Morphogenesis of the vulva and the vulval-uterine connection.

The C. elegans hermaphrodite vulva is an established model system to study mechanisms of cell fate specification and tissue morphogenesis. The adult vulva is a tubular shaped organ composed of seven concentric toroids that arise from selective fusion between differentiated vulval progeny. The dorsal end of the vulval tubule is connected to the uterus via a multinucleate syncytium utse (uterine-seam) cell. The vulval tubule and utse are formed as a result of changes in morphogenetic processes such as cell polarity, adhesion, and invagination. A number of genes controlling these processes are conserved all the way up to human and function in similar developmental contexts. This makes it possible to extend the findings to other metazoan systems. Gene expression studies in the vulval and uterine cells have revealed the presence of regulatory networks specifying distinct cell fates. Thus, these two cell types serve as a good system to understand how gene networks confer unique cell identities both experimentally and computationally. This chapter focuses on morphogenetic processes during the formation of the vulva and its connection to uterus.

[1]  Abstract , 1952 .

[2]  J. Rothman,et al.  Repression of cell-cell fusion by components of the C. elegans vacuolar ATPase complex. , 2005, Developmental cell.

[3]  G. Freyd.  Molecular analysis of the Caenorhabditis elegans cell, lineage gene lin-11 , 1991 .

[4]  K. Kemphues,et al.  PAR-1 is required for morphogenesis of the Caenorhabditis elegans vulva. , 2003, Developmental biology.

[5]  P. Sternberg,et al.  The C. elegans LIM homeobox gene lin-11 specifies multiple cell fates during vulval development , 2003, Development.

[6]  P. Sternberg,et al.  cis-Regulatory control of three cell fate-specific genes in vulval organogenesis of Caenorhabditis elegans and C. briggsae. , 2003, Developmental biology.

[7]  Min Han,et al.  The C. elegans evl-20 gene is a homolog of the small GTPase ARL2 and regulates cytoskeleton dynamics during cytokinesis and morphogenesis. , 2002, Developmental cell.

[8]  J. Culotti,et al.  Vulva morphogenesis involves attraction of plexin 1-expressing primordial vulva cells to semaphorin 1a sequentially expressed at the vulva midline , 2005, Development.

[9]  L. Chernomordik,et al.  AFF-1, a FOS-1-regulated fusogen, mediates fusion of the anchor cell in C. elegans. , 2007, Developmental cell.

[10]  B. Gupta,et al.  Dissection of lin-11 enhancer regions in Caenorhabditis elegans and other nematodes. , 2009, Developmental biology.

[11]  E. Perens,et al.  C. elegans daf-6 encodes a patched-related protein required for lumen formation. , 2005, Developmental cell.

[12]  H. Chamberlin,et al.  The Pax2/5/8 gene egl-38 coordinates organogenesis of the C. elegans egg-laying system. , 2007, Developmental biology.

[13]  H. Cinar,et al.  N-ethylmaleimide sensitive factor is required for fusion of the C. elegans uterine anchor cell. , 2006, Developmental biology.

[14]  P. Sternberg,et al.  Tissue-specific regulation of the LIM homeobox gene lin-11 during development of the Caenorhabditis elegans egg-laying system. , 2002, Developmental biology.

[15]  Mark J Alkema,et al.  Tyramine Functions Independently of Octopamine in the Caenorhabditis elegans Nervous System , 2005, Neuron.

[16]  P. Sternberg,et al.  A point mutation in the extracellular domain activates LET-23, the Caenorhabditis elegans epidermal growth factor receptor homolog , 1996, Molecular and cellular biology.

[17]  P. Sternberg,et al.  Anchor cell invasion into the vulval epithelium in C. elegans. , 2003, Developmental cell.

[18]  Channing J Der,et al.  Ras effector switching promotes divergent cell fates in C. elegans vulval patterning. , 2011, Developmental cell.

[19]  B. J. Hwang,et al.  C. elegans EVI1 proto-oncogene, EGL-43, is necessary for Notch-mediated cell fate specification and regulates cell invasion , 2007, Development.

