PL EN


Preferences help
enabled [disable] Abstract
Number of results
2012 | 59 | 4 | 647-652
Article title

Dual, enzymatic and non-enzymatic, function of ecto-5'-nucleotidase (eN, CD73) in migration and invasion of A375 melanoma cells

Content
Title variants
Languages of publication
EN
Abstracts
EN
Ecto-5'-nucleotidase (eN, CD73) mediates extracellular adenosine production from 5'-AMP. Non-enzymatic functions of eN have also been reported. The aim of the study was to investigate the role of ecto-5'-nucleotidase in aggressive melanoma behaviour. Analysis of the involvement of eN in adhesion, migration and invasion revealed eN functions unknown to date. We found that following eN blockade by concanavalin A, the strength of adhesion to different ECM proteins was not altered, but at the same time the invasion ability of the cells was decreased. On the other hand, knocking down eN in melanoma cells did not influence cell invasion but abolished their migration on tenascin C (TnC). Ecto-5'-nucleotidase seems to fulfil a more distinct role as a receptor than as an enzyme in the cell interaction and mobility on TnC. Ecto-5'-nucleotidase activates also focal adhesion kinase and enhances the formation of complexes upon cell adhesion to TnC. All these observations prove that an eN-TnC complex is involved in cell migration and invasion and thus in the regulation of melanoma progression.
Year
Volume
59
Issue
4
Pages
647-652
Physical description
Dates
published
2012
received
2012-06-28
revised
2012-10-16
accepted
2012-10-29
(unknown)
2012-11-16
References
  • Airas L, Hellman J, Salmi M, Bono P, Puurunen T, Smith DJ, Jalkanen S (1995) CD73 is involved in lymphocyte binding to the endothelium: characterization of lymphocyte-vascular adhesion protein 2 identifies it as CD73. J Exp Med 182: 1603-1608.
  • Airas L, Niemelä J, Jalkanen S (2000) CD73 engagement promotes lymphocyte binding to endothelial cells via a lymphocyte function-associated antigen-1-dependent mechanism. J Immunol 165: 5411-5417.
  • Andrade CM, Lopez PL, Noronha BT, Wink MR, Borojevic R, Margis R, Lenz G, Battastini AM, Guma FC (2011) Ecto-5'-nucleotidase/CD73 knockdown increases cell migration and mRNA level of collagen I in a hepatic stellate cell line. Cell Tissue Res 344: 279-286.
  • Balch CM, Soong SJ, Gershenwald JE, Thompson JF, Reintgen DS, Cascinelli N, Urist M, McMasters KM, Ross MI, Kirkwood JM, Atkins MB, Thompson JA, Coit DG, Byrd D, Desmond R, Zhang Y, Liu PY, Lyman GH, Morabito A (2001) Prognostic factors analysis of 17,600 melanoma patients: validation of the American Joint Committee on Cancer melanoma staging system. J Clin Oncol 19: 3622-3634.
  • Bavaresco L, Bernardi A, Braganhol E, Cappellari AR, Rockenbach L, Farias PF, Wink MR, Delgado-Cañedo A, Battastini AM (2008) The role of ecto-5'-nucleotidase/CD73 in glioma cell line proliferation. Mol Cell Biochem 319: 61-68.
  • Chiquet-Ehrismann R, Chiquet M (2003) Tenascins: regulation and putative functions during pathological stress. J Pathol 200: 488-499.
  • Cho SY, Polster J, Engles JM, Hilton J, Abraham EH, Wahl RL (2006) In vitro evaluation of adenosine 5'-monophosphate as an imaging agent of tumor metabolism. J Nucl Med 47: 837-845.
  • Fenoglio C, Necchi D, Civallero M, Ceroni M, Nano R (1997) Cytochemical demonstration of nitric oxide synthase and 5' nucleotidase in human glioblastoma. Anticancer Res 17: 2507-2511.
  • Fukuda K, Sakakura C, Miyagawa K, Kuriu Y, Kin S, Nakase Y, Hagiwara A, Mitsufuji S, Okazaki Y, Hayashizaki Y, Yamagishi H (2004) Differential gene expression profiles of radioresistant oesophageal cancer cell lines established by continuous fractionated irradiation. Br J Cancer 91: 1543-1550.
  • Fukunaga-Kalabis M, Martinez G, Nguyen TK, Kim D, Santiago-Walker A, Roesch A, Herlyn M (2010) Tenascin-C promotes melanoma progression by maintaining the ABCB5-positive side population. Oncogene 29: 6115-6124.
