Genetics of extracellular matrix remodeling during organ growth using the Caenorhabditis elegans pharynx model

Genetics

Volumn 186, Issue 3, 2010, Pages 969-982

  Jafari, Gholamali ^a   Burghoorn, Jan ^b   Kawano, Takehiro ^c,d   Mathew, Manoj ^a,e   Mörck, Catarina ^a,g   Axäng, Claes ^a   Ailion, Michael ^f,h   Thomas, James H ^f   Culotti, Joseph G ^c   Swoboda, Peter ^b   Pilon, Marc ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b KAROLINSKA INSTITUTE   (Sweden)

^c MOUNT SINAI HOSPITAL   (Canada)

^d UNIVERSITY OF TORONTO   (Canada)

^e ICFO INSTITUT DE CIENCIES FOTONIQUES   (Spain)

^f UNIVERSITY OF WASHINGTON   (United States)

^g UNIVERSITY OF CALIFORNIA   (United States)

^h UNIVERSITY OF UTAH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAMTS1 PROTEIN; COLLAGEN; FIBULIN; LAMININ; METALLOPROTEINASE; PERLECAN; SEPTIN;

ALLELE; ARTICLE; BASEMENT MEMBRANE; CAENORHABDITIS ELEGANS; EMBRYO; EXTRACELLULAR MATRIX; GENE INTERACTION; GENE MUTATION; GENETIC ANALYSIS; MODEL; NONHUMAN; ORGAN GROWTH; PHARYNX; PHENOTYPE; PRIORITY JOURNAL;

ALLELES; ANIMALS; BASEMENT MEMBRANE; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CHROMOSOME MAPPING; DISINTEGRINS; EXTRACELLULAR MATRIX; GENE KNOCKDOWN TECHNIQUES; GENES, HELMINTH; GENOTYPE; METALLOENDOPEPTIDASES; MODELS, ANIMAL; MUTATION; ORGAN SPECIFICITY; PHARYNX; PHENOTYPE; RNA INTERFERENCE; TORSION ABNORMALITY;

ANIMALIA; CAENORHABDITIS ELEGANS;

EID: 78951478996     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.110.120519     Document Type: Article

References (65)

