Skip to main content
Top
Published in: Tumor Biology 7/2015

Open Access 01-07-2015 | Research Article

Expression of colony-stimulating factor 1 is associated with occurrence of osteochondral change in pigmented villonodular synovitis

Authors: Takehiro Ota, Hiroshi Urakawa, Eiji Kozawa, Kunihiro Ikuta, Shunsuke Hamada, Satoshi Tsukushi, Yoshie Shimoyama, Naoki Ishiguro, Yoshihiro Nishida

Published in: Tumor Biology | Issue 7/2015

Login to get access

Abstract

Pigmented villonodular synovitis (PVNS) is a benign, translocation-derived neoplasm. Because of its high local recurrence rate after surgery and occurrence of osteochondral destruction, a novel therapeutic target is required. The present study aimed to evaluate the significance of protein expression possibly associated with the pathogenesis during the clinical course of PVNS. In 40 cases of PVNS, positivity of colony-stimulated factor 1 (CSF1), its receptor (CSF1R), and receptor activator of nuclear factor kappa-B ligand (RANKL) were immunohistochemically determined. The relationship between the positivity and clinical outcomes was investigated. High positivity of CSF1 staining intensity was associated with an increased incidence of osteochondral lesions (bone erosion and osteoarthritis) (p = 0.009), but not with the rate of local recurrence. Positivity of CSF1R and RANKL staining was not associated with any clinical variables. The number of giant cells was not correlated with positivity of any of the three proteins, or with the clinical outcome. Focusing on knee cases, CSF1 positivity was also associated with the incidence of osteochondal change (p = 0.02). CSF1R positivity was high in cases which had local recurrence, but not significantly so (p = 0.129). Determination of CSF1 and CSF1R expression may be useful as a prognosticator of the clinical course and/or outcomes of PVNS.
Literature
1.
go back to reference Jaffe H, Lichtenstein L, Sutro C. Pigmented villonodular synovitis, bursitis and tenosynovitis. Arch Pathol. 1941;31:731–65. Jaffe H, Lichtenstein L, Sutro C. Pigmented villonodular synovitis, bursitis and tenosynovitis. Arch Pathol. 1941;31:731–65.
2.
go back to reference Geldyyev A, Koleganova N, Piecha G, Sueltmann H, Finis K, Ruschaupt M, et al. High expression level of bone degrading proteins as a possible inducer of osteolytic features in pigmented villonodular synovitis. Cancer Lett. 2007;255:275–83.CrossRefPubMed Geldyyev A, Koleganova N, Piecha G, Sueltmann H, Finis K, Ruschaupt M, et al. High expression level of bone degrading proteins as a possible inducer of osteolytic features in pigmented villonodular synovitis. Cancer Lett. 2007;255:275–83.CrossRefPubMed
3.
go back to reference Nishida Y, Tsukushi S, Nakashima H, Sugiura H, Yamada Y, Urakawa H, et al. Osteochondral destruction in pigmented villonodular synovitis during the clinical course. J Rheumatol. 2012;39:345–51.CrossRefPubMed Nishida Y, Tsukushi S, Nakashima H, Sugiura H, Yamada Y, Urakawa H, et al. Osteochondral destruction in pigmented villonodular synovitis during the clinical course. J Rheumatol. 2012;39:345–51.CrossRefPubMed
4.
go back to reference Ravi V, Wang W-L, Lewis VO. Treatment of tenosynovial giant cell tumor and pigmented villonodular synovitis. Curr Opin Oncol. 2011;23:361–6.CrossRefPubMed Ravi V, Wang W-L, Lewis VO. Treatment of tenosynovial giant cell tumor and pigmented villonodular synovitis. Curr Opin Oncol. 2011;23:361–6.CrossRefPubMed
5.
go back to reference Yoshida W, Uzuki M, Kurose A, Yoshida M, Nishida J, Shimamura T, et al. Cell characterization of mononuclear and giant cells constituting pigmented villonodular synovitis. Hum Pathol. 2003;34:65–73.CrossRefPubMed Yoshida W, Uzuki M, Kurose A, Yoshida M, Nishida J, Shimamura T, et al. Cell characterization of mononuclear and giant cells constituting pigmented villonodular synovitis. Hum Pathol. 2003;34:65–73.CrossRefPubMed
