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Published in: BMC Cancer 1/2013

Open Access 01-12-2013 | Research article

ID3 contributes to cerebrospinal fluid seeding and poor prognosis in medulloblastoma

Authors: Ji Hoon Phi, Seung Ah Choi, Sang-Hee Lim, Joongyub Lee, Kyu-Chang Wang, Sung-Hye Park, Seung-Ki Kim

Published in: BMC Cancer | Issue 1/2013

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Abstract

Background

The inhibitor of differentiation (ID) genes have been implicated as promoters of tumor progression and metastasis in many human cancers. The current study investigated the expression and functional roles of ID genes in seeding and prognosis of medulloblastoma.

Methods

ID gene expression was screened in human medulloblastoma tissues. Knockdown of ID3 gene was performed in medulloblastoma cells in vitro. The expression of metastasis-related genes after ID3 knockdown was assessed. The effect of ID3 knockdown on tumor seeding was observed in an animal model in vivo. The survival of medulloblastoma patients was plotted according to the ID3 expression levels.

Results

Significantly higher ID3 expression was observed in medulloblastoma with cerebrospinal fluid seeding than tumors without seeding. Knockdown of ID3 decreased proliferation, increased apoptosis, and suppressed the migration of D283 medulloblastoma cells in vitro. In a seeding model of medulloblastoma, ID3 knockdown in vivo with shRNA inhibited the growth of primary tumors, prevented the development of leptomeningeal seeding, and prolonged animal survival. High ID3 expression was associated with shorter survival of medulloblastoma patients, especially in Group 4 medulloblastomas.

Conclusions

High ID3 expression is associated with medullolbastoma seeding and is a poor prognostic factor, especially in patients with Group 4 tumors. ID3 may represent the metastatic/ aggressive phenotype of a subgroup of medulloblastoma.
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Literature
1.
go back to reference Packer RJ, Goldwein J, Nicholson HS, Vezina LG, Allen JC, Ris MD, Muraszko K, Rorke LB, Wara WM, Cohen BH, et al: Treatment of children with medulloblastomas with reduced-dose craniospinal radiation therapy and adjuvant chemotherapy: A Children’s Cancer Group Study. J Clin Oncol. 1999, 17 (7): 2127-2136.PubMed Packer RJ, Goldwein J, Nicholson HS, Vezina LG, Allen JC, Ris MD, Muraszko K, Rorke LB, Wara WM, Cohen BH, et al: Treatment of children with medulloblastomas with reduced-dose craniospinal radiation therapy and adjuvant chemotherapy: A Children’s Cancer Group Study. J Clin Oncol. 1999, 17 (7): 2127-2136.PubMed
2.
go back to reference Taylor RE, Bailey CC, Robinson K, Weston CL, Ellison D, Ironside J, Lucraft H, Gilbertson R, Tait DM, Walker DA, et al: Results of a randomized study of preradiation chemotherapy versus radiotherapy alone for nonmetastatic medulloblastoma: The International Society of Paediatric Oncology/United Kingdom Children’s Cancer Study Group PNET-3 Study. J Clin Oncol. 2003, 21 (8): 1581-1591. 10.1200/JCO.2003.05.116.CrossRefPubMed Taylor RE, Bailey CC, Robinson K, Weston CL, Ellison D, Ironside J, Lucraft H, Gilbertson R, Tait DM, Walker DA, et al: Results of a randomized study of preradiation chemotherapy versus radiotherapy alone for nonmetastatic medulloblastoma: The International Society of Paediatric Oncology/United Kingdom Children’s Cancer Study Group PNET-3 Study. J Clin Oncol. 2003, 21 (8): 1581-1591. 10.1200/JCO.2003.05.116.CrossRefPubMed
3.
