Sequence features, structure, ligand interaction, and diseases in small leucine rich repeat proteoglycans

Abdelkader E, AlHilali S, Neuhaus C, Bergmann C, AlMurshed T, Schatz P (2018) Congenital stationary night blindness associated with morning glory disc malformation: a novel hemizygous mutation in CACNA1F. Ophthalmic Genet 39:659–661. https://doi.org/10.1080/13816810.2018.1498526 Acharya M, Mookherjee S, Bhattacharjee A, Thakur SK, Bandyopadhyay AK, Sen A, Chakrabarti S, Ray K (2007) Evaluation of the OPTC gene in primary open angle glaucoma: functional significance of a silent change. BMC Mol Biol 8:21 Ahmad SAI, Anam MB, Ito N, Ohta K (2018) Involvement of Tsukushi in diverse developmental processes. J Cell Commun Signal 12:205–210. https://doi.org/10.1007/s12079-018-0452-8 AlTalbishi A, Zelinger L, Zeitz C, Hendler K, Namburi P, Audo I, Sheffer R, Yahalom C, Khateb S, Banin E, Sharon D (2019) RPM1 Mutations are the most common cause of autosomal recessive congenital stationary night blindness (CSNB) in the Palestinian and Israeli populations. Sci Rep 9:12047. https://doi.org/10.1038/s41598-019-46811-7 Batkhishig D, Bilguun K, Enkhbayar P, Miyashita H, Kretsinger RH, Matsushima N (2018) Super secondary structure consisting of a polyproline II helix and a β-turn in leucine rich repeats in bacterial type III secretion system effectors. Protein J 37:223–236. https://doi.org/10.1007/s10930-018-9767-9 Batkhishig D, Enkhbayar P, Kretsinger RH, Matsushima N (2020) A strong correlation between consensus sequences and unique super secondary structures in leucine rich repeats. Proteins 88:840–852. https://doi.org/10.1002/prot.25876 Batkhishig D, Enkhbayar P, Kretsinger RH, Matsushima N (2021) A crucial residue in the hydrophobic core of the solenoid structure of leucine rich repeats. Biochim Biophys Acta Proteins Proteom 1869:140631 Bech-Hansen NT, Naylor MJ, Maybaum TA, Sparkes RL, Koop B, Birch DG, Bergen AA, Prinsen CF, Polomeno RC, Gal A, Drack AV, Musarella MA, Jacobson SG, Young RS, Weleber RG (2000) Mutations in NYX, encoding the leucine-rich proteoglycan nyctalopin, cause X-linked complete congenital stationary night blindness. Nat Genet 26:319–323 Bella J, Hindle L, McEwan PA, Lovell SC (2008) The leucine-rich repeat structure. Cell Mol Life Sci 65:2307–2333 Bengtsson E, Aspberg A, Heinegard D, Sommarin Y, Spillmann D (2000) The amino-terminal part of PRELP binds to heparin and heparan sulfate. J Biol Chem 275:40695–40702. https://doi.org/10.1074/jbc.M007917200 Bredrup C, Knappskog PM, Majewski J, Rødahl E, Boman H (2005) Congenital stromal dystrophy of the cornea caused by a mutation in the decorin gene. Investig Ophthalmol Vis Sci 46:420–426. https://doi.org/10.1167/iovs.04-0804 Burley SK, Petsko GA (1985) Aromatic-aromatic interaction: a mechanism of protein structure stabilization. Science 229:23–28. https://doi.org/10.1126/science.3892686 Cai XB, Shen SR, Chen DF, Zhang Q, Jin ZB (2019) An overview of myopia genetics. Exp Eye Res 188:107778. https://doi.org/10.1016/j.exer.2019.107778 Chebrek C, Leonard S, de Brevern AG, Gelly JC (2014) PolyprOnline: polyproline helix II and secondary structure assignment database. Database 2009:1–14 Chen S, Birk DE (2013) The regulatory roles of small leucine-rich proteoglycans in extracellular assembly. FEBS J 280:2120–2137. https://doi.org/10.1111/febs.12136 Chen S, Sun M, Meng X, Iozzo RV, Kao