Advertisement

The involvement of heparan sulfate proteoglycans in stem cell differentiation and in malignant glioma

  • Soumi Kundu
  • Anqi Xiong
  • Karin Forsberg-NilssonEmail author
Review
  • 57 Downloads
Part of the following topical collections:
  1. Focus Point on the Physics of Cancer

Abstract.

Heparan sulfate (HS) proteoglycans (HSPG) are major components of the extracellular matrix. They interact with a plethora of macromolecules that are of physiological importance. The pattern of sulfation of the HS chain determines the specificity of these interactions. The enzymes that synthesize and degrade HS are thus key regulators of processes ranging from embryonic development to tissue homeostasis and tumor development. Formation of the nervous system is also critically dependent on appropriate HSPGs as shown by several studies on the role of HS in neural induction from embryonic stem cells. High-grade glioma is the most common primary malignant brain tumor among adults, and the prognosis is poor. Neural and glioma stem cells share several traits, including sustained proliferation and highly efficient migration in the brain. There are also similarities between the neurogenic niche where adult neural stem cells reside and the tumorigenic niche, including their interactions with components of the extracellular matrix (ECM). The levels of many of these components, for example HSPGs and enzymes involved in the biosynthesis and modification of HS are attenuated in gliomas. In this paper, HS regulation of pathways involved in neural differentiation and how these may be of importance for brain development are discussed. The literature suggesting that modifications of HS could regulate glioma growth and invasion is reviewed. Targeting the invasiveness of glioma cells by modulating HS may improve upon present therapeutic options, which only marginally enhance the survival of glioma patients.

Keywords

Glioma Cell Neural Stem Cell Heparan Sulfate Sulfation Embryoid Body 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. 1.
    D.C. Kraushaar, Y. Yamaguchi, L. Wang, J. Biol. Chem. 285, 5907 (2010)CrossRefGoogle Scholar
  2. 2.
    R.J. Holley, C.E. Pickford, G. Rushton, G. Lacaud, J.T. Gallagher, V. Kouskoff, C.L. Merry, J. Biol. Chem. 286, 6241 (2011)CrossRefGoogle Scholar
  3. 3.
    C.E. Pickford, R.J. Holley, G. Rushton, M.P. Stavridis, C.M. Ward, C.L. Merry, Stem Cells 29, 629 (2011)CrossRefGoogle Scholar
  4. 4.
    M. Forsberg, K. Holmborn, S. Kundu, A. Dagalv, L. Kjellen, K. Forsberg-Nilsson, J. Biol. Chem. 287, 10853 (2012)CrossRefGoogle Scholar
  5. 5.
    J. Rong, H. Habuchi, K. Kimata, U. Lindahl, M. Kusche-Gullberg, Biochemistry 40, 5548 (2001)CrossRefGoogle Scholar
  6. 6.
    J.D. Esko, L. Zhang, Curr. Opin. Struct. Biol. 6, 663 (1996)CrossRefGoogle Scholar
  7. 7.
    M. Busse, M. Kusche-Gullberg, J. Biol. Chem. 278, 41333 (2003)CrossRefGoogle Scholar
  8. 8.
    K. Grobe, J. Ledin, M. Ringvall, K. Holmborn, E. Forsberg, J.D. Esko, L. Kjellen, Biochim. Biophys. Acta 1573, 209 (2002)CrossRefGoogle Scholar
  9. 9.
    M. Kusche-Gullberg, L. Kjellen, Curr. Opin. Struct. Biol. 13, 605 (2003)CrossRefGoogle Scholar
  10. 10.
    I. Vlodavsky, Y. Friedmann, J. Clin. Invest. 108, 341 (2001)CrossRefGoogle Scholar
  11. 11.
    X. Shi, J. Zaia, J. Biol. Chem. 284, 11806 (2009)CrossRefGoogle Scholar
  12. 12.
