Abstract
Ecto-enzymes can be defined as membrane-bound proteins that have their active site facing the extracellular millieu. In trypanosomatids, the physiological roles of these enzymes remain to be completed elucidated; however, many important events have already been related to them, such as the survival of parasites during their complex life cycle and the successful establishment of host infection. This chapter focuses on two remarkable classes of ecto-enzymes: ecto-nucleotidases and ecto-phosphatases, summarizing their occurrence and possible physiological roles in Leishmania and Trypanosoma genera. Ecto-nucleotidases are characterized by their ability to hydrolyze extracellular nucleotides, playing an important role in purinergic signaling. By the action of these ecto-enzymes, parasites are capable of modulating the host immune system, which leads to a successful parasite infection. Furthermore, ecto-nucleotidases are also involved in the purine salvage pathway, acting in the generation of nucleosides that are able to cross plasma membrane via specialized transporters. Another important ecto-enzyme present in a vast number of pathogenic organisms is the ecto-phosphatase. These enzymes are able to hydrolyze extracellular phosphorylated substrates, releasing free inorganic phosphate that can be internalized by the cell, crossing the plasma membrane through a Pi-transporter. Ecto-phosphatases are also involved in the invasion and survival of parasite in the host cells. Several alternative functions have been suggested for these enzymes in parasites, such as participation in their proliferation, differentiation, nutrition and protection. In this context, the present chapter provides an overview of recent discoveries related to the occurrence of ecto-nucleotidase and ecto-phosphatase activities in Leishmania and Trypanosoma parasites.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Abbreviations
- 2′NMP:
-
Nucleoside 2′monophosphate
- 3′AMP:
-
Adenosine 3′monophosphate
- 3′NMP:
-
Nucleoside 3′monophosphate
- 5′(deoxy)NMP:
-
Deoxynucleoside 5′monophosphate
- ACR:
-
Apyrase conserved region
- ADO:
-
Adenosine
- ADP:
-
Adenosine diphosphate
- AMP:
-
Adenosine monophosphate
- ATP:
-
Adenosine triphosphate
- cAMP:
-
Cyclic adenosine monophosphate
- cGMP:
-
Cyclic guanosine monophosphate
- CMP:
-
Cytosine monophosphate
- CTP:
-
Cytosine triphosphate
- DC:
-
Dendritic cell
- DIDS:
-
4,4′-diisothiocyanostylbene 2′-2′-disulfonic acid
- DNA:
-
Deoxyribonucleic acid
- Ecto-3′NT/NU:
-
Ecto-3′nucleotidase/nuclease
- Ecto-5′NT:
-
Ecto-5′nucleotidase
- E-NPP:
-
Ecto-nucleotide pyrophosphatase/phosphodiesterase
- E-NTPDase:
-
Ectonucleoside triphosphate diphosphohydrolase
- GMP:
-
Guanosine monophosphate
- GPI:
-
Glycosyl phosphatidyl inositol
- GTP:
-
Guanosine triphosphate
- IFN-γ:
-
Interferon-γ
- IL:
-
Interleukine
- IMP:
-
Inosine monophosphate
- ITP:
-
Inosine triphosphate
- NDP:
-
Nucleoside diphosphate
- NO:
-
Nitric oxide
- NTP:
-
Nucleoside triphosphate
- P1:
-
Adenosine receptor
- P2:
-
ATP receptor
- PFTM:
-
Purine free trypanosome medium
- PHO pathway:
-
Phosphate signal-transduction pathway
- PHP:
-
Phosphohistidine phosphatase
- Pi:
-
Inorganic phosphate
- PP:
-
Phosphoserine/threonine phosphatase
- PTP:
-
Phosphotyrosine phosphatase
- RNA:
-
Ribonucleic acid
- ROS:
-
Reactive oxygen species
- TNF-α:
-
Tumor necrosis factor-α
- TTP:
-
Thymidine triphosphate
- TYR:
-
Tyrosine
- UDP:
-
Uridine diphosphate
- UMP:
-
Uridine monophosphate
- UTP:
-
Uridine triphosphate
References
Aguirre-GarcÃa MM, Anaya-Ruiz M, Talamas-Rohana P (2002) Membrane-bound acid phosphatase (MAP) from Entamoeba histolytica has phosphotyrosine phosphatase activity and disrupts the actin cytoskeleton of host cells. Parasitology 126:195–202
