Intrinsic Astrocyte Heterogeneity Influences Tumor Growth in Glioma Mouse Models

Brain Pathology

Volumn 27, Issue 1, 2017, Pages 36-50

  Irvin, David M ^a   McNeill, Robert S ^a   Bash, Ryan E ^a   Miller, C Ryan ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

astrocytes; genetically engineered mice; glioma; heterogeneity; microenvironment

Indexed keywords

EXCITATORY AMINO ACID TRANSPORTER; GLIAL FIBRILLARY ACIDIC PROTEIN; NESTIN; EXCITATORY AMINO ACID TRANSPORTER 1; GLIAL FIBRILLARY ASTROCYTIC PROTEIN, MOUSE; NERVE PROTEIN; SLC1A3 PROTEIN, MOUSE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN REGION; CANCER MODEL; CARCINOGENESIS; CELL HETEROGENEITY; CELL LINEAGE; CELL PROLIFERATION; CELL SUBPOPULATION; CONTROLLED STUDY; GENE EXPRESSION; GENE MAPPING; GLIOMA; HUMAN; IMMUNOFLUORESCENCE; MICROGLIA; MOLECULAR PATHOLOGY; MOUSE; MOUSE MODEL; NONHUMAN; TUMOR GROWTH; TUMOR MICROENVIRONMENT; ANIMAL; BIOLOGICAL MODEL; BRAIN TUMOR; C57BL MOUSE; CELL CULTURE; CELL TRANSFORMATION; CHEMISTRY; CLASSIFICATION; DISEASE EXACERBATION; GENE KNOCK-IN; GENETICS; GLIOBLASTOMA; IMAGE PROCESSING; KNOCKOUT MOUSE; MUTATION; PATHOLOGY; TRANSGENIC MOUSE; TUMOR SUPPRESSOR GENE;

ANIMALS; ASTROCYTES; BRAIN NEOPLASMS; CELL LINEAGE; CELL TRANSFORMATION, NEOPLASTIC; CELLS, CULTURED; DISEASE PROGRESSION; EXCITATORY AMINO ACID TRANSPORTER 1; GENE KNOCK-IN TECHNIQUES; GENES, P53; GLIAL FIBRILLARY ACIDIC PROTEIN; GLIOBLASTOMA; IMAGE PROCESSING, COMPUTER-ASSISTED; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MODELS, BIOLOGICAL; MUTATION; NERVE TISSUE PROTEINS; TUMOR MICROENVIRONMENT;

EID: 84963894262     PISSN: 10156305     EISSN: 17503639     Source Type: Journal    
DOI: 10.1111/bpa.12348     Document Type: Article

References (71)