[20]  Paul W. Sternberg,et al.  A genetic pathway for the specification of the vulval cell lineages of Caenorhabditis elegans , 1987, Nature.

[21]  R. Burdine,et al.  EGL-17(FGF) expression coordinates the attraction of the migrating sex myoblasts with vulval induction in C. elegans. , 1998, Development.

[22]  John White,et al.  The type I membrane protein EFF-1 is essential for developmental cell fusion. , 2002, Developmental cell.

[23]  H. Cinar,et al.  The EGL-13 SOX domain transcription factor affects the uterine pi cell lineages in Caenorhabditis elegans. , 2003, Genetics.

[24]  P. Sternberg,et al.  The PAX gene egl-38 mediates developmental patterning in Caenorhabditis elegans. , 1997, Development.

[25]  Sama F. Sleiman,et al.  Developmental functions for the Caenorhabditis elegans Sp protein SPTF-3 , 2011, Mechanisms of Development.

[26]  H. Horvitz,et al.  Caenorhabditis elegans early embryogenesis and vulval morphogenesis require chondroitin biosynthesis , 2003, Nature.

[27]  H. Horvitz,et al.  The SQV-1 UDP-glucuronic acid decarboxylase and the SQV-7 nucleotide-sugar transporter may act in the Golgi apparatus to affect Caenorhabditis elegans vulval morphogenesis and embryonic development , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[28]  Christian A. Grove,et al.  Insight into transcription factor gene duplication from Caenorhabditis elegans Promoterome-driven expression patterns , 2007, BMC Genomics.

[29]  Elliott J. Hagedorn,et al.  UNC-6 (Netrin) Orients the Invasive Membrane of the Anchor Cell in C. elegans , 2008, Nature Cell Biology.

[30]  Paul W. Sternberg,et al.  Opposing Wnt Pathways Orient Cell Polarity during Organogenesis , 2008, Cell.

[31]  P. Sternberg,et al.  Caenorhabditis elegans cog-1 locus encodes GTX/Nkx6.1 homeodomain proteins and regulates multiple aspects of reproductive system development. , 2002, Developmental biology.

[32]  H. Horvitz,et al.  lin-17 mutations of Caenorhabditis elegans disrupt certain asymmetric cell divisions. , 1988, Developmental biology.

[33]  R. J. Hill,et al.  lin-17/Frizzled and lin-18 regulate POP-1/TCF-1 localization and cell type specification during C. elegans vulval development. , 2005, Developmental biology.

[34]  H. Rehrauer,et al.  LIN-39 and the EGFR/RAS/MAPK pathway regulate C. elegans vulval morphogenesis via the VAB-23 zinc finger protein , 2011, Development.

[35]  A. Hajnal,et al.  Notch Inhibition of RAS Signaling Through MAP Kinase Phosphatase LIP-1 During C. elegans Vulval Development , 2001, Science.

[36]  W. Hanna-Rose,et al.  The anchor cell initiates dorsal lumen formation during C. elegans vulval tubulogenesis. , 2009, Developmental biology.

[37]  M. Han,et al.  COG-2, a sox domain protein necessary for establishing a functional vulval-uterine connection in Caenorhabditis elegans. , 1999, Development.

[38]  J. White,et al.  Formation of the vulva in Caenorhabditis elegans: a paradigm for organogenesis. , 1999, Development.

[39]  David Q. Matus,et al.  In Vivo Identification of Regulators of Cell Invasion Across Basement Membranes , 2010, Science Signaling.

[40]  R. J. Hill,et al.  C. elegans LIN-18 Is a Ryk Ortholog and Functions in Parallel to LIN-17/Frizzled in Wnt Signaling , 2004, Cell.

[41]  H. Horvitz,et al.  SQV-7, a protein involved in Caenorhabditis elegans epithelial invagination and early embryogenesis, transports UDP-glucuronic acid, UDP-N- acetylgalactosamine, and UDP-galactose , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[42]  I. Rimann,et al.  Regulation of anchor cell invasion and uterine cell fates by the egl-43 Evi-1 proto-oncogene in Caenorhabditis elegans. , 2007, Developmental biology.

