An atlas for schistosoma mansoni organs and life-cycle stages using cell type-specific markers and confocal microscopy

PLoS Neglected Tropical Diseases

Volumn 5, Issue 3, 2011, Pages

  Collins III, James J ^a   King, Ryan S ^a   Cogswell, Alexis ^b   Williams, David L ^b   Newmark, Phillip A ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b RUSH UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MARKER; LECTIN;

ANIMAL ANATOMY; ANTIBODY LABELING; ARTICLE; CELL LABELING; CELL TYPE; CERCARIA; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FLUORESCENCE ANALYSIS; MIRACIDIUM; MORPHOLOGICAL TRAIT; NONHUMAN; SCHISTOSOMA MANSONI; TREMATODE LIFE CYCLE STAGE; WORM TEGUMENT; ANIMAL; ANIMAL STRUCTURES; FEMALE; HISTOLOGY; LIFE CYCLE STAGE; MALE; METHODOLOGY; MOUSE; PARASITOLOGY; STAINING;

ANIMAL STRUCTURES; ANIMALS; FEMALE; LIFE CYCLE STAGES; MALE; MICE; MICROSCOPY, CONFOCAL; PARASITOLOGY; SCHISTOSOMA MANSONI; STAINING AND LABELING;

EID: 79953781201     PISSN: None     EISSN: None     Source Type: Journal    
DOI: 10.1371/journal.pntd.0001009     Document Type: Article

References (63)

