Long Non-coding RNAs Influence Aging Process of Sciatic Nerves in SD Rats


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Objectives:To investigate the long non-coding RNAs (lncRNAs) changes in the sciatic nerve (SN) in Sprague Dawley (SD) rats during aging.

Methods:Eighteen healthy SD rats were selected at the age of 1 month (1M) and 24 months (24M) and SNs were collected. High-throughput transcriptome sequencing and bioinformatics analysis were performed. Protein-protein interaction (PPI) networks and competing endogenous RNA (ceRNA) networks were established according to differentially expressed genes (DEGs).

Result:As the length of lncRNAs increased, its proportion to the total number of lncRNAs decreased. A total of 4079 DElncRNAs were identified in Con vs. 24M. GO analysis was primarily clustered in nerve and lipid metabolism, extracellular matrix, and vascularization-related fields. There were 17 nodes in the PPI network of the target genes of up-regulating genes including Itgb2, Lox, Col11a1, Wnt5a, Kras, etc. Using quantitative RT-PCR, microarray sequencing accuracy was validated. There were 169 nodes constructing the PPI network of down-regulated target genes, mainly including Col1a1, Hmgcs1, Hmgcr. CeRNA interaction networks were constructed.

Conclusion:Lipid metabolism, angiogenesis, and ECM fields might play an important role in the senescence process in SNs. Col3a1, Serpinh1, Hmgcr, and Fdps could be candidates for nerve aging research.

作者简介

Rui Kuang

Department of Plastic Surgery, First Affiliated Hospital of Sun Yat-sen University

Email: info@benthamscience.net

Yi Zhang

Department of Plastic Surgery, First Affiliated Hospital of Sun Yat-sen University

Email: info@benthamscience.net

Guanggeng Wu

Department of Plastic Surgery, First Affiliated Hospital of Sun Yat-sen University

Email: info@benthamscience.net

Zhaowei Zhu

Department of Plastic Surgery, First Affiliated Hospital of Sun Yat-sen University

Email: info@benthamscience.net

Shuqia Xu

Department of Plastic Surgery, First Affiliated Hospital of Sun Yat-sen University

Email: info@benthamscience.net

Xiangxia Liu

Department of Plastic Surgery, University of Tennessee Health Science Center

编辑信件的主要联系方式.
Email: info@benthamscience.net

Yangbin Xu

Department of Plastic Surgery, First Affiliated Hospital of Sun Yat-sen University

编辑信件的主要联系方式.
Email: info@benthamscience.net

Yunxiang Luo

Department of Plastic Surgery, First Affiliated Hospital of Sun Yat-sen University

