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Published in: Graefe's Archive for Clinical and Experimental Ophthalmology 4/2021

01-04-2021 | Indomethacin | Basic Science

Subconjunctival injection of tumor necrosis factor-α pre-stimulated bone marrow-derived mesenchymal stem cells enhances anti-inflammation and anti-fibrosis in ocular alkali burns

Authors: Nuan Zhang, Xiaohui Luo, Shiyao Zhang, Ren Liu, Lingyi Liang, Wenru Su, Dan Liang

Published in: Graefe's Archive for Clinical and Experimental Ophthalmology | Issue 4/2021

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Abstract

Purpose

To investigate the therapeutic effect of subconjunctival injection of tumor necrosis factor-α (TNF-α) pre-stimulated bone marrow-derived mesenchymal stem cells (BMMSCs) on ocular alkali burns in a rat model.

Methods

After applying a 6 mm filter paper soaking in 1 N NaOH on the cornea of rats, the suspension of TNF‐α pre-stimulated BMMSCs, BMMSCs and PBS were given subconjunctivally and respectively. Corneal epithelial defect, corneal opacity, inflammation as well as PTGS2 and TSG-6 expression on day 7 and fibrosis on day 14 were compared.

Results

TNF‐α pre-stimulated BMMSCs group had a more predominate effect on promoting corneal epithelial repairing, decreasing corneal opacity, reducing inflammatory cells and CD68 + macrophages on day 7 and suppressing fibrosis on day 14 compared to BMMSCs group. Besides, it had significant increased expressions of PTGS2 and TSG-6 in vitro. Pre-treated with Indomethacin revealed a reverse effect on above-mentioned changes.

Conclusion

Subconjunctival injection of TNF‐α pre-stimulated BMMSCs enhanced anti-inflammatory and anti-fibrotic effect in ocular alkali burns, which was possibly though up regulation of PTGS2 and TSG-6 expression.
Literature
1.
go back to reference Haring RS, Sheffield ID, Channa R, Canner JK, Schneider EB (2016) Epidemiologic Trends of Chemical Ocular Burns in the United States. JAMA Ophthalmol 134(10):1119–1124PubMed Haring RS, Sheffield ID, Channa R, Canner JK, Schneider EB (2016) Epidemiologic Trends of Chemical Ocular Burns in the United States. JAMA Ophthalmol 134(10):1119–1124PubMed
2.
go back to reference Hong J, Qiu T, Wei A, Sun X, Xu J (2010) Clinical characteristics and visual outcome of severe ocular chemical injuries in Shanghai. Ophthalmology 117(12):2268–2272PubMed Hong J, Qiu T, Wei A, Sun X, Xu J (2010) Clinical characteristics and visual outcome of severe ocular chemical injuries in Shanghai. Ophthalmology 117(12):2268–2272PubMed
3.
go back to reference Cabalag MS, Wasiak J, Syed Q, Paul E, Hall AJ, Cleland H (2015) Early and late complications of ocular burn injuries. Journal of Plastic, Reconstructive & Aesthetic Surgery 68(3):356–361 Cabalag MS, Wasiak J, Syed Q, Paul E, Hall AJ, Cleland H (2015) Early and late complications of ocular burn injuries. Journal of Plastic, Reconstructive & Aesthetic Surgery 68(3):356–361
4.
go back to reference Bizrah M, Yusuf A, Ahmad S (2019) An update on chemical eye burns. Eye (Lond) 33(9):1362–1377 Bizrah M, Yusuf A, Ahmad S (2019) An update on chemical eye burns. Eye (Lond) 33(9):1362–1377
5.
go back to reference Baradaran-Rafii A, Eslani M, Haq Z, Shirzadeh E, Huvard MJ, Djalilian AR (2017) Current and Upcoming Therapies for Ocular Surface Chemical Injuries. Ocular Surface 15(1):48–64 Baradaran-Rafii A, Eslani M, Haq Z, Shirzadeh E, Huvard MJ, Djalilian AR (2017) Current and Upcoming Therapies for Ocular Surface Chemical Injuries. Ocular Surface 15(1):48–64
6.
go back to reference Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR (1999) Multilineage Potential of Adult Human Mesenchymal Stem Cells. Science 284(5411):143–147PubMed Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR (1999) Multilineage Potential of Adult Human Mesenchymal Stem Cells. Science 284(5411):143–147PubMed
7.
