The Caenorhabditis elegans epidermis as a model skin. II: Differentiation and physiological roles

Wiley Interdisciplinary Reviews: Developmental Biology

Volumn 1, Issue 6, 2012, Pages 879-902

  Chisholm, Andrew D ^a   Xu, Suhong ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEINASE ACTIVATED RECEPTOR 3;

ARTICLE; BASEMENT MEMBRANE; CAENORHABDITIS ELEGANS; CELL AGING; CELL DAMAGE; CELL DEATH; CELL DIFFERENTIATION; CUTICLE; CYTOSKELETON; ENDOCYTOSIS; EPIDERMIS; GENE EXPRESSION; GENETIC REGULATION; INNATE IMMUNITY; LIPID STORAGE; MOLTING; NERVOUS SYSTEM; NONHUMAN; SYNAPTOGENESIS; WNT SIGNALING PATHWAY; WOUND HEALING;

BARRIER EPITHELIA; EPITHELIA; MORPHOGENESIS; PAR PROTEINS; WOUND HEALING;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL AGING; CELL DIFFERENTIATION; CYTOSKELETON; EPIDERMIS; IONS; MODELS, BIOLOGICAL; SIGNAL TRANSDUCTION;

EID: 84880525415     PISSN: 17597684     EISSN: 17597692     Source Type: Journal    
DOI: 10.1002/wdev.77     Document Type: Article

References (214)

1. Chisholm AD, Hsiao TI. The Caenorhabditis elegans epidermis as a model skin. I: development, patterning, and growth XXXX, XX:XX-XX.
2. Labouesse M. Epithelial junctions and attachments. WormBook 2006, 13:1-21.
3. Ding M, Woo WM, Chisholm AD. The cytoskeleton and epidermal morphogenesis in C. elegans. Exp Cell Res 2004, 301:84-90.
4. Zhang H, Gally C, Labouesse M. Tissue morphogenesis: how multiple cells cooperate to generate a tissue. Curr Opin Cell Biol 2010, 22:575-582.
5. Grana TM, Cox EA, Lynch AM, Hardin J. SAX-7/L1CAM and HMR-1/cadherin function redundantly in blastomere compaction and non-muscle myosin accumulation during Caenorhabditis elegans gastrulation. Developmental biology 2010, 344:731-744.
6. Legouis R, Gansmuller A, Sookhareea S, Bosher JM, Baillie DL, Labouesse M. LET-413 is a basolateral protein required for the assembly of adherens junctions in Caenorhabditis elegans. Nat Cell Biol 2000, 2:415-422.
7. Totong R, Achilleos A, Nance J. PAR-6 is required for junction formation but not apicobasal polarization in C. elegans embryonic epithelial cells. Development 2007, 134:1259-1268.
8. Achilleos A, Wehman AM, Nance J. PAR-3 mediates the initial clustering and apical localization of junction and polarity proteins during C. elegans intestinal epithelial cell polarization. Development 2010, 137:1833-1842.
9. Huang CC, Hall DH, Hedgecock EM, Kao G, Karantza V, Vogel BE, Hutter H, Chisholm AD, Yurchenco PD, Wadsworth WG. Laminin alpha subunits and their role in C. elegans development. Development 2003, 130:3343-3358.
10. Koppen M, Simske JS, Sims PA, Firestein BL, Hall DH, Radice AD, Rongo C, Hardin JD. Cooperative regulation of AJM-1 controls junctional integrity in Caenorhabditis elegans epithelia. Nat Cell Biol 2001, 3:983-991.
11. Firestein BL, Rongo C. DLG-1 is a MAGUK similar to SAP97 and is required for adherens junction formation. Mol Biol Cell 2001, 12:3465-3475.
12. Raich WB, Agbunag C, Hardin J. Rapid epithelial-sheet sealing in the Caenorhabditis elegans embryo requires cadherin-dependent filopodial priming. Curr Biol 1999, 9:1139-1146.
13. Costa M, Raich W, Agbunag C, Leung B, Hardin J, Priess JR. A putative catenin-cadherin system mediates morphogenesis of the Caenorhabditis elegans embryo. J Cell Biol 1998, 141:297-308.
14. Pettitt J, Cox EA, Broadbent ID, Flett A, Hardin J. The Caenorhabditis elegans p120 catenin homologue, JAC-1, modulates cadherin-catenin function during epidermal morphogenesis. J Cell Biol 2003, 162:15-22.
15. Simske JS, Koppen M, Sims P, Hodgkin J, Yonkof A, Hardin J. The cell junction protein VAB-9 regulates adhesion and epidermal morphology in C. elegans. Nat Cell Biol 2003, 5:619-625.
16. Gattegno T, Mittal A, Valansi C, Nguyen KC, Hall DH, Chernomordik LV, Podbilewicz B. Genetic control of fusion pore expansion in the epidermis of Caenorhabditis elegans. Mol Biol Cell 2007, 18:1153-1166.
17. Priess JR, Hirsh DI. Caenorhabditis elegans morphogenesis: the role of the cytoskeleton in elongation of the embryo. Dev Biol 1986, 117:156-173.
18. Costa M, Draper BW, Priess JR. The role of actin filaments in patterning the Caenorhabditis elegans cuticle. Dev Biol 1997, 184:373-384.
19. Norman KR, Moerman DG. Alpha spectrin is essential for morphogenesis and body wall muscle formation in Caenorhabditis elegans. J Cell Biol 2002, 157:665-677.
20. McKeown C, Praitis V, Austin J. sma-1 encodes a βH-spectrin homolog required for Caenorhabditis elegans morphogenesis. Development 1998, 125:2087-2098.
21. Praitis V, Ciccone E, Austin J. SMA-1 spectrin has essential roles in epithelial cell sheet morphogenesis in C. elegans. Dev Biol 2005, 283:157-170.
22. Starr DA, Han M. Role of ANC-1 in tethering nuclei to the actin cytoskeleton. Science 2002, 298:406-409.
23. Williams-Masson EM, Heid PJ, Lavin CA, Hardin J. The cellular mechanism of epithelial rearrangement during morphogenesis of the Caenorhabditis elegans dorsal hypodermis. Dev Biol 1998, 204:263-276.
