Protective action of NDP-MSH in experimental subarachnoid hemorrhage

Experimental Neurology

Volumn 234, Issue 1, 2012, Pages 230-238

  Gatti, Stefano ^a   Lonati, Caterina ^a   Acerbi, Francesco ^b,c   Sordi, Andrea ^a   Leonardi, Patrizia ^a,c   Carlin, Andrea ^a,c   Gaini, Sergio M ^c   Catania, Anna ^a  

^a FONDAZIONE IRCCS CA GRANDA OSPEDALE MAGGIORE POLICLINICO   (Italy)

^b DEPARTMENT OF NEUROSURGERY   (Italy)

^c UNIVERSITY OF MILAN   (Italy)

Author keywords

Melanocyte stimulating hormone; Basilar artery; Gene expression profiling; Melanocortin; Preconditioning; Subarachnoid hemorrhage

Indexed keywords

ALPHA INTERMEDIN DERIVATIVE; I KAPPA B ALPHA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3;

ANIMAL EXPERIMENT; APOPTOSIS; ARTERY DIAMETER; ARTICLE; BASILAR ARTERY; BLOOD VESSEL PARAMETERS; CISTERNA MAGNA; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; GENE EXPRESSION; GENETIC TRANSCRIPTION; INFLAMMATION; MALE; NEUROPROTECTION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RAT; STRESS; SUBARACHNOID HEMORRHAGE; VASCULAR REMODELING; VASOSPASM;

ALPHA-MSH; ANALYSIS OF VARIANCE; ANIMALS; BASILAR ARTERY; DISEASE MODELS, ANIMAL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; I-KAPPA B PROTEINS; MALE; MAP KINASE SIGNALING SYSTEM; NEUROPROTECTIVE AGENTS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; SUBARACHNOID HEMORRHAGE; VASOSPASM, INTRACRANIAL;

EID: 84857506203     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2011.12.039     Document Type: Article

References (59)

