Uptake of GABA in Trypanosoma cruzi
Gamma aminobutyric acid (GABA) is widely known as a neurotransmitter and signal transduction molecule found in vertebrates, plants, and some protozoan organisms. However, the presence of GABA and its role in trypanosomatids is unknown. Here, we report the presence of intracellular GABA and the bioch...
Saved in:
| Published in: | The Journal of eukaryotic microbiology Vol. 62; no. 5; pp. 629 - 636 |
|---|---|
| Main Authors: | , , , , , |
| Format: | Journal Article |
| Language: | English |
| Published: |
United States
Society of Protozoologists
01-09-2015
Blackwell Publishing Ltd |
| Subjects: | |
| Online Access: | Get full text |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| Abstract | Gamma aminobutyric acid (GABA) is widely known as a neurotransmitter and signal transduction molecule found in vertebrates, plants, and some protozoan organisms. However, the presence of GABA and its role in trypanosomatids is unknown. Here, we report the presence of intracellular GABA and the biochemical characterization of its uptake in Trypanosoma cruzi, the etiological agent of Chagas' disease. Kinetic parameters indicated that GABA is taken up by a single transport system in pathogenic and nonpathogenic forms. Temperature dependence assays showed a profile similar to glutamate transport, but the effect of extracellular cations Na⁺, K⁺, and H⁺ on GABA uptake differed, suggesting a different uptake mechanism. In contrast to reports for other amino acid transporters in T. cruzi, GABA uptake was Na⁺ dependent and increased with pH, with a maximum activity at pH 8.5. The sensitivity to oligomycin showed that GABA uptake is dependent on ATP synthesis. These data point to a secondary active Na⁺/GABA symporter energized by Na⁺‐exporting ATPase. Finally, we show that GABA occurs in the parasite's cytoplasm under normal culture conditions, indicating that it is regularly taken up from the culture medium or synthesized through an still undescribed metabolic pathway. |
|---|---|
| AbstractList | Gamma aminobutyric acid (
GABA
) is widely known as a neurotransmitter and signal transduction molecule found in vertebrates, plants, and some protozoan organisms. However, the presence of
GABA
and its role in trypanosomatids is unknown. Here, we report the presence of intracellular
GABA
and the biochemical characterization of its uptake in
Trypanosoma cruzi
, the etiological agent of Chagas' disease. Kinetic parameters indicated that
GABA
is taken up by a single transport system in pathogenic and nonpathogenic forms. Temperature dependence assays showed a profile similar to glutamate transport, but the effect of extracellular cations Na
+
, K
+
, and H
+
on
GABA
uptake differed, suggesting a different uptake mechanism. In contrast to reports for other amino acid transporters in
T. cruzi
,
GABA
uptake was Na
+
dependent and increased with
pH
, with a maximum activity at
pH
8.5. The sensitivity to oligomycin showed that
GABA
uptake is dependent on
ATP
synthesis. These data point to a secondary active Na
+
/
GABA
symporter energized by Na
+
‐exporting
ATP
ase. Finally, we show that
GABA
occurs in the parasite's cytoplasm under normal culture conditions, indicating that it is regularly taken up from the culture medium or synthesized through an still undescribed metabolic pathway. Gamma aminobutyric acid (GABA) is widely known as a neurotransmitter and signal transduction molecule found in vertebrates, plants, and some protozoan organisms. However, the presence of GABA and its role in trypanosomatids is unknown. Here, we report the presence of intracellular GABA and the biochemical characterization of its uptake in Trypanosoma cruzi, the etiological agent of Chagas' disease. Kinetic parameters indicated that GABA is taken up by a single transport system in pathogenic and nonpathogenic forms. Temperature dependence assays showed a profile similar to glutamate transport, but the effect of extracellular cations Na(+) , K(+) , and H(+) on GABA uptake differed, suggesting a different uptake mechanism. In contrast to reports for other amino acid transporters in T. cruzi, GABA uptake was Na(+) dependent and increased with pH, with a maximum activity at pH 8.5. The sensitivity to oligomycin showed that GABA uptake is dependent on ATP synthesis. These data point to a secondary active Na(+) /GABA symporter energized by Na(+) -exporting ATPase. Finally, we show that GABA occurs in the parasite's cytoplasm under normal culture conditions, indicating that it is regularly taken up from the culture medium or synthesized through an still undescribed metabolic pathway. Gamma aminobutyric acid (GABA) is widely known as a neurotransmitter and signal transduction molecule found in