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Review

An overview of the neuroendocrine system in Parkinson’s disease: what is the impact on diagnosis and treatment?

Pages 127-135 | Received 27 Sep 2019, Accepted 03 Dec 2019, Published online: 12 Dec 2019

References

  • Toni R. The neuroendocrine system: organization and homeostatic role. J Endocrinol Invest. 2004;27(6 Suppl):35–47.
  • Prevot V. Plasticity of neuroendocrine systems. Eur J Neurosci. 2010;32:1987–1988.
  • Smith SM, Vale WW. The role of the hypothalamic-pituitary-adrenal axis in neuroendocrine responses to stress. Dialogues Clin Neurosci. 2006;8:383–395.
  • Farzi A, Fröhlich EE, Holzer P. Gut microbiota and the neuroendocrine system. Neurotherapeutics. 2018;15:5–22.
  • Mayer EA, Knight R, Mazmanian SK, et al. Gut microbes and the brain: paradigm shift in neuroscience. J Neurosci. 2014;34:15490–15496.
  • Galland L. The gut microbiome and the brain. J Med Food. 2014;17:1261–1272.
  • El Aidy S, Dinan TG, Cryan JF. Gut microbiota: the conductor in the orchestra of immune-neuroendocrine communication. Clin Ther. 2015;37:954–967.
  • DeMaagd G, Philip A. Parkinson’s disease and its management: part 1: disease entity, risk factors, pathophysiology, clinical presentation, and diagnosis. Pharm Ther. 2015;40:504–532.
  • Beach TG, Adler CH, Sue LI, et al. Multi-organ distribution of phosphorylated alpha-synuclein histopathology in subjects with Lewy body disorders. Acta Neuropathol. 2010;119:689–702.
  • Gelpi E, Navarro-Otano J, Tolosa E, et al. Multiple organ involvement by alpha-synuclein pathology in Lewy body disorders. Mov Disord. 2014;29:1010–1018.
  • De Pablo-Fernández E, Breen DP, Bouloux PM, et al. Neuroendocrine abnormalities in Parkinson’s disease. J Neurol Neurosurg Psychiatry. 2017;88:176–185.
  • Lionnet A, Leclair-Visonneau L, Neunlist M, et al. Does Parkinson’s disease start in the gut? Acta Neuropathol. 2018;135:1–12.
  • Liddle RA. Parkinson’s disease from the gut. Brain Res. 2018;1693:201–206.
  • Corbillé AG, Letournel F, Kordower JH, et al. Evaluation of alpha-synuclein immunohistochemical methods for the detection of Lewy-type synucleinopathy in gastrointestinal biopsies. Acta Neuropathol Commun. 2016;4:35.
  • Mulak A, Bonaz B. Brain-gut-microbiota axis in Parkinson’s disease. World J Gastroenterol. 2015;21:10609–10620.
  • Felice VD, Quigley EM, Sullivan AM, et al. Microbiota-gut-brain signalling in Parkinson’s disease: implications for non-motor symptoms. Parkinsonism Relat Disord. 2016;27:1–8.
  • Sampson TR, Debelius JW, Thron T, et al. Gut microbiota regulate motor deficits and neuroinflammation in a model of Parkinson’s disease. Cell. 2016;167:1469–1480.
  • Scheperjans F, Aho V, Pereira PA, et al. Gut microbiota are related to Parkinson’s disease and clinical phenotype. Mov Disord. 2015;30:350–358.
  • Keshavarzian A, Green SJ, Engen PA, et al. Colonic bacterial composition in Parkinson’s disease. Mov Disord. 2015;30:1351–1360.
  • Tremlett H, Bauer KC, Appel-Cresswell S, et al. The gut microbiome in human neurological disease: a review. Ann Neurol. 2017;81:369–382.
  • Du X, Pang TY. Is dysregulation of the HPA-axis a core pathophysiology mediating co-morbid depression in neurodegenerative diseases? Front Psychiatry. 2015;6:32.
  • Soares NM, Pereira GM, Altmann V, et al. Cortisol levels, motor, cognitive and behavioral symptoms in Parkinson’s disease: a systematic review. J Neural Transm (Vienna). 2019;126:219–232.
  • De Pablo-Fernandez E, Courtney R, Holton JL, et al. Hypothalamic α-synuclein and its relation to weight loss and autonomic symptoms in Parkinson’s disease. Mov Disord. 2017;32:296–298.
