Functional properties of ion channels and transporters in tumour vascularization

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 369, Issue 1638, 2014, Pages

  Fiorio Pla, Alessandra ^a   Munaron, Luca ^a  

^a UNIVERSITY OF TURIN   (Italy)

Author keywords

Aquaporins; Endothelial cells; Ion channels; Transporters; Tumour vascularization

Indexed keywords

BIOCHEMISTRY; CYTOLOGY; DEVELOPMENTAL BIOLOGY; FUNCTIONAL ROLE; ION; METABOLISM; PATHOLOGY; PHYSIOLOGY; PROTEIN; SIGNALING; TUMOR;

AQUAPORIN; ION CHANNEL; NICOTINIC RECEPTOR;

BIOLOGICAL MODEL; CELL ADHESION; CELL MOTION; CELL PROLIFERATION; ENDOTHELIUM CELL; HUMAN; ION TRANSPORT; METABOLISM; NEOPLASM; NEOVASCULARIZATION (PATHOLOGY); PATHOPHYSIOLOGY; PHYSIOLOGY; REVIEW; SIGNAL TRANSDUCTION; TRANSPORTERS; TUMOUR VASCULARIZATION;

AQUAPORINS; ENDOTHELIAL CELLS; ION CHANNELS; TRANSPORTERS; TUMOUR VASCULARIZATION;

CELL ADHESION; CELL MOVEMENT; CELL PROLIFERATION; ENDOTHELIAL CELLS; HUMANS; ION CHANNELS; ION TRANSPORT; MODELS, BIOLOGICAL; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; RECEPTORS, NICOTINIC; SIGNAL TRANSDUCTION;

EID: 84893432409     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2013.0103     Document Type: Review

References (108)

1. Carmeliet P. 2005 Angiogenesis in life, disease and medicine. Nature 438, 932-936. (doi:10.1038/nature04478)
2. Folkman J. 1971 Tumor angiogenesis: therapeutic implications. N. Engl. J. Med. 285, 1182-1186. (doi:10.1056/NEJM197111182852108)
3. Potente M, Gerhardt H, Carmeliet P. 2011 Basic and therapeutic aspects of angiogenesis. Cell 146, 873-887. (doi:10.1016/j.cell.2011.08.039)
4. Regan ER, Aird WC. 2012 Dynamical systems approach to endothelial heterogeneity. Circ. Res. 111, 110-130. (doi:10.1161/CIRCRESAHA.111. 261701)
5. Chi J-T et al. 2003 Endothelial cell diversity revealed by global expression profiling. Proc. Natl Acad. Sci. USA 100, 10 623-10-628. (doi:10.1073/pnas. 1434429100)
6. Bussolati B, Grange C, Camussi G. 2011 Tumor exploits alternative strategies to achieve vascularization. FASEB J. 25, 2874-2882. (doi:10.1096/fj.10-180323)
7. Ghilardi C, Chiorino G, Dossi R, Nagy Z, Giavazzi R, Bani M. 2008 Identification of novel vascular markers through gene expression profiling of tumor-derived endothelium. BMC Genomics 9, 201. (doi:10.1186/1471-2164-9-201)
8. Bhati R et al. 2008 Molecular characterization of human breast tumor vascular cells. Am. J. Pathol. 172, 1381-1390. (doi:10.2353/ajpath.2008.070988)
9. Ohga N et al. 2012 Heterogeneity of tumor endothelial cells: comparison between tumor endothelial cells isolated from high-and lowmetastatic tumors. Am. J. Pathol. 180, 1294-1307. (doi:10.1016/j.ajpath.2011.11.035)
10. Bussolati B, Deambrosis I, Russo S, Deregibus MC, Camussi G. 2003 Altered angiogenesis and survival in human tumor-derived endothelial cells. FASEB J. 17, 1159-1161.
11. Grange C, Bussolati B, Bruno S, Fonsato V, Sapino A, Camussi G. 2006 Isolation and characterization of human breast tumor-derived endothelial cells. Oncol. Rep. 15, 381-386.
12. Park M-T et al. 2012 The radiosensitivity of endothelial cells isolated from human breast cancer and normal tissue in vitro. Microvasc. Res. 84, 140-148. (doi:10.1016/j.mvr.2012.06.002)
13. 2+ entry is involved in early steps of tumor angiogenesis. Mol. Cancer Res. 6, 535-545. (doi:10.1158/1541-7786.MCR-07-0271)
14. 2+ entry and tumor-derived human endothelial cell migration. Mol. Cancer Res. 8, 1466-1476. (doi:10.1158/1541-7786.MCR-10-0002)
15. Pupo E, Pla AF, Avanzato D, Moccia F, Cruz JE, Tanzi F, Merlino A, Mancardi D, Munaron L. 2011 Hydrogen sulfide promotes calcium signals and migration in tumor-derived endothelial cells. Free Radic. Biol. Med. 51, 1765-1773. (doi:10.1016/j. freeradbiomed.2011.08.007)
16. Hanahan D, Weinberg RA. 2011 Hallmarks of cancer: the next generation. Cell 144, 646-674. (doi:10.1016/j.cell.2011.02.013)
17. Fiorio Pla A, Avanzato D, Munaron L, Ambudkar IS. 2012 Ion channels and transporters in cancer. 6. Vascularizing the tumor: TRP channels as molecular targets. Am. J. Physiol. Cell Physiol. 302, C9-C15. (doi:10.1152/ajpcell.00280.2011)
18. Munaron L, Genova T, Avanzato D, Antoniotti S, Fiorio Pla A. 2013 Targeting calcium channels to block tumor vascularization. Recent Patents Anticancer Drug Discov. 8, 27-37.
19. Yao X, Garland CJ. 2005 Recent developments in vascular endothelial cell transient receptor potential channels. Circ. Res. 97, 853-863. (doi:10.1161/01. RES.0000187473.85419.3e)
20. Watanabe H, Murakami M, Ohba T, Takahashi Y, Ito H. 2008 TRP channel and cardiovascular disease. Pharmacol. Ther. 118, 337-351. (doi:10.1016/j. pharmthera.2008.03.008)
21. Nilius B, Owsianik G, Voets T, Peters JA. 2007 Transient receptor potential cation channels in disease. Physiol. Rev. 87, 165-217. (doi:10.1152/physrev.00021.2006)
22. Nilius B, Droogmans G. 2001 Ion channels and their functional role in vascular endothelium. Physiol. Rev. 81, 1415-1459.
23. Becchetti A. 2011 Ion channels and transporters in cancer. 1. Ion channels and cell proliferation in cancer. Am. J. Physiol. Cell Physiol. 301, C255-C265. (doi:10.1152/ajpcell.00047.2011)
24. Arcangeli A, Crociani O, Lastraioli E, Masi A, Pillozzi S, Becchetti A. 2009 Targeting ion channels in cancer: a novel frontier in antineoplastic therapy. Curr. Med. Chem. 16, 66-93. (doi:10.2174/092986709787002835)
25. Wulff H, Castle NA, Pardo LA. 2009 Voltage-gated potassium channels as therapeutic targets. Nat. Rev. Drug Discov. 8, 982-1001. (doi:10.1038/nrd2983)
26. Gómez-Varela D et al. 2007 Monoclonal antibody blockade of the human Eag1 potassium channel function exerts antitumor activity. Cancer Res. 67, 7343-7349. (doi:10.1158/0008-5472.CAN-07-0107)
27. Downie BR, Sánchez A, Knötgen H, Contreras-Jurado C, Gymnopoulos M, Weber C, Stühmer W, Pardo LA. 2008 Eag1 expression interferes with hypoxia homeostasis and induces angiogenesis in tumors. J. Biol. Chem. 283, 36 234-36 240. (doi:10.1074/jbc.M801830200)
28. Wu J, Wu X, Zhong D, Zhai W, Ding Z, Zhou Y. 2012 Short hairpin RNA (shRNA) Ether àgo-go 1 (Eag1) inhibition of human osteosarcoma angiogenesis via VEGF/PI3K/AKT signaling. Int. J. Mol. Sci. 13, 12 573-12 583. (doi:10.3390/ijms131012573)
29. 2+ entry is remodelled and controls in vitro angiogenesis in endothelial progenitor cells isolated from tumoral patients. PLoS ONE 7, e42541. (doi:10.1371/journal. pone.0042541)
30. Kuang C, Yu Y, Wang K, Qian D, Den M, Huang L. 2012 Knockdown of transient receptor potential canonical-1 reduces the proliferation and migration of endothelial progenitor cells. Stem Cells Dev. 21, 487-496. (doi:10.1089/scd.2011.0027)
31. Hamdollah Zadeh MA, Glass CA, Magnussen A, Hancox JC, Bates DO. 2008 VEGF-mediated elevated intracellular calcium and angiogenesis in human microvascular endothelial cells in vitro are inhibited by dominant negative TRPC6. Microcirculation 15, 605-614. (doi:10.1080/10739680802220323)
32. Fiorio Pla A, Ong HL, Cheng KT, Brossa A, Bussolati B, Lockwich T, Paria B, Munaron L, Ambudkar IS. 2012 TRPV4 mediates tumor-derived endothelial cell migration via arachidonic acid-activated actin remodeling. Oncogene 31, 200-212. (doi:10.1038/onc.2011.231)
33. Abdullaev IF, Bisaillon JM, Potier M, Gonzalez JC, Motiani RK, Trebak M. 2008 Stim1 and Orai1 mediate CRAC currents and store-operated calcium entry important for endothelial cell proliferation. Circ. Res. 103, 1289-1299. (doi:10.1161/01.RES. 0000338496.95579.56)
34. 2+ entry and endothelial tube formation. Circ. Res. 108, 1190-1198. (doi:10.1161/CIRCRESAHA.111.243352)
35. Beech DJ. 2012 Orai1 calcium channels in the vasculature. Pflügers Arch. 463, 635-647. (doi:10.1007/s00424-012-1090-2)
36. + Channels in human endothelial cells: modulation of vascular endothelial growth factor (VEGF) signaling. J. Biol. Chem. 286, 16 846-16-860. (doi:10.1074/jbc.M110.187559)
37. Martini A, Bruno R, Mazzulla S, Nocita A, Martino G. 2010 Angiotensin II regulates endothelial cell migration through calcium influx via T-type calcium channel in human umbilical vein endothelial cells. Acta Physiol. 198, 449-455. (doi:10.1111/j.1748-1716.2009.02070.x)
38. Xu L, Fukumura D, Jain RK. 2002 Acidic extracellular pH induces vascular endothelial growth factor (VEGF) in human glioblastoma cells via ERK1/2 MAPK signaling pathway: mechanism of low pHinduced VEGF. J. Biol. Chem. 277, 11 368-11 374. (doi:10.1074/jbc.M108347200)
39. 2+ exchange is critical for vascular endothelial growth factor-mediated extracellular signal-regulated kinase (ERK) 1/2 activation and angiogenic functions of human endothelial cells. J. Biol. Chem. 286, 37 919-37 931. (doi:10.1074/jbc.M111.251777)
40. Nicchia GP, Stigliano C, Sparaneo A, Rossi A, Frigeri A, Svelto M. 2013 Inhibition of aquaporin-1 dependent angiogenesis impairs tumour growth in a mouse model of melanoma. J. Mol. Med. 91, 613-623. (doi:10.1007/s00109-012-0977-x)
41. Heeschen C, Weis M, Aicher A, Dimmeler S, Cooke JP. 2002 A novel angiogenic pathway mediated by non-neuronal nicotinic acetylcholine receptors. J. Clin. Invest. 110, 527-536.
42. Wu JCF, Chruscinski A, De Jesus Perez VA, Singh H, Pitsiouni M, Rabinovitch M, Utz PJ, Cooke JP. 2009 Cholinergic modulation of angiogenesis: role of the 7 nicotinic acetylcholine receptor. J. Cell. Biochem. 108, 433-446. (doi:10.1002/jcb.22270)
43. Yu M, Liu Q, Sun J, Yi K, Wu L, Tan X. 2011 Nicotine improves the functional activity of late endothelial progenitor cells via nicotinic acetylcholine receptors. Biochem. Cell Biol. 89, 405-410. (doi:10.1139/o11-032)
44. Ge R, Tai Y, Sun Y, Zhou K, Yang S, Cheng T, Zou Q, Shen F, Wang Y. 2009 Critical role of TRPC6 channels in VEGF-mediated angiogenesis. Cancer Lett. 283, 43-51. (doi:10.1016/j.canlet.2009. 03.023)
45. Troidl C et al. 2009 Trpv4 induces collateral vessel growth during regeneration of the arterial circulation. J. Cell. Mol. Med. 13, 2613-2621. (doi:10.1111/j.1582-4934.2008.00579.x)
46. 2+ entry and endothelial hyperpermeability. Circ. Res. 102, 347-355. (doi:10.1161/CIRCRESAHA.107.160176)
47. Inoue K, Xiong Z-G. 2009 Silencing TRPM7 promotes growth/proliferation and nitric oxide production of vascular endothelial cells via the ERK pathway. Cardiovasc. Res. 83, 547-557. (doi:10.1093/cvr/cvp153)
48. Baldoli E, Maier JAM. 2012 Silencing TRPM7 mimics the effects of magnesium deficiency in human microvascular endothelial cells. Angiogenesis 15, 47-57. (doi:10.1007/s10456-011-9242-0)
49. Baldoli E, Castiglioni S, Maier JAM. 2013 Regulation and function of TRPM7 in human endothelial cells: TRPM7 as a potential novel regulator of endothelial function. PLoS ONE 8, e59891. (doi:10.1371/journal. pone.0059891)
50. Erdogan A et al. 2005 Margatoxin inhibits VEGFinduced hyperpolarization, proliferation and nitric oxide production of human endothelial cells. J. Vasc. Res. 42, 368-376. (doi:10.1159/000087159)
51. Vacca A, Frigeri A, Ribatti D, Nicchia GP, Nico B, Ria R, Svelto M, Dammacco F. 2001 Microvessel overexpression of aquaporin 1 parallels bone marrow angiogenesis in patients with active multiple myeloma. Br. J. Haematol. 113, 415-421. (doi:10.1046/j.1365-2141.2001.02738.x)
52. Antigny F, Girardin N, Frieden M. 2012 Transient receptor potential canonical channels are required for in vitro endothelial tube formation. J. Biol. Chem. 287, 5917-5927. (doi:10.1074/jbc. M111.295733)
53. Chigurupati S et al. 2010 Receptor channel TRPC6 is a key mediator of Notch-driven glioblastoma growth and invasiveness. Cancer Res. 70, 418-427. (doi:10.1158/0008-5472.CAN-09-2654)
54. Manolopoulos VG, Liekens S, Koolwijk P, Voets T, Peters E, Droogmans G, Lelkes PI, De Clercq E, Nilius B. 2000 Inhibition of angiogenesis by blockers of volume-regulated anion channels. Gen. Pharmacol. 34, 107-116. (doi:10.1016/S0306-3623(00)00052-5)
55. Egleton RD, Brown KC, Dasgupta P. 2009 Angiogenic activity of nicotinic acetylcholine receptors: Implications in tobacco-related vascular diseases. Pharmacol. Ther. 121, 205-223. (doi:10.1016/j.pharmthera.2008.10.007)
56. 2+ entry. Role in signaling increased endothelial permeability. J. Biol. Chem. 278, 33 492-33 500. (doi:10.1074/jbc. M302401200)
57. 2+ influx and endothelial permeability. Am. J. Physiol. Lung Cell Mol. Physiol. 287, L1303-L1313. (doi:10.1152/ajplung. 00240.2004)
58. 2+ influx. Circ. Res. 96, 1282-1290. (doi:10.1161/01.RES. 0000171894.03801.03)
59. 2+ entry, endothelial permeability, and angiogenesis. J. Biol. Chem. 285, 33 082-33 091. (doi:10.1074/jbc.M110.142034)
60. Pocock TM, Foster RR, Bates DO. 2004 Evidence of a role for TRPC channels in VEGF-mediated increased vascular permeability in vivo. Am. J. Physiol. Heart Circ. Physiol. 286, H1015-H1026. (doi:10.1152/ajpheart.00826.2003)
61. 2+ entry. Sci. Signal. 6, ra18. (doi:10.1126/scisignal. 2003425)
62. Yu P, Gu S, Bu J, Du J. 2010 TRPC1 is essential for in vivo angiogenesis in zebrafish. Circ. Res. 106, 1221-1232. (doi:10.1161/CIRCRESAHA.109.207670)
63. Fortunato P, Pillozzi S, Tamburini A, Pollazzi L, Franchi A, La Torre A, Arcangeli A. 2010 Irresponsiveness of two retinoblastoma cases to conservative therapy correlates with up-regulation of hERG1 channels and of the VEGF-A pathway. BMC Cancer 10, 504. (doi:10.1186/1471-2407-10-504)
64. Blaustein MP, Lederer WJ. 1999 Sodium/calcium exchange: its physiological implications. Physiol. Rev. 79, 763-854.
65. Endo M, Jain RK, Witwer B, Brown D. 1999 Water channel (aquaporin 1) expression and distribution in mammary carcinomas and glioblastomas. Microvasc. Res. 58, 89-98. (doi:10.1006/mvre.1999.2158)
66. Saadoun S, Papadopoulos MC, Davies DC, Bell BA, Krishna S. 2002 Increased aquaporin 1 water channel expression in human brain tumours. Br. J. Cancer 87, 621-623. (doi:10.1038/sj.bjc. 6600512)
67. Saadoun S, Papadopoulos MC, Hara-Chikuma M, Verkman AS. 2005 Impairment of angiogenesis and cell migration by targeted aquaporin-1 gene disruption. Nature 434, 786-792. (doi:10.1038/nature03460)
68. Huebert RC, Jagavelu K, Hendrickson HI, Vasdev MM, Arab JP, Splinter PL, Trussoni CE, Larusso NF, Shah VH. 2011 Aquaporin-1 promotes angiogenesis, fibrosis, and portal hypertension through mechanisms dependent on osmotically sensitive microRNAs. Am. J. Pathol. 179, 1851-1860. (doi:10.1016/j.ajpath.2011.06.045)
69. Ng MKC, Wu J, Chang E, Wang B, Katzenberg-Clark R, Ishii-Watabe A, Cooke JP. 2007 A central role for nicotinic cholinergic regulation of growth factorinduced endothelial cell migration. Arterioscler. Thromb. Vasc. Biol. 27, 106-112. (doi:10.1161/01. ATV.0000251517.98396.4a)
70. Munaron L, Arcangeli A. 2013 Editorial: ion fluxes and cancer. Recent Patents Anti-Cancer Drug Discov. 8, 1-3. (doi:10.2174/1574892811308010001)
71. D'Amico M, Gasparoli L, Arcangeli A. 2013 Potassium channels: novel emerging biomarkers and targets for therapy in cancer. Recent Patents Anti-Cancer Drug Discov. 8, 53-65.
72. + channel for a macromolecular signaling complex in acute myeloid leukemia: role in cell migration and clinical outcome. Blood 110, 1238-1250. (doi:10.1182/blood-2006-02-003772)
73. Yildirim S, Altun S, Gumushan H, Patel A, Djamgoz MBA. 2012 Voltage-gated sodium channel activity promotes prostate cancer metastasis in vivo. Cancer Lett. 323, 58-61. (doi:10.1016/j.canlet.2012.03.036)
74. Djamgoz MBA, Onkal R. 2013 Persistent current blockers of voltage-gated sodium channels: a clinical opportunity for controlling metastatic disease. Recent Patents Anti-Cancer Drug Discov. 8, 66-84.
75. + channel SCN5A is a key regulator of a gene transcriptional network that controls colon cancer invasion. Cancer Res. 70, 6957-6967. (doi:10.1158/0008-5472.CAN-10-1169)
76. 2+ channel antagonists mibefradil and pimozide inhibit cell growth via different cytotoxic mechanisms. Mol. Pharmacol. 62, 210-219. (doi:10.1124/mol.62.2.210)
77. Asaga S, Ueda M, Jinno H, Kikuchi K, Itano O, Ikeda T, Kitajima M. In press. Identification of a new breast cancer-related gene by restriction landmark genomic scanning. Anticancer Res. 26, 35-42.
78. Panner A, Wurster RD. 2006 T-type calcium channels and tumor proliferation. Cell Calcium 40, 253-259. (doi:10.1016/j.ceca.2006.04.029)
79. Miura S-I, Fujino M, Matsuo Y, Tanigawa H, Saku K. 2005 Nifedipine-induced vascular endothelial growth factor secretion from coronary smooth muscle cells promotes endothelial tube formation via the kinase insert domain-containing receptor/fetal liver kinase-1/NO pathway. Hypertens. Res. 28, 147-153. (doi:10.1291/hypres.28.147)
80. Gkika D, Prevarskaya N. 2011 TRP channels in prostate cancer: the good, the bad and the ugly? Asian J. Androl. 13, 673-676. (doi:10.1038/aja.2011.18)
81. Ambudkar IS, Ong HL. 2007 Organization and function of TRPC channelosomes. Pflügers Arch. 455, 187-200. (doi:10.1007/s00424-007-0252-0)
82. Cheng H-W, James AF, Foster RR, Hancox JC, Bates DO. 2006 VEGF activates receptor-operated cation channels in human microvascular endothelial cells. Arterioscler. Thromb. Vasc. Biol. 26, 1768-1776. (doi:10.1161/01.ATV.0000231518.86795.0f)
83. Everaerts W, Nilius B, Owsianik G. 2010 The vanilloid transient receptor potential channel TRPV4: from structure to disease. Prog. Biophys. Mol. Biol. 103, 2-17. (doi:10.1016/j.pbiomolbio. 2009.10.002)
84. Vriens J, Watanabe H, Janssens A, Droogmans G, Voets T, Nilius B. 2004 Cell swelling, heat, and chemical agonists use distinct pathways for the activation of the cation channel TRPV4. Proc. Natl Acad. Sci. USA 101, 396-401. (doi:10.1073/pnas.0303329101)
85. Hartmannsgruber V, Heyken W-T, Kacik M, Kaistha A, Grgic I, Harteneck C, Liedtke W, Hoyer J, Köhler R. 2007 Arterial response to shear stress critically depends on endothelial TRPV4 expression. PLoS ONE 2, e827. (doi:10.1371/journal.pone.0000827)
86. Thodeti CK, Matthews B, Ravi A, Mammoto A, Ghosh K, Bracha AL, Ingber DE. 2009 TRPV4 channels mediate cyclic strain-induced endothelial cell reorientation through integrin-to-integrin signaling. Circ. Res. 104, 1123-1130. (doi:10.1161/CIRCRESAHA.108.192930)
87. North S, Moenner M, Bikfalvi A. 2005 Recent developments in the regulation of the angiogenic switch by cellular stress factors in tumors. Cancer Lett. 218, 1-14. (doi:10.1016/j.canlet.2004. 08.007)
88. 2-induced cell apoptosis in endothelial cells. PLoS ONE 7, e43186. (doi:10.1371/journal.pone.0043186)
89. Orfanelli U, Wenke A-K, Doglioni C, Russo V, Bosserhoff AK, Lavorgna G. 2008 Identification of novel sense and antisense transcription at the TRPM2 locus in cancer. Cell Res. 18, 1128-1140. (doi:10.1038/cr.2008.296)
90. Yogi A, Callera GE, Antunes TT, Tostes RC, Touyz RM. 2011 Transient receptor potential melastatin 7 (TRPM7) cation channels, magnesium and the vascular system in hypertension. Circ. J. 75, 237-245. (doi:10.1253/circj.CJ-10-1021)
91. Paravicini TM, Chubanov V, Gudermann T. 2012 TRPM7: a unique channel involved in magnesium homeostasis. Int. J. Biochem. Cell Biol. 44, 1381-1384. (doi:10.1016/j.biocel.2012.05.010)
92. 2+ concentration. Stem Cells 29, 1898-1907. (doi:10.1002/stem.734)
93. Taly A, Corringer P-J, Guedin D, Lestage P, Changeux J-P. 2009 Nicotinic receptors: allosteric transitions and therapeutic targets in the nervous system. 1-18. Nat. Rev. Drug Discov. 8(9): 733-750. (doi:10.1038/nrd2927)
94. Cardinale A, Nastrucci C, Cesario A, Russo P. 2012 Nicotine: specific role in angiogenesis, proliferation and apoptosis. Crit. Rev. Toxicol. 42, 68-89. (doi:10.3109/10408444.2011.623150)
95. Mousa S, Mousa SA. 2006 Cellular and molecular mechanisms of nicotine's pro-angiogenesis activity and its potential impact on cancer. J. Cell. Biochem. 97, 1370-1378. (doi:10.1002/jcb.20741)
96. Arias HR, Richards VE, Ng D, Ghafoori ME, Le V, Mousa SA. 2009 Role of non-neuronal nicotinic acetylcholine receptors in angiogenesis. Int. J. Biochem. Cell Biol. 41, 1441-1451. (doi:10.1016/j.biocel.2009.01.013)
97. Nilius B, Droogmans G. 2003 Amazing chloride channels: an overview. Acta Physiol. Scand. 177, 119-147. (doi:10.1046/j.1365-201X.2003.01060.x)
98. Monzani E, Shtil AA, La Porta CAM. 2007 The water channels, new druggable targets to combat cancer cell survival, invasiveness and metastasis. Curr. Drug Targets 8, 1132-1137. (doi:10.2174/13894500778 2151342)
99. Verkman AS. 2012 Aquaporins in clinical medicine. Annu. Rev. Med. 63, 303-316. (doi:10.1146/annurev-med-043010-193843)
100. Alleva K, Chara O, Amodeo G. 2012 Aquaporins: another piece in the osmotic puzzle. FEBS Lett. 586, 2991-2999. (doi:10.1016/j.febslet.2012.06.013)
101. + exchanger in metastasis. Nat. Rev. Cancer 5, 786-795. (doi:10.1038/nrc1713)
102. Monteith GR, Davis FM, Roberts-Thomson SJ. 2012 Calcium channels and pumps in cancer: changes and consequences. J. Biol. Chem. 287, 31 666-31 673. (doi:10.1074/jbc.R112.343061)
103. + exchanger, pH regulation and cancer. Recent Patents Anti-Cancer Drug Discov. 8, 85-99.
104. + exchanger inhibitor cariporide through downregulation of pro-angiogenesis factor VEGF. Leukemia Res. 35, 1506-1511. (doi:10.1016/j. leukres.2011.07.001)
105. Avery RL, Connor TB, Farazdaghi M. 1990 Systemic amiloride inhibits experimentally induced neovascularization. Arch. Ophthalmol. 108, 1474-1476. (doi:10.1001/archopht.1990. 01070120122041)
106. Ebos JML, Kerbel RS. 2011 Antiangiogenic therapy: impact on invasion, disease progression, and metastasis. Nat. Rev. Clin. Oncol. 8, 210-221. (doi:10.1038/nrclinonc.2011.21)
107. Cheng J, Gu Y-J, Wang Y, Cheng SH, Wong W-T. 2011 Nanotherapeutics in angiogenesis: synthesis and in vivo assessment of drug efficacy and biocompatibility in zebrafish embryos. Int. J. Nanomed. 6, 2007-2021. (doi:10.2147/IJN. S20145)
108. Carmeliet P, Jain RK. 2011 Principles and mechanisms of vessel normalization for cancer and other angiogenic diseases. Nat. Rev. Drug Discov. 10, 417-427. (doi:10.1038/nrd3455)