Home LiteratureArticle Details
PMID: 25761876 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Review

COL11A1/(pro)collagen 11A1 expression is a remarkable biomarker of human invasive carcinoma-associated stromal cells and carcinoma progression.

Tumour biology : the journal of the International Society for Oncodevelopmental Biology and Medicine ·Vol. 36 ·No. 4 ·2015-04-00 ·Pages 2213-22

Vázquez-Villa F, García-Ocaña M, Galván JA, García-Martínez J, García-Pravia C, Menéndez-Rodríguez P, González-del Rey C, Barneo-Serra L, de Los Toyos JR

Abstract

The COL11A1 human gene codes for the α1 chain of procollagen 11A1 and mature collagen 11A1, an extracellular minor fibrillar collagen. Under regular conditions, this gene and its derived products are mainly expressed by chondrocytes and mesenchymal stem cells as well as osteoblasts. Normal epithelial cells and quiescent fibroblasts from diverse locations do not express them. Mesenchyme-derived tumors and related conditions, such as scleroderma and keloids, are positive for COL11A1/(pro)collagen 11A1 expression, as well as high-grade human gliomas/glioblastomas. This expression is almost absent in benign pathological processes such as breast hyperplasia, sclerosing adenosis, idiopathic pulmonary fibrosis, cirrhosis, pancreatitis, diverticulitis, and inflammatory bowel disease. By contrast, COL11A1/(pro)collagen 11A1 is highly expressed by activated stromal cells of the desmoplastic reaction of different human invasive carcinomas, and this expression is correlated with carcinoma aggressiveness and progression, and lymph node metastasis. COL11A1 upregulation has been shown to be associated to TGF-β1, Wnt, and Hh signaling pathways, which are especially active in cancer-associated stromal cells. At the front of invasive carcinomas, neoplastic epithelial cells, putatively undergoing epithelial-to-mesenchymal transition, and carcinoma-derived cells with highly metastatic capabilities, can express COL11A1. Thus, in established metastases, the expression of COL11A1/(pro)collagen 11A1 could rely on both the metastatic epithelial cells and/or the accompanying activated stromal cells. COL11A1/(pro)collagen 11A1 expression is a remarkable biomarker of human carcinoma-associated stromal cells and carcinoma progression.

MeSH Terms
Carcinogenesis Carcinoma/genetics,pathology Collagen Type XI/biosynthesis,genetics Gene Expression Regulation, Neoplastic Humans Neoplasm Invasiveness/genetics Neoplasms/genetics,pathology Transforming Growth Factor beta1/genetics
Chemicals
COL11A1 protein, human Collagen Type XI Transforming Growth Factor beta1
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Vázquez-Villa Fernando
Surgery Department, School of Medicine and Health Sciences, University of Oviedo, 33006, Oviedo, Spain.
García-Ocaña Marcos
Galván José A
García-Martínez Jorge
García-Pravia Carmen
Menéndez-Rodríguez Primitiva
González-del Rey Carmen
Barneo-Serra Luis
de Los Toyos Juan R
References (86)
86 references, click to expand
  1. The morphological and molecular features of the epithelial-to-mesenchymal transition.
    Nat Protoc. 2009;4(11):1591-613 PMID: 19834475
  2. Secreted phosphoprotein 1 upstream invasive network construction and analysis of lung adenocarcinoma compared with human normal adjacent tissues by integrative biocomputation.
    Cell Biochem Biophys. 2010 Apr;56(2-3):59-71 PMID: 19949890
  3. Sonic hedgehog promotes desmoplasia in pancreatic cancer.
    Clin Cancer Res. 2008 Oct 1;14(19):5995-6004 PMID: 18829478
  4. Identification of prognostic molecular features in the reactive stroma of human breast and prostate cancer.
    PLoS One. 2011;6(5):e18640 PMID: 21611158
  5. ECM-related gene expression profile in vascular smooth muscle cells from human saphenous vein and internal thoracic artery.
