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Published in: Annals of Surgical Oncology 2/2008

01-02-2008 | Gastrointestinal Oncology

The Expression of Type IV Collagen α6 Chain Is Related to the Prognosis in Patients with Esophageal Squamous Cell Carcinoma

Authors: Yoshifumi Baba, Ken-ichi Iyama, MD, PhD, Koei Ikeda, Shinji Ishikawa, Naoko Hayashi, Nobutomo Miyanari, Yoshikazu Sado, Yoshifumi Ninomiya, Hideo Baba

Published in: Annals of Surgical Oncology | Issue 2/2008

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Abstract

Background

The destruction of the basement membrane (BM) is the first step in cancer cell invasion and metastasis. Type IV collagen is a major component of the BM, and is composed of six genetically distinct α(IV) chains: α1(IV) to α6(IV). The loss of α5/α6(IV) chains from the epithelial BM at the early stage of cancer cell invasion has been reported in several cancers. However, the expression of α5/α6(IV) chains in esophageal squamous cell carcinoma (ESCC) remains unclear.

Methods

The expression of α(IV) chains in 116 resected ESCC specimens was immunohistochemically examined. The role of α6(IV) chain was assessed in ESCC cell lines by short interfering RNA (siRNA).

Results

In intraepithelial carcinoma, the α5/α6(IV) chains were stained in a continuous linear pattern in the BM. In some cases of ESCC with the invasion beyond the lamina propria, the α5/α6(IV) chains were lost in the BM zone surrounding the cancer cell nests, but in other cases they remained. In the former, the disease-free survival and overall survival were significantly better than in those with the latter. The down-regulation of α6(IV) chain expression by siRNA revealed a slight increase of cancer cell invasiveness.

