Periostin and tenascin-C interaction promotes angiogenesis in ischemic proliferative retinopathy.
Aged
Animals
Cell Adhesion Molecules
/ genetics
Cells, Cultured
Diabetic Retinopathy
/ pathology
Endothelial Cells
/ metabolism
Female
Humans
Interleukin-13
/ metabolism
Male
Mice
Mice, Inbred C57BL
Mice, Knockout
Middle Aged
Neovascularization, Pathologic
/ pathology
Retinal Vessels
/ growth & development
Tenascin
/ genetics
Vitreoretinopathy, Proliferative
/ pathology
Vitreous Body
/ metabolism
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
09 06 2020
09 06 2020
Historique:
received:
16
09
2019
accepted:
18
05
2020
entrez:
11
6
2020
pubmed:
11
6
2020
medline:
15
12
2020
Statut:
epublish
Résumé
Ischemic proliferative retinopathy (IPR), such as proliferative diabetic retinopathy (PDR), retinal vein occlusion and retinopathy of prematurity is a major cause of vision loss. Our previous studies demonstrated that periostin (PN) and tenascin-C (TNC) are involved in the pathogenesis of IPR. However, the interactive role of PN and TNC in angiogenesis associated with IPR remain unknown. We found significant correlation between concentrations of PN and TNC in PDR vitreous humor. mRNA and protein expression of PN and TNC were found in pre-retinal fibrovascular membranes excised from PDR patients. Interleukin-13 (IL-13) promoted mRNA and protein expression of PN and TNC, and co-immunoprecipitation assay revealed binding between PN and TNC in human microvascular endothelial cells (HRECs). IL-13 promoted angiogenic functions of HRECs. Single inhibition of PN or TNC and their dual inhibition by siRNA suppressed the up-regulated angiogenic functions. Pathological pre-retinal neovessels of oxygen-induced retinopathy (OIR) mice were attenuated in PN knock-out, TNC knock-out and dual knock-out mice compared to wild-type mice. Both in vitro and in vivo, PN inhibition had a stronger inhibitory effect on angiogenesis compared to TNC inhibition, and had a similar effect to dual inhibition of PN and TNC. Furthermore, PN knock-out mice showed scant TNC expression in pre-retinal neovessels of OIR retinas. Our findings suggest that interaction of PN and TNC facilitates pre-retinal angiogenesis, and PN is an effective therapeutic target for IPR such as PDR.
Identifiants
pubmed: 32518264
doi: 10.1038/s41598-020-66278-1
pii: 10.1038/s41598-020-66278-1
pmc: PMC7283227
doi:
Substances chimiques
Cell Adhesion Molecules
0
Interleukin-13
0
POSTN protein, human
0
TNC protein, human
0
Tenascin
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
9299Références
Lee, P., Wang, C. C. & Adamis, A. P. Ocular neovascularization: an epidemiologic review. Surv Ophthalmol. 43, 3 (1998).
doi: 10.1016/S0039-6257(98)00035-6
Hernández-Da Mota, S. E. & Nuñez-Solorio, S. M. Experience with intravitreal bevacizumab as a preoperative adjunct in 23-G vitrectomy for advanced proliferative diabetic retinopathy. Eur. J. Ophthalmol. 20, 1047–1052 (2010).
pubmed: 20491044
doi: 10.1177/112067211002000604
Zhao, X. Y., Xia, S. & Chen, Y. X. Antivascular endothelial growth factor agents pretreatment before vitrectomy for complicated proliferative diabetic retinopathy: A meta-analysis of randomised controlled trials. Br. J. Ophthalmol. 102, 1077–1085 (2018).
pubmed: 29246890
doi: 10.1136/bjophthalmol-2017-311344
Beck, M., Munk, M. R., Ebneter, A., Wolf, S. & Zinkernagel, M. S. Retinal Ganglion Cell Layer Change in Patients Treated With Anti-Vascular Endothelial Growth Factor for Neovascular Age-related Macular Degeneration. Am. J. Ophthalmol. 167, 10–17 (2016).
