Application of optogenetics in the study of gastrointestinal motility: A mini review

Song Zhao; Ting Zhang; Weidong Tong

doi:doi:10.1142/S1793545822300130

Journal of Innovative Optical Health Sciences, 2023, 16 (3): 2230013, Published Online: May. 25, 2023

Application of optogenetics in the study of gastrointestinal motility: A mini review

论文大纲

Song Zhao ¹Ting Zhang ²Weidong Tong ^1,*

Author Affiliations

¹ Department of General Surgery, Gastric and Colorectal Surgery Division, Army Medical Center (Daping Hospital), Army Medical University Chongqing, P. R. China

² Department of General Surgery, The 983th Hospital of Joint Logistic Support Force of People’s Liberation Army, Tianjin, P. R. China

Gastrointestinal motility optogenetics

Abstract

Disorders of gastrointestinal (GI) motility are associated with various symptoms such as nausea, vomiting, and constipation. However, the underlying causes of impaired GI motility remain unclear, which has led to variation in the efficacy of therapies to treat GI dysfunction. Optogenetics is a novel approach through which target cells can be precisely controlled by light and has shown great potential in GI motility research. Here, we summarized recent studies of GI motility patterns utilizing optogenetic devices and focused on the ability of opsins, which are genetically expressed in different types of cells in the gut, to regulate the excitability of target cells. We hope that our review of recent findings regarding optogenetic control of GI cells broadens the scope of application for optogenetics in GI motility studies.

References

[1] SandersK. M.,WardS. M.,KohS. D.,“Interstitial cells: Regulators of smooth muscle function,”Physiol. Rev.94(3),859–907(2014).https://doi.org/10.1152/physrev.00037.2013

[2] SandersK. M.,“Spontaneous electrical activity and rhythmicity in gastrointestinal smooth muscles,”Adv. Exp. Med. Biol.1124,3–46(2019).https://doi.org/10.1007/978-981-13-5895-1_1

[3] SchneiderS.,WrightC. M.,HeuckerothR. O.,“Unexpected roles for the second brain: Enteric nervous system as master regulator of bowel function,”Annu. Rev. Physiol.81(1),235–259(2019).https://doi.org/10.1146/annurev-physiol-021317-121515

[4] GulbransenB. D.,“Emerging tools to study enteric neuromuscular function,”Am. J. Physiol. Gastrointest. Liver Physiol.312(5),G420–G426(2017).https://doi.org/10.1152/ajpgi.00049.2017

[5] BassottiG.,VillanacciV.,CretoiuD.,CretoiuS. M.,BecheanuG.,“Cellular and molecular basis of chronic constipation: Taking the functional/idiopathic label out,”World J. Gastroenterol.19(26),4099–4105(2013).https://doi.org/10.3748/wjg.v19.i26.4099

[6] CamilleriM.,FordA. C.,MaweG. M.et al.,“Chronic constipation,”Nat. Rev. Dis. Primers.3,17095(2017).https://doi.org/10.1038/nrdp.2017.95

[7] FurnessJ. B.,“The enteric nervous system and neurogastroenterology,”Nat. Rev. Gastroenterol. Hepatol.9(5),286–294(2012).https://doi.org/10.1038/nrgastro.2012.32

[8] YeH.,FusseneggerM.,“Optogenetic medicine: Synthetic therapeutic solutions precision-guided by light,”Cold Spring Harb Perspect Med.9(9),a034371(2019).https://doi.org/10.1101/cshperspect.a034371

[9] BoesmansW.,HaoM. M.,Vanden BergheP.,“Optogenetic and chemogenetic techniques for neurogastroenterology,”Nat. Rev. Gastroenterol. Hepatol.15(1),21–38(2018).https://doi.org/10.1038/nrgastro.2017.151

[10] MiesenbockG.,“The optogenetic catechism,”Science326(5951),395–399(2009).https://doi.org/10.1126/science.1174520

