Dolor crónico visceral y estrés

REFERENCES

Ackerman, A. L., Jellison, F. C., Lee, U. J., Bradesi, S., and Rodriguez, L. V. (2016). The Glt1 glutamate receptor mediates the establishment and perpetuation of chronic visceral pain in an animal model of stress-induced bladder hyperalgesia. Am. J. Physiol. Renal Physiol. 310, F628–F636. doi: 10.1152/ajprenal.00297.2015
 

Adeyemo, M. A., Spiegel, B. M., and Chang, L. (2010). Meta-analysis: do irritable bowel syndrome symptoms vary between men and women? Aliment. Pharmacol. Ther. 32, 738–755. doi: 10.1111/j.1365-2036.2010.04409.x Frontiers in Systems Neuroscience | www.frontiersin.org 16 November 2017 | Volume 11 | Article 86 Greenwood-Van Meerveld and Johnson Stress-Induced Visceral Pain

Agostini, S., Eutamene, H., Broccardo, M., Improta, G., Petrella, C., Theodorou, V., et al. (2009). Peripheral anti-nociceptive effect of nociceptin/orphanin FQ in inflammation and stress-induced colonic hyperalgesia in rats. Pain 141, 292–299. doi: 10.1016/j.pain.2008.12.007

Agostini, S., Goubern, M., Tondereau, V., Salvador-Cartier, C., Bezirard, V., Leveque, M., et al. (2012). A marketed fermented dairy product containing Bifidobacterium lactis CNCM I-2494 suppresses gut hypersensitivity and colonic barrier disruption induced by acute stress in rats. Neurogastroenterol. Motil. 24, 376–e172. doi: 10.1111/j.1365-2982.2011.01865.x

Aguilera, M., Vergara, P., and Martinez, V. (2013). Stress and antibiotics alter luminal and wall-adhered microbiota and enhance the local expression of visceral sensory-related systems in mice. Neurogastroenterol. Motil. 25, e515–e529. doi: 10.1111/nmo.12154

Aguirre, J. E., Winston, J. H., and Sarna, S. K. (2017). Neonatal immune challenge followed by adult immune challenge induces epigenetic-susceptibility to aggravated visceral hypersensitivity. Neurogastroenterol. Motil. 29:e13081. doi: 10.1111/nmo.13081

Ait-Belgnaoui, A., Bradesi, S., Fioramonti, J., Theodorou, V., and Bueno, L. (2005). Acute stress-induced hypersensitivity to colonic distension depends upon increase in paracellular permeability: role of myosin light chain kinase. Pain 113, 141–147. doi: 10.1016/j.pain.2004.10.002

Ait-Belgnaoui, A., Han, W., Lamine, F., Eutamene, H., Fioramonti, J., Bueno, L., et al. (2006). Lactobacillus farciminis treatment suppresses stress induced visceral hypersensitivity: a possible action through interaction with epithelial cell cytoskeleton contraction. Gut 55, 1090–1094. doi: 10.1136/gut.2005.084194

Alexander, S. P., Cidlowski, J. A., Kelly, E., Marrion, N., Peters, J. A., Benson, H. E., et al. (2015a). The concise guide to PHARMACOLOGY 2015/16: nuclear hormone receptors. Br. J. Pharmacol. 172, 5956–5978. doi: 10.1111/bph.13352

Alexander, S. P., Davenport, A. P., Kelly, E., Marrion, N., Peters, J. A., Benson, H. E., et al. (2015b). The concise guide to PHARMACOLOGY 2015/16: G proteincoupled receptors. Br. J. Pharmacol. 172, 5744–5869. doi: 10.1111/bph.13348

Alexander, S. P., Kelly, E., Marrion, N., Peters, J. A., Benson, H. E., Faccenda, E., et al. (2015c). The concise guide to PHARMACOLOGY 2015/16: transporters. Br. J. Pharmacol. 172, 6110–6202. doi: 10.1111/bph.13355

Alexander, S. P., Peters, J. A., Kelly, E., Marrion, N., Benson, H. E., Faccenda, E., et al. (2015d). The concise guide to PHARMACOLOGY 2015/16: ligand-gated ion channels. Br. J. Pharmacol. 172, 5870–5903. doi: 10.1111/bph.13350

Almeida, T. F., Roizenblatt, S., and Tufik, S. (2004). Afferent pain pathways: a neuroanatomical review. Brain Res. 1000, 40–56. doi: 10.1016/j.brainres.2003.10.073

Aloisi, A. M., and Bonifazi, M. (2006). Sex hormones, central nervous system and pain. Horm. Behav. 50, 1–7. doi: 10.1016/j.yhbeh.2005.12.002

Aloisi, A. M., and Ceccarelli, I. (2000). Role of gonadal hormones in formalin-induced pain responses of male rats: modulation by estradiol and naloxone administration. Neuroscience 95, 559–566. doi: 10.1016/S0306-4522(99)00445-5

Anda, R. F., Felitti, V. J., Bremner, J. D., Walker, J. D., Whitfield, C., Perry, B. D., et al. (2006). The enduring effects of abuse and related adverse experiences in childhood. A convergence of evidence from neurobiology and epidemiology. Eur. Arch. Psychiatry Clin. Neurosci. 256, 174–186. doi: 10.1007/s00406-005-0624-4

Annaházi, A., Dabek, M., Gecse, K., Salvador-Cartier, C., Polizzi, A., Rosztoczy, A., et al. (2012). Proteinase-activated receptor-4 evoked colorectal analgesia in mice: an endogenously activated feed-back loop in visceral inflammatory pain. Neurogastroenterol. Motil. 24, 76–85, e13. doi: 10.1111/j.1365-2982.2011.01805.x

