DOI: 10.1111/j.1365-2958.2009.06828.x. Vital role for the <i>Plasmodium</i> actin capping protein (CP) beta‐subunit in motility of malaria sporozoites

Vital role for the Plasmodium actin capping protein (CP) beta‐subunit in motility of malaria sporozoites

10.1111/j.1365-2958.2009.06828.x

Crossref journal-article

Wiley

Molecular Microbiology (311)

Abstract

SummarySuccessful malaria transmission from the mosquito vector to the mammalian host depends crucially on active sporozoite motility. Sporozoite locomotion and host cell invasion are driven by the parasite's own actin/myosin motor. A unique feature of this motor machinery is the presence of very short subpellicular actin filaments. Therefore, F‐actin stabilizing proteins likely play a central role in parasite locomotion. Here, we investigated the role of the Plasmodium berghei actin capping protein (PbCP), an orthologue of the heterodimeric regulator of filament barbed end growth, by reverse genetics. Parasites containing a deletion of the CP beta‐subunit developed normally during the pathogenic erythrocytic cycle. However, due to reduced ookinete motility, mutant parasites form fewer oocysts and sporozoites in the Anopheles vector. These sporozoites display a vital deficiency in forward gliding motility and fail to colonize the mosquito salivary glands, resulting in complete attenuation of life cycle progression. Together, our results show that the CP beta‐subunit exerts an essential role in the insect vector before malaria transmission to the mammalian host. The vital role is restricted to fast locomotion, as displayed by Plasmodium sporozoites.

Bibliography

Ganter, M., SchÃ¼ler, H., & Matuschewski, K. (2009). Vital role for the Plasmodium actin capping protein (CP) betaâsubunit in motility of malaria sporozoites. Molecular Microbiology, 74(6), 1356â1367. Portico.

Authors 3

Markus Ganter (first)
Herwig Schüler (additional)
Kai Matuschewski (additional)

References 44 Referenced 39

10.1091/mbc.4.5.459
10.1083/jcb.117.5.1067
10.1074/jbc.270.37.21472
10.1038/nrmicro1465
10.1016/j.chom.2008.02.006
10.1242/jcs.00194
10.1091/mbc.E03-06-0355
10.1074/jbc.R700020200
10.1016/S1937-6448(08)00604-7
10.1186/1471-2164-6-179
10.1002/elps.1150181505
10.2174/156652406776055131
10.1083/jcb.133.6.1293
10.1016/0092-8674(95)90080-2
10.1016/j.molbiopara.2005.09.007
10.1016/S1097-2765(03)00113-8
10.1016/j.tcb.2004.08.002
10.1016/j.mib.2007.09.015
10.1038/44183
10.1111/j.1462-5822.2006.00778.x
10.1007/978-0-387-78267-6_9
10.1074/jbc.M207315200
10.1126/science.1074553
10.1016/j.cell.2004.07.019
10.1084/jem.149.1.172
10.1038/sj.emboj.7601395
10.1371/journal.ppat.0030030
10.1083/jcb.200303023
10.1091/mbc.e05-06-0512 / Mol Biol Cell / Unusual kinetic and structural properties control rapid assembly and turnover of actin in the parasite Toxoplasma gondii by Sahoo N. (2005)
10.1083/jcb.126.2.403
10.1016/j.jmb.2005.03.056
10.1016/j.pt.2006.02.005
10.1111/j.1600-0854.2006.00484.x
10.1016/j.febslet.2004.12.037
10.1126/science.1094717
10.1371/journal.ppat.0030195
10.1111/j.1462-5822.2007.01058.x
10.1023/A:1005329114263
10.1016/S0166-6851(98)00044-9
{'key': 'e_1_2_6_41_1', 'first-page': '317', 'article-title': 'Gene targeting in Plasmodium berghei', 'volume': '72', 'author': 'Thathy V.', 'year': '2002', 'journal-title': 'Methods Mol Med'} / Methods Mol Med / Gene targeting in Plasmodium berghei by Thathy V. (2002)
10.2307/3279102
10.1016/j.tibs.2004.06.003
10.1002/(SICI)1097-0169(1999)42:1<73::AID-CM7>3.0.CO;2-Z
10.1093/emboj/cdg167

Dates

Type	When
Created	16 years, 1 month ago (Aug. 4, 2009, 6:13 a.m.)
Deposited	1 year, 10 months ago (Oct. 14, 2023, 6:55 a.m.)
Indexed	1 year ago (Aug. 6, 2024, 11 a.m.)
Issued	15 years, 9 months ago (Dec. 1, 2009)
Published	15 years, 9 months ago (Dec. 1, 2009)
Published Online	15 years, 8 months ago (Dec. 10, 2009)
Published Print	15 years, 9 months ago (Dec. 1, 2009)

