Tulathromycin exerts proresolving effects in bovine neutrophils by inhibiting phospholipases and altering leukotriene B4, prostaglandin E2, and lipoxin A4 production

Antimicrobial Agents and Chemotherapy

Volumn 58, Issue 8, 2014, Pages 4298-4307

  Fischer, Carrie D ^a   Duquette, Stephanie C ^a   Renaux, Bernard S ^a   Feener, Troy D ^a   Morck, Douglas W ^a   Hollenberg, Morley D ^a   Lucas, Merlyn J ^b   Buret, Andre G ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b ZOETIS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

15-HYDROXY-5,8,11,13-EICOSATETRAENOIC ACID; CALCIMYCIN; DISACCHARIDE; HETEROCYCLIC COMPOUND; HYDROXYICOSATETRAENOIC ACID; LEUKOTRIENE B4; LIPOXIN; LIPOXIN A; NONSTEROID ANTIINFLAMMATORY AGENT; PARTICULATE MATTER; PHOSPHOLIPASE A2; PROSTAGLANDIN E2; TULATHROMYCIN; ZYMOSAN;

AGONISTS; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; BOVINE; BRONCHOALVEOLAR LAVAGE FLUID; CHEMICALLY INDUCED; CHEMISTRY; DRUG EFFECTS; LUNG; MALE; METABOLISM; NEUTROPHIL; PARTICULATE MATTER; PATHOLOGY; PNEUMONIA; PRIMARY CELL CULTURE;

ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; BRONCHOALVEOLAR LAVAGE FLUID; CALCIMYCIN; CATTLE; DINOPROSTONE; DISACCHARIDES; HETEROCYCLIC COMPOUNDS; HYDROXYEICOSATETRAENOIC ACIDS; LEUKOTRIENE B4; LIPOXINS; LUNG; MALE; NEUTROPHILS; PARTICULATE MATTER; PHOSPHOLIPASES A2; PNEUMONIA; PRIMARY CELL CULTURE; ZYMOSAN;

EID: 84905387104     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.02813-14     Document Type: Article

References (65)