pubmed: 27084000
doi: 10.1016/j.ajo.2016.04.003
Nishijima, K. et al. Vascular Endothelial Growth Factor-A Is a Survival Factor for Retinal Neurons and a Critical Neuroprotectant during the Adaptive Response to Ischemic Injury. Am. J. Pathol. 171, 53–67 (2007).
pubmed: 17591953
pmcid: 1941589
doi: 10.2353/ajpath.2007.061237
Van Geest, R. J. et al. A shift in the balance of vascular endothelial growth factor and connective tissue growth factor by bevacizumab causes the angiofibrotic switch in proliferative diabetic retinopathy. Br. J. Ophthalmol. 96, 587–590 (2012).
pubmed: 22289291
pmcid: 3308470
doi: 10.1136/bjophthalmol-2011-301005
Li, J.-K. et al. Changes in vitreous VEGF, bFGF and fibrosis in proliferative diabetic retinopathy after intravitreal bevacizumab. Int. J. Ophthalmol. 8, 1202–1206 (2015).
pubmed: 26682173
pmcid: 4651889
Zhang, Q. et al. The relationship between anti-vascular endothelial growth factor and fibrosis in proliferative retinopathy: Clinical and laboratory evidence. Br. J. Ophthalmol. 100, 1443–1450 (2016).
pubmed: 27531356
doi: 10.1136/bjophthalmol-2015-308199
Arevalo, J. F. et al. Tractional retinal detachment following intravitreal bevacizumab (Avastin) in patients with severe proliferative diabetic retinopathy. Br. J. Ophthalmol. 92, 213–216 (2008).
pubmed: 17965108
doi: 10.1136/bjo.2007.127142
Ishikawa, K. et al. Microarray analysis of gene expression in fibrovascular membranes excised from patients with proliferative diabetic retinopathy. Invest. Ophthalmol. Vis. Sci. 56, 932–946 (2015).
pubmed: 25604687
doi: 10.1167/iovs.14-15589
Ling, L., Cheng, Y., Ding, L. & Yang, X. Association of serum periostin with cardiac function and short-term prognosis in acute myocardial infarction patients. PLoS One. 9, 1–8 (2014).
Mitamura, Y. et al. The IL-13/periostin/IL-24 pathway causes epidermal barrier dysfunction in allergic skin inflammation. Allergy. 73, 1881–1891 (2018).
pubmed: 29528494
doi: 10.1111/all.13437
Liu, Y. et al. Periostin promotes tumor angiogenesis in pancreatic cancer via Erk/VEGF signaling. Oncotarget. 7, 40148–40159 (2016).
pubmed: 27223086
pmcid: 5129999
doi: 10.18632/oncotarget.9512
Taki, J. et al. Dynamic Expression of Tenascin-C After Myocardial Ischemia and Reperfusion: Assessment by 125I-Anti-Tenascin-C Antibody Imaging. J. Nucl. Med. 51, 1116–1122 (2010).
pubmed: 20554738
doi: 10.2967/jnumed.109.071340
Ogawa, K., Ito, M., Takeuchi, K. & Nakada, A. Tenascin-C is upregulated in the skin lesions of patients with atopic dermatitis. J Dermatol Sci. 40, 35–41 (2005).
pubmed: 16043328
doi: 10.1016/j.jdermsci.2005.06.001
Calvo, A. et al. Identification of VEGF-regulated genes associated with increased lung metastatic potential: functional involvement of tenascin-C in tumor growth and lung metastasis. Oncogene. 27, 5373–5384 (2008).
pubmed: 18504437
pmcid: 2702869
doi: 10.1038/onc.2008.155
Yoshida, S. et al. Increased expression of periostin in vitreous and fibrovascular membranes obtained from patients with proliferative diabetic retinopathy. Invest. Ophthalmol. Vis. Sci. 52, 5670–5678 (2011).
pubmed: 21508107
doi: 10.1167/iovs.10-6625
Ishikawa, K. et al. Periostin promotes the generation of fibrous membranes in proliferative vitreoretinopathy. FASEB J. 28, 131–142 (2014).
