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• W2079120812 abstract "The α-chains of the collagen superfamily are encoded with information that specifies self-assembly into fibrils, microfibrils, and networks that have diverse functions in the extracellular matrix. A key self-organizing step, common to all collagen types, is trimerization that selects, binds, and registers cognate α-chains for assembly of triple helical protomers that subsequently oligomerize into specific suprastructures. In this article, we review recent findings on the mechanism of chain selection and infer that terminal noncollagenous domains function as recognition modules in trimerization and are therefore key determinants of specificity in the assembly of suprastructures. This mechanism is also illustrated with computer-generated animations. The α-chains of the collagen superfamily are encoded with information that specifies self-assembly into fibrils, microfibrils, and networks that have diverse functions in the extracellular matrix. A key self-organizing step, common to all collagen types, is trimerization that selects, binds, and registers cognate α-chains for assembly of triple helical protomers that subsequently oligomerize into specific suprastructures. In this article, we review recent findings on the mechanism of chain selection and infer that terminal noncollagenous domains function as recognition modules in trimerization and are therefore key determinants of specificity in the assembly of suprastructures. This mechanism is also illustrated with computer-generated animations. Collagens are modular triple helical proteins that constitute the major structural components of the extracellular matrix of all animals. They occur as diverse suprastructures such as fibrils, microfibrils, and networks, which serve as self-organizing scaffolds for the attachment of other macromolecular complexes including laminin networks, proteoglycans, and cell surface receptors. The suprastructures play functional roles in cell adhesion, cell differentiation, tissue development, and the structural integrity of organs. Collagen suprastructures are assembled from a large family of gene products called α-chains. To date, 43 unique α-chains that belong to 28 types of collagens (types I–XXVIII) have been discovered in vertebrates. Based on their supramolecular architectures, they are further classified as fibril-forming, fibril-associated containing interrupted triple helices (FACIT), 3The abbreviations used are: FACIT, fibril-associated collagens with interrupted triple helices; NC domain, noncollagenous domain; N-NC domain, amino-terminal noncollagenous domain, which is the same as N-propeptide; C-NC domain, carboxyl-terminal noncollagenous domain, which is the same as C-propeptide. beaded filament, anchoring fibril, network-forming, and transmembrane collagens (1Myllyharju J. Kivirikko K.I. Trends Genet. 2004; 20: 33-43Abstract Full Text Full Text PDF PubMed Scopus (899) Google Scholar, 4Veit G. Kobbe B. Keene D.R. Paulsson M. Koch M. Wagener R. J. Biol. Chem. 2006; 281: 3494-3504Abstract Full Text Full Text PDF PubMed Scopus (147) Google Scholar). The assembly of all collagen suprastructures begins with the association of three type-specific α-chains (trimerization) that subsequently intertwine to form triple helical protomers, the building blocks of larger assemblies (1Myllyharju J. Kivirikko K.I. Trends Genet. 