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Pat Nuttall

Patricia (Pat) Anne Nuttall, OBE (born 1953)[1] is a British virologist and acarologist known for her research on tick-borne diseases. Her discoveries include the fact that pathogens can be transmitted between vectors feeding on a host without being detectable in the host's blood. She is also a science administrator who served as the director of the Natural Environment Research Council (NERC) Centre for Ecology & Hydrology (2001–11).[2] As of 2015, she is professor of arbovirology in the Department of Zoology of the University of Oxford.[3]

Education edit

Nuttall gained a BSc in microbiology at the University of Bristol in 1974. Her PhD in virology (1978), under the supervision of Jim Stott and C. Kaplan, was at the Institute for Animal Health (now the Pirbright Institute) and the University of Reading.[1][4]

Career edit

From 1977, Nuttall did post-doctoral research at the Edward Grey Institute of Field Ornithology of the Department of Zoology at the University of Oxford and the NERC Unit of Invertebrate Virology in Oxford.[1][4] She remained at the NERC unit, which was renamed the Institute of Virology and Environmental Microbiology (IVEM), rising to be its director in 1996.[1][4] In 2001, IVEM merged with other bodies to become the NERC Centre for Ecology & Hydrology, and Nuttall served as the centre's director until 2011.[2] During this period she oversaw the major restructuring of the centre.[4][5] She subsequently directed national projects with NERC.[1][2] She chaired the Partnership for European Environmental Research from 2008 to 2010.[1][6]

Nuttall has been professor of arbovirology in the Department of Zoology of the University of Oxford since 2013.[1][3] She is a fellow of Wolfson College, Oxford.[7]

Research edit

 
Electron micrograph of tick-borne encephalitis virus

Her early research was on the cattle disease, bovine viral diarrhoea. Nuttall found that the bovine viral diarrhoea virus was often present as a contaminant in foetal bovine serum, a commonly used laboratory reagent, a result that was published in Nature in 1977.[4][8] She then worked with ornithologist Chris Perrins trying to identify the virus responsible for puffinosis, a disease that affects the Manx shearwater (Puffinus puffinus) sea bird.[4][9] During this research, Nuttall visited sea-bird colonies and became interested in ticks, arthropods that often infest sea birds as well as other vertebrates, and can act as vectors for disease.[4]

Nonsystemic transmission edit

In the early 1980s, Nuttall started to study viruses transmitted by ticks, initially focusing on orbiviruses, nairoviruses and thogotoviruses.[1] While performing experiments designed to explore whether Thogoto virus, an influenza-like virus, can be transmitted between ticks during mating, Nuttall and her colleagues unexpectedly found that control ticks became infected.[4] They discovered that the virus can be transmitted between infected and uninfected ticks when they feed simultaneously on apparently uninfected guinea pigs, without the virus being present at a detectable level in the blood.[10][11][12] With Milan Labuda, Nuttall subsequently demonstrated the same phenomenon with tick-borne encephalitis virus, a better-understood arthropod-transmitted virus.[13]

These results challenge the then-accepted idea that arthropod-transmitted viruses can only be transmitted when the arthropod vector feeds on an infected host in which the virus is replicating and circulating in the blood above a threshold level.[4][11][12][14] Sarah Randolph comments:

Suddenly the conventional wisdom that systemic infections above a certain threshold level were necessary for transmission, and could therefore be used to assay host competence, was over-turned. Viraemia and even bacteraemia are now seen as an inconsistent, species-specific consequence of infection but not a necessary condition for transmission.[12]

The phenomenon of nonviraemic or nonsystemic transmission turns out to be widespread – it has been subsequently observed with many other viruses transmitted by ticks, black flies and mosquitos, including major human pathogens such as West Nile virus, as well as other pathogens, including the spirochaete Borrelia burgdorferi, which causes Lyme disease.[11][15][16] – and important in natural transmission.[14] Nuttall's group has continued to study the phenomenon, and have shown that immunity to tick-borne encephalitis virus does not prevent nonsystemic transmission.[17]

