Insulin regulates alveolar epithelial function by inducing Na +/K+-ATPase translocation to the plasma membrane in a process mediated by the action of Akt

Journal of Cell Science

Volumn 123, Issue 8, 2010, Pages 1343-1351

  Comellas, Alejandro P ^a,b   Kelly, Aileen M ^a   Trejo, Humberto E ^a   Briva, Arturo ^a,c   Lee, Joyce ^a,d   Sznajder, Jacob I ^a   Dada, Laura A ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c DEPARTAMENTO DE BIOQUÍMICA   (Uruguay)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Akt; Alveolar epithelium; Na+ K+ ATPase

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ADENOSINE TRIPHOSPHATASE (POTASSIUM); INSULIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; RAB PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL FUNCTION; CELL MEMBRANE TRANSPORT; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; LUNG ALVEOLUS EPITHELIUM; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; RAT;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; BODY FLUIDS; CATTLE; CELL MEMBRANE; GTPASE-ACTIVATING PROTEINS; HUMANS; INSULIN; MALE; PNEUMOCYTES; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-AKT; RAB GTP-BINDING PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; SODIUM-POTASSIUM-EXCHANGING ATPASE; SUBCELLULAR FRACTIONS;

EID: 77951180355     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.066464     Document Type: Article

References (58)

