Comparison of plasma and cerebrospinal fluid proteomes identifies gene products guiding adult neurogenesis and neural differentiation in birds

. 2021 Mar 05 ; 11 (1) : 5312. [epub] 20210305

Jazyk angličtina Země Velká Británie, Anglie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid33674647
Odkazy

PubMed 33674647
PubMed Central PMC7935914
DOI 10.1038/s41598-021-84274-x
PII: 10.1038/s41598-021-84274-x
Knihovny.cz E-zdroje

Cerebrospinal fluid (CSF) proteins regulate neurogenesis, brain homeostasis and participate in signalling during neuroinflammation. Even though birds represent valuable models for constitutive adult neurogenesis, current proteomic studies of the avian CSF are limited to chicken embryos. Here we use liquid chromatography-tandem mass spectrometry (nLC-MS/MS) to explore the proteomic composition of CSF and plasma in adult chickens (Gallus gallus) and evolutionarily derived parrots: budgerigar (Melopsittacus undulatus) and cockatiel (Nymphicus hollandicus). Because cockatiel lacks a complete genome information, we compared the cross-species protein identifications using the reference proteomes of three model avian species: chicken, budgerigar and zebra finch (Taeniopygia guttata) and found the highest identification rates when mapping against the phylogenetically closest species, the budgerigar. In total, we identified 483, 641 and 458 unique proteins consistently represented in the CSF and plasma of all chicken, budgerigar and cockatiel conspecifics, respectively. Comparative pathways analyses of CSF and blood plasma then indicated clusters of proteins involved in neurogenesis, neural development and neural differentiation overrepresented in CSF in each species. This study provides the first insight into the proteomics of adult avian CSF and plasma and brings novel evidence supporting the adult neurogenesis in birds.

Zobrazit více v PubMed

Illes, S. Chapter 3 - More than a drainage fluid: the role of CSF in signaling in the brain and other effects on brain tissue. in Handbook of Clinical Neurology (eds. Deisenhammer, F., Teunissen, C. E. & Tumani, H.) vol. 146 33–46, 10.1016/B978-0-12-804279-3.00003-4 (Elsevier, 2018). PubMed

Reiber H. Dynamics of brain-derived proteins in cerebrospinal fluid. Clin. Chim. Acta. 2001;310:173–186. doi: 10.1016/S0009-8981(01)00573-3. PubMed DOI

Lindsey BW, Tropepe V. A comparative framework for understanding the biological principles of adult neurogenesis. Prog. Neurobiol. 2006;80:281–307. doi: 10.1016/j.pneurobio.2006.11.007. PubMed DOI

Villeda, S. A. et al. The ageing systemic milieu negatively regulates neurogenesis and cognitive function. Nature477, 90–94, 10.1038/nature10357 (2011). PubMed DOI PMC

Bachy I, Kozyraki R, Wassef M. The particles of the embryonic cerebrospinal fluid: How could they influence brain development? Brain Res. Bull. 2008;75:289–294. doi: 10.1016/j.brainresbull.2007.10.010. PubMed DOI

Zappaterra, M. W. & Lehtinen, M. K. The cerebrospinal fluid: regulator of neurogenesis, behavior, and beyond. Cell. Mol. Life Sci. 69, 2863–2878, 10.1007/s00018-012-0957-x (2012). PubMed DOI PMC

Fame RM, Lehtinen MK. Emergence and developmental roles of the cerebrospinal fluid system. Dev. Cell. 2020;52:261–275. doi: 10.1016/j.devcel.2020.01.027. PubMed DOI

Sawamoto K, et al. New neurons follow the flow of cerebrospinal fluid in the adult brain. Science. 2006;311:629–632. doi: 10.1126/science.1119133. PubMed DOI

Lehtinen MK, et al. The cerebrospinal fluid provides a proliferative niche for neural progenitor cells. Neuron. 2011;69:893–905. doi: 10.1016/j.neuron.2011.01.023. PubMed DOI PMC

Parada, C., Gato, A., Aparicio, M. & Bueno, D. Proteome analysis of chick embryonic cerebrospinal fluid. Proteomics6, 312–320, 10.1002/pmic.200500085 (2006). PubMed DOI

