دورية أكاديمية
Inhibition of Prostaglandin-Degrading Enzyme 15-PGDH Mitigates Acute Murine Lung Allograft Rejection.
| العنوان: | Inhibition of Prostaglandin-Degrading Enzyme 15-PGDH Mitigates Acute Murine Lung Allograft Rejection. |
|---|---|
| المؤلفون: | Cui Y; Department of Immunology, School of Basic Medical Sciences, Capital Medical University, #10 Xi Tou Tiao, You An Men Wai, Fengtai, Beijing, 100069, People's Republic of China. yecui@outlook.com., Lv Z; Department of Immunology, School of Basic Medical Sciences, Capital Medical University, #10 Xi Tou Tiao, You An Men Wai, Fengtai, Beijing, 100069, People's Republic of China., Yang Z; Beijing Friendship Hospital, Capital Medical University, Beijing, 100050, People's Republic of China., Lei J; Research Core Facilities, Capital Medical University, Beijing, 100069, People's Republic of China. |
| المصدر: | Lung [Lung] 2023 Dec; Vol. 201 (6), pp. 591-601. Date of Electronic Publication: 2023 Nov 07. |
| نوع المنشور: | Journal Article; Research Support, Non-U.S. Gov't |
| اللغة: | English |
| بيانات الدورية: | Publisher: Springer Verlag Country of Publication: United States NLM ID: 7701875 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1432-1750 (Electronic) Linking ISSN: 03412040 NLM ISO Abbreviation: Lung Subsets: MEDLINE |
| أسماء مطبوعة: | Publication: New York : Springer Verlag Original Publication: Heidelberg, Springer International. |
| مواضيع طبية MeSH: | Prostaglandins*/metabolism , Prostaglandins*/pharmacology , Dinoprostone*/metabolism , Dinoprostone*/pharmacology, Mice ; Animals ; CD8-Positive T-Lymphocytes ; Lung/pathology ; Graft Rejection/prevention & control ; Allografts/metabolism ; Mice, Inbred C57BL |
| مستخلص: | Purpose: Acute rejection is a frequent complication among lung transplant recipients and poses substantial therapeutic challenges. 15-hydroxyprostaglandin dehydrogenase (15-PGDH), an enzyme responsible for the inactivation of prostaglandin E2 (PGE2), has recently been implicated in inflammatory lung diseases. However, the role of 15-PGDH in lung transplantation rejection remains elusive. The present study was undertaken to examine the expression of 15-PGDH in rejected lung allografts and whether inhibition of 15-PGDH ameliorates acute lung allograft rejection. Methods: Orthotopic mouse lung transplantations were performed between donor and recipient mice of the same strain or allogeneic mismatched pairs. The expression of 15-PGDH in mouse lung grafts was measured. The efficacy of a selective 15-PGDH inhibitor (SW033291) in ameliorating acute rejection was assessed through histopathological examination, micro-CT imaging, and pulmonary function tests. Additionally, the mechanism underlying the effects of SW033291 treatment was explored using CD8 + T cells isolated from mouse lung allografts. Results: Increased 15-PGDH expression was observed in rejected allografts and allogeneic CD8 + T cells. Treatment with SW033291 led to an accumulation of PGE2, modulation of CD8 + T-cell responses and mitochondrial activity, and improved allograft function and survival. Conclusion: Our study provides new insights into the role of 15-PGDH in acute lung rejection and highlights the therapeutic potential of inhibiting 15-PGDH for enhancing graft survival. The accumulation of PGE2 and modulation of CD8 + T-cell responses represent potential mechanisms underlying the benefits of 15-PGDH inhibition in this model. Our findings provide impetus for further exploring 15-PGDH as a target for improving lung transplantation outcomes. (© 2023. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.) |
