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The truth about in vitro culture of Cryptosporidium species

Published online by Cambridge University Press:  16 November 2017

Panagiotis Karanis
Panagiotis Karanis*
Affiliation:
State Key Laboratory of Plateau Ecology and Agriculture, Centre for Biomedicine and Infectious Diseases, Qinghai Academy of Animal Science and Veterinary Medicine, Qinghai University, Xining, Qinghai, People's Republic of China Medical School, University of Cologne, Cologne, Germany
*
Author for correspondence: Panagiotis Karanis, E-mail: [email protected]
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Abstract

Cryptosporidium research has focused on the development of infection control, and effective therapy that has thus far been hampered by the inability to culture Cryptosporidium in vitro. Other limitations include inadequate animal models, cumbersome screening procedures for chemotherapeutic approaches and a lack of tools for genetic manipulation. These limitations can, however, be eased by the improvement and focused development of in vitro cultivation. The ability to culture relevant Cryptosporidium isolates in vitro and to propagate the life cycle stages that are responsible for causing disease in an infected host is still a critical link. This ability will facilitate other relevant approaches, e.g., the ability to knockout genes and the application of broader screening for drug discoveries and vaccine developments, in combination with new discoveries on the parasite's basic biology, genetic manipulation and new life cycle stages. Success in this effort represents an essential step towards significant progress in the control of cryptosporidiosis.

Keywords

Cryptosporidiumculturein vitroreview
Type
Review Article
Information
Parasitology , Volume 145 , Issue 7 , June 2018 , pp. 855 - 864
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Copyright
Copyright © Cambridge University Press 2017 

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References

Adler, S, Widerström, M, Lindh, J and Lilja, M (2017) Symptoms and risk factors of Cryptosporidium hominis infection in children: data from a large waterborne outbreak in Sweden. Parasitology Research 116, 2613–2618. doi: 10.1007/s00436-017-5558-zGoogle Scholar
Alcantara Warren, C, Destura, RV, Sevilleja, JE, Barroso, LF, Carvalho, H, Barrett, LJ, O'Brien, AD and Guerrant, RL (2008) Detection of epithelial cell injury and quantification of infection in the HCT8 organoid model of cryptosporidiosis. Journal of Infectious Diseases 198, 143–149.Google Scholar
Aldeyarbi, HM and Karanis, P (2016 a) Electron microscopic observation of the early stages of Cryptosporidium parvum and development in in vitro axenic culture. European Journal of Protistology 52, 36–44.Google Scholar
Aldeyarbi, HM and Karanis, P (2016 b) The fine structure stage development and sporogony of Cryptosporidium parvum in cell-free culture. Parasitology 143, 749–761.Google Scholar
Aldeyarbi, HM and Karanis, P (2016 c) The ultra-structural similarities between Cryptosporidium parvum and the gregarines. The Journal of Eukaryotic Microbiology 63, 79–85.Google Scholar
Arrowood, MJ (2002) In vitro cultivation of Cryptosporidium species. Clinical Microbiology Reviews 15, 390–400.Google Scholar
Baldursson, S and Karanis, P (2011) Waterborne transmission of protozoan parasites: review of worldwide outbreaks – an update 2004–2010. Water Research 45, 6603–6614.CrossRefGoogle ScholarPubMed
Barta, JR and Thompson, RCA (2006) What is Cryptosporidium? Re-appraising its biology and phylogenetic affinities. Trends in Parasitology 22, 463–468.Google Scholar
Bartfeld, S (2016) Modeling infectious diseases and host–microbe interactions in gastrointestinal organoids. Developmental Biology 420, 262–270.CrossRefGoogle ScholarPubMed
