High expression of S100A4 and endoglin is associated with metastatic disease in head and neck squamous cell carcinoma

详细信息    查看全文

• 作者：Marcos Vinícius Macedo de Oliveira (1)
  Carlos Alberto de Carvalho Fraga (1)
  Lucas Oliveira Barros (1)
  Camila Santos Pereira (1)
  Sérgio Henrique Sousa Santos (1) (2)
  John R. Basile (3)
  Ricardo Santiago Gomez (1) (4)
  André Luiz Sena Guimar?es (1) (5)
  Alfredo Maurício Batista De-Paula (1) (5) (6)
  
• 关键词：Metastasis ; Head and neck squamous cell carcinoma ; S100A4 ; Metallopeptidases ; 9 ; Annexin A2 ; Tumor neoangiogenesis ; DNA methylation ; Immunohistochemistry
• 刊名：Clinical & Experimental Metastasis
• 出版年：2014
• 出版时间：August 2014
• 年：2014
• 卷：31
• 期：6
• 页码：639-649
• 全文大小：1,458 KB
• 参考文献：1. Jemal A, Siegel R, Xu J (2010) Ward E (2010) cancer statistics. CA Cancer J Clin 60(5):277-00. doi:10.3322/caac.20073
  2. Warnakulasuriya S (2009) Global epidemiology of oral and oropharyngeal cancer. Oral Oncol 45(4-):309-16. doi:10.1016/j.oraloncology.2008.06.002 CrossRef
  3. Curado MP, Boyle P (2013) Epidemiology of head and neck squamous cell carcinoma not related to tobacco or alcohol. Curr Opin Oncol 25(3):229-34. doi:10.1097/CCO.0b013e32835ff48c
  4. De Paula AM, Souza LR, Farias LC, Correa GT, Fraga CA, Eleuterio NB, Silveira AC, Santos FB, Haikal DS, Guimaraes AL, Gomez RS (2009) Analysis of 724 cases of primary head and neck squamous cell carcinoma (HNSCC) with a focus on young patients and p53 immunolocalization. Oral Oncol 45(9):777-82 CrossRef
  5. Rothenberg SM, Ellisen LW (2012) The molecular pathogenesis of head and neck squamous cell carcinoma. J Clin Invest 122(6):1951-957 CrossRef
  6. Hiratsuka H, Miyakawa A, Nakamori K, Kido Y, Sunakawa H, Kohama G (1997) Multivariate analysis of occult lymph node metastasis as a prognostic indicator for patients with squamous cell carcinoma of the oral cavity. Cancer 80(3):351-56. doi:10.1002/(SICI)1097-0142(19970801)80 CrossRef
  7. Descot A, Oskarsson T (2013) The molecular composition of the metastatic niche. Exp Cell Res. doi:10.1016/j.yexcr.2013.04.017
  8. Langley RR, Fidler IJ (2011) The seed and soil hypothesis revisited–the role of tumor-stroma interactions in metastasis to different organs. Int J Cancer 128(11):2527-535. doi:10.1002/ijc.26031
  9. Peinado H, Lavotshkin S, Lyden D (2011) The secreted factors responsible for pre-metastatic niche formation: old sayings and new thoughts. Semin Cancer Biol 21(2):139-46. doi:10.1016/j.semcancer.2011.01.002 CrossRef
  10. Sleeman JP, Christofori G, Fodde R, Collard JG, Berx G, Decraene C, Ruegg C (2012) Concepts of metastasis in flux: the stromal progression model. Semin Cancer Biol 22(3):174-86. doi:10.1016/j.semcancer.2012.02.007 CrossRef
  11. Donato R (2001) S100: a multigenic family of calcium-modulated proteins of the EF-hand type with intracellular and extracellular functional roles. Int J Biochem Cell Biol 33(7):637-68
  12. Polans AS, Palczewski K, Asson-Batres MA, Ohguro H, Witkowska D, Haley TL, Baizer L, Crabb JW (1994) Purification and primary structure of Capl, an S-100-related calcium-binding protein isolated from bovine retina. J Biol Chem 269(8):6233-240
  13. Boye K, Maelandsmo GM (2010) S100A4 and metastasis: a small actor playing many roles. Am J Pathol 176(2):528-35. doi:10.2353/ajpath.2010.090526 CrossRef
  14. Garrett SC, Varney KM, Weber DJ, Bresnick AR (2006) S100A4, a mediator of metastasis. J Biol Chem 281(2):677-80 CrossRef
  15. Lukanidin E, Sleeman JP (2012) Building the niche: the role of the S100 proteins in metastatic growth. Semin Cancer Biol 22(3):216-25. doi:10.1016/j.semcancer.2012.02.006 CrossRef
  16. Grieve AG, Moss SE, Hayes MJ (2012) Annexin A2 at the interface of actin and membrane dynamics: a focus on its roles in endocytosis and cell polarization. Int J Cell Biol 2012:852430. doi:10.1155/2012/852430
  17. Sharma M, Ownbey RT, Sharma MC (2010) Breast cancer cell surface annexin II induces cell migration and neoangiogenesis via tPA dependent plasmin generation. Exp Mol Pathol 88(2):278-86. doi:10.1016/j.yexmp.2010.01.001 CrossRef
  18. Lokman NA, Ween MP, Oehler MK, Ricciardelli C (2011) The role of annexin A2 in tumorigenesis and cancer progression. Cancer Microenviron 4(2):199-08. doi:10.1007/s12307-011-0064-9 CrossRef
