#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Botulinum toxin A injection into the entopeduncular nucleus improves dynamic locomotory parameters in hemiparkinsonian rats


Autoři: Adrianna R. Tsang aff001;  Nagalingam Rajakumar aff002;  Mandar S. Jog aff001
Působiště autorů: Department of Physiology and Pharmacology, Western University, London, Ontario, Canada aff001;  Department of Anatomy and Cell Biology, Western University, London, Ontario, Canada aff002;  Department of Clinical Neurological Sciences, London Health Sciences Centre, London, Ontario, Canada aff003
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0223450

Souhrn

Parkinson’s disease is associated with hyperactivity of the subthalamic nucleus (STN), contributing to motor and gait disturbances. Although deep brain stimulation of the STN alleviates certain motor dysfunction, its specific effect on gait abnormalities remains controversial. This study investigated the long-term changes in locomotion following direct infusions of botulinum toxin-A into the globus pallidus internal segment (GPi) to suppress the flow of information from the STN to the GPi in a hemiparkinsonian rat model. Static and dynamic gait parameters were quantified using a CatWalk apparatus. Interestingly, botulinum toxin-A at 0.5 ng significantly reduced only the dynamic gait parameters of hemiparkinsonian rats at 1 week and 1 month post-infusion, while static gait parameters did not change. This study offers new insights into the complexity of basal ganglia in locomotor control and shows the potential of central infusion of botulinum toxin-A as a novel intervention in the study of experimental hemiparkinson’s disease.

Klíčová slova:

Rodents – Statistical data – Biological locomotion – Gait analysis – Walking – Dopaminergics – Parkinson disease – Levodopa


Zdroje

1. De Lau LM, Breteler MM. Epidemiology of Parkinson's disease. The Lancet Neurology. 2006;5: 525–535. doi: 10.1016/S1474-4422(06)70471-9 16713924

2. Fearnley JM, Lees AJ. Ageing and Parkinson's disease: Substantia nigra regional selectivity. Brain. 1991;114: 2283–2301. doi: 10.1093/brain/114.5.2283 1933245

3. Rodriguez MC, Obeso JA, Olanow CW. Subthalamic nucleus‐mediated excitotoxicity in parkinson's disease: A target for neuroprotection. Annals of Neurology. 1991;44: S1.

4. Blandini F, Nappi G, Tassorelli C, Martignoni E. Functional changes of the basal ganglia circuitry in Parkinson's disease. Progress in Neurobiology. 2000;62: 63–88. 10821982

5. Williams DR, Watt HC, Lees AJ. Predictors of falls and fractures in bradykinetic rigid syndromes: a retrospective study. Journal of Neurology, Neurosurgery & Psychiatry. 2006;77: 468–473.

6. Lewis SJ, Barker RA. A pathophysiological model of freezing of gait in Parkinson's disease. Parkinsonism & Related Disorders. 2009;15: 333–338.

7. Sofuwa O, Nieuwboer A, Desloovere K, Willems AM, Chavret F, Jonkers I. Quantitative gait analysis in Parkinson’s disease: comparison with a healthy control group. Archives of Physical Medicine and Rehabilitation. 2005;86: 1007–1013. doi: 10.1016/j.apmr.2004.08.012 15895349

8. Blin O, Ferrandez AM, Pailhous J, Serratrice G. Dopa-sensitive and dopa-resistant gait parameters in Parkinson's disease. Journal of the Neurological Sciences. 1991;103: 51–54. doi: 10.1016/0022-510x(91)90283-d 1865232

9. Lord S, Galna B, Rochester L. Moving forward on gait measurement: toward a more refined approach. Movement Disorders. 2013; 28: 1534–1543. doi: 10.1002/mds.25545 24132841

10. Krack P, Batir A, Van Blercom N, Chabardes S, Fraix V, Ardouin C, et al. Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson's disease. New England Journal of Medicine. 2003; 349: 1925–1934. doi: 10.1056/NEJMoa035275 14614167

11. Cantiniaux S, Vaugoyeau M, Robert D, Horrelou-Pitek C, Mancini J, Witjas T, Azulay JP. Comparative analysis of gait and speech in Parkinson's disease: hypokinetic or dysrhythmic disorders? Journal of Neurology, Neurosurgery & Psychiatry. 2010;81: 177–184.

