1 Alpha-helical coiled-coil oligomerization domains are almost ubiquitous in the collagen superfamily* Audrey McAlinden 1 , Thomasin A. Smith 2 , Linda J. Sandell 1 , Damien Ficheux 3 , David A.D. Parry 2 and David J.S. Hulmes 3 1 Department of Orthopedic Surgery, Washington University School of Medicine, Barnes- Jewish Hospital, St Louis, MI 63110, USA; 2 Institute of Fundamental Sciences, Massey University, Palmerston North, New Zealand; 3 Institut de Biologie et Chimie des Protéines, CNRS UMR 5086, Université Claude Bernard Lyon 1, 69367 Lyon cedex 7, France. Corresponding author : Dr D.J.S. Hulmes, IBCP, 7 passage du Vercors, 69367 Lyon cedex 07, France. Tel : (33) (0)4 72 72 26 67; Fax : (33) (0)4 72 72 26 04; e-mail : [email protected]Running Title : Coiled-coil domains in the collagen superfamily *This work was supported by the CNRS (Programme “Protéomique et Ingeniérie des Protéines”) and National Institutes of Health Grants AR48250-01 (to A.M.) and AR-36994 (to L.S.). Copyright 2003 by The American Society for Biochemistry and Molecular Biology, Inc. JBC Papers in Press. Published on August 14, 2003 as Manuscript M302429200 by guest on January 17, 2020 http://www.jbc.org/ Downloaded from
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Alpha-helical coiled-coil oligomerization domains are ... · 2 Summary Alpha-helical coiled-coils are widely occurring protein oligomerization motifs. Here we show that most members
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1
Alpha-helical coiled-coil oligomerization domains are almost ubiquitous in
the collagen superfamily*
Audrey McAlinden1, Thomasin A. Smith2, Linda J. Sandell1, Damien Ficheux3, David
A.D. Parry2 and David J.S. Hulmes3
1Department of Orthopedic Surgery, Washington University School of Medicine, Barnes-
Jewish Hospital, St Louis, MI 63110, USA; 2Institute of Fundamental Sciences, Massey
University, Palmerston North, New Zealand; 3Institut de Biologie et Chimie des Protéines,
CNRS UMR 5086, Université Claude Bernard Lyon 1, 69367 Lyon cedex 7, France.
Corresponding author :
Dr D.J.S. Hulmes, IBCP, 7 passage du Vercors, 69367 Lyon cedex 07, France.
The mechanisms controlling chain oligomerization in extracellular matrix and related
proteins are currently topics of active research (1, 2). In the case of the collagen superfamily,
which includes both collagens and collagen-like proteins (3-5), a number of structural features
have been identified that are essential for bringing together component polypeptide chains
with the correct stoichiometry, thus leading to folding of the triple-helix. Early studies on the
procollagen precursors of the fibrillar collagens (types I, II, III, V and XI) (6) showed that the
C-propeptide regions are necessary to direct correct chain association, which is followed by
zipper-like folding of the triple-helix in the C- to N-terminal direction (7). This concept was
subsequently extended to basement membrane collagen type IV (8-10), microfibril forming
collagen VI (11, 12), members of the C1q family (13) including collagens VIII and X (14-17)
and the emilins (18), and the FACITs1 (19-21).
