Increased cellular apoptosis susceptibility (CSE1L/CAS) protein expression promotes protrusion extension and enhances migration of MCF-7 breast cancer cells

Experimental Cell Research

Volumn 316, Issue 17, 2010, Pages 2969-2981

  Tai, Cheng Jeng ^a   Shen, Shing Chuan ^a   Lee, Woan Ruoh ^a   Liao, Ching Fong ^b   Deng, Win Ping ^a   Chiou, Hung Yi ^a   Hsieh, Cheng I ^a   Tung, Jai Nien ^c   Chen, Ching Shyang ^a   Chiou, Jeng Fong ^a   Li, Li Tzu ^b   Lin, Chuang Yu ^b   Hsu, Chung Huei ^a   Jiang, Ming Chung ^a  

^a TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^b INSTITUTE OF CELLULAR AND ORGANISMIC BIOLOGY   (Taiwan)

^c TUNGS' TAICHUNG METROHARBOR HOSPITAL   (Taiwan)

Author keywords

Cancer; Microtubules; Migration; Protrusion; Tubulin; Tyrosine phosphorylation

Indexed keywords

ALPHA TUBULIN; BETA TUBULIN; CELLULAR APOPTOSIS SUSCEPTIBILITY PROTEIN; GLUTATHIONE TRANSFERASE; GREEN FLUORESCENT PROTEIN; TUBULIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BREAST CANCER; CELL ASSAY; CELL INVASION; CELL MEMBRANE; CELL MIGRATION; CELL STRAIN MCF 7; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; IN VITRO STUDY; MICROTUBULE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PSEUDOPODIUM; BREAST TUMOR; CELL MOTION; CELL SURFACE; FEMALE; GENETICS; METABOLISM; PATHOLOGY; PHOSPHORYLATION; PHYSIOLOGY; TUMOR CELL LINE;

BREAST NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; CELL SURFACE EXTENSIONS; CELLULAR APOPTOSIS SUSCEPTIBILITY PROTEIN; FEMALE; HUMANS; MICROTUBULES; PHOSPHORYLATION; TUBULIN;

EID: 77956874827     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2010.07.019     Document Type: Article

References (88)

