Neural Precursor-Derived Pleiotrophin Mediates Subventricular Zone Invasion by Glioma

Cell

Volumn 170, Issue 5, 2017, Pages 845-859.e19

  Qin, Elizabeth Y ^a   Cooper, Dominique D ^a   Abbott, Keene L ^a   Lennon, James ^a   Nagaraja, Surya ^a   Mackay, Alan ^b   Jones, Chris ^b   Vogel, Hannes ^a   Jackson, Peter K ^a   Monje, Michelle ^a  

^a STANFORD UNIVERSITY   (United States)

^b INSTITUTE OF CANCER RESEARCH   (United Kingdom)

Author keywords

diffuse intrinsic pontine glioma; glioblastoma; HSP90; invasion; neural precursor cell; pleiotrophin; SPARC; SPARCL1; subventricular zone

Indexed keywords

HEAT SHOCK PROTEIN 90; HEAT SHOCK PROTEIN 90B; OSTEONECTIN; PLEIOTROPHIN; RHO KINASE; UNCLASSIFIED DRUG; CARRIER PROTEIN; CYTOKINE; RHO GUANINE NUCLEOTIDE BINDING PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CELL COMMUNICATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; FEMALE; GLIOMA; HUMAN; HUMAN CELL; HUMAN TISSUE; INTRACELLULAR SIGNALING; MALE; MOUSE; NEURAL STEM CELL; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SECRETION; SUBVENTRICULAR ZONE; TUMOR INVASION; AGED; ANIMAL; ANTAGONISTS AND INHIBITORS; BRAIN TUMOR; CANCER TRANSPLANTATION; CHILD; DRUG DELIVERY SYSTEM; LATERAL BRAIN VENTRICLE; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION; XENOGRAFT;

AGED; ANIMALS; BRAIN NEOPLASMS; CARRIER PROTEINS; CELL COMMUNICATION; CHILD; CYTOKINES; DRUG DELIVERY SYSTEMS; FEMALE; GLIOMA; HETEROGRAFTS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; LATERAL VENTRICLES; MALE; MICE; NEOPLASM INVASIVENESS; NEOPLASM TRANSPLANTATION; RHO GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION;

EID: 85027488712     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2017.07.016     Document Type: Article

References (76)

