, L. and Kemphues, K. (2000) RNAi analysis of genes expressed in the ovary of Caenorhabditis elegans. Current Biology 10: 1619-1622.
  • Piano, F. and Kemphues, K. (2000) Genetic analysis of intrinsically asymmetrical cell division. In Frontiers in Molecular Biology: Cell Polarity (D. Drubin, ed.) Oxford University Press, Oxford pp 240-268.
  • Kemphues, K.J. (2000) Parsing embryonic polarity. Cell 101: 345


Progress 01/01/99 to 12/31/99

Outputs
Asymmetric cell division is essential for many aspects of embryogenesis and homeostasis. Work in my lab focuses on understanding the mechanistic basis for polarity establishment in early embryonic cells of the nematode Caenorhabditis elegans, with particular emphasis on the roles of six genes we identified called par genes. The proteins made by these genes are required for polarized distributions of critical cell fate determinants in the one-cell stage embryo. Consistent with their role in polarity, they are distributed at the cell periphery in an asymmetric fashion and our data indicate that they affect polarity by signaling differentially at the poles of the embryo. During the past year we have focused on 1) finishing up our analysis of the par-6 gene, 2) establishing the existence of biochemical interactions between PAR-6, PAR-3 and PKC-3 proteins, 3) testing (and disproving) the hypothesis that the microtubule-associated protein Tau is a substrate for the PAR-1 protein kinase 4) carrying out screens for proteins that interact with PAR-1 and PAR-4 5) developing protocols for large scale screens for new polarity genes using RNA interference, a novel reverse genetics approach that was discovered in my lab. All of these projects have moved forward. In general our work has provided insight into how cell polarity is established. In particular, recent work in other labs during the past year has extended analysis of par-1 and par-3 to mammals and fruit flies showing that these proteins are evolutionarily conserved and probably play a role in cell polarity in both of those systems.

Impacts
This project is basic biomedical research. Although the long term impact of our work is expected to be in the area of human health, the discovery of RNA interference in my lab has had an impact on biotechnology research throughout the world.

Publications

  • Hung, T-J., and 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.
  • Zalevsky, J., MacQueen, A.J., Duffy, J.B., Kemphues, K.J., and Villeneuve, A.M. 1999. Crossing over during Caenorhabditis elegans meiosis requires a conserved MutS-based pathway that is partially dispensable in budding yeast. Genetics 153:1271-83.


Progress 01/01/98 to 12/31/98

Outputs
Our focus continues to be investigating the role of asymmetric distribution of cytoplasm in the establishment of embryonic cell fates in the nematode C. elegans. During the past year we have made significant progress in several areas. In general, all of our progress has brought us closer to a mechanistic understanding of how cell polarity is established. Major lessons are: 1) intracellular signaling is involved 2) key molecules are themselves distributed in a polar fashion 3) protein phosphorylation plays a major role.

Impacts
(N/A)

Publications

  • Izumi, Y., Hirose, T., Tamai, Y., Hirai, S., Nagashima, Y., Fujimoto, T., Tabuse, Y., Kemphues, K. J., and Ohno, S. 1998. An atypical PKC directly associates and colocalizes at the epithelial tight junction with ASIP, a mammalian homologue of Caenorhabditis elegans polarity protein PAR-3. J. Cell Biol. 143:95-106.
  • Matthews, L. R., Carter, P., Thierry-Mieg, D., and Kemphues, K. 1998. ZYG-9, a Caenorhabditis elegans protein required for microtubule organization and function, is a component of meiotic and mitotic spindle poles. J. Cell Biol. 141:1159-68.
  • Rose, L. S., and Kemphues, K. 1998. The let-99 gene is required for proper spindle orientation during cleavage of the C. elegans embryo. Development 125:1337-46.
  • Rose, L. S., and Kemphues, K. J. 1998. Early patterning of the C. elegans embryo. Ann. Rev. Genet 32:521-45.
  • Rose, L. S., Lamb, M. L., Hird, S. N., and Kemphues, K. J. 1995. Pseudocleavage is dispensable for polarity and development in C. elegans embryos. Dev. Biol. 168:479-89.
  • Tabuse, Y., Izumi, Y., Piano, F., Kemphues, K. J., Miwa, J., and Ohno, S. 1998. Atypical protein kinase C cooperates with PAR-3 to establish embryonic polarity in Caenorhabditis elegans. Development 125:3607-14.