X-ray structure of human aquaporin 2 and its implications for nephrogenic diabetes insipidus and trafficking

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 17, 2014, Pages 6305-6310

  Frick, Anna ^a   Eriksson, Urszula Kosinska ^a   De Mattia, Fabrizio ^b   Öberg, Fredrik ^a   Hedfalk, Kristina ^a   Neutze, Richard ^a   De Grip, Willem J ^c   Deen, Peter M T ^b   Törnroth Horsefield, Susanna ^a,d  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^d LUND UNIVERSITY   (Sweden)

Author keywords

Membrane protein; Water channel protein; X ray crystallography

Indexed keywords

AQUAPORIN 2; TETRAMER;

ALPHA HELIX; APICAL MEMBRANE; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL SELECTION; CONTROLLED STUDY; CRYSTALLIZATION; HUMAN; HYDROGEN BOND; MUTATION; NEPHROGENIC DIABETES INSIPIDUS; OOCYTE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; UBIQUITINATION; X RAY;

MEMBRANE PROTEIN; WATER CHANNEL PROTEIN; X-RAY CRYSTALLOGRAPHY;

AQUAPORIN 2; BINDING SITES; CADMIUM; CALCIUM; CRYSTALLOGRAPHY, X-RAY; DIABETES INSIPIDUS, NEPHROGENIC; ENDOPLASMIC RETICULUM; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; HUMANS; MODELS, MOLECULAR; OOCYTES; PROTEIN STRUCTURE, SECONDARY; PROTEIN TRANSPORT;

EID: 84899634495     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1321406111     Document Type: Article

References (52)

