About this Journal Submit a Manuscript Table of Contents
BioMed Research International
Volume 2013 (2013), Article ID 941764, 13 pages
http://dx.doi.org/10.1155/2013/941764
Research Article

Neurotensin Modulates the Migratory and Inflammatory Response of Macrophages under Hyperglycemic Conditions

1Center for Neuroscience and Cell Biology, University of Coimbra, 3004-517 Coimbra, Portugal
2CIEPQPF, Chemical Engineering Department, FCTUC, University of Coimbra, 3030-790 Coimbra, Portugal
3Faculty of Pharmacy, University of Coimbra, 3000-548 Coimbra, Portugal
4The Portuguese Diabetes Association (APDP), Rua Do Salitre, No. 118-120, 1250-203 Lisboa, Portugal

Received 8 April 2013; Revised 24 June 2013; Accepted 28 June 2013

Academic Editor: Senthil K. Venugopal

Copyright © 2013 Liane I. F. Moura 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. J. E. Shaw, R. A. Sicree, and P. Z. Zimmet, “Global estimates of the prevalence of diabetes for 2010 and 2030,” Diabetes Research and Clinical Practice, vol. 87, no. 1, pp. 4–14, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. H. Brem and M. Tomic-Canic, “Cellular and molecular basis of wound healing in diabetes,” Journal of Clinical Investigation, vol. 117, no. 5, pp. 1219–1222, 2007. View at Publisher · View at Google Scholar · View at Scopus
  3. C.-C. E. Lan, I.-H. Liu, A.-H. Fang, C.-H. Wen, and C.-S. Wu, “Hyperglycaemic conditions decrease cultured keratinocyte mobility: implications for impaired wound healing in patients with diabetes,” British Journal of Dermatology, vol. 159, no. 5, pp. 1103–1115, 2008. View at Publisher · View at Google Scholar · View at Scopus
  4. A. Tellechea, E. Leal, A. Veves, and E. Carvalho, “Inflammatory and angiogenic abnormalities in diabetic wound healing: role of neuropeptides and therapeutic perspectives,” The Open Circulation and Vascular Journal, vol. 3, pp. 43–55, 2010.
  5. L. Pradhan, C. Nabzdyk, N. D. Andersen, F. W. LoGerfo, and A. Veves, “Inflammation and neuropeptides: the connection in diabetic wound healing,” Expert Reviews in Molecular Medicine, vol. 11, article e2, 2009. View at Publisher · View at Google Scholar · View at Scopus
  6. H. Kämpfer, R. Schmidt, G. Geisslinger, J. Pfeilschifter, and S. Frank, “Wound inflammation in diabetic ob/ob mice: functional coupling of prostaglandin biosynthesis to cyclooxygenase-1 activity in diabetes-impaired wound healing,” Diabetes, vol. 54, no. 5, pp. 1543–1551, 2005. View at Publisher · View at Google Scholar · View at Scopus
  7. T. J. Koh and L. A. DiPietro, “Inflammation and wound healing: the role of the macrophage,” Expert Reviews in Molecular Medicine, vol. 13, article e23, 2011. View at Publisher · View at Google Scholar · View at Scopus
  8. J. D. Bagdade, R. K. Root, and R. J. Bulger, “Impaired leukocyte function in patients with poorly controlled diabetes,” Diabetes, vol. 23, no. 1, pp. 9–15, 1974. View at Scopus
  9. T. C. Alba-Loureiro, C. D. Munhoz, J. O. Martins et al., “Neutrophil function and metabolism in individuals with diabetes mellitus,” Brazilian Journal of Medical and Biological Research, vol. 40, no. 8, pp. 1037–1044, 2007. View at Scopus
  10. S. Khanna, S. Biswas, Y. Shang et al., “Macrophage dysfunction impairs resolution of inflammation in the wounds of diabetic mice,” PLoS ONE, vol. 5, no. 3, Article ID e9539, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. F. O. Martinez, A. Sica, A. Mantovani, and M. Locati, “Macrophage activation and polarization,” Frontiers in Bioscience, vol. 13, no. 2, pp. 453–461, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. L. F. de Souza, F. R. Jardim, I. P. Sauter, M. M. de Souza, and E. A. Bernard, “High glucose increases RAW 264.7 macrophages activation by lipoteichoic acid from Staphylococcus aureus,” Clinica Chimica Acta, vol. 398, no. 1-2, pp. 130–133, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. I. J. Elenkov, “Neurohormonal-cytokine interactions: implications for inflammation, common human diseases and well-being,” Neurochemistry International, vol. 52, no. 1, pp. 40–51, 2008. View at Publisher · View at Google Scholar · View at Scopus