WW, Birk DE (2011) Pathophysiological mechanisms of autosomal dominant congenital stromal corneal dystrophy: C-terminal-truncated decorin results in abnormal matrix assembly and altered expression of small leucine-rich proteoglycans. Am J Pathol 179:2409–2419. https://doi.org/10.1016/j.ajpath.2011.07.026 Chen S, Sun M, Iozzo RV, Kao WW, Birk DE (2013) Intracellularly-retained decorin lacking the C-terminal ear repeat causes ER stress: a cell-based etiological mechanism for congenital stromal corneal dystrophy. Am J Pathol 183:247–256. https://doi.org/10.1016/j.ajpath.2013.04.001 Cho SY, Bae JS, Kim NKD, Forzano F, Girisha KM, Baldo C, Faravelli F, Cho TJ, Kim D, Lee KY, Ikegawa S, Shim JS, Ko AR, Miyake N, Nishimura G, Superti-Furga A, Spranger J, Kim OH, Park WY, Jin DK (2016) BGN mutations in X-linked spondyloepimetaphyseal dysplasia. Am J Hum Genet 98:1243–1248 Dai S, Ying M, Wang K, Wang L, Han R, Hao P, Li N (2015) Two novel NYX gene mutations in the Chinese families with X-linked congenital stationary night blindness. Sci Rep 5:12679 Dan H, Song X, Li J, Xing Y, Li T (2017) Mutation screening of the LRIT3, CABP4, and GPR179 genes in Chinese patients with Schubert-Bornschein congenital stationary night blindness. Ophthalmic Genet 38:206–210 Dudakova L, Palos M, Hardcastle AJ, Liskova P (2014) Corneal endothelial findings in a Czech patient with compound heterozygous mutations in KERA. Ophthalmic Genet 35:252–254 Dudakova L, Vercruyssen JHJ, Balikova I, Postolache L, Leroy BP, Skalicka P, Liskova P (2018) Analysis of KERA in four families with cornea plana. Acta Ophthalmol 96(1):e87–e91. https://doi.org/10.1111/aos.13484 Ebenezer ND, Patel CB, Hariprasad SM, Chen LL, Patel RJ, Hardcastle AJ, Allen RC (2005) Clinical and molecular characterization of a family with autosomal ecessive cornea plana. Arch Ophthalmol 123:1248–1253 Enkhbayar P, Miyashita H, Kretsinger RH, Matsushima N (2014) Helical parameters and correlations of tandem leucine rich repeats in proteins. J Proteomics Bioinform 7:139–150 Forsius H, Damsten M, Eriksson AW, Fellman J, Lindh S, Tahvanainen E (1998) Autosomal recessive cornea plana. A clinical and genetic study of 78 cases in Finland. Acta Ophthalmol Scand 76:196–203 Gregg RG, Kamermans M, Klooster J, Lukasiewicz PD, Peachey NS, Vessey KA, McCall MA (2007) Nyctalopin expression in retinal bipolar cells restores visual function in a mouse model of complete X-linked congenital stationary night blindness. J Neurophysiol 98:3023–3033 Guidetti GF, Bartolini B, Bernardi B, Tira ME, Berndt MC, Balduini C, Torti M (2004) Binding of von Willebrand factor to the small proteoglycan decorin. FEBS Lett 574:95–100. https://doi.org/10.1016/j.febslet.2004.08.011 He XL, Bazan JF, McDermott G, Park JB, Wang K, Tessier-Lavigne M, He Z, Garcia KC (2003) Structure of the Nogo receptor ectodomain: a recognition module implicated in myelin inhibition. Neuron 38:177–185. https://doi.org/10.1016/s0896-6273(03)00232-0 Hildebrand A, Romarís M, Rasmussen LM, Heinegard D, Twardzik DR, Border WA, Ruoslahti E (1994) Interaction of the small interstitial proteoglycans biglycan, decorin and fibromodulin with transforming growth factor beta. Biochem J 302:527–534. https://doi.org/10.1042/bj3020527 Hindson VJ, Gallagher JT, Halfter W, Bishop PN (2019) Opticin binds to heparan and chondroitin sulfate proteoglycans. Arch Biochem Biophys 