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Quantitative proteomics analysis of human vitreous in rhegmatogenous retinal detachment associated with choroidal detachment by data-independent acquisition mass spectrometry

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Abstract

The prognosis of rhegmatogenous retinal detachment (RRD) with choroidal detachment (RRDCD) is often poor and complicated. This study focused on the identification of the characteristic proteins and signal pathways associated with the etiology of RRDCD and to provide guidance for diagnosis and treatment of RRDCD. In this study, vitreous humor samples were obtained from 16 RRDCD patients, 14 with RRD, 12 with idiopathic epiretinal macular membrane (IEMM), and 5 healthy controls from donated corpse eyes. Data-independent acquisition mass spectrometry and bioinformatics analysis were employed to identify differentially expressed proteins (DEPs). In the vitreous humor, 14,842 peptides were identified. Patients with RRDCD had 249 DEPs (93 upregulated and 156 downregulated), with 89 in patients with RRD and 61 in patients with IEMM. Enrichment analysis of the GO and Kyoto Encyclopedia of Genes and Genomes DEP databases indicated functional clusters related to inflammation and immunity, protein degradation and absorption, cell adhesion molecules (CAMs), the hedgehog signaling pathway, and lipid metabolism. Weighted gene co-expression network analysis showed that DEPs with positive co-expression of RRDCD participated in immune-related pathways led by the complement and coagulation cascade, whereas DEPs with negative co-expression of RRDCD participated in protein degradation and absorption, CAMs, and the hedgehog signaling pathway. In summary, our study provides important clues and the theoretical basis for exploring the pathogenesis, progression, and prognosis of ocular fundus disease.

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Data availability

The datasets analyzed during the current study are available from the corresponding author on reasonable request.

References

  1. Yu Y, An M, Mo B, Yang Z, Liu W (2016) Risk factors for choroidal detachment following rhegmatogenous retinal detachment in a chinese population. BMC Ophthalmol 16:140. https://doi.org/10.1186/s12886-016-0319-9

    Article  PubMed  PubMed Central  Google Scholar 

  2. Zhu J, Xu X, Zhang X (2002) Surgical therapeutic results of rhegmatogenous retinal detachment associated with choroidal detachment. Zhonghua Yan Ke Za Zhi 38:135–139

    PubMed  Google Scholar 

  3. Jarrett WH 2nd (1981) Rhematogenous retinal detachment complicated by severe intraocular inflammation, hypotony, and choroidal detachment. Trans Am Ophthalmol Soc 79:664–683

    PubMed  PubMed Central  Google Scholar 

  4. Li Z, Li Y, Huang X, yu Cai X, Chen X, Li S, Huang Y, Lu L (2012) Quantitative analysis of rhegmatogenous retinal detachment associated with choroidal detachment in Chinese using UBM. Retina 32:2020–2025

    Article  Google Scholar 

  5. Gu Y-H, Ke G-J, Wang L, Gu Q-H, Zhou E-L, Pan H-B, Wang S-Y (2016) Risk factors of rhegmatogenous retinal detachment associated with choroidal detachment in Chinese patients. Int J Ophthalmol 9:989

    PubMed  PubMed Central  Google Scholar 

  6. Adelman R, Parnes A, Sipperley J, Ducournau D (2013) European Vitreo-Retinal Society (EVRS) retinal detachment study group. Strategy for the management of complex retinal detachments. Ophthalmology 120:1809–1813. https://doi.org/10.1016/j.ophtha.2013.01.056

    Article  PubMed  Google Scholar 

  7. Wei Y, Wang N, Chen F, Wang H, Bi C, Zu Z, Yang X (2014) Vitrectomy combined with periocular/intravitreal injection of steroids for rhegmatogenous retinal detachment associated with choroidal detachment. Retina 34:136–141. https://doi.org/10.1097/IAE.0b013e3182923463

    Article  CAS  PubMed  Google Scholar 

  8. Seelenfreund MH, Kraushar MF, Schepens CL, Freilich DB (1974) Choroidal detachment associated with primary retinal detachment. Arch Ophthalmol 91:254–258. https://doi.org/10.1001/archopht.1974.03900060264003

