Table of Contents Author Guidelines Submit a Manuscript
Mediators of Inflammation
Volume 2014, Article ID 525891, 13 pages
http://dx.doi.org/10.1155/2014/525891
Review Article

Guidance Cue Netrin-1 and the Regulation of Inflammation in Acute and Chronic Kidney Disease

1Vascular Biology Center, Georgia Regents University, Augusta, GA 30912, USA
2Department of Medicine/Vascular Biology Center, CB-3702, Georgia Regents University, 1459 Laney-Walker Boulevard, Augusta, GA 30912, USA

Received 25 March 2014; Revised 1 May 2014; Accepted 12 May 2014; Published 3 June 2014

Academic Editor: Marilia Seelaender

Copyright © 2014 Punithavathi Ranganathan 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. E. A. J. Hoste and M. Schurgers, “Epidemiology of acute kidney injury: how big is the problem?” Critical Care Medicine, vol. 36, no. 4, pp. S146–S151, 2008. View at Publisher · View at Google Scholar · View at Scopus
  2. S. H. Hou, D. A. Bushinsky, J. B. Wish, J. J. Cohen, and J. T. Harrington, “Hospital-acquired renal insufficiency: a prospective study,” The American Journal of Medicine, vol. 74, no. 2, pp. 243–248, 1983. View at Google Scholar · View at Scopus
  3. J. Himmelfarb, M. Joannidis, B. Molitoris et al., “Evaluation and initial management of acute kidney injury,” Clinical Journal of the American Society of Nephrology, vol. 3, no. 4, pp. 962–967, 2008. View at Publisher · View at Google Scholar · View at Scopus
  4. P. Rossing and D. de Zeeuw, “Need for better diabetes treatment for improved renal outcome,” Kidney International, vol. 79, no. 120, pp. S28–S32, 2011. View at Publisher · View at Google Scholar · View at Scopus
  5. E. T. Rosolowsky, J. Skupien, A. M. Smiles et al., “Risk for ESRD in type 1 diabetes remains high despite renoprotection,” Journal of the American Society of Nephrology, vol. 22, no. 3, pp. 545–553, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. H.-J. Bangstad, I. Seljeflot, T. J. Berg, and K. F. Hanssen, “Renal tubulointerstitial expansion is associated with endothelial dysfunction and inflammation in type 1 diabetes,” Scandinavian Journal of Clinical and Laboratory Investigation, vol. 69, no. 1, pp. 138–144, 2009. View at Publisher · View at Google Scholar · View at Scopus
  7. J. V. Bonventre and A. Zuk, “Ischemic acute renal failure: an inflammatory disease?” Kidney International, vol. 66, no. 2, pp. 480–485, 2004. View at Publisher · View at Google Scholar · View at Scopus
  8. E. Galkina and K. Ley, “Leukocyte recruitment and vascular injury in diabetic nephropathy,” Journal of the American Society of Nephrology, vol. 17, no. 2, pp. 368–377, 2006. View at Publisher · View at Google Scholar · View at Scopus
  9. K. Furuichi, T. Wada, S. Kaneko, and P. M. Murphy, “Roles of chemokines in renal ischemia/reperfusion injury,” Frontiers in Bioscience, vol. 13, no. 11, pp. 4021–4028, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. B. Zhang, G. Ramesh, S. Uematsu, S. Akira, and W. B. Reeves, “TLR4 signaling mediates inflammation and tissue injury in nephrotoxicity,” Journal of the American Society of Nephrology, vol. 19, no. 5, pp. 923–932, 2008. View at Publisher · View at Google Scholar · View at Scopus
  11. J. F. Navarro-González and C. Mora-Fernández, “The role of inflammatory cytokines in diabetic nephropathy,” Journal of the American Society of Nephrology, vol. 19, no. 3, pp. 433–442, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. G. R. Kinsey, L. Li, and M. D. Okusa, “Inflammation in acute kidney injury,” Nephron: Experimental Nephrology, vol. 109, no. 4, pp. e102–e107, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. R. K. Tadagavadi, W. Wang, and G. Ramesh, “Netrin-1 regulates Th1/Th2/Th17 cytokine production and inflammation through UNC5B receptor and protects kidney against ischemia-reperfusion injury,” The Journal of Immunology, vol. 185, no. 6, pp. 3750–3758, 2010. View at Publisher · View at Google Scholar · View at Scopus
  14. G. Ramesh and W. B. Reeves, “TNF-α mediates chemokine and cytokine expression and renal injury in cisplatin nephrotoxicity,” Journal of Clinical Investigation, vol. 110, no. 6, pp. 835–842, 2002. View at Publisher · View at Google Scholar · View at Scopus
