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Cryptosporidium infections: molecular advances

Published online by Cambridge University Press:  28 March 2014

MATTHIAS LENDNER  and
ARWID DAUGSCHIES
MATTHIAS LENDNER*
Affiliation:
Institute for Parasitology, An den Tierkliniken 35, 04103 Leipzig, Germany
ARWID DAUGSCHIES
Affiliation:
Institute for Parasitology, An den Tierkliniken 35, 04103 Leipzig, Germany
*
* Corresponding author: Matthias Lendner, Institut für Parasitologie, An den Tierkliniken 35, 04103 Leipzig, Germany. E-mail: [email protected]
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Summary

Cryptosporidium host cell interaction remains fairly obscure compared with other apicomplexans such as Plasmodium or Toxoplasma. The reason for this is probably the inability of this parasite to complete its life cycle in vitro and the lack of a system to genetically modify Cryptosporidium. However, there is a substantial set of data about the molecules involved in attachment and invasion and about the host cell pathways involved in actin arrangement that are altered by the parasite. Here we summarize the recent advances in research on host cell infection regarding the excystation process, attachment and invasion, survival in the cell, egress and the available data on omics.

Keywords

CryptosporidiumApicomplexahost-parasite interactionattachmentinvasionegressmucinactinomics
Type
Special Issue Article
Information
Parasitology , Volume 141 , Special Issue 11: ApiCOWplexa 2013 – 2nd International Meeting on Apicomplexan Parasites in Farm Animals , September 2014 , pp. 1511 - 1532
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Copyright © Cambridge University Press 2014 

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References

REFERENCES

Abrahamsen, M. S., Templeton, T. J., Enomoto, S., Abrahante, J. E., Zhu, G., Lancto, C. A., Deng, M., Liu, C., Widmer, G., Tzipori, S., Buck, G. A., Xu, P., Bankier, A. T., Dear, P. H., Konfortov, B. A., Spriggs, H. F., Iyer, L., Anantharaman, V., Aravind, L. and Kapur, V. (2004). Complete genome sequence of the apicomplexan, Cryptosporidium parvum . Science (New York, NY) 304, 441–445. doi: 10.1126/science.1094786.Google Scholar
Anderson, A. C. (2005). Two crystal structures of dihydrofolate reductase-thymidylate synthase from Cryptosporidium hominis reveal protein-ligand interactions including a structural basis for observed antifolate resistance. Acta Crystallographica. Section F, Structural Biology and Crystallization Communications 61, 258–262. doi: 10.1107/S1744309105002435.Google Scholar
Artz, J. D., Wernimont, A. K., Allali-Hassani, A., Zhao, Y., Amani, M., Lin, Y.-H., Senisterra, G., Wasney, G. A., Fedorov, O., King, O., Roos, A., Lunin, V. V., Qiu, W., Finerty, P., Hutchinson, A., Chau, I., von Delft, F., MacKenzie, F., Lew, J., Kozieradzki, I., Vedadi, M., Schapira, M., Zhang, C., Shokat, K., Heightman, T. and Hui, R. (2011). The Cryptosporidium parvum kinome. BMC Genomics 12, 478. doi: 10.1186/1471-2164-12-478.Google Scholar
Atuma, C., Strugala, V., Allen, A. and Holm, L. (2001). The adherent gastrointestinal mucus gel layer: thickness and physical state in vivo . American Journal of Physiology. Gastrointestinal and Liver Physiology 280, G922–G929.CrossRefGoogle ScholarPubMed
Barnes, D. A., Bonnin, A., Huang, J. X., Gousset, L., Wu, J., Gut, J., Doyle, P., Dubremetz, J. F., Ward, H. and Petersen, C. (1998). A novel multi-domain mucin-like glycoprotein of Cryptosporidium parvum mediates invasion. Molecular and Biochemical Parasitology 96, 93–110. doi: 10.1016/S0166-6851(98)00119-4.Google Scholar
Barta, J. R. and Thompson, R. C. A. (2006). What is Cryptosporidium? Reappraising its biology and phylogenetic affinities. Trends in Parasitology 22, 463–468. doi: 10.1016/j.pt.2006.08.001.Google Scholar
Baum, J., Papenfuss, A. T., Baum, B., Speed, T. P. and Cowman, A. F. (2006). Regulation of apicomplexan actin-based motility. Nature Reviews. Microbiology 4, 621–628. doi: 10.1038/nrmicro1465.Google Scholar
Baum, J., Gilberger, T.-W., Frischknecht, F. and Meissner, M. (2008). Host-cell invasion by malaria parasites: insights from Plasmodium and Toxoplasma . Trends in Parasitology 24, 557–563. doi: 10.1016/j.pt.2008.08.006.Google Scholar
Belli, S. I., Witcombe, D., Wallach, M. G. and Smith, N. C. (2002). Functional genomics of gam56: characterisation of the role of a 56 kilodalton sexual stage antigen in oocyst wall formation in Eimeria maxima . International Journal for Parasitology 32, 1727–1737.Google Scholar
Beyer, T. (2002). Parasitophorous vacuole: morphofunctional diversity in different Coccidian genera (a short insight into the problem). Cell Biology International 26, 861–871. doi: 10.1006/cbir.2002.0943.Google Scholar
Bhalchandra, S., Ludington, J., Coppens, I. and Ward, H. D. (2013). Identification and characterization of Cryptosporidium parvum Clec, a novel C-type lectin domain-containing mucin-like glycoprotein. Infection and Immunity 81, 3356–3365. doi: 10.1128/IAI.00436-13.Google Scholar
Bhat, N., Joe, A., PereiraPerrin, M. and Ward, H. D. (2007). Cryptosporidium p30, a galactose/N-acetylgalactosamine-specific lectin, mediates infection in vitro . Journal of Biological Chemistry 282, 34877–34887. doi: 10.1074/jbc.M706950200.Google Scholar
Billker, O., Lourido, S. and Sibley, L. D. (2009). Calcium-dependent signaling and kinases in apicomplexan parasites. Cell Host & Microbe 5, 612–622. doi: 10.1016/j.chom.2009.05.017.Google Scholar
Bonafonte, M. T., Smith, L. M. and Mead, J. R. (2000). A 23-kDa recombinant antigen of Cryptosporidium parvum induces a cellular immune response on in vitro stimulated spleen and mesenteric lymph node cells from infected mice. Experimental Parasitology 96, 32–41. doi: 10.1006/expr.2000.4545.CrossRefGoogle ScholarPubMed