| References: | van der Mark SC, Hoek RAS, Hellemons ME (2020) Developments in lung transplantation over the past decade. Eur Respir Rev. https://doi.org/10.1183/16000617.0132-2019. (PMID: 10.1183/16000617.0132-2019326990239489139) Trachuk P, Bartash R, Abbasi M, Keene A (2020) Infectious complications in lung transplant recipients. Lung 198:879–887. https://doi.org/10.1007/s00408-020-00403-9. (PMID: 10.1007/s00408-020-00403-9331691747652055) Graham CN, Watson C, Barlev A, Stevenson M, Dharnidharka VR (2022) Mean lifetime survival estimates following solid organ transplantation in the US and UK. J Med Econ 25:230–237. https://doi.org/10.1080/13696998.2022.2033050. (PMID: 10.1080/13696998.2022.203305035068310) Assadiasl S, Nicknam MH (2022) Cytokines in Lung Transplantation. Lung 200:793–806. https://doi.org/10.1007/s00408-022-00588-1. (PMID: 10.1007/s00408-022-00588-136348053) Todd JL, Neely ML, Kopetskie H, Sever ML, Kirchner J, Frankel CW, Snyder LD, Pavlisko EN, Martinu T, Tsuang W, Shino MY, Williams N, Robien MA, Singer LG, Budev M, Shah PD, Reynolds JM, Palmer SM, Belperio JA, Weigt SS (2020) Risk factors for acute rejection in the first year after lung transplant. A multicenter study. Am J Respir Crit Care Med 202:576–585. https://doi.org/10.1164/rccm.201910-1915OC. (PMID: 10.1164/rccm.201910-1915OC323799797427399) Swaminathan AC, Todd JL, Palmer SM (2021) Advances in human lung transplantation. Annu Rev Med 72:135–149. https://doi.org/10.1146/annurev-med-080119-103200. (PMID: 10.1146/annurev-med-080119-10320033113336) Armati M, Cattelan S, Guerrieri M, Messina M, Perea B, Genovese M, d’Alessandro M, Gangi S, Cameli P, Perillo F, Bennett D, Fossi A, Bargagli E, Bergantini L, Tuscany Transplant G (2023) Collagen type IV alpha 5 chain in bronchiolitis obliterans syndrome after lung transplant: the first evidence. Lung. https://doi.org/10.1007/s00408-023-00632-8. (PMID: 10.1007/s00408-023-00632-83740289610444639) d’Alessandro M, Bergantini L, Fossi A, De Vita E, Perillo F, Luzzi L, Paladini P, Sestini P, Rottoli P, Bargagli E, Bennett D (2021) The role of galectins in chronic lung allograft dysfunction. Lung 199:281–288. https://doi.org/10.1007/s00408-021-00449-3. (PMID: 10.1007/s00408-021-00449-3339421298203538) Maher SA, Belvisi MG (2010) Prostanoids and the cough reflex. Lung 188:9–12. https://doi.org/10.1007/s00408-009-9190-2. (PMID: 10.1007/s00408-009-9190-2) Wanders A, Tufveson G, Gerdin B (1992) Effects of prostaglandin E2 (PGE2) and drugs affecting PGE2 degradation on acute rejection of rat cardiac allografts. Scand J Thorac Cardiovasc Surg 26:33–37. https://doi.org/10.3109/14017439209099050. (PMID: 10.3109/140174392090990501529295) Fujimoto Y, Iwagaki H, Ozaki M, Ogino T, Murata H, Sun DS, Sadamori H, Takahashi HK, Tanaka N, Yagi T (2005) Involvement of prostaglandin receptors (EPR2-4) in in vivo immunosuppression of PGE2 in rat skin transplant model. Int Immunopharmacol 5:1131–1139. https://doi.org/10.1016/j.intimp.2005.01.014. (PMID: 10.1016/j.intimp.2005.01.01415914318) Ogawa M, Suzuki J, Kosuge H, Takayama K, Nagai R, Isobe M (2009) The mechanism of anti-inflammatory effects of prostaglandin E2 receptor 4 activation in murine cardiac transplantation. Transplantation 87:1645–1653. https://doi.org/10.1097/TP.0b013e3181a5c84c. (PMID: 10.1097/TP.0b013e3181a5c84c19502955) Cheng H, Huang H, Guo Z, Chang Y, Li Z (2021) Role of prostaglandin E2 in tissue repair and regeneration. Theranostics 11:8836–8854. https://doi.org/10.7150/thno.63396. (PMID: 10.7150/thno.63396345222148419039) Huang W, Li H, Kiselar J, Fink SP, Regmi S, Day A, Yuan Y, Chance M, Ready JM, Markowitz SD, Taylor DJ (2023) Small molecule inhibitors of 15-PGDH exploit a physiologic induced-fit closing system. Nat Commun 14:784. https://doi.org/10.1038/s41467-023-36463-7. (PMID: 10.1038/s41467-023-36463-7367743489922282) Zhang Y, Desai A, Yang SY, Bae KB, Antczak MI, Fink SP, Tiwari S, Willis JE, Williams NS, Dawson DM, Wald D, Chen WD, Wang Z, Kasturi L, Larusch GA, He L, Cominelli F, Di Martino L, Djuric Z, Milne GL, Chance M, Sanabria J, Dealwis C, Mikkola D, Naidoo J, Wei S, Tai HH, Gerson SL, Ready JM, Posner B, Willson JK, Markowitz SD (2015) Tissue regeneration. Inhibition of the prostaglandin-degrading enzyme 15-PGDH potentiates tissue regeneration. Science 348:aaa2340. https://doi.org/10.1126/science.aaa2340. (PMID: 10.1126/science.aaa2340260688574481126) Palla AR, Ravichandran M, Wang YX, Alexandrova L, Yang AV, Kraft P, Holbrook CA, Schurch CM, Ho ATV, Blau HM (2021) Inhibition of prostaglandin-degrading enzyme 15-PGDH rejuvenates aged muscle mass and strength. Science. https://doi.org/10.1126/science.abc8059. (PMID: 10.1126/science.abc805933303683) Smith JN, Dawson DM, Christo KF, Jogasuria AP, Cameron MJ, Antczak MI, Ready JM, Gerson SL, Markowitz SD, Desai AB (2021) 15-PGDH inhibition activates the splenic niche to promote hematopoietic regeneration. JCI Insight. https://doi.org/10.1172/jci.insight.143658. (PMID: 10.1172/jci.insight.143658345497258663556) Smith JNP, Witkin MD, Jogasuria AP, Christo KF, Raffay TM, Markowitz SD, Desai AB (2020) Therapeutic targeting of 15-PGDH in murine pulmonary fibrosis. Sci Rep 10:11657. https://doi.org/10.1038/s41598-020-68336-0. (PMID: 10.1038/s41598-020-68336-0326696207363833) Barnthaler T, Theiler A, Zabini D, Trautmann S, Stacher-Priehse E, Lanz I, Klepetko W, Sinn K, Flick H, Scheidl S, Thomas D, Olschewski H, Kwapiszewska G, Schuligoi R, Heinemann A (2020) Inhibiting eicosanoid degradation exerts antifibrotic effects in a pulmonary fibrosis mouse model and human tissue. J Allergy Clin Immunol 145(818–833):e811. https://doi.org/10.1016/j.jaci.2019.11.032. (PMID: 10.1016/j.jaci.2019.11.032) Rubino M, Travers JG, Headrick AL, Enyart BT, Lemieux ME, Cavasin MA, Schwisow JA, Hardy EJ, Kaltenbacher KJ, Felisbino MB, Jonas E, Ambardekar AV, Bristow MR, Koch KA, McKinsey TA (2023) Inhibition of eicosanoid degradation mitigates fibrosis of the heart. Circ Res 132:10–29. https://doi.org/10.1161/CIRCRESAHA.122.321475. (PMID: 10.1161/CIRCRESAHA.122.32147536475698) Cui Y, Liu K, Monzon-Medina ME, Padera RF, Wang H, George G, Toprak D, Abdelnour E, D’Agostino E, Goldberg HJ, Perrella MA, Forteza RM, Rosas IO, Visner G, El-Chemaly S (2015) Therapeutic lymphangiogenesis ameliorates established acute lung allograft rejection. J Clin Invest 125:4255–4268. https://doi.org/10.1172/JCI79693. (PMID: 10.1172/JCI79693264852844639995) Imani J, Liu K, Cui Y, Assaker JP, Han J, Ghosh AJ, Ng J, Shrestha S, Lamattina AM, Louis PH, Hentschel A, Esposito AJ, Rosas IO, Liu X, Perrella MA, Azzi J, Visner G, El-Chemaly S (2021) Blocking hyaluronan synthesis alleviates acute lung allograft rejection. JCI Insight. https://doi.org/10.1172/jci.insight.142217. (PMID: 10.1172/jci.insight.142217346657828663774) Maeyashiki T, Jang J-H, Janker F, Yamada Y, Inci I, Weder W, Piegeler T, Jungraithmayr W (2019) The amide local anesthetic ropivacaine attenuates acute rejection after allogeneic mouse lung transplantation. Lung 197:217–226. https://doi.org/10.1007/s00408-019-00197-5. (PMID: 10.1007/s00408-019-00197-530739218) Issa F, Schiopu A, Wood KJ (2010) Role of T cells in graft rejection and transplantation tolerance. Expert Rev Clin Immunol 6:155–169. https://doi.org/10.1586/eci.09.64. (PMID: 10.1586/eci.09.6420383898) Liu H, Liu L, Liu K, Bizargity P, Hancock WW, Visner GA (2009) Reduced cytotoxic function of effector CD8+ T cells is responsible for indoleamine 2,3-dioxygenase-dependent immune suppression. J Immunol 183:1022–1031. https://doi.org/10.4049/jimmunol.0900408. (PMID: 10.4049/jimmunol.090040819564344) Varanasi SK, Ma S, Kaech SM (2019) T cell metabolism in a state of flux. Immunity 51:783–785. https://doi.org/10.1016/j.immuni.2019.10.012. (PMID: 10.1016/j.immuni.2019.10.01231747577) Yap M, Brouard S, Pecqueur C, Degauque N (2015) Targeting CD8 T-cell metabolism in transplantation. Front Immunol 6:547. https://doi.org/10.3389/fimmu.2015.00547. (PMID: 10.3389/fimmu.2015.00547265571234617050) Desdin-Mico G, Soto-Heredero G, Mittelbrunn M (2018) Mitochondrial activity in T cells. Mitochondrion 41:51–57. https://doi.org/10.1016/j.mito.2017.10.006. (PMID: 10.1016/j.mito.2017.10.00629032101) Lisci M, Griffiths GM (2023) Arming a killer: mitochondrial regulation of CD8(+) T cell cytotoxicity. Trends Cell Biol 33:138–147. https://doi.org/10.1016/j.tcb.2022.05.007. (PMID: 10.1016/j.tcb.2022.05.00735753961) Cui Y, Chen G, Yang Z (2020) Mitochondrial superoxide mediates PM(2.5)-induced cytotoxicity in human pulmonary lymphatic endothelial cells. Environ Pollut 263:114423. https://doi.org/10.1016/j.envpol.2020.114423. (PMID: 10.1016/j.envpol.2020.11442332222623) Myung SJ, Rerko RM, Yan M, Platzer P, Guda K, Dotson A, Lawrence E, Dannenberg AJ, Lovgren AK, Luo G, Pretlow TP, Newman RA, Willis J, Dawson D, Markowitz SD (2006) 15-Hydroxyprostaglandin dehydrogenase is an in vivo suppressor of colon tumorigenesis. Proc Natl Acad Sci USA 103:12098–12102. https://doi.org/10.1073/pnas.0603235103. (PMID: 10.1073/pnas.0603235103168804061567703) Walker NM, Badri LN, Wadhwa A, Wettlaufer S, Peters-Golden M, Lama VN (2012) Prostaglandin E2 as an inhibitory modulator of fibrogenesis in human lung allografts. Am J Respir Crit Care Med 185:77–84. https://doi.org/10.1164/rccm.201105-0834OC. (PMID: 10.1164/rccm.201105-0834OC219407903262036) Okamoto T, Okamoto S, Fujimoto Y, Tabata Y, Uemoto S (2013) Suppression of acute rejection by administration of prostaglandin E2 receptor subtype 4 agonist in rat organ transplantation models. J Surg Res 183:852–859. https://doi.org/10.1016/j.jss.2013.01.039. (PMID: 10.1016/j.jss.2013.01.03923478083) Birrell MA, Maher SA, Dekkak B, Jones V, Wong S, Brook P, Belvisi MG (2015) Anti-inflammatory effects of PGE2 in the lung: role of the EP4 receptor subtype. Thorax 70:740–747. https://doi.org/10.1136/thoraxjnl-2014-206592. (PMID: 10.1136/thoraxjnl-2014-20659225939749) 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. https://doi.org/10.1016/j.it.2003.11.001. (PMID: 10.1016/j.it.2003.11.00114698283) Hamberg M, Samuelsson B (1971) On the metabolism of prostaglandins E 1 and E 2 in man. J Biol Chem 246:6713–6721. (PMID: 10.1016/S0021-9258(19)45905-X5126221) Jarvinen L, Badri L, Wettlaufer S, Ohtsuka T, Standiford TJ, Toews GB, Pinsky DJ, Peters-Golden M, Lama VN (2008) Lung resident mesenchymal stem cells isolated from human lung allografts inhibit T cell proliferation via a soluble mediator. J Immunol 181:4389–4396. https://doi.org/10.4049/jimmunol.181.6.4389. (PMID: 10.4049/jimmunol.181.6.438918768898) Kalinski P (2012) Regulation of immune responses by prostaglandin E2. J Immunol 188:21–28. https://doi.org/10.4049/jimmunol.1101029. (PMID: 10.4049/jimmunol.110102922187483) Yang X, Ma N, Szabolcs MJ, Zhong J, Athan E, Sciacca RR, Michler RE, Anderson GD, Wiese JF, Leahy KM, Gregory S, Cannon PJ (2000) Upregulation of COX-2 during cardiac allograft rejection. Circulation 101:430–438. https://doi.org/10.1161/01.cir.101.4.430. (PMID: 10.1161/01.cir.101.4.43010653836) Rangel EB, Moura LA, Franco MF, Pacheco-Silva A (2007) Up-regulation of cyclooxygenase-2 in different grades of acute human renal allograft rejection. Prostaglandins Leukot Essent Fatty Acids 76:235–243. https://doi.org/10.1016/j.plefa.2007.01.005. (PMID: 10.1016/j.plefa.2007.01.00517382527) Osma-Garcia IC, Punzon C, Fresno M, Diaz-Munoz MD (2016) Dose-dependent effects of prostaglandin E2 in macrophage adhesion and migration. Eur J Immunol 46:677–688. https://doi.org/10.1002/eji.201545629. (PMID: 10.1002/eji.20154562926631603) Rangel Moreno J, Estrada Garcia I, La Luz De, Garcia Hernandez M, Aguilar Leon D, Marquez R, Hernandez Pando R (2002) The role of prostaglandin E2 in the immunopathogenesis of experimental pulmonary tuberculosis. Immunology 106:257–266. https://doi.org/10.1046/j.1365-2567.2002.01403.x. (PMID: 10.1046/j.1365-2567.2002.01403.x12047755) Gelman AE, Okazaki M, Lai J, Kornfeld CG, Kreisel FH, Richardson SB, Sugimoto S, Tietjens JR, Patterson GA, Krupnick AS, Kreisel D (2008) CD4+ T lymphocytes are not necessary for the acute rejection of vascularized mouse lung transplants. J Immunol 180:4754–4762. https://doi.org/10.4049/jimmunol.180.7.4754. (PMID: 10.4049/jimmunol.180.7.475418354199) Harper SJ, Ali JM, Wlodek E, Negus MC, Harper IG, Chhabra M, Qureshi MS, Mallik M, Bolton E, Bradley JA, Pettigrew GJ (2015) CD8 T-cell recognition of acquired alloantigen promotes acute allograft rejection. Proc Natl Acad Sci USA 112:12788–12793. https://doi.org/10.1073/pnas.1513533112. (PMID: 10.1073/pnas.1513533112264208744611606) Burkett JB, Doran AC, Gannon M (2023) Harnessing prostaglandin E(2) signaling to ameliorate autoimmunity. Trends Immunol 44:162–171. https://doi.org/10.1016/j.it.2023.01.004. (PMID: 10.1016/j.it.2023.01.00436707339) Ledderose C, Bao Y, Lidicky M, Zipperle J, Li L, Strasser K, Shapiro NI, Junger WG (2014) Mitochondria are gate-keepers of T cell function by producing the ATP that drives purinergic signaling. J Biol Chem 289:25936–25945. https://doi.org/10.1074/jbc.M114.575308. (PMID: 10.1074/jbc.M114.575308250708954162192) Kumar A, Chamoto K, Chowdhury PS, Honjo T (2020) Tumors attenuating the mitochondrial activity in T cells escape from PD-1 blockade therapy. elife. https://doi.org/10.7554/eLife.52330. (PMID: 10.7554/eLife.52330330636697655109) Bueno V, Pestana JO (2002) The role of CD8+ T cells during allograft rejection. Braz J Med Biol Res 35:1247–1258. https://doi.org/10.1590/s0100-879x2002001100001. (PMID: 10.1590/s0100-879x200200110000112426623) Martinu T, Chen DF, Palmer SM (2009) Acute rejection and humoral sensitization in lung transplant recipients. Proc Am Thorac Soc 6:54–65. https://doi.org/10.1513/pats.200808-080GO. (PMID: 10.1513/pats.200808-080GO191315312626504) Tong M, Tai HH (2005) 15-Hydroxyprostaglandin dehydrogenase can be induced by dexamethasone and other glucocorticoids at the therapeutic level in A549 human lung adenocarcinoma cells. Arch Biochem Biophys 435:50–55. https://doi.org/10.1016/j.abb.2004.11.031. (PMID: 10.1016/j.abb.2004.11.03115680906) Snyder LD, Palmer SM (2006) Immune mechanisms of lung allograft rejection. Semin Respir Crit Care Med 27:534–543. https://doi.org/10.1055/s-2006-954610. (PMID: 10.1055/s-2006-95461017072801) Hsiao HM, Scozzi D, Gauthier JM, Kreisel D (2017) Mechanisms of graft rejection after lung transplantation. Curr Opin Organ Transpl 22:29–35. https://doi.org/10.1097/MOT.0000000000000371. (PMID: 10.1097/MOT.0000000000000371) Fan L, Benson HL, Vittal R, Mickler EA, Presson R, Fisher AJ, Cummings OW, Heidler KM, Keller MR, Burlingham WJ, Wilkes DS (2011) Neutralizing IL-17 prevents obliterative bronchiolitis in Murine orthotopic lung transplantation. Am J Transpl 11:911–922. https://doi.org/10.1111/j.1600-6143.2011.03482.x. (PMID: 10.1111/j.1600-6143.2011.03482.x) Martinu T, Oishi H, Juvet SC, Cypel M, Liu M, Berry GJ, Hwang DM, Keshavjee S (2019) Spectrum of chronic lung allograft pathology in a mouse minor-mismatched orthotopic lung transplant model. Am J Transpl 19:247–258. https://doi.org/10.1111/ajt.15167. (PMID: 10.1111/ajt.15167) |
| معلومات مُعتمدة: | 81974050 National Natural Science Foundation of China; KM202010025003 Beijing Municipal Commission of Education; 320.6750.2021-12-4 Wu Jieping Medical Foundation |
| فهرسة مساهمة: | Keywords: 15-hydroxyprostaglandin dehydrogenase; Acute rejection; CD8+ T cell; Lung transplant; Mitochondrial activity; Prostaglandin E2 |
| المشرفين على المادة: | 0 (Prostaglandins) EC 1.1.1.141 (15-hydroxyprostaglandin dehydrogenase) 0 (SW033291) K7Q1JQR04M (Dinoprostone) |
| تواريخ الأحداث: | Date Created: 20231107 Date Completed: 20231127 Latest Revision: 20231212 |
| رمز التحديث: | 20231215 |
| DOI: | 10.1007/s00408-023-00651-5 |
| PMID: | 37934242 |
| قاعدة البيانات: | MEDLINE |
Find this article in full text from Springer Verlag. 
Full Text Finder | تدمد: | 1432-1750 |
|---|---|
| DOI: | 10.1007/s00408-023-00651-5 |