go back to reference Brown HG, Kepner JL, Perlman EJ, Friedman HS, Strother DR, Duffner PK, Kun LE, Goldthwaite PT, Burger PC: “Large cell/anaplastic” medulloblastomas: a Pediatric Oncology Group Study. J Neuropathol Exp Neurol. 2000, 59 (10): 857-865.CrossRefPubMed Brown HG, Kepner JL, Perlman EJ, Friedman HS, Strother DR, Duffner PK, Kun LE, Goldthwaite PT, Burger PC: “Large cell/anaplastic” medulloblastomas: a Pediatric Oncology Group Study. J Neuropathol Exp Neurol. 2000, 59 (10): 857-865.CrossRefPubMed
4.
go back to reference Giangaspero F, Rigobello L, Badiali M, Loda M, Andreini L, Basso G, Zorzi F, Montaldi A: Large-cell medulloblastomas. A distinct variant with highly aggressive behavior. Am J Surg Pathol. 1992, 16 (7): 687-693. 10.1097/00000478-199207000-00007.CrossRefPubMed Giangaspero F, Rigobello L, Badiali M, Loda M, Andreini L, Basso G, Zorzi F, Montaldi A: Large-cell medulloblastomas. A distinct variant with highly aggressive behavior. Am J Surg Pathol. 1992, 16 (7): 687-693. 10.1097/00000478-199207000-00007.CrossRefPubMed
5.
go back to reference Zeltzer PM, Boyett JM, Finlay JL, Albright AL, Rorke LB, Milstein JM, Allen JC, Stevens KR, Stanley P, Li H, et al: Metastasis stage, adjuvant treatment, and residual tumor are prognostic factors for medulloblastoma in children: conclusions from the Children’s Cancer Group 921 randomized phase III study. J Clin Oncol. 1999, 17 (3): 832-845.PubMed Zeltzer PM, Boyett JM, Finlay JL, Albright AL, Rorke LB, Milstein JM, Allen JC, Stevens KR, Stanley P, Li H, et al: Metastasis stage, adjuvant treatment, and residual tumor are prognostic factors for medulloblastoma in children: conclusions from the Children’s Cancer Group 921 randomized phase III study. J Clin Oncol. 1999, 17 (3): 832-845.PubMed
6.
go back to reference Jenkin D, Shabanah MA, Shail EA, Gray A, Hassounah M, Khafaga Y, Kofide A, Mustafa M, Schultz H: Prognostic factors for medulloblastoma. Int J Radiat Oncol Biol Phys. 2000, 47 (3): 573-584. 10.1016/S0360-3016(00)00431-4.CrossRefPubMed Jenkin D, Shabanah MA, Shail EA, Gray A, Hassounah M, Khafaga Y, Kofide A, Mustafa M, Schultz H: Prognostic factors for medulloblastoma. Int J Radiat Oncol Biol Phys. 2000, 47 (3): 573-584. 10.1016/S0360-3016(00)00431-4.CrossRefPubMed
7.
go back to reference Yao MS, Mehta MP, Boyett JM, Li H, Donahue B, Rorke LB, Zeltzer PM: The effect of M-stage on patterns of failure in posterior fossa primitive neuroectodermal tumors treated on CCG-921: a phase III study in a high-risk patient population. Int J Radiat Oncol Biol Phys. 1997, 38 (3): 469-476. 10.1016/S0360-3016(97)00010-2.CrossRefPubMed Yao MS, Mehta MP, Boyett JM, Li H, Donahue B, Rorke LB, Zeltzer PM: The effect of M-stage on patterns of failure in posterior fossa primitive neuroectodermal tumors treated on CCG-921: a phase III study in a high-risk patient population. Int J Radiat Oncol Biol Phys. 1997, 38 (3): 469-476. 10.1016/S0360-3016(97)00010-2.CrossRefPubMed
8.
