Skip to main content
Erschienen in: Tumor Biology 2/2016

15.09.2015 | Original Article

Tubb3 regulation by the Erk and Akt signaling pathways: a mechanism involved in the effect of arginine ADP-ribosyltransferase 1 (Art1) on apoptosis of colon carcinoma CT26 cells

verfasst von: Ming Xiao, Yi Tang, Wen-Wen Chen, Ya-Lan Wang, Lian Yang, Xian Li, Guang-Lin Song, Jing Kuang

Erschienen in: Tumor Biology | Ausgabe 2/2016

Einloggen, um Zugang zu erhalten

Abstract

The influence of the most important classical mono-ADP-ribosyltransferase, arginine ADP-ribosyltransferase 1 (Art1), on survival and apoptosis of colon carcinoma cells and the potential mechanisms have been partly discussed in our previous study but still need to be further studied. In this present study, Art1 of colon carcinoma CT26 cells was silenced with lentiviral vector-mediated short hairpin RNA (shRNA) or overexpressed with lentiviral vector-mediated complementary DNA (cDNA) and allograft transplant tumors are established in Balb/c mice. We verified Art1 knockdown increases apoptosis of CT26 cells transplant tumor; Art1 overexpression acts oppositely. Accordingly, growth of transplant tumors is inhibited in Art1 knockdown transplant tumors and increases in Art1 overexpression transplant tumors. Furthermore, activity of Akt and Erk cell signal pathways and expression of an apoptosis biomarker, βIII-tubulin (Tubb3), decrease when Art1 was silenced and increase when Art1 was overexpressed. Inhibiting Akt pathway or Erk pathway both downregulates expression of Tubb3 on protein and messenger RNA (mRNA) level, indicating that Tubb3 could be regulated by both Akt and Erk pathways, and plays a role in the influence of Art1 on apoptosis of Balb/c mice allograft transplant tumor. We also demonstrated that Bcl-2 family is not the responsible downstream factor of the Erk pathway in colon carcinoma cells which is undergoing apoptosis. These findings enrich the molecular mechanism for the function of Art1 in colon carcinoma and provide a complementary support for Art1 to be a potential therapeutic target of the treatment of this kind of malignant tumor.
Literatur
1.
Zurück zum Zitat Braren R, Glowacki G, Nissen M, Haag F, Koch-Nolte F. Molecular characterization and expression of the gene for mouse NAD+:arginine ecto-mono(ADP-ribosyl)transferase, Art1. Biochem J. 1998;336:561–8.CrossRefPubMedPubMedCentral Braren R, Glowacki G, Nissen M, Haag F, Koch-Nolte F. Molecular characterization and expression of the gene for mouse NAD+:arginine ecto-mono(ADP-ribosyl)transferase, Art1. Biochem J. 1998;336:561–8.CrossRefPubMedPubMedCentral
2.
Zurück zum Zitat Seman M, Adriouch S, Haag F, Koch-Nolte F. Ecto-ADP-ribosyltransferases (ARTs): emerging actors in cell communication and signaling. Curr Med Chem. 2004;11(7):857–72.CrossRefPubMed Seman M, Adriouch S, Haag F, Koch-Nolte F. Ecto-ADP-ribosyltransferases (ARTs): emerging actors in cell communication and signaling. Curr Med Chem. 2004;11(7):857–72.CrossRefPubMed
3.
Zurück zum Zitat Balducci E, Micossi LG, Soldaini E, Rappuoli R. Expression and selective up-regulation of toxin-related mono ADP-ribosyltransferases by pathogen-associated molecular patterns in alveolar epithelial cells. FEBS Lett. 2007;581(22):4199–204.CrossRefPubMed Balducci E, Micossi LG, Soldaini E, Rappuoli R. Expression and selective up-regulation of toxin-related mono ADP-ribosyltransferases by pathogen-associated molecular patterns in alveolar epithelial cells. FEBS Lett. 2007;581(22):4199–204.CrossRefPubMed
4.
