Cortical control of microtubule stability and polarization

Current Opinion in Cell Biology

Volumn 16, Issue 1, 2004, Pages 106-112

  Gundersen, Gregg G ^a   Gomes, Edgar R ^a   Wen, Ying ^a  

^a Black Building 1217 ^*  (United States)

Author keywords

Adenomatous polyposis coli protein; APC; CLASP; CLIP 170; CLIP associated protein; Cytoplasmic linker protein 170; LPA; Lysophosphatidic acid; Microtubule; Microtubule organizing center; MT; MTOC; PKC; Protein kinase C; SPB; Spindle pole body

Indexed keywords

RHO GUANINE NUCLEOTIDE BINDING PROTEIN;

CELL DIVISION; CELL POLARITY; CYTOSKELETON; INTERPHASE; MICROTUBULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CELL DIVISION; MICROTUBULES; RHO GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION;

EID: 1642265093     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ceb.2003.11.010     Document Type: Review

References (69)

1. Howard J., Hyman A.A. Dynamics and mechanics of the microtubule plus end. Nature. 422:2003;753-758.
2. Kirschner M., Mitchison T. Beyond self-assembly: from microtubules to morphogenesis. Cell. 45:1986;329-342.
3. Liao G., Nagasaki T., Gundersen G.G. Low concentrations of nocodazole interfere with fibroblast locomotion without significantly affecting microtubule level: implications for the role of dynamic microtubules in cell locomotion. J. Cell. Sci. 108:1995;3473-3483.
4. Tanaka E., Ho T., Kirschner M.W. The role of microtubule dynamics in growth cone motility and axonal growth. J. Cell. Biol. 128:1995;139-155.
5. Adames N.R., Cooper J.A. Microtubule interactions with the cell cortex causing nuclear movements in Saccharomyces cerevisiae. J. Cell. Biol. 149:2000;863-874.
6. Cook T.A., Nagasaki T., Gundersen G.G. Rho guanosine triphosphatase mediates the selective stabilization of microtubules induced by lysophosphatidic acid. J. Cell. Biol. 141:1998;175-185.
7. Fukata M., Watanabe T., Noritake J., Nakagawa M., Yamaga M., Kuroda S., Matsuura Y., Iwamatsu A., Perez F., Kaibuchi K. Rac1 and Cdc42 capture microtubules through IQGAP1 and CLIP-170. Cell. 109:2002;873-885 Rac1/Cdc42, IQGAP and CLIP-170 form a tripartite complex to capture and transiently stabilize MTs. Disruption of the interaction results in altered MT arrays or cells with multiple leading edges.
8. Brunner D., Nurse P. CLIP170-like tip1p spatially organizes microtubular dynamics in fission yeast. Cell. 102:2000;695-704.
9. Schuyler S.C., Pellman D. Microtubule 'plus-end-tracking proteins': the end is just the beginning. Cell. 105:2001;421-424.
10. Carvalho P., Tirnauer J.S., Pellman D. Surfing on microtubule ends. Trends Cell. Biol. 13:2003;229-237.
11. Galjart N., Perez F. A plus-end raft to control microtubule dynamics and function. Curr. Opin. Cell. Biol. 15:2003;48-53.
12. Wittmann T., Waterman-Storer C.M. Cell motility: can Rho GTPases and microtubules point the way? J. Cell. Sci. 114:2001;3795-3803.
13. Labbe J.C., Maddox P.S., Salmon E.D., Goldstein B. PAR proteins regulate microtubule dynamics at the cell cortex in C. elegans. Curr. Biol. 13:2003;707-714 MT dynamics in the anterior and posterior cortex during anaphase B are determined by measuring the time that a MT remains at the cortex. In wild-type embryos, MTs are more dynamic in the posterior cortex and depletion of Par-1 by RNAi does not affect this asymmetry. On the other hand, analysis of Par-2, Par-3 and Par-2/Par-3 (RNAi) mutants suggests that Par-3 stabilizes MT and that the effect of Par-2 on MT dynamics is due to the displacement of Par-3. Goa1 and Goa-16 depletion disrupt the asymmetry in MT dynamics, independently of Par-2 and Par-3.
14. ••], they find Cdc28 localized on both SPBs and on MT tips. Transportation of both Cdc28 and Kar9 to MT tips requires a plus-end-directed kinesin Kip2.
