Vascular endothelial growth factor receptor 1 signaling facilitates gastric ulcer healing and angiogenesis through the upregulation of epidermal growth factor expression on VEGFR1+CXCR4+ cells recruited from bone marrow

Journal of Gastroenterology

Volumn 49, Issue 3, 2014, Pages 455-469

  Sato, Takehito ^a   Amano, Hideki ^a   Ito, Yoshiya ^a   Eshima, Koji ^a   Minamino, Tsutomu ^a   Ae, Takako ^a   Katada, Chikatoshi ^a   Ohno, Takashi ^b   Hosono, Kanako ^a   Suzuki, Tatsunori ^a   Shibuya, Masabumi ^c   Koizumi, Wasaburo ^a   Majima, Masataka ^a  

^a KITASATO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b Isehara Kyodo Hospital   (Japan)

^c JOBU UNIVERSITY   (Japan)

Author keywords

Bone marrow; CXCR4; EGF; Gastric ulcer; VEGFR1

Indexed keywords

CD31 ANTIGEN; CHEMOKINE RECEPTOR CXCR4; CHEMOKINE RECEPTOR CXCR4 ANTAGONIST; EPIDERMAL GROWTH FACTOR; MESSENGER RNA; PROTEIN TYROSINE KINASE; VASCULOTROPIN; VASCULOTROPIN ANTIBODY; VASCULOTROPIN RECEPTOR 1; CXCR4 PROTEIN, MOUSE;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATTENUATION; BONE MARROW; BONE MARROW CELL; BONE MARROW TRANSPLANTATION; CELL ISOLATION; CHIMERA; CONTROLLED STUDY; GRANULATION TISSUE; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RECEPTOR DOWN REGULATION; RECEPTOR UPREGULATION; SEROSA; SIGNAL TRANSDUCTION; STOMACH MUCOSA; STOMACH ULCER; TISSUE REGENERATION; ULCER HEALING; WILD TYPE; ANIMAL; C57BL MOUSE; DISEASE MODEL; GENETICS; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PHYSIOLOGY; PROCEDURES; UPREGULATION;

ANIMALS; BONE MARROW CELLS; BONE MARROW TRANSPLANTATION; DISEASE MODELS, ANIMAL; EPIDERMAL GROWTH FACTOR; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEOVASCULARIZATION, PHYSIOLOGIC; RECEPTORS, CXCR4; SIGNAL TRANSDUCTION; STOMACH ULCER; UP-REGULATION; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1;

EID: 84897110974     PISSN: 09441174     EISSN: 14355922     Source Type: Journal    
DOI: 10.1007/s00535-013-0869-z     Document Type: Article

References (43)