1. Abel TW, Clark C, Bierie B, Chytil A, Aakre M, Gorska A, Moses HL (2009) GFAP-Cre-mediated activation of oncogenic K-ras results in expansion of the subventricular zone and infiltrating glioma. Mol Cancer Res 7:645–653.
2. Alcantara Llaguno S, Chen J, Kwon CH, Jackson EL, Li Y, Burns DK et al (2009) Malignant astrocytomas originate from neural stem/progenitor cells in a somatic tumor suppressor mouse model. Cancer Cell 15:45–56.
3. Bachoo RM, Kim RS, Ligon KL, Maher EA, Brennan C, Billings N et al (2004) Molecular diversity of astrocytes with implications for neurological disorders. Proc Natl Acad Sci U S A 101:8384–8389.
4. Bachoo RM, Maher EA, Ligon KL, Sharpless NE, Chan SS, You MJ et al (2002) Epidermal growth factor receptor and Ink4a/Arf: convergent mechanisms governing terminal differentiation and transformation along the neural stem cell to astrocyte axis. Cancer Cell 1:269–277.
5. Bandeira F, Lent R, Herculano-Houzel S (2009) Changing numbers of neuronal and non-neuronal cells underlie postnatal brain growth in the rat. Proc Natl Acad Sci U S A 106:14108–14113.
6. Brennan CW, Verhaak RG, McKenna A, Campos B, Noushmehr H, Salama SR et al (2013) The somatic genomic landscape of glioblastoma. Cell 155:462–477.
7. Cahoy JD, Emery B, Kaushal A, Foo LC, Zamanian JL, Christopherson KS et al (2008) A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J Neurosci 28:264–278.
8. Cancer Genome Atlas Research Network (2008) Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 455:1061–1068.
9. Cancer Genome Atlas Research Network (2015) Comprehensive, integrative genomic analysis of diffuse lower-grade gliomas. N Engl J Med 372:2481–2498.
10. Casper KB, Jones K, McCarthy KD (2007) Characterization of astrocyte-specific conditional knockouts. Genesis 45:292–299.
11. Chaboub LS, Deneen B (2012) Developmental origins of astrocyte heterogeneity: the final frontier of CNS development. Dev Neurosci 34:379–388.
12. Chow LM, Endersby R, Zhu X, Rankin S, Qu C, Zhang J et al (2011) Cooperativity within and among Pten, p53, and Rb pathways induces high-grade astrocytoma in adult brain. Cancer Cell 19:305–316.
13. Ding H, Roncari L, Shannon P, Wu X, Lau N, Karaskova J et al (2001) Astrocyte-specific expression of activated p21-ras results in malignant astrocytoma formation in a transgenic mouse model of human gliomas. Cancer Res 61:3826–3836.
14. Doyle JP, Dougherty JD, Heiman M, Schmidt EF, Stevens TR, Ma G et al (2008) Application of a translational profiling approach for the comparative analysis of CNS cell types. Cell 135:749–762.
15. Fomchenko EI, Dougherty JD, Helmy KY, Katz AM, Pietras A, Brennan C et al (2011) Recruited cells can become transformed and overtake PDGF-induced murine gliomas in vivo during tumor progression. PLoS One 6:e20605.
16. Friedmann-Morvinski D, Bushong EA, Ke E, Soda Y, Marumoto T, Singer O et al (2012) Dedifferentiation of neurons and astrocytes by oncogenes can induce gliomas in mice. Science 338:1080–1084.
17. Galvao RP, Kasina A, McNeill RS, Harbin JE, Foreman O, Verhaak RG et al (2014) Transformation of quiescent adult oligodendrocyte precursor cells into malignant glioma through a multistep reactivation process. Proc Natl Acad Sci U S A 111:E4214–4223.
18. Ge WP, Miyawaki A, Gage FH, Jan YN, Jan LY (2012) Local generation of glia is a major astrocyte source in postnatal cortex. Nature 484:376–380.
19. Hambardzumyan D, Amankulor NM, Helmy KY, Becher OJ, Holland EC (2009) Modeling adult gliomas using RCAS/t-va technology. Transl Oncol 2:89–95.
20. Hertz L, Rodrigues TB (2014) Astrocytic-neuronal-astrocytic pathway selection for formation and degradation of glutamate/GABA. Front Endocrinol 5:42.
21. Higashi K, Fujita A, Inanobe A, Tanemoto M, Doi K, Kubo T, Kurachi Y (2001) An inwardly rectifying K(+) channel, Kir4.1, expressed in astrocytes surrounds synapses and blood vessels in brain. Am J Physiol Cell Physiol 281:C922–931.
22. Holland EC, Celestino J, Dai C, Schaefer L, Sawaya RE, Fuller GN (2000) Combined activation of Ras and Akt in neural progenitors induces glioblastoma formation in mice. Nat Genet 25:55–57.
23. Holland EC, Hively WP, DePinho RA, Varmus HE (1998) A constitutively active epidermal growth factor receptor cooperates with disruption of G1 cell-cycle arrest pathways to induce glioma-like lesions in mice. Genes Dev 12:3675–3685.
