Non-overlapping activities of ADF and cofilin-1 during the migration of metastatic breast tumor cells

BMC Cell Biology

Volumn 14, Issue 1, 2013, Pages

  Tahtamouni, Lubna H ^a   Shaw, Alisa E ^b   Hasan, Maram H ^a   Yasin, Salem R ^a   Bamburg, James R ^b  

^a HASHEMITE UNIVERSITY   (Jordan)

^b Veterinary Dentistry and Oral Surgery   (United States)

Author keywords

ADF; Adhesion; Cofilin; Invadopodia; Lamellipodia; Metastasis

Indexed keywords

ACTIN DEPOLYMERIZING FACTOR; COFILIN 1; COLLAGEN TYPE 1; EPIDERMAL GROWTH FACTOR; F ACTIN;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; BREAST ADENOCARCINOMA; BREAST METASTASIS; CANCER CELL CULTURE; CANCER GROWTH; CELL ADHESION; CELL ELONGATION; CELL MIGRATION; CELL POLARITY; CELL SHAPE; CELL STIMULATION; CONTROLLED STUDY; FOCAL ADHESION; GENE SILENCING; HUMAN; LAMELLIPODIUM; NONHUMAN; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RAT; RNA INTERFERENCE;

RATTUS;

ACTIN CYTOSKELETON; ACTINS; ADENOCARCINOMA; ANIMALS; CELL ADHESION; CELL MOVEMENT; COFILIN 1; DESTRIN; EPIDERMAL GROWTH FACTOR; FEMALE; FOCAL ADHESIONS; GENE EXPRESSION REGULATION, NEOPLASTIC; MAMMARY NEOPLASMS, ANIMAL; NEOPLASM METASTASIS; RATS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED;

EID: 84884965692     PISSN: None     EISSN: 14712121     Source Type: Journal    
DOI: 10.1186/1471-2121-14-45     Document Type: Article

References (74)

