Skip to main content

Advertisement

SpringerLink
Log in

Swimming and L-arginine loaded chitosan nanoparticles ameliorates aging‐induced neuron atrophy, autophagy marker LC3, GABA and BDNF-TrkB pathway in the spinal cord of rats

  • Neuroscience
  • Published:
Pflügers Archiv - European Journal of Physiology Aims and scope Submit manuscript

Abstract

Aging is associated with muscle atrophy, and erosion and destruction of neuronal pathways in the spinal cord. The study aim was to assess the effect of swimming training (Sw) and L-arginine loaded chitosan nanoparticles (LA-CNPs) on the sensory and motor neuron population, autophagy marker LC3, total oxidant status/total antioxidant capacity, behavioural test, GABA and BDNF-TrkB pathway in the spinal cord of aging rats. The rats were randomized to five groups: young (8-weeks) control (n = 7), old control (n = 7), old Sw (n = 7), old LA-CNPs (n = 7) and old Sw + LA-CNPs (n = 7). Groups under LA-CNPs supplementation received 500 mg/kg/day. Sw groups performed a swimming exercise programme 5 days per week for 6 weeks. Upon the completion of the interventions the rats were euthanized and the spinal cord was fixed and frozen for histological assessment, IHC, and gene expression analysis. The old group had more atrophy in the spinal cord with higher changes in LC3 as an indicator of autophagy in the spinal cord compared to the young group (p < 0.0001). The old Sw + LA-CNPs group increased (improved) spinal cord GABA (p = 0.0187), BDNF (p = 0.0003), TrkB (p < 0.0001) gene expression, decreased autophagy marker LC3 protein (p < 0.0001), nerve atrophy and jumping/licking latency (p < 0.0001), improved sciatic functional index score and total oxidant status/total antioxidant capacity compared to the old group (p < 0.0001). In conclusion, swimming and LA-CNPs seems to ameliorate aging‐induced neuron atrophy, autophagy marker LC3, oxidant-antioxidant status, functional restoration, GABA and BDNF-TrkB pathway in the spinal cord of aging rats. Our study provides experimental evidence for a possible positive role of swimming and L-arginine loaded chitosan nanoparticles to decrease complications of aging.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

References

  1. Abbadie C, Besson J-M (1993) Effects of morphine and naloxone on basal and evoked Fos-like immunoreactivity in lumbar spinal cord neurons of arthritic rats. Pain 52:29–39

    Article  CAS  PubMed  Google Scholar 

  2. Ashrafi G, Schlehe JS, LaVoie MJ, Schwarz TL (2014) Mitophagy of damaged mitochondria occurs locally in distal neuronal axons and requires PINK1 and Parkin. J Cell Biol 206:655–670

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Belviranlı M, Okudan N (2018) Exercise training protects against aging-induced cognitive dysfunction via activation of the hippocampal PGC-1α/FNDC5/BDNF pathway. NeuroMol Med 20:386–400

    Article  Google Scholar 

  4. Brewer S, Desneves K, Pearce L, Mills K, Dunn L, Brown D, Crowe T (2010) Effect of an arginine-containing nutritional supplement on pressure ulcer healing in community spinal patients. J Wound Care 19:311–316

    Article  CAS  PubMed  Google Scholar 

  5. Buchman AS, Leurgans SE, VanderHorst VG, Nag S, Schneider JA, Bennett DA (2019) Spinal motor neurons and motor function in older adults. J Neurol 266:174–182

    Article  PubMed  Google Scholar 

  6. Castelli V, Benedetti E, Antonosante A, Catanesi M, Pitari G, Ippoliti R, Cimini A, d’Angelo M (2019) Neuronal cells rearrangement during aging and neurodegenerative disease: metabolism, oxidative stress and organelles dynamic. Front Mol Neurosci 12:132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Chen A, Xiong L-J, Tong Y, Mao M (2013) Neuroprotective effect of brain-derived neurotrophic factor mediated by autophagy through the PI3K/Akt/mTOR pathway. Mol Med Rep 8:1011–1016

    Article  CAS  PubMed  Google Scholar 

  8. Chen B, Bohnert D, Borgens RB, Cho Y (2013) Pushing the science forward: chitosan nanoparticles and functional repair of CNS tissue after spinal cord injury. J Biol Eng 7:1–9

    Article  CAS  Google Scholar 

  9. Cho Y, Shi R, Borgens RB (2010) Chitosan produces potent neuroprotection and physiological recovery following traumatic spinal cord injury. J Exp Biol 213:1513–1520

