Tumor microtubes convey resistance to surgical lesions and chemotherapy in gliomas

Neuro-Oncology

Volumn 19, Issue 10, 2017, Pages 1316-1326

  Weil, Sophie ^a,b   Osswald, Matthias ^a,b   Solecki, Gergely ^a,b   Grosch, Julia ^b   Jung, Erik ^a,b   Lemke, Dieter ^a,b   Ratliff, Miriam ^b,c   Hänggi, Daniel ^c   Wick, Wolfgang ^a,b   Winkler, Frank ^a,b  

^a UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Chemotherapy; Glioma; Resistance; Surgery; Tumor microtubes

Indexed keywords

DEXAMETHASONE; NEUROMODULIN; TEMOZOLOMIDE; ALKYLATING AGENT; DACARBAZINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DAMAGE; BRAIN REGION; BRAIN SURGERY; CANCER CHEMOTHERAPY; CANCER GROWTH; CANCER INHIBITION; CANCER RESISTANCE; CANCER SURGERY; CELL DENSITY; CELL HETEROGENEITY; CELL POPULATION; CONTROLLED STUDY; DRUG EFFECT; DRUG MEGADOSE; ENCEPHALITIS; GLIOBLASTOMA CELL LINE; GLIOMA; GLIOMA STEM CELL; HUMAN; HUMAN CELL; IN VIVO STUDY; LASER MICROSCOPY; LONGITUDINAL STUDY; MALE; MEMBRANE STRUCTURE; MOUSE; NONHUMAN; TREATMENT RESPONSE; TUMOR MICROTUBE; ANALOGS AND DERIVATIVES; ANIMAL; BRAIN TUMOR; CELL PROLIFERATION; DRUG RESISTANCE; NUDE MOUSE; PATHOLOGY; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC AGENTS, ALKYLATING; BRAIN NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; DACARBAZINE; DRUG RESISTANCE, NEOPLASM; GLIOMA; HUMANS; MICE, NUDE;

EID: 85029925185     PISSN: 15228517     EISSN: 15235866     Source Type: Journal    
DOI: 10.1093/neuonc/nox070     Document Type: Article

References (45)

