Tumor suppressor protein Lgl mediates G1 cell cycle arrest at high cell density by forming an Lgl-VprBP-DDB1 complex

Molecular Biology of the Cell

Volumn 26, Issue 13, 2015, Pages 2426-2438

  Yamashita, Kazunari ^a   Ide, Mariko ^a   Furukawa, Kana T ^a   Suzuki, Atsushi ^a,b   Hirano, Hisashi ^b   Ohno, Shigeo ^a  

^a YOKOHAMA CITY UNIVERSITY   (Japan)

^b YOKOHAMA CITY UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN; PROTEIN CUL4A; PROTEIN DDB1; PROTEIN KINASE C; PROTEIN LGL; PROTEIN LGL1; PROTEIN LGL2; PROTEIN VPRBP; TUMOR SUPPRESSOR PROTEIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; CARRIER PROTEIN; DDB1 PROTEIN, HUMAN; DNA BINDING PROTEIN; DROSOPHILA PROTEIN; LETHAL (2) GIANT LARVAE PROTEIN, DROSOPHILA; MERLIN; VPRBP PROTEIN, HUMAN;

ANIMAL CELL; ARTICLE; CELL DENSITY; CELL PROLIFERATION; COMPLEX FORMATION; CONTROLLED STUDY; EPITHELIUM CELL; G1 PHASE CELL CYCLE CHECKPOINT; HEK293 CELL LINE; HELA CELL LINE; MDCK CELL LINE; MOLECULAR BIOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN SUBUNIT; S PHASE CELL CYCLE CHECKPOINT; ANIMAL; CELL COUNT; CELL LINE; CELL POLARITY; DOG; GENETICS; HUMAN; METABOLISM; PHYSIOLOGY;

ANIMALS; CARRIER PROTEINS; CELL COUNT; CELL LINE; CELL POLARITY; DNA-BINDING PROTEINS; DOGS; DROSOPHILA PROTEINS; G1 PHASE CELL CYCLE CHECKPOINTS; HEK293 CELLS; HELA CELLS; HUMANS; MADIN DARBY CANINE KIDNEY CELLS; NEUROFIBROMIN 2; TUMOR SUPPRESSOR PROTEINS;

EID: 84934299851     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E14-10-1462     Document Type: Article

References (55)

