Pilocytic astrocytoma: pathology, molecular mechanisms and markers

Acta Neuropathologica

Volumn 129, Issue 6, 2015, Pages 775-788

  Collins, V Peter ^a   Jones, David T W ^b   Giannini, Caterina ^c  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c MAYO CLINIC   (United States)

Author keywords

Brain neoplasms; Histopathology; Immunocytochemistry; MAPK; Molecular pathology; Morphology; Oncogenes; Pilocytic astrocytoma

Indexed keywords

B RAF KINASE; FIBROBLAST GROWTH FACTOR RECEPTOR 1; HYBRID PROTEIN; K RAS PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; N [3 (5 CHLORO 1H PYRROLO[2,3 B]PYRIDINE 3 CARBONYL) 2,4 DIFLUOROPHENYL]PROPANESULFONAMIDE; NEUROFIBROMIN; SORAFENIB; VEMURAFENIB;

ANAPLASTIC CARCINOMA; ASTROCYTOMA; BRAIN BIOPSY; BRAIN CYST; CEREBELLUM TUMOR; CHEMOTHERAPY; COMPUTER ASSISTED TOMOGRAPHY; DIFFERENTIAL DIAGNOSIS; DISEASE ASSOCIATION; FAMILIAL CANCER; GENE DUPLICATION; GENE MUTATION; GLIOBLASTOMA; GLIOMA; GLIOSIS; IMMUNOCYTOCHEMISTRY; INTRACRANIAL HYPERTENSION; MALIGNANT TRANSFORMATION; MOLECULAR GENETICS; MOLECULAR PATHOLOGY; NEUROFIBROMATOSIS TYPE 1; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; PERSONALIZED MEDICINE; PILOCYTIC ASTROCYTOMA; PILOMYXOID ASTROCYTOMA; PLEOMORPHIC XANTHOASTROCYTOMA; PRIORITY JOURNAL; PROGNOSIS; REVIEW; CENTRAL NERVOUS SYSTEM TUMOR; GENETIC PREDISPOSITION; GENETICS; HUMAN; MOLECULAR BIOLOGY; MOLECULAR MODEL; PATHOLOGY; PATHOPHYSIOLOGY;

ASTROCYTOMA; CENTRAL NERVOUS SYSTEM NEOPLASMS; GENETIC PREDISPOSITION TO DISEASE; HUMANS; MODELS, MOLECULAR; MOLECULAR BIOLOGY; NEUROIMAGING;

EID: 84929703295     PISSN: 00016322     EISSN: 14320533     Source Type: Journal    
DOI: 10.1007/s00401-015-1410-7     Document Type: Review

References (67)