1. Kaley G, Hintze TH, Panzenbeck M, Messina EJ. 1985. Role of prostaglandins in microcirculatory function. Adv. Prostaglandin Thromboxane Leukot. Res. 13:27-35.
2. Williams TJ, Morley J. 1973. Prostaglandins as potentiators of increased vascular permeabilityininflammation. Nature 246:215-217. http://dx.doi.org/10. 1038/246215a0.
3. Caristi S, Piraino G, Cucinotta M, Valenti A, Loddo S, Teti D. 2005. Prostaglandin E2 induces interleukin-8 gene transcription by activating C/EBP homologous protein in human T lymphocytes. J. Biol. Chem. 280:14433-14442. http://dx.doi.org/10.1074/jbc. M410725200.
4. Tavakoli S, Cowan MJ, Benfield T, Logun C, Shelhamer JH. 2001. Prostaglandin E (2)-induced interleukin-6 release by a human airway epithelial cell line. Am. J. Physiol. Lung Cell. Mol. Physiol. 280:L127-L133.
5. Tager AM, Bromley SK, Medoff BD, Islam SA, Bercury SD, Friedrich EB, Carafone AD, Gerszten RE, Luster AD. 2003. Leukotriene B4 receptor BLT1 mediates early effectorT cell recruitment. Nat. Immunol. 4:982-990. http://dx.doi.org/ 10.1038/ni970.
6. Miyahara N, Ohnishi H, Matsuda H, Miyahara S, Takeda K, Koya T, Matsubara S, Okamoto M, Dakhama A, Haribabu B, Gelfand EW. 2008. Leukotriene B4 receptor 1 expression on dendritic cells is required for the developmentof Th2 responses and allergen-induced airway hyperresponsiveness. J. Immunol. 181:1170-1178. http://dx.doi.org/10.4049/jimmunol.181.2.1170.
7. 4, increase the release of mucus from human airways in vitro. Am. Rev. Respir. Dis. 126:449-451.
8. Canetti C, Silva JS, Ferreira SH, Cunha FQ. 2001. Tumour necrosis factor-alpha and leukotriene B (4) mediate the neutrophil migration in immune inflammation. Br. J. Pharmacol. 134:1619-1628. http://dx.doi.org/10.1038/sj.bjp. 0704403.
9. 4. Int. J. Biochem. Cell Biol. 30:173-178. http://dx.doi.org/10.1016/S1357-2725 (97) 00123-4.
10. Lewis RA, Austen KF, Soberman RJ. 1990. Leukotrienes and other products of the 5-lipoxygenase pathway. Biochemistry and relation to pathobiology in human diseases. N. Engl. J. Med. 323:645-655.
11. Hopkins H, Stull T, Von Essen SG, Robbins RA, Rennard SI. 1989. Neutrophil chemotactic factors in bacterial pneumonia. Chest 95:1021-1027. http://dx.doi.org/10.1378/chest.95.5.1021.
12. Poon IK, Lucas CD, Rossi AG, Ravichandran KS. 2014. Apoptotic cell clearance: basic biology and therapeutic potential. Nat. Rev. Immunol. 14:166-180. http://dx.doi.org/10.1038/nri3607.
13. Serhan CN, Krishnamoorthy S, Recchiuti A, Chiang N. 2011. Novel antiinflammatory-pro-resolving mediators and their receptors. Curr. Top. Med. Chem. 11:629-647. http://dx.doi.org/10.2174/1568026611109060629.
14. Whiteley LO, Maheswaran SK, Weiss DJ, Ames TR, Kannan MS. 1992. Pasteurella haemolytica A1 and bovine respiratory disease: pathogenesis. J. Vet. Intern. Med. 6:11-22. http://dx.doi.org/10.1111/j.1939-1676.1992.tb00980.x.
15. Hsuan SL, Kannan MS, Jeyaseelan S, Prakash YS, Malazdrewich C, Abrahamsen MS, Sieck GC, Maheswaran SK. 1999. Pasteurella haemolytica leukotoxin and endotoxin induced cytokine gene expression in bovine alveolar macrophages requires NF-kappaB activation and calcium elevation. Microb. Pathog. 26:263-273. http://dx.doi.org/10.1006/mpat.1998.0271.
16. Buret AG. 2010. Immuno-modulation and anti-inflammatory benefits of antibiotics: the example of tilmicosin. Can. J. Vet. Res. 74:1-10.
17. Good JT, Jr, Rollins DR, Martin RJ. 2012. Macrolides in the treatment of asthma. Curr. Opin. Pulm. Med. 18:76-84. http://dx.doi.org/10.1097/MCP. 0b013e32834daff8.
18. McArdle JR, Talwalkar JS. 2007. Macrolides in cystic fibrosis. Clin. Chest Med. 28:347-360. http://dx.doi.org/10.1016/j.ccm.2007.02.005.
19. Falcó V, Sánchez A, Pahissa A, Rello J. 2011. Emerging drugs for pneumococcal pneumonia. Expert Opin. Emerg. Drugs 16:459-477. http://dx.doi.org/10.1517/14728214.2011.576669.
