Skip to main content
Top
Published in: Virchows Archiv 5/2009

01-05-2009 | Original Article

βIII-tubulin at the invasive margin of colorectal cancer: possible link to invasion

Authors: A. Portyanko, P. Kovalev, J. Gorgun, E. Cherstvoy

Published in: Virchows Archiv | Issue 5/2009

Login to get access

Abstract

Cell locomotion, including cancer cell invasion, is closely associated with the dynamics of cytoskeletal structures. Previous in vitro studies indicated that tubulin isotype composition may affect polymerization properties and dynamics of microtubules. Colorectal cancer is a good model for studying tumour invasion because of the easily detectable invasive front. Hence, we investigated the localization of βIII-tubulin in colorectal cancer specimens. Immunohistochemical staining for βIII-tubulin was evident in cancer cells apparently budding from adjacent malignant cells with a higher differentiation and negative staining. An association between βIII-tubulin immunoreactivity and tumour budding grade was demonstrated. To the best of our knowledge, this is the first report documenting a preferential localization of βIII-tubulin in the invading epithelium. From this finding arises the possibility that changes in tubulin isotypes could modulate the invading activity of cancer cells. Further investigations are needed to determine whether our findings have clinical implications.
Literature
1.
go back to reference Banerjee A, Roach MC, Trcka P, Ludueña RF (1990) Increased microtubule assembly in bovine brain tubulin lacking the type III isotype of beta-tubulin. J Biol Chem 265:1794–1799PubMed Banerjee A, Roach MC, Trcka P, Ludueña RF (1990) Increased microtubule assembly in bovine brain tubulin lacking the type III isotype of beta-tubulin. J Biol Chem 265:1794–1799PubMed
2.
go back to reference Lu Q, Ludueña RF (1993) Removal of the βIII isotype enhances taxol induced microtubule assembly. Cell Struct Funct 18:173–182PubMedCrossRef Lu Q, Ludueña RF (1993) Removal of the βIII isotype enhances taxol induced microtubule assembly. Cell Struct Funct 18:173–182PubMedCrossRef
3.
go back to reference Lu Q, Ludueña RF (1994) In vitro analysis of microtubule assembly of isotypically pure tubulin dimers. Intrinsic differences in the assembly properties of αβII, αβIII, and αβIV tubulin dimers in the absence of microtubule-associated proteins. J Biol Chem 269:2041–2047PubMed Lu Q, Ludueña RF (1994) In vitro analysis of microtubule assembly of isotypically pure tubulin dimers. Intrinsic differences in the assembly properties of αβII, αβIII, and αβIV tubulin dimers in the absence of microtubule-associated proteins. J Biol Chem 269:2041–2047PubMed
4.
go back to reference Panda D, Miller HP, Banerjee A et al (1994) Microtubule dynamics in vitro are regulated by the tubulin isotype composition. Proc Natl Acad Sci USA 91:11358–11362PubMedCrossRef Panda D, Miller HP, Banerjee A et al (1994) Microtubule dynamics in vitro are regulated by the tubulin isotype composition. Proc Natl Acad Sci USA 91:11358–11362PubMedCrossRef
5.
go back to reference Derry WB, Wilson L, Khan IA et al (1997) Taxol differentially modulates the dynamics of microtubules assembled from unfractionated and purified β-tubulin isotypes. Biochemistry 36:3554–3562PubMedCrossRef Derry WB, Wilson L, Khan IA et al (1997) Taxol differentially modulates the dynamics of microtubules assembled from unfractionated and purified β-tubulin isotypes. Biochemistry 36:3554–3562PubMedCrossRef
6.
