Interdependence of cell attachment and cell cycle signaling

Current Opinion in Cell Biology

Volumn 18, Issue 5, 2006, Pages 507-515

  Pugacheva, Elena N ^a   Roegiers, Fabrice ^a   Golemis, Erica A ^a  

^a FOX CHASE CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CADHERIN; INTEGRIN; MERLIN;

CANCER SUSCEPTIBILITY; CARCINOGENESIS; CELL ADHESION; CELL CYCLE; CELL CYCLE G1 PHASE; CELL CYCLE M PHASE; CELL CYCLE REGULATION; CELL CYCLE S PHASE; CELL DEATH; CELL DIFFERENTIATION; CELL DIVISION; CELL MIGRATION; CELL POLARITY; CYTOKINESIS; HUMAN; MITOSIS; NONHUMAN; PLEIOTROPY; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CADHERINS; CELL ADHESION; CELL CYCLE; INTEGRINS; NEUROFIBROMIN 2; SIGNAL TRANSDUCTION;

METAZOA;

EID: 33748290074     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ceb.2006.08.014     Document Type: Review

References (55)

1. Schwikowski B., Uetz P., and Fields S. A network of protein-protein interactions in yeast. Nat Biotechnol 18 (2000) 1257-1261
2. Bill H.M., Knudsen B., Moores S.L., Muthuswamy S.K., Rao V.R., Brugge J.S., and Miranti C.K. Epidermal growth factor receptor-dependent regulation of integrin-mediated signaling and cell cycle entry in epithelial cells. Mol Cell Biol 24 (2004) 8586-8599
3. 1-phase. J Biol Chem 279 (2004) 13640-13644
4. Braga V.M., and Yap A.S. The challenges of abundance: epithelial junctions and small GTPase signalling. Curr Opin Cell Biol 17 (2005) 466-474
5. Besson A., Assoian R.K., and Roberts J.M. Regulation of the cytoskeleton: an oncogenic function for CDK inhibitors?. Nat Rev Cancer 4 (2004) 948-955
6. Edgar B.A. From cell structure to transcription: Hippo forges a new path. Cell 124 (2006) 267-273
7. Nathke I.S. The adenomatous polyposis coli protein: the Achilles heel of the gut epithelium. Annu Rev Cell Dev Biol 20 (2004) 337-366
8. 1 phase cell cycle progression. Cancer Metastasis Rev 24 (2005) 383-393
9. Zhao J., Bian Z.C., Yee K., Chen B.P., Chien S., and Guan J.L. Identification of transcription factor KLF8 as a downstream target of focal adhesion kinase in its regulation of cyclin D1 and cell cycle progression. Mol Cell 11 (2003) 1503-1515
10. Diehl J.A., Cheng M., Roussel M.F., and Sherr C.J. Glycogen synthase kinase-3β regulates cyclin D1 proteolysis and subcellular localization. Genes Dev 12 (1998) 3499-3511
11. del Pozo M.A., Balasubramanian N., Alderson N.B., Kiosses W.B., Grande-Garcia A., Anderson R.G., and Schwartz M.A. Phospho-caveolin-1 mediates integrin-regulated membrane domain internalization. Nat Cell Biol 7 (2005) 901-908. This paper, together with earlier studies from the same laboratory, defines an integrin-dependent pathway for activation of mitogenic signaling; this pathway works by inactivating a caveolin-dynamin internalization machinery that regulates proteins associated with lipid rafts/CEMMs. Importantly, this work defines a FAK-independent control pathway for regulating activation of Rac, PI3K, PAK and ERK.
12. 1/S transition. J Biol Chem 279 (2004) 26323-26330
13. Melkoumian Z.K., Peng X., Gan B., Wu X., and Guan J.L. Mechanism of cell cycle regulation by FIP200 in human breast cancer cells. Cancer Res 65 (2005) 6676-6684
14. Gan B., Melkoumian Z.K., Wu X., Guan K.L., and Guan J.L. Identification of FIP200 interaction with the TSC1-TSC2 complex and its role in regulation of cell size control. J Cell Biol 170 (2005) 379-389
15. Karbowniczek M., Cash T., Cheung M., Robertson G.P., Astrinidis A., and Henske E.P. Regulation of B-Raf kinase activity by tuberin and Rheb is mammalian target of rapamycin (mTOR)-independent. J Biol Chem 279 (2004) 29930-29937
16. Yamada S., Pokutta S., Drees F., Weis W.I., and Nelson W.J. Deconstructing the cadherin-catenin-actin complex. Cell 123 (2005) 889-901. This paper argues against the long-held view that α-catenin, β-catenin, E-cadherin and actin exist as a quaternary complex. Among other findings, the authors demonstrate that interaction of α-catenin with actin filaments significantly decreases the affinity of α-catenin for the E-cadherin-β-catenin complex. Membrane-associated actin at cell-cell contacts rapidly exchanges with a cytoplasmic actin pool and is much more mobile than α-catenin, β-catenin or E-cadherin, indicating that actin filaments are not stably associated with the cadherin-catenin complex.
