Cryptosporidium infection of human small intestinal epithelial cells induces type III interferon and impairs infectivity of Rotavirus

References

• Feng Y, Ryan UM, Xiao L. Genetic diversity and population structure of cryptosporidium. Trends Parasitol. 2018;34(11):997–22. doi:10.1016/j.pt.2018.07.009.
   PubMed Web of Science ®Google Scholar
• Kotloff KL, Nataro JP, Blackwelder WC, Nasrin D, Farag TH, Panchalingam S, Wu Y, Sow SO, Sur D, Breiman RF, et al. 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. 2013;382(9888):209–222. doi:10.1016/S0140-6736(13)60844-2.
   PubMed Web of Science ®Google Scholar
• Kotloff KL. The burden and etiology of diarrheal illness in developing countries. Pediatr Clin North Am. 2017;64(4):799–814. doi:10.1016/j.pcl.2017.03.006.
   PubMed Web of Science ®Google Scholar
• Checkley W, White AC, Jaganath D, Arrowood MJ, Chalmers RM, Chen X-M, Fayer R, Griffiths JK, Guerrant RL, Hedstrom L, et al. A review of the global burden, novel diagnostics, therapeutics, and vaccine targets for cryptosporidium. Lancet Infect Dis. 2015;15(1):85–94. doi:10.1016/S1473-3099(14)70772-8.
   PubMed Web of Science ®Google Scholar
• Theodos CM, Sullivan KL, Griffiths JK, Tzipori S. Profiles of healing and nonhealing Cryptosporidium parvum infection in C57BL/6 mice with functional B and T lymphocytes: the extent of gamma interferon modulation determines the outcome of infection. Infect Immun. 1997;65(11):4761–4769. doi:10.1128/iai.65.11.4761-4769.1997.
   Web of Science ®Google Scholar
• Rehg JE. Effect of Interferon- in Experimental Cryptosporidium parvum Infection. J Infect Dis. 1996;174(1):229–232. doi:10.1093/infdis/174.1.229.
   Web of Science ®Google Scholar
• Lee S, Beamer G, Tzipori S. The piglet acute diarrhea model for evaluating efficacy of treatment and control of cryptosporidiosis. Hum Vaccin Immunother. 2019;15(6):1445–1452. doi:10.1080/21645515.2018.1498436.
   PubMed Web of Science ®Google Scholar
• Dayao DA, Sheoran A, Carvalho A, Xu H, Beamer G, Widmer G, Tzipori S. An immunocompetent rat model of infection with Cryptosporidium hominis and Cryptosporidium parvum. Int J Parasitol. 2020;50(1):19–22. doi:10.1016/j.ijpara.2019.10.002.
   Web of Science ®Google Scholar
• Bhalchandra S, Lamisere H, Ward H. Intestinal organoid/enteroid-based models for Cryptosporidium. Curr Opin Microbiol. 2020;58:124–129. doi:10.1016/j.mib.2020.10.002.
   Web of Science ®Google Scholar
• VanDussen KL, Sonnek NM, Stappenbeck TS. L-WRN conditioned medium for gastrointestinal epithelial stem cell culture shows replicable batch-to-batch activity levels across multiple research teams. Stem Cell Res. 2019;37:101430. doi:10.1016/j.scr.2019.101430.
   PubMed Web of Science ®Google Scholar
• Wilke G, Funkhouser-Jones LJ, Wang Y, Ravindran S, Wang Q, Beatty WL, Baldridge MT, VanDussen KL, Shen B, Kuhlenschmidt MS, et al. A stem-cell-derived platform enables complete cryptosporidium development in vitro and genetic tractability. Cell Host & Microbe. 2019;26(1):123–134.e8. doi:10.1016/j.chom.2019.05.007.
   PubMed Web of Science ®Google Scholar
• Brunauer M, Roch F-F, Conrady B. Prevalence of worldwide neonatal calf diarrhoea caused by Bovine Rotavirus in combination with Bovine Coronavirus, Escherichia coli K99 and cryptosporidium spp.: a meta-analysis. Anim (Basel). 2021;11(4):1014. doi:10.3390/ani11041014.
