The surging role of Chromogranin A in cardiovascular homeostasis

Frontiers in Chemistry

Volumn 2, Issue AUG, 2014, Pages

  Tota, Bruno ^a   Angelone, Tommaso ^a   Cerra, Maria C ^a  

^a UNIVERSITY OF CALABRIA   (Italy)

Author keywords

Adreno sympathetic control; Cardioprotection; Catestatin; Chromogranin A; Endothelial signaling; Serpinin; Vasoactive peptides; Vasostatin 1

Indexed keywords

EID: 84987619288     PISSN: None     EISSN: 22962646     Source Type: Journal    
DOI: 10.3389/fchem.2014.00064     Document Type: Review

References (101)

1. Abi-Gerges, N., Fischmeister, R., and Méry, P. F. (2001). G protein-mediated inhibitory effect of a nitric oxide donor on the L-type Ca2+ current in rat ventricular myocytes. J. Physiol. 1, 117-130. doi: 10.1111/j.1469-7793.2001.0117j.x
2. Angelone, T., Mazza, R., and Cerra, M. C. (2012a). Chromogranin-A: a multifaceted cardiovascular role in health and disease. Curr. Med. Chem. 24, 4042-4050. doi: 10.2174/092986712802430009
3. Angelone, T., Quintieri, A. M., Brar, B. K., Limchaiyawat, P. T., Tota, B., Mahata, S. K., et al. (2008). The antihypertensive Chromogranin A peptide catestatin acts as a novel endocrine/paracrine modulator of cardiac inotropism and lusitropism. Endocrinology 10, 4780-4793. doi: 10.1210/en.2008-0318
4. Angelone, T., Quintieri, A. M., Pasqua, T., Gentile, S., Tota, B., Mahata, S. K., et al. (2012b). Phosphodiesterase type-2 and NO-dependent S-nitrosylation mediate the cardioinhibition of the antihypertensive catestatin. Am. J. Physiol. Heart Circ. Physiol. 302, H431-H442. doi: 10.1152/ajpheart.00491.2011
5. Angelone, T., and Tota, B. (2012). Editorial: Chromogranin A at the crossroads of health and disease. Curr. Med. Chem. 24, 4039-4041. doi: 10.2174/092986712802430027
6. Bartolomucci, A., Possenti, R., Mahata, S. K., Fischer-Colbrie, R., Loh, Y. P., and Salton, S. R. (2011). The extended granin family: structure, function, and biomedical implications. Endocr. Rev. 6, 755-797. doi: 10.1210/er.2010-0027
7. Bassino, E., Fornero, S., Gallo, M. P., Ramella, R., Mahata, S. K., Tota, B., et al. (2011). A novel catestatin-induced antiadrenergic mechanism triggered by the endothelial PI3K-eNOS pathway in the myocardium. Cardiovasc. Res. 4, 617-624. doi: 10.1093/cvr/cvr129
8. Bell, R. M., and Yellon, D. M. (2003). Bradykinin limits infarction when administered as an adjunct to reperfusion in mouse heart: the role of PI3K, Akt and eNOS. J. Mol. Cell Cardiol. 2, 185-193. doi: 10.1016/S0022-2828(02)00310-3
9. Biswas, N., Curello, E., O'Connor, D. T., and Mahata, S. K. (2010). Chromogranin/secretogranin proteins in murine heart: myocardial production of Chromogranin A fragment catestatin (Chga(364-384)). Cell Tissue Res. 3, 353-361. doi: 10.1007/s00441-010-1059-4
10. Boengler, K. (2011). Ischemia/reperfusion injury: the benefit of having STAT3 in the heart. J. Mol. Cell Cardiol. 4, 587-588. doi: 10.1016/j.yjmcc.2011.01.009
11. Brás-Silva, C., and Leite-Moreira, A. F. (2005). Modulation of the myocardial effects of selective ETB receptor stimulation and its implications for heart failure. Rev. Port. Cardiol. 9, 1125-1133.
