Molecular cloning of a novel multidomain Kunitz-type proteinase inhibitor from the hookworm Ancylostoma caninum

Journal of Parasitology

Volumn 89, Issue 2, 2003, Pages 402-407

  Hawdon, John M ^a   Datu, Bennett ^a   Crowell, Melissa ^a  

^a GEORGE WASHINGTON UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APROTININ; COMPLEMENTARY DNA; CYSTEINE; LACUNIN; PAPILIN; PROTEINASE INHIBITOR; SCLEROPROTEIN; THROMBOSPONDIN; UNCLASSIFIED DRUG;

ENZYME; PARASITOLOGY;

AMINO ACID SEQUENCE; AMPLICON; ANCYLOSTOMA CANINUM; ARTICLE; CONTROLLED STUDY; DNA LIBRARY; MOLECULAR CLONING; MOLECULAR WEIGHT; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; POLYMERASE CHAIN REACTION; PROTEIN DOMAIN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

AMINO ACID SEQUENCE; ANCYLOSTOMA; ANIMALS; BLOTTING, SOUTHERN; CLONING, MOLECULAR; DNA, COMPLEMENTARY; DNA, HELMINTH; MOLECULAR SEQUENCE DATA; PEPTIDES; PLANT PROTEINS; POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT; TRYPSIN INHIBITORS;

ANCYLOSTOMA CANINUM; ANCYLOSTOMATOIDEA; INSECTA; NEMATODA; PROTOZOA;

EID: 0037398198     PISSN: 00223395     EISSN: None     Source Type: Journal    
DOI: 10.1645/0022-3395(2003)089[0402:MCOANM]2.0.CO;2     Document Type: Article

References (37)