  14. P. Brun, C. Mastrotto, E. Beggiao et al., “Neuropeptide neurotensin stimulates intestinal wound healing following chronic intestinal inflammation,” American Journal of Physiology, vol. 288, no. 4, pp. G621–G629, 2005. View at Publisher · View at Google Scholar · View at Scopus
  15. A. V. Delgado, A. T. McManus, and J. P. Chambers, “Exogenous administration of substance P enhances wound healing in a novel skin-injury model,” Experimental Biology and Medicine, vol. 230, no. 4, pp. 271–280, 2005. View at Scopus
  16. M. Toda, T. Suzuki, K. Hosono et al., “Roles of calcitonin gene-related peptide in facilitation of wound healing and angiogenesis,” Biomedicine and Pharmacotherapy, vol. 62, no. 6, pp. 352–359, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. L. Pradhan, X. Cai, S. Wu et al., “Gene expression of pro-inflammatory cytokines and neuropeptides in diabetic wound healing,” Journal of Surgical Research, vol. 167, no. 2, pp. 336–342, 2011. View at Publisher · View at Google Scholar · View at Scopus
  18. M. H. Jiang, E. Chung, G. F. Chi, W. Ahn, J. E. Lim, H. S. Hong, et al., “Substance P induces M2-type macrophages after spinal cord injury,” Neuroreport, vol. 23, pp. 786–792, 2012.
  19. L. H. Lazarus, M. R. Brown, and M. H. Perrin, “Distribution, localization and characteristics of neurotensin binding sites in the rat brain,” Neuropharmacology, vol. 16, no. 9, pp. 625–629, 1977. View at Scopus
  20. D. Zhao, Y. Zhan, H. Zeng, H.-W. Koon, M. P. Moyer, and C. Pothoulakis, “Neurotensin stimulates interleukin-8 expression through modulation of IκBα phosphorylation and p65 transcriptional activity: involvement of protein kinase Cα,” Molecular Pharmacology, vol. 67, no. 6, pp. 2025–2031, 2005. View at Publisher · View at Google Scholar · View at Scopus
  21. H. S. Kim, S. Yumkham, J. H. Choi et al., “Neurotensin enhances nitric oxide generation via the JAK2-STAT1 pathway in murine macrophage RAW 264.7 cells during costimulation with LPS and IFNγ,” Neuropeptides, vol. 40, no. 3, pp. 221–229, 2006. View at Publisher · View at Google Scholar · View at Scopus
  22. L. da Silva, B. M. Neves, L. Moura, M. T. Cruz, and E. Carvalho, “Neurotensin downregulates the pro-inflammatory properties of skin dendritic cells and increases epidermal growth factor expression,” Biochimica et Biophysica Acta, vol. 1813, no. 10, pp. 1863–1871, 2011. View at Publisher · View at Google Scholar · View at Scopus
  23. H.-P. Hartung, “Activation of macrophages by neuropeptides,” Brain Behavior and Immunity, vol. 2, no. 4, pp. 275–281, 1988. View at Scopus
  24. D. Ganea and M. Delgado, “Neuropeptides as modulators of macrophage functions. Regulation of cytokine production and antigen presentation by VIP and PACAP,” Archivum Immunologiae et Therapiae Experimentalis, vol. 49, no. 2, pp. 101–110, 2001. View at Scopus
  25. J.-P. Vincent, J. Mazella, and P. Kitabgi, “Neurotensin and neurotensin receptors,” Trends in Pharmacological Sciences, vol. 20, no. 7, pp. 302–309, 1999. View at Publisher · View at Google Scholar · View at Scopus
  26. M. W. Pfaffl, “A new mathematical model for relative quantification in real-time RT-PCR,” Nucleic Acids Research, vol. 29, no. 9, article e45, 2001. View at Scopus
  27. H. K. Jeon, N. P. Jung, I. H. Choi, Y. K. Oh, H. C. Shin, and B. J. Gwag, “Substance P augments nitric oxide production and gene expression in murine macrophages,” Immunopharmacology, vol. 41, no. 3, pp. 219–226, 1999. View at Publisher · View at Google Scholar · View at Scopus
  28. R. Yaraee, M. Ebtekar, A. Ahmadiani, and F. Sabahi, “Neuropeptides (SP and CGRP) augment pro-inflammatory cytokine production in HSV-infected macrophages,” International Immunopharmacology, vol. 3, no. 13-14, pp. 1883–1887, 2003. View at Publisher · View at Google Scholar · View at Scopus
  29. S. Martin, J.-P. Vincent, and J. Mazella, “Involvement of the neurotensin receptor-3 in the neurotensin-induced migration of human microglia,” Journal of Neuroscience, vol. 23, no. 4, pp. 1198–1205, 2003. View at Scopus
