Abstract
Fibrillar collagens (types I, II, III, V, XI, XXIV and XXVII) constitute a sub-group within the collagen family (of which there are 28 types in humans) whose functions are to provide three-dimensional frameworks for tissues and organs. These networks confer mechanical strength as well as signalling and organizing functions through binding to cellular receptors and other components of the extracellular matrix (ECM). Here we describe the structure and assembly of fibrillar collagens, and their procollagen precursors, from the molecular to the tissue level. We show how the structure of the collagen triple-helix is influenced by the amino acid sequence, hydrogen bonding and post-translational modifications, such as prolyl 4-hydroxylation. The numerous steps in the biosynthesis of the fibrillar collagens are reviewed with particular attention to the role of prolyl 3-hydroxylation, collagen chaperones, trimerization of procollagen chains and proteolytic maturation. The multiple steps controlling fibril assembly are then discussed with a focus on the cellular control of this process in vivo. Our current understanding of the molecular packing in collagen fibrils, from different tissues, is then summarized on the basis of data from X-ray diffraction and electron microscopy. These results provide structural insights into how collagen fibrils interact with cell receptors, other fibrillar and non-fibrillar collagens and other ECM components, as well as enzymes involved in cross-linking and degradation.
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Acevedo-Jake AM, Clements KA, Hartgerink JD (2016) Synthetic, register-specific, AAB heterotrimers to investigate single point glycine mutations in Osteogenesis imperfecta. Biomacromolecules 17(3):914–921. doi:10.1021/acs.biomac.5b01562
Anantharajan J, Koski MK, Kursula P, Hieta R, Bergmann U, Myllyharju J, Wierenga RK (2013) The structural motifs for substrate binding and dimerization of the alpha subunit of collagen prolyl 4-hydroxylase. Structure 21(12):2107–2118. doi:10.1016/j.str.2013.09.005
Bann JG, Peyton DH, Bachinger HP (2000) Sweet is stable: glycosylation stabilizes collagen. FEBS Lett 473(2):237–240
Bann JG, Bachinger HP, Peyton DH (2003) Role of carbohydrate in stabilizing the triple-helix in a model for a deep-sea hydrothermal vent worm collagen. Biochemistry 42(14):4042–4048. doi:10.1021/bi027050w
Bekhouche M, Colige A (2015) The procollagen N-proteinases ADAMTS2, 3 and 14 in pathophysiology. Matrix Biol 44-46:46–53. doi:10.1016/j.matbio.2015.04.001
Bekhouche M, Leduc C, Dupont L, Janssen L, Delolme F, Vadon-Le Goff S, Smargiasso N, Baiwir D, Mazzucchelli G, Zanella-Cleon I, Dubail J, De Pauw E, Nusgens B, Hulmes DJS, Moali C, Colige A (2016) Determination of the substrate repertoire of ADAMTS2, 3, and 14 significantly broadens their functions and identifies extracellular matrix organization and TGF-beta signaling as primary targets. FASEB J 30(5):1741–1756. doi:10.1096/fj.15-279869
Bella J (2010) A new method for describing the helical conformation of collagen: dependence of the triple helical twist on amino acid sequence. J Struct Biol 170(2):377–391. doi:10.1016/j.jsb.2010.02.003
Bella J (2014) A first census of collagen interruptions: collagen’s own stutters and stammers. J Struct Biol 186(3):438–450. doi:10.1016/j.jsb.2014.03.022
Bella J (2016) Collagen structure: new tricks from a very old dog. Biochem J 473(8):1001–1025. doi:10.1042/BJ20151169
