Laminin alpha 2 enables glioblastoma stem cell growth

Annals of Neurology

Volumn 72, Issue 5, 2012, Pages 766-778

  Lathia, Justin D ^a,b   Li, Meizhang ^a   Hall, Peter E ^a   Gallagher, Joseph ^a   Hale, James S ^a   Wu, Qiulian ^a   Venere, Monica ^a   Levy, Emily ^a   Rani, M R Sandhya ^a   Huang, Ping ^a   Bae, Eunnyung ^a   Selfridge, Julia ^c   Cheng, Lin ^a   Guvenc, Hacer ^d   McLendon, Roger E ^e   Nakano, Ichiro ^d   Sloan, Andrew E ^b,f   Phillips, Heidi S ^g   Lai, Albert ^c   Gladson, Candece L ^a,b   Bredel, Markus ^h,i   Bao, Shideng ^a,b   Hjelmeland, Anita B ^a,b   Rich, Jeremy N ^a,b   more..

^a LERNER RESEARCH INSTITUTE   (United States)

^b UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d OHIO STATE UNIVERSITY   (United States)

^e DUKE UNIVERSITY MEDICAL CENTER   (United States)

^f CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^g GENENTECH INC   (United States)

^h The University of Alabama at Birmingham   (United States)

ⁱ UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA6 INTEGRIN; BETA1 INTEGRIN; HISTONE H2A; LAMININ ALPHA2; LAMININ ALPHA4;

ARTICLE; BIOINFORMATICS; CANCER INHIBITION; CANCER PROGNOSIS; CANCER STEM CELL; CELL COMPARTMENTALIZATION; CELL DEATH; CELL GROWTH; CELL PROLIFERATION; CELL RENEWAL; CELL SURVIVAL; COCULTURE; DNA REPAIR; ENDOTHELIUM CELL; EPENDYMOMA; EXTRACELLULAR MATRIX; GENE SILENCING; GLIOBLASTOMA; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN TARGETING; REFERENCE DATABASE; RNA INTERFERENCE; SIGNAL TRANSDUCTION; STEM CELL NICHE; TUMOR CELL; TUMOR GROWTH; TUMOR MICROENVIRONMENT;

ANALYSIS OF VARIANCE; ANTIGENS, CD; BRAIN NEOPLASMS; CELL SURVIVAL; COCULTURE TECHNIQUES; COMPUTATIONAL BIOLOGY; DOSE-RESPONSE RELATIONSHIP, RADIATION; ENDOTHELIAL CELLS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOBLASTOMA; GLYCOPROTEINS; HUMANS; KAPLAN-MEIER ESTIMATE; LAMININ; MAGNETIC RESONANCE IMAGING; MALE; NEOPLASTIC STEM CELLS; PEPTIDES; RADIATION; REGRESSION ANALYSIS; RNA INTERFERENCE; RNA, SMALL INTERFERING; TIME FACTORS; TISSUE ARRAY ANALYSIS; TUMOR CELLS, CULTURED; TUMOR MICROENVIRONMENT;

EID: 84871949179     PISSN: 03645134     EISSN: 15318249     Source Type: Journal    
DOI: 10.1002/ana.23674     Document Type: Article

References (65)

