OPN binds alpha V integrin to promote endothelial progenitor cell incorporation into vasculature

in Reproduction
Authors:
Theodore T Wing Department of Veterinary Integrative Biosciences, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, Texas, USA

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David W Erikson Department of Veterinary Integrative Biosciences, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, Texas, USA

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Robert C Burghardt Department of Veterinary Integrative Biosciences, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, Texas, USA

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Fuller W Bazer Department of Animal Science, Texas A&M University, College Station, Texas, USA

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Kayla J Bayless Department of Molecular and Cellular Medicine, Texas A&M Health Science Center, College Station, Texas, USA

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Greg A Johnson Department of Veterinary Integrative Biosciences, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, Texas, USA

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Correspondence should be addressed to K J Bayless or G A Johnson; Email: kbayless@medicine.tamhsc.edu or gjohnson@cvm.tamu.edu
DOI:
https://doi.org/10.1530/REP-19-0358
Volume/Issue:
Volume 159: Issue 4
Page Range:
465–478
Article Type:
Research Article
Online Publication Date:
Apr 2020
Copyright:
© 2020 Society for Reproduction and Fertility 2020
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Angiogenesis is fundamental to the expansion of the placental vasculature during pregnancy. Integrins are associated with vascular formation; and osteopontin is a candidate ligand for integrins to promote angiogenesis. Endothelial progenitor cells (EPCs) are released from bone marrow into the blood and incorporate into newly vascularized tissue where they differentiate into mature endothelium. Results of studies in women suggest that EPCs may play an important role in maintaining placental vascular integrity during pregnancy, although little is known about how EPCs are recruited to these tissues. Our goal was to determine the αv integrin mediated effects of osteopontin on EPC adhesion and incorporation into angiogenic vascular networks. EPCs were isolated from 6 h old piglets. RT-PCR revealed that EPCs initially had a monocyte-like phenotype in culture that became more endothelial-like with cell passage. Immunofluorescence microscopy confirmed that the EPCs express platelet endothelial cell adhesion molecule, vascular endothelial cadherin, and von Willebrand factor. When EPCs were cultured on OPN-coated slides, the αv integrin subunit was observed in focal adhesions at the basal surface of EPCs. Silencing of αv integrin reduced EPC binding to OPN and focal adhesion assembly. In vitro siRNA knockdown in EPCs,demonstrated that OPN stimulates EPC incorporation into human umbilical vein endothelial cell (HUVEC) networks via αv-containing integrins. Finally, in situ hybridization and immunohistochemistry localized osteopontin near placental blood vessels. In summary, OPN binds the αv integrin subunit on EPCs to support EPC adhesion and increase EPC incorporation into angiogenic vascular networks.

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Print ISSN:
1470-1626
Online ISSN:
1741-7899

  • Apparao KB, Illera MJ, Beyler SA, Olson GE, Osteen KG, Corjay MH, Boggess K & Lessey BA 2003 Regulated expression of osteopontin in the peri-implantation rabbit uterus. Biology of Reproduction 68 1484–1490. (https://doi.org/10.1095/biolreprod.101.001347)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Apte UM, Banerjee A, McRee R, Wellberg E & Ramaiah SK 2005 Role of osteopontin in hepatic neutrophil infiltration During alcoholic steatohepatitis. Toxicology and Applied Pharmacology 207 25–38. (https://doi.org/10.1016/j.taap.2004.12.018)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Asahara T, Murohara T, Sullivan A, Silver M, Van DerZee R, Li T, Witxenbichler B, Schatteman G & Isner JM 1997 Isolation of putative progenitor endothelial cells for angiogenesis. Science 275 964–967. (https://doi.org/10.1126/science.275.5302.964)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Asahara T, Masuda H, Takahashi T, Kalka C, Pastore C, Silver M, Kearne M, Magner M & Isner JM 1999 Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circulation Research 85 221–228. (https://doi.org/10.1161/01.res.85.3.221)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Barker DJ 2004 Developmental origins of adult health and disease. Journal of Epidemiology and Community Health 58 114–115. (https://doi.org/10.1136/jech.58.2.114)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Bayless KJ, Davis GE & Meininger GA 1997 Isolation and biological properties of osteopontin from bovine milk. Protein Expression and Purification 9 309–314. (https://doi.org/10.1006/prep.1996.0699)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Bayless KJ, Meininger GA, Scholtz JM & Davis GE 1998 Osteopontin is a Ligand for the α4β1 integrin. Journal of Cell Science 111 1165–1174.

