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  Table of Contents  
Year : 2013  |  Volume : 50  |  Issue : 3  |  Page : 214-218

The stem cell self-renewal gene, Musashi 1, is highly expressed in tumor and non-tumor samples of human bladder

1 Pediatric Inherited Diseases Research Center; Division of Genetics, School of Medicine; Child Growth and Development Research Center, Isfahan University of Medical Sciences, Isfahan, Iran
2 Department of Molecular Genetics, Faculty of Biological Sciences, Tarbiat Modares University, Tehran, Iran
3 Department of Biotechnology, Faculty of Medical Sciences, Tarbiat Modares University, Tehran, Iran
4 Urology and Nephrology Research Center; Department of Urology and Renal Transplantation, Shahid Labbafinejad Medical Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran

Date of Web Publication23-Sep-2013

Correspondence Address:
P Nikpour
Pediatric Inherited Diseases Research Center; Division of Genetics, School of Medicine; Child Growth and Development Research Center, Isfahan University of Medical Sciences, Isfahan
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Source of Support: UNRC, Labbafinejad Medical Center, Conflict of Interest: None

DOI: 10.4103/0019-509X.118735

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 » Abstract 

Context: The stem cell model for cancer assumes that a key event in tumorigenesis is the deregulation of genes involved in the regulation of stem cell self-renewal. The Musashi family is an evolutionarily conserved group of neural RNA-binding proteins. In mammals, the family consists of two individual genes, Musashi 1 (MSI1) and MSI2, encoding the Musashi 1 and Musashi 2 proteins. Musashi 1 is involved in the regulation of self-renewal of stem cells. Recently, its over-expression has also been reported in a variety of human tumors. Aims: To investigate a potential expression of the stem cell self-renewal gene, Musashi 1, in human bladder cancer, we examined its gene expression in a series of tumor and non-tumor tissue samples of bladder. Materials and Methods: Relative expression of MSI1 was determined by the real-time quantitative reverse transcription polymerase chain reaction (qRT-PCR) in 70 surgical samples of bladder. Results: Using specific primers for MSI1 and TBP (as an internal control) for qRT-PCR technique, we found a relatively high expression level of MSI1 in all examined tumor and non-tumor bladder tissue specimens. However, our data did not show any correlation between the level of gene expression and tumor/non-tumor states of the samples (P>0.05). Conclusions: All together, our data demonstrated that Musashi 1 is highly and un-differentially expressed in both examined tumoral and apparently normal bladder tissues.

Keywords: Bladder cancer, gene expression, Musashi1, self-renewal

How to cite this article:
Nikpour P, Mowla S J, Forouzandeh-Moghaddam M, Ziaee S A. The stem cell self-renewal gene, Musashi 1, is highly expressed in tumor and non-tumor samples of human bladder. Indian J Cancer 2013;50:214-8

How to cite this URL:
Nikpour P, Mowla S J, Forouzandeh-Moghaddam M, Ziaee S A. The stem cell self-renewal gene, Musashi 1, is highly expressed in tumor and non-tumor samples of human bladder. Indian J Cancer [serial online] 2013 [cited 2020 Jul 4];50:214-8. Available from:

 » Introduction Top

Recent studies have demonstrated many similarities between basic mechanisms mediating stem and cancer cell self-renewal. [1],[2] Increasing evidence shows that many pathways, such as the Notch, Sonic hedgehog (Shh) and Wnt signaling pathways, which are routinely linked to cancer, may also regulate normal stem cell development. [1] The stem cell model for cancer assumes that a key event in tumorigenesis is the disruption of genes involved in the regulation of stem cell self-renewal, [2] so it is not surprising that cancer cells employ the same machinery for cell division that is normally being used in self-renewal of stem cells. [1] Therefore, the study of stem cell self-renewal genes has a great potential to expand our understanding of carcinogenesis and to develop novel strategies for preventing, diagnosing and treating cancers. [3]

The Musashi family is an evolutionarily conserved group of neural RNA-binding proteins. [4],[5] In mammals, the family consists of two individual genes, Musashi 1 (MSI1) and MSI2, [6],[7] encoding the Musashi1 and Musashi2 proteins, which are highly similar at the amino acid positions critical for their RNA-binding activity. [7] Musashi1 is mainly expressed in central nervous system (CNS) stem cells and neural progenitor cells during development, [5] whereas Musashi2 is more uniformly expressed also in tissues outside the CNS. [7]