2004; 20: 33-43Abstract Full Text Full Text PDF PubMed Scopus (899) Google Scholar, 5Brodsky B. Ramshaw J.A. Matrix Biol. 1997; 15: 545-554Crossref PubMed Scopus (406) Google Scholar). Protomers are homotrimers or heterotrimers, composed of up to three different α-chains. They have in common at least one triple helical collagenous domain of varying length and two noncollagenous domains (NC) of variable sequence, size, and shape that are positioned at the N and C termini, designated herein as N-NC and C-NC domains, respectively. The terminal NC domains are excised, modified, or incorporated directly into the final suprastructure, depending on protomer type and function. Subsequently, specific protomers oligomerize into distinct suprastructures involving interactions that form end-to-end connections, lateral associations, and supercoiling of helices. Thus, protomer formation and oligomerization involve pivotal recognitions steps that target specific α-chains to assemble into a particular type of suprastructure. How the α-chains selectively recognize each other is a fundamental question in matrix biology that remains largely unanswered. Early studies on collagens I and III suggested that the C-NC domains play a critical role in the trimerization step that involves selection, binding, and registration of three α-chains (6Fessler L.I. Fessler J.H. J. Biol. Chem. 1974; 249: 7637-7646Abstract Full Text PDF PubMed Google Scholar, 9Dion A.S. Myers J.C. J. Mol. Biol. 1987; 193: 127-143Crossref PubMed Scopus (66) Google Scholar). In this article, we review recent findings on the trimerization of collagens, with an emphasis on collagens I and IV, which are the best understood. Fibril-forming collagens include the widely distributed types I, III, and V, types II and XI, prominent in cartilage and eye, and the newly discovered types XXIV and XXVII (10Boot-Handford R.P. Tuckwell D.S. Plumb D.A. Rock C.F. Poulsom R. J. Biol. Chem. 2003; 278: 31067-31077Abstract Full Text Full Text PDF PubMed Scopus (125) Google Scholar, 12Koch M. Laub F. Zhou P. Hahn R.A. Tanaka S. Burgeson R.E. Gerecke D.R. Ramirez F. Gordon M.K. J. Biol. Chem. 2003; 278: 43236-43244Abstract Full Text Full Text PDF PubMed Scopus (95) Google Scholar). All of the 12 fibril-forming α-chains share a long uninterrupted collagenous domain flanked by N- and C-terminal noncollagenous propeptides. The α-chains assemble into at least 12 type-specific protomers, characterized as homo- and heterotrimers. The terminal propeptides are further cleaved by specific proteases, which promote oligomerization and fibril formation. Type I collagen is composed of α1- and α2-chains, forming preferably an α1·α1·α2 heterotrimer (Fig. 1). However, if only the triple helical domains are considered, the (α1)3 homotrimer would be the preferred form (13Kuznetsova N.V. McBride D.J. Leikin S. J. Mol. Biol. 2003; 331: 191-200Crossref PubMed Scopus (56) Google Scholar, 14Leikina E. Mertts M.V. Kuznetsova N. Leikin S. Proc. Natl. Acad. Sci. U. S. A. 2002; 99: 1314-1318Crossref PubMed Scopus (455) Google Scholar). The pro-α1 homotrimer is formed as the default structure in the absence of pro-α2-chain, whereas the opposite is not true (15Myllyharju J. Lamberg A. Notbohm H. Fietzek P.P. Pihlajaniemi T. Kivirikko K.I. J. Biol. Chem. 1997; 272: 21824-21830Abstract Full Text Full Text PDF PubMed Scopus (78) Google Scholar). However, if the α2 C-NC domain is replaced with an artificial trimeric NC domain, an α2 homotrimer can form (16McLaughlin S.H. Bulleid N.J. Matrix Biol. 1998; 16: 369-377Crossref PubMed Scopus (99) Google Scholar, 17Bulleid N.J. Dalley J.A. Lees J.F. EMBO J. 1997; 16: 6694-6701Crossref PubMed Scopus (87) Google Scholar). Thus the α2 C-NC domain is the key domain required for heterotrimer assembly, although the α1 C-NC domain contains sufficient information for directing homotrimer formation. Disulfide bonding in the α2 C-NC domain is crucial for heterotrimer formation (18Koivu J. FEBS Lett. 1987; 217: 216-220Crossref PubMed Scopus (7) Google Scholar), particularly within the most C-terminal sequence of the α2 C-NC domain (19Lim A.L. Doyle S.A. Balian G. Smith B.D. J. Cell. Biochem. 1998; 71: 216-232Crossref PubMed Scopus (19) Google Scholar, 20Doyle S.A. Smith B.D. J. Cell. Biochem. 