Blocking of stromal cell-derived factor-1 reduces neoangiogenesis in human endometriosis lesions in a mouse model

American Journal of Reproductive Immunology

Volumn 70, Issue 5, 2013, Pages 386-397

  Virani, Sophia ^a   Edwards, Andrew K ^a   Thomas, Richard ^a   Childs, Timothy ^a   Tayade, Chandrakant ^a  

^a QUEEN S UNIVERSITY   (Canada)

Author keywords

Angiogenesis; Endometriosis; Endothelial progenitor cell; Stromal cell derived factor 1

Indexed keywords

BLOCKING ANTIBODY; CD34 ANTIGEN; STROMAL CELL DERIVED FACTOR 1; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW CELL; CAPILLARY DENSITY; CELL MIGRATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DISEASE COURSE; ENDOMETRIOSIS; ENDOMETRIUM; ENDOTHELIAL PROGENITOR CELL; ENGRAFTMENT; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOLOCALIZATION; IN VITRO STUDY; MICROVASCULATURE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SURVIVAL;

ANGIOGENESIS; ENDOMETRIOSIS; ENDOTHELIAL PROGENITOR CELL; STROMAL CELL-DERIVED FACTOR-1;

ANIMALS; ANTIBODIES, BLOCKING; ANTIGENS, CD34; CHEMOKINE CXCL12; DISEASE MODELS, ANIMAL; ENDOMETRIOSIS; ENDOMETRIUM; ENDOTHELIUM, VASCULAR; FEMALE; HUMANS; INTERLEUKIN RECEPTOR COMMON GAMMA SUBUNIT; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; MICROVESSELS; NEOVASCULARIZATION, PATHOLOGIC; TRANSPLANTATION, HETEROLOGOUS; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 84885477452     PISSN: 10467408     EISSN: 16000897     Source Type: Journal    
DOI: 10.1111/aji.12134     Document Type: Article

References (47)