1. Aboody, K.S., Brown, A., Rainov, N.G., Bower, K.A., Liu, S., Yang, W., Small, J.E., Herrlinger, U., Ourednik, V., Black, P.M., et al. Neural stem cells display extensive tropism for pathology in adult brain: evidence from intracranial gliomas. Proc. Natl. Acad. Sci. USA 97 (2000), 12846–12851.
2. Adeberg, S., König, L., Bostel, T., Harrabi, S., Welzel, T., Debus, J., Combs, S.E., Glioblastoma recurrence patterns after radiation therapy with regard to the subventricular zone. Int. J. Radiat. Oncol. Biol. Phys. 90 (2014), 886–893.
3. An, J.H., Lee, S.Y., Jeon, J.Y., Cho, K.G., Kim, S.U., Lee, M.A., Identification of gliotropic factors that induce human stem cell migration to malignant tumor. J. Proteome Res. 8 (2009), 2873–2881.
4. Ashburner, M., Ball, C.A., Blake, J.A., Botstein, D., Butler, H., Cherry, J.M., Davis, A.P., Dolinski, K., Dwight, S.S., Eppig, J.T., et al., The Gene Ontology Consortium. Gene ontology: tool for the unification of biology. Nat. Genet. 25 (2000), 25–29.
5. Baker, S.J., Ellison, D.W., Gutmann, D.H., Pediatric gliomas as neurodevelopmental disorders. Glia 64 (2015), 879–895.
6. Beaudoin, G.M.J. 3rd, Lee, S.-H., Singh, D., Yuan, Y., Ng, Y.-G., Reichardt, L.F., Arikkath, J., Culturing pyramidal neurons from the early postnatal mouse hippocampus and cortex. Nat. Protoc. 7 (2012), 1741–1754.
7. Blondet, B., Carpentier, G., Lafdil, F., Courty, J., Pleiotrophin cellular localization in nerve regeneration after peripheral nerve injury. J. Histochem. Cytochem. 53 (2005), 971–977.
8. Brose, K., Bland, K.S., Wang, K.H., Arnott, D., Henzel, W., Goodman, C.S., Tessier-Lavigne, M., Kidd, T., Slit proteins bind Robo receptors and have an evolutionarily conserved role in repulsive axon guidance. Cell 96 (1999), 795–806.
9. Caretti, V., Bugiani, M., Freret, M., Schellen, P., Jansen, M., van Vuurden, D., Kaspers, G., Fisher, P.G., Hulleman, E., Wesseling, P., et al. Subventricular spread of diffuse intrinsic pontine glioma. Acta Neuropathol. 128 (2014), 605–607.
10. Chaichana, K.L., McGirt, M.J., Frazier, J., Attenello, F., Guerrero-Cazares, H., Quinones-Hinojosa, A., Relationship of glioblastoma multiforme to the lateral ventricles predicts survival following tumor resection. J. Neurooncol. 89 (2008), 219–224.
11. Chen, L., Guerrero-Cazares, H., Ye, X., Ford, E., McNutt, T., Kleinberg, L., Lim, M., Chaichana, K., Quinones-Hinojosa, A., Redmond, K., Increased subventricular zone radiation dose correlates with survival in glioblastoma patients after gross total resection. Int. J. Radiat. Oncol. Biol. Phys. 86 (2013), 616–622.
12. Chen, L., Chaichana, K.L., Kleinberg, L., Ye, X., Quinones-Hinojosa, A., Redmond, K., Glioblastoma recurrence patterns near neural stem cell regions. Radiother. Oncol. 116 (2015), 294–300.
13. Czubayko, F., Schulte, A.M., Berchem, G.J., Wellstein, A., Melanoma angiogenesis and metastasis modulated by ribozyme targeting of the secreted growth factor pleiotrophin. Proc. Natl. Acad. Sci. USA 93 (1996), 14753–14758.
14. Donaldson, S.S., Laningham, F., Fisher, P.G., Advances toward an understanding of brainstem gliomas. J Clin Oncol. 24 (2006), 1266–1272.
15. Egorin, M.J., Zuhowski, E.G., Rosen, D.M., Sentz, D.L., Covey, J.M., Eiseman, J.L., Plasma pharmacokinetics and tissue distribution of 17-(allylamino)-17-demethoxygeldanamycin (NSC 330507) in CD2F1 mice1. Cancer Chemother. Pharmacol. 47 (2001), 291–302.