Aguirre-GarcÃa MM, Escalona-Montaño AR, Bakalara N et al (2006) Leishmania major: detection of membrane-bound protein tyrosine phosphatase. Parasitology 132:641–649
Anand A, Srivastava PK (2012) A molecular description of acid phosphatase. Appl Biochem Biotechnol 167:2174–2197
Anaya-Ruiz M, Perez-Santos JLM, Talamas-Rohana P (2003) An ecto-protein tyrosine phosphatase of Entamoeba histolytica induces cellular detachment by disruption of actin filaments in HeLa cells. Int J Parasitol 33:663–670
Andreeva AV, Kutuzov MA (2008) Protozoan protein tyrosine phosphatases. Int J Parasitol 38:1279–1295
Andrews PD, Stark MJR (2000) Type 1 protein phosphatase is required for maintenance of cell wall integrity, morphogenesis and cell cycle progression in Saccharomyces cerevisiae. J Cell Sci 113:507–520
Asai T, Miura S, Sibley LD et al (1995) Biochemical and molecular characterization of nucleoside triphosphate hydrolase isozymes from the parasitic protozoan Toxoplasma gondii. J Biol Chem 270:11391–11397
Auesukaree C, Homma T, Tochio H et al (2004) Intracellular phosphate serves as a signal for the regulation of the PHO pathway in Saccharomyces cerevisiae. J Biol Chem 279:17289–17294
Bakalara N, Santarelli X, Davis C et al (2000) Purification, cloning, and characterization of an acidic ectoprotein phosphatase differentially expressed in the infectious bloodstream form of Trypanosoma brucei. J Biol Chem 275:8863–8871
Berrêdo-Pinho M, Peres-Sampaio CE, Chrispim PPM et al (2001) A Mg-dependent ecto-ATPase in Leishmania amazonensis and its possible role in adenosine acquisition and virulence. Arch Biochem Biophys 391:16–24
Berriman M, Ghedin E, Hertz-Fowler C et al (2005) The genome of the African trypanosome Trypanosoma brucei. Science 309:416–422
Bisaggio DF, Peres-Sampaio CE, Meyer-Fernandes JR et al (2003) Ecto-ATPase activity on the surface of Trypanosoma cruzi and its possible role in the parasite-host cell interaction. Parasitol Res 91:273–282
Bowman EJ, Siebers A, Altendorf K (1988) Bafilomycins: a class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proc Natl Acad Sci USA 85:7972–7976
Brown PH, Ho THD (1986) Barley aleurone layers secrete a nuclease in response to gibberellic acid: purification and partial characterization of the associated ribonuclease, deoxyribonuclease, and 3′-nucleotidase activities. Plant Physiol 82:801–806
Burnstock G (2012) Purinergic signalling: its unpopular beginning, its acceptance and its exciting future. Bioessays 34:218–225
Burnstock G, Ralevic V (1998) Receptors for purines and pyrimidines. Pharmacol Rev 50:413–492
Bushfield M, Shoshani I, Johnson RA (1990) Tissue levels, source, and regulation of 3′-AMP: an intracellular inhibitor of adenylyl cyclases. Mol Pharmacol 38:848–853
Camici G, Manao G, Cappugi G et al (1989) The complete amino acid sequence of the low molecular weight cytosolic acid phosphatase. J Biol Chem 264:2560–2567
Carter NS, Yates P, Arendt CS et al (2008) Purine and pyrimidine metabolism in Leishmania. In: Majumder HK (ed) Drug targets in kinetoplastid parasites. Landes Bioscience and Springer Science+Business Media, New York
Caruso-Neves C, Meyer-Fernandes JR, Saad-Nehme et al (1998a) Ouabain-insensitive Na(+)-ATPase activity of malpighian tubules from Rhodnius prolixus. Comp Biochem Physiol B Biochem Mol Biol 119:807–811
Caruso-Neves C, Meyer-Fernandes JR, Saad-Nehme J et al (1998b) Osmotic modulation of the ouabain-sensitive (Na+, K+)ATPase from malpighian tubules of Rhodnius prolixus. Z Naturforsch C 53:911–917
Coimbra ES, Gonçalves-Da-Costa SC, Costa BLS et al (2008) A Leishmania (L.) amazonensis ATP diphosphohydrolase isoform and potato apyrase share epitopes: antigenicity and correlation with disease progression. Parasitology 135:327–335
Collopy-Junior I, Esteves FF, Nimrichter L et al (2006) An ectophosphatase activity in Cryptococcus neoformans. FEMS Yeast Res 6:1010–1017
