Mechanics of the Toxoplasma gondii oocyst wall

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 28, 2013, Pages 11535-11540

  Dumètre, Aurélien ^a   Dubey, Jitender P ^b   Ferguson, David J P ^c   Bongrand, Pierre ^d,e   Azas, Nadine ^a   Puech, Pierre Henri ^d  

^a AIX MARSEILLE UNIVERSITY   (France)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d Aix Marseille University Luminy Campus   (France)

^e HÔPITAL DE LA CONCEPTION   (France)

Author keywords

Oocyst integrity; Oocyst resistance; Oocyst structure; Toxoplasma infectivity; Transmission

Indexed keywords

ARTICLE; ATOMIC FORCE MICROSCOPY; CONTROLLED STUDY; ELASTICITY; ELECTRON MICROSCOPY; FLUORESCENCE; FUNGAL STRUCTURES; MECHANICS; NONHUMAN; OOCYST; OOCYST WALL; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; TOXOPLASMA GONDII; ULTRASTRUCTURE; YOUNG MODULUS;

OOCYST INTEGRITY; OOCYST RESISTANCE; OOCYST STRUCTURE; TOXOPLASMA INFECTIVITY; TRANSMISSION;

ANIMALS; CELL WALL; MICROSCOPY, ATOMIC FORCE; MICROSCOPY, FLUORESCENCE; OOCYSTS; TOXOPLASMA;

ANIMALIA; PROTOZOA; TOXOPLASMA; TOXOPLASMA GONDII;

EID: 84879891208     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1308425110     Document Type: Article

References (59)

