Vagal nerve stimulation modulates the dendritic cell profile in posthemorrhagic shock mesenteric lymph

Journal of Trauma and Acute Care Surgery

Volumn 76, Issue 3, 2014, Pages 610-618

  Morishita, Koji ^a   Costantini, Todd W ^a   Eliceiri, Brian ^a   Bansal, Vishal ^a   Coimbra, Raul ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Hemorrhagic shock; Inflammatory cells; Intestinal inflammation; Mesenteric lymph; Rats

Indexed keywords

B7 ANTIGEN; CD103 ANTIGEN; CD4 ANTIGEN; CD86 ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; TRANSCRIPTION FACTOR FOXP3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL POPULATION; CONTROLLED STUDY; DENDRITIC CELL; FLOW CYTOMETRY; FLUID RESUSCITATION; HEMORRHAGIC SHOCK; IMMUNE RESPONSE; IMMUNOMODULATION; IMPLANTED VAGUS NERVE STIMULATOR; INFLAMMATION; MALE; MESENTERY LYMPH NODE; NONHUMAN; PRIORITY JOURNAL; RAT; REGULATORY T LYMPHOCYTE; STAINING; VAGUS NERVE STIMULATION;

ANIMALS; ANTIGENS, CD; DENDRITIC CELLS; FLOW CYTOMETRY; INTEGRIN ALPHA CHAINS; LYMPH; MALE; MESENTERY; RATS; RATS, SPRAGUE-DAWLEY; SHOCK, HEMORRHAGIC; VAGUS NERVE; VAGUS NERVE STIMULATION; WOUNDS AND INJURIES;

EID: 84896721215     PISSN: 21630755     EISSN: 21630763     Source Type: Journal    
DOI: 10.1097/TA.0000000000000137     Document Type: Article

References (40)

1. Reys LG, Ortiz-Pomales YT, Lopez N, Cheadle G, de Oliveira PG, Eliceiri B, Bansal V, Costantini TW, Coimbra R. Uncovering the neuroentericpulmonary axis: vagal nerve stimulation prevents acute lung injury following hemorrhagic shock. Life Sci. 2013;92:783-792.
2. Deitch EA. Gut lymph and lymphatics: a source of factors leading to organ injury and dysfunction. Ann N Y Acad Sci. 2010;1207(Suppl 1): E103-E111.
3. Morishita K, Aiboshi J, Kobayashi T, Mikami S, Yokoyama Y, Ogawa K, Yokota H, Otomo Y. Lipidomics analysis of mesenteric lymph after trauma and hemorrhagic shock. J TraumaAcute Care Surg. 2012;72:1541-1547.
4. Moore EE, Organ CH Jr. Memorial lecture: splanchnic hypoperfusion provokes acute lung injury via a 5-lipoxygenase-dependent mechanism. Am J Surg. 2010;200:681-689.
5. Fanous MY, Phillips AJ, Windsor JA. Mesenteric lymph: the bridge to future management of critical illness. JOP. 2007;8:374-399.
6. Milling S, Yrlid U, Cerovic V, MacPherson G. Subsets of migrating intestinal dendritic cells. Immunol Rev. 2010;234:259-267.
7. Strauch UG, Grunwald N, Obermeier F, Gurster S, Rath HC. Loss of CD103+ intestinal dendritic cells during colonic inflammation. World J Gastroenterol. 2010;16:21-29.
8. Coombes JL, Siddiqui KR, Arancibia-Carcamo CV, Hall J, Sun CM, Belkaid Y, Powrie F. A functionally specialized population of mucosal CD103+ DCs induces Foxp3+ regulatory T cells via a TGF-beta and retinoic acidYdependent mechanism. J Exp Med. 2007;204:1757-1764.
9. Borovikova LV, Ivanova S, Zhang M, Yang H, Botchkina GI, Watkins LR, Abumrad N, Eaton JW, Tracey KJ. Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature. 2000;405:458-462.
10. Costantini TW, Bansal V, Peterson CY, Loomis WH, Putnam JG, Rankin F, Wolf P, Eliceiri BP, Baird A, Coimbra R. Efferent vagal nerve stimulation attenuates gut barrier injury after burn: modulation of intestinal occludin expression. J Trauma. 2010;68:1349-1354.
11. Krzyzaniak M, Peterson C, Loomis W, Hageny AM, Wolf P, Reys L, Putnam J, Eliceiri B, Baird A, Bansal V, et al. Postinjury vagal nerve stimulation protects against intestinal epithelial barrier breakdown. J Trauma. 2011;70:1168-1175.
12. Ruane DT, Lavelle EC. The role of CD103(+) dendritic cells in the intestinal mucosal immune system. Front Immunol. 2011;2:25.
13. Levy G, Fishman JE, Xu D, Chandler BT, Feketova E, Dong W, Qui Y, Alli V, Ulloa L, Deitch EA. Parasympathetic stimulation via the vagus nerve prevents systemic organ dysfunction by abrogating gut injury and lymph toxicity in trauma and hemorrhagic shock. Shock. 2013;39:39-44.
14. Matteoli G, Boeckxstaens GE. The vagal innervation of the gut and immune homeostasis. Gut. 2012;62:1214-1222.
15. Milling SW, Jenkins C, MacPherson G. Collection of lymph-borne dendritic cells in the rat. Nat Protoc. 2006;1:2263-2270.
16. Chiu CJ, McArdle AH, Brown R, Scott HJ, Gurd FN. Intestinal mucosal lesion in low-flow states. I. A morphological, hemodynamic, and metabolic reappraisal. Arch Surg. 1970;101:478-483.
17. Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature. 1998;392:245-252.
18. Diebel LN, Liberati DM. Estrogen impairs pulmonary microvascular response to gut-derived mediators after shock conditions. J Trauma. 2011;71:656-662.
19. Baue AE. Multiple organ failure, multiple organ dysfunction syndrome, and systemic inflammatory response syndrome. Why no magic bullets? Arch Surg. 1997;132:703-707.
20. Kawasaki T, Fujimi S, Lederer JA, Hubbard WJ, Choudhry MA, Schwacha MG, Bland KI, Chaudry IH. Trauma-hemorrhage induces depressed splenic dendritic cell functions in mice. J Immunol. 2006;177:4514-4520.
21. Xu YX, Ayala A, Chaudry IH. Prolonged immunodepression after trauma and hemorrhagic shock. J Trauma. 1998;44:335-341.
22. Zellweger R, Ayala A, DeMaso CM, Chaudry IH. Trauma-hemorrhage causes prolonged depression in cellular immunity. Shock. 1995;4:149-153.
23. De AK, Laudanski K, Miller-Graziano CL. Failure of monocytes of trauma patients to convert to immature dendritic cells is related to preferential macrophage-colony-stimulating factor-driven macrophage differentiation. J Immunol. 2003;170:6355-6362.
24. Kelsall B. Recent progress in understanding the phenotype and function of intestinal dendritic cells and macrophages. Mucosal Immunol. 2008;1: 460-469.
25. Iwasaki A. Mucosal dendritic cells. Annu Rev Immunol. 2007;25:381-418.
26. Farache J, Zigmond E, Shakhar G, Jung S. Contributions of dendritic cells and macrophages to intestinal homeostasis and immune defense. Immunol Cell Biol. 2013;91:232-239.
27. Rutella S, Locatelli F. Intestinal dendritic cells in the pathogenesis of inflammatory bowel disease. World J Gastroenterol. 2011;17:3761-3775.
28. Silva MA, Porras M, Jury J, Vergara P, Perdue MH. Characterization of ileal dendritic cell distribution in a rat model of acute and chronic inflammation. Inflamm Bowel Dis. 2006;12:457-470.
29. Annacker O, Coombes JL, Malmstrom V, Uhlig HH, Bourne T, Johansson-Lindbom B, Agace WW, Parker CM, Powrie F. Essential role for CD103 in the T cell-mediated regulation of experimental colitis. J Exp Med. 2005;202:1051-1061.
30. Campbell DJ, Koch MA. Phenotypical and functional specialization of FOXP3+ regulatory T cells. Nat Rev Immunol. 2011;11:119-130.
31. Krzyzaniak MJ, Peterson CY, Cheadle G, Loomis W, Wolf P, Kennedy V, Putnam JG, Bansal V, Eliceiri B, Baird A, et al. Efferent vagal nerve stimulation attenuates acute lung injury following burn: the importance of the gut-lung axis. Surgery. 2011;150:379-389.
32. Costantini TW, Krzyzaniak M, Cheadle GA, Putnam JG, Hageny AM, Lopez N, Eliceiri BP, Bansal V, Coimbra R. Targeting alpha-7 nicotinic acetylcholine receptor in the enteric nervous system: a cholinergic agonist prevents gut barrier failure after severe burn injury. Am J Pathol. 2012;181:478-486.
33. Costantini TW, Bansal V, Krzyzaniak M, Putnam JG, Peterson CY, Loomis WH, Wolf P, Baird A, Eliceiri BP, Coimbra R. Vagal nerve stimulation protects against burn-induced intestinal injury through activation of enteric glia cells. Am J Physiol Gastrointest Liver Physiol. 2010;299: G1308-G1318.
34. Huston JM, Gallowitsch-Puerta M, Ochani M, Ochani K, Yuan R, Rosas-Ballina M, Ashok M, Goldstein RS, Chavan S, Pavlov VA, et al. Transcutaneous vagus nerve stimulation reduces serum high mobility group box 1 levels and improves survival in murine sepsis. Crit Care Med. 2007;35: 2762-2768.
35. Matteoli G, Gomez-Pinilla PJ, Nemethova A, et al. A distinct vagal antiinflammatory pathway modulates intestinal muscularis resident macrophages independent of the spleen. Gut. 2013, Aug 23 [epub ahead of print].
36. Kawashima K, Yoshikawa K, Fujii YX, Moriwaki Y, Misawa H. Expression and function of genes encoding cholinergic components in murine immune cells. Life Sci. 2007;80:2314-2319.
37. Aicher A, Heeschen C, Mohaupt M, Cooke JP, Zeiher AM, Dimmeler S. Nicotine strongly activates dendritic cell-mediated adaptive immunity: potential role for progression of atherosclerotic lesions. Circulation. 2003;107:604-611.
38. Wang DW, Zhou RB, Yao YM, Zhu XM, Yin YM, Zhao GJ, Dong N, Sheng ZY. Stimulation of alpha7 nicotinic acetylcholine receptor by nicotine increases suppressive capacity of naturally occurring CD4+CD25+ regulatory T cells in mice in vitro. J Pharmacol Exp Ther. 2010;335:553-561.
39. Cerovic V, Houston SA, Scott CL, Aumeunier A, Yrlid U, Mowat AM, Milling SW. Intestinal CD103(j) dendritic cells migrate in lymph and prime effector T cells. Mucosal Immunol. 2013;6:104-113.
40. Schulz O, Jaensson E, Persson EK, Liu X, Worbs T, Agace WW, Pabst O. Intestinal CD103+, but not CX3CR1+, antigen sampling cells migrate in lymph and serve classical dendritic cell functions. J Exp Med. 2009;206:3101-3114.