Murine missing in metastasis (MIM) mediates cell polarity and regulates the motility response to growth factors

PLoS ONE

Volumn 6, Issue 6, 2011, Pages

  Yu, Dan ^a   Zhan, Xiaoguo H ^a   Niu, Shuqiong ^a   Mikhailenko, Irina ^a   Strickland, Dudley K ^a   Zhu, Jianwei ^b   Cao, Meng ^a   Zhan, Xi ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b NANTONG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; DNA; EPIDERMAL GROWTH FACTOR; FLUORESCENT DYE; GROWTH FACTOR; MISSING IN METASTASIS PROTEIN; MYC PROTEIN; PLATELET DERIVED GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; RAC1 PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SELECTIVE ESTROGEN RECEPTOR MODULATOR; TRANSFERRIN; UNCLASSIFIED DRUG; ACTIN; ACTIN BINDING PROTEIN; MTSS1 PROTEIN, MOUSE; TUMOR PROTEIN;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; CELL ADHESION; CELL MOTILITY; CELL POLARITY; CELL STRUCTURE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; FIBROBLAST; FOCAL ADHESION; INTERNALIZATION; MOUSE; NONHUMAN; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; STRESS FIBER; ANIMAL; CELL LINE; CELL MEMBRANE; CELL MOTION; CELL SHAPE; CYTOLOGY; CYTOSKELETON; DRUG EFFECT; EXTRACELLULAR SPACE; FEMALE; GENE INACTIVATION; GENE VECTOR; GENETICS; MALE; METABOLISM; PROTEIN TRANSPORT;

MAMMALIA; MURINAE; MUS;

ACTINS; ANIMALS; CELL ADHESION; CELL LINE; CELL MEMBRANE; CELL MOVEMENT; CELL POLARITY; CELL SHAPE; CYTOSKELETON; EXTRACELLULAR SPACE; FEMALE; FIBROBLASTS; GENE KNOCKOUT TECHNIQUES; GENETIC VECTORS; MALE; MICE; MICROFILAMENT PROTEINS; NEOPLASM PROTEINS; PLATELET-DERIVED GROWTH FACTOR; PROTEIN TRANSPORT; TRANSFERRIN;

EID: 79958284340     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0020845     Document Type: Article

References (46)

