Skip to main content
Top
Published in: Virchows Archiv 4/2005

01-10-2005 | Original Article

Immunolocalization and distribution patterns of type IV collagen alpha chains in oral mucosal melanoma

Authors: Hitoshi Nagatsuka, Rosario Santos Rivera, Mehmet Gunduz, You-Jin Lee, Ryo Tamamura, Esra Gunduz, Ichiro Naito, Yoshikazu Sado, Noriyuki Nagai

Published in: Virchows Archiv | Issue 4/2005

Login to get access

Abstract

The basement membrane (BM) is mainly composed of type IV collagen, which is composed of triple combinations of six distinct alpha (α) chains in a tissue-specific manner. The six collagen chain-specific antibodies (α1–α6) were used to examine the BMs of the oral epithelium (OE) and tumor clusters in oral mucosal melanoma (OMM). Eight OMM cases were examined. Results showed that the α1 and α2 chains were constantly detected at the BM of the normal OE as well as at the OE with atypical melanocytic proliferation and in invasive melanoma with nodular nests. The α1 and α2 chains were intermittently detected in in situ OMM, early invasive OMM and advanced invasive OMM with sheet-like nests. Gradual loss of α5 and α6 from the OE with atypical melanocyte through in situ OMM and early invasive OMM was observed. These findings suggest that changes in the immunolocalization and distribution patterns of type IV collagen α chains are associated with the progression of OMM. The distribution pattern of type IV collagen α chain varies depending on the architecture of the nest.
Literature
1.
go back to reference Barker BF, Carpenter WM, Daniels TE, Kahn MA, Leider AS, Lozada-Nur F, Lynch DP, Melrose R, Merrell P, Morton T, Peters E, Regezi JA, Richards SD, Rick GM, Rohrer MD, Slater L, Stewart JC, Tomich CE, Vickers RA, Wood NK, Young SK (1997) Oral mucosal melanomas: the WESTOP Banff workshop proceedings. Western Society of Teachers of Oral Pathology. Oral Surg Oral Med Oral Pathol Oral Radiol Endo 83:672–679CrossRef Barker BF, Carpenter WM, Daniels TE, Kahn MA, Leider AS, Lozada-Nur F, Lynch DP, Melrose R, Merrell P, Morton T, Peters E, Regezi JA, Richards SD, Rick GM, Rohrer MD, Slater L, Stewart JC, Tomich CE, Vickers RA, Wood NK, Young SK (1997) Oral mucosal melanomas: the WESTOP Banff workshop proceedings. Western Society of Teachers of Oral Pathology. Oral Surg Oral Med Oral Pathol Oral Radiol Endo 83:672–679CrossRef
2.
go back to reference Bonanno E, Iurlaro M, Madri JA, Nicosia RF (2000) Type IV collagen modulates angiogenesis and neovessel survival in rat aorta model. In Vitro Cell Dev Biol Anim 5:336–340CrossRef Bonanno E, Iurlaro M, Madri JA, Nicosia RF (2000) Type IV collagen modulates angiogenesis and neovessel survival in rat aorta model. In Vitro Cell Dev Biol Anim 5:336–340CrossRef
3.
go back to reference Borza DB, Bondar O, Ninomiya Y, Sado Y, Naito I, Todd P, Hudson BG (2001) The NC1 domain of collagen IV encodes a novel network composed of the alpha 1, alpha 2, alpha 5, and alpha 6 chains in smooth muscle basement membranes. J Biol Chem 276:28532–28540PubMedCrossRef Borza DB, Bondar O, Ninomiya Y, Sado Y, Naito I, Todd P, Hudson BG (2001) The NC1 domain of collagen IV encodes a novel network composed of the alpha 1, alpha 2, alpha 5, and alpha 6 chains in smooth muscle basement membranes. J Biol Chem 276:28532–28540PubMedCrossRef
4.
go back to reference Boutad A, Borza DB, Bondar O, Gunwar S, Netzer KO, Singh N, Ninomiya Y, Sado Y, Noelken ME, Hudson BG (2000) Type IV collagen of the glomerular basement membrane. Evidence that the chain specificity of network assembly is encoded by the noncollagenous NC1 domains. J Biol Chem 275:30716–30724CrossRefPubMed Boutad A, Borza DB, Bondar O, Gunwar S, Netzer KO, Singh N, Ninomiya Y, Sado Y, Noelken ME, Hudson BG (2000) Type IV collagen of the glomerular basement membrane. Evidence that the chain specificity of network assembly is encoded by the noncollagenous NC1 domains. J Biol Chem 275:30716–30724CrossRefPubMed