Musashi1 is involved in the regulation of self-renewal of neural stem cells. [5],[8] However, its expression has also been identified outside the nervous system, specifically, in the predicted stem cell enriched regions of murine and human intestinal crypts and stomach [9],[10],[11] and in epithelial progenitors in gastric mucosa, gut, mammary glands, epidermis and hair follicles. [5],[11],[12],[13] Musashi1 expression has also been reported in a variety of tumor cells, including colon cancer, [14] bladder carcinoma, [15] pulmonary carcinomas, [16] breast cancer, [17] medulloblastoma, [18] cervical carcinoma, [19] endometrial carcinoma, [20] retinoblastoma, [21] hepatoma cell lines, [22] and glioblastoma. [23] The function of Musashi1 in tumor cells is not well understood. Presumably, it may play a role in the maintenance of the self-renewal capacity of tumor (stem) cells by enhancing Notch pathway activity and preventing p21 CIP1 -induced cell cycle arrest. [15],[24] Over-expression of Musashi2 has been also shown in murine myeloid leukemia, [25] human myeloid leukemia cells, [26] human chronic myelogenous leukemia (CML) and acute myelogenous leukemia (AML). [27],[28]

To investigate a potential involvement of Musashi gene family member, MSI1, in human bladder cancer, we examined its expression in bladder specimens with and without malignant lesions.

 » Materials and Methods Top

The bladder tumor and non-tumor tissue samples were obtained from patients who had referred to Shahid Labbafinejad Medical Center. Briefly, the tissues were immediately snap-frozen in liquid nitrogen and categorized into two groups: tumor specimens prepared by transurethral resection from patients with transitional cell carcinoma of the bladder [Table 1] and tumor-free tissues taken from the margin of tumors (cystoscopically normal appearance). A total of seventy bladder tissue samples were examined for gene expression, consisting of 32 non-tumor and 38 tumor specimens. Histopathological parameters were evaluated according to the grading and TNM system for stage classification of the World Health Organization. The experimental design conformed to the Code of Ethics of the World Medical Association (Declaration of Helsinki) and was approved by the Ethics Committees of Tarbiat Modares University and the Urology and Nephrology Research Center of Shahid Beheshti University. The patients' written informed consents were obtained prior to participation. Transitional carcinoma cell line 5637, obtained from Pasteur Institute (Tehran, Iran), cultured and used in all assays as a positive control. It was cultured in DMEM (Gibco Life Technologies, Karlsruhe, Germany), supplemented with 10% fetal calf serum and 100 mg/ml penicillin/streptomycin as described elsewhere. [15] RNX plus solution (Cinnagen, Iran) was used for extraction of total RNA from powdered tissues and sub-confluent 5637 cell culture according to the manufacturer's instructions. The quality of RNA was evaluated by gel electrophoresis, and the concentration of RNA was measured by optical density at 260 nm. cDNA synthesis was performed using RevertAid MMuLV Reverse Transcriptase (Fermentas, Vilnius, Lithuania) with oligo-dT primers. Real-time quantitative reverse transcription polymerase chain reaction (qRT-PCR) assays were performed using the Rotor-gene 3000 (Qiagen, Germany). Real-time qRT-PCR for Musashi1 and TBP mRNAs was performed using specific primers [Table 2] [15] with the QuantiTect SYBR Green PCR kit (Qiagen, Hilden, Germany). The PCR for the genes included an initial denaturation step at 95°C for 10 min, followed by 40 amplification cycles consisting of denaturation at 95°C for 10 s, 55°C for 20 s and an extension at 72°C for 20 s. The identity of PCR products was further confirmed on a 2% agarose gel, stained with ethidium bromide, and visualized under ultraviolet light. Relative gene expression was calculated using the standard curve method. All measurements were performed in at least triplicates and the results were analyzed by performing Students t-test. The SPSS software, version 15.0, was used for statistical analyses and the P value less than 0.05 was considered as statistically significant.
Table 1: A brief description of patients with bladder cancer

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Table 2: Sequences of the designed PCR primers and the expected sizes of the amplified bands[15]

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 » Results Top

Prior to the quantitative analysis, optimization procedures were carried out for both ordinary and real-time RT-PCR reactions on 5637 cell line, using specific primers for human MSI1 and TBP genes. Electrophoresis of the PCR products on agarose gels demonstrated single bands with the expected sizes for the amplified MSI1 (117 bp) and TBP (128 bp) segments [Figure 1]a. Analysis of gene expression using real-time PCR showed a unique melting curve without primer dimers for each of the examined genes [Figure 1]b for MSI1], which was further confirmed by agarose gel separation and staining. To optimize the quantification technique, a cDNA synthesized from 5637 cell line was used in serial dilution and PCR efficiency near to 100% was obtained [Figure 1]c. After optimization of the real-time PCR, expression of MSI1 and TBP genes was analyzed using real-time qRT-PCR in 38 tumor and 32 non-tumor tissues of bladder. Relative expression of the target gene was calculated by dividing its expression amounts to that of the TBP gene. The results of real-time qRT-PCR experiments demonstrated that while the relative expression of Musashi 1 gene was high in some examined tumor tissues, its expression was low in some others. Interestingly, we also observed a similar gene expression profile in non-tumor bladder tissue samples. [Figure 2] shows the relative mean expression of MSI1 gene in tumor and non-tumor bladder tissue samples. As expected from the results, statistical analyses failed to show any significant difference between the Musashi gene expression of tumor specimens and that of the non-tumor ones.
Figure 1: Optimization of real-time qRT-PCR (a) RT-PCR analysis of MSI1 and TBP (as an internal control) gene expressions in the 5637 carcinoma cell line (as a positive control) (b) A unique melting curve without primer dimers showing specific amplification of MSI1 on real-time PCR (c) Amplification curves of a cDNA dilution series for determination of amplification efficiency of MSI1

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Figure 2: Relative expression of MSI1 in tumor and non-tumor tissue samples of bladder chart comparing the relative gene expression of MSI1 to TBP as determined by real-time qRT-PCR. Values shown represent the mean ± STD.

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 » Discussion Top

There is accumulating evidence suggesting the role of RNA-binding proteins in cell proliferation, apoptosis and invasiveness, by regulating the translation and mRNA stability of their target genes. [29],[30],[31],[32] Several RNA-binding proteins involved in tumorigenesis are over-expressed during the various stages of cancer. [33],[34],[35],[36] The Musashi family is an evolutionarily conserved group of neural RNA-binding proteins having representatives in C. elegans, Drosophila melanogaster, Halocynthia roretzi, Xenopus laevis, mouse and human. [6],[7],[37],[38],[39],[40],[41] In mammals, the Musashi family is important for cell fate determination in a broader sense, playing roles in maintenance of the stem-cell state, differentiation and tumorigenesis. [4],[5] In the present study, to clarify whether the Musashi gene family member, MSI1, is expressed in the bladder cancer, we examined its expression profile in a series of invasive urothelial carcinoma and benign tissue samples. By using the real-time qRT-PCR, we observed MSI1 expression in both tumor and non-tumor bladder tissue samples but with no substantial difference between the two compared groups as a whole. We [15] have previously observed MSI1 over-expression in some urothelial carcinoma cell lines, whereas other bladder cancer cell lines or normal urothelial cell cultures showed low or no expression of MSI1. MSI1 up-regulation has also been reported in tumors of APC min/+ mice. [11] MSI1 is also up-regulated in brain tumors, including medulloblastoma and gliomas. [42],[43] In another study, Sureban et al. [44] reported that expression of MSI1 mRNA is increased in human colon cancer tumors, compared to its paired uninvolved tissue. Increased expression of Musashi1 has been also reported in other cancer types. [14],[17],[19],[20],[21] We also showed recently that MSI1 is undifferentially expressed in tumoral and non-tumoral gastric cancer specimens. [45] Overall, these results demonstrate that MSI1 is an important growth regulator in various tumors. Our finding that MSI1 is expressed in non-tumor tissues, despite its lack of expression in normal urothelial cells in vitro, [15] suggests that cells other than urothelial ones might be the source of this relatively high expression. Coupling mRNA expression assays on micro-dissected tissue samples with histological staining of its protein may unravel the precise localization and expression pattern of MSI1 in normal and tumor bladder tissues. Finding novel molecular markers with differential expression in tumor and normal cells has a pivotal role in the diagnosis and treatment of cancer. The Musashi family of proteins, as regulators of stem cell self-renewal and cancer proliferation, has the potential to be utilized in the future as new tumor markers in a variety of cancer types. The present data revealed that MSI1 gene is highly and un-differentially expressed in both human non-tumor and tumor bladder tissues. At present, the mechanism governing Musashi gene expression in the adult human bladder is still mainly unknown. Functional studies are needed to clarify the characteristics of MSI1 positive cells and the role of Musashi proteins in the regulation of normal epithelial cell differentiation and metaplastic changes in the human bladder cells.

 » Acknowledgments Top

We are grateful to Ms. Nasim Hatefi for her assistance in collecting tissue samples. This work was supported, in part, by a research grant from the UNRC, Labbafinejad Medical Center.

 » References Top

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  [Table 1], [Table 2]

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