Molecular basis of Purinergic Signal Metabolism by Ectonucleotide Pyrophosphatase/Phosphodiesterases 4 and 1 and implications in Stroke

Journal of Biological Chemistry

Volumn 289, Issue 6, 2014, Pages 3294-3306

  Albright, Ronald A ^a   Ornstein, Deborah L ^b   Cao, Wenxiang ^c   Chang, William C ^c   Robert, Donna ^b   Tehan, Martin ^a   Hoyer, Denton ^c   Liu, Lynn ^c   Stabach, Paul ^a,d   Yang, Guangxiao ^a   De La Cruz, Enrique M ^c   Braddock, Demetrios T ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b DARTMOUTH MEDICAL SCHOOL   (United States)

^c YALE UNIVERSITY   (United States)

^d MIT LINCOLN LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE; ENZYME CATALYSIS; PLATELETS; PURINERGIC METABOLISM; STROKE; X-RAY CRYSTALLOGRAPHY;

ADENOSINE TRIPHOSPHATE; BLOOD PLATELETS; BRAIN; DINUCLEOSIDE PHOSPHATES; ENDOTHELIUM, VASCULAR; HUMANS; PHOSPHORIC DIESTER HYDROLASES; PLATELET AGGREGATION; POLYMORPHISM, GENETIC; PROTEIN STRUCTURE, TERTIARY; PYROPHOSPHATASES; STROKE; SUBSTRATE SPECIFICITY;

EID: 84893668900     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.505867     Document Type: Article

References (64)