  • Bayless KJ, Kwak HI & Su SC 2009 Investigating endothelial invasion and sprouting behavior in three-dimensional collagen matrices. Nature Protocols 4 1888–1898. (https://doi.org/10.1038/nprot.2009.221)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Bayless KJ, Salazar R & Davis GE 2000 RGD-Dependent Vacuolation and Lumen Formation Observed during Endothelial Cell Morphogenesis in three-Dimensional fibrin Matrices Involves the αvβ3 and α5β1 integrins. The American Journal of Pathology 156 1673–1683. (https://doi.org/10.1016/S0002-9440(10)65038-9)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Brunt KR, Hall SR, Ward CA & Melo LG 2007 Endothelial progenitor cell and mesenchymal stem cell isolation, characterization, viral transduction. Methods in Molecular Medicine 139 197–210. (https://doi.org/10.1007/978-1-59745-571-8_12)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Buemi M, Allegra A, D’anna R, Coppolino G, Crasci E, Giordano D, Loddo S, Cucinotta M, Musclino C & Teti D 2007 Concentration of circulating endothelial progenitor cells (EPC) in normal pregnancy and in pregnant women with diabetes and hypertension. American Journal of Obstetrics and Gynecology 196 68.e1–68.e6. (https://doi.org/10.1016/j.ajog.2006.08.032)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Burdo TH, Wood MR & Fox HS 2007 Osteopontin prevents monocyte recirculation and apoptosis. Journal of Leukocyte Biology 81 1504–1511. (https://doi.org/10.1189/jlb.1106711)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Caiado F & Dias S 2012 Endothelial progenitor cells and integrins: adhesive needs. Fibrogenesis and Tissue Repair 5 4. (https://doi.org/10.1186/1755-1536-5-4)

  • Cook AC, Tuck AB, McCarthy S, Turner JG, Irby RB, Bloom GC, Yeatman TJ & Chambers AF 2005 Osteopontin induces multiple changes in gene expression that reflect the six "hallmarks of cancer" in a model of breast cancer progression. Molecular Carcinogenesis 43 225–236. (https://doi.org/10.1002/mc.20105)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Crosby JR, Kaminski WE, Schatteman G, Martin PJ, Raines EW, Seifert RA & Bowen-Pope DF 2000 Endothelial cells of hematopoietic origin make a significant contribution to adult blood vessel formation. Circulation Research 87 728–730. (https://doi.org/10.1161/01.res.87.9.728)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Davis GE & Bayless KJ 2003 An integrin and rho GTPase-dependent pinocytic vacuole mechanism controls capillary lumen formation in collagen and fibrin matrices. Microcirculation 10 27–44. (https://doi.org/10.1038/sj.mn.7800175)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Davis GE & Camarillo CW 1993 Regulation of integrin-mediated myeloid cell adhesion to fibronectin: influence of disulfide reducing agents, divalent cations and phorbol ester. Journal of Immunology 151 7138–7150.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Denhardt DT & Guo X 1993 Osteopontin: a protein with diverse functions. FASEB Journal 7 1475–1482. (https://doi.org/10.1096/fasebj.7.15.8262332)