1. ACKLEY, B. D., J. R. CREW, H. ELAMAA, T. PIHLAJANIEMI, C. J. KUO et al., 2001 The NC1/Endostatin domain of Caenorhabditis elegans type XVIII collagen affects cell migration and axon guidance. J. Cell Biol. 152: 1219-1232.
2. ACKLEY, B. D., S. H. KANG, J. R. CREW, C. SUH, Y. JIN et al., 2003 The basement membrane components nidogen and type XVIII collagen regulate organization of neuromuscular junctions in Caenorhabditis elegans. J. Neurosci. 23: 3577-3587.
3. AILION, M., AND J. H. THOMAS, 2003 Isolation and characterization of high-temperature-induced Dauer formation mutants in Caenorhabditis elegans. Genetics 165: 127-144.
4. ALBERTSON, D. G., and J. N. THOMSON, 1976 The pharynx of Caenorhabditis elegans. Philos. Trans. R. Soc. Lond. B Biol. Sci. 275: 299-325.
5. AVERY, L., and B. S. SHTONDA, 2003 Food transport in the C. elegans pharynx. J. Exp. Biol. 206: 2441-2457.
6. AXÄNG, C., M. RAUTHAN, D. H. HALL and M. PILON, 2007 The twisted pharynx phenotype in C. elegans. BMC Dev. Biol. 7: 61.
7. BÉNARD, C. Y., A. BOYANOV, D.H. HALL and O. HOBERT, 2006 DIG-1, a novel giant protein non-autonomously mediates maintenance of nervous system architecture. Development 133: 3329-3340.
8. BRENNER, S., 1974 The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
9. BURKET, C. T., C. E. HIGGINS, L. C. HULL, P. M. BERNINSONE and E. F. RYDER, 2006 The C. elegans gene dig-1 encodes a giant member of the immunoglobulin superfamily that promotes fasciculation of neuronal processes. Dev. Biol. 299: 193-205.
10. CAMPBELL, A. G., L. I. FESSLER, T. SALO and J. H. FESSLER, 1987 Papilin: a Drosophila proteoglycan-like sulfated glycoprotein from basement membranes. J. Biol. Chem. 262: 17605-17612.
11. CARTER, E. M., and C. L. RAGGIO, 2009 Genetic and orthopedic aspects of collagen disorders. Curr. Opin. Pediatr. 21: 46-54.
12. FESSLER, J. H., I.KRAMEROVA, A. KRAMEROV, Y. CHEN and L. I. FESSLER, 2004 Papilin, a novel component of basement membranes, in relation to ADAMTS metalloproteases and ECM development. Int. J. Biochem. Cell Biol. 36: 1079-1084.
13. GAUDET, J., and S. E. MANGO, 2002 Regulation of organogenesis by the Caenorhabditis elegans FoxA protein PHA-4. Science 295: 821-825.
14. GILLEARD, J. S., J. D. BARRY and I. L. JOHNSTONE, 1997 cis regulatory requirements for hypodermal cell-specific expression of the Caenorhabditis elegans cuticle collagen gene dpy-7. Mol. Cell. Biol. 17: 2301-2311.
15. GLASHEEN, B. M., R. M. ROBBINS, C. PIETTE, G. J. BEITEL and A. PAGE-MCCAW, 2010 A matrix metalloproteinase mediates airway remodeling in Drosophila. Dev. Biol. 344: 772-783.
16. GRANA, T. M., E. A. COX, A.M. LYNCH and J. HARDIN, 2010 SAX-7/ L1CAM and HMR-1/cadherin function redundantly in blastomere compaction and non-muscle myosin accumulation during Caenorhabditis elegans gastrulation. Dev. Biol. 344: 731-744.
17. HESSELSON, D., C. NEWMAN, K.W. KIM and J. KIMBLE, 2004 GON-1 and fibulin have antagonistic roles in control of organ shape. Curr. Biol. 14: 2005-2010.
18. HORNER, M. A., S. QHINTIN, M. E. DOMEIER, J. KIMBLE, M. LABOUESSE et al., 1998 pha-4, an HNF-3 homolog, specifies pharyngeal organ identity in Caenorhabditis elegans. Genes Dev. 12: 1947-1952.
19. HUANG, C. C., D. H. HALL, E. M. HEDGECOCK, G. KAO, V. KARANTZA et al., 2003 Laminin alpha subunits and their role in C. elegans development. Development 130: 3343-3358.
20. HUANG, X., P. HUANG, M. K. ROBINSON, M. J. STERN and Y. JIN, 2003 UNC-71, a disintegrin and metalloprotease (ADAM) protein, regulates motor axon guidance and sex myoblast migration in C. elegans. Development 130: 3147-3161.
21. JARRIAULT, S., and I. GREENWALD, 2005 Evidence for functional redundancy between C. elegans ADAM proteins SUP-17/Kuzbanian and ADM-4/TACE. Dev. Biol. 287: 1-10.
22. JOHNSTONE, I. L., Y. SHAFI and J. D. BARRY, 1992 Molecular analysis of mutations in the Caenorhabditis elegans collagen gene dpy-7. EMBO J. 11: 3857-3863.
23. KALB, J. M., K. K. LAU, B. GOSZCZYNSKI, T. FUKUSHIGE, D. MOONS et al., 1998 pha-4 is Ce-fkh-1, a fork head/HNF-3α, β, γ homolog that functions in organogenesis of the C. elegans pharynx. Development 125: 2171-2180.
