TGFβ-Responsive HMOX1 Expression Is Associated with Stemness and Invasion in Glioblastoma Multiforme

Stem Cells

Volumn 34, Issue 9, 2016, Pages 2276-2289

  Ghosh, Dhiman ^a,b   Ulasov, Ilya V ^a   Chen, LiPing ^a   Harkins, Lualhati E ^c   Wallenborg, Karolina ^b   Hothi, Parvinder ^a   Rostad, Steven ^a,d   Hood, Leroy ^b   Cobbs, Charles S ^a,b  

^a SWEDISH MEDICAL CENTER   (United States)

^b INSTITUTE FOR SYSTEMS BIOLOGY   (United States)

^c Medical Center   (United States)

^d Cellnetix Pathology and Laboratories   (United States)

Author keywords

CSC; GBM; Invasion; Neurosphere; NSC; Pseudopalisading

Indexed keywords

ARGININE; CADMI PROTEIN; CD133 ANTIGEN; CLCC1 PROTEIN; HEME OXYGENASE 1; LYSINE; MONOCARBOXYLATE TRANSPORTER 1; NESTIN; OCTAMER TRANSCRIPTION FACTOR 4; PROTEIN; SCAMP3 PROTEIN; SMAD2 PROTEIN; TRANSCRIPTION FACTOR SOX2; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ARTICLE; CANCER PROGNOSIS; CANCER STEM CELL; CELL INVASION; CELL PROLIFERATION; CONTROLLED STUDY; FLOW CYTOMETRY; GLIOBLASTOMA; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MASS SPECTROMETRY; NEURAL STEM CELL; PHENOTYPE; PROSPECTIVE STUDY; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; STEM CELL SELF-RENEWAL; TUMOR INVASION;

EID: 84985931281     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.2411     Document Type: Article

References (95)