  • Dufour S, Mège RM & Thiery JP 2013 α-catenin, vinculin, and F-actin in Strengthening E-cadherin Cell-cell Adhesions and Mechanosensing. Cell Adhesion and Migration 7 345–350. (https://doi.org/10.4161/cam.25139)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Dumbauld DW, Lee TT, Singh A, Scrimgeour J, Gersbach CA, Zamir EA, Fu J, Chen CS, Curtis JE & Craig SW et al. 2013 How vinculin regulates force transmission. PNAS 110 9788–9793. (https://doi.org/10.1073/pnas.1216209110)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Dunlap KA, Kwak HI, Burghardt RC, Bazer FW, Magness RR, Johnson GA & Bayless KJ 2010 The sphingosine 1-phosphate (S1P) signaling pathway is regulated during pregnancy in sheep. Biology of Reproduction 82 876–887. (https://doi.org/10.1095/biolreprod.109.081604)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Duvall CL, Weiss D, Robinson ST, Alameddine FMF, Guldberg RE & Taylor WR 2008 The role of osteopontin in recovery from hind limb ischemia. Arteriosclerosis, Thrombosis, and Vascular Biology 28 290–295. (https://doi.org/10.1161/ATVBAHA.107.158485)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Enders AC & Blankenship TN 1999 Comparative placental structure. Advanced Drug Delivery Reviews 38 3–15. (https://doi.org/10.1016/s0169-409x(99)00003-4)

  • Enders AC & Carter AM 2004 What can comparative studies of placental structure tell us? A review. Placenta 25 (Supplement A) S3–S9. (https://doi.org/10.1016/j.placenta.2004.01.011)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Erikson DW, Burghardt RC, Bayless KJ & Johnson GA 2009 Secreted phosphoprotein 1 (SPP1, osteopontin) binds to integrin alphavbeta6 on porcine trophectoderm cells and integrin alphavbeta3 on uterine luminal epithelial cells, and promotes trophectoderm cell adhesion and migration. Biology of Reproduction 81 814–825. (https://doi.org/10.1095/biolreprod.109.078600)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Fadini GP, Schiavan M, Avogaro A & Agostini C 2007 The emerging role of endothelial progenitor cells in pulmonary hypertension and diffuse lung diseases. Sarcoidosis, Vasculitis, and Diffuse Lung Diseases 24 85–93.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Fadini GP, Baesso I, Agostini C, Cuccato E, Nardelli GB, Lapolla A & Avogaro A 2008 Maternal insulin therapy increases fetal endothelial progenitor cells during diabetic pregnancy. Diabetes Care 31 808–810. (https://doi.org/10.2337/dc07-1996)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Ferrara N, Carver-Moore K, Chen H, Dowd M, Lu L, O’Shea KS, Powell-Braxton L, Hillan KJ & Moore MW 1996 Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 380 439–442. (https://doi.org/10.1038/380439a0)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Findlay JK 1986 Angiogenesis in reproductive tissues. Journal of Endocrinology 111 357–366. (https://doi.org/10.1677/joe.0.1110357)

  • Fong GH, Rossant J, Gertsenstein M & Breitman ML 1995 Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature 376 66–70. (https://doi.org/10.1038/376066a0)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Ford SP, Christenson RK & Ford JJ 1982 Uterine blood flow and uterine arterial, venous and luminal concentrations of oestrogens on days 11, 13, and 15 after oestrus in pregnant and non-pregnant sows. Journal of Reproduction and Fertility 64 185–190. (https://doi.org/10.1530/jrf.0.0640185)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Frank JW, Seo H, Burghardt RC, Bayless KJ & Johnson GA 2017 ITGAV (alpha V integrins) bind SPP1 (osteopontin) to support trophoblast cell adhesion. Reproduction 153 695–706. (https://doi.org/10.1530/REP-17-0043)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Gabler C, Chapman DA & Killian GJ 2003 Expression and presence of osteopontin and integrins in the bovine oviduct during the oestrous cycle. Reproduction 126 721–729. (https://doi.org/10.1530/rep.0.1260721)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Gao YA, Agnihotri R, Vary CP & Liaw L 2004 Expression and characterization of recombinant osteopontin peptides representing matrix metalloproteinase proteolytic fragments. Matrix Biology 23 457–466. (https://doi.org/10.1016/j.matbio.2004.09.003)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Garlow JE, Ka H, Johnson GA, Burghardt RC, Jaeger LA & Bazer FW 2002 Analysis of osteopontin at the maternal-placental interface in pigs. Biology of Reproduction 66 718–725. (https://doi.org/10.1095/biolreprod66.3.718)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Gärtner C, Ziegelhöffer B, Kostelka M, Stepan H, Mohr FW & Dhein S 2012 Knock-down of endothelial connexins impairs angiogenesis. Pharmacological Research 65 347–357. (https://doi.org/10.1016/j.phrs.2011.11.012)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Giancotti FG & Ruoslahti E 1999 Integrin signaling. Science 285 1028–1033. (https://doi.org/10.1126/science.285.5430.1028)