编辑信件的主要联系方式.
Email: info@benthamscience.net

参考

  1. Schellnegger, M.; Lin, A.C.; Hammer, N.; Kamolz, L.P. Physical activity on telomere length as a biomarker for aging: A systematic review. Sports Med. Open, 2022, 8(1), 111. doi: 10.1186/s40798-022-00503-1 PMID: 36057868
  2. Sardella-Silva, G.; Mietto, B.S.; Ribeiro-Resende, V.T. Four seasons for schwann cell biology, revisiting key periods: Development, homeostasis, repair, and aging. Biomolecules, 2021, 11(12), 1887. doi: 10.3390/biom11121887 PMID: 34944531
  3. Verdier, V.; Csárdi, G.; de Preux-Charles, A.S.; Médard, J.J.; Smit, A.B.; Verheijen, M.H.G.; Bergmann, S.; Chrast, R. Aging of myelinating glial cells predominantly affects lipid metabolism and immune response pathways. Glia, 2012, 60(5), 751-760. doi: 10.1002/glia.22305 PMID: 22337502
  4. Hamilton, R.; Walsh, M.; Singh, R.; Rodriguez, K.; Gao, X.; Rahman, M.M.; Chaudhuri, A.; Bhattacharya, A. Oxidative damage to myelin proteins accompanies peripheral nerve motor dysfunction in aging C57BL/6 male mice. J. Neurol. Sci., 2016, 370, 47-52. doi: 10.1016/j.jns.2016.09.021 PMID: 27772785
  5. Schneider-Poetsch, T.; Yoshida, M. Along the central dogma-controlling gene expression with small molecules. Annu. Rev. Biochem., 2018, 87(1), 391-420. doi: 10.1146/annurev-biochem-060614-033923 PMID: 29727582
  6. Glasgow, S.M.; Deneen, B. lnc’edin to myelin. Neuron, 2017, 93(2), 252-254. doi: 10.1016/j.neuron.2017.01.002 PMID: 28103473
  7. Scheib, J.; Höke, A. Advances in peripheral nerve regeneration. Nat. Rev. Neurol., 2013, 9(12), 668-676. doi: 10.1038/nrneurol.2013.227 PMID: 24217518
  8. Djuanda, D.; He, B.; Liu, X.; Xu, S.; Zhang, Y.; Xu, Y.; Zhu, Z. Comprehensive analysis of age-related changes in lipid metabolism and myelin sheath formation in sciatic nerves. J. Mol. Neurosci., 2021, 71(11), 2310-2323. doi: 10.1007/s12031-020-01768-5 PMID: 33492614
  9. Liu, JH.; Tang, Q.; Liu, XX.; Qi, J.; Zeng, RX.; Zhu, ZW.; He, B.; Xu, YB. Analysis of transcriptome sequencing of sciatic nerves in sprague-dawley rats of different ages. Neural Regen Res, 2018, 13(12), 2182-2190. doi: 10.4103/1673-5374.241469 PMID: 30323151 PMCID: PMC6199923
  10. Melcangi, R.C.; Azcoitia, I.; Ballabio, M.; Cavarretta, I.; Gonzalez, L.C.; Leonelli, E.; Magnaghi, V.; Veiga, S.; Garcia-Segura, L.M. Neuroactive steroids influence peripheral myelination: A promising opportunity for preventing or treating age-dependent dysfunctions of peripheral nerves. Prog. Neurobiol., 2003, 71(1), 57-66. doi: 10.1016/j.pneurobio.2003.09.003 PMID: 14611868
  11. Wang, Y.J.; Zhou, C.J.; Shi, Q.; Smith, N.; Li, T.F. Aging delays the regeneration process following sciatic nerve injury in rats. J. Neurotrauma, 2007, 24(5), 885-894. doi: 10.1089/neu.2006.0156 PMID: 17518542
  12. Fuertes-Alvarez, S.; Izeta, A. Terminal schwann cell aging: Implications for age-associated neuromuscular dysfunction. Aging Dis., 2021, 12(2), 494-514. doi: 10.14336/AD.2020.0708 PMID: 33815879
  13. Painter, M.W. Aging Schwann cells: Mechanisms, implications, future directions. Curr. Opin. Neurobiol., 2017, 47, 203-208. doi: 10.1016/j.conb.2017.10.022 PMID: 29161640
