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Neurogenic angiogenesis and inflammation

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Angiogenesis in Inflammation: Mechanisms and Clinical Correlates

Part of the book series: Progress in Inflammation Research ((PIR))

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Abstract

Blood vessels can be formed through two different mechanisms: vasculogenesis or angiogenesis [1]. The first mechanism is dependent on the development of blood vessels from immature mesenchymal cells, and has been traditionally thought to be restricted to the early stages of embryo development. Angiogenesis is the sprouting of new blood vessels from pre-existing ones. This may occur physiologically during the female reproductive cycle or pathologically during tumour growth, diabetic retinopathy and chronic inflammation. It may be beneficial, for example during wound repair, or detrimental, for example in tumours or retinopathies. One of the regulators that may control angiogenesis is the nervous system. Neuropeptides are known to have angiogenic effects in vitro and in vivo. Neuropeptides are released in acute inflammatory responses but their role during chronic inflammation is much less certain. There appears to be a depletion of nerves in tissues as they become chronically inflamed. This may be related to the inability of nerves to grow at the same rate as proliferating tissue or due to a direct toxic effect of one or more components of the inflammatory milieu. Under such conditions we postulate that other peptides may take over the angiogenic roles of neuronally derived peptides, sometimes utilising the same receptors on endothelial cells. As well as promoters of angiogenesis, there is also a group of neuropeptides that are becoming increasingly recognised as being anti-angiogenic. Peptides released from the peripheral terminals of nerves may therefore either facilitate or suppress tissue growth.

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References

  1. Martinez A (2006) A new family of angiogenic factors. Cancer Lett 236: 157–163

    Article  PubMed  CAS  Google Scholar 

  2. Holzer P (1998) Neurogenic vasodilatation and plasma leakage in the skin. Gen Pharmacol 30: 5–11

    PubMed  CAS  Google Scholar 

  3. Foreman JC (1987) Peptides and neurogenic inflammation. Br Med Bull 43: 386–400

    PubMed  CAS  Google Scholar 

  4. Page NM (2004) Hemokinins and endokinins. Cell Mol Life Sci 61: 1652–1663

    Article  PubMed  CAS  Google Scholar 

  5. O—Connor TM, O—Connell J, O—Brien DI, Goode T, Bredin CP, Shanahan F (2004) The role of substance P in inflammatory disease. J Cell Physiol 201: 167–180

    Article  Google Scholar 

  6. Ziche M, Morbidelli L, Masini E, Amerini S, Granger HJ, Maggi CA, Geppetti P, Ledda F (1994) Nitric oxide mediates angiogenesis in vivo and endothelial cell growth and migration in vitro promoted by substance P. J Clin Invest 94: 2036–2044

    Article  PubMed  CAS  Google Scholar 

  7. Seegers HC, Avery PS, McWilliams DF, Haywood L, Walsh DA (2004) Combined effect of bradykinin B2 and neurokinin-1 receptor activation on endothelial cell proliferation in acute synovitis. FASEB J 18: 762–764

    PubMed  CAS  Google Scholar 

  8. Ziche M, Morbidelli L, Pacini M, Dolara P, Maggi CA (1990) NK1-receptors mediate the proliferative response of human fibroblasts to tachykinins. Br J Pharmacol 100: 11–14

    PubMed  CAS  Google Scholar 

  9. Volpert OV, Ward WF, Lingen MW, Chesler L, Solt DB, Johnson MD, Molteni A, Polverini PJ, Bouck NP (1996) Captopril inhibits angiogenesis and slows the growth of experimental tumors in rats. J Clin Invest 98: 671–679

    Article  PubMed  CAS  Google Scholar 

  10. Edvinsson L, Ekman R, Jansen I, Ottosson A, Uddman R (1987) Peptide-containing nerve fibers in human cerebral arteries: Immunocytochemistry, radioimmunoassay, and in vitro pharmacology. Ann Neurol 21: 431–437

    Article  PubMed  CAS  Google Scholar 

  11. Wiedermann CJ, Auer B, Sitte B, Reinisch N, Schratzberger P, Kahler CM (1996) Induction of endothelial cell differentiation into capillary-like structures by substance P. Eur J Pharmacol 298: 335–338

    Article  PubMed  CAS  Google Scholar 

  12. Ziche M, Parenti A, Ledda F, DelľEra P, Granger HJ, Maggi CA, Presta M (1997) Nitric oxide promotes proliferation and plasminogen activator production by coronary venular endothelium through endogenous bFGF. Circ Res 80: 845–852

