Placental vasculogenesis is regulated by keratin-mediated hyperoxia in murine decidual tissues

American Journal of Pathology

Volumn 178, Issue 4, 2011, Pages 1578-1590

  Kröger, Cornelia ^a,b   Vijayaraj, Preethi ^a,c   Reuter, Ursula ^a   Windoffer, Reinhard ^d   Simmons, David ^e   Heukamp, Lukas ^a   Leube, Rudolf ^d   Magin, Thomas M ^a,b  

^a UNIVERSITY OF BONN   (Germany)

^b UNIVERSITY OF LEIPZIG   (Germany)

^c HARVARD MEDICAL SCHOOL   (United States)

^d RWTH AACHEN UNIVERSITY   (Germany)

^e UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; KERATIN; PLACENTAL GROWTH FACTOR; PROLACTIN; PROLACTIN LIKE PROTEIN; UNCLASSIFIED DRUG; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL INFILTRATION; CONTROLLED STUDY; DECIDUA; DECIDUALIZATION; EMBRYO; EMBRYONIC STRUCTURES; FEMALE; GAS EXCHANGE; HYPEROXIA; INNER EAR; MOUSE; NATURAL KILLER CELL; NONHUMAN; PLACENTA FUNCTION; PRIORITY JOURNAL; PROTEIN SECRETION; SIGNAL TRANSDUCTION; TROPHOBLAST; VASCULARIZATION;

EID: 79953650678     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2010.12.055     Document Type: Article

References (83)

