Mariangela Bonizzoni
Mariangela Bonizzoni
affiliation: Università di Pavia
research area(s): Immunity And Infection, Computational Biology
Course: Genetics, Molecular and Cellular Biology
University/Istitution: Università di Pavia
Mariangela Bonizzoni

Dep. Biology and Biotechnology
University of Pavia
Via Ferrata 9, 27100 Pavia (Italy)

Tel: xx39 0382 986324

Research Unique Identifier: ORCID ID 0000-0003-0568-8564
ERC field of expertise: LS2, LS8, LS9
SSD: Bio05/B1

11/2018 PROFESSOR of ZOOLOGY, University of Pavia
03/2015 to present ASSOCIATE PROFESSOR of ZOOLOGY, University of Pavia
2011-2015 ASSISTANT PROJECT SCIENTIST, Program in Public Health, University of California at Irvine, USA
2007-2011 POSTDOCTORAL FELLOW, University of California at Irvine, USA
2004-2006 POSTDOCTORAL FELLOW, Biology Department, University of Basilicata, Italy
2004 Combined Italian-French PhD
Cellular Biology, University of Pavia, Italy
Genes, Genomes, Cellules, Universite’ de Paris XI, France
1997 Master in Molecular Biology
Dept. Animal Biology, University of Pavia

2017-2020 Human Science Frontier Program RGP0007/2017 (M. Bonizzoni)
Exploring the concept of adaptive immunity to viruses in mosquitoes
Role: PI
2016-2021 ERC Consolidator NIRVHOSTINT (M. Bonizzoni)
Population genomics of co-evolution between nonretrovirla RNA viruses and their hosts
Role: PI
2009-2014 PSWRCE-U54-A165359 (A.A. James)
Mosquito innate immune response to arbovirus infection
Role: Co-investigator
2012-2015 NIH R21 AI098652-01 (M. Bonizzoni)
Transcriptomics and Population Genetics of Mosquito Resistance to Pyrethroids

2017 Organizer and board member of the 3rd International Workshop on Aedes albopictus, the Asian tiger mosquito (Pavia, Italy, April 10-12, 2017)
2016 Organizer of the Symposium “Role of microbiota in vectors” to be presented at ICE 2016, XXV International Congress of Entomology Orlando Sept. 25-30, 2016
2013 Organizer and board member of the 1st International Workshop on Aedes albopictus, the Asian tiger mosquito (Pavia, Italy, March 21-22, 2013)

2017 Member of the InRoad Project, University of Pavia
2015 Ad hoc reviewer for the Netherlands Organization for Scientific Research, VICI Scheme
2014 NIH-NIAD review panel member for R13 and "International Collaborations in Infectious Diseases Research" U01 and U19 grants

2014 to present Invited Associate Editor for PLoS Neglected Tropical Diseases
2012-current Associate Editor for BMC Genetics
2007 to present Scientific Reviewer for PNAS, Genetica, Diversity and Distributions, Journal of Insect Science, Journal of Applied Entomology, Journal of Medical Entomology, Molecular Ecology, Bulletin of Entomological Research, Infection Genetics and Evolution, Journal of Insect Physiology, BMC Genomics, PLoS Neglected Tropical Diseases, PLoS One and Heredity

From 2015 Zoology (Modulo, 6 CFU Corso B) Laurea triennale in Scienze Biologiche
Molecular Entomology (6 CFU) Laurea Magistrale in “Molecular Biology and Genetics”
May 2017 Lecture in the course Frontiers in Molecular Biology “Model systems in molecular biology research: from basci processes to human diseases”, Dottorato in Genetica, Biologia Molecolare e Cellulare, Universita’ degli Studi di Pavia
2014-2015 Applied Zoology (Modulo, 6 CFU Corso B) Laurea triennale in Scienze Biologiche
2014 Guest Lectures in Vector Biology, Human Parasitology, University of California at Irvine
A well-known idiom dictates that “prevention is better than cure”. There are limited vaccines and no therapeutic treatments available for many arthropod-borne diseases. The only proven and consistent method of preventing transmission of the pathogens that cause these diseases is to act on the vectors by suppressing their contact to humans. My research agenda is guided by the above-mentioned idiom and aims at reducing the negative impact of insects on human health by studying aspects of insect biology that could be leveraged to develop innovative strategies of insect control.