pubmed: 24022401
doi: 10.1096/fj.13-229740
Nakama, T. et al. Therapeutic Effect of Novel Single-Stranded RNAi Agent Targeting Periostin in Eyes with Retinal Neovascularization. Mol. Ther. Nucleic Acids. 6, 279–289 (2017).
pubmed: 28325294
pmcid: 5363510
doi: 10.1016/j.omtn.2017.01.004
Kobayashi, Y. et al. Tenascin-C promotes angiogenesis in fibrovascular membranes in eyes with proliferative diabetic retinopathy. Mol. Vis. 22, 436–45 (2016).
pubmed: 27186070
pmcid: 4859161
Brem, R. B. et al. Immunolocalization of integrins in the human retina. Invest. Ophthalmol. Vis. Sci. 35, 3466–3474 (1994).
pubmed: 8056522
Uemura, A. et al. Tlx acts as a proangiogenic switch by regulating extracellular assembly of fibronectin matrices in retinal astrocytes. J. Clin. Invest. 116, 369–377 (2006).
pubmed: 16424942
pmcid: 1332029
doi: 10.1172/JCI25964
Stenzel, D. et al. Integrin-dependent and -independent functions of astrocytic fibronectin in retinal angiogenesis. Development. 138, 4451–4463 (2011).
pubmed: 21880786
pmcid: 3177315
doi: 10.1242/dev.071381
Robbins, S. G. et al. Immunolocalization of Integrins in Proliferative Retinal Membranes. Invest. Ophthalmol. Vis. Sci. 35, 3475–3485 (1994).
pubmed: 8056523
Casaroli Marano, R. P., Preissner, K. T. & Vilaró, S. Fibronectin, laminin, vitronectin and their receptors at newly-formed capillaries in proliferative diabetic retinopathy. Exp. Eye Res. 60, 5–17 (1995).
pubmed: 7536680
doi: 10.1016/S0014-4835(05)80079-X
McLeod, D. et al. A chronic grey matter penumbra, lateral microvascular intussusception and venous peduncular avulsion underlie diabetic vitreous haemorrhage. Br. J. Ophthalmol. 91, 677–689 (2007).
pubmed: 17446507
pmcid: 1954739
doi: 10.1136/bjo.2006.109199
Takayama, G. et al. Periostin: A novel component of subepithelial fibrosis of bronchial asthma downstream of IL-4 and IL-13 signals. J. Allergy Clin. Immunol. 118, 98–104 (2006).
pubmed: 16815144
doi: 10.1016/j.jaci.2006.02.046
Kudo, A. & Kii, I. Periostin function in communication with extracellular matrices. J. Cell Commun. Signal. 12, 301–308 (2018).
pubmed: 29086200
doi: 10.1007/s12079-017-0422-6
Kii, I. et al. Incorporation of Tenascin-C into the Extracellular Matrix by Periostin Underlies an Extracellular Meshwork Architecture. J. Biol. Chem. 285, 2028–2039 (2009).
pubmed: 19887451
pmcid: 2804360
doi: 10.1074/jbc.M109.051961
Sirica, A. E., Almenara, J. A. & Li, C. Periostin in intrahepatic cholangiocarcinoma: Pathobiological insights and clinical implications. Exp. Mol. Pathol. 97, 515–524 (2014).
pubmed: 25446840
pmcid: 4262539
doi: 10.1016/j.yexmp.2014.10.007
Yoshida, S. et al. Increased expression of M-CSF and IL-13 in vitreous of patients with proliferative diabetic retinopathy: implications for M2 macrophage-involving fibrovascular membrane formation. Br. J. Ophthalmol. 1–6 (2015).