1. Alpers CE, Davis RL, Wilson CB (1982) Persistence and late malignant transformation of childhood cerebellar astrocytoma. Case report. J Neurosurg 57:548–551. doi:10.3171/jns.1982.57.4.0548
2. Antonelli M, Badiali M, Moi L, Buttarelli FR, Baldi C, Massimino M et al (2014) KIAA1549:BRAF fusion gene in pediatric brain tumors of various histogenesis. Pediatr Blood Cancer. doi:10.1002/pbc.25272
3. Aoki Y, Niihori T, Narumi Y, Kure S, Matsubara Y (2008) The RAS/MAPK syndromes: novel roles of the RAS pathway in human genetic disorders. Hum Mutat 29:992–1006. doi:10.1002/humu.20748
4. Badiali M, Gleize V, Paris S, Moi L, Elhouadani S, Arcella A et al (2012) KIAA1549-BRAF fusions and IDH mutations can coexist in diffuse gliomas of adults. Brain Pathol 22:841–847. doi:10.1111/j.1750-3639.2012.00603.x
5. Bar EE, Lin A, Tihan T, Burger PC, Eberhart CG (2008) Frequent gains at chromosome 7q34 involving BRAF in pilocytic astrocytoma. J Neuropathol Exp Neurol 67:878–887. doi:10.1097/NEN.0b013e3181845622
6. Bohner G, Masuhr F, Distl R, Katchanov J, Klingebiel R, Zschenderlein R et al (2005) Pilocytic astrocytoma presenting as primary diffuse leptomeningeal gliomatosis: report of a unique case and review of the literature. Acta Neuropathol 110:306–311. doi:10.1007/s00401-005-1051-3
7. Bolcekova A, Nemethova M, Zatkova A, Hlinkova K, Pozgayova S, Hlavata A et al (2013) Clustering of mutations in the 5′ tertile of the NF1 gene in Slovakia patients with optic pathway glioma. Neoplasma 60:655–665. doi:10.4149/neo_2013_084
8. Bucy PC, Gustafson WA (1939) Structure, nature and classification of cerebellar astrocytomas. Amer J Cancer 35:327
9. Burkhard C, Di Patre PL, Schuler D, Schuler G, Yasargil MG, Yonekawa Y et al (2003) A population-based study of the incidence and survival rates in patients with pilocytic astrocytoma. J Neurosurg 98:1170–1174. doi:10.3171/jns.2003.98.6.1170
10. Capper D, Preusser M, Habel A, Sahm F, Ackermann U, Schindler G et al (2011) Assessment of BRAF V600E mutation status by immunohistochemistry with a mutation-specific monoclonal antibody. Acta Neuropathol 122:11–19. doi:10.1007/s00401-011-0841-z
11. Ceppa EP, Bouffet E, Griebel R, Robinson C, Tihan T (2007) The pilomyxoid astrocytoma and its relationship to pilocytic astrocytoma: report of a case and a critical review of the entity. J Neurooncol 81:191–196. doi:10.1007/s11060-006-9216-z
12. Chappe C, Padovani L, Scavarda D, Forest F, Nanni-Metellus I, Loundou A et al (2013) Dysembryoplastic neuroepithelial tumors share with pleomorphic xanthoastrocytomas and gangliogliomas BRAF(V600E) mutation and expression. Brain Pathol 23:574–583. doi:10.1111/bpa.12048
13. Cin H, Meyer C, Herr R, Janzarik WG, Lambert S, Jones DT et al (2011) Oncogenic FAM131B-BRAF fusion resulting from 7q34 deletion comprises an alternative mechanism of MAPK pathway activation in pilocytic astrocytoma. Acta Neuropathol 121:763–774. doi:10.1007/s00401-011-0817-z
14. Colin C, Padovani L, Chappe C, Mercurio S, Scavarda D, Loundou A et al (2013) Outcome analysis of childhood pilocytic astrocytomas: a retrospective study of 148 cases at a single institution. Neuropathol Appl Neurobiol 39:693–705. doi:10.1111/nan.12013
15. Daumas-Duport C, Scheithauer B, O’Fallon J, Kelly P (1988) Grading of astrocytomas. A simple and reproducible method. Cancer 62:2152–2165
16. Deshmukh H, Yu J, Shaik J, MacDonald TJ, Perry A, Payton JE et al (2011) Identification of transcriptional regulatory networks specific to pilocytic astrocytoma. BMC Med Genomics 4:57. doi:10.1186/1755-8794-4-57
17. Duerr EM, Rollbrocker B, Hayashi Y, Peters N, Meyer-Puttlitz B, Louis DN et al (1998) PTEN mutations in gliomas and glioneuronal tumors. Oncogene 16:2259–2264. doi:10.1038/sj.onc.1201756