672:108053. https://doi.org/10.1167/iovs.05-0883 Iozzo RV, Schaefer L (2015) Proteoglycan form and function: a comprehensive nomenclature of proteoglycans. Matrix Biol 42:11–55. https://doi.org/10.1016/j.matbio.2015.02.003 Iozzo RV, Buraschi S, Genua M, Xu SQ, Solomides CC, Peiper SC, Gomella LG, Owens RC, Morrione A (2011) Decorin antagonizes IGF receptor I (IGF-IR) function by interfering with IGF-IR activity and attenuating downstream signaling. J Biol Chem 286:34712–43421. https://doi.org/10.1074/jbc.M111.262766 Islam M, Gor J, Perkins SJ, Ishikawa Y, Bächinger HP, Erhard Hohenester E (2013) The concave face of decorin mediates reversible dimerization and collagen binding. J Biol Chem 288:35526–35533. https://doi.org/10.1074/jbc.M113.504530 Ivanova ME, Zolnikova IV, Gorgisheli KV, Atarshchikov DS, Ghosh P, Barh D (2019) Novel frameshift mutation in NYX gene in a Russian family with complete congenital stationary night blindness. Ophthalmic Genet 40:558–563 Jensen MM, Karring H (2020) The origins and developments of sulfation-prone tyrosine-rich and acidic N- and C-terminal extensions of class ll and lll small leucine-rich repeat proteins shed light on connective tissue evolution in vertebrates. BMC Evol Biol 20:73. https://doi.org/10.1186/s12862-020-01634-3 Jing Y, Kumar PR, Zhu L, Edward DP, Tao S, Wang L, Chuck R, Zhang C (2014) Novel decorin mutation in a Chinese family with congenital stromal corneal dystrophy. Cornea 33:288–293. https://doi.org/10.1097/ICO.0000000000000055 Kajava AV (1998) Structural diversity of leucine-rich repeat proteins. J Mol Biol 277:519–527 Kajava AV, Anisimova M, Peeters N (2008) Origin and evolution of GALA-LRR, a new member of the CC-LRR subfamily: From plants to bacteria? PLoS ONE 3:e1694 Kalamajski S, Oldberg A (2007) Fibromodulin binds collagen type I via Glu-353 and Lys-355 in leucine-rich repeat 11. J Biol Chem 282:26740–26745. https://doi.org/10.1074/jbc.M704026200 Kalamajski S, Oldberg A (2009) Homologous sequence in lumican and fibromodulin leucine-rich repeat 5–7 competes for collagen binding. J Biol Chem 284:534–539. https://doi.org/10.1074/jbc.M805721200 Kalamajski S, Oldberg A (2010) The role of small leucine-rich proteoglycans in collagen fibrillogenesis. Matrix Biol 29:248–253 Kalamajski S, Aspberg A, Oldberg A (2007) The decorin sequence SYIRIADTNIT binds collagen type I. J Biol Chem 282:16062–16067. https://doi.org/10.1074/jbc.M700073200 Kalamajski S, Aspberg A, Lindblom K, Heinegård D, Oldberg A (2009) Asporin competes with decorin for collagen binding, binds calcium and promotes osteoblast collagen mineralization. Biochem J 423(1):53–59. https://doi.org/10.1042/BJ20090542 Kalamajski S, Bihan D, Bonna A, Rubin K, Farndale RW (2016) Fibromodulin interacts with collagen cross-linking sites and activates lysyl oxidase. J Biol Chem 291:7951–7960 Kanda R, Sutoh Y, Kasamatsu J, Maenaka K, Kasahara M, Ose T (2014) Crystal structure of the lamprey variable lymphocyte receptor C reveals an unusual feature in its N-terminal capping module. PLoS ONE 9:e85875. https://doi.org/10.1371/journal.pone.0085875 Khan AO (2018) Corneal ectasia in a boy with homozygous KERA mutation. Ophthalmic Genet 39:141–143. https://doi.org/10.1080/13816810.2017.1350724 Khan A, Kambouris M (2004) A novel KERA mutation associated with autosomal recessive cornea plana. Ophthalmic Genet 25:147–152 Khan AO, Aldahmesh M, Meyer B (2006) Recessive cornea plana in the Kingdom of Saudi Arabia. Ophthalmology 113:1773–1778. https://doi.org/10.1016/j.ophtha.