vertebrates, plants, and some protozoan organisms. However, the presence of GABA and its role in trypanosomatids is unknown. Here, we report the presence of intracellular GABA and the biochemical characterization of its uptake in Trypanosoma cruzi, the etiological agent of Chagas' disease. Kinetic parameters indicated that GABA is taken up by a single transport system in pathogenic and nonpathogenic forms. Temperature dependence assays showed a profile similar to glutamate transport, but the effect of extracellular cations Na⁺, K⁺, and H⁺ on GABA uptake differed, suggesting a different uptake mechanism. In contrast to reports for other amino acid transporters in T. cruzi, GABA uptake was Na⁺ dependent and increased with pH, with a maximum activity at pH 8.5. The sensitivity to oligomycin showed that GABA uptake is dependent on ATP synthesis. These data point to a secondary active Na⁺/GABA symporter energized by Na⁺‐exporting ATPase. Finally, we show that GABA occurs in the parasite's cytoplasm under normal culture conditions, indicating that it is regularly taken up from the culture medium or synthesized through an still undescribed metabolic pathway. |
| Author | Suárez Mantilla, Brian Ahn, Il‐Young Pral, Elizabeth Mieko Furusho Galvez Rojas, Robert L Silber, Ariel Mariano Sant'Anna, Celso |
| Author_xml | – sequence: 1 fullname: Galvez Rojas, Robert L – sequence: 2 fullname: Ahn, Il‐Young – sequence: 3 fullname: Suárez Mantilla, Brian – sequence: 4 fullname: Sant'Anna, Celso – sequence: 5 fullname: Pral, Elizabeth Mieko Furusho – sequence: 6 fullname: Silber, Ariel Mariano |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/25851259$$D View this record in MEDLINE/PubMed |
| BookMark | eNp1kb1OwzAURi1URH9g4AUgEgsMaW0njtOxRKWAWhhoBJvlOA5Km8TBbgTl6XFJ6YYXW9a55-p-tw86laokAOcIDpE9o5VshghjND4CPUQIdKkPw459wyBwCfb8Lugbs4IQBRihE9DFJCQIk3EPXMX1hq-lozJnNrmdOHnlLPW25pUyquSO0M13fgqOM14Yeba_ByC-my6je3f-PHuIJnNX2B5jV1JCqAh8KDMOsfAFxjyVPk0oFDCkMBuLABKaJlTsmkth_xKfhFTQIOVWMQDXrbfW6qORZsPK3AhZFLySqjEMUTsQwdgnFr1pUaGVMVpmrNZ5yfWWIch2mTCbCfvNxLIXe22TlDI9kH8hWGDUAp95Ibf_m9jjNP5Tum1Fbjby61DB9ZoF1KOEvT7N2BuOFt4CRiy0_GXLZ1wx_q5zw-IXbNdhV4Kxh5D3A8ERgaY |
| CitedBy_id | crossref_primary_10_1007_s10863_016_9665_9 crossref_primary_10_1080_23311932_2018_1534323 crossref_primary_10_3390_pathogens7020036 crossref_primary_10_1016_j_pt_2022_02_004 crossref_primary_10_1111_jeu_12278 |
| Cites_doi | 10.1590/S1517-83822012000400001 10.1371/journal.pone.0037740 10.1371/journal.pntd.0002717 10.1111/j.1574-6968.2010.01936.x 10.1371/journal.pone.0004534 10.1111/j.1574-6968.2004.tb09630.x 10.1002/emmm.201303356 10.1016/j.ijpara.2005.10.006 10.1515/znc-1998-11-1218 10.1007/BF01945511 10.1895/wormbook.1.14.1 10.1111/j.1574-6968.2004.tb09788.x 10.2174/09298673113209990228 10.1016/S0074-7696(02)13011-7 10.1016/j.femsle.2005.04.029 10.1002/yea.2948 10.1007/s00726-010-0812-z 10.1002/nbm.1323 10.1128/IAI.00138-09 10.1016/j.yexcr.2003.07.008 10.1073/pnas.91.17.8278 10.2174/1568005053174636 10.1016/S0140-6736(10)60061-X 10.1016/S0166-6851(01)00444-3 10.1111/j.1550-7408.2002.tb00225.x 10.1159/000338542 10.1242/jeb.039594 10.1080/15216540701200084 10.1073/pnas.1037532100 10.1016/j.bbrc.2004.07.002 10.1186/1741‐7007‐11‐67 10.1016/0166-6851(85)90073-8 10.1371/journal.pntd.0002594 10.1016/j.ejphar.2004.07.032 10.1104/pp.106.088955 10.1016/j.tcb.2003.10.001 10.1016/j.chom.2012.09.013 10.4061/2011/486928 10.1111/j.1550-7408.1999.tb05132.x 10.1371/journal.pone.0092028 10.1093/nar/gkt1097 |
| ContentType | Journal Article |
| Copyright | 2015 The Author(s) Journal of Eukaryotic Microbiology © 2015 International Society of Protistologists 2015 The Author(s) Journal of Eukaryotic Microbiology © 2015 International Society of Protistologists. |
| Copyright_xml | – notice: 2015 The Author(s) Journal of Eukaryotic Microbiology © 2015 International Society of Protistologists – notice: 2015 The Author(s) Journal of Eukaryotic Microbiology © 2015 International Society of Protistologists. |
| DBID | FBQ BSCLL CGR CUY CVF ECM EIF NPM AAYXX CITATION 7X8 |
| DOI | 10.1111/jeu.12219 |
| DatabaseName | AGRIS Istex Medline MEDLINE MEDLINE (Ovid) MEDLINE MEDLINE PubMed CrossRef MEDLINE - Academic |
| DatabaseTitle | MEDLINE Medline Complete MEDLINE with Full Text PubMed MEDLINE (Ovid) CrossRef MEDLINE - Academic |
| DatabaseTitleList | CrossRef MEDLINE MEDLINE - Academic |
| Database_xml | – sequence: 1 dbid: ECM name: MEDLINE url: https://search.ebscohost.com/login.aspx?direct=true&db=cmedm&site=ehost-live sourceTypes: Index Database |
| DeliveryMethod | fulltext_linktorsrc |
| Discipline | Zoology Biology |
| EISSN | 1550-7408 |
| EndPage | 636 |
| ExternalDocumentID | 10_1111_jeu_12219 25851259 JEU12219 ark_67375_WNG_X2CM3M0C_8 US201600122311 |
