Skip to main content
Erschienen in: Pathology & Oncology Research 2/2014

01.04.2014 | Research

Clinicopathological Sex- Related Relevance of Musashi1 mRNA Expression in Esophageal Squamous Cell Carcinoma Patients

verfasst von: Meysam Moghbeli, Mohammad Mahdi Forghanifard, Azadeh Aarabi, Akram Mansourian, Mohammad Reza Abbaszadegan

Erschienen in: Pathology & Oncology Research | Ausgabe 2/2014

Einloggen, um Zugang zu erhalten

Abstract

The cancer stem cell theory is considered as the spotlight of cancer biology, in which a subpopulation of tumor cells show unlimited proliferative and self renewal capacities. Post-transcriptional regulation is involved in different cellular functions such as cell differentiation and proliferation which results in cellular diversity. Musashi1 (Msi1) is one of the most important RNA-binding proteins (RBPs) which are involved in translational inhibition. Although, Msi1 targets are largely unknown, p21WAF-1, a cell cycle regulator, and Numb, inhibitor of notch signaling pathway, are well-known factors which are suppressed by the Msi1 in normal and cancer stem cells. Msi1 expression in tumor tissues from 53 ESCC patients was compared to normal tissues using real-time polymerase chain reaction (PCR). Msi1 was significantely overexpressed in 41.5 % of tumor samples and we observed a significant correlation between Msi1 expression and sex, in which the males had shown a higher level of Msi1 expression in comparison with the females (2.00 Vs 0.78 fold changes, p = 0.05). In this study, we assessed whether Msi1 is expressed in ESCC samples suggesting this protein as a novel cancer stem cell marker which requires further studies.
Literatur
1.
Zurück zum Zitat Gholamin M, Moaven O, Memar B, Farshchian M, Naseh H, Malekzadeh R, Sotoudeh M, Rajabi-Mashhadi MT, Forghani MN, Farrokhi F, Abbaszadegan MR (2009) Overexpression and interactions of interleukin-10, transforming growth factor beta, and vascular endothelial growth factor in esophageal squamous cell carcinoma. World J Surg 33(7):1439–1445PubMedCrossRef Gholamin M, Moaven O, Memar B, Farshchian M, Naseh H, Malekzadeh R, Sotoudeh M, Rajabi-Mashhadi MT, Forghani MN, Farrokhi F, Abbaszadegan MR (2009) Overexpression and interactions of interleukin-10, transforming growth factor beta, and vascular endothelial growth factor in esophageal squamous cell carcinoma. World J Surg 33(7):1439–1445PubMedCrossRef
2.
Zurück zum Zitat Ben-Porath I, Thomson MW, Carey VJ, Ge R, Bell GW, Regev A, Weinberg RA (2008) An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat Genet 40(5):499–507PubMedCentralPubMedCrossRef Ben-Porath I, Thomson MW, Carey VJ, Ge R, Bell GW, Regev A, Weinberg RA (2008) An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat Genet 40(5):499–507PubMedCentralPubMedCrossRef
3.
Zurück zum Zitat Pardal R, Clarke MF, Morrison SJ (2003) Applying the principles of stem-cell biology to cancer. Nat Rev Cancer 3(12):895–902PubMedCrossRef Pardal R, Clarke MF, Morrison SJ (2003) Applying the principles of stem-cell biology to cancer. Nat Rev Cancer 3(12):895–902PubMedCrossRef
4.
