Deficiency of very large G-protein-coupled receptor-1 is a risk factor of tumor-related epilepsy: a whole transcriptome sequencing analysis

Journal of Neuro-Oncology

Volumn 121, Issue 3, 2015, Pages 609-616

  Wang, Yinyan ^a,b   Fan, Xing ^b   Zhang, Wei ^b   Zhang, Chuanbao ^b   Wang, Jiangfei ^b   Jiang, Tao ^a,b,c   Wang, Lei ^b  

^a CAPITAL MEDICAL UNIVERSITY   (China)

^b CAPITAL MEDICAL UNIVERSITY   (China)

^c BEIJING INSTITUTE FOR BRAIN DISORDERS   (China)

Author keywords

Transcriptome; Tumor related epilepsy; VLGR1

Indexed keywords

G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 1; TRANSCRIPTOME; UNCLASSIFIED DRUG; GPR98 PROTEIN, HUMAN;

ADULT; ARTICLE; CANCER SURVIVAL; CONTROLLED STUDY; EPILEPSY; FEMALE; GENE EXPRESSION; GLIOMA; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; PROGNOSIS; PROGRESSION FREE SURVIVAL; RNA SEQUENCE; TRANSCRIPTOMICS; TUMOR RELATED EPILEPSY; VLGR1 GENE; BRAIN TUMOR; COMPLICATION; DEFICIENCY; DISEASE FREE SURVIVAL; GENE EXPRESSION PROFILING; KAPLAN MEIER METHOD; METABOLISM; MIDDLE AGED; MORTALITY; PROPORTIONAL HAZARDS MODEL; RISK FACTOR;

ADULT; BRAIN NEOPLASMS; DISEASE-FREE SURVIVAL; EPILEPSY; FEMALE; GENE EXPRESSION PROFILING; GLIOMA; HUMANS; KAPLAN-MEIER ESTIMATE; MALE; MIDDLE AGED; PROGNOSIS; PROPORTIONAL HAZARDS MODELS; RECEPTORS, G-PROTEIN-COUPLED; RISK FACTORS;

EID: 84925493826     PISSN: 0167594X     EISSN: 15737373     Source Type: Journal    
DOI: 10.1007/s11060-014-1674-0     Document Type: Article

References (57)