Bella J, Hindle KL, McEwan PA, Lovell SC (2008) The leucine-rich repeat structure. Cell Mol Life Sci 65(15):2307–2333. doi:10.1007/s00018-008-8019-0
Bender E, Silver FH, Hayashi K, Trelstad RL (1982) Type I collagen segment long spacing banding patterns. Evidence that the alpha 2 chain is in the reference or A position. J Biol Chem 257(16):9653–9657
Birk DE (2001) Type V collagen: heterotypic type I/V collagen interactions in the regulation of fibril assembly. Micron 32(3):223–237
Blaschke UK, Eikenberry EF, Hulmes DJS, Galla HJ, Bruckner P (2000) Collagen XI nucleates self-assembly and limits lateral growth of cartilage fibrils. J Biol Chem 275(14):10370–10378
Boot-Handford RP, Tuckwell DS (2003) Fibrillar collagen: the key to vertebrate evolution? A tale of molecular incest. Bioessays 25(2):142–151. doi:10.1002/bies.10230
Boot-Handford RP, Tuckwell DS, Plumb DA, Rock CF, Poulsom R (2003) A novel and highly conserved collagen (pro(alpha)1(XXVII)) with a unique expression pattern and unusual molecular characteristics establishes a new clade within the vertebrate fibrillar collagen family. J Biol Chem 278(33):31067–31077. doi:10.1074/jbc.M212889200
Boudko SP, Engel J, Bachinger HP (2012) The crucial role of trimerization domains in collagen folding. Int J Biochem Cell Biol 44(1):21–32. doi:10.1016/j.biocel.2011.09.009
Bourhis JM, Mariano N, Zhao Y, Harlos K, Exposito JY, Jones EY, Moali C, Aghajari N, Hulmes DJS (2012) Structural basis of fibrillar collagen trimerization and related genetic disorders. Nat Struct Mol Biol 19(10):1031–1036. doi:10.1038/nsmb.2389
Bourhis JM, Vadon-Le Goff S, Afrache H, Mariano N, Kronenberg D, Thielens N, Moali C, Hulmes DJS (2013) Procollagen C-proteinase enhancer grasps the stalk of the C-propeptide trimer to boost collagen precursor maturation. Proc Natl Acad Sci U S A 110(16):6394–6399. doi:10.1073/pnas.1300480110
Broder C, Arnold P, Vadon-Le Goff S, Konerding MA, Bahr K, Muller S, Overall CM, Bond JS, Koudelka T, Tholey A, Hulmes DJS, Moali C, Becker-Pauly C (2013) Metalloproteases meprin alpha and meprin beta are C- and N-procollagen proteinases important for collagen assembly and tensile strength. Proc Natl Acad Sci U S A 110(35):14219–14224. doi:10.1073/pnas.1305464110
Brondijk TH, Bihan D, Farndale RW, Huizinga EG (2012) Implications for collagen I chain registry from the structure of the collagen von Willebrand factor A3 domain complex. Proc Natl Acad Sci U S A 109(14):5253–5258. doi:10.1073/pnas.1112388109
Bruckner P (2010) Suprastructures of extracellular matrices: paradigms of functions controlled by aggregates rather than molecules. Cell Tissue Res 339(1):7–18. doi:10.1007/s00441-009-0864-0
Cabral WA, Perdivara I, Weis M, Terajima M, Blissett AR, Chang W, Perosky JE, Makareeva EN, Mertz EL, Leikin S, Tomer KB, Kozloff KM, Eyre DR, Yamauchi M, Marini JC (2014) Abnormal type I collagen post-translational modification and crosslinking in a cyclophilin B KO mouse model of recessive osteogenesis imperfecta. PLoS Genet 10(6):e1004465. doi:10.1371/journal.pgen.1004465
Chen S, Birk DE (2013) The regulatory roles of small leucine-rich proteoglycans in extracellular matrix assembly. FEBS J 280(10):2120–2137. doi:10.1111/febs.12136
Chen S, Mienaltowski MJ, Birk DE (2015) Regulation of corneal stroma extracellular matrix assembly. Exp Eye Res 133:69–80. doi:10.1016/j.exer.2014.08.001
Chiquet M, Birk DE, Bonnemann CG, Koch M (2014) Collagen XII: protecting bone and muscle integrity by organizing collagen fibrils. Int J Biochem Cell Biol 53:51–54. doi:10.1016/j.biocel.2014.04.020