  15. K. L. Rock, E. Latz, F. Ontiveros, and H. Kono, “The sterile inflammatory response,” Annual Review of Immunology, vol. 28, pp. 321–342, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. H. Shen, D. Kreisel, and D. R. Goldstein, “Processes of sterile inflammation,” The Journal of Immunology, vol. 191, no. 6, pp. 2857–2863, 2013. View at Publisher · View at Google Scholar
  17. H. Wu, J. Ma, P. Wang et al., “HMGB1 contributes to kidney ischemia reperfusion injury,” Journal of the American Society of Nephrology, vol. 21, no. 11, pp. 1878–1890, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. Y. Shi, J. E. Evans, and K. L. Rock, “Molecular identification of a danger signal that alerts the immune system to dying cells,” Nature, vol. 425, no. 6957, pp. 516–521, 2003. View at Publisher · View at Google Scholar · View at Scopus
  19. M.-F. Tsan and B. Gao, “Heat shock proteins and immune system,” Journal of Leukocyte Biology, vol. 85, no. 6, pp. 905–910, 2009. View at Publisher · View at Google Scholar · View at Scopus
  20. M. S. Lamphier, C. M. Sirois, A. Verma, D. T. Golenbock, and E. Latz, “TLR9 and the recognition of self and non-self nucleic acids,” Annals of the New York Academy of Sciences, vol. 1082, pp. 31–43, 2006. View at Publisher · View at Google Scholar · View at Scopus
  21. D. L. Rosin and M. D. Okusa, “Dangers within: DAMP responses to damage and cell death in kidney disease,” Journal of the American Society of Nephrology, vol. 22, no. 3, pp. 416–425, 2011. View at Publisher · View at Google Scholar · View at Scopus
  22. H. Ali, B. Haribabu, R. M. Richardson, and R. Snyderman, “Mechanisms of inflammation and leukocyte activation,” Medical Clinics of North America, vol. 81, no. 1, pp. 1–28, 1997. View at Publisher · View at Google Scholar · View at Scopus
  23. R. G. Baker, M. S. Hayden, and S. Ghosh, “NF-κB, inflammation, and metabolic disease,” Cell Metabolism, vol. 13, no. 1, pp. 11–22, 2011. View at Publisher · View at Google Scholar · View at Scopus
  24. J. J. Friedewald and H. Rabb, “Inflammatory cells in ischemic acute renal failure,” Kidney International, vol. 66, no. 2, pp. 486–491, 2004. View at Publisher · View at Google Scholar · View at Scopus
  25. L. Li and M. D. Okusa, “Macrophages, dendritic cells, and kidney ischemia-reperfusion injury,” Seminars in Nephrology, vol. 30, no. 3, pp. 268–277, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. L. Li, L. Huang, S.-S. J. Sung et al., “NKT cell activation mediates neutrophil IFN-γ production and renal eschemia-reperfusion injury,” The Journal of Immunology, vol. 178, no. 9, pp. 5899–5911, 2007. View at Google Scholar · View at Scopus
  27. Y.-J. Day, L. Huang, H. Ye, L. Li, J. Linden, and M. D. Okusa, “Renal ischemia-reperfusion injury and adenosine 2A receptor-mediated tissue protection: the role of CD4+ T cells and IFN-γ,” The Journal of Immunology, vol. 176, no. 5, pp. 3108–3114, 2006. View at Google Scholar · View at Scopus
  28. H. Rabb, C. C. Mendiola, S. R. Saba et al., “Antibodies to ICAM-1 protect kidneys in severe ischemic reperfusion injury,” Biochemical and Biophysical Research Communications, vol. 211, no. 1, pp. 67–73, 1995. View at Publisher · View at Google Scholar · View at Scopus
  29. J. C. Leemans, G. Stokman, N. Claessen et al., “Renal-associated TLR2 mediates ischemia/reperfusion injury in the kidney,” Journal of Clinical Investigation, vol. 115, no. 10, pp. 2894–2903, 2005. View at Publisher · View at Google Scholar · View at Scopus
  30. S.-K. Jo, S.-A. Sung, W.-Y. Cho, K.-J. Go, and H.-K. Kim, “Macrophages contribute to the initiation of ischaemic acute renal failure in rats,” Nephrology Dialysis Transplantation, vol. 21, no. 5, pp. 1231–1239, 2006. View at Publisher · View at Google Scholar · View at Scopus
  31. M. J. Burne, F. Daniels, A. El Ghandour et al., “Identification of the CD4+ T cell as a major pathogenic factor in ischemic acute renal failure,” Journal of Clinical Investigation, vol. 108, no. 9, pp. 1283–1290, 2001. View at Publisher · View at Google Scholar · View at Scopus
  32. L. Li, L. Huang, S.-S. J. Sung et al., “The chemokine receptors CCR2 and CX3CR1 mediate monocyte/macrophage trafficking in kidney ischemia-reperfusion injury,” Kidney International, vol. 74, no. 12, pp. 1526–1537, 2008. View at Publisher · View at Google Scholar · View at Scopus