Tick saliva edit

 
The tropical bont tick, whose saliva is the source of variegin

Nuttall's recent work has focused on discovering the function of tick saliva's many constituents, as well as the mechanisms by which tick-transmitted pathogens use them to enhance their transmission.[3] Nuttall and colleagues were the first to show, in 1989, that tick saliva promotes the transmission of viruses, a phenomenon which they have called "saliva-assisted transmission"; this has been suggested as a mechanism for nonsystemic transmission.[4][12][18][19] In 1998, she and her colleagues characterised three immunoglobulin-binding proteins, which were among the first proteins from tick saliva to be sequenced.[12][20][21] With Norbert Fuchsberger, Valeria Hajnicka and others, Nuttall has shown that tick saliva suppresses the host's antiviral immune responses, including natural killer cell activity and the induction of type I interferon and cytokines involved in inflammation.[4] Her group has also shown that the proteins in saliva differ between individual ticks of the same species and also change over the course of feeding.[20]

Drugs and vaccines edit

Some components of tick saliva have potential as drugs to treat a range of conditions unrelated to tick disease.[3][22] Nuttall comments that "These molecules have been refined by millions of years of evolution. There are no toxicity problems, they work on a range of animals, they aren't fragile — and there are an awful lot of them."[22] For example, with Guido Paesen, Nuttall has characterised histamine-binding proteins that can suppress inflammation in humans by binding directly to histamine, rather than blocking its access to cell receptors, of which at least four are known.[4][22][23] One of these proteins, rEV131, was investigated by NERC spin-off company Evolutec for the treatment of hay fever and for use in recovery from cataract surgery.[4][22] Another example is the anticoagulant variegin, discovered by Nuttall and Maria Kazimirova in the tropical bont tick (Amblyomma variegatum), which represents a novel class of thrombin inhibitor; it has been shown to prevent venous thrombosis in a zebrafish model.[24][25]

Tick saliva products are also possible targets for vaccines to control tick infestation and, potentially, to prevent the diseases they carry.[3][20] One vaccine candidate explored by Nuttall's group is 64TRP, a 15 kDa Rhipicephalus appendiculatus protein from the cement cone that glues the tick's mouthparts to the host. Vaccination with 64TRP can protect against tick-borne encephalitis virus carried by a different type of tick, the castor bean tick (Ixodes ricinus), in a mouse model.[20][26]

Awards edit

Nuttall received the Ivanovsky Medal for Virology of the Russian Academy of Sciences in 1996.[4] She was awarded the OBE in the 2000 New Year Honours List, for "services to Environmental Science and Policy."[27]

Selected publications edit

Books edit

  • Nuttall PA; Bowman AS, eds. (2008), Ticks: Biology, Disease and Control, Cambridge University Press, ISBN 978-0-521-86761-0

Research papers edit

  • Labuda M, Trimnell AR, Licková M, Kazimírová M, Davies GM, Lissina O, Hails RS, Nuttall PA (2006), "An anti-vector vaccine protects against a lethal vector-borne pathogen", PLOS Pathogens, 2 (4): e27, doi:10.1371/journal.ppat.0020027, PMC 1424664, PMID 16604154
  • Paesen GC, Adams PL, Harlos K, Nuttall PA, Stuart DI (1999), "Tick histamine-binding proteins: Isolation, cloning, and three-dimensional structure", Molecular Cell, 3 (5): 661–71, doi:10.1016/s1097-2765(00)80359-7, PMID 10360182
  • Wang H, Paesen GC, Nuttall PA, Barbour AG (1998), "Male ticks help their mates to feed", Nature, 391 (6669): 753–54, Bibcode:1998Natur.391..753W, doi:10.1038/35773, PMID 9486641, S2CID 4398008
  • Labuda M, Kozuch O, Zuffová E, Elecková E, Hails RS, Nuttall PA (1997), "Tick-borne encephalitis virus transmission between ticks cofeeding on specific immune natural rodent hosts", Virology, 235 (1): 138–43, doi:10.1006/viro.1997.8622, PMID 9300045
  • Jones LD, Hodgson E, Nuttall PA (1989), "Enhancement of virus transmission by tick salivary glands", Journal of General Virology, 70 (7): 1895–98, doi:10.1099/0022-1317-70-7-1895, PMID 2544668
  • Jones LD, Davies CR, Steele GM, Nuttall PA (1987), "A novel mode of arbovirus transmission involving a nonviremic host", Science, 237 (4816): 775–77, Bibcode:1987Sci...237..775J, doi:10.1126/science.3616608, PMID 3616608