go back to reference Nauta AJ, Fibbe WE (2007) Immunomodulatory properties of mesenchymal stromal cells. Blood 110(10):3499–3506PubMed Nauta AJ, Fibbe WE (2007) Immunomodulatory properties of mesenchymal stromal cells. Blood 110(10):3499–3506PubMed
8.
go back to reference Golpanian S, Wolf A, Hatzistergos KE, Hare JM (2016) Rebuilding the Damaged Heart: Mesenchymal Stem Cells, Cell-Based Therapy, and Engineered Heart Tissue. Physiol Rev 96(3):1127–1168PubMedPubMedCentral Golpanian S, Wolf A, Hatzistergos KE, Hare JM (2016) Rebuilding the Damaged Heart: Mesenchymal Stem Cells, Cell-Based Therapy, and Engineered Heart Tissue. Physiol Rev 96(3):1127–1168PubMedPubMedCentral
9.
go back to reference Lee RH, Pulin AA, Seo MJ, Kota DJ, Ylostalo J, Larson BL, Semprun-Prieto L, Delafontaine P, Prockop DJ (2009) Intravenous hMSCs Improve Myocardial Infarction in Mice because Cells Embolized in Lung Are Activated to Secrete the Anti-inflammatory Protein TSG-6. Cell Stem Cell 5(1):54–63PubMedPubMedCentral Lee RH, Pulin AA, Seo MJ, Kota DJ, Ylostalo J, Larson BL, Semprun-Prieto L, Delafontaine P, Prockop DJ (2009) Intravenous hMSCs Improve Myocardial Infarction in Mice because Cells Embolized in Lung Are Activated to Secrete the Anti-inflammatory Protein TSG-6. Cell Stem Cell 5(1):54–63PubMedPubMedCentral
10.
go back to reference Liang J, Zhang HY, Hua BZ, Wang H, Lu LW, Shi ST, Hou YY, Zeng XF, Gilkeson GS, Sun LY (2010) Allogenicmesenchymal stem cells transplantation in refractory systemic lupus erythematosus: a pilot clinical study. Ann Rheum Dis 69(8):1423–1429PubMed Liang J, Zhang HY, Hua BZ, Wang H, Lu LW, Shi ST, Hou YY, Zeng XF, Gilkeson GS, Sun LY (2010) Allogenicmesenchymal stem cells transplantation in refractory systemic lupus erythematosus: a pilot clinical study. Ann Rheum Dis 69(8):1423–1429PubMed
11.
go back to reference Javorkova E, Trosan P, Zajicova A, Krulova M, Hajkova M, Holan V (2014) Modulation of the early inflammatory microenvironment in the alkali-burned eye by systemically administered interferon-gamma-treated mesenchymal stromal cells. Stem Cells Dev 23(20):2490–2500PubMedPubMedCentral Javorkova E, Trosan P, Zajicova A, Krulova M, Hajkova M, Holan V (2014) Modulation of the early inflammatory microenvironment in the alkali-burned eye by systemically administered interferon-gamma-treated mesenchymal stromal cells. Stem Cells Dev 23(20):2490–2500PubMedPubMedCentral
12.
go back to reference Yanez R, Lamana ML, Garcia-Castro J, Colmenero I, Ramirez M, Bueren JA (2006) Adipose tissue-derived mesenchymal stem cells have in vivo immunosuppressive properties applicable for the control of the graft-versus-host disease. Stem Cells 24(11):2582–2591PubMed Yanez R, Lamana ML, Garcia-Castro J, Colmenero I, Ramirez M, Bueren JA (2006) Adipose tissue-derived mesenchymal stem cells have in vivo immunosuppressive properties applicable for the control of the graft-versus-host disease. Stem Cells 24(11):2582–2591PubMed
13.
go back to reference Zhang L, Zheng H, Shao H, Nian H, Zhang Y, Bai L, Su C, Liu X, Dong L, Li X, Zhang X (2014) Long-term therapeutic effects of mesenchymal stem cells compared to dexamethasone on recurrent experimental autoimmune uveitis of rats. Invest Ophthalmol Vis Sci 55(9):5561–5571PubMedPubMedCentral Zhang L, Zheng H, Shao H, Nian H, Zhang Y, Bai L, Su C, Liu X, Dong L, Li X, Zhang X (2014) Long-term therapeutic effects of mesenchymal stem cells compared to dexamethasone on recurrent experimental autoimmune uveitis of rats. Invest Ophthalmol Vis Sci 55(9):5561–5571PubMedPubMedCentral
14.