    Article  CAS  PubMed  Google Scholar 

  9. Meyer JG, Schilling B (2017) Clinical applications of quantitative proteomics using targeted and untargeted data-independent acquisition techniques. Expert Rev Proteomics 14:419–429. https://doi.org/10.1080/14789450.2017.1322904

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Gillet LC, Navarro P, Tate S, Röst H, Selevsek N, Reiter L, Bonner R, Aebersold R (2012) Targeted data extraction of the MS/MS spectra generated by data-independent acquisition: a new concept for consistent and accurate proteome analysis. Mol Cell Proteomics 11(O111):016717. https://doi.org/10.1074/mcp.O111.016717

    Article  CAS  PubMed  Google Scholar 

  11. Ku X, Sun Q, Zhu L, Gu Z, Han Y, Xu N, Meng C, Yang X, Yan W, Fang W (2020) Deciphering tissue-based proteome signatures revealed novel subtyping and prognostic markers for thymic epithelial tumors. Mol Oncol 14:721–741. https://doi.org/10.1002/1878-0261.12642

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Wu Z, Ding N, Yu M, Wang K, Luo S, Zou W, Zhou Y, Yan B, Jiang Q (2016) Identification of potential biomarkers for rhegmatogenous retinal detachment associated with choroidal detachment by vitreous iTRAQ-based proteomic profiling. Int J Mol Sci. https://doi.org/10.3390/ijms17122052

    Article  PubMed  PubMed Central  Google Scholar 

  13. Jian C, Fu J, Cheng X, Shen LJ, Ji YX, Wang X, Pan S, Tian H, Tian S, Liao R, Song K, Wang HP, Zhang X, Wang Y, Huang Z, She ZG, Zhang XJ, Zhu L, Li H (2020) Low-Dose Sorafenib Acts as a Mitochondrial Uncoupler and Ameliorates Nonalcoholic Steatohepatitis. Cell Metab 31:892-908.e11. https://doi.org/10.1016/j.cmet.2020.04.011

    Article  CAS  PubMed  Google Scholar 

  14. Ma J, Chen T, Wu S, Yang C, Bai M, Shu K, Li K, Zhang G, Jin Z, He F (2019) iProX: an integrated proteome resource. Nucleic Acids Res 47:D1211–D1217

    Article  Google Scholar 

  15. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504. https://doi.org/10.1101/gr.1239303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Giulietti M, Occhipinti G, Principato G, Piva F (2017) Identification of candidate miRNA biomarkers for pancreatic ductal adenocarcinoma by weighted gene co-expression network analysis. Cell Oncol 40:181–192. https://doi.org/10.1007/s13402-017-0315-y

    Article  CAS  Google Scholar 

  17. Liu M, Pi H, Xi Y, Wang L, Tian L, Chen M, Xie J, Deng P, Zhang T, Zhou C, Liang Y, Zhang L, He M, Lu Y, Chen C, Yu Z, Zhou Z (2020) KIF5A-dependent axonal transport deficiency disrupts autophagic flux in trimethyltin chloride-induced neurotoxicity. Autophagy. https://doi.org/10.1080/15548627.2020.1739444

    Article  PubMed  PubMed Central  Google Scholar 

  18. MacLean B, Tomazela DM, Shulman N, Chambers M, Finney GL, Frewen B, Kern R, Tabb DL, Liebler DC, MacCoss MJ (2010) Skyline: an open source document editor for creating and analyzing targeted proteomics experiments. Bioinformatics 26:966–968. https://doi.org/10.1093/bioinformatics/btq054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Bansal R, Khan MM, Dasari S, Verma I, Goodlett DR, Manes NP, Nita-Lazar A, Sharma SP, Kumar A, Singh N, Chakraborti A, Gupta V, Dogra MR, Ram J, Gupta A (2021) Proteomic profile of vitreous in patients with tubercular uveitis. Tuberculosis 126:102036. https://doi.org/10.1016/j.tube.2020.102036

    Article  CAS  PubMed  Google Scholar 

  20. Wei Q, Jiang C, Ye X, Huang X, Jin H, Xu G (2019) Vitreous proteomics provides new insights into antivascular endothelial growth factor therapy for pathologic myopia choroid neovascularization. J Interferon Cytokine Res 39:786–796. https://doi.org/10.1089/jir.2019.0030