1. Tarnawski AS. Cellular and molecular mechanisms of gastrointestinal ulcer healing. Dig Dis Sci. 2005;50(Suppl 1):S24-33. (Pubitemid 41380795)
2. Folkmann J, Szabo S, Stovroff M, McNeil P, Li W, Shing Y. Duodenal ulcer. Discovery of new mechanism and development of angiogenic therapy that accelerates healing. Ann Surg. 1991;214:414-27.
3. Takahashi M, Kawabe T, Ogura K, Maeda S, Mikami Y, Kaneko N, et al. Expression of vascular endothelial growth factor at the human gastric ulcer margin and in cultured gastric fibroblasts: a new angiogenic factor for gastric ulcer healing. Biochem Biophys Res Commun. 1997;234:493-8. (Pubitemid 27243932)
4. Wallace JL, Dicay M, McKnight W, Dudar GK. Platelets accelerate gastric ulcer healing through presentation of vascular endothelial growth factor. Br J Pharmacol. 2006;148:274-8. (Pubitemid 43801174)
5. Boku K, Ohno T, Saeki T, Hayashi H, Hayashi I, Katori M, et al. Adaptive cytoprotection mediated by prostaglandin I(2) is attributable to sensitization of CRGP-containing sensory nerves. Gastroenterology. 2001;120:134-43. (Pubitemid 32061877)
6. Ohno T, Hattori Y, Komine R, Ae T, Mizuguchi S, Arai K, et al. Roles of calcitonin gene-related peptide in maintenance of gastric mucosal integrity and in enhancement of ulcer healing and angiogenesis. Gastroenterology. 2008;134:215-25. (Pubitemid 350309312)
7. Ae T, Ohno T, Hattori Y, Suzuki T, Hosono K, Minamino T, et al. Role of microsomal prostaglandin E synthase-1 in the facilitation of angiogenesis and the healing of gastric ulcers. Am J Physiol Gastrointest Liver Physiol. 2010;299:G1139-46.
8. Ferrara N. Vascular endothelial growth factor: basic science and clinical progress. Endocr Rev. 2004;25:581-611. (Pubitemid 39099316)
9. Shibuya M. Vascular endothelial growth factor receptor-2 (VEGFR-1/Flt-1): dual regulator for angiogenesis. Angiogenesis. 2006;9:225-30.
10. Szabo S, Vincze A, Sandor Z, Jadus M, Gombos Z, Pedram A, et al. Vascular approach to gastroduodenal ulceration: new studies with endothelins and VEGF. Dig Dis Sci. 1998; 43(Suppl):S40-5.
11. Takahashi M, Maeda S, Ogura K, Terano A, Omata M. The possible role of vascular endothelial growth factor (VEGF) in gastric ulcer healing: effect of sofalcone on VEGF release in vitro. J Clin Gastroenterol. 1998;27:S178-82. (Pubitemid 29028894)
12. Suzuki N, Takahashi S, Okabe S. Relationship between vascular endothelial growth factor and angiogenesis in spontaneous and indomethacin delayed healing of acetic acid-induced gastric ulcers in rats. J Physiol Pharmacol. 1998;49:515-27. (Pubitemid 29024370)
13. Jones MK, Kawanaka H, Baatar D, Szabo IL, Tsugawa Pai R, Koh GY, Kim I, Sarfeh J, Tarnawski AS. Gene therapy for gastric ulcers with single local injection of naked DNA encoding VEGF and angiopoietin-1. Gastroenterology. 2001;121:1040-7. (Pubitemid 33022082)
14. Hiratsuka S, Minowa O, Kuno J, Noda T, Shibuya M. Flt-1 lacking the tyrosine kinase domain is sufficient for normal development and angiogenesis in mice. Proc Natl Acad Sci USA. 1998;95:9349-54. (Pubitemid 28506234)
15. Hiratsuka S, Nakamura K, Iwai S, Murakami M, Itoh T, Kijima H, et al. MMP9 induction by vascular endothelial growth factor receptor-1 is involved in lung-specific metastasis. Cancer Cell. 2002;2:289-300. (Pubitemid 41043963)
16. Kaplan RN, Riba RD, Zacharoulis S, Bramley AH, Vincent L, Costa C, et al. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature. 2005;438:820-7. (Pubitemid 41753060)
17. Kato T, Ito Y, Hosono K, Suzuki T, Tamaki H, Minamino T, Kato S, et al. Vascular endothelial growth factor receptor-1 signaling promotes liver repair through restoration of liver microvasculature after acetaminophen hepatotoxicity. Toxicol Sci. 2011;120:218-29.
18. Murakami M, Zheng Y, Hirashima M, Suda T, Morita Y, Ooehara J, et al. VEGFR1 tyrosine kinase signaling promotes lymphangiogenesis as well as angiogenesis indirectly via macrophage recruitment. Arterioscler Thromb Vasc Biol. 2008;28:658-64. (Pubitemid 351651323)
19. Akimoto M, Hashimoto H, Maeda A, Shigemoto M, Yamashita K. Roles of angiogenic factors and endothelin-1 in gastric ulcer healing. Clin Sci (Lond). 2002;103(Suppl 48):450S-4S. (Pubitemid 35007209)
20. Komori M, Tsuji S, Tsujii M, Murata H, Iijima H, Yasumaru M, et al. Efficiency of bone marrow-derived cells in regeneration of the stomach after induction of ethanol-induced ulcers in rats. J Gastroenterol. 2005;40:591-9. (Pubitemid 41038788)
21. Nishida T, Tsuji S, Tsujii M, Ishii S, Yoshio T, Shinzaki S, et al. Cultured bone marrow cell local implantation accelerates healing of ulcers in mice. J Gastroenterol. 2008;43:124-35. (Pubitemid 351344554)
