Protective role for netrin-1 during diabetic nephropathy

Journal of Molecular Medicine

Volumn 91, Issue 9, 2013, Pages 1071-1080

  Tak, Eunyoung ^a   Ridyard, Douglas ^a   Badulak, Alexander ^a   Giebler, Antasia ^a   Shabeka, Uladzimir ^a   Werner, Tilmann ^b   Clambey, Eric ^a   Moldovan, Radu ^a   Zimmerman, Michael A ^c   Eltzschig, Holger K ^a   Grenz, Almut ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY HOSPITAL REGENSBURG   (Germany)

^c UNIVERSITY OF COLORADO   (United States)

Author keywords

Diabetes; Hypoxia; Inflammation; Nephropathy; Netrin 1; Vascular injury

Indexed keywords

NETRIN 1;

ALBUMINURIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIABETIC NEPHROPATHY; DISEASE SEVERITY; DRUG MECHANISM; GLOMERULUS FILTRATION RATE; HISTOLOGY; KIDNEY FUNCTION; MOUSE; NONHUMAN; OSMOTIC PUMP; RENAL PROTECTION; STREPTOZOCIN DIABETES; URINALYSIS; WILD TYPE;

ALBUMINURIA; ANIMALS; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC NEPHROPATHIES; KIDNEY; MICE; MICE, TRANSGENIC; NERVE GROWTH FACTORS; RECEPTOR, ADENOSINE A2B; RECOMBINANT PROTEINS; TUMOR SUPPRESSOR PROTEINS;

EID: 84884256510     PISSN: 09462716     EISSN: 14321440     Source Type: Journal    
DOI: 10.1007/s00109-013-1041-1     Document Type: Article

References (50)