   Google Scholar
• Li N, Zhao W, Song S, Ye H, Chu W, Guo Y, Feng Y, Xiao L. Diarrhoea outbreak caused by coinfections of Cryptosporidium parvum subtype IIdA20G1 and rotavirus in pre-weaned dairy calves. Transbound Emerg Dis. 2022;69(5):e1606–17. doi:10.1111/tbed.14496.
   Web of Science ®Google Scholar
• Kurenzvi L, Sebunya TK, Coetzee T, Paganotti GM, Teye MV. Prevalence of cryptosporidium parvum, giardia intestinalis and molecular characterization of group a rotavirus associated with diarrhea in children below five years old in Gaborone, Botswana. Pan Afr Med J. 2020;37:159. doi:10.11604/pamj.2020.37.159.25392.
   Web of Science ®Google Scholar
• Asada Y, Chua ML, Tsurumi M, Yamauchi T, Nyambe I, Harada H. Detection of Escherichia coli, rotavirus, and Cryptosporidium spp. From drinking water, kitchenware, and flies in a periurban community of Lusaka, Zambia. J Water Health. 2022;20(7):1027–1037. doi:10.2166/wh.2022.276.
   Web of Science ®Google Scholar
• Fujii S, Wang Y, Meng S, Musich RJ, Espenschied ST, Newhall K, Han Y, Sekiguchi S, Matsumoto R, Ciorba MA, et al. Long-term monolayer cultivation captures homeostatic and regenerative features of human colonic epithelial cells. bioRxiv. doi.10.1101/2024.01.01.573838.
   Google Scholar
• Wilke G, Ravindran S, Funkhouser-Jones L, Barks J, Wang Q, VanDussen KL, Stappenbeck TS, Kuhlenschmidt TB, Kuhlenschmidt MS, Sibley LD, et al. Monoclonal antibodies to intracellular stages of cryptosporidium parvum define life cycle progression in vitro. mSphere. 2018;3(3):3. doi:10.1128/mSphere.00124-18.
   Web of Science ®Google Scholar
• Griffiths JK, Moore R, Dooley S, Keusch GT, Tzipori S. Cryptosporidium parvum infection of caco-2 cell monolayers induces an apical monolayer defect, selectively increases transmonolayer permeability, and causes epithelial cell death. Infect Immun. 1994;62(10):4506–4514. doi:10.1128/iai.62.10.4506-4514.1994.
   Web of Science ®Google Scholar
• de Sablet T, Potiron L, Marquis M, Bussière FI, Lacroix-Lamandé S, Laurent F. Cryptosporidium parvum increases intestinal permeability through interaction with epithelial cells and IL-1β and TNFα released by inflammatory monocytes. Cell Microbiol. 2016;18(12):1871–1880. doi:10.1111/cmi.12632.
   Web of Science ®Google Scholar
• Kumar A, Chatterjee I, Anbazhagan AN, Jayawardena D, Priyamvada S, Alrefai WA, Sun J, Borthakur A, Dudeja PK. Cryptosporidium parvum disrupts intestinal epithelial barrier function via altering expression of key tight junction and adherens junction proteins. Cell Microbiol. 2018;20(6):e12830. doi:10.1111/cmi.12830.
   Web of Science ®Google Scholar
• Priyamvada S, Jayawardena D, Bhalala J, Kumar A, Anbazhagan AN, Alrefai WA, Borthakur A, Dudeja PK. Cryptosporidium parvum infection induces autophagy in intestinal epithelial cells. Cell Microbiol. 2021;23(4):e13298. doi:10.1111/cmi.13298.
   Web of Science ®Google Scholar
• Sateriale A, Gullicksrud JA, Engiles JB, McLeod BI, Kugler EM, Henao-Mejia J, Zhou T, Ring AM, Brodsky IE, Hunter CA, et al. The intestinal parasite Cryptosporidium is controlled by an enterocyte intrinsic inflammasome that depends on NLRP6. Proc Natl Acad Sci U S A. 2021;118(2):118. doi:10.1073/pnas.2007807118.
