Advertisement

Secretogranin II: Novel Insights into Expression and Function of the Precursor of the Neuropeptide Secretoneurin

  • Reiner Fischer-ColbrieEmail author
  • Markus Theurl
  • Rudolf Kirchmair
Chapter
Part of the UNIPA Springer Series book series (USS)

Abstract

SgII is an acidic secretory which belongs to the family of chromogranins. It is present in the large-dense cored vesicles of the regulated secretory pathway of many neurons and endocrine cells and it is well conserved during evolution. Like chromogranin A, SgII can induce granulogenesis in endocrine cells but also in cells typically lacking secretory vesicles like fibroblasts. In the secretory vesicles SgII is processed to smaller peptides, e.g. secretoeneurin, EM66 and manserin. For secretoneurin several biological effects like induction of neurotransmitter release, chemotactic activity towards immune-, endothelial- and muscle cells, and potent angiogenic and vasculogenic properties have been established. Thus, SN displays potent hormonal and paracrine effects, which help to orchestrate development, maintenance, physiologic activity and repair of the surrounding tissue. In addition, SgII has been established as valuable biomarker for endocrine tumours and cardiovascular diseases.

References

  1. Albrecht-Schgoer K, Schgoer W, Holfeld J, Theurl M, Wiedemann D, Steger C, Gupta R, Semsroth S, Fischer-Colbrie R, Beer AG, Stanzl U, Huber E, Misener S, Dejaco D, Kishore R, Pachinger O, Grimm M, Bonaros N, Kirchmair R (2012) The angiogenic factor secretoneurin induces coronary angiogenesis in a model of myocardial infarction by stimulation of vascular endothelial growth factor signaling in endothelial cells. Circulation 126:2491–2501CrossRefPubMedGoogle Scholar
  2. Albrecht-Schgoer K, Schgoer W, Theurl M, Stanzl U, Lener D, Dejaco D, Zelger B, Franz WM, Kirchmair R (2014) Topical secretoneurin gene therapy accelerates diabetic wound healing by interaction between heparan-sulfate proteoglycans and basic FGF. Angiogenesis 17:27–36CrossRefPubMedGoogle Scholar
  3. Anouar Y, Jégou S, Alexandre D, Lihrmann I, Conlon JM, Vaudry H (1996) Molecular cloning of frog secretogranin II reveals the occurrence of several highly conserved potential regulatory peptides. FEBS Lett 394:295–299CrossRefPubMedGoogle Scholar
  4. Bartolomucci A, Possenti R, Mahata SK, Fischer-Colbrie R, Loh YP, Salton SR (2011) The extended Granin family: structure, function, and biomedical implications. Endocr Rev 32:755–797CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bauer JW, Kirchmair R, Egger C, Fischer-Colbrie R (1993) Histamine induces a gene-specific synthesis regulation of secretogranin II but not of chromogranin a and B in chromaffin cells in a calcium-dependent manner. J Biol Chem 268:1586–1589PubMedGoogle Scholar
  6. Berard AR, Severini A, Coombs KM (2015) Differential reovirus-specific and herpesvirus-specific activator protein 1 activation of secretogranin II leads to altered virus secretion. J Virol 89:11954–11964CrossRefPubMedPubMedCentralGoogle Scholar
  7. Beuret N, Stettler H, Renold A, Rutishauser J, Spiess M (2004) Expression of regulated secretory proteins is sufficient to generate granule-like structures in constitutively secreting cells. J Biol Chem 279:20242–20249CrossRefPubMedGoogle Scholar