Cosentino-Gomes D, Meyer-Fernandes JR (2011) Ecto-phosphatases in protozoan parasites: possible roles in nutrition, growth and ROS sensing. J Bioenerg Biomembr 43:89–92
Cosentino-Gomes D, Russo-Abrahão T, Fonseca-de-Souza AL et al (2009) Modulation of Trypanosoma rangeli ecto-phosphatase activity by hydrogen peroxide. Free Radic Biol Med 47:152–158
Cosentino-Gomes D, Rocco-Machado N, Santi L et al (2013) Inhibition of ecto-phosphatase activity in conidia reduces adhesion and virulence of Metarhizium anisopliae on the host insect Dysdercus peruvianus. Curr Microbiol 66:467–474
Coutinho-Silva R, Ojcius DM (2012) Role of extracellular nucleotides in the immune response against intracellular bacteria and nucleotides in the immune response against intracellular bacteria and protozoan parasites. Microbes Infect 14:1271–1277
Cunningham AC (2002) Parasitic adaptive mechanisms in infection by Leishmania. Exp Mol Pathol 72:132–141
De Almeida-Amaral EE, Belmont-Firpo R, Vannier-Santos MA et al (2006) Leishmania amazonensis: characterization of an ecto-phosphatase activity. Exp Parasitol 114:334–340
de Souza LM, Thomaz R, Fonseca FV et al (2007) Trypanosoma brucei brucei: biochemical characterization of ecto-nucleoside triphosphate diphosphohydrolase activities. Exp Parasitol 115:315–323
de Souza MC, de Assis EA, Gomes RS et al (2010) The influence of ecto-nucleotidases on Leishmania amazonensis infection and immune response in C57B/6 mice. Acta Trop 115:262–269
Debrabant A, Gottlieb M, Dwyer DM (1995) Isolation and characterization of the gene encoding the surface membrane 3′-nucleotidase/nuclease of Leishmania donovani. Mol Biochem Parasitol 71:51–63
Debrabant A, Ghedin E, Dwyer DM (2000) Dissection of the functional domains of the Leishmania surface membrane 3′-nucleotidase/nuclease, a unique member of the class I nuclease family. J Biol Chem 275:16366–16372
Debrabant A, Bastien P, Dwyer DM (2001) A unique surface membrane anchored purine-salvage enzyme is conserved among a group of primitive eukaryotic human pathogens. Mol Cell Biochem 220:109–116
Denu JM, Stuckey JA, Saper MA et al (1996) Form and function in protein dephosphorylation. Cell 87:361–364
Di Virgilio F (2007) Purinergic signalling in the immune system. A brief update. Purinergic Signal 3:1–3
Dick CF, Dos Santos AL, Fonseca-de-Souza AL et al (2010) Trypanosoma rangeli: differential expression of ecto-phosphatase activities in response to inorganic phosphate starvation. Exp Parasitol 124:386–393
Dick CF, Dos Santos AL, Majerowicz D et al (2012) Na+-dependent and Na+-independent mechanisms for inorganic phosphate uptake in Trypanosoma rangeli. Biochim Biophys Acta 1820:1001–1008
Dos Santos AL, Dick CF, Alves-Bezerra M et al (2012) Interaction between Trypanosoma rangeli and the Rhodnius prolixus salivary gland depends on the phosphotyrosine ecto-phosphatase activity of the parasite. Int J Parasitol 42:819–827
Dutra PM, Rodrigues CO, Jesus JB et al (1998) A novel ecto-phosphatase activity of Herpetomonas muscarum muscarum inhibited by platelet-activating factor. Biochem Biophys Res Commun 253:164–169
Dutra PML, Dias FA, Santos MAA et al (2001) Secreted phosphatase activities in trypanossomatid parasites of plants modulated by patelet-activating factor. Phytopathology 91:408–414
Dutra PM, Couto LC, Lopes AH et al (2006) Characterization of ecto-phosphatase activities of Trypanosoma cruzi: a comparative study between Colombiana and Y strains. Acta Trop 100:88–95
Egloff MP, Cohen PT, Reinemer P et al (1995) Crystal structure of the catalytic subunit of human protein phosphatase 1 and its complex with tugstate. J Mol Biol 254:924–959
Ennes-Vidal V, Castro RO, Britto C et al (2011) CrATP interferes in the promastigote-macrophage interaction in Leishmania amazonensis infection. Parasitology 138:960–968
