Cellular and Molecular Life Sciences

, Volume 75, Issue 23, pp 4417–4443 | Cite as

Toxoplasma gondii chromosomal passenger complex is essential for the organization of a functional mitotic spindle: a prerequisite for productive endodyogeny

  • Laurence Berry
  • Chun-Ti Chen
  • Maria E. Francia
  • Amandine Guerin
  • Arnault Graindorge
  • Jean-Michel Saliou
  • Maurane Grandmougin
  • Sharon Wein
  • Chérine Bechara
  • Juliette Morlon-Guyot
  • Yann Bordat
  • Marc-Jan Gubbels
  • Maryse Lebrun
  • Jean-François Dubremetz
  • Wassim DaherEmail author
Original Article


The phylum Apicomplexa encompasses deadly pathogens such as malaria and Cryptosporidium. Apicomplexa cell division is mechanistically divergent from that of their mammalian host, potentially representing an attractive source of drug targets. Depending on the species, apicomplexan parasites can modulate the output of cell division, producing two to thousands of daughter cells at once. The inherent flexibility of their cell division mechanisms allows these parasites to adapt to different niches, facilitating their dissemination. Toxoplasma gondii tachyzoites divide using a unique form of cell division called endodyogeny. This process involves a single round of DNA replication, closed nuclear mitosis, and assembly of two daughter cells within a mother. In higher Eukaryotes, the four-subunit chromosomal passenger complex (CPC) (Aurora kinase B (ARKB)/INCENP/Borealin/Survivin) promotes chromosome bi-orientation by detaching incorrect kinetochore–microtubule attachments, playing an essential role in controlling cell division fidelity. Herein, we report the characterization of the Toxoplasma CPC (Aurora kinase 1 (Ark1)/INCENP1/INCENP2). We show that the CPC exhibits dynamic localization in a cell cycle-dependent manner. TgArk1 interacts with both TgINCENPs, with TgINCENP2 being essential for its translocation to the nucleus. While TgINCENP1 appears to be dispensable, interfering with TgArk1 or TgINCENP2 results in pronounced division and growth defects. Significant anti-cancer drug development efforts have focused on targeting human ARKB. Parasite treatment with low doses of hesperadin, a known inhibitor of human ARKB at higher concentrations, phenocopies the TgArk1 and TgINCENP2 mutants. Overall, our study provides new insights into the mechanisms underpinning cell cycle control in Apicomplexa, and highlights TgArk1 as potential drug target.


Apicomplexa Toxoplasma gondii Cytokinesis Mitosis Centrosome Kinetochore Centromere Spindle Chromosomal passenger complex Aurora kinase Endodyogeny Inner membrane complex 



Aurora-related kinase 1


Inner centromere protein


Trans-activator Trap identified


Inner membrane complex


Nuclear filamentous 2


Microtubule-associated protein RP/EB family member


Centrosomal protein



We wish to thank Dominique Soldati-Favre, Vern Carruthers, Lilach Sheiner, Sebastian Lourido, Boris Striepen, Markus Meissner, Peter Bradley, Mathieu Gissot, Christian Doerig, Con Beckers, Iain Cheeseman, Jose Garcia-Bustos, Henri Vial and Marjorie Bienvenu for their kind gift of cell lines, hesperadin drug, plasmids or antibodies, for advices and technical assistance. We also thank the “Montpellier Ressources imagerie” platform, and the electron microscopy facility of the University of Montpellier (MEA), for their assistance in light and electron microscopy experiments, respectively. Dr. Wassim DAHER, Dr. Juliette Morlon-Guyot and Dr. Maryse LEBRUN are INSERM researchers. This work was made possible through core support from the Fondation pour la Recherche Médicale (Equipe FRMDEQ20170336725), the Labex Parafrap (ANR-11-LABX-0024), and National Institute of Health Grants AI110690, AI110638, and AI128136.

Compliance with ethical standards

Conflict of interest

The authors declare that there are no conflicts of interest.