5.
go back to reference Dehan P, Waltregny D, Beschin A, Noel A, Castronovo V, Trygvason K, De Leval J, Foidart JM (1997) Loss of type IV collagen alpha 5 and alpha 6 chains in human invasive prostate carcinomas. Am J Pathol 151:1097–10104PubMed Dehan P, Waltregny D, Beschin A, Noel A, Castronovo V, Trygvason K, De Leval J, Foidart JM (1997) Loss of type IV collagen alpha 5 and alpha 6 chains in human invasive prostate carcinomas. Am J Pathol 151:1097–10104PubMed
6.
go back to reference Garzino-Demo P, Fasolis M, Maggiore GM, Pagano M, Berrone S (2004) Oral mucosal melanoma: a series of case reports. J Craniomaxillofac Surg 32:251–257PubMed Garzino-Demo P, Fasolis M, Maggiore GM, Pagano M, Berrone S (2004) Oral mucosal melanoma: a series of case reports. J Craniomaxillofac Surg 32:251–257PubMed
7.
go back to reference Hicks MJ, Flaitz CM (2000) Oral mucosal melanoma: epidemiology and pathobiology. Oral Oncol 36:152–169CrossRefPubMed Hicks MJ, Flaitz CM (2000) Oral mucosal melanoma: epidemiology and pathobiology. Oral Oncol 36:152–169CrossRefPubMed
8.
go back to reference Hiki Y, Iyama K, Tsuruta J, Egami H, Kamio T, Suko S, Naito I, Sado Y, Ninomiya Y, Ogawa M (2002) Differential distribution of basement membrane type IV collagen alpha1(IV), alpha2(IV), alpha5(IV) and alpha6(IV) chains in colorectal epithelial tumors. Pathol Int 52:224–233CrossRefPubMed Hiki Y, Iyama K, Tsuruta J, Egami H, Kamio T, Suko S, Naito I, Sado Y, Ninomiya Y, Ogawa M (2002) Differential distribution of basement membrane type IV collagen alpha1(IV), alpha2(IV), alpha5(IV) and alpha6(IV) chains in colorectal epithelial tumors. Pathol Int 52:224–233CrossRefPubMed
9.
go back to reference Hofmann UB, Westphal JR, Van Muijen GN, Ruiter DJ (2000) Matrix metalloproteinases in human melanoma. J Invest Dermatol 115:337–344CrossRefPubMed Hofmann UB, Westphal JR, Van Muijen GN, Ruiter DJ (2000) Matrix metalloproteinases in human melanoma. J Invest Dermatol 115:337–344CrossRefPubMed
10.
go back to reference Hudson BG, Reeders ST, Tryggvason K (1993) Type IV collagen: structure, gene organization, and role in human diseases. Molecular basis of Goodpasture and Alport syndromes and diffuse leiomyomatosis. J Biol Chem 268:26033–26036PubMed Hudson BG, Reeders ST, Tryggvason K (1993) Type IV collagen: structure, gene organization, and role in human diseases. Molecular basis of Goodpasture and Alport syndromes and diffuse leiomyomatosis. J Biol Chem 268:26033–26036PubMed
11.
go back to reference Kadono G, Ishihara T, Yamaguchi T, Kato K, Kondo F, Naito I, Sado Y, Saisho H (2004) Immunohistochemical localization of type IV collagen alpha chains in the basement membrane of the pancreatic duct in human normal pancreas and pancreatic diseases. Pancreas 29:61–66CrossRefPubMed Kadono G, Ishihara T, Yamaguchi T, Kato K, Kondo F, Naito I, Sado Y, Saisho H (2004) Immunohistochemical localization of type IV collagen alpha chains in the basement membrane of the pancreatic duct in human normal pancreas and pancreatic diseases. Pancreas 29:61–66CrossRefPubMed
12.
go back to reference Kagawa M, Kishiro Y, Naito I, Nemoto T, Nakanishi H, Ninomiya Y, Sado Y (1997) Epitope-defined monoclonal antibodies against type-IV collagen for diagnosis of Alport's syndrome. Nephrol Dial Transplant 12:1238–1241CrossRefPubMed Kagawa M, Kishiro Y, Naito I, Nemoto T, Nakanishi H, Ninomiya Y, Sado Y (1997) Epitope-defined monoclonal antibodies against type-IV collagen for diagnosis of Alport's syndrome. Nephrol Dial Transplant 12:1238–1241CrossRefPubMed
