Comprehensive proteomic profiling of adult Angiostrongylus costaricensis, a human parasitic nematode

Journal of Proteomics

Volumn 74, Issue 9, 2011, Pages 1545-1559

  Rebello, Karina M ^a,b   Barros, Juliana S L ^a   Mota, Ester M ^a   Carvalho, Paulo C ^a,b   Perales, Jonas ^a,b   Lenzi, Henrique L ^a   Neves Ferreira, Ana G C ^a,b  

^a INSTITUTO OSWALDO CRUZ   (Brazil)

^b Rio de Janeiro Proteomics Network   (Brazil)

Author keywords

Angiostrongylus costaricensis; Immunogenic proteins; Nematode; Proteome

Indexed keywords

CELL EXTRACT; GALECTIN; HEAT SHOCK PROTEIN;

ANGIOSTRONGYLUS; ARTICLE; CHEMICAL ANALYSIS; FEMALE; HOST PARASITE INTERACTION; IMMUNOGENICITY; IMMUNOREACTIVITY; MALE; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PROCESSING; PROTEOMICS;

ANGIOSTRONGYLUS; ANIMALS; ANTIGENS, HELMINTH; FEMALE; HELMINTH PROTEINS; HOST-PARASITE INTERACTIONS; HUMANS; IMMUNOGENETIC PHENOMENA; MALE; NEMATODA; PROTEOMICS;

ANGIOSTRONGYLUS COSTARICENSIS; VERMES;

EID: 80051666560     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2011.04.031     Document Type: Article

References (128)

