Genetic interaction between Caenorhabditis elegans teneurin ten-1 and prolyl 4-hydroxylase phy-1 and their function in collagen IV-mediated basement membrane integrity during late elongation of the embryo

Molecular Biology of the Cell

Volumn 22, Issue 18, 2011, Pages 3331-3343

  Topf, Ulrike ^a   Chiquet Ehrismann, Ruth ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 4; GENE PRODUCT; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; TENEURIN; UNCLASSIFIED DRUG;

ARTICLE; BASEMENT MEMBRANE; CAENORHABDITIS ELEGANS; CELL MIGRATION; EMBRYO; EMBRYO DEVELOPMENT; EPIDERMIS; GENE; GENE DELETION; GENE INTERACTION; GENOME; GONAD DEVELOPMENT; LETHALITY; MECHANICAL STRESS; MEMBRANE DAMAGE; MORPHOGENESIS; MUSCLE CELL; MUSCLE CONTRACTION; MUTANT; NONHUMAN; PHY 1 GENE; PHYLOGENY; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DOMAIN; PROTEIN FAMILY; RNA INTERFERENCE; TEN 1 GENE;

ANIMALS; BASEMENT MEMBRANE; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; COLLAGEN TYPE IV; EPIDERMIS; EPISTASIS, GENETIC; GENE KNOCKDOWN TECHNIQUES; GENES, LETHAL; LARVA; MEMBRANE PROTEINS; MUSCLES; PROCOLLAGEN-PROLINE DIOXYGENASE; RNA INTERFERENCE;

CAENORHABDITIS ELEGANS;

EID: 80052859562     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E10-10-0853     Document Type: Article

References (50)