Supplementary material

18_2018_2889_MOESM1_ESM.pdf (1.9 mb)
Supplementary material 1 (PDF 1935 kb)
18_2018_2889_MOESM2_ESM.xlsx (292 kb)
Supplementary material 2 (XLSX 292 kb)


  1. 1.
    Suarez CE, Bishop RP, Alzan HF, Poole WA, Cooke BM (2017) Advances in the application of genetic manipulation methods to apicomplexan parasites. Int J Parasitol 47:701–710CrossRefGoogle Scholar
  2. 2.
    Francia ME, Striepen B (2014) Cell division in apicomplexan parasites. Nat Rev Microbiol 12:125–136CrossRefGoogle Scholar
  3. 3.
    Brooks CF, Francia ME, Gissot M, Croken MM, Kim K, Striepen B (2011) Toxoplasma gondii sequesters centromeres to a specific nuclear region throughout the cell cycle. Proc Natl Acad Sci USA 108:3767–3772CrossRefGoogle Scholar
  4. 4.
    Gavin MA, Wanko T, Jacobs L (1962) Electron microscope studies of reproducing and interkinetic Toxoplasma. J Protozool 9:222–234CrossRefGoogle Scholar
  5. 5.
    Nigg EA (2001) Mitotic kinases as regulators of cell division and its checkpoints. Nat Rev Mol Cell Biol 2:21–32CrossRefGoogle Scholar
  6. 6.
    Zitouni S, Nabais C, Jana SC, Guerrero A, Bettencourt-Dias M (2014) Polo-like kinases: structural variations lead to multiple functions. Nat Rev Mol Cell Biol 15:433–452CrossRefGoogle Scholar
  7. 7.
    Chen CT, Gubbels MJ (2013) The Toxoplasma gondii centrosome is the platform for internal daughter budding as revealed by a Nek1 kinase mutant. J Cell Sci 126:3344–3355CrossRefGoogle Scholar
  8. 8.
    Courjol F, Gissot M (2018) A coiled-coil protein is required for coordination of karyokinesis and cytokinesis in Toxoplasma gondii. Cell Microbiol 20:e12832CrossRefGoogle Scholar
  9. 9.
    Francia ME et al (2012) Cell division in Apicomplexan parasites is organized by a homolog of the striated rootlet fiber of algal flagella. PLoS Biol 10:e1001444CrossRefGoogle Scholar
  10. 10.
    Morlon-Guyot J, Francia ME, Dubremetz JF, Daher W (2017) Towards a molecular architecture of the centrosome in Toxoplasma gondii. Cytoskeleton (Hoboken) 74:55–71CrossRefGoogle Scholar
  11. 11.
    Suvorova ES, Francia M, Striepen B, White MW (2015) A novel bipartite centrosome coordinates the apicomplexan cell cycle. PLoS Biol 13:e1002093CrossRefGoogle Scholar
  12. 12.
    Morlon-Guyot J, Berry L, Chen CT, Gubbels MJ, Lebrun M, Daher W (2014) The Toxoplasma gondii calcium-dependent protein kinase 7 is involved in early steps of parasite division and is crucial for parasite survival. Cell Microbiol 16:95–114CrossRefGoogle Scholar
  13. 13.
    Berry L et al (2016) The conserved apicomplexan Aurora kinase TgArk3 is involved in endodyogeny, duplication rate and parasite virulence. Cell Microbiol 18:1106–1120CrossRefGoogle Scholar
  14. 14.
    Alvarez CA, Suvorova ES (2017) Checkpoints of apicomplexan cell division identified in Toxoplasma gondii. PLoS Pathog 13:e1006483CrossRefGoogle Scholar
  15. 15.
    Deshmukh AS, Mitra P, Kolagani A, Gurupwar R (2018) Cdk-related kinase 9 regulates RNA polymerase II mediated transcription in Toxoplasma gondii. Biochim Biophys Acta 1861:572–585CrossRefGoogle Scholar
  16. 16.
    Naumov A, Kratzer S, Ting LM, Kim K, Suvorova ES, White MW (2017) The Toxoplasma centrocone houses cell cycle regulatory factors. MBio 8:e00579-17CrossRefGoogle Scholar
  17. 17.
    Andrews PD, Knatko E, Moore WJ, Swedlow JR (2003) Mitotic mechanics: the auroras come into view. Curr Opin Cell Biol 15:672–683CrossRefGoogle Scholar
  18. 18.
    Carmena M, Earnshaw WC (2003) The cellular geography of aurora kinases. Nat Rev Mol Cell Biol 4:842–854CrossRefGoogle Scholar
  19. 19.
    Hochegger H, Hegarat N, Pereira-Leal JB (2013) Aurora at the pole and equator: overlapping functions of Aurora kinases in the mitotic spindle. Open Biol 3:120185CrossRefGoogle Scholar
