Skip to main content
Top
Published in: BMC Oral Health 1/2024

Open Access 01-12-2024 | Ameloblastoma | Research

Immunohistochemical expression of SPARC in odontogenic keratocysts: a comparative study with other odontogenic cysts

Authors: Sopee Poomsawat, Sirada Choakdeewanitthumrong, Sirima Sanguansin, Ounruean Meesakul, Theerachai Kosanwat

Published in: BMC Oral Health | Issue 1/2024

Login to get access

Abstract

Background

Secreted protein acidic and rich in cysteine (SPARC) has been shown to modulate aggressive behavior in several benign and malignant tumors. Little is known about SPARC expression in odontogenic keratocyst (OKC), an odontogenic cyst with an aggressive nature. To the best of our knowledge, only one study has been investigated the expression of this protein in OKCs. This study aimed to characterize SPARC expression in OKCs. Additionally, to determine whether SPARC is associated with aggressive behavior in OKCs, SPARC expression in OKCs was compared with radicular cysts (RCs), dentigerous cysts (DCs) and calcifying odontogenic cysts (COCs). These odontogenic cysts showed no or less aggressive behavior.

Methods

SPARC expression was evaluated in 38 OKCs, 39 RCs, 35 DCs and 14 COCs using immunohistochemistry. The percentages of positive cells and the intensities of immunostaining in the epithelial lining and the cystic wall were evaluated and scored.

Results

Generally, OKCs showed similar staining patterns to RCs, DCs and COCs. In the epithelial lining, SPARC was not detected, except for ghost cells in all COCs. In the cystic wall, the majority of positive cells were fibroblasts. Compared between 4 groups of odontogenic cysts, SPARC expression in OKCs was significantly higher than those of RCs (P < 0.001), DCs (P < 0.001) and COCs (P = 0.001).