  33. M. J. Burne-Taney, D. B. Ascon, F. Daniels, L. Racusen, W. Baldwin, and H. Rabb, “B cell deficiency confers protection from renal ischemia reperfusion injury,” The Journal of Immunology, vol. 171, no. 6, pp. 3210–3215, 2003. View at Google Scholar · View at Scopus
  34. Y.-J. Day, L. Huang, H. Ye, J. Linden, and M. D. Okusa, “Renal ischemia-reperfusion injury and adenosine 2A receptor-mediated tissue protection: role of macrophages,” American Journal of Physiology: Renal Physiology, vol. 288, no. 4, pp. F722–F731, 2005. View at Publisher · View at Google Scholar · View at Scopus
  35. K. J. Kelly, W. W. Williams Jr., R. B. Colvin et al., “Intercellular adhesion molecule-1-deficient mice are protected against ischemic renal injury,” Journal of Clinical Investigation, vol. 97, no. 4, pp. 1056–1063, 1996. View at Google Scholar · View at Scopus
  36. G. R. Kinsey, R. Sharma, L. Huang et al., “Regulatory T cells suppress innate immunity in kidney ischemia-reperfusion injury,” Journal of the American Society of Nephrology, vol. 20, no. 8, pp. 1744–1753, 2009. View at Publisher · View at Google Scholar · View at Scopus
  37. L. Li, L. Huang, H. Ye et al., “Dendritic cells tolerized with adenosine A2AR agonist attenuate acute kidney injury,” Journal of Clinical Investigation, vol. 122, no. 11, pp. 3931–3942, 2012. View at Publisher · View at Google Scholar · View at Scopus
  38. P. Park, M. Haas, P. N. Cunningham, L. Bao, J. J. Alexander, and R. J. Quigg, “Injury in renal ischemia-reperfusion is independent from immunoglobulins and T lymphocytes,” American Journal of Physiology: Renal Physiology, vol. 282, no. 2, pp. F352–F357, 2002. View at Google Scholar · View at Scopus
  39. M. J. Burne-Taney, N. Yokota-Ikeda, and H. Rabb, “Effects of combined T- and B-cell deficiency on murine ischemia reperfusion injury,” American Journal of Transplantation, vol. 5, no. 6, pp. 1186–1193, 2005. View at Publisher · View at Google Scholar · View at Scopus
  40. R. K. Tadagavadi and W. B. Reeves, “Renal dendritic cells ameliorate nephrotoxic acute kidney injury,” Journal of the American Society of Nephrology, vol. 21, no. 1, pp. 53–63, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. K. K. Donnahoo, X. Meng, A. Ayala, M. P. Cain, A. H. Harken, and D. R. Meldrum, “Early kidney TNF-α expression mediates neutrophil infiltration and injury after renal ischemia-reperfusion,” American Journal of Physiology: Regulatory Integrative and Comparative Physiology, vol. 277, no. 3, pp. R922–R929, 1999. View at Google Scholar · View at Scopus
  42. M. L. Kielar, R. John, M. Bennett et al., “Maladaptive role of IL-6 in ischemic acute renal failure,” Journal of the American Society of Nephrology, vol. 16, no. 11, pp. 3315–3325, 2005. View at Publisher · View at Google Scholar · View at Scopus
  43. K. Furuichi, T. Wada, Y. Iwata et al., “CCR2 signaling contributes to ischemia-reperfusion injury in kidney,” Journal of the American Society of Nephrology, vol. 14, no. 10, pp. 2503–2515, 2003. View at Publisher · View at Google Scholar · View at Scopus
  44. K. Furuichi, S. Kaneko, and T. Wada, “Chemokine/chemokine receptor-mediated inflammation regulates pathologic changes from acute kidney injury to chronic kidney disease,” Clinical and Experimental Nephrology, vol. 13, no. 1, pp. 9–14, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. B. B. Ratliff, M. M. Rabadi, R. Vasko, K. Yasuda, and M. S. Goligorsky, “Messengers without borders: mediators of systemic inflammatory response in AKI,” Journal of the American Society of Nephrology, vol. 24, no. 4, pp. 529–536, 2013. View at Publisher · View at Google Scholar · View at Scopus
  46. S. Brenner, “The genetics of Caenorhabditis elegans,” Genetics, vol. 77, no. 1, pp. 71–94, 1974. View at Google Scholar · View at Scopus
  47. E. M. Hedgecock, J. G. Culotti, and D. H. Hall, “The unc-5, unc-6, and unc-40 genes guide circumferential migrations of pioneer axons and mesodermal cells on the epidermis in C. elegans,” Neuron, vol. 4, no. 1, pp. 61–85, 1990. View at Publisher · View at Google Scholar · View at Scopus
  48. N. Ishii, W. G. Wadsworth, B. D. Stern, J. G. Culotti, and E. M. Hedgecock, “UNC-6, a laminin-related protein, guides cell and pioneer axon migrations in C. elegans,” Neuron, vol. 9, no. 5, pp. 873–881, 1992. View at Publisher · View at Google Scholar · View at Scopus