    Article  CAS  PubMed  Google Scholar 

  10. Cruz-Sanchez F, Moral A, Tolosa E, De Belleroche J, Rossi M (1998) Evaluation of neuronal loss, astrocytosis and abnormalities of cytoskeletal components of large motor neurons in the human anterior horn in aging. J Neural Transm 105:689–701

    Article  CAS  PubMed  Google Scholar 

  11. Darband SG, Sadighparvar S, Yousefi B, Kaviani M, Mobaraki K, Majidinia M (2020) Combination of exercise training and L-arginine reverses aging process through suppression of oxidative stress, inflammation, and apoptosis in the rat heart. Pflügers Archiv-Eur J Physiol 472:169–178

    Article  CAS  Google Scholar 

  12. de Medinaceli L, Freed WJ, Wyatt RJ (1982) An index of the functional condition of rat sciatic nerve based on measurements made from walking tracks. Exp Neurol 77:634–643

    Article  PubMed  Google Scholar 

  13. Dong D, Lei T, Song M, Ma L, Zhao H (2020) The antidepressant effects of l-arginine on chronic mild stress-induced depression by augmenting the expression of brain-derived neurotrophic factor in rats. Brain Res Bull 158:128–134

    Article  CAS  PubMed  Google Scholar 

  14. Ducaji EC, Pareja-Cajiao M, Gransee HM, Sieck GC, Mantilla CB (2020) BDNF/TrkB Signaling Increases Autophagy Flux in Cervical Spinal Cord. FASEB J 34:1–1

    Article  Google Scholar 

  15. Eddy NB, Leimbach D (1953) Synthetic analgesics. II. Dithienylbutenyl-and dithienylbutylamines. J Pharmacol Exp Ther 107:385–393

    CAS  PubMed  Google Scholar 

  16. Erens C, Van Broeckhoven J, Bronckaers A, Lemmens S, Hendrix S (2022) The dark side of an essential amino acid-L-arginine in spinal cord injury. J Neurotrauma

  17. Fantozzi S, Cortesi M, Giovanardi A, Borra D, Di Michele R, Gatta G (2020) Effect of walking speed during gait in water of healthy elderly. Gait Posture 82:6–13

    Article  PubMed  Google Scholar 

  18. Farzad B, Rajabi H, Gharakhanlou R, Allison DJ, Hayat P, Jameie SB (2018) Swimming training attenuates allodynia and hyperalgesia induced by peripheral nerve injury in an adult male rat neuropathic model: effects on irisin and GAD65. Pain Med 19:2236–2245

    Article  PubMed  Google Scholar 

  19. Frake RA, Ricketts T, Menzies FM, Rubinsztein DC (2015) Autophagy and neurodegeneration. J Clin Investig 125:65–74

    Article  PubMed  PubMed Central  Google Scholar 

  20. Freiberger E, Sieber CC, Kob R (2020) Mobility in older community-dwelling persons: a narrative review. Front Physiol 11:881

    Article  PubMed  PubMed Central  Google Scholar 

  21. Fukuie M, Yamabe T, Nomura Y, Hashitomi T, Maeda S, Sugawara J (2019) The effect of head-out aquatic exercise on arterial stiffness in middle-aged and elderly people. Pulse 7:51–59

    Article  Google Scholar 

  22. Gad MZ (2010) Anti-aging effects of L-arginine. J Adv Res 1:169–177

    Article  Google Scholar 

  23. Geertsen SS, Willerslev-Olsen M, Lorentzen J, Nielsen JB (2017) Development and aging of human spinal cord circuitries. J Neurophysiol 118:1133–1140

    Article  PubMed  PubMed Central  Google Scholar 

  24. Gómez-Pinilla F, Ying Z, Opazo P, Roy R, Edgerton V (2001) Differential regulation by exercise of BDNF and NT-3 in rat spinal cord and skeletal muscle. Eur J Neurosci 13:1078–1084

    Article  PubMed  Google Scholar 

  25. Gonzalez Porras MA, Sieck GC, Mantilla CB (2018) Impaired autophagy in motor neurons: a final common mechanism of injury and death. Physiology 33:211–224

    Article  PubMed  PubMed Central  Google Scholar 

  26. Gwak YS, Tan HY, Nam TS, Paik KS, Hulsebosch CE, Leem JW (2006) Activation of spinal GABA receptors attenuates chronic central neuropathic pain after spinal cord injury. J Neurotrauma 23:1111–1124