12. Brekke, J. F., Osol, G. J., and Helle, K. B. (2002). N-terminal chromogranin-derived peptides as dilators of bovine coronary resistance arteries. Regul. Pept. 2, 93-100. doi: 10.1016/S0167-0115(02)00004-6
13. Cappello, S., Angelone, T., Tota, B., Pagliaro, P., Penna, C., Rastaldo, R., et al. (2007). Human recombinant Chromogranin A-derived vasostatin-1 mimics preconditioning via an adenosine/nitric oxide signaling mechanism. Am. J. Physiol. Heart Circ. Physiol. 1, H719-H727. doi: 10.1152/ajpheart.01352.2006
14. Ceconi, C., Ferrari, R., Bachetti, T., Opasich, C., Volterrani, M., Colombo, B., et al. (2002). Chromogranin A in heart failure; a novel neurohumoral factor and a predictor for mortality. Eur. Heart J. 12, 967-974. doi: 10.1053/euhj.2001.2977
15. Cerra, M. C., De Iuri, L., Angelone, T., Corti, A., and Tota, B. (2006). Recombinant N-terminal fragments of chromogranin-A modulate cardiac function of the Langendorff-perfused rat heart. Basic Res. Cardiol. 1, 43-52. doi: 10.1007/s00395-005-0547-2
16. Cerra, M. C., Gallo, M. P., Angelone, T., Quintieri, A. M., Pulerà E., Filice, E., et al. (2008). The homologous rat Chromogranin A1-64 (rCGA1-64) modulates myocardial and coronary function in rat heart to counteract adrenergic stimulation indirectly via endothelium-derived nitric oxide. FASEB J. 11, 3992-4004. doi: 10.1096/fj.08-110239
17. Chien, K. R., Knowlton, K. U., Zhu, H., and Chien, S. (1991). Regulation of cardiac gene expression during myocardial growth and hypertrophy: molecular studies of an adaptive physiologic response. FASEB J. 5, 3037-3046.
18. Cohn, J. N., and Yellin, A. M. (1984). Learned precise cardiovascular control through graded central sympathetic stimulation. J. Hypertens. Suppl. 2, S77-S79.
19. Colombo, B., Curnis, F., Foglieni, C., Monno, A., Arrigoni, G., and Corti, A. (2002). Chromogranin A expression in neoplastic cells affects tumor growth and morphogenesis in mouse models. Cancer Res. 3, 941-946.
20. Corti, A., Gasparri, A., Chen, F. X., Pelagi, M., Brandazza, A., Sidoli, A., et al. (1996). Characterisation of circulating Chromogranin A in human cancer patients. Br. J. Cancer. 8, 924-932. doi: 10.1038/bjc.1996.183
21. Crippa, L., Bianco, M., Colombo, B., Gasparri, A. M., Ferrero, E., Loh, Y. P., et al. (2013). A new Chromogranin A-dependent angiogenic switch activated by thrombin. Blood 2, 392-402. doi: 10.1182/blood-2012-05-430314
22. Cryer, P. E., Wortsman, J., Shah, S. D., Nowak, R. M., and Deftos, L. J. (1991). Plasma Chromogranin A as a marker of sympathochromaffin activity in humans. Am. J. Physiol. 260 (Pt 21), E243-E246.
23. D'amico, M. A., Ghinassi, B., Izzicupo, P., Manzoli, L., and Di Baldassarre, A. (2014). Biological function and clinical relevance of Chromogranin A and derived peptides. Endocr. Connect. 2, 45-54. doi: 10.1530/EC-14-0027
24. Dieplinger, B., Gegenhuber, A., Haltmayer, M., and Mueller, T. (2009). Evaluation of novel biomarkers for the diagnosis of acute destabilised heart failure in patients with shortness of breath. Heart 18, 1508-1513. doi: 10.1136/hrt.2009.170696
25. Dondossola, E., Gasparri, A. M., Colombo, B., Sacchi, A., Curnis, F., and Corti, A. (2011). Chromogranin A restricts drug penetration and limits the ability of NGR-TNF to enhance chemotherapeutic efficacy. Cancer Res. 17, 5881-5890. doi: 10.1158/0008-5472.CAN-11-1273