go back to reference Ezquer M, Urzua CA, Montecino S, Leal K, Conget P, Ezquer F (2016) Intravitreal administration of multipotentmesenchymal stromal cells triggers a cytoprotective microenvironment in the retina of diabetic mice. Stem Cell Research & Therapy 16(7):42 Ezquer M, Urzua CA, Montecino S, Leal K, Conget P, Ezquer F (2016) Intravitreal administration of multipotentmesenchymal stromal cells triggers a cytoprotective microenvironment in the retina of diabetic mice. Stem Cell Research & Therapy 16(7):42
15.
go back to reference Oh JY, Kim MK, Shin MS, Wee WR, Lee JH (2009) Cytokine secretion by human mesenchymal stem cells cocultured with damaged corneal epithelial cells. Cytokine 46(1):100–103PubMed Oh JY, Kim MK, Shin MS, Wee WR, Lee JH (2009) Cytokine secretion by human mesenchymal stem cells cocultured with damaged corneal epithelial cells. Cytokine 46(1):100–103PubMed
16.
go back to reference Jiang DS, Muschhammer J, Qi Y, Kugler A, de Vries JC, Saffarzadeh M, Sindrilaru A, Beken SV, Wlaschek M, Kluth MA, Ganss C, Frank NY, Frank MH, Preissner KT, Scharffetter-Kochanek K (2016) Suppression of Neutrophil-Mediated Tissue Damage-A Novel Skill of Mesenchymal Stem Cells. Stem Cells 34(9):2393–2406PubMedPubMedCentral Jiang DS, Muschhammer J, Qi Y, Kugler A, de Vries JC, Saffarzadeh M, Sindrilaru A, Beken SV, Wlaschek M, Kluth MA, Ganss C, Frank NY, Frank MH, Preissner KT, Scharffetter-Kochanek K (2016) Suppression of Neutrophil-Mediated Tissue Damage-A Novel Skill of Mesenchymal Stem Cells. Stem Cells 34(9):2393–2406PubMedPubMedCentral
17.
go back to reference Mittal SK, Mashaghi A, Amouzegar A, Li MS, Foulsham W, Sahu SK, Chauhan SK (2018) Mesenchymal Stromal Cells Inhibit Neutrophil Effector Functions in a Murine Model of Ocular Inflammation. Invest Ophth Vis Sci 59(3):1191–1198 Mittal SK, Mashaghi A, Amouzegar A, Li MS, Foulsham W, Sahu SK, Chauhan SK (2018) Mesenchymal Stromal Cells Inhibit Neutrophil Effector Functions in a Murine Model of Ocular Inflammation. Invest Ophth Vis Sci 59(3):1191–1198
18.
go back to reference Philipp D, Suhr L, Wahlers T, Choi YH, Paunel-Gorgulu A (2018) Preconditioning of bone marrow-derived mesenchymal stem cells highly strengthens their potential to promote IL-6-dependent M2b polarization. Stem Cell Research & Therapy 9(1):286 Philipp D, Suhr L, Wahlers T, Choi YH, Paunel-Gorgulu A (2018) Preconditioning of bone marrow-derived mesenchymal stem cells highly strengthens their potential to promote IL-6-dependent M2b polarization. Stem Cell Research & Therapy 9(1):286
19.
go back to reference Fan LX, Hu CX, Chen JJ, Cen PP, Wang J, Li LJ (2016) Interaction between Mesenchymal Stem Cells and B-Cells. Int J MolSci 17(5):650 Fan LX, Hu CX, Chen JJ, Cen PP, Wang J, Li LJ (2016) Interaction between Mesenchymal Stem Cells and B-Cells. Int J MolSci 17(5):650
20.
go back to reference Oh JY, RG, Choi H, Lee RH, Ylöstalo JH, Rosa RH Jr, Prockop DJ. (2010) Anti-inflammatory protein TSG-6 reduces inflammatory damage to the cornea following chemical and mechanical injury. ProcNatlAcadSci U S A 107(39):16875–16880 Oh JY, RG, Choi H, Lee RH, Ylöstalo JH, Rosa RH Jr, Prockop DJ. (2010) Anti-inflammatory protein TSG-6 reduces inflammatory damage to the cornea following chemical and mechanical injury. ProcNatlAcadSci U S A 107(39):16875–16880
21.
go back to reference Haldar D, Henderson NC, Hirschfield G, Newsome PN (2016) Mesenchymal stromal cells and liver fibrosis: a complicated relationship. FASEB J 30(12):3905–3928PubMed Haldar D, Henderson NC, Hirschfield G, Newsome PN (2016) Mesenchymal stromal cells and liver fibrosis: a complicated relationship. FASEB J 30(12):3905–3928PubMed
22.