[CNA2] Kim JH, Ko JM, Lee I, Kim JY, Kim MJ, Tchah H (2011) A novel mutation of the decorin gene identified in a Korean family with congenital hereditary stromal dystrophy. Cornea 30:1473–1477. https://doi.org/10.1097/ICO.0b013e3182137788 Kobe B, Deisenhofer J (1994) The leucine-rich repeat: a versatile binding motif. Trends Biochem Sci 19:415–421 Kobe B, Kajava AV (2001) The leucine-rich repeat as a protein recognition motif. Curr Opin Struct Biol 11:725–732 Kou I, Nakajima M, Ikegawa S (2010) Binding characteristics of the osteoarthritis-associated protein asporin. J Bone Miner Metab 28:395–402. https://doi.org/10.1007/s00774-009-0145-8 Kresse H, Liszio C, Schönherr E, Fisher LW (1997) Critical role of glutamate in a central leucine-rich repeat of decorin for interaction with type I collagen. J Biol Chem 272:18404–18410. https://doi.org/10.1074/jbc.272.29 Kumari D, Tiwari A, Choudhury M, Kumar A, Rao A, Dixit M (2016) A novel KERA mutation in a case of autosomal recessive cornea plana with primary angle-closure glaucoma. J Glaucoma 25:e106-109 Lee JH, Ki CS, Chung ES, Chung TY (2012) A novel decorin gene mutation in congenital hereditary stromal dystrophy: a Korean family. Korean J Ophthalmol 6:301–305. https://doi.org/10.3341/kjo.2012.26.4.301 Lehmann OJ, El-ashry MF, Ebenezer ND, Ocaka L, Francis PJ, Wilkie SE, Patel RJ, Ficker L, Jordan T, Khaw PT, Bhattacharya SS (2001) A novel keratocan mutation causing autosomal recessive cornea plana. Investig Ophthalmol Vis Sci 42:3118–3122 Leroy BP, Budde BS, Wittmer M, De Baere E, Berger W, Zeitz C (2009) A common NYX mutation in Flemish patients with X linked CSNB. Br J Ophthalmol 93:692–696 Liénart S, Merceron R, Vanderaa C, Lambert F, Colau D, Stockis J, van der Woning B, De Haard H, Saunders M, Coulie PG, Savvides SN, Lucas S (2018) Structural basis of latent TGF-β1 presentation and activation by GARP on human regulatory T cells. Science 362:952–956 Liskova P, Hysi PG, Williams D, Ainsworth JR, Shah S, de la Chapelle A, Tuft SJ, Bhattacharya SS (2007) Study of p.N247S KERA mutation in a British family with cornea plana. Mol Vis 13:1339–1347 Majava M, Bishop PN, Hagg P, Scott PG, Rice A, Inglehearn C, Hammond CJ, Spector TD, Ala-Kokko L, Mannikko M (2007) Novel mutations in the small leucine-rich repeat protein/proteoglycan (SLRP) genes in high myopia. Hum Mutat 28:336–344 Marmor MF, Zeitz C (2018) Riggs-type dominant congenital stationary night blindness: ERG findings, a new GNAT1 mutation and a systemic association. Doc Ophthalmol 137:57–62. https://doi.org/10.1007/s10633-018-9651-0 Matsushima N, Kamiya M (2000) Super-motifs of leucine-rich repeats (LRRs) proteins. Genom Inf 11:343–345 Matsushima N, Kretsinger R (2016) Leicine rich repeats: sequences, structures, ligand-interactions, and evolution. LAMBERT Academic Publishing, Saarbrücken Matsushima N, Ohyanagi T, Tanaka T, Kretsinger RH (2000) Super-motifs and evolution of tandem leucine-rich repeats within the small proteoglycans—biglycan, decorin, lumican, fibromodulin, PRELP, keratocan, osteoadherin, epiphycan, and osteoglycin. Proteins 38:210–225. https://doi.org/10.1002/(sici)1097-0134(20000201)38:2%3c210::aid-prot9%3e3.0.co;2-1 Matsushima N, Miyashita H, Mikami T, Kuroki Y (2010) A nested leucine rich repeat (LRR) domain: the precursor of LRRs is a ten or eleven residue motif. BMC Microbiol 10:235 Matsushima N, Takatsuka S, Miyashita H, Tamaki S, Kretsinger RH (2019) Leucine rich repeat proteins: Sequences, mutations, structures and diseases. Protein Pept Lett 26:108–131 Matsushima N, Miyashita H, Tamaki S, Kretsinger RH (2021) Shrinking of repeating unit length in leucine-rich repeats from double-stranded DNA viruses. Arch Virol 166:43–64 McEwan PA, Scott PG, Bishop PN, Bella J (2006) Structural correlations in the family of small leucine-rich repeat proteins and proteoglycans. J Struct Biol 155:294–305. https://doi.org/10.1016/j.jsb.2006.01.016 Meester JA, Vandeweyer G, Pintelon I, Lammens M, van Hoorick L, de Belder S, Waitzman K, Young L, Markham LW, Vogt J, Richer J, Beauchesne LM, Unger S, Superti-Furga A, Prsa M, Dhillon R, Reyniers E, Dietz HC, Wuyts W, Mortier G, Verstraeten A, van Laer L, Loeys BL (2017) Loss-of-function mutations in the X-linked biglycan gene cause a severe syndromic form of thoracic aortic aneurysms and dissections. Genet Med 19:386–395 Miyashita H, Kretsinger, RH, and Matsushima N. (2014) Comparative structural analysis of the extracellular regions of the insulin and epidermal growth factor receptors whose L1 and L2 domains have non-canonical, leucine rich repeats. Enliven: Bioinformatics 1:1–9. Morcavallo A, Buraschi S, Xu SQ, Belfiore A, Schaefer L, Iozzo RV, Morrione A (2014) Decorin differentially modulates the activity of insulin receptor isoform A ligands. Matrix Biol 35:82–90. https://doi.org/10.1016/j.matbio.2013.12.010 Nakajima M, Kizawa H, Saitoh M, Kou I, Miyazono K, Ikegawa S (2007) Mechanisms for asporin function and regulation in articular cartilage. J Biol Chem 282:32185–32192. https://doi.org/10.1074/jbc.M700522200 Niimori D, Kawano R, Felemban A, Niimori-Kita K, Tanaka H, Ihn H, Ohta K (2012) Tsukushi controls the hair cycle by regulating TGF-b1 signaling. Dev Biol 372:81–87. https://doi.org/10.1016/j.ydbio.2012.08.030 Ohta K, Lupo G, Kuriyama S, Keynes R, Holt CE, Harris WA, Tanaka H, Ohnuma S (2004) Tsukushi functions as an organizer inducer by inhibition of BMP activity in cooperation with chordin. Dev Cell 7:347–358. https://doi.org/10.1016/j.devcel.2004.08.014 Ohta K, Kuriyama S, Okafuji T, Gejima R, Ohnuma S, Tanaka H (2006) Tsukushi cooperates with VG1 to induce primitive streak and Hensen’s node formation in the chick embryo. Development 133:3777–3786. https://doi.org/10.1242/dev.02579 Ohta K, Ito A, Kuriyama S, Lupo G, Kosaka M, Ohnuma S, Nakagawa S, Tanaka H (2011) Tsukushi functions as a Wnt signaling inhibitor by competing with Wnt2b for binding to transmembrane protein Frizzled4. Proc Natl Acad Sci USA 108:14962–14967. https://doi.org/10.1073/pnas.1100513108 Ohta K, Aoyama E, Ahmad SAI, Ito N, Anam MB, Kubota S, Takigawa M (2019) CCN2/CTGF binds the small leucine rich proteoglycan protein Tsukushi. J Cell Commun Signal 13:113–118. https://doi.org/10.1007/s12079-018-0487-x Pal D, Chakrabarti P (2001) Non-hydrogen bond interactions involving the methionine sulfur atom. J Biomol Struct Dyn 19(115):128 Pang X, Dong N, Zheng Z (2020) Small leucine-rich proteoglycans in skin wound healing. Front Pharmacol 10:1649. https://doi.org/10.3389/fphar.2019.01649 Paracuellos P, Kalamajski S, Bonna A, Bihan D, Farndale RW, Erhard Hohenester E (2017) Structural and functional analysis of two small