Parada C, Gato Á, Bueno D. Mammalian embryonic cerebrospinal fluid proteome has greater apolipoprotein and enzyme pattern complexity than the avian proteome. J. Proteome Res. 2005;4:2420–2428. doi: 10.1021/pr050213t. PubMed DOI

Zappaterra MD, et al. A comparative proteomic analysis of human and rat embryonic cerebrospinal fluid. J. Proteome Res. 2007;6:3537–3548. doi: 10.1021/pr070247w. PubMed DOI

Smith JS, et al. Characterization of individual mouse cerebrospinal fluid proteomes. Proteomics. 2014;14:1102–1106. doi: 10.1002/pmic.201300241. PubMed DOI PMC

Macron, C., Lane, L., Núñez Galindo, A. & Dayon, L. Deep Dive on the Proteome of human cerebrospinal fluid: a valuable data resource for biomarker discovery and missing protein identification. J. Proteome Res.17, 4113–4126, 10.1021/acs.jproteome.8b00300 (2018). PubMed DOI

Macron C, et al. Exploration of human cerebrospinal fluid: A large proteome dataset revealed by trapped ion mobility time-of-flight mass spectrometry. Data Brief. 2020;31:105704. doi: 10.1016/j.dib.2020.105704. PubMed DOI PMC

Begcevic I, Brinc D, Drabovich AP, Batruch I, Diamandis EP. Identification of brain-enriched proteins in the cerebrospinal fluid proteome by LC-MS/MS profiling and mining of the Human Protein Atlas. Clin. Proteomics. 2016;13:11. doi: 10.1186/s12014-016-9111-3. PubMed DOI PMC

Barker JM, Boonstra R, Wojtowicz JM. From pattern to purpose: how comparative studies contribute to understanding the function of adult neurogenesis. Eur. J. Neurosci. 2011;34:963–977. doi: 10.1111/j.1460-9568.2011.07823.x. PubMed DOI

Barnea A, Pravosudov V. Birds as a model to study adult neurogenesis: bridging evolutionary, comparative and neuroethological approaches. Eur. J. Neurosci. 2011;34:884–907. doi: 10.1111/j.1460-9568.2011.07851.x. PubMed DOI PMC

Patel VJ, et al. A comparison of labeling and label-free mass spectrometry-based proteomics approaches. J. Proteome Res. 2009;8:3752–3759. doi: 10.1021/pr900080y. PubMed DOI

Zhang G, et al. Comparative genomics reveals insights into avian genome evolution and adaptation. Science. 2014;346:1311–1320. doi: 10.1126/science.1251385. PubMed DOI PMC

Clayton NS, Emery NJ. Avian models for human cognitive neuroscience: a proposal. Neuron. 2015;86:1330–1342. doi: 10.1016/j.neuron.2015.04.024. PubMed DOI

Olkowicz S, et al. Birds have primate-like numbers of neurons in the forebrain. Proc. Natl. Acad. Sci. 2016;113:7255–7260. doi: 10.1073/pnas.1517131113. PubMed DOI PMC

Němec P, Osten P. The evolution of brain structure captured in stereotyped cell count and cell type distributions. Curr. Opin. Neurobiol. 2020;60:176–183. doi: 10.1016/j.conb.2019.12.005. PubMed DOI PMC

Wirthlin M, et al. Parrot genomes and the evolution of heightened longevity and cognition. Curr. Biol. 2018;28:4001–4008.e7. doi: 10.1016/j.cub.2018.10.050. PubMed DOI PMC

Iwaniuk AN, Dean KM, Nelson JE. Interspecific allometry of the brain and brain regions in parrots (Psittaciformes): comparisons with other birds and primates. Brain. Behav. Evol. 2005;65:40–59. doi: 10.1159/000081110. PubMed DOI

Auersperg AMI, Szabo B, von Bayern AMP, Bugnyar T. Object permanence in the Goffin cockatoo (Cacatua goffini) J. Comp. Psychol. 2014;128:88–98. doi: 10.1037/a0033272. PubMed DOI

