Charcot - Marie - Tooth type 1A drug therapies: role of adenylyl cyclase activity and G - protein coupled receptors in disease pathomechanism

• Autorzy: Kiepura A.J. , Kochanski A.
• Języki publikacji: EN

Abstrakty

EN

Charcot‑Marie‑Tooth type 1A (CMT1A) is a dysmyelinating disease of the peripheral nervous system that results in a slow progressive weakening and wasting of the distal muscles of the upper and lower limbs. Despite extensive research and clinical trials there is still no treatment for CMT1A that results in complete neurological improvement. Recent studies investigating various pharmacological modulators of adenylyl cyclase activity, including ascorbic acid and ligands of G protein‑coupled receptors (GPCRs), provide hope for future treatments of this type of hereditary motor and sensory neuropathy. A review of mechanisms of action of several compounds tested for CMT1A in pre‑clinical and clinical studies ascorbic acid, onapristone, PXT3003 (baclofen, naltrexone, and sorbitol), and ADX71441, very clearly indicates an important role for adenylyl cyclase activity and GPCRs in the pathomechanism of the disease. Metabotropic γ‑aminobutyric acid receptors (GABABR), subtype mu (µ) opioid receptors (MOR), and muscarinic acetylcholine receptors (mACh) appear to be particularly significant in both pathogenesis and treatment, and their activation may exert a similar and synergistic effect on the physiology of Schwann cells as well as neurons. These receptors participate in proliferation and differentiation of Schwann cells and influence excitatory transmission in neurons. We also hypothesize that onapristone might act through a non‑classical mechanism via membrane progesterone receptor (mPR) and cAMP signaling. This review endeavors to outline a pathway leading inversely from therapy to an indispensable role for adenylyl cyclase activity and GPCRs in the modulation of dosage sensitive peripheral myelin protein (PMP22) gene expression.

• Wydawca: -
• Czasopismo: Acta Neurobiologiae Experimentalis
• Rocznik: 2018
• Tom: 78
• Numer: 3
• Opis fizyczny: p.198-209,fig.,ref.

Twórcy

autor

Kiepura A.J.

• Neuromuscular Unit, Mossakowski Medical Research Centre, Polish Academy of Sciences, Warsaw, Poland

autor

Kochanski A.

• Neuromuscular Unit, Mossakowski Medical Research Centre, Polish Academy of Sciences, Warsaw, Poland