go back to reference Grange C, Tritta S, Tapparo M, Cedrino M, Tetta C, Camussi G, Brizzi MF (2019) Stem cell-derived extracellular vesicles inhibit and revert fibrosis progression in a mouse model of diabetic nephropathy. Sci Rep 9(1):4468PubMedPubMedCentral Grange C, Tritta S, Tapparo M, Cedrino M, Tetta C, Camussi G, Brizzi MF (2019) Stem cell-derived extracellular vesicles inhibit and revert fibrosis progression in a mouse model of diabetic nephropathy. Sci Rep 9(1):4468PubMedPubMedCentral
23.
go back to reference Usunier B, Benderitter M, Tamarat R, Chapel A (2014) (2014) Management of Fibrosis: The Mesenchymal Stromal Cells Breakthrough. Stem Cells Int 2014:340257PubMedPubMedCentral Usunier B, Benderitter M, Tamarat R, Chapel A (2014) (2014) Management of Fibrosis: The Mesenchymal Stromal Cells Breakthrough. Stem Cells Int 2014:340257PubMedPubMedCentral
24.
go back to reference Yao L, Li ZR, Su WR, Li YP, Lin ML, Zhang WX, Liu Y, Wan Q, Liang D (2012) Role of mesenchymal stem cells on cornea wound healing induced by acute alkali burn. PLoS ONE 7(2):e30842PubMedPubMedCentral Yao L, Li ZR, Su WR, Li YP, Lin ML, Zhang WX, Liu Y, Wan Q, Liang D (2012) Role of mesenchymal stem cells on cornea wound healing induced by acute alkali burn. PLoS ONE 7(2):e30842PubMedPubMedCentral
25.
go back to reference Su W, Wan Q, Huang J, Han L, Chen X, Chen G, Olsen N, Zheng SG, Liang D (2015a) Culture medium from TNF-α–stimulated mesenchymal stem cells attenuates allergic conjunctivitis through multiple antiallergic mechanisms. Journal of Allergy and Clinical Immunology 136(2):423-432.e428 Su W, Wan Q, Huang J, Han L, Chen X, Chen G, Olsen N, Zheng SG, Liang D (2015a) Culture medium from TNF-α–stimulated mesenchymal stem cells attenuates allergic conjunctivitis through multiple antiallergic mechanisms. Journal of Allergy and Clinical Immunology 136(2):423-432.e428
26.
go back to reference Ke Y, Wu Y, Cui X, Liu X, Yu M, Yang C, Li X (2015) Polysaccharide hydrogel combined with mesenchymal stem cells promotes the healing of corneal alkali burn in rats. PLoS ONE 10(3):e0119725PubMedPubMedCentral Ke Y, Wu Y, Cui X, Liu X, Yu M, Yang C, Li X (2015) Polysaccharide hydrogel combined with mesenchymal stem cells promotes the healing of corneal alkali burn in rats. PLoS ONE 10(3):e0119725PubMedPubMedCentral
27.
go back to reference Oh JY, Kim MK, Shin MS, Lee HJ, Ko JH, Wee WR, Lee JH (2008) The anti-inflammatory and anti-angiogenic role of mesenchymal stem cells in corneal wound healing following chemical injury. Stem Cells 26(4):1047–1055PubMed Oh JY, Kim MK, Shin MS, Lee HJ, Ko JH, Wee WR, Lee JH (2008) The anti-inflammatory and anti-angiogenic role of mesenchymal stem cells in corneal wound healing following chemical injury. Stem Cells 26(4):1047–1055PubMed
28.
go back to reference Choi H, Phillips C, Oh JY, Stock EM, Kim DK, Won JK, Fulcher S (2017) Comprehensive Modeling of Corneal Alkali Injury in the Rat Eye. Curr Eye Res 42(10):1348–1357PubMed Choi H, Phillips C, Oh JY, Stock EM, Kim DK, Won JK, Fulcher S (2017) Comprehensive Modeling of Corneal Alkali Injury in the Rat Eye. Curr Eye Res 42(10):1348–1357PubMed
29.