1. Weller M, Wick W, Aldape K, et al. Glioma. Nat Rev Dis Primers. 2015; 1:15017.
2. Stupp R, Mason WP, van den Bent MJ, et al.; European Organisation for Research and Treatment of Cancer Brain Tumor and Radiotherapy Groups; National Cancer Institute of Canada Clinical Trials Group. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med. 2005;352(10):987-996.
3. Buckner JC, Shaw EG, Pugh SL, et al. Radiation plus procarbazine, CCNU, and vincristine in low-grade glioma. N Engl J Med. 2016;374(14):1344-1355.
4. van den Bent M, Erridge S, Vogelbaum M, et al. Results of the interim analysis of the EORTC randomized phase III CATNON trial on concurrent and adjuvant temozolomide in anaplastic glioma without 1p/19q codeletion: An Intergroup trial. Paper presented at: ASCO Annual Meeting 2016; Chicago.
5. Sahm F, Capper D, Jeibmann A, et al. Addressing diffuse glioma as a systemic brain disease with single-cell analysis. Arch Neurol. 2012;69(4):523-526.
6. Scherer H. The forms of growth in gliomas and their practical significance. Brain. 1940; 63(1):1-35.
7. Stummer W, Pichlmeier U, Meinel T, Wiestler OD, Zanella F, Reulen HJ; ALA-Glioma Study Group. Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: A randomised controlled multicentre phase III trial. Lancet Oncol. 2006;7(5):392-401.
8. Brown TJ, Brennan MC, Li M, et al. Association of the extent of resection with survival in glioblastoma: A systematic review and meta-analysis. JAMA Oncol. 2016;2(11):1460-1469.
9. Konishi Y, Muragaki Y, Iseki H, Mitsuhashi N, Okada Y. Patterns of intracranial glioblastoma recurrence after aggressive surgical resection and adjuvant management: Retrospective analysis of 43 cases. Neurol Med Chir (Tokyo). 2012;52(8):577-586.
10. Petrecca K, Guiot MC, Panet-Raymond V, Souhami L. Failure pattern following complete resection plus radiotherapy and temozolomide is at the resection margin in patients with glioblastoma. J Neurooncol. 2013;111(1):19-23.
11. Weller M, Cloughesy T, Perry JR, Wick W. Standards of care for treatment of recurrent glioblastoma-are we there yet? Neuro Oncol. 2013;15(1):4-27.
12. Lemeé JM, Clavreul A, Menei P. Intratumoral heterogeneity in glioblastoma: Don't forget the peritumoral brain zone. Neuro Oncol. 2015;17(10):1322-1332.
13. Chowdhary SA, Ryken T, Newton HB. Survival outcomes and safety of carmustine wafers in the treatment of high-grade gliomas: A meta-analysis. J Neurooncol. 2015;122(2):367-382.
14. Westphal M, Hilt DC, Bortey E, et al. A phase 3 trial of local chemotherapy with biodegradable carmustine (BCNU) wafers (Gliadel wafers) in patients with primary malignant glioma. Neuro Oncol. 2003;5(2):79-88.
15. Giordano FA, Brehmer S, Abo-Madyan Y, et al. INTRAGO: Intraoperative radiotherapy in glioblastoma multiforme-a phase I/II dose escalation study. BMC Cancer. 2014;14:992.
16. Johnson BE, Mazor T, Hong C, et al. Mutational analysis reveals the origin and therapy-driven evolution of recurrent glioma. Science. 2014;343(6167):189-193.
17. Wick W, Weller M, van den Bent M, et al. MGMT testing-the challenges for biomarker-based glioma treatment. Nat Rev Neurol. 2014;10(7):372-385.
18. Esteller M, Garcia-Foncillas J, Andion E, et al. Inactivation of the DNArepair gene MGMT and the clinical response of gliomas to alkylating agents. N Engl J Med. 2000;343(19):1350-1354.
19. Hegi ME, Diserens AC, Gorlia T, et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med. 2005;352(10):997-1003.
20. Leu S, von Felten S, Frank S, et al. IDH/MGMT-driven molecular classification of low-grade glioma is a strong predictor for long-term survival. Neuro Oncol. 2013;15(4):469-479.
21. Wick W, Hartmann C, Engel C, et al. NOA-04 randomized phase III trial of sequential radiochemotherapy of anaplastic glioma with procarbazine, lomustine, and vincristine or temozolomide. J Clin Oncol. 2009;27(35):5874-5880.
22. Wick W, Platten M, Meisner C, et al.; NOA-08 Study Group of Neuro-oncology Working Group (NOA) of German Cancer Society. Temozolomide chemotherapy alone versus radiotherapy alone for malignant astrocytoma in the elderly: The NOA-08 randomised, phase 3 trial. Lancet Oncol. 2012;13(7):707-715.
