Angiogenesis

, Volume 21, Issue 1, pp 1–14 | Cite as

Mechanisms of angiogenesis in microbe-regulated inflammatory and neoplastic conditions

  • Sanaullah Sajib
  • Fatema Tuz Zahra
  • Michail S. Lionakis
  • Nadezhda A. German
  • Constantinos M. Mikelis
Review Paper

Abstract

Commensal microbiota inhabit all the mucosal surfaces of the human body. It plays significant roles during homeostatic conditions, and perturbations in numbers and/or products are associated with several pathological disorders. Angiogenesis, the process of new vessel formation, promotes embryonic development and critically modulates several biological processes during adulthood. Indeed, deregulated angiogenesis can induce or augment several pathological conditions. Accumulating evidence has implicated the angiogenic process in various microbiota-associated human diseases. Herein, we critically review diseases that are regulated by microbiota and are affected by angiogenesis, aiming to provide a broad understanding of how angiogenesis is involved and how microbiota regulate angiogenesis in microbiota-associated human conditions.

Keywords

Microbiota Angiogenesis Gastritis Ulcer Cancer IBD 

Notes

Acknowledgements

MSL’s contribution was supported by the Division of Intramural Research, NIAID, NIH.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Carmeliet P (2000) Mechanisms of angiogenesis and arteriogenesis. Nat Med 6(4):389–395.  https://doi.org/10.1038/74651 PubMedCrossRefGoogle Scholar
  2. 2.
    Rieder F, Fiocchi C (2009) Intestinal fibrosis in IBD–a dynamic, multifactorial process. Nat Rev Gastroenterol Hepatol 6(4):228–235.  https://doi.org/10.1038/nrgastro.2009.31 PubMedCrossRefGoogle Scholar
  3. 3.
    Mongiat M, Andreuzzi E, Tarticchio G, Paulitti A (2016) Extracellular matrix, a hard player in angiogenesis. Int J Mol Sci.  https://doi.org/10.3390/ijms17111822 PubMedPubMedCentralGoogle Scholar
  4. 4.
    Human Microbiome Jumpstart Reference Strains C, Nelson KE, Weinstock GM, Highlander SK, Worley KC, Creasy HH, Wortman JR, Rusch DB, Mitreva M, Sodergren E, Chinwalla AT, Feldgarden M, Gevers D, Haas BJ, Madupu R, Ward DV, Birren BW, Gibbs RA, Methe B, Petrosino JF, Strausberg RL, Sutton GG, White OR, Wilson RK, Durkin S, Giglio MG, Gujja S, Howarth C, Kodira CD, Kyrpides N, Mehta T, Muzny DM, Pearson M, Pepin K, Pati A, Qin X, Yandava C, Zeng Q, Zhang L, Berlin AM, Chen L, Hepburn TA, Johnson J, McCorrison J, Miller J, Minx P, Nusbaum C, Russ C, Sykes SM, Tomlinson CM, Young S, Warren WC, Badger J, Crabtree J, Markowitz VM, Orvis J, Cree A, Ferriera S, Fulton LL, Fulton RS, Gillis M, Hemphill LD, Joshi V, Kovar C, Torralba M, Wetterstrand KA, Abouellleil A, Wollam AM, Buhay CJ, Ding Y, Dugan S, FitzGerald MG, Holder M, Hostetler J, Clifton SW, Allen-Vercoe E, Earl AM, Farmer CN, Liolios K, Surette MG, Xu Q, Pohl C, Wilczek-Boney K, Zhu D (2010) A catalog of reference genomes from the human microbiome. Science 328(5981):994–999.  https://doi.org/10.1126/science.1183605 CrossRefGoogle Scholar
  5. 5.
    Leger AJS, Desai JV, Drummond RA, Kugadas A, Almaghrabi F, Silver P, Raychaudhuri K, Gadjeva M, Iwakura Y, Lionakis MS, Caspi RR (2017) An ocular commensal protects against corneal infection by driving an interleukin-17 response from mucosal gammadelta T cells. Immunity 47(1):148–158.  https://doi.org/10.1016/j.immuni.2017.06.014 CrossRefGoogle Scholar
  6. 6.
    Proctor DM, Relman DA (2017) The landscape ecology and microbiota of the human nose, mouth, and throat. Cell Host Microbe 21(4):421–432.  https://doi.org/10.1016/j.chom.2017.03.011 PubMedCrossRefGoogle Scholar
  7. 7.
    Morris A, Beck JM, Schloss PD, Campbell TB, Crothers K, Curtis JL, Flores SC, Fontenot AP, Ghedin E, Huang L, Jablonski K, Kleerup E, Lynch SV, Sodergren E, Twigg H, Young VB, Bassis CM, Venkataraman A, Schmidt TM, Weinstock GM, Lung HIVMP (2013) Comparison of the respiratory microbiome in healthy nonsmokers and smokers. Am J Respir Crit Care Med 187(10):1067–1075.  https://doi.org/10.1164/rccm.201210-1913OC PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Ravel J, Gajer P, Abdo Z, Schneider GM, Koenig SS, McCulle SL, Karlebach S, Gorle R, Russell J, Tacket CO, Brotman RM, Davis CC, Ault K, Peralta L, Forney LJ (2011) Vaginal microbiome of reproductive-age women. Proc Natl Acad Sci U S A 108(Suppl 1):4680–4687.  https://doi.org/10.1073/pnas.1002611107 PubMedCrossRefGoogle Scholar
  9. 9.
    Gill SR, Pop M, Deboy RT, Eckburg PB, Turnbaugh PJ, Samuel BS, Gordon JI, Relman DA, Fraser-Liggett CM, Nelson KE (2006) Metagenomic analysis of the human distal gut microbiome. Science 312(5778):1355–1359.  https://doi.org/10.1126/science.1124234 PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO (2007) Development of the human infant intestinal microbiota. PLoS Biol 5(7):e177.  https://doi.org/10.1371/journal.pbio.0050177 PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Clark JA, Coopersmith CM (2007) Intestinal crosstalk: a new paradigm for understanding the gut as the “motor” of critical illness. Shock 28(4):384–393.  https://doi.org/10.1097/shk.0b013e31805569df PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Gerritsen J, Smidt H, Rijkers GT, de Vos WM (2011) Intestinal microbiota in human health and disease: the impact of probiotics. Genes Nutr 6(3):209–240.  https://doi.org/10.1007/s12263-011-0229-7 PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Hill DA, Artis D (2010) Intestinal bacteria and the regulation of immune cell homeostasis. Annu Rev Immunol 28:623–667.  https://doi.org/10.1146/annurev-immunol-030409-101330 PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    Mueller C, Macpherson AJ (2006) Layers of mutualism with commensal bacteria protect us from intestinal inflammation. Gut 55(2):276–284.  https://doi.org/10.1136/gut.2004.054098 PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Guarner F, Malagelada J-R (2003) Gut flora in health and disease. Lancet 361(9356):512–519.  https://doi.org/10.1016/s0140-6736(03)12489-0 PubMedCrossRefGoogle Scholar
  16. 16.