  19. Van den Steen PE, Dubois B, Nelissen I, Rudd PM, Dwek RA, Opdenakker G (2002) Biochemistry and molecular biology of gelatinase B or matrix metalloproteinase-9 (MMP-9). Crit Rev Biochem Mol Biol 37(6):375-36. doi:10.1080/10409230290771546 CrossRef
  20. Rodriguez-Manzaneque JC, Lane TF, Ortega MA, Hynes RO, Lawler J, Iruela-Arispe ML (2001) Thrombospondin-1 suppresses spontaneous tumor growth and inhibits activation of matrix metalloproteinase-9 and mobilization of vascular endothelial growth factor. Proc Natl Acad Sci U S A 98(22):12485-2490. doi:10.1073/pnas.171460498 CrossRef
  21. Bergers G, Brekken R, McMahon G, Vu TH, Itoh T, Tamaki K, Tanzawa K, Thorpe P, Itohara S, Werb Z, Hanahan D (2000) Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat Cell Biol 2(10):737-44. doi:10.1038/35036374
  22. Ramos-DeSimone N, Hahn-Dantona E, Sipley J, Nagase H, French DL, Quigley JP (1999) Activation of matrix metalloproteinase-9 (MMP-9) via a converging plasmin/stromelysin-1 cascade enhances tumor cell invasion. J Biol Chem 274(19):13066-3076 CrossRef
  23. Yu Q, Stamenkovic I (2000) Cell surface-localized matrix metalloproteinase-9 proteolytically activates TGF-beta and promotes tumor invasion and angiogenesis. Genes Dev 14(2):163-76
  24. Fonsatti E, Maio M (2004) Highlights on endoglin (CD105): from basic findings towards clinical applications in human cancer. J Trans Med 2(1):18 CrossRef
  25. Li DY, Sorensen LK, Brooke BS, Urness LD, Davis EC, Taylor DG, Boak BB, Wendel DP (1999) Defective angiogenesis in mice lacking endoglin. Science 284(5419):1534-537 CrossRef
  26. Lebrin F, Goumans MJ, Jonker L, Carvalho RL, Valdimarsdottir G, Thorikay M, Mummery C, Arthur HM, ten Dijke P (2004) Endoglin promotes endothelial cell proliferation and TGF-beta/ALK1 signal transduction. EMBO J 23(20):4018-028. doi:10.1038/sj.emboj.7600386 CrossRef
  27. She X, Matsuno F, Harada N, Tsai H, Seon BK (2004) Synergy between anti-endoglin (CD105) monoclonal antibodies and TGF-beta in suppression of growth of human endothelial cells. Int J Cancer 108(2):251-57. doi:10.1002/ijc.11551
  28. Kuiper P, Hawinkels LJ, de Jonge-Muller ES, Biemond I, Lamers CB, Verspaget HW (2011) Angiogenic markers endoglin and vascular endothelial growth factor in gastroenteropancreatic neuroendocrine tumors. World J Gastroenterol 17(2):219-25. doi:10.3748/wjg.v17.i2.219 CrossRef
  29. Saad RS, Liu YL, Nathan G, Celebrezze J, Medich D, Silverman JF (2004) Endoglin (CD105) and vascular endothelial growth factor as prognostic markers in colorectal cancer. Mod Pathol 17(2):197-03 CrossRef
  30. Lo JF, Yu CC, Chiou SH, Huang CY, Jan CI, Lin SC, Liu CJ, Hu WY, Yu YH (2011) The epithelial-mesenchymal transition mediator S100A4 maintains cancer-initiating cells in head and neck cancers. Cancer Res 71(5):1912-923. doi:10.1158/0008-5472.CAN-10-2350 CrossRef
  31. Moriyama-Kita M, Endo Y, Yonemura Y, Heizmann CW, Schafer BW, Sasaki T, Yamamoto E (2004) Correlation of S100A4 expression with invasion and metastasis in oral squamous cell carcinoma. Oral Oncol 40(5):496-00 CrossRef
  32. Sapkota D, Bruland O, Boe OE, Bakeer H, Elgindi OA, Vasstrand EN, Ibrahim SO (2008) Expression profile of the S100 gene family members in oral squamous cell carcinomas. JOral PatholMed 37(10):607-15. doi:10.1111/j.1600-0714.2008.00683.x
  33. Broders AC (1921) Squamous-cell epithelioma of the skin: a study of 256 cases. Ann Surg 73(2):141-60 CrossRef
  34. Bryne M, Koppang HS, Lilleng R, Kjaerheim A (1992) Malignancy grading of the deep invasive margins of oral squamous cell carcinomas has high prognostic value. J Pathol 166(4):375-81 CrossRef
  35. Clark SJ, Statham A, Stirzaker C, Molloy PL, Frommer M (2006) DNA methylation: bisulphite modification and analysis. Nat Protoc 1(5):2353-364. doi:10.1038/nprot.2006.324 CrossRef
  36. Reinders J, 12 (2009) Amplification of bisulfite-converted DNA for genome-wide DNA methylation profiling. Cold Spring Harb Protoc 2009:pdb.prot5342. doi:10.1101/pdb.prot5342 CrossRef
  37. Vermeulen PB, Gasparini G, Fox SB, Toi M, Martin L, McCulloch P, Pezzella F, Viale G, Weidner N, Harris AL, Dirix LY (1996) Quantification of angiogenesis in solid human tumours: an international consensus on the methodology and criteria of evaluation. Eur J Cancer 32A(14):2474-484 CrossRef
