Lysyl hydroxylase 3–mediated post-translational modifications are required for proper biosynthesis of collagen α1α1α2(IV)

Bella, 2017, Fibrillar collagens, Subcell Biochem., 82, 457, 10.1007/978-3-319-49674-0_14 Ricard-Blum, 2005, The collagen superfamily: from the extracellular matrix to the cell membrane, Pathol. Biol., 53, 430, 10.1016/j.patbio.2004.12.024 Lamande, 2020, Genetic disorders of the extracellular matrix, Anat. Rec. (Hoboken), 303, 1527, 10.1002/ar.24086 Bateman, 2009, Genetic diseases of connective tissues: cellular and extracellular effects of ECM mutations, Nat. Rev. Genet., 10, 173, 10.1038/nrg2520 Marini, 2017, Osteogenesis imperfecta, Nat. Rev. Dis. Primers, 3, 10.1038/nrdp.2017.52 Malfait, 2020, The Ehlers-Danlos syndromes, Nat. Rev. Dis. Primers, 6, 64, 10.1038/s41572-020-0194-9 Besio, 2019, Bone biology: insights from osteogenesis imperfecta and related rare fragility syndromes, FEBS J., 286, 3033, 10.1111/febs.14963 Claeys, 2021, Collagen transport and related pathways in Osteogenesis Imperfecta, Hum. Genet., 140, 1121, 10.1007/s00439-021-02302-2 Omar, 2021, Four decades in the making: collagen III and mechanisms of vascular Ehlers danlos syndrome, Matrix Biol. Plus, 12, 10.1016/j.mbplus.2021.100090 Van Damme, 2022, The ehlers-danlos syndromes against the backdrop of inborn errors of metabolism, Genes (Basel), 13, 265, 10.3390/genes13020265 Hudson, 2003, Alport's syndrome, Goodpasture's syndrome, and type IV collagen, N. Engl. J. Med., 348, 2543, 10.1056/NEJMra022296 Boudko, 2022, Prospective collagen IValpha345 therapies for Alport syndrome, Curr. Opin. Nephrol. Hypertens., 31, 213, 10.1097/MNH.0000000000000789 Jeanne, 2017, Genotype-phenotype correlations in pathology caused by collagen type IV alpha 1 and 2 mutations, Matrix Biol., 57-58, 29, 10.1016/j.matbio.2016.10.003 Mao, 2015, Type IV collagens and basement membrane diseases: cell biology and pathogenic mechanisms, Curr. Top Membr., 76, 61, 10.1016/bs.ctm.2015.09.002 Kuo, 2012, COL4A1 and COL4A2 mutations and disease: Insights into pathogenic mechanisms and potential therapeutic targets, Hum. Mol. Genet., 21, R97, 10.1093/hmg/dds346 Boyce, 2021, Epilepsy and related challenges in children with COL4A1 and COL4A2 mutations: a Gould syndrome patient registry, Epilepsy Behav., 125, 10.1016/j.yebeh.2021.108365 Mao, 2017, Genetic dissection of anterior segment dysgenesis caused by a Col4a1 mutation in mouse, Dis. Model Mech., 10, 475 Mao, 2015, Strain-dependent anterior segment dysgenesis and progression to glaucoma in Col4a1 mutant mice, Invest. Ophthalmol. Vis. Sci., 56, 6823, 10.1167/iovs.15-17527 Ishikawa, 2013, A molecular ensemble in the rER for procollagen maturation, Biochim. Biophys. Acta, 1833, 2479, 10.1016/j.bbamcr.2013.04.008 Ito, 2021, Quality control of procollagen in cells, Annu. Rev. Biochem., 90, 631, 10.1146/annurev-biochem-013118-111603 Onursal, 2021, Collagen biosynthesis, processing, and maturation in lung ageing, Front. Med. (Lausanne), 8 Ihme, 1984, Ehlers-danlos syndrome type VI: collagen type specificity of defective lysyl hydroxylation in various tissues, J. Invest. Dermatol., 83, 161, 10.1111/1523-1747.ep12263502 Weis, 2010, Location of 3-hydroxyproline residues in collagen types I, II, III, and V/XI implies a role in fibril supramolecular