Skip to main content
Top
Published in: BMC Cancer 1/2011

Open Access 01-12-2011 | Research article

Loss of aquaporin-4 expression and putative function in non-small cell lung cancer

Authors: Arne Warth, Thomas Muley, Michael Meister, Esther Herpel, Anita Pathil, Hans Hoffmann, Philipp A Schnabel, Christian Bender, Andreas Buness, Peter Schirmacher, Ruprecht Kuner

Published in: BMC Cancer | Issue 1/2011

Login to get access

Abstract

Background

Aquaporins (AQPs) have been recognized to promote tumor progression, invasion, and metastasis and are therefore recognized as promising targets for novel anti-cancer therapies. Potentially relevant AQPs in distinct cancer entities can be determined by a comprehensive expression analysis of the 13 human AQPs.

Methods

We analyzed the presence of all AQP transcripts in 576 different normal lung and non-small cell lung cancer (NSCLC) samples using microarray data and validated our findings by qRT-PCR and immunohistochemistry.

Results

Variable expression of several AQPs (AQP1, -3, -4, and -5) was found in NSCLC and normal lung tissues. Furthermore, we identified remarkable differences between NSCLC subtypes in regard to AQP1, -3 and -4 expression. Higher transcript and protein levels of AQP4 in well-differentiated lung adenocarcinomas suggested an association with a more favourable prognosis. Beyond water transport, data mining of co-expressed genes indicated an involvement of AQP4 in cell-cell signalling, cellular movement and lipid metabolism, and underlined the association of AQP4 to important physiological functions in benign lung tissue.

