Characterization of the SAM domain of the PKD-related protein ANKS6 and its interaction with ANKS3

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• 作者：Catherine N Leettola (1)
  Mary Jane Knight (1)
  Duilio Cascio (1)
  Sigrid Hoffman (2)
  James U Bowie (1)
  
  1. Department of Chemistry and Biochemistry ; UCLA-DOE Institute of Genomics and Proteomics ; Molecular Biology Institute ; University of California ; Los Angeles ; Boyer Hall 611 Charles E. Young Dr. E ; Los Angeles ; California ; 90095-1570 ; USA
  2. Medical Research Centre ; Klinikum Mannheim ; University of Heidelberg ; D-68167 ; Mannheim ; Germany
  
• 关键词：Polycystic kidney disease ; Protein ; protein interaction ; Polymerization ; Crystal structure
• 刊名：BMC Structural Biology
• 出版年：2014
• 出版时间：December 2014
• 年：2014
• 卷：14
• 期：1
• 全文大小：2,472 KB
• 参考文献：1. Wilson, PD (2004) Polycystic kidney disease. N Engl J Med 350: pp. 151-164 CrossRef
  2. Chapin, HC, Caplan, MJ (2010) The cell biology of polycystic kidney disease. J Cell Biol 191: pp. 701-710 CrossRef
  3. Torres, VE, Harris, PC, Pirson, Y (2007) Autosomal dominant polycystic kidney disease. The Lancet 369: pp. 1287-1301 CrossRef
  4. Gabow, PA (1993) Autosomal dominant polycystic kidney disease. N Engl J Med 329: pp. 332-342 CrossRef
  5. Ariza, M, Alvarez, V, Marin, R, Aguado, S, L贸pez-Larrea, C, Alvarez, J, Men茅ndez, MJ, Coto, E (1997) A family with a milder form of adult dominant polycystic kidney disease not linked to the PKD1 (16p) or PKD2 (4q) genes. J Med Genet 34: pp. 587-589 CrossRef
  6. Hanaoka, K, Qian, F, Boletta, A, Bhunia, AK, Piontek, K, Tsiokas, L, Sukhatme, VP, Guggino, WB, Germino, GG (2000) Co-assembly of polycystin-1 and 鈭? produces unique cation-permeable currents. Nature 408: pp. 990-994 CrossRef
  7. Nagao, S, Kugita, M, Yoshihara, D, Yamaguchi, T (2012) Animal models for human polycystic kidney disease. Exp Anim 61: pp. 477-488 CrossRef
  8. Guay-Woodford, LM (2003) Murine models of polycystic kidney diease: molecular and therapeutic insights. Am J Physiol - Ren Physiol 285: pp. F1034-F1049 CrossRef
  9. Sch盲fer, K, Gretz, N, Bader, M, Oberb盲umer, I, Eckardt, K-U, Kriz, W, Bachmann, S (1994) Characterization of the Han:SPRD rat model for hereditary polycystic kidney disease. Kidney Int 46: pp. 134-152 CrossRef
  10. Gretz, N, Kr盲nzlin, B, Pey, R, Schieren, G, Bach, J, Oberm眉ller, N, Ceccherini, I, Kl枚ting, I, Rohemeiss, P, Bachmann, S, Hafner, M (1996) Rat models of autosomal dominant polycystic kidney disease. Nephrol Dial Transplant 11: pp. 46-51 CrossRef
  11. Brown, JH, Bihoreau, M-T, Hoffmann, S, Kr盲nzlin, B, Tychinskaya, I, Oberm眉ller, N, Podlich, D, Boehn, SN, Kaisaki, PJ, Megel, N, Danoy, P, Copley, RR, Broxholme, J, Witzgall, R, Lathrop, M, Gretz, N, Gauguier, D (2005) Missense mutation in sterile 伪 motif of novel protein samcystin is associated with polycystic kidney disease in (cy/+) rat. J Am Soc Nephrol 16: pp. 3517-3526 CrossRef
  12. Neudecker, S, Walz, R, Menon, K, Maier, E, Bihoreau, M-T, Oberm眉ller, N, Kr盲nzlin, B, Gretz, N, Hoffmann, SC (2010) Transgenic overexpression of Anks6(p.R823W) causes polycystic kidney disease in rats. Am J Pathol 177: pp. 3000-3009 CrossRef
  13. Hoff, S, Halbritter, J, Epting, D, Frank, V, Nguyen, T-MT, van Reeuwijk, J, Boehlke, C, Schell, C, Yasunaga, T, Helmst盲dter, M, Mergen, M, Filhol, E, Boldt, K, Horn, N, Ueffing, M, Otto, EA, Eisenberger, T, Elting, MW, van Wijk, JAE, Bockenhauer, D, Sebire, NJ, Rittig, S, Vyberg, M, Ring, T, Pohl, M, Pape, L, Neuhaus, TJ, Elshakhs, NAS, Koon, SJ, Harris, PC (2013) ANKS6 is a central component of a nephronophthisis module linking NEK8 to INVS and NPHP3. Nat Genet 45: pp. 951-956 CrossRef
  14. Qiao, F, Bowie, JU (2005) The many faces of SAM. Sci STKE 2005: pp. re7
  15. Kim, CA, Bowie, JU (2003) SAM domains: uniform structure, diversity of function. Trends Biochem Sci 28: pp. 625-628 CrossRef
  16. Harada, BT, Knight, MJ, Imai, S, Qiao, F, Ramachander, R, Sawaya, MR, Gingery, M, Sakane, F, Bowie, JU (2008) Regulation of enzyme localization by polymerization: polymer formation by the SAM domain of diacylglycerol kinase 未1. Structure 16: pp. 380-387 CrossRef
  17. Kim, CA, Gingery, M, Pilpa, RM, Bowie, JU (2002) The SAM domain of polyhomeotic forms a helical polymer. Nat Struct Biol 9: pp. 453-457
  18. Kim, CA, Phillips, ML, Kim, W, Gingery, M, Tran, HH, Robinson, MA, Faham, S, Bowie, JU (2001) Polymerization of the SAM domain of TEL in leukemogenesis and transcriptional repression. EMBO J 20: pp. 4173-4182 CrossRef
  19. Baron, MK, Boeckers, TM, Vaida, B, Faham, S, Gingery, M, Sawaya, MR, Salyer, D, Gundelfinger, ED, Bowie, JU (2006) An architectural framework that may lie at the core of the postsynaptic density. Science 311: pp. 531-535 CrossRef
  20. Stafford, RL, Hinde, E, Knight, MJ, Pennella, MA, Ear, J, Digman, MA, Gratton, E, Bowie, JU (2011) Tandem SAM domain structure of human Caskin1: a presynaptic, self-assembling scaffold for CASK. Structure 19: pp. 1826-1836 CrossRef
  21. Di Pietro, SM, Cascio, D, Feliciano, D, Bowie, JU, Payne, GS (2010) Regulation of clathrin adaptor function in endocytosis: novel role for the SAM domain. EMBO J 29: pp. 1033-1044 CrossRef
  22. Knight, MJ, Leettola, C, Gingery, M, Li, H, Bowie, JU (2011) A human sterile alpha motif domain polymerizome. Protein Sci 20: pp. 1697-1706 CrossRef
  23. Ramachander, R, Kim, CA, Phillips, ML, Mackereth, CD, Thanos, CD, McIntosh, LP, Bowie, JU (2002) Oligomerization-dependent Association of the SAM Domains from Schizosaccharomyces pombe Byr2 and Ste4. J Biol Chem 277: pp. 39585-39593 CrossRef
  24. Qiao, F, Song, H, Kim, CA, Sawaya, MR, Hunter, JB, Gingery, M, Rebay, I, Courey, AJ, Bowie, JU (2004) Derepression by depolymerization: structural insights into the regulation of Yan by Mae. Cell 118: pp. 163-173 CrossRef
  25. Kwan, JJ, Warner, N, Pawson, T, Donaldson, LW (2004) The solution structure of the S.cerevisiae Ste11 MAPKKK SAM Domain and its partnership with Ste50. J Mol Biol 342: pp. 681-693 CrossRef
  26. Grimshaw, SJ, Mott, HR, Stott, KM, Nielsen, PR, Evetts, KA, Hopkins, LJ, Nietlispach, D, Owen, D (2003) Structure of the sterile 伪 Motif (SAM) domain of the saccharomyces cerevisiae mitogen-activated protein kinase pathway-modulating protein STE50 and analysis of its interaction with the STE11 SAM. J Biol Chem 279: pp. 2192-2201 CrossRef
  27. Leone, M, Cellitti, J, Pellecchia, M (2009) The Sam domain of the lipid phosphatase Ship2 adopts a common model to interact with Arap3-Sam and EphA2-Sam. BMC Struct Biol 9: pp. 59 CrossRef
  28. Qiao, F, Harada, B, Song, H, Whitelegge, J, Courey, AJ, Bowie, JU (2005) Mae inhibits Pointed-P2 transcriptional activity by blocking its MAPK docking site. EMBO J 25: pp. 70-79 CrossRef
  29. Zhang, H, Xu, Q, Krajewski, S, Krajewska, M, Xie, Z, Fuess, S, Kitada, S, Pawlowski, K, Godzik, A, Reed, JC (2000) BAR: an apoptosis regulator at the intersection of caspases and Bcl-2 family proteins. PNAS 97: pp. 2597-2602 CrossRef
  30. Aviv, T, Lin, Z, Rendl, LM, Sicheri, F, Smibert, CA (2003) The RNA-binding SAM domain of Smaug defines a new family of post-transcriptional regulators. Nat Struct Biol 10: pp. 614-621 CrossRef
  31. Barrera, FN, Poveda, JA, Gonz谩lez-Ros, JM, Neira, JL (2003) Binding of the C-terminal sterile 伪 Motif (SAM) domain of human p73 to lipid membranes. J Biol Chem 278: pp. 46878-46885 CrossRef
  32. Kim, CA, Sawaya, MR, Cascio, D, Kim, W, Bowie, JU (2005) Structural organization of a sex-comb-on-midleg/Polyhomeotic copolymer. J Biol Chem 280: pp. 27769-27775 CrossRef
  33. Rajakulendran, T, Sahmi, M, Kurinov, I, Tyers, M, Therrien, M, Sicheri, F (2008) CNK and HYP form a discrete dimer by their SAM domains to mediate RAF kinase signaling. Proc Natl Acad Sci 105: pp. 2836-2841 CrossRef
  34. Leone, M, Cellitti, J, Pellecchia, M (2008) NMR studies of a heterotypic Sam鈭扴am domain association: the interaction between the lipid phosphatase Ship2 and the EphA2 Receptor. Biochemistry 47: pp. 12721-12728 CrossRef
  35. Knight, MJ, Joubert, MK, Plotkowski, ML, Kropat, J, Gingery, M, Sakane, F, Merchant, SS, Bowie, JU (2010) Zinc binding drives sheet formation by the SAM domain of diacylglycerol kinase 未. Biochemistry 49: pp. 9667-9676 CrossRef
  36. Gundelfinger, ED, Boeckers, TM, Baron, MK, Bowie, JU (2006) A role for zinc in postsynaptic density asSAMbly and plasticity?. Trends Biochem Sci 31: pp. 366-373 CrossRef
  37. Lawrence, MS, Phillips, KJ, Liu, DR (2007) Supercharging proteins can impart unusual resilience. J Am Chem Soc 129: pp. 10110-10112 CrossRef
  38. Grucza, RA, Bradshaw, JM, Mitaxov, V, Waksman, G (2000) Role of electrostatic interactions in SH2 domain recognition: salt-dependence of tyrosyl-phosphorylated peptide binding to the tandem SH2 domain of the Syk kinase and the single SH2 domain of the Src kinase. Biochemistry 39: pp. 10072-10081 CrossRef
  39. Hileman, RE, Jennings, RN, Linhardt, RJ (1998) Thermodynamic analysis of the heparin interaction with a basic cyclic peptide using isothermal titration calorimetry. Biochemistry 37: pp. 15231-15237 CrossRef
  40. Nauli, S, Farr, S, Lee, Y-J, Kim, H-Y, Faham, S, Bowie, JU (2007) Polymer-driven crystallization. Protein Sci 16: pp. 2542-2551 CrossRef
  41. Cogswell, C, Price, SJ, Hou, X, Guay-Woodford, LM, Flaherty, L, Bryda, EC (2003) Positional cloning of jcpk/bpk locus of the mouse. Mamm Genome 14: pp. 242-249 CrossRef
  42. Stagner, EE, Bouvrette, DJ, Cheng, J, Bryda, EC (2009) The polycystic kidney disease-related proteins Bicc1 and SamCystin interact. Biochem Biophys Res Commun 383: pp. 16-21 CrossRef
  43. Kugita, M, Nishii, K, Morita, M, Yoshihara, D, Kowa-Sugiyama, H, Yamada, K, Yamaguchi, T, Wallace, DP, Calvet, JP, Kurahashi, H, Nagao, S (2010) Global gene expression profiling in early-stage polycystic kidney disease in the Han:SPRD Cy rat identifies a role for RXR signaling. AJP Ren Physiol 300: pp. F177-F188 CrossRef
  44. Senturia, R, Faller, M, Yin, S, Loo, JA, Cascio, D, Sawaya, MR, Hwang, D, Clubb, RT, Guo, F (2010) Structure of the dimerization domain of DiGeorge Critical Region 8. Protein Sci 19: pp. 1354-1365 CrossRef
  45. Schatz, PJ, Cull, MG, Martin, EL, Gates, CM (1996) Screening of peptide libraries linked to lac repressor. Methods Enzymol 267: pp. 171-191 CrossRef
  46. Malakhov, MP, Mattern, MR, Malakhova, OA, Drinker, M, Weeks, SD, Butt, TR (2004) SUMO fusions and SUMO-specific protease for efficient expression and purification of proteins. J Struct Funct Genomics 5: pp. 75-86 CrossRef
  47. Kabsch, W (2010) XDS. Acta Crystallogr D Biol Crystallogr 66: pp. 125-132 CrossRef
  48. Pape, T, Schneider, TR (2004) HKL2MAP : a graphical user interface for macromolecular phasing with SHELX programs. J Appl Crystallogr 37: pp. 843-844 CrossRef
  49. Sheldrick, GM (2010) Experimental phasing with SHELXC/D/E : combining chain tracing with density modification. Acta Crystallogr D Biol Crystallogr 66: pp. 479-485 CrossRef
  50. Winn, MD, Ballard, CC, Cowtan, KD, Dodson, EJ, Emsley, P, Evans, PR, Keegan, RM, Krissinel, EB, Leslie, AGW, McCoy, A, McNicholas, SJ, Murshudov, GN, Pannu, NS, Potterton, EA, Powell, HR, Read, RJ, Vagin, A, Wilson, KS (2011) Overview of the CCP 4 suite and current developments. Acta Crystallogr D Biol Crystallogr 67: pp. 235-242 CrossRef
  51. Adams, PD, Afonine, PV, Bunk贸czi, G, Chen, VB, Davis, IW, Echols, N, Headd, JJ, Hung, L-W, Kapral, GJ, Grosse-Kunstleve, RW, McCoy, AJ, Moriarty, NW, Oeffner, R, Read, RJ, Richardson, DC, Richardson, JS, Terwilliger, TC, Zwart, PH (2010) PHENIX : a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66: pp. 213-221 CrossRef
  52. Emsley, P, Lohkamp, B, Scott, WG, Cowtan, K (2010) Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66: pp. 486-501 CrossRef
  53. Karplus, PA (2012) Linking crystallographic model and data quality. Science 336: pp. 1030-1033 CrossRef
  54. McCoy, AJ, Grosse-Kunstleve, RW, Adams, PD, Winn, MD, Storoni, LC, Read, RJ (2007) Phaser crystallographic software. J Appl Crystallogr 40: pp. 658-674 CrossRef
  55. Laskowski, RA, MacArthur, MW, Moss, DS, Thornton, JM (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallogr 26: pp. 283-291 CrossRef
  56. Colovos, C, Yeates, TO (1993) Verification of protein structures: patterns of nonbonded atomic interactions. Protein Sci 2: pp. 1511-1519 CrossRef
  57. Bowie, JU, L眉thy, R, Eisenberg, D (1991) A method to identify protein sequences that fold into a known three-dimensional structure. Science 253: pp. 164-170 CrossRef
  58. Schr枚dinger, LLC (2010) The PyMOL Molecular Graphics System, Version 1.3.
  59. Baker, NA, Sept, D, Joseph, S, Holst, MJ, McCammon, JA (2001) Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci 98: pp. 10037-10041 CrossRef
  60. Krissinel, E, Henrick, K (2007) Inference of macromolecular assemblies from crystalline state. J Mol Biol 372: pp. 774-797 CrossRef
  
• 刊物主题：Biochemistry, general; Protein Science; Crystallography; Mass Spectrometry; Spectroscopy/Spectrometry;
• 出版者：BioMed Central
• ISSN：1472-6807

文摘

Background Autosomal dominant polycystic kidney disease (ADPKD) is the most common genetic disorder leading to end-stage renal failure in humans. In the PKD/Mhm(cy/+) rat model of ADPKD, the point mutation R823W in the sterile alpha motif (SAM) domain of the protein ANKS6 is responsible for disease. SAM domains are known protein-protein interaction domains, capable of binding each other to form polymers and heterodimers. Despite its physiological importance, little is known about the function of ANKS6 and how the R823W point mutation leads to PKD. Recent work has revealed that ANKS6 interacts with a related protein called ANKS3. Both ANKS6 and ANKS3 have a similar domain structure, with ankyrin repeats at the N-terminus and a SAM domain at the C-terminus. Results The SAM domain of ANKS3 is identified as a direct binding partner of the ANKS6 SAM domain. We find that ANKS3-SAM polymerizes and ANKS6-SAM can bind to one end of the polymer. We present crystal structures of both the ANKS3-SAM polymer and the ANKS3-SAM/ANKS6-SAM complex, revealing the molecular details of their association. We also learn how the R823W mutation disrupts ANKS6 function by dramatically destabilizing the SAM domain such that the interaction with ANKS3-SAM is lost. Conclusions ANKS3 is a direct interacting partner of ANKS6. By structurally and biochemically characterizing the interaction between the ANKS3 and ANKS6 SAM domains, our work provides a basis for future investigation of how the interaction between these proteins mediates kidney function.