Arroyo-Novoa, C. M., Figueroa-Ramos, M. I., Miaskowski, C., Padilla, G., Stotts, N., and Puntillo, K. A. (2009). Acute wound pain: gaining a better understanding. Adv. Skin Wound Care 22, 373–380; quiz 381–372. doi: 10.1097/01.ASW.0000358637.38161.8f

Asan, E., Steinke, M., and Lesch, K. P. (2013). Serotonergic innervation of the amygdala: targets, receptors, and implications for stress and anxiety. Histochem. Cell Biol. 139, 785–813. doi: 10.1007/s00418-013-1081-1

Avishai-Eliner, S., Gilles, E. E., Eghbal-Ahmadi, M., Bar-El, Y., and Baram, T. Z. (2001). Altered regulation of gene and protein expression of hypothalamic-pituitary-adrenal axis components in an immature rat model of chronic stress. J. Neuroendocrinol. 13, 799–807. doi: 10.1046/j.1365-2826.2001. 00698.x

Barbara, G., Feinle-Bisset, C., Ghoshal, U. C., Quigley, E. M., Santos, J., Vanner, S., et al. (2016). The intestinal microenvironment and functional gastrointestinal disorders. Gastroenterology 150, 1305–1318. doi: 10.1053/j.gastro.2016.02.028

Bashashati, M., Fichna, J., Piscitelli, F., Capasso, R., Izzo, A. A., Sibaev, A., et al. (2017). Targeting fatty acid amide hydrolase and transient receptor potential vanilloid-1 simultaneously to modulate colonic motility and visceral sensation in the mouse: a pharmacological intervention with N-arachidonoylserotonin (AA-5-HT). Neurogastroenterol. Motil. doi: 10.1111/nmo. 13148. [Epub ahead of print].

Beggs, S., Currie, G., Salter, M. W., Fitzgerald, M., and Walker, S. M. (2012). Priming of adult pain responses by neonatal pain experience: maintenance by central neuroimmune activity. Brain 135, 404–417. doi: 10.1093/brain/awr288

Bernstein, B. E., Meissner, A., and Lander, E. S. (2007). The mammalian epigenome. Cell 128, 669–681. doi: 10.1016/j.cell.2007.01.033

Botschuijver, S., Roeselers, G., Levin, E., Jonkers, D. M., Welting, O., Heinsbroek, S. E. M., et al. (2017). Intestinal fungal dysbiosis associates with visceral hypersensitivity in patients with irritable bowel syndrome and rats. Gastroenterology 153, 1026–1039. doi: 10.1053/j.gastro.2017.06.004

Bowery, N. G., Bettler, B., Froestl, W., Gallagher, J. P., Marshall, F., Raiteri, M., et al. (2002). International Union of Pharmacology. XXXIII. Mammalian gammaaminobutyric acid(B) receptors: structure and function. Pharmacol. Rev. 54, 247–264.

Bradesi, S., Eutamene, H., Garcia-Villar, R., Fioramonti, J., and Bueno, L. (2002). Acute and chronic stress differently affect visceral sensitivity to rectal distension in female rats. Neurogastroenterol. Motil. 14, 75–82. doi: 10.1046/j.1365-2982.2002.00305.x

Bradesi, S., Karagiannides, I., Bakirtzi, K., Joshi, S. M., Koukos, G., Iliopoulos, D., et al. (2015). Identification of spinal cord MicroRNA and gene signatures in a model of chronic stress-induced visceral hyperalgesia in rat. PLoS ONE 10:e0130938. doi: 10.1371/journal.pone.0130938

Bradesi, S., Kokkotou, E., Simeonidis, S., Patierno, S., Ennes, H. S., Mittal, Y., et al. (2006). The role of neurokinin 1 receptors in the maintenance of visceral hyperalgesia induced by repeated stress in rats. Gastroenterology 130, 1729–1742. doi: 10.1053/j.gastro.2006.01.037

Bradesi, S., Lao, L., McLean, P. G., Winchester, W. J., Lee, K., Hicks, G. A., et al. (2007). Dual role of 5-HT3 receptors in a rat model of delayed stress-induced visceral hyperalgesia. Pain 130, 56–65. doi: 10.1016/j.pain.2006.10.028

Bradesi, S., Martinez, V., Lao, L., Larsson, H., and Mayer, E. A. (2009). Involvement of vasopressin 3 receptors in chronic psychological stress-induced visceral hyperalgesia in rats. Am. J. Physiol. Gastrointest. Liver Physiol. 296, G302–G309. doi: 10.1152/ajpgi.90557.2008

Bradesi, S., Schwetz, I., Ennes, H. S., Lamy, C. M., Ohning, G., Fanselow, M., et al. (2005). Repeated exposure to water avoidance stress in rats: a new model for sustained visceral hyperalgesia. Am. J. Physiol. Gastrointest. Liver Physiol. 289, G42–G53. doi: 10.1152/ajpgi.00500.2004

Bradford, K., Shih, W., Videlock, E. J., Presson, A. P., Naliboff, B. D., Mayer, E. A., et al. (2012). Association between early adverse life events and irritable bowel syndrome. Clin. Gastroenterol. Hepatol. 10, 385–390.e3. doi: 10.1016/j.cgh.2011.12.018

Braz, J., Solorzano, C., Wang, X., and Basbaum, A. I. (2014). Transmitting pain and itch messages: a contemporary view of the spinal cord circuits that generate gate control. Neuron 82, 522–536. doi: 10.1016/j.neuron.2014.01.018