1. Verbalis JG (2003) Disorders of body water homeostasis. Best Pract Res Clin Endocrinol Metab 17(4):471-503.
2. van Os CH, Deen PM, Dempster JA (1994) Aquaporins: Water selective channels in biological membranes. Molecular structure and tissue distribution. Biochim Biophys Acta 1197(3):291-309.
3. Noda Y, Sohara E, Ohta E, Sasaki S (2010) Aquaporins in kidney pathophysiology. Nat Rev Nephrol 6(3):168-178.
4. Fushimi K, Sasaki S, Marumo F (1997) Phosphorylation of serine 256 is required for cAMP-dependent regulatory exocytosis of the aquaporin-2 water channel. J Biol Chem 272(23):14800-14804.
5. Katsura T, Gustafson CE, Ausiello DA, Brown D (1997) Protein kinase A phosphorylation is involved in regulated exocytosis of aquaporin-2 in transfected LLC-PK1 cells. Am J Physiol 272(6 Pt 2):F817-F822.
6. van Balkom BW, et al. (2002) The role of putative phosphorylation sites in the targeting and shuttling of the aquaporin-2 water channel. J Biol Chem 277(44): 41473-41479.
7. Fenton RA, et al. (2008) Acute regulation of aquaporin-2 phosphorylation at Ser-264 by vasopressin. Proc Natl Acad Sci USA 105(8):3134-3139.
8. Xie L, et al. (2010) Quantitative analysis of aquaporin-2 phosphorylation. Am J Physiol Renal Physiol 298(4):F1018-F1023.
9. Hoffert JD, et al. (2008) Vasopressin-stimulated increase in phosphorylation at Ser269 potentiates plasma membrane retention of aquaporin-2. J Biol Chem 283(36): 24617-24627.
10. Kamsteeg EJ, et al. (2006) Short-chain ubiquitination mediates the regulated endocytosis of the aquaporin-2 water channel. Proc Natl Acad Sci USA 103(48):18344-18349.
11. Katsura T, et al. (1995) Constitutive and regulated membrane expression of aquaporin 1 and aquaporin 2 water channels in stably transfected LLC-PK1 epithelial cells. Proc Natl Acad Sci USA 92(16):7212-7216.
12. Nielsen S, et al. (1995) Vasopressin increases water permeability of kidney collecting duct by inducing translocation of aquaporin-CD water channels to plasma membrane. Proc Natl Acad Sci USA 92(4):1013-1017.
13. Schrier RW, Fassett RG, Ohara M, Martin PY (1998) Vasopressin release, water channels, and vasopressin antagonism in cardiac failure, cirrhosis, and pregnancy. Proc Assoc Am Physicians 110(5):407-411.
14. Deen PM, et al. (1994) Requirement of human renal water channel aquaporin-2 for vasopressin-dependent concentration of urine. Science 264(5155):92-95.
15. Moeller HB, Rittig S, Fenton RA (2013) Nephrogenic diabetes insipidus: Essential insights into the molecular background and potential therapies for treatment. Endocr Rev 34(2):278-301.
16. Wesche D, Deen PM, Knoers NV (2012) Congenital nephrogenic diabetes insipidus: The current state of affairs. Pediatr Nephrol 27(12):2183-2204.
17. Werten PJ, et al. (2001) Large-scale purification of functional recombinant human aquaporin-2. FEBS Lett 504(3):200-205.
18. Schenk AD, et al. (2005) The 4.5 A structure of human AQP2. J Mol Biol 350(2): 278-289.
19. Horsefield R, et al. (2008) High-resolution x-ray structure of human aquaporin. Proc Natl Acad Sci USA 105(36):13327-13332.
20. Tajkhorshid E, et al. (2002) Control of the selectivity of the aquaporin water channel family by global orientational tuning. Science 296(5567):525-530.
21. Smart OS, Goodfellow JM, Wallace BA (1993) The pore dimensions of gramicidin A. Biophys J 65(6):2455-2460.
22. Sui H, Han BG, Lee JK, Walian P, Jap BK (2001) Structural basis of water-specific transport through the AQP1 water channel. Nature 414(6866):872-878.
23. Gonen T, et al. (2005) Lipid-protein interactions in double-layered two-dimensional AQP0 crystals. Nature 438(7068):633-638.
24. Harries WE, Akhavan D, Miercke LJ, Khademi S, Stroud RM (2004) The channel architecture of aquaporin 0 at a 2.2-A resolution. Proc Natl Acad Sci USA 101(39): 14045-14050.
25. van Balkom BW, et al. (2004) Role of cytoplasmic termini in sorting and shuttling of the aquaporin-2 water channel. Am J Physiol Cell Physiol 286(2):C372-C379.
26. Törnroth-Horsefield S, et al. (2006) Structural mechanism of plant aquaporin gating. Nature 439(7077):688-694.
27. Nyblom M, et al. (2009) Structural and functional analysis of SoPIP2;1 mutants adds insight into plant aquaporin gating. J Mol Biol 387(3):653-668.
28. Maurel C (2007) Plant aquaporins: Novel functions and regulation properties. FEBS Lett 581(12):2227-2236.