| Genre | article Research Support, Non-U.S. Gov't Journal Article |
| GrantInformation_xml | – fundername: Instituto Nacional de Biologia Estrutural e Química Medicinal em Doenças Infecciosas – fundername: Conselho Nacional de Desenvolvimento Científico e Tecnológico funderid: #2013/18970‐6; 308351/2013‐4 – fundername: Fundação de Amparo à Pesquisa do Estado de São Paulo funderid: #2013/18970‐6 |
| GroupedDBID | --- -DZ -JH -~X .3N .GA .Y3 05W 0R~ 10A 1OB 1OC 29K 31~ 33P 36B 3O- 3SF 4.4 50Y 50Z 51W 51X 52M 52N 52O 52P 52S 52T 52U 52W 52X 53G 5GY 5HH 5LA 5VS 702 7PT 8-0 8-1 8-3 8-4 8-5 85S 8UM 930 A03 AACFU AAESR AAEVG AAHHS AANLZ AAONW AAPSS AASGY AAXRX AAZKR ABCQN ABCUV ABEML ABHUG ABPTK ABPVW ACAHQ ACBWZ ACCFJ ACCZN ACGFS ACKIV ACNCT ACPOU ACPRK ACSCC ACXBN ACXME ACXQS ADAWD ADBBV ADDAD ADEOM ADHSS ADIZJ ADKYN ADMGS ADOYD ADOZA ADXAS ADZMN AEDJY AEEZP AEIGN AEIMD AENEX AEPYG AEQDE AEUQT AEUYR AFBPY AFDAS AFEBI AFFIJ AFFNX AFFPM AFGKR AFMIJ AFNWH AFPWT AFVGU AFZJQ AGCDD AGJLS AHEFC AI. AIURR AIWBW AJBDE AJXKR AKPMI ALAGY ALMA_UNASSIGNED_HOLDINGS ALUQN AMBMR AMYDB ASPBG ATUGU AUFTA AVWKF AZBYB AZFZN AZVAB BAFTC BDRZF BFHJK BHBCM BMNLL BMXJE BNHUX BROTX BRXPI BY8 CAG COF CS3 D-E D-F D-I D0L DC7 DCZOG DPXWK DR2 DRFUL DRSTM DU5 EBD EBS EJD EMB EMOBN F00 F01 F04 F5P FBQ FEDTE FSRTE FZ0 G-S G.N GODZA H.T H.X HF~ HVGLF HZI HZ~ H~9 J0M K48 L7B LATKE LC2 LC3 LEEKS LH4 LITHE LOXES LP6 LP7 LUTES LW6 LYRES MEWTI MK4 MM. MRFUL MRSTM MSFUL MSSTM MVM MXFUL MXSTM N04 N05 N9A NF~ O66 O9- OHT P2P P2W P2X P4D PALCI PQ0 Q.N Q11 Q5J QB0 R.K RBO RIWAO RJQFR ROL RX1 SAMSI SUPJJ SV3 TN5 TWZ UB1 UKR UPT VH1 W8V W99 WBKPD WH7 WIH WIK WNSPC WOHZO WQJ WRC WXSBR WYISQ XG1 XJT XOL YHZ YQT YZZ ZCG ZXP ZZTAW ~IA ~KM ~WT AAHBH AHBTC AITYG BSCLL H13 HGLYW OIG CGR CUY CVF ECM EIF NPM AAMNL AAYXX CITATION 7X8 |
| ID | FETCH-LOGICAL-c5239-e7557c640efa02c4c22ade47b70c0870f9c6057db7c5125ec870b4587c76da523 |
| IEDL.DBID | 33P |
| ISSN | 1066-5234 |
| IngestDate | Fri Aug 16 00:56:26 EDT 2024 Thu Nov 21 20:53:32 EST 2024 Sat Sep 28 07:56:07 EDT 2024 Sat Aug 24 00:59:46 EDT 2024 Wed Oct 30 09:59:09 EDT 2024 Wed Dec 27 19:15:01 EST 2023 |
| IsPeerReviewed | true |
| IsScholarly | true |
| Issue | 5 |
| Keywords | Na+/metabolite symporter Active metabolite transporters amino acids metabolism chemotherapy |
| Language | English |
| License | 2015 The Author(s) Journal of Eukaryotic Microbiology © 2015 International Society of Protistologists. |
| LinkModel | DirectLink |
| MergedId | FETCHMERGED-LOGICAL-c5239-e7557c640efa02c4c22ade47b70c0870f9c6057db7c5125ec870b4587c76da523 |
| Notes | http://dx.doi.org/10.1111/jeu.12219 ark:/67375/WNG-X2CM3M0C-8 Conselho Nacional de Desenvolvimento Científico e Tecnológico - No. #2013/18970-6; No. 308351/2013-4 ArticleID:JEU12219 Fundação de Amparo à Pesquisa do Estado de São Paulo - No. #2013/18970-6 istex:24668028D2B2F0CD5FCDC93212B338FE3A63A5B9 Instituto Nacional de Biologia Estrutural e Química Medicinal em Doenças Infecciosas ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 |
| PMID | 25851259 |
| PQID | 1710652245 |
| PQPubID | 23479 |
| PageCount | 8 |
| ParticipantIDs | proquest_miscellaneous_1710652245 crossref_primary_10_1111_jeu_12219 pubmed_primary_25851259 wiley_primary_10_1111_jeu_12219_JEU12219 istex_primary_ark_67375_WNG_X2CM3M0C_8 fao_agris_US201600122311 |
| PublicationCentury | 2000 |
| PublicationDate | September/October 2015 |
| PublicationDateYYYYMMDD | 2015-09-01 |
| PublicationDate_xml | – month: 09 year: 2015 text: September/October 2015 |
| PublicationDecade | 2010 |
| PublicationPlace | United States |
| PublicationPlace_xml | – name: United States |
| PublicationTitle | The Journal of eukaryotic microbiology |
| PublicationTitleAlternate | J. Eukaryot. Microbiol |
| PublicationYear | 2015 |
| Publisher | Society of Protozoologists Blackwell Publishing Ltd |
| Publisher_xml | – name: Society of Protozoologists – name: Blackwell Publishing Ltd |
| References | Contreras, V. T., Salles, J. M., Thomas, N., Morel, C. M. & Goldenberg, S. 1985. In vitro differentiation of Trypanosoma cruzi under chemically defined conditions. Mol. Biochem. Parasitol., 16:315-327. Canepa, G. E., Silber, A. M., Bouvier, L. A. & Pereira, C. A. 2004. Biochemical characterization of a low-affinity arginine permease from the parasite Trypanosoma cruzi. FEMS Microbiol. Lett., 236:79-84. Vassalle, M. 1987. Contribution of the Na+/K+-pump to the membrane potential. Experientia, 43:1135-1140. Inbar, E., Canepa, G. E., Carrillo, C., Glaser, F., Suter Grotemeyer, M., Rentsch, D., Zilberstein, D. & Pereira, C. A. 2012. Lysine transporters in human trypanosomatid pathogens. Amino Acids, 42:347-360. Cao, J., Barbosa, J. M., Singh, N. K. & Locy, R. D. 2013. GABA shunt mediates thermotolerance in