24. KAMATH, R. S., M. MARTINEZ-CAMPOS, P. ZIPPERLEN, A.G. FRASER and J. AHRINGER, 2001 Effectiveness of specific RNA-mediated interference through ingested double-stranded RNA in Caenorhabditis elegans. Genome Biol. 2: RESEARCH0002.
25. KAO, G., C. C. HUANG, E. M. HEDGECOCK, D. H. HALL and W. G. WADSWORTH, 2006 The role of the laminin beta subunit in laminin heterotrimer assembly and basement membrane function and development in C. elegans. Dev. Biol. 290: 211-219.
26. KAWANO, T., H. ZHENG, D. C. MERZ, Y. KOHARA, K. K. TAMAI et al., 2009 C. elegans mig-6 encodes papilin isoforms that affect distinct aspects of DTC migration, and interacts genetically with mig-17 and collagen IV. Development 136: 1433-1442.
27. KRAMER, J. M., 2005 Basement membranes (September 1, 2005), WormBook, ed. The C. elegans Research Community, WormBook, doi/10.1895/wormbook.1.16.1, http://www.wormbook.org.
28. KRAMER, J. M., and J. J. JOHNSON, 1993 Analysis of mutations in the sqt-1 and rol-6 collagen genes of Caenorhabditis elegans. Genetics 135: 1035-1045.
29. KRAMEROVA, I. A., N.KAWAGUCHI, L. I. FESSLER, R. E.NELSON, Y. CHEN et al., 2000 Papilin in development; a pericellular protein with a homology to the ADAMTS metalloproteinases. Development 127: 5475-5485.
30. KRAMEROVA, I. A., A. A. KRAMEROV and J. H. FESSLER, 2003 Alternative splicing of papilin and the diversity of Drosophila extracellular matrix during embryonic morphogenesis. Dev. Dyn. 226: 634-642.
31. KUBOTA, Y., R. KUROKI and K. NISHIWAKI, 2004 A fibulin-1 homolog interacts with an ADAM protease that controls cell migration in C. elegans. Curr. Biol. 14: 2011-2018.
32. KUBOTA, Y., K. OHKURA, K. K. TAMAI, K. NAGATA and K. NISHIWAKI, 2008 MIG-17/ADAMTS controls cell migration by recruiting nidogen to the basement membrane in C. elegans. Proc. Natl. Acad. Sci. USA 105: 20804-20809.
33. KUNO, K., C. BABA, A. ASAKA, C.MATSUSHIMA, K. MATSUSHIMA et al., 2002 The Caenorhabditis elegans ADAMTS family gene adt-1 is necessary for morphogenesis of the male copulatory organs. J. Biol. Chem. 277: 12228-12236.
34. LAPRISE, P., S. M. PAUL, J. BOULANGER, R. M. ROBBINS, G. J. BEITEL et al., 2010 Epithelial polarity proteins regulate Drosophila tracheal tube size in parallel to the luminal matrix pathway. Curr. Biol. 20: 55-61.
35. MANGO, S. E., E. J. LAMBIE and J. KIMBLE, 1994 The pha-4 gene is required to generate the pharyngeal primordium of Caenorhabditis elegans. Development 120: 3019-3031. (Pubitemid 24312068)
36. MATHEW, M., S. I. SANTOS, D. ZALVIDEA and P. LOZA-ALVAREZ, 2009 Multimodal optical workstation for simultaneous linear, nonlinear microscopy and nanomanipulation: upgrading a commercial confocal inverted microscope. Rev. Sci. Instrum. 80: 073701.
37. MELLO, C. C., J. M. KRAMER, D. STINCHCOMB and V. AMBROS, 1991 Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. EMBOJ. 10: 3959-3970.
38. MERZ, D. C., G. ALVES, T. KAWANO, H. ZHENG and J. G. CULOTTI, 2003 UNC-52/Perlecan affects gonadal leader cell migrations in C. elegans hermaphrodites through alterations in growth factor signaling. Dev. Biol. 256: 173-186.
39. MIYABAYASHI, T., M. T. PALFREYMAN, A. E. SLUDER, F. SLACK and P. SENGUPTA, 1999 Expression and function of members of a divergent nuclear receptor family in Caenorhabditis elegans. Dev. Biol. 215: 314-331.
40. MÖRCK, C., C. AXÄNG and M. PILON, 2003 A genetic analysis of axon guidance in the C. elegans pharynx. Dev. Biol. 260: 158-175.
41. MÖRCK, C., V. VIVEKANAND, G. JAFARI and M. PILON, 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.
42. MULLEN, G. P., T. M. ROGALSKI, J. A. BUSH, P. R. GORJI and D. G. MOERMAN, 1999 Complex patterns of alternative splicing mediate the spatial and temporal distribution of perlecan/UNC-52 in Caenorhabditis elegans. Mol. Biol. Cell 10: 3205-3221.
43. MURIEL, J. M., C. DONG, H. HUTTER and B. E. VOGEL, 2005 Fibulin-1C and fibulin-1D splice variants have distinct functions and assemble in a hemicentin-dependent manner. Development 132: 4223-4234.
44. NARDI, J. B., R. MARTOS, K. K. WALDEN, D. J. LAMPE and H. M. ROBERTSON, 1999 Expression of lacunin, a large multidomain extracellular matrix protein, accompanies morphogenesis of epithelial monolayers in Manduca sexta. Insect Biochem. Mol. Biol. 29: 883-897.