1. Morera P., Céspedes R. Angiostrongylus costaricensis n. sp. (Nematoda: Metastrongyloidea), a new lungworm occurring in man in Costa Rica. Rev Biol Trop 1971, 18:173-185.
2. Eamsobhana P., Lim P.E., Solano G., Zhang H., Gan X., Yong H.S. Molecular differentiation of Angiostrongylus taxa (Nematoda: Angiostrongylidae) by cytochrome c oxidase subunit I (COI) gene sequences. Acta Trop 2010, 116:152-156.
3. Wang Q.P., Lai D.H., Zhu X.Q., Chen X.G., Lun Z.R. Human angiostrongyliasis. Lancet Infect Dis 2008, 8:621-630.
4. Kliks M.M., Palumbo N.E. Eosinophilic meningitis beyond the Pacific Basin: the global dispersal of a peridomestic zoonosis caused by Angiostrongylus cantonensis, the nematode lungworm of rats. Soc Sci Med 1992, 34:199-212.
5. Pien F.D., Pien B.C. Angiostrongylus cantonensis eosinophilic meningitis. Int J Infect Dis 1999, 3:161-163.
6. Caldeira R.L., Mendonça C.L., Goveia C.O., Lenzi H.L., Graeff-Teixeira C., Lima W.S., et al. First record of molluscs naturally infected with Angiostrongylus cantonensis (Chen, 1935) (Nematoda: Metastrongylidae) in Brazil. Mem Inst Oswaldo Cruz 2007, 102:887-889.
7. Maldonado A., Simões R.O., Oliveira A.P., Motta E.M., Fernandez M.A., Pereira Z.M., et al. First report of Angiostrongylus cantonensis (Nematoda: Metastrongylidae) in Achatina fulica (Mollusca: Gastropoda) from Southeast and South Brazil. Mem Inst Oswaldo Cruz 2010, 105:938-941.
8. Morera P. Life history and redescription of Angiostrongylus costaricensis Morera and Céspedes, 1971. Am J Trop Med Hyg 1973, 22:613-621.
9. Céspedes R., S.J., Mekbel S., Troper L., Müllner F., Morera P. Granulomas entéricos y linfáticos con intensa eosinofilia tissular producidos por un estrongilideo (Strongylata). Acta Med Costarric 1967, 10:325-355.
10. Morera P., Bontempo I. Acción de algunos antihelminticos sobre Angiostrongylus costaricensis. Rev Méd Hosp Nac Niños Costa Rica 1985, 20:165-174.
11. Ubelaker J.E., Hall N.M. First report of Angiostrongylus costaricensis Morera and Céspedes 1971 in the United States. J Parasitol 1979, 65:307.
12. Hulbert T.V., Larsen R.A., Chandrasoma P.T. Abdominal angiostrongyliasis mimicking acute appendicitis and Meckel's diverticulum: report of a case in the United States and review. Clin Infect Dis 1992, 14:836-840.
13. Ash L.R. Human anisakiasis misdiagnosed as abdominal angiostrongyliasis. Clin Infect Dis 1993, 16:332-334.
14. Kramer M.H., Greer G.J., Quiñonez J.F., Padilla N.R., Hernández B., Arana B.A., et al. First reported outbreak of abdominal angiostrongyliasis. Clin Infect Dis 1998, 26:365-372.
15. Morera P., Ash L.R. Studies on the intermediate host of Angiostrongylus costaricensis (Morera and Céspedes, 1971). Bol Chil Parasitol 1970, 25:135.
16. Rodriguez R., Agostini A.A., Porto S.M., Olivaes A.J., Branco S.L., Genro J.P., et al. Dogs may be a reservoir host for Angiostrongylus costaricensis. Rev Inst Med Trop Sao Paulo 2002, 44:55-56.
17. Mendonça C.L., Carvalho O.S., Mota E.M., Lenzi H.L. Development of Angiostrongylus costaricensis Morera and Cespedes 1971 (Nematoda: Angiostrongylidae) larvae in the intermediate host Sarasinula marginata (Semper 1885) (Mollusca: Soleolifera). Parasitol Res 2008, 102:861-865.
18. Carvalho Odos S., Teles H.M., Mota E.M., Lafeta C., de Mendonça G.F., Lenzi H.L. Potentiality of Achatina fulica Bowdich, 1822 (Mollusca: Gastropoda) as intermediate host of the Angiostrongylus costaricensis Morera & Céspedes 1971. Rev Soc Bras Med Trop 2003, 36:743-745.
19. Graeff-Teixeira C. Expansion of Achatina fulica in Brazil and potential increased risk for angiostrongyliasis. Trans R Soc Trop Med Hyg 2007, 101:743-744.
20. Thiengo S.C., Maldonado A., Mota E.M., Torres E.J., Caldeira R., Carvalho O.S., et al. The giant African snail Achatina fulica as natural intermediate host of Angiostrongylus cantonensis in Pernambuco, northeast Brazil. Acta Trop 2010, 115:194-199.
