A comparison of the mitochondrial proteome and lipidome in the mouse and long-lived Pipistrelle bats

Abstract

It is accepted that smaller mammals with higher metabolic rates have shorter lifespans. The very few species that do not follow these rules can give insights into interesting differences. The recorded maximum lifespans of bats are exceptional - over 40 years, compared with the laboratory mouse of 4 years. We investigated the differences in the biochemical composition of mitochondria between bat and mouse species. We used proteomics and ultra-high-performance liquid chromatography coupled with high resolution mass spectrometry lipidomics, to interrogate mitochondrial fractions prepared from Mus musculus and Pipistrellus pipistrellus brain and skeletal muscle. Fatty acid binding protein 3 was found at different levels in mouse and bat muscle mitochondria and its orthologues were investigated in Caenorhabditis elegans knock-downs for LBP 4, 5 and 6. In the bat, high levels of free fatty acids and N-acylethanolamine lipid species together with a significantly greater abundance of fatty acid binding protein 3 in muscle (1.8-fold, p =0.037) were found. Manipulation of fatty acid binding protein orthologues in C. elegans suggest these proteins and their role in lipid regulation are important for mitochondrial function.

The dysregulated Pink1-Drosophila mitochondrial proteome is partially corrected with exercise

“…Label-free mass spectrometry analyses generated proteomes that we used in network enrichment analysis. Previously we have used proteomic profiling to characterise mitochondrial populations in both mice and long-lived pipistrelle bats, and here we apply this to better understand the PD phenotype as well as possible changes due to exercise (Pollard et al, 2016(Pollard et al, , 2019.…”

Optimizing dissection, sample collection and cell isolation protocols for frugivorous bats

“…Here we characterized sample collection and utilization of almost all tissues from fruit bats. While multiple groups have used bats in in vivo scientific studies for physiology (Chen, Zhu, Jones, Zhang, & Sun, 2013;Harrison & Roberts, 2000;Suarez, Hanna, & Herrera, 2009;Suarez, Welch, Hanna, & Herrera, 2009b), metabolism (Arévalo, Pérez-Suárez, & Lóapez-Luna, 1991;Bell, Price, Balthes, Cordon, & Wormell, 2019;Brunet-Rossinni, 2004;Foley et al, 2018;Funakoshi & Kunisaki, 1991;Healy et al, 2014;Hernández-Arciga et al, 2018;McMichael et al, 2016McMichael et al, , 2015Peng et al, 2017;Podlutsky, Khritankov, Ovodov, & Austad, 2005), evolution (Currie, Stawski, & Geiser, 2018;Moreno-Santillán, Machain-Williams, Hernández-Montes, & Ortega, 2019;Pollard et al, 2019;Seim et al, 2013;Shen et al, 2010) or immunological/virological studies (Aguilar-Setién et al, 2008;Ahn et al, 2019;Aída, Herrera, Flores-Martínez, & Welch, 2016;Allen, Sims, & Singht, n.d.;Barr et al, 2012;Chakravarty & Paul, 1987;Halpin et al, 2011;Davis et al, 2005;Cabrera-Romo et al, 2014;Hughes et al, 2006;Jones et al, 2015;Kandeil et al, 2019;Mackie et al, 2017;Obregón-Morales et al, 2017;…”

“…Here we characterized sample collection and utilization of almost all tissues from fruit bats. While multiple groups have used bats in in vivo scientific studies for physiology (Chen, Zhu, Jones, Zhang, & Sun, ; Harrison & Roberts, ; Suarez, Hanna, & Herrera, ; Suarez, Welch, Hanna, & Herrera, ), metabolism (Arévalo, Pérez‐Suárez, & Lóapez‐Luna, ; Bell, Price, Balthes, Cordon, & Wormell, ; Brunet‐Rossinni, ; Foley et al, ; Funakoshi & Kunisaki, ; Healy et al, ; Hernández‐Arciga et al, ; McMichael et al, , ; Peng et al, ; Podlutsky, Khritankov, Ovodov, & Austad, ), evolution (Currie, Stawski, & Geiser, ; Moreno‐Santillán, Machain‐Williams, Hernández‐Montes, & Ortega, ; Pollard et al, ; Seim et al, ; Shen et al, ) or immunological/virological studies (Aguilar‐Setién et al, ; Ahn et al, ; Aída, Herrera, Flores‐Martínez, & Welch, ; Allen, Sims, & Singht, n.d.; Barr et al, ; Chakravarty & Paul, ; Halpin et al, ; Davis et al, ; Cabrera‐Romo et al, ; Hughes et al, ; Jones et al, ; Kandeil et al, ; Mackie et al, ; Obregón‐Morales et al, ; Paweska et al, ; Perea‐Martínez et al, ; Sarkar & Chakravarty, ; Sullivan, Grimes, Eads, Menzies, & Irons, ; Swanepoel et al, ; Tong et al, ; Watanabe et al, ; Weise, Czirják, Lindecke, Bumrungsri, & Voigt, ; Yob et al, ), there is no detailed description of the methods required for efficient processing. Consistent, fast, methodology will benefit comparative biology studies on bats across multiple disciplines.…”

“…As such they developed unique biological properties to cope as warm-blooded mammals (Peng et al, 2017;Suarez, Welch, Hanna, & Herrera, 2009a;Thomas, 1975;Voigt & Winter, 1999). This includes evolution of their metabolic pathways, mitochondria and OXPHOS pathways, to cope with high energy demands (Jebb, Foley, Puechmaille, & Teeling, 2017;Pollard et al, 2019;Revel, Fawcett, & Philpott, 1963;Shen et al, 2010). Additionally, they have developed multiple mechanisms to deal with resulting temperature fluctuations, up to 42°C during flight.…”

Feeding recombinant Royalactin: Measures of improved lifespan and mitochondrial function inCaenorhabditis elegans

“…Evolutionarily conserved pathways and molecular networks are affected by these ageing processes, with mitochondrial dysfunction considered to be a common denominator [1,2]. Organisms have characteristic average lifespans and the comparative biology of long- and short-lived organisms offers a route towards untangling biochemical variations which account for lifespan differences [3,4]. Remarkable interspecific differences in lifespan can also be observed.…”