1. Dolecek TA, Propp JM, Stroup NE et al. CBTRUS statistical report: Primary brain and central nervous system tumors diagnosed in the united states in 2005-2009. Neuro Oncol 2012;14(suppl 5):v1–49.
2. Mrugala MM, Adair J, Kiem HP. Outside the box–novel therapeutic strategies for glioblastoma. Cancer J 2012;18:51–58.
3. Weller M, Cloughesy T, Perry JR et al. Standards of care for treatment of recurrent glioblastoma–are we there yet? Neuro Oncol 2013;15:4–27.
4. Bao S, Wu Q, McLendon RE et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006;444:756–760.
5. Singh SK, Clarke ID, Terasaki M et al. Identification of a cancer stem cell in human brain tumors. Cancer Res 2003;63:5821–5828.
6. Hemmati HD, Nakano I, Lazareff JA et al. Cancerous stem cells can arise from Pediatric brain tumors. Proc Natl Acad Sci USA 2003;100:15178–15183.
7. O'Brien CA, Pollett A, Gallinger S et al. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 2007;445:106–110.
8. Vaillant F, Asselin-Labat ML, Shackleton M et al. The mammary progenitor marker CD61/beta3 integrin identifies cancer stem cells in mouse models of mammary tumorigenesis. Cancer Res 2008;68:7711–7717.
9. Visvader JE, Lindeman GJ. Cancer stem cells in solid tumours: Accumulating evidence and unresolved questions. Nat Rev Cancer 2008;8:755–768.
10. Lathia JD, Mack SC, Mulkearns-Hubert EE et al. Cancer stem cells in glioblastoma. Genes Dev 2015;29:1203–1217.
11. Jackson M, Hassiotou F, Nowak A. Glioblastoma stem-like cells: At the root of tumor recurrence and a therapeutic target. Carcinogenesis 2015;36:177–185.
12. Chen J, Li Y, Yu TS et al. A restricted cell population propagates glioblastoma growth after chemotherapy. Nature 2012;488:522–526.
13. Singh SK, Venugopal C, Hallett R et al. Pyrvinium targets CD133 in human glioblastoma brain tumor-initiating cells. Clin Canc Res 2015;21:5324.
14. Bao S, Wu Q, Li Z et al. Targeting cancer stem cells through L1CAM suppresses glioma growth. Cancer Res 2008;68:6043–6048.
15. Anido J, Saez-Borderias A, Gonzalez-Junca A et al. TGF-beta receptor inhibitors target the CD44(high)/Id1(high) Glioma-initiating cell population in human Glioblastoma. Cancer Cell 2010;18:655–668.
16. Son MJ, Woolard K, Nam DH et al. SSEA-1 is an enrichment marker for tumor-initiating cells in human glioblastoma. Cell Stem Cell 2009;4:440–452.
17. Lathia JD, Gallagher J, Heddleston JM et al. Integrin alpha 6 regulates glioblastoma stem cells. Cell Stem Cell 2010;6:421–432.
18. Venere M, Horbinski C, Crish JF et al. The mitotic kinesin KIF11 is a driver of invasion, proliferation, and self-renewal in glioblastoma. Sci Transl Med 2015;7:304ra143.
19. Maness PF, Schachner M. Neural recognition molecules of the immunoglobulin superfamily: Signaling transducers of axon guidance and neuronal migration. Nat Neurosci 2007;10:19–26.
20. Sykes AM, Huttner WB. Prominin-1 (CD133) and the cell biology of neural progenitors and their Progeny. Adv Exp Med Biol 2013;777:89–98.
21. Uchida N, Buck DW, He D et al. Direct isolation of human central nervous system stem cells. Proc Natl Acad Sci USA 2000;97:14720–14725.
22. Lee A, Kessler JD, Read TA et al. Isolation of neural stem cells from the postnatal cerebellum. Nat Neurosci 2005;8:723–729.
23. Beier D, Hau P, Proescholdt M et al. CD133(+) and CD133(-) glioblastoma-derived cancer stem cells show differential growth characteristics and molecular profiles. Cancer Res 2007;67:4010–4015.
24. Meng X, Li M, Wang X et al. Both CD133+ and CD133- subpopulations of A549 and H446 cells contain cancer-initiating cells. Cancer Sci 2009;100:1040–1046.
25. Wang J, Sakariassen PO, Tsinkalovsky O et al. CD133 negative glioma cells form tumors in nude rats and give rise to CD133 positive cells. Int J Cancer 2008;122:761–768.