[11] MontgomeryK. L.,YehA. J.,HoJ. S.et al.,“Wirelessly powered, fully internal optogenetics for brain, spinal and peripheral circuits in mice,”Nat. Meth.12(10),969–974(2015).https://doi.org/10.1038/nmeth.3536

[12] ShinG.,GomezA. M.,Al-HasaniR.et al.,“Flexible near-field wireless optoelectronics as subdermal implants for broad applications in optogenetics,”Neuron93(3),509–521. e3(2017).https://doi.org/10.1016/j.neuron.2016.12.031

[13] RakhilinN.,BarthB.,ChoiJ.et al.,“Simultaneous optical and electrical in vivo analysis of the enteric nervous system,”Nat. Commun.7,11800(2016).https://doi.org/10.1038/ncomms11800

[14] MiesenbockG.,KevrekidisI. G.,“Optical imaging and control of genetically designated neurons in functioning circuits,”Annu. Rev. Neurosci.28,533–563(2005).https://doi.org/10.1146/annurev.neuro.28.051804.101610

[15] NagelG.,SzellasT.,HuhnW.et al.,“Channelrhodopsin-2, a directly light-gated cation-selective membrane channel,”Proc. Natl. Acad. Sci. USA100(24),13940–13945(2003).https://doi.org/10.1073/pnas.1936192100

[16] IshizukaT.,KakudaM.,ArakiR.,YawoH.,“Kinetic evaluation of photosensitivity in genetically engineered neurons expressing green algae light-gated channels,”Neurosci. Res.54(2),85–94(2006).https://doi.org/10.1016/j.neures.2005.10.009

[17] BiA.,CuiJ.,MaY. P.et al.,“Ectopic expression of a microbial-type rhodopsin restores visual responses in mice with photoreceptor degeneration,”Neuron50(1),23–33(2006).https://doi.org/10.1016/j.neuron.2006. 02.026

[18] LiX.,GutierrezD. V.,HansonM. G.et al.,“Fast noninvasive activation and inhibition of neural and network activity by vertebrate rhodopsin and green algae channelrhodopsin,”Proc. Natl. Acad. Sci. USA102(49),17816–17821(2005).https://doi.org/10.1073/pnas.0509030102

[19] BoydenE. S.,ZhangF.,BambergE.,NagelG.,DeisserothK.,“Millisecond-timescale, genetically targeted optical control of neural activity,”Nat. Neurosci.8(9),1263–1268(2005).https://doi.org/10.1038/nn1525

[20] DeisserothK.,FengG.,MajewskaA. K.,MiesenbockG.,TingA.,SchnitzerM. J.,“Next-generation optical technologies for illuminating genetically targeted brain circuits,”J. Neurosci.26(41),10380–10386(2006).https://doi.org/10.1523/JNEUROSCI.3863-06.2006

[21] SandersK. M.,KitoY.,HwangS. J.,WardS. M.,“Regulation of Gastrointestinal smooth muscle function by interstitial cells,”Physiology (Bethesda)31(5),316–326(2016).https://doi.org/10.1152/physiol. 00006.2016

[22] RoS.,ParkC.,JinJ.et al.,“A model to study the phenotypic changes of interstitial cells of Cajal in gastrointestinal diseases,”Gastroenterology138(3),1068–1078 e1-2(2010).https://doi.org/10.1053/j.gastro.2009. 11.007

[23] BrelandA.,HaS. E.,JorgensenB. G.et al.,“Smooth muscle transcriptome browser: Offering genome-wide references and expression profiles of transcripts expressed in intestinal SMC, ICC, and PDGFRalpha(+) cells,”Sci. Rep.9(1),387(2019).https://doi.org/10.1038/s41598-018-36607-6

[24] PeriL. E.,SandersK. M.,Mutafova-YambolievaV. N.,“Differential expression of genes related to purinergic signaling in smooth muscle cells, PDGFRalpha-positive cells, and interstitial cells of Cajal in the murine colon,”Neurogastroenterol. Motil.25(9),e609-20(2013).https://doi.org/10.1111/nmo. 12174

[25] PologrutoT. A.,YasudaR.,SvobodaK.,“Monitoring neural activity and [Ca2+] with genetically encoded Ca2+ indicators,”J. Neurosci.24(43),9572–9579(2004).https://doi.org/10.1523/JNEUROSCI.2854-04.2004

[26] DrummB. T.,HennigG. W.,BakerS. A.,SandersK. M.,“Applications of spatio-temporal mapping and particle analysis techniques to quantify intracellular Ca2+ signaling in situ,”J. Vis. Exp.7(143),10.3791/58989(2019).https://doi.org/10.3791/58989

[27] BakerS. A.,DrummB. T.,SaurD.,HennigG. W.,WardS. M.,SandersK. M.,“Spontaneous Ca(2+) transients in interstitial cells of Cajal located within the deep muscular plexus of the murine small intestine,”J. Physiol.594(12),3317–3338(2016).https://doi.org/10.1113/JP271699

[28] BakerS. A.,LeighW. A.,Del ValleG.et al.,“Ca(2+) signaling driving pacemaker activity in submucosal interstitial cells of Cajal in the murine colon,”Elife10,e64099(2021).https://doi.org/10.7554/eLife.64099

[29] SungT. S.,HwangS. J.,KohS. D.et al.,“The cells and conductance mediating cholinergic neurotransmission in the murine proximal stomach,”J. Physiol.596(9),1549–1574(2018).https://doi.org/10.1113/JP275478

[30] DrummB. T.,SungT. S.,ZhengH.,BakerS. A.,KohS. D.,SandersK. M.,“The effects of mitochondrial inhibitors on Ca(2+) signalling and electrical conductances required for pacemaking in interstitial cells of Cajal in the mouse small intestine,”Cell Calcium72,1–17(2018).https://doi.org/10.1016/j.ceca.2018.01.003

[31] DrummB. T.,HennigG. W.,BattersbyM. J.et al.,“Clustering of Ca(2+) transients in interstitial cells of Cajal defines slow wave duration,”J. Gen. Physiol.149(7),703–725(2017).https://doi.org/10.1085/jgp.201711771

[32] HennigG. W.,GouldT. W.,KohS. D.et al.,“Use of genetically encoded calcium indicators (GECIs) Combined with advanced motion tracking techniques to examine the behavior of neurons and Glia in the enteric nervous system of the intact murine colon,”Front Cell Neurosci.9,436(2015).https://doi.org/10.3389/fncel.2015.00436

[33] MattisJ.,TyeK. M.,FerencziE. A.et al.,“Principles for applying optogenetic tools derived from direct comparative analysis of microbial opsins,”Nat. Meth.9(2),159–172(2011).https://doi.org/10.1038/nmeth.1808

[34] FattahiF.,SteinbeckJ. A.,KriksS.et al.,“Deriving human ENS lineages for cell therapy and drug discovery in Hirschsprung disease,”Nature531(7592),105–109(2016).https://doi.org/10.1038/nature 16951

[35] StampL. A.,GwynneR. M.,FoongJ. P. P.et al.,“Optogenetic demonstration of functional innervation of mouse colon by neurons derived from transplanted neural cells,”Gastroenterology152(6),1407–1418(2017).https://doi.org/10.1053/j.gastro. 2017. 01.005

[36] HibberdT. J.,FengJ.,LuoJ.et al.,“Optogenetic induction of colonic motility in mice,”Gastroenterology155(2),514–528 e6(2018).https://doi.org/10.1053/j.gastro.2018.05.029

[37] NagelG.,BraunerM.,LiewaldJ. F.,AdeishviliN.,BambergE.,GottschalkA.,“Light activation of channelrhodopsin-2 in excitable cells of Caenorhabditis elegans triggers rapid behavioral responses,”Curr. Biol.15(24),2279–2284(2005).https://doi.org/10.1016/j.cub.2005.11.032

[38] SpencerN. J.,TravisL.,HibberdT.,KellyN.,FengJ.,HuH.,“Effects of optogenetic activation of the enteric nervous system on gastrointestinal motility in mouse small intestine,”Auton. Neurosci.229,102733(2020).https://doi.org/10.1016/j.autneu.2020.102733

[39] Perez-MedinaA. L.,GalliganJ. J.,“Optogenetic analysis of neuromuscular transmission in the colon of ChAT-ChR2-YFP BAC transgenic mice,”Am. J. Physiol. Gastrointest. Liver Physiol.317(5),G569–G579(2019).https://doi.org/10.1152/ajpgi.00089.2019

[40] GouldT. W.,SwopeW. A.,HerediaD. J.,CorriganR. D.,SmithT. K.,“Activity within specific enteric neurochemical subtypes is correlated with distinct patterns of gastrointestinal motility in the murine colon,”Am. J. Physiol. Gastrointest. Liver Physiol.317(2),G210–G221(2019).https://doi.org/10.1152/ajpgi.00252.2018

[41] KohS. D.,DrummB. T.,LuH.et al.,“Propulsive colonic contractions are mediated by inhibition-driven poststimulus responses that originate in interstitial cells of Cajal,”Proc. Natl. Acad. Sci. USA119(18),e2123020119(2022).https://doi.org/10.1073/pnas.2123020119

[42] FujiiK.,NakajoK.,EgashiraY.et al.,“Gastrointestinal neurons expressing HCN4 regulate retrograde peristalsis,”Cell Rep.30(9),2879–2888. e3(2020).https://doi.org/10.1016/j.celrep.2020.02.024

[43] Smith-EdwardsK. M.,EdwardsB. S.,WrightC. M.et al.,“Sympathetic input to multiple cell types in mouse and human colon produces region-specific responses,”Gastroenterology160(4),1208–1223.e4(2021).https://doi.org/10.1053/j.gastro.2020.09.030

[44] SandersK. M.,OrdogT.,WardS. M.,“Physiology and pathophysiology of the interstitial cells of Cajal: From bench to bedside. IV. Genetic and animal models of GI motility disorders caused by loss of interstitial cells of Cajal,”Am. J. Physiol. Gastrointest. Liver Physiol.282(5),G747–G756(2022).https://doi.org/10.1152/ajpgi.00362.2001

[45] ViolaM. F.,BoeckxstaensG.,“Intestinal resident macrophages: Multitaskers of the gut,”Neurogastroenterol. Motil32(8),e13843(2020).https://doi.org/10.1111/nmo.13843

[46] LuoJ.,QianA.,OetjenL. K.et al.,“TRPV4 channel signaling in macrophages promotes gastrointestinal motility via direct effects on smooth muscle cells,”Immunity49(1),107–119 e4(2018).https://doi.org/10.1016/j.immuni.2018.04.021

[47] VogtM.,SchulzB.,WagdiA.et al.,“Direct optogenetic stimulation of smooth muscle cells to control gastric contractility,”Theranostics11(11),5569–5584(2021).https://doi.org/10.7150/thno.53883

[48] WagdiA.,MalanD.,SathyanarayananU.et al.,“Selective optogenetic control of Gq signaling using human neuropsin,”Nat. Commun.13(1),1765(2022).https://doi.org/10.1038/s41467-022-29265-w

[49] WangW.,“Optogenetic manipulation of ENS - The brain in the gut,”Life Sci.192,18–25(2018).https://doi.org/10.1016/j.lfs.2017.11.010

[50] ZhangF.,WangL. P.,BraunerM.et al.,“Multimodal fast optical interrogation of neural circuitry,”Nature446(7136),633–639(2007).https://doi.org/10.1038/nature05744

Song Zhao, Ting Zhang, Weidong Tong. Application of optogenetics in the study of gastrointestinal motility: A mini review[J]. Journal of Innovative Optical Health Sciences, 2023, 16(3): 2230013.

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