Catecholamine Stress Alters Neutrophil Trafficking and Impairs Wound Healing by β2-adrenergic Receptor-mediated Upregulation of IL-6

Overview

Journal J Invest Dermatol

Publisher Elsevier

Specialty Dermatology

Date 2013 Oct 15

PMID 24121404

Citations 54

Authors

Min-Ho Kim

Farzam Gorouhi

Sandra Ramirez

Jennifer L Granick

Barbara A Byrne

Athena M Soulika

Scott I Simon

Rivkah R Isseroff

Affiliations

Soon will be listed here.

Abstract

Stress-induced hormones can alter the inflammatory response to tissue injury; however, the precise mechanism by which epinephrine influences inflammatory response and wound healing is not well defined. Here we demonstrate that epinephrine alters the neutrophil (polymorphonuclear leukocyte (PMN))-dependent inflammatory response to a cutaneous wound. Using noninvasive real-time imaging of genetically tagged PMNs in a murine skin wound, chronic, epinephrine-mediated stress was modeled by sustained delivery of epinephrine. Prolonged systemic exposure of epinephrine resulted in persistent PMN trafficking to the wound site via an IL-6-mediated mechanism, and this in turn impaired wound repair. Further, we demonstrate that β2-adrenergic receptor-dependent activation of proinflammatory macrophages is critical for epinephrine-mediated IL-6 production. This study expands our current understanding of stress hormone-mediated impairment of wound healing and provides an important mechanistic link to explain how epinephrine stress exacerbates inflammation via increased number and lifetime of PMNs.

Citing Articles

Altered neutrophil extracellular traps formation among medical residents with sleep deprivation.

Elhasid R, Baron S, Fidel V, Kaganov K, Shukrun R Heliyon. 2024; 10(15):e35470.

PMID: 39170531 PMC: 11336760. DOI: 10.1016/j.heliyon.2024.e35470.

Dopamine, an exogenous quorum sensing signaling molecule or a modulating factor in ?.

Xiang S, Xu K, Yin L, Rao Y, Wang B, Jia A Biofilm. 2024; 8:100208.

PMID: 39036334 PMC: 11260039. DOI: 10.1016/j.bioflm.2024.100208.

Influence of epinephrine reactivity to stress on meat quality in goats.

Shaik A, Batchu P, Naldurtiker A, Gurrapu P, Kouakou B, Terrill T Transl Anim Sci. 2024; 8:txae078.

PMID: 38827159 PMC: 11143493. DOI: 10.1093/tas/txae078.

Topical Anti-ulcerogenic Effect of the Beta-adrenergic Blockers on Diabetic Foot Ulcers: Recent Advances and Future Prospectives.

Singh P, Sharma S, Sharma P, Alam A Curr Diabetes Rev. 2023; 20(8):23-37.

PMID: 37867269 DOI: 10.2174/0115733998249061231009093006.

Inflammation in the pathogenesis of depression: a disorder of neuroimmune origin.

Corrigan M, ORourke A, Moran B, Fletcher J, Harkin A Neuronal Signal. 2023; 7(2):NS20220054.

PMID: 37457896 PMC: 10345431. DOI: 10.1042/NS20220054.

References

Insel P . Seminars in medicine of the Beth Israel Hospital, Boston. Adrenergic receptors--evolving concepts and clinical implications. N Engl J Med. 1996; 334(9):580-5. DOI: 10.1056/NEJM199602293340907. View

Kohm A, Sanders V . Norepinephrine and beta 2-adrenergic receptor stimulation regulate CD4+ T and B lymphocyte function in vitro and in vivo. Pharmacol Rev. 2001; 53(4):487-525. View

Diegelmann R, Evans M . Wound healing: an overview of acute, fibrotic and delayed healing. Front Biosci. 2004; 9:283-9. DOI: 10.2741/1184. View

Nahrendorf M, Swirski F, Aikawa E, Stangenberg L, Wurdinger T, Figueiredo J . The healing myocardium sequentially mobilizes two monocyte subsets with divergent and complementary functions. J Exp Med. 2007; 204(12):3037-47. PMC: 2118517. DOI: 10.1084/jem.20070885. View

Kavelaars A . Regulated expression of alpha-1 adrenergic receptors in the immune system. Brain Behav Immun. 2002; 16(6):799-807. DOI: 10.1016/s0889-1591(02)00033-8. View