Saccharomyces cerevisiae by reducing reactive oxygen production. Yeast, 30:129-144. Bouche, N., Lacombe, B. & Fromm, H. 2003b. GABA signaling: a conserved and ubiquitous mechanism. Trends Cell Biol., 13:607-610. Ramoino, P., Fronte, P., Beltrame, F., Diaspro, A., Fato, M., Raiteri, L., Stigliani, S. & Usai, C. 2003. Swimming behavior regulation by GABA-B receptors in Paramecium. Exp. Cell Res., 291:398-405. MacRae, J. I., Sheiner, L., Nahid, A., Tonkin, C., Striepen, B. & McConville, M. J. 2012. Mitochondrial metabolism of glucose and glutamine is required for intracellular growth of Toxoplasma gondii. Cell Host Microbe, 12:682-692. Bouche, N., Fait, A., Bouchez, D., Moller, S. G. & Fromm, H. 2003a. Mitochondrial succinic-semialdehyde dehydrogenase of the gamma-aminobutyrate shunt is required to restrict levels of reactive oxygen intermediates in plants. Proc. Natl Acad. Sci. U S A, 100:6843-6848. Ribeiro, J. M., Genta, F. A., Sorgine, M. H., Logullo, R., Mesquita, R. D., Paiva-Silva, G. O., Majerowicz, D., Medeiros, M., Koerich, L., Terra, W. R., Ferreira, C., Pimentel, A. C., Bisch, P. M., Leite, D. C., Diniz, M. M., da, S. G. V. J. J. L., Da Silva, M. L., Araujo, R. N., Gandara, A. C., Brosson, S., Salmon, D., Bousbata, S., Gonzalez-Caballero, N., Silber, A. M., Alves-Bezerra, M., Gondim, K. C., Silva-Neto, M. A., Atella, G. C., Araujo, H., Dias, F. A., Polycarpo, C., Vionette-Amaral, R. J., Fampa, P., Melo, A. C., Tanaka, A. S., Balczun, C., Oliveira, J. H., Goncalves, R. L., Lazoski, C., Rivera-Pomar, R., Diambra, L., Schaub, G. A., Garcia, E. S., Azambuja, P., Braz, G. R. & Oliveira, P. L. 2014. An insight into the transcriptome of the digestive tract of the bloodsucking bug, Rhodnius prolixus. PLoS Negl. Trop Dis., 8:e2594. doi: 10.1371/journal.pntd.0002594. Saye, M., Miranda, M. R., di Girolamo, F., delos Milagros Camara, M. & Pereira, C. A. 2014. Proline modulates the Trypanosoma cruzi resistance to reactive oxygen species and drugs through a novel D, L-proline transporter. PLoS ONE, 9:e92028. doi: 10.1371/journal.pone.0092028. Wong, F. H., Chen, J. S., Reddy, V., Day, J. L., Shlykov, M. A., Wakabayashi, S. T. & Saier Jr, M. H. 2012. The amino acid-polyamine-organocation superfamily. J. Mol. Microbiol. Biotechnol., 22:105-113. Silber, A. M., Rojas, R. L., Urias, U., Colli, W. & Alves, M. J. 2006. Biochemical characterization of the glutamate transport in Trypanosoma cruzi. Int. J. Parasitol., 36:157-163. Martins, R. M., Covarrubias, C., Rojas, R. G., Silber, A. M. & Yoshida, N. 2009. Use of L-proline and ATP production by Trypanosoma cruzi metacyclic forms as requirements for host cell invasion. Infect. Immun., 77:3023-3032. Magdaleno, A., Suarez Mantilla, B., Rocha, S. C., Pral, E. M. & Silber, A. M. 2011. The involvement of glutamate metabolism in the resistance to thermal, nutritional, and oxidative stress in Trypanosoma cruzi. Enzyme Res., 2011:486928. Pereira, C. A., Saye, M., Wrenger, C. & Miranda, M. R. 2013. Metabolite transporters in trypanosomatid parasites: promising therapeutic targets but.. how to deal with them? Curr. Med. Chem., 21:1707-1712. Camargo, E. P. 1964. Growth and differentiation in Trypanosoma cruzi. Rev. Inst. Med. Trop. Sao Paulo, 6:93-100. Dhakal, R., Bajpai, V. K. & Baek, K. H. 2012. Production of GABA (gamma - aminobutyric acid) by microorganisms: a review. Braz. J. Microbiol., 43:1230-1241. Magdaleno, A., Ahn, I. Y., Paes, L. S. & Silber, A. M. 2009. Actions of a proline analogue, L-thiazolidine-4-carboxylic acid (T4C), on Trypanosoma cruzi. PLoS ONE, 4:e4534. doi:10.1371/journal.pone.0004534. Rassi Jr, A., Rassi, A. & Marin-Neto, J. A. 2010. Chagas disease. Lancet, 375:1388-1402. MacRae, J. I., Dixon, M. W., Dearnley, M. K., Chua, H. H., Chambers, J. M., Kenny, S., Bottova, I., Tilley, L. & McConville, M. J. 2013. Mitochondrial metabolism of sexual and asexual blood stages of the malaria parasite Plasmodium falciparum. BMC Biol., 11:67. doi:10.1186/1741-7007-11-67. Watanabe, M., Maemura, K., Kanbara, K., Tamayama, T. & Hayasaki, H. 2002. GABA and GABA receptors in the central nervous system and other organs. Int. Rev. Cytol., 213:1-47. van der Heyden, N. & Docampo, R. 2002. Proton and sodium pumps regulate the plasma membrane potential of different stages of Trypanosoma cruzi. Mol. Biochem. Parasitol., 120:127-139. Silber, A. M., Colli, W., Ulrich, H., Alves, M. J. & Pereira, C. A. 2005. Amino acid metabolic routes in Trypanosoma cruzi: possible therapeutic targets against Chagas' disease. Curr. Drug Targets Infect. Disord., 5:53-64. Jeelani, G., Sato, D., Husain, A., Escueta-de Cadiz, A., Sugimoto, M., Soga, T., Suematsu, M. & Nozaki, T. 2012. Metabolic profiling of the protozoan parasite Entamoeba invadens revealed activation of unpredicted