  • Hamadi A, Bouali M, Dontenwill M, Stoeckel H, Takeda K, Rondé P (2005) Regulation of focal adhesion dynamics and disassembly by phosphorylation of FAK at tyrosine 397. J Cell Sci 118: 4415-4425.
  • Hastie C, Saxton M, Akpan A, Cramer R, Masters JR, Naaby-Hansen S (2005) Combined affinity labelling and mass spectrometry analysis of differential cell surface protein expression in normal and prostate cancer cells. Oncogene 24: 5905-5913.
  • Hua H, Li M, Luo T, Yin Y, Jiang Y (2011) Matrix metalloproteinases in tumorigenesis: an evolving paradigm. Cell Mol Life Sci 68: 3853-3868.
  • Ilmonen S, Jahkola T, Turunen JP, Muhonen T, Asko-Seljavaara S (2004) Tenascin-C in primary malignant melanoma of the skin. Histopathology 45: 405-411.
  • Kondo T, Nakazawa T, Murata SI, Katoh R (2006) Expression of CD73 and its ecto-5'-nucleotidase activity are elevated in papillary thyroid carcinomas. Histopathology 48: 612-614.
  • Kääriäinen E, Nummela P, Soikkeli J, Yin M, Lukk M, Jahkola T, Virolainen S, Ora A, Ukkonen E, Saksela O, Hölttä E (2006) Switch to an invasive growth phase in melanoma is associated with tenascin-C, fibronectin, and procollagen-I forming specific channel structures for invasion. J Pathol 210: 181-191.
  • Lee H, Lin EC, Liu L, Smith JW (2003) Gene expression profiling of tumor xenografts: In vivo analysis of organ-specific metastasis. Int J Cancer 107: 528-534.
  • Leth-Larsen R, Lund R, Hansen HV, Laenkholm AV, Tarin D, Jensen ON, Ditzel HJ (2009) Metastasis-related plasma membrane proteins of human breast cancer cells identified by comparative quantitative mass spectrometry. Mol Cell Proteomics 8: 1436-1449.
  • Ludwig HC, Rausch S, Schallock K, Markakis E (1999) Expression of CD 73 (ecto-5'-nucleotidase) in 165 glioblastomas by immunohistochemistry and electronmicroscopic histochemistry. Anticancer Res 19: 1747-1752.
  • Midwood KS, Schwarzbauer JE (2002) Tenascin-C modulates matrix contraction via focal adhesion kinase- and Rho-mediated signaling pathways. Mol Biol Cell 13: 3601-3613.
  • Mikhailov A, Sokolovskaya A, Yegutkin GG, Amdahl H, West A, Yagita H, Lahesmaa R, Thompson LF, Jalkanen S, Blokhin D, Eriksson JE (2008) CD73 participates in cellular multiresistance program and protects against TRAIL-induced apoptosis. J Immunol 181: 464-475.
  • Nagaharu K, Zhang X, Yoshida T, Katoh D, Hanamura N, Kozuka Y, Ogawa T, Shiraishi T, Imanaka-Yoshida K (2011) Tenascin C induces epithelial-mesenchymal transition-like change accompanied by SRC activation and focal adhesion kinase phosphorylation in human breast cancer cells. Am J Pathol 178: 754-763.
  • Navarro JM, Olmo N, Turnay J, López-Conejo MT, Lizarbe MA (1998) Ecto-5'-nucleotidase from a human colon adenocarcinoma cell line. Correlation between enzyme activity and levels in intact cells. Mol Cell Biochem 187: 121-131.
  • Ode A, Kopf J, Kurtz A, Schmidt-Bleek K, Schrade P, Kolar P, Buttgereit F, Lehmann K, Hutmacher DW, Duda GN, Kasper G (2011) CD73 and CD29 concurrently mediate the mechanically induced decrease of migratory capacity of mesenchymal stromal cells. Eur Cell Mater 22: 26-42.
  • Olmo N, Turnay J, Risse G, Deutzmann R, von der Mark K, Lizarbe MA (1992) Modulation of 5'-nucleotidase activity in plasma membranes and intact cells by the extracellular matrix proteins laminin and fibronectin. Biochem J 282 (Pt 1): 181-188.
  • Orend G, Chiquet-Ehrismann R (2006) Tenascin-C induced signaling in cancer. Cancer Lett 244: 143-163.
