Protein phosphatase-1α interacts with and dephosphorylates polycystin-1

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Parnell, Stephen C ^a,b   Puri, Sanjeev ^c   Wallace, Darren P ^a,b   Calvet, James P ^a,b  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

^c PANJAB UNIVERSITY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

CALCINEURIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; HOLOENZYME; PHOSPHOPROTEIN PHOSPHATASE 1; PHOSPHOPROTEIN PHOSPHATASE 1ALPHA; POLYCYSTIN 1; UNCLASSIFIED DRUG; AMINO ACID; HYBRID PROTEIN; POLYCYSTIC KIDNEY DISEASE 1 PROTEIN; POLYCYSTIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CONTROLLED STUDY; CYTOSOL; IMMUNOPRECIPITATION; MUTATION; PROTEIN DEPHOSPHORYLATION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SEQUENCE ANALYSIS; AMINO ACID SEQUENCE; ANIMAL; BIOLOGICAL MODEL; CELL STRAIN HEK293; CHEMISTRY; ENZYME SPECIFICITY; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; MOUSE; PHOSPHORYLATION; PROTEIN BINDING; SEQUENCE ALIGNMENT;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; AMINO ACIDS; ANIMALS; HEK293 CELLS; HOLOENZYMES; HUMANS; IMMUNOPRECIPITATION; MICE; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MUTATION; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN PHOSPHATASE 1; RECOMBINANT FUSION PROTEINS; SEQUENCE ALIGNMENT; SUBSTRATE SPECIFICITY; TRPP CATION CHANNELS;

EID: 84861880031     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0036798     Document Type: Article

References (50)

1. Ceulemans H, Bollen M, (2004) Functional diversity of protein phosphatase-1, a cellular economizer and reset button. Physiol Rev 84: 1-39.
2. Mi J, Guo C, Brautigan DL, Larner JM, (2007) Protein phosphatase-1alpha regulates centrosome splitting through Nek2. Cancer Res 67: 1082-1089.
3. Barford D, Das AK, Egloff MP, (1998) The structure and mechanism of protein phosphatases: insights into catalysis and regulation. Annu Rev Biophys Biomol Struct 27: 133-164.
4. Helps NR, Luo X, Barker HM, Cohen PT, (2000) NIMA-related kinase 2 (Nek2), a cell-cycle-regulated protein kinase localized to centrosomes, is complexed to protein phosphatase 1. Biochem J 349: 509-518.
5. Egloff MP, Johnson DF, Moorhead G, Cohen PT, Cohen P, et al. (1997) Structural basis for the recognition of regulatory subunits by the catalytic subunit of protein phosphatase 1. Embo J 16: 1876-1887.
6. Ayllon V, Cayla X, Garcia A, Fleischer A, Rebollo A, (2002) The anti-apoptotic molecules Bcl-xL and Bcl-w target protein phosphatase 1alpha to Bad. Eur J Immunol 32: 1847-1855.
7. Garcia A, Cayla X, Caudron B, Deveaud E, Roncal F, et al. (2004) New insights in protein phosphorylation: a signature for protein phosphatase 1 interacting proteins. C R Biol 327: 93-97.
8. Hendrickx A, Beullens M, Ceulemans H, Abt TD, Van Eynde A, et al. (2009) Docking motif-guided mapping of the interactome of protein phosphatase-1. Chem Biol 16: 365-371.
9. Gabow PA, (1993) Autosomal dominant polycystic kidney disease. N Engl J Med 329: 332-342.
10. Harris PC, Torres VE, (2009) Polycystic Kidney Disease. Annu Rev Med 60: 321-337.
11. Piontek K, Menezes LF, Garcia-Gonzalez MA, Huso DL, Germino GG, (2007) A critical developmental switch defines the kinetics of kidney cyst formation after loss of Pkd1. Nat Med 13: 1490-1495.
12. Grantham JJ, (2008) Clinical practice. Autosomal dominant polycystic kidney disease. N Engl J Med 359: 1477-1485.
13. Grantham JJ, Chapman AB, Torres VE, (2006) Volume progression in autosomal dominant polycystic kidney disease: the major factor determining clinical outcomes. Clin J Am Soc Nephrol 1: 148-157.
14. Qian F, Germino FJ, Cai Y, Zhang X, Somlo S, et al. (1997) PKD1 interacts with PKD2 through a probable coiled-coil domain. Nat Genet 16: 179-183.
15. Tsiokas L, (2009) Function and regulation of TRPP2 at the plasma membrane. Am J Physiol Renal Physiol 297: F1-9.
16. Nims N, Vassmer D, Maser RL, (2003) Transmembrane domain analysis of polycystin-1, the product of the polycystic kidney disease-1 (PKD1) gene: evidence for 11 membrane-spanning domains. Biochemistry 42: 13035-13048.
17. Parnell SC, Magenheimer BS, Maser RL, Rankin CA, Smine A, et al. (1998) The polycystic kidney disease-1 protein, polycystin-1, binds and activates heterotrimeric G-proteins in vitro. Biochem Biophys Res Commun 251: 625-631.
18. Shillingford JM, Murcia NS, Larson CH, Low SH, Hedgepeth R, et al. (2006) The mTOR pathway is regulated by polycystin-1, and its inhibition reverses renal cystogenesis in polycystic kidney disease. Proc Natl Acad Sci U S A 103: 5466-5471.
19. Van Bodegom D, Saifudeen Z, Dipp S, Puri S, Magenheimer BS, et al. (2006) The polycystic kidney disease-1 gene is a target for p53-mediated transcriptional repression. J Biol Chem 281: 31234-31244.
20. Eto M, Kirkbride JA, Brautigan DL, (2005) Assembly of MYPT1 with protein phosphatase-1 in fibroblasts redirects localization and reorganizes the actin cytoskeleton. Cell Motil Cytoskeleton 62: 100-109.
21. Puri S, Magenheimer BS, Maser RL, Ryan EM, Zien CA, et al. (2004) Polycystin-1 activates the calcineurin/NFAT (nuclear factor of activated T-cells) signaling pathway. J Biol Chem 279: 55455-55464.
22. Parnell SC, Magenheimer BS, Maser RL, Zien CA, Frischauf AM, et al. (2002) Polycystin-1 activation of c-Jun N-terminal kinase and AP-1 is mediated by heterotrimeric G proteins. J Biol Chem 277: 19566-19572.
23. Sutters M, Yamaguchi T, Maser RL, Magenheimer BS, John PL, et al. (2001) Polycystin-1 transforms the cAMP growth-responsive phenotype of M-1 cells. Kidney Int 60: 484-494.
24. Parnell SC, Magenheimer BS, Maser RL, Calvet JP, (1999) Identification of the major site of in vitro PKA phosphorylation in the polycystin-1 C-terminal cytosolic domain. Biochem Biophys Res Commun 259: 539-543.
25. Chauvet V, Tian X, Husson H, Grimm DH, Wang T, et al. (2004) Mechanical stimuli induce cleavage and nuclear translocation of the polycystin-1 C terminus. J Clin Invest 114: 1433-1443.
26. Reed B, McFann K, Kimberling WJ, Pei Y, Gabow PA, et al. (2008) Presence of de novo mutations in autosomal dominant polycystic kidney disease patients without family history. Am J Kidney Dis 52: 1042-1050.
27. Li HP, Geng L, Burrow CR, Wilson PD, (1999) Identification of phosphorylation sites in the PKD1-encoded protein C- terminal domain. Biochem Biophys Res Commun 259: 356-363.
28. Moorhead GB, Trinkle-Mulcahy L, Nimick M, De Wever V, Campbell DG, et al. (2008) Displacement affinity chromatography of protein phosphatase one (PP1) complexes. BMC Biochem 9: 28.
29. Schillace RV, Voltz JW, Sim AT, Shenolikar S, Scott JD, (2001) Multiple interactions within the AKAP220 signaling complex contribute to protein phosphatase 1 regulation. J Biol Chem 276: 12128-12134.
30. Trinkle-Mulcahy L, Ajuh P, Prescott A, Claverie-Martin F, Cohen S, et al. (1999) Nuclear organisation of NIPP1, a regulatory subunit of protein phosphatase 1 that associates with pre-mRNA splicing factors. J Cell Sci 112 (Pt 2): 157-168.
31. Perrichot RA, Mercier B, Simon PM, Whebe B, Cledes J, et al. (1999) DGGE screening of PKD1 gene reveals novel mutations in a large cohort of 146 unrelated patients. Hum Genet 105: 231-239.
32. Tan YC, Blumenfeld JD, Anghel R, Donahue S, Belenkaya R, et al. (2009) Novel method for genomic analysis of PKD1 and PKD2 mutations in autosomal dominant polycystic kidney disease. Hum Mutat 30: 264-273.
33. Boucher CA, Ward HH, Case RL, Thurston KS, Li X, et al. (2011) Receptor protein tyrosine phosphatases are novel components of a polycystin complex. Biochim Biophys Acta 1812 1225-1238 pp. 1225-1238.
34. Heroes E, Lesage B, Gornemann J, Beullens M, Van Meervelt L, et al. (2012) The PP1-binding code: a molecular-lego strategy that governs specificity. Febs J Epub ahead of print.
35. Bollen M, (2001) Combinatorial control of protein phosphatase-1. Trends Biochem Sci 26: 426-431.
36. Terrak M, Kerff F, Langsetmo K, Tao T, Dominguez R, (2004) Structural basis of protein phosphatase 1 regulation. Nature 429: 780-784.
37. Huang HB, Horiuchi A, Watanabe T, Shih SR, Tsay HJ, et al. (1999) Characterization of the inhibition of protein phosphatase-1 by DARPP-32 and inhibitor-2. J Biol Chem 274: 7870-7878.
38. Hurley TD, Yang J, Zhang L, Goodwin KD, Zou Q, et al. (2007) Structural basis for regulation of protein phosphatase 1 by inhibitor-2. J Biol Chem 282: 28874-28883.
39. Wakula P, Beullens M, Ceulemans H, Stalmans W, Bollen M, (2003) Degeneracy and function of the ubiquitous RVXF motif that mediates binding to protein phosphatase-1. J Biol Chem 278: 18817-18823.
40. Boletta A, (2009) Emerging evidence of a link between the polycystins and the mTOR pathways. Pathogenetics 2: 6.
41. Beullens M, Bollen M, (2002) The protein phosphatase-1 regulator NIPP1 is also a splicing factor involved in a late step of spliceosome assembly. J Biol Chem 277: 19855-19860.
42. Beullens M, Van Eynde A, Vulsteke V, Connor J, Shenolikar S, et al. (1999) Molecular determinants of nuclear protein phosphatase-1 regulation by NIPP-1. J Biol Chem 274: 14053-14061.
43. Liu J, Brautigan DL, (2000) Glycogen synthase association with the striated muscle glycogen-targeting subunit of protein phosphatase-1. Synthase activation involves scaffolding regulated by beta-adrenergic signaling. J Biol Chem 275: 26074-26081.
44. Fry AM, Mayor T, Meraldi P, Stierhof YD, Tanaka K, et al. (1998) C-Nap1, a novel centrosomal coiled-coil protein and candidate substrate of the cell cycle-regulated protein kinase Nek2. J Cell Biol 141: 1563-1574.
45. Cai Y, Anyatonwu G, Okuhara D, Lee KB, Yu Z, et al. (2004) Calcium dependence of polycystin-2 channel activity is modulated by phosphorylation at Ser812. J Biol Chem 279: 19987-19995.
46. Hu J, Bae YK, Knobel KM, Barr MM, (2006) Casein kinase II and calcineurin modulate TRPP function and ciliary localization. Mol Biol Cell 17: 2200-2211.
47. Kottgen M, Benzing T, Simmen T, Tauber R, Buchholz B, et al. (2005) Trafficking of TRPP2 by PACS proteins represents a novel mechanism of ion channel regulation. Embo J 24: 705-716.
48. Streets AJ, Moon DJ, Kane ME, Obara T, Ong AC, (2006) Identification of an N-terminal glycogen synthase kinase 3 phosphorylation site which regulates the functional localization of polycystin-2 in vivo and in vitro. Hum Mol Genet 15: 1465-1473.
49. Afzal AR, Hand M, Ternes-Pereira E, Saggar-Malik A, Taylor R, et al. (1999) Novel mutations in the 3 region of the polycystic kidney disease 1 (PKD1) gene. Hum Genet 105: 648-653.
50. Badenas C, Torra R, San Millan JL, Lucero L, Mila M, et al. (1999) Mutational analysis within the 3′ region of the PKD1 gene. Kidney Int 55: 1225-1233.