Abstract
Matrix proteins are considered to be essential for biomineralization and to be important factors in cranioharyngioma calcification. Osteopontin (OPN) is a noncollagenous, acidic bone-matrix glycoprotein, which binds tightly to hydroxyapatite and appears to form an integral part of the mineralized matrix, probably important to the integrity of cell–matrix interactions. OPN is also a ligand for a cell membrane receptor, CD44v6, which is required for efficient OPN binding. To investigate the role of OPN in craniopharyngioma calcification formation, we studied the involvement of OPN and CD44v6 in craniopharyngiomas. Immunohistochemical staining was used in human craniopharyngiomas to detect the relationship of OPN and degree of calcification, and immunogold localization of OPN was done to identify cell secretory granules. OPN expression was elevated in calcification craniopharyngioma samples. Immunohistochemical staining demonstrated that the OPN expression level was significantly correlated with the degree of calcification (χ2 = 29.987, P < 0.001); meanwhile, immunoelectron microscopy revealed subcellular sites of OPN presenting in epithelial cells, suggesting that the OPN protein is probably synthesized and secreted by stellate reticulum-like cells and ameloblast-like cells. At the same time, OPN expression was paralleled by cell surface reactivity for CD44v6, an OPN functional receptor. These results suggest that OPN is possibly involved as a core protein in the formation of craniopharyngioma calcification.
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Bunin GR, Surawicz TS, Witman PA, Preston-Martin S, Davis F, Bruner JM (1998) The descriptive epidemiology of craniopharyngioma. J Neurosurg 89:547–551
Garnett MR, Puget S, Grill J, Sainte-Rose C (2007) Craniopharyngioma. Orphanet J Rare Dis 2:18
Rekate HL (2005) Craniopharyngioma. J Neurosurg 103:297–298 discussion 298
Wisoff JH (2008) Craniopharyngioma. J Neurosurg Pediatr 1:124–125 discussion 125
Crotty TB, Scheithauer BW, Young WF Jr, Davis DH, Shaw EG, Miller GM, Burger PC (1995) Papillary craniopharyngioma: a clinicopathological study of 48 cases. J Neurosurg 83:206–214
Eldevik OP, Blaivas M, Gabrielsen TO, Hald JK, Chandler WF (1996) Craniopharyngioma: radiologic and histologic findings and recurrence. AJNR Am J Neuroradiol 17:1427–1439
Fisher PG, Jenab J, Gopldthwaite PT, Tihan T, Wharam MD, Foer DR, Burger PC (1998) Outcomes and failure patterns in childhood craniopharyngiomas. Childs Nerv Syst 14:558–563
Miller DC (1994) Pathology of craniopharyngiomas: clinical import of pathological findings. Pediatr Neurosurg 21(Suppl 1):11–17
Tsuda M, Takahashi S, Higano S, Kurihara N, Ikeda H, Sakamoto K (1997) CT and MR imaging of craniopharyngioma. Eur Radiol 7:464–469
Sato K, Kubota T (1999) Fine structure of ossification in craniopharyngiomas. Ultrastruct Pathol 23:395–399
Sato K, Kubota T, Yamamoto S, Ishikura A (1986) An ultrastructural study of mineralization in craniopharyngiomas. J Neuropathol Exp Neurol 45:463–470
Vilches J, Lopez A, Martinez MC, Gomez J, Barbera J (1981) Scanning and transmission electron microscopy of a craniopharyngioma: x-ray microanalytical study of the intratumoral mineralized deposits. Ultrastruct Pathol 2:343–356
Yoshimoto M, de Toledo SR, da Silva NS, Bayani J, Bertozzi AP, Stavale JN, Cavalheiro S, Andrade JA, Zielenska M, Squire JA (2004) Comparative genomic hybridization analysis of pediatric adamantinomatous craniopharyngiomas and a review of the literature. J Neurosurg 101:85–90
Diao H, Kon S, Iwabuchi K, Kimura C, Morimoto J, Ito D, Segawa T, Maeda M, Hamuro J, Nakayama T, Taniguchi M, Yagita H, Van Kaer L, Onoe K, Denhardt D, Rittling S, Uede T (2004) Osteopontin as a mediator of NKT cell function in T cell-mediated liver diseases. Immunity 21:539–550
