The effect of maternal malnutrition during lactation on the endometrial ERα expression, collagen type, and blood vessels in the rats offspring at puberty

Anatomical Record

Volumn 293, Issue 1, 2010, Pages 162-170

  Brasil, Flávia Bittencourt ^a   Faria, Tatiane Silva ^a   Sampaio, Francisco José Barcellos ^a   Ramos, Cristiane Da Fonte ^a  

^a STATE UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

Angiogenesis; Collagen; Endometrium; Estradiol; Lactation; Malnutrition

Indexed keywords

COLLAGEN; ESTRADIOL; ESTROGEN RECEPTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD VESSEL; BODY WEIGHT; CONTROLLED STUDY; DIETARY INTAKE; ESTRADIOL BLOOD LEVEL; FEMALE; FOOD INTAKE; LACTATION; MATERNAL NUTRITION; NONHUMAN; PRIORITY JOURNAL; PROGENY; PROTEIN CALORIE MALNUTRITION; PROTEIN EXPRESSION; PUBERTY; RAT;

ANIMALS; ANIMALS, NEWBORN; BLOOD VESSELS; BLOTTING, WESTERN; COLLAGEN; DIET, PROTEIN-RESTRICTED; ENDOMETRIUM; ESTROGEN RECEPTOR ALPHA; FEMALE; LACTATION; MATERNAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; PROTEIN-ENERGY MALNUTRITION; PUBERTY; RATS; RATS, WISTAR;

RATTUS;

EID: 74249115139     PISSN: 19328486     EISSN: 19328494     Source Type: Journal    
DOI: 10.1002/ar.21028     Document Type: Article

References (47)