Zurück zum Zitat Del Vecchio M, Balducci E. Mono ADP-ribosylation inhibitors prevent inflammatory cytokine release in alveolar epithelial cells. Mol Cell Biochem. 2008;310(1-2):77–83.CrossRefPubMed Del Vecchio M, Balducci E. Mono ADP-ribosylation inhibitors prevent inflammatory cytokine release in alveolar epithelial cells. Mol Cell Biochem. 2008;310(1-2):77–83.CrossRefPubMed
5.
Zurück zum Zitat Yang L, Wang YL, Sheng YT, Xiong W, Xu JX, Tang Y, et al. The correlation of ART1 expression with angiogenesis in colorectal carcinoma and it relationship with VEGF and integrin αVβ3 expressions. Basic Clin Med. 2012;32:1064–9. Yang L, Wang YL, Sheng YT, Xiong W, Xu JX, Tang Y, et al. The correlation of ART1 expression with angiogenesis in colorectal carcinoma and it relationship with VEGF and integrin αVβ3 expressions. Basic Clin Med. 2012;32:1064–9.
6.
Zurück zum Zitat Xu JX, Wang YL, Tang Y, Xiong W. Effect of ART1 gene silencing by RNA interference on the proliferation of mouse colon carcinoma cells and its possible mechanism. Tumor. 2012;32(12):949–54. Xu JX, Wang YL, Tang Y, Xiong W. Effect of ART1 gene silencing by RNA interference on the proliferation of mouse colon carcinoma cells and its possible mechanism. Tumor. 2012;32(12):949–54.
7.
Zurück zum Zitat Tang Y, Li M, Wang YL, Threadgill MD, Xiao M, Mou CF, et al. ART1 promotes starvation-induced autophagy: a possible protective role in the development of colon carcinoma. Am J Cancer Res. 2015;5(2):498–513.PubMedPubMedCentral Tang Y, Li M, Wang YL, Threadgill MD, Xiao M, Mou CF, et al. ART1 promotes starvation-induced autophagy: a possible protective role in the development of colon carcinoma. Am J Cancer Res. 2015;5(2):498–513.PubMedPubMedCentral
8.
Zurück zum Zitat Tang Y, Wang YL, Yang L, Xu JX, Xiong W, Xiao M, et al. Inhibition of arginine ADP-ribosyltransferase 1 reduces the expression of poly (ADP-ribose) polymerase-1 in colon carcinoma. Int J Mol Med. 2013;32(1):130.PubMed Tang Y, Wang YL, Yang L, Xu JX, Xiong W, Xiao M, et al. Inhibition of arginine ADP-ribosyltransferase 1 reduces the expression of poly (ADP-ribose) polymerase-1 in colon carcinoma. Int J Mol Med. 2013;32(1):130.PubMed
9.
Zurück zum Zitat Xiao M, Tang Y, Wang YL, Yang L, Li X, Kuang J, et al. ART1 silencing enhances apoptosis of mouse CT26 cells via the PI3K/Akt/NF-κB pathway. Cell Physiol Biochem. 2013;32(6):1587–99.CrossRefPubMed Xiao M, Tang Y, Wang YL, Yang L, Li X, Kuang J, et al. ART1 silencing enhances apoptosis of mouse CT26 cells via the PI3K/Akt/NF-κB pathway. Cell Physiol Biochem. 2013;32(6):1587–99.CrossRefPubMed
10.
Zurück zum Zitat Zolkiewska A, Moss J. Integrin alpha 7 as substrate for a glycosylphosphatidylinositol-anchored ADP-ribosyltransferase on the surface of skeletal muscle cells. J Biol Chem. 1993;268(34):25273–6.PubMed Zolkiewska A, Moss J. Integrin alpha 7 as substrate for a glycosylphosphatidylinositol-anchored ADP-ribosyltransferase on the surface of skeletal muscle cells. J Biol Chem. 1993;268(34):25273–6.PubMed
11.