1. Chitsulo L, Engels D, Montresor A, Savioli L, (2000) The global status of schistosomiasis and its control. Acta Trop 77: 41-51.
2. Basch PF, (1991) Schistosomes: Development, Reproduction, and Host Relations. New York Oxford University Press.
3. Freitas TC, Jung E, Pearce EJ, (2007) TGF-beta signaling controls embryo development in the parasitic flatworm Schistosoma mansoni. PLoS Pathog 3: e52.
4. Rinaldi G, Morales ME, Alrefaei YN, Cancela M, Castillo E, et al. (2009) RNA interference targeting leucine aminopeptidase blocks hatching of Schistosoma mansoni eggs. Mol Biochem Parasitol 167: 118-126.
5. Skelly PJ, Da'dara A, Harn DA, (2003) Suppression of cathepsin B expression in Schistosoma mansoni by RNA interference. Int J Parasitol 33: 363-369.
6. Morales ME, Rinaldi G, Gobert GN, Kines KJ, Tort JF, et al. (2008) RNA interference of Schistosoma mansoni cathepsin D, the apical enzyme of the hemoglobin proteolysis cascade. Mol Biochem Parasitol 157: 160-168.
7. Kuntz AN, Davioud-Charvet E, Sayed AA, Califf LL, Dessolin J, et al. (2007) Thioredoxin glutathione reductase from Schistosoma mansoni: an essential parasite enzyme and a key drug target. PLoS Med 4: e206.
8. Stefanic S, Dvorak J, Horn M, Braschi S, Sojka D, et al. (2010) RNA Interference in Schistosoma mansoni Schistosomula: Selectivity, Sensitivity and Operation for Larger-Scale Screening. PLoS Negl Trop Dis 4: e850.
9. Swierczewski BE, Davies SJ, (2009) A schistosome cAMP-dependent protein kinase catalytic subunit is essential for parasite viability. PLoS Negl Trop Dis 3: e505.
10. Mourao MM, Dinguirard N, Franco GR, Yoshino TP, (2009) Phenotypic screen of early-developing larvae of the blood fluke, Schistosoma mansoni, using RNA interference. PLoS Negl Trop Dis 3: e502.
11. Kines KJ, Mann VH, Morales ME, Shelby BD, Kalinna BH, et al. (2006) Transduction of Schistosoma mansoni by vesicular stomatitis virus glycoprotein-pseudotyped Moloney murine leukemia retrovirus. Exp Parasitol 112: 209-220.
12. Morales ME, Mann VH, Kines KJ, Gobert GN, Fraser MJ Jr, et al. (2007) piggyBac transposon mediated transgenesis of the human blood fluke, Schistosoma mansoni. FASEB J 21: 3479-3489.
13. Kines KJ, Morales ME, Mann VH, Gobert GN, Brindley PJ, (2008) Integration of reporter transgenes into Schistosoma mansoni chromosomes mediated by pseudotyped murine leukemia virus. FASEB J 22: 2936-2948.
14. Kines KJ, Rinaldi G, Okatcha TI, Morales ME, Mann VH, et al. (2010) Electroporation facilitates introduction of reporter transgenes and virions into schistosome eggs. PLoS Negl Trop Dis 4: e593.
15. Dillon GP, Illes JC, Isaacs HV, Wilson RA, (2007) Patterns of gene expression in schistosomes: localization by whole mount in situ hybridization. Parasitology 134: 1589-1597.
16. Berriman M, Haas BJ, LoVerde PT, Wilson RA, Dillon GP, et al. (2009) The genome of the blood fluke Schistosoma mansoni. Nature 460: 352-358.
17. Liu F, Zhou Y, Wang ZQ, Lu G, Zheng H, et al. (2009) The Schistosoma japonicum genome reveals features of host-parasite interplay. Nature 460: 345-351.
18. Neves RH, de Lamare Biolchini C, Machado-Silva JR, Carvalho JJ, Branquinho TB, et al. (2005) A new description of the reproductive system of Schistosoma mansoni (Trematoda: Schistosomatidae) analyzed by confocal laser scanning microscopy. Parasitol Res 95: 43-49.
19. Beckmann S, Quack T, Burmeister C, Buro C, Long T, et al. (2010) Schistosoma mansoni: signal transduction processes during the development of the reproductive organs. Parasitology 137: 497-520.
20. Mair GR, Maule AG, Fried B, Day TA, Halton DW, (2003) Organization of the musculature of schistosome cercariae. J Parasitol 89: 623-625.
21. Mair GR, Maule AG, Day TA, Halton DW, (2000) A confocal microscopical study of the musculature of adult Schistosoma mansoni. Parasitology 121 (Pt 2): 163-170.
22. Wu XJ, Sabat G, Brown JF, Zhang M, Taft A, et al. (2009) Proteomic analysis of Schistosoma mansoni proteins released during in vitro miracidium-to-sporocyst transformation. Mol Biochem Parasitol 164: 32-44.
23. Robb SM, Sánchez Alvarado A, (2002) Identification of immunological reagents for use in the study of freshwater planarians by means of whole-mount immunofluorescence and confocal microscopy. Genesis 32: 293-298.
24. Cebrià F, (2008) Organization of the nervous system in the model planarian Schmidtea mediterranea: an immunocytochemical study. Neurosci Res 61: 375-384.
25. Gustafsson MK, (1987) Immunocytochemical demonstration of neuropeptides and serotonin in the nervous systems of adult Schistosoma mansoni. Parasitol Res 74: 168-174.
26. Basch PF, Gupta BC, (1988) Immunocytochemical localization of regulatory peptides in six species of trematode parasites. Comp Biochem Physiol C 91: 565-570.
27. Gupta BC, Basch PF, (1989) Human chorionic gonadotropin-like immunoreactivity in schistosomes and Fasciola. Parasitol Res 76: 86-89.
28. Callaerts P, Vulsteke V, Peumans W, De Loof A, (1995) Lectin binding sites during Drosophila embryogenesis. Roux's Arch Dev Biol 204: 229-243.
29. Zayas R, Cebrià F, Guo T, Feng J, Newmark P, (2010) The use of lectins as markers for differentiated secretory cells in planarians. Developemental Dynamics In Press.
30. Hayunga EG, Sumner MP, (1986) Expression of lectin-binding surface glycoproteins during the development of Schistosoma mansoni schistosomula. J Parasitol 72: 913-920.
