Mechanism and treatment progress of hyperalgesia caused by sleep deprivation_West China Medical Journal

Authors：

LIU Jing , REN Yifeng , LI Mingming ,  ZHENG Xiaozhen

Department of Anesthesia, the First Affiliated Hospital of Henan University, Kaifeng, Henan 475000, P. R. China;

Corresponding author：

ZHENG Xiaozhen, Email: hdyfyxff@163.com

Keywords：

Sleep deprivation; Pain; Hyperalgesia; Treatment

DOI：

10.7507/1002-0179.201911071

Video：

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Abstract Full text Figures/Tables Video References Cited by

Sleep deprivation can cause hyperalgesia, and the mechanisms involve glutamic acid, dopamine, serotonin, metabotropic glutamate receptor subtype 5, adenosine A2A receptor, nicotinic acetylcholine receptor, opioid receptor, brain-derived neurotrophic factor, melatonin, etc. The mechanisms of hyperalgesia caused by sleep deprivation are complex. The current treatment methods are mainly to improve sleep and relieve pain. This paper reviews the mechanism and treatment progress of hyperalgesia induced by sleep deprivation, and aims to provide scientific evidence for the treatment of hyperalgesia caused by sleep deprivation.

Citation： LIU Jing, REN Yifeng, LI Mingming, ZHENG Xiaozhen. Mechanism and treatment progress of hyperalgesia caused by sleep deprivation. West China Medical Journal, 2020, 35(3): 352-356. doi: 10.7507/1002-0179.201911071 Copy