12.
Zurück zum Zitat Liu J, Burkin DJ, Kaufman SJ. Increasing α7β1-integrin promotes muscle cell proliferation, adhesion, and resistance to apoptosis without changing gene expression. Am J Physiol Cell Physiol. 2008;294(2):C627–40.CrossRefPubMed Liu J, Burkin DJ, Kaufman SJ. Increasing α7β1-integrin promotes muscle cell proliferation, adhesion, and resistance to apoptosis without changing gene expression. Am J Physiol Cell Physiol. 2008;294(2):C627–40.CrossRefPubMed
13.
Zurück zum Zitat Levallet G, Bergot E, Antoine M, Creveuil C, Santos AO, Beau-Faller M, et al. High TUBB3 expression, an independent prognostic marker in patients with early non-small cell lung cancer treated by preoperative chemotherapy, is regulated by K-Ras signaling pathway. Mol Cancer Ther. 2012;11(5):1203–13.CrossRefPubMed Levallet G, Bergot E, Antoine M, Creveuil C, Santos AO, Beau-Faller M, et al. High TUBB3 expression, an independent prognostic marker in patients with early non-small cell lung cancer treated by preoperative chemotherapy, is regulated by K-Ras signaling pathway. Mol Cancer Ther. 2012;11(5):1203–13.CrossRefPubMed
14.
Zurück zum Zitat Franke TF, Hornik CP, Segev L, Shostak GA, Sugimoto C. PI3K/Akt and apoptosis: size matters. Oncogene. 2003;22(56):8983–98.CrossRefPubMed Franke TF, Hornik CP, Segev L, Shostak GA, Sugimoto C. PI3K/Akt and apoptosis: size matters. Oncogene. 2003;22(56):8983–98.CrossRefPubMed
15.
Zurück zum Zitat Gan PP, Pasquier E, Kavallaris M. Class III β-tubulin mediates sensitivity to chemotherapeutic drugs in non-small cell lung cancer. Cancer Res. 2007;67(19):9356–63.CrossRefPubMed Gan PP, Pasquier E, Kavallaris M. Class III β-tubulin mediates sensitivity to chemotherapeutic drugs in non-small cell lung cancer. Cancer Res. 2007;67(19):9356–63.CrossRefPubMed
16.
Zurück zum Zitat Kavallaris M. Microtubules and resistance to tubulin-binding agents. Nat Rev Cancer. 2010;10(3):194–204.CrossRefPubMed Kavallaris M. Microtubules and resistance to tubulin-binding agents. Nat Rev Cancer. 2010;10(3):194–204.CrossRefPubMed
17.
Zurück zum Zitat Sève P, Dumontet C. Is class III β-tubulin a predictive factor in patients receiving tubulin-binding agents? Lancet Oncol. 2008;9(2):168–75.CrossRefPubMed Sève P, Dumontet C. Is class III β-tubulin a predictive factor in patients receiving tubulin-binding agents? Lancet Oncol. 2008;9(2):168–75.CrossRefPubMed
18.
Zurück zum Zitat Sève P, Lai R, Ding K, Winton T, Butts C, Mackey J, et al. Class III β-tubulin expression and benefit from adjuvant cisplatin/vinorelbine chemotherapy in operable non-small cell lung cancer: analysis of NCIC JBR. 10. Clin Cancer Res. 2007;13(3):994–9.CrossRefPubMed Sève P, Lai R, Ding K, Winton T, Butts C, Mackey J, et al. Class III β-tubulin expression and benefit from adjuvant cisplatin/vinorelbine chemotherapy in operable non-small cell lung cancer: analysis of NCIC JBR. 10. Clin Cancer Res. 2007;13(3):994–9.CrossRefPubMed
19.