1. Japp A, Gielen GH, Becker AJ (2013) Recent aspects of classification and epidemiology of epilepsy-associated tumors. Epilepsia 54(Suppl 9):5–11. doi:10.1111/epi.12436
2. Lhatoo SD, Moghimi N, Schuele S (2013) Tumor-related epilepsy and epilepsy surgery. Epilepsia 54(Suppl 9):1–4. doi:10.1111/epi.12435
3. Lynam LM, Lyons MK, Drazkowski JF, Sirven JI, Noe KH, Zimmerman RS, Wilkens JA (2007) Frequency of seizures in patients with newly diagnosed brain tumors: a retrospective review. Clin Neurol Neurosurg 109(7):634–638. doi:10.1016/j.clineuro.2007.05.017
4. van Breemen MS, Wilms EB, Vecht CJ (2007) Epilepsy in patients with brain tumours: epidemiology, mechanisms, and management. Lancet Neurol 6(5):421–430. doi:10.1016/S1474-4422(07)70103-5
5. Danfors T, Ribom D, Berntsson SG, Smits A (2009) Epileptic seizures and survival in early disease of grade 2 gliomas. Eur J Neurol 16(7):823–831. doi:10.1111/j.1468-1331.2009.02599.x
6. Pallud J, Audureau E, Blonski M, Sanai N, Bauchet L, Fontaine D, Mandonnet E, Dezamis E, Psimaras D, Guyotat J, Peruzzi P, Page P, Gal B, Parraga E, Baron MH, Vlaicu M, Guillevin R, Devaux B, Duffau H, Taillandier L, Capelle L, Huberfeld G (2014) Epileptic seizures in diffuse low-grade gliomas in adults. Brain 137(Pt 2):449–462. doi:10.1093/brain/awt345
7. Prakash O, Lukiw WJ, Peruzzi F, Reiss K, Musto AE (2012) Gliomas and seizures. Med Hypotheses 79(5):622–626. doi:10.1016/j.mehy.2012.07.037
8. Ruda R, Bello L, Duffau H, Soffietti R (2012) Seizures in low-grade gliomas: natural history, pathogenesis, and outcome after treatments. Neuro-oncology 14(Suppl 4):iv55–64. doi:10.1093/neuonc/nos199
9. Smits A, Duffau H (2011) Seizures and the natural history of World Health Organization grade II gliomas: a review. Neurosurgery 68(5):1326–1333. doi:10.1227/NEU.0b013e31820c3419
10. Englot DJ, Berger MS, Chang EF, Garcia PA (2012) Characteristics and treatment of seizures in patients with high-grade glioma: a review. Neurosurg Clin N Am 23 (2): 227–235, vii–viii. doi: 10.1016/j.nec.2012.01.009
11. Kim YH, Park CK, Kim TM, Choi SH, Kim YJ, Choi BS, Han JH, Lee SH, Kim CY, Kim IA, Heo DS, Kim IH, Kim DG, Jung HW (2013) Seizures during the management of high-grade gliomas: clinical relevance to disease progression. J Neurooncol 113(1):101–109. doi:10.1007/s11060-013-1094-6
12. Kerkhof M, Vecht CJ (2013) Seizure characteristics and prognostic factors of gliomas. Epilepsia 54(Suppl 9):12–17. doi:10.1111/epi.12437
13. van Dellen E, Douw L, Hillebrand A, Ris-Hilgersom IH, Schoonheim MM, Baayen JC, De Witt Hamer PC, Velis DN, Klein M, Heimans JJ, Stam CJ, Reijneveld JC (2012) MEG network differences between low- and high-grade glioma related to epilepsy and cognition. PLoS One 7(11):e50122. doi:10.1371/journal.pone.0050122
14. Berntsson SG, Malmer B, Bondy ML, Qu M, Smits A (2009) Tumor-associated epilepsy and glioma: are there common genetic pathways? Acta Oncol 48(7):955–963. doi:10.1080/02841860903104145
15. Huang L, You G, Jiang T, Li G, Li S, Wang Z (2011) Correlation between tumor-related seizures and molecular genetic profile in 103 Chinese patients with low-grade gliomas: a preliminary study. J Neurol Sci 302(1–2):63–67. doi:10.1016/j.jns.2010.11.024
16. Ostrom Q, Cohen ML, Ondracek A, Sloan A, Barnholtz-Sloan J (2013) Gene markers in brain tumors: what the epileptologist should know. Epilepsia 54(Suppl 9):25–29. doi:10.1111/epi.12439
17. Aronica E, Boer K, Becker A, Redeker S, Spliet WG, van Rijen PC, Wittink F, Breit T, Wadman WJ, Lopes da Silva FH, Troost D, Gorter JA (2008) Gene expression profile analysis of epilepsy-associated gangliogliomas. Neuroscience 151(1):272–292. doi:10.1016/j.neuroscience.2007.10.036
18. Gu W, Brodtkorb E, Piepoli T, Finocchiaro G, Steinlein OK (2005) LGI1: a gene involved in epileptogenesis and glioma progression? Neurogenetics 6(2):59–66. doi:10.1007/s10048-005-0216-5
19. Kunapuli P, Kasyapa CS, Hawthorn L, Cowell JK (2004) LGI1, a putative tumor metastasis suppressor gene, controls in vitro invasiveness and expression of matrix metalloproteinases in glioma cells through the ERK1/2 pathway. J Biol Chem 279(22):23151–23157. doi:10.1074/jbc.M314192200