1998; 71: 233-242Crossref PubMed Scopus (17) Google Scholar). The putative conformation and energy-minimized structures of the human α1 C-NC and α2 C-NC reveal (21Veis A. Alvares K. Malone J.P. Proc. Indian Acad. Sci. Chem. Sci. 1999; 111: 115-120Google Scholar, 22Alvares K. Siddiqui F. Malone J. Veis A. Biochemistry. 1999; 38: 5401-5411Crossref PubMed Scopus (14) Google Scholar) that each contains five subdomains (Fig. 1A) (8Doege K.J. Fessler J.H. J. Biol. Chem. 1986; 261: 8924-8935Abstract Full Text PDF PubMed Google Scholar, 23Hulmes D.J. J. Struct. Biol. 2002; 137: 2-10Crossref PubMed Scopus (451) Google Scholar). Domain I folds into subdomains Ia and Ib without α-helical or β-sheet conformations, inconsistent with suggestions that subdomain Ia participates in trimerization by forming α-helical coiled-coils (23Hulmes D.J. J. Struct. Biol. 2002; 137: 2-10Crossref PubMed Scopus (451) Google Scholar, 25McAlinden A. Smith T.A. Sandell L.J. Ficheux D. Parry D.A. Hulmes D.J. J. Biol. Chem. 2003; 278: 42200-42207Abstract Full Text Full Text PDF PubMed Scopus (68) Google Scholar). Subdomain Ib contains the interchain disulfide bonds in the assembled C-NC trimer. Domains II and IV fold into globular regions G1 and G2, respectively. These are linked by an antiparallel β-sheet assembled from domains III and V (Fig. 1). Energy minimization and molecular dynamics simulations have revealed key steps in the folding, docking, and assembly of two α1 C-NC (α11 and α12) and α2 C-NC domains into a heterotrimer (26Malone J.P. Alvares K. Veis A. Biochemistry. 2005; 44: 15269-15279Crossref PubMed Scopus (17) Google Scholar). Folding is initiated at the C terminus by bimolecular association of the α2 and α12, near the junction of domain III and domain IV-G2, and proceeds toward the N terminus (Fig. 1B). The α2 domain V appears to have a dominant effect on heterotrimer formation (19Lim A.L. Doyle S.A. Balian G. Smith B.D. J. Cell. Biochem. 1998; 71: 216-232Crossref PubMed Scopus (19) Google Scholar, 20Doyle S.A. Smith B.D. J. Cell. Biochem. 1998; 71: 233-242Crossref PubMed Scopus (17) Google Scholar). Trimerization proceeds via a second interaction between the α2-α12 dimer and the α11 at domain II-G1 after which the interchain disulfide bonds become established in domain Ib. Folding of domain Ia is the last and slowest folding step but eventually drives the folding through the C-telo-Ia junction (26Malone J.P. Alvares K. Veis A. Biochemistry. 2005; 44: 15269-15279Crossref PubMed Scopus (17) Google Scholar, 27Malone J.P. George A. Veis A. Proteins. 2004; 54: 206-215Crossref PubMed Scopus (46) Google Scholar). Overall, the α2 C-NC domain appears to provide the driving force for heterotrimer formation. Computer modeling of collagen I C-propeptide (26Malone J.P. Alvares K. Veis A. Biochemistry. 2005; 44: 15269-15279Crossref PubMed Scopus (17) Google Scholar) also suggests that the homotrimer could resemble a cruciform as seen in the collagen III C-propeptide (28Bernocco S. Finet S. Ebel C. Eichenberger D. Mazzorana M. Farjanel J. Hulmes D.J. J. Biol. Chem. 2001; 276: 48930-48936Abstract Full Text Full Text PDF PubMed Scopus (31) Google Scholar). Putative trimerization control sequences have been located within the C-NC domains (17Bulleid N.J. Dalley J.A. Lees J.F. EMBO J. 1997; 16: 6694-6701Crossref PubMed Scopus (87) Google Scholar, 29Lees J.F. Tasab M. Bulleid N.J. EMBO J. 1997; 16: 908-916Crossref PubMed Scopus (126) Google Scholar). Replacing the α2(I) C-NC domain of the α2(I)-chain with the homotrimer-directing α1(III) C-NC permitted α2·α2·α2 homo-trimerization (17Bulleid N.J. Dalley J.A. Lees J.F. EMBO J. 1997; 16: 6694-6701Crossref PubMed Scopus (87) Google Scholar, 29Lees J.F. Tasab M. Bulleid N.J. EMBO J. 1997; 16: 908-916Crossref PubMed Scopus (126) Google Scholar)), demonstrating that