Postnatal Leptin Promotes Organ Maturation and Development in IUGR Piglets

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Attig, Linda ^a   Brisard, Daphné ^b,c,d,e   Larcher, Thibaut ^f   Mickiewicz, Michal ^g   Guilloteau, Paul ^g   Boukthir, Samir ^h   Niamba, Claude Narcisse ^a   Gertler, Arieh ⁱ   Djiane, Jean ^g   Monniaux, Danielle ^b,c,d,e   Abdennebi Najar, Latifa ^a  

^a INSTITUT POLYTECHNIQUE LASALLE BEAUVAIS   (France)

^b UMR85 PHYSIOLOGIE DE LA REPRODUCTION ET DES COMPORTEMENTS   (France)

^c CNRS   (France)

^d UNIVERSITÉ DE TOURS   (France)

^e IFCE   (France)

^f INRA UMR 703   (France)

^g CEMAGREF   (France)

^h UNIVERSITY OF TUNIS EL MANAR   (Tunisia)

ⁱ HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

CD79 ANTIGEN; CHOLESTEROL; GLUCOSE; RECOMBINANT LEPTIN; SODIUM CHLORIDE; TRANSCRIPTION FACTOR FKHRL1; TRIACYLGLYCEROL; TRYPSIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; DRUG EFFECT; ENZYME ACTIVITY; FEMALE; GERM CELL; IN VIVO STUDY; INTRAUTERINE GROWTH RETARDATION; KIDNEY MASS; LIVER WEIGHT; LYMPHOID ORGAN; NONHUMAN; OOCYTE; ORGANOGENESIS; OVARY; OVARY FOLLICLE MATURATION; PANCREAS; PERINATAL PERIOD; PEYER PATCH; PIGLET; SMALL INTESTINE; SPLEEN WEIGHT; WEIGHT GAIN;

ANIMALS; ANIMALS, NEWBORN; ANTIGENS, CD79; FEMALE; FETAL GROWTH RETARDATION; FETUS; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GONADS; HUMANS; IMMUNE SYSTEM; INFANT, NEWBORN; INJECTIONS, INTRAMUSCULAR; LEPTIN; LIVER; MALE; ORGAN SIZE; ORGANOGENESIS; PANCREAS; SWINE;

EID: 84878588009     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0064616     Document Type: Article

References (71)