  20. 20.
    Carmena M, Wheelock M, Funabiki H, Earnshaw WC (2012) The chromosomal passenger complex (CPC): from easy rider to the godfather of mitosis. Nat Rev Mol Cell Biol 13:789–803CrossRefGoogle Scholar
  21. 21.
    Lampson MA, Cheeseman IM (2011) Sensing centromere tension: Aurora B and the regulation of kinetochore function. Trends Cell Biol 21:133–140CrossRefGoogle Scholar
  22. 22.
    Liu D, Lampson MA (2009) Regulation of kinetochore-microtubule attachments by Aurora B kinase. Biochem Soc Trans 37:976–980CrossRefGoogle Scholar
  23. 23.
    Goto H, Yasui Y, Kawajiri A, Nigg EA, Terada Y, Tatsuka M, Nagata K, Inagaki M (2003) Aurora-B regulates the cleavage furrow-specific vimentin phosphorylation in the cytokinetic process. J Biol Chem 278:8526–8530CrossRefGoogle Scholar
  24. 24.
    Kawajiri A, Yasui Y, Goto H, Tatsuka M, Takahashi M, Nagata K, Inagaki M (2003) Functional significance of the specific sites phosphorylated in desmin at cleavage furrow: Aurora-B may phosphorylate and regulate type III intermediate filaments during cytokinesis coordinatedly with Rho-kinase. Mol Biol Cell 14:1489–1500CrossRefGoogle Scholar
  25. 25.
    Kondo T, Isoda R, Ookusa T, Kamijo K, Hamao K, Hosoya H (2013) Aurora B but not rho/MLCK signaling is required for localization of diphosphorylated myosin II regulatory light chain to the midzone in cytokinesis. PLoS One 8:e70965CrossRefGoogle Scholar
  26. 26.
    Landino J, Ohi R (2016) The timing of midzone stabilization during cytokinesis depends on myosin II activity and an interaction between INCENP and actin. Curr Biol 26:698–706CrossRefGoogle Scholar
  27. 27.
    Maciejowski J et al (2017) Mps1 regulates kinetochore-microtubule attachment stability via the Ska complex to ensure error-free chromosome segregation. Dev Cell 41(143–156):e6Google Scholar
  28. 28.
    Zhou X et al (2017) Phosphorylation of CENP-C by Aurora B facilitates kinetochore attachment error correction in mitosis. Proc Natl Acad Sci USA 114:E10667–E10676CrossRefGoogle Scholar
  29. 29.
    Kim K, Soldati D, Boothroyd JC (1993) Gene replacement in Toxoplasma gondii with chloramphenicol acetyltransferase as selectable marker. Science 262:911–914CrossRefGoogle Scholar
  30. 30.
    Donald RG, Roos DS (1993) Stable molecular transformation of Toxoplasma gondii: a selectable dihydrofolate reductase-thymidylate synthase marker based on drug-resistance mutations in malaria. Proc Natl Acad Sci USA 90:11703–11707CrossRefGoogle Scholar
  31. 31.
    Donald RG, Carter D, Ullman B, Roos DS (1996) Insertional tagging, cloning, and expression of the Toxoplasma gondii hypoxanthine–xanthine–guanine phosphoribosyltransferase gene. Use as a selectable marker for stable transformation. J Biol Chem 271:14010–14019CrossRefGoogle Scholar
  32. 32.
    Meissner M, Brecht S, Bujard H, Soldati D (2001) Modulation of myosin A expression by a newly established tetracycline repressor-based inducible system in Toxoplasma gondii. Nucleic Acids Res 29:E115CrossRefGoogle Scholar
  33. 33.
    Herm-Gotz A, Agop-Nersesian C, Munter S, Grimley JS, Wandless TJ, Frischknecht F, Meissner M (2007) Rapid control of protein level in the apicomplexan Toxoplasma gondii. Nat Methods 4:1003–1005CrossRefGoogle Scholar
  34. 34.
    Huynh MH, Carruthers VB (2009) Tagging of endogenous genes in a Toxoplasma gondii strain lacking Ku80. Eukaryot Cell 8:530–539CrossRefGoogle Scholar
  35. 35.
    Sheiner L, Demerly JL, Poulsen N, Beatty WL, Lucas O, Behnke MS, White MW, Striepen B (2011) A systematic screen to discover and analyze apicoplast proteins identifies a conserved and essential protein import factor. PLoS Pathog 7:e1002392CrossRefGoogle Scholar