    Article  CAS  PubMed  Google Scholar 

  21. Dai Y, Wu Z, Sheng H, Zhang Z, Yu M, Zhang Q (2015) Identification of inflammatory mediators in patients with rhegmatogenous retinal detachment associated with choroidal detachment. Mol Vis 21:417–427

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Geller SF, Lewis GP, Anderson DH, Fisher SK (1995) Use of the MIB-1 antibody for detecting proliferating cells in the retina. Invest Ophthalmol Vis Sci 36:737–744

    CAS  PubMed  Google Scholar 

  23. Takahashi S, Adachi K, Suzuki Y, Maeno A, Nakazawa M (2016) Profiles of inflammatory cytokines in the vitreous fluid from patients with rhegmatogenous retinal detachment and their correlations with clinical features. Biomed Res Int 2016:4256183. https://doi.org/10.1155/2016/4256183

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Dillingh MR, van den Blink B, Moerland M, van Dongen MG, Levi M, Kleinjan A, Wijsenbeek MS, Lupher ML Jr, Harper DM, Getsy JA, Hoogsteden HC, Burggraaf J (2013) Recombinant human serum amyloid P in healthy volunteers and patients with pulmonary fibrosis. Pulm Pharmacol Ther 26:672–676. https://doi.org/10.1016/j.pupt.2013.01.008

    Article  CAS  PubMed  Google Scholar 

  25. Behrens NE, Lipke PN, Pilling D, Gomer RH, Klotz SA (2019) Serum Amyloid P component binds fungal surface amyloid and decreases human macrophage phagocytosis and secretion of inflammatory cytokines. MBio 10:e00218–e00219. https://doi.org/10.1128/mBio.00218-19

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Vilahur G, Badimon L (2015) Biological actions of pentraxins. Vascul Pharmacol 73:38–44. https://doi.org/10.1016/j.vph.2015.05.001

    Article  CAS  PubMed  Google Scholar 

  27. Kolstoe SE, Ridha BH, Bellotti V, Wang N, Robinson CV, Crutch SJ, Keir G, Kukkastenvehmas R, Gallimore JR, Hutchinson WL, Hawkins PN, Wood SP, Rossor MN, Pepys MB (2009) Molecular dissection of Alzheimer,s disease neuropathology by depletion of serum amyloid P component. Proc Natl Acad Sci USA 106:7619–7623. https://doi.org/10.1073/pnas.0902640106

    Article  PubMed  PubMed Central  Google Scholar 

  28. Luo Z, Lei H, Sun Y, Liu X, Su DF (2015) Orosomucoid, an acute response protein with multiple modulating activities. J Physiol Biochem 71:329–340. https://doi.org/10.1007/s13105-015-0389-9

    Article  CAS  PubMed  Google Scholar 

  29. Jo M, Kim J, Song G, Seo M, Hwang E, Suk K (2017) Astrocytic Orosomucoid-2 modulates microglial activation and neuroinflammation. J Neurosci 37:2878–2894. https://doi.org/10.1523/jneurosci.2534-16.2017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Sabry R, El-Madbouly A, Abozeid H, Hassan M (2018) Urinary Orosomucoid - 2 and soluble CD14 as potential biomarkers for assessment of disease activity in rheumatoid arthritis. Egypt J Immunol 25:107–116

    PubMed  Google Scholar 

  31. Yu M, Wu Z, Zhang Z, Huang X, Zhang Q (2015) Metabolomic analysis of human vitreous in rhegmatogenous retinal detachment associated with choroidal detachment. Invest Ophthalmol Vis Sci 56:5706–5713. https://doi.org/10.1167/iovs.14-16338

    Article  PubMed  Google Scholar 

  32. Kerr MA (1990) The structure and function of human IgA. Biochem J 271:285–296. https://doi.org/10.1042/bj2710285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. McHeyzer-Williams M, Okitsu S, Wang N, McHeyzer-Williams L (2011) Molecular programming of B cell memory. Nat Rev Immunol 12:24–34. https://doi.org/10.1038/nri3128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Schroeder HW Jr, Cavacini L (2010) Structure and function of immunoglobulins. J Allergy Clin Immunol 125:S41-52. https://doi.org/10.1016/j.jaci.2009.09.046

