MTSS1: A multifunctional protein and its role in cancer invasion and metastasis

Frontiers in Bioscience - Scholar

Volumn 3 S, Issue 2, 2011, Pages 621-631

  Xie, Fei ^a,b   Ye, Lin ^a   Ta, Martin ^a   Zhang, Lijian ^b   Jiang, Wen G ^a  

^a CARDIFF UNIVERSITY SCHOOL OF MEDICINE   (United Kingdom)

^b PEKING UNIVERSITY CANCER HOSPITAL AND INSTITUTE   (China)

Author keywords

MTSS1; Review; Scaffold Protein And Shh Responsive Gene

Indexed keywords

ACTIN RELATED PROTEIN 2-3 COMPLEX; BETA CATENIN; COFILIN; CORTACTIN; DYNAMIN II; F ACTIN; G ACTIN; GUANOSINE TRIPHOSPHATASE; LIM KINASE 1; MESSENGER RNA; METASTASIS SUPPRESSOR 1; NEURAL WISKOTT ALDRICH SYNDROME PROTEIN; PLATELET DERIVED GROWTH FACTOR; PROTEIN CDC42; PROTEIN P53; RAC PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; SCAFFOLD PROTEIN; SONIC HEDGEHOG PROTEIN; TUMOR NECROSIS FACTOR ALPHA; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; VASCULOTROPIN; WISKOTT ALDRICH SYNDROME PROTEIN; ACTIN BINDING PROTEIN; MTSS1 PROTEIN, HUMAN; TUMOR PROTEIN;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ARTICLE; BINDING SITE; CANCER CELL; CARCINOGENESIS; CELL INTERACTION; CELL MEMBRANE; CELL MIGRATION; CELL MOTILITY; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; CYTOSKELETON; DISEASE FREE SURVIVAL; DNA METHYLATION; DOWN REGULATION; GENE EXPRESSION; GENE OVEREXPRESSION; HUMAN; IMMUNOREACTIVITY; IONIC STRENGTH; MEMBRANE BINDING; METASTASIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PDZ DOMAIN; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN CROSS LINKING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; STEADY STATE; TANDEM REPEAT; TRANSITIONAL CELL CARCINOMA; TUMOR INVASION; CANCER INVASION; CELL MOTION; CELL TRANSFORMATION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; PHYSIOLOGY; REVIEW;

ANIMALIA;

CELL MOVEMENT; CELL TRANSFORMATION, NEOPLASTIC; CYTOSKELETON; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICROFILAMENT PROTEINS; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASM PROTEINS; SIGNAL TRANSDUCTION;

EID: 79955978310     PISSN: 19450516     EISSN: 19450524     Source Type: Journal    
DOI: 10.2741/s175     Document Type: Article

References (83)

1. Steeg, P. S.: Metastasis suppressors alter the signal transduction of cancer cells. Nat Rev Cancer 3, 55-63 (2003)
2. Lee, Y., J. A. Macoskay, S. Korenchukx and K. J. Pientay: MIM, a potential metastasis suppressor gene in bladder cancer. Neoplasia 4, 291-294 (2002)
3. Nixdorf, S., M. Grimm, R. Loberg, A. Marreiros, P. J. Russell, K. J. Pienta, and P. Jackson: 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 (2004)
4. Utikal1, J., A. Gratchev, I. Muller-Molinet, S. Oerther, J. Kzhyshkowska, N. Arens, R. Grobholz, S. Kannookadan and S. Goerdt: The expression of metastasis suppressor MIM/MTSS1 is regulated by DNA methylation. Int J Cancer 119, 2287-2293 (2006)
5. Loberg, R. D., C. K. Neeley, L. L. Adam-day, Y. Fridman, L. N. St John, S. Nixdorf, P. Jackson, L. M. Kalikin and K. J. Pienta: Differential expression analysis of MIM (MTSS1) splice variants and a functional role of MIM in prostate cancer cell biology. Int J Oncol 26, 1699-1705 (2005)
6. Bompard, G., S. J. Sharp, G. Freiss and L. M. Machesky: Involvement of Rac in actin cytoskeleton rearrangements induced by MIM-B. J Cell Sci 118, 5393-5403 (2005)
7. Lin, J., J. Liu, Y. Wang, J. Zhu, K. Zhou, N. Smith and X. Zhan: Differential regulation of cortactin and N-WASPmediated actin polymerization by missing in metastasis (MIM) protein. Oncogene 24, 2059-2066 (2005)
8. Yamagishi, A., M. Masuda, T. Ohki, H. Onishi, and N. Mochizuki: 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 (2004)
9. Mattila, P. K., M. Salminen, T. Yamashiro, and P. Lappalainen: 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 (2003)
10. Woodings, J. A., S. J. Sharp and L. M. Machesky: MIM-B, a putative metastasis suppressor protein, binds to actin and to protein tyrosine phosphatase delta. Biochem J 371, 463-471 (2003)
11. Wang, Y., K. Zhou, X. Zeng, J. Lin, and X. Zhan: Tyrosine phosphorylation of missing in metastasis protein is implicated in platelet-derived growth factor-mediated cell shape changes. J Biol Chem 282, 7624-7631 (2007)
12. Callahan, C. A., T. Ofstad, L. Horng, J. K. Wang, H. H. Zhen, P. A. Coulombe, and A. E. Oro: MIM/BEG4, a Sonic hedgehog-responsive gene that potentiates Gli-dependent transcription. Genes Dev 18, 2724-2729 (2004)
13. Ma, S., X Guan, T. K. Lee, and K. W. Chan: Clinicopathological significance of missing in metastasis B expression in hepatocellular carcinoma. Hum Pathol 38, 1201-1206 (2007)
14. Parr, C., W. G. Jiang: Metastasis suppressor 1 (MTSS1) demonstrates prognostic value and anti-metastatic properties in breast cancer. Eur J Cancer 45, 1673-1683 (2009)
15. Condeelis, J., R. Singer, and J. E. Segall: The great escape: when cancer cells hijack the genes for chemotaxis and motility. Annu Rev Cell Dev Biol 21, 695-718 (2005)
16. Sahai, E.: Mechanisms of cancer cell invasion. Curr Opin Genet Dev 15, 87-96 (2005)
17. Yamaguchi, H., J. Wyckoff, and J. Condeelis: Cell migration in tumors. Curr Opin Cell Biol 17, 559-564 (2005)
18. Bailly, M., and J. Condeelis: Cell motility: insights from the backstage. Nat Cell Biol 4, E292-E294 (2002)
19. Pollard, T. D., and G. G. Borisy: Cellular motility driven by assembly and disassembly of actin filaments. Cell 112, 453-465 (2003)
20. Svitkina, T. M., and G. G. Borisy: Arp2/3 complex and actin depolymerizing factor/cofilin in dendritic organization and treadmilling of actin filament array in lamellipodia. J Cell Biol. 145, 1009-1026 (1999)
21. Borisy, G. G., and T. M. Svitkina: Actin machinery: pushing the envelope. Curr Opin Cell Biol 12, 104-112 (2000)
22. Pollard, T. D., L. Blanchoin, and R. D. Mullins: Molecular mechanisms controlling actin filament dynamics in nonmuscle cells. Annu Rev Biophys Biomol Struct 29, 545-76 (2000)
23. Higgs, H. N., and T. D. Pollard: Regulation of actin filament network formation through ARP2/3 complex: activation by a diverse array of proteins. Annu Rev Biochem 70, 649-676 (2001)
24. Cooper, J. A., and D. A. Schafer: Control of actin assembly and disassembly at filament ends. Curr Opin Cell Biol 12, 97-103 (2000)
25. Bamburg, J. R.: Proteins of the ADF/cofilin family: essential regulators of actin dynamics. Annu Rev Cell Dev Biol 15, 185-230 (1999)
26. Lewis, A. K., and P. C. Bridgman: Nerve growth cone lamellipodia contain two populations of actin filaments that differ in organization and polarity. J Cell Biol 119, 1219-1243 (1992)
27. Small, J. V., T. Stradal, E. Vignal, and K. Rottner: The lamellipodium: where motility begins. Trends Cell Biol 12, 112-120 (2002)
28. Svitkina, T. M., E. A. Bulanova, O. Y. Chaga, D. M. Vignjevic, S. Kojima, J. M. Vasiliev, and G. G. Borisy: Mechanism of filopodia initiation by reorganization of a dendritic network. J Cell Biol 160, 409-421 (2003)
29. Small, J. V.: Lamellipodia architecture: Actin filament turnover and the lateral flow of actin filaments during motility. Semin Cell Biol 5, 157-163 (1994)
30. Kozma, R., S. Ahmed, A. Best, and L. Lim: The Rasrelated protein Cdc42Hs and bradykinin promote formation of peripheral actin microspikes and filopodia in Swiss 3T3 fibroblasts. Mol Cell Biol 15, 1942-1952 (1995)
31. Nobes, C. D., and A. Hall.: Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81, 53-62 (1995)
32. Buccione, R., J. D. Orth, and M. A. McNiven: Foot and mouth: podosomes, invadopodia and circular dorsal ruffles, Nat Rev Mol Cell Biol 5, 647-657 (2004)
33. Condeelis, J., and J. E. Segall: Intravital imaging of cell movement in tumours. Nat Rev Cancer 3, 921-930 (2003)
34. Linder, S., and P. Kopp: Podosomes at a glance. J Cell Sci 118, 2079-2082 (2005)
35. Linder, S., and M. Aepfelbacher: Podosomes: adhesion hot-spots of invasive cells. Trends Cell Biol 13, 376-385 (2003)
36. Osiak, A. E., G. Zenner, and S. Linder: Subconfluent endothelial cells form podosomes downstream of cytokine and RhoGTPase signaling. Exp Cell Res 307, 342-353 (2005)
37. Varon, C., F. Tatin, V. Moreau, E. V. Obberghen- Schilling, S. Fernandez-Sauze, E. Reuzeau, I. Kramer, and E. Genot: Transforming growth factor beta induces rosettes of podosomes in primary aortic endothelial cells. Mol Cell Biol 26, 3582-3594 (2006)
38. Wang, W., S. Goswami, K. Lapidus, A. L. Wells, J. B. Wyckoff, E. Sahai, R. H. Singer, J. E. Segall, and J. S. Condeelis: Identification and testing of a gene expression signature of invasive carcinoma cells within primary mammary tumors. Cancer Res 64, 8585-8594 (2004)
39. Ridley, A. J., and A. Hall: The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70, 389-399 (1992)
40. Ridley, A. J., H. F. Paterson, C. L. Johnston, D. Diekmann, and A. Hall: The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell 70, 401-410 (1992)
41. Edwards, D. C., L. C. Sanders, G. M. Bokoch, and G. N. Gill: Activation of LIM-kinase by Pak1 couples Rac/Cdc42 GTPase signalling to actin cytoskeletal dynamics. Nat Cell Biol 1, 253-259 (1999)
42. Takenawa, T., and S. Suetsugu: The WASP-WAVE protein network: connecting the membrane to the cytoskeleton. Nat Rev Mol Cell Biol 8, 37-48 (2007)
43. Snapper, S. B., F. Takeshima, I. Anton, C. H. Liu, S. M. Thomas, D. Nguyen, D. Dudley, H. Fraser, D. Purich, M. Lopez-Ilasaca, C. Klein, L. Davidson, R. Bronson, R. C. Mulligan, F. Southwick, R. Geha, M. B. Goldberg, F. S. Rosen, J. H. Hartwig, and F. W. Alt: N-WASP deficiency reveals distinct pathways for cell surface projections and microbial actinbased motility. Nat Cell Biol 3, 897-904 (2001)
44. Lorenz, M., H. Yamaguchi, Y. Wang, R. H. Singer, and J. Condeelis: Imaging sites of N-WASP activity in lamellipodia and invadopodia of carcinoma cells. Curr Biol 14, 697-703 (2004)
45. Linder, S., D. Nelson, M. Weiss, and M. Aepfelbacher: Wiskott-Aldrich syndrome protein regulates podosomes in primary human macrophages. Proc Natl Acad Sci USA 96, 9648-9653 (1999)
46. Stovold, C. F., T. H. Millard, and L. M. Machesky: Inclusion of Scar/WAVE3 in a similar complex to Scar/WAVE1 and BMC Cell Biol 6, 11 (2005)
47. Mizutani, K., D. Koike, S. Suetsugu, and T. Takenawa: WAVE3 functions as a negative regulator of LDOC1. J Biochem 138, 639-646 (2005)
48. Sossey-Alaoui, K., T. A. Ranalli, X. Li, A. V. Bakin, and J. K. Cowell: WAVE3 promotes cell motility and invasion through the regulation of MMP-1, MMP-3, and MMP-9 expression. Exp Cell Res 308, 135-145 (2005)
49. Sossey-Alaoui, K., X. Li, T. A. Ranalli, and J. K. Cowell: WAVE3-mediated cell migration and lamellipodia formation are regulated downstream of phosphatidylinositol 3-kinase. J Biol Chem 280, 21748-21755 (2005)
50. Ichetovkin, I., W. Grant, and J. Condeelis: Cofilin produces newly polymerized actin filaments that are preferred for dendritic nucleation by the Arp2/3 complex. Curr Biol 12,79-84 (2002)
51. Uruno, T., J. Liu, P. Zhang, Y Fan, C. Egile, R. Li, S. C. Mueller, and X. Zhan: Activation of Arp2/3 complexmediated actin polymerization by cortactin. Nat Cell Biol 3, 259-266 (2001)
52. Weaver, A. M., A. V. Karginov, A. W. Kinley, S. A. Weed, Y. Li, J. T. Parsons, and J. A. Cooper: Cortactin promotes and stabilizes Arp2/3-induced actin filament network formation. Curr Biol 11, 370-374 (2001)
53. Martinez-Quiles, N., H. Y. Ho, M. W. Kirschner, N. Ramesh, and R. S. Geha: Erk/Src phosphorylation of cortactin acts as a switch on-switch off mechanism that controls its ability to activate N-WASP. Mol Cell Biol 24, 5269-5280 (2004)
54. Yonezawa, N., E. Nishida, K. Iida, I. Yahara, and H. Sakai: Inhibition of the interactions of cofilin, destrin, and deoxyribonuclease I with actin by phosphoinositides. J Biol Chem 265, 8382-8386 (1990)
55. Mouneimne, G., L. Soon, V. DesMarais, M. Sidani, X. Song, S. C. Yip, M. Ghosh, R. Eddy, J. M. Backer, and J. Condeelis: Phospholipase C and cofilin are required for carcinoma cell directionality in response to EGF stimulation. J Cell Biol 166, 697-708 (2004)
56. Mizuno, K., L. Okano, K. Ohashi, K. Nunoue, K. I. Kuma, T. Miyata, and T. Nakamura: Identification of a human cDNA encoding a novel protein kinase with two repeats of the LIM/double zinc finger motif. Oncogene 9, 1605-1612 (1994)
57. Okano, I., J. Hiraoka, H. Otera, K. Nunoue, K. Ohashi, S. Iwashita, M. Hiral, and K. Mizuno: Identification and characterization of a novel family of serine/threonine kinases containing N-terminal two LIM motifs. J Biol Chem 270, 31321-31330 (1995)
58. Nunoue, K., K. Ohashi, I. Okano, and K. Mizuno: LIMK-1 and LIMK-2, two members of a LIM motifcontaining protein kinase family. Oncogene 11, 701-710 (1995)
59. Yang, N., O. Higuchi, K. Ohashi, K. Nagata, A. Wada, K. Kangawa, E. Nishida and K. Mizuno: Cofilin phosphorylation by LIM-kinase 1 and its role in Racmediated actin reorganization. Nature 393, 809-812 (1998)
60. Wang, Y., J. Liu, E. Smith, K. Zhou, J. Liao, G. Yang, M. Tan and X. Zhan: Downregulation of missing in metastasis Gene (MIM) is associated with the progression of bladder transitional carcinomas. Cancer Invest 25, 79-86 (2007)
61. Paunola, E., P. K. Mattila, and P. Lappalainen: WH2 domain: A small, versatile adapter for actin monomers. FEBS Lett 513, 92-97 (2002)
62. Gonzalez-Quevedo, R., M. Shoffer, L. Horng, and A. E. Oro: Receptor tyrosine phosphatase-dependent cytoskeletal remodeling by the hedgehog-responsive gene MIM/BEG4. J Cell Biol 168, 453-463 (2005)
63. Millard, T. H., G. Bompard, M. Y. Heung, T. R Dafforn, D. J. Scott, L. M. Machesky and K. Futterer: Structural basis of filopodia formation induced by the IRSp53/MIM homology domain of human IRSp53. Embo J 24, 240-250 (2005)
64. Disanza, A., S. Mantoani, M. Hertzog, S. Gerboth, E. Frittoli, A. Steffen, K. Berhoerster, H. Kreienkamp, F. Milanesi, P. P. D. Fiore, A. Ciliberto, T. E. B. Stradal and G. Scita: Regulation of cell shape by Cdc42 is mediated by the synergic actinbundling activity of the Eps8-IRSp53 complex. Nat Cell Biol 8, 1337-1347 (2006)
