A malignant cellular network in gliomas: Potential clinical implications

Neuro-Oncology

Volumn 18, Issue 4, 2016, Pages 479-485

  Osswald, Matthias ^a,b   Solecki, Gergely ^a,b   Wick, Wolfgang ^a,b   Winkler, Frank ^a,b  

^a UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

1p 19q codeletion; astrocytoma; glioblastoma; oligodendroglioma; resistance; tumor microtubes

Indexed keywords

TUMOR MARKER;

ARTICLE; CELL MIGRATION; CHROMOSOME 19Q; CHROMOSOME 1P; CHROMOSOME DELETION; CLINICAL FEATURE; CYTOTOXICITY; GAP JUNCTION; GLIOMA; HUMAN; MOLECULARLY TARGETED THERAPY; NERVE CELL DIFFERENTIATION; NONHUMAN; ONCOLOGICAL PARAMETERS; PREDICTION; TUMOR MICROTUBE; BRAIN TUMOR; CELL FUNCTION; METABOLISM; NERVE TRACT; PATHOLOGY; SIGNAL TRANSDUCTION;

BRAIN NEOPLASMS; CELL PHYSIOLOGICAL PHENOMENA; GLIOMA; HUMANS; NEURAL PATHWAYS; SIGNAL TRANSDUCTION;

EID: 84966550419     PISSN: 15228517     EISSN: 15235866     Source Type: Journal    
DOI: 10.1093/neuonc/now014     Document Type: Article

References (50)

