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					Proposal for inclusion to INSTRUCT (Integrated Structural
Biology Infrastructure), as an Associate Centre to Oxford
University Core, the Large Scale Virus Production and
Purification facility of the Helsinki University.




Applicant:

Dennis Bamford, Professor
Director of the National Center of Excellence in Virus Research
P.O. 56 (Viikinkaari 5), 00014 University of Helsinki.
Tel: +358-9-191 59100: Fax +358-9-191 59098
e-mail: dennis.bamford@helsinki.fi
www.helsinki.fi/virres
2. Extended abstract (1 page)

The methods and principles developed for the production and purification of protein size
particles do not often apply for virus size particles with highly complex structures and
sizes in the order of tens to hundreds of MDa’s. As viruses are the most abundant life
forms and causative agents for severe infectious diseases in all cellular organisms it is
imperative to include them in INSTRUCT activities and to improve the methods to
produce, purify and prepare viruses for structural studies. I have been, for more than two
decades, involved in virus purification and crystallization methods development as well
as in the work where viral structures have been solved using both electron microscopy
and X-ray diffraction. Consequently there is an operational large scale virus purification
platform with eight ultra- and four super speed centrifuges with appropriate gradient
making and fractionation instrumentation available in my laboratory

New possibilities for virus purification methods using Asymmetric Flow Field
Fractionation (AFFF) are emerging. Such technologies need to be validated for virus
purification and their current analytical scale has to be upgraded to preparative one if
such a technology will be useful in purification of large size particles. I have initiated a
collaboration with Postnova Ltd (the manufacturer of AFFF instrumentation) to involve
them to develop novel purification methods suitable to produce virus material for
structural studies. They have committed to the work.

The material production pipeline of INSTRUCT contains the methods to provide high
quality and quantity of protein specimens for structural analysis. Although the protein
production and purification systems are well developed within INSTRUCT there is no
expertise devoted for virus production and purification in spite of the high importance of
viruses. Consequently an Associate Center connected to Oxford University Core Center
to cover this field is proposed.

The annual operating costs for the virus production and purification platform is 200 000 €
that has to be covered by national funding. Due to the multilateral nature of INSTRUCT
the external scientific community applies to use the facility with the rules developed
within INSTRUCT. Selected applicants will have free access to the infrastructure.
Depending on the expectations of an external user the operational mode can vary from
training to technical support extending to full collaboration when appropriate.

I consider that the virus production and purification facility of the University of Helsinki
is an excellent candidate for inclusion to INSTRUCT. It is an operational high power
facility with strong links to a INSTRUCT core center. It also provides expertise not
otherwise available and the materials can be provided at the scale needed.




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3. Integration plan (3 pages)
Background. The methods and principles developed for the production and purification of
protein size particles do not often apply for virus size particles with highly complex
structures and sizes in the order of tens to hundreds of MDa’s. As viruses are the most
abundant life forms and causative agents for severe infectious diseases in all cellular
organisms it is imperative to include them in INSTRUCT activities and to improve the
methods to produce, purify and prepare viruses for structural studies.

Due to their size and complexity viruses are pushing the limits of structure determination
to high resolution and are the natural interface to connect cell biology to structural
biology. The enormous viral universe is also the least explored domain of life. Each virus
is a challenge to produce in the laboratory and the standard biochemical protein
purification methods are not adequate to obtain highly purified viral particles for
structural studies. The best purification results have been obtained using methods where
the particles stay in the liquid phase. The traditional preparative gradient
ultracentrifugation methods are those mostly used for virus particle purification. When
running parallel in a number of centrifuges adequate amounts of material for structural
studies have been obtained.

