Telomere profiles and tumor-associated macrophages with different immune signatures affect prognosis in glioblastoma

Modern Pathology

Volumn 29, Issue 3, 2016, Pages 212-226

  Hung, Noelyn A ^a   Eiholzer, Ramona A ^a   Kirs, Stenar ^a   Zhou, Jean ^b   Ward Hartstonge, Kirsten ^c   Wiles, Anna K ^a   Frampton, Chris M ^d   Taha, Ahmad ^b   Royds, Janice A ^a   Slatter, Tania L ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b SOUTHERN DISTRICT HEALTH BOARD   (New Zealand)

^c UNIVERSITY OF OTAGO   (New Zealand)

^d UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; INTERFERON; PROTEIN; SUSHI REPEAT CONTAINING PROTEIN X LINKED 2 PROTEIN; TEMOZOLOMIDE; UNCLASSIFIED DRUG;

ADULT; ARTICLE; CANCER PROGNOSIS; CANCER RADIOTHERAPY; CANCER SURGERY; CANCER SURVIVAL; CLINICAL ARTICLE; GLIOBLASTOMA; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MACROPHAGE; PRIORITY JOURNAL; TELOMERE HOMEOSTASIS; TETRATRICOPEPTIDE REPEAT; TUMOR ASSOCIATED LEUKOCYTE; TUMOR IMMUNITY; AGED; BRAIN TUMOR; FEMALE; IMMUNOLOGY; KAPLAN MEIER METHOD; MALE; MIDDLE AGED; MORTALITY; PATHOLOGY; PHYSIOLOGY; POLYMERASE CHAIN REACTION; PROGNOSIS; TELOMERE; WESTERN BLOTTING;

ADULT; AGED; BLOTTING, WESTERN; BRAIN NEOPLASMS; FEMALE; GLIOBLASTOMA; HUMANS; IMMUNOHISTOCHEMISTRY; KAPLAN-MEIER ESTIMATE; MACROPHAGES; MALE; MIDDLE AGED; POLYMERASE CHAIN REACTION; PROGNOSIS; TELOMERE;

EID: 84959504281     PISSN: 08933952     EISSN: 15300285     Source Type: Journal    
DOI: 10.1038/modpathol.2015.156     Document Type: Article

References (73)