1. Ajossa S, Mais V, Guerriero S, Paoletti AM, Caffiero A, Murgia C, Melis GB: The prevalence of endometriosis in premenopausal women undergoing gynecological surgery. Clin Exp Obstet Gynecol 1994; 21:195-197.
2. Carter JE: Combined hysteroscopic and laparoscopic findings in patients with chronic pelvic pain. J Am Assoc Gynecol Laparosc 1994; 2:43-47.
3. Giudice LC: Clinical practice. Endometriosis. N Engl J Med 2010; 362:2389-2398.
4. Olive DL, Schwartz LB: Endometriosis. N Engl J Med 1993; 328:1759-1769.
5. Wheeler JM: Epidemiology of endometriosis-associated infertility. J Reprod Med 1989; 34:41-46.
6. Levy AR, Osenenko KM, Lozano-Ortega G, Sambrook R, Jeddi M, Belisle S, Reid RL: Economic burden of surgically confirmed endometriosis in canada. J Obstet Gynaecol Can 2011; 33:830-837.
7. Alcazar JL, Garcia-Manero M: Ovarian endometrioma vascularization in women with pelvic pain. Fertil Steril 2007; 87:1271-1276.
8. Ceyhan ST, Onguru O, Baser I, Gunhan O: Expression of cyclooxygenase-2 and vascular endothelial growth factor in ovarian endometriotic cysts and their relationship with angiogenesis. Fertil Steril 2008; 90:988-993.
9. Cho SH, Oh YJ, Nam A, Kim HY, Park JH, Kim JH, Park KH, Cho DJ, Lee BS: Evaluation of serum and urinary angiogenic factors in patients with endometriosis. Am J Reprod Immunol 2007; 58:497-504.
10. Hur SE, Lee JY, Moon HS, Chung HW: Angiopoietin-1, angiopoietin-2 and tie-2 expression in eutopic endometrium in advanced endometriosis. Mol Hum Reprod 2006; 12:421-426.
11. Rogers PA, D'Hooghe TM, Fazleabas A, Gargett CE, Giudice LC, Montgomery GW, Rombauts L, Salamonsen LA, Zondervan KT: Priorities for endometriosis research: recommendations from an international consensus workshop. Reprod Sci 2009; 16:335-346.
12. Asahara T, Kawamoto A, Masuda H: Concise review: circulating endothelial progenitor cells for vascular medicine. Stem Cells 2011; 29:1650-1655.
13. Ergun S, Hohn HP, Kilic N, Singer BB, Tilki D: Endothelial and hematopoietic progenitor cells (EPCs and HPCs): hand in hand fate determining partners for cancer cells. Stem Cell Rev 2008; 4:169-177.
14. Gao D, Nolan DJ, Mellick AS, Bambino K, McDonnell K, Mittal V: Endothelial progenitor cells control the angiogenic switch in mouse lung metastasis. Science 2008; 319:195-198.
15. Okamoto R, Ueno M, Yamada Y, Takahashi N, Sano H, Suda T, Takakura N: Hematopoietic cells regulate the angiogenic switch during tumorigenesis. Blood 2005; 105:2757-2763.
16. Kopp HG, Ramos CA, Rafii S: Contribution of endothelial progenitors and proangiogenic hematopoietic cells to vascularization of tumor and ischemic tissue. Curr Opin Hematol 2006; 13:175-181.
17. Becker CM, Beaudry P, Funakoshi T, Benny O, Zaslavsky A, Zurakowski D, Folkman J, D'Amato RJ, Ryeom S: Circulating endothelial progenitor cells are up-regulated in a mouse model of endometriosis. Am J Pathol 2011; 178:1782-1791.
18. Laschke MW, Giebels C, Nickels RM, Scheuer C, Menger MD: Endothelial progenitor cells contribute to the vascularization of endometriotic lesions. Am J Pathol 2011; 178:442-450.
19. Laschke MW, Giebels C, Menger MD: Vasculogenesis: a new piece of the endometriosis puzzle. Hum Reprod Update 2011; 17:628-636.
20. Butler JM, Guthrie SM, Koc M, Afzal A, Caballero S, Brooks HL, Mames RN, Segal MS, Grant MB, Scott EW: SDF-1 is both necessary and sufficient to promote proliferative retinopathy. J Clin Invest 2005; 115:86-93.
21. Jin DK, Shido K, Kopp HG, Petit I, Shmelkov SV, Young LM, Hooper AT, Amano H, Avecilla ST, Heissig B, Hattori K, Zhang F, Hicklin DJ, Wu Y, Zhu Z, Dunn A, Salari H, Werb Z, Hackett NR, Crystal RG, Lyden D, Rafii S: Cytokine-mediated deployment of SDF-1 induces revascularization through recruitment of CXCR4+ hemangiocytes. Nat Med 2006; 12:557-567.
22. Jujo K, Hamada H, Iwakura A, Thorne T, Sekiguchi H, Clarke T, Ito A, Misener S, Tanaka T, Klyachko E, Kobayashi K, Tongers J, Roncalli J, Tsurumi Y, Hagiwara N, Losordo DW: CXCR4 blockade augments bone marrow progenitor cell recruitment to the neovasculature and reduces mortality after myocardial infarction. Proc Natl Acad Sci USA 2010; 107:11008-11013.
23. Kollet O, Shivtiel S, Chen YQ, Suriawinata J, Thung SN, Dabeva MD, Kahn J, Spiegel A, Dar A, Samira S, Goichberg P, Kalinkovich A, Arenzana-Seisdedos F, Nagler A, Hardan I, Revel M, Shafritz DA, Lapidot T: HGF, SDF-1, and MMP-9 are involved in stress-induced human CD34+ stem cell recruitment to the liver. J Clin Invest 2003; 112:160-169.
24. Yu JX, Huang XF, Lv WM, Ye CS, Peng XZ, Zhang H, Xiao LB, Wang SM: Combination of stromal-derived factor-1alpha and vascular endothelial growth factor gene-modified endothelial progenitor cells is more effective for ischemic neovascularization. J Vasc Surg 2009; 50:608-616.
25. Hernandez-Lopez C, Varas A, Sacedon R, Jimenez E, Munoz JJ, Zapata AG, Vicente A: Stromal cell-derived factor 1/CXCR4 signaling is critical for early human T-cell development. Blood 2002; 99:546-554.