go back to reference Phi JH, Lee J, Wang KC, Cho BK, Kim IO, Park CK, Kim CY, Ahn HS, Kim IH, Kim SK: Cerebrospinal fluid M staging for medulloblastoma: reappraisal of Chang’s M staging based on the CSF flow. Neuro Oncol. 2011, 13 (3): 334-344. 10.1093/neuonc/noq171.CrossRefPubMed Phi JH, Lee J, Wang KC, Cho BK, Kim IO, Park CK, Kim CY, Ahn HS, Kim IH, Kim SK: Cerebrospinal fluid M staging for medulloblastoma: reappraisal of Chang’s M staging based on the CSF flow. Neuro Oncol. 2011, 13 (3): 334-344. 10.1093/neuonc/noq171.CrossRefPubMed
9.
go back to reference Burger PC, Heinz ER, Shibata T, Kleihues P: Topographic anatomy and CT correlations in the untreated glioblastoma multiforme. J Neurosurg. 1988, 68 (5): 698-704. 10.3171/jns.1988.68.5.0698.CrossRefPubMed Burger PC, Heinz ER, Shibata T, Kleihues P: Topographic anatomy and CT correlations in the untreated glioblastoma multiforme. J Neurosurg. 1988, 68 (5): 698-704. 10.3171/jns.1988.68.5.0698.CrossRefPubMed
10.
go back to reference Chang CH, Housepian EM, Herbert C: An operative staging system and a megavoltage radiotherapeutic technic for cerebellar medulloblastomas. Radiology. 1969, 93 (6): 1351-1359.CrossRefPubMed Chang CH, Housepian EM, Herbert C: An operative staging system and a megavoltage radiotherapeutic technic for cerebellar medulloblastomas. Radiology. 1969, 93 (6): 1351-1359.CrossRefPubMed
11.
go back to reference Gibson P, Tong Y, Robinson G, Thompson MC, Currle DS, Eden C, Kranenburg TA, Hogg T, Poppleton H, Martin J, et al: Subtypes of medulloblastoma have distinct developmental origins. Nature. 2010, 468 (7327): 1095-1099. 10.1038/nature09587.CrossRefPubMedPubMedCentral Gibson P, Tong Y, Robinson G, Thompson MC, Currle DS, Eden C, Kranenburg TA, Hogg T, Poppleton H, Martin J, et al: Subtypes of medulloblastoma have distinct developmental origins. Nature. 2010, 468 (7327): 1095-1099. 10.1038/nature09587.CrossRefPubMedPubMedCentral
12.
go back to reference Kool M, Korshunov A, Remke M, Jones DT, Schlanstein M, Northcott PA, Cho YJ, Koster J, Schouten-van Meeteren A, van Vuurden D, et al: Molecular subgroups of medulloblastoma: an international meta-analysis of transcriptome, genetic aberrations, and clinical data of WNT, SHH, Group 3, and Group 4 medulloblastomas. Acta Neuropathol. 2012, 123 (4): 473-484. 10.1007/s00401-012-0958-8.CrossRefPubMedPubMedCentral Kool M, Korshunov A, Remke M, Jones DT, Schlanstein M, Northcott PA, Cho YJ, Koster J, Schouten-van Meeteren A, van Vuurden D, et al: Molecular subgroups of medulloblastoma: an international meta-analysis of transcriptome, genetic aberrations, and clinical data of WNT, SHH, Group 3, and Group 4 medulloblastomas. Acta Neuropathol. 2012, 123 (4): 473-484. 10.1007/s00401-012-0958-8.CrossRefPubMedPubMedCentral
13.
go back to reference Northcott PA, Korshunov A, Witt H, Hielscher T, Eberhart CG, Mack S, Bouffet E, Clifford SC, Hawkins CE, French P, et al: Medulloblastoma comprises four distinct molecular variants. J Clin Oncol. 2011, 29 (11): 1408-1414. 10.1200/JCO.2009.27.4324.CrossRefPubMed Northcott PA, Korshunov A, Witt H, Hielscher T, Eberhart CG, Mack S, Bouffet E, Clifford SC, Hawkins CE, French P, et al: Medulloblastoma comprises four distinct molecular variants. J Clin Oncol. 2011, 29 (11): 1408-1414. 10.1200/JCO.2009.27.4324.CrossRefPubMed
14.