Conclusions

A significant increase of SPARC expression in OKCs compared with RCs, DCs and COCs suggests that SPARC may play a role in the aggressive behavior of OKCs.
Literature
1.
go back to reference Bornstein P, Sage EH. Matricellular proteins: extracellular modulators of cell function. Curr Opin Cell Biol. 2002;14(5):608–16.CrossRefPubMed Bornstein P, Sage EH. Matricellular proteins: extracellular modulators of cell function. Curr Opin Cell Biol. 2002;14(5):608–16.CrossRefPubMed
2.
go back to reference Brekken RA, Sage EH. SPARC, a matricellular protein: at the crossroads of cell-matrix communication. Matrix Biol. 2001;19(8):816–27.CrossRefPubMed Brekken RA, Sage EH. SPARC, a matricellular protein: at the crossroads of cell-matrix communication. Matrix Biol. 2001;19(8):816–27.CrossRefPubMed
3.
go back to reference Bradshaw AD, Sage EH. SPARC, a matricellular protein that functions in cellular differentiation and tissue response to injury. J Clin Invest. 2001;107(9):1049–54.CrossRefPubMedPubMedCentral Bradshaw AD, Sage EH. SPARC, a matricellular protein that functions in cellular differentiation and tissue response to injury. J Clin Invest. 2001;107(9):1049–54.CrossRefPubMedPubMedCentral
4.
go back to reference Puolakkainen P, Reed M, Vento P, Sage EH, Kiviluoto T, Kivilaakso E. Expression of SPARC (secreted protein, acidic and rich in cysteine) in healing intestinal anastomoses and short bowel syndrome in rats. Dig Dis Sci. 1999;44(8):1554–64.CrossRefPubMed Puolakkainen P, Reed M, Vento P, Sage EH, Kiviluoto T, Kivilaakso E. Expression of SPARC (secreted protein, acidic and rich in cysteine) in healing intestinal anastomoses and short bowel syndrome in rats. Dig Dis Sci. 1999;44(8):1554–64.CrossRefPubMed
5.
go back to reference Clark CJ, Sage EH. A prototypic matricellular protein in the tumor microenvironment–where there’s SPARC, there’s fire. J Cell Biochem. 2008;104(3):721–32.CrossRefPubMed Clark CJ, Sage EH. A prototypic matricellular protein in the tumor microenvironment–where there’s SPARC, there’s fire. J Cell Biochem. 2008;104(3):721–32.CrossRefPubMed
6.
go back to reference Ma G-Y, Shi S, Zhang Y-R, Guo Z-B, Bai W-W, Zhang Z-G. Prognostic significance of SPARC expression in non–small cell lung cancer: a meta–analysis and bioinformatics analysis. Oncol Lett. 2022;24(5):412.CrossRefPubMedPubMedCentral Ma G-Y, Shi S, Zhang Y-R, Guo Z-B, Bai W-W, Zhang Z-G. Prognostic significance of SPARC expression in non–small cell lung cancer: a meta–analysis and bioinformatics analysis. Oncol Lett. 2022;24(5):412.CrossRefPubMedPubMedCentral
7.
go back to reference Alcaraz LB, Mallavialle A, Mollevi C, Boissière-Michot F, Mansouri H, Simony-Lafontaine J, et al. SPARC in cancer-associated fibroblasts is an independent poor prognostic factor in non-metastatic triple-negative breast cancer and exhibits pro-tumor activity. Int J Cancer. 2023;152(6):1243–58.CrossRefPubMed Alcaraz LB, Mallavialle A, Mollevi C, Boissière-Michot F, Mansouri H, Simony-Lafontaine J, et al. SPARC in cancer-associated fibroblasts is an independent poor prognostic factor in non-metastatic triple-negative breast cancer and exhibits pro-tumor activity. Int J Cancer. 2023;152(6):1243–58.CrossRefPubMed
8.
go back to reference Drev D, Harpain F, Beer A, Stift A, Gruber ES, Klimpfinger M et al. Impact of fibroblast-derived SPARC on invasiveness of colorectal cancer cells. Cancers (Basel). 2019;11(10). Drev D, Harpain F, Beer A, Stift A, Gruber ES, Klimpfinger M et al. Impact of fibroblast-derived SPARC on invasiveness of colorectal cancer cells. Cancers (Basel). 2019;11(10).
9.
go back to reference Poomsawat S, Kosanwat T, Meesakul O, Sanguansin S. Epithelial and fibroblast SPARC expression patterns in oral leukoplakia and oral squamous cell carcinoma. Oral Surg Oral Med Oral Pathol Oral Radiol. 2022;134(2):e44–e50.CrossRefPubMed Poomsawat S, Kosanwat T, Meesakul O, Sanguansin S. Epithelial and fibroblast SPARC expression patterns in oral leukoplakia and oral squamous cell carcinoma. Oral Surg Oral Med Oral Pathol Oral Radiol. 2022;134(2):e44–e50.CrossRefPubMed
