Pituitary adenylate cyclase-activating polypeptide ameliorates experimental acute ileitis and extra-intestinal sequelae

PLoS ONE

Volumn 9, Issue 9, 2014, Pages

  Heimesaat, Markus M ^a   Dunay, Ildiko R ^b   Schulze, Silvia ^a   Fischer, André ^a   Grundmann, Ursula ^a   Alutis, Marie ^a   Kühl, Anja A ^a   Tamas, Andrea ^c   Toth, Gabor ^d   Dunay, Miklos P ^e   Göbel, Ulf B ^a   Reglodi, Dora ^c   Bereswill, Stefan ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b OTTO VON GUERICKE UNIVERSITY   (Germany)

^c UNIVERSITY OF PÉCS   (Hungary)

^d UNIVERSITY OF SZEGED   (Hungary)

^e SZENT ISTVÁN UNIVERSITY   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE; INTERLEUKIN 10; INTERLEUKIN 22; INTERLEUKIN 23P19; INTERLEUKIN 4; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; NITRIC OXIDE; PLACEBO; TRANSCRIPTION FACTOR FOXP3; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BLOOD LEVEL; CHEMOPROPHYLAXIS; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOKINE RELEASE; DOSE TIME EFFECT RELATION; DOWN REGULATION; DRUG EFFECT; ENTERITIS; EX VIVO STUDY; EXTRA INTESTINAL SEQUELAE; FEMALE; GENE EXPRESSION REGULATION; HISTOPATHOLOGY; ILEUS; IMMUNOHISTOCHEMISTRY; IMMUNOMODULATION; INTESTINE PARAMETERS; LIVER LEVEL; MACROPHAGE; MESENTERY LYMPH NODE; MONOCYTE; MOUSE; NEUTROPHIL; NONHUMAN; OXIDATIVE STRESS; PARASITE LOAD; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; SMALL INTESTINAL INFLAMMATION; SMALL INTESTINE LENGTH; SURVIVAL RATE; SURVIVAL TIME; SYSTEMIC DISEASE; TIME TO TREATMENT; UPREGULATION; WEIGHT REDUCTION; ANIMAL; C57BL MOUSE; CELLULAR IMMUNITY; DRUG EFFECTS; ILEITIS; IMMUNOLOGY; PARASITOLOGY; PATHOLOGY; SMALL INTESTINE; TIME; TOXOPLASMOSIS;

ANIMALS; ILEITIS; IMMUNITY, CELLULAR; INTESTINE, SMALL; MICE; MICE, INBRED C57BL; PARASITE LOAD; PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE; TIME FACTORS; TOXOPLASMOSIS;

EID: 84907200231     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0108389     Document Type: Article

References (57)