23. Osswald M, Jung E, Sahm F, et al. Brain tumour cells interconnect to a functional and resistant network. Nature. 2015;528(7580):93-98.
24. Goslin K, Schreyer DJ, Skene JH, Banker G. Development of neuronal polarity: GAP-43 distinguishes axonal from dendritic growth cones. Nature. 1988;336(6200):672-674.
25. Lemke D, Weiler M, Blaes J, et al. Primary glioblastoma cultures: Can profiling of stem cell markers predict radiotherapy sensitivity? J Neurochem. 2014;131(2):251-264.
26. Kienast Y, von Baumgarten L, Fuhrmann M, et al. Real-time imaging reveals the single steps of brain metastasis formation. Nat Med. 2010;16(1):116-122.
27. Winkler F, Kienast Y, Fuhrmann M, et al. Imaging glioma cell invasion in vivo reveals mechanisms of dissemination and peritumoral angiogenesis. Glia. 2009;57(12):1306-1315.
28. Winkler F, Kozin SV, Tong RT, et al. Kinetics of vascular normalization by VEGFR2 blockade governs brain tumor response to radiation: Role of oxygenation, angiopoietin-1, and matrix metalloproteinases. Cancer Cell. 2004;6(6):553-563.
29. Deutsch MB, Panageas KS, Lassman AB, Deangelis LM. Steroid management in newly diagnosed glioblastoma. J Neurooncol. 2013;113(1):111-116.
30. Hamard L, Ratel D, Selek L, Berger F, van der Sanden B, Wion D. The brain tissue response to surgical injury and its possible contribution to glioma recurrence. J Neurooncol. 2016;128(1):1-8.
31. Ratel D, van der Sanden B, Wion D. Glioma resection and tumor recurrence: Back to Semmelweis. Neuro Oncol. 2016;18(12):1688-1689.
32. Okolie O, Bago JR, Schmid RS, et al. Reactive astrocytes potentiate tumor aggressiveness in a murine glioma resection and recurrence model. Neuro Oncol. 2016;18(12):1622-1633.
33. Kolar K, Freitag-Andrade M, Bechberger J, et al. Podoplanin: A marker for reactive gliosis in gliomas and brain injury. J Neuropathol Exp Neurol. 2014; 74(1):64-74.
34. Ekblad L, Lindgren G, Persson E, Kjellén E, Wennerberg J. Cell-linespecific stimulation of tumor cell aggressiveness by wound healing factors-a central role for STAT3. BMC Cancer. 2013;13:33.
35. Mannino M, Yarnold J. Effect of breast-duct anatomy and wound-healing responses on local tumour recurrence after primary surgery for early breast cancer. Lancet Oncol. 2009;10(4):425-429.
36. Licitra L, Perrone F, Tamborini E, et al. Role of EGFR family receptors in proliferation of squamous carcinoma cells induced by wound healing fluids of head and neck cancer patients. Ann Oncol. 2011;22(8):1886-1893.
37. Murphy SF, Varghese RT, Lamouille S, et al. Connexin 43 inhibition sensitized chemoresistant glioblastoma cells to temozolomide. Cancer Res. 2016; 76(1):140-149.
38. Munoz JL, Rodriguez-Cruz V, Greco SJ, Ramkissoon SH, Ligon KL, Rameshwar P. Temozolomide resistance in glioblastoma cells occurs partly through epidermal growth factor receptor-mediated induction of connexin 43. Cell Death Dis. 2014;5:e1145.
39. Gielen PR, Aftab Q, Ma N, et al. Connexin43 confers temozolomide resistance in human glioma cells by modulating the mitochondrial apoptosis pathway. Neuropharmacology. 2013;75:539-548.
40. Hitomi M, Deleyrolle LP, Mulkearns-Hubert EE, et al. Differential connexin function enhances self-renewal in glioblastoma. Cell Rep. 2015;11(7):1031-1042.
41. Sin WC, Crespin S, Mesnil M. Opposing roles of connexin43 in glioma progression. Biochim Biophys Acta. 2012;1818(8):2058-2067.
42. Chen W, Wang D, Du X, et al. Glioma cells escaped from cytotoxicity of temozolomide and vincristine by communicating with human astrocytes. Med Oncol. 2015;32(3):43.
43. Chen Q, Boire A, Jin X, et al. Carcinoma-astrocyte gap junctions promote brain metastasis by cGAMP transfer. Nature. 2016;533(7604):493-498.
44. Sin WC, Aftab Q, Bechberger JF, Leung JH, Chen H, Naus CC. Astrocytes promote glioma invasion via the gap junction protein connexin43. Oncogene. 2016;35(12):1504-1516.
45. Lin Q, Liu Z, Ling F, Xu G. Astrocytes protect glioma cells from chemotherapy and upregulate survival genes via gap junctional communication. Mol Med Rep. 2016;13(2):1329-1335.