26. Lottaz C, Beier D, Meyer K et al. Transcriptional profiles of CD133+ and CD133- glioblastoma-derived cancer stem cell lines suggest different cells of origin. Cancer Res 2010;70:2030–2040.
27. Kenney-Herbert E, Al-Mayhani T, Piccirillo SG et al. CD15 expression does not identify a phenotypically or genetically distinct glioblastoma Population. Stem Cells Transl Med 2015;4:822–831.
28. Horst D, Scheel SK, Liebmann S et al. The cancer stem cell marker CD133 has high prognostic impact but unknown functional relevance for the metastasis of human colon cancer. J Pathol 2009;219:427–434.
29. Picotti P Aebersold R. Selected reaction monitoring-based proteomics: workflows, potential, pitfalls and future directions. Nat Methods 2012;9:555–566.
30. Schiess R, Wollscheid B Aebersold R. Targeted proteomic strategy for clinical biomarker discovery. Mol Oncol 2009;3:33–44.
31. Madhavan S, Zenklusen JC, Kotliarov Y et al. Rembrandt: helping personalized medicine become a reality through integrative translational research. Mol Cancer Res 2009;7:157–167.
32. Cancer Genome Atlas Research N. Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 2008;455:1061–1068.
33. Okumura S, Baba H, Kumada T et al. Cloning of a G-protein-coupled receptor that shows an activity to transform NIH3T3 cells and is expressed in gastric cancer cells. Canc Sci 2004;95:131–135.
34. Teh JL, Chen S. Glutamatergic signaling in cellular transformation. Pigment Cell Melanoma Res 2012;25:331–342.
35. Pollard SM, Yoshikawa K, Clarke ID et al. Glioma stem cell lines expanded in adherent culture have tumor-specific phenotypes and are suitable for chemical and genetic screens. Cell Stem Cell 2009;4:568–580.
36. Ulasov IV, Shah N, Kaverina NV et al. Tamoxifen improves cytopathic effect of oncolytic adenovirus in primary glioblastoma cells mediated through autophagy. Oncotarget 2015;6:3977–3987.
37. Wang MY, Lu KV, Zhu S et al. Mammalian target of rapamycin inhibition promotes response to epidermal growth factor receptor kinase inhibitors in PTEN-deficient and PTEN-intact glioblastoma cells. Cancer Res 2006;66:7864–7869.
38. Alcantara Llaguno S, Chen J, Kwon CH et al. Malignant astrocytomas originate from neural stem/progenitor cells in a somatic tumor suppressor mouse model. Cancer Cell 2009;15:45–56.
39. Alcantara Llaguno SR, Chen J, Parada LF. Signaling in malignant astrocytomas: role of neural stem cells and its therapeutic implications. Clin Cancer Res 2009;15:7124–7129.
40. Lim DA, Cha S, Mayo MC et al. Relationship of glioblastoma multiforme to neural stem cell regions predicts invasive and multifocal tumor phenotype. Neuro Oncol 2007;9:424–429.
41. Zhu Y, Guignard F, Zhao D et al. Early inactivation of p53 tumor suppressor gene cooperating with NF1 loss induces malignant astrocytoma. Cancer Cell 2005;8:119–130.
42. Hollon TC, Price RL, Kwon CH et al. Mutations in glioblastoma oncosuppressive pathways pave the way for oncomodulatory activity of cytomegalovirus. Oncoimmunology 2013;2:e25620.
43. Price RL, Song J, Bingmer K et al. Cytomegalovirus contributes to glioblastoma in the context of tumor suppressor mutations. Cancer Res 2013;73:3441–3450.
44. Goffart N, Kroonen J, Rogister B. Glioblastoma-initiating cells: Relationship with neural stem cells and the micro-environment. Cancers 2013;5:1049–1071.
45. Fagerberg L, Jonasson K, von Heijne G et al. Prediction of the human membrane proteome. Proteomics 2010;10:1141–1149.
46. Ghosh D, Lippert D, Krokhin O et al. Defining the membrane proteome of NK cells. J Mass Spectrom 2010;45:1–25.
47. Bereman MS, MacLean B, Tomazela DM et al. The development of selected reaction monitoring methods for targeted proteomics via empirical refinement. Proteomics 2012;12:1134–1141.
48. Maclean B, Tomazela DM, Abbatiello SE et al. Effect of collision energy optimization on the measurement of peptides by selected reaction monitoring (SRM) mass spectrometry. Anal Chem 2010;82:10116–10124.