16. Ehtesham, M., Yuan, X., Kabos, P., Chung, N.H., Liu, G., Akasaki, Y., Black, K.L., Yu, J.S., Glioma tropic neural stem cells consist of astrocytic precursors and their migratory capacity is mediated by CXCR4. Neoplasia 6 (2004), 287–293.
17. Evers, P., Lee, P.P., DeMarco, J., Agazaryan, N., Sayre, J.W., Selch, M., Pajonk, F., Irradiation of the potential cancer stem cell niches in the adult brain improves progression-free survival of patients with malignant glioma. BMC Cancer, 10, 2010, 384.
18. Furuta, M., Shiraishi, T., Okamoto, H., Mineta, T., Tabuchi, K., Shiwa, M., Identification of pleiotrophin in conditioned medium secreted from neural stem cells by SELDI-TOF and SELDI-tandem mass spectrometry. Brain Res. Dev. Brain Res. 152 (2004), 189–197.
19. González-Castillo, C., Ortuño-Sahagún, D., Guzmán-Brambila, C., Pallàs, M., Rojas-Mayorquín, A.E., Pleiotrophin as a central nervous system neuromodulator, evidences from the hippocampus. Front. Cell. Neurosci., 8, 2015, 443.
20. Grasso, C.S., Tang, Y., Truffaux, N., Berlow, N.E., Liu, L., Debily, M.-A., Quist, M.J., Davis, L.E., Huang, E.C., Woo, P.J., et al. Functionally defined therapeutic targets in diffuse intrinsic pontine glioma. Nat. Med. 21 (2015), 555–559.
21. Harroch, S., Furtado, G.C., Brueck, W., Rosenbluth, J., Lafaille, J., Chao, M., Buxbaum, J.D., Schlessinger, J., A critical role for the protein tyrosine phosphatase receptor type Z in functional recovery from demyelinating lesions. Nat. Genet. 32 (2002), 411–414.
22. Hienola, A., Pekkanen, M., Raulo, E., Vanttola, P., Rauvala, H., HB-GAM inhibits proliferation and enhances differentiation of neural stem cells. Mol. Cell. Neurosci. 26 (2004), 75–88.
23. Imitola, J., Raddassi, K., Park, K.I., Mueller, F.-J.F.-J., Nieto, M., Teng, Y.D., Frenkel, D., Li, J., Sidman, R.L., Walsh, C.A., et al. Directed migration of neural stem cells to sites of CNS injury by the stromal cell-derived factor 1alpha/CXC chemokine receptor 4 pathway. Proc. Natl. Acad. Sci. USA 101 (2004), 18117–18122.
24. Jafri, N.F., Clarke, J.L., Weinberg, V., Barani, I.J., Cha, S., Relationship of glioblastoma multiforme to the subventricular zone is associated with survival. Neuro-oncol. 15 (2013), 91–96.
25. Kidd, T., Bland, K.S., Goodman, C.S., Slit is the midline repellent for the robo receptor in Drosophila. Cell 96 (1999), 785–794.
26. Kim, D., Pertea, G., Trapnell, C., Pimentel, H., Kelley, R., Salzberg, S.L., TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol., 14, 2013, R36.
27. Kinnunen, A., Niemi, M., Kinnunen, T., Kaksonen, M., Nolo, R., Rauvala, H., Heparan sulphate and HB-GAM (heparin-binding growth-associated molecule) in the development of the thalamocortical pathway of rat brain. Eur. J. Neurosci. 11 (1999), 491–502.
28. Krellman, J.W., Ruiz, H.H., Marciano, V.A., Mondrow, B., Croll, S.D., Behavioral and neuroanatomical abnormalities in pleiotrophin knockout mice. PLoS ONE, 9, 2014, e100597.
29. Lane, T.F., Sage, E.H., The biology of SPARC, a protein that modulates cell-matrix interactions. FASEB J. 8 (1994), 163–173.
30. Lauri, S.E., Rauvala, H., Kaila, K., Taira, T., Effect of heparin-binding growth-associated molecule (HB-GAM) on synaptic transmission and early LTP in rat hippocampal slices. Eur. J. Neurosci. 10 (1998), 188–194.
31. Lee, C., Hu, J., Ralls, S., Kitamura, T., Loh, Y.P., Yang, Y., Mukouyama, Y.S., Ahn, S., et al. The molecular profiles of neural stem cell niche in the adult subventricular zone. PLoS ONE, 7, 2012, e50501.
