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Contents
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[1]J. Ferlay, E. Steliarova-Foucher, J. Lortet-Tieulent, S. Rosso, J. W. Coebergh, H. Comber, D. Forman and F. Bray: Cancer incidence and mortality patterns in Europe: estimates for 40 countries in 2012. Eur J Cancer, 49(6), 1374-403 (2013)
[2]P. Boyle and J. Ferlay: Cancer incidence and mortality in Europe, 2004. Ann Oncol, 16(3), 481-8 (2005)
[3]H. Lue, R. Kleemann, T. Calandra, T. Roger and J. Bernhagen: Macrophage migration inhibitory factor (MIF): mechanisms of action and role in disease. Microbes Infect, 4(4), 449-60 (2002)
[4]X. X. He, M. Chen and C. Y. Liu: The effects of ISO-1 on the proliferation of the colorectal cell lines. J of Hubei University For Nationalities (Medical Edition), 25, 1-4 (2008)
[5]M. L. Toh, D. Aeberli, D. Lacey, Y. Yang, L. L. Santos, M. Clarkson, L. Sharma, C. Clyne and E. F. Morand: Regulation of IL-1 and TNF receptor expression and function by endogenous macrophage migration inhibitory factor. J Immunol, 177(7), 4818-25 (2006)
[6]X. Y. LI and X. X. HE: Impact of macrophage migration inhibitory factor on cell migration of colorectal carcinoma cell lines in vitro. J of Modern Clinical Medical Bioengineering, 12, 402-404 (2006)
[7]X. X. He, J. Yang, Y. W. Ding, W. Liu, Q. Y. Shen and H. H. Xia: Increased epithelial and serum expression of macrophage migration inhibitory factor (MIF) in gastric cancer: potential role of MIF in gastric carcinogenesis. Gut, 55(6), 797-802 (2006)
[8]X. X. He, K. Chen, J. Yang, X. Y. Li, H. Y. Gan, C. Y. Liu, T. R. Coleman and Y. Al-Abed: Macrophage migration inhibitory factor promotes colorectal cancer. Mol Med, 15(1-2), 1-10 (2009)
[9]J. D. Swant, B. E. Rendon, M. Symons and R. A. Mitchell: Rho GTPase-dependent signaling is required for macrophage migration inhibitory factor-mediated expression of cyclin D1. J Biol Chem, 280(24), 23066-72 (2005)
[10]T. Hagemann, S. C. Robinson, R. G. Thompson, K. Charles, H. Kulbe and F. R. Balkwill: Ovarian cancer cell-derived migration inhibitory factor enhances tumor growth, progression, and angiogenesis. Mol Cancer Ther, 6(7), 1993-2002 (2007)
[11]E. J. Beswick, I. V. Pinchuk, G. Suarez, J. C. Sierra and V. E. Reyes: Helicobacter pylori CagA-dependent macrophage migration inhibitory factor produced by gastric epithelial cells binds to CD74 and stimulates procarcinogenic events. J Immunol, 176(11), 6794-801 (2006)
[12]K. L. Meyer-Siegler, K. A. Iczkowski, L. Leng, R. Bucala and P. L. Vera: Inhibition of macrophage migration inhibitory factor or its receptor (CD74) attenuates growth and invasion of DU-145 prostate cancer cells. J Immunol, 177(12), 8730-9 (2006)
[13]C. O’Reilly, M. Doroudian, L. Mawhinney and S. C. Donnelly: Targeting MIF in Cancer: Therapeutic Strategies, Current Developments, and Future Opportunities. Med Res Rev, 36(3), 440-60 (2016)
[14]X. X. He, C. Y. Liu, M. Chen, H. B. Guo, X. B. Peng and H. B. Quan: Effects of ISO-1 on liver metastases of mouse colonic cancer. Chinese J of General Surgery, 24(1), 62-65 (2009)
