Basement membrane sliding and targeted adhesion remodels tissue boundaries during uterine-vulval attachment in Caenorhabditis elegans

Nature Cell Biology

Volumn 13, Issue 6, 2011, Pages 641-652

  Ihara, Shinji ^a   Hagedorn, Elliott J ^a   Morrissey, Meghan A ^a   Chi, Qiuyi ^a   Motegi, Fumio ^b   Kramer, James M ^c   Sherwood, David R ^a  

^a DUKE UNIVERSITY   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 4; INA 1 PROTEIN; INTEGRIN; LAMININ; PAT 3 PROTEIN; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; VAB 19 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASEMENT MEMBRANE; BASEMENT MEMBRANE SLIDING; BLEACHING; CAENORHABDITIS ELEGANS; CELL INTERACTION; CELL INVASION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; LARVAL DEVELOPMENT; MEMBRANE BIOLOGY; MEMBRANE FORMATION; MEMBRANE STABILIZATION; NONHUMAN; PRIORITY JOURNAL; UTERINE VULVAL ATTACHMENT; UTERUS; VULVA;

ANIMALS; BASEMENT MEMBRANE; CAENORHABDITIS ELEGANS; CELL ADHESION; FEMALE; UTERUS; VULVA;

CAENORHABDITIS ELEGANS;

EID: 79957895829     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb2233     Document Type: Article

References (55)