22. Kamoshita E, Ikeda Y, Fujita M, Amano H, Oikawa A, Suzuki T, et al. Recruitment of a prostaglandin E receptor subtype, EP3-expressing bone marrow cells is crucial in wound-induced angiogenesis. Am J Pathol. 2006;169:1458-72. (Pubitemid 351194377)
23. Ogawa Y, Suzuki T, Oikawa A, Hosono K, Kubo H, Amano H, et al. Bone marrow-derived EP3-expressing stromal cells enhance tumor-associated angiogenesis and tumor growth. Biochem Biophys Res Commun. 2009;382:720-5.
24. Katoh H, Hosono K, Ito Y, Suzuki T, Ogawa Y, Kubo H, et al. COX-2 and prostaglandin EP3/EP4 signaling regulate the tumor stromal proangiogenic microenvironment via CXCL12-CXCR4 chemokine systems. Am J Pathol. 2010;176:1469-83.
25. Jin DK, Shido K, Kopp HG, Petit I, Shmelkov SV, Young LM, et al. Cytokine-mediated deployment of SDF-1 induces revascularization through recruitment of CXCR4+ hemangiocytes. Nat Med. 2006;12:557-67.
26. Hattori K, Heissig B, Wu Y, Dias S, Tejada R, Ferris B, et al. Placental growth factor reconstitutes hematopoiesis by recruiting VEGFR1(+) stem cells from bone-marrow microenvironment. Nat Med. 2002;8:841-9.
27. Hosono K, Suzuki T, Tamaki H, Sakagami H, Hayashi I, Narumiya S, Alitalo K, Majima M. Roles of prostaglandin E2-EP3/ EP4 receptor signaling in the enhancement of lymphangiogenesis during fibroblast growth factor-2-induced granulation formation. Arterioscler Thromb Vasc Biol. 2011;31:1049-58.
28. Matsui Y, Amano H, Ito Y, Eshima K, Suzuki T, Ogawa F, Iyoda A, et al. Thromboxane A2 receptor signaling facilitates tumor colonization through P-selectin-mediated interaction of tumor cells with platelets and endothelial cells. Cancer Sci. 2012;103:700-7.
29. Eshima K, Suzuki H, Shinohara N. Cross positive selection of thymocytes expressing a single TCR by multiple major histocompatibility complex molecules of both classes: implication for CD4+ versus CD8+ lineage commitment. J Immunol. 2006;176:1628-36. (Pubitemid 43134307)
30. Okamoto R, Yajima T, Yamazaki M, Kanai T, Mukai M, Okamoto S, et al. Damaged epithelia regenerated by bone marrow-derived cells in human gastrointestinal tract. Nat Med. 2002;8:1011-7. (Pubitemid 35033706)
31. + cells to the ulcer granulation tissues. Biomed Pharmacother. 2013. doi:10.1016/j.biopha.2013.01.009.
32. 2-EP3 signaling regulates tumor-associated angiogenesis and tumor growth. J Exp Med. 2003;197:221-32.
33. Majima M, Amano H, Hayashi I. Prostanoid receptor signaling relevant to tumor growth and angiogenesis. Trends Pharmacol Sci. 2003;24:524-9. (Pubitemid 37244005)
34. Hattori K, Dias S, Heissig B, Hackett NR, Lyden D, Tateno M, et al. Vascular endothelial growth factor and angiopoietin-1 stimulate postnatal hematopoiesis by recruitment of vasculogenic and hematopoietic stem cells. J Exp Med. 2001;193:1005-14. (Pubitemid 32436194)
35. Akimoto M, Hashimoto H, Shigemoto M, Maeda A, Yamashita K. Effects of antisecretory agents on angiogenesis during healing of gastric ulcers. J Gastroenterol. 2005;40:685-9. (Pubitemid 41349079)
36. Heissig B, Hattori K, Dias S, Friedrich M, Ferris B, Hackett NR, et al. Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand. Cell. 2002;109:625-37. (Pubitemid 34628725)
37. Moore MA, Hattori K, Heissig B, Shieh JH, Dias S, Crystal RG, Rafii S. Mobilization of endothelial and hematopoietic stem and progenitor cells by adenovector-mediated elevation of serum levels of SDF-1, VEGF, and angiopoietin-1. Ann N Y Acad Sci. 2001;938:36-45.
38. Barnard JA, Beauchamp RD, Russell WE, Dubois RN, Coffey RJ. Epidermal growth factor-related peptides and their relevance to gastrointestinal pathophysiology. Gastroenterology. 1995; 108:564-80.
39. Scott J, Urdea MS, Quiroga M, Sanchez-Pescador R, Fong NM, Selby M, et al. Structure of a mouse submaxillary messenger RNA encoding epidermal growth factor and seven related proteins. Science. 1983;221:236-40. (Pubitemid 13062611)
40. Hase S, Nakazawa S, Tsukamoto Y, Segawa K. Effects of prednisolone and human epidermal growth factor on angiogenesis in granulation tissue of gastric ulcer induced by acetic acid. Digestion. 1989;42:135-42. (Pubitemid 19190100)
41. Pai R, Ohta M, Itani RM, Sarfeh IJ, Tarnawski AS. Induction of mitogen activated protein kinase signal transduction pathway during gastric ulcer healing in rat model. Gastroenterology. 1998;114:706-13. (Pubitemid 28160405)
42. Wragg A, Mellad JA, Beltran LE, Konoplynnikov M, San H, Boozer S, et al. VEGFR1/CXCR4-positive progenitor cell modulate local inflammation and augment tissue perfusion by a SDF-1-dependent mechanism. J Mole Med. 2008;86:1221-32.
43. Wang F, Yamauchi M, Muramatsu M, Osawa T, Tsuchida R, Shibuya M. RACK1 regulates VEGF/Flt1-mediated cell migration voa activation of a PI3K/Akt pathway. J Biol Chem. 2001;286:9097-106.