Long-term type 1 diabetes impairs decidualization and extracellular matrix remodeling during early embryonic development in mice on occasion of the 30th anniversary of the Laboratory of Reproductive and Extracellular Matrix Biology we dedicate this article to its founder, Professor Paulo Abrahamsohn.

Placenta

Volumn 34, Issue 12, 2013, Pages 1128-1135

  Favaro, R R ^a   Salgado, R M ^a   Covarrubias, A C ^a   Bruni, F ^b   Lima, C ^b   Fortes, Z B ^a   Zorn, T M ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b INSTITUTO BUTANTAN   (Brazil)

Author keywords

Decidua; Early embryonic development; Extracellular matrix; Maternal fetal interface; Mouse; Pregnancy; Type 1 diabetes

Indexed keywords

BIGLYCAN; COLLAGEN; LUMICAN; MESSENGER RNA; PROTEOGLYCAN;

ALLOXAN DIABETES MELLITUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DECIDUALIZATION; DIABETOGENESIS; DISEASE COURSE; EMBRYO DEVELOPMENT; EXTRACELLULAR MATRIX; FEMALE; INSULIN DEPENDENT DIABETES MELLITUS; MOUSE; NONHUMAN; PATHOPHYSIOLOGY; PREGNANCY COMPLICATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSMISSION ELECTRON MICROSCOPY;

D; DAYS AFTER DIABETES INDUCTION; DECIDUA; EARLY EMBRYONIC DEVELOPMENT; ECM; ELISA; ENZYME-LINKED IMMUNOSORBENT ASSAY; EXTRACELLULAR MATRIX; GAPDH; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASE; HOURS OF PREGNANCY; HP; IL11; INTERLEUKIN 11; MATERNAL-FETAL INTERFACE; MATRIX METALLOPROTEINASE; MMP; MOUSE; PBS; PHOSPHATE BUFFERED SALINE; PREGNANCY; QPCR; QUANTITATIVE REAL TIME PCR; SLRPS; SMALL LEUCINE RICH PROTEOGLYCANS; TYPE 1 DIABETES;

ANIMALS; BIGLYCAN; CHONDROITIN SULFATE PROTEOGLYCANS; DECIDUA; DIABETES MELLITUS, TYPE 1; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; EMBRYO IMPLANTATION, DELAYED; EMBRYO LOSS; EXTRACELLULAR MATRIX; FEMALE; FETAL DISEASES; FIBRILLAR COLLAGENS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INTERLEUKIN-11; KERATAN SULFATE; MICE; PLACENTATION; PREGNANCY; PREGNANCY IN DIABETICS; RNA, MESSENGER;

EID: 84888309666     PISSN: 01434004     EISSN: 15323102     Source Type: Journal    
DOI: 10.1016/j.placenta.2013.09.012     Document Type: Article

References (46)

