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Human Brain Tumor Growth: Role of Aquaporins

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Part of the book series: Tumors of the Central Nervous System ((TCNS,volume 12))

Abstract

The aquaporins (AQPs) are a family of transmembrane water channel proteins widely distributed and play a major role in transcellular and transepithelial water movement. Moreover, recent evidence indicates that AQPs may be involved in cell migration and angiogenesis. This review article summarizes literature data concerning the involvement of AQPs in human brain tumor growth, angiogenesis and metastatic process and suggests a potential therapeutic approach by antagonizing their biological activity.

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References

  • Auguste KI, Jin S, Uchida K, Yan D, Manley GT, Papadopoulos MC, Verkman AS (2007) Greatly impaired migration of implanted aquaporin-4-deficient astroglial cells in mouse brain toward a site of injury. FASEB J 21:108–116

    Article  CAS  PubMed  Google Scholar 

  • Badaut J, Lasbennes F, Magistretti PJ, Regli L (2002) Aquaporins in brain: distribution, physiology and pathophysiology. J Cereb Blood Flow Metab 22:367–378

    Article  CAS  PubMed  Google Scholar 

  • Badaut S, Ashwal S, Adami A, Tone B, Recker R, Spagnoli D, Ternon B, Obenaus A (2011) Brain water motility decreases after astrocytic aquaporin-4 inhibition using RNA interference. J Cereb Blood Flow Metab 31:819–831

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Craven SE, Bredt DS (1998) PDZ proteins organize synaptic signaling pathways. Cell 93:495–498

    Article  CAS  PubMed  Google Scholar 

  • Ding T, Ma Y, Liu W, Ying G, Fu L, Gu F (2011) Role of aquaporin-4 in the regulation of migration and invasion of human glioma cells. Int J Oncol 38:1521–1531

    CAS  PubMed  Google Scholar 

  • Gu YT, Zhang H, Xue YX (2007) Dexamethasone treatment modulates aquaporin-4 expression after intracerebral hemorrhage in rats. Neurosci Lett 413:126–131

    Article  CAS  PubMed  Google Scholar 

  • Hasegawa H, Ma T, Skach W, Matthay MA, Verkman AS (1994) Molecular cloning of a mercurial-insensitive water channel expressed in selected water-transporting tissues. J Biol Chem 269:5497–5500

    CAS  PubMed  Google Scholar 

  • Heiss JD, Papavassiliou E, Merrill MJ, Nieman L, Knightly JJ, Walbridge S, Edwards NA, Oldfield EH (1996) Mechanisms of dexamethasone suppression of brain tumor-associated vascular permeability in rats. Involvement of the glucocorticoid receptor and vascular permeability factor. J Clin Invest 98:1400–1408

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hoque MO, Soria JC, Woo J, Lee T, Lee J, Jang SJ, Upadhyay S, Trink B, Monitto C, Desmaze C, Mao L, Sidransky D, Moon C (2006) Aquaporin is overexpressed in lung cancer and stimulates NIH-3T3 cell proliferation anchorage-independent growth. Am J Pathol 168:1345–1353

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hu J, Verkman AS (2006) Increased migration and metastatic potential of tumor cells expressing aquaporin water channels. FASEB J 20:1892–1894

    Article  CAS  PubMed  Google Scholar 

  • Jiang Y (2009) Aquaporin-1 activity of plasma membrane affects HT20 colon cancer migration. IUBMB Life 61:1001–1009

    Article  CAS  PubMed  Google Scholar 

  • Manley GT, Fujimura M, Ma T, Noshita N, Filiz F, Bollen AW, Cahn P, Verkman AS (2000) Aquaporin-4 deletion in mice reduces brain edema after acute water intoxication and ischemic stroke. Nat Med 6:159–163

    Article  CAS  PubMed  Google Scholar 

  • Marmarou A (2007) A review of progress in understanding the pathophysiology and treatment of brain edema. Neurosurg Focus 22:E1

    Google Scholar 

  • Monzani E, Shtil AA, La Porta CA (2007) The water channels, new drug gable targets to combat cancer cell survival, invasiveness and metastasis. Curr Drug Targets 8:1132–1137

    Article  CAS  PubMed  Google Scholar 

  • Monzani E, Bazzotti R, Perego C, La Porta CA (2009) AQP1 is not only a water channel: it contributes to cell migration through Lin7/beta-catenin. PLoS One 4:6167

    Article  Google Scholar 

  • Mou K, Chen M, Mao Q, Wang P, Ni R, Xia X, Liu Y (2010) AQP-4 in peritumoral edematous tissue is correlated with the degree of glioma and expression of VEGF and HIF-alpha. J Neurooncol 100:375–383

    Article  CAS  PubMed  Google Scholar 

  • Nagelhus EA, Horio Y, Inanobe A, Fujita A, Haug FM, Nielsen S, Kurachi Y, Ottersen OP (1999) Immunogold evidence suggests that coupling of K+ siphoning and water transport in rat retinal Müller cells is mediated by a co enrichment of Kir4.1 and AQP4 in specific membrane domain. Glia 26:147–154

    Article  Google Scholar 

  • Nicchia GP, Srinivas M, Li W, Brosnan CF, Frigeri A, Spray DC (2005) New possible roles for aquaporin-4 in astrocytes: cell cytoskeleton and functional relationship with connexin 43. FASEB J 19:1674–1676

    CAS  PubMed  Google Scholar 

  • Nico B, Mangieri D, Tamma R, Longo V, Annese T, Crivellato E, Pollo B, Maderna E, Ribatti D, Salmaggi A (2009) Aquaporin-4 contributes to the resolution of peritumoral brain oedema in human glioblastoma multiforme after combined chemotherapy and radiotherapy. Eur J Cancer 45:3315–3325

    Article  CAS  PubMed  Google Scholar 

  • Nico B, Tamma R, Annese T, Mangieri D, De Luca A, Corsi P, Benagiano V, Longo V, Crivellato E, Salmaggi A, Ribatti D (2010) Glial dystrophin-associated proteins, laminin and agrin, are downregulated in the brain of mdx mouse. Lab Invest 90:1645–1660

    Article  CAS  PubMed  Google Scholar 

  • Nielsen S, Nagelhus EA, Amiry-Moghaddam M, Bourque C, Agre P, Ottersen OP (1997) Specialized membrane domains for water transport in glial cells: high resolution immunogold cytochemistry of aquaporin-4 in rat brain. J Neurosci 17:171–180

    CAS  PubMed  Google Scholar 

  • Noël S, Wolburg-Buchholz K, Mach AF, Ritz R, Tatagiba M, Beschorner R, Wolburg H, Falleir-Becker P (2012) Dynamic of expression patterns of AQP4, dystroglycan, agrin and matrix metalloproteinases in human glioblastomas. Cell Tissue Res [Epub ahead of print] 347:429–441

    Google Scholar 

  • Oshio K, Binder DK, Liang Y, Bollen A, Feuerstein B, Berger MS, Manley GT (2005) Expression of the aquaporin-1 water channel in human glial tumors. Neurosurgery 56:375–381

    Article  PubMed  Google Scholar 

  • Papadopoulos MC, Saadoun S, Binder DK, Manley GT, Krishna S, Verkman AS (2004a) Molecular mechanism of brain tumor edema. Neuroscience 129:1011–1020

    Article  CAS  PubMed  Google Scholar 

  • Papadopoulos MC, Manley GT, Krishna S, Verkman AS (2004b) Aquaporin-4 facilitates reabsorption of excess fluid in vasogenic brain edema, FASEB J 18:1291–1293

    Google Scholar 

  • Papadopoulos MC, Verkman AS (2007) Aquaporin-4 and brain edema. Pediatr Nephrol 22:778–784

    Article  PubMed  Google Scholar 

  • Papadopoulos MC, Saadoun S, Verkman AS (2008) Aquaporin and cell migration. Pflugers Arch 456:693–700

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Saadoun S, Papadopoulos MC, Davies DC, Krishna S, Bell BA (2002a) Aquaporin-4 expression is increased in edematous human brain tumours. J Neurol Neurosurg Pscychiatry 72:262–265

    Article  CAS  Google Scholar 

  • Saadoun S, Papadopoulos MC, Davies DC, Bell BA, Krishna S (2002b) Increased aquaporin 1 water channel expression in human brain tumors. Br J Cancer 87:621–623

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Saadoun S, Papadoulos MC, Hara-Chikuma M, Verkman AS (2005a) Impairment of angiogenesis and cell migration by targeted aquaporin-1 gene disruption. Nature 434:786–792

    Article  CAS  PubMed  Google Scholar 

  • Saadoun S, Papadopoulos MC, Watanabe H, Yan D, Manley GT, Verkman AS (2005b) Involvement of aquaporin-4 in astroglial cell migration and glial scar formation. J Cell Sci 118:5691–5698

    Article  CAS  PubMed  Google Scholar 

  • Saadoun S, Papadopoulos MC (2010) Aquaporin-4 in brain and spinal cord oedema. Neuroscience 168:1036–1104

    Article  CAS  PubMed  Google Scholar 

  • Schneider SW, Ludwig T, Tatenhorst L, Braune S, Oberleithner H, Senner V, Paulus W (2004) Glioblastoma cells release factors that disrupt blood–brain barrier features. Acta Neuropathol 107:272–276

    Article  PubMed  Google Scholar 

  • Verkman AS (2005) More than just water channels: unexepected cellular roles of aquaporins. J Cell Sci 118:3225–3232

    Article  CAS  PubMed  Google Scholar 

  • Verkman AS, Hara-Chikuma M, Papadopoulos MC (2008) Aquaporins-new players in cancer biology. J Mol Med 86:523–529

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhou D, Jiang X, Xu R, Cai Y, Hu J, Xu G, Zou Y, Zeng Y (2008) Assessing the cytoskeleton system and its elements in C6 glioma cells and astrocytes by atomic force microscopy. Cell Mol Neurobiol 28:895–905

    Article  PubMed  Google Scholar 

  • Warth A, Mittelbronn M, Wolburg H (2005) Redistribution of the water channel protein aquaporin-4 and the K+ channel protein Kir 4.1 differ in low- and high-grade human brain tumors. Acta Neuropathol 109:418–426

    Article  CAS  PubMed  Google Scholar 

  • Warth A, Simon P, Capper D, Goeppert B, Tabatabai G, Herzog H, Dietz K, Stubenvoll F, Ajaaj R, Becker R, Weller M, Meyermann R, Wolburg H, Mittelbronn M (2007) Expression pattern of the water channel aquaporin-4 in human gliomas is associated with blood–brain barrier disturbance but not with patient survival. J Neurosci Res 85:1336–1345

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by European Union Seventh Framework Programme (FPT7/2007-2013) under grant agreement no. 278570 to DR.

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Correspondence to Domenico Ribatti .

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Nico, B., Ruggieri, S., Ribatti, D. (2014). Human Brain Tumor Growth: Role of Aquaporins. In: Hayat, M. (eds) Tumors of the Central Nervous System, Volume 12. Tumors of the Central Nervous System, vol 12. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-7217-5_4

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  • DOI: https://doi.org/10.1007/978-94-007-7217-5_4

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