Post-translational Deimination of Immunological and Metabolic Protein Markers in Plasma and Extracellular Vesicles of Naked Mole-Rat (Heterocephalus glaber)

Pamenter, M.E., Uysal Onganer, P., Huynh, K.W., Kraev, I. and Lange, S. 2019. Post-translational Deimination of Immunological and Metabolic Protein Markers in Plasma and Extracellular Vesicles of Naked Mole-Rat (Heterocephalus glaber). International Journal of Molecular Sciences. 20 (21), p. 5378. doi:10.3390/ijms20215378

TitlePost-translational Deimination of Immunological and Metabolic Protein Markers in Plasma and Extracellular Vesicles of Naked Mole-Rat (Heterocephalus glaber)
TypeJournal article
AuthorsPamenter, M.E., Uysal Onganer, P., Huynh, K.W., Kraev, I. and Lange, S.
Abstract

Naked mole-rats are long-lived animals which show unusual resistance to hypoxia, cancer and ageing. Protein deimination is an irreversible post-translational modification caused by the peptidylarginine deiminase (PADs) family of enzymes, which convert arginine into citrulline in target proteins. Protein deimination can cause structural and functional protein changes, facilitating protein moonlighting, but also leading to neo-epitope generation and effects on gene regulation. Furthermore, PADs have been found to regulate cellular release of extracellular vesicles (EVs), which are lipid-vesicles released from cells as part of cellular communication. EVs carry protein and genetic cargo and are indicative biomarkers that can be isolated from most body fluids. This study was aimed at profiling deiminated proteins in plasma and EVs of naked mole-rat. Key immune and metabolic proteins were identified to be post-translationally deiminated, with 65 proteins specific for plasma, while 42 proteins were identified to be deiminated in EVs only. Using protein-protein interaction network analysis, deiminated plasma proteins were found to belong to KEEG pathways of immunity, infection, cholesterol and drug metabolism, while deiminated proteins in EVs were in addition linked to KEEG pathways of HIF-1 signalling and glycolysis. The mole-rat EV profiles showed a poly-dispersed population of 50-300 nm, similar to observations from human plasma. Furthermore, the EVs were assessed for three key microRNAs involved in cancer, inflammation and hypoxia. The identification of post-translational deimination of critical immunological and metabolic markers may contribute to current understanding of protein moonlighting functions via post-translational changes in longevity and cancer resistance in mole-rats.

KeywordsPeptidylarginine deiminases (PADs); protein deimination; naked mole-rat (Heterocephalus glaber); extracellular vesicles (EVs); immunity; metabolism; microRNA (miR21, miR155, miR210)
Article number5378
JournalInternational Journal of Molecular Sciences
Journal citation20 (21), p. 5378
ISSN1422-0067
Year2019
PublisherMDPI
Publisher's versionijms-20-05378.pdf
Digital Object Identifier (DOI)doi:10.3390/ijms20215378
Publication dates
Published29 Oct 2019
LicenseCC BY 4.0

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Lange, S., Ansa-Addo, E.A., McCrossan, M.V. and Inal, J. 2010. Human plasma membrane-derived vesicles halt proliferation and induce differentiation of THP-1 acute monocytic leukemia cells. Journal of Immunology. 185 (9), pp. 5236-5246. doi:10.4049/jimmunol.1001656

Red cell PMVs, plasma membrane-derived vesicles calling out for standards
Hind, E., Heugh, S., Ansa-Addo, E.A., Antwi-Baffour, S., Lange, S. and Inal, J.M. 2010. Red cell PMVs, plasma membrane-derived vesicles calling out for standards. Biochemical and Biophysical Research Communications. 399 (4), pp. 465-469. doi:10.1016/j.bbrc.2010.07.095

Spinal cord regeneration: A role for peptidylarginine deiminase (PAD) in secondary injury response
Lange, S. 2010. Spinal cord regeneration: A role for peptidylarginine deiminase (PAD) in secondary injury response. SfN Minisymposium on Deimination in Opthalmic and Neurodegenerative diseases. San Diego Convention Center, California 16 Nov 2010