    Stappenbeck TS, Hooper LV, Gordon JI (2002) Developmental regulation of intestinal angiogenesis by indigenous microbes via Paneth cells. Proc Natl Acad Sci U S A 99(24):15451–15455.  https://doi.org/10.1073/pnas.202604299 PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Cohen LJ, Esterhazy D, Kim S-H, Lemetre C, Aguilar RR, Gordon EA, Pickard AJ, Cross JR, Emiliano AB, Han SM, Chu J, Vila-Farres X, Kaplitt J, Rogoz A, Calle PY, Hunter C, Bitok JK, Brady SF (2017) Commensal bacteria make GPCR ligands that mimic human signalling molecules. Nature.  https://doi.org/10.1038/nature23874. http://www.nature.com/nature/journal/vaop/ncurrent/abs/nature23874.html#supplementary-information
  18. 18.
    Reinhardt C, Bergentall M, Greiner TU, Schaffner F, Ostergren-Lunden G, Petersen LC, Ruf W, Backhed F (2012) Tissue factor and PAR1 promote microbiota-induced intestinal vascular remodelling. Nature 483(7391):627–631.  https://doi.org/10.1038/nature10893 PubMedCrossRefGoogle Scholar
  19. 19.
    Macfarlane GT, Cummings JH (1999) Probiotics and prebiotics: can regulating the activities of intestinal bacteria benefit health? BMJ.  https://doi.org/10.1136/bmj.318.7189.999 Google Scholar
  20. 20.
    De Spiegeleer B, Verbeke F, D’Hondt M, Hendrix A, Van De Wiele C, Burvenich C, Peremans K, De Wever O, Bracke M, Wynendaele E (2015) The quorum sensing peptides PhrG, CSP and EDF promote angiogenesis and invasion of breast cancer cells in vitro. PLoS ONE 10(3):e0119471.  https://doi.org/10.1371/journal.pone.0119471 PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    Danese S, Sans M, de la Motte C, Graziani C, West G, Phillips MH, Pola R, Rutella S, Willis J, Gasbarrini A, Fiocchi C (2006) Angiogenesis as a novel component of inflammatory bowel disease pathogenesis. Gastroenterology 130(7):2060–2073.  https://doi.org/10.1053/j.gastro.2006.03.054 PubMedCrossRefGoogle Scholar
  22. 22.
    Scaldaferri F, Vetrano S, Sans M, Arena V, Straface G, Stigliano E, Repici A, Sturm A, Malesci A, Panes J, Yla-Herttuala S, Fiocchi C, Danese S (2009) VEGF-A links angiogenesis and inflammation in inflammatory bowel disease pathogenesis. Gastroenterology 136(2):585–595.  https://doi.org/10.1053/j.gastro.2008.09.064 PubMedCrossRefGoogle Scholar
  23. 23.
    Danese S, Sans M, Spencer DM, Beck I, Donate F, Plunkett ML, de la Motte C, Redline R, Shaw DE, Levine AD, Mazar AP, Fiocchi C (2007) Angiogenesis blockade as a new therapeutic approach to experimental colitis. Gut 56(6):855–862.  https://doi.org/10.1136/gut.2006.114314 PubMedCrossRefGoogle Scholar
  24. 24.
    Werth N, Beerlage C, Rosenberger C, Yazdi AS, Edelmann M, Amr A, Bernhardt W, von Eiff C, Becker K, Schafer A, Peschel A, Kempf VA (2010) Activation of hypoxia inducible factor 1 is a general phenomenon in infections with human pathogens. PLoS ONE 5(7):e11576.  https://doi.org/10.1371/journal.pone.0011576 PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.
    Hartmann H, Eltzschig HK, Wurz H, Hantke K, Rakin A, Yazdi AS, Matteoli G, Bohn E, Autenrieth IB, Karhausen J, Neumann D, Colgan SP, Kempf VA (2008) Hypoxia-independent activation of HIF-1 by enterobacteriaceae and their siderophores. Gastroenterology 134(3):756–767.  https://doi.org/10.1053/j.gastro.2007.12.008 PubMedCrossRefGoogle Scholar
  26. 26.
    Gunawan E, Tsuji S, Tsujii M, Kimura A, Sun W-H, Sawaoka H, Sasayama Y, Sasaki Y, Kawano S, Hori M (2002) Influences of Helicobacter pylorion gastric angiogenesis and ulcer healing in mice. J Gastroenterol Hepatol 17(9):960–965.  https://doi.org/10.1046/j.1440-1746.2002.02782.x PubMedCrossRefGoogle Scholar
  27. 27.
    Haesebrouck F, Pasmans F, Flahou B, Chiers K, Baele M, Meyns T, Decostere A, Ducatelle R (2009) Gastric helicobacters in domestic animals and nonhuman primates and their significance for human health. Clin Microbiol Rev 22(2):202–223, Table of Contents.  https://doi.org/10.1128/CMR.00041-08
  28. 28.
    Yamaoka Y (2010) Mechanisms of disease: Helicobacter pylori virulence factors. Nat Rev Gastroenterol Hepatol 7(11):629–641.  https://doi.org/10.1038/nrgastro.2010.154 PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Stephenson JR, Purcell RH, Hall RA (2014) The BAI subfamily of adhesion GPCRs: synaptic regulation and beyond. Trends Pharmacol Sci 35(4):208–215.  https://doi.org/10.1016/j.tips.2014.02.002 PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Park D, Tosello-Trampont AC, Elliott MR, Lu M, Haney LB, Ma Z, Klibanov AL, Mandell JW, Ravichandran KS (2007) BAI1 is an engulfment receptor for apoptotic cells upstream of the ELMO/Dock180/Rac module. Nature 450(7168):430–434.  https://doi.org/10.1038/nature06329 PubMedCrossRefGoogle Scholar
  31. 31.
    Das S, Sarkar A, Ryan KA, Fox S, Berger AH, Juncadella IJ, Bimczok D, Smythies LE, Harris PR, Ravichandran KS, Crowe SE, Smith PD, Ernst PB (2014) Brain angiogenesis inhibitor 1 is expressed by gastric phagocytes during infection with Helicobacter pylori and mediates the recognition and engulfment of human apoptotic gastric epithelial cells. FASEB J 28(5):2214–2224.  https://doi.org/10.1096/fj.13-243238 PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Uehara A, Takada H (2007) Functional TLRs and NODs in human gingival fibroblasts. J Dent Res 86(3):249–254.  https://doi.org/10.1177/154405910708600310 PubMedCrossRefGoogle Scholar
  33. 33.