  14. Saio, S.; Konishi, K.; Hohjoh, H.; Tamura, Y.; Masutani, T.; Iddamalgoda, A.; Ichihashi, M.; Hasegawa, H.; Mizutani, K. Extracellular environment-controlled angiogenesis, and potential application for peripheral nerve regeneration. Int. J. Mol. Sci., 2021, 22(20), 11169. doi: 10.3390/ijms222011169 PMID: 34681829
  15. Jessen, K.R.; Mirsky, R.; Lloyd, A.C. Schwann cells: Development and role in nerve repair. Cold Spring Harb. Perspect. Biol., 2015, 7(7), a020487. doi: 10.1101/cshperspect.a020487 PMID: 25957303
  16. Siqueira Mietto, B.; Kroner, A.; Girolami, E.I.; Santos-Nogueira, E.; Zhang, J.; David, S. Role of IL-10 in resolution of inflammation and functional recovery after peripheral nerve injury. J. Neurosci., 2015, 35(50), 16431-16442. doi: 10.1523/JNEUROSCI.2119-15.2015 PMID: 26674868
  17. Arthur-Farraj, P.J.; Latouche, M.; Wilton, D.K.; Quintes, S.; Chabrol, E.; Banerjee, A.; Woodhoo, A.; Jenkins, B.; Rahman, M.; Turmaine, M.; Wicher, G.K.; Mitter, R.; Greensmith, L.; Behrens, A.; Raivich, G.; Mirsky, R.; Jessen, K.R. c-Jun reprograms Schwann cells of injured nerves to generate a repair cell essential for regeneration. Neuron, 2012, 75(4), 633-647. doi: 10.1016/j.neuron.2012.06.021 PMID: 22920255
  18. Fontana, X.; Hristova, M.; Da Costa, C.; Patodia, S.; Thei, L.; Makwana, M.; Spencer-Dene, B.; Latouche, M.; Mirsky, R.; Jessen, K.R.; Klein, R.; Raivich, G.; Behrens, A. c-Jun in Schwann cells promotes axonal regeneration and motoneuron survival via paracrine signaling. J. Cell Biol., 2012, 198(1), 127-141. doi: 10.1083/jcb.201205025 PMID: 22753894
  19. Painter, M.W.; Brosius Lutz, A.; Cheng, Y.C.; Latremoliere, A.; Duong, K.; Miller, C.M.; Posada, S.; Cobos, E.J.; Zhang, A.X.; Wagers, A.J.; Havton, L.A.; Barres, B.; Omura, T.; Woolf, C.J. Diminished Schwann cell repair responses underlie age-associated impaired axonal regeneration. Neuron, 2014, 83(2), 331-343. doi: 10.1016/j.neuron.2014.06.016 PMID: 25033179
  20. Liu, M.; Li, P.; Jia, Y.; Cui, Q.; Zhang, K.; Jiang, J. Role of non-coding RNAs in axon regeneration after peripheral nerve injury. Int. J. Biol. Sci., 2022, 18(8), 3435-3446. doi: 10.7150/ijbs.70290 PMID: 35637962
  21. Hashemi, M.; Nadafzadeh, N.; Imani, M.H.; Rajabi, R.; Ziaolhagh, S.; Bayanzadeh, S.D.; Norouzi, R.; Rafiei, R.; Koohpar, Z.K.; Raei, B.; Zandieh, M.A.; Salimimoghadam, S.; Entezari, M.; Taheriazam, A.; Alexiou, A.; Papadakis, M.; Tan, S.C. Targeting and regulation of autophagy in hepatocellular carcinoma: Revisiting the molecular interactions and mechanisms for new therapy approaches. Cell Commun. Signal., 2023, 21(1), 32. doi: 10.1186/s12964-023-01053-z PMID: 36759819
  22. Moghbeli, M. Molecular interactions of miR-338 during tumor progression and metastasis. Cell. Mol. Biol. Lett., 2021, 26(1), 13. doi: 10.1186/s11658-021-00257-w PMID: 33827418
  23. Zhang, Y.; Zhu, Z.; Liu, X.; Xu, S.; Zhang, Y.; Xu, Y.; He, B. Integrated analysis of long noncoding RNAs and mRNA expression profiles reveals the potential role of lncRNAs in early stage of post-peripheral nerve injury in Sprague-Dawley rats. Aging , 2021, 13(10), 13909-13925. doi: 10.18632/aging.202989 PMID: 33971626