the α1 C-NC domain is sufficient to direct homotrimer assembly of α2-chains with aligned triple helices. Exchanging specific sequences from the α1 C-NC domain of collagen III with the corresponding sequences of the α2 C-NC of collagen I revealed the location of a putative recognition site, a discontinuous sequence of 15 amino acids, located at the C-terminal of subdomain III (Fig. 1). This α1 sequence, when transferred to the sequence-equivalent region of the α2 C-NC domain, enabled the α2-chains to homotrimerize (17Bulleid N.J. Dalley J.A. Lees J.F. EMBO J. 1997; 16: 6694-6701Crossref PubMed Scopus (87) Google Scholar, 29Lees J.F. Tasab M. Bulleid N.J. EMBO J. 1997; 16: 908-916Crossref PubMed Scopus (126) Google Scholar). Thus, this recognition site is both necessary and sufficient to ensure that collagen chains discriminate between each other to form type-specific protomers (Fig. 1, A and C). The network-forming collagens include types IV, VIII and X. In contrast to the fibril-forming collagens, their C-NC domains are retained in their suprastructures. Importantly, crystal structures of their C-NC domains are known, which provide insight into the mechanisms of chain selection. Collagen IV—Type IV collagen is the major constituent of basement membranes. It is composed of a family of six homologous α-chains (α1–α6), each characterized by a long collagenous domain of ∼1400 residues, interrupted by about 20 short noncollagenous sequences, which is flanked by a short N-NC sequence of 25 residues and a globular C-NC domain of 230 residues. The six α-chains assemble into three heterotrimeric protomers (α1·α1·α2, α3·α4·α5, and α5·α5·α6), which further assemble into three distinct networks (30Hudson B.G. Tryggvason K. Sundaramoorthy M. Neilson E.G. N. Engl. J. Med. 2003; 348: 2543-2556Crossref PubMed Scopus (770) Google Scholar). Collagen IV has provided a unique opportunity to gain insight into chain recognition mechanisms. First, the six α-chains assemble into 3 specific protomers out of 76 possible combinations, reflecting a remarkable specificity for chain selection in vivo (30Hudson B.G. Tryggvason K. Sundaramoorthy M. Neilson E.G. N. Engl. J. Med. 2003; 348: 2543-2556Crossref PubMed Scopus (770) Google Scholar, 31Sundaramoorthy M. Meiyappan M. Todd P. Hudson B.G. J. Biol. Chem. 2002; 277: 31142-31153Abstract Full Text Full Text PDF PubMed Scopus (136) Google Scholar). Second, the extraordinary capacity of monomeric C-NC domains to recognize each other and reassemble in vitro into their original trimeric and hexameric compositions (32Boutaud A. Borza D.B. Bondar O. Gunwar S. Netzer K.O. Singh N. Ninomiya Y. Sado Y. Noelken M.E. Hudson B.G. J. Biol. Chem. 2000; 275: 30716-30724Abstract Full Text Full Text PDF PubMed Scopus (180) Google Scholar), together with their critical role in trimerization in vivo (33Soder S. Poschl E. Biochem. Biophys. Res. Commun. 2004; 325: 276-280Crossref PubMed Scopus (19) Google Scholar), indicates a recognition role in assembly and provides the means to characterize specificity and binding parameters (34Khoshnoodi J. Sigmundsson K. Cartailler J.P. Bondar O. Sundaramoorthy M. Hudson B.G. J. Biol. Chem. 2006; 281: 6058-6069Abstract Full Text Full Text PDF PubMed Scopus (44) Google Scholar). Third, the crystal structure of the C-NC hexamer is known (31Sundaramoorthy M. Meiyappan M. Todd P. Hudson B.G. J. Biol. Chem. 2002; 277: 31142-31153Abstract Full Text Full Text PDF PubMed Scopus (136) Google Scholar, 35Than M.E. Henrich S. Huber R. Ries A. Mann K. Kuhn K. Timpl R. Bourenkov G.P. Bartunik H.D. Bode W. Proc. Natl. Acad. Sci. U. S. A. 2002; 99: 6607-6612Crossref PubMed Scopus (105) Google Scholar), which reveals the nature of intermolecular interactions and their role in chain selectivity. Fourth, the known primary structure for all six C-NC domains from many species