Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-19T06:29:49.127Z Has data issue: false hasContentIssue false

Restricted nutrition-induced low birth weight, low number of nephrons and glomerular mesangium injury in Japanese quail

Published online by Cambridge University Press:  06 February 2017

H. Nishimura*
Affiliation:
Department of Physiology, University of Tennessee Health Science Center, Memphis, TN, USA Institute of Nephrology and Department of Physiology, Niigata University Graduate School of Medical and Dental Sciences, Niigata, Japan
E. Yaoita
Affiliation:
Institute of Nephrology and Department of Physiology, Niigata University Graduate School of Medical and Dental Sciences, Niigata, Japan
M. Nameta
Affiliation:
Institute of Nephrology and Department of Physiology, Niigata University Graduate School of Medical and Dental Sciences, Niigata, Japan
K. Yamaguchi
Affiliation:
Department of Physiology, Niigata University Graduate School of Medical and Dental Sciences, Niigata, Japan
M. Sato
Affiliation:
Department of Medicine, Kawasaki Medical School, Okayama, Japan
C. Ihoriya
Affiliation:
Department of Medicine, Kawasaki Medical School, Okayama, Japan
L. Zhao
Affiliation:
Institute of Nephrology and Department of Physiology, Niigata University Graduate School of Medical and Dental Sciences, Niigata, Japan
H. Kawachi
Affiliation:
Institute of Nephrology and Department of Physiology, Niigata University Graduate School of Medical and Dental Sciences, Niigata, Japan
T. Sasaki
Affiliation:
Department of Medicine, Kawasaki Medical School, Okayama, Japan
Y. Ikezumi
Affiliation:
Department of Pediatrics, Niigata University Graduate School of Medical and Dental Hospital, Niigata, Japan
Y. Ouchi
Affiliation:
Department of Geriatric Medicine, Graduate School of Medicine, University of Tokyo, Tokyo, Japan
N. Kashihara
Affiliation:
Department of Medicine, Kawasaki Medical School, Okayama, Japan
T. Yamamoto
Affiliation:
Institute of Nephrology and Department of Physiology, Niigata University Graduate School of Medical and Dental Sciences, Niigata, Japan
*
*Address for correspondence: Professor H. Nishimura, Department of Health Informatics, Niigata University of Health and Welfare, 1398 Shimamicho, Kitaku, Niigata City 950-3198, Japan. (Email [email protected])

Abstract

Insufficient nutrition during the perinatal period causes structural alterations in humans and experimental animals, leading to increased vulnerability to diseases in later life. Japanese quail, Coturnix japonica, in which partial (8–10%) egg white was withdrawn (EwW) from eggs before incubation had lower birth weights than controls (CTs). EwW birds also had reduced hatching rates, smaller glomeruli and lower embryo weight. In EwW embryos, the surface condensate area containing mesenchymal cells was larger, suggesting that delayed but active nephrogenesis takes place. In mature EwW quail, the number of glomeruli in the cortical region (mm2) was significantly lower (CT 34.7±1.4, EwW 21.0±1.2); capillary loops showed focal ballooning, and mesangial areas were distinctly expanded. Immunoreactive cell junction proteins, N-cadherin and podocin, and slit diaphragms were clearly seen. With aging, the mesangial area and glomerular size continued to increase and were significantly larger in EwW quail, suggesting compensatory hypertrophy. Furthermore, apoptosis measured by terminal deoxynucleotidyl transferase-mediated dUTP-biotin nick-end labeling analysis was higher in EwWs than in CTs on embryonic day 15 and postnatal day 4 (D4). Similarly, plasma glucocorticoid (corticosterone) was higher (P<0.01) on D4 in EwW quail. These results suggest that although nephrogenic activity is high in low-nutrition quail during the perinatal period, delayed development and increased apoptosis may result in a lower number of mature nephrons. Damaged or incompletely mature mesangium may trigger glomerular injury, leading in later life to nephrosclerosis. The present study shows that birds serve as a model for ‘fetal programming,’ which appears to have evolved phylogenetically early.

Type
Original Article
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1. Fowden, AL, Giussani, DA, Forhead, AJ. Intrauterine programming of physiological systems: causes and consequences. Physiology. 2006; 21, 2937.CrossRefGoogle ScholarPubMed
2. Ingelfinger, JR, Woods, LL. Perinatal programming, renal development, and adult renal function. Am J Hypertens. 2002; 15, 46S49S.Google Scholar
3. Luyckx, VA, Brenner, BM. Low birth weight, nephron number, and kidney disease. Kidney Int Suppl. 2005; 68, S68S77.Google Scholar
4. Baum, M. Role of the kidney in the prenatal and early postnatal programming of hypertension. Am J Physiol Renal Physiol. 2010; 298, F235F247.Google Scholar
5. Manning, J, Vehaskari, VM. Postnatal modulation of prenatally programmed hypertension by dietary Na and ACE inhibition. Am J Physiol Regul Integr Comp Physiol. 2005; 288, R80R84.Google Scholar
6. Moritz, KM, Dodic, M, Wintour, EM. Kidney development and the fetal programming of adult disease. BioEssays. 2003; 25, 212220.Google Scholar
7. Ojeda, NB, Grigore, D, Alexander, BT. Intrauterine growth restriction: fetal programming of hypertension and kidney disease. Adv Chronic Kidney Dis. 2008; 15, 101106.Google Scholar
8. Portha, B, Chavey, A, Movassat, J. Early-life origins of type 2 diabetes: fetal programming of the beta-cell mass. Exp Diabetes Res. 2011; article ID 105076, 16 pages.CrossRefGoogle ScholarPubMed
9. Burdge, GC, Lillycrop, KA. Nutrition, epigenetics and developmental plasticity: implications for understanding human disease. Annu Rev Nutr. 2010; 30, 315339.Google Scholar
10. Gluckman, PD, Hanson, MA, Buklijas, T, Low, FM, Beedle, AS. Epigenetic mechanisms that underpin metabolic and cardiovascular diseases. Nat Rev Endocrinol. 2009; 5, 401408.Google Scholar
11. Ikezumi, Y, Suzuki, T, Karasawa, T, et al. Low birthweight and premature birth are risk factors for podocytopenia and focal segmental glomerulosclerosis. Am J Nephrol. 2013; 38, 149157.Google Scholar
12. Prelipcean, A (Teusan), Prelipcean, AA, Teusan, V. Investigations on the structure, chemical composition and caloricity of the quail eggs, deposited at the plateau phase of the laying period. Lucrari Stiintifice Seria Zootehnie. 2014; 57, 113120.Google Scholar
13. Miwa, T, Nishimura, H. Diluting segment in avian kidney. II. Water and chloride transport. Am J Physiol Regul Integr Comp Physiol. 1986; 250, R341R347.Google Scholar
14. Nishimura, H, Koseki, C, Imai, M, Braun, EJ. Sodium chloride and water transport in the thin descending limb of Henle of the quail. Am J Physiol Renal Fluid Electrolyte Physiol. 1989; 257, F994F1002.CrossRefGoogle ScholarPubMed
15. Nishimura, H, Yang, Y, Lau, K, et al. Aquaporin-2 water channel in developing quail kidney: possible role in programming adult fluid homeostasis. Am J Physiol. 2007; 293, R2147R2158.Google Scholar
16. Kihara, I, Yaoita, E, Kawasaki, K, et al. Origin of hyperplastic epithelial cells in idiopathic collapsing glomerulopathy. Histopathology. 1999; 34, 537547.Google Scholar
17. Koda, R, Zhao, L, Yaoita, E, et al. Novel expression of claudin-5 in glomerular podocytes. Cell Tissue Res. 2011; 343, 637648.Google Scholar
18. Yaoita, E, Yao, J, Yoshida, Y, et al. Up-regulation of connexin43 in glomerular podocytes in response to injury. Am J Pathol. 2002; 161, 15971606.CrossRefGoogle ScholarPubMed
19. Nakatsue, T, Koike, H, Han, GD, et al. Nephrin and podocin dissociate at the onset of proteinuria in experimental membranous nephropathy. Kidney Int. 2005; 67, 22392254.Google Scholar
20. Yaoita, E, Nishimura, H, Nameta, M, et al. Adherens junction proteins in glomerular podocytes of quail kidney. J Histochem Cytochem. 2016; 64, 6776.Google Scholar
21. Satoh, M, Matter, CM, Ogita, H, et al. Inhibition of apoptosis-regulated signaling kinase-1 and prevention of congestive heart failure by estrogen. Circulation. 2007; 115, 31973204.Google Scholar
22. Sugiyama, H, Kashihara, N, Makino, H, Yamasaki, Y, Ota, Z. Apoptosis in glomerular sclerosis. Kidney Int. 1996; 49, 103111.Google Scholar
23. Neese, JW, Duncan, P, Bayse, D, et al. Development and evaluation of a hexokinase/glucose-6-phosphate dehydrogenase procedure for use as a national glucose reference method. HEW Publication No. (CDC) 77-8330. 1976. Center for Disease Control: Atlanta, GA.Google Scholar
24. Dupont, J, Dagou, C, Derouet, M, Simon, J, Taouis, M. Early steps of insulin receptor signaling in chicken and rat: apparent refractoriness in chicken muscle. Domest Anim Endocrinol. 2004; 26, 127142.Google Scholar
25. Nishizono, I, Iida, S, Suzuki, N, et al. Rapid and sensitive chemiluminescent enzyme immunoassay for measuring tumor markers. Clin Chem. 1991; 37, 16391644.Google Scholar
26. Davey, MG, Tickle, C. The chicken as a model for embryonic development. Cytogenet Genome Res. 2007; 117, 231239.Google Scholar
27. Barker, DJP, Eriksson, JG, Forsen, T, Osmond, C. Fetal origins of adult disease: strength of effects and biological basis. Int J Epidemiol. 2002; 31, 12351239.CrossRefGoogle ScholarPubMed
28. Barker, DJ, Winter, PD, Osmond, C, Margetts, B, Simmonds, SJ. Weight in infancy and death from ischaemic heart disease. Lancet. 1989; 2, 577580.Google Scholar
29. Lau, C, Rogers, JM. Embryonic and fetal programming of physiological disorders in adulthood. Birth Defects Res C Embryo Today. 2004; 72, 300312.Google Scholar
30. Taylor, PD, Poston, L. Developmental programming of obesity in mammals. Exp Physiol. 2007; 92.2, 287298.Google Scholar
31. Coupe’, B, Grit, I, Darmaun, D, Parnet, P. The timing of ‘catch-up growth’ affects metabolism and appetite regulation in male rats born with intrauterine growth restriction. Am J Physiol Regul Integr Comp Physiol. 2009; 297, R813R824.Google Scholar
32. Alexander, B, Dasinger, JH, Intapad, S. Fetal programming and cardiovascular pathology. Comp Physiol. 2015; 5, 9971025.CrossRefGoogle ScholarPubMed
33. Wu, G, Bazer, FW, Cudd, TA, Meininger, CJ, Spencer, TE. Maternal nutrition and fetal development. J Nutr. 2004; 134, 21692172.Google Scholar
34. Awazu, M, Hida, M. Maternal nutrient restriction inhibits ureteric bud branching but does not affect the duration of nephrogenesis in rats. Pediatr Res. 2015; 77, 633639.Google Scholar
35. Ibáñez, L, Suárez, L, Lopez-Bermejo, A, et al. Early development of visceral fat excess after spontaneous catch-up growth in children with low birth weight. J Clin Endocrinol Metab. 2008; 93, 925928.Google Scholar
36. Sakai, T, Kriz, W. The structural relationship between mesangial cells and basement membrane of the renal glomerulus. Anat Embryol. 1987; 176, 373386.Google Scholar
37. Sakai, T, Lemley, KV, Hackenthal, E, et al. Changes in glomerular structure following acute mesangial failure in the isolated perfused kidney. Kidney Int. 1992; 41, 533541.Google Scholar
38. Nishimura, H, Xi, Z, Zhang, L, et al. Maturation dependent neointima formation in fowl aorta. Comp Biochem Physiol A Mol Integr Physiol. 2001; 30, 3954.Google Scholar
39. Sugizawa, Y. Mesangial injury associated with renal lymph stasis and blood congestion. Nihon Jinzo Gakkai Shi. 1987; 29, 3949.Google Scholar
40. Romano, LA, Ferder, L, Inserra, F, et al. Intraglomerular expression of alpha-smooth muscle actin in aging mice. Hypertension. 1994; 23(Pt 2), 889893.Google Scholar
41. Kriz, W, Lemley, KV. A potential role for mechanical forces in the detachment of podocytes and the progression of CKD. J Am Soc Nephrol. 2015; 26, 258269.Google Scholar
42. Miner, JH. Life without nephrin: It’s for the birds. J Am Soc Nephrol. 2012; 23, 369371.Google Scholar
43. Thornburg, KL, O’Tierney, PF, Louey, S. The placenta is a programming agent for cardiovascular disease. Placenta. 2010; 31, S54S59.Google Scholar
44. Ingelfinger, JR, Schnaper, HW. Renal endowment: developmental origins of adult disease. J Am Soc Nephrol. 2005; 16, 25332536.Google Scholar
45. Moisiadis, VG, Matthews, SG. Glucocorticoids and fetal programming part 1: outcomes. Nat Rev Endocrinol. 2014a; 10, 391402.Google Scholar
46. Moisiadis, VG, Matthews, SG. Glucocorticoids and fetal programming part 2: mechanisms. Nat Rev Endocrinol. 2014b; 10, 403411.Google Scholar
47. Kapoor, A, Dunn, E, Kostaki, A, Andrews, MH, Matthews, SG. Fetal programming of hypothalamo-pituitary-adrenal function: prenatal stress and glucocorticoids. J Physiol. 2006; 572, 3144.CrossRefGoogle ScholarPubMed
48. Weinstock, M. The potential influence of maternal stress hormone on development and mental health of the offspring. Brain Behav Immun. 2005; 19, 296308.Google Scholar
49. Braun, EJ, Sweazea, KL. Glucose regulation in birds. Comp Biochem Physiol B Biochem Mol Biol. 2008; 151, 19.Google Scholar
50. Srivastava, T. Nondiabetic consequences of obesity on kidney. Pediatr Nephrol. 2006; 21, 463470.Google Scholar
51. Kriz, W, Schiller, A, Kaissling, B, Taugner, R. Comparative and functional aspects of thin loop limb ultrastructure. In Functional Ultrastructure of the Kidney (eds. Maunsbach AB, Olsen TS, Christensen EI), 1980; pp. 241–250. Academic Press, New York.Google Scholar
52. Bailey, JR, Nishimura, H. Renal response of fowl to hypertonic saline infusion into the renal portal system. Am J Physiol. 1984; 246, R624R632.Google Scholar