pathway during encystation. PLoS ONE, 7:e37740. doi:10.1371/journal.pone.0037740. Teng, R., Junankar, P. R., Bubb, W. A., Rae, C., Mercier, P. & Kirk, K. 2009. Metabolite profiling of the intraerythrocytic malaria parasite Plasmodium falciparum by (1)H NMR spectroscopy. NMR Biomed., 22:292-302. Damasceno, F. S., Barison, M. J., Pral, E. M., Paes, L. S. & Silber, A. M. 2014. Memantine, an antagonist of the NMDA glutamate receptor, affects cell proliferation, differentiation and the intracellular cycle and induces apoptosis in Trypanosoma cruzi. PLoS Negl. Trop Dis., 8:e2717. doi:10.1371/journal.pntd.0002717. Tetaud, E., Bringaud, F., Chabas, S., Barrett, M. P. & Baltz, T. 1994. Characterization of glucose transport and cloning of a hexose transporter gene in Trypanosoma cruzi. Proc. Natl Acad. Sci. U S A, 91:8278-8282. Silber, A. M., Tonelli, R. R., Martinelli, M., Colli, W. & Alves, M. J. 2002. Active transport of L-proline in Trypanosoma cruzi. J. Eukaryot. Microbiol., 49:441-446. Shelp, B. J., Bown, A. W. & Faure, D. 2006. Extracellular gamma-aminobutyrate mediates communication between plants and other organisms. Plant Physiol., 142:1350-1352. Ramoino, P., Scaglione, S., Diaspro, A., Beltrame, F., Fato, M. & Usai, C. 2004. GABAA receptor subunits identified in Paramecium by immunofluorescence confocal microscopy. FEMS Microbiol. Lett., 238:449-453. Lakhani, R., Vogel, K. R., Till, A., Liu, J., Burnett, S. F., Gibson, K. M. & Subramani, S. 2014. Defects in GABA metabolism affect selective autophagy pathways and are alleviated by mTOR inhibition. EMBO Mol. Med., 6:551-566. Bouvier, L. A., Silber, A. M., Galvao Lopes, C., Canepa, G. E., Miranda, M. R., Tonelli, R. R., Colli, W., Alves, M. J. & Pereira, C. A. 2004. Post genomic analysis of permeases from the amino acid/auxin family in protozoan parasites. Biochem. Biophys. Res. Commun., 321:547-556. Schousboe, A., Larsson, O. M., Sarup, A. & White, H. S. 2004. Role of the betaine/GABA transporter (BGT-1/GAT2) for the control of epilepsy. Eur. J. Pharmacol., 500:281-287. Pereira, C. A., Alonso, G. D., Paveto, M. C., Flawia, M. M. & Torres, H. N. 1999. L-arginine uptake and L-phosphoarginine synthesis in Trypanosoma cruzi. J. Eukaryot. Microbiol., 46:566-570. Ramoino, P., Milanese, M., Candiani, S., Diaspro, A., Fato, M., Usai, C. & Bonanno, G. 2010. Gamma-amino butyric acid (GABA) release in the ciliated protozoon Paramecium occurs by neuronal-like exocytosis. J. Exp. Biol., 213:1251-1258. Caruso-Neves, C., Einicker-Lamas, M., Chagas, C., Oliveira, M. M., Vieyra, A. & Lopes, A. G. 1998. Trypanosoma cruzi epimastigotes express the ouabain- and vanadate-sensitive (Na(+)+K+)ATPase activity. Z. Naturforsch. C, 53:1049-1054. Saier Jr, M. H., Reddy, V. S., Tamang, D. G. & Vastermark, A. 2014. The transporter classification database. Nucleic Acids Res., 42:251-258. Alves, M. J. & Colli, W. 2007. Trypanosoma cruzi: adhesion to the host cell and intracellular survival. IUBMB Life, 59:274-279. Canepa, G. E., Bouvier, L. A., Urias, U., Miranda, M. R., Colli, W., Alves, M. J. & Pereira, C. A. 2005. Aspartate transport and metabolism in the protozoan parasite Trypanosoma cruzi. FEMS Microbiol. Lett., 247:65-71. Carrillo, C., Canepa, G. E., Giacometti, A., Bouvier, L. A., Miranda, M. R., de los Milagros Camara, M. & Pereira, C. A. 2010. Trypanosoma cruzi amino acid transporter TcAAAP411 mediates arginine uptake in yeasts. FEMS Microbiol. Lett., 306:97-102. 2004; 321 2009; 22 2004; 500 2010; 306 2013; 21 1964; 6 2002; 213 2006; 36 1999; 46 2003; 291 2005 2012; 12 2003a; 100 2007; 59 2014; 42 2003b; 13 2002; 49 2011; 2011 2009; 77 2004; 236 1987; 43 2002; 120 2013; 11 2010; 213 2005; 247 2013; 30 2005; 5 2010; 375 2006; 142 2009; 4 2014; 9 2014; 8 2012; 7 1994; 91 1998; 53 2014; 6 2004; 238 2012; 22 2012; 43 1985; 16 2012; 42 e_1_2_6_32_1 e_1_2_6_10_1 e_1_2_6_31_1 e_1_2_6_30_1 Camargo E. P. (e_1_2_6_6_1) 1964; 6 e_1_2_6_19_1 e_1_2_6_13_1 e_1_2_6_36_1 e_1_2_6_14_1 e_1_2_6_35_1 e_1_2_6_11_1 e_1_2_6_34_1 e_1_2_6_12_1 e_1_2_6_33_1 e_1_2_6_17_1 e_1_2_6_18_1 e_1_2_6_39_1 e_1_2_6_15_1 e_1_2_6_38_1 e_1_2_6_16_1 e_1_2_6_37_1 e_1_2_6_42_1 e_1_2_6_43_1 e_1_2_6_21_1 e_1_2_6_20_1 e_1_2_6_41_1 e_1_2_6_40_1 e_1_2_6_9_1 e_1_2_6_8_1 e_1_2_6_5_1 e_1_2_6_4_1 e_1_2_6_7_1 e_1_2_6_25_1 e_1_2_6_24_1 e_1_2_6_3_1 e_1_2_6_23_1 e_1_2_6_2_1 e_1_2_6_22_1 e_1_2_6_29_1 e_1_2_6_28_1 e_1_2_6_27_1 e_1_2_6_26_1 |