Conclusions

The evaluation of α5/α6(IV) chains may be a useful marker for determining tumor cell properties, as a prognostic factor, in patients with ESCC.
Literature
1.
go back to reference Liotta LA, Rao CN, Barsky SH. Tumor invasion and the extracellular matrix. Lab Invest 1983;49:636–49PubMed Liotta LA, Rao CN, Barsky SH. Tumor invasion and the extracellular matrix. Lab Invest 1983;49:636–49PubMed
2.
go back to reference Rohrbach DH, Timpl R. Molecular and cellular aspects of basement membrane. San Diego: Academic Press, 1993;1–437 Rohrbach DH, Timpl R. Molecular and cellular aspects of basement membrane. San Diego: Academic Press, 1993;1–437
3.
go back to reference Kalluri R. Basement membrane: Structure, assembly and role in tumor angiogenesis. Nat Rev Cancer 2003;3:422–33PubMedCrossRef Kalluri R. Basement membrane: Structure, assembly and role in tumor angiogenesis. Nat Rev Cancer 2003;3:422–33PubMedCrossRef
4.
go back to reference Blood CH, Zetter BR. Tumor interactions with the vasculatures: angiogenesis and tumor metastasis. Biochim Biophys Acta 1990;1032:89–118PubMed Blood CH, Zetter BR. Tumor interactions with the vasculatures: angiogenesis and tumor metastasis. Biochim Biophys Acta 1990;1032:89–118PubMed
5.
go back to reference Solomon E, Hall V, Kurkinen M. The human α2(IV) collagen gene, COL4A2 is systemic with the α1(IV) gene, COL4A1, on chromosome 13. Ann Hum Genet 1987;51:125–7PubMedCrossRef Solomon E, Hall V, Kurkinen M. The human α2(IV) collagen gene, COL4A2 is systemic with the α1(IV) gene, COL4A1, on chromosome 13. Ann Hum Genet 1987;51:125–7PubMedCrossRef
6.
go back to reference Mariyama M, Zheng K, Yang-Feng TL, Reeders ST: Colonization of the genes for the α3(IV) and α4(IV) chains of the type IV collagen to chromosome 2 bands q35-q37. Genomics 1992;13:809–13PubMedCrossRef Mariyama M, Zheng K, Yang-Feng TL, Reeders ST: Colonization of the genes for the α3(IV) and α4(IV) chains of the type IV collagen to chromosome 2 bands q35-q37. Genomics 1992;13:809–13PubMedCrossRef
7.
go back to reference Sugimoto M, Oohashi T, Ninomia Y. The genes COL4A5 and COL4A6, coding for the basement membrane collagen chains α5(IV) and α6(IV), are located head-to-head in close proximity on human chromosome Xq22 and COL4A6 is transcribed from two alternative promoters. Proc Natl Acad Sci USA 1994;91:11679–83PubMedCrossRef Sugimoto M, Oohashi T, Ninomia Y. The genes COL4A5 and COL4A6, coding for the basement membrane collagen chains α5(IV) and α6(IV), are located head-to-head in close proximity on human chromosome Xq22 and COL4A6 is transcribed from two alternative promoters. Proc Natl Acad Sci USA 1994;91:11679–83PubMedCrossRef
8.
go back to reference Timpl R. Structure and biological activity of basement membrane proteins. Eur J Biochem 1989;180:487–502PubMedCrossRef Timpl R. Structure and biological activity of basement membrane proteins. Eur J Biochem 1989;180:487–502PubMedCrossRef
9.
go back to reference Sado Y, Kagawa M, Naito I, et al. Organization and expression of basement membrane collagen IVgenes and their roles in human disorders. J Biochem 1998;123:767–76PubMed Sado Y, Kagawa M, Naito I, et al. Organization and expression of basement membrane collagen IVgenes and their roles in human disorders. J Biochem 1998;123:767–76PubMed
10.
go back to reference Mariyama M, Leinonen A, Mochizuki T, Tryggvan K, Reeders ST. Complete primary structure of the human α3(IV) collagen chain. Coexpression of the α3(IV) and α4(IV) collagen chains in human tissues. J Biol Chem 1994;269:23013–7PubMed Mariyama M, Leinonen A, Mochizuki T, Tryggvan K, Reeders ST. Complete primary structure of the human α3(IV) collagen chain. Coexpression of the α3(IV) and α4(IV) collagen chains in human tissues. J Biol Chem 1994;269:23013–7PubMed
11.
go back to reference Ninomiya Y, Kagawa M, Iyama K, et al. Differential expression of two basement membrane collagen genes, COL4A5 and COL4A6, demonstrating by immunofluorescence staining using peptide-specific monoclonal antibodies. J Cell Biol 1995;130:1219–29PubMedCrossRef Ninomiya Y, Kagawa M, Iyama K, et al. Differential expression of two basement membrane collagen genes, COL4A5 and COL4A6, demonstrating by immunofluorescence staining using peptide-specific monoclonal antibodies. J Cell Biol 1995;130:1219–29PubMedCrossRef
