Expression and Y435-phosphorylation of Abelson interactor 1 (Abi1) promotes tumour cell adhesion, extracellular matrix degradation and invasion by colorectal carcinoma cells

Molecular Cancer

Volumn 13, Issue 1, 2014, Pages

  Steinestel, Konrad ^a,b   Brüderlein, Silke ^b   Lennerz, Jochen K ^b   Steinestel, Julie ^b   Kraft, Klaus ^c   Pröpper, Christian ^d   Meineke, Viktor ^a   Möller, Peter ^b  

^a Bundeswehr Institute of Radiobiology   (Germany)

^b UNIVERSITY HOSPITAL ULM   (Germany)

^c Institute of Pathology and Molecular Pathology Bundeswehrkrankenhaus Ulm   (Germany)

^d UNIVERSITY OF ULM   (Germany)

Author keywords

Abelson interactor 1 (Abi1); Colorectal carcinoma; Extracellular matrix (ECM); Invasion; Metastasis

Indexed keywords

ABELSON INTERACTOR 1 PROTEIN; CASPASE 3; FIBRONECTIN; GELATINASE B; MESSENGER RNA; PROTEIN; UNCLASSIFIED DRUG; ABI1 PROTEIN, HUMAN; ACTIN; BENZAMIDE DERIVATIVE; CHD1 PROTEIN, HUMAN; CYTOSKELETON PROTEIN; DNA BINDING PROTEIN; DNA HELICASE; IMATINIB; KRAS PROTEIN, HUMAN; ONCOPROTEIN; PIPERAZINE DERIVATIVE; PYRIMIDINE DERIVATIVE; RAS PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ARTICLE; CANCER CELL CULTURE; CELL ADHESION; COLORECTAL CARCINOMA; ENZYME PHOSPHORYLATION; EXTRACELLULAR MATRIX; FEMALE; GENE EXPRESSION; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MAJOR CLINICAL STUDY; MALE; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RNA INTERFERENCE; TUMOR INVASION; AGED; CELL MOTION; COLORECTAL TUMOR; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MIDDLE AGED; PATHOLOGY; PHOSPHORYLATION; VERY ELDERLY;

ACTINS; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AGED; AGED, 80 AND OVER; BENZAMIDES; CELL ADHESION; CELL MOVEMENT; COLORECTAL NEOPLASMS; CYTOSKELETAL PROTEINS; DNA HELICASES; DNA-BINDING PROTEINS; EXTRACELLULAR MATRIX; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; MIDDLE AGED; PHOSPHORYLATION; PIPERAZINES; PROTO-ONCOGENE PROTEINS; PYRIMIDINES; RAS PROTEINS;

EID: 84903160508     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-13-145     Document Type: Article

References (48)