1. Offermanns, S. (2006) Activation of platelet function through G-proteincoupled receptors. Circ. Res. 99, 1293-1304
2. Terkeltaub, R. (2006) Physiologic and pathologic functions of the NPP nucleotide pyrophosphatase/phosphodiesterase family focusing on NPP1 in calcification. Purinergic Signal. 2, 371-377
3. Omatsu-Kanbe, M., Isono, T., and Matsuura, H. (2002) Multiple P2 receptors contribute to a transient increase in intracellular Ca2-concentration in ATP-stimulated rat brown adipocytes. Exp. Physiol. 87, 643-652
4. Schödel, J., Weise, I., Klinger, R., and Schmidt, M. (2004) Stimulation of lipogenesis in rat adipocytes by ATP, a ligand for P2-receptors. Biochem. Biophys. Res. Commun. 321, 767-773
5. Kato, K., Nishimasu, H., Okudaira, S., Mihara, E., Ishitani, R., Takagi, J., Aoki, J., and Nureki, O. (2012) Crystal structure of Enpp1, an extracellular glycoprotein involved in bone mineralization and insulin signaling. Proc. Natl. Acad. Sci. U.S.A. 109, 16876-16881
6. Vollmayer, P., Clair, T., Goding, J. W., Sano, K., Servos, J., and Zimmermann, H. (2003) Hydrolysis of diadenosine polyphosphates by nucleotide pyrophosphatases/phosphodiesterases. Eur. J. Biochem. 270, 2971-2978
7. Albright, R. A., Chang, W. C., Robert, D., Ornstein, D. L., Cao, W., Liu, L., Redick, M. E., Young, J. I., De La Cruz, E. M., and Braddock, D. T. (2012) NPP4 is a procoagulant enzyme on the surface of vascular endothelium. Blood 120, 4432-4440
8. Tokumura, A., Majima, E., Kariya, Y., Tominaga, K., Kogure, K., Yasuda, K., and Fukuzawa, K. (2002) Identification of human plasma lysophospholipase D, a lysophosphatidic acid-producing enzyme, as autotaxin, a multifunctional phosphodiesterase. J. Biol. Chem. 277, 39436-39442
9. Umezu-Goto, M., Kishi, Y., Taira, A., Hama, K., Dohmae, N., Takio, K., Yamori, T., Mills, G. B., Inoue, K., Aoki, J., and Arai, H. (2002) Autotaxin has lysophospholipaseDactivity leading to tumor cell growth and motility by lysophosphatidic acid production. J. Cell Biol. 158, 227-233
10. Saunders, L. P., Cao, W., Chang, W. C., Albright, R. A., Braddock, D. T., and De La Cruz, E. M. (2011) Kinetic analysis of autotaxin reveals substrate-specific catalytic pathways and a mechanism for lysophosphatidic acid distribution. J. Biol. Chem. 286, 30130-30141
11. Sakagami, H., Aoki, J., Natori, Y., Nishikawa, K., Kakehi, Y., Natori, Y., and Arai, H. (2005) Biochemical and molecular characterization of a novel choline-specific glycerophosphodiester phosphodiesterase belonging to the nucleotide pyrophosphatase/phosphodiesterase family. J. Biol. Chem. 280, 23084-23093
12. Duan, R. D., Bergman, T., Xu, N., Wu, J., Cheng, Y., Duan, J., Nelander, S., Palmberg, C., and Nilsson, A. (2003) Identification of human intestinal alkaline sphingomyelinase as a novel ecto-enzyme related to the nucleotide phosphodiesterase family. J. Biol. Chem. 278, 38528-38536
13. Liu, S., Umezu-Goto, M., Murph, M., Lu, Y., Liu, W., Zhang, F., Yu, S., Stephens, L. C., Cui, X., Murrow, G., Coombes, K., Muller, W., Hung, M. C., Perou, C. M., Lee, A. V., Fang, X., and Mills, G. B. (2009) Expression of autotaxin and lysophosphatidic acid receptors increases mammary tumorigenesis, invasion, and metastases. Cancer Cell 15, 539-550
14. Boucharaba, A., Serre, C. M., Guglielmi, J., Bordet, J. C., Clézardin, P., and Peyruchaud, O. (2006) The type 1 lysophosphatidic acid receptor is a target for therapy in bone metastases. Proc. Natl. Acad. Sci. U.S.A. 103, 9643-9648
15. Raj, G. V., Sekula, J. A., Guo, R., Madden, J. F., and Daaka, Y. (2004) Lysophosphatidic acid promotes survival of androgen-insensitive prostate cancer PC3 cells via activation of NF-B. Prostate 61, 105-113
16. Kishi, Y., Okudaira, S., Tanaka, M., Hama, K., Shida, D., Kitayama, J., Yamori, T., Aoki, J., Fujimaki, T., and Arai, H. (2006) Autotaxin is overexpressed in glioblastoma multiforme and contributes to cell motility of glioblastoma by converting lysophosphatidylcholine to lysophosphatidic acid. J. Biol. Chem. 281, 17492-17500
17. Sevastou, I., Kaffe, E., Mouratis, M. A., and Aidinis, V. (2013) Lysoglycerophospholipids in chronic inflammatory disorders: The PLA(2)/LPC and ATX/LPA axes. Biochim. Biophys. Acta 1831, 42-60
18. Tager, A. M., LaCamera, P., Shea, B. S., Campanella, G. S., Selman, M., Zhao, Z., Polosukhin, V., Wain, J., Karimi-Shah, B. A., Kim, N. D., Hart, W. K., Pardo, A., Blackwell, T. S., Xu, Y., Chun, J., and Luster, A. D. (2008) The lysophosphatidic acid receptor LPA1 links pulmonary fibrosis to lung injury by mediating fibroblast recruitment and vascular leak. Nat. Med. 14, 45-54
19. Tanaka, M., Okudaira, S., Kishi, Y., Ohkawa, R., Iseki, S., Ota, M., Noji, S., Yatomi, Y., Aoki, J., and Arai, H. (2006) Autotaxin stabilizes blood vessels and is required for embryonic vasculature by producing lysophosphatidic acid. J. Biol. Chem. 281, 25822-25830
20. van Meeteren, L. A., Ruurs, P., Stortelers, C., Bouwman, P., van Rooijen, M. A., Pradére, J. P., Pettit, T. R., Wakelam, M. J., Saulnier-Blache, J. S., Mummery, C. L., Moolenaar, W. H., and Jonkers, J. (2006) Autotaxin, a secreted lysophospholipase D, is essential for blood vessel formation during development. Mol. Cell. Biol. 26, 5015-5022
21. Bertrand, J., Nitschke, Y., Fuerst, M., Hermann, S., Schäfers, M., Sherwood, J., Nalesso, G., Ruether, W., Rutsch, F., Dell'Accio, F., and Pap, T. (2012) Decreased levels of nucleotide pyrophosphatase phosphodiesterase 1 are associated with cartilage calcification in osteoarthritis and trigger osteoarthritic changes in mice. Ann. Rheum. Dis. 71, 1249-1253
22. Rutsch, F., Ruf, N., Vaingankar, S., Toliat, M. R., Suk, A., Höhne, W., Schauer, G., Lehmann, M., Roscioli, T., Schnabel, D., Epplen, J. T., Knisely, A., Superti-Furga, A., McGill, J., Filippone, M., Sinaiko, A. R., Vallance, H., Hinrichs, B., Smith, W., Ferre, M., Terkeltaub, R., and Nürnberg, P. (2003) Mutations in ENPP1 are associated with "idiopathic" infantile arterial calcification. Nat. Genet. 34, 379-381
23. Mackenzie, N. C., Zhu, D., Milne, E. M., van 't Hof, R., Martin, A., Darryl Quarles, L., Quarles, D. L., Millán, J. L., Farquharson, C., and MacRae, V. E. (2012) Altered bone development and an increase in FGF-23 expression in Enpp1(-/) mice. PLoS One 7, e32177
24. Stefan, C., Jansen, S., and Bollen, M. (2005) NPP-type ectophosphodiesterases: unity in diversity. Trends Biochem. Sci. 30, 542-550
25. Collaborative Computational Project No. 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763
26. Gachet, C. (2012) P2Y(12) receptors in platelets and other hematopoietic and non-hematopoietic cells. Purinergic Signal. 8, 609-619
27. Enjyoji, K., Sévigny, J., Lin, Y., Frenette, P. S., Christie, P. D., Esch, J. S., 2nd, Imai, M., Edelberg, J. M., Rayburn, H., Lech, M., Beeler, D. L., Csizmadia, E., Wagner, D. D., Robson, S. C., and Rosenberg, R. D. (1999) Targeted disruption of cd39/ATP diphosphohydrolase results in disordered hemostasis and thromboregulation. Nat. Med. 5, 1010-1017
28. Kaczmarek, E., Koziak, K., Sévigny, J., Siegel, J. B., Anrather, J., Beaudoin, A. R., Bach, F. H., and Robson, S. C. (1996) Identification and characterization of CD39/vascular ATP diphosphohydrolase. J. Biol. Chem. 271, 33116-33122
29. Marcus, A. J., Broekman, M. J., Drosopoulos, J. H., Islam, N., Alyonycheva, T. N., Safier, L. B., Hajjar, K. A., Posnett, D. N., Schoenborn, M. A., Schooley, K. A., Gayle, R. B., and Maliszewski, C. R. (1997) The endothelial cell ecto-ADPase responsible for inhibition of platelet function is CD39. J. Clin. Invest. 99, 1351-1360
30. Knowles, A. F. (2011) The GDA1-CD39 superfamily: NTPDases with diverse functions. Purinergic Signal. 7, 21-45
31. Pearson, J. D., and Gordon, J. L. (1985) Nucleotide metabolism by endothelium. Annu. Rev. Physiol. 47, 617-627
32. Birk, A. V., Bubman, D., Broekman, M. J., Robertson, H. D., Drosopoulos, J. H., Marcus, A. J., and Szeto, H. (2002) Role of a novel soluble nucleotide phosphohydrolase from sheep plasma in inhibition of platelet reactivity: Hemostasis, thrombosis, and vascular biology. J. Lab. Clin. Med. 139, 116-124
33. Yegutkin, G. G. (2008) Nucleotide-And nucleoside-converting ectoenzymes: Important modulators of purinergic signalling cascade. Biochim. Biophys. Acta 1783, 673-694
34. Zimmermann, H. (1992) 5-Nucleotidase: molecular structure and functional aspects. Biochem. J. 285, 345-365
35. Koszalka, P., Ozüyaman, B., Huo, Y., Zernecke, A., Flögel, U., Braun, N., Buchheiser, A., Decking, U. K., Smith, M. L., Sévigny, J., Gear, A., Weber, A. A., Molojavyi, A., Ding, Z., Weber, C., Ley, K., Zimmermann, H., Gödecke, A., and Schrader, J. (2004) Targeted disruption of cd73/ecto-5-nucleotidase alters thromboregulation and augments vascular inflammatory response. Circ. Res. 95, 814-821
36. Lüthje, J., and Ogilvie, A. (1983) The presence of diadenosine 5-,5-P1,P3-triphosphate (Ap3A) in human platelets. Biochem. Biophys. Res. Commun. 115, 253-260
37. Lüthje, J., Miller, D., and Ogilvie, A. (1987) Unproportionally high concentrations of diadenosine triphosphate (Ap3A) and diadenosine tetraphosphate (Ap4A) in heavy platelets. Consequences for in vitro studies with human platelets. Blut 54, 193-200
38. Olgilvie, A. (1992) in AP4A and Other Dinucleotide Polyphosphates (McLennan, A. G., ed) pg. 357, CRC Press, Inc., Boca Raton, FL
39. Jankowski, J., Potthoff, W., van der Giet, M., Tepel, M., Zidek, W., and Schlüter, H. (1999) High performance liquid chromatographic assay of the diadenosine polyphosphates in human platelets. Anal. Biochem. 269, 72-78
40. Lüthje, J., Baringer, J., and Ogilvie, A. (1985) Effects of diadenosine triphosphate (Ap3A) and diadenosine tetraphosphate (Ap4A) on platelet aggregation in unfractionated human blood. Blut 51, 405-413
41. Ogilvie, A., Lüthje, J., Pohl, U., and Busse, R. (1989) Identification and partial characterization of an adenosine(5)tetraphospho(5) adenosine hydrolase on intact bovine aortic endothelial cells. Biochem. J. 259, 97-103
42. Goldman, S. J., Gordon, E. L., and Slakey, L. L. (1986) Hydrolysis of diadenosine 5-,5-P-,P-triphosphate (Ap3A) by porcine aortic endothelial cells. Circ. Res. 59, 362-366
43. Bollen, M., Gijsbers, R., Ceulemans, H., Stalmans, W., and Stefan, C. (2000) Nucleotide pyrophosphatases/phosphodiesterases on the move. Crit. Rev. Biochem. Mol. Biol. 35, 393-432
44. Addison, W. N., Azari, F., Sørensen, E. S., Kaartinen, M. T., and McKee, M. D. (2007) Pyrophosphate inhibits mineralization of osteoblast cultures by binding to mineral, up-regulating osteopontin, and inhibiting alkaline phosphatase activity. J. Biol. Chem. 282, 15872-15883
45. Kalya, S., and Rosenthal, A. K. (2005) Extracellular matrix changes regulate calcium crystal formation in articular cartilage. Curr. Opin. Rheumatol. 17, 325-329
46. Levy-Litan, V., Hershkovitz, E., Avizov, L., Leventhal, N., Bercovich, D., Chalifa-Caspi, V., Manor, E., Buriakovsky, S., Hadad, Y., Goding, J., and Parvari, R. (2010) Autosomal-recessive hypophosphatemic rickets is associated with an inactivation mutation in the ENPP1 gene. Am. J. Hum. Genet. 86, 273-278
47. Hirakawa, H., Kusumi, T., Nitobe, T., Ueyama, K., Tanaka, M., Kudo, H., Toh, S., and Harata, S. (2004) An immunohistochemical evaluation of extracellular matrix components in the spinal posterior longitudinal ligament and intervertebral disc of the tiptoe walking mouse. J. Orthop. Sci. 9, 591-597
48. Okawa, A., Nakamura, I., Goto, S., Moriya, H., Nakamura, Y., and Ikegawa, S. (1998) Mutation in Npps in a mouse model of ossification of the posterior longitudinal ligament of the spine. Nat. Genet. 19, 271-273
49. Flanagan, J. M., Sheehan, V., Linder, H., Howard, T. A., Wang, Y. D., Hoppe, C. C., Aygun, B., Adams, R. J., Neale, G. A., and Ware, R. E. (2013) Genetic mapping and exome sequencing identify 2 mutations associated with stroke protection in pediatric patients with sickle cell anemia. Blood 121, 3237-3245
50. Jansen, S., Stefan, C., Creemers, J. W., Waelkens, E., Van Eynde, A., Stalmans, W., and Bollen, M. (2005) Proteolytic maturation and activation of autotaxin (NPP2), a secreted metastasis-enhancing lysophospholipase D. J. Cell Sci. 118, 3081-3089
51. Saunders, L. P., Ouellette, A., Bandle, R., Chang, W. C., Zhou, H., Misra, R. N., De La Cruz, E. M., and Braddock, D. T. (2008) Identification of small-molecule inhibitors of autotaxin that inhibit melanoma cell migration and invasion. Mol. Cancer Ther. 7, 3352-3362
52. Otwinowski, Z., and Minor, W. (1997) Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326
53. Terwilliger, T. C., Adams, P. D., Read, R. J., McCoy, A. J., Moriarty, N. W., Grosse-Kunstleve, R. W., Afonine, P. V., Zwart, P. H., and Hung, L. W. (2009) Decision-making in structure solution using Bayesian estimates of map quality: the PHENIX AutoSol wizard. Acta Crystallogr. D Biol. Crystallogr. 65, 582-601
54. Terwilliger, T. C., Grosse-Kunstleve, R. W., Afonine, P. V., Moriarty, N. W., Zwart, P. H., Hung, L. W., Read, R. J., and Adams, P. D. (2008) Iterative model building, structure refinement and density modification with the PHENIX AutoBuild wizard. Acta Crystallogr. D Biol. Crystallogr. 64, 61-69
55. Zalatan, J. G., Fenn, T. D., Brunger, A. T., and Herschlag, D. (2006) Structural and functional comparisons of nucleotide pyrophosphatase/ phosphodiesterase and alkaline phosphatase: implications for mechanism and evolution. Biochemistry 45, 9788-9803
56. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501
57. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., Mc-Coy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221
58. Jansen, S., Perrakis, A., Ulens, C., Winkler, C., Andries, M., Joosten, R. P., Van Acker, M., Luyten, F. P., Moolenaar, W. H., and Bollen, M. (2012) Structure of NPP1, an ectonucleotide pyrophosphatase/phosphodiesterase involved in tissue calcification. Structure 20, 1948-1959
59. Nikolic-Hughes, I., O'brien, P. J., and Herschlag, D. (2005) Alkaline phosphatase catalysis is ultrasensitive to charge sequestered between the active site zinc ions. J. Am. Chem. Soc. 127, 9314-9315
60. Gijsbers, R., Ceulemans, H., Stalmans, W., and Bollen, M. (2001) Structural and catalytic similarities between nucleotide pyrophosphatases/ phosphodiesterases and alkaline phosphatases. J. Biol. Chem. 276, 1361-1368
61. Harahap, A. R., and Goding, J. W. (1988) Distribution of the murine plasma cell antigen PC-1 in non-lymphoid tissues. J. Immunol. 141, 2317-2320
62. Rutsch, F., Vaingankar, S., Johnson, K., Goldfine, I., Maddux, B., Schauerte, P., Kalhoff, H., Sano, K., Boisvert, W. A., Superti-Furga, A., and Terkeltaub, R. (2001) PC-1 nucleoside triphosphate pyrophosphohydro-lase deficiency in idiopathic infantile arterial calcification. Am. J. Pathol. 158, 543-554
63. Pizzuti, A., Frittitta, L., Argiolas, A., Baratta, R., Goldfine, I. D., Bozzali, M., Ercolino, T., Scarlato, G., Iacoviello, L., Vigneri, R., Tassi, V., and Trischitta, V. (1999) A polymorphism (K121Q) of the human glycoprotein PC-1 gene coding region is strongly associated with insulin resistance. Diabetes 48, 1881-1884
64. Meyre, D., Bouatia-Naji, N., Tounian, A., Samson, C., Lecoeur, C., Vatin, V., Ghoussaini, M., Wachter, C., Hercberg, S., Charpentier, G., Patsch, W., Pattou, F., Charles, M. A., Tounian, P., Clément, K., Jouret, B., Weill, J., Maddux, B. A., Goldfine, I. D., Walley, A., Boutin, P., Dina, C., and Froguel, P. (2005) Variants of ENPP1 are associated with childhood and adult obesity and increase the risk of glucose intolerance and type 2 diabetes. Nat. Genet. 37, 863-867