Bibliografia

• Addolorato G, Caputo F, Capristo E, Domenicali  M, Bernardi  M, Janiri  L, Agabio R, Colombo G, Gessa GL, Gasbarrini G (2002) Baclofen efficacy in reducing alcohol craving and intake: a preliminary double‑blind randomized controlled study. Alcohol 37: 504–508.
• Al‑Hasani R and Bruchas MR (2011) Molecular mechanisms of opioid receptor‑dependent signaling and behavior. Anesthesiology 115: 1363–1381.
• Anliker B, Choi JW, Lin ME, Gardell SE, Rivera RR, Kennedy G, Chun J (2013) Lysophosphatidic Acid (LPA) and Its Receptor, LPA1, Influence Embryonic Schwann cell Migration, Myelination, and Cell‑to‑Axon Segregation. Glia 61: 2009–2022.
• Arthur-Farraj P, Wanek K, Hantke J, Davis CM, Jayakar A, Parkinson DB, Mirsky R, Jessen KR (2011) Mouse schwann cells need both NRG1 and cyclic AMP to myelinate. Glia 59: 720–733.
• Attarian S, Vallat JM, Magy  L, Funalot B, Gonnaud PM, Lacour A, Péréon  Y, Dubourg O, Pouget J, Micallef J, Franques J, Lefebvre MN, Ghorab K, Al‑Moussawi  M, Tiffreau  V, Preudhomme  M, Magot A, Leclair‑Visonneau L, Stojkovic T, Bossi L, Lehert P, Gilbert W, Bertrand V, Mandel J, Milet A, Hajj R, Boudiaf  L, Scart‑Grès C, Nabirotchkin S, Guedj M, Chumakov I, Cohen D (2014) An exploratory randomised double‑blind and placebo‑controlled phase 2 study of a combination of baclofen, naltrexone and sorbitol (PXT3003) in patients with Charcot‑Marie‑Tooth disease type 1A. Orphanet J Rare Dis 9: 199.
• Bacallao K., Monje PV (2015) Requirement of cAMP Signalling for Schwann Cell Differentiation Restricts the onset of Myelination. PLoS ONE 10: e0116948.
• Belin S, Kaya F, Burtey S, Fontes M (2010) Ascorbic Acid and Gene Expression: Another example of regulation of gene expression by small molecules. Curr Genom 11: 52–57.
• Chance PF, Alderson MK, Leppig KA, Lensch MW, Matsunami N, Smith B, Swanson PD, Odelberg SJ, Disteche CM, Bird TD (1993) DNA deletion associated with hereditary neuropathy with liability to pressure palsies. Cell 72: 143–151.
• Chernousov MA, Yu WM, Chen ZL, Carey DJ, Strickland S (2008) Regulation of Schwann cell function by the extracellular matrix. Glia 56: 1498–1507.
• Christie MJ and North RA (1988) Agonists at µu‑opioid, M2‑muscarinic and GABAB‑receptors increase the same potassium conductance in rat lateral parabrachial neurons. Br J Pharmacol 95: 896–902.
• Chumakov I, Milet A, Cholet N, Primas G, Boucard A, Pereira Y, Graudens E, Mandel J, Laffaire J, Foucquier J, Gilbert F, Bertrand  V, Nave KA, Sereda  MW, Vial E, Guedj  M, Hajj R, Nabirotchkin S, Cohen D (2014) Polytherapy with a combination of three repurposed drugs (PXT3003) down‑regulates Pmp22 over‑expression and improves myelination, axonal and functional parameters in models of CMT1A neuropathy. Orphanet J Rare Dis 9: 201.
• Clark and Bunge (1989) Cultured Schwann cells assemble normal‑appearing basal lamina only when they ensheathe axons. Dev Biol 133: 393–404.
• Corell  M, Wicher G, Radomska KJ, Daglikoca ED, Godskesen RE, Fredriksson R, Benedikz E, Magnaghi V, Fex Svenningsen A (2015) GABA and its B‑receptor are present at the node of Ranvier in a small population of sensory fibers, implicating a role in myelination. J Neurosci Res 93: 285–295.
• De Jonghe PJL (1998) The inherited neuropathies of the peripheral nervous system in the DNA era: genotype‑phenotype correlations. PhD Thesis, Antwerpen. Désarnaud F, Do Thi AN, Brown AM, Lemke G, Suter U, Baulieu EE, Schumacher  M (1998) Progesterone Stimulates the Activity of the Promoters of Peripheral Myelin Protein‑22 and Protein Zero Genes in Schwann Cells. J Neurochem 71: 1765–1768.
