Agrin pathway is controlled by leukemia inhibitory factor (LIF) in murine implantation

Journal of Reproduction and Development

Volumn 55, Issue 3, 2009, Pages 293-298

  Terakawa, Jumpei ^a   Hondo, Eiichi ^a   Sugiyama, Makoto ^a   Wakitani, Shoichi ^a   Stewart, Colin L ^b   Kiso, Yasuo ^a  

^a YAMAGUCHI UNIVERSITY   (Japan)

^b INSTITUTE OF MEDICAL BIOLOGY   (Singapore)

Author keywords

Acetylcholine receptor; Agrin; Embryo implantation; Leukemia inhibitory factor

Indexed keywords

AGRIN; CHOLINERGIC RECEPTOR; LEUKEMIA INHIBITORY FACTOR;

ANIMAL; ARTICLE; BAGG ALBINO MOUSE; C57BL MOUSE; FEMALE; GENETICS; METABOLISM; MOUSE; MOUSE MUTANT; NIDATION; PHYSIOLOGY; PREGNANCY; REPRODUCTION; SIGNAL TRANSDUCTION; UTERUS;

AGRIN; ANIMALS; EMBRYO IMPLANTATION; FEMALE; LEUKEMIA INHIBITORY FACTOR; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; PLACENTATION; PREGNANCY; RECEPTORS, CHOLINERGIC; SIGNAL TRANSDUCTION; UTERUS;

MURINAE; MUS;

EID: 68149162537     PISSN: 09168818     EISSN: 13484400     Source Type: Journal    
DOI: 10.1262/jrd.20162     Document Type: Article

References (38)