[15]X. X. He, H. Y. Gan, H. B. Guo, F. Y. Gao and D. Chen: Anti-macrophage migration inhibitory factor antibody inhibits tumor growth and hepatic metastases in the mouse CT26 colon tumor model. Chinese J of Experimental Surgery, 25(6), 756-757 (2008)
[16]A. N. Gordon-Weeks, S. Y. Lim, A. E. Yuzhalin, K. Jones and R. Muschel: Macrophage migration inhibitory factor: a key cytokine and therapeutic target in colon cancer. Cytokine Growth Factor Rev, 26(4), 451-61 (2015)
[17]M. Zhang, L. Yan and J. A. Kim: Modulating mammary tumor growth, metastasis and immunosuppression by siRNA-induced MIF reduction in tumor microenvironment. Cancer Gene Ther, 22(10), 463-74 (2015)
[18]B. Sun, J. Nishihira, T. Yoshiki, M. Kondo, Y. Sato, F. Sasaki and S. Todo: Macrophage migration inhibitory factor promotes tumor invasion and metastasis via the Rho-dependent pathway. Clin Cancer Res, 11(3), 1050-8 (2005)
[19]G. Ozcan, B. Ozpolat, R. L. Coleman, A. K. Sood and G. Lopez-Berestein: Preclinical and clinical development of siRNA-based therapeutics. Adv Drug Deliv Rev, 87, 108-19 (2015)
[20]R. A. Mitchell, H. Liao, J. Chesney, G. Fingerle-Rowson, J. Baugh, J. David and R. Bucala: Macrophage migration inhibitory factor (MIF) sustains macrophage proinflammatory function by inhibiting p53: regulatory role in the innate immune response. Proc Natl Acad Sci U S A, 99(1), 345-50 (2002)
[21]H. Conroy, L. Mawhinney and S. C. Donnelly: Inflammation and cancer: macrophage migration inhibitory factor (MIF)--the potential missing link. QJM, 103(11), 831-6 (2010)
[22]C. T. Hu, L. L. Guo, N. Feng, L. Zhang, N. Zhou, L. L. Ma, L. Shen, G. H. Tong, Q. W. Yan, S. J. Zhu, X. W. Bian, M. D. Lai, Y. J. Deng and Y. Q. Ding: MIF, secreted by human hepatic sinusoidal endothelial cells, promotes chemotaxis and outgrowth of colorectal cancer in liver prometastasis. Oncotarget, 6(26), 22410-23 (2015)
[23]N. Weidner: Current pathologic methods for measuring intratumoral microvessel density within breast carcinoma and other solid tumors. Breast Cancer Res Treat, 36(2), 169-80 (1995)
[24]M. Chen, X. X. He, C. Y. Liu, H. Su and H. B. Guo: The effect of ISO-1on the invasion of colonic cancer cells. Guangdong Medical Science, 29(5), 734-737 (2008)
[25]L. Leng, C. N. Metz, Y. Fang, J. Xu, S. Donnelly, J. Baugh, T. Delohery, Y. Chen, R. A. Mitchell and R. Bucala: MIF signal transduction initiated by binding to CD74. J Exp Med, 197(11), 1467-76 (2003)
[26]Y. Gore, D. Starlets, N. Maharshak, S. Becker-Herman, U. Kaneyuki, L. Leng, R. Bucala and I. Shachar: Macrophage migration inhibitory factor induces B cell survival by activation of a CD74-CD44 receptor complex. J Biol Chem, 283(5), 2784-92 (2008)
[27]I. Han, M. R. Lee, K. W. Nam, J. H. Oh, K. C. Moon and H. S. Kim: Expression of macrophage migration inhibitory factor relates to survival in high-grade osteosarcoma. Clin Orthop Relat Res, 466(9), 2107-13 (2008)