    Schirbel A, Kessler S, Rieder F, West G, Rebert N, Asosingh K, McDonald C, Fiocchi C (2013) Pro-angiogenic activity of TLRs and NLRs: a novel link between gut microbiota and intestinal angiogenesis. Gastroenterology 144(3):613–623.  https://doi.org/10.1053/j.gastro.2012.11.005 PubMedCrossRefGoogle Scholar
  34. 34.
    Clark IM, Swingler TE, Sampieri CL, Edwards DR (2008) The regulation of matrix metalloproteinases and their inhibitors. Int J Biochem Cell Biol 40(6–7):1362–1378.  https://doi.org/10.1016/j.biocel.2007.12.006 PubMedCrossRefGoogle Scholar
  35. 35.
    Bergin PJ, Anders E, Sicheng W, Erik J, Jennie A, Hans L, Pierre M, Qiang PH, Marianne QJ (2004) Increased production of matrix metalloproteinases in Helicobacter pylori-associated human gastritis. Helicobacter 9(3):201–210.  https://doi.org/10.1111/j.1083-4389.2004.00232.x PubMedCrossRefGoogle Scholar
  36. 36.
    Kubben FJ, Sier CF, Schram MT, Witte AM, Veenendaal RA, van Duijn W, Verheijen JH, Hanemaaijer R, Lamers CB, Verspaget HW (2007) Eradication of Helicobacter pylori infection favourably affects altered gastric mucosal MMP-9 levels. Helicobacter 12(5):498–504.  https://doi.org/10.1111/j.1523-5378.2007.00527.x PubMedCrossRefGoogle Scholar
  37. 37.
    Rautelin HI, Oksanen AM, Veijola LI, Sipponen PI, Tervahartiala TI, Sorsa TA, Lauhio A (2009) Enhanced systemic matrix metalloproteinase response in Helicobacter pylori gastritis. Ann Med 41(3):208–215.  https://doi.org/10.1080/07853890802482452 PubMedCrossRefGoogle Scholar
  38. 38.
    Wroblewski LE, Noble PJ, Pagliocca A, Pritchard DM, Hart CA, Campbell F, Dodson AR, Dockray GJ, Varro A (2003) Stimulation of MMP-7 (matrilysin) by Helicobacter pylori in human gastric epithelial cells: role in epithelial cell migration. J Cell Sci 116(Pt 14):3017–3026.  https://doi.org/10.1242/jcs.00518 PubMedCrossRefGoogle Scholar
  39. 39.
    Pero R, Peluso S, Angrisano T, Tuccillo C, Sacchetti S, Keller S, Tomaiuolo R, Bruni CB, Lembo F, Chiariotti L (2011) Chromatin and DNA methylation dynamics of Helicobacter pylori-induced COX-2 activation. Int J Med Microbiol 301(2):140–149.  https://doi.org/10.1016/j.ijmm.2010.06.009 PubMedCrossRefGoogle Scholar
  40. 40.
    Fu S, Ramanujam KS, Wong A, Fantry GT, Drachenberg CB, James SP, Meltzer SJ, Wilson KT (1999) Increased expression and cellular localization of inducible nitric oxide synthase and cyclooxygenase 2 in Helicobacter pylori gastritis. Gastroenterology 116(6):1319–1329PubMedCrossRefGoogle Scholar
  41. 41.
    Morrissey JH, Fakhrai H, Edgington TS (1987) Molecular cloning of the cDNA for tissue factor, the cellular receptor for the initiation of the coagulation protease cascade. Cell 50(1):129–135PubMedCrossRefGoogle Scholar
  42. 42.
    Carmeliet P, Mackman N, Moons L, Luther T, Gressens P, Van Vlaenderen I, Demunck H, Kasper M, Breier G, Evrard P, Muller M, Risau W, Edgington T, Collen D (1996) Role of tissue factor in embryonic blood vessel development. Nature 383(6595):73–75.  https://doi.org/10.1038/383073a0 PubMedCrossRefGoogle Scholar
  43. 43.
    Moore WEC, Holdeman LV (1974) Human fecal flora: the normal flora of 20 Japanese-Hawaiians. Appl Microbiol 27(5):961–979PubMedPubMedCentralGoogle Scholar
  44. 44.
    Ouellette AJ, Selsted ME (1996) Paneth cell defensins: endogenous peptide components of intestinal host defense. FASEB J 10(11):1280–1289PubMedCrossRefGoogle Scholar
  45. 45.
    Ayabe T, Satchell DP, Wilson CL, Parks WC, Selsted ME, Ouellette AJ (2000) Secretion of microbicidal alpha-defensins by intestinal Paneth cells in response to bacteria. Nat Immunol 1(2):113–118.  https://doi.org/10.1038/77783 PubMedCrossRefGoogle Scholar
  46. 46.
    Tarnawski AS (2005) Cellular and molecular mechanisms of gastrointestinal ulcer healing. Dig Dis Sci 50(Suppl 1):S24–S33.  https://doi.org/10.1007/s10620-005-2803-6 PubMedCrossRefGoogle Scholar
  47. 47.
    Ricardo SD, van Goor H, Eddy AA (2008) Macrophage diversity in renal injury and repair. J Clin Investig 118(11):3522–3530.  https://doi.org/10.1172/JCI36150 PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Zavros Y, Orr MA, Xiao C, Malinowska DH (2008) Sonic hedgehog is associated with H + −K + −ATPase-containing membranes in gastric parietal cells and secreted with histamine stimulation. Am J Physiol Gastrointest Liver Physiol 295(1):G99–G111.  https://doi.org/10.1152/ajpgi.00389.2007 PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    Waghray M, Zavros Y, Saqui-Salces M, El-Zaatari M, Alamelumangapuram CB, Todisco A, Eaton KA, Merchant JL (2010) Interleukin-1beta promotes gastric atrophy through suppression of Sonic Hedgehog. Gastroenterology 138(2):562–572.  https://doi.org/10.1053/j.gastro.2009.10.043 PubMedCrossRefGoogle Scholar
  50. 50.
    Xiao C, Ogle SA, Schumacher MA, Orr-Asman MA, Miller ML, Lertkowit N, Varro A, Hollande F, Zavros Y (2010) Loss of parietal cell expression of Sonic hedgehog induces hypergastrinemia and hyperproliferation of surface mucous cells. Gastroenterology 138(2):550–561.  https://doi.org/10.1053/j.gastro.2009.11.002 PubMedCrossRefGoogle Scholar
  51. 51.
    Schumacher MA, Donnelly JM, Engevik AC, Xiao C, Yang L, Kenny S, Varro A, Hollande F, Samuelson LC, Zavros Y (2012) Gastric Sonic Hedgehog acts as a macrophage chemoattractant during the immune response to Helicobacter pylori. Gastroenterology 142(5):1150–1159.  https://doi.org/10.1053/j.gastro.2012.01.029 PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Xiao C, Feng R, Engevik AC, Martin JR, Tritschler JA, Schumacher M, Koncar R, Roland J, Nam KT, Goldenring JR, Zavros Y (2013) Sonic Hedgehog contributes to gastric mucosal restitution after injury. Lab Investig 93(1):96–111.  https://doi.org/10.1038/labinvest.2012.148 PubMedCrossRefGoogle Scholar
  53. 53.
