Adrenomedullin and the calcitonin receptor-like receptor system mRNA expressions in the rat heart and sensory ganglia in experimentally-induced long-term diabetes

General Physiology and Biophysics

Volumn 33, Issue 2, 2014, Pages 215-225

  Mistrova, Eliska ^a   Wiegand, Silke ^b   Sviglerova, Jitka ^a   Pfeil, Uwe ^b   Kuncova, Jitka ^a   Slavikova, Jana ^a   Kummer, Wolfgang ^b   Dvorakova, Magdalena Chottova ^a  

^a CHARLES UNIVERSITY   (Czech Republic)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

Adrenomedullin; Diabetes; Heart; Receptor activity modifying proteins; Sensory ganglia

Indexed keywords

ADRENOMEDULLIN; CALCITONIN GENE RELATED PEPTIDE; CALCITONIN RECEPTOR LIKE RECEPTOR; MESSENGER RNA; OLIGONUCLEOTIDE; RECEPTOR ACTIVITY MODIFYING PROTEIN 3;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; DIABETIC CARDIOMYOPATHY; DORSAL ROOT; FEMALE; GANGLION; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; HEART; HEART LEFT VENTRICLE; HEART RIGHT ATRIUM; HEART RIGHT VENTRICLE; NONHUMAN; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SENSORY GANGLION; SENSORY NERVE CELL; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; UPREGULATION;

ADRENOMEDULLIN; ANIMALS; CALCITONIN RECEPTOR-LIKE PROTEIN; DIABETES MELLITUS, EXPERIMENTAL; FEMALE; GANGLIA, SENSORY; GENE EXPRESSION REGULATION; MYOCARDIUM; RATS; RATS, WISTAR; RNA, MESSENGER; SIGNAL TRANSDUCTION;

EID: 84904874290     PISSN: 02315882     EISSN: 13384325     Source Type: Journal    
DOI: 10.4149/gpb_2013073     Document Type: Article

References (51)