Pepperberg IM, Willner MR, Gravitz LB. Development of Piagetian object permanence in grey parrot (Psittacus erithacus) J. Comp. Psychol. 1997;111:63–75. doi: 10.1037/0735-7036.111.1.63. PubMed DOI

Emery NJ, Clayton NS. Evolution of the avian brain and intelligence. Curr. Biol. 2005;15:R946–R950. doi: 10.1016/j.cub.2005.11.029. PubMed DOI

Péron F, Rat-Fischer L, Lalot M, Nagle L, Bovet D. Cooperative problem solving in African grey parrots (Psittacus erithacus) Anim. Cognit. 2011;14:545–553. doi: 10.1007/s10071-011-0389-2. PubMed DOI

Hobson EA, Avery ML, Wright TF. The socioecology of Monk Parakeets: Insights into parrot social complexitySocioecología de Myiopsitta monachus: Revelaciones de la complejidad social de los lorosMonk Parakeet socioecology. Auk Ornithol. Adv. 2014;131:756–775. doi: 10.1642/AUK-14-14.1. DOI

Brauth SE, Heaton JT, Shea SD, Durand SE, Hall WS. Functional Anatomy of Forebrain Vocal Control Pathways in the Budgerigar (Melopsittacus undulatus)a. Ann. N. Y. Acad. Sci. 1997;807:368–385. doi: 10.1111/j.1749-6632.1997.tb51933.x. PubMed DOI

Pepperberg, I. M. The Alex Studies: cognitive and communicative abilities of grey parrots, (Harvard University Press, 2009). PubMed

Emery, N. J. Cognitive ornithology: the evolution of avian intelligence. Philos. Trans. R. Soc. B Biol. Sci.361, 23–43, 10.1098/rstb.2005.1736 (2006). PubMed DOI PMC

Güntürkün O, Bugnyar T. Cognition without Cortex. Trends Cognit. Sci. 2016;20:291–303. doi: 10.1016/j.tics.2016.02.001. PubMed DOI

Lambert, M. L., Jacobs, I., Osvath, M. & Bayern, A. M. P. von. Birds of a feather? Parrot and corvid cognition compared. Behaviour156, 505–594, 10.1163/1568539X-00003527 (2019). DOI

Iwaniuk AN, Nelson JE. Developmental differences are correlated with relative brain size in birds: a comparative analysis. Can. J. Zool. 2003;81:1913–1928. doi: 10.1139/z03-190. DOI

Munshi-South J, Wilkinson GS. Diet Influences Life Span in Parrots (Psittaciformes) Auk. 2006;123:108–118. doi: 10.1093/auk/123.1.108. DOI

Provost KL, Joseph L, Smith BT. Resolving a phylogenetic hypothesis for parrots: implications from systematics to conservation. Emu - Austral Ornithol. 2018;118:7–21. doi: 10.1080/01584197.2017.1387030. DOI

Wright, J. C., Beynon, R. J. & Hubbard, S. J. Cross Species Proteomics. in Proteome Bioinformatics (eds. Hubbard, S. J. & Jones, A. R.) 123–135, 10.1007/978-1-60761-444-9_9 (Humana Press, 2010). PubMed DOI

Liska, A. J. & Shevchenko, A. Expanding the organismal scope of proteomics: Cross-species protein identification by mass spectrometry and its implications. Proteomics3, 19–28, 10.1002/pmic.200390004 (2003). PubMed DOI

Dayon, L. et al. Proteomes of paired human cerebrospinal fluid and plasma: relation to blood–brain barrier permeability in older adults. J. Proteome Res. 18, 1162–1174, 10.1021/acs.jproteome.8b00809 (2019). PubMed

Guldbrandsen A, et al. In-depth characterization of the cerebrospinal fluid (CSF) proteome displayed through the CSF proteome resource (CSF-PR) Mol. Cell. Proteomics MCP. 2014;13:3152–3163. doi: 10.1074/mcp.M114.038554. PubMed DOI PMC

Thompson, E. J. CHAPTER 4 - Differences between proteins in CSF and serum. in Proteins of the Cerebrospinal Fluid (ed. Thompson, E. J.) 33–41, https://doi.org/10.1016/B978-012369369-3/50007-2 (Academic Press, 2005).

Reiber H. Proteins in cerebrospinal fluid and blood: barriers, CSF flow rate and source-related dynamics. Restor. Neurol. Neurosci. 2003;21:79–96. PubMed

Anderson NL, Anderson NG. The human plasma proteome: history, character, and diagnostic prospects. Mol. Cell. Proteomics. 2002;1:845–867. doi: 10.1074/mcp.R200007-MCP200. PubMed DOI

Aasebø E, et al. Effects of blood contamination and the rostro-caudal gradient on the human cerebrospinal fluid proteome. PLoS ONE. 2014;9:e90429. doi: 10.1371/journal.pone.0090429. PubMed DOI PMC

You J-S, et al. The impact of blood contamination on the proteome of cerebrospinal fluid. Proteomics. 2005;5:290–296. doi: 10.1002/pmic.200400889. PubMed DOI

Zhang C. Proteomic studies on the development of the central nervous system and beyond. Neurochem. Res. 2010;35:1487–1500. doi: 10.1007/s11064-010-0218-z. PubMed DOI

Macron, C., Lane, L., Núñez Galindo, A. & Dayon, L. Identification of missing proteins in normal human cerebrospinal fluid. J. Proteome Res.17, 4315–4319, 10.1021/acs.jproteome.8b00194 (2018). PubMed

Kroksveen AC, et al. In-depth cerebrospinal fluid quantitative proteome and deglycoproteome analysis: presenting a comprehensive picture of pathways and processes affected by multiple sclerosis. J. Proteome Res. 2017;16:179–194. doi: 10.1021/acs.jproteome.6b00659. PubMed DOI

Nilsson C, et al. Circadian variation in human cerebrospinal fluid production measured by magnetic resonance imaging. Am. J. Physiol.-Regul. Integr. Comp. Physiol. 1992;262:R20–R24. doi: 10.1152/ajpregu.1992.262.1.R20. PubMed DOI

Pan S, et al. A combined dataset of human cerebrospinal fluid proteins identified by multi-dimensional chromatography and tandem mass spectrometry. Proteomics. 2007;7:469–473. doi: 10.1002/pmic.200600756. PubMed DOI

Parada, C., Parvas, M. & Bueno, D. Cerebrospinal Fluid Proteomes: From Neural Development to Neurodegenerative Diseases. Current Proteomics, 4, 89–106, 10.2174/157016407782194611 (2007).

Thouvenot E, et al. Enhanced detection of CNS cell secretome in plasma protein-depleted cerebrospinal fluid. J. Proteome Res. 2008;7:4409–4421. doi: 10.1002/pmic.200600096. PubMed DOI

Finehout EJ, Franck Z, Choe LH, Relkin N, Lee KH. Cerebrospinal fluid proteomic biomarkers for Alzheimer’s disease. Ann. Neurol. 2007;61:120–129. doi: 10.1002/ana.21038. PubMed DOI

Lehtinen MK, Walsh CA. Neurogenesis at the brain-cerebrospinal fluid interface. Annu. Rev. Cell Dev. Biol. 2011;27:653–679. doi: 10.1146/annurev-cellbio-092910-154026. PubMed DOI PMC

Martín C, et al. FGF2 plays a key role in embryonic cerebrospinal fluid trophic properties over chick embryo neuroepithelial stem cells. Dev. Biol. 2006;297:402–416. doi: 10.1016/j.ydbio.2006.05.010. PubMed DOI

Salehi Z, Mashayekhi F, Naji M, Pandamooz S. Insulin-like growth factor-1 and insulin-like growth factor binding proteins in cerebrospinal fluid during the development of mouse embryos. J. Clin. Neurosci. 2009;16:950–953. doi: 10.1016/j.jocn.2008.09.018. PubMed DOI

Buddensiek J, Dressel A, Kowalski M, Storch A, Sabolek M. Adult cerebrospinal fluid inhibits neurogenesis but facilitates gliogenesis from fetal rat neural stem cells. J. Neurosci. Res. 2009;87:3054–3066. doi: 10.1002/jnr.22150. PubMed DOI

Buddensiek J, et al. Cerebrospinal fluid promotes survival and astroglial differentiation of adult human neural progenitor cells but inhibits proliferation and neuronal differentiation. BMC Neurosci. 2010;11:48. doi: 10.1186/1471-2202-11-48. PubMed DOI PMC

Gato A, Alonso MI, Lamus F, Miyan J. Neurogenesis: a process ontogenically linked to brain cavities and their content CSF. Semin. Cell Dev. Biol. 2020;102:21–27. doi: 10.1016/j.semcdb.2019.11.008. PubMed DOI

Alvarez-Buylla A, Nottebohm F. Migration of young neurons in adult avian brain. Nature. 1988;335:353–354. doi: 10.1038/335353a0. PubMed DOI

Goldman SA, Nottebohm F. Neuronal production, migration, and differentiation in a vocal control nucleus of the adult female canary brain. Proc. Natl. Acad. Sci. USA. 1983;80:2390–2394. doi: 10.1073/pnas.80.8.2390. PubMed DOI PMC

Patel SN, Clayton NS, Krebs JR. Spatial learning induces neurogenesis in the avian brain. Behav. Brain Res. 1997;89:115–128. doi: 10.1016/S0166-4328(97)00051-X. PubMed DOI

Ling C, Zuo M, Alvarez-Buylla A, Cheng MF. Neurogenesis in juvenile and adult ring doves. J. Comp. Neurol. 1997;379:300–312. doi: 10.1002/(SICI)1096-9861(19970310)379:2<300::AID-CNE10>3.0.CO;2-T. PubMed DOI

Mezey S, et al. Postnatal changes in the distribution and density of neuronal nuclei and doublecortin antigens in domestic chicks (Gallus domesticus) J. Comp. Neurol. 2012;520:100–116. doi: 10.1002/cne.22696. PubMed DOI

Melleu FF, Santos TS, Lino-de-Oliveira C, Marino-Neto J. Distribution and characterization of doublecortin-expressing cells and fibers in the brain of the adult pigeon (Columba livia) J. Chem. Neuroanat. 2013;47:57–70. doi: 10.1016/j.jchemneu.2012.10.006. PubMed DOI

Mazengenya P, Bhagwandin A, Nkomozepi P, Manger PR, Ihunwo AO. Putative adult neurogenesis in two domestic pigeon breeds (Columba livia domestica): racing homer versus utility carneau pigeons. Neural Regen. Res. 2017;12:1086–1096. doi: 10.4103/1673-5374.211187. PubMed DOI PMC

Mazengenya P, Bhagwandin A, Manger PR, Ihunwo AO. Putative Adult Neurogenesis in Old World Parrots: The Congo African Grey Parrot (Psittacus erithacus) and Timneh Grey Parrot (Psittacus timneh) Front. Neuroanat. 2018;12:7. doi: 10.3389/fnana.2018.00007. PubMed DOI PMC

Mazengenya P, Bhagwandin A, Ihunwo AO. Putative adult neurogenesis in palaeognathous birds: The common ostrich (Struthio camelus) and emu (Dromaius novaehollandiae) Int. J. Dev. Neurosci. 2020;80:613–635. doi: 10.1002/jdn.10057. PubMed DOI

Shohayeb B, Diab M, Ahmed M, Ng DCH. Factors that influence adult neurogenesis as potential therapy. Transl. Neurodegener. 2018;7:4. doi: 10.1186/s40035-018-0109-9. PubMed DOI PMC

Doetsch F, Scharff C. Challenges for Brain Repair: Insights from Adult Neurogenesis in Birds and Mammals. Brain. Behav. Evol. 2001;58:306–322. doi: 10.1159/000057572. PubMed DOI

Anderson DK, Hazelwood RL. Chicken cerebrospinal fluid: normal composition and response to insulin administration. J. Physiol. 1969;202:83–95. doi: 10.1113/jphysiol.1969.sp008796. PubMed DOI PMC

Černá M, Kuntová B, Talacko P, Stopková R, Stopka P. Differential regulation of vaginal lipocalins (OBP, MUP) during the estrous cycle of the house mouse. Sci. Rep. 2017;7:1–10. doi: 10.1038/s41598-017-12021-2. PubMed DOI PMC