1. Stupp R, Mason WP, van den Bent MJ, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med. 2005; 352: 987-996.
2. Chen YJ, Hakin-Smith V, Teo M, et al. Association of mutant TP53 with alternative lengthening of telomeres and favorable prognosis in glioma. Cancer Res. 2006; 66: 6473-6476.
3. Hakin-Smith V, Jellinek DA, Levy D, et al. Alternative lengthening of telomeres and survival in patients with glioblastoma multiforme. Lancet. 2003; 361: 836-838.
4. Royds JA, Al Nadaf S, Wiles AK, et al. The CDKN2A G500 allele is more frequent in GBM patients with no defined telomere maintenance mechanism tumors and is associated with poorer survival. PloS One. 2011; 6: e26737.
5. Marian CO, Cho SK, McEllin BM, et al. The telomerase antagonist, imetelstat, efficiently targets glioblastoma tumor-initiating cells leading to decreased proliferation and tumor growth. Clin Cancer Res. 2010; 16: 154-163.
6. Ozawa T, Gryaznov SM, Hu LJ, et al. Antitumor effects of specific telomerase inhibitor GRN163 in human glioblastoma xenografts. Neuro Oncol. 2004; 6: 218-226.
7. Heaphy CM, Subhawong AP, Hong SM, et al. Prevalence of the alternative lengthening of telomeres telomere maintenance mechanism in human cancer subtypes. Am J Pathol. 2011; 179: 1608-1615.
8. Henson JD, Reddel RR. Assaying and investigating alternative lengthening of telomeres activity in human cells and cancers. FEBS Lett. 2010; 584: 3800-3811.
9. Henson JD, Hannay JA, McCarthy SW, et al. A robust assay for alternative lengthening of telomeres in tumors shows the significance of alternative lengthening of telomeres in sarcomas and astrocytomas. Clin Cancer Res. 2005; 11: 217-225.
10. Bryan TM, Englezou A, Dalla-Pozza L, et al. Evidence for an alternative mechanism for maintaining telomere length in human tumors and tumor-derived cell lines. Nat Med. 1997; 3: 1271-1274.
11. Bryan TM, Reddel RR. Telomere dynamics and telomerase activity in in vitro immortalised human cells. Eur J Cancer. 1997; 33: 767-773.
12. McDonald KL, McDonnell J, Muntoni A, et al. Presence of alternative lengthening of telomeres mechanism in patients with glioblastoma identifies a less aggressive tumor type with longer survival. J Neuropathol Exp Neurol. 2010; 69: 729-736.
13. Phillips HS, Kharbanda S, Chen R, et al. Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis. Cancer Cell. 2006; 9: 157-173.
14. Verhaak RG, Hoadley KA, Purdom E, et al. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell. 2010; 17: 98-110.
15. Carro MS, Lim WK, Alvarez MJ, et al. The transcriptional network for mesenchymal transformation of brain tumours. Nature. 2010; 463: 318-325.
16. Slatter T, Gifford-Garner J, Wiles A, et al. Pilocytic astrocytomas have telomere-Associated promyelocytic leukemia bodies without alternatively lengthened telomeres. Am J Pathol. 2010; 177: 2694-2700.
17. Tabori U, Vukovic B, Zielenska M, et al. The role of telomere maintenance in the spontaneous growth arrest of pediatric low-grade gliomas. Neoplasia. 2006; 8: 136-142.
18. Chen Q, Ijpma A, Greider CW. Two survivor pathways that allow growth in the absence of telomerase are generated by distinct telomere recombination events. Mol Cell Biol. 2001; 21: 1819-1827.
19. Siddiqa A, Cavazos D, Chavez J, et al. Modulation of telomeres in alternative lengthening of telomeres type I like human cells by the expression of Werner protein and telomerase. J Oncol. 2012; 2012: 806382.
20. Gocha AR, Acharya S, Groden J. WRN loss induces switching of telomerase-independent mechanisms of telomere elongation. PloS One. 2014; 9: e93991.
21. Morantz RA, Wood GW, Foster M, et al. Macrophages in experimental and human brain tumors. Part 2: Studies of the macrophage content of human brain tumors. J Neurosurg. 1979; 50: 305-311.
22. Morimura T, Neuchrist C, Kitz K, et al. Monocyte subpopulations in human gliomas: expression of Fc and complement receptors and correlation with tumor proliferation. Acta Neuropathol. 1990; 80: 287-294.
23. Roggendorf W, Strupp S, Paulus W. Distribution and characterization of microglia/macrophages in human brain tumors. Acta Neuropathol. 1996; 92: 288-293.
24. Sasai K, Nodagashira M, Nishihara H, et al. Careful exclusion of non-neoplastic brain components is required for an appropriate evaluation of O6-methylguanine-DNA methyltransferase status in glioma: relationship between immunohistochemistry and methylation analysis. Am J Surg Pathol. 2008; 32: 1220-1227.