1. Fuchs E, Cleveland DW: A structural scaffolding of intermediate filaments in health and disease. Science 1998, 279:514-519 (Pubitemid 28067272)
2. Irvine AD, McLean WH: Human keratin diseases: the increasing spectrum of disease and subtlety of the phenotype-genotype correlation. Br J Dermatol 1999, 140:815-828 (Pubitemid 29238452)
3. Magin TM, Reichelt J, Hatzfeld M: Emerging functions: diseases and animal models reshape our view of the cytoskeleton. Exp Cell Res 2004, 301:91-102 (Pubitemid 39388901)
4. Omary MB, Coulombe PA, McLean WH: Intermediate filament proteins and their associated diseases. N Engl J Med 2004, 351:2087-2100 (Pubitemid 39482502)
5. Betz RC, Planko L, Eigelshoven S, Hanneken S, Pasternack SM, Bussow H, Van Den Bogaert K, Wenzel J, Braun-Falco M, Rutten A, Rogers MA, Ruzicka T, Nothen MM, Magin TM, Kruse R: Loss-offunction mutations in the keratin 5 gene lead to Dowling-Degos disease. Am J Hum Genet 2006, 78:510-519 (Pubitemid 43291233)
6. Kim S, Wong P, Coulombe PA: A keratin cytoskeletal protein regulates protein synthesis and epithelial cell growth. Nature 2006, 441:362-365 (Pubitemid 44050202)
7. Magin TM, Vijayaraj P, Leube RE: Structural and regulatory functions of keratins. Exp Cell Res 2007, 313:2021-2032 (Pubitemid 46842973)
8. Margolis SS, Perry JA, Forester CM, Nutt LK, Guo Y, Jardim MJ, Thomenius MJ, Freel CD, Darbandi R, Ahn JH, Arroyo JD, Wang XF, Shenolikar S, Nairn AC, Dunphy WG, Hahn WC, Virshup DM, Kornbluth S: Role for the PP2A/B56delta phosphatase in regulating 14-3-3 release from Cdc25 to control mitosis. Cell 2006, 127:759-773 (Pubitemid 44781028)
9. Vijayaraj P, Kroeger C, Reuter U, Hartmann D, Magin TM: Keratins regulate yolk sac hematopoiesis and vasculogenesis through reduced BMP-4 signaling. Eur J Cell Biol 2010, 89:299-306
10. Vijayaraj P, Kroger C, Reuter U, Windoffer R, Leube RE, Magin TM: Keratins regulate protein biosynthesis through localization of GLUT1 and -3 upstream of AMP kinase and Raptor. J Cell Biol 2009, 187:175-184
11. Hesse M, Franz T, Tamai Y, Taketo MM, Magin TM: Targeted deletion of keratins 18 and 19 leads to trophoblast fragility and early embryonic lethality. EMBO J 2000, 19:5060-5070
12. Tamai Y, Ishikawa T, Bosl MR, Mori M, Nozaki M, Baribault H, Oshima RG, Taketo MM: Cytokeratins 8 and 19 in the mouse placental development. J Cell Biol 2000, 151:563-572
13. Baribault H, Price J, Miyai K, Oshima RG: Mid-gestational lethality in mice lacking keratin 8. Genes Dev 1993, 7:1191-1202 (Pubitemid 23207410)
14. Jaquemar D, Kupriyanov S, Wankell M, Avis J, Benirschke K, Baribault H, Oshima RG: Keratin 8 protection of placental barrier function. J Cell Biol 2003, 161:749-756 (Pubitemid 36648758)
15. Cross JC, Nakano H, Natale DR, Simmons DG, Watson ED: Branching morphogenesis during development of placental villi. Differentiation 2006, 74:393-401 (Pubitemid 44215410)
16. Bany BM, Cross JC: Post-implantation mouse conceptuses produce paracrine signals that regulate the uterine endometrium undergoing decidualization. Dev Biol 2006, 294:445-456 (Pubitemid 43866684)
17. Adelman DM, Gertsenstein M, Nagy A, Simon MC, Maltepe E: Placental cell fates are regulated in vivo by HIF-mediated hypoxia responses. Genes Dev 2000, 14:3191-3203 (Pubitemid 32015136)
18. Barak Y, Nelson MC, Ong ES, Jones YZ, Ruiz-Lozano P, Chien KR, Koder A, Evans RM: PPAR gamma is required for placental, cardiac, and adipose tissue development. Mol Cell 1999, 4:585-595 (Pubitemid 29531138)
19. Barak Y, Sadovsky Y, Shalom-Barak T: PPAR signaling in placental development and function. PPAR Res 2008, 2008:142082
20. Cowden Dahl KD, Fryer BH, Mack FA, Compernolle V, Maltepe E, Adelman DM, Carmeliet P, Simon MC: Hypoxia-inducible factors 1alpha and 2alpha regulate trophoblast differentiation. Mol Cell Biol 2005, 25:10479-10491 (Pubitemid 41681969)
21. Gabriel HD, Jung D, Butzler C, Temme A, Traub O, Winterhager E, Willecke K: Transplacental uptake of glucose is decreased in embryonic lethal connexin26-deficient mice. J Cell Biol 1998, 140:1453-1461 (Pubitemid 28152993)
22. Ishikawa T, Tamai Y, Zorn AM, Yoshida H, Seldin MF, Nishikawa S, Taketo MM: Mouse Wnt receptor gene Fzd5 is essential for yolk sac and placental angiogenesis. Development 2001, 128:25-33 (Pubitemid 32094383)