1. Angers S, Li T, Yi X, MacCoss MJ, Moon RT, Zheng N (2006). Molecular architecture and assembly of the DDB1-CUL4A ubiquitin ligase machinery. Nature 443, 590-593.
2. Bashir T, Dorrello NV, Amador V, Guardavaccaro D, Pagano M (2004). Control of the SCF(Skp2-Cks1) ubiquitin ligase by the APC/C(Cdh1) ubiquitin ligase. Nature 428, 190-193.
3. Besson A, Dowdy SF, Roberts JM (2008). CDK inhibitors: cell cycle regulators and beyond. Dev Cell 14, 159-169.
4. Betschinger J, Mechtler K, Knoblich JA (2003). The Par complex directs asymmetric cell division by phosphorylating the cytoskeletal protein Lgl. Nature 422, 326-330.
5. Bilder D (2004). Epithelial polarity and proliferation control: links from the Drosophila neoplastic tumor suppressors. Genes Dev 18, 1909-1925.
6. Bondar T, Kalinina A, Khair L, Kopanja D, Nag A, Bagchi S, Raychaudhuri P (2006). Cul4A and DDB1 associate with Skp2 to target p27Kip1 for proteolysis involving the COP9 signalosome. Mol Cell Biol 26, 2531-2539.
7. Brumby A, Secombe J, Horsfield J, Coombe M, Amin N, Coates D, Saint R, Richardson H (2004). A genetic screen for dominant modifiers of a cyclin E hypomorphic mutation identifies novel regulators of S-phase entry in Drosophila. Genetics 168, 227-251.
8. Carrano AC, Eytan E, Hershko A, Pagano M (1999). SKP2 is required for ubiquitin-mediated degradation of the CDK inhibitor p27. Nat Cell Biol 1, 193-199.
9. Chalmers AD, Pambos M, Mason J, Lang S, Wylie C, Papalopulu N (2005). aPKC, Crumbs3 and Lgl2 control apicobasal polarity in early vertebrate development. Development 132, 977-986.
10. Clark BS, Cui S, Miesfeld JB, Klezovitch O, Vasioukhin V, Link BA (2012). Loss of Llgl1 in retinal neuroepithelia reveals links between apical domain size, Notch activity and neurogenesis. Development 139, 1599-1610.
11. Coats S, Flanagan WM, Nourse J, Roberts JM (1996). Requirement of p27Kip1 for restriction point control of the fibroblast cell cycle. Science 272, 877-880.
12. Fagotto F, Gumbiner BM (1996). Cell contact-dependent signaling. Dev Biol 180, 445-454.
13. Gateff E (1978). Malignant neoplasms of genetic origin in Drosophila melanogaster. Science 200, 1448-1459.
14. Grifoni D, Garoia F, Schimanski CC, Schmitz G, Laurenti E, Galle PR, Pession A, Cavicchi S, Strand D (2004). The human protein Hugl-1 substitutes for Drosophila lethal giant larvae tumour suppressor function in vivo. Oncogene 23, 8688-8694.
15. Grzeschik NA, Amin N, Secombe J, Brumby AM, Richardson HE (2007). Abnormalities in cell proliferation and apico-basal cell polarity are separable in Drosophila lgl mutant clones in the developing eye. Dev Biol 311, 106-123.
16. He YJ, McCall CM, Hu J, Zeng Y, Xiong Y (2006). DDB1 functions as a linker to recruit receptor WD40 proteins to CUL4-ROC1 ubiquitin ligases. Genes Dev 20, 2949-2954.
17. Higa LA, Wu M, Ye T, Kobayashi R, Sun H, Zhang H (2006a). CUL4-DDB1 ubiquitin ligase interacts with multiple WD40-repeat proteins and regulates histone methylation. Nat Cell Biol 8, 1277-1283.
18. Higa LA, Yang X, Zheng J, Banks D, Wu M, Ghosh P, Sun H, Zhang H (2006b). Involvement of CUL4 ubiquitin E3 ligases in regulating CDK inhibitors Dacapo/p27Kip1 and cyclin E degradation. Cell Cycle 5, 71-77.
19. Horikoshi Y, Suzuki A, Yamanaka T, Sasaki K, Mizuno K, Sawada H, Yonemura S, Ohno S (2009). Interaction between PAR-3 and the aPKC-PAR-6 complex is indispensable for apical domain development of epithelial cells. J Cell Sci 122, 1595-1606.
20. Hrecka K, Gierszewska M, Srivastava S, Kozaczkiewicz L, Swanson SK, Florens L, Washburn MP, Skowronski J (2007). Lentiviral Vpr usurps Cul4-DDB1[VprBP] E3 ubiquitin ligase to modulate cell cycle. Proc Natl Acad Sci USA 104, 11778-11783.