Bartfeld, S and Clevers, H (2017) Organoids as model for infectious diseases: culture of human and murine stomach organoids and microinjection of Helicobacter pylori. Journal of Visualized Experiments 105, e53359.Google Scholar
Borowski, H, Clode, PL and Thompson, RCA (2008) Active invasion and/or encapsulation? A reappraisal of host-cell parasitism by Cryptosporidium. Trends in Parasitology 24, 509–516.Google Scholar
Borowski, H, Thompson RC, A, Armstrong, T and Clode, PL (2010) Morphological characterization of Cryptosporidium parvum life-cycle stages in an in vitro model system. Parasitology 137, 13–26.CrossRefGoogle Scholar
Boxell, A, Hijjawi, N, Monis, P and Ryan, U (2008) Comparison of various staining methods for the detection of Cryptosporidium in cell-free culture. Experimental Parasitology 120, 67–72.CrossRefGoogle ScholarPubMed
Broutier, L, Andersson-Rolf, A, Hindley, CJ, Boj, SF, Clevers, H, Koo, BK and Huch, M (2016) Culture and establishment of self-renewing human and mouse adult liver and pancreas 3D organoids and their genetic manipulation. Nature Protocols 11, 1724–1743.Google Scholar
Caccio, SM and Chalmers, R (2016) Human cryptosporidiosis in Europe. Clinical Microbiology Infection 22, 471–480.Google Scholar
Castellanos-Gonzalez, A, Cabada, MM, Nichols, J, Gomez, G and White, AC (2013) Human primary intestinal epithelial cells as an improved in vitro model for Cryptosporidium parvum infection. Infection and Immunity 81, 1996–2001.Google Scholar
Cavalier-Smith, T (2014) Gregarine site-heterogeneous 18S rDNA trees, revision of gregarine higher classification, and the evolutionary diversification of Sporozoa. European Journal of Protistology 50, 472–495.Google Scholar
Checkley, W, White, AC Jr., Jaganath, D, Arrowood, MJ, Chalmers, RM, Chen, XM, Fayer, R, Griffiths, JK, Guerrant, RL, Hedstrom, L, Huston, CD, Kotloff, KL, Kang, G, Mead, JR, Miller, M, Petri, WA Jr., Priest, JW, Roos, DS, Striepen, B, Thompson, RCA, Ward, HD, Van Voorhis, WA, Xiao, L, Zhu, G and Houpt, ER (2015) A review of the global burden, novel diagnostics, therapeutics, and vaccine targets for Cryptosporidium. The Lancet Infectious Diseases 15, 85–94.CrossRefGoogle ScholarPubMed
Clode, PL, Koh, WH and Thompson, RCA (2015) Life without a host cell: what is Cryptosporidium? Trends in Parasitology 31, 614–624.Google Scholar
Current, WL and Haynes, TB (1984) Complete development of Cryptosporidium in cell cultures. Science 224, 603–605.Google Scholar
Current, WL and Reese, NC (1986) A comparison of endogenous development of three isolates of Cryptosporidium in suckling mice. Journal of Protozoology 33, 98–108.Google Scholar
Datry, A, Danis, M and Gentilini, M (1989) Development complet de cryptosporidium en culture cellulaire: applications. Med./Sci. 5, 762–766.Google Scholar
DeCicco RePass, MA, Chen, Y, Lin, Y, Zhou, W, Kaplan, DL and Ward, HD (2017) Novel bioengineered three-dimensional human intestinal model for long-term infection of Cryptosporidium parvum. Infection and Immunity 85, e00731–16.Google Scholar
Dutta, D and Clevers, H (2017) Organoid culture systems to study host–pathogen interactions. Current Opinion in Immunology 48, 15–22.Google Scholar
Dutta, D, Heo, I and Clevers, H (2017) Disease modelling in stem cellderived 3D organoid systems. Trends in Molecular Medicine 23, 393–410.Google Scholar
Efstratiou, A, Ongerth, J and Karanis, P (2017 a). Waterborne transmission of protozoan parasites: review of worldwide outbreaks – an update 2011–2016. Water Research 114, 14–22.CrossRefGoogle ScholarPubMed
Efstratiou, A, Ongerth, J and Karanis, P (2017 b). Evolution of monitoring for Giardia and Cryptosporidium in water. Water Research 123, 96–112.Google Scholar
Ettayebi, K, Crawford, SE, Murakami, K, Broughman, JR, Karandikar, U, Tenge, VR, Neill, FH, Blutt, SE, Zeng, XL, Qu, L, Kou, B, Opekun, AR, Burrin, D, Graham, DY, Ramani, S, Atmar, RL and Estes, MK (2016) Replication of human noroviruses in stem cell-derived human enteroids. Science 80;353, 1387–1393.Google Scholar
