Abstract
Collagen XXIII is a transmembrane collagen previously shown to be upregulated in metastatic prostate cancer that has been used as a tissue and fluid biomarker for non-small cell lung cancer and prostate cancer. To determine whether collagen XXIII facilitates cancer cell metastasis in vivo and to establish a function for collagen XXIII in cancer progression, collagen XXIII knockdown cells were examined for alterations in in vivo metastasis as well as in vitro cell adhesion. In experimental and spontaneous xenograft models of metastasis, H460 cells expressing collagen XXIII shRNA formed fewer lung metastases than control cells. Loss of collagen XXIII in H460 cells also impaired cell adhesion, anchorage-independent growth and cell seeding to the lung, but did not affect cell proliferation. Corroborating a role for collagen XXIII in cell adhesion, overexpression of collagen XXIII in H1299 cells, which do not express endogenous collagen XXIII, enhanced cell adhesion. Consequent reduction in OB-cadherin, alpha-catenin, gamma-catenin, beta-catenin, vimentin and galectin-3 protein expression was also observed in response to loss of collagen XXIII. This study suggests a potential role for collagen XXIII in mediating metastasis by facilitating cell–cell and cell–matrix adhesion as well as anchorage-independent cell growth.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 50 print issues and online access
$259.00 per year
only $5.18 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
Accession codes
References
Banyard J, Bao L, Hofer MD, Zurakowski D, Spivey KA, Feldman AS et al. (2007). Collagen XXIII expression is associated with prostate cancer recurrence and distant metastases. Clin Cancer Res 13: 2634–2642.
Banyard J, Bao L, Zetter BR . (2003). Type XXIII collagen, a new transmembrane collagen identified in metastatic tumor cells. J Biol Chem 278: 20989–20994.
Barczyk M, Carracedo S, Gullberg D . (2010). Integrins. Cell Tissue Res 339: 269–280.
Bussemakers MJ, Van Bokhoven A, Tomita K, Jansen CF, Schalken JA . (2000). Complex cadherin expression in human prostate cancer cells. Int J Cancer 85: 446–450.
Chu K, Cheng CJ, Ye X, Lee YC, Zurita AJ, Chen DT et al. (2008). Cadherin-11 promotes the metastasis of prostate cancer cells to bone. Mol Cancer Res 6: 1259–1267.
Cifone MA, Fidler IJ . (1980). Correlation of patterns of anchorage-independent growth with in vivo behavior of cells from a murine fibrosarcoma. Proc Natl Acad Sci U S A 77: 1039–1043.
Diaz LA, Ratrie H, Saunders WS, Futamura S, Squiquera HL, Anhalt GJ et al. (1990). Isolation of a human epidermal cDNA corresponding to the 180-kD autoantigen recognized by bullous pemphigoid and herpes gestationis sera. Immunolocalization of this protein to the hemidesmosome. J Clin Invest 86: 1088–1094.
Di Benedetto A, Watkins M, Grimston S, Salazar V, Donsante C, Mbalaviele G et al. (2010). N-cadherin and cadherin 11 modulate postnatal bone growth and osteoblast differentiation by distinct mechanisms. J Cell Sci 123: 2640–2648.
Forsell C, Bjork BF, Lilius L, Axelman K, Fabre SF, Fratiglioni L et al. (2010). Genetic association to the amyloid plaque associated protein gene COL25A1 in Alzheimer's disease. Neurobiol Aging 31: 409–415.
Franzke CW, Bruckner P, Bruckner-Tuderman L . (2005). Collagenous transmembrane proteins: recent insights into biology and pathology. J Biol Chem 280: 4005–4008.
Franzke CW, Bruckner-Tuderman L, Blobel CP . (2009). Shedding of collagen XVII/BP180 in skin depends on both ADAM10 and ADAM9. J Biol Chem 284: 23386–23396.
Franzke CW, Tasanen K, Borradori L, Huotari V, Bruckner-Tuderman L . (2004). Shedding of collagen XVII/BP180: structural motifs influence cleavage from cell surface. J Biol Chem 279: 24521–24529.
Franzke CW, Tasanen K, Schacke H, Zhou Z, Tryggvason K, Mauch C et al. (2002). Transmembrane collagen XVII, an epithelial adhesion protein, is shed from the cell surface by ADAMs. Embo J 21: 5026–5035.
Franzke CW, Tasanen K, Schumann H, Bruckner-Tuderman L . (2003). Collagenous transmembrane proteins: collagen XVII as a prototype. Matrix Biol 22: 299–309.
Gilles C, Polette M, Piette J, Delvigne AC, Thompson EW, Foidart JM et al. (1996). Vimentin expression in cervical carcinomas: association with invasive and migratory potential. J Pathol 180: 175–180.
Glinsky VV, Glinsky GV, Glinskii OV, Huxley VH, Turk JR, Mossine VV et al. (2003). Intravascular metastatic cancer cell homotypic aggregation at the sites of primary attachment to the endothelium. Cancer Res 63: 3805–3811.
Gordon MK, Bhatt P, Song R, Hahn RA, Shakarjian M, Gerecke DR et al. (2005). Collagen XXIII facilitates adhesion of corneal epithelial cells to type IV collagen and matrigel. Invest Ophthalmol Vis Sci 46: E-abstract 869.
Hagg P, Vaisanen T, Tuomisto A, Rehn M, Tu H, Huhtala P et al. (2001). Type XIII collagen: a novel cell adhesion component present in a range of cell-matrix adhesions and in the intercalated discs between cardiac muscle cells. Matrix Biol 19: 727–742.
Hashimoto T, Wakabayashi T, Watanabe A, Kowa H, Hosoda R, Nakamura A et al. (2002). CLAC: a novel Alzheimer amyloid plaque component derived from a transmembrane precursor, CLAC-P/collagen type XXV. Embo J 21: 1524–1534.
Hu L, Lau SH, Tzang CH, Wen JM, Wang W, Xie D et al. (2004). Association of vimentin overexpression and hepatocellular carcinoma metastasis. Oncogene 23: 298–302.
Isaacs JT, Isaacs WB, Feitz WF, Scheres J . (1986). Establishment and characterization of seven dunning rat prostatic cancer cell lines and their use in developing methods for predicting metastatic abilities of prostatic cancers. Prostate 9: 261–281.
Joyce JA, Pollard JW . (2009). Microenvironmental regulation of metastasis. Nat Rev Cancer 9: 239–252.
Kakuyama H, Soderberg L, Horigome K, Winblad B, Dahlqvist C, Naslund J et al. (2005). CLAC binds to aggregated Abeta and Abeta fragments, and attenuates fibril elongation. Biochemistry 44: 15602–15609.
Khaldoyanidi SK, Glinsky VV, Sikora L, Glinskii AB, Mossine VV, Quinn TP et al. (2003). MDA-MB-435 human breast carcinoma cell homo- and heterotypic adhesion under flow conditions is mediated in part by Thomsen-Friedenreich antigen-galectin-3 interactions. J Biol Chem 278: 4127–4134.
Kvist AP, Latvanlehto A, Sund M, Eklund L, Vaisanen T, Hagg P et al. (2001). Lack of cytosolic and transmembrane domains of type XIII collagen results in progressive myopathy. Am J Pathol 159: 1581–1592.
Miles FL, Pruitt FL, van Golen KL, Cooper CR . (2008). Stepping out of the flow: capillary extravasation in cancer metastasis. Clin Exp Metastasis 25: 305–324.
Mukhopadhyay R, Theriault RL, Price JE . (1999). Increased levels of alpha6 integrins are associated with the metastatic phenotype of human breast cancer cells. Clin Exp Metastasis 17: 325–332.
Nomura Y, Tashiro H, Hisamatsu K . (1989). In vitro clonogenic growth and metastatic potential of human operable breast cancer. Cancer Res 49: 5288–5293.
Okazaki M, Takeshita S, Kawai S, Kikuno R, Tsujimura A, Kudo A et al. (1994). Molecular cloning and characterization of OB-cadherin, a new member of cadherin family expressed in osteoblasts. J Biol Chem 269: 12092–12098.
Orr FW, Wang HH . (2001). Tumor cell interactions with the microvasculature: a rate-limiting step in metastasis. Surg Oncol Clin N Am 10: 357–381.
Osada Y, Hashimoto T, Nishimura A, Matsuo Y, Wakabayashi T, Iwatsubo T . (2005). CLAC binds to amyloid beta peptides through the positively charged amino acid cluster within the collagenous domain 1 and inhibits formation of amyloid fibrils. J Biol Chem 280: 8596–8605.
Pihlajaniemi T, Tamminen M . (1990). The alpha 1 chain of type XIII collagen consists of three collagenous and four noncollagenous domains, and its primary transcript undergoes complex alternative splicing. J Biol Chem 265: 16922–16928.
Pishvaian MJ, Feltes CM, Thompson P, Bussemakers MJ, Schalken JA, Byers SW . (1999). Cadherin-11 is expressed in invasive breast cancer cell lines. Cancer Res 59: 947–952.
Rasband WS . (2010). ImageJ. US National Institutes of Health, Bethesda, MD, USA, http://imagej.nih.gov/ij/, 1997–2011.
Roman J, Ritzenthaler JD, Roser-Page S, Sun X, Han S . (2010). {alpha}5{beta}1 integrin expression is essential for tumor progression in experimental lung cancer. Am J Respir Cell Mol Biol 43: 684–691.
Schmidmaier R, Baumann P . (2008). ANTI-ADHESION evolves to a promising therapeutic concept in oncology. Curr Med Chem 15: 978–990.