1. Rowe, R. G. & Weiss, S. J. Navigating ECM barriers at the invasive front: the cancer cell-stroma interface. Annu. Rev. Cell Dev. Biol. 25, 567-595 (2009).
2. Sherwood, D. R. Cell invasion through basement membranes: an anchor of understanding. Trends Cell Biol. 16, 250-256 (2006). (Pubitemid 43744437)
3. Kalluri, R. Basement membranes: structure, assembly and role in tumour angiogenesis. Nat. Rev. Cancer 3, 422-433 (2003). (Pubitemid 37328846)
4. Even-Ram, S. & Yamada, K. M. Cell migration in 3D matrix. Curr. Opin. Cell Biol. 17, 524-532 (2005). (Pubitemid 41267167)
5. Rowe, R. G. & Weiss, S. J. Breaching the basement membrane: who, when and how? Trends. Cell Biol. 18, 560-574 (2008).
6. Nourshargh, S., Hordijk, P. L. & Sixt, M. Breaching multiple barriers: leukocyte motility through venular walls and the interstitium. Nat. Rev. Mol. Cell Biol. 11, 366-378 (2010).
7. Nakaya, Y., Sukowati, E. W., Wu, Y. & Sheng, G. RhoA and microtubule dynamics control cell-basement membrane interaction in EMT during gastrulation. Nat. Cell Biol. 10, 765-775 (2008). (Pubitemid 351927706)
8. Sherwood, D. R. & Sternberg, P. W. Anchor cell invasion into the vulval epithelium in C. elegans. Dev. Cell 5, 21-31 (2003). (Pubitemid 36827339)
9. Srivastava, A., Pastor-Pareja, J. C., Igaki, T., Pagliarini, R. & Xu, T. Basement membrane remodeling is essential for Drosophila disc eversion and tumour invasion. Proc. Natl Acad. Sci. USA 104, 2721-2726 (2007). (Pubitemid 46327946)
10. Barsky, S. H., Siegal, G. P., Jannotta, F. & Liotta, L. A. Loss of basement membrane components by invasive tumours but not by their benign counterparts. Lab. Invest. 49, 140-147 (1983). (Pubitemid 13039938)
11. Flug, M. & Kopf-Maier, P. The basement membrane and its involvement in carcinoma cell invasion. Acta. Anat. (Basel) 152, 69-84 (1995).
12. Frei, J. V. The fine structure of the basement membrane in epidermal tumours. J. Cell Biol. 15, 335-342 (1962).
13. Matus, D. Q. et al. In vivo identification of regulators of cell invasion across basement membranes. Sci. Signal. 3, ra35 (2010).
14. Spaderna, S. et al. A transient, EMT-linked loss of basement membranes indicates metastasis and poor survival in colorectal cancer. Gastroenterology 131, 830-840 (2006). (Pubitemid 44307069)
15. Cavallo-Medved, D. et al. Live-cell imaging demonstrates extracellular matrix degradation in association with active cathepsin B in caveolae of endothelial cells during tube formation. Exp. Cell Res. 315, 1234-1246 (2009).
16. Garbisa, S., Kniska, K., Tryggvason, K., Foltz, C. & Liotta, L. A. Quantitation of basement membrane collagen degradation by living tumour cells in vitro. Cancer Lett. 9, 359-366 (1980). (Pubitemid 10047706)
17. Hotary, K., Li, X. Y., Allen, E., Stevens, S. L. & Weiss, S. J. A cancer cell metalloprotease triad regulates the basement membrane transmigration program. Genes Dev. 20, 2673-2686 (2006). (Pubitemid 44498378)
18. Overall, C. M. & Kleifeld, O. Tumour microenvironment\opinion: validating matrix metalloproteinases as drug targets and anti-targets for cancer therapy. Nat. Rev. Cancer 6, 227-239 (2006). (Pubitemid 43292566)
19. Page-McCaw, A., Ewald, A. J. & Werb, Z. Matrix metalloproteinases and the regulation of tissue remodelling. Nat. Rev. Mol. Cell Biol. 8, 221-233 (2007).
20. Sameni, M., Dosescu, J., Yamada, K. M., Sloane, B. F. & Cavallo-Medved, D. Functional live-cell imaging demonstrates that beta1-integrin promotes type IV collagen degradation by breast and prostate cancer cells. Mol. Imaging 7, 199-213 (2008).
21. Sherwood, D. R., Butler, J. A., Kramer, J. M. & Sternberg, P. W. FOS-1 promotes basement-membrane removal during anchor-cell invasion in C. elegans. Cell 121, 951-962 (2005). (Pubitemid 40806425)
22. Xu, J. et al. Proteolytic exposure of a cryptic site within collagen type IV is required for angiogenesis and tumor growth in vivo. J. Cell Biol. 154, 1069-1079 (2001). (Pubitemid 34286185)
23. Liotta, L. A., Rao, N. C., Barsky, S. H. & Bryant, G. The laminin receptor and basement membrane dissolution: role in tumour metastasis. Ciba. Found. Symp. 108, 146-162 (1984).
24. Newman, A. P. & Sternberg, P. W. Coordinated morphogenesis of epithelia during development of the Caenorhabditis elegans uterine-vulval connection. Proc. Natl Acad. Sci. USA 93, 9329-9333 (1996). (Pubitemid 26296607)
25. Ding, M. et al. The cell signalling adaptor protein EPS-8 is essential for C. elegans epidermal elongation and interacts with the ankyrin repeat protein VAB-19. PLoS One 3, e3346 (2008).
26. Kakinuma, N., Zhu, Y., Wang, Y., Roy, B. C. & Kiyama, R. Kank proteins: structure, functions and diseases. Cell Mol. Life Sci. 66, 2651-2659 (2009).