12.
go back to reference Simoneau A, Herring-Gillam FE, Vachon PH, et al. Identification, distribution, and tissue origin of the α5(IV) and α6(IV) collagen chains in the developing human intestine. Dev Dyn 1998;212:437–47PubMedCrossRef Simoneau A, Herring-Gillam FE, Vachon PH, et al. Identification, distribution, and tissue origin of the α5(IV) and α6(IV) collagen chains in the developing human intestine. Dev Dyn 1998;212:437–47PubMedCrossRef
13.
go back to reference Seki T, Naito I, Oohashi T, Sado Y, Ninomiya Y. Differential expression of type IV collagen isoforms, α5(IV) and α6(IV) chains, in the basement membranes surrounding smooth muscle cells. Histochem Cell Biol 1990;110:359–66CrossRef Seki T, Naito I, Oohashi T, Sado Y, Ninomiya Y. Differential expression of type IV collagen isoforms, α5(IV) and α6(IV) chains, in the basement membranes surrounding smooth muscle cells. Histochem Cell Biol 1990;110:359–66CrossRef
14.
go back to reference Kiyofuji MA, Iyama K, Kitaoka M, Sado Y, Ninomiya Y, Ueda S. Quantitative analysis of type IV collagen alpha chains in the basement membrane of human urogenital epithelium. Histochem J 2002;34:479–86PubMedCrossRef Kiyofuji MA, Iyama K, Kitaoka M, Sado Y, Ninomiya Y, Ueda S. Quantitative analysis of type IV collagen alpha chains in the basement membrane of human urogenital epithelium. Histochem J 2002;34:479–86PubMedCrossRef
15.
go back to reference Tanaka K, Iyama K, Kitaoka M, et al. Differential expression of α1(IV), α2(IV), α5(IV) and α6(IV) collagen chains in the basement membrane of basal cell carcinoma. Histochem J 1997;29:563–70PubMedCrossRef Tanaka K, Iyama K, Kitaoka M, et al. Differential expression of α1(IV), α2(IV), α5(IV) and α6(IV) collagen chains in the basement membrane of basal cell carcinoma. Histochem J 1997;29:563–70PubMedCrossRef
16.
go back to reference Nakano S, Iyama K, Ogawa M, Yoshioka H, Sado Y, Oohashi T, Ninomiya Y. Differential tissular expression and localization of type IV collagen α1(IV), α2(IV), α5(IV) and α6(IV) chains and their mRNA in normal breast and in benign and malignant breast tumors. Lab Invest 1999;79:281–92PubMed Nakano S, Iyama K, Ogawa M, Yoshioka H, Sado Y, Oohashi T, Ninomiya Y. Differential tissular expression and localization of type IV collagen α1(IV), α2(IV), α5(IV) and α6(IV) chains and their mRNA in normal breast and in benign and malignant breast tumors. Lab Invest 1999;79:281–92PubMed
17.
go back to reference Nakano KY, Iyama K, Mori T, et al. Loss of alveolar basement membrane type IV collagen α3, α4 and α5(IV) chains in bronchioloalveolar carcinoma of the lung. J Pathol 2001;194:420–7PubMedCrossRef Nakano KY, Iyama K, Mori T, et al. Loss of alveolar basement membrane type IV collagen α3, α4 and α5(IV) chains in bronchioloalveolar carcinoma of the lung. J Pathol 2001;194:420–7PubMedCrossRef
18.
go back to reference Misumi S, Iyama K, Honda Y, et al. Differential expression of basement membrane type IV collagen α1, α2, α5 and α6 chains among the histological subtypes of adenoid cystic carcinoma. Virchow Arch 2004;445:54–62 Misumi S, Iyama K, Honda Y, et al. Differential expression of basement membrane type IV collagen α1, α2, α5 and α6 chains among the histological subtypes of adenoid cystic carcinoma. Virchow Arch 2004;445:54–62
19.
go back to reference Hiki Y, Iyama K, Tsuruta J, et al. Differential distribution of basement membrane type IV collagen α1, α2, α5 and α6 chains in colorectal epithelial tumors. Pathol Int. 2004;52:224–33CrossRef Hiki Y, Iyama K, Tsuruta J, et al. Differential distribution of basement membrane type IV collagen α1, α2, α5 and α6 chains in colorectal epithelial tumors. Pathol Int. 2004;52:224–33CrossRef
20.
go back to reference Ikeda K, Iyama K, Ishikawa S, et al. Loss of expression of Type IV collagen α5 and α6 chains in colorectal cancer associated with the hypermethylation of their promoter region. Am J Pathol 2006;168:856–65PubMedCrossRef Ikeda K, Iyama K, Ishikawa S, et al. Loss of expression of Type IV collagen α5 and α6 chains in colorectal cancer associated with the hypermethylation of their promoter region. Am J Pathol 2006;168:856–65PubMedCrossRef