15. Liakopoulos D., Kusch J., Grava S., Vogel J., Barral Y. Asymmetric loading of Kar9 onto spindle poles and microtubules ensures proper spindle alignment. Cell. 112:2003;561-574 Kar9 associates with budward-directed SPBs and MTs. Photobleaching experiments show that Kar9 localization at MT tips is due to Kap 9 loading at SPBs rather than from cortical sites. Cdc28-Clb3 and -Clb4 phosphorylate Kar9. Clb-4 is localized at the mother-bound SPB so activated Cdc28 will prevent Kar9 association.
16. Palazzo AF, Eng CE, Schlaepfer DD, Marcantonio EE, Gundersen GG: Localized stabilization of miicrotubules by integrin and FAK facilitated Rho signaling. Science 2003, in press. This paper shows that integrins and FAK regulate the ability of Rho to activate mDia to induce MT stabilization. FAK appears to regulate mDia activation indirectly by regulating the trafficking of a GM1 (ganglioside) lipid domain at the leading edge of migrating cells.
17. Etienne-Manneville S., Hall A. Rho GTPases in cell biology. Nature. 420:2002;629-635.
18. Stowers L., Yelon D., Berg L.J., Chant J. Regulation of the polarization of T cells toward antigen-presenting cells by Ras-related GTPase CDC42. Proc. Natl. Acad. Sci. U S A. 92:1995;5027-5031.
19. Palazzo A.F., Joseph H.L., Chen Y.J., Dujardin D.L., Alberts A.S., Pfister K.K., Vallee R.B., Gundersen G.G. Cdc42, dynein, and dynactin regulate MTOC reorientation independent of Rho-regulated microtubule stabilization. Curr. Biol. 11:2001;1536-1541.
20. Etienne-Manneville S., Hall A. Integrin-mediated activation of Cdc42 controls cell polarity in migrating astrocytes through PKCζ Cell. 106:2001;489-498.
21. Tzima E., Kiosses W.B., del Pozo M.A., Schwartz M.A. Localized cdc42 activation, detected using a novel assay, mediates microtubule organizing center positioning in endothelial cells in response to fluid shear stress. J. Biol. Chem. 278:2003;31020-31023 Shear stress polarizes Cdc42 activation in the direction of flow to induce MTOC reorientation in endothelial cells.
22. Gotta M., Abraham M.C., Ahringer J. CDC-42 controls early cell polarity and spindle orientation in C. elegans. Curr. Biol. 11:2001;482-488.
23. Kay A.J., Hunter C.P. CDC-42 regulates PAR protein localization and function to control cellular and embryonic polarity in C. elegans. Curr. Biol. 11:2001;474-481.
24. Etienne-Manneville S., Hall A. Cdc42 regulates GSK-3β and adenomatous polyposis coli to control cell polarity. Nature. 421:2003;753-756 Cdc42 activation of Par6/PKCζ is shown to regulate MTOC reorientation in migrating astrocytes by inhibiting GSK3β. GSK3β may regulate MTOC reorientation through its action on APC.
25. Palazzo A.F., Cook T.A., Alberts A.S., Gundersen G.G. mDia mediates Rho-regulated formation and orientation of stable microtubules. Nat. Cell. Biol. 3:2001;723-729.
26. Infante A.S., Stein M.S., Zhai Y., Borisy G.G., Gundersen G.G. Detyrosinated (Glu) microtubules are stabilized by an ATP-sensitive plus-end cap. J. Cell. Sci. 113:2000;3907-3919.
27. Kohno H., Tanaka K., Mino A., Umikawa M., Imamura H., Fujiwara T., Fujita Y., Hotta K., Qadota H., Watanabe T.et al. Bni1p implicated in cytoskeletal control is a putative target of Rho1p small GTP binding protein in Saccharomyces cerevisiae. EMBO J. 15:1996;6060-6068.
28. Lee L., Klee S.K., Evangelista M., Boone C., Pellman D. Control of mitotic spindle position by the Saccharomyces cerevisiae formin Bni1p. J. Cell. Biol. 144:1999;947-961.
29. Gundersen G.G. Evolutionary conservation of microtubule-capture mechanisms. Nat. Rev. Mol. Cell. Biol. 3:2002;296-304.
30. Daub H., Gevaert K., Vandekerckhove J., Sobel A., Hall A. Rac/Cdc42 and p65PAK regulate the microtubule-destabilizing protein stathmin through phosphorylation at serine 16. J. Biol. Chem. 276:2001;1677-1680.