1. Aoki T., Nishimura M. Targeting chronic inflammation in cerebral aneurysms: focusing on NF-kappaB as a putative target of medical therapy. Expert Opin. Ther. Targets 2010, 14:265-273.
2. Blondeau N., Widmann C., Lazdunski M., Heurteaux C. Activation of the nuclear factor-kappaB is a key event in brain tolerance. J. Neurosci. 2001, 21:4668-4677.
3. Borel C.O., McKee A., Parra A., Haglund M.M., Solan A., Prabhakar V., Sheng H., Warner D.S., Niklason L. Possible role for vascular cell proliferation in cerebral vasospasm after subarachnoid hemorrhage. Stroke 2003, 34:427-433.
4. Brzoska T., Luger T.A., Maaser C., Abels C., Bohm M. Alpha-melanocyte-stimulating hormone and related tripeptides: biochemistry, antiinflammatory and protective effects in vitro and in vivo, and future perspectives for the treatment of immune-mediated inflammatory diseases. Endocr. Rev. 2008, 29:581-602.
5. Cahill J., Calvert J.W., Zhang J.H. Mechanisms of early brain injury after subarachnoid hemorrhage. J. Cereb. Blood Flow Metab. 2006, 26:1341-1353.
6. Caruso C., Durand D., Schioth H.B., Rey R., Seilicovich A., Lasaga M. Activation of melanocortin 4 receptors reduces the inflammatory response and prevents apoptosis induced by lipopolysaccharide and interferon-gamma in astrocytes. Endocrinology 2007, 148:4918-4926.
7. Caruso C., Mohn C., Karara A.L., Rettori V., Watanobe H., Schioth H.B., Seilicovich A., Lasaga M. Alpha-melanocyte-stimulating hormone through melanocortin-4 receptor inhibits nitric oxide synthase and cyclooxygenase expression in the hypothalamus of male rats. Neuroendocrinology 2004, 79:278-286.
8. Catania A. The melanocortin system in leukocyte biology. J. Leukoc. Biol. 2007, 81:383-392.
9. Catania A. Neuroprotective actions of melanocortins: a therapeutic opportunity. Trends Neurosci. 2008, 31:353-360.
10. Catania A., Gatti S., Colombo G., Lipton J.M. Targeting melanocortin receptors as a novel strategy to control inflammation. Pharmacol. Rev. 2004, 56:1-29.
11. Catania A., Lipton J.M. Peptide modulation of fever and inflammation within the brain. Ann. N. Y. Acad. Sci. 1998, 856:62-68.
12. Catania A., Lonati C., Sordi A., Gatti S. Detrimental consequences of brain injury on peripheral cells. Brain Behav. Immun. 2009, 23:877-884.
13. Catania A., Lonati C., Sordi A., Leonardi P., Carlin A., Gatti S. The peptide NDP-MSH induces phenotype changes in the heart that resemble ischemic preconditioning. Peptides 2010, 31:116-122.
14. Chen D., Chen J.J., Yin Q., Guan J.H., Liu Y.H. Role of ERK1/2 and vascular cell proliferation in cerebral vasospasm after experimental subarachnoid hemorrhage. Acta Neurochir. (Wien) 2009, 151:1127-1134.
15. de Angelis E., Sahm U.G., Ahmed A.R., Olivier G.W., Notarianni L.J., Branch S.K., Moss S.H., Pouton C.W. Identification of a melanocortin receptor expressed by murine brain microvascular endothelial cells in culture. Microvasc. Res. 1995, 50:25-34.
16. Delgado R., Carlin A., Airaghi L., Demitri M.T., Meda L., Galimberti D., Baron P., Lipton J.M., Catania A. Melanocortin peptides inhibit production of proinflammatory cytokines and nitric oxide by activated microglia. J. Leukoc. Biol. 1998, 63:740-745.
17. Dirnagl U., Becker K., Meisel A. Preconditioning and tolerance against cerebral ischaemia: from experimental strategies to clinical use. Lancet Neurol. 2009, 8:398-412.
18. Dumont A.S., Dumont R.J., Chow M.M., Lin C.L., Calisaneller T., Ley K.F., Kassell N.F., Lee K.S. Cerebral vasospasm after subarachnoid hemorrhage: putative role of inflammation. Neurosurgery 2003, 53:123-133. (discussion 133-125).
19. Eves P.C., Haycock J.W. Melanocortin signalling mechanisms. Adv. Exp. Med. Biol. 2010, 681:19-28.
20. Fernandez A., Schmidt J.M., Claassen J., Pavlicova M., Huddleston D., Kreiter K.T., Ostapkovich N.D., Kowalski R.G., Parra A., Connolly E.S., Mayer S.A. Fever after subarachnoid hemorrhage: risk factors and impact on outcome. Neurology 2007, 68:1013-1019.
21. Gatti S., Lonati C., Sordi A., Catania A. Protective effects of melanocortins in systemic host reactions. Adv. Exp. Med. Biol. 2010, 681:117-125.
22. Getting S.J. Targeting melanocortin receptors as potential novel therapeutics. Pharmacol. Ther. 2006, 111:1-15.
