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 BIOTECHNOLOGY, AGRICULTURE AND BIODIVERSITY

Laboratory of aquatic invertebrate biochemistry

Structure-function and evolution of proteins in invasive mollusks,
pests, and parasite vectors

Work team

Principal InvestigatorHeras

Heras, Horacio

Investigator
h-heras@med.unlp.edu.ar

Dreon, Marcos SebastiánDreon

Investigator
msdreon@med.unlp.edu.ar

Ituarte, SantiagoItuarte

Investigator
santiago.ituarte@gmail.com

Pasquevich, M. YaninaPasquevich

Investigator
mypasquevich@med.unlp.edu.ar

Brola, Tabata RominaBrola

Research Fellow
btabata@med.unlp.edu.ar

Chiumiento, IgnacioChiumiento

Research Fellow
ichiumiento@med.unlp.edu.ar

Pavia, IgnacioPavia

Research Fellow
ipavia@med.unlp.edu.ar

Soldati, Kevin BrianSoldati

Research Fellow
ksoldati@med.unlp.edu.ar

Collaborators from other institutions

Jian-Wen Qiu
Hong Kong Baptist University, Republica Popular de China.

Ceolín, Marcelo
INIFTA -Instituto de Investigaciones Fisicoquímicas Teóricas y Aplicadasa (CONICET - CCT- La Plata - UNLP). La Plata. Provincia de Buenos Aires. Argentina.

Fernández, Patricia
Cátedra de Patología de la Facultad de Ciencias Veterinarias. UNLP. La Plata. Provincia de Buenos Aires. Argentina.

Line overview

Objetives

Our group is focused on classifying, identifying, and studying the structure, functions and evolution of unknown egg proteins of invasive snails that are agricultural pests and parasite vectors. We endeavour to understand the snail reproductive strategies from a biochemical perspective and, at the same time, to select some of these new proteins with potential as bioactive compounds to exploit their application in Biomedicine.

Importance of the study of snail proteins

The knowledge of the protein structure-function relationship is key to understanding biological processes. Gastropod molluscs are a rich source of bioactive molecules commonly used in Pharmacology and Medicine since they have an outstanding diversity of compounds, a reflection of their long evolutionary history. However, the proteins of mollusc eggs are very little investigated. Our research group is studying them taking as a model those of the freshwater snails of the Pomacea genus, also called apple snails. Some, such as P. canaliculata and P. maculata are worldwide invaders which have turned into serious rice and taro crops pests. They are vectors of a nematode parasite, responsible for human eosinophilic meningoencephalitis in Asia and Latin America. Their uncontrolled expansion entailed the advance of this zoonosis. Apple snail eggs are laid above the water in conspicuously coloured masses that have almost no predators. They are the most vulnerable stage and the focus of our work.

Questions we expect to answer

What kind of proteins do the eggs of these snails have and how they evolved?
Which are the properties of these proteins and what role do they play in the defence mechanism of the embryos?
Do they have any application in Biomedicine, Biotechnology or Pharmacology?

Methodology employed

Our group uses a multidisciplinary approach with collaborations with other research groups in our country and abroad in order to answer these questions, usually employing a combination of methodologies including biochemistry, molecular biology, biophysics, cellular biology, histopathological and bioassays with laboratory animals. Some of the techniques used are:
• Determination of amino acid sequence and bioinformatic analysis.
• Study of biochemical activity of inhibitors, lectins, enzymes isolated from the eggs.
• Study of structure/function of proteins through SAXS, CryoEM and other biophysical techniques.
• Microbiological studies of bacterial growth inhibition.
• In vitro studies of toxicity and interaction with cultured tumour cells.
• Basic immunological studies.
• Toxicity bioassays in murine, quail, frogs and insect models.
• histopathological studies using optical and electron microscopy; effects on the nervous and digestive systems of potential predators.