1. Brenner H, Bouvier AM, Foschi R, Hackl M, Larsen IK, Lemmens V, Mangone L, Francisci S. Progress in colorectal cancer survival in Europe from the late 1980s to the early 21st century: the EUROCARE study. Int J Cancer 2012, 131:1649-1658. 10.1002/ijc.26192, 21607946.
2. Jass JR, Love SB, Northover JM. A new prognostic classification of rectal cancer. Lancet 1987, 1:1303-1306.
3. Ueno H, Murphy J, Jass JR, Mochizuki H, Talbot IC. Tumour 'budding' as an index to estimate the potential of aggressiveness in rectal cancer. Histopathology 2002, 40:127-132. 10.1046/j.1365-2559.2002.01324.x, 11952856.
4. Linder S, Wiesner C, Himmel M. Degrading devices: invadosomes in proteolytic cell invasion. Annu Rev Cell Dev Biol 2011, 27:185-211. 10.1146/annurev-cellbio-092910-154216, 21801014.
5. Ridley AJ. Life at the leading edge. Cell 2011, 145:1012-1022. 10.1016/j.cell.2011.06.010, 21703446.
6. Le Clainche C, Carlier MF. 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. Courtney KD, Grove M, Vandongen H, Vandongen A, LaMantia AS, Pendergast AM. Localization and phosphorylation of Abl-interactor proteins, Abi-1 and Abi-2, in the developing nervous system. Mol Cell Neurosci 2000, 16:244-257. 10.1006/mcne.2000.0865, 10995551.
8. Proepper C, Johannsen S, Liebau S, Dahl J, Vaida B, Bockmann J, Kreutz MR, Gundelfinger ED, Boeckers TM. Abelson interacting protein 1 (Abi-1) is essential for dendrite morphogenesis and synapse formation. EMBO J 2007, 26:1397-1409. 10.1038/sj.emboj.7601569, 1817621, 17304222.
9. Proepper C, Steinestel K, Schmeisser MJ, Heinrich J, Steinestel J, Bockmann J, Liebau S, Boeckers TM. Heterogeneous nuclear ribonucleoprotein k interacts with Abi-1 at postsynaptic sites and modulates dendritic spine morphology. PLoS One 2011, 6:e27045. 10.1371/journal.pone.0027045, 3216941, 22102872.
10. Ito H, Morishita R, Shinoda T, Iwamoto I, Sudo K, Okamoto K, Nagata K. Dysbindin-1, WAVE2 and Abi-1 form a complex that regulates dendritic spine formation. Mol Psychiatry 2010, 15:976-986. 10.1038/mp.2010.69, 20531346.
11. Innocenti M, Gerboth S, Rottner K, Lai FP, Hertzog M, Stradal TE, Frittoli E, Didry D, Polo S, Disanza A, Benesch S, Di Fiore PP, Carlier MF, Scita G. Abi1 regulates the activity of N-WASP and WAVE in distinct actin-based processes. Nat Cell Biol 2005, 7:969-976. 10.1038/ncb1304, 16155590.
12. Takenawa T, Suetsugu S. The WASP-WAVE protein network: connecting the membrane to the cytoskeleton. Nat Rev Mol Cell Biol 2007, 8:37-48. 10.1038/nrm2069, 17183359.
13. Dubielecka PM, Ladwein KI, Xiong X, Migeotte I, Chorzalska A, Anderson KV, Sawicki JA, Rottner K, Stradal TE, Kotula L. Essential role for Abi1 in embryonic survival and WAVE2 complex integrity. Proc Natl Acad Sci U S A 2011, 108:7022-7027. 10.1073/pnas.1016811108, 3084068, 21482783.
14. Dubielecka PM, Machida K, Xiong X, Hossain S, Ogiue-Ikeda M, Carrera AC, Mayer BJ, Kotula L. Abi1/Hssh3bp1 pY213 links Abl kinase signaling to p85 regulatory subunit of PI-3 kinase in regulation of macropinocytosis in LNCaP cells. FEBS Lett 2010, 584:3279-3286. 10.1016/j.febslet.2010.06.029, 2917628, 20598684.
15. Kotula L. Abi1, a critical molecule coordinating actin cytoskeleton reorganization with PI-3 kinase and growth signaling. FEBS Lett 2012, 586:2790-2794. 10.1016/j.febslet.2012.05.015, 22617151.
16. Sun X, Li C, Zhuang C, Gilmore WC, Cobos E, Tao Y, Dai Z. Abl interactor 1 regulates Src-Id1-matrix metalloproteinase 9 axis and is required for invadopodia formation, extracellular matrix degradation and tumor growth of human breast cancer cells. Carcinogenesis 2009, 30:2109-2116. 10.1093/carcin/bgp251, 2792316, 19843640.
17. Hossain S, Dubielecka PM, Sikorski AF, Birge RB, Kotula L. Crk and ABI1: binary molecular switches that regulate abl tyrosine kinase and signaling to the cytoskeleton. Genes Cancer 2012, 3:402-413. 10.1177/1947601912460051, 3513786, 23226578.