go back to reference Parsons DW, Li M, Zhang X, Jones S, Leary RJ, Lin JC, Boca SM, Carter H, Samayoa J, Bettegowda C, et al: The genetic landscape of the childhood cancer medulloblastoma. Science. 2011, 331 (6016): 435-439. 10.1126/science.1198056.CrossRefPubMed Parsons DW, Li M, Zhang X, Jones S, Leary RJ, Lin JC, Boca SM, Carter H, Samayoa J, Bettegowda C, et al: The genetic landscape of the childhood cancer medulloblastoma. Science. 2011, 331 (6016): 435-439. 10.1126/science.1198056.CrossRefPubMed
15.
go back to reference Wu X, Northcott PA, Dubuc A, Dupuy AJ, Shih DJ, Witt H, Croul S, Bouffet E, Fults DW, Eberhart CG, et al: Clonal selection drives genetic divergence of metastatic medulloblastoma. Nature. 2012, 482 (7386): 529-533. 10.1038/nature10825.CrossRefPubMedPubMedCentral Wu X, Northcott PA, Dubuc A, Dupuy AJ, Shih DJ, Witt H, Croul S, Bouffet E, Fults DW, Eberhart CG, et al: Clonal selection drives genetic divergence of metastatic medulloblastoma. Nature. 2012, 482 (7386): 529-533. 10.1038/nature10825.CrossRefPubMedPubMedCentral
16.
go back to reference Mumert M, Dubuc A, Wu X, Northcott PA, Chin SS, Pedone CA, Taylor MD, Fults DW: Functional genomics identifies drivers of medulloblastoma dissemination. Cancer Res. 2012, 72 (19): 4944-4953. 10.1158/0008-5472.CAN-12-1629.CrossRefPubMedPubMedCentral Mumert M, Dubuc A, Wu X, Northcott PA, Chin SS, Pedone CA, Taylor MD, Fults DW: Functional genomics identifies drivers of medulloblastoma dissemination. Cancer Res. 2012, 72 (19): 4944-4953. 10.1158/0008-5472.CAN-12-1629.CrossRefPubMedPubMedCentral
17.
go back to reference Zhou L, Picard D, Ra YS, Li M, Northcott PA, Hu Y, Stearns D, Hawkins C, Taylor MD, Rutka J, et al: Silencing of thrombospondin-1 is critical for myc-induced metastatic phenotypes in medulloblastoma. Cancer Res. 2010, 70 (20): 8199-8210. 10.1158/0008-5472.CAN-09-4562.CrossRefPubMed Zhou L, Picard D, Ra YS, Li M, Northcott PA, Hu Y, Stearns D, Hawkins C, Taylor MD, Rutka J, et al: Silencing of thrombospondin-1 is critical for myc-induced metastatic phenotypes in medulloblastoma. Cancer Res. 2010, 70 (20): 8199-8210. 10.1158/0008-5472.CAN-09-4562.CrossRefPubMed
18.
go back to reference Bai AH, Milde T, Remke M, Rolli CG, Hielscher T, Cho YJ, Kool M, Northcott PA, Jugold M, Bazhin AV, et al: MicroRNA-182 promotes leptomeningeal spread of non-sonic hedgehog-medulloblastoma. Acta Neuropathol. 2012, 123 (4): 529-538. 10.1007/s00401-011-0924-x.CrossRefPubMed Bai AH, Milde T, Remke M, Rolli CG, Hielscher T, Cho YJ, Kool M, Northcott PA, Jugold M, Bazhin AV, et al: MicroRNA-182 promotes leptomeningeal spread of non-sonic hedgehog-medulloblastoma. Acta Neuropathol. 2012, 123 (4): 529-538. 10.1007/s00401-011-0924-x.CrossRefPubMed
19.
