Sustained delayed gastric emptying during repeated restraint stress in oxytocin knockout mice

Journal of Neuroendocrinology

Volumn 22, Issue 11, 2010, Pages 1181-1186

  Babygirija, R ^a   Zheng, J ^a   Bulbul M ^a   Cerjak, D ^a   Ludwig, K ^a   Takahashi, T ^a  

^a CLEMENT J ZABLOCKI VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Acute stress; Corticotrophin releasing factor; Hypothalamic pituitary adrenal axis

Indexed keywords

CORTICOTROPIN RELEASING FACTOR; MESSENGER RNA; OXYTOCIN;

ACUTE STRESS; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; GENOTYPE; HYPOTHALAMUS; IMMOBILIZATION STRESS; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STOMACH EMPTYING; THALAMUS MIDLINE NUCLEUS;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; CORTICOTROPIN-RELEASING HORMONE; GASTRIC EMPTYING; GENOTYPE; MALE; MICE; MICE, KNOCKOUT; OXYTOCIN; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; RESTRAINT, PHYSICAL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STRESS, PSYCHOLOGICAL;

EID: 77958524715     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2010.02069.x     Document Type: Article

References (65)

1. Jones MP. Evaluation and treatment of dyspepsia. Postgrad Med J 2003; 79: 25-29.
2. Pitman DL, Ottenweller JE, Natelson BH. Plasma corticosterone levels during repeated presentation of two intensities of restraint stress: chronic stress and habituation. Physiol Behav 1988; 43: 47-55.
3. Ostrander MM, Ulrich-Lai YM, Choi DC, Richtand NM, Herman JP. Hypoactivity of the hypothalamo-pituitary-adrenocortical axis during recovery from chronic variable stress. Endocrinology 2006; 147: 2008-2017.
4. Zheng J, Dobner A, Babygirija R, Ludwig K, Takahashi T. Effects of repeated restraint stress on gastric motility in rats. Am J Physiol Regul Integr Comp Physiol 2009; 296: R1358-R1365.
5. Ludwig M. Dendritic release of vasopressin and oxytocin. J Neuroendocrinol 1998; 10: 881-895.
6. Landgraf R, Neumann ID. Vasopressin and oxytocin release within the brain: a dynamic concept of multiple and variable modes of neuropeptide communication. Front Neuroendocrinol 2004; 4: 150-176.
7. Baumgartner T, Heinrichs M, Vonlanthen A, Fischbacher U, Fehr E. Oxytocin shapes the neural circuitry of trust and trust adaptation in humans. Neuron 2008; 58: 639-650.
8. Ferguson JN, Young LJ, Insel TR. The neuroendocrine basis of social recognition. Front Neuroendocrinol 2002; 23: 200-224.
9. Young LJ, Lim MM, Gingrich B, Insel TR. Cellular mechanisms of social attachment. Horm Behav 2001; 40: 133-138.
10. Domes G, Heinrichs M, Michel A, Berger C, Herpertz SC. Oxytocin improves 'mind-reading' in humans. Biol Psychiatry 2007; 61: 731-733.
11. Kosfeld M, Heinrichs M, Zak PJ, Fischbacher U, Fehr E. Oxytocin increases trust in humans. Nature 2005; 435: 673-676.
12. Windle RJ, Shanks N, Lightman SL, Ingram CD. Central oxytocin administration reduces stress-induced corticosterone release and anxiety behavior in rats. Endocrinology 1997; 138: 2829-2834.
13. Neumann ID, Kromer SA, Toschi N, Ebner K. Brain oxytocin inhibits the (re)activity of the hypothalamo-pituitary-adrenal axis in male rats: involvement of hypothalamic and limbic brain regions. Regul Pept 2000; 96: 31-38.
14. Neumann ID, Wigger A, Torner L, Holsboer F, Landgraf R. Brain oxytocin inhibits basal and stress-induced activity of the hypothalamo-pituitary-adrenal axis in male and female rats: partial action within the paraventricular nucleus. J Neuroendocrinol 2000; 12: 235-243.