25. Komohara Y, Ohnishi K, Kuratsu J, et al. Possible involvement of the M2 anti-inflammatory macrophage phenotype in growth of human gliomas. J Pathol. 2008; 216: 15-24.
26. Hsu CY, Lin SC, Ho HL, et al. Exclusion of histiocytes/ endothelial cells and using endothelial cells as internal reference are crucial for interpretation of MGMT immunohistochemistry in glioblastoma. Am J Surg Pathol. 2013; 37: 264-271.
27. Robson EJ, He SJ, Eccles MR. A PANorama of PAX genes in cancer and development. Nat Rev Cancer. 2006; 6: 52-62.
28. Hung N, Chen YJ, Taha A, et al. Increased paired box transcription factor 8 has a survival function in glioma. BMC Cancer. 2014; 14: 159.
29. Chen YJ, Campbell HG, Wiles AK, et al. PAX8 regulates telomerase reverse transcriptase and telomerase RNA component in glioma. Cancer Res. 2008; 68: 5724-5732.
30. Kim NW, Piatyszek MA, Prowse KR, et al. Specific association of human telomerase activity with immortal cells and cancer. Science. 1994; 266: 2011-2015.
31. Li R, Yu C, Li Y, et al. SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics. 2009; 25: 1966-1967.
32. Sarma SN, Kim YJ, Ryu JC. Gene expression profiles of human promyelocytic leukemia cell lines exposed to volatile organic compounds. Toxicology. 2010; 271: 122-130.
33. Baqir M, Chen CZ, Martin RJ, et al. Cigarette smoke decreases MARCO expression in macrophages: implication in Mycoplasma pneumoniae infection. Respir Med. 2008; 102: 1604-1610.
34. Gao Z, Zhang J, Bi M, et al. SRPX2 promotes cell migration and invasion via FAK dependent pathway in pancreatic cancer. Int J Clin Exp Pathol. 2015; 8: 4791-4798.
35. Boudot A, Kerdivel G, Lecomte S, et al. COUP-TFI modifies CXCL12 and CXCR4 expression by activating EGF signaling and stimulates breast cancer cell migration. BMC Cancer. 2014; 14: 407.
36. Borda JT, Alvarez X, Mohan Met al. CD163, a marker of perivascular macrophages, is up-regulated by microglia in simian immunodeficiency virus encephalitis after haptoglobin-hemoglobin complex stimulation and is suggestive of breakdown of the blood-brain barrier. Am J Pathol. 2008; 172: 725-737.
37. Madsen M, Moller HJ, Nielsen MJ, et al. Molecular characterization of the haptoglobin.hemoglobin receptor CD163. Ligand binding properties of the scavenger receptor cysteine-rich domain region. J Biol Chem. 2004; 279: 51561-51567.
38. Zhou W, Ke SQ, Huang Z, et al. Periostin secreted by glioblastoma stem cells recruits M2 tumour-Associated macrophages and promotes malignant growth. Nat Cell Biol. 2015; 17: 170-182.
39. Bingle L, Brown NJ, Lewis CE. The role of tumourassociated macrophages in tumour progression: implications for new anticancer therapies. J Pathol. 2002; 196: 254-265.
40. Noorani IPG, Grundy PL, Sharpe G, et al. Novel association between microglia and stem cells in human gliomas: A contributor to tumour proliferation?. J Pathol: Clin Res. 2015; 1: 67-75.
41. Ye XZ, Xu SL, Xin YH, et al. Tumor-Associated microglia/macrophages enhance the invasion of glioma stem-like cells via TGF-beta1 signaling pathway. J Immunol. 2012; 189: 444-453.
42. Wagner S, Czub S, Greif M, et al. Microglial/macrophage expression of interleukin 10 in human glioblastomas. Int J Cancer. 1999; 82: 12-16.
43. Hao C, Parney IF, Roa WH, et al. Cytokine and cytokine receptor mRNA expression in human glioblastomas: evidence of Th1, Th2 and Th3 cytokine dysregulation. Acta Neuropathol. 2002; 103: 171-178.
44. Moffett JR, Els T, Espey MG, et al. Quinolinate immunoreactivity in experimental rat brain tumors is present in macrophages but not in astrocytes. Exp Neurol. 1997; 144: 287-301.
45. Hussain SF, Yang D, Suki D, et al. The role of human glioma-infiltrating microglia/macrophages in mediating antitumor immune responses. Neuro Oncol. 2006; 8: 261-279.
46. Ludwig HC, Feiz-Erfan I, Bockermann V, et al. Expression of nitric oxide synthase isozymes (NOS I-III) by immunohistochemistry and DNA in situ hybridization. Correlation with macrophage presence, vascular endothelial growth factor (VEGF) and oedema volumetric data in 220 glioblastomas. Anticancer Res. 2000; 20: 299-304.
47. Arredouani MS, Franco F, Imrich A, et al. Scavenger Receptors SR-AI/II and MARCO limit pulmonary dendritic cell migration and allergic airway inflammation. J Immunol. 2007; 178: 5912-5920.
48. Arredouani MS, Palecanda A, Koziel H, et al. MARCO is the major binding receptor for unopsonized particles and bacteria on human alveolar macrophages. J Immunol. 2005; 175: 6058-6064.