  36. 36.
    Daher W, Plattner F, Carlier MF, Soldati-Favre D (2010) Concerted action of two formins in gliding motility and host cell invasion by Toxoplasma gondii. PLoS Pathog 6:e1001132CrossRefGoogle Scholar
  37. 37.
    Mann T, Beckers C (2001) Characterization of the subpellicular network, a filamentous membrane skeletal component in the parasite Toxoplasma gondii. Mol Biochem Parasitol 115:257–268CrossRefGoogle Scholar
  38. 38.
    Beck JR, Rodriguez-Fernandez IA, de Leon JC, Huynh MH, Carruthers VB, Morrissette NS, Bradley PJ (2010) A novel family of Toxoplasma IMC proteins displays a hierarchical organization and functions in coordinating parasite division. PLoS Pathog 6:e1001094CrossRefGoogle Scholar
  39. 39.
    Farrell M, Gubbels MJ (2014) The Toxoplasma gondii kinetochore is required for centrosome association with the centrocone (spindle pole). Cell Microbiol 16:78–94CrossRefGoogle Scholar
  40. 40.
    Lamarque MH et al (2014) Plasticity and redundancy among AMA-RON pairs ensure host cell entry of Toxoplasma parasites. Nat Commun 5:4098CrossRefGoogle Scholar
  41. 41.
    Frenal K, Polonais V, Marq JB, Stratmann R, Limenitakis J, Soldati-Favre D (2010) Functional dissection of the apicomplexan glideosome molecular architecture. Cell Host Microbe 8:343–357CrossRefGoogle Scholar
  42. 42.
    Sievers F et al (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:539CrossRefGoogle Scholar
  43. 43.
    Miguet L et al (2009) Proteomic analysis of malignant B-cell derived microparticles reveals CD148 as a potentially useful antigenic biomarker for mantle cell lymphoma diagnosis. J Proteome Res 8:3346–3354CrossRefGoogle Scholar
  44. 44.
    Manic G, Corradi F, Sistigu A, Siteni S, Vitale I (2017) Molecular regulation of the spindle assembly checkpoint by kinases and phosphatases. Int Rev Cell Mol Biol 328:105–161CrossRefGoogle Scholar
  45. 45.
    Ainsztein AM, Kandels-Lewis SE, Mackay AM, Earnshaw WC (1998) INCENP centromere and spindle targeting: identification of essential conserved motifs and involvement of heterochromatin protein HP1. J Cell Biol 143:1763–1774CrossRefGoogle Scholar
  46. 46.
    Krenn V, Musacchio A (2015) The Aurora B kinase in chromosome bi-orientation and spindle checkpoint signaling. Front Oncol 5:225CrossRefGoogle Scholar
  47. 47.
    Sessa F, Mapelli M, Ciferri C, Tarricone C, Areces LB, Schneider TR, Stukenberg PT, Musacchio A (2005) Mechanism of Aurora B activation by INCENP and inhibition by hesperadin. Mol Cell 18:379–391CrossRefGoogle Scholar
  48. 48.
    Sidik SM et al (2016) A genome-wide CRISPR screen in Toxoplasma identifies essential apicomplexan genes. Cell 166(1423–1435):e12Google Scholar
  49. 49.
    Murata-Hori M, Wang YL (2002) The kinase activity of aurora B is required for kinetochore-microtubule interactions during mitosis. Curr Biol 12:894–899CrossRefGoogle Scholar
  50. 50.
    Shao H, Ma C, Zhang X, Li R, Miller AL, Bement WM, Liu XJ (2012) Aurora B regulates spindle bipolarity in meiosis in vertebrate oocytes. Cell Cycle 11:2672–2680CrossRefGoogle Scholar
  51. 51.
    Adams JA, Taylor SS (1993) Divalent metal ions influence catalysis and active-site accessibility in the cAMP-dependent protein kinase. Protein Sci 2:2177–2186CrossRefGoogle Scholar
  52. 52.
    Cosmelli D, Antonelli M, Allende CC, Allende JE (1997) An inactive mutant of the alpha subunit of protein kinase CK2 that traps the regulatory CK2beta subunit. FEBS Lett 410:391–396CrossRefGoogle Scholar
  53. 53.
    Fentress SJ et al (2010) Phosphorylation of immunity-related GTPases by a Toxoplasma gondii-secreted kinase promotes macrophage survival and virulence. Cell Host Microbe 8:484–495CrossRefGoogle Scholar
  54. 54.
