Ultrasound modulates the splenic neuroimmune axis in attenuating AKI

Journal of the American Society of Nephrology

Volumn 26, Issue 10, 2015, Pages 2470-2481

  Gigliotti, Joseph C ^a   Huang, Liping ^a   Bajwa, Amandeep ^a   Ye, Hong ^a   Mace, Eric H ^a   Hossack, John A ^a   Kalantari, Kambiz ^a   Inoue, Tsuyoshi ^a   Rosin, Diane L ^a   Okusa, Mark D ^a  

^a UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BUNGAROTOXIN RECEPTOR; CD11B ANTIGEN; CD3 ANTIGEN; CD4 ANTIGEN; CREATININE; CXCL1 CHEMOKINE; INTERLEUKIN 10; INTERLEUKIN 15; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; MONOCYTE CHEMOTACTIC PROTEIN 2; OXIDOPAMINE; TUMOR NECROSIS FACTOR ALPHA;

ACUTE KIDNEY FAILURE; ADOPTIVE TRANSFER; ANIMAL CELL; ARTICLE; CHEMICAL SYMPATHECTOMY; CONTROLLED STUDY; CREATININE BLOOD LEVEL; CYTOKINE PRODUCTION; DISEASE EXACERBATION; EX VIVO STUDY; GENE EXPRESSION; IMMUNOMODULATION; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RENAL PROTECTION; SPLEEN; SPLEEN CELL; SPLENECTOMY; SURVIVAL; SYMPATHETIC INNERVATION; ULTRASOUND; ACUTE KIDNEY INJURY; ANIMAL; C57BL MOUSE; IMMUNOLOGY; RADIATION RESPONSE; ULTRASOUND THERAPY;

ACUTE KIDNEY INJURY; ANIMALS; MALE; MICE; MICE, INBRED C57BL; NEUROIMMUNOMODULATION; SPLEEN; ULTRASONIC THERAPY;

EID: 84939487794     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2014080769     Document Type: Article

References (54)