Conclusions

Our findings accentuate the need to identify functional differences and redundancies of active AQPs in normal and tumor cells in order to assess their value as promising drug targets.
Appendix
Available only for authorised users
Literature
1.
go back to reference Rojek A, Praetorius J, Frokiaer J, Nielsen S, Fenton RA: A current view of the mammalian aquaglyceroporins. Annu Rev Physiol. 2008, 70: 301-327. 10.1146/annurev.physiol.70.113006.100452.CrossRefPubMed Rojek A, Praetorius J, Frokiaer J, Nielsen S, Fenton RA: A current view of the mammalian aquaglyceroporins. Annu Rev Physiol. 2008, 70: 301-327. 10.1146/annurev.physiol.70.113006.100452.CrossRefPubMed
2.
3.
go back to reference Jablonski EM, Mattocks MA, Sokolov E, Koniaris LG, Hughes FM, Fausto N, Pierce RH, McKillop IH: Decreased aquaporin expression leads to increased resistance to apoptosis in hepatocellular carcinoma. Cancer Lett. 2007, 250 (1): 36-46. 10.1016/j.canlet.2006.09.013.CrossRefPubMed Jablonski EM, Mattocks MA, Sokolov E, Koniaris LG, Hughes FM, Fausto N, Pierce RH, McKillop IH: Decreased aquaporin expression leads to increased resistance to apoptosis in hepatocellular carcinoma. Cancer Lett. 2007, 250 (1): 36-46. 10.1016/j.canlet.2006.09.013.CrossRefPubMed
4.
go back to reference Ismail M, Bokaee S, Davies J, Harrington KJ, Pandha H: Inhibition of the aquaporin 3 water channel increases the sensitivity of prostate cancer cells to cryotherapy. Br J Cancer. 2009, 100 (12): 1889-1895. 10.1038/sj.bjc.6605093.CrossRefPubMedPubMedCentral Ismail M, Bokaee S, Davies J, Harrington KJ, Pandha H: Inhibition of the aquaporin 3 water channel increases the sensitivity of prostate cancer cells to cryotherapy. Br J Cancer. 2009, 100 (12): 1889-1895. 10.1038/sj.bjc.6605093.CrossRefPubMedPubMedCentral
5.
go back to reference Hara-Chikuma M, Verkman AS: Prevention of skin tumorigenesis and impairment of epidermal cell proliferation by targeted aquaporin-3 gene disruption. Mol Cell Biol. 2008, 28 (1): 326-332. 10.1128/MCB.01482-07.CrossRefPubMed Hara-Chikuma M, Verkman AS: Prevention of skin tumorigenesis and impairment of epidermal cell proliferation by targeted aquaporin-3 gene disruption. Mol Cell Biol. 2008, 28 (1): 326-332. 10.1128/MCB.01482-07.CrossRefPubMed
6.
go back to reference Papadopoulos MC, Saadoun S, Verkman AS: Aquaporins and cell migration. Pflugers Arch. 2008, 456 (4): 693-700. 10.1007/s00424-007-0357-5.CrossRefPubMed Papadopoulos MC, Saadoun S, Verkman AS: Aquaporins and cell migration. Pflugers Arch. 2008, 456 (4): 693-700. 10.1007/s00424-007-0357-5.CrossRefPubMed
7.
go back to reference Saadoun S, Papadopoulos MC, Hara-Chikuma M, Verkman AS: Impairment of angiogenesis and cell migration by targeted aquaporin-1 gene disruption. Nature. 2005, 434 (7034): 786-792. 10.1038/nature03460.CrossRefPubMed Saadoun S, Papadopoulos MC, Hara-Chikuma M, Verkman AS: Impairment of angiogenesis and cell migration by targeted aquaporin-1 gene disruption. Nature. 2005, 434 (7034): 786-792. 10.1038/nature03460.CrossRefPubMed
8.
go back to reference Warth A, Mittelbronn M, Hulper P, Erdlenbruch B, Wolburg H: Expression of the water channel protein aquaporin-9 in malignant brain tumors. Appl Immunohistochem Mol Morphol. 2007, 15 (2): 193-198. 10.1097/01.pai.0000213110.05108.e9.CrossRefPubMed Warth A, Mittelbronn M, Hulper P, Erdlenbruch B, Wolburg H: Expression of the water channel protein aquaporin-9 in malignant brain tumors. Appl Immunohistochem Mol Morphol. 2007, 15 (2): 193-198. 10.1097/01.pai.0000213110.05108.e9.CrossRefPubMed
9.
go back to reference Echevarria M, Munoz-Cabello AM, Sanchez-Silva R, Toledo-Aral JJ, Lopez-Barneo J: Development of cytosolic hypoxia and hypoxia-inducible factor stabilization are facilitated by aquaporin-1 expression. J Biol Chem. 2007, 282 (41): 30207-30215. 10.1074/jbc.M702639200.CrossRefPubMed Echevarria M, Munoz-Cabello AM, Sanchez-Silva R, Toledo-Aral JJ, Lopez-Barneo J: Development of cytosolic hypoxia and hypoxia-inducible factor stabilization are facilitated by aquaporin-1 expression. J Biol Chem. 2007, 282 (41): 30207-30215. 10.1074/jbc.M702639200.CrossRefPubMed
