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Gastroenterology Research and Practice
Volume 2017 (2017), Article ID 6456257, 8 pages
https://doi.org/10.1155/2017/6456257
Review Article

A Review of the Role of Neurotensin and Its Receptors in Colorectal Cancer

1Department of Surgery and Cancer, Imperial College London, Chelsea & Westminster Hospital Campus, London, UK
2Department of Colorectal Surgery, The Royal Marsden Hospital, Chelsea, London, UK

Correspondence should be addressed to Christos Kontovounisios; ku.ca.lairepmi@soisinuovotnok.c

Received 4 November 2016; Accepted 24 January 2017; Published 20 February 2017

Academic Editor: Wenhao Weng

Copyright © 2017 Shengyang Qiu et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. B. M. Evers and C. M. Townsend Jr., “Growth factors, hormones and receptors in GI cancers,” in Molecular Mechanisms in Gastrointestinal Cancer, pp. 1–196, R.G. Landes Company, 1999. View at Google Scholar
  2. L. E. Heasley, “Autocrine and paracrine signaling through neuropeptide receptors in human cancer,” Oncogene, vol. 20, no. 13, pp. 1563–1569, 2001. View at Publisher · View at Google Scholar · View at Scopus
  3. R. P. Thomas, M. R. Hellmich, C. M. Townsend Jr., and B. M. Evers, “Role of gastrointestinal hormones in the proliferation of normal and neoplastic tissues,” Endocrine Reviews, vol. 24, no. 5, pp. 571–599, 2003. View at Publisher · View at Google Scholar · View at Scopus
  4. R. Carraway and S. E. Leeman, “The isolation of a new hypotensive peptide, neurotensin, from bovine hypothalami,” The Journal of Biological Chemistry, vol. 248, no. 19, pp. 6854–6861, 1973. View at Google Scholar
  5. C. F. Ferris, R. E. Carraway, R. A. Hammer, and S. E. Leeman, “Release and degradation of neurotensin during perfusion of rat small intestine with lipid,” Regulatory Peptides, vol. 12, no. 2, pp. 101–111, 1985. View at Publisher · View at Google Scholar · View at Scopus
  6. C. F. Ferris, “Neurotensin,” in Comprehensive Physiology, pp. 559–586, Wiley & Sons, Inc., 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. D. Zhao and C. Pothoulakis, “Effects of NT on gastrointestinal motility and secretion, and role in intestinal inflammation,” Peptides, vol. 27, no. 10, pp. 2434–2444, 2006. View at Publisher · View at Google Scholar · View at Scopus
  8. P. Chalon, N. Vita, M. Kaghad et al., “Molecular cloning of a levocabastine-sensitive neurotensin binding site,” FEBS Letters, vol. 386, no. 2–3, pp. 91–94, 1996. View at Publisher · View at Google Scholar · View at Scopus
  9. J. Mazella, N. Zsurger, V. Navarro et al., “The 100-kDa neurotensin receptor is gp95/sortilin, a non-G-protein-coupled receptor,” The Journal of Biological Chemistry, vol. 273, no. 41, pp. 26273–26276, 1998. View at Publisher · View at Google Scholar · View at Scopus
  10. C. Dal Farra, P. Sarret, V. Navarro, J. M. Botto, J. Mazella, and J. P. Vincent, “Involvement of the neurotensin receptor subtype NTSR3 in the growth effect of neurotensin on cancer cell lines,” International Journal of Cancer, vol. 92, no. 4, pp. 503–509, 2001. View at Publisher · View at Google Scholar · View at Scopus
  11. S. Dupouy, V. Viardot-Foucault, M. Alifano et al., “The neurotensin receptor-1 pathway contributes to human ductal breast cancer progression,” PLoS One, vol. 4, no. 1, article e4223, 2009. View at Publisher · View at Google Scholar · View at Scopus
  12. F. Souaze, S. Dupouy, V. Viardot-Foucault et al., “Expression of neurotensin and NT1 receptor in human breast cancer: a potential role in tumor progression,” Cancer Research, vol. 66, no. 12, pp. 6243–6249, 2006. View at Publisher · View at Google Scholar · View at Scopus
  13. M. Alifano, F. Souaze, S. Dupouy et al., “Neurotensin receptor 1 determines the outcome of non-small cell lung cancer,” Clinical Cancer Research, vol. 16, no. 17, pp. 4401–4410, 2010. View at Publisher · View at Google Scholar · View at Scopus