1. Watanabe T., Noritake J., Kaibuchi K. Regulation of microtubules in cell migration. Trends Cell Biol. 2005, 15:76-83.
2. Dhamodharan R., Wadsworth P. Modulation of microtubule dynamic instability in vivo by brain microtubule associated proteins. J. Cell Sci. 1995, 108:1679-1689.
3. Nogales E. Structural insights into microtubule function. Annu. Rev. Biochem. 2000, 69:277-302.
4. Cassimeris L., Spittle C. Regulation of microtubule-associated proteins. Int. Rev. Cytol. 2001, 210:163-226.
5. Itoh T.J., Hotani H. Microtubule dynamics and the regulation by microtubule-associated proteins (MAPs). Biol. Sci. Space 2004, 18:116-117.
6. Kline-Smith S.L., Walczak C.E. Mitotic spindle assembly and chromosome segregation: refocusing on microtubule dynamics. Mol. Cell 2004, 15:317-327.
7. Honore S., Pasquier E., Braguer D. Understanding microtubule dynamics for improved cancer therapy. Cell. Mol. Life Sci. 2005, 62:3039-3056.
8. Desai A., Mitchison T.J. Microtubule polymerization dynamics. Annu. Rev. Cell Dev. Biol. 1997, 13:83-117.
9. Brackley K.I., Grantham J. Subunits of the chaperonin CCT interact with F-actin and influence cell shape and cytoskeletal assembly. Exp. Cell Res. 2010, 316:543-553.
10. Hamao K., Morita M., Hosoya H. New function of the proline rich domain in dynamin-2 to negatively regulate its interaction with microtubules in mammalian cells. Exp. Cell Res. 2009, 315:1336-1345.
11. Gao H., Sellin L.K., Pütz M., Nickel C., Imgrund M., Gerke P., Nitschke R., Walz G., Kramer-Zucker A.G. A short carboxy-terminal domain of polycystin-1 reorganizes the microtubular network and the endoplasmic reticulum. Exp. Cell Res. 2009, 315:1157-1170.
12. Giustiniani J., Couloubaly S., Baillet A., Pourci M.L., Cantaloube I., Fourniat C., Paul J.L., Poüs C. Basal endothelial nitric oxide synthase (eNOS) phosphorylation on Ser(1177) occurs in a stable microtubule- and tubulin acetylation-dependent manner. Exp. Cell Res. 2009, 315:3509-3520.
13. Aylsworth A., Jiang S.X., Desbois A., Hou S.T. Characterization of the role of full-length CRMP3 and its calpain-cleaved product in inhibiting microtubule polymerization and neurite outgrowth. Exp. Cell Res. 2009, 315:2856-2868.
14. Grimm-Günter E.M., Milbrandt M., Merkl B., Paulsson M., Plomann M. PACSIN proteins bind tubulin and promote microtubule assembly. Exp. Cell Res. 2008, 314:1991-2003.
15. Lanza D.C., Trindade D.M., Assmann E.M., Kobarg J. Over-expression of GFP-FEZ1 causes generation of multi-lobulated nuclei mediated by microtubules in HEK293 cells. Exp. Cell Res. 2008, 314:2028-2039.
16. Yang Y., Marcello M., Endris V., Saffrich R., Fischer R., Trendelenburg M.F., Sprengel R., Rappold G. MEGAP impedes cell migration via regulating actin and microtubule dynamics and focal complex formation. Exp. Cell Res. 2006, 312:2379-2393.
17. Dong X., Liu F., Sun L., Liu M., Li D., Su D., Zhu Z., Dong J.T., Fu L., Zhou J. Oncogenic function of microtubule end-binding protein 1 in breast cancer. J. Pathol. 2010, 220:361-369.
18. Soltani M.H., Pichardo R., Song Z., Sangha N., Camacho F., Satyamoorthy K., Sangueza O.P., Setaluri V. Microtubule-associated protein 2, a marker of neuronal differentiation, induces mitotic defects, inhibits growth of melanoma cells, and predicts metastatic potential of cutaneous melanoma. Am. J. Pathol. 2005, 166:1841-1850.
19. Spiegelman B.M., Penningroth S.M., Kirschner M.W. Turnover of tubulin and the N site GTP in Chinese hamster ovary cells. Cell 1977, 12:587-600.