D’Arcangelo JG, Stahmer KR, Miller EA (2013) Vesicle-mediated export from the ER: COPII coat function and regulation. Biochim Biophys Acta 1833(11):2464–2472. doi:10.1016/j.bbamcr.2013.02.003
Daubenspeck JM, Zeng H, Chen P, Dong S, Steichen CT, Krishna NR, Pritchard DG, Turnbough CL Jr (2004) Novel oligosaccharide side chains of the collagen-like region of BclA, the major glycoprotein of the Bacillus anthracis exosporium. J Biol Chem 279(30):30945–30953. doi:10.1074/jbc.M401613200
Dittmore A, Silver J, Sarkar SK, Marmer B, Goldberg GI, Neuman KC (2016) Internal strain drives spontaneous periodic buckling in collagen and regulates remodeling. Proc Natl Acad Sci U S A 113(30):8436–8441. doi:10.1073/pnas.1523228113
Dubey K, Kar K (2014) Type I collagen prevents amyloid aggregation of hen egg white lysozyme. Biochem Biophys Res Commun 448(4):480–484. doi:10.1016/j.bbrc.2014.04.135
Duran I, Csukasi F, Taylor SP, Krakow D, Becerra J, Bombarely A, Mari-Beffa M (2015a) Collagen duplicate genes of bone and cartilage participate during regeneration of zebrafish fin skeleton. Gene Expr Patterns 19(1–2):60–69. doi:10.1016/j.gep.2015.07.004
Duran I, Nevarez L, Sarukhanov A, Wu S, Lee K, Krejci P, Weis M, Eyre D, Krakow D, Cohn DH (2015b) HSP47 and FKBP65 cooperate in the synthesis of type I procollagen. Hum Mol Genet 24(7):1918–1928. doi:10.1093/hmg/ddu608
Emsley J, Knight CG, Farndale RW, Barnes MJ, Liddington RC (2000) Structural basis of collagen recognition by integrin α2β1. Cell 101(1):47–56. doi:10.1016/S0092-8674(00)80622-4
Exposito JY, Larroux C, Cluzel C, Valcourt U, Lethias C, Degnan BM (2008) Demosponge and sea anemone fibrillar collagen diversity reveals the early emergence of A/C clades and the maintenance of the modular structure of type V/XI collagens from sponge to human. J Biol Chem 283(42):28226–28235. doi:10.1074/jbc.M804573200
Exposito JY, Valcourt U, Cluzel C, Lethias C (2010) The fibrillar collagen family. Int J Mol Sci 11(2):407–426. doi:10.3390/ijms11020407
Eyre DR, Weis MA, Wu JJ (2006) Articular cartilage collagen: an irreplaceable framework? Eur Cell Mater 12:57–63. doi:10.22203/eCM
Fallas JA, Dong J, Tao YJ, Hartgerink JD (2012) Structural insights into charge pair interactions in triple helical collagen-like proteins. J Biol Chem 287(11):8039–8047. doi:10.1074/jbc.M111.296574
Fang M, Jacob R, McDougal O, Oxford JT (2012) Minor fibrillar collagens, variable regions alternative splicing, intrinsic disorder, and tyrosine sulfation. Protein Cell 3(6):419–433. doi:10.1007/s13238-012-2917-5
Farndale RW, Lisman T, Bihan D, Hamaia S, Smerling CS, Pugh N, Konitsiotis A, Leitinger B, de Groot PG, Jarvis GE, Raynal N (2008) Cell-collagen interactions: the use of peptide Toolkits to investigate collagen-receptor interactions. Biochem Soc Trans 36(Pt 2):241–250. doi:10.1042/BST0360241
Fichard A, Kleman JP, Ruggiero F (1995) Another look at collagen V and XI molecules. Matrix Biol 14(7):515–531. doi:10.1016/S0945-053X(05)80001-0
Ghosh N, McKillop TJ, Jowitt TA, Howard M, Davies H, Holmes DF, Roberts IS, Bella J (2012) Collagen-like proteins in pathogenic E. coli strains. PLoS One 7(6):e37872. doi:10.1371/journal.pone.0037872
Gjaltema RA, van der Stoel MM, Boersema M, Bank RA (2016) Disentangling mechanisms involved in collagen pyridinoline cross-linking: the immunophilin FKBP65 is critical for dimerization of lysyl hydroxylase 2. Proc Natl Acad Sci U S A 113(26):7142–7147. doi:10.1073/pnas.1600074113