    J Cardiothorac Surg. 2013 Jun 18;8:155 PMID: 23773607
  6. Carcinoma-associated fibroblasts: non-neoplastic tumour-promoting mesenchymal cells.
    J Cell Physiol. 2013 Aug;228(8):1651-7 PMID: 23460038
  7. Overexpression of proCOL11A1 as a stromal marker of breast cancer.
    Histol Histopathol. 2015 Jan;30(1):87-93 PMID: 25005174
  8. The transcription factor CCAAT-binding factor CBF/NF-Y regulates the proximal promoter activity in the human alpha 1(XI) collagen gene (COL11A1).
    J Biol Chem. 2003 Aug 29;278(35):32763-70 PMID: 12805369
  9. Activation of Wnt signalling in stroma from pancreatic cancer identified by gene expression profiling.
    J Cell Mol Med. 2008 Dec;12(6B):2823-35 PMID: 18298655
  10. Quantitation of fibroblast activation protein (FAP)-specific protease activity in mouse, baboon and human fluids and organs.
    FEBS Open Bio. 2013 Dec 08;4:43-54 PMID: 24371721
  11. Gene expression profiling of the tumor microenvironment during breast cancer progression.
    Breast Cancer Res. 2009;11(1):R7 PMID: 19187537
  12. Systematic enrichment analysis of gene expression profiling studies identifies consensus pathways implicated in colorectal cancer development.
    J Carcinog. 2011 Mar 24;10:7 PMID: 21483658
  13. Cadherin-11 increases migration and invasion of prostate cancer cells and enhances their interaction with osteoblasts.
    Cancer Res. 2010 Jun 1;70(11):4580-9 PMID: 20484040
  14. Tissue-specific gene expression of head and neck squamous cell carcinoma in vivo by complementary DNA microarray analysis.
    Arch Otolaryngol Head Neck Surg. 2003 Jul;129(7):760-70 PMID: 12874079
  15. Collagen 11a1 is indirectly activated by lymphocyte enhancer-binding factor 1 (Lef1) and negatively regulates osteoblast maturation.
    Matrix Biol. 2008 May;27(4):330-8 PMID: 18280717
  16. Mesenchymal Stem Cells and the Origin of Ewing's Sarcoma.
    Sarcoma. 2011;2011:null PMID: 20953407
  17. Targeting platelet-derived growth factor as a therapeutic approach in pulmonary fibrosis.
    J Med Invest. 2013;60(3-4):175-83 PMID: 24190033
  18. A robust topology-based algorithm for gene expression profiling.
    ISRN Bioinform. 2012 Nov 11;2012:381023 PMID: 25969748
  19. Differentially expressed genes regulating the progression of ductal carcinoma in situ to invasive breast cancer.
    Cancer Res. 2012 Sep 1;72(17):4574-86 PMID: 22751464
  20. The basics of epithelial-mesenchymal transition.
    J Clin Invest. 2009 Jun;119(6):1420-8 PMID: 19487818
  21. Canonical Wnt signaling is antagonized by noncanonical Wnt5a in hepatocellular carcinoma cells.
    Mol Cancer. 2009 Oct 22;8:90 PMID: 19849855
  22. An ex vivo model employing keloid-derived cell-seeded collagen sponges for therapy development.
    J Invest Dermatol. 2013 Feb;133(2):386-93 PMID: 22951719
  23. Procollagen trafficking, processing and fibrillogenesis.
    J Cell Sci. 2005 Apr 1;118(Pt 7):1341-53 PMID: 15788652
  24. Transcriptional evidence for the "Reverse Warburg Effect" in human breast cancer tumor stroma and metastasis: similarities with oxidative stress, inflammation, Alzheimer's disease, and "Neuron-Glia Metabolic Coupling".
    Aging (Albany NY). 2010 Apr;2(4):185-99 PMID: 20442453
  25. Carcinoma-associated fibroblast-like differentiation of human mesenchymal stem cells.
    Cancer Res. 2008 Jun 1;68(11):4331-9 PMID: 18519693
  26. Combined gene expression analysis of whole-tissue and microdissected pancreatic ductal adenocarcinoma identifies genes specifically overexpressed in tumor epithelia.