leucine-rich repeat proteoglycans, fibromodulin and chondroadherin. Matrix Biol 63:106–116. https://doi.org/10.1016/j.matbio.2017.02.002 Park H, Huxley-Jones J, Ray J, Boot-Handford P, Bishop PN, Attwood TK, Bella J (2008) LRRCE: a leucine-rich repeat cysteine capping motif unique to the chordate lineage. BMC Genom 9:599 Pearring JN, Bojang P Jr, Shen Y, Koike C, Furukawa T, Nawy S, Gregg RG (2011) A role for nyctalopin, a small leucine-rich repeat protein, in localizing the TRP melastatin 1 channel to retinal depolarizing bipolar cell dendrites. J Neurosci 31:10060–10066 Pellegata NS, Dieguez-Lucena JL, Joensuu T, Lau S, Montgomery KT, Krahe R, Kivela T, Kucherlapati R, Forsius H, de la Chapelle A (2000) Mutations in KERA, encoding keratocan, cause cornea plana. Nat Genet 25:91–95 Pietraszek-Gremplewicz K, Karamanou K, Niang A, Dauchez M, Belloy N, Maquart FX, Baud S, Brézillon S (2018) Small leucine-rich proteoglycans and matrix metalloproteinase-14: key partners? Matrix Biol 75–76:271–285 Pradhan M, Sharp D, Mora J, Wittmer M, Berger W, Vincent A (2011) A novel NYX mutation associated with X-linked congenital stationary night blindness in a New Zealand family. J Clin Exp Oohthamol 2:1–4 Pusch CM, Zeitz C, Brandau O, Pesch K, Achatz H, Feil S, Scharfe C, Maurer J, Jacobi FK, Pinckers A, Andreasson S, Hardcastle A, Wissinger B, Berger W, Meindl A (2000) The complete form of X-linked congenital stationary night blindness is caused by mutations in a gene encoding a leucine-rich repeat protein. Nat Genet 26:324–327 Ramisch S, Pramhed A, Tillgren V, Aspberg A, Logan DT (2017) Crystal structure of human chondroadherin: solving a difficult molecular-replacement problem using de novo models. Acta Crystallogr D Struct Biol 73:53–63 Rodahl E, Ginderdeuren RV, Knappskog PM, Bredrup C, Boman H (2006) A second decorin frame shift mutation in a family with congenital stromal corneal dystrophy. Am J Ophthalmol 142:520–521 Roedig H, Nastase MV, Frey H, Moreth K, Zeng-Brouwers J, Poluzzi C, Hsieh LT, Brandts C, Fulda S, Wygrecka M, Schaefer L (2019) Biglycan is a new high-affinity ligand for CD14 in macrophages. Matrix Biol 77:4–22. https://doi.org/10.1016/j.matbio.2018.05.006 Roos L, Bertelsen B, Harris P, Bygum A, Jensen H, Gronskov K, Tumer Z (2015) Case report: a novel KERA mutation associated with cornea plana and its predicted effect on protein function. BMC Med Genet 16:40 Sadler JE (2002) Biomedicine. Contact-how platelets touch von Willebrand factor. Science 297:1128–1129. https://doi.org/10.1126/science Santra M, Reed CC, Iozzo RV (2002) Decorin binds to a narrow region of the epidermal growth factor (EGF) receptor, partially overlapping but distinct from the EGF-binding epitope. J Biol Chem 277:35671–35681. https://doi.org/10.1074/jbc.M205317200 Schaefer L, Babelova A, Kiss E, Hausser HJ, Baliova M, Krzyzankova M, Marsche G, Young MF, Mihalik D, Götte M, Malle E, Schaefer RM, Gröne HJ (2005) The matrix component biglycan is proinflammatory and signals through Toll-like receptors 4 and 2 in macrophages. J Clin Investig 115:2223–2233. https://doi.org/10.1172/JCI23755 Schönherr E, Broszat M, Brandan E, Bruckner P, Kresse H (1998) Decorin core protein fragment Leu155-Val260 interacts with TGF-beta but does not compete for decorin binding to type I collagen. Arch Biochem Biophys 355:241–248. https://doi.org/10.1006/abbi.1998.0720 Schönherr E, Sunderkötter