6.
go back to reference Vogrincic GS, O’Connell JX, Gilks CB. Giant cell tumor of tendon sheath is a polyclonal cellular proliferation. Hum Pathol. 1997;28:815–9.CrossRefPubMed Vogrincic GS, O’Connell JX, Gilks CB. Giant cell tumor of tendon sheath is a polyclonal cellular proliferation. Hum Pathol. 1997;28:815–9.CrossRefPubMed
7.
go back to reference Sciot R, Rosai J, Dal Cin P, de Wever I, Fletcher CD, Mandahl N, et al. Analysis of 35 cases of localized and diffuse tenosynovial giant cell tumor: a report from the Chromosomes and Morphology (CHAMP) study group. Mod Pathol. 1999;12:576–9.PubMed Sciot R, Rosai J, Dal Cin P, de Wever I, Fletcher CD, Mandahl N, et al. Analysis of 35 cases of localized and diffuse tenosynovial giant cell tumor: a report from the Chromosomes and Morphology (CHAMP) study group. Mod Pathol. 1999;12:576–9.PubMed
8.
go back to reference Nilsson M, Höglund M, Panagopoulos I, Sciot R, Dal Cin P, Debiec-Rychter M, et al. Molecular cytogenetic mapping of recurrent chromosomal breakpoints in tenosynovial giant cell tumors. Virchows Arch. 2002;441:475–80.CrossRefPubMed Nilsson M, Höglund M, Panagopoulos I, Sciot R, Dal Cin P, Debiec-Rychter M, et al. Molecular cytogenetic mapping of recurrent chromosomal breakpoints in tenosynovial giant cell tumors. Virchows Arch. 2002;441:475–80.CrossRefPubMed
9.
go back to reference Möller E, Mandahl N, Mertens F, Panagopoulos I. Molecular identification of COL6A3-CSF1 fusion transcripts in tenosynovial giant cell tumors. Gene Chrom Cancer. 2008;47:21–5.CrossRef Möller E, Mandahl N, Mertens F, Panagopoulos I. Molecular identification of COL6A3-CSF1 fusion transcripts in tenosynovial giant cell tumors. Gene Chrom Cancer. 2008;47:21–5.CrossRef
10.
go back to reference West RB, Rubin BP, Miller MA, Subramanian S, Kaygusuz G, Montgomery K, et al. A landscape effect in tenosynovial giant-cell tumor from activation of CSF1 expression by a translocation in a minority of tumor cells. Proc Natl Acad Sci U S A. 2006;103:690–5.CrossRefPubMedPubMedCentral West RB, Rubin BP, Miller MA, Subramanian S, Kaygusuz G, Montgomery K, et al. A landscape effect in tenosynovial giant-cell tumor from activation of CSF1 expression by a translocation in a minority of tumor cells. Proc Natl Acad Sci U S A. 2006;103:690–5.CrossRefPubMedPubMedCentral
11.
go back to reference Molena B, Sfriso P, Oliviero F, Pagnin E, Teramo A, Lunardi F, et al. Synovial colony-stimulating factor-1 mRNA expression in diffuse pigmented villonodular synovitis. Clin Exp Rheumatol. 2011;29:547–50.PubMed Molena B, Sfriso P, Oliviero F, Pagnin E, Teramo A, Lunardi F, et al. Synovial colony-stimulating factor-1 mRNA expression in diffuse pigmented villonodular synovitis. Clin Exp Rheumatol. 2011;29:547–50.PubMed
12.
go back to reference Cupp JS, Miller MA, Montgomery KD, Nielsen TO, O’Connell JX, Huntsman D, et al. Translocation and expression of CSF1 in pigmented villonodular synovitis, tenosynovial giant cell tumor, rheumatoid arthritis and other reactive synovitides. Am J Surg Pathol. 2007;31:970–6.CrossRefPubMed Cupp JS, Miller MA, Montgomery KD, Nielsen TO, O’Connell JX, Huntsman D, et al. Translocation and expression of CSF1 in pigmented villonodular synovitis, tenosynovial giant cell tumor, rheumatoid arthritis and other reactive synovitides. Am J Surg Pathol. 2007;31:970–6.CrossRefPubMed
13.