21.
go back to reference Oka Y, Naito I, Manabe K, et al. Distribution of collagen type IV α1-α6 chains in human normal colorectum and colorectal cancer demonstrated by immunofluorescence staining using chain-specific epitope defined monoclonal antibodies. J Gastroenterol Hepatol 2002;17:980–6PubMedCrossRef Oka Y, Naito I, Manabe K, et al. Distribution of collagen type IV α1-α6 chains in human normal colorectum and colorectal cancer demonstrated by immunofluorescence staining using chain-specific epitope defined monoclonal antibodies. J Gastroenterol Hepatol 2002;17:980–6PubMedCrossRef
22.
go back to reference Martinella-Catusse C, Polette M, Noel A, et al. Downregulation of MT1-MMP expression by the α3 chain pf type IV collagen inhibits bronchial tumor cell line invasion. Lab Invest 2001;81:167–75PubMed Martinella-Catusse C, Polette M, Noel A, et al. Downregulation of MT1-MMP expression by the α3 chain pf type IV collagen inhibits bronchial tumor cell line invasion. Lab Invest 2001;81:167–75PubMed
23.
go back to reference Pasco S, Ramont L, Venteo L, Pluot M, Maquart FX, Monboisse JC. In vivo overexpression of tumostatin domains by tumor cells inhibits their invasive properties in a mouse melanoma model. Exp Cell Res 2004;301:251–65PubMedCrossRef Pasco S, Ramont L, Venteo L, Pluot M, Maquart FX, Monboisse JC. In vivo overexpression of tumostatin domains by tumor cells inhibits their invasive properties in a mouse melanoma model. Exp Cell Res 2004;301:251–65PubMedCrossRef
24.
go back to reference He GA, Luo JX, Zhang TY, Hu ZS, Wang FY. The C-terminal domain of canstatin suppresses in vivo tumor growth associated with proliferation of endothelial cells. Biochem Biophys Res Commun 2004;318:354–60PubMedCrossRef He GA, Luo JX, Zhang TY, Hu ZS, Wang FY. The C-terminal domain of canstatin suppresses in vivo tumor growth associated with proliferation of endothelial cells. Biochem Biophys Res Commun 2004;318:354–60PubMedCrossRef
25.
go back to reference Petitclerc E, Boutaud A, Prestayko A, et al. New functions for non-collagenous domains of human collagen type IV. Novel integrin ligands inhibiting angiogenesis and tumor growth in vivo. J Biol Chem 2000;275:8051–61PubMedCrossRef Petitclerc E, Boutaud A, Prestayko A, et al. New functions for non-collagenous domains of human collagen type IV. Novel integrin ligands inhibiting angiogenesis and tumor growth in vivo. J Biol Chem 2000;275:8051–61PubMedCrossRef
26.
go back to reference Maeshima Y, Colorado PC, Torre A, et al. Distinct antitumor properties of a type IV collagen derived from basement membrane. J Biol Chem 2000;275:21340–8PubMedCrossRef Maeshima Y, Colorado PC, Torre A, et al. Distinct antitumor properties of a type IV collagen derived from basement membrane. J Biol Chem 2000;275:21340–8PubMedCrossRef
27.
go back to reference Kamphaus GD, Colorado PC, Panka DJ, et al. Canstatin, a novel matrix-derived inhibitor of angiogenesis and tumor growth. J Biol Chem 2000;275:1209–15PubMedCrossRef Kamphaus GD, Colorado PC, Panka DJ, et al. Canstatin, a novel matrix-derived inhibitor of angiogenesis and tumor growth. J Biol Chem 2000;275:1209–15PubMedCrossRef
28.
go back to reference Sobin LH, Wittekind CH. TNM classification of malignant tumors, 6th ed. New York: Wiley 2002 Sobin LH, Wittekind CH. TNM classification of malignant tumors, 6th ed. New York: Wiley 2002
29.
go back to reference Hamilton SR, Aaltonen LA. World Health Organization classification of tumours. Tumours of the Digestive System. Lyon: IARC Press, 2000 Hamilton SR, Aaltonen LA. World Health Organization classification of tumours. Tumours of the Digestive System. Lyon: IARC Press, 2000
30.
go back to reference Sado Y, Kagawa M, Kishiro Y, et al. Establishment by the rat lymph mode method of epitope-defined monoclonal antibodies recognizing the six different α chains of human type IV collagen. Histochem Cell Biol1995;104:267–75PubMedCrossRef Sado Y, Kagawa M, Kishiro Y, et al. Establishment by the rat lymph mode method of epitope-defined monoclonal antibodies recognizing the six different α chains of human type IV collagen. Histochem Cell Biol1995;104:267–75PubMedCrossRef