1.	Chen M, Zhang X, Xu H, et al. Inhibitory effect of spinal mGlu(5) receptor antisense oligonucleotide on the up-regulated expression of spinal G protein associated with chronic morphine treatment. Eur J Pharmacol, 2014, 723: 253-258.
2.	Abrams RM. Sleep deprivation. Obstet Gynecol Clin North Am, 2015, 42(3): 493-506.
3.	Finan PH, Goodin BR, Smith MT. The association of sleep and pain: an update and a path forward. J Pain, 2013, 14(12): 1539-1552.
4.	Lautenbacher S, Kundermann B, Krieg JC. Sleep deprivation and pain perception. Sleep Med Rev, 2006, 10(5): 357-369.
5.	Fletcher D, Martinez V. Opioid-induced hyperalgesia in patients after surgery: a systematic review and a meta-analysis. BrJ Anaesth, 2014, 112(6): 991-1004.
6.	Hambrecht-Wiedbusch VS, Gabel M, Liu LJ, et al. Preemptive caffeine administration blocks the increase in postoperative pain caused by previous sleep loss in the rat: a potential role for preoptic adenosine A2A receptors in sleep-pain interactions. Sleep. (2017-08-03)[2020-03-16]. https://academic.oup.com/sleep/article/40/9/zsx116/4037126.
7.	Mayer ML. The challenge of interpreting glutamate-receptor ion-channel structures. Biophys J, 2017, 113(10): 2143-2151.
8.	He S, Zhang X, Qu S. Glutamate, glutamate transporters, and circadian rhythm sleep disorders in neurodegenerative diseases. ACS Chem Neurosci, 2019, 10(1): 175-181.
9.	Woolf CJ, Salter MW. Neuronal plasticity: increasing the gain in pain. Science, 2000, 288(5472): 1765-1769.
10.	Wei H, Zhao W, Wang YX, et al. Pain-related behavior following REM sleep deprivation in the rat: influence of peripheral nerve injury, spinal glutamatergic receptors and nitric oxide. Brain Res, 2007, 1148: 105-112.
11.	Wood PB. Role of central dopamine in pain and analgesia. Expert Rev Neurother, 2008, 8(5): 781-797.
12.	Meyer PJ, Morgan MM, Kozell LB, et al. Contribution of dopamine receptors to periaqueductal gray-mediated antinociception. Psychopharmacology (Berl), 2009, 204(3): 531-540.
13.	Kim JY, Tillu DV, Quinn TL, et al. Spinal dopaminergic projections control the transition to pathological pain plasticity via a D1/D5-mediated mechanism. J Neurosci, 2015, 35(16): 6307-6317.
14.	Tufik S, Andersen ML, Bittencourt LR, et al. Paradoxical sleep deprivation: neurochemical, hormonal and behavioral alterations. Evidence from 30 years of research. An Acad Bras Cienc, 2009, 81(3): 521-538.
15.	Volkow ND, Wang GJ, Telang F, et al. Sleep deprivation decreases binding of [¹¹C]raclopride to dopamine D2/D3 receptors in the human brain. J Neurosci, 2008, 28(34): 8454-8461.
16.	Martins RC, Andersen ML, Garbuio SA, et al. Dopamine transporter regulation during four nights of REM sleep deprivation followed by recovery--an in vivo molecular imaging study in humans. Sleep, 2010, 33(2): 243-251.
17.	Flores JA, El Banoua F, Galán-Rodríguez B, et al. Opiate anti-nociception is attenuated following lesion of large dopamine neurons of the periaqueductal grey: critical role for D1(not D2) dopamine receptors. Pain, 2004, 110(1/2): 205-214.