go back to reference Su WR, Zhang QZ, Shi SH, Nguyen AL, Le AD (2011) Human gingiva-derived mesenchymal stromal cells attenuate contact hypersensitivity via prostaglandin E2-dependent mechanisms. Stem Cells 29(11):1849–1860PubMed Su WR, Zhang QZ, Shi SH, Nguyen AL, Le AD (2011) Human gingiva-derived mesenchymal stromal cells attenuate contact hypersensitivity via prostaglandin E2-dependent mechanisms. Stem Cells 29(11):1849–1860PubMed
30.
go back to reference Ma Y, Xu Y, Xiao Z, Yang W, Zhang C, Song E, Du Y, Li L (2006) Reconstruction of chemically burned rat corneal surface by bone marrow-derived human mesenchymal stem cells. Stem Cells 24(2):315–321PubMed Ma Y, Xu Y, Xiao Z, Yang W, Zhang C, Song E, Du Y, Li L (2006) Reconstruction of chemically burned rat corneal surface by bone marrow-derived human mesenchymal stem cells. Stem Cells 24(2):315–321PubMed
31.
go back to reference Almaliotis D, Koliakos G, Papakonstantinou E, Komnenou A, Thomas A, Petrakis S, Nakos I, Gounari E, Karampatakis V (2015) Mesenchymal stem cells improve healing of the cornea after alkali injury. Graefes Arch ClinExpOphthalmol 253(7):1121–1135 Almaliotis D, Koliakos G, Papakonstantinou E, Komnenou A, Thomas A, Petrakis S, Nakos I, Gounari E, Karampatakis V (2015) Mesenchymal stem cells improve healing of the cornea after alkali injury. Graefes Arch ClinExpOphthalmol 253(7):1121–1135
32.
go back to reference Acar U, Pinarli FA, Acar DE, Beyazyildiz E, Sobaci G, Ozgermen BB, Sonmez AA, Delibasi T (2015) Effect of Allogeneic LimbalMesenchymal Stem Cell Therapy in Corneal Healing: Role of Administration Route. Ophthalmic Res 53(2):82–89PubMed Acar U, Pinarli FA, Acar DE, Beyazyildiz E, Sobaci G, Ozgermen BB, Sonmez AA, Delibasi T (2015) Effect of Allogeneic LimbalMesenchymal Stem Cell Therapy in Corneal Healing: Role of Administration Route. Ophthalmic Res 53(2):82–89PubMed
33.
go back to reference Shukla S, Mittal SK, Foulsham W, Elbasiony E, Singhania D, Sahu SK, Chauhan SK (2019) Therapeutic efficacy of different routes of mesenchymal stem cell administration in corneal injury. Ocular Surface 17(4):729–736 Shukla S, Mittal SK, Foulsham W, Elbasiony E, Singhania D, Sahu SK, Chauhan SK (2019) Therapeutic efficacy of different routes of mesenchymal stem cell administration in corneal injury. Ocular Surface 17(4):729–736
34.
go back to reference Yan L, Zheng DJ, Xu RH (2018) Critical Role of Tumor Necrosis Factor Signaling in Mesenchymal Stem Cell-Based Therapy for Autoimmune and inflammatory Diseases. Front Immunol 9(20):1658PubMedPubMedCentral Yan L, Zheng DJ, Xu RH (2018) Critical Role of Tumor Necrosis Factor Signaling in Mesenchymal Stem Cell-Based Therapy for Autoimmune and inflammatory Diseases. Front Immunol 9(20):1658PubMedPubMedCentral
35.
go back to reference English K, Barry FP, Field-Corbett CP, Mahon BP (2007) IFN-gamma and TNF-alpha differentially regulate immunomodulation by murine mesenchymal stem cells. ImmunolLett 110(2):91–100 English K, Barry FP, Field-Corbett CP, Mahon BP (2007) IFN-gamma and TNF-alpha differentially regulate immunomodulation by murine mesenchymal stem cells. ImmunolLett 110(2):91–100
36.
go back to reference Broekman, W, Amatngalim, GD, de Mooij-Eijk, Y, Oostendorp, J, Roelofs, H, Taube, C, Stolk, J, Hiemstra, PS. (2016) TNF-alpha and IL-1beta-activated human mesenchymal stromal cells increase airway epithelial wound healing in vitro via activation of the epidermal growth factor receptor. Respir Res. 173. Broekman, W, Amatngalim, GD, de Mooij-Eijk, Y, Oostendorp, J, Roelofs, H, Taube, C, Stolk, J, Hiemstra, PS. (2016) TNF-alpha and IL-1beta-activated human mesenchymal stromal cells increase airway epithelial wound healing in vitro via activation of the epidermal growth factor receptor. Respir Res. 173.
37.
go back to reference Saika S, Ikeda K, Yamanaka O, Flanders KC, Okada Y, Miyamoto T, Kitano A, Ooshima A, Nakajima Y, Ohnishi Y, Kao WW (2006) Loss of tumor necrosis factor alpha potentiates transforming growth factor beta-mediated pathogenic tissue response during wound healing. Am J Pathol 168(6):1848–1860PubMedPubMedCentral Saika S, Ikeda K, Yamanaka O, Flanders KC, Okada Y, Miyamoto T, Kitano A, Ooshima A, Nakajima Y, Ohnishi Y, Kao WW (2006) Loss of tumor necrosis factor alpha potentiates transforming growth factor beta-mediated pathogenic tissue response during wound healing. Am J Pathol 168(6):1848–1860PubMedPubMedCentral
38.
go back to reference Kim YS, HJP, Moon Hwa Hong, Peter M. Kang, James P. Morgan, Myung Ho Jeong, JeongGwan Cho, Jong Chun Park, YoungkeunAhn, (2009) TNF-alpha enhances engraftment of mesenchymal stem cells into infarcted myocardium. Front Biosci 1(14):2845–2856 Kim YS, HJP, Moon Hwa Hong, Peter M. Kang, James P. Morgan, Myung Ho Jeong, JeongGwan Cho, Jong Chun Park, YoungkeunAhn, (2009) TNF-alpha enhances engraftment of mesenchymal stem cells into infarcted myocardium. Front Biosci 1(14):2845–2856
39.
go back to reference Miettinen JA, PM, Salonen RJ, Ohlmeier S, Ylitalo K, Huikuri HV, Lehenkari P. (2011) Tumor necrosis factor alpha promotes the expression of immunosuppressive proteins and enhances the cell growth in a human bone marrow-derived stem cell culture. Exp Cell Res 317(6):791–801PubMed Miettinen JA, PM, Salonen RJ, Ohlmeier S, Ylitalo K, Huikuri HV, Lehenkari P. (2011) Tumor necrosis factor alpha promotes the expression of immunosuppressive proteins and enhances the cell growth in a human bone marrow-derived stem cell culture. Exp Cell Res 317(6):791–801PubMed
40.
go back to reference Ren G, Zhang L, Zhao X, Xu G, Zhang Y, Roberts AI, Zhao RC, Shi Y (2008) Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide. Cell Stem Cell 2(2):141–150PubMed Ren G, Zhang L, Zhao X, Xu G, Zhang Y, Roberts AI, Zhao RC, Shi Y (2008) Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide. Cell Stem Cell 2(2):141–150PubMed
41.
go back to reference Lee MJ, Kim J, Kim MY, Bae YS, Ryu SH, Lee TG, Kim JH (2010) Proteomic analysis of tumor necrosis factor-alpha-induced secretome of human adipose tissue-derived mesenchymal stem cells. J Proteome Res 9(4):1754–1762PubMed Lee MJ, Kim J, Kim MY, Bae YS, Ryu SH, Lee TG, Kim JH (2010) Proteomic analysis of tumor necrosis factor-alpha-induced secretome of human adipose tissue-derived mesenchymal stem cells. J Proteome Res 9(4):1754–1762PubMed
42.
go back to reference Miettinen JA, Pietila M, Salonen RJ, Ohlmeier S, Ylitalo K, Huikuri HV, Lehenkari P (2011) Tumor necrosis factor alpha promotes the expression of immunosuppressive proteins and enhances the cell growth in a human bone marrow-derived stem cell culture. Exp Cell Res 317(6):791–801PubMed Miettinen JA, Pietila M, Salonen RJ, Ohlmeier S, Ylitalo K, Huikuri HV, Lehenkari P (2011) Tumor necrosis factor alpha promotes the expression of immunosuppressive proteins and enhances the cell growth in a human bone marrow-derived stem cell culture. Exp Cell Res 317(6):791–801PubMed
43.
go back to reference Saika S, Miyamoto T, Yamanaka O, Kato T, Ohnishi Y, Flanders KC, Ikeda K, Nakajima Y, Kao WW, Sato M, Muragaki Y, Ooshima A (2005) Therapeutic effect of topical administration of SN50, an inhibitor of nuclear factor-kappaB, in treatment of corneal alkali burns in mice. Am J Pathol 166(5):1393–1403PubMedPubMedCentral Saika S, Miyamoto T, Yamanaka O, Kato T, Ohnishi Y, Flanders KC, Ikeda K, Nakajima Y, Kao WW, Sato M, Muragaki Y, Ooshima A (2005) Therapeutic effect of topical administration of SN50, an inhibitor of nuclear factor-kappaB, in treatment of corneal alkali burns in mice. Am J Pathol 166(5):1393–1403PubMedPubMedCentral
44.