12. Zibetti M, Merola A, Rizzi L, Ricchi V, Angrisano S, Azzaro C, et al. Beyond nine years of continuous subthalamic nucleus deep brain stimulation in Parkinson's disease. Movement Disorders. 2011;26: 2327–2334. doi: 10.1002/mds.23903 22012750

13. Kelly VE, Israel SM, Samii A, Slimp JC, Goodkin R, Shumway-Cook A. Assessing the effects of subthalamic nucleus stimulation on gait and mobility in people with Parkinson disease. Disability and Rehabilitation. 2010;32: 929–936. doi: 10.3109/09638280903374139 19874214

14. Kelly VE, Samii A, Slimp JC, Price R, Goodkin R, Shumway-Cook A. Gait changes in response to subthalamic nucleus stimulation in people with Parkinson disease: a case series report. Journal of Neurologic Physical Therapy. 2006;30: 184–194. 17233926

15. Cossu G, Pau M. Subthalamic nucleus stimulation and gait in Parkinson’s disease: a not always fruitful relationship. Gait & Posture. 2017;52: 205–210.

16. Tillerson JL, Cohen AD, Philhower J, Miller GW, Zigmond MJ, Schallert T. Forced limb-use effects on the behavioral and neurochemical effects of 6-hydroxydopamine. Journal of Neuroscience. 2001;21: 4427–4435. 11404429

17. Iancu R, Mohapel P, Brundin P, Paul G. Behavioral characterization of a unilateral 6-OHDA-lesion model of Parkinson's disease in mice. Behavioural Brain Research. 2005;162: 1–10. doi: 10.1016/j.bbr.2005.02.023 15922062

18. De Medinaceli L, Freed WJ, Wyatt RJ. An index of the functional condition of rat sciatic nerve based on measurements made from walking tracks. Experimental Neurology. 1982;77: 634–643. doi: 10.1016/0014-4886(82)90234-5 7117467

19. Hamers FP, Lankhorst AJ, van Laar TJ, Veldhuis WB, Gispen WH. Automated quantitative gait analysis during overground locomotion in the rat: its application to spinal cord contusion and transection injuries. Journal of Neurotrauma. 2001;18: 187–201. doi: 10.1089/08977150150502613 11229711

20. Vlamings R, Visser-Vandewalle V, Koopmans G, Joosten EAJ, Kozan R, Kapla S, et al. High frequency stimulation of the subthalamic nucleus improves speed of locomotion but impairs forelimb movement in Parkinsonian rats. Neuroscience. 2007;148: 815–823. doi: 10.1016/j.neuroscience.2007.06.043 17706885

21. Chuang CS, Su HL, Cheng FC, Hsu SH, Chuang CF. Liu CS. Quantitative evaluation of motor function before and after engraftment of dopaminergic neurons in a rat model of Parkinson's disease. Journal of Biomedical Science. 2010;17, 9. doi: 10.1186/1423-0127-17-9 20152049

22. Vandeputte C, Taymans JM, Casteels C, Coun F, Ni Y, Van Laere K, Baekelandt V. Automated quantitative gait analysis in animal models of movement disorders. BMC Neuroscience. 2010;11: 92. doi: 10.1186/1471-2202-11-92 20691122

23. Westin JE, Janssen MLF, Sager TN, Temel Y. Automated gait analysis in bilateral Parkinsonian rats and the role of L-DOPA therapy. Behavioural Brain Research. 2012;226: 519–528. doi: 10.1016/j.bbr.2011.10.006 22008381

24. Zhou M, Zhang W, Chang J, Wang J, Zheng W, Yang Y, et al. Gait analysis in three different 6-hydroxydopamine rat models of Parkinson's disease. Neuroscience Letters. 2015;584: 184–189. doi: 10.1016/j.neulet.2014.10.032 25449863

25. Aron AR, Poldrack RA. Cortical and subcortical contributions to stop signal response inhibition: role of the subthalamic nucleus. Journal of Neuroscience. 2006;26: 2424–2433. doi: 10.1523/JNEUROSCI.4682-05.2006 16510720

