Professor Richard McCulloch
- Professor (Parasitology)
telephone:
01413305946
email:
Richard.McCulloch@glasgow.ac.uk
RB618 Level B6, Iii - Gbrc, 120 University Place, Glasgow G12 8TA
Research interests
Current Research: DNA recombination, replication, repair and antigenic variation in trypanosomatid parasites
DNA recombination, replication and repair are central to the functioning and propagation of all organisms, maintaining genome stability for growth and reproduction. Homologous recombination, one of a number of repair pathways in cells, functions in repair of DNA double strand breaks, a severe form of genome damage, and ensures completion of DNA replication. In African trypanosomes, homologous recombination also plays a pivotal role in antigenic variation, a survival strategy that relies on changes in surface antigens (Variant Surface Glycoproteins), allowing host immune response evasion and infection of partially immune hosts. This is a hugely elaborate system, involving expression of a single VSG gene from >1000 silent copies in the genome. We are exploring how homologous recombination and other DNA repair pathways operate in trypanosomes and influence antigenic variation. In addition, we are characterising the process of nuclear DNA replication, which not only appears unusual in this parasite but, remarkably, also influences antigenic variation. Ongoing projects are examining homologous recombination in response to induced DNA double strand breaks, in characterising the machinery and timing of nuclear replication, examining the role of excision repair pathways in mitochondrial and nuclear genome stability, elucidating the DNA damage response in T. brucei, and in the enzymatic machinery and initiation of VSG switching throughout T. brucei chronic infections.
Publications
2024
Reis-Cunha, J. L., Pimenta-Carvalho, S. A., Almeida, L. V., Coqueiro-Dos-Santos, A., Marques, C. A. , Black, J. A., Damasceno, J. , McCulloch, R. , Bartholomeu, D. C. and Jeffares, D. C. (2024) Ancestral aneuploidy and stable chromosomal duplication resulting in differential genome structure and gene expression control in trypanosomatid parasites. Genome Research, 34(3), pp. 441-453. (doi: 10.1101/gr.278550.123) (PMID:38604731) (PMCID:PMC11067883)
2023
Girasol, M. J. et al. (2023) RAD51-mediated R-loop formation acts to repair transcription associated DNA breaks driving antigenic variation in Trypanosoma brucei. Proceedings of the National Academy of Sciences of the United States of America, 120(48), e230930612. (doi: 10.1073/pnas.2309306120) (PMID:37988471) (PMCID:PMC10691351)
Girasol, M. J., Briggs, E., Marques, C. A. , Batista, J. M., Beraldi, D., Buchmore, R., Lemgruber, L. and McCulloch, R. (2023) Immunoprecipitation of RNA-DNA hybrid interacting proteins in Trypanosoma brucei reveals conserved and novel activities, including in the control of surface antigen expression needed for immune evasion by antigenic variation. Nucleic Acids Research, 51(20), pp. 11123-11141. (doi: 10.1093/nar/gkad836) (PMID:37843098) (PMCID:PMC10639054)
Black, J. A., Klinger, C. M., Lemgruber, L. , Dacks, J. B., Mottram, J. C. and McCulloch, R. (2023) AAK1-like: a putative pseudokinase with potential roles in cargo uptake in bloodstream form Trypanosoma brucei parasites. Journal of Eukaryotic Microbiology, 70(6), e12994. (doi: 10.1111/jeu.12994) (PMID:37548427)
2022
Faria, J., Briggs, E. M., Black, J. A. and McCulloch, R. (2022) Emergence and adaptation of the cellular machinery directing antigenic variation in the African trypanosome. Current Opinion in Microbiology, 70, 102209. (doi: 10.1016/j.mib.2022.102209) (PMID:36215868)
da Silva, M. S., McCulloch, R. and Cano, M. I. N. (2022) Editorial: Nuclear genome stability: DNA replication, telomere maintenance, and DNA repair. Frontiers in Cell and Developmental Biology, 10, 875749. (doi: 10.3389/fcell.2022.875749) (PMID:35359435) (PMCID:PMC8961442)
2021
Briggs, E. M., Rojas, F., McCulloch, R. , Matthews, K. R. and Otto, T. D. (2021) Single-cell transcriptomic analysis of bloodstream Trypanosoma brucei reconstructs cell cycle progression and developmental quorum sensing. Nature Communications, 12, 5268. (doi: 10.1038/s41467-021-25607-2) (PMID:34489460) (PMCID:PMC8421343)
Briggs, E. M., Warren, F. S.L., Matthews, K. R., McCulloch, R. and Otto, T. D. (2021) Application of single cell transcriptomics to kinetoplastid research. Parasitology, 148(10), pp. 1223-1236. (doi: 10.1017/S003118202100041X) (PMID:33678213) (PMCID:PMC8311972)
Silva, G. L.A., Tosi, L. R.O., McCulloch, R. and Black, J. A. (2021) Unpicking the roles of DNA damage protein kinases in trypanosomatids. Frontiers in Cell and Developmental Biology, 9, 636615. (doi: 10.3389/fcell.2021.636615) (PMID:34422791) (PMCID:PMC8377203)
Damasceno, J. D. , Marques, C. A., Black, J., Briggs, E. and McCulloch, R. (2021) Read, write, adapt: challenges and opportunities during kinetoplastid genome replication. Trends in Genetics, 37(1), pp. 21-34. (doi: 10.1016/j.tig.2020.09.002) (PMID:32993968) (PMCID:PMC9213392)
2020
Saldivia, M. et al. (2020) Targeting the trypanosome kinetochore with CLK1 protein kinase inhibitors. Nature Microbiology, 5(10), pp. 1207-1216. (doi: 10.1038/s41564-020-0745-6) (PMID:32661312) (PMCID:PMC7610364)
Damasceno, J. D. , Marques, C. A. , Beraldi, D., Crouch, K. , Lapsley, C., Obonaga, R., Tosi, L. R.O. and McCulloch, R. (2020) Genome duplication in Leishmania major relies on persistent subtelomeric DNA replication. eLife, 9, e58030. (doi: 10.7554/eLife.58030) (PMID:32897188) (PMCID:PMC7511235)
Damasceno, J. D. , Reis-Cunha, J., Crouch, K. , Beraldi, D., Lapsley, C., Tosi, L. R.O., Bartholomeu, D. and McCulloch, R. (2020) Conditional knockout of RAD51-related genes in Leishmania major reveals a critical role for homologous recombination during genome replication. PLoS Genetics, 16(7), e1008828. (doi: 10.1371/journal.pgen.1008828) (PMID:32609721) (PMCID:PMC7360064)