Spinal cord regeneration: peptidylarginine deiminase (PAD) and epigentic regulation of injury response
Lange, S., Ferretti, P., Goegel, S., Leung, K.T., Nicholas, A.P., Thompson, P.R. and Greene, N.D.E. 2010. Spinal cord regeneration: peptidylarginine deiminase (PAD) and epigentic regulation of injury response. FENS Forum 2010. Amsterdam 04 Jul 2010 Federation of European Neuroscience Societies.

Changes in progenitor populations and ongoing neurogenesis in the regenerating chick spinal cord
Lange, S., Whalley, K., Gogel, S. and Ferretti, P. 2009. Changes in progenitor populations and ongoing neurogenesis in the regenerating chick spinal cord. Developmental Biology. 332 (2), p. 234–245. doi:10.1016/j.ydbio.2009.05.569

Proteome changes in developing and injured chick spinal cord
Goegel, S., Lange, S., Greene, N.D.E. and Ferretti, P. 2007. Proteome changes in developing and injured chick spinal cord. Neuron Glia Biology. pp. S122-S122.

Differential gene expression following chick spinal cord injury at permissive and non permissive stages for regeneration
Lange, S., Goegel, S., Greene, N.D.E. and Ferretti, P. 2007. Differential gene expression following chick spinal cord injury at permissive and non permissive stages for regeneration. Neuron Glia Biology. pp. S121-S121.

The complement regulatory receptor CRIT is expressed in the developing kidney
Lange, S., Hui Kwok-M, Schifferli, J. and Inal, J.M. 2007. The complement regulatory receptor CRIT is expressed in the developing kidney. Molecular Immunology. 44 (16), p. 3991. doi:10.1016/j.molimm.2007.06.213

Complement C2 and CRIT are involved in the terminal differentiation of monocytes
Inal, J.M., Eva, W., Lange, S., Shamshiev, A. and Schifferli, J. 2007. Complement C2 and CRIT are involved in the terminal differentiation of monocytes. Journal of Immunology. 178, p. 83.17.

Immunostimulation of larvae and juveniles of cod, Gadus morhua L.
Lange, S., Magnadóttir, B., Gudmundsdóttir, B.K., Bambir, S.H., Steinarsson, A., Oddgeirsson, M., Bowden, T., Bricknell, I., Dalmo, R.A. and Gudmundsdottir, S. 2006. Immunostimulation of larvae and juveniles of cod, Gadus morhua L. Journal of Fish Diseases. 29 (3), p. 147–155. doi:10.1111/j.1365-2761.2006.00701.x.

CRIT is expressed on podocytes in normal human kidney and upregulated in membranous nephropathy
Lange, S., Moll, S., Mihatsch M, J., Schifferli, J. and Inal, J. 2006. CRIT is expressed on podocytes in normal human kidney and upregulated in membranous nephropathy. Kidney International. 69 (11), p. 1961–1968. doi:10.1038/sj.ki.5000379

Complement component C3 transcription in Atlantic halibut (Hippoglossus hippoglossus L.) larvae
Lange, S., Bambir, S.H., Dodds, A.W., Bowden, T., Bricknell, I., Espelid, S. and Magnadóttir, B. 2006. Complement component C3 transcription in Atlantic halibut (Hippoglossus hippoglossus L.) larvae. Fish & Shellfish Immunology. 20 (3), p. 285–294. doi:10.1016/j.fsi.2005.05.004

Complement C2 receptor inhibitor trispanning: a novel human complement inhibitory receptor
Lange, S., Inal, J., Hui Kwok-M, Miot, S., Ramirez, M., Schneider, B. and Krueger, G. 2005. Complement C2 receptor inhibitor trispanning: a novel human complement inhibitory receptor. The Journal of Immunology. 174 (1), pp. 356-366.

The ontogenic transcription of complement component C3 and Apolipoprotein A-I tRNA in Atlantic cod (Gadus morhua L.): a role in development and homeostasis?
Lange, S., Dodds, A.W., Bambir, S.H., Gudmundsdottir, S. and Magnadóttir, B. 2005. The ontogenic transcription of complement component C3 and Apolipoprotein A-I tRNA in Atlantic cod (Gadus morhua L.): a role in development and homeostasis? Developmental & Comparative Immunology. 29 (12), p. 1065–1077. doi:10.1016/j.dci.2005.03.009

The Complement Systems of Two Teleost Species with Emphasis on Ontogeny
Lange, S. 2005. The Complement Systems of Two Teleost Species with Emphasis on Ontogeny. PhD thesis University of Iceland Faculty of Medicine

Ontogeny of humoral immune parameters in fish
Magnadóttir, B., Lange, S., Gudmundsdottir, S., Bogwald, J. and Dalmo, R.A. 2005. Ontogeny of humoral immune parameters in fish. Fish and Shellfish Immunology. 19 (5), pp. 429-439. doi:10.1016/j.fsi.2005.03.010

The ontogeny of complement component C3 in Atlantic cod (Gadus morhua L.)—an immunohistochemical study
Lange, S., Bambir, S., Dodds, A.W. and Magnadóttir, B. 2004. The ontogeny of complement component C3 in Atlantic cod (Gadus morhua L.)—an immunohistochemical study. Fish & Shellfish Immunology. 16 (3), pp. 359-367. doi:10.1016/j.fsi.2003.06.001

Is Apolipoprotein A-I a regulating protein for the complement system of cod (Gadus morhua L.)?
Magnadóttir, B. and Lange, S. 2004. Is Apolipoprotein A-I a regulating protein for the complement system of cod (Gadus morhua L.)? Fish and Shellfish Immunology. 16 (2), pp. 265-269. doi:10.1016/S1050-4648(03)00061-5

Isolation and characterization of complement component C3 from Atlantic cod (Gadus morhua L.) and Atlantic halibut (Hippoglossus hippoglossus L.)
Lange, S., Dodds, A.W. and Magnadóttir, B. 2004. Isolation and characterization of complement component C3 from Atlantic cod (Gadus morhua L.) and Atlantic halibut (Hippoglossus hippoglossus L.). Fish and Shellfish Immunology. 16 (2), pp. 227-239. doi:10.1016/S1050-4648(03)00081-0

Spontaneous haemolytic activity of Atlantic halibut (Hippoglossus hippoglossus L.) and sea bass (Dicentrarchus labrax) serum
Lange, S. and Magnadóttir, B. 2003. Spontaneous haemolytic activity of Atlantic halibut (Hippoglossus hippoglossus L.) and sea bass (Dicentrarchus labrax) serum. Comparative Biochemistry and Physiology - Part B: Biochemistry & Molecular Biology. 136 (1), pp. 99-106. doi:10.1016/S1096-4959(03)00173-8

Protection against atypical furunculosis in Atlantic halibut, Hippoglossus hippoglossus (L.); comparison of a commercial furunculosis vaccine and an autogenous vaccine
Gudmundsdottir, S., Lange, S., Magnadóttir, B. and Gudmundsdóttir, B.K. 2003. Protection against atypical furunculosis in Atlantic halibut, Hippoglossus hippoglossus (L.); comparison of a commercial furunculosis vaccine and an autogenous vaccine. Journal of Fish Diseases. 26 (6), pp. 331-338. doi:10.1046/j.1365-2761.2003.00462.x

Humoral immune parameters of cultured Atlantic halibut (Hippoglossus hippoglossus L.)
Lange, S., Guđmundsdottir, B.K. and Magnadóttir, B. 2001. Humoral immune parameters of cultured Atlantic halibut (Hippoglossus hippoglossus L.). Fish and Shellfish Immunology. 11 (6), pp. 523-535. doi:10.1006/fsim.2000.0333

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