Escalona-Montaño AR, Pardavé-Alejandr D, Cervantes-Sarabia R et al (2010) Leishmania mexicana promastigotes secrete a protein tyrosine phosphatase. Parasitol Res 107:309–315
Faria-Pinto R, Rezende-Soares FA, Molica AM et al (2008) Mapping of the conserved antigenic domains shared between potato apyrase and parasites ATP diphosphohydrolases: potential application in human parasitic diseases. Parasitology 135:943–953
Felicioli RA, Senesi S, Marmocchi F et al (1973) Nucleoside phosphomonoesterases during growth cycle of Bacillus subtilis. Biochemistry 12:547–552D
Fernandes EC, Meyer-Fernandes FR, Silva-Neto MAC (1997) Trypanosoma brucei: ecto-phosphatase activity on the surface of intact procyclic forms. Z Naturforsch 52C:351–358
Fernandes EC, Granjeiro JM, Aoyama H et al (2003a) A metallo phosphatase activity present on the surface of Trypanosoma brucei procyclic forms. Vet Parasitol 118:19–23
Fernandes EC, Granjeiro JM, Mikio Taga E et al (2003b) Phosphatase activity characterization on the surface of intact bloodstream forms of Trypanosoma brucei. FEMS Microbiol Lett 220:197–206
Fernandes AC, Soares DC, Saraiva EM et al (2013) Different secreted phosphatase activities in Leishmania amazonensis. FEMS Microbiol Lett 340:117–128
Fietto JL, De Marco R, Nascimento IP et al (2004) Characterization and immunolocalization of an NTP diphosphohydrolase of Trypanosoma cruzi. Biochem Biophys Res Commun 316:454–460
Fonseca FV, Fonseca-de-Souza AL, Mariano AC et al (2006) Trypanosoma rangeli: characterization of a Mg-dependent ecto-ATP-diphosphohydrolase activity. Exp Parasitol 112:76–84
Fonseca-de-Souza AL, Dick CF, Dos Santos ALA et al (2008) A Mg(2+)-dependent ecto-phosphatase activity on the external surface of Trypanosoma rangeli modulated by exogenous inorganic phosphate. Acta Trop 107:153–158
Fonseca-de-Souza AL, Dick CF, dos Santos AL et al (2009) Trypanosoma rangeli: a possible role for ecto-phosphatase activity on cell proliferation. Exp Parasitol 122:242–246
Furuya T, Zhong L, Meyer-Fernandes JR et al (1998) Ecto-protein tyrosine phosphatase activity in Trypanosoma cruzi infective stages. Mol Biochem Parasitol 92:339–348
Gbenle GO, Dwyer DM (1992) Purification and properties of 3′-nucleotidase of Leishmania donovani. Biochem J 285:41–46
Gbenle GO, Opperdoes FR, Van Roy J (1986) Localization of 3′-nucleotidase and calcium-dependent endoribonuclease in the plasma-membrane of Trypanosoma brucei. Acta Trop 43:295–305
Goding JW (2000) Ecto-enzymes: physiology meets pathology. J Leukoc Biol 67:285–311
Gomes SA, Fonseca-de-Souza AL, Silva BA et al (2006) Trypanosoma rangeli: differential expression of cell surface polypeptides and ecto-phosphatase activity in short and long epimastigote forms. Exp Parasitol 112:253–262
Gomes MT, Lopes AH, Meyer-Fernandes JR (2011) Possible roles of ectophosphatases in host-parasite interactions. J Parasitol Res 2011:1–7
Gottilieb M, Dwyer DM (1982) Identification and partial characterization of an extracellular acid phosphatase activity of Leishmania donovani promastigotes. Mol Cell Biol 2:76–81
Gottlieb M (1989) The surface membrane 3′-nucleotidase/nuclease of trypanosomatid protozoa. Parasitol Today 5:257–260
Gottlieb M, Cohn CS (1997) The acquisition of purines by trypanosomatids. Parasitol Today 13:231–235
Gottlieb M, Dwyer DM (1981) Protozoan parasite of humans: surface membrane with externally disposed acid phosphatase. Science 212:939–941
Gottlieb M, Dwyer DM (1983) Evidence for distinct 5′- and 3′-nucleotidase activities in the surface membrane fraction of Leishmania donovani promastigotes. Mol Biochem Parasitol 7:303–311
Gottlieb M, Gardiner PR, Dwyer DM (1986) 3′-nucleotidase activity in procyclic and bloodstream stages of Trypanosoma rhodesiense. Comp Biochem Physiol B 83:63–69