27. Newman, A. P., White, J. G. & Sternberg, P. W. Morphogenesis of the C. elegans hermaphrodite uterus. Development 122, 3617-3626 (1996). (Pubitemid 26396003)
28. Lints, R. & Hall, D. H. Reproductive system, egglaying apparatus. WormAtlas doi:10.3908/wormatlas.1.24 (2010).
29. Kao, G., Huang, C. C., Hedgecock, E. M., Hall, D. H. & Wadsworth, W. G. 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 (2006). (Pubitemid 43083616)
30. Ziel, J. W., Hagedorn, E. J., Audhya, A. & Sherwood, D. R. UNC-6 (netrin) orients the invasive membrane of the anchor cell in C. elegans. Nat. Cell Biol. 11, 183-189 (2009).
31. Fitzgerald, M. C. & Schwarzbauer, J. E. Importance of the basement membrane protein SPARC for viability and fertility in Caenorhabditis elegans. Curr. Biol. 8, 1285-1288 (1998). (Pubitemid 28540058)
32. Kramer, J. M. Basement membranes. WormBook 1-15 (2005).
33. Hagedorn, E. J. et al. Integrin acts upstream of netrin signalling to regulate formation of the anchor cell's invasive membrane in C. elegans. Dev. Cell 17, 187-198 (2009).
34. Kimble, J. & Hirsh, D. The postembryonic cell lineages of the hermaphrodite and male gonads in Caenorhabditis elegans. Dev. Biol. 70, 396-417 (1979). (Pubitemid 10223307)
35. Liu, J., Tzou, P., Hill, R. J. & Sternberg, P. W. Structural requirements for the tissue-specific and tissue-general functions of the Caenorhabditis elegans epidermal growth factor LIN-3. Genetics 153, 1257-1269 (1999). (Pubitemid 29522140)
36. Gurskaya, N. G. et al. Engineering of a monomeric green-to-red photoactivatable fluorescent protein induced by blue light. Nat. Biotechnol. 24, 461-465 (2006).
37. Baum, P. D. & Garriga, G. Neuronal migrations and axon fasciculation are disrupted in ina-1 integrin mutants. Neuron 19, 51-62 (1997). (Pubitemid 27332993)
38. Yurchenco, P. D., Amenta, P. S. & Patton, B. L. Basement membrane assembly, stability and activities observed through a developmental lens. Matrix Biol. 22, 521-538 (2004). (Pubitemid 38283776)
39. Leptin, M., Bogaert, T., Lehmann, R. & Wilcox, M. The function of PS integrins during Drosophila embryogenesis. Cell 56, 401-408 (1989).
40. Marlin, S. D., Morton, C. C., Anderson, D. C. & Springer, T. A. LFA-1 immunodeficiency disease. Definition of the genetic defect and chromosomal mapping of alpha and beta subunits of the lymphocyte function-associated antigen 1 (LFA-1) by complementation in hybrid cells. J. Exp. Med. 164, 855-867 (1986). (Pubitemid 16024839)
41. Ding, M., Goncharov, A., Jin, Y. & Chisholm, A. D. C. elegans ankyrin repeat protein VAB-19 is a component of epidermal attachment structures and is essential for epidermal morphogenesis. Development 130, 5791-5801 (2003). (Pubitemid 37540852)
42. Madsen, C. D. & Sahai, E. Cancer dissemination\lessons from leukocytes. Dev. Cell 19, 13-26 (2010).
43. Wolf, K. et al. Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasion. Nat. Cell Biol. 9, 893-904 (2007). (Pubitemid 47190444)
44. Altun, Z. F. & Hall, D. H. Muscle system, somatic muscle. WormAtlas doi:10.3908/wormatlas.1.7, (2009).
45. Cox, E. A., Tuskey, C. & Hardin, J. Cell adhesion receptors in C. elegans. J. Cell Sci. 117, 1867-1870 (2004). (Pubitemid 38745120)
46. Leardkamolkarn, V. & Abrahamson, D. R. Binding of intravenously injected antibodies against laminin to developing and mature endocrine glands. Cell Tissue Res. 251, 171-181 (1988). (Pubitemid 18002683)
47. Price, R. G. & Spiro, R. G. Studies on the metabolism of the renal glomerular basement membrane. Turnover measurements in the rat with the use of radiolabelled amino acids. J. Biol. Chem. 252, 8597-8602 (1977). (Pubitemid 8243623)
48. Trier, J. S., Allan, C. H., Abrahamson, D. R. & Hagen, S. J. Epithelial basement membrane of mouse jejunum. Evidence for laminin turnover along the entire crypt-villus axis. J. Clin. Invest. 86, 87-95 (1990). (Pubitemid 20226979)
49. Zamir, E. A., Rongish, B. J. & Little, C. D. The ECM moves during primitive streak formation\computation of ECM versus cellular motion. PLoS Biol. 6 e247 (2008).
50. Hanahan, D. & Weinberg, R. A. The hallmarks of cancer. Cell 100, 57-70 (2000). (Pubitemid 30046295)
51. Brenner, S. The genetics of Caenorhabditis elegans. Genetics 77, 71-94 (1974).
52. Fraser, A. G. et al. Functional genomic analysis of C. elegans chromosome I by systematic RNA interference. Nature 408, 325-330 (2000).
53. Rual, J. F. et al. Toward improving Caenorhabditis elegans phenome mapping with an ORFeome-based RNAi library. Genome Res. 14, 2162-2168 (2004).
54. Green, R. A. et al. Expression and imaging of fluorescent proteins in the C. elegans gonad and early embryo. Methods Cell Biol. 85, 179-218 (2008).
55. Hagedorn, E. & Sherwood, D. Optically highlighting basement membrane components C. elegans. Protocol Exchange doi:10.1038/protex.2011.230 (2011).