MOTOR ALTERATIONS IN HEPATIC ENCEPHALOPATHY MECHANISMS AND TREATMENTS

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1 MOTOR ALTERATIONS IN HEPATIC ENCEPHALOPATHY MECHANISMS AND TREATMENTS Patients with liver disease show alterations in motor function and coordination including: psychomotor slowing, ataxia, flapping tremor, hypokinesia, bradikinesia, mini-asterixis, asterixis Different types of motor alterations may appear at different stages of progression of liver disease and of hepatic encephalopathy 1

2 Some motor alterations may appear before minimal hepatic encephalopathy is detectable using the PHES battery of psychometric tests Butz M, Timmermann L, Braun M, Groiss SJ, Wojtecki L, Ostrowski S, Krause H, Pollok B, Gross J, Südmeyer M, Kircheis G, Häussinger D, Schnitzler A. Acta Neurol Scand Jul;122(1): ataxia, tremor, and slowing of finger movements are early markers for cerebral dysfunction in HE patients even prior to neuropsychometric alterations becoming detectable. Similar findings by Jover et al, Alicante, Spain This indicates that: There are some neurological (motor) alterations which are not detected with the PHES battery and are detected by other procedures The PHES battery detects some types of minimal hepatic encephalopathy but not others 2

3 Which are the mechanisms leading to motor alterations in HE? A main neuronal circuit modulating motor activity is the Basal ganglia-thalamus-cortex Different groups have proposed that motor alterations in patients with liver cirrhosis are due to altered functional connections within the basal ganglia-thalamo-cortical loop Weissenborn K, Kolbe H.Metab Brain Dis.1998; 13: Amodio P, Montagnese S, Gatta A, Morgan MY. Metab Brain Dis ; 19: Timmermann L, Gross J, Butz M, Kircheis G, Haussinger D, Schnitzler A. Neurology. 2003; 61: However, the function of the circuit and the mechanisms leading to the possible functional alterations have not been clarified. 3

4 1.Alterations in the function of the neuronal circuits between basal ganglia-thalamus-cortex in rats with HE due to PCS. 2.Molecular mechanisms leading to hypokinesia in rats with HE due to PCS. Restoration of motor activity by pharmacological treatment. 3.Role of neuroinflammation in motor alterations in rats with HE due to PCS 4.Role of hyperammonemia in the induction of neuroinflammation and of motor alterations in hepatic encephalopathy Activation of metabotropic glutamate receptors in activates the basal ganglia-thalamus-cortex circuit and induces motor activity Motor activation MDT VP mglur We have analyzed the function of this neuronal circuit in vivo by microdialysis in freely moving rats and its alteration in rats with HE (porta-caval shunt) 4

5 Motor activation induced by activation of mglurs in is higher in rats with PCS than in control rats Motor activation VP MDT Analysis of neurotransmission in the basal ganglia-thalamus-cortex circuit in control rats and rats with HE due to PCS DA VP Motor activation MDT We insert a cannula in to inject the agonist of mglurs and microdialysis probes in, ventral pallidum, medio-dorsal thalamus and cortex to determine extracellular Glu, DA and GABA 5

6 Motor activation DA in DA GLU in PFCx GABA in VP VP MDT GABA in MDT In PCS rats, activation of mglurs in does not activates the normal neuronal circuit, but increases glutamate in cortex and motor activity Is an alternative circuit activated? DA VP Motor activation mglur MDT Motor activation? 6

7 Motor activation GLU in GLU in PFCx GABA in GABA in Motor activation induced by activation of mglurs in is mediated by different mechanisms and neuronal circuits in rats with HE and in control rats CONTROL RATS PCS RATS Motor activation Motor activation DA Nacc M PFCx Glu VP MDT VP MDT mglur mglur 7

8 The function of the basal ganglia-thalamuscortex circuit is altered in rats with HE and hyperammonemia, leading to altered modulation of motor function. Cauli, O., Mlili, N., Llansola, M. and Felipo, V. Eur. J. Neurosci. (2007) 25, Cauli, O, Mlili, N., Rodrigo, R. and Felipo, V. J. Neurochem. (2007) 103:38-46 This supports that motor symptoms in patients with liver cirrhosis are due to altered functional connections within the basal ganglia-thalamocortical loop, as proposed by several groups 1.Alterations in the function of the neuronal circuits between basal ganglia-thalamus-cortex in rats with HE due to PCS. 2.Molecular mechanisms leading to hypokinesia in rats with HE due to PCS. Restoration of motor activity by pharmacological treatment. 3.Role of neuroinflammation in motor alterations in rats with HE due to PCS 4.Role of hyperammonemia in the induction of neuroinflammation and of motor alterations in hepatic encephalopathy 8

9 Activation of mglurs in induces more motor activity in PCS than in control rats. However, under basal conditions, PCS rats show reduced motor activity, reproducing the hypokinesia of patients with HE Motor activation Hypokinesia Under basal conditions, extracellular glutamate is increased more than 10-fold in of PCS rats. This increase is responsible for hypokinesia in these rats Hypokinesia 9

10 Hypokinesia Hypokinesia mglur1 CPCCOEt Cauli, O, Llansola M, Erceg S, and Felipo, V. J. Hepatol. (2006) 45: Hypokinesia CPCCOEt Hypokinesia in rats with PCS is due to increased extracellular glutamate and activation of mglur1 in Blocking mglur1 in restores motor activity 10

11 Altered glutamatergic Hypokinesia neurotransmission in one area () may lead to altered GABAergic neurotransmission in another area (), which, in turn, may alter glutamatergic neurotransmission in another area (cortex) The neurological alterations in HE are the consequence of sequential alterations in different neurotransmitter systems and in the function of neuronal circuits 1.Alterations in the function of the neuronal circuits between basal ganglia-thalamus-cortex in rats with HE due to PCS. 2.Molecular mechanisms leading to hypokinesia in rats with HE due to PCS. Restoration of motor activity by pharmacological treatment. 3.Role of neuroinflammation in motor alterations in rats with HE due to PCS 4.Role of hyperammonemia in the induction of neuroinflammation and of motor alterations in hepatic encephalopathy 11

12 WHICH FACTORS ASSOCIATED WITH CHRONIC LIVER FAILURE ARE RESPONSIBLE FOR DECREASED MOTOR ACTIVITY? HYPERAMMONEMIA INFLAMMATION NEUROINFLAMMATION IN PCS RATS PCS increases inflammatory parameters in cerebral cortex. Effect of Ibuprofen PARAMETER CONTROL RATS CONTROL + IBUPROFEN PCS RATS PCS + IBUPROFEN Blood ammonia (μm) 74 ± 8 (19) 102 ± 9 (17) 203 ± 14*** (21) 185 ± 17** (22) IL-6 (pg/ml) 57 ± 4 (6) 65 ± 3 (6) 77 ± 7* (6) 86 ± 7** (6) TNF-α (pg/ml) 26 ± 4 (5) 23 ± 4 (5) 17 ± 3 (5) 33 ± 2 a (5) COX activity (U/mg protein) inos activity (cpm/mg prot.min) 2.2 ± 0.4 (7) 14 ± 1 (16) 1.9 ± 0.4 (7) 16 ± 1 (14) 20 ± 3*** (7) 18 ± 1** (17) 3.0 ± 0.9 a (7) 14 ± 1 a (14) Cauli, O., Rodrigo, R., Piedrafita, B., Boix, J. and Felipo, V. Hepatology (2007) 46,

13 Treatmentwithananti-inflammatory (ibuprofen) normalizes COX activity in cortex of rats with HE due to PCS Cauli, O., Rodrigo, R., Piedrafita, B., Boix, J. and Felipo, V. Hepatology (2007) 46, Treatment with an anti-inflammatory (ibuprofen) normalizes motor activity of PCS rats MOTOR ACTIVITY (ambulatory counts in 60 min) B B B B B B B B SHAM/VEH * PCS/VEH * * * * * * * * * Sham PCS Sham PCS Sham PCS Ibuprofen (mg/kd.day) DAYS AFTER STARTING IBUPROFEN (10 DAYS AFTER SURGERY) SHAM/IBU5 PCS/IBU5 SHAM/IBU15 PCS/IBU15 SHAM/IBU30 PCS/IBU30 Cauli, O., Rodrigo, R., Piedrafita, B., Llansola, M., Mansouri, MT and Felipo, V. J Neurosci Res. (2009) 87(6):

14 Treatment with ibuprofen restores the amount of glutamate transportes and reduces extracellular glutamate in and hypokinesia in PCS rats Glutamate transporters EAAC-1 Extracellular Glutamate Hypokinesia GLT-1 Sham PCS IBU + + Sham PCS IBU + + Cauli, O., Rodrigo, R., Piedrafita, B., Llansola, M. Mansouri, MT and Felipo, V. J Neurosci Res. (2009) 87(6): Hypokinesia Hypokinesia in rats with HE due to PCS is due to neuroinflammation Treatmentwithanantiinflammatory restores motor activity 14

15 1.Alterations in the function of the neuronal circuits between basal ganglia-thalamus-cortex in rats with HE due to PCS. 2.Molecular mechanisms leading to hypokinesia in rats with HE due to PCS. Restoration of motor activity by pharmacological treatment. 3.Role of neuroinflammation in motor alterations in rats with HE due to PCS 4.Role of hyperammonemia in the induction of neuroinflammation and of motor alterations in hepatic encephalopathy WHICH FACTORS ASSOCIATED WITH CHRONIC LIVER FAILURE ARE RESPONSIBLE FOR DECREASED MOTOR ACTIVITY? HYPERAMMONEMIA INFLAMMATION 15

16 Experiments to assess the role of hyperammonemia in the motor alterations in HE ANIMAL MODEL OF CHRONIC HEPATIC ENCEPHALOPATHY Rats with PCS Rats with bile duct ligation ANIMAL MODEL OF CHRONIC HYPERAMMONEMIA without LIVER FAILURE Rats fed an ammoniumcontaining diet for at least 3 weeks RATS WITH PURE CHRONIC HYPERAMMONEMIA WITHOUT LIVER FAILURE ALSO SHOW HYPOLOCOMOTION, WHICH IS REVERSED BY IBUPROFEN, AN ANTI-INFLAMMATORY MOTOR ACTIVITY C C HA HA IBU

17 RATS WITH PURE CHRONIC HYPERAMMONEMIA SHOW NEUROINFLAMMATION WITH INCREASED LEVELS OF IL-1ß AND PGE2, IN CEREBELLUM WHICH ARE NORMALIZED BY IBUPROFEN IL-1ß PGE2 Control Hyperammon IBU + + RATS WITH PURE CHRONIC HYPERAMMONEMIA SHOW MICROGLIAL ACTIVATION, WHICH IS REVERSED BY IBUPROFEN Control Control Hyperam Hyperam IBU + + Rodrigo, R, Cauli, O, Gomez-Pinedo, U, Agusti, A, Hernandez-Rabaza, V, Garcia-Verdugo, JM and Felipo, V. Gastroenterology (2010) 139:

18 Hyperammonemia per se induces neuroinflammation which contributes to motor alterations in HE LIVER FAILURE HYPERAMMONEMIA Altered modulation of dopamine and glutamate release by mglurs in N. Acc. Altered function of the basal gangliathalamus-cortex circuit Motor alterations in HE 18

19 LIVER FAILURE Hyperammonemia Neuroinflammation? Increased extracellular glutamate in Altered function of the basal gangliathalamus-cortex circuit Hypokinesia in HE MOTOR ACTIVITY MAY BE RESTORED IN RATS WITH HE DUE TO PORTACAVAL SHUNTS BY: a) Antagonists of mglur1 in b) Anti-inflammatories Anti-inflammatories also normalize motor activity in rats with HE due to bile duct ligation and in rats with chronic hyperammonemia 19

20 LABORATORY OF NEUROBIOLOGY 20

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