1. Pallotto EK, Kilbride HW, (2006) Perinatal outcome and later implications of intrauterine growth restriction. Clin Obstet Gynecol 49: 257-269.
2. Boehm G, Bierbach U, Senger H, Jakobsson I, Minoli I, et al. (1990) Postnatal adaptation of lipase- and trypsin-activities in duodenal juice of premature infants appropriate for gestational age. Biomed Biochim Acta 49: 369-373.
3. Xanthou M, (1985) Immunologic deficiencies in small-for-dates neonates. Acta Paediatr Scand 185suppl 319: 143-149.
4. de Bruin JP, Dorland M, Bruinse HW, Spliet W, Nikkels PG, et al. (1998) Fetal growth retardation as a cause of impaired ovarian development. Early Hum Dev 51: 39-46.
5. Ibanez L, de Zegher F, (2006) Puberty after prenatal growth restraint. Horm Res 65Suppl 3: 112-115.
6. Hales CN (1997) Metabolic consequences of intrauterine growth retardation. Acta Paediatr Suppl 423: 184-187; discussion 188.
7. Albertsson-Wikland K, Boguszewski M, Karlberg J, (1998) Children born small-for-gestational age: postnatal growth and hormonal status. Horm Res 49: 7-13.
8. Fattal-Valevski A, Toledano-Alhadef H, Golander A, Leitner Y, Harel S, (2005) Endocrine profile of children with intrauterine growth retardation. J Pediatr Endocrinol Metab 18: 671-676.
9. Kilby MD, Verhaeg J, Gittoes N, Somerset DA, Clark PM, et al. (1998) Circulating thyroid hormone concentrations and placental thyroid hormone receptor expression in normal human pregnancy and pregnancy complicated by intrauterine growth restriction (IUGR). J Clin Endocrinol Metab 83: 2964-2971.
10. Djiane J, Attig L, (2008) Role of leptin during perinatal metabolic programming and obesity. J Physiol Pharmacol 59Suppl 1: 55-63.
11. Jaquet D, Leger J, Levy-Marchal C, Oury JF, Czernichow P, (1998) Ontogeny of leptin in human fetuses and newborns: effect of intrauterine growth retardation on serum leptin concentrations. J Clin Endocrinol Metab 83: 1243-1246.
12. Gautron L, Elmquist JK, (2011) Sixteen years and counting: an update on leptin in energy balance. J Clin Invest 121: 2087-2093.
13. Attig L, Djiane J, Gertler A, Rampin O, Larcher T, et al. (2008) Study of hypothalamic leptin receptor expression in low-birth-weight piglets and effects of leptin supplementation on neonatal growth and development. Am J Physiol Endocrinol Metab 295: E1117-1125.
14. Vickers MH, Gluckman PD, Coveny AH, Hofman PL, Cutfield WS, et al. (2005) Neonatal leptin treatment reverses developmental programming. Endocrinology 146: 4211-4216.
15. Margetic S, Gazzola C, Pegg GG, Hill RA, (2002) Leptin: a review of its peripheral actions and interactions. Int J Obes Relat Metab Disord 26: 1407-1433.
16. Proulx K, Richard D, Walker CD, (2002) Leptin regulates appetite-related neuropeptides in the hypothalamus of developing rats without affecting food intake. Endocrinology 143: 4683-4692.
17. Ahima RS, Prabakaran D, Flier JS, (1998) Postnatal leptin surge and regulation of circadian rhythm of leptin by feeding. Implications for energy homeostasis and neuroendocrine function. J Clin Invest 101: 1020-1027.
18. Bouret SG, (2010) Neurodevelopmental actions of leptin. Brain Res 1350: 2-9.
19. Attig L, Larcher T, Gertler A, Abdennebi-Najar L, Djiane J, (2011) Postnatal leptin is necessary for maturation of numerous organs in newborn rats. Organogenesis 7: 88-94.
20. Poore KR, Forhead AJ, Gardner DS, Giussani DA, Fowden AL, (2002) The effects of birth weight on basal cardiovascular function in pigs at 3 months of age. J Physiol 539: 969-978.
21. Poore KR, Fowden AL, (2002) The effect of birth weight on glucose tolerance in pigs at 3 and 12 months of age. Diabetologia 45: 1247-1254.
22. Poore KR, Fowden AL, (2004) The effects of birth weight and postnatal growth patterns on fat depth and plasma leptin concentrations in juvenile and adult pigs. J Physiol 558: 295-304.
23. Litten JC, Mostyn A, Perkins KS, Corson AM, Symonds ME, et al. (2005) Effect of administration of recombinant human leptin during the neonatal period on the plasma concentration and gene expression of leptin in the piglet. Biol Neonate 87: 1-7.