23. Giuliani D., Mioni C., Altavilla D., Leone S., Bazzani C., Minutoli L., Bitto A., Cainazzo M.M., Marini H., Zaffe D., Botticelli A.R., Pizzala R., Savio M., Necchi D., Schioth H.B., Bertolini A., Squadrito F., Guarini S. Both early and delayed treatment with melanocortin 4 receptor-stimulating melanocortins produces neuroprotection in cerebral ischemia. Endocrinology 2006, 147:1126-1135.
24. Giuliani D., Ottani A., Mioni C., Bazzani C., Galantucci M., Minutoli L., Bitto A., Zaffe D., Botticelli A.R., Squadrito F., Guarini S. Neuroprotection in focal cerebral ischemia owing to delayed treatment with melanocortins. Eur. J. Pharmacol. 2007, 570:57-65.
25. Hadley M.E., Dorr R.T. Melanocortin peptide therapeutics: historical milestones, clinical studies and commercialization. Peptides 2006, 27:921-930.
26. Holloway P.M., Smith H.K., Renshaw D., Flower R.J., Getting S.J., Gavins F.N. Targeting the melanocortin receptor system for anti-stroke therapy. Trends Pharmacol. Sci. 2011, 32:90-98.
27. Huang Q., Tatro J.B. Alpha-melanocyte stimulating hormone suppresses intracerebral tumor necrosis factor-alpha and interleukin-1beta gene expression following transient cerebral ischemia in mice. Neurosci. Lett. 2002, 334:186-190.
28. Ichiyama T., Campbell I.L., Furukawa S., Catania A., Lipton J.M. Autocrine alpha-melanocyte-stimulating hormone inhibits NF-kappaB activation in human glioma. J. Neurosci. Res. 1999, 58:684-689.
29. Ichiyama T., Zhao H., Catania A., Furukawa S., Lipton J.M. Alpha-melanocyte-stimulating hormone inhibits NF-kappaB activation and IkappaBalpha degradation in human glioma cells and in experimental brain inflammation. Exp. Neurol. 1999, 157:359-365.
30. Kozniewska E., Michalik R., Rafalowska J., Gadamski R., Walski M., Frontczak-Baniewicz M., Piotrowski P., Czernicki Z. Mechanisms of vascular dysfunction after subarachnoid hemorrhage. J. Physiol. Pharmacol. 2006, 57(Suppl 11):145-160.
31. Lehotsky J., Burda J., Danielisova V., Gottlieb M., Kaplan P., Saniova B. Ischemic tolerance: the mechanisms of neuroprotective strategy. Anat. Rec. (Hoboken) 2009, 292:2002-2012.
32. Lipton J.M., Catania A. Anti-inflammatory actions of the neuroimmunomodulator alpha-MSH. Immunol. Today 1997, 18:140-145.
33. Lipton J.M., Catania A., Delgado R. Peptide modulation of inflammatory processes within the brain. Neuroimmunomodulation 1998, 5:178-183.
34. Lubrano-Berthelier C., Dubern B., Lacorte J.M., Picard F., Shapiro A., Zhang S., Bertrais S., Hercberg S., Basdevant A., Clement K., Vaisse C. Melanocortin 4 receptor mutations in a large cohort of severely obese adults: prevalence, functional classification, genotype-phenotype relationship, and lack of association with binge eating. J. Clin. Endocrinol. Metab. 2006, 91:1811-1818.
35. Macdonald R.L., Higashida R.T., Keller E., Mayer S.A., Molyneux A., Raabe A., Vajkoczy P., Wanke I., Bach D., Frey A., Marr A., Roux S., Kassell N. Clazosentan, an endothelin receptor antagonist, in patients with aneurysmal subarachnoid haemorrhage undergoing surgical clipping: a randomised, double-blind, placebo-controlled phase 3 trial (CONSCIOUS-2). Lancet Neurol. 2011, 10:618-625.
36. Macdonald R.L., Pluta R.M., Zhang J.H. Cerebral vasospasm after subarachnoid hemorrhage: the emerging revolution. Nat. Clin. Pract. Neurol. 2007, 3:256-263.
37. Maddahi A., Ansar S., Chen Q., Edvinsson L. Blockade of the MEK/ERK pathway with a raf inhibitor prevents activation of pro-inflammatory mediators in cerebral arteries and reduction in cerebral blood flow after subarachnoid hemorrhage in a rat model. J. Cereb. Blood Flow Metab. 2011, 31:144-154.
38. Magnoni S., Stocchetti N., Colombo G., Carlin A., Colombo A., Lipton J.M., Catania A. Alpha-melanocyte-stimulating hormone is decreased in plasma of patients with acute brain injury. J. Neurotrauma 2003, 20:251-260.
39. Mountjoy K.G. Distribution and function of melanocortin receptors within the brain. Adv. Exp. Med. Biol. 2010, 681:29-48.
40. Muceniece R., Dambrova M. Melanocortins in brain inflammation: the role of melanocortin receptor subtypes. Adv. Exp. Med. Biol. 2010, 681:61-70.
41. Muceniece R., Zvejniece L., Liepinsh E., Kirjanova O., Baumane L., Petrovska R., Mutulis F., Mutule I., Kalvinsh I., Wikberg J.E., Dambrova M. The MC3 receptor binding affinity of melanocortins correlates with the nitric oxide production inhibition in mice brain inflammation model. Peptides 2006, 27:1443-1450.