Zurück zum Zitat Schwanhausser B, Busse D, Li N, Dittmar G, Schuchhardt J, Wolf J, Chen W, Selbach M (2011) Global quantification of mammalian gene expression control. Nature 473(7347):337–342 Schwanhausser B, Busse D, Li N, Dittmar G, Schuchhardt J, Wolf J, Chen W, Selbach M (2011) Global quantification of mammalian gene expression control. Nature 473(7347):337–342
5.
Zurück zum Zitat Jackson RJ, Hellen CU, Pestova TV (2010) The mechanism of eukaryotic translation initiation and principles of its regulation. Nat Rev Mol Cell Biol 11(2):113–127 Jackson RJ, Hellen CU, Pestova TV (2010) The mechanism of eukaryotic translation initiation and principles of its regulation. Nat Rev Mol Cell Biol 11(2):113–127
6.
7.
Zurück zum Zitat Grzmil M, Hemmings BA (2012) Translation regulation as a therapeutic target in cancer. Cancer Res 72(16):3891–3900 Grzmil M, Hemmings BA (2012) Translation regulation as a therapeutic target in cancer. Cancer Res 72(16):3891–3900
8.
Zurück zum Zitat Battelli C, Nikopoulos GN, Mitchell JG, Verdi JM (2006) The RNA-binding protein Musashi-1 regulates neural development through the translational repression of p21WAF-1. Mol Cell Neurosci 31(1):85–96PubMedCrossRef Battelli C, Nikopoulos GN, Mitchell JG, Verdi JM (2006) The RNA-binding protein Musashi-1 regulates neural development through the translational repression of p21WAF-1. Mol Cell Neurosci 31(1):85–96PubMedCrossRef
9.
Zurück zum Zitat Imai T, Tokunaga A, Yoshida T, Hashimoto M, Mikoshiba K, Weinmaster G, Nakafuku M, Okano H (2001) The neural RNA-binding protein Musashi1 translationally regulates mammalian numb gene expression by interacting with its mRNA. Mol Cell Biol 21(12):3888–3900PubMedCentralPubMedCrossRef Imai T, Tokunaga A, Yoshida T, Hashimoto M, Mikoshiba K, Weinmaster G, Nakafuku M, Okano H (2001) The neural RNA-binding protein Musashi1 translationally regulates mammalian numb gene expression by interacting with its mRNA. Mol Cell Biol 21(12):3888–3900PubMedCentralPubMedCrossRef
10.
Zurück zum Zitat Kawahara H, Imai T, Imataka H, Tsujimoto M, Matsumoto K, Okano H (2008) Neural RNA-binding protein Musashi1 inhibits translation initiation by competing with eIF4G for PABP. J Cell Biol 181(4):639–653PubMedCentralPubMedCrossRef Kawahara H, Imai T, Imataka H, Tsujimoto M, Matsumoto K, Okano H (2008) Neural RNA-binding protein Musashi1 inhibits translation initiation by competing with eIF4G for PABP. J Cell Biol 181(4):639–653PubMedCentralPubMedCrossRef
11.
Zurück zum Zitat Okano H, Kawahara H, Toriya M, Nakao K, Shibata S, Imai T (2005) Function of RNA-binding protein Musashi-1 in stem cells. Exp Cell Res 306(2):349–356PubMedCrossRef Okano H, Kawahara H, Toriya M, Nakao K, Shibata S, Imai T (2005) Function of RNA-binding protein Musashi-1 in stem cells. Exp Cell Res 306(2):349–356PubMedCrossRef
12.
Zurück zum Zitat Guo M, Jan LY, Jan YN (1996) Control of daughter cell fates during asymmetric division: interaction of Numb and Notch. Neuron 17(1):27–41PubMedCrossRef Guo M, Jan LY, Jan YN (1996) Control of daughter cell fates during asymmetric division: interaction of Numb and Notch. Neuron 17(1):27–41PubMedCrossRef
13.