1. Maeda YT, Inose J, Matsuo MY, Iwaya S, Sano M. Ordered patterns of cell shape and orientational correlation during spontaneous cell migration. PLoS One 2008, 3:e3734. 10.1371/journal.pone.0003734, 2581918, 19011688.
2. Petrie RJ, Doyle AD, Yamada KM. Random versus directionally persistent cell migration. Nat Rev Mol Cell Biol 2009, 10:538-549. 10.1038/nrm2729, 2752299, 19603038.
3. Ananthakrishnan R, Ehrlicher A. The forces behind cell movement. Int J Biol Sci 2007, 3:303-317. 1893118, 17589565.
4. Streuli C. Cell Matrix Adhesion, Cell-Cell Interactions, and Malignancy. The Molecular Biology of Cancer 2006, 357-389. Oxford: Blackwell Publishing, Pelengaris SM, Khan M, 3.
5. Yamaguchi H, Condeelis J. Regulation of the actin cytoskeleton in cancer cell migration and invasion: a review. Biochim Biophys ACTA 2007, 1773:642-652. 10.1016/j.bbamcr.2006.07.001, 16926057.
6. Le Clainche C, Carlier M. Regulation of actin assembly associated with protrusion and adhesion in cell migration. Physiol Rev 2008, 88:489-513. 10.1152/physrev.00021.2007, 18391171.
7. Saarikangas J, Zhao H, Lappalainen P. Regulation of the actin cytoskeleton-plasma membrane interplay by phosphoinositides. Physiol Rev 2010, 90:259-289. 10.1152/physrev.00036.2009, 20086078.
8. Maciver S, Hussey P. The ADF/Cofilin family: actin-remodeling proteins: a review. Genome Biol 2002, 5:3007.1-3007.12.
9. Bernstein B, Bamburg J. ADF/Cofilin: a functional node in cell biology: a review. Trends Cell Biol 2010, 20:187-195. 10.1016/j.tcb.2010.01.001, 2849908, 20133134.
10. Kuure S, Cebrian C, Machingo Q, Lu BC, Chi X, Hyink D, D'Agati V, Gurniak C, Witke W, Costantini F. Actin depolymerizing factors cofilin1 and destrin are required for ureteric bud branching morphogenesis. PLoS Genet 2010, 6:e1001176. 10.1371/journal.pgen.1001176, 2965756, 21060807.
11. Yeoh S, Pope B, Mannherz H, Weeds A. Determining the differences in actin binding by human ADF and cofilin. J Mol Biol 2002, 315:911-925. 10.1006/jmbi.2001.5280, 11812157.
12. Andrianantoandro E, Pollard TD. Mechanism of actin filament turnover by severing and nucleation at different concentrations of ADF/cofilin. Mol Cell 2006, 24:13-23. 10.1016/j.molcel.2006.08.006, 17018289.
13. Ono S. Mechanism of depolymerization and severing of actin filaments and its significance in cytoskeletal dynamics. Int J Cytol 2007, 258:1-82.
14. Chen H, Bernstein BW, Sneider JM, Boyle JA, Minamide LS, Bamburg JR. In vitro activity differences between proteins of the ADF/cofilin family define two distinct subgroups. Biochem 2004, 43:7127-7142.
15. Devineni N, Minamide LS, Niu M, Safer D, Verma R, Bamburg JR, Nachmias VT. A quantitative analysis of G-actin binding proteins and the G-actin pool in developing chick brain. Brain Res 1999, 823:129-140. 10.1016/S0006-8993(99)01147-6, 10095019.
16. Bernstein B, Painter W, Chen H, Minamide L, Abe H, Bamburg J. Intracellular pH modulation of ADF/Cofilin proteins. Cell Mol Biol 2000, 47:319-336.
17. Agnew B, Minamide L, Bamburg J. Reactivation of phosphorylated actin depolymerizing factor and identification of the regulatory site. J Biol Chem 1995, 270:17582-17587. 10.1074/jbc.270.29.17582, 7615564.
18. Niwa R, Nagata-Ohashi K, Takeichi M, Mizuno K, Uemura T. Control of actin reorganization by slingshot, a family of phosphatases that dephosphorylate ADF/cofilin. Cell 2002, 108:233-246. 10.1016/S0092-8674(01)00638-9, 11832213.
19. Gohla A, Birkenfeld J, Bokoch G. Chronophin, a novel HAD-type serine protein phosphatase, regulates cofilin-dependent actin dynamics. Nat Cell Biol 2004, 7:21-29.
20. Huang TY, DerMardirossian C, Bokoch GM. Cofilin phosphatases and regulation of actin dynamics. Curr Opin Cell Biol 2006, 18:26-31. 10.1016/j.ceb.2005.11.005, 16337782.
21. Yonezawa N, Nishida E, Sakai H. pH control of actin polymerization by cofilin. J Biol Chem 1985, 260:14410-14412.
22. Hawkins M, Pope B, Maciver SK, Weeds AG. Human actin depolymerizing factor mediates a pH-sensitive destruction of actin filaments. Biochem 1993, 32:9985-9993.
