Intrauterine infusion of latency-associated peptide (LAP) during early porcine pregnancy affects conceptus elongation and placental size

Biology of Reproduction

Volumn 82, Issue 3, 2010, Pages 534-542

  Massuto, Dana A ^a   Hooper, R Neil ^a   Kneese, Eric C ^a   Johnson, Greg A ^a   Ing, Nancy H ^b   Weeks, Bradley R ^a   Jaeger, Laurie A ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Conceptus; Implantation; Integrins; Pig; Pregnancy; Transforming growth factor beta; Uterus

Indexed keywords

INTEGRIN; LATENCY ASSOCIATED PEPTIDE; SMAD1 PROTEIN; SMAD2 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; ENDOMETRIUM; EXPERIMENTAL PIG; FETUS; FETUS DEVELOPMENT; FETUS WEIGHT; GESTATIONAL AGE; IMPLANTATION; NONHUMAN; OSMOTIC PUMP; PLACENTA; PREGNANCY; PRIORITY JOURNAL; VAGINAL HYSTERECTOMY; ANIMAL; ANIMAL DISEASE; BLASTOCYST; BREEDING; CLINICAL TRIAL; CYTOLOGY; DRUG ADMINISTRATION ROUTE; DRUG EFFECT; FEMALE; INFUSION PUMP; NIDATION; ORGAN SIZE; OSMOSIS; SWINE; UTERUS;

SUIDAE; SUS;

ANIMALS; BLASTOCYST; DRUG ADMINISTRATION ROUTES; EMBRYO IMPLANTATION; EMBRYONIC DEVELOPMENT; FEMALE; FETAL WEIGHT; GESTATIONAL AGE; INFUSION PUMPS; ORGAN SIZE; OSMOSIS; PLACENTA; PREGNANCY; PREGNANCY, ANIMAL; SWINE; TRANSFORMING GROWTH FACTOR BETA1; UTERUS;

EID: 77953104042     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.109.081893     Document Type: Article

References (67)