[28]Y. H. Liu, C. Y. Lin, W. C. Lin, S. W. Tang, M. K. Lai and J. Y. Lin: Up-regulation of vascular endothelial growth factor-D expression in clear cell renal cell carcinoma by CD74: a critical role in cancer cell tumorigenesis. J Immunol, 181(9), 6584-94 (2008)
[29]S. H. Lee, J. Kunz, S. H. Lin and L. Y. Yu-Lee: 16-kDa prolactin inhibits endothelial cell migration by down-regulating the Ras-Tiam1-Rac1-Pak1 signaling pathway. Cancer Res, 67(22), 11045-53 (2007)
[30]A. Malliri, T. P. Rygiel, R. A. van der Kammen, J. Y. Song, R. Engers, A. F. Hurlstone, H. Clevers and J. G. Collard: The rac activator Tiam1 is a Wnt-responsive gene that modifies intestinal tumor development. J Biol Chem, 281(1), 543-8 (2006)
[31]P. A. Singleton, R. Salgia, L. Moreno-Vinasco, J. Moitra, S. Sammani, T. Mirzapoiazova and J. G. Garcia: CD44 regulates hepatocyte growth factor-mediated vascular integrity. Role of c-Met, Tiam1/Rac1, dynamin 2, and cortactin. J Biol Chem, 282(42), 30643-57 (2007)
[32]B. Xu, F. Shen, J. Cao and L. Jia: Angiogenesis in liver metastasis of colo-rectal carcinoma. Front Biosci (Landmark Ed), 18, 1435-43 (2013)
[33]Z. Xing, E. M. Conway, C. Kang and A. Winoto: Essential role of survivin, an inhibitor of apoptosis protein, in T cell development, maturation, and homeostasis. J Exp Med, 199(1), 69-80 (2004)
[34]Z. Zhao, P. Lu, H. Zhang, H. Xu, N. Gao, M. Li and C. Liu: Nestin positively regulates the Wnt/beta-catenin pathway and the proliferation, survival and invasiveness of breast cancer stem cells. Breast Cancer Res, 16(4), 408 (2014)
[35]C. Bozzo, M. Sabbatini, R. Tiberio, V. Piffanelli, C. Santoro and M. Cannas: Activation of caspase-8 triggers anoikis in human neuroblastoma cells. Neurosci Res, 56(2), 145-53 (2006)
[36]E. L. Taylor, J. T. Li, J. C. Tupper, A. G. Rossi, R. K. Winn and J. M. Harlan: GEA 3162, a peroxynitrite donor, induces Bcl-2-sensitive, p53-independent apoptosis in murine bone marrow cells. Biochem Pharmacol, 74(7), 1039-49 (2007)
[37]D. L.L., S. D., G. D., M. White and I. Grierson: Investigation of apoptosis by p53 effector PERP in Uveal Melanoma cell lines. Invest Ophthalmol Vis Sci, 50, 5553-5561 (2009)
[38]J. Y. Hsia, C. Y. Chen, J. T. Chen, C. P. Hsu, S. E. Shai, S. S. Yang, C. Y. Chuang, P. Y. Wang and J. Miaw: Prognostic significance of caspase-3 expression in primary resected esophageal squamous cell carcinoma. Eur J Surg Oncol, 29(1), 44-8 (2003)
[39]J. J. Oudejans, A. Harijadi, S. A. Cillessen, P. Busson, I. B. Tan, D. F. Dukers, W. Vos, B. Hariwiyanto, J. Middeldorp and C. J. Meijer: Absence of caspase 3 activation in neoplastic cells of nasopharyngeal carcinoma biopsies predicts rapid fatal outcome. Mod Pathol, 18(7), 877-85 (2005)
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Frontiers in Bioscience-Landmark (FBL) is published by IMR Press from Volume 26 Issue 5 (2021). Previous articles were published by another publisher on a subscription basis, and they are hosted by IMR Press on imrpress.com as a courtesy and upon agreement with Frontiers in Bioscience.