    PubMed  CAS  Google Scholar 

  13. Lotz M, Vaughan JH, Carson DA (1988) Effect of neuropeptides on production of inflammatory cytokines by human monocytes. Science 241: 1218–1221

    Article  PubMed  CAS  Google Scholar 

  14. Ho WZ, Kaufman D, Uvaydova M, Douglas SD (1996) Substance P augments interleukin-10 and tumor necrosis factor-alpha release by human cord blood monocytes and macrophages. J Neuroimmunol 71: 73–80

    Article  PubMed  CAS  Google Scholar 

  15. Serra MC, Calzetti F, Ceska M, Cassatella MA (1994) Effect of substance P on superoxide anion and IL-8 production by human PMNL. Immunology 82: 63–69

    PubMed  CAS  Google Scholar 

  16. Luber-Narod J, Kage R, Leeman SE (1994) Substance P enhances the secretion of tumor necrosis factor-alpha from neuroglial cells stimulated with lipopolysaccharide. J Immunol 152: 819–824

    PubMed  CAS  Google Scholar 

  17. Martin FC, Charles AC, Sanderson MJ, Merrill JE (1992) Substance P stimulates IL-1 production by astrocytes via intracellular calcium. Brain Res 599: 13–18

    Article  PubMed  CAS  Google Scholar 

  18. Lowman MA, Benyon RC, Church MK (1988) Characterization of neuropeptide-induced histamine release from human dispersed skin mast cells. Br J Pharmacol 95: 121–130

    PubMed  CAS  Google Scholar 

  19. Fan TP, Hu DE, Guard S, Gresham GA, Watling KJ (1993) Stimulation of angiogenesis by substance P and interleukin-1 in the rat and its inhibition by NK1 or interleukin-1 receptor antagonists. Br J Pharmacol 110: 43–49

    PubMed  CAS  Google Scholar 

  20. Hu DE, Hori Y, Presta M, Gresham GA, Fan TP (1994) Inhibition of angiogenesis in rats by IL-1 receptor antagonist and selected cytokine antibodies. Inflammation 18: 45–58

    Article  PubMed  CAS  Google Scholar 

  21. Hu DE, Hiley CR, Smither RL, Gresham GA, Fan TP (1995) Correlation of 133Xe clearance, blood flow and histology in the rat sponge model for angiogenesis. Further studies with angiogenic modifiers. Lab Invest 72: 601–610

    PubMed  CAS  Google Scholar 

  22. Juaneda C, Dumont Y, Quirion R (2000) The molecular pharmacology of CGRP and related peptide receptor subtypes. Trends Pharmacol Sci 21: 432–438

    Article  PubMed  CAS  Google Scholar 

  23. Taylor CK, Smith DD, Hulce M, Abel PW (2006) Pharmacological characterization of novel alpha-calcitonin gene-related peptide (CGRP) receptor peptide antagonists that are selective for human CGRP receptors. J Pharmacol Exp Ther 319: 749–757

    Article  PubMed  CAS  Google Scholar 

  24. McLatchie LM, Fraser NJ, Main MJ, Wise A, Brown J, Thompson N, Solari R, Lee MG, Foord SM (1998) RAMPs regulate the transport and ligand specificity of the calcitoninreceptor-like receptor. Nature 393: 333–339

    Article  PubMed  CAS  Google Scholar 

  25. Husmann K, Born W, Fischer JA, Muff R (2003) Three receptor-activity-modifying proteins define calcitonin gene-related peptide or adrenomedullin selectivity of the mouse calcitonin-like receptor in COS-7 cells. Biochem Pharmacol 66: 2107–2115

    Article  PubMed  CAS  Google Scholar 

  26. Evans BN, Rosenblatt MI, Mnayer LO, Oliver KR, Dickerson IM (2000) CGRP-RCP, a novel protein required for signal transduction at calcitonin gene-related peptide and adrenomedullin receptors. J Biol Chem 275: 31438–31443

    Article  PubMed  CAS  Google Scholar 

  27. Haegerstrand A, Dalsgaard CJ, Jonzon B, Larsson O, Nilsson J (1990) Calcitonin generelated peptide stimulates proliferation of human endothelial cells. Proc Natl Acad Sci USA 87: 3299–3303