23. Hayden SM, Miller PS, Brauweiler A, Bamburg JR. Analysis of the interactions of actin depolymerizing factor with G- and F-actin. Biochem 1993, 32:9994-10004.
24. Pope BJ, Zierler-Gould KM, Kühne R, Weeds AG, Ball LJ. Solution structure of human cofilin: actin binding, pH sensitivity, and relationship to actin-depolymerizing factor. J Biol Chem 2004, 279:4840-4848.
25. Hotulainen P, Paunola E, Vartiainen M, Lappalainen P. Actin-depolymerizing factor and cofilin-1 play overlapping roles in promoting rapid F-actin depolymerization in mammalian nonmuscle cells. Mol Biol Cell 2005, 16:649-664. 545901, 15548599.
26. Gurniak C, Emerald P, Witke W. The actin depolymerizing factor n-Cofilin is essential for neural tube morphogenesis and neural crest cell migration. Dev Biol 2005, 278:231-241. 10.1016/j.ydbio.2004.11.010, 15649475.
27. Ikeda S, Cunningham L, Boggess D, Hobson C, Sundberg J, Naggert J, Smith R, Nishina P. Aberrant actin cytoskeleton leads to accelerated proliferation of corneal epithelial cells in mice deficient for destrin (actin depolymerizing factor). Hum Mol Genet 2003, 12:1029-1036. 10.1093/hmg/ddg112, 12700171.
28. Wiggan O, Shaw AE, DeLuca JG, Bamburg JR. ADF/cofilin regulates actomyosin assembly through competitive inhibition of myosin II binding to F-actin. Dev Cell 2012, 22:530-543. 10.1016/j.devcel.2011.12.026, 3306597, 22421043.
29. Estornes Y, Gay F, Gevrey JC, Navoizat S, Nejjari M, Scoazec JY, Chayvialle JA, Saurin JC, Abello J. Differential involvement of destrin and Cofilin-1 in the control of invasive properties of Isreco1 human colon cancer cells. Int J Cancer 2007, 121:2162-2171. 10.1002/ijc.22911, 17583572.
30. Nebl G, Meuer SC, Samstag Y. Dephosphorylation of serine 3 regulates nuclear translocation of cofilin. J Biol Chem 1996, 271:26276-26280. 10.1074/jbc.271.42.26276, 8824278.
31. Turhani D, Krapfenbauer K, Thurnher D, Langen H, Fountoulakis M. Identification of differentially expressed, tumor-associated proteins in oral squamous cell carcinoma by proteomic analysis. Electrophoresis 2006, 27:1417-1423. 10.1002/elps.200500510, 16568407.
32. Unwin RD, Craven RA, Harnden P, Hanrahan S, Totty N, Knowles M, Eardley I, Selby PJ, Banks RE. Proteomic changes in renal cancer and co-ordinate demonstration of both the glycolytic and mitochondrial aspects of the Warburg effect. Proteomics 2003, 3:1620-1632. 10.1002/pmic.200300464, 12923786.
33. Martoglio AM, Tom BD, Starkey M, Corps AN, Charnock-Jones DS, Smith SK. Changes in tumorigenesis- and angiogenesis-related gene transcript abundance profiles in ovarian cancer detected by tailored high density cDNA arrays. Mol Med 2000, 6:750-765. 1949983, 11071270.
34. Aizawa H, Sutoh K, Tsubuki S, Kawashima S, Ishii A, Yahara I. Identification, characterization, and intracellular distribution of cofilin in Dictyostelium discoideum. J Biol Chem 1995, 270:10923-10932. 10.1074/jbc.270.18.10923, 7738034.
35. Yap CT, Simpson TI, Pratt T, Price DJ, Maciver SK. The motility of glioblastoma tumor cells is modulated by intracellular cofilin expression in a concentration-dependent manner. Cell Motil Cytoskeleton 2005, 60:153-165. 10.1002/cm.20053, 15662725.
36. Dang D, Bamburg JR, Ramos DM. Alphavbeta3 integrin and cofilin modulate K1735 melanoma cell invasion. Exp Cell Res 2006, 312:468-477. 10.1016/j.yexcr.2005.11.011, 16337627.
37. Yoshioka K, Foletta V, Bernard O, Itoh K. A role for LIM kinase in cancer invasion. Proc Natl Acad Sci USA 2003, 100:7247-7252. 10.1073/pnas.1232344100, 165861, 12777619.
38. Bagheri-Yarmand R, Mazumdar A, Sahin A, Kumar R. LIM kinase 1 increases tumor metastasis of human breast cancer cells via regulation of the urokinase-type plasminogen activator system. Int J Cancer 2006, 118:2703-2710. 10.1002/ijc.21650, 16381000.
39. Suyama E, Wadhwa R, Kawasaki H, Yaguchi T, Kaul SC, Nakajima M, Taira K. LIM kinase-2 targeting as a possible anti-metastasis therapy. J Gene Med 2004, 6:357-363. 10.1002/jgm.491, 15026997.