1. Al-Khalili, L., Yu, M. and Chibalin, A. V. (2003). Na+,K+-ATPase trafficking in skeletal muscle: insulin stimulates translocation of both [alpha]1- and [alpha]2-subunit isoforms. FEBS Lett. 536, 198-202.
2. Babbey, C. M., Ahktar, N., Wang, E., Chen, C. C.-H., Grant, B. D. and Dunn, K. W. (2006). Rab10 regulates membrane transport through early endosomes of polarized madin-darby canine kidney cells. Mol. Biol. Cell 17, 3156-3175.
3. Bellmeyer, A., Martino, J. M., Chandel, N. S., Scott Budinger, G. R., Dean, D. A. and Mutlu, G. M. (2007). Leptin resistance protects mice from hyperoxia-induced acute lung injury. Am. J. Respir. Crit. Care Med. 175, 587-594.
4. Bertorello, A. M., Ridge, K. M., Chibalin, A. V., Katz, A. I. and Sznajder, J. I. (1999). Isoproterenol increases Na+-K+-ATPase activity by membrane insertion of alpha-subunits in lung alveolar cells. Am J. Physiol. Lung Cell Mol. Physiol. 276, L20-L27.
5. Bertorello, A. M., Komarova, Y., Smith, K., Leibiger, I. B., Efendiev, R., Pedemonte, C. H., Borisy, G. and Sznajder, J. I. (2003). Analysis of Na+,K+-ATPase motion and incorporation into the plasma membrane in response to G protein-coupled receptor signals in living cells. Mol. Biol. Cell 14, 1149-1157.
6. Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
7. Briva, A., Vadasz, I., Lecuona, E., Welch, L. C., Chen, J., Dada, L. A., Trejo, H. E., Dumasius, V., Azzam, Z. S., Myrianthefs, P. M. et al. (2007). High CO(2) levels impair alveolar epithelial function independently of pH. PLoS ONE 2, e1238.
8. Bruss, M. D., Arias, E. B., Lienhard, G. E. and Cartee, G. D. (2005). Increased phosphorylation of Akt substrate of 160 kDa (AS160) in rat skeletal muscle in response to insulin or contractile activity. Diabetes 54, 41-50.
9. Carranza, M. L., Rousselot, M., Chibalin, A. V., Bertorello, A. M., Favre, H. and Feraille, E. (1998). Protein kinase A induces recruitment of active Na+,K+-ATPase units to the plasma membrane of rat proximal convoluted tubule cells. J. Physiol. 511, 235-243.
10. Cong, L. N., Chen, H., Li, Y., Zhou, L., McGibbon, M. A., Taylor, S. I. and Quon, M. J. (1997). Physiological role of Akt in insulin-stimulated translocation of GLUT4 in transfected rat adipose cells. Mol. Endocrinol. 11, 1881-1890.
11. Dada, L. A., Chandel, N. S., Ridge, K. M., Pedemonte, C., Bertorello, A. M. and Sznajder, J. I. (2003). Hypoxia-induced endocytosis of Na,K-ATPase in alveolar epithelial cells is mediated by mitochondrial reactive oxygen species and PKC-zeta. J. Clin. Invest. 111, 1057-1064.
12. Dada, L. A., Novoa, E., Lecuona, E., Sun, H. and Sznajder, J. I. (2007). Role of the small GTPase RhoA in the hypoxia-induced decrease of plasma membrane Na,K-ATPase in A549 cells. J. Cell Sci. 120, 2214-2222.
13. Deachapunya, C., Palmer-Densmore, M. and O'Grady, S. M. (1999). Insulin stimulates transepithelial sodium transport by activation of a protein phosphatase that increases Na-K ATPase activity in endometrial epithelial cells. J. Gen. Physiol. 114, 561-574.
14. Eguez, L., Lee, A., Chavez, J. A., Mîinea, C. P., Kane, S., Lienhard, G. E. and McGraw, T. E. (2005). Full intracellular retention of GLUT4 requires AS160 Rab GTPase activating protein. Cell Metab. 2, 263-272.
15. Ewart, H. S. and Klip, A. (1995). Hormonal regulation of the Na(+)-K(+)-ATPase: mechanisms underlying rapid and sustained changes in pump activity. Am J. Physiol. Lung Cell Mol. Physiol. 269, C295-C311.
16. Feraille, E., Carranza, M. L., Gonin, S., Beguin, P., Pedemonte, C., Rousselot, M., Caverzasio, J., Geering, K., Martin, P.-Y. and Favre, H. (1999). Insulin-induced stimulation of Na+,K+-ATPase activity in kidney proximal tubule cells depends on phosphorylation of the alpha -subunit at Tyr-10. Mol. Biol. Cell 10, 2847-2859.
17. Gonzalez, E. and McGraw, T. E. (2006). Insulin signaling diverges into Akt-dependent and -independent signals to regulate the recruitment/docking and the fusion of GLUT4 vesicles to the plasma membrane. Mol. Biol. Cell 17, 4484-4493.
18. Gonzalez, E. and McGraw, T. E. (2009). Insulin-modulated Akt subcellular localization determines Akt isoform-specific signaling. Proc. Natl. Acad. Sci. USA 106, 7004-7009.