go back to reference Banerjee A, Ludueña RF (1992) Kinetics of colchicine binding to purified β-tubulin isotypes from bovine brain. J Biol Chem 267:13335–13339PubMed Banerjee A, Ludueña RF (1992) Kinetics of colchicine binding to purified β-tubulin isotypes from bovine brain. J Biol Chem 267:13335–13339PubMed
7.
go back to reference Banerjee A, D’Hoore A, Engelborghs Y (1994) Interaction of desacetamidocolchicine a fast binding analogue of colchicine with isotypically pure tubulin dimers αβII, αβIII and αβIV. J Biol Chem 269:10324–10329PubMed Banerjee A, D’Hoore A, Engelborghs Y (1994) Interaction of desacetamidocolchicine a fast binding analogue of colchicine with isotypically pure tubulin dimers αβII, αβIII and αβIV. J Biol Chem 269:10324–10329PubMed
8.
go back to reference Laing N, Dahllof B, Hartley-Asp B et al (1997) Interaction of estramustine with tubulin isotypes. Biochemistry 36:871–878PubMedCrossRef Laing N, Dahllof B, Hartley-Asp B et al (1997) Interaction of estramustine with tubulin isotypes. Biochemistry 36:871–878PubMedCrossRef
9.
go back to reference Banerjee A, Engelborghs Y, D'Hoore A et al (1997) Interaction of a bicyclic analogue of colchicine with purified β-tubulin isoforms from bovine brain. Eur J Biochem 246:420–424PubMedCrossRef Banerjee A, Engelborghs Y, D'Hoore A et al (1997) Interaction of a bicyclic analogue of colchicine with purified β-tubulin isoforms from bovine brain. Eur J Biochem 246:420–424PubMedCrossRef
10.
go back to reference Kavallaris M, Kuo D, Burkhart CA et al (1997) Taxol-resistant epithelial ovarian tumous are associated with altered expression of specific β-tubulin isotypes. J Clin Invest 100:1282–1293PubMedCrossRef Kavallaris M, Kuo D, Burkhart CA et al (1997) Taxol-resistant epithelial ovarian tumous are associated with altered expression of specific β-tubulin isotypes. J Clin Invest 100:1282–1293PubMedCrossRef
11.
go back to reference Ranganathan S, Benetatos CA, Colarusso PJ et al (1998) Altered β-tubulin isotype expression in paclitaxel-resistant human prostate carcinoma cells. Br J Cancer 77:562–566PubMed Ranganathan S, Benetatos CA, Colarusso PJ et al (1998) Altered β-tubulin isotype expression in paclitaxel-resistant human prostate carcinoma cells. Br J Cancer 77:562–566PubMed
12.
go back to reference Sangrajrang S, Denoulet P, Laing NM et al (1998) Association of estramustine resistance in human prostatic carcinoma cells with modified patterns of tubulin expression. Biochem Pharmacol 55:325–331PubMedCrossRef Sangrajrang S, Denoulet P, Laing NM et al (1998) Association of estramustine resistance in human prostatic carcinoma cells with modified patterns of tubulin expression. Biochem Pharmacol 55:325–331PubMedCrossRef
13.
go back to reference Ueno H, Murphy J, Jass JR et al (2002) Tumour ‘budding’ as an index to estimate the potential of aggressiveness in rectal cancer. Histopathology 40:127–132PubMedCrossRef Ueno H, Murphy J, Jass JR et al (2002) Tumour ‘budding’ as an index to estimate the potential of aggressiveness in rectal cancer. Histopathology 40:127–132PubMedCrossRef
14.
go back to reference Okuyama T, Oya M, Ishikawa H (2003) Budding as a useful prognostic marker in pT3 well- or moderately-differentiated rectal adenocarcinoma. J Surg Oncol 83:42–47PubMedCrossRef Okuyama T, Oya M, Ishikawa H (2003) Budding as a useful prognostic marker in pT3 well- or moderately-differentiated rectal adenocarcinoma. J Surg Oncol 83:42–47PubMedCrossRef
15.