    Choi KS, Song H, Kim EH, Choi JH, Hong H, Han YM, Hahm KB (2012) Inhibition of hydrogen sulfide-induced angiogenesis and inflammation in vascular endothelial cells: potential mechanisms of gastric cancer prevention by Korean Red Ginseng. J Ginseng Res 36(2):135–145.  https://doi.org/10.5142/jgr.2012.36.2.135 PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Keates AC, Tummala S, Peek RM Jr, Csizmadia E, Kunzli B, Becker K, Correa P, Romero-Gallo J, Piazuelo MB, Sheth S, Kelly CP, Robson SC, Keates S (2008) Helicobacter pylori infection stimulates plasminogen activator inhibitor 1 production by gastric epithelial cells. Infect Immun 76(9):3992–3999.  https://doi.org/10.1128/IAI.00584-08 PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Tuccillo C, Cuomo A, Rocco A, Martinelli E, Staibano S, Mascolo M, Gravina AG, Nardone G, Ricci V, Ciardiello F, Del Vecchio Blanco C, Romano M (2005) Vascular endothelial growth factor and neo-angiogenesis in H. pylori gastritis in humans. J Pathol 207(3):277–284.  https://doi.org/10.1002/path.1844 PubMedCrossRefGoogle Scholar
  56. 56.
    Nakamura M, Murayama SY, Serizawa H, Sekiya Y, Eguchi M, Takahashi S, Nishikawa K, Takahashi T, Matsumoto T, Yamada H, Hibi T, Tsuchimoto K, Matsui H (2007) “Candidatus Helicobacter heilmannii” from a cynomolgus monkey induces gastric mucosa-associated lymphoid tissue lymphomas in C57BL/6 mice. Infect Immun 75(3):1214–1222.  https://doi.org/10.1128/IAI.01459-06 PubMedCrossRefGoogle Scholar
  57. 57.
    Nakamura M, Tsuchimoto K, Matsui H (2005) Relation of Helicobacter heilmannii to gastric mucosal damage as a model of zoonosis between men and pets. Nihon Rinsho 63(Suppl 11):605–608PubMedGoogle Scholar
  58. 58.
    Genta RM, Huberman RM, Graham DY (1994) The gastric cardia in Helicobacter pylori infection. Hum Pathol 25(9):915–919.  https://doi.org/10.1016/0046-8177(94)90011-6 PubMedCrossRefGoogle Scholar
  59. 59.
    Nakamura M, Matsui H, Murayama SY, Matsumoto T, Yamada H, Takahashi S, Tsuchimoto K (2007) Interaction of VEGF to gastric low grade MALT lymphoma by Helicobacter heilmannii infection in C57/BL/6 mice. Inflammopharmacology 15(3):115–118.  https://doi.org/10.1007/s10787-007-1549-5 PubMedCrossRefGoogle Scholar
  60. 60.
    Nishikawa K, Nakamura M, Takahashi S, Matsui H, Murayama SY, Matsumoto T, Yamada H, Tsuchimoto K (2007) Increased apoptosis and angiogenesis in gastric low-grade mucosa-associated lymphoid tissue-type lymphoma by Helicobacter heilmannii infection in C57/BL6 mice. FEMS Immunol Med Microbiol 50(2):268–272.  https://doi.org/10.1111/j.1574-695X.2007.00252.x PubMedCrossRefGoogle Scholar
  61. 61.
    Nakamura M, Takahashi T, Matsui H, Takahashi S, Murayama SY, Suzuki H, Tsuchimoto K (2014) New pharmaceutical treatment of gastric MALT lymphoma: anti-angiogenesis treatment using VEGF receptor antibodies and celecoxib. Curr Pharm Des 20(7):1097–1103PubMedPubMedCentralCrossRefGoogle Scholar
  62. 62.
    Asaka M (2002) Helicobacter pylori infection and gastric cancer. Intern Med 41(1):1–6PubMedCrossRefGoogle Scholar
  63. 63.
    Ren Z, Pang G, Clancy R, Li LC, Lee CS, Batey R, Borody T, Dunkley M (2001) Shift of the gastric T-cell response in gastric carcinoma. J Gastroenterol Hepatol 16(2):142–148.  https://doi.org/10.1046/j.1440-1746.2001.02385.x PubMedCrossRefGoogle Scholar
  64. 64.
    Siegel RL, Miller KD, Jemal A (2017) Cancer statistics, 2017. CA Cancer J Clin 67(1):7–30.  https://doi.org/10.3322/caac.21387 PubMedCrossRefGoogle Scholar
  65. 65.
    Venerito M, Vasapolli R, Malfertheiner P (2016) Helicobacter pylori and gastric cancer: timing and impact of preventive measures. Adv Exp Med Biol 908:409–418.  https://doi.org/10.1007/978-3-319-41388-4_20 PubMedCrossRefGoogle Scholar
  66. 66.
    Macedo F, Ladeira K, Longatto-Filho A, Martins SF (2017) Gastric cancer and angiogenesis: Is VEGF a useful biomarker to assess progression and remission? J Gastric Cancer 17(1):1–10.  https://doi.org/10.5230/jgc.2017.17.e1 PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Takahashi Y, Cleary KR, Mai M, Kitadai Y, Bucana CD, Ellis LM (1996) Significance of vessel count and vascular endothelial growth factor and its receptor (KDR) in intestinal-type gastric cancer. Clin Cancer Res 2(10):1679–1684PubMedGoogle Scholar
  68. 68.
    Maeda K, Kang SM, Onoda N, Ogawa M, Kato Y, Sawada T, Chung KH (1999) Vascular endothelial growth factor expression in preoperative biopsy specimens correlates with disease recurrence in patients with early gastric carcinoma. Cancer 86(4):566–571PubMedCrossRefGoogle Scholar
  69. 69.
    Kanai T, Konno H, Tanaka T, Baba M, Matsumoto K, Nakamura S, Yukita A, Asano M, Suzuki H, Baba S (1998) Anti-tumor and anti-metastatic effects of human-vascular-endothelial-growth-factor-neutralizing antibody on human colon and gastric carcinoma xenotransplanted orthotopically into nude mice. Int J Cancer 77(6):933–936PubMedCrossRefGoogle Scholar
  70. 70.