26. Ferrero, E., Magni, E., Curnis, F., Villa, A., Ferrero, M. E., and Corti, A. (2002). Regulation of endothelial cell shape and barrier function by Chromogranin A. Ann. N.Y. Acad. Sci. 971, 355-358. doi: 10.1111/j.1749-6632.2002.tb04495.x
27. Ferrero, E., Scabini, S., Magni, E., Foglieni, C., Belloni, D., Colombo, B., et al. (2004). Chromogranin A protects vessels against tumor necrosis factor alpha-induced vascular leakage. FASEB J. 3, 554-556. doi: 10.1096/fj.03-0922fje
28. Fung, M. M., Salem, R. M., Mehtani, P., Thomas, B., Lu, C. F., Perez, B., et al. (2010). Direct vasoactive effects of the Chromogranin A (CHGA) peptide catestatin in humans in vivo. Clin. Exp. Hypertens. 5, 278-287. doi: 10.3109/10641960903265246
29. Giusti, M., Sidoti, M., Augeri, C., Rabitti, C., and Minuto, F. (2004). Effect of short-term treatment with low dosages of the proton-pump inhibitor omeprazole on serum Chromogranin A levels in man. Eur. J. Endocrinol. 3, 299-303. doi: 10.1530/eje.0.1500299
30. Glattard, E., Angelone, T., Strub, J. M., Corti, A., Aunis, D., Tota, B., et al. (2006). Characterization of natural vasostatin-containing peptides in rat heart. FEBS J. 14, 3311-3321. doi: 10.1111/j.1742-4658.2006.05334.x
31. Goetze, J. P., Alehagen, U., Flyvbjerg, A., and Rehfeld, J. F. (2014). Chromogranin A as a biomarker in cardiovascular disease. Biomark Med. 1, 133-140. doi: 10.2217/bmm.13.102
32. Hartell, N. A., Archer, H. E., and Bailey, C. J. (2005). Insulin-stimulated endothelial nitric oxide release is calcium independent and mediated via protein kinase B. Biochem. Pharmacol. 5, 781-790. doi: 10.1016/j.bcp.2004.11.022
33. Hausenloy, D. J. (2009). Signalling pathways in ischaemic postconditioning. Thromb Haemost 4, 626-634. doi: 10.1160/TH08-11-0734
34. Hausenloy, D. J. (2012). Conditioning the heart to prevent myocardial reperfusion injury during PPCI. Eur. Heart. J. Acute Cardiovasc. Care 1, 13-32. doi: 10.1177/2048872612438805
35. Hausenloy, D. J., Lecour, S., and Yellon, D. M. (2011). Reperfusion injury salvage kinase and survivor activating factor enhancement prosurvival signaling pathways in ischemic postconditioning: two sides of the same coin. Antioxid Redox Signal 5, 893-907. doi: 10.1089/ars.2010.3360
36. Helle, K. B., Corti, A., Metz-Boutigue, M. H., and Tota, B. (2007). The endocrine role for Chromogranin A: a prohormone for peptides with regulatory properties. Cell. Mol. Life Sci. 22, 2863-2886. doi: 10.1007/s00018-007-7254-0
37. Ho-Tin-Noé, B., Enslen, H., Doeuvre, L., Corsi, J. M., Lijnen, H. R., and Anglés-Cano, E. (2009). Role of plasminogen activation in neuronal organization and survival. Mol.Cell. Neurosci. 4, 288-295. doi: 10.1016/j.mcn.2009.08.001
38. Hove-Madsen, L., Méry, P. F., Jurevicius, J., Skeberdis, A. V., and Fischmeister, R. (1996). Regulation of myocardial calcium channels by cyclic AMP metabolism. Basic Res. Cardiol. 2, 1-8. doi: 10.1007/BF00795355
39. Hutton, J. C., Davidson, H. W., Grimaldi, K. A., and Peshavaria, M. (1987). Biosynthesis of betagranin in pancreatic beta-cells. Identification of a Chromogranin A-like precursor and its parallel processing with proinsulin. Biochem. J. 2, 449-456.