21. Humbert PO, Grzeschik NA, Brumby AM, Galea R, Elsum I, Richardson HE (2008). Control of tumourigenesis by the Scribble/Dlg/Lgl polarity module. Oncogene 27, 6888-6907.
22. Jin J, Arias EE, Chen J, Harper JW, Walter JC (2006). A family of diverse Cul4-Ddb1-interacting proteins includes Cdt2, which is required for S phase destruction of the replication factor Cdt1. Mol Cell 23, 709-721.
23. Kalmes A, Merdes G, Neumann B, Strand D, Mechler BM (1996). A serine-kinase associated with the p127-l(2)gl tumour suppressor of Drosophila may regulate the binding of p127 to nonmuscle myosin II heavy chain and the attachment of p127 to the plasma membrane. J Cell Sci 109, 1359-1368.
24. Klezovitch O, Fernandez TE, Tapscott SJ, Vasioukhin V (2004). Loss of cell polarity causes severe brain dysplasia in Lgl1 knockout mice. Genes Dev 18, 559-571.
25. Kuphal S, Wallner S, Schimanski CC, Bataille F, Hofer P, Strand S, Strand D, Bosserhoff AK (2006). Expression of Hugl-1 is strongly reduced in malignant melanoma. Oncogene 25, 103-110.
26. Levenberg S, Yarden A, Kam Z, Geiger B (1999). p27 is involved in N-cadherin-mediated contact inhibition of cell growth and S-phase entry. Oncogene 18, 869-876.
27. Li B, Jia N, Kapur R, Chun KT (2006). Cul4A targets p27 for degradation and regulates proliferation, cell cycle exit, and differentiation during erythropoiesis. Blood 107, 4291-4299.
28. Li W, You L, Cooper J, Schiavon G, Pepe-Caprio A, Zhou L, Ishii R, Giovannini M, Hanemann CO, Long SB, et al. (2010). Merlin/NF2 suppresses tumorigenesis by inhibiting the E3 ubiquitin ligase CRL4(DCAF1) in the nucleus. Cell 140, 477-490.
29. Maddika S, Chen J (2009). Protein kinase DYRK2 is a scaffold that facilitates assembly of an E3 ligase. Nat Cell Biol 11, 409-419.
30. McCall CM, Miliani de Marval PL, Chastain PD 2nd, Jackson SC, He YJ, Kotake Y, Cook JG, Xiong Y (2008). Human immunodeficiency virus type 1 Vpr-binding protein VprBP, a WD40 protein associated with the DDB1-CUL4 E3 ubiquitin ligase, is essential for DNA replication and embryonic development. Mol Cell Biol 28, 5621-5633.
31. McClatchey AI, Yap AS (2012). Contact inhibition (of proliferation) redux. Curr Opin Cell Biol 24, 685-694.
32. Miranda-Carboni GA, Krum SA, Yee K, Nava M, Deng QE, Pervin S, Collado-Hidalgo A, Galic Z, Zack JA, Nakayama K, et al. (2008). A functional link between Wnt signaling and SKP2-independent p27 turnover in mammary tumors. Genes Dev 22, 3121-3134.
33. Nagase T, Yamakawa H, Tadokoro S, Nakajima D, Inoue S, Yamaguchi K, Itokawa Y, Kikuno RF, Koga H, Ohara O (2008). Exploration of human ORFeome: high-throughput preparation of ORF clones and efficient characterization of their protein products. DNA Res 15, 137-149.
34. Nakayama K, Ishida N, Shirane M, Inomata A, Inoue T, Shishido N, Horii I, Loh DY (1996). Mice lacking p27(Kip1) display increased body size, multiple organ hyperplasia, retinal dysplasia, and pituitary tumors. Cell 85, 707-720.
35. Ohno S (2001). Intercellular junctions and cellular polarity: the PAR-aPKC complex, a conserved core cassette playing fundamental roles in cell polarity. Curr Opin Cell Biol 13, 641-648.
36. Ohshiro T, Yagami T, Zhang C, Matsuzaki F (2000). Role of cortical tumour-suppressor proteins in asymmetric division of Drosophila neuroblast. Nature 408, 593-596.
37. Okada T, You L, Giancotti FG (2007). Shedding light on Merlin's wizardry. Trends Cell Biol 17, 222-229.
38. Peng CY, Manning L, Albertson R, Doe CQ (2000). The tumour-suppressor genes lgl and dlg regulate basal protein targeting in Drosophila neuroblasts. Nature 408, 596-600.
39. Peters JM (2006). The anaphase promoting complex/cyclosome: a machine designed to destroy. Nat Rev Mol Cell Biol 7, 644-656.