17. -/- brains. Cyclopamine, an inhibitor of this pathway, rescues cell cycle and apoptosis abnormalities but not cortical disorganization.
18. Hamaratoglu F., Willecke M., Kango-Singh M., Nolo R., Hyun E., Tao C., Jafar-Nejad H., and Halder G. The tumour-suppressor genes NF2/Merlin and Expanded act through Hippo signalling to regulate cell proliferation and apoptosis. Nat Cell Biol 8 (2006) 27-36. In developing imaginal discs, Merlin (mer) and Expanded (Ex) signal through the recently defined Hippo (Hpo) pathway to inhibit proliferation through control of Cyclin E, and apoptosis through control of Drosophila inhibitor of apoptosis protein-1 (Diap1). Mer, Ex and Hpo regulate the number of cells in epithelial tissues, but, unlike other tumor suppressors such as TSC1, do not affect cell size.
19. Huang J., Wu S., Barrera J., Matthews K., and Pan D. The Hippo signaling pathway coordinately regulates cell proliferation and apoptosis by inactivating Yorkie, the Drosophila homolog of YAP. Cell 122 (2005) 421-434. This study is the first to identify Yorkie (Yki), the Drosophila ortholog of the mammalian transcriptional coactivator Yes-associated protein (YAP), as a downstream target and interactive partner of the Hippo-pathway kinase Warts (Wts). Yki is required for normal tissue growth and Diap1 transcription, and is phosphorylated and inactivated by Wts. Mutant clones of Hpo or Wts, or Yki-overexpressing cells, are characterized by enhanced proliferation: interestingly, each phase of the cell cycle is proportionally accelerated. Yki-overexpressing cells minimize contacts with their neighbors and form round smooth borders, and have a reduced rate of apoptosis.
20. Poulikakos PI, Xiao GH, Gallagher R, Jablonski S, Jhanwar SC, Testa JR: Re-expression of the tumor suppressor NF2/merlin inhibits invasiveness in mesothelioma cells and negatively regulates FAK. Oncogene 2006. in press.
21. Okada T., Lopez-Lago M., and Giancotti F.G. Merlin/NF-2 mediates contact inhibition of growth by suppressing recruitment of Rac to the plasma membrane. J Cell Biol 171 (2005) 361-371
22. Avizienyte E., and Frame M.C. Src and FAK signalling controls adhesion fate and the epithelial-to-mesenchymal transition. Curr Opin Cell Biol 17 (2005) 542-547
23. Doxsey S., McCollum D., and Theurkauf W. Centrosomes in cellular regulation. Annu Rev Cell Dev Biol 21 (2005) 411-434
24. Yamakita Y., Totsukawa G., Yamashiro S., Fry D., Zhang X., Hanks S.K., and Matsumura F. Dissociation of FAK/p130(CAS)/c-Src complex during mitosis: role of mitosis-specific serine phosphorylation of FAK. J Cell Biol 144 (1999) 315-324
25. Clarke D.M., Brown M.C., LaLonde D.P., and Turner C.E. Phosphorylation of actopaxin regulates cell spreading and migration. J Cell Biol 166 (2004) 901-912
26. Pugacheva E.N., and Golemis E.A. The focal adhesion scaffolding protein HEF1 regulates activation of the Aurora-A and Nek2 kinases at the centrosome. Nat Cell Biol 7 (2005) 937-946. The Cas family focal adhesion adaptor protein HEF1 directly regulates centrosome dynamics and mitotic entry through activation of mitotic kinase Aurora A and inhibition of the NUMA-related kinase Nek2. Over-expression of HEF1 causes Aurora A hyperactivation and cytokinetic defects, followed by accumulation of cells with extra centrosomes. Depletion of HEF1 induces premature centriole splitting and activation of Nek2 kinase, and inhibits Aurora A activation.
27. Zhao Z.S., Lim J.P., Ng Y.W., Lim L., and Manser E. The GIT-associated kinase PAK targets to the centrosome and regulates Aurora-A. Mol Cell 20 (2005) 237-249. Pak kinase, long appreciated as a mediator of cell migration signals at focal adhesions, is shown to bind GIT at the centrosome. This activates Pak, which in turn promotes Aurora A phosphorylation and progression through mitosis.
28. Pugacheva EN, Golemis EA: HEF1-Aurora A interactions: points of dialog between the cell cycle and cell attachment signaling networks. Cell Cycle 2006. 5:in press.
29. De Luca M, Lavia P, Guarguaglini G: A functional interplay between Aurora-A, Plk1 and TPX2 at spindle poles: Plk1 controls centrosomal localization of Aurora-A and TPX2 spindle association. Cell Cycle 2006. in press.
