Functional vacuolar ATPase (V-ATPase) proton pumps traffic to the enterocyte brush border membrane and require CFTR

American Journal of Physiology - Cell Physiology

Volumn 305, Issue 9, 2013, Pages

  Collaco, Anne M ^a   Geibel, Peter ^a   Lee, Beth S ^b   Geibel, John P ^a   Ameen, Nadia A ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

cAMP regulated traffic; CFTR; Intestine; V ATPase

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CYCLIC AMP DEPENDENT PROTEIN KINASE ANCHORING PROTEIN; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; PROTON; PROTON PUMP; UNCLASSIFIED DRUG; VACUOLAR ADENOSINE TRIPHOSPHATE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BASOLATERAL MEMBRANE; BRUNNER GLAND; CELL MIGRATION; CELL POLARITY; CELLULAR DISTRIBUTION; CYTOPLASM; ENDOSOME; ENZYME ACTIVITY; ENZYME LOCALIZATION; HUMAN; HUMAN CELL; INTESTINE BRUSH BORDER MEMBRANE; MALE; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

CAMP-REGULATED TRAFFIC; CFTR; INTESTINE; V-ATPASE;

ANIMALS; CACO-2 CELLS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; ENTEROCYTES; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROVILLI; PROTEIN TRANSPORT; RATS; RATS, SPRAGUE-DAWLEY; VACUOLAR PROTON-TRANSLOCATING ATPASES;

EID: 84887002424     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00067.2013     Document Type: Article

References (93)