49. Rong Y, Durden DL, Van Meir EG et al. ‘Pseudopalisading’ necrosis in glioblastoma: A familiar morphologic feature that links vascular pathology, hypoxia, and angiogenesis. J Neuropathol Exp Neurol 2006;65:529–539.
50. Laks DR, Masterman-Smith M, Visnyei K et al. Neurosphere formation is an independent predictor of clinical outcome in malignant glioma. Stem Cells 2009;27:980–987.
51. Reynolds BA, Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 1992;255:1707–1710.
52. Reynolds BA, Rietze RL. Neural stem cells and neurospheres–re-evaluating the relationship. Nat Methods 2005;2:333–336.
53. Pastrana E, Silva-Vargas V, Doetsch F. Eyes wide open: A critical review of sphere-formation as an assay for stem cells. Cell Stem Cell 2011;8:486–498.
54. Singh A, Settleman J. EMT, cancer stem cells and drug resistance: An emerging axis of evil in the war on cancer. Oncogene 2010;29:4741–4751.
55. Pattabiraman DR, Weinberg RA. Tackling the cancer stem cells—what challenges do they pose? Nat Rev Drug Discov 2014;13:497–512.
56. Johns LD, Babcock G, Green D et al. Transforming growth factor-beta 1 differentially regulates proliferation and MHC class-II antigen expression in forebrain and brainstem astrocyte primary cultures. Brain Res 1992;585:229–236.
57. Rich JN, Zhang M, Datto MB et al. Transforming growth factor-beta-mediated p15(INK4B) induction and growth inhibition in astrocytes is SMAD3-dependent and a pathway prominently altered in human glioma cell lines. J Biol Chem 1999;274:35053–35058.
58. Aigner L, Bogdahn U. TGF-beta in neural stem cells and in tumors of the central nervous system. Cell Tissue Res 2008;331:225–241.
59. Golestaneh N, Mishra B. TGF-beta, neuronal stem cells and glioblastoma. Oncogene 2005;24:5722–5730.
60. Massague J. TGFbeta signalling in context. Nat Rev Mol Cell Biol 2012;13:616–630.
61. Li DM, Sun H. TEP1, encoded by a candidate tumor suppressor locus, is a novel protein tyrosine phosphatase regulated by transforming growth factor beta. Cancer Res 1997;57:2124–2129.
62. Chow JY, Quach KT, Cabrera BL et al. RAS/ERK modulates TGFbeta-regulated PTEN expression in human pancreatic adenocarcinoma cells. Carcinogenesis 2007;28:2321–2327.
63. Hjelmeland AB, Hjelmeland MD, Shi Q et al. Loss of phosphatase and tensin homologue increases transforming growth factor beta-mediated invasion with enhanced SMAD3 transcriptional activity. Cancer Res 2005;65:11276–11281.
64. Chen W, Zhong X, Wei Y et al. TGF-beta regulates survivin to affect cell cycle and the expression of EGFR and MMP9 in Glioblastoma. Mol Neurobiol 2016; 53:1648–1653.
65. Pala A, Karpel-Massler G, Kast RE et al. Epidermal to mesenchymal transition and failure of EGFR-targeted therapy in Glioblastoma. Cancers 2012;4:523–530.
66. Penuelas S, Anido J, Prieto-Sanchez RM et al. TGF-beta increases glioma-initiating cell self-renewal through the induction of LIF in human glioblastoma. Cancer Cell 2009;15:315–327.
67. Shao H, Chung J, Balaj L et al. Protein typing of circulating microvesicles allows real-time monitoring of glioblastoma therapy. Nat Med 2012;18:1835–1840.
68. Li XJ, Hayward C, Fong PY et al. A blood-based proteomic classifier for the molecular characterization of pulmonary nodules. Sci Transl Med 2013;5:207ra142.
69. Lathia JD, Li M, Sinyuk M et al. High-throughput flow cytometry screening reveals a role for junctional adhesion molecule a as a cancer stem cell maintenance factor. Cell Rep 2014;6:117–129.
70. Wang Y, Yang J, Zheng H et al. Expression of mutant p53 proteins implicates a lineage relationship between neural stem cells and malignant astrocytic glioma in a murine model. Cancer Cell 2009;15:514–526.
71. Zheng H, Ying H, Yan H et al. p53 and pten control neural and glioma stem/progenitor cell renewal and differentiation. Nature 2008;455:1129–1133.