18. Elvidge AR, Penfield W, Cone W (1939) Gliomas of the Central Nervous System (a study of 210 verfified cases). Res Publ Ass Nerv Ment Dis 16:107
19. Ferner RE, Huson SM, Thomas N, Moss C, Willshaw H, Evans DG et al (2007) Guidelines for the diagnosis and management of individuals with neurofibromatosis 1. J Med Genet 44:81–88. doi:10.1136/jmg.2006.045906
20. Fisher PG, Breiter SN, Carson BS, Wharam MD, Williams JA, Weingart JD et al (2000) A clinicopathologic reappraisal of brain stem tumor classification. Identification of pilocystic astrocytoma and fibrillary astrocytoma as distinct entities. Cancer 89:1569–1576
21. Forshew T, Tatevossian RG, Lawson AR, Ma J, Neale G, Ogunkolade BW et al (2009) Activation of the ERK/MAPK pathway: a signature genetic defect in posterior fossa pilocytic astrocytomas. J Pathol 218:172–181. doi:10.1002/path.2558
22. Fryssira H, Leventopoulos G, Psoni S, Kitsiou-Tzeli S, Stavrianeas N, Kanavakis E (2008) Tumor development in three patients with Noonan syndrome. Eur J Pediatr 167:1025–1031. doi:10.1007/s00431-007-0636-3
23. Gessi M, Moneim YA, Hammes J, Goschzik T, Scholz M, Denkhaus D et al (2014) FGFR1 Mutations in Rosette-Forming Glioneuronal Tumors of the Fourth Ventricle. J Neuropathol Exp Neurol 73:580–584. doi:10.1097/NEN.0000000000000080
24. Giannini C, Scheithauer BW, Burger PC, Christensen MR, Wollan PC, Sebo TJ et al (1999) Cellular proliferation in pilocytic and diffuse astrocytomas. J Neuropathol Exp Neurol 58:46–53
25. Gutmann DH, McLellan MD, Hussain I, Wallis JW, Fulton LL, Fulton RS et al (2013) Somatic neurofibromatosis type 1 (NF1) inactivation characterizes NF1-associated pilocytic astrocytoma. Genome Res 23:431–439. doi:10.1101/gr.142604.112
26. Ida CM, Lambert SR, Rodriguez FJ, Voss JS, Mc Cann BE, Seys AR et al (2012) BRAF alterations are frequent in cerebellar low-grade astrocytomas with diffuse growth pattern. J Neuropathol Exp Neurol 71:631–639. doi:10.1097/NEN.0b013e31825c448a
27. Ida CM, Rodriguez FJ, Burger PC, Caron AA, Jenkins SM, Spears GM et al (2014) Pleomorphic Xanthoastrocytoma: natural History and Long-term Follow-up. Brain Pathol. doi:10.1111/bpa.12217
28. Ilgren EB, Stiller CA (1987) Cerebellar astrocytomas. Part II. Pathologic features indicative of malignancy. Clin Neuropathol 6:201–214
29. Jacob K, Albrecht S, Sollier C, Faury D, Sader E, Montpetit A et al (2009) Duplication of 7q34 is specific to juvenile pilocytic astrocytomas and a hallmark of cerebellar and optic pathway tumours. Br J Cancer 101:722–733. doi:10.1038/sj.bjc.6605179
30. Janzarik WG, Kratz CP, Loges NT, Olbrich H, Klein C, Schafer T et al (2007) Further evidence for a somatic KRAS mutation in a pilocytic astrocytoma. Neuropediatrics 38:61–63. doi:10.1055/s-2007-984451
31. Johnson MW, Eberhart CG, Perry A, Tihan T, Cohen KJ, Rosenblum MK et al (2010) Spectrum of pilomyxoid astrocytomas: intermediate pilomyxoid tumors. Am J Surg Pathol 34:1783–1791. doi:10.1097/PAS.0b013e3181fd66c3
32. Jones DT, Hutter B, Jager N, Korshunov A, Kool M, Warnatz HJ et al (2013) Recurrent somatic alterations of FGFR1 and NTRK2 in pilocytic astrocytoma. Nat Genet 45:927–932. doi:10.1038/ng.2682
33. Jones DT, Ichimura K, Liu L, Pearson DM, Plant K, Collins VP (2006) Genomic analysis of pilocytic astrocytomas at 0.97 Mb resolution shows an increasing tendency toward chromosomal copy number change with age. J Neuropathol Exp Neurol 65:1049–1058. doi:10.1097/01.jnen.0000240465.33628.87
34. Jones DT, Kocialkowski S, Liu L, Pearson DM, Backlund LM, Ichimura K et al (2008) Tandem duplication producing a novel oncogenic BRAF fusion gene defines the majority of pilocytic astrocytomas. Cancer Res 68:8673–8677. doi:10.1158/0008-5472.CAN-08-2097
