Neuroanatomical circuitry between kidney and rostral elements of brain: a virally mediated transsynaptic tracing study in mice

Ye-ting Zhou , Zhi-gang He , Tao-tao Liu , Mao-hui Feng , Ding-yu Zhang , Hong-bing Xiang

Current Medical Science ›› 2017, Vol. 37 ›› Issue (1) : 63 -69.

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Current Medical Science ›› 2017, Vol. 37 ›› Issue (1) : 63 -69. DOI: 10.1007/s11596-017-1695-y
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Neuroanatomical circuitry between kidney and rostral elements of brain: a virally mediated transsynaptic tracing study in mice

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Abstract

The identity of higher-order neurons and circuits playing an associative role to control renal function is not well understood. We identified specific neural populations of rostral elements of brain regions that project multisynaptically to the kidneys in 3–6 days after injecting a retrograde tracer pseudorabies virus (PRV)-614 into kidney of 13 adult male C57BL/6J strain mice. PRV-614 infected neurons were detected in a number of mesencephalic (e.g. central amygdala nucleus), telencephalic regions and motor cortex. These divisions included the preoptic area (POA), dorsomedial hypothalamus (DMH), lateral hypothalamus, arcuate nucleus (Arc), suprachiasmatic nucleus (SCN), periventricular hypothalamus (PeH), and rostral and caudal subdivision of the paraventricular nucleus of the hypothalamus (PVN). PRV-614/Tyrosine hydroxylase (TH) double-labeled cells were found within DMH, Arc, SCN, PeH, PVN, the anterodorsal and medial POA. A subset of neurons in PVN that participated in regulating sympathetic outflow to kidney was catecholaminergic or serotonergic. PRV-614 infected neurons within the PVN also contained arginine vasopressin or oxytocin. These data demonstrate the rostral elements of brain innervate the kidney by the neuroanatomical circuitry.

Keywords

kidney / hypothalamus / autonomic control / alpha-herpes virus / tryptophan hydroxylase / tyrosine hydroxylase / arginine vasopressin / oxytocin

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Ye-ting Zhou, Zhi-gang He, Tao-tao Liu, Mao-hui Feng, Ding-yu Zhang, Hong-bing Xiang. Neuroanatomical circuitry between kidney and rostral elements of brain: a virally mediated transsynaptic tracing study in mice. Current Medical Science, 2017, 37(1): 63-69 DOI:10.1007/s11596-017-1695-y

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References

[1]

CooteJH. A role for the paraventricular nucleus of the hypothalamus in the autonomic control of heart and kidney. Exp Physiol, 2005, 90(2): 169-173 PMID: 15604110

[2]

YangZ, SmithL, CooteJH. Paraventricular nucleus activation of renal sympathetic neurones is synaptically depressed by nitric oxide and glycine acting at a spinal level. Neuroscience, 2004, 124(2): 421-428 PMID: 14980391

[3]

DibonaGF. Differentiation of vasoactive renal sympathetic nerve fibres. Acta Physiol Scand, 2000, 168(1): 195-200 PMID: 10691800

[4]

LiuTT, LiuBW, HeZG, et al. . Delineation of the central melanocortin circuitry controlling the kidneys by a virally mediated transsynaptic tracing study in transgenic mouse model. Oncotarget, 2016, 7(43): 69256-69266 PMID: 27626491

[5]

ChenM, HeZG, LiuSG, et al. . Motor cortex-periaqueductal gray-rostral ventromedial medulla neuronal circuitry may involve in modulation of nociception by melanocortinergic-opioidergic signaling. Int J Clin Exp Pathol, 2016, 9(8): 7897-7907

[6]

CanoG, CardJP, SvedAF. Dual viral transneuronal tracing of central autonomic circuits involved in the innervation of the two kidneys in rat. J Comp Neurol, 2004, 471(4): 462-481 PMID: 15022264

[7]

CardJP, KobilerO, McCambridgeJ, et al. . Microdissection of neural networks by conditional reporter expression from a Brainbow herpesvirus. Proc Natl Acad Sci USA, 2011, 108(8): 3377-3382 PMID: 21292985 PMCID: 3044368