10.
go back to reference Soluk-Tekkeşin M, Wright JM. The World Health Organization Classification of odontogenic lesions: A summary of the changes of the 2017 (4th) Edition. Turk Patoloji Derg. 2018;34(1). Soluk-Tekkeşin M, Wright JM. The World Health Organization Classification of odontogenic lesions: A summary of the changes of the 2017 (4th) Edition. Turk Patoloji Derg. 2018;34(1).
11.
go back to reference Shen LC, Chen YK, Hsue SS, Shaw SY. Expression of osteonectin/secreted protein acidic and rich in cysteine and matrix metalloproteinases in ameloblastoma. J Oral Pathol Med. 2010;39(3):242–9.CrossRefPubMed Shen LC, Chen YK, Hsue SS, Shaw SY. Expression of osteonectin/secreted protein acidic and rich in cysteine and matrix metalloproteinases in ameloblastoma. J Oral Pathol Med. 2010;39(3):242–9.CrossRefPubMed
12.
go back to reference Indirapriyadarsini K, Raghunath V, Naidu BV, Ramakrishna BB, Tangudu A, Lokesh KV. Immunohistochemical expression of osteonectin, matrix metalloproteinases-9 and Ki-67 in ameloblastoma. J Oral Maxillofac Pathol. 2018;22(3):446.CrossRefPubMedPubMedCentral Indirapriyadarsini K, Raghunath V, Naidu BV, Ramakrishna BB, Tangudu A, Lokesh KV. Immunohistochemical expression of osteonectin, matrix metalloproteinases-9 and Ki-67 in ameloblastoma. J Oral Maxillofac Pathol. 2018;22(3):446.CrossRefPubMedPubMedCentral
13.
go back to reference Slusarenko da Silva Y, Stoelinga PJW, Grillo R. Da Graça Naclério-Homem M. Cyst or Tumor? A systematic review and meta-analysis on the expression of p53 marker in odontogenic keratocysts. J Craniomaxillofac Surg. 2021;49(12):1101–6.CrossRefPubMed Slusarenko da Silva Y, Stoelinga PJW, Grillo R. Da Graça Naclério-Homem M. Cyst or Tumor? A systematic review and meta-analysis on the expression of p53 marker in odontogenic keratocysts. J Craniomaxillofac Surg. 2021;49(12):1101–6.CrossRefPubMed
14.
go back to reference Titinchi F. Protocol for management of odontogenic keratocysts considering recurrence according to treatment methods. J Korean Assoc Oral Maxillofac Surg. 2020;46(5):358–60.CrossRefPubMedPubMedCentral Titinchi F. Protocol for management of odontogenic keratocysts considering recurrence according to treatment methods. J Korean Assoc Oral Maxillofac Surg. 2020;46(5):358–60.CrossRefPubMedPubMedCentral
15.
go back to reference Hong Y, Zhang J, Zhang H, Li X, Qu J, Zhai J, et al. Heterozygous PTCH1 mutations impact the bone metabolism in patients with nevoid basal cell Carcinoma Syndrome likely by regulating SPARC expression. J Bone Min Res. 2016;31(7):1413–28.CrossRef Hong Y, Zhang J, Zhang H, Li X, Qu J, Zhai J, et al. Heterozygous PTCH1 mutations impact the bone metabolism in patients with nevoid basal cell Carcinoma Syndrome likely by regulating SPARC expression. J Bone Min Res. 2016;31(7):1413–28.CrossRef
16.
go back to reference Nel C, Robinson L, Roza A, Vargas PA, Nortjé CJ, van Heerden WF. Calcifying odontogenic cysts: a 20-year retrospective clinical and radiological review. Dentomaxillofac Radiol. 2021;50(6):20200586.CrossRefPubMedPubMedCentral Nel C, Robinson L, Roza A, Vargas PA, Nortjé CJ, van Heerden WF. Calcifying odontogenic cysts: a 20-year retrospective clinical and radiological review. Dentomaxillofac Radiol. 2021;50(6):20200586.CrossRefPubMedPubMedCentral
17.
go back to reference Takata T, Zhao M, Nikai H, Uchida T, Wang T. Ghost cells in calcifying odontogenic cyst express enamel-related proteins. Histochem J. 2000;32(4):223–9.CrossRefPubMed Takata T, Zhao M, Nikai H, Uchida T, Wang T. Ghost cells in calcifying odontogenic cyst express enamel-related proteins. Histochem J. 2000;32(4):223–9.CrossRefPubMed
18.