1. Albertson DG, Thomson JN (1976). The pharynx of Caenorhabditis elegans. Philos Trans R Soc Lond B Biol Sci 275, 299-325.
2. Baumgartner S, Martin D, Hagios C, Chiquet-Ehrismann R (1994). Tenm, a Drosophila gene related to tenascin, is a new pair-rule gene. EMBO J 13, 3728-3740.
3. Ben-Zur T, Feige E, Motro B, Wides R (2000). The mammalian Odz gene family: homologs of a Drosophila pair-rule gene with expression implying distinct yet overlapping developmental roles. Dev Biol 217, 107-120.
4. Bercher M, Wahl J, Vogel BE, Lu C, Hedgecock EM, Hall DH, Plenefisch JD (2001). mua-3, a gene required for mechanical tissue integrity in Caenorhabditis elegans, encodes a novel transmembrane protein of ephithelial attachment complexes. J Cell Biol 154, 415-426.
5. Bosher JM, Hahn BS, Legouis R, Sookhareea S, Weimer RM, Gansmuller A, Chisholm AD, Rose AM, Bessereau JL, Labouesse M (2003). The Caenorhabditis elegans vab-10 spectraplakin isoforms protect the epidermis against internal and external forces. J Cell Biol 161, 757-768.
6. Brown NH (2000). Cell-cell adhesion via the ECM: integrin genetics in fly and worm. Matrix Biol 19, 191-201.
7. Brenner S (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
8. Chin-Sang ID, Chisholm AD (2000). Form of the worm: genetics of epidermal morphogenesis in C. elegans. Trends Genet 16, 544-551.
9. Clopper C, Pearson S (1934). The use of confidence or fiducial limits illustrated in the case of the binomial. Biometrika 26, 404-413.
10. Ding M, King RS, Berry EC, Wang Y, Hardin J, Chisholm AD (2008). 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 3, e3346.
11. Drabikowski K, Trzebiatowska A, Chiquet-Ehrismann R (2005). ten-1, an essential gene for germ cell development, epidermal morphogenesis, gonad migration, and neuronal pathfinding in Caenorhabditis elegans. Dev Biol 282, 27-38.
12. Fascetti N, Baumgartner S (2002). Expression of Drosophila Ten-a, a dimeric receptor during embryonic development. Mech Dev 114, 197-200.
13. Feng K, Zhou XH, Oohashi T, Morgelin M, Lustig A, Hirakawa S, Ninomiya Y, Engel J, Rauch U, Fassler R (2002). All four members of the Ten-m/Odz family of transmembrane proteins form dimers. J Biol Chem 277, 26128-26135.
14. Fessler JH, Fessler LI (1978). Biosynthesis of procollagen. Annu Rev Biochem 47, 129-162.
15. Francis R, Waterston RH (1991). Muscle cell attachment in Caenorhabditis elegans. J Cell Biol 114, 465-479.
16. Friedman L, Higgin JJ, Moulder G, Barstead R, Raines RT, Kimble J (2000). Prolyl 4-hydroxylase is required for viability and morphogenesis in Caenorhabditis elegans. Proc Natl Acad Sci USA 97, 4736-4741.
17. Graham PL, Johnson JJ, Wang S, Sibley MH, Gupta MC, Kramer JM (1997). 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 137, 1171-1183.
18. Gupta MC, Graham PL, Kramer JM (1997). Characterization of alpha1(IV) collagen mutations in Caenorhabditis elegans and the effects of alpha1 and alpha2(IV) mutations on type IV collagen distribution. J Cell Biol 137, 1185-1196.
19. Hill KL, Harfe BD, Dobbins CA, L'Hernault SW (2000). dpy-18 encodes an alpha-subunit of prolyl-4-hydroxylase in Caenorhabditis elegans. Genetics 155, 1139-1148.
20. Holster T, Pakkanen O, Soininen R, Sormunen R, Nokelainen M, Kivirikko KI, Myllyharju J (2007). Loss of assembly of the main basement membrane collagen, type IV, but not fibril-forming collagens and embryonic death in collagen prolyl 4-hydroxylase I null mice. J Biol Chem 282, 2512-2519.
21. Hresko MC, Schriefer LA, Shrimankar P, Waterston RH (1999). Myotactin, a novel hypodermal protein involved in muscle-cell adhesion in Caenorhabditis elegans. J Cell Biol 146, 659-672.
22. Hresko MC, Williams BD, Waterston RH (1994). Assembly of body wall muscle and muscle cell attachment structures in Caenorhabditis elegans. J Cell Biol 124, 491-506.
23. Kenzelmann-Broz D, Tucker RP, Leachman NT, Chiquet-Ehrismann R (2010). The expression of teneurin-4 in the avian embryo: potential roles in patterning of the limb and nervous system. Int J Dev Biol 54, 1509-1516.
24. Keskiaho K, Kukkola L, Page AP, Winter AD, Vuoristo J, Sormunen R, Nissi R, Riihimaa P, Myllyharju J (2008). Characterization of a novel Caenorhabditis elegans prolyl 4-hydroxylase with a unique substrate specificity and restricted expression in the pharynx and excretory duct. J Biol Chem 283, 10679-10689.
25. Levine A, Bashan-Ahrend A, Budai-Hadrian O, Gartenberg D, Menasherow S, Wides R (1994). Odd Oz: a novel Drosophila pair rule gene. Cell 77, 587-598.
26. Mackinnon AC, Qadota H, Norman KR, Moerman DG, Williams BD (2002). C. elegans PAT-4/ILK functions as an adaptor protein within integrin adhesion complexes. Curr Biol 14, 787-797.