Hammond AJ, Gutteridge WE (1984) Purine and pyrimidine metabolism in the trypanosomatidae. Mol Biochem Parasitol 13:242–261
Heneberg P (2012) Finding the smoking gun: protein tyrosine phosphatases as tools and targets of unicellular microorganisms and viruses. Curr Med Chem 19:1530–1566
Hertog D, Groen A, Van der Wijk T (2005) Redox regulation of protein-tyrosine phosphatases. Arch Biochem Biophys 434:11–15
Hourani SM, Chown JA (1989) The effects of some possible inhibitors of ectonucleotidases on the breakdown and pharmalogical effects of ATP in the guinea-pig urinary bladder. Gen Pharmacol 20:413–416
Ivanov MI, Stuckey JA, Schubert HL et al (2005) Two substrate-targeting sites in the Yersinia protein tyrosine phosphatase co-operate to promote bacterial virulence. Mol Microbiol 55:1346–1356
Jadin JM, Creemers J (1972) The role of excretion of acid phosphatase in Trypanosoma brucei and T. cruzi. Trans R Soc Trop Med Hyg 66:8–9
Jaffe CL, Perez LM, Schunur LF (1990) Lipophosphoglycan and secreted acid phosphatase of Leishmania tropica share species-specific epitopes. Mol Biochem Parasitol 41:233–240
Jedrzejas MJ (2000) Structure, function, and evolution of phosphoglycerate mutases: comparison with fructose-2,6-bisphosphatase, acid phosphatase, and alkaline phosphatase. Prog Biophys Mol Biol 73:263–287
Junger WG (2011) Immune cell regulation by autocrine purinergic signaling. Nat Rev Immunol 11:201–212
Kiffer-Moreira T, de Sá Pinheiro AA, Alviano WS et al (2007) An ecto-phosphatase activity in Candida parapsilosis influences the interaction of fungi with epithelial cells. FEMS Yeast Res 7:621–628
Klumpp S, Krieglstein J (2002) Phosphorylation and dephosphorylation of histidine residues on proteins. Eur J Biochem 269:1067–1071
Kneipp LF, Rodrigues ML, Holandino C et al (2004) Ectophosphatase activity in conidial forms of Fonsecaea pedrosoi is modulated by exogenous phosphate and influences fungal adhesion to mammalian cells. Microbiology 150:3355–3362
Kneipp LF, Magalhães AS, Abi-Chacra EA et al (2012) Surface phosphatase in Rhinocladiella aquaspersa: biochemical properties and its involvement with adhesion. Med Mycol 50:570–578
Knowles AF, Li C (2006) Molecular cloning and characterization of expressed human ecto-nucleoside triphosphate diphosphohydrolase 8 (E-NTPDase 8) and its soluble extracellular domain. Biochemistry 45:7323–7333
Kouni MH (2003) Potential chemotherapeutic targets in the purine metabolism of parasites. Pharmacol Ther 99:283–309
Kowalske D, Kroeker WD, Laskowski M (1976) Mung bean nuclease I. physical, chemical, and catalytic properties. Biochemistry 15:4457–4463
Kutuzov MA, Andreeva AV (2008) Protein Ser/Thr phosphatases of parasitic protozoa. Mol Biochem Parasitol 161:81–90
Lakhal-Naouar I, Ben Achour-Chenik Y, Boublik Y et al (2008) Identification and characterization of a new Leishmania major specific 3′nucleotidase/nuclease protein. Biochem Biophys Res Commun 375:54–58
Leite PM, Gomes RS, Figueiredo AB et al (2012) Ecto-nucleotidase activities of promastigotes from Leishmanis (Viannia) braziliensis relates to parasite infectivity and disease clinical outcome. PLoS Negl Trop Dis 6:e1850
Maia AC, Porcino GN, Detoni MD et al (2013) An antigenic domain within a catalytically active Leishmania infantum nucleoside triphosphate diphosphohydrolase (NTPDase 1) is a target of inhibitory antibodies. Parasitol Int 62:44–52
Maioli TU, Takane E, Arantes RM et al (2004) Immune response induced by New World Leishmania species in C57BL/6 mice. Parasitol Res 94:207–212
Marques-da-Silva EA, Oliveira JC, Figueiredo AB et al (2008) Extracellular nucleotide metabolism in Leishmania: influence of adenosine in the establishment of infection. Microbes Infect 10:850–857
Martiny A, Vannier-Santos MA, Borges VM (1996) Leishmania-induced tyrosine phosphorylation in the host macrophage and its implication to infection. Eur J Cell Biol 71:206–215