  14. J. G. Wang, N. N. Li, H. N. Li, L. Cui, and P. Wang, “Pancreatic cancer bears overexpression of neurotensin and neurotensin receptor subtype-1 and SR 48692 counteracts neurotensin induced cell proliferation in human pancreatic ductal carcinoma cell line PANC-1,” Neuropeptides, vol. 45, no. 2, pp. 151–156, 2011. View at Publisher · View at Google Scholar · View at Scopus
  15. A. E. Allen, D. N. Carney, and T. W. Moody, “Neurotensin binds with high affinity to small cell lung cancer cells,” Peptides, vol. 9, Supplement 1, pp. 57–61, 1988. View at Publisher · View at Google Scholar · View at Scopus
  16. P. Gromova, B. P. Rubin, A. Thys, C. Erneux, and J. M. Vanderwinden, “Neurotensin receptor 1 is expressed in gastrointestinal stromal tumors but not in interstitial cells of Cajal,” PLoS One, vol. 6, no. 2, article e14710, 2011. View at Publisher · View at Google Scholar · View at Scopus
  17. R. M. Myers, J. W. Shearman, M. O. Kitching, A. Ramos-Montoya, D. E. Neal, and S. V. Ley, “Cancer, chemistry, and the cell: molecules that interact with the neurotensin receptors,” ACS Chemical Biology, vol. 4, no. 7, pp. 503–525, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. C. Rovere, P. Barbero, J. J. Maoret, M. Laburthe, and P. Kitabgi, “Pro-neurotensin/neuromedin N expression and processing in human colon cancer cell lines,” Biochemical and Biophysical Research Communications, vol. 246, no. 1, pp. 155–159, 1998. View at Publisher · View at Google Scholar · View at Scopus
  19. C. Rovere, P. Barbero, and P. Kitabgi, “Evidence that PC2 is the endogenous pro-neurotensin convertase in rMTC 6-23 cells and that PC1- and PC2-transfected PC12 cells differentially process pro-neurotensin,” The Journal of Biological Chemistry, vol. 271, no. 19, pp. 11368–11375, 1996. View at Publisher · View at Google Scholar
  20. B. M. Evers, J. Ishizuka, D. H. Chung, C. M. Townsend Jr., and J. C. Thompson, “Neurotensin expression and release in human colon cancers,” Annals of Surgery, vol. 216, no. 4, pp. 421–430, 1992. View at Publisher · View at Google Scholar
  21. J. J. Maoret, Y. Anini, C. Rouyer-Fessard, D. Gully, and M. Laburthe, “Neurotensin and a non-peptide neurotensin receptor antagonist control human colon cancer cell growth in cell culture and in cells xenografted into nude mice,” International Journal of Cancer, vol. 80, no. 3, pp. 448–454, 1999. View at Google Scholar
  22. J. J. Maoret, D. Pospai, C. Rouyer-Fessard et al., “Neurotensin receptor and its mRNA are expressed in many human colon cancer cell lines but not in normal colonic epithelium: binding studies and RT-PCR experiments,” Biochemical and Biophysical Research Communications, vol. 203, no. 1, pp. 465–471, 1994. View at Publisher · View at Google Scholar · View at Scopus
  23. F. Souaze, V. Viardot-Foucault, N. Roullet et al., “Neurotensin receptor 1 gene activation by the Tcf/beta-catenin pathway is an early event in human colonic adenomas,” Carcinogenesis, vol. 27, no. 4, pp. 708–716, 2006. View at Publisher · View at Google Scholar · View at Scopus
  24. C. Bossard, F. Souaze, A. Jarry et al., “Over-expression of neurotensin high-affinity receptor 1 (NTS1) in relation with its ligand neurotensin (NT) and nuclear beta-catenin in inflammatory bowel disease-related oncogenesis,” Peptides, vol. 28, no. 10, pp. 2030–2035, 2007. View at Publisher · View at Google Scholar · View at Scopus
  25. S. Amar, P. Kitabgi, and J. P. Vincent, “Activation of phosphatidylinositol turnover by neurotensin receptors in the human colonic adenocarcinoma cell line HT29,” FEBS Letters, vol. 201, no. 1, pp. 31–36, 1986. View at Publisher · View at Google Scholar · View at Scopus
  26. J. C. Bozou, N. Rochet, I. Magnaldo, J. P. Vincent, and P. Kitabgi, “Neurotensin stimulates inositol trisphosphate-mediated calcium mobilization but not protein kinase C activation in HT29 cells. Involvement of a G-protein,” The Biochemical Journal, vol. 264, no. 3, pp. 871–878, 1989. View at Publisher · View at Google Scholar