Previous activity in the field of application. I have been, for more than two decades,
involved in virus purification and crystallization methods development as well as in the
work where viral structures have been solved both using electron microscopy and X-ray
diffraction. Consequently there is an operational large scale virus purification platform
with eight ultra- and four super speed centrifuges with appropriate gradient making and
fractionation instrumentation available in my laboratory. Gradient ultracentrifugations are
utilized and mastered. This is mature technology but widely used as the virus purification
paradigm. For new initiatives for virus purification technology see below.
Examples for methods development and virus structure determination where our large
scale virus purification platform has been used are illustrated in references given below:

Examples of methods developed for virus X-ray analysis
Kivela HM, Abrescia NG, Bamford JK, Grimes JM, Stuart DI, Bamford DH. (2008).
Selenomethionine labeling of large biological macromolecular complexes: Probing the
structure of marine bacterial virus PM2. J Struct Biol 161(2), 204-210.
 Cockburn JJ, Bamford JK, Grimes JM, Bamford DH, Stuart DI. (2003).
Crystallization of the membrane-containing bacteriophage PRD1 in quartz
capillaries by vapour diffusion. Acta Crystallogr D Biol Crystallogr 59(Pt 3), 538-540.
Bamford JK, Cockburn JJ, Diprose J, Grimes JM, Sutton G, Stuart DI, Bamford DH.
(2002). Diffraction quality crystals of PRD1, a 66-MDa dsDNA virus with an internal
membrane. J Struct Biol 139(2), 103-112.
Walin L, Tuma R, Thomas GJ,Jr, Bamford DH. (1994).
Purification of viruses and macromolecular assemblies for structural
investigations using a novel ion exchange method. Virology 201(1), 1-7.
Bamford JK, Bamford DH. (1991). Large-scale purification of membrane-containing
bacteriophage PRD1 and its subviral particles. Virology 181(1), 348-352.


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Examples of Virus Particle Structures Solved (40-80 MDa)
Abrescia NG, Grimes JM, Kivela HM, Assenberg R, Sutton GC, Butcher SJ, Bamford
JK, Bamford DH, Stuart DI. (2008). Insightsinto virus evolution and membrane
biogenesis from the structure of the marine lipid-containing bacteriophage PM2. Mol Cell
31(5), 749-761.
Jaalinoja HT, Roine E, Laurinmaki P, Kivela HM, Bamford DH, Butcher SJ. (2008).
Structure and host-cell interaction of SH1, a membrane-containing, halophilic
euryarchaeal virus. Proc Natl Acad Sci U S A 105(23), 8008-8013.
Jaatinen ST, Happonen LJ, Laurinmaki P, Butcher SJ, Bamford DH. (2008).
Biochemical and structural characterization of membrane-containing icosahedral dsDNA
bacteriophages infecting thermophilic Thermus thermophilus. Virology 379(1), 10-19
Huiskonen JT, de Haas F, Bubeck D, Bamford DH, Fuller SD, Butcher SJ. (2006).
Structure of the bacteriophage phi6 nucleocapsid suggests a mechanism for sequential
RNA packaging. Structure 14(6), 1039-1048.
Laurinmaki PA, Huiskonen JT, Bamford DH, Butcher SJ. (2005). Membrane proteins
modulate the bilayer curvature in the bacterial virus bam35. Structure (Camb) 13(12),
1819-1828.
Abrescia NG, Cockburn JJ, Grimes JM, Sutton GC, Diprose JM, Butcher SJ, Fuller SD,
San Martin C, Burnett RM, Stuart DI, Bamford DH, Bamford JK. (2004). Insights into
assembly from structural analysis of bacteriophage PRD1. Nature 432(7013), 68-74.
Cockburn JJ, Abrescia NG, Grimes JM, Sutton GC, Diprose JM, Benevides JM,
Thomas GJ,Jr, Bamford JK, Bamford DH, Stuart DI. (2004). Membrane structure and
interactions with protein and DNA in bacteriophage PRD1. Nature 432(7013), 122-125.
Huiskonen JT, Kivela HM, Bamford DH, Butcher SJ. (2004). The PM2 virion has a
novel organization with an internal membrane and pentameric receptor binding spikes.
Nat Struct Mol Biol 11(9), 850-856.
San Martin C, Huiskonen JT, Bamford JK, Butcher SJ, Fuller SD, Bamford DH, Burnett
RM. (2002). Minor proteins, mobile arms and membrane-capsid interactions in the
bacteriophage PRD1 capsid. Nat Struct Biol 9(10), 756-763.
Martin CS, Burnett RM, de Haas F, Heinkel R, Rutten T, Fuller SD, Butcher SJ,
Bamford DH. (2001). Combined EM/X-ray imaging yields a quasi-atomic model of the
adenovirus-related bacteriophage PRD1 and shows key capsid and membrane
interactions. Structure (Camb) 9(10), 917-930.
Butcher SJ, Dokland T, Ojala PM, Bamford DH, Fuller SD. (1997). Intermediates in the
assembly pathway of the double-stranded RNA virus phi6. EMBO J 16(14), 4477-4487.
Butcher SJ, Bamford DH, Fuller SD. (1995). DNA packaging orders the membrane of
bacteriophage PRD1. EMBO J 14(24), 6078-6086.