    Article  PubMed  CAS  Google Scholar 

  28. Dong YL, Reddy DM, Green KE, Chauhan MS, Wang HQ, Nagamani M, Hankins GD, Yallampalli C (2007) Calcitonin gene-related peptide (CALCA) is a proangiogenic growth factor in the human placental development. Biol Reprod 76: 892–899

    Article  PubMed  CAS  Google Scholar 

  29. Yu XJ, Li CY, Wang KY, Dai HY (2006) Calcitonin gene-related peptide regulates the expression of vascular endothelial growth factor in human HaCaT keratinocytes by activation of ERK1/2 MAPK. Regul Pept 137: 134–139

    Article  PubMed  CAS  Google Scholar 

  30. Jiang WY, Raychaudhuri SP, Farber EM (1998) Double-labeled immunofluorescence study of cutaneous nerves in psoriasis. Int J Dermatol 37: 572–574

    Article  PubMed  CAS  Google Scholar 

  31. Torii H, Hosoi J, Beissert S, Xu S, Fox FE, Asahina A, Takashima A, Rook AH, Granstein RD (1997) Regulation of cytokine expression in macrophages and the Langerhans cell-like line XS52 by calcitonin gene-related peptide. J Leukoc Biol 61: 216–223

    PubMed  CAS  Google Scholar 

  32. Tang Y, Han C, Wang X (1999) Role of nitric oxide and prostaglandins in the potentiating effects of calcitonin gene-related peptide on lipopolysaccharide-induced interleukin-6 release from mouse peritoneal macrophages. Immunology 96: 171–175

    Article  PubMed  CAS  Google Scholar 

  33. Brain SD, Grant AD (2004) Vascular actions of calcitonin gene-related peptide and adrenomedullin. Physiol Rev 84: 903–934

    Article  PubMed  CAS  Google Scholar 

  34. Karimian M, Ferrell WR (1994) Plasma protein extravasation into the rat knee joint induced by calcitonin gene-related peptide. Neurosci Lett 166: 39–42

    Article  PubMed  CAS  Google Scholar 

  35. Kjartansson J, Dalsgaard CJ (1987) Calcitonin gene-related peptide increases survival of a musculocutaneous critical flap in the rat. Eur J Pharmacol 142: 355–358

    Article  PubMed  CAS  Google Scholar 

  36. Jansen GB, Torkvist L, Lofgren O, Raud J, Lundeberg T (1999) Effects of calcitonin gene-related peptide on tissue survival, blood flow and neutrophil recruitment in experimental skin flaps. Br J Plast Surg 52: 299–303

    Article  PubMed  CAS  Google Scholar 

  37. Mapp PI, Turley MJ, McWilliams DF, Walsh DA (2007) Calcitonin gene-related peptide causes endothelial cell proliferation in vivo. Rheumatology 46: i43

    Article  Google Scholar 

  38. Movafagh S, Hobson JP, Spiegel S, Kleinman HK, Zukowska Z (2006) Neuropeptide Y induces migration, proliferation, and tube formation of endothelial cells bimodally via Y1, Y2, and Y5 receptors. FASEB J 20: 1924–1926

    Article  PubMed  CAS  Google Scholar 

  39. Ekstrand AJ, Cao R, Bjorndahl M, Nystrom S, Jonsson-Rylander AC, Hassani H, Hallberg B, Nordlander M, Cao Y (2003) Deletion of neuropeptide Y (NPY) 2 receptor in mice results in blockage of NPY-induced angiogenesis and delayed wound healing. Proc Natl Acad Sci USA 100: 6033–6038

    Article  PubMed  CAS  Google Scholar 

  40. Zukowska Z, Grant DS, Lee EW (2003) Neuropeptide Y: A novel mechanism for ischemic angiogenesis. Trends Cardiovasc Med 13: 86–92

    Article  PubMed  CAS  Google Scholar 

  41. Seegers HC, Hood VC, Kidd BL, Cruwys SC, Walsh DA (2003) Enhancement of angiogenesis by endogenous substance P release and neurokinin-1 receptors during neurogenic inflammation. J Pharmacol Exp Ther 306: 8–12

    Article  PubMed  CAS  Google Scholar 

  42. Mapp PI, Kidd BL, Gibson SJ, Terry JM, Revell PA, Ibrahim NB, Blake DR, Polak JM (1990) Substance P-, calcitonin gene-related peptide-and C-flanking peptide of neuropeptide Y-immunoreactive fibres are present in normal synovium but depleted in patients with rheumatoid arthritis. Neuroscience 37: 143–153