20. Gonzalez-Garay M.L., Cabral F. Overexpression of an epitope-tagged ß-tubulin in Chinese hamster ovary cells causes an increase in endogenous α-tubulin synthesis. Cell Motil. Cytoskeleton 1995, 31:259-272.
21. McKean P.G., Vaughan S., Gull K. The extended tubulin super-family. J. Cell Sci. 2001, 114:2723-2733.
22. Westermann S., Weber K. Post-translational modifications regulate microtubule function. Nat. Rev. Mol. Cell Biol. 2003, 4:938-947.
23. Rosenbaum J. Cytoskeleton, functions for tubulin modifications at last. Curr. Biol. 2000, 10:R801-R803.
24. Bulinski J.C., Gundersen G.G. Stabilization of post-translational modification of microtubules during cellular morphogenesis. BioEssays 1991, 13:285-293.
25. Khawaja S., Gundersen G.G., Bulinski J.C. Enhanced stability of microtubules enriched in detyrosinated tubulin is not a direct function of detyrosination level. J. Cell Biol. 1988, 106:141-149.
26. Gurland G., Gundersen G.G. Protein phosphatase inhibitors induce the selective breakdown of stable microtubules in fibroblasts and epithelial cells. Proc. Natl. Acad. Sci. USA 1993, 90:8827-8831.
27. Wandosell F., Serrano L., Avila J. Phosphorylation of alpha-tubulin carboxyl-terminal tyrosine prevents its incorporation into microtubules. J. Biol. Chem. 1987, 262:8268-8273.
28. Brinkmann U., Brinkmann E., Gallo M., Pastan I. Cloning and characterization of a cellular apoptosis susceptibility gene, the human homologue to the yeast chromosome segregation gene CSE1. Proc. Natl. Acad. Sci. USA 1995, 92:10427-10431.
29. Scherf U., Pastan I., Willingham M.C., Brinkmann U. The human CAS protein which is homologous to the CSE1 yeast chromosome segregation gene product is associated with microtubules and mitotic spindle. Proc. Natl. Acad. Sci. USA 1996, 93:2670-2674.
30. C.J. Tai, C.H. Hsu, S.C. Shen, W.R. Lee, M.C. Jiang, Cellular apoptosis susceptibility (CSE1L/CAS) protein in cancer metastasis and chemotherapeutic drug-induced apoptosis, J. Exp. Clin. Cancer Res. 29 (2010) 110.
31. J.N. Tung, T.Y. Tsao, C.J. Tai, K.T. Yeh, Y.W. Cheng, M.C. Jiang, Distribution of LAMP-1, LAMP-2 and cathepsin D in eosinophilic granular bodies: possible relationship to cyst development in pilocytic astrocytomas, J. Int. Med. Res. (in press).
32. W.C. Uen, C.J. Tai, S.C. Shen, W.R. Lee, T.Y. Tsao, W.P. Deng, H.Y. Chiou, C.H. Hsu, C.I. Hsieh, C.F. Liao, M.C. Jiang, Differential distributions of CSE1L/CAS and E-cadherin in the polarized and non-polarized epithelial glands of neoplastic colorectal epithelium, J. Mol. Histol. http://doi:10.1007/s10735-010-9286-2.
33. Jiang M.C., Luo S.F., Li L.T., Lin C.C., Du S.Y., Lin C.Y., Hsu Y.W., Liao C.F. Synergic CSE1L/CAS, TNFR-1, and p53 apoptotic pathways in combined interferon-gamma/adriamycin-induced apoptosis of Hep G2 hepatoma cells. J. Exp. Clin. Cancer Res. 2007, 26:91-99.
34. Liao C.F., Luo S.F., Shen T.Y., Lin C.H., Chien J.T., Du S.Y., Jiang M.C. CSE1L/CAS, a microtubule-associated protein, inhibits taxol (paclitaxel)-induced apoptosis but enhances cancer cell apoptosis induced by various chemotherapeutic drugs. BMB Rep. 2008, 41:210-216.
35. Liao C.F., Luo S.F., Tsai C.S., Tsao T.Y., Chen S.L., Jiang M.C. CAS enhances chemotherapeutic drug-induced p53 accumulation and apoptosis: use of CAS for high-sensitivity anticancer drug screening. Toxicol. Mech. Methods 2008, 18:771-776.