1. R. Vargas, J.T. Repke, and S.H. Ural Type 1 diabetes mellitus and pregnancy Rev Obstet Gynecol 3 3 2010 92 100
2. H. Otani, O. Tanaka, R. Tatewaki, H. Naora, and T. Yoneyama Diabetic environment and genetic predisposition as causes of congenital malformations in NOD mouse embryos Diabetes 40 10 1991 1245 1250
3. P.A. Abrahamsohn, and T.M. Zorn Implantation and decidualization in rodents J Exp Zool 266 6 1993 603 628
4. P.A. Abrahamsohn, T.M.T. Zorn, and S.F. Oliveira Decidua in rodents S.R. Glasser, J.D. Aplin, L.C. Guidice, S. Tabibzadeh, The endometrium 1st ed. 2002 Informa Healthcare London 279 293
5. R. Favaro, P. Abrahamsohn, and T. Zorn Decidualization and endometrial extracellular matrix remodeling A. Croy, A.T. Yamada, F. DeMayo, S.L. Adamson, The guide to investigation of mouse pregnancy 1st ed. 2013 Elsevier [in press]
6. T.M. Zorn, E.M. Bevilacqua, and P.A. Abrahamsohn Collagen remodeling during decidualization in the mouse Cell Tissue Res 244 2 1986 443 448
7. M.C. Alberto-Rincon, T.M. Zorn, and P.A. Abrahamsohn Diameter increase of collagen fibrils of the mouse endometrium during decidualization Am J Anat 186 4 1989 417 429
8. S.F. Oliveira, T. Nagata, and P.A. Abrahamsohn Electron microscopic radioautographic study on the incorporation of 3H-proline by mouse decidual cells Cell Mol Biol 37 3 1991 315 323
9. W.R. Teodoro, S.S. Witzel, A.P. Velosa, M. Shimokomaki, P.A. Abrahamsohn, and T.M. Zorn Increase of interstitial collagen in the mouse endometrium during decidualization Connect Tissue Res 44 2 2003 96 103
10. K. Spiess, and T.M. Zorn Collagen types I, III, and V constitute the thick collagen fibrils of the mouse decidua Microsc Res Tech 70 1 2007 18 25
11. K. Spiess, W.R. Teodoro, and T.M. Zorn Distribution of collagen types I, III, and V in pregnant mouse endometrium Connect Tissue Res 48 2 2007 99 108
12. S. San Martin, M. Soto-Suazo, S.F. De Oliveira, J.D. Aplin, P. Abrahamsohn, and T.M. Zorn Small leucine-rich proteoglycans (SLRPs) in uterine tissues during pregnancy in mice Reproduction 125 4 2003 585 595
13. S. San Martin, and T.M. Zorn The small proteoglycan biglycan is associated with thick collagen fibrils in the mouse decidua Cell Mol Biol (Noisy-le-grand) 49 4 2003 673 678
14. J.C. Sanches, C.J. Jones, J.D. Aplin, R.V. Iozzo, T.M. Zorn, and S.F. Oliveira Collagen fibril organization in the pregnant endometrium of decorin-deficient mice J Anat 216 1 2010 144 155
15. L. Robb, R. Li, L. Hartley, H.H. Nandurkar, F. Koentgen, and C.G. Begley Infertility in female mice lacking the receptor for interleukin 11 is due to a defective uterine response to implantation Nat Med 4 3 1998 303 308
16. C.A. White, L. Robb, and L.A. Salamonsen Uterine extracellular matrix components are altered during defective decidualization in interleukin-11 receptor alpha deficient mice Reprod Biol Endocrinol 2 2004 76
17. A. Jawerbaum, and E. Gonzalez Diabetic pregnancies: the challenge of developing in a pro-inflammatory environment Curr Med Chem 13 18 2006 2127 2138
18. R. Higa, M. Kurtz, E. Capobianco, N. Martínez, V. White, and A. Jawerbaum Altered matrix metalloproteinases and tissue inhibitors of metalloproteinases in embryos from diabetic rats during early organogenesis Reprod Toxicol 32 4 2011 449 462
19. R.R. Favaro, R.M. Salgado, P.R. Raspantini, Z.B. Fortes, and T.M. Zorn Effects of long-term diabetes on the structure and cell proliferation of the myometrium in the early pregnancy of mice Int J Exp Pathol 91 5 2010 426 435
20. R.M. Salgado, R.R. Favaro, S.S. Martin, and T.M. Zorn The estrous cycle modulates small leucine-rich proteoglycans expression in mouse uterine tissues Anat Rec (Hoboken) 292 1 2009 138 153
21. R.M. Salgado, L.P. Capelo, R.R. Favaro, J.D. Glazier, J.D. Aplin, and T.M. Zorn Hormone-regulated expression and distribution of versican in mouse uterine tissues Reprod Biol Endocrinol 7 2009 60
22. R.M. Salgado, R.R. Favaro, and T.M. Zorn Modulation of small leucine-rich proteoglycans (SLRPs) expression in the mouse uterus by estradiol and progesterone Reprod Biol Endocrinol 9 2011 22
23. Renato M. Salgado, Ambart C. Covarrubias, R.R. Favaro, Caroline Serrano-Nascimento, Maria Tereza Nunes, and T.M. Zorn Estradiol induces transcriptional and posttranscriptional modifications in versican expression in the mouse uterus J Mol Histol 44 2013 221