Broers, C., Melchior, C., Van Oudenhove, L., Vanuytsel, T., Van Houtte, B., Scheerens, C., et al. (2017). The effect of intravenous corticotropinreleasing hormone administration on esophageal sensitivity and motility in health. Am. J. Physiol. Gastrointest. Liver Physiol. 312, G526–G534. doi: 10.1152/ajpgi.00437.2016

Brookes, S. J., Spencer, N. J., Costa, M., and Zagorodnyuk, V. P. (2013). Extrinsic primary afferent signalling in the gut. Nat. Rev. Gastroenterol. Hepatol. 10, 286–296. doi: 10.1038/nrgastro.2013.29

Bushnell, M. C., Ceko, M., and Low, L. A. (2013). Cognitive and emotional control of pain and its disruption in chronic pain. Nat. Rev. Neurosci. 14, 502–511. doi: 10.1038/nrn3516

Butler, R. K., and Finn, D. P. (2009). Stress-induced analgesia. Prog. Neurobiol. 88, 184–202. doi: 10.1016/j.pneurobio.2009.04.003

Camilleri, M., Madsen, K., Spiller, R., Greenwood-Van Meerveld, B., and Verne, G. N. (2012). Intestinal barrier function in health and gastrointestinal disease. Neurogastroenterol. Motil. 24, 503–512. doi: 10.1111/j.1365-2982.2012.01921.x Frontiers in Systems Neuroscience | www.frontiersin.org 17 November 2017 | Volume 11 | Article 86 Greenwood-Van Meerveld and Johnson Stress-Induced Visceral Pain 

Camp, L. L., and Rudy, J. W. (1988). Changes in the categorization of appetitive and aversive events during postnatal development of the rat. Dev. Psychobiol. 21, 25–42. doi: 10.1002/dev.420210103

Cao, D. Y., Bai, G., Ji, Y., and Traub, R. J. (2015). Epigenetic upregulation of metabotropic glutamate receptor 2 in the spinal cord attenuates oestrogen-induced visceral hypersensitivity. Gut 64, 1913–1920. doi: 10.1136/gutjnl-2014-307748

Cao, D. Y., Bai, G., Ji, Y., Karpowicz, J. M., and Traub, R. J. (2016). EXPRESS: histone hyperacetylation modulates spinal type II metabotropic glutamate receptor alleviating stress-induced visceral hypersensitivity in female rats. Mol. Pain 12:1744806916660722. doi: 10.1177/1744806916660722

Castro, J., Harrington, A. M., Garcia-Caraballo, S., Maddern, J., Grundy, L., Zhang, J., et al. (2017). Alpha-Conotoxin Vc1.1 inhibits human dorsal root ganglion neuroexcitability and mouse colonic nociception via GABAB receptors. Gut 66, 1083–1094. doi: 10.1136/gutjnl-2015-310971

Chaloner, A., and Greenwood-Van Meerveld, B. (2013). Sexually dimorphic effects of unpredictable early life adversity on visceral pain behavior in a rodent model. J. Pain 14, 270–280. doi: 10.1016/j.jpain.2012.11.008

Chang, L., Toner, B. B., Fukudo, S., Guthrie, E., Locke, G. R., Norton, N. J., et al. (2006). Gender, age, society, culture, and the patient’s perspective in the functional gastrointestinal disorders. Gastroenterology 130, 1435–1446. doi: 10.1053/j.gastro.2005.09.071 Chen, J. H., Wei, S. Z.,

Chen, J., Wang, Q., Liu, H. L., Gao, X. H., et al. (2009). Sensory denervation reduces visceral hypersensitivity in adult rats exposed to chronic unpredictable stress: evidences of neurogenic inflammation. Dig. Dis. Sci. 54, 1884–1891. doi: 10.1007/s10620-008-0575-5

Chen, J., Winston, J. H., and Sarna, S. K. (2013). Neurological and cellular regulation of visceral hypersensitivity induced by chronic stress and colonic inflammation in rats. Neuroscience 248C, 469–478. doi: 10.1016/j.neuroscience.2013.06.024

Chial, H. J., and Camilleri, M. (2002). Gender differences in irritable bowel syndrome. J. Gend. Specif. Med. 5, 37–45.

Coutinho, S. V., Plotsky, P. M., Sablad, M., Miller, J. C., Zhou, H., Bayati, A. I., et al. (2002). Neonatal maternal separation alters stress-induced responses to viscerosomatic nociceptive stimuli in rat. Am. J. Physiol. Gastrointest. Liver Physiol. 282, G307–G316. doi: 10.1152/ajpgi.00240.2001

da Costa Gomez, T. M., and Behbehani, M. M. (1995). An electrophysiological characterization of the projection from the central nucleus of the amygdala to the periaqueductal gray of the rat: the role of opioid receptors. Brain Res. 689, 21–31. doi: 10.1016/0006-8993(95)00525-U

Da Silva, S., Robbe-Masselot, C., Ait-Belgnaoui, A., Mancuso, A., MercadeLoubiere, M., Salvador-Cartier, C., et al. (2014). Stress disrupts intestinal mucus barrier in rats via mucin O-glycosylation shift: prevention by a probiotic treatment. Am. J. Physiol. Gastrointest. Liver Physiol. 307, G420–G429. doi: 10.1152/ajpgi.00290.2013

