Hypoxia-induced migration in pulmonary arterial smooth muscle cells requires calcium-dependent upregulation of aquaporin 1

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 303, Issue 4, 2012, Pages

  Leggett, Kyle ^a   Maylor, Julie ^a   Undem, Clark ^a   Lai, Ning ^a,b   Lu, Wenju ^a   Schweitzer, Kelly ^a   King, Landon S ^a   Myers, Allen C ^a   Sylvester, J T ^a   Sidhaye, Venkataramana ^a   Shimoda, Larissa A ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b GUANGZHOU MEDICAL UNIVERSITY   (China)

Author keywords

AQP1; Vascular smooth muscle

Indexed keywords

AQUAPORIN 1; CALCIUM; CATION CHANNEL; SMALL INTERFERING RNA;

ANIMAL CELL; AORTA; ARTERY MUSCLE; ARTICLE; BINDING SITE; CALCIUM BINDING; CALCIUM CELL LEVEL; CELL MIGRATION; CONTROLLED STUDY; CYTOPLASM; HYPOXIA; IMMUNOBLOTTING; IN VIVO STUDY; LUNG ALVEOLUS CELL; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PULMONARY ARTERY; RAT; REAL TIME POLYMERASE CHAIN REACTION; SMOOTH MUSCLE FIBER; UPREGULATION;

ANIMALS; AORTA; AQUAPORIN 1; CALCIUM; CELL HYPOXIA; CELL MOVEMENT; CELL PROLIFERATION; INTRACELLULAR SPACE; MALE; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; PULMONARY ARTERY; RATS; RATS, WISTAR; UP-REGULATION;

EID: 84865137448     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00130.2012     Document Type: Article

References (35)

1. Abreu-Rodriguez I, Sanchez Silva R, Martins AP, Soveral G, Toledo-Aral JJ, Lopez-Barneo J, Echevarria M. Functional and transcriptional induction of aquaporin-1 gene by hypoxia; analysis of promoter and role of HIF-1 α. PLoS One 6: e28385, 2011.
2. Abud EM, Maylor J, Undem C, Punjabi A, Zaiman AL, Myers AC, Sylvester JT, Semenza GL, Shimoda LA. Digoxin inhibits development of hypoxic pulmonary hypertension in mice. Proc Natl Acad Sci USA 109: 1239-1244, 2012.
3. Chen BB, Coon TA, Glasser JR, Mallampalli RK. Calmodulin antagonizes a calcium-activated SCF ubiquitin E3 ligase subunit, FBXL2, to regulate surfactant homeostasis. Mol Cell Biol 31: 1905-1920, 2011.
4. Conner MT, Conner AC, Bland CE, Taylor LH, Brown JE, Parri HR, Bill RM. Rapid aquaporin translocation regulates cellular water flow: the mechanism of hypotonicity-induced sub-cellular localization of the aquaporin 1 water channel. J Biol Chem 287: 11516-11525, 2012.
5. Cornfield DN, Stevens T, McMurtry IF, Abman SH, Rodman DM. Acute hypoxia increases cytosolic calcium in fetal pulmonary artery smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 265: L53-L56, 1993.
6. 2+-binding domain at the C terminus of AQP1. J Mol Biol 318: 1381-1394, 2002.
7. Hayashi S, Takahashi N, Kurata N, Yamaguchi A, Matsui H, Kato S, Takeuchi K. Involvement of aquaporin-1 in gastric epithelial cell migration during wound repair. Biochem Biophys Res Commun 386: 483-487, 2009.
8. Hu J, Verkman AS. Increased migration and metastatic potential of tumor cells expressing aquaporin water channels. FASEB J 20: 1892-1894, 2006.
9. Ishibashi K, Hara S, Kondo S. Aquaporin water channels in mammals. Clin Exp Nephrol 13: 107-117, 2009.
10. King LS, Nielsen S, Agre P. Aquaporin-1 water channel protein in lung: ontogeny, steroid-induced expression, and distribution in rat. J Clin Invest 97: 2183-2191, 1996.
11. Kreda SM, Gynn MC, Fenstermacher DA, Boucher RC, Gabriel SE. Expression and localization of epithelial aquaporins in the adult human lung. Am J Respir Cell Mol Biol 24: 224-234, 2001.
12. Leitch V, Agre P, King LS. Altered ubiquitination and stability of aquaporin-1 in hypertonic stress. Proc Natl Acad Sci USA 98: 2894-2898, 2001.
13. Monzani E, Bazzotti R, Perego C, La Porta CA. AQP1 is not only a water channel: it contributes to cell migration through Lin7/beta-catenin. PLoS One 4: e6167, 2009.
14. Nielsen S, King LS, Christensen BM, Agre P. Aquaporins in complex tissues. II. Subcellular distribution in respiratory and glandular tissues of rat. Am J Physiol Cell Physiol 273: C1549-C1561, 1997.
15. Papadopoulos MC, Saadoun S, Verkman AS. Aquaporins and cell migration. Pflügers Arch 456: 693-700, 2008.
16. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45, 2001.
17. Potthast R, Abbey-Hosch SE, Antos LK, Marchant JS, Kuhn M, Potter LR. Calcium-dependent dephosphorylation mediates the hyperosmotic and lysophosphatidic acid-dependent inhibition of natriuretic peptide receptor-B/guanylyl cyclase-B. J Biol Chem 279: 48513-48519, 2004.
18. Saadoun S, Papadopoulos MC, Hara-Chikuma M, Verkman AS. Impairment of angiogenesis and cell migration by targeted aquaporin-1 gene disruption. Nature 434: 786-792, 2005.
19. Vchannel and endothelin-1. Am J Physiol Lung Cell Mol Physiol 279: L262-L272, 2000.
20. Shanahan CM, Connolly DL, Tyson KL, Cary NR, Osbourn JK, Agre P, Weissberg PL. Aquaporin-1 is expressed by vascular smooth muscle cells and mediates rapid water transport across vascular cell membranes. J Vasc Res 36: 353-362, 1999.
21. Shimoda LA, Undem C. Interactions between calcium and reactive oxygen species in pulmonary arterial smooth muscle responses to hypoxia. Respir Physiol Neurobiol 174: 221-229, 2010.
22. Sidhaye VK, Schweitzer KS, Caterina MJ, Shimoda L, King LS. Shear stress regulates aquaporin-5 and airway epithelial barrier function. Proc Natl Acad Sci USA 105: 3345-3350, 2008.
23. Stenmark KR, McMurtry IF. Vascular remodeling versus vasoconstriction in chronic hypoxic pulmonary hypertension: a time for reappraisal? Circ Res 97: 95-98, 2005.
24. Stenmark KR, Meyrick B, Galie N, Mooi WJ, McMurtry IF. Animal models of pulmonary arterial hypertension: the hope for etiological discovery and pharmacological cure. Am J Physiol Lung Cell Mol Physiol 297: L1013-L1032, 2009.
25. Sylvester JT, Shimoda LA, Aaronson PI, Ward JP. Hypoxic pulmonary vasoconstriction. Physiol Rev 92: 367-520, 2012.
26. Tanaka A, Sakurai K, Kaneko K, Ogino J, Yagui K, Ishikawa K, Ishibashi T, Matsumoto T, Yokote K, Saito Y. The role of the hypoxiainducible factor 1 binding site in the induction of aquaporin-1 mRNA expression by hypoxia. DNA Cell Biol 30: 539-544, 2011.
27. Tie L, Lu N, Pan X, Pan Y, An Y, Gao J, Lin Y, Yu H, Li X. Hypoxia-induced up-regulation of aquaporin-1 protein in prostate cancer cells in a p38-dependent manner. Cell Physiol Biochem 29: 269-280, 2012.
28. 2+in pulmonary and cerebral arterial myocytes. Am J Physiol Lung Cell Mol Physiol 265: L591-L597, 1993.
29. Voelkel NF, Tuder RM. Hypoxia-induced pulmonary vascular remodeling: a model for what human disease? J Clin Invest 106: 733-738, 2000.
30. Wang J, Peng Q, Lin Q, Childress C, Carey D, Yang W. Calcium activates Nedd4 E3 ubiquitin ligases by releasing the C2 domain-mediated auto-inhibition. J Biol Chem 285: 12279-12288, 2010.
31. 2+entry. Am J Physiol Lung Cell Mol Physiol 288: L1059-L1069, 2005.
32. 2+in pulmonary arterial smooth muscle cells. Circ Res 98: 1528-1537, 2006.
33. +channel expression in pulmonary arterial myocytes. Am J Physiol Lung Cell Mol Physiol 294: L309-L318, 2008.
34. Yamamoto N, Yoneda K, Asai K, Sobue K, Tada T, Fujita Y, Katsuya H, Fujita M, Aihara N, Mase M, Yamada K, Miura Y, Kato T. Alterations in the expression of the AQP family in cultured rat astrocytes during hypoxia and reoxygenation. Brain Res Mol Brain Res 90: 26-38, 2001.
35. Zheng YM, Wang QS, Liu QH, Rathore R, Yadav V, Wang YX. Heterogeneous gene expression and functional activity of ryanodine receptors in resistance and conduit pulmonary as well as mesenteric artery smooth muscle cells. J Vasc Res 45: 469-479, 2008.