Table Of ContentGenetic Control of Malaria
and Dengue
Genetic Control of
Malaria and Dengue
Edited by
Zach N. Adelman
FralinLife Science Institute and Department ofEntomology,
VirginiaTech, Blacksburg, VA, USA
AMSTERDAM(cid:129)BOSTON(cid:129)HEIDELBERG(cid:129)LONDON
NEWYORK(cid:129)OXFORD(cid:129)PARIS(cid:129)SANDIEGO
SANFRANCISCO(cid:129)SINGAPORE(cid:129)SYDNEY(cid:129)TOKYO
AcademicPressisanimprintofElsevier
AcademicPressisanimprintofElsevier
125,LondonWall,EC2Y5AS.
525BStreet,Suite1800,SanDiego,CA92101-4495,USA
225WymanStreet,Waltham,MA02451,USA
TheBoulevard,LangfordLane,Kidlington,OxfordOX51GB,UK
Copyrightr2016ElsevierInc.Allrightsreserved.
Nopartofthispublicationmaybereproducedortransmittedinanyformorbyanymeans,electronic
ormechanical,includingphotocopying,recording,oranyinformationstorageandretrievalsystem,
withoutpermissioninwritingfromthepublisher.Detailsonhowtoseekpermission,further
informationaboutthePublisher’spermissionspoliciesandourarrangementswithorganizations
suchastheCopyrightClearanceCenterandtheCopyrightLicensingAgency,canbefoundatour
website:www.elsevier.com/permissions.
Thisbookandtheindividualcontributionscontainedinitareprotectedundercopyrightbythe
Publisher(otherthanasmaybenotedherein).
Notices
Knowledgeandbestpracticeinthisfieldareconstantlychanging.Asnewresearchandexperience
broadenourunderstanding,changesinresearchmethods,professionalpractices,ormedicaltreatment
maybecomenecessary.
Practitionersandresearchersmustalwaysrelyontheirownexperienceandknowledgeinevaluating
andusinganyinformation,methods,compounds,orexperimentsdescribedherein.Inusingsuch
informationormethodstheyshouldbemindfuloftheirownsafetyandthesafetyofothers,including
partiesforwhomtheyhaveaprofessionalresponsibility.
Tothefullestextentofthelaw,neitherthePublishernortheauthors,contributors,oreditors,assume
anyliabilityforanyinjuryand/ordamagetopersonsorpropertyasamatterofproductsliability,
negligenceorotherwise,orfromanyuseoroperationofanymethods,products,instructions,orideas
containedinthematerialherein.
ISBN:978-0-12-800246-9
BritishLibraryCataloguing-in-PublicationData
AcataloguerecordforthisbookisavailablefromtheBritishLibrary.
LibraryofCongressCataloging-in-PublicationData
AcatalogrecordforthisbookisavailablefromtheLibraryofCongress.