New methods for virus purification. New possibilities for virus purification methods
using Asymmetric Flow Field Fractionation (AFFF) are emerging (for the working
principle see Figure 1). Such technologies need to be validated for virus purification and
their current analytical scale has to be upgraded to preparative scale if such a technology
will be useful in purification of large size particles. Such instrumentation has been
purchased from Postnova Ltd and is in the process to be installed at the Viikki Campus
of the Helsinki University. I have also initiated collaboration with Postnova to involve the



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instrument manufacturer to develop novel purification methods suitable to produce virus
material for structural studies. They have committed to the work.




Figure 1. Separation principles of the asymmetric flow field fractionation. For more
details please go to www.postnova.com

Integration to INSTRUCT. The material production pipeline of INSTRUCT contains the
methods to provide high quality and quantity of protein specimens for structural analysis.
Although the protein production and purification systems are well developed within
INSTRUCT there is no expertise devoted for virus production and purification in spite of
the high importance of viruses. INSTRUCT WG I was established by the management
committee to investigate European readiness in this field with the recommendation to
open a call for an Associate Center for large scale virus production and development
of purification methods for structural analysis.

The virus production and purification facility at the Helsinki University has been
developed over the years and is an established infrastructure. It has successfully
collaborated with the Oxford core center (see references given). It is currently also
exploring novel methods for virus purification (see above).

Currently the facility produces prokaryotic viruses infecting both bacterial and archaeal
hosts. Expertise to produce plant viruses exist on the campus and this capacity will be
integrated during the first year of operation of the proposed Associate Center provided
that national funding can be guaranteed (see financial plan). There is also a plan to
include facilities for nonpathogenic animal virus and virus like particle production during
the second year again depending on the national funding. Provided that financial support
can be guaranteed for instrumentation updates, renewal and technical support, up to 25%
of the capacity of the unit will be provided to external usage for European scientist
according to INSTRUCT principles.

Accordingly I consider that the virus production and purification facility of the University
of Helsinki is an excellent candidate for inclusion to INSTRUCT. It is an operational



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high power facility with strong links to a INSTRUCT core center. It also provides
expertise not otherwise available.

4. Business plan (2 pages)
Expenses to be covered

Current instrumentation. The virus production platform has as a core of eight
ultracentrifuges and four super speed centrifuges including 24 rotors. It is an established
facility with instruments in different stages of their expected life time. The purchase
value for such an infrastructure is close to 1.5 M€. The investment has been done through
national funding sources (the Center of Excellent funding, Academy professor funding
and instrument funding through the University).

The estimated annual average renewal investment for the centrifugation platform is
60 000 €

The AFFF instrumentation has been purchased through the Helsinki University
infrastructure funding program 2009 (250 000 €). The methods development for virus
purification will be carried out together with Postnova Ltd where the company covers its
own cost. However, we will seek external funding for Academia – SME collaboration
preferably from EU sources.

Personnel cost. To keep up the facilities, produce the viruses and to offer training and
support services to European and national users two technicians are required.

The annual total cost for a technician/engineer at the needed expertise level is 45 000
Totaling 90 000 €

Running costs. For annual operational cots including smaller necessary instrumentation,
consumables and travel is 50.000 €

The annual cost for the virus production and purification platform is 200.000 €. If animal
virus production facility will be added later it needs separate funding.

INSTRUCT requires a plan to cover the first five year expenses (1.4.2010-1.4.2015)
leading to a total of 1 M€.

Cost coverage plan

The decision of the national states to cover the ESFRI operational expenses through
national budgets requests a national infrastructure funding system (the preparatory phase
is funded by the EU). The Center of Excellence in Virus Research (Director D. Bamford)
is a joint operation between the Institute of Biotechnology and Department of Biological
and Environmental Sciences. The inclusion of the virus production and purification
platform to INSTRUCT is strongly supported by the home institutions and is within the


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strategic focus areas of the University of Helsinki and Ministry of Education (see support
letters form the University and the Ministry).

