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CHAPTER  2:   Materials and Methods 42

3.1   Introduction 58

 

Many  recombinant  enteroviruses  have  been  isolated  and  characterised  from  field  samples   following  outbreaks  of  infection  (Kew  et  al.,  2002,  Zhang  et  al.,  2010,  Oberste  et  al.,  2004a).   Early  studies  have  highlighted  potential  triggers  found  in  the  RNA  sequence  and  RNA  secondary   structure  that  provides  preferential  sites  for  recombination  (section  1.3).  However,  the  

mechanisms  of  recombination  still  remain  poorly  understood.  The  field  isolates  studied  in  all   examples  have  been  exposed  to  a  highly  selective  and  dynamic  environment,  and  may  not   necessarily  represent  the  initial  recombinant  molecules  produced.  Characterising  the  

mechanisms  that  drive  recombination  will  help  us  understand  a  basic  evolutionary  mechanism.   Additionally,  potential  strategies  to  limit  the  occurrences  of  such  events  can  be  developed.  This   would  be  helpful  in  the  fight  to  eradicate  poliovirus  for  example;  production  of  a  live  attenuated   vaccine  strain  that  doesn’t  recombine  would  be  very  beneficial  to  this  process.  

 

Recombination  is  a  rare  event,  with  intertypic  recombinants  estimated  to  have  frequencies  of   1x  10-­‐6  (Kirkegaard  and  Baltimore,  1986b,  Jiang  et  al.,  2007).  Identification  of  recombinant  

genomes  in  a  population  that  is  predominately  made  up  of  parental  viruses  has  therefore  been   an  issue  in  all  cell  based  studies.  Early  in  vitro  approaches  have  largely  relied  upon  crossing   parental  genomes  carrying  different  selectable  markers.  Those  that  ‘escape’  the  selection   process  will  have  inherited  the  mutations  from  the  two  parental  strains  and  would  be   recombinant  viruses  (Kirkegaard  and  Baltimore,  1986a).  There  is  no  doubt  that  such  studies   have  provided  some  interesting  observations,  most  notably  the  ‘copy-­‐choice’  model  of  

recombination  (section  1.3).  Although,  identification  of  the  recombinant  viruses  isolated  under   such  selective  pressures  was  limited  to  only  a  small  region  of  the  genome  as  defined  by  the   selectable  markers  and  may  again  not  have  represented  the  initial  recombination  event.  An   additional  risk  of  reversion  is  also  a  possibility  in  such  approaches,  with  a  point  mutation   reverting  a  genome  back  to  wild  type  around  10-­‐100  fold  more  likely  that  an  intertypic   recombination  event  (Crotty  et  al.,  2001).  To  overcome  such  issues,  a  novel  in  vitro  assay  has  

been  developed  by  a  previous  student  (Kym  Lowry)  that  uses  two  defective  parental  genomes   that  are  each  unable  to  generate  infectious  virus.  Only  a  recombination  event  can  produce  a   genome  that  can  be  potentially  infectious.  

 

Methodology  

 

The  first  parental  RNA  is  a  sub-­‐genomic  replicon  that  has  a  large  deletion  of  the  virus  genome.   The  capsid  region  (P1)  was  replaced  with  a  reporter  gene;  in  this  study  it  is  a  firefly  luciferase   gene.  This  type  of  genome  can  translate  and  replicate  successfully  as  it  contains  the  key  cis-­‐

acting  elements  and  is  a  well  established  approach  used  to  study  polioviruses  (Barclay  et  al.,   1998,  Percy  et  al.,  1992).  The  lack  of  a  capsid  region  ensures  no  virus  particles  are  produced   when  transfected  into  permissive  cells  alone.  In  any  recombination  assay  this  genome  would   provide  the  non-­‐structural  P2  and  P3  regions,  and  is  therefore  considered  the  ‘donor’.  The   second  genome  (the  acceptor  in  a  recombination  event)  would  be  required  to  produce  the   capsid-­‐coding  region,  but  carry  a  defect  in  the  non-­‐structural  region  preventing  production  of  a   viable  virus  upon  transfection.  A  suitable  candidate  is  the  well  characterised  genome  that   carries  eight  synonymous  mutations  in  the  highly  conserved  2C  CRE  that  disrupts  positive   strand  RNA  synthesis  (Goodfellow  et  al.,  2003a).  This  genome  can  produce  negative  strand  RNA   so  is  considered  suitable  for  a  replicative  recombination  assay,  as  it  is  believed  recombination   occurs  during  negative  strand  synthesis  (Kirkegaard  and  Baltimore,  1986b).  This  approach   relies  upon  delivering  both  RNA  templates  into  cells,  via  transfection,  where  subsequent   recombination  and  genomic  re-­‐arrangements  can  occur.  Donation  of  a  capsid  from  one  parental   genome  and  a  functional  CRE  from  the  other  parental  genome  would  in  principle  produce  a   viable  virus,  and  is  termed  the  CRE-­‐REP  assay  (figure  3.1).  In  principle,  this  provides  a  region  of   1.058  Kb,  between  the  end  of  VP1  and  the  2C  CRE,  where  recombination  can  occur.  Importantly,   the  use  of  rodent  cell  lines  like  the  murine  L929  or  baby  hamster  BsrT7  cells  allows  minimal   selection  of  recombinant  virus  as  is  possible.  Both  cell  types  lack  the  poliovirus  receptor  CD155,   but  can  support  RNA  replication.  They  are  therefore  deemed  permissive  but  not  susceptible  to   infection.  Any  recombinant  virus  produced  and  released  from  the  cell  into  the  media  