15. Blume A, Bosch OJ, Miklos S, Torner L, Wales L, Waldherr M, Neumann ID. Oxytocin reduces anxiety via ERK1/2 activation: local effect within the rat hypothalamic paraventricular nucleus. Eur J Neurosci 2008; 27: 1947-1956.
16. Ring RH, Malberg JE, Potestio L, Ping J, Boikess S, Luo B, Schechter LE, Rizzo S, Rahman Z, Rosenzweig-Lipson S. Anxiolytic-like activity of oxytocin in male mice: behavioral and autonomic evidence, therapeutic implications. Psychopharmacology (Berl) 2006; 185: 218-225.
17. Neumann ID. Brain oxytocin: a key regulator of emotional and social behaviours in both females and males. J Neuroendocrinol 2008; 20: 858-865.
18. Neumann ID, Torner L, Wigger A. Brain oxytocin: differential inhibition of neuroendocrine stress responses and anxiety-related behaviour in virgin, pregnant and lactating rats. Neuroscience 2000; 95: 567-575.
19. Rogers RC, Hermann GE. Hypothalamic paraventricular nucleus stimulation-induced gastric acid secretion and bradycardia suppressed by oxytocin antagonist. Peptides. 1986; 7: 695-700.
20. McCann MJ, Rogers RC. Oxytocin excites gastric-related neurones in rat dorsal vagal complex. J Physiol 1990; 428: 95-108.
21. Nakade Y, Tsuchida D, Fukuda H, Iwa M, Pappas TN, Takahashi T. Restraint stress delays solid gastric emptying via a central CRF and peripheral sympathetic neuron in rats. Am J Physiol Regul Integr Comp Physiol 2005; 288: R427-R432.
22. Tache Y, Bonaz B. Corticotropin-releasing factor receptors and stress-related alterations of gut motor function. J Clin Invest 2007; 117: 33-40.
23. Tache Y, Maeda-Hagiwara M, Turkelson CM. Central nervous system action of corticotropin-releasing factor to inhibit gastric emptying in rats. Am J Physiol 1987; 1: G241-G245.
24. Lenz HJ, Raedler A, Greten H, Vale WW, Rivier JE. Stress-induced gastrointestinal secretory and motor responses in rats are mediated by endogenous corticotropin-releasing factor. Gastroenterology 1988; 95: 1510-1517.
25. Gomez F, Manalo S, Dallman MF. Androgen-sensitive changes in regulation of restraint-induced adrenocorticotropin secretion between early and late puberty in male rats. Endocrinology 2004; 145: 59-70.
26. Da Costa AP, Ma X, Ingram CD, Lightman SL, Aguilera G. Hypothalamic and amygdaloid corticotropin-releasing hormone (CRH) and CRH receptor-1 mRNA expression in the stress-hyporesponsive late pregnant and early lactating rat. Brain Res Mol Brain Res 2001; 2: 119-130.
27. Jorgensen H, Knigge U, Kjaer A, Warberg J. Serotonergic involvement in stress-induced vasopressin and oxytocin secretion. Eur J Endocrinol 2002; 147: 815-824.
28. Ferguson JN, Young LJ, Hearn EF, Matzuk MM, Insel TR, Winslow JT. Social amnesia in mice lacking the oxytocin gene. Nat Genet 2000; 25: 284-288.
29. Ferguson JN, Aldag JM, Insel TR, Young LJ. Oxytocin in the medial amygdala is essential for social recognition in the mouse. J Neurosci 2001; 21: 8278-8285.
30. Winslow JT, Hearn EF, Ferguson J, Young LJ, Matzuk MM, Insel TR. Infant vocalization, adult aggression, and fear behavior of an oxytocin null mutant mouse. Horm Behav 2000; 37: 145-155.
31. Zheng J, Babygirija R, Bulbul M, Cerjak D, Ludwig K, Takahashi T. Hypothalamic oxytocin mediates adaptation mechanism against chronic stress in rats. Am J Physiol Gastrointest Liver Physiol. 2010 Aug 5 [Epub ahead of print] in press.