20. Leu S, von Felten S, Frank S, Vassella E, Vajtai I, Taylor E, Schulz M, Hutter G, Hench J, Schucht P, Boulay JL, Mariani L (2013) IDH/MGMT-driven molecular classification of low-grade glioma is a strong predictor for long-term survival. Neuro-oncology 15(4):469–479. doi:10.1093/neuonc/nos317
21. Okita Y, Narita Y, Miyakita Y, Ohno M, Matsushita Y, Fukushima S, Sumi M, Ichimura K, Kayama T, Shibui S (2012) IDH1/2 mutation is a prognostic marker for survival and predicts response to chemotherapy for grade II gliomas concomitantly treated with radiation therapy. Int J Oncol 41(4):1325–1336. doi:10.3892/ijo.2012.1564
22. Stockhammer F, Misch M, Helms HJ, Lengler U, Prall F, von Deimling A, Hartmann C (2012) IDH1/2 mutations in WHO grade II astrocytomas associated with localization and seizure as the initial symptom. Seizure 21(3):194–197. doi:10.1016/j.seizure.2011.12.007
23. Liang R, Fan Y, Wang X, Mao Q, Liu Y (2013) The significance of IDH1 mutations in tumor-associated seizure in 60 Chinese patients with low-grade gliomas. ScientificWorldJournal 2013:403942. doi:10.1155/2013/403942
24. Reimers MS, Bastiaannet E, Langley RE, van Eijk R, van Vlierberghe RL, Lemmens VE, van Herk-Sukel MP, van Wezel T, Fodde R, Kuppen PJ, Morreau H, van de Velde CJ, Liefers GJ (2014) Expression of HLA class I antigen, aspirin use, and survival after a diagnosis of colon cancer. JAMA Intern Med 174(5):732–739. doi:10.1001/jamainternmed.2014.511
25. You G, Feng L, Yan W, Zhang W, Wang YZ, Li SW, Li SW, Li GL, Song YJ, Kang CS, You YP, Jiang T (2013) BCL2A1 is a potential biomarker for postoperative seizure control in patients with low-grade gliomas. CNS Neurosci Ther 19(11):882–888. doi:10.1111/cns.12148
26. Soffietti R, Baumert BG, Bello L, von Deimling A, Duffau H, Frenay M, Grisold W, Grant R, Graus F, Hoang-Xuan K, Klein M, Melin B, Rees J, Siegal T, Smits A, Stupp R, Wick W, European Federation of Neurological Societies (2010) Guidelines on management of low-grade gliomas: report of an EFNS–EANO task force. Eur J Neurol 17(9):1124–1133. doi:10.1111/j.1468-1331.2010.03151.x
27. de Groot M, Reijneveld JC, Aronica E, Heimans JJ (2012) Epilepsy in patients with a brain tumour: focal epilepsy requires focused treatment. Brain 135(Pt 4):1002–1016. doi:10.1093/brain/awr310
28. Heuser K, Szokol K, Tauboll E (2014) The role of glial cells in epilepsy. Tidsskr Nor Laegeforen 134(1):37–41. doi:10.4045/tidsskr.12.1344
29. Skradski SL, White HS, Ptacek LJ (1998) Genetic mapping of a locus (mass1) causing audiogenic seizures in mice. Genomics 49(2):188–192. doi:10.1006/geno.1998.5229
30. Skradski SL, Clark AM, Jiang H, White HS, Fu YH, Ptacek LJ (2001) A novel gene causing a mendelian audiogenic mouse epilepsy. Neuron 31(4):537–544
31. Scheel H, Tomiuk S, Hofmann K (2002) A common protein interaction domain links two recently identified epilepsy genes. Hum Mol Genet 11(15):1757–1762
32. Proposal for revised clinical and electroencephalographic classification of epileptic seizures. From the Commission on Classification and Terminology of the International League Against Epilepsy (1981). Epilepsia 22(4):489–501
33. Yan L, Yang M, Guo H, Yang L, Wu J, Li R, Liu P, Lian Y, Zheng X, Yan J, Huang J, Li M, Wu X, Wen L, Lao K, Li R, Qiao J, Tang F (2013) Single-cell RNA-seq profiling of human preimplantation embryos and embryonic stem cells. Nat Struct Mol Biol 20(9):1131–1139. doi:10.1038/nsmb.2660
34. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5(7):621–628. doi:10.1038/nmeth.1226
35. Yagi H, Noguchi Y, Kitamura K, Sato M (2009) Deficiency of Vlgr1 resulted in deafness and susceptibility to audiogenic seizures while the degree of hearing impairment was not correlated with seizure severity in C57BL/6- and 129-backcrossed lines of Vlgr1 knockout mice. Neurosci Lett 461(2):190–195. doi:10.1016/j.neulet.2009.06.012
36. van Wijk E, van der Zwaag B, Peters T, Zimmermann U, Te Brinke H, Kersten FF, Marker T, Aller E, Hoefsloot LH, Cremers CW, Cremers FP, Wolfrum U, Knipper M, Roepman R, Kremer H (2006) The DFNB31 gene product whirlin connects to the Usher protein network in the cochlea and retina by direct association with USH2A and VLGR1. Hum Mol Genet 15(5):751–765. doi:10.1093/hmg/ddi490
37. Nakayama J, Arinami T (2006) Molecular genetics of febrile seizures. Epilepsy Res 70(Suppl 1):S190–S198. doi:10.1016/j.eplepsyres.2005.11.023