24. Fridolfsson HN, Starr DA. Kinesin-1 and dynein at the nuclear envelope mediate the bidirectional migrations of nuclei. J Cell Biol 2010, 191:115-128.
25. Francis R, Waterston RH. Muscle cell attachment in Caenorhabditis elegans. J Cell Biol 1991, 114:465-479.
26. Plenefisch JD, Zhu X, Hedgecock EM. Fragile skeletal muscle attachments in dystrophic mutants of Caenorhabditis elegans: isolation and characterization of the mua genes. Development 2000, 127:1197-1207.
27. Hresko MC, Williams BD, Waterston RH. Assembly of body wall muscle and muscle cell attachment structures in Caenorhabditis elegans. J Cell Biol 1994, 124:491-506.
28. Bosher JM, Hahn BS, Legouis R, Sookhareea S, Weimer RM, Gansmuller A, Chisholm AD, Rose AM, Bessereau JL, Labouesse M. The Caenorhabditis elegans vab-10 spectraplakin isoforms protect the epidermis against internal and external forces. J Cell Biol 2003, 161:757-768.
29. Karabinos A, Schmidt H, Harborth J, Schnabel R, Weber K. Essential roles for four cytoplasmic intermediate filament proteins in Caenorhabditis elegans development. Proc Natl Acad Sci USA 2001, 98:7863-7868.
30. Hapiak V, Hresko MC, Schriefer LA, Saiyasisongkhram K, Bercher M, Plenefisch J. mua-6, a gene required for tissue integrity in Caenorhabditis elegans, encodes a cytoplasmic intermediate filament. Dev Biol 2003, 263:330-342.
31. Woo WM, Goncharov A, Jin Y, Chisholm AD. Intermediate filaments are required for C. elegans epidermal elongation. Dev Biol 2004, 267:216-229.
32. Kaminsky R, Denison C, Bening-Abu-Shach U, Chisholm AD, Gygi SP, Broday L. SUMO regulates the assembly and function of a cytoplasmic intermediate filament protein in C. elegans. Dev Cell 2009, 17:724-735.
33. Ding M, Goncharov A, Jin Y, Chisholm AD. C. elegans ankyrin repeat protein VAB-19 is a component of epidermal attachment structures and is essential for epidermal morphogenesis. Development 2003, 130:5791-5801.
34. Ding M, King RS, Berry EC, Wang Y, Hardin J, Chisholm AD. The cell signaling adaptor protein EPS-8 is essential for C. elegans epidermal elongation and interacts with the ankyrin repeat protein VAB-19. PLoS One 2008, 3:e3346.
35. Hetherington S, Gally C, Fritz JA, Polanowska J, Reboul J, Schwab Y, Zahreddine H, Behm C, Labouesse M. PAT-12, a potential anti-nematode target, is a new spectraplakin partner essential for Caenorhabditis elegans hemidesmosome integrity and embryonic morphogenesis. Dev Biol 2011, 350:267-278.
36. Hresko MC, Schriefer LA, Shrimankar P, Waterston RH. Myotactin, a novel hypodermal protein involved in muscle-cell adhesion in Caenorhabditis elegans. J Cell Biol 1999, 146:659-672.
37. Bercher M, Wahl J, Vogel BE, Lu C, Hedgecock EM, Hall DH, Plenefisch JD. mua-3, a gene required for mechanical tissue integrity in Caenorhabditis elegans, encodes a novel transmembrane protein of epithelial attachment complexes. J Cell Biol 2001, 154:415-426.
38. Hong L, Elbl T, Ward J, Franzini-Armstrong C, Rybicka KK, Gatewood BK, Baillie DL, Bucher EA. MUP-4 is a novel transmembrane protein with functions in epithelial cell adhesion in Caenorhabditis elegans. J Cell Biol 2001, 154:403-414.
39. Zahreddine H, Zhang H, Diogon M, Nagamatsu Y, Labouesse M. CRT-1/calreticulin and the E3 ligase EEL-1/HUWE1 control hemidesmosome maturation in C. elegans development. Curr Biol 2010, 20:322-327.
40. Williams BD, Waterston RH. Genes critical for muscle development and function in Caenorhabditis elegans identified through lethal mutations. J Cell Biol 1994, 124:475-490.
41. Zhang H, Landmann F, Zahreddine H, Rodriguez D, Koch M, Labouesse M. A tension-induced mechanotransduction pathway promotes epithelial morphogenesis. Nature 2011, 471:99-103.
42. Graham PL, Johnson JJ, Wang S, Sibley MH, Gupta MC, Kramer JM. Type IV collagen is detectable in most, but not all, basement membranes of Caenorhabditis elegans and assembles on tissues that do not express it. J Cell Biol 1997, 137:1171-1183.
43. Woo WM, Berry EC, Hudson ML, Swale RE, Goncharov A, Chisholm AD. The C. elegans F-spondin family protein SPON-1 maintains cell adhesion in neural and non-neural tissues. Development 2008, 135: 2747-2756.
44. Johnson RP, Kang SH, Kramer JM. C. elegans dystroglycan DGN-1 functions in epithelia and neurons, but not muscle, and independently of dystrophin. Development 2006, 133:1911-1921.
45. Gotenstein JR, Swale RE, Fukuda T, Wu Z, Giurumescu CA, Goncharov A, Jin Y, Chisholm AD. The C. elegans peroxidasin PXN-2 is essential for embryonic morphogenesis and inhibits adult axon regeneration. Development 2010, 137:3603-3613.
46. Muriel JM, Dong C, Hutter H, Vogel BE. Fibulin-1C and Fibulin-1D splice variants have distinct functions and assemble in a hemicentin-dependent manner. Development 2005, 132:4223-4234.
47. Spike CA, Davies AG, Shaw JE, Herman RK. MEC-8 regulates alternative splicing of unc-52 transcripts in C. elegans hypodermal cells. Development 2002, 129: 4999-5008.
48. Davies AG, Spike CA, Shaw JE, Herman RK. Functional overlap between the mec-8 gene and five sym genes in Caenorhabditis elegans. Genetics 1999, 153:117-134.
49. Yochem J, Bell LR, Herman RK. The identities of sym-2, sym-3 and sym-4, three genes that are synthetically lethal with mec-8 in Caenorhabditis elegans. Genetics 2004, 168:1293-1306.