1. Serafini T, Colamarino SA, Leonardo ED, Wang H, Beddington R et al (1996) Netrin-1 is required for commissural axon guidance in the developing vertebrate nervous system. Cell 87:1001-1014
2. Grenz A, Clambey E, Eltzschig HK (2012) Hypoxia signaling during intestinal ischemia and inflammation. Curr Opin Crit Care 18:178-185
3. Aherne CM, Collins CB, Masterson JC, Tizzano M, Boyle TA et al (2012) Neuronal guidance molecule netrin-1 attenuates inflammatory cell trafficking during acute experimental colitis. Gut 61:695-705
4. Grenz A, Dalton JH, Bauerle JD, Badulak A, Ridyard D et al (2011) Partial netrin-1 deficiency aggravates acute kidney injury. PLoS One 6:e14812
5. Rosenberger P, Schwab JM, Mirakaj V, Masekowsky E, Mager A et al (2009) Hypoxia-inducible factor-dependent induction of netrin-1 dampens inflammation caused by hypoxia. Nat Immunol 10:195-202
6. Eltzschig HK, Sitkovsky MV, Robson SC (2012) Purinergic signaling during inflammation. N Engl J Med 367:2322-2333
7. Eltzschig HK, Carmeliet P (2011) Hypoxia and inflammation. N Engl J Med 364:656-665
8. Eltzschig HK, Eckle T (2011) Ischemia and reperfusion - from mechanism to translation. Nat Med 17:1391-1401
9. van Gils JM, Derby MC, Fernandes LR, Ramkhelawon B, Ray TD et al (2012) The neuroimmune guidance cue netrin-1 promotes atherosclerosis by inhibiting the emigration of macrophages from plaques. Nat Immunol 13:136-143
10. Grenz A, Homann D, Eltzschig HK (2011) Extracellular adenosine: a safety signal that dampens hypoxia-induced inflammation during ischemia. Antioxid Redox Signal 15:2221-2234
11. Mirakaj V, Gatidou D, Potzsch C, Konig K, Rosenberger P (2011) Netrin-1 signaling dampens inflammatory peritonitis. J Immunol 186:549-555
12. Mirakaj V, Thix CA, Laucher S, Mielke C, Morote-Garcia JC et al (2010) Netrin-1 dampens pulmonary inflammation during acute lung injury. Am J Respir Crit Care Med 181:815-824
13. Mutz C, Mirakaj V, Vagts DA, Westermann P, Waibler K et al (2010) The neuronal guidance protein netrin-1 reduces alveolar inflammation in a porcine model of acute lung injury. Crit Care 14:R189
14. Mohamed R, Jayakumar C, Ranganathan PV, Ganapathy V, Ramesh G (2012) 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. Am J Pathol 181:1991-2002
15. Grenz A, Bauerle JD, Dalton JH, Ridyard D, Badulak A et al (2012) Equilibrative nucleoside transporter 1 (ENT1) regulates postischemic blood flow during acute kidney injury in mice. J Clin Invest 122:693-710
16. Tadagavadi RK, Wang W, Ramesh G (2010) Netrin-1 regulates Th1/Th2/Th17 cytokine production and inflammation through UNC5B receptor and protects kidney against ischemia-reperfusion injury. J Immunol 185:3750-3758
17. Grenz A, Osswald H, Eckle T, Yang D, Zhang H et al (2008) The reno-vascular A2B adenosine receptor protects the kidney from ischemia. PLoS Med 5:e137
18. Grenz A, Zhang H, Eckle T, Mittelbronn M, Wehrmann M et al (2007) Protective role of ecto-5′-nucleotidase (CD73) in renal ischemia. J Am Soc Nephrol 18:833-845
19. Eltzschig HK (2009) Adenosine: an old drug newly discovered. Anesthesiology 111:904-915
20. Colgan SP, Eltzschig HK (2012) Adenosine and hypoxia-inducible factor signaling in intestinal injury and recovery. Annu Rev Physiol 74:153-175
21. Koeppen M, Eckle T, Eltzschig HK (2011) The hypoxia-inflammation link and potential drug targets. Curr Opin Anaesthesiol 24:363-369
22. Koeppen M, Eckle T, Eltzschig HK (2011) Interplay of hypoxia and A2B adenosine receptors in tissue protection. Adv Pharmacol 61:145-186
23. Bauerle JD, Grenz A, Kim JH, Lee HT, Eltzschig HK (2011) Adenosine generation and signaling during acute kidney injury. J Am Soc Nephrol 22:14-20
24. Eckle T, Koeppen M, Eltzschig HK (2009) Role of extracellular adenosine in acute lung injury. Physiology (Bethesda) 24:298-306
25. Ly NP, Komatsuzaki K, Fraser IP, Tseng AA, Prodhan P et al (2005) Netrin-1 inhibits leukocyte migration in vitro and in vivo. Proc Natl Acad Sci U S A 102:14729-14734
26. Morote-Garcia JC, Rosenberger P, Nivillac NM, Coe IR, Eltzschig HK (2009) Hypoxia-inducible factor-dependent repression of equilibrative nucleoside transporter 2 attenuates mucosal inflammation during intestinal hypoxia. Gastroenterology 136:607-618
27. Morote-Garcia JC, Rosenberger P, Kuhlicke J, Eltzschig HK (2008) HIF-1-dependent repression of adenosine kinase attenuates hypoxia-induced vascular leak. Blood 111:5571-5580
28. Frick JS, MacManus CF, Scully M, Glover LE, Eltzschig HK et al (2009) Contribution of adenosine A2B receptors to inflammatory parameters of experimental colitis. J Immunol 182:4957-4964