Bonhomme, A., Bouchot, A., Pezzella, N., Gomez, J., Le Moal, H. and Pinon, J. M. (1999). Signaling during the invasion of host cells by Toxoplasma gondii . FEMS Microbiology Reviews 23, 551–561.CrossRefGoogle ScholarPubMed
Bonnin, A., Lapillonne, A., Petrella, T., Lopez, J., Chaponnier, C., Gabbiani, G., Robine, S. and Dubremetz, J. F. (1999). Immunodetection of the microvillous cytoskeleton molecules villin and ezrin in the parasitophorous vacuole wall of Cryptosporidium parvum (Protozoa: Apicomplexa). European Journal of Cell Biology 78, 794–801.Google Scholar
Bouzid, M., Tyler, K. M., Christen, R., Chalmers, R. M., Elwin, K. and Hunter, P. R. (2010). Multi-locus analysis of human infective Cryptosporidium species and subtypes using ten novel genetic loci. BMC Microbiology 10, 213. doi: 10.1186/1471-2180-10-213.CrossRefGoogle ScholarPubMed
Bouzid, M., Hunter, P. R., Chalmers, R. M. and Tyler, K. M. (2013 a). Cryptosporidium pathogenicity and virulence. Clinical Microbiology Reviews 26, 115–134. doi: 10.1128/CMR.00076-12.Google Scholar
Bouzid, M., Hunter, P. R., McDonald, V., Elwin, K., Chalmers, R. M. and Tyler, K. M. (2013 b). A new heterogeneous family of telomerically encoded Cryptosporidium proteins. Evolutionary Applications 6, 207–217. doi: 10.1111/j.1752-4571.2012.00277.x.CrossRefGoogle ScholarPubMed
Bushkin, G. G., Motari, E., Carpentieri, A., Dubey, J. P., Costello, C. E., Robbins, P. W. and Samuelson, J. (2013). Evidence for a structural role for acid-fast lipids in oocyst walls of Cryptosporidium, Toxoplasma, and Eimeria . mBio 4, e00387–e00313. doi: 10.1128/mBio.00387-13.Google Scholar
Cai, X., Herschap, D. and Zhu, G. (2005). Functional characterization of an evolutionarily distinct phosphopantetheinyl transferase in the apicomplexan Cryptosporidium parvum . Eukaryotic Cell 4, 1211–1220. doi: 10.1128/EC.4.7.1211-1220.2005.Google Scholar
Camero, L., Shulaw, W. P. and Xiao, L. (2003). Characterization of a Cryptosporidium parvum gene encoding a protein with homology to long chain fatty acid synthetase. Journal of Eukaryotic Microbiology 50 (Suppl.), 534–538.Google Scholar
Carreno, R. A., Martin, D. S. and Barta, J. R. (1999). Cryptosporidium is more closely related to the gregarines than to coccidia as shown by phylogenetic analysis of apicomplexan parasites inferred using small-subunit ribosomal RNA gene sequences. Parasitology Research 85, 899–904. doi: 10.1007/s004360050655.Google Scholar
Carryn, S., Schaefer, D. A., Imboden, M., Homan, E. J., Bremel, R. D. and Riggs, M. W. (2012). Phospholipases and cationic peptides inhibit Cryptosporidium parvum sporozoite infectivity by parasiticidal and non-parasiticidal mechanisms. Journal of Parasitology 98, 199–204. doi: 10.1645/GE-2822.1.Google Scholar
Cevallos, A. M., Zhang, X., Waldor, M. K., Jaison, S., Zhou, X., Tzipori, S., Neutra, M. R. and Ward, H. D. (2000 a). Molecular cloning and expression of a gene encoding Cryptosporidium parvum glycoproteins gp40 and gp15. Infection and Immunity 68, 4108–4116.Google Scholar
Cevallos, A. M., Bhat, N., Verdon, R., Hamer, D. H., Stein, B., Tzipori, S., Pereira, M. E. A., Keusch, G. T. and Ward, H. D. (2000 b). Mediation of Cryptosporidium parvum infection in vitro by mucin-like glycoproteins defined by a neutralizing monoclonal antibody. Infection and Immunity 68, 5167–5175. doi: 10.1128/IAI.68.9.5167-5175.2000.Google Scholar
Chandramohanadas, R., Davis, P. H., Beiting, D. P., Harbut, M. B., Darling, C., Velmourougane, G., Lee, M. Y., Greer, P. A., Roos, D. S. and Greenbaum, D. C. (2009). Apicomplexan parasites co-opt host calpains to facilitate their escape from infected cells. Science 324, 794–797. doi: 10.1126/science.1171085.Google Scholar
Chatterjee, A., Banerjee, S., Steffen, M., O'Connor, R. M., Ward, H. D., Robbins, P. W. and Samuelson, J. (2010). Evidence for mucin-like glycoproteins that tether sporozoites of Cryptosporidium parvum to the inner surface of the oocyst wall. Eukaryotic Cell 9, 84–96. doi: 10.1128/EC.00288-09.Google Scholar
Chen, X. M. and LaRusso, N. F. (2000). Mechanisms of attachment and internalization of Cryptosporidium parvum to biliary and intestinal epithelial cells. Gastroenterology 118, 368–379.Google Scholar
Chen, X. M., Levine, S. A., Tietz, P., Krueger, E., McNiven, M. A., Jefferson, D. M., Mahle, M. and LaRusso, N. F. (1998). Cryptosporidium parvum is cytopathic for cultured human biliary epithelia via an apoptotic mechanism. Hepatology 28, 906–913. doi: 10.1002/hep.510280402.Google Scholar
Chen, X. M., Gores, G. J., Paya, C. V and LaRusso, N. F. (1999). Cryptosporidium parvum induces apoptosis in biliary epithelia by a Fas/Fas ligand-dependent mechanism. American Journal of Physiology 277, G599–G608.Google Scholar
Chen, X.-M., Huang, B. Q., Splinter, P. L., Cao, H., Zhu, G., McNiven, M. A. and LaRusso, N. F. (2003). Cryptosporidium parvum invasion of biliary epithelia requires host cell tyrosine phosphorylation of cortactin via c-Src. Gastroenterology 125, 216–228. doi: 10.1016/S0016-5085(03)00662-0.Google Scholar
Chen, X.-M., Huang, B. Q., Splinter, P. L., Orth, J. D., Billadeau, D. D., McNiven, M. A. and LaRusso, N. F. (2004 a). Cdc42 and the actin-related protein/neural Wiskott-Aldrich syndrome protein network mediate cellular invasion by Cryptosporidium parvum . Infection and Immunity 72, 3011–3021. doi: 10.1128/IAI.72.5.3011-3021.2004.Google Scholar
Chen, X.-M., Splinter, P. L., Tietz, P. S., Huang, B. Q., Billadeau, D. D. and LaRusso, N. F. (2004 b). Phosphatidylinositol 3-kinase and frabin mediate Cryptosporidium parvum cellular invasion via activation of Cdc42. Journal of Biological Chemistry 279, 31671–31678. doi: 10.1074/jbc.M401592200.Google Scholar