50. Hedgecock EM, Culotti JG, Hall DH, Stern BD. Genetics of cell and axon migrations in Caenorhabditis elegans. Development 1987, 100:365-382.
51. Knobel KM, Jorgensen EM, Bastiani MJ. Growth cones stall and collapse during axon outgrowth in Caenorhabditis elegans. Development 1999, 126: 4489-4498.
52. White JG, Southgate E, Thomson JN, Brenner S. The structure of the ventral nerve cord of Caenorhabditis elegans. Phil Trans R Soc Lond B Biol Sci 1976, 275:327-348.
53. Hobert O, Bulow H. Development and maintenance of neuronal architecture at the ventral midline of C. elegans. Curr Opin Neurobiol 2003, 13:70-78.
54. Shibata Y, Fujii T, Dent JA, Fujisawa H, Takagi S. EAT-20, a novel transmembrane protein with EGF motifs, is required for efficient feeding in Caenorhabditis elegans. Genetics 2000, 154:635-646.
55. Bergmann DC, Crew JR, Kramer JM, Wood WB. Cuticle chirality and body handedness in Caenorhabditis elegans. Dev Genet 1998, 23:164-174.
56. Bulow HE, Boulin T, Hobert O. Differential functions of the C. elegans FGF receptor in axon outgrowth and maintenance of axon position. Neuron 2004, 42: 367-374.
57. Bulow HE, Hobert O. Differential sulfations and epimerization define heparan sulfate specificity in nervous system development. Neuron 2004, 41:723-736.
58. Hedgecock EM, Culotti JG, Hall DH. The unc-5, unc-6, and unc-40 genes guide circumferential migrations of pioneer axons and mesodermal cells on the epidermis in C. elegans. Neuron 1990, 4:61-85.
59. Wadsworth WG, Bhatt H, Hedgecock EM. Neuroglia and pioneer neurons express UNC-6 to provide global and local netrin cues for guiding migrations in C. elegans. Neuron 1996, 16:35-46.
60. Huang X, Huang P, Robinson MK, Stern MJ, Jin Y. UNC-71, a disintegrin and metalloprotease (ADAM) protein, regulates motor axon guidance and sex myoblast migration in C. elegans. Development 2003, 130:3147-3161.
61. Colavita A, Tessier-Lavigne M. A Neurexin-related protein, BAM-2, terminates axonal branches in C. elegans. Science 2003, 302:293-296.
62. Habibi-Babadi N, Su A, de Carvalho CE, Colavita A. The N-glycanase png-1 acts to limit axon branching during organ formation in Caenorhabditis elegans. J Neurosci 2010, 30:1766-1776.
63. Shen K, Fetter RD, Bargmann CI. Synaptic specificity is generated by the synaptic guidepost protein SYG-2 and its receptor, SYG-1. Cell 2004, 116:869-881.
64. Hagedorn EJ, Sherwood DR. Cell invasion through basement membrane: the anchor cell breaches the barrier. Curr Opin Cell Biol 2011, 23:589-596.
65. Ihara S, Hagedorn EJ, Morrissey MA, Chi Q, Motegi F, Kramer JM, Sherwood DR. Basement membrane sliding and targeted adhesion remodels tissue boundaries during uterine-vulval attachment in Caenorhabditis elegans. Nat Cell Biol 2011, 13:641-651.
66. Whangbo J, Harris J, Kenyon C. Multiple levels of regulation specify the polarity of an asymmetric cell division in C. elegans. Development 2000, 127: 4587-4598.
67. Gleason JE, Eisenmann DM. Wnt signaling controls the stem cell-like asymmetric division of the epithelial seam cells during C. elegans larval development. Dev Biol 2010, 348:58-66.
68. Pan CL, Howell JE, Clark SG, Hilliard M, Cordes S, Bargmann CI, Garriga G. Multiple Wnts and frizzled receptors regulate anteriorly directed cell and growth cone migrations in Caenorhabditis elegans. Dev Cell 2006, 10:367-377.
69. Hilliard MA, Bargmann CI. Wnt signals and frizzled activity orient anterior-posterior axon outgrowth in C. elegans. Dev Cell 2006, 10:379-390.
70. Whangbo J, Kenyon C. A Wnt signaling system that specifies two patterns of cell migration in C. elegans. Mol Cell 1999, 4:851-858.
71. Herman MA, Vassilieva LL, Horvitz HR, Shaw JE, Herman RK. The C. elegans gene lin-44, which controls the polarity of certain asymmetric cell divisions, encodes a Wnt protein and acts cell nonautonomously. Cell 1995, 83:101-110.
72. Kolotuev I, Apaydin A, Labouesse M. Secretion of Hedgehog-related peptides and WNT during Caenorhabditis elegans development. Traffic 2009, 10: 803-810.
73. Harris JE, Crofton HD. Structure and function the nematodes: internal pressure and cuticular structure in Ascaris. J Exp Biol. 1957, 34:116-130.
74. Pujol N, Cypowyj S, Ziegler K, Millet A, Astrain A, Goncharov A, Jin Y, Chisholm AD, Ewbank JJ. Distinct innate immune responses to infection and wounding in the C. elegans epidermis. Curr Biol 2008, 18: 481-489.
75. Park SJ, Goodman MB, Pruitt BL. Analysis of nematode mechanics by piezoresistive displacement clamp. Proc Natl Acad Sci USA 2007, 104:17376-17381.
76. Petzold BC, Park SJ, Ponce P, Roozeboom C, Powell C, Goodman MB, Pruitt BL. Caenorhabditis elegans body mechanics are regulated by body wall muscle tone. Biophys J 2011, 100:1977-1985.
77. Van De Velde MC, Coomans A. A putative new hydrostatic skeletal function for the epidermis in Monhysterids (Nematoda). Tissue Cell 1989, 21:525-533.
78. Page AP, Johnstone IL. The cuticle (2007), WormBook, ed. The C. elegans Research Community, WormBook, doi:10.1895/wormbook.1.138.
79. Fujimoto D, Kanaya S. Cuticlin: a noncollagen structural protein from Ascaris cuticle. Arch Biochem Biophys 1973, 157:1-6.
80. Sapio MR, Hilliard MA, Cermola M, Favre R, Bazzicalupo P. The Zona Pellucida domain containing proteins, CUT-1, CUT-3 and CUT-5, play essential roles in the development of the larval alae in Caenorhabditis elegans. Dev Biol 2005, 282:231-245.