1. Adeghate E. (2004): Molecular and cellular basis of the aetiology and management of diabetic cardiomyopathy: a short review. Mol. Cell. Biochem. 261, 187-191 http://dx.doi.org/10.1023/B:MCBI.0000028755.86521.11
2. Belai A., Calcutt N. A., Carrington A. L., Diemel L. T., Tomlinso D. R., Burnstock C. (1996): Enteric neuropeptides in streptozotocin- diabetic rats; effects of insulin and aldose reductase inhibition. J. Auton. Nerv. Syst. 58, 163-169 http://dx.doi.org/10.1016/0165-1838(95)00129-8
3. Brain S. D., Grant A. D. (2004): Vascular actions of calcitonin gene-related peptide and adrenomedullin. Physiol. Rev. 84, 903-934 http://dx.doi.org/10.1152/physrev.00037.2003
4. Bunton D. C., Petrie M. C., Hillier C., Johnston F., McMurray J. J. (2004): The clinical relevance of adrenomedullin: a promising profile? Pharmacol. Ther. 103, 179-201 http://dx.doi.org/10.1016/j.pharmthera.2004.07.002
5. Chakravarty P., Suthar T. P., Coppock H. A., Nicholl C. G., Bloom S. R., Legon S., Smith D. M. (2000): CGRP and adrenomedullin binding correlates with transcript levels for calcitonin receptorlike receptor (CRLR) and receptor activity modifying proteins (RAMPs) in rat tissues. Br. J. Pharmacol. 130, 189-195 http://dx.doi.org/10.1038/sj.bjp.0702975
6. Chottova Dvorakova M., Kuncova J., Pfeil U., McGregor G. P., Sviglerova J., Slavikova J., Kummer W. (2005): Cardiomyopathy in streptozotocin-induced diabetes involves intra-axonal accumulation of calcitonin gene-related peptide and altered expression of its receptor in rats. Neuroscience 134, 51-58 http://dx.doi.org/10.1016/j.neuroscience.2005.03.058
7. Cormier-Regard S., Nguyen S. V., Claycomb W. C. (1998): Adrenomedullin gene expression is developmentally regulated and induced by hypoxia in rat ventricular cardiac myocytes. J. Biol. Chem. 273, 17787-17792 http://dx.doi.org/10.1074/jbc.273.28.17787
8. Cottrell G. S., Roosterman D., Marvizon J. C., Song B., Wick E., Pikios S., Wong H., Berthelier C., Tang Y., Sternini C., Bunnett N. W., Grady E. F. (2005): Localization of calcitonin receptorlike receptor and receptor activity modifying protein 1 in enteric neurons, dorsal root ganglia, and the spinal cord of the rat. J. Comp. Neurol. 490, 239-255 http://dx.doi.org/10.1002/cne.20669
9. Cueille C., Pidoux E., de Vernejoul M. C., Ventura-Clapier R., Garel J. M. (2002): Increased myocardial expression of RAMP1 and RAMP3 in rats with chronic heart failure. Biochem. Biophys. Res. Commun. 294, 340-346 http://dx.doi.org/10.1016/S0006-291X(02)00487-4
10. Dobrzynski E., Montanari D., Agata J., Zhu J., Chao J., Chao L. (2002): Adrenomedullin improves cardiac function and prevents renal damage in streptozotocin-induced diabetic rats. Am. J. Physiol. Endocrinol. Metab. 283, E1291-1298
11. Fernández A. P., Serrano J., Martínez-Murillo R., Martínez A. (2010): Lack of adrenomedullin in the central nervous system results in apparently paradoxical alterations on pain sensitivity. Endocrinology 151, 4908-4915 http://dx.doi.org/10.1210/en.2010-0121
12. Fischer A., McGregor G. P., Saria A., Philippin B., Kummer W. (1996): Induction of tachykinin gene and peptide expression in guinea pig nodose primary afferent neurons by allergic airway inflammation. J. Clin. Invest. 98, 2284-2291 http://dx.doi.org/10.1172/JCI119039
13. Fu L. W., Longhurst J. C. (2009): Regulation of cardiac afferent excitability in ischemia. Handb. Exp. Pharmacol. 194, 185-225 http://dx.doi.org/10.1007/978-3-540-79090-7-6
14. García-Unzueta M. T., Montalban C., Pesquera C., Berrazueta J. R., Amado J. A. (1998): Plasma adrenomedullin levels in type 1 diabetes. Relationship with clinical parameters. Diabetes Care 21, 999-1003 http://dx.doi.org/10.2337/diacare.21.6.999
15. Gardiner S. M., Kemp P. A., March J. E., Bennett T. (1995): Regional haemodynamic effects of human and rat adrenomedullin in conscious rats. Br. J. Pharmacol. 114, 584-591 http://dx.doi.org/10.1111/j.1476-5381.1995.tb17179.x
16. Gibbons C., Dackor R, Dunworth W., Fritz-Six K., Caron K. M. (2007): Receptor activity-modifying proteins: RAMPing up adrenomedullin signaling. Mol. Endocrinol. 21, 783-796 http://dx.doi.org/10.1210/me.2006-0156
17. Guić M. M., Kosta V., Aljinović J., Sapunar D., Grković I. (2010): Characterization of spinal afferent neurons projecting to different chambers of the rat heart. Neurosci. Lett. 469, 314-318 http://dx.doi.org/10.1016/j.neulet.2009.12.016