  • Hill JM, Zalos G, Halcox JP, Schenke WH, Waclawiw MA, Quyyumi AA & Finkel T 2003 Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. New England Journal of Medicine 348 593–600. (https://doi.org/10.1056/NEJMoa022287)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Hirschi KK, Ingram DA & Yoder MC 2008 Assessing identity, phenotype, and fate of endothelial progenitor cells. Arteriosclerosis, Thrombosis, and Vascular Biology 28 1584–1595. (https://doi.org/10.1161/ATVBAHA.107.155960)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Hoshiga M, Alpers CE, Smith LL, Ciachelli CM & Schwartz SM 1995 Alpha-v beta-3 integrin expression in normal and atherosclerotic artery. Circulation Research 77 1129–1135. (https://doi.org/10.1161/01.res.77.6.1129)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Hristov M & Weber C 2004 Endothelial progenitor cells: characterization, pathophysiology, and possible clinical relevance. Journal of Cellular and Molecular Medicine 8 498–508. (https://doi.org/10.1111/j.1582-4934.2004.tb00474.x)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Hu Z, Zhang F, Yang Z, Yang N, Zhang D, Zhang J & Cao K 2001 Combination of simvastatin and EPC transplantation enhances angiogenesis and protects against apoptosis for hindlimb ischemia. Journal of Biomedical Science 15 509–517.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Humphries JD, Byron A & Humphries MJ 2006 Integrin ligands at a glance. Journal of Cell Science 119 3901–3903. (https://doi.org/10.1242/jcs.03098)

  • Imanishi T, Moriwaki C, Hano T & Nishio I 2005 Endothelial progenitor cell senescence is accelerated in both experimental hypertensive rats and patients with essential hypertension. Journal of Hypertension 10 1831–1837.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Iwakura A, Luedemann C, Shastry S, Hanley A, Kearney M, Aikawa R, Isner JM, Asahara T & Losordo DW 2003 Estrogen-mediated, endothelial nitric oxide synthase-dependent mobilization of bone marrow-derived endothelial progenitor cells contributes to reendothelialization after arterial injury. Circulation 108 3115–3121. (https://doi.org/10.1161/01.CIR.0000106906.56972.83)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Jackson KA, Majka SM, Wang H, Pocius J, Hartley CJ, Majesky MW, Entman ML, Michael LH, Hirschi KK & Goodell MA 2001 Regeneration of ischemic cardiac muscle and vascular endothelium by adult stem cells. Journal of Clinical Investigation 107 1395–1402. (https://doi.org/10.1172/JCI12150)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Jaffe RB 2000 Importance of angiogenesis in reproductive physiology. Seminars in Perinatology 24 79–81. (https://doi.org/10.1016/s0146-0005(00)80062-2)

