Trichinella spiralis infection changes immune response in mice performed abdominal heterotopic cardiac transplantation and prolongs cardiac allograft survival time

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• 作者：Gengguo Deng ; Ronghai Deng ; Jianping Yao ; Bing Liao ; Yinghua Chen…
• 关键词：Allograft rejection ; Trichinella spiralis ; Cardiac allograft ; Transplantation
• 刊名：Parasitology Research
• 出版年：2016
• 出版时间：January 2016
• 年：2016
• 卷：115
• 期：1
• 页码：407-414
• 全文大小：3,940 KB
• 参考文献：Abdi R, Means TK, Ito T, Smith RN, Najafian N, Jurewicz M, Tchipachvili V, Charo I, Auchincloss H Jr, Sayegh MH, Luster AD (2004) Differential role of CCR2 in islet and heart allograft rejection: tissue specificity of chemokine/chemokine receptor function in vivo. J Immunol 172(2):767–775CrossRef PubMed
  Alexander J, Bryson K (2005) T helper (h)1/Th2 and Leishmania: paradox rather than paradigm. Immunol Lett 99(1):17–23CrossRef PubMed
  Alkarmi T, Ijaz MK, Dar FK, Abdou S, Alharbi S, Frossard P, Naiem M (1995) Suppression of transplant immunity in experimental trichinellosis. Comp Immunol Microbiol Infect Dis 18(3):171–177CrossRef PubMed
  Ananthaswamy HN (1986) Relationship between expression of tumor-specific transplantation antigens and neoplastic transformation in an ultraviolet radiation-induced murine skin cancer. Cancer Res 46(12 Pt 1):6322–6326PubMed
  Araujo FG, Coelho PM, Pereira LH, Pellegrino J (1977) Schistosoma mansoni: impairment of the cell-mediated immune response in mice. Clin Exp Immunol 28(2):289–291PubMedCentral PubMed
  Braun RK, Molitor-Dart M, Wigfield C, Xiang Z, Fain SB, Jankowska-Gan E, Seroogy CM, Burlingham WJ, Wilkes DS, Brand DD, Torrealba J, Love RB (2009) Transfer of tolerance to collagen type V suppresses T-helper-cell-17 lymphocyte-mediated acute lung transplant rejection. Transplantation 88(12):1341–1348PubMedCentral CrossRef PubMed
  Cook CH, Bickerstaff AA, Wang JJ, Zimmerman PD, Forster MR, Nadasdy T, Colvin RB, Hadley GA, Orosz CG (2009) Disruption of murine cardiac allograft acceptance by latent cytomegalovirus. Am J Transplant 9(1):42–53PubMedCentral CrossRef PubMed
  Dallman MJ (1995) Cytokines and transplantation: Th1/Th2 regulation of the immune response to solid organ transplants in the adult. Curr Opin Immunol 7(5):632–638CrossRef PubMed
  Degauque N, Mariat C, Kenny J, Zhang D, Gao W, Vu MD, Alexopoulos S, Oukka M, Umetsu DT, DeKruyff RH, Kuchroo V, Zheng XX, Strom TB (2008) Immunostimulatory Tim-1-specific antibody deprograms Tregs and prevents transplant tolerance in mice. J Clin Invest 118(2):735–741PubMedCentral CrossRef PubMed
  Dennis DT, Despommier DD, Davis N (1970) Infectivity of the newborn larva of Trichinella spiralis in the rat. J Parasitol 56(5):974–977CrossRef PubMed
  Dvoroznakova E, Hurnikova Z, Kolodziej-Sobocinska M (2011) Development of cellular immune response of mice to infection with low doses of Trichinella spiralis, Trichinella britovi and Trichinella pseudospiralis larvae. Parasitol Res 108(1):169–176CrossRef PubMed
  Ekberg H, Tedesco-Silva H, Demirbas A, Vitko S, Nashan B, Gurkan A, Margreiter R, Hugo C, Grinyo JM, Frei U, Vanrenterghem Y, Daloze P, Halloran PF (2007) Reduced exposure to calcineurin inhibitors in renal transplantation. N Engl J Med 357(25):2562–2575CrossRef PubMed
  Elliott DE, Weinstock JV (2012) Helminth-host immunological interactions: prevention and control of immune-mediated diseases. Ann N Y Acad Sci 1247:83–96PubMedCentral CrossRef PubMed