C, Iozzo RV, Schaefer L (2005) Decorin, a novel player in the insulin-like growth factor system. J Biol Chem 280:15767–15772. https://doi.org/10.1074/jbc.M500451200 Scott PG, McEwan PA, Dodd CM, Bergmann EM, Bishop PN, Bella J (2004) Crystal structure of the dimeric protein core of decorin, the archetypal small leucine-rich repeat proteoglycan. Proc Natl Acad Sci USA 101:15633–15638 Scott PG, Dodd CM, Bergmann EM (2006) Crystal structure of the biglycan dimer core protein. J Biol Chem 281:13324–13332 Sjoblom T, Jones S, Wood LD, Parsons DW, Lin J, Barber TD, Mandelker D, Leary RJ, Ptak J, Silliman N, Szabo S, Buckhaults P, Farrell C, Meeh P, Markowitz SD, Willis J, Dawson D, Willson JK, Gazdar AF, Hartigan J, Wu L, Liu C, Parmigiani G, Park BH, Bachman KE, Papadopoulos N, Vogelstein B, Kinzler KW, Velculescu VE (2006) The consensus coding sequences of human breast and colorectal cancers. Science 314:268–274 Sui R, Li F, Zhao J, Jiang R (2008) Clinical and genetic characterization of a Chinese family with CSNB1. Adv Exp Med Biol 613:245–252 Svensson L, Heinegård D, Oldberg A (1995) Decorin-binding sites for collagen type I are mainly located in leucine-rich repeats 4–5. J Biol Chem 270:20712–20716. https://doi.org/10.1074/jbc.270.35.20712 Svensson L, Närlid I, Oldberg A (2000) Fibromodulin and lumican bind to the same region on collagen type I fibrils. FEBS Lett 470:178–182. https://doi.org/10.1016/s0014-5793(00)01314-4 Tashima T, Nagatoishi S, Caaveiro JMM, Nakakido M, Sagara H, Kusano-Arai O, Iwanari H, Mimuro H, Hamakubo T, Ohnuma SI, Tsumoto K (2018) Molecular basis for governing the morphology of type-I collagen fibrils by Osteomodulin. Commun Biol 1:33–33 Tillgren V, Onnerfjord P, Haglund L, Heinegård D (2009) The tyrosine sulfate-rich domains of the LRR proteins fibromodulin and osteoadherin bind motifs of basic clusters in a variety of heparin-binding proteins, including bioactive factors. J Biol Chem 284:28543–28553. https://doi.org/10.1074/jbc.M109.047076 Tsang SH, Sharma T (2018) Congenital stationary night blindness. Adv Exp Med Biol 1085:61–64. https://doi.org/10.1007/978-3-319-95046-4_13 van der Lee R, Buljan M, Lang B, Weatheritt RJ, Daughdrill GW, Dunker AK, Fuxreiter M, Gough J, Gsponer J, Jones DT, Kim PM, Kriwacki RW, Oldfield CJ, Pappu RV, Tompa P, Uversky VN, Wright PE, Babu MM (2014) Classification of intrinsically disordered regions and proteins. Chem Rev 114:6589–6631. https://doi.org/10.1021/cr400525m Wang P, Li S, Xiao X, Guo X, Zhang Q (2009) An evaluation of OPTC and EPYC as candidate genes for high myopia. Mol Vis 15:2045–2049 Wang Q, GaoY LS, Guo X, Zhang Q (2012) Mutation screening of TRPM1, GRM6, NYX and CACNA1F genes in patients with congenital stationary night blindness. Int J Mol Med 30:521–526 Weber DS, Warren JJ (2019) The interaction between methionine and two aromatic amino acids is an abundant and multifunctional motif in proteins. Arch Biochem Biophys 672:108053. https://doi.org/10.1016/j.abb.2019.07.018 Wu F, Vij N, Roberts L, Lopez-Briones S, Joyce S, Chakravarti S (2007) A novel role of the lumican core protein in bacterial lipopolysaccharide-induced innate immune response. J Biol Chem 282:26409–26417. https://doi.org/10.1074/jbc.M702402200 Xiao X, Jia X, Guo X, Li S, Yang Z, Zhang Q (2006) CSNB1 in Chinese families associated with novel mutations in NYX. J Hum Genet 51:634–640 Yamaguchi