18.	Skinner GO, Damasceno F, Gomes A, et al. Increased pain perception and attenuated opioid antinociception in paradoxical sleep-deprived rats are associated with reduced tyrosine hydroxylase staining in the periaqueductal gray matter and are reversed by L-dopa. Pharmacol Biochem Behav, 2011, 99(1): 94-99.
19.	Luppi PH, Gervasoni D, Verret L, et al. Paradoxical (REM) sleep genesis: the switch from an aminergic-cholinergic to a GABAergic-glutamatergic hypothesis. J Physiol Paris, 2006, 100(5/6): 271-283.
20.	Ohayon MM. Pain sensitivity, depression, and sleep deprivation: links with serotoninergic dysfunction. J Psychiatr Res, 2009, 43(16): 1243-1245.
21.	Kashiwagi M, Hayashi Y. The function of REM sleep: implications from transgenic mouse models. Brain Nerve, 2016, 68(10): 1205-1211.
22.	王光杰, 顾俊峰, 肖昀. 代谢型谷氨酸受体 5 在周围神经痛大鼠脊髓和背根神经节的表达. 中华实用诊断与治疗杂志, 2019, 33(11): 1049-1052.
23.	Harvey BD, Siok CJ, Kiss T, et al. Neurophysiological signals as potential translatable biomarkers for modulation of metabotropic glutamate 5 receptors. Neuropharmacology, 2013, 75: 19-30.
24.	Oishi Y, Lazarus M. The control of sleep and wakefulness by mesolimbic dopamine systems. Neurosci Res, 2017, 118: 66-73.
25.	Sardi NF, Tobaldini G, Morais RN, et al. Nucleus accumbens mediates the pronociceptive effect of sleep deprivation: the role of adenosine A2A and dopamine D2 receptors. Pain, 2018, 159(1): 75-84.
26.	Porkka-Heiskanen T, Kalinchuk AV. Adenosine, energy metabolism and sleep homeostasis. Sleep Med Rev, 2011, 15(2): 123-135.
27.	Hirotsu C, Pedroni MN, Berro LF, et al. Nicotine and sleep deprivation: impact on pain sensitivity and immune modulation in rats. Sci Rep, 2018, 8(1): 13837.
28.	Brozmanova M, Mazurova L, Ru F, et al. Mechanisms of the adenosine A2A receptor-induced sensitization of esophagealC fibers. Am J Physiol Gastrointest Liver Physiol, 2016, 310(3): G215-G223.
29.	Millan MJ. Descending control of pain. Prog Neurobiol, 2002, 66(6): 355-474.
30.	Umana IC, Daniele CA, Miller BA, et al. Nicotinic modulation of descending pain control circuitry. Pain, 2017, 158(10): 1938-1950.
31.	Sivertsen B, Lallukka T, Petrie KJ, et al. Sleep and pain sensitivity in adults. Pain, 2015, 156(8): 1433-1439.
32.	Bagdas D, Ergun D, Jackson A, et al. Allosteric modulation of α4β2^* nicotinic acetylcholine receptors: desformylflustrabromine potentiates antiallodynic response of nicotine in a mouse model of neuropathic pain. Eur J Pain, 2018, 22(1): 84-93.
33.	Campbell CM, Bounds SC, Kuwabara H, et al. Individual variation in sleep quality and duration is related to cerebral mu opioid receptor binding potential during tonic laboratory pain in healthy subjects. Pain Med, 2013, 14(12): 1882-1892.
34.	Browne CA, Lucki I. Targeting opioid dysregulation in depression for the development of novel therapeutics. Pharmacol Ther, 2019, 201: 51-76.