1. Dubey J (2010) Toxoplasmosis of Animals and Humans (CRC Press, Boca Raton, FL), 2nd Ed, pp 1-313.
2. Bahia-Oliveira LMG, et al. (2003) Highly endemic, waterborne toxoplasmosis in north Rio de Janeiro state, Brazil. Emerg Infect Dis 9(1):55-62.
3. de Moura L, et al. (2006) Waterborne toxoplasmosis, Brazil, from field to gene. Emerg Infect Dis 12(2):326- 329.
4. Jones JL, Dubey JP (2010) Waterborne toxoplasmosis - recent developments. Exp Parasitol 124(1):10-25.
5. Boyer K, et al.; Toxoplasmosis Study Group (2011) Unrecognized ingestion of Toxoplasma gondii oocysts leads to congenital toxoplasmosis and causes epidemics in North America. Clin Infect Dis 53(11):1081-1089.
6. Dattoli VCC, et al. (2011) Oocyst ingestion as an important transmission route of Toxoplasma gondii in Brazilian urban children. J Parasitol 97(6):1080-1084.
7. Robert-Gangneux F, Dardé M-L (2012) Epidemiology of and diagnostic strategies for toxoplasmosis. Clin Microbiol Rev 25(2):264-296.
8. Dumètre A, et al. (2012) Interaction forces drive the environmental transmission of pathogenic protozoa. Appl Environ Microbiol 78(4):905-912.
9. Bushkin GG, et al. (2012) β-1,3-glucan, which can be targeted by drugs, forms a trabecular scaffold in the oocyst walls of Toxoplasma and Eimeria. mBio 3(5):e00258-12.
10. Fritz HM, Bowyer PW, Bogyo M, Conrad PA, Boothroyd JC (2012) Proteomic analysis of fractionated Toxoplasma oocysts reveals clues to their environmental resistance. PLoS ONE 7(1):e29955.
11. Fritz HM, et al. (2012) Transcriptomic analysis of toxoplasma development reveals many novel functions and structures specific to sporozoites and oocysts. PLoS ONE 7:2):e29998.
12. Mai K, et al. (2009) Oocyst wall formation and composition in coccidian parasites. Mem Inst Oswaldo Cruz 104(2):281-289.
13. Possenti A, et al. (2010) Molecular characterisation of a novel family of cysteine-rich proteins of Toxoplasma gondii and ultrastructural evidence of oocyst wall localisation. Int J Parasitol 40(14):1639- 1649.
14. Dumètre A, et al. (2008) Effects of ozone and ultraviolet radiation treatments on the infectivity of Toxoplasma gondii oocysts. Vet Parasitol 153(3-4):209- 213.
15. Wainwright KE, et al. (2007) Chemical inactivation of Toxoplasma gondii oocysts in water. J Parasitol 93(4):925-931. (Pubitemid 47502210)
16. Wainwright KE, et al. (2007) Physical inactivation of Toxoplasma gondii oocysts in water. Appl Environ Microbiol 73(17):5663-5666. (Pubitemid 47378777)
17. Villegas EN, et al. (2010) Using quantitative reverse transcriptase PCR and cell culture plaque assays to determine resistance of Toxoplasma gondii oocysts to chemical sanitizers. J Microbiol Methods 81(3):219-225.
18. Ware MW, et al. (2010) Determining UV inactivation of Toxoplasma gondii oocysts by using cell culture and a mouse bioassay. Appl Environ Microbiol 76(15):5140-5147.
19. Dubey JP, Frenkel JK (1972) Cyst-induced toxoplasmosis in cats. J Protozool 19(1):155-177.
20. Ferguson DJ, Hutchison WM, Dunachie JF, Siim JC (1974) Ultrastructural study of early stages of asexual multiplication and microgametogony of Toxoplasma gondii in the small intestine of the cat. Acta Pathol Microbiol Scand B Microbiol Immunol 82(2):167-181.
21. Ferguson DJ, Hutchison WM, Siim JC (1975) The ultrastructural development of the macrogamete and formation of the oocyst wall of Toxoplasma gondii. Acta Pathol Microbiol Scand [B] 83(5):491-505.
22. Dubey JP, Miller NL, Frenkel JK (1970) The Toxoplasma gondii oocyst from cat feces. J Exp Med 132(4):636-662.
23. Ferguson DJ, Birch-Andersen A, Siim JC, Hutchison WM (1979) Ultrastructural studies on the sporulation of oocysts of Toxoplasma gondii. III. Formation of the sporozoites within the sporocysts. Acta Pathol Microbiol Scand [B] 87(4):253-260.
24. Speer CA, Clark S, Dubey JP (1998) Ultrastructure of the oocysts, sporocysts, and sporozoites of Toxoplasma gondii. J Parasitol 84(3):505-512. (Pubitemid 28280652)
25. Dumètre A, Dardé ML (2003) How to detect Toxoplasma gondii oocysts in environmental samples? FEMS Microbiol Rev 27(5):651-661.
26. Belli SI, Smith NC, Ferguson DJP (2006) The coccidian oocyst: A tough nut to crack!. Trends Parasitol 22(9):416-423. (Pubitemid 44176413)
27. Dubey JP (1998) Toxoplasma gondii oocyst survival under defined temperatures. J Parasitol 84(4):862-865.
28. Belli SI, Wallach MG, Luxford C, Davies MJ, Smith NC (2003) Roles of tyrosine-rich precursor glycoproteins and dityrosine- and 3,4- dihydroxyphenylalanine-mediated protein cross-linking in development of the oocyst wall in the coccidian parasite Eimeria maxima. Eukaryot Cell 2(3):456-464. (Pubitemid 36774694)
29. Lindquist HDA, et al. (2003) Autofluorescence of Toxoplasma gondii and related coccidian oocysts. J Parasitol 89(4):865-867. (Pubitemid 37151600)
30. Franz C, Puech P-H (2008) Atomic force microscopy: A versatile tool for studying cell morphology, adhesion and mechanics. Cell Mol Bioeng 1(4):289-300.