  • Politis M, Piccini P, Pavese N, et al. Evidence of dopamine dysfunction in the hypothalamus of patients with Parkinson’s disease: an in vivo 11C-raclopride PET study. Exp Neurol. 2008;214:112–116.
  • Gorges M, Kuntz B, Del Tredici K, et al. Morphological MRI investigations of the hypothalamus in 232 individuals with Parkinson’s disease. Mov Disord. 2019;34:1566–1570.
  • Cote TE, Felder R, Kebabian JW, et al. D-2 dopamine receptor-mediated inhibition of pro-opiomelanocortin synthesis in rat intermediate lobe. Abolition by pertussis toxin or activators of adenylate cyclase. J Biol Chem. 1986;261:4555–4561.
  • Djamshidian A, Lees AJ. Can stress trigger Parkinson’s disease? J Neurol Neurosurg Psychiatry. 2014;85:878–881.
  • Müller T, Welnic J, Muhlack S. Acute levodopa administration reduces cortisol release in patients with Parkinson’s disease. J Neural Transm. 2007;114:347–350.
  • Ružicka E, Nováková L, Jech R, et al. Decrease in blood cortisol corresponds to weight gain following deep brain stimulation of the subthalamic nucleus in Parkinson’s disease. Stereotact Funct Neurosurg. 2012;90:410–411.
  • Beriwal N, Namgyal T, Sangay P, et al. Role of immune-pineal axis in neurodegenerative diseases, unraveling novel hybrid dark hormone therapies. Heliyon. 2019;5:e01190.
  • Saper CB. The central circadian timing system. Curr Opin Neurobiol. 2013;23:747–751.
  • Breen DP, Nombela C, Vuono R, et al. Hypothalamic volume loss is associated with reduced melatonin output in Parkinson’s disease. Mov Disord. 2016;31:1062–1066.
  • Breen DP, Vuono R, Nawarathna U, et al. Sleep and circadian rhythm regulation in early Parkinson disease. JAMA Neurol. 2014;71:589–595.
  • Willis GL. Parkinson’s disease as a neuroendocrine disorder of circadian function: dopamine-melatonin imbalance and the visual system in the genesis and progression of the degenerative process. Rev Neurosci. 2008;19:245–316.
  • Lax P, Ortuño-Lizarán I, Maneu V, et al. Photosensitive melanopsin-containing retinal ganglion cells in health and disease: implications for circadian rhythms. Int J Mol Sci. 2019;20:13.
  • Joyce DS, Feigl B, Kerr G, et al. Melanopsin-mediated pupil function is impaired in Parkinson’s disease. Sci Rep. 2018;8:7796.
  • Videnovic A, Noble C, Reid KJ, et al. Circadian melatonin rhythm and excessive daytime sleepiness in Parkinson disease. JAMA Neurol. 2014;71:463–469.
  • Bolitho SJ, Naismith SL, Rajaratnam SM, et al. Disturbances in melatonin secretion and circadian sleep-wake regulation in Parkinson disease. Sleep Med. 2014;15:342–347.
  • Mack M, Schamne MG, Sampaio TB, et al. Melatoninergic system in Parkinson’s disease: from neuroprotection to the management of motor and nonmotor symptoms. Oxid Med Cell Longev. 2016;2016:3472032.
  • Seppi K, Weintraub D, Coelho M, et al. The movement disorder society evidence-based medicine review update: treatments for the non-motor symptoms of Parkinson’s disease. Mov Disord. 2011;26(Suppl 3):S42–80.
  • Golden RN, Gaynes BN, Ekstrom RD, et al. The efficacy of light therapy in the treatment of mood disorders: a review and meta-analysis of the evidence. Am J Psychiatry. 2005;162:656–662.
  • Umehara T, Matsuno H, Toyoda C, et al. Thyroid hormone level is associated with motor symptoms in de novo Parkinson’s disease. J Neurol. 2015;262:1762–1768.
  • Wingert TD, Hershman JM. Sinemet and thyroid function in Parkinson’s disease. Neurology. 1979;29:1073–1074.
  • Spiegel J, Hellwig D, Samnick S, et al. Striatal FP-CIT uptake differs in the subtypes of early Parkinson’s disease. J Neural Transm. 2007;114:331–335.