40. Vlecken DH, Bagowski CP. LIMK1 and LIMK2 are important for metastatic behavior and tumor cell-induced angiogenesis of pancreatic cancer cells. Zebrafish 2009, 6:433-439. 10.1089/zeb.2009.0602, 20047470.
41. Condeelis J, Pollard JW. Macrophages: obligate partners for tumor cell migration, invasion, and metastasis. Cell 2006, 124:263-266. 10.1016/j.cell.2006.01.007, 16439202.
42. Mouneimne G, Soon L, DesMarais V, Sidani M, Song X, Yip S, Ghosh M, Eddy R, Backer J, Condeelis J. Phospholipase C and cofilin are required for carcinoma cell directionality in response to EGF stimulation. J Cell Biol 2004, 166:697-708. 10.1083/jcb.200405156, 2172433, 15337778.
43. vanRheenen J, Song X, Roosmalen W, Cammer M, Chen X, DesMarais V, Yip S, Backer J, Eddy R, Condeelis J. EGF-induced PIP2 hydrolysis releases and activates cofilin locally in carcinoma cells. J Cell Biol 2007, 179:1247-1259. 10.1083/jcb.200706206, 2140025, 18086920.
44. Chen P, Xie H, Sekar MC, Gupta K, Wells A. Epidermal growth factor receptor-mediated cell motility: phospholipase C activity is required, but mitogen-activated protein kinase activity is not sufficient for induced cell movement. J Cell Biol 1994, 127:847-857. 10.1083/jcb.127.3.847, 2120228, 7962064.
45. Chen L, Janetopoulos C, Huang Y, Iijima M, Borleis J, Devreotes P. Two phases of actin polymerization display different dependencies on PI(3,4,5)P3 accumulation and have unique roles during chemotaxis. Mol Biol Cell 2003, 14:5028-5037. 10.1091/mbc.E03-05-0339, 284804, 14595116.
46. Chan Y, Bailly M, Zebda N, Segall J, Condeelis J. Role of cofilin in epidermal growth factor-stimulated actin polymerization and lamellipod protrusion. J Cell Biol 2000, 148:531-542. 10.1083/jcb.148.3.531, 2174812, 10662778.
47. Yamaguchi H, Yoshida S, Muroi E, Kawamura M, Kouchi Z, Nakamura Y, Sakai R, Fukami K. Phosaphatidylinositol 4,5-biphosphate and PIP5-kinaseIα are required for invadopodia formation in human breast cancer cells. Cancer Sci 2010, 101:1632-1638. 10.1111/j.1349-7006.2010.01574.x, 20426790.
48. Shaw AE, Minamide LS, Bill CL, Funk JD, Maiti S, Bamburg JR. Cross-reactivity of antibodies to actin- depolymerizing factor/cofilin family proteins and identification of the major epitope recognized by a mammalian actin-depolymerizing factor/cofilin antibody. Electrophoresis 2004, 25:2611-2620. 10.1002/elps.200406017, 15300782.
49. Tammana T, Sahasrabuddhe A, Bajpai V, Gupta M. ADF/Cofilin-driven actin dynamics in early events of Leishmania cell division. J Cell Sci 2010, 123:1894-1901. 10.1242/jcs.068494, 20460437.
50. Sidani M, Wessels D, Mouneimne G, Ghosh M, Goswami S, Sarmiento C, Wang W, Kuhl S, El-Sibai M, Backer J, Eddy R, Soll D, Condeelis J. Cofilin determines the migration behavior and turning frequency of metastatic cancer cells. J Cell Biol 2007, 179:777-791. 10.1083/jcb.200707009, 2080932, 18025308.
51. Zebda N, Bernard O, Bailly M, Welti S, Lawrence D, Condeelis J. Phosphorylation of ADF/Cofilin abolishes EGF-induced actin nucleation at the leading edge and subsequent lamellipod extension. J Cell Biol 2000, 151:1119-1128. 10.1083/jcb.151.5.1119, 2174362, 11086013.
52. Artym VV, Yamada KM, Mueller SC. ECM degradation assays for analyzing local cell invasion. Methods Mol Biol 2009, 522:211-219. 10.1007/978-1-59745-413-1_15, 19247615.
53. Montanez E, Piwko-Czuchra A, Bauer M, Li S, Yurchenco P, Fassler R. Integrin. Methods of Enzymology 2007, 239-286. San Diego: Academic Press, Cheresh DA, 2.
54. Wang W, Goswami S, Lapidus K, Wells AL, Wyckoff JB, Sahai E, Singer RH, Segall JE, Condeelis JS. Identification and testing of a gene expression signature of invasive carcinoma cells within primary mammary tumors. Cancer Res 2004, 64:8585-8594. 10.1158/0008-5472.CAN-04-1136, 15574765.
55. Wang W, Mouneimne G, Sidani M, Wyckoff J, Chen X, Makris A, Goswami S, Bresnick AR, Condeelis JS. The activity status of cofilin is directly related to invasion, intravasation, and metastasis of mammary tumors. J Cell Biol 2006, 173:395-404. 10.1083/jcb.200510115, 2063840, 16651380.