36. Tsao T.Y., Tsai C.S., Tung J.N., Chen S.L., Yue C.H., Liao C.F., Wang C.C., Jiang M.C. Function of CSE1L/CAS in the secretion of HT-29 human colorectal cells and its expression in human colon. Mol. Cell. Biochem. 2009, 327:163-170.
37. Liao C.F., Luo S.F., Li L.T., Lin C.Y., Chen Y.C., Jiang M.C. CSE1L/CAS, the cellular apoptosis susceptibility protein, enhances invasion and metastasis but not proliferation of cancer cells. J. Exp. Clin. Cancer Res. 2008, 27:15.
38. Tung M.C., Tsai C.S., Tung J.N., Tsao T.Y., Chen H.C., Yeh K.T., Liao C.F., Jiang M.C. Higher prevalence of secretory CSE1L/CAS in sera of patients with metastatic cancer. Cancer Epidemiol. Biomark. Prev. 2009, 18:1570-1577.
39. Tsai C.S., Chen H.C., Tung J.N., Tsou S.S., Tsao T.Y., Liao C.F., Chen Y.C., Yeh C.Y., Yeh K.T., Jiang M.C. Serum cellular apoptosis susceptibility protein is a potential prognostic marker for metastatic colorectal cancer. Am. J. Pathol. 2010, 176:1619-1628.
40. Ayala I., Baldassarre M., Caldieri G., Buccione R. Invadopodia: a guided tour. Eur. J. Cell Biol. 2006, 85:159-164.
41. 2α. Biomed. Pharmacother. 2009, 63:522-527.
42. Wandosell F., Serrano L., Avila J. Phosphorylation of alpha-tubulin carboxyl-terminal tyrosine prevents its incorporation into microtubules. J. Biol. Chem. 1987, 262:8268-8273.
43. Spiegelman B.M., Penningroth S.M., Kirschner M.W. Turnover of tubulin and the N site GTP in Chinese hamster ovary cells. Cell 1977, 12:587-600.
44. Libotte T., Kaiser H.W., Alt W., Bretschneider T. Polarity, protrusion-retraction dynamics and their interplay during keratinocyte cell migration. Exp. Cell Res. 2001, 270:129-137.
45. Chodniewicz D., Klemke R.L. Guiding cell migration through directed extension and stabilization of pseudopodia. Exp. Cell Res. 2004, 301:31-37.
46. Rodriguez O.C., Schaefer A.W., Mandato C.A., Forscher P., Bement W.M., Waterman-Storer C.M. Conserved microtubule-actin interactions in cell movement and morphogenesis. Nat. Cell Biol. 2003, 5:599-609.
47. Akhmanova A., Hoogenraad C.C. Microtubule plus-end-tracking proteins: mechanisms and functions. Curr. Opin. Cell Biol. 2005, 17:47-54.
48. Wandosell F., Serrano L., Hernandez M.A., Avila J. Phosphorylation of tubulin by a calmodulin-dependent protein kinase. J. Biol. Chem. 1986, 261:10332-10339.
49. Ley S.C., Verbi W., Pappin D.J., Druker B., Davies A.A., Crumpton M.J. Tyrosine phosphorylation of alpha tubulin in human T lymphocytes. Eur. J. Immunol. 1994, 24:99-106.
50. Akiyama T., Kadowaki T., Nishida E., Kadooka T., Ogawara H., Fukami Y., Sakai H., Takaku F., Kasuga M. Substrate specificities of tyrosine-specific protein kinases toward cytoskeletal proteins in vitro. J. Biol. Chem. 1986, 261:14797-14803.
51. Ishibashi K., Fujioka T., Ui M. Decreases in cAMP phosphodiesterase activity in hepatocytes cultured with herbimycin A due to cellular microtubule polymerization related to inhibition of tyrosine phosphorylation of alpha-tubulin. Eur. J. Biochem. 1999, 260:398-408.
52. Whipple R.A., Cheung A.M., Martin S.S. Detyrosinated microtubule protrusions in suspended mammary epithelial cells promote reattachment. Exp. Cell Res. 2007, 313:1326-1336.
53. Carman C.V., Som T., Kim C.M., Benovic J.L. Binding and phosphorylation of tubulin by G protein-coupled receptor kinases. J. Biol. Chem. 1998, 273:20308-20316.