19. Ishikura, S. and Klip, A. (2008). Muscle cells engage Rab8A and myosin Vb in insulin-dependent GLUT4 translocation. Am J. Physiol. Cell Physiol. 295, C1016-C1025.
20. Ishikura, S., Bilan, P. J. and Klip, A. (2007). Rabs 8A and 14 are targets of the insulin-regulated Rab-GAP AS160 regulating GLUT4 traffic in muscle cells. Biochem. Biophys. Res. Commun. 353, 1074-1079.
21. Jordens, I., Marsman, M., Kuijl, C. and Neefjes, J. (2005). Rab proteins, connecting transport and vesicle fusion. Traffic 6, 1070-1077.
22. Junutula, J. R., De Maziere, A. M., Peden, A. A., Ervin, K. E., Advani, R. J., van Dijk, S. M., Klumperman, J. and Scheller, R. H. (2004). Rab14 is involved in membrane trafficking between the golgi complex and endosomes. Mol. Biol. Cell 15, 2218-2229.
23. Kane, S., Sano, H., Liu, S. C., Asara, J. M., Lane, W. S., Garner, C. C. and Lienhard, G. E. (2002). A method to identify serine kinase substrates. Akt phosphorylates a novel adipocyte protein with a Rab GTPase-activating protein (GAP) domain. J. Biol. Chem. 277, 22115-22118.
24. Klip, A. (2009). The many ways to regulate glucose transporter 4. Appl. Physiol. Nutr. Metab. 34, 481-487.
25. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
26. Lecuona, E., Garcia, A. and Sznajder, J. I. (2000). A novel role for protein phosphatase 2A in the dopaminergic regulation of Na,K-ATPase. FEBS Lett. 481, 217-220.
27. Lecuona, E., Dada, L. A., Sun, H., Butti, M. L., Zhou, G., Chew, T.-L. and Sznajder, J. I. (2006). Na,K-ATPase α1-subunit dephosphorylation by protein phosphatase 2A is necessary for its recruitment to the plasma membrane FASEB J. 20, 2618-2620.
28. Lecuona, E., Minin, A., Trejo, H. E., Chen, J., Comellas, A. P., Sun, H., Grillo, D., Nekrasova, O. E., Welch, L. C., Szleifer, I. et al. (2009a). Myosin-Va restrains the trafficking of Na+/K+-ATPase-containing vesicles in alveolar epithelial cells. J. Cell Sci. 122, 3915-3922.
29. Lecuona, E., Sun, H., Vohwinkel, C., Ciechanover, A. and Sznajder, J. I. (2009b). Ubiquitination participates in the lysosomal degradation of the Na,K-ATPase in steady-state conditions. Am. J. Respir. Cell Mol. Biol. 41, 671-679.
30. Lieber, M., Smith, B., Szakal, A., Nelson-Rees, W. and Todaro, G. (1976). A continuous tumor-cell line from a human lung carcinoma with properties of type II alveolar epithelial cells. Int. J. Cancer 17, 62-70.
31. Lingrel, J. B. and Kuntzweiler, T. (1994). Na+,K(+)-ATPase. J. Biol. Chem. 269, 19659-19662.
32. Matthay, M. A., Folkesson, H. G. and Verkman, A. S. (1996). Salt and water transport across alveolar and distal airway epithelia in the adult lung. Am J. Physiol. Lung Cell Mol. Physiol. 270, L487-L503.
33. McDonough, A. A., Geering, K. and Farley, R. A. (1990). The sodium pump needs its beta subunit. FASEB J. 4, 1598-1605.
34. Mîinea, C. P., Sano, H., Kane, S., Sano, E., Fukuda, M., Peranen, J., Lane, W. S. and Lienhard, G. E. (2005). AS160, the Akt substrate regulating GLUT4 translocation, has a functional Rab GTPase-activating protein domain. Biochem. J. 391, 87-93.
35. Mutlu, G. M. and Sznajder, J. I. (2005). Mechanisms of pulmonary edema clearance. Am J. Physiol. Lung Cell Mol. Physiol. 289, L685-L695.
36. Myrianthefs, P. M., Briva, A., Lecuona, E., Dumasius, V., Rutschman, D. H., Ridge, K. M., Baltopoulos, G. J. and Sznajder, J. I. (2005). Hypocapnic but not metabolic alkalosis impairs alveolar fluid reabsorption. Am. J. Respir. Crit. Care Med. 171, 1267-1271.
37. Ragolia, L., Cherpalis, B., Srinivasan, M. and Begum, N. (1997). Role of serine/threonine protein phosphatases in insulin regulation of Na+/K+-ATPase activity in cultured rat skeletal muscle cells. J. Biol. Chem. 272, 23653-23658.
38. Ridge, K. M., Rutschman, D. H., Factor, P., Katz, A. I., Bertorello, A. M. and Sznajder, J. I. (1997). Differential expression of Na-K-ATPase isoforms in rat alveolar epithelial cells. Am. J. Physiol. 273, L246-L255.
39. Ridge, K. M., Dada, L., Lecuona, E., Bertorello, A. M., Katz, A. I., Mochly-Rosen, D. and Sznajder, J. I. (2002). Dopamine-induced exocytosis of Na,K-ATPase is dependent on activation of protein kinase C-epsilon and -delta. Mol. Biol. Cell 13, 1381-1389.
40. Roach, W. G., Chavez, J. A., Mîinea, C. P. and Lienhard, G. E. (2007). Substrate specificity and effect on GLUT4 translocation of the Rab GTPase-activating protein Tbc1d1. Biochem. J. 403, 353-358.
41. Rosé, S. D., Lejen, L. C., Larson, R. E., Pene, T. D. and Trifaro, J. M. (2003). Myosins II and V in chromaffin cells: myosin V is a chromaffin vesicle molecular motor involved in secretion. J. Neurochem. 85, 287-298.
42. Rutschman, D. H., Olivera, W. and Sznajder, J. I. (1993). Active transport and passive liquid movement in isolated perfused rat lungs. J. Appl. Physiol. 75, 1574-1580.
43. Sakamoto, K. and Holman, G. D. (2008). Emerging role for AS160/TBC1D4 and TBC1D1 in the regulation of GLUT4 traffic. Am J. Physiol. Endocrinol. Metab. 295, E29-E37.
44. Saldias, F., Lecuona, E., Friedman, E., Barnard, M. L., Ridge, K. M. and Sznajder, J. I. (1998). Modulation of lung liquid clearance by isoproterenol in rat lungs. Am J. Physiol. Lung Cell Mol. Physiol. 274, L694-L701.
45. Saldias, F. J., Lecuona, E., Comellas, A. P., Ridge, K. M., Rutschman, D. H. and Sznajder, J. I. (2000). beta -adrenergic stimulation restores rat lung ability to clear edema in ventilator-associated lung injury. Am. J. Respir. Crit. Care Med. 162, 282-287.
46. Saldias, F. J., Azzam, Z. S., Ridge, K. M., Yeldandi, A., Rutschman, D. H., Schraufnagel, D. and Sznajder, J. I. (2001). Alveolar fluid reabsorption is impaired by increased left atrial pressures in rats. Am J. Physiol. Lung Cell Mol. Physiol. 281, L591-L597.
47. Saldias, F. J., Comellas, A. P., Pesce, L., Lecuona, E. and Sznajder, J. I. (2002). Dopamine increases lung liquid clearance during mechanical ventilation. Am J. Physiol. Lung Cell Mol. Physiol. 283, L136-L143.
48. Sano, H., Kane, S., Sano, E., Mîinea, C. P., Asara, J. M., Lane, W. S., Garner, C. W. and Lienhard, G. E. (2003). Insulin-stimulated phosphorylation of a Rab GTPase-activating protein regulates GLUT4 translocation. J. Biol. Chem. 278, 14599-14602.
49. Sano, H., Roach, W. G., Peck, G. R., Fukuda, M. and Lienhard, G. E. (2008). Rab10 in insulin-stimulated GLUT4 translocation. Biochem. J. 411, 89-95.
50. Shiojima, I. and Walsh, K. (2002). Role of Akt signaling in vascular homeostasis and angiogenesis. Circ. Res. 90, 1243-1250.
51. Sugahara, K., Freidenberg, G. R. and Mason, R. J. (1984). Insulin binding and effects on glucose and transepithelial transport by alveolar type II cells. Am. J. Physiol. 247, C472-C477.
52. Sweeney, G., Niu, W., Canfield, V. A., Levenson, R. and Klip, A. (2001). Insulin increases plasma membrane content and reduces phosphorylation of Na+-K+ pump alpha 1-subunit in HEK-293 cells. Am. J. Physiol. Lung Cell Mol. Physiol. 281, C1797-C1803.
53. Sznajder, J. I., Factor, P. and Ingbar, D. H. (2002). Lung edema clearance: 20 years of progress: invited review: Lung edema clearance: role of Na+-K+-ATPase. J. Appl. Physiol. 93, 1860-1866.
54. Taniguchi, C. M., Emanuelli, B. and Kahn, C. R. (2006). Critical nodes in signalling pathways: insights into insulin action. Nat. Rev. Mol. Cell. Biol. 7, 85-96.
55. Thong, F. S. L., Bilan, P. J. and Klip, A. (2007). The Rab GTPase-activating protein AS160 integrates Akt, protein kinase C, and AMP-activated protein kinase signals regulating GLUT4 traffic. Diabetes 56, 414-423.
56. Vadasz, I., Dada, L. A., Briva, A., Trejo, H. E., Welch, L. C., Chen, J., Toth, P. T., Lecuona, E., Witters, L. A., Schumacker, P. T. et al. (2008). AMP-activated protein kinase regulates CO2-induced alveolar epithelial dysfunction in rats and human cells by promoting Na,K-ATPase endocytosis. J. Clin. Invest. 118, 752-762.
57. Vinciguerra, M., Mordasini, D., Vandewalle, A. and Feraille, E. (2005). Hormonal and nonhormonal mechanisms of regulation of the NA,K-pump in collecting duct principal cells. Semin. Nephrol. 25, 312-321.
58. Whiteman, E. L., Cho, H. and Birnbaum, M. J. (2002). Role of Akt/protein kinase B in metabolism. Trends Endocrinol. Metab. 13, 444-451.