Zurück zum Zitat Mariani M, Shahabi S, Sieber S, Scambia G, Ferlini C. Class III-tubulin (TUBB3): more than a biomarker in solid tumors? Curr Mol Med. 2011;11(9):726–31.CrossRefPubMed Mariani M, Shahabi S, Sieber S, Scambia G, Ferlini C. Class III-tubulin (TUBB3): more than a biomarker in solid tumors? Curr Mol Med. 2011;11(9):726–31.CrossRefPubMed
20.
Zurück zum Zitat Yoon SO, Kim WY, Go H, Paik JH, Kim JE, Kim YA, et al. Class III beta-tubulin shows unique expression patterns in a variety of neoplastic and non-neoplastic lymphoproliferative disorders. Am J Surg Pathol. 2010;34(5):645–55.PubMed Yoon SO, Kim WY, Go H, Paik JH, Kim JE, Kim YA, et al. Class III beta-tubulin shows unique expression patterns in a variety of neoplastic and non-neoplastic lymphoproliferative disorders. Am J Surg Pathol. 2010;34(5):645–55.PubMed
21.
Zurück zum Zitat McCarroll JA, Gan PP, Erlich RB, Liu M, Dwarte T, Sagnella S, et al. TUBB3/beta III-tubulin acts through the PTEN/AKT signaling axis to promote tumorigenesis and anoikis resistance in non-small cell lung cancer. Cancer Res. 2015;75(2):415–25.CrossRefPubMed McCarroll JA, Gan PP, Erlich RB, Liu M, Dwarte T, Sagnella S, et al. TUBB3/beta III-tubulin acts through the PTEN/AKT signaling axis to promote tumorigenesis and anoikis resistance in non-small cell lung cancer. Cancer Res. 2015;75(2):415–25.CrossRefPubMed
22.
Zurück zum Zitat Gan PP, McCarroll JA, Po’uha ST, Kamath K, Jordan MA, Kavallaris M. Microtubule dynamics, mitotic arrest, and apoptosis: drug-induced differential effects of βIII-tubulin. Mol Cancer Ther. 2010;9(5):1339–48.CrossRefPubMed Gan PP, McCarroll JA, Po’uha ST, Kamath K, Jordan MA, Kavallaris M. Microtubule dynamics, mitotic arrest, and apoptosis: drug-induced differential effects of βIII-tubulin. Mol Cancer Ther. 2010;9(5):1339–48.CrossRefPubMed
23.
Zurück zum Zitat Roque DM, Buza N, Glasgow M, Bellone S, Bortolomai I, Gasparrini S, et al. Class III beta-tubulin overexpression within the tumor microenvironment is a prognostic biomarker for poor overall survival in ovarian cancer patients treated with neoadjuvant carboplatin/paclitaxel. Clin Exp Metastasis. 2014;31(1):101–10.CrossRefPubMed Roque DM, Buza N, Glasgow M, Bellone S, Bortolomai I, Gasparrini S, et al. Class III beta-tubulin overexpression within the tumor microenvironment is a prognostic biomarker for poor overall survival in ovarian cancer patients treated with neoadjuvant carboplatin/paclitaxel. Clin Exp Metastasis. 2014;31(1):101–10.CrossRefPubMed
24.
Zurück zum Zitat Tsourlakis MC, Weigand P, Grupp K, Kluth M, Steurer S, Schlomm T, et al. betaIII-Tubulin overexpression is an independent predictor of prostate cancer progression tightly linked to ERG fusion status and PTEN deletion. Am J Pathol. 2014;184(3):609–17.CrossRefPubMed Tsourlakis MC, Weigand P, Grupp K, Kluth M, Steurer S, Schlomm T, et al. betaIII-Tubulin overexpression is an independent predictor of prostate cancer progression tightly linked to ERG fusion status and PTEN deletion. Am J Pathol. 2014;184(3):609–17.CrossRefPubMed
25.