go back to reference Perk J, Iavarone A, Benezra R: Id family of helix-loop-helix proteins in cancer. Nat Rev Cancer. 2005, 5 (8): 603-614. 10.1038/nrc1673.CrossRefPubMed Perk J, Iavarone A, Benezra R: Id family of helix-loop-helix proteins in cancer. Nat Rev Cancer. 2005, 5 (8): 603-614. 10.1038/nrc1673.CrossRefPubMed
20.
go back to reference Sikder HA, Devlin MK, Dunlap S, Ryu B, Alani RM: Id proteins in cell growth and tumorigenesis. Cancer Cell. 2003, 3 (6): 525-530. 10.1016/S1535-6108(03)00141-7.CrossRefPubMed Sikder HA, Devlin MK, Dunlap S, Ryu B, Alani RM: Id proteins in cell growth and tumorigenesis. Cancer Cell. 2003, 3 (6): 525-530. 10.1016/S1535-6108(03)00141-7.CrossRefPubMed
21.
go back to reference Asirvatham AJ, Carey JP, Chaudhary J: ID1-, ID2-, and ID3-regulated gene expression in E2A positive or negative prostate cancer cells. Prostate. 2007, 67 (13): 1411-1420. 10.1002/pros.20633.CrossRefPubMed Asirvatham AJ, Carey JP, Chaudhary J: ID1-, ID2-, and ID3-regulated gene expression in E2A positive or negative prostate cancer cells. Prostate. 2007, 67 (13): 1411-1420. 10.1002/pros.20633.CrossRefPubMed
22.
go back to reference Hu YC, Lam KY, Law S, Wong J, Srivastava G: Identification of differentially expressed genes in esophageal squamous cell carcinoma (ESCC) by cDNA expression array: overexpression of Fra-1, Neogenin, Id-1, and CDC25B genes in ESCC. Clin Cancer Res. 2001, 7 (8): 2213-2221.PubMed Hu YC, Lam KY, Law S, Wong J, Srivastava G: Identification of differentially expressed genes in esophageal squamous cell carcinoma (ESCC) by cDNA expression array: overexpression of Fra-1, Neogenin, Id-1, and CDC25B genes in ESCC. Clin Cancer Res. 2001, 7 (8): 2213-2221.PubMed
23.
go back to reference Lin CQ, Singh J, Murata K, Itahana Y, Parrinello S, Liang SH, Gillett CE, Campisi J, Desprez PY: A role for Id-1 in the aggressive phenotype and steroid hormone response of human breast cancer cells. Cancer Res. 2000, 60 (5): 1332-1340.PubMed Lin CQ, Singh J, Murata K, Itahana Y, Parrinello S, Liang SH, Gillett CE, Campisi J, Desprez PY: A role for Id-1 in the aggressive phenotype and steroid hormone response of human breast cancer cells. Cancer Res. 2000, 60 (5): 1332-1340.PubMed
24.
go back to reference Okaji Y, Tsuno NH, Kitayama J, Sakurai D, Tsuchiya N, Saito S, Takegami K, Tsuchiya T, Kawai K, Yazawa K, et al: Effects of down-regulating the Id genes in human colorectal cancer cells on early steps of haematogenous metastasis. Eur J Cancer. 2006, 42 (5): 668-673. 10.1016/j.ejca.2005.11.016.CrossRefPubMed Okaji Y, Tsuno NH, Kitayama J, Sakurai D, Tsuchiya N, Saito S, Takegami K, Tsuchiya T, Kawai K, Yazawa K, et al: Effects of down-regulating the Id genes in human colorectal cancer cells on early steps of haematogenous metastasis. Eur J Cancer. 2006, 42 (5): 668-673. 10.1016/j.ejca.2005.11.016.CrossRefPubMed
25.