65. Miki, H., H. Yamaguchi, S. Suetsugu and T. Takenawa: IRSp53 is an essential intermediate between Rac and WAVE in the regulation of membrane ruffling. Nature 408, 732-735 (2000)
66. Lee, S. H., F. Kerff, D. Chereau, F. Ferron, A. Klug, and R. Dominguez: Structural basis for the antin-binding function of missing-in-metastasis. Structure 15, 145-155 (2007)
67. Habermann, B.: The BAR-domain family of proteins: A case of bending and binding? EMBO Rep 5, 250-255 (2004)
68. Mattila, P. K., A. Pykäläinen, J. Saarikangas, V. O. Paavilainen, H. Vihinen, E. Jokitalo, and P. Lappalainen: Missing-in-metastasis and IRSp53 deform PI (4,5)P2-rich membranes by an inverse BAR domain-like mechanism. J Cell Biol 176, 953-964 (2007)
69. Suetsugu, S., K. Murayama, A. Sakamoto, K. Hanawa- Suetsugu, A. Seto, T. Oikawa, C. Mishima, M. Shirouzu, T. Takenawa and S. Yokoyama: The RAC binding domain/IRSp53 -MIM homology domain of IRSp53 induces RAC-dependent membrane deformation. J Biol Chem 281, 35347-35358 (2006)
70. Lammers, R., R. Lerch, and A. Ullrich:The carboxylterminal tyrosine residue of protein tyrosine phosphatase alpha mediates association with focal adhesion plaques. J Biol Chem 275, 3391-3396 (2000)
71. Mustelin, T., R. T. Abraham, C. E. Rudd, A. Alonso, and J. J. Merlo: Protein tyrosine phosphorylation in T cell signaling. Front Biosci 7, d918-d969 (2002)
72. Callahan, C. A. and A. E. Oro: Monstrous attempts at adnexogenesis: Regulating hair follicle progenitors through Sonic hedgehog signaling. Curr Opin Genet Dev 11, 541-546 (2001)
73. Methot, N. and K. Basler: An absolute requirement for Cubitus interruptus in Hedgehog signaling. Development 128, 733-742 (2001)
74. Bai, C. B., W. Auerbach, J. S. Lee, D. Stephen, and A. L. Joyner: Gli2, but not Gli1, is required for initial Shh signaling and ectopic activation of the Shh pathway. Development 129, 4753-4761 (2002)
75. Taipale, J. and P. A. Beachy: The Hedgehog and Wnt signalling pathways in cancer. Nature 411, 349-354 (2001)
76. Moon, R. T., B. Bowerman, M. Boutros, and N. Perrimon: The promise and perils of Wnt signaling through ?-catenin. Science 296, 1644-1646 (2002)
77. Maeda, O., N. Usami, M. Kondo, M. Takahashi, H. Goto, K. Shimokata, K. Kusugami, and Y. Sekido: Plakoglobin (?-catenin) has TCF/LEF family-dependent transcriptional activity in ?-catenin-deficient cell line. Oncogene 23, 964-972 (2004)
78. Prokhortchouk, A., B. Hendrich, H. Jorgensen, A. Ruzov, M. Wilm, G. Georgiev, A. Bird, and E. Prokhortchouk: The p120 catenin partner Kaiso is a DNA methylation dependent transcriptional repressor. Genes and Dev. 15, 1613-1618 (2001)
79. Yamashita, S., Y. Tsujino, K. Moriguchi, M. Tatematsu, T. Ushijima: Chemical genomic screening for methylation-silenced genes in gastric cancer cell lines using 5-aza-20 deoxycytidine treatment and oligonucleotide microarray. Cancer Sci 97, 64-71 (2006)
80. Millard, T. H., S. J. Sharp and L. M. Machesky: Signalling to actin assembly via the WASP (Wiskott- Aldrich syndrome protein)-family proteins and the Arp2/3 complex. Biochem J 380, 1-17 (2004)
81. Glassmann, A., S. Molly, L. Surchev, T. A. Nazwar, M. Holst, W. Hartmann, S. L. Baader, J. Oberdick, T. Pietsch and K. Schilling: Developmental expression and differentiation-related neuron-specific splicing of metastasis suppressor 1 (Mtss1) in normal and transformed cerebellar cells. BMC Dev Biol 7, 111 (2007)
82. Zhai, L., P. Zhao, A. Panebra, A. L. Guerrerio, and S. Khurana: Tyrosine phosphorylation of villin regulates the organization of the actin cytoskeleton. J Biol Chem 276, 36163-36167 (2001)
83. Williams, R. L. and S. Urbe: The emerging shape of the ESCRT machinery. Nat Rev Mol Cell Biol 8, 355-368 (2007)