Primary cilia utilize glycoprotein-dependent adhesion mechanisms to stabilize long-lasting cilia-cilia contacts

Cilia

Volumn 1, Issue , 2012, Pages

  Ott, Carolyn ^a   Elia, Natalie ^a   Jeong, Suh Young ^a   Insinna, Christine ^b   Sengupta, Prabuddha ^a   Lippincott Schwartz, Jennifer ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Adhesion; Contact; Direct sensing; Glycoprotein; Primary cilia

Indexed keywords

CALCIUM; DITHIOTHREITOL; GLYCOPROTEIN; PROTEINASE; SWAINSONINE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CELL CONTACT; CELL DIVISION; CILIARY MOTILITY; CONTROLLED STUDY; EUKARYOTIC FLAGELLUM; LIVER CELL; MDCK CELL; MITOSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; RETINA ROD;

MAMMALIA;

EID: 84871833081     PISSN: None     EISSN: 20462530     Source Type: Journal    
DOI: 10.1186/2046-2530-1-3     Document Type: Article

References (41)

1. Veland IR, Awan A, Pedersen LB, Yoder BK, Christensen ST. Primary cilia and signaling pathways in mammalian development, health and disease. Nephron Physiol 2009, 111:39-53.
2. Scholey JM. Intraflagellar transport motors in cilia: moving along the cell's antenna. J Cell Biol 2008, 180:23-29. 10.1083/jcb.200709133, 2213603, 18180368.
3. Wolfe J, Mpoke S, Tirone SF. Cilia, ciliary concanavalin A-binding proteins, and mating recognition in Tetrahymena thermophila. Exp Mol Pathol 1993, 209:342-349.
4. Plumper E, Freiburg M, Heckmann K. Conjugation in the ciliate Euplotes octocarinatus: comparison of ciliary and cell body-associated glycoconjugates of non-mating-competent, mating-competent, and conjugating cells. Exp Cell Res 1995, 217:490-496. 10.1006/excr.1995.1114, 7698250.
5. Kooijman R, de Wildt P, Beumer S, van der Vliet G, Homan W, Kalshoven H, Musgrave A, van den Ende H. Wheat germ agglutinin induces mating reactions in Chlamydomonas eugametos by cross-linking agglutinin-associated glycoproteins in the flagellar membrane. J Cell Biol 1989, 109:1677-1687. 10.1083/jcb.109.4.1677, 2115781, 2551909.
6. Wang Q, Snell WJ. Flagellar adhesion between mating type plus and mating type minus gametes activates a flagellar protein-tyrosine kinase during fertilization in Chlamydomonas. J Biol Chem 2003, 278:32936-32942. 10.1074/jbc.M303261200, 12821679.
7. Lam X, Gieseke C, Knoll M, Talbot P. Assay and importance of adhesive interaction between hamster (Mesocricetus auratus) oocyte-cumulus complexes and the oviductal epithelium. Biol Reprod 2000, 62:579-588. 10.1095/biolreprod62.3.579, 10684798.
8. Talbot P, Geiske C, Knoll M. Oocyte pickup by the mammalian oviduct. Mol Biol Cell 1999, 10:5-8. 25149, 9880322.
9. Romero MR, Kelstrup HC, Strathmann RR. Capture of particles by direct interception by cilia during feeding of a gastropod veliger. Biol Bull 2010, 218:145-159.
10. Hillman DE. New ultrastructural findings regarding a vestibular ciliary apparatus and its possible functional significance. Brain Res 1969, 13:407-412. 10.1016/0006-8993(69)90301-1, 5305680.
11. Michel V, Goodyear RJ, Weil D, Marcotti W, Perfettini I, Wolfrum U, Kros CJ, Richardson GP, Petit C. Cadherin 23 is a component of the transient lateral links in the developing hair bundles of cochlear sensory cells. Dev Biol 2005, 280:281-294. 10.1016/j.ydbio.2005.01.014, 15882573.