Alpha-helical coiled coils have been shown to be oligomerization domains in both
collagens and collagen-like proteins. The paradigm here is the collectin family (22), which
includes the lung surfactant proteins (SP-A, SP-D), mannan binding proteins (MBP-A, MBP-
C), conglutinin and collectin-43. Collectins are trimeric molecules in which each chain
contains a collagen-like domain followed by an α-helical coiled-coil region and then a
carbohydrate recognition domain (CRD). The amino acid sequence of the coiled-coil domain
is characterized by up to four heptad repeats (a-b-c-d-e-f-g) in which hydrophobic amino acid
residues occur at positions a and d (23). Three dimensional structures of the coiled-coil and
CRD regions in MBP and SP-D show that chains within the trimer are associated via a three-
stranded coiled coil, with the three CRDs arranged as distinct lobes (24-26). Several studies
have shown that the coiled-coil region is both necessary and sufficient for trimerization of SP-
D (27, 28). In a recent study (29), the first two heptad repeats of SP-D were shown to be
1 The abbreviations used are: CHO, chinese hamster ovary; CPII, C-propeptide region of procollagen II; CRD,carbohydrate recognition domain; FACITs, fibril associated collagens with interrupted triple-helices; SP-D,
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| hep1 | hep2 | hep3 | hep4Ia1_h(1190-1259) GPPSAGFD-FSFLP-QPPQEKAHDGGRYYRADD------ NV RDRDLE DTT KS SQQ EN RS EGSRKNPARTCIIa1_h(1143-1214) GPPGPGID-MSAFAGLGPREKGPDPLQYMRADQA----- GG RQHDAE DAT KS NNQ ES RS EGSRKNPARTCIa2_h(1099-1163) GPPGVSGGG---------YDFGYDG-DFYRADQPRS---A SLR KDYE DAT KS NNQ ET LT EGSRKNPARTCIIIa1_h(1191-1262) GAPGPCCGGVGAAAIAGIGGEKAGGFAPYYGDE------ MD KINTDE MTS KS NGQ ES IS DGSRKNPARNCVa2_h(1221-1293) GPPGHLTAALGDIM-GHYDESMPDPLPEFTEDQAA---- DDKNKTD G HAT KS SSQ ET RS DGSKKHPARTCVa1_h(1567-1639) GPPGEVIQP-LPIQASR-TRRNIDASQLLDDG---NGEN VD ADG EE FGS NS KLE EQ KR LGTQQNPARTCXIa1_h(1537-1607) GPPGEVIQP-LPILSSKKTRRHTEGMQADAD------DN LD SDG EE FGS NS KQD EH KF MGTQTNPARTCXIa2_h(1495-1571) GPPGEVIQP-LPIQMPKKTRRSVDGSRLMQEDEAIPTGGA GS GG EE FGS DS REE EQ RR TGTQDSPARTCXXIVa1_h(1471-1545) GPPGAPGPRKQMDINAAIQALIESNTALQMESYQNT---EVT IDHSEE FKT NY SNL HS KN LGTRDNPARICXXVIIa1_h(1616-1859) GPPGGPIQLQQDDLGAAFQTWMDTSGALRPESYSYP---DRL LDQGGE FKT HY SNL QS KT LGTKENPARVC abcdefgabcdefgabcdefgabcdefgabcdefgaGCN4-pII R KQ EDK EE LSK YH ENE AR KKL GER | | | | | 0 7 14 21 28
B conglutinin_b(178-220) ---GLAE NA KQR TI DGH RR QNA SQ KKA LFP-DGQAVGEcollectin43_b(160-205) GETSVLE DT RQR RN EGE QR QNI TQ RKA LFP-DGQAVGESP-D_h(220-262) ---GLPD AS RQQ EA QGQ QH QAA SQ KKVELFP-NGQSVGEMBP_h(98-136) -------GKSPDGDSSL ASERKA QTE AR KKW TFS-LGKQVGNSP-A_h(98-136 --------GLPAHLDEE QAT HD RHQ LQTRGA SLQGSIMTVGECL-L1_h(116-157) --GTVCDCGRYRKF GQ DIS AR KTS KF KNV AGI---RETEE abcdefgabcdefgabcdefgabcdefga