31. Linder E, (1985) Schistosoma mansoni: visualization with fluorescent lectins of secretions and surface carbohydrates of living cercariae. Exp Parasitol 59: 307-312.
32. Linder E, Huldt G, (1982) Distribution of exposed and hidden carbohydrates of Schistosoma mansoni adult worms demonstrated by selective binding of fluorochrome-conjugated lectins. Parasitology 85 (Pt 3): 503-509.
33. Nanduri J, Dennis JE, Rosenberry TL, Mahmoud AA, Tartakoff AM, (1991) Glycocalyx of bodies versus tails of Schistosoma mansoni cercariae. Lectin-binding, size, charge, and electron microscopic characterization. J Biol Chem 266: 1341-1347.
34. Coles G, Jansson H, Zuckerman B, (1988) Lectin studies of surface carbohydrates and induction of gland secretion in the free-living stages of Schistosoma mansoni. Journal of Chemical Ecology 14: 691-700.
35. Lewis F, (2001) Schistosomiasis. Curr Protoc Immunol Chapter 19: Unit 19 11.
36. Mann VH, Morales ME, Rinaldi G, Brindley PJ, (2009) Culture for genetic manipulation of developmental stages of Schistosoma mansoni. Parasitology 137: 451-462.
37. Abramoff MD, Magelhaes PJ, Ram SJ, (2004) Image Processing with ImageJ. Biophotonics International 11: 36-42.
38. Dorsey CH, Cousin CE, Lewis FA, Stirewalt MA, (2002) Ultrastructure of the Schistosoma mansoni cercaria. Micron 33: 279-323.
39. Hyman L, (1951) The Invertebrates: Platyhelminthes and Rhynchocoela The Acoelomate Bilateria. New York McGraw-Hill Book Company, Inc.
40. Dorsey CH, Stirewalt MA, (1971) Schistosoma mansoni: fine structure of cercarial acetabular glands. Exp Parasitol 30: 199-214.
41. Stirewalt MA, Austin BE, (1973) Collection of secreted protease from the preacetabular glands of cercariae of Schistosoma mansoni. J Parasitol 59: 741-743.
42. Stirewalt MA, Walters M, (1973) Schistosoma mansoni: histochemical analysis of the postacetabular gland secretion of cercariae. Exp Parasitol 33: 56-72.
43. Dorsey CH, (1976) Schistosoma mansoni: description of the head gland of cercariae and schistosomules at the ultrastructural level. Exp Parasitol 39: 444-459.
44. Wilson RA, Webster LA, (1974) Protonephridia. Biol Rev Camb Philos Soc 49: 127-160.
45. Faghiri Z, Skelly PJ, (2009) The role of tegumental aquaporin from the human parasitic worm, Schistosoma mansoni, in osmoregulation and drug uptake. FASEB J 23: 2780-2789.
46. Skelly PJ, Shoemaker CB, (2001) Schistosoma mansoni proteases Sm31 (cathepsin B) and Sm32 (legumain) are expressed in the cecum and protonephridia of cercariae. J Parasitol 87: 1218-1221.
47. Halton DW, Maule AG, (2004) Flatworm nerve-muscle: structural and functional analysis. Canadian Journal of Zoology 82: 316-333.
48. Collins JJ III, Hou X, Romanova EV, Lambrus BG, Miller CM, et al. (2010) Genome-Wide Analyses Reveal a Role for Peptide Hormones in Planarian Germline Development. PLoS Biol 8: e1000509.
49. Klagges BR, Heimbeck G, Godenschwege TA, Hofbauer A, Pflugfelder GO, et al. (1996) Invertebrate synapsins: a single gene codes for several isoforms in Drosophila. J Neurosci 16: 3154-3165.
50. Bogers JJ, Nibbeling HA, van Marck EA, Deelder AM, (1994) Immunofluorescent visualization of the excretory and gut system of Schistosoma mansoni by confocal laser scanning microscopy. Am J Trop Med Hyg 50: 612-619.
51. Gönnert R, (1955) Schistosomiasis studies. I. Contributions to the anatomy and histology of Schistosoma mansoni. Z Tropenmed Parasitol 6: 18-33.
52. Robinson DN, Cant K, Cooley L, (1994) Morphogenesis of Drosophila ovarian ring canals. Development 120: 2015-2025.
53. Smyth JD, Halton DW, (1983) The Physiology of Trematodes. Cambridge Cambridge University Press.
54. Wells KE, Cordingley JS, (1991) Schistosoma mansoni: eggshell formation is regulated by pH and calcium. Exp Parasitol 73: 295-310.
55. Erasmus DA, (1973) A comparative study of the reproductive system of mature, immature and "unisexual" female Schistosoma mansoni. Parasitology 67: 165-183.
56. Spence IM, Silk MH, (1971) Ultrastructural studies of the blood fluke-Schistosoma mansoni. V. The female reproductive system-a preliminary report. S Afr J Med Sci 36: 41-50.
57. Gönnert R, (1955) Schistosomiasis studies. II. Oogenesis of Schistosoma mansoni and the development of the eggs in the host organism. Z Tropenmed Parasitol 6: 33-52.
58. Pan SC, (1980) The fine structure of the miracidium of Schistosoma mansoni. J Invertebr Pathol 36: 307-372.
59. Bahia D, Avelar LG, Vigorosi F, Cioli D, Oliveira GC, et al. (2006) The distribution of motor proteins in the muscles and flame cells of the Schistosoma mansoni miracidium and primary sporocyst. Parasitology 133: 321-329.
60. Sato H, Kusel JR, Thornhill J, (2004) Excretion of fluorescent substrates of mammalian multidrug resistance-associated protein (MRP) in the Schistosoma mansoni excretory system. Parasitology 128: 43-52.
61. Sato H, Kusel JR, Thornhill J, (2002) Functional visualization of the excretory system of adult Schistosoma mansoni by the fluorescent marker resorufin. Parasitology 125: 527-535.
62. Kusel JR, Oliveira FA, Todd M, Ronketti F, Lima SF, et al. (2006) The effects of drugs, ions, and poly-l-lysine on the excretory system of Schistosoma mansoni. Mem Inst Oswaldo Cruz 101 (Suppl 1): 293-298.
63. Tan HH, Thornhill JA, Al-Adhami BH, Akhkha A, Kusel JR, (2003) A study of the effect of surface damage on the uptake of Texas Red-BSA by schistosomula of Schistosoma mansoni. Parasitology 126: 235-240.