go back to reference Wittekind CH, Meyer HJ, Bootz F (2002) International Union Against Cancer (UICC): TNM-Klassifikation maligner Tumoren, 6th edn. Springer, Berlin Wittekind CH, Meyer HJ, Bootz F (2002) International Union Against Cancer (UICC): TNM-Klassifikation maligner Tumoren, 6th edn. Springer, Berlin
16.
go back to reference Wachs FP, Couillard-Despres S, Engelhardt M et al (2003) High efficacy of clonal growth and expansion of adult neural stem cells. Lab Invest 83:949–962PubMedCrossRef Wachs FP, Couillard-Despres S, Engelhardt M et al (2003) High efficacy of clonal growth and expansion of adult neural stem cells. Lab Invest 83:949–962PubMedCrossRef
17.
go back to reference Ohishi Y, Oda Y, Basaki Y et al (2007) Expression of beta-tubulin isotypes in human primary ovarian carcinoma. Gynecol Oncol 105:586–592PubMedCrossRef Ohishi Y, Oda Y, Basaki Y et al (2007) Expression of beta-tubulin isotypes in human primary ovarian carcinoma. Gynecol Oncol 105:586–592PubMedCrossRef
18.
go back to reference Packer MA, Stasiv Y, Benraiss A et al (2003) Nitric oxide negatively regulates mammalian adult neurogenesis. Proc Natl Acad Sci USA 100:9566–9571PubMedCrossRef Packer MA, Stasiv Y, Benraiss A et al (2003) Nitric oxide negatively regulates mammalian adult neurogenesis. Proc Natl Acad Sci USA 100:9566–9571PubMedCrossRef
19.
go back to reference Shinto E, Mochizuki H, Ueno H et al (2005) A novel classification of tumour budding in colorectal cancer based on the presence of cytoplasmic pseudo-fragments around budding foci. Histopathology 47:25–31PubMedCrossRef Shinto E, Mochizuki H, Ueno H et al (2005) A novel classification of tumour budding in colorectal cancer based on the presence of cytoplasmic pseudo-fragments around budding foci. Histopathology 47:25–31PubMedCrossRef
20.
go back to reference Prall F, Ostwald C (2007) High-degree tumor budding and podiaformation in sporadic colorectal carcinomas with K-ras gene mutations. Hum Pathol 38:1696–1702PubMedCrossRef Prall F, Ostwald C (2007) High-degree tumor budding and podiaformation in sporadic colorectal carcinomas with K-ras gene mutations. Hum Pathol 38:1696–1702PubMedCrossRef
21.
go back to reference Katsetos CD, Frankfurter A, Christakos S et al (1993) Differential localization of class III β-tubulin isotype (βIII) and calbindin-D28k identifies distinct neuronal types in the developing human cerebellar cortex. J Neuropathol Exp Neurol 52:655–666PubMedCrossRef Katsetos CD, Frankfurter A, Christakos S et al (1993) Differential localization of class III β-tubulin isotype (βIII) and calbindin-D28k identifies distinct neuronal types in the developing human cerebellar cortex. J Neuropathol Exp Neurol 52:655–666PubMedCrossRef
22.
go back to reference Katsetos CD, Karkavelas G, Herman MM et al (1998) Class III β-tubulin isotype in the adrenal medulla, I: localization in the developing human adrenal medulla. Anat Rec 250:343–349 Katsetos CD, Karkavelas G, Herman MM et al (1998) Class III β-tubulin isotype in the adrenal medulla, I: localization in the developing human adrenal medulla. Anat Rec 250:343–349
23.
go back to reference Moody SA, Quigg MS, Frankfurter A (1989) The development of the peripheral trigeminal system in the chick revealed by an isotype-specific anti-β-tubulin monoclonal antibody. J Comp Neurol 279:567–580PubMedCrossRef Moody SA, Quigg MS, Frankfurter A (1989) The development of the peripheral trigeminal system in the chick revealed by an isotype-specific anti-β-tubulin monoclonal antibody. J Comp Neurol 279:567–580PubMedCrossRef
24.