Main results

Perivitelline fluid (PVF). It surrounds the embryos. an extracellular fluid found in the eggs of most gastropods and constitutes the main source of nutrition and defense for their embryos. We found Pomacea PVF is mainly composed of the sugar galactogen and proteins calles perivitellins. Both are used in the nutrition and defense of embryos. More details on the perivitelline fluid of apple snails can be found at https://en.wikipedia.org/wiki/Perivitelline_fluid https://en.wikipedia.org/wiki/Perivitelline_fluid
Studying the proteome of perivitelline fluid from several Pomacea eggs we demonstrated that P. canaliculata and P. maculata and other Pomacea have a fascinating antipredator defence mechanism where perivitellins play a central role, providing the embryos with one of the best biochemical defences in animals. We characterized their major perivitellins Perivitellin-1 (PcOvo , PmPV1) and Perivitellin -2 (PcPV2 and PmPV2) that participate in embryo protection as follows:

Perivitellin-1 PcOvo and PmPV1 are caroteno-proteins massively accumulated in eggs that provide photoprotective and antioxidant compounds to the developing embryo. At the same time, it gives eggs a conspicuous colour that would warn potential predators of the presence of various toxins of perivitelline fluid surrounding the embryo (aposematic defense). PcOvo also is non-digestible lowering the nutritional value of eggs to a predator (antinutritive defence). Orally administered, it diminishes the growth rate in rats.

Perivitellin-2 (PV2) is a pore-forming toxin present in the egg perivitelline fluid of the apple snails Pomacea maculata (PmPV2) and Pomacea canaliculata (PcPV2). This protein, called perivitellin, is massively acumulated in the eggs (~20 % total protein. As a toxin PV2 protects eggs from predators, but it also nourishes the developing snail embryos.
These proteins are lethal for rodents and are the first protein toxins described within an egg. Its structure differs from all other animal toxins since it combines a lectin subunit that recognizes specific sequences of membrane sugars, attached to a subunit that forms large pores in cell membranes that belong to the Membrane Attack Complex and Perforin (MACPF) family (toxic unit) eventually leading to cell death. Even though there is no equal in animals, it is similar to AB toxins described in plant seeds and bacteria such as the botulinum toxin. Whether this novel defence system is present in the eggs of other species remains unknown.
We continue studying its properties and mechanism of action. More details on structure, function and evolution can be found in Wikpedia at https://en.wikipedia.org/wiki/Perivitellin-2
On the eggs of Pomacea scalaris and Pomacea difussa, we characterized their major egg proteins -called scalarin (PsSC) and PdPV1, respectively.
They provide eggs with a pink-salmon colour that could also function as a warning signal. We demonstrated they are powerful lectins that are orthologs that share many sequence, structural and functional similarities with PcOvo.
They seem defence proteins as the ingestion of these toxic lectins adversely affects the morphology of the digestive system of potential predators. They also bind with specificity to some tumour cells, potentially serving as biomarkers. Other gastropod lectins have impact on medical practice and are commercialized to improve the pharmacokinetics of glycoprotein drugs or in the diagnosis of diseases such as tumour markers.
A property shared by these snail proteins is that they are very resistant to high temperatures, extreme pHs and gastrointestinal digestion, highlighting other features that can be employed in potential applications.

Evolutionary and ecological implications

The selective pressure exerted by predators and hostile environment on the eggs would have led to the acquisition of new properties to endure the air development of an aquatic animal. At the biochemical level it seems that these adaptations would involve the acquisition of a new type of perivitellins that besides being a reserve protein provide very efficient defences against predation together with protective properties to the embryo facing a hostile environment.
The presence of eggs protected with proteins of these characteristics has not been found in other members of the animal kingdom, but it is similar to the plant defences against herbivory.