38. 2+ exchangers define a cation binding domain. Mol Endocrinol 14(9):1351–1364. doi:10.1210/mend.14.9.0511
39. McMillan DR, Kayes-Wandover KM, Richardson JA, White PC (2002) Very large G protein-coupled receptor-1, the largest known cell surface protein, is highly expressed in the developing central nervous system. J Biol Chem 277(1):785–792. doi:10.1074/jbc.M108929200
40. Lerche H, Weber YG, Jurkat-Rott K, Lehmann-Horn F (2005) Ion channel defects in idiopathic epilepsies. Curr Pharm Des 11(21):2737–2752
41. Lerche H, Jurkat-Rott K, Lehmann-Horn F (2001) Ion channels and epilepsy. Am J Med Genet 106(2):146–159. doi:10.1002/ajmg.1582
42. Olsen ML, Sontheimer H (2008) Functional implications for Kir4.1 channels in glial biology: from K+ buffering to cell differentiation. J Neurochem 107(3):589–601. doi:10.1111/j.1471-4159.2008.05615.x
43. Pallud J, Capelle L, Huberfeld G (2013) Tumoral epileptogenicity: how does it happen? Epilepsia 54(Suppl 9):30–34. doi:10.1111/epi.12440
44. Campbell SL, Buckingham SC, Sontheimer H (2012) Human glioma cells induce hyperexcitability in cortical networks. Epilepsia 53(8):1360–1370. doi:10.1111/j.1528-1167.2012.03557.x
45. Wen PY, Kesari S (2008) Malignant gliomas in adults. N Engl J Med 359(5):492–507. doi:10.1056/NEJMra0708126
46. Melom JE, Littleton JT (2013) Mutation of a NCKX eliminates glial microdomain calcium oscillations and enhances seizure susceptibility. J Neurosci 33(3):1169–1178. doi:10.1523/JNEUROSCI.3920-12.2013
47. Omuro A, DeAngelis LM (2013) Glioblastoma and other malignant gliomas: a clinical review. JAMA 310(17):1842–1850. doi:10.1001/jama.2013.280319
48. Carico C, Nuno M, Mukherjee D, Elramsisy A, Dantis J, Hu J, Rudnick J, Yu JS, Black KL, Bannykh SI, Patil CG (2012) Loss of PTEN is not associated with poor survival in newly diagnosed glioblastoma patients of the temozolomide era. PLoS One 7(3):e33684. doi:10.1371/journal.pone.0033684
49. Bate L, Gardiner M (1999) Molecular genetics of human epilepsies. Expert Rev Mol Med 1999:1–22. doi:10.1017/S1462399499001349
50. Youland RS, Schomas DA, Brown PD, Nwachukwu C, Buckner JC, Giannini C, Parney IF, Laack NN (2013) Changes in presentation, treatment, and outcomes of adult low-grade gliomas over the past fifty years. Neuro-oncology 15(8):1102–1110. doi:10.1093/neuonc/not080
51. You G, Sha ZY, Yan W, Zhang W, Wang YZ, Li SW, Sang L, Wang Z, Li GL, Li SW, Song YJ, Kang CS, Jiang T (2012) Seizure characteristics and outcomes in 508 Chinese adult patients undergoing primary resection of low-grade gliomas: a clinicopathological study. Neuro-oncology 14(2):230–241. doi:10.1093/neuonc/nor205
52. Chang EF, Potts MB, Keles GE, Lamborn KR, Chang SM, Barbaro NM, Berger MS (2008) Seizure characteristics and control following resection in 332 patients with low-grade gliomas. J Neurosurg 108(2):227–235. doi:10.3171/JNS/2008/108/2/0227
53. Wang Y, Qian T, You G, Peng X, Chen C, You Y, Yao K, Wu C, Ma J, Sha Z, Wang S, Jiang T (2014) Localizing seizure-susceptible brain regions associated with low-grade gliomas using voxel-based lesion-symptom mapping. Neuro Oncol. doi:10.1093/neuonc/nou130
54. Lee JW, Wen PY, Hurwitz S, Black P, Kesari S, Drappatz J, Golby AJ, Wells WM 3rd, Warfield SK, Kikinis R, Bromfield EB (2010) Morphological characteristics of brain tumors causing seizures. Arch Neurol 67(3):336–342. doi:10.1001/archneurol.2010.2
55. Yang P, Wang Y, Peng X, You G, Zhang W, Yan W, Bao Z, Wang Y, Qiu X, Jiang T (2013) Management and survival rates in patients with glioma in China (2004–2010): a retrospective study from a single-institution. J Neurooncol 113(2):259–266. doi:10.1007/s11060-013-1103-9
56. Pallud J, Capelle L, Taillandier L, Fontaine D, Mandonnet E, Guillevin R, Bauchet L, Peruzzi P, Laigle-Donadey F, Kujas M, Guyotat J, Baron MH, Mokhtari K, Duffau H (2009) Prognostic significance of imaging contrast enhancement for WHO grade II gliomas. Neuro-oncology 11(2):176–182. doi:10.1215/15228517-2008-066
57. Chaichana KL, McGirt MJ, Niranjan A, Olivi A, Burger PC, Quinones-Hinojosa A (2009) Prognostic significance of contrast-enhancing low-grade gliomas in adults and a review of the literature. Neurol Res 31(9):931–939. doi:10.1179/174313209X395454