Francisella tularensis LVS induction of prostaglandin biosynthesis by infected macrophages requires specific host phospholipases and lipid phosphatases

Infection and Immunity

Volumn 82, Issue 8, 2014, Pages 3299-3311

  Navratil, Aaron R ^a   Brummett, Ashley M ^a   Bryan, Joshua D ^a   Woolard, Matthew D ^a  

^a LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARACHIDONIC ACID; CYCLOOXYGENASE 2; CYTOSOLIC PHOSPHOLIPASE A2; LIPOPROTEIN LIPASE; PHOSPHATIDATE PHOSPHATASE; PHOSPHOLIPASE; PHOSPHOLIPASE C; PHOSPHOLIPASE D; PHOSPHOLIPID; PROSTAGLANDIN E SYNTHASE 1; PROSTAGLANDIN E2;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CYTOKINE RESPONSE; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ENZYME REGULATION; FEMALE; HOST CELL; INFLAMMATION; MACROPHAGE; MACROPHAGE ACTIVATION; MACROPHAGE FUNCTION; MOUSE; NONHUMAN; PHOSPHOLIPID MEMBRANE; PRIORITY JOURNAL; PROSTAGLANDIN SYNTHESIS; TULAREMIA; WESTERN BLOTTING;

ANIMALS; DINOPROSTONE; FEMALE; FRANCISELLA TULARENSIS; HUMANS; LIPOPROTEIN LIPASE; MACROPHAGES; MICE; MICE, INBRED C57BL; NUCLEAR PROTEINS; PHOSPHATIDATE PHOSPHATASE; PHOSPHOLIPASE D;

EID: 84904735652     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.02060-14     Document Type: Article

References (65)

1. Dienst FT, Jr. 1963. Tularemia: a perusal of three hundred thirty-nine cases. J. La. State Med. Soc. 115:114-127.
2. Saslaw S, Eigelsbach HT, Prior JA, Wilson HE, Carhart S. 1961. Tularemia vaccine study. II. Respiratory challenge. Arch. Intern. Med. 107: 702-714.
3. Dennis DT, Inglesby TV, Henderson DA, Bartlett JG, Ascher MS, Eitzen E, Fine AD, Friedlander AM, Hauer J, Layton M, Lillibridge SR, McDade JE, Osterholm MT, O'Toole T, Parker G, Perl TM, Russell PK, Tonat K. 2001. Tularemia as a biological weapon: medical and public health management. JAMA 285:2763-2773. http://dx.doi.org/10.1001 /jama.285.21.2763.
4. Gallagher-Smith M, Kim J, Al-Bawardy R, Josko D. 2004. Francisella tularensis: possible agent in bioterrorism. Clin. Lab. Sci. 17:35-39.
5. Baron GS, Nano FE. 1998. MglA and MglB are required for the intramacrophage growth of Francisella novicida. Mol. Microbiol. 29:247-259. http: //dx.doi.org/10.1046/j.1365-2958.1998.00926.x.
6. Barrigan LM, Tuladhar S, Brunton JC, Woolard MD, Chen CJ, Saini D, Frothingham R, Sempowski GD, Kawula TH, Frelinger JA. 2013. Infection with Francisella tularensis LVS clpB leads to an altered yet protective immune response. Infect. Immun. 81:2028-2042. http://dx.doi.org /10.1128/IAI.00207-13.
7. Jones CL, Napier BA, Sampson TR, Llewellyn AC, Schroeder MR, Weiss DS. 2012. Subversion of host recognition and defense systems by Francisella spp. Microbiol. Mol. Biol. Rev. 76:383-404. http://dx.doi.org /10.1128/MMBR.05027-11.
8. Woolard MD, Wilson JE, Hensley LL, Jania LA, Kawula TH, Drake JR, Frelinger JA. 2007. Francisella tularensis-infected macrophages release prostaglandin E2 that blocks T cell proliferation and promotes a Th2-like response. J. Immunol. 178:2065-2074. http://dx.doi.org/10.4049/jimmunol .178.4.2065.
9. Woolard MD, Barrigan LM, Fuller JR, Buntzman AS, Bryan J, Manoil C, Kawula TH, Frelinger JA. 2013. Identification of Francisella novicida mutants that fail to induce prostaglandin E(2) synthesis by infected macrophages. Front. Microbiol. 4:16. http://dx.doi.org/10.3389/fmicb.2013 .00016.