de Araujo, C. B. et al. (2020) Replication origin location might contribute to genetic variability in Trypanosoma cruzi. BMC Genomics, 21, 414. (doi: 10.1186/s12864-020-06803-8) (PMID:32571205) (PMCID:PMC7310030)
Grazielle-Silva, V., Zeb, T. F., Machado, C. R., McCulloch, R. and Teixeira, S. M. R. (2020) Trypanosoma brucei and Trypanosoma cruzi DNA mismatch repair proteins act differently in the response to DNA damage caused by oxidative stress. Frontiers in Cellular and Infection Microbiology, 10, 154. (doi: 10.3389/fcimb.2020.00154) (PMID:32373549) (PMCID:PMC7176904)
Briggs, E. M., Marques, C. A., Reis-Cunha, J., Black, J., Campbell, S., Damasceno, J. , Bartholomeu, D., Crouch, K. and McCulloch, R. (2020) Next-generation analysis of trypanosomatid genome stability and instability. In: Michels, P. A.M., Ginger, M. L. and Zilberstein, D. (eds.) Trypanosomatids: Methods and Protocols. Series: Methods in Molecular Biology (2116). Springer, pp. 225-262. ISBN 9781071602935 (doi: 10.1007/978-1-0716-0294-2_15)
Black, J. A., Crouch, K. , Lemgruber, L. , Lapsley, C., Dickens, N. , Tosi, L. R.O., Mottram, J. C. and McCulloch, R. (2020) Trypanosoma brucei ATR links DNA damage signalling during antigenic variation with regulation of RNA Polymerase I-transcribed surface antigens. Cell Reports, 30(3), 836-851.e5. (doi: 10.1016/j.celrep.2019.12.049) (PMID:31968257) (PMCID:PMC6988115)
2019
da Silva, M. S. et al. (2019) Transcription activity contributes to the firing of non-constitutive origins in African trypanosomes helping to maintain robustness in S-phase duration. Scientific Reports, 9, 18512. (doi: 10.1038/s41598-019-54366-w) (PMID:31811174) (PMCID:PMC6898680)
Briggs, E., Crouch, K. , Lemgruber Soares, L. , Hamilton, G., Lapsley, C. and McCulloch, R. (2019) Trypanosoma brucei ribonuclease H2A is an essential R-loop processing enzyme whose loss causes DNA damage during transcription initiation and antigenic variation. Nucleic Acids Research, 47(17), pp. 9180-9197. (doi: 10.1093/nar/gkz644) (PMID:31350892) (PMCID:PMC6753483)
Nenarokova, A., Záhonová, K., Krasilnikova, M., Gahura, O., McCulloch, R. , Zíková, A., Yurchenko, V. and Lukeš, J. (2019) Causes and effects of loss of classical non-homologous end joining pathway in parasitic eukaryotes. mBio, 10(4), e01541-9. (doi: 10.1128/mBio.01541-19) (PMID:31311886) (PMCID:PMC6635534)
Jayaraman, S. et al. (2019) Application of long read sequencing to determine expressed antigen diversity in Trypanosoma brucei infections. PLoS Neglected Tropical Diseases, 13(4), e0007262. (doi: 10.1371/journal.pntd.0007262) (PMID:30943202) (PMCID:PMC6464242)
Vieira Da Rocha, J.P., Passos-Silva, D.G., Mendes, I.C., Rocha, E.A., Gomes, D.A., Machado, C.R. and McCulloch, R. (2019) The DNA damage response is developmentally regulated in the African trypanosome. DNA Repair, 73, pp. 78-90. (doi: 10.1016/j.dnarep.2018.11.005) (PMID:30470509) (PMCID:PMC6329875)
2018
Briggs, E., Hamilton, G., Crouch, K. , Lapsley, C. and McCulloch, R. (2018) Genome-wide mapping reveals conserved and diverged R-loop activities in the unusual genetic landscape of the African trypanosome genome. Nucleic Acids Research, 46(22), pp. 11789-11805. (doi: 10.1093/nar/gky928) (PMID:30304482) (PMCID:PMC6294496)
Damasceno, J. D. , Obonaga, R., Silva, G. L.A., Reis-Cunha, J. L., Duncan, S. M., Bartholomeu, D. C., Mottram, J. C. , McCulloch, R. and Tosi, L. R.O. (2018) Conditional genome engineering reveals canonical and divergent roles for the Hus1 component of the 9-1-1 complex in the maintenance of the plastic genome of Leishmania. Nucleic Acids Research, 46(22), pp. 11835-11846. (doi: 10.1093/nar/gky1017) (PMID:30380080) (PMCID:PMC6294564)
Briggs, E., Crouch, K. , Lemgruber, L. , Lapsley, C. and McCulloch, R. (2018) Ribonuclease H1-targeted R-loops in surface antigen gene expression sites can direct trypanosome immune evasion. PLoS Genetics, 14(12), e1007729. (doi: 10.1371/journal.pgen.1007729) (PMID:30543624) (PMCID:PMC6292569)
Santos da Silva, M., Hovel-Miner, G. A., Briggs, E. M., Elias, M. C. and McCulloch, R. (2018) Evaluation of mechanisms that may generate DNA lesions triggering antigenic variation in African trypanosomes. PLoS Pathogens, 14(11), e1007321. (doi: 10.1371/journal.ppat.1007321) (PMID:30440029) (PMCID:PMC6237402)
Gomes Passos Silva, D. et al. (2018) The in vivo and in vitro roles of Trypanosoma cruzi Rad51 in the repair of DNA double strand breaks and oxidative lesions. PLoS Neglected Tropical Diseases, 12(11), e0006875. (doi: 10.1371/journal.pntd.0006875) (PMID:30422982) (PMCID:PMC6258567)
Marques, C. A. and McCulloch, R. (2018) Conservation and variation in strategies for DNA replication of kinetoplastid nuclear genomes. Current Genomics, 19(2), pp. 98-109. (doi: 10.2174/1389202918666170815144627) (PMID:29491738) (PMCID:PMC5814967)
Almeida, L. V., Coqueiro-Dos-Santos, A., Rodriguez-Luiz, G. F., McCulloch, R. , Bartholomeu, D. C. and Reis-Cunha, J. L. (2018) Chromosomal copy number variation analysis by next generation sequencing confirms ploidy stability in Trypanosoma brucei subspecies. Microbial Genomics, 4(10), e000223. (doi: 10.1099/mgen.0.000223) (PMID:30256189) (PMCID:PMC6249438)
2017
McCulloch, R. , Cobbold, C. A. , Figueiredo, L., Jackson, A., Morrison, L. J., Mugnier, M. R., Papavasiliou, N., Schnaufer, A. and Matthews, K. (2017) Emerging challenges in understanding trypanosome antigenic variation. Emerging Topics in Life Sciences, 1(6), pp. 585-592. (doi: 10.1042/ETLS20170104) (PMID:30271884) (PMCID:PMC6162063)
da Silva, M. S., Pavani, R. S., Damasceno, J. D. , Marques, C. A. , McCulloch, R. , Tosi, L. R. O. and Elias, M. C. (2017) Nuclear DNA replication in trypanosomatids: there are no easy methods for solving difficult problems. Trends in Parasitology, 33(11), pp. 858-874. (doi: 10.1016/j.pt.2017.08.002) (PMID:28844718) (PMCID:PMC5662062)
Stortz, J. A. et al. (2017) Genome-wide and protein kinase-focused RNAi screens reveal conserved and novel damage response pathways in Trypanosoma brucei. PLoS Pathogens, 13(7), e1006477. (doi: 10.1371/journal.ppat.1006477) (PMID:28742144) (PMCID:PMC5542689)