isolated  and  characterised  as  near  to  the  recombination  event  as  possible.  Additionally,  by   minimising  selection,  this  approach  allows  isolation  of  a  range  of  recombinant  regardless  of   growth  advantages.  This  is  in  contrast  to  previous  in  vitro  cell  based  approaches  that  have   largely  used  HeLa  cells  that  are  susceptible  to  re-­‐infection  due  to  the  availability  of  receptor.   This  may  have  biased  the  identification  of  recombinant  viruses  to  the  ones  that  had  a  growth   advantage  over  others.  Quantification  of  any  recombinant  virus  is  by  plaque  assay,  media   supernatant  is  isolated  from  transfected  rodent  cells  following  an  incubation  period  and   subsequently  used  with  permissive  and  susceptible  cell  lines  like  HeLa  (section  2.1  for  full   description).  

 

The  CRE-­‐REP  has  allowed  various  combinations  of  enterovirus  partners  to  be  used  previously   (Lowry  et  al.,  2014).  The  primary  enterovirus  serotypes  studied  in  this  investigation  were   poliovirus  type  1  (Mahoney)  and  type  3  (Leon).  This  was  due  to  the  availability  of  cDNA,  the   subsequent  re-­‐producibility  of  the  CRE-­‐REP  assay  when  using  these  partners  (outlined  in  text   later),  and  the  vast  amount  of  past  research  into  the  life  cycle  of  this  virus.    

 

Aims  

The  aim  was  to  build  upon  the  findings  of  a  previous  student,  Kym  Lowry.  These  included:   comparing  intratypic  and  intertypic  poliovirus  recombination  frequencies,  characterisation  of   early  intratypic  and  intertypic  recombinant  isolates,  cell  specificity  and  characterisation  of  early   intertypic  recombinants  to  those  following  serial  passage.  In  addition,  it  was  felt  important  to   develop  a  non-­‐replicative  recombination  assay  that  would  contrast  the  CRE-­‐REP  assay,  which   was  presumed  to  be  replicative  i.e.  recombinant  virus  genome  produced  during  replication  of   the  parental  RNA.  This  would  determine  if  the  recombinant  progeny  was  produced  via  a   replicative  mechanism  like  ‘copy-­‐choice’,  whilst  also  highlighting  the  relative  contribution  of   non-­‐replicative  recombination  to  the  overall  yield  of  virus.  The  results  in  this  chapter  have   contributed  to  the  manuscript  Lowry  et  al.,  2014.  

     

 

 

Figure  3.1:  Overview  of  the  CRE-­‐REP  assay  

Two  genomes,  upper  [dark  shading]  bears  a  defective  CRE  indicated  as  a  broken  line  with  a   superimposed  X  in  the  2C-­‐coding  region.  Lower  genome  is  a  luciferase-­‐encoding  sub-­‐genomic   replicon  (light  shading).    Following  co-­‐transfection  into  permissive  cells  (indicated  by  an   arrow),  a  recombinant  replication  competent  genome  may  be  recovered  of  the  generic  structure   shown,  consisting  of  the  5’  part  of  the  genome  derived  from  the  CRE-­‐defective  parent  (the   recipient)  and  the  3’  part  of  the  genome  from  the  luciferase-­‐encoding  replicon  (the  donor).    The   graduated  shading  between  the  3’  end  of  the  VP1-­‐coding  region  and  the  2C  CRE  indicates  the   area  within  which  recombination  must  occur  to  produce  a  functional  genome.  

 

 

 

 

 

 

 

 

 

 

 

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VP4 VPg VP1 VP3 VP2 2A 2B 2C 3A 3C 3D 2A 2B 2C 3A 3C 3D luc VP1 VP3 VP2 3A 3C 3D Crossover region 5’ NCR 3’ NCR CRE

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Co-transfect RNA to permissive cells Clone by limit dilution PCR and sequence analysis Serial passage Further analysis Growth analysis

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PV3/PV3 PV1/PV3 10 100 1000 pfu/ml * pT7Rep3-L pT7/SL3 GuHCl

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