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Review

The influence of Nav1.9 channels on intestinal hyperpathia and dysmotility

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Article: 2212350 | Received 10 Mar 2023, Accepted 02 May 2023, Published online: 15 May 2023

References

  • Bennett DL, Clark AJ, Huang J, et al. The role of voltage-gated sodium channels in pain signaling. Physiol Rev. 2019 Apr 1;99(2):1079–15.
  • Hockley JR, Winchester WJ, Bulmer DC. The voltage-gated sodium channel NaV 1.9 in visceral pain. Neurogastroenterol Motil. 2016 Mar;28(3):316–326.
  • Coates MD, Vrana KE, Ruiz-Velasco V. The influence of voltage-gated sodium channels on human gastrointestinal nociception. Neurogastroenterol Motil. 2019 Feb;31(2):e13460.
  • Osorio N, Korogod S, Delmas P. Specialized functions of Nav1.5 and Nav1.9 channels in electrogenesis of myenteric neurons in intact mouse ganglia. J Neurosci. 2014 Apr 9;34(15):5233–5244.
  • Dib-Hajj SD, Black JA, Waxman SG. NaV1.9: a sodium channel linked to human pain. Nat Rev Neurosci. 2015 Sep;16(9):511–519.
  • Yang L, Li L, Tang H, et al. Alcohol-aggravated episodic pain in humans with SCN11A mutation and ALDH2 polymorphism. Pain. 2020 Jul;161(7):1470–1482.
  • Bennett DL, Woods CG. Painful and painless channelopathies. Lancet Neurol. 2014 Jun;13(6):587–599.
  • Kabata R, Okuda H, Noguchi A, et al. Familial episodic limb pain in kindreds with novel Nav1.9 mutations. PLoS ONE. 2018;13(12):e0208516. DOI:10.1371/journal.pone.0208516
  • Huang J, Estacion M, Zhao P, et al. A novel gain-of-function Nav1.9 mutation in a child with episodic pain. Front Neurosci. 2019;13:918.
  • King MK, Leipold E, Goehringer JM, et al. Pain insensitivity: distal S6-segment mutations in Na(V)1.9 emerge as critical hotspot. Neurogenetics. 2017 Jul;18(3):179–181.
  • Leipold E, Liebmann L, Korenke GC, et al. A de novo gain-of-function mutation in SCN11A causes loss of pain perception. Nature Genet. 2013 Nov;45(11):1399–1404.
  • Copel C, Clerc N, Osorio N, et al. The Nav1.9 channel regulates colonic motility in mice. Front Neurosci. 2013;7:58.
  • Saha L. Irritable bowel syndrome: pathogenesis, diagnosis, treatment, and evidence-based medicine. World J Gastroenterol. 2014 Jun 14;20(22):6759–6773.
  • Boeckxstaens G, Camilleri M, Sifrim D, et al. Fundamentals of neurogastroenterology: physiology/motility – sensation. Gastroenterology. 2016 Feb 18;150(6):1292–1304.e2.
  • Catterall WA. Forty years of sodium channels: structure, function, pharmacology, and epilepsy. Neurochem Res. 2017 Sep;42(9):2495–2504.
  • Catterall WA, Goldin AL, Waxman SG. International Union of Pharmacology. XLVII. Nomenclature and structure-function relationships of voltage-gated sodium channels. Pharmacol Rev. 2005 Dec;57(4):397–409.
  • Catterall WA, Lenaeus MJ, Gamal El-Din TM. Structure and pharmacology of voltage-gated sodium and calcium channels. Annual review of pharmacology and toxicology. Annu Rev Pharmacol Toxicol. 2020 Jan 6;60(1):133–154.
  • Zeisel A, Hochgerner H, Lönnerberg P, et al. Molecular architecture of the mouse nervous system. Cell. 2018 Aug 9;174(4):999–1014.e22.
  • González-Cano R, Ruiz-Cantero MC, Santos-Caballero M, et al. Tetrodotoxin, a potential drug for neuropathic and cancer pain relief? Toxins (Basel). 2021 Jul 12;13(7). doi :10.3390/toxins13070483.