Zurück zum Zitat Urano N, Fujiwara Y, Doki Y, Kim SJ, Miyoshi Y, Noguchi S, et al. Clinical significance of class III beta-tubulin expression and its predictive value for resistance to docetaxel-based chemotherapy in gastric cancer. Int J Oncol. 2006;28(2):375–81.PubMed Urano N, Fujiwara Y, Doki Y, Kim SJ, Miyoshi Y, Noguchi S, et al. Clinical significance of class III beta-tubulin expression and its predictive value for resistance to docetaxel-based chemotherapy in gastric cancer. Int J Oncol. 2006;28(2):375–81.PubMed
26.
Zurück zum Zitat Yu J, Gao J, Lu Z, Gong J, Li Y, Dong B, et al. Combination of microtubule associated protein-tau and β-tubulin III predicts chemosensitivity of paclitaxel in patients with advanced gastric cancer. Eur J Cancer. 2004;50(13):2328–35.CrossRef Yu J, Gao J, Lu Z, Gong J, Li Y, Dong B, et al. Combination of microtubule associated protein-tau and β-tubulin III predicts chemosensitivity of paclitaxel in patients with advanced gastric cancer. Eur J Cancer. 2004;50(13):2328–35.CrossRef
27.
Zurück zum Zitat Mariani M, Zannoni GF, Sioletic S, Sieber S, Martino C, Martinelli E, et al. Gender influences the class III and V beta-tubulin ability to predict poor outcome in colorectal cancer. Clin Cancer Res. 2012;18(10):2964–75.CrossRefPubMed Mariani M, Zannoni GF, Sioletic S, Sieber S, Martino C, Martinelli E, et al. Gender influences the class III and V beta-tubulin ability to predict poor outcome in colorectal cancer. Clin Cancer Res. 2012;18(10):2964–75.CrossRefPubMed
28.
Zurück zum Zitat Kuang J, Wang YL, Xiao M, Tang Y, Chen WW, Song GL, et al. Synergistic effect of arginine-specific ADP-ribosyltransferase 1 and poly(ADP-ribose) polymerase-1 on apoptosis induced by cisplatin in CT26 cells. Oncol Rep. 2014;31(5):2335–43.PubMed Kuang J, Wang YL, Xiao M, Tang Y, Chen WW, Song GL, et al. Synergistic effect of arginine-specific ADP-ribosyltransferase 1 and poly(ADP-ribose) polymerase-1 on apoptosis induced by cisplatin in CT26 cells. Oncol Rep. 2014;31(5):2335–43.PubMed
29.
Zurück zum Zitat O’Dwyer PJ, Moyer JD, Suffness M, Harrison SD, Cysyk R, Hamilton TC, et al. Antitumor activity and biochemical effects of aphidicolin glycinate (NSC 303812) alone and in combination with cisplatin in vivo. Cancer Res. 1994;54(3):724–9.PubMed O’Dwyer PJ, Moyer JD, Suffness M, Harrison SD, Cysyk R, Hamilton TC, et al. Antitumor activity and biochemical effects of aphidicolin glycinate (NSC 303812) alone and in combination with cisplatin in vivo. Cancer Res. 1994;54(3):724–9.PubMed
30.
Zurück zum Zitat Lee CK, Park KK, Lim SS, Park JHY, Chung WY. Effects of the licorice extract against tumor growth and cisplatin-induced toxicity in a mouse xenograft model of colon cancer. Biol Pharm Bull. 2007;30(11):2191–5.CrossRefPubMed Lee CK, Park KK, Lim SS, Park JHY, Chung WY. Effects of the licorice extract against tumor growth and cisplatin-induced toxicity in a mouse xenograft model of colon cancer. Biol Pharm Bull. 2007;30(11):2191–5.CrossRefPubMed
31.
Zurück zum Zitat Carlsson G, Gullberg B, Hafström L. Estimation of liver tumor volume using different formulas—an experimental study in rats. J Cancer Res Clin Oncol. 1983;105(1):20–3.CrossRefPubMed Carlsson G, Gullberg B, Hafström L. Estimation of liver tumor volume using different formulas—an experimental study in rats. J Cancer Res Clin Oncol. 1983;105(1):20–3.CrossRefPubMed
32.