Fernandez-Cortes, F., Serafim, T. D., Wilkes, J. M. , Jones, N. G., Ritchie, R., McCulloch, R. and Mottram, J. C. (2017) RNAi screening identifies Trypanosoma brucei stress response protein kinases required for survival in the mouse. Scientific Reports, 7, 6156. (doi: 10.1038/s41598-017-06501-8) (PMID:28733613) (PMCID:PMC5522463)
Devlin, R., Marques, C. A. and McCulloch, R. (2017) Does DNA replication direct locus-specific recombination during host immune evasion by antigenic variation in the African trypanosome? Current Genetics, 63(3), pp. 441-449. (doi: 10.1007/s00294-016-0662-7) (PMID:27822899) (PMCID:PMC5422504)
Cabrera, G., Silva, V. G., Mendes, I. C., Machado, C. R. and McCulloch, R. (2017) Genome maintenance in Trypanosomatids. In: Santos da Silva, M. and Cano, M. I. N. (eds.) Molecular and Cellular Biology of Pathogenic Trypanosomatids. Series: Frontiers in parasitology, 1. Bentham Science, pp. 195-260. ISBN 9781681084060 (doi: 10.2174/9781681084053117010008)
2016
Biéler, S. et al. (2016) Evaluation of antigens for development of a serological test for human African trypanosomiasis. PLoS ONE, 11(12), e0168074. (doi: 10.1371/journal.pone.0168074) (PMID:27936225) (PMCID:PMC5148118)
Marques, C. A. , Tiengwe, C., Lemgruber Soares, L. , Damasceno, J. D., Scott, A., Paape, D. , Marcello, L. and McCulloch, R. (2016) Diverged composition and regulation of the Trypanosoma brucei origin recognition complex that mediates DNA replication initiation. Nucleic Acids Research, 44(10), pp. 4763-4784. (doi: 10.1093/nar/gkw147) (PMID:26951375) (PMCID:PMC4889932)
Damasceno, J. D., Obonaga, R., Santos, E. V., Scott, A., McCulloch, R. and Tosi, L. R.O. (2016) Functional compartmentalization of Rad9 and Hus1 reveals diverse assembly of the 9-1-1 complex components during the DNA damage response in Leishmania. Molecular Microbiology, 101(6), pp. 1054-1068. (doi: 10.1111/mmi.13441) (PMID:27301589) (PMCID:PMC5453112)
McCulloch, R. and Navarro, M. (2016) The protozoan nucleus. Molecular and Biochemical Parasitology, 209(1-2), pp. 76-87. (doi: 10.1016/j.molbiopara.2016.05.002) (PMID:27181562)
Devlin, R., Marques, C. A. , Paape, D. , Prorocic, M., Zurita-Leal, A. C., Campbell, S. J., Lapsley, C., Dickens, N. and McCulloch, R. (2016) Mapping replication dynamics in Trypanosoma brucei reveals a link with telomere transcription and antigenic variation. eLife, 5, e12765. (doi: 10.7554/eLife.12765) (PMID:27228154) (PMCID:PMC4946898)
2015
Rodenko, B., Wanner, M., Alkhaldi, A., Ebiloma, G., Barnes, R., Kaiser, M., Brun, R., McCulloch, R. , Koomen, G.-J. and De Koning, H. P. (2015) Targeting the parasite's DNA with methyltriazenyl purine analogs Is a safe, selective, and efficacious antitrypanosomal strategy. Antimicrobial Agents and Chemotherapy, 59(11), pp. 6708-6716. (doi: 10.1128/aac.00596-15) (PMID:26282430) (PMCID:PMC4604408)
Marques, C. A. , Dickens, N. J. , Paape, D. , Campbell, S. J. and McCulloch, R. (2015) Genome-wide mapping reveals single-origin chromosome replication in Leishmania, a eukaryotic microbe. Genome Biology, 16, 230. (doi: 10.1186/s13059-015-0788-9) (PMID:26481451) (PMCID:PMC4612428)
Matthews, K. R., McCulloch, R. and Morrison, L. J. (2015) The within-host dynamics of African trypanosome infections. Philosophical Transactions of the Royal Society B: Biological Sciences, 370(1675), 20140288. (doi: 10.1098/rstb.2014.0288) (PMID:26150654) (PMCID:PMC4528486)
McCulloch, R. and Field, M. C. (2015) Quantitative sequencing confirms VSG diversity as central to immune evasion by Trypanosoma brucei. Trends in Parasitology, 31(8), pp. 346-349. (doi: 10.1016/j.pt.2015.05.001) (PMID:25999027)
Grazielle-Silva, V., Zeb, T.F., Bolderson, J., Campos, P.C., Miranda, J.B., Alves, C.L., Machado, C.R., McCulloch, R. and Teixeira, S.M. R. (2015) Distinct phenotypes caused by mutation of MSH2 in trypanosome insect and mammalian life cycle forms are associated with parasite adaptation to oxidative stress. PLoS Neglected Tropical Diseases, 9(6), e0003870. (doi: 10.1371/journal.pntd.0003870) (PMID:26083967) (PMCID:PMC4470938)
Dagnachew, S., Terefe, G., Abebe, G., Barry, D., McCulloch, R. and Goddeeris, B. (2015) In vivo experimental drug resistance study in Trypanosoma vivax isolates from tsetse infested and non-tsetse infested areas of Northwest Ethiopia. Acta Tropica, 146, pp. 95-100. (doi: 10.1016/j.actatropica.2015.03.014) (PMID:25792418)
Calderano, S.G., Drosopoulos, W.C., Quaresma, M. M., Marques, C.A. , Kosiyatrakul, S., McCulloch, R. , Schildkraut, C.L. and Elias, M.C. (2015) Single molecule analysis of Trypanosoma brucei DNA replication dynamics. Nucleic Acids Research, 43(5), pp. 2655-2665. (doi: 10.1093/nar/gku1389) (PMID:25690894) (PMCID:PMC4357695)
McCulloch, R. , Morrison, L. J. and Hall, J. P.J. (2015) DNA recombination strategies during antigenic variation in the African Trypanosome. In: Craig, N. L., Chandler, M., Gellert, M., Lambowitz, A. M., Rice, P. A. and Sandmeyer, S. B. (eds.) Mobile DNA III. ASM Press: Washington, DC, pp. 409-435. ISBN 9781555819200 (doi: 10.1128/microbiolspec.MDNA3-0016-2014)
2014
Machado, C. R. et al. (2014) Nucleotide excision repair in Trypanosoma brucei: specialization of transcription-coupled repair due to multigenic transcription. Molecular Microbiology, 92(4), pp. 756-776. (doi: 10.1111/mmi.12589) (PMID:24661334) (PMCID:PMC4138998)
Tiengwe, C., Marques, C. A. and McCulloch, R. (2014) Nuclear DNA replication initiation in kinetoplastid parasites: new insights into an ancient process. Trends in Parasitology, 30(1), pp. 27-36. (doi: 10.1016/j.pt.2013.10.009)
2013
Trenaman, A., Hartley, C., Prorocic, M., Passos-Silva, D. G., van den Hoek, M., Nechyporuk-Zloy, V., Machado, C. R. and McCulloch, R. (2013) Trypanosoma brucei BRCA2 acts in a life cycle-specific genome stability process and dictates BRC repeat number-dependent RAD51 subnuclear dynamics. Nucleic Acids Research, 41(2), pp. 943-960. (doi: 10.1093/nar/gks1192)
2012