10. Walker C, Kristensen F, Bettens F, deWeck AL. 1983. Lymphokine regulation of activated (G1) lymphocytes. I. Prostaglandin E2-induced inhibition of interleukin 2 production. J. Immunol. 130:1770-1773.
11. Garcia-Penarrubia P, Bankhurst AD, Koster FT. 1989. Prostaglandins from human T suppressor/cytotoxic cells modulate natural killer antibacterial activity. J. Exp. Med. 170:601-606. http://dx.doi.org/10.1084/jem .170.2.601.
12. Woolard MD, Hensley LL, Kawula TH, Frelinger JA. 2008. Respiratory Francisella tularensis live vaccine strain infection induces Th17 cells and prostaglandin E2, which inhibits generation of gamma interferon-positive T cells. Infect. Immun. 76:2651-2659. http://dx.doi.org/10.1128/IAI .01412-07.
13. Elkins KL, Rhinehart-Jones TR, Culkin SJ, Yee D, Winegar RK. 1996. Minimal requirements for murine resistance to infection with Francisella tularensis LVS. Infect. Immun. 64:3288-3293.
14. Fortier AH, Polsinelli T, Green SJ, Nacy CA. 1992. Activation of macrophages for destruction of Francisella tularensis: identification of cytokines, effector cells, and effector molecules. Infect. Immun. 60:817-825.
15. Wilson JE, Katkere B, Drake JR. 2009. Francisella tularensis induces ubiquitin-dependent major histocompatibility complex class II degradation in activated macrophages. Infect. Immun. 77:4953-4965. http://dx .doi.org/10.1128/IAI.00844-09.
16. Qi HY, Shelhamer JH. 2005. Toll-like receptor 4 signaling regulates cytosolic phospholipase A2 activation and lipid generation in lipopolysaccharide-stimulated macrophages. J. Biol. Chem. 280:38969-38975. http: //dx.doi.org/10.1074/jbc.M509352200.
17. Hamberg M, Samuelsson B. 1973. Detection and isolation of an endoperoxide intermediate in prostaglandin biosynthesis. Proc. Natl. Acad. Sci. U. S. A. 70:899-903. http://dx.doi.org/10.1073/pnas.70.3.899.
18. Brummett AM, Navratil AR, Bryan JD, Woolard MD. 16 December 2013. Janus kinase 3 activity is necessary for the phosphorylation of cytosolic phospholipase A2 and prostaglandin E2 synthesis by macrophages infected with Francisella tularensis live vaccine strain. Infect. Immun. http://dx.doi.org/10.1128/IAI.01461-13.
19. Allen AC, Gammon CM, Ousley AH, McCarthy KD, Morell P. 1992. Bradykinin stimulates arachidonic acid release through the sequential actions of an sn-1 diacylglycerol lipase and a monoacylglycerol lipase. J. Neurochem. 58:1130-1139. http://dx.doi.org/10.1111/j.1471-4159.1992 .tb09372.x.
20. Morell P, Allen AC, Gammon CM, Lyons SA. 1991. Arachidonate release consequent to bradykinin-stimulated phospholipid metabolism in dorsal root ganglion cells. Biochem. Soc. Trans. 19:411-416.
21. Bisogno T, Howell F, Williams G, Minassi A, Cascio MG, Ligresti A, Matias I, Schiano-Moriello A, Paul P, Williams EJ, Gangadharan U, Hobbs C, Di Marzo V, Doherty P. 2003. Cloning of the first sn1-DAG lipases points to the spatial and temporal regulation of endocannabinoid signaling in the brain. J. Cell Biol. 163:463-468. http://dx.doi.org/10.1083 /jcb.200305129.
22. Kai M, Wada I, Imai S, Sakane F, Kanoh H. 1997. Cloning and characterization of two human isozymes of Mg2_-independent phosphatidic acid phosphatase. J. Biol. Chem. 272:24572-24578. http://dx.doi.org/10 .1074/jbc.272.39.24572.
23. Hefner Y, Borsch-Haubold AG, Murakami M, Wilde JI, Pasquet S, Schieltz D, Ghomashchi F, Yates JR, III, Armstrong CG, Paterson A, Cohen P, Fukunaga R, Hunter T, Kudo I, Watson SP, Gelb MH. 2000. Serine 727 phosphorylation and activation of cytosolic phospholipase A2 by MNK1-related protein kinases. J. Biol. Chem. 275:37542-37551. http: //dx.doi.org/10.1074/jbc.M003395200.
24. Scott SA, Selvy PE, Buck JR, Cho HP, Criswell TL, Thomas AL, Armstrong MD, Arteaga CL, Lindsley CW, Brown HA. 2009. Design of isoform-selective phospholipase D inhibitors that modulate cancer cell invasiveness. Nat. Chem. Biol. 5:108-117. http://dx.doi.org/10.1038 /nchembio.140.
25. Stella N, Schweitzer P, Piomelli D. 1997. A second endogenous cannabinoid that modulates long-term potentiation. Nature 388:773-778. http: //dx.doi.org/10.1038/42015.
26. Pappu AS, Hauser G. 1983. Propranolol-induced inhibition of rat brain cytoplasmic phosphatidate phosphohydrolase. Neurochem. Res. 8:1565- 1575. http://dx.doi.org/10.1007/BF00964158.
27. Kusner DJ, Hall CF, Schlesinger LS. 1996. Activation of phospholipase D is tightly coupled to the phagocytosis of Mycobacterium tuberculosis or opsonized zymosan by human macrophages. J. Exp. Med. 184:585-595. http://dx.doi.org/10.1084/jem.184.2.585.
28. Ali WH, Chen Q, Delgiorno KE, Su W, Hall JC, Hongu T, Tian H, Kanaho Y, Di Paolo G, Crawford HC, Frohman MA. 2013. Deficiencies of the lipid-signaling enzymes phospholipase D1 and D2 alter cytoskeletal organization, macrophage phagocytosis, and cytokine-stimulated neutrophil recruitment. PLoS One 8:e55325. http://dx.doi.org/10.1371/journal .pone.0055325.
29. Lai XH, Golovliov I, Sjostedt A. 2001. Francisella tularensis induces cytopathogenicity and apoptosis in murine macrophages via a mechanism that requires intracellular bacterial multiplication. Infect. Immun. 69: 4691-4694. http://dx.doi.org/10.1128/IAI.69.7.4691-4694.2001.
30. Shibata Y. 1995. Prostaglandin E2 release triggered by phagocytosis of latex particles. A distinct association with prostaglandin synthase isozymes in bone marrow macrophages. J. Immunol. 154:2878-2887.
31. Lasa M, Mahtani KR, Finch A, Brewer G, Saklatvala J, Clark AR. 2000. Regulation of cyclooxygenase 2 mRNA stability by the mitogen-activated protein kinase p38 signaling cascade. Mol. Cell. Biol. 20:4265-4274. http: //dx.doi.org/10.1128/MCB.20.12.4265-4274.2000.
32. D'Acquisto F, Iuvone T, Rombola L, Sautebin L, Di Rosa M, Carnuccio R. 1997. Involvement of NF-kappaB in the regulation of cyclooxygenase-2 protein expression in LPS-stimulated J774 macrophages. FEBS Lett. 418: 175-178. http://dx.doi.org/10.1016/S0014-5793(97)01377-X.
33. Grkovich A, Johnson CA, Buczynski MW, Dennis EA. 2006. Lipopolysaccharide-induced cyclooxygenase-2 expression in human U937 macrophages is phosphatidic acid phosphohydrolase-1-dependent. J. Biol. Chem. 281:32978-32987. http://dx.doi.org/10.1074/jbc.M605935200.
34. Paranavitana C, Pittman P, Velauthapillai M, DaSilva L. 2008. Temporal cytokine profiling of Francisella tularensis-infected human peripheral blood mononuclear cells. J. Microbiol. Immunol. Infect. 41:192-199. http://dx.doi.org/10.1111/2049-632X.12113.
35. Carman GM. 2006. Roles of phosphatidate phosphatase enzymes in lipid metabolism. Trends Biochem. Sci. 31:694-699. http://dx.doi.org/10.1016 /j.tibs.2006.10.003.
36. Barrett AM, Cullum VA. 1968. The biological properties of the optical isomers of propranolol and their effects on cardiac arrhythmias. Br. J. Pharmacol. 34:43-55. http://dx.doi.org/10.1111/j.1476-5381.1968.tb07949.x.
37. Roberts R, Sciorra VA, Morris AJ. 1998. Human type 2 phosphatidic acid phosphohydrolases. Substrate specificity of the type 2a, 2b, and 2c enzymes and cell surface activity of the 2a isoform. J. Biol. Chem. 273: 22059-22067.
38. Nanjundan M, Possmayer F. 2003. Pulmonary phosphatidic acid phosphatase and lipid phosphate phosphohydrolase. Am. J. Physiol. Lung Cell. Mol. Physiol. 284:L1-L23.
39. Roberts RZ, Morris AJ. 2000. Role of phosphatidic acid phosphatase 2a in uptake of extracellular lipid phosphate mediators. Biochim. Biophys. Acta 1487:33-49. http://dx.doi.org/10.1016/S1388-1981(00)00081-0.
40. Valdearcos M, Esquinas E, Meana C, Pena L, Gil-de-Gomez L, Balsinde J, Balboa MA. 2012. Lipin-2 reduces proinflammatory signaling induced by saturated fatty acids in macrophages. J. Biol. Chem. 287:10894-10904. http://dx.doi.org/10.1074/jbc.M112.342915.
41. Petit JC, Richard G, Burghoffer B, Daguet GL. 1985. Suppression of cellular immunity to Listeria monocytogenes by activated macrophages: mediation by prostaglandins. Infect. Immun. 49:383-388.
42. Koster FT, Williams JC, Goodwin JS. 1985. Cellular immunity in Q fever: specific lymphocyte unresponsiveness in Q fever endocarditis. J. Infect. Dis. 152:1283-1289. http://dx.doi.org/10.1093/infdis/152.6.1283.
43. Edwards CK, III, Hedegaard HB, Zlotnik A, Gangadharam PR, Johnston RB, Jr, Pabst MJ. 1986. Chronic infection due to Mycobacterium intracellulare in mice: association with macrophage release of prostaglandin E2 and reversal by injection of indomethacin, muramyl dipeptide, or interferon-gamma. J. Immunol. 136:1820-1827.
44. Felts RL, Reilly TJ, Tanner JJ. 2006. Structure of Francisella tularensis AcpA: prototype of a unique superfamily of acid phosphatases and phospholipases C. J. Biol. Chem. 281:30289-30298. http://dx.doi.org/10.1074 /jbc.M606391200.
45. Gijon MA, Spencer DM, Siddiqi AR, Bonventre JV, Leslie CC. 2000. Cytosolic phospholipase A2 is required for macrophage arachidonic acid release by agonists that do and do not mobilize calcium. Novel role of mitogen-activated protein kinase pathways in cytosolic phospholipase A2 regulation. J. Biol. Chem. 275:20146-20156. http://dx.doi.org/10.1074 /jbc.M908941199.
46. Astudillo AM, Perez-Chacon G, Meana C, Balgoma D, Pol A, Del Pozo MA, Balboa MA, Balsinde J. 2011. Altered arachidonate distribution in macrophages from caveolin-1 null mice leading to reduced eicosanoid synthesis. J. Biol. Chem. 286:35299-35307. http://dx.doi.org/10.1074/jbc .M111.277137.
47. Perez-Chacon G, Astudillo AM, Balgoma D, Balboa MA, Balsinde J. 2009. Control of free arachidonic acid levels by phospholipases A2 and lysophospholipid acyltransferases. Biochim. Biophys. Acta 1791:1103- 1113. http://dx.doi.org/10.1016/j.bbalip.2009.08.007.
48. Chilton FH, Fonteh AN, Surette ME, Triggiani M, Winkler JD. 1996. Control of arachidonate levels within inflammatory cells. Biochim. Biophys. Acta 1299:1-15. http://dx.doi.org/10.1016/0005-2760(95)00169-7.
49. Kozak KR, Rowlinson SW, Marnett LJ. 2000. Oxygenation of the endocannabinoid, 2-arachidonylglycerol, to glyceryl prostaglandins by cyclooxygenase- J. Biol. Chem. 275:33744-33749. http://dx.doi.org/10.1074 /jbc.M007088200.
50. Hu SS, Bradshaw HB, Chen JS, Tan B, Walker JM. 2008. Prostaglandin E2 glycerol ester, an endogenous COX-2 metabolite of 2-arachidonoylglycerol, induces hyperalgesia and modulates NFkappaB activity. Br. J. Pharmacol. 153:1538-1549. http://dx.doi.org/10.1038/bjp.2008.33.
51. Rola-Pleszczynski M, Gagnon L, Chavaillaz PA. 1988. Immune regulation by leukotriene B4. Ann. N. Y. Acad. Sci. 524:218-226. http://dx.doi .org/10.1111/j.1749-6632.1988.tb38545.x.
52. Rola-Pleszczynski M, Stankova J. 1992. Leukotriene B4 enhances interleukin-6 (IL-6) production and IL-6 messenger RNA accumulation in human monocytes in vitro: transcriptional and posttranscriptional mechanisms. Blood 80:1004-1011.