29. Canfield MC, Tamarappoo BK, Moses AM, Verkman AS, Holtzman EJ (1997) Identification and characterization of aquaporin-2 water channel mutations causing nephrogenic diabetes insipidus with partial vasopressin response. Hum Mol Genet 6(11): 1865-1871.
30. Mulders SM, et al. (1997) New mutations in the AQP2 gene in nephrogenic diabetes insipidus resulting in functional but misrouted water channels. J Am Soc Nephrol 8(2): 242-248.
31. Marr N, et al. (2002) Cell-biologic and functional analyses of five new Aquaporin-2 missense mutations that cause recessive nephrogenic diabetes insipidus. J Am Soc Nephrol 13(9):2267-2277.
32. Marr N, Kamsteeg EJ, van Raak M, van Os CH, Deen PM (2001) Functionality of aquaporin-2 missense mutants in recessive nephrogenic diabetes insipidus. Pflugers Arch 442(1):73-77.
33. Hendriks G, et al. (2004) Glycosylation is important for cell surface expression of the water channel aquaporin-2 but is not essential for tetramerization in the endoplasmic reticulum. J Biol Chem 279(4):2975-2983.
34. Guyon C, et al. (2009) Characterization of D150E and G196D aquaporin-2 mutations responsible for nephrogenic diabetes insipidus: Importance of a mild phenotype. Am J Physiol Renal Physiol 297(2):F489-F498.
35. Iolascon A, et al. (2007) Characterization of two novel missense mutations in the AQP2 gene causing nephrogenic diabetes insipidus. Nephron, Physiol 105(3):33-41.
36. Ho JD, et al. (2009) Crystal structure of human aquaporin 4 at 1.8 A and its mechanism of conductance. Proc Natl Acad Sci USA 106(18):7437-7442.
37. Lin SH, et al. (2002) Two novel aquaporin-2 mutations responsible for congenital nephrogenic diabetes insipidus in Chinese families. J Clin Endocrinol Metab 87(6): 2694-2700.
38. Champigneulle A, Siga E, Vassent G, Imbert-Teboul M (1993) V2-like vasopressin receptor mobilizes intracellular Ca2+ in rat medullary collecting tubules. Am J Physiol 265(1 Pt 2):F35-F45.
39. Ecelbarger CA, Chou CL, Lolait SJ, Knepper MA, DiGiovanni SR (1996) Evidence for dual signaling pathways for V2 vasopressin receptor in rat inner medullary collecting duct. Am J Physiol 270(4 Pt 2):F623-F633.
40. Maeda Y, Han JS, Gibson CC, Knepper MA (1993) Vasopressin and oxytocin receptors coupled to Ca2+ mobilization in rat inner medullary collecting duct. Am J Physiol 265(1 Pt 2):F15-F25.
41. Star RA, Nonoguchi H, Balaban R, Knepper MA (1988) Calcium and cyclic adenosine monophosphate as second messengers for vasopressin in the rat inner medullary collecting duct. J Clin Invest 81(6):1879-1888.
42. Yip KP (2002) Coupling of vasopressin-induced intracellular Ca2+ mobilization and apical exocytosis in perfused rat kidney collecting duct. J Physiol 538(Pt 3):891-899.
43. Levine SD, Kachadorian WA, Levin DN, Schlondorff D (1981) Effects of trifluoperazine on function and structure of toad urinary bladder. Role of calmodulin vasopressinstimulation of water permeability. J Clin Invest 67(3):662-672.
44. Chou CL, et al. (2000) Regulation of aquaporin-2 trafficking by vasopressin in the renal collecting duct. Roles of ryanodine-sensitive Ca2+ stores and calmodulin. J Biol Chem 275(47):36839-36846.
45. Boone M, et al. (2010) The lysosomal trafficking regulator interacting protein-5 localizes mainly in epithelial cells. J Mol Histol 41(1):61-74.
46. van Balkom BW, et al. (2009) LIP5 interacts with aquaporin 2 and facilitates its lysosomal degradation. J Am Soc Nephrol 20(5):990-1001.
47. Skalicky JJ, et al. (2012) Interactions of the human LIP5 regulatory protein with endosomal sorting complexes required for transport. J Biol Chem 287(52):43910-43926.
48. Reichow SL, Gonen T (2008) Noncanonical binding of calmodulin to aquaporin-0: Implications for channel regulation. Structure 16(9):1389-1398.
49. Reichow SL, et al. (2013) Allosteric mechanism of water-channel gating by Ca2+-calmodulin. Nat Struct Mol Biol 20(9):1085-1092.
50. Noda Y, et al. (2004) Aquaporin-2 trafficking is regulated by PDZ-domain containing protein SPA-1. FEBS Lett 568(1-3):139-145.
51. Lu HA, et al. (2007) Heat shock protein 70 interacts with aquaporin-2 and regulates its trafficking. J Biol Chem 282(39):28721-28732.
52. Kamsteeg EJ, et al. (2007) MAL decreases the internalization of the aquaporin-2 water channel. Proc Natl Acad Sci USA 104(42):16696-16701.