  27. M. A. Chowdhury, A. A. Peters, S. J. Roberts-Thomson, and G. R. Monteith, “Effects of differentiation on purinergic and neurotensin-mediated calcium signaling in human HT-29 colon cancer cells,” Biochemical and Biophysical Research Communications, vol. 439, no. 1, pp. 35–39, 2013. View at Publisher · View at Google Scholar · View at Scopus
  28. R. A. Ehlers 2nd, R. M. Bonnor, X. Wang, M. R. Hellmich, and B. M. Evers, “Signal transduction mechanisms in neurotensin-mediated cellular regulation,” Surgery, vol. 124, no. 2, pp. 237–246, 1998. View at Publisher · View at Google Scholar · View at Scopus
  29. K. Briviba, S. L. Abrahamse, B. L. Pool-Zobel, and G. Rechkemmer, “Neurotensin-and EGF-induced metabolic activation of colon carcinoma cells is diminished by dietary flavonoid cyanidin but not by its glycosides,” Nutrition and Cancer, vol. 41, no. 1–2, pp. 172–179, 2001. View at Publisher · View at Google Scholar
  30. V. Navarro, S. Martin, and J. Mazella, “Internalization-dependent regulation of HT29 cell proliferation by neurotensin,” Peptides, vol. 27, no. 10, pp. 2502–2507, 2006. View at Publisher · View at Google Scholar · View at Scopus
  31. Q. Wang, Y. Zhou, and B. M. Evers, “Neurotensin phosphorylates GSK-3alpha/beta through the activation of PKC in human colon cancer cells,” Neoplasia, vol. 8, no. 9, pp. 781–787, 2006. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Younes, Z. Wu, S. Dupouy et al., “Neurotensin (NTS) and its receptor (NTSR1) causes EGFR, HER2 and HER3 over-expression and their autocrine/paracrine activation in lung tumors, confirming responsiveness to erlotinib,” Oncotarget, vol. 5, no. 18, pp. 8252–8269, 2014. View at Publisher · View at Google Scholar
  33. F. Massa, A. Tormo, S. Beraud-Dufour, T. Coppola, and J. Mazella, “Neurotensin-induced Erk1/2 phosphorylation and growth of human colonic cancer cells are independent from growth factors receptors activation,” Biochemical and Biophysical Research Communications, vol. 414, no. 1, pp. 118–122, 2011. View at Publisher · View at Google Scholar · View at Scopus
  34. K. Bakirtzi, M. Hatziapostolou, I. Karagiannides et al., “Neurotensin signaling activates microRNAs-21 and -155 and Akt, promotes tumor growth in mice, and is increased in human colon tumors,” Gastroenterology, vol. 141, no. 5, pp. 1749–1761.e1, 2011. View at Publisher · View at Google Scholar · View at Scopus
  35. D. Zhao, S. Kuhnt-Moore, H. Zeng, J. S. Wu, M. P. Moyer, and C. Pothoulakis, “Neurotensin stimulates IL-8 expression in human colonic epithelial cells through rho GTPase-mediated NF-kappa B pathways,” American Journal of Physiology. Cell Physiology, vol. 284, no. 6, pp. C1397–C1404, 2003. View at Publisher · View at Google Scholar
  36. N. A. Banker, M. R. Hellmich, H. J. Kim, C. M. Townsend Jr., and B. M. Evers, “Src-mediated activation of the human neurotensin/neuromedin N promoter,” Surgery, vol. 122, no. 2, pp. 180–186, 1997. View at Publisher · View at Google Scholar · View at Scopus
  37. D. Zhao, Y. Zhan, H. W. Koon et al., “Metalloproteinase-dependent transforming growth factor-alpha release mediates neurotensin-stimulated MAP kinase activation in human colonic epithelial cells,” The Journal of Biological Chemistry, vol. 279, no. 42, pp. 43547–43554, 2004. View at Publisher · View at Google Scholar · View at Scopus
  38. B. M. Evers, Z. Zhou, P. Celano, and J. Li, “The neurotensin gene is a downstream target for Ras activation,” The Journal of Clinical Investigation, vol. 95, no. 6, pp. 2822–2830, 1995. View at Publisher · View at Google Scholar
  39. K. M. Muller, I. H. Tveteraas, M. Aasrum et al., “Role of protein kinase C and epidermal growth factor receptor signalling in growth stimulation by neurotensin in colon carcinoma cells,” BMC Cancer, vol. 11, no. 1, p. 421, 2011. View at Publisher · View at Google Scholar · View at Scopus
