What is the clinical value of cancer stem cell markers in gliomas?

International Journal of Clinical and Experimental Pathology

Volumn 6, Issue 3, 2013, Pages 334-348

  Dahlrot, Rikke Hedegaard ^a,b   Hermansen, Simon Kjær ^a,b   Hansen, Steinbjørn ^a,b   Kristensen, Bjarne Winther ^a,b  

^a ODENSE UNIVERSITY HOSPITAL   (Denmark)

^b UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

Cancer stem cell; CD133; Glioma; Immunohistochemistry; Nestin; Prognosis

Indexed keywords

CD133 ANTIGEN; GLYCOPROTEIN; INTERMEDIATE FILAMENT PROTEIN; LEUKOCYTE ANTIGEN; NERVE PROTEIN; NESTIN; PEPTIDE; TUMOR MARKER;

BRAIN TUMOR; CANCER STEM CELL; CD133; CELL MEMBRANE; GLIOMA; HUMAN; IMMUNOHISTOCHEMISTRY; MEDLINE; METABOLISM; MORTALITY; PATHOLOGY; PROGNOSIS; REVIEW; SURVIVAL RATE;

CANCER STEM CELL; CD133; GLIOMA; IMMUNOHISTOCHEMISTRY; NESTIN; PROGNOSIS;

ANTIGENS, CD; BRAIN NEOPLASMS; CELL MEMBRANE; GLIOMA; GLYCOPROTEINS; HUMANS; INTERMEDIATE FILAMENT PROTEINS; NEOPLASTIC STEM CELLS; NERVE TISSUE PROTEINS; PEPTIDES; PROGNOSIS; PUBMED; SURVIVAL RATE; TUMOR MARKERS, BIOLOGICAL;

EID: 84881478223     PISSN: None     EISSN: 19362625     Source Type: Journal    
DOI: None     Document Type: Article

References (82)