45. NGUYEN, T. Q., H. SAWA, H. OKANO and J. G. WHITE, 2000 The C. elegans septin genes, unc-59 and unc-61, are required for normal postembryonic cytokineses and morphogenesis but have no essential function in embryogenesis. J. Cell Sci. 113: 3825-3837.
46. NISHIWAKI, K., N. HISAMOTO and K. MATSUMOTO, 2000 A metalloprotease disintegrin that controls cell migration in Caenorhabditis elegans. Science 288: 2205-2208.
47. NISHIWAKI, K., Y. KUBOTA, Y. CHIGIRA, S. K. ROY, M. SUZUKI et al., 2004 An NDPase links ADAM protease glycosylation with organ morphogenesis in C. elegans. Nat. Cell Biol. 6: 31-37.
48. PARK, Y. S., and J. M. KRAMER, 1994 The C. elegans sqt-1 and rol-6 collagen genes are coordinately expressed during development, but not at all stages that display mutant phenotypes. Dev. Biol. 163: 112-124.
49. PEIXOTO, C. A., J. V. DE MELO, J. M. KRAMER and W. DE SOUZA, 1998 Ultrastructural analyses of the Caenorhabditis elegans rol-6 (su1006) mutant, which produces abnormal cuticle collagen. J. Parasitol. 84: 45-49.
50. PERKINS, L. A., E. M. HEDGECOCK, J. N. THOMSON and J. G. CULOTTI, 1986 Mutant sensory cilia in the nematode Caenorhabditis elegans. Dev. Biol. 117: 456-487.
51. PORTEREIKO, M. F., and S. E. MANGO, 2001 Early morphogenesis of the Caenorhabditis elegans pharynx. Dev. Biol. 233: 482-494.
52. PSILODIMITRAKOPOULOS, S., S. I. SANTOS, I. AMAT-ROLDAN, A. K. THAYIL, D. ARTIGAS et al., 2009 In vivo, pixel-resolution mapping of thick filaments' orientation in nonfibrilar muscle using polarization-sensitive second harmonic generation microscopy. J. Biomed. Opt. 14: 014001.
53. ROGALSKI, T. M., B. D. WILLIAMS, G. P. MULLEN and D. G. MOERMAN, 1993 Products of the unc-52 gene in Caenorhabditis elegans are homologous to the core protein of the mammalian basement membrane heparan sulfate proteoglycan. Genes Dev. 7: 1471-1484.
54. ROGALSKI, T. M., G. P. MULLEN, J. A. BUSH, E. J. GILCHRIST and D. G. MOERMAN, 2001 UNC-52/perlecan isoform diversity and function in Caenorhabditis elegans. Biochem. Soc. Trans. 29: 171-176.
55. ROZARIO, T., and D. W. DESIMONE, 2010 The extracellular matrix in development and morphogenesis: a dynamic view. Dev. Biol. 341: 126-140.
56. SASAKURA, H., H. INADA, A. KUHARA, E. FUSAOKA, D. TAKEMOTO et al., 2005 Maintenance of neuronal positions in organized ganglia by SAX-7, a Caenorhabditis elegans homologue of L1. EMBO J. 24: 1477-1488.
57. SCHESSL, J., Y. ZOU and C. G. BONNEMANN, 2006 Congenital muscular dystrophies and the extracellular matrix. Semin. Pediatr. Neurol. 13: 80-89.
58. STARICH, T. A.,R. K. HERMAN, C. K.KARI, W. H. YEH, W. S. SCHACKWITZ et al., 1995 Mutations affecting the chemosensory neurons of Caenorhabditis elegans. Genetics 139: 171-188.
59. SULSTON, J. E., and J. A. HODGKIN, 1988 Methods, pp. 587-606 in The Nematode Caernorhabditis elegans, edited by W. B. Wood. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
60. THEIN, M. C., G. MCCORMACK, A. D. WINTER, I. L. JOHNSTONE, C. B. SHOEMAKER et al., 2003 Caenorhabditis elegans exoskeleton collagen COL-19: an adult-specific marker for collagen modification and assembly, and the analysis of organismal morphology. Dev. Dyn. 226: 523-539.
61. TONNING, A., J. HEMPHALA, E. TANG, U. NANNMARK, C. SAMAKOVLIS et al., 2005 A transient luminal chitinous matrix is required to model epithelial tube diameter in the Drosophila trachea. Dev. Cell 9: 423-430.
62. TSANG, K. Y., M. C. CHEUNG, D. CHAN AND K. S. CHEAH, 2010 The developmental roles of the extracellular matrix: beyond structure to regulation. Cell Tissue Res. 339: 93-110.
63. VOGEL, B. E., and E. M. HEDGECOCK, 2001 Hemicentin, a conserved extracellular member of the immunoglobulin superfamily, organizes epithelial and other cell attachments into oriented line-shaped junctions. Development 128: 883-894.
64. WANG, X., J. KWEON, S. LARSON and L. CHEN, 2005 A role for the C. elegans L1CAM homologue lad-1/sax-7 in maintaining tissue attachment. Dev. Biol. 284: 273-291.
65. WEN, C., M. M. METZSTEIN and I. GREENWALD, 1997 SUP-17, a Caenorhabditis elegans ADAM protein related to Drosophila KUZBANIAN, and its role in LIN-12/NOTCH signalling. Development 124: 4759-4767.