35.	Nascimento DC, Andersen ML, Hipólide DC, et al. Pain hypersensitivity induced by paradoxical sleep deprivation is not due to altered binding to brain mu-opioid receptors. Behav Brain Res, 2007, 178(2): 216-220.
36.	Célèrier E, Laulin JP, Corcuff JB, et al. Progressive enhancement of delayed hyperalgesia induced by repeated heroin administration:a sensitization process. J Neurosci, 2001, 21(11): 4074-4080.
37.	Tomim DH, Pontarolla FM, Bertolini JF, et al. The pronociceptive effect of paradoxical sleep deprivation in rats: evidence for a role of descending pain modulation mechanisms. Mol Neurobiol, 2016, 53(3): 1706-1717.
38.	Mills EP, Di Pietro F, Alshelh Z, et al. Brainstem pain-control circuitry connectivity in chronic neuropathic pain. J Neurosci, 2018, 38(2): 465-473.
39.	Wan J, Ding Y, Tahir AH, et al. Electroacupuncture attenuates visceral hypersensitivity by inhibiting JAK2/STAT3 signaling pathway in the descending pain modulation system. Front Neurosci, 2017, 11: 644.
40.	Walker SM, Fitzgerald M, Hathway GJ. Surgical injury in the neonatal rat alters the adult pattern of descending modulation from the rostroventral medulla. Anesthesiology, 2015, 122(6): 1391-1400.
41.	Xue J, Li H, Xu Z, et al. Paradoxical sleep deprivation aggravates and prolongs incision-induced pain hypersensitivity via BDNF signaling-mediated descending facilitation in rats. Neurochem Res, 2018, 43(12): 2353-2361.
42.	Garner JM, Chambers J, Barnes AK, et al. Changes in brain-derived neurotrophic factor expression influence sleep-wake activity and homeostatic regulation of rapid eye movement sleep. Sleep, 2018, 41(2): zsx194.
43.	Zisapel N. New perspectives on the role of melatonin in human sleep, circadian rhythms and their regulation. Br J Pharmacol, 2018, 175(16): 3190-3199.
44.	Kaur T, Shyu BC. Melatonin: a new-generation therapy for reducing chronic pain and improving sleep disorder-related pain. Adv Exp Med Biol, 2018, 1099: 229-251.
45.	Huang CT, Chiang RP, Chen CL, et al. Sleep deprivation aggravates median nerve injury-induced neuropathic pain and enhances microglial activation by suppressing melatonin secretion. Sleep, 2014, 37(9): 1513-1523.
46.	Brewster GS, Riegel B, Gehrman PR. Insomnia in the older adult. Sleep Med Clin, 2018, 13(1): 13-19.
47.	Sys J, Van Cleynenbreugel S, Deschodt M, et al. Efficacy and safety of non-benzodiazepine and non-Z-drug hypnotic medication for insomnia in older people: a systematic literature review. Eur J Clin Pharmacol, 2019: 14.
48.	Li S, Zeng J, Wan X, et al. Enhancement of spinal dorsal horn neuron NMDA receptor phosphorylation as the mechanism of remifentanil induced hyperalgesia: roles of PKC and CaMKⅡ. Mol Pain, 2017, 13: 1744806917723789.
49.	Araldi D, Ferrari LF, Lotufo CM, et al. Peripheral inflammatory hyperalgesia depends on the COX increase in the dorsal root ganglion. Proc Natl Acad Sci U S A, 2013, 110(9): 3603-3608.
50.	Weinbroum AA. Postoperative hyperalgesia-a clinically applicable narrative review. Pharmacol Res, 2017, 120: 188-205.

1. Chen M, Zhang X, Xu H, et al. Inhibitory effect of spinal mGlu(5) receptor antisense oligonucleotide on the up-regulated expression of spinal G protein associated with chronic morphine treatment. Eur J Pharmacol, 2014, 723: 253-258.
2. Abrams RM. Sleep deprivation. Obstet Gynecol Clin North Am, 2015, 42(3): 493-506.
3. Finan PH, Goodin BR, Smith MT. The association of sleep and pain: an update and a path forward. J Pain, 2013, 14(12): 1539-1552.
4. Lautenbacher S, Kundermann B, Krieg JC. Sleep deprivation and pain perception. Sleep Med Rev, 2006, 10(5): 357-369.
5. Fletcher D, Martinez V. Opioid-induced hyperalgesia in patients after surgery: a systematic review and a meta-analysis. BrJ Anaesth, 2014, 112(6): 991-1004.
6. Hambrecht-Wiedbusch VS, Gabel M, Liu LJ, et al. Preemptive caffeine administration blocks the increase in postoperative pain caused by previous sleep loss in the rat: a potential role for preoptic adenosine A2A receptors in sleep-pain interactions. Sleep. (2017-08-03)[2020-03-16]. https://academic.oup.com/sleep/article/40/9/zsx116/4037126.
7. Mayer ML. The challenge of interpreting glutamate-receptor ion-channel structures. Biophys J, 2017, 113(10): 2143-2151.
8. He S, Zhang X, Qu S. Glutamate, glutamate transporters, and circadian rhythm sleep disorders in neurodegenerative diseases. ACS Chem Neurosci, 2019, 10(1): 175-181.
9. Woolf CJ, Salter MW. Neuronal plasticity: increasing the gain in pain. Science, 2000, 288(5472): 1765-1769.
10. Wei H, Zhao W, Wang YX, et al. Pain-related behavior following REM sleep deprivation in the rat: influence of peripheral nerve injury, spinal glutamatergic receptors and nitric oxide. Brain Res, 2007, 1148: 105-112.
11. Wood PB. Role of central dopamine in pain and analgesia. Expert Rev Neurother, 2008, 8(5): 781-797.
12. Meyer PJ, Morgan MM, Kozell LB, et al. Contribution of dopamine receptors to periaqueductal gray-mediated antinociception. Psychopharmacology (Berl), 2009, 204(3): 531-540.
13. Kim JY, Tillu DV, Quinn TL, et al. Spinal dopaminergic projections control the transition to pathological pain plasticity via a D1/D5-mediated mechanism. J Neurosci, 2015, 35(16): 6307-6317.
14. Tufik S, Andersen ML, Bittencourt LR, et al. Paradoxical sleep deprivation: neurochemical, hormonal and behavioral alterations. Evidence from 30 years of research. An Acad Bras Cienc, 2009, 81(3): 521-538.
15. Volkow ND, Wang GJ, Telang F, et al. Sleep deprivation decreases binding of [¹¹C]raclopride to dopamine D2/D3 receptors in the human brain. J Neurosci, 2008, 28(34): 8454-8461.
16. Martins RC, Andersen ML, Garbuio SA, et al. Dopamine transporter regulation during four nights of REM sleep deprivation followed by recovery--an in vivo molecular imaging study in humans. Sleep, 2010, 33(2): 243-251.
17. Flores JA, El Banoua F, Galán-Rodríguez B, et al. Opiate anti-nociception is attenuated following lesion of large dopamine neurons of the periaqueductal grey: critical role for D1(not D2) dopamine receptors. Pain, 2004, 110(1/2): 205-214.
18. Skinner GO, Damasceno F, Gomes A, et al. Increased pain perception and attenuated opioid antinociception in paradoxical sleep-deprived rats are associated with reduced tyrosine hydroxylase staining in the periaqueductal gray matter and are reversed by L-dopa. Pharmacol Biochem Behav, 2011, 99(1): 94-99.
19. Luppi PH, Gervasoni D, Verret L, et al. Paradoxical (REM) sleep genesis: the switch from an aminergic-cholinergic to a GABAergic-glutamatergic hypothesis. J Physiol Paris, 2006, 100(5/6): 271-283.
20. Ohayon MM. Pain sensitivity, depression, and sleep deprivation: links with serotoninergic dysfunction. J Psychiatr Res, 2009, 43(16): 1243-1245.
21. Kashiwagi M, Hayashi Y. The function of REM sleep: implications from transgenic mouse models. Brain Nerve, 2016, 68(10): 1205-1211.
22. 王光杰, 顾俊峰, 肖昀. 代谢型谷氨酸受体 5 在周围神经痛大鼠脊髓和背根神经节的表达. 中华实用诊断与治疗杂志, 2019, 33(11): 1049-1052.
23. Harvey BD, Siok CJ, Kiss T, et al. Neurophysiological signals as potential translatable biomarkers for modulation of metabotropic glutamate 5 receptors. Neuropharmacology, 2013, 75: 19-30.
24. Oishi Y, Lazarus M. The control of sleep and wakefulness by mesolimbic dopamine systems. Neurosci Res, 2017, 118: 66-73.
25. Sardi NF, Tobaldini G, Morais RN, et al. Nucleus accumbens mediates the pronociceptive effect of sleep deprivation: the role of adenosine A2A and dopamine D2 receptors. Pain, 2018, 159(1): 75-84.
26. Porkka-Heiskanen T, Kalinchuk AV. Adenosine, energy metabolism and sleep homeostasis. Sleep Med Rev, 2011, 15(2): 123-135.
27. Hirotsu C, Pedroni MN, Berro LF, et al. Nicotine and sleep deprivation: impact on pain sensitivity and immune modulation in rats. Sci Rep, 2018, 8(1): 13837.
28. Brozmanova M, Mazurova L, Ru F, et al. Mechanisms of the adenosine A2A receptor-induced sensitization of esophagealC fibers. Am J Physiol Gastrointest Liver Physiol, 2016, 310(3): G215-G223.
29. Millan MJ. Descending control of pain. Prog Neurobiol, 2002, 66(6): 355-474.
30. Umana IC, Daniele CA, Miller BA, et al. Nicotinic modulation of descending pain control circuitry. Pain, 2017, 158(10): 1938-1950.
31. Sivertsen B, Lallukka T, Petrie KJ, et al. Sleep and pain sensitivity in adults. Pain, 2015, 156(8): 1433-1439.
32. Bagdas D, Ergun D, Jackson A, et al. Allosteric modulation of α4β2^* nicotinic acetylcholine receptors: desformylflustrabromine potentiates antiallodynic response of nicotine in a mouse model of neuropathic pain. Eur J Pain, 2018, 22(1): 84-93.
33. Campbell CM, Bounds SC, Kuwabara H, et al. Individual variation in sleep quality and duration is related to cerebral mu opioid receptor binding potential during tonic laboratory pain in healthy subjects. Pain Med, 2013, 14(12): 1882-1892.
34. Browne CA, Lucki I. Targeting opioid dysregulation in depression for the development of novel therapeutics. Pharmacol Ther, 2019, 201: 51-76.
35. Nascimento DC, Andersen ML, Hipólide DC, et al. Pain hypersensitivity induced by paradoxical sleep deprivation is not due to altered binding to brain mu-opioid receptors. Behav Brain Res, 2007, 178(2): 216-220.
36. Célèrier E, Laulin JP, Corcuff JB, et al. Progressive enhancement of delayed hyperalgesia induced by repeated heroin administration:a sensitization process. J Neurosci, 2001, 21(11): 4074-4080.
37. Tomim DH, Pontarolla FM, Bertolini JF, et al. The pronociceptive effect of paradoxical sleep deprivation in rats: evidence for a role of descending pain modulation mechanisms. Mol Neurobiol, 2016, 53(3): 1706-1717.
38. Mills EP, Di Pietro F, Alshelh Z, et al. Brainstem pain-control circuitry connectivity in chronic neuropathic pain. J Neurosci, 2018, 38(2): 465-473.
39. Wan J, Ding Y, Tahir AH, et al. Electroacupuncture attenuates visceral hypersensitivity by inhibiting JAK2/STAT3 signaling pathway in the descending pain modulation system. Front Neurosci, 2017, 11: 644.
40. Walker SM, Fitzgerald M, Hathway GJ. Surgical injury in the neonatal rat alters the adult pattern of descending modulation from the rostroventral medulla. Anesthesiology, 2015, 122(6): 1391-1400.
41. Xue J, Li H, Xu Z, et al. Paradoxical sleep deprivation aggravates and prolongs incision-induced pain hypersensitivity via BDNF signaling-mediated descending facilitation in rats. Neurochem Res, 2018, 43(12): 2353-2361.
42. Garner JM, Chambers J, Barnes AK, et al. Changes in brain-derived neurotrophic factor expression influence sleep-wake activity and homeostatic regulation of rapid eye movement sleep. Sleep, 2018, 41(2): zsx194.
43. Zisapel N. New perspectives on the role of melatonin in human sleep, circadian rhythms and their regulation. Br J Pharmacol, 2018, 175(16): 3190-3199.
44. Kaur T, Shyu BC. Melatonin: a new-generation therapy for reducing chronic pain and improving sleep disorder-related pain. Adv Exp Med Biol, 2018, 1099: 229-251.
45. Huang CT, Chiang RP, Chen CL, et al. Sleep deprivation aggravates median nerve injury-induced neuropathic pain and enhances microglial activation by suppressing melatonin secretion. Sleep, 2014, 37(9): 1513-1523.
46. Brewster GS, Riegel B, Gehrman PR. Insomnia in the older adult. Sleep Med Clin, 2018, 13(1): 13-19.
47. Sys J, Van Cleynenbreugel S, Deschodt M, et al. Efficacy and safety of non-benzodiazepine and non-Z-drug hypnotic medication for insomnia in older people: a systematic literature review. Eur J Clin Pharmacol, 2019: 14.
48. Li S, Zeng J, Wan X, et al. Enhancement of spinal dorsal horn neuron NMDA receptor phosphorylation as the mechanism of remifentanil induced hyperalgesia: roles of PKC and CaMKⅡ. Mol Pain, 2017, 13: 1744806917723789.
49. Araldi D, Ferrari LF, Lotufo CM, et al. Peripheral inflammatory hyperalgesia depends on the COX increase in the dorsal root ganglion. Proc Natl Acad Sci U S A, 2013, 110(9): 3603-3608.
50. Weinbroum AA. Postoperative hyperalgesia-a clinically applicable narrative review. Pharmacol Res, 2017, 120: 188-205.

West China Medical Journal

Mechanism and treatment progress of hyperalgesia caused by sleep deprivation

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