18. Bellone G, Ferrero D, Carbone A, de Quadros MR, Gramigni C, Prati A, Davidson W, Mioli P, Dughera L, Emanuelli G, Rodeck U. Inhibition of cell survival and invasive potential of colorectal carcinoma cells by the tyrosine kinase inhibitor STI571. Cancer Biol Ther 2004, 3:385-392.
19. Smith-Pearson PS, Greuber EK, Yogalingam G, Pendergast AM. Abl kinases are required for invadopodia formation and chemokine-induced invasion. J Biol Chem 2010, 285:40201-40211. 10.1074/jbc.M110.147330, 3001002, 20937825.
20. Attoub S, Rivat C, Rodrigues S, van Bocxlaer S, Bedin M, Bruyneel E, Louvet C, Kornprobst M, Andre T, Mareel M, Mester J, Gespach C. The c-kit tyrosine kinase inhibitor STI571 for colorectal cancer therapy. Cancer Res 2002, 62:4879-4883.
21. Popow-Wozniak A, Wozniakowska A, Kaczmarek L, Malicka-Blaszkiewicz M, Nowak D. Apoptotic effect of imatinib on human colon adenocarcinoma cells: influence on actin cytoskeleton organization and cell migration. Eur J Pharmacol 2011, 667:66-73. 10.1016/j.ejphar.2011.05.036, 21658383.
22. Steinestel K, Bruderlein S, Steinestel J, Markl B, Schwerer MJ, Arndt A, Kraft K, Propper C, Moller P. Expression of Abelson interactor 1 (Abi1) correlates with inflammation, KRAS mutation and adenomatous change during colonic carcinogenesis. PLoS One 2012, 7:e40671. 10.1371/journal.pone.0040671, 3393686, 22808230.
23. Carpenter B, McKay M, Dundas SR, Lawrie LC, Telfer C, Murray GI. Heterogeneous nuclear ribonucleoprotein K is over expressed, aberrantly localised and is associated with poor prognosis in colorectal cancer. Br J Cancer 2006, 95:921-927. 10.1038/sj.bjc.6603349, 2360539, 16953238.
24. Klimek-Tomczak K, Mikula M, Dzwonek A, Paziewska A, Karczmarski J, Hennig E, Bujnicki JM, Bragoszewski P, Denisenko O, Bomsztyk K, Ostrowski J. Editing of hnRNP K protein mRNA in colorectal adenocarcinoma and surrounding mucosa. Br J Cancer 2006, 94:586-592. 10.1038/sj.bjc.6602938, 2361188, 16404425.
25. Iwaya K, Oikawa K, Semba S, Tsuchiya B, Mukai Y, Otsubo T, Nagao T, Izumi M, Kuroda M, Domoto H, Mukai K. Correlation between liver metastasis of the colocalization of actin-related protein 2 and 3 complex and WAVE2 in colorectal carcinoma. Cancer Sci 2007, 98:992-999. 10.1111/j.1349-7006.2007.00488.x, 17459058.
26. Yanagawa R, Furukawa Y, Tsunoda T, Kitahara O, Kameyama M, Murata K, Ishikawa O, Nakamura Y. Genome-wide screening of genes showing altered expression in liver metastases of human colorectal cancers by cDNA microarray. Neoplasia (New York, NY) 2001, 3:395.
27. Giannelli G, Falk-Marzillier J, Schiraldi O, Stetler-Stevenson WG, Quaranta V. Induction of cell migration by matrix metalloprotease-2 cleavage of laminin-5. Science 1997, 277:225-228. 10.1126/science.277.5323.225, 9211848.
28. Stradal T, Courtney KD, Rottner K, Hahne P, Small JV, Pendergast AM. The Abl interactor proteins localize to sites of actin polymerization at the tips of lamellipodia and filopodia. Curr Biol 2001, 11:891-895. 10.1016/S0960-9822(01)00239-1, 11516653.
29. Chen H, Wu X, Pan ZK, Huang S. Integrity of SOS1/EPS8/ABI1 tri-complex determines ovarian cancer metastasis. Cancer Res 2010, 70:9979-9990. 10.1158/0008-5472.CAN-10-2394, 3059077, 21118970.
30. Wang C, Tran-Thanh D, Moreno JC, Cawthorn TR, Jacks LM, Wang DY, McCready DR, Done SJ. Expression of Abl interactor 1 and its prognostic significance in breast cancer: a tissue-array-based investigation. Breast Cancer Res Treat 2011, 129:373-386. 10.1007/s10549-010-1241-0, 21046228.
31. The GeneSapiens database. [http://www.genesapiens.org].
32. The human protein atlas. [http://www.proteinatlas.org].
33. Uhlen M, Oksvold P, Fagerberg L, Lundberg E, Jonasson K, Forsberg M, Zwahlen M, Kampf C, Wester K, Hober S, Wernerus H, Björling L, Ponten F. Towards a knowledge-based Human Protein Atlas. Nat Biotechnol 2010, 28:1248-1250. 10.1038/nbt1210-1248, 21139605.