Macrophage migration inhibitory factor siRNA inhibits hepatic metastases of colorectal cancer cells
1 Department of Gastroenterology, The First Affiliated Hospital of Guangdong Pharmaceutical University, Guangzhou, Guangdong 510080, China
2 Department of Gastroenterology, The 101 Hospital of the Chinese People’s Liberation Army, Wuxi, Jiangsu 214000, China
3 Department of Gastroenterology, Qingyuan Renmin Hospital, Qingyuan, Guangdong 511500, China
4 Institute of Vascular Biology, Guangdong Pharmaceutical University, Guangzhou, Guangdong 510080, China
Abstract
The purpose of this study was to assess the anti-tumor effects of macrophage migration inhibitory factor (MIF) siRNA on colorectal cancer in a mouse xenograft model. MIF specific siRNA (MIF siRNA) or a nonspecific control siRNA was introduced to murine colorectal cancer CT-26 cells. Mouse xenograft models of colorectal cancer were established. MIF siRNA, control siRNA or water was injected twice a week intravenously for 4 weeks. MIF siRNA inhibited the proliferation and migration, while induced apoptosis of CT-26 cells in vitro. Injection of MIF siRNA resulted in a significant decrease of serum MIF and VEGF levels, and the weight and volume of cecum-grafted tumors in vivo. In contrast, the number of apoptotic cells and caspase-3 expression were increased by MIF siRNA in cecum graft tumor tissues. Moreover, the water and fodder consumption were significantly improved by MIF siRNA treatment. Importantly, MIF siRNA reduced the hepatic metastases from colorectal cancer. Our results suggest that siRNA targeting MIF is a promising agent for the treatment of hepatic metastasis of colorectal cancer cells.
Keywords
- Colorectal cancer
- Hepatic metastases
- Macrophage migration inhibitory factor
- SiRNA
- Tumor suppressor
References
- [1] J. Ferlay, E. Steliarova-Foucher, J. Lortet-Tieulent, S. Rosso, J. W. Coebergh, H. Comber, D. Forman and F. Bray: Cancer incidence and mortality patterns in Europe: estimates for 40 countries in 2012. Eur J Cancer, 49(6), 1374-403 (2013)
- [2] P. Boyle and J. Ferlay: Cancer incidence and mortality in Europe, 2004. Ann Oncol, 16(3), 481-8 (2005)
- [3] H. Lue, R. Kleemann, T. Calandra, T. Roger and J. Bernhagen: Macrophage migration inhibitory factor (MIF): mechanisms of action and role in disease. Microbes Infect, 4(4), 449-60 (2002)
- [4] X. X. He, M. Chen and C. Y. Liu: The effects of ISO-1 on the proliferation of the colorectal cell lines. J of Hubei University For Nationalities (Medical Edition), 25, 1-4 (2008)
- [5] M. L. Toh, D. Aeberli, D. Lacey, Y. Yang, L. L. Santos, M. Clarkson, L. Sharma, C. Clyne and E. F. Morand: Regulation of IL-1 and TNF receptor expression and function by endogenous macrophage migration inhibitory factor. J Immunol, 177(7), 4818-25 (2006)
- [6] X. Y. LI and X. X. HE: Impact of macrophage migration inhibitory factor on cell migration of colorectal carcinoma cell lines in vitro. J of Modern Clinical Medical Bioengineering, 12, 402-404 (2006)
- [7] X. X. He, J. Yang, Y. W. Ding, W. Liu, Q. Y. Shen and H. H. Xia: Increased epithelial and serum expression of macrophage migration inhibitory factor (MIF) in gastric cancer: potential role of MIF in gastric carcinogenesis. Gut, 55(6), 797-802 (2006)
- [8] X. X. He, K. Chen, J. Yang, X. Y. Li, H. Y. Gan, C. Y. Liu, T. R. Coleman and Y. Al-Abed: Macrophage migration inhibitory factor promotes colorectal cancer. Mol Med, 15(1-2), 1-10 (2009)