  49. T. Serafini, T. E. Kennedy, M. J. Galko, C. Mirzayan, T. M. Jessell, and M. Tessier-Lavigne, “The netrins define a family of axon outgrowth-promoting proteins homologous to C. elegans UNC-6,” Cell, vol. 78, no. 3, pp. 409–424, 1994. View at Publisher · View at Google Scholar · View at Scopus
  50. S. A. Colamarino and M. Tessler-Lavigne, “The axonal chemoattractant netrin-1 is also a chemorepellent for trochlear motor axons,” Cell, vol. 81, no. 4, pp. 621–629, 1995. View at Google Scholar · View at Scopus
  51. C. Furne, N. Rama, V. Corset, A. Chédotal, and P. Mehlen, “Netrin-1 is a survival factor during commissural neuron navigation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 38, pp. 14465–14470, 2008. View at Publisher · View at Google Scholar · View at Scopus
  52. T. E. Kennedy, T. Serafini, J. R. de la Torre, and M. Tessier-Lavigne, “Netrins are diffusible chemotropic factors for commissural axons in the embryonic spinal cord,” Cell, vol. 78, no. 3, pp. 425–435, 1994. View at Publisher · View at Google Scholar · View at Scopus
  53. T. Serafini, S. A. Colamarino, E. D. Leonardo et al., “Netrin-1 is required for commissural axon guidance in the developing vertebrate nervous system,” Cell, vol. 87, no. 6, pp. 1001–1014, 1996. View at Publisher · View at Google Scholar · View at Scopus
  54. J. R. de la Torre, V. H. Höpker, G.-L. Ming et al., “Turning of retinal growth cones in a netrin-1 gradient mediated by the netrin receptor DCC,” Neuron, vol. 19, no. 6, pp. 1211–1224, 1997. View at Publisher · View at Google Scholar · View at Scopus
  55. J. D. Lauderdale, N. M. Davis, and J. Y. Kuwada, “Axon tracts correlate with netrin-1a expression in the zebrafish embryo,” Molecular and Cellular Neurosciences, vol. 9, no. 4, pp. 293–313, 1997. View at Publisher · View at Google Scholar · View at Scopus
  56. U. Strähle, N. Fischer, and P. Blader, “Expression and regulation of a netrin homologue in the zebrafish embryo,” Mechanisms of Development, vol. 62, no. 2, pp. 147–160, 1997. View at Publisher · View at Google Scholar · View at Scopus
  57. J. A. Meyerhardt, K. Caca, B. C. Eckstrand et al., “Netrin-1: interaction with deleted in colorectal cancer (DCC) and alterations in brain tumors and neuroblastomas,” Cell Growth and Differentiation, vol. 10, no. 1, pp. 35–42, 1999. View at Google Scholar · View at Scopus
  58. T. J. van Raay, S. M. Foskett, T. D. Connors, K. W. Klinger, G. M. Landes, and T. C. Burn, “The NTN2L gene encoding a novel human netrin maps to the autosomal dominant polycystic kidney disease region on chromosome 16p13.3,” Genomics, vol. 41, no. 2, pp. 279–282, 1997. View at Publisher · View at Google Scholar · View at Scopus
  59. H. Wang, N. G. Copeland, D. J. Gilbert, N. A. Jenkins, and M. Tessier-Lavigne, “Netrin-3, a mouse homolog of human NTN2L, is highly expressed in sensory ganglia and shows differential binding to netrin receptors,” Journal of Neuroscience, vol. 19, pp. 4938–4947, 1999. View at Google Scholar
  60. K. L. W. Sun, J. P. Correia, and T. E. Kennedy, “Netrins: versatile extracellular cues with diverse functions,” Development, vol. 138, no. 11, pp. 2153–2169, 2011. View at Publisher · View at Google Scholar · View at Scopus
  61. T. Nakashiba, T. Ikeda, S. Nishimura et al., “Netrin-G1: a novel glycosyl phosphatidylinositol-linked mammalian netrin that is functionally divergent from classical netrins,” Journal of Neuroscience, vol. 20, no. 17, pp. 6540–6550, 2000. View at Google Scholar · View at Scopus
  62. T. Nakashiba, S. Nishimura, T. Ikeda, and S. Itohara, “Complementary expression and neurite outgrowth activity of netrin-G subfamily members,” Mechanisms of Development, vol. 111, no. 1-2, pp. 47–60, 2002. View at Publisher · View at Google Scholar · View at Scopus
  63. K. Keino-Masu, M. Masu, L. Hinck et al., “Deleted in Colorectal Cancer (DCC) encodes a netrin receptor,” Cell, vol. 87, no. 2, pp. 175–185, 1996. View at Publisher · View at Google Scholar · View at Scopus
  64. K. Hong, L. Hinck, M. Nishiyama, M.-M. Poo, M. Tessier-Lavigne, and E. Stein, “A ligand-gated association between cytoplasmic domains of UNC5 and DCC family receptors converts netrin-induced growth cone attraction to repulsion,” Cell, vol. 97, no. 7, pp. 927–941, 1999. View at Publisher · View at Google Scholar · View at Scopus