40. Polyak K, Kato JY, Solomon MJ, Sherr CJ, Massague J, Roberts JM, Koff A (1994). p27Kip1, a cyclin-Cdk inhibitor, links transforming growth factor-beta and contact inhibition to cell cycle arrest. Genes Dev 8, 9-22.
41. Reischauer S, Levesque MP, Nusslein-Volhard C, Sonawane M (2009). Lgl2 executes its function as a tumor suppressor by regulating ErbB signaling in the zebrafish epidermis. PLoS Genet 5, e1000720.
42. Schimanski CC, Schmitz G, Kashyap A, Bosserhoff AK, Bataille F, Schafer SC, Lehr HA, Berger MR, Galle PR, Strand S, et al. (2005). Reduced expression of Hugl-1, the human homologue of Drosophila tumour suppressor gene lgl, contributes to progression of colorectal cancer. Oncogene 24, 3100-3109.
43. Seluanov A, Hine C, Azpurua J, Feigenson M, Bozzella M, Mao Z, Catania KC, Gorbunova V (2009). Hypersensitivity to contact inhibition provides a clue to cancer resistance of naked mole-rat. Proc Natl Acad Sci USA 106, 19352-19357.
44. Sonawane M, Carpio Y, Geisler R, Schwarz H, Maischein HM, Nuesslein-Volhard C (2005). Zebrafish penner/lethal giant larvae 2 functions in hemidesmosome formation, maintenance of cellular morphology and growth regulation in the developing basal epidermis. Development 132, 3255-3265.
45. St Croix B, Sheehan C, Rak JW, Florenes VA, Slingerland JM, Kerbel RS (1998). E-Cadherin-dependent growth suppression is mediated by the cyclin-dependent kinase inhibitor p27(KIP1). J Cell Biol 142, 557-571.
46. Sutterluty H, Chatelain E, Marti A, Wirbelauer C, Senften M, Muller U, Krek W (1999). p45SKP2 promotes p27Kip1 degradation and induces S phase in quiescent cells. Nat Cell Biol 1, 207-214.
47. Suzuki A, Yamanaka T, Hirose T, Manabe N, Mizuno K, Shimizu M, Akimoto K, Izumi Y, Ohnishi T, Ohno S (2001). Atypical protein kinase C is involved in the evolutionarily conserved par protein complex and plays a critical role in establishing epithelia-specific junctional structures. J Cell Biol 152, 1183-1196.
48. Takai Y, Miyoshi J, Ikeda W, Ogita H (2008). Nectins and nectin-like molecules: roles in contact inhibition of cell movement and proliferation. Nat Rev Mol Cell Biol 9, 603-615.
49. Tamori Y, Bialucha CU, Tian AG, Kajita M, Huang YC, Norman M, Harrison N, Poulton J, Ivanovitch K, Disch L, et al. (2011). Involvement of Lgl and Mahjong/VprBP in cell competition. PLoS Biol 8, e1000422.
50. Tanaka J, Miwa Y, Miyoshi K, Ueno A, Inoue H (1999). Construction of Epstein-Barr virus-based expression vector containing mini-oriP. Biochem Biophys Res Commun 264, 938-943.
51. Tsuruga T, Nakagawa S, Watanabe M, Takizawa S, Matsumoto Y, Nagasaka K, Sone K, Hiraike H, Miyamoto Y, Hiraike O, et al. (2007). Loss of Hugl-1 expression associates with lymph node metastasis in endometrial cancer. Oncol Res 16, 431-435.
52. Wei W, Ayad NG, Wan Y, Zhang GJ, Kirschner MW, Kaelin WG Jr (2004). Degradation of the SCF component Skp2 in cell-cycle phase G1 by the anaphase-promoting complex. Nature 428, 194-198.
53. Yamanaka T, Horikoshi Y, Izumi N, Suzuki A, Mizuno K, Ohno S (2006). Lgl mediates apical domain disassembly by suppressing the PAR-3-aPKC-PAR-6 complex to orient apical membrane polarity. J Cell Sci 119, 2107-2118.
54. Yamanaka T, Horikoshi Y, Sugiyama Y, Ishiyama C, Suzuki A, Hirose T, Iwamatsu A, Shinohara A, Ohno S (2003). Mammalian Lgl forms a protein complex with PAR-6 and aPKC independently of PAR-3 to regulate epithelial cell polarity. Curr Biol 13, 734-743.
55. Zhang S, Feng Y, Narayan O, Zhao LJ (2001). Cytoplasmic retention of HIV-1 regulatory protein Vpr by protein-protein interaction with a novel human cytoplasmic protein VprBP. Gene 263, 131-140.