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Published in: Pathology & Oncology Research 2/2014

01-04-2014 | Research

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

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

Published in: Pathology & Oncology Research | Issue 2/2014

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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.
Literature
1.
go back to reference 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.
go back to reference 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.
go back to reference 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.
go back to reference 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.
go back to reference 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.
go back to reference 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.
go back to reference 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.
go back to reference 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.
go back to reference 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.
go back to reference 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.
go back to reference 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.
go back to reference 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.
go back to reference 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.
go back to reference 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
17.
go back to reference 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.
go back to reference 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.
go back to reference 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.
go back to reference 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.
go back to reference 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.
go back to reference 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.
go back to reference 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.
go back to reference 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.
go back to reference 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.
go back to reference 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.
go back to reference 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.
go back to reference 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.
go back to reference 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.
go back to reference 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.
go back to reference 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.
go back to reference 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.
go back to reference 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.
go back to reference 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.
go back to reference 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.
go back to reference 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.
go back to reference 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.
go back to reference 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
Metadata
Title
Clinicopathological Sex- Related Relevance of Musashi1 mRNA Expression in Esophageal Squamous Cell Carcinoma Patients
Authors
Meysam Moghbeli
Mohammad Mahdi Forghanifard
Azadeh Aarabi
Akram Mansourian
Mohammad Reza Abbaszadegan
Publication date
01-04-2014
Publisher
Springer Netherlands
Published in
Pathology & Oncology Research / Issue 2/2014
Print ISSN: 1219-4956
Electronic ISSN: 1532-2807
DOI
https://doi.org/10.1007/s12253-013-9712-3

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