32. Lee, P., Eppinga, W., Lagerwaard, F., Cloughesy, T., Slotman, B., Nghiemphu, P.L., Wang, P.-C., Kupelian, P., Agazaryan, N., Demarco, J., et al. Evaluation of high ipsilateral subventricular zone radiation therapy dose in glioblastoma: a pooled analysis. Int. J. Radiat. Oncol. Biol. Phys. 86 (2013), 609–615.
33. Li, X., Lee, A.Y.W., Semaphorin 5A and plexin-B3 inhibit human glioma cell motility through RhoGDIalpha-mediated inactivation of Rac1 GTPase. J. Biol. Chem. 285 (2010), 32436–32445.
34. Li, Y.S., Milner, P.G., Chauhan, A.K., Watson, M.A., Hoffman, R.M., Kodner, C.M., Milbrandt, J., Deuel, T.F., Cloning and expression of a developmentally regulated protein that induces mitogenic and neurite outgrowth activity. Science 250 (1990), 1690–1694.
35. Li, S., Gao, Y., Tokuyama, T., Yamamoto, J., Yokota, N., Yamamoto, S., Terakawa, S., Kitagawa, M., Namba, H., Genetically engineered neural stem cells migrate and suppress glioma cell growth at distant intracranial sites. Cancer Lett. 251 (2007), 220–227.
36. Liao, Y., Smyth, G.K., Shi, W., featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30 (2014), 923–930.
37. Lin, G.L., Monje, M., A protocol for rapid post-mortem cell culture of diffuse intrinsic pontine glioma (DIPG). J. Vis. Exp., 2017, 10.3791/55360.
38. Lin, C.-C., Chen, J.-T., Yang, J.-S., Lu, H.-F., Hsu, S.-C., Tan, T.-W., Lin, Y.-T., Ma, Y.-S., Ip, S.-W., Wu, J.-J., et al. Danthron inhibits the migration and invasion of human brain glioblastoma multiforme cells through the inhibition of mRNA expression of focal adhesion kinase, Rho kinases-1 and metalloproteinase-9. Oncol. Rep. 22 (2009), 1033–1037.
39. Louis, D.N., Perry, A., Reifenberger, G., von Deimling, A., Figarella-Branger, D., Cavenee, W.K., Ohgaki, H., Wiestler, O.D., Kleihues, P., Ellison, D.W., The 2016 World Health Organization Classification of Tumors of the Central Nervous System: a summary. Acta Neuropathol. 131 (2016), 803–820.
40. Love, M.I., Huber, W., Anders, S., Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol., 15, 2014, 550.
41. Lu, K.V., Jong, K.A., Kim, G.Y., Singh, J., Dia, E.Q., Yoshimoto, K., Wang, M.Y., Cloughesy, T.F., Nelson, S.F., Mischel, P.S., Differential induction of glioblastoma migration and growth by two forms of pleiotrophin. J. Biol. Chem. 280 (2005), 26953–26964.
42. Maeda, N., Noda, M., Involvement of receptor-like protein tyrosine phosphatase zeta/RPTPbeta and its ligand pleiotrophin/heparin-binding growth-associated molecule (HB-GAM) in neuronal migration. J Cell Biol. 142 (1998), 203–216.
43. Maekawa, M., Ishizaki, T., Boku, S., Watanabe, N., Fujita, A., Iwamatsu, A., Obinata, T., Ohashi, K., Mizuno, K., Narumiya, S., Signaling from Rho to the actin cytoskeleton through protein kinases ROCK and LIM-kinase. Science 285 (1999), 895–898.
44. McClain, C.R., Sim, F.J., Goldman, S.A., Pleiotrophin suppression of receptor protein tyrosine phosphatase-β/ζ maintains the self-renewal competence of fetal human oligodendrocyte progenitor cells. J. Neurosci. 32 (2012), 15066–15075.
45. Mertsch, S., Schmitz, N., Jeibmann, A., Geng, J.-G., Paulus, W., Senner, V., Slit2 involvement in glioma cell migration is mediated by Robo1 receptor. J. Neurooncol. 87 (2008), 1–7.
46. Mi, R., Chen, W., Höke, A., Pleiotrophin is a neurotrophic factor for spinal motor neurons. Proc. Natl. Acad. Sci. USA 104 (2007), 4664–4669.