56. Zaidel-Bar R, Cohen M, Addadi L, Geiger B. Hierarchical assembly of cell matrix adhesion complexes. Biochem Soc T 2004, 32:416-420.
57. Hotulainen P, Lappalainen P. Stress fibers are generated by two distinct actin assembly mechanisms in motile cells. J Cell Biol 2006, 173:383-394. 10.1083/jcb.200511093, 2063839, 16651381.
58. Chen C, Alonso J, Ostuni E, Whitesides G, Ingberb D. Cell shape provides global control of focal adhesion assembly. Biochem Biophys Res Comm 2003, 307:355-361. 10.1016/S0006-291X(03)01165-3, 12859964.
59. Deguchi S, Sato M. Biomechanical properties of actin stress fibers of non-motile cells. Biorheology 2009, 46:93-105.
60. Guo WH, Wang YL. A three component mechanism for fibroblast migration with a contractile cell body that couples a myosin II-independent propulsive anterior to a myosin II-dependent resistive tail. Mol Biol Cell 2012, 23:1657-1663. 10.1091/mbc.E11-06-0556, 3338433, 22398722.
61. Horita Y, Ohashi K, Mukai M, Inoue M, Mizuno K. Suppression of the invasive capacity of rat ascites hepatoma cells by knockdown of slingshot or LIM-kinase. J Biol Chem 2008, 283:6013-6021. 10.1074/jbc.M706538200, 18171679.
62. Toshima J, Toshima J, Amano T, Yang N, Narumiya S, Mizuno K. Cofilin phosphorylation by protein kinase testicular protein kinase 1 and its role in integrin-mediated actin reorganization and focal adhesion formation. Mol Biol Cell 2001, 12:1131-1145. 10.1091/mbc.12.4.1131, 32292, 11294912.
63. Marshall TW, Aloor HL, Bear JE. Coronin 2A regulates a subset of focal-adhesion-turnover events through the cofilin pathway. J Cell Sci 2009, 122:3061-3069. 10.1242/jcs.051482, 2729258, 19654210.
64. Mseka T, Bamburg J, Cramer L. ADF/Cofilin family proteins control formation of oriented actin-filament bundles in the cell body to trigger fibroblast polarization. J Cell Sci 2007, 120:4332-4344. 10.1242/jcs.017640, 18042624.
65. Dawe H, Minamide L, Bamburg J, Cramer L. ADF/Cofilin controls cell polarity during fibroblast migration. Curr Biol 2003, 13:252-257. 10.1016/S0960-9822(03)00040-X, 12573223.
66. Mseka T, Cramer LP. Actin depolymerization-based force retracts the cell rear in polarizing and migrating cells. Curr Biol 2011, 21:2085-2091. 10.1016/j.cub.2011.11.006, 22137472.
67. Vartiainen K, Mustonen T, Mattila K, Ojala J, Thesleff I, Partanen J, Lappalainen P. The three mouse actin-depolymerizing factor/cofilins evolved to fulfill cell-type-specific requirements for actin dynamics. Mol Biol Cell 2002, 13:183-194. 10.1091/mbc.01-07-0331, 65081, 11809832.
68. Lee CW, Vitriol EA, Shim S, Wise AL, Velayutham RP, Zheng HQ. Dynamic localization of G-actin during membrane protrusion in neuronal motility. Curr Biol 2013, 23:1-11.
69. Rochelle T, Daubon T, Van Troys M, Harnois T, Waterschoot D, Ampe C, Roy L, Bourmeyster N, Constantin B. p210bcr-abl induces amoeboid motility by recruiting ADF/destrin through RhoA/ROCK1. FASEB J 2013, 27:123-134. 10.1096/fj.12-205112, 23047898.
70. Brummelkamp TR, Bernards R, Agami R. Stable suppression of tumorigenicity by virus-mediated RNA interference. Cancer Cell 2002, 2:243-247. 10.1016/S1535-6108(02)00122-8, 12242156.
71. He TC, Zhou S, da Costa LT, Yu J, Kinzler KW, Vogelstein B. A simplified system for generating recombinant adenoviruses. Proc Natl Acad Sci USA 1998, 95:2509-2514. 10.1073/pnas.95.5.2509, 19394, 9482916.
72. Garvalov B, Flynn K, Neukirchen D, Meyn L, Teusch N, Wu X, Brakebusch C, Bamburg J, Bradke F. Cdc42 regulates cofilin during the establishment of neuronal polarity. J Neurosci 2007, 27:13117-13129. 10.1523/JNEUROSCI.3322-07.2007, 18045906.
73. Minamide L, Shaw A, Sarmiere P, Wiggan O, Maloney M, Bernstein B, Sneider J, Gonzalez J, Bamburg J. Production and use of replication-deficient adenovirus for transgene expression in neurons. Methods Cell Biol 2003, 71:387-416.
74. Wessel D, Flügge UI. A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal Biochem 1984, 138:141-143. 10.1016/0003-2697(84)90782-6, 6731838.