[43]  M. Sundaram,et al.  ced-10 Rac and mig-2 function redundantly and act with unc-73 trio to control the orientation of vulval cell divisions and migrations in Caenorhabditis elegans. , 2002, Developmental biology.

[44]  K. Kornfeld,et al.  Identification of cis-regulatory elements from the C. elegans Hox gene lin-39 required for embryonic expression and for regulation by the transcription factors LIN-1, LIN-31 and LIN-39. , 2006, Developmental biology.

[45]  H. Horvitz,et al.  The Caenorhabditis elegans vulval morphogenesis gene sqv-4 encodes a UDP-glucose dehydrogenase that is temporally and spatially regulated , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[46]  H. Horvitz,et al.  Three proteins involved in Caenorhabditis elegans vulval invagination are similar to components of a glycosylation pathway. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[47]  Paul W Sternberg,et al.  The tailless Ortholog nhr-67 Regulates Patterning of Gene Expression and Morphogenesis in the C. elegans Vulva , 2007, PLoS genetics.

[48]  Cornelia I. Bargmann,et al.  The Immunoglobulin Superfamily Protein SYG-1 Determines the Location of Specific Synapses in C. elegans , 2003, Cell.

[49]  J. White,et al.  Morphogenesis of the C. elegans hermaphrodite uterus. , 1996, Development.

[50]  W. Hanna-Rose,et al.  EGF signaling overcomes a uterine cell death associated with temporal mis-coordination of organogenesis within the C. elegans egg-laying apparatus. , 2006, Developmental biology.

[51]  Kyuhyung Kim,et al.  Expression and regulation of an FMRFamide‐related neuropeptide gene family in Caenorhabditis elegans , 2004, The Journal of comparative neurology.

[52]  P. Sternberg,et al.  C. elegans BED domain transcription factor BED-3 controls lineage-specific cell proliferation during organogenesis. , 2010, Developmental biology.

[53]  Min Han,et al.  Cis regulatory requirements for vulval cell-specific expression of the Caenorhabditis elegans fibroblast growth factor gene egl-17. , 2003, Developmental biology.

[54]  Min Han,et al.  The Caenorhabditis elegans EGL-26 protein mediates vulval cell morphogenesis. , 2002, Developmental biology.

[55]  J. Bettinger,et al.  The terminal differentiation factor LIN-29 is required for proper vulval morphogenesis and egg laying in Caenorhabditis elegans. , 1997, Development.

[56]  J. Vandekerckhove,et al.  unc-53 controls longitudinal migration in C. elegans. , 2002, Development.

[57]  Paul W Sternberg,et al.  The Caenorhabditis elegans vulva: A post-embryonic gene regulatory network controlling organogenesis , 2008, Proceedings of the National Academy of Sciences.

[58]  H. Horvitz,et al.  The Caenorhabditis elegans gene lin-17, which is required for certain asymmetric cell divisions, encodes a putative seven-transmembrane protein similar to the Drosophila frizzled protein. , 1996, Genes & development.

[59]  I. Greenwald.  LIN-12/Notch signaling in C. elegans. , 2005, WormBook : the online review of C. elegans biology.

[60]  Valerie Reinke,et al.  Protein kinase VRK-1 regulates cell invasion and EGL-17/FGF signaling in Caenorhabditis elegans. , 2009, Developmental biology.

[61]  D. Hirsh,et al.  The postembryonic cell lineages of the hermaphrodite and male gonads in Caenorhabditis elegans. , 1979, Developmental biology.

[62]  H. Horvitz,et al.  sqv mutants of Caenorhabditis elegans are defective in vulval epithelial invagination. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[63]  S. K. Kim,et al.  Protruding vulva mutants identify novel loci and Wnt signaling factors that function during Caenorhabditis elegans vulva development. , 2000, Genetics.

[64]  H. Chamberlin,et al.  The Caenorhabditis elegans heterochronic gene lin‐14 coordinates temporal progression and maturation in the egg‐laying system , 2009, Developmental dynamics : an official publication of the American Association of Anatomists.

[65]  P. Sternberg,et al.  Patterning of the C. elegans 1 degrees vulval lineage by RAS and Wnt pathways. , 2000, Development.