20. Frank MO, Sullivan GW, Carper HT, Mandell GL. 1992. In vitro demonstration of transport and delivery of antibiotics by polymorphonuclear leukocytes. Antimicrob. Agents Chemother. 36:2584-2588. http://dx.doi.org/10. 1128/AAC.36.12.2584.
21. Gladue RP, Bright GM, Isaacson RE, Newborg MF. 1989. In vitro and in vivo uptake of azithromycin (CP-62, 993) by phagocytic cells: possible mechanism ofdelivery and releaseatsitesofinfection. Antimicrob. Agents Chemother. 33:277-282. http://dx.doi.org/10.1128/AAC.33.3.277.
22. Anderson N, Borlak J. 2006. Drug-induced phospholipidosis. FEBS Lett. 580:5533-5540. http://dx.doi.org/10.1016/j.febslet.2006.08.061.
23. Van Bambeke F, Gerbaux C, Michot JM, D'Yvoire MB, Montenez JP, Tulkens PM. 1998. Lysosomal alterations induced in cultured rat fibroblasts by long-term exposure to low concentrations of azithromycin. J. Antimicrob. Chemother. 42:761-767. http://dx.doi.org/10.1093/jac/42.6.761.
24. Munic V, Banjanac M, Koštrun S, Nujić K, Bosnar M, Marjanović N, Ralić J, Matijašić M, Hlevnjak M, Eraković Haber V. 2011. Intensity of macrolide anti-inflammatory activity in J774A.1 cells positively correlates with cellular accumulation and phospholipidosis. Pharmacol. Res. 64:298-307. http://dx.doi.org/10.1016/j.phrs. 2011.03.011.
25. Montenez JP, Van Bambeke F, Piret J, Brasseur R, Tulkens PM, Mingeot-Leclercq MP. 1999. Interactions of macrolide antibiotics (erythromycin A, roxithromycin, erythromycylamine [dirithromycin], and azithromycin) with phospholipids: computer-aided conformational analysis and studies on acellular and cell culture models. Toxicol. Appl. Pharmacol. 156:129-140. http://dx.doi.org/10.1006/taap. 1999.8632.
26. Evans NA. 2005. Tulathromycin: an overview of a new triamilide antibiotic for livestock respiratory disease. Vet. Ther. 6:83-95.
27. Rooney KA, Nutsch RG, Skogerboe TL, Weigel DJ, Gajewski K, Kilgore WR. 2005. Efficacy of tulathromycin compared with tilmicosin and florfenicol for the control of respiratory disease in cattle at high risk of developing bovine respiratory disease. Vet. Ther. 6:154-166.
28. Fischer CD, Beatty JK, Zvaigzne CG, Morck DW, Lucas MJ, Buret AG. 2011. Anti-inflammatory benefits of antibiotic-induced neutrophil apoptosis: tulathromycin induces caspase-3-dependent neutrophil programmed cell death and inhibits NF-kappaB signaling and CXCL8 transcription. Antimicrob. Agents Chemother. 55:338-348. http://dx.doi.org/10.1128/AAC.01052-10.
29. Fischer CD, Beatty JK, Duquette SC, Morck DW, Lucas MJ, Buret AG. 2013. Direct and indirect anti-inflammatory effects of tulathromycin in bovine macrophages: inhibition of CXCL-8 secretion, induction of apoptosis, and promotion of efferocytosis. Antimicrob. Agents Chemother. 57:1385-1393. http://dx.doi.org/10.1128/AAC.01598-12.
30. Chin AC, Morck DW, Merrill JK, Ceri H, Olson ME, Read RR, Dick P, Buret AG. 1998. Anti-inflammatory benefits of tilmicosin in calves with Pasteurella haemolytica-infected lungs. Am. J. Vet. Res. 59:765-771.
31. Takeuchi K, Umeki Y, Matsumoto N, Yamamoto K, Yoshida M, Suzuki K, Aratani Y. 2012. Severe neutrophil-mediated lung inflammation in myeloperoxidase-deficient mice exposed to zymosan. Inflamm. Res. 61:197-205. http://dx.doi.org/10.1007/s00011-011-0401-y.
32. Mollay C, Kreil G. 1974. Enhancement of bee venom phospholipase A2 activity by melittin, direct lytic factor from cobra venom and polymyxin B. FEBS Lett. 46:141-144. http://dx.doi.org/10.1016/0014-5793 (74) 80354-6.
33. Lee SY, Oh JY, Lee MJ, Jang MJ, Park HY, Kim JW, Min DS, Park YM, Chang YC, Bae YS, Kwak JY. 2004. Anti-apoptotic mechanism and reduced expression of phospholipase D in spontaneous and Fasstimulated apoptosis of human neutrophils. Eur. J. Immunol. 34:2760-2770. http://dx.doi.org/10.1002/eji.200425117.
34. Doerschuk CM, Tasaka S, Wang Q. 2000. CD11/CD18-dependent and -independent neutrophil emigration in the lungs: how do neutrophils know which route to take? Am. J. Respir. Cell Mol. Biol. 23:133-136. http://dx.doi.org/10. 1165/ajrcmb.23.2.f193.
