Collagen XII mediated cellular and extracellular mechanisms regulate establishment of tendon structure and function.
Cell–cell communication
Collagen XII
Collagen fibril assembly
Mechanical properties
Tendon
Tendon extracellular matrix assembly
Journal
Matrix biology : journal of the International Society for Matrix Biology
ISSN: 1569-1802
Titre abrégé: Matrix Biol
Pays: Netherlands
ID NLM: 9432592
Informations de publication
Date de publication:
01 2021
01 2021
Historique:
received:
19
06
2020
revised:
06
10
2020
accepted:
15
10
2020
pubmed:
24
10
2020
medline:
29
10
2021
entrez:
23
10
2020
Statut:
ppublish
Résumé
Tendons have a uniaxially aligned structure with a hierarchical organization of collagen fibrils crucial for tendon function. Collagen XII is expressed in tendons and has been implicated in the regulation of fibrillogenesis. It is a non-fibrillar collagen belonging to the Fibril-Associated Collagens with Interrupted Triple Helices (FACIT) family. Mutations in COL12A1 cause myopathic Ehlers Danlos Syndrome with a clinical phenotype involving both joints and tendons supporting critical role(s) for collagen XII in tendon development and function. Here we demonstrate the molecular function of collagen XII during tendon development using a Col12a1 null mouse model. Col12a1 deficiency altered tenocyte shape, formation of interacting cell processes, and organization resulting in impaired cell-cell communication and disruption of hierarchal structure as well as decreased tissue stiffness. Immuno-localization revealed that collagen XII accumulated on the tenocyte surface and connected adjacent tenocytes by building matrix bridges between the cells, suggesting that collagen XII regulates intercellular communication. In addition, there was a decrease in fibrillar collagen I in collagen XII deficient tenocyte cultures compared with controls suggesting collagen XII signaling specifically alters tenocyte biosynthesis. This suggests that collagen XII provides feedback to tenocytes regulating extracellular collagen I. Together, the data indicate dual roles for collagen XII in determination of tendon structure and function. Through association with fibrils it functions in fibril packing, fiber assembly and stability. In addition, collagen XII influences tenocyte organization required for assembly of higher order structure; intercellular communication necessary to coordinate long range order and feedback on tenocytes influencing collagen synthesis. Integration of both regulatory roles is required for the acquisition of hierarchal structure and mechanical properties.
Identifiants
pubmed: 33096204
pii: S0945-053X(20)30094-9
doi: 10.1016/j.matbio.2020.10.004
pmc: PMC7870578
mid: NIHMS1648519
pii:
doi:
Substances chimiques
COL12A1 protein, human
0
Collagen Type XII
0
Fibrillar Collagens
0
Collagen
9007-34-5
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
52-67Subventions
Organisme : NIAMS NIH HHS
ID : P30 AR050950
Pays : United States
Organisme : NIAMS NIH HHS
ID : R01 AR044745
Pays : United States
Informations de copyright
Copyright © 2020 The Authors. Published by Elsevier B.V. All rights reserved.
Déclaration de conflit d'intérêts
Declaration of Competing Interest The author(s) declare no competing interests.
Références
Hum Mol Genet. 2014 May 1;23(9):2339-52
pubmed: 24334604
Matrix Biol. 2020 Jul;89:59-75
pubmed: 31862401
J Biomech Eng. 2005 Feb;127(1):181-5
pubmed: 15868800
J Anat. 1996 Dec;189 ( Pt 3):593-600
pubmed: 8982835
Cell Struct Funct. 2008;33(2):203-10