  8. Blázquez M, Bosma PT, Chang JP, Docherty K, Trudeau VL (1998) G-aminobutyric acid up-regulates the expression of a novel secretogranin-II messenger ribonucleic acid in the goldfish pituitary. Endocrinology 139:4870–4880CrossRefPubMedGoogle Scholar
  9. Cohn DV, Zangerle R, Fischer-Colbrie R, Chu LLH, Elting JJ, Hamilton JW, Winkler H (1982) Similarity of secretory protein I from parathyroid gland to chromogranin a from adrenal medulla. Proc Natl Acad Sci U S A 79:6056–6059CrossRefPubMedPubMedCentralGoogle Scholar
  10. Collins JJ, Wilson K, Fischer-Colbrie R, Papka RE (2000) Distribution and origin of secretoneurin-immunoreactive nerves in the female rat uterus. Neuroscience 95:255–264CrossRefPubMedGoogle Scholar
  11. Conlon JM (2010) Granin-derived peptides as diagnostic and prognostic markers for endocrine tumors. Regul Pept 165:5–11CrossRefPubMedGoogle Scholar
  12. Courel M, El Yamani FZ, Alexandre D, El Fatemi H, Delestre C, Montero-Hadjadje M, Tazi F, Amarti A, Magoul R, Chartrel N, Anouar Y (2014) Secretogranin II is overexpressed in advanced prostate cancer and promotes the neuroendocrine differentiation of prostate cancer cells. Eur J Cancer 50(17):3039–3049CrossRefPubMedGoogle Scholar
  13. Courel M, Soler-Jover A, Rodriguez-Flores JL, Mahata SK, Elias S, Montero-Hadjadje M, Anouar Y, Giuly RJ, O’Connor DT, Taupenot L (2010) Pro-hormone secretogranin II regulates dense core secretory granule biogenesis in catecholaminergic cells. J Biol Chem 285:10030–10043CrossRefPubMedPubMedCentralGoogle Scholar
  14. Courel M, Vasquez MS, Hook VY, Mahata SK, Taupenot L (2008) Sorting of the neuroendocrine secretory protein Secretogranin II into the regulated secretory pathway: role of N- and C-terminal alpha-helical domains. J Biol Chem 283:11807–11822CrossRefPubMedPubMedCentralGoogle Scholar
  15. Cubeddu LX, O’Connor DT, Parmer RJ (1995) Plasma chromogranin A: a marker of serotonin release and of emesis associated with cisplatin chemotherapy. J Clin Oncol 13:681–687CrossRefPubMedGoogle Scholar
  16. Dunzendorfer S, Kaser A, Meierhofer C, Tilg H, Wiedermann CJ (2001) Peripheral neuropeptides attract immature and arrest mature blood-derived dendritic cells. J Immunol 166:2167–2172CrossRefPubMedGoogle Scholar
  17. Dunzendorfer S, Schratzberger P, Reinisch N, Kähler CM, Wiedermann CJ (1998) Secretoneurin, a novel neuropeptide, is a potent chemoattractant for human eosinophils. Blood 91:1527–1532PubMedGoogle Scholar
  18. Eder U, Leitner B, Kirchmair R, Pohl P, Jobst KA, Smith AD, Mally J, Benzer A, Riederer P, Reichmann H, Saria A, Winkler H (1998) Levels and proteolytic processing of chromogranin a and B and secretogranin II in cerebrospinal fluid in neurological diseases. J Neural Transm 105:39–51CrossRefPubMedGoogle Scholar
  19. Eder U, Hukkanen M, Leitner B, Mur E, Went P, Kirchmair R, Fischer-Colbrie R, Polak JM, Winkler H (1997) The presence of secretoneurin in human synovium and synovial fluid. Neurosci Lett 224:139–131CrossRefPubMedGoogle Scholar
  20. Egger M, Schgoer W, Beer AG, Jeschke J, Leierer J, Theurl M, Frauscher S, Tepper OM, Niederwanger A, Ritsch A, Kearney M, Wanschitz J, Gurtner GC, Fischer-Colbrie R, Weiss G, Piza-Katzer H, Losordo DW, Patsch JR, Schratzberger P, Kirchmair R (2007) Hypoxia up-regulates the angiogenic cytokine secretoneurin via an HIF-1alpha- and basic FGF-dependent pathway in muscle cells. FASEB J 21:2906–2917CrossRefPubMedGoogle Scholar