    Honda R, Korner R, Nigg EA (2003) Exploring the functional interactions between Aurora B, INCENP, and survivin in mitosis. Mol Biol Cell 14:3325–3341CrossRefGoogle Scholar
  55. 55.
    Gubbels MJ, White M, Szatanek T (2008) The cell cycle and Toxoplasma gondii cell division: tightly knit or loosely stitched? Int J Parasitol 38:1343–1358CrossRefGoogle Scholar
  56. 56.
    Radke JR, Striepen B, Guerini MN, Jerome ME, Roos DS, White MW (2001) Defining the cell cycle for the tachyzoite stage of Toxoplasma gondii. Mol Biochem Parasitol 115:165–175CrossRefGoogle Scholar
  57. 57.
    Anderson-White B, Beck JR, Chen CT, Meissner M, Bradley PJ, Gubbels MJ (2012) Cytoskeleton assembly in Toxoplasma gondii cell division. Int Rev Cell Mol Biol 298:1–31CrossRefGoogle Scholar
  58. 58.
    Nishi M, Hu K, Murray JM, Roos DS (2008) Organellar dynamics during the cell cycle of Toxoplasma gondii. J Cell Sci 121:1559–1568CrossRefGoogle Scholar
  59. 59.
    Gissot M, Hovasse A, Chaloin L, Schaeffer-Reiss C, Van Dorsselaer A, Tomavo S (2017) An evolutionary conserved zinc finger protein is involved in Toxoplasma gondii mRNA nuclear export. Cell Microbiol 19:e12644CrossRefGoogle Scholar
  60. 60.
    Gubbels MJ, Vaishnava S, Boot N, Dubremetz JF, Striepen B (2006) A MORN-repeat protein is a dynamic component of the Toxoplasma gondii cell division apparatus. J Cell Sci 119:2236–2245CrossRefGoogle Scholar
  61. 61.
    Hu K (2008) Organizational changes of the daughter basal complex during the parasite replication of Toxoplasma gondii. PLoS Pathog 4:e10CrossRefGoogle Scholar
  62. 62.
    Chen CT et al (2015) Compartmentalized Toxoplasma EB1 bundles spindle microtubules to secure accurate chromosome segregation. Mol Biol Cell 26:4562–4576CrossRefGoogle Scholar
  63. 63.
    Gissot M, Walker R, Delhaye S, Huot L, Hot D, Tomavo S (2012) Toxoplasma gondii chromodomain protein 1 binds to heterochromatin and colocalises with centromeres and telomeres at the nuclear periphery. PLoS One 7:e32671CrossRefGoogle Scholar
  64. 64.
    Hu Y, Zhang J, Musharrafieh R, Hau R, Ma C, Wang J (2017) Chemical genomics approach leads to the identification of hesperadin, an aurora B kinase inhibitor, as a broad-spectrum influenza antiviral. Int J Mol Sci 18:1929CrossRefGoogle Scholar
  65. 65.
    Shamsipour F, Hosseinzadeh S, Arab SS, Vafaei S, Farid S, Jeddi-Tehrani M, Balalaie S (2014) Synthesis and investigation of new Hesperadin analogues antitumor effects on HeLa cells. J Chem Biol 7:85–91CrossRefGoogle Scholar
  66. 66.
    Hauf S et al (2003) The small molecule Hesperadin reveals a role for Aurora B in correcting kinetochore-microtubule attachment and in maintaining the spindle assembly checkpoint. J Cell Biol 161:281–294CrossRefGoogle Scholar
  67. 67.
    Dubremetz JF (1973) Ultrastructural study of schizogonic mitosis in the coccidian, Eimeria necatrix (Johnson 1930). J Ultrastruct Res 42:354–376CrossRefGoogle Scholar
  68. 68.
    Dubremetz JF, Elsner YY (1979) Ultrastructural study of schizogony of Eimeria bovis in cell cultures. J Protozool 26:367–376CrossRefGoogle Scholar
  69. 69.
    Samejima K, Platani M, Wolny M, Ogawa H, Vargiu G, Knight PJ, Peckham M, Earnshaw WC (2015) The inner centromere protein (INCENP) coil is a single alpha-helix (SAH) domain that binds directly to microtubules and is important for chromosome passenger complex (CPC) localization and function in mitosis. J Biol Chem 290:21460–21472CrossRefGoogle Scholar
  70. 70.
    Karg T, Warecki B, Sullivan W (2015) Aurora B-mediated localized delays in nuclear envelope formation facilitate inclusion of late-segregating chromosome fragments. Mol Biol Cell 26:2227–2241CrossRefGoogle Scholar
  71. 71.
    Mackay DR, Makise M, Ullman KS (2010) Defects in nuclear pore assembly lead to activation of an Aurora B-mediated abscission checkpoint. J Cell Biol 191:923–931CrossRefGoogle Scholar
  72. 72.
    Mackay DR, Ullman KS (2011) Coordinating postmitotic nuclear pore complex assembly with abscission timing. Nucleus 2:283–288CrossRefGoogle Scholar
  73. 73.
    Courjol F et al (2017) Characterization of a nuclear pore protein sheds light on the roles and composition of the Toxoplasma gondii nuclear pore complex. Cell Mol Life Sci 74:2107–2125CrossRefGoogle Scholar
  74. 74.
    Shannon KB, Salmon ED (2002) Chromosome dynamics: new light on Aurora B kinase function. Curr Biol 12:R458–R460CrossRefGoogle Scholar
  75. 75.
    Song J, Salek-Ardakani S, So T, Croft M (2007) The kinases aurora B and mTOR regulate the G1-S cell cycle progression of T lymphocytes. Nat Immunol 8:64–73CrossRefGoogle Scholar
  76. 76.
    Mackay DR, Ullman KS (2015) ATR and a Chk1-Aurora B pathway coordinate postmitotic genome surveillance with cytokinetic abscission. Mol Biol Cell 26:2217–2226CrossRefGoogle Scholar
  77. 77.
    Mathieu J et al (2013) Aurora B and cyclin B have opposite effects on the timing of cytokinesis abscission in Drosophila germ cells and in vertebrate somatic cells. Dev Cell 26:250–265CrossRefGoogle Scholar
  78. 78.
    Thoresen SB, Campsteijn C, Vietri M, Schink KO, Liestol K, Andersen JS, Raiborg C, Stenmark H (2014) ANCHR mediates Aurora-B-dependent abscission checkpoint control through retention of VPS4. Nat Cell Biol 16:550–560CrossRefGoogle Scholar
  79. 79.
    Dhara A, de Paula Baptista R, Kissinger JC, Snow EC, Sinai AP (2017) Ablation of an ovarian tumor family deubiquitinase exposes the underlying regulation governing the plasticity of cell cycle progression in Toxoplasma gondii. MBio 8:e01846-17CrossRefGoogle Scholar
  80. 80.
    van der Horst A, Vromans MJ, Bouwman K, van der Waal MS, Hadders MA, Lens SM (2015) Inter-domain cooperation in INCENP promotes Aurora B relocation from centromeres to microtubules. Cell Rep 12:380–387CrossRefGoogle Scholar
  81. 81.
    de Groot CO et al (2015) A cell biologist’s field guide to aurora kinase inhibitors. Front Oncol 5:285CrossRefGoogle Scholar
  82. 82.
    Falchook GS, Bastida CC, Kurzrock R (2015) Aurora kinase inhibitors in oncology clinical trials: current state of the progress. Semin Oncol 42:832–848CrossRefGoogle Scholar
  83. 83.
    Lok W, Klein RQ, Saif MW (2010) Aurora kinase inhibitors as anti-cancer therapy. Anticancer Drugs 21:339–350CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • Laurence Berry
    • 1
  • Chun-Ti Chen
    • 2
  • Maria E. Francia
    • 3
  • Amandine Guerin
    • 1
    • 4
  • Arnault Graindorge
    • 1
  • Jean-Michel Saliou
    • 5
  • Maurane Grandmougin
    • 5
  • Sharon Wein
    • 1
  • Chérine Bechara
    • 1
    • 6
  • Juliette Morlon-Guyot
    • 1
  • Yann Bordat
    • 1
  • Marc-Jan Gubbels
    • 2
  • Maryse Lebrun
    • 1
  • Jean-François Dubremetz
    • 1
  • Wassim Daher
    • 1
    Email author
  1. 1.Dynamique des Interactions Membranaires Normales et Pathologiques, UMR5235 CNRS, INSERMUniversité de MontpellierMontpellierFrance
  2. 2.Department of BiologyBoston CollegeChestnut HillUSA
  3. 3.Molecular Biology UnitInstitut Pasteur de MontevideoMontevideoUruguay
  4. 4.Department of Pathobiology, School of Veterinary MedicineUniversity of PennsylvaniaPhiladelphiaUSA
  5. 5.CNRS, INSERM, CHU Lille, Institut Pasteur de Lille, U1019, UMR 8204, CIIL-Centre d’Infection et d’Immunité de LilleUniversity of LilleLilleFrance
  6. 6.Institut de Génomique Fonctionnelle, CNRS, UMR5230 INSERM U1191University of MontpellierMontpellierFrance

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