47. Mistry, A.M., Hale, A.T., Chambless, L.B., Weaver, K.D., Thompson, R.C., Ihrie, R.A., Influence of glioblastoma contact with the lateral ventricle on survival: a meta-analysis. J. Neurooncol. 131 (2017), 125–133.
48. Mistry, A.M., Dewan, M.C., White-Dzuro, G.A., Brinson, P.R., Weaver, K.D., Thompson, R.C., Ihrie, R.A., Chambless, L.B., Decreased survival in glioblastomas is specific to contact with the ventricular-subventricular zone, not subgranular zone or corpus callosum. J. Neurooncol. 132 (2017), 341–349.
49. Mitchison, T.J., Cramer, L.P., Actin-based cell motility and cell locomotion. Cell 84 (1996), 371–379.
50. Monje, M., Mitra, S.S., Freret, M.E., Raveh, T.B., Kim, J., Masek, M., Attema, J.L., Li, G., Haddix, T., Edwards, M.S.B., et al. Hedgehog-responsive candidate cell of origin for diffuse intrinsic pontine glioma. Proc. Natl. Acad. Sci. USA 108 (2011), 4453–4458.
51. Müller, S., Kunkel, P., Lamszus, K., Ulbricht, U., Lorente, G.A., Nelson, A.M., von Schack, D., Chin, D.J., Lohr, S.C., Westphal, M., Melcher, T., A role for receptor tyrosine phosphatase ζ in glioma cell migration. Oncogene 22 (2003), 6661–6668.
52. Nagaraja, S., Vitanza, N.A., Woo, P.J., Taylor, K.R., Liu, F., Zhang, L., Li, M., Meng, W., Ponnuswami, A., Sun, W., et al. Transcriptional dependencies in diffuse intrinsic pontine glioma. Cancer Cell 31 (2017), 635–652.
53. Nakada, M., Anderson, E.M., Demuth, T., Nakada, S., Reavie, L.B., Drake, K.L., Hoelzinger, D.B., Berens, M.E., The phosphorylation of ephrin-B2 ligand promotes glioma cell migration and invasion. Int. J. Cancer 126 (2010), 1155–1165.
54. Niisato, K., Fujikawa, A., Komai, S., Shintani, T., Watanabe, E., Sakaguchi, G., Katsuura, G., Manabe, T., Noda, M., Age-dependent enhancement of hippocampal long-term potentiation and impairment of spatial learning through the Rho-associated kinase pathway in protein tyrosine phosphatase receptor type Z-deficient mice. J. Neurosci. 25 (2005), 1081–1088.
55. Oellers, P., Schröer, U., Senner, V., Paulus, W., Thanos, S., ROCKs are expressed in brain tumors and are required for glioma-cell migration on myelinated axons. Glia 57 (2009), 499–509.
56. Parri, M., Chiarugi, P., Rac and Rho GTPases in cancer cell motility control. Cell Commun. Signal., 8, 2010, 23.
57. Pavlov, I., Võikar, V., Kaksonen, M., Lauri, S.E., Hienola, A., Taira, T., Rauvala, H., Role of heparin-binding growth-associated molecule (HB-GAM) in hippocampal LTP and spatial learning revealed by studies on overexpressing and knockout mice. Mol. Cell. Neurosci. 20 (2002), 330–342.
58. Rauvala, H., Pihlaskari, R., Isolation and some characteristics of an adhesive factor of brain that enhances neurite outgrowth in central neurons. J. Biol. Chem. 262 (1987), 16625–16635.
59. Rieger, J., Wick, W., Weller, M., Human malignant glioma cells express semaphorins and their receptors, neuropilins and plexins. Glia 42 (2003), 379–389.
60. Salhia, B., Rutten, F., Nakada, M., Beaudry, C., Berens, M., Kwan, A., Rutka, J.T., Inhibition of Rho-kinase affects astrocytoma morphology, motility, and invasion through activation of Rac1. Cancer Res. 65 (2005), 8792–8800.
61. Sanai, N., Tramontin, A.D., Quiñones-Hinojosa, A., Barbaro, N.M., Gupta, N., Kunwar, S., Lawton, M.T., McDermott, M.W., Parsa, A.T., Manuel-García Verdugo, J., et al. Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 427 (2004), 740–744.
62. Shimizu, A., Nakayama, H., Wang, P., König, C., Akino, T., Sandlund, J., Coma, S., Italiano, J.E. Jr., Mammoto, A., Bielenberg, D.R., Klagsbrun, M., Netrin-1 promotes glioblastoma cell invasiveness and angiogenesis by multiple pathways including activation of RhoA, cathepsin B, and cAMP-response element-binding protein. J. Biol. Chem. 288 (2013), 2210–2222.
63. Sikkema, A.H., den Dunnen, W.F.A., Hulleman, E., van Vuurden, D.G., Garcia-Manero, G., Yang, H., Scherpen, F.J.G., Kampen, K.R., Hoving, E.W., Kamps, W.A., et al. EphB2 activity plays a pivotal role in pediatric medulloblastoma cell adhesion and invasion. Neuro-oncol. 14 (2012), 1125–1135.
64. Sim, F.J., Lang, J.K., Waldau, B., Roy, N.S., Schwartz, T.E., Pilcher, W.H., Chandross, K.J., Natesan, S., Merrill, J.E., Goldman, S.A., Complementary patterns of gene expression by human oligodendrocyte progenitors and their environment predict determinants of progenitor maintenance and differentiation. Ann. Neurol. 59 (2006), 763–779.
65. Staflin, K., Zuchner, T., Honeth, G., Darabi, A., Lundberg, C., Identification of proteins involved in neural progenitor cell targeting of gliomas. BMC Cancer, 9, 2009, 206.
66. Sumi, T., Matsumoto, K., Shibuya, A., Nakamura, T., Activation of LIM kinases by myotonic dystrophy kinase-related Cdc42-binding kinase alpha. J. Biol. Chem. 276 (2001), 23092–23096.
67. Tamura, H., Fukada, M., Fujikawa, A., Noda, M., Protein tyrosine phosphatase receptor type Z is involved in hippocampus-dependent memory formation through dephosphorylation at Y1105 on p190 RhoGAP. Neurosci. Lett. 399 (2006), 33–38.
68. Tsirmoula, S., Dimas, K., Hatziapostolou, M., Lamprou, M., Ravazoula, P., Papadimitriou, E., Implications of pleiotrophin in human PC3 prostate cancer cell growth in vivo. Cancer Sci. 103 (2012), 1826–1832.
69. Ulbricht, U., Brockmann, M.A., Aigner, A., Eckerich, C., Müller, S., Fillbrandt, R., Westphal, M., Lamszus, K., Expression and function of the receptor protein tyrosine phosphatase zeta and its ligand pleiotrophin in human astrocytomas. J. Neuropathol. Exp. Neurol. 62 (2003), 1265–1275.
70. Venkatesh, H.S., Johung, T.B., Caretti, V., Noll, A., Tang, Y., Nagaraja, S., Gibson, E.M., Mount, C.W., Polepalli, J., Mitra, S.S., et al. Neuronal activity promotes glioma growth through neuroligin-3 secretion. Cell 161 (2015), 803–816.
71. Walker, T.L., Kempermann, G., One mouse, two cultures: isolation and culture of adult neural stem cells from the two neurogenic zones of individual mice. J. Vis. Exp., 2014, 10.3791/51225.
72. Wellstein, A., Fang, W.J., Khatri, A., Lu, Y., Swain, S.S., Dickson, R.B., Sasse, J., Riegel, A.T., Lippman, M.E., A heparin-binding growth factor secreted from breast cancer cells homologous to a developmentally regulated cytokine. J. Biol. Chem. 267 (1992), 2582–2587.
73. Wiech, H., Buchner, J., Zimmermann, R., Jakob, U., Hsp90 chaperones protein folding in vitro. Nature 358 (1992), 169–170.
74. Wu, H., Barusevicius, A., Babb, J., Klein-Szanto, A., Godwin, A., Elenitsas, R., Gelfand, J.M., Lessin, S., Seykora, J.T., Pleiotrophin expression correlates with melanocytic tumor progression and metastatic potential. J. Cutan. Pathol. 32 (2005), 125–130.
75. Zhang, L., Kundu, S., Feenstra, T., Li, X., Jin, C., Laaniste, L., El Hassan, T.E.A., Ohlin, K.E., Yu, D., Olofsson, T., et al. Pleiotrophin promotes vascular abnormalization in gliomas and correlates with poor survival in patients with astrocytomas. Sci. Signal., 8, 2015, ra125.
76. Zhou, X., Ma, L., Li, J., Gu, J., Shi, Q., Yu, R., Effects of SEMA3G on migration and invasion of glioma cells. Oncol. Rep. 28 (2012), 269–275.