35. Jones DT, Kocialkowski S, Liu L, Pearson DM, Ichimura K, Collins VP (2009) Oncogenic RAF1 rearrangement and a novel BRAF mutation as alternatives to KIAA1549:BRAF fusion in activating the MAPK pathway in pilocytic astrocytoma. Oncogene 28:2119–2123. doi:10.1038/onc.2009.73
36. Katsetos CD, Krishna L, Friedberg E, Reidy J, Karkavelas G, Savory J (1994) Lobar pilocytic astrocytomas of the cerebral hemispheres: II. Pathobiology–morphogenesis of the eosinophilic granular bodies. Clin Neuropathol 13:306–314
37. Kleinschmidt-DeMasters BK, Aisner DL, Birks DK, Foreman NK (2013) Epithelioid GBMs show a high percentage of BRAF V600E mutation. Am J Surg Pathol 37:685–698. doi:10.1097/PAS.0b013e31827f9c5e
38. Lambert SR, Witt H, Hovestadt V, Zucknick M, Kool M, Pearson DM et al (2013) Differential expression and methylation of brain developmental genes define location-specific subsets of pilocytic astrocytoma. Acta Neuropathol 126:291–301. doi:10.1007/s00401-013-1124-7
39. Lewis RA, Gerson LP, Axelson KA, Riccardi VM, Whitford RP (1984) von Recklinghausen neurofibromatosis. II. Incidence of optic gliomata. Ophthalmology 91:929–935
40. Listernick R, Charrow J, Gutmann DH (1999) Intracranial gliomas in neurofibromatosis type 1. Am J Med Genet 89:38–44
41. Lito P, Rosen N, Solit DB (2013) Tumor adaptation and resistance to RAF inhibitors. Nat Med 19:1401–1409. doi:10.1038/nm.3392
42. Louis DN, Ohgaki H, Wiestler OD, Cavenee WK (2007) Tumours of the central nervous system. IARC, Lyon
43. Louis DN, Perry A, Burger P, Ellison DW, Reifenberger G, von Deimling A et al (2014) International Society Of Neuropathology-Haarlem consensus guidelines for nervous system tumor classification and grading. Brain Pathol 24:429–435. doi:10.1111/bpa.12171
44. Minehan KJ, Brown PD, Scheithauer BW, Krauss WE, Wright MP (2009) Prognosis and treatment of spinal cord astrocytoma. Int J Radiat Oncol Biol Phys 73:727–733. doi:10.1016/j.ijrobp.2008.04.060
45. Minehan KJ, Shaw EG, Scheithauer BW, Davis DL, Onofrio BM (1995) Spinal cord astrocytoma: pathological and treatment considerations. J Neurosurg 83:590–595. doi:10.3171/jns.1995.83.4.0590
46. Nair S, Fort JA, Yachnis AT, Williams CA (2015) Optic nerve pilomyxoid astrocytoma in a patient with Noonan syndrome. Pediatr Blood Cancer. doi:10.1002/pbc.25382
47. Ohgaki H, Kleihues P (2005) Population-based studies on incidence, survival rates, and genetic alterations in astrocytic and oligodendroglial gliomas. J Neuropathol Exp Neurol 64:479–489
48. Ostrom QT, Gittleman H, Liao P, Rouse C, Chen Y, Dowling J et al (2014) CBTRUS statistical report: primary brain and central nervous system tumors diagnosed in the United States in 2007–2011. Neuro Oncol 16(Suppl 4):1–63. doi:10.1093/neuonc/nou223
49. Pfister S, Janzarik WG, Remke M, Ernst A, Werft W, Becker N et al (2008) BRAF gene duplication constitutes a mechanism of MAPK pathway activation in low-grade astrocytomas. J Clin Invest 118:1739–1749. doi:10.1172/JCI33656
50. Roberts AE, Allanson JE, Tartaglia M, Gelb BD (2013) Noonan syndrome. Lancet 381:333–342. doi:10.1016/S0140-6736(12)61023-X
51. Rodriguez FJ, Perry A, Gutmann DH, O’Neill BP, Leonard J, Bryant S et al (2008) Gliomas in neurofibromatosis type 1: a clinicopathologic study of 100 patients. J Neuropathol Exp Neurol 67:240–249. doi:10.1097/NEN.0b013e318165eb75
52. Rodriguez FJ, Scheithauer BW, Burger PC, Jenkins S, Giannini C (2010) Anaplasia in pilocytic astrocytoma predicts aggressive behavior. Am J Surg Pathol 34:147–160. doi:10.1097/PAS.0b013e3181c75238