go back to reference Su W, Wan Q, Huang J, Han L, Chen X, Chen G, Olsen N, Zheng SG, Liang D (2015b) Culture medium from TNF-alpha-stimulated mesenchymal stem cells attenuates allergic conjunctivitis through multiple antiallergic mechanisms. J Allergy ClinImmunol 136(2):423-432.e8 Su W, Wan Q, Huang J, Han L, Chen X, Chen G, Olsen N, Zheng SG, Liang D (2015b) Culture medium from TNF-alpha-stimulated mesenchymal stem cells attenuates allergic conjunctivitis through multiple antiallergic mechanisms. J Allergy ClinImmunol 136(2):423-432.e8
45.
go back to reference Lin KJ, Loi MX, Lien GS, Cheng CF, Pao HY, Chang YC, Ji AT, Ho JH (2013) Topical administration of orbital fat-derived stem cells promotes corneal tissue regeneration. Stem Cell Res Ther 4(3):72PubMedPubMedCentral Lin KJ, Loi MX, Lien GS, Cheng CF, Pao HY, Chang YC, Ji AT, Ho JH (2013) Topical administration of orbital fat-derived stem cells promotes corneal tissue regeneration. Stem Cell Res Ther 4(3):72PubMedPubMedCentral
46.
go back to reference Myrna KE, Mendonsa R, Russell P, Pot SA, Liliensiek SJ, Jester JV, Nealey PF, Brown D, Murphy CJ (2012) Substratum topography modulates corneal fibroblast to myofibroblast transformation. Invest Ophthalmol Vis Sci 53(2):811–816PubMedPubMedCentral Myrna KE, Mendonsa R, Russell P, Pot SA, Liliensiek SJ, Jester JV, Nealey PF, Brown D, Murphy CJ (2012) Substratum topography modulates corneal fibroblast to myofibroblast transformation. Invest Ophthalmol Vis Sci 53(2):811–816PubMedPubMedCentral
47.
go back to reference De Miguel MP, Alio J, Arnalich-Montiel F, Fuentes-Julian S, de Benito-Llopis L, Amparo F, Bataille L (2010) Cornea and ocular surface treatment. Curr Stem Cell Res Ther 5(2):195–204PubMed De Miguel MP, Alio J, Arnalich-Montiel F, Fuentes-Julian S, de Benito-Llopis L, Amparo F, Bataille L (2010) Cornea and ocular surface treatment. Curr Stem Cell Res Ther 5(2):195–204PubMed
48.
go back to reference Choi H, Lee RH, Bazhanov N, Oh JY, Prockop DJ (2011) Anti-inflammatory protein TSG-6 secreted by activated MSCs attenuates zymosan-induced mouse peritonitis by decreasing TLR2/NF-kappaB signaling in resident macrophages. Blood 118(2):330–338PubMedPubMedCentral Choi H, Lee RH, Bazhanov N, Oh JY, Prockop DJ (2011) Anti-inflammatory protein TSG-6 secreted by activated MSCs attenuates zymosan-induced mouse peritonitis by decreasing TLR2/NF-kappaB signaling in resident macrophages. Blood 118(2):330–338PubMedPubMedCentral
49.
go back to reference Qi Y, Jiang D, Sindrilaru A, Stegemann A, Schatz S, Treiber N, Rojewski M, Schrezenmeier H, Vander Beken S, Wlaschek M, Bohm M, Seitz A, Scholz N, Durselen L, Brinckmann J, Ignatius A, Scharffetter-Kochanek K (2014) TSG-6 released from intradermally injected mesenchymal stem cells accelerates wound healing and reduces tissue fibrosis in murine full-thickness skin wounds. J Invest Dermatol 134(2):526–537PubMed Qi Y, Jiang D, Sindrilaru A, Stegemann A, Schatz S, Treiber N, Rojewski M, Schrezenmeier H, Vander Beken S, Wlaschek M, Bohm M, Seitz A, Scholz N, Durselen L, Brinckmann J, Ignatius A, Scharffetter-Kochanek K (2014) TSG-6 released from intradermally injected mesenchymal stem cells accelerates wound healing and reduces tissue fibrosis in murine full-thickness skin wounds. J Invest Dermatol 134(2):526–537PubMed
50.