1. Ahmad A, Khundmiri SJ, Pribble F, Merchant ML, Ameen M, Klein JB, Levi M, Lederer ED. Role of vacuolar ATPase in the trafficking of renal type IIa sodium-phosphate cotransporter. Cell Physiol Biochem 27: 703-714, 2011.
2. al-Awqati Q, Barasch J, Landry D. Chloride channels of intracellular organelles and their potential role in cystic fibrosis. J Exp Biol 172: 245-266, 1992.
3. Allman E, Johnson D, Nehrke K. Loss of the apical V-ATPase a-subunit VHA-6 prevents acidification of the intestinal lumen during a rhythmic behavior in C. elegans. Am J Physiol Cell Physiol 297: C1071-C1081, 2009.
4. +-ATPase localization and activity via direct phosphorylation of the a subunit in kidney cells. J Biol Chem 285: 24676-24685, 2010.
5. Ameen N, Apodaca G. Defective CFTR apical endocytosis and enterocyte brush border in myosin VI-deficient mice. Traffic 8: 998-1006, 2007.
6. Ameen NA, Marino C, Salas PJ. cAMP-dependent exocytosis and vesicle traffic regulate CFTR and fluid transport in rat jejunum in vivo. Am J Physiol Cell Physiol 284: C429-C438, 2003.
7. Ameen NA, van Donselaar E, Posthuma G, de Jonge H, McLaughlin G, Geuze HJ, Marino C, Peters PJ. Subcellular distribution of CFTR in rat intestine supports a physiologic role for CFTR regulation by vesicle traffic. Histochem Cell Biol 114: 219-228, 2000.
8. Banerjee A, Shih T, Alexander EA, Schwartz JH. SNARE proteins regulate H(+)-ATPase redistribution to the apical membrane in rat renal inner medullary collecting duct cells. J Biol Chem 274: 26518-26522, 1999.
9. Barasch J, al-Awqati Q. Defective acidification of the biosynthetic pathway in cystic fibrosis. J Cell Sci Suppl 17: 229-233, 1993.
10. Barasch J, Kiss B, Prince A, Saiman L, Gruenert D, al-Awqati Q. Defective acidification of intracellular organelles in cystic fibrosis. Nature 352: 70-73, 1991.
11. Barriere H, Bagdany M, Bossard F, Okiyoneda T, Wojewodka G, Gruenert D, Radzioch D, Lukacs GL. Revisiting the role of cystic fibrosis transmembrane conductance regulator and counterion permeability in the pH regulation of endocytic organelles. Mol Biol Cell 20: 3125-3141, 2009.
12. 2+-releasing channel. J Cell Biol 162: 211-222, 2003.
13. Bilan F, Nacfer M, Fresquet F, Norez C, Melin P, Martin-Berge A, Costa de Beauregard MA, Becq F, Kitzis A, Thoreau V. Endosomal SNARE proteins regulate CFTR activity and trafficking in epithelial cells. Exp Cell Res 314: 2199-2211, 2008.
14. Biwersi J, Verkman AS. Functional CFTR in endosomal compartment of CFTR-expressing fibroblasts and T84 cells. Am J Physiol Cell Physiol 266: C149-C156, 1994.
15. + absorption increases survival and decreases the incidence of intestinal obstructions in cystic fibrosis mice. Am J Physiol Gastrointest Liver Physiol 296: G886-G898, 2009.
16. Breton S, Brown D. New insight into the regulation of V-ATPasedependent proton secretion. Am J Physiol Renal Physiol 292: F1-F10, 2007.
17. Brown D, Breton S. H(+)V-ATPase-dependent luminal acidification in the kidney collecting duct and the epididymis/vas deferens: vesicle recycling and transcytotic pathways. J Exp Biol 203: 137-145, 2000.
18. Brown D, Paunescu TG, Breton S, Marshansky V. Regulation of the V-ATPase in kidney epithelial cells: dual role in acid-base homeostasis and vesicle trafficking. J Exp Biol 212: 1762-1772, 2009.
19. +-ATPase activity in kidney proximal tubule. Cell Physiol Biochem 26: 563-576, 2010.
20. Castellani S, Guerra L, Favia M, Di Gioia S, Casavola V, Conese M. NHERF1 and CFTR restore tight junction organisation and function in cystic fibrosis airway epithelial cells: role of ezrin and the RhoA/ROCK pathway. Lab Invest 92: 1527-1540, 2012.
21. Chandy G, Grabe M, Moore HP, Machen TE. Proton leak and CFTR in regulation of Golgi pH in respiratory epithelial cells. Am J Physiol Cell Physiol 281: C908-C921, 2001.
22. Collaco A, Jakab R, Hegan P, Mooseker M, Ameen N. Alpha-AP-2 directs myosin VI-dependent endocytosis of cystic fibrosis transmembrane conductance regulator chloride channels in the intestine. J Biol Chem 285: 17177-17187, 2010.
23. Collaco A, Marathe J, Kohnke H, Kravstov D, Ameen N. Syntaxin 3 is necessary for cAMP-and cGMP-regulated exocytosis of CFTR: implications for enterotoxigenic diarrhea. Am J Physiol Cell Physiol 299: C1450-C1460, 2010.