Darbaky, Y., Evrard, B., Patrier, S., Falenta, J., Garcin, S., Tridon, A., et al. (2017). Oral probiotic treatment of Lactobacillus rhamnosus Lcr35(R) prevents visceral hypersensitivity to a colonic inflammation and an acute psychological stress. J. Appl. Microbiol. 122, 188–200. doi: 10.1111/jam.13320

de Kloet, E. R., Joels, M., and Holsboer, F. (2005). Stress and the brain: from adaptation to disease. Nat. Rev. Neurosci. 6, 463–475. doi: 10.1038/nrn1683

Denk, F., Mcmahon, S. B., and Tracey, I. (2014). Pain vulnerability: a neurobiological perspective. Nat. Neurosci. 17, 192–200. doi: 10.1038/nn.3628

Dhabhar, F. S., Mcewen, B. S., and Spencer, R. L. (1997). Adaptation to prolonged or repeated stress–comparison between rat strains showing intrinsic differences in reactivity to acute stress. Neuroendocrinology 65, 360–368.

Di, S., Malcher-Lopes, R., Halmos, K. C., and Tasker, J. G. (2003). Nongenomic glucocorticoid inhibition via endocannabinoid release in the hypothalamus: a fast feedback mechanism. J. Neurosci. 23, 4850–4857.

Dina, O. A., Khasar, S. G., Alessandri-Haber, N., Green, P. G., Messing, R. O., and Levine, J. D. (2008). Alcohol-induced stress in painful alcoholic neuropathy. Eur. J. Neurosci. 27, 83–92. doi: 10.1111/j.1460-9568.2007.05987.x

Dong, F., Xie, W., Strong, J. A., and Zhang, J. M. (2012). Mineralocorticoid receptor blocker eplerenone reduces pain behaviors in vivo and decreases excitability in small-diameter sensory neurons from local inflamed dorsal root ganglia in vitro. Anesthesiology 117, 1102–1112. doi: 10.1097/ALN.0b013e3182700383

Drake, B., and Pandey, S. (1996). Understanding the relationship between neighborhood poverty and specific types of child maltreatment. Child Abuse Negl. 20, 1003–1018. doi: 10.1016/0145-2134(96)00091-9

Drossman, D. A., Chang, L., Bellamy, N., Gallo-Torres, H. E., Lembo, A., Mearin, F., et al. (2011). Severity in irritable bowel syndrome: a Rome foundation working team report. Am. J. Gastroenterol. 106, 1749–1759; quiz 1760. doi: 10.1038/ajg.2011.201

Drossman, D. A., Leserman, J., Nachman, G., Li, Z. M., Gluck, H., Toomey, T. C., et al. (1990). Sexual and physical abuse in women with functional or organic gastrointestinal disorders. Ann. Intern. Med. 113, 828–833. doi: 10.7326/0003-4819-113-11-828

Eckersell, C. B., Popper, P., and Micevych, P. E. (1998). Estrogen-induced alteration of mu-opioid receptor immunoreactivity in the medial preoptic nucleus and medial amygdala. J. Neurosci. 18, 3967–3976.

Enna, S. J., and Bowery, N. G. (2004). GABA(B) receptor alterations as indicators of physiological and pharmacological function. Biochem. Pharmacol. 68, 1541–1548. doi: 10.1016/j.bcp.2004.06.037

Eutamene, H., Bradesi, S., Larauche, M., Theodorou, V., Beaufrand, C., Ohning, G., et al. (2010). Guanylate cyclase C-mediated antinociceptive effects of linaclotide in rodent models of visceral pain. Neurogastroenterol. Motil. 22, 312–e384. doi: 10.1111/j.1365-2982.2009.01385.x

Evanson, N. K., Tasker, J. G., Hill, M. N., Hillard, C. J., and Herman, J. P. (2010). Fast feedback inhibition of the HPA axis by glucocorticoids is mediated by endocannabinoid signaling. Endocrinology 151, 4811–4819. doi: 10.1210/en.2010-0285

Farh, K. K., Grimson, A., Jan, C., Lewis, B. P., Johnston, W. K., Lim, L. P., et al. (2005). The widespread impact of mammalian MicroRNAs on mRNA repression and evolution. Science 310, 1817–1821. doi: 10.1126/science.1121158

Fichna, J., Salaga, M., Stuart, J., Saur, D., Sobczak, M., Zatorski, H., et al. (2014). Selective inhibition of FAAH produces antidiarrheal and antinociceptive effect mediated by endocannabinoids and cannabinoid-like fatty acid amides. Neurogastroenterol. Motil. 26, 470–481. doi: 10.1111/nmo.12272

Fichna, J., Wood, J. T., Papanastasiou, M., Vadivel, S. K., Oprocha, P., Salaga, M., et al. (2013). Endocannabinoid and cannabinoid-like fatty acid amide levels correlate with pain-related symptoms in patients with IBS-D and IBS-C: a pilot study. PLoS ONE 8:e85073. doi: 10.1371/journal.pone.0085073

Fioramonti, J., Gaultier, E., Toulouse, M., Sanger, G. J., and Bueno, L. (2003). Intestinal anti-nociceptive behaviour of NK3 receptor antagonism in conscious rats: evidence to support a peripheral mechanism of action. Neurogastroenterol. Motil. 15, 363–369. doi: 10.1046/j.1365-2982.2003.00420.x

Fitch, R. H., and Denenberg, V. H. (1998). A role for ovarian hormones in sexual differentiation of the brain. Behav. Brain Sci. 21, 311–327; discussion 327–352.