49. Dahl M, Bauer AK, Arredouani M, et al. Protection against inhaled oxidants through scavenging of oxidized lipids by macrophage receptors MARCO and SR-AI/II. J Clin Invest. 2007; 117: 757-764.
50. Thakur SA, Beamer CA, Migliaccio CT, et al. Critical role of MARCO in crystalline silica-induced pulmonary inflammation. Toxicol Sci. 2009; 108: 462-471.
51. Ghosh S, Gregory D, Smith A, et al. MARCO regulates early inflammatory responses against influenza: a useful macrophage function with adverse outcome. Am J Respir Cell Mol Biol. 2011; 45: 1036-1044.
52. Murthy S, Larson-Casey JL, Ryan AJ, et al. Alternative activation of macrophages and pulmonary fibrosis are modulated by scavenger receptor, macrophage receptor with collagenous structure. FASEB J. 2015; 29: 3527-3536.
53. Stoger JL, Gijbels MJ, van der Velden S, et al. Distribution of macrophage polarization markers in human atherosclerosis. Atherosclerosis. 2012; 225: 461-468.
54. Martinez FO, Sica A, Mantovani A, et al. Macrophage activation and polarization. Front Biosci. 2008; 13: 453-461.
55. Kissick HT, Dunn LK, Ghosh S, et al. The scavenger receptor MARCO modulates TLR-induced responses in dendritic cells. PloS One. 2014; 9: e104148.
56. Kryczek I, Lange A, Mottram P, et al. CXCL12 and vascular endothelial growth factor synergistically induce neoangiogenesis in human ovarian cancers. Cancer Res. 2005; 65: 465-472.
57. Miljkovic-Licina M, Hammel P, Garrido-Urbani S, et al. Sushi repeat protein X-linked 2, a novel mediator of angiogenesis. FASEB J. 2009; 23: 4105-4116.
58. Deininger MH, Pater S, Strik H, et al. Macrophage/ microglial cell subpopulations in glioblastoma multiforme relapses are differentially altered by radiochemotherapy. J Neurooncol. 2001; 55: 141-147.
59. Geisenberger C, Mock A, Warta R, et al. Molecular profiling of long-Term survivors identifies a subgroup of glioblastoma characterized by chromosome 19/20 cogain. Acta Neuropathol. 2015; 130: 419-434.
60. Strachan DC, Ruffell B, Oei Y, et al. CSF1R inhibition delays cervical and mammary tumor growth in murine models by attenuating the turnover of tumor-Associated macrophages and enhancing infiltration by CD8 T cells. Oncoimmunology. 2013; 2: e26968.
61. Pyonteck SM, Akkari L, Schuhmacher AJ, et al. CSF-1R inhibition alters macrophage polarization and blocks glioma progression. Nat Med. 2013; 19: 1264-1272.
62. Yi X, Shay JW, Wright WE. Quantitation of telomerase components and hTERT mRNA splicing patterns in immortal human cells. Nucleic Acids Res. 2001; 29: 4818-4825.
63. Weng NP, Levine BL, June CH, et al. Regulated expression of telomerase activity in human T lymphocyte development and activation. J Exp Med. 1996; 183: 2471-2479.
64. Qin Y, Guo H, Tang B, et al. The non-reverse transcriptase activity of the human telomerase reverse transcriptase promotes tumor progression (review). Int J Oncol. 2014; 45: 525-531.
65. Staudt ND, Jo M, Hu J, et al. Myeloid cell receptor LRP1/ CD91 regulates monocyte recruitment and angiogenesis in tumors. Cancer Res. 2013; 73: 3902-3912.
66. Ling EA, Wong WC. The origin and nature of ramified and amoeboid microglia: a historical review and current concepts. Glia. 1993; 7: 9-18.
67. Sen GC, Sarkar SN. The interferon-stimulated genes: targets of direct signaling by interferons, doublestranded RNA, and viruses. Curr Top Microbiol Immunol. 2007; 316: 233-250.
68. Diamond MS, Farzan M. The broad-spectrum antiviral functions of IFIT and IFITM proteins. Nat Rev Immunol. 2013; 13: 46-57.
69. Yu M, Tong JH, Mao M, et al. Cloning of a gene (RIG-G) associated with retinoic acid-induced differentiation of acute promyelocytic leukemia cells and representing a new member of a family of interferon-stimulated genes. Proc Natl Acad Sci USA. 1997; 94: 7406-7411.
70. Daffis S, Samuel MA, Keller BC, et al. Cell-specific IRF-3 responses protect against West Nile virus infection by interferon-dependent and -independent mechanisms. PLoS Pathog. 2007; 3: e106.
71. Alentorn A, Duran-Pena A, Malousi A, et al. Differential gene methylation in paired glioblastomas suggests a role of immune response pathways in tumor progression. J Neurooncol. 2015; 124: 385-392.
72. Potter C, Harris AL. Hypoxia inducible carbonic anhydrase IX, marker of tumour hypoxia, survival pathway and therapy target. Cell Cycle. 2004; 3: 164-167.
73. Lewis C, Murdoch C. Macrophage responses to hypoxia: implications for tumor progression and anticancer therapies. Am J Pathol. 2005; 167: 627-635.