  30. M. De La Fuente, J. J. Garrido, R. M. Arahuetes, and A. Hernanz, “Stimulation of phagocytic function in mouse macrophages by neurotensin and neuromedin N,” Journal of Neuroimmunology, vol. 42, no. 1, pp. 97–104, 1993. View at Publisher · View at Google Scholar · View at Scopus
  31. S. Devaraj, S. K. Venugopal, U. Singh, and I. Jialal, “Hyperglycemia induces monocytic release of interleukin-6 via induction of protein kinase C-α and -β,” Diabetes, vol. 54, no. 1, pp. 85–91, 2005. View at Publisher · View at Google Scholar · View at Scopus
  32. E. Hatanaka, P. T. Monteagudo, M. S. M. Marrocos, and A. Campa, “Neutrophils and monocytes as potentially important sources of proinflammatory cytokines in diabetes,” Clinical and Experimental Immunology, vol. 146, no. 3, pp. 443–447, 2006. View at Publisher · View at Google Scholar · View at Scopus
  33. M. R. Dasu, S. Devaraj, L. Zhao, D. H. Hwang, and I. Jialal, “High glucose induces toll-like receptor expression in human monocytes Mechanism of activation,” Diabetes, vol. 57, no. 11, pp. 3090–3098, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. J. M. Cavaillon, “Cytokines and macrophages,” Biomedicine and Pharmacotherapy, vol. 48, no. 10, pp. 445–453, 1994. View at Publisher · View at Google Scholar · View at Scopus
  35. N. Silswal, A. K. Singh, B. Aruna, S. Mukhopadhyay, S. Ghosh, and N. Z. Ehtesham, “Human resistin stimulates the pro-inflammatory cytokines TNF-α and IL-12 in macrophages by NF-κB-dependent pathway,” Biochemical and Biophysical Research Communications, vol. 334, no. 4, pp. 1092–1101, 2005. View at Publisher · View at Google Scholar · View at Scopus
  36. J. R. Hill, G. Kwon, C. A. Marshall, and M. L. McDaniel, “Hyperglycemic levels of glucose inhibit interleukin 1 release from RAW 264.7 murine macrophages by activation of protein kinase C,” Journal of Biological Chemistry, vol. 273, no. 6, pp. 3308–3313, 1998. View at Publisher · View at Google Scholar · View at Scopus
  37. C. Sia, “Imbalance in Th cell polarization and its relevance in type 1 diabetes mellitus,” Review of Diabetic Studies, vol. 2, pp. 182–186, 2005.
  38. E. Dicou, J.-P. Vincent, and J. Mazella, “Neurotensin receptor-3/sortilin mediates neurotensin-induced cytokine/chemokine expression in a marine microglial cell line,” Journal of Neuroscience Research, vol. 78, no. 1, pp. 92–99, 2004. View at Publisher · View at Google Scholar · View at Scopus
  39. M. C. Dvoráková, U. Pfeil, J. Kuncová et al., “Down-regulation of vasoactive intestinal peptide and altered expression of its receptors in rat diabetic cardiomyopathy,” Cell and Tissue Research, vol. 323, no. 3, pp. 383–393, 2006. View at Publisher · View at Google Scholar · View at Scopus
  40. E. Hermans and J.-M. Maloteaux, “Mechanisms of regulation of neurotensin receptors,” Pharmacology and Therapeutics, vol. 79, no. 2, pp. 89–104, 1998. View at Publisher · View at Google Scholar · View at Scopus
  41. J. Mazella, “Sortilin/neurotensin receptor-3: a new tool to investigate neurotensin signaling and cellular trafficking?” Cellular Signalling, vol. 13, no. 1, pp. 1–6, 2001. View at Publisher · View at Google Scholar · View at Scopus
  42. F. Mule, R. Serio, and A. Postorino, “Motility pattern of isolated rat proximal colon and excitatory action of neurotensin,” European Journal of Pharmacology, vol. 275, no. 2, pp. 131–137, 1995. View at Publisher · View at Google Scholar · View at Scopus
  43. S. Hashim, Y. Li, and M. B. Anand-Srivastava, “G protein-linked cell signaling and cardiovascular functions in diabetes/hyperglycemia,” Cell Biochemistry and Biophysics, vol. 44, no. 1, pp. 51–64, 2006. View at Scopus
  44. A. Akabayashi, C. T. B. V. Zaia, I. Silva, H. J. Chae, and S. F. Leibowitz, “Neuropeptide Y in the arcuate nucleus is modulated by alterations in glucose utilization,” Brain Research, vol. 621, no. 2, pp. 343–348, 1993. View at Publisher · View at Google Scholar · View at Scopus
  45. R. Matyal, F. Mahmood, M. Robich et al., “Chronic type II diabetes mellitus leads to changes in neuropeptide y receptor expression and distribution in human myocardial tissue,” European Journal of Pharmacology, vol. 665, no. 1–3, pp. 19–28, 2011. View at Publisher · View at Google Scholar · View at Scopus