Gordon MK, Hahn RA (2010) Collagens. Cell Tissue Res 339(1):247–257. doi:10.1007/s00441-009-0844-4
Gorres KL, Raines RT (2010) Prolyl 4-hydroxylase. Crit Rev Biochem Mol Biol 45(2):106–124. doi:10.3109/10409231003627991
Hamaia S, Farndale RW (2014) Integrin recognition motifs in the human collagens. Adv Exp Med Biol 819:127–142. doi:10.1007/978-94-017-9153-3_9
Hamaia SW, Pugh N, Raynal N, Nemoz B, Stone R, Gullberg D, Bihan D, Farndale RW (2012) Mapping of potent and specific binding motifs, GLOGEN and GVOGEA, for integrin α1β1 using collagen toolkits II and III. J Biol Chem 287(31):26019–26028. doi:10.1074/jbc.M112.353144
Heino J (2007) The collagen family members as cell adhesion proteins. Bioessays 29(10):1001–1010. doi:10.1002/bies.20636
Heino J (2014) Cellular signaling by collagen-binding integrins. Adv Exp Med Biol 819:143–155. doi:10.1007/978-94-017-9153-3_10
Herchenhan A, Uhlenbrock F, Eliasson P, Weis M, Eyre D, Kadler KE, Magnusson SP, Kjaer M (2015) Lysyl oxidase activity is required for ordered collagen fibrillogenesis by tendon cells. J Biol Chem 290(26):16440–16450. doi:10.1074/jbc.M115.641670
Hoffman GG, Branam AM, Huang G, Pelegri F, Cole WG, Wenstrup RM, Greenspan DS (2010) Characterization of the six zebrafish clade B fibrillar procollagen genes, with evidence for evolutionarily conserved alternative splicing within the pro-alpha1(V) C-propeptide. Matrix Biol 29(4):261–275. doi:10.1016/j.matbio.2010.01.006
Hofmann H, Fietzek PP, Kuhn K (1978) The role of polar and hydrophobic interactions for the molecular packing of type I collagen: a three-dimensional evaluation of the amino acid sequence. J Mol Biol 125(2):137–165. doi:10.1016/0022-2836(78)90342-X
Hohenester E (2014) Signalling complexes at the cell-matrix interface. Curr Opin Struct Biol 29:10–16. doi:10.1016/j.sbi.2014.08.009
Hohenester E, Sasaki T, Giudici C, Farndale RW, Bachinger HP (2008) Structural basis of sequence-specific collagen recognition by SPARC. Proc Natl Acad Sci U S A 105(47):18273–18277. doi:10.1073/pnas.0808452105
Holmes DF, Kadler KE (2006) The 10+4 microfibril structure of thin cartilage fibrils. Proc Natl Acad Sci U S A 103(46):17249–17254. doi:10.1073/pnas.0608417103
Holmes DF, Gilpin CJ, Baldock C, Ziese U, Koster AJ, Kadler KE (2001) Corneal collagen fibril structure in three dimensions: structural insights into fibril assembly, mechanical properties, and tissue organization. Proc Natl Acad Sci U S A 98(13):7307–7312. doi:10.1073/pnas.111150598
Hudson DM, Eyre DR (2013) Collagen prolyl 3-hydroxylation: a major role for a minor post-translational modification? Connect Tissue Res 54(4–5):245–251. doi:10.3109/03008207.2013.800867
Hudson DM, Werther R, Weis M, Wu JJ, Eyre DR (2014) Evolutionary origins of C-terminal (GPP)n 3-hydroxyproline formation in vertebrate tendon collagen. PLoS One 9(4):e93467. doi:10.1371/journal.pone.0093467
Hulmes DJS (2008a) Collagen diversity, synthesis and assembly. In: Fratzl P (ed) Collagen – structure and mechanics. Springer, New York, pp 15–47
Hulmes DJS (2008b) Vertebrate collagens – structures, functions and biomedical applications. In: Scheibel T (ed) Fibrous proteins. Landes Biosciences, Austin, pp 12–29
Hulmes DJS, Miller A (1979) Quasi-hexagonal molecular packing in collagen fibrils. Nature 282(5741):878–880
Hulmes DJS, Holmes DF, Cummings C (1985) Crystalline regions in collagen fibrils. J Mol Biol 184(3):473–477
Hulmes DJS, Wess TJ, Prockop DJ, Fratzl P (1995) Radial packing, order, and disorder in collagen fibrils. Biophys J 68(5):1661–1670. doi:10.1016/S0006-3495(95)80391-7