- [9] J. D. Swant, B. E. Rendon, M. Symons and R. A. Mitchell: Rho GTPase-dependent signaling is required for macrophage migration inhibitory factor-mediated expression of cyclin D1. J Biol Chem, 280(24), 23066-72 (2005)
- [10] T. Hagemann, S. C. Robinson, R. G. Thompson, K. Charles, H. Kulbe and F. R. Balkwill: Ovarian cancer cell-derived migration inhibitory factor enhances tumor growth, progression, and angiogenesis. Mol Cancer Ther, 6(7), 1993-2002 (2007)
- [11] E. J. Beswick, I. V. Pinchuk, G. Suarez, J. C. Sierra and V. E. Reyes: Helicobacter pylori CagA-dependent macrophage migration inhibitory factor produced by gastric epithelial cells binds to CD74 and stimulates procarcinogenic events. J Immunol, 176(11), 6794-801 (2006)
- [12] K. L. Meyer-Siegler, K. A. Iczkowski, L. Leng, R. Bucala and P. L. Vera: Inhibition of macrophage migration inhibitory factor or its receptor (CD74) attenuates growth and invasion of DU-145 prostate cancer cells. J Immunol, 177(12), 8730-9 (2006)
- [13] C. O’Reilly, M. Doroudian, L. Mawhinney and S. C. Donnelly: Targeting MIF in Cancer: Therapeutic Strategies, Current Developments, and Future Opportunities. Med Res Rev, 36(3), 440-60 (2016)
- [14] X. X. He, C. Y. Liu, M. Chen, H. B. Guo, X. B. Peng and H. B. Quan: Effects of ISO-1 on liver metastases of mouse colonic cancer. Chinese J of General Surgery, 24(1), 62-65 (2009)
- [15] X. X. He, H. Y. Gan, H. B. Guo, F. Y. Gao and D. Chen: Anti-macrophage migration inhibitory factor antibody inhibits tumor growth and hepatic metastases in the mouse CT26 colon tumor model. Chinese J of Experimental Surgery, 25(6), 756-757 (2008)
- [16] A. N. Gordon-Weeks, S. Y. Lim, A. E. Yuzhalin, K. Jones and R. Muschel: Macrophage migration inhibitory factor: a key cytokine and therapeutic target in colon cancer. Cytokine Growth Factor Rev, 26(4), 451-61 (2015)
- [17] M. Zhang, L. Yan and J. A. Kim: Modulating mammary tumor growth, metastasis and immunosuppression by siRNA-induced MIF reduction in tumor microenvironment. Cancer Gene Ther, 22(10), 463-74 (2015)
- [18] B. Sun, J. Nishihira, T. Yoshiki, M. Kondo, Y. Sato, F. Sasaki and S. Todo: Macrophage migration inhibitory factor promotes tumor invasion and metastasis via the Rho-dependent pathway. Clin Cancer Res, 11(3), 1050-8 (2005)
- [19] G. Ozcan, B. Ozpolat, R. L. Coleman, A. K. Sood and G. Lopez-Berestein: Preclinical and clinical development of siRNA-based therapeutics. Adv Drug Deliv Rev, 87, 108-19 (2015)
- [20] R. A. Mitchell, H. Liao, J. Chesney, G. Fingerle-Rowson, J. Baugh, J. David and R. Bucala: Macrophage migration inhibitory factor (MIF) sustains macrophage proinflammatory function by inhibiting p53: regulatory role in the innate immune response. Proc Natl Acad Sci U S A, 99(1), 345-50 (2002)
- [21] H. Conroy, L. Mawhinney and S. C. Donnelly: Inflammation and cancer: macrophage migration inhibitory factor (MIF)--the potential missing link. QJM, 103(11), 831-6 (2010)
- [22] C. T. Hu, L. L. Guo, N. Feng, L. Zhang, N. Zhou, L. L. Ma, L. Shen, G. H. Tong, Q. W. Yan, S. J. Zhu, X. W. Bian, M. D. Lai, Y. J. Deng and Y. Q. Ding: MIF, secreted by human hepatic sinusoidal endothelial cells, promotes chemotaxis and outgrowth of colorectal cancer in liver prometastasis. Oncotarget, 6(26), 22410-23 (2015)
- [23] N. Weidner: Current pathologic methods for measuring intratumoral microvessel density within breast carcinoma and other solid tumors. Breast Cancer Res Treat, 36(2), 169-80 (1995)
- [24] M. Chen, X. X. He, C. Y. Liu, H. Su and H. B. Guo: The effect of ISO-1on the invasion of colonic cancer cells. Guangdong Medical Science, 29(5), 734-737 (2008)