References edit

  1. ^ a b c d e f g h "Curriculum Vitae", Epidemiology and Vaccinal Prevention website, OOO "Antorium", retrieved 16 March 2015
  2. ^ a b c "Professor Mark Bailey becomes acting Director of the Centre for Ecology & Hydrology", Centre for Ecology & Hydrology website, Natural Environment Research Council, 1 March 2011, retrieved 16 March 2015
  3. ^ a b c d e "Pat Nuttall", Department of Zoology website, University of Oxford, retrieved 16 March 2015
  4. ^ a b c d e f g h i j k l m n Nuttall, P. (2003), "An interview with Patricia Nuttall, Ph.D.", Vector-Borne and Zoonotic Diseases, 3 (4): 249–53, doi:10.1089/153036603322662228, PMID 14733676
  5. ^ House of Commons: Science and Technology Committee, Research Council Institutes: Fourth Report of Session 2006–07, Vol. 2: Oral and Written Evidence, The Stationery Office, pp. Ev47–49
  6. ^ "METIER Final Conference: Schedule and Lecturers" (PDF), Website, Partnership for European Environmental Research, retrieved 18 March 2015
  7. ^ "Prof Patricia Nuttall", website, Wolfson College, Oxford, retrieved 16 March 2015
  8. ^ Nuttall PA, Luther PD, Stott EJ (1977), "Viral contamination of bovine foetal serum and cell cultures", Nature, 266 (5605): 835–37, Bibcode:1977Natur.266..835N, doi:10.1038/266835a0, PMID 194159, S2CID 4269062
  9. ^ Brooke M (2010), The Manx Shearwater, A & C Black, pp. 8, 161
  10. ^ Jones LD, Davies CR, Steele GM, Nuttall PA (1987), "A novel mode of arbovirus transmission involving a nonviremic host", Science, 237 (4816): 775–77, Bibcode:1987Sci...237..775J, doi:10.1126/science.3616608, JSTOR 1699212, PMID 3616608
  11. ^ a b c Higgs S, Schneider BS, Vanlandingham DL, Klingler KA, Gould EA (2005), "Nonviremic transmission of West Nile virus", Proceedings of the National Academy of Sciences of the United States of America, 102 (25): 8871–74, Bibcode:2005PNAS..102.8871H, doi:10.1073/pnas.0503835102, PMC 1157059, PMID 15951417
  12. ^ a b c d e Randolph SE (2009), "Tick-borne disease systems emerge from the shadows: the beauty lies in molecular detail, the message in epidemiology", Parasitology, 136 (12): 1403–13, doi:10.1017/s0031182009005782, PMID 19366480, S2CID 22845163
  13. ^ Labuda M, Jones LD, Williams T, Danielova V, Nuttall PA (1993), "Efficient transmission of tick-borne encephalitis virus between cofeeding ticks", Journal of Medical Entomology, 30: 295–99, doi:10.1093/jmedent/30.1.295, PMID 8433342
  14. ^ a b Lord CC, Tabachnick WJ (2002), "Influence of nonsystemic transmission on the epidemiology of insect borne arboviruses: A case study of vesicular stomatitis epidemiology in the Western United States", Journal of Medical Entomology, 39 (3): 417–26, doi:10.1603/0022-2585-39.3.417, PMID 12061433
  15. ^ Kuno G, Chang GJ (2005), "Biological transmission of arboviruses: Reexamination of and new insights into components, mechanisms, and unique traits as well as their evolutionary trends", Clinical Microbiology Reviews, 18 (4): 608–37, doi:10.1128/cmr.18.4.608-637.2005, PMC 1265912, PMID 16223950
  16. ^ Patrican LA (1997), "Acquisition of Lyme disease spirochetes by cofeeding Ixodes scapularis ticks", American Journal of Tropical Medicine and Hygiene, 57 (5): 589–93, doi:10.4269/ajtmh.1997.57.589, PMID 9392600
  17. ^ Labuda M, Kozuch O, Zuffová E, Elecková E, Hails RS, Nuttall PA (1997), "Tick-borne encephalitis virus transmission between ticks cofeeding on specific immune natural rodent hosts", Virology, 235 (1): 138–43, doi:10.1006/viro.1997.8622, PMID 9300045
  18. ^ Jones LD, Hodgson E, Nuttall PA (1989), "Enhancement of virus transmission by tick salivary glands", Journal of General Virology, 70 (7): 1895–98, doi:10.1099/0022-1317-70-7-1895, PMID 2544668
  19. ^ Sonenshine DE; Roe RM, eds. (2013), Biology of Ticks, Volume 2, Oxford University Press
  20. ^ a b c d Willadsen P (2004), "Anti-tick vaccines" (PDF), Parasitology, 129: S367-87, doi:10.1017/s0031182003004657, PMID 15938519, S2CID 40368916
  21. ^ Wang H, Paesen GC, Nuttall PA, Barbour AG (1998), "Male ticks help their mates to feed", Nature, 391 (6669): 753–54, Bibcode:1998Natur.391..753W, doi:10.1038/35773, PMID 9486641, S2CID 4398008
  22. ^ a b c d Macilwain C (2006), "Ticking the right boxes", Nature, 439 (7076): 533, Bibcode:2006Natur.439..533M, doi:10.1038/439533a, PMID 16452953, S2CID 4425421
  23. ^ Paesen GC, Adams PL, Harlos K, Nuttall PA, Stuart DI (1999), "Tick histamine-binding proteins: Isolation, cloning, and three-dimensional structure", Molecular Cell, 3 (5): 661–71, doi:10.1016/s1097-2765(00)80359-7, PMID 10360182
  24. ^ Koh CY, Kazimirova M, Trimnell A, Takac P, Labuda M, Nuttall PA, Kini RM (2007), "Variegin, a novel fast and tight binding thrombin inhibitor from the tropical bont tick", Journal of Biological Chemistry, 282 (40): 29101–13, doi:10.1074/jbc.m705600200, PMID 17684009
  25. ^ "Drugs designed by nature could prevent heart attacks and blood clots", Centre for Ecology & Hydrology website, Natural Environment Research Council, retrieved 18 March 2015
  26. ^ Labuda M, Trimnell AR, Licková M, Kazimírová M, Davies GM, Lissina O, Hails RS, Nuttall PA (2006), "An anti-vector vaccine protects against a lethal vector-borne pathogen", PLOS Pathogens, 2 (4): e27, doi:10.1371/journal.ppat.0020027, PMC 1424664, PMID 16604154
  27. ^ "New Year Honours List — United Kingdom", The London Gazette, 55710: 15, 31 December 1999

nuttall, patricia, anne, nuttall, born, 1953, british, virologist, acarologist, known, research, tick, borne, diseases, discoveries, include, fact, that, pathogens, transmitted, between, vectors, feeding, host, without, being, detectable, host, blood, also, sc. Patricia Pat Anne Nuttall OBE born 1953 1 is a British virologist and acarologist known for her research on tick borne diseases Her discoveries include the fact that pathogens can be transmitted between vectors feeding on a host without being detectable in the host s blood She is also a science administrator who served as the director of the Natural Environment Research Council NERC Centre for Ecology amp Hydrology 2001 11 2 As of 2015 she is professor of arbovirology in the Department of Zoology of the University of Oxford 3 Contents 1 Education 2 Career 3 Research 3 1 Nonsystemic transmission 3 2 Tick saliva 3 3 Drugs and vaccines 4 Awards 5 Selected publications 5 1 Books 5 2 Research papers 6 ReferencesEducation editNuttall gained a BSc in microbiology at the University of Bristol in 1974 Her PhD in virology 1978 under the supervision of Jim Stott and C Kaplan was at the Institute for Animal Health now the Pirbright Institute and the University of Reading 1 4 Career editFrom 1977 Nuttall did post doctoral research at the Edward Grey Institute of Field Ornithology of the Department of Zoology at the University of Oxford and the NERC Unit of Invertebrate Virology in Oxford 1 4 She remained at the NERC unit which was renamed the Institute of Virology and Environmental Microbiology IVEM rising to be its director in 1996 1 4 In 2001 IVEM merged with other bodies to become the NERC Centre for Ecology amp Hydrology and Nuttall served as the centre s director until 2011 2 During this period she oversaw the major restructuring of the centre 4 5 She subsequently directed national projects with NERC 1 2 She chaired the Partnership for European Environmental Research from 2008 to 2010 1 6 Nuttall has been professor of arbovirology in the Department of Zoology of the University of Oxford since 2013 1 3 She is a fellow of Wolfson College Oxford 7 Research edit nbsp Electron micrograph of tick borne encephalitis virusHer early research was on the cattle disease bovine viral diarrhoea Nuttall found that the bovine viral diarrhoea virus was often present as a contaminant in foetal bovine serum a commonly used laboratory reagent a result that was published in Nature in 1977 4 8 She then worked with ornithologist Chris Perrins trying to identify the virus responsible for puffinosis a disease that affects the Manx shearwater Puffinus puffinus sea bird 4 9 During this research Nuttall visited sea bird colonies and became interested in ticks arthropods that often infest sea birds as well as other vertebrates and can act as vectors for disease 4 Nonsystemic transmission edit In the early 1980s Nuttall started to study viruses transmitted by ticks initially focusing on orbiviruses nairoviruses and thogotoviruses 1 While performing experiments designed to explore whether Thogoto virus an influenza like virus can be transmitted between ticks during mating Nuttall and her colleagues unexpectedly found that control ticks became infected 4 They discovered that the virus can be transmitted between infected and uninfected ticks when they feed simultaneously on apparently uninfected guinea pigs without the virus being present at a detectable level in the blood 10 11 12 With Milan Labuda Nuttall subsequently demonstrated the same phenomenon with tick borne encephalitis virus a better understood arthropod transmitted virus 13 These results challenge the then accepted idea that arthropod transmitted viruses can only be transmitted when the arthropod vector feeds on an infected host in which the virus is replicating and circulating in the blood above a threshold level 4 11 12 14 Sarah Randolph comments Suddenly the conventional wisdom that systemic infections above a certain threshold level were necessary for transmission and could therefore be used to assay host competence was over turned Viraemia and even bacteraemia are now seen as an inconsistent species specific consequence of infection but not a necessary condition for transmission 12 The phenomenon of nonviraemic or nonsystemic transmission turns out to be widespread it has been subsequently observed with many other viruses transmitted by ticks black flies and mosquitos including major human pathogens such as West Nile virus as well as other pathogens including the spirochaete Borrelia burgdorferi which causes Lyme disease 11 15 16 and important in natural transmission 14 Nuttall s group has continued to study the phenomenon and have shown that immunity to tick borne encephalitis virus does not prevent nonsystemic transmission 17 Tick saliva edit nbsp The tropical bont tick whose saliva is the source of varieginNuttall s recent work has focused on discovering the function of tick saliva s many constituents as well as the mechanisms by which tick transmitted pathogens use them to enhance their transmission 3 Nuttall and colleagues were the first to show in 1989 that tick saliva promotes the transmission of viruses a phenomenon which they have called saliva assisted transmission this has been suggested as a mechanism for nonsystemic transmission 4 12 18 19 In 1998 she and her colleagues characterised three immunoglobulin binding proteins which were among the first proteins from tick saliva to be sequenced 12 20 21 With Norbert Fuchsberger Valeria Hajnicka and others Nuttall has shown that tick saliva suppresses the host s antiviral immune responses including natural killer cell activity and the induction of type I interferon and cytokines involved in inflammation 4 Her group has also shown that the proteins in saliva differ between individual ticks of the same species and also change over the course of feeding 20 Drugs and vaccines edit Some components of tick saliva have potential as drugs to treat a range of conditions unrelated to tick disease 3 22 Nuttall comments that These molecules have been refined by millions of years of evolution There are no toxicity problems they work on a range of animals they aren t fragile and there are an awful lot of them 22 For example with Guido Paesen Nuttall has characterised histamine binding proteins that can suppress inflammation in humans by binding directly to histamine rather than blocking its access to cell receptors of which at least four are known 4 22 23 One of these proteins rEV131 was investigated by NERC spin off company Evolutec for the treatment of hay fever and for use in recovery from cataract surgery 4 22 Another example is the anticoagulant variegin discovered by Nuttall and Maria Kazimirova in the tropical bont tick Amblyomma variegatum which represents a novel class of thrombin inhibitor it has been shown to prevent venous thrombosis in a zebrafish model 24 25 Tick saliva products are also possible targets for vaccines to control tick infestation and potentially to prevent the diseases they carry 3 20 One vaccine candidate explored by Nuttall s group is 64TRP a 15 kDa Rhipicephalus appendiculatus protein from the cement cone that glues the tick s mouthparts to the host Vaccination with 64TRP can protect against tick borne encephalitis virus carried by a different type of tick the castor bean tick Ixodes ricinus in a mouse model 20 26 Awards editNuttall received the Ivanovsky Medal for Virology of the Russian Academy of Sciences in 1996 4 She was awarded the OBE in the 2000 New Year Honours List for services to Environmental Science and Policy 27 Selected publications editBooks edit Nuttall PA Bowman AS eds 2008 Ticks Biology Disease and Control Cambridge University Press ISBN 978 0 521 86761 0Research papers edit Labuda M Trimnell AR Lickova M Kazimirova M Davies GM Lissina O Hails RS Nuttall PA 2006 An anti vector vaccine protects against a lethal vector borne pathogen PLOS Pathogens 2 4 e27 doi 10 1371 journal ppat 0020027 PMC 1424664 PMID 16604154 Paesen GC Adams PL Harlos K Nuttall PA Stuart DI 1999 Tick histamine binding proteins Isolation cloning and three dimensional structure Molecular Cell 3 5 661 71 doi 10 1016 s1097 2765 00 80359 7 PMID 10360182 Wang H Paesen GC Nuttall PA Barbour AG 1998 Male ticks help their mates to feed Nature 391 6669 753 54 Bibcode 1998Natur 391 753W doi 10 1038 35773 PMID 9486641 S2CID 4398008 Labuda M Kozuch O Zuffova E Eleckova E Hails RS Nuttall PA 1997 Tick borne encephalitis virus transmission between ticks cofeeding on specific immune natural rodent hosts Virology 235 1 138 43 doi 10 1006 viro 1997 8622 PMID 9300045 Jones LD Hodgson E Nuttall PA 1989 Enhancement of virus transmission by tick salivary glands Journal of General Virology 70 7 1895 98 doi 10 1099 0022 1317 70 7 1895 PMID 2544668 Jones LD Davies CR Steele GM Nuttall PA 1987 A novel mode of arbovirus transmission involving a nonviremic host Science 237 4816 775 77 Bibcode 1987Sci 237 775J doi 10 1126 science 3616608 PMID 3616608References edit a b c d e f g h Curriculum Vitae Epidemiology and Vaccinal Prevention website OOO Antorium retrieved 16 March 2015 a b c Professor Mark Bailey becomes acting Director of the Centre for Ecology amp Hydrology Centre for Ecology amp Hydrology website Natural Environment Research Council 1 March 2011 retrieved 16 March 2015 a b c