Extracellular leucine-rich repeat proteins are required to organize the apical extracellular matrix and maintain epithelial junction integrity in C. elegans

Development

Volumn 139, Issue 5, 2012, Pages 979-990

  Mancuso, Vincent P ^a   Parry, Jean M ^a   Storer, Luke ^a   Poggioli, Corey ^a   Nguyen, Ken C Q ^b   Hall, David H ^b   Sundaram, Meera V ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

C. elegans; Epithelia; Extracellular matrix

Indexed keywords

DECORIN; EGG 6 PROTEIN; EXTRACELLULAR LEUCINE RICH REPEAT PROTEIN; LET 4 PROTEIN; MEMBRANE PROTEIN; PROTEIN SERINE THREONINE KINASE; UNCLASSIFIED DRUG;

ARTICLE; CAENORHABDITIS ELEGANS; CELL ADHESION; CELL JUNCTION; CONTROLLED STUDY; EPIDERMIS CELL; EPITHELIUM CELL; EXTRACELLULAR MATRIX; NONHUMAN; PRIORITY JOURNAL; SYNAPSE;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL POLARITY; EPITHELIAL CELLS; EXTRACELLULAR MATRIX; GENOTYPE; INTERCELLULAR JUNCTIONS; PROTEINS; RECOMBINANT FUSION PROTEINS;

CAENORHABDITIS ELEGANS; MAMMALIA;

EID: 84856722598     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.075135     Document Type: Article

References (87)