- [25] L. Leng, C. N. Metz, Y. Fang, J. Xu, S. Donnelly, J. Baugh, T. Delohery, Y. Chen, R. A. Mitchell and R. Bucala: MIF signal transduction initiated by binding to CD74. J Exp Med, 197(11), 1467-76 (2003)
- [26] Y. Gore, D. Starlets, N. Maharshak, S. Becker-Herman, U. Kaneyuki, L. Leng, R. Bucala and I. Shachar: Macrophage migration inhibitory factor induces B cell survival by activation of a CD74-CD44 receptor complex. J Biol Chem, 283(5), 2784-92 (2008)
- [27] I. Han, M. R. Lee, K. W. Nam, J. H. Oh, K. C. Moon and H. S. Kim: Expression of macrophage migration inhibitory factor relates to survival in high-grade osteosarcoma. Clin Orthop Relat Res, 466(9), 2107-13 (2008)
- [28] Y. H. Liu, C. Y. Lin, W. C. Lin, S. W. Tang, M. K. Lai and J. Y. Lin: Up-regulation of vascular endothelial growth factor-D expression in clear cell renal cell carcinoma by CD74: a critical role in cancer cell tumorigenesis. J Immunol, 181(9), 6584-94 (2008)
- [29] S. H. Lee, J. Kunz, S. H. Lin and L. Y. Yu-Lee: 16-kDa prolactin inhibits endothelial cell migration by down-regulating the Ras-Tiam1-Rac1-Pak1 signaling pathway. Cancer Res, 67(22), 11045-53 (2007)
- [30] A. Malliri, T. P. Rygiel, R. A. van der Kammen, J. Y. Song, R. Engers, A. F. Hurlstone, H. Clevers and J. G. Collard: The rac activator Tiam1 is a Wnt-responsive gene that modifies intestinal tumor development. J Biol Chem, 281(1), 543-8 (2006)
- [31] P. A. Singleton, R. Salgia, L. Moreno-Vinasco, J. Moitra, S. Sammani, T. Mirzapoiazova and J. G. Garcia: CD44 regulates hepatocyte growth factor-mediated vascular integrity. Role of c-Met, Tiam1/Rac1, dynamin 2, and cortactin. J Biol Chem, 282(42), 30643-57 (2007)
- [32] B. Xu, F. Shen, J. Cao and L. Jia: Angiogenesis in liver metastasis of colo-rectal carcinoma. Front Biosci (Landmark Ed), 18, 1435-43 (2013)
- [33] Z. Xing, E. M. Conway, C. Kang and A. Winoto: Essential role of survivin, an inhibitor of apoptosis protein, in T cell development, maturation, and homeostasis. J Exp Med, 199(1), 69-80 (2004)
- [34] Z. Zhao, P. Lu, H. Zhang, H. Xu, N. Gao, M. Li and C. Liu: Nestin positively regulates the Wnt/beta-catenin pathway and the proliferation, survival and invasiveness of breast cancer stem cells. Breast Cancer Res, 16(4), 408 (2014)
- [35] C. Bozzo, M. Sabbatini, R. Tiberio, V. Piffanelli, C. Santoro and M. Cannas: Activation of caspase-8 triggers anoikis in human neuroblastoma cells. Neurosci Res, 56(2), 145-53 (2006)
- [36] E. L. Taylor, J. T. Li, J. C. Tupper, A. G. Rossi, R. K. Winn and J. M. Harlan: GEA 3162, a peroxynitrite donor, induces Bcl-2-sensitive, p53-independent apoptosis in murine bone marrow cells. Biochem Pharmacol, 74(7), 1039-49 (2007)
- [37] D. L.L., S. D., G. D., M. White and I. Grierson: Investigation of apoptosis by p53 effector PERP in Uveal Melanoma cell lines. Invest Ophthalmol Vis Sci, 50, 5553-5561 (2009)
- [38] J. Y. Hsia, C. Y. Chen, J. T. Chen, C. P. Hsu, S. E. Shai, S. S. Yang, C. Y. Chuang, P. Y. Wang and J. Miaw: Prognostic significance of caspase-3 expression in primary resected esophageal squamous cell carcinoma. Eur J Surg Oncol, 29(1), 44-8 (2003)
- [39] J. J. Oudejans, A. Harijadi, S. A. Cillessen, P. Busson, I. B. Tan, D. F. Dukers, W. Vos, B. Hariwiyanto, J. Middeldorp and C. J. Meijer: Absence of caspase 3 activation in neoplastic cells of nasopharyngeal carcinoma biopsies predicts rapid fatal outcome. Mod Pathol, 18(7), 877-85 (2005)