Baker J . The selectivity of beta-adrenoceptor antagonists at the human beta1, beta2 and beta3 adrenoceptors. Br J Pharmacol. 2005; 144(3):317-22. PMC: 1576008. DOI: 10.1038/sj.bjp.0706048. View

Campbell T, Meagher M, Sieve A, Scott B, Storts R, Welsh T . The effects of restraint stress on the neuropathogenesis of Theiler's virus infection: I. Acute disease. Brain Behav Immun. 2001; 15(3):235-54. DOI: 10.1006/brbi.2000.0598. View

Pradhan L, Nabzdyk C, Andersen N, LoGerfo F, Veves A . Inflammation and neuropeptides: the connection in diabetic wound healing. Expert Rev Mol Med. 2009; 11:e2. PMC: 3708299. DOI: 10.1017/S1462399409000945. View

Gohel M, Windhaber R, Tarlton J, Whyman M, Poskitt K . The relationship between cytokine concentrations and wound healing in chronic venous ulceration. J Vasc Surg. 2008; 48(5):1272-7. DOI: 10.1016/j.jvs.2008.06.042. View

10.

Rough J, Engdahl R, Opperman K, Yerrum S, Monroy M, Daly J . beta2 Adrenoreceptor blockade attenuates the hyperinflammatory response induced by traumatic injury. Surgery. 2009; 145(2):235-42. DOI: 10.1016/j.surg.2008.09.013. View

11.

Padgett D, Marucha P, Sheridan J . Restraint stress slows cutaneous wound healing in mice. Brain Behav Immun. 1998; 12(1):64-73. DOI: 10.1006/brbi.1997.0512. View

12.

Carpenter L, Gawuga C, Tyrka A, Lee J, Anderson G, Price L . Association between plasma IL-6 response to acute stress and early-life adversity in healthy adults. Neuropsychopharmacology. 2010; 35(13):2617-23. PMC: 2978751. DOI: 10.1038/npp.2010.159. View

13.

Johnson J, Campisi J, Sharkey C, Kennedy S, Nickerson M, Greenwood B . Catecholamines mediate stress-induced increases in peripheral and central inflammatory cytokines. Neuroscience. 2005; 135(4):1295-307. DOI: 10.1016/j.neuroscience.2005.06.090. View

14.

Tymen S, Rojas I, Zhou X, Fang Z, Zhao Y, Marucha P . Restraint stress alters neutrophil and macrophage phenotypes during wound healing. Brain Behav Immun. 2012; 28:207-17. PMC: 3878450. DOI: 10.1016/j.bbi.2012.07.013. View

15.

Webster J, Tonelli L, Sternberg E . Neuroendocrine regulation of immunity. Annu Rev Immunol. 2002; 20:125-63. DOI: 10.1146/annurev.immunol.20.082401.104914. View

16.

Flierl M, Rittirsch D, Nadeau B, Chen A, Sarma J, Zetoune F . Phagocyte-derived catecholamines enhance acute inflammatory injury. Nature. 2007; 449(7163):721-5. DOI: 10.1038/nature06185. View

17.

Stow J, Low P, Offenhauser C, Sangermani D . Cytokine secretion in macrophages and other cells: pathways and mediators. Immunobiology. 2009; 214(7):601-12. DOI: 10.1016/j.imbio.2008.11.005. View

18.

Sedowofia K, Barclay C, Quaba A, Smith A, Stephen R, Thomson M . The systemic stress response to thermal injury in children. Clin Endocrinol (Oxf). 1998; 49(3):335-41. DOI: 10.1046/j.1365-2265.1998.00553.x. View

19.

Hubner G, Brauchle M, Smola H, MADLENER M, Fassler R, Werner S . Differential regulation of pro-inflammatory cytokines during wound healing in normal and glucocorticoid-treated mice. Cytokine. 1996; 8(7):548-56. DOI: 10.1006/cyto.1996.0074. View

20.

Small K, McGraw D, Liggett S . Pharmacology and physiology of human adrenergic receptor polymorphisms. Annu Rev Pharmacol Toxicol. 2003; 43:381-411. DOI: 10.1146/annurev.pharmtox.43.100901.135823. View