Tiengwe, C. et al. (2012) Genome-wide analysis reveals extensive functional interaction between DNA replication initiation and transcription in the genome of trypanosoma brucei. Cell Reports, 2(1), pp. 185-197. (doi: 10.1016/j.celrep.2012.06.007)
Tiengwe, C., Marcello, L., Farr, H., Gadelha, C., Burchmore, R. , Barry, J.D., Bell, S.D. and McCulloch, R. (2012) Identification of ORC1/CDC6-interacting factors in trypanosoma brucei reveals critical features of origin recognition complex architecture. PLoS ONE, 7(3), e32674. (doi: 10.1371/journal.pone.0032674) (PMID:22412905) (PMCID:PMC3297607)
2011
Dobson, R., Stockdale, C., Lapsley, C., Wilkes, J. and McCulloch, R. (2011) Interactions among Trypanosoma brucei RAD51 paralogues in DNA repair and antigenic variation. Molecular Microbiology, 81(2), pp. 434-456. (doi: 10.1111/j.1365-2958.2011.07703.x)
2010
Horn, D. and McCulloch, R. (2010) Molecular mechanisms underlying the control of antigenic variation in African trypanosomes. Current Opinion in Microbiology, 13(6), pp. 700-705. (doi: 10.1016/j.mib.2010.08.009)
2009
Morrison, L. J., Marcello, L. and McCulloch, R. (2009) Antigenic variation in the African trypanosome: molecular mechanisms and phenotypic complexity. Cellular Microbiology, 11(12), pp. 1724-1734. (doi: 10.1111/j.1462-5822.2009.01383.x)
McCulloch, R. and Horn, D. (2009) What has DNA sequencing revealed about the VSG expression sites of African trypanosomes? Trends in Parasitology, 25(8), pp. 359-363. (doi: 10.1016/j.pt.2009.05.007)
2008
Stockdale, C., Swiderski, M. R., Barry, J. D. and McCulloch, R. (2008) Antigenic variation in Trypanosoma brucei: joining the DOTs. PLoS Biology, 6(7), e185. (doi: 10.1371/journal.pbio.0060185)
Hartley, C. L. and McCulloch, R. (2008) Trypanosoma brucei BRCA2 acts in antigenic variation and has undergone a recent expansion in BRC repeat number that is important during homologous recombination. Molecular Microbiology, 68(5), pp. 1237-1251. (doi: 10.1111/j.1365-2958.2008.06230.x)
Glover, L., McCulloch, R. and Horn, D. (2008) Sequence homology and microhomology dominate chromosomal double-strand break repair in African trypanosomes. Nucleic Acids Research, 36(8), pp. 2608-2618. (doi: 10.1093/nar/gkn104)
Machado-Silva, A., Teixeira, S. M.R., Franco, G. R., Macedo, A. M., Pena, S. D.J., McCulloch, R. and Machado, C. R. (2008) Mismatch repair in Trypanosoma brucei: Heterologous expression of MSH2 from Trypanosoma cruzi provides new insights into the response to oxidative damage. Gene, 411(1-2), pp. 19-26. (doi: 10.1016/j.gene.2007.12.021)
2007
Burton, P., McBride, D. J., Wilkes, J. M., Barry, J. D. and McCulloch, R. (2007) Ku heterodimer-independent end joining in Trypanosoma brucei cell extracts relies upon sequence microhomology. Eukaryotic Cell, 6(10), pp. 1773-1781. (doi: 10.1128/EC.00212-07)
Barnes, R. L. and McCulloch, R. (2007) Trypanosoma brucei homologous recombination is dependent on substrate length and homology, though displays a differential dependence on mismatch repair as substrate length decreases. Nucleic Acids Research, 35(10), pp. 3478-3493. (doi: 10.1093/nar/gkm249)
2006
Machado, C.R., Augusto-Pinto, L., McCulloch, R. and Teixeira, S.M.R. (2006) DNA metabolism and genetic diversity in Trypanosomes. Mutation Research-Reviews in Mutation Research, 612, pp. 40-57. (doi: 10.1016/j.mrrev.2005.05.001)
Proudfoot, C. and McCulloch, R. (2006) Trypanosoma brucei DMC1 does not act in DNA recombination, repair or antigenic variation in bloodstream stage cells. Molecular and Biochemical Parasitology, 145, pp. 245-253. (doi: 10.1016/j.molbiopara.2005.10.007)
2005
El-Sayed, N.M. et al. (2005) The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science, 309(5733), pp. 409-415. (doi: 10.1126/science.1112631)
Proudfoot, C. and McCulloch, R. (2005) Distinct roles for two RAD51-related genes in Trypanosoma brucei antigenic variation. Nucleic Acids Research, 33, pp. 6906-6919. (doi: 10.1093/nar/gki)
2004
Bell, J., Harvey, T., Sims, A. and McCulloch, R. (2004) Characterization of components of the mismatch repair machinery in Trypanosoma brucei. Molecular Microbiology, 51, pp. 159-173. (doi: 10.1046/j.1365-2958.2003.03804.x)
McCulloch, R. (2004) Antigenic variation in African trypanosomes: monitoring progress. Trends in Parasitology, 20, pp. 117-121.
McCulloch, R., Vassella, E., Burton, P., Boshart, M. and Barry, J.D. (2004) Transformation of monomorphic and pleomorphic Trypanosoma brucei. Methods in Molecular Biology, 262(1), pp. 53-86. (doi: 10.1385/1592597610)
2003
Barry, J., Ginger, M., Burton, P. and McCulloch, R. (2003) Why are parasite contingency genes often associated with telomeres? International Journal for Parasitology, 33, pp. 29-45. (doi: 10.1016/S0020-7519(02)00247-3)
Bell, J. and McCulloch, R. (2003) Mismatch repair regulates homologous recombination, but has little influence on antigenic variation, in Trypanosoma brucei. Journal of Biological Chemistry, 278, pp. 45182-45188. (doi: 10.1074/jbc.M308123200)
2002
Conway, C., McCulloch, R., Ginger, M., Robinson, N., Browitt, A. and Barry, J. (2002) Ku is important for telomere maintenance, but not for differential expression of telomeric VSG genes, in African trypanosomes. Journal of Biological Chemistry, 277, pp. 21269-21277. (doi: 10.1074/jbc.M200550200)
Conway, C., Proudfoot, C., Burton, P., Barry, J. and McCulloch, R. (2002) Two pathways of homologous recombination in Trypanosoma brucei. Molecular Microbiology, 45, pp. 1687-1700.
Robinson, N., McCulloch, R., Conway, C., Browitt, A. and Barry, J. (2002) Inactivation of Mre11 does not affect VSG gene duplication mediated by homologous recombination in Trypanosoma brucei. Journal of Biological Chemistry, 277, pp. 26185-26193. (doi: 10.1074/jbc.M203205200)
2001
Barry, J. and McCulloch, R. (2001) Antigenic variation in trypanosomes: Enhanced phenotypic variation in a eukaryotic parasite. Advances in Parasitology, 49, pp. 1-70.
Vanhamme, L., Pays, E., McCulloch, R. and Barry, J. (2001) An update on antigenic variation in African trypanosomes. Trends in Parasitology, 17, pp. 338-343.