  • Cummins TR, Dib-Hajj SD, Black JA, et al. A novel persistent tetrodotoxin-resistant sodium current in SNS-null and wild-type small primary sensory neurons. J Neurosci. 1999 Dec 15;19(24):Rc43.
  • Herzog RI, Cummins TR, Waxman SG. Persistent TTX-resistant Na+ current affects resting potential and response to depolarization in simulated spinal sensory neurons. J Neurophysiol. 2001 Sep;86(3):1351–1364.
  • Baker MD, Chandra SY, Ding Y, et al. GTP-induced tetrodotoxin-resistant Na+ current regulates excitability in mouse and rat small diameter sensory neurones. Journal of Physiology. 2003 Apr 15;548(Pt 2):373–382.
  • Wu Y, Ma H, Zhang F, et al. Selective voltage-gated sodium channel peptide toxins from animal venom: pharmacological probes and analgesic drug development. ACS Chem Neurosci. 2018 Feb 21;9(2):187–197.
  • Lin Z, Santos S, Padilla K, et al. Biophysical and pharmacological characterization of Nav1.9 voltage dependent sodium channels stably expressed in HEK-293 cells. PLoS ONE. 2016;11(8):e0161450. DOI:10.1371/journal.pone.0161450
  • Vanoye CG, Kunic JD, Ehring GR, et al. Mechanism of sodium channel NaV1.9 potentiation by G-protein signaling. J General Physiol. 2013 Feb;141(2):193–202.
  • Peng S, Chen M, Xiao Z, et al. A novel spider toxin inhibits fast inactivation of the Na(v)1.9 channel by binding to domain iii and domain iv voltage sensors. Front Pharmacol. 2021;12:778534.
  • Zhou X, Ma T, Yang L, et al. Spider venom-derived peptide induces hyperalgesia in Na(v)1.7 knockout mice by activating Na(v)1.9 channels. Nat Commun. 2020 May 8;11(1):2293.
  • Wang G, Long C, Liu W, et al. Novel sodium channel inhibitor from leeches. Front Pharmacol. 2018;9:186.
  • McMahon KL, Tay B, Deuis JR, et al. Pharmacological activity and NMR solution structure of the leech peptide HSTX-I. Biochem Pharmacol. 2020 Nov;181:114082.
  • Berta T, Qadri Y, Tan PH, et al. Targeting dorsal root ganglia and primary sensory neurons for the treatment of chronic pain. Expert Opin Ther Targets. 2017 Jul;21(7):695–703.
  • Dib-Hajj SD, Tyrrell L, Cummins TR, et al. Two tetrodotoxin-resistant sodium channels in human dorsal root ganglion neurons. FEBS Lett. 1999 Nov 26;462(1–2):117–120.
  • Benn SC, Costigan M, Tate S, et al. Developmental expression of the TTX-resistant voltage-gated sodium channels Nav1.8 (SNS) and Nav1.9 (SNS2) in primary sensory neurons. J Neurosci. 2001 Aug 15;21(16):6077–6085.
  • Fang X, Djouhri L, Black JA, et al. The presence and role of the tetrodotoxin-resistant sodium channel Na(v)1.9 (NaN) in nociceptive primary afferent neurons. J Neurosci. 2002 Sep 1;22(17):7425–7433.
  • Dib-Hajj SD, Tyrrell L, Escayg A, et al. Coding sequence, genomic organization, and conserved chromosomal localization of the mouse gene Scn11a encoding the sodium channel NaN. Genomics. 1999 Aug 1;59(3):309–318.
  • Dib-Hajj S, Black JA, Cummins TR, et al. NaN/Nav1.9: a sodium channel with unique properties. Trends Neurosci. 2002 May;25(5):253–259.
  • Priest BT, Murphy BA, Lindia JA, et al. Contribution of the tetrodotoxin-resistant voltage-gated sodium channel NaV1.9 to sensory transmission and nociceptive behavior. Proc Natl Acad Sci USA. 2005 Jun 28;102(26):9382–9387.