21. Rambo P.R., Agostini A.A., Graeff-Teixeira C. Abdominal angiostrongyliasis in southern Brazil-prevalence and parasitic burden in mollusc intermediate hosts from eighteen endemic foci. Mem Inst Oswaldo Cruz 1997, 92:9-14.
22. Graeff-Teixeira C., Goulart A.H., de Brum C.O., Laitano A.C., Sievers-Tostes C., Zanini G.M., et al. Longitudinal clinical and serological survey of abdominal angiostrongyliasis in Guapore, southern Brazil, from 1995 to 1999. Rev Soc Bras Med Trop 2005, 38:310-315.
23. Geiger S.M., Laitano A.C., Sievers-Tostes C., Agostini A.A., Schulz-Key H., Graeff-Teixeira C. Detection of the acute phase of abdominal angiostrongyliasis with a parasite-specific IgG enzyme linked immunosorbent assay. Mem Inst Oswaldo Cruz 2001, 96:515-518.
24. Palominos P.E., Gasnier R., Rodriguez R., Agostini A.A., Graeff-Teixeira C. Individual serological follow-up of patients with suspected or confirmed abdominal angiostrongyliasis. Mem Inst Oswaldo Cruz 2008, 103:93-97.
25. Graeff-Teixeira C., Camillo-Coura L., Lenzi H.L. Abdominal angiostrongyliasis-an under-diagnosed disease. Mem Inst Oswaldo Cruz 1987, 82(Suppl 4):353-354.
26. Morera P. Angiostrongiliasis abdominal, Un problema de salud pública ?. Rev Asoc Guatem Parasitol Med Trop 1987, 2:9-11.
27. Morera P., Amador J.A. Prevalencia de la angiostrongilosis abdominal y la distribución estacional de la precipitación. Rev Costarric Salud Pública 1998, 7:1-14.
28. Mesen-Ramirez P., Abrahams-Sandi E., Fernandez-Quesada K., Morera P. Angiostrongylus costaricensis egg antigen for the immunodiagnosis of abdominal angiostrongyliasis. J Helminthol 2008, 82:251-254.
29. Graeff-Teixeira C., Camillo-Coura L., Lenzi H.L. Histopathological criteria for the diagnosis of abdominal angiostrongyliasis. Parasitol Res 1991, 77:606-611.
30. Chabaud A.G. Description of Stefanskostrongylus dubosti n. sp., parasite of Potamogale and attempt at classification of Angiostrongylidae nematodes. Ann Parasitol Hum Comp 1972, 47:735-744.
31. Ubelaker J.E. Systematics of species referred to the genus Angiostrongylus. J Parasitol 1986, 72:237-244.
32. Baylis H.S. On a collection of nematodes from Nigerian mammals (chiefly rodents). Parasitology 1928, 20:280-304.
33. Fontanilla I.K., Wade C.M. The small subunit (SSU) ribosomal (r) RNA gene as a genetic marker for identifying infective 3rd juvenile stage Angiostrongylus cantonensis. Acta Trop 2008, 105:181-186.
34. Caldeira R.L., Carvalho O.S., Mendonça C.L., Graeff-Teixeira C., Silva M.C., Ben R., et al. Molecular differentiation of Angiostrongylus costaricensis, A. cantonensis, and A. vasorum by polymerase chain reaction-restriction fragment length polymorphism. Mem Inst Oswaldo Cruz 2003, 98:1039-1043.
35. Jefferies R., Shaw S.E., Viney M.E., Morgan E.R. Angiostrongylus vasorum from South America and Europe represent distinct lineages. Parasitology 2009, 136:107-115.
36. Eamsobhana P., Lim P.E., Zhang H., Gan X., Yong H.S. Molecular differentiation and phylogenetic relationships of three Angiostrongylus species and Angiostrongylus cantonensis geographical isolates based on a 66-kDa protein gene of A. cantonensis (Nematoda: Angiostrongylidae). Exp Parasitol 2010, 126:564-569.
37. Mota E.M., Lenzi H.L. Angiostrongylus costaricensis life cycle: a new proposal. Mem Inst Oswaldo Cruz 1995, 90:707-709.
38. Mota E.M., Lenzi H.L. Angiostrongylus costaricensis: complete redescription of the migratory pathways based on experimental Sigmodon hispidus infection. Mem Inst Oswaldo Cruz 2005, 100:407-420.
39. Vázquez J.J., Boils P.L., Sola J.J., Carbonell F., de Juan Burgueño M., Giner V., et al. Angiostrongyliasis in a European patient: a rare cause of gangrenous ischemic enterocolitis. Gastroenterology 1993, 105:1544-1549.
40. Neafie R.C., Marty A.M. Unusual infections in humans. Clin Microbiol Rev 1993, 6:34-56.
41. Silvera C.T., Ghali V.S., Roven S., Heimann J., Gelb A. Angiostrongyliasis: a rare cause of gastrointestinal hemorrhage. Am J Gastroenterol 1989, 84:329-332.
