Localization and functional analysis of the cytosolic and extracellular CuZn superoxide dismutases in the human parasitic nematode Onchocerca volvulus

Molecular and Biochemical Parasitology

Volumn 88, Issue 1-2, 1997, Pages 187-202

  Henkle Duhrsen K ^a   Tuan, R S ^b   Wildenburg, G ^a   Eschbach, M L ^a   Tawe, W ^a   Zipfel, P ^a   Walter, R D ^a  

^a BERNHARD NOCHT INSTITUTE FOR TROPICAL MEDICINE   (Germany)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

Environmental oxidative stress; Onchocerca volvulus; Secretory enzyme; Superoxide dismutase

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BACULOVIRUS; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME LOCALIZATION; ENZYME RELEASE; HYDROPHOBICITY; NEMATODE; ONCHOCERCA VOLVULUS; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN QUATERNARY STRUCTURE; SUBCUTANEOUS TISSUE;

ANIMALS; CYTOSOL; ESCHERICHIA COLI; EXTRACELLULAR SPACE; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; IMMUNOHISTOCHEMISTRY; ISOENZYMES; MALE; ONCHOCERCA VOLVULUS; RECOMBINANT PROTEINS; RNA, HELMINTH; RNA, MESSENGER; SUPEROXIDE DISMUTASE;

HYPODERRIS; NEMATODA; ONCHOCERCA VOLVULUS; UNIDENTIFIED BACULOVIRUS;

EID: 0343145717     PISSN: 01666851     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0166-6851(97)00092-3     Document Type: Article

References (64)