27. Meister P, Towbin BD, Pike BL, Ponti A, Gasser SM (2010). The spatial dynamics of tissue-specific promoters during C. elegans development. Genes Dev 24, 766-782.
28. Mello CC, Kramer JM, Stinchcomb D, Ambros V (1991). Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J 10, 3959-3970.
29. Mieda M, Kikuchi Y, Hirate Y, Aoki M, Okamoto H (1999). Compartmentalized expression of zebrafish ten-m3 and ten-m4, homologues of the Drosophila ten(m)/odd Oz gene, in the central nervous system. Mech Dev 87, 223-227.
30. Minet AD, Rubin BP, Tucker RP, Baumgartner S, Chiquet-Ehrismann R (1999). Teneurin-1, a vertebrate homologue of the Drosophila pair-rule gene ten-m, is a neuronal protein with a novel type of heparin-binding domain. J Cell Sci 112, 2019-2032.
31. Mohler WA, Shemer G, del Campo JJ, Valansi C, Opoku-Serebuoh E, Scranton V, Assaf N, White JG, Podbilewicz B (2002). The type I membrane protein EFF-1 is essential for developmental cell fusion. Dev Cell 2, 355-362.
32. Morck C, Vivekanand V, Jafari G, Pilon M (2010). C. elegans ten-1 is synthetic lethal with mutations in cytoskeleton regulators, and enhances many axon guidance defective mutants. BMC Dev Biol 10, 55.
33. Murakami T, Fukunaga T, Takeshita N, Hiratsuka K, Abiko Y, Yamashiro T, Takano-Yamamoto T (2010). Expression of Ten-m/Odz3 in the fibrous layer of mandibular condylar cartilage during postnatal growth in mice. J Anat 217, 236-244.
34. Myllyharju J, Kukkola L, Winter AD, Page AP (2002). The exoskeleton collagens in Caenorhabditis elegans are modified by prolyl 4-hydroxylases with unique combinations of subunits. J Biol Chem 277, 29187-29196.
35. Oohashi T, Zhou XH, Feng K, Richter B, Morgelin M, Perez MT, Su WD, Chiquet-Ehrismann R, Rauch U, Fassler R (1999). Mouse ten-m/Odz is a new family of dimeric type II transmembrane proteins expressed in many tissues. J Cell Biol 145, 563-577.
36. Priess JR, Hirsh DI (1986). Caenorhabditis elegans morphogenesis: the role of the cytoskeleton in elongation of the embryo. Dev Biol 117, 156-173.
37. Prokop A, Martin-Bermudo MD, Bate M, Brown NH (1998). Absence of PS integrins or laminin A affects extracellular adhesion, but not intracellular assembly, of hemiadherens and neuromuscular junctions in Drosophila embryos. Dev Biol 196, 58-76.
38. Rakovitsky N, Buganim Y, Swissa T, Kinel-Tahan Y, Brenner S, Cohen MA, Levine A, Wides R (2007). Drosophila Ten-a is a maternal pair-rule and patterning gene. Mech Dev 124, 911-924.
39. Riihimaa P, Nissi R, Page AP, Winter AD, Keskiaho K, Kivirikko KI, Myllyharju J (2002). Egg shell collagen formation in Caenorhabditis elegans involves a novel prolyl 4-hydroxylase expressed in spermatheca and embryos and possessing many unique properties. J Biol Chem 277, 18238-18243.
40. Shakes DC, Epstein HF (1995). Caenorhabditis elegans: Modern Biological Analysis of an Organism, San Diego, CA: Academic Press.
41. Simske JS, Hardin J (2001). Getting into shape: epidermal morphogenesis in Caenorhabditis elegans embryos. Bioessays 23, 12-23.
42. Trzebiatowska A, Topf U, Sauder U, Drabikowski K, Chiquet-Ehrismann R (2008). Caenorhabditis elegans teneurin, ten-1, is required for gonadal and pharyngeal basement membrane integrity and acts redundantly with integrin ina-1 and dystroglycan dgn-1. Mol Biol Cell 19, 3898-3908.
43. Tucker RP, Chiquet-Ehrismann R, Chevron MP, Martin D, Hall RJ, Rubin BP (2001). Teneurin-2 is expressed in tissues that regulate limb and somite pattern formation and is induced in vitro and in situ by FGF8. Dev Dyn 220, 27-39.
44. White JG (1988). The anatomy. In: The Nematode Caenorhabditis elegans, ed. WB Wood, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
45. White JG, Southgate E, Thomson JN, Brenner S (1976). The structure of the ventral nerve cord of Caenorhabditis elegans. Philos Trans Royal Soc Lond 275, 327-348.
46. Williams BD, Waterston RH (1994). Genes critical for muscle development and function in Caenorhabditis elegans identified through lethal mutations. J Cell Biol 124, 475-490.
47. Winter AD, Page AP (2000). Prolyl 4-hydroxylase is an essential procollagen-modifying enzyme required for exoskeleton formation and the maintenance of body shape in the nematode Caenorhabditis elegans. Mol Cell Biol 20, 4084-4093.
48. Woo WM, Goncharov A, Jin Y, Chisholm AD (2004). Intermediate filaments are riquired for C. elegans epidermal elongation. Dev Biol 267, 216-229.
49. Zhang H, Labouesse M (2010). The making of hemidesmosome structures in vivo. Dev Dyn 239, 1465-1476.
50. Zhou XH, Brandau O, Feng K, Oohashi T, Ninomiya Y, Rauch U, Fassler R (2003). The murine Ten-m/Odz genes show distinct but overlapping expression patterns during development and in adult brain. Gene Expr Patterns 3, 397-405.