   Web of Science ®Google Scholar
• Leoni F, Gallimore CI, Green J, McLauchlin J. Characterisation of small double stranded RNA molecule in cryptosporidium hominis, cryptosporidium felis and cryptosporidium meleagridis. Parasitol Int. 2006;55(4):299–306. doi:10.1016/j.parint.2006.06.006.
   Web of Science ®Google Scholar
• Nibert ML, Woods KM, Upton SJ, Ghabrial SA. Cryspovirus: a new genus of protozoan viruses in the family partitiviridae. Arch Virol. 2009;154(12):1959–1965. doi:10.1007/s00705-009-0513-7.
   Web of Science ®Google Scholar
• Ding S, Zhu S, Ren L, Feng N, Song Y, Ge X, Li B, Flavell RA, Greenberg HB. Rotavirus VP3 targets MAVS for degradation to inhibit type III interferon expression in intestinal epithelial cells. Elife. 2018;7:e39494. doi:10.7554/eLife.39494.
   PubMed Web of Science ®Google Scholar
• Ball JM, Tian P, Zeng CQ, Morris AP, Estes MK. Age-dependent diarrhea induced by a rotaviral nonstructural glycoprotein. Sci. 1996;272(5258):101–104. doi:10.1126/science.272.5258.101.
   PubMed Web of Science ®Google Scholar
• Hou G, Zeng Q, Matthijnssens J, Greenberg HB, Ding S, Meng X-J. Rotavirus NSP1 contributes to intestinal viral replication, Pathogenesis, and transmission. mBio. 2021;12(6):e0320821. doi:10.1128/mBio.03208-21.
   Web of Science ®Google Scholar
• Cardenas D, Bhalchandra S, Lamisere H, Chen Y, Zeng X-L, Ramani S, Karandikar UC, Kaplan DL, Estes MK, Ward HD. Two- and three-dimensional bioengineered human intestinal tissue models for cryptosporidium. Methods Mol Biol. 2020;2052:373–402.
   PubMedGoogle Scholar
• Heo I, Dutta D, Schaefer DA, Iakobachvili N, Artegiani B, Sachs N, Boonekamp KE, Bowden G, Hendrickx APA, Willems RJL, et al. Modelling Cryptosporidium infection in human small intestinal and lung organoids. Nat microbiol. 2018;3(7):814–823. doi:10.1038/s41564-018-0177-8.
   PubMed Web of Science ®Google Scholar
• Lamisere H, Bhalchandra S, Kane AV, Zeng X-L, Mo D, Adams W, Estes MK, Ward HD, Bäumler AJ. Differential response to the course of cryptosporidium parvum infection and its impact on epithelial integrity in differentiated versus undifferentiated human intestinal enteroids. Infect Immun. 2022;90(11):e0039722. doi:10.1128/iai.00397-22.
   Web of Science ®Google Scholar
• Ferguson SH, Foster DM, Sherry B, Magness ST, Nielsen DM, Gookin JL. Interferon-λ3 promotes epithelial defense and barrier function against cryptosporidium parvum infection. Cell Mol Gastroenterol Hepatol. 2019;8(1):1–20. doi:10.1016/j.jcmgh.2019.02.007.
   Web of Science ®Google Scholar
• Tang X, Cappa T, Kuhlenschmidt T, Kuhlenschmidt M, Saif T. Specific and non-specific adhesion in cancer Cells with various metastatic potentials [internet]. In: Wagoner Johnson A Harley B, editors. Mechanobiology of cell-cell and cell-Matrix Interactions. Boston, MA: Springer US; 2011. pp. 105–122. [accessed 2023 Feb 27]. doi:10.1007/978-1-4419-8083-0_6.
   Google Scholar
• Crawford CK, Kol A. The Mucosal Innate Immune Response to Cryptosporidium parvum, a Global One Health Issue. Front Cell Infect Microbiol. 2021;11:689401. doi:10.3389/fcimb.2021.689401.
   PubMed Web of Science ®Google Scholar
• Chen W, Harp JA, Harmsen AG, Havell EA. Gamma interferon functions in resistance to cryptosporidium parvum infection in severe combined immunodeficient mice. Infect Immun. 1993;61(8):3548–3551. doi:10.1128/iai.61.8.3548-3551.1993.