provides information needed to deduce candidate recognition sites from sequence variation (34Khoshnoodi J. Sigmundsson K. Cartailler J.P. Bondar O. Sundaramoorthy M. Hudson B.G. J. Biol. Chem. 2006; 281: 6058-6069Abstract Full Text Full Text PDF PubMed Scopus (44) Google Scholar). Finally, a study of sequence variation, coupled with structural and kinetic analysis, provides the requisite information needed to decipher the location and three-dimensional features of putative recognition sites (34Khoshnoodi J. Sigmundsson K. Cartailler J.P. Bondar O. Sundaramoorthy M. Hudson B.G. J. Biol. Chem. 2006; 281: 6058-6069Abstract Full Text Full Text PDF PubMed Scopus (44) Google Scholar). Two putative recognition sites were identified in the C-NC domains as prominent mediators in the mechanism of chain recognition (34Khoshnoodi J. Sigmundsson K. Cartailler J.P. Bondar O. Sundaramoorthy M. Hudson B.G. J. Biol. Chem. 2006; 281: 6058-6069Abstract Full Text Full Text PDF PubMed Scopus (44) Google Scholar). These sites (Fig. 2D) constitute a 13-residue-long β-hairpin motif (site 1) involved in the domain swapping mechanism and a 15-residue-long variable region (site 2, VR3, docking site) with sequence hypervariability across all the chains of collagen IV (34Khoshnoodi J. Sigmundsson K. Cartailler J.P. Bondar O. Sundaramoorthy M. Hudson B.G. J. Biol. Chem. 2006; 281: 6058-6069Abstract Full Text Full Text PDF PubMed Scopus (44) Google Scholar). Accordingly, we have proposed that the combination of sequence variations at these two sites and at the neighboring C-NC domains to which they interact constitutes the code that directs chain recognition in the trimerization of collagen IV (34Khoshnoodi J. Sigmundsson K. Cartailler J.P. Bondar O. Sundaramoorthy M. Hudson B.G. J. Biol. Chem. 2006; 281: 6058-6069Abstract Full Text Full Text PDF PubMed Scopus (44) Google Scholar). The relatively higher affinity of α2 C-NC domain for dimer formation with an α1 C-NC domain is the driving force in directing stoichiometry in the assembly of α1·α1·α2 heterotrimers, as determined by kinetic studies using surface plasmon resonance (34Khoshnoodi J. Sigmundsson K. Cartailler J.P. Bondar O. Sundaramoorthy M. Hudson B.G. J. Biol. Chem. 2006; 281: 6058-6069Abstract Full Text Full Text PDF PubMed Scopus (44) Google Scholar). Collagen VIII—Type VIII collagen is a prominent component of Descemet membrane and in the subendothelium of vascular walls (36Sage H. Pritzl P. Bornstein P. Biochemistry. 1980; 19: 5747-5755Crossref PubMed Scopus (92) Google Scholar). It is composed of highly conserved α1(VIII)- and α2(VIII)-chains, which contain a short collagenous domain of 454 residues flanked by a N-NC domain of 117 residues and a C-NC domain of 173 residues (37Muragaki Y. Jacenko O. Apte S. Mattei M.G. Ninomiya Y. Olsen B.R. J. Biol. Chem. 1991; 266: 7721-7727Abstract Full Text PDF PubMed Google Scholar). The chains assemble into two distinct homotrimers that assemble into hexagonal lattices (38Greenhill N.S. Ruger B.M. Hasan Q. Davis P.F. Matrix Biol. 2000; 19: 19-28Crossref PubMed Scopus (47) Google Scholar, 39Stephan S. Sherratt M.J. Hodson N. Shuttleworth C.A. Kielty C.M. J. Biol. Chem. 2004; 279: 21469-21477Abstract Full Text Full Text PDF PubMed Scopus (50) Google Scholar). The crystal structure of the α1 C-NC homotrimer is known (40Kvansakul M. Bogin O. Hohenester E. Yayon A. Matrix Biol. 2003; 22: 145-152Crossref PubMed Scopus (53) Google Scholar), but the basis for the preferred homotrimer structure remains unclear. Collagen X—Type X collagen is expressed in the endochondral growth plate. The single α1-chain contains a short collagenous domain of 154 residues, flanked by a N-NC domain of 37 residues and a C-NC domain of 161 residues (41Ninomiya Y. van der Gordon M. Rest M. Schmid T. Linsenmayer T. Olsen B.R. J. Biol. Chem. 