Y, Ruoslahti E (1988) Expression of human proteoglycan in Chinese hamster ovary cells inhibits cell proliferation. Nature 336:244–246. https://doi.org/10.1038/336244a0 Yamaguchi Y, Mann DM, Ruoslahti E (1990) Negative regulation of transforming growth factor-beta by the proteoglycan decorin. Nature 346:281–284. https://doi.org/10.1038/346281a0 Yip SP, Li CC, Yiu WC, Hung WH, Lam WW, Lai MC, Ng PW, Fung WY, Chu PH, Jiang B, Chan HH, Yap MK (2013) A novel missense mutation in the NYX gene associated with high myopia. Ophthalmic Physiol Opt 33:346–353 Zappia J, Joiret M, Sanchez C, Lambert C, Geris L, Muller M, Henrotin Y (2020) From translation to protein degradation as mechanisms for regulating biological functions: a review on the SLRP family in skeletal tissues. Biomolecules 10:80. https://doi.org/10.3390/biom10010080 Zarpellon A, Celikel R, Roberts JR, McClintock RA, Mendolicchio GL, Moore KL, Jing H, Varughese KI, Ruggeri ZM (2011) Binding of alpha-thrombin to surface-anchored platelet glycoprotein Ib(alpha) sulfotyrosines through a two-site mechanism involving exosite I. Proc Natl Acad Sci USA 108:8628–8633. https://doi.org/10.1073/pnas.1017042108 Zeitz C, Minotti R, Feil S, Matyas G, Cremers FP, Hoyng CB, Berger W (2005) Novel mutations in CACNA1F and NYX in Dutch families with X-linked congenital stationary night blindness. Mol Vis 11:179–183 Zeitz C, Robson AG, Audo I (2015) Congenital stationary night blindness: an analysis and update of genotype-phenotype correlations and pathogenic mechanisms. Prog Retin Eye Res 45:58–110 Zeitz C, Jacobson SG, Hamel CP, Bujakowska K, Neuille M, Orhan E, Zanlonghi X, Lancelot ME, Michiels C, Schwartz SB, Bocquet B, Antonio A, Audier C, Letexier M, Saraiva JP, Luu TD, Sennlaub F, Nguyen H, Poch O, Dollfus H, Lecompte O, Kohl S, Sahel JA, Bhattacharya SS, Audo I (2013) Whole-exome sequencing identifies LRIT3 mutations as a cause of autosomal-recessive complete congenital stationary night blindness. Am J Hum Genet 92:67–75 Zeng-Brouwers J, Pandey S, Trebicka J, Wygrecka M, Schaefer L (2020) Communications via the small leucine-rich proteoglycans: molecular specificity in inflammation and autoimmune diseases. J Histochem Cytochem 68:887–906. https://doi.org/10.1369/0022155420930303 Zhang Q, Xiao X, Li S, Jia X, Yang Z, Huang S, Caruso RC, Guan T, Sergeev Y, Guo X, Hejtmancik JF (2007) Mutations in NYX of individuals with high myopia, but without night blindness. Mol Vis 13:330–336 Zhong FL, Mamai O, Sborgi L, Boussofara L, Hopkins R, Robinson K, Szeverenyi I, Takeichi T, Balaji R, Lau A, Tye H, Roy K, Bonnard C, Ahl PJ, Jones LA, Baker PJ, Lacina L, Otsuka A, Fournie PR, Malecaze F, Lane EB, Akiyama M, Kabashima K, Connolly JE, Masters SL, Soler VJ, Omar SS, McGrath JA, Nedelcu R, Gribaa M, Denguezli M, Saad A, Hiller S, Reversade B (2016) Germline NLRP1 mutations cause skin inflammatory and cancer susceptibility syndromes via inflammasome activation. Cell 167:187–202. e17. https://doi.org/10.1016/j.cell.2016.09.001 Zhou L, Li T, Song X, Li Y, Li H, Dan H (2015) NYX mutations in four families with high myopia with or without CSNB1. Mol Vis 21:213–223 Zhou L, Hinerman JM, Blaszczyk M, Miller JL, Conrady DG, Barrow AD, Chirgadze DY, Bihan D, Farndale RW, Herr AB (2016) Structural basis for collagen recognition by the immune receptor OSCAR. Blood 127(5):529–537. https://doi.org/10.1182/blood-2015-08-667055