1. Alberto-Rincon MC, Zorn TM, Abrahamsohn PA. 1989. Diameter increase of collagen fibrils of the mouse endometrium during decidualization. Am J Anat 186:417-429.
2. Barker DJ. 1998. In utero programming of chronic disease. Clin Sci (Lond) 95:115-128.
3. Barker DJ, Osmond C. 1986. Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet 1:1077-1081.
4. Bayne K. 1996. Revised guide for the care and use of laboratory animals available. American Physiological Society. Physiologist 39:199, 208-111.
5. Berndt S, Perrier d'Hauterive S, Blacher S, Pequeux C, Lorquet S, Munaut C, Applanat M, Herve MA, Lamande N, Corvol P, van den Brule F, Frankenne F, Poutanen M, Huhtaniemi I, Geenen V, Noel A, Foidart JM. 2006. Angiogenic activity of human chorionic gonadotropin through LH receptor activation on endothelial and epithelial cells of the endometrium. FASEB J 20:2630-2632.
6. Birk DE, Fitch JM, Babiarz JP, Linsenmayer TF. 1988. Collagen type I and type V are present in the same fibril in the avian corneal stroma. J Cell Biol 106:999-1008.
7. Bradbury P, Rae K. 1996. Connective tissues and stains. In: Bancroft J, Stevens A, editors. Theory and practice of histological techniques. New York: Churchill Livingstone. p 113-138.
8. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254.
9. Brasil FB, Faria TS, Costa WS, Sampaio FJ, Ramos CF. 2005. The pups' endometrium morphology is affected by maternal malnutrition during suckling. Maturitas 51:405-412.
10. Cox DA, Helvering LM. 2006. Extracellular matrix integrity: a possible mechanism for differential clinical effects among selective estrogen receptor modulators and estrogens? Mol Cell Endocrinol 247:53-59.
11. Cruz-Orive LM, Weibel ER. 1990. Recent stereological methods for cell biology: a brief survey. Am J Physiol 258:L148-L156.
12. da Silva Faria T, Brasil FB, Sampaio FJB, da Fonte Ramos C. 2008. Maternal malnutrition during lactation alters the folliculogenesis and gonadotropins and estrogen isoforms ovarian receptors in the offspring at puberty. J Endocrinol 198:625-634.
13. da Silva Faria T, da Fonte Ramos C, Sampaio FJ. 2004. Puberty onset in the female offspring of rats submitted to protein or energy restricted diet during lactation. J Nutr Biochem 15:123-127.
14. Fischbeck KL, Rasmussen KM. 1987. Effect of repeated reproductive cycles on maternal nutritional status, lactational performance and litter growth in ad libitum-fed and chronically food-restricted rats. J Nutr 117:1967-1975.
15. Fleischmajer R, MacDonald ED, Perlish JS, Burgeson RE, Fisher LW. 1990a. Dermal collagen fibrils are hybrids of type I and type III collagen molecules. J Struct Biol 105:162-169.
16. Fleischmajer R, Perlish JS, Burgeson RE, Shaikh-Bahai F, Timpl R. 1990b. Type I and type III collagen interactions during fibrillogenesis. Ann NY Acad Sci 580:161-175.
17. Guzman C, Cabrera R, Cardenas M, Larrea F, Nathanielsz PW, Zambrano E. 2006. Protein restriction during fetal and neonatal development in the rat alters reproductive function and accelerates reproductive ageing in female progeny. J Physiol 572:97-108.
18. Helvering LM, Adrian MD, Geiser AG, Estrem ST, Wei T, Huang S, Chen P, Dow ER, Calley JN, Dodge JA, Grese TA, Jones SA, Halladay DL, Miles RR, Onyia JE, Ma YL, Sato M, Bryant HU. 2005. Differential effects of estrogen and raloxifene on messenger RNA and matrix metalloproteinase 2 activity in the rat uterus. Biol Reprod 72:830-841.
19. Heywood WE, Mian N, Milla PJ, Lindley KJ. 2004. Programming of defective rat pancreatic beta-cell function in offspring from mothers fed a low-protein diet during gestation and the suckling periods. Clin Sci (Lond) 107:37-45.
20. Iwahashi M, Ooshima A, Nakano R. 1997. Effects of oestrogen on the extracellular matrix in the endometrium of postmenopausal women. J Clin Pathol 50:755-759.
21. Junqueira LC, Bignolas GM, Brentani RR. 1979. Picrosirius staining plus polarization microscopy, a specific method for collagen detection in tissue sections. Histochem J 11:447-455.
22. Kelly BA, Bond BC, Poston L. 2003. Gestational profile of matrix metalloproteinases in rat uterine artery. Mol Hum Reprod 9:351-358.
23. Khorram O, Khorram N, Momeni M, Han G, Halem J, Desai M, Ross MG. 2007. Maternal undernutrition inhibits angiogenesis in the offspring: a potential mechanism of programmed hypertension. Am J Physiol Regul Integr Comp Physiol 293:R745-R753.
24. Leonhardt M, Lesage J, Croix D, Dutriez-Casteloot I, Beauvillain JC, Dupouy JP. 2003. Effects of perinatal maternal food restriction on pituitary-gonadal axis and plasma leptin level in rat pup at birth and weaning and on timing of puberty. Biol Reprod 68:390-400.