ForInformationonallAcademicPresspublications
visitourwebsiteathttp://store.elsevier.com/
Publisher:SaraTenney
AcquisitionEditor:JillLeonard
EditorialProjectManager:FentonCoulthurst
ProductionProjectManager:ChrisWortley
Designer:MarkRogers
PrintedandboundintheUnitedStatesofAmerica
List of Contributors
ZachN.Adelman, FralinLifeScienceInstituteandDepartmentofEntomology,
VirginiaTech,Blacksburg,VA,USA
OmarS.Akbari, DepartmentofEntomology,UniversityofCalifornia,Riverside,
CA,USA
TimAntonelli, DepartmentofMathematics,WorcesterStateUniversity,Worcester,
MA,USA
RobertoBarrera, EntomologyandEcologyActivity,DengueBranch,Centersfor
DiseaseControlandPrevention,SanJuan,PuertoRico
SanjayBasu, FralinLifeScienceInstituteandDepartmentofEntomology,Virginia
Tech,Blacksburg,VA,USA
MarkQ.Benedict, CentersforDiseaseControlFoundation,Atlanta,GA,USA
JamesK.Biedler, DepartmentofBiochemistry,VirginiaTech,Blacksburg,VA,
USA;FralinLifeScienceInstitute,VirginiaTech,Blacksburg,VA,USA
BenjaminJ.Blumberg, W.HarryFeinstoneDepartmentofMolecularMicrobiology
andImmunologyandtheJohnsHopkinsMalariaResearchInstitute,Bloomberg
SchoolofPublicHealth,JohnsHopkinsUniversity,Baltimore,MD,USA
MargarethL.Capurro, UniversidadedeSa˜oPaulo,Sa˜oPaulo,Brazil
DaniloO.Carvalho, UniversidadedeSa˜oPaulo,Sa˜oPaulo,Brazil
AmandaClayton, DepartmentofEconomics,NorthCarolinaStateUniversity,
Raleigh,NC,USA
JanE.Conn, TheWadsworthCenter,NewYorkStateDepartmentofHealth,
Albany,NY,USA;BiomedicalSciencesDepartment,SchoolofPublicHealth,
StateUniversityofNewYork-Albany,Albany,NY,USA
MamadouB.Coulibaly, MalariaResearchandTrainingCenter,Universityof
Sciences,TechniquesandTechnologiesofBamako,Bamako,Mali
GeorgeDimopoulos, W.HarryFeinstoneDepartmentofMolecularMicrobiology
andImmunologyandtheJohnsHopkinsMalariaResearchInstitute,Bloomberg
SchoolofPublicHealth,JohnsHopkinsUniversity,Baltimore,MD,USA
YaraA.Halasa, SchneiderInstitutesforHealthPolicy,HellerSchool,Brandeis
University,Waltham,MA,USA
BrantleyA.Hall, FralinLifeScienceInstitute,VirginiaTech,Blacksburg,VA,
USA;InterdisciplinaryPhDPrograminGenetics,Bioinformatics,and
ComputationalBiology,VirginiaTech,Blacksburg,VA,USA
xv
xvi ListofContributors
MollyHartzog, DepartmentofCommunication,Rhetoric,andDigitalMedia,North
CarolinaStateUniversity,Raleigh,NC,USA
AnthonyA.James, DepartmentofMolecularBiologyandBiochemistry,University
ofCalifornia,Irvine,CA,USA;DepartmentofMicrobiology&Molecular
Genetics,UniversityofCalifornia,Irvine,CA,USA
XiaofangJiang, FralinLifeScienceInstitute,VirginiaTech,Blacksburg,VA,USA;
InterdisciplinaryPhDPrograminGenetics,Bioinformatics,andComputational
Biology,VirginiaTech,Blacksburg,VA,USA
DeepakJoshi, DepartmentofMicrobiologyandMolecularGenetics,MichiganState
University,EastLansing,MI,USA
RheaLongley, FacultyofTropicalMedicine,MahidolVivaxResearchUnit,
MahidolUniversity,Bangkok,Thailand;TheWalterandElizaHallInstituteof
MedicalResearch,Melbourne,VIC,Australia
VanessaMacias, DepartmentofMolecularBiologyandBiochemistry,Universityof
California,Irvine,CA,USA
JohnM.Marshall, DivisionofBiostatistics,SchoolofPublicHealth,Universityof
California,Berkeley,CA,USA
ConorJ.McMeniman, DepartmentofMolecularMicrobiologyandImmunology,
MalariaResearchInstitute,JohnsHopkinsBloombergSchoolofPublicHealth,
Baltimore,MD,USA
KevinM.Myles, FralinLifeScienceInstituteandDepartmentofEntomology,
VirginiaTech,Blacksburg,VA,USA
HectorQuemada, BiosafetyResourceNetwork,InstituteofInternationalCrop