  65. M. J. Barallobre, M. Pascual, J. A. del Río, and E. Soriano, “The netrin family of guidance factors: emphasis on netrin-1 signalling,” Brain Research Reviews, vol. 49, no. 1, pp. 22–47, 2005. View at Publisher · View at Google Scholar · View at Scopus
  66. A. Ly, A. Nikolaev, G. Suresh, Y. Zheng, M. Tessier-Lavigne, and E. Stein, “DSCAM is a netrin receptor that collaborates with DCC in mediating turning responses to netrin-1,” Cell, vol. 133, no. 7, pp. 1241–1254, 2008. View at Publisher · View at Google Scholar · View at Scopus
  67. A. Stanco, C. Szekeres, N. Patel et al., “Netrin-1-α3/31 integrin interactions regulate the migration of interneurons through the cortical marginal zone,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 18, pp. 7595–7600, 2009. View at Publisher · View at Google Scholar · View at Scopus
  68. M. Yebra, A. M. P. Montgomery, G. R. Diaferia et al., “Recognition of the neural chemoattractant netrin-1 by integrins α6β4 and α3β1 regulates epithelial cell adhesion and migration,” Developmental Cell, vol. 5, no. 5, pp. 695–707, 2003. View at Publisher · View at Google Scholar · View at Scopus
  69. P. C. G. Haddick, I. Tom, E. Luis et al., “Defining the ligand specificity of the Deleted in Colorectal Cancer (DCC) receptor,” PLoS ONE, vol. 9, Article ID e84823, 2014. View at Publisher · View at Google Scholar
  70. E. Stein, Y. Zou, M. Poo, and M. Tessier-Lavigne, “Binding of DCC by netrin-1 to mediate axon guidance independent of adenosine A2B receptor activation,” Science, vol. 291, no. 5510, pp. 1976–1982, 2001. View at Publisher · View at Google Scholar · View at Scopus
  71. E. Matsunaga, S. Tauszig-Delamasure, P. P. Monnier et al., “RGM and its receptor neogenin regulate neuronal survival,” Nature Cell Biology, vol. 6, no. 8, pp. 749–755, 2004. View at Publisher · View at Google Scholar · View at Scopus
  72. E. Lejmi, L. Leconte, S. Pédron-Mazoyer et al., “Netrin-4 inhibits angiogenesis via binding to neogenin and recruitment of Unc5B,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 34, pp. 12491–12496, 2008. View at Publisher · View at Google Scholar · View at Scopus
  73. Y. Matsumoto, F. Irie, M. Inatani, M. Tessier-Lavigne, and Y. Yamaguchi, “Netrin-1/DCC signaling in commissural axon guidance requires cell-autonomous expression of heparan sulfate,” Journal of Neuroscience, vol. 27, no. 16, pp. 4342–4350, 2007. View at Publisher · View at Google Scholar · View at Scopus
  74. G. J. Bashaw and C. S. Goodman, “Chimeric axon guidance receptors: the cytoplasmic domains of slit and netrin receptors specify attraction versus repulsion,” Cell, vol. 97, no. 7, pp. 917–926, 1999. View at Publisher · View at Google Scholar · View at Scopus
  75. H. Arakawa, “Netrin-1 and its receptors in tumorigenesis,” Nature Reviews Cancer, vol. 4, no. 12, pp. 978–987, 2004. View at Publisher · View at Google Scholar · View at Scopus
  76. P. Mehlen and D. E. Bredesen, “The dependence receptor hypothesis,” Apoptosis, vol. 9, no. 1, pp. 37–49, 2004. View at Publisher · View at Google Scholar · View at Scopus
  77. D. E. Bredesen, P. Mehlen, and S. Rabizadeh, “Apoptosis and dependence receptors: a molecular basis for cellular addiction,” Physiological Reviews, vol. 84, no. 2, pp. 411–430, 2004. View at Publisher · View at Google Scholar · View at Scopus
  78. C. Guenebeaud, D. Goldschneider, M. Castets et al., “The dependence receptor UNC5H2/B triggers apoptosis via PP2A-mediated dephosphorylation of DAP kinase,” Molecular Cell, vol. 40, no. 6, pp. 863–876, 2010. View at Publisher · View at Google Scholar · View at Scopus
  79. P. Mehlen and D. E. Bredesen, “Meeting report: cellular dependence—old concept, new mechanisms,” Science's STKE, vol. 2003, no. 213, article e55, 2003. View at Google Scholar · View at Scopus
  80. P. Mehlen and C. Guenebeaud, “Netrin-1 and its dependence receptors as original targets for cancer therapy,” Current Opinion in Oncology, vol. 22, no. 1, pp. 46–54, 2010. View at Publisher · View at Google Scholar · View at Scopus
  81. J. C. Lin, W.-H. Ho, A. Gurney, and A. Rosenthal, “The netrin-G1 ligand NGL-1 promotes the outgrowth of thalamocortical axons,” Nature Neuroscience, vol. 6, no. 12, pp. 1270–1276, 2003. View at Publisher · View at Google Scholar · View at Scopus