    Hepatogastroenterology. 2008 Nov-Dec;55(88):2016-27 PMID: 19260470
  27. The role of tenascin-C in tissue injury and tumorigenesis.
    J Cell Commun Signal. 2009 Dec;3(3-4):287-310 PMID: 19838819
  28. A gene expression signature that defines breast cancer metastases.
    Clin Exp Metastasis. 2009;26(3):205-13 PMID: 19112599
  29. Gene profiling of scleroderma skin reveals robust signatures of disease that are imperfectly reflected in the transcript profiles of explanted fibroblasts.
    Arthritis Rheum. 2006 Jun;54(6):1961-73 PMID: 16736506
  30. Global expression analysis of the fibroblast transcriptional response to TGFbeta.
    Clin Exp Rheumatol. 2004 Jan-Feb;22(3 Suppl 33):S47-57 PMID: 15344598
  31. Cadherin-11 promotes the metastasis of prostate cancer cells to bone.
    Mol Cancer Res. 2008 Aug;6(8):1259-67 PMID: 18708358
  32. Colorectal carcinogenesis is associated with stromal expression of COL11A1 and COL5A2.
    Carcinogenesis. 2001 Jun;22(6):875-8 PMID: 11375892
  33. Gene expression analysis of early and advanced gastric cancers.
    Oncogene. 2007 Jun 21;26(29):4284-94 PMID: 17297478
  34. Great potential of a panel of multiple hMTH1, SPD, ITGA11 and COL11A1 markers for diagnosis of patients with non-small cell lung cancer.
    Oncol Rep. 2006 Nov;16(5):981-8 PMID: 17016581
  35. Tumor vascular proteins as biomarkers in ovarian cancer.
    J Clin Oncol. 2007 Mar 1;25(7):852-61 PMID: 17327606
  36. Role of pancreatic stellate cells in pancreatic cancer metastasis.
    Am J Pathol. 2010 Nov;177(5):2585-96 PMID: 20934972
  37. Analysis of differentially expressed genes in keloids and normal skin with cDNA microarray.
    J Surg Res. 2003 Aug;113(2):208-16 PMID: 12957131
  38. ASPN and GJB2 Are Implicated in the Mechanisms of Invasion of Ductal Breast Carcinomas.
    J Cancer. 2012;3:175-83 PMID: 22514560
  39. Human cancer cells express Slug-based epithelial-mesenchymal transition gene expression signature obtained in vivo.
    BMC Cancer. 2011 Dec 30;11:529 PMID: 22208948
  40. Progression-specific genes identified by expression profiling of matched ductal carcinomas in situ and invasive breast tumors, combining laser capture microdissection and oligonucleotide microarray analysis.
    Cancer Res. 2006 May 15;66(10):5278-86 PMID: 16707453
  41. Multi-cancer computational analysis reveals invasion-associated variant of desmoplastic reaction involving INHBA, THBS2 and COL11A1.
    BMC Med Genomics. 2010 Nov 03;3:51 PMID: 21047417
  42. Systematic assessment of the human osteoblast transcriptome in resting and induced primary cells.
    Physiol Genomics. 2008 May 13;33(3):301-11 PMID: 18334548
  43. Overexpression of COL11A1 by cancer-associated fibroblasts: clinical relevance of a stromal marker in pancreatic cancer.
    PLoS One. 2013 Oct 23;8(10):e78327 PMID: 24194920
  44. Cardiac fibroblasts, fibrosis and extracellular matrix remodeling in heart disease.
    Fibrogenesis Tissue Repair. 2012 Sep 03;5(1):15 PMID: 22943504
  45. Hedgehog signaling is restricted to the stromal compartment during pancreatic carcinogenesis.
    Proc Natl Acad Sci U S A. 2009 Mar 17;106(11):4254-9 PMID: 19246386
  46. COL11A1 in FAP polyps and in sporadic colorectal tumors.
    BMC Cancer. 2001;1:17 PMID: 11707154
  47. Differential gene expression in glioblastoma defined by ADC histogram analysis: relationship to extracellular matrix molecules and survival.
