Proline Dehydrogenase Regulates Redox State and Respiratory Metabolism in Trypanosoma cruzi

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Paes, Lisvane Silva ^a   Suárez Mantilla, Brian ^a   Zimbres, Flávia Menezes ^a   Pral, Elisabeth Mieko Furusho ^a   Diogo de Melo, Patrícia ^b   Tahara, Erich B ^a   Kowaltowski, Alicia J ^a   Elias, Maria Carolina ^b   Silber, Ariel Mariano ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b INSTITUTO BUTANTAN   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C OXIDASE; FLAVINE ADENINE NUCLEOTIDE; MESSENGER RNA; PROLINE; PROLINE DEHYDROGENASE; PYRROLINE 5 CARBOXYLATE DEHYDROGENASE;

AEROBIC METABOLISM; AMINO ACID METABOLISM; ARTICLE; BIOACCUMULATION; CELL PROTECTION; CONTROLLED STUDY; DIMERIZATION; ENERGY METABOLISM; ENZYME ACTIVITY; EPIMASTIGOTE; ESCHERICHIA COLI; GENE; GENE INTERACTION; MITOCHONDRIAL RESPIRATION; MITOCHONDRIAL VESICLE; MITOCHONDRION; NONHUMAN; NULL ALLELE; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PROTEIN EXPRESSION; PUT1 GENE; SACCHAROMYCES CEREVISIAE; SPECIES COMPARISON; TCPRODH GENE; TRYPANOSOMA CRUZI; UPREGULATION;

AMINO ACID SEQUENCE; ANIMALS; DOWN-REGULATION; ELECTRON TRANSPORT; FLAVIN-ADENINE DINUCLEOTIDE; INTRACELLULAR SPACE; LIFE CYCLE STAGES; MOLECULAR SEQUENCE DATA; OXIDATIVE STRESS; PROLINE; PROLINE OXIDASE; PROTEIN TRANSPORT; TRYPANOSOMA CRUZI;

EID: 84880663565     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0069419     Document Type: Article

References (74)

1. Hoek JB, Njogu RM, (1980) The role of glutamate transport in the regulation of the pathway of proline oxidation in rat liver mitochondria. J Biol Chem 255: 8711-8718.
2. Phang JM, (2008) Introduction to second proline symposium. Amino Acids 35: 653-654.
3. Chen C, Dickman MB, (2005) Proline suppresses apoptosis in the fungal pathogen Colletotrichum trifolii. Proc Natl Acad Sci U S A 102: 3459-3464.
4. Chen C, Wanduragala S, Becker DF, Dickman MB, (2006) Tomato QM-like protein protects Saccharomyces cerevisiae cells against oxidative stress by regulating intracellular proline levels. Appl Environ Microbiol 72: 4001-4006.
5. Nomura M, Takagi H, (2004) Role of the yeast acetyltransferase Mpr1 in oxidative stress: regulation of oxygen reactive species caused by a toxic proline catabolism intermediate. Proc Natl Acad Sci U S A 101: 12616-12621.
6. Krishnan N, Becker DF, (2006) Oxygen reactivity of PutA from Helicobacter species and proline-linked oxidative stress. J Bacteriol 188: 1227-1235.
7. Monaghan PJ, Leys D, Scrutton NS, (2007) Mechanistic aspects and redox properties of hyperthermophilic L-proline dehydrogenase from Pyrococcus furiosus related to dimethylglycine dehydrogenase/oxidase. FEBS J 274: 2070-2087.
8. Wood JM, (1988) Proline porters effect the utilization of proline as nutrient or osmoprotectant for bacteria. J Membr Biol 106: 183-202.
9. Skopelitis DS, Paranychianakis NV, Paschalidis KA, Pliakonis ED, Delis ID, et al. (2006) Abiotic stress generates ROS that signal expression of anionic glutamate dehydrogenases to form glutamate for proline synthesis in tobacco and grapevine. Plant Cell 18: 2767-2781.
10. Verbruggen N, Hua XJ, May M, Van Montagu M, (1996) Environmental and developmental signals modulate proline homeostasis: evidence for a negative transcriptional regulator. Proc Natl Acad Sci U S A 93: 8787-8791.