go back to reference Poomsawat S, Punyasingh J, Vejchapipat P. Expression of basement membrane components in odontogenic tumors. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2007;104(5):666–75.CrossRefPubMed Poomsawat S, Punyasingh J, Vejchapipat P. Expression of basement membrane components in odontogenic tumors. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2007;104(5):666–75.CrossRefPubMed
20.
go back to reference Gilles C, Bassuk JA, Pulyaeva H, Sage EH, Foidart JM, Thompson EW. SPARC/osteonectin induces matrix metalloproteinase 2 activation in human breast cancer cell lines. Cancer Res. 1998;58(23):5529–36.PubMed Gilles C, Bassuk JA, Pulyaeva H, Sage EH, Foidart JM, Thompson EW. SPARC/osteonectin induces matrix metalloproteinase 2 activation in human breast cancer cell lines. Cancer Res. 1998;58(23):5529–36.PubMed
21.
go back to reference Jacob K, Webber M, Benayahu D, Kleinman HK. Osteonectin promotes prostate cancer cell migration and invasion: a possible mechanism for metastasis to bone. Cancer Res. 1999;59(17):4453–7.PubMed Jacob K, Webber M, Benayahu D, Kleinman HK. Osteonectin promotes prostate cancer cell migration and invasion: a possible mechanism for metastasis to bone. Cancer Res. 1999;59(17):4453–7.PubMed
22.
go back to reference Lu M, Rabie AB. Matrix metalloproteinase-9 regulates graft bone resorption. Angle Orthod. 2006;76(4):598–604.PubMed Lu M, Rabie AB. Matrix metalloproteinase-9 regulates graft bone resorption. Angle Orthod. 2006;76(4):598–604.PubMed
23.
go back to reference Bigg HF, Rowan AD, Barker MD, Cawston TE. Activity of matrix metalloproteinase-9 against native collagen types I and III. FEBS J. 2007;274(5):1246–55.CrossRefPubMed Bigg HF, Rowan AD, Barker MD, Cawston TE. Activity of matrix metalloproteinase-9 against native collagen types I and III. FEBS J. 2007;274(5):1246–55.CrossRefPubMed
24.
go back to reference Nyman JS, Lynch CC, Perrien DS, Thiolloy S, O’Quinn EC, Patil CA, et al. Differential effects between the loss of MMP-2 and MMP-9 on structural and tissue-level properties of bone. J Bone Min Res. 2011;26(6):1252–60.CrossRef Nyman JS, Lynch CC, Perrien DS, Thiolloy S, O’Quinn EC, Patil CA, et al. Differential effects between the loss of MMP-2 and MMP-9 on structural and tissue-level properties of bone. J Bone Min Res. 2011;26(6):1252–60.CrossRef
25.
go back to reference Yardley DA. Nab-Paclitaxel mechanisms of action and delivery. J Control Release. 2013;170(3):365–72.CrossRefPubMed Yardley DA. Nab-Paclitaxel mechanisms of action and delivery. J Control Release. 2013;170(3):365–72.CrossRefPubMed
26.
go back to reference Nian Q, Li J, Han Z, Liang Q, Liu M, Yang C, et al. SPARC in hematologic malignancies and novel technique for hematological disease with its abnormal expression. Biomed Pharmacother. 2022;153:113519.CrossRefPubMed Nian Q, Li J, Han Z, Liang Q, Liu M, Yang C, et al. SPARC in hematologic malignancies and novel technique for hematological disease with its abnormal expression. Biomed Pharmacother. 2022;153:113519.CrossRefPubMed
27.
go back to reference Desai N, Trieu V, Damascelli B, Soon-Shiong P. SPARC expression correlates with tumor response to albumin-bound Paclitaxel in head and neck cancer patients. Transl Oncol. 2009;2(2):59–64.CrossRefPubMedPubMedCentral Desai N, Trieu V, Damascelli B, Soon-Shiong P. SPARC expression correlates with tumor response to albumin-bound Paclitaxel in head and neck cancer patients. Transl Oncol. 2009;2(2):59–64.CrossRefPubMedPubMedCentral
Metadata
Title
Immunohistochemical expression of SPARC in odontogenic keratocysts: a comparative study with other odontogenic cysts
Authors
Sopee Poomsawat
Sirada Choakdeewanitthumrong
Sirima Sanguansin
Ounruean Meesakul
Theerachai Kosanwat
Publication date
01-12-2024
Publisher
BioMed Central
Published in
BMC Oral Health / Issue 1/2024
Electronic ISSN: 1472-6831
DOI
https://doi.org/10.1186/s12903-024-03978-4

Other articles of this Issue 1/2024

BMC Oral Health 1/2024 Go to the issue