  21. Erlich R, Gleeson PA, Campbell P, Dietzsch E, Toh BH (1996) Molecular characterization of trans-Golgi p230. A human peripheral membrane protein encoded by a gene on chromosome 6p12–22 contains extensive coiled-coil alpha-helical domains and a granin motif. J Biol Chem 271:8328–8337CrossRefPubMedGoogle Scholar
  22. Fischer-Colbrie R, Kirchmair R, Kähler CM, Wiedermann CJ, Saria A (2005) Secretoneurin: a new player in angiogenesis and chemotaxis linking nerves, blood vessels and the immune system. Curr Protein Pept Sci 6:373–385CrossRefPubMedGoogle Scholar
  23. Fischer-Colbrie R, Kirchmair R, Schobert A, Olenik C, Meyer DK, Winkler H (1993) Secretogranin II is synthesized and secreted in astrocyte cultures. J Neurochem 60:2312–2314CrossRefPubMedGoogle Scholar
  24. Fischer-Colbrie R, Gutierrez J, Hsu CM, Iacangelo A, Eiden LE (1990) Sequence analysis, tissue distribution and regulation by cell depolarization, and second messengers of bovine secretogranin II (chromogranin C) mRNA. J Biol Chem 265:9208–9213PubMedGoogle Scholar
  25. Fischer-Colbrie R, Laslop A, Kirchmair R (1995) Secretogranin II: molecular properties, regulation of biosynthesis and processing to the neuropeptide secretoneurin. Prog Neurobiol 46:49–70CrossRefPubMedGoogle Scholar
  26. Fournier I, Gaucher D, Chich JF, Bach C, Shooshtarizadeh P, Picaud S, Bourcier T, Speeg-Schatz C, Strub JM, Van Dorsselaer A, Corti A, Aunis D, Metz-Boutigue MH (2011) Processing of chromogranins/secretogranin in patients with diabetic retinopathy. Regul Pept 167:118–124CrossRefPubMedGoogle Scholar
  27. Fujita Y, Katagi J, Tabuchi A, Tsuchiya T, Tsuda M (1999) Coactivation of secretogranin-II and BDNF genes mediated by calcium signals in mouse cerebellar granule cells. Mol Brain Res 63:316–324CrossRefPubMedGoogle Scholar
  28. Gasser MC, Berti I, Hauser KF, Fischer-Colbrie R, Saria A (2003) Secretoneurin promotes pertussis toxin-sensitive neurite outgrowth in cerebellar granule cells. J Neurochem 85:662–669CrossRefPubMedGoogle Scholar
  29. Guillemot J, Anouar Y, Montero-Hadjadje M, Grouzmann E, Grumolato L, Roshmaninho-Salgado J, Turquier V, Duparc C, Lefebvre H, Plouin PF, Klein M, Muresan M, Chow BK, Vaudry H, Yon L (2006) Circulating EM66 is a highly sensitive marker for the diagnosis and follow-up of pheochromocytoma. Int J Cancer 118:2003–2012CrossRefPubMedGoogle Scholar
  30. Gupta N, Bark SJ, Lu WD, Taupenot L, O’Connor DT, Pevzner P, Hook V (2010) Mass spectrometry-based neuropeptidomics of secretory vesicles from human adrenal medullary pheochromocytoma reveals novel peptide products of prohormone processing. J Proteome Res 9:5065–5075CrossRefPubMedPubMedCentralGoogle Scholar
  31. Hasslacher J, Lehner GF, Harler U, Beer R, Ulmer H, Kirchmair R, Fischer-Colbrie R, Bellmann R, Dunzendorfer S, Joannidis M (2014) Secretoneurin as a marker for hypoxic brain injury after cardiopulmonary resuscitation. Intensive Care Med 40:1518–1527CrossRefPubMedGoogle Scholar
  32. Helle KB (2010) Chromogranins a and B and secretogranin II as prohormones for regulatory peptides from the diffuse neuroendocrine system. Results Probl Cell Differ 50:21–44PubMedGoogle Scholar