  82. W. Wang and G. Ramesh, “Segment-specific expression of netrin-1 receptors in normal and ischemic mouse kidney,” American Journal of Nephrology, vol. 30, no. 3, pp. 186–193, 2009. View at Publisher · View at Google Scholar · View at Scopus
  83. W. Wang, W. B. Reeves, and G. Ramesh, “Netrin-1 and kidney injury. I. Netrin-1 protects against ischemia-reperfusion injury of the kidney,” American Journal of Physiology: Renal Physiology, vol. 294, no. 4, pp. F739–F747, 2008. View at Publisher · View at Google Scholar · View at Scopus
  84. M. Tessier-Lavigne and C. S. Goodman, “The molecular biology of axon guidance,” Science, vol. 274, no. 5290, pp. 1123–1133, 1996. View at Publisher · View at Google Scholar · View at Scopus
  85. N. P. Ly, K. Komatsuzaki, I. P. Fraser et al., “Netrin-1 inhibits leukocyte migration in vitro and in vivo,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 41, pp. 14729–14734, 2005. View at Publisher · View at Google Scholar · View at Scopus
  86. P. V. Ranganathan, C. Jayakumar, and G. Ramesh, “Netrin-1-treated macrophages protect the kidney against ischemia-reperfusion injury and suppress inflammation by inducing M2 polarization,” American Journal of Physiology: Renal Physiology, vol. 304, no. 7, pp. F948–F957, 2013. View at Publisher · View at Google Scholar · View at Scopus
  87. L. E. White and H. T. Hassoun, “Inflammatory mechanisms of organ crosstalk during ischemic acute kidney injury,” International Journal of Nephrology, vol. 2012, Article ID 505197, 8 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  88. P. Rosenberger, J. M. Schwab, V. Mirakaj et al., “Hypoxia-inducible factor-dependent induction of netrin-1 dampens inflammation caused by hypoxia,” Nature Immunology, vol. 10, no. 2, pp. 195–202, 2009. View at Publisher · View at Google Scholar · View at Scopus
  89. H. K. Eltzschig and T. Eckle, “Ischemia and reperfusion-from mechanism to translation,” Nature Medicine, vol. 17, no. 11, pp. 1391–1401, 2011. View at Publisher · View at Google Scholar · View at Scopus
  90. A. Grenz, J. H. Dalton, J. D. Bauerle et al., “Partial netrin-1 deficiency aggravates acute kidney injury,” PLoS ONE, vol. 6, no. 5, Article ID e14812, 2011. View at Publisher · View at Google Scholar · View at Scopus
  91. W. Wang, W. B. Reeves, L. Pays, P. Mehlen, and G. Ramesh, “Netrin-1 overexpression protects kidney from ischemia reperfusion injury by suppressing apoptosis,” American Journal of Pathology, vol. 175, no. 3, pp. 1010–1018, 2009. View at Publisher · View at Google Scholar · View at Scopus
  92. C. M. Aherne, C. B. Collins, J. C. Masterson et al., “Neuronal guidance molecule netrin-1 attenuates inflammatory cell trafficking during acute experimental colitis,” Gut, vol. 61, no. 5, pp. 695–705, 2012. View at Publisher · View at Google Scholar · View at Scopus
  93. P. Ranganathan, C. Jayakumar, M. Santhakumar, and G. Ramesh, “Netrin-1 regulates colon-kidney cross talk through suppression of IL-6 function in a mouse model of DSS-colitis,” American Journal of Physiology: Renal Physiology, vol. 304, no. 9, pp. F1187–F1197, 2013. View at Publisher · View at Google Scholar · View at Scopus
  94. V. Mirakaj, C. A. Thix, S. Laucher et al., “Netrin-1 dampens pulmonary inflammation during acute lung injury,” American Journal of Respiratory and Critical Care Medicine, vol. 181, no. 8, pp. 815–824, 2010. View at Publisher · View at Google Scholar · View at Scopus
  95. V. Mirakaj, D. Gatidou, C. Pötzsch, K. König, and P. Rosenberger, “Netrin-1 signaling dampens inflammatory peritonitis,” The Journal of Immunology, vol. 186, no. 1, pp. 549–555, 2011. View at Publisher · View at Google Scholar · View at Scopus
  96. A. Rajasundari, L. Pays, P. Mehlen, and G. Ramesh, “Netrin-1 overexpression in kidney proximal tubular epithelium ameliorates cisplatin nephrotoxicity,” Laboratory Investigation, vol. 91, no. 12, pp. 1717–1726, 2011. View at Publisher · View at Google Scholar · View at Scopus
  97. R. Jofré, P. Rodriguez-Benitez, J. M. López-Gómez, and R. Pérez-Garcia, “Inflammatory syndrome in patients on hemodialysis,” Journal of the American Society of Nephrology, vol. 17, no. 3, pp. S274–S280, 2006. View at Publisher · View at Google Scholar · View at Scopus