1. Pope WF, Maurer RR, Stormshak F. Survival of porcine embryos after asynchronous transfer (41495). Proc Soc Exp Biol Med 1982; 171:179-183.
2. Pope WF, Lawyer MS, Nara BS, First NL. Effect of asynchronous superinduction on embryo survival and range of blastocyst development in swine. Biol Reprod 1986; 35:133-137.
3. Geisert RD, Ross JW, Ashworth MD, White FJ, Johnson GA, DeSilva U. Maternal recognition of pregnancy signal or endocrine disruptor: the two faces of oestrogen during establishment of pregnancy in the pig. Soc Reprod Fertil Suppl 2006; 62:131-145.
4. Geisert RD, Renegar RH, Thatcher WW, Roberts RM, Bazer FW. Establishment of pregnancy in the pig, I: interrelationships between preimplantation development of the pig blastocyst and uterine endometrial secretions. Biol Reprod 1982; 27:925-939.
5. Keys JL, King GJ. Microscopic examination of porcine conceptus-maternal interface between days 10 and 19 of pregnancy. Am J Anat 1990; 188:221-238.
6. Pratt BR, Butcher RL, Inskeep EK. Effect of continuous intrauterine administration of prostaglandin E2 on life span of corpora lutea of nonpregnant ewes. J Anim Sci 1979; 48:1441-1446.
7. Ayad VJ, Parkinson TJ, Matthews EL, Wild ML. Effects of pregnancy and systemic or intrauterine oxytocin infusion on the distribution of endometrial oxytocin receptors in the ewe: an autoradiographic study. J Endocrinol 1993; 137:423-431.
8. Vanderwall DK, Woods GL, Weber JA, Lichtenwalner AB. Corpus luteal function in nonpregnant mares following intrauterine administration of prostaglandin E(2) or estradiol-17beta. Theriogenology 1994; 42:1069-1083.
9. Joyce MM, Burghardt JR, Burghardt RC, Hooper RN, Jaeger LA, Spencer TE, Bazer FW, Johnson GA. Pig conceptuses increase uterine interferonregulatory factor 1 (IRF1), but restrict expression to stroma through estrogen-induced IRF2 in luminal epithelium. Biol Reprod 2007; 77:292-302.
10. Joyce MM, Burghardt JR, Burghardt RC, Hooper RN, Bazer FW, Johnson GA. Uterine MHC class I molecules and beta 2-microglobulin are regulated by progesterone and conceptus interferons during pig pregnancy. J Immunol 2008; 181:2494-2505.
11. Joyce MM, Burghardt RC, Geisert RD, Burghardt JR, Hooper RN, Ross JW, Ashworth MD, Johnson GA. Pig conceptuses secrete estrogen and interferons to differentially regulate uterine STAT1 in a temporal and cell type-specific manner. Endocrinology 2007; 148:4420-4431.
12. Bowen JA, Bazer FW, Burghardt RC. Spatial and temporal analyses of integrin and Muc-1 expression in porcine uterine epithelium and trophectoderm in vivo. Biol Reprod 1996; 55:1098-1106.
13. Burghardt RC, Johnson GA, Jaeger LA, Ka H, Garlow JE, Spencer TE, Bazer FW. Integrins and extracellular matrix proteins at the maternal-fetal interface in domestic animals. Cells Tissues Organs 2002; 172:202-217. (Pubitemid 36005558)
14. Gupta A, Bazer FW, Jaeger LA. Differential expression of beta transforming growth factors (TGF beta 1, TGF beta 2, and TGF beta 3) and their receptors (type I and type II) in peri-implantation porcine conceptuses. Biol Reprod 1996; 55:796-802.
15. Gupta A, Dekaney CM, Bazer FW, Madrigal MM, Jaeger LA. Beta transforming growth factors (TGFbeta) at the porcine conceptus-maternal interface, part II: uterine TGFbeta bioactivity and expression of immunoreactive TGFbetas (TGFbeta1, TGFbeta2, and TGFbeta3) and their receptors (type I and type II). Biol Reprod 1998; 59:911-917.
16. Gupta A, Ing NH, Bazer FW, Bustamante LS, Jaeger LA. Beta transforming growth factors (TGFss) at the porcine conceptus-maternal interface, part I: expression of TGFbeta1, TGFbeta2, and TGFbeta3 messenger ribonucleic acids. Biol Reprod 1998; 59:905-910. (Pubitemid 28463344)
17. Gentry LE, Lioubin MN, Purchio AF, Marquardt H. Molecular events in the processing of recombinant type 1 pre-pro-transforming growth factor beta to the mature polypeptide. Mol Cell Biol 1988; 8:4162-4168.
18. Lawrence DA, Pircher R, Kryceve-Martinerie C, Jullien P. Normal embryo fibroblasts release transforming growth factors in a latent form. J Cell Physiol 1984; 121:184-188. (Pubitemid 14017248)
19. Miyazono K, Hellman U, Wernstedt C, Heldin CH. Latent high molecular weight complex of transforming growth factor beta 1. Purification from human platelets and structural characterization. J Biol Chem 1988; 263: 6407-6415.
20. Macias-Silva M, Abdollah S, Hoodless PA, Pirone R, Attisano L, Wrana JL. MADR2 is a substrate of the TGFbeta receptor and its phosphorylation is required for nuclear accumulation and signaling. Cell 1996; 87:1215-1224. (Pubitemid 27010105)
21. Nakao A, Imamura T, Souchelnytskyi S, Kawabata M, Ishisaki A, Oeda E, Tamaki K, Hanai J, Heldin CH, Miyazono K, ten Dijke P. TGF-beta receptor-mediated signalling through Smad2, Smad3 and Smad4. EMBO J 1997; 16:5353-5362.
22. Zhang Y, Feng X, We R, Derynck R. Receptor-associated Mad homologues synergize as effectors of the TGF-beta response. Nature 1996; 383:168-172. (Pubitemid 26303979)
23. Annes JP, Munger JS, Rifkin DB. Making sense of latent TGFbeta activation. J Cell Sci 2003; 116:217-224.
24. Wipff PJ, Hinz B. Integrins and the activation of latent transforming growth factor beta1 - an intimate relationship. Eur J Cell Biol 2008; 87: 601-615.
25. Jenkins G. The role of proteases in transforming growth factor-beta activation. Int J Biochem Cell Biol 2008; 40:1068-1078.
26. Ruoslahti E. RGD and other recognition sequences for integrins. Annu Rev Cell Dev Biol 1996; 12:697-715. (Pubitemid 26422728)
27. Bershadsky A, Kozlov M, Geiger B. Adhesion-mediated mechanosensitivity: a time to experiment, and a time to theorize. Curr Opin Cell Biol 2006; 18:472-481. (Pubitemid 44332917)
28. Hynes RO. Integrins: versatility, modulation, and signaling in cell adhesion. Cell 1992; 69:11-25.
29. Wozniak MA, Modzelewska K, Kwong L, Keely PJ. Focal adhesion regulation of cell behavior. Biochim Biophys Acta 2004; 1692:103-119. (Pubitemid 38891769)
30. Zaidel-Bar R, Itzkovitz S, Ma'ayan A, Iyengar R, Geiger B. Functional atlas of the integrin adhesome. Nat Cell Biol 2007; 9:858-867.
31. Ludbrook SB, Barry ST, Delves CJ, Horgan CM. The integrin alphavbeta3 is a receptor for the latency-associated peptides of transforming growth factors beta1 and beta3. Biochem J 2003; 369:311-318.
32. Mu D, Cambier S, Fjellbirkeland L, Baron JL, Munger JS, Kawakatsu H, Sheppard D, Broaddus VC, Nishimura SL. The integrin alpha(v)beta8 mediates epithelial homeostasis through MT1-MMP-dependent activation of TGF-beta1. J Cell Biol 2002; 157:493-507.
33. Munger JS, Harpel JG, Giancotti FG, Rifkin DB. Interactions between growth factors and integrins: latent forms of transforming growth factor-beta are ligands for the integrin alphavbeta1. Mol Biol Cell 1998; 9:2627-2638.
34. Munger JS, Huang X, Kawakatsu H, Griffiths MJ, Dalton SL, Wu J, Pittet JF, Kaminski N, Garat C, Matthay MA, Rifkin DB, Sheppard D. The integrin alpha v beta 6 binds and activates latent TGF beta 1: a mechanism for regulating pulmonary inflammation and fibrosis. Cell 1999; 96:319-328. (Pubitemid 29077586)
35. Jaeger LA, Spiegel AK, Ing NH, Johnson GA, Bazer FW, Burghardt RC. Functional effects of transforming growth factor beta on adhesive properties of porcine trophectoderm. Endocrinology 2005; 146:3933-3942.
36. Harney JP, Bazer FW. Effects of conceptus and conceptus secretory products on uterine development in the pig. Reprod Fertil Dev 1990; 2: 179-187.
37. Sample GL, Kubotsu SL, Carnahan KG, Mirando MA. Interestrous interval of cyclic gilts is decreased by systemic but not intrauterine administration of exogenous oxytocin. J Anim Sci 2000; 78:2393-2398.
38. Sample GL, Blackwell DM, Kubotsu SL, Mirando MA. Endocrine secretion of prostaglandin F2alpha in cyclic gilts is decreased by intrauterine administration of exogenous oxytocin. Anim Reprod Sci 2004; 84:395-406.
39. Jana B, Kucharski J, Dzienis A, Deptula K. Changes in prostaglandin production and ovarian function in gilts during endometritis induced by Escherichia coli infection. Anim Reprod Sci 2007; 97:137-150. (Pubitemid 44708539)
40. Bennett GL, Leymaster KA. Integration of ovulation rate, potential embryonic viability and uterine capacity into a model of litter size in swine. J Anim Sci 1989; 67:1230-1241.
41. Stroband HW, Van der Lende T. Embryonic and uterine development during early pregnancy in pigs. J Reprod Fertil Suppl 1990; 40:261-277.
42. Illera MJ, Cullinan E, Gui Y, Yuan L, Beyler SA, Lessey BA. Blockade of the alpha(v)beta(3) integrin adversely affects implantation in the mouse. Biol Reprod 2000; 62:1285-1290.
43. Fassler R, Meyer M. Consequences of lack of beta 1 integrin gene expression in mice. Genes Dev 1995; 9:1896-1908.
44. Hynes RO, Bader BL. Targeted mutations in integrins and their ligands: their implications for vascular biology. Thromb Haemost 1997; 78:83-87.
45. Bader BL, Rayburn H, Crowley D, Hynes RO. Extensive vasculogenesis, angiogenesis, and organogenesis precede lethality in mice lacking all alpha v integrins. Cell 1998; 95:507-519. (Pubitemid 28533307)