53. Kim HB, Kumar A, Wang L, Liu GH, Keller SR, Lawrence JC, Jr, Finck BN, Harris TE. 2010. Lipin 1 represses NFATc4 transcriptional activity in adipocytes to inhibit secretion of inflammatory factors. Mol. Cell. Biol. 30:3126-3139. http://dx.doi.org/10.1128/MCB.01671-09.
54. Finck BN, Gropler MC, Chen Z, Leone TC, Croce MA, Harris TE, Lawrence JC, Jr, Kelly DP. 2006. Lipin 1 is an inducible amplifier of the hepatic PGC-1alpha/PPARalpha regulatory pathway. Cell Metab. 4:199- 210. http://dx.doi.org/10.1016/j.cmet.2006.08.005.
55. Peterfy M, Phan J, Xu P, Reue K. 2001. Lipodystrophy in the fld mouse results from mutation of a new gene encoding a nuclear protein, lipin. Nat. Genet. 27:121-124. http://dx.doi.org/10.1038/83685.
56. Valdearcos M, Esquinas E, Meana C, Gil-de-Gomez L, Guijas C, Balsinde J, Balboa MA. 2011. Subcellular localization and role of lipin-1 in human macrophages. J. Immunol. 186:6004-6013. http://dx.doi.org/10 .4049/jimmunol.1003279.
57. Sands WA, Clark JS, Liew FY. 1994. The role of a phosphatidylcholinespecific phospholipase C in the production of diacylglycerol for nitric oxide synthesis in macrophages activated by IFN-gamma and LPS. Biochem. Biophys. Res. Commun. 199:461-466. http://dx.doi.org/10 .1006/bbrc.1994.1251.
58. Pettus BJ, Bielawski J, Porcelli AM, Reames DL, Johnson KR, Morrow J, Chalfant CE, Obeid LM, Hannun YA. 2003. The sphingosine kinase 1/sphingosine-1-phosphate pathway mediates COX-2 induction and PGE2 production in response to TNF-alpha. FASEB J. 17:1411-1421. http: //dx.doi.org/10.1096/fj.02-1038com.
59. McQuiston T, Luberto C, Del Poeta M. 2010. Role of host sphingosine kinase 1 in the lung response against Cryptococcosis. Infect. Immun. 78: 2342-2352. http://dx.doi.org/10.1128/IAI.01140-09.
60. Duong CQ, Bared SM, Abu-Khader A, Buechler C, Schmitz A, Schmitz G. 2004. Expression of the lysophospholipid receptor family and investigation of lysophospholipid-mediated responses in human macrophages. Biochim. Biophys. Acta 1682:112-119. http://dx.doi.org/10.1016/j.bbalip .2004.03.002.
61. Hammad SM, Crellin HG, Wu BX, Melton J, Anelli V, Obeid LM. 2008. Dual and distinct roles for sphingosine kinase 1 and sphingosine 1 phosphate in the response to inflammatory stimuli in RAW macrophages. Prostaglandins Other Lipid Mediat. 85:107-114. http://dx.doi.org/10 .1016/j.prostaglandins.2007.11.002.
62. Fueller M, Wang DA, Tigyi G, Siess W. 2003. Activation of human monocytic cells by lysophosphatidic acid and sphingosine-1-phosphate. Cell. Signal. 15:367-375. http://dx.doi.org/10.1016/S0898-6568(02)00117-1.
63. Fan H, Zingarelli B, Harris V, Tempel GE, Halushka PV, Cook JA. 2008. Lysophosphatidic acid inhibits bacterial endotoxin-induced proinflammatory response: potential anti-inflammatory signaling pathways. Mol. Med. 14:422-428. http://dx.doi.org/10.2119/2007-00106.Fan.
64. Awojoodu AO, Ogle ME, Sefcik LS, Bowers DT, Martin K, Brayman KL, Lynch KR, Peirce-Cottler SM, Botchwey E. 2013. Sphingosine 1-phosphate receptor 3 regulates recruitment of anti-inflammatory monocytes to microvessels during implant arteriogenesis. Proc. Natl. Acad. Sci. U. S. A. 110:13785-13790. http://dx.doi.org/10.1073/pnas.1221309110.
65. Hughes JE, Srinivasan S, Lynch KR, Proia RL, Ferdek P, Hedrick CC. 2008. Sphingosine-1-phosphate induces an antiinflammatory phenotype in macrophages. Circ. Res. 102:950-958. http://dx.doi.org/10.1161/CIRCRESAHA .107.170779.