1986; 261: 5041-5050Abstract Full Text PDF PubMed Google Scholar). Its protomer is a homotrimer. The C-NC domains function as nucleation sites for trimer and multimer formation, based on experiments using recombinant C-NC domains (42Zhang Y. Chen Q. J. Biol. Chem. 1999; 274: 22409-22413Abstract Full Text Full Text PDF PubMed Scopus (31) Google Scholar). A comparison of the x-ray crystal structures of the C-NC trimer of collagens X and VIII revealed them to be highly homologous, but they differ in intermolecular contact residues that govern trimer stability. Such differences may also confer specificity (40Kvansakul M. Bogin O. Hohenester E. Yayon A. Matrix Biol. 2003; 22: 145-152Crossref PubMed Scopus (53) Google Scholar, 43Bogin O. Kvansakul M. Rom E. Singer J. Yayon A. Hohenester E. Structure. 2002; 10: 165-173Abstract Full Text Full Text PDF PubMed Scopus (96) Google Scholar). The FACIT collagens include types IX, XII, XIV, XVI, XIX, XX, XXI, and XXII. Collagen IX is composed of three α-chains and all others of one α-chain, each of which is characterized by short collagenous domains interrupted by several NC domains (1Myllyharju J. Kivirikko K.I. Trends Genet. 2004; 20: 33-43Abstract Full Text Full Text PDF PubMed Scopus (899) Google Scholar, 2Ricard-Blum S. Ruggiero F. Pathol. Biol. (Paris). 2005; 53: 430-442Crossref PubMed Scopus (279) Google Scholar). The protomer of collagen IX is a heterotrimer, and all others are homotrimers, accounting for at least 9 distinct protomers. Unlike the fibril-forming collagens, the FACITs have significantly shorter C-NC domains: 75 residues for collagen XII and fewer than 30 residues for collagen IX, whereas those of fibrillar collagen are about 260 residues. The FACITs share a remarkable sequence homology at their COL1/C-NC1 junctions by having two strictly conserved cysteine residues separated by four residues at the NC domain. Several lines of evidence suggest that the COL1 domain at the COL1/C-NC junction (which contains the first cysteine residue) and the C-NC domain (containing the second conserved cysteine) are involved in the mechanism of chain selection in the assembly of collagens XII and XIV (44Mazzorana M. Gruffat H. van der Sergeant A. Rest M. J. Biol. Chem. 1993; 268: 3029-3032Abstract Full Text PDF PubMed Google Scholar, 46Lesage A. Penin F. Geourjon C. van der Marion D. Rest M. Biochemistry. 1996; 35: 9647-9660Crossref PubMed Scopus (32) Google Scholar). Independent studies by Mazzorana et al. (44Mazzorana M. Gruffat H. van der Sergeant A. Rest M. J. Biol. Chem. 1993; 268: 3029-3032Abstract Full Text PDF PubMed Google Scholar, 45Mazzorana M. van der Giry-Lozinguez C. Rest M. Matrix Biol. 1995; 14: 583-588Crossref PubMed Scopus (14) Google Scholar) and Lesage et al. (46Lesage A. Penin F. Geourjon C. van der Marion D. Rest M. Biochemistry. 1996; 35: 9647-9660Crossref PubMed Scopus (32) Google Scholar) strongly suggest that both the collagenous portion and the NC domain are involved in formation and stabilization of protomers in collagens XII and XIV (47Mazzorana M. Cogne S. Goldschmidt D. Aubert-Foucher E. J. Biol. Chem. 2001; 276: 27989-27998Abstract Full Text Full Text PDF PubMed Scopus (17) Google Scholar). Collagen VI—Type VI collagen is ubiquitously expressed in connective tissues. It is composed of three genetically distinct α-chains, α1, α2, and α3, that form extensive beaded filaments (48Lamande S.R. Morgelin M. Adams N.E. Selan C. Allen J.M. J. Biol. Chem. 2006; 281: 16607-16614Abstract Full Text Full Text PDF PubMed Scopus (53) Google Scholar, 50Ball S.G. Baldock C. Kielty C.M. Shuttleworth C.A. J. Biol. Chem. 2001; 276: 7422-7430Abstract Full Text Full Text PDF PubMed Scopus (36) Google Scholar). Each chain contains a relatively short collagenous domain of ∼335 residues flanked by N-NC and C-NC globular domains The α1- and α2-chains