    Article  PubMed  CAS  Google Scholar 

  43. Pereira da Silva JA, Carmo-Fonseca M (1990) Peptide containing nerves in human synovium: Immunohistochemical evidence for decreased innervation in rheumatoid arthritis. J Rheumatol 17: 1592–1599

    PubMed  CAS  Google Scholar 

  44. Kabemura T, Misawa T, Chijiiwa Y, Nasu T, Nawata H (1992) Substance P, vasoactive intestinal polypeptide, and gastrin catabolism in canine liver and kidney. Dig Dis Sci 37: 1661–1665

    Article  PubMed  CAS  Google Scholar 

  45. Zhang Y, Lu L, Furlonger C, Wu GE, Paige CJ (2000) Hemokinin is a hematopoietic-specific tachykinin that regulates B lymphopoiesis. Nat Immunol 1: 392–397

    Article  PubMed  CAS  Google Scholar 

  46. Camarda V, Rizzi A, Calo G, Guerrini R, Salvadori S, Regoli D (2002) Pharmacological profile of hemokinin 1: A novel member of the tachykinin family. Life Sci 71: 363–370

    Article  PubMed  CAS  Google Scholar 

  47. Page NM, Bell NJ, Gardiner SM, Manyonda IT, Brayley KJ, Strange PG, Lowry PJ (2003) Characeterization of the endokinins: human tachykinins with cardiovascular activity. Proc Natl Acad Sci USA 100: 6245–6250

    Article  PubMed  CAS  Google Scholar 

  48. Zhang Y, Paige CJ (2003) T-cell developmental blockage by tachykinin antagonists and the role of hemokinin 1 in T lymphopoiesis. Blood 102: 2165–2172

    Article  PubMed  CAS  Google Scholar 

  49. Bellucci F, Carini F, Catalani C, Cucchi P, Lecci A, Meini S, Patacchini R, Quartara L, Ricci R, Tramontana M et al (2002) Pharmacological profile of the novel mammalian tachykinin, hemokinin 1. Br J Pharmacol 135: 266–274

    Article  PubMed  CAS  Google Scholar 

  50. Walsh DA, Hu DE, Mapp PI, Polak JM, Blake DR, Fan TP (1996) Innervation and neurokinin receptors during angiogenesis in the rat sponge granuloma. Histochem J 28: 759–769

    Article  PubMed  CAS  Google Scholar 

  51. Metwali A, Blum AM, Elliott DE, Setiawan T, Weinstock JV (2004) Cutting edge: Hemokinin has substance P-like function and expression in inflammation. J Immunol 172: 6528–6532

    PubMed  CAS  Google Scholar 

  52. Pinter E, Than M, Chu DQ, Fogg C, Brain SD (2002) Interaction between interleukin 1beta and endogenous neurokinin 1 receptor agonists in mediating plasma extravasation and neutrophil accumulation in the cutaneous microvasculature of the rat. Neurosci Lett 318: 13–16

    Article  PubMed  CAS  Google Scholar 

  53. 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

    Article  PubMed  CAS  Google Scholar 

  54. Nikitenko LL, Fox SB, Kehoe S, Rees MC, Bicknell R (2006) Adrenomedullin and tumour angiogenesis. Br J Cancer 94: 1–7

    Article  PubMed  CAS  Google Scholar 

  55. Miyashita K, Itoh H, Sawada N, Fukunaga Y, Sone M, Yamahara K, Yurugi T, Nakao K (2003) Adrenomedullin promotes proliferation and migration of cultured endothelial cells. Hypertens Res 26(Suppl): S93–98

    Article  PubMed  CAS  Google Scholar 

  56. Zhao Y, Hague S, Manek S, Zhang L, Bicknell R, Rees MC (1998) PCR display identifies tamoxifen induction of the novel angiogenic factor adrenomedullin by a non estrogenic mechanism in the human endometrium. Oncogene 16: 409–415

    Article  PubMed  CAS  Google Scholar 

  57. Nikitenko LL, MacKenzie IZ, Rees MC, Bicknell R (2000) Adrenomedullin is an autocrine regulator of endothelial growth in human endometrium. Mol Hum Reprod 6: 811–819