Furger KA, Menon RK, Tuck AB, Bramwell VH, Chambers AF (2001) The functional and clinical roles of osteopontin in cancer and metastasis. Curr Mol Med 1:621–632
Haylock DN, Nilsson SK (2006) Osteopontin: a bridge between bone and blood. Br J Haematol 134:467–474
O’Regan A, Berman JS (2000) Osteopontin: a key cytokine in cell-mediated and granulomatous inflammation. Int J Exp Pathol 81:373–390
Prince CW, Butler WT (1987) 1, 25-Dihydroxyvitamin D3 regulates the biosynthesis of osteopontin, a bone-derived cell attachment protein, in clonal osteoblast-like osteosarcoma cells. Coll Relat Res 7:305–313
Rangaswami H, Bulbule A, Kundu GC (2006) Osteopontin: role in cell signaling and cancer progression. Trends Cell Biol 16:79–87
Shinohara ML, Jansson M, Hwang ES, Werneck MB, Glimcher LH, Cantor H (2005) T-bet-dependent expression of osteopontin contributes to T cell polarization. Proc Natl Acad Sci USA 102:17101–17106
Shinohara ML, Lu L, Bu J, Werneck MB, Kobayashi KS, Glimcher LH, Cantor H (2006) Osteopontin expression is essential for interferon-alpha production by plasmacytoid dendritic cells. Nat Immunol 7:498–506
Weber GF (2001) The metastasis gene osteopontin: a candidate target for cancer therapy. Biochim Biophys Acta 1552:61–85
Brown LF, Berse B, Van de Water L, Papadopoulos-Sergiou A, Perruzzi CA, Manseau EJ, Dvorak HF, Senger DR (1992) Expression and distribution of osteopontin in human tissues: widespread association with luminal epithelial surfaces. Mol Biol Cell 3:1169–1180
Chen Y, Bal BS, Gorski JP (1992) Calcium and collagen binding properties of osteopontin, bone sialoprotein, and bone acidic glycoprotein-75 from bone. J Biol Chem 267:24871–24878
Rittling SR, Chambers AF (2004) Role of osteopontin in tumour progression. Br J Cancer 90:1877–1881
Weber GF, Ashkar S, Cantor H (1997) Interaction between CD44 and osteopontin as a potential basis for metastasis formation. Proc Assoc Am Physicians 109:1–9
Ponta H, Sherman L, Herrlich PA (2003) CD44: from adhesion molecules to signalling regulators. Nat Rev Mol Cell Biol 4:33–45
Ermak G, Gerasimov G, Troshina K, Jennings T, Robinson L, Ross JS, Figge J (1995) Deregulated alternative splicing of CD44 messenger RNA transcripts in neoplastic and nonneoplastic lesions of the human thyroid. Cancer Res 55:4594–4598
Ermak G, Jennings T, Robinson L, Ross JS, Figge J (1996) Restricted patterns of CD44 variant exon expression in human papillary thyroid carcinoma. Cancer Res 56:1037–1042
Chhieng DC, Ross JS, McKenna BJ (1997) CD44 immunostaining of thyroid fine-needle aspirates differentiates thyroid papillary carcinoma from other lesions with nuclear grooves and inclusions. Cancer 81:157–162
Lee JL, Wang MJ, Sudhir PR, Chen GD, Chi CW, Chen JY (2007) Osteopontin promotes integrin activation through outside-in and inside-out mechanisms: OPN-CD44V interaction enhances survival in gastrointestinal cancer cells. Cancer Res 67:2089–2097
Matsubara A, Laake JH, Davanger S, Usami S, Ottersen OP (1996) Organization of AMPA receptor subunits at a glutamate synapse: a quantitative immunogold analysis of hair cell synapses in the rat organ of Corti. J Neurosci 16:4457–4467
Akagi T, Ishida K, Hanasaka T, Hayashi S, Watanabe M, Hashikawa T, Tohyama K (2006) Improved methods for ultracryotomy of CNS tissue for ultrastructural and immunogold analyses. J Neurosci Methods 153:276–282
Senger DR, Perruzzi CA, Gracey CF, Papadopoulos A, Tenen DG (1988) Secreted phosphoproteins associated with neoplastic transformation: close homology with plasma proteins cleaved during blood coagulation. Cancer Res 48:5770–5774
Franzen A, Heinegard D (1985) Isolation and characterization of two sialoproteins present only in bone calcified matrix. Biochem J 232:715–724