40. Jansson, A. M., Røsjø, H., Omland, T., Karlsson, T., Hartford, M., Flyvbjerg, A., et al. (2009). Prognostic value of circulating Chromogranin A levels in acute coronary syndromes. Eur. Heart J. 1, 25-32. doi: 10.1093/eurheartj/ehn513
41. Katz, A. M. (1990). Inotropic and lusitropic abnormalities in heart failure. Eur. Heart J. 11 (Suppl. A), 27-31. doi: 10.1093/eurheartj/11.suppl_A.27
42. Kim, T., and Loh, Y. P. (2006). Protease nexin-1 promotes secretory granule biogenesis by preventing granule protein degradation. Mol. Biol. Cell. 2, 789-798. doi: 10.1091/mbc.E05-08-0755
43. Kim, T., Tao-Cheng, J. H., Eiden, L. E., and Loh, Y. P. (2001). Chromogranin A, an "on/off" switch controlling dense-core secretory granule biogenesis. Cell. 4, 499-509. doi: 10.1016/S0092-8674(01)00459-7
44. Koeslag, J. H., Saunders, P. T., and Wessels, J. A. (1999). The chromogranins and the counter-regulatory hormones: do they make homeostatic sense? J. Physiol. 3, 643-649. doi: 10.1111/j.1469-7793.1999.0643s.x
45. Koshimizu, H., Cawley, N. X., Yergy, A. L., and Loh, Y. P. (2011). Role of pGlu-serpinin, a novel Chromogranin A-derived peptide in inhibition of cell death. J. Mol. Neurosci. 2, 294-303. doi: 10.1007/s12031-011-9521-7
46. Koshimizu, H., Kim, T., Cawley, N. X., and Loh, Y. P. (2010). Reprint of: Chromogranin A: a new proposal for trafficking, processing and induction of granule biogenesis. Regul. Pept. 1, 95-101. doi: 10.1016/j.regpep.2010.09.006
47. Krylova, M. I. (2007). Chromogranin A: immunocytochemical localization in secretory granules of frog atrial cardiomyocytes. Tsitologiia 7, 538-543.
48. Kubota, M. (1997). Vasopressin: basic and clinical aspects. Nihon Shinkei Seishin Yakurigaku Zasshi 3, 113-121.
49. Mahapatra, N. R., O'Connor, D. T., Vaingankar, S. M., Hikim, A. P., Mahata, M., Ray, S., et al. (2005). Hypertension from targeted ablation of Chromogranin A can be rescued by the human ortholog. J. Clin. Invest. 7, 1942-1952. doi: 10.1172/JCI24354
50. Mahata, S. K., Kozak, C. A., Szpirer, J., Szpirer, C., Modi, W. S., Gerdes, H. H., et al. (1996). Dispersion of chromogranin/secretogranin secretory protein family loci in mammalian genomes. Genomics 1, 135-139. doi: 10.1006/geno.1996.0171
51. Mahata, S. K., Mahata, M., Fung, M. M., and O'Connor, D. T. (2010). Reprint of: catestatin: a multifunctional peptide from Chromogranin A. Regul. Pept. 1, 52-62. doi: 10.1016/j.regpep.2010.09.007
52. Mahata, S. K., O'Connor, D. T., Mahata, M., Yoo, S. H., Taupenot, L., Wu, H., et al. (1997). Novel autocrine feedback control of catecholamine release. A discrete Chromogranin A fragment is a noncompetitive nicotinic cholinergic antagonist. J. Clin. Invest. 6, 1623-1633. doi: 10.1172/JCI119686
53. Maniatis, N. A., Brovkovych, V., Allen, S. E., John, T. A., Shajahan, A. N., Tiruppathi, C., et al. (2006). Novel mechanism of endothelial nitric oxide synthase activation mediated by caveolae internalization in endothelial cells. Circ. Res. 8, 870-877. doi: 10.1161/01.RES.0000245187.08026.47
54. 2 receptor gene and protein levels are differentially expressed in the hearts of rodents and humans. J. Pharmacol. Exp. Ther. 2, 786-795. doi: 10.1124/jpet.103.063065
55. 2_/calmodulin-dependent protein kinase: a key component in the contractile recovery from acidosis. Cardiovasc. Res. 73, 648-656. doi: 10.1016/j.cardiores.2006.12.002
56. Metz-Boutigue, M. H., Garcia-Sablone, P., Hogue-Angeletti, R., and Aunis, D. (1993). Intracellular and extracellular processing of Chromogranin A. Determination of cleavage sites. Eur. J. Biochem. 1, 247-257. doi: 10.1111/j.1432-1033.1993.tb18240.x
57. Miserez, B., Annaert, W., Dillen, L., Aunis, D., and De Potter, W. (1992). Chromogranin A processing in sympathetic neurons and release of Chromogranin A fragments from sheep spleen. FEBS Lett. 2, 122-124. doi: 10.1016/0014-5793(92)80956-H
58. Montero-Hadjadje, M., Vaingankar, S., Elias, S., Tostivint, H., Mahata, S. K., and Anouar, Y. (2008). Chromogranins A and B and secretogranin II: evolutionary and functional aspects. Acta Physiol. (Oxf). 2, 309-324. doi: 10.1111/j.1748-1716.2007.01806.x
59. Murphy, E., Kohr, M., Menazza, S., Nguyen, T., Evangelista, A., Sun, J., et al. (2014). Signaling by S-nitrosylation in the heart. Mol. Cell. Cardiol. 73, 18-25. doi: 10.1016/j.yjmcc.2014.01.003
60. O'Connor, D. T., Kailasam, M. T., Kennedy, B. P., Ziegler, M. G., Yanaihara, N., and Parmer, R. J. (2002). Early decline in the catecholamine release-inhibitory peptide catestatin in humans at genetic risk of hypertension. J. Hypertens. 7, 1335-1345. doi: 10.1097/00004872-200207000-00020
61. O'Connor, D. T., Pandlan, M. R., Carlton, E., Cervenka, J. H., and Hslao, R. J. (1989). Rapid radioimmunoassay of circulating Chromogranin A: in vitro stability, exploration of the neuroendocrine character of neoplasia, and assessment of the effects of organ failure. Clin. Chem. 35, 1631-1637.