    Caputo R, Tuccillo C, Manzo BA, Zarrilli R, Tortora G, Blanco CDV, Ricci V, Ciardiello F, Romano M (2003) Helicobacter pylori VacA toxin upregulates vascular endothelial growth factor expression in MKN 28 gastric cells through an epidermal growth factor receptor-, cyclooxygenase-2-dependent mechanism. Clin Cancer Res 9(6):2015–2021PubMedGoogle Scholar
  71. 71.
    Park JH, Kim TY, Jong HS, Kim TY, Chun YS, Park JW, Lee CT, Jung HC, Kim NK, Bang YJ (2003) Gastric epithelial reactive oxygen species prevent normoxic degradation of hypoxia-inducible factor-1alpha in gastric cancer cells. Clin Cancer Res 9(1):433–440PubMedGoogle Scholar
  72. 72.
    Dumas EK, Cox PM, Fullenwider CO, Nguyen M, Centola M, Frank MB, Dozmorov I, James JA, Farris AD (2011) Anthrax lethal toxin-induced gene expression changes in mouse lung. Toxins (Basel) 3(9):1111–1130.  https://doi.org/10.3390/toxins3091111 CrossRefGoogle Scholar
  73. 73.
    Innocenti M, Thoreson AC, Ferrero RL, Stromberg E, Bolin I, Eriksson L, Svennerholm AM, Quiding-Jarbrink M (2002) Helicobacter pylori-induced activation of human endothelial cells. Infect Immun 70(8):4581–4590PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Yeo M, Kim DK, Han SU, Lee JE, Kim YB, Cho YK, Kim JH, Cho SW, Hahm KB (2006) Novel action of gastric proton pump inhibitor on suppression of Helicobacter pylori induced angiogenesis. Gut 55(1):26–33.  https://doi.org/10.1136/gut.2005.067454 PubMedPubMedCentralCrossRefGoogle Scholar
  75. 75.
    Koch A, Polverini P, Kunkel S, Harlow L, DiPietro L, Elner V, Elner S, Strieter R (1992) Interleukin-8 as a macrophage-derived mediator of angiogenesis. Science 258(5089):1798–1801.  https://doi.org/10.1126/science.1281554 PubMedCrossRefGoogle Scholar
  76. 76.
    Strieter RM, Kunkel SL, Elner VM, Martonyi CL, Koch AE, Polverini PJ, Elner SG (1992) Interleukin-8. A corneal factor that induces neovascularization. Am J Pathol 141(6):1279–1284PubMedPubMedCentralGoogle Scholar
  77. 77.
    Kuai WX, Wang Q, Yang XZ, Zhao Y, Yu R, Tang XJ (2012) Interleukin-8 associates with adhesion, migration, invasion and chemosensitivity of human gastric cancer cells. World J Gastroenterol 18(9):979–985.  https://doi.org/10.3748/wjg.v18.i9.979 PubMedPubMedCentralCrossRefGoogle Scholar
  78. 78.
    Ju D, Sun D, Xiu L, Meng X, Zhang C, Wei P (2012) Interleukin-8 is associated with adhesion, migration and invasion in human gastric cancer SCG-7901 cells. Med Oncol 29(1):91–99.  https://doi.org/10.1007/s12032-010-9780-0 PubMedCrossRefGoogle Scholar
  79. 79.
    Kitadai Y, Haruma K, Mukaida N, Ohmoto Y, Matsutani N, Yasui W, Yamamoto S, Sumii K, Kajiyama G, Fidler IJ, Tahara E (2000) Regulation of disease-progression genes in human gastric carcinoma cells by interleukin 8. Clin Cancer Res 6(7):2735–2740PubMedGoogle Scholar
  80. 80.
    Waugh DJ, Wilson C (2008) The interleukin-8 pathway in cancer. Clin Cancer Res 14(21):6735–6741.  https://doi.org/10.1158/1078-0432.CCR-07-4843 PubMedCrossRefGoogle Scholar
  81. 81.
    Shi J, Li YJ, Yan B, Wei PK (2015) Interleukin-8: a potent promoter of human lymphatic endothelial cell growth in gastric cancer. Oncol Rep 33(6):2703–2710.  https://doi.org/10.3892/or.2015.3916 PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    Eftang LL, Esbensen Y, Tannaes TM, Bukholm IR, Bukholm G (2012) Interleukin-8 is the single most up-regulated gene in whole genome profiling of H. pylori exposed gastric epithelial cells. BMC Microbiol 12:9.  https://doi.org/10.1186/1471-2180-12-9 PubMedPubMedCentralCrossRefGoogle Scholar
  83. 83.
    Ando T, Kusugami K, Ohsuga M, Shinoda M, Sakakibara M, Saito H, Fukatsu A, Ichiyama S, Ohta M (1996) Interleukin-8 activity correlates with histological severity in Helicobacter pylori-associated antral gastritis. Am J Gastroenterol 91(6):1150–1156PubMedGoogle Scholar
  84. 84.
    Lin CS, He PJ, Hsu WT, Wu MS, Wu CJ, Shen HW, Hwang CH, Lai YK, Tsai NM, Liao KW (2010) Helicobacter pylori-derived heat shock protein 60 enhances angiogenesis via a CXCR2-mediated signaling pathway. Biochem Biophys Res Commun 397(2):283–289.  https://doi.org/10.1016/j.bbrc.2010.05.101 PubMedCrossRefGoogle Scholar
  85. 85.
    Zhang L-J (2009) Anti-Helicobacter pylori therapy followed by celecoxib on progression of gastric precancerous lesions. World J Gastroenterol 15(22):2731.  https://doi.org/10.3748/wjg.15.2731 PubMedPubMedCentralCrossRefGoogle Scholar
  86. 86.
    Targosz A, Brzozowski T, Pierzchalski P, Szczyrk U, Ptak-Belowska A, Konturek SJ, Pawlik W (2012) Helicobacter pylori promotes apoptosis, activates cyclooxygenase (COX)-2 and inhibits heat shock protein HSP70 in gastric cancer epithelial cells. Inflamm Res 61(9):955–966.  https://doi.org/10.1007/s00011-012-0487-x PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    Saukkonen K, Rintahaka J, Sivula A, Buskens CJ, Van Rees BP, Rio MC, Haglund C, Van Lanschot JJ, Offerhaus GJ, Ristimaki A (2003) Cyclooxygenase-2 and gastric carcinogenesis. APMIS 111(10):915–925PubMedCrossRefGoogle Scholar
  88. 88.
    Uefuji K, Ichikura T, Mochizuki H (2000) Cyclooxygenase-2 expression is related to prostaglandin biosynthesis and angiogenesis in human gastric cancer. Clin Cancer Res 6(1):135–138PubMedGoogle Scholar
  89. 89.
    Bamba H, Ota S, Kato A, Kawamoto C, Fujiwara K (2000) Prostaglandins up-regulate vascular endothelial growth factor production through distinct pathways in differentiated U937 cells. Biochem Biophys Res Commun 273(2):485–491.  https://doi.org/10.1006/bbrc.2000.2969 PubMedCrossRefGoogle Scholar
  90. 90.