23. Katschinski DM, Le L, Schindler SG, Thomas T, Voss AK, Wenger RH: Interaction of the PAS B domain with HSP90 accelerates hypoxia-inducible factor-1alpha stabilization. Cell Physiol Biochem 2004, 14: 351-360 (Pubitemid 39179204)
24. Kozak W, Wrotek S, Walentynowicz K: Hypoxia-induced sickness behaviour. J Physiol Pharmacol 2006, 57(Suppl 8):35-50 (Pubitemid 46548775)
25. Mudgett JS, Ding J, Guh-Siesel L, Chartrain NA, Yang L, Gopal S, Shen MM: Essential role for p38alpha mitogen-activated protein kinase in placental angiogenesis. Proc Natl Acad Sci U S A 2000, 97:10454-10459
26. Schorpp-Kistner M, Wang ZQ, Angel P, Wagner EF: JunB is essential for mammalian placentation. EMBO J 1999, 18:934-948 (Pubitemid 29082273)
27. Steingrimsson E, Tessarollo L, Reid SW, Jenkins NA, Copeland NG: The bHLH-Zip transcription factor Tfeb is essential for placental vascularization. Development 1998, 125:4607-4616 (Pubitemid 29027191)
28. Voss AK, Thomas T, Gruss P: Mice lacking HSP90beta fail to develop a placental labyrinth. Development 2000, 127:1-11 (Pubitemid 30064383)
29. Xu X, Weinstein M, Li C, Naski M, Cohen RI, Ornitz DM, Leder P, Deng C: Fibroblast growth factor receptor 2 (FGFR2)-mediated reciprocal regulation loop between FGF8 and FGF10 is essential for limb induction. Development 1998, 125:753-765 (Pubitemid 28108099)
30. Suri C, Jones PF, Patan S, Bartunkova S, Maisonpierre PC, Davis S, Sato TN, Yancopoulos GD: Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell 1996, 87:1171-1180 (Pubitemid 27010101)
31. Maisonpierre PC, Suri C, Jones PF, Bartunkova S, Wiegand SJ, Radziejewski C, Compton D, McClain J, Aldrich TH, Papadopoulos N, Daly TJ, Davis S, Sato TN, Yancopoulos GD: Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis. Science 1997, 277:55-60 (Pubitemid 27450643)
32. Breier G, Clauss M, Risau W: Coordinate expression of vascular endothelial growth factor receptor-1 (flt-1) and its ligand suggests a paracrine regulation of murine vascular development. Dev Dyn 1995, 204:228-239
33. Duarte A, Hirashima M, Benedito R, Trindade A, Diniz P, Bekman E, Costa L, Henrique D, Rossant J: Dosage-sensitive requirement for mouse Dll4 in artery development. Genes Dev 2004, 18:2474-2478 (Pubitemid 39362889)
34. Fong GH, Rossant J, Gertsenstein M, Breitman ML: Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature 1995, 376:66-70
35. Gale NW, Dominguez MG, Noguera I, Pan L, Hughes V, Valenzuela DM, Murphy AJ, Adams NC, Lin HC, Holash J, Thurston G, Yancopoulos GD: Haploinsufficiency of delta-like 4 ligand results in embryonic lethality due to major defects in arterial and vascular development. Proc Natl Acad Sci U S A 2004, 101:15949-15954 (Pubitemid 39507907)
36. Limbourg FP, Takeshita K, Radtke F, Bronson RT, Chin MT, Liao JK: Essential role of endothelial Notch1 in angiogenesis. Circulation 2005, 111:1826-1832 (Pubitemid 40525149)
37. Shalaby F, Rossant J, Yamaguchi TP, Gertsenstein M, Wu XF, Breitman ML, Schuh AC: Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 1995, 376:62-66
38. Dumont DJ, Gradwohl G, Fong GH, Puri MC, Gertsenstein M, Auerbach A, Breitman ML: Dominant-negative and targeted null mutations in the endothelial receptor tyrosine kinase, tek, reveal a critical role in vasculogenesis of the embryo. Genes Dev 1994, 8:1897-1909 (Pubitemid 24273890)
39. Sato TN, Tozawa Y, Deutsch U, Wolburg-Buchholz K, Fujiwara Y, Gendron-Maguire M, Gridley T, Wolburg H, Risau W, Qin Y: Distinct roles of the receptor tyrosine kinases Tie-1 and Tie-2 in blood vessel formation. Nature 1995, 376:70-74
40. Hustin J, Schaaps JP: Echographic [corrected] and anatomic studies of the maternotrophoblastic border during the first trimester of pregnancy. Am J Obstet Gynecol 1987, 157:162-168 (Pubitemid 17099909)
41. Pringle KG, Kind KL, Thompson JG, Roberts CT: Complex interactions between hypoxia inducible factors, insulin-like growth factor-II and oxygen in early murine trophoblasts. Placenta 2007, 28:1147-1157 (Pubitemid 47570906)
42. Dunwoodie SL: The role of hypoxia in development of the mammalian embryo. Dev Cell 2009, 17:755-773
43. Ramirez-Bergeron DL, Runge A, Adelman DM, Gohil M, Simon MC: HIF-dependent hematopoietic factors regulate the development of the embryonic vasculature. Dev Cell 2006, 11:81-92 (Pubitemid 43960804)