1993
Blakely, G., May, G. , McCulloch, R. , Arciszewska, L. K., Burke, M., Lovett, S. T. and Sherratt, D. J. (1993) Two related recombinases are required for site-specific recombination at dif and cer in E. coli K12. Cell, 75(2), pp. 351-61. (doi: 10.1016/0092-8674(93)80076-Q) (PMID:8402918)
Sherratt, D., Blakely, G., Burke, M., Colloms, S. , Leslie, N., McCulloch, R. , May, G. and Roberts, J. (1993) Site-specific recombination and the partition of bacterial chromosomes. In: Heslop-Harrison, J. and Flavell, R. (eds.) The Chromosome. BIOS Scientific Publishers: Oxford, pp. 25-41. ISBN 1872748325
Articles
Reis-Cunha, J. L., Pimenta-Carvalho, S. A., Almeida, L. V., Coqueiro-Dos-Santos, A., Marques, C. A. , Black, J. A., Damasceno, J. , McCulloch, R. , Bartholomeu, D. C. and Jeffares, D. C. (2024) Ancestral aneuploidy and stable chromosomal duplication resulting in differential genome structure and gene expression control in trypanosomatid parasites. Genome Research, 34(3), pp. 441-453. (doi: 10.1101/gr.278550.123) (PMID:38604731) (PMCID:PMC11067883)
Girasol, M. J. et al. (2023) RAD51-mediated R-loop formation acts to repair transcription associated DNA breaks driving antigenic variation in Trypanosoma brucei. Proceedings of the National Academy of Sciences of the United States of America, 120(48), e230930612. (doi: 10.1073/pnas.2309306120) (PMID:37988471) (PMCID:PMC10691351)
Girasol, M. J., Briggs, E., Marques, C. A. , Batista, J. M., Beraldi, D., Buchmore, R., Lemgruber, L. and McCulloch, R. (2023) Immunoprecipitation of RNA-DNA hybrid interacting proteins in Trypanosoma brucei reveals conserved and novel activities, including in the control of surface antigen expression needed for immune evasion by antigenic variation. Nucleic Acids Research, 51(20), pp. 11123-11141. (doi: 10.1093/nar/gkad836) (PMID:37843098) (PMCID:PMC10639054)
Black, J. A., Klinger, C. M., Lemgruber, L. , Dacks, J. B., Mottram, J. C. and McCulloch, R. (2023) AAK1-like: a putative pseudokinase with potential roles in cargo uptake in bloodstream form Trypanosoma brucei parasites. Journal of Eukaryotic Microbiology, 70(6), e12994. (doi: 10.1111/jeu.12994) (PMID:37548427)
Faria, J., Briggs, E. M., Black, J. A. and McCulloch, R. (2022) Emergence and adaptation of the cellular machinery directing antigenic variation in the African trypanosome. Current Opinion in Microbiology, 70, 102209. (doi: 10.1016/j.mib.2022.102209) (PMID:36215868)
da Silva, M. S., McCulloch, R. and Cano, M. I. N. (2022) Editorial: Nuclear genome stability: DNA replication, telomere maintenance, and DNA repair. Frontiers in Cell and Developmental Biology, 10, 875749. (doi: 10.3389/fcell.2022.875749) (PMID:35359435) (PMCID:PMC8961442)
Briggs, E. M., Rojas, F., McCulloch, R. , Matthews, K. R. and Otto, T. D. (2021) Single-cell transcriptomic analysis of bloodstream Trypanosoma brucei reconstructs cell cycle progression and developmental quorum sensing. Nature Communications, 12, 5268. (doi: 10.1038/s41467-021-25607-2) (PMID:34489460) (PMCID:PMC8421343)
Briggs, E. M., Warren, F. S.L., Matthews, K. R., McCulloch, R. and Otto, T. D. (2021) Application of single cell transcriptomics to kinetoplastid research. Parasitology, 148(10), pp. 1223-1236. (doi: 10.1017/S003118202100041X) (PMID:33678213) (PMCID:PMC8311972)
Silva, G. L.A., Tosi, L. R.O., McCulloch, R. and Black, J. A. (2021) Unpicking the roles of DNA damage protein kinases in trypanosomatids. Frontiers in Cell and Developmental Biology, 9, 636615. (doi: 10.3389/fcell.2021.636615) (PMID:34422791) (PMCID:PMC8377203)
Damasceno, J. D. , Marques, C. A., Black, J., Briggs, E. and McCulloch, R. (2021) Read, write, adapt: challenges and opportunities during kinetoplastid genome replication. Trends in Genetics, 37(1), pp. 21-34. (doi: 10.1016/j.tig.2020.09.002) (PMID:32993968) (PMCID:PMC9213392)
Saldivia, M. et al. (2020) Targeting the trypanosome kinetochore with CLK1 protein kinase inhibitors. Nature Microbiology, 5(10), pp. 1207-1216. (doi: 10.1038/s41564-020-0745-6) (PMID:32661312) (PMCID:PMC7610364)
Damasceno, J. D. , Marques, C. A. , Beraldi, D., Crouch, K. , Lapsley, C., Obonaga, R., Tosi, L. R.O. and McCulloch, R. (2020) Genome duplication in Leishmania major relies on persistent subtelomeric DNA replication. eLife, 9, e58030. (doi: 10.7554/eLife.58030) (PMID:32897188) (PMCID:PMC7511235)
Damasceno, J. D. , Reis-Cunha, J., Crouch, K. , Beraldi, D., Lapsley, C., Tosi, L. R.O., Bartholomeu, D. and McCulloch, R. (2020) Conditional knockout of RAD51-related genes in Leishmania major reveals a critical role for homologous recombination during genome replication. PLoS Genetics, 16(7), e1008828. (doi: 10.1371/journal.pgen.1008828) (PMID:32609721) (PMCID:PMC7360064)
de Araujo, C. B. et al. (2020) Replication origin location might contribute to genetic variability in Trypanosoma cruzi. BMC Genomics, 21, 414. (doi: 10.1186/s12864-020-06803-8) (PMID:32571205) (PMCID:PMC7310030)
Grazielle-Silva, V., Zeb, T. F., Machado, C. R., McCulloch, R. and Teixeira, S. M. R. (2020) Trypanosoma brucei and Trypanosoma cruzi DNA mismatch repair proteins act differently in the response to DNA damage caused by oxidative stress. Frontiers in Cellular and Infection Microbiology, 10, 154. (doi: 10.3389/fcimb.2020.00154) (PMID:32373549) (PMCID:PMC7176904)
Black, J. A., Crouch, K. , Lemgruber, L. , Lapsley, C., Dickens, N. , Tosi, L. R.O., Mottram, J. C. and McCulloch, R. (2020) Trypanosoma brucei ATR links DNA damage signalling during antigenic variation with regulation of RNA Polymerase I-transcribed surface antigens. Cell Reports, 30(3), 836-851.e5. (doi: 10.1016/j.celrep.2019.12.049) (PMID:31968257) (PMCID:PMC6988115)
da Silva, M. S. et al. (2019) Transcription activity contributes to the firing of non-constitutive origins in African trypanosomes helping to maintain robustness in S-phase duration. Scientific Reports, 9, 18512. (doi: 10.1038/s41598-019-54366-w) (PMID:31811174) (PMCID:PMC6898680)
Briggs, E., Crouch, K. , Lemgruber Soares, L. , Hamilton, G., Lapsley, C. and McCulloch, R. (2019) Trypanosoma brucei ribonuclease H2A is an essential R-loop processing enzyme whose loss causes DNA damage during transcription initiation and antigenic variation. Nucleic Acids Research, 47(17), pp. 9180-9197. (doi: 10.1093/nar/gkz644) (PMID:31350892) (PMCID:PMC6753483)
Nenarokova, A., Záhonová, K., Krasilnikova, M., Gahura, O., McCulloch, R. , Zíková, A., Yurchenko, V. and Lukeš, J. (2019) Causes and effects of loss of classical non-homologous end joining pathway in parasitic eukaryotes. mBio, 10(4), e01541-9. (doi: 10.1128/mBio.01541-19) (PMID:31311886) (PMCID:PMC6635534)
Jayaraman, S. et al. (2019) Application of long read sequencing to determine expressed antigen diversity in Trypanosoma brucei infections. PLoS Neglected Tropical Diseases, 13(4), e0007262. (doi: 10.1371/journal.pntd.0007262) (PMID:30943202) (PMCID:PMC6464242)