go back to reference Shuno Y, Tsuno NH, Okaji Y, Tsuchiya T, Sakurai D, Nishikawa T, Yoshikawa N, Sasaki K, Hongo K, Tsurita G, et al: Id1/Id3 knockdown inhibits metastatic potential of pancreatic cancer. J Surg Res. 2010, 161 (1): 76-82. 10.1016/j.jss.2008.10.031.CrossRefPubMed Shuno Y, Tsuno NH, Okaji Y, Tsuchiya T, Sakurai D, Nishikawa T, Yoshikawa N, Sasaki K, Hongo K, Tsurita G, et al: Id1/Id3 knockdown inhibits metastatic potential of pancreatic cancer. J Surg Res. 2010, 161 (1): 76-82. 10.1016/j.jss.2008.10.031.CrossRefPubMed
26.
go back to reference Gupta GP, Perk J, Acharyya S, de Candia P, Mittal V, Todorova-Manova K, Gerald WL, Brogi E, Benezra R, Massague J: ID genes mediate tumor reinitiation during breast cancer lung metastasis. Proc Natl Acad Sci U S A. 2007, 104 (49): 19506-19511. 10.1073/pnas.0709185104.CrossRefPubMedPubMedCentral Gupta GP, Perk J, Acharyya S, de Candia P, Mittal V, Todorova-Manova K, Gerald WL, Brogi E, Benezra R, Massague J: ID genes mediate tumor reinitiation during breast cancer lung metastasis. Proc Natl Acad Sci U S A. 2007, 104 (49): 19506-19511. 10.1073/pnas.0709185104.CrossRefPubMedPubMedCentral
27.
go back to reference Livak KJ, Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) Method. Methods. 2001, 25 (4): 402-408. 10.1006/meth.2001.1262.CrossRefPubMed Livak KJ, Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) Method. Methods. 2001, 25 (4): 402-408. 10.1006/meth.2001.1262.CrossRefPubMed
28.
go back to reference Phi JH, Park SH, Kim SK, Paek SH, Kim JH, Lee YJ, Cho BK, Park CK, Lee DH, Wang KC: Sox2 expression in brain tumors: a reflection of the neuroglial differentiation pathway. Am J Surg Pathol. 2008, 32 (1): 103-112. 10.1097/PAS.0b013e31812f6ba6.CrossRefPubMed Phi JH, Park SH, Kim SK, Paek SH, Kim JH, Lee YJ, Cho BK, Park CK, Lee DH, Wang KC: Sox2 expression in brain tumors: a reflection of the neuroglial differentiation pathway. Am J Surg Pathol. 2008, 32 (1): 103-112. 10.1097/PAS.0b013e31812f6ba6.CrossRefPubMed
29.
go back to reference Shimato S, Natsume A, Takeuchi H, Wakabayashi T, Fujii M, Ito M, Ito S, Park IH, Bang JH, Kim SU, et al: Human neural stem cells target and deliver therapeutic gene to experimental leptomeningeal medulloblastoma. Gene Ther. 2007, 14 (15): 1132-1142. 10.1038/sj.gt.3302932.CrossRefPubMed Shimato S, Natsume A, Takeuchi H, Wakabayashi T, Fujii M, Ito M, Ito S, Park IH, Bang JH, Kim SU, et al: Human neural stem cells target and deliver therapeutic gene to experimental leptomeningeal medulloblastoma. Gene Ther. 2007, 14 (15): 1132-1142. 10.1038/sj.gt.3302932.CrossRefPubMed
30.
go back to reference Northcott PA, Shih DJ, Peacock J, Garzia L, Morrissy AS, Zichner T, Stutz AM, Korshunov A, Reimand J, Schumacher SE, et al: Subgroup-specific structural variation across 1,000 medulloblastoma genomes. Nature. 2012, 488 (7409): 49-56. 10.1038/nature11327.CrossRefPubMedPubMedCentral Northcott PA, Shih DJ, Peacock J, Garzia L, Morrissy AS, Zichner T, Stutz AM, Korshunov A, Reimand J, Schumacher SE, et al: Subgroup-specific structural variation across 1,000 medulloblastoma genomes. Nature. 2012, 488 (7409): 49-56. 10.1038/nature11327.CrossRefPubMedPubMedCentral
31.