31.
go back to reference Kihara AH, Moriscot AS, Ferreira PJ, Hamassaki DM. Protecting RNA in fixed tissue: An alternative method for LCM users. J Neurosci Methods 2005;148:103–7PubMedCrossRef Kihara AH, Moriscot AS, Ferreira PJ, Hamassaki DM. Protecting RNA in fixed tissue: An alternative method for LCM users. J Neurosci Methods 2005;148:103–7PubMedCrossRef
32.
go back to reference Strenlicht MD, Werb Z. How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol 2001;17:463–516CrossRef Strenlicht MD, Werb Z. How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol 2001;17:463–516CrossRef
33.
go back to reference Sato H, Takino T, Okada Y, Cao J, Shinagawa A, Yamamoto E, Seike M. A matrix metalloproteinase expressed on the surface of invasive tumor cells. Nature 1994;370:61–5PubMedCrossRef Sato H, Takino T, Okada Y, Cao J, Shinagawa A, Yamamoto E, Seike M. A matrix metalloproteinase expressed on the surface of invasive tumor cells. Nature 1994;370:61–5PubMedCrossRef
34.
go back to reference Ohashi K, Nemoto T, Nakamura K, Nemori R. Increased expression of matrix metalloproteinase 7 and 9 and membrane type 1 –matrix metalloproteinase in esophageal squamous cell carcinoma. Cancer 2000;88:2201–9PubMedCrossRef Ohashi K, Nemoto T, Nakamura K, Nemori R. Increased expression of matrix metalloproteinase 7 and 9 and membrane type 1 –matrix metalloproteinase in esophageal squamous cell carcinoma. Cancer 2000;88:2201–9PubMedCrossRef
35.
go back to reference Gu ZD, Li JY, Li M, Gu J, Shi XT, Ke Y, Chen KN. Matrix metalloproteinase expression correlates with survival in patients with esophageal squamous cell carcinoma. Am J Gastroenterol 2005;100:1835–43PubMedCrossRef Gu ZD, Li JY, Li M, Gu J, Shi XT, Ke Y, Chen KN. Matrix metalloproteinase expression correlates with survival in patients with esophageal squamous cell carcinoma. Am J Gastroenterol 2005;100:1835–43PubMedCrossRef
36.
go back to reference Tamamura R, Nagatsuka H, Siar CH, et al. Differential expression of basement membrane collagen-IV α1 to α6 chains during oral carcinogenesis. Virchow Arch 2006;449:358–66CrossRef Tamamura R, Nagatsuka H, Siar CH, et al. Differential expression of basement membrane collagen-IV α1 to α6 chains during oral carcinogenesis. Virchow Arch 2006;449:358–66CrossRef
37.
go back to reference Robey-Cafferty SS, el-Naggar AK, Sahin AA, Bruner JM, Ro JY, Clearly KR. Prognostic factors in esophageal squamous carcinoma. A study of histologic features, blood group expression, and DNA ploidy. Am J Clin Pathol 1991;95:844–89PubMed Robey-Cafferty SS, el-Naggar AK, Sahin AA, Bruner JM, Ro JY, Clearly KR. Prognostic factors in esophageal squamous carcinoma. A study of histologic features, blood group expression, and DNA ploidy. Am J Clin Pathol 1991;95:844–89PubMed
38.
go back to reference Edwards JM, Hillier VF, Lawson RA, Moussalli H, Hasleton PS. Squamous carcinoma of the oesophagus: histological criteria and their prognostic significance. Br J Cancer 1989:59:429–33PubMed Edwards JM, Hillier VF, Lawson RA, Moussalli H, Hasleton PS. Squamous carcinoma of the oesophagus: histological criteria and their prognostic significance. Br J Cancer 1989:59:429–33PubMed
39.
go back to reference Khan OA, Alexiou C, Soomro I, Duffy JP, Morgan WE, Beggs FD. Pathological determinants of survival in node-negative oesophageal cancer. Br J Surg 2004:91:1586–91PubMedCrossRef Khan OA, Alexiou C, Soomro I, Duffy JP, Morgan WE, Beggs FD. Pathological determinants of survival in node-negative oesophageal cancer. Br J Surg 2004:91:1586–91PubMedCrossRef
Metadata
Title
The Expression of Type IV Collagen α6 Chain Is Related to the Prognosis in Patients with Esophageal Squamous Cell Carcinoma
Authors
Yoshifumi Baba
Ken-ichi Iyama, MD, PhD
Koei Ikeda
Shinji Ishikawa
Naoko Hayashi
Nobutomo Miyanari
Yoshikazu Sado
Yoshifumi Ninomiya
Hideo Baba
Publication date
01-02-2008
Publisher
Springer-Verlag
Published in
Annals of Surgical Oncology / Issue 2/2008
Print ISSN: 1068-9265
Electronic ISSN: 1534-4681
DOI
https://doi.org/10.1245/s10434-007-9592-4

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