Funders 0

None

BibTeX

@article{Ganter_2009, title={Vital role for the Plasmodium actin capping protein (CP) beta‐subunit in motility of malaria sporozoites}, volume={74}, ISSN={1365-2958}, url={http://dx.doi.org/10.1111/j.1365-2958.2009.06828.x}, DOI={10.1111/j.1365-2958.2009.06828.x}, number={6}, journal={Molecular Microbiology}, publisher={Wiley}, author={Ganter, Markus and Schüler, Herwig and Matuschewski, Kai}, year={2009}, month=dec, pages={1356–1367} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2024,
        8,
        6
      ]
    ],
    "date-time": "2024-08-06T15:00:32Z",
    "timestamp": 1722956432076
  },
  "reference-count": 44,
  "publisher": "Wiley",
  "issue": "6",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            2009,
            8,
            4
          ]
        ],
        "date-time": "2009-08-04T00:00:00Z",
        "timestamp": 1249344000000
      },
      "content-version": "vor",
      "delay-in-days": 0,
      "URL": "http://onlinelibrary.wiley.com/termsAndConditions#vor"
    }
  ],
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        2009,
        12
      ]
    ]
  },
  "abstract": "<jats:title>Summary</jats:title><jats:p>Successful malaria transmission from the mosquito vector to the mammalian host depends crucially on active sporozoite motility. Sporozoite locomotion and host cell invasion are driven by the parasite's own actin/myosin motor. A unique feature of this motor machinery is the presence of very short subpellicular actin filaments. Therefore, F\u2010actin stabilizing proteins likely play a central role in parasite locomotion. Here, we investigated the role of the <jats:italic>Plasmodium berghei</jats:italic> actin capping protein (<jats:italic>Pb</jats:italic>CP), an orthologue of the heterodimeric regulator of filament barbed end growth, by reverse genetics. Parasites containing a deletion of the CP beta\u2010subunit developed normally during the pathogenic erythrocytic cycle. However, due to reduced ookinete motility, mutant parasites form fewer oocysts and sporozoites in the <jats:italic>Anopheles</jats:italic> vector. These sporozoites display a vital deficiency in forward gliding motility and fail to colonize the mosquito salivary glands, resulting in complete attenuation of life cycle progression. Together, our results show that the CP beta\u2010subunit exerts an essential role in the insect vector before malaria transmission to the mammalian host. The vital role is restricted to fast locomotion, as displayed by <jats:italic>Plasmodium</jats:italic> sporozoites.</jats:p>",
  "DOI": "10.1111/j.1365-2958.2009.06828.x",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2009,
        8,
        4
      ]
    ],
    "date-time": "2009-08-04T10:13:32Z",
    "timestamp": 1249380812000
  },
  "page": "1356-1367",
  "source": "Crossref",
  "is-referenced-by-count": 39,
  "title": "Vital role for the <i>Plasmodium</i> actin capping protein (CP) beta\u2010subunit in motility of malaria sporozoites",
  "prefix": "10.1111",
  "volume": "74",
  "author": [
    {
      "given": "Markus",
      "family": "Ganter",
      "sequence": "first",
      "affiliation": []
    },
    {
      "given": "Herwig",
      "family": "Sch\u00fcler",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Kai",
      "family": "Matuschewski",
      "sequence": "additional",
      "affiliation": []
    }
  ],
  "member": "311",
  "published-online": {
    "date-parts": [
      [
        2009,
        12,
        10
      ]
    ]
  },
  "reference": [
    {
      "key": "e_1_2_6_2_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1091/mbc.4.5.459"
    },
    {
      "key": "e_1_2_6_3_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1083/jcb.117.5.1067"
    },
    {
      "key": "e_1_2_6_4_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.270.37.21472"
    },
    {
      "key": "e_1_2_6_5_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/nrmicro1465"
    },
    {
      "key": "e_1_2_6_6_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/j.chom.2008.02.006"
    },
    {
      "key": "e_1_2_6_7_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1242/jcs.00194"
    },
    {
      "key": "e_1_2_6_8_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1091/mbc.E03-06-0355"
    },
    {
      "key": "e_1_2_6_9_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.R700020200"
    },
    {
      "key": "e_1_2_6_10_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S1937-6448(08)00604-7"
    },
    {
      "key": "e_1_2_6_11_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1186/1471-2164-6-179"
    },
    {
      "key": "e_1_2_6_12_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/elps.1150181505"
    },
    {
      "key": "e_1_2_6_13_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.2174/156652406776055131"
    },
    {
      "key": "e_1_2_6_14_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1083/jcb.133.6.1293"
    },
    {
      "key": "e_1_2_6_15_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(95)90080-2"
    },
    {
      "key": "e_1_2_6_16_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/j.molbiopara.2005.09.007"
    },
    {
      "key": "e_1_2_6_17_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S1097-2765(03)00113-8"
    },
    {
      "key": "e_1_2_6_18_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/j.tcb.2004.08.002"
    },
    {
      "key": "e_1_2_6_19_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/j.mib.2007.09.015"
    },
    {
      "key": "e_1_2_6_20_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/44183"
    },
    {
      "key": "e_1_2_6_21_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1462-5822.2006.00778.x"
    },
    {
      "key": "e_1_2_6_22_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/978-0-387-78267-6_9"
    },
    {
      "key": "e_1_2_6_23_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.M207315200"
    },
    {
      "key": "e_1_2_6_24_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.1074553"
    },
    {
      "key": "e_1_2_6_25_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/j.cell.2004.07.019"
    },
    {
      "key": "e_1_2_6_26_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1084/jem.149.1.172"
    },
    {
      "key": "e_1_2_6_27_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/sj.emboj.7601395"
    },
    {
      "key": "e_1_2_6_28_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1371/journal.ppat.0030030"
    },
    {
      "key": "e_1_2_6_29_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1083/jcb.200303023"
    },
    {
      "key": "e_1_2_6_30_1",
      "doi-asserted-by": "crossref",
      "first-page": "895",
      "DOI": "10.1091/mbc.e05-06-0512",
      "article-title": "Unusual kinetic and structural properties control rapid assembly and turnover of actin in the parasite Toxoplasma gondii",
      "volume": "17",
      "author": "Sahoo N.",
      "year": "2005",
      "journal-title": "Mol Biol Cell"
    },
    {
      "key": "e_1_2_6_31_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1083/jcb.126.2.403"
    },
    {
      "key": "e_1_2_6_32_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/j.jmb.2005.03.056"
    },
    {
      "key": "e_1_2_6_33_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/j.pt.2006.02.005"
    },
    {
      "key": "e_1_2_6_34_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1600-0854.2006.00484.x"
    },
    {
      "key": "e_1_2_6_35_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/j.febslet.2004.12.037"
    },
    {
      "key": "e_1_2_6_36_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.1094717"
    },
    {
      "key": "e_1_2_6_37_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1371/journal.ppat.0030195"
    },
    {
      "key": "e_1_2_6_38_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1462-5822.2007.01058.x"
    },
    {
      "key": "e_1_2_6_39_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1023/A:1005329114263"
    },
    {
      "key": "e_1_2_6_40_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0166-6851(98)00044-9"
    },
    {
      "key": "e_1_2_6_41_1",
      "first-page": "317",
      "article-title": "Gene targeting in Plasmodium berghei",
      "volume": "72",
      "author": "Thathy V.",
      "year": "2002",
      "journal-title": "Methods Mol Med"
    },
    {
      "key": "e_1_2_6_42_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.2307/3279102"
    },
    {
      "key": "e_1_2_6_43_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/j.tibs.2004.06.003"
    },
    {
      "key": "e_1_2_6_44_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/(SICI)1097-0169(1999)42:1<73::AID-CM7>3.0.CO;2-Z"
    },
    {
      "key": "e_1_2_6_45_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/emboj/cdg167"
    }
  ],
  "container-title": "Molecular Microbiology",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://api.wiley.com/onlinelibrary/tdm/v1/articles/10.1111%2Fj.1365-2958.2009.06828.x",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "text-mining"
    },
    {
      "URL": "https://onlinelibrary.wiley.com/doi/pdf/10.1111/j.1365-2958.2009.06828.x",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        10,
        14
      ]
    ],
    "date-time": "2023-10-14T10:55:56Z",
    "timestamp": 1697280956000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://onlinelibrary.wiley.com/doi/10.1111/j.1365-2958.2009.06828.x"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2009,
        12
      ]
    ]
  },
  "references-count": 44,
  "journal-issue": {
    "issue": "6",
    "published-print": {
      "date-parts": [
        [
          2009,
          12
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1111/j.1365-2958.2009.06828.x"
  ],
  "URL": "http://dx.doi.org/10.1111/j.1365-2958.2009.06828.x",
  "relation": {},
  "ISSN": [
    "0950-382X",
    "1365-2958"
  ],
  "subject": [],
  "container-title-short": "Molecular Microbiology",
  "published": {
    "date-parts": [
      [
        2009,
        12
      ]
    ]
  }
}