24. Collaco AM, Jakab RL, Hoekstra N, Mitchell K, Brooks A, Ameen NA. Regulated traffic of anion transporters in mammalian Brunner's glands: a role for water and fluid transport. Am J Physiol Gastrointest Liver Physiol 305: G258-G275, 2013.
25. Curtis LM, Gluck S. Distribution of Rab GTPases in mouse kidney and comparison with vacuolar H+-ATPase. Nephron Physiol 100: 31-42, 2005.
26. Di A, Brown ME, Deriy LV, Li C, Szeto FL, Chen Y, Huang P, Tong J, Naren AP, Bindokas V, Palfrey HC, Nelson DJ. CFTR regulates phagosome acidification in macrophages and alters bactericidal activity. Nat Cell Biol 8: 933-944, 2006.
27. DiCiccio JE, Steinberg BE. Lysosomal pH and analysis of the counter ion pathways that support acidification. J Gen Physiol 137: 385-390, 2011.
28. Donowitz M, Mohan S, Zhu CX, Chen TE, Lin R, Cha B, Zachos NC, Murtazina R, Sarker R, Li X. NHE3 regulatory complexes. J Exp Biol 212: 1638-1646, 2009.
29. Drose S, Altendorf K. Bafilomycins and concanamycins as inhibitors of V-ATPases and P-ATPases. J Exp Biol 200: 1-8, 1997.
30. + secretion by cortical distal tubule. J Membr Biol 157: 193-201, 1997.
31. Frattini A, Orchard PJ, Sobacchi C, Giliani S, Abinun M, Mattsson JP, Keeling DJ, Andersson AK, Wallbrandt P, Zecca L, Notarangelo LD, Vezzoni P, Villa A. Defects in TCIRG1 subunit of the vacuolar proton pump are responsible for a subset of human autosomal recessive osteopetrosis. Nat Genet 25: 343-346, 2000.
32. Gawenis LR, Franklin CL, Simpson JE, Palmer BA, Walker NM, Wiggins TM, Clarke LL. cAMP inhibition of murine intestinal Na/H exchange requires CFTR-mediated cell shrinkage of villus epithelium. Gastroenterology 125: 1148-1163, 2003.
33. Geyer M, Fackler OT, Peterlin BM. Subunit H of the V-ATPase involved in endocytosis shows homology to beta-adaptins. Mol Biol Cell 13: 2045-2056, 2002.
34. Golin-Bisello F, Bradbury N, Ameen N. STa and cGMP stimulate CFTR translocation to the surface of villus enterocytes in rat jejunum and is regulated by protein kinase G. Am J Physiol Cell Physiol 289: C708-C716, 2005.
35. +-ATPase apical accumulation in kideny intercalated cells is regulated by PKA and AMP-activated protein kinase. Am J Physiol Renal Physiol 298: F1162-F1169, 2010.
36. Grubb BR. Ion transport across the murine intestine in the absence and presence of CFTR. Comp Biochem Physiol A Physiol 118: 277-282, 1997.
37. + exchanger regulatory factor isoform 1 overexpression modulates cystic fibrosis transmembrane conductance regulator (CFTR) expression and activity in human airway 16HBE14o-cells and rescues DeltaF508 CFTR functional expression in cystic fibrosis cells. J Biol Chem 280: 40925-40933, 2005.
38. 3 secretion in marine fish osmoregulation. Am J Physiol Regul Integr Comp Physiol 301: R1682-R1691, 2011.
39. Hiesinger PR, Fayyazuddin A, Mehta SQ, Rosenmund T, Schulze KL, Zhai RG, Verstreken P, Cao Y, Zhou Y, Kunz J, Bellen HJ. The v-ATPase V0 subunit a1 is required for a late step in synaptic vesicle exocytosis in Drosophila. Cell 121: 607-620, 2005.
40. Hurtado-Lorenzo A, Skinner M, El Annan J, Futai M, Sun-Wada GH, Bourgoin S, Casanova J, Wildeman A, Bechoua S, Ausiello DA, Brown D, Marshansky V. V-ATPase interacts with ARNO and Arf6 in early endosomes and regulates the protein degradative pathway. Nat Cell Biol 8: 124-136, 2006.
41. Huss M, Ingenhorst G, Konig S, Gassel M, Drose S, Zeeck A, Altendorf K, Wieczorek H. Concanamycin A, the specific inhibitor of V-ATPases, binds to the V(o) subunit c. J Biol Chem 277: 40544-40548, 2002.
42. Huss M, Wieczorek H. Inhibitors of V-ATPases: old and new players. J Exp Biol 212: 341-346, 2009.
43. Ikuma M, Binder HJ, Geibel J. Role of apical H-K exchange and basolateral K channel in the regulation of intracellular pH in rat distal colon crypt cells. J Membr Biol 166: 205-212, 1998.
44. Jakab RL, Collaco AM, Ameen NA. Cell-specific effects of luminal acid, bicarbonate, cAMP, and carbachol on transporter trafficking in the intestine. Am J Physiol Gastrointest Liver Physiol 303: G937-G950, 2012.