1. Hegi ME, Diserens AC, Gorlia T, Hamou MF, de TN, Weller M, Kros JM, Hainfellner JA, Mason W, Mariani L, Bromberg JE, Hau P, Mirimanoff RO, Cairncross JG, Janzer RC and Stupp R. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 2005; 352: 997-1003.
2. Bao S, Wu Q, Li Z, Sathornsumetee S, Wang H, McLendon RE, Hjelmeland AB and Rich JN. Targeting cancer stem cells through L1CAM suppresses glioma growth. Cancer Res 2008; 68: 6043-6048.
3. Dean M, Fojo T and Bates S. Tumour stem cells and drug resistance. Nat Rev Cancer 2005; 5: 275-284.
4. Bishop M and de la Monte SM. Dual lineage of astrocytomas. Am J Pathol 1989; 135: 517-527.
5. Chinnaiyan P, Wang M, Rojiani AM, Tofilon PJ, Chakravarti A, Ang KK, Zhang HZ, Hammond E, Curran W Jr and Mehta MP. The prognostic value of nestin expression in newly diagnosed glioblastoma: report from the Radiation Therapy Oncology Group. Radiat Oncol 2008; 3: 32.
6. Christensen K, Schroeder HD and Kristensen BW. CD133 identifies perivascular niches in grade II-IV astrocytomas. J Neurooncol 2008; 90: 157-170.
7. Dahlstrand J, Collins VP and Lendahl U. Expression of the class VI intermediate filament nestin in human central nervous system tumors. Cancer Res 1992; 52: 5334-5341.
8. Du Z, Jia D, Liu S, Wang F, Li G, Zhang Y, Cao X, Ling EA and Hao A. Oct4 is expressed in human gliomas and promotes colony formation in glioma cells. Glia 2009; 57: 724-733.
9. Ehrmann J, Kolar Z and Mokry J. Nestin as a diagnostic and prognostic marker: immunohistochemical analysis of its expression in different tumours. J Clin Pathol 2005; 58: 222-223.
10. Ernst A, Hofmann S, Ahmadi R, Becker N, Korshunov A, Engel F, Hartmann C, Felsberg J, Sabel M, Peterziel H, Durchdewald M, Hess J, Barbus S, Campos B, Starzinski-Powitz A, Unterberg A, Reifenberger G, Lichter P, Herold-Mende C and Radlwimmer B. Genomic and expression profiling of glioblastoma stem celllike spheroid cultures identifies novel tumorrelevant genes associated with survival. Clin Cancer Res 2009; 15: 6541-6550.
11. Hayry V, Tynninen O, Haapasalo HK, Wolfer J, Paulus W, Hasselblatt M, Sariola H, Paetau A, Sarna S, Niemela M, Wartiovaara K and Nupponen NN. Stem cell protein BMI-1 is an independent marker for poor prognosis in oligodendroglial tumours. Neuropathol Appl Neurobiol 2008; 34: 555-563.
12. Kanemura Y, Mori K, Sakakibara S, Fujikawa H, Hayashi H, Nakano A, Matsumoto T, Tamura K, Imai T, Ohnishi T, Fushiki S, Nakamura Y, Yamasaki M, Okano H and Arita N. Musashi1, an evolutionarily conserved neural RNA-binding protein, is a versatile marker of human glioma cells in determining their cellular origin, malignancy, and proliferative activity. Differentiation 2001; 68: 141-152.
13. Kim KJ, Lee KH, Kim HS, Moon KS, Jung TY, Jung S and Lee MC. The presence of stem cell marker-expressing cells is not prognostically significant in glioblastomas. Neuropathology 2011 Oct; 31: 494-502.
14. Ma YH, Mentlein R, Knerlich F, Kruse ML, Mehdorn HM and Held-Feindt J. Expression of stem cell markers in human astrocytomas of different WHO grades. J Neurooncol 2008; 86: 31-45.
15. Maderna E, Salmaggi A, Calatozzolo C, Limido L and Pollo B. Nestin, PDGFRbeta, CXCL12 and VEGF in glioma patients: different profiles of (pro-angiogenic) molecule expression are related with tumor grade and may provide prognostic information. Cancer Biol Ther 2007; 6: 1018-1024.
16. Mishima K, Kato Y, Kaneko MK, Nishikawa R, Hirose T and Matsutani M. Increased expression of podoplanin in malignant astrocytic tumors as a novel molecular marker of malignant progression. Acta Neuropathol 2006; 111: 483-488.