31. Wittmann T., Bokoch G.M., Waterman-Storer C.M. Regulation of leading edge microtubule and actin dynamics downstream of Rac1. J. Cell. Biol. 161:2003;845-851 Rac1 is shown to promote MT plus end growth and turnover in PtK1 cells.
32. Bloom K. It's a kar9ochore to capture microtubules. Nat. Cell. Biol. 2:2000;E96-E98.
33. Lee L., Tirnauer J.S., Li J., Schuyler S.C., Liu J.Y., Pellman D. Positioning of the mitotic spindle by a cortical-microtubule capture mechanism. Science. 287:2000;2260-2262.
34. Korinek W.S., Copeland M.J., Chaudhuri A., Chant J. Molecular linkage underlying microtubule orientation toward cortical sites in yeast. Science. 287:2000;2257-2259.
35. Gundersen G.G. Microtubule capture: IQGAP and CLIP-170 expand the repertoire. Curr. Biol. 12:2002;R645-R647.
36. Miller R.K., Rose M.D. Kar9p is a novel cortical protein required for cytoplasmic microtubule orientation in yeast. J. Cell. Biol. 140:1998;377-390.
37. Yin H., Pruyne D., Huffaker T.C., Bretscher A. Myosin V orientates the mitotic spindle in yeast. Nature. 406:2000;1013-1015.
38. Bretscher A. Polarized growth and organelle segregation in yeast: the tracks, motors, and receptors. J. Cell. Biol. 160:2003;811-816.
39. ••] show that Kar9-associated MTs do not search for the bud cortex; rather, they bind to Myo2 and are actively transported on actin cables to the bud tip. Myo2 localizes to MT plus ends. Cells with Myo2 mutants with a slower velocity also show reduced cytoplasmic MT movement.
40. Heil-Chapdelaine R.A., Oberle J.R., Cooper J.A. The cortical protein Num1p is essential for dynein-dependent interactions of microtubules with the cortex. J. Cell. Biol. 151:2000;1337-1344.
41. Farkasovsky M., Kuntzel H. Cortical Num1p interacts with the dynein intermediate chain Pac11p and cytoplasmic microtubules in budding yeast. J. Cell. Biol. 152:2001;251-262.
42. ••]). The localization is lost in Pac1 (LIS1)-deleted cells and enhanced in cells lacking Num1 or Arp1 (a dynactin component). This suggests that dynein is delivered on MTs to the cortex where it generates forces for MT sliding.
43. Glued) results in enhanced dynein association with MTs.
44. Perez F., Diamantopoulos G.S., Stalder R., Kreis T.E. CLIP-170 highlights growing microtubule ends in vivo. Cell. 96:1999;517-527.
45. Faulkner N.E., Dujardin D.L., Tai C.Y., Vaughan K.T., O'Connell C.B., Wang Y., Vallee R.B. A role for the lissencephaly gene LIS1 in mitosis and cytoplasmic dynein function. Nat. Cell. Biol. 2:2000;784-791.
46. Lin H., de Carvalho P., Kho D., Tai C.Y., Pierre P., Fink G.R., Pellman D. Polyploids require Bik1 for kinetochore-microtubule attachment. J. Cell. Biol. 155:2001;1173-1184.
47. Coquelle F.M., Caspi M., Cordelieres F.P., Dompierre J.P., Dujardin D.L., Koifman C., Martin P., Hoogenraad C.C., Akhmanova A., Galjart N.et al. LIS1, CLIP-170's key to the dynein/dynactin pathway. Mol Cell Biol. 22:2002;3089-3102 The MT tip protein CLIP-170 is shown to interact with dynein/dynactin through LIS1.
48. Han G., Liu B., Zhang J., Zuo W., Morris N.R., Xiang X. The Aspergillus cytoplasmic dynein heavy chain and NUDF localize to microtubule ends and affect microtubule dynamics. Curr. Biol. 11:2001;719-724.
49. Suelmann R., Sievers N., Fischer R. Nuclear traffic in fungal hyphae: in vivo study of nuclear migration and positioning in Aspergillus nidulans. Mol. Microbiol. 25:1997;757-769.
50. Vaughan K.T., Tynan S.H., Faulkner N.E., Echeverri C.J., Vallee R.B. Colocalization of cytoplasmic dynein with dynactin and CLIP-170 at microtubule distal ends. J. Cell. Sci. 112:1999;1437-1447.