   Web of Science ®Google Scholar
• Mead JR, You X. Susceptibility differences to Cryptosporidium parvum infection in two strains of gamma interferon knockout mice. J Parasitol. 1998;84(5):1045–1048. doi:10.2307/3284643.
   Web of Science ®Google Scholar
• Hayward AR, Chmura K, Cosyns M. Interferon-γ is required for innate immunity to cryptosporidium parvum in mice. J Infect Dis. 2000;182(3):1001–1004. doi:10.1086/315802.
   Web of Science ®Google Scholar
• Leav BA, Yoshida M, Rogers K, Cohen S, Godiwala N, Blumberg RS, Ward H. An early intestinal mucosal source of gamma interferon is associated with resistance to and control of Cryptosporidium parvum infection in mice. Infect Immun. 2005;73(12):8425–8428. doi:10.1128/IAI.73.12.8425-8428.2005.
   Web of Science ®Google Scholar
• Gullicksrud JA, Sateriale A, Engiles JB, Gibson AR, Shaw S, Hutchins ZA, Martin L, Christian DA, Taylor GA, Yamamoto M, et al. Enterocyte–innate lymphoid cell crosstalk drives early IFN-γ-mediated control of cryptosporidium. Mucosal Immunol. 2021;15(12):1–11.
   Google Scholar
• Pollok RC, Farthing MJ, Bajaj-Elliott M, Sanderson IR, McDonald V. Interferon gamma induces enterocyte resistance against infection by the intracellular pathogen Cryptosporidium parvum. Gastroenterology. 2001;120(1):99–107. doi:10.1053/gast.2001.20907.
   Web of Science ®Google Scholar
• Choudhry N, Korbel DS, Edwards LA, Bajaj-Elliott M, McDonald V. Dysregulation of interferon-γ-mediated signalling pathway in intestinal epithelial cells by Cryptosporidium parvum infection. Cell Microbiol. 2009;11(9):1354–1364. doi:10.1111/j.1462-5822.2009.01336.x.
   Web of Science ®Google Scholar
• Gomez Morales MA, Ausiello CM, Urbani F, Pozio E. Crude extract and recombinant protein of Cryptosporidium parvum oocysts induce proliferation of human peripheral blood mononuclear cells in vitro. J Infect Dis. 1995;172(1):211–216. doi:10.1093/infdis/172.1.211.
   Web of Science ®Google Scholar
• Gomez Morales MA, La Rosa G, Ludovisi A, Onori AM, Pozio E. Cytokine profile induced by Cryptosporidium antigen in peripheral blood mononuclear cells from immunocompetent and immunosuppressed persons with cryptosporidiosis. J Infect Dis. 1999;179(4):967–973. doi:10.1086/314665.
   Web of Science ®Google Scholar
• White AC, Robinson P, Okhuysen PC, Lewis DE, Shahab I, Lahoti S, DuPont HL, Chappell CL. Interferon-γ expression in Jejunal Biopsies in experimental human cryptosporidiosis correlates with prior sensitization and control of oocyst excretion. J Infect Dis. 2000;181(2):701–709. doi:10.1086/315261.
   Web of Science ®Google Scholar
• Choudhry N, Petry F, van Rooijen N, McDonald V. A protective role for interleukin 18 in interferon γ–mediated innate immunity to cryptosporidium parvum that is Independent of natural killer cells. J Infect Dis. 2012;206(1):117–124. doi:10.1093/infdis/jis300.
   Web of Science ®Google Scholar
• Ghimire L, Paudel S, Jin L, Jeyaseelan S. The NLRP6 inflammasome in health and disease. Mucosal Immunol. 2020;13(3):388–398. doi:10.1038/s41385-020-0256-z.
   PubMed Web of Science ®Google Scholar
• Barakat FM, McDonald V, Foster GR, Tovey MG, Korbel DS. Cryptosporidium parvum infection rapidly induces a protective innate immune response involving type I interferon. J Infect Dis. 2009;200(10):1548–1555. doi:10.1086/644601.
