Journal of Neuro-Oncology

, Volume 98, Issue 1, pp 21–30 | Cite as

Involvement of osteopontin as a core protein in craniopharyngioma calcification formation

  • Qi SongTao
  • Huang GuangLong
  • Pan Jun
  • Li Jia
  • Zhang Xi’An
  • Fang LuXiong
  • Liu BaoGuo
  • Meng Wei
  • Zhang YongMing
  • Liu XiaoJun
Laboratory Investigation - Human/Animal Tissue
First Online:
Received:
Accepted:

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.

Keywords

Osteopontin Craniopharyngioma Calcification CD44v6 Immunohistochemistry 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgments

This study was partially supported by the Research Center of Clinical Medicine, Nanfang Hospital, Southern Medical University, China.

References

  1. 1.
    Bunin GR, Surawicz TS, Witman PA, Preston-Martin S, Davis F, Bruner JM (1998) The descriptive epidemiology of craniopharyngioma. J Neurosurg 89:547–551CrossRefPubMedGoogle Scholar
  2. 2.
    Garnett MR, Puget S, Grill J, Sainte-Rose C (2007) Craniopharyngioma. Orphanet J Rare Dis 2:18CrossRefPubMedGoogle Scholar
  3. 3.
    Rekate HL (2005) Craniopharyngioma. J Neurosurg 103:297–298 discussion 298PubMedGoogle Scholar
  4. 4.
    Wisoff JH (2008) Craniopharyngioma. J Neurosurg Pediatr 1:124–125 discussion 125CrossRefPubMedGoogle Scholar
  5. 5.
    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 83:206–214CrossRefPubMedGoogle Scholar
  6. 6.
    Eldevik OP, Blaivas M, Gabrielsen TO, Hald JK, Chandler WF (1996) Craniopharyngioma: radiologic and histologic findings and recurrence. AJNR Am J Neuroradiol 17:1427–1439PubMedGoogle Scholar
  7. 7.
    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 14:558–563CrossRefPubMedGoogle Scholar
  8. 8.
    Miller DC (1994) Pathology of craniopharyngiomas: clinical import of pathological findings. Pediatr Neurosurg 21(Suppl 1):11–17CrossRefPubMedGoogle Scholar
  9. 9.
    Tsuda M, Takahashi S, Higano S, Kurihara N, Ikeda H, Sakamoto K (1997) CT and MR imaging of craniopharyngioma. Eur Radiol 7:464–469CrossRefPubMedGoogle Scholar
  10. 10.
    Sato K, Kubota T (1999) Fine structure of ossification in craniopharyngiomas. Ultrastruct Pathol 23:395–399CrossRefPubMedGoogle Scholar
  11. 11.
    Sato K, Kubota T, Yamamoto S, Ishikura A (1986) An ultrastructural study of mineralization in craniopharyngiomas. J Neuropathol Exp Neurol 45:463–470CrossRefPubMedGoogle Scholar
  12. 12.
    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 2:343–356CrossRefPubMedGoogle Scholar
  13. 13.
    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 101:85–90PubMedGoogle Scholar
  14. 14.
    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 21:539–550CrossRefPubMedGoogle Scholar
  15. 15.
    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 1:621–632CrossRefPubMedGoogle Scholar
  16. 16.
    Haylock DN, Nilsson SK (2006) Osteopontin: a bridge between bone and blood. Br J Haematol 134:467–474CrossRefPubMedGoogle Scholar
  17. 17.
    O’Regan A, Berman JS (2000) Osteopontin: a key cytokine in cell-mediated and granulomatous inflammation. Int J Exp Pathol 81:373–390CrossRefPubMedGoogle Scholar
  18. 18.
    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 7:305–313PubMedGoogle Scholar
  19. 19.
    Rangaswami H, Bulbule A, Kundu GC (2006) Osteopontin: role in cell signaling and cancer progression. Trends Cell Biol 16:79–87CrossRefPubMedGoogle Scholar
  20. 20.
    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 102:17101–17106CrossRefPubMedGoogle Scholar
  21. 21.
    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 7:498–506CrossRefPubMedGoogle Scholar
  22. 22.
    Weber GF (2001) The metastasis gene osteopontin: a candidate target for cancer therapy. Biochim Biophys Acta 1552:61–85PubMedGoogle Scholar
  23. 23.
    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 3:1169–1180PubMedGoogle Scholar
  24. 24.
    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 267:24871–24878PubMedGoogle Scholar
  25. 25.