  40. C. Munck Petersen, M. S. Nielsen, C. Jacobsen et al., “Propeptide cleavage conditions sortilin/neurotensin receptor-3 for ligand binding,” The EMBO Journal, vol. 18, no. 3, pp. 595–604, 1999. View at Publisher · View at Google Scholar · View at Scopus
  41. S. Martin, V. Navarro, J. P. Vincent, and J. Mazella, “Neurotensin receptor-1 and -3 complex modulates the cellular signaling of neurotensin in the HT29 cell line,” Gastroenterology, vol. 123, no. 4, pp. 1135–1143, 2002. View at Publisher · View at Google Scholar · View at Scopus
  42. A. Morinville, S. Martin, M. Lavallee, J. P. Vincent, A. Beaudet, and J. Mazella, “Internalization and trafficking of neurotensin via NTS3 receptors in HT29 cells,” The International Journal of Biochemistry & Cell Biology, vol. 36, no. 11, pp. 2153–2168, 2004. View at Publisher · View at Google Scholar · View at Scopus
  43. T. R. Ulich, L. Cheng, H. Glover, K. Yang, and K. J. Lewin, “A colonic adenocarcinoma with argentaffin cells. An immunoperoxidase study demonstrating the presence of numerous neuroendocrine products,” Cancer, vol. 51, no. 8, pp. 1483–1489, 1983. View at Google Scholar
  44. C. Chao, M. L. Tallman, K. L. Ives, C. M. Townsend Jr., and M. R. Hellmich, “Gastrointestinal hormone receptors in primary human colorectal carcinomas,” The Journal of Surgical Research, vol. 129, no. 2, pp. 313–321, 2005. View at Publisher · View at Google Scholar · View at Scopus
  45. X. Gui, G. Guzman, P. R. Dobner, and S. S. Kadkol, “Increased neurotensin receptor-1 expression during progression of colonic adenocarcinoma,” Peptides, vol. 29, no. 9, pp. 1609–1615, 2008. View at Publisher · View at Google Scholar · View at Scopus
  46. M. Tasuta, H. Iishi, M. Baba, and H. Taniguchi, “Enhancement by neurotensin of experimental carcinogenesis induced in rat colon by azoxymethane,” British Journal of Cancer, vol. 62, no. 3, pp. 368–371, 1990. View at Publisher · View at Google Scholar · View at Scopus
  47. K. Yoshinaga, B. M. Evers, M. Izukura et al., “Neurotensin stimulates growth of colon cancer,” Surgical Oncology, vol. 1, no. 2, pp. 127–134, 1992. View at Publisher · View at Google Scholar · View at Scopus
  48. J. M. Bugni, L. A. Rabadi, K. Jubbal, I. Karagiannides, G. Lawson, and C. Pothoulakis, “The neurotensin receptor-1 promotes tumor development in a sporadic but not an inflammation-associated mouse model of colon cancer,” International Journal of Cancer, vol. 130, no. 8, pp. 1798–1805, 2012. View at Publisher · View at Google Scholar · View at Scopus
  49. S. Kamimae, E. Yamamoto, M. Kai et al., “Epigenetic silencing of NTSR1 is associated with lateral and noninvasive growth of colorectal tumors,” Oncotarget, vol. 6, no. 30, pp. 29975–29990, 2015. View at Publisher · View at Google Scholar · View at Scopus
  50. F. Alshoukr, C. Rosant, V. Maes et al., “Novel neurotensin analogues for radioisotope targeting to neurotensin receptor-positive tumors,” Bioconjugate Chemistry, vol. 20, no. 8, pp. 1602–1610, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. P. J. Janssen, M. de Visser, S. M. Verwijnen et al., “Five stabilized 111In-labeled neurotensin analogs in nude mice bearing HT29 tumors,” Cancer Biotherapy & Radiopharmaceuticals, vol. 22, no. 3, pp. 374–381, 2007. View at Google Scholar
  52. Z. Wu, L. Li, S. Liu et al., “Facile preparation of a thiol-reactive (18)F-labeling agent and synthesis of (18)F-DEG-VS-NT for PET imaging of a neurotensin receptor-positive tumor,” Journal of Nuclear Medicine, vol. 55, no. 7, pp. 1178–1184, 2014. View at Publisher · View at Google Scholar · View at Scopus