Chen, X., O'Hara, S. P., Huang, B. Q., Nelson, J. B., Lin, J. J., Zhu, G., Ward, H. D. and LaRusso, N. F. (2004 c). Apical organelle discharge by Cryptosporidium parvum is temperature, cytoskeleton, and intracellular calcium dependent and required for host cell invasion. Infection and Immunity 72, 6806–6816. doi: 10.1128/IAI.72.12.6806-6816.2004.Google Scholar
Chen, X.-M., O'Hara, S. P., Huang, B. Q., Splinter, P. L., Nelson, J. B. and LaRusso, N. F. (2005). Localized glucose and water influx facilitates Cryptosporidium parvum cellular invasion by means of modulation of host-cell membrane protrusion. Proceedings of the National Academy of Sciences USA 102, 6338–6343. doi: 10.1073/pnas.0408563102.Google Scholar
Cook, W. J., Senkovich, O., Aleem, K. and Chattopadhyay, D. (2012). Crystal structure of Cryptosporidium parvum pyruvate kinase. PloS One 7, e46875. doi: 10.1371/journal.pone.0046875.Google Scholar
Ctrnáctá, V., Stejskal, F., Keithly, J. S. and Hrdý, I. (2007). Characterization of S-adenosylhomocysteine hydrolase from Cryptosporidium parvum . FEMS Microbiology Letters 273, 87–95. doi: 10.1111/j.1574-6968.2007.00795.x.Google Scholar
Deng, M., Templeton, T. J., London, N. R., Bauer, C., Schroeder, A. A. and Abrahamsen, M. S. (2002). Cryptosporidium parvum genes containing thrombospondin type 1 domains. Infection and Immunity 70, 6987–6995.Google Scholar
Doan, L. T., Martucci, W. E., Vargo, M. A., Atreya, C. E. and Anderson, K. S. (2007). Nonconserved residues Ala287 and Ser290 of the Cryptosporidium hominis thymidylate synthase domain facilitate its rapid rate of catalysis. Biochemistry 46, 8379–8391. doi: 10.1021/bi700531r.Google Scholar
Ehrenman, K., Wanyiri, J. W., Bhat, N., Ward, H. D. and Coppens, I. (2013). Cryptosporidium parvum scavenges LDL-derived cholesterol and micellar cholesterol internalized into enterocytes. Cellular Microbiology 15, 1182–1197. doi: 10.1111/cmi.12107.Google Scholar
Enriquez, F. J. and Riggs, M. W. (1998). Role of immunoglobulin A monoclonal antibodies against P23 in controlling murine Cryptosporidium parvum infection. Infection and Immunity 66, 4469–4473.Google Scholar
Fayer, R. and Leek, R. G. (1984). The effects of reducing conditions, medium, pH, temperature, and time on in vitro excystation of Cryptosporidium . Journal of Protozoology 31, 567–569.Google Scholar
Fayer, R. and Xiao, L. (ed.) (2008). Cryptosporidium and Cryptosporidiosis, 2nd Edn. (ed. Fayer, R. and Xiao, L.). CRC Press, New York, NY, USA.Google Scholar
Forney, J. R., Yang, S., Du, C. and Healey, M. C. (1996 a). Efficacy of serine protease inhibitors against Cryptosporidium parvum infection in a bovine fallopian tube epithelial cell culture system. Journal of Parasitology 82, 638–640.Google Scholar
Forney, J. R., Yang, S. and Healey, M. C. (1996 b). Protease activity associated with excystation of Cryptosporidium parvum oocysts. Journal of Parasitology 82, 889–892.CrossRefGoogle ScholarPubMed
Forney, J. R., DeWald, D. B., Yang, S., Speer, C. A. and Healey, M. C. (1999). A role for host phosphoinositide 3-kinase and cytoskeletal remodeling during Cryptosporidium parvum infection. Infection and Immunity 67, 844–852.Google Scholar
Foster, D. M., Stauffer, S. H., Stone, M. R. and Gookin, J. L. (2012). Proteasome inhibition of pathologic shedding of enterocytes to defend barrier function requires X-linked inhibitor of apoptosis protein and nuclear factor κB. Gastroenterology 143, 133–144.e4. doi: 10.1053/j.gastro.2012.03.030.Google Scholar
Franco, S. J. and Huttenlocher, A. (2005). Regulating cell migration: calpains make the cut. Journal of Cell Science 118, 3829–3838. doi: 10.1242/jcs.02562.CrossRefGoogle ScholarPubMed
Fritzler, J. M. and Zhu, G. (2007). Functional characterization of the acyl-[acyl carrier protein] ligase in the Cryptosporidium parvum giant polyketide synthase. International Journal for Parasitology 37, 307–316. doi: 10.1016/j.ijpara.2006.10.014.Google Scholar
Fritzler, J. M., Millership, J. J. and Zhu, G. (2007). Cryptosporidium parvum long-chain fatty acid elongase. Eukaryotic Cell 6, 2018–2028. doi: 10.1128/EC.00210-07.Google Scholar
Galazka, J., Striepen, B. and Ullman, B. (2006). Adenosine kinase from Cryptosporidium parvum . Molecular and Biochemical Parasitology 149, 223–230. doi: 10.1016/j.molbiopara.2006.06.001.Google Scholar
Gardner, M. J., Bishop, R., Shah, T., de Villiers, E. P., Carlton, J. M., Hall, N., Ren, Q., Paulsen, I. T., Pain, A., Berriman, M., Wilson, R. J. M., Sato, S., Ralph, S. A., Mann, D. J., Xiong, Z., Shallom, S. J., Weidman, J., Jiang, L., Lynn, J., Weaver, B., Shoaibi, A., Domingo, A. R., Wasawo, D., Crabtree, J., Wortman, J. R., Haas, B., Angiuoli, S. V., Creasy, T. H., Lu, C., Suh, B., Silva, J. C., Utterback, T. R., Feldblyum, T. V., Pertea, M., Allen, J., Nierman, W. C., Taracha, E. L. N., Salzberg, S. L., White, O. R., Fitzhugh, H. A., Morzaria, S., Venter, J. C., Fraser, C. M. and Nene, V. (2005). Genome sequence of Theileria parva, a bovine pathogen that transforms lymphocytes. Science (New York, NY) 309, 134–137. doi: 10.1126/science.1110439.Google Scholar
Geriletu, , Xu, R., Jia, H., Terkawi, M. A., Xuan, X. and Zhang, H. (2011). Immunogenicity of orally administrated recombinant Lactobacillus casei Zhang expressing Cryptosporidium parvum surface adhesion protein P23 in mice. Current Microbiology 62, 1573–1580. doi: 10.1007/s00284-011-9894-4.Google Scholar
Gong, A.-Y., Zhou, R., Hu, G., Liu, J., Sosnowska, D., Drescher, K. M., Dong, H. and Chen, X.-M. (2010). Cryptosporidium parvum induces B7-H1 expression in cholangiocytes by down-regulating microRNA-513. Journal of Infectious Diseases 201, 160–169. doi: 10.1086/648589.Google Scholar
Grüner, A. C., Snounou, G., Fuller, K., Jarra, W., Rénia, L. and Preiser, P. R. (2004). The Py235 proteins: glimpses into the versatility of a malaria multigene family. Microbes and Infection 6, 864–873. doi: 10.1016/j.micinf.2004.04.004.Google Scholar