go back to reference Nakano K, Okada Y, Saito K, Tanikawa R, Sawamukai N, Sasaguri Y, et al. Rheumatoid synovial endothelial cells produce macrophage colony-stimulating factor leading to osteoclastogenesis in rheumatoid arthritis. Rheumatology (Oxford). 2007;46:597–603.CrossRef Nakano K, Okada Y, Saito K, Tanikawa R, Sawamukai N, Sasaguri Y, et al. Rheumatoid synovial endothelial cells produce macrophage colony-stimulating factor leading to osteoclastogenesis in rheumatoid arthritis. Rheumatology (Oxford). 2007;46:597–603.CrossRef
14.
go back to reference Taylor R, Kashima TG, Knowles H, Gibbons CLMH, Whitwell D, Athanasou NA. Osteoclast formation and function in pigmented villonodular synovitis. J Pathol. 2011;225:151–6.CrossRefPubMed Taylor R, Kashima TG, Knowles H, Gibbons CLMH, Whitwell D, Athanasou NA. Osteoclast formation and function in pigmented villonodular synovitis. J Pathol. 2011;225:151–6.CrossRefPubMed
15.
go back to reference Sarma U, Flanagan AM. Macrophage colony-stimulating factor induces substantial osteoclast generation and bone resorption in human bone marrow cultures. Blood. 1996;88:2531–40.PubMed Sarma U, Flanagan AM. Macrophage colony-stimulating factor induces substantial osteoclast generation and bone resorption in human bone marrow cultures. Blood. 1996;88:2531–40.PubMed
16.
go back to reference Ma X, Shi G, Xia C, Liu H, He J, Jin W. Pigmented villonodular synovitis: a retrospective study of seventy five cases (eighty one joints). Int Orthop. 2013;37:1165–70.CrossRefPubMedPubMedCentral Ma X, Shi G, Xia C, Liu H, He J, Jin W. Pigmented villonodular synovitis: a retrospective study of seventy five cases (eighty one joints). Int Orthop. 2013;37:1165–70.CrossRefPubMedPubMedCentral
17.
go back to reference Aurégan J-C, Klouche S, Bohu Y, Lefèvre N, Herman S, Hardy P. Treatment of pigmented villonodular synovitis of the knee. Arthroscopy. 2014;30(10):1327–41.CrossRefPubMed Aurégan J-C, Klouche S, Bohu Y, Lefèvre N, Herman S, Hardy P. Treatment of pigmented villonodular synovitis of the knee. Arthroscopy. 2014;30(10):1327–41.CrossRefPubMed
18.
go back to reference Uchibori M, Nishida Y, Tabata I, Sugiura H, Nakashima H, Yamada Y, et al. Expression of matrix metalloproteinases and tissue inhibitors of metalloproteinases in pigmented villonodular synovitis suggests their potential role for joint destruction. J Rheumatol. 2004;31:110–9.PubMed Uchibori M, Nishida Y, Tabata I, Sugiura H, Nakashima H, Yamada Y, et al. Expression of matrix metalloproteinases and tissue inhibitors of metalloproteinases in pigmented villonodular synovitis suggests their potential role for joint destruction. J Rheumatol. 2004;31:110–9.PubMed
19.
go back to reference O’Keefe RJ, Rosier RN, Teot LA, Stewart JM, Hicks DG. Cytokine and matrix metalloproteinase expression in pigmented villonodular synovitis may mediate bone and cartilage destruction. Iowa Orthop J. 1998;18:26–34.PubMedPubMedCentral O’Keefe RJ, Rosier RN, Teot LA, Stewart JM, Hicks DG. Cytokine and matrix metalloproteinase expression in pigmented villonodular synovitis may mediate bone and cartilage destruction. Iowa Orthop J. 1998;18:26–34.PubMedPubMedCentral
20.
go back to reference Weckauf H, Helmchen B, Hinz U, Meyer-Scholten C, Aulmann S, Otto HF, et al. Expression of cell cycle-related gene products in different forms of primary versus recurrent PVNS. Cancer Lett. 2004;210:111–8.CrossRefPubMed Weckauf H, Helmchen B, Hinz U, Meyer-Scholten C, Aulmann S, Otto HF, et al. Expression of cell cycle-related gene products in different forms of primary versus recurrent PVNS. Cancer Lett. 2004;210:111–8.CrossRefPubMed
21.