42. Loria-Cortes R., Lobo-Sanahuja J.F. Clinical abdominal angiostrongylosis. A study of 116 children with intestinal eosinophilic granuloma caused by Angiostrongylus costaricensis. Am J Trop Med Hyg 1980, 29:538-544.
43. Lobo Sanahuja F., Loria Cortes R., Gonzalez G. Abdominal angiostrongylosis. Clinical aspects, treatment and review of the literature. Bol Med Hosp Infant Mex 1987, 44:4-9.
44. Graeff-Teixeira C., Camillo-Coura L., Lenzi H.L. Clinical and epidemiological aspects of abdominal angiostrongyliasis in southern Brazil. Rev Inst Med Trop Sao Paulo 1991, 33:373-378.
45. Morera P., Perez F., Mora F., Castro L. Visceral larva migrans-like syndrome caused by Angiostrongylus costaricensis. Am J Trop Med Hyg 1982, 31:67-70.
46. Duarte Z., Morera P., Vuong P.N. Abdominal angiostrongyliasis in Nicaragua: a clinico-pathological study on a series of 12 cases reports. Ann Parasitol Hum Comp 1991, 66:259-262.
47. Vázquez J.J., Sola J.J., Boils P.L. Hepatic lesions induced by Angiostrongylus costaricensis. Histopathology 1994, 25:489-491.
48. Rodriguez R., Dequi R.M., Peruzzo L., Mesquita P.M., Garcia E., Fornari F. Abdominal angiostrongyliasis: report of two cases with different clinical presentations. Rev Inst Med Trop Sao Paulo 2008, 50:339-341.
49. Solano-Parada J., Gonzalez-Gonzalez G., Torro L.M., dos Santos M.F., Espino A.M., Burgos M., et al. Effectiveness of intranasal vaccination against Angiostrongylus costaricensis using a serine/threonine phosphatase 2 A synthetic peptide and recombinant antigens. Vaccine 2010, 28:5185-5196.
50. Harris T.W., Antoshechkin I., Bieri T., Blasiar D., Chan J., Chen W.J., et al. WormBase: a comprehensive resource for nematode research. Nucleic Acids Res 2010, 38:D463-D467.
51. The_C.elegans_Sequencing_Consortium Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 1998, 282:2012-2018.
52. Stein L.D., Bao Z., Blasiar D., Blumenthal T., Brent M.R., Chen N., et al. The genome sequence of Caenorhabditis briggsae: a platform for comparative genomics. PLoS Biol 2003, 1:E45.
53. Ghedin E., Wang S., Spiro D., Caler E., Zhao Q., Crabtree J., et al. Draft genome of the filarial nematode parasite Brugia malayi. Science 2007, 317:1756-1760.
54. Abad P., Gouzy J., Aury J.M., Castagnone-Sereno P., Danchin E.G., Deleury E., et al. Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nat Biotechnol 2008, 26:909-915.
55. Opperman C.H., Bird D.M., Williamson V.M., Rokhsar D.S., Burke M., Cohn J., et al. Sequence and genetic map of Meloidogyne hapla: A compact nematode genome for plant parasitism. Proc Natl Acad Sci U S A 2008, 105:14802-14807.
56. Dieterich C., Clifton S.W., Schuster L.N., Chinwalla A., Delehaunty K., Dinkelacker I., et al. The Pristionchus pacificus genome provides a unique perspective on nematode lifestyle and parasitism. Nat Genet 2008, 40:1193-1198.
57. Mitreva M., Jasmer D.P., Zarlenga D.S., Wang Z., Abubucker S., Martin J., et al. The draft genome of the parasitic nematode Trichinella spiralis. Nat Genet 2011, 43:228-235.
58. Shim Y.H., Paik Y.K. Caenorhabditis elegans proteomics comes of age. Proteomics 2010, 10:846-857.
59. Mitreva M., Zarlenga D.S., McCarter J.P., Jasmer D.P. Parasitic nematodes - from genomes to control. Vet Parasitol 2007, 148:31-42.
60. Barrett J. Forty years of helminth biochemistry. Parasitology 2009, 1-10.
61. Ranganathan S., Garg G. Secretome: clues into pathogen infection and clinical applications. Genome Med 2009, 1:113.
62. Yatsuda A.P., Krijgsveld J., Cornelissen A.W., Heck A.J., de Vries E. Comprehensive analysis of the secreted proteins of the parasite Haemonchus contortus reveals extensive sequence variation and differential immune recognition. J Biol Chem 2003, 278:16941-16951.
63. Robinson M., Gare D., Connolly B. Profiling excretory/secretory proteins of muscle larvae by two-dimensional gel electrophoresis and mass spectrometry. Vet Parasitol 2005, 132:37-41.