assembly, J. Biol. Chem., 285, 2580, 10.1074/jbc.M109.068726 Ishikawa, 2021, Type I and type V procollagen triple helix uses different subsets of the molecular ensemble for lysine posttranslational modifications in the rER, J. Biol. Chem., 296, 10.1016/j.jbc.2021.100453 Ishikawa, 2014, A substrate preference for the rough endoplasmic reticulum resident protein FKBP22 during collagen biosynthesis, J. Biol. Chem., 289, 18189, 10.1074/jbc.M114.561944 Taga, 2016, Developmental stage-dependent regulation of prolyl 3-hydroxylation in tendon type I collagen, J. Biol. Chem., 291, 837, 10.1074/jbc.M115.686105 Salo, 2021, Prolyl and lysyl hydroxylases in collagen synthesis, Exp. Dermatol., 30, 38, 10.1111/exd.14197 Basak, 2016, Comprehensive characterization of glycosylation and hydroxylation of basement membrane collagen IV by high-resolution mass spectrometry, J. Proteome Res., 15, 245, 10.1021/acs.jproteome.5b00767 Berg, 1973, The thermal transition of a non-hydroxylated form of collagen. Evidence for a role for hydroxyproline in stabilizing the triple-helix of collagen, Biochem. Biophys. Res. Commun., 52, 115, 10.1016/0006-291X(73)90961-3 Mizuno, 2004, Hydroxylation-induced stabilization of the collagen triple helix. Acetyl-(glycyl-4(R)-hydroxyprolyl-4(R)-hydroxyprolyl)(10)-NH(2) forms a highly stable triple helix, J. Biol. Chem., 279, 38072, 10.1074/jbc.M402953200 Taga, 2021, In-depth correlation analysis demonstrates that 4-hydroxyproline at the Yaa position of Gly-Xaa-Yaa repeats dominantly stabilizes collagen triple helix, Matrix Biol. Plus, 10, 10.1016/j.mbplus.2021.100067 Montgomery, 2018, Post-translational modification of type IV collagen with 3-hydroxyproline affects its interactions with glycoprotein VI and nidogens 1 and 2, J. Biol. Chem., 293, 5987, 10.1074/jbc.RA117.000406 Grafe, 2014, Excessive transforming growth factor-beta signaling is a common mechanism in osteogenesis imperfecta, Nat. Med., 20, 670, 10.1038/nm.3544 Hennet, 2019, Collagen glycosylation, Curr. Opin. Struct. Biol., 56, 131, 10.1016/j.sbi.2019.01.015 De Giorgi, 2021, Collagen hydroxylysine glycosylation: non-conventional substrates for atypical glycosyltransferase enzymes, Biochem. Soc. Trans., 49, 855, 10.1042/BST20200767 Geister, 2019, Loss of function of Colgalt1 disrupts collagen post-translational modification and causes musculoskeletal defects, Dis. Model Mech., 12 Miyatake, 2018, Biallelic COLGALT1 variants are associated with cerebral small vessel disease, Ann. Neurol., 84, 843, 10.1002/ana.25367 Teunissen, 2021, Biallelic variants in the COLGALT1 gene causes severe congenital porencephaly: a case report, Neurol. Genet., 7, e564, 10.1212/NXG.0000000000000564 Salo, 2008, A connective tissue disorder caused by mutations of the lysyl hydroxylase 3 gene, Am. J. Hum. Genet., 83, 495, 10.1016/j.ajhg.2008.09.004 Ewans, 2019, Pathogenic variants in PLOD3 result in a Stickler syndrome-like connective tissue disorder with vascular complications, J. Med. Genet., 56, 629, 10.1136/jmedgenet-2019-106019 Vahidnezhad, 2019, Mutations in PLOD3, encoding lysyl hydroxylase 3, cause a complex connective tissue disorder including recessive dystrophic epidermolysis bullosa-like blistering phenotype with abnormal anchoring fibrils and type VII collagen deficiency, Matrix Biol., 81, 91, 