24. Huang Y, Hoffman C, Rajappa P, Kim JH, Hu W, Huse J et al (2014) Oligodendrocyte progenitor cells promote neovascularization in glioma by disrupting the blood-brain barrier. Cancer Res 74:1011–1021.
25. Jackson EL, Willis N, Mercer K, Bronson RT, Crowley D, Montoya R et al (2001) Analysis of lung tumor initiation and progression using conditional expression of oncogenic K-ras. Genes Dev 15:3243–3248.
26. Kang SH, Fukaya M, Yang JK, Rothstein JD, Bergles DE (2010) NG2+ CNS glial progenitors remain committed to the oligodendrocyte lineage in postnatal life and following neurodegeneration. Neuron 68:668–681.
27. Ko Y, Ament SA, Eddy JA, Caballero J, Earls JC, Hood L, Price ND (2013) Cell type-specific genes show striking and distinct patterns of spatial expression in the mouse brain. Proc Natl Acad Sci U S A 110:3095–3100.
28. Koren S, Reavie L, Couto JP, De Silva D, Stadler MB, Roloff T et al (2015) PIK3CA(H1047R) induces multipotency and multi-lineage mammary tumours. Nature 525:114–118.
29. Kwon CH, Zhao D, Chen J, Alcantara S, Li Y, Burns DK et al (2008) Pten haploinsufficiency accelerates formation of high-grade astrocytomas. Cancer Res 68:3286–3294.
30. Le DM, Besson A, Fogg DK, Choi KS, Waisman DM, Goodyer CG et al (2003) Exploitation of astrocytes by glioma cells to facilitate invasiveness: a mechanism involving matrix metalloproteinase-2 and the urokinase-type plasminogen activator-plasmin cascade. J Neurosci 23:4034–4043.
31. Lei L, Sonabend AM, Guarnieri P, Soderquist C, Ludwig T, Rosenfeld S et al (2011) Glioblastoma models reveal the connection between adult glial progenitors and the proneural phenotype. PLoS One 6:e20041.
32. Lindberg N, Jiang Y, Xie Y, Bolouri H, Kastemar M, Olofsson T et al (2014) Oncogenic signaling is dominant to cell of origin and dictates astrocytic or oligodendroglial tumor development from oligodendrocyte precursor cells. J Neurosci 34:14644–14651.
33. Lindberg N, Kastemar M, Olofsson T, Smits A, Uhrbom L (2009) Oligodendrocyte progenitor cells can act as cell of origin for experimental glioma. Oncogene 28:2266–2275.
34. Liu C, Sage JC, Miller MR, Verhaak RG, Hippenmeyer S, Vogel H et al (2011) Mosaic analysis with double markers reveals tumor cell of origin in glioma. Cell 146:209–221.
35. Louis DN, Ohgaki H, Wiestler OD, Cavenee WK (2007) WHO classification of tumours of the central nervous system. In: WHO Classification of Tumours, p. 312. IARC: Lyon.
36. Madisen L, Zwingman TA, Sunkin SM, Oh SW, Zariwala HA, Gu H et al (2010) A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat Neurosci 13:133–140.
37. Markovic DS, Glass R, Synowitz M, Rooijen N, Kettenmann H (2005) Microglia stimulate the invasiveness of glioma cells by increasing the activity of metalloprotease-2. J Neuropathol Exp Neurol 64:754–762.
38. Marshall CA, Suzuki SO, Goldman JE (2003) Gliogenic and neurogenic progenitors of the subventricular zone: who are they, where did they come from, and where are they going? Glia 43:52–61.
39. McNeill RS, Schmid RS, Bash RE et al (2014) Modeling astrocytoma pathogenesis in vitro and in vivo using cortical astrocytes or neural stem cells from conditional, genetically engineered mice. J Vis Exp e51763.
40. Miller CR, Perry A (2007) Glioblastoma. Arch Pathol Lab Med 131:397–406.
41. Molofsky AV, Krencik R, Ullian EM, Tsai HH, Deneen B, Richardson WD et al (2012) Astrocytes and disease: a neurodevelopmental perspective. Genes Dev 26:891–907.
42. Nikolaishvilli-Feinberg N, Cohen SM, Midkiff B, Zhou Y, Olorvida M, Ibrahim JG et al (2014) Development of DNA damage response signaling biomarkers using automated, quantitative image analysis. J Histochem Cytochem 62:185–196.
43. Noushmehr H, Weisenberger DJ, Diefes K, Phillips HS, Pujara K, Berman BP et al (2010) Identification of a CpG island methylator phenotype that defines a distinct subgroup of glioma. Cancer Cell 17:510–522.
44. Ohgaki H, Kleihues P (2013) The definition of primary and secondary glioblastoma. Clin Cancer Res 19:764–772.
45. Perego C, Vanoni C, Bossi M, Massari S, Basudev H, Longhi R, Pietrini G (2000) The GLT-1 and GLAST glutamate transporters are expressed on morphologically distinct astrocytes and regulated by neuronal activity in primary hippocampal cocultures. J Neurochem 75:1076–1084.
46. Phillips HS, Kharbanda S, Chen R, Forrest WF, Soriano RH, Wu TD et al (2006) Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis. Cancer Cell 9:157–173.