• DiVincenzo C, Elzinga CD, Medeiros AC, Karbassi I, Jones JR, Evans MC, Braastad CD, Bishop CM, Jaremko M, Wang Z, Liaquat K, Hoffman CA, York MD, Batish SD, Lupski JR, Higgins JJ (2014) The allelic spectrum of Charcot‑Marie‑Tooth disease in over 17,000 individuals with neuropathy. Mol Genet Genomic Med 2: 522–529.
• Dyck PJ and Lambert EH (1968) Lower motor and primary sensory neuron diseases with peroneal muscular atrophy. Neurologic, genetic and electrophysiologic findings in hereditary polyneuropathies. Arch Neurol 18: 603–618.
• Dyer T (2013) Addex Announces Positive Data with ADX71441 in a  Pre-Clinical Transgenic Model of Charcot-Marie-Tooth 1A Disease. Addex press release. addextherapeutics.com/en/news-and-events/ press-releases. Dziedzicka‑Wasylewska M, Przewłocki R (1995) The effect of mu and kappa opioid receptor agonists on cAMP level in hippocampus of kainic acid‑treated rats. Pol J Pharmacol 47: 121–126.
• Eglen RM (2006) Muscarinic receptor subtypes in neuronal and non‑neuronal cholinergic function. Auton Autacoid Pharmacol 26: 219–233.
• Ekins S, Litterman NK, Arnold RJG,. Burgess RG, Freundlich JS, Gray SJ, Higgins JJ, Langley B, Willis DE, Notterpek  L, Pleasure D, Sereda MW, Moore A (2015) A brief review of recent Charcot‑Marie‑Tooth research and priorities. F1000Research 4: 53.
• Fields RD, Dutta DJ, Belgrad J, Robnett  M (2017) Cholinergic signaling in myelination. Glia 65: 687–698.
• Fledrich R, Stassart RM, Klink A, Rasch LM, Prukop T, Haag L, Czesnik D, Kungl T, Abdelaal TA, Keric N, Stadelmann C, Brück  W, Nave KA, Sereda MW (2014) Soluble neuregulin‑1 modulates disease pathogenesis in rodent models of Charcot‑Marie‑Tooth disease 1A. Nat Med 20: 105510–105561.
• Gellersen B and Brosens J (2003) Cyclic AMP and progesterone receptor cross‑talk in human endometrium: a decidualizing affair. J Endocrin 178: 357–372.
• Gemignani F and Marbini A (2001) Charcot–Marie–Tooth disease (CMT): distinctive phenotypic and genotypic features in CMT type 2. J Neurol Sci 184: 1–9.
• Gess B, Röhr D, Fledrich R, Sereda MW, Kleffner I, Humberg A, Nowitzki J, Strecker JK, Halfter H, Young P (2011) Sodium-dependent vitamin C transporter 2 deficiency causes hypomyelination and extracellularmatrix defects in the peripheral nervous system. J  Neurosci 31: 17180–17192.
• Guitart X, Thompson MA, Mirante CK, Greenberg ME, Nestler EJ (1992) Regulation of cyclic AMP response element‑binding protein (CREB) phosphorylation by acute and chronic morphine in the rat locus coeruleus. J Neurochem 58: 1168–1171.
• Hantke J, Carty  L, Wagstaff LJ, Turmaine  M, Wilton DK, Quintes S, Koltzenburg  M, Baas F, Mirsky R, Jessen KR (2014) c‑Jun activation in Schwann cells protects against loss of sensory axons in inherited neuropathy. Brain 137: 2922–2937.
• Hudgson P, Weightman D, Cartlidge NE (1972) Clinical trial of baclofen against placebo. Postgrad Med J 48: Suppl 5: 37–40.
• Huxley C, Passage E, Manson A, Putzu G, Figarella‑Branger D, Pellissier J, Fontés M (1996) Construction of a mouse model of Charcot‑Marie‑Tooth disease type 1A by pronuclear injection of human YAC DNA. Hum Mol Genet 5: 563–569.
• Huxley C, Passage E, Robertson AM, Youl B, Huston S, Manson A, Sabéran-Djoniedi D, Figarella-Branger D, Pellissier JF, Thomas PK, Fontés M (1998) Correlation between varying levels of PMP22 expression and the degree of demyelination and reduction in nerve conduction velocity in transgenic mice. Hum Mol Genet 7: 449–455.
• Jung‑Testas I, Do‑Thi A, Koenig H, Desarnaud F, Shazand K, Schumacher M, Baulieu EE (1999) Progesterone as a neurosteroid: synthesis and actions in rat glial cells. J Steroid Biochem Mol Biol 69: 97–107.
• Kalinichev M, Palea S, Haddouk H, Royer-Urios I, Guilloteau V, Lluel P, Schneider M, Saporito M, Poli S (2014) ADX71441, a novel, potent and selective positive allosteric modulator of the GABA(B) receptor, shows efficacy in rodent models of overactive bladder. Br J Pharmacol 171: 995–1006.
• Kalinichev M, Girard F, Haddouk H, Rouillier M, Riguet E, Royer-Urios I, Mutel V, Lütjens R, Poli S (2107) The drug candidate, ADX71441, is a novel, potent and selective positive allosteric modulator of the GABAB receptor with a potential for treatment of anxiety, pain and spasticity. Neuropharmacology 114: 34–47.
• Katona I, Wu X, Feely SM, Sottile S, Siskind CE, Miller LJ, Shy ME, Li J (2009) PMP22 expression in dermal nerve myelin from patients with CMT1A. Brain 132: 1734–1740.
• Kaya F, Belin S, Bourgeois P, Micaleff J, Blin O, Fontés M (2007) Ascorbic acid inhibits PMP22 expression by reducing cAMP levels. Neuromuscul Disord 17: 248–253.
• Kaya F, Belin S, Diamantidis G, Fontes M (2008) Ascorbic acid is a regulator of the intracellular cAMP concentration: Old molecule, new functions? FEBS Lett 582: 3614–3618.
• Kochański A (2008) Perspektywa terapeutyczna w chorobie Charcot‑Marie‑Tooth typu 1A. Therapeutic perspective in Charcot‑Marie‑Tooth type 1A disease. Neurologia Dziecięca 34: 43–47.
• Kuffer A, Lakkaraju AK, Mogha A, Petersen SC, Airich K, Doucerain C, Marpakwar R, Bakirci P, Senatore A, Monnard A, Schiavi C, Nuvolone  M, Grosshans B, Hornemann S, Bassilana F, Monk KR, Aguzzi A (2016) The prion protein is an agonistic ligand of the G protein‑coupled receptor Adgrg6. Nature 536: 464–468.
• Lewis RA, McDermott MP, Herrmann DN, Hoke A, Clawson LL, Siskind C, Feely SM, Miller LJ, Barohn RJ, Smith P, Luebbe E, Wu X, Shy ME, Muscle Study Group (2013) High-dosage ascorbic acid treatment in Charcot-Marie-Tooth disease type 1A: results of a randomized, double-masked, controlled trial. JAMA Neurol 70: 981–987.
• Liu P, Gelowani V, Zhang F, Drory VE, Ben‑Shachar S, Roney E, Medeiros AC, Moore RJ, DiVincenzo C, Burnette WB, Higgins JJ, Li J, Orr‑Urtreger A, Lupski JR (2014) Mechanism, prevalence, and more severe neuropathy phenotype of the Charcot-Marie-Tooth type 1A triplication. Am J Hum Genet 94: 462–469.
• Liu TP, Juang SW, Cheng JT, Tong YC (2005) The role of sorbitol pathway and treatment effect of aldose reductase inhibitor ONO2235 in the up-regulation of cardiac M2-muscarinic receptors in streptozotocin-induced diabetic rats. Neurosci Lett 383: 131–135.
• Loreti S, Vilaró MT, Visentin S, Rees H, Levey AI, Tata AM (2006) Rat Schwann cells express M1–M4 muscarinic receptor subtypes. J Neurosci Res 84: 97–105.
• Lupski JR, de Oca‑Luna RM, Slaugenhaupt S, Pentao L, Guzzetta V, Trask BJ, Saucedo‑Cardenas O, Barker DF, Killian JM, Garcia CA, Chakravarti A, Patel PI (1991) DNA duplication associated with Charcot‑Marie‑Tooth disease type 1A. Cell 66: 219–232.
• Lupski JR, Wise CA, Kuwano A, Pentao L, Parke JT, Glaze DG, Ledbetter DH, Greenberg F, Patel PI (1992) Gene dosage is a  mechanism for Charcot‑Marie‑Tooth disease type 1A. Nat Genet 1: 29–33.
• Magnaghi V, Cavarretta I, Galbiati M, Martini L, Melcangi RC (2001) Neuroactive steroids and peripheral myelin proteins. Brain Res Rev 37: 360–371.
• Magnaghi V, Ballabio M, Cavarretta ITC, Froestl W, Lambert JJ, Zucchi I, Melcangi RC (2004) GABA‑B receptors in Schwann cells influence proliferation and myelin protein expression. Eur J  Neurosci 19: 2641–2649.
• Magnaghi V, Ballabio M, Consoli A, Lambert JJ, Roglio I, Melcangi RC (2006) GABA‑receptor mediated effects in the peripheral nervous system: a cross‑interaction with neuroactive steroids. J Mol Neurosci 28: 89–102.
• Magyar J, Martini R, Ruelicke T, Aguzzi A, Adlkofer K, Dembic Z, Zielasek J, Toyka K, Suter U (1996) Impaired differentiation of Schwann cells in transgenic mice with increased PMP22 gene dosage. J  Neurosci 16: 5351–5360.
• Mannelli P, Gottheil E, Peoples JF, Oropeza VC, Van Bockstaele EJ (2004) Chronic very low dose naltrexone administration attenuates opioid withdrawal expression. Biol Psychiatry 56: 261–268.
• Martini R, Klein D, Groh J (2013) Similarities between inherited demyelinating neuropathies and Wallerian degeneration: an old repair program may cause myelin and axon perturbation under nonlesion conditions. Am J Pathol 83: 655–660.
• Martini R (2014) Neuregulin-1 alleviates Charcot-Marie-Tooth disease in rats. Nat Med 20: 984–985.
• May LT, Leach K, Sexton PM, Christopoulos A (2007) Allosteric Modulation of G Protein–Coupled Receptors. Ann Rev Pharmacol Toxicol 47: 1–5.
• Melcangi RC, Cavarretta I, Ballabio  M, Leonelli E, Schenone A, Azcoitia I, Garcia‑Segura LM, Magnaghi V (2005) Peripheral nerves: a target for the action of neuroactive steroids. Brain Res Rev 48: 328–338.
• Melcangi RC, Magnaghi V, Cavarretta I, Martini L, Piva F (1998) Age induced decrease of glycoprotein Po and myelin basic protein gene expression in the rat sciatic nerve. Repair by steroid derivatives. Neuroscience 85: 569–578.
• Melcangi RC, Magnaghi  V, Cavarretta I, Zucchi I, Bovolin P, D’Urso D, Martini L (1999) Progesterone derivatives are able to influence peripheral myelin protein 22 and Po gene expression: possible mechanisms of action. J Neurosci Res 56: 349–357.
• Meyer zu Horste G, Prukop T, Liebetanz D, Mobius W, Nave KA, Sereda MW (2007) Antiprogesterone therapy uncouples axonal loss from demyelination in a transgenic rat model of CMT1A neuropathy. Ann Neurol 61: 61–72.
• Mogha A, D’Rozario  M, Monk KR (2016) G Protein‑Coupled Receptors in Myelinating Glia. Trends Pharmacol Sci 37: 977–987.
• Monje PV (2015) To myelinate or not to myelinate: fine tuning cAMP signaling in Schwann cells to balance cell proliferation and differentiation. Neural Regen Res 10: 1936–1937.
• Monk KR, Naylor SG, Glenn TD, Mercurio S, Perlin JR, Dominguez C, Moens CB, Talbot WS (2009) A G protein‑coupled receptor is essential for Schwann cells to initiate myelination. Science 325: 1402–1405.
• Monk KR, Oshima K, Jörs S, Heller S, Talbot WS (2011) Gpr126 is essential for peripheral nerve development and myelination in mammals. Development 138: 2673–2680.
• Morris LS, Baek K, Tait R, Elliott R, Ersche KD, Flechais R, McGonigle J, Murphy A, Nestor LJ, Orban C, Passetti F, Paterson LM, Rabiner I, Reed L, Smith D, Suckling J, Taylor EM, Bullmore ET, Lingford‑Hughes AR, Deakin B, Nutt DJ, Sahakian BJ, Robbins TW, Voon V, ICCAM Consortium (2018) Naltrexone ameliorates functional network abnormalities in alcohol‑dependent individuals. Addict Biol 23: 425–436.
• Nicholson GA, Valentijn LJ, Cherryson AK, Kennerson ML, Bragg TL, DeKroon RM, Ross DA, Pollard JD, McLeod, JG, Bolhuis PA, Baas F (1994) A frame shift mutation in the PMP22 gene in hereditary neuropathy with liability to pressure palsies. Nat Genet 6: 263–266.
• Nobbio  L, Visigalli D, Radice D, Fiorina E, Solari A, Lauria G, Reilly MM, Santoro L, Schenone A, Pareyson D (2014) PMP22 messenger RNA levels in skin biopsies: testing the effectiveness of a Charcot‑Marie‑Tooth 1A biomarker. Brain 137: 1614–1620.
• Paavola KJ, Sidik H, Zuchero JB, Eckart M, Talbot WS (2014) Type IV collagen is an activating ligand for the adhesion G protein‑coupled receptor GPR126. Sci Signal 7: ra76.
• Pareyson D, Reilly MM, Schenone A, Fabrizi GM, Cavallaro T, Santoro  L, Vita  G, Quattrone A, Padua  L, Gemignani F, Visioli F, Laurà  M, Radice D, Calabrese D, Hughes RA, Solari A, CMT‑TRIAAL, CMT‑TRAUK groups (2011) Ascorbic acid in Charcot–Marie–Tooth disease type 1A (CMT‑TRIAAL and CMT‑TRAUK): a double‑blind randomized trial. Lancet Neurol 10: 320–328.
• Passage E, Norreel JC, Noack‑Fraissignes P, Sanguedolce  V, Pizant J, Thirion X, Robaglia‑Schlupp A, Pellissier JF, Fontes M (2004) Ascorbic acid treatment corrects the phenotype of a  mouse model of Charcot‑Marie‑Tooth disease. Nat Med 10: 396–401.
• Patel PI, Roa BB, Welcher AA, Schoener‑Scott R, Trask BJ, Pentao  L, Snipes GJ, Garcia CA, Francke U, Shooter EM, Lupski JR, Suter U (1992) The gene for the peripheral myelin protein PMP‑22 is a candidate for Charcot‑Marie‑Tooth disease type 1A. Nat Genet 1: 159–165.
• Petersen SC, Luo R, Liebscher I, Giera S, Jeong SJ, Mogha A, Ghidinelli M, Feltri ML, Schoneberg T, Piao X, Monk KR (2015) The adhesion GPCR GPR126 has distinct, domain‑dependent functions in Schwann cell development mediated by interaction with laminin‑211. Neuron 85: 755–769.
• Raeymaekers P, Timmerman V, Nelis E, De Jonghe P, Hoogenduk JE, Baas F, Barker DF, Martin JJ, De Visser M, Bolhuis PA, Van Broeckhoven C, HMSN Collaborative Research Group (1991) Duplication in chromosome 17p11.2 in Charcot‑Marie‑Tooth neuropathy type 1a (CMT 1a). Neuromusc Disord 1: 93–97.
• Resnick RB, Washton AM, Thomas MA, Kestenbaum RS (1978) Naltrexone in the treatment of opiate dependence. NIDA Res Monogr 19: 321–332.
• Roa BB, Garcia CA, Suter U, Kulpa DA, Wise CA, Mueller J, Welcher AA, Snipes GJ, Shooter EM, Patel PI, Lupski JR (1993) Charcot‑Marie‑Tooth disease type 1A. Association with a spontaneous point mutation in the PMP22 gene. N Engl J Med 329: 96–101.
• Robaglia‑Schlupp A, Pizant J, Norreel JC, Passage E, Saberan‑Djoneidi  D, Ansaldi JL, Vinay  L, Figarella‑Branger D, Levy N, Clarac F, Cau P, Pellissier JF, Fontes M (2002) PMP22 overexpression causes dysmyelination in mice. Brain125: 2213–2221.
• Robertson JF, Willsher PC, Winterbottom L, Blamey RW, Thorpe S (1999) Onapristone, a progesterone receptor antagonist, as first‑line therapy in primary breast cancer. Eur J Cancer 35: 214–218.
• Rosa KA, Gadotti VM, Rosa AO, Rodrigues ALS, Calixto JB, Santos ARS (2005) Evidence for the involvement of glutamatergic system in the antinociceptive effect of ascorbic acid. Neurosci Lett 381: 185–188.
• Russell KR, Potter DE (2001) Biphasic alterations of cAMP levels and inhibition of norepinephrine release in iris-ciliary body by bremazocine. J Pharmacol Exp Ther 298: 941–946.
• Saitoh F, Wakatsuki S, Tokunaga S, Fujieda H, Araki T (2016) Glutamate signals through mGluR2 to control Schwann cell differentiation and proliferation. Scientific Reports 6: 29856.
• Schenone A, Nobbio  L, Mandich P, Bellone E, Abbruzzese  M, Aymar F, Mancardi GL, Windebank AJ (1997) Underexpression of messenger RNA for peripheral myelin protein 22 in hereditary neuropathy with liability to pressure palsies. Neurology 48: 445–449.
• Scherer SS and Wrabetz L (2008) Molecular Mechanisms of Inherited Demyelinating Neuropathies. Glia 56: 1578–1589.
• Sereda M, Griffiths I, Pühlhofer A, Stewart H, Rossner M, Zimmerman F, Magyar J, Schneider A, Hund E, Meinck H, Suter U, Nave K (1996) A  transgenic rat model of Charcot–Marie‑Tooth disease.  Neuron 16: 1049–1060.
• Sereda M, Meyer zu Horste G, Suter U, Uzma N, Nave KA (2003) Therapeutic administration of progesterone antagonist in a model of Charcot‑Marie‑Tooth disease (CMT‑1A). Nat Med 9: 1533–1537.
• Singh M, Su C, and Ng S (2013) Non‑genomic mechanisms of progesterone action in the brain. Front Neurosci 7: 159.
• Sinkiewicz‑Darol E, Lacerda AF, Kostera‑Pruszczyk A, Potulska‑Chromik A, Sokołowska B, Kabzińska D, Brunetti CR, Hausmanowa‑Petrusewicz I, Kochański A (2015) The LITAF/SIMPLE I92V sequence variant results in an earlier age of onset of CMT1A/HNPP diseases. Neurogenetics 16: 27–32.
• Stein C, Lang LJ (2009) Peripheral mechanisms of opioid analgesia. Curr Opin Pharmacol 9: 3–8. Suter U, Nave KA (1999) Transgenic mouse models of CMT1A and HNPP. Ann N Y Acad Sci 883: 247–253.
• Thomas P and Pang Y (2012) Membrane Progesterone Receptors (mPRs): Evidence for Neuroprotective, Neurosteroid Signaling and Neuroendocrine Functions in Neuronal Cells. Neuroendocrinology 96: 162–171.
• Trimarco A, Forese MG, Alfieri  V, Lucente A, Brambilla P, Dina G, Pieragostino D, Sacchetta P, Urade Y, Boizet‑Bonhoure B, Martinelli Boneschi F, Quattrini A, Taveggia C (2014) Prostaglandin D2 synthase/ GPR44: a signaling axis in PNS myelination. Nat Neurosci 17: 1682–1692.
• Uggenti C, De Stefano ME, Costantino  M, Loreti S, Pisano A, Avallone B, Talora C, Magnaghi V, Tata AM (2014) M2 muscarinic receptor activation regulates schwann cell differentiation and myelin organization. Dev Neurobiol 74: 676–691.
• Verhamme C, King RH, ten Asbroek AL, Muddle JR, Nourallah  M, Wolterman R, Baas F, van Schaik IN (2011) Myelin and axon pathology in a long‑term study of PMP22‑overexpressing mice. J Neuropathol Exp Neurol 70: 386–398.
• Vestal‑Laborde AA, Eschenroeder AC, Bigbee JW, Robinson SE, Sato‑Bigbee C (2014) The opioid system and brain development: methadone effects on the oligodendrocyte lineage and the early stages of myelination. Devl Neurosci 36: 409–421.
• Visigalli D, Castagnola P, Capodivento G, Geroldi A, Bellone E, Mancardi G, Pareyson D, Schenone A, Nobbio L (2016) Alternative Splicing in the Human PMP22 Gene: Implications in CMT1A Neuropathy. Hum Mutat 37: 98–109.
• Wake H, Lee PR, Fields RD (2011) Control of local protein synthesis and initial events in myelination by action potentials. Science 333: 1647–1651.
• Wake H, Ortiz FC, Woo DH, Lee PR, Angulo MC, Fields RD (2015) Nonsynaptic junctions on myelinating glia promote preferential myelination of electrically active axons. Nat Commun 6: 7844.
• Warner LE, Roa BB, Lupski JR (1996) Absence of PMP22 coding region mutations in CMT1A duplication patients: further evidence supporting gene dosage as a mechanism for Charcot‑Marie‑Tooth disease type 1A. Hum Mut 8: 362.
• Weterman MA, van RF, de WM, Bordewijk  L, Samijn JP, van der Pol WL, Meggouh F, Baas F (2010) Copy number variation upstream of PMP22 in Charcot‑Marie‑Tooth disease. Eur J Hum Genet 18: 421–428.
• Yoshikawa H, Nishimura T, Nakatsuji Y, Fujimura H, Himoro M, Hayasaka K, Sakoda S, Yanagihara T (1994) Elevated expression of messenger RNA for peripheral myelin protein 22 in biopsied peripheral nerves of patients with Charcot‑Marie‑Tooth disease type 1A. Ann Neurol 35: 445.
• Zhu Y, Rice CD, Pang Y, Pace M, Thomas P (2003a) Cloning, expression, and characterization of a membrane progestin receptor and evidence it is an intermediary in meiotic maturation of fish oocytes. Proc Natl Acad Sci 100: 2231–2236.
• Zhu Y and Thomas P (2003b) Identification, classification, and partial characterization of genes in humans and other vertebrates homologous to a fish membrane progestin receptor Proc Natl Acad Sci 100: 2237–2242.

Identyfikatory

DOI

10.21307/ane‑2018‑018