13.
go back to reference Kato T, Takematsu H, Tomita Y, Takahashi M, Abe R (1987) Malignant melanoma of mucous membranes. A clinicopathologic study of 13 cases in Japanese patients. Arch Dermatol 123:216–220CrossRefPubMed Kato T, Takematsu H, Tomita Y, Takahashi M, Abe R (1987) Malignant melanoma of mucous membranes. A clinicopathologic study of 13 cases in Japanese patients. Arch Dermatol 123:216–220CrossRefPubMed
14.
go back to reference Lee YJ, Nagai N, Siar CH, Nakano K, Nagatsuka H, Tsujigiwa H, Roan CH, Gunduz M (2002) Angioarchitecture of primary oral malignant melanomas. J Histochem Cytochem 50:1555–1562PubMed Lee YJ, Nagai N, Siar CH, Nakano K, Nagatsuka H, Tsujigiwa H, Roan CH, Gunduz M (2002) Angioarchitecture of primary oral malignant melanomas. J Histochem Cytochem 50:1555–1562PubMed
15.
go back to reference Marneros AG, Olsen BR (2001) The role of collagen-derived proteolytic fragments in angiogenesis. Matrix Biol 5–6:337–345CrossRef Marneros AG, Olsen BR (2001) The role of collagen-derived proteolytic fragments in angiogenesis. Matrix Biol 5–6:337–345CrossRef
16.
go back to reference Maniotis AJ, Folberg R, Hess A, Seftor EA, Gardner LM, Pe'er J, Trent JM, Meltzer PS, Hendrix MJ (1999) Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry. Am J Pathol 155:739–752PubMed Maniotis AJ, Folberg R, Hess A, Seftor EA, Gardner LM, Pe'er J, Trent JM, Meltzer PS, Hendrix MJ (1999) Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry. Am J Pathol 155:739–752PubMed
17.
go back to reference Misumi S, Iyama K, Honda Y, Kitano T, Sado Y, Ninomiya Y, Shinohara M (2004) Differential expression of basement membrane type-IV collagen alpha1, alpha2, alpha5 and alpha6 chains among the histological subtypes of adenoid cystic carcinoma. Virchows Arch 445:54–462PubMed Misumi S, Iyama K, Honda Y, Kitano T, Sado Y, Ninomiya Y, Shinohara M (2004) Differential expression of basement membrane type-IV collagen alpha1, alpha2, alpha5 and alpha6 chains among the histological subtypes of adenoid cystic carcinoma. Virchows Arch 445:54–462PubMed
19.
go back to reference Nagatsuka H, Siar CH, Nakano K, Tsujigiwa H, Gunduz M, Choufuku H, Lee YJ, Naito I, Sado Y, Nagai N (2002) Differential expression of collagen IV alpha1 to alpha6 chains in basement membranes of benign and malignant odontogenic tumors. Virchows Arch 441:392–399CrossRefPubMed Nagatsuka H, Siar CH, Nakano K, Tsujigiwa H, Gunduz M, Choufuku H, Lee YJ, Naito I, Sado Y, Nagai N (2002) Differential expression of collagen IV alpha1 to alpha6 chains in basement membranes of benign and malignant odontogenic tumors. Virchows Arch 441:392–399CrossRefPubMed
20.
go back to reference Nakano KY, Iyama KI, Mori T, Yoshioka M, Hiraoka T, Sado Y, Ninomiya Y (2001) Loss of alveolar basement membrane type IV collagen alpha3, alpha4, and alpha5 chains in bronchioloalveolar carcinoma of the lung. J Pathol 194:420–427CrossRefPubMed Nakano KY, Iyama KI, Mori T, Yoshioka M, Hiraoka T, Sado Y, Ninomiya Y (2001) Loss of alveolar basement membrane type IV collagen alpha3, alpha4, and alpha5 chains in bronchioloalveolar carcinoma of the lung. J Pathol 194:420–427CrossRefPubMed
21.
go back to reference Nakano S, Iyama K, Ogawa M, Yoshioka H, Sado Y, Oohashi T, Ninomiya Y (1999) Differential tissular expression and localization of type IV collagen alpha1(IV), alpha2(IV), alpha5(IV), and alpha6(IV) chains and their mRNA in normal breast and in benign and malignant breast tumors. Lab Invest 79:281–292PubMed Nakano S, Iyama K, Ogawa M, Yoshioka H, Sado Y, Oohashi T, Ninomiya Y (1999) Differential tissular expression and localization of type IV collagen alpha1(IV), alpha2(IV), alpha5(IV), and alpha6(IV) chains and their mRNA in normal breast and in benign and malignant breast tumors. Lab Invest 79:281–292PubMed