51. Dujardin DL, Barnhart LE, Stehman S, Gomes ER, Gundersen GG, Vallee RB: A role for cytoplasmic dynein in directed cell movement. J Cell Biol 2003, in press. Dynein, dynactin and Lis1 are localized at the leading edge of a migrating cell. Disruption of dynein or dynactin inhibits cell migration.
52. Akhmanova A., Hoogenraad C.C., Drabek K., Stepanova T., Dortland B., Verkerk T., Vermeulen W., Burgering B.M., De Zeeuw C.I., Grosveld F., Galjart N. CLASPS are CLIP-115 and -170 associating proteins involved in the regional regulation of microtubule dynamics in motile fibroblasts. Cell. 104:2001;923-935.
53. Mata J., Nurse P. tea1 and the microtubular cytoskeleton are important for generating global spatial order within the fission yeast cell. Cell. 89:1997;939-949.
54. Snaith H.A., Sawin K.E. Fission yeast mod5p regulates polarized growth through anchoring of tea1p at cell tips. Nature. 423:2003;647-651 Mod5 is identified as a cortical receptor for tea1. In mod5-deletion cells, tea1 is transported efficiently to MT tips, but it does not accumulate normally at cell tips.
55. Allan V., Nathke I.S. Catch and pull a microtubule: getting a grasp on the cortex. Nat. Cell. Biol. 3:2001;E226-E228.
56. Mimori-Kiyosue Y., Shiina N., Tsukita S. Adenomatous polyposis coli (APC) protein moves along microtubules and concentrates at their growing ends in epithelial cells. J. Cell. Biol. 148:2000;505-518.
57. Kaverina I., Krylyshkina O., Small J.V. Microtubule targeting of substrate contacts promotes their relaxation and dissociation. J. Cell. Biol. 146:1999;1033-1044.
58. Krylyshkina O., Anderson K.I., Kaverina I., Upmann I., Manstein D.J., Small J.V., Toomre D.K. Nanometer targeting of microtubules to focal adhesions. J. Cell. Biol. 161:2003;853-859 Using total-internal-reflection fluorescence microscopy, polymerizing MTs are shown to approach within 50 nm of focal adhesions. Shrinking MTs quickly move away from the cortex, suggesting that they may track along cortical elements during MT growth.
59. •]. Fluorescence speckle microscopy of the actin and MT cytoskeletons shows that the two polymers are coordinately moved rearward in the cell body.
60. •] of coordinated movements of actin and MTs, but in neuronal growth cones.
61. Ligon L.A., Karki S., Tokito M., Holzbaur E.L. Dynein binds to β-catenin and may tether microtubules at adherens junctions. Nat. Cell. Biol. 3:2001;913-917.
62. Heil-Chapdelaine R.A., Adames N.R., Cooper J.A. Formin' the connection between microtubules and the cell cortex. J. Cell. Biol. 144:1999;809-811.
63. Wallenfang M.R., Seydoux G. Polarization of the anterior-posterior axis of C. elegans is a microtubule-directed process. Nature. 408:2000;89-92.
64. Grill S.W., Gonczy P., Stelzer E.H., Hyman A.A. Polarity controls forces governing asymmetric spindle positioning in the Caenorhabditis elegans embryo. Nature. 409:2001;630-633.
65. Etemad-Moghadam B., Guo S., Kemphues K.J. Asymmetrically distributed PAR-3 protein contributes to cell polarity and spindle alignment in early C. elegans embryos. Cell. 83:1995;743-752.
66. Hung T.J., Kemphues K.J. PAR-6 is a conserved PDZ domain-containing protein that colocalizes with PAR-3 in Caenorhabditis elegans embryos. Development. 126:1999;127-135.
67. Tabuse Y., Izumi Y., Piano F., Kemphues K.J., Miwa J., Ohno S. Atypical protein kinase C cooperates with PAR-3 to establish embryonic polarity in Caenorhabditis elegans. Development. 125:1998;3607-3614.
68. Skop A.R., White J.G. The dynactin complex is required for cleavage plane specification in early Caenorhabditis elegans embryos. Curr. Biol. 8:1998;1110-1116.
69. Gonczy P., Pichler S., Kirkham M., Hyman A.A. Cytoplasmic dynein is required for distinct aspects of MTOC positioning, including centrosome separation, in the one cell stage Caenorhabditis elegans embryo. J. Cell. Biol. 147:1999;135-150.