35. Claesson HE, Odlander B, Jakobsson PJ. 1992. Leukotriene B4 in the immune system. Int. J. Immunopharmacol. 14:441-449. http://dx.doi.org/10.1016/0192- 0561 (92) 90174-J.
36. Marshall J, Krump E, Lindsay T, Downey G, Ford DA, Zhu P, Walker P, Rubin B. 2000. Involvement of cytosolic phospholipase A2 and secretory phospholipase A2 in arachidonic acid release from human neutrophils. J. Immunol. 164:2084-2091. http://dx.doi.org/10.4049/jimmunol.164.4.2084.
37. Degousee N, Ghomashchi F, Stefanski E, Singer A, Smart BP, Borregaard N, Reithmeier R, Lindsay TF, Lichtenberger C, Reinisch W, Lambeau G, Arm J, Tischfield J, Gelb MH, Rubin BB. 2002. Groups IV, V, and X phospholipases A2s in human neutrophils: role in eicosanoid production and Gram-negative bacterial phospholipid hydrolysis. J. Biol. Chem. 277:5061-5073. http://dx.doi.org/10. 1074/jbc. M109083200.
38. Petrin D, Turcotte S, Gilbert AK, Rola-Pleszczynski M, Stankova J. 2006. The anti-apoptotic effect of leukotriene B4 in neutrophils: a role for phosphatidylinositol 3-kinase, extracellular signal-regulated kinase and Mcl-1. Cell. Signal. 18:479-487. http://dx.doi.org/10.1016/j.cellsig.2005.05.021.
39. O'Flaherty JT, Kreutzer DL, Ward PA. 1979. Effect of prostaglandins E1, E2 and F2alpha on neutrophil aggregation. Prostaglandins 17:201-210.
40. Pouliot M, Fiset ME, Massé M, Naccache PH, Borgeat P. 2002. Adenosine up-regulates cyclooxygenase-2 in human granulocytes: impact on the balance of eicosanoid generation. J. Immunol. 169:5279-5286. http://dx.doi.org/10.4049/jimmunol.169.9.5279.
41. Vancheri C, Mastruzzo C, Sortino MA, Crimi N. 2004. The lung as a privileged site for the beneficial actions of PGE2. Trends Immunol. 25:40-46. http://dx.doi.org/10.1016/j.it.2003.11.001.
42. Medeiros AI, Serezani CH, Lee SP, Peters-Golden M. 2009. Efferocytosis impairs pulmonary macrophage and lung antibacterial function via PGE2/EP2 signaling. J. Exp. Med. 206:61-68. http://dx.doi.org/10.1084/jem.20082058.
43. Hung ND, Kim MR, Sok DE. 2011. Oral administration of 2-docosahexaenoyl lysophosphatidylcholine displayed anti-inflammatory effects on zymosan A-induced peritonitis. Inflammation 34:147-160. http://dx.doi.org/10.1007/s10753-010- 9218-z.
44. Griffiths RJ, Li SW, Wood BE, Blackham A. 1991. A comparison of the anti-inflammatory activity of selective 5-lipoxygenase inhibitors with dexamethasone and colchicine in a model of zymosan induced inflammationinthe rat knee joint and peritoneal cavity. Agents Actions 32:312-320. http://dx.doi.org/10.1007/BF01980892.
45. Leypoldt JK, Kamerath CD, Gilson JF. 2007. Acute peritonitis in a C57BL/6 mouse model of peritoneal dialysis. Adv. Perit. Dial. 23:66-70.
46. Tolone G, Bonasera L, Brai M, Tolone C. 1977. Prostaglandin production by human polymorphonuclear leucocytes during phagocytosis in vitro. Experientia 33:961-962. http://dx.doi.org/10.1007/BF01951305.
47. Lakritz J, Tyler JW, Marsh AE, Romesburg-Cockrell M, Smith K, Holle JM. 2002. Tilmicosin reduces lipopolysaccharide-stimulated bovine alveolar macrophage prostaglandin E (2) production via a mechanism involving phospholipases. Vet. Ther. 3:7-21.
48. Cao XY, Dong M, Shen JZ, Wu BB, Wu CM, Du XD, Wang Z, Qi YT, Li BY. 2006. Tilmicosin and tylosin have anti-inflammatory properties via modulation of COX-2 and iNOS gene expression and production of cytokines in LPS-induced macrophages and monocytes. Int. J. Antimicrob. Agents 27:431-438. http://dx.doi.org/10.1016/j.ijantimicag.2005.12.010.
49. Gilroy DW, Newson J, Sawmynaden P, Willoughby DA, Croxtall JD. 2004. A novel role for phospholipase A2 isoforms in the checkpoint control of acute inflammation. FASEB J. 18:489-498. http://dx.doi.org/10.1096/fj.03-0837com.
50. Levy BD, Clish CB, Schmidt B, Gronert K, Serhan CN. 2001. Lipid mediator class switching during acute inflammation: signals in resolution. Nat. Immunol. 2:612-619. http://dx.doi.org/10.1038/89759.