go back to reference Prockop DJ, Oh JY (2012) Mesenchymal stem/stromal cells (MSCs): role as guardians of inflammation. MolTher 20(1):14–20 Prockop DJ, Oh JY (2012) Mesenchymal stem/stromal cells (MSCs): role as guardians of inflammation. MolTher 20(1):14–20
51.
go back to reference Torricelli AA, Wilson SE (2014) Cellular and extracellular matrix modulation of corneal stromal opacity. Exp Eye Res (129): 151–160 Torricelli AA, Wilson SE (2014) Cellular and extracellular matrix modulation of corneal stromal opacity. Exp Eye Res (129): 151–160
52.
go back to reference ME F (1999) Keratocyte and fibroblast phenotypes in the repairing cornea. ProgRetin Eye Res 18(4):529–551 ME F (1999) Keratocyte and fibroblast phenotypes in the repairing cornea. ProgRetin Eye Res 18(4):529–551
53.
go back to reference Navas A, Magaña-Guerrero FS, Domínguez-López A, Chávez-García C, Partido G, Graue-Hernández EO, Sánchez-García FJ, Garfias Y (2018) Anti-Inflammatory and Anti-Fibrotic Effects of Human Amniotic Membrane Mesenchymal Stem Cells and Their Potential in Corneal Repair. STEM CELLS Translational Medicine 7(12):906–917PubMedPubMedCentral Navas A, Magaña-Guerrero FS, Domínguez-López A, Chávez-García C, Partido G, Graue-Hernández EO, Sánchez-García FJ, Garfias Y (2018) Anti-Inflammatory and Anti-Fibrotic Effects of Human Amniotic Membrane Mesenchymal Stem Cells and Their Potential in Corneal Repair. STEM CELLS Translational Medicine 7(12):906–917PubMedPubMedCentral
54.
go back to reference Mindrescu C, Le J, Wisniewski HG, Vilcek J (2005) Up-regulation of cyclooxygenase-2 expression by TSG-6 protein in macrophage cell line. BiochemBiophys Res Commun 330(3):737–745 Mindrescu C, Le J, Wisniewski HG, Vilcek J (2005) Up-regulation of cyclooxygenase-2 expression by TSG-6 protein in macrophage cell line. BiochemBiophys Res Commun 330(3):737–745
55.
go back to reference Lee TH, Wisniewski HG, Vilcek J (1992) A novel secretory tumor necrosis factor-inducible protein (TSG-6) is a member of the family of hyaluronate binding proteins, closely related to the adhesion receptor CD44. J Cell Biol 116(2):545–557PubMed Lee TH, Wisniewski HG, Vilcek J (1992) A novel secretory tumor necrosis factor-inducible protein (TSG-6) is a member of the family of hyaluronate binding proteins, closely related to the adhesion receptor CD44. J Cell Biol 116(2):545–557PubMed
56.
go back to reference Roddy GW, Oh JY, Lee RH, Bartosh TJ, Ylostalo J, Coble K, Rosa RH Jr, Prockop DJ (2011) Action at a distance: systemically administered adult stem/progenitor cells (MSCs) reduce inflammatory damage to the cornea without engraftment and primarily by secretion of TNF-alpha stimulated gene/protein 6. Stem Cells 29(10):1572–1579PubMed Roddy GW, Oh JY, Lee RH, Bartosh TJ, Ylostalo J, Coble K, Rosa RH Jr, Prockop DJ (2011) Action at a distance: systemically administered adult stem/progenitor cells (MSCs) reduce inflammatory damage to the cornea without engraftment and primarily by secretion of TNF-alpha stimulated gene/protein 6. Stem Cells 29(10):1572–1579PubMed
Metadata
Title
Subconjunctival injection of tumor necrosis factor-α pre-stimulated bone marrow-derived mesenchymal stem cells enhances anti-inflammation and anti-fibrosis in ocular alkali burns
Authors
Nuan Zhang
Xiaohui Luo
Shiyao Zhang
Ren Liu
Lingyi Liang
Wenru Su
Dan Liang
Publication date
01-04-2021
Publisher
Springer Berlin Heidelberg
Keyword
Indomethacin
Published in
Graefe's Archive for Clinical and Experimental Ophthalmology / Issue 4/2021
Print ISSN: 0721-832X
Electronic ISSN: 1435-702X
DOI
https://doi.org/10.1007/s00417-020-05017-8

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