Huxley-Jones J, Robertson DL, Boot-Handford RP (2007) On the origins of the extracellular matrix in vertebrates. Matrix Biol 26(1):2–11. doi:10.1016/j.matbio.2006.09.008
Ishikawa Y, Bachinger HP (2013) A molecular ensemble in the rER for procollagen maturation. Biochim Biophys Acta 1833(11):2479–2491. doi:10.1016/j.bbamcr.2013.04.008
Ishikawa Y, Boudko S, Bachinger HP (2015) Ziploc-ing the structure: triple helix formation is coordinated by rough endoplasmic reticulum resident PPIases. Biochim Biophys Acta 1850(10):1983–1993. doi:10.1016/j.bbagen.2014.12.024
Kadler KE, Holmes DF, Trotter JA, Chapman JA (1996) Collagen fibril formation. Biochem J 316(Pt 1):1–11
Kadler KE, Baldock C, Bella J, Boot-Handford RP (2007) Collagens at a glance. J Cell Sci 120(Pt 12):1955–1958. doi:10.1242/jcs.03453
Kadler KE, Hill A, Canty-Laird EG (2008) Collagen fibrillogenesis: fibronectin, integrins, and minor collagens as organizers and nucleators. Curr Opin Cell Biol 20(5):495–501. doi:10.1016/j.ceb.2008.06.008
Kalamajski S, Oldberg A (2010) The role of small leucine-rich proteoglycans in collagen fibrillogenesis. Matrix Biol 29(4):248–253. doi:10.1016/j.matbio.2010.01.001
Kalamajski S, Liu C, Tillgren V, Rubin K, Oldberg A, Rai J, Weis M, Eyre DR (2014) Increased C-telopeptide cross-linking of tendon type I collagen in fibromodulin-deficient mice. J Biol Chem 289(27):18873–18879. doi:10.1074/jbc.M114.572941
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(15):7951–7960. doi:10.1074/jbc.M115.693408
Kalson NS, Starborg T, Lu Y, Mironov A, Humphries SM, Holmes DF, Kadler KE (2013) Nonmuscle myosin II powered transport of newly formed collagen fibrils at the plasma membrane. Proc Natl Acad Sci U S A 110(49):E4743–E4752. doi:10.1073/pnas.1314348110
Kalson NS, Lu Y, Taylor SH, Starborg T, Holmes DF, Kadler KE (2015) A structure-based extracellular matrix expansion mechanism of fibrous tissue growth. eLife 4:e05958. doi:10.7554/eLife.05958
Keen AN, Fenna AJ, McConnell JC, Sherratt MJ, Gardner P, Shiels HA (2016) The dynamic nature of hypertrophic and fibrotic remodeling of the fish ventricle. Front Physiol 6:427. doi:10.3389/fphys.2015.00427
Knupp C, Pinali C, Lewis PN, Parfitt GJ, Young RD, Meek KM, Quantock AJ (2009) The architecture of the cornea and structural basis of its transparency. Adv Protein Chem Struct Biol 78:25–49. doi:10.1016/S1876-1623(08)78002-7
Koch M, Laub F, Zhou P, Hahn RA, Tanaka S, Burgeson RE, Gerecke DR, Ramirez F, Gordon MK (2003) Collagen XXIV, a vertebrate fibrillar collagen with structural features of invertebrate collagens: selective expression in developing cornea and bone. J Biol Chem 278(44):43236–43244. doi:10.1074/jbc.M302112200
Konitsiotis AD, Raynal N, Bihan D, Hohenester E, Farndale RW, Leitinger B (2008) Characterization of high affinity binding motifs for the discoidin domain receptor DDR2 in collagen. J Biol Chem 283(11):6861–6868. doi:10.1074/jbc.M709290200
Kramer RZ, Bella J, Brodsky B, Berman HM (2001) The crystal and molecular structure of a collagen-like peptide with a biologically relevant sequence. J Mol Biol 311(1):131–147. doi:10.1006/jmbi.2001.4849
Lees JF, Tasab M, Bulleid NJ (1997) Identification of the molecular recognition sequence which determines the type-specific assembly of procollagen. EMBO J 16(5):908–916. doi:10.1093/emboj/16.5.908
Leikina E, Mertts MV, Kuznetsova N, Leikin S (2002) Type I collagen is thermally unstable at body temperature. Proc Natl Acad Sci U S A 99(3):1314–1318. doi:10.1073/pnas.032307099