    Article  PubMed  CAS  Google Scholar 

  58. Oehler MK, Hague S, Rees MC, Bicknell R (2002) Adrenomedullin promots formation of xenografted endometrial tumors by stimulation of autocrine growth and angiogenesis. Oncogene 21: 2815–2821

    Article  PubMed  CAS  Google Scholar 

  59. Nagoshi Y, Kuwasako K, Ito K, Uemura T, Kato J, Kitamura K, Eto T (2002) The calcitonin receptor-like receptor/receptor activity-modifying protein 1 heterodimer can function as a calcitonin gene-related peptide-(8–37)-sensitive adrenomedullin receptor. Eur J Pharmacol 450: 237–243

    Article  PubMed  CAS  Google Scholar 

  60. Matsushita T, Matsui N, Yoshiya S, Fujioka H, Kurosaka M (2004) Production of adrenomedullin from synovial cells in rheumatoid arthritis patients. Rheumatol Int 24: 20–24

    Article  PubMed  CAS  Google Scholar 

  61. Pozo D, Delgado M, Martinez M, Guerrero JM, Leceta J, Gomariz RP, Calvo JR (2000) Immunobiology of vasoactive intestinal peptide (VIP). Immunol Today 21: 7–11

    Article  PubMed  CAS  Google Scholar 

  62. Ogasawara M, Murata J, Kamitani Y, Hayashi K, Saiki I (1999) Inhibition by vasoactive intestinal polypeptide (VIP) of angiogenesis induced by murine Colon 26-L5 carcinoma cells metastasized in liver. Clin Exp Metastasis 17: 283–291

    Article  PubMed  CAS  Google Scholar 

  63. Delgado M, Abad C, Martinez C, Leceta J, Gomariz RP (2001) Vasoactive intestinal peptide prevents experimental arthritis by downregulating both autoimmune and inflammatory components of the disease. Nat Med 7: 563–568

    Article  PubMed  CAS  Google Scholar 

  64. Dasgupta P (2004) Somatostatin analogues: Multiple roles in cellular proliferation, neoplasia, and angiogenesis. Pharmacol Ther 102: 61–85

    Article  PubMed  CAS  Google Scholar 

  65. Wu PC, Liu CC, Chen CH, Kou HK, Shen SC, Lu CY, Chou WY, Sung MT, Yang LC (2003) Inhibition of experimental angiogenesis of cornea by somatostatin. Graefes Arch Clin Exp Ophthalmol 241: 63–69

    Article  PubMed  CAS  Google Scholar 

  66. Watson JC, Balster DA, Gebhardt BM, O—Dorisio TM, O—Dorisio MS, Espenan GD, Drouant GJ, Woltering EA (2001) Growing vascular endothelial cells express somatostatin subtype 2 receptors. Br J Cancer 85: 266–272

    Article  PubMed  CAS  Google Scholar 

  67. Mentlein R, Eichler O, Forstreuter F, Held-Feindt J (2001) Somatostatin inhibits the production of vascular endothelial growth factor in human glioma cells. Int J Cancer 92: 545–550

    Article  PubMed  CAS  Google Scholar 

  68. Pal S, Wu J, Murray JK, Gellman SH, Wozniak MA, Keely PJ, Boyer ME, Gomez TM, Hasso SM, Fallon JF et al (2006) An antiangiogenic neurokinin-B/thromboxane A2 regulatory axis. J Cell Biol 174: 1047–1058

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Academic Rheumatology, University of Nottingham, Clinical Sciences Building, Nottingham City Hospital, Hucknall Road, Nottingham, NG5 1 PB, UK

    Paul L. Mapp & David A. Walsh

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  1. Paul L. Mapp
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  2. David A. Walsh
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  1. Centre for Experimental Medicine and Rheumatology William Harvey Research Institute, St. Bartholomew’s Hospital, Charterhouse Square, London, E1M 6BQ, UK

    Michael P. Seed

  2. Academic Rheumatology, University of Nottingham, Clinical Sciences Building City Hospital Hucknall Road, Nottingham, NG5 1PB, UK

    David A. Walsh

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Mapp, P.L., Walsh, D.A. (2008). Neurogenic angiogenesis and inflammation. In: Seed, M.P., Walsh, D.A. (eds) Angiogenesis in Inflammation: Mechanisms and Clinical Correlates. Progress in Inflammation Research. Birkhäuser Basel. https://doi.org/10.1007/978-3-7643-7650-5_1

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