Fornasari, D. (2012). Pain mechanisms in patients with chronic pain. Clin. Drug Investig. 32(Suppl. 1), 45–52. doi: 10.2165/11630070-000000000-00000

Fourie, N. H., Peace, R. M., Abey, S. K., Sherwin, L. B., Rahim-Williams, B., Smyser, P. A., et al. (2014). Elevated circulating miR-150 and miR-342-3p in patients with irritable bowel syndrome. Exp. Mol. Pathol. 96, 422–425. doi: 10.1016/j.yexmp.2014.04.009

Gallagher, J. P., Orozco-Cabal, L. F., Liu, J., and Shinnick-Gallagher, P. (2008). Synaptic physiology of central CRH system. Eur. J. Pharmacol. 583, 215–225. doi: 10.1016/j.ejphar.2007.11.075

Gilet, M., Eutamene, H., Han, H., Kim, H. W., and Bueno, L. (2014). Influence of a new 5-HT4 receptor partial agonist, YKP10811, on visceral hypersensitivity in rats triggered by stress and inflammation. Neurogastroenterol. Motil. 26, 1761–1770. doi: 10.1111/nmo.12458

Gilles, E. E., Schultz, L., and Baram, T. Z. (1996). Abnormal corticosterone regulation in an immature rat model of continuous chronic stress. Pediatr. Neurol. 15, 114–119. doi: 10.1016/0887-8994(96)00153-1

Gillespie, C. F., Phifer, J., Bradley, B., and Ressler, K. J. (2009). Risk and resilience: genetic and environmental influences on development of the stress response. Depress. Anxiety 26, 984–992. doi: 10.1002/da.20605

Girotti, M., Pace, T. W., Gaylord, R. I., Rubin, B. A., Herman, J. P., and Spencer, R. L. (2006). Habituation to repeated restraint stress is associated with lack of stress-induced c-fos expression in primary sensory processing areas of the rat brain. Neuroscience 138, 1067–1081. doi: 10.1016/j.neuroscience.2005. 12.002

Gorzalka, B. B., Hill, M. N., and Hillard, C. J. (2008). Regulation of endocannabinoid signaling by stress: implications for stressrelated affective disorders. Neurosci. Biobehav. Rev. 32, 1152–1160. doi: 10.1016/j.neubiorev.2008.03.004

Goudet, C., Magnaghi, V., Landry, M., Nagy, F., Gereau, R. W. T., and Pin, J. P. (2009). Metabotropic receptors for glutamate and GABA in pain. Brain Res. Rev. 60, 43–56. doi: 10.1016/j.brainresrev.2008.12.007 Frontiers in Systems Neuroscience | www.frontiersin.org 18 November 2017 | Volume 11 | Article 86 Greenwood-Van Meerveld and Johnson Stress-Induced Visceral Pain

Grace, P. M., Hutchinson, M. R., Maier, S. F., and Watkins, L. R. (2014). Pathological pain and the neuroimmune interface. Nat. Rev. Immunol. 14, 217–231. doi: 10.1038/nri3621

Greenwood-Van Meerveld, B., Gibson, M., Gunter, W., Shepard, J., Foreman, R., and Myers, D. (2001). Stereotaxic delivery of corticosterone to the amygdala modulates colonic sensitivity in rats. Brain Res. 893, 135–142. doi: 10.1016/S0006-8993(00)03305-9

Greenwood-Van Meerveld, B., Prusator, D. K., and Johnson, A. C. (2015). Animal models of gastrointestinal and liver diseases. Animal models of visceral pain: pathophysiology, translational relevance, and challenges. Am. J. Physiol. Gastrointest. Liver Physiol. 308, G885–G903. doi: 10.1152/ajpgi.00463.2014

Greenwood-Van Meerveld, B., Prusator, D. K., Ligon, C. O., Johnson, A. C., and Moloney, R. D. (2016). “Chapter 41 - Epigenetics of Pain Management A2,” in Medical Epigenetics, ed T.O. Tollefsbol (Boston, MA: Academic Press), 827–841. doi: 10.1016/B978-0-12-803239-8.00041-7

Griebel, G., Pichat, P., Beeske, S., Leroy, T., Redon, N., Jacquet, A., et al. (2015). Selective blockade of the hydrolysis of the endocannabinoid 2-arachidonoylglycerol impairs learning and memory performance while producing antinociceptive activity in rodents. Sci. Rep. 5:7642. doi: 10.1038/srep07642

Gu, X., Wang, S., Yang, L., Sung, B., Lim, G., Mao, J., et al. (2007). Timedependent effect of epidural steroid on pain behavior induced by chronic compression of dorsal root ganglion in rats. Brain Res. 1174, 39–46. doi: 10.1016/j.brainres.2007.08.030

Gué, M., Del Rio-Lacheze, C., Eutamene, H., Theodorou, V., Fioramonti, J., and Bueno, L. (1997). Stress-induced visceral hypersensitivity to rectal distension in rats: role of CRF and mast cells. Neurogastroenterol. Motil. 9, 271–279. doi: 10.1046/j.1365-2982.1997.d01-63.x

Gunn, B. G., Cunningham, L., Mitchell, S., Swinny, J. D., Lambert, J. J., and Belelli, D. (2014). GABA receptor-acting neurosteroids: a role in the development and regulation of the stress response. Front. Neuroendocrinol. 36, 28–48. doi: 10.1016/j.yfrne.2014.06.001

Gupta, A., Kilpatrick, L., Labus, J., Tillisch, K., Braun, A., Hong, J. Y., et al. (2014). Early adverse life events and resting state neural networks in patients with chronic abdominal pain: evidence for sex differences. Psychosom. Med. 76, 404–412. doi: 10.1097/PSY.0000000000000089