1. Wang Y, Liu J, Smith E, Zhou K, Liao J, et al. (2007) Downregulation of missing in metastasis gene (MIM) is associated with the progression of bladder transitional carcinomas. Cancer Invest 25: 79-86 777189587.
2. Nixdorf S, Grimm MO, Loberg R, Marreiros A, Russell PJ, et al. (2004) Expression and regulation of MIM (Missing In Metastasis), a novel putative metastasis suppressor gene, and MIM-B, in bladder cancer cell lines. Cancer Lett 215: 209-220 S0304-3835(04)00348-9.
3. Lee YG, Macoska JA, Korenchuk S, Pienta KJ, (2002) MIM, a potential metastasis suppressor gene in bladder cancer. Neoplasia 4: 291-294.
4. Parr C, Jiang WG, (2009) Metastasis suppressor 1 (MTSS1) demonstrates prognostic value and anti-metastatic properties in breast cancer. Eur J Cancer 45: 1673-1683 S0959-8049(09)00148-8.
5. van DM, van MR, Vissers KJ, Hop WC, Dinjens WN, et al. (2007) High-resolution array comparative genomic hybridization of chromosome 8q: evaluation of putative progression markers for gastroesophageal junction adenocarcinomas. Cytogenet Genome Res 118: 130-137.
6. Gallop JL, McMahon HT, (2005) BAR domains and membrane curvature: bringing your curves to the BAR. Biochem Soc Symp pp. 223-231.
7. Frost A, Unger VM, De CP, (2009) The BAR domain superfamily: membrane-molding macromolecules. Cell 137: 191-196.
8. Scita G, Confalonieri S, Lappalainen P, Suetsugu S, (2008) IRSp53: crossing the road of membrane and actin dynamics in the formation of membrane protrusions. Trends Cell Biol 18: 52-60.
9. Lee SH, Kerff F, Chereau D, Ferron F, Klug A, Dominguez R, (2007) Structural basis for the actin-binding function of missing-in-metastasis. Structure 15: 145-155.
10. Millard TH, Bompard G, Heung MY, Dafforn TR, Scott DJ, et al. (2005) Structural basis of filopodia formation induced by the IRSp53/MIM homology domain of human IRSp53. EMBO J 24: 240-250.
11. Mattila PK, Salminen M, Yamashiro T, Lappalainen P, (2003) Mouse MIM, a tissue-specific regulator of cytoskeletal dynamics, interacts with ATP-actin monomers through its C-terminal WH2 domain. J Biol Chem 278: 8452-8459.
12. Saarikangas J, Zhao H, Pykalainen A, Laurinmaki P, Mattila PK, et al. (2009) Molecular mechanisms of membrane deformation by I-BAR domain proteins. Curr Biol 19: 95-107.
13. Suetsugu S, Murayama K, Sakamoto A, Hanawa-Suetsugu K, Seto A, et al. (2006) The RAC binding domain/IRSp53-MIM homology domain of IRSp53 induces RAC-dependent membrane deformation. J Biol Chem 281: 35347-35358.
14. Yamagishi A, Masuda M, Ohki T, Onishi H, Mochizuki N, (2004) A novel actin bundling/filopodium-forming domain conserved in insulin receptor tyrosine kinase substrate p53 and missing in metastasis protein. J Biol Chem 279: 14929-14936.
15. Zhao H, Pykalainen A, Lappalainen P, (2010) I-BAR domain proteins: linking actin and plasma membrane dynamics. Curr Opin Cell Biol.
16. Gonzalez-Quevedo R, Shoffer M, Horng L, Oro AE, (2005) Receptor tyrosine phosphatase-dependent cytoskeletal remodeling by the hedgehog-responsive gene MIM/BEG4. J Cell Biol 168: 453-463.
17. Bompard G, Sharp SJ, Freiss G, Machesky LM, (2005) Involvement of Rac in actin cytoskeleton rearrangements induced by MIM-B. J Cell Sci 118: 5393-5403.
18. Woodings JA, Sharp SJ, Machesky LM, (2003) MIM-B, a putative metastasis suppressor protein, binds to actin and to protein tyrosine phosphatase delta. Biochem J 371: 463-471.
19. Lin J, Liu J, Wang Y, Zhu J, Zhou K, et al. (2005) Differential regulation of cortactin and N-WASP-mediated actin polymerization by missing in metastasis (MIM) protein. Oncogene 24: 2059-2066.
20. Quinones GA, Jin J, Oro AE, (2010) I-BAR protein antagonism of endocytosis mediates directional sensing during guided cell migration. J Cell Biol 189: 353-367.
21. Wang Y, Zhou K, Zeng X, Lin J, Zhan X, (2007) Tyrosine phosphorylation of missing in metastasis protein is implicated in platelet-derived growth factor-mediated cell shape changes. J Biol Chem 282: 7624-7631.
22. Bershteyn M, Atwood SX, Woo WM, Li M, Oro AE, (2010) MIM and cortactin antagonism regulates ciliogenesis and hedgehog signaling. Dev Cell 19: 270-283.
23. Ridley AJ, Hall A, (1992) Distinct patterns of actin organization regulated by the small GTP-binding proteins Rac and Rho. Cold Spring Harb Symp Quant Biol 57: 661-671.