Leitinger B (2011) Transmembrane collagen receptors. Annu Rev Cell Dev Biol 27:265–290. doi:10.1146/annurev-cellbio-092910-154013
Leitinger B, Hohenester E (2007) Mammalian collagen receptors. Matrix Biol 26(3):146–155. doi:10.1016/j.matbio.2006.10.007
Mak KM, Png CY, Lee DJ (2016) Type V collagen in health, disease, and fibrosis. Anat Rec (Hoboken) 299(5):613–629. doi:10.1002/ar.23330
Manka SW, Carafoli F, Visse R, Bihan D, Raynal N, Farndale RW, Murphy G, Enghild JJ, Hohenester E, Nagase H (2012) Structural insights into triple-helical collagen cleavage by matrix metalloproteinase 1. Proc Natl Acad Sci U S A 109(31):12461–12466. doi:10.1073/pnas.1204991109
McAlinden A (2014) Alternative splicing of type II procollagen: IIB or not IIB? Connect Tissue Res 55(3):165–176. doi:10.3109/03008207.2014.908860
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(2):294–305. doi:10.1016/j.jsb.2006.01.016
Mienaltowski MJ, Birk DE (2014) Structure, physiology, and biochemistry of collagens. Adv Exp Med Biol 802:5–29. doi:10.1007/978-94-007-7893-1_2
Myllyharju J (2005) Intracellular post-translational modifications of collagens. Top Curr Chem 247:115–247. doi:10.1007/b103821
Myllyharju J (2008) Prolyl 4-hydroxylases, key enzymes in the synthesis of collagens and regulation of the response to hypoxia, and their roles as treatment targets. Ann Med 40(6):402–417. doi:10.1080/07853890801986594
Myllyharju J, Kivirikko KI (2004) Collagens, modifying enzymes and their mutations in humans, flies and worms. Trends Genet 20(1):33–43. doi:10.1016/j.tig.2003.11.004
Nishi Y, Uchiyama S, Doi M, Nishiuchi Y, Nakazawa T, Ohkubo T, Kobayashi Y (2005) Different effects of 4-hydroxyproline and 4-fluoroproline on the stability of collagen triple helix. Biochemistry 44(16):6034–6042. doi:10.1021/bi047887m
Okuyama K, Bachinger HP, Mizuno K, Boudko S, Engel J, Berisio R, Vitagliano L (2009) Re: microfibrillar structure of type I collagen in situ. Acta Crystallogr D Biol Crystallogr 65(Pt 9):1007–1008. doi:10.1107/S0907444909023051author reply 1009-1010
Olsen BR (1997) Collagen IX. Int J Biochem Cell Biol 29(4):555–558
Orgel JPRO (2009) On the packing structure of collagen: response to Okuyama et al.’s comment on Microfibrillar Structure of Type I Collagens in situ. Acta Cryst D65:1009–1010
Orgel JPRO, Wess TJ, Miller A (2000) The in situ conformation and axial location of the intermolecular cross-linked non-helical telopeptides of type I collagen. Structure 8(2):137–142
Orgel JPRO, Miller A, Irving TC, Fischetti RF, Hammersley AP, Wess TJ (2001) The in situ supermolecular structure of type I collagen. Structure 9(11):1061–1069
Orgel JPRO, Irving TC, Miller A, Wess TJ (2006) Microfibrillar structure of type I collagen in situ. Proc Natl Acad Sci U S A 103(24):9001–9005. doi:10.1073/pnas.0502718103
Orgel JPRO, Eid A, Antipova O, Bella J, Scott JE (2009) Decorin core protein (decoron) shape complements collagen fibril surface structure and mediates its binding. PLoS One 4(9):e7028. doi:10.1371/journal.pone.0007028
Orgel JPRO, Antipova O, Sagi I, Bitler A, Qiu D, Wang R, Xu Y, San Antonio JD (2011a) Collagen fibril surface displays a constellation of sites capable of promoting fibril assembly, stability, and hemostasis. Connect Tissue Res 52(1):18–24. doi:10.3109/03008207.2010.511354
Orgel JPRO, San Antonio JD, Antipova O (2011b) Molecular and structural mapping of collagen fibril interactions. Connect Tissue Res 52(1):2–17. doi:10.3109/03008207.2010.511353