10.
go back to reference Kang SK, Chae YK, Woo J, Kim MS, Park JC, Lee J, Soria JC, Jang SJ, Sidransky D, Moon C: Role of human aquaporin 5 in colorectal carcinogenesis. Am J Pathol. 2008, 173 (2): 518-525. 10.2353/ajpath.2008.071198.CrossRefPubMedPubMedCentral Kang SK, Chae YK, Woo J, Kim MS, Park JC, Lee J, Soria JC, Jang SJ, Sidransky D, Moon C: Role of human aquaporin 5 in colorectal carcinogenesis. Am J Pathol. 2008, 173 (2): 518-525. 10.2353/ajpath.2008.071198.CrossRefPubMedPubMedCentral
11.
go back to reference Monzani E, Shtil AA, La Porta CA: The water channels, new druggable targets to combat cancer cell survival, invasiveness and metastasis. Curr Drug Targets. 2007, 8 (10): 1132-1137. 10.2174/138945007782151342.CrossRefPubMed Monzani E, Shtil AA, La Porta CA: The water channels, new druggable targets to combat cancer cell survival, invasiveness and metastasis. Curr Drug Targets. 2007, 8 (10): 1132-1137. 10.2174/138945007782151342.CrossRefPubMed
12.
go back to reference Jeyaseelan K, Sepramaniam S, Armugam A, Wintour EM: Aquaporins: a promising target for drug development. Expert Opin Ther Targets. 2006, 10 (6): 889-909. 10.1517/14728222.10.6.889.CrossRefPubMed Jeyaseelan K, Sepramaniam S, Armugam A, Wintour EM: Aquaporins: a promising target for drug development. Expert Opin Ther Targets. 2006, 10 (6): 889-909. 10.1517/14728222.10.6.889.CrossRefPubMed
14.
go back to reference Mobasheri A, Airley R, Hewitt SM, Marples D: Heterogeneous expression of the aquaporin 1 (AQP1) water channel in tumors of the prostate, breast, ovary, colon and lung: a study using high density multiple human tumor tissue microarrays. Int J Oncol. 2005, 26 (5): 1149-1158.PubMed Mobasheri A, Airley R, Hewitt SM, Marples D: Heterogeneous expression of the aquaporin 1 (AQP1) water channel in tumors of the prostate, breast, ovary, colon and lung: a study using high density multiple human tumor tissue microarrays. Int J Oncol. 2005, 26 (5): 1149-1158.PubMed
15.
go back to reference 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: Aquaporin 1 is overexpressed in lung cancer and stimulates NIH-3T3 cell proliferation and anchorage-independent growth. Am J Pathol. 2006, 168 (4): 1345-1353. 10.2353/ajpath.2006.050596.CrossRefPubMedPubMedCentral 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: Aquaporin 1 is overexpressed in lung cancer and stimulates NIH-3T3 cell proliferation and anchorage-independent growth. Am J Pathol. 2006, 168 (4): 1345-1353. 10.2353/ajpath.2006.050596.CrossRefPubMedPubMedCentral
16.
go back to reference Hu J, Verkman AS: Increased migration and metastatic potential of tumor cells expressing aquaporin water channels. Faseb J. 2006, 20 (11): 1892-1894. 10.1096/fj.06-5930fje.CrossRefPubMed Hu J, Verkman AS: Increased migration and metastatic potential of tumor cells expressing aquaporin water channels. Faseb J. 2006, 20 (11): 1892-1894. 10.1096/fj.06-5930fje.CrossRefPubMed
17.
go back to reference Liu YL, Matsuzaki T, Nakazawa T, Murata S, Nakamura N, Kondo T, Iwashina M, Mochizuki K, Yamane T, Takata K, Katoh R: Expression of aquaporin 3 (AQP3) in normal and neoplastic lung tissues. Hum Pathol. 2007, 38 (1): 171-178. 10.1016/j.humpath.2006.07.015.CrossRefPubMed Liu YL, Matsuzaki T, Nakazawa T, Murata S, Nakamura N, Kondo T, Iwashina M, Mochizuki K, Yamane T, Takata K, Katoh R: Expression of aquaporin 3 (AQP3) in normal and neoplastic lung tissues. Hum Pathol. 2007, 38 (1): 171-178. 10.1016/j.humpath.2006.07.015.CrossRefPubMed
18.