46. Stephens LE, Sutherland AE, Klimanskaya IV, Andrieux A, Meneses J, Pedersen RA, Damsky CH. Deletion of beta 1 integrins in mice results in inner cell mass failure and peri-implantation lethality. Genes Dev 1995; 9: 1883-1895.
47. Chung IB, Yelian FD, Zaher FM, Gonik B, Evans MI, Diamond MP, Svinarich DM. Expression and regulation of vascular endothelial growth factor in a first trimester trophoblast cell line. Placenta 2000; 21:320-324. (Pubitemid 30364865)
48. Dickson MC, Martin JS, Cousins FM, Kulkarni AB, Karlsson S, Akhurst RJ. Defective haematopoiesis and vasculogenesis in transforming growth factor-beta 1 knock out mice. Development 1995; 121:1845-1854.
49. Blomberg L, Hashizume K, Viebahn C. Blastocyst elongation, trophoblastic differentiation, and embryonic pattern formation. Reproduction 2008; 135:181-195. (Pubitemid 351267388)
50. Wilson ME, Biensen NJ, Ford SP. Novel insight into the control of litter size in pigs, using placental efficiency as a selection tool. J Anim Sci 1999; 77:1654-1658.
51. Wilson ME, Ford SP. Comparative aspects of placental efficiency. Reprod Suppl 2001; 58:223-232.
52. Wilson ME, Ford SP. Effect of estradiol-17beta administration during the time of conceptus elongation on placental size at term in Meishan pigs. J Anim Sci 2000; 78:1047-1052.
53. Rhodes M, Brendemuhl JH, Hansen PJ. Litter characteristics of gilts artificially inseminated with transforming growth factor-beta. Am J Reprod Immunol 2006; 56:153-156.
54. Rahimi RA, Leof EB. TGF-beta signaling: a tale of two responses. J Cell Biochem 2007; 102:593-608.
55. Sato Y, Rifkin DB. Inhibition of endothelial cell movement by pericytes and smooth muscle cells: activation of a latent transforming growth factor-beta 1-like molecule by plasmin during co-culture. J Cell Biol 1989; 109: 309-315. (Pubitemid 19180138)
56. Shull MM, Ormsby I, Kier AB, Pawlowski S, Diebold RJ, Yin M, Allen R, Sidman C, Proetzel G, Calvin D, Annunziata N, Doetschman T. Targeted disruption of the mouse transforming growth factor-beta 1 gene results in multifocal inflammatory disease. Nature 1992; 359:693-699.
57. Taipale J, Koli K, Keski-Oja J. Release of transforming growth factor-beta 1 from the pericellular matrix of cultured fibroblasts and fibrosarcoma cells by plasmin and thrombin. J Biol Chem 1992; 267:25378-25384.
58. Huang XZ, Wu JF, Cass D, Erle DJ, Corry D, Young SG, Farese RV Jr, Sheppard D. Inactivation of the integrin beta 6 subunit gene reveals a role of epithelial integrins in regulating inflammation in the lung and skin. J Cell Biol 1996; 133:921-928. (Pubitemid 26160991)
59. Zhu J, Motejlek K, Wang D, Zang K, Schmidt A, Reichardt LF. Beta8 integrins are required for vascular morphogenesis in mouse embryos. Development 2002; 129:2891-2903. (Pubitemid 34874268)
60. Annes JP, Rifkin DB, Munger JS. The integrin alphaVbeta6 binds and activates latent TGFbeta3. FEBS Lett 2002; 511:65-68.
61. Asano Y, Ihn H, Yamane K, Jinnin M, Mimura Y, Tamaki K. Increased expression of integrin alpha(v)beta3 contributes to the establishment of autocrine TGF-beta signaling in scleroderma fibroblasts. J Immunol 2005; 175:7708-7718.
62. Asano Y, Ihn H, Yamane K, Jinnin M, Mimura Y, Tamaki K. Involvement of alphavbeta5 integrin-mediated activation of latent transforming growth factor beta1 in autocrine transforming growth factor beta signaling in systemic sclerosis fibroblasts. Arthritis Rheum 2005; 52:2897-2905. (Pubitemid 41369121)
63. Lyons RM, Gentry LE, Purchio AF, Moses HL. Mechanism of activation of latent recombinant transforming growth factor beta 1 by plasmin. J Cell Biol 1990; 110:1361-1367. (Pubitemid 20136511)
64. Yu Q, Stamenkovic I. Cell surface-localized matrix metalloproteinase-9 proteolytically activates TGF-beta and promotes tumor invasion and angiogenesis. Genes Dev 2000; 14:163-176. (Pubitemid 30070982)
65. Foxcroft GR, Dixon WT, Treacy BK, Jiang L, Novak S, Mao J, Almeida FL. Insights into conceptus-reproductive tract interaction in the pig. J Anim Sci 2000; 77:1-15.
66. Kayser JP, Kim JG, Cerny RL, Vallet JL. Global characterization of porcine intrauterine proteins during early pregnancy. Reproduction 2006; 131:379-388.
67. Fazleabas AT, Geisert RD, Bazer FW, Roberts RM. Relationship between release of plasminogen activator and estrogen by blastocysts and secretion of plasmin inhibitor by uterine endometrium in the pregnant pig. Biol Reprod 1983; 29:225-238.