  • Johnson GA, Spencer TE, Burghardt RC & Bazer FW 1999 Ovine osteopontin: I. Cloning and expression of mRNA in the uterus during the peri-implantation period. Biology of Reproduction 61 884–891. (https://doi.org/10.1095/biolreprod61.4.884)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Johnson GA, Bazer FW, Jaeger LA, Ka H, Garlow JE, Pfarrer C, Spencer TE & Burghardt RC 2001 Muc-1, integrin and osteopontin expression during the implantation cascade in sheep. Biology of Reproduction 65 820–828. (https://doi.org/10.1095/biolreprod65.3.820)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Johnson GA, Burghardt RC, Bazer FW & Spencer TE 2003 Osteopontin: roles in implantation and placentation. Biology of Reproduction 69 1458–1471. (https://doi.org/10.1095/biolreprod.103.020651)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Johnson GA, Burghardt RC & Bazer FW 2014 Osteopontin: a leading candidate adhesion molecule for implantation in pigs and sheep. Journal of Animal Science and Biotechnology 5 56. (https://doi.org/10.1186/2049-1891-5-56)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Joyce MM, Gonzalez JF, Lewis S, Woldesenbet S, Burghardt RC, Newton GR & Johnson GA 2005 Caprine uterine and placental osteopontin expression is distinct among epitheliochorial implanting species. Placenta 26 160–170. (https://doi.org/10.1016/j.placenta.2004.05.009)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kelpke SS, Zinn KR, Rue LW & Thompson JA 2004 Site-specific delivery of acidic fibroblast growth factor stimulates angiogenic and osteogenic responses in vivo. Journal of Biomedical Materials Research: Part A 71 316–325. (https://doi.org/10.1002/jbm.a.30163)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kim J, Erikson DW, Burghardt RC, Spencer TE, Wu G, Bayless KJ, Johnson GA & Bazer FW 2010 Secreted phosphoprotein 1 binds integrins to initiate multiple cell signaling pathways, including FRAP1/mTOR, to support attachment and force-generated migration of trophectoderm cells. Matrix Biology 29 369–382. (https://doi.org/10.1016/j.matbio.2010.04.001)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kovacic JC, Moore J, Herbert A, Ma D, Boehm M & Graham RM 2008 Endothelial progenitor cells, angioblasts, and angiogenesis old terms reconsidered From a current perspective. Trends in Cardiovascular Medicine 18 45–51. (https://doi.org/10.1016/j.tcm.2007.12.002)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Lain KY & Roberts JM 2002 Contemporary concepts of the pathogenesis and management of preeclampsia. JAMA 287 3183–3186. (https://doi.org/10.1001/jama.287.24.3183)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Leali D, Dell’Era P, Stabile H, Sennino B, Chambers AF, Naldini A, Sozzani S, Nico B, Ribatti D & Presta M 2003 Osteopontin (Eta-1) and fibroblast growth factor-2 cross-talk in angiogenesis. Journal of Immunology 171 1085–1093. (https://doi.org/10.4049/jimmunol.171.2.1085)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Liam L, Linder V, Schwartz SM, Chamber AF & Giachelli CM 1995 Osteopontin and beta 3 integrin are coordinately expressed in regenerating endothelium in vivo and stimulate Arg-Gly-Asp-dependent endothelial migration in vitro. Circulation Research 77 665–672. (https://doi.org/10.1161/01.res.77.4.665)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Loomans CJ, De Koning EJ, Staal FJ, Rookmaaker MB, Verseyden C, De Boer HC, Verhaar MC, Braam B, Rabelink TJ & van Zonneveld AJ 2004 Endothelial progenitor cell dysfunction: a novel concept in the pathogenesis of vascular complications of type 1 diabetes. Diabetes 53 195–199. (https://doi.org/10.2337/diabetes.53.1.195)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Matsubara K, Abe E, Matsubara Y, Kameda K & Ito M 2006 Circulating endothelial progenitor cells during normal pregnancy and pre-eclampsia. American Journal of Reproductive Immunology 56 79–85. (https://doi.org/10.1111/j.1600-0897.2006.00387.x)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Mayhew TM, Charnock-Jones DS & Kaufmann P 2004 Aspects of human fetoplacental vasculogenesis and angiogenesis. III. Changes in complicated pregnancies. Placenta 25 127–139. (https://doi.org/10.1016/j.placenta.2003.10.010)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • McFarland RJ, Garza S, Butler WT & Hook M 1995 The mutagenesis of the RGD sequence of recombinant osteopontin causes it to lose its cell adhesion ability. Annals of the New York Academy of Sciences 760 327–331. (https://doi.org/10.1111/j.1749-6632.1995.tb44649.x)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Mirkin S, Arslan M, Churikov D, Corica A, Diaz JI, Williams S, Bocca S & Oehninger S 2005 In search of candidate genes critically expressed in the human endometrium during the window of implantation. Human Reproduction 20 2104–2117. (https://doi.org/10.1093/humrep/dei051)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Murayama T, Tepper OM, Silver M, Ma H, Losordo DW, Isner JM, Asahara T & Kalka C 2002 Determination of bone marrow-derived endothelial progenitor cell significance in angiogenic growth factor-induced neovascularization in vivo. Experimental Hematology 30 967–972. (https://doi.org/10.1016/s0301-472x(02)00867-6)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Naldini A, Leali D, Pucci A, Morena E, Carraro F, Nico B, Ribatti D & Presta M 2006 Cutting edge-IL-1β mediates the proangiogenic activity of osteopontin-activated human monocytes. Journal of Immunology 177 4267–4270. (https://doi.org/10.4049/jimmunol.177.7.4267)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Nomura S, Wills AJ, Edwards DR, Heath JK & Hogan BL 1988 Developmental expression of 2ar (osteopontin) and SPARC (osteonectin) RNA as revealed by in situ hybridization. Journal of Cell Biology 106 441–450. (https://doi.org/10.1083/jcb.106.2.441)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Oliveira E, Tavares KADS, Gomes MTV, Salzedas-Netto AA, Sartori MGF, Castro RA, Fernandes CE & Girao MJBC 2017 Description and evaluation of experimental models for uterine transplantation in pigs. Einstein 15 481–485. (https://doi.org/10.1590/S1679-45082017AO4066)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Orlic D, Kajstura J, Chimenti S, Limana F, Jakoniuk I, Quaini F, Nadal-Ginard B, Bodine DM, Leri A & Anversa P 2001 Mobilized bone marrow cells repair the infarcted heart, improving function and survival. PNAS 98 10344–10349. (https://doi.org/10.1073/pnas.181177898)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Parant O, Dubernard G, Challier JC, Oster M, Uzan S, Aractingi S & Khosrotehrani K 2009 CD34+ cells in maternal placental blood are mainly fetal in origin and express endothelial markers. Laboratory Investigation 89 915–923. (https://doi.org/10.1038/labinvest.2009.55)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Renegar RH, Bazer FW & Roberts RM 1982 Placental transport and distribution of uteroferrin in the fetal pig. Biology of Reproduction 27 1247–1260. (https://doi.org/10.1095/biolreprod27.5.1247)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Rüegg C & Mariotti A 2003 Vascular integrins: pleiotropic adhesion and signaling molecules in vascular homeostasis and angiogenesis. Cellular and Molecular Life Sciences 60 1135–1157. (https://doi.org/10.1007/s00018-003-2297-3)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Samuel CA & Perry JS 1972 The ultrastructure of pig trophoblast tranplanted to an ectopic site in the uterine wall. Journal of Anatomy 113 139–149.