Briefly, my main research interests are as follows:

Co-evolution between arthropod vectors and arboviruses.
Emerging or resurging infectious diseases include several caused by arthropod-borne viruses (arboviruses). An example is dengue, with 100 million people infected annually. Despite having different replication strategies, all arboviruses are maintained in a natural cycle involving transmission by the bite of an infected hematophagous arthropod (vector) to a vertebrate host. Once infected with an arbovirus, the vector becomes persistently infected for life. Mosquito competence for arboviruses is a complex and evolving phenotype because it depends on the interaction of genetic factors from both mutation-prone RNA viruses and mosquito vectors with environmental variables. Understanding the genetic components of vector competence and how these genetic elements are distributed in natural populations and interact with environmental factors is essential for predicting the risk of arboviral diseases and for developing new transmission-blocking strategies. I use the tools from a number of scientific disciplines to probe the complicated biology of vector-mediated pathogen transmission, with a current focus on mosquito genomics and immunity pathways.
Recent References:
1. Houé, V., Bonizzoni, M., Failloux, A. Endogenous non-retroviral elements in genomes of Aedes mosquitoes and vector competence. Emerging Microbes and Infections 8(1): 542-555.
2. Souza-Neto, J.A., Powell, J.R., Bonizzoni, M. Aedes aegypti vector competence studies: a review. (2019) Infection, Genetics and Evolution 67: 191-209.
3. Pischedda, E., Scolari, F., Valerio, F., Carballar-Lejarazu, R., Catapano, P.L., Watershouse, R.M., Bonizzoni, M. Insights Into an Unexplored Component of the Mosquito Repeatome: Distribution and Variability of Viral Sequences Integrated Into the Genome of the Arboviral Vector Aedes albopictus (2019) Frontiers in Genetics fgene.2019.00093

Insecticide resistance in vectors.
Insecticide resistance is recognized as one of the main obstacles in the malaria elimination/eradication agenda. Understanding the molecular mechanisms of insecticide resistance will provide the tools to derive markers to predict resistance and possibly identify targets for novel insecticide formulations. I applied transcriptomics and molecular ecology approaches to study insecticide resistance mechanisms and the emergence of resistance in malaria and arboviral vectors.

Recent References:
1. Machani, M.G., Ochomo, E., Sang, D., Bonizzoni, M., Zhou, G., Githeko, A., Yan, G., Afrane, Y.A. Influence of blood meal and age of mosquitoes on susceptibility to pyrethroids in Anopheles gambiae from Western Kenya. Malaria Journal 18(1): 112.
2. Xu, J., Su, X., Bonizzoni, M., Zhong, D., Li, Y., Zhou, G., Nguyen, H., Tong, S., Yan, G., Chen, X.-G.Comparative transcriptome analysis and RNA interference reveal CYP6A8 and SNPs related to pyrethroid resistance in Aedes albopictus (2018) PLoS Neglected Tropical Diseases, 12:e0006828.
3. Xu, J., Bonizzoni, M., Zhong, D., Zhou, G., Cai, S., Li, Y., Wang, X., Lo, E., Lee, R., Sheen, R., Duan, J., Yan, G., Chen, X.-G. Multi-country Survey Revealed Prevalent and Novel F1534S Mutation in Voltage-Gated Sodium Channel (VGSC) Gene in Aedes albopictus (2016) PLoS Neglected Tropical Diseases: e0004696

Population genetic analyses and studies of invasion/diffusion processes.
Population genetic approaches are informative in the analyses of the genetic plasticity of an organism, in assessing its demographic history, in studying its spread and the widespread of key features such as mutations associated with insecticide resistance. I characterized and applied molecular markers to understand the population genetic structure and the invasion/diffusion potentials of different organisms.

Recent References:
1. Lo, E., Bonizzoni, M., Hemming-Schroeder, E., Ford, A., Janies, D.A., James, A.A., Afrane, Y., Etemesi, H.,Zhou, G., Githeko, A., Yan, G. Selection and Utility of Single Nucleotide Polymorphism markers to reveal fine-scale population structure in human malaria parasite Plasmodium falciparum (2018) Frontiers in Ecology and Evolution fevo.2018.00145
Scolari F, Casiraghi M, Bonizzoni M. Aedes spp. and Their Microbiota: A Review. Front Microbiol. 2019; doi: 10.3389/fmicb.2019.02036.