| References_xml | – volume: 43 start-page: 1230 year: 2012 end-page: 1241 article-title: Production of GABA (gamma – aminobutyric acid) by microorganisms: a review publication-title: Braz. J. Microbiol. – volume: 213 start-page: 1251 year: 2010 end-page: 1258 article-title: Gamma‐amino butyric acid (GABA) release in the ciliated protozoon Paramecium occurs by neuronal‐like exocytosis publication-title: J. Exp. Biol. – volume: 21 start-page: 1707 year: 2013 end-page: 1712 article-title: Metabolite transporters in trypanosomatid parasites: promising therapeutic targets but.. how to deal with them? publication-title: Curr. Med. Chem. – volume: 12 start-page: 682 year: 2012 end-page: 692 article-title: Mitochondrial metabolism of glucose and glutamine is required for intracellular growth of publication-title: Cell Host Microbe – year: 2005 – volume: 5 start-page: 53 year: 2005 end-page: 64 article-title: Amino acid metabolic routes in : possible therapeutic targets against Chagas' disease publication-title: Curr. Drug Targets Infect. Disord. – volume: 6 start-page: 93 year: 1964 end-page: 100 article-title: Growth and differentiation in Trypanosoma cruzi publication-title: Rev. Inst. Med. Trop. Sao Paulo – volume: 49 start-page: 441 year: 2002 end-page: 446 article-title: Active transport of L‐proline in publication-title: J. Eukaryot. Microbiol. – volume: 9 start-page: e92028 year: 2014 article-title: Proline modulates the resistance to reactive oxygen species and drugs through a novel D, L‐proline transporter publication-title: PLoS ONE – volume: 306 start-page: 97 year: 2010 end-page: 102 article-title: amino acid transporter TcAAAP411 mediates arginine uptake in yeasts publication-title: FEMS Microbiol. Lett. – volume: 11 start-page: 67 year: 2013 article-title: Mitochondrial metabolism of sexual and asexual blood stages of the malaria parasite publication-title: BMC Biol. – volume: 142 start-page: 1350 year: 2006 end-page: 1352 article-title: Extracellular gamma‐aminobutyrate mediates communication between plants and other organisms publication-title: Plant Physiol. – volume: 4 start-page: e4534 year: 2009 article-title: Actions of a proline analogue, L‐thiazolidine‐4‐carboxylic acid (T4C), on publication-title: PLoS ONE – volume: 6 start-page: 551 year: 2014 end-page: 566 article-title: Defects in GABA metabolism affect selective autophagy pathways and are alleviated by mTOR inhibition publication-title: EMBO Mol. Med. – volume: 42 start-page: 347 year: 2012 end-page: 360 article-title: Lysine transporters in human trypanosomatid pathogens publication-title: Amino Acids – volume: 36 start-page: 157 year: 2006 end-page: 163 article-title: Biochemical characterization of the glutamate transport in publication-title: Int. J. Parasitol. – volume: 213 start-page: 1 year: 2002 end-page: 47 article-title: GABA and GABA receptors in the central nervous system and other organs publication-title: Int. Rev. Cytol. – volume: 238 start-page: 449 year: 2004 end-page: 453 article-title: GABAA receptor subunits identified in Paramecium by immunofluorescence confocal microscopy publication-title: FEMS Microbiol. Lett. – volume: 91 start-page: 8278 year: 1994 end-page: 8282 article-title: Characterization of glucose transport and cloning of a hexose transporter gene in publication-title: Proc. Natl Acad. Sci. U S A – volume: 43 start-page: 1135 year: 1987 end-page: 1140 article-title: Contribution of the Na+/K+‐pump to the membrane potential publication-title: Experientia – volume: 100 start-page: 6843 year: 2003a end-page: 6848 article-title: Mitochondrial succinic‐semialdehyde dehydrogenase of the gamma‐aminobutyrate shunt is required to restrict levels of reactive oxygen intermediates in plants publication-title: Proc. Natl Acad. Sci. U S A – volume: 22 start-page: 105 year: 2012 end-page: 113 article-title: The amino acid‐polyamine‐organocation superfamily publication-title: J. Mol. Microbiol. Biotechnol. – volume: 13 start-page: 607 year: 2003b end-page: 610 article-title: GABA signaling: a conserved and ubiquitous mechanism publication-title: Trends Cell Biol. – volume: 8 start-page: e2594 year: 2014 article-title: An insight into the transcriptome of the digestive tract of the bloodsucking bug, publication-title: PLoS Negl. Trop Dis. – volume: 120 start-page: 127 year: 2002 end-page: 139 article-title: Proton and sodium pumps regulate the plasma membrane potential of different stages of publication-title: Mol. Biochem. Parasitol. – volume: 247 start-page: 65 year: 2005 end-page: 71 article-title: Aspartate transport and metabolism in the protozoan parasite publication-title: FEMS Microbiol. Lett. – volume: 8 start-page: e2717 year: 2014 article-title: Memantine, an antagonist of the NMDA glutamate receptor, affects cell proliferation, differentiation and the intracellular cycle and induces apoptosis in publication-title: PLoS Negl. Trop Dis. – volume: 375 start-page: 1388 year: 2010 end-page: 1402 article-title: Chagas disease publication-title: Lancet – volume: 53 start-page: 1049 year: 1998 end-page: 1054 article-title: epimastigotes express the