  • Savvidou MD, Xiao Q, Kaihura C, Anderson JM & Nicolaides KH 2008 Maternal circulating endothelial progenitor cells in normal singleton and twin pregnancy. American Journal of Obstetrics and Gynecology 198 414.e1–414.e5. (https://doi.org/10.1016/j.ajog.2007.10.800)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Senger DR & Perruzzi CA 1996 Cell migration promoted by a potent GRGDS-containing thrombin-cleavage fragment of osteopontin. Biochimica et Biophysica Acta 1314 13–24. (https://doi.org/10.1016/s0167-4889(96)00067-5)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Senger DR, Claffey KP, Benes JE, Perruzzi CA, Sergiou AP & Detmar M 1997 Angiogenesis promoted by vascular endothelial growth factor: regulation through α1β1 and α2β1 integrins. PNAS 94 13612–13617. (https://doi.org/10.1073/pnas.94.25.13612)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Senger DR, Perruzzi CA, Streit M, Koteliansky VE, de Fougerolles AR & Detmar M 2002 The α1β1 and α2β1 integrins provide critical support for vascular endothelial growth factor signaling, endothelial cell migration, and tumor angiogenesis. American Journal of Pathology 160 195–204. (https://doi.org/10.1016/S0002-9440(10)64363-5)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Shalaby F, Rossant J, Yamaguchi TP, Gertsenstein M, Wu XF, Breitman ML & Schuh AC 1995 Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 376 62–66. (https://doi.org/10.1038/376062a0)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Shijubo N, Uede T, Kon S, Nagata M & Abe S 2000 Vascular endothelial growth factor and osteopontin in tumor biology. Critical Reviews in Oncogenesis 11 135–146.