  • Maingret F, Coste B, Padilla F, et al. Inflammatory mediators increase Nav1.9 current and excitability in nociceptors through a coincident detection mechanism. J General Physiol. 2008 Mar;131(3):211–225.
  • Amsalem M, Poilbout C, Ferracci G, et al. Membrane cholesterol depletion as a trigger of Nav1.9 channel-mediated inflammatory pain. Embo J. 2018 Apr 13;37(8). doi :10.15252/embj.201797349.
  • Yu YQ, Zhao F, Guan SM, et al. Antisense-mediated knockdown of Na(V)1.8, but not Na(V)1.9, generates inhibitory effects on complete Freund’s adjuvant-induced inflammatory pain in rat. PLoS ONE. 2011 May 10;6(5):e19865.
  • Fertleman CR, Ferrie CD, Aicardi J, et al. Paroxysmal extreme pain disorder (previously familial rectal pain syndrome). Neurology. 2007 Aug 7;69(6):586–595.
  • Okuda H, Noguchi A, Kobayashi H, et al. Infantile Pain episodes associated with novel Nav1.9 mutations in familial episodic pain syndrome in japanese families. PLoS ONE. 2016;11(5):e0154827. DOI:10.1371/journal.pone.0154827
  • Zhang XY, Wen J, Yang W, et al. Gain-of-function mutations in SCN11A cause familial episodic pain. Am J Hum Genet. 2013 Nov 7;93(5):957–966.
  • Ginanneschi F, Rubegni A, Moro F, et al. SCN11A variant as possible pain generator in sensory axonal neuropathy. Neurol Sci. 2019 Jun;40(6):1295–1297.
  • Sambuughin N, Ren M, Capacchione JF, et al. Multifactorial origin of exertional rhabdomyolysis, recurrent hematuria, and episodic pain in a service member with sickle cell trait. Case Rep Genet. 2018;2018:6898546.
  • Huang J, Han C, Estacion M, et al. Gain-of-function mutations in sodium channel Na(v)1.9 in painful neuropathy. Brain. 2014 Jun;137(Pt 6):1627–1642.
  • Han C, Yang Y, de Greef BT, et al. The domain II S4-S5 linker in Nav1.9: a missense mutation enhances activation, impairs fast inactivation, and produces human painful neuropathy. Neuromolecular Med. 2015 Jun;17(2):158–169.
  • Kleggetveit IP, Schmidt R, Namer B, et al. Pathological nociceptors in two patients with erythromelalgia-like symptoms and rare genetic Nav 1.9 variants. Brain Behav. 2016 Oct;6(10):e00528.
  • Eijkenboom I, Sopacua M, Hoeijmakers JGJ, et al. Yield of peripheral sodium channels gene screening in pure small fibre neuropathy. J Neurol Neurosurg Psychiatry. 2019 Mar;90(3):342–352.
  • Wadhawan S, Pant S, Golhar R, et al. Na(v) channel variants in patients with painful and nonpainful peripheral neuropathy. Neurol Genet. 2017 Dec;3(6):e207.
  • Zhou L. Small fiber neuropathy. Semin Neurol. 2019 Oct;39(5):570–577.
  • Cazzato D, Lauria G. Small fibre neuropathy. Curr Opin Neurol. 2017 Oct;30(5):490–499.
  • Schon KR, Parker APJ, Woods CG. Congenital Insensitivity to Pain Overview. In: Adam M, Ardinger H, and Pagon R, et al., editors. GeneReviews(®). Seattle (WA): University of Washington, Seattle, Copyright © 1993-2023.2018; NBK481553 .
  • Poojary S, Jaiswal S, Shah KS, et al. Sisters with no pain, no tears: a report of a new variant of hereditary sensory and autonomic neuropathy (Type IX) caused by a novel SCN11A mutation. Indian J Dermatol. 2020 Jul-Aug;65(4):299–303.