Fayer, R (2008) General biology. In Fayer, R and Xiao, L (eds). Cryptosporidium and Cryptosporidiosis. Boca Raton, London, New York: Taylor and Francis Group, CRC Press, pp. 1–7.Google Scholar
Flanigan, TP, Aji, T, Marshall, R, Soave, R, Aikawa, M and Kaetzel, C (1991) Asexual development of Cryptosporidium parvum within a differentiated human enterocyte cell line. Infection and Immunity 59, 234–239.CrossRefGoogle ScholarPubMed
GBD Diarrhoeal Diseases Collaborators (2017) Estimates of global, regional, and national morbidity, mortality, and aetiologies of diarrhoeal diseases: a systematic analysis for the Global Burden of Disease Study 2015. Lancet Infectious Diseases 17, 909–948.Google Scholar
Girouard, D, Gallant, J, Akiyoshi, DE, Nunnari, J and Tzipori, S (2006) Failure to propagate Cryptosporidium spp. in cell-free culture. Journal of Parasitology 92, 399–400.Google Scholar
Harris, JR, Adrian, M and Petry, F (2003) Structure of the Cryptosporidium parvum microneme: a metabolically and osmotically labile apicomplexan organelle. Microneme 34, 65–78.CrossRefGoogle ScholarPubMed
Hedstrom, L (2015) Cryptosporidium: a first step toward tractability. Trends in Parasitology 31, 401–402.Google Scholar
Hijjawi, N (2010) Cryptosporidium: new developments in cell culture. Experimental Parasitology 124, 54–60.Google Scholar
Hijjawi, N, Estcourt, A, Yang, R, Monis, P and Ryan, U (2010) Complete development and multiplication of Cryptosporidium hominis in cell-free culture. Veterinary Parasitology 169, 29–36.Google Scholar
Hijjawi, NS, Meloni, BP, Ng'anzoc, M, Ryan, UM, Olson, ME, Cox, PT, Monis, PT and Thompson, RCA (2004) Complete development of Cryptosporidium parvum in host cell-free culture. International Journal for Parasitology 34, 769–777.Google Scholar
Hijjawi, NS, Meloni, BP, Ryan, UM, Olson, ME and Thompson, RC (2002) Successful in vitro cultivation of Cryptosporidium andersoni: evidence for the existence of novel extracellular stages in the life cycle and implications for the classification of Cryptosporidium. International Journal for Parasitology 32, 1719–1726.Google Scholar
Karanis, P and Aldeyarbi, HM (2011) Evolution of Cryptosporidium in vitro culture. International Journal for Parasitology 12, 1231–1242.Google Scholar
Karanis, P and Ey, PL (1998) Characterization of axenic isolates of Giardia intestinalis established from humans and animals in Germany. Parasitology Research 84, 442–449.Google Scholar
Karanis, P and Schoenen, D (2001) Biological test for the detection of low concentrations of infectious Cryptosporidium parvum oocysts in water. Acta Hydrochimica Hydrobiologica 29, 242–245.3.0.CO;2-2>CrossRefGoogle Scholar
Karanis, P, Kourenti, C and Smith, H (2007) Water-borne transmission of protozoan parasites: a review of worldwide outbreaks and lessons learned. Journal of Water and Health 5, 1–38.CrossRefGoogle Scholar
Karanis, P, Kimura, A, Igarashi, I, Nagasawa, H and Suzuki, N (2008) Observations on Cryptosporidium life cycle stages during excystation. Journal for Parasitology 94, 298–300.Google Scholar
King, BJ, Hoefel, D, Lim, SP, Robinson, BS and Monis, PT (2009) Flow cytometric assessment of distinct physiological stages within Cryptosporidium parvum sporozoites post-excystation. International Journal of Parasitology 136, 953–966.Google Scholar
Koh, W, Clode, P, Monis, P and Thompson, RCA (2013) Multiplication of the waterborne pathogen Cryptosporidium parvum in an aquatic biofilm system. Parasite Vectors 6, 270.CrossRefGoogle Scholar
Koh, W, Thompson, A, Edwards, H, Monis, P and Clode, PL (2014) Extracellular excystation and development of Cryptosporidium: tracing the fate of oocysts within Pseudomonas aquatic biofilm systems. BMC Microbiology 14, 281.Google Scholar