pubmed: 18957791
Matrix Biol. 2019 Jan;75-76:1-11
pubmed: 30130584
J Cell Biol. 1991 May;113(4):971-8
pubmed: 2026656
Matrix Biol. 2020 Aug;90:20-39
pubmed: 32112888
Matrix Biol. 2011 Jan;30(1):53-61
pubmed: 20951202
Tissue Barriers. 2020;8(1):1695491
pubmed: 31818195
J Cell Biol. 1984 Dec;99(6):2024-33
pubmed: 6542105
Proc Natl Acad Sci U S A. 2013 Dec 3;110(49):E4743-52
pubmed: 24248360
Matrix Biol. 2020 Jan;85-86:47-67
pubmed: 31655293
J Cell Sci. 1994 Feb;107 ( Pt 2):669-81
pubmed: 8207089
Mol Cell Biol. 2007 Sep;27(17):6218-28
pubmed: 17562872
J Biol Chem. 2006 Dec 15;281(50):38592-8
pubmed: 17020878
Dev Biol. 2002 Jul 15;247(2):351-66
pubmed: 12086472
Nat Rev Mol Cell Biol. 2017 Dec;18(12):728-742
pubmed: 29115301
Exp Cell Res. 1999 Mar 15;247(2):320-8
pubmed: 10066359
Dev Dyn. 1993 Jan;196(1):37-46
pubmed: 8334298
Comp Biochem Physiol A Mol Integr Physiol. 2002 Dec;133(4):1135-57
pubmed: 12485697
Matrix Biol. 2013 Jan;32(1):3-13
pubmed: 23178232
Matrix Biol. 2014 Jan;33:47-53
pubmed: 23954412
J Cell Sci. 2000 Oct;113 ( Pt 20):3583-91
pubmed: 11017874
Trends Biochem Sci. 1991 May;16(5):191-4
pubmed: 1882421
Matrix Biol. 1996 Nov;15(5):341-8
pubmed: 8981330
J Anat. 1998 Aug;193 ( Pt 2):215-22
pubmed: 9827637
Ann Clin Transl Neurol. 2019 Oct;6(10):1980-1988
pubmed: 31509352
J Cell Biol. 1986 Jul;103(1):231-40
pubmed: 3722266
Cell Tissue Res. 1984;238(2):319-27
pubmed: 6509510
J Cell Biol. 2000 Nov 13;151(4):779-88
pubmed: 11076963
Hum Mol Genet. 2014 May 1;23(9):2353-63
pubmed: 24334769
Adv Exp Med Biol. 2014;802:5-29
pubmed: 24443018
Int J Biochem Cell Biol. 2014 Aug;53:51-4
pubmed: 24801612
Genet Med. 2020 Jan;22(1):112-123
pubmed: 31273343
J Mol Biol. 2000 Jan 28;295(4):891-902
pubmed: 10656798
Nat Commun. 2017 Jul 25;8(1):126
pubmed: 28743881
Matrix Biol. 2018 Oct;71-72:205-224
pubmed: 29499355
Connect Tissue Res. 2012;53(1):2-13
pubmed: 21851252
J Biol Chem. 2012 Jun 29;287(27):22549-59
pubmed: 22573329
J R Soc Interface. 2012 Nov 7;9(76):3108-17
pubmed: 22764132
FEBS J. 2013 May;280(10):2120-37
pubmed: 23331954
Matrix Biol. 2020 Dec;94:57-76
pubmed: 32890632
Matrix Biol. 2018 Oct;71-72:1-9
pubmed: 29625183
Cell Tissue Res. 2016 Jun;364(3):677-679
pubmed: 26965696
J Cell Biol. 1995 Aug;130(4):1005-14
pubmed: 7642694
J Cell Sci. 2005 Apr 1;118(Pt 7):1341-53
pubmed: 15788652
J Musculoskelet Neuronal Interact. 2005 Mar;5(1):5-21
pubmed: 15788867
J Cell Biol. 2011 Jun 13;193(6):1115-30
pubmed: 21670218
J Dent Res. 1995 Jan;74(1):313-8
pubmed: 7876423
Birth Defects Res C Embryo Today. 2008 Sep;84(3):228-44
pubmed: 18773462
Dev Dyn. 1995 Dec;204(4):432-45
pubmed: 8601036
Matrix Biol. 2004 Jan;22(7):595-601
pubmed: 15065570
Eur J Cell Biol. 2006 Nov;85(11):1145-54
pubmed: 16859807
Development. 1989 Nov;107(3):437-43
pubmed: 2612371
Cells. 2020 Feb 11;9(2):
pubmed: 32053901
J Anat. 2003 May;202(5):411-20
pubmed: 12739618
Muscle Nerve. 2017 Feb;55(2):277-281
pubmed: 27348394
J Biol Chem. 2009 Mar 27;284(13):8427-38
pubmed: 19136672
J Anat. 1994 Jun;184 ( Pt 3):457-63
pubmed: 7928635
Am J Med Genet C Semin Med Genet. 2017 Mar;175(1):8-26
pubmed: 28306229
J Cell Biochem. 2006 Aug 15;98(6):1436-49
pubmed: 16518859
Data Brief. 2017 Nov 04;16:65-70
pubmed: 29204466
Matrix Biol. 2020 Dec;94:77-94
pubmed: 32950601
Am J Pathol. 2015 May;185(5):1436-47
pubmed: 25797646
J Orthop Res. 2006 Nov;24(11):2124-32
pubmed: 16944473
Eur J Biochem. 1998 Oct 15;257(2):362-71
pubmed: 9826181
J Cell Biol. 2004 May 24;165(4):553-63
pubmed: 15159420
Nat Commun. 2020 Jun 15;11(1):3025
pubmed: 32541821