29. Hart ML, Gorzolla IC, Schittenhelm J, Robson SC, Eltzschig HK (2010) SP1-dependent induction of CD39 facilitates hepatic ischemic preconditioning. J Immunol 184:4017-4024
30. Eltzschig HK, Kohler D, Eckle T, Kong T, Robson SC et al (2009) Central role of Sp1-regulated CD39 in hypoxia/ischemia protection. Blood 113:224-232
31. Hart ML, Grenz A, Gorzolla IC, Schittenhelm J, Dalton JH et al (2011) Hypoxia-inducible factor-1alpha-dependent protection from intestinal ischemia/reperfusion injury involves ecto-5′-nucleotidase (CD73) and the A2B adenosine receptor. J Immunol 186:4367-4374
32. Hart ML, Jacobi B, Schittenhelm J, Henn M, Eltzschig HK (2009) Cutting edge: A2B adenosine receptor signaling provides potent protection during intestinal ischemia/reperfusion injury. J Immunol 182:3965-3968
33. Hart ML, Henn M, Kohler D, Kloor D, Mittelbronn M et al (2008) Role of extracellular nucleotide phosphohydrolysis in intestinal ischemia-reperfusion injury. FASEB J 22:2784-2797
34. Hart ML, Much C, Gorzolla IC, Schittenhelm J, Kloor D et al (2008) Extracellular adenosine production by ecto-5′-nucleotidase protects during murine hepatic ischemic preconditioning. Gastroenterology 135:1739-1750, e1733
35. Reutershan J, Vollmer I, Stark S, Wagner R, Ngamsri KC et al (2009) Adenosine and inflammation: CD39 and CD73 are critical mediators in LPS-induced PMN trafficking into the lungs. FASEB J 23:473-482
36. Eltzschig HK, Macmanus CF, Colgan SP (2008) Neutrophils as sources of extracellular nucleotides: functional consequences at the vascular interface. Trends Cardiovasc Med 18:103-107
37. Eltzschig HK, Eckle T, Mager A, Kuper N, Karcher C et al (2006) ATP release from activated neutrophils occurs via connexin 43 and modulates adenosine-dependent endothelial cell function. Circ Res 99:1100-1108
38. Eckle T, Kohler D, Lehmann R, El Kasmi KC, Eltzschig HK (2008) Hypoxia-inducible factor-1 is central to cardioprotection: a new paradigm for ischemic preconditioning. Circulation 118:166-175
39. Grenz A, Zhang H, Weingart J, von Wietersheim S, Eckle T et al (2007) Lack of effect of extracellular adenosine generation and signalling on renal erythropoietin secretion during hypoxia. Am J Physiol Renal Physiol 293:F1501-F1511
40. Eltzschig HK, Faigle M, Knapp S, Karhausen J, Ibla J et al (2006) Endothelial catabolism of extracellular adenosine during hypoxia: the role of surface adenosine deaminase and CD26. Blood 108:1602-1610
41. Kong T, Westerman KA, Faigle M, Eltzschig HK, Colgan SP (2006) HIF-dependent induction of adenosine A2B receptor in hypoxia. FASEB J 20:2242-2250
42. Thompson LF, Eltzschig HK, Ibla JC, Van De Wiele CJ, Resta R et al (2004) Crucial role for ecto-5′-nucleotidase (CD73) in vascular leakage during hypoxia. J Exp Med 200:1395-1405
43. Eltzschig HK, Ibla JC, Furuta GT, Leonard MO, Jacobson KA et al (2003) Coordinated adenine nucleotide phosphohydrolysis and nucleoside signaling in posthypoxic endothelium: role of ectonucleotidases and adenosine A2B receptors. J Exp Med 198:783-796
44. Synnestvedt K, Furuta GT, Comerford KM, Louis N, Karhausen J et al (2002) Ecto-5′-nucleotidase (CD73) regulation by hypoxia-inducible factor-1 mediates permeability changes in intestinal epithelia. J Clin Invest 110:993-1002
45. Eckle T, Faigle M, Grenz A, Laucher S, Thompson LF et al (2008) A2B adenosine receptor dampens hypoxia-induced vascular leak. Blood 111:2024-2035
46. Ehrentraut H, Westrich JA, Eltzschig HK, Clambey ET (2012) Adora2b adenosine receptor engagement enhances regulatory T cell abundance during endotoxin-induced pulmonary inflammation. PLoS One 7:e32416
47. Eltzschig HK, Thompson LF, Karhausen J, Cotta RJ, Ibla JC et al (2004) Endogenous adenosine produced during hypoxia attenuates neutrophil accumulation: coordination by extracellular nucleotide metabolism. Blood 104:3986-3992
48. Eckle T, Hartmann K, Bonney S, Reithel S, Mittelbronn M et al (2012) Adora2b-elicited Per2 stabilization promotes a HIF-dependent metabolic switch crucial for myocardial adaptation to ischemia. Nat Med 18:774-782
49. Eckle T, Krahn T, Grenz A, Kohler D, Mittelbronn M et al (2007) Cardioprotection by ecto-5′-nucleotidase (CD73) and A2B adenosine receptors. Circulation 115:1581-1590
50. Kohler D, Eckle T, Faigle M, Grenz A, Mittelbronn M et al (2007) CD39/ectonucleoside triphosphate diphosphohydrolase 1 provides myocardial protection during cardiac ischemia/reperfusion injury. Circulation 116:1784-1794