d e Pat Nuttall Department of Zoology website University of Oxford retrieved 16 March 2015 a b c d e f g h i j k l m n Nuttall P 2003 An interview with Patricia Nuttall Ph D Vector Borne and Zoonotic Diseases 3 4 249 53 doi 10 1089 153036603322662228 PMID 14733676 House of Commons Science and Technology Committee Research Council Institutes Fourth Report of Session 2006 07 Vol 2 Oral and Written Evidence The Stationery Office pp Ev47 49 METIER Final Conference Schedule and Lecturers PDF Website Partnership for European Environmental Research retrieved 18 March 2015 Prof Patricia Nuttall website Wolfson College Oxford retrieved 16 March 2015 Nuttall PA Luther PD Stott EJ 1977 Viral contamination of bovine foetal serum and cell cultures Nature 266 5605 835 37 Bibcode 1977Natur 266 835N doi 10 1038 266835a0 PMID 194159 S2CID 4269062 Brooke M 2010 The Manx Shearwater A amp C Black pp 8 161 Jones LD Davies CR Steele GM Nuttall PA 1987 A novel mode of arbovirus transmission involving a nonviremic host Science 237 4816 775 77 Bibcode 1987Sci 237 775J doi 10 1126 science 3616608 JSTOR 1699212 PMID 3616608 a b c Higgs S Schneider BS Vanlandingham DL Klingler KA Gould EA 2005 Nonviremic transmission of West Nile virus Proceedings of the National Academy of Sciences of the United States of America 102 25 8871 74 Bibcode 2005PNAS 102 8871H doi 10 1073 pnas 0503835102 PMC 1157059 PMID 15951417 a b c d e Randolph SE 2009 Tick borne disease systems emerge from the shadows the beauty lies in molecular detail the message in epidemiology Parasitology 136 12 1403 13 doi 10 1017 s0031182009005782 PMID 19366480 S2CID 22845163 Labuda M Jones LD Williams T Danielova V Nuttall PA 1993 Efficient transmission of tick borne encephalitis virus between cofeeding ticks Journal of Medical Entomology 30 295 99 doi 10 1093 jmedent 30 1 295 PMID 8433342 a b Lord CC Tabachnick WJ 2002 Influence of nonsystemic transmission on the epidemiology of insect borne arboviruses A case study of vesicular stomatitis epidemiology in the Western United States Journal of Medical Entomology 39 3 417 26 doi 10 1603 0022 2585 39 3 417 PMID 12061433 Kuno G Chang GJ 2005 Biological transmission of arboviruses Reexamination of and new insights into components mechanisms and unique traits as well as their evolutionary trends Clinical Microbiology Reviews 18 4 608 37 doi 10 1128 cmr 18 4 608 637 2005 PMC 1265912 PMID 16223950 Patrican LA 1997 Acquisition of Lyme disease spirochetes by cofeeding Ixodes scapularis ticks American Journal of Tropical Medicine and Hygiene 57 5 589 93 doi 10 4269 ajtmh 1997 57 589 PMID 9392600 Labuda M Kozuch O Zuffova E Eleckova E Hails RS Nuttall PA 1997 Tick borne encephalitis virus transmission between ticks cofeeding on specific immune natural rodent hosts Virology 235 1 138 43 doi 10 1006 viro 1997 8622 PMID 9300045 Jones LD Hodgson E Nuttall PA 1989 Enhancement of virus transmission by tick salivary glands Journal of General Virology 70 7 1895 98 doi 10 1099 0022 1317 70 7 1895 PMID 2544668 Sonenshine DE Roe RM eds 2013 Biology of Ticks Volume 2 Oxford University Press a b c d Willadsen P 2004 Anti tick vaccines PDF Parasitology 129 S367 87 doi 10 1017 s0031182003004657 PMID 15938519 S2CID 40368916 Wang H Paesen GC Nuttall PA Barbour AG 1998 Male ticks help their mates to feed Nature 391 6669 753 54 Bibcode 1998Natur 391 753W doi 10 1038 35773 PMID 9486641 S2CID 4398008 a b c d Macilwain C 2006 Ticking the right boxes Nature 439 7076 533 Bibcode 2006Natur 439 533M doi 10 1038 439533a PMID 16452953 S2CID 4425421 Paesen GC Adams PL Harlos K Nuttall PA Stuart DI 1999 Tick histamine binding proteins Isolation cloning and three dimensional structure Molecular Cell 3 5 661 71 doi 10 1016 s1097 2765 00 80359 7 PMID 10360182 Koh CY Kazimirova M Trimnell A Takac P Labuda M Nuttall PA Kini RM 2007 Variegin a novel fast and tight binding thrombin inhibitor from the tropical bont tick Journal of Biological Chemistry 282 40 29101 13 doi 10 1074 jbc m705600200 PMID 17684009 Drugs designed by nature could prevent heart attacks and blood clots Centre for Ecology amp Hydrology website Natural Environment Research Council retrieved 18 March 2015 Labuda M Trimnell AR Lickova M Kazimirova M Davies GM Lissina O Hails RS Nuttall PA 2006 An anti vector vaccine protects against a lethal vector borne pathogen PLOS Pathogens 2 4 e27 doi 10 1371 journal ppat 0020027 PMC 1424664 PMID 16604154 New Year Honours List United Kingdom The London Gazette 55710 15 31 December 1999 Retrieved from https en wikipedia org w index php title Pat Nuttall amp oldid 1188159018, wikipedia, wiki, book, books, library,

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