    C.L. Merry, S.L. Bullock, D.C. Swan, A.C. Backen, M. Lyon, R.S. Beddington, V.A. Wilson, J.T. Gallagher, J. Biol. Chem. 276, 35429 (2001)CrossRefGoogle Scholar
  13. 13.
    A.C. Rapraeger, A. Krufka, B.B. Olwin, Science 252, 1705 (1991)ADSCrossRefGoogle Scholar
  14. 14.
    A. Yayon, M. Klagsbrun, J.D. Esko, P. Leder, D.M. Ornitz, Cell 64, 841 (1991)CrossRefGoogle Scholar
  15. 15.
    K. Forsten-Williams, C.C. Chua, M.A. Nugent, J. Theor. Biol. 233, 483 (2005)CrossRefGoogle Scholar
  16. 16.
    R. Ruppert, E. Hoffmann, W. Sebald, Eur. J. Biochem. 237, 295 (1996)CrossRefGoogle Scholar
  17. 17.
    F. Reichsman, L. Smith, S. Cumberledge, J. Cell. Biol. 135, 819 (1996)CrossRefGoogle Scholar
  18. 18.
    I. The, Y. Bellaiche, N. Perrimon, Mol. Cell 4, 633 (1999)CrossRefGoogle Scholar
  19. 19.
    A. Molist, M. Romaris, U. Lindahl, J. Villena, M. Touab, A. Bassols, Eur. J. Biochem. 254, 371 (1998)CrossRefGoogle Scholar
  20. 20.
    G. Fager, G. Camejo, U. Olsson, G. Ostergren-Lunden, G. Bondjers, In Vitro Cell Dev. Biol. 28A, 176 (1992)CrossRefGoogle Scholar
  21. 21.
    A. Abramsson, S. Kurup, M. Busse, S. Yamada, P. Lindblom, E. Schallmeiner, D. Stenzel, D. Sauvaget, J. Ledin, M. Ringvall, U. Landegren, L. Kjellen, G. Bondjers, J.P. Li, U. Lindahl, D. Spillmann, C. Betsholtz, H. Gerhardt, Genes. Dev. 21, 316 (2007)CrossRefGoogle Scholar
  22. 22.
    S. Gengrinovitch, B. Berman, G. David, L. Witte, G. Neufeld, D. Ron, J. Biol. Chem. 274, 10816 (1999)CrossRefGoogle Scholar
  23. 23.
    H.G. Kuhn, J. Winkler, G. Kempermann, L.J. Thal, F.H. Gage, J. Neurosci. 17, 5820 (1997)Google Scholar
  24. 24.
    A. Androutsellis-Theotokis, R.R. Leker, F. Soldner, D.J. Hoeppner, R. Ravin, S.W. Poser, M.A. Rueger, S.K. Bae, R. Kittappa, R.D. McKay, Nature 442, 823 (2006)ADSCrossRefGoogle Scholar
  25. 25.
    Q. Qu, G. Sun, W. Li, S. Yang, P. Ye, C. Zhao, R.T. Yu, F.H. Gage, R.M. Evans, Y. Shi, Nat. Cell Biol. 12, 31 (2010)CrossRefGoogle Scholar
  26. 26.
    D.C. Lie, S.A. Colamarino, H.J. Song, L. Desire, H. Mira, A. Consiglio, E.S. Lein, S. Jessberger, H. Lansford, A.R. Dearie, F.H. Gage, Nature 437, 1370 (2005)ADSCrossRefGoogle Scholar
  27. 27.
    A. Erlandsson, K. Brannvall, S. Gustafsdottir, B. Westermark, K. Forsberg-Nilsson, Cancer Res. 66, 8042 (2006)CrossRefGoogle Scholar
  28. 28.
    R.C. Rao, J. Boyd, R. Padmanabhan, J.G. Chenoweth, R.D. McKay, Stem Cells 27, 116 (2009)CrossRefGoogle Scholar
  29. 29.