64. Robinson M.W., Greig R., Beattie K.A., Lamont D.J., Connolly B. Comparative analysis of the excretory-secretory proteome of the muscle larva of Trichinella pseudospiralis and Trichinella spiralis. Int J Parasitol 2007, 37:139-148.
65. Craig H., Wastling J.M., Knox D.P. A preliminary proteomic survey of the in vitro excretory/secretory products of fourth-stage larval and adult Teladorsagia circumcincta. Parasitology 2006, 132:535-543.
66. Moreno Y., Geary T.G. Stage- and gender-specific proteomic analysis of Brugia malayi excretory-secretory products. PLoS Negl Trop Dis 2008, 2:e326.
67. Hewitson J.P., Harcus Y.M., Curwen R.S., Dowle A.A., Atmadja A.K., Ashton P.D., et al. The secretome of the filarial parasite, Brugia malayi: proteomic profile of adult excretory-secretory products. Mol Biochem Parasitol 2008, 160:8-21.
68. Bennuru S., Semnani R., Meng Z., Ribeiro J.M., Veenstra T.D., Nutman T.B. Brugia malayi excreted/secreted proteins at the host/parasite interface: stage- and gender-specific proteomic profiling. PLoS Negl Trop Dis 2009, 3:e410.
69. Dea-Ayuela M.A., Bolas-Fernandez F. Two-dimensional electrophoresis and mass spectrometry for the identification of species-specific Trichinella antigens. Vet Parasitol 2005, 132:43-49.
70. Calvo E., Flores-Romero P., Lopez J.A., Navas A. Identification of proteins expressing differences among isolates of Meloidogyne spp. (Nematoda: Meloidogynidae) by nano-liquid chromatography coupled to ion-trap mass spectrometry. J Proteome Res 2005, 4:1017-1021.
71. Yan F., Xu L., Liu L., Yan R., Song X., Li X. Immunoproteomic analysis of whole proteins from male and female adult Haemonchus contortus. Vet J 2010, 185:174-179.
72. Islam M.K., Miyoshi T., Yokomizo Y., Tsuji N. The proteome expression patterns in adult Ascaris suum under exposure to aerobic/anaerobic environments analyzed by two-dimensional electrophoresis. Parasitol Res 2004, 93:96-101.
73. Morgan C., LaCourse E.J., Rushbrook B.J., Greetham D., Hamilton J.V., Barrett J., et al. Plasticity demonstrated in the proteome of a parasitic nematode within the intestine of different host strains. Proteomics 2006, 6:4633-4645.
74. Thiengo S.C., Vicente J.J., Pinto R.M. Redescription of Angiostrongylus (Paranstrongylus) costaricensis Morera & Céspedes (nematoda: metastrongyloidea) from brazilian strain. Rev Bras Zool 1997, 14:839-844.
75. Ubelaker J.E. Systematics of species referred to the genus Angiostrongylus. J Parasitol 1986, 72:237-244.
76. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
77. Rocha S.L., Neves-Ferreira A.G., Trugilho M.R., Chapeaurouge A., Leon I.R., Valente R.H., et al. Crotalid snake venom subproteomes unraveled by the antiophidic protein DM43. J Proteome Res 2009, 8:2351-2360.
78. León I.R., Neves-Ferreira A.G.C., Valente R.H., Mota E.M., Lenzi H.L., Perales J. Improved protein identification efficiency by mass spectrometry using N-terminal chemical derivatization of peptides from Angiostrongylus costaricensis, a nematode with unknown genome. J Mass Spectrom 2007, 42:781-792.
79. Ma B., Zhang K., Hendrie C., Liang C., Li M., Doherty-Kirby A., et al. PEAKS: powerful software for peptide de novo sequencing by tandem mass spectrometry. Rapid Commun Mass Spectrom 2003, 17:2337-2342.
80. Carvalho P.C., Fischer J.S.G., Chen E.I., Yates J.R., Barbosa V.C. PatternLab for proteomics: a tool for differential shotgun proteomics. BMC Bioinformatics 2008, 9:316.
81. Carvalho P.C., Fischer J.S.G., Chen E.I., Domont G.B., Carvalho M.G.C., Degrave W.M., et al. GO Explorer: A gene-ontology tool to aid in the interpretation of shotgun proteomics data. Proteome Sci 2009, 7:6.
82. McCarthy F.M., Wang N., Magee G.B., Nanduri B., Lawrence M.L., Camon E.B., et al. AgBase: a functional genomics resource for agriculture. BMC Genomics 2006, 7:229.
83. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J Mol Biol 1990, 215:403-410.
84. Ashburner M., Ball C.A., Blake J.A., Botstein D., Butler H., Cherry J.M., et al. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 2000, 25:25-29.