Hashim, A., Mulcahy, G., Bourke, B. and Clyne, M. (2006). Interaction of Cryptosporidium hominis and Cryptosporidium parvum with primary human and bovine intestinal cells. Infection and Immunity 74, 99–107. doi: 10.1128/IAI.74.1.99-107.2006.Google Scholar
Heiges, M., Wang, H., Robinson, E., Aurrecoechea, C., Gao, X., Kaluskar, N., Rhodes, P., Wang, S., He, C.-Z., Su, Y., Miller, J., Kraemer, E. and Kissinger, J. C. (2006). CryptoDB: a Cryptosporidium bioinformatics resource update. Nucleic Acids Research 34, D419–D422. doi: 10.1093/nar/gkj078.Google Scholar
Huang, J., Mullapudi, N., Lancto, C. A., Scott, M., Abrahamsen, M. S. and Kissinger, J. C. (2004 a). Phylogenomic evidence supports past endosymbiosis, intracellular and horizontal gene transfer in Cryptosporidium parvum . Genome Biology 5, R88. doi: 10.1186/gb-2004-5-11-r88.Google Scholar
Huang, B. Q., Chen, X.-M. and LaRusso, N. F. (2004 b). Cryptosporidium parvum attachment to and internalization by human biliary epithelia in vitro: a morphologic study. Journal of Parasitology 90, 212–221.Google Scholar
Jakobi, V. and Petry, F. (2006). Differential expression of Cryptosporidium parvum genes encoding sporozoite surface antigens in infected HCT-8 host cells. Microbes and Infection 8, 2186–2194. doi: 10.1016/j.micinf.2006.04.012.Google Scholar
Jenkins, M. C., Fayer, R., Tilley, M. and Upton, S. J. (1993). Cloning and expression of a cDNA encoding epitopes shared by 15- and 60-kilodalton proteins of Cryptosporidium parvum sporozoites. Infection and Immunity 61, 2377–2382.Google Scholar
Jenkins, M. C., O'Brien, C., Miska, K., Schwarz, R. S., Karns, J., Santin, M. and Fayer, R. (2011). Gene expression during excystation of Cryptosporidium parvum oocysts. Parasitology Research 109, 509–513. doi: 10.1007/s00436-011-2308-5.Google Scholar
Joe, A., Hamer, D. H., Kelley, M. A., Pereira, M. E., Keusch, G. T., Tzipori, S. and Ward, H. D. (1994). Role of a Gal/GalNAc-specific sporozoite surface lectin in Cryptosporidium parvum-host cell interaction. Journal of Eukaryotic Microbiology 41, 44S.Google Scholar
Joe, A., Verdon, R., Tzipori, S., Keusch, G. T. and Ward, H. D. (1998). Attachment of Cryptosporidium parvum sporozoites to human intestinal epithelial cells. Infection and Immunity 66, 3429–3432.Google Scholar
Kafsack, B. F. C., Pena, J. D. O., Coppens, I., Ravindran, S., Boothroyd, J. C. and Carruthers, V. B. (2009). Rapid membrane disruption by a perforin-like protein facilitates parasite exit from host cells. Science 323, 530–533. doi: 10.1126/science.1165740.Google Scholar
Kang, J.-M., Ju, H.-L., Yu, J.-R., Sohn, W.-M. and Na, B.-K. (2012). Cryptostatin, a chagasin-family cysteine protease inhibitor of Cryptosporidium parvum . Parasitology 139, 1029–1037. doi: 10.1017/S0031182012000297.Google Scholar
Keithly, J. S., Zhu, G., Upton, S. J., Woods, K. M., Martinez, M. P. and Yarlett, N. (1997). Polyamine biosynthesis in Cryptosporidium parvum and its implications for chemotherapy. Molecular and Biochemical Parasitology 88, 35–42.Google Scholar
King, B. J., Keegan, A. R., Phillips, R., Fanok, S. and Monis, P. T. (2012). Dissection of the hierarchy and synergism of the bile derived signal on Cryptosporidium parvum excystation and infectivity. Parasitology 139, 1533–1546. doi: 10.1017/S0031182012000984.CrossRefGoogle ScholarPubMed
Lamkanfi, M. and Dixit, V. M. (2010). Manipulation of host cell death pathways during microbial infections. Cell Host & Microbe 8, 44–54. doi: 10.1016/j.chom.2010.06.007.Google Scholar
Langer, R. C. and Riggs, M. W. (1999). Cryptosporidium parvum apical complex glycoprotein CSL contains a sporozoite ligand for intestinal epithelial cells. Infection and Immunity 67, 5282–5291.Google Scholar
Langer, R. C., Schaefer, D. A. and Riggs, M. W. (2001). Characterization of an intestinal epithelial cell receptor recognized by the Cryptosporidium parvum sporozoite ligand CSL. Infection and Immunity 69, 1661–1670. doi: 10.1128/IAI.69.3.1661-1670.2001.CrossRefGoogle ScholarPubMed
Lebart, M.-C. and Benyamin, Y. (2006). Calpain involvement in the remodeling of cytoskeletal anchorage complexes. FEBS Journal 273, 3415–3426. doi: 10.1111/j.1742-4658.2006.05350.x.Google Scholar
Li, W., Zhang, N., Liang, X., Li, J., Gong, P., Yu, X., Ma, G., Ryan, U. M. and Zhang, X. (2009). Transient transfection of Cryptosporidium parvum using green fluorescent protein (GFP) as a marker. Molecular and Biochemical Parasitology 168, 143–148. doi: 10.1016/j.molbiopara.2009.07.003.Google Scholar
Lidell, M. E., Moncada, D. M., Chadee, K. and Hansson, G. C. (2006). Entamoeba histolytica cysteine proteases cleave the MUC2 mucin in its C-terminal domain and dissolve the protective colonic mucus gel. Proceedings of the National Academy of Sciences USA 103, 9298–9303. doi: 10.1073/pnas.0600623103.Google Scholar
Lourido, S., Shuman, J., Zhang, C., Shokat, K. M., Hui, R. and Sibley, L. D. (2010). Calcium-dependent protein kinase 1 is an essential regulator of exocytosis in Toxoplasma . Nature 465, 359–362. doi: 10.1038/nature09022.Google Scholar
Lüder, C. G., Gross, U. and Lopes, M. F. (2001). Intracellular protozoan parasites and apoptosis: diverse strategies to modulate parasite-host interactions. Trends in Parasitology 17, 480–486.Google Scholar
Martin, K. H., Slack, J. K., Boerner, S. A., Martin, C. C. and Parsons, J. T. (2002). Integrin connections map: to infinity and beyond. Science (New York, NY) 296, 1652–1653. doi: 10.1126/science.296.5573.1652.CrossRefGoogle ScholarPubMed
Martucci, W. E., Vargo, M. A. and Anderson, K. S. (2008). Explaining an unusually fast parasitic enzyme: folate tail-binding residues dictate substrate positioning and catalysis in Cryptosporidium hominis thymidylate synthase. Biochemistry 47, 8902–8911. doi: 10.1021/bi800466z.Google Scholar