go back to reference Yan W, Young AZ, Soares VC, Kelley R, Benezra R, Zhuang Y: High incidence of T-cell tumors in E2A-null mice and E2A/Id1 double-knockout mice. Mol Cell Biol. 1997, 17 (12): 7317-7327.CrossRefPubMedPubMedCentral Yan W, Young AZ, Soares VC, Kelley R, Benezra R, Zhuang Y: High incidence of T-cell tumors in E2A-null mice and E2A/Id1 double-knockout mice. Mol Cell Biol. 1997, 17 (12): 7317-7327.CrossRefPubMedPubMedCentral
32.
go back to reference Loveys DA, Streiff MB, Kato GJ: E2A basic-helix-loop-helix transcription factors are negatively regulated by serum growth factors and by the Id3 protein. Nucleic Acids Res. 1996, 24 (14): 2813-2820. 10.1093/nar/24.14.2813.CrossRefPubMedPubMedCentral Loveys DA, Streiff MB, Kato GJ: E2A basic-helix-loop-helix transcription factors are negatively regulated by serum growth factors and by the Id3 protein. Nucleic Acids Res. 1996, 24 (14): 2813-2820. 10.1093/nar/24.14.2813.CrossRefPubMedPubMedCentral
33.
go back to reference Fong S, Debs RJ, Desprez PY: Id genes and proteins as promising targets in cancer therapy. Trends Mol Med. 2004, 10 (8): 387-392. 10.1016/j.molmed.2004.06.008.CrossRefPubMed Fong S, Debs RJ, Desprez PY: Id genes and proteins as promising targets in cancer therapy. Trends Mol Med. 2004, 10 (8): 387-392. 10.1016/j.molmed.2004.06.008.CrossRefPubMed
34.
go back to reference Anido J, Saez-Borderias A, Gonzalez-Junca A, Rodon L, Folch G, Carmona MA, Prieto-Sanchez RM, Barba I, Martinez-Saez E, Prudkin L, et al: TGF-beta receptor inhibitors target the CD44(high)/Id1(high) glioma-initiating cell population in human glioblastoma. Cancer Cell. 2010, 18 (6): 655-668. 10.1016/j.ccr.2010.10.023.CrossRefPubMed Anido J, Saez-Borderias A, Gonzalez-Junca A, Rodon L, Folch G, Carmona MA, Prieto-Sanchez RM, Barba I, Martinez-Saez E, Prudkin L, et al: TGF-beta receptor inhibitors target the CD44(high)/Id1(high) glioma-initiating cell population in human glioblastoma. Cancer Cell. 2010, 18 (6): 655-668. 10.1016/j.ccr.2010.10.023.CrossRefPubMed
35.
go back to reference Li B, Tsao SW, Li YY, Wang X, Ling MT, Wong YC, He QY, Cheung AL: Id-1 promotes tumorigenicity and metastasis of human esophageal cancer cells through activation of PI3K/AKT signaling pathway. Int J Cancer. 2009, 125 (11): 2576-2585. 10.1002/ijc.24675.CrossRefPubMed Li B, Tsao SW, Li YY, Wang X, Ling MT, Wong YC, He QY, Cheung AL: Id-1 promotes tumorigenicity and metastasis of human esophageal cancer cells through activation of PI3K/AKT signaling pathway. Int J Cancer. 2009, 125 (11): 2576-2585. 10.1002/ijc.24675.CrossRefPubMed
36.
go back to reference Cheung PY, Yip YL, Tsao SW, Ching YP, Cheung AL: Id-1 induces cell invasiveness in immortalized epithelial cells by regulating cadherin switching and Rho GTPases. J Cell Biochem. 2011, 112 (1): 157-168. 10.1002/jcb.22911.CrossRefPubMed Cheung PY, Yip YL, Tsao SW, Ching YP, Cheung AL: Id-1 induces cell invasiveness in immortalized epithelial cells by regulating cadherin switching and Rho GTPases. J Cell Biochem. 2011, 112 (1): 157-168. 10.1002/jcb.22911.CrossRefPubMed
37.
