Endosomal acidification by Na+/H+ exchanger NHE5 regulates TrkA cell-surface targeting and NGF-induced PI3K signaling

Molecular Biology of the Cell

Volumn 24, Issue 21, 2013, Pages 3435-3448

  Diering, Graham H ^a,b   Numata, Yuka ^a   Fan, Steven ^a   Church, John ^a   Numata, Masayuki ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

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

Author keywords

[No Author keywords available]

Indexed keywords

BAFILOMYCIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; NERVE GROWTH FACTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN TYROSINE KINASE A; SHORT HAIRPIN RNA; SODIUM PROTON EXCHANGE PROTEIN; SODIUM PROTON EXCHANGE PROTEIN NHE5; UNCLASSIFIED DRUG;

ACIDIFICATION; ANIMAL CELL; ARTICLE; BIOTINYLATION; BRAIN CELL; CELL SURFACE; CONTROLLED STUDY; ENDOSOME; ENZYME PHOSPHORYLATION; NERVE FIBER GROWTH; NEURITE; NONHUMAN; PC12 CELL; PH; PLASMID; PRIMARY CULTURE; PRIORITY JOURNAL; PROTEIN DEPLETION; RAT; SIGNAL TRANSDUCTION;

ACIDS; ANIMALS; BLOTTING, WESTERN; CELL MEMBRANE; CELLS, CULTURED; CEREBRAL CORTEX; ENDOSOMES; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HYDROGEN-ION CONCENTRATION; MICROSCOPY, FLUORESCENCE; NERVE GROWTH FACTOR; NEURITES; NEURONS; PC12 CELLS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RECEPTOR, TRKA; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SODIUM-HYDROGEN ANTIPORTER;

EID: 84887056932     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E12-06-0445     Document Type: Article

References (103)

1. Arimura N et al. (2009). Anterograde transport of TrkB in axons is mediated by direct interaction with Slp1 and Rab27. Dev Cell 16, 675-686.
2. Arimura N, Kaibuchi K. (2007). Neuronal polarity: from extracellular signals to intracellular mechanisms. Nat Rev Neurosci 8, 194-205. (Pubitemid 46294662)
3. Ascano M, Richmond A, Borden P., Kuruvilla R. (2009). Axonal targeting of Trk receptors via transcytosis regulates sensitivity to neurotrophin responses. J Neurosci 29, 11674-11685.
4. + exchanger (NHE5) highly expressed in brain. J Biol Chem 274, 4383-4388.
5. Baass PC, Di Guglielmo GM, Authier F, Posner BI, Bergeron J.J. (1995). Compartmentalized signal transduction by receptor tyrosine kinases. Trends Cell Biol 5, 465-470.
6. Bacac M, Fusco C, Planche A., Santodomingo J, Demaurex N, Leemann-Zakaryan R, Provero P., Stamenkovic I. (2011). Securin and separase modulate membrane traffic by affecting endosomal acidification. Traffic 12, 615-626.
7. + exchanger isoform 5 (NHE5) from human brain. J Biol Chem 274, 4377-4382.
8. Barbacid M (1994). The Trk family of neurotrophin receptors. J Neurobiol 25, 1386-1403. (Pubitemid 24325064)
9. Bernstein BW, Bamburg J.R. (2010). ADF/cofilin: a functional node in cell biology. Trends Cell Biol 20, 187-195.
10. Bradke F, Dotti C.G. (1998). Membrane traffic in polarized neurons. Biochim Biophys Acta 1404, 245-258. (Pubitemid 28375719)
11. Bray GE, Ying Z, Baillie L.D., Zhai R., Mulligan SJ, Verge VMK (2013). Extracellular pH and neuronal depolarization serve as dynamic switches to rapidly mobilize TrkA to the membrane of adult sensory neurons. J Neurosci 33, 8202-8215.
12. + exchanger Nhx1 regulates cellular pH to control vesicle trafficking. Mol Biol Cell 16, 1396-1405. (Pubitemid 40349573)
13. Casey JR, Grinstein S, Orlowski J. (2010). Sensors and regulators of intracellular pH. Nat Rev Mol Cell Biol 11, 50-61.
14. Chao MV (2003). Neurotrophins and their receptors: a convergence point for many signalling pathways. Nat Rev Neurosci 4, 299-309. (Pubitemid 37271375)
15. Chen ZY, Ieraci A, Tanowitz M., Lee F.S. (2005). A novel endocytic recycling signal distinguishes biological responses of Trk neurotrophin receptors. Mol Biol Cell 16, 5761-5772. (Pubitemid 41752224)
16. Clague MJ, Urbe S, Aniento F., Gruenberg J. (1994). Vacuolar ATPase activity is required for endosomal carrier vesicle formation. J Biol Chem 269, 21-24. (Pubitemid 24026612)
17. Counts SE, Nadeem M, Wuu J., Ginsberg SD, Saragovi HU, Mufson EJ (2004). Reduction of cortical TrkA but not p75NTR protein in early-stage Alzheimer's disease. Ann Neurol 56, 520-531. (Pubitemid 39319342)
18. Cox GA, Lutz CM, Yang C.L., Biemesderfer D., Bronson RT, Fu A, Aronson PS, Noebels J.L., Frankel W.N. (1997). Sodium/hydrogen exchanger gene defect in slow-wave epilepsy mutant mice. Cell 91, 139-148. (Pubitemid 27431320)
19. Dent EW, Gertler F.B. (2003). Cytoskeletal dynamics and transport in growth cone motility and axon guidance. Neuron 40, 209-227. (Pubitemid 37244093)
20. +-ATPase (V-ATPase) activity in yeast generates an iron deprivation signal that is moderated by induction of the peroxiredoxin TSA2. J Biol Chem 288, 11366-11377.
21. + exchanger NHE5. J Biol Chem 284, 13892-13903.
22. + exchanger NHE5. Mol Biol Cell 22, 2246-2257.
23. Dobrowolski R, Vick P, Ploper D., Gumper I, Snitkin H, Sabatini D.D., De Robertis EM (2012). Presenilin deficiency or lysosomal inhibition enhances Wnt signaling through relocalization of GSK3 to the late-endosomal compartment. Cell Rep 2, 1316-1328.
24. + exchangers. Mol Aspects Med 34, 236-251.
25. + exchanger 3 accumulates and is functional in recycling endosomes. J Biol Chem 273, 2035-2043. (Pubitemid 28069250)
26. Flinn RJ, Yan Y, Goswami S., Parker PJ, Backer J.M. (2010). The late endosome is essential for mTORC1 signaling. Mol Biol Cell 21, 833-841.
27. Forgac M (2007). Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology. Nat Rev Mol Cell Biol 8, 917-929. (Pubitemid 47622561)
28. Frantz C, Barreiro G, Dominguez L., Chen X, Eddy R, Condeelis J., Kelly MJ, Jacobson M P, Barber D.L. (2008). Cofilin is a pH sensor for actin free barbed end formation: role of phosphoinositide binding. J Cell Biol 183, 865-879.
29. Fujioka Y, Tsuda M, Hattori T., Sasaki J, Sasaki T, Miyazaki T., Ohba Y. (2011). The Ras-PI3K signaling pathway is involved in clathrin-independent endocytosis and the internalization of influenza viruses. PLoS One 6, e16324.
30. Gagescu R, Demaurex N, Parton R.G., Hunziker W., Huber LA, Gruenberg J. (2000). The recycling endosome of Madin-Darby canine kidney cells is a mildly acidic compartment rich in raft components. Mol Biol Cell 11, 2775-2791. (Pubitemid 30645042)
31. Garcia-Regalado A., Guzman-Hernandez ML, Ramirez-Rangel I, Robles-Molina E, Balla T, Vazquez-Prado J, Reyes-Cruz G (2008). G protein-coupled receptor-promoted trafficking of Gbeta1gamma2 leads to AKT activation at endosomes via a mechanism mediated by Gbeta1gamma2-Rab11a interaction. Mol Biol Cell 19, 4188-4200.
32. Golachowska MR, Hoekstra D, van IJzendoorn IS (2010). Recycling endosomes in apical plasma membrane domain formation and epithelial cell polarity. Trends Cell Biol 20, 618-626.
33. Grant BD, Donaldson J.G. (2009). Pathways and mechanisms of endocytic recycling. Nat Rev Mol Cell Biol 10, 597-608.
34. Greene LA, Tischler A.S. (1976). Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc Natl Acad Sci USA 73, 2424-2428.
35. Grimes ML, Zhou J, Beattie E.C., Yuen EC, Hall DE, Valletta JS, Topp K.S., LaVail JH, Bunnett NW, Mobley W.C. (1996). Endocytosis of activated TrkA: evidence that nerve growth factor induces formation of signaling endosomes. J Neurosci 16, 7950-7964. (Pubitemid 26405058)
36. Habauzit D, Flouriot G, Pakdel F., Saligaut C. (2011). Effects of estrogens and endocrine-disrupting chemicals on cell differentiation-survival- proliferation in brain: contributions of neuronal cell lines. J Toxicol Environ Health B Crit Rev 14, 300-327.
37. Harrill JA, Mundy W.R. (2011). Quantitative assessment of neurite outgrowth in PC12 cells. Methods Mol Biol 758, 331-348.
38. Harrington AW, St Hillaire C, Zweifel LS, Glebova N.O., Philippidou P., Halegoua S, Ginty D.D. (2011). Recruitment of actin modifiers to TrkA endosomes governs retrograde NGF signaling and survival. Cell 146, 421-434.
39. Hsu VW, Prekeris R. (2010). Transport at the recycling endosome. Curr Opin Cell Biol 22, 528-534.
40. Huang EJ, Reichardt L.F. (2001). Neurotrophins: roles in neuronal development and function. Annu Rev Neurosci 24, 677-736. (Pubitemid 32695243)
41. Huotari J, Helenius A. (2011). Endosome maturation. EMBO J 30, 3481-3500.
42. Hurtado-Lorenzo A et al. (2006). V-ATPase interacts with ARNO and Arf6 in early endosomes and regulates the protein degradative pathway. Nat Cell Biol 8, 124-136.
43. Jewell JL, Russell RC, Guan K.L. (2013). Amino acid signalling upstream of mTOR. Nat Rev Mol Cell Biol 14, 133-139.
44. Joffre C, Barrow R, Menard L., Calleja V, Hart IR, Kermorgant S. (2011). A direct role for Met endocytosis in tumorigenesis. Nat Cell Biol 13, 827-837.
45. Jullien J, Guili V, Reichardt L.F., Rudkin B.B. (2002). Molecular kinetics of nerve growth factor receptor trafficking and activation. J Biol Chem 277, 38700-38708. (Pubitemid 35154731)
46. Kozik P, Hodson NA, Sahlender D.A., Simecek N., Soromani C, Wu J, Collinson L.M., Robinson M.S. (2013). A human genome-wide screen for regulators of clathrin-coated vesicle formation reveals an unexpected role for the V-ATPase. Nat Cell Biol 15, 50-60.
47. Kuruvilla R, Zweifel LS, Glebova N.O., Lonze BE, Valdez G, Ye H, Ginty D.D. (2004). A neurotrophin signaling cascade coordinates sympathetic neuron development through differential control of TrkA trafficking and retrograde signaling. Cell 118, 243-255. (Pubitemid 38962579)
48. Ledesma MD, Dotti C.G. (2003). Membrane and cytoskeleton dynamics during axonal elongation and stabilization. Int Rev Cytol 227, 183-219. (Pubitemid 37128651)
49. Li X, Difiglia M. (2012). The recycling endosome and its role in neurological disorders. Prog Neurobiol 97, 127-141.
50. Lin DC, Quevedo C, Brewer N.E., Bell A., Testa JR, Grimes ML, Miller FD, Kaplan D.R. (2006). APPL1 associates with TrkA and GIPC1 and is required for nerve growth factor-mediated signal transduction. Mol Cell Biol 26, 8928-8941. (Pubitemid 44851950)
51. + exchanger NHE7 by a novel binding module. Cell Signal 19, 978-988. (Pubitemid 46436437)
52. Liu Y, Zaun HC, Orlowski J, Ackerman S.L. (2013). CHP1-mediated NHE1 biosynthetic maturation is required for Purkinje cell axon homeostasis. J Neurosci 33, 12656-12669.
53. Lowery LA, Van Vactor D (2009). The trip of the tip: understanding the growth cone machinery. Nat Rev Mol Cell Biol 10, 332-343.
54. + exchanger NHE5 is sorted to discrete intracellular vesicles in the central and peripheral nervous systems. In: Sodium Calcium Exchange: A Growing Spectrum of Pathophysiological Implications, ed. L Annunziato, New York: Springer, 397-410.
55. Magalhaes MA, Larson DR, Mader C.C., Bravo-Cordero JJ, Gil-Henn H, Oser M., Chen X, Koleske AJ, Condeelis J. (2011). Cortactin phosphorylation regulates cell invasion through a pH-dependent pathway. J Cell Biol 195, 903-920.
56. +-ATPase in vesicular trafficking: targeting, regulation and function. Curr Opin Cell Biol 20, 415-426.
57. Martin TF, Grishanin R.N. (2003). PC12 cells as a model for studies of regulated secretion in neuronal and endocrine cells. Methods Cell Biol 71, 267-286.
58. + exchanger. Eur J Med Chem 38, 547-554. (Pubitemid 36773859)
59. Maxfield FR, McGraw T.E. (2004). Endocytic recycling. Nat Rev Mol Cell Biol 5, 121-132. (Pubitemid 38160255)
60. Meldolesi J (2011). Neurite outgrowth: this process, first discovered by Santiago Ramon y Cajal, is sustained by the exocytosis of two distinct types of vesicles. Brain Res Rev 66, 246-255.
61. Mellman I, Fuchs R, Helenius A. (1986). Acidification of the endocytic and exocytic pathways. Annu Rev Biochem 55, 663-700. (Pubitemid 16070784)
62. Miaczynska M, Pelkmans L, Zerial M. (2004). Not just a sink: endosomes in control of signal transduction. Curr Opin Cell Biol 16, 400-406. (Pubitemid 38903146)
63. Murphy JE, Padilla BE, Hasdemir B, Cottrell G.S., Bunnett N.W. (2009). Endosomes: a legitimate platform for the signaling train. Proc Natl Acad Sci USA 106, 17615-17622.
64. Nakayama M et al. (2013). Spatial regulation of VEGF receptor endocytosis in angiogenesis. Nat Cell Biol 15, 249-260.
65. Nazarewicz RR, Salazar G, Patrushev N., San Martin A, Hilenski L, Xiong S., Alexander R.W. (2011). Early endosomal antigen 1 (EEA1) is an obligate scaffold for angiotensin II-induced, PKC-alpha-dependent Akt activation in endosomes. J Biol Chem 286, 2886-2895.
66. + exchanger NHE6 in the endosomal recycling system is involved in the development of apical bile canalicular surface domains in HepG2 cells. Mol Biol Cell 21, 1293-1304.
67. Palamidessi A, Frittoli E, Garre M., Faretta M, Mione M, Testa I., Diaspro A, Lanzetti L, Scita G., Di Fiore PP (2008). Endocytic trafficking of Rac is required for the spatial restriction of signaling in cell migration. Cell 134, 135-147. (Pubitemid 351905741)
68. Parachoniak CA, Luo Y, Abella J.V., Keen JH, Park M. (2011). GGA3 functions as a switch to promote Met receptor recycling, essential for sustained ERK and cell migration. Dev Cell 20, 751-763.
69. Platta HW, Stenmark H. (2011). Endocytosis and signaling. Curr Opin Cell Biol 23, 393-403.
70. Presley JF, Mayor S, McGraw T.E., Dunn KW, Maxfield F.R. (1997). Bafilomycin A1 treatment retards transferrin receptor recycling more than bulk membrane recycling. J Biol Chem 272, 13929-13936. (Pubitemid 27224837)
71. Puthenveedu MA, Lauffer B, Temkin P., Vistein R, Carlton P, Thorn K., Taunton J, Weiner OD, Parton R.G., von Zastrow M (2010). Sequence-dependent sorting of recycling proteins by actin-stabilized endosomal microdomains. Cell 143, 761-773.
72. Reichardt LF (2006). Neurotrophin-regulated signalling pathways. Philos Trans R Soc B Biol Sci 361, 1545-1564. (Pubitemid 44450210)
73. Sadowski L, Pilecka I, Miaczynska M. (2009). Signaling from endosomes: location makes a difference. Exp Cell Res 315, 1601-1609.
74. Sancak Y, Bar-Peled L, Zoncu R., Markhard AL, Nada S, Sabatini D.M. (2010). Ragulator-Rag complex targets mTORC1 to the lysosomal surface and is necessary for its activation by amino acids. Cell 141, 290-303.
75. Sann S, Wang Z, Brown H., Jin Y. (2009). Roles of endosomal trafficking in neurite outgrowth and guidance. Trends Cell Biol 19, 317-324.
76. Schenck A, Goto-Silva L, Collinet C., Rhinn M, Giner A, Habermann B., Brand M, Zerial M. (2008). The endosomal protein Appl1 mediates Akt substrate specificity and cell survival in vertebrate development. Cell 133, 486-497. (Pubitemid 351608689)
77. Scita G, Di Fiore PP (2010). The endocytic matrix. Nature 463, 464-473.
78. Scott CC, Gruenberg J. (2011). Ion flux and the function of endosomes and lysosomes: pH is just the start: the flux of ions across endosomal membranes influences endosome function not only through regulation of the luminal pH. Bioessays 33, 103-110.
79. Sigismund S, Argenzio E, Tosoni D., Cavallaro E, Polo S, Di Fiore PP (2008). Clathrin-mediated internalization is essential for sustained EGFR signaling but dispensable for degradation. Dev Cell 15, 209-219.
80. + exchanger NHE1. J Neurosci 29, 8946-8959.
81. Slessareva JE, Routt SM, Temple B, Bankaitis V.A., Dohlman H.G. (2006). Activation of the phosphatidylinositol 3-kinase Vps34 by a G protein α subunit at the endosome. Cell 126, 191-203.
82. - indicator: evidence for chloride accumulation during acidification. J Biol Chem 277, 5506-5513. (Pubitemid 34968601)
83. Sorkin A, von Zastrow M (2009). Endocytosis and signalling: intertwining molecular networks. Nat Rev Mol Cell Biol 10, 609-622.
84. Steinberg F, Heesom KJ, Bass M.D., Cullen P.J. (2012). SNX17 protects integrins from degradation by sorting between lysosomal and recycling pathways. J Cell Biol 197, 219-230.
85. Straube T, von Mach T, Hönig E, Greb C., Schneider D, Jacob R. (2013). pH-dependent recycling of galectin-3 at the apical membrane of epithelial cells. Traffic 14, 1014-1027.
86. Straud S, Zubovych I, De Brabander JK, Roth M.G. (2010). Inhibition of iron uptake is responsible for differential sensitivity to V-ATPase inhibitors in several cancer cell lines. PLoS One 5, e11629.
87. + exchanger NHE5 isoform. Proc Natl Acad Sci USA 102, 2790-2795. (Pubitemid 40299871)
88. + exchanger isoform 5 stably expressed in Chinese hamster ovary cells. J Biol Chem 275, 6302-6307. (Pubitemid 30129922)
89. + exchanger NHE5 isoform. Regulation by phosphatidylinositol 3'-kinase and the actin cytoskeleton. J Biol Chem 277, 42623-42632. (Pubitemid 35285630)
90. Taelman VF, Dobrowolski R, Plouhinec J.L., Fuentealba LC, Vorwald P P, Gumper I, Sabatini D.D., De Robertis EM (2010). Wnt signaling requires sequestration of glycogen synthase kinase 3 inside multivesicular endosomes. Cell 143, 1136-1148.
91. Tsutsumi K, Fujioka Y, Tsuda M., Kawaguchi H, Ohba Y. (2009). Visualization of Ras-PI3K interaction in the endosome using BiFC. Cell Signal 21, 1672-1679.
92. Urbanska A, Sadowski L, Kalaidzidis Y., Miaczynska M. (2011). Biochemical characterization of APPL endosomes: the role of annexin A2 in APPL membrane recruitment. Traffic 12, 1227-1241.
93. Vaegter CB et al. (2011). Sortilin associates with Trk receptors to enhance anterograde transport and neurotrophin signaling. Nat Neurosci 14, 54-61.
94. Vanhaesebroeck B, Guillermet-Guibert J, Graupera M., Bilanges B. (2010). The emerging mechanisms of isoform-specific PI3K signalling. Nat Rev Mol Cell Biol 11, 329-341.
95. van Weert A.W., Dunn KW, Gueze H.J., Maxfield FR, Stoorvogel W. (1995). Transport from late endosomes to lysosomes, but not sorting of integral membrane proteins in endosomes, depends on the vacuolar proton pump. J Cell Biol 130, 821-834.
96. Varsano T, Dong MQ, Niesman I, Gacula H., Lou X, Ma T, Testa J.R., Yates JR 3rd, Farquhar MG (2006). GIPC is recruited by APPL to peripheral TrkA endosomes and regulates TrkA trafficking and signaling. Mol Cell Biol 26, 8942-8952. (Pubitemid 44851951)
97. Vaudry D, Stork PJ, Lazarovici P, Eiden L.E. (2002). Signaling pathways for PC12 cell differentiation: making the right connections. Science 296, 1648-1649. (Pubitemid 34579153)
98. Walz HA, Shi X, Chouinard M., Bue CA, Navaroli DM, Hayakawa A, Zhou Q.L., Nadler J., Leonard DM, Corvera S. (2010). Isoform-specific regulation of Akt signaling by the endosomal protein WDFY2. J Biol Chem 285, 14101-14108.
99. Wang E, Brown PS, Aroeti B, Chapin S.J., Mostov KE, Dunn K.W. (2000). Apical and basolateral endocytic pathways of MDCK cells meet in acidic common endosomes distinct from a nearly-neutral apical recycling endosome. Traffic 1, 480-493.
100. Weisz OA, Rodriguez-Boulan E (2009). Apical trafficking in epithelial cells: signals, clusters and motors. J Cell Sci 122, 4253-4266.
101. Winckler B, Mellman I. (2010). Trafficking guidance receptors. Cold Spring Harb Perspect Biol 2, a001826.
102. Xie C, Lovell MA, Xiong S, Kindy M.S., Guo J., Xie J, Amaranth V, Montine T.J., Markesbery W.R. (2001). Expression of glutathione-S-transferase isozyme in the SY5Y neuroblastoma cell line increases resistance to oxidative stress. Free Radic Biol Med 31, 73-81. (Pubitemid 32568426)
103. +-ATPase. Science 334, 678-683.