81. Sebastiano M, Lassandro F, Bazzicalupo P. cut-1, a Caenorhabditis elegans gene coding for a dauer-specific noncollagenous component of the cuticle. Dev Biol 1991, 146:519-530.
82. Zhang Y, Foster JM, Nelson LS, Ma D, Carlow CK. The chitin synthase genes chs-1 and chs-2 are essential for C. elegans development and responsible for chitin deposition in the eggshell and pharynx, respectively. Dev Biol 2005, 285:330-339.
83. Edens WA, Sharling L, Cheng G, Shapira R, Kinkade JM, Lee T, Edens HA, Tang X, Sullards C, Flaherty DB, et al. Tyrosine cross-linking of extracellular matrix is catalyzed by Duox, a multidomain oxidase/peroxidase with homology to the phagocyte oxidase subunit gp91phox. J Cell Biol 2001, 154: 879-891.
84. Thein MC, Winter AD, Stepek G, McCormack G, Stapleton G, Johnstone IL, Page AP. Combined extracellular matrix cross-linking activity of the peroxidase MLT-7 and the dual oxidase BLI-3 is critical for post-embryonic viability in Caenorhabditis elegans. J Biol Chem 2009, 284:17549-17563.
85. Johnstone IL. Cuticle collagen genes. Expression in Caenorhabditis elegans. Trends Genet 2000, 16: 21-27.
86. McMahon L, Muriel JM, Roberts B, Quinn M, Johnstone IL. Two sets of interacting collagens form functionally distinct substructures within a Caenorhabditis elegans extracellular matrix. Mol Biol Cell 2003, 14: 1366-1378.
87. Gilleard JS, McGhee JD. Activation of hypodermal differentiation in the Caenorhabditis elegans embryo by GATA transcription factors ELT-1 and ELT-3. Mol Cell Biol 2001, 21:2533-2544.
88. Kouns NA, Nakielna J, Behensky F, Krause MW, Kostrouch Z, Kostrouchova M. NHR-23 dependent collagen and hedgehog-related genes required for molting. Biochem Biophys Res Commun 2011, 413: 515-520.
89. Gissendanner CR, Crossgrove K, Kraus KA, Maina CV, Sluder AE. Expression and function of conserved nuclear receptor genes in Caenorhabditis elegans. Dev Biol 2004, 266:399-416.
90. Cai L, Phong BL, Fisher AL, Wang Z. Regulation of fertility, survival, and cuticle collagen function by the Caenorhabditis elegans eaf-1 and ell-1 genes. J Biol Chem 2011, 286:35915-35921.
91. Liu Z, Kirch S, Ambros V. The Caenorhabditis elegans heterochronic gene pathway controls stage-specific transcription of collagen genes. Development 1995, 121:2471-2478.
92. Rougvie AE, Ambros V. The heterochronic gene lin-29 encodes a zinc finger protein that controls a terminal differentiation event in Caenorhabditis elegans. Development 1995, 121:2491-2500.
93. Blaxter M, Bird D. Parasitic nematodes. In: Riddle DL, Blumenthal T, Meyer BJ, Priess JR, eds. C. elegans II. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 1997.
94. Peixoto CA, De Souza W. Freeze-fracture and deep-etched view of the cuticle of Caenorhabditis elegans. Tissue Cell 1995, 27:561-568.
95. Grenache DG, Caldicott I, Albert PS, Riddle DL, Politz SM. Environmental induction and genetic control of surface antigen switching in the nematode Caenorhabditis elegans. Proc Natl Acad Sci USA 1996, 93:12388-12393.
96. Politz SM, Philipp M, Estevez M, O'Brien PJ, Chin KJ. Genes that can be mutated to unmask hidden antigenic determinants in the cuticle of the nematode Caenorhabditis elegans. Proc Natl Acad Sci USA 1990, 87:2901-2905.
97. Link CD, Silverman MA, Breen M, Watt KE, Dames SA. Characterization of Caenorhabditis elegans lectin-binding mutants. Genetics 1992, 131:867-881.
98. Gravato-Nobre MJ, Nicholas HR, Nijland R, O'Rourke D, Whittington DE, Yook KJ, Hodgkin J. Multiple genes affect sensitivity of Caenorhabditis elegans to the bacterial pathogen Microbacterium nematophilum. Genetics 2005, 171:1033-1045.
99. Darby C, Chakraborti A, Politz SM, Daniels CC, Tan L, Drace K. Caenorhabditis elegans mutants resistant to attachment of Yersinia biofilms. Genetics 2007, 176:221-230.
100. Drace K, McLaughlin S, Darby C. Caenorhabditis elegans BAH-1 is a DUF23 protein expressed in seam cells and required for microbial biofilm binding to the cuticle. PLoS One 2009, 4:e6741.
101. Gravato-Nobre MJ, Stroud D, O'Rourke D, Darby C, Hodgkin J. Glycosylation genes expressed in seam cells determine complex surface properties and bacterial adhesion to the cuticle of Caenorhabditis elegans. Genetics 2011, 187:141-155.
102. Plenefisch J, Xiao H, Mei B, Geng J, Komuniecki PR, Komuniecki R. Secretion of a novel class of iFABPs in nematodes: coordinate use of the Ascaris/Caenorhabditis model systems. Mol Biochem Parasitol 2000, 105:223-236.
103. Mancuso VP, Parry JM, Storer L, Poggioli C, Nguyen KC, Hall DH, Sundaram MV. Extracellular leucine-rich repeat proteins are required to organize the apical extracellular matrix and maintain epithelial junction integrity in C. elegans. Development 2012, 139:979-990.
104. Roberts B, Clucas C, Johnstone IL. Loss of SEC-23 in Caenorhabditis elegans causes defects in oogenesis, morphogenesis, and extracellular matrix secretion. Mol Biol Cell 2003, 14:4414-4426.
105. White JG. The anatomy. In: Wood WB, ed. The Nematode Caenorhabditis elegans. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 1988, 81-122.
106. Liegeois S, Benedetto A, Garnier JM, Schwab Y, Labouesse M. The V0-ATPase mediates apical secretion of exosomes containing Hedgehog-related proteins in Caenorhabditis elegans. J Cell Biol 2006, 173: 949-961.
