Intracellular mechanisms of molecular recognition and sorting for transport of large extracellular matrix molecules.
Extracellular matrix (ECM) proteins are biosynthesized in the rough endoplasmic reticulum (rER) and transported via the Golgi apparatus to the extracellular space. The coat protein complex II (COPII) transport vesicles are approximately 60-90 nm in diameter. However, several ECM molecules are much larger, up to several hundreds of nanometers. Therefore, special COPII vesicles are required to coat and transport these molecules. Transmembrane Protein Transport and Golgi Organization 1 (TANGO1) facilitates loading of collagens into special vesicles. The Src homology 3 (SH3) domain of TANGO1 was proposed to recognize collagen molecules, but how the SH3 domain recognizes various types of collagen is not understood. Moreover, how are large noncollagenous ECM molecules transported from the rER to the Golgi? Here we identify heat shock protein (Hsp) 47 as a guide molecule directing collagens to special vesicles by interacting with the SH3 domain of TANGO1. We also consider whether the collagen secretory model applies to other large ECM molecules.
Research Department, Shriners Hospital for Children, Portland, OR 97239; Department of Biochemistry and Molecular Biology, Oregon Health & Science University, Portland, OR 97239.
Yoshihiro
Y
Ishikawa
Department of Molecular Biosciences, Faculty of Life Sciences, Kyoto Sangyo University, Kyoto 603-8555, Japan.
Shinya
S
Ito
Department of Molecular Biosciences, Faculty of Life Sciences, Kyoto Sangyo University, Kyoto 603-8555, Japan.
Kazuhiro
K
Nagata
Research Department, Shriners Hospital for Children, Portland, OR 97239; Department of Biochemistry and Molecular Biology, Oregon Health & Science University, Portland, OR 97239.
Lynn Y
LY
Sakai
Research Department, Shriners Hospital for Children, Portland, OR 97239; Department of Biochemistry and Molecular Biology, Oregon Health & Science University, Portland, OR 97239; hpb@shcc.org.
Hans Peter
HP
Bächinger
D051784:Aryl Hydrocarbon Receptor Nuclear Translocator / Q000737:chemistry / Q000378:metabolism; D022181:COP-Coated Vesicles; D003094:Collagen / Q000378:metabolism; D004721:Endoplasmic Reticulum / Q000378:metabolism; D005109:Extracellular Matrix; D016326:Extracellular Matrix Proteins / Q000378:metabolism*; D000071838:Fibrillin-1 / Q000378:metabolism; D015870:Gene Expression; D006056:Golgi Apparatus / Q000378:metabolism; D050958:HSP47 Heat-Shock Proteins / Q000378:metabolism; D006801:Humans; D042541:Intracellular Space / Q000378:metabolism; D011485:Protein Binding; D054730:Protein Interaction Domains and Motifs; D021381:Protein Transport; D011994:Recombinant Proteins; D018909:src Homology Domains / Q000235:genetics
C497396:ARNT protein, human; D016326:Extracellular Matrix Proteins; D000071838:Fibrillin-1; D050958:HSP47 Heat-Shock Proteins; D011994:Recombinant Proteins; D051784:Aryl Hydrocarbon Receptor Nuclear Translocator; D003094:Collagen
COPII vesicles; Hsp47; TANGO1; collagen; secretion
J Biol Chem. 2001 Jul 6;276(27):25399-403
11333272
PLoS One. 2007 Oct 10;2(10):e1029
17925877
J Biol Chem. 1994 Dec 9;269(49):31224-8
7983065
Biochim Biophys Acta. 2013 Nov;1833(11):2430-7
23583305
Cell. 1998 Dec 23;95(7):993-1003
9875853
EMBO J. 2003 Jun 2;22(11):2571-82
12773374
J Biol Chem. 2014 Jun 27;289(26):18189-201
24821723
Mol Biol Cell. 2011 Jul 1;22(13):2301-8
21525241
Annu Rev Cell Dev Biol. 2015;31:109-24
26422332
FEBS Lett. 2012 Aug 14;586(17):2609-14
22710157
Nature. 1991 Jul 25;352(6333):334-7
1852207
Int J Biochem Cell Biol. 2014 Feb;47:57-67
24333299
Cold Spring Harb Perspect Biol. 2011 Jan 01;3(1):a004978
21421911
Methods Enzymol. 2011;499:167-82
21683254
J Biol Chem. 2001 Feb 23;276(8):6046-55
11087755
Curr Opin Cell Biol. 2013 Aug;25(4):420-7
23702145
J Cell Biol. 2011 May 30;193(5):935-51
21606205
Biochim Biophys Acta. 2013 Nov;1833(11):2542-59
23770047
Am J Hum Genet. 2010 Mar 12;86(3):389-98
20188343
PLoS Genet. 2009 Jul;5(7):e1000579
19629171
J Cell Biol. 2000 Sep 18;150(6):1499-506
10995453
J Biol Chem. 1997 Mar 14;272(11):7368-73
9054436
J Biol Chem. 2015 Jul 17;290(29):17679-89
26004778
J Biol Chem. 2010 May 28;285(22):17253-62
20363744
J Biol Chem. 2006 Apr 21;281(16):11177-85
16484215
J Cell Biol. 1986 Dec;103(6 Pt 1):2499-509
3536967
J Cell Biol. 1986 Jul;103(1):223-9
3722264
J Mol Biol. 1996 Apr 26;258(1):104-16
8613981
Elife. 2015 Nov 14;4:null
26568311
Cell. 2006 Oct 20;127(2):291-304
17055431
Biochem J. 2000 Dec 15;352 Pt 3:907-11
11104702
Mol Biol Cell. 2006 May;17(5):2346-55
16525016
Cell Mol Life Sci. 2015 Oct;72(19):3709-20
26082182
Cell. 2009 Mar 6;136(5):891-902
19269366
J Biol Chem. 1987 Aug 15;262(23):11345-50
3112157
J Biol Chem. 2008 Nov 14;283(46):31584-90
18786928
Genomics. 1993 Aug;17 (2):476-84
7691719
Proc Natl Acad Sci U S A. 2012 Aug 14;109(33):13243-7
22847422
Nat Rev Genet. 2009 Mar;10(3):173-83
19204719
J Biol Chem. 1998 Oct 9;273(41):26692-7
9756911
J Biol Chem. 1991 Aug 5;266(22):14763-70
1860873
Matrix Biol. 2001 Nov;20(7):439-50
11691584
Biochim Biophys Acta. 2013 Nov;1833(11):2464-72
23419775
Hum Mol Genet. 2014 Sep 15;23(18):4822-31
24777781
Biochem Biophys Res Commun. 2016 Jan 15;469(3):437-42
26692483
J Biol Chem. 1997 Jan 10;272(2):1231-6
8995426
Nature. 2012 Feb 22;482(7386):495-500
22358839
Elife. 2014 May 19;3:e02784
24842878
J Biol Chem. 2006 Feb 10;281(6):3432-8
16326708
Science. 2012 Sep 28;337(6102):1668-72
23019651
Curr Opin Pediatr. 2014 Aug;26(4):500-7
25007323
J Cell Sci. 1999 Nov;112 ( Pt 22):4163-71
10547375
Biochim Biophys Acta. 2013 Nov;1833(11):2479-91
23602968
J Biol Chem. 1997 Dec 5;272(49):30993-7
9388247
J Biol Chem. 1989 May 25;264(15):8956-62
2656691