24. P.W. Nathanielsz Animal models that elucidate basic principles of the developmental origins of adult diseases ILAR J 47 1 2006 73 82
25. P. White Pregnancy complicating diabetes Am J Med 7 5 1949 609 616
26. L.M. Pedersen, I. Tygstrup, and J. Pedersen Congenital malformations in newborn infants of diabetic women. Correlation with maternal diabetic vascular complications Lancet 1 7343 1964 1124 1126
27. K. Karlsson, and I. Kjellmer The outcome of diabetic pregnancies in relation to the mother's blood sugar level Am J Obstet Gynecol 112 2 1972 213 220
28. H. Kalter Reproductive toxicology in animals with induced and spontaneous diabetes Reprod Toxicol 10 6 1996 417 438
29. A. Jawerbaum, and V. White Animal models in diabetes and pregnancy Endocr Rev 31 5 2010 680 701
30. D.R. Garris Effects of diabetes on uterine condition, decidualization, vascularization, and corpus luteum function in the pseudopregnant rat Endocrinology 122 2 1988 665 672
31. A.J. Albaghdadi, and F.W. Kan Endometrial receptivity defects and impaired implantation in diabetic NOD mice Biol Reprod 87 2 2012 30 1-16
32. D.R. Armant Blastocysts don't go it alone. Extrinsic signals fine-tune the intrinsic developmental program of trophoblast cells Dev Biol 280 2 2005 260 280
33. U.K. Rout, J. Wang, B.C. Paria, and D.R. Armant Alpha5beta1, alphaVbeta3 and the platelet-associated integrin alphaIIbbeta3 coordinately regulate adhesion and migration of differentiating mouse trophoblast cells Dev Biol 268 1 2004 135 151
34. D.R. Garris, C. Smith, D. Davis, A.R. Diani, and G.C. Gerritsen Morphometric evaluation of the hypothalamic-ovarian axis of the ketonuric, diabetic Chinese hamster: relationship to the reproductive cycle Diabetologia 23 3 1982 275 279
35. M. Tesone, R.G. Ladenheim, R.M. Oliveira-Filho, V.A. Chiauzzi, V.G. Foglia, and E.H. Charreau Ovarian dysfunction in streptozotocin-induced diabetic rats Proc Soc Exp Biol Med 174 1983 123 130
36. S. Jesmin, I. Sakuma, Y. Hattori, and A. Kitabatake Role of angiotensin II in altered expression of molecules responsible for coronary matrix remodeling in insulin-resistant diabetic rats Arterioscler Thromb Vasc Biol 23 2003 2021 2026
37. F.R. Giachini, V. Carriel, L.P. Capelo, R.C. Tostes, M.H. Carvalho, and Z.B. Fortes Maternal diabetes affects specific extracellular matrix components during placentation J Anat 212 1 2008 31 41
38. L. Schaefer, I. Raslik, H.J. Grone, E. Shonherr, K. Macakova, and J. Ugorcakova Small proteoglycans in human diabetic nephropathy: discrepancy between glomerular expression and protein accumulation of decorin, biglycan, lumican, and fibromodulin FASEB J 15 3 2001 559 561
39. A. Dixon, and C. Maric 17beta-Estradiol attenuates diabetic kidney disease by regulating extracellular matrix and transforming growth factor-beta protein expression and signaling Am J Physiol Renal Physiol 293 5 2007 F1678 F1690
40. W.P. Grant, R. Sullivan, D.E. Sonenshine, M. Adam, J.H. Slusser, and K.A. Carson Electron microscopic investigation of the effects of diabetes mellitus on the Achilles tendon J Foot Ankle Surg 36 4 1997 272 278
41. P. Odetti, I. Aragno, R. Rolandi, S. Garibaldi, S. Valentini, and L. Cosso Scanning force microscopy reveals structural alterations in diabetic rat collagen fibrils: role of protein glycation Diabetes Metab Res Rev 16 2 2000 74 81
42. D.L. Ribeiro, S.R. Taboga, and R.M. Goes Diabetes induces stromal remodelling and increase in chondroitin sulphate proteoglycans of the rat ventral prostate Int J Exp Pathol 90 4 2009 400 411
43. D.E. Birk, J.M. Fitch, J.P. Babiarz, K.J. Doane, and T.F. Linsenmayer Collagen fibrillogenesis in vitro: interaction of types I and V collagen regulates fibril diameter J Cell Sci 95 Pt 4 1990 649 657
44. K.G. Danielson, H. Baribault, D.F. Holmes, H. Graham, K.E. Kadler, and R.V. Iozzo Targeted disruption of decorin leads to abnormal collagen fibril morphology and skin fragility J Cell Biol 136 3 1997 729 743
45. K.L. Reigle, G. Di Lullo, K.R. Turner, J.A. Last, I. Chervoneva, and D.E. Birk Non-enzymatic glycation of type I collagen diminishes collagen- proteoglycan binding and weakens cell adhesion J Cell Biochem 104 5 2008 1684 1698
46. The Diabetes Control and Complications Trial Research Group The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus N Engl J Med 329 14 1993 977 986