22.
go back to reference Ninomiya Y, Kagawa M, Iyama K, Naito I, Kishiro Y, Seyer JM, Sugimoto M, Oohashi T, Sado Y (1995) Differential expression of two basement membrane collagen genes, COL4A6 and COL4A5, demonstrated by immunofluorescence staining using peptide-specific monoclonal antibodies. J Cell Biol 5:1219–1229CrossRef Ninomiya Y, Kagawa M, Iyama K, Naito I, Kishiro Y, Seyer JM, Sugimoto M, Oohashi T, Sado Y (1995) Differential expression of two basement membrane collagen genes, COL4A6 and COL4A5, demonstrated by immunofluorescence staining using peptide-specific monoclonal antibodies. J Cell Biol 5:1219–1229CrossRef
23.
go back to reference Oka Y, Naito I, Manabe K, Sado Y, Matsushima H, Ninomiya Y, Mizuno M, Tsuji T (2002) Distribution of collagen type IV alpha1-6 chains in human normal colorectum and colorectal cancer demonstrated by immunofluorescence staining using chain-specific epitope-defined monoclonal antibodies. J Gastroenterol Hepatol 9:980–986CrossRef Oka Y, Naito I, Manabe K, Sado Y, Matsushima H, Ninomiya Y, Mizuno M, Tsuji T (2002) Distribution of collagen type IV alpha1-6 chains in human normal colorectum and colorectal cancer demonstrated by immunofluorescence staining using chain-specific epitope-defined monoclonal antibodies. J Gastroenterol Hepatol 9:980–986CrossRef
24.
go back to reference Pasco S, Ramont L, Maquart FX, Monboisse JC (2004) Control of melanoma progression by various matrikines from basement membrane macromolecules. Crit Rev Oncol Hematol 49:221–233PubMedCrossRef Pasco S, Ramont L, Maquart FX, Monboisse JC (2004) Control of melanoma progression by various matrikines from basement membrane macromolecules. Crit Rev Oncol Hematol 49:221–233PubMedCrossRef
25.
go back to reference Rapidis AD, Apostolidis C, Vilos G, Valsamis S (2003) Primary malignant melanoma of the oral mucosa. J Oral Maxillofac Surg 61:1132–1139CrossRefPubMed Rapidis AD, Apostolidis C, Vilos G, Valsamis S (2003) Primary malignant melanoma of the oral mucosa. J Oral Maxillofac Surg 61:1132–1139CrossRefPubMed
26.
go back to reference Regezi JA, Hayward JR, Pickens TN (1978) Superficial melanomas of oral mucous membranes. Oral Surg Oral Med Oral Pathol 5:730–740CrossRef Regezi JA, Hayward JR, Pickens TN (1978) Superficial melanomas of oral mucous membranes. Oral Surg Oral Med Oral Pathol 5:730–740CrossRef
27.
go back to reference Sado Y, Kagawa M, Kishiro Y, Sugihara K, Naito I, Seyer JM, Sugimoto M, Oohashi T, Ninomiya Y (1995) Establishment by the rat lymph node method of epitope-defined monoclonal antibodies recognizing the six different α chains of human type IV collagen. Histochem Cell Biol 104:267–275CrossRefPubMed Sado Y, Kagawa M, Kishiro Y, Sugihara K, Naito I, Seyer JM, Sugimoto M, Oohashi T, Ninomiya Y (1995) Establishment by the rat lymph node method of epitope-defined monoclonal antibodies recognizing the six different α chains of human type IV collagen. Histochem Cell Biol 104:267–275CrossRefPubMed
28.
go back to reference Sado Y, Kagawa M, Naito I, Ueki Y, Seki T, Momota R, Oohashi T, Ninomya Y (1998) Organization and expression of basement membrane collagen IV genes and their roles in human disorders. J Biochem (Tokyo) 15:767–776 Sado Y, Kagawa M, Naito I, Ueki Y, Seki T, Momota R, Oohashi T, Ninomya Y (1998) Organization and expression of basement membrane collagen IV genes and their roles in human disorders. J Biochem (Tokyo) 15:767–776
29.