    Article  PubMed  PubMed Central  Google Scholar 

  35. Baudouin C, Fredj-Reygrobellet D, Gordon WC, Baudouin F, Peyman G, Lapalus P, Gastaud P, Bazan NG (1990) Immunohistologic study of epiretinal membranes in proliferative vitreoretinopathy. Am J Ophthalmol 110:593–598. https://doi.org/10.1016/s0002-9394(14)77054-0

    Article  CAS  PubMed  Google Scholar 

  36. Grisanti S, Wiedemann P, Heimann K (1993) Proliferative vitreoretinopathy. On the significance of protein transfer through the blood-retina barrier. Ophthalmologe 90:468–471

    CAS  PubMed  Google Scholar 

  37. Jongbloets BC, Ramakers GM, Pasterkamp RJ (2013) Semaphorin7A and its receptors: pleiotropic regulators of immune cell function, bone homeostasis, and neural development. Semin Cell Dev Biol 24:129–138. https://doi.org/10.1016/j.semcdb.2013.01.002

    Article  CAS  PubMed  Google Scholar 

  38. Song Y, Wang L, Zhang L, Huang D (2021) The involvement of semaphorin 7A in tumorigenic and immunoinflammatory regulation. J Cell Physiol. https://doi.org/10.1002/jcp.30340

    Article  PubMed  Google Scholar 

  39. Suzuki K, Okuno T, Yamamoto M, Pasterkamp RJ, Takegahara N, Takamatsu H, Kitao T, Takagi J, Rennert PD, Kolodkin AL, Kumanogoh A, Kikutani H (2007) Semaphorin 7A initiates T-cell-mediated inflammatory responses through alpha1beta1 integrin. Nature 446:680–684. https://doi.org/10.1038/nature05652

    Article  CAS  PubMed  Google Scholar 

  40. Chen S, Jen A, Gentleman S, Jen L (1999) Effects of bFGF and TGFbeta on the expression of amyloid precursor and B-cell lymphoma protooncogene proteins in the rat retina. NeuroReport 10:509–512. https://doi.org/10.1097/00001756-199902250-00012

    Article  CAS  PubMed  Google Scholar 

  41. Cavallaro U, Dejana E (2011) Adhesion molecule signalling: not always a sticky business. Nat Rev Mol Cell Biol 12:189–197. https://doi.org/10.1038/nrm3068

    Article  CAS  PubMed  Google Scholar 

  42. Martins T, Eusebio N, Correia A, Marinho J, Casares F, Pereira PS (2017) TGFβ/Activin signalling is required for ribosome biogenesis and cell growth in <i>Drosophila</i> salivary glands. Open Biol 7:160258. https://doi.org/10.1098/rsob.160258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Lutty GA, Merges C, Threlkeld AB, Crone S, McLeod DS (1993) Heterogeneity in localization of isoforms of TGF-beta in human retina, vitreous, and choroid. Invest Ophthalmol Vis Sci 34:477–487

    CAS  PubMed  Google Scholar 

  44. Bai Y, Liang S, Yu W, Zhao M, Huang L, Zhao M, Li X (2014) Semaphorin 3A blocks the formation of pathologic choroidal neovascularization induced by transforming growth factor beta. Mol Vis 20:1258–1270

    PubMed  PubMed Central  Google Scholar 

  45. Kawahara S, Hata Y, Kita T, Arita R, Miura M, Nakao S, Mochizuki Y, Enaida H, Kagimoto T, Goto Y, Hafezi-Moghadam A, Ishibashi T (2008) Potent inhibition of cicatricial contraction in proliferative vitreoretinal diseases by statins. Diabetes 57:2784–2793. https://doi.org/10.2337/db08-0302

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Connor TB Jr, Roberts AB, Sporn MB, Danielpour D, Dart LL, Michels RG, de Bustros S, Enger C, Kato H, Lansing M et al (1989) Correlation of fibrosis and transforming growth factor-beta type 2 levels in the eye. J Clin Invest 83:1661–1666. https://doi.org/10.1172/jci114065