24. Hedberg KM, Bengtsson T, Safiejko-Mroczka B, Bell PB, Lindroth M, (1993) PDGF and neomycin induce similar changes in the actin cytoskeleton in human fibroblasts. Cell Motil Cytoskeleton 24: 139-149.
25. Gao Y, Dickerson JB, Guo F, Zheng J, Zheng Y, (2004) Rational design and characterization of a Rac GTPase-specific small molecule inhibitor. Proc Natl Acad Sci U S A 101: 7618-7623.
26. Saarikangas J, Mattila PK, Varjosalo M, Bovellan M, Hakanen J, et al. (2011) Missing-in-metastasis MIM/MTSS1 promotes actin assembly at intercellular junctions and is required for integrity of kidney epithelia. J Cell Sci 124: 1245-1255.
27. Nakagawa H, Miki H, Nozumi M, Takenawa T, Miyamoto S, et al. (2003) IRSp53 is colocalised with WAVE2 at the tips of protruding lamellipodia and filopodia independently of Mena. J Cell Sci 116: 2577-2583.
28. Zheng D, Niu S, Yu D, Zhan XH, Zeng X, et al. (2010) Abba promotes PDGF-mediated membrane ruffling through activation of the small GTPase Rac1. Biochem Biophys Res Commun 401: 527-532.
29. Zigmond SH, (1996) Signal transduction and actin filament organization. Curr Opin Cell Biol 8: 66-73.
30. Quinones GA, Jin J, Oro AE, (2010) I-BAR protein antagonism of endocytosis mediates directional sensing during guided cell migration. J Cell Biol 189: 353-367.
31. Abou-Kheir W, Isaac B, Yamaguchi H, Cox D, (2008) Membrane targeting of WAVE2 is not sufficient for WAVE2-dependent actin polymerization: a role for IRSp53 in mediating the interaction between Rac and WAVE2. J Cell Sci 121: 379-390.
32. Roberts-Galbraith RH, Gould KL, (2010) Setting the F-BAR: functions and regulation of the F-BAR protein family. Cell Cycle 9: 4091-4097 13587 [pii].
33. Youn JY, Friesen H, Kishimoto T, Henne WM, Kurat CF, et al. (2010) Dissecting BAR domain function in the yeast Amphiphysins Rvs161 and Rvs167 during endocytosis. Mol Biol Cell 21: 3054-3069.
34. Andersson F, Low P, Brodin L, (2010) Selective perturbation of the BAR domain of endophilin impairs synaptic vesicle endocytosis. Synapse 64: 556-560.
35. Douglas LM, Martin SW, Konopka JB, (2009) BAR domain proteins Rvs161 and Rvs167 contribute to Candida albicans endocytosis, morphogenesis, and virulence. Infect Immun 77: 4150-4160.
36. Ryan TA, (2006) A pre-synaptic to-do list for coupling exocytosis to endocytosis. Curr Opin Cell Biol 18: 416-421.
37. Veltman DM, Auciello G, Spence HJ, Machesky LM, Rappoport JZ, et al. (2011) Functional analysis of Dictyostelium IBARa reveals a conserved role of the I-BAR domain in endocytosis. Biochem J 436: 45-52.
38. Toguchi M, Richnau N, Ruusala A, Aspenstrom P, (2010) Members of the CIP4 family of proteins participate in the regulation of platelet-derived growth factor receptor-beta-dependent actin reorganization and migration. Biol Cell 102: 215-230.
39. Kruth HS, Jones NL, Huang W, Zhao B, Ishii I, et al. (2005) Macropinocytosis is the endocytic pathway that mediates macrophage foam cell formation with native low density lipoprotein. J Biol Chem 280: 2352-2360.
40. Fiorentini C, Falzano L, Fabbri A, Stringaro A, Logozzi M, et al. (2001) Activation of rho GTPases by cytotoxic necrotizing factor 1 induces macropinocytosis and scavenging activity in epithelial cells. Mol Biol Cell 12: 2061-2073.
41. Caron E, Hall A, (1998) Identification of two distinct mechanisms of phagocytosis controlled by different Rho GTPases. Science 282: 1717-1721.
42. Borm B, Requardt RP, Herzog V, Kirfel G, (2005) Membrane ruffles in cell migration: indicators of inefficient lamellipodia adhesion and compartments of actin filament reorganization. Exp Cell Res 302: 83-95.
43. Suetsugu S, Yamazaki D, Kurisu S, Takenawa T, (2003) Differential roles of WAVE1 and WAVE2 in dorsal and peripheral ruffle formation for fibroblast cell migration. Dev Cell 5: 595-609.
44. Miki H, Yamaguchi H, Suetsugu S, Takenawa T, (2000) IRSp53 is an essential intermediate between Rac and WAVE in the regulation of membrane ruffling. Nature 408: 732-735.
45. McNiven MA, Kim L, Krueger EW, Orth JD, Cao H, et al. (2000) Regulated interactions between dynamin and the actin-binding protein cortactin modulate cell shape. J Cell Biol 151: 187-198.
46. Yu D, Zhang H, Blanpied TA, Smith E, Zhan X, (2010) Cortactin is implicated in murine zygotic development. Exp Cell Res 316: 848-858.