  98. M. A. Spittle, N. A. Hoenich, G. J. Handelman, R. Adhikarla, P. Homel, and N. W. Levin, “Oxidative stress and inflammation in hemodialysis patients,” American Journal of Kidney Diseases, vol. 38, no. 6, pp. 1408–1413, 2001. View at Google Scholar · View at Scopus
  99. J. Zimmermann, S. Herrlinger, A. Pruy, T. Metzger, and C. Wanner, “Inflammation enhances cardiovascular risk and mortality in hemodialysis patients,” Kidney International, vol. 55, no. 2, pp. 648–658, 1999. View at Publisher · View at Google Scholar · View at Scopus
  100. K. Kalantar-Zadeh, T. A. Ikizler, G. Block, M. M. Avram, and J. D. Kopple, “Malnutrition-inflammation complex syndrome in dialysis patients: causes and consequences,” American Journal of Kidney Diseases, vol. 42, no. 5, pp. 864–881, 2003. View at Google Scholar · View at Scopus
  101. J. J. White, R. Mohamed, C. Jayakumar, and G. Ramesh, “Tubular injury marker netrin-1 is elevated early in experimental diabetes,” Journal of Nephrology, vol. 26, no. 6, pp. 1055–1064, 2013. View at Publisher · View at Google Scholar
  102. C. Jayakumar, F. L. Nauta, S. J. Bakker et al., “Netrin-1, a urinary proximal tubular injury marker, is elevated early in the time course of human diabetes,” Journal of Nephrology, vol. 27, no. 2, pp. 151–157, 2014. View at Publisher · View at Google Scholar
  103. C. Jayakumar, R. Mohamed, P. V. Ranganathan, and G. Ramesh, “Intracellular kinases mediate increased translation and secretion of netrin-1 from renal tubular epithelial cells,” PLoS ONE, vol. 6, no. 10, Article ID e26776, 2011. View at Publisher · View at Google Scholar · View at Scopus
  104. R. Mohamed, C. Jayakumar, P. V. Ranganathan, V. Ganapathy, and G. Ramesh, “Kidney proximal tubular epithelial-specific overexpression of netrin-1 suppresses inflammation and albuminuria through suppression of COX-2-mediated PGE2 production in streptozotocin-induced diabetic mice,” American Journal of Pathology, vol. 181, no. 6, pp. 1991–2002, 2012. View at Publisher · View at Google Scholar · View at Scopus
  105. E. Tak, D. Ridyard, A. Badulak et al., “Protective role for netrin-1 during diabetic nephropathy,” Journal of Molecular Medicine, vol. 91, no. 9, pp. 1071–1080, 2013. View at Publisher · View at Google Scholar
  106. L. Li, L. Huang, A. L. Vergis et al., “IL-17 produced by neutrophils regulates IFN-γ-mediated neutrophil migration in mouse kidney ischemia-reperfusion injury,” Journal of Clinical Investigation, vol. 120, no. 1, pp. 331–342, 2010. View at Publisher · View at Google Scholar · View at Scopus
  107. K. J. Kelly, W. W. Williams Jr., R. B. Colvin, and J. V. Bonventre, “Antibody to intercellular adhesion molecule 1 protects the kidney against ischemic injury,” Proceedings of the National Academy of Sciences of the United States of America, vol. 91, no. 2, pp. 812–816, 1994. View at Google Scholar · View at Scopus
  108. N. Yokota, F. Daniels, J. Crosson, and H. Rabb, “Protective effect of T cell depletion in murine renal ischemia-reperfusion injury,” Transplantation, vol. 74, no. 6, pp. 759–763, 2002. View at Google Scholar · View at Scopus
  109. S. Manicassamy and B. Pulendran, “Modulation of adaptive immunity with Toll-like receptors,” Seminars in Immunology, vol. 21, no. 4, pp. 185–193, 2009. View at Publisher · View at Google Scholar · View at Scopus
  110. J. Roman, T. Rangasamy, J. Guo et al., “T-cell activation under hypoxic conditions enhances IFN-γ secretion,” American Journal of Respiratory Cell and Molecular Biology, vol. 42, no. 1, pp. 123–128, 2010. View at Publisher · View at Google Scholar · View at Scopus
  111. X. Dong, L. A. Bachman, M. N. Miller, K. A. Nath, and M. D. Griffin, “Dendritic cells facilitate accumulation of IL-17 T cells in the kidney following acute renal obstruction,” Kidney International, vol. 74, no. 10, pp. 1294–1309, 2008. View at Publisher · View at Google Scholar · View at Scopus
  112. C. Edgerton, J. C. Crispín, C. M. Moratz et al., “IL-17 producing CD4+ T cells mediate accelerated ischemia/reperfusion-induced injury in autoimmunity-prone mice,” Clinical Immunology, vol. 130, no. 3, pp. 313–321, 2009. View at Publisher · View at Google Scholar · View at Scopus