1. Stupp R, Hegi ME, Mason WP, et al. 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 2009; 10: 459-466.
2. Furnari FB, Fenton T, Bachoo RM, et al. Malignant astrocytic glioma: genetics, biology, and paths to treatment. Genes Dev 2007; 21: 2683-2710. (Pubitemid 350070717)
3. Venere M, Fine HA, Dirks PB, Rich JN,. Cancer stem cells in gliomas: identifying and understanding the apex cell in cancer's hierarchy. Glia 2011; 59: 1148-1154.
4. Singh SK, Clarke ID, Terasaki M, et al. Identification of a cancer stem cell in human brain tumors. Cancer Res 2003; 63: 5821-5828. (Pubitemid 37187480)
5. Singh SK, Hawkins C, Clarke ID, et al. Identification of human brain tumour initiating cells. Nature 2004; 432: 396-401. (Pubitemid 39551674)
6. Ignatova TN, Kukekov VG, Laywell ED, et al. Human cortical glial tumors contain neural stem-like cells expressing astroglial and neuronal markers in vitro. Glia 2002; 39: 193-206.
7. Hemmati HD, Nakano I, Lazareff JA, et al. Cancerous stem cells can arise from pediatric brain tumors. Proc Natl Acad Sci U S A 2003; 100: 15178-15183. (Pubitemid 37518036)
8. Galli R, Binda E, Orfanelli U, et al. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res 2004; 64: 7011-7021. (Pubitemid 39331011)
9. Bao S, Wu Q, Sathornsumetee S, et al. Stem cell-like glioma cells promote tumor angiogenesis through vascular endothelial growth factor. Cancer Res 2006; 66: 7843-7848. (Pubitemid 44299144)
10. 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. (Pubitemid 44949604)
11. Cheng L, Wu Q, Guryanova OA, et al. Elevated invasive potential of glioblastoma stem cells. Biochem Biophys Res Commun 2011; 406: 643-648.
12. Lathia JD, Heddleston JM, Venere M, Rich JN,. Deadly teamwork: neural cancer stem cells and the tumor microenvironment. Cell Stem Cell 2011; 8: 482-485.
13. Calabrese C, Poppleton H, Kocak M, et al. A perivascular niche for brain tumor stem cells. Cancer Cell 2007; 11: 69-82. (Pubitemid 46054518)
14. Gilbertson RJ, Rich JN,. Making a tumour's bed: glioblastoma stem cells and the vascular niche. Nat Rev Cancer 2007; 7: 733-736. (Pubitemid 47463683)
15. 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.
16. Zhu T, Costello MA, Talsma CE, et al. Endothelial cells create a stem cell niche in glioblastoma by providing Notch ligands that nurture self-renewal of cancer stem-like cells. Cancer Res 2011; 71: 6061-6072.
17. Friedman HS, Prados MD, Wen PY, et al. Bevacizumab alone and in combination with irinotecan in recurrent glioblastoma. J Clin Oncol 2009; 27: 4733-4740.
18. Paez-Ribes M, Allen E, Hudock J, et al. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell 2009; 15: 220-231.
19. Lathia JD, Rao MS, Mattson MP, Ffrench-Constant C. The microenvironment of the embryonic neural stem cell: lessons from adult niches? Dev Dyn 2007; 236: 3267-3282. (Pubitemid 350276385)
20. Kokovay E, Goderie S, Wang Y, et al. Adult SVZ lineage cells home to and leave the vascular niche via differential responses to SDF1/CXCR4 signaling. Cell Stem Cell 2010; 7: 163-173.
21. Shen Q, Wang Y, Kokovay E, et al. Adult SVZ stem cells lie in a vascular niche: A quantitative analysis of niche cell-cell interactions. Cell Stem Cell 2008; 3: 289-300.
22. Miner JH, Yurchenco PD,. Laminin functions in tissue morphogenesis. Annu Rev Cell Dev Biol 2004; 20: 255-284. (Pubitemid 39488639)
23. Colognato H, Ffrench-Constant C, Feltri ML,. Human diseases reveal novel roles for neural laminins. Trends Neurosci 2005; 28: 480-486. (Pubitemid 41187797)