72. Kemper K, Sprick MR, de Bree M et al. The AC133 epitope, but not the CD133 protein, is lost upon cancer stem cell differentiation. Cancer Res 2010;70:719–729.
73. Ginestier C, Hur MH, Charafe-Jauffret E et al. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 2007;1:555–567.
74. Piccirillo SG, Combi R, Cajola L et al. Distinct pools of cancer stem-like cells coexist within human glioblastomas and display different tumorigenicity and independent genomic evolution. Oncogene 2009;28:1807–1811.
75. Brat DJ, Castellano-Sanchez AA, Hunter SB et al. Pseudopalisades in glioblastoma are hypoxic, express extracellular matrix proteases, and are formed by an actively migrating cell population. Cancer Res 2004;64:920–927.
76. Poss KD, Tonegawa S. Reduced stress defense in heme oxygenase 1-deficient cells. Proc Natl Acad Sci USA 1997;94:10925–10930.
77. Was H, Sokolowska M, Sierpniowska A et al. Effects of heme oxygenase-1 on induction and development of chemically induced squamous cell carcinoma in mice. Free Radic Biol Med 2011;51:1717–1726.
78. Vieira HL, Alves PM, Vercelli A. Modulation of neuronal stem cell differentiation by hypoxia and reactive oxygen species. Progr Neurobiol 2011;93:444–455.
79. Almeida AS, Figueiredo-Pereira C, Vieira HL. Carbon monoxide and mitochondria-modulation of cell metabolism, redox response and cell death. Front Physiol 2015;6:33.
80. Lo Iacono L, Boczkowski J, Zini R et al. A carbon monoxide-releasing molecule (CORM-3) uncouples mitochondrial respiration and modulates the production of reactive oxygen species. Free Radic Biol Med 2011;50:1556–1564.
81. Queiroga CS, Almeida AS, Vieira HL. Carbon monoxide targeting mitochondria. Biochem Res Int 2012;2012:749845.
82. Wegiel B, Gallo D, Csizmadia E et al. Carbon monoxide expedites metabolic exhaustion to inhibit tumor growth. Cancer Res 2013;73:7009–7021.
83. Diehn M, Cho RW, Lobo NA et al. Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 2009;458:780–783.
84. Dong XZ, Zhang M, Wang K et al. Sanguinarine inhibits vascular endothelial growth factor release by generation of reactive oxygen species in MCF-7 human mammary adenocarcinoma cells. BioMed Res Int 2013;2013:517698.
85. Burger JA, Peled A. CXCR4 antagonists: targeting the microenvironment in leukemia and other cancers. Leukemia 2009;23:43–52.
86. Lu J, Ye X, Fan F et al. Endothelial cells promote the colorectal cancer stem cell phenotype through a soluble form of Jagged-1. Cancer Cell 2013;23:171–185.
87. Butler JM, Kobayashi H, Rafii S. Instructive role of the vascular niche in promoting tumour growth and tissue repair by angiocrine factors. Nat Rev Cancer 2010;10:138–146.
88. Hossain A, Gumin J, Gao F et al. Mesenchymal stem cells isolated from human gliomas increase proliferation and maintain stemness of glioma stem cells through the IL-6/gp130/STAT3 Pathway. Stem Cells 2015;33:2400–2415.
89. Witz IP. The tumor microenvironment: the making of a paradigm. Cancer Microenviron 2009;2(suppl 1):9–17.
90. Persano L, Rampazzo E, Basso G et al. Glioblastoma cancer stem cells: Role of the microenvironment and therapeutic targeting. Biochem Pharmacol 2013;85:612–622.
91. Rich JN. The role of transforming growth factor-beta in primary brain tumors. Front Biosci 2003;8:e245–e260.
92. Joseph JV, Balasubramaniyan V, Walenkamp A et al. TGF-beta as a therapeutic target in high grade gliomas—promises and challenges. Biochem Pharmacol 2013;85:478–485.
93. Imamura T, Hikita A, Inoue Y. The roles of TGF-beta signaling in carcinogenesis and breast cancer metastasis. Breast Cancer 2012;19:118–124.
94. Wierenga AT, Vellenga E Schuringa JJ. Convergence of hypoxia and TGFbeta pathways on cell cycle regulation in human hematopoietic stem/progenitor cells. PloS One 2014;9:e93494.
95. Cobbs CS, Matlaf L, Harkins LE. Methods for the detection of cytomegalovirus in glioblastoma cells and tissues. Methods Mol Biol 2014;1119:165–196.