Matsubayashi, M., Teramoto-Kimata, I., Uni, S., Lillehoj, H. S., Matsuda, H., Furuya, M., Tani, H. and Sasai, K. (2013). Elongation factor-1α is a novel protein associated with host cell invasion and a potential protective antigen of Cryptosporidium parvum . Journal of Biological Chemistry 288, 34111–34120. doi: 10.1074/jbc.M113.515544.Google Scholar
Mauzy, M. J., Enomoto, S., Lancto, C. A., Abrahamsen, M. S. and Rutherford, M. S. (2012). The Cryptosporidium parvum transcriptome during in vitro development. PloS One 7, e31715. doi: 10.1371/journal.pone.0031715.Google Scholar
McCole, D. F., Eckmann, L., Laurent, F. and Kagnoff, M. F. (2000). Intestinal epithelial cell apoptosis following Cryptosporidium parvum infection. Infection and Immunity 68, 1710–1713. doi: 10.1128/IAI.68.3.1710-1713.2000. Google Scholar
Moncada, D., Keller, K. and Chadee, K. (2003). Entamoeba histolytica cysteine proteinases disrupt the polymeric structure of colonic mucin and alter its protective function. Infection and Immunity 71, 838–844.Google Scholar
Morada, M., Pendyala, L., Wu, G., Merali, S. and Yarlett, N. (2013). Cryptosporidium parvum induces an endoplasmic stress response in the intestinal adenocarcinoma HCT-8 cell line. Journal of Biological Chemistry 288, 30356–30364. doi: 10.1074/jbc.M113.459735.Google Scholar
Morahan, B. J., Wang, L. and Coppel, R. L. (2009). No TRAP, no invasion. Trends in Parasitology 25, 77–84. doi: 10.1016/j.pt.2008.11.004.Google Scholar
Moreno, S. N. J. and Docampo, R. (2003). Calcium regulation in protozoan parasites. Current Opinion in Microbiology 6, 359–364. doi: 10.1016/S1369-5274(03)00091-2.Google Scholar
Murphy, R. C., Ojo, K. K., Larson, E. T., Castellanos-Gonzalez, A., Perera, B. G. K., Keyloun, K. R., Kim, J. E., Bhandari, J. G., Muller, N. R., Verlinde, C. L. M. J., White, A. C., Merritt, E. A., Van Voorhis, W. C. and Maly, D. J. (2010). Discovery of potent and selective inhibitors of calcium-dependent protein kinase 1 (CDPK1) from C. parvum and T. gondii . ACS Medicinal Chemistry Letters 1, 331–335. doi: 10.1021/ml100096t.Google Scholar
Na, B.-K., Kang, J.-M., Cheun, H.-I., Cho, S.-H., Moon, S.-U., Kim, T.-S. and Sohn, W.-M. (2009). Cryptopain-1, a cysteine protease of Cryptosporidium parvum, does not require the pro-domain for folding. Parasitology 136, 149–157. doi: 10.1017/S0031182008005350.Google Scholar
Naitza, S., Spano, F., Robson, K. J. and Crisanti, A. (1998). The thrombospondin-related protein family of apicomplexan parasites: the gears of the cell invasion machinery. Parasitology Today 14, 479–484.CrossRefGoogle ScholarPubMed
Ndao, M., Nath-Chowdhury, M., Sajid, M., Marcus, V., Mashiyama, S. T., Sakanari, J., Chow, E., Mackey, Z., Land, K. M., Jacobson, M. P., Kalyanaraman, C., McKerrow, J. H., Arrowood, M. J. and Caffrey, C. R. (2013). A cysteine protease inhibitor rescues mice from a lethal Cryptosporidium parvum infection. Antimicrobial Agents and Chemotherapy 57, 6063–6073. doi: 10.1128/AAC.00734-13.Google Scholar
Nelson, J. B., O'Hara, S. P., Small, A. J., Tietz, P. S., Choudhury, A. K., Pagano, R. E., Chen, X. and LaRusso, N. F. (2006). Cryptosporidium parvum infects human cholangiocytes via sphingolipid-enriched membrane microdomains. Cellular Microbiology 8, 1932–1945. doi: 10.1111/j.1462-5822.2006.00759.x.Google Scholar
Nesterenko, M. V., Woods, K. and Upton, S. J. (1999). Receptor/ligand interactions between Cryptosporidium parvum and the surface of the host cell. Biochimica et Biophysica Acta 1454, 165–173.Google Scholar
O'Connor, R. M., Kim, K., Khan, F. and Ward, H. D. (2003). Expression of Cpgp40/15 in Toxoplasma gondii: a surrogate system for the study of Cryptosporidium glycoprotein antigens. Infection and Immunity 71, 6027–6034.Google Scholar
O'Connor, R. M., Wanyiri, J. W., Wojczyk, B. S., Kim, K. and Ward, H. (2007 a). Stable expression of Cryptosporidium parvum glycoprotein gp40/15 in Toxoplasma gondii . Molecular and Biochemical Parasitology 152, 149–158. doi: 10.1016/j.molbiopara.2007.01.003.Google Scholar
O'Connor, R. M., Wanyiri, J. W., Cevallos, A. M., Priest, J. W. and Ward, H. D. (2007 b). Cryptosporidium parvum glycoprotein gp40 localizes to the sporozoite surface by association with gp15. Molecular and Biochemical Parasitology 156, 80–83. doi: 10.1016/j.molbiopara.2007.07.010.Google Scholar
O'Connor, R. M., Burns, P. B., Ha-Ngoc, T., Scarpato, K., Khan, W., Kang, G. and Ward, H. (2009). Polymorphic mucin antigens CpMuc4 and CpMuc5 are integral to Cryptosporidium parvum infection in vitro . Eukaryotic Cell 8, 461–469. doi: 10.1128/EC.00305-08.Google Scholar
O'Hara, S. P., Yu, J.-R. and Lin, J. J.-C. (2004). A novel Cryptosporidium parvum antigen, CP2, preferentially associates with membranous structures. Parasitology Research 92, 317–327. doi: 10.1007/s00436-003-1057-5.Google Scholar
O'Hara, S. P., Gajdos, G. B., Trussoni, C. E., Splinter, P. L. and LaRusso, N. F. (2010). Cholangiocyte myosin IIB is required for localized aggregation of sodium glucose cotransporter 1 to sites of Cryptosporidium parvum cellular invasion and facilitates parasite internalization. Infection and Immunity 78, 2927–2936. doi: 10.1128/IAI.00077-10.Google Scholar
Oberstaller, J., Joseph, S. J. and Kissinger, J. C. (2013). Genome-wide upstream motif analysis of Cryptosporidium parvum genes clustered by expression profile. BMC Genomics 14, 516. doi: 10.1186/1471-2164-14-516.Google Scholar
Ojcius, D. M., Perfettini, J. L., Bonnin, A. and Laurent, F. (1999). Caspase-dependent apoptosis during infection with Cryptosporidium parvum . Microbes and Infection 1, 1163–1168.Google Scholar