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Carrington L, McLeod D, Boulton M (2000) IL-10 and antibodies to TGF-beta2 and PDGF inhibit RPE-mediated retinal contraction. Invest Ophthalmol Vis Sci 41:1210–1216

    CAS  PubMed  Google Scholar 

  48. Yao H, Ge T, Zhang Y, Li M, Yang S, Li H, Wang F (2019) BMP7 antagonizes proliferative vitreoretinopathy through retinal pigment epithelial fibrosis in vivo and in vitro. Faseb j 33:3212–3224. https://doi.org/10.1096/fj.201800858RR

    Article  CAS  PubMed  Google Scholar 

  49. Dvashi Z, Goldberg M, Adir O, Shapira M, Pollack A (2015) TGF-β1 induced transdifferentiation of rpe cells is mediated by TAK1. PLoS ONE 10:e0122229. https://doi.org/10.1371/journal.pone.0122229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Zheng XZ, Du LF, Wang HP (2010) An immunohistochemical analysis of a rat model of proliferative vitreoretinopathy and a comparison of the expression of TGF-β and PDGF among the induction methods. Bosn J Basic Med Sci 10:204–209. https://doi.org/10.17305/bjbms.2010.2686

    Article  PubMed  PubMed Central  Google Scholar 

  51. Palomares-Ordóñez JL, Sánchez-Ramos JA, Ramírez-Estudillo JA, Robles-Contreras A (2019) Correlation of transforming growth factor β-1 vitreous levels with clinical severity of proliferative vitreoretinopathy in patients with rhegmatogenous retinal detachment. Arch Soc Esp Oftalmol 94:12–17. https://doi.org/10.1016/j.oftal.2018.08.002

    Article  PubMed  Google Scholar 

  52. Shinomura T, Nishida Y, Ito K, Kimata K (1993) cDNA cloning of PG-M, a large chondroitin sulfate proteoglycan expressed during chondrogenesis in chick limb buds. Alternative spliced multiforms of PG-M and their relationships to versican. J Biol Chem 268:14461–14469

    Article  CAS  Google Scholar 

  53. Keenan TD, Clark SJ, Unwin RD, Ridge LA, Day AJ, Bishop PN (2012) Mapping the differential distribution of proteoglycan core proteins in the adult human retina, choroid, and sclera. Invest Ophthalmol Vis Sci 53:7528–7538. https://doi.org/10.1167/iovs.12-10797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Inoue Y, Yoneda M, Miyaishi O, Iwaki M, Zako M (2009) Hyaluronan dynamics during retinal development. Brain Res 1256:55–60. https://doi.org/10.1016/j.brainres.2008.12.023

    Article  CAS  PubMed  Google Scholar 

  55. Ohno-Jinno A, Isogai Z, Yoneda M, Kasai K, Miyaishi O, Inoue Y, Kataoka T, Zhao JS, Li H, Takeyama M, Keene DR, Sakai LY, Kimata K, Iwaki M, Zako M (2008) Versican and fibrillin-1 form a major hyaluronan-binding complex in the ciliary body. Invest Ophthalmol Vis Sci 49:2870–2877. https://doi.org/10.1167/iovs.07-1488

    Article  PubMed  Google Scholar 

  56. Theocharis DA, Skandalis SS, Noulas AV, Papageorgakopoulou N, Theocharis AD, Karamanos NK (2008) Hyaluronan and chondroitin sulfate proteoglycans in the supramolecular organization of the mammalian vitreous body. Connect Tissue Res 49:124–128. https://doi.org/10.1080/03008200802148496

    Article  CAS  PubMed  Google Scholar 

  57. Osterwalder T, Cinelli P, Baici A, Pennella A, Krueger SR, Schrimpf SP, Meins M, Sonderegger P (1998) The axonally secreted serine proteinase inhibitor, neuroserpin, inhibits plasminogen activators and plasmin but not thrombin. J Biol Chem 273:2312–2321. https://doi.org/10.1074/jbc.273.4.2312

    Article  CAS  PubMed  Google Scholar 

  58. Lebeurrier N, Liot G, Lopez-Atalaya JP, Orset C, Fernandez-Monreal M, Sonderegger P, Ali C, Vivien D (2005) The brain-specific tissue-type plasminogen activator inhibitor, neuroserpin, protects neurons against excitotoxicity both in vitro and in vivo. Mol Cell Neurosci 30:552–558. https://doi.org/10.1016/j.mcn.2005.09.005