   Web of Science ®Google Scholar
• Ye L, Schnepf D, Staeheli P. Interferon-λ orchestrates innate and adaptive mucosal immune responses. Nat Rev Immunol. 2019;19(10):614–625. doi:10.1038/s41577-019-0182-z.
   PubMed Web of Science ®Google Scholar
• Gibson AR, Sateriale A, Dumaine JE, Engiles JB, Pardy RD, Gullicksrud JA, O’Dea KM, Doench JG, Beiting DP, Hunter CA, et al. A genetic screen identifies a protective type III interferon response to Cryptosporidium that requires TLR3 dependent recognition. PLoS Pathog. 2022;18(5):e1010003. doi:10.1371/journal.ppat.1010003.
   Web of Science ®Google Scholar
• Fitzgerald KA, McWhirter SM, Faia KL, Rowe DC, Latz E, Golenbock DT, Coyle AJ, Liao S-M, Maniatis T. IKKε and TBK1 are essential components of the IRF3 signaling pathway. Nat Immunol. 2003;4(5):491–496. doi:10.1038/ni921.
   PubMed Web of Science ®Google Scholar
• Deng S, He W, Gong A-Y, Li M, Wang Y, Xia Z, Zhang X-T, Huang Pacheco AS, Naqib A, Jenkins M, et al. Cryptosporidium uses CSpV1 to activate host type I interferon and attenuate antiparasitic defenses. Nat Commun. 2023;14(1):1456. doi:10.1038/s41467-023-37129-0.
   Web of Science ®Google Scholar
• Villares M, Berthelet J, Weitzman JB. The clever strategies used by intracellular parasites to hijack host gene expression. Semin Immunopathol. 2020;42(2):215–226. doi:10.1007/s00281-020-00779-z.
   PubMed Web of Science ®Google Scholar
• Zhang X, Liu S, Wang Y, Hu H, Li L, Wu Y, Cao D, Cai Y, Zhang J, Zhang X. Interleukin22 regulates the homeostasis of the intestinal epithelium during inflammation. Int J Mol Med. 2019;43:1657–1668. doi:10.3892/ijmm.2019.4092.
   Web of Science ®Google Scholar
• Južnić L, Peuker K, Strigli A, Brosch M, Herrmann A, Häsler R, Koch M, Matthiesen L, Zeissig Y, Löscher B-S, et al. SETDB1 is required for intestinal epithelial differentiation and the prevention of intestinal inflammation. Gut. 2021;70(3):485–498. doi:10.1136/gutjnl-2020-321339.
   Web of Science ®Google Scholar
• Crawford SE, Ramani S, Tate JE, Parashar UD, Svensson L, Hagbom M, Franco MA, Greenberg HB, O’Ryan M, Kang G, et al. Rotavirus infection. Nat Rev Dis Primers. 2017;3(1):1–16. doi:10.1038/nrdp.2017.83.
   Google Scholar
• Varghese T, Kang G, Steele AD. Understanding rotavirus vaccine efficacy and effectiveness in countries with high child mortality. Vaccines. 2022;10(3):346. doi:10.3390/vaccines10030346.
   Web of Science ®Google Scholar
• Carvalho MF, Gill D. Rotavirus vaccine efficacy: current status and areas for improvement. Hum Vaccin Immunother. 2019;15(6):1237–1250. doi:10.1080/21645515.2018.1520583.
   PubMed Web of Science ®Google Scholar
• Ingle H, Peterson ST, Baldridge MT. Distinct effects of type I and III interferons on enteric viruses. Viruses. 2018;10(1):46. doi:10.3390/v10010046.
   Web of Science ®Google Scholar
• Iaconis G, Jackson B, Childs K, Boyce M, Goodbourn S, Blake N, Iturriza-Gomara M, Seago J. Rotavirus NSP1 inhibits type I and type III interferon induction. Viruses. 2021;13(4):589. doi:10.3390/v13040589.
   Web of Science ®Google Scholar
• Doldan P, Dai J, Metz-Zumaran C, Patton JT, Stanifer ML, Boulant S, López S. Type III and not type I interferons efficiently prevent the spread of rotavirus in human intestinal epithelial cells. J Virol. 2022;96(17):e0070622. doi:10.1128/jvi.00706-22.