    Vidal O, Soriano-Izquierdo A, Pera M, Elizalde JI, Palacin A, Castells A, Pique JM, Volant A, Metges JP (2008) Positive VEGF immunostaining independently predicts poor prognosis in curatively resected gastric cancer patients: results of a study assessing a panel of angiogenic markers. J Gastrointest Surg 12(6):1005–1014.  https://doi.org/10.1007/s11605-007-0336-3 PubMedCrossRefGoogle Scholar
  91. 91.
    Yao L, Liu F, Hong L, Sun L, Liang S, Wu K, Fan D (2011) The function and mechanism of COX-2 in angiogenesis of gastric cancer cells. J Exp Clin Cancer Res.  https://doi.org/10.1186/1756-9966-30-13 PubMedPubMedCentralGoogle Scholar
  92. 92.
    Kim N, Kim CH, Ahn DW, Lee KS, Cho SJ, Park JH, Lee MK, Kim JS, Jung HC, Song IS (2009) Anti-gastric cancer effects of celecoxib, a selective COX-2 inhibitor, through inhibition of Akt signaling. J Gastroenterol Hepatol 24(3):480–487.  https://doi.org/10.1111/j.1440-1746.2008.05599.x PubMedCrossRefGoogle Scholar
  93. 93.
    Pidgeon GP, Barr MP, Harmey JH, Foley DA, Bouchier-Hayes DJ (2001) Vascular endothelial growth factor (VEGF) upregulates BCL-2 and inhibits apoptosis in human and murine mammary adenocarcinoma. Br J Cancer 85(2):273–278.  https://doi.org/10.1054/bjoc.2001.1876 PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Chu AJ, Chou TH, Chen BD (2004) Prevention of colorectal cancer using COX-2 inhibitors: basic science and clinical applications. Front Biosci 9:2697–2713PubMedCrossRefGoogle Scholar
  95. 95.
    Rao DS, Gui D, Koski ME, Popoviciu LM, Wang H, Reiter RE, Said JW (2006) An inverse relation between COX-2 and E-cadherin expression correlates with aggressive histologic features in prostate cancer. Appl Immunohistochem Mol Morphol 14(4):375–383.  https://doi.org/10.1097/01.pai.0000210417.61117.6c PubMedCrossRefGoogle Scholar
  96. 96.
    Dicken BJ, Graham K, Hamilton SM, Andrews S, Lai R, Listgarten J, Jhangri GS, Saunders LD, Damaraju S, Cass C (2006) Lymphovascular invasion is associated with poor survival in gastric cancer. Ann Surg 243(1):64–73.  https://doi.org/10.1097/01.sla.0000194087.96582.3e PubMedPubMedCentralCrossRefGoogle Scholar
  97. 97.
    Zhao Y, Zhou S, Heng CK (2009) Celecoxib inhibits serum amyloid a-induced matrix metalloproteinase-10 expression in human endothelial cells. J Vasc Res 46(1):64–72.  https://doi.org/10.1159/000139134 PubMedCrossRefGoogle Scholar
  98. 98.
    Hakansson A, Molin G (2011) Gut microbiota and inflammation. Nutrients 3(6):637–682.  https://doi.org/10.3390/nu3060637 PubMedPubMedCentralCrossRefGoogle Scholar
  99. 99.
    West NR, McCuaig S, Franchini F, Powrie F (2015) Emerging cytokine networks in colorectal cancer. Nat Rev Immunol 15(10):615–629.  https://doi.org/10.1038/nri3896 PubMedCrossRefGoogle Scholar
  100. 100.
    Sanz-Pamplona R, Berenguer A, Cordero D, Mollevi DG, Crous-Bou M, Sole X, Pare-Brunet L, Guino E, Salazar R, Santos C, de Oca J, Sanjuan X, Rodriguez-Moranta F, Moreno V (2014) Aberrant gene expression in mucosa adjacent to tumor reveals a molecular crosstalk in colon cancer. Mol Cancer 13:46.  https://doi.org/10.1186/1476-4598-13-46 PubMedPubMedCentralCrossRefGoogle Scholar
  101. 101.
    Prorok-Hamon M, Friswell MK, Alswied A, Roberts CL, Song F, Flanagan PK, Knight P, Codling C, Marchesi JR, Winstanley C, Hall N, Rhodes JM, Campbell BJ (2014) Colonic mucosa-associated diffusely adherent afaC + Escherichia coli expressing lpfA and pks are increased in inflammatory bowel disease and colon cancer. Gut 63(5):761–770.  https://doi.org/10.1136/gutjnl-2013-304739 PubMedCrossRefGoogle Scholar
  102. 102.
    Cane G, Ginouves A, Marchetti S, Busca R, Pouyssegur J, Berra E, Hofman P, Vouret-Craviari V (2010) HIF-1alpha mediates the induction of IL-8 and VEGF expression on infection with Afa/Dr diffusely adhering E. coli and promotes EMT-like behaviour. Cell Microbiol 12(5):640–653.  https://doi.org/10.1111/j.1462-5822.2009.01422.x PubMedCrossRefGoogle Scholar
  103. 103.
    Waldner MJ, Wirtz S, Jefremow A, Warntjen M, Neufert C, Atreya R, Becker C, Weigmann B, Vieth M, Rose-John S, Neurath MF (2010) VEGF receptor signaling links inflammation and tumorigenesis in colitis-associated cancer. J Exp Med 207(13):2855–2868.  https://doi.org/10.1084/jem.20100438 PubMedPubMedCentralCrossRefGoogle Scholar
  104. 104.
    Betis F, Brest P, Hofman V, Guignot J, Kansau I, Rossi B, Servin A, Hofman P (2003) Afa/Dr diffusely adhering Escherichia coli infection in T84 cell monolayers induces increased neutrophil transepithelial migration, which in turn promotes cytokine-dependent upregulation of decay-accelerating factor (CD55), the receptor for Afa/Dr adhesins. Infect Immun 71(4):1774–1783PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Thiery JP, Acloque H, Huang RY, Nieto MA (2009) Epithelial-mesenchymal transitions in development and disease. Cell 139(5):871–890.  https://doi.org/10.1016/j.cell.2009.11.007 PubMedCrossRefGoogle Scholar
  106. 106.
    Wu S, Rhee KJ, Albesiano E, Rabizadeh S, Wu X, Yen HR, Huso DL, Brancati FL, Wick E, McAllister F, Housseau F, Pardoll DM, Sears CL (2009) A human colonic commensal promotes colon tumorigenesis via activation of T helper type 17 T cell responses. Nat Med 15(9):1016–1022.  https://doi.org/10.1038/nm.2015 PubMedPubMedCentralCrossRefGoogle Scholar
  107. 107.