are similar in size and contain one N-NC domain and a C-NC domain with two subdomains, C1 and C2. In contrast, the α3-chain is much longer, and the N-NC domain contains ten subdomains, N1–N10, and five C-NC subdomains, C1–C5 (48Lamande S.R. Morgelin M. Adams N.E. Selan C. Allen J.M. J. Biol. Chem. 2006; 281: 16607-16614Abstract Full Text Full Text PDF PubMed Scopus (53) Google Scholar). The protomer is an α1·α2·α3 heterotrimer. Studies conducted on cell lines lacking or expressing different combinations of recombinant α-chains have shown that the α3-chain contains sequences necessary for chain association and protomer formation (48Lamande S.R. Morgelin M. Adams N.E. Selan C. Allen J.M. J. Biol. Chem. 2006; 281: 16607-16614Abstract Full Text Full Text PDF PubMed Scopus (53) Google Scholar, 50Ball S.G. Baldock C. Kielty C.M. Shuttleworth C.A. J. Biol. Chem. 2001; 276: 7422-7430Abstract Full Text Full Text PDF PubMed Scopus (36) Google Scholar). Deletion studies have demonstrated that whereas the C5 subdomain of the α3-chain is required for the extracellular microfibril formation, the C1 subdomain, illustrated in Fig. 3, in all chains is sufficient for chain recognition and protomer assembly (48Lamande S.R. Morgelin M. Adams N.E. Selan C. Allen J.M. J. Biol. Chem. 2006; 281: 16607-16614Abstract Full Text Full Text PDF PubMed Scopus (53) Google Scholar, 50Ball S.G. Baldock C. Kielty C.M. Shuttleworth C.A. J. Biol. Chem. 2001; 276: 7422-7430Abstract Full Text Full Text PDF PubMed Scopus (36) Google Scholar). Collagen VII—Type VII collagen is a major component of anchoring fibrils that maintain the epidermal-dermal adherence of skin. It is composed of three identical α-chains, each consisting of a collagenous domain of 1530 residues with 19 interruptions, which are flanked by N-NC and C-NC domains (51Christiano A.M. Greenspan D.S. Lee S. Uitto J. J. Biol. Chem. 1994; 269: 20256-20262Abstract Full Text PDF PubMed Google Scholar). Protomers form anti-parallel dimers that are stabilized by disulfide bonding via the C-NC domains of adjacent protomers. Following proteolytic modification of the C-NC domain, dimers of protomers oligomerize laterally to form anchoring fibrils with large globular N-NC domains at both ends of the microfibril (52Chen M. Costa F.K. Lindvay C.R. Han Y.P. Woodley D.T. J. Biol. Chem. 2002; 277: 2118-2124Abstract Full Text Full Text PDF PubMed Scopus (71) Google Scholar). Recent studies, using recombinant constructs and site-directed mutagenesis, have revealed that the C-NC domain mediates protomer formation and oligomerization of protomers (52Chen M. Costa F.K. Lindvay C.R. Han Y.P. Woodley D.T. J. Biol. Chem. 2002; 277: 2118-2124Abstract Full Text Full Text PDF PubMed Scopus (71) Google Scholar). Transmembrane collagens include types XIII, XVII, XXIII, and XXV and other collagen-related proteins, such as the macrophage receptor MARCO (53Elomaa O. Sankala M. Pikkarainen T. Bergmann U. Tuuttila A. Raatikainen-Ahokas A. Sariola H. Tryggvason K. J. Biol. Chem. 1998; 273: 4530-4538Abstract Full Text Full Text PDF PubMed Scopus (123) Google Scholar). They function as cell surface receptors and matrix components (54Franzke C.W. Bruckner P. Bruckner-Tuderman L. J. Biol. Chem. 2005; 280: 4005-4008Abstract Full Text Full Text PDF PubMed Scopus (148) Google Scholar). The α-chain of each type contains an N-terminal NC domain, which is comprised of (a) three subdomains, an intracellular, a single transmembrane, and an extracellular juxtamembrane linker subdomain and (b) a large extracellular domain, which is composed of multiple collagenous domains interrupted by NC domains. The protomer of each α-chain is a homotrimer. The extracellular linker subdomain contains an α-helical coiled-coil, the conformation of which is thought to prompt trimerization and subsequent zipper-like folding