go back to reference Chae YK, Woo J, Kim MJ, Kang SK, Kim MS, Lee J, Lee SK, Gong G, Kim YH, Soria JC, Jang SJ, Sidransky D, Moon C: Expression of aquaporin 5 (AQP5) promotes tumor invasion in human non small cell lung cancer. PLoS ONE. 2008, 3 (5): e2162-10.1371/journal.pone.0002162.CrossRefPubMedPubMedCentral Chae YK, Woo J, Kim MJ, Kang SK, Kim MS, Lee J, Lee SK, Gong G, Kim YH, Soria JC, Jang SJ, Sidransky D, Moon C: Expression of aquaporin 5 (AQP5) promotes tumor invasion in human non small cell lung cancer. PLoS ONE. 2008, 3 (5): e2162-10.1371/journal.pone.0002162.CrossRefPubMedPubMedCentral
19.
go back to reference Zhang Z, Chen Z, Song Y, Zhang P, Hu J, Bai C: Expression of aquaporin 5 increases proliferation and metastasis potential of lung cancer. J Pathol. 2010, 221 (2): 210-220. 10.1002/path.2702.CrossRefPubMed Zhang Z, Chen Z, Song Y, Zhang P, Hu J, Bai C: Expression of aquaporin 5 increases proliferation and metastasis potential of lung cancer. J Pathol. 2010, 221 (2): 210-220. 10.1002/path.2702.CrossRefPubMed
20.
go back to reference World Health Organization classification of tumors. Pathology and genetics. Tumours of the lung, pleura, thymus and heart. 2004, Lyon: IARC Press World Health Organization classification of tumors. Pathology and genetics. Tumours of the lung, pleura, thymus and heart. 2004, Lyon: IARC Press
21.
go back to reference Kuner R, Muley T, Meister M, Ruschhaupt M, Buness A, Xu EC, Schnabel P, Warth A, Poustka A, Sultmann H, Hoffmann H: Global gene expression analysis reveals specific patterns of cell junctions in non-small cell lung cancer subtypes. Lung Cancer. 2008 Kuner R, Muley T, Meister M, Ruschhaupt M, Buness A, Xu EC, Schnabel P, Warth A, Poustka A, Sultmann H, Hoffmann H: Global gene expression analysis reveals specific patterns of cell junctions in non-small cell lung cancer subtypes. Lung Cancer. 2008
22.
go back to reference Beer DG, Kardia SL, Huang CC, Giordano TJ, Levin AM, Misek DE, Lin L, Chen G, Gharib TG, Thomas DG, Lizyness ML, Kuick R, Hayasaka S, Taylor JM, Ianettoni MD, Orringer MB, Hanash S: Gene-expression profiles predict survival of patients with lung adenocarcinoma. Nat Med. 2002, 8 (8): 816-824.PubMed Beer DG, Kardia SL, Huang CC, Giordano TJ, Levin AM, Misek DE, Lin L, Chen G, Gharib TG, Thomas DG, Lizyness ML, Kuick R, Hayasaka S, Taylor JM, Ianettoni MD, Orringer MB, Hanash S: Gene-expression profiles predict survival of patients with lung adenocarcinoma. Nat Med. 2002, 8 (8): 816-824.PubMed
23.
go back to reference Bhattacharjee A, Richards WG, Staunton J, Li C, Monti S, Vasa P, Ladd C, Beheshti J, Bueno R, Gillette M, Loda M, Weber G, Mark EJ, Lander ES, Wong W, Johnson BE, Golub TR, Sugarbaker DJ, Meyerson M: Classification of human lung carcinomas by mRNA expression profiling reveals distinct adenocarcinoma subclasses. Proc Natl Acad Sci USA. 2001, 98 (24): 13790-13795. 10.1073/pnas.191502998.CrossRefPubMedPubMedCentral Bhattacharjee A, Richards WG, Staunton J, Li C, Monti S, Vasa P, Ladd C, Beheshti J, Bueno R, Gillette M, Loda M, Weber G, Mark EJ, Lander ES, Wong W, Johnson BE, Golub TR, Sugarbaker DJ, Meyerson M: Classification of human lung carcinomas by mRNA expression profiling reveals distinct adenocarcinoma subclasses. Proc Natl Acad Sci USA. 2001, 98 (24): 13790-13795. 10.1073/pnas.191502998.CrossRefPubMedPubMedCentral
24.
go back to reference Garber ME, Troyanskaya OG, Schluens K, Petersen S, Thaesler Z, Pacyna-Gengelbach M, van de Rijn M, Rosen GD, Perou CM, Whyte RI, Altman RB, Brown PO, Botstein D, Petersen I: Diversity of gene expression in adenocarcinoma of the lung. Proc Natl Acad Sci USA. 2001, 98 (24): 13784-13789. 10.1073/pnas.241500798.CrossRefPubMedPubMedCentral Garber ME, Troyanskaya OG, Schluens K, Petersen S, Thaesler Z, Pacyna-Gengelbach M, van de Rijn M, Rosen GD, Perou CM, Whyte RI, Altman RB, Brown PO, Botstein D, Petersen I: Diversity of gene expression in adenocarcinoma of the lung. Proc Natl Acad Sci USA. 2001, 98 (24): 13784-13789. 10.1073/pnas.241500798.CrossRefPubMedPubMedCentral