44. Caniggia I, Mostachfi H, Winter J, Gassmann M, Lye SJ, Kuliszewski M, Post M: Hypoxia-inducible factor-1 mediates the biological effects of oxygen on human trophoblast differentiation through TGFbeta(3). J Clin Invest 2000, 105:577-587 (Pubitemid 30146504)
45. Nagamatsu T, Fujii T, Kusumi M, Zou L, Yamashita T, Osuga Y, Momoeda M, Kozuma S, Taketani Y: Cytotrophoblasts up-regulate soluble fms-like tyrosine kinase-1 expression under reduced oxygen: an implication for the placental vascular development and the pathophysiology of preeclampsia. Endocrinology 2004, 145:4838-4845 (Pubitemid 39551100)
46. Jauniaux E, Watson AL, Hempstock J, Bao YP, Skepper JN, Burton GJ: Onset of maternal arterial blood flow and placental oxidative stress. A possible factor in human early pregnancy failure. Am J Pathol 2000, 157:2111-2122
47. Jauniaux E, Hempstock J, Greenwold N, Burton GJ: Trophoblastic oxidative stress in relation to temporal and regional differences in maternal placental blood flow in normal and abnormal early pregnancies. Am J Pathol 2003, 162:115-125 (Pubitemid 36041994)
48. Reichelt J, Magin TM: Hyperproliferation, induction of c-Myc and 14-3-3sigma, but no cell fragility in keratin-10-null mice. J Cell Sci 2002, 115:2639-2650 (Pubitemid 34846505)
49. McManus JF: Histological and histochemical uses of periodic acid. Stain Technol 1948, 23:99-108
50. Simmons DG, Natale DR, Begay V, Hughes M, Leutz A, Cross JC: Early patterning of the chorion leads to the trilaminar trophoblast cell structure in the placental labyrinth. Development 2008, 135:2083-2091 (Pubitemid 352015143)
51. Anson-Cartwright L, Dawson K, Holmyard D, Fisher SJ, Lazzarini RA, Cross JC: The glial cells missing-1 protein is essential for branching morphogenesis in the chorioallantoic placenta. Nat Genet 2000, 25:311-314 (Pubitemid 30437319)
52. Colosi P, Thordarson G, Hellmiss R, Singh K, Forsyth IA, Gluckman P, Wood WI: Cloning and expression of ovine placental lactogen. Mol Endocrinol 1989, 3:1462-1469 (Pubitemid 19241040)
53. Lescisin KR, Varmuza S, Rossant J: Isolation and characterization of a novel trophoblast-specific cDNA in the mouse. Genes Dev 1988, 2:1639-1646
54. Lin J, Poole J, Linzer DI: Three new members of the mouse prolactin/growth hormone family are homologous to proteins expressed in the rat. Endocrinology 1997, 138:5541-5549 (Pubitemid 27509720)
55. Basyuk E, Cross JC, Corbin J, Nakayama H, Hunter P, Nait-Oumesmar B, Lazzarini RA: Murine Gcm1 gene is expressed in a subset of placental trophoblast cells. Dev Dyn 1999, 214:303-311 (Pubitemid 29160207)
56. Ain R, Tash JS, Soares MJ: Prolactin-like protein-A is a functional modulator of natural killer cells at the maternal-fetal interface. Mol Cell Endocrinol 2003, 204:65-74 (Pubitemid 36871553)
57. Muller H, Liu B, Croy BA, Head JR, Hunt JS, Dai G, Soares MJ: Uterine natural killer cells are targets for a trophoblast cell-specific cytokine, prolactin-like protein A. Endocrinology 1999, 140:2711-2720 (Pubitemid 32245151)
58. Croy BA, Luross JA, Guimond MJ, Hunt JS: Uterine natural killer cells: insights into lineage relationships and functions from studies of pregnancies in mutant and transgenic mice. Nat Immun 1996, 15:22-33 (Pubitemid 27042054)
59. Paffaro VA, Jr., Bizinotto MC, Joazeiro PP, Yamada AT: Subset classification of mouse uterine natural killer cells by DBA lectin reactivity. Placenta 2003, 24:479-488 (Pubitemid 37184769)
60. Hanna J, Goldman-Wohl D, Hamani Y, Avraham I, Greenfield C, Natanson-Yaron S, Prus D, Cohen-Daniel L, Arnon TI, Manaster I, Gazit R, Yutkin V, Benharroch D, Porgador A, Keshet E, Yagel S, Mandelboim O: Decidual NK cells regulate key developmental processes at the human fetal-maternal interface. Nat Med 2006, 12:1065-1074 (Pubitemid 44353388)
61. Croy BA, Ashkar AA, Minhas K, Greenwood JD: Can murine uterine natural killer cells give insights into the pathogenesis of preeclampsia? J Soc Gynecol Investig 2000, 7:12-20
62. Soares MJ, Konno T, Alam SM: The prolactin family: effectors of pregnancy-dependent adaptations. Trends Endocrinol Metab 2007, 18:114-121 (Pubitemid 46464021)
63. Yadi H, Burke S, Madeja Z, Hemberger M, Moffett A, Colucci F: Unique receptor repertoire in mouse uterine NK cells. J Immunol 2008, 181:6140-6147
64. Baumhueter S, Singer MS, Henzel W, Hemmerich S, Renz M, Rosen SD, Lasky LA: Binding of L-selectin to the vascular sialomucin CD34. Science 1993, 262:436-438 (Pubitemid 23353389)
65. Baldwin HS, Shen HM, Yan HC, DeLisser HM, Chung A, Mickanin C, Trask T, Kirschbaum NE, Newman PJ, Albelda SM, et al: Platelet endothelial cell adhesion molecule-1 (PECAM-1/CD31): alternatively spliced, functionally distinct isoforms expressed during mammalian cardiovascular development. Development 1994, 120:2539-2553
66. Ginouves A, Ilc K, Macias N, Pouyssegur J, Berra E: PHDs overactivation during chronic hypoxia "desensitizes" HIFalpha and protects cells from necrosis. Proc Natl Acad Sci U S A 2008, 105:4745-4750
67. Levy AP, Levy NS, Wegner S, Goldberg MA: Transcriptional regulation of the rat vascular endothelial growth factor gene by hypoxia. J Biol Chem 1995, 270:13333-13340
68. Achen MG, Gad JM, Stacker SA, Wilks AF: Placenta growth factor and vascular endothelial growth factor are co-expressed during early embryonic development. Growth Factors 1997, 15:69-80 (Pubitemid 27485259)
69. Yancopoulos GD, Davis S, Gale NW, Rudge JS, Wiegand SJ, Holash J: Vascular-specific growth factors and blood vessel formation. Nature 2000, 407:242-248
70. Kanasaki K, Palmsten K, Sugimoto H, Ahmad S, Hamano Y, Xie L, Parry S, Augustin HG, Gattone VH, Folkman J, Strauss JF, Kalluri R: Deficiency in catechol-O-methyltransferase and 2-methoxyoestradiol is associated with pre-eclampsia. Nature 2008, 453:1117-1121 (Pubitemid 351871733)
71. Simmons DG, Fortier AL, Cross JC: Diverse subtypes and developmental origins of trophoblast giant cells in the mouse placenta. Dev Biol 2007, 304:567-578 (Pubitemid 46533975)
72. Adamson SL, Lu Y, Whiteley KJ, Holmyard D, Hemberger M, Pfarrer C, Cross JC: Interactions between trophoblast cells and the maternal and fetal circulation in the mouse placenta. Dev Biol 2002, 250:358-373 (Pubitemid 35216421)
73. Bordeleau F, Galarneau L, Gilbert S, Loranger A, Marceau N: Keratin 8/18 modulation of protein kinase C-mediated integrin-dependent adhesion and migration of liver epithelial cells. Mol Biol Cell 2010, 21:1698-1713
74. Jackson D, Volpert OV, Bouck N, Linzer DI: Stimulation and inhibition of angiogenesis by placental proliferin and proliferin-related protein. Science 1994, 266:1581-1584
75. Toivola DM, Krishnan S, Binder HJ, Singh SK, Omary MB: Keratins modulate colonocyte electrolyte transport via protein mistargeting. J Cell Biol 2004, 164:911-921 (Pubitemid 38366902)
76. Ma GT, Linzer DI: GATA-2 restricts prolactin-like protein A expression to secondary trophoblast giant cells in the mouse. Biol Reprod 2000, 63:570-574 (Pubitemid 30639948)
77. Ain R, Dai G, Dunmore JH, Godwin AR, Soares MJ: A prolactin family paralog regulates reproductive adaptations to a physiological stressor. Proc Natl Acad Sci U S A 2004, 101:16543-16548 (Pubitemid 39557749)
78. Tayade C, Hilchie D, He H, Fang Y, Moons L, Carmeliet P, Foster RA, Croy BA: Genetic deletion of placenta growth factor in mice alters uterine NK cells. J Immunol 2007, 178:4267-4275 (Pubitemid 46492377)
79. Brusselmans K, Bono F, Collen D, Herbert JM, Carmeliet P, Dewerchin M: A novel role for vascular endothelial growth factor as an autocrine survival factor for embryonic stem cells during hypoxia. J Biol Chem 2005, 280:3493-3499 (Pubitemid 40223814)
80. Gerber HP, Malik AK, Solar GP, Sherman D, Liang XH, Meng G, Hong K, Marsters JC, Ferrara N: VEGF regulates haematopoietic stem cell survival by an internal autocrine loop mechanism. Nature 2002, 417:954-958 (Pubitemid 34716872)
81. Rhodes KE, Gekas C, Wang Y, Lux CT, Francis CS, Chan DN, Conway S, Orkin SH, Yoder MC, Mikkola HK: The emergence of hematopoietic stem cells is initiated in the placental vasculature in the absence of circulation. Cell Stem Cell 2008, 2:252-263 (Pubitemid 351298590)
82. Pankov R, Neznanov N, Umezawa A, Oshima RG: AP-1. ETS, and transcriptional silencers regulate retinoic acid-dependent induction of keratin 18 in embryonic cells. Mol Cell Biol 1994, 14:7744-7757
83. Maynard SE, Min JY, Merchan J, Lim KH, Li J, Mondal S, Libermann TA, Morgan JP, Sellke FW, Stillman IE, Epstein FH, Sukhatme VP, Karumanchi SA: Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J Clin Invest 2003, 111:649-658 (Pubitemid 36278583)