1. Zülch KJ. Brain Tumors: Their Biology and Pathology (English edition based on 2nd German edition; translated by A. B. Rothballer and Jerzy Olszewski). New York: Springer; 1957.
2. Osswald M, Jung E, Sahm F, et al. Brain tumour cells interconnect to a functional and resistant network. Nature. 2015;528(7580):93-98.
3. Sontheimer H. Brain cancer: tumour cells on neighbourhood watch. Nature. 2015;528(7580):49-50.
4. Sin WC, Crespin S, Mesnil M. Opposing roles of connexin43 in glioma progression. Biochim Biophys Acta. 2012;1818(8):2058-2067.
5. Egeblad M, Nakasone ES, Werb Z. Tumors as organs: complex tissues that interface with the entire organism. Dev Cell. 2010; 18(6):884-901.
6. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144(5):646-674.
7. Cuddapah VA, Robel S, Watkins S, et al. A neurocentric perspective on glioma invasion. Nat Rev Neurosci. 2014;15(7):455-465.
8. Goslin K, Schreyer DJ, Skene JH, et al. Development of neuronal polarity: GAP-43 distinguishes axonal from dendritic growth cones. Nature. 1988;336(6200):672-674.
9. Skene JH, Jacobson RD, Snipes GJ, et al. A protein induced during nerve growth (GAP-43) is a major component of growth-cone membranes. Science. 1986;233(4765):783-786.
10. Haag D, Zipper P, Westrich V, et al. Nos2 inactivation promotes the development of medulloblastoma in Ptch1(+/-) mice by deregulation of Gap43-dependent granule cell precursor migration. PLoS Genet. 2012;8(3):e1002572.
11. Aigner L, Arber S, Kapfhammer JP, et al. Overexpression of the neural growth-associated protein GAP-43 induces nerve sprouting in the adult nervous system of transgenic mice. Cell. 1995;83(2): 269-278.
12. Zuber MX, Goodman DW, Karns LR, et al. The neuronal growth-associated protein GAP-43 induces filopodia in non-neuronal cells. Science. 1989;244(4909):1193-1195.
13. Fulga TA, Rorth P. Invasive cell migration is initiated by guided growth of long cellular extensions. Nat Cell Biol. 2002;4(9):715-719.
14. Yee KT, Simon HH, Tessier-Lavigne M, et al. Extension of long leading processes and neuronal migration in the mammalian brain directed by the chemoattractant netrin-1. Neuron. 1999; 24(3):607-622.
15. Rorth P. Communication by touch: role of cellular extensions in complex animals. Cell. 2003;112(5):595-598.
16. Ramirez-Weber FA, Kornberg TB. Cytonemes: cellular processes that project to the principal signaling center in Drosophila imaginal discs. Cell. 1999;97(5):599-607.
17. Inaba M, Buszczak M, Yamashita YM. Nanotubes mediate niche-stem-cell signalling in the Drosophila testis. Nature. 2015; 523(7560):329-332.
18. Hsiung F, Ramirez-Weber FA, Iwaki DD, et al. Dependence of Drosophila wing imaginal disc cytonemes on decapentaplegic. Nature. 2005;437(7058):560-563.
19. Smith IF, Shuai J, Parker I. Active generation and propagation of Ca2+ signals within tunneling membrane nanotubes. Biophys J. 2011;100(8):L37-L39.
20. Wang X, Veruki ML, Bukoreshtliev NV, et al. Animal cells connected by nanotubes can be electrically coupled through interposed gap-junction channels. Proc Natl Acad Sci U S A. 2010;107(40): 17194-17199.
21. Lou E, Fujisawa S, Morozov A, et al. Tunneling nanotubes provide a unique conduit for intercellular transfer of cellular contents in human malignant pleural mesothelioma. PLoS One. 2012;7(3): e33093.
22. Sherer NM. Long-distance relationships: do membrane nanotubes regulate cell-cell communication and disease progression? Mol Biol Cell. 2013;24(8):1095-1098.
23. Wesseling P, van den Bent M, Perry A. Oligodendroglioma: pathology, molecular mechanisms and markers. Acta Neuropathol. 2015; 129(6):809-827.
24. Wiestler B, Capper D, Sill M, et al. Integrated DNA methylation and copy-number profiling identify three clinically and biologically relevant groups of anaplastic glioma. Acta Neuropathol. 2014; 128(4):561-571.
25. Brat DJ, Verhaak RG, Aldape KD, et al. Comprehensive, integrative genomic analysis of diffuse lower-grade gliomas. N Engl J Med. 2015;372(26):2481-2498.
26. Eckel-Passow JE, Lachance DH, Molinaro AM, et al. Glioma groups based on 1p/19q, IDH, and TERT promoter mutations in tumors. N Engl J Med. 2015;372(26):2499-2508.
27. van den Bent MJ, Brandes AA, Taphoorn MJ, et al. Adjuvant procarbazine, lomustine, and vincristine chemotherapy in newly diagnosed anaplastic oligodendroglioma: long-term follow-up of EORTC brain tumor group study 26951. J Clin Oncol. 2013;31(3): 344-350.
28. Cairncross G, Wang M, Shaw E, et al. Phase III trial of chemoradiotherapy for anaplastic oligodendroglioma: long-term results of RTOG 9402. J Clin Oncol. 2013;31(3):337-343.
29. Wharton SB, Maltby E, Jellinek DA, et al. Subtypes of oligodendroglioma defined by 1p,19q deletions, differ in the proportion of apoptotic cells but not in replication-licensed non-proliferating cells. Acta Neuropathol. 2007;113(2):119-127.
30. Cairncross JG, Wang M, Jenkins RB, et al. Benefit from procarbazine, lomustine, and vincristine in oligodendroglial tumors is associated with mutation of IDH. JClinOncol. 2014;32(8):783-790.
31. Tombal B, Denmeade SR, Gillis JM, et al. A supramicromolar elevation of intracellular free calcium ([Ca(2+)](i)) is consistently required to induce the execution phase of apoptosis. Cell Death Differ. 2002;9(5):561-573.
32. McFerrin MB, Turner KL, Cuddapah VA, et al. Differential role of IK and BK potassium channels as mediators of intrinsic and extrinsic apoptotic cell death. Am J Physiol Cell Physiol. 2012;303(10): C1070-C1078.
33. Le HT, Sin WC, Lozinsky S, et al. Gap junction intercellular communication mediated by connexin43 in astrocytes is essential for their resistance to oxidative stress. J Biol Chem. 2014;289(3):1345-1354.
34. Wang Y, Cui J, Sun X, et al. Tunneling-nanotube development in astrocytes depends on p53 activation. Cell Death Differ. 2011; 18(4):732-742.
35. Wick A, Wick W, Hirrlinger J, et al. Chemotherapy-induced cell death in primary cerebellar granule neurons but not in astrocytes: in vitro paradigm of differential neurotoxicity. J Neurochem. 2004;91(5):1067-1074.
36. Lin Q, Balasubramanian K, Fan D, et al. Reactive astrocytes protect melanoma cells from chemotherapy by sequestering intracellular calcium through gap junction communication channels. Neoplasia. 2010;12(9):748-754.
37. Zhang L, Zhang S, Yao J, et al. Microenvironment-induced PTEN loss by exosomal microRNA primes brain metastasis outgrowth. Nature. 2015;527(7576):100-104.
38. Knobbe CB, Merlo A, Reifenberger G. PTEN signaling in gliomas. Neuro Oncol. 2002;4(3):196-211.
39. Suzhi Z, Liang T, Yuexia P, et al. Gap junctions enhance the antiproliferative effect of microRNA-124-3p in glioblastoma cells. J Cell Physiol. 2015;230(10):2476-2488.
40. Leybaert L, Sanderson MJ. Intercellular Ca(2+) waves: mechanisms and function. Physiol Rev. 2012;92(3):1359-1392.
41. Kuchibhotla KV, Lattarulo CR, Hyman BT, et al. Synchronous hyperactivity and intercellular calcium waves in astrocytes in Alzheimer mice. Science. 2009;323(5918):1211-1215.
42. Cornell-Bell AH, Finkbeiner SM, Cooper MS, et al. Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling. Science. 1990;247(4941):470-473.
43. Weissman TA, Riquelme PA, Ivic L, et al. Calcium waves propagate through radial glial cells and modulate proliferation in the developing neocortex. Neuron. 2004;43(5):647-661.
44. Hitomi M, Deleyrolle LP, Mulkearns-Hubert EE, et al. Differential connexin function enhances self-renewal in glioblastoma. Cell Rep. 2015;11(7):1031-1042.
45. Murphy SF, Varghese RT, Lamouille S, et al. Connexin 43 inhibition sensitizes chemoresistant glioblastoma cells to temozolomide. Cancer Res. 2016;76(1):139-149.
46. Benowitz LI, Routtenberg A. GAP-43: an intrinsic determinant of neuronal development and plasticity. Trends Neurosci. 1997; 20(2):84-91.
47. 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.
48. Wick W, Platten M, Meisner C, et al. 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.
49. Capper D, Zentgraf H, Balss J, et al. Monoclonal antibody specific for IDH1 R132H mutation. Acta Neuropathol. 2009;118(5):599-601.
50. Weber PA, Chang HC, Spaeth KE, et al. The permeability of gap junction channels to probes of different size is dependent on connexin composition and permeant-pore affinities. Biophys J. 2004;87(2):958-973.