  24. Zhang, J.; Liu, Y.; Lu, L. Emerging role of MicroRNAs in peripheral nerve system. Life Sci., 2018, 207, 227-233. doi: 10.1016/j.lfs.2018.06.011 PMID: 29894714
  25. Zhou, S.; Ding, F.; Gu, X. Non-coding RNAs as emerging regulators of neural injury responses and regeneration. Neurosci. Bull., 2016, 32(3), 253-264. doi: 10.1007/s12264-016-0028-7 PMID: 27037691
  26. Du, S.; Wu, S.; Feng, X.; Wang, B.; Xia, S.; Liang, L.; Zhang, L.; Govindarajalu, G.; Bunk, A.; Kadakia, F.; Mao, Q.; Guo, X.; Zhao, H.; Berkman, T.; Liu, T.; Li, H.; Stillman, J.; Bekker, A.; Davidson, S.; Tao, Y.X. A nerve injury-specific long noncoding RNA promotes neuropathic pain by increasing Ccl2 expression. J. Clin. Invest., 2022, 132(13), e153563. doi: 10.1172/JCI153563 PMID: 35775484
  27. Wang, D.; Zheng, T.; Ge, X.; Xu, J.; Feng, L.; Jiang, C.; Tao, J.; Chen, Y.; Liu, X.; Yu, B.; Zhou, S.; Zhu, J. Unfolded protein response-induced expression of long noncoding RNA Ngrl1 supports peripheral axon regeneration by activating the PI3K-Akt pathway. Exp. Neurol., 2022, 352, 114025. doi: 10.1016/j.expneurol.2022.114025 PMID: 35227685
  28. Yin, G.; Lin, Y.; Wang, P.; Zhou, J.; Lin, H. Upregulated lncARAT in Schwann cells promotes axonal regeneration by recruiting and activating proregenerative macrophages. Mol. Med., 2022, 28(1), 76. doi: 10.1186/s10020-022-00501-9 PMID: 35768768
  29. Cantuti-Castelvetri, L.; Fitzner, D.; Bosch-Queralt, M.; Weil, M.T.; Su, M.; Sen, P.; Ruhwedel, T.; Mitkovski, M.; Trendelenburg, G.; Lütjohann, D.; Möbius, W.; Simons, M. Defective cholesterol clearance limits remyelination in the aged central nervous system. Science, 2018, 359(6376), 684-688. doi: 10.1126/science.aan4183 PMID: 29301957
  30. Faizy, T.D.; Thaler, C.; Broocks, G.; Flottmann, F.; Leischner, H.; Kniep, H.; Nawabi, J.; Schön, G.; Stellmann, J.P.; Kemmling, A.; Reddy, R.; Heit, J.J.; Fiehler, J.; Kumar, D.; Hanning, U. The myelin water fraction serves as a marker for age-related myelin alterations in the cerebral white matter - A multiparametric MRI aging study. Front. Neurosci., 2020, 14, 136. doi: 10.3389/fnins.2020.00136 PMID: 32153358
  31. Esquisatto, M.A.M.; de Aro, A.A.; Fêo, H.B.; Gomes, L. Changes in the connective tissue sheath of Wistar rat nerve with aging. Ann. Anat., 2014, 196(6), 441-448. doi: 10.1016/j.aanat.2014.08.005 PMID: 25282682
  32. Clements, M.P.; Byrne, E.; Camarillo Guerrero, L.F.; Cattin, A.L.; Zakka, L.; Ashraf, A.; Burden, J.J.; Khadayate, S.; Lloyd, A.C.; Marguerat, S.; Parrinello, S. The wound microenvironment reprograms schwann cells to invasive mesenchymal-like cells to drive peripheral nerve regeneration. Neuron, 2017, 96(1), 98-114.e7. doi: 10.1016/j.neuron.2017.09.008 PMID: 28957681
  33. Luo, Y.; Pan, H.; Jiang, J.; Zhao, C.; Zhang, J.; Chen, P.; Lin, X.; Fan, S. Desktop-stereolithography 3D printing of a polyporous extracellular matrix bioink for bone defect regeneration. Front. Bioeng. Biotechnol., 2020, 8, 589094. doi: 10.3389/fbioe.2020.589094 PMID: 33240866
  34. Kornfeld, T.; Vogt, P.M.; Radtke, C. Nerve grafting for peripheral nerve injuries with extended defect sizes. Wien. Med. Wochenschr., 2019, 169(9-10), 240-251. doi: 10.1007/s10354-018-0675-6 PMID: 30547373
  35. Li, X.; Zhang, X.; Hao, M.; Wang, D.; Jiang, Z.; Sun, L.; Gao, Y.; Jin, Y.; Lei, P.; Zhuo, Y. The application of collagen in the repair of peripheral nerve defect. Front. Bioeng. Biotechnol., 2022, 10, 973301. doi: 10.3389/fbioe.2022.973301 PMID: 36213073
  36. Hopf, A.; Schaefer, D.J.; Kalbermatten, D.F.; Guzman, R.; Madduri, S. Schwann cell-like cells: Origin and usability for repair and regeneration of the peripheral and central nervous system. Cells, 2020, 9(9), 1990. doi: 10.3390/cells9091990 PMID: 32872454
  37. Widgerow, A.D.; Salibian, A.A.; Lalezari, S.; Evans, G.R.D. Neuromodulatory nerve regeneration: Adipose tissue-derived stem cells and neurotrophic mediation in peripheral nerve regeneration. J. Neurosci. Res., 2013, 91(12), 1517-1524. doi: 10.1002/jnr.23284 PMID: 24105674
  38. Gregory, H.; Phillips, J.B. Materials for peripheral nerve repair constructs: Natural proteins or synthetic polymers? Neurochem. Int., 2021, 143, 104953. doi: 10.1016/j.neuint.2020.104953 PMID: 33388359
  39. Fujimaki, H; Uchida, K; Inoue, G; Miyagi, M; Nemoto, N; Saku, T; Isobe, Y; Inage, K; Matsushita, O; Yagishita, S; Sato, J; Takano, S; Sakuma, Y; Ohtori, S; Takahashi, K; Takaso, M Oriented collagen tubes combined with basic fibroblast growth factor promote peripheral nerve regeneration in a 15mm sciatic nerve defect rat model. J. Biomed. Mater. Res. A, 2017, 105(1), 8-14. doi: 10.1002/jbm.a.35866
  40. Koopmans, G.; Hasse, B.; Sinis, N. Chapter 19: The role of collagen in peripheral nerve repair. Int. Rev. Neurobiol., 2009, 87, 363-379. doi: 10.1016/S0074-7742(09)87019-0 PMID: 19682648
  41. Tian, W.M.; Hou, S.P.; Ma, J.; Zhang, C.L.; Xu, Q.Y.; Lee, I.S.; Li, H.D.; Spector, M.; Cui, F.Z. Hyaluronic acid-poly-D-lysine-based three-dimensional hydrogel for traumatic brain injury. Tissue Eng., 2005, 11(3-4), 513-525. doi: 10.1089/ten.2005.11.513 PMID: 15869430
  42. Song, S.; Wang, X.; Wang, T.; Yu, Q.; Hou, Z.; Zhu, Z.; Li, R. Additive manufacturing of nerve guidance conduits for regeneration of injured peripheral nerves. Front. Bioeng. Biotechnol., 2020, 8, 590596. doi: 10.3389/fbioe.2020.590596 PMID: 33102468
  43. Peng, Y.; Li, K.Y.; Chen, Y.F.; Li, X.J.; Zhu, S.; Zhang, Z.Y.; Wang, X.; Duan, L.N.; Luo, Z.J.; Du, J.J.; Wang, J.C. Beagle sciatic nerve regeneration across a 30 mm defect bridged by chitosan/PGA artificial nerve grafts. Injury, 2018, 49(8), 1477-1484. doi: 10.1016/j.injury.2018.03.023 PMID: 29921534
  44. Cattin, A.L.; Burden, J.J.; Van Emmenis, L.; Mackenzie, F.E.; Hoving, J.J.A.; Garcia Calavia, N.; Guo, Y.; McLaughlin, M.; Rosenberg, L.H.; Quereda, V.; Jamecna, D.; Napoli, I.; Parrinello, S.; Enver, T.; Ruhrberg, C.; Lloyd, A.C. Macrophage-induced blood vessels guide schwann cell-mediated regeneration of peripheral nerves. Cell, 2015, 162(5), 1127-1139. doi: 10.1016/j.cell.2015.07.021 PMID: 26279190
  45. Malheiro, A.; Seijas-Gamardo, A.; Harichandan, A.; Mota, C.; Wieringa, P.; Moroni, L. Development of an in vitro biomimetic peripheral neurovascular platform. ACS Appl. Mater. Interfaces, 2022, 14(28), 31567-31585. doi: 10.1021/acsami.2c03861 PMID: 35815638
  46. He, B.; Pang, V.; Liu, X.; Xu, S.; Zhang, Y.; Djuanda, D.; Wu, G.; Xu, Y.; Zhu, Z. Interactions among nerve regeneration, angiogenesis, and the immune response immediately after sciatic nerve crush injury in sprague-dawley rats. Front. Cell. Neurosci., 2021, 15, 717209. doi: 10.3389/fncel.2021.717209 PMID: 34671243
  47. Gu, X.; Ding, F.; Williams, D.F. Neural tissue engineering options for peripheral nerve regeneration. Biomaterials, 2014, 35(24), 6143-6156. doi: 10.1016/j.biomaterials.2014.04.064 PMID: 24818883
  48. Wariyar, S.S.; Brown, A.D.; Tian, T.; Pottorf, T.S.; Ward, P.J. Angiogenesis is critical for the exercise-mediated enhancement of axon regeneration following peripheral nerve injury. Exp. Neurol., 2022, 353, 114029. doi: 10.1016/j.expneurol.2022.114029 PMID: 35259353
  49. Pola, R.; Aprahamian, T.R.; Bosch-Marcé, M.; Curry, C.; Gaetani, E.; Flex, A.; Smith, R.C.; Isner, J.M.; Losordo, D.W. Age-dependent VEGF expression and intraneural neovascularization during regeneration of peripheral nerves. Neurobiol. Aging, 2004, 25(10), 1361-1368. doi: 10.1016/j.neurobiolaging.2004.02.028 PMID: 15465634
  50. Wang, Y.; Li, Y.; Huang, Z.; Yang, B.; Mu, N.; Yang, Z.; Deng, M.; Liao, X.; Yin, G.; Nie, Y.; Chen, T.; Ma, H. Gene delivery of chitosan-graft-polyethyleneimine vectors loaded on scaffolds for nerve regeneration. Carbohydr. Polym., 2022, 290, 119499. doi: 10.1016/j.carbpol.2022.119499 PMID: 35550777
  51. Mehta, K.; Behl, T.; Kumar, A.; Uddin, M.S.; Zengin, G.; Arora, S. Deciphering the neuroprotective role of glucagon-like peptide-1 agonists in diabetic neuropathy: Current perspective and future directions. Curr. Protein Pept. Sci., 2021, 22(1), 4-18. doi: 10.2174/1389203721999201208195901 PMID: 33292149
  52. Sun, J.; Li, N.; Xu, M.; Li, L.; Chen, J.L.; Chen, Y.; Xu, J.G.; Wang, T.H. Mechanism of gene network in the treatment of intracerebral hemorrhage by natural plant drugs in Lutong granules. PLoS One, 2022, 17(11), e0274639. doi: 10.1371/journal.pone.0274639 PMID: 36441671
  53. Chikkannaiah, M.; Reyes, I. New diagnostic and therapeutic modalities in neuromuscular disorders in children. Curr. Probl. Pediatr. Adolesc. Health Care, 2021, 51(7), 101033. doi: 10.1016/j.cppeds.2021.101033 PMID: 34281812
  54. Stratton, J.A.; Eaton, S.; Rosin, N.L.; Jawad, S.; Holmes, A.; Yoon, G.; Midha, R.; Biernaskie, J. Macrophages and associated ligands in the aged injured nerve: A defective dynamic that contributes to reduced axonal regrowth. Front. Aging Neurosci., 2020, 12, 174. doi: 10.3389/fnagi.2020.00174 PMID: 32595489
  55. Scheib, J.L.; Höke, A. An attenuated immune response by Schwann cells and macrophages inhibits nerve regeneration in aged rats. Neurobiol. Aging, 2016, 45, 1-9. doi: 10.1016/j.neurobiolaging.2016.05.004 PMID: 27459920

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