12. Ahmed ZM, Goodyear R, Riazuddin S, Lagziel A, Legan PK, Behra M, Burgess SM, Lilley KS, Wilcox ER, Griffith AJ, Frolenkov GI, Belyantseva IA, Richardson GP, Friedman TB. The tip-link antigen, a protein associated with the transduction complex of sensory hair cells, is protocadherin-15. J Neurosci 2006, 26:7022-7034. 10.1523/JNEUROSCI.1163-06.2006, 16807332.
13. Wakabayashi Y, Chua J, Larkin JM, Lippincott-Schwartz J, Arias IM. Four-dimensional imaging of filter-grown polarized epithelial cells. Histochem Cell Biol 2007, 127:463-472. 10.1007/s00418-007-0274-x, 17308935.
14. Elia N, Lippincott-Schwartz J. Culturing MDCK cells in three dimensions for analyzing intracellular dynamics. Curr Protoc Cell Biol 2009, Chapter 4:Unit 4.
15. Chakrabarti O, Hegde RS. Functional depletion of mahogunin by cytosolically exposed prion protein contributes to neurodegeneration. Cell 2009, 137:1136-1147. 10.1016/j.cell.2009.03.042, 2709807, 19524515.
16. Insinna C, Besharse JC. Intraflagellar transport and the sensory outer segment of vertebrate photoreceptors. Dev Dyn 2008, 237:1982-1992. 10.1002/dvdy.21554, 2692564, 18489002.
17. Masyuk AI, Masyuk TV, LaRusso NF. Cholangiocyte primary cilia in liver health and disease. Dev Dyn 2008, 237:2007-2012. 10.1002/dvdy.21530, 2574848, 18407555.
18. Nielsen SK, Mollgard K, Clement CA, Veland IR, Awan A, Yoder BK, Novak I, Christensen ST. Characterization of primary cilia and Hedgehog signaling during development of the human pancreas and in human pancreatic duct cancer cell lines. Dev Dyn 2008, 237:2039-2052. 10.1002/dvdy.21610, 18629868.
19. Florek M, Bauer N, Janich P, Wilsch-Braeuninger M, Fargeas CA, Marzesco AM, Ehninger G, Thiele C, Huttner WB, Corbeil D. Prominin-2 is a cholesterol-binding protein associated with apical and basolateral plasmalemmal protrusions in polarized epithelial cells and released into urine. Cell Tissue Res 2007, 328:31-47. 10.1007/s00441-006-0324-z, 17109118.
20. Praetorius HA, Praetorius J, Nielsen S, Frokiaer J, Spring KR. Beta1-integrins in the primary cilium of MDCK cells potentiate fibronectin-induced Ca2+ signaling. Am J Physiol Renal Physiol 2004, 287:F969-F978. 10.1152/ajprenal.00096.2004, 15226154.
21. Takeichi M. The cadherins: cell-cell adhesion molecules controlling animal morphogenesis. Development 1988, 102:639-655.
22. Xiao T, Takagi J, Coller BS, Wang JH, Springer TA. Structural basis for allostery in integrins and binding to fibrinogen-mimetic therapeutics. Nature 2004, 432:59-67. 10.1038/nature02976, 15378069.
23. Hughes J, Ward CJ, Peral B, Aspinwall R, Clark K, San Millan JL, Gamble V, Harris PC. The polycystic kidney disease 1 (PKD1) gene encodes a novel protein with multiple cell recognition domains. Nat Genet 1995, 10:151-160. 10.1038/ng0695-151, 7663510.
24. Ibraghimov-Beskrovnaya O, Bukanov NO, Donohue LC, Dackowski WR, Klinger KW, Landes GM. Strong homophilic interactions of the Ig-like domains of polycystin-1, the protein product of an autosomal dominant polycystic kidney disease gene, PKD1. Hum Mol Genet 2000, 9:1641-1649. 10.1093/hmg/9.11.1641, 10861291.
25. Ferris PJ, Waffenschmidt S, Umen JG, Lin H, Lee JH, Ishida K, Kubo T, Lau J, Goodenough UW. Plus and minus sexual agglutinins from Chlamydomonas reinhardtii. Plant Cell 2005, 17:597-615. 10.1105/tpc.104.028035, 548829, 15659633.