Vieira Da Rocha, J.P., Passos-Silva, D.G., Mendes, I.C., Rocha, E.A., Gomes, D.A., Machado, C.R. and McCulloch, R. (2019) The DNA damage response is developmentally regulated in the African trypanosome. DNA Repair, 73, pp. 78-90. (doi: 10.1016/j.dnarep.2018.11.005) (PMID:30470509) (PMCID:PMC6329875)
Briggs, E., Hamilton, G., Crouch, K. , Lapsley, C. and McCulloch, R. (2018) Genome-wide mapping reveals conserved and diverged R-loop activities in the unusual genetic landscape of the African trypanosome genome. Nucleic Acids Research, 46(22), pp. 11789-11805. (doi: 10.1093/nar/gky928) (PMID:30304482) (PMCID:PMC6294496)
Damasceno, J. D. , Obonaga, R., Silva, G. L.A., Reis-Cunha, J. L., Duncan, S. M., Bartholomeu, D. C., Mottram, J. C. , McCulloch, R. and Tosi, L. R.O. (2018) Conditional genome engineering reveals canonical and divergent roles for the Hus1 component of the 9-1-1 complex in the maintenance of the plastic genome of Leishmania. Nucleic Acids Research, 46(22), pp. 11835-11846. (doi: 10.1093/nar/gky1017) (PMID:30380080) (PMCID:PMC6294564)
Briggs, E., Crouch, K. , Lemgruber, L. , Lapsley, C. and McCulloch, R. (2018) Ribonuclease H1-targeted R-loops in surface antigen gene expression sites can direct trypanosome immune evasion. PLoS Genetics, 14(12), e1007729. (doi: 10.1371/journal.pgen.1007729) (PMID:30543624) (PMCID:PMC6292569)
Santos da Silva, M., Hovel-Miner, G. A., Briggs, E. M., Elias, M. C. and McCulloch, R. (2018) Evaluation of mechanisms that may generate DNA lesions triggering antigenic variation in African trypanosomes. PLoS Pathogens, 14(11), e1007321. (doi: 10.1371/journal.ppat.1007321) (PMID:30440029) (PMCID:PMC6237402)
Gomes Passos Silva, D. et al. (2018) The in vivo and in vitro roles of Trypanosoma cruzi Rad51 in the repair of DNA double strand breaks and oxidative lesions. PLoS Neglected Tropical Diseases, 12(11), e0006875. (doi: 10.1371/journal.pntd.0006875) (PMID:30422982) (PMCID:PMC6258567)
Marques, C. A. and McCulloch, R. (2018) Conservation and variation in strategies for DNA replication of kinetoplastid nuclear genomes. Current Genomics, 19(2), pp. 98-109. (doi: 10.2174/1389202918666170815144627) (PMID:29491738) (PMCID:PMC5814967)
Almeida, L. V., Coqueiro-Dos-Santos, A., Rodriguez-Luiz, G. F., McCulloch, R. , Bartholomeu, D. C. and Reis-Cunha, J. L. (2018) Chromosomal copy number variation analysis by next generation sequencing confirms ploidy stability in Trypanosoma brucei subspecies. Microbial Genomics, 4(10), e000223. (doi: 10.1099/mgen.0.000223) (PMID:30256189) (PMCID:PMC6249438)
McCulloch, R. , Cobbold, C. A. , Figueiredo, L., Jackson, A., Morrison, L. J., Mugnier, M. R., Papavasiliou, N., Schnaufer, A. and Matthews, K. (2017) Emerging challenges in understanding trypanosome antigenic variation. Emerging Topics in Life Sciences, 1(6), pp. 585-592. (doi: 10.1042/ETLS20170104) (PMID:30271884) (PMCID:PMC6162063)
da Silva, M. S., Pavani, R. S., Damasceno, J. D. , Marques, C. A. , McCulloch, R. , Tosi, L. R. O. and Elias, M. C. (2017) Nuclear DNA replication in trypanosomatids: there are no easy methods for solving difficult problems. Trends in Parasitology, 33(11), pp. 858-874. (doi: 10.1016/j.pt.2017.08.002) (PMID:28844718) (PMCID:PMC5662062)
Stortz, J. A. et al. (2017) Genome-wide and protein kinase-focused RNAi screens reveal conserved and novel damage response pathways in Trypanosoma brucei. PLoS Pathogens, 13(7), e1006477. (doi: 10.1371/journal.ppat.1006477) (PMID:28742144) (PMCID:PMC5542689)
Fernandez-Cortes, F., Serafim, T. D., Wilkes, J. M. , Jones, N. G., Ritchie, R., McCulloch, R. and Mottram, J. C. (2017) RNAi screening identifies Trypanosoma brucei stress response protein kinases required for survival in the mouse. Scientific Reports, 7, 6156. (doi: 10.1038/s41598-017-06501-8) (PMID:28733613) (PMCID:PMC5522463)
Devlin, R., Marques, C. A. and McCulloch, R. (2017) Does DNA replication direct locus-specific recombination during host immune evasion by antigenic variation in the African trypanosome? Current Genetics, 63(3), pp. 441-449. (doi: 10.1007/s00294-016-0662-7) (PMID:27822899) (PMCID:PMC5422504)
Biéler, S. et al. (2016) Evaluation of antigens for development of a serological test for human African trypanosomiasis. PLoS ONE, 11(12), e0168074. (doi: 10.1371/journal.pone.0168074) (PMID:27936225) (PMCID:PMC5148118)
Marques, C. A. , Tiengwe, C., Lemgruber Soares, L. , Damasceno, J. D., Scott, A., Paape, D. , Marcello, L. and McCulloch, R. (2016) Diverged composition and regulation of the Trypanosoma brucei origin recognition complex that mediates DNA replication initiation. Nucleic Acids Research, 44(10), pp. 4763-4784. (doi: 10.1093/nar/gkw147) (PMID:26951375) (PMCID:PMC4889932)
Damasceno, J. D., Obonaga, R., Santos, E. V., Scott, A., McCulloch, R. and Tosi, L. R.O. (2016) Functional compartmentalization of Rad9 and Hus1 reveals diverse assembly of the 9-1-1 complex components during the DNA damage response in Leishmania. Molecular Microbiology, 101(6), pp. 1054-1068. (doi: 10.1111/mmi.13441) (PMID:27301589) (PMCID:PMC5453112)
McCulloch, R. and Navarro, M. (2016) The protozoan nucleus. Molecular and Biochemical Parasitology, 209(1-2), pp. 76-87. (doi: 10.1016/j.molbiopara.2016.05.002) (PMID:27181562)
Devlin, R., Marques, C. A. , Paape, D. , Prorocic, M., Zurita-Leal, A. C., Campbell, S. J., Lapsley, C., Dickens, N. and McCulloch, R. (2016) Mapping replication dynamics in Trypanosoma brucei reveals a link with telomere transcription and antigenic variation. eLife, 5, e12765. (doi: 10.7554/eLife.12765) (PMID:27228154) (PMCID:PMC4946898)
Rodenko, B., Wanner, M., Alkhaldi, A., Ebiloma, G., Barnes, R., Kaiser, M., Brun, R., McCulloch, R. , Koomen, G.-J. and De Koning, H. P. (2015) Targeting the parasite's DNA with methyltriazenyl purine analogs Is a safe, selective, and efficacious antitrypanosomal strategy. Antimicrobial Agents and Chemotherapy, 59(11), pp. 6708-6716. (doi: 10.1128/aac.00596-15) (PMID:26282430) (PMCID:PMC4604408)
Marques, C. A. , Dickens, N. J. , Paape, D. , Campbell, S. J. and McCulloch, R. (2015) Genome-wide mapping reveals single-origin chromosome replication in Leishmania, a eukaryotic microbe. Genome Biology, 16, 230. (doi: 10.1186/s13059-015-0788-9) (PMID:26481451) (PMCID:PMC4612428)
Matthews, K. R., McCulloch, R. and Morrison, L. J. (2015) The within-host dynamics of African trypanosome infections. Philosophical Transactions of the Royal Society B: Biological Sciences, 370(1675), 20140288. (doi: 10.1098/rstb.2014.0288) (PMID:26150654) (PMCID:PMC4528486)
McCulloch, R. and Field, M. C. (2015) Quantitative sequencing confirms VSG diversity as central to immune evasion by Trypanosoma brucei. Trends in Parasitology, 31(8), pp. 346-349. (doi: 10.1016/j.pt.2015.05.001) (PMID:25999027)
Grazielle-Silva, V., Zeb, T.F., Bolderson, J., Campos, P.C., Miranda, J.B., Alves, C.L., Machado, C.R., McCulloch, R. and Teixeira, S.M. R. (2015) Distinct phenotypes caused by mutation of MSH2 in trypanosome insect and mammalian life cycle forms are associated with parasite adaptation to oxidative stress. PLoS Neglected Tropical Diseases, 9(6), e0003870. (doi: 10.1371/journal.pntd.0003870) (PMID:26083967) (PMCID:PMC4470938)