  53. E. Garcia-Garayoa, P. Blauenstein, A. Blanc, V. Maes, D. Tourwe, and P. A. Schubiger, “A stable neurotensin-basedradiopharmaceutical for targeted imaging and therapy of neurotensin receptor-positive tumours,” European Journal of Nuclear Medicine and Molecular Imaging, vol. 36, no. 1, pp. 37–47, 2009. View at Publisher · View at Google Scholar · View at Scopus
  54. J. Ishii, A. Oda, S. Togawa et al., “Microbial fluorescence sensing for human neurotensin receptor type 1 using Galpha-engineered yeast cells,” Analytical Biochemistry, vol. 446, pp. 37–43, 2014. View at Publisher · View at Google Scholar · View at Scopus
  55. G. Sgourakis, A. Papapanagiotou, C. Kontovounisios et al., “The combined use of serum neurotensin and IL-8 as screening markers for colorectal cancer,” Tumour Biology, vol. 35, no. 6, pp. 5993–6002, 2014. View at Publisher · View at Google Scholar · View at Scopus
  56. X. Wang, L. N. Jackson, S. M. Johnson, Q. Wang, and B. M. Evers, “Suppression of neurotensin receptor type 1 expression and function by histone deacetylase inhibitors in human colorectal cancers,” Molecular Cancer Therapeutics, vol. 9, no. 8, pp. 2389–2398, 2010. View at Google Scholar
  57. K. Iwase, B. M. Evers, M. R. Hellmich et al., “Indirect inhibitory effect of a neurotensin receptor antagonist on human colon cancer (LoVo) growth,” Surgical Oncology, vol. 5, no. 5–6, pp. 245–251, 1996. View at Publisher · View at Google Scholar
  58. A. Levy, R. Gal, R. Granoth, Z. Dreznik, M. Fridkin, and I. Gozes, “In vitro and in vivo treatment of colon cancer by VIP antagonists,” Regulatory Peptides, vol. 109, no. 1–3, pp. 127–133, 2002. View at Publisher · View at Google Scholar · View at Scopus
  59. X. Wang, Q. Wang, K. L. Ives, and B. M. Evers, “Curcumin inhibits neurotensin-mediated interleukin-8 production and migration of HCT116 human colon cancer cells,” Clinical Cancer Research, vol. 12, no. 18, pp. 5346–5355, 2006. View at Publisher · View at Google Scholar · View at Scopus
  60. C. Falciani, A. Accardo, J. Brunetti et al., “Target-selective drug delivery through liposomes labeled with oligobranched neurotensin peptides,” ChemMedChem, vol. 6, no. 4, pp. 678–685, 2011. View at Publisher · View at Google Scholar · View at Scopus
  61. M. E. Hernandez, J. D. Rembao, D. Hernandez-Baltazar et al., “Safety of the intravenous administration of neurotensin-polyplex nanoparticles in BALB/c mice,” Nanomedicine, vol. 10, no. 4, pp. 745–754, 2014. View at Publisher · View at Google Scholar · View at Scopus
  62. N. G. Hernandez-Chan, M. J. Bannon, C. E. Orozco-Barrios et al., “Neurotensin-polyplex-mediated brain-derived neurotrophic factor gene delivery into nigral dopamine neurons prevents nigrostriatal degeneration in a rat model of early Parkinson's disease,” Journal of Biomedical Science, vol. 22, no. 1, p. 59, 2015. View at Publisher · View at Google Scholar · View at Scopus
  63. Q. Ouyang, X. Gong, H. Xiao et al., “Neurotensin promotes the progression of malignant glioma through NTSR1 and impacts the prognosis of glioma patients,” Molecular Cancer, vol. 14, no. 1, p. 21, 2015. View at Publisher · View at Google Scholar · View at Scopus
  64. K. Takahashi, C. Furukawa, A. Takano et al., “The neuromedin U-growth hormone secretagogue receptor 1b/neurotensin receptor 1 oncogenic signaling pathway as a therapeutic target for lung cancer,” Cancer Research, vol. 66, no. 19, pp. 9408–9419, 2006. View at Publisher · View at Google Scholar · View at Scopus
  65. Z. Wu, D. Martinez-Fong, J. Tredaniel, and P. Forgez, “Neurotensin and its high affinity receptor 1 as a potential pharmacological target in cancer therapy,” Frontiers in Endocrinology, vol. 3, p. 184, 2012. View at Publisher · View at Google Scholar · View at Scopus
  66. S. Dupouy, V. K. Doan, Z. Wu et al., “Activation of EGFR, HER2 and HER3 by neurotensin/neurotensin receptor 1 renders breast tumors aggressive yet highly responsive to lapatinib and metformin in mice,” Oncotarget, vol. 5, no. 18, pp. 8235–8251, 2014. View at Publisher · View at Google Scholar