Identification of Unique α4 Chain Structure and Conserved Antiangiogenic Activity of α3NC1 Type IV Collagen in Zebrafish

Overview

Journal Dev Dyn

Publisher Wiley

Specialty Anatomy & Histology

Date 2023 Apr 1

PMID 37002899

Authors

Valerie S LeBleu

Jianli Dai

Susan Tsutakawa

Brian A MacDonald

Joseph L Alge

Malin Sund

Liang Xie

Hikaru Sugimoto

John Tainer

Leonard I Zon

Raghu Kalluri

Affiliations

Soon will be listed here.

Abstract

Background: Type IV collagen is an abundant component of basement membranes in all multicellular species and is essential for the extracellular scaffold supporting tissue architecture and function. Lower organisms typically have two type IV collagen genes, encoding α1 and α2 chains, in contrast with the six genes in humans, encoding α1-α6 chains. The α chains assemble into trimeric protomers, the building blocks of the type IV collagen network. The detailed evolutionary conservation of type IV collagen network remains to be studied.

Results: We report on the molecular evolution of type IV collagen genes. The zebrafish α4 non-collagenous (NC1) domain, in contrast with its human ortholog, contains an additional cysteine residue and lacks the M93 and K211 residues involved in sulfilimine bond formation between adjacent protomers. This may alter α4 chain interactions with other α chains, as supported by temporal and anatomic expression patterns of collagen IV chains during the zebrafish development. Despite the divergence between zebrafish and human α3 NC1 domain (endogenous angiogenesis inhibitor, Tumstatin), the zebrafish α3 NC1 domain exhibits conserved antiangiogenic activity in human endothelial cells.

Conclusions: Our work supports type IV collagen is largely conserved between zebrafish and humans, with a possible difference involving the α4 chain.

References

Brodsky B, Ramshaw J . The collagen triple-helix structure. Matrix Biol. 1997; 15(8-9):545-54. DOI: 10.1016/s0945-053x(97)90030-5. View

LeBleu V, Sund M, Sugimoto H, Birrane G, Kanasaki K, Finan E . Identification of the NC1 domain of {alpha}3 chain as critical for {alpha}3{alpha}4{alpha}5 type IV collagen network assembly. J Biol Chem. 2010; 285(53):41874-85. PMC: 3009915. DOI: 10.1074/jbc.M110.149534. View

Kelley P, Sado Y, Duncan M . Collagen IV in the developing lens capsule. Matrix Biol. 2002; 21(5):415-23. DOI: 10.1016/s0945-053x(02)00014-8. View

Zehnder A, Adams J, Santi P, Kristiansen A, Wacharasindhu C, Mann S . Distribution of type IV collagen in the cochlea in Alport syndrome. Arch Otolaryngol Head Neck Surg. 2005; 131(11):1007-13. DOI: 10.1001/archotol.131.11.1007. View

Eikesdal H, Sugimoto H, Birrane G, Maeshima Y, Cooke V, Kieran M . Identification of amino acids essential for the antiangiogenic activity of tumstatin and its use in combination antitumor activity. Proc Natl Acad Sci U S A. 2008; 105(39):15040-5. PMC: 2567489. DOI: 10.1073/pnas.0807055105. View

Marneros A, Olsen B . The role of collagen-derived proteolytic fragments in angiogenesis. Matrix Biol. 2001; 20(5-6):337-45. DOI: 10.1016/s0945-053x(01)00151-2. View

Vanacore R, Ham A, Voehler M, Sanders C, Conrads T, Veenstra T . A sulfilimine bond identified in collagen IV. Science. 2009; 325(5945):1230-4. PMC: 2876822. DOI: 10.1126/science.1176811. View

Kelemen-Valkony I, Kiss M, Csiha J, Kiss A, Bircher U, Szidonya J . Drosophila basement membrane collagen col4a1 mutations cause severe myopathy. Matrix Biol. 2011; 31(1):29-37. DOI: 10.1016/j.matbio.2011.09.004. View

Driever W, Stemple D, Schier A . Zebrafish: genetic tools for studying vertebrate development. Trends Genet. 1994; 10(5):152-9. DOI: 10.1016/0168-9525(94)90091-4. View

10.

Kalluri R, Gattone 2nd V, Hudson B . Identification and localization of type IV collagen chains in the inner ear cochlea. Connect Tissue Res. 1998; 37(1-2):143-50. DOI: 10.3109/03008209809028906. View

11.

Mariyama M, Leinonen A, Mochizuki T, Tryggvason K, Reeders S . Complete primary structure of the human alpha 3(IV) collagen chain. Coexpression of the alpha 3(IV) and alpha 4(IV) collagen chains in human tissues. J Biol Chem. 1994; 269(37):23013-7. View

12.

Sessions A, Kaushik G, Parker S, Raedschelders K, Bodmer R, Van Eyk J . Extracellular matrix downregulation in the Drosophila heart preserves contractile function and improves lifespan. Matrix Biol. 2016; 62:15-27. PMC: 5405015. DOI: 10.1016/j.matbio.2016.10.008. View

13.

Urabe N, Naito I, Saito K, Yonezawa T, Sado Y, Yoshioka H . Basement membrane type IV collagen molecules in the choroid plexus, pia mater and capillaries in the mouse brain. Arch Histol Cytol. 2002; 65(2):133-43. DOI: 10.1679/aohc.65.133. View

14.

Thisse C, Thisse B, Schilling T, Postlethwait J . Structure of the zebrafish snail1 gene and its expression in wild-type, spadetail and no tail mutant embryos. Development. 1993; 119(4):1203-15. DOI: 10.1242/dev.119.4.1203. View

15.

Ero-Tolliver I, Hudson B, Bhave G . The Ancient Immunoglobulin Domains of Peroxidasin Are Required to Form Sulfilimine Cross-links in Collagen IV. J Biol Chem. 2015; 290(35):21741-8. PMC: 4571896. DOI: 10.1074/jbc.M115.673996. View

16.

Hudson B, Tryggvason K, Sundaramoorthy M, Neilson E . Alport's syndrome, Goodpasture's syndrome, and type IV collagen. N Engl J Med. 2003; 348(25):2543-56. DOI: 10.1056/NEJMra022296. View

17.

Fidler A, Darris C, Chetyrkin S, Pedchenko V, Boudko S, Brown K . Collagen IV and basement membrane at the evolutionary dawn of metazoan tissues. Elife. 2017; 6. PMC: 5395295. DOI: 10.7554/eLife.24176. View

18.

Than M, Henrich S, Huber R, Ries A, Mann K, Kuhn K . The 1.9-A crystal structure of the noncollagenous (NC1) domain of human placenta collagen IV shows stabilization via a novel type of covalent Met-Lys cross-link. Proc Natl Acad Sci U S A. 2002; 99(10):6607-12. PMC: 124450. DOI: 10.1073/pnas.062183499. View

19.

Khoshnoodi J, Sigmundsson K, Cartailler J, Bondar O, Sundaramoorthy M, Hudson B . Mechanism of chain selection in the assembly of collagen IV: a prominent role for the alpha2 chain. J Biol Chem. 2005; 281(9):6058-69. DOI: 10.1074/jbc.M506555200. View

20.

Pedchenko V, Bondar O, Fogo A, Vanacore R, Voziyan P, Kitching A . Molecular architecture of the Goodpasture autoantigen in anti-GBM nephritis. N Engl J Med. 2010; 363(4):343-54. PMC: 4144421. DOI: 10.1056/NEJMoa0910500. View