C a1_su(1155-1231) GPPGQVQSSYGVRYPSFQSGG-KGQGSSPYGYAYRDDSKNDA KIQDTE LGA SA GQQ EL KAPQGKAKTNPARSCa2_su(2929-3009) GPPGEVSMAAMPRMPQQQ----QSKGPSQYSHYYRDEIPKTVEQLDRTQ QIY AK ESE LS IEPLG-SRDQPIRSChd1a_ab(1126-1187) GPPG-----YGPVYSPQPSWN-KGP-----DPYQYDEPE------GGMA YEN NR REA VR GHSRLGSRTSPGKNChd2a_ab(1170-1238) GPPGES--VYGRAMTGWATGS-KGPGYMGDVPSAEGEPE------E RN IKA KD EEE KK RDPTG-TKDAPGRTCemf1_sp GPPGPT--GGGIILVPVNDQN-PTRSPVSGSVFYRGQAE---ETDVNLGSVAD IE HKK QH KSPTG-TKDSPARSCfam1a_ar GPPGSS--SYGGDY..(19 aa)..MGDDPKA--TGRVRSKEDLKKDEN FEA VE GDA EA KNPTG-THAAPARTCfap1a_al GPPGMM----QEMN..(19 aa)..YGDDPNAGKTSKRYTKEDLKKDET FEA VE GEA EA KNPTG-TRAAPARTCfcol_rf GPPGNS--DYGAAP..(19 aa)..MGDDPNR-----MDT-KDEKPEXG WAS AQ QA KNPTG-TKDMPARTCfcol_hy(1107-1207) GPPGPAMLPPWSGG..(34 aa)..YQVYRYYSSNKTKT DE TEIENN NNR KI KSS EA KKPNG-SKEFPARTC abcdefgabcdefgabcdefgabcdefg
D ColQ_h(286-353) GPPGRCLCGPTMNVNNPSYGESVYGPSSPRVPVIF VNNQEE ER NTQNAI FRRDQRSLYFKDSLGXVa1_h(1124-1191) GQPGLPGSRNLVTAFSNMDDMLQKAHLVIEGTFIY RDSTEF IR RDG KK QLGELIPIPADSPPPXVIIIa1_h(1195-1263) GPPGTMGASSGVRLWATRQAMLGQVHEVPEGWLIF AEQEEL VR QNG RK QLE RTPLPRGTDNEXXVIa1_m(324-393) GAPGSQGLVDERVVARPSGEPSVKEEEDKASAAEGEG QQ REA KI AER LI EHM GVHDPLASPEG abcdefgabcdefgabcdefga
E transmembrane region
XIIIa1_h(39-123) LPSPGSCG LTL LCSLALSLL HFRTAE QAR LR EAERGEQQMETAILGRVNQLLDE..(22 aa)..GPPXXIIIa1_h(32-123) GSRAVSALCLLLSVGSAAACLL GVQ AA QGR AA EEEREL RRAGPPGALDAWAEPH..(29 aa)..GPPXXVa1_h(30-125) TMPPC VL ALLSVV VVSCLY GYKTND QAR AA ESAKGAPSIHLLPDTLDHLKTMV..(33 aa)..GPPXVIIa1_h(466-569) KWLLG LLTWLL LG LFG IA AEE RK KAR DE ERIRRS LPYGDSMDRIEKDRLQ..(41 aa)..GSPMARCO_h(41-150) GVNFS AV VIY IL TAG GL VVQ LN QAR RV EMY LNDTLAAEDSPSFSLLQSA..(47 aa)..GEQEDA_h(35-182) GEGNSCIL LGF GLSLALHLLTLCC LE RRERGAESR GGSGTPGTSGTLSSLG..(85 aa)..GPP abcdefgabcdefgabcdefgabcdefgabcdefgabcd
F XXVIa1(131-202) CTR SD SER TT EAK LL EAAEQPSGPDNDLPPPQSTPPTWNEDFLPDAIPIAHPGPRRRRPTGPAGPP abcdefgabcdefgabcd
G COL2 NC2 COL1
IXa1I_h(745-798) GLPGVQGPPGR-------APTDQH KQ C R QEH AE AAS KRP-DS-----------GATGLPGRPGPPIXa2_h(508-561) GQPGRQGVEGR-------DATDQH VD A K QEQ AE AVS KRE-AL-----------GAVGMMGPPGPPXVIa1_h(1421-1483) GLPGVPGSMGD---MVNYDE KRF RQEI K DER AY TSR QFP-MEMAAAP------GRPGPPGKDGAPXIXa1_h(998-1066) GPPGSPGIPGIPADAVSFEE KKY NQEV R EER AV LSQ KLP-AAMLAAQA----YGRPGPPGKDGLPIXa3_h(508-562) GITGKPGVPGK-------EASEQR RE CGG SEQ AQ AAH RKPLAP-----------GSIGRPGPAGPPXXIa1_h(776-836) GPPGLDGKPGR-------EFSEQF RQ CTD RAQ PV GSPGIPGPPGPIXIIa1_h(2887-2953) GLKGEKGDRGD---IASQNM RAV RQ CEQ SGQ NR NQM NQIPNDYQSS---RNQPGPPGPPGPPGSAXIVa1_h GAKGERGERGD---LQSQAM RSV RQ CEQ QSH AR TAI NQIPSHSSSI---RTVQGPPGEPGRPGSPXXa1_c(1297-1366) GPKGERGEKGE---PQS AT YQL SQ CER QSH LK DSF HEHARKPVPVWEGRLKPGEPGSPGPPGPP abcdefgabcdefga abcdefgabcdefga
H COL2 NC3 COL3
XIIIa1_h(430-475) GPKGSKGEPGKGE VD NGN NE LQE RT ALMGPPGLPGQIGPPXXVa1_h(415-460) GPPGQKGDQGATK ID NGN HE LQR TT TVTGPPGPPGPQGLQXXIIIa1_h(384-423) GADGLKGEKGESASDS QES AQ IVE------PGPPGPPGPPGPM abcdefgabcdefgabcd
I VIIa1_h(1928-1990) GERGLRGEPGSVPN DRL ET GIK SA REI ET DESSGSFLPVPERRRGPKGDSGEQGPP defgabcdefgabcdefgabcd
J VIIa1_h(1044-1259) QTPVCPRGLADVVFLPHATQDN HR EATRRV ERL LA GPLGPQAVQVGLLSYSHRP..(151 aa)..GQKVIa1_h(662-720) GPD..(69 aa)..MQEHVSLRSPSIRN QE KEA KS QWM GGTFTGEALQYTRDQLLPPSPNVIa2_h(587-719) GLT..(71 aa)..TFEAIQLDDEHIDS SS KEA KN EWI GGTWTPSALKFAYDRLIKESRRVia3_h(2371-2505) GDS..(73 aa)..TTEIRFADSKRKSV LDKIKN QV LTSKQQSLETAMSFVARNTFKRVRNG abcdefgabcdefgabcd