25.
go back to reference Lee ES, Son DS, Kim SH, Lee J, Jo J, Han J, Kim H, Lee HJ, Choi HY, Jung Y, Park M, Lim YS, Kim K, Shim Y, Kim BC, Lee K, Huh N, Ko C, Park K, Lee JW, Choi YS, Kim J: Prediction of recurrence-free survival in postoperative non-small cell lung cancer patients by using an integrated model of clinical information and gene expression. Clin Cancer Res. 2008, 14 (22): 7397-7404. 10.1158/1078-0432.CCR-07-4937.CrossRefPubMed Lee ES, Son DS, Kim SH, Lee J, Jo J, Han J, Kim H, Lee HJ, Choi HY, Jung Y, Park M, Lim YS, Kim K, Shim Y, Kim BC, Lee K, Huh N, Ko C, Park K, Lee JW, Choi YS, Kim J: Prediction of recurrence-free survival in postoperative non-small cell lung cancer patients by using an integrated model of clinical information and gene expression. Clin Cancer Res. 2008, 14 (22): 7397-7404. 10.1158/1078-0432.CCR-07-4937.CrossRefPubMed
26.
go back to reference Buness A, Kuner R, Ruschhaupt M, Poustka A, Sultmann H, Tresch A: Identification of aberrant chromosomal regions from gene expression microarray studies applied to human breast cancer. Bioinformatics. 2007, 23 (17): 2273-2280. 10.1093/bioinformatics/btm340.CrossRefPubMed Buness A, Kuner R, Ruschhaupt M, Poustka A, Sultmann H, Tresch A: Identification of aberrant chromosomal regions from gene expression microarray studies applied to human breast cancer. Bioinformatics. 2007, 23 (17): 2273-2280. 10.1093/bioinformatics/btm340.CrossRefPubMed
27.
go back to reference 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: 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. 2007, 85 (6): 1336-1346. 10.1002/jnr.21224.CrossRefPubMed 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: 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. 2007, 85 (6): 1336-1346. 10.1002/jnr.21224.CrossRefPubMed
28.
go back to reference Kato T, Miyamoto M, Kato K, Cho Y, Itoh T, Morikawa T, Okushiba S, Kondo S, Ohbuchi T, Katoh H: Difference of caveolin-1 expression pattern in human lung neoplastic tissue. Atypical adenomatous hyperplasia, adenocarcinoma and squamous cell carcinoma. Cancer Lett. 2004, 214 (1): 121-128. 10.1016/j.canlet.2004.04.017.CrossRefPubMed Kato T, Miyamoto M, Kato K, Cho Y, Itoh T, Morikawa T, Okushiba S, Kondo S, Ohbuchi T, Katoh H: Difference of caveolin-1 expression pattern in human lung neoplastic tissue. Atypical adenomatous hyperplasia, adenocarcinoma and squamous cell carcinoma. Cancer Lett. 2004, 214 (1): 121-128. 10.1016/j.canlet.2004.04.017.CrossRefPubMed
29.
go back to reference Chen SC, Lin CY, Chen YH, Fang HY, Cheng CY, Chang CW, Chen RA, Tai HL, Lee CH, Chou MC, Lin TS, Hsu LS: Aberrant promoter methylation of EDNRB in lung cancer in Taiwan. Oncol Rep. 2006, 15 (1): 167-172.PubMed Chen SC, Lin CY, Chen YH, Fang HY, Cheng CY, Chang CW, Chen RA, Tai HL, Lee CH, Chou MC, Lin TS, Hsu LS: Aberrant promoter methylation of EDNRB in lung cancer in Taiwan. Oncol Rep. 2006, 15 (1): 167-172.PubMed
30.
go back to reference Chen G, Wang H, Miller CT, Thomas DG, Gharib TG, Misek DE, Giordano TJ, Orringer MB, Hanash SM, Beer DG: Reduced selenium-binding protein 1 expression is associated with poor outcome in lung adenocarcinomas. J Pathol. 2004, 202 (3): 321-329. 10.1002/path.1524.CrossRefPubMed Chen G, Wang H, Miller CT, Thomas DG, Gharib TG, Misek DE, Giordano TJ, Orringer MB, Hanash SM, Beer DG: Reduced selenium-binding protein 1 expression is associated with poor outcome in lung adenocarcinomas. J Pathol. 2004, 202 (3): 321-329. 10.1002/path.1524.CrossRefPubMed
31.
go back to reference Cai D, Latham VM, Zhang X, Shapiro GI: Combined depletion of cell cycle and transcriptional cyclin-dependent kinase activities induces apoptosis in cancer cells. Cancer Res. 2006, 66 (18): 9270-9280. 10.1158/0008-5472.CAN-06-1758.CrossRefPubMed Cai D, Latham VM, Zhang X, Shapiro GI: Combined depletion of cell cycle and transcriptional cyclin-dependent kinase activities induces apoptosis in cancer cells. Cancer Res. 2006, 66 (18): 9270-9280. 10.1158/0008-5472.CAN-06-1758.CrossRefPubMed