The national level research infrastructure policy in Finland is currently under
consideration (Ministry of Education in lead). The idea of INSTRUCT to offer important
research infrastructures for pan European usage is a novel and radical concept. It means
multilateral availability of research infrastructures in the field of structural biology. As
Finland does not, and will not, provide such high investment infrastructures (in the range
of billions of euros) it is necessary to have an access to such technologies. This proposal
is the only one that proposes an associate INSTRUCT center residing in Finland and
consequently would be the Finnish contribution to European level infrastructures in the
field of structural biology. This ESFRI proposal will be included to the Helsinki
University budget plan that will be negotiated with the Ministry of Education during
early fall.

External user policy. Due to the multilateral nature of INSTRUCT the external scientific
community applies to use the facility using the rules developed within INSTRUCT.
Selected applicants will have free access to the infrastructure and support personnel.
What will not be covered are travel and accommodation costs (there may be funding
sources in the future for such activities). Also the consumables will be charged from the
external user (or their institution). Depending on the expectations of an external user the
operational mode can vary from training to technical support extending to full
collaboration when appropriate.

5. Curriculum Vitae
1. Full names: Dennis Henry Bamford
2. Date and place of birth: December 17, 1948 Helsinki, Finland
3. Current position: Professor, Research Director, University of Helsinki

4. Education and training

       M.Sc. 1975 Department of Genetics, University of Helsinki
       Ph.D. 1980         -"-                   -"-
       Docent 1981-1993 University of Helsinki

       EMBO-fellowship Public Health Research Institute, New York 1981 - 1982.
       Short term visits to institutions such as: EMBL; LMB Cambridge; Univ. of
       Missouri Kansas City; Public Health Research Institute, New York, Oxford
       University, California Institute of Technology

5. Previous professional appointments

       Teaching assistant, Dept. of Genetics, Univ. of Helsinki 1975 – 1981.
       Senior Researcher, Academy of Finland 1983 – 1991.
       Senior Scientist, Academy of Finland 1991 - 1992.


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       Research Director, Professor, Institute of Biotechnology 1992-1997.
       Professor in General Microbiology 1993-, Univ. of Helsinki
       Academy Professor 2002-2007.

6. Professional activities and prizes

       Faculty council member, Faculty of Mathematics and Natural Sciences, Univ.
       Helsinki 1992-1998.
       Scientific Advisory board, Maj and Tor Nessling Foundation, Helsinki, member
       1988-1992, chairman 1992-1993.
       Department of Electron microscopy, Univ. Helsinki, board member 1992-1995.
       University of Helsinki, Faculty of Mathematics and Natural Sciences International
       Evaluation committee, member 1993, chairman 1994.
       Foundation for Biotechnical and Industrial Fermentation Research, Helsinki,
       Executive committee member 1995-1998.
       Biocentrum Helsinki (National Center of Excellence) member, 1995-2009.
       Laboratory Animal Facility, Univ. Helsinki, board member 1994-1997.
       Board for Gene Technology (Competent Authority, EU), vice chairman 1995-
       1999.
       International Committee on Taxonomy of Viruses, Executive Committee member
       1996-2002, bacterial virus subcommittee chair on lipid containing bacteriophages
       1985-.
       Artti Foundation, chairman, 1997-1999; 2002-2003, 2005-, board member 2000-
       2001; 2004-2005.
       University of Helsinki Regional Student Union (Karjalainen Osakunta) elected
       university representative (Inspehtori) 1996-.
       Societas Biochemica, Biophysica et Microbiologica Fenniae, President1999-2005.
       Director, Program on Structural Virology a National Center of Excellence 2000-
       2005.
       UNESCO Associated Center of Excellence, Vilnius University, SAB member
       2000-2005.
       Finnish Academy of Science and Letters member elected 2002.
       Steering Group Member, Viikki Graduate School in Biosciences, 2000-,
       Chairman 2008-.
       Faculty Council Member, Faculty of Biosciences, University of Helsinki, 2004-.
       Research Group Organization in Molecular Biosciences, University of Helsinki,
       Chairman 2000-2006, member 2008-.
       University of Helsinki, 2005 Prize for scientific innovation (molecular
       biosciences).
       Director, Finnish Center of Excellence in Virus Research, 2006-2011.
       European Molecular Biology Organization (EMBO) member, elected 2006.
       EMBL, Hamburg outstation Evaluation Board member, 2007.
       Program Committee member, 3rd FEMS Congress of European Microbiologists,
       2009.

7. Editorial board memberships



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       Journal of General Virology, 1981 - 1983; 2006 - 2010
       Journal of Virology, 2006-2011
       Encyclopaedia of Virology (Elsevier) editor responsible for bacterial and archaeal
       viruses, 2005-2008.

8. Memberships in scientific societies

       Societas Genetica Fenniae 1974-
       The Scandinavian Association of Geneticists 1975-
       Societas Biochemica, Biophysica et Microbiologica Fenniae (honorary member)
       American Society for Microbiology 1979-
       Society for General Microbiology 1979-2000
       The New York Academy of Sciences 1981-1988
       American Association of Advancement of Science 1992-

9. Supervised students

       I have supervised 28 graduate students and jointly two additional ones. Five of the
       previous graduate students have obtained a professor or comparable status. Three
       are research group PIs.


10. Referee activity in journals like:

       Journal of Bacteriology, Journal of Virology, Journal of General Virology,
       Microbiology, Journal of Molecular Biology, RNA, NAR, European Journal of
       Biochemistry, Gene, Plasmid, FEMS Microbiology Letters, PNAS, Biochemistry,
       Archives in Virology, EMBO Journal, Science, Molecular Cell, Cell, Virology,
       Nature, Nature Reviews in Microbiology.


PRIMARY ARTICLES 2009-2005

Krupovic M, Bamford DH. (2009). Does the evolution of viral polymerases reflect the
origin and evolution of viruses? Nat Rev Microbiol 7(3), 250. [PubMed]

Krupovic M, Ravantti JJ, Bamford DH. (2009). Geminiviruses: a tale of a plasmid
becoming a virus. BMC Evol Biol 9112. [PubMed]

Kukkaro P, Bamford DH. (2009). Virus-host interactions in environments with a wide
range of ionic strengths. Environ Microbiol Reports 1(1), 71-77.

Lee HC, Chang SS, Choudhary S, Aalto AP, Maiti M, Bamford DH, Liu Y. (2009).
qiRNA is a new type of small interfering RNA induced by DNA damage. Nature
459(7244), 274-277. [PubMed]



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Pietila MK, Roine E, Paulin L, Kalkkinen N, Bamford DH. (2009). An ssDNA virus
infecting archaea: a new lineage of viruses with a membrane envelope. Mol
Microbiol 72(2), 307-319. [PubMed]

Sarin LP, Poranen MM, Lehti NM, Ravantti JJ, Koivunen MR, Aalto AP, van Dijk AA,
Stuart DI, Grimes JM, Bamford DH. (2009). Insights into the pre-initiation events of
bacteriophage phi 6 RNA-dependent RNA polymerase: towards the assembly of a
productive binary complex. Nucleic Acids Res 37(4), 1182-1192. [PubMed]

Ziedaite G, Kivela HM, Bamford JK, Bamford DH. (2009). Purified membrane-
containing procapsids of bacteriophage PRD1 package the viral genome. J Mol Biol
386(3), 637-647. [PubMed]

Abrescia NG, Grimes JM, Kivela HM, Assenberg R, Sutton GC, Butcher SJ, Bamford
JK, Bamford DH, Stuart DI. (2008). Insights into virus evolution and membrane
biogenesis from the structure of the marine lipid-containing bacteriophage PM2.
Mol Cell 31(5), 749-761. [PubMed]

Jaalinoja HT, Roine E, Laurinmaki P, Kivela HM, Bamford DH, Butcher SJ. (2008).
Structure and host-cell interaction of SH1, a membrane-containing, halophilic
euryarchaeal virus. Proc Natl Acad Sci U S A 105(23), 8008-8013. [PubMed]

Jaatinen ST, Happonen LJ, Laurinmaki P, Butcher SJ, Bamford DH. (2008).
Biochemical and structural characterisation of membrane-containing icosahedral
dsDNA bacteriophages infecting thermophilic Thermus thermophilus. Virology
379(1), 10-19. [PubMed]

Kainov DE, Mancini EJ, Telenius J, Lisal J, Grimes JM, Bamford DH, Stuart DI, Tuma
R. (2008). Structural Basis of Mechanochemical Coupling in a Hexameric Molecular
Motor. J Biol Chem 283(6), 3607-3617. [PubMed]

Kivela HM, Abrescia NG, Bamford JK, Grimes JM, Stuart DI, Bamford DH. (2008).
Selenomethionine labeling of large biological macromolecular complexes: Probing
the structure of marine bacterial virus PM2. J Struct Biol 161(2), 204-210. [PubMed]

Kivela HM, Madonna S, Krupovic M, Tutino ML, Bamford JK. (2008). Genetics for
Pseudoalteromonas provides tools to manipulate marine bacterial virus PM2. J
Bacteriol 190(4), 1298-1307. [PubMed]

Krupovic M, Bamford DH. (2008). Archaeal proviruses TKV4 and MVV extend the
PRD1-adenovirus lineage to the phylum Euryarchaeota. Virology 375(1), 292-300.
[PubMed]

Krupovic M, Bamford DH. (2008). Holin of bacteriophage lambda: structural insights
into a membrane lesion. Mol Microbiol 69(4), 781-783. [PubMed]




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Krupovic M, Cvirkaite-Krupovic V, Bamford DH. (2008). Identification and functional
analysis of the Rz/Rz1-like accessory lysis genes in the membrane-containing
bacteriophage PRD1. Mol Microbiol 68(2), 492-503. [PubMed]

Poranen MM, Butcher SJ, Simonov VM, Laurinmaki P, Bamford DH. (2008). Roles of
the Minor Capsid Protein P7 in the Assembly and Replication of Double-Stranded
RNA Bacteriophage varphi6. J Mol Biol [PubMed]

Poranen MM, Koivunen MR, Bamford DH. (2008). Nontemplated terminal
nucleotidyltransferase activity of double-stranded RNA bacteriophage phi6 RNA-
dependent RNA polymerase. J Virol 82(18), 9254-9264. [PubMed]

Ravantti JJ, Ruokoranta TM, Alapuranen AM, Bamford DH. (2008). Global
transcriptional responses of Pseudomonas aeruginosa to phage PRR1 infection. J
Virol 82(5), 2324-2329. [PubMed]

Aalto AP, Sarin LP, van Dijk AA, Saarma M, Poranen MM, Arumae U, Bamford DH.
(2007). Large-scale production of dsRNA and siRNA pools for RNA interference
utilizing bacteriophage phi6 RNA-dependent RNA polymerase. RNA 13(3), 422-429.
[PubMed]

Daugelavicius R, Gaidelyte A, Cvirkaite-Krupovic V, Bamford DH. (2007). On-line
monitoring of changes in host cell physiology during the one-step growth cycle of
Bacillus phage Bam35. J Microbiol Methods 69(1), 174-179. [PubMed]

Gaidelyte A, Vaara M, Bamford DH. (2007). Bacteria, phages and septicemia. PLoS
ONE 2(11), e1145. [PubMed]

Jaalinoja HT, Huiskonen JT, Butcher SJ. (2007). Electron cryomicroscopy comparison
of the architectures of the enveloped bacteriophages phi6 and phi8. Structure 15(2),
157-167. [PubMed]

Karhu NJ, Ziedaite G, Bamford DH, Bamford JK. (2007). Efficient DNA packaging of
bacteriophage PRD1 requires the unique vertex protein P6. J Virol 81(6), 2970-2979.
[PubMed]

Krupovic M, Bamford DH. (2007). Putative prophages related to lytic tailless marine
dsDNA phage PM2 are widespread in the genomes of aquatic bacteria. BMC
Genomics 8236. [PubMed]

Krupovic M, Daugelavicius R, Bamford DH. (2007). A novel lysis system in PM2, a
lipid-containing marine double-stranded DNA bacteriophage. Mol Microbiol 64(6),
1635-1648. [PubMed]




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Krupovic M, Daugelavicius R, Bamford DH. (2007). Polymyxin B induces lysis of
marine pseudoalteromonads. Antimicrob Agents Chemother 51(11), 3908-3914.
[PubMed]