ouabain‐ and vanadate‐sensitive (Na(+)+K+)ATPase activity publication-title: Z. Naturforsch. C – volume: 77 start-page: 3023 year: 2009 end-page: 3032 article-title: Use of L‐proline and ATP production by metacyclic forms as requirements for host cell invasion publication-title: Infect. Immun. – volume: 42 start-page: 251 year: 2014 end-page: 258 article-title: The transporter classification database publication-title: Nucleic Acids Res. – volume: 321 start-page: 547 year: 2004 end-page: 556 article-title: Post genomic analysis of permeases from the amino acid/auxin family in protozoan parasites publication-title: Biochem. Biophys. Res. Commun. – volume: 30 start-page: 129 year: 2013 end-page: 144 article-title: GABA shunt mediates thermotolerance in by reducing reactive oxygen production publication-title: Yeast – volume: 291 start-page: 398 year: 2003 end-page: 405 article-title: Swimming behavior regulation by GABA‐B receptors in Paramecium publication-title: Exp. Cell Res. – volume: 22 start-page: 292 year: 2009 end-page: 302 article-title: Metabolite profiling of the intraerythrocytic malaria parasite by (1)H NMR spectroscopy publication-title: NMR Biomed. – volume: 500 start-page: 281 year: 2004 end-page: 287 article-title: Role of the betaine/GABA transporter (BGT‐1/GAT2) for the control of epilepsy publication-title: Eur. J. Pharmacol. – volume: 236 start-page: 79 year: 2004 end-page: 84 article-title: Biochemical characterization of a low‐affinity arginine permease from the parasite publication-title: FEMS Microbiol. Lett. – volume: 59 start-page: 274 year: 2007 end-page: 279 article-title: : adhesion to the host cell and intracellular survival publication-title: IUBMB Life – volume: 2011 start-page: 486928 year: 2011 article-title: The involvement of glutamate metabolism in the resistance to thermal, nutritional, and oxidative stress in publication-title: Enzyme Res. – volume: 46 start-page: 566 year: 1999 end-page: 570 article-title: L‐arginine uptake and L‐phosphoarginine synthesis in publication-title: J. Eukaryot. Microbiol. – volume: 7 start-page: e37740 year: 2012 article-title: Metabolic profiling of the protozoan parasite revealed activation of unpredicted pathway during encystation publication-title: PLoS ONE – volume: 16 start-page: 315 year: 1985 end-page: 327 article-title: differentiation of under chemically defined conditions publication-title: Mol. Biochem. Parasitol. – ident: e_1_2_6_14_1 doi: 10.1590/S1517-83822012000400001 – ident: e_1_2_6_17_1 doi: 10.1371/journal.pone.0037740 – ident: e_1_2_6_13_1 doi: 10.1371/journal.pntd.0002717 – ident: e_1_2_6_10_1 doi: 10.1111/j.1574-6968.2010.01936.x – ident: e_1_2_6_22_1 doi: 10.1371/journal.pone.0004534 – ident: e_1_2_6_8_1 doi: 10.1111/j.1574-6968.2004.tb09630.x – ident: e_1_2_6_19_1 doi: 10.1002/emmm.201303356 – ident: e_1_2_6_37_1 doi: 10.1016/j.ijpara.2005.10.006 – ident: e_1_2_6_11_1 doi: 10.1515/znc-1998-11-1218 – ident: e_1_2_6_41_1 doi: 10.1007/BF01945511 – ident: e_1_2_6_18_1 doi: 10.1895/wormbook.1.14.1 – ident: e_1_2_6_29_1 doi: 10.1111/j.1574-6968.2004.tb09788.x – ident: e_1_2_6_26_1 doi: 10.2174/09298673113209990228 – ident: e_1_2_6_42_1 doi: 10.1016/S0074-7696(02)13011-7 – ident: e_1_2_6_7_1 doi: 10.1016/j.femsle.2005.04.029 – ident: e_1_2_6_9_1 doi: 10.1002/yea.2948 – ident: e_1_2_6_16_1 doi: 10.1007/s00726-010-0812-z – ident: e_1_2_6_39_1 doi: 10.1002/nbm.1323 – ident: e_1_2_6_24_1 doi: 10.1128/IAI.00138-09 – ident: e_1_2_6_27_1 doi: 10.1016/j.yexcr.2003.07.008 – ident: e_1_2_6_40_1 doi: 10.1073/pnas.91.17.8278 – ident: e_1_2_6_36_1 doi: 10.2174/1568005053174636 – ident: e_1_2_6_30_1 doi: 10.1016/S0140-6736(10)60061-X – ident: e_1_2_6_15_1 doi: 10.1016/S0166-6851(01)00444-3 – ident: e_1_2_6_38_1 doi: 10.1111/j.1550-7408.2002.tb00225.x – ident: e_1_2_6_43_1 doi: 10.1159/000338542 – ident: e_1_2_6_28_1 doi: 10.1242/jeb.039594 – ident: e_1_2_6_2_1 doi: 10.1080/15216540701200084 – ident: e_1_2_6_3_1 doi: 10.1073/pnas.1037532100 – ident: e_1_2_6_5_1 doi: 10.1016/j.bbrc.2004.07.002 – ident: e_1_2_6_20_1 doi: 10.1186/1741‐7007‐11‐67 – ident: e_1_2_6_12_1 doi: 10.1016/0166-6851(85)90073-8 – ident: e_1_2_6_31_1 doi: 10.1371/journal.pntd.0002594 – ident: e_1_2_6_34_1 doi: 10.1016/j.ejphar.2004.07.032 – ident: e_1_2_6_35_1 doi: 10.1104/pp.106.088955 – ident: e_1_2_6_4_1 doi: 10.1016/j.tcb.2003.10.001 – volume: 6 start-page: 93 year: 1964 ident: e_1_2_6_6_1 article-title: Growth and differentiation in Trypanosoma cruzi publication-title: Rev. Inst. Med. Trop. Sao Paulo contributor: fullname: Camargo E. P. – ident: e_1_2_6_21_1 doi: 10.1016/j.chom.2012.09.013 – ident: e_1_2_6_23_1 doi: 10.4061/2011/486928 – ident: e_1_2_6_25_1 doi: 10.1111/j.1550-7408.1999.tb05132.x – ident: e_1_2_6_33_1 doi: 10.1371/journal.pone.0092028 – ident: e_1_2_6_32_1 doi: 10.1093/nar/gkt1097 |