    Rittling SR, Chambers AF (2004) Role of osteopontin in tumour progression. Br J Cancer 90:1877–1881CrossRefPubMedGoogle Scholar
  26. 26.
    Weber GF, Ashkar S, Cantor H (1997) Interaction between CD44 and osteopontin as a potential basis for metastasis formation. Proc Assoc Am Physicians 109:1–9PubMedGoogle Scholar
  27. 27.
    Ponta H, Sherman L, Herrlich PA (2003) CD44: from adhesion molecules to signalling regulators. Nat Rev Mol Cell Biol 4:33–45CrossRefPubMedGoogle Scholar
  28. 28.
    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 55:4594–4598PubMedGoogle Scholar
  29. 29.
    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 56:1037–1042PubMedGoogle Scholar
  30. 30.
    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 81:157–162CrossRefPubMedGoogle Scholar
  31. 31.
    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 67:2089–2097CrossRefPubMedGoogle Scholar
  32. 32.
    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 16:4457–4467PubMedGoogle Scholar
  33. 33.
    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 153:276–282CrossRefPubMedGoogle Scholar
  34. 34.
    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 48:5770–5774PubMedGoogle Scholar
  35. 35.
    Franzen A, Heinegard D (1985) Isolation and characterization of two sialoproteins present only in bone calcified matrix. Biochem J 232:715–724PubMedGoogle Scholar
  36. 36.
    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):513–520PubMedGoogle Scholar
  37. 37.
    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 39:775–782CrossRefPubMedGoogle Scholar
  38. 38.
    Mohler ER III, Adam LP, McClelland P, Graham L, Hathaway DR (1997) Detection of osteopontin in calcified human aortic valves. Arterioscler Thromb Vasc Biol 17:547–552PubMedGoogle Scholar
  39. 39.
    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 161:2035–2046PubMedGoogle Scholar
  40. 40.
    Heinegard D, Andersson G, Reinholt FP (1995) Roles of osteopontin in bone remodeling. Ann N Y Acad Sci 760:213–222CrossRefPubMedGoogle Scholar
  41. 41.
    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):132–135CrossRefPubMedGoogle Scholar
  42. 42.
    Denhardt DT, Noda M (1998) Osteopontin expression and function: role in bone remodeling. J Cell Biochem (Suppl 30–31):92–102CrossRefPubMedGoogle Scholar
  43. 43.
    Wada T, McKee MD, Steitz S, Giachelli CM (1999) Calcification of vascular smooth muscle cell cultures: inhibition by osteopontin. Circ Res 84:166–178PubMedGoogle Scholar
  44. 44.
    Bellahcene A, Castronovo V (1995) Increased expression of osteonectin and osteopontin, two bone matrix proteins, in human breast cancer. Am J Pathol 146:95–100PubMedGoogle Scholar
  45. 45.
    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 72:64–69PubMedGoogle Scholar
  46. 46.
    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 50:531–535CrossRefPubMedGoogle Scholar
  47. 47.
    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 16:1087–1097CrossRefPubMedGoogle Scholar
  48. 48.
    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 43:191–203PubMedGoogle Scholar
  49. 49.
    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 14:293–298CrossRefPubMedGoogle Scholar
  50. 50.
    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 62:5336–5343PubMedGoogle Scholar
  51. 51.
    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 168:1676–1685CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC. 2009

Authors and Affiliations

  • Qi SongTao
    • 1
  • Huang GuangLong
    • 1
  • Pan Jun
    • 1
  • Li Jia
    • 2
  • Zhang Xi’An
    • 1
  • Fang LuXiong
    • 1
  • Liu BaoGuo
    • 1
  • Meng Wei
    • 1
  • Zhang YongMing
    • 1
  • Liu XiaoJun
    • 1
  1. 1.Department of NeurosurgeryNanfang Hospital, Southern Medical UniversityGuangzhouThe People’s Republic of China
  2. 2.Department of Endocrine and MetabolismNanfang Hospital, Southern Medical UniversityGuangzhouThe People’s Republic of China

Personalised recommendations