Laurinavicius S, Bamford DH, Somerharju P. (2007). Transbilayer distribution of
phospholipids in bacteriophage membranes. Biochim Biophys Acta 1768(10), 2568-
2577. [PubMed]

Gaidelyte A, Cvirkaite-Krupovic V, Daugelavicius R, Bamford JK, Bamford DH. (2006).
The entry mechanism of membrane-containing phage Bam35 infecting Bacillus
thuringiensis. J Bacteriol 188(16), 5925-5934. [PubMed]

Huiskonen JT, de Haas F, Bubeck D, Bamford DH, Fuller SD, Butcher SJ. (2006).
Structure of the bacteriophage phi6 nucleocapsid suggests a mechanism for
sequential RNA packaging. Structure 14(6), 1039-1048. [PubMed]

Kivela HM, Roine E, Kukkaro P, Laurinavicius S, Somerharju P, Bamford DH. (2006).
Quantitative dissociation of archaeal virus SH1 reveals distinct capsid proteins and
a lipid core. Virology 356(1-2), 4-11. [PubMed]

Krupovic M, Vilen H, Bamford JK, Kivela HM, Aalto JM, Savilahti H, Bamford DH.
(2006). Genome Characterization of Lipid-Containing Marine Bacteriophage PM2
by Transposon Insertion Mutagenesis. J Virol 80(18), 9270-9278. [PubMed]

Poranen MM, Ravantti JJ, Grahn AM, Gupta R, Auvinen P, Bamford DH. (2006). Global
changes in cellular gene expression during bacteriophage PRD1 infection. J Virol
80(16), 8081-8088. [PubMed]

Ruokoranta TM, Grahn AM, Ravantti JJ, Poranen MM, Bamford DH. (2006). Complete
Genome Sequence of the Broad Host Range Single-Stranded RNA Phage PRR1
Places It in the Levivirus Genus with Characteristics Shared with Alloleviviruses. J
Virol 80(18), 9326-9330. [PubMed]

Salgado PS, Koivunen MR, Makeyev EV, Bamford DH, Stuart DI, Grimes JM. (2006).
The Structure of an RNAi Polymerase Links RNA Silencing and Transcription.
PLoS Biol 4(12), e434. [PubMed]

Abrescia NG, Kivela HM, Grimes JM, Bamford JK, Bamford DH, Stuart DI. (2005).
Preliminary crystallographic analysis of the major capsid protein P2 of the lipid-
containing bacteriophage PM2. Acta Crystallograph Sect F Struct Biol Cryst Commun
61(Pt 8), 762-765. [PubMed]

Bamford DH, Grimes JM, Stuart DI. (2005). What does structure tell us about virus
evolution? Curr Opin Struct Biol 15(6), 655-663. [PubMed]




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Bamford DH, Ravantti JJ, Ronnholm G, Laurinavicius S, Kukkaro P, Dyall-Smith M,
Somerharju P, Kalkkinen N, Bamford JK. (2005). Constituents of SH1, a novel lipid-
containing virus infecting the halophilic euryarchaeon Haloarcula hispanica. J Virol
79(14), 9097-9107. [PubMed]

Daugelavicius R, Cvirkaite V, Gaidelyte A, Bakiene E, Gabrenaite-Verkhovskaya R,
Bamford DH. (2005). Penetration of Enveloped Double-Stranded RNA
Bacteriophages phi13 and phi6 into Pseudomonas syringae Cells. J Virol 79(8), 5017-
5026. [PubMed]

Gaidelyte A, Jaatinen ST, Daugelavicius R, Bamford JK, Bamford DH. (2005). The
linear double-stranded DNA of phage Bam35 enters lysogenic host cells, but the late
phage functions are suppressed. J Bacteriol 187(10), 3521-3527. [PubMed]

Laurila MR, Salgado PS, Makeyev EV, Nettelship J, Stuart DI, Grimes JM, Bamford DH.
(2005). Gene silencing pathway RNA-dependent RNA polymerase of Neurospora
crassa: yeast expression and crystallization of selenomethionated QDE-1 protein. J
Struct Biol 149(1), 111-115. [PubMed]

Laurila MR, Salgado PS, Stuart DI, Grimes JM, Bamford DH. (2005). Back-priming
mode of phi6 RNA-dependent RNA polymerase. J Gen Virol 86(Pt 2), 521-526.
[PubMed]