1. WHO Expert Committee on Onchocerciasis Control. Onchocerciasis and its control. WHO Tech Rep Ser, 1995:852.
2. Drobniewski FA. Onchocerciasis and the onchocerciasis control programme. Microbiol Eur 1993;Sept/Oct:24-9.
3. Callahan HL, Crouch RK, James ER. Helminth anti-oxidant enzymes: a protective mechanism against host oxidants?. Parasitol Today 1988;4:218-25.
4. Cross AR, Jones OTG. Enzymic mechanisms of superoxide production. Biochim Biophys Acta 1991;1057:281-98.
5. Sies H. Strategies of anti-oxidant defense. Eur J Biochem 1993;215:213-9.
6. Babior B. Oxidants from phagocytes: Agents of defense and destruction. Blood 1984;64:959-66.
7. Jesaitis AJ, Quinn MT, Mukherjee G, Ward PA, Dratz EA. Death by oxygen: the molecular basis of oxidative damage by leukocytes. New Biol 1992;3:651-5.
8. Maizels RM, Bundy DAP, Selkirk ME, Smith DF, Anderson RM. Immunological modulation and evasion by helminth parasites in human populations. Nature 1993;365:797-805.
9. Greene BM, Taylor HR, Aikawa M. Cellular killing of microfilariae of Onchocerca volvulus: eosinophil and neutrophil-mediated immune serum-dependent destruction. J Immunol 1981;127:1611-8.
10. Brattig NW, Tischendorf FW, Strote G, Medina-De la Garza CE. Eosinophil-larval-interaction in onchocerciasis: heterogeneity of in vitro adherence of eosinophils to infective third and fourth stage larvae and microfilariae of Onchocerca volvulus. Parasite Immunol 1991;13:13-22.
11. Cesbron J-Y, Capron A, Vargaftig BB, Lagarde M, Pincemail J, Braquet P, Taelman H, Joseph M. Platelets mediate the action of diethylcarbamazine on microfilariae. Nature 1987;325:533-6.
12. Wei N, Sadrzadeh SM. Enhancement of hemin-induced membrane damage by artemisinin. Biochem Pharmacol 1994;48:737-41.
13. Docampo R, Moreno SNJ. Free-radical intermediates in the antiparasitic action of drugs and phagocytic cells. In: Pryor WA, editor. Free Radicals in Biology. New York: Academic Press, 1984:239-288.
14. Rzepczyk C, Bishop CJ. Immunological and ultrastructural aspects of the cell-mediated killing of Dirofilaria immitis microfilariae. Parasite Immunol 1984;6:443-57.
15. Kazura JW, Meshnik SR. Scavenger enzymes and resistance to oxygen mediated damage in Trichinella spiralis. Mol Biochem Parasitol 1984;10:1-10.
16. Callahan HL, Crouch RK, James ER. Hydrogen peroxide is the most toxic oxygen species for Onchocerca cervicalis microfilariae. Parasitology 1990;100:407-15.
17. Ou X, Tang L, McCrossan M, Henkle-Dührsen K, Selkirk ME. Brugia malayi: Localization and differential expression of extracellular and cytoplasmic CuZn superoxide dismutases in adults and microfilariae. Exp Parasitol 1995;80:515-29.
18. Bannister JV, Bannister WH, Rotilio G. Aspects of the structure, function and applications of superoxide dismutase. Crit Rev Biochem 1987;22:111-80.
19. Fridovich I. Superoxide radical and superoxide dismutases. Annu Rev Biochem 1995;64:97-112.
20. Crappo JD, Oury T, Rabouille C, Slot JW, Chang L-Y. Copper, zinc superoxide dismutase is primarily a cytosolic protein in human cells. Proc Natl Acad Sci USA 1992;89:10405-9.
21. Marklund SL. Extracellular superoxide dismutase in human tissues and human cell lines. J Clin Invest 1984;74:1398-403.
22. Weisiger RA, Fridovich I. Mitochondrial superoxide dismutase. Site of synthesis and intramitochondrial localization. J Biol Chem 1973;248:4793-6.
23. Henkle KJ, Liebau E, Müller S, Bergmann B, Walter RD. Characterization and molecular cloning of the CuZn superoxide dismutase from the human parasite Onchocerca volvulus. Infect Immun 1991;59:2063-9.
24. James ER, McLean D, Perler F. Molecular cloning of an Onchocerca volvulus extracellular CuZn superoxide dismutase. Infect Immun 1994;62:713-6.
25. Henkle KJ, Liebau E, Walter RD. Characterization of the Onchocerca volvulus superoxide dismutase gene and mRNA processing. Mol Biochem Parasitol 1993;58:173-6.
26. Henkle-Dührsen K, Tawe W, Warnecke C, Walter RD. Characterization of a Mn superoxide dismutase cDNA and gene from the human parasite Onchocerca volvulus. Biochem J 1995;308:441-6.
27. Henkle-Dührsen K, Warnecke C, Brattig N, Liebau E, Walter RD. Characterization of enzymatically active Onchocerca volvulus Cu/Zn superoxide dismutase expressed in Escherichia coli. Mol Biochem Parasitol 1994;67:41-7.
28. Clos J, Brandau S. Two high-copy-number vectors for T7 RNA polymerase-dependent expression of recombinant genes in Escherichia coli. Prot Express Purif 1994;5:133-7.
29. Schulz-Key H, Albiez EJ, Büttner DW. Isolation of living adult Onchocerca volvulus from nodules. Trop Med Parasitol 1977;28:428-30.
30. Liebau E, Wildenburg G, Walter RD, Henkle-Dührsen K. A novel type of glutathione S-transferase in Onchocerca volvulus. Infect Immun 1994;62:4762-7.
31. Sambrook J, Fritsch EF, Maniatis T. Molecular Cloning. A Laboratory Manual. 2nd edition. New York: Cold Spring Harbor Laboratory Press, 1989.
32. Albiez EJ, Büttner DW, Duke BOL. Diagnosis and extirpation of nodules in human onchocerciasis. Trop Med Parasitol 1988;39:331-46.