10.1016/j.matbio.2018.11.006 Maddirevula, 2019, Autozygome and high throughput confirmation of disease genes candidacy, Genet. Med., 21, 736, 10.1038/s41436-018-0138-x Zhou, 2022, Cerebral small vessel disease caused by PLOD3 mutation: expanding the phenotypic spectrum of lysyl hydroxylase-3 deficiency, Pediatric Investig., 6, 219, 10.1002/ped4.12328 Ruotsalainen, 2006, Glycosylation catalyzed by lysyl hydroxylase 3 is essential for basement membranes, J. Cell Sci., 119, 625, 10.1242/jcs.02780 Rautavuoma, 2004, Premature aggregation of type IV collagen and early lethality in lysyl hydroxylase 3 null mice, Proc. Natl. Acad. Sci. U. S. A., 101, 14120, 10.1073/pnas.0404966101 Sipila, 2007, Secretion and assembly of type IV and VI collagens depend on glycosylation of hydroxylysines, J. Biol. Chem., 282, 33381, 10.1074/jbc.M704198200 Heikkinen, 2000, Lysyl hydroxylase 3 is a multifunctional protein possessing collagen glucosyltransferase activity, J. Biol. Chem., 275, 36158, 10.1074/jbc.M006203200 Rautavuoma, 2002, Characterization of three fragments that constitute the monomers of the human lysyl hydroxylase isoenzymes 1-3. The 30-kDa N-terminal fragment is not required for lysyl hydroxylase activity, J. Biol. Chem., 277, 23084, 10.1074/jbc.M112077200 Wang, 2002, The third activity for lysyl hydroxylase 3: Galactosylation of hydroxylysyl residues in collagens in vitro, Matrix Biol., 21, 559, 10.1016/S0945-053X(02)00071-9 Scietti, 2018, Molecular architecture of the multifunctional collagen lysyl hydroxylase and glycosyltransferase LH3, Nat. Commun., 9, 3163, 10.1038/s41467-018-05631-5 Guo, 2021, A collagen glucosyltransferase drives lung adenocarcinoma progression in mice, Commun. Biol., 4, 482, 10.1038/s42003-021-01982-w Duncan, 1983, Procollagen IV. Association to tetramers, J. Biol. Chem., 258, 5869, 10.1016/S0021-9258(20)81976-0 Mirigian, 2014, Pulse-chase analysis of procollagen biosynthesis by azidohomoalanine labeling, Connect Tissue Res., 55, 403, 10.3109/03008207.2014.959120 Syx, 2021, Aberrant binding of mutant HSP47 affects posttranslational modification of type I collagen and leads to osteogenesis imperfecta, PLoS Genet., 17, 10.1371/journal.pgen.1009339 Fessler, 1982, Identification of the carboxyl peptides of mouse procollagen IV and its implications for the assembly and structure of basement membrane procollagen, J. Biol. Chem., 257, 9804, 10.1016/S0021-9258(18)34143-7 Lunstrum, 1988, Drosophila basement membrane procollagen IV. I. Protein characterization and distribution, J. Biol. Chem., 263, 18318, 10.1016/S0021-9258(19)81362-5 Toth, 1999, Biosynthesis of alpha2(IV) and alpha1(IV) chains of collagen IV and interactions with matrix metalloproteinase-9, J. Cell Physiol., 180, 131, 10.1002/(SICI)1097-4652(199907)180:1<131::AID-JCP15>3.0.CO;2-S Matsuoka, 2004, Insufficient folding of type IV collagen and formation of abnormal basement membrane-like structure in embryoid bodies derived from Hsp47-null embryonic stem cells, Mol. Biol. Cell, 15, 4467, 10.1091/mbc.e04-01-0050 Ishida, 2006, Type I collagen in Hsp47-null cells is aggregated in endoplasmic reticulum and deficient in N-propeptide processing and fibrillogenesis, Mol. Biol. Cell, 17, 2346, 10.1091/mbc.e05-11-1065 Vranka, 2010, Prolyl 3-hydroxylase 1 null mice display abnormalities in