  Faubert GM, Tanner CE (1975) Leucoagglutination and cytotoxicity of the serum of infected mice and of extracts of Trichinella spiralis larvae and the capacity of infected mouse sera to prolong skin allografts. Immunology 28(6):1041–1050PubMedCentral PubMed
  Froscher W, Gullotta F, Saathoff M, Tackmann W (1988) Chronic trichinosis. Clinical, bioptic, serological and electromyographic observations. Eur Neurol 28(4):221–226CrossRef PubMed
  Garrod KR, Cahalan MD (2008) Murine skin transplantation. J Vis Exp: JoVE(11)
  Hasegawa T, Visovatti SH, Hyman MC, Hayasaki T, Pinsky DJ (2007) Heterotopic vascularized murine cardiac transplantation to study graft arteriopathy. Nat Protoc 2(3):471–480CrossRef PubMed
  He W, Fang Z, Wang F, Wu K, Xu Y, Zhou H, Du D, Gao Y, Zhang WN, Niki T, Hirashima M, Yuan J, Chen ZK (2009) Galectin-9 significantly prolongs the survival of fully mismatched cardiac allografts in mice. Transplantation 88(6):782–790CrossRef PubMed
  Heidt S, Segundo DS, Chadha R, Wood KJ (2010) The impact of Th17 cells on transplant rejection and the induction of tolerance. Curr Opin Organ Transplant 15(4):456–461PubMedCentral CrossRef PubMed
  Ilic N, Gruden-Movsesijan A, Sofronic-Milosavljevic L (2012) Trichinella spiralis: shaping the immune response. Immunol Res 52(1-2):111–119CrossRef PubMed
  Ishikawa N, Goyal PK, Mahida YR, Li KF, Wakelin D (1998) Early cytokine responses during intestinal parasitic infections. Immunology 93(2):257–263PubMedCentral CrossRef PubMed
  Jankovic D, Kullberg MC, Caspar P, Sher A (2004) Parasite-induced Th2 polarization is associated with down-regulated dendritic cell responsiveness to Th1 stimuli and a transient delay in T lymphocyte cycling. J Immunol 173(4):2419–2427CrossRef PubMed
  Joffre O, Santolaria T, Calise D, Al Saati T, Hudrisier D, Romagnoli P, van Meerwijk JP (2008) Prevention of acute and chronic allograft rejection with CD4+CD25+Foxp3+ regulatory T lymphocytes. Nat Med 14(1):88–92PubMedCentral CrossRef PubMed
  Kang SA, Cho MK, Park MK, Kim DH, Hong YC, Lee YS, Cha HJ, Ock MS, Yu HS (2012) Alteration of helper T-cell related cytokine production in splenocytes during Trichinella spiralis infection. Vet Parasitol 186(3-4):319–327CrossRef PubMed
  Le Moine A, Goldman M, Abramowicz D (2002) Multiple pathways to allograft rejection. Transplantation 73(9):1373–1381CrossRef PubMed
  Ledingham DL, McAlister VC, Ehigiator HN, Giacomantonio C, Theal M, Lee TD (1996) Prolongation of rat kidney allograft survival by nematodes. Transplantation 61(2):184–188CrossRef PubMed
  Li J, Simeoni E, Fleury S, Dudler J, Fiorini E, Kappenberger L, von Segesser LK, Vassalli G (2006) Gene transfer of soluble interleukin-17 receptor prolongs cardiac allograft survival in a rat model. Eur J Cardiothorac Surg 29(5):779–783CrossRef PubMed
  Li T, Zhao JM, Zhang Y, Pai ZL, Zhang W, Tuxun TH, Bai L, Wu J, Wen H (2011) Suppression of acute rejective response following orthotopic liver transplantation in experimental rats infected with Echinococcus multilocularis. Chin Med J (Engl) 124(18):2818–2823
  Liu Z, Fan H, Jiang S (2013) CD4(+) T-cell subsets in transplantation. Immunol Rev 252(1):183–191CrossRef PubMed
  Liwski R, Zhou J, McAlister V, Lee TD (2000) Prolongation of allograft survival by Nippostrongylus brasiliensis is associated with decreased allospecific cytotoxic T lymphocyte activity and development of T cytotoxic cell type 2 cells. Transplantation 69(9):1912–1922CrossRef PubMed
  Ljungstrom I, Huldt G (1977) Effect of experimental trichinosis on unrelated humoral and cell mediated immunity. Acta Pathol Microbiol Scand C 85(2):131–141PubMed
  McDiarmid SV, Busuttil RW, Ascher NL, Burdick J, D’Alessandro AM, Esquivel C, Kalayoglu M, Klein AS, Marsh JW, Miller CM et al (1995) FK506 (tacrolimus) compared with cyclosporine for primary immunosuppression after pediatric liver transplantation. Results from the U.S. Multicenter Trial. Transplantation 59(4):530–536CrossRef PubMed
  Meier-Kriesche HU, Schold JD, Kaplan B (2004a) Long-term renal allograft survival: have we made significant progress or is it time to rethink our analytic and therapeutic strategies? Am J Transplant 4(8):1289–1295CrossRef PubMed
  Meier-Kriesche HU, Schold JD, Srinivas TR, Kaplan B (2004b) Lack of improvement in renal allograft survival despite a marked decrease in acute rejection rates over the most recent era. Am J Transplant 4(3):378–383CrossRef PubMed
  Nagano I, Wu Z, Takahashi Y (2009) Functional genes and proteins of Trichinella spp. Parasitol Res 104(2):197–207CrossRef PubMed
  Platz KP, Mueller AR, Blumhardt G, Bachmann S, Bechstein WO, Kahl A, Neuhaus P (1994) Nephrotoxicity after orthotopic liver transplantation in cyclosporin A and FK 506-treated patients. Transpl Int 7(Suppl 1):S52–S57CrossRef PubMed
  Ring GH, Saleem S, Dai Z, Hassan AT, Konieczny BT, Baddoura FK, Lakkis FG (1999) Interferon-gamma is necessary for initiating the acute rejection of major histocompatibility complex class II-disparate skin allografts. Transplantation 67(10):1362–1365CrossRef PubMed
  Svet-Moldavsky GJ, Shaghijan GS, Mkheidze DM, Litovchenko TA, Ozeretskovskaya NN, Kadaghidze ZG, Chernyakhovskaya IY (1969) Mouse transplantation immunity depressed by Trichinella spiralis. Lancet 2(7615):320CrossRef PubMed
  Tang Q, Bluestone JA (2008) The Foxp3+ regulatory T cell: a jack of all trades, master of regulation. Nat Immunol 9(3):239–244PubMedCentral CrossRef PubMed
  Ueno T, Habicht A, Clarkson MR, Albin MJ, Yamaura K, Boenisch O, Popoola J, Wang Y, Yagita H, Akiba H, Ansari MJ, Yang J, Turka LA, Rothstein DM, Padera RF, Najafian N, Sayegh MH (2008) The emerging role of T cell Ig mucin 1 in alloimmune responses in an experimental mouse transplant model. J Clin Invest 118(2):742–751PubMedCentral CrossRef PubMed
  Vincenti F, Charpentier B, Vanrenterghem Y, Rostaing L, Bresnahan B, Darji P, Massari P, Mondragon-Ramirez GA, Agarwal M, Di Russo G, Lin CS, Garg P, Larsen CP (2010) A phase III study of belatacept-based immunosuppression regimens versus cyclosporine in renal transplant recipients (BENEFIT study). Am J Transplant 10(3):535–546CrossRef PubMed
  Waldmann H, Graca L, Cobbold S, Adams E, Tone M, Tone Y (2004) Regulatory T cells and organ transplantation. Semin Immunol 16(2):119–126CrossRef PubMed
  Youssef AR, Otley C, Mathieson PW, Smith RM (2004) Role of CD4+ and CD8+ T cells in murine skin and heart allograft rejection across different antigenic desparities. Transpl Immunol 13(4):297–304CrossRef PubMed
  Yu YR, Deng MJ, Lu WW, Jia MZ, Wu W, Qi YF (2013) Systemic cytokine profiles and splenic toll-like receptor expression during Trichinella spiralis infection. Exp Parasitol 134(1):92–101CrossRef PubMed
  Zeiser R, Nguyen VH, Beilhack A, Buess M, Schulz S, Baker J, Contag CH, Negrin RS (2006) Inhibition of CD4+CD25+ regulatory T-cell function by calcineurin-dependent interleukin-2 production. Blood 108(1):390–399PubMedCentral CrossRef PubMed
  
• 作者单位：Gengguo Deng (1)
  Ronghai Deng (1)
  Jianping Yao (2)
  Bing Liao (6)
  Yinghua Chen (1)
  Zhongdao Wu (4)
  Hongxing Hu (5)
  Xingwang Zhou (3)
  Yi Ma (1)
  
  1. Organ Transplant Center, the First Affiliated Hospital, Sun Yat-sen University, No. 58 Zhongshan 2nd Road, Guangzhou, 510080, China
  2. Department of Cardiac Surgery, the First Affiliated Hospital, Sun Yat-sen University, Guangzhou, China
  6. Department of Pathology, the First Affiliated Hospital, Sun Yat-sen University, No. 58 Zhongshan 2nd Road, Guangzhou, 510080, China
  4. Department of Parasitology, Sun Yat-sen University Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou, China
  5. Guangzhou First People’s Hospital, Guangzhou Medical University, Guangzhou, China
  3. Department of Biochemistry and Molecular Biology, Sun Yat-sen University Zhongshan School of Medicine, Sun Yat-sen University, 74 Zhongshan 2nd Road, Guangzhou, 510080, China
  
• 刊物类别：Biomedical and Life Sciences
• 刊物主题：Biomedicine
  Medical Microbiology
  Microbiology
  Immunology
  
• 出版者：Springer Berlin / Heidelberg
• ISSN：1432-1955

文摘

Allograft rejection has been an obstacle for long-term survival of patients for many years. Current strategies for transplant rejection are not as optimal as we expected, especially for long-term treatments. Trichinella spiralis, a nematode parasitized in mammalian muscle and as an invader, maintains harmonious with host in the long term by evading host immune attack. To determine whether T. spiralis infection impacts on allograft rejection, we performed mice cardiac allograft transplantation model by using BALB/c (H-2b) mice as donors and C57BL/6 (H-2b) mice orally infected with 300 muscle larvae for 28 days as recipients. Graft survival was monitored by daily palpation of the abdomen; histologic change was observed by H&E stain; and CD4+, CD8+, CD4+IFN-γ+, and CD4+IL-17+ T cells and regulatory T cells were examined with the use of flow cytometry. Serum cytokine levels were measured by Luminex. Finally, we found that mean survival time of cardiac allografts in T. spiralis group was 23.40 ± 1.99 days, while the vehicle control group was 10.60 ± 0.75 days. Furthermore, we observed alleviated histological changes in the heart allograft, decreased corresponding CD8+ T cells, suppressed Th1 and Th17 responses, and increased regulatory T cell frequency in a murine cardiac transplantation model at day 7 post-transplantation in experimental group. These data suggest that T. spiralis infection resulted in prolonged allograft survival following murine cardiac transplantation, with suppressed Th1/Th17 responses and augmented regulatory T cells.