34. Uhlen M, Bjorling E, Agaton C, Szigyarto CA, Amini B, Andersen E, Andersson AC, Angelidou P, Asplund A, Asplund C, Berglund L, Bergström K, Brumer H, Cerjan D, Ekström M, Elobeid A, Eriksson C, Fagerberg L, Falk R, Fall J, Forsberg M, Björklund MG, Gumbel K, Halimi A, Hallin I, Hamsten C, Hansson M, Hedhammar M, Hercules G, Kampf C, et al. A human protein atlas for normal and cancer tissues based on antibody proteomics. Mol Cell Proteomics 2005, 4:1920-1932. 10.1074/mcp.M500279-MCP200, 16127175.
35. Betge J, Pollheimer MJ, Lindtner RA, Kornprat P, Schlemmer A, Rehak P, Vieth M, Hoefler G, Langner C. Intramural and extramural vascular invasion in colorectal cancer: prognostic significance and quality of pathology reporting. Cancer 2012, 118:628-638. 10.1002/cncr.26310, 21751188.
36. Remy L, Trespeuch C, Bachy S, Scoazec JY, Rousselle P. Matrilysin 1 influences colon carcinoma cell migration by cleavage of the laminin-5 beta3 chain. Cancer Res 2006, 66:11228-11237. 10.1158/0008-5472.CAN-06-1187, 17145868.
37. Makrodouli E, Oikonomou E, Koc M, Andera L, Sasazuki T, Shirasawa S, Pintzas A. BRAF and RAS oncogenes regulate Rho GTPase pathways to mediate migration and invasion properties in human colon cancer cells: a comparative study. Mol Cancer 2011, 10:118. 10.1186/1476-4598-10-118, 3189908, 21943101.
38. Lin Y-N, Izbicki JR, König A, Habermann JK, Blechner C, Lange T, Schumacher U, Windhorst S. Expression of DIAPH1 is up-regulated in colorectal cancer and its down-regulation strongly reduces the metastatic capacity of colon carcinoma cells. Int J Cancer 2014, 134:1571-1582. 10.1002/ijc.28486, 24105619.
39. Giannelli G, Antonaci S. Biological and clinical relevance of Laminin-5 in cancer. Clin Exp Metastasis 2000, 18:439-443. 10.1023/A:1011879900554, 11592300.
40. Kim YW, Ko YT, Kim NK, Chung HC, Min BS, Lee KY, Park JP, Kim H. A comparative study of protein expression in primary colorectal cancer and synchronous hepatic metastases: the significance of matrix metalloproteinase-1 expression as a predictor of liver metastasis. Scand J Gastroenterol 2010, 45:217-225. 10.3109/00365520903453158, 20095886.
41. Murray GI, Duncan ME, O'Neil P, Melvin WT, Fothergill JE. Matrix metalloproteinase-1 is associated with poor prognosis in colorectal cancer. Nat Med 1996, 2:461-462. 10.1038/nm0496-461, 8597958.
42. Kilpinen S, Autio R, Ojala K, Iljin K, Bucher E, Sara H, Pisto T, Saarela M, Skotheim RI, Bjorkman M, Mpindi JP, Haapa-Paananen S, Vainio P, Edgren H, Wolf M, Astola J, Nees M, Hautaniemi S, Kallioniemi O. Systematic bioinformatic analysis of expression levels of 17,330 human genes across 9,783 samples from 175 types of healthy and pathological tissues. Genome Biol 2008, 9:R139. 10.1186/gb-2008-9-9-r139, 2592717, 18803840.
43. Moller P, Koretz K, Leithauser F, Bruderlein S, Henne C, Quentmeier A, Krammer PH. Expression of APO-1 (CD95), a member of the NGF/TNF receptor superfamily, in normal and neoplastic colon epithelium. Int J Cancer 1994, 57:371-377. 10.1002/ijc.2910570314, 8168998.
44. Liebau S, Steinestel J, Linta L, Kleger A, Storch A, Schoen M, Steinestel K, Proepper C, Bockmann J, Schmeisser MJ, Boeckers TM. An SK3 channel/nWASP/Abi-1 complex is involved in early neurogenesis. PLoS One 2011, 6:e18148. 10.1371/journal.pone.0018148, 3064656, 21464958.
45. Collins TJ. ImageJ for microscopy. Biotechniques 2007, 43:25-30.
46. 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.
47. Chu CY, Rana TM. Potent RNAi by short RNA triggers. RNA 2008, 14:1714-1719. 10.1261/rna.1161908, 2525957, 18658119.
48. Terranova VP, Hujanen ES, Loeb DM, Martin GR, Thornburg L, Glushko V. Use of a reconstituted basement membrane to measure cell invasiveness and select for highly invasive tumor cells. Proc Natl Acad Sci U S A 1986, 83:465-469. 10.1073/pnas.83.2.465, 322880, 3455782.