[66]  Elliott J. Hagedorn,et al.  Integrin acts upstream of netrin signaling to regulate formation of the anchor cell's invasive membrane in C. elegans. , 2009, Developmental cell.

[67]  D. M. Eisenmann.  Wnt signaling. , 2005, WormBook : the online review of C. elegans biology.

[68]  P. Sternberg,et al.  Reciprocal EGF signaling back to the uterus from the induced C. elegans vulva coordinates morphogenesis of epithelia , 1999, Current Biology.

[69]  B. Gupta,et al.  Evolution of Developmental Control Mechanism Conserved mechanism of Wnt signaling function in the specification of vulval precursor fates in C. elegans and C. briggsae , 2010 .

[70]  Kavita S Oommen,et al.  Co-regulation by Notch and Fos is required for cell fate specification of intermediate precursors during C. elegans uterine development , 2007, Development.

[71]  J. White,et al.  The Caenorhabditis elegans lin-12 gene mediates induction of ventral uterine specialization by the anchor cell. , 1995, Development.

[72]  P. Sternberg,et al.  The Caenorhabditis elegans heterochronic gene lin-29 coordinates the vulval–uterine–epidermal connections , 2000, Current Biology.

[73]  P. Sternberg,et al.  Transcriptional network underlying Caenorhabditis elegans vulval development. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[74]  P. Sternberg,et al.  The small ubiquitin-like modifier (SUMO) is required for gonadal and uterine-vulval morphogenesis in Caenorhabditis elegans. , 2004, Genes & development.

[75]  B. Lakowski,et al.  The tailless ortholog nhr-67 functions in the development of the C. elegans ventral uterus. , 2011, Developmental biology.

[76]  W B Wood,et al.  cdh-3, a gene encoding a member of the cadherin superfamily, functions in epithelial cell morphogenesis in Caenorhabditis elegans. , 1996, Development.

[77]  A. Jose,et al.  A Specific Subset of Transient Receptor Potential Vanilloid-Type Channel Subunits in Caenorhabditis elegans Endocrine Cells Function as Mixed Heteromers to Promote Neurotransmitter Release , 2007, Genetics.

[78]  H. Horvitz,et al.  The Caenorhabditis elegans Genes sqv-2and sqv-6, Which Are Required for Vulval Morphogenesis, Encode Glycosaminoglycan Galactosyltransferase II and Xylosyltransferase* 210 , 2003, The Journal of Biological Chemistry.

[79]  H. Horvitz,et al.  The lin-11 LIM domain transcription factor is necessary for morphogenesis of C. elegans uterine cells. , 1999, Development.

[80]  B. J. Hwang,et al.  A cell-specific enhancer that specifies lin-3 expression in the C. elegans anchor cell for vulval development , 2004, Development.

[81]  W. Hanna-Rose,et al.  Membrane localization of the NlpC/P60 family protein EGL-26 correlates with regulation of vulval cell morphogenesis in Caenorhabditis elegans. , 2007, Developmental biology.

[82]  H. Horvitz,et al.  Cell interactions coordinate the development of the C. elegans egg-laying system , 1990, Cell.

[83]  Rainer Breitling,et al.  A circuit model of the temporal pattern generator of Caenorhabditis egg-laying behavior , 2010, BMC Systems Biology.

[84]  M. Tessier-Lavigne,et al.  A Neurexin-Related Protein, BAM-2, Terminates Axonal Branches in C. elegans , 2003, Science.

[85]  M. Chalfie,et al.  Organogenesis in C. elegans: Positioning of neurons and muscles in the egg-laying system , 1990, Neuron.

[86]  Cornelia I Bargmann,et al.  Synaptic Specificity Is Generated by the Synaptic Guidepost Protein SYG-2 and Its Receptor, SYG-1 , 2004, Cell.

[87]  P. Sternberg,et al.  FOS-1 Promotes Basement-Membrane Removal during Anchor-Cell Invasion in C. elegans , 2005, Cell.

[88]  Thomas R Bürglin,et al.  Comprehensive analysis of gene expression patterns of hedgehog-related genes , 2006, BMC Genomics.