1. Okusa MD, Molitoris BA, Palevsky PM, Chinchilli VM, Liu KD, Cheung AK, Weisbord SD, Faubel S, Kellum JA, Wald R, Chertow GM, Levin A, Waikar SS, Murray PT, Parikh CR, Shaw AD, Go AS, Chawla LS, Kaufman JS, Devarajan P, Toto RM, Hsu CY, Greene TH, Mehta RL, Stokes JB, Thompson AM, Thompson BT, Westenfelder CS, Tumlin JA, Warnock DG, Shah SV, Xie Y, Duggan EG, Kimmel PL, Star RA: Design of clinical trials in acute kidney injury: a report fromanNIDDK workshop-prevention trials. Clin J Am Soc Nephrol 7: 851-855, 2012.
2. Bonventre JV, Basile D, Liu KD, McKay D, Molitoris BA, Nath KA, Nickolas TL, Okusa MD, Palevsky PM, Schnellmann R, Rys-Sikora K, Kimmel PL, Star RA; Kidney Research National Dialogue (KRND): AKI: A path forward. Clin J Am Soc Nephrol 8: 1606-1608, 2013.
3. Bonventre JV, Yang L: Cellular pathophysiology of ischemic acute kidney injury. J Clin Invest 121: 4210-4221, 2011.
4. Rosin DL, Okusa MD: Dangers within: DAMP responses to damage and cell death in kidney disease. J Am Soc Nephrol 22: 416-425, 2011.
5. Li X, Hassoun HT, Santora R, Rabb H: Organ crosstalk: The role of the kidney. Curr Opin Crit Care 15: 481-487, 2009.
6. Faubel S: Acute kidney injury and multiple organ dysfunction syndrome. Minerva Urol Nefrol 61: 171-188, 2009.
7. Ratliff BB, Rabadi MM, Vasko R, Yasuda K, Goligorsky MS: Messengers without borders: Mediators of systemic inflammatory response in AKI. J AmSoc Nephrol 24: 529-536, 2013.
8. Andrés-Hernando A, Altmann C, Ahuja N, Lanaspa MA, Nemenoff R, He Z, Ishimoto T, Simpson PA, Weiser-Evans MC, Bacalja J, Faubel S: Splenectomy exacerbates lung injury after ischemic acute kidney injury in mice. Am J Physiol Renal Physiol 301: F907-F916, 2011.
9. Leelahavanichkul A, Yasuda H, Doi K, Hu X, Zhou H, Yuen PS, Star RA: Methyl-2-acetamidoacrylate, an ethyl pyruvate analog, decreases sepsis-induced acute kidney injury in mice. Am J Physiol Renal Physiol 295: F1825-F1835, 2008.
10. Jiang H, Meng F, Li W, Tong L, Qiao H, Sun X: Splenectomy ameliorates acute multiple organ damage induced by liver warm ischemia reperfusion in rats. Surgery 141: 32-40, 2007.
11. Ajmo CT Jr, Vernon DO, Collier L, Hall AA, Garbuzova-Davis S, Willing A, Pennypacker KR: The spleen contributes to stroke-induced neurodegeneration. J Neurosci Res 86: 2227-2234, 2008.
12. Gigliotti JC, Huang L, Ye H, Bajwa A, Chattrabhuti K, Lee S, Klibanov AL, Kalantari K, Rosin DL, Okusa MD: Ultrasound prevents renal ischemiareperfusion injury by stimulating the splenic cholinergic anti-inflammatory pathway. J Am Soc Nephrol 24: 1451-1460, 2013.
13. Tracey KJ: Physiology and immunology of the cholinergic antiinflammatory pathway. J Clin Invest 117: 289-296, 2007.
14. Rosas-Ballina M, Ochani M, Parrish WR, Ochani K, Harris YT, Huston JM, Chavan S, Tracey KJ: Splenic nerve is required for cholinergic antiinflammatory pathway control of TNF in endotoxemia. Proc Natl Acad Sci U S A 105: 11008-11013, 2008.
15. Brimijoin S, Molinoff PB: Effects of 6-hydroxydopamine on the activity of tyrosine hydroxylase and dopamine-b-hydroxylase in sympathetic ganglia of the rat. J Pharmacol Exp Ther 178: 417-424, 1971.
16. Sadis C, Teske G, Stokman G, Kubjak C, Claessen N, Moore F, Loi P, Diallo B, Barvais L, Goldman M, Florquin S, Le-Moine A: Nicotine protects kidney from renal ischemia/reperfusion injury through the cholinergic anti-inflammatory pathway. PLoS One 2: e469, 2007.
17. Wolf J, Rose-John S, Garbers C: Interleukin-6 and its receptors: A highly regulated and dynamic system. Cytokine 70: 11-20, 2014.
18. Hotchkiss RS, Monneret G, Payen D: Sepsis-induced immunosuppression: Fromcellular dysfunctions to immunotherapy. Nat Rev Immunol 13: 862-874, 2013.
19. Deutschman CS, Tracey KJ: Sepsis: Current dogma and new perspectives. Immunity 40: 463-475, 2014.
20. Doi K, Leelahavanichkul A, Hu X, Sidransky KL, Zhou H, Qin Y, Eisner C, Schnermann J, Yuen PS, Star RA: Pre-existing renal disease promotes sepsis-induced acute kidney injury and worsens outcome. Kidney Int 74: 1017-1025, 2008.
21. Langenberg C, Bagshaw SM, May CN, Bellomo R: The histopathology of septic acute kidney injury: A systematic review. Crit Care 12: R38, 2008.
22. Holly MK, Dear JW, Hu X, Schechter AN, Gladwin MT, Hewitt SM, Yuen PS, Star RA: Biomarker and drug-target discovery using proteomics in a new ratmodel of sepsis-induced acute renal failure. Kidney Int 70: 496- 506, 2006.
23. Steinman L: Elaborate interactions between the immune and nervous systems. Nat Immunol 5: 575-581, 2004.
24. Kox M, van Eijk LT, Zwaag J, van den Wildenberg J, Sweep FC, van der Hoeven JG, Pickkers P: Voluntary activation of the sympathetic nervous systemand attenuation of the innate immune response in humans. Proc Natl Acad Sci U S A 111: 7379-7384, 2014.
25. Matteoli G, Boeckxstaens GE: The vagal innervation of the gut and immune homeostasis. Gut 62: 1214-1222, 2013.
26. Costes LM, Boeckxstaens GE, de-Jonge WJ, Cailotto C: Neural networks in intestinal immunoregulation. Organogenesis 9: 216- 223, 2013.
27. Jänig W, Green PG: Acute inflammation in the joint: Its control by the sympathetic nervous system and by neuroendocrine systems. Auton Neurosci 182: 42-54, 2014.
28. Van-der Poll T, Jansen J, Endert E, Sauerwein HP, van-Deventer SJ: Noradrenaline inhibits lipopolysaccharide-induced tumor necrosis factor and interleukin 6 production in human whole blood. Infect Immun 62: 2046-2050, 1994.
29. Siegmund B, Eigler A, Hartmann G, Hacker U, Endres S: Adrenaline enhances LPS-induced IL-10 synthesis: Evidence for protein kinase A-mediated pathway. Int J Immunopharmacol 20: 57-69, 1998.
30. Andersson U, Tracey KJ: Neural reflexes in inflammation and immunity. J Exp Med 209: 1057-1068, 2012.
31. Brandon KW, Rand MJ: Acetylcholine and the sympathetic innervation of the spleen. J Physiol 157: 18-32, 1961.
32. Leaders FE, Dayrit C: The cholinergic component in the sympathetic innervation to the spleen. J Pharmacol Exp Ther 147: 145-152, 1965.
33. Reardon C, Duncan GS, Brüstle A, BrennerD, Tusche MW, Olofsson PS, Rosas-Ballina M, Tracey KJ, Mak TW: Lymphocyte-derived ACh regulates local innate but not adaptive immunity. Proc Natl Acad Sci U S A 110: 1410-1415, 2013.
34. Rosas-Ballina M, Olofsson PS, Ochani M, Valdés-Ferrer SI, Levine YA, Reardon C, Tusche MW, Pavlov VA, Andersson U, Chavan S, Mak TW, Tracey KJ: Acetylcholine-synthesizing T cells relay neural signals in a vagus nerve circuit. Science 334: 98-101, 2011.
35. Straub RH: Complexity of the bi-directional neuroimmune junction in the spleen. Trends Pharmacol Sci 25: 640-646, 2004.
36. Tsui PH, Wang SH, Huang CC: In vitro effects of ultrasound with different energies on the conduction properties of neural tissue. Ultrasonics 43: 560-565, 2005.
37. Mehic E, Xu JM, Caler CJ, Coulson NK, Moritz CT, Mourad PD: Increased anatomical specificity of neuromodulation via modulated focused ultrasound. PLoS One 9: e86939, 2014.
38. Ungerstedt U: 6-Hydroxy-dopamine induced degeneration of central monoamine neurons. Eur J Pharmacol 5: 107-110, 1968.
39. Kostrzewa RM, Jacobowitz DM: Pharmacological actions of 6-hydroxydopamine. Pharmacol Rev 26: 199-288, 1974.
40. Wirth T, Westendorf AM, Bloemker D, Wildmann J, Engler H, Mollerus S, Wadwa M, Schäfer MK, Schedlowski M, del-Rey A: The sympathetic nervous system modulates CD4(+)Foxp3(+) regulatory T cells via noradrenaline-dependent apoptosis in a murine model of lymphoproliferative disease. Brain Behav Immun 38: 100-110, 2014.
41. Bellinger DL, Lorton D: Autonomic regulation of cellular immune function. Auton Neurosci, 182: 15-41, 2014.
42. Bhowmick S, Singh A, Flavell RA, Clark RB, O'Rourke J, Cone RE: The sympathetic nervous system modulates CD4(+)FoxP3(+) regulatory T cells via a TGF-beta-dependent mechanism. J Leukoc Biol 86: 1275- 1283, 2009.
43. Grebe KM, Hickman HD, Irvine KR, Takeda K, Bennink JR, Yewdell JW: Sympathetic nervous system control of anti-influenza CD8+ T cell responses. Proc Natl Acad Sci U S A 106: 5300-5305, 2009.
44. Kruszewska B, Felten SY, Moynihan JA: Alterations in cytokine and antibody production following chemical sympathectomy in two strains of mice. J Immunol 155: 4613-4620, 1995.
45. De-Jonge WJ, Ulloa L: The alpha7 nicotinic acetylcholine receptor as a pharmacological target for inflammation. Br J Pharmacol 151: 915- 929, 2007.
46. Chiarandini DJ, Stefani E, Gerschenfeld HM: Ionic mechanisms of cholinergic excitation inmolluscan neurons. Science 156: 1597-1599, 1967.
47. Wang H, Liao H, Ochani M, Justiniani M, Lin X, Yang L, Al-Abed Y, Wang H, Metz C, Miller EJ, Tracey KJ, Ulloa L: Cholinergic agonists inhibit HMGB1 release and improve survival in experimental sepsis. Nat Med 10: 1216-1221, 2004.
48. Nizri E, Irony-Tur-Sinai M, Lory O, Orr-Urtreger A, Lavi E, Brenner T: Activation of the cholinergic anti-inflammatory system by nicotine attenuates neuroinflammation via suppression of Th1 and Th17 responses. J Immunol 183: 6681-6688, 2009.
49. Kielar ML, John R, Bennett M, Richardson JA, Shelton JM, Chen L, Jeyarajah DR, Zhou XJ, Zhou H, Chiquett B, Nagami GT, Lu CY: Maladaptive role of IL-6 in ischemic acute renal failure. J Am Soc Nephrol 16: 3315-3325, 2005.
50. Li L, Huang L, Sung SS, Vergis AL, Rosin DL, Rose CE Jr, Lobo PI, Okusa MD: The chemokine receptors CCR2 and CX3CR1 mediate monocyte/macrophage trafficking in kidney ischemia-reperfusion injury. Kidney Int 74: 1526-1537, 2008.
51. Zhang W, He J, Zhang F, Huang C, Wu Y, Han Y, Zhang W, Zhao Y: Prognostic role of C-reactive protein and interleukin-6 in dialysis patients: A systematic review and meta-analysis. J Nephrol 26: 243- 253, 2013.
52. Cho Y, Johnson DW, Vesey DA, Hawley CM, Pascoe EM, Clarke M, Topley N: Baseline serum interleukin-6 predicts cardiovascular events in incident peritoneal dialysis patients [published online ahead of print April 7, 2014]. Perit Dial Int doi:10.3747/pdi.2013.00272.
53. Leelahavanichkul A, Huang Y, Hu X, Zhou H, Tsuji T, Chen R, Kopp JB, Schnermann J, Yuen PS, Star RA: Chronic kidney diseaseworsens sepsis and sepsis-induced acute kidney injury by releasing high mobility group box protein-1. Kidney Int 80: 1198-1211, 2011.
54. Day Y-J, Huang L, McDuffie MJ, RosinDL, Ye H, Chen JF, Schwarzschild MA, Fink JS, Linden J, Okusa MD: Renal protection from ischemia mediated by A2A adenosine receptors on bone marrow-derived cells. J Clin Invest 112: 883-891, 2003.