25. Lydrup ML, Ferno M. 2003. Correlation between estrogen receptor alpha expression, collagen content and stiffness in human uterine arteries. Acta Obstet Gynecol Scand 82:610-615.
26. Manase K, Endo T, Chida M, Nagasawa K, Honnma H, Yamazaki K, Kitajima Y, Goto T, Kanaya M, Hayashi T, Mitaka T, Saito T. 2006. Coordinated elevation of membrane type 1-matrix metalloproteinase and matrix metalloproteinase-2 expression in rat uterus during postpartum involution. Reprod Biol Endocrinol 4:32.
27. Mandarim-de-Lacerda CA. 2003. Stereological tools in biomedical research. An Acad Bras Cienc 75:469-486.
28. Manni A, Baker R, Arafah BM, Pearson OH. 1981. Uterine oestrogen and progesterone receptors in the ovariectomized rat. J Endocrinol 91:281-287.
29. Moura AS, Caldeira Filho JS, de Freitas Mathias PC, de Sa CC. 1997. Insulin secretion impairment and insulin sensitivity improvement in adult rats undernourished during early lactation. Res Commun Mol Pathol Pharmacol 96:179-192.
30. Nephew KP, Long X, Osborne E, Burke KA, Ahluwalia A, Bigsby RM. 2000. Effect of estradiol on estrogen receptor expression in rat uterine cell types. Biol Reprod 62:168-177.
31. Olsen BR, Ninomiya Y. 1999. Fibrillar collagens. In: Kreis T, Vale R, editors. Guidebook to the extracellular matrix, anchor and adhesion proteins. Oxford: Oxford University Press. p 383-387.
32. Passos MCF, Ramos CF, Moura EG. 2000. Short and long term effects of malnutrition in rats during lactation on the body weight of offspring. Nutr Res 20:1603-1612.
33. Pavelock K, Braas K, Ouafik L, Osol G, May V. 2001. Differential expression and regulation of the vascular endothelial growth factor receptors neuropilin-1 and neuropilin-2 in rat uterus. Endocrinology 142:613-622.
34. Poston L. 2007. Influences of maternal nutritional status on vascular function in the offspring. Curr Drug Targets 8:914-922.
35. Ramos CF, Lima AP, Teixeira CV, Brito PD, Moura EG. 1997. Thyroid function in post-weaning rats whose dams were fed a low-protein diet during suckling. Braz J Med Biol Res 30:133-137.
36. Reeves PG, Nielsen FH, Fahey GC, Jr. 1993. AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr 123:1939-1951.
37. Rodriguez HA, Kass L, Varayoud J, Ramos JG, Ortega HH, Durando M, Munoz-De-Toro M, Luque EH. 2003. Collagen remodelling in the guinea-pig uterine cervix at term is associated with a decrease in progesterone receptor expression. Mol Hum Reprod 9:807-813.
38. Rosser M, Chorich L, Howard E, Zamorano P, Mahesh VB. 1993. Changes in rat uterine estrogen receptor messenger ribonucleic acid levels during estrogen- and progesterone-induced estrogen receptor depletion and subsequent replenishment. Biol Reprod 48:89-98.
39. Sokal RR, Rohlf FJ. 1995. Biometry: the principles and practice of statistics in biological research. 3rd ed. W. H. Freeman and Co.: New York. p 887.
40. Srivastava RK, Gu Y, Ayloo S, Zilberstein M, Gibori G. 1998. Developmental expression and regulation of basic fibroblast growth factor and vascular endothelial growth factor in rat decidua and in a decidual cell line. J Mol Endocrinol 21:355-362.
41. Teixeira C, Passos M, Ramos C, Dutra S, Moura E. 2002. Leptin serum concentration, food intake and body weight in rats whose mothers were exposed to malnutrition during lactation. J Nutr Biochem 13:493.
42. Teixeira CV, Silandre D, de Souza Santos AM, Delalande C, Sampaio FJ, Carreau S, da Fonte Ramos C. 2007. Effects of maternal undernutrition during lactation on aromatase, estrogen, and androgen receptors expression in rat testis at weaning. J Endocrinol 192:301-311.
43. Teodoro WR, Witzel SS, Velosa AP, Shimokomaki M, Abrahamsohn PA, Zorn TM. 2003. Increase of interstitial collagen in the mouse endometrium during decidualization. Connect Tissue Res 44:96-103.
44. Wang H, Masironi B, Eriksson H, Sahlin L. 1999. A comparative study of estrogen receptors alpha and beta in the rat uterus. Biol Reprod 61:955-964.
45. Zhou Y, Chorich LP, Mahesh VB, Ogle TF. 1993. Regulation of estrogen receptor protein and messenger ribonucleic acid by estradiol and progesterone in rat uterus. J Steroid Biochem Mol Biol 46:687-698.
46. Zhou Y, Shughrue PJ, Dorsa DM. 1995. Estrogen receptor protein is differentially regulated in the preoptic area of the brain and in the uterus during the rat estrous cycle. Neuroendocrinology 61:276-283.
47. Zorn TM, Bevilacqua EM, Abrahamsohn PA. 1986. Collagen remodeling during decidualization in the mouse. Cell Tissue Res 244:443-448.