17. Pallini R, Ricci-Vitiani L, Banna GL, Signore M, Lombardi D, Todaro M, Stassi G, Martini M, Maira G, Larocca LM and De MR. Cancer stem cell analysis and clinical outcome in patients with glioblastoma multiforme. Clin Cancer Res 2008; 14: 8205-8212.
18. Phi JH, Park SH, Kim SK, Paek SH, Kim JH, Lee YJ, Cho BK, Park CK, Lee DH and Wang KC. Sox2 expression in brain tumors: a reflection of the neuroglial differentiation pathway. Am J Surg Pathol 2008; 32: 103-112.
19. Piepmeier JM, Fried I and Makuch R. Lowgrade astrocytomas may arise from different astrocyte lineages. Neurosurgery 1993; 33: 627-632.
20. Strojnik T, Rosland GV, Sakariassen PO, Kavalar R and Lah T. Neural stem cell markers, nestin and musashi proteins, in the progression of human glioma: correlation of nestin with prognosis of patient survival. Surg Neurol 2007; 68: 133-143.
21. Thon N, Damianoff K, Hegermann J, Grau S, Krebs B, Schnell O, Tonn JC and Goldbrunner R. Presence of pluripotent CD133+ cells correlates with malignancy of gliomas. Mol Cell Neurosci 2010; 43: 51-59.
22. Tirabosco R, De MG, Skrap M, Falconieri G and Pizzolitto S. Expression of the Polycomb-Group protein BMI1 and correlation with p16 in astrocytomas an immunohistochemical study on 80 cases. Pathol Res Pract 2008; 204: 625-631.
23. Toda M, Iizuka Y, Yu W, Imai T, Ikeda E, Yoshida K, Kawase T, Kawakami Y, Okano H and Uyemura K. Expression of the neural RNA-binding protein Musashi1 in human gliomas. Glia 2001; 34: 1-7.
24. Vandeputte DA, Troost D, Leenstra S, Ijlst-Keizers H, Ramkema M, Bosch DA, Baas F, Das NK and Aronica E. Expression and distribution of id helix-loop-helix proteins in human astrocytic tumors. Glia 2002; 38: 329-338.
25. Wan F, Herold-Mende C, Campos B, Centner FS, Dictus C, Becker N, Devens F, Mogler C, Felsberg J, Grabe N, Reifenberger G, Lichter P, Unterberg A, Bermejo JL and Ahmadi R. Association of stem cell-related markers and survival in astrocytic gliomas. Biomarkers 2011; 16: 136-143.
26. Zeppernick F, Ahmadi R, Campos B, Dictus C, Helmke BM, Becker N, Lichter P, Unterberg A, Radlwimmer B and Herold-Mende CC. Stem cell marker CD133 affects clinical outcome in glioma patients. Clin Cancer Res 2008; 14: 123-129.
27. Zhang M, Song T, Yang L, Chen R, Wu L, Yang Z and Fang J. Nestin and CD133: valuable stem cell-specific markers for determining clinical outcome of glioma patients. J Exp Clin Cancer Res 2008; 27: 85.
28. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ and Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A 2003; 100: 3983-3988.
29. Lapidot T, Sirard C, Vormoor J, Murdoch B, Hoang T, Caceres-Cortes J, Minden M, Paterson B, Caligiuri MA and Dick JE. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 1994; 367: 645-648.
30. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J and Dirks PB. Identification of a cancer stem cell in human brain tumors. Cancer Res 2003; 63: 5821-5828.
31. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, Henkelman RM, Cusimano MD and Dirks PB. Identification of human brain tumour initiating cells. Nature 2004; 432: 396-401.
32. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, Dewhirst MW, Bigner DD and Rich JN. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006; 444: 756-760.
33. Collins AT and Maitland NJ. Prostate cancer stem cells. Eur J Cancer 2006; 42: 1213-1218.
34. Ricci-Vitiani L, Lombardi DG, Pilozzi E, Biffoni M, Todaro M, Peschle C and De MR. Identification and expansion of human colon-cancer-initiating cells. Nature 2007; 445: 111-115.