18. Hayat S. A., Patel B., Khattar R. S., Malik R. A. (2004): Diabetic cardiomyopathy: mechanisms, diagnosis and treatment. Clin. Sci. (Lond) 107, 539-557 http://dx.doi.org/10.1042/CS20040057
19. Hayakawa T., Kuwahara-Otani S., Maeda S., Tanak K., Seki M. (2011): Projections of calcitonin gene-related peptide immunoreactive neurons in the vagal ganglia of the rat. J. Chem. Neuroanat. 41, 55-62 http://dx.doi.org/10. 1016/j.jchemneu.2010.11.003
20. Hinson J. P., Kapas S., Smith D. M. (2000): Adrenomedullin, a multifunctional regulatory peptide. Endocr. Rev. 21, 138-167
21. He R. X., Gu C. L., Shen F., Zhang X. M. (2007): Changes in expression of adrenomedullin in the myocardium of streptozotocin- induced diabetic rats. Chin. Med. J. (Engl) 120, 187-191
22. Hong Y., Liu Y., Chabot J. G, Fournier A., Quirion R. (2009): Upregulation of adrenomedullin in the spinal cord and dorsal root ganglia in the early phase of CFA-induced inflammation in rats. Pain 146, 105-113 http://dx.doi.org/10.1016/j.pain.2009.07.015
23. Horio T., Nishikimi T., Yoshihara F., Matsuo H., Takishita S., Kangawa K. (1999): Effects of adrenomedulin on cultured rat cardiac myocytes and fibroblasts. Eur. J. Pharmacol. 382, 1-9 http://dx.doi.org/10.1016/S0014- 2999(99)00559-2
24. Ihara T., Ikeda U., Tate Y., Ishibashi S., Shimada K. (2000): Positive inotropic effects of adrenomedullin on rat papillary muscle. Eur. J. Pharmacol. 390, 167-172 http://dx.doi.org/10.1016/S0014-2999(00)00011-X
25. Jougasaki M., Rodeheffer R. J., Redfield M. M., Yamamoto K., Wei C. M., McKinley L. J., Burnett J. C. Jr. (1996): Cardiac secretion of adrenomedullin in human heart failure. J. Clin. Invest. 97, 2370-2376 http://dx.doi.org/10.1172/ JCI118680
26. Karanth S. S., Springall D. R., Francavilla S., Mirrlees D. J., Polak J. M. (1990). Early increase in CGRP- and VIP-immunoreactive nerves in the skin of streptozotocin-induced diabetic rats. Histochemistry 94, 659-666 http://dx.doi.org/10.1007/BF00271994
27. Kitamura K., Kangawa K., Kawamoto M., Ichiki Y., Nakamura S., Matsuo H., Eto T. (1993): Adrenomedullin: A novel hypotensive peptide isolated from human pheochromocytoma. Biochem. Biophys. Res. Commun. 192, 553-560 http://dx.doi.org/10.1006/bbrc.1993.1451
28. Kuwasako K., Kitamura K., Nagata S., Hikosaka T., Takei Y., Kato J. (2011): Shared and separate functions of the RAMP-based adrenomedullin receptors. Peptides 32, 1540-1550 http://dx.doi.org/10.1016/j.peptides.2011.05. 022
29. Marfurt C. F., Echtenkamp S. F. (1995): The effect of diabetes on neuropeptide content in the rat cornea and iris. Invest. Ophthalmol. Vis. Sci. 36, 1100-1106
30. Nishikimi T., Tadokoro K., Mori Y., Wang X., Akimoto K., Yoshihara F., Minamino N., Kangawa K., Matsuoka H. (2003): Ventricular adrenomedullin system in the transition from LVH to heart failure in rats. Hypertension 41, 512-518 http://dx.doi.org/10.1161/01.HYP.0000053447.64213.C4
31. Oie E., Vinge L. E., Yndestad A., Sandberg C., Grogaard H. K., Attramadal H. (2000): Induction of a myocardial adrenomedullin signaling system during ischemic heart failure in rats. Circulation 101, 415-422 http://dx.doi.org/10. 1161/01.CIR.101.4.415
32. Oie E., Vinge L. E., Andersen G. O., Yndestad A., Krobert K. A., Sandberg C., Ahmed M. S., Haug T., Levy F. O., Skomedal T., Attramadal H. (2005): RAMP2 and RAMP3 mRNA levels are increased in failing rat cardiomyocytes and associated with increased responsiveness to adrenomedullin. J. Mol. Cell. Cardiol. 38, 145-151 http://dx.doi.org/10.1016/j.yjmcc.2004.10.009
33. Pan C. S., Jiang W., Wu S. Y., Zhao J., Pang Y. Z., Tang C. S., Qi Y. F. (2006): Potentiated response to adrenomedullin in myocardia and aortas in spontaneously hypertensive rat. Basic Res. Cardiol. 101, 193-203 http://dx.doi.org/10.1007/s00395-005-0583-y
34. Pfeil U., Paddenberg R., Kummer W. (2006): Mitochondrial regulation of hypoxia-induced increase of adrenomedullin mRNA in HL-1 cells. Biochem. Biophys. Res. Commun. 343, 885-892 http://dx.doi.org/10.1016/j.bbrc.2006.03.042
35. Rakieten N., Rakieten M. L., Nadkarni M. V. (1963): Studies on the diabetogenic action of streptozotocin. Cancer Chemother. Rep. 29, 91-98
36. Regalia J., Cai F., Helke C. (2002): Streptozotocin-induced diabetes and the neurochemistry of vagal afferent neurons. Brain Res. 938, 7-14 http://dx.doi.org/10.1016/S0006-8993(02)02456-3
37. Rittenhouse P. A., Marchand J. E., Chen J., Kream R. M., Leeman S. E. (1996): Streptozotocin-induced diabetes is associated with altered expression of peptide-encoding mRNAs in rat sensory neurons. Peptides 17, 1017-1022 http://dx.doi.org/10.1016/0196-9781(96)00129-5
38. Ruzicska E., Foldes G., Lako-Futo Z., Sarman B., Wellmann J., Szenasi G., Tulassay Z., Ruskoaho H., Toth M., Somogyi A. (2004): Cardiac gene expression of natriuretic substances is altered in streptozotocin-induced diabetes during angiotensin II-induced pressure overload. J. Hypertens. 22, 1191-1200 http://dx.doi.org/10.1097/00004872-200406000-00021
39. Saito A., Kimura S., Goto K. (1986): Calcitonin gene-related peptide as potential neurotransmitter in guinea-pig right atrium. Am. J. Physiol. 250, H693-698
40. Shimekake Y., Nagata K., Ohta S., Kambayashi Y., Teraoka H., Kitamura K., Eto T., Kangawa K., Matsuo H. (1995): Adrenomedullin stimulates two signal transduction pathways, cAMP accumulation and Ca2+ mobilization, in bovine aortic endothelial cells. J. Biol. Chem. 270, 4412-4417 http://dx.doi.org/10.1074/jbc. 270.9.4412
41. Shimosawa T., Matsui H., Xing G., Itamura K., Ando K., Fujita T. (2003): Organ-protective effects of adrenomedullin. Hypertens. Res. 26, S109-112 http://dx.doi.org/10.1291/hypres.26.S109
42. Skopek P., Hynie S., Chottova Dvorakova M., Sida P., Slavikova J., Mistrova E., Klenerova V. (2012): Effects of acute stressors on the expression of oxytocin receptor mRNA in hearts of rats with different activity of HPA axis. Neuro Endocrinol. Lett. 33, 101-109
43. Tang F., Hwang I. S., Wong M.P, Li Y. Y. (2007): Adrenomedullin gene expression and peptide levels in the heart and blood vessels of streptozotocin-diabetic rats. Horm. Metab. Res. 39, 3-8 http://dx.doi.org/10. 1055/s-2007-956517
44. Tixier E., Leconte C., Touzani O., Roussel S., Petit E., Bernaudin M. (2008): Adrenomedullin protects neurons against oxygen glucose deprivation stress in an autocrine and paracrine manner. J. Neurochem. 106, 1388-1403 http://dx.doi.org/10.1111/j.1471-4159.2008.05494.x
45. Toth C., Martinez J., Zochodne D. W. (2007): AGE, diabetes, and the nervous system. Curr. Mol. Med. 7, 766-776 http://dx.doi.org/10.2174/ 156652407783220705
46. Totsune K., Takahashi K., Mackenzie H. S., Murakami O., Arihara Z., Sone M., Mouri T., Brenner B. M., Ito S. (2000): Increased gene expression of adrenomedullin and adrenomedullin-receptor complexes, receptor-activity modifying protein (RAMP)2 and calcitonin-receptor-like receptor (CRLR) in the hearts of rats with congestive heart failure. Clin. Sci. (Lond) 99, 541-546 http://dx.doi.org/10.1042/CS20000108
47. Tsuruda T., Kato J., Kitamura K., Kuwasako K., Imamura T., Koiwaya Y., Tsuji T., Kangawa K. (1998): Adrenomedullin: a possible autocrine or paracrine inhibitor of hypertrophy of cardiomyocytes. Hypertension 31, 505-510 http://dx.doi.org/10.1161/01.HYP.31.1.505
48. Tsuruda T., Kato J., Kitamura K., Imamura T., Koiwaya Y., Kangawa K., Komoro I., Yazaki Y., Eto T. (2000): Enhanced adrenomedullin production by mechanical stretching in cultured rat cardiomyocytes. Hypertension 35, 1210-1214 http://dx.doi.org/10.1161/01.HYP.35.6.1210
49. Wharton J., Gulbenkian S., Mulderry P. K., Ghatei M. A., McGregor G. P., Bloom S. R., Polak J. M. (1986). Capsaicin induces a depletion of calcitonin gene-related peptide (CGRP)-immunoreactive nerves in the cardiovascular system of the guinea pig and rat. J. Auton. Nerv. Syst. 16, 289-309 http://dx.doi.org/10.1016/0165-1838(86)90035-4
50. Zochodne D. W., Verge V., Cheng M. C., Sun J., Johnstan J. (2001): Does diabetes target ganglion neurones? Progressive sensory neurone involvement in long-term experimental diabetes. Brain 124, 2319-2334 http://dx.doi.org/10.1093/ brain/124.11.2319
51. Zhao Y., Bell D., Smith L. R., Zhao L., Devine A. B., McHenry E. M., Nicholls D. P., McDermott B.S. (2006): Differential expression of components of the cardiomyocyte adrenomedullin/intermedin receptor system following blood pressure reduction in nitric oxide-deficient hypertension. J. Pharmacol. Exp. Ther. 316, 1269-1281 http://dx.doi.org/10.1124/jpet.105.092783