    Dejea CM, Wick EC, Hechenbleikner EM, White JR, Mark Welch JL, Rossetti BJ, Peterson SN, Snesrud EC, Borisy GG, Lazarev M, Stein E, Vadivelu J, Roslani AC, Malik AA, Wanyiri JW, Goh KL, Thevambiga I, Fu K, Wan F, Llosa N, Housseau F, Romans K, Wu X, McAllister FM, Wu S, Vogelstein B, Kinzler KW, Pardoll DM, Sears CL (2014) Microbiota organization is a distinct feature of proximal colorectal cancers. Proc Natl Acad Sci U S A 111(51):18321–18326.  https://doi.org/10.1073/pnas.1406199111 PubMedPubMedCentralCrossRefGoogle Scholar
  108. 108.
    Pitari GM, Zingman LV, Hodgson DM, Alekseev AE, Kazerounian S, Bienengraeber M, Hajnoczky G, Terzic A, Waldman SA (2003) Bacterial enterotoxins are associated with resistance to colon cancer. Proc Natl Acad Sci U S A 100(5):2695–2699.  https://doi.org/10.1073/pnas.0434905100 PubMedPubMedCentralCrossRefGoogle Scholar
  109. 109.
    Ghiso N, Rohan RM, Amano S, Garland R, Adamis AP (1999) Suppression of hypoxia-associated vascular endothelial growth factor gene expression by nitric oxide via cGMP. Invest Ophthalmol Vis Sci 40(6):1033–1039PubMedGoogle Scholar
  110. 110.
    Pellizzaro C, Coradini D, Daidone MG (2002) Modulation of angiogenesis-related proteins synthesis by sodium butyrate in colon cancer cell line HT29. Carcinogenesis 23(5):735–740.  https://doi.org/10.1093/carcin/23.5.735 PubMedCrossRefGoogle Scholar
  111. 111.
    Collard CDA, Agah A, Reenstra W, Buras J, Stahl GL (1999) Endothelial nuclear factor-κ B translocation and vascular cell adhesion molecule-1 induction by complement inhibition with anti-human C5 therapy or cGMP analogues. Arterioscler Thromb Vasc Biol 19(11):2623–2629.  https://doi.org/10.1161/01.ATV.19.11.2623 PubMedCrossRefGoogle Scholar
  112. 112.
    Saha S, Chowdhury P, Pal A, Chakrabarti MK (2008) Downregulation of human colon carcinoma cell (COLO-205) proliferation through PKG-MAP kinase mediated signaling cascade by E. coli heat stable enterotoxin (STa), a potent anti-angiogenic and anti-metastatic molecule. J Appl Toxicol 28(4):475–483.  https://doi.org/10.1002/jat.1297 PubMedCrossRefGoogle Scholar
  113. 113.
    Punj V, Bhattacharyya S, Saint-Dic D, Vasu C, Cunningham EA, Graves J, Yamada T, Constantinou AI, Christov K, White B, Li G, Majumdar D, Chakrabarty AM, Das Gupta TK (2004) Bacterial cupredoxin azurin as an inducer of apoptosis and regression in human breast cancer. Oncogene 23(13):2367–2378.  https://doi.org/10.1038/sj.onc.1207376 PubMedCrossRefGoogle Scholar
  114. 114.
    Yang DS, Miao XD, Ye ZM, Feng J, Xu RZ, Huang X, Ge FF (2005) Bacterial redox protein azurin induce apoptosis in human osteosarcoma U2OS cells. Pharmacol Res 52(5):413–421.  https://doi.org/10.1016/j.phrs.2005.06.002 PubMedCrossRefGoogle Scholar
  115. 115.
    Apiyo D, Wittung-Stafshede P (2005) Unique complex between bacterial azurin and tumor-suppressor protein p53. Biochem Biophys Res Commun 332(4):965–968.  https://doi.org/10.1016/j.bbrc.2005.05.038 PubMedCrossRefGoogle Scholar
  116. 116.
    De Grandis V, Bizzarri AR, Cannistraro S (2007) Docking study and free energy simulation of the complex between p53 DNA-binding domain and azurin. J Mol Recognit 20(4):215–226.  https://doi.org/10.1002/jmr.840 PubMedCrossRefGoogle Scholar
  117. 117.
    Taranta M, Bizzarri AR, Cannistraro S (2008) Probing the interaction between p53 and the bacterial protein azurin by single molecule force spectroscopy. J Mol Recognit 21(1):63–70.  https://doi.org/10.1002/jmr.869 PubMedCrossRefGoogle Scholar
  118. 118.
    Punj V, Das Gupta TK, Chakrabarty AM (2003) Bacterial cupredoxin azurin and its interactions with the tumor suppressor protein p53. Biochem Biophys Res Commun 312(1):109–114.  https://doi.org/10.1016/j.bbrc.2003.09.217 PubMedCrossRefGoogle Scholar
  119. 119.
    Mehta RR, Yamada T, Taylor BN, Christov K, King ML, Majumdar D, Lekmine F, Tiruppathi C, Shilkaitis A, Bratescu L, Green A, Beattie CW, Das Gupta TK (2011) A cell penetrating peptide derived from azurin inhibits angiogenesis and tumor growth by inhibiting phosphorylation of VEGFR-2, FAK and Akt. Angiogenesis 14(3):355–369.  https://doi.org/10.1007/s10456-011-9220-6 PubMedCrossRefGoogle Scholar
  120. 120.
    Rogers MS, Christensen KA, Birsner AE, Short SM, Wigelsworth DJ, Collier RJ, D’Amato RJ (2007) Mutant anthrax toxin B moiety (protective antigen) inhibits angiogenesis and tumor growth. Cancer Res 67(20):9980–9985.  https://doi.org/10.1158/0008-5472.CAN-07-0829 PubMedCrossRefGoogle Scholar
  121. 121.
    Alfano RW, Leppla SH, Liu S, Bugge TH, Duesbery NS, Frankel AE (2008) Potent inhibition of tumor angiogenesis by the matrix metalloproteinase-activated anthrax lethal toxin: implications for broad anti-tumor efficacy. Cell Cycle 7(6):745–749.  https://doi.org/10.4161/cc.7.6.5627 PubMedCrossRefGoogle Scholar
  122. 122.
    Cross MJ, Claesson-Welsh L (2001) FGF and VEGF function in angiogenesis: signalling pathways, biological responses and therapeutic inhibition. Trends Pharmacol Sci 22(4):201–207PubMedCrossRefGoogle Scholar
  123. 123.
    Sattler M, Reddy MM, Hasina R, Gangadhar T, Salgia R (2011) The role of the c-Met pathway in lung cancer and the potential for targeted therapy. Ther Adv Med Oncol 3(4):171–184.  https://doi.org/10.1177/1758834011408636 PubMedPubMedCentralCrossRefGoogle Scholar
  124. 124.