62. O'Connor, D. T., Zhu, G., Rao, F., Taupenot, L., Fung, M. M., Das, M., et al. (2008). Heritability and genome-wide linkage in US and australian twins identify novel genomic regions controlling Chromogranin A: implications for secretion and blood pressure. Circulation 3, 247-257. doi: 10.1161/CIRCULATIONAHA.107.709105
63. Omland, T., Dickstein, K., and Syversen, U. (2003). Association between plasma Chromogranin A concentration and long-term mortality after myocardial infarction. Am. J. Med. 1, 25-30. doi: 10.1016/S0002-9343(02)01425-0
64. Ozawa, K., Whalen, E. J., Nelson, C. D., Mu, Y., Hess, D. T., Lefkowitz, R. J., et al. (2008). S-nitrosylation of beta-arrestin regulates beta-adrenergic receptor trafficking. Mol. Cell. 3, 395-405. doi: 10.1016/j.molcel.2008.05.024
65. Pagliaro, P., Chiribiri, A., Mancardi, D., Rastaldo, R., Gattullo, D., and Losano, G. (2003). Coronary endothelial dysfunction after ischemia and reperfusion and its prevention by ischemic preconditioning. Ital Heart J. 6, 383-394.
66. Pagliaro, P., Moro, F., Tullio, F., Perrelli, M. G., and Penna, C. (2011). Cardioprotective pathways during reperfusion: focus on redox signaling and other modalities of cell signaling. Antioxid Redox Signal 14, 833-850. doi: 10.1089/ars.2010.3245
67. Parmer, R. J., Mahata, M., Gong, Y., Mahata, S. K., Jiang, Q., O'Connor, D. T., et al. (2000). Processing of Chromogranin A by plasmin provides a novel mechanism for regulating catecholamine secretion. J. Clin. Invest. 7, 907-915. doi: 10.1172/JCI7394
68. Pasqua, T., Corti, A., Gentile, S., Pochini, L., Bianco, M., Metz-Boutigue, M. H., et al. (2013). Full-length human chromogranin-A cardioactivity: myocardial, coronary, and stimulus-induced processing evidence in normotensive and hypertensive male rat hearts. Endocrinology 9, 3353-3365. doi: 10.1210/en.2012-2210
69. Penna, C., Alloatti, G., Gallo, M. P., Cerra, M. C., Levi, R., Tullio, F., et al. (2010). Catestatin improves post-ischemic left ventricular function and decreases ischemia/reperfusion injury in heart. Cell Mol. Neurobiol. 8, 1171-1179. doi: 10.1007/s10571-010-9598-5
70. Penna, C., Angotti, C., and Pagliaro, P. (2014b). Protein S-nitrosylation in preconditioning and postconditioning. Exp. Biol. Med. 239, 647-662. doi: 10.1177/1535370214522935
71. Penna, C., Mancardi, D., Rastaldo, R., and Pagliaro, P. (2009). Cardioprotection: a radical view Free radicals in pre and postconditioning. Biochim. Biophys. Acta. 7, 781-793. doi: 10.1016/j.bbabio.2009.02.008
72. Penna, C., Pasqua, T., Amelio, D., Perrelli, M. G., Angotti, C., Tullio, F., et al. (2014a). Catestatin increases the expression of anti-apoptotic and pro-angiogenetic factors in the post-ischemic hypertrophied heart of SHR. PLoS ONE 9:e102536. doi: 10.1371/Journal.pone.0102536
73. Penna, C., Tullio, F., Perrelli, M. G., Mancardi, D., and Pagliaro, P. (2012). Cardioprotection against ischemia/reperfusion injury and Chromogranin A-derived peptides. Curr. Med. Chem. 24, 4074-4085. doi: 10.2174/092986712802429966
74. Perrelli, M. G., Tullio, F., Angotti, C., Cerra, M. C., Angelone, T., Tota, B., et al. (2013). P.Catestatin reduces myocardial ischaemia/reperfusion injury: involvement of PI3K/Akt, PKCs, mitochondrial KATP channels and ROS signalling. P. Pflugers Arch. 7, 1031-1040. doi: 10.1007/s00424-013-1217-0