54. Vallano M.L., Goldenring J.R., Lasher R.S., Delorenzo R.J. Association of calcium/calmodulin-dependent kinase with cytoskeletal preparations: phosphorylation of tubulin, neurofilament, and microtubule-associated proteins. Ann. NY Acad. Sci. 1986, 466:357-374.
55. Serrano L., Díaz-Nido J., Wandosell F., Avila J. Tubulin phosphorylation by casein kinase II is similar to that found in vivo. J. Cell Biol. 1987, 105:1731-1739.
56. Gonda M.A., Aaronson S.A., Ellmore N., Zeve V.H., Nagashima K. Ultrastructural studies of surface features of human normal and tumor cells in tissue culture by scanning and transmission electron microscopy. J. Natl. Cancer Inst. 1976, 56:245-263.
57. Berrieman H.K., Lind M.J., Cawkwell L. Do beta-tubulin mutations have a role in resistance to chemotherapy?. Lancet Oncol. 2004, 5:158-164.
58. Bunker J.M., Wilson L., Jordan M.A., Feinstein S.C. Modulation of microtubule dynamics by tau in living cells: implications for development and neurodegeneration. Mol. Biol. Cell 2004, 15:2720-2728.
59. Mennella V., Rogers G.C., Rogers S.L., Buster D.W., Vale R.D., Sharp D.J. Functionally distinct kinesin-13 family members cooperate to regulate microtubule dynamics during interphase. Nat. Cell Biol. 2005, 7:235-245.
60. Ovechkina Y., Wordeman L. Unconventional motoring: an overview of the Kin C and Kin I kinesins. Traffic 2003, 4:367-375.
61. Ligon L.A., Shelly S.S., Tokito M., Holzbaur E.L. The microtubule plus-end proteins EB1 and dynactin have differential effects on microtubule polymerization. Mol. Biol. Cell 2003, 14:1405-1417.
62. Orban-Nemeth Z., Simader H., Badurek S., Trancikova A., Propst F. Microtubule-associated protein 1S, a short and ubiquitously expressed member of the microtubule-associated protein 1 family. J. Biol. Chem. 2005, 280:2257-2265.
63. Gorovoy M., Niu J., Bernard O., Profirovic J., Minshall R., Neamu R., Voyno-Yasenetskaya T. LIM kinase 1 coordinates microtubule stability and actin polymerization in human endothelial cells. J. Biol. Chem. 2005, 280:26533-26542.
64. Tirnauer J.S., Grego S., Salmon E.D., Mitchison T.J. EB1-microtubule interactions in Xenopus egg extracts: role of EB1 in microtubule stabilization and mechanisms of targeting to microtubules. Mol. Biol. Cell 2002, 13:3614-3626.
65. Ohkura H., Garcia M.A., Toda T. Dis1/TOG universal microtubule adaptors-one MAP for all?. J. Cell Sci. 2001, 114:3805-3812.
66. Gard D.L., Kirschner M.W. A microtubule-associated protein from Xenopus eggs that specifically promotes assembly at the plus-end. J. Cell Biol. 1987, 105:2203-2215.
67. Charrasse S., Schroeder M., Gauthier-Rouviere C., Ango F., Cassimeris L., Gard D.L., Larroque C. The TOGp protein is a new human microtubule-associated protein homologous to the Xenopus XMAP215. J. Cell Sci. 1998, 111:1371-1383.
68. Galjart N. CLIPs and CLASPs and cellular dynamics. Nat. Rev. Mol. Cell Biol. 2005, 6:487-498.
69. Carvalho P., Jr M.L., Gupta M.A.Hoyt, Pellman D. Cell cycle control of kinesin-mediated transport of Bik1 (CLIP 170) regulates microtubule stability and dynein activation. Dev. Cell 2004, 6:815-829.
70. Komarova Y.A., Akhmanova A.S., Kojima S., Galjart N., Borisy G.G. Cytoplasmic linker proteins promote microtubule rescue in vivo. J. Cell Biol. 2002, 159:589-599.
71. Arnal I., Heichette C., Diamantopoulos G.S., Chretien D. CLIP-170/tubulin-curved oligomers coassemble at microtubule ends and promote rescues. Curr. Biol. 2004, 14:2086-2095.