35. Bonnet D and Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 1997; 3: 730-737.
36. Galli R, Binda E, Orfanelli U, Cipelletti B, Gritti A, De VS, Fiocco R, Foroni C, Dimeco F and Vescovi A. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res 2004; 64: 7011-7021.
37. Pfenninger CV, Roschupkina T, Hertwig F, Kottwitz D, Englund E, Bengzon J, Jacobsen SE and Nuber UA. CD133 is not present on neurogenic astrocytes in the adult subventricular zone, but on embryonic neural stem cells, ependymal cells, and glioblastoma cells. Cancer Res 2007; 67: 5727-5736.
38. Wang J, Sakariassen PO, Tsinkalovsky O, Immervoll H, Boe SO, Svendsen A, Prestegarden L, Rosland G, Thorsen F, Stuhr L, Molven A, Bjerkvig R and Enger PO. CD133 negative glioma cells form tumors in nude rats and give rise to CD133 positive cells. Int J Cancer 2008; 122: 761-768.
39. Ogasawara S, Kaneko MK, Price JE and Kato Y. Characterization of anti-podoplanin monoclonal antibodies: critical epitopes for neutralizing the interaction between podoplanin and CLEC- 2. Hybridoma (Larchmt) 2008; 27: 259-267.
40. Ordonez NG. Podoplanin: a novel diagnostic immunohistochemical marker. Adv Anat Pathol 2006; 13: 83-88.
41. Shibahara J, Kashima T, Kikuchi Y, Kunita A and Fukayama M. Podoplanin is expressed in subsets of tumors of the central nervous system. Virchows Arch 2006; 448: 493-499.
42. Wicki A, Lehembre F, Wick N, Hantusch B, Kerjaschki D and Christofori G. Tumor invasion in the absence of epithelial-mesenchymal transition: podoplanin-mediated remodeling of the actin cytoskeleton. Cancer Cell 2006; 9: 261-272.
43. Sulman E, Goodman LD, Le TT, Pelloski CE, Bhat K, Gumin J, Lang FF and Adape K. A novel marker of glioma stem cells that is prognostic for treatment respons and patient outcome. Proceedings of the 99th Annual Meeting of the American Association for Cancer Research; 2008 Apr 12-16; San Diego, CA. Philadelphia (PA): Abstract nr 3777.
44. Reifenberger G, Sieth P, Niederhaus M and Wechsler W. Expression of CD15 in tumours of the nervous system. Histochem J 1992; 24: 890-901.
45. Mao XG, Zhang X, Xue XY, Guo G, Wang P, Zhang W, Fei Z, Zhen HN, You SW and Yang H. Brain Tumor Stem-Like Cells Identified by Neural Stem Cell Marker CD15. Transl Oncol 2009; 2: 247-257.
46. Read TA, Fogarty MP, Markant SL, McLendon RE, Wei Z, Ellison DW, Febbo PG and Wechsler-Reya RJ. Identification of CD15 as a marker for tumor-propagating cells in a mouse model of medulloblastoma. Cancer Cell 2009; 15: 135-147.
47. Son MJ, Woolard K, Nam DH, Lee J and Fine HA. SSEA-1 is an enrichment marker for tumorinitiating cells in human glioblastoma. Cell Stem Cell 2009; 4: 440-452.
48. Balik V, Mirossay P, Bohus P, Sulla I, Mirossay L and Sarissky M. Flow cytometry analysis of neural differentiation markers expression in human glioblastomas may predict their response to chemotherapy. Cell Mol Neurobiol 2009; 29: 845-858.
49. Tchoghandjian A, Baeza N, Colin C, Cayre M, Metellus P, Beclin C, Ouafik L and Figarella-Branger D. A2B5 cells from human glioblastoma have cancer stem cell properties. Brain Pathol 2010; 20: 211-221.
50. Almqvist PM, Mah R, Lendahl U, Jacobsson B and Hendson G. Immunohistochemical detection of nestin in pediatric brain tumors. J Histochem Cytochem 2002; 50: 147-158.
51. Mangiola A, Lama G, Giannitelli C, De BP, Anile C, Lauriola L, La TG, Sabatino G, Maira G, Jhanwar-Uniyal M and Sica G. Stem cell marker nestin and c-Jun NH2-terminal kinases in tumor and peritumor areas of glioblastoma multiforme: possible prognostic implications. Clin Cancer Res 2007; 13: 6970-6977.