1. Abdus-Saboor, I., Mancuso, V. P., Murray, J. I., Palozola, K., Norris, C., Hall, D. H., Howell, K., Huang, K. and Sundaram, M. V. (2011). Notch and Ras promote sequential steps of excretory tube development in C. elegans. Development 138, 3545-3555.
2. Achilleos, A., Wehman, A. M. and Nance, J. (2010). PAR-3 mediates the initial clustering and apical localization of junction and polarity proteins during C. elegans intestinal epithelial cell polarization. Development 137, 1833-1842.
3. Ackley, B. D., Kang, S. H., Crew, J. R., Suh, C., Jin, Y. and Kramer, J. M. (2003). The basement membrane components nidogen and type XVIII collagen regulate organization of neuromuscular junctions in Caenorhabditis elegans. J. Neurosci. 23, 3577-3587.
4. Acloque, H., Adams, M. S., Fishwick, K., Bronner-Fraser, M. and Nieto, M. A. (2009). Epithelial-mesenchymal transitions: the importance of changing cell state in development and disease. J. Clin. Invest. 119, 1438-1449.
5. Allen, H. G. (1969). Analysis and design of structural sandwich panels. Oxford, UK: Pergamon Press.
6. Ameye, L. and Young, M. F. (2002). Mice deficient in small leucine-rich proteoglycans: novel in vivo models for osteoporosis, osteoarthritis, Ehlers- Danlos syndrome, muscular dystrophy, and corneal diseases. Glycobiology 12, 107R-116R.
7. Bafna, S., Kaur, S. and Batra, S. K. (2010). Membrane-bound mucins: the mechanistic basis for alterations in the growth and survival of cancer cells. Oncogene 29, 2893-2904.
8. Baum, B. and Georgiou, M. (2011). Dynamics of adherens junctions in epithelial establishment, maintenance, and remodeling. J. Cell Biol. 192, 907-917.
9. Benenati, G., Penkov, S., Muller-Reichert, T., Entchev, E. V. and Kurzchalia, T. V. (2009). Two cytochrome P450s in Caenorhabditis elegans are essential for the organization of eggshell, correct execution of meiosis and the polarization of embryo. Mech. Dev. 126, 382-393.
10. Berrier, A. L. and Yamada, K. M. (2007). Cell-matrix adhesion. J. Cell. Physiol. 213, 565-573.
11. Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
12. Brose, N. (2009). Synaptogenic proteins and synaptic organizers: 'many hands make light work'. Neuron 61, 650-652.
13. Buechner, M. (2002). Tubes and the single C. elegans excretory cell. Trends Cell Biol. 12, 479-484.
14. Buechner, M., Hall, D. H., Bhatt, H. and Hedgecock, E. M. (1999). Cystic canal mutants in Caenorhabditis elegans are defective in the apical membrane domain of the renal (excretory) cell. Dev. Biol. 214, 227-241.
15. Bulow, H. E. and Hobert, O. (2006). The molecular diversity of glycosaminoglycans shapes animal development. Annu. Rev. Cell Dev. Biol. 22, 375-407.
16. Carvalho, A., Olson, S. K., Gutierrez, E., Zhang, K., Noble, L. B., Zanin, E., Desai, A., Groisman, A. and Oegema, K. (2011). Acute drug treatment in the early C. elegans embryo. PLoS One 6, e24656.
17. Chalfie, M. and Au, M. (1989). Genetic control of differentiation of the Caenorhabditis elegans touch receptor neurons. Science 243, 1027-1033.
18. Chamcheu, J. C., Siddiqui, I. A., Syed, D. N., Adhami, V. M., Liovic, M. and Mukhtar, H. (2011). Keratin gene mutations in disorders of human skin and its appendages. Arch. Biochem. Biophys. 508, 123-137.
19. Costa, M., Draper, B. W. and Priess, J. R. (1997). The role of actin filaments in patterning the Caenorhabditis elegans cuticle. Dev. Biol. 184, 373-384.
20. Costa, M., Raich, W., Agbunag, C., Leung, B., Hardin, J. and Priess, J. R. (1998). A putative catenin-cadherin system mediates morphogenesis of the Caenorhabditis elegans embryo. J. Cell Biol. 141, 297-308.
21. Davies, A. G., Spike, C. A., Shaw, J. E. and Herman, R. K. (1999). Functional overlap between the mec-8 gene and five sym genes in Caenorhabditis elegans. Genetics 153, 117-134.
22. de Wit, J., Sylwestrak, E., O'Sullivan, M. L., Otto, S., Tiglio, K., Savas, J. N., Yates, J. R., 3rd, Comoletti, D., Taylor, P. and Ghosh, A. (2009). LRRTM2 interacts with Neurexin1 and regulates excitatory synapse formation. Neuron 64, 799-806.