1. ARNHEIM, N., AND H. ERLICH. 1992. Polymerase chain reaction strategy. Annual Review of Biochemistry 61: 131-156.
2. BEKTESH, S., K. VAN DOREN, AND D. HIRSH. 1988. Presence of the Caenorhabditis elegans spliced leader on different mRNAs and in different genera of nematodes. Genes and Development 2: 1277-1283.
3. BERNARD, V. D., AND R. J. PEANASKY. 1993. The serine protease inhibitor family from Ascaris suum: Chemical determination of the five disulfide bridges. Archives of Biochemistry and Biophysics 303: 367-376.
4. BLUMENTHAL, T., AND K. STEWARD. 1997. RNA processing and gene structure. In C. elegans II, D. L. Riddle, T. Blumenthal, B. J. Meyer, and J. R. Priess (eds.). Cold Spring Harbor Laboratory Press, Plainview, New York, p. 117-145.
5. BRIGGS, M. S., AND L. M. GIERASCH. 1986. Molecular mechanisms of protein secretion: The role of the signal sequence. Advances in Protein Chemistry 38: 109-180.
6. CAPPELLO, M., J. M. HAWDON, B. F. JONES, W. P. KENNEDY, AND P. J. HOTEZ. 1996. Ancylostoma caninum anticoagulant peptide: Cloning by PCR and expression of soluble, active protein in E. coli. Molecular and Biochemical Parasitology 80: 113-117.
7. DUFTON, M. J. 1985. Proteinase inhibitors and dendrotoxins. Sequence classification, structural prediction and structure/activity. European Journal of Biochemistry 153: 647-654.
8. EFF, J. A. 1966. Nature of an anticoagulant from the cephalic glands of Ancylostoma caninum. Journal of Parasitology 52: 833-843.
9. FALQUET, L., M. PAGNI, P. BUCHER, N. HULO, C. J. SIGRIST, K. HOFMANN, AND A. BAIROCH. 2002. The PROSITE database: Its status in 2002. Nucleic Acids Research 30: 235-238.
10. FIORETTI, E., G. IACOPINO, M. ANGELETTI, D. BARRA, F. BOSSA, AND F. ASCOLI. 1985. Primary structure and antiproteolytic activity of a Kunitz-type inhibitor from bovine spleen. Journal of Biological Chemistry 260: 11451-11455.
11. HAMMERBERG, B., AND J. F. WILLIAMS. 1978. Interaction between Taenia taeniaeformis and the complement system. Journal of Immunology 120: 1033-1038.
12. HATTORI, M., AND Y. SAKAKI. 1986. Dideoxy sequencing method using denatured plasmid templates. Analytical Biochemistry 152: 232-238.
13. HAWDON, J. M., B. F. JONES, D. R. HOFFMAN, AND P. J. HOTEZ. 1996. Cloning and characterization of Ancylostoma secreted protein: A novel protein associated with the transition to parasitism by infective hookworm larvae. Journal of Biological Chemistry 271: 6672-6678.
14. HAWDON, J. M., B. F. JONES, AND P. J. HOTEZ. 1995. Cloning and characterization of a cDNA encoding the catalytic subunit of a cAMP-dependent protein kinase from Ancylostoma caninum third-stage infective larvae. Molecular and Biochemical Parasitology 69: 127-130.
15. HAWDON, J. M., S. NARASIMHAN, AND P. J. HOTEZ. 1999. Ancylostoma secreted protein 2: Cloning and characterization of a second member of a family of nematode secreted proteins from Ancylostoma caninum. Molecular and Biochemical Parasitology 99: 149-165.
16. HAWLEY, J. H., AND R. J. PEANASKY. 1992. Ascaris suum: Are trypsin inhibitors involved in the species specificity of Ascarid nematodes? Experimental Parasitology 75: 112-118.
17. LASKOWSKI, M., JR, AND I. KATO. 1980. Protein inhibitors of proteinases. Annual Review of Biochemistry 49: 593-626.
18. LEID, R. W., C. M. SUQUET, H. G. BOUWER, AND D. J. HINRICHS. 1986. Interleukin inhibition by a parasite proteinase inhibitor, taeniaestatin. Journal of Immunology 137: 2700-2702.
19. LILI, Z., Z. BINGXIANG, T. HONG, X. SHUHUA, P. HOTEZ, Z. BING, L. YANGZHONG, L. YING, X. HAICHOU, J. HAWDON, Y. HUI, W. HUIZHEN, AND F. ZHEN. 2000. Epidemiology of human geohelminth infections (ascariasis, trichuriasis and necatoriasis) in Lushui and Puer Counties, Yunnan Province, China. Southeast Asian Journal of Tropical Medicine and Public Health 31: 448-453.
20. LIU, C. H., X. R. ZHANG, D. C. QIU, S. H. XIAO, P. J. HOTEZ, D. F. ZHEN, H. L. ZHEN, M. D. LI, H. N. REN, B. ZHAN, H. C. XUE, J. HAWDON, AND Z. FENG. 1999. Epidemiology of human hookworm infections among adult villagers in Hejiang and Santai Counties, Sichuan Province, China. Acta Tropica 73: 243-249.