Improvement,DonaldDanforthPlantScienceCenter,St.Louis,MI,USA
PauloE.Ribolla, DepartamentodeParasitologia,InstitutodeBiocieˆncias,
UniversidadeEstadualPaulista“Ju´liodeMesquitaNeto”,Botucatu,Sa˜oPaulo,
Brazil
JetsumonSattabongkot, FacultyofTropicalMedicine,MahidolVivaxResearch
Unit,MahidolUniversity,Bangkok,Thailand
PatriciaY.Scaraffia, DepartmentofTropicalMedicine,Vector-BorneInfectious
DiseaseResearchCenter,SchoolofPublicHealthandTropicalMedicine,Tulane
University,NewOrleans,LA,USA
MaxwellJ.Scott, DepartmentofEntomology,NorthCarolinaStateUniversity,
Raleigh,NC,USA
DonaldS.Shepard, SchneiderInstitutesforHealthPolicy,HellerSchool,Brandeis
University,Waltham,MA,USA
SarahM.Short, W.HarryFeinstoneDepartmentofMolecularMicrobiologyand
ImmunologyandtheJohnsHopkinsMalariaResearchInstitute,Bloomberg
SchoolofPublicHealth,JohnsHopkinsUniversity,Baltimore,MD,USA
RobertE.Sinden, TheJennerInstitute,TheUniversityofOxford,Oxford,UK;The
DepartmentofLifeSciences,ImperialCollegeLondon,SouthKensington,UK
PatcharaSriwichai, FacultyofTropicalMedicine,DepartmentofMedical
Entomology,MahidolUniversity,Bangkok,Thailand
ListofContributors xvii
YeyaT.Toure´, MalariaResearchandTrainingCenter,UniversityofSciences,
TechniquesandTechnologiesofBamako,Bamako,Mali
SekouF.Traore´, MalariaResearchandTrainingCenter,UniversityofSciences,
TechniquesandTechnologiesofBamako,Bamako,Mali
ZhijianJ.Tu, DepartmentofBiochemistry,VirginiaTech,Blacksburg,VA,USA;
FralinLifeScienceInstitute,VirginiaTech,Blacksburg,VA,USA;
InterdisciplinaryPhDPrograminGenetics,Bioinformatics,andComputational
Biology,VirginiaTech,Blacksburg,VA,USA
EduardoA.Undurraga, SchneiderInstitutesforHealthPolicy,HellerSchool,
BrandeisUniversity,Waltham,MA,USA
SophiaWebster, DepartmentofEntomology,NorthCarolinaStateUniversity,
Raleigh,NC,USA
ZhiyongXi, DepartmentofMicrobiologyandMolecularGenetics,MichiganState
University,EastLansing,MI,USA
GabrielZilnik, DepartmentofEntomology,NorthCarolinaStateUniversity,
Raleigh,NC,USA
Biography
CHAPTER 1
Tim Antonelli is an IGERT fellow and a PhD student in Biomathematics at
North Carolina State University. He is interested in modeling how mosquito
populations react to various control strategies, including the release of genet-
icallymodified mosquitoes thatareunabletotransmit disease.He also works
on parameter identifiability and parameter estimation for mosquito models
using data collectedfrom Iquitos, Peru.
Amanda Clayton received her BA in Economics from Illinois Wesleyan
University. She is currently an IGERT fellow and a PhD student in
Economics at North Carolina State University. Her research interests include
microeconomic development, global health, feminist economics, and the
policy and regulation ofgenetic engineering technologies.
MollyH.StormentisanIGERTfellowandaPhDstudentinCommunication,
Rhetoric, and Digital Media at North Carolina State University. Broadly
speaking,shestudieshowlanguageshapesknowledgeproductioninthesciences.
Her dissertation explores the influence of digital informationtechnologies, such
astheGenBankdatabase,oninventioningeneticengineering.
Sophia Webster is an IGERT fellow and a PhD student in Entomology at
North Carolina State University. Under the direction of Dr. Max Scott,
she works with the dengue mosquito vector, Aedes aegypti, to develop gene
drivesystems for mosquito population suppression andreplacement.
Gabriel Zilnik received his BA in Anthropology from Arizona State
University where he became interested in the evolutionary effects of agri-
culture on arthropods. Gabriel is currently an IGERT fellow and a PhD
student in Entomology, studying the genetics of adaptation using juvenile-
hormonedisruptinginsecticidesasasystemunderthetutelageofFredGould.
CHAPTER 2
Maxwell J. Scott began his career working on the chromatin structure of
steroid hormone inducible genes in chickens. A continued interest in
epigenetics but a desire to work on a system with better genetic tools led to
studies on X chromosome dosage compensation in Drosophila melanogaster.
This work led to arealization that the sex determination and dosage compen-
sation genetic regulatory systems could potentially be manipulated to make
xix
xx Biography
male-only strains of insect pests. His lab has continued to investigate epige-
netic regulatory mechanisms in Drosophila and to develop conditional
female lethal strains of insect pests. The latter has been mostly on the
Australian sheep blowfly and the New World screwworm fly, which are
major pests of livestock. He is currently a Professor in the Department of
Entomology, North Carolina State University,Raleigh, NC, USA.
Mark Q. Benedict began his career working on Anopheles albimanus
classical and aberration genetics in a laboratory developing tools for genetic
control. His interests have continued in this vein and have ranged from
developing genetic sexing strains, studying species complexes, germline
transformation methods, predicting species distributions in the context of
control, molecular biology and biosafety. In addition, he has published
papers on mosquito physiology and larval development density effects. He
led the vector activities of the Malaria Research and Reference Reagent
Resource Center (MR4) and led the mosquito SIT group at the International
Atomic Energy Agency (IAEA) where he developed methods, field sites,
and equipment for mass-rearing. He is currently a research biologist at the
CDC Foundation in Atlanta, GA, USA.
CHAPTER 3
Mamadou B. Coulibaly is a graduate from the University of Notre Dame
(2006). Since then, Dr. Coulibaly has been back in Mali where he leads a
research laboratory at the Malaria Research and Training Center at the
University of Sciences, Techniques and Technologies of Bamako. His lines
of research include developing novel genetic approaches for malaria vector
control. He is also involved in operational research oriented toward malaria
vector control (ITNs/LLINs, IRS) to help making informed decisions by
policymakers.
Sekou F. Traore´ is currently the Director of the Malaria Research and
Training Center Entomology/Mali ICER (International Center for Excellence
in Research). He has more than 20 years of experience as a specialist in
Entomology and control of vector-borne diseases in developing countries.
His current research involves field and laboratory studies on malaria, leish-
maniasis, filariasis, and recurrent tick-borne fevers. Additional research
lines involve interdisciplinary studies on vector-borne diseases in both urban
and rural environments, development and field-testing improved methods for
vectorcontrol.
Yeya T. Toure´led the Malaria Research and Training Center up to 2001
when he joined the Tropical Disease Research program at the World Health
Organization (TDR/WHO). “He played an essential role in stimulating
research molecular biology, genetics, and genomics of tropical disease
vectors. This led to the completion of the genome sequence of the malaria
mosquito, the Anopheles gambiae, which opened opportunities to better
Biography xxi
understand vector biology and insecticide resistance mechanisms and
develop new tools” (credit; Jamie Guth, WHO senior communication man-
ager, 2014). Prof. Toure retired from TDR/WHO when he was leading the
unit for vectors, environment, and society research.
CHAPTER 4
Patchara Sriwichai received her PhD in Tropical Medicine at the Faculty of
Tropical Medicine, Mahidol University in 2007. She is currently a lecturer in
the Department ofMedical Entomology at this faculty. She has experience in
medical entomology of Tropical disease. Her research focus is on malaria(cid:1)
vector relationship, vector biology, disease transmission, vector competency
and insect immunity specifically related to vector(cid:1)parasite interaction, as
well as vector surveillance, prediction, and evaluation of vector capacity in
the endemic areas. Sheis alsointerested inmalaria elimination programsand
utilization of integration of vector control tools. Some of her previous work
has involved protein targets that have potential to be malaria transmission
blockingvaccines.
Rhea Longley is a postdoctoral researcher at the Mahidol Vivax Research
Unit, Mahidol University, Thailand, and the Walter and Eliza Hall Institute
of Medical Research, Australia, where she researchers Plasmodium vivax
malaria. Her current work focuses on understanding the human immune
response to P. vivax, and how this can be used to eliminate malaria from the
Asia Pacific region. She received her PhD in 2014 from the University of
Oxford,and was a2010 Rhodes scholar.
Jetsumon Sattabongkot (Prachumsri) was a senior scientist for more than
25 years at the USA Medical Component, Armed Forces Research Institute
of Medical Sciences (AFRIMS), an oversea laboratory of the Walter Reed
Army Institute of Research, Bethesda, MD, USA. She has moved to the
Faculty of Tropical Medicine, Mahidol University in 2011 to establish the
Mahidol Vivax Research Unit, where she is the director of the unit. This unit
is under Center of Excellence for Malaria. Her research focus is on malaria
transmission and epidemiology, biology of different stages of malaria para-
sites in human and mosquito vectors, new tools for diagnosis and surveil-
lance,andevaluationoftoolsformalariacontrolandeliminationsuchas,but
not limited to, integrated vector control, transmission blocking vaccines,
antiliverstagecompounds,etc.Shehasinternational collaborationworldwide
andpublishedmorethan152papersunderJ.SattabongkotandJ.Prachumsri.
CHAPTER 5
Jan E. Conn is a biologist who conducts research on malaria vector adapta-
tion, genetics, and ecology in the Neotropics. She is a Research Scientist at
the Wadsworth Center, New York State Department of Health, and Professor
xxii Biography
in the Biomedical Sciences Department at the School of Public Health at
SUNY-Albany.
Paulo E. Ribolla is a biologist with a specialization in Biochemistry
and Molecular Biology who conducts research on different aspects of
neglected diseases in Brazil. He is an Associate Professor at the University
of Sa˜o Paulo, lecturing in Human Parasitology. His lab develops projects on
dengue, malaria,and leishmaniasis.
CHAPTER 6
Roberto Barrera conducted his first studies on the ecology of Aedes aegypti
in 1977, when he was pursuing the biology degree at the Central University
of Venezuela (UCV). He continued investigating the ecology of mosquitoes
inhabiting natural and artificial containers and obtained his PhD from the
Ecology Program at Pennsylvania State University in 1988. He did a post-
doctoral at the Entomology Department, University of Florida (1994(cid:1)1995).
After retiring as a full Professor from UCV, he accepted a position as
Entomology and Ecology Activity Chief, Dengue Branch, CDC in 2003. His
main research interests are vector ecology and control and eco-epidemiology
of vector-borne pathogens, such as dengue.
CHAPTER 7
Robert E. Sinden has for the past 40 years studied the cell biology of malaria
parasites, in particular of the sexual stages and biology of transmission—on
which he has published approximately 300 papers. He has contributed to
global reviews of malaria research activities (MalERA) and remains a strong
advocate of the “rediscovered” philosophy of attacking malarial parasites not
only to reduce clinical disease in the infected patient, but more importantly
to achieve stable/sustainable reductions in transmission between persons in
endemic communities. His research team is currently focusing on translating
the knowledge acquired from previous basic research into the discovery,
development and implementation of effective transmission-blocking drugs
and vaccines. He is currently Head of Malaria Cell Biology at the Jenner
Institute, the UniversityofOxford.
CHAPTERS 8, 13
Zach N. Adelman is an associate professor in the Department of Entomology
and Fralin Life Science Institute at Virginia Tech. Following earlier work on
the generation of pathogen-resistant mosquitoes and the development of
novel mosquito promoters, Dr. Adelman’s research has more recently
focused on the development of novel gene editing/gene replacement