Okhuysen, P. C., Chappell, C. L., Kettner, C. and Sterling, C. R. (1996). Cryptosporidium parvum metalloaminopeptidase inhibitors prevent in vitro excystation. Antimicrobial Agents and Chemotherapy 40, 2781–2784.Google Scholar
Okhuysen, P. C., Rogers, G. A., Crisanti, A., Spano, F., Huang, D. B., Chappell, C. L. and Tzipori, S. (2004). Antibody response of healthy adults to recombinant thrombospondin-related adhesive protein of Cryptosporidium 1 after experimental exposure to Cryptosporidium oocysts. Clinical and Diagnostic Laboratory Immunology 11, 235–238. doi: 10.1128/CDLI.11.2.235-238.2004.Google Scholar
Padda, R. S., Tsai, A., Chappell, C. L. and Okhuysen, P. C. (2002). Molecular cloning and analysis of the Cryptosporidium parvum aminopeptidase N gene. International Journal for Parasitology 32, 187–197.Google Scholar
Perez-Cordon, G., Nie, W., Schmidt, D., Tzipori, S. and Feng, H. (2011). Involvement of host calpain in the invasion of Cryptosporidium parvum . Microbes and Infection/Institut Pasteur 13, 103–107. doi: 10.1016/j.micinf.2010.10.007.Google Scholar
Perkins, M. E. (1999). CpABC, a Cryptosporidium parvum ATP-binding cassette protein at the host-parasite boundary in intracellular stages. Proceedings of the National Academy of Sciences USA 96, 5734–5739. doi: 10.1073/pnas.96.10.5734.Google Scholar
Perryman, L. E., Riggs, M. W., Mason, P. H. and Fayer, R. (1990). Kinetics of Cryptosporidium parvum sporozoite neutralization by monoclonal antibodies, immune bovine serum, and immune bovine colostrum. Infection and Immunity 58, 257–259.Google Scholar
Perryman, L. E., Kapil, S. J., Jones, M. L. and Hunt, E. L. (1999). Protection of calves against cryptosporidiosis with immune bovine colostrum induced by a Cryptosporidium parvum recombinant protein. Vaccine 17, 2142–2149.Google Scholar
Petersen, C., Gut, J., Doyle, P. S., Crabb, J. H., Nelson, R. G. and Leech, J. H. (1992). Characterization of a >900 000-M(r) Cryptosporidium parvum sporozoite glycoprotein recognized by protective hyperimmune bovine colostral immunoglobulin. Infection and Immunity 60, 5132–5138.Google Scholar
Pollok, R. C. G., McDonald, V., Kelly, P. and Farthing, M. J. G. (2003). The role of Cryptosporidium parvum-derived phospholipase in intestinal epithelial cell invasion. Parasitology Research 90, 181–186. doi: 10.1007/s00436-003-0831-8.Google Scholar
Puiu, D., Enomoto, S., Buck, G. A., Abrahamsen, M. S. and Kissinger, J. C. (2004). CryptoDB: the Cryptosporidium genome resource. Nucleic Acids Research 32, D329–D331. doi: 10.1093/nar/gkh050.Google Scholar
Putignani, L., Possenti, A., Cherchi, S., Pozio, E., Crisanti, A. and Spano, F. (2008). The thrombospondin-related protein CpMIC1 (CpTSP8) belongs to the repertoire of micronemal proteins of Cryptosporidium parvum . Molecular and Biochemical Parasitology 157, 98–101. doi: 10.1016/j.molbiopara.2007.09.004.Google Scholar
Reduker, D. W. and Speer, C. A. (1985). Factors influencing excystation in Cryptosporidium oocysts from cattle. Journal of Parasitology 71, 112–115.Google Scholar
Reduker, D. W., Speer, C. A. and Blixt, J. A. (1985). Ultrastructure of Cryptosporidium parvum oocysts and excysting sporozoites as revealed by high resolution scanning electron microscopy. Journal of Protozoology 32, 708–711.Google Scholar
Rider, S. D. and Zhu, G. (2010). Cryptosporidium: genomic and biochemical features. Experimental Parasitology 124, 2–9. doi: 10.1016/j.exppara.2008.12.014.Google Scholar
Riggs, M. W., McGuire, T. C., Mason, P. H. and Perryman, L. E. (1989). Neutralization-sensitive epitopes are exposed on the surface of infectious Cryptosporidium parvum sporozoites. Journal of Immunology 143, 1340–1345.Google Scholar
Riggs, M. W., Cama, V. A., Leary, H. L. and Sterling, C. R. (1994). Bovine antibody against Cryptosporidium parvum elicits a circumsporozoite precipitate-like reaction and has immunotherapeutic effect against persistent cryptosporidiosis in SCID mice. Infection and Immunity 62, 1927–1939.Google Scholar
Riggs, M. W., Schaefer, D. A., Kapil, S. J., Barley-Maloney, L., Perryman, L. E. and McNeil, M. R. (2001). Targeted disruption of CSL ligand-host cell receptor interaction in treatment of Cryptosporidium parvum infection. Journal of Eukaryotic Microbiology (Suppl.), 44S–46S.Google Scholar
Riggs, M. W., Schaefer, D. A., Kapil, S. J., Barley-Maloney, L. and Perryman, L. E. (2002). Efficacy of monoclonal antibodies against defined antigens for passive immunotherapy of chronic gastrointestinal cryptosporidiosis. Antimicrobial Agents and Chemotherapy 46, 275–282.Google Scholar
Robertson, L. J., Campbell, A. T. and Smith, H. V. (1993). In vitro excystation of Cryptosporidium parvum . Parasitology 106, 13–19.Google Scholar
Roiko, M. S. and Carruthers, V. B. (2009). New roles for perforins and proteases in apicomplexan egress. Cellular Microbiology 11, 1444–1452. doi: 10.1111/j.1462-5822.2009.01357.x.Google Scholar
Sanderson, S. J., Xia, D., Prieto, H., Yates, J., Heiges, M., Kissinger, J. C., Bromley, E., Lal, K., Sinden, R. E., Tomley, F. and Wastling, J. M. (2008). Determining the protein repertoire of Cryptosporidium parvum sporozoites. Proteomics 8, 1398–1414. doi: 10.1002/pmic.200700804.Google Scholar
Sasahara, T., Maruyama, H., Aoki, M., Kikuno, R., Sekiguchi, T., Takahashi, A., Satoh, Y., Kitasato, H., Takayama, Y. and Inoue, M. (2003). Apoptosis of intestinal crypt epithelium after Cryptosporidium parvum infection. Journal of Infection and Chemotherapy 9, 278–281. doi: 10.1007/s10156-003-0259-1.Google Scholar
Schaefer, D. A., Auerbach-Dixon, B. A. and Riggs, M. W. (2000). Characterization and formulation of multiple epitope-specific neutralizing monoclonal antibodies for passive immunization against cryptosporidiosis. Infection and Immunity 68, 2608–2616.Google Scholar