fibrillar collagen-rich tissues such as tendons, skin, and bones, J. Biol. Chem., 285, 17253, 10.1074/jbc.M110.102228 Pedchenko, 2019, A chloride ring is an ancient evolutionary innovation mediating the assembly of the collagen IV scaffold of basement membranes, J. Biol. Chem., 294, 7968, 10.1074/jbc.RA119.007426 Ivanov, 2021, Collagen IV exploits a Cl- step gradient for scaffold assembly, Adv. Exp. Med. Biol., 21, 129, 10.1007/5584_2020_582 Bhatnagar, 1996, Circular dichroism of collagen and related polypeptides, 183 Ono, 2012, Direct in vitro and in vivo evidence for interaction between Hsp47 protein and collagen triple helix, J. Biol. Chem., 287, 6810, 10.1074/jbc.M111.280248 Ishikawa, 2016, Intracellular mechanisms of molecular recognition and sorting for transport of large extracellular matrix molecules, Proc. Natl. Acad. Sci. U. S. A., 113, E6036, 10.1073/pnas.1609571113 Sricholpech, 2012, Lysyl hydroxylase 3-mediated glucosylation in type I collagen: molecular loci and biological significance, J. Biol. Chem., 287, 22998, 10.1074/jbc.M112.343954 Gould, 2005, Mutations in Col4a1 cause perinatal cerebral hemorrhage and porencephaly, Science, 308, 1167, 10.1126/science.1109418 Gould, 2006, Role of COL4A1 in small-vessel disease and hemorrhagic stroke, N. Engl. J. Med., 354, 1489, 10.1056/NEJMoa053727 Breedveld, 2006, Novel mutations in three families confirm a major role of COL4A1 in hereditary porencephaly, J. Med. Genet., 43, 490, 10.1136/jmg.2005.035584 Vahedi, 2007, Clinical and brain MRI follow-up study of a family with COL4A1 mutation, Neurology, 69, 1564, 10.1212/01.wnl.0000295994.46586.e7 Coste, 2022, COL4A1/COL4A2 and inherited platelet disorder gene variants in fetuses showing intracranial hemorrhage, Prenat Diagn., 42, 601, 10.1002/pd.6113 Aro, 2015, Severe extracellular matrix abnormalities and chondrodysplasia in mice lacking collagen prolyl 4-hydroxylase isoenzyme II in combination with a reduced amount of isoenzyme I, J. Biol. Chem., 290, 16964, 10.1074/jbc.M115.662635 Zou, 2017, P4HA1 mutations cause a unique congenital disorder of connective tissue involving tendon, bone, muscle and the eye, Hum. Mol. Genet., 26, 2207, 10.1093/hmg/ddx110 Al-Shaer, 2021, Sequence-dependent mechanics of collagen reflect its structural and functional organization, Biophys. J., 120, 4013, 10.1016/j.bpj.2021.08.013 Taga, 2012, Development of a novel method for analyzing collagen O-glycosylations by hydrazide chemistry, Mol. Cell Proteomics, 11, 10.1074/mcp.M111.010397 Morris, 1986, The tissue form of type VII collagen is an antiparallel dimer, J. Biol. Chem., 261, 5638, 10.1016/S0021-9258(19)57262-3 Macdonald, 2001, HSP47 binds cooperatively to triple helical type I collagen but has little effect on the thermal stability or rate of refolding, J. Biol. Chem., 276, 25399, 10.1074/jbc.M102471200 Fujii, 2019, Lowering the culture temperature corrects collagen abnormalities caused by HSP47 gene knockout, Sci. Rep., 9, 10.1038/s41598-019-53962-0 Taga, 2014, Stable isotope-labeled collagen: A novel and versatile tool for quantitative collagen analyses using mass spectrometry, J. Proteome Res., 13, 3671, 10.1021/pr500213a Backenroth, 2014, CANOES: detecting rare copy number variants from whole exome sequencing data, Nucleic Acids Res., 42, e97, 10.1093/nar/gku345