Zurück zum Zitat Vlahos CJ, Matter WF, Hui KY, Brown RF. A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J Biol Chem. 1994;269(7):5241–8.PubMed Vlahos CJ, Matter WF, Hui KY, Brown RF. A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J Biol Chem. 1994;269(7):5241–8.PubMed
33.
Zurück zum Zitat Alessi DR, Cuenda A, Cohen P, Dudley DT, Saltiel AR. PD 098059 is a specific inhibitor of the activation of mitogen-activated protein kinase kinase in vitro and in vivo. J Biol Chem. 1995;270(46):27489–94.CrossRefPubMed Alessi DR, Cuenda A, Cohen P, Dudley DT, Saltiel AR. PD 098059 is a specific inhibitor of the activation of mitogen-activated protein kinase kinase in vitro and in vivo. J Biol Chem. 1995;270(46):27489–94.CrossRefPubMed
34.
Zurück zum Zitat Soldani C, Scovassi A. Poly (ADP-ribose) polymerase-1 cleavage during apoptosis: an update. Apoptosis. 2002;7(4):321–8.CrossRefPubMed Soldani C, Scovassi A. Poly (ADP-ribose) polymerase-1 cleavage during apoptosis: an update. Apoptosis. 2002;7(4):321–8.CrossRefPubMed
35.
Zurück zum Zitat Peralta-Leal A, Rodríguez-Vargas JM, Aguilar-Quesada R, Rodríguez MI, Linares JL, de Almodóvar MR, et al. PARP inhibitors: new partners in the therapy of cancer and inflammatory diseases. Free Radic Biol Med. 2009;47:13–26.CrossRefPubMed Peralta-Leal A, Rodríguez-Vargas JM, Aguilar-Quesada R, Rodríguez MI, Linares JL, de Almodóvar MR, et al. PARP inhibitors: new partners in the therapy of cancer and inflammatory diseases. Free Radic Biol Med. 2009;47:13–26.CrossRefPubMed
36.
Zurück zum Zitat Galluzzi L, Vitale I, Abrams JM, et al. Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death. Cell Death Differ. 2012;19:107–2.CrossRefPubMed Galluzzi L, Vitale I, Abrams JM, et al. Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death. Cell Death Differ. 2012;19:107–2.CrossRefPubMed
37.
Zurück zum Zitat Langelier MF, Pascal JM. PARP-1 mechanism for coupling DNA damage detection to poly(ADP-ribose) synthesis. Curr Opin Struct Biol. 2013;23:134–43.CrossRefPubMedPubMedCentral Langelier MF, Pascal JM. PARP-1 mechanism for coupling DNA damage detection to poly(ADP-ribose) synthesis. Curr Opin Struct Biol. 2013;23:134–43.CrossRefPubMedPubMedCentral
38.
Zurück zum Zitat Kavallaris M, Kuo DY, Burkhart CA, Regl DL, Norris MD, Haber M, et al. Taxol-resistant epithelial ovarian tumors are associated with altered expression of specific beta-tubulin isotypes. J Clin Investig. 1997;100(5):1282–93.CrossRefPubMedPubMedCentral Kavallaris M, Kuo DY, Burkhart CA, Regl DL, Norris MD, Haber M, et al. Taxol-resistant epithelial ovarian tumors are associated with altered expression of specific beta-tubulin isotypes. J Clin Investig. 1997;100(5):1282–93.CrossRefPubMedPubMedCentral
39.