McLaughlin J (1986) The association of distinct acid phosphatases with the flagella pocket and surface membrane fractions obtained from bloodstream forms of Trypanosoma rhodesiense. Mol Cell Biochem 70:177–184
Menz B, Winter G, Ilg T et al (1991) Purification and characterization of a membrane-bound acid phosphatase of Leishmania Mexicana. Mol Biochem Parasitol 47:101–108
Meyer-Fernandes JR (2002) Ecto-ATPases in protozoa parasites: looking for a function. Parasitol Int 51:299–303
Meyer-Fernandes JR, Dutra PML, Rodrigues CO et al (1997) Mg-dependent ecto-ATPase activity in Leishmania tropica. Arch Biochem Biophys 341:40–46
Meyer-Fernandes JR, Da Silva-Neto MA, Dos Santo SM (1999) Ecto-phosphatase activities on the cell surface of the amastigote forms of Trypanosoma cruzi. Z Naturforsch 54:977–984
Meyer-Fernandes JR, Saad-Nehme J, Peres-Sampaio CE et al (2004) A Mg-dependent ecto-ATPase is increased in the infective stages of Trypanosoma cruzi. Parasitol Res 93:41–50
Meyer-Fernandes JR, Cosentino-Gomes D, Vieira DP et al (2010) Ecto-nucleoside triphosphate diphosphohydrolase activities in trypanosomatids: possible roles in infection, virulence and purine recycling. Open Parasitol J 4:116–119
Mikalsen SO, Kaalhus O (1998) Properties of per-vanadate and permolybdate. J Biol Chem 273:10036–10045
Moreira OC, Rios PF, Esteves FF et al (2009) CrATP as a new inhibitor of ectoATPases of trypanosomatids. Parasitology 136:35–44
Nakaas V, Beckers CJ, Polotsky V et al (1998) Basis for substrate specificity of the Toxoplasma gondii nucleoside triphosphate hydrolase. Mol Biochem Parasitol 97:209–220
Nakagura KH, Tachibana H, Kaneda Y (1985) Alteration of the cell surface acid phosphatase concomitant with morphological transformation in Trypanosoma cruzi. Comp Biochem Physiol 81B:815–817
Nascimento M, Zhang W, Ghosh A et al (2006) Identification and characterization of a protein-tyrosine phosphatase in Leishmania: involvement in virulence. J Biol Chem 281:36257–36268
Ogawa N, De Risi J, Brown PO (2000) New components of a system for phosphate accumulation and polyphosphate metabolism in Saccharomyces cerevisiae revealed by genomic expression analysis. Mol Biol Cell 11:4309–4321
Olson AE, Janski AM, Fahrlander PD et al (1982) Nuclease I from suspension-cultured Nicotiana tabacum: purification and properties of the extracellular enzyme. Arch Biochem Biophys 216:223–233
Oshima Y (1997) The phosphatase system in Saccharomyces cerevisiae. Genes Genet Syst 72:323–334
Oshima Y, Ogawa N, Harashima S (1996) Regulation of phosphatase synthesis in saccharomyces cerevisiae – a review. Gene 179:171–177
Paletta-Silva R, Meyer-Fernandes JR (2012) Adenosine and immune imbalance in visceral leishmaniasis: the possible role of ectonucleotidases. J Trop Med 2012:1–6
Paletta-Silva R, Vieira DP, Vieira-Bernardo R et al (2011) Leishmania amazonensis: characterization of an ecto-3′-nucleotidase activity and its possible role in virulence. Exp Parasitol 129:277–283
Peacock CS, Seeger K, Harris D et al (2007) Comparative genomic analysis of three Leishmania species that cause diverse human disease. Nat Genet 39:839–847
Peres-Sampaio CE, Palumbo ST, Meyer-Fernandes JR (2001) An ecto-ATPase activity present is Leishmania tropica stimulated by dextran Sulfate. Z Naturforsch C 56:820–825
Peres-Sampaio CE, de Almeida-Amaral EE, Giarola NL et al (2008) Leishmania amazonensis: effects of heat shock on ecto-ATPase activity. Exp Parasitol 119:135–143
Persson BL, Petersson J, Fristedt U (1999) Phosphate permeases of Saccharomyces cerevisiae: structure, function and regulation. Biochim Biophys Acta 1422:255–272
Pinheiro CM, Martins-Duarte ES, Ferraro RB et al (2006) Leishmania amazonensis: biological and biochemical characterization of ectonucleoside triphosphate diphosphohydrolase activities. Exp Parasitol 114:16–25