1. Miyata A, Arimura A, Dahl RR, Minamino N, Uehara A, et al. (1989) Isolation of a novel 38 residue-hypothalamic polypeptide which stimulates adenylate cyclase in pituitary cells. Biochem Biophys Res Commun 164: 567-574.
2. Vaudry D, Gonzalez BJ, Basille M, Yon L, Fournier A, et al. (2000) Pituitary adenylate cyclase-activating polypeptide and its receptors: from structure to functions. Pharmacol Rev 52: 269-324.
3. Gomariz RP, Juarranz Y, Abad C, Arranz A, Leceta J, et al. (2006) VIP-PACAP system in immunity: new insights for multitarget therapy. Ann N Y Acad Sci 1070: 51-74.
4. Abad C, Gomariz RP, Waschek JA (2006) Neuropeptide mimetics and antagonists in the treatment of inflammatory disease: focus on VIP and PACAP. Curr Top Med Chem 6: 151-163.
5. Vaudry D, Falluel-Morel A, Bourgault S, Basille M, Burel D, et al. (2009) Pituitary adenylate cyclase-activating polypeptide and its receptors: 20 years after the discovery. Pharmacol Rev 61: 283-357.
6. Abad C, Martinez C, Leceta J, Gomariz RP, Delgado M (2001) Pituitary adenylate cyclase-activating polypeptide inhibits collagen-induced arthritis: an experimental immunomodulatory therapy. J Immunol 167: 3182-3189.
7. Kato H, Ito A, Kawanokuchi J, Jin S, Mizuno T, et al. (2004) Pituitary adenylate cyclase-activating polypeptide (PACAP) ameliorates experimental autoimmune encephalomyelitis by suppressing the functions of antigen presenting cells. Mult Scler 10: 651-659.
8. Nemetz N, Abad C, Lawson G, Nobuta H, Chhith S, et al. (2008) Induction of colitis and rapid development of colorectal tumors in mice deficient in the neuropeptide PACAP. Int J Cancer 122: 1803-1809.
9. Azuma YT, Hagi K, Shintani N, Kuwamura M, Nakajima H, et al. (2008) PACAP provides colonic protection against dextran sodium sulfate induced colitis. J Cell Physiol 216: 111-119.
10. Abad C, Martinez C, Juarranz MG, Arranz A, Leceta J, et al. (2003) Therapeutic effects of vasoactive intestinal peptide in the trinitrobenzene sulfonic acid mice model of Crohn's disease. Gastroenterology 124: 961-971.
11. Podolsky DK (2002) The current future understanding of inflammatory bowel disease. Best Pract Res Clin Gastroenterol 16: 933-943.
12. Podolsky DK (2002) Inflammatory bowel disease. N Engl J Med 347: 417-429.
13. Basset C, Holton J (2002) Inflammatory bowel disease: is the intestine a Trojan horse? Sci Prog 85: 33-56.
14. Liesenfeld O, Kosek J, Remington JS, Suzuki Y (1996) Association of CD4+ T cell-dependent, interferon-gamma-mediated necrosis of the small intestine with genetic susceptibility of mice to peroral infection with Toxoplasma gondii. J Exp Med 184: 597-607.
15. Khan IA, Schwartzman JD, Matsuura T, Kasper LH (1997) A dichotomous role for nitric oxide during acute Toxoplasma gondii infection in mice. Proc Natl Acad Sci U S A 94: 13955-13960.
16. Mennechet FJ, Kasper LH, Rachinel N, Li W, Vandewalle A, et al. (2002) Lamina propria CD4+ T lymphocytes synergize with murine intestinal epithelial cells to enhance proinflammatory response against an intracellular pathogen. J Immunol 168: 2988-2996.
17. Vossenkamper A, Struck D, Alvarado-Esquivel C, Went T, Takeda K, et al. (2004) Both IL-12 and IL-18 contribute to small intestinal Th1-type immunopathology following oral infection with Toxoplasma gondii, but IL-12 is dominant over IL-18 in parasite control. Eur J Immunol 34: 3197-3207.
18. Buzoni-Gatel D, Schulthess J, Menard LC, Kasper LH (2006) Mucosal defences against orally acquired protozoan parasites, emphasis on Toxoplasma gondii infections. Cell Microbiol 8: 535-544.
19. Munoz M, Heimesaat MM, Danker K, Struck D, Lohmann U, et al. (2009) Interleukin (IL)-23 mediates Toxoplasma gondii-induced immunopathology in the gut via matrixmetalloproteinase-2 and IL-22 but independent of IL-17. J Exp Med 206: 3047-3059.