[8]

ZermannDH, IshigookaM, Doggweiler-WiygulR, et al. . Central autonomic innervation of the kidney. What can we learn from a transneuronal tracing study in an animal model?. J Urol, 2005, 73(3): 1033-1038

[9]

LiuBW, HeZG, ShenSE, et al. . CeA-RVMM serotonergic circuits and sudden unexpected death in epilepsy. Int J Clin Exp Med, 2016, 9(6): 9752-9758

[10]

LiuBW, LiuQQ, LiuSG, et al. . Renal disease and neural circuits: brain-kidney crosstalk. Int J Clind Exp Med, 2016, 9(3): 5326-5333

[11]

HuangJ, WeissML. Characterization of the central cell groups regulating the kidney in the rat. Brain Res, 1999, 845(1): 77-91 PMID: 10529446

[12]

SchrammLP, StrackAM, PlattKB, et al. . Peripheral and central pathways regulating the kidney: a study using pseudorabies virus. Brain Res, 1993, 616(1-2): 251-262 PMID: 7689411

[13]

GlatzerNR, DerbenevAV, BanfieldBW, et al. . Endomorphin-1 modulates intrinsic inhibition in the dorsal vagal complex. J Neurophysiol, 2007, 98(3): 1591-1599 PMID: 17615134

[14]

WillhiteDC, NguyenKT, MasurkarAV, et al. . Viral tracing identifies distributed columnar organization in the olfactory bulb. Proc Natl Acad Sci USA, 2006, 103(33): 12592-12597 PMID: 16895993 PMCID: 1567923

[15]

ZhangY, KermanIA, LaqueA, et al. . Leptin-receptor-expressing neurons in the dorsomedial hypothalamus and median preoptic area regulate sympathetic brown adipose tissue circuits. J Neurosci, 2011, 31(5): 1873-1884 PMID: 21289197 PMCID: 3069639

[16]

XiangHB, LiuC, LiuTT, et al. . Central circuits regulating the sympathetic outflow to lumbar muscles in spinally transected mice by retrograde transsynaptic transport. Int J Clin Exp Pathol, 2014, 7(6): 2987-2897 PMID: 25031717 PMCID: 4097212

[17]

YeDW, LiRC, WuW, et al. . Role of spinal cord in regulating mouse kidney: a virally mediated trans-synaptic tracing study. Urology, 2012, 79(3): 745e1-4

[18]

YeDW, LiuC, LiuTT, et al. . Motor cortex-periaqueductal gray-spinal cord neuronal circuitry may involve in modulation of nociception: a virally mediated transsynaptic tracing study in spinally transected transgenic mouse model. PLoS One, 2014, 9(2): e89486 PMID: 24586817 PMCID: 3929690

[19]

HaoY, TianXB, LiuC, et al. . Retrograde tracing of medial vestibular nuclei connections to the kidney in mice. Int J Clin Exp Pathol, 2014, 7(8): 5348-5354 PMID: 25197422 PMCID: 4152112

[20]

HaoY, TianXB, LiuTT, et al. . MC4R expression in pedunculopontine nucleus involved in the modulation of midbrain dopamine system. Int J Clin Exp Pathol, 2015, 8(2): 2039-2043 PMID: 25973101 PMCID: 4396322

[21]

LiuTT, HongQX, XiangHB. The change in cerebral glucose metabolism after electroacupuncture: a possible marker to predict the therapeutic effect of deep brain stimulation for refractory anorexia nervosa. Int J Clin Exp Med, 2015, 8(10): 19481-19485 PMID: 26770596 PMCID: 4694496

[22]

YeD, GuoQ, FengJ, et al. . Laterodorsal tegmentum and pedunculopontine tegmental nucleus circuits regulate renal functions: Neuroanatomical evidence in mice models. J Huazhong Univ Sci Technolog Med Sci, 2012, 32(2): 216-220 PMID: 22528223

[23]

Voss-AndreaeA, MurphyJG, EllacottKL, et al. . Role of the central melanocortin circuitry in adaptive thermogenesis of brown adipose tissue. Endocrinology, 2007, 148(4): 1550-1560 PMID: 17194736

[24]

FanW, DinulescuDM, ButlerAA, et al. . The central melanocortin system can directly regulate serum insulin levels. Endocrinology, 2000, 141(9): 3072-3079 PMID: 10965876

[25]

FanW, EllacottKL, HalatchevIG, et al. . Cholecystokinin-mediated suppression of feeding involves the brainstem melanocortin system. Nat Neurosci, 2004, 7(4): 335-336 PMID: 15034587

[26]

Franklin KB, Paxinos G. The mouse Brain in Stereotaxic Coordinates. Third Edition. San Diego, CA: Academic Press. 2007.

[27]

GoelN, BaleTL. Sex differences in the serotonergic influence on the hypothalamic-pituitary-adrenal stress axis. Endocrinology, 2010, 151(4): 1784-1794 PMID: 20185764 PMCID: 2850237

[28]

HonigG, LiouA, BergerM, et al. . Precise pattern of recombination in serotonergic and hypothalamic neurons in a Pdx1-cre transgenic mouse line. J Biomed Sci, 2010, 17: 82 PMID: 20950489 PMCID: 2966455

[29]

XiangHB, ZhuWZ, BuHL, et al. . Possible mechanism of subthalamic nucleus stimulation-induced acute renal failure: A virally mediated transsynaptic tracing study in transgenic mouse model. Mov Disord, 2013, 28(14): 2037-2038 PMID: 24038459

[30]

BalthasarN, DalgaardLT, LeeCE, et al. . Divergence of melanocortin pathways in the control of food intake and energy expenditure. Cell, 2005, 123(3): 493-505 PMID: 16269339

[31]

CirielloJ. Afferent renal inputs to paraventricular nucleus vasopressin and oxytocin neurosecretory neurons. Am J Physiol, 1998, 275: R1745-1754 PMID: 9843863

[32]

SimonJK, ZhangTX, CirielloJ. Renal denervation alters forebrain hexokinase activity in neurogenic hypertensive rats. Am J Physiol, 1989, 256: R930-938 PMID: 2705581

[33]

SimonJK, KastingNW, CirielloJ. Afferent renal nerve effects on plasma vasopressin and oxytocin in conscious rats. Am J Physiol, 1989, 256: R1240-1244 PMID: 2735450

[34]

SunZ. Genetic AVP deficiency abolishes cold-induced diuresis but does not attenuate cold-induced hypertension. Am J Physiol Renal Physiol, 2006, 290(6): F1472-1477 PMID: 16396942

[35]

SchmidtA, JardS, DreifussJJ, et al. . Oxytocin receptors in rat kidney during development. Am J Physiol, 1990, 259: F872-881 PMID: 2175561

[36]

LeeHJ, MacbethAH, PaganiJH, et al. . Oxytocin: the great facilitator of life. Prog Neurobiol, 2009, 88(2): 127-151 PMID: 19482229 PMCID: 2689929

[37]

FergusonAV. Systemic angiotensin acts at the subfornical organ to control the activity of paraventricular nucleus neurons with identified projections to the median eminence. Neuroendocrinology, 1988, 47(6): 489-497 PMID: 3399033

[38]

FergusonAV, RenaudLP. Systemic angiotensin acts at subfornical organ to facilitate activity of neurohypophysial neurons. Am J Physiol, 1986, 251: R712-717 PMID: 3766770

[39]

LeeTK, LoisJH, TroupeJH, et al. . Transneuronal tracing of neural pathways that regulate hindlimb muscle blood flow. Am J Physiol Regul Integr Comp Physiol, 2007, 292(4): R1532-1541 PMID: 17158263

[40]

YeZY, LiDP. Activation of the melanocortin-4 receptor causes enhanced excitation in presympathetic paraventricular neurons in obese Zucker rats. Regul Pept, 2011, 166(1-3): 112-120 PMID: 20937332

[41]

Ulrich-LaiYM, HermanJP. Neural regulation of endocrine and autonomic stress responses. Nat Rev Neurosci, 2009, 10(6): 397-409 PMID: 19469025 PMCID: 4240627

[42]

SimmonsDM, SwansonLW. Comparison of the spatial distribution of seven types of neuroendocrine neurons in the rat paraventricular nucleus: toward a global 3D model. J Comp Neurol, 2009, 516(5): 423-441 PMID: 19655400

[43]

BowersRR, FestucciaWT, SongCK, et al. . Sympathetic innervation of white adipose tissue and its regulation of fat cell number. Am J Physiol Regul Integr Comp Physiol, 2004, 286(6): R1167-1175 PMID: 15142857

[44]

MarkAL, AgassandianK, MorganDA, et al. . Leptin signaling in the nucleus tractus solitarii increases sympathetic nerve activity to the kidney. Hypertension, 2009, 53(2): 375-380 PMID: 19103999

[45]

AmannK, VeelkenR. Mechanisms and consequences of sympathetic hyperactivity in renal disease. Clin Nephrol, 2003, 60: S81-92 PMID: 12940538

[46]

RagnauthAK, DevidzeN, MoyV, et al. . Female oxytocin gene-knockout mice, in a semi-natural environment, display exaggerated aggressive behavior. Genes Brain Behav, 2005, 4(4): 229-239 PMID: 15924555

[47]

TeffKL. Visceral nerves: vagal and sympathetic innervation. JPEN J Parenter Enteral Nutr, 2008, 32(5): 569-571 PMID: 18753395

[48]

MarsenicO. Glucose control by the kidney: an emerging target in diabetes. Am J Kidney Dis, 2009, 53(5): 875-883 PMID: 19324482

[49]

ChoiS, DallmanMF. Hypothalamic obesity: multiple routes mediated by loss of function in medial cell groups. Endocrinology, 1999, 140(9): 4081-4088

[50]

ChoiS, HorsleyC, AguilaS, et al. . The hypothalamic ventromedial nuclei couple activity in the hypothalamo-pituitary-adrenal axis to the morning fed or fasted state. J Neurosci, 1996, 16(24): 8170-8180 PMID: 8987842

[51]

WilliamsG, BingC, CaiXJ, et al. . The hypothalamus and the control of energy homeostasis: different circuits, different purposes. Physiol Behav, 2001, 74(4-5): 683-701 PMID: 11790431

[52]

RinamanL. Ascending projections from the caudal visceral nucleus of the solitary tract to brain regions involved in food intake and energy expenditure. Brain Res, 2010, 1350: 18-34 PMID: 20353764 PMCID: 2909454

[53]

BuijsRM, ChunSJ, NiijimaA, et al. . Parasympathetic and sympathetic control of the pancreas: a role for the suprachiasmatic nucleus and other hypothalamic centers that are involved in the regulation of food intake. J Comp Neurol, 2001, 431(4): 405-423 PMID: 11223811

[54]

AllenDE, GellaiM. Mechanisms for the diuresis of acute cold exposure: role for vasopressin?. Am J Physiol, 1993, 264: R524-532 PMID: 8457004

[55]

MurgatroydC, WiggerA, FrankE, et al. . Impaired repression at a vasopressin promoter polymorphism underlies overexpression of vasopressin in a rat model of trait anxiety. J Neurosci, 2004, 24(35): 7762-7770 PMID: 15342744

[56]

NakamuraK, MorrisonSF. A thermosensory pathway that controls body temperature. Nat Neurosci, 2008, 11(1): 62-71 PMID: 18084288

[57]

FanW, Voss-AndreaeA, CaoWH, et al. . Regulation of thermogenesis by the central melanocortin system. Peptides, 2005, 26(10): 1800-1813 PMID: 15979759

[58]

MorrisonSF, NakamuraK, MaddenCJ. Central control of thermogenesis in mammals. Exp Physiol, 2008, 93(7): 773-797 PMID: 18469069 PMCID: 2496891

[59]

MorrisonSF, NakamuraK. Central neural pathways for thermoregulation. Front Biosci, 2011, 16: 74-104

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