21. LU, C. C., T. NGUYEN, S. MORRIS, D. HILL, AND J. A. SAKANARI. 1998. Anisakis simplex: Mutational bursts in the reactive site centers of serine protease inhibitors from an ascarid nematode. Experimental Parasitology 89: 257-261.
22. MARTZEN, M. R., B. A. MCMULLEN, N. E. SMITH, K. FUJIKAWA, AND R. J. PEANASKY. 1990. Primary structure of the major pepsin inhibitor from the intestinal parasitic nematode Ascaris suum. Biochemistry 29: 7366-7372.
23. MILSTONE, A. M., L. M. HARRISON, R. D. BUNGIRO, P. KUZMIC, AND M. CAPPELLO. 2000. A broad spectrum Kunitz type serine protease inhibitor secreted by the hookworm Ancylostoma ceylanicum. Journal of Biological Chemistry 275: 29391-29399.
24. NARDI, J. B., C. GAO, AND M. R. KANOST. 2001. The extracellular matrix protein lacunin is expressed by a subset of hemocytes involved in basal lamina morphogenesis. Journal of Insect Physiology 47: 997-1006.
25. NARDI, J. B., R. MARTOS, K. K. WALDEN, D. J. LAMPE, AND H. M. ROBERTSON. 1999. Expression of lacunin, a large multidomain extracellular matrix protein, accompanies morphogenesis of epithelial monolayers in Manduca sexta. Insect Biochemistry and Molecular Biology 29: 883-897.
26. NIELSEN, H., J. ENGELBRECHT, S. BRUNAK, AND G. VON HEIJNE. 1997. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Engineering 10: 1-6.
27. POTTER, K. A., AND R. W. LEID. 1986. Isolation and partial characterization of an eosinophil chemotactic factor from metacestodes of Taenia taeniaeformis (ECF-Tt). Journal of Immunology 136: 1712-1717.
28. RHOADS, M. L., R. H. FETTERER, AND D. E. HILL. 2000. Trichuris suis: A secretory serine protease inhibitor. Experimental Parasitology 94: 1-7.
29. RIFFKIN, M., H.-E SEOW, D. JACKSON, L. BROWN, AND P. WOOD. 1996. Defence against the immune barrage: Helminth survival strategies. Immunology and Cell Biology 74: 564-574.
30. SANGER, E, S. NICKLEN, AND A. R. COULSON. 1977. DNA sequencing with chain-terminating inhibitors. Proceedings of the National Academy of Science of the United States of America 74: 5463-5467.
31. SCHULTZ, J., F. MILPETZ, P. BORK, AND C. P. PONTING. 1998. SMART, a simple modular architecture research tool: Identification of signaling domains. Proceedings of the National Academy of Sciences of the United States of America 95: 5857-5864.
32. SHORT, J. M., AND J. A. SORGE. 1992. In vivo excision properties of bacteriophage lambda ZAP expression vectors. Methods in Enzymology 216: 495-508.
33. SPRECHER, C. A., W. KISIEL, S. MATHEWES, AND D. C. FOSTER. 1994. Molecular cloning, expression, and partial characterization of a second human tissue-factor-pathway inhibitor. Proceedings of the National Academy of Sciences of the United States of America 91: 3353-3357.
34. STANSSENS, P., P. W. BERGUM, Y. GANSEMANS, L. JESPERS, Y. LAROCHE, S. HUANG, S. MAKI, J. MESSENS, M. LAUWEREYS, M. CAPPELLO, P. J. HOTEZ, I. LASTERS, AND G. P. VLASUK. 1996. Anticoagulant repertoire of the hookworm Ancylostoma caninum. Proceedings of the National Academy of Sciences of the United States of America 93: 2149-2154.
35. SUN, F., Z. WU, Y. QIAN, H. CAO, H. XUE, H. REN, S. XIAO, B. ZHAN, J. M. HAWDON, Z. FENG, AND P. J. HOTEZ. 1998. Epidemiology of human intestinal nematode infections in Wujiang and Pizhou Counties, Jiangsu Province, China. Southeast Asian Journal of Tropical Medicine and Public Health 29: 605-610.
36. WUN, T. C., K. K. KRETZMER, T. J. GIRARD, J. P. MILETICH, AND G. J. BROZE JR. 1988. Cloning and characterization of a cDNA coding for the lipoprotein-associated coagulation inhibitor shows that it consists of three tandem Kunitz-type inhibitory domains. Journal of Biological Chemistry 263: 6001-6004.
37. YONG, W., S. GUANGJIN, W. WEITU, X. SHUHUA, P. J. HOTEZ, L. QIYANG, X. HAICHOU, Y. XIAOMEI, L. XIAOMING, Z. BIN, J. M. HAWDON, C. LI, J. HONG, H. CHUNMEI, AND F. ZHENG. 1999. Epidemiology of human ancylostomiasis among rural villagers in Nanlin County (Zhongzhou village), Anhui Province, China: Age-associated prevalence, intensity and hookworm species identification. Southeast Asian Journal of Tropical Medicine and Public Health 30: 692-697.