75. Pieroni, M., Corti, A., Tota, B., Curnis, F., Angelone, T., Colombo, B., et al. (2007). Myocardial production of Chromogranin A in human heart: a new regulatory peptide of cardiac function. Eur. Heart J. 9, 1117-1127. doi: 10.1093/eurheartj/ehm022
76. Ramella, R., Boero, O., Alloatti, G., Angelone, T., Levi, R., and Gallo, M. P. (2010). Vasostatin 1 activates eNOS in endothelial cells through a proteoglycan-dependent mechanism. J. Cell Biochem. 110, 70-79. doi: 10.1002/jcb.22510
77. Reddy, A. G., Mishra, S. K., Prakash, V. R., Tandan, S. K., Tripathi, H. C., and Varshney, V. P. (1999). Evaluation of the activity of receptor-operated Ca2+ channels in rat portal vein in induced hyperthyroidism. Indian J. Physiol. Pharmacol. 3, 389-392.
78. Samuels, M. A. (2007). The brain-heart connection. Circulation 1, 77-84. doi: 10.1161/CIRCULATIONAHA.106.678995
79. Satoh, K., Matsu-Ura, T., Enomoto, M., Nakamura, H., Michikawa, T., and Mikoshiba, K. (2011). Highly cooperative dependence of sarco/endoplasmic reticulum calcium ATPase(SERCA) 2a pump activity on cytosolic calcium in living cells. J. Biol. Chem. 286, 20591-20599. doi: 10.1074/jbc.M110.204685
80. Schmidt, A. G., Edes, I., and Kranias, E. G. (2001). Phospholamban: a promising therapeutic target in heart failure? Cardiovasc Drugs Ther. 15, 387-396. doi: 10.1023/A:1013381204658
81. Shaul, P. W., Afshar, S., Gibson, L. L., Sherman, T. S., Kerecman, J. D., Grubb, P. H., et al. (2002). Developmental changes in nitric oxide synthase isoform expression and nitric oxide production in fetal baboon lung. Am. J. Physiol. Lung. Cell Mol. Physiol. 6, L1192-L1199.
82. Sivaraman, V., Mudalagiri, N. R., Di Salvo, C., Kolvekar, S., Hayward, M., Yap, J., et al. (2007). Postconditioning protects human atrial muscle through the activation of the RISK pathway. Basic Res. Cardiol. 5, 453-459. doi: 10.1007/s00395-007-0664-1
83. Steiner, H. J., Weiler, R., Ludescher, C., Schmid, K. W., and Winkler, H. (1990). Chromogranins A and B are co-localized with atrial natriuretic peptides in secretory granules of rat heart. J. Histochem. Cytochem. 6, 845-850. doi: 10.1177/38.6.2139887
84. Takiyyuddin, M. A., Parmer, R. J., Kailasam, M. T., Cervenka, J. H., Kennedy, B., Ziegler, M. G., et al. (1995). Chromogranin A in human hypertension. Influence of heredity. Hypertension 1, 213-220. doi: 10.1161/01.HYP.26.1.213
85. Taupenot, L., Harper, K. L., and O'Connor, D. T. (2002). The Chromogranin Secretogranin Family. N. Engl. J. Med. 348, 1134-1149. doi: 10.1056/NEJMra021405
86. Theurl, M., Schgoer, W., Albrecht, K., Jeschke, J., Egger, M., Beer, A. G., et al. (2010). The neuropeptide catestatin acts as a novel angiogenic cytokine via a basic fibroblast growth factor-dependent mechanism. Circ Res. 11, 1326-1335. doi: 10.1161/CIRCRESAHA.110.219493
87. Tota, B., Angelone, T., Mazza, R., and Cerra, M. C. (2008). The Chromogranin A-derived vasostatins: new players in the endocrine heart. Curr. Med. Chem. 14, 1444-1451. doi: 10.2174/092986708784567662
88. Tota, B., Cerra, M. C., and Gattuso, A. (2010). Catecholamines, cardiac natriuretic peptides and Chromogranin A: evolution and physiopathology of a "whip-brake" system of the endocrine heart. J. Exp. Biol. 18, 3081-3103. doi: 10.1242/jeb.027391