26. Adair WS, Monk BC, Cohen R, Hwang C, Goodenough UW. Sexual agglutinins from the Chlamydomonas flagellar membrane Partial purification and characterization. J Biol Chem 1982, 257:4593-4602.
27. Elbein AD, Solf R, Dorling PR, Vosbeck K. Swainsonine: an inhibitor of glycoprotein processing. Proc Natl Acad Sci USA 1981, 78:7393-7397. 10.1073/pnas.78.12.7393, 349273, 6801650.
28. Elbein AD, Dorling PR, Vosbeck K, Horisberger M. Swainsonine prevents the processing of the oligosaccharide chains of influenza virus hemagglutinin. J Biol Chem 1982, 257:1573-1576.
29. Nieminen J, St-Pierre C, Sato S. Galectin-3 interacts with naive and primed neutrophils, inducing innate immune responses. J Leukoc Biol 2005, 78:1127-1135.
30. Huang K, Diener DR, Mitchell A, Pazour GJ, Witman GB, Rosenbaum JL. Function and dynamics of PKD2 in Chlamydomonas reinhardtii flagella. J Cell Biol 2007, 179:501-514. 10.1083/jcb.200704069, 2064795, 17984324.
31. Wang Q, Snell WJ. Wheat germ agglutinin induces mating reactions in Chlamydomonas eugametos by cross-linking agglutinin-associated glycoproteins in the flagellar membrane. J Biol Chem 1989, 109:1677-1687.
32. Rieder CL, Jensen CG, Jensen LC. The resorption of primary cilia during mitosis in a vertebrate (PtK1) cell line. J Ultrastruct Res 1979, 68:173-185. 10.1016/S0022-5320(79)90152-7, 480410.
33. Weidner KM, Sachs M, Birchmeier W. The Met receptor tyrosine kinase transduces motility, proliferation, and morphogenic signals of scatter factor/hepatocyte growth factor in epithelial cells. J Cell Biol 1993, 121:145-154. 10.1083/jcb.121.1.145, 2119778, 8384622.
34. Ward S, Thomson N, White JG, Brenner S. Electron microscopical reconstruction of the anterior sensory anatomy of the nematode Caenorhabditis elegans.?2UU. J Comp Neurol 1975, 160:313-337. 10.1002/cne.901600305, 1112927.
35. Adair WS, Hwang C, Goodenough UW. Identification and visualization of the sexual agglutinin from the mating-type plus flagellar membrane of Chlamydomonas. Cell 1983, 33:183-193. 10.1016/0092-8674(83)90347-1, 6678609.
36. Zhang Q, Young TF, Ross RF. Glycolipid receptors for attachment of Mycoplasma hyopneumoniae to porcine respiratory ciliated cells. Infect Immun 1994, 62:4367-4373. 303118, 7927697.
37. Tuomanen E, Towbin H, Rosenfelder G, Braun D, Larson G, Hansson GC, Hill R. Receptor analogs and monoclonal antibodies that inhibit adherence of Bordetella pertussis to human ciliated respiratory epithelial cells. J Exp Med 1988, 168:267-277. 10.1084/jem.168.1.267, 2188977, 2899620.
38. Saukkonen K, Burnette WN, Mar VL, Masure HR, Tuomanen EI. Pertussis toxin has eukaryotic-like carbohydrate recognition domains. Proc Natl Acad Sci USA 1992, 89:118-122. 10.1073/pnas.89.1.118, 48187, 1729677.
39. Snell WJ, Moore WS. Aggregation-dependent turnover of flagellar adhesion molecules in Chlamydomonas gametes. J Cell Biol 1980, 84:203-210. 10.1083/jcb.84.1.203, 2110524, 7350168.
40. Christensen ST, Ott CM. Cell signaling. A ciliary signaling switch. Science 2007, 317:330-331. 10.1126/science.1146180, 17641189.
41. Praetorius HA, Spring KR. Bending the MDCK cell primary cilium increases intracellular calcium. J Membr Biol 2001, 184:71-79. 10.1007/s00232-001-0075-4, 11687880.