24. Halfter W, Dong S, Yip YP, et al. A critical function of the pial basement membrane in cortical histogenesis. J Neurosci 2002; 22: 6029-6040. (Pubitemid 35387646)
25. Lathia JD, Patton B, Eckley DM, et al. Patterns of laminins and integrins in the embryonic ventricular zone of the CNS. J Comp Neurol 2007; 505: 630-643. (Pubitemid 350247130)
26. Hall PE, Lathia JD, Miller NG, et al. Integrins are markers of human neural stem cells. Stem Cells 2006; 24: 2078-2084. (Pubitemid 44477133)
27. Georges-Labouesse E, Mark M, Messaddeq N, Gansmuller A,. Essential role of alpha 6 integrins in cortical and retinal lamination. Curr Biol 1998; 8: 983-986. (Pubitemid 28447951)
28. Loulier K, Lathia JD, Marthiens V, et al. Beta1 integrin maintains integrity of the embryonic neocortical stem cell niche. PLoS Biol 2009; 7: e1000176.
29. Graus-Porta D, Blaess S, Senften M, et al. Beta1-class integrins regulate the development of laminae and folia in the cerebral and cerebellar cortex. Neuron 2001; 31: 367-379. (Pubitemid 32778557)
30. Lathia JD, Gallagher J, Heddleston JM, et al. Integrin alpha 6 regulates glioblastoma stem cells. Cell Stem Cell 2010; 6: 421-432.
31. Kawataki T, Yamane T, Naganuma H, et al. Laminin isoforms and their integrin receptors in glioma cell migration and invasiveness: evidence for a role of alpha5-laminin(s) and alpha3beta1 integrin. Exp Cell Res 2007; 313: 3819-3831. (Pubitemid 47566379)
32. Ljubimova JY, Fugita M, Khazenzon NM, et al. Association between laminin-8 and glial tumor grade, recurrence, and patient survival. Cancer 2004; 101: 604-612. (Pubitemid 38970612)
33. 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.
34. Fael Al-Mayhani TM, Ball SL, Zhao JW, et al. An efficient method for derivation and propagation of glioblastoma cell lines that conserves the molecular profile of their original tumours. J Neurosci Methods 2009; 176: 192-199.
35. Irizarry RA, Bolstad BM, Collin F, et al. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 2003; 31: e15.
36. Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 2008; 455: 1061-1068.
37. 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.
38. Lai A, Kharbanda S, Pope WB, et al. Evidence for sequenced molecular evolution of IDH1 mutant glioblastoma from a distinct cell of origin. J Clin Oncol 2011; 29: 4482-4490.
39. Eyler CE, Wu Q, Yan K, et al. Glioma stem cell proliferation and tumor growth are promoted by nitric oxide synthase-2. Cell 2011; 146: 53-66.
40. Li Z, Bao S, Wu Q, et al. Hypoxia-inducible factors regulate tumorigenic capacity of glioma stem cells. Cancer Cell 2009; 15: 501-513.
41. Kelly JJ, Stechishin O, Chojnacki A, et al. Proliferation of human glioblastoma stem cells occurs independently of exogenous mitogens. Stem Cells 2009; 27: 1722-1733.
42. Huang P, Rani MR, Ahluwalia MS, et al. Endothelial expression of TNF receptor-1 generates a proapoptotic signal inhibited by integrin alpha6beta1 in glioblastoma. Cancer Res 2012; 72: 1428-1437.
43. Miyazaki T, Pan Y, Joshi K, et al. Telomestatin impairs glioma stem cell survival and growth through the disruption of telomeric G-quadruplex and inhibition of the proto-oncogene, c-Myb. Clin Cancer Res 2012; 18: 1268-1280.
44. 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. (Pubitemid 43357943)
45. Hall PE, Lathia JD, Caldwell MA, Ffrench-Constant C,. Laminin enhances the growth of human neural stem cells in defined culture media. BMC Neurosci 2008; 9: 71.
