Microtubules and cadherins: A neglected partnership

Frontiers in Bioscience

Volumn 14, Issue 8, 2009, Pages 3159-3167

  Stehbens, Samantha J ^a   Akhmanova, Anna ^b   Yap, Alpha S ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

Adherens junction; Cell cell contact; E cadherin; Epithelia; Microtubule; Review

Indexed keywords

CADHERIN;

CELL COMMUNICATION; HUMAN; MICROTUBULE; PHYSIOLOGY; REVIEW;

CADHERINS; CELL COMMUNICATION; HUMANS; MICROTUBULES;

EID: 63849176160     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2735/3442     Document Type: Article

References (69)

1. Gumbiner, B. M.: Regulation of cadherin-mediated adhesion in morphogenesis. Nat Rev Mol Cell Biol, 6, 622- 34 (2005). (Pubitemid 41081266)
2. Yap, A. S.: The morphogenetic role of cadherin cell adhesion molecules in human cancer: a thematic review. Cancer Investigation, 16, 252-261 (1998). (Pubitemid 28211011)
3. Mege, R. M., J. Gavard & M. Lambert: Regulation of cell-cell junctions by the cytoskeleton. Curr Opin Cell Biol, 18, 541-8 (2006). (Pubitemid 44349065)
4. Yap, A. S. & E. M. Kovacs: Direct cadherin-activated cell signaling: a view from the plasma membrane. J. Cell Biol., 160, 11-16 (2003). (Pubitemid 36091712)
5. Xiao, K., R. G. Oas, C. M. Chiasson & A. P. Kowalczyk: Role of p120-catenin in cadherin trafficking. Biochim Biophys Acta, 1773, 8-16 (2007). (Pubitemid 44914097)
6. Keating, T. J. & G. G. Borisy: Centrosomal and noncentrosomal microtubules. Biol Cell, 91, 321-9 (1999).
7. Meads, T. & T. A. Schroer: Polarity and nucleation of microtubules in polarized epithelial cells. Cell Motil Cytoskeleton, 32, 273-288 (1995).
8. Bre, M. H., R. Pepperkok, A. M. Hill, N. Levilliers, W. Ansorge, E. H. Stelzer & E. Karsenti: Regulation of microtubule dynamics and nucleation during polarization in MDCK II cells. J Cell Biol, 111, 3013-21 (1990). (Pubitemid 120034039)
9. Reilein, A., S. Yamada & W. J. Nelson: Selforganization of an acentrosomal microtubule network at the basal cortex of polarized epithelial cells. J Cell Biol, 171, 845-55 (2005). (Pubitemid 41746586)
10. Stehbens, S. J., A. D. Paterson, M. S. Crampton, A. M. Shewan, C. Ferguson, A. Akhmanova, R. G. Parton & A. S. Yap: Dynamic microtubules regulate the local concentration of E-cadherin at cell-cell contacts. J Cell Sci, 119, 1801-11 (2006). (Pubitemid 43811006)
11. Ligon, L. A., S. Karki, M. Tokito & E. L. Holzbaur: Dynein binds to beta-catenin and may tether microtubules at adherens junctions. Nat Cell Biol, 3, 913-7 (2001). (Pubitemid 32952256)
12. Lechler, T. & E. Fuchs: Desmoplakin: an unexpected regulator of microtubule organization in the epidermis. J Cell Biol, 176, 147-54 (2007). (Pubitemid 46143255)
13. Bacallao, R., C. Antony, E. Karsenti, E. Stelzer & K. Simons: The subcellular organization of Madin-Darby Canine Kidney cells during the formation of a polarized epithelium. J. Cell Biol., 109, 2817-2832 (1989). (Pubitemid 20011909)
14. Jaulin, F., X. Xue, E. Rodriguez-Boulan & G. Kreitzer: Polarization-dependent selective transport to the apical membrane by KIF5B in MDCK cells. Dev Cell, 13, 511-22 (2007). (Pubitemid 47500806)
15. Bre, M. H., T. E. Kreis & E. Karsenti: Control of microtubule nucleation and stability in Madin-Darby canine kidney cells: the occurrence of noncentrosomal, stable detyrosinated microtubules. J Cell Biol, 105, 1283-96 (1987). (Pubitemid 18029852)
16. Kaufmann, U., J. Kirsch, A. Irintchev, A. Wernig & A. Starzinski-Powitz: The M-cadherin catenin complex interacts with microtubules in skeletal muscle cells: implications for the fusion of myoblasts. J Cell Sci, 112 ( Pt 1), 55-68 (1999).
17. Ligon, L. A. & E. L. Holzbaur: Microtubules tethered at epithelial cell junctions by dynein facilitate efficient junction assembly. Traffic, 8, 808-19 (2007). (Pubitemid 46971629)
18. Waterman-Storer, C. M., W. C. Salmon & E. D. Salmon: Feedback interactions between cell-cell adherens junctions and cytoskeletal dynamics in newt lung epithelial cells. Mol Biol Cell, 11, 2471-83 (2000). (Pubitemid 30489928)
19. Carramusa, L., C. Ballestrem, Y. Zilberman & A. D. Bershadsky: Mammalian diaphanous-related formin Dia1 controls the organization of E-cadherin-mediated cell-cell junctions. J Cell Sci (2007).
20. Shaw, R. M., A. J. Fay, M. A. Puthenveedu, M. von Zastrow, Y. N. Jan & L. Y. Jan: Microtubule plus-end-tracking proteins target gap junctions directly from the cell interior to adherens junctions. Cell, 128, 547-60 (2007). (Pubitemid 46198893)
21. Reipert, S., H. Kotisch, B. Wysoudil & G. Wiche: Rapid Microwave Fixation of Cell Monolayers Preserves Microtubule-associated Cell Structures. J Histochem Cytochem (2008).
22. Moss, D. K., G. Bellett, J. M. Carter, M. Liovic, J. Keynton, A. R. Prescott, E. B. Lane & M. M. Mogensen: Ninein is released from the centrosome and moves bidirectionally along microtubules. J Cell Sci, 120, 3064-74 (2007). (Pubitemid 47517089)
23. Chausovsky, A., A. D. Bershadsky & G. G. Borisy: Cadherin-mediated regulation of microtubule dynamics. Nat. Cell Biol., 2, 797-804 (2000).
24. Nagasaki, T., C. J. Chapin & G. G. Gundersen: Distribution of detyrosinated microtubules in motile NRK fibroblasts is rapidly altered upon cell-cell contact: implications for contact inhibition of locomotion. Cell Motil Cytoskeleton, 23, 45-60 (1992).
25. Braga, V. M. & A. S. Yap: The challenges of abundance: epithelial junctions and small GTPase signalling. Curr Opin Cell Biol, 17, 466-74 (2005). (Pubitemid 41267160)
26. Yamada, S. & W. J. Nelson: Localized zones of Rho and Rac activities drive initiation and expansion of epithelial cell cell adhesion. J Cell Biol, 178, 517-27 (2007). (Pubitemid 47196158)
27. Wittmann, T., G. M. Bokoch & C. M. Waterman-Storer: Regulation of leading edge microtubule and actin dynamics downstream of Rac1. J Cell Biol, 161, 845-51 (2003). (Pubitemid 36718418)
28. Akhmanova, A. & C. C. Hoogenraad: Microtubule plusend- tracking proteins: mechanisms and functions. Curr Opin Cell Biol, 17, 47-54 (2005). (Pubitemid 40138087)
29. Gundersen, G. G.: Evolutionary conservation of microtubule-capture mechanisms. Nat Rev Mol Cell Biol, 3, 296-304 (2002). (Pubitemid 34619265)
30. Fukata, M., T. Watanabe, J. Noritake, M. Nakagawa, M. Yamaga, S. Kuroda, Y. Matsuura, A. Iwamatsu, F. Perez & K. Kaibuchi: Rac1 and Cdc42 capture microtubules through IQGAP1 and CLIP-170. Cell, 109, 873-85 (2002). (Pubitemid 34786002)
31. Kuroda, S., M. Fukata, M. Nakagawa, K. Fujii, T. Nakamura, t. Ookubo, I. Izawa, T. Nagase, N. Nomura, H. Tani, I. Shoji, Y. Matsuura, S. Yonehara & K. Kaibuchi: Role of IQGAP1, a target of the small GTPases Cdc42 and Rac1, in regulation of E-cadherin-mediated cell-cell adhesion. Science, 281, 832-835 (1998). (Pubitemid 28376045)
32. Askham, J. M., P. Moncur, A. F. Markham & E. E. Morrison: Regulation and function of the interaction between the APC tumour suppressor protein and EB1. Oncogene, 19, 1950-8 (2000). (Pubitemid 30219038)
33. Jimbo, T., Y. Kawasaki, R. Koyama, R. Sato, S. Takada, K. Haraguchi & T. Akiyama: Identification of a link between the tumour suppressor APC and the kinesin superfamily. Nat Cell Biol, 4, 323-7 (2002). (Pubitemid 34308860)
34. Mimori-Kiyosue, Y., N. Shiina & S. Tsukita: Adenomatous polyposis coli (APC) protein moves along microtubules and concentrates at their growing ends in epithelial cells. J Cell Biol, 148, 505-18 (2000).
35. Su, L. K., M. Burrell, D. E. Hill, J. Gyuris, R. Brent, R. Wiltshire, J. Trent, B. Vogelstein & K. W. Kinzler: APC binds to the novel protein EB1. Cancer Res, 55, 2972-7 (1995).
36. Rosin-Arbesfeld, R., G. Ihrke & M. Bienz: Actindependent membrane association of the APC tumour suppressor in polarized mammalian epithelial cells. EMBOJ., 20, 5929-5939 (2001). (Pubitemid 33049268)
37. Townsley, F. M. & M. Bienz: Actin-dependent membrane association of a Drosophila epithelial APC protein and its effect on junctional Armadillo. Curr Biol, 10, 1339-48 (2000).
38. Barth, A. I., K. A. Siemers & W. J. Nelson: Dissecting interactions between EB1, microtubules and APC in cortical clusters at the plasma membrane. J Cell Sci, 115, 1583-90 (2002). (Pubitemid 34520588)
39. Watanabe, T., S. Wang, J. Noritake, K. Sato, M. Fukata, M. Takefuji, M. Nakagawa, N. Izumi, T. Akiyama & K. Kaibuchi: Interaction with IQGAP1 links APC to Rac1, Cdc42, and actin filaments during cell polarization and migration. Dev Cell, 7, 871-83 (2004). (Pubitemid 39654731)
40. Wen, Y., C. H. Eng, J. Schmoranzer, N. Cabrera-Poch, E. J. Morris, M. Chen, B. J. Wallar, A. S. Alberts & G. G. Gundersen: EB1 and APC bind to mDia to stabilize microtubules downstream of Rho and promote cell migration. Nat Cell Biol, 6, 820-30 (2004). (Pubitemid 39207247)
41. Karakesisoglou, I., Y. Yang & E. Fuchs: An epidermal plakin that integrates actin and microtubule networks at cellular junctions. J Cell Biol, 149, 195-208 (2000). (Pubitemid 30196709)
42. Kodama, A., I. Karakesisoglou, E. Wong, A. Vaezi & E. Fuchs: ACF7: an essential integrator of microtubule dynamics. Cell, 115, 343-54 (2003). (Pubitemid 37487707)
43. Yap, A. S., B. R. Stevenson, K. C. Abel, E. J. Cragoe, Jr. & S. W. Manley: Microtubule integrity is necessary for the barrier function of cultured thyroid cell monolayers. Experimental Cell Research, 218, 540-550 (1995).
44. Laplante, I., R. Beliveau & J. Paquin: RhoA/ROCK and Cdc42 regulate cell-cell contact and N-cadherin protein level during neurodetermination of P19 embryonal stem cells. J Neurobiol, 60, 289-307 (2004). (Pubitemid 39031261)
45. Lorenowicz, M. J., M. Fernandez-Borja, A. M. van Stalborch, M. A. van Sterkenburg, P. S. Hiemstra & P. L. Hordijk: Microtubule dynamics and Rac-1 signaling independently regulate barrier function in lung epithelial cells. Am J Physiol Lung Cell Mol Physiol, 293, L1321-31 (2007). (Pubitemid 350159417)
46. Kee, S. H. & P. M. Steinert: Microtubule disruption in keratinocytes induces cell-cell adhesion through activation of endogenous E-cadherin. Mol Biol Cell, 12, 1983-93 (2001). (Pubitemid 33049693)
47. Jordan, M. A. & L. Wilson: Use of drugs to study role of microtubule assembly dynamics in living cells. Methods Enzymol, 298, 252-276 (1998). (Pubitemid 28450758)
48. Perez, F., G. S. Diamantopoulos, R. Stalder & T. E. Kreis: CLIP-170 highlights growing microtubule ends in vivo. Cell, 96, 517-27 (1999). (Pubitemid 29106839)
49. Bryant, D. M. & J. L. Stow: The ins and outs of Ecadherin trafficking. Trends Cell Biol, 14, 427-34 (2004).
50. Chen, Y.-H., D. B. Stewart & W. J. Nelson: Coupling assembly of the E-cadherin/β-catenin complex to efficient endoplasmic reticulum exit and basal-lateral membrane targeting of E-cadherin in polarized MDCK cells. J. Cell Biol., 144, 687-699 (1999). (Pubitemid 29234547)
51. Le, T. L., A. S. Yap & J. L. Stow: Recycling of Ecadherin: a potential mechanism for regulating cadherin dynamics. J. Cell Biol., 146, 219-232 (1999). (Pubitemid 29349976)
52. Lock, J. G. & J. L. Stow: Rab11 in Recycling Endosomes Regulates the Sorting and Basolateral Transport of E-Cadherin. Mol Biol Cell (2005).