107. Liegeois S, Benedetto A, Michaux G, Belliard G, Labouesse M. Genes required for osmoregulation and apical secretion in Caenorhabditis elegans. Genetics 2007, 175:709-724.
108. Frand AR, Russel S, Ruvkun G. Functional genomic analysis of C. elegans molting. PLoS Biol 2005, 3:e312.
109. Magner DB, Antebi A. Caenorhabditis elegans nuclear receptors: insights into life traits. Trends Endocrinol Metab 2008, 19:153-160.
110. Kurzchalia TV, Ward S. Why do worms need cholesterol? Nat Cell Biol 2003, 5:684-688.
111. Yochem J, Tuck S, Greenwald I, Han M. A gp330/megalin-related protein is required in the major epidermis of Caenorhabditis elegans for completion of molting. Development 1999, 126:597-606.
112. Grigorenko AP, Moliaka YK, Soto MC, Mello CC, Rogaev EI. The Caenorhabditis elegans IMPAS gene, imp-2, is essential for development and is functionally distinct from related presenilins. Proc Natl Acad Sci USA 2004, 101:14955-14960.
113. Roudier N, Lefebvre C, Legouis R. CeVPS-27 is an endosomal protein required for the molting and the endocytic trafficking of the low-density lipoprotein receptor-related protein 1 in Caenorhabditis elegans. Traffic 2005, 6:695-705.
114. Monsalve GC, Van Buskirk C, Frand AR. LIN-42/PERIOD controls cyclical and developmental progression of C. elegans molts. Curr Biol 2011, 21: 2033-2045.
115. Broday L, Hauser CA, Kolotuev I, Ronai Z. Muscle-epidermis interactions affect exoskeleton patterning in Caenorhabditis elegans. Dev Dyn 2007, 236: 3129-3136.
116. Ruaud AF, Bessereau JL. Activation of nicotinic receptors uncouples a developmental timer from the molting timer in C. elegans. Development 2006, 133: 2211-2222.
117. Ruaud AF, Bessereau JL. The P-type ATPase CATP-1 is a novel regulator of C. elegans developmental timing that acts independently of its predicted pump function. Development 2007, 134:867-879.
118. Stenvall J, Fierro-Gonzalez JC, Swoboda P, Saamarthy K, Cheng Q, Cacho-Valadez B, Arner ES, Persson OP, Miranda-Vizuete A, Tuck S. Selenoprotein TRXR-1 and GSR-1 are essential for removal of old cuticle during molting in Caenorhabditis elegans. Proc Natl Acad Sci USA 2011, 108:1064-1069.
119. Craig H, Isaac RE, Brooks DR. Unravelling the moulting degradome: new opportunities for chemotherapy? Trends Parasitol 2007, 23:248-253.
120. Hashmi S, Zhang J, Oksov Y, Lustigman S. The Caenorhabditis elegans cathepsin Z-like cysteine protease, Ce-CPZ-1, has a multifunctional role during the worms' development. J Biol Chem 2004, 279: 6035-6045.
121. Page AP, McCormack G, Birnie AJ. Biosynthesis and enzymology of the Caenorhabditis elegans cuticle: identification and characterization of a novel serine protease inhibitor. Int J Parasitol 2006, 36:681-689.
122. Davis MW, Birnie AJ, Chan AC, Page AP, Jorgensen EM. A conserved metalloprotease mediates ecdysis in Caenorhabditis elegans. Development 2004, 131:6001-6008.
123. Stepek G, McCormack G, Birnie AJ, Page AP. The astacin metalloprotease moulting enzyme NAS-36 is required for normal cuticle ecdysis in free-living and parasitic nematodes. Parasitology 2011, 138: 237-248.
124. Meli VS, Osuna B, Ruvkun G, Frand AR. MLT-10 defines a family of DUF644 and proline-rich repeat proteins involved in the molting cycle of Caenorhabditis elegans. Mol Biol Cell 2010, 21:1648-1661.
125. Aspock G, Kagoshima H, Niklaus G, Burglin TR. Caenorhabditis elegans has scores of hedgehog-related genes: sequence and expression analysis. Genome Res 1999, 9:909-923.
126. Hao L, Johnsen R, Lauter G, Baillie D, Burglin TR. Comprehensive analysis of gene expression patterns of hedgehog-related genes. BMC Genomics 2006, 7:280.
127. Hao L, Mukherjee K, Liegeois S, Baillie D, Labouesse M, Burglin TR. The hedgehog-related gene qua-1 is required for molting in Caenorhabditis elegans. Dev Dyn 2006, 235:1469-1481.
128. Dejima K, Murata D, Mizuguchi S, Nomura KH, Izumikawa T, Kitagawa H, Gengyo-Ando K, Yoshina S, Ichimiya T, Nishihara S, et al. Two Golgi-resident 3′-Phosphoadenosine 5′-phosphosulfate transporters play distinct roles in heparan sulfate modifications and embryonic and larval development in Caenorhabditis elegans. J Biol Chem 2010, 285:24717-24728.
129. Zugasti O, Rajan J, Kuwabara PE. The function and expansion of the Patched- and Hedgehog-related homologs in C. elegans. Genome Res 2005, 15: 1402-1410.
130. Hornsten A, Lieberthal J, Fadia S, Malins R, Ha L, Xu X, Daigle I, Markowitz M, O'Connor G, Plasterk R, et al. APL-1, a Caenorhabditis elegans protein related to the human beta-amyloid precursor protein, is essential for viability. Proc Natl Acad Sci USA 2007, 104:1971-1976.
131. Niwa R, Zhou F, Li C, Slack FJ. The expression of the Alzheimer's amyloid precursor protein-like gene is regulated by developmental timing microRNAs and their targets in Caenorhabditis elegans. Dev Biol 2008, 315:418-425.
132. Van Wynsberghe PM, Kai ZS, Massirer KB, Burton VH, Yeo GW, Pasquinelli AE. LIN-28 co-transcriptionally binds primary let-7 to regulate miRNA maturation in Caenorhabditis elegans. Nat Struct Mol Biol 2011, 18:302-308.
133. Hayes GD, Frand AR, Ruvkun G. The mir-84 and let-7 paralogous microRNA genes of Caenorhabditis elegans direct the cessation of molting via the conserved nuclear hormone receptors NHR-23 and NHR-25. Development 2006, 133:4631-4641.
134. Jeon M, Gardner HF, Miller EA, Deshler J, Rougvie AE. Similarity of the C. elegans developmental timing protein LIN-42 to circadian rhythm proteins. Science 1999, 286:1141-1146.
135. Hammell CM, Karp X, Ambros V. A feedback circuit involving let-7-family miRNAs and DAF-12 integrates environmental signals and developmental timing in Caenorhabditis elegans. Proc Natl Acad Sci USA 2009, 106:18668-18673.
136. Bethke A, Fielenbach N, Wang Z, Mangelsdorf DJ, Antebi A. Nuclear hormone receptor regulation of microRNAs controls developmental progression. Science 2009, 324:95-98.
137. Kostrouchova M, Krause M, Kostrouch Z, Rall JE. CHR3: a Caenorhabditis elegans orphan nuclear hormone receptor required for proper epidermal development and molting. Development 1998, 125: 1617-1626.
138. Russel S, Frand AR, Ruvkun G. Regulation of the C. elegans molt by pqn-47. Dev Biol 2011, 360:297-309.
139. Altun ZF, Chen B, Wang ZW, Hall DH. High resolution map of Caenorhabditis elegans gap junction proteins. Dev Dyn 2009, 238:1936-1950.
140. Van Buskirk C, Sternberg PW. Epidermal growth factor signaling induces behavioral quiescence in Caenorhabditis elegans. Nat Neurosci 2007, 10: 1300-1307.
141. Singh K, Chao MY, Somers GA, Komatsu H, Corkins ME, Larkins-Ford J, Tucey T, Dionne HM, Walsh MB, Beaumont EK, et al. C. elegans Notch signaling regulates adult chemosensory response and larval molting quiescence. Curr Biol 2011, 21:825-834.
142. Zaidel-Bar R, Miller S, Kaminsky R, Broday L. Molting-specific downregulation of C. elegans body-wall muscle attachment sites: the role of RNF-5 E3 ligase. Biochem Biophys Res Commun 2010, 395: 509-514.
143. Albert PS, Riddle DL. Developmental alterations in sensory neuroanatomy of the Caenorhabditis elegans dauer larva. J Comp Neurol 1983, 219:461-481.
144. Melendez A, Talloczy Z, Seaman M, Eskelinen EL, Hall DH, Levine B. Autophagy genes are essential for dauer development and life-span extension in C. elegans. Science 2003, 301:1387-1391.
145. Cox GN, Staprans S, Edgar RS. The cuticle of Caenorhabditis elegans. II. Stage-specific changes in ultrastructure and protein composition during postembryonic development. Dev Biol 1981, 86:456-470.
146. Muriel JM, Brannan M, Taylor K, Johnstone IL, Lithgow GJ, Tuckwell D. M142.2 (cut-6), a novel Caenorhabditis elegans matrix gene important for dauer body shape. Dev Biol 2003, 260:339-351.
147. Mak HY, Ruvkun G. Intercellular signaling of reproductive development by the C. elegans DAF-9 cytochrome P450. Development 2004, 131: 1777-1786.
148. Gerisch B, Antebi A. Hormonal signals produced by DAF-9/cytochrome P450 regulate C. elegans dauer diapause in response to environmental cues. Development 2004, 131:1765-1776.
149. Antebi A. Nuclear hormone receptors in C. elegans (2006), WormBook, ed. The C. elegans Research Community, WormBook doi:10.1895/wormbook.1.64.1.
150. Hristova M, Birse D, Hong Y, Ambros V. The Caenorhabditis elegans heterochronic regulator LIN-14 is a novel transcription factor that controls the developmental timing of transcription from the insulin/insulin-like growth factor gene ins-33 by direct DNA binding. Mol Cell Biol 2005, 25:11059-11072.
151. Moribe H, Yochem J, Yamada H, Tabuse Y, Fujimoto T, Mekada E. Tetraspanin protein (TSP-15) is required for epidermal integrity in Caenorhabditis elegans. J Cell Sci 2004, 117:5209-5220.
152. Rand JB, Johnson CD. Genetic pharmacology: interactions between drugs and gene products in Caenorhabditis elegans. Methods Cell Biol 1995; 48:187-204.
153. Kage-Nakadai E, Kobuna H, Kimura M, Gengyo-Ando K, Inoue T, Arai H, Mitani S. Two very long chain fatty acid acyl-CoA synthetase genes, acs-20 and acs-22, have roles in the cuticle surface barrier in Caenorhabditis elegans. PLoS One 2010, 5:e8857.
154. Partridge FA, Tearle AW, Gravato-Nobre MJ, Schafer WR, Hodgkin J. The C. elegans glycosyltransferase BUS-8 has two distinct and essential roles in epidermal morphogenesis. Dev Biol 2008, 317:549-559.
155. Yook K, Hodgkin J. Mos1 mutagenesis reveals a diversity of mechanisms affecting response of Caenorhabditis elegans to the bacterial pathogen Microbacterium nematophilum. Genetics 2007, 175:681-697.
156. Loer CM, Davidson B, McKerrow J. A phenylalanine hydroxylase gene from the nematode C. elegans is expressed in the hypodermis. J Neurogenet 1999, 13:157-180.
157. Calvo AC, Pey AL, Ying M, Loer CM, Martinez A. Anabolic function of phenylalanine hydroxylase in Caenorhabditis elegans. FASEB J 2008, 22: 3046-3058.
158. Coomans A, Verschuren D, Vanderhaeghen R. The demanian system, traumatic insemination and reproductive strategy in Oncholaimus oxyuris Ditlevsen (Nematoda, Oncholaimina). Zool Scripta 2005, 17: 15-23.
159. Hodgkin J, Kuwabara PE, Corneliussen B. A novel bacterial pathogen, Microbacterium nematophilum, induces morphological change in the nematode C. elegans. Curr Biol 2000, 10:1615-1618.
160. Jansson HB. Adhesion of conidia of Drechmeria coniospora to Caenorhabditis elegans wild type and mutants. J Nematol 1994, 26:430-435.
161. Couillault C, Pujol N, Reboul J, Sabatier L, Guichou JF, Kohara Y, Ewbank JJ. TLR-independent control of innate immunity in Caenorhabditis elegans by the TIR domain adaptor protein TIR-1, an ortholog of human SARM. Nat Immunol 2004, 5:488-494.
162. Ziegler K, Kurz CL, Cypowyj S, Couillault C, Pophillat M, Pujol N, Ewbank JJ. Antifungal innate immunity in C. elegans: PKCδ links G protein signaling and a conserved p38 MAPK cascade. Cell Host Microbe 2009, 5:341-352.
163. Pujol N, Zugasti O, Wong D, Couillault C, Kurz CL, Schulenburg H, Ewbank JJ. Anti-fungal innate immunity in C. elegans is enhanced by evolutionary diversification of antimicrobial peptides. PLoS Pathog 2008, 4:e1000105.
164. Zugasti O, Ewbank JJ. Neuroimmune regulation of antimicrobial peptide expression by a noncanonical TGF-beta signaling pathway in Caenorhabditis elegans epidermis. Nat Immunol 2009, 10:249-256.
165. Xu S, Chisholm AD. A Gαq-Ca(2+) signaling pathway promotes actin-mediated epidermal wound closure in C. elegans. Curr Biol 2011, 21:1960-1967.
166. O'Rourke D, Baban D, Demidova M, Mott R, Hodgkin J. Genomic clusters, putative pathogen recognition molecules, and antimicrobial genes are induced by infection of C. elegans with M. nematophilum. Genome Res 2006, 16:1005-1016.
167. Nicholas HR, Hodgkin J. The ERK MAP kinase cascade mediates tail swelling and a protective response to rectal infection in C. elegans. Curr Biol 2004, 14: 1256-1261.
168. Rohlfing AK, Miteva Y, Hannenhalli S, Lamitina T. Genetic and physiological activation of osmosensitive gene expression mimics transcriptional signatures of pathogen infection in C. elegans. PLoS One 2010, 5:e9010.
169. Dierking K, Polanowska J, Omi S, Engelmann I, Gut M, Lembo F, Ewbank JJ, Pujol N. Unusual regulation of a STAT protein by an SLC6 family transporter in C. elegans epidermal innate immunity. Cell Host Microbe 2011, 9:425-435.
170. Tong A, Lynn G, Ngo V, Wong D, Moseley SL, Ewbank JJ, Goncharov A, Wu YC, Pujol N, Chisholm AD. Negative regulation of Caenorhabditis elegans epidermal damage responses by death-associated protein kinase. Proc Natl Acad Sci USA 2009, 106: 1457-1461.
171. Van Epps H, Dai Y, Qi Y, Goncharov A, Jin Y. Nuclear pre-mRNA 3'-end processing regulates synapse and axon development in C. elegans. Development 2010, 137:2237-2250.
172. Lamitina ST, Morrison R, Moeckel GW, Strange K. Adaptation of the nematode Caenorhabditis elegans to extreme osmotic stress. Am J Physiol Cell Physiol 2004, 286:C785-C791.
173. Choe KP, Strange K. Evolutionarily conserved WNK and Ste20 kinases are essential for acute volume recovery and survival after hypertonic shrinkage in Caenorhabditis elegans. Am J Physiol Cell Physiol 2007, 293:C915-C927.
174. Petalcorin MI, Oka T, Koga M, Ogura K, Wada Y, Ohshima Y, Futai M. Disruption of clh-1, a chloride channel gene, results in a wider body of Caenorhabditis elegans. J Mol Biol 1999, 294:347-355.
175. Solomon A, Bandhakavi S, Jabbar S, Shah R, Beitel GJ, Morimoto RI. Caenorhabditis elegans OSR-1 regulates behavioral and physiological responses to hyperosmotic environments. Genetics 2004, 167:161-170.
176. Wheeler JM, Thomas JH. Identification of a novel gene family involved in osmotic stress response in Caenorhabditis elegans. Genetics 2006, 174: 1327-1336.
177. Rohlfing AK, Miteva Y, Moronetti L, He L, Lamitina T. The Caenorhabditis elegans mucin-like protein OSM-8 negatively regulates osmosensitive physiology via the transmembrane protein PTR-23. PLoS Genet 2011, 7:e1001267.
178. Soloviev A, Gallagher J, Marnef A, Kuwabara PE. C. elegans patched-3 is an essential gene implicated in osmoregulation and requiring an intact permease transporter domain. Dev Biol 2011, 351:242-253.
179. Mizuno T, Fujiki K, Sasakawa A, Hisamoto N, Matsumoto K. Role of the Caenorhabditis elegans Shc adaptor protein in the c-Jun N-terminal kinase signaling pathway. Mol Cell Biol 2008, 28: 7041-7049.
180. Budde MW, Roth MB. The response of Caenorhabditis elegans to hydrogen sulfide and hydrogen cyanide. Genetics 2011, 189:521-532.
181. Chen C, Samuel TK, Krause M, Dailey HA, Hamza I. Heme utilization in the Caenorhabditis elegans hypodermal cells is facilitated by heme responsive gene-2. J Biol Chem 2012, 287:9601-9612.
182. O'Rourke EJ, Soukas AA, Carr CE, Ruvkun G. C. elegans major fats are stored in vesicles distinct from lysosome-related organelles. Cell Metab 2009, 10: 430-435.
183. Hellerer T, Axang C, Brackmann C, Hillertz P, Pilon M, Enejder A. Monitoring of lipid storage in Caenorhabditis elegans using coherent anti-Stokes Raman scattering (CARS) microscopy. Proc Natl Acad Sci USA 2007, 104:14658-14663.
184. Narbonne P, Roy R. Caenorhabditis elegans dauers need LKB1/AMPK to ration lipid reserves and ensure long-term survival. Nature 2009, 457:210-214.
185. Robertson AMG, Thomson JN. Morphology of programmed cell death in the ventral nerve cord of Caenorhabditis elegans larvae. J Embryol Exp Morph 1982, 67:89-100.
186. Hall DH, Gu G, Garcia-Anoveros J, Gong L, Chalfie M, Driscoll M. Neuropathology of degenerative cell death in Caenorhabditis elegans. J Neurosci 1997, 17:1033-1045.
187. Chisholm AD, Hardin J. Epidermal morphogenesis, WormBook, ed. The C. elegans Research Community, WormBook, doi:10.1895/wormbook.1.35.1.