Dagnachew, S., Terefe, G., Abebe, G., Barry, D., McCulloch, R. and Goddeeris, B. (2015) In vivo experimental drug resistance study in Trypanosoma vivax isolates from tsetse infested and non-tsetse infested areas of Northwest Ethiopia. Acta Tropica, 146, pp. 95-100. (doi: 10.1016/j.actatropica.2015.03.014) (PMID:25792418)
Calderano, S.G., Drosopoulos, W.C., Quaresma, M. M., Marques, C.A. , Kosiyatrakul, S., McCulloch, R. , Schildkraut, C.L. and Elias, M.C. (2015) Single molecule analysis of Trypanosoma brucei DNA replication dynamics. Nucleic Acids Research, 43(5), pp. 2655-2665. (doi: 10.1093/nar/gku1389) (PMID:25690894) (PMCID:PMC4357695)
Machado, C. R. et al. (2014) Nucleotide excision repair in Trypanosoma brucei: specialization of transcription-coupled repair due to multigenic transcription. Molecular Microbiology, 92(4), pp. 756-776. (doi: 10.1111/mmi.12589) (PMID:24661334) (PMCID:PMC4138998)
Tiengwe, C., Marques, C. A. and McCulloch, R. (2014) Nuclear DNA replication initiation in kinetoplastid parasites: new insights into an ancient process. Trends in Parasitology, 30(1), pp. 27-36. (doi: 10.1016/j.pt.2013.10.009)
Trenaman, A., Hartley, C., Prorocic, M., Passos-Silva, D. G., van den Hoek, M., Nechyporuk-Zloy, V., Machado, C. R. and McCulloch, R. (2013) Trypanosoma brucei BRCA2 acts in a life cycle-specific genome stability process and dictates BRC repeat number-dependent RAD51 subnuclear dynamics. Nucleic Acids Research, 41(2), pp. 943-960. (doi: 10.1093/nar/gks1192)
Tiengwe, C. et al. (2012) Genome-wide analysis reveals extensive functional interaction between DNA replication initiation and transcription in the genome of trypanosoma brucei. Cell Reports, 2(1), pp. 185-197. (doi: 10.1016/j.celrep.2012.06.007)
Tiengwe, C., Marcello, L., Farr, H., Gadelha, C., Burchmore, R. , Barry, J.D., Bell, S.D. and McCulloch, R. (2012) Identification of ORC1/CDC6-interacting factors in trypanosoma brucei reveals critical features of origin recognition complex architecture. PLoS ONE, 7(3), e32674. (doi: 10.1371/journal.pone.0032674) (PMID:22412905) (PMCID:PMC3297607)
Dobson, R., Stockdale, C., Lapsley, C., Wilkes, J. and McCulloch, R. (2011) Interactions among Trypanosoma brucei RAD51 paralogues in DNA repair and antigenic variation. Molecular Microbiology, 81(2), pp. 434-456. (doi: 10.1111/j.1365-2958.2011.07703.x)
Horn, D. and McCulloch, R. (2010) Molecular mechanisms underlying the control of antigenic variation in African trypanosomes. Current Opinion in Microbiology, 13(6), pp. 700-705. (doi: 10.1016/j.mib.2010.08.009)
Morrison, L. J., Marcello, L. and McCulloch, R. (2009) Antigenic variation in the African trypanosome: molecular mechanisms and phenotypic complexity. Cellular Microbiology, 11(12), pp. 1724-1734. (doi: 10.1111/j.1462-5822.2009.01383.x)
McCulloch, R. and Horn, D. (2009) What has DNA sequencing revealed about the VSG expression sites of African trypanosomes? Trends in Parasitology, 25(8), pp. 359-363. (doi: 10.1016/j.pt.2009.05.007)
Stockdale, C., Swiderski, M. R., Barry, J. D. and McCulloch, R. (2008) Antigenic variation in Trypanosoma brucei: joining the DOTs. PLoS Biology, 6(7), e185. (doi: 10.1371/journal.pbio.0060185)
Hartley, C. L. and McCulloch, R. (2008) Trypanosoma brucei BRCA2 acts in antigenic variation and has undergone a recent expansion in BRC repeat number that is important during homologous recombination. Molecular Microbiology, 68(5), pp. 1237-1251. (doi: 10.1111/j.1365-2958.2008.06230.x)
Glover, L., McCulloch, R. and Horn, D. (2008) Sequence homology and microhomology dominate chromosomal double-strand break repair in African trypanosomes. Nucleic Acids Research, 36(8), pp. 2608-2618. (doi: 10.1093/nar/gkn104)
Machado-Silva, A., Teixeira, S. M.R., Franco, G. R., Macedo, A. M., Pena, S. D.J., McCulloch, R. and Machado, C. R. (2008) Mismatch repair in Trypanosoma brucei: Heterologous expression of MSH2 from Trypanosoma cruzi provides new insights into the response to oxidative damage. Gene, 411(1-2), pp. 19-26. (doi: 10.1016/j.gene.2007.12.021)
Burton, P., McBride, D. J., Wilkes, J. M., Barry, J. D. and McCulloch, R. (2007) Ku heterodimer-independent end joining in Trypanosoma brucei cell extracts relies upon sequence microhomology. Eukaryotic Cell, 6(10), pp. 1773-1781. (doi: 10.1128/EC.00212-07)
Barnes, R. L. and McCulloch, R. (2007) Trypanosoma brucei homologous recombination is dependent on substrate length and homology, though displays a differential dependence on mismatch repair as substrate length decreases. Nucleic Acids Research, 35(10), pp. 3478-3493. (doi: 10.1093/nar/gkm249)
Machado, C.R., Augusto-Pinto, L., McCulloch, R. and Teixeira, S.M.R. (2006) DNA metabolism and genetic diversity in Trypanosomes. Mutation Research-Reviews in Mutation Research, 612, pp. 40-57. (doi: 10.1016/j.mrrev.2005.05.001)
Proudfoot, C. and McCulloch, R. (2006) Trypanosoma brucei DMC1 does not act in DNA recombination, repair or antigenic variation in bloodstream stage cells. Molecular and Biochemical Parasitology, 145, pp. 245-253. (doi: 10.1016/j.molbiopara.2005.10.007)
El-Sayed, N.M. et al. (2005) The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science, 309(5733), pp. 409-415. (doi: 10.1126/science.1112631)
Proudfoot, C. and McCulloch, R. (2005) Distinct roles for two RAD51-related genes in Trypanosoma brucei antigenic variation. Nucleic Acids Research, 33, pp. 6906-6919. (doi: 10.1093/nar/gki)
Bell, J., Harvey, T., Sims, A. and McCulloch, R. (2004) Characterization of components of the mismatch repair machinery in Trypanosoma brucei. Molecular Microbiology, 51, pp. 159-173. (doi: 10.1046/j.1365-2958.2003.03804.x)
McCulloch, R. (2004) Antigenic variation in African trypanosomes: monitoring progress. Trends in Parasitology, 20, pp. 117-121.
McCulloch, R., Vassella, E., Burton, P., Boshart, M. and Barry, J.D. (2004) Transformation of monomorphic and pleomorphic Trypanosoma brucei. Methods in Molecular Biology, 262(1), pp. 53-86. (doi: 10.1385/1592597610)
Barry, J., Ginger, M., Burton, P. and McCulloch, R. (2003) Why are parasite contingency genes often associated with telomeres? International Journal for Parasitology, 33, pp. 29-45. (doi: 10.1016/S0020-7519(02)00247-3)
Bell, J. and McCulloch, R. (2003) Mismatch repair regulates homologous recombination, but has little influence on antigenic variation, in Trypanosoma brucei. Journal of Biological Chemistry, 278, pp. 45182-45188. (doi: 10.1074/jbc.M308123200)
Conway, C., McCulloch, R., Ginger, M., Robinson, N., Browitt, A. and Barry, J. (2002) Ku is important for telomere maintenance, but not for differential expression of telomeric VSG genes, in African trypanosomes. Journal of Biological Chemistry, 277, pp. 21269-21277. (doi: 10.1074/jbc.M200550200)
Conway, C., Proudfoot, C., Burton, P., Barry, J. and McCulloch, R. (2002) Two pathways of homologous recombination in Trypanosoma brucei. Molecular Microbiology, 45, pp. 1687-1700.