46. Leins A, Riva P, Lindstedt R, et al. Expression of tenascin-C in various human brain tumors and its relevance for survival in patients with astrocytoma. Cancer 2003; 98: 2430-2439. (Pubitemid 37466658)
47. Behrem S, Zarkovic K, Eskinja N, Jonjic N,. Distribution pattern of tenascin-C in glioblastoma: correlation with angiogenesis and tumor cell proliferation. Pathol Oncol Res 2005; 11: 229-235. (Pubitemid 43266926)
48. Ziu M, Schmidt NO, Cargioli TG, et al. Glioma-produced extracellular matrix influences brain tumor tropism of human neural stem cells. J Neurooncol 2006; 79: 125-133. (Pubitemid 44349939)
49. Hambardzumyan D, Becher OJ, Rosenblum MK, et al. PI3K pathway regulates survival of cancer stem cells residing in the perivascular niche following radiation in medulloblastoma in vivo. Genes Dev 2008; 22: 436-448. (Pubitemid 351272752)
50. Witt H, Mack SC, Ryzhova M, et al. Delineation of two clinically and molecularly distinct subgroups of posterior fossa ependymoma. Cancer Cell 2011; 20: 143-157.
51. Cordes N, Seidler J, Durzok R, et al. Beta1-integrin-mediated signaling essentially contributes to cell survival after radiation-induced genotoxic injury. Oncogene 2006; 25: 1378-1390. (Pubitemid 43336466)
52. Hovinga KE, Shimizu F, Wang R, et al. Inhibition of notch signaling in glioblastoma targets cancer stem cells via an endothelial cell intermediate. Stem Cells 2010; 28: 1019-1029.
53. Campos LS, Decker L, Taylor V, Skarnes W,. Notch, epidermal growth factor receptor, and beta1-integrin pathways are coordinated in neural stem cells. J Biol Chem 2006; 281: 5300-5309. (Pubitemid 43847794)
54. Estrach S, Cailleteau L, Franco CA, et al. Laminin-binding integrins induce dll4 expression and notch signaling in endothelial cells. Circ Res 2011; 109: 172-182.
55. Karsan A,. Notch and integrin affinity: A sticky situation. Sci Signal 2008; 1: pe2.
56. Li H, Chang YW, Mohan K, et al. Activated Notch1 maintains the phenotype of radial glial cells and promotes their adhesion to laminin by upregulating nidogen. Glia 2008; 56: 646-658.
57. Tabatabai G, Tonn JC, Stupp R, Weller M,. The role of integrins in glioma biology and anti-glioma therapies. Curr Pharm Des 2011; 17: 2402-2410.
58. Wang H, Lathia JD, Wu Q, et al. Targeting interleukin 6 signaling suppresses glioma stem cell survival and tumor growth. Stem Cells 2009; 27: 2393-2404.
59. Charles N, Ozawa T, Squatrito M, et al. Perivascular nitric oxide activates notch signaling and promotes stem-like character in PDGF-induced glioma cells. Cell Stem Cell 2010; 6: 141-152.
60. Galan-Moya EM, Le Guelte A, Lima Fernandes E, et al. Secreted factors from brain endothelial cells maintain glioblastoma stem-like cell expansion through the mTOR pathway. EMBO Rep 2011; 12: 470-476.
61. El Hallani S, Boisselier B, Peglion F, et al. A new alternative mechanism in glioblastoma vascularization: Tubular vasculogenic mimicry. Brain 2010; 133 (pt 4): 973-982.
62. Ricci-Vitiani L, Pallini R, Biffoni M, et al. Tumour vascularization via endothelial differentiation of glioblastoma stem-like cells. Nature 2010; 468: 824-828.
63. Wang R, Chadalavada K, Wilshire J, et al. Glioblastoma stem-like cells give rise to tumour endothelium. Nature 2010; 468: 829-833.
64. Soda Y, Marumoto T, Friedmann-Morvinski D, et al. Transdifferentiation of glioblastoma cells into vascular endothelial cells. Proc Natl Acad Sci U S A 2011; 108: 4274-4280.
65. Campos LS, Leone DP, Relvas JB, et al. Beta1 integrins activate a MAPK signalling pathway in neural stem cells that contributes to their maintenance. Development 2004; 131: 3433-3444. (Pubitemid 39139889)