33. Cordell JL, Falini B, Erber WN, Ghosh AK, Abdulaziz Z, Macdonald S, Pulford KAF, Stein H, Mason DY. Immunoenzymatic labeling of monoclonal antibodies using immune complexes of alkaline phosphatase and monoclonal anti-alkaline phosphatase (APAAP complexes). J Histochem Cytochem 1984;32:219-29.
34. Humason G. Animal Tissue Techniques. 3rd edition. San Francisco: Freeman, 1972.
35. Kiernan JA. Histological and Histochemical Methods, Theory and Practice. Oxford: Pergamon Press, 1981.
36. McDonald SA, Tuan RS. Expression of collagen type transcripts in chick embryonic bone detected by in situ cDNA-mRNA hybridization. Dev Biol 1989;133:221-34.
37. Tuan RS, Lamb BT, Jesinkey CB. Mouse placental 57-kDa calcium-binding protein. II. Localization of gene expression by in situ mRNA-cDNA hybridization. Differentiation 1988;37:198-204.
38. Lo CW. Localization of low abundance DNA sequences in tissue sections by in situ hybridization. J Cell Sci 1986;81:143-62.
39. Langer P, Waldrop A, Ward D. Enzymatic synthesis of biotin-labeled polynucleotides: novel nucleic acid affinity probes. Proc Natl Acad Sci USA 1981;78:6633-7.
40. Kühn S, Zipfel PF. The baculovirus expression vector pBSV-8H is directs secretion of histidine-tagged proteins. Gene 1995;162:225-9.
41. Summers MD, Smith GE. A Manual of Methods for Baculovirus Vectors and Insect Cell Culture Procedures, Texas Agricultural Experiment Station Bulletin, 1987:1555.
42. McCord JM, Fridovich I. Superoxide dismutase: an enzymic function of erythrocuprein (hemocuprein). J Biol Chem 1969;244:6049-55.
43. Flohe L, Ötting F. Superoxide dismutase assays. Methods Enzymol 1984;105:93-104.
44. Bradford MM. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976;72:248-54.
45. Strote G, Bonow I, Attah S. The ultrastructure of the anterior end of male Onchocerca volvulus: papillae, amphids, nerve ring and first indication of an excretory system in the adult filarial worm. Parasitology 1996;113:71-85.
46. Franz M. The morphology of adult Onchocerca volvulus based on electron microscopy. Trop Med Parasitol 1988;39:359-66.
47. Radi R, Beckman JS, Bush KM, Freeman BA. Peroxynitrite oxidation of sulfhydryls. The cytotoxic potential of superoxide and nitric oxide. J Biol Chem 1991;266:4244-50.
48. Radi R, Beckman JS, Bush KM, Freeman BA. Peroxynitrite-induced membrane lipid peroxidation: the cytotoxic potential of superoxide and nitric oxide. Arch Biochem Biophys 1991;288:481-7.
49. Zhu L, Gunn C, Beckman JS. Bactericidal activity of peroxynitrite. Arch Biochem Biophys 1992;298:452-7.
50. Denicola A, Rubbo H, Rodriguez D, Radi R. Peroxynitrite-mediated cytotoxicity to Trypanosoma cruzi. Arch Biochem Biophys 1993;304:279-86.
51. Tibell L, Hjalmarsson K, Edlund T, Skogman G, Engström A, Marklund SL. Expression of human extracellular superoxide dismutase in Chinese hamster ovary cells and characterization of the product. Proc Natl Acad Sci USA 1987;84:6634-8.
52. Hong Z, LoVerde PT, Thakur A, Hammarskjöld ML, Rekosh D. Schistosoma mansoni: A Cu/Zn superoxide dismutase is glycosylated when expressed in mammalian cells and localises to a subtegumental region in adult schistosomes. Exp Parasitol 1993;76:101-14.
53. Tang L, Ou X, Henkle-Dührsen KJ, Selkirk M. Extracellular and cytoplasmic CuZn superoxide dismutases from Brugia lymphatic filarial nematode parasites. Infect Immun 1994;62:961-7.
54. Simurda M, van Keulen CH, Rekosh DM, LoVerde PT. Schistosoma mansoni: Identification and analysis of an mRNA and a gene encoding superoxide dismutase (Cu-Zn). Exp Parasitol 1988;67:73-84.
55. Hjalmarsson K, Marklund SL, Engström A, Edlund T. Isolation and sequence of a complementary DNA encoding human extracellular superoxide dismutase. Proc Natl Acad Sci USA 1987;84:6340-4.
56. Perry ACF, Jones R, Hall L. Isolation and characterization of a rat cDNA clone encoding a secreted superoxide dismutase reveals the epididymis to be a major site of its expression. Biochem J 1993;293:21-5.
57. Karlsson K, Sandstrom J, Edlund A, Marklund SL. Turnover of extracellular superoxide dismutase in tissues. Labor Invest 1994;70:705-10.
58. Gao B, Flores SC, McCord JM. A site-directed mutant of CuZn-superoxide dismutase modeled after native extracellular superoxide dismutase. Biol Trace Elem Res 1995;47:95-100.
59. Von Heijne G. Signal sequences, the limits of variation. J Mol Biol 1985;184:99-105.
60. Von Heijne G. A new method for predicting signal sequence cleavage sites. Nucleic Acids Res 1986;14:4683-90.
61. Steinman HM, Ely B. Copper-zinc superoxide dismutase of Caulobacter crescentus: cloning, sequencing, and mapping of the gene and periplasmic location of the enzyme. J Bacteriol 1990;172:2901-10.
62. Benov LT, Fridovich I. Escherichia coli expresses a copper- and zinc-containing superoxide dismutase. J Biol Chem 1994;269:25310-4.
63. Filice GA, Beaman BL, Krick JA, Remington JS. Effects of human neutrophils and monocytes on Nocardia asteroides: failure of killing despite occurrence of the oxidative metabolic burst. J Infect Dis 1980;142:432-8.
64. Beaman BL, Black CM, Doughty F, Beaman L. Role of superoxide dismutase and catalase as determinants of pathogenicity of Nocardia asteroides: Importance in resistance to microbicidal activities of human polymorphonuclear neutrophils. Infect Immun 1985;47:135-41.