Gustafsson, J. K., and Greenwood-Van Meerveld, B. (2011). Amygdala activation by corticosterone alters visceral and somatic pain in cycling female rats. Am. J. Physiol. Gastrointest. Liver Physiol. 300, G1080–G1085. doi: 10.1152/ajpgi.00349.2010

Haller, J., Mikics, E., and Makara, G. B. (2008). The effects of non-genomic glucocorticoid mechanisms on bodily functions and the central neural system. A critical evaluation of findings. Front. Neuroendocrinol. 29, 273–291. doi: 10.1016/j.yfrne.2007.10.004

Hammes, S. R., and Levin, E. R. (2011). Minireview: recent advances in extranuclear steroid receptor actions. Endocrinology 152, 4489–4495. doi: 10.1210/en.2011-1470

Handa, R. J., Burgess, L. H., Kerr, J. E., and O’keefe, J. A. (1994). Gonadal steroid hormone receptors and sex differences in the hypothalamo-pituitary-adrenal axis. Horm. Behav. 28, 464–476. doi: 10.1006/hbeh.1994.1044

Heinricher, M. M., Tavares, I., Leith, J. L., and Lumb, B. M. (2009). Descending control of nociception: specificity, recruitment and plasticity. Brain Res. Rev. 60, 214–225. doi: 10.1016/j.brainresrev.2008.12.009

Heitkemper, M. M., and Chang, L. (2009). Do fluctuations in ovarian hormones affect gastrointestinal symptoms in women with irritable bowel syndrome? Gend. Med. 6(Suppl. 2), 152–167. doi: 10.1016/j.genm.2009.03.004

Heitkemper, M., and Jarrett, M. (2008). Irritable bowel syndrome: does gender matter? J. Psychosom. Res. 64, 583–587. doi: 10.1016/j.jpsychores.2008.02.020

Herman, J. P., and Cullinan, W. E. (1997). Neurocircuitry of stress: central control of the hypothalamo-pituitary-adrenocortical axis. Trends Neurosci. 20, 78–84. doi: 10.1016/S0166-2236(96)10069-2

Hill, M. N., and McEwen, B. S. (2010). Involvement of the endocannabinoid system in the neurobehavioural effects of stress and glucocorticoids. Prog. Neuropsychopharmacol. Biol. Psychiatry 34, 791–797. doi: 10.1016/j.pnpbp.2009.11.001

Hillhouse, T. M., and Negus, S. S. (2016). Effects of the noncompetitive Nmethyl-d-aspartate receptor antagonists ketamine and MK-801 on painstimulated and pain-depressed behaviour in rats. Eur. J. Pain 20, 1229–1240. doi: 10.1002/ejp.847

Holschneider, D. P., Guo, Y., Mayer, E. A., and Wang, Z. (2016). Early life stress elicits visceral hyperalgesia and functional reorganization of pain circuits in adult rats. Neurobiol. Stress 3, 8–22. doi: 10.1016/j.ynstr.2015.12.003

Hong, S., Fan, J., Kemmerer, E. S., Evans, S., Li, Y., and Wiley, J. W. (2009). Reciprocal changes in vanilloid (TRPV1) and endocannabinoid (CB1) receptors contribute to visceral hyperalgesia in the water avoidance stressed rat. Gut 58, 202–210. doi: 10.1136/gut.2008.157594

Hong, S., Zheng, G., and Wiley, J. W. (2015). Epigenetic regulation of genes that modulate chronic stress-induced visceral pain in the peripheral nervous system. Gastroenterology 148, 148–157.e7. doi: 10.1053/j.gastro.2014.09.032

Hong, S., Zheng, G., Wu, X., Snider, N. T., Owyang, C., and Wiley, J. W. (2011). Corticosterone mediates reciprocal changes in CB 1 and TRPV1 receptors in primary sensory neurons in the chronically stressed rat. Gastroenterology 140, 148–157.e7. doi: 10.1053/j.gastro.2010.11.003

Hooten, W. M. (2016). Chronic pain and mental health disorders: shared neural mechanisms, epidemiology, and treatment. Mayo Clin. Proc. 91, 955–970. doi: 10.1016/j.mayocp.2016.04.029

Icenhour, A., Witt, S. T., Elsenbruch, S., Lowen, M., Engstrom, M., Tillisch, K., et al. (2017). Brain functional connectivity is associated with visceral sensitivity in women with Irritable Bowel Syndrome. Neuroimage Clin. 15, 449–457. doi: 10.1016/j.nicl.2017.06.001

Ivy, A. S., Brunson, K. L., Sandman, C., and Baram, T. Z. (2008). Dysfunctional nurturing behavior in rat dams with limited access to nesting material: a clinically relevant model for early-life stress. Neuroscience 154, 1132–1142. doi: 10.1016/j.neuroscience.2008.04.019

Jaggi, A. S., and Singh, N. (2011). Role of different brain areas in peripheral nerve injury-induced neuropathic pain. Brain Res. 1381, 187–201. doi: 10.1016/j.brainres.2011.01.002

Ji, G., and Neugebauer, V. (2007). Differential effects of CRF1 and CRF2 receptor antagonists on pain-related sensitization of neurons in the central nucleus of the amygdala. J. Neurophysiol. 97, 3893–3904. doi: 10.1152/jn.00135.2007

Ji, G., and Neugebauer, V. (2008). Pro- and anti-nociceptive effects of corticotropin-releasing factor (CRF) in central amygdala neurons are mediated through different receptors. J. Neurophysiol. 99, 1201–1212. doi: 10.1152/jn.01148.2007

Ji, Y., Bai, G., Cao, D. Y., and Traub, R. J. (2015). Estradiol modulates visceral hyperalgesia by increasing thoracolumbar spinal GluN2B subunit activity in female rats. Neurogastroenterol. Motil. 27, 775–786. doi: 10.1111/nmo.12549

Ji, Y., Tang, B., and Traub, R. J. (2008). The visceromotor response to colorectal distention fluctuates with the estrous cycle in rats. Neuroscience 154, 1562–1567. doi: 10.1016/j.neuroscience.2008.04.070

Jia, F. Y., Li, X. L., Li, T. N., Wu, J., Xie, B. Y., and Lin, L. (2013). Role of nesfatin-1 in a rat model of visceral hypersensitivity. World J. Gastroenterol. 19, 3487–3493. doi: 10.3748/wjg.v19.i22.3487

Johnson, A. C., and Greenwood Van-Meerveld, B. (2012). Evidence to support the non-genomic modulation of the HPA axis. J. Steroids Horm. Sci. 3:e109. doi: 10.4172/2157-7536.1000e109

Johnson, A. C., and Greenwood-Van Meerveld, B. (2015). Knockdown of steroid receptors in the central nucleus of the amygdala induces heightened pain behaviors in the rat. Neuropharmacology 93, 116–123. doi: 10.1016/j.neuropharm.2015.01.018

Johnson, A. C., and Greenwood-Van Meerveld, B. (2017). Critical evaluation of animal models of gastrointestinal disorders. Handb. Exp. Pharmacol. 239, 289–317. doi: 10.1007/164_2016_120

Johnson, A. C., Myers, B., Lazovic, J., Towner, R., and Greenwood-Van Meerveld, B. (2010). Brain activation in response to visceral stimulation in rats with amygdala implants of corticosterone: an FMRI study. PLoS ONE 5:e8573. doi: 10.1371/journal.pone.0008573

Johnson, A. C., Tran, L., and Greenwood-Van Meerveld, B. (2015). Knockdown of corticotropin-releasing factor in the central amygdala reverses persistent viscerosomatic hyperalgesia. Transl. Psychiatry 5:e517. doi: 10.1038/tp.2015.16

Johnson, A. C., Tran, L., Schulkin, J., and Greenwood-Van Meerveld, B. (2012). Importance of stress receptor-mediated mechanisms in the amygdala on visceral pain perception in an intrinsically anxious rat. Neurogastroenterol. Motil. 24, 479-486. doi: 10.1111/j.1365-2982.2012.01899.x

Johnson, L. R., Farb, C., Morrison, J. H., Mcewen, B. S., and Ledoux, J. E. (2005). Localization of glucocorticoid receptors at postsynaptic membranes in the lateral amygdala. Neuroscience 136, 289–299. doi: 10.1016/j.neuroscience.2005.06.050 Frontiers in Systems Neuroscience | www.frontiersin.org 19 November 2017 | Volume 11 | Article 86 Greenwood-Van Meerveld and Johnson Stress-Induced Visceral Pain

Johnson, M. P., Muhlhauser, M. A., Nisenbaum, E. S., Simmons, R. M., Forster, B. M., Knopp, K. L., et al. (2017). Broad spectrum efficacy with LY2969822, an oral prodrug of metabotropic glutamate 2/3 receptor agonist LY2934747, in rodent pain models. Br. J. Pharmacol. 174, 822–835. doi: 10.1111/bph.13740

Kalinichev, M., Girard, F., Haddouk, H., Rouillier, M., Riguet, E., Royer-Urios, I., et al. (2017). 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. doi: 10.1016/j.neuropharm.2016.11.016

Kane, S. V., Sable, K., and Hanauer, S. B. (1998). The menstrual cycle and its effect on inflammatory bowel disease and irritable bowel syndrome: a prevalence study. Am. J. Gastroenterol. 93, 1867–1872. doi: 10.1111/j.1572-0241.1998.540_i.x

Kannampalli, P., Babygirija, R., Zhang, J., Poe, M. M., Li, G., Cook, J. M., et al. (2017a). Neonatal bladder inflammation induces long-term visceral pain and altered responses of spinal neurons in adult rats. Neuroscience 346, 349–364. doi: 10.1016/j.neuroscience.2017.01.021

Kannampalli, P., Poli, S. M., Bolea, C., and Sengupta, J. N. (2017b). Analgesic effect of ADX71441, a positive allosteric modulator (PAM) of GABAB receptor in a rat model of bladder pain. Neuropharmacology 126, 1–11. doi: 10.1016/j.neuropharm.2017.08.023

Karst, H., Berger, S., Turiault, M., Tronche, F., Schutz, G., and Joels, M. (2005). Mineralocorticoid receptors are indispensable for nongenomic modulation of hippocampal glutamate transmission by corticosterone. Proc. Natl. Acad. Sci. U.S.A. 102, 19204–19207. doi: 10.1073/pnas.0507572102

Kayser, V., Berkley, K. J., Keita, H., Gautron, M., and Guilbaud, G. (1996). Estrous and sex variations in vocalization thresholds to hindpaw and tail pressure stimulation in the rat. Brain Res. 742, 352–354. doi: 10.1016/S0006-8993(96)01108-0

Kuner, R. (2010). Central mechanisms of pathological pain. Nat. Med. 16, 1258–1266. doi: 10.1038/nm.2231

Laessle, R. G., Tuschl, R. J., Schweiger, U., and Pirke, K. M. (1990). Mood changes and physical complaints during the normal menstrual cycle in healthy young women. Psychoneuroendocrinology 15, 131–138.

Lampe, A., Doering, S., Rumpold, G., Solder, E., Krismer, M., KantnerRumplmair, W., et al. (2003). Chronic pain syndromes and their relation to childhood abuse and stressful life events. J. Psychosom. Res. 54, 361–367. doi: 10.1016/S0022-3999(02)00399-9

Larauche, M., Gourcerol, G., Wang, L., Pambukchian, K., Brunnhuber, S., Adelson, D. W., et al. (2009). Cortagine, a CRF1 agonist, induces stresslike alterations of colonic function and visceral hypersensitivity in rodents primarily through peripheral pathways. Am. J. Physiol. Gastrointest. Liver Physiol. 297, G215–G227. doi: 10.1152/ajpgi.00072.2009

Lee, U. J., Ackerman, A. L., Wu, A., Zhang, R., Leung, J., Bradesi, S., et al. (2015). Chronic psychological stress in high-anxiety rats induces sustained bladder hyperalgesia. Physiol. Behav. 139, 541–548. doi: 10.1016/j.physbeh.2014. 11.045

Leyro, T. M., Zvolensky, M. J., and Bernstein, A. (2010). Distress tolerance and psychopathological symptoms and disorders: a review of the empirical literature among adults. Psychol. Bull. 136, 576–600. doi: 10.1037/a0019712

Liao, X. J., Mao, W. M., Wang, Q., Yang, G. G., Wu, W. J., and Shao, S. X. (2016). MicroRNA-24 inhibits serotonin reuptake transporter expression and aggravates irritable bowel syndrome. Biochem. Biophys. Res. Commun. 469, 288–293. doi: 10.1016/j.bbrc.2015.11.102

Ligon, C. O., Moloney, R. D., and Greenwood-Van Meerveld, B. (2016). Targeting epigenetic mechanisms for chronic pain: a valid approach for the development of novel therapeutics. J. Pharmacol. Exp. Ther. 357, 84–93. doi: 10.1124/jpet.115.231670

Liu, H. R., Fang, X. Y., Wu, H. G., Wu, L. Y., Li, J., Weng, Z. J., et al. (2015). Effects of electroacupuncture on corticotropin-releasing hormone in rats with chronic visceral hypersensitivity. World J. Gastroenterol. 21, 7181–7190. doi: 10.3748/wjg.v21.i23.7181

Liu, S. B., Zhang, M. M., Cheng, L. F., Shi, J., Lu, J. S., and Zhuo, M. (2015). Longterm upregulation of cortical glutamatergic AMPA receptors in a mouse model of chronic visceral pain. Mol. Brain 8:76. doi: 10.1186/s13041-015-0169-z

Liu, S., Hagiwara, S. I., and Bhargava, A. (2017). Early-life adversity, epigenetics, and visceral hypersensitivity. Neurogastroenterol. Motil. 29:e13170. doi: 10.1111/nmo.13170

Lu, N. Z., Wardell, S. E., Burnstein, K. L., Defranco, D., Fuller, P. J., Giguere, V., et al. (2006). International Union of Pharmacology. LXV. The pharmacology and classification of the nuclear receptor superfamily: glucocorticoid, mineralocorticoid, progesterone, and androgen receptors. Pharmacol. Rev. 58, 782–797. doi: 10.1124/pr.58.4.9

Luongo, L., Maione, S., and Di Marzo, V. (2014). Endocannabinoids and neuropathic pain: focus on neuron-glia and endocannabinoidneurotrophin interactions. Eur. J. Neurosci. 39, 401–408. doi: 10.1111/ejn. 12440

Ly, H. G., Ceccarini, J., Weltens, N., Bormans, G., Van Laere, K., Tack, J., et al. (2015). Increased cerebral cannabinoid-1 receptor availability is a stable feature of functional dyspepsia: a [F]MK-9470 PET study. Psychother. Psychosom. 84, 149–158. doi: 10.1159/000375454

Ma, X., Li, S., Tian, J., Jiang, G., Wen, H., Wang, T., et al. (2015). Altered brain spontaneous activity and connectivity network in irritable bowel syndrome patients: a resting-state fMRI study. Clin. Neurophysiol. 126, 1190–1197. doi: 10.1016/j.clinph.2014.10.004

Maizels, M., Aurora, S., and Heinricher, M. (2012). Beyond neurovascular: migraine as a dysfunctional neurolimbic pain network. Headache 52, 1553–1565. doi: 10.1111/j.1526-4610.2012.02209.x

Matos, R., Serrao, P., Rodriguez, L., Birder, L. A., Cruz, F., and Charrua, A. (2017). The water avoidance stress induces bladder pain due to a prolonged alpha1A adrenoceptor stimulation. Naunyn Schmiedebergs. Arch. Pharmacol. 390, 839–844. doi: 10.1007/s00210-017-1384-1

McIlwrath, S. L., and Westlund, K. N. (2015). Pharmacological attenuation of chronic alcoholic pancreatitis induced hypersensitivity in rats. World J. Gastroenterol. 21, 836–853. doi: 10.3748/wjg.v21.i3.836

McLean, S. A., Williams, D. A., Stein, P. K., Harris, R. E., Lyden, A. K., Whalen, G., et al. (2006). Cerebrospinal fluid corticotropin-releasing factor concentration is associated with pain but not fatigue symptoms in patients with fibromyalgia. Neuropsychopharmacology 31, 2776–2782. doi: 10.1038/sj.npp. 1301200