30. 2/M phase stimulates association of the mitotic kinase Plk1 and accumulation of GTP-bound RhoA. Oncogene 25 (2006) 827-837
31. Dadke D., Jarnik M., Pugacheva E.N., Singh M.K., and Golemis E.A. Deregulation of HEF1 impairs M-phase progression by disrupting the RhoA activation cycle. Mol Biol Cell 17 (2006) 1204-1217
32. Du J., and Hannon G.J. Suppression of p160ROCK bypasses cell cycle arrest after Aurora-A/STK15 depletion. Proc Natl Acad Sci U S A 101 (2004) 8975-8980
33. Narumiya S., and Yasuda S. Rho GTPases in animal cell mitosis. Curr Opin Cell Biol 18 (2006) 199-205. A comprehensive recent review of the complex role of Rho signaling during M-phase.
34. Maddox A.S., and Burridge K. RhoA is required for cortical retraction and rigidity during mitotic cell rounding. J Cell Biol 160 (2003) 255-265
35. Vasiliev J.M., Omelchenko T., Gelfand I.M., Feder H.H., and Bonder E.M. Rho overexpression leads to mitosis-associated detachment of cells from epithelial sheets: a link to the mechanism of cancer dissemination. Proc Natl Acad Sci U S A 101 (2004) 12526-12530. Colonies of cells transfected with active RhoA are multi-tiered, and have a dramatic decrease in surface area and increased contractile activity, as a result of myosin II being activated. Transfected cells are characterized by a change in the plane of the cleavage furrow from perpendicular to parallel to the substrate. Reorientation occurs as a consequence of misorientation of the mitotic spindle.
36. Liu X.F., Ishida H., Raziuddin R., and Miki T. Nucleotide exchange factor ECT2 interacts with the polarity protein complex Par6/Par3/protein kinase Cζ (PKCζ) and regulates PKCζ activity. Mol Cell Biol 24 (2004) 6665-6675
37. Zheng X.M., and Shalloway D. Two mechanisms activate PTPα during mitosis. EMBO J 20 (2001) 6037-6049
38. Bhatt A.S., Erdjument-Bromage H., Tempst P., Craik C.S., and Moasser M.M. Adhesion signaling by a novel mitotic substrate of src kinases. Oncogene 24 (2005) 5333-5343
39. Hirota T., Morisaki T., Nishiyama Y., Marumoto T., Tada K., Hara T., Masuko N., Inagaki M., Hatakeyama K., and Saya H. Zyxin, a regulator of actin filament assembly, targets the mitotic apparatus by interacting with h-warts/LATS1 tumor suppressor. J Cell Biol 149 (2000) 1073-1086
40. Bothos J., Tuttle R.L., Ottey M., Luca F.C., and Halazonetis T.D. Human LATS1 is a mitotic exit network kinase. Cancer Res 65 (2005) 6568-6575
41. Hirota T., Kunitoku N., Sasayama T., Marumoto T., Zhang D., Nitta M., Hatakeyama K., and Saya H. Aurora-A and an interacting activator, the LIM protein Ajuba, are required for mitotic commitment in human cells. Cell 114 (2003) 585-598
42. Marie H., Pratt S.J., Betson M., Epple H., Kittler J.T., Meek L., Moss S.J., Troyanovsky S., Attwell D., Longmore G.D., et al. The LIM protein Ajuba is recruited to cadherin-dependent cell junctions through an association with α-catenin. J Biol Chem 278 (2003) 1220-1228
43. Pratt S.J., Epple H., Ward M., Feng Y., Braga V.M., and Longmore G.D. The LIM protein Ajuba influences p130Cas localization and Rac1 activity during cell migration. J Cell Biol 168 (2005) 813-824
44. 1 progression, and cytokinesis. Genes Dev 17 (2003) 2465-2479
45. Ng M.M., Chang F., and Burgess D.R. Movement of membrane domains and requirement of membrane signaling molecules for cytokinesis. Dev Cell 9 (2005) 781-790. This study shows formation of an equatorial membrane domainproxiaml to the contractile ring and enriched in ganglioside GM1 and cholesterol, occurs prior to furrow formation and remains as a distinct band in the cleavage furrow until late cytokinesis. Src and PLCγ are important components of this domain; these proteins are specifically phosphorylated at cytokinesis, and their activity is required for cleavage furrow progression.
46. Piel M., Nordberg J., Euteneuer U., and Bornens M. Centrosome-dependent exit of cytokinesis in animal cells. Science 291 (2001) 1550-1553
47. Gromley A., Yeaman C., Rosa J., Redick S., Chen C.T., Mirabelle S., Guha M., Sillibourne J., and Doxsey S.J. Centriolin anchoring of exocyst and SNARE complexes at the midbody is required for secretory-vesicle-mediated abscission. Cell 123 (2005) 75-87. The authors demonstrate that centriolin interacts with snapin (sec15), sec3 and sec8, proteins associated with vesicle-targeting exocyst complexes and vesicle-fusion SNARE complexes. Vesicles move to the midbody ring asymmetrically from one prospective daughter cell, promoting membrane fusion and abscission. Centriolin is required for midbody localization of the exocyst; disruption of exocyst of SNARE complexes inhibits abscission.