51. Takata S, Papayianni A, Matsubara M, Jimenez W, Pronovost PH, Brady HR. 1994. 15-Hydroxyeicosatetraenoic acid inhibits neutrophil migration across cytokine-activated endothelium. Am. J. Pathol. 145:541-549.
52. Smith RJ, Justen JM, Nidy EG, Sam LM, Bleasdale JE. 1993. Transmembrane signaling in human polymorphonuclear neutrophils: 15 (S) - hydroxy-(5Z, 8Z, 11Z, 13E)-eicosatetraenoic acid modulates receptor agonist-triggered cell activation. Proc. Natl. Acad. Sci. U. S. A. 90:7270-7274. http://dx.doi.org/10. 1073/pnas.90.15.7270.
53. Johnson HG, McNee ML, Sun FF. 1985. 15-Hydroxyeicosatetraenoic acid is a potent inflammatory mediator and agonist of canine tracheal mucus secretion. Am. Rev. Respir. Dis. 131:917-922.
54. Melendez AJ, Bruetschy L, Floto RA, Harnett MM, Allen JM. 2001. Functional coupling of FcgammaRItonicotinamide adenine dinucleotide phosphate (reduced form) oxidative burst and immune complex trafficking requires the activation of phospholipase D1. Blood 98:3421-3428. http://dx.doi.org/10.1182/ blood. V98.12.3421.
55. Hitomi T, Zhang J, Nicoletti LM, Grodzki AC, Jamur MC, Oliver C, Siraganian RP. 2004. Phospholipase D1 regulates high-affinity IgE receptor-induced mast cell degranulation. Blood 104:4122-4128. http://dx.doi.org/10.1182/blood-2004-06-2091.
56. Lehman N, Di Fulvio M, McCray N, Campos I, Tabatabaian F, Gomez-Cambronero J. 2006. Phagocyte cell migration is mediated by phospholipases PLD1 and PLD2. Blood 108:3564-3572. http://dx.doi.org/10.1182/blood-2006-02- 005959.
57. Brown GB, Roth JA. 1991. Comparison of the response of bovine and human neutrophils to various stimuli. Vet. Immunol. Immunopathol. 28:201-218. http://dx.doi.org/10.1016/0165-2427 (91) 90115-S.
58. Ahmed M, Kimura K, Soliman M, Yamaji D, Okamatsu-Ogura Y, Makondo K, Inanami O, Saito M. 2007. Effects of leptin and tumor necrosis factor-alpha on degranulation and superoxide production of polymorphonuclear neutrophils from Holstein cows. J. Vet. Med. Sci. 69:125-131. http://dx.doi.org/10.1292/jvms.69. 125.
59. Abdelghaffar H, Vazifeh D, Labro MT. 1997. Erythromycin A-derived macrolides modify the functional activities of human neutrophils by altering the phospholipase D-phosphatidate phosphohydrolase transduction pathway: L-cladinose is involved both in alterations of neutrophil functions and modulation of this transductional pathway. J. Immunol. 159:3995-4005.
60. Levy BD, Hickey L, Morris AJ, Larvie M, Keledjian R, Petasis NA, Bannenberg G, Serhan CN. 2005. Novel polyisoprenyl phosphates block phospholipase D and human neutrophil activation in vitro and murine peritoneal inflammation in vivo. Br. J. Pharmacol. 146:344-351. http://dx.doi.org/10.1038/ sj.bjp. 0706338.
61. Wang Z, Clarke CR, Clinkenbeard KD. 1999. Role of phospholipase D in Pasteurella haemolytica leukotoxin-induced increase in phospholipase A (2) activity in bovine neutrophils. Infect. Immun. 67:3768-3772.
62. Bosnar M, Kelneric Z, Munic V, Erakovic V, Parnham MJ. 2005. Cellular uptake and efflux of azithromycin, erythromycin, clarithromycin, telithromycin, and cethromycin. Antimicrob. Agents Chemother. 49:2372-2377. http://dx.doi.org/10.1128/AAC.49.6.2372-2377.2005.
63. Van Bambeke F, Montenez JP, Piret J, Tulkens PM, Courtoy PJ, Mingeot-Leclercq MP. 1996. Interaction of the macrolide azithromycin with phospholipids. I. Inhibition of lysosomal phospholipase A1 activity. Eur. J. Pharmacol. 314:203-214.
64. Banjanac M, Munic Kos V, Nujic K, Vrancic M, Belamaric D, Crnkovic S, Hlevnjak M, Erakovic Haber V. 2012. Anti-inflammatory mechanism of action of azithromycin in LPS-stimulated J774A.1 cells. Pharmacol. Res. 66:357-362. http://dx.doi.org/10.1016/j.phrs.2012.06.011.
65. Piccotti JR, La Gattuta MS, Knight SA, Gonzales AJ, Bleavins MR. 2005. Induction of apoptosis by cationic amphiphilic drugs amiodarone and imipramine. Drug Chem. Toxicol. 28:117-133. http://dx.doi.org/10.1081/DCT-39743.