85. Görg A., Weiss W., Dunn M.J. Current two-dimensional electrophoresis technology for proteomics. Proteomics 2004, 4:3665-3685.
86. Rabilloud T. Use of thiourea to increase the solubility of membrane proteins in two-dimensional electrophoresis. Electrophoresis 1998, 19:758-760.
87. Ishih A., Rodriguez B.O., Sano M. Scanning electron microscopic observations of first and third-stage larvae and adults of Angiostrongylus costaricensis. Southeast Asian J Trop Med Public Health 1990, 21:568-573.
88. Carrette O., Burkhard P.R., Sanchez J.C., Hochstrasser D.F. State-of-the-art two-dimensional gel electrophoresis: a key tool of proteomics research. Nat Protoc 2006, 1:812-823.
89. Garcia-Murria M.J., Valero M.L., Sanchez del Pino M.M. Simple chemical tools to expand the range of proteomics applications. J Proteomics 2011, 74:137-150.
90. Kiel M., Josh P., Jones A., Windon R., Hunt P., Kongsuwan K. Identification of immuno-reactive proteins from a sheep gastrointestinal nematode, Trichostrongylus colubriformis, using two-dimensional electrophoresis and mass spectrometry. Int J Parasitol 2007, 37:1419-1429.
91. Weinkopff T., Atwood J.A., Punkosdy G.A., Moss D., Weatherly D.B., Orlando R., et al. Identification of antigenic Brugia adult worm proteins by peptide mass fingerprinting. J Parasitol 2009, 95:1429-1435.
92. Roberts L., Janovy J.J. Foundations in Parasitology 1996, 659. Wm.C.Brown Publishers, Chicago, USA. 5th edition.
93. Jolodar A., Fischer P., Bergmann S., Buttner D.W., Hammerschmidt S., Brattig N.W. Molecular cloning of an alpha-enolase from the human filarial parasite Onchocerca volvulus that binds human plasminogen. Biochim Biophys Acta 2003, 1627:111-120.
94. Bernal D., de la Rubia J.E., Carrasco-Abad A.M., Toledo R., Mas-Coma S., Marcilla A. Identification of enolase as a plasminogen-binding protein in excretory-secretory products of Fasciola hepatica. FEBS Lett 2004, 563:203-206.
95. Ramajo-Hernandez A., Perez-Sanchez R., Ramajo-Martin V., Oleaga A. Schistosoma bovis: plasminogen binding in adults and the identification of plasminogen-binding proteins from the worm tegument. Exp Parasitol 2007, 115:83-91.
96. Perez-Sanchez R., Valero M.L., Ramajo-Hernandez A., Siles-Lucas M., Ramajo-Martin V., Oleaga A. A proteomic approach to the identification of tegumental proteins of male and female Schistosoma bovis worms. Mol Biochem Parasitol 2008, 161:112-123.
97. Chiumiento L., Bruschi F. Enzymatic antioxidant systems in helminth parasites. Parasitol Res 2009, 105:593-603.
98. Bell A., Monaghan P., Page A.P. Peptidyl-prolyl cis-trans isomerases (immunophilins) and their roles in parasite biochemistry, host-parasite interaction and antiparasitic drug action. Int J Parasitol 2006, 36:261-276.
99. Bridges D., Moorhead G.B. 14-3-3 proteins: a number of functions for a numbered protein. Sci STKE 2005, 2005:re10.
100. Siles-Lucas M., Nunes C.P., Zaha A., Breijo M. The 14-3-3 protein is secreted by the adult worm of Echinococcus granulosus. Parasite Immunol 2000, 22:521-528.
101. McGonigle S., Loschiavo M., Pearce E.J. 14-3-3 proteins in Schistosoma mansoni; identification of a second epsilon isoform. Int J Parasitol 2002, 32:685-693.
102. Schechtman D., Tarrab-Hazdai R., Arnon R. The 14-3-3 protein as a vaccine candidate against schistosomiasis. Parasite Immunol 2001, 23:213-217.
103. Graeff-Teixeira C., Agostini A.A., Camillo-Coura L., Ferreira-da-Cruz M.F. Seroepidemiology of abdominal angiostrongyliasis: the standardization of an immunoenzymatic assay and prevalence of antibodies in two localities in southern Brazil. Trop Med Int Health 1997, 2:254-260.
104. Geiger S.M., Graeff-Teixeira C., Soboslay P.T., Schulz-Key H. Experimental Angiostrongylus costaricensis infection in mice: immunoglobulin isotype responses and parasite-specific antigen recognition after primary low-dose infection. Parasitol Res 1999, 85:200-205.