    Article  CAS  PubMed  Google Scholar 

  59. Yepes M, Sandkvist M, Wong MK, Coleman TA, Smith E, Cohan SL, Lawrence DA (2000) Neuroserpin reduces cerebral infarct volume and protects neurons from ischemia-induced apoptosis. Blood 96:569–576

    Article  CAS  Google Scholar 

  60. Gu RP, Fu LL, Jiang CH, Xu YF, Wang X, Yu J (2015) Retina is protected by neuroserpin from ischemic/reperfusion-induced injury independent of tissue-type plasminogen activator. PLoS ONE 10:e0130440. https://doi.org/10.1371/journal.pone.0130440

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Gupta V, Mirzaei M, Gupta VB, Chitranshi N, Dheer Y, Vander Wall R, Abbasi M, You Y, Chung R, Graham S (2017) Glaucoma is associated with plasmin proteolytic activation mediated through oxidative inactivation of neuroserpin. Sci Rep 7:8412–8412. https://doi.org/10.1038/s41598-017-08688-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Brand Y, Sung M, Pak K, Chavez E, Wei E, Radojevic V, Bodmer D, Ryan A (2015) Neural cell adhesion molecule NrCAM is expressed in the mammalian inner ear and modulates spiral ganglion neurite outgrowth in an in vitro alternate choice assay. J Mol Neurosci 55:836–844. https://doi.org/10.1007/s12031-014-0436-y

    Article  CAS  PubMed  Google Scholar 

  63. Qu S-C, Xu D, Li T-T, Zhang J-F, Liu F (2019) iTRAQ-based proteomics analysis of aqueous humor in patients with dry age-related macular degeneration. Int J Ophthalmol 12:1758–1766. https://doi.org/10.18240/ijo.2019.11.15

    Article  PubMed  PubMed Central  Google Scholar 

  64. Nüsslein-Volhard C, Wieschaus E (1980) Mutations affecting segment number and polarity in Drosophila. Nature 287:795–801. https://doi.org/10.1038/287795a0

    Article  PubMed  Google Scholar 

  65. Nilsson DE (2004) Eye evolution: a question of genetic promiscuity. Curr Opin Neurobiol 14:407–414. https://doi.org/10.1016/j.conb.2004.07.004

    Article  CAS  PubMed  Google Scholar 

  66. Cavodeassi F, Creuzet S, Etchevers HC (2019) The hedgehog pathway and ocular developmental anomalies. Hum Genet 138:917–936. https://doi.org/10.1007/s00439-018-1918-8

    Article  PubMed  Google Scholar 

  67. Cvekl A, Duncan MK (2007) Genetic and epigenetic mechanisms of gene regulation during lens development. Prog Retin Eye Res 26:555–597. https://doi.org/10.1016/j.preteyeres.2007.07.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Donnai D, Barrow M (1993) Diaphragmatic hernia, exomphalos, absent corpus callosum, hypertelorism, myopia, and sensorineural deafness: a newly recognized autosomal recessive disorder? Am J Med Genet 47:679–682. https://doi.org/10.1002/ajmg.1320470518

    Article  CAS  PubMed  Google Scholar 

  69. Kantarci S, Al-Gazali L, Hill RS, Donnai D, Black GC, Bieth E, Chassaing N, Lacombe D, Devriendt K, Teebi A, Loscertales M, Robson C, Liu T, MacLaughlin DT, Noonan KM, Russell MK, Walsh CA, Donahoe PK, Pober BR (2007) Mutations in LRP2, which encodes the multiligand receptor megalin, cause Donnai-Barrow and facio-oculo-acoustico-renal syndromes. Nat Genet 39:957–959. https://doi.org/10.1038/ng2063

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Pober BR, Longoni M, Noonan KM (2009) A review of Donnai-Barrow and facio-oculo-acoustico-renal (DB/FOAR) syndrome: clinical features and differential diagnosis. Birth Defects Res A Clin Mol Teratol 85:76–81. https://doi.org/10.1002/bdra.20534

