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Involvement of Supraoptic Astrocytes in Basilar Artery Occlusion-Evoked Differential Activation of Vasopressin Neurons and Vasopressin Secretion in Rats

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Abstract

Vasopressin (VP) is a key factor in the development of brain injury in ischemic stroke. However, the regulation of VP secretion in basilar artery occlusion (BAO) remains unclear. To clarify the regulation of VP secretion in BAO and the underlying mechanisms, we performed this study in a rat model of BAO with (BC) or without common carotid artery occlusion (CCAO). The results showed that BAO and BC time-dependently increased neurological scores and that BC also increased water contents in the medulla at 2 h and in the pontine at 8 h. Moreover, plasma VP level increased significantly at BAO-8 h, CCAO and BC-2 h but not at BC-8 h; however, VP expressions increased in the supraoptic nucleus (SON) at BC-8 h. The neurological scores were highly correlated with pontine water contents and plasma VP levels. The number of phosphorylated extracellular signal-regulated protein kinase1/2-positive VP neurons increased significantly in the SON at BC-8 h. Similarly, the number of c-Fos-positive VP neurons increased significantly in the SON at BAO-8 h and BC-8 h. In addition, the length of glial fibrillary acidic protein (GFAP) filaments increased significantly in BC compared to BAO only. Aquaporin 4 (AQP4) puncta around VP neurons increased significantly at BC-8 h relative to BC-2 h, which had negative correlation with plasma VP levels. These findings indicate that BAO facilitates VP secretion and increases VP neuronal activity in the SON. The peripheral VP release is possibly under a negative feedback regulation of central VP neuronal activity through increasing GFAP and AQP4 expression in astrocytic processes.

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Abbreviations

AQP4:

Aquaporin 4

BAO:

Basilar artery occlusion

BC:

BAO plus CCAO

CCAO:

Common carotid artery occlusion

ERK1/2:

Extracellular signal-regulated protein kinase1/2

GFAP:

Glial fibrillary acidic protein

pERK1/2:

Phosphorylated ERK1/2

PVN:

Paraventricular nucleus

SON:

Supraoptic nucleus

VP:

Vasopressin

References

  1. Lin SH, Lai CC, Tsai DR, Lo HL (2012) Basilar artery occlusion. J Emerg Med 43:e265–e266

    Article  Google Scholar 

  2. Castaigne P, Lhermitte F, Buge A, Escourolle R, Hauw JJ, Lyon-Caen O (1981) Paramedian thalamic and midbrain infarct: clinical and neuropathological study. Ann Neurol 10:127–148

    Article  CAS  Google Scholar 

  3. Kim J, Choi HY, Nam HS, Lee JY, Heo JH (2008) Mechanism of tuberothalamic infarction. Eur J Neurol 15:1118–1123

    Article  CAS  Google Scholar 

  4. Wojak JC, DeCrescito V, Young W (1991) Basilar artery occlusion in rats. Stroke 22:247–252

    Article  CAS  Google Scholar 

  5. Jia SW, Liu XY, Wang SC, Wang YF (2016) Vasopressin hypersecretion-associated brain edema formation in ischemic stroke: underlying mechanisms. J Stroke Cerebrovasc Dis 25:1289–1300

    Article  Google Scholar 

  6. Kozniewska E, Romaniuk K (2008) Vasopressin in vascular regulation and water homeostasis in the brain. J Physiol Pharmacol 59(Suppl 8):109–116

    PubMed  Google Scholar 

  7. Ermisch A, Landgraf R (1990) Vasopressin, the blood-brain barrier, and brain performance. Adv Exp Med Biol 274:71–89

    Article  CAS  Google Scholar 

  8. Zhao XY, Wu CF, Yang J, Gao Y, Sun FJ, Wang DX, Wang CH, Lin BC (2015) Effect of arginine vasopressin on the cortex edema in the ischemic stroke of Mongolian gerbils. Neuropeptides 51:55–62

    Article  Google Scholar 

  9. Huang W, Yang Y, Wu S, Jin Z, Bao D, Gan H (2001) Early changes of arginine vasopressin and angiotensin II in patients with acute cerebral injury. Chin J Traumatol 4:161–163

    CAS  PubMed  Google Scholar 

  10. Cui D, Jia S, Yu J, Li D, Li T, Liu Y, Chang J, Wang X, Liu X, Wang Y-F (2020) Alleviation of cerebral infarction of rats with middle cerebral artery occlusion by inhibition of aquaporin 4 in the Supraoptic nucleus. ASN Neuro 12:1759091420960550