32.
go back to reference Wang IC, Meliton L, Tretiakova M, Costa RH, Kalinichenko VV, Kalin TV: Transgenic expression of the forkhead box M1 transcription factor induces formation of lung tumors. Oncogene. 2008, 27 (30): 4137-4149. 10.1038/onc.2008.60.CrossRefPubMed Wang IC, Meliton L, Tretiakova M, Costa RH, Kalinichenko VV, Kalin TV: Transgenic expression of the forkhead box M1 transcription factor induces formation of lung tumors. Oncogene. 2008, 27 (30): 4137-4149. 10.1038/onc.2008.60.CrossRefPubMed
33.
go back to reference Takai N, Hamanaka R, Yoshimatsu J, Miyakawa I: Polo-like kinases (Plks) and cancer. Oncogene. 2005, 24 (2): 287-291. 10.1038/sj.onc.1208272.CrossRefPubMed Takai N, Hamanaka R, Yoshimatsu J, Miyakawa I: Polo-like kinases (Plks) and cancer. Oncogene. 2005, 24 (2): 287-291. 10.1038/sj.onc.1208272.CrossRefPubMed
34.
go back to reference Ceppi P, Volante M, Novello S, Rapa I, Danenberg KD, Danenberg PV, Cambieri A, Selvaggi G, Saviozzi S, Calogero R, Papotti M, Scagliotti GV: ERCC1 and RRM1 gene expressions but not EGFR are predictive of shorter survival in advanced non-small-cell lung cancer treated with cisplatin and gemcitabine. Ann Oncol. 2006, 17 (12): 1818-1825. 10.1093/annonc/mdl300.CrossRefPubMed Ceppi P, Volante M, Novello S, Rapa I, Danenberg KD, Danenberg PV, Cambieri A, Selvaggi G, Saviozzi S, Calogero R, Papotti M, Scagliotti GV: ERCC1 and RRM1 gene expressions but not EGFR are predictive of shorter survival in advanced non-small-cell lung cancer treated with cisplatin and gemcitabine. Ann Oncol. 2006, 17 (12): 1818-1825. 10.1093/annonc/mdl300.CrossRefPubMed
35.
go back to reference Xu H, Zhang Y, Wei W, Shen L, Wu W: Differential expression of aquaporin-4 in human gastric normal and cancer tissues. Gastroenterol Clin Biol. 2009, 33 (1 Pt 1): 72-76.CrossRefPubMed Xu H, Zhang Y, Wei W, Shen L, Wu W: Differential expression of aquaporin-4 in human gastric normal and cancer tissues. Gastroenterol Clin Biol. 2009, 33 (1 Pt 1): 72-76.CrossRefPubMed
36.
go back to reference McCoy E, Sontheimer H: Expression and function of water channels (aquaporins) in migrating malignant astrocytes. Glia. 2007, 55 (10): 1034-1043. 10.1002/glia.20524.CrossRefPubMedPubMedCentral McCoy E, Sontheimer H: Expression and function of water channels (aquaporins) in migrating malignant astrocytes. Glia. 2007, 55 (10): 1034-1043. 10.1002/glia.20524.CrossRefPubMedPubMedCentral
37.
go back to reference Bai C, Fukuda N, Song Y, Ma T, Matthay MA, Verkman AS: Lung fluid transport in aquaporin-1 and aquaporin-4 knockout mice. J Clin Invest. 1999, 103 (4): 555-561. 10.1172/JCI4138.CrossRefPubMedPubMedCentral Bai C, Fukuda N, Song Y, Ma T, Matthay MA, Verkman AS: Lung fluid transport in aquaporin-1 and aquaporin-4 knockout mice. J Clin Invest. 1999, 103 (4): 555-561. 10.1172/JCI4138.CrossRefPubMedPubMedCentral
38.
go back to reference Frigeri A, Nicchia GP, Svelto M: Aquaporins as targets for drug discovery. Curr Pharm Des. 2007, 13 (23): 2421-2427.CrossRefPubMed Frigeri A, Nicchia GP, Svelto M: Aquaporins as targets for drug discovery. Curr Pharm Des. 2007, 13 (23): 2421-2427.CrossRefPubMed
Metadata
Title
Loss of aquaporin-4 expression and putative function in non-small cell lung cancer
Authors
Arne Warth
Thomas Muley
Michael Meister
Esther Herpel
Anita Pathil
Hans Hoffmann
Philipp A Schnabel
Christian Bender
Andreas Buness
Peter Schirmacher
Ruprecht Kuner
Publication date
01-12-2011
Publisher
BioMed Central
Published in
BMC Cancer / Issue 1/2011
Electronic ISSN: 1471-2407
DOI
https://doi.org/10.1186/1471-2407-11-161

Other articles of this Issue 1/2011

BMC Cancer 1/2011 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine