The altered expression of perineuronal net elements during neural differentiation

• Autorzy: Eskici N.F. , Erdem-Ozdamar S. , Dayangac-Erden D.
• Języki publikacji: EN

Abstrakty

EN

Background: Perineuronal nets (PNNs), which are localized around neurons during development, are specialized forms of neural extracellular matrix with neuroprotective and plasticity-regulating roles. Hyaluronan and proteoglycan link protein 1 (HAPLN1), tenascin-R (TNR) and aggrecan (ACAN) are key elements of PNNs. In diseases characterized by neuritogenesis defects, the expression of these proteins is known to be downregulated, suggesting that PNNs may have a role in neural differentiation. Methods: In this study, the mRNA and protein levels of HAPLN1, TNR and ACAN were determined and compared at specific time points of neural differentiation. We used PC12 cells as the in vitro model because they reflect this developmental process. Results: On day 7, the HAPLN1 mRNA level showed a 2.9-fold increase compared to the non-differentiated state. However, the cellular HAPLN1 protein level showed a decrease, indicating that the protein may have roles in neural differentiation, and may be secreted during the early period of differentiation. By contrast, TNR mRNA and protein levels remained unchanged, and the amount of cellular ACAN protein showed a 3.7-fold increase at day 7. These results suggest that ACAN may be secreted after day 7, possibly due to its large amount of post-translational modifications. Conclusions: Our results provide preliminary data on the expression of PNN elements during neural differentiation. Further investigations will be performed on the role of these elements in neurological disease models.

• Wydawca: -
• Czasopismo: Cellular and Molecular Biology Letters
• Rocznik: 2018
• Tom: 23
• Opis fizyczny: p.1-12,fig.,ref.

Twórcy

autor

Eskici N.F.

• Faculty of Medicine Department of Medical Biology, Hacettepe University, Ankara, Turkey

autor

Erdem-Ozdamar S.

• Faculty of Medicine Department of Medical Biology, Hacettepe University, Ankara, Turkey

autor

Dayangac-Erden D.

• Faculty of Medicine Department of Medical Biology, Hacettepe University, Ankara, Turkey

Bibliografia

• 1. Yamada J, Jinno S. Spatio-temporal differences in perineuronal net expression in the mouse hippocampus, with reference to parvalbumin. Neuroscience. 2013;253:368–79.
• 2. Dzyubenko E, Gottschling C, Faissner A. Neuron-glia interactions in neural plasticity: contributions of neural extracellular matrix and Perineuronal nets. Neural Plasticity. 2016;2016:14.
• 3. Reichardt LF, Tomaselli KJ. Extracellular matrix molecules and their receptors: functions in neural development. Annu Rev Neurosci. 1991;14:531–70.
• 4. Giamanco KA, Morawski M, Matthews RT. Perineuronal net formation and structure in aggrecan knockout mice. Neuroscience. 2010;170(4):1314–27.
• 5. Kwok JC, Carulli D, Fawcett JW. In vitro modeling of perineuronal nets: hyaluronan synthase and link protein are necessary for their formation and integrity. J Neurochem. 2010;114(5):1447–59.
• 6. Mueller AL, Davis A, Sovich S, Carlson SS, Robinson FR. Distribution of N-Acetylgalactosamine-positive Perineuronal nets in the macaque brain: anatomy and implications. Neural Plasticity. 2016;2016:19.
• 7. Ueno H, Suemitsu S, Okamoto M, Matsumoto Y, Ishihara T. Parvalbumin neurons and perineuronal nets in the mouse prefrontal cortex. Neuroscience. 2017;343:115–27.
• 8. Kwok JC, Dick G, Wang D, Fawcett JW. Extracellular matrix and perineuronal nets in CNS repair. Dev Neurobiol. 2011;71(11):1073–89.
• 9. Giamanco KA, Matthews RT. Deconstructing the perineuronal net: cellular contributions and molecular composition of the neuronal extracellular matrix. Neuroscience. 2012;218:367–84.
• 10. Kiani C, Chen L, Wu YJ, Yee AJ, Yang BB. Structure and function of aggrecan. Cell Res. 2002;12(1):19–32.
• 11. Yamada J, Jinno S. Molecular heterogeneity of aggrecan-based perineuronal nets around five subclasses of parvalbumin-expressing neurons in the mouse hippocampus. J Comp Neurol. 2017;525(5):1234–49.
• 12. Horii-Hayashi N, Sasagawa T, Nishi M. Insights from extracellular matrix studies in the hypothalamus: structural variations of perineuronal nets and discovering a new perifornical area of the anterior hypothalamus. Anat Sci Int. 2017;92(1):18–24.
• 13. Mouw JK, Ou G, Weaver VM. Extracellular matrix assembly: a multiscale deconstruction. Nat Rev Mol Cell Biol. 2014;15(12):771–85.
• 14. Frischknecht R, Happel MFK. Impact of the extracellular matrix on plasticity in juvenile and adult brains. e-Neuroforum. 2016;7(1):1–6.
• 15. Su J, Cole J, Fox MA. Loss of interneuron-derived collagen XIX leads to a reduction in Perineuronal nets in the mammalian telencephalon. ASN Neuro. 2017;9(1):1759091416689020.
• 16. Thakur R, Mishra DP. Matrix reloaded: CCN, tenascin and SIBLING group of matricellular proteins in orchestrating cancer hallmark capabilities. Pharmacol Ther. 2016;168:61–74.
• 17. Pesheva P, Gloor S, Schachner M, Probstmeier R. Tenascin-R Is an intrinsic autocrine factor for oligodendrocyte differentiation and promotes cell adhesion by a SulfatideMediated mechanism. J Neurosci. 1997;17(12):4642–51.
• 18. Pesheva P, Probstmeier R, Skubitz AP, McCarthy JB, Furcht LT, Schachner M. Tenascin-R J1 160/180 inhibits fibronectin-mediated cell adhesion–functional relatedness to tenascin-C. J Cell Sci. 1994;107(Pt 8):2323–33.
• 19. Galtrey CM, Kwok JC, Carulli D, Rhodes KE, Fawcett JW. Distribution and synthesis of extracellular matrix proteoglycans, hyaluronan, link proteins and tenascin-R in the rat spinal cord. Eur J Neurosci. 2008;27(6):1373–90.
• 20. Chiquet-Ehrismann R. Tenascins. Int J Biochem Cell Biol. 2004;36(6):986–90.
• 21. Suttkus A, Morawski M, Arendt T. Protective properties of neural extracellular matrix. Mol Neurobiol. 2016;53(1):73–82.
• 22. Sethi MK, Zaia J. Extracellular matrix proteomics in schizophrenia and Alzheimer’s disease. Anal Bioanal Chem. 2017;409(2):379–94.
• 23. Fiedler A, Reinert T, Morawski M, Brückner G, Arendt T, Butz T. Intracellular iron concentration of neurons with and without perineuronal nets. Nucl Instrum Methods Phys Res, Sect B. 2007;260(1):153–8.
• 24. Morawski M, Bruckner MK, Riederer P, Bruckner G, Arendt T. Perineuronal nets potentially protect against oxidative stress. Exp Neurol. 2004;188(2):309–15.
• 25. Morawski M, Pavlica S, Seeger G, Grosche J, Kouznetsova E, Schliebs R, Bruckner G, Arendt T. Perineuronal nets are largely unaffected in Alzheimer model Tg2576 mice. Neurobiol Aging. 2010;31(7):1254–6.
• 26. Miyata S, Nishimura Y, Nakashima T. Perineuronal nets protect against amyloid beta-protein neurotoxicity in cultured cortical neurons. Brain Res. 2007;1150:200–6.
• 27. Morawski M, Bruckner G, Jager C, Seeger G, Arendt T. Neurons associated with aggrecan-based perineuronal nets are protected against tau pathology in subcortical regions in Alzheimer’s disease. Neuroscience. 2010;169(3):1347–63.
• 28. De Luca C, Papa M. Looking inside the matrix: Perineuronal nets in plasticity, maladaptive plasticity and neurological disorders. Neurochem Res. 2016;41(7):1507–15.
• 29. Bitanihirwe BKY, Mauney SA, Woo T-UW. Weaving a net of neurobiological mechanisms in schizophrenia and unraveling the underlying pathophysiology. Biol Psychiatry. 2016;80(8):589–98.
• 30. Wang Z, Winsor K, Nienhaus C, Hess E, Blackmore MG. Combined chondroitinase and KLF7 expression reduce net retraction of sensory and CST axons from sites of spinal injury. Neurobiol Dis. 2017;99:24–35.
• 31. Bowerman M, Shafey D, Kothary R. Smn depletion alters profilin II expression and leads to upregulation of the RhoA/ROCK pathway and defects in neuronal integrity. J Mol Neurosci. 2007;32(2):120–31.
• 32. Al-Bader MD, Al-Sarraf HA. Housekeeping gene expression during fetal brain development in the rat-validation by semi-quantitative RT-PCR. Brain Res Dev Brain Res. 2005;156(1):38–45.
• 33. Carulli D, Rhodes KE, Fawcett JW. Upregulation of aggrecan, link protein 1, and hyaluronan synthases during formation of perineuronal nets in the rat cerebellum. J Comp Neurol. 2007;501(1):83–94.
• 34. Gundelfinger ED, Frischknecht R, Choquet D, Heine M. Converting juvenile into adult plasticity: a role for the brain’s extracellular matrix. Eur J Neurosci. 2010;31(12):2156–65.
• 35. Lahiani A, Zahavi E, Netzer N, Ofir R, Pinzur L, Raveh S, Arien-Zakay H, Yavin E, Lazarovici P. Human PLacental eXpanded (PLX) mesenchymal-like adherent stromal cells confer neuroprotection to nerve growth factor (NGF)- differentiated PC12 cells exposed to ischemia by secretion of IL-6 and VEGF. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research. 2015;1853(2):422–30.
• 36. Garcia-Manteiga JM, Bonfiglio S, Malosio ML, Lazarevic D, Stupka E, Cittaro D, Meldolesi J. Epigenomics of neural cells: REST-induced down- and upregulation of gene expression in a two-clone PC12 cell model. Biomed Res Int. 2015;2015:13.
• 37. Slotkin TA, Card J, Stadler A, Levin ED, Seidler FJ. Effects of tobacco smoke on PC12 cell neurodifferentiation are distinct from those of nicotine or benzo[a]pyrene. Neurotoxicology and Teratology. 2014;43(Supplement C):19–24.
• 38. Costa LG. Neurotoxicity testing: a discussion of in vitro alternatives. Environ Health Perspect. 1998;106(Suppl 2):505–10.
• 39. Malagelada C, Greene LA. Chapter 29 - PC12 cells as a model for parkinson's disease research. In: Parkinson's Disease. San Diego: Academic press; 2008. p. 375–87.
• 40. Arien-Zakay H, Lecht S, Bercu MM, Tabakman R, Kohen R, Galski H, Nagler A, Lazarovici P. Neuroprotection by cord blood neural progenitors involves antioxidants, neurotrophic and angiogenic factors. Exp Neurol. 2009;216(1):83–94.
• 41. Carulli D, Pizzorusso T, Kwok JC, Putignano E, Poli A, Forostyak S, Andrews MR, Deepa SS, Glant TT, Fawcett JW. Animals lacking link protein have attenuated perineuronal nets and persistent plasticity. Brain. 2010;133(Pt 8): 2331–47.
• 42. Chiquet-Ehrismann R. Anti-adhesive molecules of the extracellular matrix. Curr Opin Cell Biol. 1991;3(5):800–4.
• 43. Miyata S, Kitagawa H. Chondroitin 6-Sulfation regulates Perineuronal net formation by controlling the stability of Aggrecan. Neural Plasticity. 2016;2016:13.
• 44. Bustin S. Molecular biology of the cell, sixth edition; ISBN: 9780815344643; and molecular biology of the cell, sixth edition, the problems book; ISBN 9780815344537. Int J Mol Sci. 2015;16(12):28123–5.
• 45. Vogel C, Marcotte EM. Insights into the regulation of protein abundance from proteomic and transcriptomic analyses. Nat Rev Genet. 2012;13(4):227–32.
• 46. Ghazalpour A, Bennett B, Petyuk VA, Orozco L, Hagopian R, Mungrue IN, Farber CR, Sinsheimer J, Kang HM, Furlotte N, et al. Comparative analysis of proteome and transcriptome variation in mouse. PLoS Genet. 2011;7(6):e1001393.
• 47. Davies E, Stankovic B, Vian A, Wood AJ. Where has all the message gone? Plant Sci. 2012;185-186:23–32.
• 48. Payne SH. The utility of protein and mRNA correlation. Trends Biochem Sci. 2015;40(1):1–3.
• 49. Uhlén M, Fagerberg L, Hallström BM, Lindskog C, Oksvold P, Mardinoglu A, Sivertsson Å, Kampf C, Sjöstedt E, Asplund A, et al. Tissue-based map of the human proteome. Science. 2015;347(6220)
• 50. Edfors F, Danielsson F, Hallstrom BM, Kall L, Lundberg E, Ponten F, Forsstrom B, Uhlen M. Gene-specific correlation of RNA and protein levels in human cells and tissues. Mol Syst Biol. 2016;12(10):883.

Identyfikatory

DOI

10.1186/s11658-018-0073-5