Collagen, type XXIII, alpha 1

COL23A1
Identifiers
AliasesCOL23A1, collagen type XXIII alpha 1 chain
External IDsOMIM: 610043; MGI: 2653243; HomoloGene: 72101; GeneCards: COL23A1; OMA:COL23A1 - orthologs
Orthologs
SpeciesHumanMouse
Entrez
Ensembl
UniProt
RefSeq (mRNA)

NM_173465

NM_153393

RefSeq (protein)

NP_775736

NP_700442

Location (UCSC)Chr 5: 178.24 – 178.59 MbChr 11: 51.18 – 51.47 Mb
PubMed search[3][4]
Wikidata
View/Edit HumanView/Edit Mouse

Collagen α-1 (XXIII) chain is a protein encoded by COL23A1 gene, which is located on chromosome 5q35 in humans, and on chromosome 11B1+2 in mice.[5] The location of this gene was discovered by genomic sequence analysis.

Collagen XXIII is a type II transmembrane protein and the fourth in the subfamily of non-fibrillar transmembranous collagens. This kind of collagens have a single pass hydrophobic transmembrane domain. The molecule of collagen XXIII can be found either in membrane-bond form or in shed form.

Type XXIII collagen is expressed in both adult tissues and developing organs. It can be found in the epidermis and other epithelia such as those in tongue, gut and lung, but also in the brain, the kidney and the cornea. It has been shown that in prostate collagen XXIII expression is associated with tumor progression.

The functions of collagen XXIII are still unknown, although it is believed that they could be similar to other transmembrane proteins, such as collagen XIII.

Discovery

Collagen XXIII was first identified and isolated from rat prostate carcinoma cells by Jacqueline Banyard, Lere Bao and Bruce R. Zetter in 2003.[6] They also identified this protein in human tissue. They concluded that at the nucleotide level, human and rat collagen XXIII alpha 1 show 76% identity. Furthermore, cellular localization of collagen XXIII was determined by immunofluorescence staining, using an antibody that recognizes the carboxyl terminus of the protein. It was demonstrated that the carboxyl terminus of collagen XXIII is present on the cell surface.

Structure

Protein structure

Collagen XXIII

Human collagen α1(XXIII), which is a homotrimer, contains 540 amino acids distributed in:

  • A long amino-terminal non-collagenous domain (NC-1) of 120 amino acids which can be divided in three parts: a short cytoplasmic region, a transmembrane region and a short extracellular region.
  • A 420-amino-acid-long extracellular region organized in three collagenous (COL1, COL2 and COL3) domains which are interrupted by short non-collagenous domains (NC2, NC3 and NC4), as shown in the schematic.

Structural homology

Comparison of collagens XXIII, XIII and XXV

Collagen XXIII belongs to the transmembranous subfamily of collagens. Proteins which are included in this group present an amino-terminal cytoplasmic domain followed by a membrane-spanning hydrophobic domain and at least one extracellular triple-helical collagenous domain alternated with short non-collagenous domains.

Collagens XIII, XVII, and XXV, and related proteins such as class A macrophage scavenger receptors, ectodysplasin A or the MARCO1 receptor, are also part of this group. An alternative name for this type of protein is MACITs (membrane-associated collagens with interrupted triple helices).

Collagen XXIII shows structural homology with collagen XIII and collagen XXV[7] . Apart from having the characteristic structure of transmembranous collagens, all three proteins present a high level of amino acid residue conservation in collagenous and non-collagenous domains.

Collagens α1(XIII), α1(XXIII) and α1(XXV) display three collagenous domains (Col 1, Col 2, and Col 3) and four non-collagenous domains (NC1, which is also a transmembranous domain, NC2, NC3 and NC4).

It has been reported that Col 1 domain of α1(XXIII) shows similarities with regions of both Col 1 and Col 2 domains of collagen types α1(XIII) and α1(XXV), whilst sequences of Col 2 and Col 3 domains of α1(XXIII) are related to the Col 3 domain of types α1(XIII)and α1(XXV).

Short non-collagenous domains also exhibit similarities, especially in the NC1 and NC4 domains. Between 60 and 78% of the amino acid residues of these domains are identical in all three chains. Furthermore, possible recognition sequences for furin (a major physiological protease) cleavage sites have been found in both amino-terminal NC1 domain and carboxyl-terminal NC4 domain of each one of these collagens. The activity of this protease is vital to explain the origin of the two forms that collagen types XIII, XXIII and XXV can adopt.

Shedding

Collagen XXIII shedding in different compartments. Collagen XXIII molecule might be shed at Golgi apparatus or the cellular membrane. The molecule can also keep its full-length form as long as it is protected from the action of the sheddase (furin) by lipid rafts.

A common feature of transmembrane collagens is the presence of two forms of the molecule: a full-length membrane-bound form and an ectodomain shed form. This characteristic can be also applicable to collagen XXIII.

The distribution of both collagen XXIII forms is tissue-specific, since there are organs such as the brain where the shed form is predominant, whereas in the lungs the molecule is generally found as the full-length form.

It has been reported that the cell is able to regulate the amounts of collagen XXIII in the membrane-bound form and in the secreted shed form, influencing the production of one form or the other when it is needed. For that reason, the shedding process of collagen XXIII has been described as a selective proteolysis, carried out principally by furin,[8] although there are other enzymes, like serine and cysteine proteases, which are able to shed the molecule too.