  33. Hohl M, Thiel G (2005) Cell type-specific regulation of RE-1 silencing transcription factor (REST) target genes. Eur J Neurosci 22:2216–2230CrossRefPubMedGoogle Scholar
  34. Hotta K, Hosaka M, Tanabe A, Takeuchi T (2009) Secretogranin II binds to secretogranin III and forms secretory granules with orexin, neuropeptide Y, and POMC. J Endocrinol 202:111–121CrossRefPubMedGoogle Scholar
  35. Huttner WB, Gerdes HH, Rosa P (1991) The granin (chromogranin/secretogranin) family. TIBS 16:27–30PubMedGoogle Scholar
  36. Ischia R, Gasser RW, Fischer-Colbrie R, Eder U, Pagani A, Cubeddu LX, Lovisetti-Scamihorn P, Finkenstedt G, Laslop A, Winkler H (2000a) Levels and molecular properties of secretoneurin-immunoreactivity in the serum and urine of control and neuroendocrine tumor patients. J Clin Endocrinol Metab 85:355–360PubMedGoogle Scholar
  37. Ischia R, Hobisch A, Bauer R, Weiss U, Gasser RW, Horninger W, Bartsch G Jr, Fuchs D, Bartsch G, Winkler H, Klocker H, Fischer-Colbrie R, Culig Z (2000b) Elevated levels of serum secretoneurin in patients with therapy resistant carcinoma of the prostate. J Urol 163:1161–1164CrossRefPubMedGoogle Scholar
  38. Kähler CM, Kirchmair R, Kaufmann G, Kähler STEA, Reinisch N, Fischer-Colbrie R, Hogue-Angeletti R, Winkler H, Wiedermann CJ (1997a) Inhibition of proliferation and stimulation of migration of endothelial cells by secretoneurin in vitro. Arterioscler Thromb Vasc Biol 17:932–939CrossRefPubMedGoogle Scholar
  39. Kähler CM, Schratzberger P, Wiedermann CJ (1997b) Response of vascular smooth muscle cells to the neuropeptide secretoneurin. A functional role for migration and proliferation in vitro. Arterioscler Thromb Vasc Biol 17:2029–2035CrossRefPubMedGoogle Scholar
  40. Kähler CM, Fischer-Colbrie R (2000) Secretoneurin - a novel link between the nervous and the immune system. Conservation of the sequence and functional aspects. Adv Exp Med Biol 482:279–290CrossRefPubMedGoogle Scholar
  41. Kim HJ, Denli AM, Wright R, Baul TD, Clemenson GD, Morcos AS, Zhao C, Schafer ST, Gage FH, Kagalwala MN (2015) REST regulates non-cell-autonomous neuronal differentiation and maturation of neural progenitor cells via secretogranin II. J Neurosci 35:14872–14884CrossRefPubMedPubMedCentralGoogle Scholar
  42. Kim T, Zhang CF, Sun Z, Wu H, Loh YP (2005) Chromogranin a deficiency in transgenic mice leads to aberrant chromaffin granule biogenesis. J Neurosci 25:6958–6961CrossRefPubMedGoogle Scholar
  43. Kim YD, Sohn NW, Kang C, Soh Y (2002) DNA array reveals altered gene expression in response to focal cerebral ischemia. Brain Res Bull 58:491–498CrossRefPubMedGoogle Scholar
  44. Kirchmair R, Egger M, Walter DH, Eisterer W, Niederwanger A, Woell E, Nagl M, Pedrini M, Murayama T, Frauscher S, Hanley A, Silver M, Brodmann M, Sturm W, Fischer-Colbrie R, Losordo DW, Patsch JR, Schratzberger P (2004a) Secretoneurin, an angiogenic neuropeptide, induces postnatal vasculogenesis. Circulation 110:1121–1127CrossRefPubMedGoogle Scholar
  45. Kirchmair R, Gander R, Egger M, Hanley A, Silver M, Ritsch A, Murayama T, Kaneider N, Sturm W, Kearny M, Fischer-Colbrie R, Kircher B, Gaenzer H, Wiedermann CJ, Ropper AH, Losordo DW, Patsch JR, Schratzberger P (2004b) The neuropeptide secretoneurin acts as a direct angiogenic cytokine in vitro and in vivo. Circulation 109:777–783CrossRefPubMedGoogle Scholar