Nagata T, Bellows CG, Kasugai S, Butler WT, Sodek J (1991) Biosynthesis of bone proteins [SPP-1 (secreted phosphoprotein-1, osteopontin), BSP (bone sialoprotein) and SPARC (osteonectin)] in association with mineralized-tissue formation by fetal-rat calvarial cells in culture. Biochem J 274(Pt 2):513–520
Nagata T, Yokota M, Ohishi K, Nishikawa S, Shinohara H, Wakano Y, Ishida H (1994) 1 alpha, 25-dihydroxyvitamin D3 stimulation of osteopontin expression in rat clonal dental pulp cells. Arch Oral Biol 39:775–782
Mohler ER III, Adam LP, McClelland P, Graham L, Hathaway DR (1997) Detection of osteopontin in calcified human aortic valves. Arterioscler Thromb Vasc Biol 17:547–552
Steitz SA, Speer MY, McKee MD, Liaw L, Almeida M, Yang H, Giachelli CM (2002) Osteopontin inhibits mineral deposition and promotes regression of ectopic calcification. Am J Pathol 161:2035–2046
Heinegard D, Andersson G, Reinholt FP (1995) Roles of osteopontin in bone remodeling. Ann N Y Acad Sci 760:213–222
Miyauchi A, Alvarez J, Greenfield EM, Teti A, Grano M, Colucci S, Zambonin-Zallone A, Ross FP, Teitelbaum SL, Cheresh D et al (1993) Binding of osteopontin to the osteoclast integrin alpha v beta 3. Osteoporos Int 3(Suppl 1):132–135
Denhardt DT, Noda M (1998) Osteopontin expression and function: role in bone remodeling. J Cell Biochem (Suppl 30–31):92–102
Wada T, McKee MD, Steitz S, Giachelli CM (1999) Calcification of vascular smooth muscle cell cultures: inhibition by osteopontin. Circ Res 84:166–178
Bellahcene A, Castronovo V (1995) Increased expression of osteonectin and osteopontin, two bone matrix proteins, in human breast cancer. Am J Pathol 146:95–100
Hirota S, Ito A, Nagoshi J, Takeda M, Kurata A, Takatsuka Y, Kohri K, Nomura S, Kitamura Y (1995) Expression of bone matrix protein messenger ribonucleic acids in human breast cancers. Possible involvement of osteopontin in development of calcifying foci. Lab Invest 72:64–69
Maki M, Hirota S, Kaneko Y, Morohoshi T (2000) Expression of osteopontin messenger RNA by macrophages in ovarian serous papillary cystadenocarcinoma: a possible association with calcification of psammoma bodies. Pathol Int 50:531–535
Rodrigues LR, Teixeira JA, Schmitt FL, Paulsson M, Lindmark-Mansson H (2007) The role of osteopontin in tumor progression and metastasis in breast cancer. Cancer Epidemiol Biomarkers Prev 16:1087–1097
Liszczak T, Richardson EP Jr, Phillips JP, Jacobson S, Kornblith PL (1978) Morphological, biochemical, ultrastructural, tissue culture and clinical observations of typical and aggressive craniopharyngiomas. Acta Neuropathol 43:191–203
Matusan-Ilijas K, Behrem S, Jonjic N, Zarkovic K, Lucin K (2008) Osteopontin expression correlates with angiogenesis and survival in malignant astrocytoma. Pathol Oncol Res 14:293–298
Ding Q, Stewart J Jr, Prince CW, Chang PL, Trikha M, Han X, Grammer JR, Gladson CL (2002) Promotion of malignant astrocytoma cell migration by osteopontin expressed in the normal brain: differences in integrin signaling during cell adhesion to osteopontin versus vitronectin. Cancer Res 62:5336–5343
Jang T, Savarese T, Low HP, Kim S, Vogel H, Lapointe D, Duong T, Litofsky NS, Weimann JM, Ross AH, Recht L (2006) Osteopontin expression in intratumoral astrocytes marks tumor progression in gliomas induced by prenatal exposure to N-ethyl-N-nitrosourea. Am J Pathol 168:1676–1685
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This study was partially supported by the Research Center of Clinical Medicine, Nanfang Hospital, Southern Medical University, China.
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SongTao, Q., GuangLong, H., Jun, P. et al. Involvement of osteopontin as a core protein in craniopharyngioma calcification formation. J Neurooncol 98, 21–30 (2010). https://doi.org/10.1007/s11060-009-0053-8
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DOI: https://doi.org/10.1007/s11060-009-0053-8