Orgel JPRO, Persikov AV, Antipova O (2014) Variation in the helical structure of native collagen. PLoS One 9(2):e89519. doi:10.1371/journal.pone.0089519
Page AP, Johnstone IL (2007) The cuticle. WormBook:1–15. doi:10.1895/wormbook.1.138.1
Parmar AS, Nunes AM, Baum J, Brodsky B (2012) A peptide study of the relationship between the collagen triple-helix and amyloid. Biopolymers 97(10):795–806. doi:10.1002/bip.22070
Persikov AV, Brodsky B (2002) Unstable molecules form stable tissues. Proc Natl Acad Sci U S A 99(3):1101–1103. doi:10.1073/pnas.042707899
Persikov AV, Ramshaw JA, Brodsky B (2005) Prediction of collagen stability from amino acid sequence. J Biol Chem 280(19):19343–19349. doi:10.1074/jbc.M501657200
Perumal S, Antipova O, Orgel JPRO (2008) Collagen fibril architecture, domain organization, and triple-helical conformation govern its proteolysis. Proc Natl Acad Sci U S A 105(8):2824–2829. doi:10.1073/pnas.0710588105
Piez KA, Trus BL (1981) A new model for packing of type-I collagen molecules in the native fibril. Biosci Rep 1(10):801–810
Plumb DA, Dhir V, Mironov A, Ferrara L, Poulsom R, Kadler KE, Thornton DJ, Briggs MD, Boot-Handford RP (2007) Collagen XXVII is developmentally regulated and forms thin fibrillar structures distinct from those of classical vertebrate fibrillar collagens. J Biol Chem 282(17):12791–12795. doi:10.1074/jbc.C700021200
Raspanti M, Reguzzoni M, Protasoni M, Martini D (2011) Evidence of a discrete axial structure in unimodal collagen fibrils. Biomacromolecules 12 (12):4344–4347. doi:10.1021/bm201314e
Ricard-Blum S (2011) The collagen family. Cold Spring Harb Perspect Biol 3(1):a004978. doi:10.1101/cshperspect.a004978
Rosset EM, Bradshaw AD (2016) SPARC/osteonectin in mineralized tissue. Matrix Biol 52-54:78–87. doi:10.1016/j.matbio.2016.02.001
Saffarian S, Collier IE, Marmer BL, Elson EL, Goldberg G (2004) Interstitial collagenase is a Brownian ratchet driven by proteolysis of collagen. Science 306(5693):108–111. doi:10.1126/science.1099179
Sarkar SK, Marmer B, Goldberg G, Neuman KC (2012) Single-molecule tracking of collagenase on native type I collagen fibrils reveals degradation mechanism. Curr Biol 22(12):1047–1056. doi:10.1016/j.cub.2012.04.012
Schumacher MA, Mizuno K, Bachinger HP (2006) The crystal structure of a collagen-like polypeptide with 3(S)-hydroxyproline residues in the Xaa position forms a standard 7/2 collagen triple helix. J Biol Chem 281(37):27566–27574. doi:10.1074/jbc.M602797200
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 U S A 101(44):15633–15638. doi:10.1073/pnas.0402976101
Sharma U, Carrique L, Vadon-Le Goff S, Mariano N, Georges RN, Delolme F, Koivunen P, Myllyharju J, Moali C, Aghajari N, Hulmes DJS (2016) Structural basis of homo- and heterotrimerization of collagen I. Nature Commun, in press
Shoulders MD, Raines RT (2009) Collagen structure and stability. Annu Rev Biochem 78:929–958. doi:10.1146/annurev.biochem.77.032207.120833
Shoulders MD, Satyshur KA, Forest KT, Raines RT (2010) Stereoelectronic and steric effects in side chains preorganize a protein main chain. Proc Natl Acad Sci U S A 107(2):559–564. doi:10.1073/pnas.0909592107
Smith SM, Birk DE (2012) Focus on molecules: collagens V and XI. Exp Eye Res 98:105–106. doi:10.1016/j.exer.2010.08.003
Sun M, Chen S, Adams SM, Florer JB, Liu H, Kao WW, Wenstrup RJ, Birk DE (2011) Collagen V is a dominant regulator of collagen fibrillogenesis: dysfunctional regulation of structure and function in a corneal-stroma-specific Col5a1-null mouse model. J Cell Sci 124(Pt 23):4096–4105. doi:10.1242/jcs.091363