  • Munhoz RP, Teive HA, Troiano AR, et al. Parkinson’s disease and thyroid dysfunction. Parkinsonism Relat Disord. 2004;10:381–383.
  • Garcia-Moreno JM, Chacon J. Hypothyroidism concealed by Parkinson’s disease. Rev Neurol. 2002;35:741–742.
  • Garcia-Moreno JM, Chacon-Pena J. Hypothyroidism and Parkinson’s disease and the issue of diagnostic confusion. Mov Disord. 2003;18:1058–1059.
  • Prakash KM. Hyperthyroidism “masked” the levodopa response in newly diagnosed Parkinson’s disease patients. Parkinsonism Relat Disord. 2010;16:691–692.
  • Kimber J, Watson L, Mathias CJ. Neuroendocrine responses to levodopa in multiple system atrophy (MSA). Mov Disord. 1999;14:981–987.
  • Mannisto P, Mattila J, Kaakkola S. Possible involvement of nigrostriatal dopamine system in the inhibition of thyrotropin secretion in the rat. Eur J Pharmacol. 1981;76:403–409.
  • Gupta A, Haboubi N, Thomas P. Screening for thyroid dysfunction in the elderly. Arch Intern Med. 2001;161:130.
  • Jurado-Coronel JC, Cabezas R, Ávila Rodríguez MF, et al. Sex differences in Parkinson’s disease: features on clinical symptoms, treatment outcome, sexual hormones and genetics. Front Neuroendocrinol. 2018;50:18–30.
  • Schipper HM. The impact of gonadal hormones on the expression of human neurological disorders. Neuroendocrinology. 2016;103:417–431.
  • Labandeira-Garcia JL, Rodriguez-Perez AI, Valenzuela R, et al. Menopause and Parkinson’s disease. Interaction between estrogens and brain renin-angiotensin system in dopaminergic degeneration. Front Neuroendocrinol. 2016;43:44–59.
  • Pavon JM, Whitson H, Okun MS. Parkinson’s disease in women: a call for improved clinical studies and for comparative effectiveness research. Maturitas. 2010;65:352–358.
  • Gillies GE, McArthur S. Estrogen actions in the brain and the basis for differential action in men and women: a case for sex-specific medicines. Pharmacol Rev. 2010;62:155–198.
  • Marras C, Saunders-Pullman R. The complexities of hormonal influences and risk of Parkinson’s disease. Mov Disord. 2014;29:845–848.
  • Liu B, Dluzen DE. Oestrogen and nigrostriatal dopaminergic neurodegeneration: animal models and clinical reports of Parkinson’s disease. Clin Exp Pharmacol Physiol. 2007;34:555–565.
  • Gillies GE, Pienaar IS, Vohra S, et al. Sex differences in Parkinson’s disease. Front Neuroendocrinol. 2014;35:370–384.
  • Gillies GE, Virdee K, McArthur S, et al. Sex-dependent diversity in ventral tegmental dopaminergic neurons and developmental programing: a molecular, cellular and behavioral analysis. Neuroscience. 2014;282:69–85.
  • Chandran S, Krishnan S, Rao RM, et al. Gender influence on selection and outcome of deep brain stimulation for Parkinson’s disease. Ann Indian Acad Neurol. 2014;17:66–70.
  • Litim N, Morissette M, Di Paolo T. Neuroactive gonadal drugs for neuroprotection in male and female models of Parkinson’s disease. Neurosci Biobehav Rev. 2016;67:79–88.
  • Gillies GE, McArthur S. Independent influences of sex steroids of systemic and central origin in a rat model of Parkinson’s disease: a contribution to sex-specific neuroprotection by estrogens. Horm Behav. 2010;57:23–34.
  • Parkinson Study Group POETRY Investigators. A randomized pilot trial of estrogen replacement therapy in post-menopausal women with Parkinson’s disease. Parkinsonism Relat Disord. 2011;17:757e60.
  • Tsang KL, Ho SL, Lo SK. Estrogen improves motor disability in parkinsonian postmenopausal women with motor fluctuations. Neurology. 2000;54:2292e8.
  • Cereda E, Barichella M, Cassani E, et al. Reproductive factors and clinical features of Parkinson’s disease. Parkinsonism Relat Disord. 2013;19:1094–1099.
  • Liu R, Baird D, Park Y, et al. Female reproductive factors, menopausal hormone use, Parkinson’s disease. Mov Disord. 2014;29:889–896.
  • Okun MS, Fernandez HH, Rodriguez RL, et al. Testosterone therapy in men with Parkinson disease: results of the TEST-PD Study. Arch Neurol. 2006;63:729–735.
  • Tenkorang MA, Snyder B, Cunningham RL. Sex-related differences in oxidative stress and neurodegeneration. Steroids. 2018;133:21–27.
  • Solla P, Cannas A, Ibba FC, et al. Gender differences in motor and non-motor symptoms among Sardinian patients with Parkinson’s disease. J Neurol Sci. 2012;323:33–39.
  • Accolla E, Caputo E, Cogiamanian F, et al. Gender differences in patients with Parkinson’s disease treated with subthalamic deep brain stimulation. Mov Disord. 2007;22:1150–1156.
  • Romito LM, Contarino FM, Albanese A. Transient gender-related effects in Parkinson’s disease patients with subthalamic stimulation. J Neurol. 2010;257:603–608.
  • Chandra R, Hiniker A, Kuo YM, et al. α-Synuclein in gut endocrine cells and its implications for Parkinson’s disease. JCI Insight. 2017;2:e92295.
  • Bohórquez DV, Shahid RA, Erdmann A, et al. Neuroepithelial circuit formed by innervation of sensory enteroendocrine cells. J Clin Invest. 2015;125:782–786.
  • Bohórquez DV, Samsa LA, Roholt A, et al. An enteroendocrine cell-enteric glia connection revealed by 3D electron microscopy. PLoS ONE. 2014;9:e89881.
  • Braak H, Rüb U, Gai WP, et al. Idiopathic Parkinson’s disease: possible routes by which vulnerable neuronal types may be subject to neuroinvasion by an unknown pathogen. J Neural Transm (Vienna). 2003;110:517–536.
  • Braak H, Del Tredici K. Neuroanatomy and pathology of sporadic Parkinson’s disease. Adv Anat Embryol Cell Biol. 2009;201:1–119.
  • Hawkes CH, Del Tredici K, Braak H. A timeline for Parkinson’s disease. Parkinsonism Relat Disord. 2010;16:79–84.
  • Bu J, Liu J, Liu K, et al. Diagnostic utility of gut α-synuclein in Parkinson’s disease: a systematic review and meta-analysis. Behav Brain Res. 2019;364:340–347.
  • Svensson E, Horváth-Puhó E, Thomsen RW, et al. Vagotomy and subsequent risk of Parkinson’s disease. Ann Neurol. 2015;78:522–529.
  • Breen DP, Halliday GM, Lang AE. Gut-brain axis and the spread of α-synuclein pathology: vagal highway or dead end? Mov Disord. 2019;34:307–316.
  • Natale G, Pasquali L, Paparelli A, et al. Parallel manifestations of neuropathologies in the enteric and central nervous systems. Neurogastroenterol Motil. 2011;23:1056–1065.
  • Dong D, Xie J, Wang J. Neuroprotective effects of brain-gut peptides: a potential therapy for Parkinson’s disease. Neurosci Bull. 2019;35:1085–1096.
  • Kim DS, Choi HI, Wang Y, et al. A new treatment strategy for Parkinson’s disease through the gut-brain axis: the glucagon-like peptide-1 receptor pathway. Cell Transplant. 2017;261:560–571.
  • Lee S, Lee DY. Glucagon-like peptide-1 and glucagon-like peptide-1 receptor agonists in the treatment of type 2 diabetes. Ann Pediatr Endocrinol Metab. 2017;22:15–26.
  • Athauda D, Foltynie T. Protective effects of the GLP-1mimetic exendin-4 in Parkinson’s disease. Neuropharmacology. 2018;136:260–270.
  • Aviles-Olmos I, Limousin P, Lees A, et al. Parkinson’s disease, insulin resistance and novel agents of neuroprotection. Brain. 2013;136:374–384.
  • Cereda E, Barichella M, Cassani E, et al. Clinical features of Parkinson disease when onset of diabetes came first: a case-control study. Neurology. 2012;78:1507–1511.
  • Giuntini M, Baldacci F, Del Prete E, et al. Diabetes is associated with postural and cognitive domains in Parkinson’s disease. Results from a single-center study. Parkinsonism Relat Disord. 2014;20:671–672.
  • Aksoy D, Solmaz V, Cavusoglu T, et al. Neuroprotective effects of eexenatide in a rotenone-induced rat model of Parkinson’s disease. Am J Med Sci. 2017;354:319–324.
  • Badawi GA, Abd El Fattah MA, Zaki HF, et al. Sitagliptin and liraglutide reversed nigrostriatal degeneration of rodent brain in rotenone-induced Parkinson’s disease. Inflammopharmacology. 2017;25:369–382.
  • Athauda D, Foltynie T. The glucagon-like peptide 1 (GLP) receptor as a therapeutic target in Parkinson’s disease: mechanisms of action. Drug Discov Today. 2016;21:802–818.
  • Aviles-Olmos I, Dickson J, Kefalopoulou Z, et al. Motor and cognitive advantages persist 12 months after exenatide exposure in Parkinson’s disease. J Parkinsons Dis. 2014;4:337–344.
  • Unger MM, Moller JC, Mankel K, et al. Postprandial ghrelin response is reduced in patients with Parkinson’s disease and idiopathic REM sleep behaviour disorder: a peripheral biomarker for early Parkinson’s disease? J Neurol. 2011;258:982–990.
  • Karasawa H, Pietra C, Giuliano C, et al. New ghrelin agonist, HM01 alleviates constipation and L-dopa-delayed gastric emptying in 6-hydroxydopamine rat model of Parkinson’s disease. Neurogastroenterol Motil. 2014;26:1771–1782.
  • Ferreira-Marques M, Aveleira CA, Carmo-Silva S, et al. Caloric restriction stimulates autophagy in rat cortical neurons through neuropeptide Y and ghrelin receptors activation. Aging (Albany NY). 2016;8:1470–1484.
  • Srivastava S, Haigis MC. Role of sirtuins and calorie restriction in neuroprotection: implications in Alzheimer’s and Parkinson’s diseases. Curr Pharm Des. 2011;17:3418–3433.
  • Bayliss JA, Lemus MB, Stark R, et al. Ghrelin-AMPK signaling mediates the neuroprotective effects of calorie restriction in Parkinson’s disease. J Neurosci. 2016;36:3049–3063.
  • Bayliss JA, Lemus M, Santos VV, et al. Acylated but not des-acyl ghrelin is neuroprotective in an MPTP mouse model of Parkinson’s disease. J Neurochem. 2016;137:460–471.
  • Rhee SH, Pothoulakis C, Mayer EA. Principles and clinical implications of the brain-gut-enteric microbiota axis. Nat Rev Gastroenterol Hepatol. 2009;6:306–314.
  • Borre YE, O’Keeffe GW, Clarke G, et al. Microbiota and neurodevelopmental windows: implications for brain disorders. Trends Mol Med. 2014;20:509–518.
  • Mayer EA, Tillisch K, Gupta A. Gut/brain axis and the microbiota. J Clin Invest. 2015;125:926–938.
  • Lyte M. Microbial endocrinology: host-microbiota neuroendocrine interactions influencing brain and behavior. Gut Microbes. 2014;5:381–389.
  • Burcelin R, Cani PD, Knauf C. Glucagon-like peptide-1 and energy homeostasis. J Nutr. 2007;137(11Suppl):2534s–8s.
  • Musso G, Gambino R, Cassader M. Interactions between gut microbiota and host metabolism predisposing to obesity and diabetes. Annu Rev Med. 2011;62:361–380.
  • Sandrini S, Aldriwesh M, Alruways M, et al. Microbial endocrinology: host-bacteria communication within the gut microbiome. J Endocrinol. 2015;225:R21–34.
  • Rahne KE, Tagesson C, Nyholm D. Motor fluctuations and Helicobacter pylori in Parkinson’s disease. J Neurol. 2013;260:2974–2980.
  • Lyte M. Microbial endocrinology as a basis for improved L-DOPA bioavailability in Parkinson’s patients treated for Helicobacter pylori. Med Hypotheses. 2010;74:895–897.
  • Perez-Pardo P, Kliest T, Dodiya HB, et al. The gut-brain axis in Parkinson’s disease: possibilities for food-based therapies. Eur J Pharmacol. 2017;817:86–95.
  • Dutta SK, Verma S, Jain V, et al. Parkinson’s disease: the emerging role of gut dysbiosis, antibiotics, probiotics, and fecal microbiota transplantation. J Neurogastroenterol Motil. 2019;25:363–376.

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