Zurück zum Zitat Seve P, Mackey J, Isaac S, Tredan O, Souquet PJ, Perol M, et al. Class III beta-tubulin expression in tumor cells predicts response and outcome in patients with non-small cell lung cancer receiving paclitaxel. Mol Cancer Ther. 2005;4(12):2001–7.CrossRefPubMed Seve P, Mackey J, Isaac S, Tredan O, Souquet PJ, Perol M, et al. Class III beta-tubulin expression in tumor cells predicts response and outcome in patients with non-small cell lung cancer receiving paclitaxel. Mol Cancer Ther. 2005;4(12):2001–7.CrossRefPubMed
40.
Zurück zum Zitat Ferrandina G, Zannoni GF, Martinelli E, Paglia A, Gallotta V, Mozzetti S, et al. Class III β-tubulin overexpression is a marker of poor clinical outcome in advanced ovarian cancer patients. Clin Cancer Res. 2006;12(9):2774–9.CrossRefPubMed Ferrandina G, Zannoni GF, Martinelli E, Paglia A, Gallotta V, Mozzetti S, et al. Class III β-tubulin overexpression is a marker of poor clinical outcome in advanced ovarian cancer patients. Clin Cancer Res. 2006;12(9):2774–9.CrossRefPubMed
41.
Zurück zum Zitat Mozzetti S, Ferlini C, Concolino P, Filippetti F, Raspaglio G, Prislei S, et al. Class III β-tubulin overexpression is a prominent mechanism of paclitaxel resistance in ovarian cancer patients. Clin Cancer Res. 2005;11(1):298–305.PubMed Mozzetti S, Ferlini C, Concolino P, Filippetti F, Raspaglio G, Prislei S, et al. Class III β-tubulin overexpression is a prominent mechanism of paclitaxel resistance in ovarian cancer patients. Clin Cancer Res. 2005;11(1):298–305.PubMed
42.
Zurück zum Zitat Derry WB, Wilson L, Khan IA, Luduena RF, Jordan MA. Taxol differentially modulates the dynamics of microtubules assembled from unfractionated and purified beta-tubulin isotypes. Biochemistry. 1997;36(12):3554–62.CrossRefPubMed Derry WB, Wilson L, Khan IA, Luduena RF, Jordan MA. Taxol differentially modulates the dynamics of microtubules assembled from unfractionated and purified beta-tubulin isotypes. Biochemistry. 1997;36(12):3554–62.CrossRefPubMed
43.
Zurück zum Zitat Raspaglio G, Filippetti F, Prislei S, Penci R, De Maria I, Cicchillitti L, et al. Hypoxia induces class III beta-tubulin gene expression by HIF-1α binding to its 3′ flanking region. Gene. 2008;409(1):100–8.CrossRefPubMed Raspaglio G, Filippetti F, Prislei S, Penci R, De Maria I, Cicchillitti L, et al. Hypoxia induces class III beta-tubulin gene expression by HIF-1α binding to its 3′ flanking region. Gene. 2008;409(1):100–8.CrossRefPubMed
44.
Zurück zum Zitat Powell S, Kaizer A, Koopmeiners JS, Iwamoto C, Klein M. High expression of class III β-tubulin in small cell lung carcinoma. Oncol Lett. 2014;7(2):405–10.PubMed Powell S, Kaizer A, Koopmeiners JS, Iwamoto C, Klein M. High expression of class III β-tubulin in small cell lung carcinoma. Oncol Lett. 2014;7(2):405–10.PubMed
45.
46.
Zurück zum Zitat Carre M, Carles G, Andre N, Douillard S, Ciccolini J, Briand C, et al. Involvement of microtubules and mitochondria in the antagonism of arsenic trioxide on paclitaxel-induced apoptosis. Biochem Pharmacol. 2002;63(10):1831–42.CrossRefPubMed Carre M, Carles G, Andre N, Douillard S, Ciccolini J, Briand C, et al. Involvement of microtubules and mitochondria in the antagonism of arsenic trioxide on paclitaxel-induced apoptosis. Biochem Pharmacol. 2002;63(10):1831–42.CrossRefPubMed
47.