Phylogenetic variations in a novel family of hyperstable apple snail egg proteins: insights into structural stability and functional trends.
Pasquevich, M. Y; Diupotex-Chong, M. N; Dreon, M. S; Heras, H.
2024 J. Exp. Biol. 227,15
DOI https://doi.org/10.1242/jeb.247277

Egg toxic compounds in the animal kingdom. A comprehensive review.
Gigio, M.; Boland, W; Heras, H.
2022. Natural Product Report 39
DOI https://doi.org/10.1039/d2np00029f

Ingestion of Poisonous Eggs of the Invasive Apple Snail Pomacea canaliculata Adversely Affects Bullfrog Lithobathes catesbeianus Intestine Morphophysiology.
Brola, Tabata R.; Dreon, Marcos S.; Fernández, Patricia E.; Portiansky, Enrique L.; Heras, Horacio.
2021. Malacologia.
doi: 10.4002/040.063.0202

Biochemical and morphological features of the uropygial gland of the Chilean Flamingo and their functional implications.
Chiale, María Cecilia; Cadierno, María Pilar; Fernández, Patricia; Mijailovsky, Sergio; Heras, Horacio; Barbeito, Claudio; Montalti, Diego.
2021. Zoology.
doi:10.1016/j.zool.2021.125941

Dynamics of circulating lipoproteins and lipids in Brown Skua (Stercorarius antarcticus lonnbergi) during the breeding cycle.
Ibañez, A.E.; Pasquevich, M.Y.; Machulsky, N. Fernandez; Berg, G.; Heras, H.; Montalti, D.; Grilli, M. Graña.
2021. Polar biology.
doi.org/10.1007/s00300-020-02793-1

Exaptation of two ancient immune proteins into a new dimeric pore-forming toxin in snails.
Giglio, M. L.; Ituarte, S.; Milesi, V.; Dreon, M.S.; Brola, T. R.; Caramelo, J.; Ip, J. C. H.; Maté, S.; Qiu, J. W.; Otero, L. H.; Heras, H.
2020. Journal of structural biology.
doi.org/10.1016/j.jsb.2020.107531

Apple snail egg perivitellin coloration, as a taxonomic character for invasive Pomacea maculata and P. canaliculata, determined by a simple method.
Pasquevich, M. Y.; Heras, H.
2020. Biological invasions.
doi.org/10.1007/s10530-020-02255-z

A highly stable, nondigestible lectin from Pomacea difusa unveils clade-related protection systems in apple snail eggs.
Brola, T. R; Dreon, M. S; Qiu, J. W; Heras, H.
2020. Journal of experimental biology.
doi.org/10.1242/jeb.231878

Novel Role for Animal Innate Immune Molecules: Enterotoxic Activity of a Snail Egg.
Giglio, Matías L.; Ituarte, Santiago; Ibañez, Andrés E.; Dreon, Marcos S.; Prieto, Eduardo; Fernández, Patricia E.; Heras, Horacio.
2020. MACPF-Toxin. Frontiers in immunology.
doi.org/10.3389/fimmu.2020.00428

Egg perivitelline fluid proteome of a freshwater snail: Insight into the transition from aquatic to terrestrial egg deposition
Ip, Jack C.H.; Mu, Huawei; Zhang, Yanjie; Heras, Horacio; Qiu, Jian.
2020. Rapid Communications in Mass Spectrometry.
doi.org/10.1002/rcm.8605

Hemocyanin of the Caenogastropod Pomacea canaliculata exhibits evolutionary differences among gastropod clades.
Chiumiento, IR., Ituarte, S., Sun, J., Qiu, J-W., Heras, H. and Dreon, MS. >
2020. Plos one.
doi.org/10.1371/journal.pone.0228325

Understanding the Transition from Water to Land: Insights from Multi-omic Analyses of the Perivitelline Fluid of Apple Snail Eggs.
Ip, J, Mu, H., Zhang, Y., Sun, J., Heras, H., Chu, FH, Qiu, J-W.
2019. J. Proteomics.
doi.org/10.1016/j.jprot.2018.12.014

Non-digestible proteins and protease inhibitors: Implications for defense of the colored eggs of freshwater apple snails.
Ituarte, S., Brola, TR., Dreon, MS., Sun, J., Qiu, J-W., Heras, H.
2019. Can. J. Zool.
doi.org/10.1139/cjz-2018-0210