Simonneau L, Kitagawa M, Suzuki S, Thiery JP . (1995). Cadherin 11 expression marks the mesenchymal phenotype: towards new functions for cadherins? Cell Adhes Commun 3: 115–130.
Soderberg L, Dahlqvist C, Kakuyama H, Thyberg J, Ito A, Winblad B et al. (2005). Collagenous Alzheimer amyloid plaque component assembles amyloid fibrils into protease resistant aggregates. FEBS J 272: 2231–2236.
Spivey KA, Banyard J, Solis LM, Wistuba II, Barletta JA, Gandhi L et al. (2010). Collagen XXIII: a potential biomarker for the detection of primary and recurrent non-small cell lung cancer. Cancer Epidemiol Biomarkers Prev 19: 1362–1372.
Takenaka K, Shibuya M, Takeda Y, Hibino S, Gemma A, Ono Y et al. (2000). Altered expression and function of beta1 integrins in a highly metastatic human lung adenocarcinoma cell line. Int J Oncol 17: 1187–1194.
Tomita K, van Bokhoven A, van Leenders GJ, Ruijter ET, Jansen CF, Bussemakers MJ et al. (2000). Cadherin switching in human prostate cancer progression. Cancer Res 60: 3650–3654.
Tong Y, Xu Y, Scearce-Levie K, Ptacek LJ, Fu YH . (2010). COL25A1 triggers and promotes Alzheimer's disease-like pathology in vivo. Neurogenetics 11: 41–52.
Torimura T, Ueno T, Kin M, Ogata R, Inuzuka S, Sugawara H et al. (1999). Integrin alpha6beta1 plays a significant role in the attachment of hepatoma cells to laminin. J Hepatol 31: 734–740.
Tu H, Sasaki T, Snellman A, Gohring W, Pirila P, Timpl R et al. (2002). The type XIII collagen ectodomain is a 150-nm rod and capable of binding to fibronectin, nidogen-2, perlecan, and heparin. J Biol Chem 277: 23092–23099.
Vaisanen MR, Vaisanen T, Pihlajaniemi T . (2004). The shed ectodomain of type XIII collagen affects cell behaviour in a matrix-dependent manner. Biochem J 380: 685–693.
Vaisanen T, Vaisanen MR, Autio-Harmainen H, Pihlajaniemi T . (2005). Type XIII collagen expression is induced during malignant transformation in various epithelial and mesenchymal tumours. J Pathol 207: 324–335.
Veit G, Zimina EP, Franzke CW, Kutsch S, Siebolds U, Gordon MK et al. (2007). Shedding of collagen XXIII is mediated by furin and depends on the plasma membrane microenvironment. J Biol Chem 282: 27424–27435.
Veit G, Zwolanek D, Eckes B, Niland S, Käpylä J, Zweers MC et al. (2011). Collagen XXIII - novel ligand for integrin α2β1 in the epidermis. J Biol Chem 286: 27804–27813.
Wewer UM, Shaw LM, Albrechtsen R, Mercurio AM . (1997). The integrin alpha 6 beta 1 promotes the survival of metastatic human breast carcinoma cells in mice. Am J Pathol 151: 1191–1198.
Whiteside TL . (2008). The tumor microenvironment and its role in promoting tumor growth. Oncogene 27: 5904–5912.
Acknowledgements
We thank Dr Jenny Mu for her assistance with the survival surgery performed in our spontaneous model of metastasis experiment. We also thank Colin Tasi for his assistance with the western blots.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
B Zetter is a consultant and has equity in Predictive Biosciences, which has licensed the rights to collagen XXIII when used as a cancer biomarker. K Spivey, I Chung, J. Banyard, I Adini and H Feldman declare no conflict of interest.
Additional information
Supplementary Information accompanies the paper on the Oncogene website
Supplementary information
Rights and permissions
About this article
Cite this article
Spivey, K., Chung, I., Banyard, J. et al. A role for collagen XXIII in cancer cell adhesion, anchorage-independence and metastasis. Oncogene 31, 2362–2372 (2012). https://doi.org/10.1038/onc.2011.406
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/onc.2011.406
Keywords
This article is cited by
-
Hepatic passaging of NRAS-mutant melanoma influences adhesive properties and metastatic pattern
BMC Cancer (2023)
-
RNA-sequencing of human aortic valves identifies that miR-629-3p and TAGLN miRNA-mRNA pair involving in calcified aortic valve disease
Journal of Physiology and Biochemistry (2022)
-
Collagen biology making inroads into prognosis and treatment of cancer progression and metastasis
Cancer and Metastasis Reviews (2020)
-
The role of collagen in cancer: from bench to bedside
Journal of Translational Medicine (2019)
-
Collagen XXV promotes myoblast fusion during myogenic differentiation and muscle formation
Scientific Reports (2019)