    Article  CAS  Google Scholar 

  11. Cui D, Jia S, Li T, Li D, Wang X, Liu X, Wang Y-F (2021) Alleviation of brain injury by applying TGN-020 in the supraoptic nucleus via inhibiting vasopressin neurons in rats of focal ischemic stroke. Life Sci 264:118683

  12. Zeynalov E, Jones SM, Seo JW, Snell LD, Elliott JP (2015) Arginine-vasopressin receptor blocker Conivaptan reduces brain edema and blood-brain barrier disruption after experimental stroke in mice. PLoS One 10:e0136121

    Article  Google Scholar 

  13. Hedna VS, Bidari S, Gubernick D, Ansari S, Satriotomo I, Khan AA, Qureshi AI (2014) Treatment of stroke related refractory brain edema using mixed vasopressin antagonism: a case report and review of the literature. BMC Neurol 14:213

    Article  Google Scholar 

  14. Wang YF, Parpura V (2016) Central role of maladapted astrocytic plasticity in ischemic brain edema formation. Front Cell Neurosci 10:129

    PubMed  PubMed Central  Google Scholar 

  15. Wang YF, Parpura V (2018) Astroglial modulation of Hydromineral balance and cerebral edema. Front Mol Neurosci 11:204

    Article  Google Scholar 

  16. Li D, Liu H, Liu X, Wang H, Li T, Wang X, Jia S, Wang P, Wang YF (2020) Involvement of hyperpolarization-activated cyclic nucleotide-Gated Channel 3 in oxytocin neuronal activity in lactating rats with pup deprivation. ASN Neuro 12:1759091420944658

    Article  CAS  Google Scholar 

  17. Lin L, Huang Y, Zhang W (2008) Acute basilar artery occlusion: topographic study of infarcts. Neurol Res 30:341–343

    Article  Google Scholar 

  18. Namioka A, Namioka T, Sasaki M, Kataoka-Sasaki Y, Oka S, Nakazaki M, Onodera R, Suzuki J, Sasaki Y, Nagahama H, Kocsis JD, Honmou O (2018) Intravenous infusion of mesenchymal stem cells for protection against brainstem infarction in a persistent basilar artery occlusion model in the adult rat. J Neurosurg:1–9

  19. Jimenez A, Gonzalez-Mariscal G (2019) Maternal responsiveness to suckling is modulated by time post-nursing: a behavioural and c-Fos/oxytocin immunocytochemistry study in rabbits. J Neuroendocrinol 31:e12788

    Article  Google Scholar 

  20. Wang SC, Parpura V, Wang Y-F (2020) Astroglial regulation of magnocellular neuroendocrine cell activities in the supraoptic nucleus. Neurochem Res. https://doi.org/10.1007/s11064-020-03172-2

  21. Martin NA, Macagba-Crain CL, Geffner M, Peacock W (1990) Isolated growth hormone deficiency associated with a giant arteriovenous varix. Neurosurgery 27:295–299

    Article  CAS  Google Scholar 

  22. Brillault J, Lam TI, Rutkowsky JM, Foroutan S, O'Donnell ME (2008) Hypoxia effects on cell volume and ion uptake of cerebral microvascular endothelial cells. Am J Physiol Cell Physiol 294:C88–C96

    Article  CAS  Google Scholar 

  23. Dreier JP, Lemale CL, Kola V, Friedman A, Schoknecht K (2018) Spreading depolarization is not an epiphenomenon but the principal mechanism of the cytotoxic edema in various gray matter structures of the brain during stroke. Neuropharmacology 134:189–207

    Article  CAS  Google Scholar 

  24. Katori E, Ohta T, Nakazato Y, Ito S (2001) Vasopressin-induced contraction in the rat basilar artery in vitro. Eur J Pharmacol 416:113–121

    Article  CAS  Google Scholar 

  25. Hou D, Jin F, Li J, Lian J, Liu M, Liu X-N, Xu Y, Zhang C, Zhao C, Jia S, Jiao R, Liu X-Y, Wang X, Zhang Y, Wang Y-F (2016) Model roles of the hypothalamo-Neurohypophysial system in neuroscience study. Biochem Pharmacol (Los Angel) 5:211

  26. Lozic M, Sarenac O, Murphy D, Japundzic-Zigon N (2018) Vasopressin, central autonomic control and blood pressure regulation. Curr Hypertens Rep 20:11

    Article  Google Scholar 

  27. Radak D, Resanovic I, Isenovic ER (2014) Changes in hypothalamus-pituitary-adrenal axis following transient ischemic attack. Angiology 65:723–732

    Article  Google Scholar 

  28. Franceschini R, Tenconi GL, Zoppoli F, Barreca T (2001) Endocrine abnormalities and outcome of ischaemic stroke. Biomed Pharmacother 55:458–465

    Article  CAS  Google Scholar 

  29. Grindstaff RJ, Grindstaff RR, Sullivan MJ, Cunningham JT (2000) Role of the locus ceruleus in baroreceptor regulation of supraoptic vasopressin neurons in the rat. Am J Physiol Regul Integr Comp Physiol 279:R306–R319

    Article  CAS  Google Scholar 

  30. Senatorov VV, Renaud LP (1999) Projections of medullary and pontine noradrenergic neurons to the horizontal limb of the nucleus of diagonal band in the rat. Neuroscience 88:939–947

    Article  CAS  Google Scholar 

  31. Ludwig M, Sabatier N, Bull PM, Landgraf R, Dayanithi G, Leng G (2002) Intracellular calcium stores regulate activity-dependent neuropeptide release from dendrites. Nature 418:85–89

    Article  CAS  Google Scholar 

  32. Wang Y-F, Hatton GI (2009) Astrocytic plasticity and patterned oxytocin neuronal activity: dynamic interactions. J Neurosci 29:1743–1754

    Article  CAS  Google Scholar 

  33. Liu X, Jia S, Zhang Y, Wang Y-F (2016) Pulsatile but not tonic secretion of oxytocin plays the role of anti-precancerous lesions of the mammary glands in rat dams separated from the pups during lactation. M J Neuro 1:002

    Google Scholar 

  34. Wang YF, Ponzio TA, Hatton GI (2006) Autofeedback effects of progressively rising oxytocin concentrations on supraoptic oxytocin neuronal activity in slices from lactating rats. Am J Physiol Regul Integr Comp Physiol 290:R1191–R1198

    Article  CAS  Google Scholar 

  35. Li D, Li T, Yu J, Liu X, Jia S, Wang X, Wang P, Wang YF (2020) Astrocytic modulation of Supraoptic oxytocin neuronal activity in rat dams with pup-deprivation at different stages of lactation. Neurochem Res. https://doi.org/10.1007/s11064-11020-03129-11065

  36. Wang YF, Sun MY, Hou Q, Parpura V (2013) Hyposmolality differentially and spatiotemporally modulates levels of glutamine synthetase and serine racemase in rat supraoptic nucleus. Glia 61:529–538

    Article  Google Scholar 

  37. Wang YF, Sun MY, Hou Q, Hamilton KA (2013) GABAergic inhibition through synergistic astrocytic neuronal interaction transiently decreases vasopressin neuronal activity during hypoosmotic challenge. Eur J Neurosci 37:1260–1269

    Article  Google Scholar 

  38. Hatton GI (2004) Morphological plasticity of astroglial/neuronal interactions: functional implications. In: Hatton GI, Parpura V (eds) Glial neuronal signaling. Kluwer Academic Publishers, Boston, pp 99–124

    Chapter  Google Scholar 

  39. Curras-Collazo MC, Patel UB, Hussein MO (2002) Reduced susceptibility of magnocellular neuroendocrine nuclei of the rat hypothalamus to transient focal ischemia produced by middle cerebral artery occlusion. Exp Neurol 178:268–279

    Article  Google Scholar 

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Funding

This work was supported by the higher education talents funds of Heilongjiang province (grant No. 002000154, YFW) and the fund of “Double-First-Class” Construction of Harbin Medical University (key laboratory of preservation of human genetic resources and disease control in China).

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DYL collected and analyzed data and wrote the first draft, DC participated the preliminary study, all participated in the discussion and revision of this work, and YFW designed the study and edited the draft.

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Correspondence to Dongyang Li or Yu-Feng Wang.

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All authors claim that there are no conflicts of interest.

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Special issue: In Honor of Prof. Vladimir Parpura.

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Li, D., Cui, D., Jia, S. et al. Involvement of Supraoptic Astrocytes in Basilar Artery Occlusion-Evoked Differential Activation of Vasopressin Neurons and Vasopressin Secretion in Rats. Neurochem Res 46, 2651–2661 (2021). https://doi.org/10.1007/s11064-021-03246-9

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  • DOI: https://doi.org/10.1007/s11064-021-03246-9

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