  • Ostapkowicz A, Inai K, Smith L, Kreda S, Spychala J (2006) Lipid rafts remodeling in estrogen receptor-negative breast cancer is reversed by histone deacetylase inhibitor. Mol Cancer Ther 5: 238-245.
  • Sadej R, Inai K, Rajfur Z, Ostapkowicz A, Kohler J, Skladanowski AC, Mitchell BS, Spychala J (2008) Tenascin C interacts with ecto-5'-nucleotidase (eN) and regulates adenosine generation in cancer cells. Biochim Biophys Acta 1782: 35-40.
  • Sadej R, Spychala J, Skladanowski AC (2006a) Ecto-5'-nucleotidase (eN, CD73) is coexpressed with metastasis promoting antigens in human melanoma cells. Nucleosides Nucleotides Nucleic Acids 25: 1119-1123.
  • Sadej R, Spychala J, Skladanowski AC (2006b) Expression of ecto-5'-nucleotidase (eN, CD73) in cell lines from various stages of human melanoma. Melanoma Res 16: 213-222.
  • Shen TL, Guan JL (2001) Differential regulation of cell migration and cell cycle progression by FAK complexes with Src, PI3K, Grb7 and Grb2 in focal contacts. FEBS Lett 499: 176-181.
  • Spychala J, Lazarowski E, Ostapkowicz A, Ayscue LH, Jin A, Mitchell BS (2004) Role of estrogen receptor in the regulation of ecto-5'-nucleotidase and adenosine in breast cancer. Clin Cancer Res 10: 708-717.
  • Stagg J, Divisekera U, McLaughlin N, Sharkey J, Pommey S, Denoyer D, Dwyer KM, Smyth MJ (2010) Anti-CD73 antibody therapy inhibits breast tumor growth and metastasis. Proc Natl Acad Sci U S A 107: 1547-1552.
  • Stefanovic V, Mandel P, Rosenberg A (1975) Concanavalin A inhibition of ecto-5'-nucleotidase of intact cultured C6 glioma cells. J Biol Chem 250: 7081-7083.
  • Stella J, Bavaresco L, Braganhol E, Rockenbach L, Farias PF, Wink MR, Azambuja AA, Barrios CH, Morrone FB, Oliveira Battastini AM (2010) Differential ectonucleotidase expression in human bladder cancer cell lines. Urol Oncol 28: 260-267.
  • Supernat A, Markiewicz A, Welnicka-Jaskiewicz M, Seroczynska B, Skokowski J, Sejda A, Szade J, Czapiewski P, Biernat W, Zaczek A (2012) CD73 expression as a potential marker of good prognosis in breast carcinoma. Appl Immunohistochem Mol Morphol 20: 103-107.
  • Ujházy P, Berleth ES, Pietkiewicz JM, Kitano H, Skaar JR, Ehrke MJ, Mihich E (1996) Evidence for the involvement of ecto-5'-nucleotidase (CD73) in drug resistance. Int J Cancer 68: 493-500.
  • Wang L, Zhou X, Zhou T, Ma D, Chen S, Zhi X, Yin L, Shao Z, Ou Z, Zhou P (2008) Ecto-5'-nucleotidase promotes invasion, migration and adhesion of human breast cancer cells. J Cancer Res Clin Oncol 134: 365-372.
  • Woodhouse EC, Amanatullah DF, Schetz JA, Liotta LA, Stracke ML, Clair T (1998) Adenosine receptor mediates motility in human melanoma cells. Biochem Biophys Res Commun 246: 888-894.
  • Yegutkin GG, Henttinen T, Samburski SS, Spychala J, Jalkanen S (2002) The evidence for two opposite, ATP-generating and ATP-consuming, extracellular pathways on endothelial and lymphoid cells. Biochem J 367: 121-128.
  • Yoshida T, Yoshimura E, Numata H, Sakakura Y, Sakakura T (1999) Involvement of tenascin-C in proliferation and migration of laryngeal carcinoma cells. Virchows Arch 435: 496-500.
  • Zhi X, Chen S, Zhou P, Shao Z, Wang L, Ou Z, Yin L (2007) RNA interference of ecto-5'-nucleotidase (CD73) inhibits human breast cancer cell growth and invasion. Clin Exp Metastasis 24: 439-448.
Document Type
Publication order reference
YADDA identifier
bwmeta1.element.bwnjournal-article-abpv59p647kz
Identifiers
JavaScript is turned off in your web browser. Turn it on to take full advantage of this site, then refresh the page.