Sestak, K., Ward, L. A., Sheoran, A., Feng, X., Akiyoshi, D. E., Ward, H. D. and Tzipori, S. (2002). Variability among Cryptosporidium parvum genotype 1 and 2 immunodominant surface glycoproteins. Parasite Immunology 24, 213–219.Google Scholar
Sharman, P. A., Smith, N. C., Wallach, M. G. and Katrib, M. (2010). Chasing the golden egg: vaccination against poultry coccidiosis. Parasite Immunology 32, 590–598. doi: 10.1111/j.1365-3024.2010.01209.x.Google Scholar
Sibley, L. D. (2010). How apicomplexan parasites move in and out of cells. Current Opinion in Biotechnology 21, 592–598. doi: 10.1016/j.copbio.2010.05.009.Google Scholar
Siddiki, A. Z. (2013). Sporozoite proteome analysis of Cryptosporidium parvum by one-dimensional SDS-PAGE and liquid chromatography tandem mass spectrometry. Journal of Veterinary Science 14, 107–114. doi: 10.4142/jvs.2013.14.2.107.Google Scholar
Snelling, W. J., Lin, Q., Moore, J. E., Millar, B. C., Tosini, F., Pozio, E., Dooley, J. S. G. and Lowery, C. J. (2007). Proteomics analysis and protein expression during sporozoite excystation of Cryptosporidium parvum (Coccidia, Apicomplexa). Molecular & Cellular Proteomics 6, 346–355. doi: 10.1074/mcp.M600372-MCP200.Google Scholar
Spano, F., Puri, C., Ranucci, L., Putignani, L. and Crisanti, A. (1997). Cloning of the entire COWP gene of Cryptosporidium parvum and ultrastructural localization of the protein during sexual parasite development. Parasitology 114, 427–437.Google Scholar
Spano, F., Putignani, L., Naitza, S., Puri, C., Wright, S. and Crisanti, A. (1998). Molecular cloning and expression analysis of a Cryptosporidium parvum gene encoding a new member of the thrombospondin family. Molecular and Biochemical Parasitology 92, 147–162. doi: 10.1016/S0166-6851(97)00243-0.Google Scholar
Spielmann, T., Montagna, G. N., Hecht, L. and Matuschewski, K. (2012). Molecular make-up of the Plasmodium parasitophorous vacuolar membrane. International Journal of Medical Microbiology 302, 179–186. doi: 10.1016/j.ijmm.2012.07.011.Google Scholar
Striepen, B., Pruijssers, A. J. P., Huang, J., Li, C., Gubbels, M.-J., Umejiego, N. N., Hedstrom, L. and Kissinger, J. C. (2004). Gene transfer in the evolution of parasite nucleotide biosynthesis. Proceedings of the National Academy of Sciences USA 101, 3154–3159. doi: 10.1073/pnas.0304686101.Google Scholar
Strong, W. B. and Nelson, R. G. (2000). Preliminary profile of the Cryptosporidium parvum genome: an expressed sequence tag and genome survey sequence analysis. Molecular and Biochemical Parasitology 107, 1–32.Google Scholar
Strong, W. B., Gut, J. and Nelson, R. G. (2000). Cloning and sequence analysis of a highly polymorphic Cryptosporidium parvum gene encoding a 60-kilodalton glycoprotein and characterization of its 15- and 45-kilodalton zoite surface antigen products. Infection and Immunity 68, 4117–4134.Google Scholar
Sturbaum, G. D., Jost, B. H. and Sterling, C. R. (2003). Nucleotide changes within three Cryptosporidium parvum surface protein encoding genes differentiate genotype I from genotype II isolates. Molecular and Biochemical Parasitology 128, 87–90. doi: 10.1016/S0166-6851(03)00017-3.Google Scholar
Sturbaum, G. D., Schaefer, D. A., Jost, B. H., Sterling, C. R. and Riggs, M. W. (2008). Antigenic differences within the Cryptosporidium hominis and Cryptosporidium parvum surface proteins P23 and GP900 defined by monoclonal antibody reactivity. Molecular and Biochemical Parasitology 159, 138–141. doi: 10.1016/j.molbiopara.2008.02.009.Google Scholar
Takashima, Y., Xuan, X., Kimata, I., Iseki, M., Kodama, Y., Nagane, N., Nagasawa, H., Matsumoto, Y., Mikami, T. and Otsuka, H. (2003). Recombinant bovine herpesvirus-1 expressing p23 protein of Cryptosporidium parvum induces neutralizing antibodies in rabbits. Journal of Parasitology 89, 276–282. doi: 10.1645/0022-3395(2003)089[0276:RBHEPP]2.0.CO;2.Google Scholar
Templeton, T. J., Lancto, C. A., Vigdorovich, V., Liu, C., London, N. R., Hadsall, K. Z. and Abrahamsen, M. S. (2004 a). The Cryptosporidium oocyst wall protein is a member of a multigene family and has a homolog in Toxoplasma . Infection and Immunity 72, 980–987.Google Scholar
Templeton, T. J., Iyer, L. M., Anantharaman, V., Enomoto, S., Abrahante, J. E., Subramanian, G. M., Hoffman, S. L., Abrahamsen, M. S. and Aravind, L. (2004 b). Comparative analysis of apicomplexa and genomic diversity in eukaryotes. Genome Research 14, 1686–1695. doi: 10.1101/gr.2615304.Google Scholar
Templeton, T. J., Enomoto, S., Chen, W.-J., Huang, C.-G., Lancto, C. A., Abrahamsen, M. S. and Zhu, G. (2010). A genome-sequence survey for Ascogregarina taiwanensis supports evolutionary affiliation but metabolic diversity between a Gregarine and Cryptosporidium . Molecular Biology and Evolution 27, 235–248. doi: 10.1093/molbev/msp226.Google Scholar
Tilley, M., Upton, S. J., Fayer, R., Barta, J. R., Chrisp, C. E., Freed, P. S., Blagburn, B. L., Anderson, B. C. and Barnard, S. M. (1991). Identification of a 15-kilodalton surface glycoprotein on sporozoites of Cryptosporidium parvum . Infection and Immunity 59, 1002–1007.Google Scholar
Tosini, F., Agnoli, A., Mele, R., Gomez Morales, M. A. and Pozio, E. (2004). A new modular protein of Cryptosporidium parvum, with ricin B and LCCL domains, expressed in the sporozoite invasive stage. Molecular and Biochemical Parasitology 134, 137–147. doi: 10.1016/j.molbiopara.2003.11.014.Google Scholar
Umejiego, N. N., Li, C., Riera, T., Hedstrom, L. and Striepen, B. (2004). Cryptosporidium parvum IMP dehydrogenase: identification of functional, structural, and dynamic properties that can be exploited for drug design. Journal of Biological Chemistry 279, 40320–40327. doi: 10.1074/jbc.M407121200.Google Scholar