  113. Z. Yang, A. K. Sharma, J. Linden, I. L. Kron, and V. E. Laubach, “CD4+ T lymphocytes mediate acute pulmonary ischemia-reperfusion injury,” Journal of Thoracic and Cardiovascular Surgery, vol. 137, no. 3, pp. 695–702, 2009. View at Publisher · View at Google Scholar · View at Scopus
  114. C. C. Caldwell, T. Okaya, A. Martignoni, T. Husted, R. Schuster, and A. B. Lentsch, “Divergent functions of CD4+ T lymphocytes in acute liver inflammation and injury after ischemia-reperfusion,” American Journal of Physiology: Gastrointestinal and Liver Physiology, vol. 289, no. 5, pp. G969–G976, 2005. View at Publisher · View at Google Scholar · View at Scopus
  115. P. Ranganathan, C. Jayakumar, S. Navankasattusas, D. Y. Li, I. M. Kim, and G. Ramesh, “UNC5B receptor deletion exacerbates tissue injury in response to AKI,” Journal of the American Society of Nephrology, vol. 25, no. 2, pp. 239–249, 2014. View at Publisher · View at Google Scholar
  116. P. V. Ranganathan, C. Jayakumar, R. Mohamed, Z. Dong, and G. Ramesh, “Netrin-1 regulates the inflammatory response of neutrophils and macrophages, and suppresses ischemic acute kidney injury by inhibiting COX-2-mediated PGE2 production,” Kidney International, vol. 83, no. 6, pp. 1087–1098, 2013. View at Publisher · View at Google Scholar · View at Scopus
  117. S. W. Moore, K. L. W. Sun, F. Xie, P. A. Barker, M. Conti, and T. E. Kennedy, “Soluble adenylyl cyclase is not required for axon guidance to netrin-1,” Journal of Neuroscience, vol. 28, no. 15, pp. 3920–3924, 2008. View at Publisher · View at Google Scholar · View at Scopus
  118. K. Y. Wu, J. H. Zippin, D. R. Huron et al., “Soluble adenylyl cyclase is required for netrin-1 signaling in nerve growth cones,” Nature Neuroscience, vol. 9, no. 10, pp. 1257–1264, 2006. View at Publisher · View at Google Scholar · View at Scopus
  119. H. C. Heystek, A.-C. Thierry, P. Soulard, and C. Moulon, “Phosphodiesterase 4 inhibitors reduce human dendritic cell inflammatory cytokine production and Th 1-polarizing capacity,” International Immunology, vol. 15, no. 7, pp. 827–835, 2003. View at Google Scholar · View at Scopus
  120. E. M. Aandahl, W. J. Moretto, P. A. Haslett et al., “Inhibition of antigen-specific T cell proliferation and cytokine production by protein kinase A type I,” The Journal of Immunology, vol. 169, no. 2, pp. 802–808, 2002. View at Google Scholar · View at Scopus
  121. H. P. Lemos, R. Grespan, S. M. Vieira et al., “Prostaglandin mediates IL-23/IL-17-induced neutrophil migration in inflammation by inhibiting IL-12 and IFNγ production,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 14, pp. 5954–5959, 2009. View at Publisher · View at Google Scholar · View at Scopus
  122. S. Gordon, “Alternative activation of macrophages,” Nature Reviews Immunology, vol. 3, no. 1, pp. 23–35, 2003. View at Publisher · View at Google Scholar · View at Scopus
  123. S. Gordon and P. R. Taylor, “Monocyte and macrophage heterogeneity,” Nature Reviews Immunology, vol. 5, no. 12, pp. 953–964, 2005. View at Publisher · View at Google Scholar · View at Scopus
  124. Y. Wang and D. C. H. Harris, “Macrophages in renal disease,” Journal of the American Society of Nephrology, vol. 22, pp. 21–27, 2011. View at Publisher · View at Google Scholar
  125. J. Xue, S. Schmidt, J. Sander et al., “Transcriptome-based network analysis reveals a spectrum model of human macrophage activation,” Immunity, vol. 40, no. 2, pp. 274–288, 2014. View at Publisher · View at Google Scholar
  126. A. Mantovani, A. Sica, and M. Locati, “Macrophage polarization comes of age,” Immunity, vol. 23, no. 4, pp. 344–346, 2005. View at Publisher · View at Google Scholar · View at Scopus
  127. S. Gordon and F. O. Martinez, “Alternative activation of macrophages: mechanism and functions,” Immunity, vol. 32, no. 5, pp. 593–604, 2010. View at Publisher · View at Google Scholar · View at Scopus
  128. R. A. Daynes and D. C. Jones, “Emerging roles of PPARs in inflammation and immunity,” Nature Reviews Immunology, vol. 2, no. 10, pp. 748–759, 2002. View at Publisher · View at Google Scholar · View at Scopus
  129. F. Chen, M. Wang, J. P. O'Connor, M. He, T. Tripathi, and L. E. Harrison, “Phosphorylation of PPARγ via Active ERK1/2 Leads to its Physical Association with p65 and Inhibition of NF-κβ,” Journal of Cellular Biochemistry, vol. 90, no. 4, pp. 732–744, 2003. View at Publisher · View at Google Scholar · View at Scopus