52. Wei LC, Shi M, Cao R, Chen LW and Chan YS. Nestin small interfering RNA (siRNA) reduces cell growth in cultured astrocytoma cells. Brain Res 2008; 1196: 103-112.
53. Yang XH, Wu QL, Yu XB, Xu CX, Ma BF, Zhang XM, Li SN, Lahn BT and Xiang AP. Nestin expression in different tumours and its relevance to malignant grade. J Clin Pathol 2008; 61: 467-473.
54. Dell'Albani P. Stem cell markers in gliomas. Neurochem Res 2008; 33: 2407-2415.
55. Arai H, Ikota H, Sugawara K, Nobusawa S, Hirato J and Nakazato Y. Nestin expression in brain tumors: its utility for pathological diagnosis and correlation with the prognosis of highgrade gliomas. Brain Tumor Pathol 2012; 29: 160-167.
56. Kanamori M, Kumabe T, Sonoda Y, Nishino Y, Watanabe M and Tominaga T. Predictive factors for overall and progression-free survival, and dissemination in oligodendroglial tumors. J Neurooncol 2009; 93: 219-228.
57. Good P, Yoda A, Sakakibara S, Yamamoto A, Imai T, Sawa H, Ikeuchi T, Tsuji S, Satoh H and Okano H. The human Musashi homolog 1 (MSI1) gene encoding the homologue of Musashi/Nrp-1, a neural RNA-binding protein putatively expressed in CNS stem cells and neural progenitor cells. Genomics 1998; 52: 382-384.
58. Nakano A, Kanemura Y, Mori K, Kodama E, Yamamoto A, Sakamoto H, Nakamura Y, Okano H, Yamasaki M and Arita N. Expression of the Neural RNA-binding protein Musashi1 in pediatric brain tumors. Pediatr Neurosurg 2007; 43: 279-284.
59. Hemmati HD, Nakano I, Lazareff JA, Masterman-Smith M, Geschwind DH, Bronner-Fraser M and Kornblum HI. Cancerous stem cells can arise from pediatric brain tumors. Proc Natl Acad Sci U S A 2003; 100: 15178-15183.
60. Abdouh M, Facchino S, Chatoo W, Balasingam V, Ferreira J and Bernier G. BMI1 sustains human glioblastoma multiforme stem cell renewal. J Neurosci 2009; 29: 8884-8896.
61. Venugopal C, Li N, Wang X, Manoranjan B, Hawkins C, Gunnarsson T, Hollenberg R, Klurfan P, Murty N, Kwiecien J, Farrokhyar F, Provias JP, Wynder C and Singh SK. Bmi1 marks intermediate precursors during differentiation of human brain tumor initiating cells. Stem Cell Res 2012; 8: 141-153.
62. Brandes AA, Tosoni A, Cavallo G, Reni M, Franceschi E, Bonaldi L, Bertorelle R, Gardiman M, Ghimenton C, Iuzzolino P, Pession A, Blatt V and Ermani M. J Clin Oncol 2006; 24: 4746-4753.
63. Cairncross G and Jenkins R. Gliomas with 1p/19q codeletion: a.k.a. oligodendroglioma. Cancer J 2008; 14: 352-357.
64. Jenkins RB, Blair H, Ballman KV, Giannini C, Arusell RM, Law M, Flynn H, Passe S, Felten S, Brown PD, Shaw EG and Buckner JC. A t(1;19) (q10;p10) mediates the combined deletions of 1p and 19q and predicts a better prognosis of patients with oligodendroglioma. Cancer Res 2006; 66: 9852-9861.
65. Kanner AA, Staugaitis SM, Castilla EA, Chernova O, Prayson RA, Vogelbaum MA, Stevens G, Peereboom D, Suh J, Lee SY, Tubbs RR and Barnett GH. The impact of genotype on outcome in oligodendroglioma: validation of the loss of chromosome arm 1p as an important factor in clinical decision making. J Neurosurg 2006; 104: 542-550.
66. Walker C, Haylock B, Husband D, Joyce KA, Fildes D, Jenkinson MD, Smith T, Broome J, du Plessis DG and Warnke PC. Clinical use of genotype to predict chemosensitivity in oligodendroglial tumors. Neurology 2006; 66: 1661-1667.
67. Cenci T, Martini M, Montano N, D'Alessandris QG, Falchetti ML, Annibali D, Savino M, Bianchi F, Pierconti F, Nasi S, Pallini R and Larocca LM. Prognostic relevance of c-Myc and BMI1 expression in patients with glioblastoma. Am J Clin Pathol 2012; 138: 390-396.
68. Gangemi RM, Griffero F, Marubbi D, Perera M, Capra MC, Malatesta P, Ravetti GL, Zona GL, Daga A and Corte G. SOX2 silencing in glioblastoma tumor-initiating cells causes stop of proliferation and loss of tumorigenicity. Stem Cells 2009; 27: 40-48.
69. Iavarone A and Lasorella A. ID proteins as targets in cancer and tools in neurobiology. Trends Mol Med 2006; 12: 588-594.
70. Phi JH, Kim JH, Eun KM, Wang KC, Park KH, Choi SA, Kim YY, Park SH, Cho BK and Kim SK. Upregulation of SOX2, NOTCH1, and ID1 in supratentorial primitive neuroectodermal tumors: a distinct differentiation pattern from that of medulloblastomas. J Neurosurg Pediatr 2010; 5: 608-614.
71. Anido J, Saez-Borderias A, Gonzalez-Junca A, Rodon L, Folch G, Carmona MA, Prieto-Sanchez RM, Barba I, Martinez-Saez E, Prudkin L, Cuartas I, Raventos C, Martinez-Ricarte F, Poca MA, Garcia-Dorado D, Lahn MM, Yingling JM, Rodon J, Sahuquillo J, Baselga J and Seoane J. TGF-beta Receptor Inhibitors Target the CD44(high)/Id1(high) Glioma-Initiating Cell Population in Human Glioblastoma. Cancer Cell 2010; 18: 655-668.
72. Atlasi Y, Mowla SJ, Ziaee SA, Gokhale PJ and Andrews PW. OCT4 spliced variants are differentially expressed in human pluripotent and nonpluripotent cells. Stem Cells 2008; 26: 3068-3074.
73. Chen YC, Hsu HS, Chen YW, Tsai TH, How CK, Wang CY, Hung SC, Chang YL, Tsai ML, Lee YY, Ku HH and Chiou SH. Oct-4 expression maintained cancer stem-like properties in lung cancer- derived CD133-positive cells. PLoS One 2008; 3: e2637.
74. Seigel GM, Hackam AS, Ganguly A, Mandell LM and Gonzalez-Fernandez F. Human embryonic and neuronal stem cell markers in retinoblastoma. Mol Vis 2007; 13: 823-832.
75. Beier D, Wischhusen J, Dietmaier W, Hau P, Proescholdt M, Brawanski A, Bogdahn U and Beier CP. CD133 expression and cancer stem cells predict prognosis in high-grade oligodendroglial tumors. Brain Pathol 2008; 18: 370-377.
76. Hermansen SK, Christensen KG, Jensen SS and Kristensen BW. Inconsistent Immunohistochemical Expression Patterns of Four Different CD133 Antibody Clones in Glioblastoma. J Histochem Cytochem 2011; 59: 391-407.
77. Gaspar L, Scott C, Rotman M, Asbell S, Phillips T, Wasserman T, McKenna WG and Byhardt R. Recursive partitioning analysis (RPA) of prognostic factors in three Radiation Therapy Oncology Group (RTOG) brain metastases trials. Int J Radiat Oncol Biol Phys 1997; 37: 745-751.
78. Altman DG and Lyman GH. Methodological challenges in the evaluation of prognostic factors in breast cancer. Breast Cancer Res Treat 1998; 52: 289-303.
79. Hayes DF, Bast RC, Desch CE, Fritsche H Jr, Kemeny NE, Jessup JM, Locker GY, Macdonald JS, Mennel RG, Norton L, Ravdin P, Taube S and Winn RJ. Tumor marker utility grading system: a framework to evaluate clinical utility of tumor markers. J Natl Cancer Inst 1996; 88: 1456-1466.
80. Hayes DF, Trock B and Harris AL. Assessing the clinical impact of prognostic factors: when is "statistically significant" clinically useful? Breast Cancer Res Treat 1998; 52: 305-319.
81. McShane LM, Altman DG, Sauerbrei W, Taube SE, Gion M and Clark GM. REporting recommendations for tumor MARKer prognostic studies (REMARK). Nat Clin Pract Oncol 2005; 2: 416-422.
82. Christensen BC, Smith AA, Zheng S, Koestler DC, Houseman EA, Marsit CJ, Wiemels JL, Nelson HH, Karagas MR, Wrensch MR, Kelsey KT and Wiencke JK. DNA methylation, isocitrate dehydrogenase mutation, and survival in glioma. J Natl Cancer Inst 2011; 103: 143-153.