53. Mary, S., S. Charrasse, M. Meriane, F. Comunale, P. Travo, A. Blangy & C. Gauthier-Rouviere: Biogenesis of N-Cadherin-dependent Cell-Cell Contacts in Living Fibroblasts Is a Microtubule-dependent Kinesin-driven Mechanism. Mol Biol Cell, 13, 285-301. (2002). (Pubitemid 34106076)
54. Chen, X., S. Kojima, G. G. Borisy & K. J. Green: p120 catenin associates with kinesin and facilitates the transport of cadherin-catenin complexes to intercellular junctions. J. Cell Biol., 163, 547-557 (2003). (Pubitemid 37429868)
55. Yanagisawa, M., I. N. Kaverina, A. Wang, Y. Fujita, A. B. Reynolds & P. Z. Anastasiadis: A novel interaction between kinesin and p120 modulates p120 localization and function. J Biol Chem, 279, 9512-9521 (2004). (Pubitemid 38296019)
56. Teng, J., T. Rai, Y. Tanaka, Y. Takei, T. Nakata, M. Hirasawa, A. B. Kulkarni & N. Hirokawa: The KIF3 motor transports N-cadherin and organizes the developing neuroepithelium. Nat Cell Biol, 7, 474-82 (2005). (Pubitemid 40637407)
57. Lien, W. H., O. Klezovitch, T. E. Fernandez, J. Delrow & V. Vasioukhin: alphaE-catenin controls cerebral cortical size by regulating the hedgehog signaling pathway. Science, 311, 1609-12 (2006).
58. Perrais, M., X. Chen, M. Perez-Moreno & B. M. Gumbiner: E-cadherin homophilic ligation inhibits cell growth and epidermal growth factor receptor signaling independently of other cell interactions. Mol Biol Cell, 18, 2013-25 (2007). (Pubitemid 46911354)
59. Rodriguez, O. C., A. W. Schaefer, C. A. Mandato, P. Forscher, W. M. Bement & C. M. Waterman-Storer: Conserved microtubule-actin interactions in cell movement and morphogenesis. Nat Cell Biol, 5, 599-609 (2003). (Pubitemid 36818081)
60. Kawasaki, Y., T. Senda, T. Ishidate, R. Koyama, T. Morishita, Y. Iwayama, O. Higuchi & T. Akiyama: Asef, a link between the tumor suppressor APC and G-protein signaling. Science, 289, 1194-7 (2000). (Pubitemid 30650732)
61. Kitano, M., M. Nakaya, T. Nakamura, S. Nagata & M. Matsuda: Imaging of Rab5 activity identifies essential regulators for phagosome maturation. Nature (2008).
62. Rogers, S. L., U. Wiedemann, U. Hacker, C. Turck & R. D. Vale: Drosophila RhoGEF2 associates with microtubule plus ends in an EB1-dependent manner. Curr Biol, 14, 1827-33 (2004). (Pubitemid 39408772)
63. Parks, S. & E. Wieschaus: The Drosophila gastrulation gene concertina encodes a G alpha-like protein. Cell, 64, 447-58 (1991). (Pubitemid 121001268)
64. Shewan, A. M., M. Maddugoda, A. Kraemer, S. J. Stehbens, S. Verma, E. M. Kovacs & A. S. Yap: Myosin 2 Is a Key Rho Kinase Target Necessary for the Local Concentration of E-Cadherin at Cell-Cell Contacts. Mol Biol Cell, 16, 4531-4532 (2005).
65. Schultz, T., M. Schmuel, T. Hyman & Y. Altschuler: btubulin cofactor D and ARL2 take part in apical junctional complex disassembly and abrogate epithelial structure. FASB J., 22, 168-182 (2008).
66. Ivanov, A. I., I. C. McCall, B. Babbin, S. N. Samarin, A. Nusrat & C. A. Parkos: Microtubules regulate disassembly of epithelial apical junctions. BMC Cell Biol, 7, 12 (2006).
67. Gumbiner, B., B. Stevenson & A. Grimaldi: The role of the cell adhesion molecule uvomorulin in the formation and maintenance of the epithelial junctional complex. J. Cell Biol., 197, 1575-1587 (1988).
68. Wheelock, M. J. & P. J. Jensen: Regulation of keratinocyte intercellular junction organization and epidermal morphogenesis by E-cadherin. J Cell Biol, 117, 415-25 (1992).
69. Nejsum, L. N. & W. J. Nelson: A molecular mechanism directly linking E-cadherin adhesion to initiation of epithelial cell surface polarity. J Cell Biol, 178, 323-35 (2007). (Pubitemid 47076467)