    AJNR Am J Neuroradiol. 2012 Jun;33(6):1059-64 PMID: 22268080
  48. Autocrine TGF-beta and stromal cell-derived factor-1 (SDF-1) signaling drives the evolution of tumor-promoting mammary stromal myofibroblasts.
    Proc Natl Acad Sci U S A. 2010 Nov 16;107(46):20009-14 PMID: 21041659
  49. Regulation of gene expression in inflammatory bowel disease and correlation with IBD drugs: screening by DNA microarrays.
    Inflamm Bowel Dis. 2004 Jan;10(1):1-14 PMID: 15058520
  50. Development of myofibroblasts from human bone marrow mesenchymal stem cells cocultured with human colon carcinoma cells and TGF beta 1.
    In Vitro Cell Dev Biol Anim. 2000 Feb;36(2):77-80 PMID: 10718362
  51. Gene expression profiling of tumour epithelial and stromal compartments during breast cancer progression.
    Breast Cancer Res Treat. 2012 Aug;135(1):153-65 PMID: 22718308
  52. Collagen type XI α1 facilitates head and neck squamous cell cancer growth and invasion.
    Br J Cancer. 2013 Dec 10;109(12):3049-56 PMID: 24231953
  53. Intestinal myofibroblasts: targets for stem cell therapy.
    Am J Physiol Gastrointest Liver Physiol. 2011 May;300(5):G684-96 PMID: 21252048
  54. Differentially expressed genes between primary cancer and paired lymph node metastases predict clinical outcome of node-positive breast cancer patients.
    Breast Cancer Res Treat. 2007 Jul;103(3):319-29 PMID: 17123152
  55. Carcinoma-associated fibroblasts are a promising therapeutic target.
    Cancers (Basel). 2013 Jan 31;5(1):149-69 PMID: 24216702
  56. Lymph node stromal cells enhance drug-resistant colon cancer cell tumor formation through SDF-1α/CXCR4 paracrine signaling.
    Neoplasia. 2011 Sep;13(9):874-86 PMID: 21969820
  57. Prognostic gene-expression signature of carcinoma-associated fibroblasts in non-small cell lung cancer.
    Proc Natl Acad Sci U S A. 2011 Apr 26;108(17):7160-5 PMID: 21474781
  58. Gene expression profiling of human lymph node metastases and matched primary breast carcinomas: clinical implications.
    Mol Oncol. 2007 Sep;1(2):172-80 PMID: 19383293
  59. Circulating tumor cells from patients with advanced prostate and breast cancer display both epithelial and mesenchymal markers.
    Mol Cancer Res. 2011 Aug;9(8):997-1007 PMID: 21665936
  60. Molecular profiling and the identification of genes associated with metastatic oral cavity/pharynx squamous cell carcinoma.
    Arch Otolaryngol Head Neck Surg. 2004 Mar;130(3):295-302 PMID: 15023835
  61. Characterization of a novel mouse monoclonal antibody, clone 1E8.33, highly specific for human procollagen 11A1, a tumor-associated stromal component.
    Int J Oncol. 2012 May;40(5):1447-54 PMID: 22322826
  62. Hedgehog signaling and osteoblast gene expression are regulated by purmorphamine in human mesenchymal stem cells.
    J Cell Biochem. 2012 Jan;113(1):204-8 PMID: 21898541
  63. Roles of epithelial cell-derived periostin in TGF-beta activation, collagen production, and collagen gel elasticity in asthma.
    Proc Natl Acad Sci U S A. 2010 Aug 10;107(32):14170-5 PMID: 20660732
  64. Biomarkers for epithelial-mesenchymal transitions.
    J Clin Invest. 2009 Jun;119(6):1429-37 PMID: 19487819
  65. Microarray-based transcriptional and epigenetic profiling of matrix metalloproteinases, collagens, and related genes in cancer.