go back to reference Avnet S, Salerno M, Zini N, Alberghini M, Gibellini D, Baldini N. Sustained autocrine induction and impaired negative feedback of osteoclastogenesis in CD14(+) cells of giant cell tumor of bone. Am J Pathol. 2013;182:1357–66.CrossRefPubMed Avnet S, Salerno M, Zini N, Alberghini M, Gibellini D, Baldini N. Sustained autocrine induction and impaired negative feedback of osteoclastogenesis in CD14(+) cells of giant cell tumor of bone. Am J Pathol. 2013;182:1357–66.CrossRefPubMed
22.
go back to reference Chin KR, Barr SJ, Winalski C, Zurakowski D, Brick GW. Treatment of advanced primary and recurrent diffuse pigmented villonodular synovitis of the knee. J Bone Joint Surg Am. 2002;84-A:2192–202.CrossRefPubMed Chin KR, Barr SJ, Winalski C, Zurakowski D, Brick GW. Treatment of advanced primary and recurrent diffuse pigmented villonodular synovitis of the knee. J Bone Joint Surg Am. 2002;84-A:2192–202.CrossRefPubMed
23.
go back to reference Cheng H, Clarkson PW, Gao D, Pacheco M, Wang Y, Nielsen TO. Therapeutic antibodies targeting CSF1 impede macrophage recruitment in a xenograft model of tenosynovial giant cell tumor. Sarcoma. 2010;2010:174528.CrossRefPubMedPubMedCentral Cheng H, Clarkson PW, Gao D, Pacheco M, Wang Y, Nielsen TO. Therapeutic antibodies targeting CSF1 impede macrophage recruitment in a xenograft model of tenosynovial giant cell tumor. Sarcoma. 2010;2010:174528.CrossRefPubMedPubMedCentral
24.
go back to reference Stacchiotti S, Crippa F, Messina A, Pilotti S, Gronchi A, Blay JY, et al. Response to imatinib in villonodular pigmented synovitis (PVNS) resistant to nilotinib. Clin Sarcoma Res. 2013;3:8.CrossRefPubMedPubMedCentral Stacchiotti S, Crippa F, Messina A, Pilotti S, Gronchi A, Blay JY, et al. Response to imatinib in villonodular pigmented synovitis (PVNS) resistant to nilotinib. Clin Sarcoma Res. 2013;3:8.CrossRefPubMedPubMedCentral
25.
go back to reference Dewar AL, Cambareri AC, Zannettino ACW, Miller BL, Doherty KV, Hughes TP, et al. Macrophage colony-stimulating factor receptor c-fms is a novel target of imatinib. Blood. 2005;105:3127–32.CrossRefPubMed Dewar AL, Cambareri AC, Zannettino ACW, Miller BL, Doherty KV, Hughes TP, et al. Macrophage colony-stimulating factor receptor c-fms is a novel target of imatinib. Blood. 2005;105:3127–32.CrossRefPubMed
26.
go back to reference Blay J-Y, El Sayadi H, Thiesse P, Garret J, Ray-Coquard I. Complete response to imatinib in relapsing pigmented villonodular synovitis/tenosynovial giant cell tumor (PVNS/TGCT). Ann Oncol. 2008;19:821–2.CrossRefPubMed Blay J-Y, El Sayadi H, Thiesse P, Garret J, Ray-Coquard I. Complete response to imatinib in relapsing pigmented villonodular synovitis/tenosynovial giant cell tumor (PVNS/TGCT). Ann Oncol. 2008;19:821–2.CrossRefPubMed
27.
go back to reference Cassier PA, Gelderblom H, Stacchiotti S, Thomas D, Maki RG, Kroep JR, et al. Efficacy of imatinib mesylate for the treatment of locally advanced and/or metastatic tenosynovial giant cell tumor/pigmented villonodular synovitis. Cancer. 2012;118:1649–55.CrossRefPubMed Cassier PA, Gelderblom H, Stacchiotti S, Thomas D, Maki RG, Kroep JR, et al. Efficacy of imatinib mesylate for the treatment of locally advanced and/or metastatic tenosynovial giant cell tumor/pigmented villonodular synovitis. Cancer. 2012;118:1649–55.CrossRefPubMed
Metadata
Title
Expression of colony-stimulating factor 1 is associated with occurrence of osteochondral change in pigmented villonodular synovitis
Authors
Takehiro Ota
Hiroshi Urakawa
Eiji Kozawa
Kunihiro Ikuta
Shunsuke Hamada
Satoshi Tsukushi
Yoshie Shimoyama
Naoki Ishiguro
Yoshihiro Nishida
Publication date
01-07-2015
Publisher
Springer Netherlands
Published in
Tumor Biology / Issue 7/2015
Print ISSN: 1010-4283
Electronic ISSN: 1423-0380
DOI
https://doi.org/10.1007/s13277-015-3197-5

Other articles of this Issue 7/2015

Tumor Biology 7/2015 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine