Characterization of a monoclonal antibody as the first specific inhibitor of human NTP diphosphohydrolase-3: Partial characterization of the inhibitory epitope and potential applications

FEBS Journal

Volumn 276, Issue 2, 2009, Pages 479-496

  Munkonda, Mercedes N ^a   Pelletier, Julie ^a   Ivanenkov, Vasily V ^b   Fausther, Michel ^a   Tremblay, Alain ^a   Künzli, Beat ^c   Kirley, Terence L ^b   Sévigny, Jean ^a  

^a LAVAL UNIVERSITY   (Canada)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF MUNICH   (Germany)

Author keywords

ATP; Immunological techniques; Inhibitor; Monoclonal antibody; NTPDase

Indexed keywords

APYRASE; CYSTEINE; EPITOPE; HN3 B3S ANTIBODY; HN3 H10S ANTIBODY; KLH11 ANTIBODY; KLH12 ANTIBODY; LEUCINE; MONOCLONAL ANTIBODY; POLYCLONAL ANTIBODY; PROLINE; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ANTIBODY PRODUCTION; ANTIBODY SPECIFICITY; ANTIGEN BINDING; ANTIGEN RECOGNITION; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DISULFIDE BOND; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME DENATURATION; ENZYME INHIBITION; ENZYME LOCALIZATION; EPITOPE MAPPING; HUMAN; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS;

AMINO ACID SUBSTITUTION; ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODY FORMATION; ANTIBODY SPECIFICITY; CELL LINE; CERCOPITHECUS AETHIOPS; ENZYME INHIBITORS; EPITOPES; HUMANS; MICE; MICE, INBRED BALB C; MODELS, MOLECULAR; PANCREAS; PROTEIN STRUCTURE, TERTIARY; PYROPHOSPHATASES; RECOMBINANT PROTEINS;

EID: 58149267844     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2008.06797.x     Document Type: Article

References (62)

1. Robson SC, Sévigny J Zimmermann H (2006) The E-NTPDase family of ectonucleotidases: structure, function, relationships and pathophysiological significance. Purinergic Signal 2, 409 430.
2. Kukulski F, Lévesque SA, Lavoie EG, Lecka J, Bigonnesse F, Knowles AF, Robson SC, Kirley TL Sévigny J (2005) Comparative hydrolysis of P2 receptor agonists by NTPDases 1, 2, 3 and 8. Purinergic Signal 1, 193 204.
3. Enjyoji K, Sévigny J, Lin Y, Frenette PS, Christie PD, Schulte Am Esch J II., Imai M, Edelberg JM, Rayburn H, Lech M et al. (1999) Targeted disruption of CD39/ATP diphosphohydrolase results in disordered hemostasis and thromboregulation. Nat Med 5, 1010 1017.
4. Goepfert C, Sundberg C, Sévigny J, Enjyoji K, Hoshi T, Csizmadia E Robson S (2001) Disordered cellular migration and angiogenesis in cd39-null mice. Circulation 104, 3109 3115.
5. Mizumoto N, Kumamoto T, Robson SC, Sévigny J, Matsue H, Enjyoji K Takashima A (2002) CD39 is the dominant Langerhans cell-associated ecto-NTPDase: modulatory roles in inflammation and immune responsiveness. Nat Med 8, 358 365.
6. Sévigny J, Sundberg C, Braun N, Guckelberger O, Csizmadia E, Qawi I, Imai M, Zimmermann H Robson SC (2002) Differential catalytic properties and vascular topography of murine nucleoside triphosphate diphosphohydrolase 1 (NTPDase1) and NTPDase2 have implications for thromboregulation. Blood 99, 2801 2809.
7. Jhandier MN, Kruglov EA, Lavoie EG, Sévigny J Dranoff JA (2005) Portal fibroblasts regulate the proliferation of bile duct epithelia via expression of NTPDase2. J Biol Chem 280, 22986 22992.
8. Grenz A, Zhang H, Hermes M, Eckle T, Klingel K, Huang DY, Muller CE, Robson SC, Osswald H Eltzschig HK (2007) Contribution of E-NTPDase1 (CD39) to renal protection from ischemia-reperfusion injury. FASEB J 21, 2863 2873.
9. Friedman DJ, Rennke HG, Csizmadia E, Enjyoji K Robson SC (2007) The vascular ectonucleotidase ENTPD1 is a novel renoprotective factor in diabetic nephropathy. Diabetes 56, 2371 2379.
10. Deaglio S, Dwyer KM, Gao W, Friedman D, Usheva A, Erat A, Chen JF, Enjyoji K, Linden J, Oukka M et al. (2007) Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression. J Exp Med 204, 1257 1265.
11. Imai M, Kaczmarek E, Koziak K, Sévigny J, Goepfert C, Guckelberger O, Csizmadia E, Schulte Am Esch J II. Robson SC (1999) Suppression of ATP diphosphohydrolase/CD39 in human vascular endothelial cells. Biochemistry 38, 13473 13479.
12. Mishra SK, Braun N, Shukla V, Fullgrabe M, Schomerus C, Korf HW, Gachet C, Ikehara Y, Sévigny J, Robson SC et al. (2006) Extracellular nucleotide signaling in adult neural stem cells: synergism with growth factor-mediated cellular proliferation. Development 133, 675 684.
13. Lavoie ÉG, Kukulski F, Lévesque SA, Lecka J Sévigny J (2004) Cloning and characterization of mouse nucleoside triphosphate diphosphohydrolase-3. Biochem Pharmacol 67, 1917 1926.
14. Kirley TL (2006) NTPDase3. AfCS-Nature Molecule Pages doi :.
15. Belcher SM, Zsarnovszky A, Crawford AR, Hemani H, Spurling L Kirley TL (2005) Immunolocalization of ectonucleoside triphosphate diphosphohydrolase 3 in rat brain: implication for modulation of multiple homeostatic systems including feeding and sleep-wake behaviors. Neuroscience 137, 1331 1346.
16. Appelbaum L, Skariah G, Mourrain P Mignot E (2007) Comparative expression of P2X receptors and ecto-nucleoside triphosphate diphosphohydrolase 3 in hypocretin and sensory neurons in zebrafish. Brain Res 1174, 66 75.
17. Vlajkovic SM, Vinayagamoorthy A, Thorne PR, Robson SC, Wang CJ Housley GD (2006) Noise-induced up-regulation of NTPDase3 expression in the rat cochlea: Implications for auditory transmission and cochlear protection. Brain Res 1104, 55 63.
18. Vekaria RM, Shirley DG, Sévigny J Unwin RJ (2006) Immunolocalization of ectonucleotidases along the rat nephron. Am J Physiol Renal Physiol 290, F550 F560.
19. Gendron FP, Halbfinger E, Fischer B, Duval M, D'Orleans-Juste P Beaudoin AR (2000) Novel inhibitors of nucleoside triphosphate diphosphohydrolases: chemical synthesis and biochemical and pharmacological characterizations. J Med Chem 43, 2239 2247.
20. Gendron FP, Benrezzak O, Krugh BW, Kong Q, Weisman GA Beaudoin AR (2002) Purine signaling and potential new therapeutic approach: possible outcomes of NTPDase inhibition. Curr Drug Targets 3, 229 245.
21. Muller CE, Iqbal J, Bagi Y, Zimmermann H, Rollich A Stephan H (2006) Polyoxometalates - a new class of potent ecto-nucleoside triphosphate diphosphohydrolase (NTPDase) inhibitors. Bioorg Med Chem Lett 16, 5943 5947.
22. Munkonda MN, Kauffenstein G, Kukulski F, Lévesque SA, Legendre C, Pelletier J, Lavoie EG, Lecka J Sévigny J (2007) Inhibition of human and mouse plasma membrane bound NTPDases by P2 receptor antagonists. Biochem Pharmacol 74, 1524 1534.
23. Lévesque SA, Lavoie EG, Lecka J, Bigonnesse F Sévigny J (2007) Specificity of the ecto-ATPase inhibitor ARL 67156 on human and mouse ectonucleotidases. Br J Pharmacol 152, 141 150.
24. Smith TM Kirley TL (1998) Cloning, sequencing, and expression of a human brain ecto-apyrase related to both the ecto-ATPases and CD39 ecto-apyrases. Biochim Biophys Acta - Protein Struct Mol Enzymol 1386, 65 78.
25. Ivanenkov VV, Meller J Kirley TL (2005) Characterization of disulfide bonds in human nucleoside triphosphate diphosphohydrolase 3 (NTPDase3): implications for NTPDase structural modeling. Biochemistry 44, 8998 9012.
26. Martín-Satué M, Lavoie EG, Pelletier J, Fausther M, Csizmadia E, Guckelberger O, Robson SC Sévigny J (2009) Localization of plasma membrane bound NTPDases in the murine reproductive tract. Histochem Cell Biol, in press.
27. Vorhoff T, Zimmermann H, Pelletier J, Sévigny J Braun N (2005) Cloning and characterization of the ecto-nucleotidase NTPDase3 from rat brain: predicted secondary structure and relation to other members of the E-NTPDase family and actin. Purinergic Signal 1, 259 270.
28. 2+transients in isolated human and rodent insulin-secreting cells. Purinergic receptor signalling and [Ca2+]i in human beta-cells. Adv Exp Med Biol 426, 173 179.
29. Verspohl EJ, Johannwille B, Waheed A Neye H (2002) Effect of purinergic agonists and antagonists on insulin secretion from INS-1 cells (insulinoma cell line) and rat pancreatic islets. Can J Physiol Pharmacol 80, 562 568.
30. Hellman B, Jansson L, Dansk H Grapengiesser E (2007) Effects of external ATP on Ca(2+) signalling in endothelial cells isolated from mouse islets. Endocrine 32, 33 40.
31. Lavoie EG Sévigny J (2006) Localization of nucleoside triphosphate diphosphohydrolyse-3 in mouse digestive associated glands. Purinergic Signal 2, 245.
32. Chadwick BP Frischauf AM (1998) The CD39-like gene family - identification of three new human members (CD39L2, CD39L3, and CD39L4), their murine homologues, and a member of the gene family from Drosophila melanogaster. Genomics 50, 357 367.
33. Kittel A, Pelletier J, Bigonnesse F, Guckelberger O, Kordas K, Braun N, Robson SC Sévigny J (2004) Localization of nucleoside triphosphate diphosphohydrolase-1 (NTPDase1) and NTPDase2 in pancreas and salivary gland. J Histochem Cytochem 52, 861 871.
34. Degani Y Patchornik A (1974) Cyanylation of sulfhydryl groups by 2-nitro-5-thiocyanobenzoic acid. High-yield modification and cleavage of peptides at cysteine residues. Biochemistry 13, 1 11.
35. Tang HY Speicher DW (2004) Identification of alternative products and optimization of 2-nitro-5-thiocyanatobenzoic acid cyanylation and cleavage at cysteine residues. Anal Biochem 334, 48 61.
36. Murphy DM, Ivanenkov VV Kirley TL (2002) Identification of cysteine residues responsible for oxidative cross-linking and chemical inhibition of human nucleoside-triphosphate diphosphohydrolase 3. J Biol Chem 277, 6162 6169.
37. Maley F, Trimble RB, Tarentino AL Plummer TH Jr. (1989) Characterization of glycoproteins and their associated oligosaccharides through the use of endoglycosidases. Anal Biochem 180, 195 204.
38. Helenius A Aebi M (2001) Intracellular functions of N-linked glycans. Science 291, 2364 2369.
39. Smith TM Kirley TL (1999) Glycosylation is essential for functional expression of a human brain ecto-apyrase. Biochemistry 38, 1509 1516.
40. Zimmermann H (2000) Extracellular metabolism of ATP and other nucleotides. Naunyn Schmiedebergs Arch Pharmacol 362, 299 309.
41. Gendron FP, Halbfinger E, Fischer B Beaudoin AR (2000) Inhibitors of NTPDase: key players in the metabolism of extracellular purines. Adv Exp Med Biol 486, 119 123.
42. Iqbal J, Vollmayer P, Braun N, Zimmermann H Muller CE (2005) A capillary electrophoresis method for the characterization of ecto-nucleoside triphosphate diphosphohydrolases (NTPDases) and the analysis of inhibitors by in-capillary enzymatic microreaction. Purinergic Signal 1, 349 358.
43. Knowles AF, Isler RE Reece JF (1983) The common occurrence of ATP diphosphohydrolase in mammalian plasma membranes. Biochim Biophys Acta 731, 88 96.
44. Beaudoin AR, Sévigny J Picher M (1996) ATP-diphosphohydrolases, apyrases, and nucleotide phosphohydrolases: biochemical properties and functions. In ATPases (Lee AG, ed. pp. 369 401. JAI Press Inc, Greenwich.
45. Knowles AE Nagy AK (1999) Inhibition of an ecto-ATP-diphosphohydrolase by azide. Eur J Biochem 262, 349 357.
46. Sévigny J, Picher M, Grondin G Beaudoin AR (1997) Purification and immunohistochemical localization of the ATP diphosphohydrolase in bovine lungs. Am J Physiol Lung Cell Mol Physiol 272, L939 L950.
47. Sévigny J, Levesque FP, Grondin G Beaudoin AR (1997) Purification of the blood vessel ATP diphosphohydrolase, identification and localization by immunological techniques. Biochim Biophys Acta 1334, 73 88.
48. Sévigny J, Robson SC, Waelkens E, Csizmadia E, Smith RN Lemmens R (2000) Identification and characterization of a novel hepatic canalicular ATP diphosphohydrolase. J Biol Chem 275, 5640 5647.
49. Lemmens R, Vanduffel L, Kittel A, Beaudoin AR, Benrezzak O Sévigny J (2000) Distribution, cloning, and characterization of porcine nucleoside triphosphate diphosphohydrolase-1. Eur J Biochem 267, 4106 4114.
50. Christoforidis S, Papamarcaki T, Galaris D, Kellner R Tsolas O (1995) Purification and properties of human placental ATP diphosphohydrolase. Eur J Biochem 234, 66 74.
51. Fausther M, Lecka J, Kukulski F, Lévesque SA, Pelletier J, Zimmermann H, Dranoff JA Sévigny J (2007) Cloning, purification and identification of the liver canalicular ecto-ATPase as NTPDase8. Am J Physiol Gastrointest Liver Physiol 292, G785 G795.
52. Bigonnesse F, Lévesque SA, Kukulski F, Lecka J, Robson SC, Fernandes MJG Sévigny J (2004) Cloning and characterization of mouse nucleoside triphosphate diphosphohydrolase-8. Biochemistry 43, 5511 5519.
53. Brunschweiger A, Iqbal J, Umbach F, Scheiff AB, Munkonda MN, Sevigny J, Knowles AF Muller CE (2008) Selective nucleoside triphosphate diphosphohydrolase-2 (NTPDase2) inhibitors: nucleotide mimetics derived from uridine-5′-carboxamide. J Med Chem 51, 4518 4528.
54. Crawford AR, Gaddie KJ, Smith TM Kirley TL (2007) Characterization of an alternative splice variant of human nucleoside triphosphate diphosphohydrolase 3 (NTPDase3): a possible modulator of nucleotidase activity and purinergic signaling. Arch Biochem Biophys 457, 7 15.
55. Zebisch M Strater N (2008) Structural insight into signal conversion and inactivation by NTPDase2 in purinergic signaling. Proc Natl Acad Sci USA 105, 6882 6887.
56. Lavoie EG, Fausther M Sévigny J (2008) Regulation of insulin secretion by NTPDase3. Purinergic Signal 4, S50.
57. Kaczmarek E, Koziak K, Sévigny J, Siegel JB, Anrather J, Beaudoin AR, Bach FH Robson SC (1996) Identification and characterization of CD39 vascular ATP diphosphohydrolase. J Biol Chem 271, 33116 33122.
58. Knowles AF Chiang WC (2003) Enzymatic and transcriptional regulation of human ecto-ATPase/E-NTPDase 2. Arch Biochem Biophys 418, 217 227.
59. Bradford MM (1976) A rapid and sensitive method for quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72, 248 254.
60. Braun N, Sévigny J, Mishra SK, Robson SC, Barth SW, Gerstberger R, Hammer K Zimmermann H (2003) Expression of the ecto-ATPase NTPDase2 in the germinal zones of the developing and adult rat brain. Eur J Neurosci 17, 1355 1364.
61. Baykov AA, Evtushenko OA Avaeva SM (1988) A malachite green procedure for orthophosphate determination and its use in alkaline phosphatase-based enzyme immunoassay. Anal Biochem 171, 266 270.
62. Smith TM Kirley TL (1999) Site-directed mutagenesis of a human brain ecto-apyrase: evidence that the E-type ATPases are related to the actin/heat shock 70/sugar kinase superfamily. Biochemistry 38, 321 328.