32. Babygirija R, Zheng J, Ludwig K, Takahashi T. Central oxytocin is involved in restoring impaired gastric motility following chronic repeated stress in mice. Am J Physiol Regul Integr Comp Physiol 2010; 298: R157-R165.
33. Asakawa A, Inui A, Ueno N, Makino S, Fujino MA, Kasuga M. Urocortin reduces food intake and gastric emptying in lean and ob/ob obese mice. Gastroenterology 1999; 116: 1287-1292.
34. Antoni FA. Hypothalamic control of adrenocorticotropin secretion: advances since the discovery of 41-residue corticotropin-releasing factor. Endocr Rev 1986; 7: 351-378.
35. Sawchenko PE, Swanson LW, Steinbusch HW, Verhofstad AA. The distribution and cells of origin of serotonergic inputs to the paraventricular and supraoptic nuclei of the rat. Brain Res 1983; 277: 355-360.
36. Sawchenko PE, Brown ER, Chan RK, Ericsson A, Li HY, Roland BL, Kovacs KJ. The paraventricular nucleus of the hypothalamus and the functional neuroanatomy of visceromotor responses to stress. Prog Brain Res 1996; 107: 201-222.
37. Herman JP, Cullinan WE, Ziegler DR, Tasker JG. Role of the paraventricular nucleus microenvironment in stress integration. Eur J Neurosci 2002; 16: 381-385.
38. Bunck M, Czibere L, Horvath C, Graf C, Frank E, Kessler MS, Murgatroyd C, Muller-Myhsok B, Gonik M, Weber P, Putz B, Muigg P, Panhuysen M, Singewald N, Bettecken T, Deussing JM, Holsboer F, Spengler D, Landgraf R. A hypomorphic vasopressin allele prevents anxiety-related behavior. PLoS ONE 2009; 4: e5129.
39. Paxinos G The Mouse Brain in Stereotaxic Coordinates, 2nd edn, San Diego, CA: Academic Press, 2001.
40. Gourcerol G, Gallas S, Mounien L, Leblanc I, Bizet P, Boutelet I, Leroi AM, Ducrotte P, Vaudry H, Jegou S. Gastric electrical stimulation modulates hypothalamic corticotropin-releasing factor-producing neurons during post-operative ileus in rat. Neuroscience 2007; 148: 775-781.
41. Pacak K, Palkovits M. Stressor specificity of central neuroendocrine responses: implications for stress-related disorders. Endocr Rev 2001; 22: 502-548.
42. Nishioka T, Anselmo-Franci JA, Li P, Callahan MF, Morris M. Stress increases oxytocin release within the hypothalamic paraventricular nucleus. Brain Res 1998; 2: 56-60.
43. Wotjak CT, Ganster J, Kohl G, Holsboer F, Landgraf R, Engelmann M. Dissociated central and peripheral release of vasopressin, but not oxytocin, in response to repeated swim stress: new insights into the secretory capacities of peptidergic neurons. Neuroscience 1998; 85: 1209-1222.
44. Wigger A, Neumann ID. Endogenous opioid regulation of stress-induced oxytocin release within the hypothalamic paraventricular nucleus is reversed in late pregnancy: a microdialysis study. Neuroscience 2002; 112: 121-129.
45. Harbuz MS, Lightman SL. Responses of hypothalamic and pituitary mRNA to physical and psychological stress in the rat. J Endocrinol 1989; 122: 705-711.
46. Harbuz MS, Jessop DS, Lightman SL, Chowdrey HS. The effects of restraint or hypertonic saline stress on corticotrophin-releasing factor, arginine vasopressin, and proenkephalin A mRNAs in the CFY, Sprague-Dawley and Wistar strains of rat. Brain Res 1994; 667: 6-12.
47. Makino S, Smith MA, Gold PW. Increased expression of corticotropin-releasing hormone and vasopressin messenger ribonucleic acid (mRNA) in the hypothalamic paraventricular nucleus during repeated stress: association with reduction in glucocorticoid receptor mRNA levels. Endocrinology 1995; 136: 3299-3309.