    Asiedu MK, Beauchamp-Perez FD, Ingle JN, Behrens MD, Radisky DC, Knutson KL (2014) AXL induces epithelial-to-mesenchymal transition and regulates the function of breast cancer stem cells. Oncogene 33(10):1316–1324.  https://doi.org/10.1038/onc.2013.57 PubMedCrossRefGoogle Scholar
  125. 125.
    Hollier BG, Tinnirello AA, Werden SJ, Evans KW, Taube JH, Sarkar TR, Sphyris N, Shariati M, Kumar SV, Battula VL, Herschkowitz JI, Guerra R, Chang JT, Miura N, Rosen JM, Mani SA (2013) FOXC2 expression links epithelial-mesenchymal transition and stem cell properties in breast cancer. Cancer Res 73(6):1981–1992.  https://doi.org/10.1158/0008-5472.CAN-12-2962 PubMedPubMedCentralCrossRefGoogle Scholar
  126. 126.
    Sarrio D, Rodriguez-Pinilla SM, Hardisson D, Cano A, Moreno-Bueno G, Palacios J (2008) Epithelial-mesenchymal transition in breast cancer relates to the basal-like phenotype. Cancer Res 68(4):989–997.  https://doi.org/10.1158/0008-5472.CAN-07-2017 PubMedCrossRefGoogle Scholar
  127. 127.
    Iliev ID, Funari VA, Taylor KD, Nguyen Q, Reyes CN, Strom SP, Brown J, Becker CA, Fleshner PR, Dubinsky M, Rotter JI, Wang HL, McGovern DP, Brown GD, Underhill DM (2012) Interactions between commensal fungi and the C-type lectin receptor Dectin-1 influence colitis. Science 336(6086):1314–1317.  https://doi.org/10.1126/science.1221789 PubMedPubMedCentralCrossRefGoogle Scholar
  128. 128.
    Blander JM, Longman RS, Iliev ID, Sonnenberg GF, Artis D (2017) Regulation of inflammation by microbiota interactions with the host. Nat Immunol 18(8):851–860.  https://doi.org/10.1038/ni.3780 PubMedCrossRefGoogle Scholar
  129. 129.
    Pousa ID, Gisbert JP, Mate J (2006) Vascular development in inflammatory bowel disease. Gastroenterol Hepatol 29(7):414–421PubMedCrossRefGoogle Scholar
  130. 130.
    Danese S, Scaldaferri F, Vetrano S, Stefanelli T, Graziani C, Repici A, Ricci R, Straface G, Sgambato A, Malesci A, Fiocchi C, Rutella S (2007) Critical role of the CD40 CD40-ligand pathway in regulating mucosal inflammation-driven angiogenesis in inflammatory bowel disease. Gut 56(9):1248–1256.  https://doi.org/10.1136/gut.2006.111989 PubMedPubMedCentralCrossRefGoogle Scholar
  131. 131.
    Griga T, Werner S, Koller M, Tromm A, May B (1999) Vascular endothelial growth factor (VEGF) in Crohn’s disease: increased production by peripheral blood mononuclear cells and decreased VEGF165 labeling of peripheral CD14 + monocytes. Dig Dis Sci 44(6):1196–1201PubMedCrossRefGoogle Scholar
  132. 132.
    Griga T, Voigt E, Gretzer B, Brasch F, May B (1999) Increased production of vascular endothelial growth factor by intestinal mucosa of patients with inflammatory bowel disease. Hepatogastroenterology 46(26):920–923PubMedGoogle Scholar
  133. 133.
    Griga T, Gutzeit A, Sommerkamp C, May B (1999) Increased production of vascular endothelial growth factor by peripheral blood mononuclear cells in patients with inflammatory bowel disease. Eur J Gastroenterol Hepatol 11(2):175–179PubMedCrossRefGoogle Scholar
  134. 134.
    Di Sabatino A, Ciccocioppo R, Armellini E, Morera R, Ricevuti L, Cazzola P, Fulle I, Corazza GR (2004) Serum bFGF and VEGF correlate respectively with bowel wall thickness and intramural blood flow in Crohn’s disease. Inflamm Bowel Dis 10(5):573–577PubMedCrossRefGoogle Scholar
  135. 135.
    Danese S (2010) Narrow-band imaging endoscopy to assess mucosal angiogenesis in inflammatory bowel disease: a pilot study. World J Gastroenterol 16(19):2396.  https://doi.org/10.3748/wjg.v16.i19.2396 PubMedPubMedCentralCrossRefGoogle Scholar
  136. 136.
    Haller D, Jobin C (2004) Interaction between resident luminal bacteria and the host: can a healthy relationship turn sour? J Pediatr Gastroenterol Nutr 38(2):123–136PubMedCrossRefGoogle Scholar
  137. 137.
    Kraehenbuhl JP, Corbett M (2004) Keeping the gut microflora at bay. Science 303(5664):1624–1625.  https://doi.org/10.1126/science.1096222 PubMedCrossRefGoogle Scholar
  138. 138.
    Sartor RB (2006) Mechanisms of disease: pathogenesis of Crohn’s disease and ulcerative colitis. Nat Clin Pract Gastroenterol Hepatol 3(7):390–407.  https://doi.org/10.1038/ncpgasthep0528 PubMedCrossRefGoogle Scholar
  139. 139.
    Xavier RJ, Podolsky DK (2007) Unravelling the pathogenesis of inflammatory bowel disease. Nature 448(7152):427–434.  https://doi.org/10.1038/nature06005 PubMedCrossRefGoogle Scholar
  140. 140.
    Davaatseren M, Hwang JT, Park JH, Kim MS, Wang S, Sung MJ (2013) Poly-gamma-glutamic acid attenuates angiogenesis and inflammation in experimental colitis. Mediat Inflamm 2013:982383.  https://doi.org/10.1155/2013/982383 CrossRefGoogle Scholar
  141. 141.
    Im E, Choi YJ, Kim CH, Fiocchi C, Pothoulakis C, Rhee SH (2009) The angiogenic effect of probiotic Bacillus polyfermenticus on human intestinal microvascular endothelial cells is mediated by IL-8. Am J Physiol Gastrointest Liver Physiol 297(5):G999–G1008PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2017

Authors and Affiliations

  • Sanaullah Sajib
    • 1
  • Fatema Tuz Zahra
    • 1
  • Michail S. Lionakis
    • 2
  • Nadezhda A. German
    • 3
  • Constantinos M. Mikelis
    • 1
  1. 1.Department of Biomedical Sciences, School of PharmacyTexas Tech University Health Sciences CenterAmarilloUSA
  2. 2.Laboratory of Clinical Immunology and Microbiology, Fungal Pathogenesis UnitNIAID, NIHBethesdaUSA
  3. 3.Department of Pharmaceutical Sciences, School of PharmacyTexas Tech University Health Sciences CenterAmarilloUSA

Personalised recommendations