| SSID | ssj0016211 |
| Score | 2.1684616 |
| Snippet | Gamma aminobutyric acid (GABA) is widely known as a neurotransmitter and signal transduction molecule found in vertebrates, plants, and some protozoan... Gamma aminobutyric acid ( GABA ) is widely known as a neurotransmitter and signal transduction molecule found in vertebrates, plants, and some protozoan... |
| SourceID | proquest crossref pubmed wiley istex fao |
| SourceType | Aggregation Database Index Database Publisher |
| StartPage | 629 |
| SubjectTerms | Active metabolite transporters adenosine triphosphate Adenosine Triphosphate - biosynthesis adenosinetriphosphatase amino acid transporters Amino Acids - metabolism Animals biochemical pathways Biological Transport - drug effects cations Chagas disease chemotherapy culture media cytoplasm etiological agents Fluorescent Antibody Technique gamma-aminobutyric acid gamma-Aminobutyric Acid - metabolism glutamic acid Glutamic Acid - metabolism Hydrogen-Ion Concentration Na+/metabolite symporter oligomycin Oligomycins - pharmacology parasites potassium Potassium - metabolism protons signal transduction sodium Sodium - metabolism symporters temperature Trypanosoma cruzi Trypanosoma cruzi - drug effects Trypanosoma cruzi - metabolism Trypanosoma cruzi - ultrastructure vertebrates |
| Title | Uptake of GABA in Trypanosoma cruzi |
| URI | https://api.istex.fr/ark:/67375/WNG-X2CM3M0C-8/fulltext.pdf https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fjeu.12219 https://www.ncbi.nlm.nih.gov/pubmed/25851259 https://search.proquest.com/docview/1710652245 |
| Volume | 62 |
| hasFullText | 1 |
| inHoldings | 1 |
| isFullTextHit | |
| isPrint | |
| link | http://sdu.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwpV1bS8MwFD6oIPji_VJvVBH1pdKmabLi05xTERRhDsWXkKapyLAdmwX113uSbsWBguBbCE1ocnKS78tJvgAcJJJyyXjs8Qy5CaWx9iQPA49oRmIaNdDmZh_yqsNvHxvnbSOTczq-C1PpQ9QbbsYz7HxtHFwmw-9OrsuTgBAr-YkswV7fCO_qCAIj9u1dZDzMkC06UhWyp3jGJSfWoulMFohQTee-_wQ3J9GrXX4uFv7144swP0KdbrMaJkswpfNlmK3eofzA1FNhUytwhMPG7fbfZE-7ReZeNs-a7kvu3g8-cNYohsWrdNWg_HxZhe5F-7515Y3eUvAUtj72NI8irhj1dSZ9oqgiRKaa8oT7ykefzWKFxIanCVcIASKtMC9BW3HFWSqxijWYyYtcb4Cb-KGSJmDrZz6VYZywmEVZloYIDSnmOLA_7lXRryQzRE01tNGuxrY7sIH9LeQzTmWi2yFG6M5E-cIgcODQGqEuLAc9c_yMR-Lh9lI8ktZNeOO3RMOBvbGVBDqFiXTIXBflUASImxgiSxo5sF6Zr66NmEAokj4Hjq2Vfv9Hcd3u2sTm3z_dgjlsS1SdQtuGmbdBqXdgepiWu3Z8fgGKQt3K |
| link.rule.ids | 315,782,786,1408,27933,27934,46064,46488 |
| linkProvider | Wiley-Blackwell |
| linkToHtml | http://sdu.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwpV3dS-QwEB_8QPTFU8_T3vlR5fB8qbRpmmzBl3VdXT92EdxFuZeQpqmI2MquhfP--puku0VB4cC3EJKQZGaS32SSXwB-JpJyyXjs8Qx9E0pj7UkeBh7RjMQ0aqDMzTlk55r3bhvHbUOTczh5C1PxQ9QHbsYy7HptDNwcSL-2cl0eBIQYzs9ZylARzQOO8KqOITBif99Fn4cZd4uOeYXsPZ5J1Te70XQmC8SoZnr_vAc43-JXuwGdfPlc15dgcQw83WalKcswpfMVmKu-onzB1O_Cpr7CL9Qcd_D0LB-0W2TuafOo6d7nbn_4ggtHMSoepauG5d_7VRictPutjjf-TsFTOPzY0zyKuGLU15n0iaKKEJlqyhPuKx_NNosV-jY8TbhCFBBphXkJiosrzlKJTXyDmbzI9Tq4iR8qaWK2fuZTGcYJi1mUZWmI6JBijgO7k2kVTxVrhqi9DW3oq3HsDqzjhAt5h6uZGFwTw3VnAn1hEDiwZ6VQV5bDB3MDjUfipncqbkmrG3b9lmg4sDMRk0C7MMEOmeuiHIkAoRNDcEkjB9Yq-dWtERMLRb_PgX0rpo_7KM7bA5v4_v9Ft2G-0-9eisuz3sUPWMBxRdWltA2YeR6WehOmR2m5ZZX1H7IU4fI |
| linkToPdf | http://sdu.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwpV3dT9swED8NJiZe-NgGhI-RoWnbS1DiOHYjnkpp-a6QoALtxXIcGyFEUrVEGvvrOTttBNKQJu3NsmLL9t3Zv_M5vwP4lknKJeNpwA36JpSmOpA8jgKiGUlp0kKZ23vIo0vev2kddC1Nzt70X5iaH6K5cLOW4fZra-DD3Lw0cl3tRoRYys_3FGG4Jc6P44smhMCIS76LLg-z3had0Aq5ZzzTpq8OoxkjS4SodnV__w1vvoav7vzpLf7XyJdgYQI7_XatJ8vwThcfYa5ORPmEpV-lK32CH6g3_mD4KO-1Xxr_sL3f9u8K_2r0hNtGOS4fpK9G1Z-7zzDoda86R8EkmUKgcPZpoHmScMVoqI0MiaKKEJlryjMeqhCN1qQKPRueZ1whBki0wroMhcUVZ7nELlZgtigLvQZ-FsZK2ohtaEIq4zRjKUuMyWPEhhRrPNiZrqoY1pwZovE1tCWvxrl7sIbrLeQt7mVicEks050N88VR5MF3J4SmsRzd2_dnPBHX_UNxQzrn8XnYES0Pvk6lJNAqbKhDFrqsxiJC4MQQWtLEg9VafE1vxEZC0evz4KeT0ttjFCfdgSus__un2_Dh4qAnzo77pxswj9NK6hdpmzD7OKr0FsyM8-qLU9Vn9zfgmA |
| openUrl | ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=The+Uptake+of+GABA+in+Trypanosoma+cruzi&rft.jtitle=The+Journal+of+eukaryotic+microbiology&rft.au=Galvez+Rojas%2C+Robert+L.&rft.au=Ahn%2C+Il%E2%80%90Young&rft.au=Su%C3%A1rez+Mantilla%2C+Brian&rft.au=Sant%27Anna%2C+Celso&rft.date=2015-09-01&rft.issn=1066-5234&rft.eissn=1550-7408&rft.volume=62&rft.issue=5&rft.spage=629&rft.epage=636&rft_id=info:doi/10.1111%2Fjeu.12219&rft.externalDBID=10.1111%252Fjeu.12219&rft.externalDocID=JEU12219 |
| thumbnail_l | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1066-5234&client=summon |
| thumbnail_m | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1066-5234&client=summon |
| thumbnail_s | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1066-5234&client=summon |