Robinson, N., McCulloch, R., Conway, C., Browitt, A. and Barry, J. (2002) Inactivation of Mre11 does not affect VSG gene duplication mediated by homologous recombination in Trypanosoma brucei. Journal of Biological Chemistry, 277, pp. 26185-26193. (doi: 10.1074/jbc.M203205200)
Barry, J. and McCulloch, R. (2001) Antigenic variation in trypanosomes: Enhanced phenotypic variation in a eukaryotic parasite. Advances in Parasitology, 49, pp. 1-70.
Vanhamme, L., Pays, E., McCulloch, R. and Barry, J. (2001) An update on antigenic variation in African trypanosomes. Trends in Parasitology, 17, pp. 338-343.
Blakely, G., May, G. , McCulloch, R. , Arciszewska, L. K., Burke, M., Lovett, S. T. and Sherratt, D. J. (1993) Two related recombinases are required for site-specific recombination at dif and cer in E. coli K12. Cell, 75(2), pp. 351-61. (doi: 10.1016/0092-8674(93)80076-Q) (PMID:8402918)
Book Sections
Briggs, E. M., Marques, C. A., Reis-Cunha, J., Black, J., Campbell, S., Damasceno, J. , Bartholomeu, D., Crouch, K. and McCulloch, R. (2020) Next-generation analysis of trypanosomatid genome stability and instability. In: Michels, P. A.M., Ginger, M. L. and Zilberstein, D. (eds.) Trypanosomatids: Methods and Protocols. Series: Methods in Molecular Biology (2116). Springer, pp. 225-262. ISBN 9781071602935 (doi: 10.1007/978-1-0716-0294-2_15)
Cabrera, G., Silva, V. G., Mendes, I. C., Machado, C. R. and McCulloch, R. (2017) Genome maintenance in Trypanosomatids. In: Santos da Silva, M. and Cano, M. I. N. (eds.) Molecular and Cellular Biology of Pathogenic Trypanosomatids. Series: Frontiers in parasitology, 1. Bentham Science, pp. 195-260. ISBN 9781681084060 (doi: 10.2174/9781681084053117010008)
McCulloch, R. , Morrison, L. J. and Hall, J. P.J. (2015) DNA recombination strategies during antigenic variation in the African Trypanosome. In: Craig, N. L., Chandler, M., Gellert, M., Lambowitz, A. M., Rice, P. A. and Sandmeyer, S. B. (eds.) Mobile DNA III. ASM Press: Washington, DC, pp. 409-435. ISBN 9781555819200 (doi: 10.1128/microbiolspec.MDNA3-0016-2014)
Sherratt, D., Blakely, G., Burke, M., Colloms, S. , Leslie, N., McCulloch, R. , May, G. and Roberts, J. (1993) Site-specific recombination and the partition of bacterial chromosomes. In: Heslop-Harrison, J. and Flavell, R. (eds.) The Chromosome. BIOS Scientific Publishers: Oxford, pp. 25-41. ISBN 1872748325
Grants
Grants and Awards listed are those received whilst working with the University of Glasgow.
- Trypanosoma cruzi genome structural variability, gene expression control and consequences
Medical Research Council
2024 - 2027
- Understanding the DNA replication programmes of the African trypanosome and Leishmania
Wellcome Trust
2022 - 2027
- A distinct mode of DNA replication initiation in trypanosomes?
Biotechnology and Biological Sciences Research Council
2021 - 2024
- Bridging epigenetic, metabolism and cell cycle in pathogenic trypanosomatids
Medical Research Council
2019 - 2022
- UK:Brazil Joint Centre Partnership in leishmaniasis
Medical Research Council
2019 - 2022
- Does genome replication in the protozoan parasite Leishmania rely on origin-indepenent initiation?
Biotechnology and Biological Sciences Research Council
2018 - 2021
- Challenging trypanosome antigenic variation paradigms using natural systems
Wellcome Trust
2018 - 2022
- Challenging trypanosome antigenic variation paradigms using natural systems
Wellcome Trust
2018 - 2023
- RECREPEMLE
European Commission
2017 - 2019
- How do common and diverged features of the replicative stress response shape the biology of TriTryp
Biotechnology and Biological Sciences Research Council
2016 - 2019
- 14CONFAP Understanding diverged genome repair and replication functions in trypanosomatid parasites
Biotechnology and Biological Sciences Research Council
2015 - 2016
- The Wellcome Centre for Molecular Parasitology ( Core Support )
Wellcome Trust
2014 - 2021
- Kinase dependent control of DNA replication and repair as a drug target in Trypanosoma brucei.
Biotechnology and Biological Sciences Research Council
2013 - 2016
- Chromosomal recombination and repair in African trypanosomes
Wellcome Trust
2009 - 2014
- Characterisation of Orc1/Cdc6 and DNA replication initiation in Trypanosoma brucei.
Wellcome Trust
2008 - 2011
- DNA recombination pathways and antigenic variation in trypanosoma brucei
Medical Research Council
2006 - 2008
- DNA recombination in trypanosome antigenic variation
The Royal Society
1997 - 2006
Additional information
Invited International Presentations
- 2013: Foz do Iguacu, Brazil - 11th International Conference on Environmental Mutagens
- 2013: Woods Hole, Massachusetts, USA - Plenary lecture, V Kinetoplastid Molecular Cell Biology meeting
- 2013: Sao Paulo, Brazil - V Fundamental Aspects of DNA repair and Mutagenesis symposium
- 2012: Glasgow, Scotland, UK - British Society for Parasitology Spring meeting and Trypanosomiasis and Leishmaniasis symposium
- 2011: Foz do Iguacu, Brazil - XXVI Annual Meeting of the Brazilian Society of Protozoology
- 2011: Woods Hole, Massachusetts, USA - IV Kinetoplastid Molecular Cell Biology meeting
- 2010: Annecy, France - Fondation Merieux sponsored conference on antigenic variation and immune evasion
- 2009: Belo Horizonte, Brazil - IV Fundamental Aspects of DNA Repair and Mutagenesis symposium
- 2008: Newcastle, England, UK - British Society of Parasitology Spring meeting and Trypanosomiasis and Leishmaniasis symposium
- 2007: Belo Horizonte, Brazil - Universidade Federal de Minas Gerais
- 2007: Rio de Janeiro, Brazil - VIII Brazilian Environmental Mutagenesis, Carcinogenesis and Teratogenesis Meeting
- 2007: Caxambu, Brazil - XXII Annual Meeting of the Brazilian Society of Protozoology
- 2006: Glasgow, Scotland, UK - ICOPA IX (11th International Conference of Parasitology)
- 2006: Orlando, Florida, USA - Divisional Lecture, American Society for Microbilogy 106th General Meeting
- 2005: Keystone, Colorado, USA - Keystone symposium on DNA replication and recombination
- 2005: Woods Hole, Massachusetts, USA - Kinetoplastid Molecular and Cell Biology meeting
- 2004: Cambridge, England, UK - Trypanosomatid genome sequence annotation meeting, Wellcome Sanger Centre
- 2004: Ceske Budejovice, Czech Republic - British Society for Parasitology Trypanosomiasis and Leishmaniasis Seminar
- 2003: Woods Hole, Massachusetts, USA - Molecular Parasitology meeting
- 2002: Snowbird, Utah, USA - Keystone symposium on DNA replication and recombination
- 2002: Woods Hole, Massachusetts, USA - Molecular Parasitology meeting
Research Fellowship
- 1997 - 2006: Royal Society University Research Fellowship
- 1994 - 1997: Wellcome Trust International Prize Travelling Fellowship