  46. Kirchmair R, Hogue-Angeletti R, Gutierrez J, Fischer-Colbrie R, Winkler H (1993) Secretoneurin--a neuropeptide generated in brain, adrenal medulla and other endocrine tissues by proteolytic processing of secretogranin II (chromogranin C). Neuroscience 53:359–365CrossRefPubMedGoogle Scholar
  47. Kuliawat R, Arvan P (1994) Distinct molecular mechanisms for protein sorting within immature secretory granules of pancreatic beta-cells. J Cell Biol 126:77–86CrossRefPubMedGoogle Scholar
  48. Lechner T, Adlassnig C, Humpel C, Kaufmann WA, Maier H, Reinstadler-Kramer K, Hinterholzl J, Mahata SK, Jellinger KA, Marksteiner J (2004) Chromogranin peptides in Alzheimer’s disease. Exp Gerontol 39:101–113CrossRefPubMedGoogle Scholar
  49. Lee JE, Atkins N, Hatcher NG, Zamdborg L, Gillette MU, Sweedler JV, Kelleher NL (2010) Endogenous peptide discovery of the rat circadian clock: a focused study of the suprachiasmatic nucleus by ultrahigh performance tandem mass spectrometry. Mol Cell Proteomics 9:285–297CrossRefPubMedGoogle Scholar
  50. Li L, Hung AC, Porter AG (2008) Secretogranin II: a key AP-1-regulated protein that mediates neuronal differentiation and protection from nitric oxide-induced apoptosis of neuroblastoma cells. Cell Death Differ 15:879–888CrossRefPubMedGoogle Scholar
  51. Liang H, Studach L, Hullinger RL, Xie J, Andrisani OM (2014) Down-regulation of RE-1 silencing transcription factor (REST) in advanced prostate cancer by hypoxia-induced miR-106b~25. Exp Cell Res 320:188–199CrossRefPubMedGoogle Scholar
  52. Lin TP, Chang YT, Lee SY, Campbell M, Wang TC, Shen SH, Chung HJ, Chang YH, Chiu AW, Pan CC, Lin CH, Chu CY, Kung HJ, Cheng CY, Chang PC (2016) REST reduction is essential for hypoxia-induced neuroendocrine differentiation of prostate cancer cells by activating autophagy signaling. Oncotarget 7:26137–26151CrossRefPubMedPubMedCentralGoogle Scholar
  53. Mahata SK, Kozak CA, Szpirer J, Szpirer C, Modi WS, Gerdes HH, Huttner WB, O’Connor DT (1996) Dispersion of chromogranin/secretogranin secretory protein family loci in mammalian genomes. Genomics 33:135–139CrossRefPubMedGoogle Scholar
  54. Mahata SK, Mahata M, Livsey CV, Gerdes HH, Huttner WB, O’Connor DT (1999) Neuroendocrine cell type-specific and inducible expression of the secretogranin II gene: crucial role of cyclic adenosine monophosphate and serum response elements. Endocrinology 140:739–749CrossRefPubMedGoogle Scholar
  55. Marti E, Ferrer I, Blasi J (2001) Differential regulation of chromogranin a, chromogranin B and secretoneurin protein expression after transient forebrain ischemia in the gerbil. Acta Neuropathol 101:159–166PubMedGoogle Scholar
  56. Mattsson N, Ruetschi U, Podust VN, Stridsberg M, Li S, Andersen O, Haghighi S, Blennow K, Zetterberg H (2007) Cerebrospinal fluid concentrations of peptides derived from chromogranin B and secretogranin II are decreased in multiple sclerosis. J Neurochem 103:1932–1939CrossRefPubMedGoogle Scholar
  57. Mikwar M, Navarro-Martin L, Xing L, Volkoff H, Hu W, Trudeau VL (2016) Stimulatory effect of the secretogranin-ll derived peptide secretoneurin on food intake and locomotion in female goldfish (Carassius Auratus). Peptides 78:42–50CrossRefPubMedGoogle Scholar