of the triple helical domain. Studies using deletion constructs have shown that the N-NC domains of collagens XIII and XVII are necessary for triple helix formation, suggesting that nucleation of the triple helix occurs at the N-terminal region and proceeds in a N- to C-terminal direction, which is opposite to that of all other classes of collagens (55Snellman A. Tu H. Vaisanen T. Kvist A.P. Huhtala P. Pihlajaniemi T. EMBO J. 2000; 19: 5051-5059Crossref PubMed Scopus (78) Google Scholar, 56Areida S.K. Reinhardt D.P. Muller P.K. Fietzek P.P. Kowitz J. Marinkovich M.P. Notbohm H. J. Biol. Chem. 2001; 276: 1594-1601Abstract Full Text Full Text PDF PubMed Scopus (60) Google Scholar). For collagen XIII, a short sequence of 21 residues located at the juxtamembrane linker subdomain, has been identified as a putative recognition site for trimerization (Fig. 3). Little is known about the assembly of collagen XV (57Myers J.C. Kivirikko S. Gordon M.K. Dion A.S. Pihlajaniemi T. Proc. Natl. Acad. Sci. U. S. A. 1992; 89: 10144-10148Crossref PubMed Scopus (65) Google Scholar) and XVIII (58Rehn M. Hintikka E. Pihlajaniemi T. J. Biol. Chem. 1994; 269: 13929-13935Abstract Full Text PDF PubMed Google Scholar) and the newly discovered XXVI (59Sato K. Yomogida K. Wada T. Yorihuzi T. Nishimune Y. Hosokawa N. Nagata K. J. Biol. Chem. 2002; 277: 37678-37684Abstract Full Text Full Text PDF PubMed Scopus (74) Google Scholar) and XXVIII (4Veit G. Kobbe B. Keene D.R. Paulsson M. Koch M. Wagener R. J. Biol. Chem. 2006; 281: 3494-3504Abstract Full Text Full Text PDF PubMed Scopus (147) Google Scholar). Each type is composed of a single α-chain that contains a collagenous domain, with frequent interruptions, flanked by N-NC and C-NC domains. The C-NC domain of XVIII forms trimers in vitro suggesting a role in protomer assembly (60Sasaki T. Fukai N. Mann K. Gohring W. Olsen B.R. Timpl R. EMBO J. 1998; 17: 4249-4256Crossref PubMed Scopus (328) Google Scholar). The crystal structures of fragments of C-NC domains of XV and XVIII are highly similar but distinct (61Hohenester E. Sasaki T. Olsen B.R. Timpl R. EMBO J. 1998; 17: 1656-1664Crossref PubMed Scopus (199) Google Scholar, 62Sasaki T. Larsson H. Tisi D. Claesson-Welsh L. Hohenester E. Timpl R. J. Mol. Biol. 2000; 301: 1179-1190Crossref PubMed Scopus (196) Google Scholar), and they differ greatly with the three-dimensional structures of the C-NC domains of collagens VIII, X, and IV (see above); such distinctions are consistent with a special role of C-NC domains in chain selection. Over the last decade, findings have emerged on several collagen types that provide new insights into the chain selection mechanism. Based on the body of evidence reviewed here, we infer that the terminal NC domains function as recognition modules that select, bind, and register three cognate α-chains for self-assembly of triple helical protomers. The C-NC domains govern chain selection for all classes except for the transmembrane collagens, which are governed by the N-NC domains (Fig. 3). As recognition modules, they contain sites that are characterized by positive determinants of shape complementarity, electrostatic charge distribution and magnitude, and hydrophobicity for selection of cognate α-chains and negative determinants for the exclusion of all other unrelated α-chains." @default.
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• W2079120812 date "2006-12-01" @default.
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• W2079120812 title "Molecular Recognition in the Assembly of Collagens: Terminal Noncollagenous Domains Are Key Recognition Modules in the Formation of Triple Helical Protomers" @default.
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• W2079120812 doi "https://doi.org/10.1074/jbc.r600025200" @default.
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