Porcino GN, Carvalho-Campos C, Maia AC et al (2012) Leishmania (Viannia) braziliensis nucleoside triphosphate diphosphohydrolase (NTPDase 1): localization and in vitro inhibition of promastigotes growth by polyclonal antibodies. Exp Parasitol 132:293–309
Portela MB, Kneipp LF, Souza IPR et al (2010) Ectophosphatase activity in Candida albicans influences fungal adhesion: study between HIV-positive and HIV-negative isolates. Oral Dis 16:431–437
Remaley AT, Kuhns DB, Basford RE et al (1984) Leishmanial phosphatase blocks neutrophil O-2 production. J Biol Chem 259:11173–11175
Remaley AT, Glew RH, Kuhns DB et al (1985) Leishmania donovani: surface membrane acid phosphatase blocks neutrophils oxidative metabolite production. Exp Parasitol 60:331–341
Rezende-Soares FA, Carvalho-Campos C, Marques MJ et al (2010) Cytochemical localization of ATP diphosphohydrolase from Leishmania (Viannia) braziliensis promastigotes and identification of an antigenic and catalytically active isoform. Parasitology 137:773–783
Robson SC, Sévigny J, Zimmermann H (2006) The E-NTPDase family of ectonucleotidases: structure function relationships and pathophysiological significance. Purinergic Signal 2:409–430
Rodden JL, Scocca JJ (1972) Purification and properties of cyclic phosphodiesterase: 3′nucleotidase, a periplasmic enzyme of Haemophilus influenzae. Arch Biochem Biophys 153:837–844
Rodrigues CO, Dutra PM, Barros FS (1999) Platelet-activating factor induction of secreted phosphatase activity in Trypanosoma cruzi. Biochem Biophys Res Commun 266:36–42
Russo-Abrahão T, Alves-Bezerra M, Majerowicz D et al (2013) Transport of inorganic phosphate in Leishmania infantum and compensatory regulation at low inorganic phosphate concentration. Biochim Biophys Acta 1830:2683–2689
Saha AK, Das S, Glew RH et al (1985) Resistance of leishmanial phosphatases to inactivation by oxygen metabolites. J Clin Microbiol 22:329–332
Sansom F (2012) The role of the NTPDase enzyme family in parasites: what do we know, and where to from here? Parasitology 139:963–980
Sansom FM, Robson SC, Hartland EL (2008) Possible effects of microbial ecto-nucleoside triphosphate diphosphohydrolases on host-pathogen interactions. Microbiol Mol Biol Rev 72:765–781
Santos ALS, Souto-Padrón T, Alviano CS et al (2002) Secreted phosphatase activity induced by dimethylsulfoxide in Herpetomonas samuelpessoai. Arch Biochem Biophys 405:191–198
Santos RF, Pôssa MA, Bastos MS et al (2009) Influence of ecto-nucleoside triphosphate diphosphohydrolase activity on Trypanosoma cruzi infectivity and virulence. PLoS Negl Trop Dis 3:e387
Scheibe RJ, Kuehl H, Krautwald S et al (2000) Ecto-alkaline phosphatase activity identified at physiological pH range on intact P19 and HL-60 cells is induced by retinoic acid. J Cell Biochem 76:420–436
Shakarian AM, Joshi MB, Ghedin E et al (2002) Molecular dissection of the functional domains of a unique, tartrate-resistant, surface membrane acid phosphatase in the primitive human pathogen Leishmania donovani. J Biol Chem 277:17994–18001
Shimada K, Sugino Y (1969) Cyclic phosphodiesterase having 3′nucleotidase activity from Bacillus subtilis. Purification and some properties of the enzyme. Biochim Biophys Acta 185:367–380
Shishido K, Ando T (1985) Single-strand specific nucleases. In: Linn SM, Roberts RS (eds) Nucleases. Cold Spring Harbor Laboratory, New York
Singla N, Khuller GK, Vinayak VK et al (1992) Acid phosphatase activity of promastigotes of Leishamania donovani: a marker of virulence. FEMS Microbiol Lett 94:221–226
Sopwith WF, Debrabant A, Yamageb M et al (2002) Developmentally regulated expression of a cell surface class I nuclease in Leishmania Mexicana. Int J Parasitol 32:449–459