  • Smith S, Pfeifer SM & Collins JA 2003 Diagnosis and management of female infertility. JAMA 290 1767–1770. (https://doi.org/10.1001/jama.290.13.1767)

  • Steinhauser CB, Bazer FW, Burghardt RC & Johnson GA 2017 Expression of progesterone receptor in the porcine uterus and placenta throughout gestation: correlation with expression of uteroferrin and osteopontin. Domestic Animal Endocrinology 58 19–29. (https://doi.org/10.1016/j.domaniend.2016.07.002)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Su SC, Mendoza EA & Bayless KJ 2008 Molecular profile of endothelial invasion of three-dimensional collagen matrices: insights into angiogenic sprout induction in wound healing. American Journal of Physiology: Heart and Circulatory Physiology 295 C1215–C1229.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Su SC, Maxwell SA & Bayless KJ 2010 Annexin 2 regulates endothelial morphogenesis by controlling AKT activation and junctional integrity. Journal of Biological Chemistry 285 40624–40634. (https://doi.org/10.1074/jbc.M110.157271)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Sugawara J, Mitsui-Saito M, Hoshiai T, Hayashi C, Kimura Y & Okamura K 2005a Circulating endothelial progenitor cells during human pregnancy. Journal of Clinical Endocrinology and Metabolism 90 1845–1848. (https://doi.org/10.1210/jc.2004-0541)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Sugawara J, Mitsui-Saito M, Hayashi C, Hoshiai T, Senoo M, Chisaka H, Yaegashi N & Okamura K 2005b Decrease and senescence of endothelial progenitor cells in patients with preeclampsia. Journal of Clinical Endocrinology and Metabolism 90 5329–5332. (https://doi.org/10.1210/jc.2005-0532)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Turner CE 2000 Paxillin and focal adhesion signalling. Nature Cell Biology 2 E231–E236. (https://doi.org/10.1038/35046659)

  • Urbich C & Dimmeler S 2004 Endothelial progenitor cells: characterization and role in vascular biology. Circulation Research 95 343–353. (https://doi.org/10.1161/01.RES.0000137877.89448.78).

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Wagner DD, Olmsted JB & Marder VJ 1982 Immunolocalization of von Willebrand protein in Weibel-Palade bodies of human endothelial cells. Journal of Cell Biology 95 355–360. (https://doi.org/10.1083/jcb.95.1.355)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Wallez Y & Huber P 2008 Endothelial adherens and tight junctions in cascular homeostasis, inflammation and angiogenesis. Biochimica et Biophysica Acta 1778 794–809. (https://doi.org/10.1016/j.bbamem.2007.09.003)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Wallez Y, Vilgrain I & Huber P 2006 Angiogenesis: the VE-cadherin switch. Trends in Cardiovascular Medicine 16 55–59. (https://doi.org/10.1016/j.tcm.2005.11.008)

  • White FJ, Foss JW, Joyce MM, Geisert RD, Burghardt RC & Johnson GA 2005 Steroid regulation of cell-specific secreted phosphoprotein 1 (osteopontin) expression in the pregnant porcine uterus. Biology of Reproduction 73 1294–1301. (https://doi.org/10.1095/biolreprod.105.045153)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Yu J, Wuj J, Bagchi IC, Bagchi MK, Sidell N & Taylor RN 2011 Disruption of gap junctions reduces biomarkers of decidualization and angiogenesis and increases inflammatory mediators in human endometrial stromal cell cultures. Molecular and Cellular Endocrinology 344 25–34. (https://doi.org/10.1016/j.mce.2011.04.011)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Zygmunt M, Herr F, Münstedt K, Lang U & Liang OD 2003 Angiogenesis and vasculogenesis in pregnancy. European Journal of Obstetrics, Gynecology, and Reproductive Biology 110 (Supplement 1) S10–S18. (https://doi.org/10.1016/s0301-2115(03)00168-4)

    • PubMed
    • Search Google Scholar
    • Export Citation