Zurück zum Zitat Mollinedo F, Gajate C. Microtubules, microtubule-interfering agents and apoptosis. Apoptosis. 2003;8(5):413–50.CrossRefPubMed Mollinedo F, Gajate C. Microtubules, microtubule-interfering agents and apoptosis. Apoptosis. 2003;8(5):413–50.CrossRefPubMed
48.
Zurück zum Zitat Carré M, André N, Carles G, Borghi H, Brichese L, Briand C, et al. Tubulin is an inherent component of mitochondrial membranes that interacts with the voltage-dependent anion channel. J Biol Chem. 2002;277(37):33664–9.CrossRefPubMed Carré M, André N, Carles G, Borghi H, Brichese L, Briand C, et al. Tubulin is an inherent component of mitochondrial membranes that interacts with the voltage-dependent anion channel. J Biol Chem. 2002;277(37):33664–9.CrossRefPubMed
49.
Zurück zum Zitat Rostovtseva TK, Sheldon KL, Hassanzadeh E, Monge C, Saks V, Bezrukov SM, et al. Tubulin binding blocks mitochondrial voltage-dependent anion channel and regulates respiration. Proc Natl Acad Sci U S A. 2008;105(48):18746–51.CrossRefPubMedPubMedCentral Rostovtseva TK, Sheldon KL, Hassanzadeh E, Monge C, Saks V, Bezrukov SM, et al. Tubulin binding blocks mitochondrial voltage-dependent anion channel and regulates respiration. Proc Natl Acad Sci U S A. 2008;105(48):18746–51.CrossRefPubMedPubMedCentral
50.
Zurück zum Zitat Tsujimoto Y. Bcl-2 family of proteins: life-or-death switch in mitochondria. Biosci Rep. 2002;22(1):47–58.CrossRefPubMed Tsujimoto Y. Bcl-2 family of proteins: life-or-death switch in mitochondria. Biosci Rep. 2002;22(1):47–58.CrossRefPubMed
51.
Zurück zum Zitat Shimizu S, Matsuoka Y, Shinohara Y, Yoneda Y, Tsujimoto Y. Essential role of voltage-dependent anion channel in various forms of apoptosis in mammalian cells. J Cell Biol. 2001;152(2):237–50.CrossRefPubMedPubMedCentral Shimizu S, Matsuoka Y, Shinohara Y, Yoneda Y, Tsujimoto Y. Essential role of voltage-dependent anion channel in various forms of apoptosis in mammalian cells. J Cell Biol. 2001;152(2):237–50.CrossRefPubMedPubMedCentral
52.
Zurück zum Zitat Zhao Z, Gruszczynska-Biegala J, Zolkiewska A. ADP-ribosylation of integrin alpha7 modulates the binding of integrin alpha7beta1 to laminin. Biochem J. 2005;385(Pt 1):309–17.CrossRefPubMed Zhao Z, Gruszczynska-Biegala J, Zolkiewska A. ADP-ribosylation of integrin alpha7 modulates the binding of integrin alpha7beta1 to laminin. Biochem J. 2005;385(Pt 1):309–17.CrossRefPubMed
Metadaten
Titel
Tubb3 regulation by the Erk and Akt signaling pathways: a mechanism involved in the effect of arginine ADP-ribosyltransferase 1 (Art1) on apoptosis of colon carcinoma CT26 cells
verfasst von
Ming Xiao
Yi Tang
Wen-Wen Chen
Ya-Lan Wang
Lian Yang
Xian Li
Guang-Lin Song
Jing Kuang
Publikationsdatum
15.09.2015
Verlag
Springer Netherlands
Erschienen in
Tumor Biology / Ausgabe 2/2016
Print ISSN: 1010-4283
Elektronische ISSN: 1423-0380
DOI
https://doi.org/10.1007/s13277-015-4058-y

Weitere Artikel der Ausgabe 2/2016

Tumor Biology 2/2016 Zur Ausgabe

Update Onkologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.