    Article  PubMed  Google Scholar 

  27. Inoue H, Tsukita K, Iwasato T, Suzuki Y, Tomioka M, Tateno M, Nagao M, Kawata A, Saido TC, Miura M (2003) The crucial role of caspase-9 in the disease progression of a transgenic ALS mouse model. EMBO J 22:6665–6674

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Iwabe S, Moreno-Mendoza NA, Trigo-Tavera F, Crowder C, García-Sánchez GA (2007) Retrograde axonal transport obstruction of brain-derived neurotrophic factor (BDNF) and its TrkB receptor in the retina and optic nerve of American Cocker Spaniel dogs with spontaneous glaucoma. Vet Ophthalmol 10:12–19

    Article  PubMed  Google Scholar 

  29. Jia S, Lu Z, Gao Z, An J, Wu X, Li X, Dai X, Zheng Q, Sun Y (2016) Chitosan oligosaccharides alleviate cognitive deficits in an amyloid-β1–42-induced rat model of Alzheimer’s disease. Int J Biol Macromol 83:416–425

    Article  CAS  PubMed  Google Scholar 

  30. Koo J-H, Jang Y-C, Hwang D-J, Um H-S, Lee N-H, Jung J-H, Cho J-Y (2017) Treadmill exercise produces neuroprotective effects in a murine model of Parkinson’s disease by regulating the TLR2/MyD88/NF-κB signaling pathway. Neuroscience 356:102–113

    Article  CAS  PubMed  Google Scholar 

  31. Kruman I, Bruce-Keller AJ, Bredesen D, Waeg G, Mattson MP (1997) Evidence that 4-hydroxynonenal mediates oxidative stress-induced neuronal apoptosis. J Neurosci 17:5089–5100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Kullberg S, Ramirez-Leon V, Johnson H, Ulfhake B (1998) Decreased axosomatic input to motoneurons and astrogliosis in the spinal cord of aged rats. J Gerontol A Biol Sci Med Sci 53:B369–B379

    Article  CAS  PubMed  Google Scholar 

  33. Lee J, Ryu H, Kowall NW (2009) Motor neuronal protection by L-arginine prolongs survival of mutant SOD1 (G93A) ALS mice. Biochem Biophys Res Commun 384:524–529

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Lee JW, Furmanski O, Castellanos DA, Daniels LA, Hama AT, Sagen J (2008) Prolonged nociceptive responses to hind paw formalin injection in rats with a spinal cord injury. Neurosci Lett 439:212–215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Li D-J, Li Y-H, Yuan H-B, Qu L-F, Wang P (2017) The novel exercise-induced hormone irisin protects against neuronal injury via activation of the Akt and ERK1/2 signaling pathways and contributes to the neuroprotection of physical exercise in cerebral ischemia. Metabolism 68:31–42

    Article  CAS  PubMed  Google Scholar 

  36. Li X, Wu Q, Xie C, Wang C, Wang Q, Dong C, Fang L, Ding J, Wang T (2019) Blocking of BDNF-TrkB signaling inhibits the promotion effect of neurological function recovery after treadmill training in rats with spinal cord injury. Spinal Cord 57:65–74

    Article  PubMed  Google Scholar 

  37. Liang M, Wang Z, Li H, Cai L, Pan J, He H, Wu Q, Tang Y, Ma J, Yang L (2018) l-Arginine induces antioxidant response to prevent oxidative stress via stimulation of glutathione synthesis and activation of Nrf2 pathway. Food Chem Toxicol 115:315–328

    Article  CAS  PubMed  Google Scholar 

  38. López-Otín C, Blasco MA, Partridge L, Serrano M, Kroemer G (2013) The hallmarks of aging. Cell 153:1194–1217

    Article  PubMed  PubMed Central  Google Scholar 

  39. Löw P (2011) The role of ubiquitin–proteasome system in ageing. Gen Comp Endocrinol 172:39–43

    Article  PubMed  Google Scholar 

  40. Luo L, Salunga RC, Guo H, Bittner A, Joy K, Galindo JE, Xiao H, Rogers KE, Wan JS, Jackson MR (1999) Gene expression profiles of laser-captured adjacent neuronal subtypes. Nat Med 5:117–122

    Article  CAS  PubMed  Google Scholar 

  41. Malysz T, Ilha J, Nascimento PSd, Angelis KD, Schaan BDA, Achaval M (2010) Beneficial effects of treadmill training in experimental diabetic nerve regeneration. Clinics 65:1329–1337

    Article  PubMed  PubMed Central  Google Scholar 

  42. Mantilla CB, Gransee HM, Zhan W-Z, Sieck GC (2013) Motoneuron BDNF/TrkB signaling enhances functional recovery after cervical spinal cord injury. Exp Neurol 247:101–109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Mirdar S, Kazemzadeh Y, Arabzadeh E, Shirvani H, Hamidian G (2019) The effects of tapering with and without ethanolic extract of Nigella sativa on Hypoxia Inducible Factor-1α and exercise-induced bronchial changes. J Mil Med 21:131–141

    Google Scholar 

  44. Morimoto N, Nagai M, Ohta Y, Miyazaki K, Kurata T, Morimoto M, Murakami T, Takehisa Y, Ikeda Y, Kamiya T (2007) Increased autophagy in transgenic mice with a G93A mutant SOD1 gene. Brain Res 1167:112–117

    Article  CAS  PubMed  Google Scholar 

  45. Nagaratnam N, Nagaratnam K, Cheuk G (2016) Neurological disorders and related problems in the elderly. In: Diseases in the Elderly. Springer, Cham. https://doi.org/10.1007/978-3-319-25787-7_7

  46. Nikoletopoulou V, Sidiropoulou K, Kallergi E, Dalezios Y, Tavernarakis N (2017) Modulation of autophagy by BDNF underlies synaptic plasticity. Cell Metab 26(230–242):e235

    Google Scholar 

  47. Oppenheim RW (1997) Related mechanisms of action of growth factors and antioxidants in apoptosis: an overview. Adv Neurol 72:69–78

    CAS  PubMed  Google Scholar 

  48. Pareja-Cajiao M, Gransee HM, Stowe JM, Rana S, Sieck GC, Mantilla CB (2021) Age-related impairment of autophagy in cervical motor neurons. Exp Gerontol 144:111193

    Article  CAS  PubMed  Google Scholar 

  49. Perluigi M, Di Domenico F, Butterfield DA (2015) mTOR signaling in aging and neurodegeneration: At the crossroad between metabolism dysfunction and impairment of autophagy. Neurobiol Dis 84:39–49

    Article  CAS  PubMed  Google Scholar 

  50. Philippidou P, Valdez G, Akmentin W, Bowers WJ, Federoff HJ, Halegoua S (2011) Trk retrograde signaling requires persistent, Pincher-directed endosomes. Proc Natl Acad Sci 108:852–857

    Article  CAS  PubMed  Google Scholar 

  51. Powers ET, Morimoto RI, Dillin A, Kelly JW, Balch WE (2009) Biological and chemical approaches to diseases of proteostasis deficiency. Annu Rev Biochem 78:959–991

    Article  CAS  PubMed  Google Scholar 

  52. Qiu L-L, Pan W, Luo D, Zhang G-F, Zhou Z-Q, Sun X-Y, Yang J-J, Ji M-H (2020) Dysregulation of BDNF/TrkB signaling mediated by NMDAR/Ca2+/calpain might contribute to postoperative cognitive dysfunction in aging mice. J Neuroinflammation 17:1–15

    Article  Google Scholar 

  53. Reichardt LF (2006) Neurotrophin-regulated signalling pathways. Philos Trans R Soc B Biol Sci 361:1545–1564

    Article  CAS  Google Scholar 

  54. Reynolds AJ, Bartlett SE, Hendry IA (2000) Molecular mechanisms regulating the retrograde axonal transport of neurotrophins. Brain Res Rev 33:169–178

    Article  CAS  PubMed  Google Scholar 

  55. Rodemer W, Selzer ME (2019) Role of axon resealing in retrograde neuronal death and regeneration after spinal cord injury. Neural Regen Res 14:399

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Romaus-Sanjurjo D, Ledo-García R, Fernández-López B, Hanslik K, Morgan JR, Barreiro-Iglesias A, Rodicio MC (2018) GABA promotes survival and axonal regeneration in identifiable descending neurons after spinal cord injury in larval lampreys. Cell Death Dis 9:1–15

    Article  CAS  Google Scholar 

  57. Romaus-Sanjurjo D, Rodicio MC, Barreiro-Iglesias A (2019) Gamma-aminobutyric acid (GABA) promotes recovery from spinal cord injury in lampreys: role of GABA receptors and perspective on the translation to mammals. Neural Regen Res 14:1695

    Article  PubMed  PubMed Central  Google Scholar 

  58. Ruegsegger C, Saxena S (2016) Proteostasis impairment in ALS. Brain Res 1648:571–579

    Article  CAS  PubMed  Google Scholar 

  59. Sadri S, Sharifi G, Dehkordi KJ (2020) Effects of high intensity interval training (up & downward running) with BCAA/nano chitosan on Foxo3 and SMAD soleus muscles of aging rat. Life Sci 252:117641

    Article  CAS  PubMed  Google Scholar 

  60. Sharebiani H, Fazeli B, Maniscalco R, Ligi D, Mannello F (2020) The imbalance among oxidative biomarkers and antioxidant defense systems in thromboangiitis obliterans (Winiwarter-Buerger Disease). J Clin Med 9:1036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Shetty AK, Bates A (2016) Potential of GABA-ergic cell therapy for schizophrenia, neuropathic pain, and Alzheimer׳ s and Parkinson׳ s diseases. Brain Res 1638:74–87

    Article  CAS  PubMed  Google Scholar 

  62. Shirvani H, Rahmati-Ahmadabad S, Broom DR, Mirnejad R (2019) Eccentric resistance training and β-hydroxy-β-methylbutyrate free acid affects muscle PGC-1α expression and serum irisin, nesfatin-1 and resistin in rats. J Exp Biol 222:jeb198424

  63. Shobeiri P, Karimi A, Momtazmanesh S, Teixeira AL, Teunissen CE, van Wegen EE, Hirsch MA, Yekaninejad MS, Rezaei N (2022) Exercise-induced increase in blood-based brain-derived neurotrophic factor (BDNF) in people with multiple sclerosis: A systematic review and meta-analysis of exercise intervention trials. PLoS One 17:e0264557

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Silveira EMSd, Kroth A, Santos MdCQ, Silva TCBd, Silveira D, Riffel APK, Scheid T, Trapp M, Partata WA (2019) Age-related changes and effects of regular low-intensity exercise on gait, balance, and oxidative biomarkers in the spinal cord of Wistar rats. Braz J Med Biol Res 52(7):1–13

  65. Simmonite M, Carp J, Foerster BR, Ossher L, Petrou M, Weissman DH, Polk TA (2019) Age-related declines in occipital GABA are associated with reduced fluid processing ability. Acad Radiol 26:1053–1061

    Article  PubMed  Google Scholar 

  66. Smart TG, Stephenson FA (2019) A half century of γ-aminobutyric acid. Brain Neurosci Adv 3:2398212819858249

    Article  PubMed  PubMed Central  Google Scholar 

  67. Smith ED, Prieto GA, Tong L, Sears-Kraxberger I, Rice JD, Steward O, Cotman CW (2014) Rapamycin and interleukin-1β impair brain-derived neurotrophic factor-dependent neuron survival by modulating autophagy. J Biol Chem 289:20615–20629

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Song X-Y, Li F, Zhang F-H, Zhong J-H, Zhou X-F (2008) Peripherally-derived BDNF promotes regeneration of ascending sensory neurons after spinal cord injury. PLoS One 3:e1707

    Article  PubMed  PubMed Central  Google Scholar 

  69. Song X, Liu B, Cui L, Zhou B, Liu W, Xu F, Hayashi T, Hattori S, Ushiki-Kaku Y, Tashiro S-i (2017) Silibinin ameliorates anxiety/depression-like behaviors in amyloid β-treated rats by upregulating BDNF/TrkB pathway and attenuating autophagy in hippocampus. Physiol Behav 179:487–493

    Article  CAS  PubMed  Google Scholar 

  70. Taniguchi H (2014) Genetic dissection of GABAergic neural circuits in mouse neocortex. Front Cell Neurosci 8:8

    Article  PubMed  PubMed Central  Google Scholar 

  71. Terao S-i, Sobue G, Hashizume Y, Li M, Inagaki T, Mitsuma T (1996) Age-related changes in human spinal ventral horn cells with special reference to the loss of small neurons in the intermediate zone: a quantitative analysis. Acta Neuropathol 92:109–114

    Article  CAS  PubMed  Google Scholar 

  72. Tu W-Z, Li S-S, Jiang X, Qian X-R, Yang G-H, Gu P-P, Lu B, Jiang S-H (2018) Effect of electro-acupuncture on the BDNF-TrkB pathway in the spinal cord of CCI rats. Int J Mol Med 41:3307–3315