26. Lee SP, Youn SW, Cho HJ, Li L, Kim TY, Yook HS, Chung JW, Hur J, Yoon CH, Park KW, Oh BH, Park YB, Kim HS: Integrin-linked kinase, a hypoxia-responsive molecule, controls postnatal vasculogenesis by recruitment of endothelial progenitor cells to ischemic tissue. Circulation 2006; 114:150-159.
27. Rosenkranz K, Kumbruch S, Lebermann K, Marschner K, Jensen A, Dermietzel R, Meier C: The chemokine SDF-1/CXCL12 contributes to the 'homing' of umbilical cord blood cells to a hypoxic-ischemic lesion in the rat brain. J Neurosci Res 2010; 88:1223-1233.
28. Stebler J, Spieler D, Slanchev K, Molyneaux KA, Richter U, Cojocaru V, Tarabykin V, Wylie C, Kessel M, Raz E: Primordial germ cell migration in the chick and mouse embryo: the role of the chemokine SDF-1/CXCL12. Dev Biol 2004; 272:351-361.
29. Tachibana K, Hirota S, Iizasa H, Yoshida H, Kawabata K, Kataoka Y, Kitamura Y, Matsushima K, Yoshida N, Nishikawa S, Kishimoto T, Nagasawa T: The chemokine receptor CXCR4 is essential for vascularization of the gastrointestinal tract. Nature 1998; 393:591-594.
30. Beider K, Abraham M, Begin M, Wald H, Weiss ID, Wald O, Pikarsky E, Abramovitch R, Zeira E, Galun E, Nagler A, Peled A: Interaction between CXCR4 and CCL20 pathways regulates tumor growth. PLoS ONE 2009; 4:e5125.
31. Jinquan T, Quan S, Jacobi HH, Madsen HO, Glue C, Skov PS, Malling HJ, Poulsen LK: CXC chemokine receptor 4 expression and stromal cell-derived factor-1alpha-induced chemotaxis in CD4+ T lymphocytes are regulated by interleukin-4 and interleukin-10. Immunology 2000; 99:402-410.
32. Raz E, Mahabaleshwar H: Chemokine signaling in embryonic cell migration: a fisheye view. Development 2009; 136:1223-1229.
33. Wang A, Fairhurst AM, Tus K, Subramanian S, Liu Y, Lin F, Igarashi P, Zhou XJ, Batteux F, Wong D, Wakeland EK, Mohan C: CXCR4/CXCL12 hyperexpression plays a pivotal role in the pathogenesis of lupus. J Immunol 2009; 182:4448-4458.
34. Wang J, Shiozawa Y, Wang Y, Jung Y, Pienta KJ, Mehra R, Loberg R, Taichman RS: The role of CXCR7/RDC1 as a chemokine receptor for CXCL12/SDF-1 in prostate cancer. J Biol Chem 2008; 283:4283-4294.
35. Balabanian K, Lagane B, Infantino S, Chow KY, Harriague J, Moepps B, Arenzana-Seisdedos F, Thelen M, Bachelerie F: The chemokine SDF-1/CXCL12 binds to and signals through the orphan receptor RDC1 in T lymphocytes. J Biol Chem 2005; 280:35760-35766.
36. Ceradini DJ, Kulkarni AR, Callaghan MJ, Tepper OM, Bastidas N, Kleinman ME, Capla JM, Galiano RD, Levine JP, Gurtner GC: Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat Med 2004; 10:858-864.
37. Lebovic DI, Mueller MD, Taylor RN: Immunobiology of endometriosis. Fertil Steril 2001; 75:1-10.
38. Aiuti A, Webb IJ, Bleul C, Springer T, Gutierrez-Ramos JC: The chemokine SDF-1 is a chemoattractant for human CD34+ hematopoietic progenitor cells and provides a new mechanism to explain the mobilization of CD34+ progenitors to peripheral blood. J Exp Med 1997; 185:111-120.
39. Dar A, Goichberg P, Shinder V, Kalinkovich A, Kollet O, Netzer N, Margalit R, Zsak M, Nagler A, Hardan I, Resnick I, Rot A, Lapidot T: Chemokine receptor CXCR4-dependent internalization and resecretion of functional chemokine SDF-1 by bone marrow endothelial and stromal cells. Nat Immunol 2005; 6:1038-1046.
40. Furuya M, Suyama T, Usui H, Kasuya Y, Nishiyama M, Tanaka N, Ishiwata I, Nagai Y, Shozu M, Kimura S: Up-regulation of CXC chemokines and their receptors: implications for proinflammatory microenvironments of ovarian carcinomas and endometriosis. Hum Pathol 2007; 38:1676-1687.
41. Glace L, Grygielko ET, Boyle R, Wang Q, Laping NJ, Sulpizio AC, Bray JD: Estrogen-induced stromal cell-derived factor-1 (SDF-1/Cxcl12) expression is repressed by progesterone and by selective estrogen receptor modulators via estrogen receptor alpha in rat uterine cells and tissues. Steroids 2009; 74:1015-1024.
42. Urbich C, Dimmeler S: Endothelial progenitor cells functional characterization. Trends Cardiovasc Med 2004; 14:318-322.
43. Voermans C, Anthony EC, Mul E, van der Schoot E, Hordijk P: SDF-1-induced actin polymerization and migration in human hematopoietic progenitor cells. Exp Hematol 2001; 29:1456-1464.
44. van Buul JD, Voermans C, van Gelderen J, Anthony EC, van der Schoot CE, Hordijk PL: Leukocyte-endothelium interaction promotes SDF-1-dependent polarization of CXCR4. J Biol Chem 2003; 278:30302-30310.
45. Nagasawa T, Hirota S, Tachibana K, Takakura N, Nishikawa S, Kitamura Y, Yoshida N, Kikutani H, Kishimoto T: Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF/SDF-1. Nature 1996; 382:635-638.
46. Donzella GA, Schols D, Lin SW, Este JA, Nagashima KA, Maddon PJ, Allaway GP, Sakmar TP, Henson G, De Clercq E, Moore JP: AMD3100, a small molecule inhibitor of HIV-1 entry via the CXCR4 co-receptor. Nat Med 1998; 4:72-77.
47. Gazvani R, Templeton A: Peritoneal environment, cytokines and angiogenesis in the pathophysiology of endometriosis. Reproduction 2002; 123:217-226.