Genomic signatures of divergence and invasiveness in apple snails.
Sun, J, H Mu, JCH Ip, R Lib, T Xub, N Kumagai, Y Yusa, A Accorsi, A Sánchez Alvarado, E Ross, A Castro-Vazquez, IA Vega, H Heras, S Ituarte, B Van Bocxlaer, KA Hayes, RH Cowie, Z Zhao, Y Zhang, P-Y Qian, J-W Qiu.
2019. Molecular Biology and Evolution.
doi.org/10.1093/molbev/msz084

Egg perivitelline fluid proteome of a freshwater snail (Caenogastropoda): insight into the transition from aquatic to terrestrial egg deposition.
Ip JCH, Mu, H., Zhang, Y., Heras, H., Chu, KH. and Qiu, J-W.
2019. Rap. Comm. Mass Spectrometry.
doi.org/10.1002/rcm.8605

Biosynthesis in the Albumen Gland-Capsule Gland Complex Limits Reproductive Effort in the Invasive Apple Snail Pomacea canaliculata.
Cadierno, M. P; Saveanu, L; Dreon, M. S; Martín, P. R; Heras, H.
2018. Biological bulletin.
doi.org/10.1086/699200

Validation by qPCR of reference genes for reproductive studies in the invasive apple snail Pomacea canaliculata.
Cadierno, M. P; Dreon, M. S; Heras, H.
2018. Malacologia.
doi.org/10.4002/040.062.0105

A lectin of a non-invasive apple snail as an egg defense against predation alters the rat gut morphophysiology.
Ituarte, S; Brola, T. R; Fernández, P. E; Mu, H; Qiu, J; Heras, H; Dreon, M. S.
2018. Plos one.
doi.org/10.1371/journal.pone.0198361

AmpuBase: a transcriptome database for eight species of apple snails (Gastropoda: Ampullariidae).
Ip, J; Mu, H; Chen, Q; Jin, S; Ituarte, S; Van Bocxlaer, B; Ganmanee, M; Huang, X; Qiu, J.
2018. BMC Genomics.
doi.org/10.1186/s12864-018-4553-9

Egg perivitelline fluid of the invasive snail Pomacea canaliculata affects mice gastrointestinal function and morphology.
Giglio, M. L; Garro, C; Caviedes Vidal, E; Heras, H.
2018. Peerj, Inc.
doi.org/10.7717/peerj.5314

An integrated proteomic and transcriptomic analysis of perivitelline fluid proteins in a freshwater gastropod laying aerial eggs.
Mu, H; Sun, J; Heras, H; Chu, K.H; Qiu, J-W.
2017. J. Proteomics.
dx.doi.org/10.1016/j.jprot.2017.01.006

Apple snail perivitellin precursor properties help explain predator´ feeding behavior.
Cadierno, M.P; Dreon, M.S; Heras, H. Physiol.
2017. Biochem. Zool.
dx.doi.org/10.1086/691526

The influence of energy, nutritional value and noxiousness in sex- and size-biased predation by Snail Kites in southern South America.
Cadierno, M.P; Burela, S; Dreon, M.S; Martin, P; Heras, H.
2017. EMU.
doi.org/10.1080/01584197.2017.1338113

Dataset for the proteomic and transcriptomic analyses of perivitelline fluid proteins in Pomacea snail eggs.
Mu, H; Sun, J; Heras, H; Chu, K.H; Qiu, J-W.
2017. Data in Brief.
dx.doi.org/10.1016/j.dib.2017.09.020

Convergent evolution of plant and animal embryo defences by hyperstable non-digestible storage proteins.
Pasquevich, M.Y; Dreon, M.S; Qiu, J-W; Mu, H; Heras, H.
2017. Scientific Reports.
dx.doi.org/10.1038/s41598-017-16185-9

The eggs of the apple snail Pomacea maculata are defended by indigestible polysaccharides and toxic proteins.
Giglio, M. L; Ituarte, S; Pasquevich, M. Y; Heras, H.
2016. Can. J. Zool.
dx.doi.org/10.1139/cjz-2016-0049

Effects of sewage discharges on lipid and fatty acid composition of the freshwater Patagonian bivalve Diplodon chilensis.
Rochetta, I; Pasquevich, M. Y; Heras, H; Rios De Molina, M. C; Luquet, C. M.
2014. Mar. Pollut. Bull.
dx.doi.org/10.1016/j.marpolbul.2013.12.011

Insights into embryo defenses of the invasive apple snail Pomacea canaliculata: egg mass ingestion affects rat intestine morphology and growth.
Dreon, M. S; Fernández, P. E; Gimeno, E; Heras, H.
2014. PLoS Neglect.
dx.doi.org/10.1371/journal.pntd.0002961

The major egg reserve protein from the invasive apple snail Pomacea maculata is a complex carotenoprotein related to those of Pomacea canaliculata and Pomacea scalaris.
Pasquevich, M. Y; Dreon, M, S; Heras, H.
2014. Comp. Biochem. Physiol.
dx.doi.org/10.1016/j.cbpb.2013.11.008

¿Por qué hay huevos que nadie quiere comer?
Heras, H. 2014. Ciencia Hoy. (Trabajo de divulgación)
cienciahoy.org.ar/2014/04/por-que-hay-huevos-que-nadie-quiere-comer/

Effect of crude oil petroleum hydrocarbons on protein expression of the prawn Macrobrachium borellii.
Pasquevich, M. Y; Dreon, M. S; Gutiérrez Rivera, J. N; Vázquez Boucard, C; Heras H.
2013. Comp. Biochem. Physiol C.
dx.doi.org/10.1016/j.cbpc.2013.03.006

Study of biochemical biomarkers in freshwater prawn Macrobrachium borellii (Crustacea: Palaemonidae) exposed to organophosphate fenitrothion.
Lavarías, S; García, C; Crespo, R; Pedrini, N; Heras H.
2013. Ecotoxicol.
dx.doi.org/10.1016/j.ecoenv.2013.05.040

Novel animal defenses against predation: A snail egg neurotoxin combining lectin and pore-forming chains that resembles plant defense and bacteria attack toxins.
Dreon, M. S; Frassa, M. V; Ceolín, M; Ituarte, S; Qiu, J. W; Sun, J; Fernández, P. E; Heras, H.
2013. PLoS One
dx.doi.org/10.1371/journal.pone.0063782

Vitellogenin and lipovitellin from the prawn Macrobrachium borellii as hydrocarbon pollution biomarker.
García, C. F; Heras, H.
2012. Mar. Poll. Bull.
dx.doi.org/10.1016/j.marpolbul.2012.05.027

First proteome of the egg perivitelline fluid of a freshwater gastropod with aerial oviposition.
Sun, J; Zhang, H; Wang, H; Heras, H; Dreon, M; Ituarte, S; Ravasi, T; Qian, P; Qiu, J. W.
2012. J. Proteome Res.
dx.doi.org/10.1021/pr3003613

Agglutinating activity and structural characterization of scalarin the major egg protein of the snail Pomacea scalaris.
Ituarte, S; Dreon, M. S; Ceolin, M; Heras, H. (d’Orbigny, 1832).
2012. PLoS ONE
dx.doi.org/10.1371/journal.pone.0050115

Antioxidant response and oxidative stress levels in Macrobrachium borellii (Crustacea: Palaemonidae)exposed to the water-soluble fraction of petroleum.
Lavarías, S; Heras, H; Pedrini, N; Turnier, H; Ansaldo, M.
2011. Comp. Biochem. Physiol.
dx.doi.org/10.1016/j.cbpc.2011.02.002

Triacylglycerol catabolism in the prawn Macrobrachium borellii (Crustacea: Palaemoniade).
Pasquevich, M. Y; Dreon, M. S; Lavarías, S; Heras, H.
2011. Comp. Biochem. Physiol.
dx.doi.org/10.1016/j.cbpb.2011.08.006

Isolation and characterization of two vitellins from eggs of the spider Polybetes pythagoricus (Araneae: Sparassidae).
Laino, A; Cunningham, M. L; Heras, H; García, C. F.
2011. Comp. Biochem. Physiol.
dx.doi.org/10.1016/j.cbpb.2010.11.001

In vitro lipid transfer between lipoproteins and midgut-diverticula in the spider Polybetes pythagoricus.
Laino, A; Cunningham, M; Heras, H; García, C. F.
2011. Comp. Biochem. Physiol.
dx.doi.org/10.1016/j.cbpb.2011.08.003

Structure and stability of the neurotoxin PV2 from the eggs of Pomacea canaliculata.
Frassa, V; Ceolin, M; Dreon, M. S; Heras, H.
2010. Biochim.Biophys.
dx.doi.org/10.1016/j.bbapap.2010.02.013

The Role of the Proteinase Inhibitor Ovorubin in Apple Snail Eggs Resembles Plant Embryo Defenses Against Predation.
Dreón, M. S; Ituarte, S; Heras, H.
2010. PLoS ONE.
dx.doi.org/10.1371/journal.pone.0015059

Carbohydrates and glycoforms of the major egg perivitellins from Pomacea apple snails (Architaenioglossa: Ampullariidae).
Ituarte, S; Dreón, M. S; Pasquevich, M. Y; Fernández, P. E; Heras, H.
2010. Comp. Biochem. Physiol.
dx.doi.org/10.1016/j.cbpb.2010.05.004

Structure and stability of crustacean lipovitellin: Influence of lipid content and composition.
García, C. F; Cunningham, M; Soulages, J. L; Heras, H; Garda, H. A.
2010. Comp. Biochem. Physiol.
dx.doi.org/10.1016/j.cbpb.2009.10.010

First insight into the lipid uptake, storage and movilization in arachnids. Role of midgut diverticula and lipoproteins.
Laino, A; Cunningham, M; García, C. F; Heras, H.
2009. J. Insect Physiol.
dx.doi.org/10.1016/j.jinsphys.2009.08.005

Partial characterization of a malonyl-CoA-sensitive carnitine o-palmitoyltransferase I from Macrobrachium borellii. (Crustacea: Palaemomidae).
Lavarías, S; Pasquevich, Y; Dreon, M. S; Heras, H.
2009. Comp. Biochem. Physiol.
dx.doi.org/10.1016/j.cbpb.2009.01.004

Isolation and characterization of a novel perivitellin from the eggs of Pomacea scalaris (Mollusca, Ampullariidae).
Ituarte, S; Dreon, M. S; Ceolin, M; Heras, H.
2008. Mol. Reprod. Dev.
dx.doi.org/10.1002/mrd.20880

First egg protein with a neurotoxic effect on mice.
Heras, H; Frassa, V; Fernández, P. E; Galosi, C. M; Gimeno, E; Dreon, M. S.
2008. Toxicon 52
dx.doi.org/10.1016/j.toxicon.2008.06.022

Global shape and pH stability of ovorubin, an oligomeric protein from the eggs of Pomacea canaliculata.
Dreón, M. S; Ituarte, S; Ceolín, M; Heras, H.
2008. FEBS J.
dx.doi.org/10.1111/j.1742-4658.2008.06595.x

Embryo lipoproteins and yolk lipovitellin consumption during embryogenesis in Macrobrachium borellii (Crustacea: Palaemonidae).
García, F; Cunningham, M; Garda, H; Heras, H.
2008. Comp. Biochem. Physiol.
dx.doi.org/10.1016/j.cbpb.2008.07.015

Astaxanthin binding and structural stability of apple snail carotenoprotein ovorubin.
Dreon, M. S; Ceolin, M; Heras, H.
2007. Arch. Biochem. Biophys.
dx.doi.org/10.1016/j.abb.2006.12.033

Effect of the water-soluble fraction of petroleum on microsomal lipid metabolism of Machrobrachium borellii (Arthropoda: Crustacea).
Lavarías, S; García, F; Pollero, R. J; Heras, H.
2007. Aquatic Toxicol.
dx.doi.org/10.1016/j.aquatox.2007.02.017

Egg carotenoproteins of neotropical ampullariidae (gastropoda: arquitaenioglossa).
Heras, H; Dreon, M. S; Ituarte, S; Pollero, R. J.
2007. Comp. Biochem. Physiol.
dx.doi.org/10.1016/j.cbpc.2006.10.013

Novel Role for Animal Innate Immune Molecules: Enterotoxic Activity of a Snail Egg MACPF-Toxin.
Giglio, M.L.; Ituarte, S; Ibañez, Andrés E.; Dreon, M.S.; Prieto, Ed; Fernandez, Pe; Heras, H; Munson, Gp; Cristin Gilbert, Rj; Pradel, G.
2022. Lausanne
DOI: 10.3389/fimmu.2020.00428

Estudios bioquímicos de la ATP citrato liasa de bacterias simbiontes de Alvinella pompejana (Anellida: Poliqueta).
Ignacio Pavía
2022. La Plata: Universidad Nacional de La Plata. Facultad de Ciencias Exactas. p. 73-78
sedici.unlp.edu.ar/handle/10915/152280

Apple Snail perivitellins. Multifunctional egg proteins¨. In: Biology and management of invasive apple snails.
Heras, H; Dreon, M.S; Ituarte, S; Pasquevich, M.Y; Cadierno, M.P.
2017. Philippine Rice Research Institute.

Métodos de control del desarrollo de floraciones cianobacterianas en ambientes acuáticos.
Bauzá, L; Giannuzzi, L; Petcheneshsky, T; Hansen, M; Benítez, R; De Titto, E.
2017. Revisión actualizada. Ciudad autónoma de Buenos Aires: Ministerio de Salud de la Nación. p. 125-146.

Changes in carbohydrate expression in the cervical spinal cord of mice intoxicatedwith perivitellin PV2 from Pomacea canaliculata. In: Poisoning by plants, mycotoxins and related toxins.
Fernández, P. E; Frassa, V; Gimeno, E. J; Dreon, M; Heras, H.
2011. Edited by Riet-Correa.

¿Por qué hay huevos que nadie quiere comer?
Heras, H.
2014. Ciencia Hoy. (Trabajo de divulgación)
See article

“IFS Jubilee Award 2006”
Premio otorgado a los investigadores sobresalientes de proyectos subsidiados por la Internacional Foundation for Science al Dr. Heras Horacio. Suecia – 2006.



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Dr. Tricerri, María Alejandra

Role of lipids in neuronal differentiation
and neurodegenerative processes.

Principal Investigator
Dr. Falomir--Lockhart, Lisandro

Antitumor mechanisms of phytochemicals and their nanovehiculization as a strategy to develop therapeutic systems with enhanced properties.

Principal Investigator
Dr. Rodenak Kladniew, Boris

Effects of metal overloads on lipid metabolism
and oxidative stress formation.
Implications for the development of Alzheimer’s disease.

Principal Investigator
Dr. Arnal, Nathalie

Fatty acid metabolism in cell proliferation and evaluation of its potential
as a therapeutic target in cancer.

Principal Investigator
Dr. Scaglia, Natalia

● Study of the structure-function of bacterial toxins in different cell types (erythrocytes, platelets, endothelial cells, Caco cells).
● Biomedical applications with toxins (design of detection kits, development of nanosponges for treatment, and immunotoxins).

Principal Investigator
Dr. Herlax, Vanesa

Role of omega-3 fatty acids on membrane composition and structure, and their relation to neuroinflammatory response, neurodegeneration, and behavior of hypertensive rats.

Principal Investigator
Dr. Maté, Sabina

Interactions between entomopathogenic fungi and their hosts.

Principal Investigator
Dr. Huarte Bonnet, Carla

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