Kaelin, W. G. Jr. & Ratcliffe, P. J. Oxygen Sensing by Metazoans: The Central Role of the HIF Hydroxylase Pathway. Mol. Cell. 30, 393–402 (2008).
pubmed: 18498744
doi: 10.1016/j.molcel.2008.04.009
Rey, S. & Semenza, G. L. Hypoxia-inducible factor-1-dependent mechanisms of vascularization and vascular remodelling. Cardiovasc. Res. 86, 236–242 (2010).
pubmed: 20164116
pmcid: 2856192
doi: 10.1093/cvr/cvq045
Fukushi, J. et al. The Activity of Soluble VCAM-1 in Angiogenesis Stimulated by IL-4 and IL-13. J. Immunol. 165, 2818–2823 (2000).
pubmed: 10946314
doi: 10.4049/jimmunol.165.5.2818
Kwee, B. J. et al. CD4 T-cells regulate angiogenesis and myogenesis. Biomaterials. 178, 109–121 (2018).
pubmed: 29920403
pmcid: 6090550
doi: 10.1016/j.biomaterials.2018.06.003
Takagi, K. et al. IL-13 enhances mesenchymal transition of pulmonary artery endothelial cells via down-regulation of miR-424 / 503 in vitro. Cell. Signal. 42, 270–280 (2018).
pubmed: 29102771
doi: 10.1016/j.cellsig.2017.10.019
Wynn, T. A. Type 2 cytokines: mechanisms and therapeutic strategies. Nat. Rev. Immunol. 15, 271–282 (2015).
pubmed: 25882242
doi: 10.1038/nri3831
Hendrix, S. & Nitsch, R. The role of T helper cells in neuroprotection and regeneration. J. Neuroimmunol. 184, 100–112 (2007).
pubmed: 17198734
doi: 10.1016/j.jneuroim.2006.11.019
Imanaka-yoshida, K. & Yoshida, T. Tenascin-C in Development and Disease of Blood Vessels. Anat. Rec. 297, 1747–1757 (2014).
doi: 10.1002/ar.22985
John, M. W., Juan, E. D. & Machemer, R. Ultrastructural Characteristics of New Vessels in Proliferative Diabetic Retinopathy. Am. J. Ophthalmol. 105, 491–499 (1988).
doi: 10.1016/0002-9394(88)90240-1
Saito, Y., Uppal, A., Byfield, G., Budd, S. & Hartnett, M. E. Activated NAD(P)H oxidase from supplemental oxygen induces neovascularization independent of VEGF in retinopathy of prematurity model. Invest Ophthalmol Vis Sci. 49, 1591–1598 (2008).
pubmed: 18385079
pmcid: 2362384
doi: 10.1167/iovs.07-1356
Stahl, A. et al. The Mouse Retina as an Angiogenesis Model. Invest Ophthalmol Vis Sci. 51, 2813–2826 (2010).
pubmed: 20484600
pmcid: 2891451
doi: 10.1167/iovs.10-5176
Nakama, T. et al. Inhibition of choroidal fibrovascular membrane formation by new class of RNA interference therapeutic agent targeting periostin. Gene Ther. 22, 127–137 (2015).
pubmed: 25503692
doi: 10.1038/gt.2014.112
Network, W. C. for the D. R. C. R. Panretinal Photocoagulation vs Intravitreous Ranibizumab for Proliferative Diabetic Retinopathy A Randomized Clinical Trial. JAMA 314, 2137–2146 (2015).
doi: 10.1001/jama.2015.15217
Ogura, Y. et al. Clinical practice pattern in management of diabetic macular edema in Japan: survey results of Japanese retinal specialists. Jpn. J. Ophthalmol. 61, 43–50 (2017).
pubmed: 27722786
doi: 10.1007/s10384-016-0481-x
Terasaki, H., Ogura, Y., Kitano, S., Sakamoto, T. & Murata, T. Management of diabetic macular edema in Japan: a review and expert opinion. Jpn. J. Ophthalmol. 62, 1–23 (2018).
pubmed: 29210010
doi: 10.1007/s10384-017-0537-6
Rofagha, S. et al. Seven-Year Outcomes in Ranibizumab-Treated Patients in ANCHOR, MARINA, and HORIZON A Multicenter Cohort Study (SEVEN-UP). Ophthalmology. 120, 2292–2299 (2013).
pubmed: 23642856
doi: 10.1016/j.ophtha.2013.03.046
Connor, K. M. et al. Quantification of oxygen-induced retinopathy in the mouse: a model of vessel loss, vessel regrowth and pathological angiogenesis. Nat. Protoc. 4, 1565–1573 (2009).
pubmed: 19816419
pmcid: 3731997
doi: 10.1038/nprot.2009.187