20. Jankovic D, Kugler DG, Sher A (2010) IL-10 production by CD4+ effector T cells: a mechanism for self-regulation. Mucosal Immunol 3: 239-246.
21. Heimesaat MM, Bereswill S, Fischer A, Fuchs D, Struck D, et al. (2006) Gramnegative bacteria aggravate murine small intestinal Th1-type immunopathology following oral infection with Toxoplasma gondii. J Immunol 177: 8785-8795.
22. Heimesaat MM, Fischer A, Jahn HK, Niebergall J, Freudenberg M, et al. (2007) Exacerbation of murine ileitis by Toll-like receptor 4 mediated sensing of lipopolysaccharide from commensal Escherichia coli. Gut 56: 941-948.
23. Erridge C, Duncan SH, Bereswill S, Heimesaat MM (2010) The induction of colitis and ileitis in mice is associated with marked increases in intestinal concentrations of stimulants of TLRs 2, 4, and 5. PLoS One 5: e9125.
24. Liesenfeld O (2002) Oral infection of C57BL/6 mice with Toxoplasma gondii: a new model of inflammatory bowel disease? J Infect Dis 185 Suppl 1: S96-101.
25. Munoz M, Liesenfeld O, Heimesaat MM (2012) Immunology of Toxoplasma gondii. Immunol Rev 240: 269-285.
26. Heimesaat MM, Plickert R, Fischer A, Gobel UB, Bereswill S (2013) Can microbiota transplantation abrogate murine colonization resistance against Campylobacter jejuni? Eur J Microbiol Immunol (Bp) 3: 36-43.
27. Bereswill S, Munoz M, Fischer A, Plickert R, Haag LM, et al. (2010) Antiinflammatory effects of resveratrol, curcumin and simvastatin in acute small intestinal inflammation. PLoS One 5: e15099.
28. Heimesaat MM, Fischer A, Siegmund B, Kupz A, Niebergall J, et al. (2007) Shift towards pro-inflammatory intestinal bacteria aggravates acute murine colitis via Toll-like receptors 2 and 4. PLoS One 2: e662.
29. Bereswill S, Fischer A, Plickert R, Haag LM, Otto B, et al. (2011) Novel Murine Infection Models Provide Deep Insights into the "Menage a Trois" of Campylobacter jejuni, Microbiota and Host Innate Immunity. PLoS One 6: e20953.
30. Haag LM, Fischer A, Otto B, Plickert R, Kuhl AA, et al. (2012) Campylobacter jejuni induces acute enterocolitis in gnotobiotic IL-102/2 mice via Toll-likereceptor- 2 and -4 signaling. PLoS One 7: e40761.
31. Moody TW, Ito T, Osefo N, Jensen RT (2011) VIP and PACAP: recent insights into their functions/roles in physiology and disease from molecular and genetic studies. Curr Opin Endocrinol Diabetes Obes 18: 61-67.
32. Delgado M, Anderson P, Garcia-Salcedo JA, Caro M, Gonzalez-Rey E (2009) Neuropeptides kill African trypanosomes by targeting intracellular compartments and inducing autophagic-like cell death. Cell Death Differ 16: 406-416.
33. Gonzalez-Rey E, Chorny A, Delgado M (2006) VIP: an agent with license to kill infective parasites. Ann N Y Acad Sci 1070: 303-308.
34. Delgado M, De la Fuente M, Martinez C, Gomariz RP (1995) Pituitary adenylate cyclase-activating polypeptides (PACAP27 and PACAP38) inhibit the mobility of murine thymocytes and splenic lymphocytes: comparison with VIP and implication of cAMP. J Neuroimmunol 62: 137-146.
35. Ganea D, Delgado M (2002) Vasoactive intestinal peptide (VIP) and pituitary adenylate cyclase-activating polypeptide (PACAP) as modulators of both innate and adaptive immunity. Crit Rev Oral Biol Med 13: 229-237.
36. Laskin DL, Pendino KJ (1995) Macrophages and inflammatory mediators in tissue injury. Annu Rev Pharmacol Toxicol 35: 655-677.
37. Delgado M, Ganea D (2001) Inhibition of endotoxin-induced macrophage chemokine production by vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide in vitro and in vivo. J Immunol 167: 966-975.
38. Tan YV, Abad C, Lopez R, Dong H, Liu S, et al. (2009) Pituitary adenylyl cyclase-activating polypeptide is an intrinsic regulator of Treg abundance and protects against experimental autoimmune encephalomyelitis. Proc Natl Acad Sci U S A 106: 2012-2017.