When collagen XXIII is inside the Golgi apparatus, furin proteases act, cleaving the protein and originating the shed form of the molecule, which will be released to the extracellular matrix by means of exocytosis.

There is also the possibility that the full-length form of the molecule reaches the cell surface before furin cleaves it. When this happens, the full molecule of collagen is introduced in the plasmatic membrane and is stabilized by its non-collagenous transmembranous domains, leaving the collagenous domains outside the cell.

Full-length molecules of collagen XXIII are usually found in lipid rafts, which are cholesterol-rich and sphingolipid-rich, tightly-packed microdomains of the cell membrane. Furin proteases are not able to reach collagen XXIII molecules when they are inside lipid rafts, therefore, collagen XXIII molecules can conserve their full-length form.

In case that these molecules lose the lipid raft protection (i.e. when membrane cholesterol levels decrease) furin proteases can act, cleaving the protein right outside the cell, releasing the shed form of collagen XXIII directly to the extracellular matrix.

Interaction with integrin α2β1

Cellular receptors for collagens belong to the family of β1 integrins. Collagen XXIII interacts in an ion-and conformation-dependent manner with integrin α2β1.[9] Integrin α2β1 is a collagen-binding integrin present at the epidermis, therefore this is the location where the interaction takes place. Both proteins co-localize on basal keratinocytes surface.

Clinical significance

Collagen XXIII plays a role as a biomarker for detection and recurrence of NCLSC cells (non-small cell lung carcinoma)[10] and the reappearance of prostate cancer.[11] Some experiments suggest that collagen XXIII influences cellular adhesion and stimulates metastasis development[12] by facilitating cancer cells growth and survival when they are rounded and not able to spread. It has been shown that loss of collagen XXIII may complicate cellular adhesion and reduce lung cancer cell retention.

See also

References

  1. ^ a b c GRCh38: Ensembl release 89: ENSG00000050767Ensembl, May 2017
  2. ^ a b c GRCm38: Ensembl release 89: ENSMUSG00000063564Ensembl, May 2017
  3. ^ "Human PubMed Reference:". National Center for Biotechnology Information, U.S. National Library of Medicine.
  4. ^ "Mouse PubMed Reference:". National Center for Biotechnology Information, U.S. National Library of Medicine.
  5. ^ "Entrez Gene: COL23A1 collagen, type XXIII, alpha 1".
  6. ^ Banyard J, Bao L, Zetter BR (June 2003). "Type XXIII collagen, a new transmembrane collagen identified in metastatic tumor cells". J. Biol. Chem. 278 (23): 20989–94. doi:10.1074/jbc.M210616200. PMID 12644459.
  7. ^ Koch M, Veit G, Stricker S, Bhatt P, Kutsch S, Zhou P, Reinders E, Hahn RA, Song R, Burgeson RE, Gerecke DR, Mundlos S, Gordon MK (May 2006). "Expression of type XXIII collagen mRNA and protein". J. Biol. Chem. 281 (30): 21546–57. doi:10.1074/jbc.M604131200. hdl:11858/00-001M-0000-0010-83E3-6. PMID 16728390.
  8. ^ Veit G, Zimina EP, Franzke CW, Kutsch S, Siebolds U, Gordon MK, Bruckner-Tuderman L, Koch M (September 2007). "Shedding of collagen XXIII is mediated by furin and depends on the plasma membrane microenvironment". J. Biol. Chem. 282 (37): 27424–35. doi:10.1074/jbc.M703425200. PMID 17627939.
  9. ^ Veit G, Zwolanek D, Eckes B, Niland S, Käpylä J, Zweers MC, Ishada-Yamamoto A, Krieg T, Heino J, Eble JA, Koch M (August 2011). "Collagen XXIII, novel ligand for integrin alpha2beta1 in the epidermis". J. Biol. Chem. 286 (31): 27804–13. doi:10.1074/jbc.M111.220046. PMC 3149370. PMID 21652699.
  10. ^ Spivey KA, Banyard J, Solis LM, Wistuba II, Barletta JA, Gandhi L, Feldman HA, Rodig SJ, Chirieac LR, Zetter BR (May 2010). "Collagen XXIII: a potential biomarker for the detection of primary and recurrent non-small cell lung cancer". Cancer Epidemiol. Biomarkers Prev. 19 (5): 1362–72. doi:10.1158/1055-9965.EPI-09-1095. PMC 2880394. PMID 20447926.
  11. ^ Banyard J, Bao L, Hofer MD, Zurakowski D, Spivey KA, Feldman AS, Hutchinson LM, Kuefer R, Rubin MA, Zetter BR (May 2007). "Collagen XXIII expression is associated with prostate cancer recurrence and distant metastases". Clin Cancer Res. 13 (9): 2634–42. doi:10.1158/1078-0432.CCR-06-2163. PMID 17473194.
  12. ^ Spivey KA, Chung I, Banyard J, Adini I, Feldman HA, Zetter BR (May 2012). "A role for collagen XXIII in cancer cell adhesion, anchorage-independence and metastasis". Oncogene. 31 (18): 2362–72. doi:10.1038/onc.2011.406. PMC 3968770. PMID 21963851.

Further reading

  • Brinckmann J (2005). Collagen: Primer in Structure, Processing and Assembly. Vol. 247. Springer. pp. 1–6. doi:10.1007/b103817.
  • Scleroproteins: Advances in Research and Application: 2013 Edition. ScholarlyEditions. 2013. ISBN 978-1-481-68001-1.

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