  58. Miller C, Kirchmair R, Troger J, Saria A, Fleischhacker WW, Fischer-Colbrie R, Benzer A, Winkler H (1996) CSF of neuroleptic-naive first-episode schizophrenic patients: levels of biogenic amines, substance P, and peptides derived from chromogranin a (GE-25) and secretogranin II (secretoneurin). Biol Psychol 39:911–918CrossRefGoogle Scholar
  59. O’Connor DT, Burton D, Deftos LJ (1983) Chromogranin a: immunohistology reveals its universal occurrence in normal polypeptide hormone producing endocrine glands. Life Sci 33:1657–1663CrossRefPubMedGoogle Scholar
  60. Ottesen AH, Louch WE, Carlson CR, Landsverk OJ, Kurola J, Johansen RF, Moe MK, Aronsen JM, Hoiseth AD, Jarstadmarken H, Nygard S, Bjoras M, Sjaastad I, Pettila V, Stridsberg M, Omland T, Christensen G, Rosjo H (2015) Secretoneurin is a novel prognostic cardiovascular biomarker associated with cardiomyocyte calcium handling. J Am Coll Cardiol 65:339–351CrossRefPubMedGoogle Scholar
  61. Oulyadi H, Davoust D, Vaudry H (1997) A determination of the solution conformation of secretoneurin, a neuropeptide originating from the processing of secretogranin II, by 1H-NMR and restrained molecular dynamics. Eur J Biochem 246:665–673CrossRefPubMedGoogle Scholar
  62. Overdick B, Kirchmair R, Marksteiner J, Fischer-Colbrie R, Troger J, Winkler H, Saria A (1996) Presence and distribution of a new neuropeptide, secretoneurin, in human retina. Peptides 17:1–4CrossRefPubMedGoogle Scholar
  63. Portela-Gomes GM, Grimelius L, Wilander E, Stridsberg M (2010) Granins and granin-related peptides in neuroendocrine tumours. Regul Pept 165:12–20CrossRefPubMedGoogle Scholar
  64. Prommegger R, Obrist P, Ensinger C, Schwelberger HG, Wolf C, Fischer-Colbrie R, Mikuz G, Bodner E (1998) Secretoneurin in carcinoids of the appendix – immunohistochemical comparison with chromogranins a, B and secretogranin II. Anticancer Res 18:3999–4002PubMedGoogle Scholar
  65. Pruneri G, Galli S, Rossi RS, Roncalli M, Coggi G, Ferrari A, Simonato A, Siccardi AG, Carboni N, Buffa R (1998) Chromogranin a and B and secretogranin II in prostatic adenocarcinomas: neuroendocrine expression in patients untreated and treated with androgen deprivation therapy. Prostate 34:113–120CrossRefPubMedGoogle Scholar
  66. Reinisch N, Kirchmair R, Kähler CM, Hogue-Angeletti R, Fischer-Colbrie R, Winkler H, Wiedermann CJ (1993) Attraction of human monocytes by the neuropeptide secretoneurin. FEBS Lett 334:41–44CrossRefPubMedGoogle Scholar
  67. Røsjø H, Stridsberg M, Florholmen G, Stenslokken KO, Ottesen AH, Sjaastad I, Husberg C, Dahl MB, Oie E, Louch WE, Omland T, Christensen G (2012) Secretogranin II; a protein increased in the myocardium and circulation in heart failure with cardioprotective properties. PLoS One 7:e37401CrossRefPubMedPubMedCentralGoogle Scholar
  68. Scammell JG, Reddy S, Valentine DL, Coker TN, Nikolopoulos SN, Ross RA (2000) Isolation and characterization of the human secretogranin II gene promoter. Mol Brain Res 75:8–15CrossRefPubMedGoogle Scholar
  69. Schgoer W, Theurl M, Albrecht-Schgoer K, Jonach V, Koller B, Lener D, Franz WM, Kirchmair R (2013) Secretoneurin gene therapy improves blood flow in an ischemia model in type 1 diabetic mice by enhancing therapeutic neovascularization. PLoS One 8:e74029CrossRefPubMedPubMedCentralGoogle Scholar