go back to reference Saito K, Naito I, Seki T, Oohashi T, Kimura E, Momota R, Kishiro Y, Sado Y, Yoshioka H, Ninomiya Y (2000) Differential expression of mouse alpha5(IV) and alpha6(IV) collagen genes in epithelial basement membranes. J Biochem (Tokyo) 3:427–434 Saito K, Naito I, Seki T, Oohashi T, Kimura E, Momota R, Kishiro Y, Sado Y, Yoshioka H, Ninomiya Y (2000) Differential expression of mouse alpha5(IV) and alpha6(IV) collagen genes in epithelial basement membranes. J Biochem (Tokyo) 3:427–434
30.
go back to reference Seki T, Naito I, Oohashi T, Sado Y, Ninomiya Y (1998) Differential expression of type IV collagen isoforms, alpha5(IV) and alpha6(IV) chains, in basement membranes surrounding smooth muscle cells. Histochem Cell Biol 4:359–366CrossRef Seki T, Naito I, Oohashi T, Sado Y, Ninomiya Y (1998) Differential expression of type IV collagen isoforms, alpha5(IV) and alpha6(IV) chains, in basement membranes surrounding smooth muscle cells. Histochem Cell Biol 4:359–366CrossRef
31.
go back to reference Schaumburg-Lever G, Lever I, Fehrenbacher B, Moller H, Bischof B, Kaiserling E, Garbe C, Rassner G (2000) Melanocytes in nevi and melanomas synthesize basement membrane and basement membrane-like material. An immunohistochemical and electron microscopic study including immunoelectron microscopy. J Cutan Pathol 27:67–75CrossRefPubMed Schaumburg-Lever G, Lever I, Fehrenbacher B, Moller H, Bischof B, Kaiserling E, Garbe C, Rassner G (2000) Melanocytes in nevi and melanomas synthesize basement membrane and basement membrane-like material. An immunohistochemical and electron microscopic study including immunoelectron microscopy. J Cutan Pathol 27:67–75CrossRefPubMed
32.
go back to reference Tanaka K, Iyama K, Kitaoka M, Ninomiya Y, Oohashi T, Sado Y, Ono T (1997) Differential expression of alpha 1(IV), alpha 2(IV), alpha 5(IV) and alpha 6(IV) collagen chains in the basement membrane of basal cell carcinoma. Histochem J 29:563–570CrossRefPubMed Tanaka K, Iyama K, Kitaoka M, Ninomiya Y, Oohashi T, Sado Y, Ono T (1997) Differential expression of alpha 1(IV), alpha 2(IV), alpha 5(IV) and alpha 6(IV) collagen chains in the basement membrane of basal cell carcinoma. Histochem J 29:563–570CrossRefPubMed
34.
go back to reference Umeda M, Komatsubara H, Shibuya Y, Yokoo S, Komori T (2002) Premalignant melanocytic dysplasia and malignant melanoma of the oral mucosa. Oral Oncol 7:714–722CrossRef Umeda M, Komatsubara H, Shibuya Y, Yokoo S, Komori T (2002) Premalignant melanocytic dysplasia and malignant melanoma of the oral mucosa. Oral Oncol 7:714–722CrossRef
35.
go back to reference Zheng K, Harvey S, Sado Y, Naito I, Ninomiya Y, Jacobs R, Thorner PS (1999) Absence of the alpha6(IV) chain of collagen type IV in Alport syndrome is related to a failure at the protein assembly level and does not result in diffuse leiomyomatosis. Am J Pathol 6:1883–1891 Zheng K, Harvey S, Sado Y, Naito I, Ninomiya Y, Jacobs R, Thorner PS (1999) Absence of the alpha6(IV) chain of collagen type IV in Alport syndrome is related to a failure at the protein assembly level and does not result in diffuse leiomyomatosis. Am J Pathol 6:1883–1891
Metadata
Title
Immunolocalization and distribution patterns of type IV collagen alpha chains in oral mucosal melanoma
Authors
Hitoshi Nagatsuka
Rosario Santos Rivera
Mehmet Gunduz
You-Jin Lee
Ryo Tamamura
Esra Gunduz
Ichiro Naito
Yoshikazu Sado
Noriyuki Nagai
Publication date
01-10-2005
Publisher
Springer-Verlag
Published in
Virchows Archiv / Issue 4/2005
Print ISSN: 0945-6317
Electronic ISSN: 1432-2307
DOI
https://doi.org/10.1007/s00428-005-0016-1

Other articles of this Issue 4/2005

Virchows Archiv 4/2005 Go to the issue