Zurück zum Zitat Di Marcotullio L, Ferretti E, Greco A, De Smaele E, Po A, Sico MA, Alimandi M, Giannini G, Maroder M, Screpanti I, Gulino A (2006) Numb is a suppressor of Hedgehog signalling and targets Gli1 for Itch-dependent ubiquitination. Nat Cell Biol 8(12):1415–1423PubMedCrossRef Di Marcotullio L, Ferretti E, Greco A, De Smaele E, Po A, Sico MA, Alimandi M, Giannini G, Maroder M, Screpanti I, Gulino A (2006) Numb is a suppressor of Hedgehog signalling and targets Gli1 for Itch-dependent ubiquitination. Nat Cell Biol 8(12):1415–1423PubMedCrossRef
14.
Zurück zum Zitat McGill MA, McGlade CJ (2003) Mammalian numb proteins promote Notch1 receptor ubiquitination and degradation of the Notch1 intracellular domain. J Biol Chem 278(25):23196–23203PubMedCrossRef McGill MA, McGlade CJ (2003) Mammalian numb proteins promote Notch1 receptor ubiquitination and degradation of the Notch1 intracellular domain. J Biol Chem 278(25):23196–23203PubMedCrossRef
15.
Zurück zum Zitat Wakamatsu Y, Maynard TM, Jones SU, Weston JA (1999) NUMB localizes in the basal cortex of mitotic avian neuroepithelial cells and modulates neuronal differentiation by binding to NOTCH-1. Neuron 23(1):71–81PubMedCrossRef Wakamatsu Y, Maynard TM, Jones SU, Weston JA (1999) NUMB localizes in the basal cortex of mitotic avian neuroepithelial cells and modulates neuronal differentiation by binding to NOTCH-1. Neuron 23(1):71–81PubMedCrossRef
16.
17.
Zurück zum Zitat Wang XY, Yin Y, Yuan H, Sakamaki T, Okano H, Glazer RI (2008) Musashi1 modulates mammary progenitor cell expansion through proliferin-mediated activation of the Wnt and Notch pathways. Mol Cell Biol 28(11):3589–3599PubMedCentralPubMedCrossRef Wang XY, Yin Y, Yuan H, Sakamaki T, Okano H, Glazer RI (2008) Musashi1 modulates mammary progenitor cell expansion through proliferin-mediated activation of the Wnt and Notch pathways. Mol Cell Biol 28(11):3589–3599PubMedCentralPubMedCrossRef
18.
Zurück zum Zitat Devgan V, Mammucari C, Millar SE, Brisken C, Dotto GP (2005) p21WAF1/Cip1 is a negative transcriptional regulator of Wnt4 expression downstream of Notch1 activation. Genes Dev 19(12):1485–1495PubMedCentralPubMedCrossRef Devgan V, Mammucari C, Millar SE, Brisken C, Dotto GP (2005) p21WAF1/Cip1 is a negative transcriptional regulator of Wnt4 expression downstream of Notch1 activation. Genes Dev 19(12):1485–1495PubMedCentralPubMedCrossRef
19.
Zurück zum Zitat Li L, Yuan H, Weaver CD, Mao J, Farr GH 3rd, Sussman DJ, Jonkers J, Kimelman D, Wu D (1999) Axin and Frat1 interact with dvl and GSK, bridging Dvl to GSK in Wnt-mediated regulation of LEF-1. Embo J 18(15):4233–4240PubMedCentralPubMedCrossRef Li L, Yuan H, Weaver CD, Mao J, Farr GH 3rd, Sussman DJ, Jonkers J, Kimelman D, Wu D (1999) Axin and Frat1 interact with dvl and GSK, bridging Dvl to GSK in Wnt-mediated regulation of LEF-1. Embo J 18(15):4233–4240PubMedCentralPubMedCrossRef
20.
Zurück zum Zitat Toda M, Iizuka Y, Yu W, Imai T, Ikeda E, Yoshida K, Kawase T, Kawakami Y, Okano H, Uyemura K (2001) Expression of the neural RNA-binding protein Musashi1 in human gliomas. Glia 34(1):1–7PubMedCrossRef Toda M, Iizuka Y, Yu W, Imai T, Ikeda E, Yoshida K, Kawase T, Kawakami Y, Okano H, Uyemura K (2001) Expression of the neural RNA-binding protein Musashi1 in human gliomas. Glia 34(1):1–7PubMedCrossRef
21.
Zurück zum Zitat Gotte M, Wolf M, Staebler A, Buchweitz O, Kelsch R, Schuring AN, Kiesel L (2008) Increased expression of the adult stem cell marker Musashi-1 in endometriosis and endometrial carcinoma. J Pathol 215(3):317–329PubMedCrossRef Gotte M, Wolf M, Staebler A, Buchweitz O, Kelsch R, Schuring AN, Kiesel L (2008) Increased expression of the adult stem cell marker Musashi-1 in endometriosis and endometrial carcinoma. J Pathol 215(3):317–329PubMedCrossRef
22.
Zurück zum Zitat Shu HJ, Saito T, Watanabe H, Ito JI, Takeda H, Okano H, Kawata S (2002) Expression of the Musashi1 gene encoding the RNA-binding protein in human hepatoma cell lines. Biochem Biophys Res Commun 293(1):150–154PubMedCrossRef Shu HJ, Saito T, Watanabe H, Ito JI, Takeda H, Okano H, Kawata S (2002) Expression of the Musashi1 gene encoding the RNA-binding protein in human hepatoma cell lines. Biochem Biophys Res Commun 293(1):150–154PubMedCrossRef
23.
Zurück zum Zitat Schulenburg A, Cech P, Herbacek I, Marian B, Wrba F, Valent P, Ulrich-Pur H (2007) CD44-positive colorectal adenoma cells express the potential stem cell markers musashi antigen (msi1) and ephrin B2 receptor (EphB2). J Pathol 213(2):152–160PubMedCrossRef Schulenburg A, Cech P, Herbacek I, Marian B, Wrba F, Valent P, Ulrich-Pur H (2007) CD44-positive colorectal adenoma cells express the potential stem cell markers musashi antigen (msi1) and ephrin B2 receptor (EphB2). J Pathol 213(2):152–160PubMedCrossRef
24.
Zurück zum Zitat Forghanifard MM, Moaven O, Farshchian M, Montazer M, Raeisossadati R, Abdollahi A, Moghbeli M, Nejadsattari T, Parivar K, Abbaszadegan MR (2012) Expression analysis elucidates the roles of MAML1 and Twist1 in esophageal squamous cell carcinoma aggressiveness and metastasis. Ann Surg Oncol 19(3):743–749 Forghanifard MM, Moaven O, Farshchian M, Montazer M, Raeisossadati R, Abdollahi A, Moghbeli M, Nejadsattari T, Parivar K, Abbaszadegan MR (2012) Expression analysis elucidates the roles of MAML1 and Twist1 in esophageal squamous cell carcinoma aggressiveness and metastasis. Ann Surg Oncol 19(3):743–749
25.
Zurück zum Zitat Kaneko Y, Sakakibara S, Imai T, Suzuki A, Nakamura Y, Sawamoto K, Ogawa Y, Toyama Y, Miyata T, Okano H (2000) Musashi1: an evolutionally conserved marker for CNS progenitor cells including neural stem cells. Dev Neurosci 22(1–2):139–153PubMedCrossRef Kaneko Y, Sakakibara S, Imai T, Suzuki A, Nakamura Y, Sawamoto K, Ogawa Y, Toyama Y, Miyata T, Okano H (2000) Musashi1: an evolutionally conserved marker for CNS progenitor cells including neural stem cells. Dev Neurosci 22(1–2):139–153PubMedCrossRef
26.
Zurück zum Zitat Siddall NA, McLaughlin EA, Marriner NL, Hime GR (2006) The RNA-binding protein Musashi is required intrinsically to maintain stem cell identity. Proc Natl Acad Sci U S A 103(22):8402–8407PubMedCentralPubMedCrossRef Siddall NA, McLaughlin EA, Marriner NL, Hime GR (2006) The RNA-binding protein Musashi is required intrinsically to maintain stem cell identity. Proc Natl Acad Sci U S A 103(22):8402–8407PubMedCentralPubMedCrossRef
27.
Zurück zum Zitat Hemmati HD, Nakano I, Lazareff JA, Masterman-Smith M, Geschwind DH, Bronner-Fraser M, Kornblum HI (2003) Cancerous stem cells can arise from pediatric brain tumors. Proc Natl Acad Sci U S A 100(25):15178–15183PubMedCentralPubMedCrossRef Hemmati HD, Nakano I, Lazareff JA, Masterman-Smith M, Geschwind DH, Bronner-Fraser M, Kornblum HI (2003) Cancerous stem cells can arise from pediatric brain tumors. Proc Natl Acad Sci U S A 100(25):15178–15183PubMedCentralPubMedCrossRef
28.
Zurück zum Zitat Yokota N, Mainprize TG, Taylor MD, Kohata T, Loreto M, Ueda S, Dura W, Grajkowska W, Kuo JS, Rutka JT (2004) Identification of differentially expressed and developmentally regulated genes in medulloblastoma using suppression subtraction hybridization. Oncogene 23(19):3444–3453PubMedCrossRef Yokota N, Mainprize TG, Taylor MD, Kohata T, Loreto M, Ueda S, Dura W, Grajkowska W, Kuo JS, Rutka JT (2004) Identification of differentially expressed and developmentally regulated genes in medulloblastoma using suppression subtraction hybridization. Oncogene 23(19):3444–3453PubMedCrossRef
29.
Zurück zum Zitat Clement V, Sanchez P, de Tribolet N, Radovanovic I, Ruiz i Altaba A (2007) HEDGEHOG-GLI1 signaling regulates human glioma growth, cancer stem cell self-renewal, and tumorigenicity. Curr Biol 17(2):165–172PubMedCentralPubMedCrossRef Clement V, Sanchez P, de Tribolet N, Radovanovic I, Ruiz i Altaba A (2007) HEDGEHOG-GLI1 signaling regulates human glioma growth, cancer stem cell self-renewal, and tumorigenicity. Curr Biol 17(2):165–172PubMedCentralPubMedCrossRef
30.
Zurück zum Zitat Gonzalez F, Barragan Monasterio M, Tiscornia G, Montserrat Pulido N, Vassena R, Batlle Morera L, Rodriguez Piza I, Izpisua Belmonte JC (2009) Generation of mouse-induced pluripotent stem cells by transient expression of a single nonviral polycistronic vector. Proc Natl Acad Sci U S A 106(22):8918–8922PubMedCentralPubMedCrossRef Gonzalez F, Barragan Monasterio M, Tiscornia G, Montserrat Pulido N, Vassena R, Batlle Morera L, Rodriguez Piza I, Izpisua Belmonte JC (2009) Generation of mouse-induced pluripotent stem cells by transient expression of a single nonviral polycistronic vector. Proc Natl Acad Sci U S A 106(22):8918–8922PubMedCentralPubMedCrossRef
31.
Zurück zum Zitat Stadtfeld M, Maherali N, Borkent M, Hochedlinger K (2010) A reprogrammable mouse strain from gene-targeted embryonic stem cells. Nat Methods 7(1):53–55 Stadtfeld M, Maherali N, Borkent M, Hochedlinger K (2010) A reprogrammable mouse strain from gene-targeted embryonic stem cells. Nat Methods 7(1):53–55
32.
Zurück zum Zitat Yu J, Hu K, Smuga-Otto K, Tian S, Stewart R, Slukvin II, Thomson JA (2009) Human induced pluripotent stem cells free of vector and transgene sequences. Science 324(5928):797–801PubMedCentralPubMedCrossRef Yu J, Hu K, Smuga-Otto K, Tian S, Stewart R, Slukvin II, Thomson JA (2009) Human induced pluripotent stem cells free of vector and transgene sequences. Science 324(5928):797–801PubMedCentralPubMedCrossRef
33.