11. Banu MN, Hoque MA, Watanabe-Sugimoto M, Islam MM, Uraji M,et al. Proline and glycinebetaine ameliorated NaCl stress via scavenging of hydrogen peroxide and methylglyoxal but not superoxide or nitric oxide in tobacco cultured cells. Biosci Biotechnol Biochem 74: 2043-2049.
12. Hu CA, Donald SP, Yu J, Lin WW, Liu Z, et al. (2007) Overexpression of proline oxidase induces proline-dependent and mitochondria-mediated apoptosis. Mol Cell Biochem 295: 85-92.
13. Krishnan N, Dickman MB, Becker DF, (2008) Proline modulates the intracellular redox environment and protects mammalian cells against oxidative stress. Free Radic Biol Med 44: 671-681.
14. Ayliffe MA, Mitchell HJ, Deuschle K, Pryor AJ, (2005) Comparative analysis in cereals of a key proline catabolism gene. Mol Genet Genomics 274: 494-505.
15. Takagi H, Sakai K, Morida K, Nakamori S, (2000) Proline accumulation by mutation or disruption of the proline oxidase gene improves resistance to freezing and desiccation stresses in Saccharomyces cerevisiae. FEMS Microbiol Lett 184: 103-108.
16. Cazzulo JJ, (1994) Intermediate metabolism in Trypanosoma cruzi. J Bioenerg Biomembr 26: 157-165.
17. El-Sayed NM, Myler PJ, Bartholomeu DC, Nilsson D, Aggarwal G, et al. (2005) The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 309: 409-415.
18. Sylvester D, Krassner SM, (1976) Proline metabolism in Trypanosoma cruzi epimastigotes. Comp Biochem Physiol B 55: 443-447.
19. Contreras VT, Morel CM, Goldenberg S, (1985) Stage specific gene expression precedes morphological changes during Trypanosoma cruzi metacyclogenesis. Mol Biochem Parasitol 14: 83-96.
20. Homsy JJ, Granger B, Krassner SM, (1989) Some factors inducing formation of metacyclic stages of Trypanosoma cruzi. J Protozool 36: 150-153.
21. Tonelli RR, Silber AM, Almeida-de-Faria M, Hirata IY, Colli W, et al. (2004) L-proline is essential for the intracellular differentiation of Trypanosoma cruzi. Cell Microbiol 6: 733-741.
22. Martins RM, Covarrubias C, Rojas RG, Silber AM, 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.
23. Bursell JD, Kirk J, Hall ST, Gero AM, Kirk K, (1996) Volume-regulatory amino acid release from the protozoan parasite Crithidia luciliae. J Membr Biol 154: 131-141.
24. Rohloff P, Montalvetti A, Docampo R, (2004) Acidocalcisomes and the contractile vacuole complex are involved in osmoregulation in Trypanosoma cruzi. J Biol Chem 279: 52270-52281.
25. Rohloff P, Rodrigues CO, Docampo R, (2003) Regulatory volume decrease in Trypanosoma cruzi involves amino acid efflux and changes in intracellular calcium. Mol Biochem Parasitol 126: 219-230.
26. Magdaleno A, Ahn IY, Paes LS, Silber AM, (2009) Actions of a proline analogue, L-thiazolidine-4-carboxylic acid (T4C), on Trypanosoma cruzi. PLoS One 4: e4534.
27. Silber AM, Tonelli RR, Lopes CG, Cunha-e-Silva N, Torrecilhas AC, et al. (2009) Glucose uptake in the mammalian stages of Trypanosoma cruzi. Mol Biochem Parasitol 168: 102-108.
28. Brener Z, Chiari E, (1963) Morphological variations observed in different strains of Trypanosoma cruzi. Rev Inst Med Trop Sao Paulo 5: 220-224.
29. Camargo EP, (1964) Growth and differentiation in Trypanosoma cruzi. I. Origin of metacyclic trypanosomes in liquid media. Rev Inst Med Trop Sao Paulo 6: 93-100.
30. Almeida-de-Faria M, Freymuller E, Colli W, Alves MJ, (1999) Trypanosoma cruzi: characterization of an intracellular epimastigote-like form. Exp Parasitol 92: 263-274.
31. Brener Z, Golgher R, Bertelli MS, Teixeira JA, (1976) Strain-dependent thermosensitivity influencing intracellular differentiation of Trypanosoma cruzi in cell culture. J Protozool 23: 147-150.
32. Schneider A, Charriere F, Pusnik M, Horn EK, (2007) Isolation of mitochondria from procyclic Trypanosoma brucei. Methods Mol Biol 372: 67-80.
33. Bradford MM, (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
34. Ramos CR, Abreu PA, Nascimento AL, Ho PL, (2004) A high-copy T7 Escherichia coli expression vector for the production of recombinant proteins with a minimal N-terminal His-tagged fusion peptide. Braz J Med Biol Res 37: 1103-1109.
35. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
36. Laemmli UK, (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
37. Schagger H, Bentlage H, Ruitenbeek W, Pfeiffer K, Rotter S, et al. (1996) Electrophoretic separation of multiprotein complexes from blood platelets and cell lines: technique for the analysis of diseases with defects in oxidative phosphorylation. Electrophoresis 17: 709-714.
38. Strecker V, Wumaier Z, Wittig I, Schagger H, (2010) Large pore gels to separate mega protein complexes larger than 10 MDa by blue native electrophoresis: isolation of putative respiratory strings or patches. Proteomics 10: 3379-3387.
39. Lamour N, Riviere L, Coustou V, Coombs GH, Barrett MP, et al. (2005) Proline metabolism in procyclic Trypanosoma brucei is down-regulated in the presence of glucose. J Biol Chem 280: 11902-11910.
40. Johnson AB, Strecker HJ, (1962) The interconversion of glutamic acid and proline. IV. The oxidation of proline by rat liver mitochondria. J Biol Chem 237: 1876-1882.
41. Sarkar D, Bhowmik PC, Kwon YI, Shetty K, (2009) Clonal response to cold tolerance in creeping bentgrass and role of proline-associated pentose phosphate pathway. Bioresour Technol 100: 5332-5339.
42. Kyte J, Doolittle RF, (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157: 105-132.
43. Pereira CM, Sattlegger E, Jiang HY, Longo BM, Jaqueta CB, et al. (2005) IMPACT, a protein preferentially expressed in the mouse brain, binds GCN1 and inhibits GCN2 activation. J Biol Chem 280: 28316-28323.
44. Bontempi E, Martinez J, Cazzulo JJ, (1989) Subcellular localization of a cysteine proteinase from Trypanosoma cruzi. Mol Biochem Parasitol 33: 43-47.
45. Gietz RD, Schiestl RH, (2007) High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat Protoc 2: 31-34.
46. Castillo FJ, Penel C, Greppin H, (1984) Peroxidase release induced by ozone in Sedum album leaves: Involvement of Ca. Plant Physiol 74: 846-851.
47. Bates LS, (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39: 205-207.
48. Lee YH, Nadaraia S, Gu D, Becker DF, Tanner JJ, (2003) Structure of the proline dehydrogenase domain of the multifunctional PutA flavoprotein. Nat Struct Biol 10: 109-114.
49. Wanduragala S, Sanyal N, Liang X, Becker DF, (2010) Purification and characterization of Put1p from Saccharomyces cerevisiae. Arch Biochem Biophys 498: 136-142.
50. Caceres AJ, Portillo R, Acosta H, Rosales D, Quinones W, et al. (2003) Molecular and biochemical characterization of hexokinase from Trypanosoma cruzi. Mol Biochem Parasitol 126: 251-262.
51. Juan SM, Cazzulo JJ, Segura EL, (1977) The citrate synthase from Trypanosoma cruzi. J Parasitol 63: 921-922.
52. Phang JM, Liu W, Zabirnyk O, (2010) Proline metabolism and microenvironmental stress. Annu Rev Nutr 30: 441-463.
53. Delwing D, Bavaresco CS, Wannmacher CM, Wajner M, Dutra-Filho CS, et al. (2003) Proline induces oxidative stress in cerebral cortex of rats. Int J Dev Neurosci 21: 105-110.
54. White TA, Krishnan N, Becker DF, Tanner JJ, (2007) Structure and kinetics of monofunctional proline dehydrogenase from Thermus thermophilus. J Biol Chem 282: 14316-14327.
55. Tanner JJ, (2008) Structural biology of proline catabolism. Amino Acids 35: 719-730.
56. Simondsen RP, Weber PC, Salemme FR, Tollin G, (1982) Transient kinetics of electron transfer reactions of flavodoxin: ionic strength dependence of semiquinone oxidation by cytochrome c, ferricyanide, and ferric ethylenediaminetetraacetic acid and computer modeling of reaction complexes. Biochemistry 21: 6366-6375.
57. Paes LS, Mantilla BS, Barison MJ, Wrenger C, Silber AM, (2011) The uniqueness of the Trypanosoma cruzi mitochondrion: opportunities to identify new drug target for the treatment of Chagas disease. Curr Pharm Des 17: 2074-2099.
58. Silber AM, Colli W, Ulrich H, Alves MJ, Pereira CA, (2005) Amino acid metabolic routes in Trypanosoma cruzi: possible therapeutic targets against Chagas' disease. Curr Drug Targets Infect Disord 5: 53-64.
59. Ostrander EL, Larson JD, Schuermann JP, Tanner JJ, (2009) A conserved active site tyrosine residue of proline dehydrogenase helps enforce the preference for proline over hydroxyproline as the substrate. Biochemistry 48: 951-959.
60. Emanuelsson O, von Heijne G, Schneider G, (2001) Analysis and prediction of mitochondrial targeting peptides. Methods Cell Biol 65: 175-187.
61. Adams E, Frank L, (1980) Metabolism of proline and the hydroxyprolines. Annu Rev Biochem 49: 1005-1061.
62. Silber AM, Tonelli RR, Martinelli M, Colli W, Alves MJ, (2002) Active transport of L-proline in Trypanosoma cruzi. J Eukaryot Microbiol 49: 441-446.
63. Phang JM, Donald SP, Pandhare J, Liu Y, (2008) The metabolism of proline, a stress substrate, modulates carcinogenic pathways. Amino Acids 35: 681-690.
64. Bringaud F, Barrett MP, Zilberstein D, (2012) Multiple roles of proline transport and metabolism in trypanosomatids. Front Biosci 17: 349-374.
65. Morita Y, Nakamori S, Takagi H, (2003) L-proline accumulation and freeze tolerance of Saccharomyces cerevisiae are caused by a mutation in the PRO1 gene encoding gamma-glutamyl kinase. Appl Environ Microbiol 69: 212-219.
66. Alia, Mohanty P, Matysik J, (2001) Effect of proline on the production of singlet oxygen. Amino Acids 21: 195-200.
67. Kaul S, Sharma SS, Mehta IK, (2008) Free radical scavenging potential of L-proline: evidence from in vitro assays. Amino Acids 34: 315-320.
68. Maxwell SA, Rivera A, (2003) Proline oxidase induces apoptosis in tumor cells, and its expression is frequently absent or reduced in renal carcinomas. J Biol Chem 278: 9784-9789.
69. Coustou V, Biran M, Breton M, Guegan F, Riviere L, et al. (2008) Glucose-induced remodeling of intermediary and energy metabolism in procyclic Trypanosoma brucei. J Biol Chem 283: 16342-16354.
70. Turrens JF, (1989) The role of succinate in the respiratory chain of Trypanosoma brucei procyclic trypomastigotes. Biochem J 259: 363-368.
71. Rasmusson AG, Geisler DA, Moller IM, (2008) The multiplicity of dehydrogenases in the electron transport chain of plant mitochondria. Mitochondrion 8: 47-60.
72. Thomson JF, Klipfel FJ, (1960) Studies on the enzymic dehydrogenation of deuterated succinate. Biochim Biophys Acta 44: 72-77.
73. Chamond N, Cosson A, Coatnoan N, Minoprio P, (2009) Proline racemases are conserved mitogens: characterization of a Trypanosoma vivax proline racemase. Mol Biochem Parasitol 165: 170-179.
74. Reina-San-Martin B, Degrave W, Rougeot C, Cosson A, Chamond N, et al. (2000) A B-cell mitogen from a pathogenic trypanosome is a eukaryotic proline racemase. Nat Med 6: 890-897.