go back to reference Katsetos CD, Del Valle L, Geddes JF et al (2001) Aberrant localization of the neuronal class III β-tubulin in astrocytomas. A marker for anaplastic potential. Arch Pathol Lab Med 125:613–624PubMed Katsetos CD, Del Valle L, Geddes JF et al (2001) Aberrant localization of the neuronal class III β-tubulin in astrocytomas. A marker for anaplastic potential. Arch Pathol Lab Med 125:613–624PubMed
25.
go back to reference Katsetos CD, Herman MM, Mörk SJ (2003) Class III β-tubulin in human development and cancer. Cell Motil Cytoskeleton 55:77–96PubMedCrossRef Katsetos CD, Herman MM, Mörk SJ (2003) Class III β-tubulin in human development and cancer. Cell Motil Cytoskeleton 55:77–96PubMedCrossRef
26.
go back to reference Katsetos CD, Del Valle L, Geddes JF et al (2002) Localization of the neuronal class III β-tubulin in oligodendrogliomas: comparison with Ki-67 proliferative index and 1p/19q status. J Neuropathol Exp Neurol 61:307–320PubMed Katsetos CD, Del Valle L, Geddes JF et al (2002) Localization of the neuronal class III β-tubulin in oligodendrogliomas: comparison with Ki-67 proliferative index and 1p/19q status. J Neuropathol Exp Neurol 61:307–320PubMed
27.
go back to reference Dumontet C, Isaac S, Souquet PJ et al (2002) Expression of class III β tubulin in non-small cell lung cancer is correlated with resistance to taxane chemotherapy. Elect J Oncol 1:58–64 Dumontet C, Isaac S, Souquet PJ et al (2002) Expression of class III β tubulin in non-small cell lung cancer is correlated with resistance to taxane chemotherapy. Elect J Oncol 1:58–64
28.
go back to reference Urano N, Fujiwara Y, Doki Y et al (2006) Clinical significance of class III β -tubulin expression and its predictive value for resistance to docetaxel-based chemotherapy in gastric cancer. Int J Oncol 28:375–381PubMed Urano N, Fujiwara Y, Doki Y et al (2006) Clinical significance of class III β -tubulin expression and its predictive value for resistance to docetaxel-based chemotherapy in gastric cancer. Int J Oncol 28:375–381PubMed
29.
go back to reference Gan PP, Pasquier E, Kavallaris M (2007) Class III β -tubulin mediates sensitivity to chemotherapeutic drugs in non small cell lung cancer. Cancer Res 67:9356–9363PubMedCrossRef Gan PP, Pasquier E, Kavallaris M (2007) Class III β -tubulin mediates sensitivity to chemotherapeutic drugs in non small cell lung cancer. Cancer Res 67:9356–9363PubMedCrossRef
30.
go back to reference Raspaglio G, Filippetti F, Prislei S et al (2008) Hypoxia induces class III β-tubulin gene expression by HIF-1alpha binding to its 3′ flanking region. Gene 409:100–108PubMedCrossRef Raspaglio G, Filippetti F, Prislei S et al (2008) Hypoxia induces class III β-tubulin gene expression by HIF-1alpha binding to its 3′ flanking region. Gene 409:100–108PubMedCrossRef
31.
go back to reference Izutsu N, Maesawa C, Shibazaki M et al (2008) Epigenetic modification is involved in aberrant expression of class III β-tubulin, TUBB3, in ovarian cancer cells. Int J Oncol. 32:1227–1235PubMed Izutsu N, Maesawa C, Shibazaki M et al (2008) Epigenetic modification is involved in aberrant expression of class III β-tubulin, TUBB3, in ovarian cancer cells. Int J Oncol. 32:1227–1235PubMed
Metadata
Title
βIII-tubulin at the invasive margin of colorectal cancer: possible link to invasion
Authors
A. Portyanko
P. Kovalev
J. Gorgun
E. Cherstvoy
Publication date
01-05-2009
Publisher
Springer-Verlag
Published in
Virchows Archiv / Issue 5/2009
Print ISSN: 0945-6317
Electronic ISSN: 1432-2307
DOI
https://doi.org/10.1007/s00428-009-0764-4

Other articles of this Issue 5/2009

Virchows Archiv 5/2009 Go to the issue

Review and Perspective

Mitochondria and cancer