23. Devine, W. P., Lubarsky, B., Shaw, K., Luschnig, S., Messina, L. and Krasnow, M. A. (2005). Requirement for chitin biosynthesis in epithelial tube morphogenesis. Proc. Natl. Acad. Sci. USA 102, 17014-17019.
24. Diogon, M., Wissler, F., Quintin, S., Nagamatsu, Y., Sookhareea, S., Landmann, F., Hutter, H., Vitale, N. and Labouesse, M. (2007). The RhoGAP RGA-2 and LET-502/ROCK achieve a balance of actomyosin-dependent forces in C. elegans epidermis to control morphogenesis. Development 134, 2469-2479.
25. Dolan, J., Walshe, K., Alsbury, S., Hokamp, K., O'Keeffe, S., Okafuji, T., Miller, S. F., Tear, G. and Mitchell, K. J. (2007). The extracellular leucine-rich repeat superfamily; a comparative survey and analysis of evolutionary relationships and expression patterns. BMC Genomics 8, 320.
26. Finney, M. and Ruvkun, G. (1990). The unc-86 gene product couples cell lineage and cell identity in C. elegans. Cell 63, 895-905.
27. Fox, M. A., Ho, M. S., Smyth, N. and Sanes, J. R. (2008). A synaptic nidogen: developmental regulation and role of nidogen-2 at the neuromuscular junction. Neural Dev. 3, 24.
28. Francis, R. and Waterston, R. H. (1991). Muscle cell attachment in Caenorhabditis elegans. J. Cell Biol. 114, 465-479.
29. Gally, C., Wissler, F., Zahreddine, H., Quintin, S., Landmann, F. and Labouesse, M. (2009). Myosin II regulation during C. elegans embryonic elongation: LET-502/ROCK, MRCK-1 and PAK-1, three kinases with different roles. Development 136, 3109-3119.
30. Giepmans, B. N. and van Ijzendoorn, S. C. (2009). Epithelial cell-cell junctions and plasma membrane domains. Biochim. Biophys. Acta 1788, 820-831.
31. Gilleard, J. S., Barry, J. D. and Johnstone, I. L. (1997). cis regulatory requirements for hypodermal cell-specific expression of the Caenorhabditis elegans cuticle collagen gene dpy-7. Mol. Cell. Biol. 17, 2301-2311.
32. Gobel, V., Barrett, P. L., Hall, D. H. and Fleming, J. T. (2004). Lumen morphogenesis in C. elegans requires the membrane-cytoskeleton linker erm-1. Dev. Cell 6, 865-873.
33. Goldstein, B. and Macara, I. G. (2007). The PAR proteins: fundamental players in animal cell polarization. Dev. Cell 13, 609-622.
34. Hodgkin, J. (1997). Genetics. In C. elegans II (ed. T. B. D. L. Riddle, B. J. Meyer and J. R. Priess), pp. 881-1047. Plainview, NY: Cold Spring Harbor Laboratory Press.
35. Hynes, R. O. (2009). The extracellular matrix: not just pretty fibrils. Science 326, 1216-1219.
36. Jazwinska, A., Ribeiro, C. and Affolter, M. (2003). Epithelial tube morphogenesis during Drosophila tracheal development requires Piopio, a luminal ZP protein. Nat. Cell Biol. 5, 895-901.
37. Johnson, A. D., Fitzsimmons, D., Hagman, J. and Chamberlin, H. M. (2001). EGL-38 Pax regulates the ovo-related gene lin-48 during Caenorhabditis elegans organ development. Development 128, 2857-2865.
38. Johnstone, I. L. (2000). Cuticle collagen genes. Expression in Caenorhabditis elegans. Trends Genet. 16, 21-27.
39. Johnstone, I. L. and Barry, J. D. (1996). Temporal reiteration of a precise gene expression pattern during nematode development. EMBO J. 15, 3633-3639.
40. Kalamajski, S. and Oldberg, A. (2010). The role of small leucine-rich proteoglycans in collagen fibrillogenesis. Matrix Biol. 29, 248-253.
41. Kalluri, R. and Weinberg, R. A. (2009). The basics of epithelial-mesenchymal transition. J. Clin. Invest. 119, 1420-1428.
42. Kamath, R. S., Fraser, A. G., Dong, Y., Poulin, G., Durbin, R., Gotta, M., Kanapin, A., Le Bot, N., Moreno, S., Sohrmann, M. et al. (2003). Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421, 231-237.
43. Ko, J., Fuccillo, M. V., Malenka, R. C. and Sudhof, T. C. (2009). LRRTM2 functions as a neurexin ligand in promoting excitatory synapse formation. Neuron 64, 791-798.
44. Koppen, M., Simske, J. S., Sims, P. A., Firestein, B. L., Hall, D. H., Radice, A. D., Rongo, C. and Hardin, J. D. (2001). Cooperative regulation of AJM-1 controls junctional integrity in Caenorhabditis elegans epithelia. Nat. Cell Biol. 3, 983-991.
45. Kufe, D. W. (2009). Mucins in cancer: function, prognosis and therapy. Nat. Rev. Cancer 9, 874-885.
46. Kurusu, M., Cording, A., Taniguchi, M., Menon, K., Suzuki, E. and Zinn, K. (2008). A screen of cell-surface molecules identifies leucine-rich repeat proteins as key mediators of synaptic target selection. Neuron 59, 972-985.
47. Linhoff, M. W., Lauren, J., Cassidy, R. M., Dobie, F. A., Takahashi, H., Nygaard, H. B., Airaksinen, M. S., Strittmatter, S. M. and Craig, A. M. (2009). An unbiased expression screen for synaptogenic proteins identifies the LRRTM protein family as synaptic organizers. Neuron 61, 734-749.
48. Lockwood, C., Zaidel-Bar, R. and Hardin, J. (2008). The C. elegans zonula occludens ortholog cooperates with the cadherin complex to recruit actin during morphogenesis. Curr. Biol. 18, 1333-1337.
49. Lynch, A. M. and Hardin, J. (2009). The assembly and maintenance of epithelial junctions in C. elegans. Front. Biosci. 14, 1414-1432.
50. Marchiando, A. M., Graham, W. V. and Turner, J. R. (2010). Epithelial barriers in homeostasis and disease. Annu. Rev. Pathol. 5, 119-144.
51. Mattingly, B. C. and Buechner, M. (2011). The FGD homologue EXC-5 regulates apical trafficking in C. elegans tubules. Dev. Biol. 359, 59-72.
52. Meneely, P. M. and Herman, R. K. (1979). Lethals, steriles and deficiencies in a region of the X chromosome of Caenorhabditis elegans. Genetics 92, 99-115.
53. Moerman, D. G. and Barstead, R. J. (2008). Towards a mutation in every gene in Caenorhabditis elegans. Brief. Func. Genomic. Proteomic. 7, 195-204.
54. Moribe, H., Yochem, J., Yamada, H., Tabuse, Y., Fujimoto, T. and Mekada, E. (2004). Tetraspanin protein (TSP-15) is required for epidermal integrity in Caenorhabditis elegans. J. Cell Sci. 117, 5209-5220.
55. Nance, J., Munro, E. M. and Priess, J. R. (2003). C. elegans PAR-3 and PAR-6 are required for apicobasal asymmetries associated with cell adhesion and gastrulation. Development 130, 5339-5350.
56. Nelson, F. K. and Riddle, D. L. (1984). Functional study of the Caenorhabditis elegans secretory-excretory system using laser microsurgery. J. Exp. Zool. 231, 45-56.
57. Nelson, F. K., Albert, P. S. and Riddle, D. L. (1983). Fine structure of the Caenorhabditis elegans secretory-excretory system. J. Ultrastruct. Res. 82, 156-171.
58. Page, A. P. and Johnstone, I. L. (2007). The cuticle. WormBook, 1-15.
59. Papusheva, E. and Heisenberg, C. P. (2010). Spatial organization of adhesion: force-dependent regulation and function in tissue morphogenesis. EMBO J. 29, 2753-2768.
60. Partridge, F. A., Tearle, A. W., Gravato-Nobre, M. J., Schafer, W. R. and Hodgkin, J. (2008). The C. elegans glycosyltransferase BUS-8 has two distinct and essential roles in epidermal morphogenesis. Dev. Biol. 317, 549-559.
61. Plaza, S., Chanut-Delalande, H., Fernandes, I., Wassarman, P. M. and Payre, F. (2010). From A to Z: apical structures and zona pellucida-domain proteins. Trends Cell Biol. 20, 524-532.
62. Polyak, K. and Weinberg, R. A. (2009). Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat. Rev. Cancer 9, 265-273.
63. Priess, J. R. and Hirsh, D. I. (1986). Caenorhabditis elegans morphogenesis: the role of the cytoskeleton in elongation of the embryo. Dev. Biol. 117, 156-173.
64. Rappleye, C. A., Paredez, A. R., Smith, C. W., McDonald, K. L. and Aroian, R. V. (1999). The coronin-like protein POD-1 is required for anterior-posterior axis formation and cellular architecture in the nematode caenorhabditis elegans. Genes Dev. 13, 2838-2851.
65. Roberts, B., Clucas, C. and Johnstone, I. L. (2003). Loss of SEC-23 in Caenorhabditis elegans causes defects in oogenesis, morphogenesis, and extracellular matrix secretion. Mol. Biol. Cell 14, 4414-4426.
66. Ross, M. D., Bruggeman, L. A., Hanss, B., Sunamoto, M., Marras, D., Klotman, M. E. and Klotman, P. E. (2003). Podocan, a novel small leucine-rich repeat protein expressed in the sclerotic glomerular lesion of experimental HIVassociated nephropathy. J. Biol. Chem. 278, 33248-33255.
67. Roy, L. D., Sahraei, M., Subramani, D. B., Besmer, D., Nath, S., Tinder, T. L., Bajaj, E., Shanmugam, K., Lee, Y. Y., Hwang, S. I. et al. (2011). MUC1 enhances invasiveness of pancreatic cancer cells by inducing epithelial to mesenchymal transition. Oncogene 30, 1449-1459.
68. Schaefer, L. and Iozzo, R. V. (2008). Biological functions of the small leucine-rich proteoglycans: from genetics to signal transduction. J. Biol. Chem. 283, 21305-21309.
69. Segbert, C., Johnson, K., Theres, C., van Furden, D. and Bossinger, O. (2004). Molecular and functional analysis of apical junction formation in the gut epithelium of Caenorhabditis elegans. Dev. Biol. 266, 17-26.
70. Shimizu-Hirota, R., Sasamura, H., Kuroda, M., Kobayashi, E. and Saruta, T. (2004). Functional characterization of podocan, a member of a new class in the small leucine-rich repeat protein family. FEBS Lett. 563, 69-74.
71. Shin, K., Fogg, V. C. and Margolis, B. (2006). Tight junctions and cell polarity. Annu. Rev. Cell Dev. Biol. 22, 207-235.
72. Shinza-Kameda, M., Takasu, E., Sakurai, K., Hayashi, S. and Nose, A. (2006). Regulation of layer-specific targeting by reciprocal expression of a cell adhesion molecule, capricious. Neuron 49, 205-213.
73. Shishido, E., Takeichi, M. and Nose, A. (1998). Drosophila synapse formation: regulation by transmembrane protein with Leu-rich repeats, CAPRICIOUS. Science 280, 2118-2121.
74. Siddiqui, T. J., Pancaroglu, R., Kang, Y., Rooyakkers, A. and Craig, A. M. (2010). LRRTMs and neuroligins bind neurexins with a differential code to cooperate in glutamate synapse development. J. Neurosci. 30, 7495-7506.
75. Sonnichsen, B., Koski, L. B., Walsh, A., Marschall, P., Neumann, B., Brehm, M., Alleaume, A. M., Artelt, J., Bettencourt, P., Cassin, E. et al. (2005). Fullgenome RNAi profiling of early embryogenesis in Caenorhabditis elegans. Nature 434, 462-469.
76. St Johnston, D. and Sanson, B. (2011). Epithelial polarity and morphogenesis. Curr. Opin. Cell Biol. 23, 540-546.
77. Stone, C. E., Hall, D. H. and Sundaram, M. V. (2009). Lipocalin signaling controls unicellular tube development in the Caenorhabditis elegans excretory system. Dev. Biol. 329, 201-211.
78. Sulston, J. E., Schierenberg, E., White, J. G. and Thomson, J. N. (1983). The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev. Biol. 100, 64-119.
79. Swanson, L. E., Yu, M., Nelson, K. S., Laprise, P., Tepass, U. and Beitel, G. J. (2009). Drosophila convoluted/dALS is an essential gene required for tracheal tube morphogenesis and apical matrix organization. Genetics 181, 1281-1290.
80. 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, 3607-3614.
81. Taniguchi, H., Shishido, E., Takeichi, M. and Nose, A. (2000). Functional dissection of drosophila capricious: its novel roles in neuronal pathfinding and selective synapse formation. J. Neurobiol. 42, 104-116.
82. Tonning, A., Hemphala, J., Tang, E., Nannmark, U., Samakovlis, C. and Uv, A. (2005). A transient luminal chitinous matrix is required to model epithelial tube diameter in the Drosophila trachea. Dev. Cell 9, 423-430.
83. Totong, R., Achilleos, A. and Nance, J. (2007). PAR-6 is required for junction formation but not apicobasal polarization in C. elegans embryonic epithelial cells. Development 134, 1259-1268.
84. Van Furden, D., Johnson, K., Segbert, C. and Bossinger, O. (2004). The C. elegans ezrin-radixin-moesin protein ERM-1 is necessary for apical junction remodelling and tubulogenesis in the intestine. Dev. Biol. 272, 262-276.
85. Weimer, R. M. (2006). Preservation of C. elegans tissue via high-pressure freezing and freeze-substitution for ultrastructural analysis and immunocytochemistry. Methods Mol. Biol. 351, 203-221.
86. Wilson, P. D. (2011). Apico-basal polarity in polycystic kidney disease epithelia. Biochim. Biophys. Acta 1812, 1239-1248.
87. Wissmann, A., Ingles, J. and Mains, P. E. (1999). The Caenorhabditis elegans mel-11 myosin phosphatase regulatory subunit affects tissue contraction in the somatic gonad and the embryonic epidermis and genetically interacts with the Rac signaling pathway. Dev. Biol. 209, 111-127.