72. Mimori-Kiyosue Y., Grigoriev I., Lansbergen G., Sasaki H., Matsui C., Severin F., Galjart N., Grosveld F., Vorobjev I., Tsukita S., Akhmanova A. CLASP1 and CLASP2 bind to EB1 and regulate microtubule plus-end dynamics at the cell cortex. J. Cell Biol. 2005, 168:141-153.
73. Sapir T., Elbaum M., Reiner O. Reduction of microtubule catastrophe events by LIS1, platelet-activating factor acetylhydrolase subunit. EMBO J. 1997, 16:6977-6984.
74. Wen Y., Eng C.H., Schmoranzer J., Cabrera-Poch N., Morris E.J., Chen M., Wallar B.J., Alberts A.S., Gundersen G.G. EB1 and APC bind to mDia to stabilize microtubules downstream of Rho and promote cell migration. Nat. Cell Biol. 2004, 6:820-830.
75. Kodama A., Karakesisoglou I., Wong E., Vaezi A., Fuchs E. ACF7: an essential integrator of microtubule dynamics. Cell 2003, 115:343-354.
76. Howell B., Larsson N., Gullberg M., Cassimeris L. Dissociation of the tubulin-sequestering and microtubule catastrophe-promoting activities of oncoprotein 18/stathmin. Mol. Biol. Cell 1999, 10:105-118.
77. Lin S.H., Nishino M., Luo W., Aumais J.P., Galfione M., Kuang J., Yu-Lee L.Y. Inhibition of prostate tumor growth by overexpression of NudC, a microtubule motor-associated protein. Oncogene 2004, 23:2499-2506.
78. Liu L., Tommasi S., Lee D.H., Dammann R., Pfeifer G.P. Control of microtubule stability by the RASSF1A tumor suppressor. Oncogene 2003, 22:8125-8136.
79. Zumbrunn J., Kinoshita K., Hyman A.A., Nathke I.S. Binding of the adenomatous polyposis coli protein to microtubules increases microtubule stability and is regulated by GSK3 beta phosphorylation. Curr. Biol. 2001, 11:44-49.
80. Hergovich A., Lisztwan J., Barry R., Ballschmieter P., Krek W. Regulation of microtubule stability by the von Hippel-Lindau tumour suppressor protein Pvhl. Nat. Cell Biol. 2003, 5:64-70.
81. Sankaran S., Starita L.M., Groen A.C., Ko M.J., Parvin J.D. Centrosomal microtubule nucleation activity is inhibited by BRCA1-dependent ubiquitination. Mol. Cell. Biol. 2005, 25:8656-8668.
82. Teckchandani A.M., Birukova A.A., Tar K., Verin A.D., Tsygankov A.Y. The multidomain protooncogenic protein c-Cbl binds to tubulin and stabilizes microtubules. Exp. Cell Res. 2005, 306:114-127.
83. Lolkema M.P., Mehra N., Jorna A.S., van Beest M., Giles R.H., Voest E.E. The von Hippel-Lindau tumor suppressor protein influences microtubule dynamics at the cell periphery. Exp. Cell Res. 2004, 301:139-146.
84. Artlieb U., Krepler R., Wiche G. Expression of microtubule-associated proteins, MAP-1 and MAP-2, in human neuroblastomas and differential diagnosis of immature neuroblasts. Lab. Investig. 1985, 53:684-691.
85. Green R.A., Kaplan K.B. Chromosome instability in colorectal tumor cells is associated with defects in microtubule plus-end attachments caused by a dominant mutation in APC. J. Cell Biol. 2003, 163:949-961.
86. Pfeifer G.P., Dammann R. Methylation of the tumor suppressor gene RASSF1A in human tumors. Biochemistry (Mosc.) 2005, 70:576-583.
87. Bernal S.D., Stahel R.A. Cytoskeleton-associated proteins: their role as cellular integrators in the neoplastic process. Crit. Rev. Oncol. Hematol. 1985, 3:191-204.
88. Tung J.N., Tsao T.Y., Chen S.L., Tai C.J., Shen S.C., Cheng Y.W., Jiang M.C. Presence of secretory cellular apoptosis susceptibility protein in cerebrospinal fluids of patients with intracerebral hemorrhage caused by stroke and neurotrauma. Neuro. Endocrinol. Lett. 2010, 31:390-398.