  • Phatarakijnirund V, Mumm S, McAlister WH, et al. Congenital insensitivity to pain: fracturing without apparent skeletal pathobiology caused by an autosomal dominant, second mutation in SCN11A encoding voltage-gated sodium channel 1.9. Bone. 2016 Mar;84:289–298.
  • Huang J, Vanoye CG, Cutts A, et al. Sodium channel NaV1.9 mutations associated with insensitivity to pain dampen neuronal excitability. J Clin Investig. 2017 Jun 30;127(7):2805–2814.
  • Hockley JR, Boundouki G, Cibert-Goton V, et al. Multiple roles for NaV1.9 in the activation of visceral afferents by noxious inflammatory, mechanical, and human disease-derived stimuli. Pain. 2014 Oct;155(10):1962–1975.
  • Martinez V, Melgar S. Lack of colonic-inflammation-induced acute visceral hypersensitivity to colorectal distension in Na(v)1.9 knockout mice. Eur J Pain. 2008 Oct;12(7):934–944.
  • Vanner S, Greenwood-Van Meerveld B, Mawe G, et al. Fundamentals of Neurogastroenterology: basic Science. Gastroenterology. 2016 Feb 18;150(6):1280–1291.
  • Zhao C, Jin J, Hu H, et al. The gain-of-function R222S variant in Scn11a contributes to visceral hyperalgesia and intestinal dysmotility in Scn11aR222S/R222S Mice. Front Neurol. 2022;13:856459.
  • Spencer NJ, Hu H. Enteric nervous system: sensory transduction, neural circuits and gastrointestinal motility. Nat Rev Gastroenterol Hepatol. 2020 Jun;17(6):338–351.
  • Spencer NJ, Kyloh MA, Travis L, et al. Sensory nerve endings arising from single spinal afferent neurons that innervate both circular muscle and myenteric ganglia in mouse colon: colon-brain axis. Cell Tissue Res. 2020 Jul;381(1):25–34.
  • Herrity AN, Rau KK, Petruska JC, et al. Identification of bladder and colon afferents in the nodose ganglia of male rats. J Comp Neurol. 2014 Nov 1;522(16):3667–3682.
  • Erickson A, Deiteren A, Harrington AM, et al. Voltage-gated sodium channels: (Na(v))igating the field to determine their contribution to visceral nociception. Journal of Physiology. 2018 Mar 1;596(5):785–807.
  • Brierley SM, Hughes PA, Harrington AM, et al. Identifying the ion channels responsible for signaling gastro-intestinal based pain. pharmaceuticals. (Basel, Switzerland). 2010Aug26; 3(9): 2768–2798. 10.3390/ph3092768
  • Beyak MJ, Ramji N, Krol KM, et al. Two TTX-resistant Na+ currents in mouse colonic dorsal root ganglia neurons and their role in colitis-induced hyperexcitability. Am J Physiol Gastrointest Liver Physiol. 2004 Oct;287(4):G845–55.
  • Usoskin D, Furlan A, Islam S, et al. Unbiased classification of sensory neuron types by large-scale single-cell RNA sequencing. Nat Neurosci. 2015 Jan;18(1):145–153.
  • Li JH, Duan R, Li L, et al. Unique characteristics of “the second brain” - the enteric nervous system. Sheng Li Xue Bao. 2020 Jun 25;72(3):382–390.
  • Fung C, Vanden Berghe P. Functional circuits and signal processing in the enteric nervous system. Cellular and molecular life sciences: cMLS. Nov. 2020;77(22):4505–4522. DOI:10.1007/s00018-020-03543-6
  • Costa M, Furness JB. The peristaltic reflex: an analysis of the nerve pathways and their pharmacology. Naunyn-Schmiedeberg’s Arch Pharmacol. 1976 Jul;294(1):47–60.
  • Brehmer A, Schrodl F, Neuhuber W. Morphological classifications of enteric neurons–100 years after Dogiel. Anatomy and Embryology. 1999 Aug;200(2):125–135.
  • Costa M, Spencer NJ, Brookes SJH. The role of enteric inhibitory neurons in intestinal motility. Autonomic neuroscience: basic & clinical. Auton Neurosci. 2021 Nov;235:102854.
  • Hirst GD, Holman ME, Spence I. Two types of neurones in the myenteric plexus of duodenum in the guinea-pig. Journal of Physiology. 1974 Jan;236(2):303–326.
  • Bertrand PP, Kunze WA, Bornstein JC, et al. Electrical mapping of the projections of intrinsic primary afferent neurones to the mucosa of the guinea-pig small intestine. Neurogastroenterol Motil. 1998 Dec;10(6):533–541.
  • Bertrand PP, Thomas EA. Multiple levels of sensory integration in the intrinsic sensory neurons of the enteric nervous system. Clin Exp Pharmacol. 2004 Nov;31(11):745–755.
  • Spencer NJ, Smith TK. Mechanosensory S-neurons rather than AH-neurons appear to generate a rhythmic motor pattern in guinea-pig distal colon. Journal of Physiology. 2004 Jul 15;558(Pt 2):577–596.
  • Mazzuoli G, Schemann M. Multifunctional rapidly adapting mechanosensitive enteric neurons (RAMEN) in the myenteric plexus of the guinea pig ileum. Journal of Physiology. 2009 Oct 1;587(Pt 19):4681–4694.
  • O’Donnell AM, Coyle D, Puri P. Decreased Nav1.9 channel expression in Hirschsprung’s disease. J Pediatr Surg. 2016 Sep;51(9):1458–1461.
  • Copel C, Osorio N, Crest M, et al. Activation of neurokinin 3 receptor increases Na(v)1.9 current in enteric neurons. Journal of Physiology. 2009 Apr 1;587(Pt 7):1461–1479.
  • Gwynne RM, Bornstein JC. Mechanisms underlying nutrient-induced segmentation in isolated guinea pig small intestine. Am J Physiol Gastrointest Liver Physiol. 2007 Apr;292(4):G1162–72.
  • Gwynne RM, Thomas EA, Goh SM, et al. Segmentation induced by intraluminal fatty acid in isolated guinea-pig duodenum and jejunum. Journal of Physiology. 2004 Apr 15;556(Pt 2):557–569.
  • Costa M, Dodds KN, Wiklendt L, et al. Neurogenic and myogenic motor activity in the colon of the guinea pig, mouse, rabbit, and rat. Am J Physiol Gastrointest Liver Physiol. 2013 Nov 15;305(10):G749–59.
  • Spencer NJ, Nicholas SJ, Robinson L, et al. Mechanisms underlying distension-evoked peristalsis in guinea pig distal colon: is there a role for enterochromaffin cells? Am J Physiol Gastrointest Liver Physiol. 2011 Sep;301(3):G519–27.
  • Spencer NJ, Dinning PG, Brookes SJ, et al. Insights into the mechanisms underlying colonic motor patterns. Journal of Physiology. 2016 Aug 1;594(15):4099–4116.
  • Bornstein JC, Costa M, Grider JR. Enteric motor and interneuronal circuits controlling motility. Neurogastroenterol Motil. 2004 Apr;16(Suppl 1):34–38.
  • Hansen MB. The enteric nervous system II: gastrointestinal functions. Pharmacol Toxicol. 2003 Jun;92(6):249–257.
  • Wehrwein EA, Orer HS, Barman SM. Overview of the anatomy, physiology, and pharmacology of the autonomic nervous system. Compr Physiol. 2016 Jun 13;6(3):1239–1278.
  • Furness JB. Novel gut afferents: intrinsic afferent neurons and intestinofugal neurons. Autonomic neuroscience: basic & clinical. 2006 Apr 30;125(1–2):81–85. DOI: 10.1016/j.autneu.2006.01.007
  • Linden DR. Enhanced excitability of guinea pig inferior mesenteric ganglion neurons during and following recovery from chemical colitis. Am J Physiol Gastrointest Liver Physiol. 2012 Nov 1;303(9):G1067–75.
  • Linden DR. Colitis is associated with a loss of intestinofugal neurons. Am J Physiol Gastrointest Liver Physiol. 2012 Nov 15;303(10):G1096–104.
  • Furness JB. Intestinofugal neurons and sympathetic reflexes that bypass the central nervous system. J Comp Neurol. 2003 Jan 13;455(3):281–284.
  • Bywater RA. Activity following colonic distension in enteric sensory fibres projecting to the inferior mesenteric ganglion in the guinea pig. J Auton Nerv Syst. 1994 Jan-Feb;46(1–2):19–26.
  • Miller SM, Szurszewski JH. Colonic mechanosensory afferent input to neurons in the mouse superior mesenteric ganglion. Am J Physiol. 1997 Feb;272(2 Pt 1):G357–66.
  • Kreulen DL, Szurszewski JH. Reflex pathways in the abdominal prevertebral ganglia: evidence for a colo-colonic inhibitory reflex. Journal of Physiology. 1979 Oct;295:21–32.
  • Hetz S, Acikgoez A, Moll C, et al. Age-related gene expression analysis in enteric ganglia of human colon after laser microdissection. Front Aging Neurosci. 2014;6:276.
  • Ebbinghaus M, Tuchscherr L, Segond von Banchet G, et al. Gain-of-function mutation in SCN11A causes itch and affects neurogenic inflammation and muscle function in Scn11a+/L799P mice. PLoS ONE. 2020;15(8):e0237101. DOI:10.1371/journal.pone.0237101
  • Mawe GM. Colitis-induced neuroplasticity disrupts motility in the inflamed and post-inflamed colon. J Clin Investig. 2015 Mar 2;125(3):949–955.
  • Farzaei MH, Bahramsoltani R, Abdollahi M, et al. The role of visceral hypersensitivity in irritable bowel syndrome: pharmacological targets and novel treatments. J Neurogastroenterol Motil. 2016 Oct 30;22(4):558–574.
  • Mearin F, Lacy BE, Chang L, et al. Bowel Disorders. Gastroenterology. 2016 Feb 18;150:1393-1407.
  • Gwee KA, Lu CL, Ghoshal UC. Epidemiology of irritable bowel syndrome in Asia: something old, something new, something borrowed. J Gastroenterol Hepatol. 2009 Oct;24(10):1601–1607.
  • Liu L, Liu BN, Chen S, et al. Visceral and somatic hypersensitivity, autonomic cardiovascular dysfunction and low-grade inflammation in a subset of irritable bowel syndrome patients. J Zhejiang Univ Sci B. 2014 Oct;15(10):907–914.
  • DuPont AW, Jiang ZD, Harold SA, et al. Motility abnormalities in irritable bowel syndrome. Digestion. 2014;89(2):119–123. DOI:10.1159/000356314
  • Park JH, Baek YH, Park DI, et al. Analysis of rectal dynamic and static compliances in patients with irritable bowel syndrome. Int J Colorectal Dis. 2008 Jul;23(7):659–664.
  • Fassov J, Lundby L, Worsøe J, et al. A randomised, controlled study of small intestinal motility in patients treated with sacral nerve stimulation for irritable bowel syndrome. BMC Gastroenterol. 2014 Jun 25;14:111.
  • Berumen A, Edwinson AL, Grover M. Post-infection Irritable Bowel Syndrome. Gastroenterol Clin North Am. 2021 Jun;50(2):445–461.
  • Barbara G, Grover M, Bercik P, et al. Rome foundation working team report on post-infection irritable bowel syndrome. Gastroenterology. 2019 Jan;156(1):46–58.e7.
  • Sinagra E, Pompei G, Tomasello G, et al. Inflammation in irritable bowel syndrome: myth or new treatment target? World J Gastroenterol. 2016 Feb 21;22(7):2242–2255.
  • Lolignier S, Amsalem M, Maingret F, et al. Nav1.9 channel contributes to mechanical and heat pain hypersensitivity induced by subacute and chronic inflammation. PLoS ONE. 2011;6(8):e23083. DOI:10.1371/journal.pone.0023083