Sweeney SM, Orgel JP, Fertala A, McAuliffe JD, Turner KR, Di Lullo GA, Chen S, Antipova O, Perumal S, Ala-Kokko L, Forlino A, Cabral WA, Barnes AM, Marini JC, San Antonio JD (2008) Candidate cell and matrix interaction domains on the collagen fibril, the predominant protein of vertebrates. J Biol Chem 283(30):21187–21197. doi:10.1074/jbc.M709319200
Taga Y, Kusubata M, Ogawa-Goto K, Hattori S (2016) Developmental stage-dependent regulation of prolyl 3-hydroxylation in tendon type I collagen. J Biol Chem 291(2):837–847. doi:10.1074/jbc.M115.686105
Taylor SH, Yeung CY, Kalson NS, Lu Y, Zigrino P, Starborg T, Warwood S, Holmes DF, Canty-Laird EG, Mauch C, Kadler KE (2015) Matrix metalloproteinase 14 is required for fibrous tissue expansion. Elife 4:e09345. doi:10.7554/eLife.09345
Terajima M, Perdivara I, Sricholpech M, Deguchi Y, Pleshko N, Tomer KB, Yamauchi M (2014) Glycosylation and cross-linking in bone type I collagen. J Biol Chem 289(33):22636–22647. doi:10.1074/jbc.M113.528513
Thom JR, Morris NP (1991) Biosynthesis and proteolytic processing of type XI collagen in embryonic chick sterna. J Biol Chem 266(11):7262–7269
Trackman PC (2016) Enzymatic and non-enzymatic functions of the lysyl oxidase family in bone. Matrix Biol 52-54:7–18. doi:10.1016/j.matbio.2016.01.001
Vadon-Le Goff S, Hulmes DJS, Moali C (2015) BMP-1/tolloid-like proteinases synchronize matrix assembly with growth factor activation to promote morphogenesis and tissue remodeling. Matrix Biol 44-46:14–23. doi:10.1016/j.matbio.2015.02.006
Vitagliano L, Berisio R, Mazzarella L, Zagari A (2001) Structural bases of collagen stabilization induced by proline hydroxylation. Biopolymers 58(5):459–464. doi:10.1002/1097-0282(20010415)58:5<459::AID-BIP1021>3.0.CO;2-V
Vranka JA, Pokidysheva E, Hayashi L, Zientek K, Mizuno K, Ishikawa Y, Maddox K, Tufa S, Keene DR, Klein R, Bachinger HP (2010) Prolyl 3-hydroxylase 1 null mice display abnormalities in fibrillar collagen-rich tissues such as tendons, skin, and bones. J Biol Chem 285(22):17253–17262. doi:10.1074/jbc.M110.102228
Wang L, Uhlig PC, Eikenberry EF, Robenek H, Bruckner P, Hansen U (2014) Lateral growth limitation of corneal fibrils and their lamellar stacking depend on covalent collagen cross-linking by transglutaminase-2 and lysyl oxidases, respectively. J Biol Chem 289(2):921–929. doi:10.1074/jbc.M113.496364
Weis MA, Hudson DM, Kim L, Scott M, Wu JJ, Eyre DR (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(4):2580–2590. doi:10.1074/jbc.M109.068726
Widmer C, Gebauer JM, Brunstein E, Rosenbaum S, Zaucke F, Drogemuller C, Leeb T, Baumann U (2012) Molecular basis for the action of the collagen-specific chaperone Hsp47/SERPINH1 and its structure-specific client recognition. Proc Natl Acad Sci U S A 109(33):13243–13247. doi:10.1073/pnas.1208072109
Yamauchi M, Sricholpech M (2012) Lysine post-translational modifications of collagen. Essays Biochem 52:113–133. doi:10.1042/bse0520113
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. doi:10.1182/blood-2015-08-667055
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Bella, J., Hulmes, D.J.S. (2017). Fibrillar Collagens. In: Parry, D., Squire, J. (eds) Fibrous Proteins: Structures and Mechanisms. Subcellular Biochemistry, vol 82. Springer, Cham. https://doi.org/10.1007/978-3-319-49674-0_14
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