Houé V, Gabiane G, Dauga C, Suez M, Madec Y, Mousson L, Marconcini M, Yen PS, de Lamballerie X, Bonizzoni M, Failloux AB. Evolution and biological significance of flaviviral elements in the genome of the arboviral vector Aedes albopictus. Emerg Microbes Infect. 2019; doi: 10.1080/22221751.2019.1657785.

Blair CD, Olson KE, Bonizzoni M. The Widespread Occurrence and Potential Biological Roles of Endogenous Viral Elements in Insect Genomes. Curr Issues Mol Biol. 2019 doi: 10.21775/cimb.034.013.

Machani MG, Ochomo E, Sang D, Bonizzoni M, Zhou G, Githeko AK, Yan G, Afrane YA. Influence of blood meal and age of mosquitoes on susceptibility to pyrethroids in Anopheles gambiae from Western Kenya. Malar J. 2019 doi: 10.1186/s12936-019-2746-6.

Houé V, Bonizzoni M, Failloux AB. Endogenous non-retroviral elements in genomes of Aedes mosquitoes and vector competence. Emerg Microbes Infect. 2019; doi: 10.1080/22221751.2019.1599302.

Pischedda E, Scolari F, Valerio F, Carballar-Lejarazú R, Catapano PL, Waterhouse RM, Bonizzoni M. Insights Into an Unexplored Component of the Mosquito Repeatome: Distribution and Variability of Viral Sequences Integrated Into the Genome of the Arboviral Vector Aedes albopictus. Front Genet. 2019 doi: 10.3389/fgene.2019.00093.

Souza-Neto JA, Powell JR, Bonizzoni M. Aedes aegypti vector competence studies: A review. Infect Genet Evol. 2019 doi:10.1016/j.meegid.2018.11.009.

Xu J, Su X, Bonizzoni M, Zhong D, Li Y, Zhou G, Nguyen H, Tong S, Yan G, Chen XG. Comparative transcriptome analysis and RNA interference reveal CYP6A8 and SNPs related to pyrethroid resistance in Aedes albopictus. PLoS Negl Trop Dis. 2018 e0006828.

Bonizzoni M, Attardo G. Editorial overview: Vectors and medical and veterinary entomology: Becoming vectors or victims, the intriguing interplay between insects and viruses. Curr Opin Insect Sci. 2017 doi: 10.1016/j.cois.2017.07.010.

Olson KE, Bonizzoni M. Nonretroviral integrated RNA viruses in arthropod vectors: an occasional event or something more? Curr Opin Insect Sci. 2017 22:45-53.

Palatini U, Miesen P, Carballar-Lejarazu R, Ometto L, Rizzo E, Tu Z, van Rij RP, Bonizzoni M. Comparative genomics shows that viral integrations are abundant and express piRNAs in the arboviral vectors Aedes aegypti and Aedes albopictus. BMC Genomics. 2017 18:512.

Xu J, Bonizzoni M, Zhong D, Zhou G, Cai S, Li Y, Wang X, Lo E, Lee R, Sheen R, Duan J, Yan G, Chen XG. Multi-country Survey Revealed Prevalent and Novel F1534S Mutation in Voltage-Gated Sodium Channel (VGSC) Gene in Aedes albopictus. PLoS Negl Trop Dis. 2016 10(5):e0004696.

Chang X, Zhong D, Lo E, Fang Q, Bonizzoni M, Wang X, Lee MC, Zhou G, Zhu G, Qin Q, Chen X, Cui L, Yan G. Landscape genetic structure and evolutionary genetics of insecticide resistance gene mutations in Anopheles sinensis. Parasit Vectors. 2016 9:228.

Chen XG, Jiang X, Gu J, Xu M, Wu Y, Deng Y, Zhang C, Bonizzoni M, Dermauw W, Vontas J, Armbruster P, Huang X, Yang Y, Zhang H, He W, Peng H, Liu Y, Wu K, Chen J, Lirakis M, Topalis P, Van Leeuwen T, Hall AB, Jiang X, Thorpe C, Mueller RL, Sun C, Waterhouse RM, Yan G, Tu ZJ, Fang X, James AA. Genome sequence of the Asian Tiger mosquito, Aedes albopictus, reveals insights into its biology, genetics, and evolution. Proc Natl Acad Sci U S A. 2015 112(44):E5907-15.

Bonizzoni M, Ochomo E, Dunn WA, Britton M, Afrane Y, Zhou G, Hartsel J, Lee MC, Xu J, Githeko A, Fass J, Yan G. RNA-seq analyses of changes in the Anopheles gambiae transcriptome associated with resistance to pyrethroids in Kenya: identification of candidate-resistance genes and candidate-resistance SNPs. Parasit Vectors. 2015 Sep 17;8:474.

Evans BR, Gloria-Soria A, Hou L, McBride C, Bonizzoni M, Zhao H, Powell JR. A
Multipurpose, High-Throughput Single-Nucleotide Polymorphism Chip for the Dengue
and Yellow Fever Mosquito, Aedes aegypti. G3 (Bethesda). 2015 5:711-8.
doi: 10.1534/g3.114.016196.
Project Title:
Mosquito microbiota and virome: a focus on Italy
Arboviral diseases are caused by viruses, like Dengue, Chikungunya and Zika, which are spread to people by the bite of infected arthropods, primarily Aedes spp. mosquitoes. Traditionally considered only a minor contributor to global mortality, arboviral diseases have seen an unprecedented resurgence in the past five decades. At the moment, there are no specific arboviral drugs, and licensed vaccines are either available for a limited number of arboviruses, for instance there is not a vaccine for Chikungunya and Zika viruses and only one commercial vaccine is available for Dengue, but it may be accessible for few people at risk of infection, mainly due to its cost. Given this situation, prevention of transmission is critical and the only effective method currently available to reduce the risk of transmission is to act on mosquitoes. Besides being carriers of arboviruses, mosquitoes can be infected with insect-specific viruses (ISVs). ISVs are phylogenetically-related to arboviruses but are not able to replicate in vertebrate cells and infect humans and other vertebrates. Vertical transmission has been demonstrated for ISVs and it is likely the major mechanism ensuring their persistence in nature. Cell-fusing Agent (CSA) was the first ISV isolated from mosquitoes in 1975. More than two decades passed before a second ISV, Kamiti River Virus, was described. This temporal gap was caused by the absence of appropriate tools for a global virome analyses, but also the lack of interest in the scientific community for the study of ISVs, probably due to their not-pathogenic nature in vertebrates. However, this absence of pathogenicity, is what makes them perfect candidates for the control of infection and replication of pathogenic arbovirus in the mosquito vector. Several ISVs, including the Palm Creek virus and Eilat virus, have already been tested for their capacity to interfere with arbovirus growth with promising results.
There are no studies yet on the widespread of ISVs or the use of ISVs for the control of arboviral infections in Ae. albopictus. As a first step to the potential application of ISVs as biological agents for the control of arboviruses in Italian mosquitoes, this project aims to characterise the virome of Italian mosquitoes.

Project Title:
The impact of temperature on Aedes albopictus immunity.
Establishment of the arboviral vector Aedes albopictus in temperate regions of the world fostered the re-emergence or the new introduction of arboviruses. For instance, Chikungunya outbreaks occurred in Italy in 2007 and 2017; France and Croatia suffered from autochthonous cases of Dengue and Chikungunya in several occasions since 2010.
Europe is characterized by a temperate climate with a clear seasonality that translates into a seasonal emergence and activity of mosquitoes. When mosquito emerge in late spring (May-June), temperature averages between 16-18ºC in Italy, while in summer temperature averages 24-25 ºC, with picks above 30ºC. Temperatures at the time of mosquito emergence and during the pick of summer have already been proven to be thermal stressor linked to modulation in immunity gene expression and susceptibility to viral infection. However, there is not a clear understanding of the molecular mechanisms underpinning this adaptation process. This project will combine transcriptional and physiological analyses to understand the impact of temperature on mosquito immunity.