    Y.G. Brickman, M.D. Ford, J.T. Gallagher, V. Nurcombe, P.F. Bartlett, J.E. Turnbull, J. Biol. Chem. 273, 4350 (1998)CrossRefGoogle Scholar
  30. 30.
    A.V. Nairn, A. Kinoshita-Toyoda, H. Toyoda, J. Xie, K. Harris, S. Dalton, M. Kulik, J.M. Pierce, T. Toida, K.W. Moremen, R.J. Linhardt, J. Proteome Res. 6, 4374 (2007)CrossRefGoogle Scholar
  31. 31.
    C.E. Johnson, B.E. Crawford, M. Stavridis, G. Ten Dam, A.L. Wat, G. Rushton, C.M. Ward, V. Wilson, T.H. van Kuppevelt, J.D. Esko, A. Smith, J.T. Gallagher, C.L. Merry, Stem Cells 25, 1913 (2007)CrossRefGoogle Scholar
  32. 32.
    T. Izumikawa, N. Kanagawa, Y. Watamoto, M. Okada, M. Saeki, M. Sakano, K. Sugahara, K. Sugihara, M. Asano, H. Kitagawa, J. Biol. Chem. 285, 12190 (2010)CrossRefGoogle Scholar
  33. 33.
    X. Lin, G. Wei, Z. Shi, L. Dryer, J.D. Esko, D.E. Wells, M.M. Matzuk, Dev. Biol. 224, 299 (2000)CrossRefGoogle Scholar
  34. 34.
    M. Ringvall, J. Ledin, K. Holmborn, T. van Kuppevelt, F. Ellin, I. Eriksson, A.M. Olofsson, L. Kjellen, E. Forsberg, J. Biol. Chem. 275, 25926 (2000)CrossRefGoogle Scholar
  35. 35.
    E. Forsberg, G. Pejler, M. Ringvall, C. Lunderius, B. Tomasini-Johansson, M. Kusche-Gullberg, I. Eriksson, J. Ledin, L. Hellman, L. Kjellen, Nature 400, 773 (1999)ADSCrossRefGoogle Scholar
  36. 36.
    G.R. Martin, Proc. Natl. Acad. Sci. U.S.A. 78, 7634 (1981)ADSCrossRefGoogle Scholar
  37. 37.
    J.A. Thomson, J. Itskovitz-Eldor, S.S. Shapiro, M.A. Waknitz, J.J. Swiergiel, V.S. Marshall, J.M. Jones, Science 282, 1145 (1998)ADSCrossRefGoogle Scholar
  38. 38.
    N.M. Gough, R.L. Williams, D.J. Hilton, S. Pease, T.A. Willson, J. Stahl, D.P. Gearing, N.A. Nicola, D. Metcalf, Reprod. Fertil. Dev. 1, 281 (1989)CrossRefGoogle Scholar
  39. 39.
    E.D. Rosen, P. Sarraf, A.E. Troy, G. Bradwin, K. Moore, D.S. Milstone, B.M. Spiegelman, R.M. Mortensen, Mol. Cell 4, 611 (1999)CrossRefGoogle Scholar
  40. 40.
    B.W. Phillips, N. Belmonte, C. Vernochet, G. Ailhaud, C. Dani, Biochem. Biophys. Res. Commun. 284, 478 (2001)CrossRefGoogle Scholar
  41. 41.
    L. Conti, S.M. Pollard, T. Gorba, E. Reitano, M. Toselli, G. Biella, Y. Sun, S. Sanzone, Q.L. Ying, E. Cattaneo, A. Smith, PLoS Biol. 3, e283 (2005)CrossRefGoogle Scholar
  42. 42.
    G. Keller, Genes. Dev. 19, 1129 (2005)CrossRefGoogle Scholar
  43. 43.
    S. Okabe, K. Forsberg-Nilsson, A.C. Spiro, M. Segal, R.D. McKay, Mech. Dev. 59, 89 (1996)CrossRefGoogle Scholar
  44. 44.