48. Yamashita Y.M., Jones D.L., and Fuller M.T. Orientation of asymmetric stem cell division by the APC tumor suppressor and centrosome. Science 301 (2003) 1547-1550
49. Thery M., Racine V., Pepin A., Piel M., Chen Y., Sibarita J.B., and Bornens M. The extracellular matrix guides the orientation of the cell division axis. Nat Cell Biol 7 (2005) 947-953. Using a micro-contact printing technique to control the spatial distribution of an ECM substrate, the authors investigate the role of the ECM in determining the orientation of the division axis of HeLa cells. In round mitotic cells, the cortex is not homogeneous and contains cortical cues that modulate spindle orientation. These cues are associated with retraction fibers, and originate from the cortical heterogeneity of the pre-mitotic cell. The localization of and requirement for intracellular actin regulatory proteins were investigated, with cortactin and ezrin being implicated in this signaling.
50. Lechler T., and Fuchs E. Asymmetric cell divisions promote stratification and differentiation of mammalian skin. Nature 437 (2005) 275-280. Polarization cues program basal epidermal cells to divide asymmetrically, generating a committed suprabasal cell and a proliferative basal cell. This work demonstrates that both integrins and cadherins are essential for the apical localization of atypical protein kinase C, the Par3-LGN-Inscuteable complex and NuMA-dynactin. Together, these complexes align the spindle, contributing to the stratification of squamous epithelium.
51. Munro E.M. PAR proteins and the cytoskeleton: a marriage of equals. Curr Opin Cell Biol 18 (2006) 86-94
52. Ciruna B., Jenny A., Lee D., Mlodzik M., and Schier A.F. Planar cell polarity signalling couples cell division and morphogenesis during neurulation. Nature 439 (2006) 220-224. This study is one of the first to demonstrate the role of PCP signaling in vertebrate development. Genetic analysis of the interactions of Wnt, Van Gogh-like 2 (Vangl2/Strabismustrilobite) and Prickle shows the Wnt/PCP pathway polarizes neural progenitors along the anteroposterior axis. While this polarity is transiently lost during cell division, anchoring of dividing cells through these signals allows re-intercalation of daughter cells into the neuroepithelium. Defects in this pathway result in accumulation of ectopic neural progenitor cells and neural tube defects.
53. Fischer E., Legue E., Doyen A., Nato F., Nicolas J.F., Torres V., Yaniv M., and Pontoglio M. Defective planar cell polarity in polycystic kidney disease. Nat Genet 38 (2006) 21-23. This study demonstrates that lengthening of renal tubules is associated with mitotic orientation of cells along the tubule axis, requiring intrinsic planar cell polarization. The authors also find that mitotic orientations are significantly distorted in rodent polycystic kidney models, providing insights into the etiology of this disease. In this study, the non-motile renal cell cilia are suggested to act as mechanosensors for directional flow of fluids, organizing the PCP response.
54. Kai T., and Spradling A. Differentiating germ cells can revert into functional stem cells in Drosophila melanogaster ovaries. Nature 428 (2004) 564-569. Drosophila germline cystocytes generated either in second instar larval ovaries or in adults over-producing the BMP4-like stem cell signal Decapentaplegic efficiently convert into single stem-like cells. These de-differentiated cells can develop into functional germline stem cells and support normal fertility. As part of this study, the authors demonstrate that polarized Dpp cues emanating from a germline stem cell can regulate the timing of ring canal closure, a cytokinetic process previously shown to be under the control of Src.
55. Kim M., Gans J.D., Nogueira C., Wang A., Paik J.H., Feng B., Brennan C., Hahn W.C., Cordon-Cardo C., Wagner S.N., et al. Comparative oncogenomics identifies NEDD9 as a melanoma metastasis gene. Cell 125 (2006) 1269-1281