48. Kant GJ, Leu JR, Anderson SM, Mougey EH. Effects of chronic stress on plasma corticosterone, ACTH and prolactin. Physiol Behav 1987; 40: 775-779.
49. Hashimoto K, Suemaru S, Takao T, Sugawara M, Makino S, Ota Z. Corticotropin-releasing hormone and pituitary-adrenocortical responses in chronically stressed rats. Regul Pept 1988; 23: 117-126.
50. Nomura M, Saito J, Ueta Y, Muglia LJ, Pfaff DW, Ogawa S. Enhanced up-regulation of corticotropin-releasing hormone gene expression in response to restraint stress in the hypothalamic paraventricular nucleus of oxytocin gene-deficient male mice. J Neuroendocrinol 2003; 15: 1054-1061.
51. Miyata S, Itoh T, Lin SH, Ishiyama M, Nakashima T, Kiyohara T. Temporal changes of c-fos expression in oxytocinergic magnocellular neuroendocrine cells of the rat hypothalamus with restraint stress. Brain Res Bull 1995; 37: 391-395.
52. Windle RJ, Kershaw YM, Shanks N, Wood SA, Lightman SL, Ingram CD. Oxytocin attenuates stress-induced c-fos mRNA expression in specific forebrain regions associated with modulation of hypothalamo-pituitary-adrenal activity. J Neurosci 2004; 24: 2974-2982.
53. Patel H, Chowdrey HS, Lightman SL. Lactation abolishes corticotropin-releasing factor-induced oxytocin secretion in the conscious rat. Endocrinology 1991; 128: 725-727.
54. Inenaga K, Yamashita H. Excitation of neurones in the rat paraventricular nucleus in vitro by vasopressin and oxytocin. J Physiol 1986; 370: 165-180.
55. Roland BL, Sawchenko PE. Local origins of some GABAergic projections to the paraventricular and supraoptic nuclei of the hypothalamus in the rat. J Comp Neurol 1993; 332: 123-143.
56. Cullinan WE, Ziegler DR, Herman JP. Functional role of local GABAergic influences on the HPA axis. Brain Struct Funct 2008; 213: 63-72.
57. Bali B, Kovacs KJ. GABAergic control of neuropeptide gene expression in parvocellular neurons of the hypothalamic paraventricular nucleus. Eur J Neurosci 2003; 18: 1518-1526.
58. Cullinan WE. GABA(A) receptor subunit expression within hypophysiotropic CRH neurons: a dual hybridization histochemical study. J Comp Neurol 2000; 419: 344-351.
59. Di S, Tasker JG. Rapid synapse-specific regulation of hypothalamic magnocellular neurons by glucocorticoids. Prog Brain Res 2008; 170: 379-388.
60. Huber D, Veinante P, Stoop R. Vasopressin and oxytocin excite distinct neuronal populations in the central amygdala. Science 2005; 308: 245-248.
61. Amico JA, Mantella RC, Vollmer RR, Li X. Anxiety and stress responses in female oxytocin deficient mice. J Neuroendocrinol 2004; 16: 319-324.
62. Mantella RC, Vollmer RR, Li X, Amico JA. Female oxytocin-deficient mice display enhanced anxiety-related behavior. Endocrinology 2003; 144: 2291-2296.
63. Bernatova I, Rigatto KV, Key MP, Morris M. Stress-induced pressor and corticosterone responses in oxytocin-deficient mice. Exp Physiol 2004; 89: 549-557.
64. Mantella RC, Vollmer RR, Rinaman L, Li X, Amico JA. Enhanced corticosterone concentrations and attenuated Fos expression in the medial amygdala of female oxytocin knockout mice exposed to psychogenic stress. Am J Physiol Regul Integr Comp Physiol 2004; 287: R1494-R1504.
65. Mantella RC, Vollmer RR, Amico JA. Corticosterone release is heightened in food or water deprived oxytocin deficient male mice. Brain Res 2005; 1058: 56-61.