1. Carson DD, Bagchi I, Dey SK, Enders AC, Fazleabas AT, Lessey BA, Yoshinaga K. Embryo implantation. Dev Biol 2000; 223: 217-237.
2. Hardingham TE, Fosang AJ. Proteoglycans: many forms and many functions. FASEB J 1992; 6: 861-870.
3. Kirn-Safran CB, D'Souza SS, Carson DD. Heparan sulfate proteoglycans and their binding proteins in embryo implantation and placentation. Semin Cell Dev Biol 2008; 19: 187-193
4. Chen CP, Liu SH, Lee MY, Chen YY. Heparan sulfate proteoglycans in the basement membranes of the human placenta and decidua. Placenta 2008; 29: 309-316.
5. Nakato H, Kimata K. Heparan sulfate fine structure and specificity of proteoglycan functions. Biochim Biophys Acta 2002; 1573: 312-318.
6. Jokimaa V, Inki P, Kujari H, Hirvonen O, Ekholm E, Anttila L. Expression of syndecan-1 in human placenta and decidua. Placenta 1998; 19: 157-163.
7. Crescimanno C, Marzioni D, Paradinas FJ, Schrurs B, Mühlhauser J, Todros T, Newlands E, David G, Castellucci M. Expression pattern alterations of syndecans and glypican-1 in normal and pathological trophoblast. J Pathol 1999; 189: 600-608.
8. Khan S, Blackburn M, Mao DL, Huber R, Schlessinger D, Fant M. Glypican-3 (GPC3) expression in human placenta: localization to the differentiated syncytiotrophoblast. Histol Histopathol 2001; 16: 71-78.
9. Bix G, Iozzo RV. Matrix revolutions: 'tails' of basement-membrane components with angiostatic functions. Trends Cell Biol 2005; 15: 52-60.
10. Stringer SE. The role of heparan sulphate proteoglycans in angiogenesis. Biochem Soc Trans 2006; 34: 451-453.
11. Pollheimer J, Bauer S, Huber A, Husslein P, Aplin JD, Knöfler M. Expression pattern of collagen XVIII and its cleavage product, the angiogenesis inhibitor endostatin, at the fetal-maternal interface. Placenta 2004; 25: 770-779.
12. San Martin S, Soto-Suazo M, Zorn TM. Perlecan and syndecan-4 in uterine tissues during the early pregnancy in mice. Am J Reprod Immunol 2004; 52: 53-59.
13. D'Souza SS, Daikoku T, Farach-Carson MC, Carson DD. Heparanase expression and function during early pregnancy in mice. Biol Reprod 2007; 77: 433-441.
14. Nitkin RM, Smith MA, Magill C, Fallon JR, Yao YM, Wallace BG, McMahan UJ. Identification of agrin, a synaptic organizing protein from Torpedo electric organ. J Cell Biol 1987; 105: 2471-2478.
15. Witzemann V. Development of the neuromuscular junction. Cell Tissue Res 2006; 326: 263-271.
16. Stewart CL, Kaspar P, Brunet LJ, Bhatt H, Gadi I, Köntgen F, Abbondanzo SJ. Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor.Nature 1992; 359: 76-77.
17. Shen MM, Leder P. Leukemia inhibitory factor is expressed by the preimplantation uterus and selectively blocks primitive ectoderm formation in vitro. Proc Natl Acad Sci USA 1992; 89: 8240-8244.
18. Chen JR, Cheng JG, Shatzer T, Sewell L, Hernandez L, Stewart CL. Leukemia inhibitory factor can substitute for nidatory estrogen and is essential to inducing a receptive uterus for implantation but is not essential for subsequent embryogenesis. Endocrinology 2000; 141: 4365-4372.
19. Tapia A, Salamonsen LA, Manuelpillai U, Dimitriadis E. Leukemia inhibitory factor promotes human first trimester extravillous trophoblast adhesion to extracellular matrix and secretion of tissue inhibitor of metalloproteinases-1 and -2. Hum Reprod 2008; 23: 1724-1732.
20. Kawashima K, Fujii T. Basic and clinical aspects of non-neuronal acetylcholine: overview of non-neuronal cholinergic systems and their biological significance. J Pharmacol Sci 2008; 106: 167-173.
21. Grando SA, Kawashima K, Kirkpatrick CJ, Wessler I. Recent progress in understanding the non-neuronal cholinergic system in humans. Life Sci 2007; 80: 2181-2185.
22. Sastry BV. Human placental cholinergic system. Biochem Pharmacol 1997; 53: 1577-1586.
23. Horikoshi T, Fujii T, Kawashima K, Sakuragawa N. Acetylcholine increase in amniotic fluid of experimental rats for intrauterine growth retardation. Life Sci 2003; 72: 2145-2149.
24. Mayerhofer A, Kunz L, Krieger A, Proskocil B, Spindel E, Amsterdam A, Dissen GA, Ojeda SR, Wessler I. FSH regulates acetycholine production by ovarian granulosa cells. Reprod Biol Endocrinol 2006; 4: 37.
25. Schönherr E, Hausser HJ. Extracellular matrix and cytokines: a functional unit. Dev Immunol 2000; 7: 89-101.
26. Kreuger J, Spillmann D, Li JP, Lindahl U. Interactions between heparan sulfate and proteins: the concept of specificity. J Cell Biol 2006; 174: 323-327.
27. Iozzo RV. Heparan sulfate proteoglycans: intricate molecules with intriguing functions. J Clin Invest 2001; 108: 165-167.
28. Tumova S, Woods A, Couchman JR. Heparan sulfate proteoglycans on the cell surface: versatile coordinators of cellular functions. Int J Biochem Cell Biol 2000; 32: 269-288.
29. Gautam M, Noakes PG, Moscoso L, Rupp F, Scheller RH, Merlie JP, Sanes JR. Defective neuromuscular synaptogenesis in agrin-deficient mutant mice. Cell 1996; 85: 525-535.
30. Karl T. Advanced segmentation. In: The House Mouse: Atlas of Embryonic Development. New York: Springer-Verlag; 1989: 10-11.
31. Bhatt H, Brunet LJ, Stewart CL. Uterine expression of leukemia inhibitory factor coincides with the onset of blastocyst implantation. Proc Natl Acad Sci USA 1991; 88: 11408-11412.
32. Hyland RA, Shaw TJ, Png FY, Murphy CR. Pan-cadherin concentrates apically in uterine epithelial cells during uterine closure in the rat. Acta Histochem 1998; 100: 75-81.
33. Burgess RW, Skarnes WC, Sanes JR. Agrin isoforms with distinct amino termini: differential expression, localization, and function. J Cell Biol 2000; 151: 41-52.
34. Slater CR. Agrin signals at the junction. Nature 1996; 381: 478-479.
35. Trinidad JC, Fischbach GD, Cohen JB. The Agrin/MuSK signaling pathway is spatially segregated from the neuregulin/ErbB receptor signaling pathway at the neuromuscular junction. J Neurosci 2000; 20: 8762-8770.
36. Millar NS, Harkness PC. Assembly and trafficking of nicotinic acetylcholine receptors (Review). Mol Membr Biol 2008; 25: 279-292.
37. Kobayashi H, Miyahara K, Kusafuka J, Yamataka A, Lane GJ, Sueyoshi N, Miyano T, Puri P. A new rapid acetylcholinesterase staining kit for diagnosing Hirschsprung's disease. Pediatr Surg Int 2007; 23: 505-508.
38. Tátrai P, Dudás J, Batmunkh E, Máthé M, Zalatnai A, Schaff Z, Ramadori G, Kovalszky I. Agrin, a novel basement membrane component in human and rat liver, accumulates in cirrhosis and hepatocellular carcinoma. Lab Invest 2006; 86: 1149-1160.