188. Chung S, Gumienny TL, Hengartner MO, Driscoll M. A common set of engulfment genes mediates removal of both apoptotic and necrotic cell corpses in C. elegans. Nat Cell Biol 2000, 2:931-937.
189. Wu Z, Ghosh-Roy A, Yanik MF, Zhang JZ, Jin Y, Chisholm AD. Caenorhabditis elegans neuronal regeneration is influenced by life stage, ephrin signaling, and synaptic branching. Proc Natl Acad Sci USA 2007, 104:15132-15137.
190. Hammarlund M, Jorgensen EM, Bastiani MJ. Axons break in animals lacking β-spectrin. J Cell Biol 2007, 176:269-275.
191. MacDonald JM, Beach MG, Porpiglia E, Sheehan AE, Watts RJ, Freeman MR. The Drosophila cell corpse engulfment receptor Draper mediates glial clearance of severed axons. Neuron 2006, 50:869-881.
192. Maurer CW, Chiorazzi M, Shaham S. Timing of the onset of a developmental cell death is controlled by transcriptional induction of the C. elegans ced-3 caspase-encoding gene. Development 2007, 134: 1357-1368.
193. Sommer RJ, Eizinger A, Lee KZ, Jungblut B, Bubeck A, Schlak I. The Pristionchus HOX gene Ppa-lin-39 inhibits programmed cell death to specify the vulva equivalence group and is not required during vulval induction. Development 1998, 125: 3865-3873.
194. Galvin BD, Kim S, Horvitz HR. Caenorhabditis elegans genes required for the engulfment of apoptotic corpses function in the cytotoxic cell deaths induced by mutations in lin-24 and lin-33. Genetics 2008, 179: 403-417.
195. Joshi P, Eisenmann DM. The Caenorhabditis elegans pvl-5 gene protects hypodermal cells from ced-3-dependent, ced-4-independent cell death. Genetics 2004, 167:673-685.
196. Aladzsity I, Toth ML, Sigmond T, Szabo E, Bicsak B, Barna J, Regos A, Orosz L, Kovacs AL, Vellai T. Autophagy genes unc-51 and bec-1 are required for normal cell size in Caenorhabditis elegans. Genetics 2007, 177:655-660.
197. Borsos E, Erdelyi P, Vellai T. Autophagy and apoptosis are redundantly required for C. elegans embryogenesis. Autophagy 2011, 7:557-559.
198. Cinar HN, Chisholm AD. Genetic analysis of the Caenorhabditis elegans pax-6 locus: roles of paired domain-containing and nonpaired domain-containing isoforms. Genetics 2004, 168:1307-1322.
199. Emtage L, Gu G, Hartwieg E, Chalfie M. Extracellular proteins organize the mechanosensory channel complex in C. elegans touch receptor neurons. Neuron 2004, 44:795-807.
200. Vogel BE, Hedgecock EM. Hemicentin, a conserved extracellular member of the immunoglobulin superfamily, organizes epithelial and other cell attachments into oriented line-shaped junctions. Development 2001, 128:883-894.
201. Smith CJ, Watson JD, Spencer WC, O'Brien T, Cha B, Albeg A, Treinin M, Miller DM 3rd. Time-lapse imaging and cell-specific expression profiling reveal dynamic branching and molecular determinants of a multi-dendritic nociceptor in C. elegans. Dev Biol 2010, 345:18-33.
202. Albeg A, Smith CJ, Chatzigeorgiou M, Feitelson DG, Hall DH, Schafer WR, Miller DM 3rd, Treinin M. C. elegans multi-dendritic sensory neurons: morphology and function. Mol Cell Neurosci 2011, 46: 308-317.
203. Rosenbluth J. Ultrastructure of somatic muscle cells in Ascaris lumbricoides. II. Intermuscular junctions, neuromuscular junctions, and glycogen stores. J Cell Biol 1965, 26:579-591.
204. Wright KA. Some neuron-hypodermis relationships in the parasitic nematode Trichuris myocastoris Enigk. J Nematol 1970, 2:152-160.
205. White JG, Southgate E, Thomson JN, Brenner S. The structure of the nervous system of the nematode Caenorhabditis elegans. Phil Trans R Soc Lond B Biol Sci 1986, 314:1-340.
206. Stawicki TM, Zhou K, Yochem J, Chen L, Jin Y. TRPM channels modulate epileptic-like convulsions via systemic ion homeostasis. Curr Biol 2011, 21: 883-888.
207. Searcy DG, Kisiel MJ, Zuckerman BM. Age-related increase of cuticle permeability in the nematode Caenorhabditis briggsae. Exp Aging Res 1976, 2: 293-301.
208. Himmelhoch S, Zuckerman BM. Caenorhabditis briggsae: aging and the structural turnover of the outer cuticle surface and the intestine. Exp Parasitol 1978, 45:208-214.
209. Kisiel MJ, Castillo JM, Zuckerman LS, Zuckerman BM. Studies on ageing in Turbatrix aceti. Mech Ageing Dev 1975, 4:81-88.
210. Herndon LA, Schmeissner PJ, Dudaronek JM, Brown PA, Listner KM, Sakano Y, Paupard MC, Hall DH, Driscoll M. Stochastic and genetic factors influence tissue-specific decline in ageing C. elegans. Nature 2002, 419:808-814.
211. Luo S, Kleemann GA, Ashraf JM, Shaw WM, Murphy CT. TGF-β and insulin signaling regulate reproductive aging via oocyte and germline quality maintenance. Cell 2010, 143:299-312.
212. Budovskaya YV, Wu K, Southworth LK, Jiang M, Tedesco P, Johnson TE, Kim SK. An elt-3/elt-5/elt-6 GATA transcription circuit guides aging in C. elegans. Cell 2008, 134:291-303.
213. Qadota H, Inoue M, Hikita T, Koppen M, Hardin JD, Amano M, Moerman DG, Kaibuchi K. Establishment of a tissue-specific RNAi system in C. elegans. Gene 2007, 400:166-173.
214. Spencer WC, Zeller G, Watson JD, Henz SR, Watkins KL, McWhirter RD, Petersen S, Sreedharan VT, Widmer C, Jo J, et al. A spatial and temporal map of C. elegans gene expression. Genome Res 2011, 21: 325-341.