   PubMed Web of Science ®Google Scholar
• Kuhlenschmidt TB, Rutaganira FU, Long S, Tang K, Shokat KM, Kuhlenschmidt MS, Sibley LD. Inhibition of Calcium-Dependent Protein Kinase 1 (CDPK1) In Vitro by Pyrazolopyrimidine Derivatives Does Not Correlate with Sensitivity of Cryptosporidium parvum Growth in Cell Culture. Antimicrob Agents Chemother. 2016;60(1):570–579. doi:10.1128/AAC.01915-15.
   Web of Science ®Google Scholar
• Akiyoshi DE, Balakrishnan R, Huettinger C, Widmer G, Tzipori S. Molecular characterization of ribonucleotide reductase from Cryptosporidium parvum. DNA Seq. 2002;13(3):167–172. doi:10.1080/10425170290023419.
   Web of Science ®Google Scholar
• Chappell CL, Okhuysen PC, Langer-Curry R, Widmer G, Akiyoshi DE, Tanriverdi S, Tzipori S. Cryptosporidium hominis: experimental challenge of healthy adults. Am J Trop Med Hyg. 2006;75(5):851–857. doi:10.4269/ajtmh.2006.75.851.
   PubMed Web of Science ®Google Scholar
• Miyoshi H, Ajima R, Luo CT, Yamaguchi TP, Stappenbeck TS. Wnt5a potentiates TGF-β signaling to promote colonic crypt regeneration after tissue injury. Sci. 2012;338(6103):108–113. doi:10.1126/science.1223821.
   PubMed Web of Science ®Google Scholar
• Moon C, VanDussen KL, Miyoshi H, Stappenbeck TS. Development of a primary mouse intestinal epithelial cell monolayer culture system to evaluate factors that modulate IgA transcytosis. Mucosal Immunol. 2014;7(4):818–828. doi:10.1038/mi.2013.98.
   PubMed Web of Science ®Google Scholar
• Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012;9(7):676–682. doi:10.1038/nmeth.2019.
   PubMed Web of Science ®Google Scholar
• The GIMP Development Team. GIMP [Internet]. [accessed 2023 Mar 6]. https://www.gimp.org/.
   Google Scholar
• Mo D, Xu S, Rosa JP, Hasan S, Adams W. Dynamic python-based method provides quantitative analysis of intercellular junction organization during S. Pneumoniae infection of the respiratory epithelium. Front Cell Infect Microbiol. 2022;12:865528. [accessed 2023 Mar 2]. doi:10.3389/fcimb.2022.865528.
   Web of Science ®Google Scholar
• Clark HF, Hoshino Y, Bell LM, Groff J, Hess G, Bachman P, Offit PA. Rotavirus isolate WI61 representing a presumptive new human serotype. J Clin Microbiol. 1987;25(9):1757–1762. doi:10.1128/jcm.25.9.1757-1762.1987.
   PubMed Web of Science ®Google Scholar
• Sánchez-Tacuba L, Feng N, Meade NJ, Mellits KH, Jaïs PH, Yasukawa LL, Resch TK, Jiang B, López S, Ding S, et al. An optimized reverse genetics system suitable for efficient recovery of simian, human, and Murine-Like Rotaviruses. J Virol. 2020;94(18):e01294–20. doi:10.1128/JVI.01294-20.
   Web of Science ®Google Scholar
• Shaw RD, Hempson SJ, Mackow ER. Rotavirus diarrhea is caused by nonreplicating viral particles. J Virol. 1995;69(10):5946–5950. doi:10.1128/jvi.69.10.5946-5950.1995.
   Web of Science ®Google Scholar
• Zhu Y, Sánchez-Tacuba L, Hou G, Kawagishi T, Feng N, Greenberg HB, Ding S. A recombinant murine-like rotavirus with Nano-Luciferase expression reveals tissue tropism, replication dynamics, and virus transmission. Front Immunol. 2022;13:911024. [accessed 2023 Sep 28]. doi:10.3389/fimmu.2022.911024.
   Web of Science ®Google Scholar