    K. Holmborn, J. Ledin, E. Smeds, I. Eriksson, M. Kusche-Gullberg, L. Kjellen, J. Biol. Chem. 279, 42355 (2004)CrossRefGoogle Scholar
  45. 45.
    F. Lanner, K.L. Lee, M. Sohl, K. Holmborn, H. Yang, J. Wilbertz, L. Poellinger, J. Rossant, F. Farnebo, Stem Cells 28, 191 (2010)Google Scholar
  46. 46.
    S. Le Jan, M. Hayashi, Z. Kasza, I. Eriksson, J.R. Bishop, I. Weibrecht, J. Heldin, K. Holmborn, L. Jakobsson, O. Soderberg, D. Spillmann, J.D. Esko, L. Claesson-Welsh, L. Kjellen, J. Kreuger, Arterioscler. Thromb. Vasc. Biol. 32, 1255 (2012)CrossRefGoogle Scholar
  47. 47.
    D. Liu, Z. Shriver, G. Venkataraman, Y. El Shabrawi, R. Sasisekharan, Proc. Natl. Acad. Sci. U.S.A. 99, 568 (2002)ADSCrossRefGoogle Scholar
  48. 48.
    G.A. Schmale, E.U. Conrad 3rd, W.H. Raskind, J. Bone Joint Surg. Am. 76, 986 (1994)Google Scholar
  49. 49.
    S. Ropero, F. Setien, J. Espada, M.F. Fraga, M. Herranz, J. Asp, M.S. Benassi, A. Franchi, A. Patino, L.S. Ward, J. Bovee, J.C. Cigudosa, W. Wim, M. Esteller, Hum. Mol. Genet. 13, 2753 (2004)CrossRefGoogle Scholar
  50. 50.
    Z. Piao, H. Kim, B.K. Jeon, W.J. Lee, C. Park, Cancer 80, 865 (1997)CrossRefGoogle Scholar
  51. 51.
    A. Yoneda, M.E. Lendorf, J.R. Couchman, H.A. Multhaupt, J. Histochem. Cytochem. 60, 9 (2012)CrossRefGoogle Scholar
  52. 52.
    C. Bret, D. Hose, T. Reme, A.C. Sprynski, K. Mahtouk, J.F. Schved, P. Quittet, J.F. Rossi, H. Goldschmidt, B. Klein, Br. J. Haematol. 145, 350 (2009)CrossRefGoogle Scholar
  53. 53.
    W.C. Lamanna, M.A. Frese, M. Balleininger, T. Dierks, J. Biol. Chem. 283, 27724 (2008)CrossRefGoogle Scholar
  54. 54.
    K. Uchimura, M. Morimoto-Tomita, A. Bistrup, J. Li, M. Lyon, J. Gallagher, Z. Werb, S.D. Rosen, BMC Biochem. 7, 2 (2006)CrossRefGoogle Scholar
  55. 55.
    H. Lemjabbar-Alaoui, A. van Zante, M.S. Singer, Q. Xue, Y.Q. Wang, D. Tsay, B. He, D.M. Jablons, S.D. Rosen, Oncogene 29, 635 (2010)CrossRefGoogle Scholar
  56. 56.
    M. Morimoto-Tomita, K. Uchimura, A. Bistrup, D.H. Lum, M. Egeblad, N. Boudreau, Z. Werb, S.D. Rosen, Neoplasia 7, 1001 (2005)CrossRefGoogle Scholar
  57. 57.
    I. Vlodavsky, P. Beckhove, I. Lerner, C. Pisano, A. Meirovitz, N. Ilan, M. Elkin, Cancer Microenviron. 5, 115 (2012)CrossRefGoogle Scholar
  58. 58.
    D.N. Louis, H. Ohgaki, O.D. Wiestler, W.K. Cavenee, P.C. Burger, A. Jouvet, B.W. Scheithauer, P. Kleihues, Acta Neuropathol. 114, 97 (2007)CrossRefGoogle Scholar
  59. 59.
    R. Stupp, W.P. Mason, M.J. van den Bent, M. Weller, B. Fisher, M.J. Taphoorn, K. Belanger, A.A. Brandes, C. Marosi, U. Bogdahn, J. Curschmann, R.C. Janzer, S.K. Ludwin, T. Gorlia, A. Allgeier, D. Lacombe, J.G. Cairncross, E. Eisenhauer, R.O. Mirimanoff, N. Engl. J. Med. 352, 987 (2005)CrossRefGoogle Scholar
  60. 60.
    R.G. Verhaak, K.A. Hoadley, E. Purdom, V. Wang, Y. Qi, M.D. Wilkerson, C.R. Miller, L. Ding, T. Golub, J.P. Mesirov, G. Alexe, M. Lawrence, M. O'Kelly, P. Tamayo, B.A. Weir, S. Gabriel, W. Winckler, S. Gupta, L. Jakkula, H.S. Feiler, J.G. Hodgson, C.D. James, J.N. Sarkaria, C. Brennan, A. Kahn, P.T. Spellman, R.K. Wilson, T.P. Speed, J.W. Gray, M. Meyerson, G. Getz, C.M. Perou, D.N. Hayes, Cancer Cell 17, 98 (2010)CrossRefGoogle Scholar
  61. 61.
    D. Sturm, H. Witt, V. Hovestadt, D.A. Khuong-Quang, D.T. Jones, C. Konermann, E. Pfaff, M. Tonjes, M. Sill, S. Bender, M. Kool, M. Zapatka, N. Becker, M. Zucknick, T. Hielscher, X.Y. Liu, A.M. Fontebasso, M. Ryzhova, S. Albrecht, K. Jacob, M. Wolter, M. Ebinger, M.U. Schuhmann, T. van Meter, M.C. Fruhwald, H. Hauch, A. Pekrun, B. Radlwimmer, T. Niehues, G. von Komorowski, M. Durken, A.E. Kulozik, J. Madden, A. Donson, N.K. Foreman, R. Drissi, M. Fouladi, W. Scheurlen, A. von Deimling, C. Monoranu, W. Roggendorf, C. Herold-Mende, A. Unterberg, C.M. Kramm, J. Felsberg, C. Hartmann, B. Wiestler, W. Wick, T. Milde, O. Witt, A.M. Lindroth, J. Schwartzentruber, D. Faury, A. Fleming, M. Zakrzewska, P.P. Liberski, K. Zakrzewski, P. Hauser, M. Garami, A. Klekner, L. Bognar, S. Morrissy, F. Cavalli, M.D. Taylor, P. van Sluis, J. Koster, R. Versteeg, R. Volckmann, T. Mikkelsen, K. Aldape, G. Reifenberger, V.P. Collins, J. Majewski, A. Korshunov, P. Lichter, C. Plass, N. Jabado, S.M. Pfister, Cancer Cell 22, 425 (2012)CrossRefGoogle Scholar
  62. 62.
    B.E. Johnson, T. Mazor, C. Hong, M. Barnes, K. Aihara, C.Y. McLean, S.D. Fouse, S. Yamamoto, H. Ueda, K. Tatsuno, S. Asthana, L.E. Jalbert, S.J. Nelson, A.W. Bollen, W.C. Gustafson, E. Charron, W.A. Weiss, I.V. Smirnov, J.S. Song, A.B. Olshen, S. Cha, Y. Zhao, R.A. Moore, A.J. Mungall, S.J. Jones, M. Hirst, M.A. Marra, N. Saito, H. Aburatani, A. Mukasa, M.S. Berger, S.M. Chang, B.S. Taylor, J.F. Costello, Science 343, 189 (2014)ADSCrossRefGoogle Scholar
  63. 63.
    F. Mercier, J.T. Kitasako, G.I. Hatton, J. Comp. Neurol. 451, 170 (2002)CrossRefGoogle Scholar
  64. 64.
    A. Kerever, F. Mercier, R. Nonaka, S. de Vega, Y. Oda, B. Zalc, Y. Okada, N. Hattori, Y. Yamada, E. Arikawa-Hirasawa, Stem Cell Res. 12, 492 (2014)CrossRefGoogle Scholar
  65. 65.
    T. Bergstrom, K. Holmqvist, T. Tararuk, S. Johansson, K. Forsberg-Nilsson, Biochim. Biophys. Acta 1840, 2526 (2014)CrossRefGoogle Scholar
  66. 66.
    T. Mammoto, A. Jiang, E. Jiang, D. Panigrahy, M.W. Kieran, A. Mammoto, Am. J. Pathol. 183, 1293 (2013)CrossRefGoogle Scholar
  67. 67.
    C. Calabrese, H. Poppleton, M. Kocak, T.L. Hogg, C. Fuller, B. Hamner, E.Y. Oh, M.W. Gaber, D. Finklestein, M. Allen, A. Frank, I.T. Bayazitov, S.S. Zakharenko, A. Gajjar, A. Davidoff, R.J. Gilbertson, Cancer Cell 11, 69 (2007)CrossRefGoogle Scholar
  68. 68.
    P.A. Steck, R.P. Moser, J.M. Bruner, L. Liang, A.N. Freidman, T.L. Hwang, W.K. Yung, Cancer Res. 49, 2096 (1989)Google Scholar
  69. 69.
    A. Bertolotto, M.L. Magrassi, L. Orsi, C. Sitia, D. Schiffer, J. Neurooncol. 4, 43 (1986)CrossRefGoogle Scholar
  70. 70.
    G. Su, K. Meyer, C.D. Nandini, D. Qiao, S. Salamat, A. Friedl, Am. J. Pathol. 168, 2014 (2006)CrossRefGoogle Scholar
  71. 71.
    A. Watanabe, T. Mabuchi, E. Satoh, K. Furuya, L. Zhang, S. Maeda, H. Naganuma, J. Neurooncol. 77, 25 (2006)CrossRefGoogle Scholar
  72. 72.
    Y. Xu, J. Yuan, Z. Zhang, L. Lin, S. Xu, Mol. Biol. Rep. 39, 8979 (2012)CrossRefGoogle Scholar
  73. 73.
    J.J. Phillips, Oncotarget 3, 568 (2012)CrossRefGoogle Scholar
  74. 74.
    T. Reme, J.P. Hugnot, I. Bieche, V. Rigau, F. Burel-Vandenbos, V. Prevot, M. Baroncini, D. Fontaine, H. Chevassus, S. Vacher, R. Lidereau, H. Duffau, L. Bauchet, D. Joubert, PLoS One 8, e66574 (2013)ADSCrossRefGoogle Scholar
  75. 75.
    A. Wade, A.E. Robinson, J.R. Engler, C. Petritsch, C.D. James, J.J. Phillips, FEBS J. 280, 2399 (2013)CrossRefGoogle Scholar
  76. 76.
    A. Zetser, Y. Bashenko, H.Q. Miao, I. Vlodavsky, N. Ilan, Cancer Res. 63, 7733 (2003)Google Scholar
  77. 77.
    Y. Ueno, M. Yamamoto, I. Vlodavsky, I. Pecker, K. Ohshima, T. Fukushima, J. Neurosurg. 102, 513 (2005)CrossRefGoogle Scholar
  78. 78.
    X. Hong, K.K. Nelson, A.C. deCarvalho, S.N. Kalkanis, J. Neurosurg. 113, 261 (2010)CrossRefGoogle Scholar
  79. 79.
    X. Hong, F. Jiang, S.N. Kalkanis, Z.G. Zhang, X. Zhang, X. Zheng, H. Jiang, T. Mikkelsen, M. Chopp, J. Exp. Clin. Cancer Res. 27, 23 (2008)CrossRefGoogle Scholar
  80. 80.
    F.K. Johansson, J. Brodd, C. Eklof, M. Ferletta, G. Hesselager, C.F. Tiger, L. Uhrbom, B. Westermark, Proc. Natl. Acad. Sci. U.S.A. 101, 11334 (2004)ADSCrossRefGoogle Scholar
  81. 81.
    J.J. Phillips, E. Huillard, A.E. Robinson, A. Ward, D.H. Lum, M.Y. Polley, S.D. Rosen, D.H. Rowitch, Z. Werb, J. Clin. Invest. 122, 911 (2012)CrossRefGoogle Scholar
  82. 82.
    Y. Liang, M. Haring, P.J. Roughley, R.K. Margolis, R.U. Margolis, J. Cell. Biol. 139, 851 (1997)CrossRefGoogle Scholar
  83. 83.
    D. Qiao, K. Meyer, C. Mundhenke, S.A. Drew, A. Friedl, J. Biol. Chem. 278, 16045 (2003)CrossRefGoogle Scholar
  84. 84.
    R.V. Iozzo, R.D. Sanderson, J. Cell Mol. Med. 15, 1013 (2011)CrossRefGoogle Scholar
  85. 85.
    C.Y. Fears, C.L. Gladson, A. Woods, J. Biol. Chem. 281, 14533 (2006)CrossRefGoogle Scholar
  86. 86.
    H. Zhu, R.L. Carpenter, W. Han, H.W. Lo, Cancer Lett. 343, 51 (2014)CrossRefGoogle Scholar
  87. 87.
    G. Rascher, A. Fischmann, S. Kroger, F. Duffner, E.H. Grote, H. Wolburg, Acta Neuropathol. 104, 85 (2002)CrossRefGoogle Scholar
  88. 88.
    A. Warth, S. Kroger, H. Wolburg, Acta Neuropathol. 107, 311 (2004)CrossRefGoogle Scholar
  89. 89.
    M.C. Chamberlain, J. Neurooncol. 101, 319 (2011)CrossRefGoogle Scholar
  90. 90.
    M.D. Groves, V.K. Puduvalli, K.R. Hess, K.A. Jaeckle, P. Peterson, W.K. Yung, V.A. Levin, J. Clin. Oncol. 20, 1383 (2002)CrossRefGoogle Scholar
  91. 91.
    T.A. Ulrich, E.M. de Juan Pardo, S. Kumar, Cancer Res. 69, 4167 (2009)CrossRefGoogle Scholar
  92. 92.
    B. Radotra, D. McCormick, J. Pathol. 181, 434 (1997)CrossRefGoogle Scholar
  93. 93.
    Y. Akiyama, S. Jung, B. Salhia, S. Lee, S. Hubbard, M. Taylor, T. Mainprize, K. Akaishi, W. van Furth, J.T. Rutka, J. Neurooncol. 53, 115 (2001)CrossRefGoogle Scholar
  94. 94.
    H. Naganuma, E. Satoh, T. Asahara, K. Amagasaki, A. Watanabe, H. Satoh, K. Kuroda, L. Zhang, H. Nukui, J. Neurooncol. 70, 309 (2004)CrossRefGoogle Scholar
  95. 95.
    H.C. Christianson, K.J. Svensson, T.H. van Kuppevelt, J.P. Li, M. Belting, Proc. Natl. Acad. Sci. U.S.A. 110, 17380 (2013)ADSCrossRefGoogle Scholar
  96. 96.
    C.A. Thompson, A. Purushothaman, V.C. Ramani, I. Vlodavsky, R.D. Sanderson, J. Biol. Chem. 288, 10093 (2013)CrossRefGoogle Scholar

Copyright information

© Società Italiana di Fisica and Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Soumi Kundu
    • 1
  • Anqi Xiong
    • 1
  • Karin Forsberg-Nilsson
    • 1
    Email author
  1. 1.Department of Immunology, Genetics and Pathology, and Science for Life Laboratory, Rudbeck LaboratoryUppsala UniversityUppsalaSweden

Personalised recommendations