89. Tota, B., Gentile, S., Pasqua, T., Bassino, E., Koshimizu, H., Cawley, N. X., et al. (2012). The novel Chromogranin A-derived serpinin and pyroglutaminated serpinin peptides are positive cardiac β-adrenergic-like inotropes. FASEB J. 7, 2888-2898. doi: 10.1096/fj.11-201111
90. Tota, B., Quintieri, A. M., Di Felice, V., and Cerra, M. C. (2007). New biological aspects of Chromogranin A-derived peptides: focus on vasostatins. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 1, 11-18. doi: 10.1016/j.cbpa.2006.05.016
91. Tullio, F., Angotti, C., Perrelli, M. G., Penna, C., and Pagliaro, P. (2013). Redox balance and cardioprotection. Basic Res. Cardiol. 108:392. doi: 10.1007/s00395-013-0392-7
92. Veschini, L., Crippa, L., Dondossola, E., Doglioni, C., Corti, A., and Ferrero, E. (2011). The vasostatin-1 fragment of Chromogranin A preserves a quiescent phenotype in hypoxia-driven endothelial cells and regulates tumor neovascularization. FASEB J. 11, 3906-3914. doi: 10.1096/fj.11-182410
93. Videen, J. S., Mezger, M. S., Chang, Y. M., and O'Connor, D. T. (1992). Calcium and catecholamine interactions with adrenal chromogranins. Comparison of driving forces in binding and aggregation. J. Biol. Chem. 5, 3066-3073.
94. Weiergräber, M., Pereverzev, A., Vajna, R., Henry, M., Schramm, M., Nastainczyk, W., et al. (2000). Immunodetection of alpha1E voltage-gated Ca(2+) channel in chromogranin-positive muscle cells of rat heart, and in distal tubules of human kidney. J. Histochem. Cytochem. 6, 807-819. doi: 10.1177/002215540004800609
95. Winkler, H., and Fischer-Colbrie, R. (1992). The chromogranins A and B: the first 25 years and future perspectives. Neuroscience 3, 497-528. doi: 10.1016/0306-4522(92)90222-N
96. Xiao, R. P., Cheng, H., Zhou, Y. Y., Kuschel, M., and Lakatta, E. G. (1999). Recent advances in cardiac beta(2)-adrenergic signal transduction. Circ. Res. 11, 1092-1100. doi: 10.1161/01.RES.85.11.1092
97. Xie, J., Wang, W. Q., Liu, T. X., Deng, M., and Ning, G. (2008). Spatio-temporal expression of Chromogranin A during zebrafish embryogenesis. J. Endocrinol. 3, 451-458. doi: 10.1677/JOE-08-0221
98. Yano, N., Ianus, V., Zhao, T. C., Tseng, A., Padbury, J. F., and Tseng, Y. T. (2007). A novel signaling pathway for beta-adrenergic receptor-mediated activation of phosphoinositide 3-kinase in H9c2 cardiomyocytes. Am. J. Physiol. Heart Circ. Physiol. 1, H385-H393. doi: 10.1152/ajpheart.01318.2006
99. Yoo, S. H., So, S. H., Huh, Y. H., and Park, H. Y. (2002). Inositol 1, 4, 5-trisphosphate receptor/Ca(2+) channel modulatory role of chromogranins A and B. Ann. N.Y. Acad. Sci. 971, 300-310. doi: 10.1111/j.1749-6632.2002.tb04484.x
100. Zatta, A. J., Kin, H., Lee, G., Wang, N., Jiang, R., Lust, R., et al. (2006). Infarct-sparing effect of myocardial postconditioning is dependent on protein kinase C signalling. Cardiovasc Res. 2, 315-324. doi: 10.1016/j.cardiores.2005.11.030
101. Zhang, K., Chen, Y., Wen, G., Mahata, M., Rao, F., Fung, M. M., et al. (2011). Catecholamine storage vesicles: role of core protein genetic polymorphisms in hypertension. Curr. Hypertens Rep. 1, 36-45. doi: 10.1007/s11906-010-0170-y