Kotloff, K (2017) The burden and etiology of diarrheal illness in developing countries. Pediatric Clinics of North America 64, 799–814.CrossRefGoogle ScholarPubMed
Kotloff, KL, Nataro, JP, Blackwelder, WC, Nasrin, D, Farag, TH, Panchalingam, S, Wu, Y, Sow, SO, Sur, D, Breiman, RF, Faruque, AS, Zaidi, AK, Saha, D, Alonso, PL, Tamboura, B, Sanogo, D, Onwuchekwa, U, Manna, B, Ramamurthy, T, Kanungo, S, Ochieng, JB, Omore, R, Oundo, JO, Hossain, A, Das, SK, Ahmed, S, Qureshi, S, Quadri, F, Adegbola, RA, Antonio, M, Hossain, MJ, Akinsola, A, Mandomando, I, Nhampossa, T, Acacio, S, Biswas, K, O'Reilly, CE, Mintz, ED, Berkeley, LY, Muhsen, K, Sommerfelt, H, Robins Browne, RM and Levine, MM (2013) Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (The Global Enteric Multicenter Study, GEMS): a prospective, case-control study. Lancet 382, 209–222.Google Scholar
Lanternier, F, Amazzough, K, Favennec, L, Mamzer-Bruneel, MF, Abdoul, H, Tourret, J, Decramer, S, Zuber, J, Scemla, A, Legendre, C, Lortholary, O, Bougnoux, ME and ANOFEL Cryptosporidium National Network and Transplant Cryptosporidium Study Group (2017) Cryptosporidium spp. infection in solid organ transplantation: the Nationwide ‘TRANSCRYPTO’ study. Transplantation 101, 826–830.CrossRefGoogle ScholarPubMed
Leander, BS (2008) Marine gregarines: evolutionary prelude to the apicomplexan radiation? Trends in Parasitology 24, 60–67.Google Scholar
Leetz, S, Sotiriadou, S, Ongerth, J and Karanis, P (2007) An evaluation of primers amplified DNA targets for the detection of Cryptosporidium species using C. parvum HNJ-1 Japanese isolate. Parasitology Research 101, 951–962.Google Scholar
Levine, ND (1984) Taxonomy and review of the coccidian genus Cryptosporidium (Protozoa, Apicomplexa). Journal of Protozoology 31, 94–98.Google Scholar
Manjunatha, U, Vinayak, S, Zambriski, JA, Chao, AT, Sy, T, Noble, CG, Bonamy, GMC, Kondredd, RR, Zou, B, Gedeck, R, Brooks, CF, Herbert, GT, Sateriale, A, Tandel, J, Noh, S, Lakshminarayana, SB, Lim, SH, Goodman, LB, Bodenreider, C, Feng, G, Zhang, L, Blasco, F, Wagner, J, Leong, FJ, Striepen, B and Diagana, TT (2017) A Cryptosporidium PI(4)K inhibitor is a drug candidate for cryptosporidiosis. Nature. 546, 376–380. doi:10.1038/nature22337.Google Scholar
Matsubayashi, M, Ando, H, Kimata, I, Nakagawa, H, Furuya, M, Tani, H and Sasai, K (2010) Morphological changes and viability of Cryptosporidium parvum sporozoites after excystation in cell-free culture media. Parasitology 137, 1861–1866.Google Scholar
McCracken, KW, Catá, EM, Crawford, CM, Sinagoga, KL, Schumacher, M, Rockich, BE, Tsai, YH, Mayhew, CN, Spence, JR, Zavros, Y and Wells, JM (2014) Modelling human development and disease in pluripotent stem-cell-derived gastric organoids. Nature 516(7531), 400–404.Google Scholar
Meyer, EA (1976) Giardia lamblia: isolation and axenic cultivation. Experimental Parasitology 39, 101–105.Google Scholar
Morada, M, Sangun, L, Gunther-Cummins, L, Weiss, LM, Widmer, G, Tzipori, S and Yarlett, N (2016) Continuous culture of Cryptosporidium parvum using hollow fiber technology. International Journal for Parasitology 46, 21–29.Google Scholar
Perez Cordón, G, Marin, C, Romero, D, Rosales, C and Sánchez Moreno, MJ (2007) More productive in vitro culture of Cryptosporidium parvum for better study of the intra- and extracellular phases. Rosales Mem Inst Oswaldo Cruz, Rio de Janeiro 102, 567–571, 567–571.Google Scholar
Petry, F, Kneib, I and Harris, R (2009) Morphology and in vitro infectivity of sporozoites of Cryptosporidium parvum. Journal of Parasitology 95, 1243–1246.Google Scholar