39. Tan YV, Abad C, Wang Y, Lopez R, Waschek JA (2013) Pituitary adenylate cyclase activating peptide deficient mice exhibit impaired thymic and extrathymic regulatory T cell proliferation during EAE. PLoS One 8: e61200.
40. Delgado M, Gonzalez-Rey E, Ganea D (2006) Vasoactive intestinal peptide: the dendritic cellRregulatory T cell axis. Ann N Y Acad Sci 1070: 233-238.
41. Delgado M, Gonzalez-Rey E, Ganea D (2005) The neuropeptide vasoactive intestinal peptide generates tolerogenic dendritic cells. J Immunol 175: 7311-7324.
42. Delgado M (2009) Generating tolerogenic dendritic cells with neuropeptides. Hum Immunol 70: 300-307.
43. Delgado M, Leceta J, Gomariz RP, Ganea D (1999) Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide stimulate the induction of Th2 responses by up-regulating B7.2 expression. J Immunol 163: 3629-3635.
44. Bereswill S, Kuhl AA, Alutis M, Fischer A, Mohle L, et al. (2014) The impact of Toll-like-receptor-9 on intestinal microbiota composition and extra-intestinal sequelae in experimental Toxoplasma gondii induced ileitis. Gut Pathog 6: 19.
45. Heimesaat MM, Dunay IR, Fuchs D, Trautmann D, Fischer A, et al. (2011) Selective gelatinase blockage ameliorates acute DSS colitis. Eur J Microbiol Immunol (Bp) 1: 228-236.
46. Delgado M, Munoz-Elias EJ, Gomariz RP, Ganea D (1999) Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide enhance IL-10 production by murine macrophages: in vitro and in vivo studies. J Immunol 162: 1707-1716.
47. Delgado M, Abad C, Martinez C, Juarranz MG, Leceta J, et al. (2003) PACAP in immunity and inflammation. Ann N Y Acad Sci 992: 141-157.
48. Arimura A, Li M, Batuman V (2006) Treatment of renal failure associated with multiple myeloma and other diseases by PACAP-38. Ann N Y Acad Sci 1070: 1-4.
49. Khan AM, Li M, Brant E, Maderdrut JL, Majid DS, et al. (2011) Renoprotection with pituitary adenylate cyclase-activating polypeptide in cyclosporine A-induced nephrotoxicity. J Investig Med 59: 793-802.
50. Szakaly P, Laszlo E, Kovacs K, Racz B, Horvath G, et al. (2011) Mice deficient in pituitary adenylate cyclase activating polypeptide (PACAP) show increased susceptibility to in vivo renal ischemia/reperfusion injury. Neuropeptides 45: 113-121.
51. Horvath G, Brubel R, Kovacs K, Reglodi D, Opper B, et al. (2011) Effects of PACAP on oxidative stress-induced cell death in rat kidney and human hepatocyte cells. J Mol Neurosci 43: 67-75.
52. Ji H, Zhang Y, Shen XD, Gao F, Huang CY, et al. (2013) Neuropeptide PACAP in mouse liver ischemia and reperfusion injury: immunomodulation by the cAMP-PKA pathway. Hepatology 57: 1225-1237.
53. Elekes K, Sandor K, Moricz A, Kereskai L, Kemeny A, et al. (2011) Pituitary adenylate cyclase-activating polypeptide plays an anti-inflammatory role in endotoxin-induced airway inflammation: in vivo study with gene-deleted mice. Peptides 32: 1439-1446.
54. Yoshihara S, Yamada Y, Abe T, Kashimoto K, Linden A, et al. (2004) Longlasting smooth-muscle relaxation by a novel PACAP analogue in human bronchi. Regul Pept 123: 161-165.
55. Mao SS, Hua R, Zhao XP, Qin X, Sun ZQ, et al. (2012) Exogenous administration of PACAP alleviates traumatic brain injury in rats through a mechanism involving the TLR4/MyD88/NF-kappaB pathway. J Neurotrauma 29: 1941-1959.
56. Delgado M, Gomariz RP, Martinez C, Abad C, Leceta J (2000) Antiinflammatory properties of the type 1 and type 2 vasoactive intestinal peptide receptors: role in lethal endotoxic shock. Eur J Immunol 30: 3236-3246.
57. Delgado M, Martinez C, Pozo D, Calvo JR, Leceta J, et al. (1999) Vasoactive intestinal peptide (VIP) and pituitary adenylate cyclase-activation polypeptide (PACAP) protect mice from lethal endotoxemia through the inhibition of TNFalpha and IL-6. J Immunol 162: 1200-1205.