31. Müller DJ, Dufrêne YF (2011) Force nanoscopy of living cells. Curr Biol 21(6):R212-R216.
32. Müller DJ, Krieg M, Alsteens D, Dufrêne YF (2009) New frontiers in atomic force microscopy: Analyzing interactions from single-molecules to cells. Curr Opin Biotechnol 20(1):4-13.
33. Müller DJ, Dufrêne YF (2008) Atomic force microscopy as a multifunctional molecular toolbox in nanobiotechnology. Nat Nanotechnol 3(5):261-269.
34. Friedrichs J, Taubenberger A, Franz CM, Muller DJ (2007) Cellular remodelling of individual collagen fibrils visualized by time-lapse AFM. J Mol Biol 372(3):594-607. (Pubitemid 47313484)
35. Muller DJ (2008) AFM: A nanotool in membrane biology. Biochemistry 47(31):7986-7998.
36. Müller DJ, et al. (2006) Single-molecule studies of membrane proteins. Curr Opin Struct Biol 16(4):489-495. (Pubitemid 44149062)
37. Radmacher M (2002) Measuring the elastic properties of living cells by the atomic force microscope. Methods Cell Biol 68:67-90.
38. Radmacher M (2007) Studying the mechanics of cellular processes by atomic force microscopy. Methods Cell Biol 83:347-372.
39. Milosavljevic N, et al. (2010) Nongenomic effects of cisplatin: Acute inhibition of mechanosensitive transporters and channels without actin remodeling. Cancer Res 70:19):7514-7522.
40. Hampoelz B, et al. (2011) Microtubule-induced nuclear envelope fluctuations control chromatin dynamics in Drosophila embryos. Development 138(16):3377-3386.
41. Puech P-H, Poole K, Knebel D, Muller DJ (2006) A new technical approach to quantify cell-cell adhesion forces by AFM. Ultramicroscopy 106(8-9):637-644. (Pubitemid 43994307)
42. Fierro FA, et al. (2008) BCR/ABL expression of myeloid progenitors increases beta1-integrin mediated adhesion to stromal cells. J Mol Biol 377(4):1082-1093.
43. Taubenberger A, et al. (2007) Revealing early steps of alpha2beta1 integrin-mediated adhesion to collagen type I by using single-cell force spectroscopy. Mol Biol Cell 18(5):1634-1644. (Pubitemid 46717546)
44. Franz CM, Taubenberger A, Puech P-H, Müller DJ (2007) Studying integrin-mediated cell adhesion at the single-molecule level using AFM force spectroscopy. Sci STKE 2007 (406):pl5.
45. Puech P-H, et al. (2011) Force measurements of TCR/pMHC recognition at T cell surface. PLoS ONE 6(7):e22344.
46. Puech P-H, et al. (2005) Measuring cell adhesion forces of primary gastrulating cells from zebrafish using atomic force microscopy. J Cell Sci 118(Pt 18):4199-4206. (Pubitemid 41488957)
47. Ulrich F, et al. (2005) Wnt11 functions in gastrulation by controlling cell cohesion through Rab5c and E-cadherin. Dev Cell 9(4):555-564. (Pubitemid 41430738)
48. Ferguson DJ, Birch-Andersen A, Siim JC, Hutchison WM (1979) Ultrastructural studies on the sporulation of oocysts of Toxoplasma gondii. I. Development of the zygote and formation of the sporoblasts. Acta Pathol Microbiol Scand [B] 87B(3):171-181. (Pubitemid 9214176)
49. Dumètre A, Dardé M-L (2007) Detection of Toxoplasma gondii in water by an immunomagnetic separation method targeting the sporocysts. Parasitol Res 101(4):989-996.
50. Dubreuil F, Elsner N, Fery A (2003) Elastic properties of polyelectrolyte capsules studied by atomic-force microscopy and RICM. Eur Phys J E Soft Matter 12(2):215-221.
51. Dubremetz JF, Ferguson DJP (2009) The role played by electron microscopy in advancing our understanding of Toxoplasma gondii and other apicomplexans. Int J Parasitol 39(8):883 - 893.
52. Delcea M, et al. (2010) Mechanobiology: Correlation between mechanical stability of microcapsules studied by AFM and impact of cell-induced stresses. Small 6(24):2858-2862.
53. Byrd TL, Walz JY (2005) Interaction force profiles between Cryptosporidium parvum oocysts and silica surfaces. Environ Sci Technol 39(24):9574-9582. (Pubitemid 41832133)
54. Byrd TL, Walz JY (2007) Investigation of the interaction force between Cryptosporidium parvum oocysts and solid surfaces. Langmuir 23(14):7475-7483. (Pubitemid 47116405)
55. Considine RF, Dixon DR, Drummond CJ (2002) Oocysts of Cryptosporidium parvum and model sand surfaces in aqueous solutions: An atomic force microscope (AFM) study. Water Res 36(14):3421-3428. (Pubitemid 34879786)
56. Considine R, Dixon D, Drummond C (2000) Laterally-resolved force microscopy of biological microspheres-oocysts of Cryptosporidium parvum. Langmuir 16:1323-1330. (Pubitemid 30562248)
57. Dubey JP, et al. (2011) Isolation of viable Toxoplasma gondii from feral guinea fowl (Numida meleagris) and domestic rabbits (Oryctolagus cuniculus) from Brazil. J Parasitol 97(5):842-845.
58. Dumètre A, Dardé M-L (2005) Immunomagnetic separation of Toxoplasma gondii oocysts using a monoclonal antibody directed against the oocyst wall. J Microbiol Methods 61(2):209- 217.
59. Butt H-J, Jaschke M (1995) Calculation of thermal noise in atomic force microscopy. Nanotechnology 6:1-7.