  70. Schgoer W, Theurl M, Jeschke J, Beer AG, Albrecht K, Gander R, Rong S, Vasiljevic D, Egger M, Wolf AM, Frauscher S, Koller B, Tancevski I, Patsch JR, Schratzberger P, Piza-Katzer H, Ritsch A, Bahlmann FH, Fischer-Colbrie R, Wolf D, Kirchmair R (2009) Gene therapy with the angiogenic cytokine secretoneurin induces therapeutic angiogenesis by a nitric oxide-dependent mechanism. Circ Res 105:994–1002CrossRefPubMedGoogle Scholar
  71. Schimmel A, Bräunling O, Rüther U, Huttner WB, Gerdes H-H (1992) The organisation of the mouse secretogranin II gene. FEBS Lett 3:375–380CrossRefGoogle Scholar
  72. Schrott-Fischer A, Bitsche M, Humpel C, Walcher C, Maier H, Jellinger K, Rabl W, Glueckert R, Marksteiner J (2009) Chromogranin peptides in amyotrophic lateral sclerosis. Regul Pept 152:13–21CrossRefPubMedGoogle Scholar
  73. Shyu WC, Lin SZ, Chiang MF, Chen DC, Su CY, Wang HJ, Liu RS, Tsai CH, Li H (2008) Secretoneurin promotes neuroprotection and neuronal plasticity via the Jak2/Stat3 pathway in murine models of stroke. J Clin Invest 118:133–148CrossRefPubMedGoogle Scholar
  74. Song SB, Rhee M, Roberson MS, Maurer RA, Kim KE (2003) Gonadotropin-releasing hormone-induced stimulation of the rat secretogranin II promoter involves activation of CREB. Mol Cell Endocrinol 199:29–36CrossRefPubMedGoogle Scholar
  75. Stemberger K, Pallhuber J, Doblinger A, Troger J, Kirchmair R, Kralinger M, Fischer-Colbrie R, Kieselbach G (2004) Secretoneurin in the human aqueous humor and the absence of an effect of frequently used eye drops on the levels. Peptides 25:2115–2118CrossRefPubMedGoogle Scholar
  76. Stridsberg M, Eriksson B, Janson ET (2008) Measurements of secretogranins II, III, V and proconvertases 1/3 and 2 in plasma from patients with neuroendocrine tumours. Regul Pept 148:95–98CrossRefPubMedGoogle Scholar
  77. Sun M, Watanabe T, Bochimoto H, Sakai Y, Torii S, Takeuchi T, Hosaka M (2013) Multiple sorting systems for secretory granules ensure the regulated secretion of peptide hormones. Traffic 14:205–218CrossRefPubMedGoogle Scholar
  78. Taupenot L, Harper KL, O’Connor DT (2003) The chromogranin-secretogranin family. N Engl J Med 348:1134–1149CrossRefPubMedGoogle Scholar
  79. Theurl M, Schgoer W, Albrecht-Schgoer K, Lener D, Wolf D, Wolf M, Demetz E, Tymoszuk P, Tancevski I, Fischer-Colbrie R, Franz WM, Marschang P, Kirchmair R (2015) Secretoneurin gene therapy improves hind limb and cardiac ischaemia in Apo E/ mice without influencing systemic atherosclerosis. Cardiovasc Res 105:96–106CrossRefPubMedGoogle Scholar
  80. Tilemans D, Jacobs GFM, Andries M, Proost P, Devreese B, Van Damme J, Van Beeumen J, Denef C (1994) Isolation of two peptides from rat gonadotroph-conditioned medium displaying an amino acid sequence identical to fragments of secretogranin II. Peptides 15:537–545CrossRefPubMedGoogle Scholar
  81. Tooze SA (1998) Biogenesis of secretory granules in the trans-Golgi network of neuroendocrine and endocrine cells. Biochim Biophys Acta 1404:231–244CrossRefPubMedGoogle Scholar
  82. Troger J, Doblinger A, Leierer J, Laslop A, Schmid E, Teuchner B, Opatril M, Philipp W, Klimaschewski L, Pfaller K, Gottinger W, Fischer-Colbrie R (2005) Secretoneurin in the peripheral ocular innervation. Invest Ophthalmol Vis Sci 46:647–654CrossRefPubMedGoogle Scholar