Valigurová, A., Jirků, M., Koudela, B., Gelnar, M., Modrý, D. and Slapeta, J. (2008). Cryptosporidia: epicellular parasites embraced by the host cell membrane. International Journal for Parasitology 38, 913–922. doi: 10.1016/j.ijpara.2007.11.003.Google Scholar
Wanyiri, J. W., O'Connor, R., Allison, G., Kim, K., Kane, A., Qiu, J., Plaut, A. G. and Ward, H. D. (2007). Proteolytic processing of the Cryptosporidium glycoprotein gp40/15 by human furin and by a parasite-derived furin-like protease activity. Infection and Immunity 75, 184–192. doi: 10.1128/IAI.00944-06.Google Scholar
Wanyiri, J. W., Techasintana, P., O'Connor, R. M., Blackman, M. J., Kim, K. and Ward, H. D. (2009). Role of CpSUB1, a subtilisin-like protease, in Cryptosporidium parvum infection in vitro . Eukaryotic Cell 8, 470–477. doi: 10.1128/EC.00306-08.Google Scholar
Wetzel, D. M., Schmidt, J., Kuhlenschmidt, M. S., Dubey, J. P. and Sibley, L. D. (2005). Gliding motility leads to active cellular invasion by Cryptosporidium parvum sporozoites. Infection and Immunity 73, 5379–5387. doi: 10.1128/IAI.73.9.5379-5387.2005.Google Scholar
Widmer, G. and Lee, Y. (2010). Comparison of single- and multilocus genetic diversity in the protozoan parasites Cryptosporidium parvum and C. hominis . Applied and Environmental Microbiology 76, 6639–6644. doi: 10.1128/AEM.01268-10.Google Scholar
Widmer, G., Lee, Y., Hunt, P., Martinelli, A., Tolkoff, M. and Bodi, K. (2012). Comparative genome analysis of two Cryptosporidium parvum isolates with different host range. Infection, Genetics and Evolution 12, 1213–1221. doi: 10.1016/j.meegid.2012.03.027.Google Scholar
Wyatt, C. R. and Perryman, L. E. (2000). Detection of mucosally delivered antibody to Cryptosporidium parvum p23 in infected calves. Annals of the New York Academy of Sciences 916, 378–387.Google Scholar
Wyatt, C. R., Brackett, E. J., Mason, P. H., Savidge, J. and Perryman, L. E. (2000). Excretion patterns of mucosally delivered antibodies to p23 in Cryptosporidium parvum infected calves. Veterinary Immunology and Immunopathology 76, 309–317.Google Scholar
Xiao, D., Yin, C., Zhang, Q., Li, J., Gong, P., Li, S., Zhang, G., Gao, Y. and Zhang, X. (2011). Selection and identification of a new adhesion protein of Cryptosporidium parvum from a cDNA library by ribosome display. Experimental Parasitology 129, 183–189. doi: 10.1016/j.exppara.2011.06.004.Google Scholar
Xu, P., Widmer, G., Wang, Y., Ozaki, L. S., Alves, J. M., Serrano, M. G., Puiu, D., Manque, P., Akiyoshi, D., Mackey, A. J., Pearson, W. R., Dear, P. H., Bankier, A. T., Peterson, D. L., Abrahamsen, M. S., Kapur, V., Tzipori, S. and Buck, G. A. (2004). The genome of Cryptosporidium hominis . Nature 431, 1107–1112. doi: 10.1038/nature02977.Google Scholar
Yamagishi, J., Wakaguri, H., Sugano, S., Kawano, S., Fujisaki, K., Sugimoto, C., Watanabe, J., Suzuki, Y., Kimata, I. and Xuan, X. (2011). Construction and analysis of full-length cDNA library of Cryptosporidium parvum . Parasitology International 60, 199–202. doi: 10.1016/j.parint.2011.03.001.Google Scholar
Yao, L., Yin, J., Zhang, X., Liu, Q., Li, J., Chen, L., Zhao, Y., Gong, P. and Liu, C. (2007). Cryptosporidium parvum: identification of a new surface adhesion protein on sporozoite and oocyst by screening of a phage-display cDNA library. Experimental Parasitology 115, 333–338. doi: 10.1016/j.exppara.2006.09.018.Google Scholar
Yarlett, N., Wu, G., Waters, W. R., Harp, J. A., Wannemuehler, M. J., Morada, M., Athanasopoulos, D., Martinez, M. P., Upton, S. J., Marton, L. J. and Frydman, B. J. (2007). Cryptosporidium parvum spermidine/spermine N1-acetyltransferase exhibits different characteristics from the host enzyme. Molecular and Biochemical Parasitology 152, 170–180. doi: 10.1016/j.molbiopara.2007.01.004.Google Scholar
Yu, Q., Li, J., Zhang, X., Gong, P., Zhang, G., Li, S. and Wang, H. (2010). Induction of immune responses in mice by a DNA vaccine encoding Cryptosporidium parvum Cp12 and Cp21 and its effect against homologous oocyst challenge. Veterinary Parasitology 172, 1–7. doi: 10.1016/j.vetpar.2010.04.036.Google Scholar
Zeng, B. and Zhu, G. (2006). Two distinct oxysterol binding protein-related proteins in the parasitic protist Cryptosporidium parvum (Apicomplexa). Biochemical and Biophysical Research Communications 346, 591–599. doi: 10.1016/j.bbrc.2006.05.165.Google Scholar
Zeng, B., Cai, X. and Zhu, G. (2006). Functional characterization of a fatty acyl-CoA-binding protein (ACBP) from the apicomplexan Cryptosporidium parvum . Microbiology 152, 2355–2363. doi: 10.1099/mic.0.28944-0.Google Scholar
Zhang, H., Guo, F., Zhou, H. and Zhu, G. (2012 a). Transcriptome analysis reveals unique metabolic features in the Cryptosporidium parvum oocysts associated with environmental survival and stresses. BMC Genomics 13, 647. doi: 10.1186/1471-2164-13-647.Google Scholar
Zhang, H., Guo, F. and Zhu, G. (2012 b). Involvement of host cell integrin α2 in Cryptosporidium parvum infection. Infection and Immunity 80, 1753–1758. doi: 10.1128/IAI.05862-11.Google Scholar
Zhu, G. (2004). Current progress in the fatty acid metabolism in Cryptosporidium parvum . Journal of Eukaryotic Microbiology 51, 381–388.Google Scholar
Zhu, G. and Keithly, J. S. (1997). Molecular analysis of a P-type ATPase from Cryptosporidium parvum . Molecular and Biochemical Parasitology 90, 307–316. doi: 10.1016/S0166-6851(97)00168-0.Google Scholar
Zhu, G., LaGier, M. J., Stejskal, F., Millership, J. J., Cai, X. and Keithly, J. S. (2002). Cryptosporidium parvum: the first protist known to encode a putative polyketide synthase. Gene 298, 79–89.Google Scholar
Zhu, G., Li, Y., Cai, X., Millership, J. J., Marchewka, M. J. and Keithly, J. S. (2004). Expression and functional characterization of a giant Type I fatty acid synthase (CpFAS1) gene from Cryptosporidium parvum . Molecular and Biochemical Parasitology 134, 127–135.Google Scholar