  38. Weidner N (1995) Intratumor microvessel density as a prognostic factor in cancer. Am J Pathol 147(1):9-9
  39. Bird A (1992) The essentials of DNA methylation. Cell 70(1):5- CrossRef
  40. Baylin SB, Esteller M, Rountree MR, Bachman KE, Schuebel K, Herman JG (2001) Aberrant patterns of DNA methylation, chromatin formation and gene expression in cancer. Hum Mol Genet 10(7):687-92 CrossRef
  41. Ehrlich M (2009) DNA hypomethylation in cancer cells. Epigenomics 1(2):239-59. doi:10.2217/epi.09.33 CrossRef
  42. Li Y, Liu ZL, Zhang KL, Chen XY, Kong QY, Wu ML, Sun Y, Liu J, Li H (2009) Methylation-associated silencing of S100A4 expression in human epidermal cancers. Exp Dermatol 18(10):842-48 CrossRef
  43. Liu J, Guo Y, Fu S, Yang M, Sun KL, Fu WN (2010) Hypomethylation-induced expression of S100A4 increases the invasiveness of laryngeal squamous cell carcinoma. Oncol Rep 23(4):1101-107 CrossRef
  44. Xie R, Loose DS, Shipley GL, Xie S, Bassett RL Jr, Broaddus RR (2007) Hypomethylation-induced expression of S100A4 in endometrial carcinoma. Mod Pathol 20(10):1045-054 CrossRef
  45. Matos LL, Trufelli DC, de Matos MG, da Silva Pinhal MA (2010) Immunohistochemistry as an important tool in biomarkers detection and clinical practice. Biomark Insights 5:9-0 CrossRef
  46. Moriyama-Kita M, Endo Y, Yonemura Y, Heizmann CW, Miyamori H, Sato H, Yamamoto E, Sasaki T (2005) S100A4 regulates E-cadherin expression in oral squamous cell carcinoma. Cancer Lett 230(2):211-18 CrossRef
  47. Chen M, Sinha M, Luxon BA, Bresnick AR, O’Connor KL (2009) Integrin α6β4 controls the expression of genes associated with cell motility, invasion, and metastasis, including S100A4/metastasin. J Biol Chem 284(3):1484-494. doi:10.1074/jbc.M803997200 CrossRef
  48. Li ZH, Bresnick AR (2006) The S100A4 metastasis factor regulates cellular motility via a direct interaction with myosin-IIA. Cancer Res 66(10):5173-180 CrossRef
  49. Bjornland K, Winberg JO, Odegaard OT, Hovig E, Loennechen T, Aasen AO, Fodstad O, Maelandsmo GM (1999) S100A4 involvement in metastasis: deregulation of matrix metalloproteinases and tissue inhibitors of matrix metalloproteinases in osteosarcoma cells transfected with an anti-S100A4 ribozyme. Cancer Res 59(18):4702-708
  50. Schmidt-Hansen B, Ornas D, Grigorian M, Klingelhofer J, Tulchinsky E, Lukanidin E, Ambartsumian N (2004) Extracellular S100A4(mts1) stimulates invasive growth of mouse endothelial cells and modulates MMP-13 matrix metalloproteinase activity. Oncogene 23(32):5487-495 CrossRef
  51. Semov A, Moreno MJ, Onichtchenko A, Abulrob A, Ball M, Ekiel I, Pietrzynski G, Stanimirovic D, Alakhov V (2005) Metastasis-associated protein S100A4 induces angiogenesis through interaction with annexin II and accelerated plasmin formation. JBiolChem 280(21):20833-0841
  52. Oh SP, Seki T, Goss KA, Imamura T, Yi Y, Donahoe PK, Li L, Miyazono K, ten Dijke P, Kim S, Li E (2000) Activin receptor-like kinase 1 modulates transforming growth factor-beta 1 signaling in the regulation of angiogenesis. Proc Natl Acad Sci U S A 97(6):2626-631 CrossRef
  53. Fraga CA, De Oliveira MV, de Oliveira ES, Barros LO, Santos FB, Gomez RS, De-Paula AM, Guimaraes AL (2011) A high HIF-1alpha expression genotype is associated with poor prognosis of upper aerodigestive tract carcinoma patients. Oral Oncol. doi:10.1016/j.oraloncology.2011.08.023
  54. Kyzas PA, Agnantis NJ, Stefanou D (2006) Endoglin (CD105) as a prognostic factor in head and neck squamous cell carcinoma. Virchows Arch 448(6):768-75. doi:10.1007/s00428-006-0195-4 CrossRef
  55. Marioni G, D’Alessandro E, Giacomelli L, Staffieri A (2010) CD105 is a marker of tumour vasculature and a potential target for the treatment of head and neck squamous cell carcinoma. J Oral Pathol Med 39(5):361-67. doi:10.1111/j.1600-0714.2010.00888.x
  56. Rafii S, Lyden D (2006) S100 chemokines mediate bookmarking of premetastatic niches. Nat Cell Biol 8(12):1321-323. doi:10.1038/ncb1206-1321
  57. Lu P, Weaver VM, Werb Z (2012) The extracellular matrix: a dynamic niche in cancer progression. J Cell Biol 196(4):395-06. doi:10.1083/jcb.201102147 CrossRef
  58. Rucci N, Sanita P, Angelucci A (2011) Roles of metalloproteases in metastatic niche. Curr Mol Med 11(8):609-22 CrossRef
  