    J Biol Chem. 2010 Jun 18;285(25):19647-59 PMID: 20404328
  66. Organ-, inflammation- and cancer specific transcriptional fingerprints of pancreatic and hepatic stellate cells.
    Mol Cancer. 2010 Apr 23;9:88 PMID: 20416094
  67. Difference of gene expression profiles between esophageal carcinoma and its pericancerous epithelium by gene chip.
    World J Gastroenterol. 2003 Mar;9(3):417-22 PMID: 12632488
  68. Common denominator genes that distinguish colorectal carcinoma from normal mucosa.
    Int J Colorectal Dis. 2005 Jul;20(4):353-62 PMID: 15614505
  69. Collagen fibrillogenesis: fibronectin, integrins, and minor collagens as organizers and nucleators.
    Curr Opin Cell Biol. 2008 Oct;20(5):495-501 PMID: 18640274
  70. COL11A1 promotes tumor progression and predicts poor clinical outcome in ovarian cancer.
    Oncogene. 2014 Jun 26;33(26):3432-40 PMID: 23934190
  71. IGF2 over-expression in solitary fibrous tumours is independent of anatomical location and is related to loss of imprinting.
    J Pathol. 2010 Jul;221(3):300-7 PMID: 20527023
  72. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis.
    Nature. 2007 Oct 4;449(7162):557-63 PMID: 17914389
  73. Collagen as a double-edged sword in tumor progression.
    Tumour Biol. 2014 Apr;35(4):2871-82 PMID: 24338768
  74. Chemokines at the crossroads of tumor-fibroblast interactions that promote malignancy.
    J Leukoc Biol. 2011 Jan;89(1):31-9 PMID: 20628066
  75. Validation of COL11A1/procollagen 11A1 expression in TGF-β1-activated immortalised human mesenchymal cells and in stromal cells of human colon adenocarcinoma.
    BMC Cancer. 2014 Nov 23;14:867 PMID: 25417197
  76. A potential role of collagens expression in distinguishing between premalignant and malignant lesions in stomach.
    Anat Rec (Hoboken). 2009 May;292(5):692-700 PMID: 19306436
  77. Identification of gliotropic factors that induce human stem cell migration to malignant tumor.
    J Proteome Res. 2009 Jun;8(6):2873-81 PMID: 19351187
  78. Identification of unique gene expression patterns within different lesional sites of keloids.
    Wound Repair Regen. 2008 Mar-Apr;16(2):254-65 PMID: 18282266
  79. Cadherin-11 is expressed in invasive breast cancer cell lines.
    Cancer Res. 1999 Feb 15;59(4):947-52 PMID: 10029089
  80. Nuclear factor Y (NF-Y) regulates the proximal promoter activity of the mouse collagen α1(XI) gene (Col11a1) in chondrocytes.
    In Vitro Cell Dev Biol Anim. 2014 Apr;50(4):358-66 PMID: 24092017
  81. Collagen, type XI, alpha 1: an accurate marker for differential diagnosis of breast carcinoma invasiveness in core needle biopsies.
    Pathol Res Pract. 2014 Dec;210(12):879-84 PMID: 25175819
  82. Up-regulation of the lymphatic marker podoplanin, a mucin-type transmembrane glycoprotein, in human squamous cell carcinomas and germ cell tumors.
    Am J Pathol. 2005 Mar;166(3):913-21 PMID: 15743802
  83. Genomic deregulation during metastasis of renal cell carcinoma implements a myofibroblast-like program of gene expression.
    Cancer Res. 2010 Dec 1;70(23):9682-92 PMID: 20952505
  84. Novel candidate tumor marker genes for lung adenocarcinoma.
    Oncogene. 2002 Oct 24;21(49):7598-604 PMID: 12386823
  85. A collagen-remodeling gene signature regulated by TGF-β signaling is associated with metastasis and poor survival in serous ovarian cancer.
    Clin Cancer Res. 2014 Feb 1;20(3):711-23 PMID: 24218511
  86. Tumor matrix protein collagen XIα1 in cancer.
    Cancer Lett. 2015 Feb 28;357(2):448-53 PMID: 25511741
Article Info
Journal
Tumour biology : the journal of the International Society for Oncodevelopmental Biology and Medicine
Abbr.
Tumour Biol
ISSN
1423-0380
Published
2015-04-00
Epub
2015-00-12
Pages
2213-22
Language
English
Region
Netherlands
NLM ID
8409922
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]