Zurück zum Zitat Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S, Nie J, Jonsdottir GA, Ruotti V, Stewart R, Slukvin II, Thomson JA (2007) Induced pluripotent stem cell lines derived from human somatic cells. Science 318(5858):1917–1920PubMedCrossRef Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S, Nie J, Jonsdottir GA, Ruotti V, Stewart R, Slukvin II, Thomson JA (2007) Induced pluripotent stem cell lines derived from human somatic cells. Science 318(5858):1917–1920PubMedCrossRef
34.
Zurück zum Zitat Potten CS, Booth C, Tudor GL, Booth D, Brady G, Hurley P, Ashton G, Clarke R, Sakakibara S, Okano H (2003) Identification of a putative intestinal stem cell and early lineage marker; musashi-1. Differentiation 71(1):28–41PubMedCrossRef Potten CS, Booth C, Tudor GL, Booth D, Brady G, Hurley P, Ashton G, Clarke R, Sakakibara S, Okano H (2003) Identification of a putative intestinal stem cell and early lineage marker; musashi-1. Differentiation 71(1):28–41PubMedCrossRef
35.
Zurück zum Zitat Bobryshev YV, Freeman AK, Botelho NK, Tran D, Levert-Mignon AJ, Lord RV (2010) Expression of the putative stem cell marker Musashi-1 in Barrett’s esophagus and esophageal adenocarcinoma. Dis Esophagus 23(7):580–589 Bobryshev YV, Freeman AK, Botelho NK, Tran D, Levert-Mignon AJ, Lord RV (2010) Expression of the putative stem cell marker Musashi-1 in Barrett’s esophagus and esophageal adenocarcinoma. Dis Esophagus 23(7):580–589
36.
Zurück zum Zitat Nikpour P, Baygi ME, Steinhoff C, Hader C, Luca AC, Mowla SJ, Schulz WA (2011) The RNA binding protein Musashi1 regulates apoptosis, gene expression and stress granule formation in urothelial carcinoma cells. J Cell Mol Med 15(5):1210–1224 Nikpour P, Baygi ME, Steinhoff C, Hader C, Luca AC, Mowla SJ, Schulz WA (2011) The RNA binding protein Musashi1 regulates apoptosis, gene expression and stress granule formation in urothelial carcinoma cells. J Cell Mol Med 15(5):1210–1224
37.
Zurück zum Zitat Nikpour P, Emadi-Baygi M, Mohhamad-Hashem F, Maracy MR, Haghjooy-Javanmard S (2013) MSI1 overexpression in diffuse type of gastric cancer. Pathol Res Pract 209(1):10–13 Nikpour P, Emadi-Baygi M, Mohhamad-Hashem F, Maracy MR, Haghjooy-Javanmard S (2013) MSI1 overexpression in diffuse type of gastric cancer. Pathol Res Pract 209(1):10–13
38.
Zurück zum Zitat Todaro M, Francipane MG, Medema JP, Stassi G (2010) Colon cancer stem cells: promise of targeted therapy. Gastroenterology 138(6):2151–2162 Todaro M, Francipane MG, Medema JP, Stassi G (2010) Colon cancer stem cells: promise of targeted therapy. Gastroenterology 138(6):2151–2162
Metadaten
Titel
Clinicopathological Sex- Related Relevance of Musashi1 mRNA Expression in Esophageal Squamous Cell Carcinoma Patients
verfasst von
Meysam Moghbeli
Mohammad Mahdi Forghanifard
Azadeh Aarabi
Akram Mansourian
Mohammad Reza Abbaszadegan
Publikationsdatum
01.04.2014
Verlag
Springer Netherlands
Erschienen in
Pathology & Oncology Research / Ausgabe 2/2014
Print ISSN: 1219-4956
Elektronische ISSN: 1532-2807
DOI
https://doi.org/10.1007/s12253-013-9712-3

Weitere Artikel der Ausgabe 2/2014

Pathology & Oncology Research 2/2014 Zur Ausgabe

Update Onkologie

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