go back to reference Coma S, Amin DN, Shimizu A, Lasorella A, Iavarone A, Klagsbrun M: Id2 promotes tumor cell migration and invasion through transcriptional repression of semaphorin 3F. Cancer Res. 2010, 70 (9): 3823-3832. 10.1158/0008-5472.CAN-09-3048.CrossRefPubMedPubMedCentral Coma S, Amin DN, Shimizu A, Lasorella A, Iavarone A, Klagsbrun M: Id2 promotes tumor cell migration and invasion through transcriptional repression of semaphorin 3F. Cancer Res. 2010, 70 (9): 3823-3832. 10.1158/0008-5472.CAN-09-3048.CrossRefPubMedPubMedCentral
38.
go back to reference Puget S, Grill J, Valent A, Bieche I, Dantas-Barbosa C, Kauffmann A, Dessen P, Lacroix L, Geoerger B, Job B, et al: Candidate genes on chromosome 9q33-34 involved in the progression of childhood ependymomas. J Clin Oncol. 2009, 27 (11): 1884-1892. 10.1200/JCO.2007.15.4195.CrossRefPubMed Puget S, Grill J, Valent A, Bieche I, Dantas-Barbosa C, Kauffmann A, Dessen P, Lacroix L, Geoerger B, Job B, et al: Candidate genes on chromosome 9q33-34 involved in the progression of childhood ependymomas. J Clin Oncol. 2009, 27 (11): 1884-1892. 10.1200/JCO.2007.15.4195.CrossRefPubMed
39.
go back to reference Fiorilli P, Partridge D, Staniszewska I, Wang JY, Grabacka M, So K, Marcinkiewicz C, Reiss K, Khalili K, Croul SE: Integrins mediate adhesion of medulloblastoma cells to tenascin and activate pathways associated with survival and proliferation. Lab Invest. 2008, 88 (11): 1143-1156. 10.1038/labinvest.2008.89.CrossRefPubMedPubMedCentral Fiorilli P, Partridge D, Staniszewska I, Wang JY, Grabacka M, So K, Marcinkiewicz C, Reiss K, Khalili K, Croul SE: Integrins mediate adhesion of medulloblastoma cells to tenascin and activate pathways associated with survival and proliferation. Lab Invest. 2008, 88 (11): 1143-1156. 10.1038/labinvest.2008.89.CrossRefPubMedPubMedCentral
40.
go back to reference Vo DT, Subramaniam D, Remke M, Burton TL, Uren PJ, Gelfond JA, de Sousa AR, Burns SC, Qiao M, Suresh U, et al: The RNA-binding protein Musashi1 affects medulloblastoma growth via a network of cancer-related genes and is an indicator of poor prognosis. Am J Pathol. 2012, 181 (5): 1762-1772. 10.1016/j.ajpath.2012.07.031.CrossRefPubMedPubMedCentral Vo DT, Subramaniam D, Remke M, Burton TL, Uren PJ, Gelfond JA, de Sousa AR, Burns SC, Qiao M, Suresh U, et al: The RNA-binding protein Musashi1 affects medulloblastoma growth via a network of cancer-related genes and is an indicator of poor prognosis. Am J Pathol. 2012, 181 (5): 1762-1772. 10.1016/j.ajpath.2012.07.031.CrossRefPubMedPubMedCentral
Metadata
Title
ID3 contributes to cerebrospinal fluid seeding and poor prognosis in medulloblastoma
Authors
Ji Hoon Phi
Seung Ah Choi
Sang-Hee Lim
Joongyub Lee
Kyu-Chang Wang
Sung-Hye Park
Seung-Ki Kim
Publication date
01-12-2013
Publisher
BioMed Central
Published in
BMC Cancer / Issue 1/2013
Electronic ISSN: 1471-2407
DOI
https://doi.org/10.1186/1471-2407-13-291

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Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine