A novel family of apicomplexan glideosome-associated proteins with an inner membrane-anchoring role

Hayley E Bullen, Christopher J. Tonkin, Rebecca A O'Donnell, Wai Hong Tham, Anthony T. Papenfuss, Sven Gould, Alan Frederick Cowman, Brendan S. Crabb, Paul R. Gilson

Research output: Contribution to journalArticleResearchpeer-review

71 Citations (Scopus)

Abstract

The phylum Apicomplexa are a group of obligate intracellular parasites responsible for a wide range of important diseases. Central to the lifecycle of these unicellular parasites is their ability to migrate through animal tissue and invade target host cells. Apicomplexan movement is generated by a unique system of gliding motility in which substrate adhesins and invasion-related proteins are pulled across the plasma membrane by an underlying actin-myosin motor. The myosins of this motor are inserted into a dual membrane layer called the inner membrane complex (IMC) that is sandwiched between the plasma membrane and an underlying cytoskeletal basket. Central to our understanding of gliding motility is the characterization of proteins residing within the IMC, but to date only a few proteins are known. We report here a novel family of six-pass transmembrane proteins, termed the GAPM family, which are highly conserved and specific to Apicomplexa. In Plasmodium falciparum and Toxoplasma gondii the GAPMs localize to the IMC where they form highly SDS-resistant oligomeric complexes. The GAPMs co-purify with the cytoskeletal alveolin proteins and also to some degree with the actin-myosin motor itself. Hence, these proteins are strong candidates for an IMC-anchoring role, either directly or indirectly tethering the motor to the cytoskeleton.

Original languageEnglish
Pages (from-to)25353-25363
Number of pages11
JournalJournal of Biological Chemistry
Volume284
Issue number37
DOIs
Publication statusPublished - 11 Sep 2009
Externally publishedYes

Cite this

Bullen, H. E., Tonkin, C. J., O'Donnell, R. A., Tham, W. H., Papenfuss, A. T., Gould, S., ... Gilson, P. R. (2009). A novel family of apicomplexan glideosome-associated proteins with an inner membrane-anchoring role. Journal of Biological Chemistry, 284(37), 25353-25363. https://doi.org/10.1074/jbc.M109.036772
Bullen, Hayley E ; Tonkin, Christopher J. ; O'Donnell, Rebecca A ; Tham, Wai Hong ; Papenfuss, Anthony T. ; Gould, Sven ; Cowman, Alan Frederick ; Crabb, Brendan S. ; Gilson, Paul R. / A novel family of apicomplexan glideosome-associated proteins with an inner membrane-anchoring role. In: Journal of Biological Chemistry. 2009 ; Vol. 284, No. 37. pp. 25353-25363.
@article{79e66a06c2a64d5ab2f9dd847261bd18,
title = "A novel family of apicomplexan glideosome-associated proteins with an inner membrane-anchoring role",
abstract = "The phylum Apicomplexa are a group of obligate intracellular parasites responsible for a wide range of important diseases. Central to the lifecycle of these unicellular parasites is their ability to migrate through animal tissue and invade target host cells. Apicomplexan movement is generated by a unique system of gliding motility in which substrate adhesins and invasion-related proteins are pulled across the plasma membrane by an underlying actin-myosin motor. The myosins of this motor are inserted into a dual membrane layer called the inner membrane complex (IMC) that is sandwiched between the plasma membrane and an underlying cytoskeletal basket. Central to our understanding of gliding motility is the characterization of proteins residing within the IMC, but to date only a few proteins are known. We report here a novel family of six-pass transmembrane proteins, termed the GAPM family, which are highly conserved and specific to Apicomplexa. In Plasmodium falciparum and Toxoplasma gondii the GAPMs localize to the IMC where they form highly SDS-resistant oligomeric complexes. The GAPMs co-purify with the cytoskeletal alveolin proteins and also to some degree with the actin-myosin motor itself. Hence, these proteins are strong candidates for an IMC-anchoring role, either directly or indirectly tethering the motor to the cytoskeleton.",
author = "Bullen, {Hayley E} and Tonkin, {Christopher J.} and O'Donnell, {Rebecca A} and Tham, {Wai Hong} and Papenfuss, {Anthony T.} and Sven Gould and Cowman, {Alan Frederick} and Crabb, {Brendan S.} and Gilson, {Paul R.}",
year = "2009",
month = "9",
day = "11",
doi = "10.1074/jbc.M109.036772",
language = "English",
volume = "284",
pages = "25353--25363",
journal = "Journal of Biological Chemistry",
issn = "1083-351X",
publisher = "American Society for Biochemistry and Molecular Biology",
number = "37",

}

Bullen, HE, Tonkin, CJ, O'Donnell, RA, Tham, WH, Papenfuss, AT, Gould, S, Cowman, AF, Crabb, BS & Gilson, PR 2009, 'A novel family of apicomplexan glideosome-associated proteins with an inner membrane-anchoring role', Journal of Biological Chemistry, vol. 284, no. 37, pp. 25353-25363. https://doi.org/10.1074/jbc.M109.036772

A novel family of apicomplexan glideosome-associated proteins with an inner membrane-anchoring role. / Bullen, Hayley E; Tonkin, Christopher J.; O'Donnell, Rebecca A; Tham, Wai Hong; Papenfuss, Anthony T.; Gould, Sven; Cowman, Alan Frederick; Crabb, Brendan S.; Gilson, Paul R.

In: Journal of Biological Chemistry, Vol. 284, No. 37, 11.09.2009, p. 25353-25363.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - A novel family of apicomplexan glideosome-associated proteins with an inner membrane-anchoring role

AU - Bullen, Hayley E

AU - Tonkin, Christopher J.

AU - O'Donnell, Rebecca A

AU - Tham, Wai Hong

AU - Papenfuss, Anthony T.

AU - Gould, Sven

AU - Cowman, Alan Frederick

AU - Crabb, Brendan S.

AU - Gilson, Paul R.

PY - 2009/9/11

Y1 - 2009/9/11

N2 - The phylum Apicomplexa are a group of obligate intracellular parasites responsible for a wide range of important diseases. Central to the lifecycle of these unicellular parasites is their ability to migrate through animal tissue and invade target host cells. Apicomplexan movement is generated by a unique system of gliding motility in which substrate adhesins and invasion-related proteins are pulled across the plasma membrane by an underlying actin-myosin motor. The myosins of this motor are inserted into a dual membrane layer called the inner membrane complex (IMC) that is sandwiched between the plasma membrane and an underlying cytoskeletal basket. Central to our understanding of gliding motility is the characterization of proteins residing within the IMC, but to date only a few proteins are known. We report here a novel family of six-pass transmembrane proteins, termed the GAPM family, which are highly conserved and specific to Apicomplexa. In Plasmodium falciparum and Toxoplasma gondii the GAPMs localize to the IMC where they form highly SDS-resistant oligomeric complexes. The GAPMs co-purify with the cytoskeletal alveolin proteins and also to some degree with the actin-myosin motor itself. Hence, these proteins are strong candidates for an IMC-anchoring role, either directly or indirectly tethering the motor to the cytoskeleton.

AB - The phylum Apicomplexa are a group of obligate intracellular parasites responsible for a wide range of important diseases. Central to the lifecycle of these unicellular parasites is their ability to migrate through animal tissue and invade target host cells. Apicomplexan movement is generated by a unique system of gliding motility in which substrate adhesins and invasion-related proteins are pulled across the plasma membrane by an underlying actin-myosin motor. The myosins of this motor are inserted into a dual membrane layer called the inner membrane complex (IMC) that is sandwiched between the plasma membrane and an underlying cytoskeletal basket. Central to our understanding of gliding motility is the characterization of proteins residing within the IMC, but to date only a few proteins are known. We report here a novel family of six-pass transmembrane proteins, termed the GAPM family, which are highly conserved and specific to Apicomplexa. In Plasmodium falciparum and Toxoplasma gondii the GAPMs localize to the IMC where they form highly SDS-resistant oligomeric complexes. The GAPMs co-purify with the cytoskeletal alveolin proteins and also to some degree with the actin-myosin motor itself. Hence, these proteins are strong candidates for an IMC-anchoring role, either directly or indirectly tethering the motor to the cytoskeleton.

UR - http://www.scopus.com/inward/record.url?scp=69949148305&partnerID=8YFLogxK

U2 - 10.1074/jbc.M109.036772

DO - 10.1074/jbc.M109.036772

M3 - Article

VL - 284

SP - 25353

EP - 25363

JO - Journal of Biological Chemistry

JF - Journal of Biological Chemistry

SN - 1083-351X

IS - 37

ER -