Platts-Mills, JA, Babji, S, Bodhidatta, L, Gratz, J, Haque, R, Havt, A, McCormick, BJ, McGrath, M, Olortegui, MP, Samie, A, Shakoor, S, Mondal, D, Lima, IF, Hariraju, D, Rayamajhi, BB, Qureshi, S, Kabir, F, Yori, PP, Mufamadi, B, Amour, C, Carreon, JD, Richard, SA, Lang, D, Bessong, P, Mduma, E, Ahmed, T, Lima, AA, Mason, CJ, Zaidi, AK, Bhutta, ZA, Kosek, M, Guerrant, RL, Gottlieb, M, Miller, M, Kang, G and Houpt, ER (2015) MAL-ED Network investigators. pathogen-specific burdens of community diarrhoea in developing countries: a multisite birth cohort study (MAL-ED). Lancet Global Health 3, e564–e575.Google Scholar
Pompaiah, M and Bartfeld, S (2017) Gastric organoids: an emerging model system to study Helicobacter pylori pathogenesis. Current Topics in Microbiology and Immunology 400, 149–168.Google Scholar
Rosales, MJ, Cifuentes, J and Mascaró, C (1993) Cryptosporidium parvum: culture in MDCK cells. Experimental Parasitology 76, 209–212.Google Scholar
Rosales, MJ, Peréz Cordón, G, Sánchez Moreno, M, Marín Sánchez, C and Mascaró, C. (2005) Extracellular like-gregarine stages of Cryptosporidium parvum. Acta Tropica 95, 74–78.Google Scholar
Ryan, U, Paparini, A, Monis, P and Hijjawi, N (2016) It's official – Cryptosporidium is a gregarine: what are the implications for the water industry? Water Research 105, 305–313.CrossRefGoogle ScholarPubMed
Scheid, P (2017) Kryptosporidiose. Handbuch der Infektionskrankheiten, Chapter VIII –·9; ecomed Medizin.Google Scholar
Slavind, D (1995) Cryptosporidium meleagridis (sp. nov.). Journal of Comparative Pathology 65, 262–266.Google Scholar
Striepen, B (2013) Time to tackle cryptosporidiosis. Nature 503, 189–191.Google Scholar
Tetley, L, Brown, SM, McDonald, V and Coombs, GH (1998) Ultra-structural analysis of the sporozoite of Cryptosporidium parvum. Microbiology 144, 3249–3255.Google Scholar
Thompson, RCA, Koh, WH and Clode, PL (2016) Cryptosporidium – What is it? Food and Waterborne Parasitology 4, 54–61.Google Scholar
Tyzzer, EE (1907) A sporozoon found in the peptic glands of the common mouse. Proceedings of the Society for Experimental Biology and Medicine 5, 12–13.Google Scholar
Tyzzer, EE (1910) An extracellular coccidium, Cryptosporidium muris (gen. et sp. nov.), of the gastric glands of the common mouse. Journal of Medical Research 23, 487–509.Google Scholar
Tyzzer, EE (1912) Cryptosporidium parvum (sp. nov.), a coccidium found in the small intestine of the common mouse. Archiv für Protistenkunde 26, 394–412.Google Scholar
Valigurová, A., Hofmannová, L., Koudela, B and Vávra, J (2007) An ultrastructural comparison of the attachment sites between Gregarina steini and Cryptosporidium muris. Journal of Eukaryotic Microbiology 54, 495–510.Google Scholar
Varughese, EA, Bennett-Stamper, CL, Wymer, LJ and Yadav, JS (2014) A new in vitro model using small intestinal epithelial cells to enhance infection of Cryptosporidium parvum. Journal of Microbiological Methods 106, 47–54.Google Scholar
Villanueva, MT (2017) Decrypting Cryptosporidium. Nature Reviews Drug Discovery. 16, 527. Published online 31 Jul 2017. doi: 10.1038/nrd.2017.147.Google Scholar
Vinayak, S, Pawlowic, MC, Sateriale, A, Brooks, CF, Studstill, CJ, Bar-Peled, Y, Cipriano, MJ and Striepen, B (2015) Genetic modification of the diarrhoeal pathogen Cryptosporidium parvum. Nature 523, 477–480.Google Scholar
Ward, HD (2017) New tools for Cryptosporidium lead to new hope for cryptosporidiosis. Trends in Parasitology 33, 662–664.Google Scholar
Widmer, G, Klein, P and Bonilla, R (2007) Adaptation of Cryptosporidium oocysts to different excystation conditions. Parasitology 134, 1–6.Google Scholar
Woodmansee, DB (1986) An in vitro study of sporulation in Cryptosporidium species. Journal of Parasitology 72, 347–349.Google Scholar
Woods, KM and Upton, SJ (2007) In vitro development of Cryptosporidium parvum in serum-free media. Letters of Applied Microbiology 44, 520–523.Google Scholar
Zhang, L, Sheoran, AS and Widmer, G (2009) Cryptosporidium parvum DNA replication in cell-free culture. Journal of Parasitology 95, 1239–1242.Google Scholar