Cox J, et al. Accurate Proteome-wide Label-free Quantification by Delayed Normalization and Maximal Peptide Ratio Extraction Termed MaxLFQ. Mol. Cell. Proteomics MCP. 2014;13:2513–2526. doi: 10.1074/mcp.M113.031591. PubMed DOI PMC

Rodriguez J, Gupta N, Smith RD, Pevzner PA. Does Trypsin Cut Before Proline? J. Proteome Res. 2008;7:300–305. doi: 10.1021/pr0705035. PubMed DOI

Perez-Riverol, Y. et al. The PRIDE database and related tools and resources in 2019: improving support for quantification data. Nucleic Acids Res. 47, D442–D450, 10.1093/nar/gky1106 (2019). PubMed PMC

Hillier LW, et al. Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature. 2004;432:695–716. doi: 10.1038/nature03154. PubMed DOI

Ganapathy G, et al. High-coverage sequencing and annotated assemblies of the budgerigar genome. GigaScience. 2014;3:11. doi: 10.1186/2047-217X-3-11. PubMed DOI PMC

Kriventseva EV, et al. OrthoDB v10: sampling the diversity of animal, plant, fungal, protist, bacterial and viral genomes for evolutionary and functional annotations of orthologs. Nucleic Acids Res. 2019;47:D807–D811. doi: 10.1093/nar/gky1053. PubMed DOI PMC

Thomas PD, et al. PANTHER: A Library of Protein Families and Subfamilies Indexed by Function. Genome Res. 2003;13:2129–2141. doi: 10.1101/gr.772403. PubMed DOI PMC

Ashburner M, et al. Gene Ontology: tool for the unification of biology. Nat. Genet. 2000;25:25–29. doi: 10.1038/75556. PubMed DOI PMC

Reimand J, et al. g:Profiler: a web server for functional interpretation of gene lists (2016 update) Nucleic Acids Res. 2016;44:W83–W89. doi: 10.1093/nar/gkw199. PubMed DOI PMC

Kanehisa M, Furumichi M, Tanabe M, Sato Y, Morishima K. KEGG: new perspectives on genomes, pathways, diseases and drugs. Nucleic Acids Res. 2017;45:D353–D361. doi: 10.1093/nar/gkw1092. PubMed DOI PMC

Fabregat A, et al. The Reactome pathway knowledgebase. Nucleic Acids Res. 2018;46:D649–D655. doi: 10.1093/nar/gkx1132. PubMed DOI PMC

R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.r-project.org/ (2020).

Hulsen T, de Vlieg J, Alkema W. BioVenn: a web application for the comparison and visualization of biological lists using area-proportional Venn diagrams. BMC Genomics. 2008;9:488. doi: 10.1186/1471-2164-9-488. PubMed DOI PMC

Bardou P, Mariette J, Escudié F, Djemiel C, Klopp C. jvenn: an interactive Venn diagram viewer. BMC Bioinform. 2014;15:293. doi: 10.1186/1471-2105-15-293. PubMed DOI PMC

Huber W, von Heydebreck A, Sültmann H, Poustka A, Vingron M. Variance stabilization applied to microarray data calibration and to the quantification of differential expression. Bioinformatics. 2002;18:S96–S104. doi: 10.1093/bioinformatics/18.suppl_1.S96. PubMed DOI

Välikangas T, Suomi T, Elo LL. A systematic evaluation of normalization methods in quantitative label-free proteomics. Brief. Bioinform. 2016;19:1–11. doi: 10.1093/bib/bbw095. PubMed DOI PMC

von Mering C, et al. STRING: a database of predicted functional associations between proteins. Nucleic Acids Res. 2003;31:258–261. doi: 10.1093/nar/gkg034. PubMed DOI PMC

Ge SX, Jung D, Yao R. ShinyGO: a graphical gene-set enrichment tool for animals and plants. Bioinformatics. 2020;36:2628–2629. doi: 10.1093/bioinformatics/btz931. PubMed DOI PMC

Subramanian A, et al. Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. 2005;102:15545–15550. doi: 10.1073/pnas.0506580102. PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...