• 作者单位：Marcos Vinícius Macedo de Oliveira (1)
  Carlos Alberto de Carvalho Fraga (1)
  Lucas Oliveira Barros (1)
  Camila Santos Pereira (1)
  Sérgio Henrique Sousa Santos (1) (2)
  John R. Basile (3)
  Ricardo Santiago Gomez (1) (4)
  André Luiz Sena Guimar?es (1) (5)
  Alfredo Maurício Batista De-Paula (1) (5) (6)
  
  1. Nucleus of Epidemiological and Molecular Research Catrumano. Health Research Laboratory. Health Science Post-graduate Programme, Universidade Estadual de Montes Claros, Montes Claros, MG, 39401-001, Brazil
  2. Department of Pharmacology, Universidade Federal de Minas Gerais, Belo Horizonte, MG, 31270-901, Brazil
  3. Department of Oncology and Diagnostic Sciences, University of Maryland School of Dentistry, Baltimore, MD, 21201, USA
  4. Faculty of Dentistry, Universidade Federal de Minas Gerais, Belo Horizonte, MG, 31270-901, Brazil
  5. Department of Dentistry, Universidade Estadual de Montes Claros, Montes Claros, MG, 39401-001, Brazil
  6. Programa de Pós-gradua??o em Ciências da Saúde. Sala 7. Hospital Universitário Clemente de Faria, Universidade Estadual de Montes Claros, Avenida Cula Mangabeira, 562. Bairro Santo Expedito, Montes Claros, MG, 39401-001, Brazil
  
• ISSN：1573-7276

文摘

The presence of cervical metastasis is responsible for high morbidity and mortality rates in individuals with head and neck squamous cell carcinoma (HNSCC). S100A4, a pleiotropic EF-hand calcium-binding protein, is expressed in various normal and cancer cell types. During cancer progression, molecular disturbances in S100A4 can modulate the activity and expression of pre-metastatic and metastatic genes. In this study, we investigated the association between S100A4 methylation status and protein expression as well as the expression of the S100A4 related-proteins annexin A2 (ANXA2), matrix metallopeptidase-9, and endoglin, for metastasis and other clinicopathological parameters in HNSCC. Formalin-fixed, paraffin-embedded blocks of metastatic and non-metastatic HNSCC and matched cervical lymph node (LN) samples (metastatic LN?=?mLN, non-metastatic?=?nmLN, and control LN (lymphadenitis)?=?cLN) were submitted for methylation specific-polymerase chain reaction and immunohistochemistry. Our results showed that S100A4 methylation status failed to demonstrate association with cervical metastasis and other clinicopathological factors related to HNSCC. HNSCC samples from patients that presented with metastatic disease showed high S100A4 and endoglin expression (p?