24. Raver N, Gussakovsky EE, Keisler DH, Krishna R, Mistry J, et al. (2000) Preparation of recombinant bovine, porcine, and porcine W4R/R5K leptins and comparison of their activity and immunoreactivity with ovine, chicken, and human leptins. Protein Expr Purif 19: 30-40.
25. Bernfeld P, (1955) Amylase α and ß. Methods Enzymol 1: 149-155.
26. Laine J, Beattie M, LeBel D, (1993) Simultaneous kinetic determinations of lipase, chymotrypsin, trypsin, elastase, and amylase on the same microtiter plate. Pancreas 8: 383-386.
27. Maroux S, Louvard D, Baratti J, (1973) The aminopeptidase from hog intestinal brush border. Biochim Biophys Acta 321: 282-295.
28. Aquila S, Rago V, Guido C, Casaburi I, Zupo S, et al. (2008) Leptin and leptin receptor in pig spermatozoa: evidence of their involvement in sperm capacitation and survival. Reproduction 136: 23-32.
29. Rosenberg A, (2008) The IUGR newborn. Semin Perinatol 32: 219-224.
30. Hinchliffe SA, Lynch MR, Sargent PH, Howard CV, Van Velzen D, (1992) The effect of intrauterine growth retardation on the development of renal nephrons. Br J Obstet Gynaecol 99: 296-301.
31. Kolacek S, Puntis JW, Lloyd DR, Brown GA, Booth IW, (1990) Ontogeny of pancreatic exocrine function. Arch Dis Child 65: 178-181.
32. Shanklin DR, Cooke RJ, (1993) Effects of intrauterine growth on intestinal length in the human fetus. Biol Neonate 64: 76-81.
33. Mickiewicz M, Zabielski R, Grenier B, Le Normand L, Savary G, et al. (2012) Structural and functional development of small intestine in intrauterine growth retarded porcine offspring born to gilts fed diets with differing protein ratios throughout pregnancy. J Physiol Pharmacol 63: 225-239.
34. Abdennebi-Najar L, Desai M, Han G, Casillas E, Jean D, et al. (2011) Basal, endogenous leptin is metabolically active in newborn rat pups. J Matern Fetal Neonatal Med 24: 1486-1491.
35. Ramsay TG, Richards MP, (2005) Leptin and leptin receptor expression in skeletal muscle and adipose tissue in response to in vivo porcine somatotropin treatment. J Anim Sci 83: 2501-2508.
36. Tannenbaum GS, Gurd W, Lapointe M, (1998) Leptin is a potent stimulator of spontaneous pulsatile growth hormone (GH) secretion and the GH response to GH-releasing hormone. Endocrinology 139: 3871-3875.
37. Hoggard N, Hunter L, Duncan JS, Williams LM, Trayhurn P, et al. (1997) Leptin and leptin receptor mRNA and protein expression in the murine fetus and placenta. Proc Natl Acad Sci U S A 94: 11073-11078.
38. Guilloteau P, Zabielski R, Hammon HM, Metges CC, (2010) Nutritional programming of gastrointestinal tract development. Is the pig a good model for man? Nutr Res Rev 23: 4-22.
39. Rothkotter HJ, (2009) Anatomical particularities of the porcine immune system-a physician's view. Dev Comp Immunol 33: 267-272.
40. Pierzynowski SG, Westrom BR, Erlanson-Albertsson C, Ahre'n B, Svendsen J, et al. (1993) Induction of exocrine pancreas maturation at weaning in young developing pigs. J Pediatr Gastroenterol Nutr 16: 287-293.
41. Schnapper A, Uhr G, Meyer W, (2003) Growth kinetics of porcine lymphatic organs during early postnatal life. Anat Histol Embryol 32: 297-304.
42. Da Silva-Buttkus P, van den Hurk R, te Velde ER, Taverne MA, (2003) Ovarian development in intrauterine growth-retarded and normally developed piglets originating from the same litter. Reproduction 126: 249-258.
43. McGee EA, Hsueh AJ, (2000) Initial and cyclic recruitment of ovarian follicles. Endocr Rev 21: 200-214.
44. Oxender WD, Colenbrander B, van deWiel DF, Wensing CJ, (1979) Ovarian development in fetal and prepubertal pigs. Biol Reprod 21: 715-721.
45. Abir R, Ao A, Jin S, Barnett M, Raanani H, et al. (2005) Leptin and its receptors in human fetal and adult ovaries. Fertil Steril 84: 1779-1782.
46. Cioffi JA, Van Blerkom J, Antczak M, Shafer A, Wittmer S, et al. (1997) The expression of leptin and its receptors in pre-ovulatory human follicles. Mol Hum Reprod 3: 467-472.
47. Craig J, Zhu H, Dyce PW, Petrik J, Li J, (2004) Leptin enhances oocyte nuclear and cytoplasmic maturation via the mitogen-activated protein kinase pathway. Endocrinology 145: 5355-5363.
48. Ryan NK, Woodhouse CM, Van der Hoek KH, Gilchrist RB, Armstrong DT, et al. (2002) Expression of leptin and its receptor in the murine ovary: possible role in the regulation of oocyte maturation. Biol Reprod 66: 1548-1554.
49. Joo JK, Joo BS, Kim SC, Choi JR, Park SH, et al. (2010) Role of leptin in improvement of oocyte quality by regulation of ovarian angiogenesis. Animal reproduction science 119: 329-334.
50. Fruhbeck G, (2006) Intracellular signalling pathways activated by leptin. Biochem J 393 (Pt 1): 7-20.
51. Ye Y, Kawamura K, Sasaki M, Kawamura N, Groenen P, et al. (2009) Leptin and ObRa/MEK signalling in mouse oocyte maturation and preimplantation embryo development. Reproductive biomedicine online 19: 181-190.
52. Fan HY, Sun QY, (2004) Involvement of mitogen-activated protein kinase cascade during oocyte maturation and fertilization in mammals. Biology of reproduction 70: 535-547.
53. Cirillo D, Rachiglio AM, la Montagna R, Giordano A, Normanno N, (2008) Leptin signaling in breast cancer: an overview. J Cell Biochem 105: 956-964.
54. Huang XF, Chen JZ, (2009) Obesity, the PI3K/Akt signal pathway and colon cancer. Obes Rev 10: 610-616.
55. Uddin S, Hussain AR, Siraj AK, Khan OS, Bavi PP, et al. (2011) Role of leptin and its receptors in the pathogenesis of thyroid cancer. Int J Clin Exp Pathol 4: 637-643.
56. Wang D, Chen J, Chen H, Duan Z, Xu Q,et al. Leptin regulates proliferation and apoptosis of colorectal carcinoma through PI3K/Akt/mTOR signalling pathway. J Biosci 37: 91-101.
57. Adhikari D, Liu K, (2009) Molecular mechanisms underlying the activation of mammalian primordial follicles. Endocrine reviews 30: 438-464.
58. Castrillon DH, Miao L, Kollipara R, Horner JW, DePinho RA, (2003) Suppression of ovarian follicle activation in mice by the transcription factor Foxo3a. Science 301: 215-218.
59. John GB, Gallardo TD, Shirley LJ, Castrillon DH, (2008) Foxo3 is a PI3K-dependent molecular switch controlling the initiation of oocyte growth. Dev Biol 321: 197-204.
60. Reddy P, Zheng W, Liu K, (2010) Mechanisms maintaining the dormancy and survival of mammalian primordial follicles. Trends Endocrinol Metab 21: 96-103.
61. Ding W, Wang W, Zhou B, Zhang W, Huang P, et al. (2010) Formation of primordial follicles and immunolocalization of PTEN, PKB and FOXO3A proteins in the ovaries of fetal and neonatal pigs. J Reprod Dev 56: 162-168.
62. Xu RJ, Mellor DJ, Tungthanathanich P, Birtles MJ, Reynolds GW, et al. (1992) Growth and morphological changes in the small and the large intestine in piglets during the first three days after birth. J Dev Physiol 18: 161-172.
63. Boehm G, Bierbach U, Senger H, Jakobsson I, Minoli I, et al. (1991) Activities of lipase and trypsin in duodenal juice of infants small for gestational age. J Pediatr Gastroenterol Nutr 12: 324-327.
64. Bernstein IM, Horbar JD, Badger GJ, Ohlsson A, Golan A, (2000) Morbidity and mortality among very-low-birth-weight neonates with intrauterine growth restriction. The Vermont Oxford Network. Am J Obstet Gynecol 182: 198-206.
65. Wolinski J, Biernat M, Guilloteau P, Westrom BR, Zabielski R, (2003) Exogenous leptin controls the development of the small intestine in neonatal piglets. J Endocrinol 177: 215-222.
66. Bock T, Kyhnel A, Pakkenberg B, Buschard K, (2003) The postnatal growth of the beta-cell mass in pigs. J Endocrinol 179: 245-252.
67. Petrik J, Reusens B, Arany E, Remacle C, Coelho C, et al. (1999) A low protein diet alters the balance of islet cell replication and apoptosis in the fetal and neonatal rat and is associated with a reduced pancreatic expression of insulin-like growth factor-II. Endocrinology 140: 4861-4873.
68. Ruddle NH, Akirav EM, (2009) Secondary lymphoid organs: responding to genetic and environmental cues in ontogeny and the immune response. J Immunol 183: 2205-2212.
69. Rothkotter HJ, Pabst R, (1989) Lymphocyte subsets in jejunal and ileal Peyer's patches of normal and gnotobiotic minipigs. Immunology 67: 103-108.
70. Singh M, Manerikar S, Malaviya AN, Premawathi, Gopalan R, et al. (1978) Immune status of low birth weight babies. Indian Pediatr 15: 563-567.
71. Fantuzzi G, Faggioni R, (2000) Leptin in the regulation of immunity, inflammation, and hematopoiesis. J Leukoc Biol 68: 437-446.