47. Rakic P (2003) Elusive radial glial cells: historical and evolutionary perspective. Glia 43:19–32.
48. Regan MR, Huang YH, Kim YS, Dykes-Hoberg MI, Jin L, Watkins AM et al (2007) Variations in promoter activity reveal a differential expression and physiology of glutamate transporters by glia in the developing and mature CNS. J Neurosci 27:6607–6619.
49. Rothstein JD, Martin L, Levey AI, Dykes-Hoberg M, Jin L, Wu D et al (1994) Localization of neuronal and glial glutamate transporters. Neuron 13:713–725.
50. Rutledge WC, Kong J, Gao J, Gutman DA, Cooper LA, Appin C et al (2013) Tumor-infiltrating lymphocytes in glioblastoma are associated with specific genomic alterations and related to transcriptional class. Clin Cancer Res 19:4951–4960.
51. Schmid RS, Simon JM, Vitucci M, McNeill RS, Bash RE, Werneke AM, Huey L, White KK, Ewend MG, Wu J, Miller CR (2016) Core pathway mutations induce de-differentiation of murine astrocytes into glioblastoma stem cells that are sensitive to radiation but resistant to temozolomide. Neuro Oncol DOI:10.1093/neuonc/nov321.
52. Schmid RS, Vitucci M, Miller CR (2012) Genetically engineered mouse models of diffuse gliomas. Brain Res Bull 88:72–79.
53. Schmitt A, Asan E, Puschel B, Kugler P (1997) Cellular and regional distribution of the glutamate transporter GLAST in the CNS of rats: nonradioactive in situ hybridization and comparative immunocytochemistry. J Neurosci 17:1–10.
54. Sohn J, Orosco L, Guo F, Chung SH, Bannerman P, Mills Ko E et al (2015) The subventricular zone continues to generate corpus callosum and rostral migratory stream astroglia in normal adult mice. J Neurosci 35:3756–3763.
55. Song Y, Zhang Q, Kutlu B, Difilippantonio S, Bash R, Gilbert D et al (2013) Evolutionary etiology of high-grade astrocytomas. Proc Natl Acad Sci U S A 110:17933–17938.
56. Stupp R, Hegi ME, Mason WP, van den Bent MJ, Taphoorn MJ, Janzer RC et al (2009) Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol 10:459–466.
57. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ et al (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:987–996.
58. Suzuki A, Yamaguchi MT, Ohteki T, Sasaki T, Kaisho T, Kimura Y et al (2001) T cell-specific loss of Pten leads to defects in central and peripheral tolerance. Immunity 14:523–534.
59. Tsai HH, Li H, Fuentealba LC, Molofsky AV, Taveira-Marques R, Zhuang H et al (2012) Regional astrocyte allocation regulates CNS synaptogenesis and repair. Science 337:358–362.
60. Uhrbom L, Dai C, Celestino JC, Rosenblum MK, Fuller GN, Holland EC (2002) Ink4a-Arf loss cooperates with KRas activation in astrocytes and neural progenitors to generate glioblastomas of various morphologies depending on activated Akt. Cancer Res 62:5551–5558.
61. Verhaak RG, Hoadley KA, Purdom E, Wang V, Qi Y, Wilkerson MD et al (2010) Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 17:98–110.
62. Visvader JE (2011) Cells of origin in cancer. Nature 469:314–322.
63. Vitucci M, Karpinich NO, Bash RE, Werneke AM, Schmid RS, White KK et al (2013) Cooperativity between MAPK and PI3K signaling activation is required for glioblastoma pathogenesis. Neuro Oncol 15:1317–1329.
64. Wagner S, Czub S, Greif M, Vince GH, Suss N, Kerkau S et al (1999) Microglial/macrophage expression of interleukin 10 in human glioblastomas. Int J Cancer 82:12–16.
65. Wang DD, Bordey A (2008) The astrocyte odyssey. Prog Neurobiol 86:342–367.
66. Ward RJ, Dirks PB (2007) Cancer stem cells: at the headwaters of tumor development. Annu Rev Pathol 2:175–189.
67. Xiao A, Wu H, Pandolfi PP, Louis DN, Van Dyke T (2002) Astrocyte inactivation of the pRb pathway predisposes mice to malignant astrocytoma development that is accelerated by PTEN mutation. Cancer Cell 1:157–168.
68. Yeh TH, Lee da Y, Gianino SM, Gutmann DH (2009) Microarray analyses reveal regional astrocyte heterogeneity with implications for neurofibromatosis type 1 (NF1)-regulated glial proliferation. Glia 57:1239–1249.
69. Zhai H, Heppner FL, Tsirka SE (2011) Microglia/macrophages promote glioma progression. Glia 59:472–485.
70. Zheng H, Ying H, Yan H, Kimmelman AC, Hiller DJ, Chen AJ et al (2008) p53 and Pten control neural and glioma stem/progenitor cell renewal and differentiation. Nature 455:1129–1133.
71. Zhu Y, Guignard F, Zhao D, Liu L, Burns DK, Mason RP et al (2005) Early inactivation of p53 tumor suppressor gene cooperating with NF1 loss induces malignant astrocytoma. Cancer Cell 8:119–130.