Souza VL, Veras PS, Welby-Borges M et al (2011) Immune and inflammatory responses to Leishmania amazonensis isolated from different clinical forms of human leishmaniasis in CBA mice. Mem Inst Oswaldo Cruz 106:23–31
Steenkamp DJ (2002) Trypanosomal antioxidants and emerging aspects of redox regulation in the trypanosomatids. Antioxid Redox Signal 4:105–121
Steverding D (2005) Ubiquitination of plasma membrane ectophosphatase in bloodstream forms of Trypanosoma brucei. Parasitol Res 98:157–161
Szöör B (2010) Trypanosomatid protein phosphatases. Mol Biochem Parasitol 173:53–63
Ticconi CA, Delatorre CA, Abel S (2001) Attenuation of phosphate starvation responses by phosphite in Arabidopsis. Plant Physiol 127:963–972
Torriani A (1990) From cell membrane to nucleotides: the phosphate regulon in Escherichia coli. Bioessays 12:371–376
Tosomba OM, Coetzer THT, Lonsdale-Eccles JD (1996) Localisation of acid phosphatase activity on the surface of bloodstream forms of Trypanosoma congolense. Exp Parasitol 84:429–438
Van Belle H (1976) Alkaline phosphatase. I. Kinetics and inhibition by levamisole of purified isoenzymes from humans. Clin Chem 22:972–976
Vieira DP, Paletta-Silva R, Saraiva EM et al (2011) Leishmania chagasi: an ecto-3′-nucleotidase activity modulated by inorganic phosphate and its possible involvement in parasite-macrophage interaction. Exp Parasitol 127:702–707
Vincent JB, Crowder MW, Averill BA (1992) Hydrolysis of phosphate monoesters: a biological problem with multiple chemical solutions. Trends Biochem Sci 17:105–110
Wiese M, Berger O, Stierhof YD et al (1996) Gene cloning and cellular localization of a membrane-bound acid phosphatase of Leishmania mexicana. Mol Biochem Parasitol 82:153–165
Yegutkin GG (2008) Nucleotide- and nucleoside-converting ectoenzymes: important modulators of purinergic signaling cascade. Biochim Biophys Acta 1783:673–694
Zhan XL, Hong Y, Zhu T et al (2000) Essential functions of protein tyrosine phosphatase Ptp2 and Ptp3 and Rim11 tyrosine phosphorylation in Saccharomyces cerevisiae meiosis and sporulation. Mol Biol Cell 11:663–676
Zhong L, Lu HG, Moreno SN et al (1998) Tyrosine phosphate hydrolysis of host proteins by Trypanosoma cruzi is linked to cell invasion. FEMS Microbiol Lett 161:15–20
Ziganshin AU, Ziganshina LE, King BF, Burnstock G (1995) Characteristics of ecto-ATPase of Xenopus oocytes and the inhibitory actions of suramin on ATP breakdown. Pflugers Arch 429:412–418
Zilberstein D, Dwyer DM (1985) Protonmotive force-driven active transport of D-glucose and L-proline in the protozoan parasite Leishmania donovani. Proc Natl Acad Sci USA 82:1716–1720
Zimmermann H (2001) Ectonucleotidases: some recent developments and a note on nomenclature. Drug Dev Res 52:44–56
Zimmermann H, Beaudoin AR, Bollen M et al (2000) Nomenclature for two families of novel ecto-nucleotidases. In: Vanduffel L, Lemmens R (eds) Second international workshop on ecto-ATPases and related ecto-nucleotidase. Shaker Publishing BV Maastricht, The Netherlands
Zimmermann H, Zebisch M, Sträter N (2012) Cellular function and molecular structure of ecto-nucleotidases. Purinergic Signal 8:437–502
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2014 Springer Science+Business Media Dordrecht
About this chapter
Cite this chapter
Freitas-Mesquita, A.L., Meyer-Fernandes, J.R. (2014). Ecto-nucleotidases and Ecto-phosphatases from Leishmania and Trypanosoma Parasites. In: Santos, A., Branquinha, M., d’Avila-Levy, C., Kneipp, L., Sodré, C. (eds) Proteins and Proteomics of Leishmania and Trypanosoma. Subcellular Biochemistry, vol 74. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-7305-9_10
Download citation
DOI: https://doi.org/10.1007/978-94-007-7305-9_10
Published:
Publisher Name: Springer, Dordrecht
Print ISBN: 978-94-007-7304-2
Online ISBN: 978-94-007-7305-9
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)