    CAS  PubMed  PubMed Central  Google Scholar 

  73. Tuncer MC, Hatipoglu ES, Ozturk H, Kervancioglu P, Buyukbayram H (2005) The effects of L-arginine on neurological function, histopathology, and expression of hypoxia-inducible factor-1 alpha following spinal cord ischemia in rats. Eur Surg Res 37:323–329

    Article  CAS  PubMed  Google Scholar 

  74. Ulmann L, Hatcher JP, Hughes JP, Chaumont S, Green PJ, Conquet F, Buell GN, Reeve AJ, Chessell IP, Rassendren F (2008) Up-regulation of P2X4 receptors in spinal microglia after peripheral nerve injury mediates BDNF release and neuropathic pain. J Neurosci 28:11263–11268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Vinsova J, Vavrikova E (2011) Chitosan derivatives with antimicrobial, antitumour and antioxidant activities-a review. Curr Pharm Des 17:3596–3607

    Article  CAS  Google Scholar 

  76. Weishaupt N, Blesch A, Fouad K (2012) BDNF: the career of a multifaceted neurotrophin in spinal cord injury. Exp Neurol 238:254–264

    Article  CAS  PubMed  Google Scholar 

  77. Xu Y, Du Y, Huang R, Gao L (2003) Preparation and modification of N-(2-hydroxyl) propyl-3-trimethyl ammonium chitosan chloride nanoparticle as a protein carrier. Biomaterials 24:5015–5022

    Article  CAS  PubMed  Google Scholar 

  78. Yardim A, Gur C, Comakli S, Ozdemir S, Kucukler S, Celik H, Kandemir FM (2022) Investigation of the effects of berberine on bortezomib-induced sciatic nerve and spinal cord damage in rats through pathways involved in oxidative stress and neuro-inflammation. Neurotoxicology 89:127–139

    Article  CAS  PubMed  Google Scholar 

  79. Zarei M, Sabetkasaei M, Moini Zanjani T, Sahebi Vaighan N (2022) The effect of microglial inhibition on the expression of BDNF, KCC2, and GABAA receptor before and after the establishment of CCI-induced neuropathic pain model. Fundam Clin Pharmacol 36:277–285

    Article  CAS  PubMed  Google Scholar 

  80. Zargani M, Hatami Nasab Z, Feizolahi F, Arabzadeh E (2022) Swimming exercise with l-arginine coated nanoparticles supplementation upregulated HAND2 and TBX5 expression in the cardiomyocytes of aging male rats. Biogerontology 23:473–484

    Article  CAS  PubMed  Google Scholar 

  81. Zhang E, Yi M-H, Ko Y, Kim H-W, Seo JH, Lee YH, Lee W, Kim DW (2013) Expression of LC3 and Beclin 1 in the spinal dorsal horn following spinal nerve ligation-induced neuropathic pain. Brain Res 1519:31–39

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Exercise Physiology, Karaj Branch, Islamic Azad University, Karaj, Iran

    Mehdi Zargani

  2. Exercise and Rehabilitation Sciences Laboratory, School of Physical Therapy, Faculty of Rehabilitation Sciences, Universidad Andres Bello, 7591538, Santiago, Chile

    Rodrigo Ramirez-Campillo

  3. Exercise Physiology Research Center, Life Style Institute, Baqiyatallah University of Medical Sciences, Tehran, Iran

    Ehsan Arabzadeh

Authors
  1. Mehdi Zargani
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rodrigo Ramirez-Campillo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ehsan Arabzadeh
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

M. Z. and E. A. contributed to the study conception and design, material preparation and data collection. Data were analysed and interpreted by all authors. E. A. and R. R. C. were involved in the drafting of the manuscript and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Ehsan Arabzadeh.

Ethics declarations

Ethical approval

All animal experiments were according to the NIH Guide for the Care and Use of Laboratory Animals, country laws and regulations, and in compliance with the Institutional Animal Care and Use Committee (IACUC) at Azad University (Karaj, Iran). The study was endorsed by the Ethics Committee of the University underneath protocol number IR.IAU.K.REC.1400.37.

Competing interests

The authors declares that they have no conflict of interest.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zargani, M., Ramirez-Campillo, R. & Arabzadeh, E. Swimming and L-arginine loaded chitosan nanoparticles ameliorates aging‐induced neuron atrophy, autophagy marker LC3, GABA and BDNF-TrkB pathway in the spinal cord of rats. Pflugers Arch - Eur J Physiol 475, 621–635 (2023). https://doi.org/10.1007/s00424-023-02795-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00424-023-02795-y

Keywords

Search

Navigation