26. Obeso JA, Marin C, Rodriguez‐Oroz C, Blesa J, Benitez‐Temiño B, Mena‐Segovia J, et al. The basal ganglia in Parkinson's disease: current concepts and unexplained observations. Annals of Neurology. 2008; 64: S30–S46. doi: 10.1002/ana.21481 19127584

27. Tewari A, Jog R, Jog MS. The striatum and subthalamic nucleus as independent and collaborative structures in motor control. Frontiers in systems neuroscience. 2016;10: 17. doi: 10.3389/fnsys.2016.00017 26973474

28. Benabid AL, Pollak P, Louveau A, Henry S, De Rougemont J. Combined (thalamotomy and stimulation) stereotactic surgery of the VIM thalamic nucleus for bilateral Parkinson disease. Stereotactic and Functional Neurosurgery. 1987;50: 344–346.

29. Burgen ASV, Dickens F, Zatman LJ. The action of botulinum toxin on the neuro‐muscular junction. The Journal of Physiology. 1949;109: 10–24. doi: 10.1113/jphysiol.1949.sp004364 15394302

30. Samotus O, Rahimi F, Lee J, Jog MS. Functional Ability Improved in Essential Tremor by IncobotulinumtoxinA Injections Using Kinematically Determined Biomechanical Patterns–A New Future. PLOS One. 2016;11: e0153739. doi: 10.1371/journal.pone.0153739 27101283

31. Sanchez‐Prieto J, Sihra TS, Evans D, Ashton A, Dolly JO, Nicholls DG. Botulinum toxin A blocks glutamate exocytosis from guinea‐pig cerebral cortical synaptosomes. The FEBS Journal. 1987;165: 675–681.

32. Bigalke H, Heller I, Bizzini B, Habermann E. Tetanus toxin and botulinum A toxin inhibit release and uptake of various transmitters, as studied with particulate preparations from rat brain and spinal cord. Naunyn-Schmiedeberg's Archives of Pharmacology. 1981;316: 244–251. doi: 10.1007/bf00505657 6114440

33. McMahon HT, Foran P, Dolly JO, Verhage M, Wiegant VM, Nicholls DG. Tetanus toxin and botulinum toxins type A and B inhibit glutamate, gamma-aminobutyric acid, aspartate, and met-enkephalin release from synaptosomes. Clues to the locus of action. Journal of Biological Chemistry. 1992;267: 21338–21343. 1356988

34. Hawlitschka A, Antipova V, Schmitt O, Witt M, Benecke R, Mix E, Wree A. Intracerebrally applied botulinum neurotoxin in experimental neuroscience. Current Pharmaceutical Biotechnology. 2013;14: 124–130. 23092264

35. Wree A, Mix E, Hawlitschka A, Antipova V, Witt M, Schmitt O, Benecke R. Intrastriatal botulinum toxin abolishes pathologic rotational behaviour and induces axonal varicosities in the 6-OHDA rat model of Parkinson's disease. Neurobiology of Disease. 2011;41: 291–298. doi: 10.1016/j.nbd.2010.09.017 20955797

36. Antipova VA, Holzmann C, Schmitt O, Wree A, Hawlitschka A. Botulinum Neurotoxin A Injected Ipsilaterally or Contralaterally into the Striatum in the Rat 6-OHDA Model of Unilateral Parkinson’s Disease Differently Affects Behavior. Frontiers in Behavioral Neuroscience. 2017;11: 119. doi: 10.3389/fnbeh.2017.00119 28680396

37. Antipova VA, Hawlitschka A, Mix E, Schmitt O, Dräger D, Benecke R, Wree A. Behavioral and structural effects of unilateral intrastriatal injections of botulinum neurotoxin a in the rat model of Parkinson's disease. Journal of Neuroscience Research. 2013;91: 838–847. doi: 10.1002/jnr.23210 23553727

38. Hawlitschka A, Holzmann C, Witt S, Spiewok J, Neumann AM, Schmitt O, et al. Intrastriatally injected botulinum neurotoxin-A differently effects cholinergic and dopaminergic fibers in C57BL/6 mice. Brain Research. 2017;1676: 46–56. doi: 10.1016/j.brainres.2017.09.016 28919466

39. Wedekind F, Oskamp A, Lang M, Hawlitschka A, Zilles K, Wree A, Bauer A. Intrastriatal administration of botulinum neurotoxin A normalizes striatal D2R binding and reduces striatal D1R binding in male hemiparkinsonian rats. Journal of Neuroscience Research. 2018;96: 75–86. doi: 10.1002/jnr.24110 28695985

40. Tsang AR, Rajakumar N, Jog MS. Intrapallidal injection of botulinum toxin A recovers gait deficits in a parkinsonian rodent model. Acta Physiologica. 2018;226: e13230. doi: 10.1111/apha.13230 30506881

41. Schallert T, Tillerson JL. Intervention strategies for degeneration of dopamine neurons in parkinsonism. In: Emerich DF, Dean RL, Sanberg PR, editors. Central nervous system diseases. Totowa: Humana Press; 2000. pp. 131–151.

42. Olsson M, Nikkhah G, Bentlage C, Bjorklund A. Forelimb akinesia in the rat Parkinson model: differential effects of dopamine agonists and nigral transplants as assessed by a new stepping test. Journal of Neuroscience. 1995;15: 3863–3875. 7751951

43. Metz GA, Tse A, Ballermann M, Smith LK, Fouad K. The unilateral 6‐OHDA rat model of Parkinson's disease revisited: an electromyographic and behavioural analysis. European Journal of Neuroscience. 2005;22: 735–744. doi: 10.1111/j.1460-9568.2005.04238.x 16101755

44. Shi LH, Luo F, Woodward DJ, Chang JY. Basal ganglia neural responses during behaviorally effective deep brain stimulation of the subthalamic nucleus in rats performing a treadmill locomotion test. Synapse. 2006;59: 445–457. doi: 10.1002/syn.20261 16521122

45. Dibble LE, Nicholson DE, Shultz B, MacWilliams BA, Marcus RL, Moncur C. Sensory cueing effects on maximal speed gait initiation in persons with Parkinson's disease and healthy elders. Gait & Posture. 2004;19: 215–225.

46. Krystkowiak P, Blatt JL, Bourriez JL, Duhamel A, Perina M, Blond S, et al. Effects of subthalamic nucleus stimulation and levodopa treatment on gait abnormalities in Parkinson disease. Archives of Neurology. 2003;60: 80–84. doi: 10.1001/archneur.60.1.80 12533092

47. Kim SD, Yiannikas C, Mahant N, Vucic S, Fung VS. Treatment of proximal upper limb tremor with botulinum toxin therapy. Movement Disorders. 2014;29: 835–838. doi: 10.1002/mds.25739 24519658

48. Samotus O, Rahimi F, Lee J, Jog M. Functional ability improved in essential tremor by incobotulinumtoxinA injections using kinematically determined biomechanical patterns–A new future. PLOS One. 2016;11: e0153739. doi: 10.1371/journal.pone.0153739 27101283

49. Zakin E, Simpson D. Botulinum toxin in management of limb tremor. Toxins. 2017;9: 365.

50. Lau B, Welter ML, Belaid H, Fernandez Vidal S, Bardinet E, Grabli D, Karachi C. The integrative role of the pedunculopontine nucleus in human gait. Brain. 2015;138: 1284–1296. doi: 10.1093/brain/awv047 25765327

51. Kordys E, Apetz N, Schneider K, Duncan E, Büschbell B, Rohleder C, et al. Motor impairment and compensation in a hemiparkinsonian rat model: Correlation between dopamine depletion severity, cerebral metabolism and gait patterns. EJNMMI Research;2017;7: 68. doi: 10.1186/s13550-017-0317-9 28831764

52. Takakusaki K. Functional neuroanatomy for posture and gait control. Journal of Movement Disorders. 2017;10: 1. doi: 10.14802/jmd.16062 28122432


Článok vyšiel v časopise

PLOS One


2019 Číslo 10
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#