105. Bender A.L., Maurer R.L., da Silva M.C., Ben R., Terraciano P.B., da Silva A.C., et al. Eggs and reproductive organs of female Angiostrongylus costaricensis are more intensely recognized by human sera from acute phase in abdominal angiostrongyliasis. Rev Soc Bras Med Trop 2003, 36:449-454.
106. Lehman W., Szent-Gyorgyi A.G. Regulation of muscular contraction. Distribution of actin control and myosin control in the animal kingdom. J Gen Physiol 1975, 66:1-30.
107. Otey C.A., Kalnoski M.H., Lessard J.L., Bulinski J.C. Immunolocalization of the gamma isoform of nonmuscle actin in cultured cells. J Cell Biol 1986, 102:1726-1737.
108. Galletta B.J., Cooper J.A. Actin and endocytosis: mechanisms and phylogeny. Curr Opin Cell Biol 2009, 21:20-27.
109. Dell A., Haslam S.M., Morris H.R., Khoo K.H. Immunogenic glycoconjugates implicated in parasitic nematode diseases. Biochim Biophys Acta 1999, 1455:353-362.
110. Zugel U., Kaufmann S.H. Role of heat shock proteins in protection from and pathogenesis of infectious diseases. Clin Microbiol Rev 1999, 12:19-39.
111. Lindquist S., Craig E.A. The heat-shock proteins. Annu Rev Genet 1988, 22:631-677.
112. Suto R., Srivastava P.K. A mechanism for the specific immunogenicity of heat shock protein-chaperoned peptides. Science 1995, 269:1585-1588.
113. Michalak M., Corbett E.F., Mesaeli N., Nakamura K., Opas M. Calreticulin: one protein, one gene, many functions. Biochem J 1999, 344(Pt 2):281-292.
114. Ramírez G., Valck C., Ferreira V.P., López N., Ferreira A. Extracellular Trypanosoma cruzi calreticulin in the host-parasite interplay. Trends Parasitol 2011, 27:115-122.
115. Park B.J., Lee D.G., Yu J.R., Jung S.K., Choi K., Lee J., et al. Calreticulin, a calcium-binding molecular chaperone, is required for stress response and fertility in Caenorhabditis elegans. Mol Biol Cell 2001, 12:2835-2845.
116. Rzepecka J., Rausch S., Klotz C., Schnoller C., Kornprobst T., Hagen J., et al. Calreticulin from the intestinal nematode Heligmosomoides polygyrus is a Th2-skewing protein and interacts with murine scavenger receptor-A. Mol Immunol 2009, 46:1109-1119.
117. Kasper G., Brown A., Eberl M., Vallar L., Kieffer N., Berry C., et al. A calreticulin-like molecule from the human hookworm Necator americanus interacts with C1q and the cytoplasmic signalling domains of some integrins. Parasite Immunol 2001, 23:141-152.
118. Winter A.D., McCormack G., Page A.P. Protein disulfide isomerase activity is essential for viability and extracellular matrix formation in the nematode Caenorhabditis elegans. Dev Biol 2007, 308:449-461.
119. Larsen P.L., Albert P.S., Riddle D.L. Genes that regulate both development and longevity in Caenorhabditis elegans. Genetics 1995, 139:1567-1583.
120. Curran S.P., Ruvkun G. Lifespan regulation by evolutionarily conserved genes essential for viability. PLoS Genet 2007, 3:e56.
121. Cassada R.C., Russell R.L. The dauerlarva, a post-embryonic developmental variant of the nematode Caenorhabditis elegans. Dev Biol 1975, 46:326-342.
122. Klass M.R. Aging in the nematode Caenorhabditis elegans: major biological and environmental factors influencing life span. Mech Ageing Dev 1977, 6:413-429.
123. Leffler H., Carlsson S., Hedlund M., Qian Y., Poirier F. Introduction to galectins. Glycoconj J 2004, 19:433-440.
124. Young A.R., Meeusen E.N. Galectins in parasite infection and allergic inflammation. Glycoconj J 2004, 19:601-606.
125. Dzik J.M. Molecules released by helminth parasites involved in host colonization. Acta Biochim Pol 2006, 53:33-64.
126. Hirabayashi J., Kasai K. The family of metazoan metal-independent beta-galactoside-binding lectins: structure, function and molecular evolution. Glycobiology 1993, 3:297-304.
127. Leffler H. Introduction to galectins. Trends Glycosci Glycotechnol 1997, 45:9-19.
128. Arata Y., Akimoto Y., Hirabayashi J., Kasai K., Hirano H. An immunohistochemical study of the 32-kDa galectin (beta-galactoside-binding lectin) in the nematode Caenorhabditis elegans. Histochem J 1996, 28:201-207.