45. Jakab RL, Collaco AM, Ameen NA. Characterization of CFTR high expresser cells in the intestine. Am J Physiol Gastrointest Liver Physiol. First published July 18, 2013; doi:10.1152/ajpgi.00094.2013.
46. Jakab RL, Collaco AM, Ameen NA. Physiological relevance of cellspecific distribution patterns of CFTR, NKCC1, NBCe1, and NHE3 along the crypt-villus axis in the intestine. Am J Physiol Gastrointest Liver Physiol 300: G82-G98, 2011.
47. Jefferies KC, Cipriano DJ, Forgac M. Function, structure and regulation of the vacuolar (H+)-ATPases. Arch Biochem Biophys 476: 33-42, 2008.
48. Ji YJ, Choi KY, Song HO, Park BJ, Yu JR, Kagawa H, Song WK, Ahnn J. VHA-8, the E subunit of V-ATPase, is essential for pH homeostasis and larval development in C. elegans. FEBS Lett 580: 3161-3166, 2006.
49. +-ATPase cause renal tubular acidosis with sensorineural deafness. Nat Genet 21: 84-90, 1999.
50. Kato A, Romero MF. Regulation of electroneutral NaCl absorption by the small intestine. Annu Rev Physiol 73: 261-281, 2011.
51. +-ATPase subunit ATP6V0A2. Nat Genet 40: 32-34, 2008.
52. Kravtsov DV, Caputo C, Collaco A, Hoekstra N, Egan ME, Mooseker MS, Ameen NA. Myosin Ia is Required for CFTR brush border membrane trafficking and ion transport in the mouse small intestine. Traffic 13: 1072-1082, 2012.
53. Lee SK, Li W, Ryu SE, Rhim T, Ahnn J. Vacuolar (H+)-ATPases in Caenorhabditis elegans: what can we learn about giant H+ pumps from tiny worms? Biochim Biophys Acta 1797: 1687-1695, 2010.
54. Ma T, Thiagarajah JR, Yang H, Sonawane ND, Folli C, Galietta LJ, Verkman AS. Thiazolidinone CFTR inhibitor identified by high-throughput screening blocks cholera toxin-induced intestinal fluid secretion. J Clin Invest 110: 1651-1658, 2002.
55. + permeability in regulation of Golgi pH. JOP 2: 229-236, 2001.
56. +-ATPase in vesicular trafficking: targeting, regulation and function. Curr Opin Cell Biol 20: 415-426, 2008.
57. +-ATPase from a single vertebrate species. Cloning, gene expression and protein characterization of functionally distinct isoforms in Gallus gallus. Eur J Biochem 267: 4115-4126, 2000.
58. Musch MW, Arvans DL, Wang Y, Nakagawa Y, Solomaha E, Chang EB. Cyclic AMP-mediated endocytosis of intestinal epithelial NHE3 requires binding to synaptotagmin 1. Am J Physiol Gastrointest Liver Physiol 298: G203-G211, 2010.
59. +)-ATPase associates with and is phosphorylated by the 50-kDa polypeptide of the clathrin assembly protein AP-2. J Biol Chem 268: 9184-9186, 1993.
60. Nishi T, Forgac M. Molecular cloning and expression of three isoforms of the 100-kDa a subunit of the mouse vacuolar proton-translocating ATPase. J Biol Chem 275: 6824-6830, 2000.
61. +)-ATPases-nature's most versatile proton pumps. Nat Rev Mol Cell Biol 3: 94-103, 2002.
62. Oehlke O, Martin HW, Osterberg N, Roussa E. Rab11b and its effector Rip11 regulate the acidosis-induced traffic of V-ATPase in salivary ducts. J Cell Physiol 226: 638-651, 2011.
63. Oehlke O, Schlosshardt C, Feuerstein M, Roussa E. Acidosis-induced V-ATPase trafficking in salivary ducts is initiated by cAMP/PKA/CREB pathway via regulation of Rab11b expression. Int J Biochem Cell Biol 44: 1254-1265, 2012.
64. Pastor-Soler N, Beaulieu V, Litvin TN, Da Silva N, Chen Y, Brown D, Buck J, Levin LR, Breton S. Bicarbonate-regulated adenylyl cyclase (sAC) is a sensor that regulates pH-dependent V-ATPase recycling. J Biol Chem 278: 49523-49529, 2003.
65. Pastor-Soler NM, Hallows KR, Smolak C, Gong F, Brown D, Breton S. Alkaline pH-and cAMP-induced V-ATPase membrane accumulation is mediated by protein kinase A in epididymal clear cells. Am J Physiol Cell Physiol 294: C488-C494, 2008.
66. Paunescu TG, Ljubojevic M, Russo LM, Winter C, McLaughlin MM, Wagner CA, Breton S, Brown D. cAMP stimulates apical V-ATPase accumulation, microvillar elongation, and proton extrusion in kidney collecting duct A-intercalated cells. Am J Physiol Renal Physiol 298: F643-F654, 2010.
67. Peng SB, Li X, Crider BP, Zhou Z, Andersen P, Tsai SJ, Xie XS, Stone DK. Identification and reconstitution of an isoform of the 116-kDa subunit of the vacuolar proton translocating ATPase. J Biol Chem 274: 2549-2555, 1999.
68. Peri F, Nusslein-Volhard C. Live imaging of neuronal degradation by microglia reveals a role for v0-ATPase a1 in phagosomal fusion in vivo. Cell 133: 916-927, 2008.
69. Peterson MD, Bement WM, Mooseker MS. An in vitro model for the analysis of intestinal brush border assembly. II. Changes in expression and localization of brush border proteins during cell contact-induced brush border assembly in Caco-2BBe cells. J Cell Sci 105: 461-472, 1993.
70. Peterson MD, Mooseker MS. Characterization of the enterocyte-like brush border cytoskeleton of the C2BBe clones of the human intestinal cell line, Caco-2. J Cell Sci 102: 581-600, 1992.
71. Picciano JA, Ameen N, Grant BD, Bradbury NA. Rme-1 regulates the recycling of the cystic fibrosis transmembrane conductance regulator. Am J Physiol Cell Physiol 285: C1009-C1018, 2003.
72. Pietrement C, Sun-Wada GH, Silva ND, McKee M, Marshansky V, Brown D, Futai M, Breton S. Distinct expression patterns of different subunit isoforms of the V-ATPase in the rat epididymis. Biol Reprod 74: 185-194, 2006.
73. Poschet JF, Fazio JA, Timmins GS, Ornatowski W, Perkett E, Delgado M, Deretic V. Endosomal hyperacidification in cystic fibrosis is due to defective nitric oxide-cylic GMP signalling cascade. EMBO Rep 7: 553-559, 2006.
74. Pratha VS, Hogan DL, Martensson BA, Bernard J, Zhou R, Isenberg JI. Identification of transport abnormalities in duodenal mucosa and duodenal enterocytes from patients with cystic fibrosis. Gastroenterology 118: 1051-1060, 2000.
75. +-ATPases from rat small intestine brush-border membranes. Pflügers Arch 434: 495-498, 1997.
76. +-ATPase subunit Voa1 and Voa2 cooperatively regulate secretory vesicle acidification, transmitter uptake and storage. Mol Biol Cell 22: 3394-3409, 2011.
77. +-ATPases containing a1, a2, a3, or a4 (ATP6V0A1-4) subunit isoforms along the nephron. Cell Physiol Biochem 20: 109-120, 2007.
78. Seksek O, Biwersi J, Verkman AS. Evidence against defective trans-Golgi acidification in cystic fibrosis. J Biol Chem 271: 15542-15548, 1996.
79. Shum WW, Da Silva N, Brown D, Breton S. Regulation of luminal acidification in the male reproductive tract via cell-cell crosstalk. J Exp Biol 212: 1753-1761, 2009.
80. Silvis MR, Bertrand CA, Ameen N, Golin-Bisello F, Butterworth MB, Frizzell RA, Bradbury NA. Rab11b regulates the apical recycling of CFTR in polarized intestinal epithelial cells. Mol Biol Cell 20: 2337-2350, 2009.
81. +-ATPase prevent segregation of lysosomal-and secretory-pathway proteins. J Cell Sci 122: 3542-3553, 2009.
82. Stauber T, Jentsch TJ. Chloride in vesicular trafficking and function. Annu Rev Physiol 75: 453-477, 2013.
83. Stevens TH, Forgac M. Structure, function and regulation of the vacuolar (H+)-ATPase. Annu Rev Cell Dev Biol 13: 779-808, 1997.
84. +-dependent bile acid transporter: protein-protein interaction and intracellular trafficking. J Biol Chem 279: 16295-16300, 2004.
85. Sundaram U, Knickelbein RG, Dobbins JW. Mechanism of intestinal secretion: effect of cyclic AMP on rabbit ileal crypt and villus cells. Proc Natl Acad Sci USA 88: 6249-6253, 1991.
86. +-ATPase with the a3 isoform during osteoclast differentiation. J Biol Chem 278: 22023-22030, 2003.
87. Toyomura T, Oka T, Yamaguchi C, Wada Y, Futai M. Three subunit a isoforms of mouse vacuolar H(+)-ATPase. Preferential expression of the a3 isoform during osteoclast differentiation. J Biol Chem 275: 8760-8765, 2000.
88. Vandewalle A, Cluzeaud F, Peng KC, Bens M, Luchow A, Gunther W, Jentsch TJ. Tissue distribution and subcellular localization of the ClC-5 chloride channel in rat intestinal cells. Am J Physiol Cell Physiol 280: C373-C381, 2001.
89. Wagner CA, Finberg KE, Breton S, Marshansky V, Brown D, Geibel JP. Renal vacuolar-ATPase. Physiol Rev 84: 1263-1314, 2004.
90. Webster P, Vanacore L, Nairn AC, Marino CR. Subcellular localization of CFTR to endosomes in a ductal epithelium. Am J Physiol Cell Physiol 267: C340-C348, 1994.
91. Weisz OA. Organelle acidification and disease. Traffic 4: 57-64, 2003.
92. Wilschanski M, Durie PR. Patterns of GI disease in adulthood associated with mutations in the CFTR gene. Gut 56: 1153-1163, 2007.
93. + exchange. Annu Rev Physiol 67: 411-413, 2005.