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Collery RF, Link BA (2019) Precise short sequence insertion in zebrafish using a CRISPR/Cas9 approach to generate a constitutively soluble Lrp2 protein. Front Cell Develop Biol 7:167–167. https://doi.org/10.3389/fcell.2019.00167

    Article  Google Scholar 

  72. Cases O, Joseph A, Obry A, Santin MD, Ben-Yacoub S, Pâques M, Amsellem-Levera S, Bribian A, Simonutti M, Augustin S, Debeir T, Sahel JA, Christ A, de Castro F, Lehéricy S, Cosette P, Kozyraki R (2015) Foxg1-Cre mediated Lrp2 inactivation in the developing mouse neural retina, ciliary and retinal pigment epithelia models congenital high myopia. PLoS ONE 10:e0129518. https://doi.org/10.1371/journal.pone.0129518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Veth KN, Willer JR, Collery RF, Gray MP, Willer GB, Wagner DS, Mullins MC, Udvadia AJ, Smith RS, John SW, Gregg RG, Link BA (2011) Mutations in zebrafish lrp2 result in adult-onset ocular pathogenesis that models myopia and other risk factors for glaucoma. PLoS Genet 7:e1001310. https://doi.org/10.1371/journal.pgen.1001310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Collery R, Link B (2018) Proteolytic processing of LRP2 on RPE cells regulates BMP activity to control eye size and refractive error

  75. Christ A, Marczenke M, Willnow TE (2020) LRP2 controls sonic hedgehog-dependent differentiation of cardiac progenitor cells during outflow tract formation. Hum Mol Genet 29:3183–3196. https://doi.org/10.1093/hmg/ddaa200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Christ A, Christa A, Kur E, Lioubinski O, Bachmann S, Willnow TE, Hammes A (2012) LRP2 is an auxiliary SHH receptor required to condition the forebrain ventral midline for inductive signals. Dev Cell 22:268–278. https://doi.org/10.1016/j.devcel.2011.11.023

    Article  CAS  PubMed  Google Scholar 

  77. Christ A, Christa A, Klippert J, Eule JC, Bachmann S, Wallace VA, Hammes A, Willnow TE (2015) LRP2 Acts as SHH clearance receptor to protect the retinal margin from mitogenic stimuli. Dev Cell 35:36–48. https://doi.org/10.1016/j.devcel.2015.09.001

    Article  CAS  PubMed  Google Scholar 

  78. Cases O, Perea-Gomez A, Aguiar DP, Nykjaer A, Amsellem S, Chandellier J, Umbhauer M, Cereghini S, Madsen M, Collignon J, Verroust P, Riou JF, Creuzet SE, Kozyraki R (2013) Cubilin, a high affinity receptor for fibroblast growth factor 8, is required for cell survival in the developing vertebrate head. J Biol Chem 288:16655–16670. https://doi.org/10.1074/jbc.M113.451070

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Spoelgen R, Hammes A, Anzenberger U, Zechner D, Andersen OM, Jerchow B, Willnow TE (2005) LRP2/megalin is required for patterning of the ventral telencephalon. Development 132:405–414. https://doi.org/10.1242/dev.01580

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank the Shanghai Applied Protein Technology Co., Ltd. (APTBIO) for technological assistance.

Funding

This study was supported by the Social Development Project of Jiangsu Provincial Science and Technology Department (BE2017627), the high-end talent project of Wuxi Health Committee, the youth project of Wuxi Health Committee (Q202038), and the reserve top talent project of Wuxi Municipal Health Commission (HB2020032).

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Authors

Contributions

Conceptualization, ZW and SL; methodology, SL and HX; formal analysis, SL; investigation, SL, HX, LY, and XG; resources, JS and XC; writing—original draft preparation, SL and HX; writing—review and editing, ZW.

Corresponding author

Correspondence to Zhifeng Wu.

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The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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Luo, S., Xu, H., Yang, L. et al. Quantitative proteomics analysis of human vitreous in rhegmatogenous retinal detachment associated with choroidal detachment by data-independent acquisition mass spectrometry. Mol Cell Biochem 477, 1849–1863 (2022). https://doi.org/10.1007/s11010-022-04409-0

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