  83. Troger J, Kirchmair R, Marksteiner J, Seidl CV, Fischer-Colbrie R, Saria A, Winkler H (1994) Release of secretoneurin and noradrenaline from hypothalamic slices and its differential inhibition by calcium channel blockers. Naunyn-Schmied Arch Pharmacol 349:565–569CrossRefGoogle Scholar
  84. Trudeau VL, Martyniuk CJ, Zhao E, Hu H, Volkoff H, Decatur WA, Basak A (2012) Is secretoneurin a new hormone? Gen Comp Endocrinol 175:10–18CrossRefPubMedGoogle Scholar
  85. Vaudry H, Conlon JM (1991) Identification of a peptide arising from the specific post-translation processing of secretogranin II. FEBS Lett 284:31–33CrossRefPubMedGoogle Scholar
  86. Wagner M, Stridsberg M, Peterson CG, Sangfelt P, Lampinen M, Carlson M (2013) Increased fecal levels of chromogranin a, chromogranin B, and secretoneurin in collagenous colitis. Inflammation 36:855–861CrossRefPubMedGoogle Scholar
  87. Watanabe Y, Kameoka S, Gopalakrishnan V, Aldape KD, Pan ZZ, Lang FF, Majumder S (2004) Conversion of myoblasts to physiologically active neuronal phenotype. Genes Dev 18:889–900CrossRefPubMedPubMedCentralGoogle Scholar
  88. Wechselberger K, Schmid A, Posod A, Hock M, Neubauer V, Fischer-Colbrie R, Kiechl-Kohlendorfer U, Griesmaier E (2016) Secretoneurin serum levels in healthy term neonates and neonates with hypoxic-ischaemic encephalopathy. Neonatology 110:14–20CrossRefPubMedGoogle Scholar
  89. Wiedenmann B, Waldherr R, Buhr H, Hille A, Rosa P, Huttner WB (1988) Identification of gastroenteropancreatic neuroendocrine cells in normal and neoplastic human tissue with antibodies against synaptophysin, chromogranin a, secretogranin I (chromogranin B), and secetogranin II. Gastroenterology 95:1364–1374CrossRefPubMedGoogle Scholar
  90. Wolkersdorfer M, Laslop A, Lazure C, Fischer-Colbrie R, Winkler H (1996) Processing of chromogranins in chromaffin cell culture: effects of reserpine and a-methyl p-tyrosine. Biochem J 316:953–958CrossRefPubMedPubMedCentralGoogle Scholar
  91. Xu R, Li Q, Zhou J, Zhou X, Perelman JM, Kolosov VP (2014) Secretoneurin induces airway mucus hypersecretion by enhancing the binding of EGF to NRP1. Cell Physiol Biochem 33:446–456CrossRefPubMedGoogle Scholar
  92. Yajima A, Narita N, Narita M (2008) Recently identified a novel neuropeptide manserin colocalize with the TUNEL-positive cells in the top villi of the rat duodenum. J Pept Sci 14:773–776CrossRefPubMedGoogle Scholar
  93. Yajima A, Ikeda M, Miyazaki K, Maeshima T, Narita N, Narita M (2004) Manserin, a novel peptide from secretogranin II in the neuroendocrine system. Neuroreport 15:1755–1759CrossRefPubMedGoogle Scholar
  94. Yoo SH, Chu SY, Kim KD, Huh YH (2007) Presence of secretogranin II and high-capacity, low-affinity Ca2+ storage role in nucleoplasmic Ca2+ store vesicles. Biochemistry 46:14663–14671CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Reiner Fischer-Colbrie
    • 1
    Email author
  • Markus Theurl
    • 2
  • Rudolf Kirchmair
    • 2
  1. 1.Department of PharmacologyMedical University InnsbruckInnsbruckAustria
  2. 2.Cardiology & Angiology, Internal Medicine IIIMedical University InnsbruckInnsbruckAustria

Personalised recommendations