Laurinmaki PA, Huiskonen JT, Bamford DH, Butcher SJ. (2005). Membrane proteins
modulate the bilayer curvature in the bacterial virus bam35. Structure (Camb)
13(12), 1819-1828. [PubMed]

Meier C, Mancini EJ, Bamford DH, Walsh MA, Stuart DI, Grimes JM. (2005).
Overcoming the false-minima problem in direct methods: structure determination
of the packaging enzyme P4 from bacteriophage phi13. Acta Crystallogr D Biol
Crystallogr 61(Pt 9), 1238-1244. [PubMed]

Merckel MC, Huiskonen JT, Bamford DH, Goldman A, Tuma R. (2005). The Structure
of the Bacteriophage PRD1 Spike Sheds Light on the Evolution of Viral Capsid
Architecture. Mol Cell 18(2), 161-170. [PubMed]

Porter K, Kukkaro P, Bamford JK, Bath C, Kivela HM, Dyall-Smith ML, Bamford DH.
(2005). SH1: A novel, spherical halovirus isolated from an Australian hypersaline
lake. Virology 335(1), 22-33. [PubMed]

Salgado PS, Walsh MA, Laurila MR, Stuart DI, Grimes JM. (2005). Going soft and
SAD with manganese. Acta Crystallogr D Biol Crystallogr 61(Pt 1), 108-111. [PubMed]

Saren AM, Ravantti JJ, Benson SD, Burnett RM, Paulin L, Bamford DH, Bamford JK.
(2005). A snapshot of viral evolution from genome analysis of the tectiviridae family.
J Mol Biol 350(3), 427-440. [PubMed]


                                                                                   13
Stromsten NJ, Bamford DH, Bamford JK. (2005). In vitro DNA Packaging of PRD1: A
Common Mechanism for Internal-membrane Viruses. J Mol Biol 348(3), 617-629.
[PubMed]

Ziedaite G, Daugelavicius R, Bamford JK, Bamford DH. (2005). The Holin protein of
bacteriophage PRD1 forms a pore for small-molecule and endolysin translocation. J
Bacteriol 187(15), 5397-5405. [PubMed]



Reviews 2009-2005

Koivunen MRL, Sarin LP, Bamford DH. (2008). Structure-Function insights into the
RNA-dependent RNA polymerase of the dsRNA bacteriophage phi6. Segmented
Double Stranded RNA Viruses:Structure and molecular biology (ed J.T. Patton),239-257.

Krupovic M, Bamford DH. (2008). Holin of bacteriophage lambda: structural insights
into a membrane lesion. Mol Microbiol 69(4), 781-783. [PubMed]

Poranen MM, Bamford DH. (2008). Entry of a segmented dsRNA virus into the
bacterial cell. Segmented Double Stranded RNA Viruses:Structure and molecular
biology (ed J.T. Patton),215-226.

Poranen MM, Tuma R, Bamford DH. (2008). Dissecting the assembly pathway of
bacterial dsRNA viruses: Infectious nucleocapsids produced by self-assembly.
Segmented Double Stranded RNA Viruses:Structure and molecular biology (ed J.T.
Patton),115-132.

Bamford DH, Bamford JKH. (2006). Lipid-containing bacteriophage PM2, the type-
organism of Corticoviridae. The Bacteriophages (ed R Calendar)171-174.

Grahn AM, Butcher SJ, Bamford JKH, Bamford DH. (2006). PRD1 - dissecting the
genome, structure and entry. The Bacteriophages (ed R Calendar)161-170.

Pirttimaa MJ, Bamford DH. (2005). Nucleic acid packaging of RNA viruses.
Encyclopedia of Molecular Cell Biology and Molecular Medicine (ed R A Mayers)9, 2nd
Edition363-375.

Poranen MM, Pirttimaa MJ, Bamford DH. (2005). Encapsidation of the segmented
double-stranded RNA genome of bacteriophage phi6. Viral Genome Packaging
Machines:Genetics, Structure, and Mechanisms,117-130.

Poranen MM, Tuma R, Bamford DH. (2005). Assembly of double-stranded RNA
bacteriophages. Adv Virus Res 6415-43. [PubMed]




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