42. Prunell G.F., Mathiesen T., Diemer N.H., Svendgaard N.A. Experimental subarachnoid hemorrhage: subarachnoid blood volume, mortality rate, neuronal death, cerebral blood flow, and perfusion pressure in three different rat models. Neurosurgery 2003, 52:165-175. (discussion 175-166).
43. Rajora N., Boccoli G., Burns D., Sharma S., Catania A.P., Lipton J.M. Alpha-MSH modulates local and circulating tumor necrosis factor-alpha in experimental brain inflammation. J. Neurosci. 1997, 17:2181-2186.
44. Rajora N., Ceriani G., Catania A., Star R.A., Murphy M.T., Lipton J.M. Alpha-MSH production, receptors, and influence on neopterin in a human monocyte/macrophage cell line. J. Leukoc. Biol. 1996, 59:248-253.
45. Ravati A., Ahlemeyer B., Becker A., Klumpp S., Krieglstein J. Preconditioning-induced neuroprotection is mediated by reactive oxygen species and activation of the transcription factor nuclear factor-kappaB. J. Neurochem. 2001, 78:909-919.
46. Sawyer T.K., Sanfilippo P.J., Hruby V.J., Engel M.H., Heward C.B., Burnett J.B., Hadley M.E. 4-Norleucine, 7-d-phenylalanine-alpha-melanocyte-stimulating hormone: a highly potent alpha-melanotropin with ultralong biological activity. Proc. Natl. Acad. Sci. U. S. A. 1980, 77:5754-5758.
47. Scholzen T.E., Brzoska T., Kalden D.H., Hartmeyer M., Fastrich M., Luger T.A., Armstrong C.A., Ansel J.C. Expression of functional melanocortin receptors and proopiomelanocortin peptides by human dermal microvascular endothelial cells. Ann. N. Y. Acad. Sci. 1999, 885:239-253.
48. Shih S.T., Khorram O., Lipton J.M., McCann S.M. Central administration of alpha-MSH antiserum augments fever in the rabbit. Am. J. Physiol. 1986, 250:R803-R806.
49. Star R.A., Rajora N., Huang J., Stock R.C., Catania A., Lipton J.M. Evidence of autocrine modulation of macrophage nitric oxide synthase by alpha-melanocyte-stimulating hormone. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:8016-8020.
50. Stevens R.D., Nyquist P.A. The systemic implications of aneurysmal subarachnoid hemorrhage. J. Neurol. Sci. 2007, 261:143-156.
51. Stevens S.L., Leung P.Y., Vartanian K.B., Gopalan B., Yang T., Simon R.P., Stenzel-Poore M.P. Multiple preconditioning paradigms converge on interferon regulatory factor-dependent signaling to promote tolerance to ischemic brain injury. J. Neurosci. 2011, 31:8456-8463.
52. Suzuki H., Kanamaru K., Tsunoda H., Inada H., Kuroki M., Sun H., Waga S., Tanaka T. Heme oxygenase-1 gene induction as an intrinsic regulation against delayed cerebral vasospasm in rats. J. Clin. Invest. 1999, 104:59-66.
53. Taherzadeh S., Sharma S., Chhajlani V., Gantz I., Rajora N., Demitri M.T., Kelly L., Zhao H., Ichiyama T., Catania A., Lipton J.M. alpha-MSH and its receptors in regulation of tumor necrosis factor-alpha production by human monocyte/macrophages. Am. J. Physiol. 1999, 276:R1289-R1294.
54. Tang Y., Pacary E., Freret T., Divoux D., Petit E., Schumann-Bard P., Bernaudin M. Effect of hypoxic preconditioning on brain genomic response before and following ischemia in the adult mouse: identification of potential neuroprotective candidates for stroke. Neurobiol. Dis. 2006, 21:18-28.
55. Teare K.A., Pearson R.G., Shakesheff K.M., Haycock J.W. Alpha-MSH inhibits inflammatory signalling in Schwann cells. Neuroreport 2004, 15:493-498.
56. Vandesompele J., De Preter K., Pattyn F., Poppe B., Van Roy N., De Paepe A., Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002, 3. (RESEARCH0034).
57. Vellimana A.K., Milner E., Azad T.D., Harries M.D., Zhou M.L., Gidday J.M., Han B.H., Zipfel G.J. Endothelial nitric oxide synthase mediates endogenous protection against subarachnoid hemorrhage-induced cerebral vasospasm. Stroke 2011, 42:776-782.
58. Vikman P., Beg S., Khurana T.S., Hansen-Schwartz J., Edvinsson L. Gene expression and molecular changes in cerebral arteries following subarachnoid hemorrhage in the rat. J. Neurosurg. 2006, 105:438-444.
59. Zhou M.L., Shi J.X., Hang C.H., Cheng H.L., Qi X.P., Mao L., Chen K.F., Yin H.X. Potential contribution of nuclear factor-kappaB to cerebral vasospasm after experimental subarachnoid hemorrhage in rabbits. J. Cereb. Blood Flow Metab. 2007, 27:1583-1592.