53. Sanoudou D, Tingby O, Ferguson-Smith MA, Collins VP, Coleman N (2000) Analysis of pilocytic astrocytoma by comparative genomic hybridization. Br J Cancer 82:1218–1222. doi:10.1054/bjoc.1999.1066
54. Scheithauer BW, Hawkins C, Tihan T, VandenBerg SR, Burger PC (2007) Pilocytic Astrocytoma. In: Louis DN, Ohagaki H, Wiestler OD, Cavenee WK (eds) WHO Classification of tumours of the central nervous system. International Agency for Research on Cancer, Lyon, pp 14–21
55. Schiffman JD, Hodgson JG, VandenBerg SR, Flaherty P, Polley MY, Yu M et al (2010) Oncogenic BRAF mutation with CDKN2A inactivation is characteristic of a subset of pediatric malignant astrocytomas. Cancer Res 70:512–519. doi:10.1158/0008-5472.CAN-09-1851
56. Schindler G, Capper D, Meyer J, Janzarik W, Omran H, Herold-Mende C et al (2011) Analysis of BRAF V600E mutation in 1,320 nervous system tumors reveals high mutation frequencies in pleomorphic xanthoastrocytoma, ganglioglioma and extra-cerebellar pilocytic astrocytoma. Acta Neuropathol 121:397–405. doi:10.1007/s00401-011-0802-6
57. Sharif S, Upadhyaya M, Ferner R, Majounie E, Shenton A, Baser M et al (2011) A molecular analysis of individuals with neurofibromatosis type 1 (NF1) and optic pathway gliomas (OPGs), and an assessment of genotype-phenotype correlations. J Med Genet 48:256–260. doi:10.1136/jmg.2010.081760
58. Sharma MK, Mansur DB, Reifenberger G, Perry A, Leonard JR, Aldape KD et al (2007) Distinct genetic signatures among pilocytic astrocytomas relate to their brain region origin. Cancer Res 67:890–900. doi:10.1158/0008-5472.CAN-06-0973
59. Sievert AJ, Jackson EM, Gai X, Hakonarson H, Judkins AR, Resnick AC et al (2009) Duplication of 7q34 in pediatric low-grade astrocytomas detected by high-density single-nucleotide polymorphism-based genotype arrays results in a novel BRAF fusion gene. Brain Pathol 19:449–458. doi:10.1111/j.1750-3639.2008.00225.x
60. Sievert AJ, Lang SS, Boucher KL, Madsen PJ, Slaunwhite E, Choudhari N et al (2013) Paradoxical activation and RAF inhibitor resistance of BRAF protein kinase fusions characterizing pediatric astrocytomas. Proc Natl Acad Sci USA 110:5957–5962. doi:10.1073/pnas.1219232110
61. Singh D, Chan JM, Zoppoli P, Niola F, Sullivan R, Castano A et al (2012) Transforming fusions of FGFR and TACC genes in human glioblastoma. Science 337:1231–1235. doi:10.1126/science.1220834
62. Tchoghandjian A, Fernandez C, Colin C, El Ayachi I, Voutsinos-Porche B, Fina F et al (2009) Pilocytic astrocytoma of the optic pathway: a tumour deriving from radial glia cells with a specific gene signature. Brain 132:1523–1535. doi:10.1093/brain/awp048
63. Tihan T, Fisher PG, Kepner JL, Godfraind C, McComb RD, Goldthwaite PT et al (1999) Pediatric astrocytomas with monomorphous pilomyxoid features and a less favorable outcome. J Neuropathol Exp Neurol 58:1061–1068
64. White JB, Piepgras DG, Scheithauer BW, Parisi JE (2008) Rate of spontaneous hemorrhage in histologically proven cases of pilocytic astrocytoma. J Neurosurg 108:223–226. doi:10.3171/JNS/2008/108/2/0223
65. Wu G, Diaz AK, Paugh BS, Rankin SL, Ju B, Li Y et al (2014) The genomic landscape of diffuse intrinsic pontine glioma and pediatric non-brainstem high-grade glioma. Nat Genet 46:444–450. doi:10.1038/ng.2938
66. Wu J, Dombi E, Jousma E, Scott Dunn R, Lindquist D, Schnell BM et al (2012) Preclincial testing of sorafenib and RAD001 in the Nf(flox/flox);DhhCre mouse model of plexiform neurofibroma using magnetic resonance imaging. Pediatr Blood Cancer 58:173–180. doi:10.1002/pbc.23015
67. Zhang J, Wu G, Miller CP, Tatevossian RG, Dalton JD, Tang B et al (2013) Whole-genome sequencing identifies genetic alterations in pediatric low-grade gliomas. Nat Genet 45:602–612. doi:10.1038/ng.2611